Open access peer-reviewed chapter
Abstract
Malignant melanoma is the sixth most commonly diagnosed cancer in developed countries. Like in many cancers, survival rates are closely associated with the time of melanoma detection. Regrettably, most cases of melanoma are caught at diffuse state and methods used in clinical practice and experimental trials are not effective. Thus, there is a great interest in discovering biomarkers that could be used for screening those with melanoma, as prognostic and prediction factors as well as new potential targets for melanoma treatment. For this purpose, many groups have examined alteration in the structure and expression of carbohydrate part of glycoconjugates to identify changes that occur with melanoma. The observed changes include increased β1,6 branching correlating with higher abundance of polylactosamine extension, increased sialylation accompanied by differences in the position of sialic acid residues, increased fucosylation, higher levels of T and Tn antigens as well as changes in the expression of ganglioside structures. As a consequence of glycan modification, the loosened matrix adhesion, increased motility, higher invasive potential and metastasis formation have been observed. Growth and migration of melanoma cells have been also found to be stimulated by advanced glycation end products. Biomarker discovery is a multi-step process and the recent glycomic data on melanoma are mostly related to the discovery phase, as the first one leading to validation and standardisation steps.
Keywords
- glycosylation
- glycation
- malignant melanoma
- tumour-associated carbohydrate antigens
1. Introduction
The population of patients with cutaneous melanoma is one of the most rapidly increasing cancer groups worldwide over the last 50 years in most fair-skinned populations [1, 2]. The vast majority of cases (almost 85%) occur in developed countries, where melanoma is the sixth most commonly diagnosed cancer. Despite the improvements in the diagnosis thereof, the best chance of melanoma recovery remains the surgical removal of a thin early-stage lesion, because methods used on large scale in clinical practices as well as experimental trials are not able to cure this type of cancer at diffuse state [3, 4]. Palliative treatment for inoperable recurrence or metastatic disease is frequently toxic and ineffective. Thus, appropriate means for predicting prognosis or effective treatments are still needed.
Understanding the biology of tumour cells is an important factor for the development of new strategies for cancer treatment. Unfortunately, reliable biomarkers are not available for the vast majority of cancers. Macro-molecules present at the cell membrane surface and in the membranes themselves constitute an important field for study in the understanding of cancer cell behaviour. Nowadays, investigation on structural properties and function of cancer-associated glycosylation changes, as indicators of tumourigenesis, is gaining more attention in order to discover new markers suitable for early detection, for differentiating between benign and malignant stages and for therapeutic purposes. For a long time carbohydrates have been merely regarded as an integral structural component of glycoconjugates (glycoproteins, glycolipids and proteoglycans) and a storage material. Although they are ubiquitous constituents of almost all living organisms, glycoconjugates were believed to be deprived of any biological function. Progress in glycoconjugates research due to application of new powerful tools has enabled researches to discover the broad range of biological activities in which carbohydrates are involved [5–8]. Glycoconjugates participate in several processes, including protein conformational stability, protection from proteolytic degradation, protein thermal stability, biological activity, protein targeting, circulating life-time and their ultimate fate, immunogenicity, the transduction of information between cells, sperm-egg interactions, leukocyte traffic to sites of inflammation, leukocyte migration (homing) to lymphoid organs, blood clotting, apoptosis and host-pathogen interactions. Moreover, changes in glycoconjugates have been proved to be associated with a number of pathological processes, for example, carbohydrate deficiency diseases, inflammation, allergy, rheumatoid arthritis, thrombosis, infarction, diabetes and cancer [7, 9–12]. The aim of this chapter is to highlight the contribution of the defined tumour-associated carbohydrate antigens present on the cell surface of melanoma cells to their behaviour during tumour progression and metastasis, as well as to present glycomic opportunities in defining markers for melanoma early detection, disease progression or predicting therapy outcome that might help to defeat one of the deadliest forms of cancer.
2. Glycoconjugates and cancer
Glycosylation is the most frequent post-translational modification of macro-molecules. Carbohydrate part (glycan) biosynthesis involves various types of glycosyltransferases, glycosidases and sugar nucleotides [8, 13]. As glycosylation is not template-driven, but is indirectly controlled by a number of genes (1–2% of translated genome) and the environmental factors integrate at the level of glycan biosynthesis, the relative amounts and structure of glycans is cell-, tissue- and species-dependent [14]. The biosynthetic basis of such diversity consists in the alteration in the activity of various glycosyltransferases and competition between enzymes for acceptor intermediates during glycan elongation. Additionally, in cancer cells the activity of glycosyltransferases and glycosidases is controlled by other factors such as the levels of nucleotide sugars and their transporters, the expression of chaperons that regulate protein folding and quality control of proteins, endogenous lectin as well as by altered expression of the enzymes engaged in biosynthetic process together with their proper localisation [15]. Recently, it has been shown that the aberrant expression of glyco-genes in cancer is also due to aberrant promotor methylation. In melanoma a difference in methylation of 20 genes involved in O-glycosylation has been stated [16]. These results suggest new potential targets for melanoma treatment, and indicate that the methylation status of selected glyco-genes might be used for prognostic purposes.
The hallmarks of all types of human, as well as experimental rodent cancers include profound changes in the structure and expression of carbohydrate part of glycoconjugates, resulting from activation of particular oncogenes or rearrangements of glycan biosynthetic pathways [1, 11, 12, 17]. Generally, cancer-associated changes in glycosylation profile are associated either with the expression and secretion of inappropriate glycosylated molecules or the appearance of new antigens (onco-foetal or
Protein-carbohydrate interactions have not only biological but also medical implication, since glycosylation profile is dynamically modified by many intra- and/or extra-cellular stimuli. Additionally, these interactions are involved in the control of cell homeostasis and its social behaviour. Therefore, alterations in carbohydrate structures of glycoconjugates including cell adhesion molecules, commonly found in various tumours, are considered to be the basis for abnormal social behaviour of tumour cells, such as invasion to the surrounding tissue and metastasis, loose of cell-cell contact and epithelial-mesenchymal transition (EMT) [15, 18, 28–34]. These macro-molecules could also significantly change antigenicity and immunogenicity of tumour cells and therefore promote tumour progression by chronic inflammation and angiogenesis [24].
3. Glycosylation and melanoma
Over 5000 cell lines are currently available for studying cutaneous and ocular melanoma, which covers different stages of the disease progression from primary melanomas to metastases in distinct organs [35]. The most frequently used model to study the linkage between glycosylation and metastatic behaviour of melanoma cells is B16 murine melanoma cell line and its sub-lines of a different metastatic potential. Detailed analysis of B16 sub-lines with high- and low-metastatic potentials has revealed that although these sub-lines expressed comparable amount of sialic acids, α2,3-linked sialic acids were predominantly found in high-metastatic sub-line, while α2,6-linked sialic acids were observed in low-metastatic sub-line [36]. Other studies performed on a poorly metastasising wheat germ agglutinin-resistant mutants of B16 melanoma cells have proved that the variant cell line displayed well-defined changes in its cell surface glycosylation profile in comparison to wild-type cells, involving the decrease in the number of side chains in oligosaccharides, the loss of sialic acids α2,3-linked to galactose, concomitant with the increase in the amount of fucose α1,3-linked to N-acetylglucosamine [37]. Such cells were less adherent to extracellular matrix components and showed decreased metastatic potential. The observed effects resulted from a 60-fold increase in α1,3-fucosyltransferase activity, while sialyltransferase activity did not decrease significantly [38]. Participation of sialic acids in metastasis formation has been also demonstrated by transfection of murine B16, JB/RH and JB/MS cells with gene for α1,3-galactosyltransferase (α1,3GT). α1,3GT competes with α2,3-sialyltransferase and α2,6-sialyltransferase for the same acceptor, i.e. N-acetyllactosamine moieties (Figure 1) [39]. The transfected cells showed reduced metastasis formation which was caused by the reduction of cell membrane sialylation. Similar great reduction of metastatic capacity has been observed after the use of swainsonine (SW), a competitive inhibitor of Golgi α-mannosidase II which stops N-oligosaccharide synthesis on hybrid and high-mannose-type structures preventing the synthesis of complex-type structures (Figure 1) [40]. It has also been demonstrated that the loss of sialylated lactosamine antenae and decreased branching of N-oligosaccharides on B16-F10 melanoma cells (cells of high incidence of lung colonisation) reduced their pulmonary colonisation when the cells were injected into the circulation of syngeneic mice [41]. This was consistent with the observation that SW treatment of athymic nude mice bearing human MeWo cells significantly reduced solid tumour growth and inhibited tumour cell proliferation both
Figure 1.
