NMR structure of bitistatin - A missing piece in the evolutionary pathway of snake venom disintegrins

FEBS Journal

Volumn 282, Issue 2, 2015, Pages 341-360

  Carbajo, Rodrigo J ^a   Sanz, Libia ^b   Perez, Alicia ^b   Calvete, Juan J ^b  

^a CENTRO DE INVESTIGACIÓN PRÍNCIPE FELIPE   (Spain)

^b INSTITUTO DE BIOMEDICINA DE VALENCIA   (Spain)

Author keywords

disintegrin bitistatin; integrin antagonist; molecular evolution; NMR structure; snake venom protein

Indexed keywords

BITISTATIN; DISINTEGRIN; PEPTIDE; SNAKE VENOM;

AMINO ACID SEQUENCE; ANIMAL; CHEMISTRY; GENETICS; MOLECULAR EVOLUTION; PHYLOGENY; STRUCTURE ACTIVITY RELATION; VIPERIDAE; X RAY CRYSTALLOGRAPHY;

AMINO ACID SEQUENCE; ANIMALS; CRYSTALLOGRAPHY, X-RAY; DISINTEGRINS; EVOLUTION, MOLECULAR; PEPTIDES; PHYLOGENY; SNAKE VENOMS; STRUCTURE-ACTIVITY RELATIONSHIP; VIPERIDAE;

EID: 84926107653     PISSN: 1742464X     EISSN: 17424658     Source Type: Journal    
DOI: 10.1111/febs.13138     Document Type: Article

References (72)

