All Title Author
Keywords Abstract


Genetic Basis for Variation of Metalloproteinase-Associated Biochemical Activity in Venom of the Mojave Rattlesnake (Crotalus scutulatus scutulatus)

DOI: 10.1155/2013/251474

Full-Text   Cite this paper   Add to My Lib

Abstract:

The metalloproteinase composition and biochemical profiles of rattlesnake venom can be highly variable among rattlesnakes of the same species. We have previously shown that the neurotoxic properties of the Mojave rattlesnake (Crotalus scutulatus scutulatus) are associated with the presence of the Mojave toxin A subunit suggesting the existence of a genetic basis for rattlesnake venom composition. In this report, we hypothesized the existence of a genetic basis for intraspecies variation in metalloproteinase-associated biochemical properties of rattlesnake venom of the Mojave rattlesnake. To address this question, we PCR-amplified and compared the genomic DNA nucleotide sequences that code for the mature metalloproteinase domain of fourteen Mojave rattlesnakes captured from different geographical locations across the southwest region of the United States. In addition, the venoms from the same rattlesnakes were tested for their ability to hydrolyze fibrinogen, fibrin, casein, and hide powder azure and for induction of hemorrhage in mice. Overall, based on genomic sequencing and biochemical data, we classified Mojave rattlesnake venom into four distinct groups of metalloproteinases. These findings indicate that differences in nucleotide sequences encoding the mature proteinase domain and noncoding regions contribute to differences in venom metalloproteinase activities among rattlesnakes of the same species. 1. Introduction Rattlesnake venom metalloproteinases are zinc-dependent enzymes that hydrolyze fibrin and fibrinogen, inactivate complement proteins, and promote hemorrhage in vivo [1–4]. In addition, rattlesnake venom metalloproteinases show differences in substrate specificity, proteolytic activity, molecular weight, and composition of structural domains [5, 6]. Rattlesnake venom metalloproteinases are members of the Reprolysin superfamily of metalloproteinases [7]. These venom enzymes have been subcategorized into four classes (P-I to P-IV) based on the differences in structural domains, molecular weight, and biochemical properties [7, 8]. The P-I group of rattlesnake venom metalloproteinases contains a proteinase domain, whereas the P-II group contains an additional disintegrin-like domain. The P-III group has an additional disintegrin-like domain and cysteine-rich sequence, whereas the P-IV group has an additional lectin-like sequence [8]. The P-II and P-III classes of rattlesnake venom metalloproteinases are one- to twofold more potent at inducing hemorrhage than the P-I metalloproteinases [8–11]. This observation suggests that the

