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Antiviral Mechanism of Serine Protease in Various Insects

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Trends in Insect Molecular Biology and Biotechnology
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Abstract

During the last two decades, insects have had the self-ability to develop a vigorous and potent immune system that contests a huge diversity of pathogens and lead them to grow into the most distinct and efficient organisms in the world. Immune reactions against pathogens are basically characterized by invasion of their cellular and humoral response. In the present era of challenging environmental conditions, there is an urgent need for the prevention and control of viral diseases. Serine proteases (SPs) are a vast group of proteolytic enzymes that play an enormous role in anatomical systems (cell signaling, defenses, and movement, etc.); thus, they are crucial to the antiviral mechanism (hemolymph coagulation, activation of antimicrobial peptide, and melanin synthesis). They participate in various biochemical and physiochemical pathways and act as catalysts that break down the peptide bond in the protein. SPs are vital to numerous microorganisms and contribute to several structural and biochemical concerns, including a conserved catalytic triad (Ser, Asp, and His) that enacts the fundamental principle for the classification of a protein. SPs have diverse functions and play a vital role in cellular differentiation, digestion, complement activation, the immune response, and hemostasis. Recently, immunological responses in many insects such as Bombyx mori, Drosophila, Anopheles, etc., are maintained by circulatory hemocytes and performed a significant role in innate immune system, namely, the synthesis of antimicrobial proteins, encapsulation, and phenoloxidase. Most of the antimicrobial proteins such as cecropins, attacins, lebocin, moricin, gloverins, lysozyme, defensins, hemolin, etc., are effectively engaged in defense reactions against invading pathogens. For antiviral mechanisms, molecular and cell target-based analysis are valuable studies for identifying the genome and expression analysis of SPs, and their homologs in the silkworm, Drosophila melanogaster, Apis mellifera, and Anopheles gambiae, are generally considered to be model organisms for providing the relevant information regarding such biological functions. In this chapter, we devote our endeavors to the antiviral mechanism of SPs in various insects and critique the recent data on visualizing the role of antiviral pathways. Furthermore, the antiviral pathways may encounter the infectious virus towards the systemic and specific level.

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References

  • Alto BW, Bettinardi D (2013) Temperature and dengue virus infection in mosquitoes: independent effects on the immature and adult stages. Am J Trop Med Hyg 88:497–505

    Article  PubMed  PubMed Central  Google Scholar 

  • Altschul SF, Madden TL, Schaffer AA, Zhang J, Zhang Z, Miller W, Lipman DJ (1997) Gapped BLAST and PSIBLAST: a new generation of protein database search programs. Nucl Acids Res 25:3389–3402

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • An C, Ishibashi J, Ragan EJ, Jiang H, Kanost MR (2009) Functions of Manduca sexta hemolymph proteinases HP6 and HP8 in two innate immune pathways. J Biol Chem 284:19716–19726

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • An C, Zhang M, Chu Y, Zhangwu Zhao Z (2013) Serine protease MP2 activates prophenoloxidase in the melanization immune response of drosophila. PLoS One 8(11):1–10

    Article  Google Scholar 

  • Ashida M, Brey PT (1997) Recent advances in research on the insect prophenoloxidase cascade. In: Brey PT, Hultmark D (eds) Molecular mechanisms of immune responses in insects. Chapman and Hall, London, pp 135–172

    Google Scholar 

  • Ashida M, Brey PT (1998) In: Brey PT, Hultmark D (eds) Molecular mechanisms of immune responses in insects. Chapman & Hall, London, pp 135–172

    Google Scholar 

  • Bao YY, Tang XD, Lv ZY, Wang XY, Tian CH, YP X, Zhang CX (2009) Gene expression profiling of resistant and susceptible Bombyx mori strains reveals nucleopolyhedrovirus-associated variations in host gene transcript levels. Genomics 94(2):138–145

    Article  CAS  PubMed  Google Scholar 

  • Barett AJ (1994) Proteolytic enzymes: serine and cysteine peptidases. Methods Enzymol 244:1–15

    Article  Google Scholar 

  • Beier JC (1998) Malaria parasite development in mosquitoes. Annu Rev Entomol 43:519–543