1. Escalante T, Rucavado A, Fox JW, &, Gutiérrez JM, (2011) Key events in microvascular damage induced by snake venom hemorrhagic metalloproteinases. J Proteomics 74, 1781-1794.
2. Markland FS, &, Swenson S, (2013) Snake venom metalloproteinases. Toxicon 62, 3-18.
3. Fry BG, Vidal N, Norman JA, Vonk FJ, Scheib H, Ramjan SF, Kuruppu S, Fung K, Hedges SB, Richardson MK, et al,. (2006) Early evolution of the venom system in lizards and snakes. Nature 439, 584-588.
4. Fry BG, Casewell NR, Wüster W, Vidal N, Young B, &, Jackson TN, (2012) The structural and functional diversification of the Toxicofera reptile venom system. Toxicon 60, 434-448.
5. Hedges SB, &, Vidal N, (2009) Lizards, snakes, and amphisbaenians (Squamata). In The Timetree of Life (, Hedges SB, &, Kumar S, eds), pp. 383-389. University Press, Oxford.
6. Alföldi J, Di Palma F, Grabherr M, Williams C, Kong L, Mauceli E, Russell P, Lowe CB, Glor RE, Jaffe JD, et al,. (2011) The genome of the green anole lizard and a comparative analysis with birds and mammals. Nature 477, 587-591.
7. Casewell NR, (2012) On the ancestral recruitment of metalloproteinases into the venom of snakes. Toxicon 60, 449-454.
8. Fox JW, &, Serrano SMT, (2008) Insights into and speculations about snake venom metalloproteinase (SVMP) synthesis, folding and disulfide bond formation and their contribution to venom complexity. FEBS J 275, 3016-3030.
9. Takeda S, Takeya H, &, Iwanaga S, (2012) Snake venom metalloproteinases: structure, function and relevance to the mammalian ADAM/ADAMTS family proteins. Biochim Biophys Acta 1824, 164-176.
10. Moura-da-Silva AM, Theakston RD, &, Crampton JM, (1996) Evolution of disintegrin cysteine-rich and mammalian matrix-degrading metalloproteinases: gene duplication and divergence of a common ancestor rather than convergent evolution. J Mol Evol 43, 263-269.
11. Casewell NR, Wagstaff SC, Harrison RA, Renjifo C, &, Wüster W, (2011) Domain loss facilitates accelerated evolution and neofunctionalization of duplicate snake venom metalloproteinase toxin genes. Mol Biol Evol 28, 2637-2649.
12. Fox JW, &, Serrano SMT, (2005) Structural considerations of the snake venom metalloproteinases, key members of the M12 reprolysin family of metalloproteinases. Toxicon 45, 969-985.
13. Lu X, Lu D, Scully MF, &, Kakkar VV, (2005) Snake venom metalloproteinase containing a disintegrin-like domain, its structure-activity relationships at interacting with integrins. Curr Med Chem Cardiovasc Hematol Agents 3, 249-260.
14. Tan NH, &, Saifuddin MN, (1990) Isolation and characterization of a hemorrhagin from the venom of Ophiophagus hannah (king cobra). Toxicon 28, 385-392.
15. Peichoto ME, Tavares FL, Santoro ML, &, Mackessy SP, (2012) Venom proteomes of South and North American opisthoglyphous (Colubridae and Dipsadidae) snake species: a preliminary approach to understanding their biological roles. Comp Biochem Physiol Part D Genomics Proteomics 7, 361-369.
16. Ovadia M, (1987) Isolation and characterization of a hemorrhagic factor from the venom of the snake Atractaspis engaddensis (Atractaspididae). Toxicon 25, 621-630.
17. Fry BG, (2005) From genome to 'venome': molecular origin and evolution of the snake venom proteome inferred from phylogenetic analysis of toxin sequences and related body proteins. Genome Res 15, 403-420.
18. Pyron RA, &, Burbrink FT, (2012) Extinction, ecological opportunity, and the origins of global snake diversity. Evolution 66, 163-178.
19. Okuda D, Koike H, &, Morita T, (2002) A new gene structure of the disintegrin family: a subunit of dimeric disintegrin has a short coding region. Biochemistry 41, 14248-14254.
20. Kini R, &, Evans HJ, (1992) Structural domains in venom proteins: evidence that metalloproteinases and nonenzymatic platelet aggregation inhibitors (disintegrins) from snake venoms are derived by proteolysis from a common precursor. Toxicon 30, 265-293.
21. Calvete JJ, Moreno-Murciano MP, Theakston RDG, Kisiel DG, &, Marcinkiewicz C, (2003) Snake venom disintegrins: novel dimeric disintegrins and structural diversification by disulfide bond engineering. Biochem J 372, 725-734.
22. 1 antagonist from Eristocophis macmahoni venom. Biochem J 345, 573-581.
23. Bilgrami S, Tomar S, Yadav S, Kaur P, Kumar J, Jabeen T, Sharma S, &, Singh TP, (2004) Crystal structure of schistatin, a disintegrin homodimer from saw-scaled viper (Echis carinatus) at 2.5 Å resolution. J Mol Biol 341, 829-837.
