Gene Expression Networks Underlying Ovarian Development in Wild Largemouth Bass (Micropterus salmoides)

PLoS ONE

Volumn 8, Issue 3, 2013, Pages

  Martyniuk, Christopher J ^a,b   Prucha, Melinda S ^a   Doperalski, Nicholas J ^a   Antczak, Philipp ^c   Kroll, Kevin J ^a   Falciani, Francesco ^c   Barber, David S ^a   Denslow, Nancy D ^a  

^a UNIVERSITY OF FLORIDA   (United States)

^b UNIVERSITY OF NEW BRUNSWICK   (Canada)

^c UNIVERSITY OF LIVERPOOL   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIVIN; ADRENERGIC RECEPTOR; B LYMPHOCYTE RECEPTOR; ESTRADIOL; FIBRONECTIN; GROWTH DIFFERENTIATION FACTOR 9; INHIBIN; LUTEINIZING HORMONE; NERVE GROWTH FACTOR; NEU DIFFERENTIATION FACTOR; OSTEOGENIC PROTEIN 1; REACTIVE OXYGEN METABOLITE; RETINOID X RECEPTOR; SPHINGOLIPID; T LYMPHOCYTE RECEPTOR; TESTOSTERONE; VASOPRESSIN RECEPTOR; VITELLOGENIN;

ACTIN FILAMENT; ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BREEDING; CELL TYPE; CONTROLLED STUDY; DEVELOPMENTAL STAGE; DOWN REGULATION; FEMALE; GAP JUNCTION; GENE CONTROL; GENE EXPRESSION; GENE EXPRESSION PROFILING; GONADOTROPE; HISTOLOGY; LARGEMOUTH BASS; LIPID METABOLISM; LYMPHOCYTE ACTIVATION; MALE; MAST CELL; MOLECULAR GENETICS; MORPHOLOGY; NATURAL KILLER CELL; NONHUMAN; OOCYTE DEVELOPMENT; OOCYTE MATURATION; OVARY DEVELOPMENT; OVARY FOLLICLE ATRESIA; OVULATION; OXIDATIVE PHOSPHORYLATION; PROTEIN BLOOD LEVEL; PROTEIN FAMILY; REGULATORY MECHANISM; SIGNAL TRANSDUCTION; TRANSCRIPTOMICS; UPREGULATION; VITELLOGENESIS; VITELLOGENIN BLOOD LEVEL; WILD ANIMAL;

ANIMALS; BASS; BETA CATENIN; CLUSTER ANALYSIS; COMPUTATIONAL BIOLOGY; ESTROGENS; FEMALE; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GENE REGULATORY NETWORKS; INTEGRIN ALPHA5BETA1; MALE; OOGENESIS; OVARY; REPRODUCTION; SIGNAL TRANSDUCTION; VITELLOGENINS;

EID: 84875207224     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0059093     Document Type: Article

References (57)