    Article  CAS  PubMed  Google Scholar 

  • Bhatt S, Gething PW, Brady OJ, Messina JP, Farlow AW, Moyes CL et al (2013) The global distribution and burden of dengue. Nature 496:504–507

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cerenius L, Lee BL, Soderhall K (2008) The proPO-system: pros and cons for its role in invertebrate immunity. Trends Immunol 29:263

    Article  CAS  PubMed  Google Scholar 

  • Chang C, Liu X, Chen K (2011) Molecular cloning, expression and characterization of a novel geneβ-N-acetylglucosaminidase from Bombyx mori. Adv Biosci Biotechnol 2(2):123–127

    Article  CAS  Google Scholar 

  • Chen J, X-F W, Zhang YZ (2006) Expression, purification and characterization of human GM-CSF using silkworm pupae (Bombyx morie) as a bioreactor. J Biotechnol 123:236–247

    Article  CAS  PubMed  Google Scholar 

  • Cheng Y, Wang X-Y, Hao H, Killiny N, Jia-Ping X (2014) A hypothetical model of crossing Bombyx mori nucleopolyhedrovirus through Its host midgut physical barrier. PLoS One 9(12):e115032

    Article  PubMed  PubMed Central  Google Scholar 

  • Choi YS, Lee KS, Yoon HJ, Kim I, Sohn HD, Jin BR (2006) A bumblebee thioredoxin-like protein gene that is upregulated by a temperature stimulus and lipopolysaccharide injection. Eur J Entomol 103:291–296

    Article  CAS  Google Scholar 

  • Choo YM, Lee KS, Yoon HJ, Lee SB, Kim JH, Sohn HD, Jin BR (2007) A serine protease from the midgut of the bumblebee, Bombus ignitus (hymenoptera: apidae): cDNA cloning, gene structure, expression and enzyme activity. Eur J Entomol 104:1–7

    Article  CAS  Google Scholar 

  • Choo YM, Lee KS, Yoon HJ, Kim BY, Sohn MR, Roh JY, Je YH, Kim NJ, Kim I, Woo SD, Sohn HD, Jin BR (2010) Dual function of a bee venom serine protease: prophenoloxidase-activating factor in arthropods and fibrin(ogen)olytic enzyme in mammals. PLoS One 5(5):1–10

    Article  Google Scholar 

  • Christophides GK, Zdobnov E, Barillas-Mury C, Birney E, Blandin S, Blass C, Brey PT, Collins FH, Danielli A, Dimopoulos G (2002) Immunity-related genes and gene families in Anopheles gambiae. Science 298(5591):159–165

    Article  CAS  PubMed  Google Scholar 

  • Danielli A, Loukeris TG, Lagueux M, Muller HM, Richman A, Kafatos FC (2000) A modular chitin-binding protease associated with hemocytes and hemolymph in the mosquito Anopheles gambiae. Proc Natl Acad Sci U S A 97:7136–7141

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • De Gregorio E, Han SJ, Lee WJ, Baek MJ, Osaki T et al (2002) An immune-responsive Serpin regulates the melanization cascade in Drosophila. Dev Cell 3:581

    Article  PubMed  Google Scholar 

  • Dimopoulos G, Richman A, Mullar HM, Kafatos FC (1997) Molecular immune responses of the mosquito Anopheles gambiae to bacteria and malaria parasites. Proc Natl Acad Sci U S A 94:11508–11513

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Engelhard EK, Volkman LE (1995) Developmental resistance in fourth instar Trichoplusia ni orally inoculated with Autographa californica M nuclear polyhedrosis virus. Virology 209:384–389

    Article  CAS  PubMed  Google Scholar 

  • Feng Fan, Hu Ping and Chen Keping (2013) Progress of antiviral mechanisms in the mulberry silkworm: A review 7(14):1173–1178

    Google Scholar 

  • Felfoldi G, Eleftherianos I, Ffrench-Constant RH, Venekei I (2011) A serine proteinase homolog, SPH-3, plays a central role in insect immunity. J Immunol 186:4828–4834

