Hypothalamic Kiss1 and RFRP gene expressions are changed by a high dose of lipopolysaccharide in female rats

Hormones and Behavior

Volumn 66, Issue 2, 2014, Pages 309-316

  Iwasa, Takeshi ^a   Matsuzaki, Toshiya ^a   Tungalagsuvd, Altankhuu ^a   Munkhzaya, Munkhsaikhan ^a   Kawami, Takako ^a   Niki, Hirobumi ^a   Kato, Takeshi ^a   Kuwahara, Akira ^a   Uemura, Hirokazu ^a   Yasui, Toshiyuki ^a   Irahara, Minoru ^a  

^a UNIVERSITY OF TOKUSHIMA   (Japan)

Author keywords

GnRH; GPR147; Kiss1; Kisspeptin; LPS; RFRP; Stress

Indexed keywords

GONADORELIN; LIPOPOLYSACCHARIDE; LUTEINIZING HORMONE; MESSENGER RNA; METASTIN; HORMONE; KISS1 PROTEIN, RAT; KISSPEPTIN; NEUROPEPTIDE; RFAMIDE PEPTIDE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANOREXIA; ARTICLE; ENERGY; FEMALE; FEVER; GENE; GENE EXPRESSION; GNRH GENE; GONADOTROPIN RELEASE; GPR147 GENE; HYPOTHALAMUS; IMMUNE RESPONSE; KISS1 GENE; LUTEINIZING HORMONE BLOOD LEVEL; NONHUMAN; OVARIECTOMY; PRIORITY JOURNAL; RAT; RFRP GENE; STRESS; ANIMAL; BIOSYNTHESIS; BLOOD; BODY TEMPERATURE; DOSE RESPONSE; DRUG EFFECTS; EATING; GENETICS; METABOLISM; SPRAGUE DAWLEY RAT;

ANIMALS; BODY TEMPERATURE; DOSE-RESPONSE RELATIONSHIP, DRUG; EATING; FEMALE; HORMONES; HYPOTHALAMUS; KISSPEPTINS; LIPOPOLYSACCHARIDES; NEUROPEPTIDES; OVARIECTOMY; RATS; RATS, SPRAGUE-DAWLEY;

EID: 84903442072     PISSN: 0018506X     EISSN: 10956867     Source Type: Journal    
DOI: 10.1016/j.yhbeh.2014.06.007     Document Type: Article

References (62)

