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Convergent Recruitment of Proteins Into Animal Venoms

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Convergent Recruitment of Proteins Into Animal Venoms ANRV386-GG10-22 ARI 7 August 2009 8:22 The Toxicogenomic Multiverse: Convergent Recruitment of Proteins Into Animal Venoms Bryan G. Fry,1 Kim Roelants,2,∗,∗∗ Donald E. Champagne,3 Holger Scheib,4 Joel D.A. Tyndall,5 Glenn F. King,6 Timo J. Nevalainen,7 Janette A. Norman,8,∗∗ Richard J. Lewis,6 Raymond S. Norton,9,∗∗ Camila Renjifo,10 and Ricardo C. Rodrıguez´ de la Vega11 1Department of Biochemistry and Molecular Biology, Bio21 Institute, University of Melbourne, Melbourne 3010 Australia; email: [email protected] Annu. Rev. Genomics Hum. Genet. 2009. Key Words 10:483–511 toxin, phylogeny, evolution, convergence First published online as a Review in Advance on July 16, 2009 Abstract The Annual Review of Genomics and Human Genetics Throughout evolution, numerous proteins have been convergently is online at genom.annualreviews.org recruited into the venoms of various animals, including centipedes, This article’s doi: cephalopods, cone snails, fish, insects (several independent venom sys- 10.1146/annurev.genom.9.081307.164356 tems), platypus, scorpions, shrews, spiders, toxicoferan reptiles (lizards Copyright c 2009 by Annual Reviews. and snakes), and sea anemones. The protein scaffolds utilized con- by UNIVERSITY OF MELBOURNE on 10/08/09. For personal use only. All rights reserved vergently have included AVIT/colipase/prokineticin, CAP, chitinase, 1527-8204/09/0922-0483$20.00 cystatin, defensins, hyaluronidase, Kunitz, lectin, lipocalin, natriuretic ∗ See page 511 for coauthor affiliations. peptide, peptidase S1, phospholipase A2, sphingomyelinase D, and Annu. Rev. Genom. Human Genet. 2009.10:483-511. Downloaded from arjournals.annualreviews.org SPRY. Many of these same venom protein types have also been con- vergently recruited for use in the hematophagous gland secretions of invertebrates (e.g., fleas, leeches, kissing bugs, mosquitoes, and ticks) and vertebrates (e.g., vampire bats). Here, we discuss a number of over- arching structural, functional, and evolutionary generalities of the pro- tein families from which these toxins have been frequently recruited and propose a revised and expanded working definition for venom. Given the large number of striking similarities between the protein composi- tions of conventional venoms and hematophagous secretions, we argue that the latter should also fall under the same definition. 483 ANRV386-GG10-22 ARI 7 August 2009 8:22 INTRODUCTION combinations of proteins (ranging from multi- unit globular enzymes to small peptides), salts, Venom systems are key evolutionary innova- and organic molecules such as polyamines, tions in a broad phylogenetic range of animal amino acids, and neurotransmitters (49, 54, 72, lineages and are used for defense, competitor 117, 144). Proteins found in venoms are the deterrence, or predation (or a combination result of toxin recruitment events in which an thereof ). Apart from the extensively studied, ordinary protein gene, typically one involved in medically important clades (snakes, scorpions, a key regulatory process, is duplicated, and the and spiders), venomous animals include sea new gene is selectively expressed in the venom anemones, jellyfish, sea snails, cephalopods, gland. In many cases, such toxin genes were am- centipedes, several insect orders, echinoderms, plified to obtain multigene families with exten- fish, lizards, and even some mammals (platypus sive neofunctionalization (54, 81), followed by and shrews). Modes of venom delivery are the deletion of some copies and degradation of likewise diverse and include barbs, beaks, others to nonfunctional copies or pseudogenes fangs or modified teeth, harpoons, nemato- (59). The newly created toxin multigene fam- cysts, pinchers, proboscises, spines, sprays, ilies often preserve the molecular scaffold (in- spurs, and stingers. Targetsof venom action in- cluding the tertiary structure) of the ancestral clude virtually all major physiological pathways protein, but key functional residues outside the and tissue types accessible by the bloodstream. core scaffold are modified to acquire a myriad Venom delivery systems sometimes show of newly derived activities (38, 53, 54, 59, 123). great variation in structure and complexity, Despite the extraordinary diversity in the even within a single venomous clade. Within structure and function of animal venom sys- the reptile clade Toxicofera, for example, tems, several protein groups have been conver- venom was a single ancient innovation; igua- gently recruited for use as venom toxins in mul- nian and anguimorph lizards share a com- tiple animal lineages (Table 1). The convergent mon venomous ancestor with snakes (56). In origin of toxins across the entire metazoan spec- iguanian