Hemorrhagic activity of HF3, a snake venom metalloproteinase: Insights from the proteomic analysis of mouse skin and blood plasma

Journal of Proteome Research

Volumn 11, Issue 1, 2012, Pages 279-291

  Paes Leme, Adriana F ^a,b   Sherman, Nicholas E ^c   Smalley, David M ^c   Sizukusa, Letícia O ^a   Oliveira, Ana K ^a   Menezes, Milene C ^a   Fox, Jay W ^c   Serrano, Solange M T ^a  

^a INSTITUTO BUTANTAN   (Brazil)

^b BRAZILIAN CENTER FOR RESEARCH IN ENERGY AND MATERIALS CNPEM   (Brazil)

^c UNIVERSITY OF VIRGINIA   (United States)

Author keywords

Hemorrhage; metalloproteinase; peptidome; plasma; proteome; skin; snake venom

Indexed keywords

ALPHA 2 MICROGLOBULIN; BETA GLOBIN; CARBONATE DEHYDRATASE III; COLLAGEN; COLLAGEN TYPE 1; COLLAGEN TYPE 2; COLLAGEN TYPE 4; COLLAGEN TYPE 6; CREATINE KINASE M TYPE; CYTOSKELETON PROTEIN; DECORIN; DESMOYOKIN; ELONGATION FACTOR 1 ALPHA1; FIBRONECTIN; FILAGGRIN; HEMOGLOBULIN BETA2; HEMOPEXIN; HF3 PROTEIN; HIGH MOBILITY GROUP PROTEIN B1; LUMICAN; METALLOPROTEINASE; MIMECAN; PROTEINASE INHIBITOR; PROTEOGLYCAN; PROTON TRANSPORTING ADENOSINE TRIPHOSPHATE SYNTHASE; SEROTRANSFERRIN; SERUM ALBUMIN; SNAKE VENOM; TROPOMYOSIN 1 ALPHA; UNCLASSIFIED DRUG; VIMENTIN;

ARTICLE; BLEEDING; FIBRIN FORMATION; HEMOSTASIS; HYDROLYSIS; IN VIVO STUDY; MALE; MOUSE; NONHUMAN; PLASMA; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEOMICS; SKIN; TISSUE INJURY;

ANIMALS; BLOOD PROTEINS; BOTHROPS; CROTALID VENOMS; ELECTROPHORESIS, GEL, TWO-DIMENSIONAL; HEMORRHAGE; MALE; METALLOPROTEASES; MICE; MUSCLE, SKELETAL; PEPTIDE FRAGMENTS; PEPTIDE MAPPING; PROTEOLYSIS; PROTEOME; SKIN; TANDEM MASS SPECTROMETRY;

BOTHROPS JARARACA;

EID: 84855544503     PISSN: 15353893     EISSN: 15353907     Source Type: Journal    
DOI: 10.1021/pr2006439     Document Type: Article

References (55)

