Hormonal regulation of sertoli cell micro-RNAs at spermiation

Endocrinology

Volumn 152, Issue 4, 2011, Pages 1670-1683

  Nicholls, Peter K ^a,b   Harrison, Craig A ^a,b   Walton, Kelly L ^a   McLachlan, Robert I ^a   O'Donnell, Liza ^a   Stanton, Peter G ^a,b  

^a MONASH MEDICAL CENTRE   (Australia)

^b MONASH UNIVERSITY   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

EPIDERMAL GROWTH FACTOR RECEPTOR PATHWAY SUBSTRATE 15; LUCIFERASE; MICRORNA; MICRORNA 23B; PHOSPHATIDYLINOSITOL 3,4,5 TRISPHOSPHATE 3 PHOSPHATASE; UNCLASSIFIED DRUG;

3' UNTRANSLATED REGION; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BIOINFORMATICS; CONTROLLED STUDY; CYTOSKELETON; DOWN REGULATION; FOCAL ADHESION; GENE EXPRESSION; GENE FUNCTION; HORMONAL REGULATION; MALE; NONHUMAN; PRIORITY JOURNAL; RAT; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SEMINIFEROUS TUBULE; SERTOLI CELL; SPERMATID; SPERMATOGENESIS; UPREGULATION; WESTERN BLOTTING;

ANDROGENS; ANIMALS; BLOTTING, WESTERN; CALCIUM-BINDING PROTEINS; CELLS, CULTURED; COMPUTATIONAL BIOLOGY; FOLLICLE STIMULATING HORMONE; HUMANS; IMMUNOHISTOCHEMISTRY; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; MALE; MICRORNAS; PTEN PHOSPHOHYDROLASE; RATS; RATS, SPRAGUE-DAWLEY; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; SEMINIFEROUS TUBULES; SERTOLI CELLS; TESTIS;

EID: 79953165330     PISSN: 00137227     EISSN: 00137227     Source Type: Journal    
DOI: 10.1210/en.2010-1341     Document Type: Article

References (67)

