CD44v3-v10 reduces the profibrotic effects of TGF-β1 and attenuates tubular injury in the early stage of chronic obstructive nephropathy

American Journal of Physiology - Renal Physiology

Volumn 305, Issue 10, 2013, Pages

  Rampanelli, Elena ^a   Rouschop, Kasper ^b   Teske, Gwendoline J D ^a   Claessen, Nike ^a   Leemans, Jaklien C ^a   Florquin, Sandrine ^a,c  

^a UNIVERSITY OF AMSTERDAM   (Netherlands)

^b MAASTRICHT UNIVERSITY MEDICAL CENTER   (Netherlands)

^c RADBOUD UNIVERSITY NIJMEGEN   (Netherlands)

Author keywords

CD44; Fibrosis; TGF 1; Tubules; UUO

Indexed keywords

CD44V ANTIGEN; CD44V3-V10 ANTIGEN; OSTEOGENIC PROTEIN 1; SCATTER FACTOR; TRANSFORMING GROWTH FACTOR BETA1; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BIOACCUMULATION; CHRONIC OBSTRUCTIVE NEPHROPATHY; CONTROLLED STUDY; DOWN REGULATION; KIDNEY DISEASE; KIDNEY FIBROSIS; KIDNEY PROXIMAL TUBULE; KIDNEY TUBULE CELL; KIDNEY TUBULE DAMAGE; MALE; MOUSE; MYOFIBROBLAST; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; PROTEIN SYNTHESIS; RENAL PROTECTION; SIGNAL TRANSDUCTION; TRANSGENIC MOUSE; URETER OBSTRUCTION; WILD TYPE;

EID: 84887604558     PISSN: 1931857X     EISSN: 15221466     Source Type: Journal    
DOI: 10.1152/ajprenal.00340.2013     Document Type: Article

References (65)

