Epigenetic Disruption of the PIWI Pathway in Human Spermatogenic Disorders

PLoS ONE

Volumn 7, Issue 10, 2012, Pages

  Heyn, Holger ^a   Ferreira, Humberto J ^a,b   Bassas, Lluís ^c   Bonache, Sandra ^a,f   Sayols, Sergi ^a   Sandoval, Juan ^a   Esteller, Manel ^a,d,e   Larriba, Sara ^a  

^a BELLVITGE BIOMEDICAL RESEARCH INSTITUTE IDIBELL   (Spain)

^b UNIVERSITY OF COIMBRA   (Portugal)

^c FUNDACIÓ PUIGVERT   (Spain)

^d UNIVERSITY OF BARCELONA   (Spain)

^e INSTITUCIÓ CATALANA DE RECERCA I ESTUDIS AVANÇATS ICREA   (Spain)

^f HOSPITAL UNIVERSITARI VALL D HEBRON   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

GENOMIC DNA; PIWI INTERACTING RNA;

ADULT; ARTICLE; AZOOSPERMIA; CELL MATURATION; CELLULAR DISTRIBUTION; CLINICAL ARTICLE; CONTROLLED STUDY; DEVELOPMENTAL DISORDER; DNA METHYLATION; EPIGENETICS; GENE; GENE EXPRESSION REGULATION; GENE FUNCTION; GENE INACTIVATION; GENE LOCATION; GENE SILENCING; GENETIC PREDISPOSITION; GENOME; GERM CELL; HEREDITY; HUMAN; HUMAN CELL; HUMAN TISSUE; MALE; MALE INFERTILITY; NUCLEOTIDE SEQUENCE; OLIGOSPERMIA; PATHOPHYSIOLOGY; PIWIL2 GENE; PROMOTER REGION; PYROSEQUENCING; SEQUENCE ANALYSIS; SERTOLI CELL; SERTOLI CELL ONLY SYNDROME; SPERM; SPERMATID; SPERMATOCYTE; SPERMATOGENESIS; SPERMATOGENIC DISORDER; SPERMATOGONIUM; TDRD1 GENE; VALIDATION STUDY;

ADULT; ARGONAUTE PROTEINS; CARRIER PROTEINS; DNA; DNA METHYLATION; DOWN-REGULATION; HUMANS; INFERTILITY, MALE; MALE; MIDDLE AGED; RNA; SERTOLI CELL-ONLY SYNDROME; SPERMATOGENESIS; SPERMATOZOA;

MUS;

EID: 84868116558     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0047892     Document Type: Article

References (50)

