Incipient renal transplant dysfunction associates with tubular syndecan-1 expression and shedding

American Journal of Physiology - Renal Physiology

Volumn 309, Issue 2, 2015, Pages F137-F145

  Adepu, Saritha ^a   Rosman, Colin W K ^a   Dam, Wendy ^a   van Dijk, Marcory C R F ^a   Navis, Gerjan ^a   van Goor, Harry ^a   Bakker, Stephan J L ^a   van den Born, Jacob ^a  

^a UNIVERSITY MEDICAL CENTER GRONINGEN   (Netherlands)

Author keywords

Kidney function; Renal biopsies; Renal transplantation; Syndecan 1; Vascular endothelial growth factor

Indexed keywords

CREATININE; KI 67 ANTIGEN; SYNDECAN 1; TUMOR NECROSIS FACTOR ALPHA CONVERTING ENZYME; UREA; VASCULOTROPIN A; ADAM PROTEIN; BIOLOGICAL MARKER; TUMOR NECROSIS FACTOR-ALPHA CONVERTASE; VEGFA PROTEIN, HUMAN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BLOOD VESSEL WALL; CONTROLLED STUDY; CREATININE BLOOD LEVEL; CREATININE CLEARANCE; ENDOTHELIUM CELL; ENZYME INDUCTION; FEMALE; GRAFT RECIPIENT; HUMAN; HUMAN CELL; HUMAN TISSUE; KIDNEY BIOPSY; KIDNEY FUNCTION; KIDNEY TRANSPLANTATION; MAJOR CLINICAL STUDY; MALE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN BLOOD LEVEL; PROTEIN EXPRESSION; PROTEIN INDUCTION, SYNTHESIS AND MODIFICATION; PROTEIN SHEDDING; RAT; TISSUE REGENERATION; TUBULAR DYSFUNCTION; UREA BLOOD LEVEL; ADULT; ADVERSE EFFECTS; AGED; ANIMAL; BLOOD; C57BL MOUSE; COHORT ANALYSIS; CROSS-SECTIONAL STUDY; KIDNEY TUBULE; METABOLISM; MIDDLE AGED; RENAL INSUFFICIENCY; WISTAR FURTH RAT;

ADAM PROTEINS; ADULT; AGED; ANIMALS; BIOLOGICAL MARKERS; COHORT STUDIES; CROSS-SECTIONAL STUDIES; FEMALE; HUMANS; KIDNEY TRANSPLANTATION; KIDNEY TUBULES; MALE; MICE, INBRED C57BL; MIDDLE AGED; RATS, INBRED WF; RENAL INSUFFICIENCY; SYNDECAN-1; VASCULAR ENDOTHELIAL GROWTH FACTOR A;

EID: 84937826711     PISSN: 1931857X     EISSN: 15221466     Source Type: Journal    
DOI: 10.1152/ajprenal.00127.2015     Document Type: Article

References (52)

