The role of glycans in the development and progression of prostate cancer

Nature Reviews Urology

Volumn 13, Issue 6, 2016, Pages 324-333

  Munkley, Jennifer ^a   Mills, Ian G ^b,c,d   Elliott, David J ^a  

^a NEWCASTLE UNIVERSITY   (United Kingdom)

^b UNIVERSITY OF OSLO   (Norway)

^c OSLO UNIVERSITY HOSPITAL   (Norway)

^d QUEEN'S UNIVERSITY BELFAST   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

BIOLOGICAL MARKER; GLYCAN; GLYCOPROTEIN; MANNOSE; N ACETYLGLUCOSAMINE; PROTEOME; POLYSACCHARIDE;

CANCER GROWTH; CANCER PATIENT; CELL ADHESION; CELL INTERACTION; CELL METABOLISM; CELL MIGRATION; CONJUGATION; EXTRACELLULAR MATRIX; FUCOSYLATION; GENOME; GLYCOSYLATION; HUMAN; IMMUNOSURVEILLANCE; INTRACELLULAR SIGNALING; PRIORITY JOURNAL; PROSTATE CANCER; REVIEW; SIALYLATION; ANIMAL; DISEASE EXACERBATION; MALE; METABOLISM; PHYSIOLOGY; PROSTATE TUMOR;

ANIMALS; DISEASE PROGRESSION; GLYCOSYLATION; HUMANS; MALE; POLYSACCHARIDES; PROSTATIC NEOPLASMS;

EID: 84964355793     PISSN: 17594812     EISSN: 17594820     Source Type: Journal    
DOI: 10.1038/nrurol.2016.65     Document Type: Review

References (118)

