NADPH diaphorase activity and nitric oxide synthase immunoreactivity in lordosis-relevant neurons of the ventromedial hypothalamus

Brain Research

Volumn 740, Issue 1-2, 1996, Pages 291-306

  Rachman, Ilya M ^a   Pfaff, Donald W ^b   Cohen, Rochelle S ^a  

^a UNIVERSITY OF ILLINOIS AT CHICAGO   (United States)

^b ROCKEFELLER UNIVERSITY   (United States)

Author keywords

electron microscopy; estrogen receptor; immunocytochemistry; NADPH diaphorase; nitric oxide synthase; reproductive behavior; ventromedial hypothalamus

Indexed keywords

ESTROGEN RECEPTOR; NITRIC OXIDE SYNTHASE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE DEHYDROGENASE;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; FEMALE; IMMUNOCYTOCHEMISTRY; LORDOSIS; NONHUMAN; OVARIECTOMY; PRIORITY JOURNAL; RAT; ULTRASTRUCTURE; ZONA INCERTA;

ANIMALS; FEMALE; HYPOTHALAMUS; IMMUNOHISTOCHEMISTRY; MICROSCOPY, ELECTRON; NADPH DEHYDROGENASE; NITRIC OXIDE SYNTHASE; OVARIECTOMY; RATS; RATS, SPRAGUE-DAWLEY;

EID: 0030592815     PISSN: 00068993     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0006-8993(96)00901-8     Document Type: Article

References (74)

