Daily rhythms and sex differences in vasoactive intestinal polypeptide, VIPR2 receptor and arginine vasopressin mRNA in the suprachiasmatic nucleus of a diurnal rodent, Arvicanthis niloticus

European Journal of Neuroscience

Volumn 30, Issue 8, 2009, Pages 1537-1543

  Mahoney, M M ^a   Ramanathan, C ^b   Hagenauer, M H ^c   Thompson, R C ^c   Smale, L ^b   Lee, T ^c,d  

^a UNIVERSITY OF ILLINOIS AT URBANA CHAMPAIGN   (United States)

^b MICHIGAN STATE UNIVERSITY   (United States)

^c UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

^d UNIVERSITY OF MICHIGAN   (United States)

Author keywords

Circadian rhythm; Grass rat; VIP receptor

Indexed keywords

ARGIPRESSIN; ESTRADIOL; LUTEINIZING HORMONE; NEUROPEPTIDE; VASOACTIVE INTESTINAL POLYPEPTIDE RECEPTOR;

ANIMAL EXPERIMENT; ARTICLE; ARVICANTHIS NILOTICUS; CIRCADIAN RHYTHM; CONTROLLED STUDY; DIURNAL ANIMAL; FEMALE; GENE EXPRESSION; IN SITU HYBRIDIZATION; LIGHT DARK CYCLE; MALE; NOCTURNAL ANIMAL; NONHUMAN; NUCLEOTIDE SEQUENCE; OVARIECTOMY; OVULATION; PRIORITY JOURNAL; RAT; RODENT; SEX DIFFERENCE; SUPRACHIASMATIC NUCLEUS;

ANIMALS; ARGININE VASOPRESSIN; ARVICOLINAE; CIRCADIAN RHYTHM; ESTRADIOL; ESTROGENS; FEMALE; GENE EXPRESSION REGULATION; MALE; OVARIECTOMY; RECEPTORS, VASOACTIVE INTESTINAL PEPTIDE, TYPE II; RNA, MESSENGER; SEX CHARACTERISTICS; SEXUAL BEHAVIOR, ANIMAL; SUPRACHIASMATIC NUCLEUS;

EID: 70350217620     PISSN: 0953816X     EISSN: 14609568     Source Type: Journal    
DOI: 10.1111/j.1460-9568.2009.06936.x     Document Type: Article

References (44)

