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Reproductive Biology and Endocrinology
Published in: Reproductive Biology and Endocrinology 1/2010

Open Access 01-12-2010 | Research

Cellular and molecular evidence for a role of tumor necrosis factor alpha in the ovulatory mechanism of trout

Authors: Diego Crespo, Emilie Bonnet, Nerea Roher, Simon A MacKenzie, Aleksei Krasnov, Frederick W Goetz, Julien Bobe, Josep V Planas

Published in: Reproductive Biology and Endocrinology | Issue 1/2010

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Abstract

Background

The relevance of immune-endocrine interactions to the regulation of ovarian function in teleosts is virtually unexplored. As part of the innate immune response during infection, a number of cytokines such as tumor necrosis factor alpha (TNF alpha) and other immune factors, are produced and act on the reproductive system. However, TNF alpha is also an important physiological player in the ovulatory process in mammals. In the present study, we have examined for the first time the effects of TNF alpha in vitro in preovulatory ovarian follicles of a teleost fish, the brown trout (Salmo trutta).

Methods

To determine the in vivo regulation of TNF alpha expression in the ovary, preovulatory brook trout (Salvelinus fontinalis) were injected intraperitoneally with either saline or bacterial lipopolysaccharide (LPS). In control and recombinant trout TNF alpha (rtTNF alpha)-treated brown trout granulosa cells, we examined the percentage of apoptosis by flow cytometry analysis and cell viability by propidium iodide (PI) staining. Furthermore, we determined the in vitro effects of rtTNF alpha on follicle contraction and testosterone production in preovulatory brown trout ovarian follicles. In addition, we analyzed the gene expression profiles of control and rtTNF alpha-treated ovarian tissue by microarray and real-time PCR (qPCR) analyses.

Results

LPS administration in vivo causes a significant induction of the ovarian expression of TNF alpha. Treatment with rtTNF alpha induces granulosa cell apoptosis, decreases granulosa cell viability and stimulates the expression of genes known to be involved in the normal ovulatory process in trout. In addition, rtTNF alpha causes a significant increase in follicle contraction and testosterone production. Also, using a salmonid-specific microarray platform (SFA2.0 immunochip) we observed that rtTNF alpha induces the expression of genes known to be involved in inflammation, proteolysis and tissue remodeling. Furthermore, the expression of kallikrein, TOP-2, serine protease 23 and ADAM 22, genes that have been postulated to be involved in proteolytic and tissue remodeling processes during ovulation in trout, increases in follicles incubated in the presence of rtTNF alpha.

