Lepidopteran insects: emerging model organisms to study infection by enteropathogens.

Shruti Ahlawat, Krishna Kant Sharma
Author Information
  1. Shruti Ahlawat: Department of Microbiology, Faculty of Allied Health Sciences, SGT University, Gurgaon-Badli Road Chandu, Budhera, Gurugram, 122505, Haryana, India. shrutiahlawat5@gmail.com. ORCID
  2. Krishna Kant Sharma: Laboratory of Enzymology and Recombinant DNA Technology, Department of Microbiology, Maharshi Dayanand University, Rohtak, 124001, Haryana, India.

Abstract

The in vivo analysis of a pathogen is a critical step in gaining greater knowledge of pathogen biology and host-pathogen interactions. In the last two decades, there has been a notable rise in the number of studies on developing insects as a model for studying pathogens, which provides various benefits, such as ethical acceptability, relatively short life cycle, and cost-effective care and maintenance relative to routinely used rodent infection models. Furthermore, lepidopteran insects provide many advantages, such as easy handling and tissue extraction due to their large size relative to other invertebrate models, like Caenorhabditis elegans. Additionally, insects have an innate immune system that is highly analogous to vertebrates. In the present review, we discuss the components of the insect's larval immune system, which strengthens its usage as an alternative host, and present an updated overview of the research findings involving lepidopteran insects (Galleria mellonella, Manduca sexta, Bombyx mori, and Helicoverpa armigera) as infection models to study the virulence by enteropathogens due to the homology between insect and vertebrate gut.

Keywords

References

  1. Abbasifar R, Kropinski AM, Sabour PM, Chambers JR, MacKinnon J, Malig T et al (2014) Efficiency of bacteriophage therapy against Cronobacter sakazakii in Galleria mellonella (greater wax moth) larvae. Arch Virol 159:2253–2261 [PMID: 24705602]
  2. Ahlawat S, Singh AK, Shankar A, Yadav A, Sharma KK (2021) Infected insect gut reveals differentially expressed proteins for cellular redox, metal resistance and secretion system in Yersinia enterocolitica-Helicoverpa armigera pathogenic model. Biotechnol Lett 43:1845–1867 [PMID: 34165641]
  3. Ahlawat S, Singh D, Yadav A, Singh AK, Virdi JS, Sharma KK (2020) Proteomic analysis reveals the damaging role of low redox laccase from Yersinia enterocolitica strain 8081 in the midgut of Helicoverpa armigera. Biotechnol Lett 42:2189–2210 [PMID: 32472187]
  4. Alenizi D, Ringwood T, Redhwan A, Bouraha B, Wren BW, Prentice M et al (2016) All Yersinia enterocolitica are pathogenic: virulence of phylogroup 1 Y. enterocolitica in a Galleria mellonella infection model. Microbiol 162:1379–1387 [DOI: 10.1099/mic.0.000311]
  5. Ali Mohammadie Kojour M, Han YS, Jo YH (2020) An overview of insect innate immunity. Entomol Res 50:282–291 [DOI: 10.1111/1748-5967.12437]
  6. Allonsius CN, Van Beeck W, De Boeck I, Wittouck S, Lebeer S (2019) The microbiome of the invertebrate model host Galleria mellonella is dominated by Enterococcus. Anim Microbiome 1:1–7 [DOI: 10.1186/s42523-019-0010-6]
  7. Anand AAM, Vennison SH, Sankar SG, Prabhu DIG, Vasan PT, Raghuraman T et al (2010) Isolation and characterization of bacteria from the gut of Bombyx mori that degrade cellulose, xylan, pectin and starch and their impact on digestion. J Insect Sci 10:1–20 [DOI: 10.1673/031.010.10701]
