The RNase III enzyme DROSHA is essential for MicroRNA production and spermatogenesis

Journal of Biological Chemistry

Volumn 287, Issue 30, 2012, Pages 25173-25190

  Wu, Qiuxia ^a   Song, Rui ^a   Ortogero, Nicole ^a   Zheng, Huili ^a   Evanoff, Ryan ^b   Small, Chris L ^b   Griswold, Michael D ^b   Namekawa, Satoshi H ^c,d   Royo, Helene ^e   Turner, James M ^e   Yan, Wei ^a  

^a UNIVERSITY OF NEVADA SCHOOL OF MEDICINE   (United States)

^b WASHINGTON STATE UNIVERSITY   (United States)

^c CINCINNATI CHILDREN'S HOSPITAL MEDICAL CENTER   (United States)

^d UNIVERSITY OF CINCINNATI COLLEGE OF MEDICINE   (United States)

^e NATIONAL INSTITUTE FOR MEDICAL RESEARCH   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

CRE-LOXP; DOUBLE-STRANDED RNA; KNOCK OUTS; MALE FERTILITY; MICROARRAY ANALYSIS; MICRORNAS; ROUND SPERMATID; SEX CHROMOSOMES; SMALL INTERFERING RNA; SMALL RNA; SPERMATOGENIC CELLS;

BIOSYNTHESIS; RNA;

ENZYMES;

CRE RECOMBINASE; DICER; MESSENGER RNA; MICRORNA; PROTEIN DROSHA; RIBONUCLEASE III; SMALL INTERFERING RNA; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; AZOOSPERMIA; CHROMOSOME INACTIVATION; CONTROLLED STUDY; DEPLETION; ENZYME ACTIVITY; GENE FUNCTION; GENE INACTIVATION; KNOCKOUT MOUSE; LOXP SITE; MALE; MALE INFERTILITY; MICROARRAY ANALYSIS; MOUSE; NONHUMAN; OLIGOTERATOZOOSPERMIA; PACHYTENE; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN FUNCTION; RNA SYNTHESIS; SEMEN ABNORMALITY; SEX CHROMOSOME; SPERMATID; SPERMATOCYTE; SPERMATOGENESIS; TESTIS; TRANSCRIPTOMICS;

ANIMALS; AZOOSPERMIA; DEAD-BOX RNA HELICASES; FERTILITY; MALE; MICE; MICE, KNOCKOUT; MICRORNAS; OLIGOSPERMIA; RIBONUCLEASE III; SPERMATIDS; SPERMATOCYTES; SPERMATOGENESIS; TESTIS;

EID: 84864085621     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M112.362053     Document Type: Article

References (87)

