Obligate symbionts activate immune system development in the tsetse fly

Journal of Immunology

Volumn 188, Issue 7, 2012, Pages 3395-3403

  Weiss, Brian L ^a   Maltz, Michele ^a   Aksoy, Serap ^a  

^a YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMAL CELL; ARTICLE; BLOOD CELL; CELL TRANSPLANTATION; CELLULAR IMMUNITY; CONTROLLED STUDY; ESCHERICHIA COLI INFECTION; ESCHERICHIA COLI K 12; FEMALE; GENE EXPRESSION; HUMORAL IMMUNITY; IMMUNE SYSTEM; LARVA; NONHUMAN; PHAGOCYTOSIS; PHENOTYPE; PRIORITY JOURNAL; SYMBIONT; SYMBIOSIS; TSETSE FLY; WIGGLESWORTHIA; WILD TYPE;

ADJUVANTS, IMMUNOLOGIC; ANIMALS; DISEASE RESISTANCE; ENTEROBACTERIACEAE; ESCHERICHIA COLI; FEMALE; GENE EXPRESSION PROFILING; HEMOCYTES; HEMOLYMPH; IMMUNITY, CELLULAR; IMMUNITY, HUMORAL; INSECT PROTEINS; LARVA; SYMBIOSIS; TISSUE EXTRACTS; TRANSCRIPTION FACTORS; TSETSE FLIES; WIGGLESWORTHIA; WOLBACHIA;

EID: 84859407382     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1103691     Document Type: Article

References (49)

