1932
0
  1. Home
  2. A-Z Publications
  3. Annual Review of Virology
  4. Volume 8, 2021
  5. Article

Annual Review of Virology

Volume 8, 2021

Interaction of Viruses with the Insect Intestine

Abstract

In nature, insects face a constant threat of infection by numerous exogeneous viruses, and their intestinal tracts are the predominant ports of entry. Insects can acquire these viruses orally during either blood feeding by hematophagous insects or sap sucking and foliage feeding by insect herbivores. However, the insect intestinal tract forms several physical and immunological barriers to defend against viral invasion, including cell intrinsic antiviral immunity, the peritrophic matrix and the mucin layer, and local symbiotic microorganisms. Whether an infection can be successfully established in the intestinal tract depends on the complex interactions between viruses and those barriers. In this review, we summarize recent progress on virus-intestinal tract interplay in insects, in which various underlying mechanisms derived from nutritional status, dynamics of symbiotic microorganisms, and virus-encoded components play intricate roles in the regulation of virus invasion in the intestinal tract, either directly or indirectly.

Keyword(s): arbovirus, insect, intestine
Loading

Article metrics loading...

/content/journals/10.1146/annurev-virology-091919-100543
2021-09-29
2024-04-26
Loading full text...

Full text loading...

/deliver/fulltext/virology/8/1/annurev-virology-091919-100543.html?itemId=/content/journals/10.1146/annurev-virology-091919-100543&mimeType=html&fmt=ahah

