Expression profiles of fsh-regulated ovarian genes during oogenesis in coho salmon

PLoS ONE

Volumn 9, Issue 12, 2014, Pages

  Guzmán, José M ^a   Luckenbach, J Adam ^a,b   Yamamoto, Yoji ^a,c,d   Swanson, Penny ^a,b  

^a NORTHWEST FISHERIES SCIENCE CENTER   (United States)

^b WASHINGTON STATE UNIVERSITY   (United States)

^c UNIVERSITY OF WASHINGTON   (United States)

^d TOKYO UNIVERSITY OF MARINE SCIENCE AND TECHNOLOGY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

CONNECTIVE TISSUE GROWTH FACTOR; CYCLINE; DECORIN; FIBRONECTIN; FOLLITROPIN; GROWTH FACTOR; INHIBIN A; MESSENGER RNA; MINICHROMOSOME MAINTENANCE PROTEIN 4; PROTEIN KINASE PIM 1; FOLLITROPIN RECEPTOR; TRANSCRIPTOME;

ALCOHOL DEHYDROGENASE 8 LIKE GENE; ANIMAL TISSUE; ARTICLE; BONE MORPHOGENETIC PROTEIN 16 GENE; CELL DIFFERENTIATION; CELL GROWTH; CELL PROLIFERATION; CELL SURVIVAL; CLUSTERIN 1 GENE; CLUSTERIN 2 GENE; COLLAGEN ALPHA 1(I) CHAIN GENE; COLLAGEN ALPHA 2(I) CHAIN GENE; CONNECTIVE TISSUE GROWTH FACTOR GENE; CONTROLLED STUDY; CYTOCHROME P450 FAMILY 19 SUBFAMILY A POLYPEPTIDE 1A GENE; DDIT4L GENE; DECORIN GENE; DNA REPLICATION LICENSING FACTOR MCM4 GENE; EXTRACELLULAR MATRIX; FEMALE; FIBRONECTIN GENE; GENE; GENE EXPRESSION; HORMONAL REGULATION; INFLUENZA VIRUS NS1A BINDING PROTEIN A GENE; INHIBIN SPECIFIC ALPHA SUBUNIT GENE; MOTHERS AGAINST DECAPENTAPLEGIC HOMOLOG 5 LIKE GENE; NONHUMAN; ONCORHYNCHUS KISUTCH; OOCYTE DEVELOPMENT; OOCYTE MATURATION; PROLIFERATING CELL NUCLEAR ANTIGEN GENE; SERINE THREONINE PROTEIN KINASE PIM 1 GENE; STEROIDOGENESIS; WHEY ACIDIC PROTEIN DOMAIN CONTAINING LIKE GENE; WILMS TUMOR PROTEIN 2 LIKE GENE; ANIMAL; GENE EXPRESSION PROFILING; GENETIC DATABASE; GENETICS; METABOLISM; OOCYTE;

ONCORHYNCHUS KISUTCH; PISCES;

ANIMALS; DATABASES, GENETIC; FEMALE; FOLLICLE STIMULATING HORMONE; GENE EXPRESSION PROFILING; ONCORHYNCHUS KISUTCH; OOCYTES; OOGENESIS; RECEPTORS, FSH; TRANSCRIPTOME;

EID: 84916908957     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0114176     Document Type: Article

References (86)

