Membrane independent activation of fibroblast proMMP-2 by snake venom: Novel roles for venom proteinases

Toxicon

Volumn 44, Issue 7, 2004, Pages 749-764

  Saravia Otten, Patricia ^a,b   Frisan, Teresa ^a   Thelestam, Monica ^a   Gutiérrez, José María ^c  

^a KAROLINSKA INSTITUTE   (Sweden)

^b Univ S Carlos Guatemala Guatemala   (Guatemala)

^c UNIVERSIDAD DE COSTA RICA   (Costa Rica)

Author keywords

Bothrops asper; Human fibroblasts; Metalloproteinases; MMP 2 activation; Serine proteinases; Snake venom

Indexed keywords

EDETIC ACID; GELATINASE A; SNAKE VENOM;

ACUTE TOXICITY; ANIMAL TISSUE; APOPTOSIS; ARTICLE; CONCENTRATION RESPONSE; CONTROLLED STUDY; CYTOTOXICITY; ENZYME ACTIVATION; ENZYME ACTIVITY; FIBROBLAST; HUMAN; HUMAN CELL; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN EXPRESSION;

ANIMALS; BLOTTING, NORTHERN; BLOTTING, WESTERN; BOTHROPS; CELLS, CULTURED; CROTALID VENOMS; DNA PRIMERS; ENZYME ACTIVATION; ENZYME PRECURSORS; EXTRACELLULAR MATRIX; FIBROBLASTS; GELATINASES; HUMANS; L-LACTATE DEHYDROGENASE; METALLOENDOPEPTIDASES; MICE; MUSCLE, SKELETAL;

BOTHROPS; BOTHROPS ASPER; MAMMALIA; SERPENTES;

EID: 6944227500     PISSN: 00410101     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.toxicon.2004.08.002     Document Type: Article

References (68)

