The cellular immune response of the pea aphid to foreign intrusion and symbiotic challenge

PLoS ONE

Volumn 7, Issue 7, 2012, Pages

  Schmitz, Antonin ^a,b,c   Anselme, Caroline ^a,b,c,e   Ravallec, Marc ^d   Rebuf, Christian ^a,b,c   Simon, Jean Christophe ^a   Gatti, Jean Luc ^a,b,c   Poirié, Marylène ^a,b,c  

^a CEMAGREF   (France)

^b CNRS   (France)

^c UNIVERSITÉ CÔTE D'AZUR   (France)

^d UNIV MONTPELLIER   (France)

^e UNIVERSITÉ DE PICARDIE JULES VERNE   (France)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; BLOOD CELL; BLOOD CLOTTING; BUCHNERA APHIDICOLA; CELL ADHESION; CELLULAR DISTRIBUTION; CELLULAR IMMUNITY; CLONE; CONTROLLED STUDY; DIGITAL IMAGING; ESCHERICHIA COLI; FOREIGN BODY; GRANULOCYTE; HAMILTONELLA DEFENSA; HEMOLYMPH; IMMUNOCOMPETENT CELL; INTERNALIZATION; NONHUMAN; PEA APHID; PHAGOCYTOSIS; PHAGOLYSOSOME; PLASMA CELL; PROHEMOCYTE; REGIELLA INSECTICOLA; SERRATIA SYMBIOTICA; SPHERULOCYTE; SYMBIONT; SYMBIOSIS; WAX CELL;

ANIMALS; APHIDS; BLOOD COAGULATION; CELL ADHESION; CELL COUNT; ESCHERICHIA COLI; FEMALE; FOREIGN BODIES; GRANULOCYTES; HEMOCYTES; IMMUNITY, CELLULAR; MICROSPHERES; PHAGOCYTOSIS; SPECIES SPECIFICITY; SYMBIOSIS;

ACYRTHOSIPHON PISUM; APHIDIDAE; BUCHNERA APHIDICOLA; CANDIDATUS HAMILTONELLA DEFENSA; CANDIDATUS REGIELLA INSECTICOLA; CANDIDATUS SERRATIA SYMBIOTICA; ESCHERICHIA COLI;

EID: 84864415294     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0042114     Document Type: Article

References (69)

