Sex-biased miRNA expression in atlantic halibut (Hippoglossus hippoglossus) brain and gonads

Sexual Development

Volumn 6, Issue 5, 2012, Pages 257-266

  Bizuayehu, T T ^a   Babiak, J ^a   Norberg, B ^b   Fernandes, J M O ^a   Johansen, S D ^a,c   Babiak, I ^a  

^a NORD UNIVERSITY   (Norway)

^b INSTITUTE OF MARINE RESEARCH   (Norway)

^c UNIVERSITY OF TROMSØ   (Norway)

Author keywords

Atlantic halibut; Fadrozole; Methyltestosterone; MiRNA; Next generation sequencing; Sex differentiation; Sex reversal; Teleost

Indexed keywords

HIPPOGLOSSUS HIPPOGLOSSUS; TELEOSTEI;

MICRORNA;

ANIMAL; ARTICLE; ATLANTIC OCEAN; BRAIN; FEMALE; FLOUNDER; GENE EXPRESSION REGULATION; GENE LIBRARY; GENETICS; GONAD; GROWTH, DEVELOPMENT AND AGING; MALE; METABOLISM; NUCLEOTIDE SEQUENCE; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SEXUAL DEVELOPMENT;

ANIMALS; ATLANTIC OCEAN; BRAIN; CONSERVED SEQUENCE; FEMALE; FLOUNDER; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GENE LIBRARY; GONADS; MALE; MICRORNAS; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; SEX CHARACTERISTICS;

EID: 84864259011     PISSN: 16615425     EISSN: 16615433     Source Type: Journal    
DOI: 10.1159/000341378     Document Type: Article

References (60)