Structures and synthetic pathway of N-oligosaccharides.
β1,6-Branched N-oligosaccharides are tri- and tetra-antennary complex-type N-glycans formed due to the action of N-acetylglucosaminyltransferase V (GnT-V), which catalyses the transfer of GlcNAc from UDP-GlcNAc to the 6-OH position of α-Man residue in α6 arm (Figure 1). In malignant transformation, the increased β1,6-branching is a result of enhanced activity of GnT-V associated with the increased expression of GnT-V gene (i.e.
β1,6-Branched N-oligosaccharides have been shown not to be synthesised by melanocytes or by cells of early melanoma
It is well documented in the literature that elevated level of β1,6-branched N-oligosaccharides correlates with higher invasive potential, metastasis formation, reconstruction of the vascular system and growth of tumour cells [48]. Additionally, the loosened matrix adhesion of tumour cells may allow them to leave their original site in the tissue [62–64]. It is still a subject to identify glycoproteins bearing these structures. It is evident from the studies of our group that the expression level of β1,6-branched N-oligosaccharides is associated with acquisition of the metastatic potential in melanoma, and of particular interest are glycoproteins with the apparent molecular weight of 100–160 kDa [57]. We identified target glycoproteins of GnT-V from four human melanoma cell lines (WM35, WM9, WM239 and A375) by tandem mass spectrometry [48, 65]. Among the identified proteins, the largest group comprised integrin subunits (α2, α3, α4, α5, αv, β1 and β3). Additionally, N-cadherin, L1CAM, Mac-2 binding protein (Mac-2-BP), lysosome-associated membrane protein 1 (LAMP-1), CD44, melanoma-associated antigen (MAA), melanoma cell adhesion molecule (CD146, Mel-CAM), intracellular adhesion molecule 1 (CD54, ICAM-1), tumour rejection antigen-1 and melanoma-associated chondroitin sulphate proteoglycan 4 were found. The number of proteins being a substrate for GnT-V seemed to be better correlated with melanoma development and progression than with the expression of these cell adhesion molecules on melanoma cell surface. Independently of melanoma progression, αv and β1 integrin subunits as well as LAMP-1, CD146, CD54 and Mac-2-BP were always substrates for GnT-V; α3, α5 and β3 integrin subunits possessed no β1,6-branched N-oligosaccharides in WM35 cell line, being a radial growth phase primary melanoma, whereas α4 integrin subunit, CD44 and N-cadherin appeared to have these structures only in A375 cell line, which was the most aggressive melanoma cell line among the studied ones. It is well documented in the literature that the patterns of cell adhesion molecules differ between normal and malignant tissues. In cutaneous melanoma, the expression levels of α2β1, α3β1, α6β1 and αvβ3 integrins have been found to be associated with tumour progression. We demonstrated that not only gain or loss of adhesion molecule expression and increased level of β1,6-branched N-oligosaccharides, but also changes in the number of proteins being a substrate for GnT-V appear to be a consequence of disease progression from a tumourigenic to the metastatic phenotype. The involvement of these glycoproteins in adhesion and migration of cutaneous melanoma cells has been clearly demonstrated [60, 62, 63, 66–71]. In general, overexpression of β1,6-branched N-glycans on cell adhesion molecules contributed to the significant decrease in these cell adhesion level to extracellular matrix components, loss of contact inhibition as well as increased motility
Contrary results regarding the role of β1,6-branched N-glycans were obtained when glycosylation analysis was performed on tissues isolated from patients. Studies carried out on sections of 100 primary cutaneous malignant melanoma histochemically stained with five lectins (
It has also been shown that B16 melanoma cells exhibited a fivefold higher cell surface β1,4-galactosyltransferase activity in metastatic variants than their non-metastatic counterparts [78]. This enzyme catalyses the transfer of galactose residue to terminal N-acetylglucosamine residues on the cell surface glycolipid glucosylceramide (Figure 2), which is a precursor of glycosphingolipids. Glycosphingolipids which possess at least one sialic acid residue constitute a broad family of molecules called gangliosides. It has been shown that gangliosides are expressed with higher abundance in tumour cells in comparison to their normal counterparts. In normal melanocytes GM3 are expressed as their major gangliosides, whereas GM3 and GD3 are synthesised predominantly in malignant melanomas [79, 80]. A few melanomas frequently synthesise small amounts of more complex gangliosides, i.e. GM2 and GD2. In human melanomas the level of GD2 expression has been found to be associated with tumour progression and metastatic potential [81].
Figure 2.
Structures and synthetic pathway of major gangliosides.
Ganglioside expression on individual cell lines is regulated by the availability of a precursor, the expression level of β1,4-N-acetylgalactosaminyltransferase, α2,8-sialyltransferase activity and the compartmentation of the glycosylation machinery of a cell [80, 82]. Total ganglioside level has been shown to be a potential tool for evaluating the response to immunotherapy in melanoma patients [83, 84]. Furthermore, GM3 and GD3 shed by tumour cell into the micro-environment enhance tumour formation and are able to promote severe immune dysfunction [85–87]. At present, a number of gangliosides are considered to be attractive targets for cancer immunotherapy. GM3 is the precursor of the ganglioside family members that contain either N-glycolylneuraminic acid (Neu5Gc) or N-acetylneuraminic acid (Neu5Ac). The presence of Neu5Gc is a result of the expression of cytidine monophospho-N-acetylneuraminic acid hydrolase [88]. Although Neu5Gc-containing gangliosides are not self-antigens in humans [89], they have been described as tumour antigens in several human cancers including melanoma, lung and breast cancer [90–92]. The presence of Neu5GcGM3 on the cell membrane has been shown to promote cell proliferation and adhesion
One of the important basic features of melanoma cells is the property to change their adhesive interactions with other cells (keratinocytes, fibroblasts, endothelial and immune cells) and extracellular matrix protein. This property is a key element in the acquisition of the potential to detach from their original site of tumour growth, invade surrounding tissues and, finally, metastasise. These interactions are mediated by cell adhesion molecules belonging to integrins, cadherins as well as immunoglobulin (Ig) superfamily. Changes in the expression and/or function of integrins, cadherins, CD44, Mel-CAM/MUC18 and intercellular adhesion molecule -1 have been documented in the progression of primary melanoma [100, 101]. It is also well documented in the literature that changes in cell adhesion molecules and growth factor receptors as a consequence of their oligosaccharide modification are associated with the function and biological behaviour of cancer cells. In the case of the cell surface receptors, the changed glycosylation pattern may affect their conformational stability, binding ability as well as their presence in the cell membrane. Details on changes in glycosylation patterns of cadherins and integrins that can modify the adhesive properties of melanoma cells are presented in two other chapters of this book.