1. [1] Alm, P., Larsson, B., Ekblad, E., Sundler, F. and Andersson, K.-E., Immunocytochemical localization of peripheral nitric oxide synthase-containing nerves using antibodies raised against C-and N-terminal fragments of a cloned enzyme from rat brain, Acta Physiol. Scand., 148 (1993) 421-429.
2. [2] Andrew, R.D., MacVicar, B.A., Dudek, P.E. and Hatton, G.I., Dye transfer through gap junctions between neuroendocrine cells of the rat hypothalamus, Science, 211 (1981) 1187-1189.
3. [3] Aoki, C., Fenstemaker, S., Lubin, M. and Go, C.-G., Nitric oxide synthase in the visual cortex of monocular monkeys as revealed by light and electron microscopic immunocytochemistry, Brain Res., 620 (1993) 97-113.
4. [4] Arévalo, R., Sánchez, F., Alonso, J.R., Carretero, J., Vásquez, R. and Aijón, J., NADPH-diaphorase activity in hypothalamic magnocellular neurosecretory nuclei of the rat, Brain Res. Bull., 28 (1992) 599-603.
5. [5] Barrionuevo, G. and Brown, T.H., Associative long-term potentiation in hippocampal slices, Proc. Natl. Acad. Sci. USA, 80 (1983) 7347-7351.
6. [6] Belai, A., Schmidt, H.H.H.W., Hoyle, C.H.V., Hassall, C.J.S., Saffrey, M.J., Moss, J., Fostermann, U., Murad, F. and Burnstock, G., Colocalization of nitric oxide synthase and NADPH-diaphorase in the myenteric plexus of the rat gut, Neurosci. Lett., 143 (1992) 60-64.
7. [7] Bohme, G.A., Bon, C. and Stutzmann, J.M., Possible involvement of nitric oxide in long-term potetiation, Eur. J. Pharmacol., 199 (1991) 378-381.
8. [8] Bredt, D.S., Glatt, C.E., Hwang, P.M., Fotuhi, M., Dawson, T.M. and Snyder, S.H., Nitric oxide synthase protein and mRNA are discretely localized in neuronal populations of the mammalian CNS together with NADPH diaphorase, Neuron, 7 (1991) 615-624.
9. [9] Bredt, D.S., Hwang, P.M., Glatt, C.E., Lowenstein, C., Reed, R.R. and Synder, S.H., Cloned and expressed nitric oxide synthase structurally resembles cytochrome P-450, Nature, 351 (1991) 714-718.
10. [10] Bredt, D.S., Hwang, P.M. and Snyder, S.H., Localization of nitric oxide synthase indicating a role for nitric oxide, Nature, 347 (1990) 768-770.
11. [11] Bredt, D.S. and Snyder, S.H., Nitric oxide: a physiologic messenger molecule, Annu. Rev. Biochem., 63 (1994) 175-195.
12. [12] Calka, J., Wolf, G. and Brosz, M., Ultrastructural demonstration of NADPH-diaphorase histochemical activity in the supraoptic nucleus of normal and dehydrated rats, Brain Res. Bull., 34 (1994) 301-308.
13. [13] Ceccatelli, S., Scott, R., Grandison, L., Pfaff, D.W. and Kow, L.-M., Estradiol regulation of nitric oxide synthase mRNAs in rat hypothalamus, Soc. Neurosci. Abstr., 21 (1995) 1890.
14. [14] Cintra, A., Fuxe, K., Härfstrand, A., Agnati, L.F., Miller, L.S., Greene, G.L. and Gustafsson, J.-A., On the cellular localization and distribution of estrogen receptors in the rat tel- and diencephalon using monoclonal antibodies to human estrogen receptor, Neurochem. Int., 8 (1986) 587-595.
15. [15] Clemens, L.G., Dohanich, G.P. and Witcher, J.A., Cholinergic influences of estrogen-dependent sexual behavior in female rats, J. Comp. Physiol. Psychol., 95 (1981) 763-770.
16. [16] Clemens, L.G., Humphrys, R.R. and Dohanich, G.P., Cholinergic brain mechanisms and the hormonal regulation of female sexual behavior in the rat, Pharmacol. Biochem. Behav., 13 (1980) 81-88.
17. [17] Cobbett, P., Yang, Q.Z. and Hatton, G.I., Incidence of dye coupling among magnocellular paraventricular nucleus neurons in male rats is testosterone dependent, Brain Res. Bull., 18 (1987) 365-370.
18. [18] Cohen, R.S., Chung, S.K. and Pfaff, D.W., Immunocytochemical localization of actin in dendritic spines of the cerebral cortex using colloidal gold as a probe, Cell. Mol. Neurobiol., 5 (1985) 271-284.
