Skip to main content

Advertisement

Log in

Matrix metalloproteinases: their potential role in the pathogenesis of diabetic nephropathy

  • Review Article
  • Published:
Endocrine Aims and scope Submit manuscript

Abstract

Matrix metalloproteinases (MMPs), a family of proteinases including collagenases, gelatinases, stromelysins, matrilysins, and membrane-type MMPs, affect the breakdown and turnover of extracellular matrix (ECM). Moreover, they are major physiologic determinants of ECM degradation and turnover in the glomerulus. Renal hypertrophy and abnormal ECM deposition are hallmarks of diabetic nephropathy (DN), suggesting that altered MMP expression or activation contributes to renal injury in DN. Herein, we review and summarize recent information supporting a role for MMPs in the pathogenesis of DN. Specifically, studies describing dysregulated activity of MMPs and/or their tissue inhibitors in various experimental models of diabetes, including animal models of type 1 or type 2 diabetes, clinical investigations of human type 1 or type 2 diabetes, and kidney cell culture studies are reviewed.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

References

  1. American Diabetes Association, Diabetes care 26(90001), S94–S98 (2003)

    Google Scholar 

  2. R.A. DeFronzo, Diabetic nephropathy: diagnostic and therapeutic approach, in Current Therapy of Diabetes Mellitus, ed. by R.A. DeFronzo (Mosby-Year Book, Inc., Saint Louis, 1998)

    Google Scholar 

  3. A.P. Boright, A.D. Paterson, L. Mirea, S.B. Bull, A. Mowjoodi, S.W. Scherer, B. Zinman, Diabetes 54(4), 1238–1244 (2005)

    Article  CAS  PubMed  Google Scholar 

  4. L.G. Feld, Diabetic nephropathy, in Pediatric Nephrology, ed. by T.M. Barratt, E.D. Avner (Lippincott, Williams and Wilkins, Baltimore, 1999)

    Google Scholar 

  5. P. Maxwell, Practitioner 249(1666), 9–10 (2005)

    Google Scholar 

  6. R. Visse, H. Nagase, Circ. Res. 92(8), 827–839 (2003)

    Article  CAS  PubMed  Google Scholar 

  7. H. Nagase, R. Visse, G. Murphy, Cardiovasc. Res. 69(3), 562–573 (2006)

    Article  CAS  PubMed  Google Scholar 

  8. Z. Werb, Cell 91(4), 439–442 (1997)

    Article  CAS  PubMed  Google Scholar 

  9. Y. Itoh, M. Seiki, J. Cell. Physiol. 206(1), 1–8 (2006)

    Article  CAS  PubMed  Google Scholar 

  10. Y. Okada, N. Takeuchi, K. Tomita, I. Nakanishi, H. Nagase, Ann. Rheum. Dis. 48(8), 645–653 (1989)

    Article  CAS  PubMed  Google Scholar 

  11. H. Nagase, Matrix Metalloproteinases (Taylor and Francis, London, 1996)

  12. W.C. Parks, S.D. Shapiro, Respir. Res. 2(1), 10–19 (2001)

    Article  CAS  PubMed  Google Scholar 

  13. J.A. Silva, M. Lorencini, L.A. Peroni, C.L. De La Hoz, H.F. Carvalho, D.R. Stach-Machado, J. Periodontal Res. 43(1), 48–54 (2008)

    CAS  PubMed  Google Scholar 

  14. A.J. Barrett, Methods Enzymol. 80(Pt C), 737–754 (1981)

    Article  CAS  PubMed  Google Scholar 

  15. M.P. Herman, G.K. Sukhova, W. Kisiel, D. Foster, M.R. Kehry, P. Libby, U. Schonbeck, J. Clin. Invest. 107(9), 1117–1126 (2001)