1. Ahn HW, Morin RD, Zhao H, Harris RA, Coarfa C, et al: MicroRNA transcriptome in the newborn mouse ovaries determined by massive parallel sequencing. Mol Hum Reprod 16: 463-471 (2010).
2. Andersen CL, Jensen JL, Orntoft TF: Normalization of real-Time quantitative reverse transcription-PCR data: A model-based variance estimation approach to identify genes suited for normalization, applied to bladder and colon cancer data sets. Cancer Res 64: 5245-5250 (2004). (Pubitemid 39006544)
3. Armisen J, Gilchrist MJ, Wilczynska A, Standart N, Miska EA: Abundant and dynamically expressed miRNAs, piRNAs, and other small RNAs in the vertebrate Xenopus tropicalis . Genome Res 19: 1766-1775 (2009).
4. Babiak I, Ottesen O, Rudolfsen G, Johnsen S: Quantitative characteristics of Atlantic halibut, Hippoglossus hippoglossus L., semen throughout the reproductive season. Theriogenology 65: 1587-1604 (2006).
5. Babiak J, Babiak I, van Nes S, Harboe T, Haugen T, Norberg B: Induced sex reversal using an aromatase inhibitor, fadrozole, in Atlantic halibut (Hippoglossus hippoglossus L.). Aquaculture 324-325: 276-280 (2012).
6. Bail S, Swerdel M, Liu H, Jiao X, Goff LA, et al: Differential regulation of microRNA stability. RNA 16: 1032-1039 (2010).
7. Bannister SC, Tizard MLV, Doran TJ, Sinclair AH, Smith CA: Sexually dimorphic micro-RNA expression during chicken embryonic gonadal development. Biol Reprod 81: 165-176 (2009).
8. Bannister SC, Smith CA, Roeszler KN, Doran TJ, Sinclair AH, Tizard ML: Manipulation of estrogen synthesis alters mir202 expression in embryonic chicken gonads. Biol Reprod 85: 22-30 (2011).
9. Bizuayehu T, Lanes C, Furmanek T, Karlsen B, Fernandes J, et al: Differential expression patterns of conserved miRNAs and isomiRs during Atlantic halibut development. BMC Genomics 13: 11 (2012).
10. Castellano L, Giamas G, Jacob J, Coombes RC, Lucchesi W, et al: The estrogen receptor-induced microRNA signature regulates itself and its transcriptional response. Proc Natl Acad Sci USA 106: 15732-15737 (2009).
11. Cheung L, Gustavsson C, Norstedt G, Tollet-Egnell P: Sex-different and growth hormoneregulated expression of microRNA in rat liver. BMC Mol Biol 10: 13 (2009).
12. Chiang HR, Schoenfeld LW, Ruby JG, Auyeung VC, Spies N, et al: Mammalian microRNAs: Experimental evaluation of novel and previously annotated genes. Genes Dev 24: 992-1009 (2010).
13. Cochrane DR, Cittelly DM, Richer JK: Steroid receptors and microRNAs: Relationships revealed. Steroids 76: 1-10 (2011).
14. Delaloy C, Liu L, Lee J-A, Su H, Shen F, et al: MicroRNA-9 coordinates proliferation and migration of human embryonic stem cell-derived neural progenitors. Cell Stem Cell 6: 323-335 (2010).
15. Fernandes J, Mommens M, Hagen O, Babiak I, Solberg C: Selection of suitable reference genes for real-Time PCR studies of Atlantic halibut development. Comp Biochem Physiol B Biochem Mol Biol 150: 23-32 (2008).
16. Furuchi T, Masuko K, Nishimune Y, Obinata M, Matsui Y: Inhibition of testicular germ cell apoptosis and differentiation in mice misexpressing Bcl-2 in spermatogonia. Development 122: 1703-1709 (1996). (Pubitemid 26192736)
17. Gammell P: MicroRNAs: Recently discovered key regulators of proliferation and apoptosis in animal cells. Identification of miRNAs regulating growth and survival. Cytotechnology 53: 55-63 (2007). (Pubitemid 46944869)
18. Gao F-B: Context-dependent functions of specific microRNAs in neuronal development. Neural Dev 5: 25 (2010).
19. Giraldez AJ, Mishima Y, Rihel J, Grocock RJ, Van Dongen S, et al: Zebrafish mir-430 promotes deadenylation and clearance of maternal mRNAs. Science 312: 75-79 (2006).
20. Guiguen Y, Fostier A, Piferrer F, Chang CF: Ovarian aromatase and estrogens: A pivotal role for gonadal sex differentiation and sex change in fish. Gen Comp Endocrinol 165: 352-366 (2010).
