Transcriptional signature of progesterone in the fathead minnow ovary (Pimephales promelas)

General and Comparative Endocrinology

Volumn 192, Issue , 2013, Pages 159-169

  Garcia Reyero, Natàlia ^a   Martyniuk, Christopher J ^b   Kroll, Kevin J ^c   Escalon, B Lynn ^d   Spade, Daniel J ^c,e   Denslow, Nancy D ^c  

^a MISSISSIPPI STATE UNIVERSITY   (United States)

^b UNIVERSITY OF NEW BRUNSWICK   (Canada)

^c UNIVERSITY OF FLORIDA   (United States)

^d U S ARMY ENGINEER RESEARCH AND DEVELOPMENT CENTER   (United States)

^e BROWN UNIVERSITY   (United States)

Author keywords

Calcium signaling; Germinal vesicle breakdown; Microarrays; Progestins; Ribosomes

Indexed keywords

ADENOSINE TRIPHOSPHATE; CALCIUM CHANNEL; INSULIN; PROGESTERONE; PROTEIN P53; PROTEIN SERINE THREONINE KINASE; SONIC HEDGEHOG PROTEIN; TRANSCRIPTION FACTOR E2F1;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; B LYMPHOCYTE ACTIVATION; CALCIUM SIGNALING; CELL CYCLE REGULATION; CELL MIGRATION; CONTROLLED STUDY; ENZYME ACTIVITY; FEMALE; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENE IDENTIFICATION; GERMINAL VESICLE; HORMONE ACTION; IN VITRO STUDY; LONG TERM EXPOSURE; MICROARRAY ANALYSIS; NONHUMAN; NUCLEOTIDE SEQUENCE; OVARY DEVELOPMENT; PIMEPHALES PROMELAS; PRIORITY JOURNAL; PROTEIN BINDING; RIBOSOME; TRANSCRIPTION REGULATION;

CALCIUM SIGNALING; GERMINAL VESICLE BREAKDOWN; MICROARRAYS; PROGESTINS; RIBOSOMES;

ANIMALS; CALCIUM SIGNALING; CYPRINIDAE; FEMALE; GENE EXPRESSION PROFILING; OVARY; PROGESTERONE; PROGESTINS; RIBOSOMES;

EID: 84884415684     PISSN: 00166480     EISSN: 10956840     Source Type: Journal    
DOI: 10.1016/j.ygcen.2013.06.008     Document Type: Article

References (64)