    Article  CAS  PubMed  Google Scholar 

  16. K. Sharma, T.A. McGowan, Cytokine Growth Factor Rev. 11(1–2), 115–123 (2000)

    Article  CAS  PubMed  Google Scholar 

  17. B.F. Schrijvers, A.S. De Vriese, A. Flyvbjerg, Endocr. Rev. 25(6), 971–1010 (2004)

    Article  CAS  PubMed  Google Scholar 

  18. J.M. Van Noort, S. Amor, Int. Rev. Cytol. 178, 127–206 (1998)

    PubMed  Google Scholar 

  19. L. Nee, N. Tuite, M.P. Ryan, T. McMorrow, Nephron 107(2), e73–e86 (2007)

    CAS  PubMed  Google Scholar 

  20. S.V. McLennan, D.J. Kelly, M. Schache, M. Waltham, V. Dy, R.G. Langham, D.K. Yue, R.E. Gilbert, Kidney Int. 72(4), 481–488 (2007)

    Article  CAS  PubMed  Google Scholar 

  21. Y. Bai, L. Wang, Y. Li, S. Liu, J. Li, H. Wang, H. Huang, Cell Physiol. Biochem. 17(1–2), 57–68 (2006)

    Article  CAS  PubMed  Google Scholar 

  22. A.K. Death, E.J. Fisher, K.C. McGrath, D.K. Yue, Atherosclerosis 168(2), 263–269 (2003)

    Article  CAS  PubMed  Google Scholar 

  23. A. Fornoni, L.J. Striker, F. Zheng, G.E. Striker, Diabetes 51(2), 499–505 (2002)

    Article  CAS  PubMed  Google Scholar 

  24. F. Hao, J.D. Yu, Acta Pharmacol. Sin. 24(6), 534–538 (2003)

    CAS  PubMed  Google Scholar 

  25. R. Singh, R.H. Song, N. Alavi, A.A. Pegoraro, A.K. Singh, D.J. Leehey, Exp. Nephrol. 9(4), 249–257 (2001)

    Article  CAS  PubMed  Google Scholar 

  26. N. Abdel Wahab, R.M. Mason, Biochem. J. 320(Pt 3), 777–783 (1996)

    PubMed  Google Scholar 

  27. E. Ishizaki, S. Takai, M. Ueki, T. Maeno, M. Maruichi, T. Sugiyama, H. Oku, T. Ikeda, M. Miyazaki, Am. J. Ophthalmol. 141(1), 129–134 (2006)

    Article  CAS  PubMed  Google Scholar 

  28. K. Noda, S. Ishida, M. Inoue, K. Obata, Y. Oguchi, Y. Okada, E. Ikeda, Invest. Ophthalmol. Vis. Sci. 44(5), 2163–2170 (2003)

    Article  PubMed  Google Scholar 

  29. S.J. Giebel, G. Menicucci, P.G. McGuire, A. Das, Lab. Invest. 85(5), 597–607 (2005)

    Article  CAS  PubMed  Google Scholar 

  30. A. Medina, P.G. Scott, A. Ghahary, E.E. Tredget, J. Burn Care Rehabil. 26(4), 306–319 (2005)

    Article  PubMed  Google Scholar 

  31. R. Lobmann, A. Ambrosch, G. Schultz, K. Waldmann, S. Schiweck, H. Lehnert, Diabetologia 45(7), 1011–1016 (2002)

    Article  CAS  PubMed  Google Scholar 

  32. S. Jacqueminet, O. Ben Abdesselam, M.J. Chapman, N. Nicolay, M.J. Foglietti, A. Grimaldi, J.L. Beaudeux, Clin. Chim. Acta 367(1–2), 103–107 (2006)

    Article  CAS  PubMed  Google Scholar 

  33. G. Derosa, M.A. Avanzini, D. Geroldi, R. Fogari, R. Lorini, A. De Silvestri, C. Tinelli, G. Rondini, G. d’Annunzio, Diabetes Res. Clin. Pract. 70(2), 119–125 (2005)

    Article  CAS  PubMed  Google Scholar 

  34. A.W. Chung, Y.N. Hsiang, L.A. Matzke, B.M. McManus, C. van Breemen, E.B. Okon, Circ. Res. 99(2), 140–148 (2006)

    Article  CAS  PubMed  Google Scholar 

  35. S.S. Signorelli, G. Malaponte, M. Libra, L. Di Pino, G. Celotta, V. Bevelacqua, M. Petrina, G.S. Nicotra, M. Indelicato, P.M. Navolanic, G. Pennisi, M.C. Mazzarino, Vasc. Med. 10(1), 1–6 (2005)