1. M.S. Agren Gelatinase activity during wound healing Br. J. Dermatol. 131 1994 634 640
2. R.T. Aimes, and J.P. Quigley Matrix metalloproteinase-2 is an interstitial collagenase. Inhibitor-free enzyme catalyzes the cleavage of collagen fibrils and soluble native type I collagen generating the specific 3/4- and 1/4-length fragments J. Biol. Chem. 270 1995 5872 5876
3. F. Aragón-Ortiz, and F. Gubensek Characterization of thrombin-like proteinase from Bothrops asper venom P. Rosenberg Toxins: Animal, Plant and Microbial 1978 Pergamon Press Oxford 107
4. S. Araki, T. Ishida, T. Yamamoto, K. Kaji, and H. Hayashi Induction of apoptosis by hemorrhagic snake venom in vascular endothelial cells Biochem. Biophys. Res. Commun. 190 1993 148 153
5. V. Arce, F. Brenes, and J.M. Gutiérrez Degenerative and regenerative changes in murine skeletal muscle after injection of venom from the snake Bothrops asper: a histochemical and immunocytochemical study Int. J. Exp. Pathol. 72 1991 211 226
6. E.N. Baramova, K. Bajou, A. Remacle, C. L'Hoir, H.W. Krell, U.H. Weidle, A. Noel, and J.M. Foidart Involvement of PA/plasmin system in the processing of pro-MMP-9 and in the second step of pro-MMP-2 activation FEBS Lett. 405 1997 157 162
7. H. Birkedal-Hansen Proteolytic remodeling of extracellular matrix Curr. Opin. Cell Biol. 7 1995 728 735
8. J.B. Bjarnason, and J.W. Fox Hemorrhagic metalloproteinases from snake venoms Pharmacol. Ther. 62 1994 325 372
9. M.L. Corcoran, R.E. Hewitt, D.E. Kleiner Jr, and W.G. Stetler-Stevenson MMP-2: expression, activation and inhibition Enzyme Protein. 49 1996 7 19
10. H.C. Crawford, and L.M. Matrisian Tumor and stromal expression of matrix metalloproteinases and their role in tumor progression Invasion Metastasis 14 1994 234 245
11. C.J. Edgell, C.C. McDonald, and J.B. Graham Permanent cell line expressing human factor VIII-related antigen established by hybridization Proc. Natl Acad. Sci. USA. 80 1983 3734 3737
12. E. El Fahime, Y. Torrente, N.J. Caron, M.D. Bresolin, and J.P. Tremblay In vivo migration of transplanted myoblasts requires matrix metalloproteinase activity Exp. Cell Res. 258 2000 279 287
13. Z.S. Galis, R. Kranzhofer, J.W. Fenton, and P. Libby Thrombin promotes activation of matrix metalloproteinase-2 produced by cultured vascular smooth muscle cells Arterioscler. Thromb. Vasc. Biol. 17 1997 483 489
14. P.G. Gallagher, Y. Bao, S.M. Serrano, A.S. Kamiguti, R.D. Theakston, and J.W. Fox Use of microarrays for investigating the subtoxic effects of snake venoms: insights into venom-induced apoptosis in human umbilical vein endothelial cells Toxicon 41 2003 429 440
15. C. Gilles, M. Polette, M. Seiki, P. Birembaut, and E.W. Thompson Implication of collagen type I-induced membrane-type 1-matrix metalloproteinase expression and matrix metalloproteinase-2 activation in the metastatic progression of breast carcinoma Lab. Invest. 76 1997 651 660
16. J. Gutiérrez Clinical toxicology of snakebites in Central America J. Meier J. White Handbook of Clinical Toxicology of Animal Venoms and Poisons 1995 CRC Press Florida 645 665
17. 2 myotoxins from Bothrops snake venoms Toxicon. 33 1995 1405 1424
18. J.M. Gutiérrez, and B. Lomonte Efectos locales en el envenenamiento ofídico en América Latina J.L.C. Cardoso F.O.S. Franca F.H. Wen C.M.S. Málaque V. Daddad Animais Peconhentos no Brasil. Biologia, Clínica e Terapéutica dos Acidentes 2003 Sarvier Sao Paulo 310 323
19. 2: insights into the mechanism of local and systemic myotoxicity Toxicon 42 2003 915 931
20. J.M. Gutiérrez, and A. Rucavado Snake venom metalloproteinases: their role in the pathogenesis of local tissue damage Biochimie 82 2000 841 850
21. J.M. Gutiérrez, M. Romero, C. Díaz, G. Borkow, and M. Ovadia Isolation and characterization of a metalloproteinase with weak hemorrhagic activity from the venom of the snake Bothrops asper Terciopelo Toxcon 33 1995 19 29
22. D. Ingber How cells (might) sense microgravity FASEB J. 13 1999 S3 15
23. E.H. Kerkvliet, I.C. Jansen, T. Schoenmaker, W. Beertsen, and V. Everts Collagen type I, III and V differently modulate synthesis and activation of matrix metalloproteinases by cultured rabbit periosteal fibroblasts Matrix Biol. 22 2003 217 227
24. S. Kherif, C. Lafuma, M. Dehaupas, S. Lachkar, J.G. Fournier, M. Verdiere-Sahuque, M. Fardeau, and H.S. Alameddine Expression of matrix metalloproteinases 2 and 9 in regenerating skeletal muscle: a study in experimentally injured and mdx muscles Dev. Biol. 205 1999 158 170