    Article  PubMed  Google Scholar 

  • Fragkoudis R, Chi Y, Siu RW, Barry G, Attarzadeh-Yazdi G, Merits A, Nash AA, Fazakerley JK, Kohl A (2008) Semliki forest virus strongly reduces mosquito host defense signaling. Insect Mol Biol 17:647–656

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Fragkoudis R, Attarzadeh-Yazdi G, Nash AA, Fazakerley JK, Alain Kohl A (2009) Advances in dissecting mosquito innate immune responses to arbovirus infection. J Gen Virol 90:2061–2072

    Article  CAS  PubMed  Google Scholar 

  • Gabay JE (1994) Antimicrobial proteins with homology to serine protease. Ciba Found Symp 186:237–247

    CAS  PubMed  Google Scholar 

  • Gabay JE, Almeid RP (1993) Antibiotic peptides and serine protease homologs in human polymorphonuclear leukocytes: defensins and azurocidin. Curr Opin Immunol 5:97–102

    Article  CAS  PubMed  Google Scholar 

  • Gettins PG (2002) Serpin structure, mechanism, and function. Chem Rev 102:4751

    Article  CAS  PubMed  Google Scholar 

  • Gorman MJ, Paskewitz SM (2001) Serine proteases as mediators of mosquito immune responses. Insect Mol Biol 31:257–262

    Article  CAS  Google Scholar 

  • Gorman MJ, Andreeva OV, Paskewitz SM (2000a) Sp22D: a multidomain serine protease with a putative role in insect immunity. Gene 251:9–17

    Article  CAS  PubMed  Google Scholar 

  • Gorman MJ, Olga V, Andreeva OV, Susan M, Paskewitz SM (2000b) Molecular characterization of five serine protease genes cloned from Anopheles gambiae hemolymph. Insect Biochem Mol Biol 30:35–46

    Article  CAS  PubMed  Google Scholar 

  • Hartley BS (1960) Proteolytic enzymes. Annu Rev Biochem 29:45–72

    Article  CAS  PubMed  Google Scholar 

  • He WY, Zheng YP, Tang L, Zheng SC, Beliveau C, Doucet D, Cusson M, Feng QL (2009) Cloning, expression and localization of a trypsin-like serine protease in the spruce budworm, Choristoneura fumiferana. Insect Sci 16:455–464

    Article  CAS  Google Scholar 

  • Hedstrom L (2002) Serine protease mechanism and specificity. Chem Rev 102:4501–4524

    Article  CAS  PubMed  Google Scholar 

  • Herrero S, Combes E, Oers V, Vlak MM, DeMaagd RA, Beekwilder J (2005) Identification and recombinant expression of a novel chymotrypsin from Spodoptera exigua. Insect Biochem Mol Biol 35:1073–1082

    Article  CAS  PubMed  Google Scholar 

  • Holt RA, Subramanian GM, Halpern A, Sutton GG, Charlab R, Nusskern DR, Wincker P, Clark AG, Ribeiro JM, authors o (2002) The genome sequence of the malaria mosquito Anopheles gambiae. Science 298:129–149

    Article  CAS  PubMed  Google Scholar 

  • Hu Y, YX X, WY L, Yuan ZY, Quan H, Shen YJ et al (2014) De novo assembly and transcriptome characterization: novel insights into the natural resistance mechanisms of Microtus fortis against Schistosoma japonicum. BMC Genomics 15(1):1–13

    Article  Google Scholar 

  • Huang HS, Wang H, Lee SY, Johansson WM, Soderhall K, Cerenius L (2000) A cell adhesion protein from the crayfish Pacifastacus leniusculus, a serine protease homologue similar to drosophila masquerade. J Biol Chem 275:9996–10001

    Article  CAS  PubMed  Google Scholar 

  • Iwanaga S (2002) The molecular basis of innate immunity in the horseshoe crab. Curr Opin Immunol 14:87–95

    Article  CAS  PubMed  Google Scholar 

  • Jiang R, Kim EH, Gong JH, Kwon HM, Kim CH et al (2009) Three pairs of protease-serpin complexes cooperatively regulate the insect innate immune responses. J Biol Chem 284:35652