    Article  PubMed  Google Scholar 

  36. G. Derosa, A.F. Cicero, F. Scalise, M.A. Avanzini, C. Tinelli, M.N. Piccinni, E. Peros, D. Geroldi, E. Fogari, A. D’Angelo, Endothelium 14(1), 45–51 (2007)

    Article  CAS  PubMed  Google Scholar 

  37. G. Derosa, A. D’Angelo, F. Scalise, M.A. Avanzini, C. Tinelli, E. Peros, E. Fogari, A.F. Cicero, Heart Vessels 22(6), 361–370 (2007)

    Article  PubMed  Google Scholar 

  38. K.M. Thrailkill, R.C. Bunn, C.S. Moreau, G.E. Cockrell, P.M. Simpson, H.N. Coleman, J.P. Frindik, S.F. Kemp, J.L. Fowlkes, Diabetes care 30(9), 2321–2326 (2007)

    Article  CAS  PubMed  Google Scholar 

  39. J.M. Catania, G. Chen, A.R. Parrish, Am. J. Physiol. 292(3), F905–F911 (2007)

    CAS  Google Scholar 

  40. R.M. Mason, N.A. Wahab, J. Am. Soc. Nephrol. 14(5), 1358–1373 (2003)

    Article  CAS  PubMed  Google Scholar 

  41. L. Barbe, E. Lundberg, P. Oksvold, A. Stenius, E. Lewin, E. Bjorling, A. Asplund, F. Ponten, H. Brismar, M. Uhlen, H. Andersson-Svahn, Mol. Cell. Proteomics 7(3), 499–508 (2008)

    CAS  PubMed  Google Scholar 

  42. S. Hober, M. Uhlen, Curr. Opin. Biotechnol. 19(1), 30–35 (2008)

    Article  CAS  PubMed  Google Scholar 

  43. B. Lelongt, B. Legallicier, R. Piedagnel, P.M. Ronco, Curr. Opin. Nephrol. Hypertens. 10(1), 7–12 (2001)

    Article  CAS  PubMed  Google Scholar 

  44. O. Lenz, S.J. Elliot, W.G. Stetler-Stevensen, J. Am. Soc. Nephrol. 11, 574–581 (2000)

    Google Scholar 

  45. G. Zerbini, R. Bonfanti, F. Meschi, E. Bognetti, P.L. Paesano, L. Gianolli, M. Querques, A. Maestroni, G. Calori, A. Del Maschio, F. Fazio, L. Luzi, G. Chiumello, Diabetes 55(9), 2620–2625 (2006)

    Article  CAS  PubMed  Google Scholar 

  46. F.L. Frazer, L.J. Palmer, A. Clarey, S. Thonell, G.C. Byrne, J. Pediatr. Endocrinol. Metab. 14(7), 875–881 (2001)

    CAS  PubMed  Google Scholar 

  47. H.J. Baumgartl, G. Sigl, P. Banholzer, M. Haslbeck, E. Standl, Nephrol. Dial. Transplant. 13(3), 630–634 (1998)

    Article  CAS  PubMed  Google Scholar 

  48. M.L. Lawson, E.B. Sochett, P.G. Chait, J.W. Balfe, D. Daneman, Diabetes 45(1), 51–55 (1996)

    Article  CAS  PubMed  Google Scholar 

  49. G. Hasegawa, K. Nakano, M. Sawada, K. Uno, Y. Shibayama, K. Ienaga, M. Kondo, Kidney Int. 40(6), 1007–1012 (1991)

    Article  CAS  PubMed  Google Scholar 

  50. J.L. Fowlkes, K.M. Thrailkill, D.M. Serra, K. Suzuki, H. Nagase, Progress in growth factor research 6(2–4), 255–263 (1995)

