Cortisol and corticosterone in immune organs and brain of European starlings: Developmental changes, effects of restraint stress, comparison with zebra finches

American Journal of Physiology - Regulatory Integrative and Comparative Physiology

Volumn 297, Issue 1, 2009, Pages

  Schmidt, Kim L ^a   Chin, Eunice H ^a   Shah, Amit H ^a   Soma, Kiran K ^a  

^a UNIVERSITY OF BRITISH COLUMBIA   (Canada)

Author keywords

Altricial; Avian; Bird; Bursa of Fabricius; Development; Diencephalon; Glucocorticoid; Immune system; Immunosteroid; Lymphocyte; Nervous system; Neurosteroid; Songbird; Spleen; Stress hyporesponsive period; Thymus

Indexed keywords

CORTICOSTERONE; GLUCOCORTICOID; HYDROCORTISONE;

ADRENAL GLAND; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BIRD; BRAIN; CONTROLLED STUDY; CORTICOSTERONE BLOOD LEVEL; DIENCEPHALON; FEMALE; HYDROCORTISONE BLOOD LEVEL; IMMOBILIZATION STRESS; MALE; NONHUMAN; PRIORITY JOURNAL; STARLING; THYMUS;

AGE FACTORS; ANIMALS; BRAIN; BURSA OF FABRICIUS; CORTICOSTERONE; FEMALE; FINCHES; HYDROCORTISONE; LYMPHOID TISSUE; MALE; RESTRAINT, PHYSICAL; SPECIES SPECIFICITY; SPLEEN; STARLINGS; STRESS, PSYCHOLOGICAL; THYMUS GLAND;

EID: 67650034874     PISSN: 03636119     EISSN: 15221490     Source Type: Journal    
DOI: 10.1152/ajpregu.90964.2008     Document Type: Article

References (67)

