Active matrix metalloproteinase-2 promotes apoptosis of hepatic stellate cells via the cleavage of cellular N-cadherin

Liver International

Volumn 29, Issue 7, 2009, Pages 966-978

  Hartland, Stephen N ^a   Murphy, Frank ^b   Aucott, Rebecca L ^a   Abergel, Armand ^b   Zhou, Xiaoying ^b   Waung, Julian ^b   Patel, Nishit ^b   Bradshaw, Catherine ^a   Collins, Jane ^c   Mann, Derek ^c   Benyon, R Christopher ^b   Iredale, John P ^a  

^a UNIVERSITY OF EDINBURGH   (United Kingdom)

^b UNIVERSITY OF SOUTHAMPTON   (United Kingdom)

^c NEWCASTLE UNIVERSITY   (United Kingdom)

Author keywords

Apoptosis; Hepatic stellate cell; Matrix metalloproteinase; N cadherin

Indexed keywords

GELATINASE A; GLIOTOXIN; NERVE CELL ADHESION MOLECULE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; CELL ACTIVATION; CELL CULTURE; CELL SURFACE; CELL SURVIVAL; CONTROLLED STUDY; ENZYME ACTIVATION; HUMAN; HUMAN CELL; IN VITRO STUDY; ITO CELL; LIVER FIBROSIS; NONHUMAN; PROTEIN BINDING; PROTEIN CLEAVAGE; PROTEIN DEGRADATION; PROTEIN EXPRESSION; PROTEIN FUNCTION; RAT; STELLATE CELL; UPREGULATION;

ANIMALS; ANTIGENS, CD; APOPTOSIS; CADHERINS; CARBON TETRACHLORIDE; CASPASE 3; CELLS, CULTURED; CYCLOHEXIMIDE; ENZYME ACTIVATION; GLIOTOXIN; HEPATIC STELLATE CELLS; HUMANS; LIVER; LIVER CIRRHOSIS, EXPERIMENTAL; MATRIX METALLOPROTEINASE 2; MICE; MICE, INBRED C57BL; RATS; RECOMBINANT PROTEINS; SIGNAL TRANSDUCTION; TIME FACTORS;

EID: 67650474244     PISSN: 14783223     EISSN: 14783231     Source Type: Journal    
DOI: 10.1111/j.1478-3231.2009.02070.x     Document Type: Article

References (56)