1. Alleva, J.J., Waleski, M.V. Alleva, F.R. (1971) A biological clock controlling the estrous cycle of the hamster. Endocrinology, 88, 1368 1379.
2. Becu-Villalobos, D., Gonzalez Iglesias, A., Diaz-Torga, G., Hockl, P. Libertun, C. (1997) Brain sexual differentiation and gonadotropins secretion in the rat. Cell. Mol. Neurobiol., 17, 699 715.
3. van der Beek, E.M., Wiegant, V.M., van der Donk, H.A., van den Hurk, R. Buijs, R.M. (1993) Lesions of the suprachiasmatic nucleus indicate the presence of a direct vasoactive intestinal polypeptide-containing projection to gonadotropin-releasing hormone neurons in the female rat. J. Neuroendocrinol., 5, 137 144.
4. van der Beek, E.M., Horvath, T.L., Weigant, V.M., van den Hurk, R. Buijs, R. (1997) Evidence for a direct neuronal pathway from the suprachiasmatic nucleus to the gonadotrophin-releasing hormone system: combined tracing and light and electron microscopic immunocytochemical studies. J. Comp. Neurol., 384, 569 579.
5. van der Beek, E.M., Palm, I.F., Horvath, T.L., Kastelijn, J. Wiegant, V.M. (1998) Gender specific apposition of SCN-derived vasopressin containing axons on GnRH neurons in the preoptic area of adult rats. Soc. Neurosci. Abstr., 24, 545.
6. van der Beek, E.M., Swarts, H.J. Wiegant, V.M. (1999) Central administration of antiserum to vasoactive intestinal peptide delays and reduces luteinizing hormone and prolactin surges in ovariectomized, estrogen-treated rats. Neuroendocrinology, 69, 227 237.
7. Cintra, A., Fuxe, K., Harfstrand, A., Agnati, L.F., Miller, L.S., Greene, J.L. Gustafsson, J.A. (1986) On the cellular-localization and distribution of estrogen- receptors in the rat telencephalon and diencephalon using monoclonal-antibodies to human estrogen-receptor. Neurochem. Int., 8, 587 595.
8. Dardente, H., Menet, J.S., Challet, E., Tournier, B.B., Pevet, P. Masson-Pevet, M. (2004) Daily and circadian expression of neuropeptides in the suprachiasmatic nuclei of nocturnal and diurnal rodents. Brain Res. Mol. Brain Res., 124, 143 151.
9. Duncan, M.J., Cheng, X. Heller, K.S. (1995) Photoperiodic exposure and time of day modulate the expression of arginine vasopressin mRNA and vasoactive intestinal peptide mRNA in the suprachiasmatic nuclei of Siberian hamsters. Brain Res. Mol. Brain Res., 32, 181 186.
10. Duncan, M.J., Herron, J.M. Hill, S.A. (2001) Aging selectively suppresses vasoactive intestinal peptide messenger RNA expression in the suprachiasmatic nucleus of the Syrian hamster. Brain Res. Mol. Brain Res., 87, 196 203.
11. Funabashi, T., Aiba, S., Sano, A., Shinohara, K. Kimura, F. (1999) Intracerebroventricular injection of arginine-vasopressin V1 receptor antagonist attenuates the surge of luteinizing hormone and prolactin secretion in proestrous rats. Neurosci. Lett., 260, 37 40.
12. Gibson, E.M., Humber, S.A., Jain, S., Williams, W.P. III., Zhao, S., Bentley, G.E., Tsutsui, K. Kriegsfeld, L.J. (2008) Alterations in RFamide-related peptide expression are coordinated with the preovulatory luteinizing hormone surge. Endocrinology, 149, 4958 4969.
13. Harney, J.P., Scarbrough, K., Rosewell, K.L. Wise, P.M. (1996) In vivo antisense antagonism of vasoactive intestinal peptide in the suprachiasmatic nuclei causes aging-like changes in the estradiol-induced luteinizing hormone and prolactin surges. Endocrinology, 137, 3696 3701.
14. Huhman, K.L. van der Beek, E.M. (1996) Peptidergic innervation of gonadotropin releasing hormone (GnRH) neurons in female Syrian hamsters. Soc. Neurosci. Abstr., 22, 451.
15. de la Iglesia, H.O. Schwartz, W.J. (2006) Minireview: timely ovulation: circadian regulation of the female hypothalamo-pituitary-gonadal axis. Endocrinology, 147, 1148 1153.
16. de la Iglesia, H.O., Blaustein, J.D. Bittman, E.L. (1999) Oestrogen receptor-a-immunoreactive neurones project to the suprachiasmatic nucleus of the female syrian hamster. J. Neuroendocrinol., 11, 481 490.
17. Kallo, I., Kalamatianos, T., Piggins, H.D. Coen, C.W. (2004) Ageing and the diurnal expression of mRNAs for vasoactive intestinal peptide and for the VPAC2 and PAC1 receptors in the suprachiasmatic nucleus of male rats. J. Neuroendocrinol., 16, 758 766. (Pubitemid 39307222)
18. Kalsbeek, A., Verhagen, L.A., Schalij, I., Foppen, E., Saboureau, M., Bothorel, B., Buijs, R.M. Pevet, P. (2008) Opposite actions of hypothalamic vasopressin on circadian corticosterone rhythm in nocturnal versus diurnal species. Eur. J. Neurosci., 27, 818 827.
19. Klein, D.C., Moore, R.Y. Reppert, S.M eds 1991) Suprachiasmatic Nucleus: The Mind's Clock. Oxford University Press, New York.
20. Krajnak, K., Kashon, M.L., Rosewell, K.L. Wise, P.M. (1998a) Aging alters the rhythmic expression of vasoactive intestinal polypeptide mRNA but not arginine vasopressin mRNA in the suprachiasmatic nucleus of female rats. J Neuroscience, 18, 4767 4774.
21. Krajnak, K., Kashon, M.L., Rosewell, K.L. Wise, P.M. (1998b) Sex differences in the daily rhythm of vasoactive intestinal polypeptide but not arginine vasopressin messenger ribonucleic acid in the suprachiasmatic nuclei. Endocrinology, 139, 4189 4196.