1. Clermont, Y. (1972) Kinetics of spermatogenesis in mammals. Seminiferous epithelium cycle and spermatogonial renewal. Physiol. Rev. 52, 198-236
2. Hermo, L., Pelletier, R. M., Cyr, D. G., and Smith, C. E. (2010) Surfing the wave, cycle, life history, and genes/proteins expressed by testicular germ cells. Part 1. Background to spermatogenesis, spermatogonia, and spermatocytes. Microsc. Res. Tech. 73, 241-278
3. Yan, W. (2009) Male infertility caused by spermiogenic defects. Lessons from gene knockouts. Mol. Cell. Endocrinol. 306, 24-32
4. Idler, R. K., and Yan, W. (2012) Control of messenger RNA fate by RNAbinding proteins. An emphasis on mammalian spermatogenesis. J. Androl. 33, 309-337
5. Bettegowda, A., and Wilkinson, M. F. (2010) Transcription and post-transcriptional regulation of spermatogenesis. Philos. Trans. R. Soc. Lond. B Biol. Sci. 365, 1637-1651
6. He, Z., Kokkinaki, M., Pant, D., Gallicano, G. I., and Dym, M. (2009) Small RNA molecules in the regulation of spermatogenesis. Reproduction 137, 901-911
7. Paronetto, M. P., and Sette, C. (2010) Role of RNA-binding proteins in mammalian spermatogenesis. Int. J. Androl. 33, 2-12
8. Braun, R. E. (1998) Post-transcriptional control of gene expression during spermatogenesis. Semin. Cell Dev. Biol. 9, 483-489
9. Rajender, S., Avery, K., and Agarwal, A. (2011) Epigenetics, spermatogenesis, and male infertility. Mutat. Res. 727, 62-71
10. Trasler, J. M. (2009) Epigenetics in spermatogenesis. Mol. Cell. Endocrinol. 306, 33-36
11. Djuranovic, S., Nahvi, A., and Green, R. (2011) A parsimonious model for gene regulation by miRNAs. Science 331, 550-553
12. Bartel, D. P. (2009) MicroRNAs. Target recognition and regulatory functions. Cell 136, 215-233
13. Bartel, D. P., and Chen, C. Z. (2004) Micromanagers of gene expression. The potentially widespread influence of metazoan microRNAs. Nat. Rev. Genet. 5, 396-400 (Pubitemid 38529411)
14. Yang, J. S., and Lai, E. C. (2011) Alternative miRNA biogenesis pathways and the interpretation of core miRNA pathway mutants. Mol. Cell 43, 892-903
15. Murchison, E. P., and Hannon, G. J. (2004) miRNAs on the move. miRNA biogenesis and the RNAi machinery. Curr. Opin. Cell Biol. 16, 223-229 (Pubitemid 38610401)
16. Meister, G. (2007) miRNAs get an early start on translational silencing. Cell 131, 25-28
17. Bartel, D. P. (2004) MicroRNAs. Genomics, biogenesis, mechanism, and function. Cell 116, 281-297
18. Rissland, O. S., Hong, S. J., and Bartel, D. P. (2011) MicroRNA destabilization enables dynamic regulation of the miR-16 family in response to cell cycle changes. Mol. Cell 43, 993-1004
19. Schnall-Levin, M., Rissland, O. S., Johnston, W. K., Perrimon, N., Bartel, D. P., and Berger, B. (2011) Unusually effective microRNA targeting within repeat-rich coding regions of mammalian mRNAs. Genome Res. 21, 1395-1403
20. Lee, Y., Han, J., Yeom, K. H., Jin, H., and Kim, V. N. (2006) Drosha in primary microRNA processing. Cold Spring Harbor Symp. Quant. Biol. 71, 51-57
21. Tomari, Y., and Zamore, P. D. (2005) MicroRNA biogenesis. drosha can't cut it without a partner. Curr. Biol. 15, R61-R64
22. Carthew, R. W., and Sontheimer, E. J. (2009) Origins and mechanisms of miRNAs and siRNAs. Cell 136, 642-655
23. Jaskiewicz, L., and Filipowicz, W. (2008) Role of Dicer in post-transcriptional RNA silencing. Curr. Top. Microbiol. Immunol. 320, 77-97
