Seasonal aromatase activity in the brain of the male red-sided garter snake

Hormones and Behavior

Volumn 58, Issue 3, 2010, Pages 485-492

  Krohmer, Randolph W ^a   Boyle, Michael H ^a   Lutterschmidt, Deborah I ^c   Mason, Robert T ^b  

^a SAINT XAVIER UNIVERSITY   (United States)

^b OREGON STATE UNIVERSITY   (United States)

^c GEORGIA STATE UNIVERSITY   (United States)

Author keywords

Aromatase activity; Forebrain; Midbrain; Olfactory; Preoptic area; Reproduction; Reptile; Seasonal; Septum; Thamnophis sirtalis parietalis

Indexed keywords

ANDROGEN; AROMATASE; ESTROGEN; PHEROMONE; TESTOSTERONE;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ANTERIOR HYPOTHALAMUS; ARTICLE; AUTUMN; BRAIN FUNCTION; BRAIN REGION; BRAIN TISSUE; BREEDING; CONTROLLED STUDY; ENZYME ACTIVITY; GEOGRAPHIC DISTRIBUTION; HORMONE DETERMINATION; MALE; MESENCEPHALON; METABOLITE; MICRODISSECTION; NERVE CELL NETWORK; NONHUMAN; OLFACTORY CORTEX; PREOPTIC AREA; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; SEASON; SEASONAL VARIATION; SEXUAL BEHAVIOR; SNAKE; SPRING; WINTER;

ANIMALS; AROMATASE; BRAIN; COLUBRIDAE; COURTSHIP; FEMALE; MALE; SEASONS;

EID: 77955269216     PISSN: 0018506X     EISSN: 10956867     Source Type: Journal    
DOI: 10.1016/j.yhbeh.2010.04.011     Document Type: Article

References (74)

