PIWI proteins are dispensable for mouse somatic development and reprogramming of fibroblasts into pluripotent stem cells

PLoS ONE

Volumn 9, Issue 9, 2014, Pages

  Cheng, Ee Chun ^a   Kang, Dongwan ^b   Wang, Zhong ^b   Lin, Haifan ^a  

^a YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b LAWRENCE BERKELEY NATIONAL LABORATORY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

OCTAMER TRANSCRIPTION FACTOR 4; PIWI PROTEIN; TRANSCRIPTION FACTOR NANOG; TRANSCRIPTION FACTOR SOX2; ARGONAUTE PROTEIN; PIWIL1 PROTEIN, MOUSE; PIWIL2 PROTEIN, MOUSE; PIWIL4 PROTEIN, MOUSE;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; CONTROLLED STUDY; EMBRYO; EMBRYONIC STEM CELL; FEMALE; FIBROBLAST; GENE; GENE EXPRESSION PROFILING; GENE INACTIVATION; GERMLINE STEM CELL; HUMAN; HUMAN CELL; MALE; MILI GENE; MIWI GENE; MIWI2 GENE; MOUSE; NONHUMAN; NUCLEAR REPROGRAMMING; NUCLEOTIDE SEQUENCE; PHYSICAL DEVELOPMENT; PLURIPOTENT STEM CELL; UNINDEXED SEQUENCE; ANIMAL; CELL DIFFERENTIATION; CULTURE TECHNIQUE; CYTOLOGY; GENETICS; METABOLISM; PHYSIOLOGY;

ANIMALS; ARGONAUTE PROTEINS; CELL CULTURE TECHNIQUES; CELL DIFFERENTIATION; CELLULAR REPROGRAMMING; EMBRYONIC STEM CELLS; FIBROBLASTS; GENE KNOCKOUT TECHNIQUES; MICE; PLURIPOTENT STEM CELLS;

EID: 84907203613     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0097821     Document Type: Article

References (57)