Literature Cited

  1. 1. 
    Shi M, Lin XD, Chen X, Tian JH, Chen LJ et al. 2018. The evolutionary history of vertebrate RNA viruses. Nature 556:197–202
     [Google Scholar]
  2. 2. 
    Chanpanitkitchote P, Chen Y, Evans JD, Li W, Li J et al. 2018. Acute bee paralysis virus occurs in the Asian honey bee Apis cerana and parasitic mite Tropilaelaps mercedesae. J. Invertebr. Pathol. 151:131–36
     [Google Scholar]
  3. 3. 
    Grozinger CM, Flenniken ML. 2019. Bee viruses: ecology, pathogenicity, and impacts. Annu. Rev. Entomol. 64:205–26
     [Google Scholar]
  4. 4. 
    Cheng G, Liu Y, Wang P, Xiao X 2016. Mosquito defense strategies against viral infection. Trends Parasitol. 32:177–86
     [Google Scholar]
  5. 5. 
    Yu X, Zhu Y, Xiao X, Wang P, Cheng G. 2019. Progress towards understanding the mosquito-borne virus life cycle. Trends Parasitol. 35:1009–17
     [Google Scholar]
  6. 6. 
    Jia D, Chen Q, Mao Q, Zhang X, Wu W et al. 2018. Vector mediated transmission of persistently transmitted plant viruses. Curr. Opin. Virol. 28:127–32
     [Google Scholar]
  7. 7. 
    Pernice M, Simpson SJ, Ponton F. 2014. Towards an integrated understanding of gut microbiota using insects as model systems. J. Insect Physiol. 69:12–18
     [Google Scholar]
  8. 8. 
    Yin C, Sun P, Yu X, Wang P, Cheng G. 2020. Roles of symbiotic microorganisms in arboviral infection of arthropod vectors. Trends Parasitol. 36:607–15
     [Google Scholar]
  9. 9. 
    Gao H, Cui C, Wang L, Jacobs-Lorena M, Wang S 2020. Mosquito microbiota and implications for disease control. Trends Parasitol. 36:98–111
     [Google Scholar]
  10. 10. 
    Lemaitre B, Miguel-Aliaga I. 2013. The digestive tract of Drosophila melanogaster. . Annu. Rev. Genet. 47:377–404
     [Google Scholar]
  11. 11. 
    Wu K, Yang B, Huang W, Dobens L, Song H, Ling E 2016. Gut immunity in Lepidopteran insects. Dev. Comp. Immunol. 64:65–74
     [Google Scholar]
  12. 12. 
    Saraiva RG, Kang S, Simões ML, Angleró-Rodríguez YI, Dimopoulos G. 2016. Mosquito gut antiparasitic and antiviral immunity. Dev. Comp. Immunol. 64:53–64
     [Google Scholar]
  13. 13. 
    Durvasula RV, Gumbs A, Panackal A, Kruglov O, Aksoy S et al. 1997. Prevention of insect-borne disease: an approach using transgenic symbiotic bacteria. PNAS 94:3274–78
     [Google Scholar]
  14. 14. 
    Wang S, Ghosh AK, Bongio N, Stebbings KA, Lampe DJ, Jacobs-Lorena M 2012. Fighting malaria with engineered symbiotic bacteria from vector mosquitoes. PNAS 109:12734–39
     [Google Scholar]
  15. 15. 
    Shane JL, Grogan CL, Cwalina C, Lampe DJ. 2018. Blood meal-induced inhibition of vector-borne disease by transgenic microbiota. Nat. Commun. 9:4127
     [Google Scholar]
  16. 16. 
    Wu P, Sun P, Nie K, Zhu Y, Shi M et al. 2019. A gut commensal bacterium promotes mosquito permissiveness to arboviruses. Cell Host Microbe 25:101–12
     [Google Scholar]
  17. 17. 
    Dow JAT. 1987. Insect midgut function. Adv. Insect Physiol. 19:187–328
     [Google Scholar]
  18. 18. 
    Napoleão TH, Albuquerque LP, Santos ND, Nova IC, Lima TA et al. 2019. Insect midgut structures and molecules as targets of plant-derived protease inhibitors and lectins. Pest Manag. Sci. 75:1212–22
     [Google Scholar]
  19. 19. 
    Terra WR, Ferreira C 2009. Digestive system. Encyclopedia of Insects VH Resh, RT Cardé 273–81 Amsterdam: Academic, 2nd ed..
     [Google Scholar]
  20. 20. 
    Caccia S, Casartelli M, Tettamanti G. 2019. The amazing complexity of insect midgut cells: types, peculiarities, and functions. Cell Tissue Res 377:505–25
