Sex and stripping: The key to the intimate relationship between Wolbachia and host?

Communicative and Integrative Biology

Volumn 3, Issue 2, 2010, Pages 110-115

  Negri, Ilaria ^a   Pellecchia, Marco ^b   Grève, Pierre ^c   Daffonchio, Daniele ^d   Bandi, Claudio ^e   Alma, Alberto ^a  

^a UNIVERSITY OF TURIN   (Italy)

^b UNIVERSITÀ CATTOLICA DEL SACRO CUORE   (Italy)

^c UNIVERSITÉ DE POITIERS   (France)

^d DISTAM Dipartimento di Scienze e Tecnologie Alimentari e Microbiologiche   (Italy)

^e UNIVERSITY OF MILAN   (Italy)

Author keywords

Arthropods; Ecdysis; Ecdysteroids; Hormonal pathways; Insulin; Nematodes; Wolbachia

Indexed keywords

ARTHROPODA; BACTERIA (MICROORGANISMS); BRUGIA MALAYI; HEXAPODA; MAMMALIA; NEMATODA; WOLBACHIA; WOLBACHIA PIPIENTIS;

EID: 77956139256     PISSN: None     EISSN: 19420889     Source Type: Journal    
DOI: 10.4161/cib.3.2.10520     Document Type: Review

References (69)

