Journal of Surgical Research
Volume 145, Issue 2 , Pages 192-198 , April 2008

A Critical Role for Matrix Metalloproteinases in Liver Regeneration

  • Ian P.J. Alwayn, M.D., Ph.D.

      Affiliations

    • Department of Surgery and The Vascular Biology Program, Children’s Hospital, Boston, Massachusetts
    • Department of Surgery, Erasmus MC, University Medical Center, Rotterdam, The Netherlands
  • ,
  • Jennifer E. Verbesey, M.D.

      Affiliations

    • Department of Hepatobiliary Surgery and Liver Transplantation, Lahey Clinic Medical Center, Burlington, Massachusetts
  • ,
  • Sendia Kim, M.D.

      Affiliations

    • Department of Surgery and The Vascular Biology Program, Children’s Hospital, Boston, Massachusetts
  • ,
  • Roopali Roy, Ph.D.

      Affiliations

    • Department of Surgery and The Vascular Biology Program, Children’s Hospital, Boston, Massachusetts
  • ,
  • Danielle A. Arsenault, B.S.

      Affiliations

    • Department of Surgery and The Vascular Biology Program, Children’s Hospital, Boston, Massachusetts
  • ,
  • Arin K. Greene, M.D., M.M.Sc.

      Affiliations

    • Department of Surgery and The Vascular Biology Program, Children’s Hospital, Boston, Massachusetts
  • ,
  • Katherine Novak, B.S.

      Affiliations

    • Department of Surgery and The Vascular Biology Program, Children’s Hospital, Boston, Massachusetts
  • ,
  • Andrea Laforme, B.A.

      Affiliations

    • Department of Surgery and The Vascular Biology Program, Children’s Hospital, Boston, Massachusetts
    • Department of Pediatric Neuro-Oncology, Dana Farber Cancer Institute, Boston, Massachusetts
  • ,
  • Sang Lee, M.D.

      Affiliations

    • Department of Surgery and The Vascular Biology Program, Children’s Hospital, Boston, Massachusetts
  • ,
  • Marsha A. Moses, Ph.D.

      Affiliations

    • Department of Surgery and The Vascular Biology Program, Children’s Hospital, Boston, Massachusetts
  • ,
  • Mark Puder, M.D., Ph.D.

      Affiliations

    • Department of Surgery and The Vascular Biology Program, Children’s Hospital, Boston, Massachusetts
    • Corresponding Author InformationTo whom correspondence and reprint requests should be addressed at Department of Surgery, Karp Family Research Building 11213, Children’s Hospital, Boston, 300 Longwood Ave., Boston, MA 02115.