The function of CD44, a widely distributed membrane glycoprotein belonging to the Ig superfamily, which abnormal expression on tumour cells enhances the ability to grow and metastasise
It is well known that cancer metastases show organ selectivity and one of the important factors that determines the selectivity is the affinity of tumour cells towards the cells of an organ involved in metastasis. Most of the cell lines expressing β1,6-branched N-glycans have been shown to metastasise either to the liver or to the lung. β1,6-branched N-glycans are the preferred intermediate for the extension with polylactosamine chains (i.e. Galβ1,4GlcNAc β1,3- repeating units of 2 to more than 10 in length). Polylactosamine chains can be capped with various sequences, including Lewis antigens, sialic acids and fucose residues. It has been shown that lysosomal-associated membrane protein 1 (LAMP-1) present on the cell surface of high-metastatic murine B16-F10 cells was a carrier of a very high level of β1,6-branched N-glycans substituted with polylactosamine chains [105]. These structures were proved to be the key determinants in B16-F10 cells for preferred metastasising to the lungs, and organ-specific adhesion and metastasis was mediated via galectin-3 expressed in the highest amount on the lung vascular endothelium [105, 109, 110]. Complexes of galectin-3 with β1,6-branched N-glycans substituted with polylactosamine facilitated not only the initial arrest, but also took part in all the subsequent steps of extravasation and organ colonisation. Lung colonisation may also be realised by E-selectin-mediated interaction, but B16-F10 cells did not appear to use this molecule. B16-F10 cells transfected with cDNA encoding both α1,3- and α1,4-fucosyltransferases that catalyse reactions leading to the synthesis of sialyl-Lewis X and sialyl-Lewis A antigens, respectively, were not able to form metastasis in the liver in C57BL/6 mice, but formed numerous liver metastasis in E-selectin transgenic mice [111]. This means that sialyl-Lewis X (SAα2,3Galβ1,4(Fucα1,3)GlcNAcβ-) antigens on β1,6-branched N-glycans extended with polylactosamine chains did not serve as the ligand for lung colonisation in B16-F10 cells [105]. Human melanocytes did not express sialyl-Lewis X antigens and poorly expressed sialyl-Lewis A (SAα2,3Galβ1,3(Fucα1,4)GlcNAcβ-) antigens; however, these structures are overexpressed on cultured melanoma cells and melanoma tissue biopsies [112]. These findings indicated that sialyl-Lewis X and sialyl-Lewis A antigens are neoplastic differentiation antigens of human melanoma. Moreover, it has been proved that acquiring the expression level of sialyl-Lewis X antigens through the transfection of α1,3-fucosyltransferase III dramatically increased the metastatic capability of human melanoma MeWo and mouse melanoma B16 cells [113, 114]. However, T antigen, another potential ligand for galectin-3, has not been involved in mouse lung-specific metastasis [109]. Nevertheless, α 2,3-linked sialic acids on the surface of B16-F10 cells have been demonstrated to play an important role in lung metastasis [115]. The use of soyasaponin I, an inhibitor that reduces the expression of α 2,3-linked sialic acids, not only enhanced cell adhesion to extracellular matrix proteins, reduced cell migration, but also reduced the ability of melanoma cells for lung colonisation in mice. The positive correlation between the level of α1,6-fucosylated biantennary N-glycans on B16 murine cells and cellular potential to metastasise to the lung has been also demonstrated [116]. It has also been shown that cells expressing multi-antennary N-oligosaccharides un-substituted with polylactosamine chains home in the liver which expresses galectin-1 [117].
Recent advances in the discovery of microRNA (miRNA) role in cutaneous melanoma pathogenesis have revealed that miRNA can affect the cell surface proteins by interfering with their post-translational modifications. It has been found that overexpression of
To date, one monoclonal antibody TM10 produced from mice vaccinated with FasL-expressing B16-F10 mouse melanoma cells was able to recognise a range of human tumour cell lines, including melanoma [120]. Despite the fact that over 50% of cancers express tumour-associated carbohydrate antigens, such as gangliosides, Lewis antigens and Thomsen-Friedenreich antigen, none of them was the antigenic target of TM10. However, another monoclonal antibody HMB45 that recognises melanoma-specific target, i.e. Pmel17/gp100, reacts with its sialylated RPT domain [121].
4. Glycation and melanoma
The risk of melanoma is significantly associated with high fasting glucose, which is entirely independent on age, body mass index and smoking [122]. A non-enzymatic reaction (glycation) between ketones or aldehydes and amino groups of proteins contributes to the ageing of proteins and leads to the formation and accumulation of irreversible cross-linked protein derivatives termed advanced glycation end products (AGE). AGE have been proved to stimulate growth and migration of malignant melanoma
RAGE has been shown to interact with S100B [129], which is a serological biomarker widely used in clinical practice to determine the prognosis for patients with distal melanoma metastases, despite the fact that it fails to detect melanoma progression in up to 20% of patients [130–133]. Recently, it has been demonstrated that among stage III–IV melanoma patients, decreased serum levels of soluble forms of RAGE (sRAGE and esRAGE) correlated with poor overall survival [134]. Interestingly, it has also been proved that overexpression of RAGE in WM115 human primary melanoma cells was associated with mesenchymal-like morphology of the cell, a switch to a metastatic phenotype as well as up-regulation of S100B [126]. As the elevated level of S100B is known to down-regulate p53 suppressor protein, small-molecule inhibitors targeting S100B-p53 interaction are currently under intense investigations as new therapeutic strategies for malignant melanoma [135, 136]. It has also been shown that the expression of S100P, which is another member of the S100 family, was significantly higher in malignant melanoma than in primary melanoma [137]. Abnormal level of S100P can contribute to tumour growth, invasion and metastasis [138]. Other functional ligands for RAGE include chondroitin sulphate containing E disaccharide units (GlcNAβ1-3GalNAc(4,6-O-disulfate)β1-) and heparin sulphate [127].
5. Conclusions
Alterations in glycans on proteins and lipids have long been associated with malignant transformation. The observed modifications are either a direct consequence of the oncogenic process or an indirect effect of changes occurring in the tissue environment and inflammation. Analytical efforts in melanoma glycomics contribute to understanding the role of cellular and molecular properties of cells that influence the dissemination of tumour cells, which might be essential for understanding the pathogenesis of tumour development and metastasis. These studies also offer considerable possibilities for screening, selection and identification of differentially expressed glycoconjugates, in order to develop non-invasive, sensitive and discriminative
Acknowledgments
The writing of this manuscript was supported in part by grants from the Institute of Zoology, Jagiellonian University in Krakow (K/ZDS/005403) and from the National Science Centre, Poland (2013/11/B/NZ4/04315).
References
- 1.
Garbe C, Leiter U: Melanoma epidemiology and trends. Clin Dermatol. 2009;27:3–9. DOI: 10.1016/j.clindermatol.2008.09.001 - 2.
Erdmann F, Lortet-Tieulent J, Schüz J, Zeeb H, Greinert R, Breitbart EW, Bray F: International trends in the incidence of malignant melanoma 1953-2008 – are recent generations at higher of lower risk? Int J Cancer. 2013;132:385–400. DOI: 10.1002/ijc.27616 - 3.
