Hormonal and spatial regulation of nitric oxide synthases (NOS) (Neuronal NOS, Inducible NOS, and Endothelial NOS) in the oviducts

Endocrinology

Volumn 147, Issue 12, 2006, Pages 5600-5610

  Lapointe, Jérome ^a,b   Roy, Monica ^a,b   St Pierre, Isabelle ^a,b   Kimmins, Sarah ^c   Gauvreau, Danny ^a   MacLaren, Leslie A ^c   Bilodeau, Jean François ^a,b,d  

^a LAVAL UNIVERSITY   (Canada)

^b UNIVERSITÉ LAVAL   (Canada)

^c DALHOUSIE UNIVERSITY   (Canada)

^d Unité d'Ontogénie et Reproduction   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

ENDOTHELIAL NITRIC OXIDE SYNTHASE; ESTRADIOL; INDUCIBLE NITRIC OXIDE SYNTHASE; NEURONAL NITRIC OXIDE SYNTHASE; NITRIC OXIDE SYNTHASE;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CELLULAR DISTRIBUTION; CONTROLLED STUDY; ESTRUS CYCLE; HORMONAL REGULATION; IMMUNOHISTOCHEMISTRY; IN VIVO STUDY; NONHUMAN; OVIDUCT; PRIORITY JOURNAL; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; UPREGULATION;

ANIMALS; CATTLE; ESTRADIOL; ESTROUS CYCLE; FALLOPIAN TUBES; FEMALE; GENE EXPRESSION REGULATION; NITRIC OXIDE SYNTHASE; NITRIC OXIDE SYNTHASE TYPE I; NITRIC OXIDE SYNTHASE TYPE II; NITRIC OXIDE SYNTHASE TYPE III; PROTEIN ISOFORMS; TISSUE DISTRIBUTION;

EID: 33751521819     PISSN: 00137227     EISSN: 00137227     Source Type: Journal    
DOI: 10.1210/en.2005-1548     Document Type: Article

References (87)