1. Adamson RH. Permeability of frog mesenteric capillaries after partial pronase digestion of the endothelial glycocalyx. J Physiol 428: 1–13, 1990.
2. Adembri C, Sgambati E, Vitali L, Selmi V, Margheri M, Tani A, Bonaccini L, Nosi D, Caldini AL, Formigli L, De Gaudio AR. Sepsis induces albuminuria and alterations in the glomerular filtration barrier: a morphofunctional study in the rat. Crit Care 15: R277, 2011.
3. Adepu S, Katta K, Tietge UJ, Kwakernaak AJ, Dam W, van Goor H, Dullaart RP, Navis GJ, Bakker SJ, van den Born J. Hepatic syndecan-1 changes associate with dyslipidemia after renal transplantation. Am J Transplant 10: 2328–2338, 2014.
4. Annecke T, Fischer J, Hartmann H, Tschoep J, Rehm M, Conzen P, Sommerhoff CP, Becker BF. Shedding of the coronary endothelial glycocalyx: effects of hypoxia/reoxygenation vs ischaemia/reperfusion. Br J Anaesth 107: 679–686, 2011.
5. Beauvais DM, Rapraeger AC. Syndecan-1 couples the insulin-like growth factor-1 receptor to inside-out integrin activation. J Cell Sci 123: 3796–3807, 2010.
6. Bennett KL, Bradshaw J, Youngman T, Rodgers J, Greenfield B, Aruffo A, Linsley PS. Deleted in colorectal carcinoma (DCC) binds heparin via its fifth fibronectin type III domain. J Biol Chem 272: 26940–26946, 1997.
7. Bernfield M, Kokenyesi R, Kato M, Hinkes MT, Spring J, Gallo RL, Lose EJ. Biology of the syndecans: a family of transmembrane heparan sulfate proteoglycans. Annu Rev Cell Biol 8: 365–393, 1992.
8. Boersema M, Katta K, Rienstra H, Molema G, Nguyen TQ, Goldschmeding R, Navis G, van den Born J, Popa ER, Hillebrands JL. Local medial microenvironment directs phenotypic modulation of smooth muscle cells after experimental renal transplantation. Am J Transplant 12: 1429–1440, 2012.
9. Celie JW, Katta KK, Adepu S, Melenhorst WB, Reijmers RM, Slot EM, Beelen RH, Spaargaren M, Ploeg RJ, Navis G, van der Heide JJ, van Dijk MC, van Goor H, van den Born J. Tubular epithelial syndecan- 1 maintains renal function in murine ischemia/reperfusion and human transplantation. Kidney Int 81: 651–661, 2012.
10. Celie JW, Reijmers RM, Slot EM, Beelen RH, Spaargaren M, Ter Wee PM, Florquin S, van den Born J. Tubulointerstitial heparan sulfate proteoglycan changes in human renal diseases correlate with leukocyte influx and proteinuria. Am J Physiol Renal Physiol 294: F253–F263, 2008.
11. Chappell D, Jacob M, Paul O, Rehm M, Welsch U, Stoeckelhuber M, Conzen P, Becker BF. The glycocalyx of the human umbilical vein endothelial cell: an impressive structure ex vivo but not in culture. Circ Res 104: 1313–1317, 2009.
12. Derksen PW, Keehnen RM, Evers LM, van Oers MH, Spaargaren M, Pals ST. Cell surface proteoglycan syndecan-1 mediates hepatocyte growth factor binding and promotes Met signaling in multiple myeloma. Blood 99: 1405–1410, 2002.
13. Elenius K, Vainio S, Laato M, Salmivirta M, Thesleff I, Jalkanen M. Induced expression of syndecan in healing wounds. J Cell Biol 114: 585–595, 1991.
14. Fears CY, Woods A. The role of syndecans in disease and wound healing. Matrix Biol 25: 443–456, 2006.
15. Gotte M. Syndecans in inflammation. FASEB J 17: 575–591, 2003.
16. Hayashi K, Hayashi M, Jalkanen M, Firestone JH, Trelstad RL, Bernfield M. Immunocytochemistry of cell surface heparan sulfate pro-teoglycan in mouse tissues. A light and electron microscopic study. J Histochem Cytochem 35: 1079–1088, 1987.
17. Hayashida K, Johnston DR, Goldberger O, Park PW. Syndecan-1 expression in epithelial cells is induced by transforming growth factor beta through a PKA-dependent pathway. J Biol Chem 281: 24365–24374, 2006.
18. Henrich M, Gruss M, Weigand MA. Sepsis-induced degradation of endothelial glycocalix. Sci World J 10: 917–923, 2010.
