Acetylcholinesterase-positive innervation is present at undifferentiated stages of the sea turtle Lepidochelis olivacea embryo gonads: Implications for temperature-dependent sex determination

Journal of Comparative Neurology

Volumn 410, Issue 1, 1999, Pages 90-98

  Gutiérrez Ospina, Gabriel ^a   Jiménez Trejo, Francisco J ^b   Favila, Rafael ^a   Moreno Mendoza, Norma A ^b   Granados Rojas, Leticia ^a   Barrios, Fernando A ^a   Díaz Cintra, Sofía ^a   Merchant Larios, Horacio ^b  

^a INSTITUTO DE NEUROBIOLOGÍA   (Mexico)

^b UNIVERSIDAD NACIONAL AUTÓNOMA DE MÉXICO   (Mexico)

Author keywords

Brain; Heterochrony; Reptiles; Sexual differentiation; Vertebrate

Indexed keywords

ACETYLCHOLINESTERASE;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; GONAD DEVELOPMENT; HEAT SENSITIVITY; NERVOUS SYSTEM; NONHUMAN; PRIORITY JOURNAL; SENSORY NERVE; SEX DETERMINATION; SEX DIFFERENCE; SPINAL CORD; TEMPERATURE DEPENDENCE; THERMOREGULATION; TURTLE;

ACETYLCHOLINESTERASE; ANIMALS; EMBRYO, NONMAMMALIAN; FEMALE; GONADS; MALE; NERVOUS SYSTEM; SEX DIFFERENTIATION; SPINAL CORD; TEMPERATURE; TURTLES;

EID: 0345211596     PISSN: 00219967     EISSN: None     Source Type: Journal    
DOI: 10.1002/(SICI)1096-9861(19990719)410:1<90::AID-CNE8>3.0.CO;2-7     Document Type: Article

References (56)