1. Alderton WK, Cooper CE, Knowles RG 2001 Nitric oxide synthases: structure, function and inhibition. Biochem J 357:593-615
2. Lorsbach RB, Murphy WJ, Lowenstein CJ, Snyder SH, Russell SW 1993 Expression of the nitric oxide synthase gene in mouse macrophages activated for tumor cell killing. Molecular basis for the synergy between interferon-γ and lipopolysaccharide. J Biol Chem 268:1908-1913
3. Mayer B, John M, Bohme E 1990 Purification of a Ca2+/calmodulin-dependent nitric oxide synthase from porcine cerebellum. Cofactor-role of tetrahydrobiopterin. FEBS Lett 277:215-219
4. Pollock JS, Forstermann U, Mitchell JA, Warner TD, Schmidt HH, Nakane M, Murad F 1991 Purification and characterization of particulate endothelium-derived relaxing factor synthase from cultured and native bovine aortic endothelial cells. Proc Natl Acad Sci USA 88:10480-10484
5. Forstermann U, Boissel JP, Kleinert H 1998 Expressional control of the 'constitutive' isoforms of nitric oxide synthase (NOS I and NOS III). FASEB J 12:773-790
6. Chartrain NA, Geller DA, Koty PP, Sitrin NF, Nussler AK, Hoffman EP, Billiar TR, Hutchinson NI, Mudgett JS 1994 Molecular cloning, structure, and chromosomal localization of the human inducible nitric oxide synthase gene. J Biol Chem 269:6765-6772
7. Aktan F 2004 iNOS-mediated nitric oxide production and its regulation. Life Sci 75:639-653
8. Han YJ, Kwon YG, Chung HT, Lee SK, Simmons RL, Billiar TR, Kim YM 2001 Antioxidant enzymes suppress nitric oxide production through the inhibition of NF-κB activation: role of H(2)O(2) and nitric oxide in inducible nitric oxide synthase expression in macrophages. Nitric Oxide 5:504-513
9. Kleinert H, Schwarz PM, Forstermann U 2003 Regulation of the expression of inducible nitric oxide synthase. Biol Chem 384:1343-1364
10. Albrecht EW, Stegeman CA, Heeringa P, Henning RH, van Goor H 2003 Protective role of endothelial nitric oxide synthase. J Pathol 199:8-17
11. Shen W, Hintze TH, Wolin MS 1995 Nitric oxide. An important signaling mechanism between vascular endothelium and parenchymal cells in the regulation of oxygen consumption. Circulation 92:3505-3512
12. Yun HY, Dawson VL, Dawson TM 1997 Nitric oxide in health and disease of the nervous system. Mol Psychiatry 2:300-310
13. Herrero MB, Gagnon C 2001 Nitric oxide: a novel mediator of sperm function. J Androl 22:349-356
14. Dixit VD, Parvizi N 2001 Nitric oxide and the control of reproduction. Anim Reprod Sci 65:1-16
15. -/-). Physiol Behav 67:561-566
16. Maul H, Longo M, Saade GR, Garfield RE 2003 Nitric oxide and its role during pregnancy: from ovulation to delivery. Curr Pharm Des 9:359-380
17. Gyurko R, Leupen S, Huang PL 2002 Deletion of exon 6 of the neuronal nitric oxide synthase gene in mice results in hypogonadism and infertility. Endocrinology 143:2767-2774
18. Dong YL, Gangula PR, Yallampalli C 1996 Nitric oxide synthase isoforms in the rat uterus: differential regulation during pregnancy and labour. J Reprod Fertil 107:249-254
19. Ali M, Buhimschi I, Chwalisz K, Garfield RE 1997 Changes in expression of the nitric oxide synthase isoforms in rat uterus and cervix during pregnancy and parturition. Mol Hum Reprod 3:995-1003
20. Motta AB, Estevez A, Tognetti T, Gimeno MA, Franchi AM 2001 Dual effects of nitric oxide in functional and regressing rat corpus luteum. Mol Hum Reprod 7:43-47
21. Zhang J, Massmann GA, Mirabile CP, Figueroa JP 1999 Nonpregnant sheep uterine type I and type III nitric oxide synthase expression is differentially regulated by estrogen. Biol Reprod 60:1198-1203
22. Thomson AJ, Telfer JF, Kohnen G, Young A, Cameron IT, Greer IA, Norman JE 1997 Nitric oxide synthase activity and localization do not change in uterus and placenta during human parturition. Hum Reprod 12:2546-2552
23. Ledingham MA, Thomson AJ, Young A, Macara LM, Greer IA, Norman JE 2000 Changes in the expression of nitric oxide synthase in the human uterine cervix during pregnancy and parturition. Mol Hum Reprod 6:1041-1048