24. Bernstein, E., Kim, S. Y., Carmell, M. A., Murchison, E. P., Alcorn, H., Li, M. Z., Mills, A. A., Elledge, S. J., Anderson, K. V., and Hannon, G. J. (2003) Dicer is essential for mouse development. Nat. Genet. 35, 215-217 (Pubitemid 37363172)
25. da Costa Martins, P. A., Bourajjaj, M., Gladka, M., Kortland, M., van Oort, R. J., Pinto, Y. M., Molkentin, J. D., and De Windt, L. J. (2008) Conditional dicer gene deletion in the postnatal myocardium provokes spontaneous cardiac remodeling. Circulation 118, 1567-1576
26. Davis, T. H., Cuellar, T. L., Koch, S. M., Barker, A. J., Harfe, B. D., McManus, M. T., and Ullian, E. M. (2008) Conditional loss of Dicer disrupts cellular and tissue morphogenesis in the cortex and hippocampus. J. Neurosci. 28, 4322-4330
27. Frezzetti, D., Reale, C., Calì, G., Nitsch, L., Fagman, H., Nilsson, O., Scarfò, M., De Vita, G., and Di Lauro, R. (2011) The microRNA-processing enzyme Dicer is essential for thyroid function. PLoS One 6, e27648
28. Georgi, S. A., and Reh, T. A. (2010) Dicer is required for the transition from early to late progenitor state in the developing mouse retina. J. Neurosci. 30, 4048-4061
29. Georgi, S. A., and Reh, T. A. (2011) Dicer is required for the maintenance of notch signaling and gliogenic competence during mouse retinal development. Dev. Neurobiol. 71, 1153-1169
30. Harfe, B. D., McManus, M. T., Mansfield, J. H., Hornstein, E., and Tabin, C. J. (2005) The RNase III enzyme Dicer is required for morphogenesis but not patterning of the vertebrate limb. Proc. Natl. Acad. Sci. U.S.A. 102, 10898-10903 (Pubitemid 41105964)
31. Ho, J. J., and Marsden, P. A. (2008) Dicer cuts the kidney. J. Am. Soc. Nephrol. 19, 2043-2046
32. Huang, T., Liu, Y., Huang, M., Zhao, X., and Cheng, L. (2010) Wnt1-cremediated conditional loss of Dicer results in malformation of the midbrain and cerebellum and failure of neural crest and dopaminergic differentiation in mice. J. Mol. Cell Biol. 2, 152-163
33. Huang, T. C., Saharabuddhe, N. A., Kim, M. S., Getnet, D., Yang, Y., Peterson, J. M., Ghosh, B., Chaerkady, R., Leach, S. D., Marchionni, L., Wong, G. W., and Pandey, A. (2012) Regulation of lipid metabolism by dicer revealed through SILAC mice. J. Proteome Res. 11, 2193-2205
34. Kanellopoulou, C., Muljo, S. A., Kung, A. L., Ganesan, S., Drapkin, R., Jenuwein, T., Livingston, D. M., and Rajewsky, K. (2005) Dicer-deficient mouse embryonic stem cells are defective in differentiation and centromeric silencing. Genes Dev. 19, 489-501 (Pubitemid 40256280)
35. Kim, G. J., Georg, I., Scherthan, H., Merkenschlager, M., Guillou, F., Scherer, G., and Barrionuevo, F. (2010) Dicer is required for Sertoli cell function and survival. Int. J. Dev. Biol. 54, 867-875
36. Lei, L., Jin, S., Gonzalez, G., Behringer, R. R., and Woodruff, T. K. (2010) The regulatory role of Dicer in folliculogenesis in mice. Mol. Cell. Endocrinol. 315, 63-73
37. Meng, D. M., Wang, L., Xu, J. R., Yan, S. L., Zhou, L., and Mi, Q. S. (2011) Fabp4-Cre-mediated deletion of the miRNA-processing enzyme Dicer causes mouse embryonic lethality. Acta Diabetologia, in press
38. Mudhasani, R., Puri, V., Hoover, K., Czech, M. P., Imbalzano, A. N., and Jones, S. N. (2011) Dicer is required for the formation of white but not brown adipose tissue. J. Cell Physiol. 226, 1399-1406
39. Muljo, S. A., Ansel, K. M., Kanellopoulou, C., Livingston, D. M., Rao, A., and Rajewsky, K. (2005) Aberrant T cell differentiation in the absence of Dicer. J. Exp. Med. 202, 261-269 (Pubitemid 41043822)
