'Insects do not have sex hormones': A myth?

General and Comparative Endocrinology

Volumn 111, Issue 3, 1998, Pages 245-260

  De Loof, Arnold ^a   Huybrechts, Roger ^a  

^a UNIVERSITY OF LEUVEN   (Belgium)

Author keywords

Androgenic hormone; Dax1; Ecdysone; FTZ F1; Juvenile hormone; Sex determination; SF 1; Sry

Indexed keywords

ANDROGEN; ECDYSONE; JUVENILE HORMONE; PEPTIDE HORMONE; SEX HORMONE; VITELLOGENIN;

BEETLE; CUTICLE; DROSOPHILA; GENE EXPRESSION; LOCUST; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; REVIEW; SEX DETERMINATION; SEX DIFFERENTIATION; VITELLOGENESIS;

EID: 0031877523     PISSN: 00166480     EISSN: 10956840     Source Type: Journal    
DOI: 10.1006/gcen.1998.7101     Document Type: Review

References (82)

1. Berta P., Hawkins J. R., Sinclair A. H., Taylor A., Griffiths B. L., Goodfellow P. N., Fellous M. Genetic evidence equatingSRY. Nature. 348:1990;448-450.
2. Borovsky D., Carlson D. A., Griffin P. R., Shabanowitz J., Hunt D. F. Mass spectrometry and characterization ofAedes aegypti. Insect Biochem. Mol. Biol. 23:1993;703-712.
3. Briers T., De Loof A. Molting hormone activity inSarcophaga bullata. Int. J. Invertebr. Reprod. 2:1980;363-372.
4. Briers T., De Loof A. Mounting hormone activity in the adult Colorado potato beetle in relation to metamorphosis and reproduction. Int. J. Invertebr. Reprod. 2:1981;363-372.
5. 3Sarcophaga bullata. Gen. Comp. Endocrinol. 52:1983a;379-387.
6. Briers T., Van Beek E., De Loof A. Ecdysteroid activity during metamorphosis and in male and female adults of four blowfly species. Comp. Biochem. Physiol. 74A:1983b;521-524.
7. Brown M. R., Graf R., Swiderek K. M., Fendley D., Stracker T. H., Champagne D. E., Lea A. O. Identification of a steroidogenic neurohormone in female mosquitoes. J. Biol. Chem. 273:1998;3967-3971.
8. Bylemans D. Isolation, Characterization and Mode of Action of Two Novel Folliculostatins from the Grey FleshflyNeobellieria bullata. 1994;K. U. Leuven, Belgium.
9. Bylemans D., Borovsky D., Hunt D. F., Shabanowitz J., Grauwels L., De Loof A. Sequencing and characterization of trypsin modulating oostatic factor (TMOF) from the ovaries of the grey fleshfly,NeobellieriaSarcophagabullata. Regul. Peptides. 50:1994;61-72.
10. Bylemans D., Proost P., Samyn B., Borovsky D., Grauwels L., Huybrechts R., Van Damme J., Van Beeumen J., De Loof A. Neb-colloostatin, a second folliculostatin of the grey fleshflyNeobellieria bullata. Eur. J. Biochem. 228:1995;45-49.
11. Charniaux-Cotton H. Découverte chez un crustacé amphipode (Orchestia gammarella. C. R. Acad. Sci. Paris. 239:1954;780-782.
12. Darvas B., Székacs A., Fonagy A., Szési M., Toth I. Progesterone inPeriplaneta americanaNeobellieria bullata. Gen. Comp. Endocrinol. 107:1997;450-460.
13. De Clerck D., De Loof A. Effect of dietary ecdysterone on protein ingestion and copulatory behavior of the blowfly,Sarcophaga bullata. Physiol. Entomol. 8:1983;243-249.
14. De Loof A. The impact of the discovery of vertebrate-type steroids and peptide hormone-like substances in insects. Entomol. Exp. Appl. 45:1987;105-113.
15. De Loof A., Bylemans D., Schoofs L., Janssen I., Spittaels K., Vanden Broeck J., Huybrechts R., Borovsky D., Hua Y.-J., Koolman J., Sower S. Folliculostatins, gonadotropins, and a model for control of growth in the grey fleshfly,NeobellieriaSarcophagabullata. Insect Biochem. Mol. Biol. 25:1995;661-667.
16. De Loof A., Huybrechts R., Briers T. Do insects have steroid sex hormones and do compounds with juvenile hormone activity occur in vertebrates. Ann. Soc. R. Zool. Belg. 110:1981;179-184.