19. Jaakkola P, Jalkanen M. Transcriptional regulation of Syndecan-1 expression by growth factors. Prog Nucleic Acid Res Mol Biol 63: 109–138, 1999.
20. Jaakkola P, Vihinen T, Jalkanen M. Proximal promoter-independent activation of the far-upstream FGF-inducible response element of syndecan-1 gene. Biochem Biophys Res Commun 278: 432–439, 2000.
21. Jalkanen M, Rapraeger A, Saunders S, Bernfield M. Cell surface proteoglycan of mouse mammary epithelial cells is shed by cleavage of its matrix-binding ectodomain from its membrane-associated domain. J Cell Biol 105: 3087–3096, 1987.
22. Katta K, Boersema M, Adepu S, Rienstra H, Celie JW, Mencke R, Molema G, van Goor H, Berden JH, Navis G, Hillebrands JL, van den Born J. Renal heparan sulfate proteoglycans modulate fibroblast growth factor 2 signaling in experimental chronic transplant dysfunction. Am J Pathol 183: 1571–1584, 2013.
23. Kiefer MC, Stephans JC, Crawford K, Okino K, Barr PJ. Ligandaffinity cloning and structure of a cell surface heparan sulfate proteoglycan that binds basic fibroblast growth factor. Proc Natl Acad Sci USA 87: 6985–6989, 1990.
24. Li Q, Park PW, Wilson CL, Parks WC. Matrilysin shedding of syndecan- 1 regulates chemokine mobilization and transepithelial efflux of neutrophils in acute lung injury. Cell 111: 635–646, 2002.
25. Liu Y. Renal fibrosis: new insights into the pathogenesis and therapeutics. Kidney Int 69: 213–217, 2006.
26. Loverre A, Ditonno P, Crovace A, Gesualdo L, Ranieri E, Pontrelli P, Stallone G, Infante B, Schena A, Di Paolo S, Capobianco C, Ursi M, Palazzo S, Battaglia M, Selvaggi FP, Schena FP, Grandaliano G. Ischemia-reperfusion induces glomerular and tubular activation of proinflammatory and antiapoptotic pathways: differential modulation by rapamycin. J Am Soc Nephrol 15: 2675–2686, 2004.
27. Mahtouk K, Jourdan M, De Vos J, Hertogh C, Fiol G, Jourdan E, Rossi JF, Klein B. An inhibitor of the EGF receptor family blocks myeloma cell growth factor activity of HB-EGF and potentiates dexamethasone or anti-IL-6 antibody-induced apoptosis. Blood 103: 1829–1837, 2004.
28. Manon-Jensen T, Itoh Y, Couchman JR. Proteoglycans in health and disease: the multiple roles of syndecan shedding. FEBS J 277: 3876–3889, 2010.
29. Manon-Jensen T, Multhaupt HA, Couchman JR. Mapping of matrix metalloproteinase cleavage sites on syndecan-1 and syndecan-4 ectodomains. FEBS J 280: 2320–2331, 2013.
30. Mulivor AW, Lipowsky HH. Role of glycocalyx in leukocyte-endothelial cell adhesion. Am J Physiol Heart Circ Physiol 283: H1282–H1291, 2002.
31. Mulivor AW, Lipowsky HH. Inflammation- and ischemia-induced shedding of venular glycocalyx. Am J Physiol Heart Circ Physiol 286: H1672–H1680, 2004.
32. Netelenbos T, Drager AM, van het Hof B, Kessler FL, Delouis C, Huijgens PC, van den Born J, van Dijk W. Differences in sulfation patterns of heparan sulfate derived from human bone marrow and umbilical vein endothelial cells. Exp Hematol 29: 884–893, 2001.
33. Nieuwdorp M, Meuwese MC, Vink H, Hoekstra JB, Kastelein JJ, Stroes ES. The endothelial glycocalyx: a potential barrier between health and vascular disease. Curr Opin Lipidol 16: 507–511, 2005.
34. Oksala O, Salo T, Tammi R, Häkkinen L, Jalkanen M, Inki P, Larjava H. Expression of proteoglycans and hyaluronan during wound healing. J Histochem Cytochem 43: 125–135, 1995.
35. Ostrowski SR, Johansson PI. Endothelial glycocalyx degradation induces endogenous heparinization in patients with severe injury and early traumatic coagulopathy. J Trauma Acute Care Surg 73: 60–66, 2012.
36. Pruessmeyer J, Martin C, Hess FM, Schwarz N, Schmidt S, Kogel T, Hoettecke N, Schmidt B, Sechi A, Uhlig S, Ludwig A. A disintegrin and metalloproteinase 17 (ADAM17) mediates inflammation-induced shedding of syndecan-1 and -4 by lung epithelial cells. J Biol Chem 285: 555–564, 2010.