1. Ardia D.R. Cross-fostering reveals an effect of spleen size and nest temperatures on immune responses in nestling European starlings Oecologia 2005 145 2 327-334 DOI 10.1007/s00442-005-0120-6 1. Ardia DR. Cross-fostering reveals an effect of spleen size, and nest temperatures on immune responses in nestling European starlings. Oecologia 45: 327-334, 2005. (Pubitemid 41530080)
2. Aste N, Watanabe Y, Shimada K, Saito N. Sex-, and age-related variation in neurosteroidogenic enzyme mRNA levels during quail embryonic development. Brain Res 1201: 15-22, 2008.
3. Beyenburg S. Watzka M. Clusmann H. Blumcke I. Bidlingmaier F. Elger C.E. Stoffel-Wagner B. Messenger RNA of steroid 21-hydroxylase (CYP21) is expressed in the human hippocampus Neuroscience Letters 2001 308 2 111-114 DOI 10.1016/S0304-3940(01)01991-7, PII S0304394001019917 3. Beyenburg S, Watzka M, Clusmann H, Blümcke I, Bidlingmaier F, Elger CE, Stoffel-Wagner B. Messenger RNA of steroid 21-hydroxylase (CYP21) is expressed in the human hippocampus. Neurosci Lett 308: 111-114, 2001. (Pubitemid 32703680)
4. Bourgeon S. Raclot T. Corticosterone selectively decreases humoral immunity in female eiders during incubation Journal of Experimental Biology 2006 209 24 4957-4965 DOI 10.1242/jeb.02610 4. Bourgeon S, Raclot T. Corticosterone selectively decreases humoral immunity in female eiders during incubation. J Exp Biol 209: 4957-4965, 2006. (Pubitemid 46166723)
5. Buchanan K.L. Leitner S. Spencer K.A. Goldsmith A.R. Catchpole C.K. Developmental stress selectively affects the song control nucleus HVC in the zebra finch Proceedings of the Royal Society B: Biological Sciences 2004 271 1555 2381-2386 DOI 10.1098/rspb.2004.2874 5. Buchanan KL, Leitner S, Spencer KA, Goldsmith AR, Catchpole CK. Developmental stress selectively affects the song control nucleus HVC in the zebra finch. Proc Biol Sci 271: 2381-2386, 2004. (Pubitemid 40502665)
6. Buchanan K.L. Spencer K.A. Goldsmith A.R. Catchpole C.K. Song as an honest signal of past developmental stress in the European starling (Sturnus vulgaris) Proceedings of the Royal Society B: Biological Sciences 2003 270 1520 1149-1156 DOI 10.1098/rspb.2003.2330 6. Buchanan KL, Spencer KA, Goldsmith AR, Catchpole CK. Song as an honest signal of past developmental stress in the European starling (Sturnus vulgaris). Proc Biol Sci 270: 1149-1156, 2003. (Pubitemid 36683459)
7. Butte JC, Kakihana R, Farnham ML, Noble EP. The relationship between brain and plasma corticosterone stress response in developing rats. Endocrinology 92: 1775-1779, 1973.
8. Cabe PR. European starling (Sturnus vulgaris). In: The Birds of North America, edtied by Poole A and Gill F. Philadelphia: The Academy of Natural Sciences and Washington, DC: The American Ornithologists' Union, 1993, vol.48.
9. Chin EH, Shah AH, Schmidt KL, Sheldon LD, Love OP, Soma KK. Sex differences in DHEA and estradiol during development in a wild songbird: jugular versus brachial plasma. Horm Behav 54: 194-202, 2008.
10. Cohen J. Statistical Power Analysis for the Behavioral Sciences. rev. ed. New York: Academic Press, 1977.
11. Corpechot C. Robel P. Axelson M. Characterization and measurement of dehydroepiandrosterone sulfate in rat brain Proceedings of the National Academy of Sciences of the United States of America 1981 78 8 I 4704-4707 11. Corpechot C, Robel P, Axelson M, Sjovall J, Baulieu E. Characterization and measurement of dehydroepiandrosterone sulfate in rat brain. Proc Natl Acad Sci USA 78: 4704-4707, 1981. (Pubitemid 12225548)
12. Croft AP, O'Callaghan MJ, Shaw SG, Connolly G, Jacquot C, Little HJ. Effects of minor laboratory procedures, adrenalectomy, social defeat or acute alcohol on regional brain concentrations of corticosterone. Brain Res 1238: 12-22, 2008.
13. Davies E, MacKenzie SM. Extra-adrenal production of corticosteroids. Clin Exp Pharmacol Physiol 30: 437-445, 2003.