17. De Loof A., Vanden Broeck J., Janssen I. Hormones and the cytoskeleton of animals and plants. Int. Rev. Cytol. 166:1996;1-58.
18. De Loof A., Wei Z., Huybrechts R., Gijbels J., Verhaert P. The ecdysoid RH5849 induces yolk polypeptide synthesis in male flies. Invertebr. Reprod. Dev. 31:1997;69-74.
19. Dhadialla T. S., Wyatt G. R. Juvenile hormone-dependent vitellogenin synthesis inLocusta migratoria. Dev. Biol. 96:1983;436-444.
20. Don-Wheeler G., Engelmann F. Vitellogenin synthesis in the female and male cockroach.Leucophaea maderae. Am. Zool. 29:1989;49A.
21. Don-Wheeler G., Engelmann F. The female- and male-produced vitellogenins ofLeucophaea maderae. J. Insect Physiol. 37:1991;896-882.
22. Edwards G. C., Braun R. P., Wyatt G. R. Induction of vitellogenin synthesis inLocusta migratoria. J. Insect Physiol. 39:1993;609-614.
23. Eicher E. M. Sex and trinucleotide repeats. Nature Genet. 6:1994;221-223.
24. Fuller M. T. Spermatogenesis. The Development ofDrosophila melanogaster. 1993;Cold Spring Harbor Laboratory Press, Cold Spring Harbor. p. 71-147.
25. Gilbert S. F. Developmental Biology. 1997;Sinauer, Sunderland.
26. Girardie J., Girardie A. Lom OMP, a putative ecdysiotropic factor for the ovary inLocusta migratoria. J. Insect Physiol. 42:1996;215-221.
27. Girardie J., Girardie A., Huet J. C. Amino acid sequence of locust neuroparsins. FEBS Lett. 245:1989;4-8.
28. Girardie J., Geoffre S., Girardie A. Arguments for an ecdysiotropic activity of the ovary maturating parsin ofLocusta migratoria. Konopinska D. Insects: Chemical and Environmental Aspects. 1995;191-197 ISBN, Wroclaw.
29. Girardie J., Geoffre S., Delbecque J.-P., Girardie A. Arguments for two distinct gonadotropic activities triggered by different domains of the ovary maturating parsin ofLocusta migratoria. J. Insect Physiol. 1998a.
30. Girardie J., Huet J. C., Atay Kadiri Z., Ettaouil S., Delbecque J.-P., Fournier B., Pernollet J.-C., Girardie A. Isolation, physical characterization and sequence termination of neuroparsins and ovary maturating parsins ofSchistocerca gregaria. Insect Biochem. Mol. Biol. 1998b.
31. Girardie J., Richard O., Girardie A. Detection of vitellogenin in the haemolymph of larval female locusts (Locusta migratoria. J. Insect Physiol. 42:1996;107-113.
32. Gnessi L., Fabbri A., Spera G. Gonadal peptides as mediators of development and functional control of the testis: An integrated system with hormones and local environment. Endocr. Rev. 18:1997;541-609.
33. Gu S. H., Tsai R. S., Chow Y. S., Lin F. J. Sexual dimorphism in developmental rate and ecdysteroid titre inOrgyia postica. J. Insect Physiol. 38:1992;1043-1049.
34. Hale A. J., Smith C. A., Sutherland L. C., Stoneman V. E., Longthorne V. L., Culhane A. C., Williams G. T. Apoptosis: Molecular regulation of cell death. Eur. J. Biochem. 236:1996;1-26.
35. Handler A. M. Ecdysteroid titers during pupal and adult development inDrosophila melanogaster. Dev. Biol. 93:1982;73-82.
36. Hua Y.-J., Bylemans D., Koolman J., De Loof A. Inhibition of ecdysone biosynthesis in flies by a hexapeptide isolated from vitellogenic ovaries. Mol. Cell. Endocrinol. 104:1994;R1-R4.
37. Huybrechts R., De Loof A. Induction of vitellogenin synthesis in maleSarcophaga bullata. J. Insect Physiol. 23:1977;1359-1362.
38. Huybrechts R., De Loof A. Similarities in vitellogenin and vitellogenin synthesis within the generaSarcophaga, Calliphora, PhormiaLucilia. Comp. Biochem. Physiol. 72B:1982;339-342.