1. Levavi-Sivan B, Bogerd J, Mañanós EL, Gómez A, Lareyre JJ (2010) Perspectives on fish gonadotropins and their receptors. General and Comparative Endocrinology 165: 412-437.
2. Lubzens E, Young G, Bobe J, Cerdà J (2010) Oogenesis in teleosts: How fish eggs are formed. General and Comparative Endocrinology 165: 367-389.
3. Nagahama Y, Yamashita M (2008) Regulation of oocyte maturation in fish. Development, Growth & Differentiation 50: S195-S219.
4. Zohar Y, Mylonas CC (2001) Endocrine manipulations of spawning in cultured fish: from hormones to genes. Aquaculture 197: 99-136.
5. Patiño R, Sullivan C (2002) Ovarian follicle growth, maturation, and ovulation in teleost fish. Fish Physiol Biochem 26: 57-70.
6. Campbell B, Dickey J, Beckman B, Young G, Pierce A, et al. (2006) Previtellogenic oocyte growth in salmon: relationships among body growth, plasma insulin-like growth factor-1, estradiol-17beta, follicle-stimulating hormone and expression of ovarian genes for insulin-like growth factors, steroidogenic-acute regulatory protein and receptors for gonadotropins, growth hormone, and somatolactin. Biology of Reproduction 75: 34-44.
7. Luckenbach J, Iliev D, Goetz F, Swanson P (2008) Identification of differentially expressed ovarian genes during primary and early secondary oocyte growth in coho salmon, Oncorhynchus kisutch. Reproductive Biology and Endocrinology 6: 2.
8. Swanson P, Dickey JT, Campbell B (2003) Biochemistry and physiology of fish gonadotropins. Fish Physiology and Biochemistry 28: 53-59.
9. Swanson P, Suzuki K, Kawauchi H, Dickhoff W (1991) Isolation and characterization of two coho salmon gonadotropins, GTH I and GTH II. Biology of Reproduction 44: 29-38.
10. Molés G, Gómez A, Carrillo M, Zanuy S (2012) Development of a homologous enzyme-linked immunosorbent assay for European sea bass FSH. Reproductive cycle plasma levels in both sexes and in yearling precocious and non-precocious males. General and Comparative Endocrinology 176: 70-78.
11. Kim D-J, Cho YC, Sohn YC (2005) Molecular characterization of rockfish (Sebastes schlegeli) gonadotropin subunits and their mRNA expression profiles during oogenesis. General and Comparative Endocrinology 141: 282-290.
12. Tyler CR, Sumpter JP, Kawauchi H, Swanson P (1991) Involvement of gonadotropin in the uptake of vitellogenin into vitellogenic oocytes of the rainbow trout, Oncorhynchus mykiss. General and Comparative Endocrinology 84: 291-299.
13. Montserrat N, González A, Méndez E, Piferrer F, Planas JV (2004) Effects of follicle stimulating hormone on estradiol-17β production and P-450 aromatase (CYP19) activity and mRNA expression in brown trout vitellogenic ovarian follicles in vitro. General and Comparative Endocrinology 137: 123-131.
14. Polzonetti-Magni AM, Mosconi G, Soverchia L, Kikuyama S, Carnevali O (2004) Multihormonal control of vitellogenesis in lower vertebrates. International Review of Cytology: Academic Press. pp.1-46.
15. Tyler CR, Sumpter JP (1996) Oocyte growth and development in teleosts. Reviews in Fish Biology and Fisheries 6: 287-318.
16. Cerdà J, Bobe J, Babin PJ, Admon A, Lubzens E (2008) Functional genomics and proteomic approaches for the study of gamete formation and viability in farmed finfish. Reviews in Fisheries Science 16: 56-72.
17. Luckenbach JA, Dickey JT, Swanson P (2011) Follicle-stimulating hormone regulation of ovarian transcripts for steroidogenesis-related proteins and cell survival, growth and differentiation factors in vitro during early secondary oocyte growth in coho salmon. General and Comparative Endocrinology 171: 52-63.