1. Asselman M, Verhulst A, Van Ballegooijen ES, Bangma CH, Verkoelen CF, De Broe ME. Hyaluronan is apically secreted and expressed by proliferating or regenerating renal tubular cells. Kidney Int 68: 71-83, 2005.
2. Becker GJ, Hewitson TD. The role of tubulointerstitial injury in chronic renal failure. Curr Opin Nephrol Hypertens 9: 133-138, 2000.
3. Bennett KL, Jackson DG, Simon JC, Tanczos E, Peach R, Modrell B, Stamenkovic I, Plowman G, Aruffo A. CD44 isoforms containing exon V3 are responsible for the presentation of heparin-binding growth factor. J Cell Biol 128: 687-698, 1995.
4. Benz PS, Fan X, Wuthrich RP. Enhanced tubular epithelial CD44 expression in MRL-lpr lupus nephritis. Kidney Int 50: 156-163, 1996.
5. Bourguignon LY, Singleton PA, Zhu H, Zhou B. Hyaluronan promotes signaling interaction between CD44 and the transforming growth factor beta receptor I in metastatic breast tumor cells. J Biol Chem 277: 39703-39712, 2002.
6. Boutet A, De Frutos CA, Maxwell PH, Mayol MJ, Romero J, Nieto MA. Snail activation disrupts tissue homeostasis and induces fibrosis in the adult kidney. EMBO J 25: 5603-5613, 2006.
7. Chiu RK, Droll A, Dougherty ST, Carpenito C, Cooper DL, Dougherty GJ. Alternatively spliced CD44 isoforms containing exon v10 promote cellular adhesion through the recognition of chondroitin sulfatemodified CD44. Exp Cell Res 248: 314-321, 1999.
8. Dennler S, Itoh S, Vivien D, ten Dijke P, Huet S, Gauthier JM. Direct binding of Smad3, and Smad4 to critical TGF beta-inducible elements in the promoter of human plasminogen activator inhibitor-type 1 gene. EMBO J 17: 3091-3100, 1998.
9. Djamali A, Samaniego M. Fibrogenesis in kidney transplantation: potential targets for prevention and therapy. Transplantation 88: 1149-1156, 2009.
10. Dworkin LD, Gong R, Tolbert E, Centracchio J, Yano N, Zanabli AR, Esparza A, Rifai A. Hepatocyte growth factor ameliorates progression of interstitial fibrosis in rats with established renal injury. Kidney Int 65: 409-419, 2004.
11. Enck AH, Berger UV, Yu AS. Claudin-2 is selectively expressed in proximal nephron in mouse kidney. Am J Physiol Renal Physiol 281: F966-F974, 2001.
12. Florquin S, Nunziata R, Claessen N, van den Berg FM, Pals ST, Weening JJ. CD44 expression in IgA nephropathy. Am J Kidney Dis 39: 407-414, 2002.
13. Florquin S, Rouschop KM. Reciprocal functions of hepatocyte growth factor and transforming growth factor-beta1 in the progression of renal diseases: a role for CD44? Kidney Int Suppl 86: S15-20, 2003.
14. Gavard J, Gutkind JS. VE-cadherin and claudin-5: it takes two to tango. Nat Cell Biol 10: 883-885, 2008.
15. Gould SE, Day M, Jones SS, Dorai H. BMP-7 regulates chemokine, cytokine, and hemodynamic gene expression in proximal tubule cells. Kidney Int 61: 51-60, 2002.
16. Grande MT, Perez-Barriocanal F, Lopez-Novoa JM. Role of inflammation in tubulo-interstitial damage associated to obstructive nephropathy. J Inflamm 7: 19-32, 2010.
17. Graziani A, Gramaglia D, dalla Zonca P, Comoglio PM. Hepatocyte growth factor/scatter factor stimulates the Ras-guanine nucleotide exchanger. J Biol Chem 268: 9165-9168, 1993.
18. Jackson DG, Bell JI, Dickinson R, Timans J, Shields J, Whittle N. Proteoglycan forms of the lymphocyte homing receptor CD44 are alternatively spliced variants containing the v3 exon. J Cell Biol 128: 673-685, 1995.
19. Jacquemin E, Bulle F, Bernaudin JF, Wellman M, Hugon RN, Guellaen G, Hadchouel M. Pattern of expression of gamma-glutamyl transpeptidase in rat liver and kidney during development: study by immunochemistry and in situ hybridization. J Pediatr Gastroenterol Nutr 11: 89-95, 1990.
20. Jiang D, Liang J, Noble PW. Hyaluronan as an immune regulator in human diseases. Physiol Rev 91: 221-264, 2011.
21. Irie A, Habuchi H, Kimata K, Sanai Y. Heparan sulfate is required for bone morphogenetic protein-7 signaling. Biochem Biophys Res Commun 308: 858-86, 2003.
22. Ishaque A, Dunn MJ, Sorokin A. Cyclooxygenase-2 inhibits tumor necrosis factor alpha-mediated apoptosis in renal glomerular mesangial cells. J Biol Chem 278: 10629-10640, 2003.
23. Iwano M, Plieth D, Danoff TM, Xue C, Okada H, Neilson EG. Evidence that fibroblasts derive from epithelium during tissue fibrosis. J Clin Invest 110: 341-350, 2002.