  8. Ao JQ, Ling E, Yu XQ (2008) A Toll receptor from Manduca sexta is in response to Escherichia coli infection. Mol Immunol 45:543–552 [PMID: 17606296]
  9. Barnoy S, Gancz H, Zhu Y, Honnold CL, Zurawski DV, Venkatesan MM (2017) The Galleria mellonella larvae as an in vivo model for evaluation of Shigella virulence. Gut Microbes 8:335–350 [PMID: 28277944]
  10. Barrionuevo JMR, Vilanova-Cuevas B, Alvarez A, Martín E, Malizia A, Galindo-Cardona A et al (2022) The Bacterial and Fungal Gut Microbiota of the Greater Wax Moth, Galleria mellonella L. Consuming Polyethylene and Polystyrene Front Microbiol 13:918861 [DOI: 10.3389/fmicb.2022.918861]
  11. Bender JK, Wille T, Blank K, Lange A, Gerlach RG (2013) LPS structure and PhoQ activity are important for Salmonella Typhimurium virulence in the Gallleria mellonella infection model. PLoS ONE 8:e73287 [PMID: 23951347]
  12. Bergin D, Reeves EP, Renwick J, Wientjes FB, Kavanagh K (2005) Superoxide production in Galleria mellonella hemocytes: identification of proteins homologous to the NADPH oxidase complex of human neutrophils. Infect Immun 73:4161–4170 [PMID: 15972506]
  13. Bresolin G, Morgan JAW, Ilgen D, Scherer S, Fuchs TM (2006) Low temperature-induced insecticidal activity of Yersinia enterocolitica. Mol Microbial 59:503–512 [DOI: 10.1111/j.1365-2958.2005.04916.x]
  14. Browne N, Heelan M, Kavanagh K (2013) An analysis of the structural and functional similarities of insect hemocytes and mammalian phagocytes. Virulence 4:597–603 [PMID: 23921374]
  15. Büyükgüzel E, Tunaz H, Stanley D, Büyükgüzel K (2007) Eicosanoids mediate Galleria mellonella cellular immune response to viral infection. J Insect Physiol 53:99–105 [PMID: 17161422]
  16. Campbell PM, Cao AT, Hines ER, East PD, Gordon KH (2008) Proteomic analysis of the peritrophic matrix from the gut of the caterpillar, Helicoverpa armigera. Insect Biochem Mol Biol 38:950–958 [PMID: 18760362]
  17. Card R, Vaughan K, Bagnall M, Spiropoulos J, Cooley W, Strickland T et al (2016) Virulence characterisation of Salmonella enterica isolates of differing antimicrobial resistance recovered from UK livestock and imported meat samples. Front Microbial 7:640
  18. Champion OL, Cooper IA, James SL, Ford D, Karlyshev A, Wren BW et al (2009) Galleria mellonella as an alternative infection model for Yersinia pseudotuberculosis. Microbiol 155:1516–1522 [DOI: 10.1099/mic.0.026823-0]
  19. Champion OL, Karlyshev AV, Senior NJ, Woodward M, La Ragione R, Howard SL et al (2010) Insect infection model for Campylobacter jejuni reveals that O-methyl phosphoramidate has insecticidal activity. J Infect Dis 201:776–782 [PMID: 20113177]
  20. Chen RY, Keddie BA (2021) The Galleria mellonella-enteropathogenic Escherichia coli model system: characterization of pathogen virulence and insect immune responses. J Insect Sci 21:7 [PMID: 34314494]
  21. Cheng T, Lin P, Huang L, Wu Y, Jin S, Liu C et al (2016) Genome-wide analysis of host responses to four different types of microorganisms in Bombyx mori (Lepidoptera: Bombycidae). J Insect Sci 16:1–11 [DOI: 10.1093/jisesa/iew020]
  22. Clavel T, Lagkouvardos I, Blaut M, Stecher B (2016) The mouse gut microbiome revisited: from complex diversity to model ecosystems. Int J Med Microbiol 306:316–327 [PMID: 26995267]