40. Nagaraja, A. K., Andreu-Vieyra, C., Franco, H. L., Ma, L., Chen, R., Han, D. Y., Zhu, H., Agno, J. E., Gunaratne, P. H., DeMayo, F. J., and Matzuk, M. M. (2008) Deletion of Dicer in somatic cells of the female reproductive tract causes sterility. Mol. Endocrinol. 22, 2336-2352
41. Nakamura, M., Ando, R., Nakazawa, T., Yudazono, T., Tsutsumi, N., Hatanaka, N., Ohgake, T., Hanaoka, F., and Eki, T. (2007) Dicer-related drh-3 gene functions in germ line development by maintenance of chromosomal integrity in Caenorhabditis elegans. Genes Cells 12, 997-1010 (Pubitemid 47365672)
42. Pan, Y., Balazs, L., Tigyi, G., and Yue, J. (2011) Conditional deletion of Dicer in vascular smooth muscle cells leads to the developmental delay and embryonic mortality. Biochem. Biophys. Res. Commun. 408, 369-374
43. Saal, S., and Harvey, S. J. (2009) MicroRNAs and the kidney. Coming of age. Curr. Opin. Nephrol. Hypertens 18, 317-323
44. Sequeira-Lopez, M. L., Weatherford, E. T., Borges, G. R., Monteagudo, M. C., Pentz, E. S., Harfe, B. D., Carretero, O., Sigmund, C. D., and Gomez, R. A. (2010) The microRNA-processing enzyme Dicer maintains juxtaglomerular cells. J. Am. Soc. Nephrol. 21, 460-467
45. Tang, K. F., Wang, Y., Wang, P., Chen, M., Chen, Y., Hu, H. D., Hu, P., Wang, B., Yang, W., and Ren, H. (2007) Up-regulation of PHLDA2 in Dicer knockdown HEK293 cells. Biochim. Biophys. Acta 1770, 820-825 (Pubitemid 46420627)
46. Wang, Y., Medvid, R., Melton, C., Jaenisch, R., and Blelloch, R. (2007) DGCR8 is essential for microRNA biogenesis and silencing of embryonic stem cell self-renewal. Nat. Genet. 39, 380-385 (Pubitemid 46328490)
47. Suh, N., Baehner, L., Moltzahn, F., Melton, C., Shenoy, A., Chen, J., and Blelloch, R. (2010) MicroRNA function is globally suppressed in mouse oocytes and early embryos. Curr. Biol. 20, 271-277
48. Ma, J., Flemr, M., Stein, P., Berninger, P., Malik, R., Zavolan, M., Svoboda, P., and Schultz, R. M. (2010) MicroRNA activity is suppressed in mouse oocytes. Curr. Biol. 20, 265-270
49. Korhonen, H. M., Meikar, O., Yadav, R. P., Papaioannou, M. D., Romero, Y., Da Ros, M., Herrera, P. L., Toppari, J., Nef, S., and Kotaja, N. (2011) Dicer is required for haploid male germ cell differentiation in mice. PLoS One 6, e24821
50. Romero, Y., Meikar, O., Papaioannou, M. D., Conne, B., Grey, C., Weier, M., Pralong, F., De Massy, B., Kaessmann, H., Vassalli, J. D., Kotaja, N., and Nef, S. (2011) Dicer1 depletion in male germ cells leads to infertility due to cumulative meiotic and spermiogenic defects. PLoS One 6, e25241
51. Huang, C. C., and Yao, H. H. (2010) Inactivation of Dicer1 in steroidogenic factor 1-positive cells reveals tissue-specific requirement for Dicer1 in adrenal, testis, and ovary. BMC Dev. Biol. 10, 66
52. Maatouk, D. M., Loveland, K. L., McManus, M. T., Moore, K., and Harfe, B. D. (2008) Dicer1 is required for differentiation of the mouse male germ line. Biol. Reprod. 79, 696-703
53. Hayashi, K., Chuva de Sousa Lopes, S. M., Kaneda, M., Tang, F., Hajkova, P., Lao, K., O'Carroll, D., Das, P. P., Tarakhovsky, A., Miska, E. A., and Surani, M. A. (2008) MicroRNA biogenesis is required for mouse primordial germ cell development and spermatogenesis. PLoS One 3, e1738
54. Song, R., Hennig, G. W., Wu, Q., Jose, C., Zheng, H., and Yan, W. (2011) Male germ cells express abundant endogenous siRNAs. Proc. Natl. Acad. Sci. U.S.A. 108, 13159-13164