1. Arnold AP. 1996. Genetically triggered sexual differentiation of brain and behavior. Hormon Behav 30:495-505.
2. Barr ML, Kierman JA. 1986. The human nervous system: An anatomical viewpoint. New York: Harper and Row Publishers, Inc.
3. Barrios, FA, Favila R, Jinénez-Trejo F, Gutiérrez-Ospina, Díaz-Cintra S, Merchang-Larios H. 1998. Acetylcholinesterase (AchE) positive fibers in the sea turtle Lepidochelys olivacea embryonic gonads: Anatomical survey by 3D visulization. Soc Neurosci 2:160.
4. Ben-Jonathan N, Arbogast LA, Rhoades TA, Bahr JM. 1984. Norepinephrine in the rat ovary: ontogeny and de novo synthesis. Endocrinology 115:1426-1431.
5. Black IB. 1994. Information in the brain: a molecular perspective. Cambridge: MIT Press.
6. Bull JJ, Gutzke WHN, Crews D. 1998. Sex reversal by estradiol in three reptilian orders. Gen Comp Endocrinol 70:425-428.
7. Bulmer D. 1965. A histochemical study of ovarian cholinesterases. Acta Anat 62:254-265.
8. Burden HW, and Lawrence IE. Jr. 1977. The effect of denervation on compensatory ovarian hypertrophy. Neuroendocrinolgy 23:368-378.
9. Burden, HW, Lawrence IE Jr. 1978. Experimental studies on the acetylcholinesterase-positive nerves in the ovary of the rat. Anat Rec 190:233-242.
10. Burden HW, Leonard M, Smith CP, Lawrence IE, Jr. 1983. The sensory innervation of the ovary: a horseradish peroxidase study in the rat. Anat Rec 207:623-627.
11. Coomber P, Crews D, Gonzalez-Lima F. 1997. Independent effects of incubation temperature and gonadal sex on the volume and metabolic capacity of the brain nuclei in the leopard gecko (Eublepharis macularius), a lizard with temperature-dependent sex determination. J Comp Neurol 380:409-421.
12. Crews D. 1994. Animal sexuality. Sci Am 270:108-114.
13. Crews D. 1996. Temperature dependent sex determination: the interplay of steroid hormones and temperature. Zool Sci 13:1-13.
14. Crews D, Bergeron JM, Bull JJ, Flores D, Tousignant A, Skipper JK, Wibbels T. 1994. Temperature-dependent sex determination in reptiles: Proximate mechanisms, ultimate outcomes, and practical applications. Dev Gen 15:297-312.
15. Crews D, Cantú AR, Bergeron JM, Rhen T. 1995. The relative effectiveness of androstenedione, testosterone, and estrone precursors to estradiol, in sex reversal in the red-eared slider (Trachemys scripta), a turtle with temperature-dependent sex determination. Gen Com Endocrinol 100: 119-127.
16. D'Albora H, Barcia JJ. 1996. Intrinsic neuronal cell bodies in the rat ovary. Neurosci Lett 205:65-67.
17. Desvages G, Girondot M, Pieau C. 1993. Sensitive stages for the effects of temperature on gonadal aromatase activity in embryos of the marine turtle Dermochelys coriacea. Gen Comp Endocrinol 92:54-61.
18. Dorizzi M, Mignot T-M, Guichard A, Desvages G, Pieau C. 1991. Involvement of oestrogens in sexual differentiation of gonads as a function of temperature in turtles. Differentiation 47:9-17.
19. Dorizzi M, Richard-Mercier N, Desvages G, Girondot M, Pieau C. 1994. Masculinization of gonads by aromatase inhibitors in a turtle with temperature-dependent sex determination. Differentiation 58:1-8.
20. Dorizzi M, Richard-Mercier N, Pieau C. 1996. The ovary retains male potential after the thermosensitive period for sex determination in the turtle Emys orbicularis. Differentiation 60:193-201.
21. Fletcher TL, Cameron P, De Camilli P, Banker G. 1991. The distribution of synapsi I and synaptophysin in hippocampal neurons developing in culture. J Neurosci 11:1617-1626.
22. Gerendia I. 1988. Innervation of the ovary and its functional significance. In: Genazzani AR, Montemagno U, Nappi C, Petaglia F, editors. The brain and female reproduction function. New York: Parthenon Publishing Group, p 191-195.
23. Gorski RA. 1984. Sexual differentiation of the brain: Possible mechanisms and implications. Can J Physiol Pharmacol 63:577-594.
24. Gutzke WHN, Chymiy DB. 1988. Sensitive periods during embryogeny for hormonally induced sex determination in turtles. Gen Com Endocrinol 71:265-267.
25. Hensel H. 1973. Neural processes in thermoregulation. Physiol Rev 53:948-1017.
26. Hokfelt T. 1991. Neuropeptides in perspective: the last ten years. Neuron 7:867-879.
27. Hydon PG, Drapeau P. 1995. From contact to connection: Early events during synaptogenesis. TINS 18:196
28. Hydon PG, Zoran MJ. 1993. Retrograde regulation of presynaptic development during synaptogenes. J Neurobiol 25:694-706.
29. Jessen C, Mayer ET. 1971. Spinal cord and hypothalamus as core sensors of temperature in the conscious dog: equivalence of responses. Plügers Arch 324:189-209.
