DOI QR코드

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Syndecan as a Messenger to Link Diabetes and Cancer

  • Kim, Sung-Jin (Department of Pharmacology and Toxicology, School of Dentistry, Kyung Hee University) ;
  • Raman, Os Sethu (Department of Pharmacology and Toxicology, School of Dentistry, Kyung Hee University)
  • 투고 : 2011.03.31
  • 심사 : 2011.05.19
  • 발행 : 2011.07.31

초록

Syndecans are membrane-anchored proteoglycans and implicated in the pathogenesis of cancer progression and metastasis. Syndecans also play important roles in interacting with growth factors, extracellular matrix and other cell surface molecules such as IGF-1 receptor. In the present review, we discuss about the syndecan structure, their role in signaling with other receptors, in addition to its general biology. The emerging roles of syndecans in the pathophysiology of human diseases, especially insulin resistance, diabetes and cancer is discussed.

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참고문헌

  1. Alexander, C. M., Reichsman, F., Hinkes, M. T., Lincecum, J., Becker, K. A., Cumberledge, S. and Bernfi eld, M. (2000) Syndecan-1 is required for Wnt-1-induced mammary tumorigenesis in mice. Nat. Genet. 25, 329-332. https://doi.org/10.1038/77108
  2. Alexopoulou, A. N., Multhaupt, H. A. and Couchman, J. R. (2007) Syndecans in wound healing, infl ammation and vascular biology. Int. J. Biochem. Cell Biol. 39, 505-528. https://doi.org/10.1016/j.biocel.2006.10.014
  3. Andrian, E., Grenier, D. and Rouabhia, M. (2005) Porphyromonas gingivalis lipopolysaccharide induces shedding of syndecan-1 expressed by gingival epithelial cells. J. Cell Physiol. 204, 178-183. https://doi.org/10.1002/jcp.20287
  4. Anttonen, A., Kajanti, M., Heikkila, P., Jalkanen, M. and Joensuu, H. (1999) Syndecan-1 expression has prognostic signifi cance in head and neck carcinoma. Br. J. Cancer 79, 558-564. https://doi.org/10.1038/sj.bjc.6690088
  5. Barbareschi, M., Maisonneuve, P., Aldovini, D., Cangi, M. G., Pecciarini, L., Angelo Mauri, F., Veronese, S., Caffo, O., Lucenti, A., Palma, P. D., Galligioni, E. and Doglioni, C. (2003) High syndecan-1 expression in breast carcinoma is related to an aggressive phenotype and to poorer prognosis. Cancer 98, 474-483. https://doi.org/10.1002/cncr.11515
  6. Bayer-Garner, I., Dilday, B., Sanderson, R. and Smoller, B. (2001) Acantholysis and spongiosis are associated with loss of syndecan-1 expression. J. Cutan. Pathol. 28, 135-139. https://doi.org/10.1034/j.1600-0560.2001.028003135.x
  7. Beauvais, D. M. and Rapraeger, A. C. (2004) Syndecans in tumor cell adhesion and signaling. Reprod. Biol. Endocrinol. 2, 3. https://doi.org/10.1186/1477-7827-2-3
  8. Beauvais, D. M. and Rapraeger, A. C. (2010) Syndecan-1 couples the insulin-like growth factor-1 receptor to inside-out integrin activation. J. Cell Sci. 123, 3796-3807. https://doi.org/10.1242/jcs.067645
  9. Bernfi eld, M., Gotte, M., Park, P. W., Reizes, O., Fitzgerald, M. L., Lincecum, J. and Zako, M. (1999) Functions of cell surface heparan sulfate proteoglycans. Annu. Rev. Biochem. 68, 729-777. https://doi.org/10.1146/annurev.biochem.68.1.729
  10. Berster, J. M. and Goke, B. (2008) Type 2 diabetes mellitus as risk factor for colorectal cancer. Arch. Physiol. Biochem. 114, 84-98. https://doi.org/10.1080/13813450802008455