1. Le Menn F, Cerdà J, Babin PJ (2007) Ultrastructural aspects of the ontogeny and differentiation of ray-finned fish ovarian follicles. 1-32 In The Fish Oocyte: From Basic Studies to Biotechnological Applications, edited by PJ Babin, J Cerdà and E Lubzens. Published by Springer, Dordrecht, The Netherlands.
2. 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.
3. Bobe J, Montfort J, Nguyen T, Fostier A, (2006) Identification of new participants in the rainbow trout (Oncorhynchus mykiss) oocyte maturation and ovulation processes using cDNA microarrays. Reprod Biol Endocrinol 4: 39.
4. Bobe J, Nguyen T, Fostier A, (2009) Ovarian function of the trout preovulatory ovary: new insights from recent gene expression studies. Comp Biochem Physiol A Mol Integr Physiol 153: 63-68.
5. Luckenbach JA, Iliev DB, Goetz FW, Swanson P, (2008) Identification of differentially expressed ovarian genes during primary and early secondary oocyte growth in coho salmon, Oncorhynchus kisutch. Reprod Biol Endocrinol 6: 2.
6. Hook SE, Nagler JJ, Cavileer T, Verducci J, Liu Y, et al. (2011) Relationships between the transcriptome and physiological indicators of reproduction in female rainbow trout over an annual cycle. Environ Toxicol Chem 30: 309-318.
7. Reading BJ, Chapman RW, Schaff JE, Scholl EH, Opperman CH, et al. (2012) An ovary transcriptome for all maturational stages of the striped bass (Morone saxatilis), a highly advanced perciform fish. BMC Res Notes 5: 111.
8. Tingaud-Sequeira A, Chauvigné F, Lozano J, Agulleiro MJ, Asensio E, et al. (2009) New insights into molecular pathways associated with flatfish ovarian development and atresia revealed by transcriptional analysis. BMC Genomics 10: 434.
9. Villeneuve DL, Garcia-Reyero N, Martinović D, Cavallin JE, Mueller ND, et al. (2010) Influence of ovarian stage on transcript profiles in fathead minnow (Pimephales promelas) ovary tissue. Aquat Toxicol 98: 354-366.
10. von Schalburg KR, Rise ML, Brown GD, Davidson WS, Koop BF, (2005) A comprehensive survey of the genes involved in maturation and development of the rainbow trout ovary. Biol Reprod 72: 687-699.
11. Sepúlveda MS, Johnson WE, Higman JC, Denslow ND, Schoeb TR, et al. (2002) An evaluation of biomarkers of reproductive function and potential contaminant effects in Florida largemouth bass (Micropterus salmoides floridanus) sampled from the St. Johns River. Sci Total Environ 289: 133-144.
12. Martyniuk CJ, Kroll KJ, Porak WF, Steward C, Grier HJ, et al. (2009) Seasonal relationship between gonadotropin, growth hormone, and estrogen receptor mRNA expression in the pituitary gland of largemouth bass. Gen Comp Endocrinol 163: 306-317.
13. Grier HJ, Aranzabal MCU, Patino R (2009) The Ovary, Folliculogenesis, and Oogenesis in Teleosts. In: Jamieson BGM ed. Reproductive Biology and Phylogeny of Fish (Agnathans and Bony Fishes). Enfield, USA: Science Publishers, Inc.
14. Denslow ND, Chow M, Kroll KJ, Green L, (1999) Vitellogenin as a biomarker of exposure to estrogen or estrogen mimics. Ecotoxicology 8: 385-398.
15. Doperalski NJ, Martyniuk CJ, Prucha MS, Kroll KJ, Denslow ND, et al. (2011) Cloning and expression of the translocator protein (18 kDa), voltage-dependent anion channel, and diazepam binding inhibitor in the gonad of largemouth bass (Micropterus salmoides) across the reproductive cycle. Gen Comp Endocrinol 173: 86-95.
16. Garcia-Reyero N, Griffitt RJ, Liu L, Kroll KJ, Farmerie WG, et al. (2008) Construction of a robust microarray from a non-model species largemouth bass, Micropterus salmoides (Lacepede), using pyrosequencing technology. J Fish Biol 72: 2354-2376.
17. Martyniuk CJ, Doperalski NJ, Kroll KJ, Barber DS, Denslow ND, (2012b) Sexually dimorphic transcriptomic responses in the teleostean hypothalamus: A case study with the organochlorine pesticide dieldrin. Neurotoxicology 34C: 105-117.
18. Tusher VG, Tibshirani R, Chu G, (2001) Significance analysis of microarrays applied to the ionizing radiation response. Proc Natl Acad Sci USA 98: 5116-5121.
