Homology of insect corpora allata and vertebrate adenohypophysis?

Arthropod Structure and Development

Volumn 41, Issue 5, 2012, Pages 409-417

  Wirmer, Andrea ^a   Bradler, Sven ^b   Heinrich, Ralf ^b  

^a UNIVERSITY OF ULM   (Germany)

^b UNIVERSITY OF GÖTTINGEN   (Germany)

Author keywords

Adenohypophysis; Corpora allata; Homology; Insect; Neuroendocrinology; Vertebrate

Indexed keywords

CORTICOTROPIN; INTERMEDIN; NITRIC OXIDE SYNTHASE;

ADENOHYPOPHYSIS; CORPUS ALLATUM; EMBRYO DEVELOPMENT; ENDOCRINE GLAND; HORMONE RELEASE; HYPOTHALAMUS; IMMUNOCYTOCHEMISTRY; INSECT; NERVE CELL; PHYLOGENY; REVIEW; STRUCTURAL HOMOLOGY; VERTEBRATE; VITELLOGENESIS;

ANIMALS; BIOLOGICAL EVOLUTION; CORPORA ALLATA; GENE EXPRESSION REGULATION, DEVELOPMENTAL; INSECT HORMONES; INSECTS; NEUROTRANSMITTER AGENTS; PITUITARY GLAND, ANTERIOR; VERTEBRATES;

ANIMALIA; BASIDIOMYCOTA; BILATERIA; HEXAPODA; METAZOA; VERTEBRATA;

EID: 84865357365     PISSN: 14678039     EISSN: 18735495     Source Type: Journal    
DOI: 10.1016/j.asd.2012.04.003     Document Type: Review

References (126)

