Increased survivorship following bacterial infection by the mosquito Aedes aegypti as compared to Anopheles gambiae correlates with increased transcriptional induction of antimicrobial peptides

Developmental and Comparative Immunology

Volumn 37, Issue 3-4, 2012, Pages 390-401

  Coggins, Sarah A ^a   Estévez Lao, Tania Y ^a   Hillyer, Julián F ^a  

^a VANDERBILT UNIVERSITY   (United States)

Author keywords

Antimicrobial peptide; Bacteria; Hemocyte; Immunity; Mosquito; Phagocytosis

Indexed keywords

CECROPIN; DEFENSIN; MESSENGER RNA;

AEDES AEGYPTI; ANIMAL CELL; ANIMAL EXPERIMENT; ANOPHELES GAMBIAE; ARTICLE; BACTERIAL INFECTION; BACTERIUM CARRIER; BLOOD CELL COUNT; CECROPIN GENE; CELLULAR IMMUNITY; CONTROLLED STUDY; DEFENSIN GENE; FEMALE; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENE INDUCTION; HUMORAL IMMUNITY; IMMUNE RESPONSE GENE; IMMUNOCOMPETENCE; IMMUNOMODULATION; IMMUNOREACTIVITY; NONHUMAN; PHAGOCYTOSIS; PRIORITY JOURNAL; SPECIES COMPARISON; SURVIVAL RATE; TRANSCRIPTION REGULATION;

AEDES AEGYPTI; ANOPHELES GAMBIAE; BACTERIA (MICROORGANISMS);

EID: 84862136825     PISSN: 0145305X     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.dci.2012.01.005     Document Type: Article

References (70)