39. Jäger R. J., Anvret M., Hall K., Scherer G. A human XY female with a frameshift mutation in the candidate testis-determining geneSRY. Nature. 348:1990;452-454.
40. Katoh-Fukui Y., Tsuchiya R., Shiroishi T., Nakahara Y., Hashimoto N., Noguchi K., Higashinakagawa T. Male-to-female sex reversal inM33. Nature. 393:1998;688-692.
41. Koolman J., Scheller K., Bodenstein D. Ecdysteroids in the adult male blowflyCalliphora vicina. Experientia. 35:1979;134-135.
42. Koopman P., Gubbay J., Vivian N., Goodfellow P., Lovell-Badge R. Male development of chromosomally female mice transgenic forSry. Nature. 351:1991;117-121.
43. Koopman P., Münsterberg A., Capel B., Vivian N., Lovell-Badge R. Expression of a candidate sex-determining gene during mouse testsis differentiation. Nature. 348:1990;450-452.
44. Kozma R., Bownes M. Yolk induction in males of severalDrosophila. Insect Biochem. 16:1986;263-271.
45. Lagueux M., Hirn M., Hoffmann J. A. Ecdysone during ovarian development inLocusta migratoria. J. Insect Physiol. 23:1977;109-119.
46. Lagueux M., Harry P., Hoffmann J. A. Ecdysteroids are bound to vitellin in newly laid eggs ofLocusta. Mol. Cell Endocrinol. 24:1981;325-338.
47. Loeb M. J., Kochansky J., Wagner R. M., Woods C. W. Structure-function alnalysis of Lymantria testis ecdysiotropin: A search for the active core. Arch. Insect Biochem. Physiol. 38:1998;11-18.
48. Loeb M. J., Wagner R. M., Woods C. W., Gelman D. G., Harrison D., Bel R. A. Naturally occurring analogs ofLymantria dispar. Arch. Insect Biochem. Physiol. 36:1997;37-50.
49. Martin G., Juchault P., Legrand J. J. Mise en évidence d'un micro-organisme intracytoplasmique symbiote de l'oniscoïdeArmadillidium vulgare. C. R. Acad. Sci. Paris. 276:1973;2313-2316.
50. Martin G., Sorokine O., Moniatte M., Vandorsselaer A. The androgenic hormone of the crustacean IsopodArmadillidium vulgare. Ann. N.Y. Acad. Sci. 839:1998;111-117.
51. Mundall E. C., Tobe S. S., Stay B. Induction of vitellogenin and growth of implanted oocytes in male cockroaches. Nature. 282:1979;97-98.
52. Naisse J. Contrôle endocrinien de la différenciation sexuelle chez l'insecteLampyris noctiluca. Arch. Biol. 77:1966a;139-201.
53. Naisse J. Contrôle endocrinien de la différenciation sexuelle chez l'insecteLampyris noctiluca. Gen. Comp. Endocrinol. 7:1966b;85-104.
54. Naisse J. Contrôle endocrinien de la différenciation sexuelle chez l'insecteLampyris noctiluca. Gen. Comp. Endocrinol. 7:1966c;105-110.
55. Naisse J. Rôle des neurohormones dans la différenciation sexuelle deLampyris noctiluca. J. Insect Physiol. 15:1969;877-892.
56. Parker K. L., Schimmer B. P. Steroidogenic Factor 1: A key determinant of endocrine development and function. Endocr. Rev. 18:1997;361-377.
57. Parkhurst S. M., Meneely P. M. Sex determination and dosage compensation: lessons from flies and worms. Science. 264:1994;924-932.
58. Quack S., Fretz A., Spindler-Barth M., Spindler K. Receptor affinities and biological responses of nonsteroidal agonists on the epithelial cell line fromChironomus tentans. Eur. J. Entomol. 92:1995;341-347.
59. Raymond C. S., Shamu C. E., Shen M. M., Seifert K. J., Hirsch B., Hodgkin J., Zarkower D. Evidence for evolutionary conservation of sex-determining genes. Nature. 391:1998;691-694.
60. Richards A. Hormonal control of gene expression in the ovary. Endocr. Rev. 15:1994;725-751.
61. Schafer A. J., Goodfellow P. N. Sex determination in humans. BioEssays. 18:1996;955-963.
