Reproduction phase-related variations in neuropeptide Y immunoreactivity in the olfactory system, forebrain, and pituitary of the female catfish, Clarias batrachus (Linn.)

Journal of Comparative Neurology

Volumn 504, Issue 5, 2007, Pages 450-469

  Mazumdar, Minakshi ^a   Sakharkar, Amul J ^b   Singru, Praful S ^c   Subhedar, Nishikant ^a  

^a RTM NAGPUR UNIVERSITY   (India)

^b PENNINGTON BIOMEDICAL RESEARCH CENTER   (United States)

^c TUFTS MEDICAL CENTER   (United States)

Author keywords

NPY; Nucleus entopeduncularis; Nucleus preopticus periventricularis; Olfactory bulb; Olfactory receptor neurons; Pituitary; Reproduction; Teleost; Testosterone injection

Indexed keywords

GONADORELIN; LUTEINIZING HORMONE; NEUROPEPTIDE Y; TESTOSTERONE;

ANIMAL EXPERIMENT; ANTIBODY SPECIFICITY; ARTICLE; CATFISH; CONTROLLED STUDY; ENVIRONMENTAL FACTOR; ESTRUS CYCLE; FEMALE; FOREBRAIN; HYPOPHYSIS; IMMUNOREACTIVITY; MALE; NONHUMAN; OLFACTORY RECEPTOR; OLFACTORY SYSTEM; PRIORITY JOURNAL; PROTEIN FUNCTION; REPRODUCTION; SPAWNING;

ANALYSIS OF VARIANCE; ANIMALS; CATFISHES; FEMALE; GENE EXPRESSION REGULATION, DEVELOPMENTAL; LUTEINIZING HORMONE; MALE; NEUROPEPTIDE Y; OLFACTORY PATHWAYS; PITUITARY GLAND; PROSENCEPHALON; REPRODUCTION; SEASONS; TESTOSTERONE;

EID: 35348871928     PISSN: 00219967     EISSN: 10969861     Source Type: Journal    
DOI: 10.1002/cne.21462     Document Type: Article

References (64)