Dummer R, Hauschild A, Jost L: Cutaneous malignant melanoma: ESMO clinical recommendations for diagnosia, treatment and follo-up. Anna Oncol. 2008;19:86–88. DOI: 10.1093/annonc/mdn100 - 4.
Garbe C, Peris K, Hauschild A, Saiag P, Middeleton M, Spaza A, Grob JJ, Malvehy J, Newton-Bishop J, Stratigos A, Pehamberger H, Eggermont A: Diagnosis and treatment of melanoma: European consensus-based interdisciplinary guideline. Eur J Cancer. 2010;46:270–283. DOI: 10.1016/j.ejca.2009.10.032 - 5.
Ohtsubo K, Marth JD: Glycosylation in cellular mechanisms of health and disease. Cell. 2006;126:855–867 - 6.
Varki ACR, Cummings R, Esko JD, Freeze HH, Stanley P, Bertozzi CR, Hart GW, Etzler ME, editors. Essentials of Glycobiology. 2nd edition. Cold Spring Harbor (NY): Cold Spring Harbor Laboratory Press; 2009. - 7.
Jankowic M: Glycans as biomarkers: status and perspectives. J Med Biochem. 2011;30:213–223. DOI: 10.2478/v10011-011-0023-5 - 8.
Moremen KW, Tiemeyer M, Nairn AV: Vertebrate protein glycosylation: diversity, synthesis and function. Nat Rev Mol Cell Biol. 2012;13:448–462. DOI: 10.1038/nrm3383 - 9.
Adamczyk B, Tharmalingam T, Rudd PM: Glycans as cancer biomarkers. Biochem Biophys Acta. 2012;1820:1347–1353. DOI: 10.1016/j.bbagen.2011.12.001 - 10.
Hennet T: Disease of glycosylation beyond classical congenital disorders of glycosylation. Biochim Biophys Acta. 2012;1820:1306–1317. DOI: 10.1016/j.bbagen.2012.02.001 - 11.
Freire-de-Lima L: Sweet and sour: the impact of differentia glycosylation in cancer cell understanding epithelial-mesenchymal transition. Front Oncol. 2014;5:59. DOI: 10.3389/fonc.2014.00059 - 12.
Taniguchi N, Kizuka Y: Glycans and cancer: role of N-glycans in cancer biomarker, progression and metastasis, and therapeutics. Adv Cancer Res. 2015;126:11–52. DOI: 10.1016/bs.acr.2014.11.001 - 13.
Spiro R: Protein glycosylation: nature, distribution, enzymatic formation, and disease implication of glycopeptide bonds. Glycobiology. 2002;12:43–56. - 14.
Knezevic A, Gornik O, Polasek O, Pucic M, Redzic I, Novokmet M, Rudd PM, Wright AF, Campbell H, Rudan I, Lauc G: Effect of aging, body mass index, plasma lipid profiles, and smoking on human plasma N-glycans. Glycobiology. 2010;20:959–969. DOI: 10.1093/glycob/cwq051 - 15.
Strowell SR, Ju T, Cummings RD: Protein glycosylation in cancer. Annu Rev Pathol. 2015;10:473–510. DOI: 10.1146/annurev-pathol-012414-040438 - 16.
Vojta A, Samaržija I, Bočkor L, Zoldoš V: Glyco-gene change expression in cancer through aberrant methylation. Biochim Biophys Acta. 2016:1860:1776–1785. DOI: 10.1016/j.bbagen.2016.01.002 - 17.
Dennis JW, Granovsky M, Warren CE: Glycoprotein glycosylation and cancer progression. Biochim Biophys Acta. 1999;1473:21–34. - 18.
Fuster MM, Esko JD: The sweet and sour of cancer: glycans as novel therapeutic targets. Nat Rev Cancer. 2005;5:526–542. - 19.
Wandall H, Tarp MA: Therapeutic cancer vaccines: clinical trials and applications. In: Guo Z, Boons GJ, editors. Carbohydrate-based Vaccines and Immunotherapies. Hoboken, New Jersey: Wiley & Sons Inc; 2009. pp. 333–366. DOI: 10.1002/9780470473283.ch10 - 20.
Markidakis M, Vlahou A: Secretome proteomics for discovery of cancer biomarkers. J Proteom. 2010;73:2291–2305. DOI: 10.1016/j.jprot.2010.07.001 - 21.
Shukla HD, Vaitiekunas P, Cotter RJ: Advances in membrane proteomics and cancer biomarker discovery: Currant status and future prespective. Proteomics. 2012;12:3085–3104. DOI: 10.1002.pmic.201100519 - 22.
Christiansen MN, Chik JJ, Lee L, Anugraham M, Abrahams JL, Packer NH: Cell surface glycosylation in cancer. Proteomics. 2014;14:525–546. DOI: 10.1002/pmic.201300387 - 23.
De la Luz-Hernandez K, Rabas Y, Monlesinos R, Fuentes D, Santo-Tomás JF, Morales O, Aquilar Y, Pacheco B, Castillo A: Cancer vaccine characterisation: From bench to clinic. Vaccine 2014;32:2851–2858. DOI: 10.1016/j.vaccine.2014.02.017 - 24.
Padler-Karavani V: Aiming at the sweet side of cancer: aberrant glycosylation as possible target for personalized-medicine. Cancer Lett. 2014;352:102–112. DOI: 10.1016/j.canlet.2013.10.005 - 25.
Rho JH, Mead JR, Wright WS, Brenner DE, Stave JW, Gildersleeve JC, Lampe PD: Discovery of sialyl Lewis A and Lewis X modified protein cancer biomarkers using high density antibody arrays. J Proteomics. 2014;96:291–299. DOI: 10.1016/j.jprot.2013.10.030 - 26.
Zhang X, Wang Y, Qian Y, Wu X, Zhang Z, Liu X, Zhao R, Zhou L, Ruan Y, Xu J, Liu H, Ren S, Xu C, Gu J: Discovery of specific metastasis-related N-glycan alterations in epithelial ovarian cancer based on quantitative glycomics. PLoS One. 2014;9:e87978. DOI: 10.1371/journal.pone.0087978 - 27.
Packer NH, von der Lieth CW, Aoki-Kinoshita KF, Lebrilla CB, Paulson JC, Raman R, Rudd P, Sasisekharan R, Taniguchi N, York WS: Frontiers in glycomics: bioinformatics and biomarker in disease. An NIH white paper prepared from discussions by the focus group at a workshop on the NIH campus, Bethesda, MD (September 11–13, 2006). Proteomics. 2008;8:8–20. - 28.
Gu J, Taniguchi N: Potential of N-glycan in cell adhesion and migration either a positive or negative regulator. Cell Adh Migr. 2008;2:243–245. - 29.
Kufe DW: Mucins in cancer: function, prognosis and therapy. Nat Rev. 2009; 9:631–664. DOI: 10.1038/nrc2761 - 30.
Gu J, Isaji T, Xu Q, Kariya Y, Gu W, Fukuda T, Du Y: Potential roles of N-glycosylation in cell adhesion. Glycoconj J. 2012;29:599–607. DOI: 10.1007/s10719-012-9386 - 31.
Pinho SS, Oliveira P, Cabral J, Carvalho S, Huntsman D, Gärtner F, Seruca R, Reis CA, Oliveira C: Loss and recovery of Mgat3 and GnT-III mediated E-cadherin N-glycosylation is a mechanism involved in epithelial-mesenchymal-epithelial transition. PLoS One. 2012;7:e33191. DOI: 10.1371/journal.pone.0033191 - 32.