Conclusions

In view of these results, we propose that TNF alpha could have an important role in the biomechanics of follicle weakening, ovarian rupture and oocyte expulsion during ovulation in trout, primarily through its stimulation of follicular cell apoptosis and the expression of genes involved in follicle wall proteolysis and contraction.
Appendix
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Literature
1.
Currie JL, Woo PTK: Effects of the pathogenic haemoflagellate, Cryptobia salmositica on brood fish, Oncorhynchus mykiss. Environ Biol Fish. 2008, 83 (3): 355-365. 10.1007/s10641-008-9350-x.CrossRef
2.
Schreck CB, Contreras-Sanchez W, Fitzpatrick MS: Effects of stress on fish reproduction, gamete quality, and progeny. Aquaculture. 2001, 197 (1-4): 3-24. 10.1016/S0044-8486(01)00580-4.CrossRef
3.
Goetz FW, Iliev DB, McCauley LA, Liarte CQ, Tort LB, Planas JV, MacKenzie S: Analysis of genes isolated from lipopolysaccharide-stimulated rainbow trout (Oncorhynchus mykiss) macrophages. Mol Immunol. 2004, 41 (12): 1199-1210. 10.1016/j.molimm.2004.06.005.CrossRefPubMed
4.
MacKenzie S, Planas JV, Goetz FW: LPS-stimulated expression of a tumor necrosis factor-alpha mRNA in primary trout monocytes and in vitro differentiated macrophages. Dev Comp Immunol. 2003, 27 (5): 393-400. 10.1016/S0145-305X(02)00135-0.CrossRefPubMed
5.
Calleja-Agius J, Muttukrishna S, Jauniaux E: Role of TNF-α in human female reproduction. Expert Rev Endocrinol Metab. 2009, 4: 273-282. 10.1586/eem.09.4.CrossRef
6.
Amsterdam A, Keren-Tal I, Aharoni D, Dantes A, Land-Bracha A, Rimon E, Sasson R, Hirsh L: Steroidogenesis and apoptosis in the mammalian ovary. Steroids. 2003, 68 (10-13): 861-867. 10.1016/j.steroids.2003.09.003.CrossRefPubMed
7.
Roby KF, Terranova PF: Effects of tumor necrosis factor-alpha in vitro on steroidogenesis of healthy and atretic follicles of the rat: theca as a target. Endocrinology. 1990, 126 (5): 2711-2718. 10.1210/endo-126-5-2711.CrossRefPubMed
8.
Murdoch WJ, Colgin DC, Ellis JA: Role of tumor necrosis factor-alpha in the ovulatory mechanism of ewes. J Anim Science. 1997, 75 (6): 1601-1605.
9.
Murdoch WJ, Lund SA: Prostaglandin-independent anovulatory mechanism of indomethacin action: inhibition of tumor necrosis factor alpha-induced sheep ovarian cell apoptosis. Biol Reprod. 1999, 61 (6): 1655-1659. 10.1095/biolreprod61.6.1655.CrossRefPubMed
10.
MacKenzie S, Montserrat N, Mas M, Acerete L, Tort L, Krasnov A, Goetz FW, Planas JV: Bacterial lipopolysaccharide induces apoptosis in the trout ovary. Reprod Biol Endocrinol. 2006, 4: 46-10.1186/1477-7827-4-46.PubMedCentralCrossRefPubMed
11.
Goetz FW, Bergman HL: The effects of steroids on final maturation and ovulation of oocytes from brook trout (Salvelinus fontinalis) and yellow perch (Perca flavescens). Biol Reprod. 1978, 18 (2): 293-298. 10.1095/biolreprod18.2.293.CrossRefPubMed
12.
Swanson P, Suzuki K, Kawauchi H, Dickhoff WW: Isolation and characterization of two coho salmon gonadotropins, GTH I and GTH II. Biol Reprod. 1991, 44 (1): 29-38. 10.1095/biolreprod44.1.29.CrossRefPubMed
13.
Roher N, Callol A, Planas JV, Goetz FW, MacKenzie SA: Endotoxin recognition in fish results in inflammatory cytokine secretion not gene expression. Innate Immun. 2010, 10.1177/1753425909348232.
14.