21. Hattori RS, Murai Y, Oura M, Masuda S, Majhi SK, et al: A Y-linked anti-müllerian hormone duplication takes over a critical role in sex determination. Proc Natl Acad Sci USA 109: 2955-2959 (2012).
22. Hayashi K, Chuva de Sousa Lopes SM, Kaneda M, Tang F, Hajkova P, et al: MicroRNA biogenesis is required for mouse primordial germ cell development and spermatogenesis. PLoS One 3:e1738 (2008).
23. He XJ, Yan YL, Eberhart JK, Herpin A, Wagner TU, et al: MiR-196 regulates axial patterning and pectoral appendage initiation. Dev Biol 357: 463-477 (2011).
24. Hendry CI, Martin-Robichaud DJ, Benfey TJ: Gonadal sex differentiation in Atlantic halibut. J Fish Biol 60: 1431-1442 (2002).
25. Hendry CI, Martin-Robichaud DJ, Benfey TJ: Hormonal sex reversal of Atlantic halibut (Hippoglossus hippoglossus L.). Aquaculture 219: 769-781 (2003). (Pubitemid 36345547)
26. Houwing S, Kamminga LM, Berezikov E, Cronembold D, Girard A, et al: A role for Piwi and piRNAs in germ cell maintenance and transposon silencing in zebrafish. Cell 129: 69-82 (2007). (Pubitemid 46509793)
27. Imsland AK, Jonassen TM: The relation between age at first maturity and growth in Atlantic halibut (Hippoglossus hippoglossus) reared at four different light regimes. Aquaculture Res 36: 1-7 (2005). (Pubitemid 40145580)
28. Jákupsstovu S, Haug T: Growth, sexual maturation, and spawning season of Atlantic halibut, Hippoglossus hippoglossus, in Faroese waters. Fisheries Res 6: 201-215 (1988).
29. Juanchich A, Klopp C, Guiguen Y, Bobe J: MicroRNAs expression during fish oogenesis and sex differentiation. 9th International Symposium on Reproductive Physiology of Fish, vol 4, p 80 (Cochin, India 2011).
30. Juhila J, Sipila T, Icay K, Nicorici D, Ellonen P, et al: MicroRNA expression profiling reveals miRNA families regulating specific biological pathways in mouse frontal cortex and hippocampus. PLoS One 6:e21495 (2011).
31. Jung YH, Gupta MK, Shin JY, Uhm SJ, Lee HT: MicroRNA signature in testes-derived male germ-line stem cells. Mol Hum Reprod 16: 804-810 (2010).
32. Kapsimali M, Kloosterman WP, de Bruijn E, Rosa F, Plasterk RHA, Wilson SW: Micro-RNAs show a wide diversity of expression profiles in the developing and mature central nervous system. Genome Biol 8: 16 (2007).
33. Ling KH, Brautigan P, Hahn C, Daish T, Rayner J, et al: Deep sequencing analysis of the developing mouse brain reveals a novel microRNA. BMC Genomics 12: 176 (2011).
34. Linsen S, de Wit E, de Bruijn E, Cuppen E: Small RNA expression and strain specificity in the rat. BMC Genomics 11: 249 (2010).
35. Mangor-Jensen A, Harboe T, Shields RJ, Gara B, Naas KE: Atlantic halibut, Hippoglossus hippoglossus L., larvae cultivation literature, including a bibliography. Aquaculture Res 29: 857-886 (1998). (Pubitemid 29045798)
36. Matsuda M, Shinomiya A, Kinoshita M, Suzuki A, Kobayashi T, et al: Dmy gene induces male development in genetically female (XX) medaka fish. Proc Natl Acad Sci USA 104: 3865-3870 (2007). (Pubitemid 47181545)
37. Mestdagh P, Van Vlierberghe P, De Weer A, Muth D, Westermann F, et al: A novel and universal method for microRNA RT-qPCR data normalization. Genome Biol 10:R64 (2009).
38. Morin RD, O'Connor MD, Griffith M, Kuchenbauer F, Delaney A, et al: Application of massively parallel sequencing to microRNA profiling and discovery in human embryonic stem cells. Genome Res 18: 610-621 (2008). (Pubitemid 351482785)
39. Papaioannou MD, Nef S: MicroRNAs in the testis: building up male fertility. J Androl 31: 26-33 (2010).
40. Papaioannou MD, Pitetti J-L, Ro S, Park C, Aubry F, et al: Sertoli cell Dicer is essential for spermatogenesis in mice. Dev Biol 326: 250-259 (2009).
41. Pase L, Layton JE, Kloosterman WP, Carradice D, Waterhouse PM, Lieschke GJ: Mir-451 regulates zebrafish erythroid maturation in vivo via its target gata2 . Blood 113: 1794-1804 (2009).
