Possible involvement of microglia containing cyclooxygenase-1 in the accumulation of gonadotrophin-releasing hormone in the preoptic area in female rats

Journal of Neuroendocrinology

Volumn 21, Issue 12, 2009, Pages 1029-1037

  Adachi, S ^a   Fujioka, H ^a   Kakehashi, C ^a   Matsuwaki, T ^b   Nishihara, M ^b   Akema, T ^a  

^a ST MARIANNA UNIVERSITY SCHOOL OF MEDICINE   (Japan)

^b UNIVERSITY OF TOKYO   (Japan)

Author keywords

Cyclooxygenase; Gonadotrophin releasing hormone; Microglia; Prostaglandin

Indexed keywords

CYCLOOXYGENASE 1; ESTROGEN; FLURBIPROFEN; GONADORELIN; INDOMETACIN; N (2 CYCLOHEXYLOXY 4 NITROPHENYL)METHANESULFONAMIDE; PROGESTERONE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CELL COUNT; CELL TYPE; CONTROLLED STUDY; ENZYME LOCALIZATION; FEMALE; HORMONAL REGULATION; HORMONE RELEASE; IMMUNOFLUORESCENCE; IMMUNOREACTIVITY; MICROGLIA; NERVE CELL; NONHUMAN; PERIKARYON; PREOPTIC AREA; PRIORITY JOURNAL; RAT;

ANIMALS; ASTROCYTES; CYCLOOXYGENASE 1; CYCLOOXYGENASE 2 INHIBITORS; CYCLOOXYGENASE INHIBITORS; ESTROGENS; FEMALE; FLURBIPROFEN; GONADOTROPIN-RELEASING HORMONE; INDOMETHACIN; LUTEINIZING HORMONE; MEMBRANE PROTEINS; MICROGLIA; NEURONS; NITROBENZENES; OVARIECTOMY; PREOPTIC AREA; PROGESTERONE; RATS; RATS, WISTAR; SULFONAMIDES; TIME FACTORS;

EID: 70949105509     PISSN: 09538194     EISSN: 13652826     Source Type: Journal    
DOI: 10.1111/j.1365-2826.2009.01928.x     Document Type: Article

References (59)