    Article  CAS  PubMed  Google Scholar 

  51. M. Ii, H. Yamamoto, Y. Adachi, Y. Maruyama, Y. Shinomura, Exp. Biol. Med. (Maywood) 231(1), 20–27 (2006)

    CAS  Google Scholar 

  52. J.L. Fowlkes, D.M. Serra, H. Nagase, K.M. Thrailkill, Ann. N. Y. Acad. Sci. 878, 696–699 (1999)

    Article  CAS  PubMed  Google Scholar 

  53. S. Zhuang, G.R. Kinsey, K. Rasbach, R.G. Schnellmann, Am. J. Physiol. 294, F459–F468 (2008)

    Google Scholar 

  54. J. Keeling, G.A. Herrera, Kidney Int. 68(4), 1590–1603 (2005)

    Article  CAS  PubMed  Google Scholar 

  55. V. Bhuvarahamurthy, G.O. Kristiansen, M. Johannsen, S.A. Loening, D. Schnorr, K. Jung, A. Staack, Oncol. Rep. 15(5), 1379–1384 (2006)

    CAS  PubMed  Google Scholar 

  56. S. Cheng, D.H. Lovett, Am. J. Pathol. 162(6), 1937–1949 (2003)

    CAS  PubMed  Google Scholar 

  57. M. Essawy, O. Soylemezoglu, E.C. Muchaneta-Kubara, J. Shortland, C.B. Brown, A.M. el Nahas, Nephrol. Dial. Transplant. 12(1), 43–50 (1997)

    Article  CAS  PubMed  Google Scholar 

  58. S. Cheng, A.S. Pollock, R. Mahimkar, J.L. Olson, D.H. Lovett, FASEB J. 20(11), 1898–1900 (2006)

    Article  CAS  PubMed  Google Scholar 

  59. S.X. Zhang, J.J. Wang, K. Lu, R. Mott, R. Longeras, J.X. Ma, J. Am. Soc. Nephrol. 17(2), 475–486 (2006)

    Article  CAS  PubMed  Google Scholar 

  60. A. Inada, K. Nagai, H. Arai, J. Miyazaki, K. Nomura, H. Kanamori, S. Toyokuni, Y. Yamada, S. Bonner-Weir, G.C. Weir, A. Fukatsu, Y. Seino, Am. J. Pathol. 167(2), 327–336 (2005)

    PubMed  Google Scholar 

  61. S.Z. Sun, Y. Wang, Q. Li, Y.J. Tian, M.H. Liu, Y.H. Yu, Chin. Med. J. Engl. 119(10), 814–821 (2006)

    CAS  PubMed  Google Scholar 

  62. S.Y. Han, Y.H. Jee, K.H. Han, Y.S. Kang, H.K. Kim, J.Y. Han, Y.S. Kim, D.R. Cha, Nephrol. Dial. Transplant. 21(9), 2406–2416 (2006)

    Article  CAS  PubMed  Google Scholar 

  63. A.M. Romanic, C.L. Burns-Kurtis, Z. Ao, A.J. Arleth, E.H. Ohlstein, Am. J. Physiol. 281(2), F309–F317 (2001)

    CAS  Google Scholar 

  64. M. Diamant, R. Hanemaaijer, J.H. Verheijen, J.W. Smit, J.K. Radder, H.H. Lemkes, Diabet. Med. 18(5), 423–424 (2001)

    Article  CAS  PubMed  Google Scholar 

  65. M.P. Lee, G. Sweeney, Diabetes Obes. Metab. 8(3), 281–288 (2006)

    Article  CAS  PubMed  Google Scholar 

  66. S. Liu, Y. Li, H. Zhao, D. Chen, Q. Huang, S. Wang, W. Zou, Y. Zhang, X. Li, H. Huang, Mol. Cell. Biochem. 284(1–2), 9–17 (2006)

    Article  CAS  PubMed  Google Scholar 

  67. T. Kuroda, Y. Yoshida, J. Kamiie, P. Kovalenko, M. Nameta, H. Fujinaka, E. Yaoita, T. Endo, S. Ishizuka, K. Nakabayashi, A. Yamada, T. Nagasawa, T. Yamamoto, Clin. Exp. Nephrol. 8(3), 206–215 (2004)

