The mode of action of juvenile hormone and ecdysone: Towards an epi-endocrinological paradigm?

General and Comparative Endocrinology

Volumn 188, Issue 1, 2012, Pages 35-45

  De Loof, Arnold ^a   Boerjan, Bart ^a   Ernst, Ulrich R ^a   Schoofs, Liliane ^a  

^a UNIVERSITY OF LEUVEN   (Belgium)

Author keywords

Accessory glands; Chromatin modification; Epi endocrinology; Insect development; Insect hormones; Reprogramming

Indexed keywords

DNA METHYLTRANSFERASE; DNA METHYLTRANSFERASE 1; DNA METHYLTRANSFERASE 2; DNA METHYLTRANSFERASE 3; ECDYSONE; JUVENILE HORMONE; MESSENGER RNA; MICRORNA; UNCLASSIFIED DRUG;

AGING; BOMBYX; CECROPIA MOTH; CHROMATIN ASSEMBLY AND DISASSEMBLY; COLORADO POTATO BEETLE; DNA METHYLATION; DNMT1 GENE; DNMT2 GENE; DNMT3 GENE; DROSOPHILA MELANOGASTER; EMBRYO DEVELOPMENT; ENDOCRINOLOGY; EPIGENETICS; GALLERIA MELLONELLA; GENE; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENE SILENCING; GENETIC CODE; HISTONE MODIFICATION; HORMONE ACTION; HORMONE DETERMINATION; HORMONE SYNTHESIS; HUMAN; INSECT DEVELOPMENT; LEPIDOPTERA; NONHUMAN; PRIORITY JOURNAL; PROTEIN PROCESSING; REVIEW; RNA INTERFERENCE; SCHISTOCERCA GREGARIA;

EID: 84878989249     PISSN: 00166480     EISSN: 10956840     Source Type: Journal    
DOI: 10.1016/j.ygcen.2013.02.004     Document Type: Review

References (109)