1. Amano M, Hyodo S, Urano A, Okumoto N, Kitamura S, Ikuta K, Suzuki Y, Aida K. 1994. Activation of salmon gonadotropin-releasing hormone synthesis by 17 alpha-methyl testosterone administrations in yearling masu salmon, Oncorhynchus masou. Gen Comp Endocrinol 95:374-380.
2. Amano M, Ikuta K, Kitamura S, Aida K. 1999. Effects of photoperiod on salmon GnRH mRNA levels in brain of castrated underyearling precocious male masu salmon. Gen Comp Endocrinol 115:70-75.
3. Anglade I, Zandbergen T, Kah O. 1993. Origin of the pituitary innervation in the goldfish. Cell Tissue Res 273:345-355.
4. Biju KC, Singru PS, Schreibman MP, Subhedar N. 2003. Reproduction phase-related expression of GnRH-like immunoreactivity in the olfactory receptor neurons, their projections to the olfactory bulb and in the nervus terminalis in the female Indian major carp Cirrhinus mrigala (Ham.). Gen Comp Endocrinol 133:358-367.
5. Breton B, Sambroni E. 1996. Steroid activation of the brain-pituitary complex gonadotropic function in the triploid rainbow trout, Oncorhynchus mykiss. Gen Comp Endocrinol 101:155-164.
6. Burzawa-Gerard E. 1982. Chemical data on pituitary gonadotropins and their implication to evolution. Can J Fish Aquat Sci 39:80-91.
7. Bushnik T, Fernald RD. 1995. The population of GnRH-containing neurons showing socially mediated size changes project to the pituitary in a teleost, Haplochromis burtoni. Brain Behav Evol 46:371-377.
8. Cambré ML, Verdonck W, Ollevier F, Vandesande F, Batten TFC, Kuhn ER. 1986. Immunocytochemical identification and localization of the different cell types in the pituitary of the seabass (Dicentrarchus labrax). Gen Comp Endocrinol 61:368-375.
9. Chiba A. 1997. Distribution of neuropeptide Y-like immunoreactivity in the brain of the bichir, Polypterus senegalus, with special regard to the terminal nerve. Cell Tissue Res 289:275-284.
10. Demski LS, Northcutt RG. 1983. The terminal nerve: a new chemosensory system in vertebrates? Science 220:435-437.
11. Dobbins A, Lubbers LS, Jackson GL, Kuehl DE, Hileman SM. 2004. Neuropeptide Y gene expression in male sheep: influence of photoperiod and testosterone. Neuroendocrinology 79:82-89.
12. Doyon C, Leclair J, Trudeau VL, Moon TW. 2006. Corticotropin-releasing factor and neuropeptide Y mRNA levels are modified by glucocorticoids in rainbow trout, Oncorhynchus mykiss. Gen Comp Endocrinol 146:126-135.
13. Dufourny L, Caraty A, Clarke IJ, Robinson JE, Skinner DC. 2005. Progesterone-receptive dopaminergic and neuropeptide Y neurons project from the arcuate nucleus to gonadotropin-releasing hormone-rich regions of the ovine preoptic area. Neuroendocrinology 82:21-31.
14. Francis RC, Jacobson B, Wingfield JC, Fernald RD. 1992. Hypertrophy of gonadotropin releasing hormone-containing neurons after castration in the teleost Haplochromis burtoni. J Neurobiol 23:1084-1093.
15. Gaikwad A, Biju KC, Subhedar N. 2003. GnRH-LH secreting cells axis in the pituitary of the teleost Clarias batrachus responds to neuropeptide Y treatment: an immunocytochemical study. Gen Comp Endocrinol 131:126-133.
16. Gaikwad A, Biju KC, Saha SG, Subhedar N. 2004. Neuropeptide Y in the olfactory system, forebrain and pituitary of the teleost, Clarias batrachus. J Chem Neuroanat 27:55-70.
17. Gaikwad A, Biju KC, Muthal PL, Saha S, Subhedar N. 2005. Role of neuropeptide Y in the regulation of gonadotropin-releasing hormone system in the forebrain of Clarias batrachus (Linn.): immunocytochemistry and high performance liquid chromatography-electrospray ionization-mass spectrometry analysis. Neuroscience 133:267-279.
18. Gruenewald DA, Naai MA, Marck BT, Matsumoto AM. 1994. Age-related decrease in neuropeptide-Y gene expression in the arcuate nucleus of the male rat brain is independent of testicular feedback. Endocrinology 134:2383-2389.
19. Hamson DK, Jones BA, Watson NV. 2004. Distribution of androgen receptor immunoreactivity in the brainstem of male rats. Neuroscience 127:797-803.
20. Hofmann MH, Meyer DL. 1995. The extrabulbar olfactory pathway: primary olfactory fibers bypassing the olfactory bulb in bony fishes? Brain Behav Evol 46:378-388.
21. Hwang IK, Kang TC, Park SK, An SJ, Suh JG, Lee JY, Lee IS, Yoon YS, Oh YS, Won MH. 2001. Age-related change of neuropeptide Y-immunoreactive neurons in the rat anterior olfactory nucleus. J Neurocytol 30:967-972.