1. Werren JH, Baldo L, Clark ME. Wolbachia: master manipulators of invertebrate biology. Nat Rev Microbiol 2008; 6:741-51.
2. Bandi C, McCall JW, Genchi C, Corona S, Venco L, Sacchi L. Effects of tetracycline on the filarial worms Brugia pahangi and Dirofilaria immitis and their bacterial endosymbionts Wolbachia. Int J Parasitol 1999; 29:357-64.
3. Casiraghi M, McCall JW, Simoncini L, Kramer LH, Sacchi L, Genchi C, et al. Tetracycline treatment and sex-ratio distortion: a role for Wolbachia in the moulting of filarial nematodes? Int J Parasitol 2002; 32:1457-68.
4. Arumugam S, Pfarr KM, Hoerauf A. Infection of the intermediate mite host with Wolbachia-depleted Litomosoides sigmodontis microfilariae: impaired L1 to L3 development and subsequent sex-ratio distortion in adult worms. Int J Parasitol 2008; 38:981-7.
5. Ewer J. How the ecdysozoan changed its coat. PLoS Biology 2005; 3:1696-9.
6. Gilbert LI, Rybczynski R, Warren JT. Control and biochemical nature of the ecdysteroidogenic pathway. Annu Rev Entomol 2002; 47:883-916.
7. Ghedin E, et al. Draft genome of the filarial nematode parasite Brugia malayi. Science 2007; 317:1756-60.
8. Crossgrove K, Maina CV, Robinson-Rechavi M, Lochner MC. Orthologues of the Drosophila melanogaster E75 molting control gene in the filarial parasites Brugia malayi and Dirofilaria immitis. Mol Biochem Parasitol 2008; 157:92-7.
9. Motola DL, Cummins CL, Rottiers V, Sharma KK, Li TT, Li Y, et al. Identification of ligands for DAF-12 that govern dauer formation and reproduction in C. elegans. Cell 2006; 124:1209-23.
10. Höss S, Weltje L. Endocrine disruption in nematodes: effects and mechanisms. Ecotoxicology 2007; 16:15-28.
11. Bandi C, Trees AJ, Brattig N. Wolbachia in filarial nematodes: evolutionary aspects and implications for the pathogenesis and treatment of filarial diseases. Vet Parasitol 2001; 98:215-38.
12. Taylor MJ, Bandi C, Hoerauf A. Wolbachia bacterial endosymbionts of filarial nematodes. Adv Parasitol 2005; 60:245-84.
13. Foster J, et al. The Wolbachia genome of Brugia malayi: endosymbiont evolution within a human pathogenic nematode. PLoS Biol 2005; 3:121.
14. Brownlie JC, O'Neill SL. Wolbachia genomes: insights into an intracellular lifestyle. Curr Biol 2005; 15:507-9.
15. Iturbe-Ormaetxe I, O'Neill S. Wolbachia-host interactions: connecting phenotype to genotype. Curr Opin Microbiol 2007; 10:1-4.
16. Swevers L, Raikhel AS, Sappington TW, Shirk P, Iatrou K. Vitellogenesis and post-vitellogenic maturation of the insect ovarian follicle. In: Gilbert LI, Iatrou K, Gill SS, eds. Comprehensive Molecular Insect Science. Reproduction and Development. Oxford, UK: Elsevier Ltd 2005; 87-156.
17. Raikhel AS, Brown M, Belles X. Hormonal control of reproductive processes. In: Gilbert LI, Iatrou K, Gill SS, eds. Comprehensive Molecular Insect Science. Endocrinology. Oxford, UK: Elsevier Ltd 2005; 433-91.
18. Ganter GK, Walton KL, Merriman JO, Salmon MV, Brooks KM, Maddula S, Kravitz EA. Increased malemale courtship in ecdysone receptor deficient adult flies. Behav Genet 2007; 37:507-12.
19. De Loof A. Ecdysteroids: the overlooked sex steroids of insect? Males: the black box. Insect Science 2006; 13:325-38.
20. Schütt C, Nöthiger R. Structure, function and evolution of sex-determining systems in Dipteran insects. Development 2000; 127:667-77.
21. DeFalco T, Camara N, Le Bras S, Van Doren M. Nonautonomous sex determination controls sexually dimorphic development of the Drosophila gonad. Dev Cell 2008; 14:275-86.
22. Legrand JJ, Legrand-Hamelin E, Juchault P. Sex determination in Crustacea. Biol Rev 1987; 62:439-70.
23. Martin G, Juchault P, Legrand JJ. Mise en évidence d'un micro-organisme intracytoplasmique symbiote de l'oniscoïde Armadillidium vulgare Latreille dont la présence accompagne l'intersexualité ou la féminisation totale des mâles génétiques de la lignée thélygène. C R Acad Sc Paris 1973; 276:2313-6.
24. Rigaud T, Moreau J, Juchault P. Wolbachia infection in the terrestrial isopod Oniscus asellus: sex ratio distortion and effect on fecundity. Heredity 1999; 83:469-75.
25. Marcadé I, Souty-Grosset C, Bouchon D, Rigaud T, Raimond R. Mitochondrial DNA variability and Wolbachia infection in two sibling woodlice species. Heredity 1999; 83:71-8.