1. Wernegreen, J. J. 2002. Genome evolution in bacterial endosymbionts of insects. Nat. Rev. Genet. 3: 850-861. (Pubitemid 35303517)
2. Moran, N. A. 2006. Symbiosis. Curr. Biol. 16: R866-R871. (Pubitemid 44573826)
3. Teixeira, L., A. Ferreira, and M. Ashburner. 2008. The bacterial symbiont Wolbachia induces resistance to RNA viral infections in Drosophila melanogaster. PLoS Biol. 6: e2.
4. Dong, Y., F. Manfredini, and G. Dimopoulos. 2009. Implication of the mosquito midgut microbiota in the defense against malaria parasites. PLoS Pathog. 5: e1000423.
5. Rodrigues, J., F. A. Brayner, L. C. Alves, R. Dixit, and C. Barillas-Mury. 2010. Hemocyte differentiation mediates innate immune memory in Anopheles gambiae mosquitoes. Science 329: 1353-1355.
6. Cirimotich, C. M., Y. Dong, A. M. Clayton, S. L. Sandiford, J. A. Souza-Neto, M. Mulenga, and G. Dimopoulos. 2011. Natural microbe-mediated refractoriness to Plasmodium infection in Anopheles gambiae. Science 332: 855-858.
7. Attardo, G. M., C. Lohs, A. Heddi, U. H. Alam, S. Yildirim, and S. Aksoy. 2008. Analysis of milk gland structure and function in Glossina morsitans: milk protein production, symbiont populations and fecundity. J. Insect Physiol. 54: 1236-1242.
8. Cheng, Q., T. D. Ruel, W. Zhou, S. K. Moloo, P. Majiwa, S. L. O'Neill, and S. Aksoy. 2000. Tissue distribution and prevalence of Wolbachia infections in tsetse flies, Glossina spp. Med. Vet. Entomol. 14: 44-50. (Pubitemid 30186108)
9. Pais, R., C. Lohs, Y. Wu, J. Wang, and S. Aksoy. 2008. The obligate mutualist Wigglesworthia glossinidia influences reproduction, digestion, and immunity processes of its host, the tsetse fly. Appl. Environ. Microbiol. 74: 5965-5974.
10. Wang, J., Y. Wu, G. Yang, and S. Aksoy. 2009. Interactions between mutualist Wigglesworthia and tsetse peptidoglycan recognition protein (PGRP-LB) influence trypanosome transmission. Proc. Natl. Acad. Sci. USA 106: 12133-12138.
11. Weiss, B. L., J. Wang, and S. Aksoy. 2011. Tsetse immune system maturation requires the presence of obligate symbionts in larvae. PLoS Biol. 9: e1000619.
12. Moloo, S. K. 1971. An artificial feeding technique for Glossina. Parasitology 63: 507-512.
13. Weiss, B. L., Y. Wu, J. J. Schwank, N. S. Tolwinski, and S. Aksoy. 2008. An insect symbiosis is influenced by bacterium-specific polymorphisms in outer-membrane protein A. Proc. Natl. Acad. Sci. USA 105: 15088-15093.
14. Dale, C., and I. Maudlin. 1999. Sodalis gen. nov. and Sodalis glossinidius sp. nov., a microaerophilic secondary endosymbiont of the tsetse fly Glossina morsitans morsitans. Int. J. Syst. Bacteriol. 49: 267-275. (Pubitemid 29225889)
15. Castillo, J. C., A. E. Robertson, and M. R. Strand. 2006. Characterization of hemocytes from the mosquitoes Anopheles gambiae and Aedes aegypti. Insect Biochem. Mol. Biol. 36: 891-903. (Pubitemid 46053792)
16. Alam, U., J. Medlock, C. Brelsfoard, R. Pais, C. Lohs, S. Balmand, J. Carnogursky, A. Heddi, P. Takac, A. Galvani, and S. Aksoy. 2011. Wolbachia symbiont infections induce strong cytoplasmic incompatibility in the tsetse fly Glossina morsitans. PLoS Pathog. 7: e1002415.
17. Holmes, D. S., and J. B. Bonner. 1973. Preparation, molecular weight, base composition, and secondary structure of giant nuclear ribonucleic acid. Biochemistry 12: 2330-2338.
18. Weiss, B. L., and S. Aksoy. 2011. Microbiome influences on insect host vector competence. Trends Parasitol. 27: 514-522.
19. Elrod-Erickson, M., S. Mishra, and D. S. Schneider. 2000. Interactions between the cellular and humoral immune responses in Drosophila. Curr. Biol. 10: 781-784. (Pubitemid 30466941)
20. Zaidman-Rémy, A., M. Hervé, M. Poidevin, S. Pili-Floury, M. S. Kim, D. Blanot, B. H. Oh, R. Ueda, D. Mengin-Lecreulx, and B. Lemaitre. 2006. The Drosophila amidase PGRP-LB modulates the immune response to bacterial infection. Immunity 24: 463-473.
21. Ryu, J. H., S. H. Kim, H. Y. Lee, J. Y. Bai, Y. D. Nam, J. W. Bae, D. G. Lee, S. C. Shin, E. M. Ha, and W. J. Lee. 2008. Innate immune homeostasis by the homeobox gene caudal and commensal-gut mutualism in Drosophila. Science 319: 777-782.
22. Krzemień, J., L. Dubois, R. Makki, M. Meister, A. Vincent, and M. Crozatier. 2007. Control of blood cell homeostasis in Drosophila larvae by the posterior signalling centre. Nature 446: 325-328. (Pubitemid 46426162)
23. Makki, R., M. Meister, D. Pennetier, J. M. Ubeda, A. Braun, V. Daburon, J. Krzemień, H. M. Bourbon, R. Zhou, A. Vincent, and M. Crozatier. 2010. A short receptor downregulates JAK/STAT signalling to control the Drosophila cellular immune response. PLoS Biol. 8: e1000441.
24. Ha, E. M., C. T. Oh, Y. S. Bae, andW. J. Lee. 2005. A direct role for dual oxidase in Drosophila gut immunity. Science 310: 847-850.