24. Keerthisingam CB, Jenkins RG, Harrison NK, Hernandez-Rodriguez NA, Booth H, Laurent GJ, Hart SL, Foster ML, McAnulty RJ. Cyclooxygenase-2 deficiency results in a loss of the anti-proliferative response to transforming growth factor-beta in human fibrotic lung fibroblasts and promotes bleomycin-induced pulmonary fibrosis in mice. Am J Pathol 158: 1411-1422, 2001.
25. Kers J, Xu-Dubois YC, Rondeau E, Claessen N, Idu MM, Roelofs JJ, Bemelman FJ, ten Berge IJ, Florquin S. Intragraft tubular vimentin and CD44 expression correlate with long-term renal allograft function and interstitial fibrosis and tubular atrophy. Transplantation 90: 502-509, 2010.
26. Kolodsick JE, Peters-Golden M, Larios J, Toews GB, Thannickal VJ, Moore BB. Prostaglandin E2 inhibits fibroblast to myofibroblast transition via E prostanoid receptor 2 signaling and cyclic adenosine monophosphate elevation. Am J Respir Cell Mol Biol 29: 537-544, 2003.
27. Lee YH, Suzuki YJ, Griffin AJ, Day RM. Hepatocyte growth factor regulates cyclooxygenase-2 expression via beta-catenin, Akt, and p42/p44 MAPK in human bronchial epithelial cells. Am J Physiol Lung Cell Mol Physiol 294: L778-L786, 2008.
28. Leeuwis JW, Nguyen TQ, Chuva de Sousa Lopes SM, van der Giezen DM, van der Ven K, Rouw PJ, Offerhaus GJ, Mummery CL, Goldschmeding R. Direct visualization of Smad1/5/8-mediated transcriptional activity identifies podocytes and collecting ducts as major targets of BMP signaling in healthy and diseased kidneys. J Pathol 224: 121-132, 2011.
29. Luo DD, Phillips A, Fraser D. Bone morphogenetic protein-7 inhibits proximal tubular epithelial cell Smad3 signaling via increased SnoN expression. Am J Pathol 176: 1139-1147, 2010.
30. Medici D, Hay ED, Goodenough DA. Cooperation between snail and LEF-1 transcription factors is essential for TGF-beta1-induced epithelialmesenchymal transition. Mol Biol Cell 17: 1871-1879, 2006.
31. Meng XM, Chung AC, Lan HY. Role of the TGF-beta/BMP-7/Smad pathways in renal diseases. Clin Sci (Lond) 124: 243-254, 2013.
32. Mitu G, Hirschberg R. Bone morphogenetic protein-7 (BMP7) in chronic kidney disease. Front Biosci 13: 4726-4739, 2008.
33. Mizuno S, Matsumoto K, Nakamura T. HGF as a renotrophic and antifibrotic regulator in chronic renal disease. Front Biosci 13: 7072-7086, 2008.
34. Moore AE, Greenhough A, Roberts HR, Hicks DJ, Patsos HA, Williams AC, Paraskeva C. HGF/Met signalling promotes PGE(2) biogenesis via regulation of COX-2 and 15-PGDH expression in colorectal cancer cells. Carcinogenesis 30: 1796-1804, 2009.
35. Moore BB, Paine R, 3rd Christensen PJ, Moore TA, Sitterding S, Ngan R, Wilke CA, Kuziel WA, Toews GB. Protection from pulmonary fibrosis in the absence of CCR2 signaling. J Immunol 167: 4368-4377, 2001.
36. Okada H, Kalluri R. Cellular and molecular pathways that lead to progression and regression of renal fibrogenesis. Curr Mol Med 5: 467-474, 2005.
37. Ophascharoensuk V, Giachelli CM, Gordon K, Hughes J, Pichler R, Brown P, Liaw L, Schmidt R, Shankland SJ, Alpers CE, Couser WG, Johnson RJ. Obstructive uropathy in the mouse: role of osteopontin in interstitial fibrosis and apoptosis. Kidney Int 56: 571-580, 1999.
38. Orian-Rousseau V, Chen L, Sleeman JP, Herrlich P, Ponta H. CD44 is required for two consecutive steps in HGF/c-Met signaling. Genes Dev 16: 3074-3086, 2002.
39. Ortiz A, Ucero AC, Egido J. Unravelling fibrosis: two newcomers and an old foe. Nephrol Dial Transplant 25: 3492-3495, 2010.
40. Persy VP, Verhulst A, Ysebaert DK, De Greef KE, De Broe ME. Reduced postischemic macrophage infiltration and interstitial fibrosis in osteopontin knockout mice. Kidney Int 63: 543-553, 2003.
41. Peterson RS, Andhare RA, Rousche KT, Knudson W, Wang W, Grossfield JB, Thomas RO, Hollingsworth RE, Knudson CB. CD44 modulates Smad1 activation in the BMP-7 signaling pathway. J Cell Biol 166: 1081-1091, 2004.
42. Ponta H, Sherman L, Herrlich PA. CD44: from adhesion molecules to signalling regulators. Nat Rev Mol Cell Biol 4: 33-45, 2003.
43. Pulskens WP, Rampanelli E, Teske GJ, Butter LM, Claessen N, Luirink IK, van der Poll T, Florquin S, Leemans JC. TLR4 promotes fibrosis but attenuates tubular damage in progressive renal injury. J Am Soc Nephrol 21: 1299-1308, 2010.
44. Quinlan MR, Docherty NG, Watson RW, Fitzpatrick JM. Exploring mechanisms involved in renal tubular sensing of mechanical stretch following ureteric obstruction. Am J Physiol Renal Physiol 295: F1-F11, 2008.
45. Reyes JL, Lamas M, Martin D, del Carmen Namorado M, Islas S, Luna J, Tauc M, Gonzalez-Mariscal L. The renal segmental distribution of claudins changes with development. Kidney Int 62: 476-487, 2002.