1. Holdcraft RW, Braun RE 2004 Hormonal regulation of spermatogenesis. Int J Androl 27:335-342 (Pubitemid 39665391)
2. McLachlan RI, O'Donnell L, Meachem SJ, Stanton PG, de Kretser DM, Pratis K, Robertson DM 2002 Identification of specific sites of hormonal regulation in spermatogenesis in rats, monkeys, and man. Recent Prog Horm Res 57:149-179
3. O'Donnell L, Meachem SJ, Stanton PG, McLachlan RI 2006 Endocrine regulation of spermatogenesis. In: Neill JD, ed. Knobil and Neill's physiology of reproduction. 3rd ed. San Diego: Elsevier
4. Walker WH, Cheng J 2005 FSH and testosterone signaling in Sertoli cells. Reproduction 130:15-28 (Pubitemid 41015229)
5. Ruwanpura SM, McLachlan RI, Stanton PG, Meachem SJ 2008 Follicle-stimulating hormone affects spermatogonial survival by regulating the intrinsic apoptotic pathway in adult rats. Biol Reprod 78:705-713 (Pubitemid 351469356)
6. Sluka P, O'Donnell L, Bartles JR, Stanton PG 2006 FSH regulates the formation of adherens junctions and ectoplasmic specialisations between rat Sertoli cells in vitro and in vivo. J Endocrinol 189:381-395
7. Beardsley A, Robertson DM, O'Donnell L 2006 A complex containing alpha6beta1-integrin and phosphorylated focal adhesion kinase between Sertoli cells and elongated spermatids during spermatid release from the seminiferous epithelium. J Endocrinol 190:759-770 (Pubitemid 44560251)
8. Saito K, O'Donnell L, McLachlan RI, Robertson DM 2000 Spermiation failure is a major contributor to early spermatogenic suppression caused by hormone withdrawal in adult rats. Endocrinology 141:2779-2785 (Pubitemid 32250439)
9. O'Donnell L, Pratis K, Wagenfeld A, Gottwald U, Müller J, Leder G, McLachlan RI, Stanton PG 2009 Transcriptional profiling of the hormone-responsive stages of spermatogenesis reveals cell-, stage-, and hormone-specific events. Endocrinology 150:5074-5084
10. El Chami N, Ikhlef F, Kaszas K, Yakoub S, Tabone E, Siddeek B, Cunha S, Beaudoin C, Morel L, Benahmed M, Régnier DC 2005 Androgen-dependent apoptosis in male germ cells is regulated through the proto-oncoprotein Cbl. J Cell Biol 171:651-661 (Pubitemid 41668724)
11. Pascall JC 1997 Post-transcriptional regulation of gene expression by androgens: recent observations from the epidermal growth factor gene. J Mol Endocrinol 18:177-180
12. Sahmi M, Nicola ES, Price CA 2006 Hormonal regulation of cytochrome P450 aromatase mRNA stability in non-luteinizing bovine granulosa cells in vitro. J Endocrinol 190:107-115 (Pubitemid 44161066)
13. Fiedler SD, Carletti MZ, Hong X, Christenson LK 2008 Hormonal regulation of microRNA expression in periovulatory mouse mural granulosa cells. Biol Reprod 79:1030-1037
14. Pan Q, Luo X, Chegini N 2008 Differential expression of microRNAs in myometrium and leiomyomas and regulation by ovarian steroids. J Cell Mol Med 12:227-240 (Pubitemid 351430465)
15. Pan Q, Luo X, Chegini N 2010 MicroRNA 21: response to hormonal therapies and regulatory function in leiomyoma, transformed leiomyoma and leiomyosarcoma cells. Mol Hum Reprod 16:215-227
16. Yao N, Lu CL, Zhao JJ, Xia HF, Sun DG, Shi XQ, Wang C, Li D, Cui Y, Ma X 2009 A network of miRNAs expressed in the ovary are regulated by FSH. Front Biosci 14:3239-3245
17. Peter ME 2010 Targeting of mRNAs by multiple miRNAs: the next step. Oncogene 29:2161-2164
18. Bannister SC, Tizard ML, Doran TJ, Sinclair AH, Smith CA 2009 Sexually dimorphic microRNA expression during chicken embryonic gonadal development. Biol Reprod 81:165-176