18. Luckenbach JA, Yamamoto Y, Guzmán JM, Swanson P (2013) Identification of ovarian genes regulated by follicle-stimulating hormone (Fsh) in vitro during early secondary oocyte growth in coho salmon. Molecular and Cellular Endocrinology 366: 38-52.
19. Layman LC (2000) Mutations in the follicle-stimulating hormone-beta (FSH beta) and FSH receptor genes in mice and humans. Seminars in Reproductive Medicine 18: 5-10.
20. Layman LC, McDonough PG (2000) Mutations of follicle stimulating hormone-β and its receptor in human and mouse: genotype/phenotype. Molecular and Cellular Endocrinology 161: 9-17.
21. Grieshaber NA, Ko C, Grieshaber SS, Ji I, Ji TH (2003) Follicle-stimulating hormone-responsive cytoskeletal genes in rat granulosa cells: class I β-tubulin, tropomyosin-4, and kinesin heavy chain. Endocrinology 144: 29-39.
22. Thomas FH, Ethier J-F, Shimasaki S, Vanderhyden BC (2005) Follicle-stimulating hormone regulates oocyte growth by modulation of expression of oocyte and granulosa cell factors. Endocrinology 146: 941-949.
23. Nakamura I, Evans JC, Kusakabe M, Nagahama Y, Young G (2005) Changes in steroidogenic enzyme and steroidogenic acute regulatory protein messenger RNAs in ovarian follicles during ovarian development of rainbow trout (Oncorhynchus mykiss). General and Comparative Endocrinology 144: 224-231.
24. Rocha A, Zanuy S, Carrillo M, Gómez A (2009) Seasonal changes in gonadal expression of gonadotropin receptors, steroidogenic acute regulatory protein and steroidogenic enzymes in the European sea bass. General and Comparative Endocrinology 162: 265-275.
25. Kitano H, Irie S, Ohta K, Hirai T, Yamaguchi A, et al. (2011) Molecular cloning of two gonadotropin receptors and their distinct mRNA expression profiles in daily oogenesis of the wrasse Pseudolabrus sieboldi. General and Comparative Endocrinology 172: 268-276.
26. Yamamoto Y, Luckenbach JA, Middleton M, Swanson P (2011) The spatiotemporal expression of multiple coho salmon ovarian connexin genes and their hormonal regulation in vitro during oogenesis. Reproductive Biology and Endocrinology 9: 52.
27. Deloffre LAM, Andrade A, Filipe AI, Canario AVM (2012) Reference genes to quantify gene expression during oogenesis in a teleost fish. Gene 506: 69-75.
28. Davies B, Bromage N, Swanson P (1999) The brain-pituitary-gonadal axis of female rainbow trout Oncorhynchus mykiss: Effects of photoperiod manipulation. General and Comparative Endocrinology 115: 155-166.
29. Gomez JM, Weil C, Ollitrault M, Le Bail P-Y, Breton B, et al. (1999) Growth hormone (GH) and gonadotropin subunit gene expression and pituitary and plasma changes during spermatogenesis and oogenesis in rainbow trout (Oncorhynchus mykiss). General and Comparative Endocrinology 113: 413-428.
30. Kobayashi T, Pakarinen P, Torgersen J, Huhtaniemi I, Andersen Ø (2008) The gonadotropin receptors FSH-R and LH-R of Atlantic halibut (Hippoglossus hippoglossus)-2. Differential follicle expression and asynchronous oogenesis. General and Comparative Endocrinology 156: 595-602.
31. Kusakabe M, Todo T, McQuillan HJ, Goetz FW, Young G (2002) Characterization and expression of steroidogenic acute regulatory protein and MLN64 cDNAs in trout. Endocrinology 143: 2062-2070.
32. Sakai N, Tanaka M, Takahashi M, Fukada S, Mason JI, et al. (1994) Ovarian 3 beta-hydroxysteroid dehydrogenase/delta 5-4-isomerase of rainbow trout: its cDNA cloning and properties of the enzyme expressed in a mammalian cell. FEBS Letters 350: 309-313.
33. Yamamoto Y, Luckenbach J, Goetz F, Young G, Swanson P (2011) Disruption of the salmon reproductive endocrine axis through prolonged nutritional stress: Changes in circulating hormone levels and transcripts for ovarian genes involved in steroidogenesis and apoptosis. General and Comparative Endocrinology 172: 331-343.