55. Aoki, K., and Taketo, M. M. (2008) Tissue-specific transgenic, conditional knock-out and knock-in mice of genes in the canonical Wnt signaling pathway. Methods Mol. Biol. 468, 307-331
56. Wang, X. (2009) Cre transgenic mouse lines. Methods Mol. Biol. 561, 265-273
57. Yu, Y., and Zuo, J. (2009) The practical use of Cre and loxP technologies in mouse auditory research. Methods Mol. Biol. 493, 87-102
58. Chong, M. M., Rasmussen, J. P., Rudensky, A. Y., Rundensky, A. Y., and Littman, D. R. (2008) The RNase III enzyme Drosha is critical in T cells for preventing lethal inflammatory disease. J. Exp. Med. 205, 2005-2017
59. Sadate-Ngatchou, P. I., Payne, C. J., Dearth, A. T., and Braun, R. E. (2008) Cre recombinase activity specific to postnatal, premeiotic male germ cells in transgenic mice. Genesis 46, 738-742
60. Muzumdar, M. D., Tasic, B., Miyamichi, K., Li, L., and Luo, L. (2007) A global double-fluorescent Cre reporter mouse. Genesis 45, 593-605 (Pubitemid 350013057)
61. Bellvé, A. R. (1993) Purification, culture, and fractionation of spermatogenic cells. Methods Enzymol. 225, 84-113
62. Song, R., Ro, S., Michaels, J. D., Park, C., McCarrey, J. R., and Yan, W. (2009) Many X-linked microRNAs escape meiotic sex chromosome inactivation. Nat. Genet. 41, 488-493
63. Zheng, H., Stratton, C. J., Morozumi, K., Jin, J., Yanagimachi, R., and Yan, W. (2007) Lack of Spem1 causes aberrant cytoplasm removal, sperm deformation, and male infertility. Proc. Natl. Acad. Sci. U.S.A. 104, 6852-6857 (Pubitemid 47175590)
64. Mituyama, T., Yamada, K., Hattori, E., Okida, H., Ono, Y., Terai, G., Yoshizawa, A., Komori, T., and Asai, K. (2009) The functional RNA database 3.0. Databases to support mining and annotation of functional RNAs. Nucleic Acids Res. 37, D89-D92
65. Marioni, J. C., Mason, C. E., Mane, S. M., Stephens, M., and Gilad, Y. (2008) RNA-seq. An assessment of technical reproducibility and comparison with gene expression arrays. Genome Res. 18, 1509-1517
66. Hogarth, C. A., Mitchell, D., Evanoff, R., Small, C., and Griswold, M. (2011) Identification and expression of potential regulators of the mammalian mitotic-to-meiotic transition. Biol. Reprod. 84, 34-42
67. Royo, H., Polikiewicz, G., Mahadevaiah, S. K., Prosser, H., Mitchell, M., Bradley, A., de Rooij, D. G., Burgoyne, P. S., and Turner, J. M. (2010) Evidence that meiotic sex chromosome inactivation is essential for male fertility. Curr. Biol. 20, 2117-2123
68. Turner, J. M., Mahadevaiah, S. K., Ellis, P. J., Mitchell, M. J., and Burgoyne, P. S. (2006) Pachytene asynapsis drives meiotic sex chromosome inactivation and leads to substantial postmeiotic repression in spermatids. Dev. Cell 10, 521-529
69. Namekawa, S. H., and Lee, J. T. (2011) Detection of nascent RNA, singlecopy DNA and protein localization by immuno-FISH in mouse germ cells and preimplantation embryos. Nat. Protoc. 6, 270-284
70. McCarrey, J. R., Berg, W. M., Paragioudakis, S. J., Zhang, P. L., Dilworth, D. D., Arnold, B. L., and Rossi, J. J. (1992) Differential transcription of Pgk genes during spermatogenesis in the mouse. Dev. Biol. 154, 160-168
71. Ro, S., Park, C., Sanders, K. M., McCarrey, J. R., and Yan, W. (2007) Cloning and expression profiling of testis-expressed microRNAs. Dev. Biol. 311, 592-602 (Pubitemid 350064371)