19. Barad O, Meiri E, Avniel A, Aharonov R, Barzilai A, Bentwich I, Einav U, Gilad S, Hurban P, Karov Y, Lobenhofer EK, Sharon E, Shiboleth YM, Shtutman M, Bentwich Z, Einat P 2004 MicroRNA expression detected by oligonucleotide microarrays: system establishment and expression profiling in human tissues. Genome Res 14:2486-2494 (Pubitemid 40012232)
20. Mishima T, Takizawa T, Luo SS, Ishibashi O, Kawahigashi Y, Mizuguchi Y, Ishikawa T, Mori M, Kanda T, Goto T, Takizawa T 2008 MicroRNA (miRNA) cloning analysis reveals sex differences in miRNA expression profiles between adult mouse testis and ovary. Reproduction 136:811-822
21. Ro S, Park C, Sanders KM, McCarrey JR, Yan W 2007 Cloning and expression profiling of testis-expressed microRNAs. Dev Biol 311:592-602 (Pubitemid 350064371)
22. Song R, Ro S, Michaels JD, Park C, McCarrey JR, Yan W 2009 Many X-linked microRNAs escape meiotic sex chromosome inactivation. Nat Genet 41:488-493
23. Yan N, Lu Y, Sun H, Qiu W, Tao D, Liu Y, Chen H, Yang Y, Zhang S, Li X, Ma Y 2009 Microarray profiling of microRNAs expressed in testis tissues of developing primates. J Assist Reprod Genet 26:179-186
24. Yan N, Lu Y, Sun H, Tao D, Zhang S, Liu W, Ma Y 2007 A microarray for microRNA profiling in mouse testis tissues. Reproduction 134:73-79 (Pubitemid 47244840)
25. Papaioannou MD, Pitetti JL, Ro S, Park C, Aubry F, Schaad O, Vejnar CE, Kühne F, Descombes P, Zdobnov EM, McManus MT, Guillou F, Harfe BD, Yan W, Jégou B, Nef S 2009 Sertoli cell Dicer is essential for spermatogenesis in mice. Dev Biol 326:250-259
26. Hayashi K, Chuva de Sousa Lopes SM, Kaneda M, Tang F, Hajkova P, Lao K, O'Carroll D, Das PP, Tarakhovsky A, Miska EA, Surani MA 2008 MicroRNA biogenesis is required for mouse primordial germ cell development and spermatogenesis. PLoS ONE 3:e1738
27. Tseden K, Topaloglu O, Meinhardt A, Dev A, Adham I, Müller C, Wolf S, Böhm D, Schlüter G, Engel W, Nayernia K 2007 Premature translation of transition protein 2 mRNA causes sperm abnormalities and male infertility. Mol Reprod Dev 74:273-279 (Pubitemid 46147803)
28. Toloubeydokhti T, Pan Q, Luo X, Bukulmez O, Chegini N 2008 The expression and ovarian steroid regulation of endometrial micro- RNAs. Reprod Sci 15:993-1001
29. Ambs S, Prueitt RL, Yi M, Hudson RS, Howe TM, Petrocca F, Wallace TA, Liu CG, Volinia S, Calin GA, Yfantis HG, Stephens RM, Croce CM 2008 Genomic profiling of microRNA and messenger RNA reveals deregulated microRNA expression in prostate cancer. Cancer Res 68:6162-6170
30. Wang G, Wang Y, Feng W, Wang X, Yang JY, Zhao Y, Liu Y 2008 Transcription factor and microRNA regulation in androgen-dependent and -independent prostate cancer cells. BMC Genomics 9(Suppl 2):S22
31. Shi XB, Xue L, Yang J, Ma AH, Zhao J, Xu M, Tepper CG, Evans CP, Kung HJ, deVere White RW 2007 An androgen-regulated miRNA suppresses Bak1 expression and induces androgen-independent growth of prostate cancer cells. Proc Natl Acad Sci USA 104:19983-19988
32. Le MT, Teh C, Shyh-Chang N, Xie H, Zhou B, Korzh V, Lodish HF, Lim B 2009 MicroRNA-125b is a novel negative regulator of p53. Genes Dev 23:862-876
33. Beardsley A, O'Donnell L 2003 Characterization of normal spermiation and spermiation failure induced by hormone suppression in adult rats. Biol Reprod 68:1299-1307 (Pubitemid 36359118)
34. Kaitu'u-Lino TJ, Sluka P, Foo CF, Stanton PG 2007 Claudin-11 expression and localisation is regulated by androgens in rat Sertoli cells in vitro. Reproduction 133:1169-1179