1. Abraham E.G., Pinto S.B., Ghosh A., Vanlandingham D.L., Budd A., Higgs S., Kafatos F.C., Jacobs-Lorena M., Michel K. An immune-responsive serpin, SRPN6, mediates mosquito defense against malaria parasites. Proc. Natl. Acad. Sci. USA 2005, 102:16327-16332.
2. An C., Budd A., Kanost M.R., Michel K. Characterization of a regulatory unit that controls melanization and affects longevity of mosquitoes. Cell Mol. Life. Sci. 2011, 68:1929-1939.
3. Andereck J.W., King J.G., Hillyer J.F. Contraction of the ventral abdomen potentiates extracardiac retrograde hemolymph propulsion in the mosquito hemocoel. PLoS ONE 2010, 5:e12943.
4. Bartholomay L.C., Cho W.-L., Rocheleau T.A., Boyle J.P., Beck E.T., Fuchs J.F., Liss P., Rusch M., Butler K.M., Wu R.C.-C., Lin S.-P., Kuo H.-Y., Tsao I.-Y., Huang C.-Y., Liu T.-T., Hsiao K.-J., Tsai S.-F., Yang U.-C., Nappi A.J., Perna N.T., Chen C.-C., Christensen B.M. Description of the transcriptomes of immune response-activated hemocytes from the mosquito vectors Aedes aegypti and Armigeres subalbatus. Infect. Immun. 2004, 72:4114-4126.
5. Bartholomay L.C., Fuchs J.F., Cheng L.-L., Beck E.T., Vizioli J., Lowenberger C., Christensen B.M. Reassessing the role of defensin in the innate immune response of the mosquito, Aedes aegypti. Insect Mol. Biol. 2004, 13:125-132.
6. Bartholomay L.C., Waterhouse R.M., Mayhew G.F., Campbell C.L., Michel K., Zou Z., Ramirez J.L., Das S., Alvarez K., Arensburger P., Bryant B., Chapman S.B., Dong Y., Erickson S.M., Karunaratne S.H.P.P., Kokoza V., Kodira C.D., Pignatelli P., Shin S.W., Vanlandingham D.L., Atkinson P.W., Birren B., Christophides G.K., Clem R.J., Hemingway J., Higgs S., Megy K., Ranson H., Zdobnov E.M., Raikhel A.S., Christensen B.M., Dimopoulos G., Muskavitch M.A.T. Pathogenomics of Culex quinquefasciatus and meta-analysis of infection responses to diverse pathogens. Science 2010, 330:88-90.
7. Baton L., Robertson A., Warr E., Strand M., Dimopoulos G. Genome-wide transcriptomic profiling of Anopheles gambiae hemocytes reveals pathogen-specific signatures upon bacterial challenge and Plasmodium berghei infection. BMC Genomics 2009, 10:257.
8. Becker N., Petric D., Zgomba M., Boase C., Dahl C., Madon M., Kaiser A. Mosquitoes and Their Control 2010, Springer-Verlag, New York. 2nd ed.
9. Biron D.G., Agnew P., Marché L., Renault L., Sidobre C., Michalakis Y. Proteome of Aedes aegypti larvae in response to infection by the intracellular parasite Vavraia culicis. Int. J. Parasitol. 2005, 35:1385-1397.
10. Blandin S.A., Moita L.F., Köcher T., Wilm M., Kafatos F.C., Levashina E.A. Reverse genetics in the mosquito Anopheles gambiae: targeted disruption of the Defensin gene. EMBO Rep. 2002, 3:852-856.
11. Castillo J., Brown M.R., Strand M.R. Blood feeding and insulin-like peptide 3 stimulate proliferation of hemocytes in the mosquito Aedes aegypti. PLoS Pathog. 2011, 7:e1002274.
12. Castillo J.C., Robertson A.E., Strand M.R. Characterization of hemocytes from the mosquitoes Anopheles gambiae and Aedes aegypti. Insect Biochem. Mol. Biol. 2006, 36:891-903.
13. Cheng G., Cox J., Wang P., Krishnan M.N., Dai J., Qian F., Anderson J.F., Fikrig E. A C-type lectin collaborates with a CD45 phosphatase homolog to facilitate West Nile virus infection of mosquitoes. Cell 2010, 142:714-725.
14. Christensen B.M., Huff B.M., Miranpuri G.S., Harris K.L., Christensen L.A. Hemocyte population changes during the immune response of Aedes aegypti to inoculated microfilariae of Dirofilaria immitis. J. Parasitol. 1989, 75:119-123.