1. Ojeda SR, Urbanski HF, Junier MP, Capdevila J. The role of arachidonic acid and its metabolites in the release of neuropeptides. Ann NY Acad Sci 1989, 559:192-207.
2. Kuderling I, Dorsch G, Warnhoff M, Pirke KM. The actions of prostaglandin E2, naloxone and testosterone on starvation-induced suppression of luteinizing hormone-releasing hormone and luteinizing-hormone secretion. In vitro and in vivo studies. Neuroendocrinology 1984, 39:530-537.
3. Ojeda SR, Negro-Vilar A. Prostaglandin E2-induced luteinizing hormone-releasing hormone release involves mobilization of intracellular Ca+2. Endocrinology 1985, 116:1763-1770.
4. Gerozissis K, Bommelaer-Bayet MC, Wisner A, Saadi M, Ramassamy C, Dray F. Prostaglandin E2 and leukotriene C4-induced luteinizing hormone-releasing hormone release from immature and adult male rat median eminences in vitro: eicosanoid formation and binding parameters. Prostaglandins 1991, 41:345-357.
5. Nakamura K, Kaneko T, Yamashita Y, Hasegawa H, Katoh H, Negishi M. Immunohistochemical localization of prostaglandin EP3 receptor in the rat nervous system. J Comp Neurol 2000, 421:543-569.
6. Rage F, Lee BJ, Ma YJ, Ojeda SR. Estradiol enhances prostaglandin E2 receptor gene expression in luteinizing hormone-releasing hormone (LHRH) neurons and facilitates the LHRH response to PGE2 by activating a glia-to-neuron signaling pathway. J Neurosci 1997, 17:9145-9156.
7. Jasoni CL, Todman MG, Han S-K, Herbison AE. Expression of mRNAs encoding receptors that mediate stress signals in gonadotropin-releasing hormone neurons of the mouse. Neuroendocrinology 2005, 82:320-328.
8. Feng L, Sun W, Xia Y, Tang WW, Chanmugam P, Soyoola E, Wilson CB, Hwang D. Cloning two isoforms of rat cyclooxygenase: differential regulation of their expression. Arch Biochem Biophys 1993, 307:361-368.
9. Vane JR, Bakhle YS, Botting RM. Cyclooxygenases 1 and 2. Ann Rev Pharmacol Toxicol 1998, 38:97-120.
10. Simmons DL, Botting RM, Hla T. Cyclooxygenase isozymes: the biology of prostaglandin synthesis and inhibition. Pharmacol Rev 2004, 56:387-437.
11. Chandrasekharan NV, Dai H, Roos K, Evanson NK, Tomsik J, Elton TS, Simmons DL. COX-3, a cyclooxygenase-1 variant inhibited by acetaminophen and other analgesic/antipyretic drugs: cloning, structure, and expression. Proc Natl Acad Sci USA 2002, 99:13926-13931.
12. Dubois RN, Abramson SB, Crofford L, Gupta RA, Simon LS, van de Putte LBA, Lipsky PE. Cyclooxygenase in biology and disease. FASEB J 1998, 12:1063-1073.
13. Parente L, Perretti M. Advances in the pathophysiology of constitutive and inducible cyclooxygenases: two enzymes in the spotlight. Biochem Pharmacol 2003, 65:153-159.
14. Breder CD, Dewit D, Kraig RP. Characterization of inducible cyclooxygenase in rat brain. J Comp Neurol 1995, 355:296-315.
15. Hetu P-O, Riendeau D. Cyclo-oxygenase-2 contributes to constitutive prostanoid production in rat kidney and brain. Biochem J 2005, 391:561-566.
16. Schneider C, Boeglin WE, Brash AR. Human cyclo-oxygenase-1 and an alternative splice variant: contrasts in expression of mRNA, protein and catalytic activities. Biochem J 2005, 385:57-64.
17. Kis B, Snipes JA, Busija DW. Acetaminophen and the cyclooxygenase-3 puzzle: sorting out facts, fictions, and uncertainties. J Pharmacol Exp Ther 2005, 315:1-7.
18. Zu S, Guo S, Jiang X, Yin Q, Umezawa T, Hisamitsu T. Effect of indomethacin on the c-fos expression in AVP and TH neurons in rat brain induced by lipopolysaccharide. Brain Res 2003, 966:13-18.
19. Rothwell NJ, Busbridge NJ, Lefeuvre RA, Hardwick AJ, Gauldie J, Hopkins SJ. Interleukin-6 is a centrally acting endogenous pyrogen in the rat. Can J Physiol Pharmacol 1991, 69:1465-1469.
20. Matsumura K, Cao C, Watanabe Y. Possible role of cyclooxygenase-2 in the brain vasculature in febrile response. Ann NY Acad Sci 1997, 813:302-306.
21. Terao A, Matsumura H, Yoneda H, Saito M. Enhancement of slow-wave sleep by tumor necrosis factor-α is mediated by cyclooxygenase-2 in rats. Neuroreport 1998, 9:3791-3796.
22. 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.
23. Chiba A, Akema T, Toyoda J. Effects of pinealectomy and melatonin on the timing of the proestrous luteinizing hormone surge in the rat. Neuroendocrinology 1994, 59:163-168.
24. Nakagawa T, Wakamatsu K, Zhang N, Maeda S, Minami M, Satoh M, Kaneko S. Intrathecal administration of ATP produces long-lasting allodynia in rats: differential mechanisms in the phase of the induction and maintenance. Neuroscience 2007, 147:445-455.
25. Albe-Fessard D, Libouban S, Stutinsky F. Atlas stéréotaxique du diencéphale du rat blanc 1966, Paris, Centre National de la Recherche Scientifique
26. Funabashi T, Jinnai K, Kimura F. Bicuculline infusion advances the timing of Fos expression in LHRH neurons in the preoptic area of proestrous rats. Neuroreport 1997, 8:771-774.
27. Mitsushima D, Funabashi T, Kimura F. Fos expression in gonadotropin-releasing hormone neurons by naloxone or bicuculline in intact male rats. Brain Res 1999, 839:209-212.
28. Ojeda SR, Harms PG, McCann SM. Effect of inhibitors of prostaglandin synthesis on gonadotropin release in the rat. Endocrinology 1975, 97:843-854.
29. Anton RF, Wallis C, Randall CL. In vivo regional levels of PGE and thromboxane in mouse brain: effect of decapitation, focused microwave fixation, and indomethacin. Prostaglandins 1983, 26:421-429.