14. Dawson A, Howe PD. Plasma corticosterone in wild starlings (Sturnus vulgaris) immediately following capture and in relation to body weight during the annual cycle. Gen Comp Endocrinol 51: 303-308, 1983.
15. Dawson A. McNaughton F.J. Puberty in European starlings: can nestlings perceive daylength? Ornis Scandinavica 1992 23 3 209-213 15. Dawson A, McNaughton FJ. Puberty in European starlings: can nestlings perceive daylength? Ornis Scandinavica, 23: 209-213, 1992. (Pubitemid 23403784)
16. Droste S.K. De Groote L. Atkinson H.C. Lightman S.L. Reul J.M.H.M. Linthorst A.C.E. Corticosterone levels in the brain show a distinct ultradian rhythm but a delayed response to forced swim stress Endocrinology 2008 149 7 3244-3253 http://endo.endojournals.org/cgi/reprint/149/7/3244 DOI 10.1210/en.2008-0103 16. Droste SK, de Groote L, Atkinson HC, Lightman SL, Reul JM, Linthorst AC. Corticosterone levels in the brain show a distinct ultradian rhythm but a delayed response to forced swim stress. Endocrinology 149: 3244-3253, 2008. (Pubitemid 351919572)
17. Gomez-Sanchez CE, Zhou MY, Cozza EN, Morita H, Foecking MF, Gomez-Sanchez EP. Aldosterone biosynthesis in the rat brain. Endocrinology 138: 3369-3373, 1997.
18. Herold MJ, McPherson KG, Reichardt HM. Glucocorticoids in T cell apoptosis, function. Cell Mol Life Sci 63: 60-72, 2006.
19. Hodgson Z.G. Meddle S.L. Roberts M.L. Buchanan K.L. Evans M.R. Metzdorf R. Gahr M. Healy S.D. Spatial ability is impaired and hippocampal mineralocorticoid receptor mRNA expression reduced in zebra finches (Taeniopygia guttata) selected for acute high corticosterone response to stress Proceedings of the Royal Society B: Biological Sciences 2007 274 1607 239-245 DOI 10.1098/rspb.2006.3704 19. Hodgson ZG, Meddle SL, Roberts ML, Buchanan KL, Evans MR, Metzdorf R, Gahr M, Healy SD. Spatial ability is impaired and hippocampal mineralcorticoid receptor mRNA expression reduced in zebra finches (Taeniopygia guttata) selected for acute high corticosterone response to stress. Proc Biol Sci 274: 239-245, 2007. (Pubitemid 47055480)
20. Karssen A.M. Meijer O.C. Van Der Sandt I.C.J. Lucassen P.J. De Lange E.C.M. De Boer A.G. De Kloet E.R. Multidrug resistance P-glycoprotein hampers the access of cortisol but not of corticosterone to mouse and human brain Endocrinology 2001 142 6 2686-2694 DOI 10.1210/en.142.6.2686 20. Karssen AM, Meijer OC, Van der Sandt CJ, Lucassen PJ, De Lange ECM, De Boer AG, De Kloet ER. Multidrug resistance P glycoprotein hampers the access of cortisol but not of corticosterone to mouse and human Brain. Endocrinology 142: 2686-2694, 2001. (Pubitemid 32473126)
21. Katz A. Heiblum R. Meidan R. Robinzon B. Distinct features of dehydrocorticosterone reduction into corticosterone in the liver and duodenum of the domestic fowl (Gallus gallus domesticus) General and Comparative Endocrinology 2007 154 1 3 67-74 DOI 10.1016/j.ygcen.2007.06.015, PII S0016648007002420 21. Katz A, Heiblum R, Meidan R, Robinzon B. Distinct features of dehydrocorticosterone reduction into corticosterone in the liver and duodenum of the domestic fowl (Gallus gallus domesticus). Gen Comp Endocrinol 154: 67-74, 2007. (Pubitemid 47362122)
22. Lechner O. Dietrich H. Wiegers G.J. Vacchio M. Wick G. Glucocorticoid production in the chicken bursa and thymus International Immunology 2001 13 6 769-776 22. Lechner O, Dietrich H, Wiegers GJ, Vacchio M, Wick G. Glucocorticoid production in the chicken bursa and thymus. Int Immunol 13: 769-776, 2001. (Pubitemid 32514701)
23. Lee KA, Klasing KC. A role for immunology in invasion biology. Trends Ecol Evol 19: 523-529, 2004.
24. Lee K.A. Wikelski M. Robinson W.D. Robinson T.R. Klasing K.C. Constitutive immune defences correlate with life-history variables in tropical birds Journal of Animal Ecology 2008 77 2 356-363 DOI 10.1111/j.1365-2656.2007. 01347.x 24. Lee KA, Wikelski M, Robinson WD, Robinson TR, Klasing KC. Constitutive immune defenses correlate with life-history variables in tropical birds. J Anim Ecol 77: 356-363, 2008. (Pubitemid 351191060)