1. Clark RA. Regulation of fibroplasia in cutaneous wound repair. Am J Med Sci 1993; 306: 42-8.
2. Iredale JP, Benyon RC, Pickering J, et al. Mechanisms of spontaneous resolution of rat liver fibrosis: Hepatic stellate cell apoptosis and reduced hepatic expression of metalloproteinase inhibitors. J Clin Invest 1998; 102: 538-49.
3. Duffield JS, Erwig LP, Wei X, et al. Activated macrophages direct apoptosis and suppress mitosis of mesangial cells. J Immunol 2000; 164: 2110-9.
4. Issa R, Zhou X, Constandinou CM, et al. Spontaneous recovery from micronodular cirrhosis: Evidence for incomplete resolution associated with matrix cross-linking. Gastroenterology 2004; 126: 1795-808.
5. Wu WB, Huang TF. Activation of MMP-2, cleavage of matrix proteins and adherens junctions during a snake venom metalloproteinase-induced endothelial cell apoptosis. Exp Cell Res 2003; 288: 143-57.
6. Menon B, Singh M, Ross RS, Johnson JN, Singh K. β-adrenergic receptor-stimulated apoptosis in adult cardiac myocytes involves MMP-2-mediated disruption of β 1 integrin signalling and mitochondrial pathway. Am J Physiol Cell Physiol 2006; 290: C254-61.
7. Covington MD, Burghardt RC, Parrish AR. Ischemia-induced cleavage of cadherins in NRK cells requires MT1-MMP (MMP-14). Am J Physiol Renal Physiol 2006; 290: F43-51.
8. Alexander CM, Howard EW, Bissell MJ, Werb Z. Rescue of mammary epithelial cell apoptosis and entactin degradation by a tissue inhibitor of metalloproteinases-1 transgene. J Cell Biol 1996; 135: 1669-77.
9. Takeichi M. Morphogenetic roles of classic cadherins. Curr Opin Cell Biol 1995; 7: 619-27.
10. Steinberg MS, McNutt PM. Cadherins and their connections: Adhesion junctions have broader functions. Curr Opin Cell Biol 1999; 11: 554-60.
11. Linask KK, Ludwig C, Han MD, et al. Cadherin/catenin-mediated morphoregulation of somite formation. Dev Biol 1998; 202: 85-102.
12. Gumbiner BM. Cell adhesion: The molecular basis of tissue architecture and morphogenesis. Cell 1996; 84: 345-57.
13. Huber O, Bierkamp C, Kemler R. Cadherins and catenins in development. Curr Opin Cell Biol 1996; 8: 685-91.
14. Vleminckx K, Kemler R. Cadherins and tissue formation: Integrating adhesion and signaling. Bioessays 1999; 21: 211-20.
15. Lochter A, Galosy S, Muschler J, et al. Matrix metalloproteinase stromelysin-1 triggers a cascade of molecular alterations that leads to stable epithelial-to-mesenchymal conversion and a premalignant phenotype in mammary epithelial cells. J Cell Biol 1997; 139: 1861-72.
16. Lochter A, Srebrow A, Sympson CJ, et al. Misregulation of stromelysin-1 expression in mouse mammary tumor cells accompanies acquisition of stromelysin-1-dependent invasive properties. J Biol Chem 1997; 272: 5007-15.
17. Sternlicht MD, Lochter A, Sympson CJ, et al. The stromal proteinase MMP3/ stromelysin-1 promotes mammary carcinogenesis. Cell 1999; 98: 137-46.
18. Takahashi A, Musy PY, Martins LM, et al. CrmA/SPI-2 inhibition of an endogenous ICE-related protease responsible for lamin A cleavage and apoptotic nuclear fragmentation. J Biol Chem 1996; 271: 32487-90.
19. Herren B, Levkau B, Raines EW, Ross R. Cleavage of beta-catenin and plakoglobin and shedding of VE-cadherin during endothelial apoptosis: evidence for a role for caspases and metalloproteinases. Mol Biol Cell 1998; 9: 1589-601.
20. Pon YL, Auersperg N, Wong AST. Gonadotropins regulate N-cadherin-mediated human ovarian surface epithelial cell survival at both post-translational and transcriptional levels through a cyclic AMP/ protein kinase A pathway. J Biol Chem 2005; 280: 15438-48.
21. Ho AT, Voura EB, Soloway PD, Watson KL, Khokha R. MMP inhibitors augment fibroblast adhesion through stabilization of focal adhesion contacts and up-regulation of cadherin function. J Biol Chem 2001; 276: 40215-24.
22. Clunn GF, Refson JS, Lymn JS, Hughes AD. Platelet-derived growth factor beta-receptors can both promote and inhibit chemotaxis in human vascular smooth muscle cells. Arterioscler Thromb Vasc Biol 1997; 17: 2622-9.
23. Koutsouki E, Beeching CA, Slater SC, et al. N-cadherin-dependent cell-cell contacts promote human saphenous vein smooth muscle cell survival. Arterioscler Thromb Vasc Biol 2005; 25: 982-8.
24. Bennett MR, Evan GI, Schwartz SM. Apoptosis of human vascular smooth muscle cells derived form normal vessels and coronary atherosclerotic plaques. J Clin Invest 1995; 95: 2266-74.
25. Bennett MR, Boyle JJ. Apoptosis of vascular smooth muscle cells in atherosclerosis. Atherosclerosis 1998; 138: 3-9.
26. Hermiston ML, Gordon JI. In vivo analysis of cadherin function in the mouse intestinal epithelium: Essential roles in adhesion, maintenance of differentiation, and regulation of programmed cell death. J Cell Biol 1995; 129: 489-506.
27. Kantak SS, Kramer RH. E-cadherin regulates anchorage-independent growth and survival in oral squamous cell carcinoma cells. J Biol Chem 1998; 273: 16953-61.
28. Trolice MP, Pappalardo A, Peluso JJ. Basic fibroblast growth factor and N-cadherin maintain rat granulosa cell and ovarian surface epithelial cell viability by stimulating the tyrosine phosphorylation of the fibroblast growth factor receptors. Endocrinology 1997; 138: 107-13.
29. Blaschuk OW, Rowlands TM. Plasma membrane components of adherens junctions. Mol Membr Biol 2002; 19: 75-80.