Li N, Xu H, Fan K, Liu X, Qi J, Zhao C, Yin P, Wang L, Li Z, Zha X: Altered β1,6-GlcNAC branched N-glycans impair TGF-β-mediated epithelial-to-mesenchymal transition through Smad signalling pathway in human lung cancer. J Cell Mol Med. 2014;18:1975–1991. DOI: 10.1111/jcmm.12331 - 33.
Radhakrishnan P, Dabelsteen S, Madsen FB, Francavilla C, Kopp KL, Steentoft C, Vahhrushev SY, Olsen JV, Hansen L, Bennet EP, Woetmann A, Yin G, Chen L, Song H, Bak M, Hlady RA, Peters SL, Opavsky R, Thode C, Qvortrup K, Schjoldager KT, Clausen H, Hollingsworth MA, Wandall HH: Immature truncated O-glycophenotype of cancer directly induces oncogenic features. Proc Natl Acad Sci U S A. 2014;111:E4066-75. DOI: 10.1073/pnas.1406619111 - 34.
Tan Z, Lu W, Li X, Yang G, Guo J, Yu H, Li Z, Guan F: Alteed N-glycan expression profile in epithelial-to-mesenchymaltransition of NMuMG cells revealed by an integrated strategy using mass spectrometry and glycogene and lectin microarray analysis. J Proteome Res. 2014;13:2783–2795. DOI: 10.1021/pr401185z - 35.
Herlyn M, Fukunaga-Kalabis M: What is a good model for melanoma? J Invest Dermatol. 2010;130:911–912. DOI: 10.1038/jid.2009.441 - 36.
Passaniti A, Hart GW: Cell surface sialylation and tumor metastasis. Metastatic potential of B16 melanoma variants correlates with their relative number of specific penultimate oligosaccharide structures. J Biol Chem. 1988;263:7591–7603. - 37.
Finne J, Tao TW, Burger MM: Carbohydrate changes in glycoproteins of a poorly metastasizing wheat germ agglutinin-resistant melanoma clone. Cancer Res. 1980;40:25802587. - 38.
Burger MM, Tao TW, Finne J, Prieels JP: The influence of membrane mutations on metastasis. Biosci Rep. 1982;2:597–599. - 39.
Gorelik E, Duty L, Anakari F, Galili U: Alterations of cell surface carbohydrates and inhibition of metastatic property of murine melanomas by alpha 1,3 galactosyltransferasegene expression. Melanoma Res. 1995;55:4168–4173. - 40.
Tulsiani DRP, Harris TM, Touster O: Swainsonine inhibits the biosynthesis of complex glycoproteins by inhibition of Golgi α-mannosidase II. J Biol Chem. 1982;257:7936–7939. - 41.
Humphries MJ, Matsumoto K, White SL, Olden K: Oligosaccharide modification by swainsonine treatment inhibits pulmonary colonization by B16F10 murine melanoma cells. Proc Natl Acad Sci U S A. 1986;S3:1752–2756. - 42.
Dennis JW, Koch K, Yousefi S, VanderElst: Growth inhibition of human melanoma tumor xenografts in athymic nude mice by swainsonine. Cancer Res. 1990;50:1867–1872. - 43.
Goss PE, Reid CL, Bailey D, Dennis JW: Phase IB clinical trial of the oligosaccharide processing inhibitor swainsonine in patients with advanced malignancies. Clin Cancer Res. 1997;3:1077–1086. - 44.
Yoshimura M, Nishikawa A, Ihara Y, Taniguchi S, Taniguchi N: Suppression of lung metastasis of B16 mouse melanoma by N-acetylglucosaminyltransferase III gene transfection. Proc Natl Acad Sci USA. 1995;92:8754–8758. - 45.
Yoshimura M, Ihera Y, Matsuzawa Y, Taniguchi N: Abberant glycosylation of E-cadherin enhances cell-cell binging to suppress metastasis. J Biol Chem. 1996;271:3811–3815. - 46.
Dricu A, Carlberg M, Wang M, Larsson O: Inhibition of N-linked glycosylation using tunicamycin causes cell death in malignant cells: role of down regulation of the insulin-like growth factor 1 receptor in induction of apoptosis. Cancer Res. 1997;57:543–548. - 47.
Dricu A, Wang M, Hjertman M, Malec M, Blegen H, Wejde J, Carlberg M, Larsson O: Mevalonate-regulated mechanizms in cell growth control: role of dolichyl phosphate in expression of the insulin-like growth factor-1 receptor (IGF-IR) in comparison to Ras prenylation and expression of c-myc. Glycobiology. 1997:7:625–633. - 48.
Przybyło M, Martuszewska D, Pocheć E, Hoja-Łukowicz D, Lityńska A: Identification of proteins bearing β1-6 branched N-glycans In human melanoma cell lines from different progression stages by tandem mass spectrometry analysis. Biochim Biophys Acta. 2007;1770:1427–1435. - 49.
Taniguchi N, Korekane H: Branched N-glycans and their implications for cell adhesion, signaling and clinical application for cancer biomarkers and in therapeutics. BMB Rep. 2011;44:772–781. - 50.
Gorelik E, Galili U, Raz A: On the role of cell surface carbohydrates and their binding proteins (lectins) in tumor metastasis. Cancer Metastasis Rev. 2001;20:245–277. - 51.
Chakraborty AK, Pawelek J, Ikeda Y, Miyoshi E, Kolesnimova N, Funasaka Y, Ichihashi M, Taniguchi N: Fusion hybrids with macrophage and melanoma cells up-regulate N-acetylglucosaminyltransferase V, β1-6 branching, and metastasis. Cell Growth Differ. 2001;12:623–630. - 52.
Pawelek JM: Viewing malignant melanoma cells as macrophage tumor hybrids. Cell Adh Migr. 2007;1:2–6. - 53.
Pawelek JM, Chakraborty AK: The cancer cell-leucocyte fusion theory of metastasis. Adv Cancer Res. 2008;101:397–444. DOI: 10.1016/S0065-230X(08)00410-7 - 54.
Lazova R, Pawelek JM: Why melanomas get so dark? Exp Dermatol. 2009;18:934–938. DOI: 10.1111/j.1600-0625.2009.00933.x - 55.
Lazova R, Klump V, Pawelek J: Autophagy in cutaneous malignant melanoma. J Cutan Pathol. 2010;37:256–268. DOI: 10.1111/j.1600-0560.2009.01359.x - 56.
Granovsky M, Fata J, Pawling J, Muller WJ, Khokha R, Dennis JW: Supression of tumor growth and metastasis in Mgat5-deficient mice. Nature. 2000;6:306–312. - 57.
Lityńska A, Przybyło M, Pocheć E, Hoja-Łukowicz D, Ciołczyk D, Laidler P, Gil D: Comparison of the lectin-binding pattern in different human melanoma cell lines. Melanoma Res. 2001;11:201–212. - 58.
Mendoza I, Olaso E, Anasagasti MJ, Fuentes AM, Vidal-Vanaclocha F: Mannose receptor-mediated endothelial activation contributes to B16 melanoma cell adhesion and metastasis in liver. J Cell Physiol. 1998;174:322–330. - 59.
Laidler P, Lityńska A, Hoja-Łukowicz D, Łabędź M, Przybyło M, Ciołczyk-Wierzbicka D, Pocheć E, Trębacz E, Kremser E: Characterization of glycosylation and adherent properties of melanoma cells. Cancer Immunol Immuther. 2006;55:112–118. DOI: 10.1007/s00262-005-0019-4 - 60.