  11. Brockstedt, U., Dobra, K., Nurminen, M. and Hjerpe, A. (2002) Immunoreactivity to cell surface syndecans in cytoplasm and nucleus: tubulin-dependent rearrangements. Exp. Cell Res. 274, 235-245. https://doi.org/10.1006/excr.2002.5477
  12. Burbach, B. J., Friedl, A., Mundhenke, C. and Rapraeger, A. C. (2003) Syndecan-1 accumulates in lysosomes of poorly differentiated breast carcinoma cells. Matrix Biol. 22, 163-177. https://doi.org/10.1016/S0945-053X(03)00009-X
  13. Calle, E. E. and Kaaks, R. (2004) Overweight, obesity and cancer: epidemiological evidence and proposed mechanisms. Nat. Rev. Cancer 4, 579-591. https://doi.org/10.1038/nrc1408
  14. Chan, J. M., Stampfer, M. J., Giovannucci, E., Gann, P. H., Ma, J., Wilkinson, P., Hennekens, C. H. and Pollak, M. (1998) Plasma insulin-like growth factor-I and prostate cancer risk: a prospective study. Science 279, 563-566. https://doi.org/10.1126/science.279.5350.563
  15. Chen, L. and Sanderson, R. D. (2009) Heparanase regulates levels of syndecan-1 in the nucleus. PLoS One 4, e4947. https://doi.org/10.1371/journal.pone.0004947
  16. Chung, Y. W., Han, D. S., Park, K. H., Eun, C. S., Yoo, K. S. and Park, C. K. (2008) Insulin therapy and colorectal adenoma risk among patients with Type 2 diabetes mellitus: a case-control study in Korea. Dis. Colon Rectum 51, 593-597. https://doi.org/10.1007/s10350-007-9184-1
  17. Cohen, A. R., Woods, D. F., Marfatia, S. M., Walther, Z., Chishti, A. H. and Anderson, J. M. (1998) Human CASK/LIN-2 binds syndecan-2 and protein 4.1 and localizes to the basolateral membrane of epithelial cells. J. Cell Biol. 142, 129-138. https://doi.org/10.1083/jcb.142.1.129
  18. Conejo, J. R., Kleeff, J., Koliopanos, A., Matsuda, K., Zhu, Z. W., Goecke, H., Bicheng, N., Zimmermann, A., Korc, M., Friess, H. and Buchler, M. W. (2000) Syndecan-1 expression is up-regulated in pancreatic but not in other gastrointestinal cancers. Int. J. Cancer 88, 12-20. https://doi.org/10.1002/1097-0215(20001001)88:1<12::AID-IJC3>3.0.CO;2-T
  19. Couchman, J. R. (2003) Syndecans: proteoglycan regulators of cellsurface microdomains? Nat. Rev. Mol. Cell Biol. 4, 926-937. https://doi.org/10.1038/nrm1257
  20. Couchman, J. R., Chen, L. and Woods, A. (2001) Syndecans and cell adhesion. Int. Rev. Cytol. 207, 113-150. https://doi.org/10.1016/S0074-7696(01)07004-8
  21. Cowey, S. and Hardy, R. W. (2006) The metabolic syndrome: A highrisk state for cancer? Am. J. Pathol. 169, 1505-1522. https://doi.org/10.2353/ajpath.2006.051090
  22. Dobra, K., Nurminen, M. and Hjerpe, A. (2003) Growth factors regulate the expression profi le of their syndecan co-receptors and the differentiation of mesothelioma cells. Anticancer Res. 23, 2435-2444.
  23. Elenius, V., Gotte, M., Reizes, O., Elenius, K. and Bernfi eld, M. (2004) Inhibition by the soluble syndecan-1 ectodomains delays wound repair in mice overexpressing syndecan-1. J. Biol. Chem. 279, 41928-41935. https://doi.org/10.1074/jbc.M404506200
  24. Endo, K., Takino, T., Miyamori, H., Kinsen, H., Yoshizaki, T., Furukawa, M. and Sato, H. (2003) Cleavage of syndecan-1 by membrane type matrix metalloproteinase-1 stimulates cell migration. J. Biol. Chem. 278, 40764-40770. https://doi.org/10.1074/jbc.M306736200