25. Kumar, S., A. Molina-Cruz, L. Gupta, J. Rodrigues, and C. Barillas-Mury. 2010. A peroxidase/dual oxidase system modulates midgut epithelial immunity in Anopheles gambiae. Science 327: 1644-1648.
26. Oliveira, J. H., R. L. Gonçalves, F. A. Lara, F. A. Dias, A. C. Gandara, R. F. Menna-Barreto, M. C. Edwards, F. R. Laurindo, M. A. Silva-Neto, M. H. Sorgine, and P. L. Oliveira. 2011. Blood meal-derived heme decreases ROS levels in the midgut of Aedes aegypti and allows proliferation of intestinal microbiota. PLoS Pathog. 7: e1001320.
27. Jung, S. H., C. J. Evans, C. Uemura, and U. Banerjee. 2005. The Drosophila lymph gland as a developmental model of hematopoiesis. Development 132: 2521-2533. (Pubitemid 40883253)
28. Strand, M. R. 2008. The insect cellular immune response. Insect Sci. 15: 1-15.
29. Bou Aoun, R., C. Hetru, L. Troxler, D. Doucet, D. Ferrandon, and N. Matt. 2011. Analysis of thioester-containing proteins during the innate immune response of Drosophila melanogaster. J. Innate Immun. 3: 52-64.
30. Cirimotich, C. M., J. L. Ramirez, and G. Dimopoulos. 2011. Native microbiota shape insect vector competence for human pathogens. Cell Host Microbe 10: 307-310.
31. Chen, X., S. Li, and S. Aksoy. 1999. Concordant evolution of a symbiont with its host insect species: molecular phylogeny of genus Glossina and its bacteriome-associated endosymbiont, Wigglesworthia glossinidia. J. Mol. Evol. 48: 49-58. (Pubitemid 29044250)
32. Hedges, L. M., J. C. Brownlie, S. L. O'Neill, and K. N. Johnson. 2008. Wolbachia and virus protection in insects. Science 322: 702.
33. Osborne, S. E., Y. S. Leong, S. L. O'Neill, and K. N. Johnson. 2009. Variation in antiviral protection mediated by different Wolbachia strains in Drosophila simulans. PLoS Pathog. 5: e1000656.
34. McMeniman, C. J., R. V. Lane, B. N. Cass, A. W. Fong, M. Sidhu, Y. F. Wang, and S. L. O'Neill. 2009. Stable introduction of a life-shortening Wolbachia infection into the mosquito Aedes aegypti. Science 323: 141-144.
35. Kambris, Z., P. E. Cook, H. K. Phuc, and S. P. Sinkins. 2009. Immune activation by life-shortening Wolbachia and reduced filarial competence in mosquitoes. Science 326: 134-136.
36. Moreira, L. A., I. Iturbe-Ormaetxe, J. A. Jeffery, G. Lu, A. T. Pyke, L. M. Hedges, B. C. Rocha, S. Hall-Mendelin, A. Day, M. Riegler, et al. 2009. A Wolbachia symbiont in Aedes aegypti limits infection with dengue, Chikungunya, and Plasmodium. Cell 139: 1268-1278.
37. Lindh, J. M., and M. J. Lehane. 2011. The tsetse fly Glossina fuscipes fuscipes (Diptera: Glossina) harbours a surprising diversity of bacteria other than symbionts. Antonie van Leeuwenhoek 99: 711-720.
38. Matova, N., and K. V. Anderson. 2006. Rel/NF-kappaB double mutants reveal that cellular immunity is central to Drosophila host defense. Proc. Natl. Acad. Sci. USA 103: 16424-16429. (Pubitemid 44715212)
39. Haine, E. R., Y. Moret, M. T. Siva-Jothy, and J. Rolff. 2008. Antimicrobial defense and persistent infection in insects. Science 322: 1257-1259.
40. Blandin, S. A., and E. A. Levashina. 2007. Phagocytosis in mosquito immune responses. Immunol. Rev. 219: 8-16. (Pubitemid 47390006)
41. Eleftherianos, I., M. Xu, H. Yadi, R. H. Ffrench-Constant, and S. E. Reynolds. 2009. Plasmatocyte-spreading peptide (PSP) plays a central role in insect cellular immune defenses against bacterial infection. J. Exp. Biol. 212: 1840-1848.
42. Mazmanian, S. K., and D. L. Kasper. 2006. The love-hate relationship between bacterial polysaccharides and the host immune system. Nat. Rev. Immunol. 6: 849-858. (Pubitemid 44631653)
43. Mazmanian, S. K., C. H. Liu, A. O. Tzianabos, and D. L. Kasper. 2005. An immunomodulatory molecule of symbiotic bacteria directs maturation of the host immune system. Cell 122: 107-118. (Pubitemid 40977944)
44. Clarke, T. B., K. M. Davis, E. S. Lysenko, A. Y. Zhou, Y. Yu, and J. N. Weiser. 2010. Recognition of peptidoglycan from the microbiota by Nod1 enhances systemic innate immunity. Nat. Med. 16: 228-231.
45. Aksoy, S. 2000. Tsetse - A haven for microorganisms. Parasitol. Today (Regul. Ed.) 16: 114-118.
46. Hosokawa, T., R. Koga, Y. Kikuchi, X. Y. Meng, and T. Fukatsu. 2010. Wolbachia as a bacteriocyte-associated nutritional mutualist. Proc. Natl. Acad. Sci. USA 107: 769-774.
47. Douglas, A. E. 2011. Lessons from studying insect symbioses. Cell Host Microbe 10: 359-367.
48. Nogge, G. 1976. Sterility in tsetse flies (Glossina morsitans Westwood) caused by loss of symbionts. Experientia 32: 995-996.
49. Akman, L., A. Yamashita, H. Watanabe, K. Oshima, T. Shiba, M. Hattori, and S. Aksoy. 2002. Genome sequence of the endocellular obligate symbiont of tsetse flies, Wigglesworthia glossinidia. Nat. Genet. 32: 402-407. (Pubitemid 35266115)