  23. Coates CJ, Lim J, Harman K, Rowley AF, Griffiths DJ, Emery H et al (2019) The insect, Galleria mellonella, is a compatible model for evaluating the toxicology of okadaic acid. Cell Biol Toxicol 35:219–232 [PMID: 30426330]
  24. Consentino L, Rejasse A, Crapart N, Bevilacqua C, Nielsen-LeRoux C (2021) Laser capture microdissection to study Bacillus cereus iron homeostasis gene expression during Galleria mellonella in vivo gut colonization. Virulence 12:2104–2121 [PMID: 34374318]
  25. Cook SM, McArthur JD (2013) Developing Galleria mellonella as a model host for human pathogens. Virulence 4:350–353 [PMID: 23799664]
  26. de Freitas LL, da Silva FP, Fernandes KM, Carneiro DG, de Oliveira LL, Martins GF et al (2021) The virulence of Salmonella Enteritidis in Galleria mellonella is improved by N-dodecanoyl-homoserine lactone. Microb Pathog 152:104730 [DOI: 10.1016/j.micpath.2021.104730]
  27. De la Cruz MA, Morgan JK, Ares MA, Yáñez-Santos JA, Riordan JT, Girón JA (2016) The two-component system CpxRA negatively regulates the locus of enterocyte effacement of enterohemorrhagic Escherichia coli involving σ32 and Lon protease. Front Cell Infect Microbiol 6:11 [PMID: 26904510]
  28. Dubovskiy IM, Grizanova EV, Whitten MM, Mukherjee K, Greig C, Alikina T et al (2016) Immuno-physiological adaptations confer wax moth Galleria mellonella resistance to Bacillus thuringiensis. Virulence 7:860–870 [PMID: 27029421]
  29. Dubovskiy IM, Whitten MMA, Kryukov VY, Yaroslavtseva ON, Grizanova EV, Greig C et al (2013) More than a colour change: insect melanism, disease resistance and fecundity. Proc R Soc b: Biol Sci 280:20130584 [DOI: 10.1098/rspb.2013.0584]
  30. Emery H, Butt TM, Coates CJ (2021a) Nutraceutical intervention protects against bacterial and chemical-induced gastrotoxicity in a non-mammalian model Galleria Mellonella. Food Chem Toxicol 154:112354 [PMID: 34146620]
  31. Emery H, Johnston R, Rowley AF, Coates CJ (2019) Indomethacin-induced gut damage in a surrogate insect model, Galleria mellonella. Arch Toxicol 93:2347–2360 [PMID: 31270586]
  32. Emery H, Traves W, Rowley AF, Coates CJ (2021b) The diarrhetic shellfish-poisoning toxin, okadaic acid, provokes gastropathy, dysbiosis and susceptibility to bacterial infection in a non-rodent bioassay, Galleria mellonella. Arch Toxicol 95:3361–3376 [PMID: 34374792]
  33. Emery O, Schmidt K, Engel P (2017) Immune system stimulation by the gut symbiont Frischella perrara in the honey bee (Apis mellifera). Mol Ecol. https://doi.org/10.1111/mec.14058 [DOI: 10.1111/mec.14058]
  34. Erickson DL, Russell CW, Johnson KL, Hileman T, Stewart RM (2011) PhoP and OxyR transcriptional regulators contribute to Yersinia pestis virulence and survival within Galleria mellonella. Microb Pathog 51:389–395 [PMID: 21964409]
  35. Feng M, Xia J, Fei S, Peng R, Wang X, Zhou Y et al (2021) Identification of silkworm hemocyte subsets and analysis of their response to baculovirus infection based on single-cell RNA sequencing. Front Immunol 12:1521 [DOI: 10.3389/fimmu.2021.645359]
  36. Freitak D, Schmidtberg H, Dickel F, Lochnit G, Vogel H, Vilcinskas A (2014) The maternal transfer of bacteria can mediate trans-generational immune priming in insects. Virulence 5:547–554 [PMID: 24603099]
  37. Fuchs TM, Bresolin G, Marcinowski L, Schachtner J, Scherer S (2008) Insecticidal genes of Yersinia spp.: taxonomical distribution, contribution to toxicity towards Manduca sexta and Galleria mellonella, and evolution. BMC Microbial 8:1–11
