Why the honey badger don't care: Convergent evolution of venom-targeted nicotinic acetylcholine receptors in mammals that survive venomous snake bites

Toxicon

Volumn 99, Issue , 2015, Pages 68-72

  Drabeck, Danielle H ^a   Dean, Antony M ^a   Jansa, Sharon A ^a  

^a UNIVERSITY OF MINNESOTA   (United States)

Author keywords

Convergent evolution; Honey badger; Mellivora capensis; Nicotinic acetylcholine receptor; Venom resistance

Indexed keywords

ALPHA NEUROTOXIN; GENOMIC DNA; NEUROTOXIN; NICOTINIC RECEPTOR; NICOTINIC RECEPTOR ALPHA1; UNCLASSIFIED DRUG; LIGAND; NERVE PROTEIN; SNAKE VENOM;

AMINO ACID SEQUENCE; AMINO ACID SUBSTITUTION; ANIMAL TISSUE; ARTICLE; BADGER; CHRNA1 RECEPTOR GENE; CONTROLLED STUDY; CONVERGENT EVOLUTION; ELAPIDAE; HONEY BADGER; MOLECULAR EVOLUTION; MONGOOSE; NONHUMAN; PHYLOGENY; PHYSICAL RESISTANCE; PREDATOR PREY INTERACTION; PRIORITY JOURNAL; PROTEIN TARGETING; SNAKEBITE; SURFACE CHARGE; SURVIVAL; VENOM RESISTANCE; ANIMAL; ANTAGONISTS AND INHIBITORS; BINDING SITE; BLOOD; CHEMICAL STRUCTURE; CHEMISTRY; GENETICS; METABOLISM; MULTIDRUG RESISTANCE; MUSTELIDAE; PATHOPHYSIOLOGY; PHYSIOLOGY; PREDATION; PROTEIN CONFORMATION; PROTEIN DATABASE; VETERINARY; ZOO ANIMAL;

ELAPIDAE; ERINACEIDAE; HERPESTIDAE; MAMMALIA; MELLIVORA CAPENSIS; SERPENTES; SUIDAE;

ANIMALS; ANIMALS, ZOO; BINDING SITES; DATABASES, PROTEIN; DRUG RESISTANCE, MULTIPLE; ELAPID VENOMS; ELAPIDAE; EVOLUTION, MOLECULAR; LIGANDS; MODELS, MOLECULAR; MUSTELIDAE; NERVE TISSUE PROTEINS; NEUROTOXINS; PHYLOGENY; PREDATORY BEHAVIOR; PROTEIN CONFORMATION; RECEPTORS, NICOTINIC; SNAKE BITES;

EID: 84925753226     PISSN: 00410101     EISSN: 18793150     Source Type: Journal    
DOI: 10.1016/j.toxicon.2015.03.007     Document Type: Article

References (53)

