抑制剂胱氨酸结多肽的抗菌和杀虫活性及进化
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摘要
抑制剂胱氨酸结(inhibitor cystine knot, ICK)多肽是胱氨酸结(cystine knot, CK)多肽的三大家族成员之一。这种类型的多肽含有反向平行的3个β折叠,由3对二硫键形成稳定的拓扑学打结。它们广泛地分布在动物、植物、真菌甚至原核生物中,具有蛋白酶抑制剂,离子通道毒素以及抗微生物、抗疟疾及抗病毒活性等多种生物学功能。本文首先总结了昆虫中已发现的抗微生物活性和离子通道毒素活性的ICK肽;然后介绍了有毒动物尤其是蜘蛛、蝎子,以及植物中一些神经毒素活性的ICK肽,它们通常靶向昆虫体内的各种离子通道,从而发挥杀虫效果;最后结合ICK肽的基因序列特征,结构域和二硫键数目以及物种分布,对其进化多样性进行了探讨。
Inhibitor cystine knot(ICK) peptides are one of the three family members of cystine knot(CK) peptides. Peptides of this kind consist of a triplet-stranded antiparallel β-sheet stabilized by three disulfide bonds to form a topological knot. They are widely distributed in animals, plants, fungi and even prokaryotes, exhibiting a diversity of biological functions including protease inhibitors, ion channel toxins, and antimicrobial, antimalarial and antiviral activities. In this article, we firstly summarized the ICK peptides found in insects with antimicrobial and ion channel toxin activities, and then introduced some neurotoxic ICK peptides in poisonous animals especially spiders and scorpions, as well as plants. These toxins usually target various ion channels of insects to exert their insecticidal activity. Finally, we discussed the evolutionary diversity of ICK peptides in combination with their gene sequence characteristics, the numbers of their domains and disulfide bonds and species distribution.
Inhibitor cystine knot(ICK) peptides are one of the three family members of cystine knot(CK) peptides. Peptides of this kind consist of a triplet-stranded antiparallel β-sheet stabilized by three disulfide bonds to form a topological knot. They are widely distributed in animals, plants, fungi and even prokaryotes, exhibiting a diversity of biological functions including protease inhibitors, ion channel toxins, and antimicrobial, antimalarial and antiviral activities. In this article, we firstly summarized the ICK peptides found in insects with antimicrobial and ion channel toxin activities, and then introduced some neurotoxic ICK peptides in poisonous animals especially spiders and scorpions, as well as plants. These toxins usually target various ion channels of insects to exert their insecticidal activity. Finally, we discussed the evolutionary diversity of ICK peptides in combination with their gene sequence characteristics, the numbers of their domains and disulfide bonds and species distribution.
引文
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Bende NS, Dziemborowicz S, Herzig V, Ramanujam V, Brown GW, Bosmans F, Nicholson GM, King GF, Mobli M, 2015. The insecticidal spider toxin SFI1 is a knottin peptide that blocks the pore of insect voltage-gated sodium channels via a large beta-hairpin loop. FEBS J., 282(5): 904-920.
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Bernard C, Corzo G, Mosbah A, Nakajima T, Darbon H, 2001. Solution structure of Ptu1, a toxin from the assassin bug Peirates turpis that blocks the voltage-sensitive calcium channel N-type. Biochemistry, 40(43): 12795-12800.
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Hardy MC, Daly NL, Mobli M, Morales RA, King GF, 2013. Isolation of an orally active insecticidal toxin from the venom of an Australian tarantula. PLoS ONE, 8(9): e73136.
Hariton Shalev A, Sobol I, Ghanim M, Liu SS, Czosnek H, 2016. The whitefly Bemisia tabaci knottin-1 gene is implicated in regulating the quantity of tomato yellow leaf curl virus ingested and transmitted by the insect. Viruses, 8(7): 205.
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Barbault F, Landon C, Guenneugues M, Meyer JP, Schott V, Dimarcq JL, Vovelle F, 2003. Solution structure of Alo-3: a new knottin-type antifungal peptide from the insect Acrocinus longimanus. Biochemistry, 42(49): 14434-14442.
Bende NS, Dziemborowicz S, Herzig V, Ramanujam V, Brown GW, Bosmans F, Nicholson GM, King GF, Mobli M, 2015. The insecticidal spider toxin SFI1 is a knottin peptide that blocks the pore of insect voltage-gated sodium channels via a large beta-hairpin loop. FEBS J., 282(5): 904-920.