References

[1]  F. S. Markland, “Rattlesnake venom enzymes that interact with components of the hemostatic system,” Journal of Toxicology, vol. 2, no. 2, pp. 119–160, 1983.
[2]  O. Molina, R. K. Seriel, M. Martinez, M. L. Sierra, A. Varela-Ramirez, and E. D. Rael, “Isolation of two hemorrhagic toxins from Crotalus basiliscus basiliscus (mexican west coast rattlesnake) venom and their effect on blood clotting and complement,” International Journal of Biochemistry, vol. 22, no. 3, pp. 253–261, 1990.
[3]  E. D. Rael, C. S. Lieb, N. Maddux, A. Varela-Ramirez, and J. Perez, “Hemorrhagic and Mojave toxins in the venoms of the offspring of two Mojave rattlesnakes (Crotalus scutulatus scutulatus),” Comparative Biochemistry and Physiology B, vol. 106, no. 3, pp. 595–600, 1993.
[4]  E. D. Rael, J. Z. Rivas, T. Chen, N. Maddux, E. Huizar, and C. S. Lieb, “Differences in fibrinolysis and complement inactivation by venom from different northern blacktailed rattlesnakes (Crotalus molossus molossus),” Toxicon, vol. 35, no. 4, pp. 505–513, 1997.
[5]  T. Chen and E. D. Rael, “Purification of M5, a fibrinolytic proteinase from Crotalus molossus molossus venom that attacks complement,” International Journal of Biochemistry and Cell Biology, vol. 29, no. 5, pp. 789–799, 1997.
[6]  E. D. Rael, M. Martinez, and O. Molina, “Isolation of a fibrinolytic protease, M4, from venom of Crotalus molossus molossus (Northern blacktail rattlesnake),” Haemostasis, vol. 22, no. 1, pp. 41–49, 1992.
[7]  L. A. Hite, L.-G. Jia, J. B. Bjarnason, and J. W. Fox, “cDNA sequences for four snake venom metalloproteinases: structure, classification, and their relationship to mammalian reproductive proteins,” Archives of Biochemistry and Biophysics, vol. 308, no. 1, pp. 182–191, 1994.
[8]  L. Jia, X. Wang, J. D. Shannon, J. B. Bjarnason, and J. W. Fox, “Function of disintegrin-like/cysteine-rich domains of atrolysin A. Inhibition of platelet aggregation by recombinant protein and peptide antagonists,” Journal of Biological Chemistry, vol. 272, no. 20, pp. 13094–13102, 1997.
[9]  J. M. Gutiérrez and A. Rucavado, “Snake venom metalloproteinases: their role in the pathogenesis of local tissue damage,” Biochimie, vol. 82, no. 9-10, pp. 841–850, 2000.
[10]  L. G. Jia, X. Wang, J. D. Shannon, J. B. Bjarnason, and J. W. Fox, “Inhibition of platelet aggregation by the recombinant cysteine-rich domain of the hemorrhagic snake venom metalloproteinase, atrolysin A,” Archives of Biochemistry and Biophysics, vol. 373, no. 1, pp. 281–286, 2000.
[11]  Q. Zhou, P. Hu, M. R. Ritter et al., “Molecular cloning and functional expression of contortrostatin, a homodimeric disintegrin from southern copperhead snake venom,” Archives of Biochemistry and Biophysics, vol. 375, no. 2, pp. 278–288, 2000.
[12]  J. B. Bjarnason and J. W. Fox, “Hemorrhagic metalloproteinases from snake venoms,” Pharmacology and Therapeutics, vol. 62, no. 3, pp. 325–372, 1994.
[13]  K. Shimokawa, L. Jia, X. Wang, and J. W. Fox, “Expression, activation, and processing of the recombinant snake venom metalloproteinase, Pro-atrolysin E,” Archives of Biochemistry and Biophysics, vol. 335, no. 2, pp. 283–294, 1996.
[14]  M. Anaya, E. D. Rael, C. S. Lieb, J. C. Perez, and R. J. Salo, “Antibody detection of venom protein variation within a population of prairie rattlesnake Crotalus v. viridis,” Journal of Herpetology, no. 26, pp. 473–482, 1992.
[15]  J. L. Glenn and R. Straight, “Mojave rattlesnake Crotalus scutulatus scutulatus venom: variation in toxicity with geographical origin,” Toxicon, vol. 16, no. 1, pp. 81–84, 1978.
[16]  J. L. Glenn, R. C. Straight, M. C. Wolfe, and D. L. Hardy, “Geographical variation in Crotalus scutulatus scutulatus (Mojave rattlesnake) venom properties,” Toxicon, vol. 21, no. 1, pp. 119–130, 1983.
[17]  L. G. Jia, K. Shimokawa, J. B. Bjarnason, and J. W. Fox, “Snake venom metalloproteinaes: structure, function and relationship to the adams family of proteins,” Toxicon, vol. 34, no. 11-12, pp. 1269–1276, 1996.
[18]  B. J. Wooldridge, G. Pineda, J. J. Banuelas-Ornelas et al., “Mojave rattlesnakes (Crotalus scutulatus scutulatus) lacking the acidic subunit DNA sequence lack Mojave toxin in their venom,” Comparative Biochemistry and Physiology B, vol. 130, no. 2, pp. 169–179, 2001.
[19]  W. J. French, W. K. Hayes, S. P. Bush, M. D. Cardwell, J. O. Bader, and E. D. Rael, “Mojave toxin in venom of Crotalus helleri (Southern Pacific Rattlesnake): molecular and geographic characterization,” Toxicon, vol. 44, no. 7, pp. 781–791, 2004.