1. Adelman J.S., Bentley G.E., Wingfield J.C., Martin L.B., Hau M. Population differences in fever and sickness behaviors in a wild passerine: a role for cytokines. J. Exp. Biol. 2010, 213:4099-4109.
2. Bonneaud C., Mazuc J., Gonzalez G., Haussy C., Chastel O., Faivre B., Sorci G. Assessing the cost of mounting an immune response. Am. Nat. 2003, 161:367-379.
3. Castellano J.M., Bentsen A.H., Romero M., Pineda R., Ruiz-Pino F., Garcia-Galiano D., Sanchez-Garrido M.A., Pinilla L., Mikkelsen J.D., Tena-Sempere M. Acute inflammation reduces kisspeptin immunoreactivity at the arcuate nucleus and decreases responsiveness to kisspeptin independently of its anorectic effects. Am. J. Physiol. Endocrinol. Metab. 2010, 299:54-61.
4. Chowdhury V.S., Tomonaga S., Nishimura S., Tabata S., Cockrem J.F., Tsutsui K., Furuse M. Hypothalamic gonadotropin-inhibitory hormone precursor mRNA is increased during depressed food intake in heat-exposed chicks. Comp. Biochem. Physiol. A Mol. Integr. Physiol. 2012, 162:227-233.
5. Clarke I.J., Qi Y., Sari I.P., Smith J.T. Evidence that RF-amide related peptides are inhibitors of reproduction in mammals. Front. Neuroendocrinol. 2009, 30:371-378.
6. Du Ruisseau P., Tache Y., Brazeau P., Collu R. Effects of chronic immobilization stress on pituitary hormone secretion, on hypothalamic factor levels, and on pituitary responsiveness to LHRH and TRH in female rats. Neuroendocrinology 1979, 29:90-99.
7. Ducret E., Anderson G.M., Herbison A.E. RFamide-related peptide-3, a mammalian gonadotropininhibitory hormone ortholog, regulates gonadotropin-releasing hormone neuron firing in the mouse. Endocrinology 2009, 150:2799-2804.
8. Ebisui O., Fukata J., Tominaga T., Murakami N., Kobayashi H., Segawa H., Muro S., Naito Y., Nakai Y., Masui Y., Nishida T., Imura H. Roles of interleukin-1a and -1b in endotoxin-induced suppression of plasma gonadotropin levels in rats. Endocrinology 1992, 130:3307-3313.
9. Faggioni R., Fantuzzi G., Fuller J., Dinarello C.A., Feingold K.R., Grunfeld C. IL-1b mediates leptin induction during inflammation. Am. J. Physiol. Regul. Integr. Comp. Physiol. 1998, 274:204-208.
10. Geary N., Asarian L., Sheahan J., Langhans W. Estradiol-mediated increases in the anorexia induced by intraperitoneal injection of bacterial lipopolysaccharide in female rats. Physiol. Behav. 2004, 82:251-261.
11. Gonzarez-Quijano M.I., Ariznavarreta C., Martin A.I., Treguerres J.A., Lopez-Calderon A. Naltrexone does not reverse the inhibitory effect of chronic restraint on gonadotropin secretion in the intact male rat. Neuroendocrinology 1991, 54:447-453.
12. Goymann W., Wingfield J.C. Allostatic load, social status and stress hormones: the costs of social status matter. Anim. Behav. 2004, 67:591-602.
13. Grunfeld C., Zhao C., Fuller J., Pollock A., Moser A., Friedman J., Feingold R. Endotoxin and cytokines induce expression of leptin, the ob gene product, in hamsters. J. Clin. Invest. 1996, 97:2152-2157.
14. Harris T.G., Battaglia D.F., Brown M.E., Brown M.B., Carlson N.E., Viguie C., Williams C.Y., Karsch F.J. Prostaglandins mediate the endotoxin-induced suppression of pulsatile gonadotropin-releasing hormone and luteinizing hormone secretion in the ewe. Endocrinology 2000, 141:1050-1058.
15. Hart B.L. Biological basis of the behavior of sick animals. Neurosci. Biobehav. Rev. 1988, 12:123-137.