1. Anderson T., Forlin L., Olsen S., Fostier A., Breton B. Pituitary as a target organ for toxic effects of P4501A1 inducting chemicals. Molecular and Cellular Endocrinology 1993, 91:99-105.
2. Arendt D. The evolution of cell types in animals: emerging principles from molecular studies. Nature Reviews Genetics 2008, 9:868-882.
3. Arendt D., Nübler-Jung K. Inversion of dorsoventral axis?. Nature 1994, 371:26.
4. Asa L.S., Bilbao J.M., Kovacs K., Linfoot J.A. Hypothalamic neuronal hamartoma associated with pituitary growth hormone cell adenoma and acromegaly. Acta Neuropathologica 1980, 52:231-234.
5. Baldwin W.S., Marko P.B., Nelson D.R. The cytochrome P450 (CYP) gene superfamiliy in Daphnia pulex. BMC Genomics 2009, 10:169.
6. Barnes M.J., Lapanowski K., Rafols J.A., Lawson D.M., Dunbar J.C. GnRH and gonadotropin release is decreased in chronic nitric oxide deficiency. Experimental Biology and Medicine 2001, 226:701-706.
7. Batten T.F.C., Ball J.N. Ultrastructure of the neurohypophysis of the teleost Poecilia latipinna in relation to neural control of the adenohypophysial cells. Cell and Tissue Research 1977, 185:409-433.
8. Bernstein H.-G., Stanarius A., Baumann B., Henning H., Krell D., Danos P., Falkai P., Bogerts B. Nitric oxide synthase-containing neurons in the human hypothalamus: reduced number of immunoreactive cells in the paraventricular nucleus of depressive patients and schizophrenics. Neuroscience 1998, 83:867-875.
9. Bronson F.H. Establishment of social rank among grouped male mice: relative effects on circulating FSH, LH, and corticosterone. Physiology & Behavior 1973, 10:947-951.
10. Candani S., Holland D.D., Oliveri D., Parodi M., Pestarino M. Expression of the amphioxus Pit-1 gene (AmphiPOU1F1/Pit-1) exclusively in the developing preoral organ, a putative homolog of the vertebrate adenohypophysis. Brain Research Bulletin 2008, 75:324-330.
11. Capdevila J., Snijder G.D., Falck J.R. Epoxygenation of arachidonic acid by rat anterior pituitary microsomal fractions. FEBS Letters 1984, 178:319-322.
12. Carroll L.S., Carrow G.M., Calabrese R.L. Localization and release of FMRFamide-like immunoreactivity in the cerebral neuroendocrine system of Manduca sexta. Journal of Experimental Biology 1986, 126:1-14.
13. Cassier P. The corpora allata of insects. International Review of Cytology 1979, 57:1-73.
14. Ceccatelli S., Hulting A.-L., Zhang X., Gustafsson L., Villar M., Hökfelt T. Nitric oxide synthase in the rat anterior pituitary gland and the role of nitric oxide in regulation of luteinising hormone secretion. Proceedings of the National Academy of Sciences of the United States of America 1993, 90:11292-11296.
15. Chiang A.-S., Wen C.-J., Lin C.-Y., Yeh C.-H. Nadph-diaphorase activity in corpus allatum cells of the cockroach Diploptera punctata. Insect Biochemistry and Molecular Biology 2000, 30:747-753.
16. Chitnis A., Henrique D., Lewis J., Ish-Horowicz D., Kintner C. Primary neurogenesis in Xenopus embryos regulated by a homologue of the Drosophila neurogenic gene Delta. Nature 1995, 375:761-766.
17. De Loof A., Schoofs L. Homologies between the amino acid sequences of some vertebrate peptide hormones and peptides isolated from invertebrate sources. Comparative Biochemistry and Physiology 1990, 95B:459-468.
18. De Robertis E.M., Sasai Y. A common plan for dorsoventral patterning in Bilateria. Nature 1996, 380:37-40.
19. De Velasco B., Shen J., Go S., Hartenstein V. Embryonic development of the Drosophila corpus cardiacum, a neuroendocrine gland with similarity to the vertebrate pituitary, is controlled by sine oculis and glass. Developmental Biology 2004, 274:280-294.
20. De Velasco B., Erclik T., Shy D., Sclafani J., Lipshitz H., McInnes R., Hartenstein V. Specification and development of the pars intercerebralis and pars lateralis neuroendocrine command centres in the Drosophila brain. Developmental Biology 2007, 302:309-323.
