High glucose-induced intestinal epithelial barrier damage is aggravated by syndecan-1 destruction and heparanase overexpression

Journal of Cellular and Molecular Medicine

Volumn 19, Issue 6, 2015, Pages 1366-1374

  Qing, Qing ^a,b   Zhang, Shaoheng ^c   Chen, Ye ^d   Li, Runhua ^d   Mao, Hua ^c   Chen, Qikui ^a  

^a SUN YAT SEN UNIVERSITY   (China)

^b GUANGZHOU MEDICAL UNIVERSITY   (China)

^c SOUTHERN MEDICAL UNIVERSITY   (China)

^d SOUTHERN MEDICAL UNIVERSITY   (China)

Author keywords

Diabetes; Heparanase; High glucose; Intestinal epithelial barrier; Syndecan 1

Indexed keywords

ANTIDIABETIC AGENT; BETA GLUCURONIDASE; GLUCOSE; HEPARANASE; INSULIN; MITOGEN ACTIVATED PROTEIN KINASE P38; OCCLUDIN; PROTEIN ZO1; SYNDECAN 1;

ANIMAL; CELL LINE; CYTOLOGY; DRUG EFFECTS; EPITHELIUM CELL; EXPERIMENTAL DIABETES MELLITUS; FEMALE; FLUORESCENCE MICROSCOPY; GENE EXPRESSION; GENETICS; IMPEDANCE; INTESTINE; METABOLISM; MOUSE; PATHOPHYSIOLOGY; PHYSIOLOGY; RAT; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; WESTERN BLOTTING;

ANIMALS; BLOTTING, WESTERN; CELL LINE; DIABETES MELLITUS, EXPERIMENTAL; ELECTRIC IMPEDANCE; EPITHELIAL CELLS; FEMALE; GENE EXPRESSION; GLUCOSE; GLUCURONIDASE; HYPOGLYCEMIC AGENTS; INSULIN; INTESTINES; MICE; MICROSCOPY, FLUORESCENCE; OCCLUDIN; P38 MITOGEN-ACTIVATED PROTEIN KINASES; RATS; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; SYNDECAN-1; ZONULA OCCLUDENS-1 PROTEIN;

EID: 84929948673     PISSN: 15821838     EISSN: None     Source Type: Journal    
DOI: 10.1111/jcmm.12523     Document Type: Article

References (40)