  25. Ethell, I. M., Hagihara, K., Miura, Y., Irie, F. and Yamaguchi, Y. (2000) Synbindin, A novel syndecan-2-binding protein in neuronal dendritic spines. J. Cell Biol. 151, 53-68. https://doi.org/10.1083/jcb.151.1.53
  26. Fanning, A. S. and Anderson, J. M. (1996) Protein-protein interactions: PDZ domain networks. Curr. Biol. 6, 1385-1388. https://doi.org/10.1016/S0960-9822(96)00737-3
  27. Fears, C. Y. and Woods, A. (2006) The role of syndecans in disease and wound healing. Matrix Biol. 25, 443-456. https://doi.org/10.1016/j.matbio.2006.07.003
  28. Fedarko, N. S., Ishihara, M. and Conrad, H. E. (1989) Control of cell division in hepatoma cells by exogenous heparan sulfate proteoglycan. J. Cell Physiol. 139, 287-294. https://doi.org/10.1002/jcp.1041390210
  29. Flood, A., Mai, V., Pfeiffer, R., Kahle, L., Remaley, A. T., Lanza, E. and Schatzkin, A. (2007) Elevated serum concentrations of insulin and glucose increase risk of recurrent colorectal adenomas. Gastroenterology 133, 1423-1429. https://doi.org/10.1053/j.gastro.2007.08.040
  30. Fornoni, A., Ijaz, A., Tejada, T. and Lenz, O. (2008) Role of infl ammation in diabetic nephropathy. Curr. Diabetes Rev. 4, 10-17. https://doi.org/10.2174/157339908783502361
  31. Frayling, T. M., Colhoun, H. and Florez, J. C. (2008) A genetic link between type 2 diabetes and prostate cancer. Diabetologia 51, 1757-1760. https://doi.org/10.1007/s00125-008-1114-9
  32. Fujiya, M., Watari, J., Ashida, T., Honda, M., Tanabe, H., Fujiki, T., Saitoh, Y. and Kohgo, Y. (2001) Reduced expression of syndecan-1 affects metastatic potential and clinical outcome in patients with colorectal cancer. Jpn. J. Cancer Res. 92, 1074-1081. https://doi.org/10.1111/j.1349-7006.2001.tb01062.x
  33. Gao, Y., Li, M., Chen, W. and Simons, M. (2000) Synectin, syndecan-4 cytoplasmic domain binding PDZ protein, inhibits cell migration. J. Cell Physiol. 184, 373-379. https://doi.org/10.1002/1097-4652(200009)184:3<373::AID-JCP12>3.0.CO;2-I
  34. Giovannucci, E., Rimm, E. B., Liu, Y. and Willett, W. C. (2004) Height, predictors of C-peptide and cancer risk in men. Int. J. Epidemiol. 33, 217-225. https://doi.org/10.1093/ije/dyh020
  35. Granes, F., Urena, J. M., Rocamora, N. and Vilaro, S. (2000) Ezrin links syndecan-2 to the cytoskeleton. J. Cell Sci. 113(Pt 7), 1267-1276.
  36. Grootjans, J. J., Zimmermann, P., Reekmans, G., Smets, A., Degeest, G., Durr, J. and David, G. (1997) Syntenin, a PDZ protein that binds syndecan cytoplasmic domains. Proc. Natl. Acad. Sci. U S A 94, 13683-13688. https://doi.org/10.1073/pnas.94.25.13683
  37. Gunter, M. J., Hoover, D. R., Yu, H., Wassertheil-Smoller, S., Manson, J. E., Li, J., Harris, T. G., Rohan, T. E., Xue, X., Ho, G. Y., Einstein, M. H., Kaplan, R. C., Burk, R. D., Wylie-Rosett, J., Pollak, M. N., Anderson, G., Howard, B. V. and Strickler, H. D. (2008) A prospective evaluation of insulin and insulin-like growth factor-I as risk factors for endometrial cancer. Cancer Epidemiol. Biomarkers Prev. 17, 921-929. https://doi.org/10.1158/1055-9965.EPI-07-2686
  38. Harman, S. M., Metter, E. J., Blackman, M. R., Landis, P. K. and Carter, H. B. (2000) Serum levels of insulin-like growth factor I (IGFI), IGF-II, IGF-binding protein-3, and prostate-specifi c antigen as predictors of clinical prostate cancer. J. Clin. Endocrinol. Metab. 85, 4258-4265. https://doi.org/10.1210/jc.85.11.4258