     [Google Scholar]
  21. 21. 
    de Sousa G, Conte H 2013. Midgut morphophysiology in Sitophilus zeamais Motschulsky, 1855 (Coleoptera: Curculionidae). Micron 51:1–8
     [Google Scholar]
  22. 22. 
    Harvey WR, Cioffi M, Wolfersberger MG. 1983. Chemiosmotic potassium ion pump of insect epithelia. Am. J. Physiol. 244:163–75
     [Google Scholar]
  23. 23. 
    Hakim RS, Baldwin KM, Loeb M. 2001. The role of stem cells in midgut growth and regeneration. In Vitro Cell. Dev. Biol. Anim. 37:338–42
     [Google Scholar]
  24. 24. 
    Hegedus D, Erlandson M, Gillott C, Toprak U. 2009. New insights into peritrophic matrix synthesis, architecture, and function. Annu. Rev. Entomol. 54:285–302
     [Google Scholar]
  25. 25. 
    Peters W. 1992. Peritrophic Membranes Berlin: Springer
  26. 26. 
    Lehane MJ. 1997. Peritrophic matrix structure and function. Annu. Rev. Entomol. 42:525–50
     [Google Scholar]
  27. 27. 
    Kato N, Mueller CR, Fuchs JF, McElroy K, Wessely V et al. 2008. Evaluation of the function of a type I peritrophic matrix as a physical barrier for midgut epithelium invasion by mosquito-borne pathogens in Aedes aegypti. . Vector Borne Zoonotic Dis 8:701–12
     [Google Scholar]
  28. 28. 
    Kumar S, Molina-Cruz A, Gupta L, Rodrigues J, Barillas-Mury C. 2010. A peroxidase/dual oxidase system modulates midgut epithelial immunity in Anopheles gambiae. . Science 327:1644–48
     [Google Scholar]
  29. 29. 
    Wang P, Granados RR 1997. An intestinal mucin is the target substrate for a baculovirus enhancin. PNAS 94:6977–82
     [Google Scholar]
  30. 30. 
    Wang P, Granados RR. 1997. Molecular cloning and sequencing of a novel invertebrate intestinal mucin cDNA. J. Biol. Chem. 272:16663–69
     [Google Scholar]
  31. 31. 
    Johansson ME, Hansson GC. 2016. Immunological aspects of intestinal mucus and mucins. Nat. Rev. Immunol. 16:639–49
     [Google Scholar]
  32. 32. 
    Engel P, Moran NA. 2013. The gut microbiota of insects—diversity in structure and function. FEMS Microbiol. Rev. 37:699–735
     [Google Scholar]
  33. 33. 
    Pang X, Xiao X, Liu Y, Zhang R, Liu J et al. 2016. Mosquito C-type lectins maintain gut microbiome homeostasis. Nat. Microbiol. 1:16023
     [Google Scholar]
  34. 34. 
    Xiao X, Yang L, Pang X, Zhang R, Zhu Y et al. 2017. A Mesh–Duox pathway regulates homeostasis in the insect gut. Nat. Microbiol. 2:17020
     [Google Scholar]
  35. 35. 
    Ayhan N, Charrel RN. 2017. Of phlebotomines (sandflies) and viruses: a comprehensive perspective on a complex situation. Curr. Opin. Insect Sci. 22:117–24
     [Google Scholar]
  36. 36. 
    Zhu Y, Zhang R, Zhang B, Zhao T, Wang P et al. 2017. Blood meal acquisition enhances arbovirus replication in mosquitoes through activation of the GABAergic system. Nat. Commun. 8:1262
     [Google Scholar]
  37. 37. 
    Weaver SC, Charlier C, Vasilakis N, Lecuit M. 2018. Zika, chikungunya, and other emerging vector-borne viral diseases. Annu. Rev. Med. 69:395–408
     [Google Scholar]
  38. 38. 
    Bhatt S, Gething PW, Brady OJ, Messina JP, Farlow AW et al. 2013. The global distribution and burden of dengue. Nature 496:504–7
     [Google Scholar]
  39. 39. 
    Zeller H, Van Bortel W, Sudre B. 2016. Chikungunya: its history in Africa and Asia and its spread to new regions in 2013–2014. J. Infect. Dis. 214:S436–40
     [Google Scholar]
  40. 40. 
    Parra B, Lizarazo J, Jiménez-Arango JA, Zea-Vera AF, González-Manrique G et al. 2016. Guillain–Barré syndrome associated with Zika virus infection in Colombia. N. Engl. J. Med. 375:1513–23