25. D.E. Kleiner Jr, A. Tuuttila, K. Tryggvason, and W.G. Stetler-Stevenson Stability analysis of latent and active 72-kDa type IV collagenase: the role of tissue inhibitor of metalloproteinases-2 (TIMP-2) Biochemistry 32 1993 1583 1592
26. H. Kolkenbrock, A. Hecker-Kia, D. Orgel, W. Ruppitsch, and N. Ulbrich Activity of ternary gelatinase A-TIMP-2-matrix metallo-proteinase complexes Biol. Chem. Hoppe Seyler. 375 1994 589 595
27. T. Koshiba, R. Hosotani, M. Wada, Y. Miyamoto, K. Fujimoto, J.U. Lee, R. Doi, S. Arii, and M. Imamura Involvement of matrix metalloproteinase-2 activity in invasion and metastasis of pancreatic carcinoma Cancer 82 1998 642 650
28. U.K. Laemmli Cleavage of structural proteins during the assembly of the head of bacteriophage T4 Nature 227 1970 680 685
29. M.A. Lafleur, M.D. Hollenberg, S.J. Atkinson, V. Knauper, G. Murphy, and D.R. Edwards Activation of pro-(matrix metalloproteinase-2) (pro-MMP-2) by thrombin is membrane-type-MMP-dependent in human umbilical vein endothelial cells and generates a distinct 63 kDa active species Biochem. J. 357 2001 107 115
30. F.S. Markland Snake venoms and the hemostatic system Toxicon 36 1998 1749 1800
31. B.C. McKaig, D. McWilliams, S.A. Watson, and Y.R. Mahida Expression and regulation of tissue inhibitor of metalloproteinase-1 and matrix metalloproteinases by intestinal myofibroblasts in inflammatory bowel disease Am. J. Pathol. 162 2003 1355 1360
32. J. Meier, and K.F. Stocker Biology and distribution of venomous snakes of medical importance and the composition of snake venoms J. Meier J. White Handbook of Clinical Toxicology of Animal Venoms and Poisons 1995 CRC Press Florida 367 412
33. S. Monea, K. Lehti, J. Keski-Oja, and P. Mignatti Plasmin activates pro-matrix metalloproteinase-2 with a membrane-type 1 matrix metalloproteinase-dependent mechanism J. Cell Physiol. 192 2002 160 170
34. M.A. Moses, M. Marikovsky, J.W. Harper, P. Vogt, E. Eriksson, M. Klagsbrun, and R. Langer Temporal study of the activity of matrix metalloproteinases and their endogenous inhibitors during wound healing J. Cell Biochem. 60 1996 379 386
35. B.E. Muhs, G. Plitas, Y. Delgado, I. Ianus, J.P. Shaw, M.A. Adelman, P. Lamparello, P. Shamamian, and P. Gagne Temporal expression and activation of matrix metalloproteinases-2, -9, and membrane type 1-matrix metalloproteinase following acute hindlimb ischemia J. Surg. Res. 111 2003 8 15
36. G. Murphy, H. Stanton, S. Cowell, G. Butler, V. Knauper, S. Atkinson, and J. Gavrilovic Mechanisms for pro matrix metalloproteinase activation APMIS 107 1999 38 44
37. H. Nagase, and J.F. Woessner Jr Matrix metalloproteinases J. Biol. Chem. 274 1999 21491 21494
38. M. Nguyen, J. Arkell, and C.J. Jackson Thrombin rapidly and efficiently activates gelatinase A in human microvascular endothelial cells via a mechanism independent of active MT1 matrix metalloproteinase Lab. Invest. 79 1999 467 475
39. M. Nguyen, J. Arkell, and C.J. Jackson Activated protein C directly activates human endothelial gelatinase A J. Biol. Chem. 275 2000 9095 9098
40. M. Nguyen, J. Arkell, and C.J. Jackson Human endothelial gelatinases and angiogenesis Int. J. Biochem. Cell Biol. 33 2001 960 970
41. T. Nikai, and Y. Komori Kinin-releasing and kinin-degrading enzymes G.S. Bailey Enzymes from Snake Venom 1998 Alakken Fort Collins, USA 287 316
42. H. Nomura, H. Sato, M. Seiki, M. Mai, and Y. Okada Expression of membrane-type matrix metalloproteinase in human gastric carcinomas Cancer Res. 55 1995 3263 3266
43. V.L. Petricevich, C.F. Teixeira, D.V. Tambourgi, and J.M. Gutiérrez Increments in serum cytokine and nitric oxide levels in mice injected with Bothrops asper and Bothrops jararaca snake venoms Toxicon 38 2000 1253 1266
44. A.M. Preaux, M.P. D'Ortho, M.P. Bralet, Y. Laperche, and P. Mavier Apoptosis of human hepatic myofibroblasts promotes activation of matrix metalloproteinase-2 Hepatology 36 2002 615 622
45. N. Ruangpanit, D. Chan, K. Holmbeck, H. Birkedal-Hansen, J. Polarek, C. Yang, J.F. Bateman, and E.W. Thompson Gelatinase A (MMP-2) activation by skin fibroblasts: dependence on MT1-MMP expression and fibrillar collagen form Matrix Biol. 20 2001 193 203
46. A. Rucavado, B. Lomonte, M. Ovadia, and J.M. Gutierrez Local tissue damage induced by BaP1, a metalloproteinase isolated from Bothrops asper (Terciopelo) snake venom Exp. Mol. Pathol. 63 1995 186 199