1. Gianotten J, Lombardi MP, Zwinderman AH, Lilford RJ, van der Veen F, (2004) Idiopathic impaired spermatogenesis: genetic epidemiology is unlikely to provide a short-cut to better understanding. Hum Reprod Update 10: 533-539 doi:10.1093/humupd/dmh045.
2. Schrader M, Müller-Tidow C, Ravnik S, Müller M, Schulze W, et al. (2002) Cyclin A1 and gametogenesis in fertile and infertile patients: a potential new molecular diagnostic marker. Hum Reprod 17: 2338-2343 doi:10.1093/humrep/17.9.2338.
3. Steger K, Fink L, Failing K, Bohle RM, Kliesch S, et al. (2003) Decreased protamine-1 transcript levels in testes from infertile men. Mol Hum Reprod 9: 331-336 doi:10.1093/molehr/gag041.
4. Lin YM, Kuo PL, Lin YH, Teng YN, Lin JSN, (2005) Messenger RNA transcripts of the meiotic regulator BOULE in the testis of azoospermic men and their application in predicting the success of sperm retrieval. Hum Reprod 20: 782-788 doi:10.1093/humrep/deh647.
5. Lin YM, Teng YN, Chung CL, Tsai WC, Lin YH, et al. (2006) Decreased mRNA transcripts of M-phase promoting factor and its regulators in the testes of infertile men. Hum Reprod 21: 138-144 doi:10.1093/humrep/dei285.
6. Cheng YS, Kuo PL, Teng YN, Kuo TY, Chung CL, et al. (2006) Association of spermatogenic failure with decreased CDC25A expression in infertile men. Hum Reprod 21: 2346-2352 doi:10.1093/humrep/del163.
7. Terribas E, Bonache S, Garcia-arevalo M, Sanchez J, Franco E, et al. (2010) Changes in the Expression Profile of the Meiosis-Involved Mismatch Repair Genes in Impaired Human Spermatogenesis. J Androl 31: 346-357 doi:10.2164/jandrol.109.008805.
8. Hammoud SS, Nix DA, Zhang H, Purwar J, Carrell DT, et al. (2009) Distinctive Chromatin in Human Sperm Packages Genes for Embryo Development. Nature 460: 473-478 doi:10.1038/nature08162.
9. Irizarry RA, Ladd-Acosta C, Wen B, Wu Z, Montano C, et al. (2009) The human colon cancer methylome shows similar hypo- and hypermethylation at conserved tissue-specific CpG island shores. Nat Genet 41: 178-186 doi:10.1038/ng.298.
10. De Carvalho DD, You JS, Jones PA, (2010) DNA methylation and cellular reprogramming. Trends Cell Biol 20: 609-617 doi:10.1016/j.tcb.2010.08.003.
11. Berdasco M, Esteller M, (2010) Aberrant epigenetic landscape in cancer: how cellular identity goes awry. Dev Cell 19: 698-711 doi:10.1016/j.devcel.2010.10.005.
12. Rodríguez-Paredes M, Esteller M, (2011) Cancer epigenetics reaches mainstream oncology. Nat Med 17: 330-339 doi:10.1038/nm.2305.
13. Rakyan VK, Down TA, Balding DJ, Beck S, (2011) Epigenome-wide association studies for common human diseases. Nat Rev Genet 12: 529-541 doi:10.1038/nrg3000.
14. Feinberg AP, (2007) Phenotypic plasticity and the epigenetics of human disease. Nature 447: 433-440 doi:10.1038/nature05919.
15. Urdinguio RG, Sanchez-Mut JV, Esteller M, (2009) Epigenetic mechanisms in neurological diseases: genes, syndromes, and therapies. Lancet Neurol 8: 1056-1072 doi:10.1016/S1474-4422(09)70262-5.
16. Yaman R, Grandjean V, (2006) Timing of entry of meiosis depends on a mark generated by DNA methyltransferase 3a in testis. Mol Reprod Dev 73: 390-397 doi:10.1002/mrd.20430.
17. Bourc'his D, Bestor TH, (2004) Meiotic catastrophe and retrotransposon reactivation in male germ cells lacking Dnmt3L. Nature 431: 96-99 doi:10.1038/nature02886.
18. Takashima S, Takehashi M, Lee J, Chuma S, Okano M, et al. (2009) Abnormal DNA Methyltransferase Expression in Mouse Germline Stem Cells Results in Spermatogenic Defects. Biol Reprod 81: 155-164 doi:10.1095/biolreprod.108.074708.
19. Kobayashi H, Sato A, Otsu E, Hiura H, Tomatsu C, et al. (2007) Aberrant DNA methylation of imprinted loci in sperm from oligospermic patients. Hum Mol Genet 16: 2542-2551 doi:10.1093/hmg/ddm187.
20. Marques CJ, Carvalho F, Sousa M, Barros A, (2004) Genomic imprinting in disruptive spermatogenesis. Lancet 363: 1700-1702 doi:10.1016/S0140-6736(04)16256-9.
21. Marques CJ, Costa P, Vaz B, Carvalho F, Fernandes S, et al. (2008) Abnormal methylation of imprinted genes in human sperm is associated with oligozoospermia. Mol Hum Reprod 14: 67-74 doi:10.1093/molehr/gam093.
22. Houshdaran S, Cortessis VK, Siegmund K, Yang A, Laird PW, et al. (2007) Widespread Epigenetic Abnormalities Suggest a Broad DNA Methylation Erasure Defect in Abnormal Human Sperm. PLoS ONE 2. doi:10.1371/journal.pone.0001289.
23. Teschendorff AE, Menon U, Gentry-Maharaj A, Ramus SJ, Weisenberger DJ, et al. (2010) Age-dependent DNA methylation of genes that are suppressed in stem cells is a hallmark of cancer. Genome Res 20: 440-446 doi:10.1101/gr.103606.109.
24. Rakyan VK, Down TA, Maslau S, Andrew T, Yang T-P, et al. (2010) Human aging-associated DNA hypermethylation occurs preferentially at bivalent chromatin domains. Genome Res 20: 434-439 doi:10.1101/gr.103101.109.
25. Deng W, Lin H, (2002) miwi, a murine homolog of piwi, encodes a cytoplasmic protein essential for spermatogenesis. Dev Cell 2: 819-830.