1. Klotz L, & Emberton M. Management of low risk prostate cancer-Active surveillance and focal therapy. Nat. Rev. Clin. Oncol. 11, 324-334 (2014).
2. Humphrey P. A. Gleason grading and prognostic factors in carcinoma of the prostate. Mod. Pathol. 17, 292-306 (2004).
3. Massie C. E, et al. The androgen receptor fuels prostate cancer by regulating central metabolism and biosynthesis. EMBO J. 30, 2719-2733 (2011).
4. Sharma N. L, et al. The androgen receptor induces a distinct transcriptional program in castration-resistant prostate cancer in man. Cancer Cell. 23, 35-47 (2013).
5. Mills I. G. Maintaining and reprogramming genomic androgen receptor activity in prostate cancer. Nat. Rev. Cancer. 14, 187-198 (2014).
6. Stray-Pedersen A, et al. PGM3 mutations cause a congenital disorder of glycosylation with severe immunodeficiency and skeletal dysplasia. Am. J. Hum. Genet. 95, 96-107 (2014).
7. Hakomori S. I, & Murakami W. T. Glycolipids of hamster fibroblasts and derived malignant-Transformed cell lines. Proc. Natl Acad. Sci. USA. 59, 254-261 (1968).
8. Ladenson R. P, Schwartz S. O, & Ivy A. C. Incidence of the blood groups and the secretor factor in patients with pernicious anemia and stomach carcinoma. Am. J. Med. Sci. 217, 194-197 (1949).
9. Hakomori S, & Kannagi R. Glycosphingolipids as tumor-Associated and differentiation markers. J. Natl Cancer Inst. 71, 231-251 (1983).
10. Johnson V. G, et Al. Analysis of A Human Tumor-Associated Glycoprotein (TAG 72) Identified by Monoclonal Antibody B72.3. Cancer Res. 46, 850-857 (1986).
11. Herlyn M, Sears H. F, Steplewski Z, & Koprowski H. Monoclonal antibody detection of a circulating tumor-Associated antigen. I. Presence of antigen in sera of patients with colorectal, gastric, and pancreatic carcinoma. J. Clin. Immunol. 2, 135-140 (1982).
12. Klug T. L, et al. Monoclonal antibody immunoradiometric assay for an antigenic determinant (CA 125) associated with human epithelial ovarian carcinomas. Cancer Res. 44, 1048-1053 (1984).
13. Munkley J, & Elliott D. J. Hallmarks of glycosylation in cancer. Oncotarget http://dx.doi.org/10.18632/.oncotarget.8155 (2016
14. Lilja H, Ulmert D, & Vickers A. J. Prostate-specific antigen and prostate cancer: prediction, detection and monitoring. Nat. Rev. Cancer. 8, 268-278 (2008).
15. Dhanasekaran S. M, et al. Delineation of prognostic biomarkers in prostate cancer. Nature. 412, 822-826 (2001).
16. Barry M. J. Prostate-specific-Antigen testing for early diagnosis of prostate cancer. N. Engl. J. Med. 344, 1373-1377 (2001).
17. Barry M. J. Screening for prostate cancer - The controversy that refuses to die. N. Engl. J. Med. 360, 1351-1354 (2009).
18. Gilgunn S, Conroy P. J, Saldova R, Rudd P. M, & OKennedy R. J. Aberrant PSA glycosylation - A sweet predictor of prostate cancer. Nat. Rev. Urol. 10, 99-107 (2013).
19. Drake R. R, Jones E, E, Powers T. W, & Nyalwidhe J. O. Chapter ten - Altered glycosylation in prostate cancer. Adv. Cancer Res. 126, 345-382 (2015).
20. Okada T, et al. Structural characteristics of the N glycans of two isoforms of prostate-specific antigens purified from human seminal fluid. Biochim. Biophys. Acta 1525, 149-160 (2001).
21. Prakash S, & Robbins P. W. Glycotyping of prostate specific antigen. Glycobiology. 10, 173-176 (2000).
22. Peracaula R, et al. Altered glycosylation pattern allows the distinction between prostate-specific antigen (PSA) from normal and tumor origins. Glycobiology. 13, 457-470 (2003).
23. White K. Y, et al. Glycomic characterization of prostate-specific antigen and prostatic acid phosphatase in prostate cancer and benign disease seminal plasma fluids. J. Proteome Res. 8, 620-630 (2009).
24. Tajiri M, Ohyama C, & Wada Y. Oligosaccharide profiles of the prostate specific antigen in free and complexed forms from the prostate cancer patient serum and in seminal plasma: a glycopeptide approach. Glycobiology. 18, 2-8 (2008).
25. Dwek M. V, Jenks A, & Leathem A. J. A sensitive assay to measure biomarker glycosylation demonstrates increased fucosylation of prostate specific antigen (PSA) in patients with prostate cancer compared with benign prostatic hyperplasia. Clin. Chim. Acta. 411, 1935-1939 (2010).