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jupatanakul N, Shuzhen Sim S, Angleroa-Rodroaguez YI, Souza-Neto J, Das S, Poti KE, Rossi SL, Bergren N, Vasilakis N, Dimopoulos G (2017) Engineered Aedes aegypti JAK/STAT pathway-mediated immunity to dengue virus. PLoS Negl Trop Dis 1:24

    Google Scholar 

  • Kaji K, Tomino S, Asano T (2009) A serine protease in the midgut of the silkworm, Bombyx mori: protein sequencing, identification of cDNA, demonstration of its synthesis as zymogen form and activation during midgut remodeling. Insect Biochem Mol Biol 39:207–217

    Article  CAS  PubMed  Google Scholar 

  • Kanost MR, Gorman MJ (2008) Phenoloxidases in insect immunity. In: Beckage NE (ed) Insect immunology. Elsevier/Academic, Manhattan, pp 69–96

    Chapter  Google Scholar 

  • Katsuma S, Daimon T, Horie S, Kobayashi M, Shimada T (2006) N-linked glycans of Bombyx mori nucleopolyhedrovirus fibroblast growth factor are crucial for its secretion. Biochem Biophys Res Commun 350(4):1069–1075

    Article  CAS  PubMed  Google Scholar 

  • Kim CH, Kim SJ, Kan H, Kwon HM, Roh KB et al (2008) A three-step proteolytic cascade mediates the activation of the peptidoglycan-induced toll pathway in an insect. J Biol Chem 283:7599–7607

    Article  CAS  PubMed  Google Scholar 

  • Kim SY, Jeong EJ, Song J, Park KS (2009) Molecular cloning and characterization of a serine protease-like protein from silkworm (Bombyx Morie). Gene Genom 31(5):387–395

    Article  CAS  Google Scholar 

  • Kotani E, Niwa T, Tokizane M, Suga K, Sugimura Y, Oda K, Mori M, Furusawa T, (1999) Cloning and sequence of a cDNA for a highly basic protease from the digestive juice of the silkworm, Bombyx mori. Insect Mol. Biol. 8:299–304

    Google Scholar 

  • Kwon TH, Kim MS, Choi HW, Joo CH, Cho MY, Lee BL (2000) A masquerade-like serine protease homologue necessary for phenoloxidase activity in the coleopteran insect Holotrichia diomphalia larvae. Eur J Biochem 267:6188–6196

    Article  CAS  PubMed  Google Scholar 

  • Lavine MD, Strand MR (2002). Insect hemocytes and their role in immunity. Insect Biochem. Mol. Biol. 32(10):1295–1309

    Google Scholar 

  • Lehane MJ, Aksoy S, Levashina E (2004) Immune responses and parasite transmission in blood-feeding insects. Trends Parasitol 20(9):433–439

    Article  CAS  PubMed  Google Scholar 

  • Lemaitre B, Hoffmann J (2007) The host defense of Drosophila melanogaster. Annu Rev Immunol 25:697–743

    Article  CAS  PubMed  Google Scholar 

  • Lin H, Lin X, Zhu J, XO Y, Xia X, Yao F, Guang Yang G, You M (2017) Characterization and expression profiling of serine protease inhibitors in the diamondback moth, Plutella xylostella (Lepidoptera: Plutellidae). BMC Genomics 18:162

    Article  PubMed  PubMed Central  Google Scholar 

  • Lindsay S, Wasserman SA (2014) Conventional and non-conventional Drosophila Toll signaling. Dev Comp Immunol 42(1):10.10–10.16

    Article  Google Scholar 

  • Liu HW, Li YS, Tang X, Guo PC, Wang DD, Chun-Yan Zhou CY, Xia QY, Zhao P (2016) A midgut-specific serine protease, BmSP36, is involved in dietary protein digestion in the silkworm, Bombyx mori. Insect Sci:1–15. https://doi.org/10.1111/1744-7917.12369

  • Liu Y, Sui YP, Wang JX, Zhao XF (2009) Characterization of the trypsin-like protease (Ha-TLP2) constitutively expressed in the integument of the cotton bollworm, Helicoverpa armigera. Arch Insect Biochem Physiol 72:74–87