species, venom glands develop only trum suggests that there are functional and/or to an incipient stage and seem to have lit- structural constraints on the evolution of ani- tle ecological relevance. However, anguimorph mal venoms. Intriguingly, some of the proteins lizards (e.g., monitor lizards and Gila mon- recruited as venom toxins are also recruited by sters) have a derived, encapsulated, and com- hematophagous insects for utilization in their partmentalized mandibular venom gland with feeding secretions; with a wide range of con- developmentally suppressed maxillary glands vergent activities within the neurological and (56). In contrast, snakes possess highly de- hematological systems. The aim of this review by UNIVERSITY OF MELBOURNE on 10/08/09. For personal use only. veloped but non-compartmentalized maxillary is thus twofold: ( ) to consider the structural and venom glands with developmentally suppressed a functional constraints on recruitment and evo- mandibular glands. Spread across the advanced lution of venom proteins and ( ) to explore the snakes is an enormous variation of fang and b implications of these findings for the definition Annu. Rev. Genom. Human Genet. 2009.10:483-511. Downloaded from arjournals.annualreviews.org venom gland morphologies (55) that arose from of what constitutes a venomous animal. the ancient serpent dental uncoupling (156). Further, within the advanced snakes, diver- gence has resulted in four derived lineages [twice within the Lamprophiidae family (Atrac- CONVERGENTLY RECRUITED taspis and Homoroselaps genera), and once each PROTEIN FAMILIES at the base of the Elapidae and Viperidae fami- lies] that possess intricate hollow-front, fanged, AVIT/Colipase/Prokineticin and high-pressure delivery systems (55). First isolated from black mamba venom Venoms across the Kingdom Animalia (mamba intestinal toxin 1, MIT-1) (21, are complex mixtures that include variable 142), AVIT peptides have subsequently been 484 Fry et al. ANRV386-GG10-22 ARI 7 August 2009 8:22 Table 1 Convergently recruited proteins∗ AVIT CAP Chi Cys Def Hya Kun Lec Lip Nat PS1 PLA2 Sm-D SPRY Amphibian X Cephalopod X X X X X Cnidarian X X Cone snail X X Fish X X X Insect (bristle) X X X X X Insect (proboscis) X X X X X X X X Insect (stinger) X X X X X X Platypus X X Scorpion X X X X X Shrew X Spider X X X X(2) X Reptile X X X(2) X X X X X X X X(3) X Tick X X X X X X X X ∗Abbreviations used: CAP, CRISP (cysteine rich secretory proteins), antigen 5 (Ag5) and pathogenesis-related (PR-1) proteins; Chi, chitinase; Cys, cystatin; Def, defensin; Hya, hyaluronidase; Kun, kunitz; lec, lectin; Lip, lipocalin; Nat, natriuretic peptide; PS1, peptidase S1; PLA2, phospholipase A2; Sm-D, sphingomyelinase. identified in the venom of monitor lizards as peptides (MIT-like atracotoxins, ACTX) that part of the Toxicofera reptile core chemical ar- show a similar motif as vertebrate AVIT senal (56). Similar bioactive peptides are found peptides consisting of 10 conserved cysteine in the defensive skin secretions of Bombina fire- residues (148, 162). However, these peptides bellied toads (Bm8, Bo8, and Bv8) (30, 31, 102). test negative in assays of PK1/PK2 activity, AVIT scaffold peptides found in reptile venom lack the N-terminal AVIT sequence, and are and Bombina skin secretion defensive toxins much more diverse in amino acid composition, are potent agonists of mammalian prokineticin sequence length, and scaffold shape. Consistent receptors, and their binding mimics the effect with the likelihood that they fulfill distinct func- of an endogenous prokineticin overdose. This tions, comparative three-dimensional model- effect is reinforced by their highly elevated effi- ing of AVIT and MIT-like ACTX peptides ciency in binding mammal receptors; both Bv8 has shown dissimilar tertiary structures and and MIT-1 bind to mammal PKR1 and PKR2 markedly different surface chemistries. These by UNIVERSITY OF MELBOURNE on 10/08/09. For personal use only. (prokineticin receptors 1 and 2) with an affinity results are perhaps not surprising because that exceeds that of the normal mammalian insects, which constitute the majority of spider peptide PK2 (prokineticin 2) by one order of prey, appear to lack the PK/PKR system. So far, magnitude and that of PK1 (prokineticin 1) by insecticidal assays have not revealed a lethal ef- Annu. Rev. Genom. Human Genet. 2009.10:483-511. Downloaded from arjournals.annualreviews.org two orders of magnitude (108). Their toxicity is fect, even at high doses (148). Nevertheless, the mainly determined by their two potent short- diversity of MIT-like ACTX peptides within term physiological effects (within minutes), individual species, their presence in a broad namely gastric smooth muscle contraction phylogenetic range of spiders (suggesting their and hyperalgesia (increased pain sensitivity). ancient
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