26. Bouchon D, Cordaux R, Grève P. Feminizing Wolbachia and evolution of sex determination in isopods. In: Bourtzis K, Miller TA, eds. Insect symbiosis. Boca Raton FL. Taylor and Francis Group LLC 2008; 273-94.
27. Hiroki M, Kato Y, Kamito T, Miura K. Feminization of genetic males by a simbiotic bacterium in a butterfly, Eurema hecabe (Lepidoptera: Pieridae). Naturwissenschaften 2002; 89:167-70.
28. Negri I, Pellecchia M, Mazzoglio PJ, Patetta, Alma A. Feminizing Wolbachia in Zyginidia pullula (Insecta, Hemiptera), a leafhopper with an XX/X0 sex-determination system. Proc R Soc B 2006; 273:2409-16.
29. Rigaud T, Juchault P. Sterile intersexuality in an isopod induced by the interaction between a bacterium (Wolbachia) and the environment. Can J Zool 1998; 76:493-9.
30. Narita S, Nomura M, Kageyama D. Naturally occurring single and double infection with Wolbachia strains in the butterfly Eurema hecabe: transmission efficiencies and population density dynamics of each Wolbachia strain. FEMS Microbiol Ecol 2007; 61:235-45.
31. Negri I, Franchini A, Gonella E, Daffonchio D, Mazzoglio PJ, Mandrioli M, Alma A. Unravelling the Wolbachia evolutionary role: the reprogramming of the host genomic imprinting. Proc R Soc B 2009; 276:2485-91.
32. Fujii T, Shimada T. Sex determination in the silkworm, Bombyx mori: a female determinant on the W chromosome and the sex-determining gene cascade. Semin Cell Dev Biol 2007; 18:379-88.
33. Cruz J, Mané Padròs D, Belleés X, Martìn D. Functions of the ecdysone receptor isoform-A in the hemimetabolous insect Blattella germanica revealed by systemic RNAi in vivo. Dev Biol 2006; 297:158-71.
34. Davis MB, Carney GE, Robertson AE, Bender M. Phenotypic analysis of EcR-A mutants suggests that EcR isoforms have unique functions during Drosophila development. Dev Biol 2005; 282:385-96.
35. Lobbia S, Niitsu S, Fujiwara H. Female-specific wing degeneration caused by ecdysteroid in the Tussock Moth, Orgyia recens: hormonal and developmental regulation of sexual dimorphism. J Insect Sci 2003; 3:1-7.
36. Juchault P, Legrand JJ. Croisement des néo-mâles expérimentaux chez Armadillidium vulgare Latr. (Crustacé Isopode Oniscoïde). Mise en évidence d'une hétérogamétie femelle. C R Acad Sci Paris 1972; 274:1387-9.
37. Martin G, Sorokine O, Moniatte M, Bulet P, Hetru C, Van Dorsselaer A. The structure of a glycosylated protein hormone responsible for sex determination in the isopod, Armadillidium vulgare. Eur J Biochem 1999; 262:727-36.
38. Juchault P, Legrand JJ. Mechanism of the refractory state of androgen hormone in Armadillidium vulgare Latr. (crustacean, isopod, oniscoid) harboring a feminizing bacteria. Gen Comp Endocrinol 1985; 60:463-7.
39. Ohira T, Hasegawa Y, Tominaga S, Okuno A, Nagasawa H. Molecular cloning and expression analysis of cDNAs encoding androgenic gland hormone precursors from two porcellionidae species, Porcellio scaber and P. dilatatus. Zoolog Sci 2003; 20:75-81.
40. Okuno A, Hasegawa Y, Ohira T, Katakura Y, Nagasawa H. Characterization and cDNA cloning of androgenic gland hormone of the terrestrial isopod Armadillidium vulgare. Biochem Biophys Res Commun 1999; 264:419-23.
41. Grève P, Braquart-Varnier C, Strub J-M, Félix C, Van Dorsselaer A, Martin G. The glycosylated androgenic hormone of the terrestrial isopod Porcellio scaber (Crustacea). Gen Comp Endocr 2004; 136:389-97.
42. Manor R, Weil S, Oren S, Glazer L, Aflalo ED, Ventura T, et al. Insulin and gender: an insulin-like gene expressed exclusively in the androgenic gland of the male crayfish. Gen Comp Endocrinol 2007; 150:326-36.
43. Okuno A, Hasegawa Y, Nagasawa H. Purification and proprieties of androgenic gland hormone from the terrestrial isopod Armadillidium vulgare. Zool Sci 1997; 14:837-42.
44. Barki A, Karplus I, Khalaila I, Manor R, Sagi A. Male-like behavioral patterns and physiological alterations induced by androgenic gland implantation in female crayfish. J Exp Biol 2003; 206:1791-7.
45. Manor R, Aflalo ED, Segall C, Weil S, Azulay D, Ventura T, Sagi A. Androgenic gland implantation promotes growth and inhibits vitellogenesis in Cherax quadricarinatus females held in individual compartments. Invertebr Reprod Dev 2004; 45:151-9.
46. Ventura T, Manor R, Aflalo ED, Weil S, Raviv S, Glazer L, Sagi A. Temporal silencing of an androgenic gland-specific insulin-like gene affecting phenotypical gender differences and spermatogenesis. Endocrinology 2009; 150:1278-86.
