Aromatase regulates aggression in the African cichlid fish Astatotilapia burtoni

Physiology and Behavior

Volumn 112-113, Issue , 2013, Pages 77-83

  Huffman, Lin S ^a   O'Connell, Lauren A ^a   Hofmann, Hans A ^a  

^a UNIVERSITY OF TEXAS AT AUSTIN   (United States)

Author keywords

Aggression; Aromatase; Estrogen; Fadrozole; Testosterone

Indexed keywords

AROMATASE; ESTRADIOL; FADROZOLE; SODIUM CHLORIDE; TESTOSTERONE;

AGGRESSION; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; ASTATOTILAPIA BURTONI; CONTROLLED STUDY; FISH; MALE; MOLECULAR MECHANICS; NONHUMAN; PHYSIOLOGY; PREOPTIC AREA; PRIORITY JOURNAL; PROTEIN EXPRESSION; REPRODUCTION; TREATMENT RESPONSE;

EID: 84875533752     PISSN: 00319384     EISSN: 1873507X     Source Type: Journal    
DOI: 10.1016/j.physbeh.2013.02.004     Document Type: Article

References (58)

1. Adkins E.K., Bop J.J., Koutnik D.L., Morris J.B., Pniewski E.E. Further evidence that androgen aromatization is essential for the activation of copulation in male quail. Physiol Behav 1980, 24:441-446.
2. Afonso L.O.B., Iwama G.K., Smith J., Donaldson E.M. Effects of the aromatase inhibitor fadrozole on plasma sex steroid secretion and ovulation rate in female Coho salmon, Oncorhynchus kisutch, close to final maturation. Gen Comp Endocrinol 1999, 113:221-229.
3. Balthazart J., Baillien M., Cornil C.A., Ball G.F. Preoptic aromatase modulates male sexual behavior: slow and fast mechanisms of action. Physiol Behav 2004, 83:247-270.
4. Balthazart J., Baillien M., Ball G.F. Rapid and reversible inhibition of brain aromatase activity. J Neuroendocrinol 2001, 13:63-73.
5. Benjamini Y., Hochberg Y. Controlling the false discovery rate: a practical and powerful approach to multiple testing. J R Stat Soc B Methodol 1995, 57:289-300.
6. Black M.P., Balthazart J., Baillien M., Grober M.S. Socially induced and rapid increases in aggression are inversely related to brain aromatase activity in a sex- changing fish, Lythrypnus dalli. Proc Biol Sci 2005, 272:2435-2440.
7. Borg B., Timmers R.J., Lambert J.G. Aromatase activity in the brain of the three-spined stickleback, Gasterosteus aculeatus. I. Distribution and effects of season and photoperiod. Exp Biol 1987, 47:63-68.
8. Crews D., Bergeron J.M., Flores D., Bull J.J., Skipper J.K., Tousignant A., et al. Temperature-dependent sex determination in reptiles: proximate mechanisms, ultimate outcomes, and practical applications. Dev Genet 1994, 15:297-312.
9. Diotel N., Le Page Y., Mouriec K., Tong S.K., Pellegrini E., Vaillant C., et al. Aromatase in the brain of teleost fish: expression, regulation and putative functions. Front Neuroendocrinol 2010, 31:172-192.
10. Fernald R.D. Quantitative behavioural observations of Haplochromis burtoni under semi-natural conditions. Anim Behav 1977, 25:643-653.
11. Fernald R.D., Hirata N.R. Field study of Haplochromis burtoni: quantitative behavioural observations. Anim Behav 1977, 25:964-975.
12. Forlano P.M., Deitcher D.L., Myers D.A., Bass A.H. Anatomical distribution and cellular basis for high levels of aromatase activity in the brain of teleost fish: aromatase enzyme and mRNA expression identify glia as source. J Neurosci 2001, 21:8943-8955.
13. Forlano P.M., Bass A.H. Seasonal plasticity of brain aromatase mRNA expression in glia: divergence across sex and vocal phenotypes. J Neurobiol 2005, 65:37-49.
14. Forlano P.M., Schlinger B.A., Bass A.H. Brain aromatase: new lessons from non- mammalian vertebrate systems. Front Neuroendocrinol 2006, 27:247-274.
15. Goncalves D., Alpedrinha J., Teles M., Oliveira R.F. Endocrine control of sexual behavior in sneaker males of the peacock blenny Salaria pavo: effects of castration, aromatase inhibition, testosterone and estradiol. Horm Behav 2007, 51:534-541.
16. Goncalves D., Teles M., Alpedrinha J., Oliveira R.F. Brain and gonadal aromatase activity and steroid hormone levels in female and polymorphic males of the peacock blenny Salaria pavo. Horm Behav 2008, 54:717-725.