26. Fukushima K, Satoh T, Baba S, & Yamashita K. α1, 2 fucosylated and β N acetylgalactosaminylated prostate-specific antigen as an efficient marker of prostatic cancer. Glycobiology. 20, 452-460 (2010).
27. Sarrats A, et al. Differential percentage of serum prostate-specific antigen subforms suggests a new way to improve prostate cancer diagnosis. Prostate. 70, 1-9 (2010).
28. Sarrats A, et al. Glycan characterization of PSA 2 DE subforms from serum and seminal plasma. OMICS. 14, 465-474 (2010).
29. Ohyama C, et al. Carbohydrate structure and differential binding of prostate specific antigen to Maackia amurensis lectin between prostate cancer and benign prostate hypertrophy. Glycobiology. 14, 671-679 (2004).
30. Meany D. L, & Chan D. W. Aberrant glycosylation associated with enzymes as cancer biomarkers. Clin. Proteomics. 8, 7 (2011).
31. Chen Z, Gulzar Z. G, St Hill C. A, Walcheck B, & Brooks J. D. Increased expression of GCNT1 is associated with altered O glycosylation of PSA, PAP, and MUC1 in human prostate cancers. Prostate. 74, 1059-1067 (2014).
32. Leymarie N, et al. Interlaboratory study on differential analysis of protein glycosylation by mass spectrometry: the ABRF glycoprotein research multi-institutional study 2012. Mol. Cell. Proteomics. 12, 2935-2951 (2013).
33. Stura E. A, et al. Crystal structure of human prostate-specific antigen in a sandwich antibody complex. J. Mol. Biol. 414, 530-544 (2011).
34. Vanhooren V, et al. Serum N glycan profile shift during human ageing. Exp. Gerontol. 45, 738-743 (2010).
35. Yoshida K. I, et al. Serial lectin affinity chromatography with concavalin A and wheat germ agglutinin demonstrates altered asparagine-linked sugar-chain structures of prostatic acid phosphatase in human prostate carcinoma. J. Chromatogr. B Biomed. Sci. Appl. 695, 439-443 (1997).
36. Kudelka M. R, Ju T, Heimburg-Molinaro J, & Cummings R. D. Chapter three - imple sugars to complex disease - mucin-Type O glycans in cancer. Adv. Cancer Res. 126, 53-135 (2015).
37. Pinho S. S, & Reis C. A. Glycosylation in cancer: mechanisms and clinical implications. Nat. Rev. Cancer. 15, 540-555 (2015).
38. Radhakrishnan P, et al. Immature truncated O glycophenotype of cancer directly induces oncogenic features. Proc. Natl Acad. Sci. USA 111, E4066-E4075 (2014).
39. Kobayashi H, Terao T, & Kawashima Y. Sialyl Tn as a prognostic marker in epithelial ovarian cancer. Br. J. Cancer. 66, 984-985 (1992).
40. Kobayashi H, Terao T, & Kawashima Y. Serum sialyl Tn as an independent predictor of poor prognosis in patients with epithelial ovarian cancer. J. Clin. Oncol. 10, 95-101 (1992).
41. Soares R, Marinho A, & Schmitt F. Expression of sialyl Tn in breast cancer correlation with prognostic parameters. Pathol. Res. Pract. 192, 1181-1186 (1996).
42. Munkley J. The role of Sialyl Tn in cancer. Int. J. Mol. Sci. 17, 275 (2016).
43. Arai T, Fujita K, Fujime M, & Irimura T. Expression of sialylated MUC1 in prostate cancer: relationship to clinical stage and prognosis. Int. J. Urol. 12, 654-661 (2005).
44. Munkley J, et al. The androgen receptor controls expression of the cancer-Associated sTn antigen and cell adhesion through induction of ST6GalNAc1 in prostate cancer. Oncotarget. 6, 34358-34374 (2015).
45. Genega E. M, Hutchinson B, Reuter V. E, & Gaudin P. B. Immunophenotype of high-grade prostatic adenocarcinoma and urothelial carcinoma. Mod. Pathol. 13, 1186-1191 (2000).
46. Munkley J. The role of sialyl-Tn in cancer. Int. J. Mol. Sci. 17, E275 (2016).
47. Myers R. B, et al. Tumor associated glycoprotein 72 is highly expressed in prostatic adenocarcinomas. J. Urol. 152, 243-246 (1994).
48. Ozaki H, et al. Enhancement of metastatic ability by ectopic expression of ST6GalNAcI on a gastric cancer cell line in a mouse model. Clin. Exp. Metastasis. 29, 229-238 (2012).
49. Julien S, et al. ST6GalNAc I expression in MDA MB 231 breast cancer cells greatly modifies their O glycosylation pattern and enhances their tumourigenicity. Glycobiology. 16, 54-64 (2006).