19. [19] Cohen, R.S. and Pfaff, D.W., Ventromedial hypothalamic neurons in the mediation of long-lasting effects of estrogen on lordosis behavior, Prog. Neurobiol., 38 (1992) 423-453.
20. [20] Crepel, F. and Jaillard, D., Protein kinases, nitric oxide, and long-term depression of synapses in the cerebellum, NeuroReport, 1 (1990) 133-136.
21. [21] Daniel, H., Hemart, N., Jaillard, D. and Crepel, F., Long-term depression requires nitric oxide and guanosine 3′,5′-cyclic monophosphate production in cerebellar Purkinje cells, Eur. J. Neurosci., 5 (1993) 1079-1082.
22. [22] Dawson, T.M., Bredt, D.S., Fotuhi, M., Hwang, P.M. and Snyder, S.H., Nitric oxide synthase and neuronal NADPH diaphorase are identical in brain and peripheral tissue, Proc. Natl. Acad. Sci. USA, 88 (1991) 7797-7801.
23. [23] De Kloet, E.R., Voorhuis, T.A.M. and Elands, J., Estradiol induces oxytocin binding sites in the rat hypothalamic ventromedial nucleus, Eur. J. Pharmacol., 118 (1985) 185-186.
24. [24] Dinerman, J.L., Dawson, T.M., Schell, M.J., Snowman, A. and Snyder, S.H., Endothelial nitric oxide synthase localized to hippocampal pyramidal cells: implications for synaptic plasticity, Proc. Natl. Acad. Sci. USA, 91 (1994) 4214-4218.
25. [25] Dohanich, G.P., Barr, P.J., Witcher, J.A. and Clemens, L.G., Pharmacological and anatomical aspects of cholinergic activation of female sexual behavior, Physiol. Behav., 32 (1984) 1021-1026.
26. [26] Dohanich, G.P., McMullan, D.M., Cada, D.A. and Mangum, K.A., Muscarinic receptor subtypes and sexual behavior in female rats, Pharmacol. Biochem. Behav., 38 (1991) 115-124.
27. [27] Dun, N.J., Dun, S.L. and Forstermann, U., Nitric oxide synthase immunoreactivity in rat pontine medullary neurons, Neuroscience, 59 (1994) 429-445.
28. [28] Frankfurt, M., Gould, E., Woolley, C.S. and McEwen, B.S., Gonadal steroids modify dendritic spine density in ventromedial hypothalamic neurons: a golgi study in the adult rat, Neuroendocrinology, 51 (1990) 530-535.
29. [29] Frankfurt, M. and McEwen, B., Estrogen increases axodendritic synapses in the VMN of rats after ovariectomy, NeuroReport, 2 (1991) 380-382.
30. [30] Gally, J.A., Read Montague, P., Reeke, Jr., J.N. and Edelman, G.M., The NO hypothesis: possible effects of a short-lived, rapidly diffusible signal in the development and function of the nervous system, Proc. Natl. Acad. Sci. USA, 87 (1990) 3547-3551.
31. [31] Greene, G.L., Nolan, C., Engler, J.P., Jensen, E.V., Monoclonal antibodies to human estrogen receptor, Proc. Natl. Acad. Sci. USA, 77 (1980) 5115-5119.
32. [32] Hatton, G.I., Yang, Q.Z. and Koran, L.E., Effects of ovariectomy and estrogen replacement on dye coupling among rat supraoptic nucleus neurons, Brain Res, 572 (1992) 291-295.
33. [33] Hope, B.T., Michael, G.J., Knigge, K.M. and Vincent, S.R., Neuronal NADPH diaphorase is a nitric oxide synthase, Proc. Natl. Acad. Sci. USA, 88 (1991) 2811-2814.
34. [34] Ito, M. and Karachot, L., Messengers mediating long-term desensitization in cerebellar Purkinje cells, NeuroReport, 1 (1990) 129-132.
35. [35] Johnson, A.E., Coirini, H., Ball, G.F. and McEwen, B.S., Anatomical localization of the effects of 17β-estradiol on oxytocin receptor binding in the ventromedial hypothalamic nucleus. Endocrinology, 124 (1989) 207-211.
36. [36] Kandel, E.R. and O'Dell, T.J., Are adult learning mechanisms also used for development? Science, 258 (1992) 243-245.
37. [37] Kaufman, L.S., Pfaff, D.W. and McEwen, B.S. Cholinergic mechanisms of lordotic behavior in rats, Physiol. Behav., 43 (1988) 507-514.
38. [38] King, W.J. and Greene, G.L., Monoclonal antibodies localize estrogen receptor in the nuclei of target cells. Nature, 307 (1984) 745-747.