Bende NS, Kang E, Herzig V, Bosmans F, Nicholson GM, Mobli M, King GF, 2013. The insecticidal neurotoxin Aps III is an atypical knottin peptide that potently blocks insect voltage-gated sodium channels. Biochem. Pharmacol., 85(10): 1542-1554.
Bernard C, Corzo G, Adachi-Akahane S, Foures G, Kanemaru K, Furukawa Y, Nakajima T, Darbon H, 2004. Solution structure of ADO1, a toxin extracted from the saliva of the assassin bug, Agriosphodrus dohrni. Proteins, 54(2): 195-205.
Bernard C, Corzo G, Mosbah A, Nakajima T, Darbon H, 2001. Solution structure of Ptu1, a toxin from the assassin bug Peirates turpis that blocks the voltage-sensitive calcium channel N-type. Biochemistry, 40(43): 12795-12800.
Bloch G, Cohen M, 2014. The expression and phylogenetics of the Inhibitor Cysteine Knot peptide OCLP1 in the honey bee Apis mellifera. J. Insect Physiol., 65: 1-8.
Bohlen CJ, Priel A, Zhou S, King D, Siemens J, Julius D, 2010. A bivalent tarantula toxin activates the capsaicin receptor, TRPV1, by targeting the outer pore domain. Cell, 141(5): 834-845.
Candido-Silva JA, Zanarotti GM, Gallina AP, de Almeida JC, 2007. Developmental regulation of BhSGAMP-1, a gene encoding an antimicrobial peptide in the salivary glands of Bradysia hygida (Diptera, Sciaridae). Genesis, 45(10): 630-638.
Chen J, Xu Y, San MK, Cao ZJ, Li WX, Wu YL, Chen ZY, 2015. Cloning and genomic characterization of a natural insecticidal peptide LaIT1 with unique DDH structural fold. J. Biochem. Mol. Toxicol., 29(5): 207-212.
Choi SJ, Parent R, Guillaume C, Deregnaucourt C, Delarbre C, Ojcius DM, Montagne JJ, Celerier ML, Phelipot A, Amiche M, Molgo J, Camadro JM, Guette C, 2004. Isolation and characterization of Psalmopeotoxin I and II: two novel antimalarial peptides from the venom of the tarantula Psalmopoeus cambridgei. FEBS Lett., 572(1-3): 109-117.
Chouabe C, Eyraud V, Da Silva P, Rahioui I, Royer C, Soulage C, Bonvallet R, Huss M, Gressent F, 2011. New mode of action for a knottin protein bioinsecticide: pea albumin 1 subunit b (PA1b) is the first peptidic inhibitor of V-ATPase. J. Biol. Chem., 286(42): 36291-36296.
Craik DJ, Daly NL, Waine C, 2001. The cystine knot motif in toxins and implications for drug design. Toxicon, 39(1): 43-60.
Da Silva P, Strzepa A, Jouvensal L, Rahioui I, Gressent F, Delmas AF, 2009. A folded and functional synthetic PA1b: an interlocked entomotoxic miniprotein. Biopolymers, 92(5): 436-444.
Daquinag AC, Sato T, Koda H, Takao T, Fukuda M, Shimonishi Y, Tsukamoto T, 1999. A novel endogenous inhibitor of phenoloxidase from Musca domestica has a cystine motif commonly found in snail and spider toxins. Biochemistry, 38(7): 2179-2188.
Deng YC, Gu JW, Nie F, Xiao L, 2016. Cystine knot peptide’s properties and its applications for drug design and molecular engineering. J. Pharm. Pract., 34(6): 481-484, 496. [邓宇晨, 顾嘉伟, 聂菲, 肖良, 2016. 胱氨酸结模体多肽的特征及其在药物设计和分子工程中的应用. 药学实践杂志, 34(6): 481-484, 496]
Gao B, Harvey PJ, Craik DJ, Ronjat M, De Waard M, Zhu SY, 2013. Functional evolution of scorpion venom peptides with an inhibitor cystine knot fold. Biosci. Rep., 33(3): 513-527.
Gelly JC, Gracy J, Kaas Q, Le-Nguyen D, Heitz A, Chiche L, 2004. The KNOTTIN website and database: a new information system dedicated to the knottin scaffold. Nucleic Acids Res., 32(Database issue): D156-D159.