Pocheć E, Janik M, Hoja-Łukowicz D, Link-Lenczowski P, Przybyło M, Lityńska A: Expression of integrins α3β1 and α5β1 and GlcNAc β 1,6 glycan branching influences metastatic melanoma cell migration on fibronectin. Eur J Cell Biol. 2013;92:355–362. DOI: 10.1016/j.ejcb.2013.10.007 - 61.
Handerson T, Berger A, Harigopol M, Rimm D, Nishigori C, Ueda M, Miyoshi E, Taniguchi N, Pawelek J: Melanophages reside in hypermelanotic, aberrantly glycosylated tumor areas and predict improved outcome in primary cutaneous malignant melanoma. J Clin Pathol. 2007;34:679–686. DOI: 10.1111/j.1600-0560.2006.00681 - 62.
Litynska A, Przybylo M, Pochec E, Kremser E, Hoja-Lukowicz D, Sulowska U: Does glycosylation of melanoma cells influence their interaction with fibronectin? Biochimie. 2006;88:527–534. - 63.
Przybyło M, Pocheć E, Link-Lenczowski P, Lityńska A: β1-6 branching of cell surface glycoproteins may contribute to uveal melanoma progression by up-regulating cell motility. Mol Vis. 2008;14:625–636. - 64.
Krähling H, Mally S, Eble JA, Noël J, Schwab A, Stock C: The glycocalyx maintains a cell surface pH nanoenvironment crucial for integrin-mediated migration of human melanoma cells. Pflugers Arch. 2009;458:1069–1083. DOI: 10.1007/s00424-009-0694-7 - 65.
Ochwat D, Hoja-Łukowicz D, Lityńska A: N-glycoproteins bearing β1-6 branched oligosaccharides from the A375 human melanoma cell line analysed by tandem mass spectrometry. Melanoma Res. 2004;14:479–485. - 66.
Pocheć E, Lityńska A, Amoresano A, Casbarra A: Glycosylation profile of integrin α3β1 integrin changes with melanoma progression. Biochim Biophys Acta. 2003;1644:113–123. - 67.
Ciołczyk-Wierzbicka D, Amoresano A, Casbarr A, Hoja-Łukowicz D, Lityńska A, Laidler P: The structure of the oligosaccharides of N-cadherin from human melanoma cell lines. Glycoconjugate J. 2004;20:483–492. - 68.
Kremser ME, Przybyło M, Hoja-Łukowicz D, Pocheć E, Amoresano A, Carpentieri A, Bubka M, Lityńska A: Characterisation of α3β1 and αvβ3 integrin N-oligosaccharides in metastatic melanoma WM9 and WM239 cell lines. Biochim Biophys Acta. 2008;1780:1421–1431. DOI: 10.1016/j.bbagen.2008.07.011 - 69.
Janik ME, Przybyło M, Pocheć E, Pokrywka M, Lityńska A: Effect of α3β1 and αvβ3 integrin glycosylation on interaction of melanoma cells with vitronectin. Acta Biochim Pol. 2010;57:55–61. - 70.
Hoja-Łukowicz D, Link-Lenczowski P, Carpentieri A, Amoresano A, Pocheć E, Artemenko K, Bergquist J, Lityńska A: L1CAM from human melanoma carries a novel type of N-glycan with Galβ1-4Galβ1- motif. Involvement of N-linked glycans in migratory and invasive behaviour of melanoma cells. Glycoconj J. 2013;30:205–225. DOI: 10.1007/s10719-012-9374-5 - 71.
Janik ME, Lityńska A, Przybyło M: Studies on primary uveal and cutaneous melanoma cell interaction with vitronectin. Cell Biol Int. 2014;38:942–952. DOI: 10.1002/cbin.10280 - 72.
Taniguchi N, Miyoshi E, Jianguo G, Honke K, Matsumoto A: Decoding sugar function by identifying target glycoproteins. Curr Opin Struct Biol. 2006;16:561–566. - 73.
Thies A, Moll I, Berger J, Schumacher U: Lectin binding to cutaneous malignant melanoma: HPA is associated with metastasis formation. Br J Cancer. 2001;84:819–823. - 74.
Singhal A, Fohn M, Hakomori S: Induction of α-N-acetylgalactosamine-O-serine/threonine (Tn) antigen-mediated cellular response for active immunotherapy in mice. Cancer Res. 1991;51:1406–1411. - 75.
Hoja-Łukowicz D, Przybyło P, Pocheć E, Drabik A, Silberring J, Kremser M, Schadendorf D, Laidler P, Lityńska A: The new face of nucleolin in human melanoma. Cancer Immunol Immunother. 2009;58:1471–1480. DOI: 10.1007/s00262-009-0705-8 - 76.
Ostankovitch M, Altrich-VanLith M, Robila V, Engelhard VH: N-glycosylation enhances presentation of a MHC class I-restricted epitope from tyrosinase. J Immunol. 2009;182:4830–4835. DOI: 10.4049/jimmunol.0802902 - 77.
Kittlesen DJ, Thompson LW, Gulden PH, Skipper JC, Colella TA, Shabanowitz JA, Hunt DF, Engelhard VH, Slingluff Jr CL: Human melanoma patients recognize an HLA-A1-restricted CTL epitope from tyrosinase containing two cysteine residues: implications for tumor vaccine development. J Immunol. 1998; 160:2099–2106. - 78.
Passaniti A, Hart GW: Metastasis-associated murine melanoma cell surface galactosyltransferase: characterisation of enzyme activity and identification of major surface substrates. Cancer Res. 1990;50:7261–7271. - 79.
Ruan S, Lioyd KO: Glycosylation pathways in the biosynthesis of gangliosides in melanoma and neuroblastoma cells: relative glycosyltransferase levels determine ganglioside patterns. Cancer Res. 1992;52:5725–5731. - 80.
Yamashiro S, Ruan S, Furukawa K, Tai T, Lloyd KO, Shiku H, Furukawa K: Genetic and enzymatic basis for the differential expression of GM2 and GD2 gangliosides in human cancer cell lines. Cancer Res. 1993;53:5395–5400. - 81.
Morton DL, Ravindranath MH, Irie RF: Tumor gangliosides as targets for active specific immunotherapy of melanoma in men. Prog Brain Res. 1994;101:251–275. - 82.
Yamashiro S, Haraguchi M, Furukawa K, Takamiya K, Yamamoto A, Nagata Y, Lloyd KO, Shiku H, Furukawa K: Substrate specificity of β1,4 N-acetylgalactosaminyltransferase in vitro and in cDNA-transfected cells. GM2/GD2 synthase efficiently generates asialo-GM2 in certain cells. J Biol Chem. 1995;270:6149–6155. - 83.
Ravindranath MH, Hsueh EC, Verma M, Ye W, Morton DL: Serum total ganglioside level correlates with clinical course in melanoma patients after immunotherapy with therapeutic cancer vaccine. J Immunother. 2003;26:277–285. - 84.
Kavanagh D, Hill AD, Djikstra B, Kennelly R, McDermott EM, O’Higgins NJ: Adjuvant therapies in the treatment of stage II and III malignant melanoma. Surgeon. 2005;3:245–256. - 85.
Ladisch S, Kitada S, Hays EF: Gangliosides shed by tumor cells enhance tumor formation in mice. J Clin Invest. 1987;79:1879–1882. - 86.
Carr A, Mazorra Z, Alonso DF, Mesa C, Valiente O, Gomez DE, Perez R, Fernandez LE: A purified GM3 ganglioside conjugated vaccine induces specific, adjuvant-dependent and non-transient antitumour activity against B16 mouse melanoma in vitro and in vivo. Melanoma Res. 2001;11:219–227. - 87.