1. Ownby, C. L.; Bjarnason, J.; Tu, A. T. Hemorrhagic toxins from rattlesnake (Crotalus atrox) venom. Pathogenesis of hemorrhage induced by three purified toxins Am. J. Pathol. 1978, 93, 201-218 (Pubitemid 9025512)
2. Ohsaka, A.; Ikezawa, H.; Kondo, H.; Kondo, S.; Uchida, N. Haemorrhagic activities of habu snake venom, and their relations to lethal toxicity, proteolytic activities and other pathological activities Br. J. Exp. Pathol. 1960, 41, 478-486
3. Bjarnason, J. B.; Fox, J. W. Hemorrhagic metalloproteinases from snake venoms Pharmacol. Ther. 1994, 62, 325-372 (Pubitemid 24248422)
4. White, J. Snake venoms and coagulopathy Toxicon 2005, 45, 951-967 (Pubitemid 40732573)
5. Gutiérrez, J. M.; Rucavado, A.; Escalante, T.; Díaz, C. Hemorrhage induced by snake venom metalloproteinases: biochemical and biophysical mechanisms involved in microvessel damage Toxicon 2005, 45, 997-1011 (Pubitemid 40732576)
6. Bjarnason, J. B.; Fox, J. W. Snake venom metalloendopeptidases: reprolysins Methods Enzymol. 1995, 248, 345-368
7. Fox, J. W.; Serrano, S. M. Insights into and speculations about snake venom metalloproteinase (SVMP) synthesis, folding and disulfide bond formation and their contribution to venom complexity FEBS J. 2008, 275, 3016-3030 (Pubitemid 351743588)
8. White, J. M. ADAMs: modulators of cell-cell and cell-matrix interactions Curr. Opin. Cell Biol. 2003, 15, 598-606 (Pubitemid 37176969)
9. Tang, B. L.; Hong, W. ADAMTS: a novel family of proteases with an ADAM protease domain and thrombospondin 1 repeats FEBS Lett. 1999, 445, 223-225 (Pubitemid 29117216)
10. Baramova, E. N.; Shannon, J. D.; Bjarnason, J. B.; Fox, J. W. Degradation of extracellular matrix proteins by hemorrhagic metalloproteinases Arch. Biochem. Biophys. 1989, 275, 63-71 (Pubitemid 19280687)
11. Shannon, J. D.; Baramova, E. N.; Bjarnason, J. B.; Fox, J. W. Amino acid sequence of a Crotalus atrox venom metalloproteinase which cleaves type IV collagen and gelatin J. Biol. Chem. 1989, 264, 11575-11583 (Pubitemid 19185322)
12. Jia, L. G.; Wang, X. M.; Shannon, J. D.; Bjarnason, J. B.; Fox, J. W. Inhibition of platelet aggregation by the recombinant cysteine-rich domain of the hemorrhagic snake venom metalloproteinase, atrolysin A Arch. Biochem. Biophys. 2000, 373, 281-286 (Pubitemid 30046516)
13. Zigrino, P.; Kamiguti, A. S.; Eble, J.; Drescher, C.; Nischt, R.; Fox, J. W.; Mauch, C. The reprolysin jararhagin, a snake venom metalloproteinase, functions as a fibrillar collagen agonist involved in fibroblast cell adhesion and signaling J. Biol. Chem. 2002, 277, 40528-40535 (Pubitemid 35215631)
14. Kamiguti, A. S.; Gallagher, P.; Marcinkiewicz, C.; Theakston, R. D.; Zuzel, M.; Fox, J. W. Identification of sites in the cysteine-rich domain of the class P-III snake venom metalloproteinases responsible for inhibition of platelet function FEBS Lett. 2003, 549, 129-134 (Pubitemid 36959857)
15. Kamiguti, A. S.; Hay, C. R.; Zuzel, M. Inhibition of collagen-induced platelet aggregation as the result of cleavage of alpha 2 beta 1-integrin by the snake venom metalloproteinase jararhagin Biochem. J. 1996, 320, 635-641 (Pubitemid 26417791)
16. Lu, Q.; Clemetson, J. M.; Clemetson, K. J. Snake venoms and hemostasis J. Thromb. Haemost. 2005, 3, 1791-1799 (Pubitemid 41716566)