[20]  D. J. Massey, J. J. Calvete, E. E. Sánchez et al., “Venom variability and envenoming severity outcomes of the Crotalus scutulatus scutulatus (Mojave rattlesnake) from Southern Arizona,” Journal of Proteomics, vol. 75, no. 9, pp. 2576–2587, 2012.
[21]  L. A. Hite, J. W. Fox, and J. B. Bjarnason, “A new family of proteinases is defined by several snake venom metalloproteinases,” Biological Chemistry Hoppe-Seyler, vol. 373, no. 7, pp. 381–385, 1992.
[22]  O. Zhou, B. J. Smith, and M. H. Grossman, “Molecular cloning and expression of catrocollastatin, a snake-venom protein from Crotalus atrox (western diamondback rattlesnake) which inhibits platelet adhesion to collagen,” Biochemical Journal, vol. 307, no. 2, pp. 411–417, 1995.
[23]  M. Martinez, E. D. Rael, and N. L. Maddux, “Isolation of a hemorrhagic toxin from mojave rattlesnake (Crotalus scutulatus scutulatus) venom,” Toxicon, vol. 28, no. 6, pp. 685–694, 1990.
[24]  R. A. Martinez, S. Y. Huang, and J. C. Perez, “Antigenic relationships of fractionated western diamondback rattlesnake (Crotalus atrox) hemorrhagic toxins and other rattlesnake venoms as indicated by monoclonal antibodies,” Toxicon, vol. 27, no. 2, pp. 239–245, 1989.
[25]  E. D. Rael and L. P. Jones, “Isolation of an anticomplement factor from the venom of the Mojave rattlesnake (Crotalus scutulatus scutulatus),” Toxicon, vol. 21, no. 1, pp. 57–65, 1983.
[26]  J. B. Bjarnason and A. T. Tu, “Hemorrhagic toxins from western diamondback rattlesnake (Crotalus atrox) venom: isolation and characterization of five toxins and the role of zinc in hemorrhagic toxin,” Biochemistry, vol. 17, no. 16, pp. 3395–3404, 1978.
[27]  J. G. Soto, J. C. Perez, M. M. Lopez, et al., “Comparative enzymatic study of HPLC-fractionated Crotalus venoms,” Comparative Biochemistry and Physiology B, vol. 93, no. 4, pp. 847–855, 1989.
[28]  S. Y. Huang, J. C. Perez, E. D. Rael, C. Lieb, M. Martinez, and S. A. Smith, “Variation in the antigenic characteristics of venom from the Mojave rattlesnake (Crotalus scutulatus scutulatus),” Toxicon, vol. 30, no. 4, pp. 387–396, 1992.
[29]  M. W. Schwartz and A. L. Bieber, “Characterization of two arginine ester hydrolases from Mojave rattlesnake (Crotalus scutulatus scutulatus) venom,” Toxicon, vol. 23, no. 2, pp. 255–269, 1985.
[30]  A. H. Henschen-Edman, I. Theodor, B. F. P. Edwards, and H. Pirkle, “Crotalase, a fibrinogen-clotting snake venom enzyme: primary structure and evidence for a fibrinogen recognition exosite different from thrombin,” Thrombosis and Haemostasis, vol. 81, no. 1, pp. 81–86, 1999.
[31]  H. de Araujo and C. Ownby, “Molecular cloning and sequence analysis of cDNAs for metalloproteinases from broad-banded copperhead Agkistrodon contortrix laticinctus,” Archives of Biochemistry and Biophysics, vol. 320, no. 1, pp. 141–148, 1995.
[32]  Y. Jia, B. A. Cantu, E. E. Sánchez, and J. C. Pérez, “Complementary DNA sequencing and identification of mRNAs from the venomous gland of Agkistrodon piscivorus leucostoma,” Toxicon, vol. 51, no. 8, pp. 1457–1466, 2008.
[33]  Y. Jia and J. C. Pérez, “Molecular cloning and characterization of cDNAs encoding metalloproteinases from snake venom glands,” Toxicon, vol. 55, no. 2-3, pp. 462–469, 2010.
[34]  H. E. Van Wart and H. Birkedal-Hansen, “The cysteine switch: a principle of regulation of metalloproteinase activity with potential applicability to the entire matrix metalloproteinase gene family,” Proceedings of the National Academy of Sciences of the United States of America, vol. 87, no. 14, pp. 5578–5582, 1990.
[35]  L. A. Hite, J. D. Shannon, J. B. Bjarnason, and J. W. Fox, “Sequence of a cDNA clone encoding the zinc metalloproteinase hemorrhagic toxin e from Crotalus atrox: evidence for signal, zymogen, and disintegrin-like structures,” Biochemistry, vol. 31, no. 27, pp. 6203–6211, 1992.
[36]  J. B. Bjarnason and J. W. Fox, “Hemorrhagic metalloproteinases from snake venoms,” Pharmacology and Therapeutics, vol. 62, no. 3, pp. 325–372, 1994.
[37]  N. Maeda and O. Smithies, “The evolution of multigene families: human haptoglobin genes,” Annual Review of Genetics, vol. 20, pp. 81–108, 1986.
[38]  K. Nakashima, I. Nobuhisa, M. Deshimaru et al., “Accelerated evolution in the protein-coding regions is universal in crotalinae snake venom gland phospholipase A2 isozyme genes,” Proceedings of the National Academy of Sciences of the United States of America, vol. 92, no. 12, pp. 5605–5609, 1995.

Full-Text

comments powered by Disqus