21. Denes A.S., Jekely G., Steinmetz P.R.H., Raible F., Snyman H., Prud'homme B., Ferrier D.E.K., Blavoine G., Arendt D. Molecular architecture of annelid nerve cord supports common origin of nervous system centralization in bilateria. Cell 2007, 129:277-288.
22. Denver R. The molecular basis of thyroid hormone-dependent central nervous system remodeling during amphibian metamorphosis. Comparative Biochemistry and Physiology Part C: Pharmacology Toxicology and Endocrinology 1997, 119:219-228.
23. Di Cosmo A., Di Cristo C. Neuropeptidergic control of the optic gland of Octopus vulgaris: FMRF-amide and GnRH immunoreactivity. The Journal of Comparative Neurology 1998, 398:1-12.
24. Dores R.M., Lecaudé S., Bauer D., Danielson P.B. Analyzing the evolution of the opioid/orphan gene family. Mass Spectrometry Reviews 2002, 21:220-243.
25. Dunn C.W., Hejnol A., Matus D.Q., Pang K., Browne W.E., Smith S.A., Seaver E., Rouse G.W., Obst M., Edgecombe G.D., et al. Broad phylogenomic sampling improves resolution of the animal tree of life. Nature 2008, 452:745-749.
26. 8. Cell and Tissue Research 1991, 263:285-291.
27. Duvilanski B.H., Zambruno C., Seilicovich A., Pisera D., Lasaga M., Diaz M.C., Belova N., Rettori V., McCann S.M. Role of nitric oxide in control of prolactin release by the adenohypophysis. Proceedings of the National Academy of Sciences of the United States of America 1995, 92:170-174.
28. Eichmüller S., Hammer M., Schäfer S. Neurosecretory cells in the honeybee brain and suboesophageal ganglion show FMRFamide-like immunoreactivity. The Journal of Comparative Neurology 1991, 312:164-174.
29. Enayetallah A.E., French R.A., Thibodeau M.S., Grant D.F. Distribution of soluble epoxide hydrolase and of cytochrome P4502C8, 2C9, and 2J2 in human tissues. Journal of Histochemistry and Cytochemistry 2004, 52:447-454.
30. Gallardo M.E., Lopez-Rios J., Fernaud-Espinosa I., Granadino B., Sanz R., Ramos C., Ayuso C., Seller M.J., Brunner H.G., Bovolenta P., Rodríguez de Córdoba S. Genomic cloning and characterization of the human homeobox gene SIX6 reveals a cluster of SIX genes in chromosome 14 and associates SIX6 hemizygosity with bilateral anophthalmia and pituitary anomalies. Genomics 1999, 61:82-91.
31. Garcia-Lavandeira M., Quereda V., Flores I., Saez C., Diaz-Rodriguez E., Japon M.A., Ryan A.K., Blasco M.A., Dieguez C., Malumbres M., Alvarez C.V. A GRFa2/Prop1/Stem (GPS) cell niche in the pituitary. PLoS One 2009, 4:e4815.
32. Gerisch B., Antebi A. Hormonal signals produced by DAF-9/cytochome P450 regulate C. elegans dauer diapause in response to environmental cues. Development 2004, 131:1765-1776.
33. González-Domenech C.M., Muñoz-Chápuli R. Molecular evolution of nitric oxide synthase in metazoans. Comparative Biochemistry and Physiology Part D: Genomics and Proteomics 2010, 5:295-301.
34. Griffiths P.E. The phenomena of homology. Biology and Philosophy 2007, 22:643-658.
35. Hansen B.L., Hansen G.N., Scharrer B. Immunoreactive material resembling vertebrate neuropeptides in the corpus cardiacum and corpus allatum of the insect Leucophaea maderae. Cell and Tissue Research 1982, 225:319-329.
36. Harding C.F. Social modulation of circulating hormone levels in the male. American Zoologist 1981, 21:223-231.
37. Hartenstein V. The neuroendocrine system of invertebrates: a developmental and evolutionary perspective. Journal of Endocrinology 2006, 190:555-570.
38. Hartfelder K. Insect juvenile hormone: from 'status quo' to high society. Brazilian Journal of Medical and Biological Research 2000, 33:157-177.
39. Harzsch S., Wanninger A. Evolution of invertebrate nervous systems: the Chaetognatha as a case study. Acta Zoologica 2010, 91:35-43.
40. Heinrich, R., Kunst, M., Wirmer, A. Reproduction-related sound production of grasshoppers regulated by internal state and actual sensory environment. Frontiers in Decision Neuroscience 6, 89. http://dx.doi.org/10.3389/fnins.2012.00089.
41. Helle J., Dircksen H., Eckert M., Nässel D.R., Spörhase-Eichmann U., Schürmann F.-W. Putative neurohemal areas in the peripheral nervous system of an insect, Gryllus bimaculatus, revealed by immunocytochemistry. Cell and Tissue Research 1995, 281:43-61.