     [Google Scholar]
  41. 41. 
    Blanc S, Drucker M, Uzest M. 2014. Localizing viruses in their insect vectors. Annu. Rev. Phytopathol. 52:403–25
     [Google Scholar]
  42. 42. 
    Hogenhout SA, Ammar ED, Whitfield AE, Redinbaugh MG. 2008. Insect vector interactions with persistently transmitted viruses. Annu. Rev. Phytopathol. 46:327–59
     [Google Scholar]
  43. 43. 
    Chen Q, Wei T. 2016. Viral receptors of the gut: insect-borne propagative plant viruses of agricultural importance. Curr. Opin. Insect Sci. 16:9–13
     [Google Scholar]
  44. 44. 
    Zogli P, Pingault L, Grover S, Louis J 2020. Ento(o)mics: the intersection of ‘omic’ approaches to decipher plant defense against sap-sucking insect pests. Curr. Opin. Plant Biol. 56:153–61
     [Google Scholar]
  45. 45. 
    Brault V, Herrbach E, Reinbold C. 2007. Electron microscopy studies on luteovirid transmission by aphids. Micron 38:302–12
     [Google Scholar]
  46. 46. 
    Ammar ED, Gargani D, Lett JM, Peterschmitt M. 2009. Large accumulations of maize streak virus in the filter chamber and midgut cells of the leafhopper vector Cicadulina mbila. Arch. Virol. 154:255–62
     [Google Scholar]
  47. 47. 
    Watanabe S, Bressan A. 2013. Tropism, compartmentalization and retention of banana bunchy top virus (Nanoviridae) in the aphid vector Pentalonia nigronervosa. . J. Gen. Virol. 94:209–19
     [Google Scholar]
  48. 48. 
    Gray S, Gildow FE. 2003. Luteovirus-aphid interactions. Annu. Rev. Phytopathol. 41:539–66
     [Google Scholar]
  49. 49. 
    Chen Y, Evans J, Feldlaufer M. 2006. Horizontal and vertical transmission of viruses in the honey bee, Apis mellifera. . J. Invertebr. Pathol. 92:152–59
     [Google Scholar]
  50. 50. 
    Williams T, Virto C, Murillo R, Caballero P. 2017. Covert infection of insects by baculoviruses. Front. Microbiol. 8:1337
     [Google Scholar]
  51. 51. 
    Jehle JA, Blissard GW, Bonning BC, Cory JS, Herniou EA et al. 2006. On the classification and nomenclature of baculoviruses: a proposal for revision. Arch. Virol. 151:1257–66
     [Google Scholar]
  52. 52. 
    Blissard GW, Theilmann DA. 2018. Baculovirus entry and egress from insect cells. Annu. Rev. Virol. 5:113–39
     [Google Scholar]
  53. 53. 
    Skinner MA, Buller RM, Damon IK, Lefkowitz EJ, McFadden G et al. 2012. Poxviridae. Virus Taxonomy: Ninth Report of the International Committee on Taxonomy of Viruses AMQ King, MJ Adams, EB Carstens, EJ Lefkowitz 291–309 Oxford, UK: Elsevier
     [Google Scholar]
  54. 54. 
    Mitsuhashi W, Sato M, Hirai Y. 2000. Involvement of spindles of an entomopoxvirus (EPV) in infectivity of the EPVs to their host insect. Arch. Virol. 145:1465–71
     [Google Scholar]
  55. 55. 
    Mitsuhashi W, Kawakita H, Murakami R, Takemoto Y, Saiki T et al. 2007. Spindles of an entomopoxvirus facilitate its infection of the host insect by disrupting the peritrophic membrane. J. Virol. 81:4235–43
     [Google Scholar]
  56. 56. 
    Franz AW, Kantor AM, Passarelli AL, Clem RJ. 2015. Tissue barriers to arbovirus infection in mosquitoes. Viruses 7:3741–67
     [Google Scholar]
  57. 57. 
    Blair CD, Olson KE. 2015. The role of RNA interference (RNAi) in arbovirus-vector interactions. Viruses 7:820–43
     [Google Scholar]
  58. 58. 
    Sánchez-Vargas I, Scott JC, Poole-Smith BK, Franz AW, Barbosa-Solomieu V et al. 2009. Dengue virus type 2 infections of Aedes aegypti are modulated by the mosquito's RNA interference pathway. PLOS Pathog 5:e1000299
     [Google Scholar]
  59. 59. 