    Article  CAS  PubMed  Google Scholar 

  • Ma S, Kang Z, Lü P, Yang Y, Yao Q, Xia H, Chen K (2015) Molecular and physiological characterization of two novel multirepeat β-thymosins from silkworm, Bombyx mori. PLoS One 10(10):e0140182

    Article  PubMed  PubMed Central  Google Scholar 

  • Miao XX, SJ X, Li MH, Li MW, Huang JH, Dai FY, Marino SW, Mills DR, Zeng PY, Mita K, Jia H, Zhang Y, Liu WB, Xiang H, Guo QH, AY X, Kong XY, Lin HX, Shi YZ, Lu G, Zhang XL, Huang W, Yasukochi Y, Sugasaki T, Shimada T, Nagaraju J, Xiang ZH, Wang SY, Goldsmith MR, Lu C, Zhao GP, Huang YP (2005) Simple sequence repeat-based consensus linkage map of Bombyx mori. Proc Natl Acad Sci U S A 102:16303–16308

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Monsma SA, Oomens AG, Blissard GW (1996) The GP64 envelope fusion protein is an essential baculovirus protein required for cell-to-cell transmission of infection. J Virol 70(7):4607–4616

    CAS  PubMed  PubMed Central  Google Scholar 

  • Morisato D (1995) Signaling pathways that establish the dorsal-ventral pattern of the Drosophila embryo. Annu Rev Genet 29:371–399

    CAS  PubMed  Google Scholar 

  • Murugasu-Oei B, Rodrigues V, Yang X, Chia W (1995) Masquerade: a novel secreted serine protease-like molecule is required for somatic muscle attachment in the drosophila embryo. Genes Dev 9:139–154

    Article  CAS  PubMed  Google Scholar 

  • Nakamura T, Nishizawa T, Hagiya M, Seki T, Shionishi M, Sugiura A, Tashiro K, Shiizu S (1989) Molecular cloning and expression of human hepatocyte growth factor. Nature 342:440–443

    Article  CAS  PubMed  Google Scholar 

  • Nakazawa H, Tsuneishi E, Ponnuvel KM, Furukawa S, Asaoka A, Tanaka H, Ishibashi J, Yamakawa M (2004) Antiviral activity of a serine protease from the digestive juice of Bombyx mori larvae against nucleopolyhedrovirus. Virology 321(1):154–162

    Article  CAS  PubMed  Google Scholar 

  • Nappi A, Poirie M, Carton Y (2009) The role of melanization and cytotoxic byproducts in the cellular immune responses of drosophila against parasitic wasps. Adv Parasitol 70:99–121

    Article  CAS  PubMed  Google Scholar 

  • Perona JJ, Craik CS (1995) Structural basis of substrate specificity in the serine proteases. Protein Sci 4(3):337–360

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Polgar L (2005) The catalytic triad of serine peptidases CMLS. Cell Mol Life Sci 62:2161–2172

    Article  CAS  PubMed  Google Scholar 

  • Ponnuvel KM, Nakazawa H, Furukawa S, Asaoka A, Ishibashi J, Tanaka H, Yamakawa M (2003) A lipase isolated from the silkworm Bombyx mori shows antiviral activity against nucleopolyhedrovirus. J Virol 77(19):10725–10729

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ponnuvel KM, Koundinya PR, Sinha RK, Kamble CK (2008) Mechanism of viral resistance in mulberry silkworm, Bombyx mori L. Indian J Seric 47(1):1–6

    Google Scholar 

  • Ponnuvel KM, Nithya K, Sirigineedi S, Awasthi AK, Yamakawa M (2012) In vitro antiviral activity of an alkaline trypsin from the digestive juice of Bombyx mori larvae against nucleopolyhedrovirus. Arch Insect Biochem 81(2):90–104

    Article  CAS  Google Scholar 

  • Popham HJ, Shelby KS, Brandt SL, Coudron TA (2004) Potent virucidal activity in larval Heliothis virescens plasma against Helicoverpa zea single capsid nucleopolyhedrovirus. J Gen Virol 85(8):2255–2261

    Article  CAS  PubMed  Google Scholar 

  • Qin L, Xia H, Shi H, Zhou Y, Chen L, Yao Q, Liu X, Feng F, Yuan Y, Chen K (2012) Comparative proteomic analysis reveals that caspase-1 and serine protease may be involved in silkworm resistance to Bombyx mori nuclear polyhedrosis virus. J Proteome 75:3630–3638