  39. Hirabayashi, K., Numa, F., Suminami, Y., Murakami, A., Murakami, T. and Kato, H. (1998) Altered proliferative and metastatic potential associated with increased expression of syndecan-1. Tumour Biol. 19, 454-463. https://doi.org/10.1159/000030037
  40. Hoeben, A., Landuyt, B., Highley, M. S., Wildiers, H., Van Oosterom, A. T. and De Bruijn, E. A. (2004) Vascular endothelial growth factor and angiogenesis. Pharmacol. Rev. 56, 549-580. https://doi.org/10.1124/pr.56.4.3
  41. Hsia, E., Richardson, T. P. and Nugent, M. A. (2003) Nuclear localization of basic fi broblast growth factor is mediated by heparan sulfate proteoglycans through protein kinase C signaling. J. Cell. Biochem. 88, 1214-1225. https://doi.org/10.1002/jcb.10470
  42. Ibrahim, Y. H. and Yee, D. (2004) Insulin-like growth factor-I and cancer risk. Growth Horm. IGF Res. 14, 261-269. https://doi.org/10.1016/j.ghir.2004.01.005
  43. Inki, P. and Jalkanen, M. (1996) The role of syndecan-1 in malignancies. Ann. Med. 28, 63-67. https://doi.org/10.3109/07853899608999076
  44. Inki, P., Joensuu, H., Grenman, R., Klemi, P. and Jalkanen, M. (1994a) Association between syndecan-1 expression and clinical outcome in squamous cell carcinoma of the head and neck. Br. J. Cancer 70, 319-323. https://doi.org/10.1038/bjc.1994.300
  45. Inki, P., Stenback, F., Grenman, S. and Jalkanen, M. (1994b) Immunohistochemical localization of syndecan-1 in normal and pathological human uterine cervix. J. Pathol. 172, 349-355. https://doi.org/10.1002/path.1711720410
  46. Kaaks, R., Lukanova, A., Rinaldi, S., Biessy, C., Soderberg, S., Olsson, T., Stenman, U. H., Riboli, E., Hallmans, G. and Stattin, P. (2003) Interrelationships between plasma testosterone, SHBG, IGF-I, insulin and leptin in prostate cancer cases and controls. Eur. J. Cancer Prev. 12, 309-315. https://doi.org/10.1097/00008469-200308000-00011
  47. Klatka, J. (2002) Syndecan-1 expression in laryngeal cancer. Eur. Arch. Otorhinolaryngol. 259, 115-118. https://doi.org/10.1007/s00405-001-0429-7
  48. Kotsovilis, S., Tseleni-Balafouta, S., Charonis, A., Fourmousis, I., Nikolidakis, D. and Vrotsos, J. A. (2010) Syndecan-1 immunohistochemical expression in gingival tissues of chronic periodontitis patients correlated with various putative factors. J. Periodontal Res. 45, 520-531.
  49. Kovalszky, I., Dudas, J., Olah-Nagy, J., Pogany, G., Tovary, J., Timar, J., Kopper, L., Jeney, A. and Iozzo, R. V. (1998) Inhibition of DNA topoisomerase I activity by heparan sulfate and modulation by basic fi broblast growth factor. Mol. Cell Biochem. 183, 11-23. https://doi.org/10.1023/A:1006898920637
  50. Kumar-Singh, S., Jacobs, W., Dhaene, K., Weyn, B., Bogers, J., Weyler, J. and Van Marck, E. (1998) Syndecan-1 expression in malignant mesothelioma: correlation with cell differentiation, WT1 expression, and clinical outcome. J. Pathol. 186, 300-305. https://doi.org/10.1002/(SICI)1096-9896(1998110)186:3<300::AID-PATH180>3.0.CO;2-Q
  51. Levy, P., Munier, A., Baron-Delage, S., Chastre, E., Gespach, C., Capeau, J. and Cherqui, G. (1997) [Oncogenic activation of p21ras or pp60c-src in human colonic Caco-2 cells induces post-translation alterations of syndecan-1]. Bull. Cancer 84, 235-237.