47. A. Rucavado, J. Nuñez, and J.M. Gutiérrez Blister formation and skin damage induced by BaP1, a haemorrhagic metalloproteinase from the venom of the snake Bothrops asper Int. J. Exp. Pathol. 79 1998 245 254
48. A. Rucavado, T. Escalante, C.F. Teixeira, C.M. Fernandes, C. Díaz, and J.M. Gutiérrez Increments in cytokines and matrix metalloproteinases in skeletal muscle after injection of tissue-damaging toxins from the venom of the snake Bothrops asper Mediators Inflamm. 11 2002 121 128
49. T. Salo, M. Makela, M. Kylmaniemi, H. Autio-Harmainen, and H. Larjava Expression of matrix metalloproteinase-2 and -9 during early human wound healing Lab. Invest. 70 1994 176 182
50. J. Sambrok, E.F. Fritsch, and T. Maniatis Molecular Cloning: A Laboratory Manual 1989 Cold Spring Harbor Laboratory Press Cold Spring Harbor, NY
51. H. Sato, T. Takino, Y. Okada, J. Cao, A. Shinagawa, E. Yamamoto, and M. Seiki A matrix metalloproteinase expressed on the surface of invasive tumour cells Nature 370 1994 61 65
52. M. Seiki Membrane-type matrix metalloproteinases APMIS 107 1999 137 143
53. P. Shamamian, J.D. Schwartz, B.J. Pocock, S. Monea, D. Whiting, S.G. Marcus, and P. Mignatti Activation of progelatinase A (MMP-2) by neutrophil elastase, cathepsin G, and proteinase-3: a role for inflammatory cells in tumor invasion and angiogenesis J. Cell Physiol. 189 2001 197 206
54. A.J. Singer, and R.A. Clark Cutaneous wound healing N. Engl. J. Med. 341 1999 738 746
55. H. Smolian, A. Aurer, M. Sittinger, J. Zacher, J.P. Bernimoulin, G.R. Burmester, and H. Kolkenbrock Secretion of gelatinases and activation of gelatinase A (MMP-2) by human rheumatoid synovial fibroblasts Biol. Chem. 382 2001 1491 1499
56. C. Soo, W.W. Shaw, X. Zhang, M.T. Longaker, E.W. Howard, and K. Ting Differential expression of matrix metalloproteinases and their tissue-derived inhibitors in cutaneous wound repair Plast. Reconstr. Surg. 105 2000 638 647
57. M.D. Sternlicht, and Z. Werb How matrix metalloproteinases regulate cell behavior Annu. Rev. Cell Dev. Biol. 17 2001 463 516
58. W.G. Stetler-Stevenson, R. Hewitt, and M. Corcoran Matrix metalloproteinases and tumor invasion: from correlation and causality to the clinic Semin. Cancer Biol. 7 1996 147 154
59. C. Streuli Extracellular matrix remodelling and cellular differentiation Curr. Opin. Cell Biol. 11 1999 634 640
60. K. Suzuki, M. Nakamura, Y. Hatanaka, Y. Kayanoki, H. Tatsumi, and N. Taniguchi Induction of apoptotic cell death in human endothelial cells treated with snake venom: implication of intracellular reactive oxygen species and protective effects of glutathione and superoxide dismutases J. Biochem. 122 1997 1260 1264
61. K. Tokunaga, Y. Nakamura, K. Sakata, K. Fujimori, M. Ohkubo, K. Sawada, and S. Sakiyama Enhanced expression of a glyceraldehyde-3-phosphate dehydrogenase gene in human lung cancers Cancer Res. 47 1987 5616 5619
62. N.J. Trengove, M.C. Stacey, S. MacAuley, N. Bennett, J. Gibson, F. Burslem, G. Murphy, and G. Schultz Analysis of the acute and chronic wound environments: the role of proteases and their inhibitors Wound Repair Regen. 7 1999 442 452
63. K. Tsuji, K. Uno, G.X. Zhang, and M. Tamura Periodontal ligament cells under intermittent tensile stress regulate mRNA expression of osteoprotegerin and tissue inhibitor of matrix metalloprotease-1 and -2 J. Bone Miner. Metab. 22 2004 94 103
64. T.H. Vu, and Z. Werb Gelatinase B. structure, regulation and function 1998 Academic Press San Diego
65. T.H. Vu, J.M. Shipley, G. Bergers, J.E. Berger, J.A. Helms, D. Hanahan, S.D. Shapiro, R.M. Senior, and Z. Werb MMP-9/gelatinase B is a key regulator of growth plate angiogenesis and apoptosis of hypertrophic chondrocytes Cell 93 1998 411 422
66. J.F. Woessner Jr Matrix metalloproteinases and their inhibitors in connective tissue remodeling FASEB J. 5 1991 2145 2154
67. W.B. Wu, and T.F. Huang Activation of MMP-2, cleavage of matrix proteins, and adherens junctions during a snake venom metalloproteinase-induced endothelial cell apoptosis Exp. Cell Res. 288 2003 143 157
68. S. Zucker, C. Conner, B.I. DiMassmo, H. Ende, M. Drews, M. Seiki, and W.F. Bahou Thrombin induces the activation of progelatinase A in vascular endothelial cells. Physiologic regulation of angiogenesis J. Biol. Chem. 270 1995 23730 23738