22. Jadhao AG, Malz CR. 2004. Nicotinamide adenine dinucleotide phosphate (NADPH)-diaphorase activity in the brain of a cichlid fish, with remarkable findings in the entopeduncular nucleus: a histochemical study. J Chem Neuroanat 27:75-86.
23. Kah O, Breton B, Dulka JG, Nunez-Rodriguez J, Peter RE, Corrigan A, Rivier JE, Vale WW. 1986. A reinvestigation of the GnRH (gonadotrophin-releasing hormone) systems in the goldfish brain using antibodies to salmon GnRH. Cell Tissue Res 244:327-337.
24. Kah O, Anglade I, Leprêtre E, Dubourg P, de Monbrison D. 1993. The reproductive brain in fish. Fish Physiol Biochem 11:85-98.
25. Kalra SP, Horvath T, Naftolin F, Xu B, Pu S, Kalra PS. 1997. The interactive language of hypothalamus for the gonadotropin releasing hormone (GnRH) system. J Endocrinol 9:569-576.
26. Khan FA, Jain MR, Saha SG, Sarkar S, Subhedar N. 1998. FMRFamide-like immunoreactivity in the olfactory system responds to morphine treatment in the teleost Clarias batrachus (Linn.): involvement of opiate receptors. Gen Comp Endocrinol 110:79-87.
27. Khan FA, Saha SG, Sarkar S, Subhedar N. 1999. β-Endorphin-like immunoreactivity in the forebrain and pituitary of the teleost, Clarias batrachus (Linn.). Gen Comp Endocrinol 113:290-301.
28. Kyle AL, Sorensen PW, Stacey NE, Dulka JG. 1987. Medial olfactory tract pathways controlling sexual reflexes and behavior in teleosts. Ann N Y Acad Sci 519:97-107.
29. Mazumdar M, Lal B, Sakharkar AJ, Deshmukh M, Singru PS, Subhedar N. 2006. Involvement of neuropeptide Y Y1 receptors in the regulation of LH and GH cells in the pituitary of the catfish, Clarias batrachus: an immunocytochemical study. Gen Comp Endocrinol 149:190-196.
30. Meek J, Nieuwenhuys R. 1998. Holosteans and teleosts. In: Nieuwenhuys R, Ten Donkelaar HJ, Nicholson C, editors. The central nervous system of vertebrates. Berlin: Springer. p 758-937.
31. Moons L, Cambre M, Ollevier F, Vandesande F. 1989. Immunocytochemical demonstration of close relationships between neuropeptidergic nerve fibers and hormone-producing cell types in the adenohypophysis of the sea bass (Dicentrarchus labrax). Gen Comp Endocrinol 73:270-283.
32. Navas JM, Anglade I, Bailhache T, Pakdel F, Breton B, Jeko P, Kah O. 1995. Do gonadotropin-releasing hormone neurons express estrogen receptors in the rainbow trout? A double immunohistochemical study. J Comp Neurol 363:461-474.
33. Oukouchoud R, Vivien-Roels B, Pevet P, Lakhdar-Ghazal N. 2003. Testosterone-dependent and -independent mechanisms involved in the photoperiodic control of neuropeptide levels in the brain of the jerboa (Jaculus orientalis). Brain Res 967:63-72.
34. Parhar IS, Sim MK. 1994. Central dopaminergic neurons in tilapia: effects of gonadectomy and hypothalamic lesion. Neurosci Res 18:255-266.
35. Parhar IS, Soga T, Sakuma Y. 1998. Quantitative in situ hybridization of three gonadotropin-releasing hormone-encoding mRNAs in castrated and progesterone-treated male tilapia. Gen Comp Endocrinol 112:406-414.
36. Peng C, Trudeau VL, Peter RE. 1993. Seasonal variation of neuropeptide Y actions on growth hormone and gonadotropin-II secretion in the goldfish: effect of sex steroids. J Neuroendocrinol 5:273-280.
37. Peng C, Gallin W, Peter RE, Blomqvist AG, Larhammar D. 1994. Neuropeptide-Y gene expression in the goldfish brain: distribution and regulation by ovarian steroids. Endocrinology 134:1095-1103.
38. Peter RE, Paulencu CR. 1980. Involvement of the preoptic region in gonadotropin release-inhibition in goldfish, Carassius auratus. Neuroendocrinology 31:133-141.
39. Pickavance LC, Staines WA, Fryer JN. 1992. Distributions and colocalization of neuropeptide Y and somatostatin in the goldfish brain. J Chem Neuroanat 5:221-233.
40. Pirone A, Betti L, Mascia G, Giannaccini G, Lucacchini A, Fabiani O. 2003. Autoradiographic distribution of neuropeptide Y binding sites in the brain of the carp Cyprinus carpio L. (Cyprinidae, Teleostei). Comp Biochem Physiol A134:757-762.
41. Rama Krishna NS, Subhedar N. 1989. Hypothalamic innervation of the pituitary in the catfish, Clarias batrachus (L.): a retrograde horseradish peroxidase study. Neurosci Lett 107:39-44.
42. Sakharkar AJ, Singru PS, Sarkar K, Subhedar N. 2005. Neuropeptide Y in the forebrain of the adult male cichlid fish Oreochromis mossambicus: distribution, effects of castration and testosterone replacement. J Comp Neurol 489:148-165.