  52. Levy, P., Munier, A., Baron-Delage, S., Di Gioia, Y., Gespach, C., Capeau, J. and Cherqui, G. (1996) Syndecan-1 alterations during the tumorigenic progression of human colonic Caco-2 cells induced by human Ha-ras or polyoma middle T oncogenes. Br. J. Cancer 74, 423-431. https://doi.org/10.1038/bjc.1996.376
  53. Li, Q., Park, P. W., Wilson, C. L. and Parks, W. C. (2002) Matrilysin shedding of syndecan-1 regulates chemokine mobilization and transepithelial effl ux of neutrophils in acute lung injury. Cell 111, 635-646. https://doi.org/10.1016/S0092-8674(02)01079-6
  54. Matsumoto, A., Ono, M., Fujimoto, Y., Gallo, R. L., Bernfi eld, M. and Kohgo, Y. (1997) Reduced expression of syndecan-1 in human hepatocellular carcinoma with high metastatic potential. Int. J. Cancer 74, 482-491. https://doi.org/10.1002/(SICI)1097-0215(19971021)74:5<482::AID-IJC2>3.0.CO;2-#
  55. Monroy, A., Kamath, S., Chavez, A. O., Centonze, V. E., Veerasamy, M., Barrentine, A., Wewer, J. J., Coletta, D. K., Jenkinson, C., Jhingan, R. M., Smokler, D., Reyna, S., Musi, N., Khokka, R., Federici, M., Tripathy, D., DeFronzo, R. A. and Folli, F. (2009) Impaired regulation of the TNF-alpha converting enzyme/tissue inhibitor of metalloproteinase 3 proteolytic system in skeletal muscle of obese type 2 diabetic patients: a new mechanism of insulin resistance in humans. Diabetologia 52, 2169-2181. https://doi.org/10.1007/s00125-009-1451-3
  56. Nackaerts, K., Verbeken, E., Deneffe, G., Vanderschueren, B., Demedts, M. and David, G. (1997) Heparan sulfate proteoglycan expression in human lung-cancer cells. Int. J. Cancer 74, 335-345. https://doi.org/10.1002/(SICI)1097-0215(19970620)74:3<335::AID-IJC18>3.0.CO;2-A
  57. Nakanishi, K., Yoshioka, N., Oka, K. and Hakura, A. (1999) Reduction of syndecan-1 mRNA in cervical-carcinoma cells is involved with the 3' untranslated region. Int. J. Cancer 80, 527-532. https://doi.org/10.1002/(SICI)1097-0215(19990209)80:4<527::AID-IJC8>3.0.CO;2-Y
  58. Numa, F., Hirabayashi, K., Kawasaki, K., Sakaguchi, Y., Sugino, N., Suehiro, Y., Suminami, Y., Hirakawa, H., Umayahara, K., Nawata, S., Ogata, H. and Kato, H. (2002) Syndecan-1 expression in cancer of the uterine cervix: association with lymph node metastasis. Int. J. Oncol. 20, 39-43.
  59. Perrimon, N. and Bernfi eld, M. (2001) Cellular functions of proteoglycans-- an overview. Semin. Cell Dev. Biol. 12, 65-67. https://doi.org/10.1006/scdb.2000.0237
  60. Pulkkinen, J. O., Penttinen, M., Jalkanen, M., Klemi, P. and Grenman, R. (1997) Syndecan-1: a new prognostic marker in laryngeal cancer. Acta Otolaryngol. 117, 312-315. https://doi.org/10.3109/00016489709117794
  61. Purushothaman, A., Chen, L., Yang, Y. and Sanderson, R. D. (2008) Heparanase stimulation of protease expression implicates it as a master regulator of the aggressive tumor phenotype in myeloma. J. Biol. Chem. 283, 32628-32636. https://doi.org/10.1074/jbc.M806266200
  62. Reizes, O., Goldberger, O., Smith, A. C., Xu, Z., Bernfi eld, M. and Bickel, P. E. (2006) Insulin promotes shedding of syndecan ectodomains from 3T3-L1 adipocytes: a proposed mechanism for stabilization of extracellular lipoprotein lipase. Biochemistry 45, 5703-5711. https://doi.org/10.1021/bi052263h
  63. Rintala, M., Inki, P., Klemi, P., Jalkanen, M. and Grenman, S. (1999) Association of syndecan-1 with tumor grade and histology in primary invasive cervical carcinoma. Gynecol. Oncol. 75, 372-378. https://doi.org/10.1006/gyno.1999.5595
  64. Sanderson, R. D. (2001) Heparan sulfate proteoglycans in invasion and metastasis. Semin. Cell Dev. Biol. 12, 89-98. https://doi.org/10.1006/scdb.2000.0241
  65. Sanderson, R. D. and Borset, M. (2002) Syndecan-1 in B lymphoid malignancies. Ann. Hematol. 81, 125-135. https://doi.org/10.1007/s00277-002-0437-8
  66. Smith, M. R., Lee, H. and Nathan, D. M. (2006) Insulin sensitivity during combined androgen blockade for prostate cancer. J. Clin. Endocrinol. Metab. 91, 1305-1308. https://doi.org/10.1210/jc.2005-2507
  67. Songyang, Z., Fanning, A. S., Fu, C., Xu, J., Marfatia, S. M., Chishti, A. H., Crompton, A., Chan, A. C., Anderson, J. M. and Cantley, L. C. (1997) Recognition of unique carboxyl-terminal motifs by distinct PDZ domains. Science 275, 73-77. https://doi.org/10.1126/science.275.5296.73
  68. Soukka, T., Pohjola, J., Inki, P. and Happonen, R. P. (2000) Reduction of syndecan-1 expression is associated with dysplastic oral epithelium. J. Oral Pathol. Med. 29, 308-313. https://doi.org/10.1034/j.1600-0714.2000.290704.x
  69. Stanley, M. J., Stanley, M. W., Sanderson, R. D. and Zera, R. (1999) Syndecan-1 expression is induced in the stroma of infi ltrating breast carcinoma. Am. J. Clin. Pathol. 112, 377-383. https://doi.org/10.1093/ajcp/112.3.377
  70. Steinfeld, R., Van Den Berghe, H. and David, G. (1996) Stimulation of fi broblast growth factor receptor-1 occupancy and signaling by cell surface-associated syndecans and glypican. J. Cell Biol. 133, 405-416. https://doi.org/10.1083/jcb.133.2.405
  71. Sun, D., McAlmon, K. R., Davies, J. A., Bernfi eld, M. and Hay, E. D. (1998) Simultaneous loss of expression of syndecan-1 and E-cadherin in the embryonic palate during epithelial-mesenchymal transformation. Int. J. Dev. Biol. 42, 733-736.