Bennaceur K, Popa I, Portoukalian J, Berthier-Vergnes O, Péguet-Navarro J: Melanoma-derived gangliosides impair migratory and antigen-presenting function of human epidermal Langerhans cells and induce their apoptosis. Int Immunol. 2006;18:879–886. - 88.
Shaw L, Schauer R: The biosynthesis of N-glycoloylneuraminic acid occurs by hydroxylation of the CMP-glycoside of N-acetylneuraminic acid. Biol Chem Hoppe Seyler. 1988;369:477–486. - 89.
Irie A, Koyama S, Kozutsumi Y, Kawasaki T, Suzuki A: The molecular basis for the absence of N-glycolylneuraminic acid in humans. J Biol Chem. 1998; 273:15866–15871. - 90.
Malykh YN, Schauer R, Shaw L: N-Glycolylneuraminic acid in human tumours. Biochimie. 2001;83:623–634. - 91.
Carr A, Mullet A, Mazorra Z, Vazquez AM, Alfonso M, Mesa C, Rengifo E, Perez R, Fernandez LE: A mouse IgG1 monoclonal antibody specific for N-glycolyl GM3 ganglioside recognized breast and melanoma tumors. Hybridoma. 2000;19:241–247. - 92.
Fernandez A, Mesa C, Marigo I, Dolcetti L, Clavell M, Oliver L, Fernandez LE, Bronte V: Inhibition of tumor-induced myeloid-derived suppressor cell function by nanoparticulated adjuvant. J Immunol. 2011;186:264–274. DOI: 10.4049/jimmunol.1001465 - 93.
Gabri MR, Mazorra Z, Ripoll GV, Mesa C, Fernandez LE, Gomez DE, Alonso DF: Complete antitumor protection by perioperative immunization with GM3/VSSP vaccine in a preclinical mouse melanoma model. Clin Cancer Res. 2006;12:7092–7098. - 94.
Segatori VI, Otero LL, Fernandez LE, Gomez DE, Alonso DF, Gabri MR: Antitumor protection by NGcGM3/VSSP vaccine against transfected B16 mouse melanoma cell overexpression N-glycolylated gangliosides. In Vivo. 2012;26:609–617. - 95.
de Leon J, Fernandez A, Mesa C, Clavel M, Fernandez LE: Role of tumour associated N-glycolylated variant of GM3 ganglioside in cancer progression: effect over CD4 expression on T cells. Cancer Immunol Immunother. 2006;55:443–450. - 96.
Machado YJ, Rabasa Y, Montesinos R, Cremata J, Besada V, Fuentes D, Castillo A, de la Luz KR, Vázquez AM, Himly M: Physicochemical and biological characterization of 1E10 anti-idiotype vaccine. BMC Biotechnol. 2011;11:12. DOI: 10.1186/1472-6750-11-112 - 97.
Ragupathi G, Meyers M, Adluri S, Howard L, Musselli C, Livingston PO: Induction of antibodies against GD3 ganglioside in melanoma patients by vaccination with GD3-lactone-KLH conjugate plus immunological adjuvant QS-21. Int J Cancer. 2000;85:659–666. - 98.
Cheresh DA, Reisfeld RA, Varki AP: O-acetylation of disialoganglioside GD3 by human melanoma cells creates a unique antigenic determinant. Science. 1984;225:844–846. - 99.
Kohla G, Stockfleth E, Schauer R: Gangliosides with O-acetylated sialic acids in tumors of neuroectodermal origin. Neurochem Res. 2002;27:583–592. - 100.
Bogenrieder T, Herlyn M: Cell-surface proteolysis, growth factor activation and intracellular communication in the progression of melanoma. Crit Rev Oncol Hematol. 2002;44:1–15. - 101.
Li G, Satayamoorthy K, Herlyn M: Dynamics of cell interactions and communication during melanoma development. Crit Rev Oral Biol Mol. 2002;13:62–70. DOI: 10.1111/j.1600-0560.2009.01359.x - 102.
Bennet KL, Modrell B, Greenfield B, Bartolazzi A, Stamenkovic I, Peach R, Jackson DG, Spring F, Aruffo A: Regulation of CD44 binding to hyaluronan by glycosylation of variable spliced exons. J Cell Biol. 1995;131:1623–1633. - 103.
Bartolazzi A, Nocks A, Aruffo A, Spring F, Stamenkovic I: Glycosylation of CD44 is implicated in CD44-mediated cell adhesion to hyaluronan. J Cell Biol. 1996;132:1199–1208. - 104.
Sheng Y, Yoshimura M, Inouke S, Oritani K, Nishiura T, Yoshida H, Ogawa M, Okajima Y, Matsuzawa Y, Taniguchi N: Remodeling of glycoconjugates on CD44 enhances cell adhesion to hyaluronate, tumor growth and metastasis in B16 melanoma cees expressing β1,4-N-acetylglycosaminyltransferase III. Int J Cancer. 1997;73:850–858. - 105.
Krishnan V, Bane SM, Kawle PD, Naresh KN, Kalraiya RD: Altered melanoma cell surface glycosylation mediates organ specific adhesion and metastasis via lectin receptors on the lung vascular endothelium. Clin Exp Metastasis. 2005;22:11–24. - 106.
Ogura T, Noguchi T, Murai-Takebe R, Hosooka T, Honma N, Kasuga M: Resistance of B16 melanoma cells to CD47-induced negative regulation of motility as a result of aberrant N-glycosylation of SHPS-1. J Biol Chem. 2004;279:13711–13720. - 107.
Schinkel AH, Kemp S, Dolle M, Rudenko G, Wagenaar E: N-glycosylation and deletion mutants of the human MDR1 P-glycoprotein. J Biol Chem. 1993;268:7474–7481 - 108.
Selim MA, Burchette JL, Bowers EV, de Ridder GG, Mo L, Pizzo SV, Gonzalez-Gronow M: Changes in oligosaccharide chains of autoantibodies of GRP78 expressed during progression of malignant melanoma stimulate melanoma cell growth and survival. Melanoma Res. 2011;21:323–334. DOI: 10.1097/CMR.0b013e3283471042 - 109.
Srinivasan N, Bane SM, Ahire SD, Ingle AD, Kalraiya RD: Poly-N-acetyllactosamine substitution on N- and nor O-oligosaccharides or Thomsen-Friedenreich antigen facilitate lung specific metastasis of melanoma cells via galectin-3. Glycocon J. 2009;26:445–456. DOI: 10.1007/s10719-008-9194-9 - 110.
More SK, Srinivasan N, Budnar S, Bane SM, Upadhya A, Thorat RA, Ingle AD, Chiplunkar SV, Kalraiya RD: N-glycans and metastasis in galectin-3 transgenic mice. Biochem Biophys Res Commun. 2015;460:302–307. DOI: 10.1016/j.bbrc.2015.03.030 - 111.
Biancone L, Araki M, Araki K, Vassalli P, Stamenkovic I: Redirection of tumor metastasis by expressing E-selectin in vivo. J Exp Med. 1996;183:581–587. - 112.
Ravindranath MH, Amiri AA, Bauer PM, Kelley MC, Essner R, Morton DL: Endothelial-selectin ligands sialyl Lewis x and sialyl Lewis a are differentiation antigens immunogenic in human melanoma. Cancer. 1997;79:1686–1697. - 113.
Ohyama C, Tsuboi S, Fukuda M: Dual roles of sialyl Lewis X oligosaccharides in tumor metastasis and rejection by natural killer cells. EMBO J. 1999;18:1516–1525. - 114.