1. Broderick NA, Welchman DP, Lemaitre B, ((2009)) Recognition and response to microbial infection in Drosophila. In: Insect Infection and Immunity. Rolff J, Reynolds S, editors. Oxford University Press, USA pp. 13--33.
2. Cerenius L, Kawabata S-I, Lee BL, Nonaka M, Söderhäll K, ((2010)) Proteolytic cascades and their involvement in invertebrate immunity. Trends Biochem Sci 35:: 575--583.
3. Nappi A, Poirié M, Carton Y, ((2009)) The Role of melanization and cytotoxic by-products in the cellular immune response of Drosophila against parasitic wasps. Adv Parasitol 70:: 99--121.
4. Zou Z, Evans JD, Lu Z, Zhao P, Williams M, et al. ((2007)) Comparative genomic analysis of the Tribolium immune system. Genome Biol 8:: R177.
5. Evans JD, Aronstein A, Chen YP, Hetru C, Imler J-L, et al. ((2006)) Immune pathways and defence mechanisms in honey bees Apis mellifera. Insect Mol Biol 15(5):: 645--56.
6. The International Aphid Genomics Consortium ((2010)) Genome sequence of the pea aphid Acyrthosiphon pisum. PLoS Biol 8:: e1000313.
7. Gerardo NM, Altincicek B, Anselme C, Atamian H, Barribeau SM, et al. ((2010)) Immunity and other defenses in pea aphids, Acyrthosiphon pisum. Genome Biol 11:: R21.
8. Altincicek B, Gross J, Vilcinskas A, ((2008)) Wounding-mediated gene expression and accelerated viviparous reproduction of the pea aphid Acyrthosiphon pisum. Insect Mol Biol 17:: 711--716.
9. Gross R, Vavre F, Heddi A, Hurst GDD, Zchori-Fein E, et al. ((2009)) Immunity and symbiosis. Mol Microbiol 73:: 751--759.
10. Hurst GDD, Darby AC, ((2009)) The inherited microbiota of arthropods, and their importance in understanding resistance and immunity. In: Insect Infection and Immunity. Rolff J, Reynolds SE, editors. Oxford University Press pp. 119--137.
11. Welchman DP, Aksoy S, Jiggins F, Lemaitre B, ((2009)) Insect immunity: from pattern recognition to symbiont-mediated host defense. Cell Host Microbe 6:: 107--114.
12. Fytrou A, Schofield PG, Kraaijeveld AR, Hubbard SF, ((2006)) Wolbachia infection suppresses both host defence and parasitoid counter-defence. Proc R Soc Lond B Biol Sci 273:: 791--796.
13. Braquart-Varnier C, Lachat M, Herbinière J, Johnson M, Caubet Y, et al. ((2008)) Wolbachia mediate variation of host immunocompetence. PLoS ONE 3:: e3286.
14. Hedges LM, Brownlie JC, O'Neill SL, Johnson KN, ((2008)) Wolbachia and virus protection in insects. Science 322:: 702.
15. Anselme C, Pérez-Brocal V, Vallier A, Vincent-Monegat C, Charif D, et al. ((2008)) Identification of the weevil immune genes and their expression in the bacteriome tissue. BMC Biol 6:: 43.
16. Hypsa V, Grubhoffer L, ((1997)) Two hemocyte populations in Triatoma infestans: ultrastructural and lectin-binding characterization. Folia Parasitol 44:: 62--70.
17. Weiss BL, Wu Y, Schwank JJ, Tolwinski NS, Aksoy S, ((2008)) An insect symbiosis is influenced by bacterium-specific polymorphisms in outer-membrane protein A. Proc Natl Acad Sci USA 105:: 15088--15093.
18. Login FH, Balmand S, Vallier A, Vincent-Monégat C, Vigneron A, et al. ((2011)) Antimicrobial peptides keep insect endosymbionts under control. Science 334:: 362--365.
19. Scarborough CL, Ferrari J, Godfray HCJ, ((2005)) Aphid protected from pathogen by endosymbiont. Science 310:: 1781.
20. Oliver KM, Moran NA, Hunter MS, ((2005)) Variation in resistance to parasitism in aphids is due to symbionts not host genotype. Proc Natl Acad Sci USA 102:: 12795--12800.
21. Fukatsu T, Nikoh N, Kawai R, Koga R, ((2000)) The secondary endosymbiotic bacterium of the Pea Aphid Acyrthosiphon pisum (Insecta: Homoptera). Appl Environ Microbiol 66:: 2748--2758.
22. Oliver KM, Degnan PH, Burke GR, Moran NA, ((2010)) Facultative symbionts in aphids and the horizontal transfer of ecologically important traits. Annu Rev Entomol 55:: 247--266.
23. Boiteau G, Perron JM, ((1976)) Etude des hémocytes de Macrosiphum euphorbiae (Thomas) (Homoptera: Aphididae). Can J Zool 54:: 228--234.
24. Laughton AM, Garcia JR, Altincicek B, Strand MR, Gerardo NM, ((2011)) Characterisation of immune responses in the pea aphid, Acyrthosiphon pisum. J Insect Physiol 57:: 830--839.