1. O. Asher, M. Lupu-Meiri, B.S. Jensen, T. Papema, S. Fuchs, and Y. Oron Functional characterization of mongoose nicotinic acetylcholine receptor α-subunit: resistance to α-bungarotoxin and high sensitivity to acetylcholine FEBS Lett. 431 1997 411 414
2. O. Asher, B.S. Jensen, M. Lupu-Meiri, Y. Oron, and S. Fuchs The mongoose acetylcholine receptor α-subunit: analysis of glycosylation and α-bungarotoxin binding FEBS Lett. 426 1998 212 216
3. D. Barchan, M. Ovadia, E. Kochva, and S. Fuchs The binding site of the nicotinic acetylcholine receptor in animal species resistant to α-bungarotoxin Biochemistry 34 1995 9172 9176
4. D. Barchan, S. Kachalsky, D. Neumann, Z. Vogel, M. Ovadia, E. Kochva, and S. Fuchs How the mongoose can fight the snake: the binding site of the mongoose acetylcholine receptor Proc. Natl. Acad. Sci. 89 1992 7717 7721
5. C.M. Begg, K.S. Begg, J.T. Du Toit, and M.G.L. Mills Sexual and seasonal variation in the diet and foraging behavior of a sexually dimorphic carnivore, the honey badger (Mellivora capensis) J. Zoo. Lond 260 2003 301 316
6. A. Calmette Venoms: venomous animals and antivenomous serum-therapeutics (The English translation of -Calmette A 1895). Contribution à l'étude des venins, des toxines et des sérums antitoxiques Ann. Inst. Pasteur 9 1908 225 254
7. J.J. Catanese, and L.F. Kress Isolation from opossum serum of a metalloproteinase inhibitor homologous to human α1B-glycoprotein Biochemistry 31 1992 410 418
8. C.D. Dellisanti, Y. Yao, J.C. Stroud, Z.-Z. Wang, and L. Chen Structural determinant for α-neurotoxin sensitivity in muscle nAChR and their implications for the gating mechanism Channels 1 2007 234 237
9. C.D. Dellisanti, Y. Yao, J.C. Stroud, Z.-Z. Wang, and L. Chen Crystal structure of the extracellular domain of nAChR alpha1 bound to alpha-bungarotoxin at 1.94 A resolution Nat. Neurosci. 10 2007 953 962
10. N. Dimitropoulos, A. Papakyriakou, G.A. Dalkas, C.T. Chasapis, K. Poulas, and G.A. Spyroulias A computational investigation on the role of glycosylation in the binding of alpha1 nicotinic acetylcholine receptor with two alpha-neurotoxins Proteins 79 2011 142 152
11. G.B. Domont, J. Perales, and C. Moussatche Natural anti-snake venom proteins Toxicon 29 1991 1183 1194
12. A.J. Drummond, B. Ashton, S. Buxton, M. Cheung, A. Cooper, C. Duran, M. Field, J. Heled, M. Kearse, S. Markowitz, R. Moir, S. Stones-Havas, S. Sturrock, T. Thierer, and A. Wilson Geneious v5.5 2010 http://www.geneious.com
13. R.C. Edgar MUSCLE: multiple sequence alignment with high accuracy and high throughput Nucleic Acids Res. 32 2004 1792 1797
14. D. Gifford-Gonzalez, and O. Hanotte Domesticating animals in Africa: implications of genetic and archaeological findings J. World Prehist. 24 2011 1 23
15. E. Giuffra, J.M. Kijas, V. Amarger, O. Carlborg, J.T. Jeon, and L. Andersson The origin of the domestic pig: independent domestication and subsequent introgression Genetics 154 2000 1785 1791
16. E. Grasset, M.D. (Geneva), A. Zoutendykanda, and A. Schaafsma Studies on the toxic and antigenic properties of Southern African snake venoms with special reference to the polyvalency of South African antivenene Trans. R. Soc. Trop. Med. Hygeine 28 1935 601 612
17. J.G. Haggerty, and S.C. Froehner Restoration of 125 I-alpha-bungarotoxin binding activity to the alpha subunit of Torpedo acetylcholine receptor isolated by gel electrophoresis in sodium dodecyl sulfate J. Biol. Chem. 256 1981 8294 8297
18. C.J. Hartley, R.D. Newcomb, R.J. Russell, C.G. Yong, J.R. Stevens, D.K. Yeates, J. La Salle, and J.G. Oakeshott Amplification of DNA from preserved specimens shows blowflies were preadapted for the rapid evolution of insecticide resistance Proc. Natl. Acad. Sci. U. S. A. 103 2006 8757 8762
19. K. Herter Hedgehogs: a comprehensive study 1965 Phoenix House, U.K
20. I. Hiebl, G. Braunitzer, and D. Schneeganss The primary structures of the major and minor hemoglobin-components of adult Andean goose (Chloephaga melanoptera, Anatidae): the mutation Leu>Ser in position 55 of the β-chains Biol. Chem. Hoppe-Seyler 368 1987 1559 1569
21. H.E. Hoekstra, R.J. Hirschmann, R.A. Bundey, P.A. Insel, and J.P.A. Crossland Single amino acid mutation contributes to adaptive beach mouse color pattern Science 313 2006 101 104
22. Hughes D, and Hughes C (Directors), Begg CM, Begg KS (Performers). 2013. Snake Killers: Honey Badgers Of The Kalahari [Documentary]. UK: National Geographic.
23. S.A. Jansa, and R.S. Voss Adaptive evolution of the venom-targeted vWF protein in opossums that eat pitvipers PLoS One 6 2011 1 9
24. T.H. Jessen, R.E. Weber, G. Fermi, J. Tame, and G. Braunitzer Adaptation of bird hemoglobins to high altitudes: demonstration of molecular mechanism by protein engineering Proc. Natl. Acad. Sci. U. S. A. 88 1991 6519 6522
25. P.N. Kao, A.J. Dwork, R.J. Kaldany, M.L. Silver, J. Wideman, S. Stein, and A. Karlin J. Biol. Chem. 259 1984 11662 11665