19. Subramanian A, Tamayo P, Mootha VK, Mukherjee S, Ebert BL, et al. (2005) Gene set enrichment analysis: a knowledge-based approach for interpreting genome-wide expression profiles. Proc Natl Acad Sci USA 102: 15545-15550.
20. Kotelnikova E, Shkrob MA, Pyatnitskiy MA, Ferlini A, Daraselia N, (2012) Novel approach to meta-analysis of microarray datasets reveals muscle remodeling-related drug targets and biomarkers in Duchenne muscular dystrophy. PLoS Comput Biol 8: e1002365.
21. Martyniuk CJ, Denslow ND, (2012) Exploring androgen-regulated pathways in teleost fish using transcriptomics and proteomics. Integr. Comp. Biol. 52: 695-704.
22. Martyniuk CJ, Alvarez S, Lo BP, Elphick JR, Marlatt VL, (2012a) Hepatic Protein Expression Networks Associated with Masculinization in the Female Fathead Minnow (Pimephales promelas). J Proteome Res 11: 4147-4161.
23. Rozen S, Skaletsky HJ (2000) Primer3 on the WWW for general users and for biologist programmers. In: Krawetz S, Misener S (eds) Bioinformatics Methods and Protocols: Methods in Molecular Biology. Humana Press, Totowa, NJ 365-386.
24. Ings JS, Van Der Kraak GJ, (2006) Characterization of the mRNA expression of StAR and steroidogenic enzymes in zebrafish ovarian follicles. Mol Reprod Dev 73: 943-954.
25. 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. Gen Comp Endocrinol 162: 265-275.
26. Essex-Fraser PA, Steele SL, Bernier NJ, Murray BW, Stevens ED, et al. (2005) Expression of four glutamine synthetase genes in the early stages of development of rainbow trout (Oncorhynchus mykiss) in relationship to nitrogen excretion. J Biol Chem 280: 20268-20273.
27. Billiau AD, Sefrioui H, Overbergh L, Rutgeerts O, Goebels J, et al. (2001) Transforming growth factor-beta inhibits lymphokine activated killer cytotoxicity of bone marrow cells: implications for the graft-versus-leukemia effect in irradiation allogeneic bone marrow chimeras. Transplantation 71: 292-299.
28. Mylonas CC, Scott AP, Zohar Y, (1997) Plasma gonadotropin II, sex steroids, and thyroid hormones in wild striped bass (Morone saxatilis) during spermiation and final oocyte maturation. Gen Comp Endocrinol. 108: 223-236.
29. Mylonas CC, Woods LC 3rd, Thomas P, Zohar Y (1998) Endocrine profiles of female striped bass (Morone saxatilis) in captivity, during postvitellogenesis and induction of final oocyte maturation via controlled-release GnRHa-delivery systems. Gen Comp Endocrinol 110: 276-289.
30. Sabo-Attwood T, Blum JL, Kroll KJ, Patel V, Birkholz D, et al. (2007) Distinct expression and activity profiles of largemouth bass (Micropterus salmoides) estrogen receptors in response to estradiol and nonylphenol. J Mol Endocrinol. 39: 223-237.
31. Sabo-Attwood T, Kroll KJ, Denslow ND, (2004) Differential expression of largemouth bass (Micropterus salmoides) estrogen receptor isotypes alpha, beta, and gamma by estradiol. Mol Cell Endocrinol 218: 107-118.
32. Kocerha J, Prucha MS, Kroll KJ, Steinhilber D, Denslow N, (2010) Regulation of steroidogenic acute regulatory protein transcription in largemouth bass by orphan nuclear receptor signaling pathways. Endocrinology 151: 341-349.
33. Baron D, Houlgatte R, Fostier A, Guiguen Y, (2005) Large-scale temporal gene expression profiling during gonadal differentiation and early gametogenesis in rainbow trout. Biol Reprod 73: 959-966.
34. Santos EM, Workman VL, Paull GC, Filby AL, Van Look KJ, et al. (2007) Molecular basis of sex and reproductive status in breeding zebrafish. Physiol Genomics. 30: 111-22.
35. Blythe WG, Helfrich LA, Sullivan CV, (1994) Sex steroid hormone and vitellogenin levels in striped bass (Morone saxatilis) maturing under 6-, 9-, and 12-month photothermal cycles. Gen Comp Endocrinol 94: 122-134.
36. Lokman PM, Kazeto Y, Ijiri S, Young G, Miura T, et al. (2003) Ovarian mitochondrial cytochrome b mRNA levels increase with sexual maturity in freshwater eels (Anguilla spp.). J Comp Physiol B 173: 11-19.