25. Levine S. The ontogeny of the hypothalamic-pituitary-adrenal axis. The influence of maternal factors Annals of the New York Academy of Sciences 1994 746 275-288 25. Levine S. The ontogeny of the hypothalamic-pituitary-adrenal axis. The influence of maternal factors. Ann NY Acad Sci 30: 275-288, 1994. (Pubitemid 26005903)
26. Loiseau C. Sorci G. Dano S. Chastel O. Effects of experimental increase of corticosterone levels on begging behavior, immunity and parental provisioning rate in house sparrows General and Comparative Endocrinology 2008 155 1 101-108 DOI 10.1016/j.ygcen.2007.03.004, PII S0016648007001116 26. Loiseau C, Sorci G, Dano S, Chastel O. Effects of experimental increase of corticosterone levels on begging behavior, immunity, and parental provisioning rate in house sparrows. Gen Comp Endocrinol 155: 101-108, 2008. (Pubitemid 350122475)
27. London S.E. Schlinger B.A. Steroidogenic enzymes along the ventricular proliferative zone in the developing songbird brain Journal of Comparative Neurology 2007 502 4 507-521 DOI 10.1002/cne.21335 27. London SE, Schlinger BA. Steroidogenic enzymes along the ventricular proliferative zone in the developing songbird brain. J Comp Neurol 502: 507-521, 2007. (Pubitemid 46732505)
28. Love OP, Breuner CW, Vézina F, Williams TD. Mediation of a corticosterone-induced reproductive conflict. Horm Behav 46: 59-65, 2004.
29. MacDonald I.F. Kempster B. Zanette L. MacDougall-Shackleton S.A. Early nutritional stress impairs development of a song-control brain region in both male and female juvenile song sparrows (Melospiza melodia) at the onset of song learning Proceedings of the Royal Society B: Biological Sciences 2006 273 1600 2559-2564 DOI 10.1098/rspb.2006.3547 29. MacDonald IF, Kempster B, Zanette L, MacDougall-Shackleton SA. Early nutritional stress impairs development of a song-control brain region in both male and female juvenile song sparrows (Melospiza melodia) at the onset of song learning. Proc Biol Sci 273: 2559-2564, 2006. (Pubitemid 44439678)
30. MacKenzie S.M. Clark C.J. Fraser R. Gomez-Sanchez C.E. Connell J.M.C. Davies E. Expression of 11β-hydroxylase and aldosterone synthase genes in the rat brain Journal of Molecular Endocrinology 2000 24 3 321-328 30. MacKenzie SM, Clark CJ, Fraser R, Gómez-Sánchez CE, Connell JMC, Davies E. Expression of 11β-hydroxylase and aldosterone synthase genes in the rat brain. J Mol Endocrinol 24: 321-328, 2000. (Pubitemid 30415006)
31. MacKenzie S.M. Clark C.J. Ingram M.C. Lai M. Seckl J. Gomez-Sanchez C.E. Fraser R. Connell J.M.C. Davies E. Corticosteroid production by fetal rat hippocampal neurons Endocrine Research 2000 26 4 531-535 31. MacKenzie SM, Clark CJ, Ingram MC, Lai M, Seckl J, Gomez-Sanchez CE, Fraser R, Connell JM, Davies E. Corticosteroid production by fetal rat hippocampal neurons. Endocr Res 26: 531-535, 2000. (Pubitemid 32053069)
32. Martin 2nd LB, Hasselquist D, Wikelski M. Investment in immune defense is linked to pace of life in house sparrows. Oecologia 147: 565-575, 2006.
33. Martin 2nd LB, Weil ZM, Nelson RJ. Immune defense, and reproductive pace of life in Peromyscus mice. Ecology 88: 2516-2528, 2007.
34. McDade T.W. Life history, maintenance, and the early origins of immune function American Journal of Human Biology 2005 17 1 81-94 DOI 10.1002/ajhb.20095 34. McDade TW. Life history, maintenance, and the early origins of immune function. Am J Hum Biol 17: 81-94, 2005. (Pubitemid 40214397)
35. Mellon S.H. Deschepper C.F. Neurosteroid biosynthesis: Genes for adrenal steroidogenic enzymes are expressed in the brain Brain Research 1993 629 2 283-292 DOI 10.1016/0006-8993(93)91332-M 35. Mellon SH, Deschepper CF. Neurosteroid biosynthesis: genes for adrenal steroidogenic enzymes are expressed in the brain. Brain Res 629: 283-292, 1993. (Pubitemid 23337803)