26. 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 doi:10.1242/dev.00973.
27. Wang J, Saxe JP, Tanaka T, Chuma S, Lin H, (2009) Mili interacts with tudor domain-containing protein 1 in regulating spermatogenesis. Curr Biol 19: 640-644 doi:10.1016/j.cub.2009.02.061.
28. Reuter M, Chuma S, Tanaka T, Franz T, Stark A, et al. (2009) Loss of the Mili-interacting Tudor domain-containing protein-1 activates transposons and alters the Mili-associated small RNA profile. Nat Struct Mol Biol 16: 639-646 doi:10.1038/nsmb.1615.
29. Shoji M, Tanaka T, Hosokawa M, Reuter M, Stark A, et al. (2009) The TDRD9-MIWI2 complex is essential for piRNA-mediated retrotransposon silencing in the mouse male germline. Dev Cell 17: 775-787 doi:10.1016/j.devcel.2009.10.012.
30. WHO, World Health Organization Laboratory (1999) Manual for the Examination of Human Semen and Sperm-Cervical Mucus Interaction. 4th ed. New York: Cambridge University Press. p.
31. Simoni M, Bakker E, Eurlings MC, Matthijs G, Moro E, et al. (1999) Laboratory guidelines for molecular diagnosis of Y-chromosomal microdeletions. Int J Androl 22: 292-299 doi:10.1046/j.1365-2605.1999.00193.x.
32. Simoni M, Bakker E, Krausz C, (2004) EAA/EMQN best practice guidelines for molecular diagnosis of y-chromosomal microdeletions. State of the art 2004. Int J Androl 27: 240-249 doi:10.1111/j.1365-2605.2004.00495.x.
33. Schulze W, Thoms F, Knuth U, (1999) Testicular sperm extraction: comprehensive analysis with simultaneously performed histology in 1418 biopsies from 766 subfertile men. Hum Reprod 14: 82-96.
34. Vandesompele J, De Preter K, Pattyn F, Poppe B, Van Roy N, et al. (2002) Accurate normalization of real-time quantitative RT-PCR data by geometric averaging of multiple internal control genes. Genome Biol 3: RESEARCH0034.
35. Kanduri M, Cahill N, Göransson H, Enström C, Ryan F, et al. (2010) Differential genome-wide array-based methylation profiles in prognostic subsets of chronic lymphocytic leukemia. Blood 115: 296-305 doi:10.1182/blood-2009-07-232868.
36. Girard A, Sachidanandam R, Hannon GJ, Carmell MA, (2006) A germline-specific class of small RNAs binds mammalian Piwi proteins. Nature 442: 199-202 doi:10.1038/nature04917.
37. Doerksen T, Benoit G, Trasler JM, (2000) Deoxyribonucleic Acid Hypomethylation of Male Germ Cells by Mitotic and Meiotic Exposure to 5-Azacytidine Is Associated with Altered Testicular Histology. Endocrinology 141: 3235-3244 doi:10.1210/en.141.9.3235.
38. Oakes CC, La Salle S, Smiraglia DJ, Robaire B, Trasler JM, (2007) A unique configuration of genome-wide DNA methylation patterns in the testis. Proc Natl Acad Sci U S A 104: 228-233 doi:10.1073/pnas.0607521104.
39. Netto GJ, Nakai Y, Nakayama M, Jadallah S, Toubaji A, et al. (2008) Global DNA hypomethylation in intratubular germ cell neoplasia and seminoma, but not in nonseminomatous male germ cell tumors. Mod Pathol 21: 1337-1344.
40. 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 doi:10.1074/jbc.M809104200.
41. Lee JH, Schütte D, Wulf G, Füzesi L, Radzun H-J, et al. (2006) Stem-cell protein Piwil2 is widely expressed in tumors and inhibits apoptosis through activation of Stat3/Bcl-XL pathway. Hum Mol Genet 15: 201-211 doi:10.1093/hmg/ddi430.
42. Kuramochi-Miyagawa S, Watanabe T, Gotoh K, Totoki Y, Toyoda A, et al. (2008) DNA methylation of retrotransposon genes is regulated by Piwi family members MILI and MIWI2 in murine fetal testes. Genes Dev 22: 908-917 doi:10.1101/gad.1640708.
43. Aravin A, Gaidatzis D, Pfeffer S, Lagos-Quintana M, Landgraf P, et al. (2006) A novel class of small RNAs bind to MILI protein in mouse testes. Nature 442: 203-207 doi:10.1038/nature04916.
44. Siomi MC, Mannen T, Siomi H, (2010) How does the Royal Family of Tudor rule the PIWI-interacting RNA pathway? Genes Dev 24: 636-646 doi:10.1101/gad.1899210.
45. Carmell MA, Girard A, van de Kant HJG, 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 doi:10.1016/j.devcel.2007.03.001.
46. Brennecke J, Aravin AA, Stark A, Dus M, Kellis M, et al. (2007) Discrete small RNA-generating loci as master regulators of transposon activity in Drosophila. Cell 128: 1089-1103 doi:10.1016/j.cell.2007.01.043.
47. Aravin AA, Hannon GJ, Brennecke J, (2007) The Piwi-piRNA pathway provides an adaptive defense in the transposon arms race. Science 318: 761-764 doi:10.1126/science.1146484.
48. 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 doi:10.1016/j.molcel.2008.09.003.
49. Aravin AA, Sachidanandam R, Girard A, Fejes-Toth K, Hannon GJ, (2007) Developmentally regulated piRNA clusters implicate MILI in transposon control. Science 316: 744-747 doi:10.1126/science.1142612.
50. Watanabe T, Tomizawa S, Mitsuya K, Totoki Y, Yamamoto Y, et al. (2011) Role for piRNAs and Noncoding RNA in de Novo DNA Methylation of the Imprinted Mouse Rasgrf1 Locus. Science 332: 848-852 doi:10.1126/science.1203919.