37. Agulleiro MJ, André M, Morais S, Cerdà J, Babin PJ, (2007) High transcript level of fatty acid-binding protein 11 but not of very low-density lipoprotein receptor is correlated to ovarian follicle atresia in a teleost fish (Solea senegalensis). Biol Reprod 77: 504-516.
38. Dominguez GA, Quattro JM, Denslow ND, Kroll KJ, Prucha MS, et al. (2012) Identification and transcriptional modulation of the largemouth bass, Micropterus salmoides, vitellogenin receptor during oocyte development by insulin and sex steroids. Biol Reprod 87: 67.
39. Gohin M, Bodinier P, Fostier A, Chesnel F, Bobe J, (2011) Aromatase is expressed and active in the rainbow trout oocyte during final oocyte maturation. Mol Reprod Dev 78: 510-518.
40. Trudeau VL, Spanswick D, Fraser EJ, Larivière K, Crump D, et al. (2000) The role of amino acid neurotransmitters in the regulation of pituitary gonadotropin release in fish. Biochem Cell Biol 78: 241-259.
41. Erdö SL, László A, (1984) High specific gamma-aminobutyric acid binding to membranes of the human ovary. J Neurochem. 42: 1464-1467.
42. 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. Biol Reprod 57: 856-864.
43. Oliveira PF, Sousa M, Barros A, Moura T, Rebelo da Costa A, (2009) Intracellular pH regulation in human Sertoli cells: role of membrane transporters. Reproduction 137: 353-359.
44. Krishna A, Beesley K, Terranova PF, (1989) Histamine, mast cells and ovarian function. J Endocrinol 120: 363-371.
45. Chaves-Pozo E, Zou J, Secombes CJ, Cuesta A, Tafalla C, (2010) The rainbow trout (Oncorhynchus mykiss) interferon response in the ovary. Mol Immunol 47: 1757-1764.
46. Lara HE, McDonald JK, Ojeda SR, (1990) Involvement of nerve growth factor in female sexual development. Endocrinology 126: 364-375.
47. Russell DL, Richards JS, (1999) Differentiation-dependent prolactin responsiveness and stat (signal transducers and activators of transcription) signaling in rat ovarian cells. Mol Endocrinol 13: 2049-2064.
48. Knight PG, Glister C, (2006) TGF-beta superfamily members and ovarian follicle development. Reproduction 132: 191-206.
49. Tubbs C, Pace M, Thomas P, (2009) Expression and gonadotropin regulation of membrane progestin receptor alpha in Atlantic croaker (Micropogonias undulatus) gonads: role in gamete maturation. Gen Comp Endocrinol 165: 144-154.
50. Kazeto Y, Goto-Kazeto R, Thomas P, Trant JM, (2005a) Molecular characterization of three forms of putative membrane-bound progestin receptors and their tissue-distribution in channel catfish, Ictalurus punctatus. J Mol Endocrinol 34: 781-791.
51. Kazeto Y, Goto-Kazeto R, Trant JM, (2005b) 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 142: 204-211.
52. Tokumoto M, Nagahama Y, Thomas P, Tokumoto T, (2006) Cloning and identification of a membrane progestin receptor in goldfish ovaries and evidence it is an intermediary in oocyte meiotic maturation. Gen. Comp. Endocrinol 145: 101-108.
53. Campbell B, Dickey J, Beckman B, Young G, Pierce A, Fukada H, 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. Biol Reprod 75: 34-44.
54. Gomez JM, Mourot B, Fostier A, Le Gac F, (1999) Growth hormone receptors in ovary and liver during gametogenesis in female rainbow trout (Oncorhynchus mykiss). J Reprod Fertil 115: 275-285.
55. Ma X, Liu X, Zhang Y, Zhu P, Ye W, et al. (2007) Two growth hormone receptors in Nile tilapia (Oreochromis niloticus): molecular characterization, tissue distribution and expression profiles in the gonad during the reproductive cycle. Comp Biochem Physiol B Biochem Mol Biol 147: 325-339.
56. Kwok HF, So WK, Wang Y, Ge W, (2005) Zebrafish gonadotropins and their receptors: I. Cloning and characterization of zebrafish follicle-stimulating hormone and luteinizing hormone receptors-evidence for their distinct functions in follicle development. Biol Reprod 72: 1370-1381.
57. Mittelholzer C, Andersson E, Taranger GL, Consten D, Hirai T, et al. (2009) Molecular characterization and quantification of the gonadotropin receptors FSH-R and LH-R from Atlantic cod (Gadus morhua). Gen Comp Endocrinol 160: 47-58.