36. Moller A.P. Evidence of larger impact of parasites on hosts in the tropics: Investment in immune function within and outside the tropics Oikos 1998 82 2 265-270 36. Moller AP. Evidence of larger impact of parasites on host in the tropics: investment in immune function within, and outside the tropics. OIKOS 82: 265-270, 1998. (Pubitemid 28336109)
37. Moller A.P. Merino S. Brown C.R. Robertson R.J. Immune defense and host sociality: A comparative study of swallows and martins American Naturalist 2001 158 2 136-145 DOI 10.1086/321308 37. Moller AP, Merino S, Brown CR, Robertson RJ. Immune defense and host sociality: a comparative study of swallows and martins. Am Nat 158: 136-145, 2001. (Pubitemid 32682540)
38. Moller A.P. Erritzoe J. Parasite virulence and host immune defense: Host immune response is related to nest reuse in birds Evolution 1996 50 5 2066-2072 38. Moller AP, Erritzoe J. Parasite virulence and host immune defense: host immune response is related to nest reuse in birds. Evolution 50: 2066-2072, 1996. (Pubitemid 26394296)
39. Newman A.E.M. Chin E.H. Schmidt K.L. Bond L. Wynne-Edwards K.E. Soma K.K. Analysis of steroids in songbird plasma and brain by coupling solid phase extraction to radioimmunoassay General and Comparative Endocrinology 2008 155 3 503-510 DOI 10.1016/j.ygcen.2007.08.007, PII S001664800700305X 39. Newman AEM, Chin EH, Schmidt KL, Bond L, Wynne-Edwards KE, Soma KK. Analysis of steroids in songbird plasma and brain by coupling solid phase extraction to radioimmunoassay. Gen Comp Endocrinol 155: 503-510, 2008a. (Pubitemid 351191907)
40. Newman A.E.M. Pradhan D.S. Soma K.K. Dehydroepiandrosterone and corticosterone are regulated by season and acute stress in a wild songbird: Jugular versus brachial plasma Endocrinology 2008 149 5 2537-2545 http://endo.endojournals.org/cgi/reprint/149/5/2537 DOI 10.1210/en.2007-1363 40. Newman AEM, Pradhan DS, Soma KK. DHEA and corticosterone are regulated by season and acute stress in a wild songbird: jugular versus brachial plasma. Endocrinology 149: 2537-2545, 2008b. (Pubitemid 351574498)
41. Newman AEM, Soma KK. Corticosterone and DHEA in songbird plasma and brain: effects of season and acute stress. Eur J Neurosci 149: in press, 2009.
42. Pazirandeh A. Jondal M. Okret S. Conditional expression of a glucocorticoid receptor transgene in thymocytes reveals a role for thymic-derived glucocorticoids in thymopoiesis in vivo Endocrinology 2005 146 6 2501-2507 DOI 10.1210/en.2004-0943 42. Pazirandeh A, Jondal M, Okret S. Conditional expression of a glucocorticoid receptor transgene in thymocytes reveals a role for thymic-derived glucocorticoids in thymopoiesis in vivo. Endocrinology 146: 2501-2507, 2005. (Pubitemid 40695550)
43. Petrini M, Galimberti S, Sabbatini A, Bianchi F, Bernardini N, Dolfi A, Lupetti M. Expression of multidrug resistance (mdr) gene(s) in primary lymphoid organs of chicken immune system during embryonic development. Experientia 51: 137-140, 1995.
44. Pradhan D.S. Yu Y. Soma K.K. Rapid estrogen regulation of DHEA metabolism in the male and female songbird brain Journal of Neurochemistry 2008 104 1 244-253 DOI 10.1111/j.1471-4159.2007.04953.x 44. Pradhan DS, Yu Y, Soma KK. Rapid estrogen regulation of DHEA metabolism in the male and female songbird brain. J Neurochem 104: 244-253, 2008. (Pubitemid 350265052)
45. Qiao S, Chen L, Okret S, Jondal M. Age-related synthesis of glucocorticoids in thymocytes. Exp Cell Res 314: 3027-3035, 2008.
46. Ricklefs RE, Wikelski M. The physiology/life-history nexus. Trends Ecol Evol 17: 462-468, 2002.