34. Planas J, Athos J, Goetz F, Swanson P (2000) Regulation of ovarian steroidogenesis in vitro by follicle-stimulating hormone and luteinizing hormone during sexual maturation in salmonid fish. Biology of Reproduction 62: 1262-1269.
35. Matsubara H, Kazeto Y, Ijiri S, Hirai T, Adachi S, et al. (2003) Changes in mRNA levels of ovarian steroidogenic enzymes during artificial maturation of Japanese eel Anguilla japonica. Fisheries Science 69: 979-988.
36. Gen K, Okuzawa K, Kumakura N, Yamaguchi S, Kagawa H (2001) Correlation between messenger RNA expression of cytochrome P450 aromatase and its enzyme activity during oocyte development in the red seabream (Pagrus major). Biology of Reproduction 65: 1186-1194.
37. Kumar RS, Ijiri S, Trant JM (2000) Changes in the expression of genes encoding steroidogenic enzymes in the channel catfish (Ictalurus punctatus) ovary throughout a reproductive cycle. Biology of Reproduction 63: 1676-1682.
38. Mahon MG, Lindstedt KA, Hermann M, Nimpf J, Schneider WJ (1999) Multiple involvement of clusterin in chicken ovarian follicle development: Binding to two oocyte-specific members of the low density lipoprotein receptor gene family. Journal of Biological Chemistry 274: 4036-4044.
39. Zwain I, Amato P (2000) Clusterin protects granulosa cells from apoptotic cell death during follicular atresia. Experimental Cell Research 257: 101-110.
40. Le Menn F, Cerdà J, Babin P (2007) Ultrastructural aspects of the ontogeny and differentiation of ray-finned fish ovarian follicles. In: Babin P, Cerda J, Lubzens E, editors. The Fish Oocyte: Springer Netherlands. pp. 1-37.
41. Sasagawa K, Matsudo Y, Kang M, Fujimura L, Iitsuka Y, et al. (2002) Identification of Nd1, a novel murine kelch family protein, involved in stabilization of actin filaments. Journal of Biological Chemistry 277: 44140-44146.
42. Chang B, Liu G, Yang G, Mercado-Uribe I, Huang M, et al. (2009) REDD1 is required for RAS-mediated transformation of human ovarian epithelial cells. Cell Cycle 8: 780-786.
43. Berkholtz C, Lai B, Woodruff T, Shea L (2006) Distribution of extracellular matrix proteins type I collagen, type IV collagen, fibronectin, and laminin in mouse folliculogenesis. Histochemistry and Cell Biology 126: 583-592.
44. Huet C, Pisselet C, Mandon-Pepin B, Monget P, Monniaux D (2001) Extracellular matrix regulates ovine granulosa cell survival, proliferation and steroidogenesis: relationships between cell shape and function. Journal of Endocrinology 169: 347-360.
45. Huet C, Monget P, Pisselet C, Monniaux D (1997) Changes in extracellular matrix components and steroidogenic enzymes during growth and atresia of antral ovarian follicles in the sheep. Biology of Reproduction 56: 1025-1034.
46. Horiguchi M, Fujimori C, Ogiwara K, Moriyama A, Takahashi T (2008) Collagen type-I α1 chain mRNA is expressed in the follicle cells of the medaka ovary. Zoological Science 25: 937-945.
47. Wu H, Wang S, Xue A, Liu Y, Liu YE, et al. (2008) Overexpression of decorin induces apoptosis and cell growth arrest in cultured rat mesangial cells in vitro. Nephrology 13: 607-615.
48. Pankov R, Yamada KM (2002) Fibronectin at a glance. Journal of Cell Science 115: 3861-3863.
49. Asem EK, Carnegie JA, Tsang BK (1992) Fibronectin production by chicken granulosa cells in vitro: effect of follicular development. Acta Endocrinologica 127: 466-470.
50. Nagashima T, Kim J, Li Q, Lydon JP, DeMayo FJ, et al. (2011) Connective tissue growth factor is required for normal follicle development and ovulation. Molecular Endocrinology 25: 1740-1759.