Ohyama C, Kanto S, Kato K, Nakano O, Arai Y, Kato T, Chen S, Fukuda MN, Fukuda M: Natural killer cells attack tumor cells expressing high levels of sialyl Lewis x oligosaccharides. PNAS. 2002;99:13789–13794. - 115.
Chang WW, Yu CY, Lin TW, Wang PH, Tsai YC: Soyasaponin I decreases the expression α2,3-linked sialic acids on the cell surface and supresses the metastatic potential of B16F10 melanoma cells. Biochim Biophys Res Commun. 2006;341:614–619. - 116.
Sakuma K, Fujimoto I, Hitoshi S, Tanaka F, Ikeda T, Tanabe K, Toyokuni S, Wada H, Mio T, Mishima M, Ikenaka K: An N-glycan structure correlates with pulmonary metastatic ability of cancer cells. Biochim Biophys Res Commun. 2006;340:829–835. - 117.
Reddy BV, Kalraiya RD: Sialylated beta1,6 branched N-oligosaccharides modulate adhesion, chemotaxis and motility of melanoma cells: Effect on invasion and spontaneous metastasis properties. Biochim Biophys Acta 2006;1760:1393–1402. - 118.
Gaziel-Sovran A, Segura MF, Di Micco R, Collins MK, Hanniford D, Vega-Saenz de Miera E, Rakus JF, Dankert JF, Shang S, Kerbel RS, Bhardwaj N, Shao Y, Darvishian F, Zavadil J, Erlebacher A, Mahal LK, Osman I, Hernando E. miR-30b/30d regulation of GalNAc transferase enhances invasion and immunosuppression during metastasis. Cancer Cell. 2011;20:104–118. DOI: 10.1016/j.ccr.2011.05.027 - 119.
Ten Hagen KG, Fritz TA, Tabak LA: All in the family: the UDP-GalNAc:polypeptide N-acetylgalactosaminyltransferases. Glycobiology. 2003;13:1R–16R - 120.
Nowsom-Davis TE, Wang D, Stein L, Chen PFT, Wang LX, Simon AK, Screaton GR: Enhanced immune recognition of cryptic glycan markers in human tumors. Cancer Res. 2009;69:2018–2025. DOI: 10.1158/0008-5472.CAN-08-3589 - 121.
Hoashi T, Tamaki K, Hearing VJ: The secreted form of a melanocyte membrane-bound glycoprotein (Pmel17/gp100) is released by ectodomain shedding. FASEB J. 2010;24:916–930. DOI: 10.1096/fj.09-140921 - 122.
Stattin P, Björ O, Ferrari P, Lukanova A, Lenner P, Lindhal B, Hallmans G, Kaaks R: Prospective study of hyperglycemia and cancer risk. Diabetes Care. 2007;30:561–567. - 123.
Abe R, Shimizu T, Sugawara H, Watanabe H, Nakamura H, Choei H, Sasaki N, Yamagishi S, Takeuchi M, Shimizu H: Regulation of human melanoma growth and metastasis by AGE-AGR receptor interactions. J Invest Dermatol. 2004;122:461–467. - 124.
Takeuchi M, Samagishi S: TAGE (toxic AGEs) hypothesis in various chronic diseases. Med Hypoth. 2004;63:449–452. - 125.
Ojima A, Matsui T, Maeda S, Takeuchi M, Inoue H, Higashimoto Y, Yamagishi SI: DNA aptamer raised against advanced glycation end products inhibits melanoma growth in nude mice. Lab Invest. 2014;94:422–429. DOI: 10.1038/labinvest.2014.5 - 126.
Meghnani V, Vetter SW, Leclerc E: RAGE overexpression confers a metastatic phenotype of the WM115 human primary melanoma cell line. Biochim Biophys Acta. 2014;1842;1017–1027. DOI: 10.1016/j.bbadis.2014.02.01 - 127.
Mizumoto S, Sugahara K: Glycosaminoglycans are functional ligands for receptor for advanced glycation end-product in tumors. FEBS J. 2012;280:2462–2470. DOI: 10.1111/febs.12156 - 128.
Saha A, Lee YC, Zhang Z, Chandra G, Su SB, Makherjee AB: Lack of an endogenous anti-inflammatory protein in mice enhances colonization of B16F10 melanoma cell in the lungs. J Biol Chem. 2010;285:10822–10831. DOI: 10.1074/jbc.M109.083550 - 129.
Hofmann MA, Drury S, Fu C, Qu W, Taguchi A, Lu Y, Avila C, Kambham N, Bierhaus A, Nawroth P, Neurath MF, Slattery T, Beach D, McClary J, Nagashima M, Morser J, Stern D, Schmidt MA: RAGE mediates a novel proinflamatory axis: a central cell surface receptor for S100/calgranulin polypeptides. Cell. 1999;97:889–901. - 130.
Salama I, Malone PS, Mihaimeed F, Jones JL: A review of the S100 proteins in cancer. EJSO. 2008;34:357–364. DOI: 10.1016/j.ejso.2007.04.009 - 131.
Ugurel S, Utikal J, Becker JC: Tumor biomarkers in melanoma. Cancer Control. 2009;16:219–224. - 132.
Weide B, Elsasser M, Büttner P, Pflugfelder A, Leiter U, Eigentler TK, Bauer J, Witte M, Meier F, Garbe C: Serum markers lactate dehydrogenase and S100B predict independently disease outcome in melanoma patients with distant metastasis. Br J Cancer. 2012;107:422–428. DOI: 10.1038/bjc.2012.306 - 133.
Gebhardt C, Lichtenberger R, Utikal J: Biomarker value and pitfalls of serum S100B in the follow-up of high-risk melanoma patients. J Dtsch Dermatol Ges. 2016;14:158–164. DOI: 10.1111/ddg.12727 - 134.
Wagner NB, Weide B, Reith M, Tarnanidis K, Kehrel C, Lichtenberger R, Pflugfelder A, Herpel E, Eubel J, Ikenberg K, Busch C, Holland-Letz T, Naeher H, Garbe C, Umansky V, Enk A, Utikal J, Gebhardt C: Diminished levels of the soluble form of RAGE are related to poor survival in malignant melanoma. Int J Cancer. 2015;137:2607–2617. DOI: 10.1002/ijc.29619 - 135.
Yoshimura C, Miyafusa T, Tsumoto K: Identification of small-molecule inhibitors of the human S100B-p53 interaction and evaluation of their activity in human melanoma cells. Bioorg Med Chem. 2013;21:1109–1115. DOI: 10.1016/j.bmc.2012.12.042 - 136.
Zimmer DB, Lapidus RG, Weber DJ: In vivo screening of S100B inhibitors for melanoma therapy. Methods Mol Biol. 2013;963:303–317. DOI: 10.1007/978-1-62703-230-8_18 - 137.
Zhu L, Ito T, Nakahara T, Nagae K, Fuyuno Y, Nakao M, Akahoshi M, Nakagawa R, Tu Y, Uchi H, Furue M: Upregulation of S100P, receptor for advanced glycation end products and ezrin in malignant melanoma. J Dermatol. 2013;40:973–979. DOI: 10.1111/1346-8138.12323 - 138.
Wang G, Platt-Higgins A, Carroll J, de Silva Rudland S, Winstanley J, Barraclough R, Rudland PS: Induction of metastasis by S100P in a rat mammary model and its association with poor survival of breast cancer patients. Cancer Res. 2006;66:1199–1207.