17. Oliveira, A. K.; Paes Leme, A. F.; Asega, A. F.; Camargo, A. C. M.; Fox, J. W.; Serrano, S. M. T. New insights into the structural elements involved in the skin hemorrhage induced by snake venom metalloproteinases Thromb. Haemost. 2010, 104, 485-497
18. Kamiguti, A. S.; Slupsky, J. R.; Zuzel, M.; Hay, C. R. Properties of fibrinogen cleaved by Jararhagin, a metalloproteinase from the venom of Bothrops jararaca Thromb. Haemost. 1994, 72, 244-249 (Pubitemid 24251288)
19. Gallagher, P.; Bao, Y.; Serrano, S. M.; Laing, G. D.; Theakston, R. D.; Gutiérrez, J. M.; Escalante, T.; Zigrino, P.; Moura-da-Silva, A. M.; Nischt, R.; Mauch, C.; Moskaluk, C.; Fox, J. W. Role of the snake venom toxin jararhagin in proinflammatory pathogenesis: in vitro and in vivo gene expression analysis of the effects of the toxin Arch. Biochem. Biophys. 2005, 441, 1-15 (Pubitemid 41188347)
20. Serrano, S. M.; Jia, L. G.; Wang, D.; Shannon, J. D.; Fox, J. W. Function of the cysteine-rich domain of the haemorrhagic metalloproteinase atrolysin A: targeting adhesion proteins collagen I and von Willebrand factor Biochem. J. 2005, 391, 69-76 (Pubitemid 41445477)
21. Serrano, S. M.; Kim, J.; Wang, D.; Dragulev, B.; Shannon, J. D.; Mann, H. H.; Veit, G.; Wagener, R.; Koch, M.; Fox, J. W. The cysteine-rich domain of snake venom metalloproteinases is a ligand for von Willebrand factor A domains: role in substrate targeting J. Biol. Chem. 2006, 281, 39746-39756 (Pubitemid 46041778)
22. Serrano, S. M.; Wang, D.; Shannon, J. D.; Pinto, A. F.; Polanowska-Grabowska, R. K.; Fox, J. W. Interaction of the cysteine-rich domain of snake venom metalloproteinases with the A1 domain of von Willebrand factor promotes site-specific proteolysis of von Willebrand factor and inhibition of von Willebrand factor-mediated platelet aggregation FEBS J. 2007, 274, 3611-21 (Pubitemid 47052400)
23. Baldo, C.; Jamora, C.; Yamanouye, N.; Zorn, T. M.; Moura-da-Silva, A. M. Mechanisms of vascular damage by hemorrhagic snake venom metalloproteinases: tissue distribution and in situ hydrolysis PLoS Neglected Trop. Dis. 2010, 4, e727
24. Anderson, N. L.; Anderson, N. G. The human plasma proteome: history, character, and diagnostic prospects Mol. Cell. Proteomics 2002, 1, 845-867
25. Huang, C. M.; Elmets, C. A.; van Kampen, K. R.; Desilva, T. S.; Barnes, S.; Kim, H.; Tang, D. C. Prospective highlights of functional skin proteomics Mass Spectrom. Rev. 2005, 24, 647-660 (Pubitemid 41615713)
26. Assakura, M. T.; Reichl, A. P.; Mandelbaum, F. R. Comparison of immunological, biochemical and biophysical properties of three hemorrhagic factors isolated from the venom of Bothrops jararaca (jararaca) Toxicon 1986, 24, 943-946 (Pubitemid 17209321)
27. Silva, C. A.; Zuliani, J. P.; Assakura, M. T.; Mentele, R.; Camargo, A. C.; Teixeira, C. F.; Serrano, S. M. Activation of αMβ2-mediated phagocytosis by HF3, a P-III class metalloproteinase isolated from the venom of Bothrops jararaca Biochem. Biophys. Res. Commun. 2004, 322, 950-956 (Pubitemid 39164445)
28. Oliveira, A. K.; Paes Leme, A. F.; Assakura, M. T.; Menezes, M. C.; Zelanis, A.; Tashima, A. K.; Lopes-Ferreira, M.; Lima, C.; Camargo, A. C.; Fox, J. W.; Serrano, S. M. Simplified procedures for the isolation of HF3, bothropasin, disintegrin-like/cysteine-rich protein and a novel P-I metalloproteinase from Bothrops jararaca venom Toxicon 2009, 53, 797-801