17. Gonzalez A., Piferrer F. Aromatase activity in the European sea bass (Dicentrarchus labrax L.) brain. Distribution and changes in relation to age, sex, and the annual reproductive cycle. Gen Comp Endocrinol 2003, 132:223-230.
18. Handa R.J., Pak T.R., Kudwa A.E., Lund T.D., Hinds L. An alternate pathway for androgen regulation of brain function: activation of estrogen receptor beta by the metabolite of dihydrotestosterone, 5α-androstane-3β, 17β-diol. Horm Behav 2008, 53:741-752.
19. Hoke K.L., Burmeister S.S., Fernald R.D., Rand A.S., Ryan M.J., Wilczynski W. Functional mapping of the auditory midbrain during mate call reception. J Neurosci 2004, 24:11264-11272.
20. Huffman L.S., Mitchell M.M., O'Connell L.A., Hofmann H.A. Rising StARs: behavioral, hormonal, and molecular responses to social challenge and opportunity. Horm Behav 2012, 61:631-641.
21. Kidd C.E., Kidd M.R., Hofmann H.A. Measuring multiple hormones from a single water sample using enzyme immunoassays. Gen Comp Endocrinol 2010, 165:277-285.
22. Kwon J.Y., McAndrew B.J., Penman D.J. Cloning of brain aromatase gene and expression of brain and ovarian aromatase genes during sexual differentiation in genetic male and female Nile tilapia Oreochromis niloticus. Mol Reprod Dev 2001, 59:359-370.
23. Liang K., Zeger S.L. Longitudinal data analysis using generalized linear models. Biometrika 1986, 73:13-22.
24. McDonald P.G., Beyer C., Newton F., Brien B., Baker R., Tan H.S., et al. Failure of 5a-dihydrotestosterone to initiate sexual behavior in the castrated male rat. Nature 1970, 227:964-965.
25. McEwen B.S. Neural gonadal steroid actions. Science 1981, 211:1303-1311.
26. Melo A.C., Ramsdell J.S. Sexual dimorphism of brain aromatase activity in medaka: induction of a female phenotype by estradiol. Environ Health Perspect 2001, 109:257-264.
27. Menuet A., Anglade I., Le Guevel R., Pellegrini E., Pakdel F., Kah O. Distribution of aromatase mRNA and protein in the brain and pituitary of female rainbow trout: comparison with estrogen receptor alpha. J Comp Neurol 2003, 462:180-193.
28. Moore F.L., Lowry C.A. Comparative neuroanatomy of vasotocin and vasopressin in amphibians and other vertebrates. Comp Biochem Physiol C 1998, 119:251-260.
29. Munchrath L.A., Hofmann H.A. Distribution of androgen, estrogen, and progesterone receptors in the brain of an African cichlid fish, Astatotilapia burtoni. J Comp Neurol 2010, 518:3302-3326.
30. Newman S. The medial extended amygdala in male reproductive behavior. A node in the mammalian social behavior network. Ann N Y Acad Sci 1999, 877:242-257.
31. O'Connell L.A., Hofmann H.A. The vertebrate mesolimbic reward system and social behavior network: a comparative synthesis. J Comp Neurol 2011, 519:3599-3639.
32. O'Connell L.A., Hofmann H.A. Genes, hormones, and circuits: an integrative approach to study the evolution of social behavior. Front Neuroendocrinol 2011, 32:320-335.
33. O'Connell L.A., Hofmann H.A. Social status predicts how sex steroid receptors regulate complex behavior across levels of biological organization. Endocrinology 2012, 153:1341-1351.
34. Parikh V.N., Clement T.S., Fernald R.D. Androgen level and male social status in the African cichlid, Astatotilapia burtoni. Behav Brain Res 2006, 166:291-295.
35. Pasmanik M., Callard G.V. A high abundance androgen receptor in goldfish brain: characteristics and seasonal changes. Endocrinology 1988, 123:1162-1171.
36. Renn S.C.P., Aubin-Horth N., Hofmann H.A. Fish & chips: functional genomics of social plasticity in an African cichlid fish. J Exp Biol 2008, 211:3041-3056.
37. Roselli C.E., Salisbury R.L., Resko J.A. Genetic evidence for androgen-dependent and independent control of aromatase activity in the rat brain. Endocrinology 1987, 121:2205-2210.
38. Schlinger B.A., Callard G.V. Aromatization mediates aggressive behavior in quail. Gen Comp Endocrinol 1990, 79:39-53.