47. Nässel DR. Neuropeptides in the nervous system of Drosophila and other insects: multiple roles as neuromodulators and neurohormones. Progr Neurobiol 2002; 68:1-84.
48. Wu Q, Brown MR. Signaling and function on insuline-like peptides in insects. Annu Rev Entomol 2006; 51:1-24.
49. Okamoto N, Yamanaka N, Satake H, Saegusa H, Kataoka H, Mizoguchi A. An ecdysteroid-inducible insulin-like growth factor-like peptide regulates adult development of the silkmoth Bombyx mori. FEBS J 2009; 276:1221-32.
50. Truman JW. Steroid hormone secretion in insects comes of age. Proc Natl Acad Sci USA 2006; 24:8909-10.
51. De Loof A. Ecdysteroids, juvenile hormone and insect neuropeptides: recent successes and remaining major challenges. Gen Comp Endocrinol 2008; 155:3-13.
52. Böhni R, Riesgo-Escovar J, Oldham S, Brogiolo W, Stocker H, Andruss BF, et al. Autonomous control of cell and organ size by CHICO, a Drosophila homolog of vertebrate IRS1-4. Cell 1999; 97:865-75.
53. Richard DS, Rybczynski R, Wilson TG, Wang Y, Wayne ML, Zhou Y, et al. Insulin signaling is necessary for vitellogenesis in Drosophila melanogaster independent of the roles of juvenile hormone and ecdysteroids: female sterility of the chico1 insulin signaling mutation is autonomous to the ovary. J Insect Physiol 2005; 51:455-64.
54. Clark ME, Anderson CL, Cande J, Karr TL. Widespread prevalence of Wolbachia in laboratory stocks and the implications for Drosophila research. Genetics 2005; 170:1667-75.
55. Ikeya T, Broughton S, Alic N, Grandison R, Partridge L. The endosymbiont Wolbachia increases insulin/IGF-like signalling in Drosophila. Proc Biol Sci 2009; 276:3799-807.
56. Kageyama D, Traut W. Opposite sex-specific effects of Wolbachia and interference with the sex determination of its host Ostrinia scapulalis. Proc R Soc B 2003; 271:251-8.
57. Sakamoto H, Kageyama D, Hoshizaki S, Yshikawa Y. Sex specific death in the Asian corn borer moth (Ostrinia furnacalis) infected by Wolbachia occurs across larval development. Genome 2007; 50:645-52.
58. Kozlova T, Thummel CS. Essential roles for ecdysone signaling during Drosophila mid-embryonic development. Science 2003; 301:1911-4.
59. Gaziova I, Bonnette PC, Henrich VC, Jindra M. Cell-autonomous roles of the ecdysoneless gene in Drosophila development and oogenesis. Development 2004; 131:2715-25.
60. Warren JT, Petryk A, Marqués G, Jarcho M, Parvy J-P, Dauphin-Villemant C, et al. Molecular and biochemical characterization of two P450 enzymes in the ecdysteroidogenic pathway of Drosophila melanogaster. Proc Natl Acad Sci USA 2002; 17:11043-8.
61. Bentley JK, Veneti Z, Heraty J, Hurst GDD. The pathology of embryo death caused by the male-killing Spiroplasma bacterium in Drosophila nebulosa. BMC Biol 2007; 15:5-9.
62. Ankley G, et al. Overview of a workshop on screening methods for detecting potential (anti-) estrogenic/androgenic chemicals in wildlife. Environ Toxicol Chem 1998; 17:68-87.
63. Izumi N, Yanagibori R, Shigeno S, Sajiki J. Effects of bisphenol A on the development, growth and sex ratio of the housefly Musca domestica. Environ Toxicol Chem 2008; 27:1343-53.
64. Biddinger D, Hull L, Huang H, McPheron B, Loyer M. Sublethal effects of chronic exposure to tebufenozide on the development, survival and reproduction of the tufted apple bud moth (Lepidoptera: Tortricidae). J Econ Entomol 2006; 99:834-42.
65. Hahn T, Liess M, Schulz R. Effects of the hormone mimetic insecticide tebufenozide on Chironomus riparius larvae in two different exposure setups. Ecotox Environ Safe 2001; 49:171-8.
66. Dedeine F, Vavre F, Fleury F, Loppin B, Hochberg ME, Bouletreau M. Removing symbiotic Wolbachia bacteria specifically inhibits oogenesis in a parasitic wasp. Proc Natl Acad Sci USA 2001; 98:6247-52.
67. Moran NA, McCutcheon JP, Nakabach A. Genomics and evolution of heritable bacterial symbionts. Annu Rev Genet 2008; 42:165-90.
68. Weeks AR, Turelli M, Harcombe WR, 3rd, Reynolds KT, Hoffmann AA. From parasite to mutualist: rapid evolution of Wolbachia in natural populations of Drosophila. PLoS Biol 2007; 5:114.
69. Unckless RL, Boelio LM, Herren JK, Jaenike J. Wolbachia as populations within individual insects: causes and consequences of density variation in natural populations. Proc R Soc B 2009; 276:2805-11.