Planas JV, Goetz FW, Swanson P: Stimulation of brook trout ovarian steroidogenesis by gonadotropins I and II is mediated by the cyclic adenosine 3',5'-monophosphate/protein kinase A pathway. Biol Reprod. 1997, 57 (3): 647-654. 10.1095/biolreprod57.3.647.CrossRefPubMed
15.
Goetz FW, Bradley JA: Stimulation of in vitro ovulation and contraction of brook trout (Salvelinus fontinalis) follicles by adrenaline through alpha-adrenoreceptors. J Reprod Fertil. 1994, 100 (2): 381-385.CrossRefPubMed
16.
Hsu SY, Goetz FW: The effects of E and F prostaglandins on ovarian cAMP production and follicular contraction in the brook trout (Salvelinus fontinalis). Gen Comp Endocrinol. 1992, 88 (3): 434-443. 10.1016/0016-6480(92)90238-F.CrossRefPubMed
17.
Méndez E, Mæland M, Skålhegg BS, Planas JV: Activation of the cAMP-dependent protein kinase signaling pathway by luteinizing hormone in trout theca layers. Mol Cell Endocrinol. 2003, 205 (1-2): 11-20. 10.1016/S0303-7207(03)00208-9.CrossRefPubMed
18.
Montserrat N, González A, Méndez E, Piferrer F, Planas JV: Effects of follicle stimulating hormone on estradiol-17[beta] production and P-450 aromatase (CYP19) activity and mRNA expression in brown trout vitellogenic ovarian follicles in vitro. Gen Comp Endocrinol. 2004, 137 (2): 123-131. 10.1016/j.ygcen.2004.02.011.CrossRefPubMed
19.
Koskinen H, Pehkonen P, Vehniäinen E, Krasnov A, Rexroad C, Afanasyev S, Mölsa H, Oikari A: Response of rainbow trout transcriptome to model chemical contaminants. Biochem Biophys Res Commun. 2004, 320 (3): 745-753. 10.1016/j.bbrc.2004.06.024.CrossRefPubMed
20.
Krasnov A, Koskinen H, Pehkonen P, Rexroad CE, Afanasyev S, Molsa H: Gene expression in the brain and kidney of rainbow trout in response to handling stress. BMC Genomics. 2005, 6 (1): 3-10.1186/1471-2164-6-3.PubMedCentralCrossRefPubMed
21.
Ashburner M, Ball CA, Blake JA, Botstein D, Butler H, Cherry JM, Davis AP, Dolinski K, Dwight SS, Eppig JT, Harris MA, Hill DP, Issel-Tarver L, Kasarskis A, Lewis S, Matese JC, Richardson JE, Ringwald M, Rubin GM, Sherlock G: Gene ontology: tool for the unification of biology. The Gene Ontology Consortium. Nat Genet. 2000, 25 (1): 25-29. 10.1038/75556.PubMedCentralCrossRefPubMed
22.
Livak KJ, Schmittgen TD: Analysis of Relative Gene Expression Data Using Real-Time Quantitative PCR and the 2(-Delta DeltaC(T)) Method. Methods. 2001, 25 (4): 402-408. 10.1006/meth.2001.1262.CrossRefPubMed
23.
MacKenzie S, Balasch JC, Novoa B, Ribas L, Roher N, Krasnov A, Figueras A: Comparative analysis of the acute response of the trout, O. mykiss, head kidney to in vivo challenge with virulent and attenuated infectious hematopoietic necrosis virus and LPS-induced inflammation. BMC Genomics. 2008, 9: 141-10.1186/1471-2164-9-141.PubMedCentralCrossRefPubMed
24.
MacKenzie S, Iliev D, Liarte C, Koskinen H, Planas JV, Goetz FW, Molsa H, Krasnov A, Tort L: Transcriptional analysis of LPS-stimulated activation of trout (Oncorhynchus mykiss) monocyte/macrophage cells in primary culture treated with cortisol. Mol Immunol. 2006, 43 (9): 1340-1348. 10.1016/j.molimm.2005.09.005.CrossRefPubMed
25.
Djordjevic B, Skugor S, Jorgensen SM, Overland M, Mydland LT, Krasnov A: Modulation of splenic immune responses to bacterial lipopolysaccharide in rainbow trout (Oncorhynchus mykiss) fed lentinan, a beta-glucan from mushroom Lentinula edodes. Fish Shellfish Immunol. 2009, 26 (2): 201-209. 10.1016/j.fsi.2008.10.012.CrossRefPubMed