25. Bensadia F, Boudreault S, Guay J-F, Michaud D, Cloutier C, ((2006)) Aphid clonal resistance to a parasitoid fails under heat stress. J Insect Physiol 52:: 146--157.
26. Chen S, Edwards J, ((1972)) Observations on the structure of secretory cells associated with aphid cornicles. Z Zellforsch Mikrosk Anat 130:: 312--317.
27. Swanson JA, Baer SC, ((1995)) Phagocytosis by zippers and triggers. Trends Cell Biol 5:: 89--93.
28. Hollande A, ((1911)) Etude histologique comparée du sang des insectes à hémorrhée et des insectes sans hémorrhée. Arch Zool 5:: 283--323.
29. Behura BK, Dash PA, ((1978)) Haemocytes of the common maize aphid, Rhopalosiphum maidis (Fitch) (Homoptera Aphididae) in relation to the action of six insecticides. J Entomol Res 2:: 199--202.
30. Behera MK, Behera R, Patro B, ((1999)) Studies on the haemocytes of the common chrysanthemum aphid, Macrosiphoniela sanborni. Indian J Entomol 61:: 51--55.
31. Patro B, Toda S, Komazaki S, ((2005)) Studies on the haemocytes of Aphis gossypii glover (Aphididae: homoptera). Indian J Agric Res 39:: 192--197.
32. Bohidar K, Behura BK, ((1987)) Haemocytes of Rhopalosiphum nymphaeae (l.) (Aphididae: homoptera). J Aphidol 1:: 42--46.
33. Behura B, Bohidar K, ((1983)) On the haemocytes of four species of aphids. Pranikee 4:: 376--379.
34. Outreman Y, Le Ralec A, Plantegenest M, Chaubet B, Pierre JS, ((2001)) Superparasitism limitation in an aphid parasitoid: cornicle secretion avoidance and host discrimination ability. J Insect Physiol 47:: 339--348.
35. Bowers W, Nault L, Webb R, SR D, ((1972)) Aphid alarm pheromone: isolation, identification, synthesis. Science 177:: 1121--1122.
36. Wigglesworth V, ((1988)) The source of lipids and polyphenols for the insect cuticle: The role of fat body, oenocytes and oenocytoids. Tissue & Cell 20:: 919--932.
37. Gregoire C, ((1951)) Blood Coagulation in Arthropods: II. Phase Contrast Microscopic Observations on Hemolymph Coagulation in Sixty-one Species of Insects. Blood 6:: 1173--1198.
38. Brehelin M, Zachary D, Hoffmann JA, ((1978)) A comparative ultrastructural study of blood cells from nine insect orders. Cell Tiss Res 195:: 45--57.
39. Schmidt O, Söderhäll K, Theopold U, Faye I, ((2010)) Role of adhesion in arthropod immune recognition. Annu Rev Entomol 55:: 485--504.
40. Labrosse C, Eslin P, Doury G, Drezen JM, Poirié M, ((2005)) Haemocyte changes in D. melanogaster in response to long gland components of the parasitoid wasp Leptopilina boulardi: a Rho-GAP protein as an important factor. J Insect Physiol 51:: 161--170.
41. Strand MR, ((2008)) Insect hemocytes and their role in immunity. In Insect immunology Beckage NE, (Elsevier) pp. 25--47.
42. Carver M, Woolcock L, ((1985)) Interactions between Acyrthosiphon kondoi (Homoptera: Aphidoidea) and Aphelinus asychis (Hymenoptera: Chalcidoidea) and other parasites and hosts. Entomophaga 30:: 193--198.
43. Carton Y, Poirié M, Nappi AJ, ((2008)) Insect immune resistance to parasitoids. Insect Sci 15:: 67--87.
44. Henter HJ, Via S, ((1995)) The potential for coevolution in a host-parasitoid system. II. Genetic variation within a population of wasps in the ability to parasitize an aphid population. Evolution 49:: 439--445.
45. Kapranas A, Federici B, Luck RF, Johnson J, ((2009)) Cellular immune response of brown soft scale Coccus hesperidum L. (Hemiptera: Coccidae) to eggs of Metaphycus luteolus Timberlake (Hymenoptera: Encyrtidae). Biol Control 48:: 1--5.
46. Howell L, Sampson CJ, Xavier MJ, Bolukbasi E, Heck MM, et al. ((2012)) A directed miniscreen for genes involved in the Drosophila anti-parasitoid immune response. Immunogenetics 64(2):: 155--161.
47. Altincicek B, Ter Braak B, Laughton AM, Udekwu KI, Gerardo NM, ((2011)) Escherichia coli K-12 pathogenicity in the pea aphid, Acyrthosiphon pisum, reveals reduced antibacterial defense in aphids. Dev Comp Immunol 35:: 1091--1097 doi:017.