1. Yabuta Y, Kurimoto K, Ohinata Y, Seki Y, Saitou M (2006) Gene expression dynamics during germline specification in mice identified by quantitative singlecell gene expression profiling. Biol Reprod 75: 705-716.
2. Matzuk MM (2009) LIN28 lets BLIMP1 take the right course. Dev Cell 17: 160-161.
3. Seydoux G, Braun RE (2006) Pathway to totipotency: lessons from germ cells. Cell 127: 891-904.
4. Chia NY, Chan YS, Feng B, Lu X, Orlov YL, et al. (2010) A genome-wide RNAi screen reveals determinants of human embryonic stem cell identity. Nature 468: 316-320.
5. Grabole N, Tischler J, Hackett JA, Kim S, Tang F, et al. (2013) Prdm14 promotes germline fate and naive pluripotency by repressing FGF signalling and DNA methylation. EMBO Rep 14: 629-637.
6. Ma Z, Swigut T, Valouev A, Rada-Iglesias A, Wysocka J (2011) Sequencespecific regulator Prdm14 safeguards mouse ESCs from entering extraembryonic endoderm fates. Nat Struct Mol Biol 18: 120-127.
7. Takahashi K, Yamanaka S (2006) Induction of pluripotent stem cells from mouse embryonic and adult fibroblast cultures by defined factors. Cell 126: 663-676.
8. Hayashi K, Ohta H, Kurimoto K, Aramaki S, Saitou M (2011) Reconstitution of the mouse germ cell specification pathway in culture by pluripotent stem cells. Cell 146: 519-532.
9. Yu J, Vodyanik MA, Smuga-Otto K, Antosiewicz-Bourget J, Frane JL, et al. (2007) Induced pluripotent stem cell lines derived from human somatic cells. Science 318: 1917-1920.
10. Anderson RA, Fulton N, Cowan G, Coutts S, Saunders PT (2007) Conserved and divergent patterns of expression of DAZL, VASA and OCT4 in the germ cells of the human fetal ovary and testis. BMC Dev Biol 7: 136.
11. Arnold K, Sarkar A, Yram MA, Polo JM, Bronson R, et al. (2011) Sox2(+) adult stem and progenitor cells are important for tissue regeneration and survival of mice. Cell Stem Cell 9: 317-329.
12. Gillis AJ, Stoop H, Biermann K, van Gurp RJ, Swartzman E, et al. (2011) Expression and interdependencies of pluripotency factors LIN28, OCT3/4, NANOG and SOX2 in human testicular germ cells and tumours of the testis. Int J Androl 34: e160-174.
13. Izadyar F, Pau F, Marh J, Slepko N, Wang T, et al. (2008) Generation of multipotent cell lines from a distinct population of male germ line stem cells. Reproduction 135: 771-784.
14. Kuijk EW, de Gier J, Lopes SM, Chambers I, van Pelt AM, et al. (2010) A distinct expression pattern in mammalian testes indicates a conserved role for NANOG in spermatogenesis. PLoS One 5: e10987.
15. Liu S, Tang Z, Xiong T, Tang W (2011) Isolation and characterization of human spermatogonial stem cells. Reprod Biol Endocrinol 9: 141.
16. Ventela S, Makela JA, Kulmala J, Westermarck J, Toppari J (2012) Identification and regulation of a stage-specific stem cell niche enriched by Nanog-positive spermatogonial stem cells in the mouse testis. Stem Cells 30: 1008-1020.
17. Zheng K, Wu X, Kaestner KH, Wang PJ (2009) The pluripotency factor LIN28 marks undifferentiated spermatogonia in mouse. BMC Dev Biol 9: 38.
18. Resnick JL, Bixler LS, Cheng L, Donovan PJ (1992) Long-term proliferation of mouse primordial germ cells in culture. Nature 359: 550-551.
19. Matsui Y, Zsebo K, Hogan BL (1992) Derivation of pluripotential embryonic stem cells from murine primordial germ cells in culture. Cell 70: 841-847.
20. Zwaka TP, Thomson JA (2005) A germ cell origin of embryonic stem cells? Development 132: 227-233.
21. Nagamatsu G, Kosaka T, Kawasumi M, Kinoshita T, Takubo K, et al. (2011) A germ cell-specific gene, Prmt5, works in somatic cell reprogramming. J Biol Chem 286: 10641-10648.
22. Cox DN, Chao A, Lin H (2000) piwi encodes a nucleoplasmic factor whose activity modulates the number and division rate of germline stem cells. Development 127: 503-514.
23. Cox DN, Chao A, Baker J, Chang L, Qiao D, et al. (1998) A novel class of evolutionarily conserved genes defined by piwi are essential for stem cell selfrenewal. Genes Dev 12: 3715-3727.
24. Harris AN, Macdonald PM (2001) Aubergine encodes a Drosophila polar granule component required for pole cell formation and related to eIF2C. Development 128: 2823-2832.
25. Kirino Y, Kim N, de Planell-Saguer M, Khandros E, Chiorean S, et al. (2009) Arginine methylation of Piwi proteins catalysed by dPRMT5 is required for Ago3 and Aub stability. Nat Cell Biol 11: 652-658.
26. Megosh HB, Cox DN, Campbell C, Lin H (2006) The role of PIWI and the miRNA machinery in Drosophila germline determination. Curr Biol 16: 1884-1894.
27. Juliano C, Wang J, Lin H (2011) Uniting germline and stem cells: the function of Piwi proteins and the piRNA pathway in diverse organisms. Annu Rev Genet 45: 447-469.
28. Thomson T, Lin H (2009) The biogenesis and function of PIWI proteins and piRNAs: progress and prospect. Annu Rev Cell Dev Biol 25: 355-376.
29. Deng W, Lin H (2002) miwi, a murine homolog of piwi, encodes a cytoplasmic protein essential for spermatogenesis. Dev Cell 2: 819-830.