1. WHO. 2013. Diabetes. Available at http://www.who.int/mediacentre/factsheets/fs312/en/ (accessed 29 July 2014).
2. Chan JC, Malik V, Jia W, et al. Diabetes in asia: epidemiology, risk factors, and pathophysiology. JAMA. 2009; 301: 2129-40.
3. de Kort S, Keszthelyi D, Masclee AA. Leaky gut and diabetes mellitus: what is the link? Obes Rev. 2011; 12: 449-58.
4. Zhao J, Frokjaer JB, Drewes AM, et al. Upper gastrointestinal sensory-motor dysfunction in diabetes mellitus. World J Gastroenterol. 2006; 12: 2846-57.
5. Rayner CK, Horowitz M. Gastrointestinal motility and glycemic control in diabetes: the chicken and the egg revisited? J Clin Invest. 2006; 116: 299-302.
6. Bernfield M, Gotte M, Park PW, et al. Functions of cell surface heparan sulfate proteoglycans. Annu Rev Biochem. 1999; 68: 729-77.
7. Bernfield M, Kokenyesi R, Kato M, et al. Biology of the syndecans: a family of transmembrane heparan sulfate proteoglycans. Annu Rev Cell Biol. 1992; 8: 365-93.
8. Varki A. Biological roles of oligosaccharides: all of the theories are correct. Glycobiology. 1993; 3: 97-130.
9. Manon-Jensen T, Itoh Y, Couchman JR. Proteoglycans in health and disease: the multiple roles of syndecan shedding. FEBS J. 2010; 277: 3876-89.
10. Vreys V, David G. Mammalian heparanase: what is the message? J Cell Mol Med. 2007; 11: 427-52.
11. Yang Y, Macleod V, Miao HQ, et al. Heparanase enhances syndecan-1 shedding: a novel mechanism for stimulation of tumor growth and metastasis. J Biol Chem. 2007; 282: 13326-33.
12. Bode L, Salvestrini C, Park PW, et al. Heparan sulfate and syndecan-1 are essential in maintaining murine and human intestinal epithelial barrier function. J Clin Invest. 2008; 118: 229-38.
13. Lerner I, Hermano E, Zcharia E, et al. Heparanase powers a chronic inflammatory circuit that promotes colitis-associated tumorigenesis in mice. J Clin Invest. 2011; 121: 1709-21.
14. Bode L, Murch S, Freeze HH. Heparan sulfate plays a central role in a dynamic in vitro model of protein-losing enteropathy. J Biol Chem. 2006; 281: 7809-15.
15. Henry-Stanley MJ, Hess DJ, Erlandsen SL, et al. Ability of the heparan sulfate proteoglycan syndecan-1 to participate in bacterial translocation across the intestinal epithelial barrier. Shock. 2005; 24: 571-6.
16. Wang Z, Gleichmann H. Glut2 in pancreatic islets: crucial target molecule in diabetes induced with multiple low doses of streptozotocin in mice. Diabetes. 1998; 47: 50-6.
17. Han J, Hiebert LM. Alteration of endothelial proteoglycan and heparanase gene expression by high glucose, insulin and heparin. Vascul Pharmacol. 2013; 59: 112-8.
18. Niederlechner S, Baird C, Petrie B, et al. Epidermal growth factor receptor expression and signaling are essential in glutamine's cytoprotective mechanism in heat-stressed intestinal epithelial-6 cells. Am J Physiol Gastrointest Liver Physiol. 2013; 304: G543-52.
19. Hu Y, Sun H, Owens RT, et al. Syndecan-1-dependent suppression of pdk1/akt/bad signaling by docosahexaenoic acid induces apoptosis in prostate cancer. Neoplasia. 2010; 12: 826-36.
20. Cao M, Jiang J, Du Y, et al. Mitochondria-targeted antioxidant attenuates high glucose-induced p38 mapk pathway activation in human neuroblastoma cells. Mol Med Rep. 2012; 5: 929-34.
21. Xu ZG, Kim KS, Park HC, et al. High glucose activates the p38 mapk pathway in cultured human peritoneal mesothelial cells. Kidney Int. 2003; 63: 958-68.
22. Fujiya M, Watari J, Ashida T, et al. Reduced expression of syndecan-1 affects metastatic potential and clinical outcome in patients with colorectal cancer. Jpn J Cancer Res. 2001; 92: 1074-81.
23. Li JP, Vlodavsky I. Heparin, heparan sulfate and heparanase in inflammatory reactions. Thromb Haemost. 2009; 102: 823-8.
24. Sanderson RD, Yang Y. Syndecan-1: a dynamic regulator of the myeloma microenvironment. Clin Exp Metastasis. 2008; 25: 149-59.
25. Deng L, Gui Z, Zhao L, et al. Diabetes mellitus and the incidence of colorectal cancer: an updated systematic review and meta-analysis. Dig Dis Sci. 2012; 57: 1576-85.
26. Goulet O, Kedinger M, Brousse N, et al. Intractable diarrhea of infancy with epithelial and basement membrane abnormalities. J Pediatr. 1995; 127: 212-9.
27. Karlsson-Lindahl L, Schmidt L, Haage D, et al. Heparanase affects food intake and regulates energy balance in mice. PLoS ONE. 2012; 7: e34313.
28. Reizes O, Lincecum J, Wang Z, et al. Transgenic expression of syndecan-1 uncovers a physiological control of feeding behavior by syndecan-3. Cell. 2001; 106: 105-16.
29. Deng Y, Foley EM, Gonzales JC, et al. Shedding of syndecan-1 from human hepatocytes alters very low density lipoprotein clearance. Hepatology. 2012; 55: 277-86.
30. Pei-Ling Chiu A, Wang F, Lal N, et al. Endothelial cells respond to hyperglycemia by increasing the lpl transporter gpihbp1. Am J Physiol Endocrinol Metab. 2014; 306: E1274-83.
31. Smith AJ, Schacker TW, Reilly CS, et al. A role for syndecan-1 and claudin-2 in microbial translocation during hiv-1 infection. J Acquir Immune Defic Syndr. 2010; 55: 306-15.
32. Lv ZM, Wang Q, Wan Q, et al. The role of the p38 mapk signaling pathway in high glucose-induced epithelial-mesenchymal transition of cultured human renal tubular epithelial cells. PLoS ONE. 2011; 6: e22806.
33. Bhowmick NA, Zent R, Ghiassi M, et al. Integrin beta 1 signaling is necessary for transforming growth factor-beta activation of p38mapk and epithelial plasticity. J Biol Chem. 2001; 276: 46707-13.
34. Liu X, Fang H, Chen H, et al. An artificial mirna against hpse suppresses melanoma invasion properties, correlating with a down-regulation of chemokines and mapk phosphorylation. PLoS ONE. 2012; 7: e38659.
35. Purushothaman A, Babitz SK, Sanderson RD. Heparanase enhances the insulin receptor signaling pathway to activate extracellular signal-regulated kinase in multiple myeloma. J Biol Chem. 2012; 287: 41288-96.
36. Zetser A, Bashenko Y, Edovitsky E, et al. Heparanase induces vascular endothelial growth factor expression: correlation with p38 phosphorylation levels and src activation. Cancer Res. 2006; 66: 1455-63.
37. Cui H, Shao C, Liu Q, et al. Heparanase enhances nerve-growth-factor-induced pc12 cell neuritogenesis via the p38 mapk pathway. Biochem J. 2011; 440: 273-82.
38. Chen B, Chen XP, Wu MS, et al. Expressions of heparanase and upstream stimulatory factor in hepatocellular carcinoma. Eur J Med Res. 2014; 19: 45.
39. Hiebert LM, Han J, Mandal AK. Glycosaminoglycans, hyperglycemia, and disease. Antioxid Redox Signal. 2014; 21: 1032-43.
40. Simeonovic CJ, Ziolkowski AF, Wu Z, et al. Heparanase and autoimmune diabetes. Front Immunol. 2013; 4: 471.