1. Auger C.J., Coss D., Auger A.P., Forbes-Lorman R.M. Epigenetic control of vasopressin expression is maintained by steroid hormones in the adult male rat brain. Proc. Natl. Acad. Sci. USA 2011, 108:4242-42477.
2. Bang L., Lagueux M., Hirn M., Hoffmann J.A. Identification by gas chromatography and mass spectrometry, of ecdysone synthesized in the ovaries of adult female Locusta migratoria (Insecta Orthoptera). C. R. Acad. Sci. Hebd. Séances Sci. D. 1976, 283:1081-1084.
3. Boerjan B., Sas F., Ernst U.R., Tobback J., Lemière F., Vandegehuchte M.B., Janssen C.R., Badisco L., Marchal E., Verlinden H., Schoofs L., De Loof A. Locust phase polyphenism: does epigenetic precede endocrine regulation?. Gen. Comp. Endocrinol. 2011, 173:120-128.
4. Boros I.M. Histone modification in Drosophila. Brief Funct. Genomics. 2012, 11:319-331.
5. Borovsky D., Carlson D.A., Ujváry I., Prestwich G.D. Biosynthesis of (10R)-juvenile hormone III from farnesoic acid by Aedes aegypti ovary. Arch. Insect Biochem. Physiol. 1994, 27:11-25.
6. Borovsky D., Carlson D.A., Hancock R.G., Rembold H., van Handel E. De novo biosynthesis of juvenile hormone III and I by the accessory glands of the male mosquito. Insect Biochem. Mol. Biol. 1994, 24:437-444.
7. Briers T., De Loof A. Moulting hormone activity in the adult Colorado potato beetle, Leptinotarsa decemlineata Say in relation to reproduction and diapause. Int. J. Invert. Reprod. 1980, 3:145-155.
8. 3H] ecdysone in the vitellogenic follicles of Sarcophaga bullata (Diptera) and its localization by autoradiography. Int. J. Invert. Reprod. 1982, 4:343-357.
9. Briers T., Peferoen M., De Loof A. Ecdysteroids and adult diapause in the Colorado potato beetle Leptinotarsa decemlineata. Physiol. Entomol. 1982, 7:379-386.
10. 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. 1983, 74A:521-524.
11. Briers T., Van Beek E., De Loof A. Metabolism of injected ecdysone in female Sarcophaga bullata. Comp. Biochem. Physiol. 1983, 75B:9-14.
12. De Loof A., de Wilde J. Hormonal control of synthesis of vitellogenic female proteins in the Colorado potato beetle Leptinotarsa decemlineata. J. Insect Physiol. 1970, 16:1455-1466.
13. De Loof A., Van Loon J. A redescription of the Galleria bioassay for juvenile hormones and compounds with juvenile hormone activity. Annales Soc. R. Zool. Belg. (=now Belgian Journal of Zoology) 1979, 109:19-28.
14. De Loof A., Huybrechts R., Kotanen S. Reproduction and love: strategies of the organism's cellular defense system?. Comp. Biochem. Physiol. C Pharmacol. Toxicol. Endocrinol. 1998, 120:167-176.
15. De Loof A., Huybrechts R., Geens M., Vandersmissen T., Boerjan B., Schoofs L. Sexual differentiation in adult insects: male-specific cuticular yellowing in Schistocerca gregaria as a model for reevaluating some current (neuro)endocrine concepts. J. Insect Physiol. 2010, 56:919-925.
16. De Loof A., De Haes W., Boerjan B., Schoofs L. The fading electricity theory of ageing: the missing biophysical principle?. Ageing Res. Rev. 2013, 12:58-66.
17. de Wilde J. Diapause and seasonal synchronization in the adult Colorado beetle (Leptinotarsa decemlineata say). Dormancy and survival. Symp. Soc. Exper. Biol. 1969, 23:263-284.
18. Deguchi R., Takeda N., Stricker S.A. Comparative biology of cAMP-induced germinal vesicle breakdown in marine invertebrate oocytes. Mol. Reprod. Dev. 2011, 78:708-725.
19. Delbecque J.P., Lanzrein B., Bordereau C., Imboden H., Hirn M., O'Connor J.D., Noirot C., Lüscher M. Ecdysone and ecdysterone in physogastric queens and eggs of Macrotermes bellicosus and Macrotermes subhalynus. Gen. Comp. Endocrinol. 1978, 36:40-47.
20. Denlinger D.L. Regulation of diapause. Annu. Rev. Entomol. 2002, 47:93-122.
21. Drewell R.A., Bush E.C., Remnant E.J., Wong G.T., Stringham J.L., Lim J., Goudie F., Oldroyd B.P. Genomic imprinting in the honey bee methylome. Proceedings of the 5th congress of the European sections of the International Union for the Study of Social Insects 2012, 154.