42. Helvig C., Koener J.F., Unnithan G.C., Feyereisen R. CYP15A1, the cytochrome P450 that catalyzes epoxidation of methyl farnesoate to juvenile hormone III in cockroach corpora allata. Proceedings of the National Academy of Sciences of the United States of America 2004, 101:4024-4029.
43. Hirth F. On the origin and evolution of the tripartite brain. Brain, Behavior and Evolution 2010, 76:3-10.
44. Holland N.D. Early central nervous system evolution: an era of skin brains?. Nature Reviews. Neuroscience 2003, 4:1-11.
45. Huang P., Rannug A., Ahlbom E., Hakansson H., Ceccatelli S. Effect of 2,3,7,8-tetrachlorodibenzo-p-dioxin on the expression of cytochrome P450 1A1, the aryl hydrocarbon receptor, and the aryl hydrocarbon receptor nuclear translocator in rat brain and pituitary. Toxicology and Applied Pharmacology 2000, 169:159-167.
46. Jacobs D.K., Gates R.D. Developmental genes and the reconstruction of metazoan evolution - implications of evolutionary loss, limits on inference of ancestry and type 2 errors. Integrative and Comparative Biology 2003, 43:11-18.
47. Johnson A.L., Tilly J.L. Second messenger pathways mediating chicken luteinizing hormone secretion from dispersed pituitary cells. Biology of Reproduction 1991, 45:64-72.
48. Kano S. Genomics and developmental approaches to an ascidian adenohypophysis primordium. Integrative and Comparative Biology 2010, 50:35-52.
49. Kawamura K., Kouki T., Kawahara G., Kikuyama S. Hypophyseal development in vertebrates from amphibians to mammals. General and Comparative Endocrinology 2002, 126:130-135.
50. Khan M.A., Koopmanschap A.B., de Kort C.A.D. The relative importance of nervous and humoral pathways for control of corpus allatum activity in the adult colorado potato beetle, Leptinotarsa decemlineata (Say). General and Comparative Endocrinology 1983, 52:214-221.
51. Kobayashi Y., Ando H. Embryonic development of the alimentary canal and ectodermal derivatives in the primitive moth, Neomicropteryx nipponensis Issiki (Lepidoptera, Micropterygidae). Journal of Morphology 1983, 176:289-314.
52. Kontogeorgos G., Mourouti G., Kyrodimou E., Liapi-Avgeri L., Parasi E. Ganglion cell containing pituitary adenomas: signs of neuronal differentiation in adenoma cells. Acta Neuropathologica 2006, 112:21-28.
53. Kou R., Chou S.-Y., Huang Z.Y., Yang R.-L. Juvenile hormone levels are increased in winners of cockroach fights. Hormones and Behavior 2008, 54:521-527.
54. Kouki T., Imai H., Aoto K., Eto K., Shioda S., Kawamura K., Kikuyama S. Developmental origin of the rat adenohypophysis prior to the formation of Rathke's pouch. Development 2001, 128:959-963.
55. Kutsch W., Breidbach O. Homologous structures in the nervous systems of Arthropoda. Advances in Insect Physiology 1994, vol. 24:1-113. Academic Press Limited.
56. Larrere M., Couillaud F. Role of juvenile hormone biosynthesis in dominance and reproduction of the bumble bee, Bombus terrestris. Behavioral Ecology and Sociobiology 1993, 33:335-338.
57. Laufer H., Biggers W.J. Unifying concepts learned from methyl farnesoate for invertebrate reproduction and post-embryonic development. American Zoologist 2001, 41:442-457.
58. Liu S. Peptidergic innervation in pars distalis of the human anterior pituitary. Brain Research 2004, 1008:61-68.
59. Loher W. Die Kontrolle des Weibchengesanges von Gomphocerus rufus L. (Acridinae) durch die Corpora allata. Naturwissenschaften 1962, 49:406.
60. Löhr H., Hammerschmidt M. Zebrafish in endocrine systems: recent advances and implications for human disease. Annual Review of Physiology 2011, 73:183-211.
61. Malagoli D., Accorsi A., Ottaviani E. The evolution of pro-opiomelanocortin: looking for the invertebrate fingerprints. Peptides 2011, 32:2137-2140.
62. Martinelli G.P., Friedrich V.L., Holstein G.R. L-citrulline immunostaining identifies nitric oxide production sites within neurons. Neuroscience 2002, 114:111-122.