15. Christophides G.K., Zdobnov E., Barillas-Mury C., Birney E., Blandin S.A., Blass C., Brey P.T., Collins F.H., Danielli A., Dimopoulos G., Hetru C., Hoa N.T., Hoffmann J.A., Kanzok S.M., Letunic I., Levashina E.A., Loukeris T.G., Lycett G.J., Meister S., Michel K., Moita L.F., Müller H.-M., Osta M.A., Paskewitz S.M., Reichhart J.-M., Rzhetsky A., Troxler L., Vernick K.D., Vlachou D., Volz J., von Mering C., Xu J., Zheng L., Bork P., Kafatos F.C. Immunity-related genes and gene families in Anopheles gambiae. Science 2002, 298:159-165.
16. Das S., Dong Y., Garver L., Dimopoulos G. Specificity of the innate immune system: a closer look at the mosquito pattern-recognition receptor repertoire. Insect Infection and Immunity: Evolution, Ecology, and Mechanisms 2009, 69-85. Oxford University Press, Oxford. J. Rolff, S.E. Reynolds (Eds.).
17. Dong Y., Aguilar R., Xi Z., Warr E., Mongin E., Dimopoulos G. Anopheles gambiae immune responses to human and rodent Plasmodium parasite species. PLoS Pathog. 2006, 2:e52.
18. Dong Y., Dimopoulos G. Anopheles fibrinogen-related proteins provide expanded pattern recognition capacity against bacteria and malaria parasites. J. Biol. Chem. 2009, 284:9835-9844.
19. Enserink M. Meet the mosquitoes. Science 2002, 298:95.
20. Glenn J.D., King J.G., Hillyer J.F. Structural mechanics of the mosquito heart and its function in bidirectional hemolymph transport. J. Exp. Biol. 2010, 213:541-550.
21. González-Lázaro M., Dinglasan R.R., Hernández-Hernández F.D.L.C., Rodríguez M.H., Laclaustra M., Jacobs-Lorena M., Flores-Romo L. Anopheles gambiae Croquemort SCRBQ2, expression profile in the mosquito and its potential interaction with the malaria parasite Plasmodium berghei. Insect Biochem. Mol. Biol. 2009, 39:395-402.
22. Gorman M.J., Paskewitz S.M. Persistence of infection in mosquitoes injected with bacteria. J. Invertebr. Pathol. 2000, 75:296-297.
23. Gratz N., Steffen R., Cocksedge W. Why aircraft disinsection?. Bull. World Health Organ. 2000, 78:995-1004.
24. Haine E.R., Moret Y., Siva-Jothy M.T., Rolff J. Antimicrobial defense and persistent infection in insects. Science 2008, 322:1257-1259.
25. Hillyer J.F. Mosquito immunity. Invertebr. Immunity 2010, 708:218-238.
26. Hillyer J.F., Barreau C., Vernick K.D. Efficiency of salivary gland invasion by malaria sporozoites is controlled by rapid sporozoite destruction in the mosquito haemocoel. Int. J. Parasitol. 2007, 37:673-681.
27. Hillyer J.F., Christensen B.M. Characterization of hemocytes from the yellow fever mosquito, Aedes aegypti. Histochem. Cell Biol. 2002, 117:431-440.
28. Hillyer J.F., Christensen B.M. Mosquito phenoloxidase and defensin colocalize in melanization innate immune responses. J. Histochem. Cytochem. 2005, 53:689-698.
29. Hillyer J.F., Estévez-Lao T.Y. Nitric oxide is an essential component of the hemocyte-mediated mosquito immune response against bacteria. Dev. Comp. Immunol. 2010, 34:141-149.
30. Hillyer J.F., Schmidt S.L., Christensen B.M. Hemocyte-mediated phagocytosis and melanization in the mosquito Armigeres subalbatus following immune challenge by bacteria. Cell Tissue Res. 2003, 313:117-127.
31. Hillyer J.F., Schmidt S.L., Christensen B.M. Rapid phagocytosis and melanization of bacteria and Plasmodium sporozoites by hemocytes of the mosquito Aedes aegypti. J. Parasitol. 2003, 89:62-69.
32. Hillyer J.F., Schmidt S.L., Christensen B.M. The antibacterial innate immune response by the mosquito Aedes aegypti is mediated by hemocytes and independent of Gram type and pathogenicity. Microbes Infect. 2004, 6:448-459.
33. Hillyer J.F., Schmidt S.L., Fuchs J.F., Boyle J.P., Christensen B.M. Age-associated mortality in immune challenged mosquitoes (Aedes aegypti) correlates with a decrease in haemocyte numbers. Cell Microbiol. 2005, 7:39-51.