22. Ebert A., Lein S., Schotta G., Reuter G. Histone modification and the control of heterochromatic gene silencing in Drosophila. Chromosome Res. 2006, 14:377-392.
23. Endo T., Imai A., Shimaoka T., Kano K., Naito K. Histone exchange activity and its correlation with histone acetylation status in porcine oocytes. Reproduction 2011, 141:397-405.
24. Falckenhayn C., Boerjan B., Raddatz G., Frohme M., Schoofs L., Lyko F. Characterization of genome methylation patterns in the desert locust Schistocerca gregaria. J. Exp. Biol. 2012, 10.1242/jeb080754.
25. Feng S., Jacobsen S.E., Reik W. Epigenetic reprogramming in plant and animal development. Science 2010, 330:622-627.
26. Flores K.B., Wolschin F., Allen A.N., Corneveaux J.J., Huentelman M., Amdam G.V. Genome-wide association between DNA methylation and alternative splicing in an invertebrate. BMC Genomics 2012, 13:480.
27. Gálikova M., Klepsatel P., Senti G., Flatt T. Steroid hormone regulation of C. elegans and Drosophila aging and life history. Exp. Gerontol. 2011, 46:141-147.
28. Ghodageri M.G., Katti P. In vitro induction/inhibition of germinal vesicle breakdown (GVBD) in frog (Euphlyctis cyanophlyctis) oocytes by endocrine active compounds. Drug Chem. Toxicol. 2012, 5. 10.3109/01480545.2012.710623.
29. Glastad K.M., Hunt B.G., Yi S.V., Goodisman M.A.D. DNA methylation in insects: on the brink of the epigenomic era. Insect Mol. Biol. 2011, 20:553-565.
30. Goll M.G., Bestor T.H. Eukaryotic cytosine methyltransferases. Annu. Rev. Biochem. 2005, 74:481-514.
31. Goltzené F., Lageux M., Charlet M., Hoffmann J.A. The follicle cell epithelium of maturing ovaries of Locusta migratoria: a new biosynthetic tissue for ecdysone. Hoppe Seylers Z. Physiol. Chem. 1978, 359:1427-1434.
32. Greer E.L., Maures T.J., Hauswirth A.G., Green E.M., Leeman D.S., Maro G.S., Han S., Banko M.R., Gozani O., Brunet A. Members of the H3K4trimethylation complex regulate lifespan in a germline-dependent manner in C. elegans. Nature 2010, 466:383-387.
33. Greer E.L., Maures T.J., Ucar D., Hauswirth A.G., Macini E., Lim J.P., Benayoun B.A., Shi Y., Brunet A. Transgenerational epigenetic inheritance of longevity in Caenorhabditis elegans. Nature 2011, 479:365-371.
34. Hahn D.A., Denlinger D.L. Energetics of insect diapause. Annu. Rev. Entomol. 2011, 56:103-121.
35. Hartfelder K. Insect juvenile hormone: from "status quo" to high society. Braz. J. Med. Biol. Res. 2000, 33:157-177.
36. Herb B.R., Wolfschin F., Hansen K.D., Aryee M.J., Langmead B., Irizarry R., Amdam G.R., Feinberg A. Reversible switching between epigenetic states in honeybee behavioral subcastes. Nat. Neurosci. 2012, 15:1371-1373.
37. Hétru C., Luu B., Hoffmann J.A. Ecdysone conjugates: isolation and identification. Meth. Enzymol. 1985, 111:411-419.
38. Heyn H., Li N., Ferrera H.J., Moran S., Pisano D.G., Gomez A., Diez J., Sanchez-Mut J.V., Setien F., Carmona F.J., Puca A.A., Sayols S., Pujana M.A., Serra-Musach J., Iglesias-Platas I., Formiga F., Fernandez A.F., Fraga M.F., Heath S.C., Valencia A., Gut I.G., Wang J., Esteller M. Distinct DNA methylomes of newborns and centenarians. Proc. Natl. Acad. Sci. USA 2012, 109:10522-10527.
39. Homberg U., Brandl C., Clynen E., Schoofs L., Veenstra J.A. Mas-allatotropin/Lom-AG-myotropin I immunostaining in the brain of the locust Schistocerca gregaria. Cell Tissue Res. 2004, 318:439-457.
40. Hongmei L. RNAi Knockdown of DNA Methylation Affects Gene Splicing in the Honey Bee Apis mellifera 2012, Abstract at the XXIV International Congress of Entomology, New Era to Entomology, Daegu Korea, Aug., 19-25.
41. Huang Y., Marton L.J., Woster P.M., Casero R.A. Polyamine analogues targeting epigenetic gene regulation. Essays Biochem. 2009, 46:95-110.
42. Hult E.F., Tobe S.S., Chang B.S. Molecular evolution of ultraspiracle protein (USP/RXR) in insects. PLoS One 2011, 6(8):e23416.