63. Masuo R., Misawa K., Ito E. Genomic structure of nitric oxide synthase in the terrestrial slug is highly conserved. Gene 2008, 415:74-81.
64. Mathewson S.F. Gonadotrophic hormones affect aggressive behavior in starling. Science 1961, 134:1522-1523.
65. Meunier B., de Visser S.P., Shaik S. Mechanism of oxidation reactions catalyzed by cytochrome P450 enzymes. Chemical Reviews 2004, 104:3947-3980.
66. Moroz L.L. On the independent origin of complex brains and neurons. Brain, Behavior and Evolution 2009, 74:177-190.
67. Nässel D.R. Neuropeptides in the nervous system of Drosophila and other insects: multiple roles as neuromodulators and neurohormones. Progress in Neurobiology 2002, 68:1-84.
68. Navarro V.M., Castellano J.M., Fernandez-Fernandez R., Tovar S., Roa J., Mayen A., Nogueiras R., Vazquez M.J., Barreiro M.L., Magni P., et al. Characterization of the potent luteinising hormone-releasing activity of KiSS-1 peptide, the natural ligand of GPR54. Endocrinology 2005, 146:156-163.
69. Nelson D.R. The cytochrome P450 homepage. Human Genomics 2009, 4:59-65.
70. Nixon K.C., Carpenter J.M. On homology. Cladistics 2011, 27:1-10.
71. Pavlinov I.Y. The contemporary concepts of homology in biology: a theoretical review. Biology Bulletin Reviews 2012, 2:36-54.
72. Peter R.E., Yu K.-L., Marchant T.A., Rosenblum P.M. Direct neural regulation of the teleost adenohypophysis. The Journal of Experimental Zoology - Supplement 1990, 4:84-89.
73. Peterson K.J., Cotton J.A., Gehling J.G., Pisani D. The Ediacaran emergence of bilaterians: congruence between the genetic and the geological fossil records. Philosophical Transactions of the Royal Society B: Biological Sciences 2008, 363:1435-1443.
74. Popa G., Fielding U. A portal circulation from the pituitary to the hypothalamus region. Journal of Anatomy 1930, 65:88-91.
75. Posnien N., Koniszewski N., Bucher G. Insect Tc-six4 marks a unit with similarity to vertebrate placodes. Developmental Biology 2011, 350:208-216.
76. Radovick S., Nations M., Du Y.F., Berg L.A., Weintraub B.D., Wondisford F.E. A mutation in the POU-homeodomain of Pit-1 responsible for combined pituitary hormone deficiency. Science 1992, 257:1115-1118.
77. Remane A. The enterocoelic origin of the coelom. The Lower Metazoa 1963, 78-90. University of California Press, Berkeley, CA. E.C. Dougherty (Ed.).
78. Rheem A.T., Rettie A.E. Cytochrome P450 2C8: substrates inhibitors, pharmacogenetics, and clinical relevance. Clinical Pharmacology & Therapeutics 2005, 77:341-352.
79. Rizzoti K., Lovell-Badge R. Early development of the pituitary gland: induction and shaping of Rathke's pouch. Reviews in Endocrine & Metabolic Disorders 2005, 6:161-172.
80. Röseler P.F. Endocrine basis of dominance and reproduction in polistine paper wasps. Experimental Behavioral Ecology and Socio-biology 1985, 259-272. Sinauer Ass, Sunderland, MA. B. Hölldobler, M. Lindauer (Eds.).
81. Rosselli M., Keller P.J., Dubey R.K. Role of nitric oxide in the biology, physiology and pathophysiology of reproduction. Human Reproduction Update 1998, 4:3-24.
82. Rubinek T., Rubinfeld H., Hadini M., Barkai G., Shimon I. Nitric oxide stimulates growth hormone secretion from human fetal pituitaries and cultured pituitary adenomas. Endocrine 2005, 28:209-216.
83. Salzet M., Verger-Bocquet M., Bulet P., Beauvillain J.-C., Malecha J. Purification, sequence analysis, and cellular localization of a prodynorphin-derived peptide related to the α-neo-endorphin in the rhynchobdellid leech Theromyzon tessulatum. Journal of Biological Chemistry 1996, 271:13191-13196.
84. Scharrer B. Neurosecretion III: the cerebral organ of the nemerteans. The Journal of Comparative Neurology 1941, 74:109-130.
85. Scharrer B. Insects as models in neuroendocrine research. Annual Review of Entomology 1987, 32:1-16.
86. Schoofs L., Jégou S., Vaudry H., Verhaert P., de Loof A. Localization of melanotropin-like peptides in the central nervous system of two insect species, the migratory locust, Locusta migratoria, and the fleshfly, Sarcophaga bullata. Cell and Tissue Research 1987, 248:25-31.