    Article  CAS  Google Scholar 

  • Rahman MM, Gopinathan KP (2004) Systemic and in vitro infection process of Bombyx mori nucleopolyhedrovirus. Virus Res 101:109–118

    Article  CAS  PubMed  Google Scholar 

  • Randall RE, Goodbourn S (2008) Interferons and viruses: interplay between induction, signaling, antiviral responses and virus countermeasures. J Gen Virol 89:1–47

    Article  CAS  PubMed  Google Scholar 

  • Rao MB, Tanksale AM, Ghatge MS, Deshpande VV (1998) Molecular and biotechnological aspects of microbial protease. Microbial Mol Biol Rev 62:597–615

    CAS  Google Scholar 

  • Rawlings ND, Barrett AJ (2000) MEROPS: the peptidase database. Nucleic Acids Res 28:323–325

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Richman AM, Bulet P, Hetru C, Barillas-Mury C, Hoffmann JA et al (1996) Inducible immune factors of the vector mosquito Anopheles gambiae: biochemical purification of a defensin antibacterial peptide and molecular cloning of preprodefensin cDNA. Insect Mol Biol 5:203–210

    Article  CAS  PubMed  Google Scholar 

  • Riddell CE, Garces JDL, Adams S, Barribeau SM, David Twell D, Eamonn B, Mallon EB (2014) Differential gene expression and alternative splicing in insect immune specificity. BMC Genomics 15(1):1031

    Article  PubMed  PubMed Central  Google Scholar 

  • Romualdi C, Bortoluzzi S, DAlessi F, Danieli GA (2003) IDEG6: a web tool for detection of differentially expressed genes in multiple tag sampling experiments. Physiol Genomics 12(2):159–162

    Article  CAS  PubMed  Google Scholar 

  • Ross J, Jiang H, Kanost MR, Wang Y (2003) Serine proteases and their homologs in the Drosophila melanogaster genome: an initial analysis of sequence conservation and phylogenetic relationships. Gene 304:117–131

    Article  CAS  PubMed  Google Scholar 

  • Saleem M, Rehman A, Yasmin R, Munir B (2012) Biochemical analysis and investigation on the prospective applications of alkaline protease from a Bacillus cereus strain. Mol Biol Rep 39(6):6399–6408

    Article  CAS  PubMed  Google Scholar 

  • Soares TS, Watanabe RM, Lemos FJ, Tanaka AS (2011) Molecular characterization of genes encoding trypsin-like enzymes from Aedes aegypti larvae and identification of digestive enzymes. Gene 489:70–75

    Article  CAS  PubMed  Google Scholar 

  • Souza-Neto JA, Sim S, Dimopoulos G (2009) An evolutionary conserved function of the JAK-STAT pathway in anti-dengue defense. Proc Natl Acad Sci U S A 106:17841–17846

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tanaka H, Ishibashi J, Fujita K, Nakajima Y, Sagisaka A, Tomimoto K, Suzuki N, Yoshiyama M, Kaneko Y, Iwasaki T (2008) A genome-wide analysis of genes and gene families involved in innate immunity of Bombyx mori. Insect Biochem Mol Biol 38(12):1087–1110

    Article  CAS  PubMed  Google Scholar 

  • Verma J, Modi DR, Sharma R, Saxena S (2011) Vital role of alkaline protease in bio-industries: a review. Plant Archives 11(2):1083–1092

    Google Scholar 

  • Wang H, Blair CD, Olson KE, Clem RJ (2008) Effects of inducing or inhibiting apoptosis on Sindbis virus replication in mosquito cells. J Gen Virol 89:2651–2661

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wang XY, HZ Y, Geng L, JP X, Yu D, Zhang SZ, Ma Y, Dong-Qiong Fei DQ (2016) Comparative transcriptome analysis of Bombyx mori (Lepidoptera) larval midgut response to BmNPV in susceptible and near-isogenic resistant strains. PLoS One 11(5):1–22