    Article  CAS  PubMed  Google Scholar 

  68. T.S. Ahuja, A. Gopalani, P. Davies, H. Ahuja, Nephron Clin. Pract. 95(3), c100–c104 (2003)

    Article  CAS  PubMed  Google Scholar 

  69. N. Kawata, Y. Nagane, T. Igarashi, H. Hirakata, T. Ichinose, T. Hachiya, Y. Takimoto, S. Takahashi, Urology 68(3), 523–527 (2006)

    Article  PubMed  Google Scholar 

  70. G. Qing-Hua, L. Ju-Ming, P. Chang-Yu, L. Zhao-Hui, Z. Xiao-Man, M. Yi-Ming, J. Diabetes Complicat. 22, 408–412 (2007)

    Google Scholar 

  71. K. Tashiro, I. Koyanagi, I. Ohara, T. Ito, A. Saitoh, S. Horikoshi, Y. Tomino, J. Clin. Lab. Anal. 18(3), 206–210 (2004)

    Article  CAS  PubMed  Google Scholar 

  72. A. Lauhio, T. Sorsa, R. Srinivas, M. Stenman, T. Tervahartiala, U.H. Stenman, C. Gronhagen-Riska, E. Honkanen, Ann. Med. 40(4), 312–320 (2008)

    Article  CAS  PubMed  Google Scholar 

  73. H. Pavenstadt, W. Kriz, M. Kretzler, Physiol. Rev. 83(1), 253–307 (2003)

    CAS  PubMed  Google Scholar 

  74. K. Asanuma, I. Shirato, K. Ishidoh, E. Kominami, Y. Tomino, Kidney Int. 62(3), 822–831 (2002)

    Article  CAS  PubMed  Google Scholar 

  75. S. Liu, Y. Liang, H. Huang, L. Wang, Y. Li, J. Li, X. Li, H. Wang, Cell Physiol. Biochem. 16(4–6), 207–216 (2005)

    Article  CAS  PubMed  Google Scholar 

  76. K. Susztak, A.C. Raff, M. Schiffer, E.P. Bottinger, Diabetes 55(1), 225–233 (2006)

    Article  CAS  PubMed  Google Scholar 

  77. G. Wolf, S. Chen, F.N. Ziyadeh, Diabetes 54(6), 1626–1634 (2005)

    Article  CAS  PubMed  Google Scholar 

  78. T. Nakamura, C. Ushiyama, S. Suzuki, M. Hara, N. Shimada, I. Ebihara, H. Koide, Nephrol. Dial. Transplant. 15(9), 1379–1383 (2000)

    Article  CAS  PubMed  Google Scholar 

  79. K. Surendran, T.C. Simon, H. Liapis, J.K. McGuire, Kidney Int. 65(6), 2212–2222 (2004)

    Article  CAS  PubMed  Google Scholar 

  80. M. Riera, S. Burtey, M. Fontes, Kidney Int. 69(9), 1558–1563 (2006)

    Article  CAS  PubMed  Google Scholar 

  81. A. Henger, M. Kretzler, P. Doran, M. Bonrouhi, H. Schmid, E. Kiss, C.D. Cohen, S. Madden, S. Porubsky, E.F. Grone, D. Schlondorff, P.J. Nelson, H.J. Grone, Kidney Int. 65(3), 904–917 (2004)

    Article  CAS  PubMed  Google Scholar 

  82. V.H. Rao, G.E. Lees, C.E. Kashtan, D.C. Delimont, R. Singh, D.T. Meehan, G. Bhattacharya, B.R. Berridge, D. Cosgrove, Pediatr. Nephrol. 20(6), 732–739 (2005)

    Article  PubMed  Google Scholar 

  83. G. Sarkissian, P. Fergelot, P.J. Lamy, J.J. Patard, S. Culine, P. Jouin, N. Rioux-Leclercq, B. Darbouret, Clin. Chem. 54(3), 574–581 (2008)

    Article  CAS  PubMed  Google Scholar 

  84. E. Patraki, M.R. Cardillo, Int. J. Immunopathol. Pharmacol. 20(4), 697–705 (2007)

    CAS  PubMed  Google Scholar 

  85. A. Melk, E.S. Mansfield, S.C. Hsieh, T. Hernandez-Boussard, P. Grimm, D.C. Rayner, P.F. Halloran, M.M. Sarwal, Kidney Int. 68(6), 2667–2679 (2005)

