Gastroenterology
Volume 125, Issue 1 , Pages 192-201 , July 2003

Protection against liver damage by cardiotrophin-1: a hepatocyte survival factor up-regulated in the regenerating liver in rats

  • Matilde Bustos

      Affiliations

    • Department of Medicine, Division of Hepatology and Gene Therapy, Clinica Universitaria and Medical School, University of Navarra, Pamplona, Spain
    • Corresponding Author InformationAddress requests for reprints to: Matilde Bustos, M.D., Department of Medicine and Liver Unit, Clinica Universitaria, 31008 Pamplona, Spain; fax: (34) 948-29-67-85
    • M.B. and N.B. contributed equally to this work.
    • ,
  • Naiara Beraza

      Affiliations

    • Department of Medicine, Division of Hepatology and Gene Therapy, Clinica Universitaria and Medical School, University of Navarra, Pamplona, Spain
    • M.B. and N.B. contributed equally to this work.
    • ,
  • Juan-Jose Lasarte

      Affiliations

    • Department of Medicine, Division of Hepatology and Gene Therapy, Clinica Universitaria and Medical School, University of Navarra, Pamplona, Spain
    • ,
  • Elena Baixeras

      Affiliations

    • Department of Medicine, Division of Hepatology and Gene Therapy, Clinica Universitaria and Medical School, University of Navarra, Pamplona, Spain
    • ,
  • Pilar Alzuguren

      Affiliations

    • Department of Medicine, Division of Hepatology and Gene Therapy, Clinica Universitaria and Medical School, University of Navarra, Pamplona, Spain
    • ,
  • Thierry Bordet

      Affiliations

    • Institut National de la Santé et de la Recherche Médicale (INSERM), Institut Cochin de Génétique Moléculaire, Paris, France
    • ,
  • Jesus Prieto

      Affiliations

    • Department of Medicine, Division of Hepatology and Gene Therapy, Clinica Universitaria and Medical School, University of Navarra, Pamplona, Spain