    Erlandson MA, Toprak U, Hegedus DD. 2019. Role of the peritrophic matrix in insect-pathogen interactions. J. Insect Physiol. 117:103894
     [Google Scholar]
  60. 60. 
    Peng J, Zhong J, Granados RR. 1999. A baculovirus enhancin alters the permeability of a mucosal midgut peritrophic matrix from lepidopteran larvae. J. Insect Physiol. 45:159–66
     [Google Scholar]
  61. 61. 
    Toprak U, Harris S, Baldwin D, Theilmann D, Gillott C et al. 2012. Role of enhancin in Mamestra configurata nucleopolyhedrovirus virulence: selective degradation of host peritrophic matrix proteins. J. Gen. Virol. 93:744–53
     [Google Scholar]
  62. 62. 
    Zhu Y, Tong L, Nie K, Wiwatanaratanabutr I, Sun P et al. 2019. Host serum iron modulates dengue virus acquisition by mosquitoes. Nat. Microbiol. 4:2405–15
     [Google Scholar]
  63. 63. 
    Nguyet MN, Duong TH, Trung VT, Nguyen TH, Tran CN et al. 2013. Host and viral features of human dengue cases shape the population of infected and infectious Aedes aegypti mosquitoes. PNAS 110:9072–77
     [Google Scholar]
  64. 64. 
    Wagar ZL, Tree MO, Mpoy MC, Conway MJ. 2017. Low density lipopolyprotein inhibits flavivirus acquisition in Aedes aegypti. . Insect Mol. Biol. 26:734–42
     [Google Scholar]
  65. 65. 
    Povey S, Cotter SC, Simpson SJ, Wilson K 2013. Dynamics of macronutrient self-medication and illness-induced anorexia in virally infected insects. J. Anim. Ecol. 83:245–55
     [Google Scholar]
  66. 66. 
    Lee KP, Cory JS, Wilson K, Raubenheimer D, Simpson SJ. 2006. Flexible diet choice offsets protein costs of pathogen resistance in a caterpillar. Proc. Biol. Sci. 273:823–29
     [Google Scholar]
  67. 67. 
    Shikano I, Cory JS. 2016. Altered nutrient intake by baculovirus-challenged insects: self-medication or compensatory feeding?. J. Invertebr. Pathol. 139:25–33
     [Google Scholar]
  68. 68. 
    Shikano I, Ericsson JD, Cory JS, Myers JH 2010. Indirect plant-mediated effects on insect immunity and disease resistance in a tritrophic system. Basic Appl. Ecol. 11:15–22
     [Google Scholar]
  69. 69. 
    Popham HJ, Shelby KS. 2009. Ascorbic acid influences the development and immunocompetence of larval heliothis virescens. . Entomol. Exp. Appl. 133:57–64
     [Google Scholar]
  70. 70. 
    Popham HJR, Shelby KS, Popham TW. 2005. Effect of dietary selenium supplementation on resistance to baculovirus infection. Biol. Control 32:419–26
     [Google Scholar]
  71. 71. 
    Lawrence SD, Novak NG. 2006. Expression of poplar chitinase in tomato leads to inhibition of development in Colorado potato beetle. Biotechnol. Lett. 28:593–99
     [Google Scholar]
  72. 72. 
    Liu J, Liu Y, Nie K, Du S, Qiu J et al. 2016. Flavivirus NS1 protein in infected host sera enhances viral acquisition by mosquitoes. Nat. Microbiol. 1:16087
     [Google Scholar]
  73. 73. 
    Liu Y, Liu J, Du S, Shan C, Nie K et al. 2017. Evolutionary enhancement of Zika virus infectivity in Aedes aegypti mosquitoes. Nature 545:482–86
     [Google Scholar]
  74. 74. 
    Plymale R, Grove MJ, Cox-Foster D, Ostiguy N, Hoover K. 2008. Plant-mediated alteration of the peritrophic matrix and baculovirus infection in lepidopteran larvae. J. Insect Physiol. 54:737–49
     [Google Scholar]
  75. 75. 
    Chen E, Kolosov D, O'Donnell MJ, Erlandson MA, McNeil JN, Donly C 2018. The effect of diet on midgut and resulting changes in infectiousness of AcMNPV baculovirus in the cabbage looper, Trichoplusia ni. Front. Physiol. 9:1348
     [Google Scholar]
  76. 76. 