1. Azhar S., Menon K.M. Receptor-mediated gonadotropin action in the ovary. Regulatory role of cyclic nucleotide phosphodiesterase(s) in intracellular adenosine 3':5'-cyclic monophosphate turnover and gonadotropin-stimulated progesterone production by rat ovarian cells. Biochem. J. 1979, 180(1):201-211.
2. Babin P.J., Cerdà J., Lubzens E. The Fish Oocyte: from Basic Studies to Biotechnological Applications 2007, Springer-Verlag, Dordrecht, pp. 508.
3. Benjamini Y., Hochberg Y. Controlling the false discovery rate: a practical and powerful approach to multiple testing. Journal of the Royal Statistical Society Series B 1995, 57(1):287-300.
4. Bobe J., Nguyen T., Fostier A. Ovarian function of the trout preovulatory ovary: new insights from recent gene expression studies. Comp. Biochem. Physiol. A: Mol. Integr. Physiol. 2009, 153:63-68.
5. Calvano S.E., Xiao W., Richards D.R., Felciano R.M., Baker H.V., Cho R.J., Chen R.O., Brownstein B.H., Cobb J.P., Tschoeke S.K., Miller-Graziano C., Moldawer L.L., Mindrinos M.N., Davis R.W., Tompkins R.G., Lowry S.F., Inflamm and Host Response to Injury Large Scale Collab.Res.Program A network-based analysis of systemic inflammation in humans. Nature 2005, 437:1032-1037.
6. Campbell M., Kiang A.-S., Kenna P.F., Kerskens C., Blau C., O'Dwyer L., Tivnan A., Kelly J.A., Brankin B., Farrar G.-J., Humphries P. RNAi-mediated reversible opening of the blood-brain barrier. J. Gene Med. 2008, 10:930-947.
7. Chen S.X., Bogerd J., García-López A., de Jonge H., de Waal P.P., Hong W.S., Schulz R.W. Molecular cloning and functional characterization of a zebrafish nuclear progesterone receptor. Biol. Reprod. 2010, 82:171-181.
8. Clelland E.S., Kelly S.P. Tight junction proteins in zebrafish ovarian follicles: stage specific mRNA abundance and response to 17beta-estradiol, human chorionic gonadotropin, and maturation inducing hormone. Gen. Comp. Endocrinol. 2010, 168:388-400.
9. Das S., Thomas P. Pesticides interfere with the nongenomic action of a progestogen on meiotic maturation by binding to its plasma membrane receptor on fish oocytes. Endocrinology 1999, 140:1953-1956.
10. Eichenlaub-Ritter U., Peschke M. Expression in in-vivo and in-vitro growing and maturing oocytes: focus on regulation of expression at the translational level. Hum. Reprod. Update 2002, 8:21-41.
11. Filby A.L. Molecular characterization of estrogen receptors 1, 2a, and 2b and their tissue and ontogenic expression profiles in fathead minnow (Pimephales promelas). Biol. Reprod. 2005, 73:648-662.
12. Franczak A., Kurowicka B., Kowalik M., Ciereszko R.E., Kotwica G. The effect of oxytocin on progesterone secretion, phosphoinositide hydrolysis and intracellular mobilisation of Ca2+ in porcine luteal cells. Acta Vet. Hung. 2009, 57(1):115-125.
13. Garcia-Reyero N., Villeneuve D.L., Kroll K.J., Liu L., Orlando E.F., Watanabe K.H., Sepulveda M.S., Ankley G.T., Denslow N.D. Expression signatures for a model androgen and antiandrogen in the fathead minnow (Pimephales promelas) ovary. Environ. Sci. Technol. 2009, 43:2614-2619.
14. Greeley Jr M.S., Calder D.R., Taylor M.H., Hols H., Wallace R.A. Oocyte maturation in the mummichog (Fundulus heteroclitus): effects of steroids on germinal vesicle breakdown of intact follicles in vitro. Gen. Comp. Endocrinol. 1986, 62(2):281-289.
15. Gupta I.R., Ryan A.K. Claudins: unlocking the code to tight junction function during embryogenesis and in disease. Clin. Genet. 2010, 77:314-325.