47. Romero L.M. Reed J.M. Collecting baseline corticosterone samples in the field: Is under 3 min good enough? Comparative Biochemistry and Physiology - A Molecular and Integrative Physiology 2005 140 1 73-79 DOI 10.1016/j.cbpb.2004. 11.004, PII S1095643304003095 47. Romero LM, Reed JM. Collecting baseline corticosterone samples in the field: is under 3 min good enough? Comp Biochem Physiol A Mol Integr Physiol 140: 73-79, 2005. (Pubitemid 40139157)
48. Romero L.Michael Remage-Healey L. Daily and seasonal variation in response to stress in captive starlings (Sturnus vulgaris): Corticosterone General and Comparative Endocrinology 2000 119 1 52-59 DOI 10.1006/gcen.2000. 7491 48. Romero LM, Remage-Healey L. Daily and seasonal variation in response to stress in captive starlings (Sturnus vulgaris): corticosterone. Gen Comp Endocrinol 119: 52-59, 2000. (Pubitemid 30640234)
49. Rubolini D. Romano M. Boncoraglio G. Ferrari R.P. Martinelli R. Galeotti P. Fasola M. Saino N. Effects of elevated egg corticosterone levels on behavior, growth, and immunity of yellow-legged gull (Larus michahellis) chicks Hormones and Behavior 2005 47 5 592-605 DOI 10.1016/j.yhbeh.2005.01.006 49. Rubolini D, Romano M, Boncoraglio G, Ferrari RP, Martinelli R, Galeotti P, Fasola M, Saino N. Effects of elevated egg corticosterone levels on behavior, growth, and immunity of yellow-legged gull (Larus michahellis) chicks. Horm Behav 47: 592-605, 2005. (Pubitemid 40462066)
50. Sapolsky R.M. Meaney M.J. Maturation of the adrenocortical stress response: Neuroendocrine control mechanisms and the stress hyporesponsive period Brain Research Reviews 1986 11 1 65-76 DOI 10.1016/0165-0173(86)90010-X 50. Sapolsky RM, Meaney MJ. Maturation of the adrenocortical stress response: neuroendocrine control mechanisms and the stress hyporesponsive period. Brain Res 396: 64-76, 1986. (Pubitemid 16126207)
51. Schmidt KL, Pradhan DS, Shah AS, Charlier TD, Chin EH, Soma KK. Neurosteroids, immunosteroids, and the Balkanization of endocrinology. Gen Comp Endocrinol 157: 266-274, 2008.
52. Schmidt KL, Soma KK. Cortisol and corticosterone in the songbird immune and nervous systems: local versus systemic levels during development. Am J Physiol Regul Integr Comp Physiol 295: R103-R110, 2008.
53. Seckl J.R. Walker B.R. Minireview: 11β-hydroxysteroid dehydrogenase type 1 - A tissue-specific amplifier of glucocorticoid action Endocrinology 2001 142 4 1371-1376 DOI 10.1210/en.142.4.1371 53. Seckl JR, Walker BR. Minireview: 11-hydroxysteroid dehydrogenase type 1-a tissue specific amplifier of glucocorticoid action. Endocrinology 142: 1371-1376, 2001. (Pubitemid 32299662)
54. Sims C.G. Holberton R.L. Development of the corticosterone stress response in young Northern Mockingbirds (Mimus polyglottos) General and Comparative Endocrinology 2000 119 2 193-201 DOI 10.1006/gcen.2000.7506 54. Sims CG, Holberton RC. Development of the corticosterone stress response in young northern mockingbirds (Mimus polyglottos). Gen Comp Endocrinol 19: 193-201, 2000. (Pubitemid 30651156)
55. Smits JEG, Bortolotti GR. Immunological development in nestling American Kestrels Falco sparverius: Posthatching ontogeny of the antibody response. Comp Biochem Physiol A Mol Integr Physiol 151: 711-716, 2008.
56. Soma K.K. Alday N.A. Hau M. Schlinger B.A. Dehydroepiandrosterone metabolism by 3β-hydroxysteroid dehydrogenase/γ5-γ4 isomerase in adult zebra finch brain: Sex difference and rapid effect of stress Endocrinology 2004 145 4 1668-1677 DOI 10.1210/en.2003-0883 56. Soma KK, Alday NA, Hau M, Schlinger BA. Dehydroepiandrosterone metabolism by 3β-hydroxysteroid dehydrogenase/Δ5-Δ4 isomerase in adult zebra finch brain: sex difference and rapid effect of stress. Endocrinology 45: 1668-1677, 2004. (Pubitemid 38402374)
57. Spencer KA, Buchanan KL, Goldsmith AR, Catchpole CK. Song as an honest signal of developmental stress in the zebra finch (Taeniopygia guttata). Horm Behav 44: 132-139, 2003.