30. Rudy TA, Williams JW, Yaksh TL. Antagonism by indomethacin of neurogenic hyperthermia produced by unilateral puncture of the anterior hypothalamic/preoptic region. J Physiol 1977, 272:721-736.
31. Linton EA, Bennett GW, Whitehead SA. Prostaglandins and the release of LHRH from hypothalamic synaptosomes. Effects of indomethacin pretreatment. Neuroendocrinology 1979, 28:394-401.
32. Herbison AE, Porteous R, Pape JR, Mora JM, Hurst PR. Gonadotropin-releasing hormone neuron requirements for puberty, ovulation, and fertility. Endocrinology 2008, 149:597-604.
33. Sarkar DM, Chiappa SA, Fink G. Gonadotropin-releasing hormone surge in pro-oestrous rats. Nature 1976, 264:461-466.
34. Levine JE, Ramirez VD. Luteinizing hormone-releasing hormone release during the rat estrous cycle and after ovariectomy, as estimated with push-pull cannulae. Endocrinology 1982, 111:1439-1448.
35. Wang H-J, Hoffman GE, Smith MS. Increased GnRH mRNA in the GnRH neurons expressing cFos during the proestrous LH surge. Endocrinology 1995, 136:3673-3676.
36. Ottem EN, Godwin JG, Petersen SL. Glutamatergic signaling through the N-methyl-d-aspartate receptor directly activates medial subpopulations of luteinizing hormone-releasing hormone (LHRH) neurons, but does not appear to mediate the effects of oestradiol on LHRH gene expression. Endocrinology 2002, 143:4837-4845.
37. Luo J, Lang JA, Miller MW. Transforming growth factor β1 regulates expression of cyclooxygenase in cultured cortical astrocytes and neurons. J Neurochem 1998, 71:526-534.
38. Pardue S, Rapoport SI, Bosetti F. Co-localization of cytosolic phospholipase A and cyclooxygenase-2 in 2 rhesus monkey cerebellum. Brain Res Mol Brain Res 2003, 116:106-114.
39. Ju W-K, Neufeld AH. Cellular localization of cyclooxygenase-1 and cyclooxygenase-2 in the normal mouse, rat, and human retina. J Comp Neurol 2002, 452:392-399.
40. Maihofner C, Tegeder I, Euchenhofer C, Dewitt D, Brune K, Bang R, Neuhuber W, Geisslinger G. Localization and regulation of cyclooxygenase- 1 and -2 and neuronal nitric oxide synthase in mouse spinal cord. Neuroscience 2000, 101:1093-1108.
41. Thore CR, Nam MJ, Busija DW. Immunofluorescent localization of constitutive and inducible prostaglandin H synthase in ovine astroglia. J Comp Neurol 1996, 367:1-9.
42. Hoozemans JJM, Rozemuller AJM, Janssen I, De Groot CJA, Veerhuis R, Eikelenboom P. Cyclooxygenase expression in microglia and neurons in Alzheimer's disease and control brain. Acta Neuropathol 2001, 101:2-8.
43. Deininger MH, Weller M, Streffer J, Mittelbronn M, Meyermann R. Patterns of cyclooxygenase-1 and -2 expression in human gliomas in vivo. Acta Neuropathol 1999, 98:240-244.
44. Mahesh VB, Dhandapani KM, Brann DW. Role of astrocytes in reproduction and neuroprotection. Mol Cell Endocrinol 2006, 246:1-9.
45. Garcia-Segura LM, Betty Lorenz B, DonCarlos LL. The role of glia in the hypothalamus: implications for gonadal steroid feedback and reproductive neuroendocrine output. Reproduction 2008, 135:419-429.
46. Ojeda SR, Lomniczi A, Sandau US. Glial-gonadotrophin hormone (GnRH) neurone interactions in the median eminence and the control of GnRH secretion. J Neuroendocrinol 2008, 20:732-742.
47. Micevych PE, Chaban V, Ogi J, Dewing P, Lu JK, Sinchak K. Estradiol stimulates progesterone synthesis in hypothalamic astrocyte cultures. Endocrinology 2007, 148:782-789.
48. Mor G, Nilsen J, Horvath T, Bechmann I, Brown S, Garcia-Segura LM, Naftolin F. Estrogen and microglia: a regulatory system that affects the brain. J Neurobiol 1999, 40:484-496.
49. Sierra A, Gottfried-Blackmore A, Milner TA, McEwen BS, Bulloch K. Steroid hormone receptor expression and function in microglia. Glia 2008, 56:659-674.
50. Gottfried-Blackmore A, Sierra A, Jellinck PH, McEwen BS, Bulloch K. Brain microglia express steroid-converting enzymes in the mouse. J Steroid Biochem Mol Biol 2008, 109:96-107.
51. Baker AE, Brautigam VM, Watters JJ. Estrogen modulates microglial inflammatory mediator production via interactions with estrogen receptor β. Endocrinology 2004, 145:5021-5032.
52. Hanisch UK, Kettenmann H. Microglia: active sensor and versatile effector cells in the normal and pathologic brain. Nature Neurosci 2007, 10:1387-1394.
53. Kim SU, de Vellis J. Microglia in health and disease. J Neurosci Res 2005, 81:302-313.
54. Cullheim S, Thams S. The microglial networks of the brain and their role in neuronal network plasticity after lesion. Brain Res Rev 2007, 55:89-96.
55. Cohen PE, Zhu L, Nishimura K, Pollard JW. Colony-stimulating factor 1 regulation of neuroendocrine pathways that control gonadal function in mice. Endocrinology 2002, 143:1413-1422.
56. Sun X-R, Hedger MP, Risbridger GP. The effect of testicular macrophages and interleukin-1 on testosterone production by purified adult rat Leydig cells cultured under in vitro maintenance conditions. Endocrinology 1993, 132:186-192.
57. Hutson JC, Garner CW, Doris PA. Purification and characterization of a lipophilic factor from testicular macrophages that stimulates testosterone production by Leydig cells. J Androl 1996, 17:502-508.
58. Gilchrist RB, Rowe DB, Ritter LJ, Robertson SA, Norman RJ, Armstrong DT. Effect of granulocyte-macrophage colony-stimulating factor deficiency on ovarian follicular cell function. J Reprod Fertil 2000, 120:283-292.
59. Cohen PE, Nishimura K, Zhu L, Pollard JW. Macrophages: important accessory cells for reproductive function. J Leukoc Biol 1999, 66:765-772.