43. Huybrechts R., De Loof A. Similarities in vitellogenin and control of vitellogenin synthesis within the genera Sarcophaga, Calliphora, Phormia and Lucilia (Diptera). Comp. Biochem. Physiol. 1982, 72B:339-344.
44. Inoue A., Ogushi S., Saitou M., Suzuki M.G., Aoki F. Involvement of mouse nucleoplasmin 2 in the decondensation of sperm chromatin after fertilization. Biol. Reprod. 2011, 85:70-77.
45. Jindra M., Pälli S.R., Riddiford L.M. The juvenile hormone signaling pathway in insect development. Annu. Rev. Entomol. 2013, 10.1146/annurev-ento-120811-153700.
46. Jurkowski T.P., Jeltsch A. On the evolutionary origin of eukaryotic DNA methyltransferases and Dnmt2. PLoS One 2011, 6:e28104.
47. Kamakura M. Royalactin induces queen differentiation in honeybees. Nature 2011, 473:478-483.
48. Kantlehner M., Kirchner R., Hartmann P., Ellwart J., Alunni-Fabbroni M., Schumacher A. A high-throughput DNA methylation analysis of a single cell. Nucleic Acids Res. 2011, 39:1-9.
49. Karlson P., Ecdyson Das Häutungshormon der Insekten. Naturwissenschaften 1966, 53:445-453.
50. Khoueiry R., Ibala-Rhomdane S., Méry L., Blachère T., Guérin J.F., Lomage J., Lefèvre A. Dynamic CpG methylation of the KCNQ1OT1 gene during maturation of human oocytes. J. Med. Genet. 2008, 45:583-588.
51. Konopova B., Jindra M. Juvenile hormone resistance gene Methoprene-tolerant controls entry into metamorphosis in the beetle Tribolium castaneum. Proc. Natl. Acad. Sci. USA 2007, 104:10488-10493.
52. Koolman J., Hoffmann J.A., Karlson P. Sulphate esters as inactivation products of ecdysone in Locusta migratoria. Hoppe Seylers Z. Physiol. Chem. 1973, 354:1043-1048.
53. Korb J., Hoffmann K., Hartfelder K. Molting dynamics and juvenile hormone titer profiles in the nymphal stages of a lower termite, Cryptotermes secundus (Kalotermitidae) - signatures of developmental plasticity. J. Insect Physiol. 2012, 58:376-386.
54. Krauss V., Reuter G. DNA methylation in Drosophila-a critical evaluation. Prog. Mol. Biol. Transl. Sci. 2011, 101:177-191.
55. 2+. Exp. Cell Res. 1973, 82:89-94.
56. Kucharski R., Maleszka J., Foret S., Maleszka R. Nutritional control of reproductive status in honeybees via DNA methylation. Science 2008, 319:1827-1830.
57. Lachaise F., Hoffmann J.A. Ecdysteroids and embryonic development in the shore crab, Carcinus maenas. Hoppe Seylers Z. Physiol. Chem. 1982, 363:1059-1069.
58. Lachaise F., Goudeau M., Hétru C., Kappler C., Hoffmann J.A. Ecdysteroids and ovarian development in the shore crab, Carcinus maenas. Hoppe Seylers Z. Physiol. Chem. 1981, 362:521-529.
59. Lanot R., Thiebold J., Costet-Corio M.F., Benveniste P., Hoffmann J.A. Further experimental evidence for the involvment of ecdysone in the control of meiotic reinitiation in oocytes of Locusta migratoria (Insecta, Orthoptera). Dev. Biol. 1988, 126:212-214.
60. Leonhardt H., Cardoso M.C. DNA methylation, nuclear structure, gene expression and cancer. J. Cell Biochem 2000, Suppl. 35:78-83.
61. Lezzi M., Gilbert L.I. Control of gene activities in the polytene chromosomes of Chironomus tentans by ecdysone and juvenile hormone. Proc. Natl. Acad. Sci. USA 1969, 64:498-503.
62. Lyko F., Ramsahoye B.H., Jaenisch R. DNA methylation in Drosophila melanogaster. Nature 2000, 408:538-540.
63. Madeo F., Eisenberg T., Büttner S., Ruckenstuhl C., Kroemer G. Spermidine: a novel autophagy inducer and longevity elixir. Autophagy 2010, 6:160-162.
64. Marchal E., Badisco L., Verlinden H., Vandersmissen T., Van Soest S., Van Wielendaele P., Vanden Broeck J. Role of the Halloween genes, Spook and Phantom in ecdysteroidogenesis in the desert locust Schistocerca gregaria. J. Insect Physiol. 2011, 57:1240-1248.
65. Marchal E., Zhang J., Badisco L., Verlinden H., Hult E.F., Van Wielendaele P., Yagi K.J., Tobe S.S., Vanden Broeck J. Final steps in juvenile hormone biosynthesis in the desert locust Schistocerca gregaria. Insect Biochem. Mol. Biol. 2011, 41:219-227.