  38. Grizanova EV, Coates CJ, Dubovskiy IM, Butt TM (2019) Metarhizium brunneum infection dynamics differ at the cuticle interface of susceptible and tolerant morphs of Galleria mellonella. Virulence 10:999–1012 [PMID: 31724467]
  39. Guerrieri CG, Pereira MF, Galdino ACM, Santos ALSD, Elias WP, Schuenck RP et al (2019) Typical and atypical enteroaggregative Escherichia coli are both virulent in the Galleria mellonella model. Front Microbiol 10:1791 [PMID: 31456762]
  40. He C, Nan X, Zhang Z, Li M (2013) Composition and diversity analysis of the gut bacterial community of the oriental armyworm, Mythimna separata, determined by culture-independent and culture-dependent techniques. J Insect Sci 13:165 [PMID: 24773514]
  41. Holden B (2015) Charles W. The remarkable life of UC’s first entomologist. Brian Holden Publishing, Woodworth
  42. Hugenholtz F, de Vos WM (2018) Mouse models for human intestinal microbiota research: a critical evaluation. Cell Mol Life Sci 75:149–160 [PMID: 29124307]
  43. Ignasiak K, Maxwell A (2018) Oxytetracycline reduces the diversity of tetracycline-resistance genes in the Galleria mellonella gut microbiome. BMC Microbiol 18:1–8 [DOI: 10.1186/s12866-018-1377-3]
  44. Insua JL, Llobet E, Moranta D, Pérez-Gutiérrez C, Tomás A, Garmendia J, Bengoechea JA (2013) Modeling Klebsiella pneumoniae pathogenesis by infection of the wax moth Galleria mellonella. Infect Immun 81:3552–3565 [PMID: 23836821]
  45. Jønsson R, Struve C, Jenssen H, Krogfelt KA (2017) The wax moth Galleria mellonella as a novel model system to study enteroaggregative Escherichia coli pathogenesis. Virulence 8:1894–1899 [PMID: 27824518]
  46. Joseph W (2014) Origins and activation of prophenoloxidases in the digestive tract of the cricket, Gryllus bimaculatus. Arch Insect Biochem Physiol 87:95–104 [PMID: 25042687]
  47. Junqueira JC, Mylonakis E, Borghi E (2021) Galleria mellonella experimental model: advances and future directions. Pathog Dis 79:ftab021
  48. Kaito C, Akimitsu N, Watanabe H, Sekimizu K (2002) Silkworm larvae as an animal model of bacterial infection pathogenic to humans. Microb Pathog 32:183–190 [PMID: 12079408]
  49. Kang E, Crouse A, Chevallier L, Pontier SM, Alzahrani A, Silué N, Campbell-Valois F, Montagutelli X, Gruenheid S, Malo D (2018) Enterobacteria and host resistance to infection. Mamm Genome 29:558–576 [PMID: 29785663]
  50. Kemp MW, Massey RC (2007) The use of insect models to study human pathogens. Drug Discov Today Dis Models 4:105–110 [DOI: 10.1016/j.ddmod.2007.06.007]
  51. Krachler AM, Sirisaengtaksin N, Monteith P, Timothy Paine CE, Coates CJ, Lim J (2021) Defective phagocyte association during infection of Galleria mellonella with Yersinia pseudotuberculosis is detrimental to both insect host and microbe. Virulence 12:638–653 [PMID: 33550901]
  52. Krishnan M, Bharathiraja C, Pandiarajan J, Prasanna VA, Rajendhran J, Gunasekaran P (2014) Insect gut microbiome–an unexploited reserve for biotechnological application. Asian Pac J Trop Biomed 4:S16–S21 [PMID: 25183073]
  53. Kurstak E, Vega CE (1968) Infection bactérienne à Salmonella typhimurium chez un invertébré, Galleria mellonella L. Can J Microbiol 14:233–237 [PMID: 4871974]