39. [39] Kow, L.-M., Mobbs, C.V. and Pfaff, D.W., Roles of second messenger systems and neuronal activity in the regulation of lordosis by neurotransmitters, neuropeptides, and estrogen: a review, Neurosci. Biobehav. Rev., 18 (1994) 251-268.
40. [40] Kow, L.-M. and Pfaff, D.W., Estrogen effects on neuronal responsiveness to electrical and neurotransmitter stimulation: an in vitro study on the ventromedial nucleus of the hypothalamus, Brain Res., 347 (1985) 1-10.
41. [41] Levine, W., Giuditta, A., England, S. and Strecker, H.J., Brain diaphorases, J. Neurochem., 6 (1960) 28-36.
42. [42] Mani, S.K., Allen, J.M.C., Rettori, V., McCann, S., O'Malley, B.W. and Clark, J.H., Nitric oxide mediates sexual behavior in female rats, Proc. Natl. Acad. Sci. USA, 91 (1994) 6468-6472.
43. [43] Mizukawa, K., Vincent, S.R., McGeer. P.L. and McGeer, E.G., Distribution of reduced nicotinamide-adenine-dinucleotide-phosphate diaphorase-positive cells and fibers in the cat central nervous system, J. Comp. Neurol., 279 (1989) 281-311.
44. [44] Nelson, R.J., Demas, G.E., Hwang, P.L., Fishman, M.C., Dawson, V.L., Dawson, T.M. and Synder, S.H., Behavioral abnormalities in male mice lacking neuronal nitric oxide synthase, Nature, 378 (1995) 383-386.
45. [45] Nishizuka, M. and Pfaff, D.W., Intrinsic synapses in the ventromedial nucleus of the hypothalamus: an ultrastructural study, J. Comp. Neurol., 286 (1989) 260-268.
46. [46] O'Dell, T.J., Hawkins, R.D., Kandel, E.R. and Arancio, O., Tests on the roles of two diffusible substances in LTP: evidence for nitric oxide as a possible early retrograde messenger. Proc. Natl. Acad. Sci. USA, 88 (1991) 11285-11289.
47. [47] O'Dell, T.J., Huang, P.L., Dawson, T.M., Dinerman, J.L., Snyder, S.L., Kandel, E.R. and Fishman, M.C., Endothelial NOS and the blockade of LTP by NOS inhibitors in mice lacking neuronal NOS, Science, 265 (1994) 542-546.
48. [48] Okamura, H., Yokosuka, M., McEwen, B.S. and Hayashi, S., Colocalization of NADPH-diaphorase and estrogen receptor immunoreactivity in the rat ventromedial hypothalamic nucleus: stimulatory effect of estrogen on NADPH-diaphorase activity, Endocrinology, 135 (1994) 1705-1708.
49. [49] Paxino, G. and Watson, C., The Rat Brain in Stereotaxic Coordinates, Academic Press, New York, 1982, 84 pp.
50. 1b-noradrenergic receptors in the hypothalamus and preoptic area, J. Neurosci., 12 (1992) 3869-3876.
51. [51] Pfaff, D.W., Estrogens and Brain Function. Neural Analysis of a Hormone-Controlled Mammalian Reproductive Behavior, Springer, New York, 1980, 281 pp.
52. [52] Pfaff, D.W. and Keiner, M., Atlas of estradiol-concentrating cells in the central nervous system of the female rat, J. Comp. Neurol., 151 (1973) 121-158.
53. [53] Pfaff, D.W., Schwartz-Giblin, S., McCarthy, M.M. and Kow, L.-M., Cellular and molecular mechanisms of female reproductive behaviors. In E. Knobil and J.D. Neill (Eds.), The Physiology of Reproduction, 2nd edn., Raven Press, New York, 1994, pp. 107-220.
54. 2 release from the hypothalamus, Proc. Natl. Acad. Sci. USA, 89 (1992) 11543-11546.
55. [55] Rettori, V., Kamat, A. and McCann, S.M., Nitric oxide mediates the stimulation of luteinizing-hormone releasing hormone release induced by glutamic acid in vitro, Brain Res. Bull., 33 (1994) 501-503.
56. [56] Ridgway, R.L. and Chestnut, M.H., Processing small tissue specimens in acrylic resins for ultramicrotomy: improved handing and orientation, J. Electron Microsc. Techn., 1 (1984) 205-206.
57. [57] Rivier, C. and Shen, G.H., In the rat, endogenous nitric oxide modulates the response of the hypothalamic-pituitary-adrenal axis to interleukin-1β, vasopressin, and oxytocin, J. Neurosci., 14 (1994) 1985-1993.