References 

  1. Mochida S, Ogata I, Hirata K, Ohta Y, Yamada S, Fujiwara K. Provocation of massive hepatic necrosis by endotoxin after partial hepatectomy in rats. Gastroenterology. 1990;92:1174–1180
  2. Hasegawa S, Kubota T, Fukuyama N, Kurosawa H, Sekido H, Togo S, et al. Apoptosis of hepatocytes is a main cause of inducing lethal hepatic failure after excessive hepatectomy in rats. Transplant Proc. 1999;31:558–559
  3. Bernuau J, Benhamou J. Fulminant and subfulminant liver failure. In:  Bircher J,  Benhamou JP,  McIntyre N,  Rizzetto M,  Rodes J editor. Textbook of clinical hepatology. 2:Oxford Medical Publications; 1999;p. 1–40
  4. Pennica D, King KL, Shaw KJ, Luis E, Rullamas J, Luoh SM, et al  Expression cloning of cardiotrophin 1, a cytokine that induces cardiac myocyte hypertrophy. Proc Natl Acad Sci U S A. 1995;92:1142–1146
  5. Wollert KC, Taga T, Saito M, Narazaki M, Kishimoto T, Glembotski CC, et al. Cardiotrophin-1 activates a distinct form of cardiac muscle cell hypertrophy. Assembly of sarcomeric units in series VIA gp130/leukemia inhibitory factor receptor-dependent pathways. J Biol Chem. 1996;271:9535–9545
  6. Sheng Z, Pennica D, Wood WI, Chien KR. Cardiotrophin-1 displays early expression in the murine heart tube and promotes cardiac myocyte survival. Development. 1996;122:419–428
  7. Pennica D, Arce V, Swanson TA, Vejsada R, Pollock RA, Armanini M, et al. Cardiotrophin-1, a cytokine present in embryonic muscle, supports long-term survival of spinal motoneurons. Neuron. 1996;17:63–74
  8. Oppenheim RW, Wiese S, Prevette D, Armanini M, Wang S, Houenou LJ, et al. Cardiotrophin-1, a muscle-derived cytokine, is required for the survival of subpopulations of developing motoneurons. J Neurosci. 2001;21:1283–1291
  9. Sheng Z, Knowlton K, Chen J, Hoshijima M, Brown JH, Chien KR. Cardiotrophin 1 (CT-1) inhibition of cardiac myocyte apoptosis via a mitogen-activated protein kinase-dependent pathway. Divergence from downstream CT-1 signals for myocardial cell hypertrophy. J Biol Chem. 1997;272:5783–5791
  10. Stephanou A, Brar B, Heads R, Knight RD, Marber MS, Pennica D, et al. Cardiotrophin-1 induces heat shock protein accumulation in cultured cardiac cells and protects them from stressful stimuli. J Mol Cell Cardiol. 1998;30:849–855
  11. Robledo O, Fourcin M, Chevalier S, Guillet C, Auguste P, Pouplard-Barthelaix A, et al. Signaling of the cardiotrophin-1 receptor. Evidence for a third receptor component. J Biol Chem. 1997;272:4855–4863
  12. Oh H, Fujio Y, Kunisada K, Hirota H, Matsui H, Kishimoto T, et al. Activation of phosphatidylinositol 3-kinase through glycoprotein 130 induces protein kinase B and p70 S6 kinase phosphorylation in cardiac myocytes. J Biol Chem. 1998;273:9703–9710
  13. Kuwahara K, Saito Y, Kishimoto I, Miyamoto Y, Harada M, Ogawa E, et al. Cardiotrophin-1 phosphorylates akt and BAD, and prolongs cell survival via a PI3K-dependent pathway in cardiac myocytes. J Mol Cell Cardiol. 2000;32:1385–1394
  14. Brar BK, Stephanou A, Liao Z, O’Leary RM, Pennica D, Yellon DM, et al. Cardiotrophin-1 can protect cardiac myocytes from injury when added both prior to simulated ischaemia and at reoxygenation. Cardiovasc Res. 2001;51:265–274
  15. Peters M, Roeb E, Pennica D, Meyer zum Buschenfelde KH, Rose-John S. A new hepatocyte stimulating factor (cardiotrophin-1 (CT-1)). FEBS Lett. 1995;372:177–180
  16. Jin H, Yang R, Keller GA, Ryan A, Ko A, Finkle D, et al. In vivo effects of cardiotrophin-1. Cytokine. 1996;8:920–926
  17. Baixeras E, Jeay S, Kelly PA, Postel-Vinay MC. The proliferative and antiapoptotic actions of growth hormone and insulin-like growth factor-1 are mediated through distinct signaling pathways in the Pro-B Ba/F3 cell line. Endocrinology. 2001;142:2968–2977
  18. Herrera B, Fernandez M, Alvarez AM, Roncero C, Benito M, Gil J, et al. Activation of caspases occurs downstream from radical oxygen species production, Bcl-xL down-regulation, and early cytochrome C release in apoptosis induced by transforming growth factor beta in rat fetal hepatocytes. Hepatology. 2001;34:548–556
  19. Chomczynski P. A reagent for the single-step simultaneous isolation of RNA, DNA and proteins from cell and tissue samples. Biotechniques. 1993;15:532–534 536–537
  20. Lesbordes JC, Bordet T, Haase G, Castelnau-Ptakhine L, Rouhani S, Gilgenkrantz H, et al. In vivo electrotransfer of the cardiotrophin-1 gene into skeletal muscle slows down progression of motor neuron degeneration in pmn mice. Hum Mol Genet. 2002;11:1615–1625
  21. Bordet T, Schmalbruch H, Pettmann B, Hagege A, Castelnau-Ptakhine L, Kahn A, et al. Adenoviral cardiotrophin-1 gene transfer protects pmn mice from progressive motor neuronopathy. J Clin Invest. 1999;104:1077–1085