16. Hanna R.N., Daly S.C.J., Pang Y., Anglade I., Kah O., Thomas P., Zhu Y. Characterization and expression of the nuclear progestin receptor in zebrafish gonads and brain. Biol. Reprod. 2010, 82:112-122.
17. Heyer B.S., Kochanowski H., Solter D. Expression of Melk, a new protein kinase, during early mouse development. Dev. Dyn. 1999, 215:344-351.
18. Hoshino Y., Yokoo M., Yoshida N., Sasada H., Matsumoto H., Sato E. Phosphatidylinositol 3-kinase and Akt participate in the FSH-induced meiotic maturation of mouse oocytes. Mol. Reprod. Dev. 2004, 69:77-86.
19. Hsieh M., Thao K., Conti M. Genetic dissection of epidermal growth factor receptor signaling during luteinizing hormone-induced oocyte maturation. PLoS ONE 2011, 6:e21574.
20. Kagawa H., Takano K., Nagahama Y. Correlation of plasma estradiol-17 beta and progesterone levels with ultrastructure and histochemistry of ovarian follicles in the white-spotted char, Salvelinus leucomaenis. Cell Tissue Res. 1981, 218:315-329.
21. Kagawa H., Kobayashi M., Hasegawa Y., Aida K. Insulin and insulin-like growth factors I and II induce final maturation of oocytes of red seabream, Pagrus major, in vitro. Gen. Comp. Endocrinol. 1994, 95:293-300.
22. Kalous J., Kubelka M., Solc P., Susor A., Motlík J. AKT (protein kinase B) is implicated in meiotic maturation of porcine oocytes. Reproduction 2009, 138:645-654.
23. Kalous J., Solc P., Baran V., Kubelka M., Schultz R.M., Motlík J. PKB/AKT is involved in resumption of meiosis in mouse oocytes. Biol. Cell 2012, 98:111-123.
24. Kazeto Y., Goto-Kazeto R., Trant J.M. Membrane-bound progestin receptors in channel catfish and zebrafish ovary: changes in gene expression associated with the reproductive cycles and hormonal reagents. Gen. Comp. Endocrinol. 2005, 142:204-211.
25. Kollmar R., Nakamura S.K., Kappler J.A., Hudspeth A.J. Expression and phylogeny of claudins in vertebrate primordia. Proc. Natl. Acad. Sci. USA 2001, 98:10196-10201.
26. Lessman C.A. Oocyte maturation: converting the zebrafish oocyte to the fertilizable egg. Gen. Comp. Endocrinol. 2009, 161:53-57.
27. Li J., Li N., Ma M., Giesy J.P., Wang Z. In vitro profiling of the endocrine disrupting potency of organochlorine pesticides. Toxicol. Lett. 2008, 183:65-71.
28. Lo J., Lee S., Xu M., Liu F., Ruan H., Eun A., He Y., Ma W., Wang W., Wen Z., Peng J. 15000 unique zebrafish EST clusters and their future use in microarray for profiling gene expression patterns during embryogenesis. Genome Res. 2003, 13(3):455-466.
29. Lubzens E., Young G., Bobe J., Cerdà J. Oogenesis in teleosts: how fish eggs are formed. Gen. Comp. Endocrinol. 2010, 165:367-389.
30. Martyniuk C.J., Prucha M.S., Doperalski N.J., Antczak P., Kroll K.J., Falciani F., Barber D.S., Denslow N.D. Gene expression networks underlying ovarian development in wild largemouth bass (Micropterus salmoides). PLoS ONE 2013, 8:e59093.
31. Matsuoka Y., Kobayashi T., Kihara K., Nagahama Y. Molecular cloning of Plk1 and Nek2 and their expression in mature gonads of the teleost fish Nile tilapia (Oreochromis niloticus). Mol. Reprod. Dev. 2008, 75:989-1001.
32. Miura C., Higashino T., Miura T. A progestin and an estrogen regulate early stages of oogenesis in fish. Biol. Reprod. 2007, 77:822-828.
33. Mukherjee D., Mukherjee D., Sen U., Paul S., Bhattacharyya S.P. In vitro effects of insulin-like growth factors and insulin on oocyte maturation and maturation-inducing steroid production in ovarian follicles of common carp, Cyprinus carpio. Comp. Biochem. Physiol. A: Mol. Integr. Physiol. 2006, 144:63-77.