50. Slovin S. F, et al. Fully synthetic carbohydrate-based vaccines in biochemically relapsed prostate cancer: clinical trial results with α N acetylgalactosamine-O serine/threonine conjugate vaccine. J. Clin. Oncol. 21, 4292-4298 (2003).
51. Amado M, Carneiro F, Seixas M, Clausen H, & Sobrinho-Simoes M. Dimeric sialyl Lex expression in gastric carcinoma correlates with venous invasion and poor outcome. Gastroenterology. 114, 462-470 (1998).
52. Baldus S. E, et al. Histopathological subtypes and prognosis of gastric cancer are correlated with the expression of mucin-Associated sialylated antigens: Sialosyl-Lewisa, Sialosyl-Lewisx and sialosyl Tn. Tumour Biol. 19, 445-453 (1998).
53. Walker P. D, Karnik S, deKernion J. B, & Pramberg J. C. Cell surface blood group antigens in prostatic carcinoma. Am. J. Clin. Pathol. 81, 503-506 (1984).
54. Culig Z, et al. Expression of Lewis carbohydrate antigens in metastatic lesions from human prostatic carcinoma. Prostate. 36, 162-167 (1998).
55. Jorgensen T, et al. Up regulation of the oligosaccharide sialyl Lewisx: a new prognostic parameter in metastatic prostate cancer. Cancer Res. 55, 1817-1819 (1995).
56. Martensson S, et al. Sialyl-Lewisx and related carbohydrate antigens in the prostate. Hum. Pathol. 26, 735-739 (1995).
57. Okamoto T, et al. Core2 O glycan-expressing prostate cancer cells are resistant to NK cell immunity. Mol. Med. Rep. 7, 359-364 (2013).
58. Carvalho A. S, et al. Differential expression of α 2, 3 sialyltransferases and α 1, 3/4 fucosyltransferases regulates the levels of sialyl Lewis a and sialyl Lewis x in gastrointestinal carcinoma cells. Int. J. Biochem. Cell Biol. 42, 80-89 (2010).
59. Saldova R, Fan Y, Fitzpatrick J. M, Watson R. W, & Rudd P. M. Core fucosylation and α2 3 sialylation in serum N glycome is significantly increased in prostate cancer comparing to benign prostate hyperplasia. Glycobiology. 21, 195-205 (2011).
60. Tabares G, et al. Different glycan structures in prostate-specific antigen from prostate cancer sera in relation to seminal plasma PSA. Glycobiology. 16, 132-145 (2006).
61. Kyselova Z, et al. Alterations in the serum glycome due to metastatic prostate cancer. J. Proteome Res. 6, 1822-1832 (2007).
62. Shah P, et al. Integrated proteomic and glycoproteomic analyses of prostate cancer cells reveal glycoprotein alteration in protein abundance and glycosylation. Mol. Cell. Proteomics. 14, 2753-2763 (2015).
63. Wang X, et al. Overexpression of α (1, 6) fucosyltransferase associated with aggressive prostate cancer. Glycobiology. 24, 935-944 (2014).
64. Barthel S. R, et al. Alpha 1, 3 fucosyltransferases are master regulators of prostate cancer cell trafficking. Proc. Natl Acad. Sci. USA. 106, 19491-19496 (2009).
65. Lange T, et al. Human prostate cancer in a clinically relevant xenograft mouse model: identification of β(1, 6)-branched oligosaccharides as a marker of tumor progression. Clin. Cancer Res. 18, 1364-1373 (2012).
66. Tsui K. H, et al. Evaluating the function of matriptase and N acetylglucosaminyltransferase V in prostate cancer metastasis. Anticancer Res. 28, 1993-1999 (2008).
67. Ishibashi Y, et al. Serum tri-And tetra-Antennary N glycan is a potential predictive biomarker for castration-resistant prostate cancer. Prostate. 74, 1521-1529 (2014).
68. Newsom-Davis T. E, et al. Enhanced immune recognition of cryptic glycan markers in human tumors. Cancer Res. 69, 2018-2025 (2009).
69. Wang D, et al. N-glycan cryptic antigens as active immunological targets in prostate cancer patients. J. Proteomics Bioinform. 5, 090-095 (2012).
70. Wang D, et al. Anti-oligomannose antibodies as potential serum biomarkers of aggressive prostate cancer. Drug Dev. Res. 74, 65-80 (2013).
71. Ravindranath M. H, et al. Gangliosides of organ-confined versus metastatic androgen-receptor-negative prostate cancer. Biochem. Biophys. Res. Commun. 324, 154-165 (2004).
72. Hatano K, et al. Androgen-regulated transcriptional control of sialyltransferases in prostate cancer cells. PLoS ONE 7, e31234 (2012).