62. Schoofs L., Veelaert D., De Loof A., Huybrechts R., Isaac Z. Immunocytochemical distribution of angiotensin I-converting enzyme-like immunoreactivity in the brain and testis of insects. Brain Res. 785:1998;215-227.
63. Schoofs L., Spittaels K., Janssen I., Devreese B., Van Beeumen J., De Loof A. Isolation of a peptide that stimulates cAMP production in the ovaries ofNeobellieria bullata. Konopinskaet al. D. Insects: Chemical, Physiological, and Environmental Aspects. 1995;155-160 Wydawnictwa Uniwerssytetu Wroclawskiego.
64. Shen M. M., Hodgkin J. mab-3,C. elegans. Cell. 54:1988;1019-1031.
65. Sinclair A. H., Berta P., Palmer M. S., Hawkins J. R., Griffiths B. L., Smith M. J., Foster J. W., Frischauf A-M., Lovell-Badge R., Goodfellow P. N. A gene from the human sex determining region encodes a protein with homology to a conserved DNA-binding motif. Nature. 346:1990;240-244.
66. Spittaels K., Devreese B., Schoofs L., Neven H., Janssen I., Grauwels L., Van Beeumen J., De Loof A. Isolation and identification of a cAMP generating peptide from the flesh fly,Neobellieria bullata. Arch. Insect Biochem. Physiol. 31:1996;135-147.
67. Spittaels K., Verhaert P., Shaw C., Johnston R. N., Devreese B., Van Beeumen J., De Loof A. Insect Neuropeptide F (NPF)-related peptides: isolation from Colorado Potato beetle (Leptinotarsa decemlineata. Insect Biochem. Mol. Biol. 26:1996;375-382.
68. Staub N. L., De Beer M. The role of androgens in female vertebrates. Gen. Comp. Endocrinol. 108:1997;1-24.
69. Swain A., Narvaez V., Burgoyne P., Camerino G., Lovell-Badge R. Dax1Sry. Nature. 391:1998;761-767.
70. Swevers L., Lambert J. G. D., De Loof A. Synthesis and metabolism of vertebrate-type steroids by tissues of insects: A critical evaluation. Experientia. 47:1991a;687-698.
71. 1918Locusta migratoria. Gen. Comp. Endocrinol. 84:1991b;237-248.
72. Talbot W. S., Swyryd E. A., Hogness D. S. Drosophila. Cell. 73:1993;1323-1337.
73. Tamarelle M., Girardie J. Immunogold detection of two neurohormones: the locust ovary maturating parsin and neuroparsin. Neurocytology. 23:1994;393-399.
74. Tips A., Schoofs L., Paemen L., Hendrickx K., De Loof A. False positive immunostaining ofLocusta. Gen. Comp. Endocrinol. 106:1997;231-240.
75. Ueda H., Sonoda S., Brown J. L., Scott M. P., Wu C. A sequence specific DNA-binding protein that activatesfushi tarazu. Genes Dev. 4:1990;624-635.
76. Wagner R. M., Loeb M. J., Kochansky J. P., Gelman D. B., Lusby W. R., Bell R. A. Identification and characterization of an ecdysiotropic peptide from brain extracts of the Gypsy Moth,Lymantria dispar. Arch. Insect Biochem. Physiol. 34:1997;175-189.
77. White E. Life, death, and the pursuit of apoptosis. Genes Dev. 10:1996;1-15.
78. Wing K. D. RH-5849, a nonsteroidal ecdysone agonist: Effects on aDrosophila. Science. 241:1988;467-469.
79. Wünsch S., Schneider S., Schwab A., Oberleiter H. 20-OH-ecdysone swells nuclear volume by alkalinization in salivary glands ofDrosophila melanogaster. Cell Tissue Res. 274:1993;145-151.
80. Wyatt G. R. Vitellogenin synthesis and the analysis of juvenile hormone action in locust fat body. Can. J. Zool. 66:1988;2600-2610.
81. Wyatt G. R., Chin B. C., Cook K. E., Kanost M. R., Zhang J. Z. Juvenile hormone analog and injection effects on locust hemolymph protein synthesis. Arch. Insect Biochem. Physiol. 20:1992;167-180.
82. Yao T.-P., Forman B. M., Jiang Z., Cherbas L., Chen J. D., McKeown M., Cherbas P., Evans R. M. Functional ecdysone receptor is the product of EcR and Ultraspiracle genes. Nature. 366:1993;476-679.