24. Chwalisz K, Garfield RE 2000 Role of nitric oxide in implantation and menstruation. Hum Reprod 15(Suppl 3):96-111
25. Drazen DL, Klein SL, Burnett AL, Wallach EE, Crone JK, Huang PL, Nelson RJ 1999 Reproductive function in female mice lacking the gene for endothelial nitric oxide synthase. Nitric Oxide 3:366-374
26. Jablonka-Shariff A, Ravi S, Beltsos AN, Murphy LL, Olson LM 1999 Abnormal estrous cyclicity after disruption of endothelial and inducible nitric oxide synthase in mice. Biol Reprod 61:171-177
27. Tranguch S, Huet-Hudson Y 2003 Decreased viability of nitric oxide synthase double knockout mice. Mol Reprod Dev 65:175-179
28. Ekerhovd E, Norstrom A 2004 Involvement of a nitric oxide-cyclic guanosine monophosphate pathway in control of fallopian tube contractility. Gynecol Endocrinol 19:239-246
29. Wu TP, Huang BM, Tsai HC, Lui MC, Liu MY 2004 Effects of nitric oxide on human spermatozoa activity, fertilization and mouse embryonic development. Arch Androl 50:173-179
30. Jablonka-Shariff A, Basuray R, Olson LM 1999 Inhibitors of nitric oxide synthase influence oocyte maturation in rats. J Soc Gynecol Investig 6:95-101
31. Manser RC, Leese HJ, Houghton FD 2004 Effect of inhibiting nitric oxide production on mouse preimplantation embryo development and metabolism. Biol Reprod 71:528-533
32. Hunter RH 1988 The Fallopian tubes (their role in fertility and infertility). Berlin, Heidelberg, and New York: Springer-Verlag
33. Hafez ESE, Blandau RJ 1969 The Mammalian oviduct (comparative biology and methodology). Chicago: The University of Chicago Press
34. Mwanza AM, Einarsson S, Madej A, Lundeheim N, Rodriguez-Martinez H, Kindahl H 2002 Postovulatory effect of repeated administration of prostaglandin F2α on the endocrine status, ova transport, binding of accessory spermatozoa to the zona pellucida and embryo development of recently ovulated sows. Theriogenology 58:1111-1124
35. Bennett WA, Watts TL, Blair WD, Waldhalm SJ, Fuquay JW 1988 Patterns of oviducal motility in the cow during the oestrous cycle. J Reprod Fertil 83:537-543
36. Ellington JE 1991 The bovine oviduct and its role in reproduction: a review of the literature. Cornell Vet 81:313-328
37. Hunter RH 2002 Vital aspects of Fallopian tube physiology in pigs. Reprod Domest Anim 37:186-190
38. Rodriguez PC, O'Flaherty CM, Beconi MT, Beorlegui NB 2005 Nitric oxide-induced capacitation of cryopreserved bull spermatozoa and assessment of participating regulatory pathways. Anim Reprod Sci 85:231-242
39. Sengoku K, Tamate K, Yoshida T, Takaoka Y, Miyamoto T, Ishikawa M 1998 Effects of low concentrations of nitric oxide on the zona pellucida binding ability of human spermatozoa. Fertil Steril 69:522-527
40. Francavilla F, Santucci R, Macerola B, Ruvolo G, Romano R 2000 Nitric oxide synthase inhibition in human sperm affects sperm-oocyte fusion but not zona pellucida binding. Biol Reprod 63:425-429
41. Kim BH, Kim CH, Jung KY, Jeon BH, Ju EJ, Choo YK 2004 Involvement of nitric oxide during in vitro fertilization and early embryonic development in mice. Arch Pharm Res 27:86-93
42. Tranguch S, Steuerwald N, Huet-Hudson YM 2003 Nitric oxide synthase production and nitric oxide regulation of preimplantation embryo development. Biol Reprod 68:1538-1544
43. Chen HW, Jiang WS, Tzeng CR 2001 Nitric oxide as a regulator in preimplantation embryo development and apoptosis. Fertil Steril 75:1163-1171
44. Perez Martinez S, Franchi AM, Viggiano JM, Herrero MB, Gimeno M 1998 Effect of prostaglandin F2 α (PGF2α) on oviductal nitric oxide synthase (NOS) activity: possible role of endogenous NO on PGF2α-induced contractions in rat oviduct. Prostaglandins Other Lipid Mediat 56:155-166
45. Rosselli M, Imthurn B, Macas E, Keller PJ, Dubey RK 1994 Endogenous nitric oxide modulates endothelin-1 induced contraction of bovine oviduct. Biochem Biophys Res Commun 201:143-148
46. Ekerhovd E, Brannstrom M, Weijdegard B, Norstrom A 1999 Localization of nitric oxide synthase and effects of nitric oxide donors on the human Fallopian tube. Mol Hum Reprod 5:1040-1047