24. Bilgrami S, Yadav S, Sharma S, Perbandt M, Betzel C, &, Singh TP, (2005) Crystal structure of the disintegrin heterodimer from saw-scaled viper (Echis carinatus) at 1.9 Å resolution. Biochemistry 44, 11058-11066.
25. Calvete JJ, Juárez P, &, Sanz L, (2009) Snake venomics and disintegrins. Portrait and evolution of a family of snake venom integrin antagonists. In Handbook of Venoms and Toxins of Reptiles (, Mackessy SP, ed.), pp. 337-357. CRC Press, Taylor & Francis, Boca Ratõn.
26. Calvete JJ, (2010) Brief history and molecular determinants of snake venom disintegrin evolution. In Toxins and Hemostasis: from Bench to Bedside (, Kini RM, Markland F, McLane MA, &, Morita T, eds), pp. 285-300. Springer Verlag, Amsterdam.
27. Juárez P, Comas I, González-Candelas F, &, Calvete JJ, (2008) Evolution of snake venom disintegrins by positive Darwinian selection. Mol Biol Evol 25, 2391-2407.
28. Scarborough RM, Rose JW, Hsu MA, Phillips DR, Fried VA, Campbell AM, Nannizzi L, &, Charo IF, (1991) Barbourin. A GPIIb-IIIa-specific integrin antagonist from the venom of Sistrurus m. barbouri. J Biol Chem 266, 9359-9362.
29. 1 integrin. Curr Pharm Des 13, 2853-2859.
30. 1 integrin. Biochem J 417, 95-101.
31. Sanz-Soler R, Lorente C, Company B, Sanz L, Juárez P, Pérez A, Zhang Y, Jin Y, Chen R, Eble JA, et al,. (2012) Recombinant expression of mutants of the Frankenstein disintegrin, RTS-ocellatusin. Evidence for the independent origin of RGD and KTS/RTS disintegrins. Toxicon 60, 665-675.
32. Takeda S, Igarashi T, Mori H, &, Araki S, (2006) Crystal structures of VAP1 reveal ADAMs' MDC domain architecture and its unique C-shaped scaffold. EMBO J 25, 2388-2396.
33. Takeda S, Igarashi T, &, Mori H, (2007) Crystal structure of RVV-X: an example of evolutionary gain of specificity by ADAM proteinases. FEBS Lett 581, 5859-5864.
34. Igarashi T, Araki S, Mori H, &, Takeda S, (2007) Crystal structures of catrocollastatin/VAP2B reveal a dynamic, modular architecture of ADAM/adamalysin/reprolysin family proteins. FEBS Lett 581, 2416-2422.
35. Muniz JR, Ambrosio AL, Selistre-de-Araujo HS, Cominetti MR, Moura-da-Silva AM, Oliva G, Garratt RC, &, Souza DH, (2008) The three-dimensional structure of bothropasin, the main hemorrhagic factor from Bothrops jararaca venom: insights for a new classification of snake venom metalloprotease subgroups. Toxicon 52, 807-816.
36. Zhu Z, Gao Y, Zhu Z, Yu Y, Zhang X, Zang J, Teng M, &, Niu L, (2009) Structural basis of the autolysis of AaHIV suggests a novel target recognizing model for ADAM/reprolysin family proteins. Biochem Biophys Res Commun 386, 159-164.
37. Guan HH, Goh KS, Davamani F, Wu PL, Huang YW, Jeyakanthan J, Wu WG, &, Chen CJ, (2010) Structures of two elapid snake venom metalloproteases with distinct activities highlight the disulfide patterns in the D domain of ADAMalysin family proteins. J Struct Biol 169, 294-303.
38. Senn H, &, Klaus W, (1993) The nuclear magnetic resonance solution structure of flavoridin, an antagonist of the platelet GP IIb-IIIa receptor. J Mol Biol 232, 907-925.
39. 1H NMR spectroscopy and simulated annealing calculations. Int J Pept Protein Res 48, 220-228.
40. Shin J, Hong SY, Chung K, Kang I, Jang Y, Kim SD, &, Lee W, (2003) Solution structure of a novel disintegrin, salmosin, from Agkistrondon halys venom. Biochemistry 42, 14408-14415.
41. 1H NMR and restrained molecular dynamics. Int J Pept Protein Res 43, 563-572.
42. Monleõn D, Esteve V, Kovacs H, Calvete JJ, &, Celda B, (2005) Conformation and concerted dynamics of the integrin-binding site and the C-terminal region of echistatin revealed by homonuclear NMR. Biochem J 387, 57-66.
43. Moreno-Murciano MP, Monleõn D, Marcinkiewicz C, Calvete JJ, &, Celda B, (2003) NMR solution structure of the non-RGD disintegrin obtustatin. J Mol Biol 329, 135-145.
44. 1. Proteins 79, 2530-2542.
45. Fujii Y, Okuda D, Fujimoto Z, Horii K, Morita T, &, Mizuno H, (2003) Crystal structure of trimestatin, a disintegrin containing a cell adhesion recognition motif RGD. J Mol Biol 332, 1115-1122.
46. Moiseeva N, Bau R, Swenson SD, Markland FS Jr, Choe JY, Liu ZJ, &, Allaire M, (2008) Structure of acostatin, a dimeric disintegrin from Southern copperhead (Agkistrodon contortrix contortrix), at 1.7 Å resolution. Acta Crystallogr D Biol Crystallogr 64, 466-470.
47. Janes PW, Saha N, Barton WA, Kolev MV, Wimmer-Kleikamp SH, Nievergall E, Blobel CP, Himanen JP, Lackmann M, &, Nikolov DB, (2005) Adam meets Eph: an ADAM substrate recognition module acts as a molecular switch for ephrin cleavage in trans. Cell 123, 291-304.