34. Holt R.A., Subramanian G.M., Halpern A., Sutton G.G., Charlab R., Nusskern D.R., Wincker P., Clark A.G., Ribeiro J.M.C., Wides R., Salzberg S.L., Loftus B., Yandell M., Majoros W.H., Rusch D.B., Lai Z., Kraft C.L., Abril J.F., Anthouard V., Arensburger P., Atkinson P.W., Baden H., de Berardinis V., Baldwin D., Benes V., Biedler J., Blass C., Bolanos R., Boscus D., Barnstead M., Cai S., Center A., Chaturverdi K., Christophides G.K., Chrystal M.A., Clamp M., Cravchik A., Curwen V., Dana A., Delcher A., Dew I., Evans C.A., Flanigan M., Grundschober-Freimoser A., Friedli L., Gu Z., Guan P., Guigo R., Hillenmeyer M.E., Hladun S.L., Hogan J.R., Hong Y.S., Hoover J., Jaillon O., Ke Z., Kodira C., Kokoza E., Koutsos A., Letunic I., Levitsky A., Liang Y., Lin J.-J., Lobo N.F., Lopez J.R., Malek J.A., McIntosh T.C., Meister S., Miller J., Mobarry C., Mongin E., Murphy S.D., O'Brochta D.A., Pfannkoch C., Qi R., Regier M.A., Remington K., Shao H., Sharakhova M.V., Sitter C.D., Shetty J., Smith T.J., Strong R., Sun J., Thomasova D., Ton L.Q., Topalis P., Tu Z., Unger M.F., Walenz B., Wang A., Wang J., Wang M., Wang X., Woodford K.J., Wortman J.R., Wu M., Yao A., Zdobnov E.M., Zhang H., Zhao Q., Zhao S., Zhu S.C., Zhimulev I., Coluzzi M., della Torre A., Roth C.W., Louis C., Kalush F., Mural R.J., Myers E.W., Adams M.D., Smith H.O., Broder S., Gardner M.J., Fraser C.M., Birney E., Bork P., Brey P.T., Venter J.C., Weissenbach J., Kafatos F.C., Collins F.H., Hoffman S.L. The genome sequence of the malaria mosquito Anopheles gambiae. Science 2002, 298:129-149.
35. Kajla M.K., Andreeva O., Gilbreath T.M., Paskewitz S.M. Characterization of expression, activity and role in antibacterial immunity of Anopheles gambiae lysozyme c-1. Comp. Biochem. Physiol. B, Biochem. Mol. Biol. 2010, 155:201-209.
36. Kajla M.K., Shi L., Li B., Luckhart S., Li J., Paskewitz S.M. A new role for an old antimicrobial: lysozyme c-1 can function to protect malaria parasites in Anopheles mosquitoes. PLoS ONE 2011, 6:e19649.
37. Kim G.S., Kim Y. Up-regulation of circulating hemocyte population in response to bacterial challenge is mediated by octopamine and 5-hydroxytryptamine via Rac1 signal in Spodoptera exigua. J. Insect Physiol.. 2010, 56:559-566.
38. Kim J.H., Min J.S., Kang J.S., Kwon D.H., Yoon K.S., Strycharz J., Koh Y.H., Pittendrigh B.R., Clark J.M., Lee S.H. Comparison of the humoral and cellular immune responses between body and head lice following bacterial challenge. Insect Biochem. Mol. Biol. 2011, 41:332-339.
39. Kim W., Koo H., Richman A.M., Seeley D., Vizioli J., Klocko A.D., O'Brochta D.A. Ectopic expression of a cecropin transgene in the human malaria vector mosquito Anopheles gambiae (Diptera: Culicidae): effects on susceptibility to Plasmodium. J. Med. Entomol. 2004, 41:447-455.
40. Kokoza V., Ahmed A., Woon Shin S., Okafor N., Zou Z., Raikhel A.S. Blocking of Plasmodium transmission by cooperative action of Cecropin A and Defensin A in transgenic Aedes aegypti mosquitoes. Proc. Natl. Acad. Sci. USA 2010, 107:8111-8116.
41. Kumar S., Molina-Cruz A., Gupta L., Rodrigues J., Barillas-Mury C. A peroxidase/dual oxidase system modulates midgut epithelial immunity in Anopheles gambiae. Science 2010, 327:1644-1648.
42. Lapcharoen P., Komalamisra N., Rongsriyam Y., Wangsuphachart V., Dekumyoy P., Prachumsri J., Kajla M.K., Paskewitz S.M. Investigations on the role of a lysozyme from the malaria vector Anopheles dirus during malaria parasite development. Dev. Comp. Immunol. 2012, 36:104-111.