    Article  CAS  PubMed  Google Scholar 

  86. J. F. Woessner, H. Nagase (eds.), in Protein Substrates of the MMPs. Matrix Metalloproteinases and TIMPs, 1st edn., (Oxford University Press, New York, 2000)

  87. A. Maldonado, L. He, B.A. Game, A. Nareika, J.J. Sanders, S.D. London, M.F. Lopes-Virella, Y. Huang, J. Periodont. Res. 39(6), 415–423 (2004)

    Article  CAS  PubMed  Google Scholar 

  88. A. Flyvbjerg, Diabetologia 43(10), 1205–1223 (2000)

    Article  CAS  PubMed  Google Scholar 

  89. I.S. Park, H. Kiyomoto, F. Alvarez, Y.C. Xu, H.E. Abboud, S.L. Abboud, Am. J. Kidney Dis. 32(6), 1000–1010 (1998)

    Article  CAS  PubMed  Google Scholar 

  90. S. Miyamoto, K. Yano, S. Sugimoto, G. Ishii, T. Hasebe, Y. Endoh, K. Kodama, M. Goya, T. Chiba, A. Ochiai, Cancer Res 64(2), 665–671 (2004)

    Article  CAS  PubMed  Google Scholar 

  91. E. Hemers, C. Duval, C. McCaig, M. Handley, G.J. Dockray, A. Varro, Cancer Res. 65(16), 7363–7369 (2005)

    Article  CAS  PubMed  Google Scholar 

  92. C. McCaig, C. Duval, E. Hemers, I. Steele, D.M. Pritchard, S. Przemeck, R. Dimaline, S. Ahmed, K. Bodger, D.D. Kerrigan, T.C. Wang, G.J. Dockray, A. Varro, Gastroenterology 130(6), 1754–1763 (2006)

    Article  CAS  PubMed  Google Scholar 

  93. Y. Liu, Kidney Int. 69(2), 213–217 (2006)

    Article  CAS  PubMed  Google Scholar 

  94. E.P. Bottinger, M. Bitzer, J. Am. Soc. Nephrol. 13(10), 2600–2610 (2002)

    Article  PubMed  Google Scholar 

  95. K. Imai, A. Hiramatsu, D. Fukushima, M.D. Pierschbacher, Y. Okada, Biochem. J. 322(Pt 3), 809–814 (1997)

    CAS  PubMed  Google Scholar 

  96. W.H. Yu, J.F. Woessner Jr., J.D. McNeish, I. Stamenkovic, Genes Dev. 16(3), 307–323 (2002)

    Article  CAS  PubMed  Google Scholar 

  97. Y.J. Lee, S.J. Shin, S.R. Lin, M.S. Tan, J.H. Tsai, Biochem. Biophys. Res. Commun. 207(1), 216–222 (1995)

    Article  CAS  PubMed  Google Scholar 

  98. J. Movassat, C. Saulnier, P. Serradas, B. Portha, Diabetologia 40(8), 916–925 (1997)

    Article  CAS  PubMed  Google Scholar 

  99. V. Portik-Dobos, A.K. Harris, W. Song, J. Hutchinson, M.H. Johnson, J.D. Imig, D.M. Pollock, A. Ergul, Am. J. Physiol. Regul. Integr. Comp. Physiol. 290(2), R435–R441 (2006)

    CAS  PubMed  Google Scholar 

  100. E. Boucher, G. Mayer, I. Londono, M. Bendayan, Kidney Int. 69(9), 1570–1577 (2006)

    Article  CAS  PubMed  Google Scholar 

  101. P. Osenkowski, M. Toth, R. Fridman, J. Cell. Physiol. 200(1), 2–10 (2004)

    Article  CAS  PubMed  Google Scholar 

  102. Q. Yang, R.J. Xie, T. Yang, L. Fang, B. Han, G.Z. Zhang, M.L. Cheng, Chin. Med. Sci. J. 22(4), 243–249 (2007)

    CAS  PubMed  Google Scholar 

  103. T. Nakamura, M. Fukui, I. Ebihara, S. Osada, Y. Tomino, H. Koide, Ren. Physiol. Biochem. 17(6), 316–325 (1994)

    CAS  PubMed  Google Scholar 

  104. D. Suzuki, M. Miyazaki, K. Jinde, T. Koji, M. Yagame, M. Endoh, Y. Nomoto, H. Sakai, Kidney Int. 52(1), 111–119 (1997)

