Preliminary studies on different modes of interaction between hemorrhagic and non-hemorrhagic p-i snake venom metalloproteinases with basement membrane substrates: insights from an In silico approach
Main Article Content
Abstract
It has been demonstrated that, in vivo, a hemorrhagic P-I SVMP hydrolyzes type IV collagen and perlecan to a higher extent than a non-hemorrhagic P-I SVMP. In order to gain further insights on this phenomenon, the protein-protein docking approach was used to analyze the mode of interaction of four different SVMPs with two different domains of perlecan and two different domains of type IV collagen. The hemorrhagic SVMPs are BaP1 and acutolysin-A, and the non-hemorrhagic ones are BmooMPα-I and H2-proteinase. In general, hemorrhagic SVMPs could form catalytic complexes with the triple-helical domain of type IV collagen, and with laminin-like globular domain 3 and immunoglobulin (IG)-like domain of perlecan. It is hypothesized that the formation of these catalytic complexes may explain the differences observed in vivo in the degradation of collagen IV and perlecan. Moreover, our results suggest that there are differences in the area and volume of the active site cleft between hemorrhagic and non-hemorrhagic P-I SVMPs, since the latter present a larger volume and area. We suggest that this structural characteristic favors the interaction with substrates; nevertheless, at the same time, it could decrease the probability to achieve a stable complex. However, these results should be confirmed by means of experimental and bioinformatics assays.
Keywords:
Snake venom metalloproteinases, protein-protein docking, collagen type IV, perlecan, hemorrhage
Article Details
How to Cite
PEREANEZ, Andres et al.
Preliminary studies on different modes of interaction between hemorrhagic and non-hemorrhagic p-i snake venom metalloproteinases with basement membrane substrates: insights from an In silico approach.
Medical Research Archives, [S.l.], v. 6, n. 11, nov. 2018.
ISSN 2375-1924.
Available at: <https://esmed.org/MRA/mra/article/view/1856>. Date accessed: 27 dec. 2024.
doi: https://doi.org/10.18103/mra.v6i11.1856.
Section
Research Articles
The Medical Research Archives grants authors the right to publish and reproduce the unrevised contribution in whole or in part at any time and in any form for any scholarly non-commercial purpose with the condition that all publications of the contribution include a full citation to the journal as published by the Medical Research Archives.
References
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34. Paes-Leme AF, Escalante T, Pereira JG, Oliveira AK, Sanchez EF, et al. High resolution analysis of snake venom metalloproteinase (SVMP) peptide bond cleavage specificity using proteome based peptide libraries and mass spectrometry. J. Proteomics. 2011; 74: 401-410.
35. Manka SW, Carafoli F, Visse R, Bihan D, Raynal N, et al. Structural insights into triple-helical collagen cleavage by matrix metalloproteinase 1. Proc. Natl. Acad. Sci. U S A. 2012; 109: 12461-12466.
36. Baramova EN, Shannon JD, Bjarnason JB, Fox JW. Identification of the cleavage sites by a hemorrhagic metalloproteinase in type IV collagen. Matrix. 1990; 10: 91-97.
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2. Fox JW, Serrano SMT. Structural considerations of the snake venom metalloproteinases, key members of the M12 reprolysin family of metalloproteinases. Toxicon. 2005; 45: 969-985.
3. Gutiérrez JM, Rucavado A, Escalante T. Snake venom metalloproteinases. Biological roles and participation in the pathophysiology of envenomation. In Mackessy SP, ed., Handbook of Venoms and Toxins of Reptiles. Boca Raton: CRC Press; 2010. pp 114-128.
4. Gutiérrez JM, 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.
5. Escalante T, Rucavado A, Fox JW, Gutiérrez JM. Key events in microvascular damage induced by snake venom hemorrhagic metalloproteinases. J. Proteomics. 2011b; 74: 1781-1794.
6. Escalante T, Shannon J, Moura-da-Silva AM, Gutiérrez JM, Fox JW. 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.
7. Fox JW, Serrano SM. Insights into and speculations about snake venom metalloproteinase (SVMP) synthesis, folding and disulfide bond formation and their contribution to venom complexity. FEBS Journal. 2008; 275: 3016-3030.
8. Akao PK, Tonoli CC, Navarro MS, Cintra AC, Neto JR, et al. Structural studies of BmooMPalpha-I, a non-hemorrhagic metalloproteinase from Bothrops moojeni venom. Toxicon. 2010; 55: 361-368.
9. Bello CA, Hermogenes AL, Magalhaes A, Veiga SS, Gremski LH, et al. Isolation and biochemical characterization of a fibrinolytic proteinase from Bothrops leucurus (white-tailed jararaca) snake venom. Biochimie. 2006; 88: 189–200.
10. Gong W, Zhu X, Liu S, Teng M, Niu L. Crystal structures of acutolysin A, a three-disulfide hemorrhagic zinc metalloproteinase from the snake venom of Agkistrodon acutus. J. Mol. Biol. 1998; 283: 657-668.
11. Gutiérrez JM, Romero M, Díaz C, Borkow G, Ovadia M. Isolation and characterization of a metalloproteinase with weak hemorrhagic activity from the venom of the snake Bothrops asper (terciopelo). Toxicon. 1995; 33: 19-29.
12. Kumasaka T, Yamamoto M, Moriyama H, Tanaka N, Sato M, et al. Crystal structure of H2-proteinase from the venom of Trimeresurus flavoviridis. J. Biochem. 1996; 119: 49-57.