30. Jessen C, Mclean JA, Calvert DT, Findlay JD. 1972. Balanced and unbalanced temperature signals generated in spinal cord of the ox. Am J Physiol 222:1343-1347.
31. Lance VA. 1997. Sex determination in reptiles: an update. Am Zool 37:504-513.
32. Lance VA, Bogart MH. 1991. Tamoxifen "sex reverses" alligator embryos at male producing temperature, but is an antiestrogen in female hatchlings. Experientia 47:263-266.
33. Lauder JM. 1993. Neurotransmitters as growth regulatory signals: Role of receptors and second messengers. TINS 16:223-240.
34. Mercer JB, Simon E. 1984. A comparison between total body thermosensitivity and local thermosensitivity in mammals and birds. Pflügers Arch 400:228-234.
35. Merchant-Larios H, Villanlpando I. 1990. Effect of temperature on gonadal sex differentiation in the sea turtle Lepidochelys olivacea: an organ culture study. J Exp Zool 254:327-331.
36. Merchant-Larios H, Villalpando-Fierro I, Centeno-Urruiza B. 1989. Gonadal morphogenesis under controlled temperature in the sea turtle Lepidochelys qlivacea. Herpetol monogrs 3:43-61.
37. Merchant-Larious H, Ruiz-Ramirez S, Moreno-Mendoza N, Marmolejo-Valencia A. 1997. Correlation among thermosensitive period, estradiol response, and gonad differentiation in the sea turtle Lepidochelys olivacea. Gen Comp Endocrinol 107:373-385.
38. Nelson DO, Heath JE, Presser CL. 1984. Evolution of temperature regulatory mechanisms. Am Zool 24:791-807.
39. Pieau C, Mignot T-M, Dorizzi M, Guichard A. 1982. Gonadal steroid levels in the turtle Emys orbicularis L.: a preliminary study in embryos, hatchlings, and young as a function of the incubation temperature of eggs. Gen Comp Endocrinol 47:392-398.
40. Purves D, Lichtman J. 1987. Principles of neural development. Cambridge, MA: Sinauer Associates, Inc.
41. Rhen TR, Lang JW. 1994. Temperature-dependent sex determination in the snapping turtle: manipulation of the embryonic sex steroid environment. Gen Com Endocrinol 96:243-254.
42. Richard-Mercier N, Dorizzi M, Desvages G, Girondot M, Pieau C. 1995. Endocrine sex reversal of gonads by the aromatase inhibitor letrozole (CGS 20267) in Emys orbicularis, a turtle with temperature-dependent sex determination. Gen Comp Endocrinol 100:314-326.
43. Riedel W, Siaplauras G, Simon E. 1973. Intra-abdominal thermosensitivity in the rabbit as compared with spinal thermosensitivity. Plügers Arch 34059-70.
44. Salame-Méndez A, Herrera-Muñoz, Moreno-Mendoza N, Merchant-Larios H. 1998. Response of diencephalon but not the gonad to female-promoting temperature with elevated estradiol levels in the sea turtle Lepidochelys olivacea. J Exp Zool 280:304-313.
45. Satinoff E. 1978. Neural organization and evolution of thermal regulation in mammals. Science 201:16-22.
46. Simon E. 1974. Temperature regulation: the spinal cord as a site of extrahypothalamic thermoregulatory functions. Rev Physiol Biochem Pharmacol 71:1-76.
47. Spotila JR, Spotila LD, Kaufer NF. 1994. Molecular mechanisms of TSD in reptiles: A search, for the magic bullet. J Exp Zool 270:117-127.
48. Stefenson A, Owman Ch, Sjöberg N-O, Sporrong B, Walles B. 1981. Comparative study of the autonomic innervation of the mammalian ovary, with particular regard to the follicular system. Cell Tissue Res 215:47-62.
49. von Bartheld CS, Cunningham DE, Rubel EW. 1990. Neuronal tracing with DiI: Decalcification, cryosectioning, and photoconversion for light and electron microscopic analysis J Histochem Cytochem 38:725-733.
50. White RB, Thomas P. 1992. Stimulation of in vitro steroidogenesis by pituitaty hormones in a turtle (Trachemys scripta) within the temperature-sensitive period for sex determination. Biol Reprod 47:952-959.
51. Wibbels T, Crews D. 1994. Putative aromatase inhibitor induces male sex determination in a female unisexual lizard and in a turtle with temperature-dependent sex determination. J Endocrinol 141:295-299.
52. Wibbels T, Crews D. 1995, Steroid-induced sex determination at incubation temperatures mixed sex ratios in a turtle with TSD. Gen Comp Endocrinol 100:53-60.
53. Wibbels T, Bull JJ, Crews D. 1991. Synergism between temperature and estradiol: A common pathway in turtle sex determination? J Exp Zool 260:130-134.
54. Wibbels T, Bull JJ, Crews D. 1992. Steroid-induced male sex determination in an amniotic vertebrate. J Exp Zool 262:454-457.
55. Wibbels T, Gideon P, Bull JJ, Crews D. 1993. Estrogen-and temperature-induced medullary cord regression during gonadal differentiation in a turtle. Differentiation 53:149-153.
56. Wibbels T, Bull JJ, Crews D. 1994. Temperature-dependent sex determination: A mechanistic approach. J Exp Zool 270:71-78.