DOI QR코드

DOI QR Code

Functions of PIWI proteins in spermatogenesis

  • Bak, Chong-Won (Fertility Center of Gangnam Medical Center, CHA University College of Medicine) ;
  • Yoon, Tae-Ki (Fertility Center of Gangnam Medical Center, CHA University College of Medicine) ;
  • Choi, Young-Sok (Fertility Center of Gangnam Medical Center, CHA University College of Medicine)
  • Received : 2011.05.03
  • Accepted : 2011.06.03
  • Published : 2011.06.30

Abstract

Recently, a significant understanding of the molecular mechanisms regulating spermatogenesis has been achieved utilizing small RNA molecules (small RNAs), including small interfering RNAs (siRNAs), microRNAs (miRNAs), and Piwi-interacting RNAs (piRNAs) which emerged as important regulators of gene expression at the post-transcriptional or translation level. piRNAs are only present in pachytene spermatocytes and round spermatids, whereas miRNAs are expressed abundantly in male germ cells throughout spermatogenesis. This review is aimed at providing a glimpse of piRNAs and their interacting family proteins such as PIWIL1, PIWIL2, and PIWIL4 in spermatogenesis.

References

  1. Baccetti B, Afzelius BA. The biology of the sperm cell. Monogr Dev Biol 1976;(10):1-254.
  2. Eddy EM. Male germ cell gene expression. Recent Prog Horm Res 2002;57:103-28. https://doi.org/10.1210/rp.57.1.103
  3. Plasterk RH. Micro RNAs in animal development. Cell 2006;124:877-81. https://doi.org/10.1016/j.cell.2006.02.030
  4. Tolia NH, Joshua-Tor L. Slicer and the argonautes. Nat Chem Biol 2007;3:36-43. https://doi.org/10.1038/nchembio848
  5. Slotkin RK, Martienssen R. Transposable elements and the epigenetic regulation of the genome. Nat Rev Genet 2007;8:272-85.
  6. Lander ES, Linton LM, Birren B, Nusbaum C, Zody MC, Baldwin J, et al. Initial sequencing and analysis of the human genome. Nature 2001;409:860-921. https://doi.org/10.1038/35057062
  7. Mouse Genome Sequencing Consortium, Waterston RH, Lindblad-Toh K, Birney E, Rogers J, Abril JF, et al. Initial sequencing and comparative analysis of the mouse genome. Nature 2002;420:520-62. https://doi.org/10.1038/nature01262
  8. Kazazian HH Jr. Mobile elements: drivers of genome evolution. Science 2004;303:1626-32. https://doi.org/10.1126/science.1089670
  9. Li E, Bestor TH, Jaenisch R. Targeted mutation of the DNA methyltransferase gene results in embryonic lethality. Cell 1992;69:915-26. https://doi.org/10.1016/0092-8674(92)90611-F
  10. Walsh CP, Chaillet JR, Bestor TH. Transcription of IAP endogenous retroviruses is constrained by cytosine methylation. Nat Genet 1998;20:116-7. https://doi.org/10.1038/2413
  11. Bourc'his D, Bestor TH. Meiotic catastrophe and retrotransposon reactivation in male germ cells lacking Dnmt3L. Nature 2004;431:96-9. https://doi.org/10.1038/nature02886
  12. Aravin A, Gaidatzis D, Pfeffer S, Lagos-Quintana M, Landgraf P, Iovino N, et al. A novel class of small RNAs bind to MILI protein in mouse testes. Nature 2006;442:203-7.
  13. Girard A, Sachidanandam R, Hannon GJ, Carmell MA. A germline-specific class of small RNAs binds mammalian Piwi proteins. Nature 2006;442:199-202.
  14. Grivna ST, Beyret E, Wang Z, Lin H. A novel class of small RNAs in mouse spermatogenic cells. Genes Dev 2006;20:1709-14. https://doi.org/10.1101/gad.1434406
  15. Watanabe T, Takeda A, Tsukiyama T, Mise K, Okuno T, Sasaki H, et al. Identification and characterization of two novel classes of small RNAs in the mouse germline: retrotransposon-derived siRNAs in oocytes and germline small RNAs in testes. Genes Dev 2006;20:1732-43. https://doi.org/10.1101/gad.1425706
  16. Grivna ST, Pyhtila B, Lin H. MIWI associates with translational machinery and PIWI-interacting RNAs (piRNAs) in regulating spermatogenesis. Proc Natl Acad Sci U S A 2006;103:13415-20. https://doi.org/10.1073/pnas.0605506103
  17. Lau NC, Seto AG, Kim J, Kuramochi-Miyagawa S, Nakano T, Bartel DP, et al. Characterization of the piRNA complex from rat testes. Science 2006;313:363-7. https://doi.org/10.1126/science.1130164