58. [58] Rodrigo, J., Springall, D.R. Uttenthal, O., Bentura, M.L., Abadia-Molina, F., Riveros-Moreno, V., Martinez-Murillo, R., Polak, J.M. and Moncada, S., Localization of nitric oxide synthase in the adult rat brain, Phil. Trans. R. Soc. Lond. B, 345 (1994) 175-221.
59. [59] Saito, S., Kidd, G.J., Trapp, B.D., Dawson, T.M., Bredt, D.S., Wilson, D.A., Traystman, R.J., Snyder, S.H. and Hanley, D.F., Rat spinal cord neurons contain nitric oxide synthase, Neuroscience, 59 (1994) 447-456.
60. [60] Scherer-Singler, U., Vincent, S.R., Kimura, H. and McGeer, E.G., Demonstration of a unique population of neurons with NADPH-diaphorase histochemistry, J. Neurosci. Methods, 9 (1983) 229-234.
61. [61] Schmidt, R.E., Dorsey, D.A., McDaniel, M.L. and Corbett, J.A., Characterization of NADPH diaphorase activity in rat sympathetic autonomic ganglia - effect of diabetes and aging, Brain Res, 617 (1993) 343-348.
62. [62] Schmidt, H.H.H.W., Gagne, G.D., Nakan, M., Pollack, J.S., Miller, M.F. and Murad, F., Mapping of neuronal nitric oxide synthase in the rat suggests frequent colocalization with NADPH diaphorase but not with soluble guanyl cyclase and novel paraneural functions of nitrinergic signal transduction, J. Histochem. Cytochem., 40 (1992) 1439-1456.
63. [63] Schuman, E.M. and Madison, D.V., A requirement of the intercellular messenger nitric oxide in long-term potentiation, Science, 254 (1991) 1503-1506.
64. [64] Schuman, E.M. and Madison, D.V., Locally distributed synaptic potentiation in the hippocampus, Science, 263 (1994) 532-536.
65. [65] Schuman, E.M. and Madison, D.V., Nitric oxide and synaptic function, Annu. Rev. Neurosci., 17 (1994) 153-183.
66. [66] Shibuki, K. and Okada, D., Endogenous nitric oxide release required for long-term synaptic depression in the cerebellum, Nature, 349 (1991) 326-328.
67. [67] Torres, G., Lee, S. and Rivier, C., Ontogeny of the rat hypothalamic nitric oxide synthase and co-localization with neuropeptides, Mol. Cellul. Neurosci., 4 (1993) 155-163.
68. [68] Vincent, S.R., Johansson, O., Hokfelt, T., Skirboll, L., Elde, R.P., Terenius, L., Kimmel, J. and Goldstein, M., NADPH-diaphorase: a selective histochemical marker for striatal neurons containing both somatostatin and avian pancreatic polypeptide (APP)-like immunoreactivity, J. Comp. Neurol., 217 (1993) 252-263.
69. [69] Vincent, S.R. and Kimura, H., Histochemical mapping of nitric oxide synthase in the rat brain, Neuroscience, 46 (1992) 755-784.
70. [70] Vizzard, M.A., Erdman, S.L., Föstermann, U. and deGroat, W.C., Differential distribution of nitric oxide synthase in neural pathways to the urogenital organic (urethra, penis, urinary bladder) of the rat, Brain Res., 646 (1994) 279-291.
71. [71] Vizzard, M.A., Erdman, S.L., Roppolo, J.R., Föstermann, U. and deGroat, W.C., Differential localization of neuronal nitric synthase immunoreactivity and NADPH-diaphorase activity in the cat spinal cord, Cell Tiss. Res., 278 (1994) 299-309.
72. [72] Ward, S.M., Xue, C., Shuttleworth, C.W., Bredt, D.S., Snyder, S.H. and Sanders, K.M., NADPH diaphorase and nitric oxide synthase colocalization in enteric neurons of canine proximal colon, Am. J. Physiol., 263 (Gastrointest. Liver Physiol., 26) (1992) G277-G284.
73. [73] Wu, H.H., Williams, C.V. and McLoon, S.C., Involvement of a nitric oxide in the elimination of a transient retinotectal projection in development, Science, 265 (1994) 1593-1596.
74. [74] Zhuo, M., Small, S.A., Kandel, E.R. and Hawkins, R.D., Nitric oxide and carbon monoxide produce activity-dependent long-term synaptic enhancement in hippocampus, Science, 260 (1993) 1946-1950.