35. Nicholls PK, Harrison CA, Gilchrist RB, Farnworth PG, Stanton PG 2009 Growth differentiation factor 9 is a germ cell regulator of Sertoli cell function. Endocrinology 150:2481-2490
36. Wine RN, Chapin RE 1999 Adhesion and signaling proteins spatiotemporally associated with spermiation in the rat. J Androl 20:198-213 (Pubitemid 29203350)
37. Kotaja N, Kimmins S, Brancorsini S, Hentsch D, Vonesch JL, Davidson I, Parvinen M, Sassone-Corsi P 2004 Preparation, isolation and characterization of stage-specific spermatogenic cells for cellular and molecular analysis. Nat Methods 1:249-254
38. Lampa J, Hoogerbrugge JW, Baarends WM, Stanton PG, Perryman KJ, Grootegoed JA, Robertson DM 1999 Follicle-stimulating hormone and testosterone stimulation of immature and mature Sertoli cells in vitro: inhibin and N-cadherin levels and round spermatid binding. J Androl 20:399-406 (Pubitemid 29289100)
39. Friedman RC, Farh KK, Burge CB, Bartel DP 2009 Most mammalian mRNAs are conserved targets of microRNAs. Genome Res 19:92-105
40. Papadopoulos GL, Alexiou P, Maragkakis M, Reczko M, Hatzigeorgiou AG 2009 DIANA-mirPath: integrating human and mouse microRNAs in pathways. Bioinformatics 25:1991-1993
41. Loya CM, Lu CS, Van Vactor D, Fulga TA 2009 Transgenic microRNA inhibition with spatiotemporal specificity in intact organisms. Nat Methods 6:897-903
42. Chapin RE, Wine RN, Harris MW, Borchers CH, Haseman JK 2001 Structure and control of a cell-cell adhesion complex associated with spermiation in rat seminiferous epithelium. J Androl 22:1030-1052 (Pubitemid 33020325)
43. Kerr JB, Loveland KL, O'Bryan MK, de Kretser DM 2006 Cytology of the testis and intrinsic control mechanisms. 3rd ed. St. Louis: Elsevier Academic Press
44. Simoni M, Weinbauer GF, Gromoll J, Nieschlag E 1999 Role of FSH in male gonadal function. Ann Endocrinol (Paris) 60:102-106 (Pubitemid 29359899)
45. O'Donnell L, McLachlan RI, Wreford NG, de Kretser DM, Robertson DM 1996 Testosterone withdrawal promotes stage-specific detachment of round spermatids from the rat seminiferous epithelium. Biol Reprod 55:895-901 (Pubitemid 26304769)
46. O'Donnell L, Stanton PG, Bartles JR, Robertson DM 2000 Sertoli cell ectoplasmic specializations in the seminiferous epithelium of the testosterone-suppressed adult rat. Biol Reprod 63:99-108 (Pubitemid 30429390)
47. Muffly KE, Nazian SJ, Cameron DF 1994 Effects of follicle-stimulating hormone on the junction-related Sertoli cell cytoskeleton and daily sperm production in testosterone-treated hypophysectomized rats. Biol Reprod 51:158-166 (Pubitemid 24179234)
48. Siu MK, Wong CH, Lee WM, Cheng CY 2005 Sertoli-germ cell anchoring junction dynamics in the testis are regulated by an interplay of lipid and protein kinases. J Biol Chem 280:25029-25047 (Pubitemid 40934595)
49. Olive V, Bennett MJ, Walker JC, Ma C, Jiang I, Cordon-Cardo C, Li QJ, Lowe SW, Hannon GJ, He L 2009 miR-19 is a key oncogenic component of mir-17-92. Genes Dev 23:2839-2849
50. Kato M, Putta S, Wang M, Yuan H, Lanting L, Nair I, Gunn A, Nakagawa Y, Shimano H, Todorov I, Rossi JJ, Natarajan R 2009 TGF-β activates Akt kinase through a microRNA-dependent amplifying circuit targeting PTEN. Nat Cell Biol 11:881-889
51. Young JS, Guttman JA, Vaid KS, Vogl AW 2009 Tubulobulbar complexes are intercellular podosome-like structures that internalize intact intercellular junctions during epithelial remodeling events in the rat testis. Biol Reprod 80:162-174