26. nd ed. 1972 University of California Press Berkeley
27. K.-P. Koepfli, K.A. Deere, G.J. Slater, C.M. Begg, K.S. Begg, L. Grassman, M. Lucherini, G. Veron, and R.K. Wayne Multigene phylogeny of the Mustelidae: resolving relationships, tempo and biogeographic history of a mammalian adaptive radiation BMC Biol. 6 2008 10
28. J.R. Kornegay, J.W. Schilling, and A.C. Wilson Molecular adaptation of a leaf-eating bird: stomach lysozyme of the hoatzin Mol. Biol. Evol. 11 1994 921 928
29. M.F. Lovo-Farah, M. One, J.C. Novello, M.H. Toyama, J. Perales, H. Moussatche, G.B. Domont, B. Oliveira, and S. Marangoni Isolation of protein factors from opossum (Didelphis albiventris) serum which protect against Bothrops jararaca venom Toxicon 34 1996 1067 1071
30. W.P. Maddison, and D.R. Maddison Mesquite: a Modular System for Evolutionary Analysis 2011 Version 2.75 http://mesquiteproject.org
31. L. McDougall The Complete Tracker: Tracks, Signs, and Habits of North American Wildlife. Connecticut 1997 The Global Pequot Press
32. P.A. Melo, and G. Suarez-Kurtz Release of sarcoplasmic enzymes from skeletal muscle by Bothrops jararacussu venom: antagonism by heparin and by the serum of South American marsupials Toxicon 26 1988 87 95
33. J.M. Menchaca, and J.C. Perez The purification and characterization of an antihemorrhagic factor in opossum (Didelphis virginiana) serum Toxicon 19 1981 623
34. R.W. Meredith, J.E. Janecka, J. Gatesy, O.A. Ryder, C.A. Fisher, E.C. Teeling, A. Goodbla, E. Eizirik, T.L.L. Simao, T. Stadler, and D.L. Rabosky et al. Impacts of the cretaceous terrestrial revolution and KPg extinction on mammal diversification Science 334 2011 521 524
35. M.W. Nachman, H.E. Hoekstra, and S.L. D'Agostino The genetic basis of adaptive melanism in pocket mice Proc. Natl. Acad. Sci. U. S. A. 100 2003 5268 5273
36. D. Neumann, D. Barchan, M. Fridkin, and S. Fuchs Analysis of ligand binding to the synthetic dodecapeptide 185-196 of the acetylcholine receptor alpha subunit Proc. Natl. Acad. Sci. U. S. A. 83 1986 9250 9253
37. A.G.C. Neves-Ferreira, R.H. Valente, J. Perales, and G.B. Domont Natural inhibitors: innate immunity to snake venoms S.P. Mackessy, Handbook of Venoms and Toxins of Reptiles 2010 CRC Press Boca Raton 259 284
38. J.C. Perez, S. Pichyangkul, and V.E. Garcia The resistance of three species of warm-blooded animals to western diamondback rattlesnake (Crotales atrox) venom Toxicon 17 1979 601
39. N. Reeve Hedgehogs. T & AD Poyser (Natural History), London 1994
40. L. Rousseau The Dark Stream: the Story of Eugène N Marais 1982 Jonathan Ball Johannesburg
41. Y. Shi, F.B. Radlwimmer, and S. Yokoyama Molecular genetics and the evolution of ultraviolet vision in vertebrates Proc. Natl. Acad. Sci. U. S. A. 98 2001 11731 11736
42. Y. Shi, and S. Yokoyama Molecular analysis of the evolutionary significance of ultraviolet vision in vertebrates Proc. Natl. Acad. Sci. U. S. A. 100 2003 8308 8313
43. Z. Takacs, K.C. Wilhelmsen, and S. Sorota Snake α-neurotoxin binding site on the Egyptian cobra (Naja haje) nicotinic acetylcholine receptor is conserved Mol. Biol. Evol. 18 2001 1800 1809
44. Z. Takacs, K.C. Wilhelmsen, and S. Sorota Cobra (Naja spp.) nicotinic acetylcholine receptor exhibits resistance to Erabu sea snake (Laticauda semifasciata) short-chain α-neurotoxin J. Mol. Evol. 58 2004 516 526
45. S.F. Tarng, S.Y. Huang, and J.C. Pérez Isolation of antihemorrhagic factors in opossum (Didelphis virginiana) serum using a monoclonal antibody immunoadsorbent Toxicon 24 1986 567 573
46. S.J. Tzartos, and M.S. Remoundos Fine localization of the major alpha-bungarotoxin binding site to residues alpha 189-195 of the Torpedo acetylcholine receptor. Residues 189, 190, and 195 are indispensable for binding J. Biol. Chem. 256 1990 21462 21467
47. R.S. Voss, and S.A. Jansa Snake-venom resistance as a mammalian trophic adaptation: lessons from didelphid marsupials Biol. Rev. 87 2012 822 837
48. O.B. Waxman A Brief History of the Honey Badger: in Light of the PBS Nature Documentary on the Honey Badger Airing Tonight, Some Background on 2011's Favorite Viral Video 2014 Time. URL http://newsfeed.time.com/2014/02/19/a-brief-history-of-the-honey-badger-meme/
49. Z. Yang PAML 4: Phylogenetic analysis by maximum likelihood Mol. Biol. Evol. 24 2007 1586 1591
50. Z. Yang, W.S.W Wong, and R. Nielsen Bayes empirical Bayes inference of amino acid sites under positive selection Mol. Biol. Evol. 22 2005 1107 1118
51. S. Yokoyama Molecular genetic basis of adaptive selection: examples from color vision in vertebrates Annu. Rev. Genet. 105 1998 13480 13485
52. S. Yokoyama, and T. Tada Adaptive evolution of the African and Indonesian coelacanths to deep-sea environments Gene 261 2000 35 42
53. J. Zhang Parallel adaptive origins of digestive RNases in Asian and African leaf monkeys Nat. Genet. 38 2006 819 823