    Wang P, Hammer DA, Granados RR. 1994. Interaction of Trichoplusia ni granulosis virus-encoded enhancin with the midgut epithelium and peritrophic membrane of four lepidopteran insects. J. Gen. Virol. 75:1961–67
     [Google Scholar]
  77. 77. 
    Wang P, Granados RR. 1998. Observations on the presence of the peritrophic membrane in larval Trichoplusia ni and its role in limiting baculovirus infection. J. Invertebr. Pathol. 72:57–62
     [Google Scholar]
  78. 78. 
    Lepore LS, Roelvink PR, Granados RR. 1996. Enhancin, the granulosis virus protein that facilitates nucleopolyhedrovirus (NPV) infections, is a metalloprotease. J. Invertebr. Pathol. 68:131–40
     [Google Scholar]
  79. 79. 
    Bischoff DS, Slavicek JM. 1997. Phenotypic and genetic analysis of Lymantria dispar nucleopolyhedrovirus few polyhedra mutants: Mutations in the 25K FP gene may be caused by DNA replication errors. J. Virol. 71:1097–106
     [Google Scholar]
  80. 80. 
    Popham HJ, Bischoff DS, Slavicek JM. 2001. Both Lymantria dispar nucleopolyhedrovirus enhancin genes contribute to viral potency. J. Virol. 75:8639–48
     [Google Scholar]
  81. 81. 
    Konno K, Mitsuhashi W. 2019. The peritrophic membrane as a target of proteins that play important roles in plant defense and microbial attack. J. Insect Physiol. 117:103912
     [Google Scholar]
  82. 82. 
    Mitsuhashi W, Miyamoto K. 2003. Disintegration of the peritrophic membrane of silkworm larvae due to spindles of an entomopoxvirus. J. Invertebr. Pathol. 82:34–40
     [Google Scholar]
  83. 83. 
    Liu X, Ma X, Lei C, Xiao Y, Zhang Z, Sun X. 2011. Synergistic effects of Cydia pomonella granulovirus GP37 on the infectivity of nucleopolyhedroviruses and the lethality of Bacillus thuringiensis. . Arch. Virol. 156:1707–15
     [Google Scholar]
  84. 84. 
    Li Z, Li C, Yang K, Wang L, Yin C et al. 2003. Characterization of a chitin-binding protein GP37 of Spodoptera litura multicapsid nucleopolyhedrovirus. Virus Res. 96:113–22
     [Google Scholar]
  85. 85. 
    Buchon N, Broderick NA, Lemaitre B. 2013. Gut homeostasis in a microbial world: insights from Drosophila melanogaster. . Nat. Rev. Microbiol. 11:615–26
     [Google Scholar]
  86. 86. 
    Minard G, Mavingui P, Moro CV. 2013. Diversity and function of bacterial microbiota in the mosquito holobiont. Parasite Vectors 6:146
     [Google Scholar]
  87. 87. 
    Mereghetti V, Chouaia B, Montagna M. 2017. New insights into the microbiota of moth pests. Int. J. Mol. Sci. 18:2450
     [Google Scholar]
  88. 88. 
    Favia G, Ricci I, Damiani C, Raddadi N, Crotti E et al. 2007. Bacteria of the genus Asaia stably associate with Anopheles stephensi, an Asian malarial mosquito vector. PNAS 104:9047–51
     [Google Scholar]
  89. 89. 
    Chen S, Blom J, Walker ED. 2017. Genomic, physiologic, and symbiotic characterization of Serratia marcescens strains isolated from the mosquito Anopheles stephensi. . Front. Microbiol. 8:1483
     [Google Scholar]
  90. 90. 
    Perlmutter JI, Bordenstein SR. 2020. Microorganisms in the reproductive tissues of arthropods. Nat. Rev. Microbiol. 18:97–111
     [Google Scholar]
  91. 91. 
    Strand MR. 2018. Composition and functional roles of the gut microbiota in mosquitoes. Curr. Opin. Insect Sci. 28:59–65
     [Google Scholar]
  92. 92. 
    Coon KL, Brown MR, Strand MR. 2016. Mosquitoes host communities of bacteria that are essential for development but vary greatly between local habitats. Mol. Ecol. 25:5806–26
     [Google Scholar]
  93. 93. 