30. Erez N, Zamir E, Gour BJ, Blaschuk OW, Geiger B. Induction of apoptosis in endothelial cells by cadherin antagonist peptide: Involvement of fibroblast growth factor receptor-mediated signaling. Exp Cell Res 2004; 294: 366-78.
31. Tran N, Adams DG, Vaillancourt RR, Heimark RL. Signal transduction from N-cadherin increases Bcl-2. Regulation of the phosphattidylinositol 3-kinase/Akt pathway by homophilic adhesion and actin cytoskeletal organization. J Biol Chem 2002; 277: 32905-14.
32. Williams EJ, Furness J, Walsh FS, Doherty P. Activation of the FGF receptor underlies neurite outgrowth stimulated by L1, N-CAM and N-cadherin. Neuron 1994; 13: 583-94.
33. Peluso JJ. Putative mechanism through which N-cadherin-mediated cell contact maintains calcium homeostasis and thereby prevents ovarian cells from undergoing apoptosis. Biochem Pharmocol 1997; 54: 847-53.
34. Suyama K, Shapiro I, Guttman M, Hazan RB. A signalling pathway leading to metastasis is controlled by N-cadherin and the FGF receptor. Cancer Cell 2002; 2: 301-14.
35. Zhou X, Hovell CJ, Pawley S, et al. Expression of matrix metalloproteinase-2 and -14 persists during early resolution of experimental liver fibrosis and might contribute to fibrolysis. Liver Int 2004; 24: 492-501.
36. Iredale JP, Murphy G, Hembry RM, Friedman SL, Arthur MJP. Human hepatic lipocytes synthesize tissue inhibitor of metalloproteinases-1 (TIMP-1): implications for regulation of matrix degradation in liver. J Clin Invest 1992; 90: 282-7.
37. Preaux AM, D'ortho MP, Bralet MP, Laperche Y, Mavier P. Apoptosis of human hepatic myofibroblasts promotes activation of matrix metalloproteinase-2. Hepatology 2002; 36: 615-22.
38. Iredale JP, Goddard S, Murphy G, Benyon RC, Arthur MJP. Tissue inhibitor of metalloproteinase-1 and interstitial collagenase expression in autoimmune chronic active hepatitis and activated human hepatic lipocytes. Clin Sci 1995; 89: 75-81.
39. Arthur MJP, Friedman SL, Roll FJ, Bissell DM. Lipocytes from normal rat liver release a neutral metalloproteinase that degrades basement membrane (type IV) collagen. J Clin Invest 1989; 84: 1076-85.
40. Murphy FR, Issa R, Zhou X, et al. Inhibition of apoptosis of activated hepatic stellate cells by tissue inhibitor of metalloproteinase-1 is mediated via effects on matrix metalloproteinase inhibition. Implications for reversibility of liver fibrosis. J Biol Chem 2002; 277: 11069-76.
41. Wright MC, Issa R, Smart DE, et al. Gliotoxin stimulates the apoptosis of human and rat hepatic stellate cells and enhances the resolution of liver fibrosis in rats. Gastroenterology 2001; 121: 685-98.
42. Emonard H, Marcq V, Mirand C, Hornebeck W. Inhibition of gelatinase A by oleic acid. Ann NY Acad Sci 1999; 878: 647-9.
43. Williams G, Williams EJ, Doherty P. Dimeric versions of two short N-cadherin binding motifs (HAVDI and INPISG) function as N-cadherin agonists. J Biol Chem 2002; 277: 4361-7.
44. McQuibban GA, Gong JH, Tam EM, et al. Inflammation dampened by gelatinase A cleavage of monocyte chemoattractant protein-3. Science 2000; 289: 1202-6.
45. Williams LM, Gibbons DL, Gearing A, et al. Paradoxical effects of a synthetic metalloproteinase inhibitor that blocks both p55 and p75 TNF receptor shedding and TNF alpha processing in RA synovial membrane cell cultures. J Clin Invest 1996; 97: 2833-41.
46. Issa R, Zhou X, Trim N, et al. Mutation in collagen-I that confers resistance to the action of collagenase results in failure of recovery from CCl4-induced liver fibrosis, persistence of activated hepatic stellate cells, and diminished hepatocyte regeneration. FASEB J 2002; 17: 47-9.
47. Senoo H, Imai K, Sato M, et al. Three-dimensional structure of extracellular matrix reversibly regulates morphology, proliferation and collagen metabolism of perisinusoidal stellate cells (vitamin A-storing cells). Cell Biol Int 1996; 20: 501-12.
48. Bergin E, Levine JS, Koh JS, Lieberthal W. Mouse proximal tubular cell-cell adhesion inhibits apoptosis by a cadherin-dependent mechanism. Am J Physiol Renal Physiol 2000; 278: F758-68.
49. Utton MA, Eickolt B, Howell FV, Wallis J, Doherty P. Soluble N-cadherin stimulates fibroblast growth factor receptor dependent neurite outgrowth and N-cadherin and the fibroblast growth factor receptor co-cluster in cells. J Neurochem 2001; 76: 1421-30.
50. Klint P, Kanda S, Claesson-Welsh L. Shc and a novel 89-kDa component couple to the Grb2-Sos complex in fibroblast growth factor-2-stimulated cells. J Biol Chem 1995; 270: 23337-44.
51. Nagase H, Woessner JF. Jr. Matrix metalloproteinases. J Biol Chem 1999; 274: 21491-4.
52. Chen EI, Kridel SJ, Howard EW, et al. A unique substrate recognition profile for matrix metalloproteinase-2. J Biol Chem 2002; 277: 4485-91.
53. Boudreau N, Sympson CJ, Werb Z, Bissell MJ. Suppression of ICE and apoptosis in mammary epithelial cells by extracellular matrix. Science 1995; 267: 891-3.
54. Pereira AMM, Strasberg-Rieber M, Rieber M. Invasion-associated MMP-2 and MMP-9 are up-regulated intracellularly in concert with apoptosis linked to melanoma cell detachment. Clin Exp Metastasis 2005; 22: 285-95.
55. Bian J, Sun Y. Transcriptional activation by p53 of the human type IV collagenase (gelatinase A or matrix metalloproteinase 2) promoter. Mol Cell Biol 1997; 17: 6330-8.
56. Salgado S, Garcia J, Vera J, et al. Liver cirrhosis is reverted by urokinase-type plasminogen activator gene therapy. Mol Ther 2000; 2: 545-51.