26.
Mahajan KN, Mitchell BS: Role of human Pso4 in mammalian DNA repair and association with terminal deoxynucleotidyl transferase. Proc Natl Acad Sci. 2003, 100 (19): 10746-10751. 10.1073/pnas.1631060100.PubMedCentralCrossRefPubMed
27.
Massard C, Zermati Y, Pauleau AL, Larochette N, Metivier D, Sabatier L, Kroemer G, Soria JC: hTERT: a novel endogenous inhibitor of the mitochondrial cell death pathway. Oncogene. 2006, 25 (33): 4505-4514. 10.1038/sj.onc.1209487.CrossRefPubMed
28.
Bobe J, Goetz FW: A novel osteopontin-like protein is expressed in the trout ovary during ovulation. FEBS Lett. 2001, 489 (2-3): 119-124. 10.1016/S0014-5793(01)02090-7.CrossRefPubMed
29.
Garczynski MA, Goetz FW: Molecular characterization of a ribonucleic acid transcript that is highly up-regulated at the time of ovulation in the brook trout (Salvelinus fontinalis) ovary. Biol Reprod. 1997, 57 (4): 856-864. 10.1095/biolreprod57.4.856.CrossRefPubMed
30.
Hajnik CA, Goetz FW, Hsu SY, Sokal N: Characterization of a ribonucleic acid transcript from the brook trout (Salvelinus fontinalis) ovary with structural similarities to mammalian adipsin/complement factor D and tissue kallikrein, and the effects of kallikrein-like serine proteases on follicle contraction. Biol Reprod. 1998, 58 (4): 887-897. 10.1095/biolreprod58.4.887.CrossRefPubMed
31.
Wada S, Kudo T, Kudo M, Sakuragi N, Hareyama H, Nishihira J, Fujimoto S: Induction of macrophage migration inhibitory factor in human ovary by human chorionic gonadotrophin. Hum Reprod. 1999, 14 (2): 395-399. 10.1093/humrep/14.2.395.CrossRefPubMed
32.
Bobe J, Goetz FW: A tumor necrosis factor decoy receptor homologue is up-regulated in the brook trout (Salvelinus fontinalis) ovary at the completion of ovulation. Biol Reprod. 2000, 62 (2): 420-426. 10.1095/biolreprod62.2.420.CrossRefPubMed
33.
Murdoch WJ, Van Kirk EA, Murdoch J: Plasmin cleaves tumor necrosis factor alpha exodomain from sheep follicular endothelium: implication in the ovulatory process. Biol Reprod. 1999, 60 (5): 1166-1171. 10.1095/biolreprod60.5.1166.CrossRefPubMed
34.
Terranova PF: Potential roles of tumor necrosis factor-alpha in follicular development, ovulation, and the life span of the corpus luteum. Domest Anim Endocrinol. 1997, 14 (1): 1-15. 10.1016/S0739-7240(96)00094-X.CrossRefPubMed
35.
Loret de Mola JR, Goldfarb JM, Hecht BR, Baumgardner GP, Babbo CJ, Friedlander MA: Gonadotropins induce the release of interleukin-1 beta, interleukin-6 and tumor necrosis factor-alpha from the human preovulatory follicle. Am J Reprod Immunol. 1998, 39 (6): 387-390.CrossRefPubMed
36.
Zolti M, Meirom R, Shemesh M, Wollach D, Mashiach S, Shore L, Rafael ZB: Granulosa cells as a source and target organ for tumor necrosis factor-alpha. FEBS Lett. 1990, 261 (2): 253-255. 10.1016/0014-5793(90)80565-Z.CrossRefPubMed
37.
38.
Terranova PF, Rice VM: Review: cytokine involvement in ovarian processes. Am J Reprod Immunol. 1997, 37 (1): 50-63.CrossRefPubMed
39.
Wang HG, Takayama S, Rapp UR, Reed JC: Bcl-2 interacting protein, BAG-1, binds to and activates the kinase Raf-1. Proc Natl Acad Sci. 1996, 93 (14): 7063-7068. 10.1073/pnas.93.14.7063.PubMedCentralCrossRefPubMed
40.
Flaws JA, Hirshfield AN, Hewitt JA, Babus JK, Furth PA: Effect of bcl-2 on the primordial follicle endowment in the mouse ovary. Biol Reprod. 2001, 64 (4): 1153-1159. 10.1095/biolreprod64.4.1153.CrossRefPubMed