1. Aleksiuk M., Gregory P.T. Regulation of seasonal mating behavior in Thamnophis sirtalis parietalis. Copeia 1974, 1974:681-689.
2. Aste N., Panzica G.C., Aimar P., Viglietti-Panzica C., Foidart A., Balthazart J. Implications of testosterone metabolism in the control of the sexually dimorphic nucleus of the quail preoptic area. Brain Res. Bull. 1993, 99:601-611.
3. Bakker J., Honda S., Harada N., Balthazart J. The aromatase knock-out mouse provides new evidence that estradiol is required during development in the female for the expression of sociosexual behaviors in adulthood. J. Neurosci. 2002, 22:9104-9112.
4. Balthazart J., Taziaux M., Holloway K., Ball G.F., Cornil C. Behavioral effects of brain-derived estrogens in birds. Trends Comp. Endocrinol. Neurobiol.: Ann. N.Y. Acad. Sci. 2009, 1163:31-48.
5. Balthazart J. Steroid metabolism and the activation of social behavior. Advances in Comparative and Environmental Physiology, Vol 3 1989, 105-159. Springer Verlag, Berlin.
6. Balthazart J., Adkins-Regan E. Sexual differentiation of brain and behavior in birds. Hormones, Brain and Behavior, Vol 2 2002, 223-301. Academic Press, San Diego. D.W. Pfaff, A.P. Arnold, A.M. Etgen, S.E. Fahrbach, R.T. Rubin (Eds.).
7. Ball G.F., Balthazart J. Hormonal regulation of brain circuits mediating male sexual behavior in birds. Physiol. Behav. 2004, 83:329-346.
8. Ball G.F., Balthazart J. Neuroendocrine mechanisms regulating reproductive cycles and reproductive behavior in birds. Hormones Brain and Behavior, Vol 2 2002, 649-798. Academic Press, San Diego. D.W. Pfaff, A.P. Arnold, A.M. Etgen, S.E. Fahrbach, R.T. Rubin (Eds.).
9. Baum M.J. Activational and organizational effects of estradiol on male behavioral neuroendocrine function. Scand. J. Psychol. 2003, 44:213-220.
10. Beck L.A., Wade J. Effects of estradiol, sex and season on estrogen receptor alpha mRNA expression and forebrain morphology in adult green anole lizards. Neurosci. 2009, 160:577-586.
11. Beck L.A., Wade J. Morphology and estrogen receptor alpha mRNA expression in the developing green anole forebrain. J. Exp. Zool. 2009, 311:162-171.
12. Beck L.A., O'Bryant E.L., Wade J. Sex and seasonal differences in morphology of limbic forebrain nuclei in the green anole lizard. Brain Res. 2008, 127:68-75.
13. Bona-Gallo A., Licht P. Effect of temperature on sexual receptivity and ovarian recrudescence in the garter snake, Thamnophis sirtalis parietalis. Herpetologica 1983, 39:173-182.
14. Brennan P.A. The vomeronasal system. Cell. Mol. Life Sci. 2001, 58:546-555.
15. Callard G.V. Androgen and estrogen actions in the vertebrate brain. Am. Zool. 1983, 23:607-620.
16. Callard G.V., Petro Z., Ryan K.J. Identification of aromatase in the reptilian brain. Endocrinology 1977, 100:1214-1218.
17. Callard G.V., Petro Z., Ryan K.J. Phylogenetic distribution of aromatase and other androgen-converting enzymes in the central nervous system. Endocrinology 1978, 103:2283-2290.
18. Callard G.V., Petro Z., Ryan K.J. Conversion of androgen to estrogen and other steroids in the vertebrate brain. Am. Zool. 1978, 18:511-523.
19. Camazine B., Garstka W., Tokarz R., Crews D. Effects of castration and androgen replacement on male courtship behavior in the red-sided garter snake (Thamnophis sirtalis parietalis). Horm. Behav. 1980, 14:358-372.
20. Canick J.A., Ryan K.J. Cytochrome p-450 and the aromatization of 16α hydroxytestosterone and androstenedione by human placental microsomes. Mol. Cell. Endocrinol. 1976, 6:105-109.
21. Cherry J.A., Basham M.E., Weaver C.E., Krohmer R.W., Baum M.J. Ontogeny of the sexually dimorphic male nucleus in the preoptic/anterior hypothalamus of ferrets and its manipulation by gonadal steroids. J. Neurobiol. 1990, 21:844-847.
22. Crews D. Gamete production, sex steroid secretion and mating behavior uncoupled. Horm. Behav. 1984, 18:21-28.
23. Crews D., Silver R. Reproductive physiology and interactions in non-mammalian vertebrates. Handbook of Behavioral Neurobiology, Vol. 7 1985, 101-182. Plenum, New York. N. Alder, D.W. Pfaff, R.W. Goy (Eds.).
24. Crews D. Tran-seasonal action of androgen in the control of spring courtship in male red-sided garter snakes. Proc. Natl. Acad. Sci. 1991, 88:3545-3548.
25. Crews D., Camazine B., Diamond M., Mason R., Tokarz R., Gastka W.R. Hormonal independence of courtship behavior in the male garter snake. Horm. Behav. 1984, 18:29-41.