  54. Lange A, Schäfer A, Bender A, Steimle A, Beier S, Parusel R et al (2018) Galleria mellonella: a novel invertebrate model to distinguish intestinal symbionts from pathobionts. Front Immunol 9:2114 [PMID: 30283451]
  55. Leuko S, Raivio TL (2012) Mutations that impact the enteropathogenic Escherichia coli Cpx envelope stress response attenuate virulence in Galleria mellonella. Infect Immun 80:3077–3085 [PMID: 22710873]
  56. Liang X, Fu Y, Tong L, Liu H (2014) Microbial shifts of the silkworm larval gut in response to lettuce leaf feeding. Appl Microbiol Biotechnol 98:3769–3776 [PMID: 24493569]
  57. Liu W, Liu J, Lu Y, Gong Y, Zhu M, Chen F et al (2015) Immune signaling pathways activated in response to different pathogenic micro-organisms in Bombyx mori. Mol Immunol 65:391–397 [PMID: 25745806]
  58. Lou Y, Ekaterina P, Yang SS, Lu B, Liu B, Ren N et al (2020) Biodegradation of polyethylene and polystyrene by greater wax moth larvae (Galleria mellonella L.) and the effect of co-diet supplementation on the core gut microbiome. Environ Sci Technol 54:2821–2831 [PMID: 32013402]
  59. Marzban R, He Q, Zhang Q, Liu XX (2013) Histopathology of cotton bollworm midgut infected with Helicoverpa armigera cytoplasmic polyhedrosis virus. Braz J Microbiol 44:1231–1236 [PMID: 24688516]
  60. Meng X, Zhu F, Chen K (2017) Silkworm: a promising model organism in life science. J Insect Sci 17:97 [PMID: 29117372]
  61. Mil-Homens D, Martins M, Barbosa J, Serafim G, Sarmento MJ, Pires RF et al (2021) Carbapenem-resistant Klebsiella pneumoniae clinical isolates: in vivo virulence assessment in Galleria mellonella and potential therapeutics by polycationic oligoethyleneimine. Antibiotics 10:56 [PMID: 33430101]
  62. Mishra PK, Tandon SM (2003) Gut bacterial flora of Helicoverpa armigera (Hub.) (Lepidoptera: Noctuidae). Indian J Microbiol 43:55–56
  63. Mitsuhashi W, Miyamoto K (2020) Interaction of Bacillus thuringiensis cry toxins and the insect midgut with a focus on the silkworm (Bombyx mori) midgut. Biocontrol Sci Technol 30:68–84 [DOI: 10.1080/09583157.2019.1684439]
  64. Morgan JK, Ortiz JA, Riordan JT (2014) The role for TolA in enterohemorrhagic Escherichia coli pathogenesis and virulence gene transcription. Microb Pathog 201477:42–52 [DOI: 10.1016/j.micpath.2014.10.010]
  65. Morin N, Santiago AE, Ernst RK, Guillot SJ, Nataro JP (2013) Characterization of the AggR regulon in enteroaggregative Escherichia coli. Infect Immun 81:122–132 [PMID: 23090962]
  66. Müller U, Vogel P, Alber G, Schaub GA (2008) The innate immune system of mammals and insects. Trends in Innate Immunity 15:21–44
  67. Murray GL, Attridge SR, Morona R (2005) Inducible serum resistance in Salmonella typhimurium is dependent on wzzfepE-regulated very long O antigen chains. Microbes Infect 7:1296–1304 [PMID: 16027021]
  68. Nguyen TLA, Vieira-Silva S, Liston A, Raes J (2015) How informative is the mouse for human gut microbiota research? Dis Model Mech 8:1–16 [PMID: 25561744]
  69. Ochoa S, Fernández F, Devotto L, France Iglesias A, Collado L (2021) Virulence assessment of enterohepatic Helicobacter species carried by dogs using the wax moth larvae Galleria mellonella as infection model. Helicobacter 26:e12808 [PMID: 33884706]
  70. Pati NB, Doijad SP, Schultze T, Mannala GK, Yao Y, Jaiswal S et al (2018) Enterobacter bugandensis: a novel enterobacterial species associated with severe clinical infection. Sci Rep 8:1–11 [DOI: 10.1038/s41598-018-23069-z]