  72. Tkachenko, E., Rhodes, J. M. and Simons, M. (2005) Syndecans: new kids on the signaling block. Circ. Res. 96, 488-500. https://doi.org/10.1161/01.RES.0000159708.71142.c8
  73. Verheus, M., Peeters, P. H., Rinaldi, S., Dossus, L., Biessy, C., Olsen, A., Tjonneland, A., Overvad, K., Jeppesen, M., Clavel-Chapelon, F., Tehard, B., Nagel, G., Linseisen, J., Boeing, H., Lahmann, P. H., Arvaniti, A., Psaltopoulou, T., Trichopoulou, A., Palli, D., Tumino, R., Panico, S., Sacerdote, C., Sieri, S., van Gils, C. H., Bueno-de- Mesquita, B. H., Gonzalez, C. A., Ardanaz, E., Larranaga, N., Garcia, C. M., Navarro, C., Quiros, J. R., Key, T., Allen, N., Bingham, S., Khaw, K. T., Slimani, N., Riboli, E. and Kaaks, R. (2006) Serum C-peptide levels and breast cancer risk: results from the European Prospective Investigation into Cancer and Nutrition (EPIC). Int. J. Cancer 119, 659-667. https://doi.org/10.1002/ijc.21861
  74. Wang, Z., Telci, D. and Griffi n, M. (2011) Importance of syndecan-4 and syndecan -2 in osteoblast cell adhesion and survival mediated by a tissue transglutaminase-fi bronectin complex. Exp. Cell Res. 317, 367-381. https://doi.org/10.1016/j.yexcr.2010.10.015
  75. Wiksten, J. P., Lundin, J., Nordling, S., Lundin, M., Kokkola, A., von Boguslawski, K. and Haglund, C. (2001) Epithelial and stromal syndecan- 1 expression as predictor of outcome in patients with gastric cancer. Int. J. Cancer 95, 1-6. https://doi.org/10.1002/1097-0215(20010120)95:1<1::AID-IJC1000>3.0.CO;2-5
  76. Woods, A. (2001) Syndecans: transmembrane modulators of adhesion and matrix assembly. J. Clin. Invest. 107, 935-941. https://doi.org/10.1172/JCI12802
  77. Yang, Y., Macleod, V., Miao, H. Q., Theus, A., Zhan, F., Shaughnessy, J. D., Jr., Sawyer, J., Li, J. P., Zcharia, E., Vlodavsky, I. and Sanderson, R. D. (2007) Heparanase enhances syndecan-1 shedding: a novel mechanism for stimulation of tumor growth and metastasis. J. Biol. Chem. 282, 13326-13333. https://doi.org/10.1074/jbc.M611259200
  78. Yang, Y. X., Hennessy, S. and Lewis, J. D. (2004) Insulin therapy and colorectal cancer risk among type 2 diabetes mellitus patients. Gastroenterology 127, 1044-1050. https://doi.org/10.1053/j.gastro.2004.07.011
  79. Yang, Y. X., Hennessy, S. and Lewis, J. D. (2005) Type 2 diabetes mellitus and the risk of colorectal cancer. Clin. Gastroenterol. Hepatol. 3, 587-594. https://doi.org/10.1016/S1542-3565(05)00152-7
  80. Zendehdel, K., Nyren, O., Ostenson, C. G., Adami, H. O., Ekbom, A. and Ye, W. (2003) Cancer incidence in patients with type 1 diabetes mellitus: a population-based cohort study in Sweden. J. Natl. Cancer Inst. 95, 1797-1800. https://doi.org/10.1093/jnci/djg105

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