26. Foidart A., Reid J., Absil P., Yoshimura N., Harada N., Balthazart J. Critical re-examination of the distribution of aromatase-immunoreactive cells in the quail forebrain using antibodies raised against human placental aromatase and against the recombinant quail, mouse or human enzyme. J. Chem. Neuroant. 1995, 8:267-282.
27. Ford N.B. Seasonality of pheromone trailing behavior in two species of garter snake, Thamnophis (Colubridae). Southwest. Nat. 1981, 26:385-388.
28. Ford N.B. Species specificity of sex pheromone trails of sympatric and allopatric garter snakes (Thamnophis). Copeia 1982, 1982:10-13.
29. Friedman D., Crews D. Role of the anterior hypothalamus-preoptic area in the regulation of courtship behavior in the male Canadian red-sided garter snake (Thamnophis sirtalis parietalis): intracranial implantation experiments. Horm. Behav. 1985, 19:122-136.
30. Friedman D., Crews D. Role of the anterior hypothalamus-preoptic area in the regulation of courtship behavior in the male Canadian red-sided garter snake (Thamnophis sirtalis parietalis): lesion experiments. Behav. Neurosci. 1985, 99:942-949.
31. Garstka W.R., Camazine B., Crews D. Interaction of behavior and physiology during the annual reproductive cycle of the red-sided garter snake (Thamnophis sirtalis parietalis). Herpetologica 1982, 38:104-123.
32. Gobbetti A., Zerani M., DiForce M.M., Botte V. Relationships among GnRH, substance P, prostaglandins, sex steroids and aromatase activity in the brain of the male lizard Podarcis sicula sicula during reproduction. J. Rep. Fert. 1994, 101:523-529.
33. Gonçalves D., Saraiva J., Teles M., Teodósio R., Canário A.V.M., Oliveira R.F. Brain aromatase mRNA expression in two populations of the peacock blenny Salaria pavo with divergent mating systems. Horm. Behav. 2009, 57:155-161.
34. Halpern M. The telencephalon of snakes. Comparative Neurology of the Telencephalon 1980, 257-295. Plenum Press, New York. S.O.E. Ebbesson (Ed.).
35. Halpern M. Nasal chemical senses in reptiles: structure and function. Biology of the Reptilia. Physiology E: Hormones, Brain, and Behavior, Vol 18 1992, 423-523. University of Chicago Press. C. Gans, D. Crews (Eds.).
36. 3H-testosterone localization in the brains of garter snakes: an autoradiographic study. Gen. Comp. Endocrinol. 1982, 46:221-224.
37. Ingle D., Crews D. Vertebrate neuroethology: definitions and paradigms. Ann. Rev. Neurosci. 1985, 8:457-494.
38. Krohmer R.W., Baum M.J. Effects of sex, intrauterine position, and androgen manipulation on the development of the brain aromatase activity in fetal ferrets. J. Neuroendocrinol. 1989, 1:265-271.
39. Krohmer R.W., Crews D. Temperature activation of courtship behavior in the male red-sided garter snake (Thamnophis sirtalis parietalis): role of the anterior hypothalamus-preoptic area. Behav. Neurosci. 1987, 101:228-236.
40. Krohmer R.W., Crews D. Facilitation of courtship behavior in the male red-sided garter snake (Thamnophis sirtalis parietalis) following lesions to the septum or nucleus sphericus. Physiol. Behav. 1987, 40:759-765.
41. Krohmer R.W., Grassman M., Crews D. Annual reproductive cycle in the male red-sided garter snake, Thamnophis sirtalis parietalis: field and laboratory studies. Gen. Comp. Endocrinol. 1987, 68:64-75.
42. Krohmer R.W., Bieganski G.J., Baleckaitis D.D., Harada N., Balthazart J. Distribution of aromatase immunoreactivity in the forebrain of red-sided garter snakes at the beginning of the winter dormancy. J. Chem. Neuroant. 2002, 23:59-71.
43. LeMaster M.P., Mason R.T. Evidence for a female sex pheromone mediating male trailing behavior in the red-sided garter snake, Thamnophis sirtalis parietalis. Chemoecology 2001, 11:149-152.
44. LeMaster M.P., Mason R.T. Variation in a female sexual attractiveness pheromone controls male mate choice in garter snakes. J. Chem. Ecol. 2002, 28:1269-1285.
45. Licht P. Reptiles. Marshall's Physiology of Reproduction, Vol 1. Reproductive Cycles of Vertebrates 1984, 206-282. Livingstone, Edinburgh, UK. G.E. Lamming (Ed.).
46. Lowry O.H., Rosenbrough N.J., Farr A.L., Randall R.J. Protein measurement with Folin phenol reagent. J. Biol. Chem. 1951, 193:265-275.
47. Lutterschmidt D.I., Mason R.T. Endocrine mechanisms mediating temperature-induced reproductive behavior in red-sided garter snakes (Thamnophis sirtalis parietalis). J. Exp. Biol. 2009, 212:3108-3118.
48. Mason R.T., Fales H.M., Jones T.H., Pannell L.K., Chinn J.W., Crews D. Sex pheromones in garter snakes. Science 1989, 245:290-293.