46. Rouschop KM, Roelofs JJ, Sylva M, Rowshani AT, Ten Berge IJ, Weening JJ, Florquin S. Renal expression of CD44 correlates with acute renal allograft rejection. Kidney Int 70: 1127-1134, 2006.
47. Rouschop KM, Sewnath ME, Claessen N, Roelofs JJ, Hoedemaeker I, van der Neut R, Aten J, Pals ST, Weening JJ, Florquin S. CD44 deficiency increases tubular damage but reduces renal fibrosis in obstructive nephropathy. J Am Soc Nephrol 15: 674-686, 2004.
48. Roy-Chaudhury P, Khong TF, Williams JH, Haites NE, Wu B, Simpson JG, Power DA. CD44 in glomerulonephritis: expression in human renal biopsies, the Thy 1.1 model, and by cultured mesangial cells. Kidney Int 50: 272-281, 1996.
49. Sato M, Muragaki Y, Saika S, Roberts AB, Ooshima A. Targeted disruption of TGF-beta1/Smad3 signaling protects against renal tubulointerstitial fibrosis induced by unilateral ureteral obstruction. J Clin Invest 112: 1486-1494, 2003.
50. Scarpa M, Grillo AR, Brun P, Macchi V, Stefani A, Signori S, Buda A, Fabris P, Giordani MT, De Caro R, Palu G, Castagliuolo I, Martines D. Snail1 transcription factor is a critical mediator of hepatic stellate cell activation following hepatic injury. Am J Physiol Gastrointest Liver Physiol 300: G316-G326, 2011.
51. Screaton GR, Bell MV, Jackson DG, Cornelis FB, Gerth U, Bell JI. Genomic structure of DNA encoding the lymphocyte homing receptor CD44 reveals at least 12 alternatively spliced exons. Proc Natl Acad Sci USA 89: 12160-12164, 1992.
52. Sibalic V, Fan X, Loffing J, Wuthrich RP. Upregulated renal tubular CD44, hyaluronan, and osteopontin in kdkd mice with interstitial nephritis. Nephrol Dial Transplant 12: 1344-1353, 1997.
53. Takahashi K, Stamenkovic I, Cutler M, Dasgupta A, Tanabe KK. Keratan sulfate modification of CD44 modulates adhesion to hyaluronate. J Biol Chem 271: 9490-9496, 1996.
54. van der Voort R, Manten-Horst E, Smit L, Ostermann E, van den Berg F, Pals ST. Binding of cell-surface expressed CD44 to hyaluronate is dependent on splicing and cell type. Biochem Biophys Res Commun 214: 137-144, 1995.
55. van der Voort R, Taher TE, Wielenga VJ, Spaargaren M, Prevo R, Smit L, David G, Hartmann G, Gherardi E, Pals ST. Heparan sulfatemodified CD44 promotes hepatocyte growth factor/scatter factor-induced signal transduction through the receptor tyrosine kinase c-Met. J Biol Chem 274: 6499-6506, 1999.
56. Wilborn J, Crofford LJ, Burdick MD, Kunkel SL, Strieter RM, Peters-Golden M. Cultured lung fibroblasts isolated from patients with idiopathic pulmonary fibrosis have a diminished capacity to synthesize prostaglandin E2 and to express cyclooxygenase-2. J Clin Invest 95: 1861-1868, 1995.
57. Wuthrich RP. The proinflammatory role of hyaluronan-CD44 interactions in renal injury. Nephrol Dial Transplant 14: 2554-2556, 1999.
58. Wynn TA. Cellular and molecular mechanisms of fibrosis. J Pathol 214: 199-210, 2008.
59. Yokoi H, Sugawara A, Mukoyama M, Mori K, Makino H, Suganami T, Nagae T, Yahata K, Fujinaga Y, Tanaka I, Nakao K. Role of connective tissue growth factor in profibrotic action of transforming growth factor-beta: a potential target for preventing renal fibrosis. Am J Kidney Dis 38: S134-138, 2001.
60. Yoshino J, Monkawa T, Tsuji M, Inukai M, Itoh H, Hayashi M. Snail1 is involved in the renal epithelial-mesenchymal transition. Biochem Biophys Res Commun 362: 63-68, 2007.
61. Yu Q, Stamenkovic I. Cell surface-localized matrix metalloproteinase-9 proteolytically activates TGF-beta and promotes tumor invasion and angiogenesis. Genes Dev 14: 163-176, 2000.
62. Yu WH, Woessner JF Jr, McNeish JD, Stamenkovic I. CD44 anchors the assembly of matrilysin/MMP-7 with heparin-binding epidermal growth factor precursor and ErbB4 and regulates female reproductive organ remodeling. Genes Dev 16: 307-323, 2002.
63. Zeisberg M, Hanai J, Sugimoto H, Mammoto T, Charytan D, Strutz F, Kalluri R. BMP-7 counteracts TGF-beta1-induced epithelial-to-mesenchymal transition and reverses chronic renal injury. Nat Med 9: 964-968, 2003.
64. Zeisberg M, Muller GA, Kalluri R. Are there endogenous molecules that protect kidneys from injury? The case for bone morphogenic protein-7 (BMP-7). Nephrol Dial Transplant 19: 759-761, 2004.
65. Zhang A, Wang MH, Dong Z, Yang T. Prostaglandin E2 is a potent inhibitor of epithelial-to-mesenchymal transition: interaction with hepatocyte growth factor. Am J Physiol Renal Physiol 291: F1323-F1331, 2006.