  18. Klattenhoff C, Theurkauf W. Biogenesis and germline functions of piRNAs. Development 2008;135:3-9.
  19. Betel D, Sheridan R, Marks DS, Sander C. Computational analysis of mouse piRNA sequence and biogenesis. PLoS Comput Biol 2007;3:e222. https://doi.org/10.1371/journal.pcbi.0030222
  20. Rongo C, Lehmann R. Regulated synthesis, transport and assembly of the Drosophila germ plasm. Trends Genet 1996;12:102-9. https://doi.org/10.1016/0168-9525(96)81421-1
  21. Cox DN, Chao A, Baker J, Chang L, Qiao D, Lin H. A novel class of evolutionarily conserved genes defined by piwi are essential for stem cell self-renewal. Genes Dev 1998;12:3715-27. https://doi.org/10.1101/gad.12.23.3715
  22. King FJ, Szakmary A, Cox DN, Lin H. Yb modulates the divisions of both germline and somatic stem cells through piwi- and hhmediated mechanisms in the Drosophila ovary. Mol Cell 2001;7:497-508. https://doi.org/10.1016/S1097-2765(01)00197-6
  23. Deng W, Lin H. miwi, a murine homolog of piwi, encodes a cytoplasmic protein essential for spermatogenesis. Dev Cell 2002;2:819-30. https://doi.org/10.1016/S1534-5807(02)00165-X
  24. Kimura T, Ito C, Watanabe S, Takahashi T, Ikawa M, Yomogida K, et al. Mouse germ cell-less as an essential component for nuclear integrity. Mol Cell Biol 2003;23:1304-15. https://doi.org/10.1128/MCB.23.4.1304-1315.2003
  25. Tanaka SS, Toyooka Y, Akasu R, Katoh-Fukui Y, Nakahara Y, Suzuki R, et al. The mouse homolog of Drosophila Vasa is required for the development of male germ cells. Genes Dev 2000;14:841-53.
  26. Lin H, Spradling AC. A novel group of pumilio mutations affects the asymmetric division of germline stem cells in the Drosophila ovary. Development 1997;124:2463-76.
  27. Vagin VV, Sigova A, Li C, Seitz H, Gvozdev V, Zamore PD. A distinct small RNA pathway silences selfish genetic elements in the germline. Science 2006;313:320-4. https://doi.org/10.1126/science.1129333
  28. Gunawardane LS, Saito K, Nishida KM, Miyoshi K, Kawamura Y, Nagami T, et al. A slicer-mediated mechanism for repeat-associated siRNA 5' end formation in Drosophila. Science 2007;315:1587-90. https://doi.org/10.1126/science.1140494
  29. Brennecke J, Aravin AA, Stark A, Dus M, Kellis M, Sachidanandam R, et al. Discrete small RNA-generating loci as master regulators of transposon activity in Drosophila. Cell 2007;128:1089-103. https://doi.org/10.1016/j.cell.2007.01.043
  30. Lin H. piRNAs in the germ line. Science 2007;316:397. https://doi.org/10.1126/science.1137543
  31. Aravin AA, Sachidanandam R, Girard A, Fejes-Toth K, Hannon GJ. Developmentally regulated piRNA clusters implicate MILI in transposon control. Science 2007;316:744-7. https://doi.org/10.1126/science.1142612
  32. Carmell MA, Girard A, van de Kant HJ, Bourc'his D, Bestor TH, de Rooij DG, et al. MIWI2 is essential for spermatogenesis and repression of transposons in the mouse male germline. Dev Cell 2007;12:503-14. https://doi.org/10.1016/j.devcel.2007.03.001
  33. Hayashi K, Chuva de Sousa Lopes SM, Kaneda M, Tang F, Hajkova P, Lao K, et al. MicroRNA biogenesis is required for mouse primordial germ cell development and spermatogenesis. PLoS One 2008;3:e1738. https://doi.org/10.1371/journal.pone.0001738
  34. Reddien PW, Oviedo NJ, Jennings JR, Jenkin JC, Sanchez Alvarado A. SMEDWI-2 is a PIWI-like protein that regulates planarian stem cells. Science 2005;310:1327-30. https://doi.org/10.1126/science.1116110
  35. Russell LD, Ettlin RA, Sinha-Hikim AP, Clegg ED. Histological and histopathological evaluation of the testis. 1st ed. Clear- water: Cache River Press; 1990.
  36. Kuramochi-Miyagawa S, Kimura T, Yomogida K, Kuroiwa A, Tadokoro Y, Fujita Y, et al. Two mouse piwi-related genes: miwi and mili. Mech Dev 2001;108:121-33. https://doi.org/10.1016/S0925-4773(01)00499-3
  37. Aravin AA, Sachidanandam R, Bourc'his D, Schaefer C, Pezic D, Toth KF, et al. A piRNA pathway primed by individual transposons is linked to de novo DNA methylation in mice. Mol Cell 2008;31:785-99. https://doi.org/10.1016/j.molcel.2008.09.003