87. Scully K.M., Rosenfeld M.G. Pituitary development: regulatory codes in mammalian organogenesis. Science 2002, 295:2231-2235.
88. Shimizu T., Wolfe L.S. Arachidonic acid cascade and signal transduction. Journal of Neurochemistry 1990, 55:1-15.
89. Shiomi K., Fujiwara Y., Yasukochi Y., Kajiura Z., Nakagaki M., Yaginuma T. The Pitx homeobox gene in Bombyx mori: regulation of DH-PBAN neuropeptide hormone gene expression. Molecular and Cellular Neuroscience 2007, 34:209-218.
90. Simmons D.W., Voss J.W., Ingraham H.A., Holloway J.M., Broide R.S., Rosenfeld M.G., Swanson L.W. Pituitary cell phenotypes involve cell-specific Pit-1 mRNA translation and synergistic interactions with other classes of transcription factors. Molecular and Cellular Neuroscience 1990, 4:695-711.
91. Šimo L., Slovák M., Park Y., Žitňan D. Identification of a complex peptidergic neuroendocrine network in the hard tick, Rhipicephalus appendiculatus. Cell and Tissue Research 2009, 335:639-655.
92. Skinner J.R., Ren M., Chan K.K., Stay B. NADPH diaphorase and nitric oxide synthase in the corpus cardiacum-corpus allatum of the cockroach Diploptera punctata. Arthropod Structure 2000, 29:85-94.
93. Slowik F., Fazekas I., Bálint K., Gazsó L., Pásztor E., Czirják S., Lapis K. Intrasellar hamartoma associated with pituitary adenoma. Acta Neuropathologica 1990, 80:328-333.
94. 2+ in anterior pituitary cells. Biochemical and Biophysical Research Communications 1986, 139:1188-1194.
95. Snyder G.D., Yadagiri P., Falck J.R. Effect of epoxyeicosatrienoic acids on growth hormone release from somatotrophs. American Journal of Physiology - Endocrinology and Metabolism 1989, 256:E221-E226.
96. Sower S.A. Brain and pituitary hormones of lampreys, recent findings and their evolutionary significance. American Zoologist 1998, 38:15-38.
97. Spieker M., Darius H., Hankeln T., Soufi M., Sattler A.M., Schaefer J.R., Node K., Börgel J., Mügge A., Lindpaintner K., Huesing A., Maisch B., Zeldin D.C., Liao J.K. Risk of coronary artery disease associated with polymorphism of the cytochrome p450 epoxygenase CYP2J2. Circulation 2004, 110:2132-2136.
98. Stanley-Samuelson D.W. Comparative eicosanoid physiology in invertebrate animals. American Journal of Physiology - Regulatory, Integrative and Comparative Physiology 1991, 260:R849-R853.
99. Stay B., Tobe S.S. Control of juvenile hormone biosynthesis during the reproductive cycle of a viviparous cockroach. General and Comparative Endocrinology 1977, 33:531-540.
100. Stay B., Tobe S.S. The role of allatostatin in juvenile hormone synthesis in insects and crustaceans. Annual Review of Entomology 2007, 52:277-299.
101. Stay B., Zhang J.R., Kwok R.D., Tobe S.S. Localization and physiological effects of RFamides in the corpora allata of the cockroach Diploptera punctata in relation to allatostatins. Peptides 2003, 24:1501-1510.
102. Steinmetz P.R.H., Urbach R., Posnien N., Eriksson J., Kostyunchenko R.P., Brena C., Guy K., Akam M., Bucher G., Arendt D. Six3 demarcates the anterior-most developing brain region in bilaterian animals. EvoDevo 2010, 1:14.
103. Stern M., Böger N., Eickhoff R., Lorbeer C., Kerssen U., Ziegler M., Martinelli G.P., Holstein G.R., Bicker G. Development of nitrergic neurons in the nervous system of the locust embryo. The Journal of Comparative Neurology 2010, 518:1157-1175.
104. Stout J., Atkins G., Zacharias D. Regulation of cricket phonotaxis through hormonal control of the threshold of an identified auditory neuron. Journal of Comparative Physiology A 1991, 169:565-772.
105. Sutherland T.D., Unnithan G.C., Feyereisen R. Terpenoid ω-hydroxylase (CYP4C7) messenger RNA levels in the corpora allata: a marker for ovarian control of juvenile hormone synthesis in Diploptera punctata. Journal of Insect Physiology 2000, 46:1219-1227.
106. Szeto D.P., Rodriguez-Esteban C., Eyan A.K., O'Connell S., Liu R., Kioussi C., Gleiberman A.S., Izpisua-Belmonte J.C., Rosenfeld M.G. Role of the bicoid-related homeodomain factor Pitx1 in specifying hindlimb morphogenesis and pituitary development. Molecular and Cellular Neuroscience 1999, 13:484-494.