48. Grenier A-M, Duport G, Pagès S, Condemine G, Rahbé Y, ((2006)) The phytopathogen Dickeya dadantii (Erwinia chrysanthemi 3937) is a pathogen of the pea aphid. Appl Environ Microbiol 72:: 1956--1965.
49. Darby AC, Chandler SM, Welburn SC, Douglas AE, Al DET, et al. ((2005)) Aphid-symbiotic bacteria cultured in insect cell lines. Appl Environ Microbiol 71:: 4833--4839.
50. Degnan PH, Yu Y, Sisneros N, Wing Ra, Moran NA, ((2009)) Hamiltonella defensa, genome evolution of protective bacterial endosymbiont from pathogenic ancestors. Proc Natl Acad Sci USA 106:: 9063--9068.
51. Degnan PH, Leonardo TE, Cass BN, Hurwitz B, Stern D, et al. ((2009)) Dynamics of genome evolution in facultative symbionts of aphids. Environ Microbiol 12:: 2060--2069.
52. Burke GR, Moran NA, ((2011)) Massive genomic decay in Serratia symbiotica, a recently evolved symbiont of aphids. Genome Biol Evol 3:: 195--208.
53. Dale C, Young SA, Haydon DT, Welburn SC, ((2001)) The insect endosymbiont Sodalis glossinidius utilizes a type III secretion system for cell invasion. Proc Natl Acad Sci USA 98:: 1883--1888.
54. Toh H, Weiss B, Perkin S, Yamashita A, Oshima K, et al. ((2006)) Massive genome erosion and functional adaptations provide insights into the symbiotic lifestyle of Sodalis glossinidius in the tsetse host. Genome Res 16:: 149--156.
55. Abel J, Goldmann O, Ziegler C, Höltje C, Smeltzer M, et al. ((2011)) Staphylococcus aureus evades the extracellular antimicrobial activity of mast cells by promoting its own uptake. J Innate Immun 3:: 95--507.
56. Fields P, Swanson R, Haidaris C, Heffron F, ((1986)) Mutants of Salmonella typhimurium that cannot survive within the macrophage are avirulent. Proc Natl Acad Sci USA 83:: 5189--5193.
57. Oliver KM, Campos J, Moran NA, Hunter MS, ((2008)) Population dynamics of defensive symbionts in aphids. Proc R Soc Lond B Biol Sci 275:: 293--299.
58. Simon J-C, Boutin S, Tsuchida T, Koga R, Le Gallic J-F, et al. ((2011)) Facultative symbiont infections affect aphid reproduction. PLoS ONE 6:: e21831.
59. Chevalier F, Herbinière-Gaboreau J, Bertaux J, Raimond M, Morel F, Bouchon D, Grève P, Braquart-Varnier C, ((2011)) The immune cellular effectors of terrestrial isopod Armadillidium vulgare: Meeting with their invaders, Wolbachia. PLoS One 6 (4): e18531.
60. Wilkinson TL, Fukatsu T, Ishikawa H, ((2003)) Transmission of symbiotic bacteria Buchnera to parthenogenetic embryos in the aphid Acyrthosiphon pisum (Hemiptera: Aphidoidea). Arthropod Struct Dev 32:: 241--245.
61. Koga R, Meng X, Tsuchida T, Fukatsu T, ((2012)) Cellular mechanism for selective vertical transmission of an obligate insect symbiont at the bacteriocyte-embryo interface. Proc Natl Acad Sci USA DOI: 10.1073/pnas.1119212109.
62. Douglas AE, ((1998)) Nutritional interactions in insect-microbial symbioses: aphids and their symbiotic bacteria Buchnera. Annu Rev Entomol 43:: 17--37.
63. Douglas AE, Bouvaine S, Russell RR, ((2011)) How the insect immune system interacts with an obligate symbiotic bacterium. Proc R Soc Lond B Biol Sci 278:: 333--338.
64. Shigenobu S, Watanabe H, Hattori M, Sakaki Y, Ishikawa H, ((2000)) Genome sequence of the endocellular bacterial symbiont of aphids Buchnera sp. Nature 407:: 81--86.
65. Weiss BL, Wang J, Aksoy S, ((2011)) Tsetse immune system maturation requires the presence of obligate symbionts in larvae. PLoS Biol 9:: e1000619.
66. Koga R, Tsuchida T, Sakurai M, Fukatsu T, ((2007)) Selective elimination of aphid endosymbionts: effects of antibiotic dose and host genotype, and fitness consequences. FEMS Microbiol Ecol 60:: 229--239.
67. Ling E, Yu X-Q, ((2005)) Prophenoloxidase binds to the surface of hemocytes and is involved in hemocyte melanization in Manduca sexta. Insect Biochem Mol Biol 35:: 1356--1366.
68. Menschik Z, ((1953)) Nile Blue Histochemical Method For Phospholipids. Stain Technology 28:: 13--18.
69. Tsuchida T, Koga R, Meng XY, Matsumoto T, Fukatsu T, ((2005)) Characterization of a facultative endosymbiotic bacterium of the pea aphid Acyrthosiphon pisum. Microbial Ecol 49:: 126--133.