66. Marchal E., Verlinden H., Badisco L., Van Wielendaele P., Vanden Broeck J. RNAi-mediated knockdown of Shade negatively affects ecdysone-20-hydroxylation in the desert locust Schistocerca gregaria. J. Insect Physiol. 2012, 58:890-896.
67. Marhold J., Rothe N., Pauli A., Mund C., Kuehle K., Brueckner B., Lyko F. Conservation of DNA methylation in dipteran insects. Insect Mol. Biol. 2004, 13:117-123.
68. Minami R., Wakabayashi M., Sugimori S., Taniguchi K., Kokuryo A., Imano T., Adachi-Yamada T., Watanabe N., Nakagoshi H. The homeodomain protein defective proventriculus is essential for male accessory gland development to enhance fecundity in Drosophila. PLoS One 2012, 7(3):e32302.
69. Mochizuki K., Matsui Y. Epigenetic profiles in primordial germ cells: global modulation and fine tuning of the epigenome for acquisition of totipotency. Dev. Growth Differ. 2010, 52:517-525.
70. Nagahama Y., Yamashita M. Regulation of oocyte maturation in fish. Dev. Growth Differ. 2008, 50(Suppl. 1):195-219.
71. Okano M., Xie S., Li E. Cloning and characterization of a family of novel mammalian DNA (cytosine-5) methyltransferases. Nat. Genet. 1998, 19:219-220.
72. Paemen L., Tips A., Schoofs L., Proost P., Van Damme J., De Loof A. Lom-AG-myotropin: a novel myotropic peptide from the male accessory glands of Locusta migratoria. Peptides 1991, 12:7-10.
73. Pasque V., Halley-Stott R.P., Gillich A., Garrett N., Gurdon J.B. Epigenetic stability of repressed states involving the histone variant macroH2A revealed by nuclear transfer to Xenopus oocytes. Nucleus 2011, 2:533-539.
74. Peferoen M., De Loof A. The juvenile hormone titer in Galleria mellonella. Annales Soc. R. Zool. Belg. (=Belg. J. Zool) 1980, 109:87-90.
75. Peferoen M., Fransen P., De Loof A. Influence of procaine HCl on larval development, adult lifespan and acid phosphatase activity in Musca domestica. Arch. Int. Physiol. Biochem. 1982, 90:309-315.
76. Pener M.P., Simpson S.J. Locust phase polyphenism: an update. Adv. Insect Physiol. 2009, 36:1-272.
77. Peterson C.L., Laniel M.-A. Histones and histone modification. Curr. Biol. 2004, 14:R546-R551.
78. Popp C., Dean W., Feng S., Cokus S.J., Andrews S., Pellegrini M., Jacobsen S.E., Reik W. Genome-wide erasure of DNA methylation in mouse primordial germ cells is affected by AID deficiency. Nature 2010, 463:1101-1105.
79. Rai K., Chidester S., Zavala C.V., Manos E.J., James S.R., Karpf A.R., Jones D.A., Cairns B.R. Dnmt2 functions in the cytoplasm to promote liver, brain, and retina development in zebrafish. Genes Dev. 2007, 21:261-266.
80. Retnakaran A., Granett G., Ennis T. Insect Growth Regulators in Comprehensive Insect Physiology, Biochemistry and Pharmacology 1985, 529-601. Oxford, Pergamon. G.A. Kerkut, L.I. Gilbert (Eds.).
81. Riddiford L.M. How does juvenile hormone control insect metamorphosis and reproduction. Gen. Comp. Endocrinol. 2012, 179:477-484.
82. Riddiford L.M., Bilen J. The Juvenile Hormone-Methoprene-Tolerant Complex Regulates Maturation of the Adult Optic Lobe and Female Receptivity in Drosophila 2012, Abstract at the XXIV International Congress of Entomology, New Era to Entomology, Daegu Korea, Aug., 19-25.
83. Riddiford L.M., Truman J.W., Mirth C.K., Yen Y.C. A role for juvenile hormone in the prepupal development of Drosophila melanogaster. Development 2010, 137:1117-1126.
84. Rinterknecht E. Cuticulogenesis correlated with ultrastructural changes in oenocytes and epidermal cells in the late cockroach embryo. Tissue Cell. 1985, 17:723-743.
85. Sall C., Kappler C., Lagueux M., Zachary D., Luu B., Hoffmann J.A. Fate of maternal conjugated ecdysteroids during embryonic development in Locusta migratoria. J. Insect Physiol. 1983, 29:491-507.
86. Sato F., Tsuchiya S., Meltzer S.J., Shimizu K. MicroRNAs and epigenetics. FEBS J. 2011, 278:1598-1609.