22. Kriegsfeld, L.J. Silver, R. (2006) The regulation of neuroendocrine function: timing is everything. Horm. Behav., 49, 557 574.
23. Kruijver, F.P., Balesar, R., Espila, A.M., Unmehopa, U.A. Swaab, D.F. (2003) Estrogen-receptor-beta distribution in the human hypothalamus: similarities and differences with ERalpha distribution. J. Comp. Neurol., 466, 251 277.
24. Lambert, C.M., Machida, K.K., Smale, L., Nunez, A.A. Weaver, D.R. (2005) Analysis of the prokineticin 2 system in a diurnal rodent, the unstriped Nile grass rat (Arvicanthis niloticus). J. Biol. Rhythms, 20, 206 218.
25. Mahoney, M.M. Smale, L. (2005) A daily rhythm in mating behavior in a diurnal murid rodent Arvicanthis niloticus. Horm. Behav., 47, 8 13.
26. McElhinny, T.L. (1996) Reproductive Biology and Biological Rhythms in Arvicanthis niloticus. Department of Zoology, Michigan State University, East Lansing (MI).
27. McElhinny, T.L., Sisk, C.L., Holekamp, K.E. Smale, L. (1999) A morning surge in plasma luteinizing hormone coincides with elevated Fos expression in gonadotropin-releasing hormone-immunoreactive neurons in the diurnal rodent, Arvicanthis niloticus. Biol. Reprod., 61, 1115 1122.
28. Nakamura, T.J., Shinohara, K., Funabashi, T. Kimura, F. (2001) Effect of estrogen on the expression of Cry1 and Cry2 mRNAs in the suprachiasmatic nucleus of female rats. Neurosci. Res., 41, 251 255. (Pubitemid 32982892)
29. Nakamura, T.J., Moriya, T., Inoue, S., Shimazoe, T., Watanabe, S., Ebihara, S. Shinohara, K. (2005) Estrogen differentially regulates expression of Per1 and Per2 genes between central and peripheral clocks and between reproductive and nonreproductive tissues in female rats. J. Neurosci. Res., 82, 622 630.
30. Palm, I.F., van der Beek, E.M., Wiegant, V.M., Buijs, R.M. Kalsbeek, A. (1999) Vasopressin induces a luteinizing hormone surge in ovariectomized, estradiol-treated rats with lesions of the suprachiasmatic nucleus. Neuroscience, 93, 659 666.
31. Palm, I.F., van der Beek, E.M., Wiegant, V.M., Buijs, R.M. Kalsbeek, A. (2001) The stimulatory effect of vasopressin on the luteinizing hormone surge in ovariectomized, estradiol-treated rats is time-dependent. Brain Res., 901, 109 116.
32. Perreau-Lenz, S., Pevet, P., Buijs, R.M. Kalsbeek, A. (2004) The biological clock: the bodyguard of temporal homeostasis. Chronobiol. Int., 21, 1 25.
33. Peterfi, Z., Churchill, L., Hajdu, I., Obal, F. Jr., Krueger, J.M. Parducz, A. (2004) Fos-immunoreactivity in the hypothalamus: dependency on the diurnal rhythm, sleep, gender, and estrogen. Neuroscience, 124, 695 707.
34. Ramanathan, C., Nunez, A.A., Martinez, G.S., Schwartz, M.D. Smale, L. (2006) Temporal and spatial distribution of immunoreactive PER1 and PER2 proteins in the suprachiasmatic nucleus and peri-suprachiasmatic region of the diurnal grass rat (Arvicanthis niloticus). Brain Res., 1073-1074, 348 358.
35. Schwartz, M.D., Nunez, A.A. Smale, L. (2004) Differences in the suprachiasmatic nucleus and lower subparaventricular zone of diurnal and nocturnal rodents. Neuroscience, 127, 13 23.
36. Shinohara, K., Funabashi, T. Kimura, F. (1999) Temporal profiles of vasoactive intestinal polypeptide precursor mRNA and its receptor mRNA in the rat suprachiasmatic nucleus. Brain Res. Mol. Brain Res., 63, 262 267.
37. Shinohara, K., Funabashi, T., Nakamura, T.J. Kimura, F. (2001) Effects of estrogen and progesterone on the expression of connexin-36 mRNA in the suprachiasmatic nucleus of female rats. Neurosci. Lett., 309, 37 40. (Pubitemid 32728254)
38. Smale, L. Boverhof, J. (1999) The suprachiasmatic nucleus and intergeniculate leaflet of Arvicanthis niloticus, a diurnal murid rodent from East Africa. J. Comp. Neurol., 403, 190 208.
39. Smale, L., Lee, T. Nunez, A.A. (2003) Mammalian diurnality: some facts and gaps. J. Biol. Rhythms, 18, 356 366.
40. Sodersten, P., Eneroth, P. Hansen, S. (1981) Neuroendocrine control of daily rhythms in rat reproductive behavior. In Fuxe, K., Wetterberg, L. Gustafsson, J.A. (Eds Steroid Hormonal Regulation of Brain. Pergamon, New York, pp. 301 315.
41. Su, J.D., Qiu, J., Zhong, Y.P. Chen, Y.Z. (2001) Expression of estrogen receptor -alpha and -beta immunoreactivity in the cultured neonatal suprachiasmatic nucleus: with special attention to GABAergic neurons. NeuroReport, 12, 1955 1959. (Pubitemid 32553714)
42. Thind, K.K., Boggan, J.E. Goldsmith, P.C. (1991) Interactions between vasopressin- and gonadotropin-releasing-hormone-containing neuroendocrine neurons in the monkey supraoptic nucleus. Neuroendocrinology, 53, 287 297.
43. Vida, B., Hrabovszky, E., Kalamatianos, T., Coen, C.W., Liposits, Z. Kallo, I. (2008) Oestrogen receptor alpha and beta immunoreactive cells in the suprachiasmatic nucleus of mice: distribution, sex differences and regulation by gonadal hormones. J. Neuroendocrinol., 20, 1270 1277.
44. Weigand, S.J. Terasawa, E. (1982) Discrete lesions reveal functional heterogeneity of suprachiasmatic structures in regulation of gonadotropin secretion in the female rat. Neuroendocrinology, 34, 395 404.