41.
Pham CG, Bubici C, Zazzeroni F, Papa S, Jones J, Alvarez K, Jayawardena S, De Smaele E, Cong R, Beaumont C, Torti FM, Torti SV, Franzoso G: Ferritin heavy chain upregulation by NF-kappaB inhibits TNFalpha-induced apoptosis by suppressing reactive oxygen species. Cell. 2004, 119 (4): 529-542. 10.1016/j.cell.2004.10.017.CrossRefPubMed
42.
Curry TE, Smith MF: Impact of extracellular matrix remodeling on ovulation and the folliculo-luteal transition. Semin Reprod Med. 2006, 24 (4): 228-241. 10.1055/s-2006-948552.CrossRefPubMed
43.
Berndtson AK, Goetz FW: Protease activity in brook trout (Salvelinus fontinalis) follicle walls demonstrated by substrate-polyacrylamide gel electrophoresis. Biol Reprod. 1988, 38 (2): 511-516. 10.1095/biolreprod38.2.511.CrossRefPubMed
44.
Berndtson AK, Goetz FW: Metallo-protease activity increases prior to ovulation in brook trout (Salvelinus fontinalis) and yellow perch (Perca flavescens) follicle walls. Biol Reprod. 1990, 42 (2): 391-398. 10.1095/biolreprod42.2.391.CrossRefPubMed
45.
Coffman MA, Pinter JH, Goetz FW: Trout ovulatory proteins: site of synthesis, regulation, and possible biological function. Biol Reprod. 2000, 62 (4): 928-938. 10.1095/biolreprod62.4.928.CrossRefPubMed
46.
Bobe J, Montfort J, Nguyen T, Fostier A: Identification of new participants in the rainbow trout (Oncorhynchus mykiss) oocyte maturation and ovulation processes using cDNA microarrays. Reprod Biol Endocrinol. 2006, 4: 39-10.1186/1477-7827-4-39.PubMedCentralCrossRefPubMed
47.
Ogiwara K, Takano N, Shinohara M, Murakami M, Takahashi T: Gelatinase A and membrane-type matrix metalloproteinases 1 and 2 are responsible for follicle rupture during ovulation in the medaka. Proc Natl Acad Sci. 2005, 102 (24): 8442-8447. 10.1073/pnas.0502423102.PubMedCentralCrossRefPubMed
48.
Carnevali O, Cionna C, Tosti L, Lubzens E, Maradonna F: Role of cathepsins in ovarian follicle growth and maturation. Gen Comp Endocrinol. 2006, 146 (3): 195-203. 10.1016/j.ygcen.2005.12.007.CrossRefPubMed
49.
Walters KA, Allan CM, Handelsman DJ: Androgen actions and the ovary. Biol Reprod. 2008, 78 (3): 380-389. 10.1095/biolreprod.107.064089.CrossRefPubMed
50.
Fitzpatrick MS, Kraak Van der G, Schreck CB: Profiles of plasma sex steroids and gonadotropin in coho salmon, Oncorhynchus kisutch, during final maturation. Gen Comp Endocrinol. 1986, 62 (3): 437-451. 10.1016/0016-6480(86)90054-7.CrossRefPubMed
51.
Crespo D, Planas JV, Bobe J: Lipopolysaccharide administration in preovulatory rainbow trout (Oncorhynchus mykiss) reduces egg quality. Aquaculture. 2010, 300 (1-4): 240-242.CrossRef
52.
Bobe J, Goetz FW: Molecular cloning and expression of a TNF receptor and two TNF ligands in the fish ovary. Comp Biochem Physiol. 2001, 129 (2-3): 475-481. 10.1016/S1096-4959(01)00353-0.CrossRef
Metadata
Title
Cellular and molecular evidence for a role of tumor necrosis factor alpha in the ovulatory mechanism of trout
Authors
Diego Crespo
Emilie Bonnet
Nerea Roher
Simon A MacKenzie
Aleksei Krasnov
Frederick W Goetz
Julien Bobe
Josep V Planas
Publication date
01-12-2010
Publisher
BioMed Central
Published in
Reproductive Biology and Endocrinology / Issue 1/2010
Electronic ISSN: 1477-7827
DOI
https://doi.org/10.1186/1477-7827-8-34

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