    Google Scholar 

  • Wang Y, Wang F, Riyuan Wang R, Zhao P, Xia Q (2017) 2A self-cleaving peptide-based multi-gene expression system in the silkworm Bombyx mori. Sci Rep 5:16273

    Article  Google Scholar 

  • Wei Z, Yin YP, Zhang B, Wang ZK, Peng GX, Cao YQ, Xia YX (2007) Cloning of a novel protease required for the molting of Locusta migratoria manilensis. Develop Growth Differ 49:611–621

    Article  CAS  Google Scholar 

  • Xia Q, Zhou Z, Lu C, Cheng D, Dai F, Li B, Zhao P, Zha X, Cheng T, Chai C (2004) A draft sequence for the genome of the domesticated silkworm (Bombyx mori). Science 306(5703):1937–1940

    Article  PubMed  Google Scholar 

  • Xia Q, Cheng D, Duan J, Wang G, Cheng T, Zha X, Liu C, Zhao P, Dai F, Zhang Z (2007) Microarray-based gene expression profiles in multiple tissues of the domesticated silkworm, Bombyx mori. Genome Biol 8(8):R162

    Article  PubMed  PubMed Central  Google Scholar 

  • Xia Q, Guo Y, Zhang Z, Li D, Xuan Z, Li Z (2009) Complete resequencing of 40 genomes reveals domestication events and genes in silkworm (Bombyx morie). Science 326:433–436

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Xia X, Liying Yu l, Xue M, Yu X, Vasseur L, Gurr GM, Baxter SW, Lin H, Lin J, You M (2015) Genome-wide characterization and expression profiling of immune genes in the diamondback moth, Plutella xylostella (L.) Sci Rep 5:1–13

    CAS  Google Scholar 

  • Xu QY, Lu AR, Xiao GH, Yang B, Zhang J, Li XQ, Guan JM, Shao QM, Beerntsen BT, Zhang P, Wang CS, Ling EJ (2012) Transcriptional profiling of midgut immunity response and degeneration in the wandering silkworm, Bombyx mori. PLoS One 7:43769

    Article  Google Scholar 

  • You M et al (2013) A heterozygous moth genome provides insights into herbivory and detoxification. Nat Genet 45:220–225

    Article  CAS  PubMed  Google Scholar 

  • Zdobnov EM, Von Mering C, Letunic I, Torrents D, Suyama M, Copley RR, Christophides GK, Thomasova D, Holt RA, Subramanian GM, Mueller HM, Dimopoulos G, Law JH, Wells MA, Birney E, Charlab R, Halpern AL, Kokoza E, Kraft CL, Lai Z, Lewis S, Louis C, Barillas-Mury C, Nusskern D, Rubin GM, Salzberg SL, Sutton GG, Topalis P, Wides R, Wincker P, Yandell M, Collins FH, Ribeiro J, Gelbart WM, Kafatos FC, Bork P (2002) Comparative genome and proteome analysis of Anopheles gambiae and Drosophila melanogaster. Science 298:149–159

    Article  CAS  PubMed  Google Scholar 

  • Zhao P, Wang GH, Dong ZM, Duan J, PZ X, Cheng TC, Xiang ZH, Xia QY (2010) Genome-wide identification and expression analysis of serine proteases and homologs in the silkworm Bombyx mori. BMC Genomics 11:405

    Article  PubMed  PubMed Central  Google Scholar 

  • Zhao P, Dong ZM, Duan J, Wang GH, Wang LY, Li YS, Xiang ZH, Xia QY (2012) Genome-wide identification and immune response analysis of serine protease inhibitor genes in the silkworm, Bombyx mori. PLoS One 7(2):e31168

    Google Scholar 

  • Zou Z, Lopez DL, Kanost MR, Evans JD, Jiang H (2006) Comparative analysis of serine protease-related genes in the honey bee genome: possible involvement in embryonic development and innate immunity. Insect Mol Biol 15(5):603–614

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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Verma, J. (2018). Antiviral Mechanism of Serine Protease in Various Insects. In: Kumar, D., Gong, C. (eds) Trends in Insect Molecular Biology and Biotechnology. Springer, Cham. https://doi.org/10.1007/978-3-319-61343-7_8

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