47. Francis M, Arkle M, Martin L, Butler TM, Cruz MC, Opare-Aryee G, Dacke CG, Brown JF 2003 Relaxant effects of parathyroid hormone and parathyroid hormone-related peptides on oviduct motility in birds and mammals: possible role of nitric oxide. Gen Comp Endocrinol 133:243-251
48. Perez Martinez S, Viggiano M, Franchi AM, Herrero MB, Ortiz ME, Gimeno MF, Villalon M 2000 Effect of nitric oxide synthase inhibitors on ovum transport and oviductal smooth muscle activity in the rat oviduct. J Reprod Fertil 118:111-117
49. Gawronska B, Bodek G, Ziecik AJ 2000 Distribution of NADPH-diaphorase and nitric oxide synthase (NOS) in different regions of porcine oviduct during the estrous cycle. J Histochem Cytochem 48:867-875
50. Majewski M, Sienkiewicz W, Kaleczyc J, Mayer B, Czaja K, Lakomy M 1995 The distribution and co-localization of immunoreactivity to nitric oxide synthase, vasoactive intestinal polypeptide and substance P within nerve fibres supplying bovine and porcine female genital organs. Cell Tissue Res 281:445-464
51. Rosselli M, Dubey RK, Rosselli MA, Macas E, Fink D, Lauper U, Keller PJ, Imthurn B 1996 Identification of nitric oxide synthase in human and bovine oviduct. Mol Hum Reprod 2:607-612
52. Arosh JA, Parent J, Chapdelaine P, Sirois J, Fortier MA 2002 Expression of cyclooxygenases 1 and 2 and prostaglandin e synthase in bovine endometrial tissue during the estrous cycle. Biol Reprod 67:161-169
53. Kimmins S, Russell GL, Lim HC, Hall BK, MacLaren LA 2003 The effects of estrogen, its antagonist ICI 182, 780, and interferon-τ -on the expression of estrogen receptors and integrin αVβ3 on cycle day 16 in bovine endometrium. Reprod Biol Endocrinol 1:38
54. Bérubé R, Malenfant J, Gauvin D, Blais M, Gagnon E, Dumas R, Racine MC, Bourque J, Bélanger A Quantitation of androgenic and estrogenic steroids in rat and monkey serum using gas chromatography and negative chemical ionization mass spectrometry. Proc 48th ASMS Conference on Mass Spectrometry and Allied Topics, Long Beach, CA, June 2000, p 605 (Abstract)
55. Lapointe J, Kimmins S, Maclaren LA, Bilodeau JF 2005 Estrogen selectively up-regulates the phospholipid hydroperoxide glutathione peroxidase (PHGPx) in the oviducts. Endocrinology 146:2583-2592
56. Lapointe J, Bilodeau JF 2003 Antioxidant defenses are modulated in the cow oviduct during the estrous cycle. Biol Reprod 68:1157-1164
57. Kang J, Chapdelaine P, Parent J, Madore E, Laberge PY, Fortier MA 2005 Expression of human prostaglandin transporter in the human endometrium across the menstrual cycle. J Clin Endocrinol Metab 90:2308-2313
58. Emond V, MacLaren LA, Kimmins S, Arosh JA, Fortier MA, Lambert RD 2004 Expression of cyclooxygenase-2 and granulocyte-macrophage colony-stimulating factor in the endometrial epithelium of the cow is up-regulated during early pregnancy and in response to intrauterine infusions of interferon-tau. Biol Reprod 70:54-64
59. Jablonka-Shariff A, Olson LM 2000 Nitric oxide is essential for optimal meiotic maturation of murine cumulus-oocyte complexes in vitro. Mol Reprod Dev 55:412-421
60. Burnett TG, Tash JS, Hunt JS 2002 Investigation of the role of nitric oxide synthase 2 in pregnancy using mutant mice. Reproduction 124:49-57
61. Buhi WC 2002 Characterization and biological roles of oviduct-specific, oestrogen-dependent glycoprotein. Reproduction 123:355-362
62. Robb GB, Carson AR, Tai SC, Fish JE, Singh S, Yamada T, Scherer SW, Nakabayashi K, Marsden PA 2004 Post-transcriptional regulation of endothelial nitric-oxide synthase by an overlapping antisense mRNA transcript. J Biol Chem 279:37982-37996
63. Chesler DA, McCutcheon JA, Reiss CS 2004 Posttranscriptional regulation of neuronal nitric oxide synthase expression by IFN-γ. J Interferon Cytokine Res 24:141-149
64. Eliasson MJ, Blackshaw S, Schell MJ, Snyder SH 1997 Neuronal nitric oxide synthase alternatively spliced forms: prominent functional localizations in the brain. Proc Natl Acad Sci USA 94:3396-3401
65. Leese HJ, Tay JI, Reischl J, Downing SJ 2001 Formation of Fallopian tubal fluid: role of a neglected epithelium. Reproduction 121:339-346