  22. Qian C, Bilbao R, Bruna O, Prieto J. Induction of sensitivity to ganciclovir in human hepatocellular carcinoma cells by adenovirus-mediated gene transfer of herpes simplex virus thymidine kinase. Hepatology. 1995;22:118–123
  23. Chen RH, Chang TY. Involvement of caspase family proteases in transforming growth factor-beta-induced apoptosis. Cell Growth Differ. 1997;8:821–827
  24. Fausto N. Liver regeneration. In:  Arias I editors. The liver, biology and pathobiology. Philadelphia: Lippincott Williams and Wilkins; 2001;p. 591–610
  25. Bordet T, Lesbordes JC, Rouhani S, Castelnau-Ptakhine L, Schmalbruch H, Haase G, et al. Protective effects of cardiotrophin-1 adenoviral gene transfer on neuromuscular degeneration in transgenic ALS mice. Hum Mol Genet. 2001;10:1925–1933
  26. Hayami S, Yaita M, Ogiri Y, Sun F, Nakata R, Kojo S. Change in caspase-3-like protease in the liver and plasma during rat liver regeneration following partial hepatectomy. Biochem Pharmacol. 2000;60:1883–1886
  27. Tiegs G, Hentschel J, Wendel A. A T cell-dependent experimental liver injury in mice inducible by concanavalin A. J Clin Invest. 1992;90:196–203
  28. Chen RH, Chang MC, Su YH, Tsai YT, Kuo ML. Interleukin-6 inhibits transforming growth factor beta-induced apoptosis through the phosphatidylinositol 3-kinase/Akt and signal transducers and activators of transcription 3 pathways. J Biol Chem. 1999;274:23013–23019
  29. Yasukawa H, Hoshijima M, Gu Y, Nakamura T, Pradervand S, Hanada T, et al. Suppressor of cytokine signaling-3 is a biomechanical stress-inducible gene that suppresses gp-130-mediated cardiac myocyte hypertrophy and survival pathways. J Clin Invest. 2001;108:1459–1467
  30. Fausto N. Liver regeneration. J Hepatol. 2000;32:19–31
  31. Ujike K, Shinji T, Hirasaki S, Shiraha H, Nakamura M, Tsuji T, et al. Kinetics of expression of connective tissue growth factor gene during liver regeneration after partial hepatectomy and D-galactosamine-induced liver injury in rats. Biochem Biophys Res Commun. 2000;277:448–454
  32. Bissell DM, Roulot D, George J. Transforming growth factor beta and the liver. Hepatology. 2001;34:859–867
  33. Takehara T, Hayashi N, Mita E, Kanto T, Tatsumi T, Sasaki Y, et al. Delayed Fas-mediated hepatocyte apoptosis during liver regeneration in mice (hepatoprotective role of TNF alpha). Hepatology. 1998;27:1643–1651
  34. Houck KA, Michalopoulos GK. Altered responses of regenerating hepatocytes to norepinephrine and transforming growth factor type beta. J Cell Physiol. 1989;141:503–509
  35. Kobayashi N, Fujiwara T, Westerman KA, Inoue Y, Sakaguchi M, Noguchi H, et al. Prevention of acute liver failure in rats with reversibly immortalized human hepatocytes. Science. 2000;287:1258–1262
  36. Fukada T, Ohtani T, Yoshida Y, Shirogane T, Nishida K, Nakajima K, et al. STAT3 orchestrates contradictory signals in cytokine-induced G1 to S cell-cycle transition. EMBO J. 1998;17:6670–6677
  37. Muise-Helmericks RC, Grimes HL, Bellacosa A, Malstrom SE, Tsichlis PN, Rosen N. Cyclin D expression is controlled post-transcriptionally via a phosphatidylinositol 3-kinase/Akt-dependent pathway. J Biol Chem. 1998;273:29864–29872
  38. Rescan C, Coutant A, Talarmin H, Theret N, Glaise D, Guguen-Guillouzo C, et al. Mechanism in the sequential control of cell morphology and S phase entry by epidermal growth factor involves distinct MEK/ERK activations. Mol Biol Cell. 2001;12:725–738
  39. Faouzi S, Burckhardt BE, Hanson JC, Campe CB, Schrum LW, Rippe RA, et al. Anti-Fas induces hepatic chemokines and promotes inflammation by an NF-kappa B-independent, caspase-3-dependent pathway. J Biol Chem. 2001;276:49077–49082
  40. Jaeschke H. Inflammation in response to hepatocellular apoptosis. Hepatology. 2002;35:964–966
  41. Mizuhara H, O’Neil E, Seki N, Ogawa T, Kusunoki C, Otsuka K, et al. T cell activation-associated hepatic injury (mediation by tumor necrosis factors and protection by interleukin-6). J Exp Med. 1994;179:1529–1537
  42. Galun E, Zeira E, Pappo O, Peters M, Rose-John S. Liver regeneration induced by a designer human IL6/sIL-6R fusion protein reverses severe hepatocellular injury. FASEB J. 2000;14:1979–1987
  43. Hecht N, Pappo O, Shouval D, Rose-John S, Galun E, Axelrod JH. Hyper-IL-6 gene therapy reverses fulminant hepatic failure. Mol Ther. 2001;3:683–687

☆ Supported by an FIS grant from the Ministerio de Sanidad y Consumo 01/723 (to M.B.), grant from the Gobierno de Navarra (to M.B.), and grant SAF 2002-0327 from the Ministerio de Sanidad y Consumo (to J.P.) and Instituto de Salud Carlos III C02/03. N.B. was supported by the FIS.

PII: S0016-5085(03)00698-X

doi: 10.1016/S0016-5085(03)00698-X

Gastroenterology
Volume 125, Issue 1 , Pages 192-201 , July 2003

Article Tools

* Image Usage & Resolution