39. Schlinger B.A., Greco C., Bass A.H. Aromatase activity in the hindbrain vocal control region of a teleost fish: divergence among males with alternative reproductive tactics. Proc R Soc Lond B Biol Sci 1999, 266:131-136.
40. Simpson E.R. Sources of estrogen and their importance. J Steroid Biochem Mol Biol 2003, 86:225-230.
41. Soma K.K., Francis R.C., Wingfield J.C., Fernald R.D. Androgen regulation of hypothalamic neurons containing gonadotropin-releasing hormone in a cichlid fish: integration with social cues. Horm Behav 1996, 30:216-226.
42. Soma K.K., Tramontin A.D., Wingfield J.C. Oestrogen regulates male aggression in the non-breeding season. Proc R Soc Lond B Biol Sci 2000, 267:1089-1096.
43. Strobl-Mazzulla P.H., Moncaut N.P., Lopez G.C., Miranda L.A., Canario A.V., Somoza G.M. Brain aromatase from pejerrey fish (Odontesthes bonariensis): cDNA cloning, tissue expression, and immunohistochemical localization. Gen Comp Endocrinol 2005, 143:21-32.
44. Trainor B.C., Greiwe K.M., Nelson R.J. Individual differences in estrogen receptor alpha in select brain nuclei are associated with individual differences in aggression. Horm Behav 2006, 50:338-345.
45. Trainor B.C., Kyomen H.H., Marler C.A. Estrogenic encounters: how interactions between aromatase and the environment modulate aggression. Front Neuroendocrinol 2006, 27:170-179.
46. Wade J., Schlinger B.A., Hodges L., Arnold A.P. Fadrozole: a potent and specific inhibitor of aromatase in the zebra finch brain. Gen Comp Endocrinol 1994, 94:53-61.
47. Zumpe D., Bonsall R.W., Michael R.P. Effects of the nonsteroidal aromatase inhibitor, fadrozole, on the sexual behavior of male cynomolgus monkeys (Macaca fascicularis). Horm Behav 1993, 27:200-215.
48. Burmeister S.S., Jarvis E.D., Fernald R.D. Rapid behavioral and genomic responses to social opportunity. PLoS Biol 2005, 3:e363.
49. Maruska K.P., Fernald R.D. Behavioral and physiological plasticity: rapid changes during social ascent in an African cichlid fish. Horm Behav 2010, 58:230-240.
50. Renn S.C.P., Fraser E.J., Aubin-Horth N., Trainer B.C., Hofmann H.A. Females of an African cichlid fish display male-typical social dominance behavior and elevated androgens in the absence of males. Horm Behav 2012, 61:496-503.
51. Trainor B.C., Hofmann H.A. Somatostatin regulates aggressive behavior in an African cichlid fish. Endocrinol 2006, 147:5119-5125.
52. Hofmann HA, Benson ME, Fernald RD. Social status regulates growth rate: Consequences for life-history strategies. Proc Nat Acad Sci U S A 199;95:14171-6.
53. Burmeister S.S., Mangiamele L.A., Lebonville C.L. Acoustic modulation of immediate early gene expression in the auditory midbrain of female túngara frogs. Brain Res 2008, 1190:105-114.
54. Ankley G.T., Kahl M.D., Jensen K.M., Hornung M.W., Korte J.J., Makynen E.A., et al. Evaluation of the aromatase inhibitor fadrozole in a short-term reproduction assay with the fathead minnow (Pimephales promelas). Toxicol Sci 2002, 67:121-130.
55. Trainor B.C., Bird I.M., Marler C.A. Opposing hormonal mechanisms of aggression revealed through short-lived testosterone manipulations and multiple winning experiences. Horm Behav 2004, 45:115-121.
56. Demski L.S., Knigge K.M. The telencephalon and hypothalamus of the bluegill (Lepomis macrochirus): evoked feeding, aggressive and reproductive behavior with representative frontal sections. J Comp Neurol 1971, 143:1-16.
57. Satou M., Oka Y., Kusunoki M., Matsushima T., Kato M., Fujita I., et al. Telencephalic and preoptic areas integrate sexual behavior in hime salmon (landlocked red salmon, Oncorhynchus nerka): results of electrical brain stimulation experiments. Physiol Behav 1984, 33:441-447.
58. Greenwood A.K., Wark A.R., Fernald R.D., Hofmann H.A. Expression of arginine vasotocin in distinct preoptic regions is associated with dominant and subordinate behaviour in an African cichlid fish. Proc Biol Sci 2008, 275:2393-2402.