16. He D., Sato I., Kimura F., Akema T. Lipopolysaccharide inhibits luteinizing hormone release through interaction with opioid and excitatory amino acid inputs to gonadotropin-releasing hormone neurones in female rats: possible evidence for a common mechanism involved in infection and immobilization stress. J. Neuroendocrinol. 2003, 15:559-563.
17. Hinuma S., Shintani Y., Fukusumi S., Iijima N., Matsumoto Y., Hosoya M., Fujii R., Watanabe T., Kikuchi K., Terao Y., Yano T., Yamamoto T., Kawamura Y., Habata Y., Asada M., Kitada C., Kurokawa T., Onda H., Nishimura O., Tanaka M., Ibata Y., Fujino M. New neuropeptides containing carboxy-terminal RFamide and their receptor in mammals. Nat. Cell Biol. 2000, 2:703-708.
18. Iwasa T., Matsuzaki T., Murakami M., Shimizu F., Kuwahara A., Yausi T., Irahara M. Decreased expression of kisspeptin mediates acute immune/inflammatory stress-induced suppression of gonadotropin secretion in female rat. J. Endocrinol. Invest. 2008, 31:656-659.
19. Iwasa T., Matsuzaki T., Murakami M., Fujisawa S., Kinouchi R., Gereltsetseg G., Kuwahara A., Yasui T., Irahara M. Effects of intrauterine undernutrition on hypothalamic Kiss1 expression and the timing of puberty in female rats. J. Physiol. 2010, 588:821-829.
20. Iwasa T., Matsuzaki T., Murakami M., Kinouchi R., Gereltsetseg G., Fujisawa S., Kuwahara A., Yasui T., Irahara M. Sensitivities of mRNA expression levels of Kiss1 and its receptor, Kiss1r, to undernutritional status are changed during the developmental period in female rats. J. Endocrinol. 2010, 207:195-202.
21. Iwasa T., Matsuzaki T., Murakami M., Kinouchi R., Gereltsetseg G., Nakazawa H., Yamamoto S., Kuwahara A., Yasui T., Irahara M. Changes in responsiveness of appetite, leptin and hypothalamic IL-1β and TNF-α to lipopolysaccharide in developing rats. J. Neuroimmunol. 2011, 236:10-16.
22. Iwasa T., Matsuzaki T., Kinouchi R., Gereltsetseg G., Murakami M., Munkhzaya M., Althankhuu T.S., Kuwahara A., Yasui T., Irahara M. Changes in central and peripheral inflammatory responses to lipopolysaccharide in ovariectomized female rats. Cytokine 2014, (in press).
23. Kalamatianos T., Grimshaw S.E., Poorun R., Hahn J.D., Coen C.W. Fasting reduces KiSS-1 expression in the anteroventral periventricular nucleus (AVPV): effects of fasting on the expression of KiSS-1 and neuropeptide Y in the AVPV or arcuate nucleus of female rats. J. Neuroendocrinol. 2008, 20:1089-1097.
24. Kirby E.D., Geraghty A.C., Ubuka T., Bentley G.E., Kaufer D. Stress increases putative gonadotropin inhibitory hormone and luteinizing hormone in male rats. Proc. Natl. Acad. Sci. U. S. A. 2009, 106:11324-11329.
25. Knox A.M., Li X.F., Kinsey-Jones J.S., Wilkinson E.S., Wu X.Q., Cheng Y.S., Milligan S.R., Lightman S.L., O'Byrne K.T. Neonatal lipopolysaccharide exposure delays puberty and alters hypothalamic Kiss1 and Kiss1r mRNA expression in the female rat. J. Neuroendocrinol. 2009, 21:683-689.
26. Kriegsfeld L.J., Mei D.F., Bentley G.E., Ubuka T., Mason A.O., Inoue K., Ukena K., Tsutsui K., Silver R. Identification and characterization of a gonadotropin-inhibitory system in the brain of mammals. Proc. Natl. Acad. Sci. U. S. A. 2006, 103:2410-2415.
27. Kriegsfeld L.J., Gibson E.M., Williams W.P., Zhao S., Mason A.O., Bentley G.E., Tsutsui K. The roles of RFamide-related peptide-3 in mammalian reproductive function and behavior. J. Neuroendocrinol. 2010, 22:692-700.