48. Juárez P, Wagstaff SC, Oliver J, Sanz L, Harrison RA, &, Calvete JJ, (2006) Molecular cloning of disintegrin-like transcript BA-5A from Bitis arietans venom gland cDNA library: a putative intermediate in the evolution of the long chain disintegrin bitistatin. J Mol Evol 63, 142-152.
49. Shen Y, Delaglio F, Cornilescu G, &, Bax A, (2009) TALOS+: a hybrid method for predicting protein backbone torsion angles from NMR chemical shifts. J Biomol NMR 44, 213-223.
50. Calvete JJ, Schrader M, Raida M, McLane MA, Romero A, &, Niewiarowski S, (1997) The disulphide bond pattern of bitistatin, a disintegrin isolated from the venom of the viper Bitis arietans. FEBS Lett 416, 197-202.
51. Kwan AH, Mobli M, Gooley PR, King GF, &, Mackay JP, (2011) Macromolecular NMR spectroscopy for the non-spectroscopist. FEBS J 278, 687-703.
52. Adler M, Lazarus RA, Dennis MS, &, Wagner G, (1991) Solution structure of Kistrin, a potent platelet-aggregation inhibitor and GPIIb/IIIa antagonist. Science 253, 445-448.
53. Monleõn D, Moreno-Murciano MP, Kovacs H, Marcinkiewicz C, Calvete JJ, &, Celda B, (2003) Concerted motions of the integrin-binding loop and the C-terminal tail of the non-RGD disintegrin obtustatin. J Biol Chem 278, 45570-45576.
54. Aumailley M, Gurrath M, Müller G, Calvete J, Timpl R, &, Kessler H, (1991) Arg-Gly-Asp constrained within cyclic pentapeptides. Strong and selective inhibitors of cell adhesion to vitronectin and laminin fragment P1. FEBS Lett 291, 50-54.
55. 1 integrins. J Biol Chem 269, 20233-20238.
56. Scarborough RM, Rose JW, Naughton MA, Phillips DR, Nannizzi L, Arfsten A, Campbell AM, &, Charo IF, (1993) Characterization of the integrin specificities of disintegrins isolated from American pit viper venoms. J Biol Chem 268, 1058-1065.
57. Shebuski RJ, Ramjit DR, Bencen GH, &, Polokoff MA, (1989) Characterization and platelet inhibitory activity of bitistatin, a potent arginine-glycine-aspartic acid-containing peptide from the venom of the viper Bitis arietans. J Biol Chem 264, 21550-21556.
58. 3 on tumor and vascular cells. Nucl Med Biol 34, 371-381.
59. Burgen ASV, Roberts GCK, &, Freeney J, (1975) Binding of flexible ligands to macromolecules. Nature 253, 753-755.
60. Williams RJP, (1989) NMR studies of mobility within protein structure. Eur J Biochem 183, 479-497.
61. Calvete JJ, Schäfer W, Soszka T, Lu W, Cook JJ, Jameson BA, &, Niewiarowski S, (1991) Identification of the disulfide bond pattern in albolabrin, an RGD-containing peptide from the venom of Trimeresurus albolabris: significance for the expression of platelet aggregation inhibitory activity. Biochemistry 30, 5225-5229.
62. Bhattacharyya R, Pal D, &, Chakrabarti P, (2004) Disulfide bonds, their stereospecific environment and conservation in protein structures. Prot Eng Des Select 17, 795-808.
63. Fry BG, Roelants K, Champagne DE, Scheib H, Tyndall JD, King GF, Nevalainen TJ, Norman JA, Lewis RJ, Norton RS, et al,. (2009) The toxicogenomic multiverse: convergent recruitment of proteins into animal venoms. Annu Rev Genomics Hum Genet 10, 483-511.
64. Janes DE, Organ CL, Fujita MK, Shedlock AM, &, Edwards SV, (2010) Genome evolution in Reptilia, the sister group of mammals. Annu Rev Genomics Hum Genet 11, 239-264.
65. Barrick JE, &, Lenski RE, (2013) Genome dynamics during experimental evolution. Nature Rev Genet 14, 827-839.
66. Paine MJ, Desmond HP, Theakston RD, &, Crampton JM, (1992) Purification, cloning, and molecular characterization of a high molecular weight hemorrhagic metalloprotease, jararhagin, from Bothrops jararaca venom. Insights into the disintegrin gene family. J Biol Chem 267, 22869-22876.
67. Goddard TD, &, Kneller DG, (2001) SPARKY 3. University of California, San Francisco.
68. 15N chemical shift referencing in biomolecular NMR. J Biomolec NMR 6, 135-140.
69. Brunger AT, Adams PD, Clore GM, Gros P, Grosse-Kunstleve RW, Jiang J-S, Kuszewski J, Nilges N, Pannu NS, Read RJ, et al,. (1998) Crystallography & NMR System (CNS), a new software suite for macromolecular structure determination. Acta Cryst D54, 905-921.
70. Brunger AT, (2007) Version 1.2 of the Crystallography and NMR System. Nat Protoc 2, 2728-2733.
71. Laskowski RA, Rullmannn JA, MacArthur MW, Kaptein R, &, Thornton JM, (1996) AQUA and PROCHECK-NMR: programs for checking the quality of protein structures solved by NMR. J Biomol NMR 8, 477-486.
72. Koradi R, Billeter M, &, Wüthrich K, (1996) MOLMOL: A program for display and analysis of macromolecular structures. J Mol Graphics 14, 51-55.