73. Nonaka M, et al. Determination of carbohydrate structure recognized by prostate-specific F77 monoclonal antibody through expression analysis of glycosyltransferase genes. J. Biol. Chem. 289, 16478-16486 (2014).
74. Gao C, et al. Carbohydrate sequence of the prostate cancer-Associated antigen F77 assigned by a mucin O glycome designer array. J. Biol. Chem. 289, 16462-16477 (2014).
75. Carroll A. M, et al. Monoclonal antibodies to tissue-specific cell surface antigens. I. Characterization of an antibody to a prostate tissue antigen. Clin. Immunol. Immunopathol. 33, 268-281 (1984).
76. Zhang G, et al. Suppression of human prostate tumor growth by a unique prostate-specific monoclonal antibody F77 targeting a glycolipid marker. Proc. Natl Acad. Sci. USA. 107, 732-737 (2010).
77. Hagisawa S, et al. Expression of core 2 β1, 6 N acetylglucosaminyltransferase facilitates prostate cancer progression. Glycobiology. 15, 1016-1024 (2005).
78. Ricciardelli C, et al. Elevated stromal chondroitin sulfate glycosaminoglycan predicts progression in early-stage prostate cancer. Clin. Cancer Res. 3, 983-992 (1997).
79. Iozzo R. V, & Sanderson R. D. Proteoglycans in cancer biology, tumour microenvironment and angiogenesis. J. Cell. Mol. Med. 15, 1013-1031 (2011).
80. Afratis N, et al. Glycosaminoglycans: key players in cancer cell biology and treatment. FEBS J. 279, 1177-1197 (2012).
81. Edwards I. J. Proteoglycans in prostate cancer. Nat. Rev. Urol. 9, 196-206 (2012).
82. Suhovskih A. V, et al. Proteoglycan expression in normal human prostate tissue and prostate cancer. ISRN Oncol. 2013, 680136 (2013).
83. Henke A, et al. Stromal expression of decorin, Semaphorin6D, SPARC, Sprouty1 and Tsukushi in developing prostate and decreased levels of decorin in prostate cancer. PLoS ONE 7, e42516 (2012).
84. Hu Y, et al. Decorin suppresses prostate tumor growth through inhibition of epidermal growth factor and androgen receptor pathways. Neoplasia. 11, 1042-1053 (2009).
85. Datta M. W, et al. Perlecan, a candidate gene for the CAPB locus, regulates prostate cancer cell growth via the Sonic Hedgehog pathway. Mol. Cancer. 5, 9 (2006).
86. Ricciardelli C, et al. Elevated levels of versican but not decorin predict disease progression in early-stage prostate cancer. Clin. Cancer Res. 4, 963-971 (1998).
87. Touab M, Villena J, Barranco C, Arumi-Uria M, & Bassols A. Versican is differentially expressed in human melanoma and may play a role in tumor development. Am. J. Pathol. 160, 549-557 (2002).
88. Pukkila M, et al. High stromal versican expression predicts unfavourable outcome in oral squamous cell carcinoma. J. Clin. Pathol. 60, 267-272 (2007).
89. Skandalis S. S, Kletsas D, Kyriakopoulou D, Stavropoulos M, & Theocharis D. A. The greatly increased amounts of accumulated versican and decorin with specific post-Translational modifications may be closely associated with the malignant phenotype of pancreatic cancer. Biochim. Biophys. Acta 1760, 1217-1225 (2006).
90. Sakko A. J, et al. Immunohistochemical level of unsulfated chondroitin disaccharides in the cancer stroma is an independent predictor of prostate cancer relapse. Cancer Epidemiol. Biomarkers Prev. 17, 2488-2497 (2008).
91. Ricciardelli C, et al. Formation of hyaluronan-And versican-rich pericellular matrix by prostate cancer cells promotes cell motility. 282, 10814-10825 (2007).
92. Ricciardelli C, et al. Elevated levels of peritumoral chondroitin sulfate are predictive of poor prognosis in patients treated by radical prostatectomy for early-stage prostate cancer. Cancer Res. 59, 2324-2328 (1999).
93. Shimada K, et al. Syndecan 1 (CD138) contributes to prostate cancer progression by stabilizing tumour-initiating cells. J. Pathol. 231, 495-504 (2013).
94. Fujii T, et al. Syndecan 1 up regulates microRNA 331 3p and mediates epithelial-To mesenchymal transition in prostate cancer. Mol. Carcinog. http://dx.doi.org/10.1002/mc.22381 (2015).
95. Fujii T, Shimada K, Tatsumi Y, Fujimoto K, & Konishi N. Syndecan 1 responsive microRNA 126 and 149 regulate cell proliferation in prostate cancer. Biochem. Biophys. Res. Commun. 456, 183-189 (2015).