Gracy J, Le-Nguyen D, Gelly JC, Kaas Q, Heitz A, Chiche L, 2008. KNOTTIN: the knottin or inhibitor cystine knot scaffold in 2007. Nucleic Acids Res., 36(Database issue): D314-D319.
Hardy MC, Daly NL, Mobli M, Morales RA, King GF, 2013. Isolation of an orally active insecticidal toxin from the venom of an Australian tarantula. PLoS ONE, 8(9): e73136.
Hariton Shalev A, Sobol I, Ghanim M, Liu SS, Czosnek H, 2016. The whitefly Bemisia tabaci knottin-1 gene is implicated in regulating the quantity of tomato yellow leaf curl virus ingested and transmitted by the insect. Viruses, 8(7): 205.
Herzig V, King GF, 2015. The cystine knot is responsible for the exceptional stability of the insecticidal spider toxin omega-Hexatoxin-Hv1a. Toxins (Basel), 7(10): 4366-4380.
Horita S, Matsushita N, Kawachi T, Ayabe R, Miyashita M, Miyakawa T, Nakagawa Y, Nagata K, Miyagawa H, Tanokura M, 2011. Solution structure of a short-chain insecticidal toxin LaIT1 from the venom of scorpion Liocheles australasiae. Biochem. Biophys. Res. Commun., 411(4): 738-744.
Hwang B, Hwang JS, Lee J, Lee DG, 2010. Antifungal properties and mode of action of psacotheasin, a novel knottin-type peptide derived from Psacothea hilaris. Biochem. Biophys. Res. Commun., 400(3): 352-357.
Hwang B, Hwang JS, Lee J, Lee DG, 2011. The antimicrobial peptide, psacotheasin induces reactive oxygen species and triggers apoptosis in Candida albicans. Biochem. Biophys. Res. Commun., 405(2): 267-271.
Hwang JS, Lee J, Hwang B, Nam SH, Yun EY, Kim SR, Lee DG, 2010. Isolation and characterization of psacotheasin, a novel knottin-type antimicrobial peptide, from Psacothea hilaris. J. Microbiol. Biotechnol., 20(4): 708-711.
Jouvensal L, Quillien L, Ferrasson E, Rahbe Y, Gueguen J, Vovelle F, 2003. PA1b, an insecticidal protein extracted from pea seeds (Pisum sativum): 1H-2-D NMR study and molecular modeling. Biochemistry, 42(41): 11915-11923.
Khan SA, Zafar Y, Briddon RW, Malik KA, Mukhtar Z, 2006. Spider venom toxin protects plants from insect attack. Transgenic Res., 15(3): 349-357.
Kintzing JR, Cochran JR, 2016. Engineered knottin peptides as diagnostics, therapeutics, and drug delivery vehicles. Curr. Opin. Chem. Biol., 34: 143-150.
Kuhn-Nentwig L, Fedorova IM, Luscher BP, Kopp LS, Trachsel C, Schaller J, Vu XL, Seebeck T, Streitberger K, Nentwig W, Sigel E, Magazanik LG, 2012. A venom-derived neurotoxin, CsTx-1, from the spider Cupiennius salei exhibits cytolytic activities. J. Biol. Chem., 287(30): 25640-25649.
Kuzmenkov AI, Fedorova IM, Vassilevski AA, Grishin EV, 2013. Cysteine-rich toxins from Lachesana tarabaevi spider venom with amphiphilic C-terminal segments. Biochim. Biophys. Acta, 1828(2): 724-731.
Li DL, Xiao YC, Hu WJ, Xie JY, Bosmans F, Tytgat J, Liang SP, 2003. Function and solution structure of hainantoxin-I, a novel insect sodium channel inhibitor from the Chinese bird spider Selenocosmia hainana. FEBS Lett., 555(3): 616-622.
Matsubara FH, Meissner GO, Herzig V, Justa HC, Dias BC, Trevisan-Silva D, Gremski LH, Gremski W, Senff-Ribeiro A, Chaim OM, King GF, Veiga SS, 2017. Insecticidal activity of a recombinant knottin peptide from Loxosceles intermedia venom and recognition of these peptides as a conserved family in the genus. Insect Mol. Biol., 26(1): 25-34.
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