72. Wu, H., Xu, H., Miraglia, L. J., and Crooke, S. T. (2000) Human RNase III is a 160-kDa protein involved in preribosomal RNA processing. J. Biol. Chem. 275, 36957-36965 (Pubitemid 32002110)
73. Kim, V. N., Han, J., and Siomi, M. C. (2009) Biogenesis of small RNAs in animals. Nat. Rev. Mol. Cell Biol. 10, 126-139
74. Shukla, K. K., Mahdi, A. A., and Rajender, S. (2012) Apoptosis, spermatogenesis, and male infertility. Front. Biosci. (Elite Ed) 4, 746-754
75. Print, C. G., and Loveland, K. L. (2000) Germ cell suicide. New insights into apoptosis during spermatogenesis. BioEssays 22, 423-430 (Pubitemid 30308268)
76. Yang, J., Medvedev, S., Yu, J., Tang, L. C., Agno, J. E., Matzuk, M. M., Schultz, R. M., and Hecht, N. B. (2005) Absence of the DNA-/RNA-binding protein MSY2 results in male and female infertility. Proc. Natl. Acad. Sci. U.S.A. 102, 5755-5760 (Pubitemid 40559632)
77. Guo, H., Ingolia, N. T., Weissman, J. S., and Bartel, D. P. (2010) Mammalian microRNAs predominantly act to decrease target mRNA levels. Nature 466, 835-840
78. Namekawa, S. H., Park, P. J., Zhang, L. F., Shima, J. E., McCarrey, J. R., Griswold, M. D., and Lee, J. T. (2006) Postmeiotic sex chromatin in the male germ line of mice. Curr. Biol. 16, 660-667
79. Turner, J. M. (2007) Meiotic sex chromosome inactivation. Development 134, 1823-1831
80. Namekawa, S. H., VandeBerg, J. L., McCarrey, J. R., and Lee, J. T. (2007) Sex chromosome silencing in the marsupial male germ line. Proc. Natl.Acad. Sci. U.S.A. 104, 9730-9735 (Pubitemid 47175335)
81. Kaneko, H., Dridi, S., Tarallo, V., Gelfand, B. D., Fowler, B. J., Cho, W. G., Kleinman, M. E., Ponicsan, S. L., Hauswirth, W. W., Chiodo, V. A., Karikó, K., Yoo, J. W., Lee, D. K., Hadziahmetovic, M., Song, Y., Misra, S., Chaudhuri, G., Buaas, F. W., Braun, R. E., Hinton, D. R., Zhang, Q., Grossniklaus, H. E., Provis, J. M., Madigan, M. C., Milam, A. H., Justice, N. L., Albuquerque, R. J., Blandford, A. D., Bogdanovich, S., Hirano, Y., Witta, J., Fuchs, E., Littman, D. R., Ambati, B. K., Rudin, C. M., Chong, M. M., Provost, P., Kugel, J. F., Goodrich, J. A., Dunaief, J. L., Baffi, J. Z., and Ambati, J. (2011) DICER1 deficit induces Alu RNA toxicity in age-related macular degeneration. Nature 471, 325-330
82. Murchison, E. P., Stein, P., Xuan, Z., Pan, H., Zhang, M. Q., Schultz, R. M., and Hannon, G. J. (2007) Critical roles for Dicer in the female germ line. Genes Dev. 21, 682-693 (Pubitemid 46440290)
83. Lomelí, H., Ramos-Mejía, V., Gertsenstein, M., Lobe, C. G., and Nagy, A. (2000) Targeted insertion of Cre recombinase into the TNAP gene. Excision in primordial germ cells. Genesis 26, 116-117 (Pubitemid 30158092)
84. Nakahara, K., and Carthew, R. W. (2004) Expanding roles for miRNAs and siRNAs in cell regulation. Curr. Opin. Cell Biol. 16, 127-133 (Pubitemid 38757288)
85. Vasudevan, S., Tong, Y., and Steitz, J. A. (2007) Switching from repression to activation. MicroRNAs can up-regulate translation. Science 318, 1931-1934
86. Suh, N., and Blelloch, R. (2011) Small RNAs in early mammalian development. From gametes to gastrulation. Development 138, 1653-1661
87. Tam, O. H., Aravin, A. A., Stein, P., Girard, A., Murchison, E. P., Cheloufi, S., Hodges, E., Anger, M., Sachidanandam, R., Schultz, R. M., and Hannon, G. J. (2008) Pseudogene-derived small interfering RNAs regulate gene expression in mouse oocytes. Nature 453, 534-538 (Pubitemid 351733314)