42. Pfaffl MW, Horgan GW, Dempfle L: Relative expression software tool (RESTR) for groupwise comparison and statistical analysis of relative expression results in real-Time PCR. Nucleic Acids Res 30:e36 (2002).
43. Print CG, Loveland KL: Germ cell suicide: New insights into apoptosis during spermatogenesis. Bioessays 22: 423-430 (2000). (Pubitemid 30308268)
44. Ro S, Song R, Park C, Zheng H, Sanders KM, Yan W: Cloning and expression profiling of small RNAs expressed in the mouse ovary. RNA 13: 2366-2380 (2007). (Pubitemid 350127576)
45. Rodriguez I, Ody C, Araki K, Garcia I, Vassalli P: An early and massive wave of germinal cell apoptosis is required for the development of functional spermatogenesis. EMBO J 16: 2262-2270 (1997). (Pubitemid 27260376)
46. Schulte JH, Marschall T, Martin M, Rosenstiel P, Mestdagh P, et al: Deep sequencing reveals differential expression of microRNAs in favorable versus unfavorable neuroblastoma. Nucleic Acids Res 38: 5919-5938 (2010).
47. Schulz RW, de Franca LR, Lareyre JJ, Legac F, Chiarini-Garcia H, et al: Spermatogenesis in fish. Gen Comp Endocrinol 165: 390-411 (2010).
48. Sempere L, Freemantle S, Pitha-Rowe I, Moss E, Dmitrovsky E, Ambros V: Expression profiling of mammalian microRNAs uncovers a subset of brain-expressed microRNAs with possible roles in murine and human neuronal differentiation. Genome Biol 5:R13 (2004).
49. Shi XB, Xue L, Yang J, Ma AH, Zhao J, et al: An androgen-regulated miRNA suppresses Bak1 expression and induces androgen-independent growth of prostate cancer cells. Proc Natl Acad Sci USA 104: 19983-19988 (2007).
50. Sirotkin AV, Lauková M, Ovcharenko D, Brenaut P, Mlynček M: Identification of microRNAs controlling human ovarian cell proliferation and apoptosis. J Cell Physiol 223: 49-56 (2010).
51. Soares A, Pereira P, Santos B, Egas C, Gomes A, et al: Parallel DNA pyrosequencing unveils new zebrafish microRNAs. BMC Genomics 10: 195 (2009).
52. Tong MH, Mitchell D, Evanoff R, Griswold MD: Expression of Mirlet7 family microRNAs in response to retinoic acid-induced spermatogonial differentiation in mice. Biol Reprod 85: 189-197 (2011).
53. Tvedt HB, Benfey TJ, Martin-Robichaud DJ, Mc-Gowan C, Reith M: Gynogenesis and sex determination in Atlantic halibut (Hippoglossus hippoglossus) . Aquaculture 252: 573-583 (2006). (Pubitemid 43220232)
54. Ugras S, Brill E, Jacobsen A, Hafner M, Socci ND, et al: Small RNA sequencing and functional characterization reveals micro-RNA-143 tumor suppressor activity in liposarcoma. Cancer Res 71: 5659-5669 (2011).
55. van Nes S, Andersen Ø: Temperature effects on sex determination and ontogenetic gene expression of the aromatases cyp19a and cyp19b, and the estrogen receptors esr1 and esr2 in Atlantic halibut (Hippoglossus hippoglossus) . Mol Reprod Dev 73: 1481-1490 (2006). (Pubitemid 44637100)
56. van Nes S, Moe M, Andersen O: Molecular characterization and expression of two cyp19 (p450 aromatase) genes in embryos, larvae, and adults of Atlantic halibut (Hippoglossus hippoglossus) . Mol Reprod Dev 72: 437-449 (2005). (Pubitemid 41511035)
57. Warren WC, Clayton DF, Ellegren H, Arnold AP, Hillier LW, et al: The genome of a songbird. Nature 464: 757-762 (2010).
58. Weltzien FA, Taranger GL, Karlsen O, Norberg B: Spermatogenesis and related plasma androgen levels in Atlantic halibut (Hippoglossus hippoglossus L.). Comp Biochem Physiol A Mol Int Physiol 132: 567-575 (2002). (Pubitemid 34607314)
59. Xu N, Papagiannakopoulos T, Pan GJ, Thomson JA, Kosik KS: MicroRNA-145 regulates OCT4, SOX2, and KLF4 and represses pluripotency in human embryonic stem cells. Cell 137: 647-658 (2009).
60. Yuva-Aydemir Y, Simkin A, Gascon E, Gao FB: MicroRNA-9 functional evolution of a conserved small regulatory RNA. RNA Biol 8: 557-564 (2011).