34. Nagahama Y. 17 alpha, 20 beta-dihydroxy-4-pregnen-3-one, a maturation-inducing hormone in fish oocytes: mechanisms of synthesis and action. Steroids 1997, 62:190-196.
35. Nagahama Y., Adachi S. Identification of maturation-inducing steroid in a teleost, the amago salmon (Oncorhynchus rhodurus). Developmental Biology 1985, 109(2):428-435.
36. Nagahama Y., Yamashita M. Regulation of oocyte maturation in fish. Dev. Growth Differ. 2008, 50:S195-S219.
37. Nakamura I., Evans J.C., Kusakabe M., Nagahama Y., Young G. Changes in steroidogenic enzyme and steroidogenic acute regulatory protein messenger RNAs in ovarian follicles during ovarian development of rainbow trout (Oncorhynchus mykiss). Gen. Comp. Endocrinol. 2005, 144:224-231.
38. Nakano I., Masterman-Smith M., Saigusa K., Paucar A.A., Horvath S., Shoemaker L., Watanabe M., Negro A., Bajpai R., Howes A., Lelievre V., Waschek J.A., Lazareff J.A., Freije W.A., Liau L.M., Gilbertson R.J., Cloughesy T.F., Geschwind D.H., Nelson S.F., Mischel P.S., Terskikh A.V., Kornblum H.I. Maternal embryonic leucine zipper kinase is a key regulator of the proliferation of malignant brain tumors, including brain tumor stem cells. J. Neurosci. Res. 2008, 86(1):48-60.
39. Nishimura R., Shibaya M., Skarzynski D.J., Okuda K. Progesterone stimulation by LH involves the phospholipase-C pathway in bovine luteal cells. J. Reprod. Dev. 2004, 50:257-261.
40. Ohta K., Yamaguchi S., Yamaguchi A., Gen K., Okuzawa K., Kagawa H., Matsuyama M. Biosynthesis of steroids in ovarian follicles of red seabream, Pagrus major (Sparidae, Teleostei) during final oocyte maturation and the relative effectiveness of steroid metabolites for germinal vesicle breakdown in vitro. Comp. Biochem. Physiol. Biochem. Mol. Biol. 2002, 133:45-54.
41. O'regan L., Blot J., Fry A.M. Mitotic regulation by NIMA-related kinases. Cell Div. 2007, 2:25.
42. Paulos P., Runnalls T.J., Nallani G., La Point T., Scott A.P., Sumpter J.P., Huggett D.B. Reproductive responses in fathead minnow and Japanese medaka following exposure to a synthetic progestin, Norethindrone. Aquat. Toxicol. 2010, 99:256-262.
43. Peluso J.J., Pappalardo A. Progesterone regulates granulosa cell viability through a protein kinase G-dependent mechanism that may involve 14-3-3sigma. Biol. Reprod. 2004, 71:1870-1878.
44. Rime H., Nguyen T., Bobe J., Fostier A., Monod G. Prochloraz-induced oocyte maturation in rainbow trout (Oncorhynchus mykiss), a molecular and functional analysis. Toxicol. Sci. 2010, 118:61-70.
45. Russell M.C., Cowan R.G., Harman R.M., Walker A.L., Quirk S.M. The hedgehog signaling pathway in the mouse ovary. Biol. Reprod. 2007, 77(2):226-236.
46. Schultz R.M. The molecular foundations of the maternal to zygotic transition in the preimplantation embryo. Hum. Reprod. Update 2002, 8:323-331.
47. Scippo M.-L., Argiris C., Van De Weerdt C., Muller M., Willemsen P., Martial J., Maghuin-Rogister G. Recombinant human estrogen, androgen and progesterone receptors for detection of potential endocrine disruptors. Anal. Bioanal. Chem. 2004, 378:664-669.
48. Senthilkumaran B., Yoshikuni M., Nagahama Y. A shift in steroidogenesis occurring in ovarian follicles prior to oocyte maturation. Mol. Cell. Endocrinol. 2004, 215:11-18.
49. Sorensen P.W., Murphy C.A., Loomis K., Maniak P., Thomas P. Evidence that 4-pregnen-17, 20β, 21-triol-3-one functions as a maturation-inducing hormone and pheromonal precursor in the percid fish, Gymnocephalus cernuus. Gen. Comp. Endocrinol. 2004, 139:1-11.