30. Unhavaithaya Y, Hao Y, Beyret E, Yin H, Kuramochi-Miyagawa S, et al. (2009) MILI, a PIWI-interacting RNA-binding protein, is required for germ line stem cell self-renewal and appears to positively regulate translation. J Biol Chem 284: 6507-6519.
31. Kuramochi-Miyagawa S, Kimura T, Ijiri TW, Isobe T, Asada N, et al. (2004) Mili, a mammalian member of piwi family gene, is essential for spermatogenesis. Development 131: 839-849.
32. Carmell MA, Girard A, van de Kant HJ, Bourc'his D, Bestor TH, et al. (2007) MIWI2 is essential for spermatogenesis and repression of transposons in the mouse male germline. Dev Cell 12: 503-514.
33. Aravin AA, Sachidanandam R, Bourc'his D, Schaefer C, Pezic D, et al. (2008) A piRNA pathway primed by individual transposons is linked to de novo DNA methylation in mice. Mol Cell 31: 785-799.
34. Vourekas A, Zheng Q, Alexiou P, Maragkakis M, Kirino Y, et al. (2012) Mili and Miwi target RNA repertoire reveals piRNA biogenesis and function of Miwi in spermiogenesis. Nat Struct Mol Biol 19: 773-781.
35. Mani SR, Megosh H, Lin H (2013) PIWI proteins are essential for early Drosophila embryogenesis. Dev Biol.
36. Brambrink T, Foreman R, Welstead GG, Lengner CJ, Wernig M, et al. (2008) Sequential expression of pluripotency markers during direct reprogramming of mouse somatic cells. Cell Stem Cell 2: 151-159.
37. Huangfu D, Osafune K, Maehr R, Guo W, Eijkelenboom A, et al. (2008) Induction of pluripotent stem cells from primary human fibroblasts with only Oct4 and Sox2. Nat Biotechnol 26: 1269-1275.
38. Lee DF, Su J, Sevilla A, Gingold J, Schaniel C, et al. (2012) Combining competition assays with genetic complementation strategies to dissect mouse embryonic stem cell self-renewal and pluripotency. Nat Protoc 7: 729-748.
39. Sato N, Meijer L, Skaltsounis L, Greengard P, Brivanlou AH (2004) Maintenance of pluripotency in human and mouse embryonic stem cells through activation of Wnt signaling by a pharmacological GSK-3-specific inhibitor. Nat Med 10: 55-63.
40. Burdon T, Stracey C, Chambers I, Nichols J, Smith A (1999) Suppression of SHP-2 and ERK signalling promotes self-renewal of mouse embryonic stem cells. Dev Biol 210: 30-43.
41. Ying QL, Nichols J, Chambers I, Smith A (2003) BMP induction of Id proteins suppresses differentiation and sustains embryonic stem cell self-renewal in collaboration with STAT3. Cell 115: 281-292.
42. Niwa H, Burdon T, Chambers I, Smith A (1998) Self-renewal of pluripotent embryonic stem cells is mediated via activation of STAT3. Genes Dev 12: 2048-2060.
43. Maekawa M, Yamaguchi K, Nakamura T, Shibukawa R, Kodanaka I, et al. (2011) Direct reprogramming of somatic cells is promoted by maternal transcription factor Glis1. Nature 474: 225-229.
44. Yin H, Lin H (2007) An epigenetic activation role of Piwi and a Piwi-associated piRNA in Drosophila melanogaster. Nature 450: 304-308.
45. Brower-Toland B, Findley SD, Jiang L, Liu L, Yin H, et al. (2007) Drosophila PIWI associates with chromatin and interacts directly with HP1a. Genes Dev 21: 2300-2311.
46. Peng JC, Lin H (2013) Beyond transposons: the epigenetic and somatic functions of the Piwi-piRNA mechanism. Curr Opin Cell Biol 25: 190-194.
47. Gangaraju VK, Yin H, Weiner MM, Wang J, Huang XA, et al. (2011) Drosophila Piwi functions in Hsp90-mediated suppression of phenotypic variation. Nat Genet 43: 153-158.
48. Specchia V, Piacentini L, Tritto P, Fanti L, D'Alessandro R, et al. (2010) Hsp90 prevents phenotypic variation by suppressing the mutagenic activity of transposons. Nature 463: 662-665.
49. Nolde MJ, Cheng EC, Guo S, Lin H (2013) Piwi genes are dispensable for normal hematopoiesis in mice. PLoS One 8: e71950.
50. Takahashi K, Okita K, Nakagawa M, Yamanaka S (2007) Induction of pluripotent stem cells from fibroblast cultures. Nat Protoc 2: 3081-3089.
51. Huangfu D, Maehr R, Guo W, Eijkelenboom A, Snitow M, et al. (2008) Induction of pluripotent stem cells by defined factors is greatly improved by small-molecule compounds. Nat Biotechnol 26: 795-797.
52. Li H, Durbin R (2009) Fast and accurate short read alignment with Burrows-Wheeler transform. Bioinformatics 25: 1754-1760.
53. Anders S, Huber W (2010) Differential expression analysis for sequence count data. Genome Biol 11: R106.
54. Robinson MD, McCarthy DJ, Smyth GK (2010) edgeR: a Bioconductor package for differential expression analysis of digital gene expression data. Bioinformatics 26: 139-140.
55. Hardcastle TJ, Kelly KA (2010) baySeq: empirical Bayesian methods for identifying differential expression in sequence count data. BMC Bioinformatics 11: 422.
56. Hong F, Breitling R, McEntee CW, Wittner BS, Nemhauser JL, et al. (2006) RankProd: a bioconductor package for detecting differentially expressed genes in meta-analysis. Bioinformatics 22: 2825-2827.
57. Benjamini Y, Drai D, Elmer G, Kafkafi N, Golani I (2001) Controlling the false discovery rate in behavior genetics research. Behav Brain Res 125: 279-284.