Received 30 June 2006

References 

  1. Court FG, Wemyss-Holden SA, Dennison AR, et al. The mystery of liver regeneration. Br J Surg. 2002;89:1089
  2. Greene AK, Wiener S, Puder M, et al. Endothelial-directed hepatic regeneration after partial hepatectomy. Ann Surg. 2003;237:530
  3. Bucher NL. Liver regeneration: An overview. J Gastroenterol Hepatol. 1991;6:615
  4. Kaido T, Oe H, Imamura M. Interleukin-6 augments hepatocyte growth factor-induced liver regeneration: Involvement of STAT3 activation. Hepatogastroenterology. 2004;51:1667
  5. Taub R. Hepatoprotection via the IL-6/Stat3 pathway. J Clin Invest. 2003;112:978
  6. Koniaris LG, McKillop IH, Schwartz SI, et al. Liver regeneration. J Am Coll Surg. 2003;197:634
  7. Blindenbacher A, Wang X, Langer I, et al. Interleukin 6 is important for survival after partial hepatectomy in mice. Hepatology. 2003;38:674
  8. Cressman DE, Greenbaum LE, DeAngelis RA, et al. Liver failure and defective hepatocyte regeneration in interleukin-6-deficient mice. Science. 1996;274:1379
  9. Starace D, Riccioli A, D’Alessio A, et al. Characterization of signaling pathways leading to Fas expression induced by TNF-α: Pivotal role of NF-kappaB. Faseb J. 2005;19:473
  10. Takada Y, Aggarwal BB. TNF activates Syk protein tyrosine kinase leading to TNF-induced MAPK activation, NF-κB activation, and apoptosis. J Immunol. 2004;173:1066
  11. Sekiya M, Yahagi N, Matsuzaka T, et al. Polyunsaturated fatty acids ameliorate hepatic steatosis in obese mice by SREBP-1 suppression. Hepatology. 2003;38:1529
  12. Roy R. Making the cut: Protease-mediated regulation of angiogenesis. ZB Moses M Exp Cell Res. 2005;In press
  13. Fernandez CA, Butterfield C, Jackson G, et al. Structural and functional uncoupling of the enzymatic and angiogenic inhibitory activities of tissue inhibitor of metalloproteinase-2 (TIMP-2): Loop 6 is a novel angiogenesis inhibitor. J Biol Chem. 2003;278:40989
  14. Greene AK, Puder M, Roy R, et al. Urinary matrix metalloproteinases and their endogenous inhibitors predict hepatic regeneration after murine partial hepatectomy. Transplantation. 2004;78:1139
  15. Moses MA. The regulation of neovascularization of matrix metalloproteinases and their inhibitors. Stem Cells. 1997;15:180
  16. Folkman J. Angiogenesis. In:  Braunwald E, et al. editor. Harrison’s Textbook of Internal Medicine. New York: McGraw Hill; 2001;p. 517
  17. Moses MA, Sudhalter J, Langer R. Identification of an inhibitor of neovascularization from cartilage. Science. 1990;248:1408
  18. Murphy AN, Unsworth EJ, Stetler-Stevenson WG. Tissue inhibitor of metalloproteinases-2 inhibits bFGF-induced human microvascular endothelial cell proliferation. J Cell Physiol. 1993;157:351
  19. Higgins G. Experimental pathology of the liver. Arch Pathol. 1931;186
  20. Michalopoulos GK, DeFrances MC. Liver regeneration. Science. 1997;276:60
  21. Greene AK, Puder M. Partial hepatectomy in the mouse: Technique and perioperative management. J Invest Surg. 2003;16:99
  22. Tsuji F, Oki K, Okahara A, et al. Differential effects between marimastat, a TNF-α converting enzyme inhibitor, and anti-TNF-α antibody on murine models for sepsis and arthritis. Cytokine. 2002;17:294
  23. Camphausen K, Moses MA, Beecken WD, et al. Radiation therapy to a primary tumor accelerates metastatic growth in mice. Cancer Res. 2001;61:2207
  24. Wu I, Moses MA. Molecular cloning and expression analysis of the cDNA encoding rat tissue inhibitor of metalloproteinase-4. Matrix Biol. 1998;16:339
  25. Braunhut SJ, Moses MA. Retinoids modulate endothelial cell production of matrix-degrading proteases and tissue inhibitors of metalloproteinases (TIMP). J Biol Chem. 1994;269:13472
  26. Haruyama T, Ajioka I, Akaike T, et al. Regulation and significance of hepatocyte-derived matrix metalloproteinases in liver remodeling. Biochem Biophys Res Commun. 2000;272:681
  27. Kim TH, Mars WM, Stolz DB, et al. Expression and activation of pro-MMP-2 and pro-MMP-9 during rat liver regeneration. Hepatology. 2000;31:75
  28. Knittel T, Mehde M, Grundmann A, et al. Expression of matrix metalloproteinases and their inhibitors during hepatic tissue repair in the rat. Histochem Cell Biol. 2000;113:443
  29. Rundhaug JE. Matrix metalloproteinases, angiogenesis, and cancer: Commentary re: A. C. Lockhart et al (Reduction of wound angiogenesis in patients treated with BMS-275291, a broad spectrum matrix metalloproteinase inhibitor). Clin Cancer Res. 2003;9:551
  30. Laconi S, Curreli F, Diana S, et al. Liver regeneration in response to partial hepatectomy in rats treated with retrorsine: A kinetic study. J Hepatol. 1999;31:1069
  31. Assy N, Gong Y, Zhang M, et al. Use of proliferating cell nuclear antigen as a marker of liver regeneration after partial hepatectomy in rats. J Lab Clin Med. 1998;131:251

1 Ian P.J. Alwayn and Jennifer E. Verbesey contributed equally to this work.

PII: S0022-4804(07)00248-X

doi: 10.1016/j.jss.2007.04.002

Journal of Surgical Research
Volume 145, Issue 2 , Pages 192-198 , April 2008