43. Sakharkar AJ, Singru PS, Mazumdar M, Subhedar N. 2006. Reproduction phase-related expression of β-endorphin-like immunoreactivity in the nucleus lateralis tuberis of the female Indian major carp Cirrhinus mrigala: correlation with the luteinising hormone cells-ovary axis. J Neuroendocrinol 18:319-329.
44. Sar M, Sahu A, Crowley WR, Kalra SP. 1990. Localization of neuropeptide-Y immunoreactivity in estradiol-concentrating cells in the hypothalamus. Endocrinology 127:2752-2756.
45. Sarkar S, Subhedar N. 2001. Seasonal changes in β-endorphin-like immunoreactivity in the olfactory system of the female catfish, Clarias batrachus (Linn). Gen Comp Endocrinol 123:127-136.
46. Satou M. 1990. Synaptic organization, local neuronal circuitry, and functional segregation of the teleost olfactory bulb. Prog Neurobiol 34:115-142.
47. Schreibman MP, Margolis-Nunno H. 1987. Reproductive biology of the terminal nerve (nucleus olfactoretinalis) and other LHRH pathways in teleosts fishes. Ann N Y Acad Sci 519:60-68.
48. Siegmund I, Troncoso S, Caorsi CE, Gonzalez CB. 1987. Identification and distribution of the cell types in the pituitary gland of Austromenidia lacticlavia (Teleostei, Atherinidae). Gen Comp Enocrinol 67:348-355.
49. Singh SP, Singh TP. 1981. Relative concentrations of prolactin, gonadotropin and thyrotropin in the pituitary gland and blood serum during different phases of annual reproductive cycle in the freshwater catfish, Clarias batrachus. Endocrinology 77:39-50.
50. Skinner DC, Herbison AE. 1997. Effects of photoperiod on estrogen receptor, tyrosine hydroxylase, neuropeptide Y, and β-endorphin immunoreactivity in the ewe hypothalamus. Endocrinology 138:2585-2595.
51. Soga T, Sakuma Y, Parhar IS. 1998. Testosterone differentially regulates expression of GnRH messenger RNAs in the terminal nerve, preoptic and midbrain of male tilapia. Brain Res Mol Brain Res 60:13-20.
52. Sohn EH, Wolden-Hanson T, Matsumoto AM. 2002. Testosterone (T)-induced changes in arcuate nucleus cocaine-amphetamine-regulated transcript and NPY mRNA are attenuated in old compared to young male brown Norway rats: contribution of T to age-related changes in cocaine-amphetamine-regulated transcript and NPY gene expression. Endocrinology 143:954-963.
53. Soma KK, Francis RC, Wingfield JC, Fernald RD. 1996. Androgen regulation of hypothalamic neurons containing gonadotropin-releasing hormone in a cichlid fish: integration with social cues. Horm Behav 30:216-226.
54. Sorensen PW, Caprio J. 1998. Chemoreception. In: Evans DH, editor. The physiology of fishes. Boca Raton, FL: CRC Press. p 375-405.
55. Stefanini M, De Mortino C, Zamboni L. 1967. Fixation of ejaculated spermatozoa for electron microscopy. Nature 216:173-174.
56. Subhedar N, Rama Krishna NS. 1988. Immunocytochemical localization of LH-RH in the brain and pituitary of the catfish, Clarias batrachus (Linn.). Gen Comp Endocrinol 72:431-442.
57. Subhedar N, Cerdá J, Wallace RA. 1996. Neuropeptide Y in the forebrain and retina of the killifish, Fundulus heteroclitus. Cell Tissue Res 283:313-323.
58. Tiwary BK, Kirubagaran R, Ray AK. 2002. Testosterone triggers the brain-pituitary-gonad axis of juvenile female catfish (Heteropneustes fossilis: Bloch) for precocious ovarian maturation. Gen Comp Endocrinol 126:23-29.
59. Toubeau G, Poilve A, Baras E, Nonclercq D, Moor SD, Beckers JF, Dessy-Doize C, Heuson-Stiennon JA. 1991. Immunocytochemical study of cell type distribution in the pituitary of Barbus barbus (Teleostei, Cyprinidae). Gen Comp Endocrinol 83:35-47.
60. Trudeau VL. 1997. Neuroendocrine regulation of gonadotropin II release and gonadal growth in the goldfish, Carassius auratus. Rev Reprod 2:55-68.
61. Urban JH, Das I, Levine JE. 1996. Steroid modulation of neuropeptide Y-induced luteinizing hormone releasing hormone release from median eminence fragments from male rats. Neuroendocrinology 63:112-119.
62. Yamamoto N, Parhar IS, Sawai N, Oka Y, Ito H. 1998. Preoptic gonadotropin-releasing hormone (GnRH) neurons innervate the pituitary in teleosts. Neurosci Res 31:31-38.
63. Yan HY, Thomas P. 1991. Histochemical and immunocytochemical identification of the pituitary cell types in three sciaenid fishes: Atlantic croaker (Micropogonias undulatus), spotted seatrout (Cynoscion nebulosus), and red drum (Sciaenops ocellatus). Gen Comp Endocrinol 84:389-400.
64. Zandbergen MA, Voormolen AHT, Peute J, Kah O, Goos HJT. 1994. Immunohistochemical localization of neuropeptide Y positive cell bodies and fibres in forebrain and pituitary of the African catfish, Clarias gariepinus. Neth J Zool 44:43-54.