107. Tessmar-Raible K. The evolution of neurosecretory centres in bilaterian forebrains: insights from protostomes. Seminars in Cell & Developmental Biology 2007, 18:492-501.
108. Tessmar-Raible K., Raible F., Christodoulou F., Guy K., Rembold M., Hausen H., Arendt D. Conserved sensory-neurosecretory cell types in annelid and fish forebrain: insights into hypothalamus evolution. Cell 2007, 129:1389-1400.
109. Tibbetts E.A., Izzo A.S. Endocrine mediated phenotypic plasticity: condition dependent effects of juvenile hormone on dominance and fertility of wasp queens. Hormones and Behavior 2009, 56:527-531.
110. Tiegs O.N., Murray F.U. Embryonic development of Calandra oryzae. Quarterly Journal of Microscopical Science 1938, 80:159-284.
111. Tomer R., Denes A.S., Tessmar-Raible K., Arendt D. Profiling by image registration reveals common origin of annelid mushroom bodies and vertebrate pallium. Cell 2010, 142:800-809.
112. Tsutsui K. A new key neurohormone controlling reproduction, gonadotropin-inhibitory hormone (GnIH): biosynthesis, mode of action and functional significance. Progress in Neurobiology 2009, 88:76-88.
113. Tsutsui K., Saigoh E., Ukena K., Tranishi H., Fujisawa Y., Kikuchi M., Ishii S., Sharp P.J. A novel avian hypothalamic peptide inhibiting gonadotropin release. Biochemical and Biophysical Research Communications 2000, 275:661-667.
114. Virant-Doberlet M., Horseman G., Loher W., Huber F. Neurons projecting from the brain to the corpora allata in orthopteroid insects: anatomy and physiology. Cell and Tissue Research 1994, 277:39-50.
115. Vorbruggen G., Constien R., Zilian O., Wimmer E.A., Dowe G., Taubert H., Noll M., Jackle H. Embryonic expression and characterization of a PTx1 homolog in Drosophila. Mechanisms of Development 1997, 68:139-147.
116. Wägele J.W. Rejection of the " Uniramia" hypothesis and implications of the Mandibulata concept. Zoologische Jahrbücher: Abteilung für Systematik, ökologie und Geographie der Tiere 1993, 120:253-288.
117. Wang S., Tulina N., Carlin D.L., Rulifson E.J. The origin of islet-like cells in Drosophila identifies parallels to the vertebrate endocrine axis. Proceedings of the National Academy of Sciences of the United States of America 2007, 104:19873-19878.
118. Weinrich A., Kunst M., Wirmer A., Holstein G.R., Heinrich R. Suppression of grasshopper sound production by nitric oxide-releasing neurons of the central complex. Journal of Comparative Physiology A 2008, 194:763-776.
119. Wildemann B., Bicker G. Developmental expression of nitric oxide/cyclic GMP synthesizing cells in the nervous system of Drosophila melanogaster. Journal of Neurobiology 1998, 38:1-15.
120. Wiley E.O., Lieberman B.S. Phylogenetics: the Theory of Phylogenetic Systematics 2011, Blackwell publishing. second ed.
121. Wirmer A., Heinrich R. Nitric oxide/cGMP signaling in the corpora allata of female grasshoppers. Journal of Insect Physiology 2011, 57:94-107.
122. 3 cells. Biochemical Pharmacology 2000, 60:251-262.
123. Yamada K., Xu Z.Q., Zhang X., Gustafsson L., Hulting A.L., de Vente J., Steinbusch H.W., Hökfelt T. Nitric oxide synthase and cGMP in the anterior pituitary gland: effect of a GnRH antagonist and nitric oxide donors. Neuroendocrinology 1997, 65:147-156.
124. Yamazaki F., Donaldson E.M. The effects of partially purified salmon pituitary gonadotropin on spermatogenesis, vitellogenesis, and ovulation in hypophysectomised goldfish (Carassius auratus). General and Comparative Endocrinology 1968, 11:292-299.
125. Zayas R.M., Qazi S., Morton D.B., Trimmer B.A. Neurons involved in nitric oxide mediated cGMP signalling in the tobacco hornworm, Manduca sexta. The Journal of Comparative Neurology 2000, 419:422-438.
126. Zhu M., Gleiberman A.S., Rosenfeld M.G. Molecular physiology of pituitary development; signalling and transcriptional networks. Physiology Reviews 2007, 87:933-963.