49. Mason R.T., Jones T.H., Fales H.M., Pannell L.K., Crews D. Characterization, synthesis, and behavioral responses to the sex attractiveness pheromone of the red-sided garter snake (Thamnophis sirtalis parietalis). J. Chem. Ecol. 1990, 16:2353-2369.
50. Moore I.T., Mason R.T. Behavioral and hormonal responses to corticosterone in the male red-sided garter snake, Thamnophis sirtalis parietalis. Phys. Behav. 2001, 70:669-674.
51. Moore I.T., LeMaster M.P., Mason R.T. Behavioral and hormonal responses to capture stress in the male red-sided garter snake, Thamnophis sirtalis parietalis. Anim. Behav. 2000, 59:529-534.
52. Moore I.T., Green M.J., Mason R.T. Environmental and seasonal adaptations of the adrenocortical and gonadal response to capture stress in two populations of the male garter snake, Thamnophis sirtatis. J. Exp. Zool. 2001, 289:99-108.
53. Naftolin F., Horvath T.L., Jakab R.L., Leranth C., Harada N., Balthazart J. Aromatase immunoreactivity in axon terminals of the vertebrate brain. Neuroendocrinology 1997, 63:149-155.
54. Naftolin F., Rayan K.J., Davies I.J., Reddy V.V., Flores F., Petro Z., White R.J., Takoaka Y., Wolin L. The formation of estrogens by central neruroendocrine tissues. Rec. Prog. Horm. Res. 1975, 31:295-319.
55. O'Bryant E.L., Wade J. Seasonal and sexual dimorphisms in the green anole forebrain. Horm. Behav. 2002, 41:384-395.
56. O'Donnell R.P., Shine R., Mason R.T. Seasonal anorexia in the male red-sided garter snake, Thamnophis sirtalis parietalis. Behav. Ecol. Sociobiol. 2004, 56:413-419.
57. Palkovitz M. Isolated removal of hypothalamic or other brain nuclei of the rat. Brain Res. 1973, 59:449-456.
58. Palkovits M., Brownstein M.J. Microdissection of brain areas by the punch technique. Proc. Ann. Meet. Soc. Neurosci. 1983, 60-71.
59. Panzica G.C., Viglietti-Panzica C., Balthazart J. The sexually dimorphic medical preoptic nucleus in quail: a key brain area mediating steroid action on male sexual behaviour. Front. Neuroendocrinol. 1996, 1:51-125.
60. Roselli C.F. Brain aromatase: roles in reproduction and neuroprotection. J. Steroid Biochem. Mol. Biol. 2007, 106:143-150.
61. Roselli C.E., Horton L.E., Resko J.A. Distribution and regulation of aromatase activity in the rat hypothalamus and limbic system. Endocrinol. 1985, 117:2471-2477.
62. Rosen G.J., Wade J. Androgen metabolism in the brain of the green anole lizard (Anolis carolinensis): effects of sex and season. Gen. Comp. Endocrinol. 2001, 122:40-47.
63. Saint Girons H., Bradshaw S.D., Bradshaw F.J. Sexual activity and plasma levels of sex steroids in the Aspic viper Vipera aspis L. (Reptilia, Viperidae). Gen. Comp. Endocrinol. 1993, 91:287-297.
64. SPSS SPSS. Version 17.0 2008, SPSS, Chicago.
65. Systat SigmaStat 3.5 2006, Systat Software, Point Richmond, CA.
66. Tobet S.A., Zahniser D.J., Baum M.J. Differentiation in male ferrets of a sexually dimorphic nucleus of the preoptic/anterior hypothalamic area requires prenatal estrogen. Neuroendocrinology 1986, 44:299-308.
67. Tobet S.A., Shim J.H., Osiecki S.T., Baum M.J., Canick J.A. Androgen aromatization and 5-alpha reduction in ferret brain during perinatal development: effects of sex and testosterone manipulation. Endocrinology 1985, 116:1869-1877.
68. Wade J. Androgen metabolism in the brain of the green anole lizard (Anolis carolinensis). Gen. Comp. Endocrinol. 1997, 106:127-137.
69. Wallen K., Baum M.J. Masculinization and defeminization in altricial and precocial mammals: comparative aspects of steroid hormone action. Hormones, Brain and Behavior, Vol 4 2002, 385-423. Academic Press, San Diego. D.W. Pfaff, A.P. Arnold, A.M. Etgen, S.E. Fahrbach, R.T. Rubin (Eds.).
70. Wang R.T., Kubie J.L., Halpern M. Brevital sodium: an effective anesthetic agent for performing surgery on small reptiles. Copeia 1977, 1977:738-743.
71. Wesson D.W., Keller M., Douhard Q., Baum M.J., Bakker J. Enhanced urinary odor discrimination in female aromatase knockout (ArKO) mice. Horm. Behav. 2006, 49:580-586.
72. Whittier J.M., Mason R.T., Crews D., Licht P. Role of light and temperature in the regulation of reproduction in the red-sided garter snake, Thamnophis sirtalis parietalis. Can. J. Zool. 1987, 65:2090-2096.
73. Winkler S.M., Wade J. Aromatase activity and regulation of sexual behaviors in the green anole lizard. Phys. Behav. 1998, 64:723-731.
74. Woolley S.C., Sakata J.T., Crews D. Evolutionary insights into the regulation of courtship behavior in male amphibians and reptiles. Physiol. Behav. 2004, 83:347-360.