52. Benmerah A, Bayrou M, Cerf-Bensussan N, Dautry-Varsat A 1999 Inhibition of clathrin-coated pit assembly by an Eps15 mutant. J Cell Sci 112 (Pt 9):1303-1311 (Pubitemid 29243453)
53. Sikand K, Slane SD, Shukla GC 2009 Intrinsic expression of host genes and intronic miRNAs in prostate carcinoma cells. Cancer Cell Int 9:21
54. Lui WY, Wong CH, Mruk DD, Cheng CY 2003 TGF-β3 regulates the blood-testis barrier dynamics via the p38 mitogen activated protein (MAP) kinase pathway: an in vivo study. Endocrinology 144:1139-1142 (Pubitemid 36428452)
55. Dupont J, Musnier A, Decourtye J, Boulo T, Lécureuil C, Guillou H, Valet S, Fouchécourt S, Pitetti JL, Nef S, Reiter E, Crépieux P 2010 FSH-stimulated PTEN activity accounts for the lack of FSH mitogenic effect in prepubertal rat Sertoli cells. Mol Cell Endocrinol 315:271-276
56. Mao YS, Yin HL 2007 Regulation of the actin cytoskeleton by phosphatidylinositol 4-phosphate 5 kinases. Pflugers Arch 455:5-18 (Pubitemid 47403983)
57. Trotman LC, Niki M, Dotan ZA, Koutcher JA, Di Cristofano A, Xiao A, Khoo AS, Roy-Burman P, Greenberg NM, Van Dyke T, Cordon-Cardo C, Pandolfi PP 2003 Pten dose dictates cancer progression in the prostate. PLoS Biol 1:E59
58. Rainey MA, George M, Ying G, Akakura R, Burgess DJ, Siefker E, Bargar T, Doglio L, Crawford SE, Todd GL, Govindarajan V, Hess RA, Band V, Naramura M, Band H 2010 The endocytic recycling regulator EHD1 is essential for spermatogenesis and male fertility in mice. BMC Dev Biol 10:37
59. Ribas J, Ni X, Haffner M, Wentzel EA, Salmasi AH, Chowdhury WH, Kudrolli TA, Yegnasubramanian S, Luo J, Rodriguez R, Mendell JT, Lupold SE 2009 miR-21: an androgen receptor-regulated microRNA that promotes hormone-dependent and hormone-independent prostate cancer growth. Cancer Res 69:7165-7169
60. Pan Q, Luo X, Toloubeydokhti T, Chegini N 2007 The expression profile of micro-RNA in endometrium and endometriosis and the influence of ovarian steroids on their expression. Mol Hum Reprod 13:797-806 (Pubitemid 350131353)
61. Maillot G, Lacroix-Triki M, Pierredon S, Gratadou L, Schmidt S, Bénès V, Roché H, Dalenc F, Auboeuf D, Millevoi S, Vagner S 2009 Widespread estrogen-dependent repression of microRNAs involved in breast tumor cell growth. Cancer Res 69:8332-8340
62. Schultz J, Lorenz P, Gross G, Ibrahim S, Kunz M 2008 MicroRNA let-7b targets important cell cycle molecules in malignant melanoma cells and interferes with anchorage-independent growth. Cell Res 18:549-557 (Pubitemid 351630945)
63. Yu Z, Wang C, Wang M, Li Z, Casimiro MC, Liu M, Wu K, Whittle J, Ju X, Hyslop T, McCue P, Pestell RG 2008 A cyclin D1/microRNA 17/20 regulatory feedback loop in control of breast cancer cell proliferation. J Cell Biol 182:509-517
64. Ji J, Zhao L, Budhu A, Forgues M, Jia HL, Qin LX, Ye QH, Yu J, Shi X, Tang ZY, Wang XW 2010 Let-7g targets collagen type I α2 and inhibits cell migration in hepatocellular carcinoma. J Hepatol 52:690-697
65. Müller DW, Bosserhoff AK 2008 Integrin β3 expression is regulated by let-7a miRNA in malignant melanoma. Oncogene 27:6698-6706
66. Salvi A, Sabelli C, Moncini S, Venturin M, Arici B, Riva P, Portolani N, Giulini SM, De Petro G, Barlati S 2009 MicroRNA-23b mediates urokinase and c-met downmodulation and a decreased migration of human hepatocellular carcinoma cells. FEBS J 276:2966-2982
67. Meng F, Henson R, Wehbe-Janek H, Ghoshal K, Jacob ST, Patel T 2007 MicroRNA-21 regulates expression of the PTEN tumor suppressor gene in human hepatocellular cancer. Gastroenterology 133:647-658 (Pubitemid 47187346)