51. Harlow CR, Bradshaw AC, Rae MT, Shearer KD, Hillier SG (2007) Oestrogen formation and connective tissue growth factor expression in rat granulosa cells. Journal of Endocrinology 192: 41-52.
52. Zhu G, Kang L, Yang C, Zhang X, Wang M, et al. (2012) Differential expression of CTGF in pre- and post-ovulatory granulosa cells in the hen ovary is regulated by TGFβ1 and gonadotrophins. General and Comparative Endocrinology 178: 314-322.
53. Wandji S-A, Gadsby JE, Barber JA, Hammond JM (2000) Messenger ribonucleic acids for MAC25 and connective tissue growth factor (CTGF) are inversely regulated during folliculogenesis and early luteogenesis. Endocrinology 141: 2648-2657.
54. Coffman MA, Pinter JH, Goetz FW (2000) Trout ovulatory proteins: site of synthesis, regulation, and possible biological function. Biology of Reproduction 62: 928-938.
55. Garczynski MA, Goetz FW (1997) Molecular characterization of a ribonucleic acid transcript that is highly up-regulated at the time of ovulation in the brook trout (Salvelinus fontinalis) ovary. Biology of Reproduction 57: 856-864.
56. Lyman-Gingerich J, Pelegri F (2007) Maternal factors in fish oogenesis and embryonic development. In: Babin P, Cerdà J, Lubzens E, editors. The Fish Oocyte: Springer Netherlands. pp. 141-174.
57. Narlik-Grassow M, Blanco-Aparicio C, Carnero A (2014) The PIM Family of Serine/Threonine Kinases in Cancer. Medicinal Research Reviews 34: 136-159.
58. Zippo A, De Robertis A, Bardelli M, Galvagni F, Oliviero S (2004) Identification of Flk-1 target genes in vasculogenesis: Pim-1 is required for endothelial and mural cell differentiation in vitro. Blood 103: 4536-4544.
59. Rimon E, Sasson R, Dantes A, Land-Bracha A, Amsterdam A (2004) Gonadotropin-induced gene regulation in human granulosa cells obtained from IVF patients: Modulation of genes coding for growth factors and their receptors and genes involved in cancer and other diseases. International Journal of Oncology 24: 1325-1338.
60. Xu B, Hua J, Zhang Y, KJiang X, Zhang H, et al. (2011) Proliferating cell nuclear antigen (PCNA) regulates primordial follicle assembly by promoting apoptosis of oocytes in fetal and neonatal mouse ovaries. Plos ONE 6: 1-15.
61. Korfsmeier K-H (2002) PCNA in the ovary of zebrafish (Brachydanio rerio, Ham.- Buch.). Acta Histochemica 104: 73-76.
62. Hyrien O, Marheineke K, Goldar A (2003) Paradoxes of eukaryotic DNA replication: MCM proteins and the random completion problem. Bioessays 25: 116-125.
63. Winkler GS (2010) The mammalian anti-proliferative BTG/Tob protein family. Journal of Cellular Physiology 222: 66-72.
64. Shimasaki S, Moore R, Otsuka F, Erickson G (2004) The bone morphogenetic protein system in mammalian reproduction. Endocrine Reviews 25: 72-101.
65. Li CW, Ge W (2011) Spatiotemporal expression of bone morphogenetic protein family ligands and receptors in the zebrafish ovary: A potential paracrine-signaling mechanism for oocyte-follicle cell communication. Biology of Reproduction 85: 977-986.
66. Lankford SE, Weber GM (2010) Temporal mRNA expression of transforming growth factor-beta superfamily members and inhibitors in the developing rainbow trout ovary. General and Comparative Endocrinology 166: 250-258.
67. García-López Á, Sánchez-Amaya MI, Prat F (2011) Targeted gene expression profiling in European sea bass (Dicentrarchus labrax, L.) follicles from primary growth to late vitellogenesis. Comparative Biochemistry and Physiology Part A: Molecular & Integrative Physiology 160: 374-380.
68. Clelland E, Kohli G, Campbell RK, Sharma S, Shimasaki S, et al. (2006) Bone morphogenetic protein-15 in the zebrafish ovary: complementary deoxyribonucleic acid cloning, genomic organization, tissue distribution, and role in oocyte maturation. Endocrinology 147: 201-209.