  71. Pauchet Y, Muck A, Svatoš A, Heckel DG, Preiss S (2008) Mapping the larval midgut lumen proteome of Helicoverpa armigera, a generalist herbivorous insect. J Proteome Res 7:1629–1639 [PMID: 18314941]
  72. Pereira MF, Rossi CC, da Silva GC, Rosa JN, Bazzolli DMS (2020) Galleria mellonella as an infection model: an in-depth look at why it works and practical considerations for successful application. Pathog Dis 78:ftaa056
  73. Piatek M, Sheehan G, Kavanagh K (2020) Utilising Galleria mellonella larvae for studying in vivo activity of conventional and novel antimicrobial agents. Pathog Dis 78:ftaa059
  74. Polenogova OV, Kabilov MR, Tyurin MV, Rotskaya UN, Krivopalov AV, Morozova VV et al (2019) Parasitoid envenomation alters the Galleria mellonella midgut microbiota and immunity, thereby promoting fungal infection. Sci Rep 9:1–12 [DOI: 10.1038/s41598-019-40301-6]
  75. Rajagopal R (2009) Beneficial interactions between insects and gut bacteria. Indian J Microbiol 49:114–119 [PMID: 23100759]
  76. Scalfaro C, Iacobino A, Nardis C, Franciosa G (2017) Galleria mellonella as an in vivo model for assessing the protective activity of probiotics against gastrointestinal bacterial pathogens. FEMS Microbiol Lett 364:fnx064
  77. Scully LR, Bidochka MJ (2006) Developing insect models for the study of current and emerging human pathogens. FEMS Microbiol Lett 263:1–9 [PMID: 16958844]
  78. Senior NJ, Bagnall MC, Champion OL, Reynolds SE, La Ragione RM, Woodward MJ et al (2011) Galleria mellonella as an infection model for Campylobacter jejuni virulence. J Med Microbiol 60:661–669 [PMID: 21233296]
  79. Shao Q, Yang B, Xu Q, Li X, Lu Z, Wang C et al (2012) Hindgut innate immunity and regulation of fecal microbiota through melanization in insects. J Biol Chem 287:14270–14279 [PMID: 22375003]
  80. Shinde AA, Shaikh FK, Gadge PP, Padul MV, Govindwar SP, Kachole MS (2019) Conserved nature of Helicoverpa armigera gut bacterial flora on different host plants and in vitro interactions with PI proteins advocates role in host digestive physiology. J Saudi Soc Agric Sci 18:141–149
  81. Tang X, Freitak D, Vogel H, Ping L, Shao Y, Cordero EA et al (2012) Complexity and variability of gut commensal microbiota in polyphagous lepidopteran larvae. PLoS ONE 7:e36978 [PMID: 22815679]
  82. Tsai CJY, Loh JMS, Proft T (2016) Galleria mellonella infection models for the study of bacterial diseases and for antimicrobial drug testing. Virulence 7:214–229 [PMID: 26730990]
  83. Van Der Hoeven R, Betrabet G, Forst S (2008) Characterization of the gut bacterial community in Manduca sexta and effect of antibiotics on bacterial diversity and nematode reproduction. FEMS Microbiol Lett 286:249–256 [PMID: 18647359]
  84. Vilela FP, Gomes CN, Paziani MH, Braz VS, dos Prazeres RD, Costa RG et al (2020) Virulence traits and expression of bstA, fliC and sopE2 in Salmonella Dublin strains isolated from humans and animals in Brazil. Infect Genet Evol 80:104193 [PMID: 31931258]
  85. Vodovar N, Vinals M, Liehl P, Basset A, Degrouard J, Spellman P et al (2005) Drosophila host defense after oral infection by an entomopathogenic Pseudomonas species. PNAS 102:11414–11419 [PMID: 16061818]
  86. Wagley S, Borne R, Harrison J, Baker-Austin C, Ottaviani D, Leoni F et al (2018) Galleria mellonella as an infection model to investigate virulence of Vibrio parahaemolyticus. Virulence 9:197–207 [PMID: 28960137]