28. Lam K.K., Hu C.T., Ou T.Y., Yen M.H., Chen H.I. Effects of oestrogen replacement on steady and pulsatile haemodynamics in ovariectomized rats. Br. J. Pharmacol. 2002, 136:811-818.
29. Li X.F., Kinsey-Jones J.S., Knox A.M.I., Wu X.Q., Tahsinsoy D., Brain S.D., Lightman S.L., O'Byrne K.T. Neonatal lipopolysaccharide exposure exacerbates stress-induced suppression of LH pulse frequency in adulthood. Endocrinology 2007, 148:5984-5990.
30. Lopes P.C., Wingfield J.C., Bentley G.E. Lipopolysaccharide injection induces rapid decrease of hypothalamic GnRH mRNA and peptide, but does not affect GnIH in zebra finches. Horm. Behav. 2012, 62:173-179.
31. Luheshi G.N., Gardner J.D., Rushforth D.A., Loudon A.S. Leptin actions on food intake and body temperature are mediated by IL-1. Proc. Natl. Acad. Sci. U. S. A. 1999, 96:7047-7052.
32. Matsuwaki T., Kayasuga Y., Yamanouchi K., Nishihara M. Maintenance of gonadotropin secretion by glucocorticoids under stress conditions through the inhibition of prostaglandin synthesis in the brain. Endocrinology 2006, 147:1087-1093.
33. McEwen B.S. Stress, adaptation, and disease. Allostasis and allostatic load. Ann. N. Y. Acad. Sci. 1998, 840:33-44.
34. McEwen B.S., Gianaros P.J. Stress- and allostasis-induced brain plasticity. Annu. Rev. Med. 2011, 62:431-445.
35. McEwen B.S., Wingfield J.C. The concept of allostasis in biology and biomedicine. Horm. Behav. 2003, 43:2-15.
36. Meli R., Pacilio M., Raso G.M., Esposito E., Coppola A., Nasti A., Di Carlo C., Nappi C., Di Carlo R. Estrogen and raloxifene modulate leptin and its receptor in hypothalamus and adipose tissue from ovariectomized rats. Endocrinology 2004, 145:3115-3121.
37. Murakami M., Matsuzaki T., Iwasa T., Yasui T., Irahara M., Osugi T., Tsutsui K. Hypophysiotropic role of RFamide-related peptide-3 in the inhibition of LH secretion in female rats. J. Endocrinol. 2008, 199:105-112.
38. O'Callaghan E.K., Anderson S.T., Moynagh P.N., Coogan A.N. Long-lasting effects of sepsis on circadian rhythms in the mouse. PLoS One 2012, 7:e47087.
39. Owen-Ashley N.T., Turner M., Hahn T.P., Wingfield J.C. Hormonal, behavioral, and thermoregulatory responses to bacterial lipopolysaccharide in captive and free-living white-crowned sparrows (Zonotrichia leucophrys gambelii). Horm. Behav. 2006, 49:15-29.
40. Pauli S.A., Berga S.L. Athletic amenorrhea: energy deficit or psychogenic challenge?. Ann. N.Y. Acad. Sci. 2010, 1205:33-38.
41. Plata-Salaman C.R. Cytokines and feeding. Int. J. Obes. 2001, 25:48-52.
42. Qin L., Wu X., Block M.L., Liu Y., Breese G.R., Hong J.S., Knapp D.J., Crews F.T. Systemic LPS causes chronic neuroinflammation and progressive neurodegeneration. Glia 2007, 55:453-462.
43. Reddy M.M., Mahipal S.V., Subhashini J., Reddy M.C., Roy K.R., Reddy G.V., Reddy P.R., Reddanna P. Bacterial lipopolysaccharide-induced oxidative stress in the impairment of steroidogenesis and spermatogenesis in rats. Reprod. Toxicol. 2006, 22:493-500.
44. Refojo D., Arias P., Moguilevsky J.A., Feleder C. Effect of bacterial endotoxin on in vivo pulsatile gonadotropin secretion in adult male rats. Neuroendocrinology 1998, 67:275-281.
45. Rivier C., Rivest S. Effect of stress on the activity of the hypothalamic-pituitary-gonadal axis: peripheral and central mechanisms. Biol. Reprod. 1991, 45:523-532.
46. Rivier C., Rivier J., Vale W. Stress-induced inhibition of reproductive functions: role of endogenous corticotropin-releasing factor. Science 1986, 231:607-609.