66. Bellve AR, McDonald MF 1970 Directional flow of fallopian tube secretion in the ewe at onset of the breeding season. J Reprod Fertil 22:147-149
67. Black DL, Davis J 1962 A blocking mechanism in the cow oviduct. J Reprod Fertil 4:21-26
68. Perez Martinez S, Farina M, Ogando D, Ribeiro ML, Gimeno M, Franchi AM 2000 Nitric oxide inhibits prostanoid synthesis in the rat oviduct. Prostaglandins Leukot Essent Fatty Acids 62:239-242
69. Brundin J 1965 Distribution and function of adrenergic nerves in the rabbit fallopian tube. Acta Physiol Scand Suppl 259:1-57
70. Suarez SS 2002 Formation of a reservoir of sperm in the oviduct. Reprod Domest Anim 37:140-143
71. Weinberg JB, Doty E, Bonaventura J, Haney AF 1995 Nitric oxide inhibition of human sperm motility. Fertil Steril 64:408-413
72. Herrero MB, Cebral E, Boquet M, Viggiano JM, Vitullo A, Gimeno MA 1994 Effect of nitric oxide on mouse sperm hyperactivation. Acta Physiol Pharmacol Ther Latinoam 44:65-69
73. O'Flaherty C, Rodriguez P, Srivastava S 2004 L-Arginine promotes capacitation and acrosome reaction in cryopreserved bovine spermatozoa. Biochim Biophys Acta 1674:215-221
74. Yaniz JL, Lopez-Gatius F, Santolaria P, Mullins KJ 2000 Study of the functional anatomy of bovine oviductal mucosa. Anat Rec 260:268-278
75. Blandau RJ 1978 Comparative aspects of tubal anatomy and physiology as they relate to reconstructive procedures. J Reprod Med 21:7-15
76. Li D, Shirakami G, Zhan X, Johns RA 2000 Regulation of ciliary beat frequency by the nitric oxide-cyclic guanosine monophosphate signaling pathway in rat airway epithelial cells. Am J Respir Cell Mol Biol 23:175-181
77. Kim JW, Min YG, Rhee CS, Lee CH, Koh YY, Rhyoo C, Kwon TY, Park SW 2001 Regulation of mucociliary motility by nitric oxide and expression of nitric oxide synthase in the human sinus epithelial cells. Laryngoscope 111:246-250
78. Ogando D, Farina M, Ribeiro ML, Perez Martinez S, Cella M, Rettori V, Franchi A 2003 Steroid hormones augment nitric oxide synthase activity and expression in rat uterus. Reprod Fertil Dev 15:269-274
79. Al-Khlaiwi T, Al-Drees A, Gursoy E, Qureshi I, Biber T, Kalimi M 2005 Estrogen protects cardiac myogenic (H9c2) rat cells against lethal heat shock-induced cell injury: modulation of estrogen receptor α, glucocorticoid receptors, heat shock protein 70, and iNOS. J Cardiovasc Pharmacol 45:217-224
80. You HJ, Kim JY, Jeong HG 2003 17β-estradiol increases inducible nitric oxide synthase expression in macrophages. Biochem Biophys Res Commun 303:1129-1134
81. Liang M, Ekblad E, Lydrup ML, Nilsson BO 2003 Combined lack of estrogen receptors α and α affects vascular iNOS protein expression. Cell Tissue Res 313:63-70
82. Nuedling S, Karas RH, Mendelsohn ME, Katzenellenbogen JA, Katzenellenbogen BS, Meyer R, Vetter H, Grohe C 2001 Activation of estrogen receptor β is a prerequisite for estrogen-dependent upregulation of nitric oxide synthases in neonatal rat cardiac myocytes. FEBS Lett 502:103-108
83. Ulbrich SE, Kettler A, Einspanier R 2003 Expression and localization of estrogen receptor α, estrogen receptor β and progesterone receptor in the bovine oviduct in vivo and in vitro. J Steroid Biochem Mol Biol 84:279-289
84. Miyamoto Y, Koh YH, Park YS, Fujiwara N, Sakiyama H, Misonou Y, Ookawara T, Suzuki K, Honke K, Taniguchi N 2003 Oxidative stress caused by inactivation of glutathione peroxidase and adaptive responses. Biol Chem 384:567-574
85. Orihuela PA, Parada-Bustamante A, Cortes PP, Gatica C, Croxatto HB 2003 Estrogen receptor, cyclic adenosine monophosphate, and protein kinase A are involved in the nongenomic pathway by which estradiol accelerates oviductal oocyte transport in cyclic rats. Biol Reprod 68:1225-1231
86. Humphrey KW, Martin L 1968 The effects of oestrogens and anti-oestrogens on ovum transport in the laboratory mouse. Aust J Biol Sci 21:1239-1248
87. Bareither ML, Verhage HG 1981 Control of the secretory cell cycle in cat oviduct by estradiol and progesterone. Am J Anat 162:107-118