29. Menezes, M. C.; Paes Leme, A. F.; Melo, R. L.; Silva, C. A.; Della Casa, M.; Bruni, F. M.; Lima, C.; Lopes-Ferreira, M.; Camargo, A. C.; Fox, J. W.; Serrano, S. M. Activation of leukocyte rolling by the cysteine-rich domain and the hyper-variable region of HF3, a snake venom hemorrhagic metalloproteinase FEBS Lett. 2008, 582, 3915-3921
30. Mortz, E.; Krogh, T. N.; Vorum, H.; Gorg, A. Improved silver staining protocols for high sensitivity protein identification using matrix assisted laser desorption/ionization-time of flight analysis Proteomics 2001, 1, 1359-1363 (Pubitemid 33587891)
31. Hanna, S. L.; Sherman, N. E.; Kinter, M. T.; Goldberg, J. B. Comparison of proteins expressed by Pseudomonas aeruginosa strains representing initial and chronic isolates from a cystic fibrosis patient: an analysis by 2-D gel electrophoresis and capillary column liquid chromatography-tandem mass spectrometry Microbiology 2000, 146, 2495-2508
32. Aristoteli, L. P.; Molloy, M. P.; Baker, M. S. Evaluation of endogenous plasma peptide extraction methods for mass spectrometric biomarker discovery J. Proteome Res. 2007, 6, 571-581 (Pubitemid 46340161)
33. Serrano, S. M.; Shannon, J. D.; Wang, D.; Camargo, A. C.; Fox, J. W. A multifaceted analysis of viperid snake venoms by two-dimensional gel electrophoresis: an approach to understanding venom proteomics Proteomics 2005, 5, 501-510 (Pubitemid 40262067)
34. Laemmli, U. K. Cleavage of structural proteins during the assembly of the head of bacteriophage T4 Nature 1970, 227, 680-685
35. Escalante, T.; Shannon, J.; Moura-da-Silva, A. M.; Gutiérrez, J. M.; Fox, J. W. Novel insights into capillary vessel basement membrane damage by snake venom hemorrhagic metalloproteinases: a biochemical and immunohistochemical study Arch. Biochem. Biophys. 2006, 455, 144-153 (Pubitemid 44708849)
36. Rucavado, A.; Lomonte, B.; Ovadia, M.; Gutiérrez, J. M. Local tissue damage induced by BaP1, a metalloproteinase isolated from Bothrops asper (Terciopelo) snake venom Exp. Mol. Pathol. 1995, 63, 186-199 (Pubitemid 27149447)
37. Escalante, T.; Rucavado, A.; Pinto, A. F.; Terra, R. M.; Gutiérrez, J. M.; Fox, J. W. Wound exudate as a proteomic window to reveal different mechanisms of tissue damage by snake venom toxins J. Proteome Res. 2009, 8, 5120-5131
38. Tortorella, M. D.; Pratta, M. A.; Fox, J. W.; Arner, E. C. The interglobular domain of cartilage aggrecan is cleaved by hemorrhagic metalloproteinase HT-d (atrolysin C) at the matrix metalloproteinase and aggrecanase sites J. Biol. Chem. 1998, 273, 5846-5850 (Pubitemid 28124062)
39. Yanagishita, M. Function of proteoglycans in the extracellular matrix Acta Pathol. Jpn. 1993, 43, 283-293 (Pubitemid 23174979)
40. Formigli, L.; Meacci, E.; Zecchi-Orlandini, S.; Orlandini, G. E. Cytoskeletal reorganization in skeletal muscle differentiation: from cell morphology to gene expression Eur. J. Histochem. 2007, 51, 21-28
41. Gutiérrez, J. M.; Ownby, C. L. Skeletal muscle degeneration induce by venom phospholipases A2: insights into the mechanisms of local and systemic myotoxicity Toxicon 2003, 42, 915-931 (Pubitemid 38201492)