  87. Wand ME, McCowen JW, Nugent PG, Sutton JM (2013) Complex interactions of Klebsiella pneumoniae with the host immune system in a Galleria mellonella infection model. J Med Microbiol 62:1790–1798 [PMID: 24000226]
  88. Wang Q, Liu Y, He HJ et al (2010) Immune responses of Helicoverpa armigera to different kinds of pathogens. BMC Immunol. https://doi.org/10.1186/1471-2172-11-9 [DOI: 10.1186/1471-2172-11-9]
  89. Wang Y, Li DD, Jiang YY, Mylonakis E (2013) Utility of insects for studying human pathogens and evaluating new antimicrobial agents. In: Berlin I (ed) Yellow Biotechnology. Springer, pp 1–25
  90. Whitten MM, Coates CJ (2017) Re-evaluation of insect melanogenesis research: views from the dark side. Pigment Cell Melanoma Res 30:386–401 [PMID: 28378380]
  91. Wu G, Yi Y (2018) Transcriptome analysis of differentially expressed genes involved in innate immunity following Bacillus thuringiensis challenge in Bombyx mori larvae. Mol Immunol 103:220–228 [PMID: 30316186]
  92. Wu K, Yang B, Huang W, Dobens L, Song H, Ling E (2016) Gut immunity in lepidopteran insects. Dev Comp Immunol 64:65–74 [PMID: 26872544]
  93. Wu S, Zhang X, He Y, Shuai J, Chen X, Ling E (2010) Expression of antimicrobial peptide genes in Bombyx mori gut modulated by oral bacterial infection and development. Dev Comp Immunol 34:1191–1198 [PMID: 20600274]
  94. Xiong GH, Xing LS, Lin Z, Saha TT, Wang C, Jiang H et al (2015) High throughput profiling of the cotton bollworm Helicoverpa armigera immunotranscriptome during the fungal and bacterial infections. BMC Genom 16:1–21 [DOI: 10.1186/s12864-015-1509-1]
  95. Yamano Y, Matsumoto M, Inoue K, Kawabata T, Morishima I (1994) Cloning of cDNAs for cecropins A and B, and expression of the genes in the silkworm, Bombyx mori. Biosci Biotechnol Biochem 58:1476–1478 [PMID: 7765280]
  96. Zhang L, Lu Z (2015) Expression, purification and characterization of an atypical 2-Cys peroxiredoxin from the silkworm, Bombyx mori. Insect Mol Biol 24:203–212 [PMID: 25512182]
  97. Zhang S, Xu Y, Fu Q, Jia L, Xiang Z, He N (2011) Proteomic analysis of larval midgut from the silkworm (Bombyx mori). Comp Funct Genomics. https://doi.org/10.1155/2011/876064 [DOI: 10.1155/2011/876064]
  98. Zhang X, Guo W (2011) Isolation and identification of insect intestinal mucin HaIIM86-the new target for Helicoverpa armigera biocontrol. Int J Biol Sci 7:286 [PMID: 21448339]

MeSH Term

Animals
Moths
Manduca
Larva

Word Cloud

Created with Highcharts 10.0.0insectsinfectionmodelspathogenmodelrelativelepidopterandueimmunesystempresenthostGalleriamellonellaManducasextaBombyxmoriHelicoverpaarmigerastudyenteropathogensvivoanalysiscriticalstepgaininggreaterknowledgebiologyhost-pathogeninteractionslasttwodecadesnotablerisenumberstudiesdevelopingstudyingpathogensprovidesvariousbenefitsethicalacceptabilityrelativelyshortlifecyclecost-effectivecaremaintenanceroutinelyusedrodentFurthermoreprovidemanyadvantageseasyhandlingtissueextractionlargesizeinvertebratelikeCaenorhabditiselegansAdditionallyinnatehighlyanalogousvertebratesreviewdiscusscomponentsinsect'slarvalstrengthensusagealternativeupdatedoverviewresearchfindingsinvolvingvirulencehomologyinsectvertebrategutLepidopteraninsects:emergingorganismsAlternativeEnteropathogen

Similar Articles

Cited By