37. Rehm M, Bruegger D, Christ F, Conzen P, Thiel M, Jacob M, Chappell D, Stoeckelhuber M, Welsch U, Reichart B, Peter K, Becker BF. Shedding of the endothelial glycocalyx in patients undergoing major vascular surgery with global and regional ischemia. Circulation 116: 1896–1906, 2007.
38. Reitsma S, Slaaf DW, Vink H, van Zandvoort MA, oude Egbrink MG. The endothelial glycocalyx: composition, functions, and visualization. Pflugers Arch 454: 345–359, 2007.
39. Rienstra H, Katta K, Celie JW, van Goor H, Navis G, van den Born J, Hillebrands JL. Differential expression of proteoglycans in tissue remodeling and lymphangiogenesis after experimental renal transplantation in rats. PLoS One 5: e9095, 2010.
40. Roskams T, Moshage H, De Vos R, Guido D, Yap P, Desmet V. Heparan sulfate proteoglycan expression in normal human liver. Hepatology 21: 950–958, 1995.
41. Sanderson RD, Lalor P, Bernfield M. B lymphocytes express and lose syndecan at specific stages of differentiation. Cell Regul 1: 27–35, 1989.
42. Seidel C, Ringden O, Remberger M. Increased levels of syndecan-1 in serum during acute graft-versus-host disease. Transplantation 76: 423–426, 2003.
43. Snoeijs MG, van Bijnen A, Swennen E, Haenen GR, Roberts LJ II, Christiaans MH, Peppelenbosch AG, Buurman WA, Ernest van Heurn LW. Tubular epithelial injury and inflammation after ischemia and reperfusion in human kidney transplantation. Ann Surg 253: 598–604, 2011.
44. Snoeijs MG, Vink H, Voesten N, Christiaans MH, Daemen JW, Peppelenbosch AG, Tordoir JH, Peutz-Kootstra CJ, Buurman WA, Schurink GW, van Heurn LW. Acute ischemic injury to the renal microvasculature in human kidney transplantation. Am J Physiol Renal Physiol 299: F1134–F1140, 2010.
45. Stanford KI, Bishop JR, Foley EM, Gonzales JC, Niesman IR, Witztum JL, Esko JD. Syndecan-1 is the primary heparan sulfate proteoglycan mediating hepatic clearance of triglyceride-rich lipoproteins in mice. J Clin Invest 119: 3236–3245, 2009.
46. Stein-Oakley AN, Tzanidis A, Fuller PJ, Jablonski P, Thomson NM. Expression and distribution of epidermal growth factor in acute and chronic renal allograft rejection. Kidney Int 46: 1207–1215, 1994.
47. Stepp MA, Daley WP, Bernstein AM, Pal-Ghosh S, Tadvalkar G, Shashurin A, Palsen S, Jurjus RA, Larsen M. Syndecan-1 regulates cell migration and fibronectin fibril assembly. Exp Cell Res 316: 2322–2339, 2010.
48. Svennevig K, Hoel T, Thiara A, Kolset S, Castelheim A, Mollnes T, Brosstad F, Fosse E, Svennevig J. Syndecan-1 plasma levels during coronary artery bypass surgery with and without cardiopulmonary bypass. Perfusion 23: 165–171, 2008.
49. Van Ree RM, Oterdoom LH, de Vries AP, Gansevoort RT, van der Heide JJ, van Son WJ, Ploeg RJ, de Jong PE, Gans RO, Bakker SJ. Elevated levels of C-reactive protein independently predict accelerated deterioration of graft function in renal transplant recipients. Nephrol Dial Transplant 22: 246–253, 2007.
50. Van Ree RM, de Vries AP, Oterdoom LH, Seelen MA, Gansevoort RT, Schouten JP, Struck J, Navis G, Gans RO, van der Heide JJ, van Son WJ, Bakker SJ. Plasma procalcitonin is an independent predictor of graft failure late after renal transplantation. Transplantation 88: 279–287, 2009.
51. Villanueva S, Cespedes C, Vio CP. Ischemic acute renal failure induces the expression of a wide range of nephrogenic proteins. Am J Physiol Regul Integr Comp Physiol 290: R861–R870, 2006.
52. Watanabe A, Mabuchi T, Satoh E, Furuya K, Zhang L, Maeda S, Naganuma H. Expression of syndecans, a heparan sulfate proteoglycan, in malignant gliomas: participation of nuclear factor-κB in upregulation of syndecan-1 expression. J Neurooncol 77: 25–32, 2006.