42. Ivaska, J.; Pallari, H. M.; Nevo, J.; Eriksson, J. E. Novel functions of vimentin in cell adhesion, migration, and signaling Exp. Cell Res. 2007, 313, 2050-2062 (Pubitemid 46842979)
43. Mor-Vaknin, N.; Punturieri, A.; Sitwala, K.; Markovitz, D. M. Vimentin is secreted by activated macrophages Nat. Cell Biol. 2003, 5, 59-63 (Pubitemid 36054330)
44. Tanjoni, I.; Weinlich, R.; Della-Casa, M. S.; Clissa, P. B.; Saldanha-Gama, R. F.; de Freitas, M. S.; Barja-Fidalgo, C.; Amarante-Mendes, G. P.; Moura-da-Silva, A. M. Jararhagin, a snake venom metalloproteinase, induces a specialized form of apoptosis (anoikis) selective to endothelial cells Apoptosis 2005, 10, 851-861 (Pubitemid 41187083)
45. Benaud, C.; Gentil, B. J.; Assard, N.; Court, M.; Garin, J.; Delphin, C.; Baudier, J. AHNAK interaction with the annexin 2/S100A10 complex regulates cell membrane cytoarchitecture Cell Biol. 2004, 164, 133-144 (Pubitemid 38082464)
46. Kuypers, F. A.; Larkin, S. K.; Emeis, J. J.; Allison, A. C. Interaction of an annexin V homodimer (Diannexin) with phosphatidylserine on cell surfaces and consequent antithrombotic activity Thromb. Haemost. 2007, 97, 478-486 (Pubitemid 46437812)
47. Pinto, A. F.; Ma, L.; Dragulev, B.; Guimaraes, J. A.; Fox, J. W. Use of SILAC for exploring sheddase and matrix degradation of fibroblasts in culture by the PIII SVMP atrolysin A: identification of two novel substrates with functional relevance Arch. Biochem. Biophys. 2007, 465, 11-15 (Pubitemid 47299085)
48. Ousman, S. S.; Tomooka, B. H.; van Noort, J. M.; Wawrousek, E. F.; O'Connor, K. C.; Hafler, D. A.; Sobel, R. A.; Robinson, W. H.; Steinman, L. Protective and therapeutic role for alphaB-Crystallin in autoimmune demyelination Nature 2007, 448, 474-479 (Pubitemid 47123511)
49. Carson, S. D. Tissue factor (coagulation factor III) inhibition by apolipoprotein A-II J. Biol. Chem. 1987, 262, 718-721 (Pubitemid 17005242)
50. Tajima, T.; Yoshida, E.; Yamashita, A.; Ohmura, S.; Tomitaka, Y.; Sugiki, M.; Asada, Y.; Maruyama, M. Hemoglobin stimulates the expression of matrix metalloproteinases, MMP-2 and MMP-9 by synovial cells: a possible cause of joint damage after intra-articular hemorrhage J. Orthop. Res. 2005, 23, 891-898 (Pubitemid 40960043)
51. Baramova, E. N.; Shannon, J. D.; Bjarnason, J. B.; Gonias, S. L.; Fox, J. W. Interaction of hemorrhagic metalloproteinases with human a2-macroglobulin Biochemistry 1990, 29, 1069-1074 (Pubitemid 20053823)
52. Makogonenko, E.; Tsurupa, G.; Ingham, K.; Medeved, L. Interaction of fibrin(ogen) with fibronectin: further characterization and localization of the fibronectin-binding site Biochemistry 2002, 41, 7907-7913 (Pubitemid 34655155)
53. Tolosano, E.; Altruda, F. Hemopexin: structure, function, and regulation DNA Cell Biol. 2002, 21, 297-306 (Pubitemid 34594543)
54. Kratzer, I.; Bernhart, E.; Wintersperger, A.; Hammer, A.; Waltl, S.; Malle, E.; Sperk, G.; Wietzorrek, G.; Dieplinger, H.; Sattler, W. Afamin is synthesized by cerebrovascular endothelial cells and mediates alpha-tocopherol transport across an in vitro model of the blood-brain barrier J. Neurochem. 2009, 108, 707-718
55. Catanese, J. J.; Kress, L. F. Isolation from opossum serum of a metalloproteinase inhibitor homologous to human alpha 1B-glycoprotein Biochemistry 1992, 31, 310-418