58. Spencer K.A. Verhulst S. Delayed behavioral effects of postnatal exposure to corticosterone in the zebra finch (Taeniopygia guttata) Hormones and Behavior 2007 51 2 273-280 DOI 10.1016/j.yhbeh.2006.11.001, PII S0018506X06003163 58. Spencer KA, Verhulst S. Delayed behavioural effects of postnatal exposure to corticosterone in the zebra finch (Taeniopygia guttata). Horm Behav 51: 273-280, 2007. (Pubitemid 46072841)
59. Sreedevi B. LeFever L.J. Sommer-Wagner S.E. Jackwood D.J. Characterization of infectious bursal disease viruses from four layer flocks in the United States Avian Diseases 2007 51 4 845-850 http://avdi.allenpress.com/ pdfserv/10.1637%2F7923-020607-REGR1.1 DOI 10.1637/7923-020607-REGR1.1 59. Sreedevi B, LeFever LJ, Sommer-Wagner SE, Jackwood DJ. Characterization of infectious bursal disease viruses from four layer flocks in the United States. Avian Dis 51: 845-850, 2007. (Pubitemid 350291443)
60. Strömstedt M, Waterman MR. Messenger RNAs encoding steroidogenic enzymes are expressed in rodent brain. Brain Res Mol Brain Res 34: 75-88, 1995.
61. Ukena K. Usui M. Kohchi C. Tsutsui K. Cytochrome P450 side-chain cleavage enzyme in the cerebellar Purkinje neuron and its neonatal change in rats Endocrinology 1998 139 1 137-147 DOI 10.1210/en.139.1.137 61. Ukena K, Usui M, Kohchi C, Tsutsui K. Cytochrome P450 side-chain cleavage enzyme in the cerebellar Purkinje neuron and its neonatal change in rats. Endocrinology 139: 137-147, 1998. (Pubitemid 28166302)
62. Vacchio M.S. Ashwell J.D. King L.B. A positive role for thymus-derived steroids in formation of the T-cell repertoire Annals of the New York Academy of Sciences 1998 840 317-327 DOI 10.1111/j.1749-6632.1998.tb09571.x 62. Vacchio MS, Ashwell JD, King LB. A positive role for thymus-derived steroids in formation of the T-cell repertoire. Ann NY Acad Sci 840: 317-327, 1998. (Pubitemid 28302058)
63. Vacchio M.S. Papadopoulos V. Ashwell J.D. Steroid production in the thymus: Implications for thymocyte selection Journal of Experimental Medicine 1994 179 6 1835-1846 DOI 10.1084/jem.179.6.1835 63. Vacchio MS, Papadopoulos V, Ashwell JD. Steroid production in the thymus: implications for thymocyte selection. J Exp Med 179: 1835-1846, 1994. (Pubitemid 24155664)
64. Wada H. Hahn T.P. Breuner C.W. Development of stress reactivity in white-crowned sparrow nestlings: Total corticosterone response increases with age, while free corticosterone response remains low General and Comparative Endocrinology 2007 150 3 405-413 DOI 10.1016/j.ygcen.2006.10.002, PII S0016648006003224 64. Wada H, Hahn TP, Breuner CW. Development of stress reactivity in white-crowned sparrow nestlings: total corticosterone response increases with age, while free corticosterone response remains low. Gen Comp Endocrinol 150: 405-413, 2007. (Pubitemid 46037652)
65. Wang Y.S. Wang Z.C. Tang Y.D. Shi Z.L. He K.W. Li Y. Hou J.B. Yao H.C. Fan H.J. Lu C.P. Comparison of four infectious bursal disease viruses isolated from different bird species Archives of Virology 2007 152 10 1787-1797 DOI 10.1007/s00705-007-1022-1 65. Wang YS, Wang ZC, Tang YD, Shi ZL, He KW, Li Y, Hou JB, Yao HC, Fan HJ, Lu CP. Comparison of four infectious bursal disease viruses isolated from different bird species. Arch Virol 152: 1787-1797, 2007. (Pubitemid 47498142)
66. Ye P. Kenyon C.J. MacKenzie S.M. Nichol K. Seckl J.R. Fraser R. Connell J.M.C. Davies E. Effects of ACTH, dexamethasone, and adrenalectomy on 11β-hydroxylase (CYP11B1) and aldosterone synthase (CYP11B2) gene expression in the rat central nervous system Journal of Endocrinology 2008 196 2 305-311 DOI 10.1677/JOE-07-0439 66. Ye P, Kenyon CJ, Mackenzie SM, Nichol K, Seckl JR, Fraser R, Connell JM, Davies E. Effects of ACTH dexamethasone, and adrenalectomy on 11β-hydroxylase (CYP11B1) and aldosterone synthase (CYP11B2) gene expression in the rat central nervous system. J Endocrinol 196: 305-311, 2008. (Pubitemid 351298515)
67. Zann RE. The Zebra Finch: Synthesis of Field and Laboratory Studies. New York: Oxford University Press, 1996.