50. Spicer L.J., Sudo S., Aad P.Y., Wang L.S., Chun S.-Y., Ben-Shlomo I., Klein C., Hsueh A.J.W. The hedgehog-patched signaling pathway and function in the mammalian ovary: a novel role for hedgehog proteins in stimulating proliferation and steroidogenesis of theca cells. Reproduction 2009, 138:329-339.
51. Sreenivasulu G., Senthilkumaran B. A role for cytochrome P450 17alpha-hydroxylase/c17-20 lyase during shift in steroidogenesis occurring in ovarian follicles prior to oocyte maturation. J. Steroid Biochem. Mol. Biol. 2009, 115:77-85.
52. Tanaka M., Nakajin S., Kobayashi D., Fukada S., Guan G., Todo T., Senthilkumaran B., Nagahama Y. Teleost ovarian carbonyl reductase-like 20beta-hydroxysteroid dehydrogenase: potential role in the production of maturation-inducing hormone during final oocyte maturation. Biol. Reprod. 2002, 66:1498-1504.
53. Thélie A., Papillier P., Pennetier S., Perreau C., Traverso J.M., Uzbekova S., Mermillod P., Joly C., Humblot P., Dalbiès-Tran R. Differential regulation of abundance and deadenylation of maternal transcripts during bovine oocyte maturation in vitro and in vivo. BMC Dev. Biol. 2007, 7:125.
54. Thomas P. Rapid steroid hormone actions initiated at the cell surface and the receptors that mediate them with an emphasis on recent progress in fish models. Gen. Comp. Endocrinol. 2012, 175:367-383.
55. Tomek W. Activation of Akt (protein kinase B) stimulates metaphase I to metaphase II transition in bovine oocytes. Reproduction 2005, 130:423-430.
56. Tubbs C., Pace M., Thomas P. Expression and gonadotropin regulation of membrane progestin receptor alpha in Atlantic croaker (Micropogonias undulatus) gonads: role in gamete maturation. Gen. Comp. Endocrinol. 2010, 165:144-154.
57. Upadhyaya N., Haider S. Germinal vesicle breakdown in oocytes of catfish, Mystus vittatus (Bloch): relative in vitro effectiveness of estradiol-17 beta, androgens, corticosteroids, progesterone, and other pregnene derivatives. Gen. Comp. Endocrinol. 1986, 63:70-76.
58. Villa-Diaz L.G., Miyano T. Activation of p38 MAPK during porcine oocyte maturation. Biol. Reprod. 2004, 71(2):691-696.
59. Villeneuve D.L., Garcia-Reyero N., Martinović D., Cavallin J.E., Mueller N.D., Wehmas L.C., Kahl M.D., Linnum A.L., Perkins E.J., Ankley G.T. Influence of ovarian stage on transcript profiles in fathead minnow (Pimephales promelas) ovary tissue. Aquat. Toxicol. 2010, 98:354-366.
60. Wakiyama M., Imataka H., Sonenberg N. Interaction of eIF4G with poly(A)-binding protein stimulates translation and is critical for Xenopus oocyte maturation. Curr. Biol. 2000, 10:1147-1150.
61. Weber G.M., Moore A.B., Sullivan C.V. In vitro actions of insulin-like growth factor-I on ovarian follicle maturation in white perch (Morone americana). Gen. Comp. Endocrinol. 2007, 151:180-187.
62. Yao H.H.-C., Whoriskey W., Capel B. Desert hedgehog/Patched 1 signaling specifies fetal Leydig cell fate in testis organogenesis. Genes Dev. 2002, 16:1433-1440.
63. Zhou L.-Y., Wang D.-S., Kobayashi T., Yano A., Paul-Prasanth B., Suzuki A., Sakai F., Nagahama Y. A novel type of P450c17 lacking the lyase activity is responsible for C21-steroid biosynthesis in the fish ovary and head kidney. Endocrinology 2007, 148:4282-4291.
64. Zhou L.-Y., Wang D.-S., Shibata Y., Paul-Prasanth B., Suzuki A., Nagahama Y. Characterization, expression and transcriptional regulation of P450c17-I and -II in the medaka, Oryzias latipes. Biochem. Biophys. Res. Commun. 2007, 362:619-625.