96. Love D. C, & Hanover J. A. The hexosamine signaling pathway: deciphering the O GlcNAc code. Sci. signal. 2005, re13 (2005).
97. Hanover J. A, Krause M. W, & Love D. C. Bittersweet memories: linking metabolism to epigenetics through O GlcNAcylation. Nat. Rev. Mol. Cell Biol. 13, 312-321 (2012).
98. Bond M. R, & Hanover J. A. A little sugar goes a long way: the cell biology of O GlcNAc. J. Cell Biol. 208, 869-880 (2015).
99. Butkinaree C, Park K, & Hart G. W. O linked β N acetylglucosamine (O GlcNAc): extensive crosstalk with phosphorylation to regulate signaling and transcription in response to nutrients and stress. Biochim. Biophys. Acta 1800, 96-106 (2010).
100. Schwarz F, & Aebi M. Mechanisms and principles of N linked protein glycosylation. Curr. Opin. Struct. Biol. 21, 576-582 (2011).
101. Itkonen H. M, et al. O GlcNAc transferase integrates metabolic pathways to regulate the stability of c MYC in human prostate cancer cells. Cancer Res. 73, 5277-5287 (2013).
102. Lynch T. P, et al. Critical role of O linked β N acetylglucosamine transferase in prostate cancer invasion, angiogenesis, and metastasis. J. Biol. Chem. 287, 11070-11081 (2012).
103. Kamigaito T, et al. Overexpression of O GlcNAc by prostate cancer cells is significantly associated with poor prognosis of patients. Prostate Cancer Prostatic Dis. 17, 18-22 (2014).
104. Itknonen H.M, et al. Inhibition of O-GlcNAc transferase activity reprograms prostate cancer cell metabolism. http://dx.doi.org/10.18632/oncotarget.7039 (2016).
105. Itkonen H. M, et al. UAP1 is overexpressed in prostate cancer and is protective against inhibitors of N linked glycosylation. Oncogene. 34, 3744-3750 (2014).
106. Barfeld S. J, East P, Zuber V, & Mills I. G. Meta-Analysis of prostate cancer gene expression data identifies a novel discriminatory signature enriched for glycosylating enzymes. BMC Med. Genom. 7, 513 (2014).
107. Itkonen H. M, & Mills I. G. N linked glycosylation supports cross-Talk between receptor tyrosine kinases and androgen receptor. PLoS ONE 8, e65016 (2013).
108. Mitchell B. S, & Schumacher U. The use of the lectin Helix pomatia agglutinin (HPA) as a prognostic indicator and as a tool in cancer research. Histol. Histopathol. 14, 217-226 (1999).
109. Laack E, et al. Lectin histochemistry of resected adenocarcinoma of the lung: helix pomatia agglutinin binding is an independent prognostic factor. Am. J. Pathol. 160, 1001-1008 (2002).
110. Kakeji Y, Tsujitani S, Mori M, Maehara Y, & Sugimachi K. Helix pomatia agglutinin binding activity is a predictor of survival time for patients with gastric carcinoma. Cancer. 68, 2438-2442 (1991).
111. Thies A, Moll I, Berger J, & Schumacher U. Lectin binding to cutaneous malignant melanoma: HPA is associated with metastasis formation. Br. J. Cancer. 84, 819-823 (2001).
112. Lange T, et al. Aberrant presentation of HPA-reactive carbohydrates implies selectin-independent metastasis formation in human prostate cancer. Clin. Cancer Res. 20, 1791-1802 (2014).
113. Powers T. W, et al. Matrix assisted laser desorption ionization imaging mass spectrometry workflow for spatial profiling analysis of N linked glycan expression in tissues. Anal. Chem. 85, 9799-9806 (2013).
114. Powers T. W, et al. MALDI imaging mass spectrometry profiling of N glycans in formalin-fixed paraffin embedded clinical tissue blocks and tissue microarrays. PLoS ONE 9, e106255 (2014).
115. Yoneyama T, et al. Measurement of aberrant glycosylation of prostate specific antigen can improve specificity in early detection of prostate cancer. Biochem. Biophys. Res. Commun. 448, 390-396 (2014).
116. Drake R. R, & Kislinger T. The proteomics of prostate cancer exosomes. Expert Rev. Proteomics. 11, 167-177 (2014).
117. Taniguchi N, & Kizuka Y. Chapter two - glycans and cancer: role of N glycans in cancer biomarker, progression and metastasis, and therapeutics. Adv. Cancer Res. 126, 11-51 (2015).
118. Rini J, Esko J, & Varki A, et al. Essentials of Glycobiology (eds Varki A. et al.) (2009).