13. Escalante T, Ortiz N, Rucavado A, Sanchez EF, Richardson M, et al. Role of collagens and perlecan in microvascular stability: exploring the mechanism of capillary vessel damage by snake venom metalloproteinases. PLoS One. 2011a; 6: e28017.
14. Ramos OH, Selistre-de-Araujo HS. Comparative analysis of the catalytic domain of hemorrhagic and non-hemorrhagic snake venom metallopeptidases using bioinformatic tools. Toxicon. 2004; 44: 529-538.
15. Wallnoefer HG, Lingott T, Gutiérrez JM, Merfort I, Liedl KR. Backbone flexibility controls the activity and specificity of a protein-protein interface: specificity in snake venom metalloproteinases. J. Am. Chem. Soc. 2010; 132: 10330-10337.
16. Watanabe L, Shannon JD, Valente RH, Rucavado A, Alape-Girón A, et al. Amino acid sequence and crystal structure of BaP1, a metalloproteinase from Bothrops asper snake venom that exerts multiple tissue-damaging activities. Protein Sci. 2003; 12: 2273-2281.
17. Kuntal BK, Aparoy P, Reddanna P. EasyModeller: A graphical interface to MODELLER. BMC Res. 2010; Notes 3: 226.
18. Sali A, Blundell TL. Comparative protein modelling by satisfaction of spatial restraints. J. Mol. Biol. 1993; 234: 779-815.
19. Laskowski RA, MacArthur MW, Moss DS, Hornton DS. PROCHECK: a program to check the stereochemical quality of protein structures. J. Appl. Crystallogr. 1993; 26: 283-291.
20. Bowie JU, Lüthy R, Eisenberg D. A method to identify protein sequences that fold into a known three-dimensional structure. Science. 1991; 253: 164-170.
21. Sippl MJ. Recognition of errors in three-dimensional structures of proteins. Proteins. 1993; 17: 355-362.
22. Wiederstein M, Sippl MJ. ProSA-web: interactive web service for the recognition of errors in three-dimensional structures of proteins. Nucleic Acids Res. 2007; 35: W407-410.
23. Schneidman-Duhovny D, Inbar Y, Nussinov R, Wolfson HJ. PatchDock and SymmDock: servers for rigid and symmetric docking. Nucleic Acids Res. 2005; 33: W363-367.
24. Mashiach E, Nussinov R, Wolfson HJ. FiberDock: Flexible induced-fit backbone refinement in molecular docking. Proteins. 2010a; 78: 1503-1519.
25. Mashiach E, Nussinov R, Wolfson HJ. FiberDock: a web server for flexible induced-fit backbone refinement in molecular docking. Nucleic Acids Res. 2010b; 38: W457-461.
26. Dundas J, Ouyang Z, Tseng J, Binkowski A, Turpaz Y, et al. CASTp: computed atlas of surface topography of proteins with structural and topographical mapping of functionally annotated residues. Nucleic Acids Res. 2006; 34: W116-118.
27. Serrano SM, Jia LG, Wang D, Shannon JD, Fox JW. 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.
28. Serrano SM, Kim J, Wang D, Dragulev B, Shannon JD, et al. 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.
29. Serrano SM, Wang D, Shannon JD, Pinto AF, Polanowska-Grabowska RK, et al. 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: 3611-3621.
30. Tanjoni I, Evangelista K, Della-Casa MS, Butera D, Magalhães GS, et al. Different regions of the class P-III snake venom metalloproteinase jararhagin are involved in binding to α21integrin and collagen. Toxicon. 2010; 55: 1093-1099.
31. Hudson BG, Reeders ST, Tryggvason K. Type IV collagen: structure, gene organization, and role in human diseases. Molecular basis of Goodpasture and Alport syndromes and diffuse leiomyomatosis. J. Biol. Chem. 1993; 268: 26033-26036.
32. Farach-Carson MC, Carson DD. Perlecan--a multifunctional extracellular proteoglycan scaffold. Glycobiology. 2007; 17: 897-905.
33. Iozzo RV. Basement membrane proteoglycans: from cellar to ceiling. Nat. Rev. Mol. Cell. Biol. 2005; 6: 646-656.
34. Paes-Leme AF, Escalante T, Pereira JG, Oliveira AK, Sanchez EF, et al. High resolution analysis of snake venom metalloproteinase (SVMP) peptide bond cleavage specificity using proteome based peptide libraries and mass spectrometry. J. Proteomics. 2011; 74: 401-410.
35. Manka SW, Carafoli F, Visse R, Bihan D, Raynal N, et al. Structural insights into triple-helical collagen cleavage by matrix metalloproteinase 1. Proc. Natl. Acad. Sci. U S A. 2012; 109: 12461-12466.
36. Baramova EN, Shannon JD, Bjarnason JB, Fox JW. Identification of the cleavage sites by a hemorrhagic metalloproteinase in type IV collagen. Matrix. 1990; 10: 91-97.
37. Sundaramoorthy M, Meiyappan M, Todd P, Hudson BG. Crystal structure of NC1 domains. Structural basis for type IV collagen assembly in basement membranes. J. Biol. Chem. 2002; 277: 31142-31153.
38. Yurchenco PD, Amenta PS, Patton BL. Basement membrane assembly, stability and activities observed through a developmental lens. Matrix Biol. 2004; 22: 521-538.