43. Li B., Paskewitz S.M. A role for lysozyme in melanization of Sephadex beads in Anopheles gambiae. J. Insect Physiol. 2006, 52:936-942.
44. Livak K.J., Schmittgen T.D. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. Methods 2001, 25:402-408.
45. Lounibos L.P. Invasions by insect vectors of human disease. Annu. Rev. Entomol. 2002, 47:233-266.
46. Lowenberger C., Bulet P., Charlet M., Hetru C., Hodgeman B., Christensen B.M., Hoffmann J.A. Insect immunity: isolation of three novel inducible antibacterial defensins from the vector mosquito, Aedes aegypti. Insect Biochem. Mol. Biol. 1995, 25:867-873.
47. Lowenberger C., Charlet M., Vizioli J., Kamal S., Richman A., Christensen B.M., Bulet P. Antimicrobial activity spectrum, cDNA cloning, and mRNA expression of a newly isolated member of the cecropin family from the mosquito vector Aedes aegypti. J. Biol. Chem. 1999, 274:20092-20097.
48. Lowenberger C.A., Kamal S., Chiles J., Paskewitz S., Bulet P., Hoffmann J.A., Christensen B.M. Mosquito-Plasmodium interactions in response to immune activation of the vector. Exp. Parasitol. 1999, 91:59-69.
49. Magalhaes T., Leandro D.C., Ayres C.F.J. Knock-down of REL2, but not defensin A, augments Aedes aegypti susceptibility to Bacillus subtilis and Escherichia coli. Acta Trop. 2010, 113:167-173.
50. Márkus R., Laurinyecz B., Kurucz E., Honti V., Bajusz I., Sipos B., Somogyi K., Kronhamn J., Hultmark D., Andó I. Sessile hemocytes as a hematopoietic compartment in Drosophila melanogaster. Proc. Natl. Acad. Sci. USA 2009, 106:4805-4809.
51. Martins G.F., Pimenta P.F.P. Structural changes in fat body of Aedes aegypti caused by aging and blood feeding. J. Med. Entomol. 2008, 45:1102-1107.
52. Michel K., Budd A., Pinto S., Gibson T.J., Kafatos F.C. Anopheles gambiae SRPN2 facilitates midgut invasion by the malaria parasite Plasmodium berghei. EMBO Rep. 2005, 6:891-897.
53. Molina-Cruz A., DeJong R.J., Charles B., Gupta L., Kumar S., Jaramillo-Gutierrez G., Barillas-Mury C. Reactive oxygen species modulate Anopheles gambiae immunity against bacteria and Plasmodium. J. Biol. Chem. 2008, 283:3217-3223.
54. Nene V., Wortman J.R., Lawson D., Haas B., Kodira C., Tu Z.J., Loftus B., Xi Z., Megy K., Grabherr M., Ren Q., Zdobnov E.M., Lobo N.F., Campbell K.S., Brown S.E., Bonaldo M.F., Zhu J., Sinkins S.P., Hogenkamp D.G., Amedeo P., Arensburger P., Atkinson P.W., Bidwell S., Biedler J., Birney E., Bruggner R.V., Costas J., Coy M.R., Crabtree J., Crawford M., Debruyn B., Decaprio D., Eiglmeier K., Eisenstadt E., El-Dorry H., Gelbart W.M., Gomes S.L., Hammond M., Hannick L.I., Hogan J.R., Holmes M.H., Jaffe D., Johnston J.S., Kennedy R.C., Koo H., Kravitz S., Kriventseva E.V., Kulp D., Labutti K., Lee E., Li S., Lovin D.D., Mao C., Mauceli E., Menck C.F.M., Miller J.R., Montgomery P., Mori A., Nascimento A.L., Naveira H.F., Nusbaum C., O'leary S., Orvis J., Pertea M., Quesneville H., Reidenbach K.R., Rogers Y.-H., Roth C.W., Schneider J.R., Schatz M., Shumway M., Stanke M., Stinson E.O., Tubio J.M.C., Vanzee J.P., Verjovski-Almeida S., Werner D., White O., Wyder S., Zeng Q., Zhao Q., Zhao Y., Hill C.A., Raikhel A.S., Soares M.B., Knudson D.L., Lee N.H., Galagan J., Salzberg S.L., Paulsen I.T., Dimopoulos G., Collins F.H., Birren B., Fraser-Liggett C.M., Severson D.W. Genome sequence of Aedes aegypti, a major arbovirus vector. Science 2007, 316:1718-1723.
55. Oliveira J.H.M., Gonçalves R.L.S., Lara F.A., Dias F.A., Gandara A.C.P., Menna-Barreto R.F.S., Edwards M.C., Laurindo F.R.M., Silva-Neto M.A.C., Sorgine M.H.F., Oliveira P.L. Blood meal-derived heme decreases ROS levels in the midgut of Aedes aegypti and allows proliferation of intestinal microbiota. PLoS Pathog. 2011, 7:e1001320.