    Article  CAS  PubMed  Google Scholar 

  105. T. Aoyama, S. Yamamoto, A. Kanematsu, O. Ogawa, Y. Tabata, Tissue Eng. 9(6), 1289–1299 (2003)

    Article  CAS  PubMed  Google Scholar 

  106. J.M. Cruzado, N. Lloberas, J. Torras, M. Riera, C. Fillat, I. Herrero-Fresneda, J.M. Aran, G. Alperovich, A. Vidal, J.M. Grinyo, Diabetes 53(4), 1119–1127 (2004)

    Article  CAS  PubMed  Google Scholar 

  107. J. Rysz, M. Banach, R.A. Stolarek, J. Pasnik, A. Cialkowska-Rysz, R. Koktysz, M. Piechota, Z. Baj, J. Nephrol. 20(4), 444–452 (2007)

    CAS  PubMed  Google Scholar 

  108. M. Kanauchi, H. Nishioka, Y. Nakashima, T. Hashimoto, K. Dohi, Nippon Jinzo Gakkai Shi 38(3), 124–128 (1996)

    CAS  PubMed  Google Scholar 

  109. Z. Qi, H. Fujita, J. Jin, L.S. Davis, Y. Wang, A.B. Fogo, M.D. Breyer, Diabetes 54(9), 2628–2637 (2005)

    Article  CAS  PubMed  Google Scholar 

  110. K.G. Ewens, R.A. George, K. Sharma, F.N. Ziyadeh, R.S. Spielman, Diabetes 54(11), 3305–3318 (2005)

    Article  CAS  PubMed  Google Scholar 

  111. A.K. Ahmed, J.L. Haylor, A.M. El Nahas, T.S. Johnson, Kidney Int. 71(8), 755–763 (2007)

    Article  CAS  PubMed  Google Scholar 

  112. G. Remuzzi, T. Bertani, N. Engl. J. Med. 339(20), 1448–1456 (1998)

    Article  CAS  PubMed  Google Scholar 

  113. M. Abbate, C. Zoja, G. Remuzzi, J. Am. Soc. Nephrol. 17(11), 2974–2984 (2006)

    Article  CAS  PubMed  Google Scholar 

  114. M. Zeisberg, M. Khurana, V.H. Rao, D. Cosgrove, J.P. Rougier, M.C. Werner, C.F. Shield 3rd, Z. Werb, R. Kalluri, PLoS Med. 3(4), e100 (2006)

    Article  PubMed  CAS  Google Scholar 

  115. S.V. McLennan, D.J. Kelly, A.J. Cox, Z. Cao, J.G. Lyons, D.K. Yue, R.E. Gilbert, Diabetologia 45(2), 268–275 (2002)

    Article  CAS  PubMed  Google Scholar 

  116. R.H. Song, A.K. Singh, D.J. Leehey, Am. J. Nephrol. 19(3), 441–446 (1999)

    Article  CAS  PubMed  Google Scholar 

  117. S.V. McLennan, S.Y. Martell, D.K. Yue, Diabetologia 43(5), 642–648 (2000)

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

This work was supported in part by grants from the National Institutes of Health to KMT (R01-DK62999) and from the Arkansas Children’s Hospital Research Institute CUMG Award Program to KMT (#036054).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Kathryn M. Thrailkill.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Thrailkill, K.M., Clay Bunn, R. & Fowlkes, J.L. Matrix metalloproteinases: their potential role in the pathogenesis of diabetic nephropathy. Endocr 35, 1–10 (2009). https://doi.org/10.1007/s12020-008-9114-6

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12020-008-9114-6

Keywords

Navigation