87. Schaefer M., Lyko F. Solving the Dnmt2 enigma. Chromosoma 2010, 119:35-40.
88. Schoofs L., Vanden Broeck J., De Loof A. The myotropic peptides of Locusta migratoria: structures, distribution, functions and receptors. Insect Biochem. Mol. Biol. 1993, 23:859-881.
89. Schwedes C.C., Carney G.E. Ecdysone signaling in adult Drosophila melanogaster. J. Insect Physiol. 2012, 58:293-302.
90. Shirk P.D., Dahm K.H., Röller H. The accessory sex glands as the repository for juvenile hormone in male cecropia moths. Z. Naturforsch. C 1976, 31:199-200.
91. Shirk P.D., Bhaskaran G., Röller H. The transfer of juvenile hormone from male to female during mating in the Cecropia silkmoth. Experientia 1980, 36:682-683.
92. Simpson S.J. From Individuals to Populations: A Tale of Swarms, Cannibals, Ageing, and Human Obesity 2012, Abstract at the XXIV International Congress of Entomology, New Era to Entomology, Daegu Korea, Aug., 19-25.
93. Simpson S.J., Sword G.A., Lo N. Polyphenism in insects. Curr. Biol. 2011, 21:R738-R749.
94. Sonobe H., Yamada R. Ecdysteroids during early embryonic development in silkworm Bombyx mori: metabolism and functions. Zool. Sci. 2004, 21:503-516.
95. Spannhoff A., Kim Y.K., Raynal N.J-M., Gharibyan V., Su M.B., Zhou Y.Y., Li J., Castellano S., Sbardella G., Issa J-P.J., Bedford M.T. Histone deacetylase inhibitor activity in royal jelly might facilitate caste switching in bees. EMBO Reports 2011, 12:238-243.
96. Tian L., Ji B.Z., Liu S.W., He C.L., Jin F., Gao J., Stanley D., Li S. JH biosynthesis by reproductive tissues and corpora allata in adult longhorned beetles Apriona germari. Arch. Insect Biochem. Physiol. 2010, 75:275-286.
97. Tobe S.S., Pratt G.E. Corpus allatum activity in vitro during ovarian maturation in the desert locust Schistocerca gregaria. J Exp. Biol. 1975, 62:611-627.
98. Vaissière T., Sawan C., Herceg Z. Epigenetic interplay between histone modifications and DNA methylation in gene silencing. Mutat. Res. 2008, 659:40-48.
99. Villar-Garea A., Fraga M.F., Espada J., Esteller M. Procaine is a DNA-demethylating agent with growth-inhibitory effects in human cancer cells. Cancer Res. 2003, 63:4984-4989.
100. Vuerinckx K., Verlinden H., Lindemans M., Vanden Broeck J., Huybrechts R. Characterization of an allatotropin-like receptor in the red flour beetle Tribolium castaneum. Insect Biochem. Mol. Biol. 2011, 41:815-822.
101. Wang Z., Zhao T., Zhang P., Zhang S., Guan J., Ma X., Yin Y., Zhang J., Tang B., Li Z. Histone deacetylase 1 down-regulation on developmental capability and histone acetylation in bovine oocytes and partenogenetic embryos. Reprod. Domest. Anim. 2011, 46:1022-1028.
102. Williams C.M. The juvenile hormone. III. Its accumulation and storage in the abdomens of certain male moths. Biol. Bull. 1963, 124:355-367.
103. Willis J.H. Juvenile hormone: the status of "Status quo". Am. Zool. 1981, 21:763-773.
104. Willis J.H. The paradigm of stage-specific gene sets in insect metamorphosis: time for revision!. Arch. Insect Biochem. Physiol. 1986, Suppl. 1:47-57.
105. Yamawaki T.M., Berman J.R., Suchanek-Kavipurapu M., McCormick M., Gaglia M.M., Lee S.J., Kenyon C. The somatic reproductive tissues of C. elegans promote longevity through steroid hormone signaling. PLoS Biol. 2010, 8(8):e1000468.
106. Zemach A., McDaniel I.E., Silva P., Zilberman D. Genome-wide evolutionary analysis of eukaryotic DNA methylation. Science 2010, 328:916-919.
107. Zhang X., Ho S.M. Epigenetics meets endocrinology. J. Mol. Endocrinol. 2011, 46:R11-R32.
108. Zitnan D., Kim Y.J., Zitnanová I., Roller L., Adams M.E. Complex steroid-peptide-receptor cascade controls insect ecdysis. Gen. Comp. Endocrinol. 2007, 153:88-95.
109. Zwier M.V., Verhulst E.C., Zwahlen R.D., Beukeboom L.W., van de Zande L. DNA methylation plays a crucial role during early Nasonia development. Insect Mol. Biol. 2012, 21:129-138.