56. Paskewitz S.M., Brown M.R., Collins F.H., Lea A.O. Ultrastructural localization of phenoloxidase in the midgut of refractory Anopheles gambiae and association of the enzyme with encapsulated Plasmodium cynomolgi. J. Parasitol. 1989, 75:594-600.
57. Pinto S.B., Kafatos F.C., Michel K. The parasite invasion marker SRPN6 reduces sporozoite numbers in salivary glands of Anopheles gambiae. Cell Microbiol. 2008, 10:891-898.
58. Pinto S.B., Lombardo F., Koutsos A.C., Waterhouse R.M., McKay K., An C., Ramakrishnan C., Kafatos F.C., Michel K. Discovery of Plasmodium modulators by genome-wide analysis of circulating hemocytes in Anopheles gambiae. Proc. Natl. Acad. Sci. USA 2009, 106:21270-21275.
59. Schnitger A.K.D., Yassine H., Kafatos F.C., Osta M.A. Two C-type lectins cooperate to defend Anopheles gambiae against Gram-negative bacteria. J. Biol. Chem. 2009, 284:17616-17624.
60. Shiao S.-H., Higgs S., Adelman Z., Christensen B.M., Liu S.H., Chen C.-C. Effect of prophenoloxidase expression knockout on the melanization of microfilariae in the mosquito Armigeres subalbatus. Insect Mol. Biol. 2001, 10:315-321.
61. Telang A., Qayum A.A., Parker A., Sacchetta B.R., Byrnes G.R. Larval nutritional stress affects vector immune traits in adult yellow fever mosquito Aedes aegypti (Stegomyia aegypti). Med. Vet. Entomol. 2011, 10.1111/j.1365-2915.2011.00993.x.
62. Ursic Bedoya R.J., Mitzey A.M., Obraztsova M., Lowenberger C. Molecular cloning and transcriptional activation of lysozyme-encoding cDNAs in the mosquito Aedes aegypti. Insect Mol. Biol. 2005, 14:89-94.
63. Vezzani D., Carbajo A.E. Aedes aegypti, Aedes albopictus, and dengue in Argentina: current knowledge and future directions. Mem. Inst. Oswaldo Cruz 2008, 103:66-74.
64. Vizioli J., Bulet P., Charlet M., Lowenberger C., Blass C., Müller H.M., Dimopoulos G., Hoffmann J., Kafatos F.C., Richman A. Cloning and analysis of a cecropin gene from the malaria vector mosquito, Anopheles gambiae. Insect Mol. Biol. 2000, 9:75-84.
65. Vizioli J., Bulet P., Hoffmann J.A., Kafatos F.C., Müller H.M., Dimopoulos G. Gambicin: a novel immune responsive antimicrobial peptide from the malaria vector Anopheles gambiae. Proc. Natl. Acad. Sci. USA 2001, 98:12630-12635.
66. Volz J., Müller H.-M., Zdanowicz A., Kafatos F.C., Osta M.A. A genetic module regulates the melanization response of Anopheles to Plasmodium. Cell Microbiol. 2006, 8:1392-1405.
67. Volz J., Osta M.A., Kafatos F.C., Müller H.-M. The roles of two clip domain serine proteases in innate immune responses of the malaria vector Anopheles gambiae. J. Biol. Chem. 2005, 280:40161-40168.
68. Warr E., Das S., Dong Y., Dimopoulos G. The Gram-negative bacteria-binding protein gene family: its role in the innate immune system of Anopheles gambiae and in anti-Plasmodium defence. Insect Mol. Biol. 2008, 17:39-51.
69. Waterhouse R.M., Kriventseva E.V., Meister S., Xi Z., Alvarez K.S., Bartholomay L.C., Barillas-Mury C., Bian G., Blandin S.A., Christensen B.M., Dong Y., Jiang H., Kanost M.R., Koutsos A.C., Levashina E.A., Li J., Ligoxygakis P., MacCallum R.M., Mayhew G.F., Mendes A., Michel K., Osta M.A., Paskewitz S.M., Shin S.W., Vlachou D., Wang L., Wei W., Zheng L., Zou Z., Severson D.W., Raikhel A.S., Kafatos F.C., Dimopoulos G., Zdobnov E.M., Christophides G.K. Evolutionary dynamics of immune-related genes and pathways in disease-vector mosquitoes. Science 2007, 316:1738-1743.
70. Zou Z., Shin S.W., Alvarez K.S., Kokoza V., Raikhel A.S. Distinct melanization pathways in the mosquito Aedes aegypti. Immunity 2010, 32:41-53.