47. Roa J., Navarro V.M., Tena-Sempere M. Kisspeptins in reproductive biology: consensus knowledge and recent developments. Biol. Reprod. 2011, 85:650-660.
48. Rogers N.H., Perfield J.W., Strissel J., Obin M.S., Greenberg A.S. Reduced energy expenditure and increased inflammation are early events in the development of ovariectomy-induced obesity. Endocrinology 2009, 150:2161-2168.
49. Sanchez-Garrido M.A., Tena-Sempere M. Metabolic control of puberty: roles of leptin and kisspeptins. Horm. Behav. 2013, 64:187-194.
50. Sari I.P., Rao A., Smith J.T., Tilbrook A.J., Clarke I.J. Effect of RF-amide-related peptide-3 on luteinizing hormone and follicle-stimulating hormone synthesis and secretion in ovine pituitary gonadotropes. Endocrinology 2009, 150:5549-5556.
51. Smith J.T. Sex steroid regulation of kisspeptin circuits. Adv. Exp. Med. Biol. 2013, 784:275-295.
52. Smith J.T., Coolen L.M., Kriegsfeld L.J., Sari I.P., Jaafarzadehshirazi M.R., Maltby M., Bateman K., Goodman R.L., Tilbrook A.J., Ubuka T., Bentley G.E., Clarke I.J., Lehman M.N. Variation in kisspeptin and RFamide-related peptide (RFRP) expression and terminal connections to gonadotropin-releasing hormone neurons in the brain: a novel medium for seasonal breeding in the sheep. Endocrinology 2008, 149:5770-5782.
53. Straub R.H. The complex role of estrogens in inflammation. Endocr. Rev. 2007, 28:521-574.
54. Tachibana T., Masuda N., Tsutsui K., Ukena K., Ueda H. The orexigenic effect of GnIH is mediated by central opioid receptors in chicks. Comp. Biochem. Physiol. A Mol. Integr. Physiol. 2008, 150:21-25.
55. Terasaka T., Otsuka F., Tsukamoto N., Nakamura E., Inagaki K., Toma K., Ogura-Ochi K., Glidewell-Kenney C., Lawson M.A., Makino H. Mutual interaction of kisspeptin, estrogen and bone morphogenetic protein-4 activity in GnRH regulation by GT1-7 cells. Mol. Cell. Endocrinol. 2013, 381:8-15.
56. Tsutusi K., Ubuka T., Bentley G.E., Kriegsfeld L.J. Review: regulatory mechanisms of gonadotropin-inhibitory hormone (GnIH) synthesis and release in photoperiodic animals. Front. Neurosci. 2014, (in press).
57. Ubuka T., Son Y.L., Bentley G.E., Millar R.P., Tsutsui K. Gonadotropin-inhibitory hormone (GnIH), GnIH receptor and cell signaling. Gen. Comp. Endocrinol. 2013, 190:10-17.
58. Watanobe H., Hayakawa Y. Hypothalamic interleukin-1b and tumor necrosis factor-a, but not interleukin-6, mediate the endotoxin-induced suppression of the reproductive axis in rats. Endocrinology 2003, 144:4868-4875.
59. Weberpals M., Hermes M., Hermann S., Kummer M.P., Terwel D., Semmler A., Berger M., Schäfers M., Heneka M.T. NOS2 gene deficiency protects from sepsis-induced long-term cognitive deficits. J. Neurosci. 2009, 29:14117-14184.
60. Wu M., Dumalska I., Morozova E., van den Pol A.N., Alreja M. Gonadotropin inhibitory hormone inhibits basal forebrain vGlu T2-gonadotropin-releasing hormone neurons via a direct postsynaptic mechanism. J. Physiol. 2009, 587:1401-1411.
61. Xiao E., Xia-Zhang L., Ferin M. Inhibitory effects of endotoxin on LH secretion in the ovariectomized monkey are prevented by naloxone but not by an interleukin-1 receptor antagonist. Neuroimmunomodulation 2000, 7:6-15.
62. Yirmiya R., Avitsur R., Donchin O., Cohen E. Interleukin-1 inhibits sexual behavior in female but not in male-rats. Brain Behav. Immun. 1995, 9:220-223.