  38. Kuramochi-Miyagawa S, Watanabe T, Gotoh K, Totoki Y, Toyoda A, Ikawa M, et al. DNA methylation of retrotransposon genes is regulated by Piwi family members MILI and MIWI2 in murine fetal testes. Genes Dev 2008;22:908-17. https://doi.org/10.1101/gad.1640708
  39. Sasaki T, Shiohama A, Minoshima S, Shimizu N. Identification of eight members of the Argonaute family in the human genome small star, filled. Genomics 2003;82:323-30. https://doi.org/10.1016/S0888-7543(03)00129-0
  40. Zheng K, Xiol J, Reuter M, Eckardt S, Leu NA, McLaughlin KJ, et al. Mouse MOV10L1 associates with Piwi proteins and is an essential component of the Piwi-interacting RNA (piRNA) pathway. Proc Natl Acad Sci U S A 2010;107:11841-6. https://doi.org/10.1073/pnas.1003953107
  41. Tanner NK, Linder P. DExD/H box RNA helicases: from generic motors to specific dissociation functions. Mol Cell 2001;8:251-62. https://doi.org/10.1016/S1097-2765(01)00329-X
  42. Tomari Y, Du T, Haley B, Schwarz DS, Bennett R, Cook HA, et al. RISC assembly defects in the Drosophila RNAi mutant armitage. Cell 2004;116:831-41. https://doi.org/10.1016/S0092-8674(04)00218-1
  43. Shoji M, Tanaka T, Hosokawa M, Reuter M, Stark A, Kato Y, et al. The TDRD9-MIWI2 complex is essential for piRNA-mediated retrotransposon silencing in the mouse male germline. Dev Cell 2009;17:775-87. https://doi.org/10.1016/j.devcel.2009.10.012
  44. Reuter M, Chuma S, Tanaka T, Franz T, Stark A, Pillai RS. Loss of the Mili-interacting Tudor domain-containing protein-1 activates transposons and alters the Mili-associated small RNA profile. Nat Struct Mol Biol 2009;16:639-46. https://doi.org/10.1038/nsmb.1615
  45. Vagin VV, Wohlschlegel J, Qu J, Jonsson Z, Huang X, Chuma S, et al. Proteomic analysis of murine Piwi proteins reveals a role for arginine methylation in specifying interaction with Tudor family members. Genes Dev 2009;23:1749-62. https://doi.org/10.1101/gad.1814809
  46. Wang J, Saxe JP, Tanaka T, Chuma S, Lin H. Mili interacts with tudor domain-containing protein 1 in regulating spermatogenesis. Curr Biol 2009;19:640-4. https://doi.org/10.1016/j.cub.2009.02.061
  47. Wang G, Reinke V. A C. elegans Piwi, PRG-1, regulates 21U-RNAs during spermatogenesis. Curr Biol 2008;18:861-7. https://doi.org/10.1016/j.cub.2008.05.009
  48. Batista PJ, Ruby JG, Claycomb JM, Chiang R, Fahlgren N, Kasschau KD, et al. PRG-1 and 21U-RNAs interact to form the piRNA complex required for fertility in C. elegans. Mol Cell 2008;31:67-78. https://doi.org/10.1016/j.molcel.2008.06.002
  49. Conine CC, Batista PJ, Gu W, Claycomb JM, Chaves DA, Shirayama M, et al. Argonautes ALG-3 and ALG-4 are required for spermatogenesis-specific 26G-RNAs and thermotolerant sperm in Caenorhabditis elegans. Proc Natl Acad Sci U S A 2010;107:3588-93. https://doi.org/10.1073/pnas.0911685107
  50. Iguchi N, Xu M, Hori T, Hecht NB. Noncoding RNAs of the mammalian testis: the meiotic transcripts Nct1 and Nct2 encode piRNAs. Ann N Y Acad Sci 2007;1120:84-94. https://doi.org/10.1196/annals.1411.002
  51. Xu M, You Y, Hunsicker P, Hori T, Small C, Griswold MD, et al. Mice deficient for a small cluster of Piwi-interacting RNAs implicate Piwi-interacting RNAs in transposon control. Biol Reprod 2008;79:51-7. https://doi.org/10.1095/biolreprod.108.068072
  52. Kuramochi-Miyagawa S, Kimura T, Ijiri TW, Isobe T, Asada N, Fujita Y, et al. Mili, a mammalian member of piwi family gene, is essential for spermatogenesis. Development 2004;131:839-49. https://doi.org/10.1242/dev.00973
  53. Thomson T, Lin H. The biogenesis and function of PIWI proteins and piRNAs: progress and prospect. Annu Rev Cell Dev Biol 2009;25:355-76. https://doi.org/10.1146/annurev.cellbio.24.110707.175327
  54. Tushir JS, Zamore PD, Zhang Z. SnapShot: mouse piRNAs, PIWI proteins, and the ping-pong cycle. Cell 2009;139: 830-830.e1. https://doi.org/10.1016/j.cell.2009.10.042