69. Kamada S, Kubota T, Taguchi M, Ho WR, Sakamoto S, et al. (1992) Effects of insulin-like growth factor-II on prolifferation and differentiation of ovarian granulosa cells. Hormone Research 37: 141-149.
70. Bobe J, Nguyen T, Jalabert B (2004) Targeted gene expression profiling in the rainbow trout (Oncorhynchus mykiss) ovary during maturational competence acquisition and oocyte maturation. Biol Reprod 71: 73-82.
71. Reinecke M (2010) Insulin-like growth factors and fish reproduction. Biology of Reproduction 82: 656-661.
72. Picha ME, Shi B, Thomas P (2012) Dual role of IGF-II in oocyte maturation in southern flounder Paralichthys lethostigma: Up-regulation of mPRα and resumption of meiosis. General and Comparative Endocrinology 177: 220-230.
73. Srivastava RK, Van Der Kraak G (1994) Regulation of DNA synthesis in goldfish vitellogenic ovarian follicles by hormones and growth factors. Journal of Experimental Zoology 270: 263-272.
74. Spicer LJ, Aad PY (2007) Insulin-like growth factor (IGF) 2 stimulates steroidogenesis and mitosis of bovine granulosa cells through the IGF1 receptor: Role of follicle-stimulating hormone and IGF2 receptor. Biology of Reproduction 77: 18-27.
75. Makanji Y, Harrison C, Robertson D (2011) Feedback regulation by inhibins A and B of the pituitary secretion of follicle-stimulating hormone. Vitamins and Hormones 85: 299-321.
76. Poon S-K, So W-K, Yu X, Liu L, Ge W (2009) Characterization of inhibin α subunit (inha) in the zebrafish: evidence for a potential feedback loop between the pituitary and ovary. Reproduction 138: 709-719.
77. Richards JS (1994) Hormonal control of gene expression in the ovary. Endocrine Reviews 15: 725-751.
78. Kaivo-Oja N, Jeffery L, Ritvos O, Mottershead D (2006) Smad signalling in the ovary. Reproductive Biology and Endocrinology 4: 21.
79. Ge W (2005) Intrafollicular paracrine communication in the zebrafish ovary: The state of the art of an emerging model for the study of vertebrate folliculogenesis. Molecular and Cellular Endocrinology 237: 1-10.
80. Wang Y, Ge W (2003) Spatial expression patterns of activin and its signaling system in the zebrafish ovarian follicle: evidence for paracrine action of activin on the oocytes. Biology of Reproduction 69: 1998-2006.
81. Hsu SY, Kubo M, Chun SY, Haluska FG, Housman DE, et al. (1995) Wilms' tumor protein WT1 as an ovarian transcription factor: decreases in expression during follicle development and repression of inhibin-alpha gene promoter. Molecular Endocrinology 9: 1356-1366.
82. Logan KA, McNatty KP, Juengel JL (2003) Expression of Wilms' tumor gene and protein localization during ovarian formation and follicular development in sheep. Biology of Reproduction 68: 635-643.
83. Chun S-Y, McGee EA, Hsu SY, Minami S, LaPolt PS, et al. (1999) Restricted expression of WT1 messenger ribonucleic acid in immature ovarian follicles: uniformity in mammalian and avian species and maintenance during reproductive senescence. Biology of Reproduction 60: 365-373.
84. Levi L, Levavi-Sivan B, Lubzens E (2008) Expression of genes associated with retinoid metabolism in the trout ovarian follicle. Biology of Reproduction 79: 570-577.
85. Lubzens E, Lissauer L, Levavi-Sivan B, Avarre JC, Sammar M (2003) Carotenoid and retinoid transport to fish oocytes and eggs: what is the role of retinol binding protein? Molecular Aspects of Medicine 24: 441-457.
86. Dasmahapatra AK, Wang X, Haasch ML (2005) Expression of Adh8 mRNA is developmentally regulated in Japanese medaka (Oryzias latipes). Comparative Biochemistry and Physiology Part B: Biochemistry and Molecular Biology 140: 657-664.