    Ramirez JL, Souza-Neto J, Torres Cosme R, Rovira J, Ortiz A et al. 2012. Reciprocal tripartite interactions between the Aedes aegypti midgut microbiota, innate immune system and dengue virus influences vector competence. PLOS Negl. Trop. Dis. 6:e1561
     [Google Scholar]
  94. 94. 
    Xi Z, Ramirez JL, Dimopoulos G. 2008. The Aedes aegypti Toll pathway controls dengue virus infection. PLOS Pathog 4:e1000098
     [Google Scholar]
  95. 95. 
    Dong Y, Morton JC Jr., Ramirez JL, Souza-Neto JA, Dimopoulos G. 2012. The entomopathogenic fungus Beauveria bassiana activate Toll and JAK-STAT pathway-controlled effector genes and anti-dengue activity in Aedes aegypti. . Insect Biochem. Mol. Biol. 42:126–32
     [Google Scholar]
  96. 96. 
    Chamy LE, Matt N, Ntwasa M, Reichhart JM. 2015. The multilayered innate immune defense of the gut. Biomed. J. 38:276–84
     [Google Scholar]
  97. 97. 
    Rodgers FH, Gendrin M, Wyer CAS, Christophides GK. 2017. Microbiota-induced peritrophic matrix regulates midgut homeostasis and prevents systemic infection of malaria vector mosquitoes. PLOS Pathog 13:e1006391
     [Google Scholar]
  98. 98. 
    Angleró-Rodríguez YI, Talyuli OA, Blumberg BJ, Kang S, Demby C et al. 2017. An Aedes aegypti-associated fungus increases susceptibility to dengue virus by modulating gut trypsin activity. eLife 6:e28844
     [Google Scholar]
  99. 99. 
    Liu R, Wang W, Liu X, Lu Y, Xiang T et al. 2018. Characterization of a lipase from the silkworm intestinal bacterium Bacillus pumilus with antiviral activity against Bombyx mori (Lepidoptera: Bombycidae) nucleopolyhedrovirus in vitro. J. Insect Sci. 18:3
     [Google Scholar]
  100. 100. 
    Rao R, Fiandra L, Giordana B, de Eguileor M, Congiu T et al. 2004. AcMNPV ChiA protein disrupts the peritrophic membrane and alters midgut physiology of Bombyx mori larvae. Insect Biochem. Mol. Biol. 34:1205–13
     [Google Scholar]
  101. 101. 
    Shapiro M, Preisler HK, Robertson JL. 1987. Enhancement of baculovirus activity on gypsy moth (Lepidoptera: Lymantriidae) by chitinase. J. Econ. Entomol. 80:1113–16
     [Google Scholar]
  102. 102. 
    Saraiva RG, Fang J, Kang S, Angleró-Rodríguez YI, Dong Y, Dimopoulos G 2018. Aminopeptidase secreted by Chromobacterium sp. Panama inhibits dengue virus infection by degrading the E protein. PLOS Negl. Trop. Dis. 12:e0006443
     [Google Scholar]
  103. 103. 
    Yu X, Zhang L, Tong L, Zhang N, Wang H et al. 2020. Broad-spectrum virucidal activity of bacterial secreted lipases against flaviviruses, SARS-CoV-2 and other enveloped viruses. bioRxiv 2020.05.22.109900. https://doi.org/10.1101/2020.05.22.109900
    [Crossref]
  104. 104. 
    Joyce JD, Nogueira JR, Bales AA, Pittman KE, Anderson JR. 2011. Interactions between La Crosse virus and bacteria isolated from the digestive tract of Aedes albopictus (Diptera: Culicidae). J. Med. Entomol. 48:389–94
     [Google Scholar]
  105. 105. 
    Apte-Deshpande A, Paingankar M, Gokhale MD, Deobagkar DN. 2012. Serratia odorifera a midgut inhabitant of Aedes aegypti mosquito enhances its susceptibility to dengue-2 virus. PLOS ONE 7:e40401
     [Google Scholar]
/content/journals/10.1146/annurev-virology-091919-100543
Loading
Interaction of Viruses with the Insect Intestine
Annual Review of Virology 8, 115 (2021); https://doi.org/10.1146/annurev-virology-091919-100543
/content/journals/10.1146/annurev-virology-091919-100543
/content/journals/10.1146/annurev-virology-091919-100543
Loading

Data & Media loading...

  • Article Type: Review Article

Most Cited Most Cited RSS feed

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error