Identification of genomic features in environmentally induced epigenetic transgenerational inherited sperm epimutations

PLoS ONE

Volumn 9, Issue 6, 2014, Pages

  Guerrero Bosagna, Carlos ^a,b   Weeks, Shelby ^a   Skinner, Michael K ^a  

^a WASHINGTON STATE UNIVERSITY   (United States)

^b LINKÖPING UNIVERSITY   (Sweden)

Author keywords

[No Author keywords available]

Indexed keywords

DNA METHYLTRANSFERASE; GUANINE QUADRUPLEX; ZINC FINGER PROTEIN;

ANIMAL CELL; ARTICLE; BINDING AFFINITY; BINDING SITE; BIOINFORMATICS; CHROMATIN; CHROMATIN ASSEMBLY AND DISASSEMBLY; CONTROLLED STUDY; CPG ISLAND; DATA ANALYSIS; DNA METHYLATION; DNA MODIFICATION; DNA SEQUENCE; ENVIRONMENTAL FACTOR; EPIGENETICS; GENE MUTATION; GENE STRUCTURE; GENETIC ASSOCIATION; GENOME ANALYSIS; GENOTYPE ENVIRONMENT INTERACTION; MOLECULAR DYNAMICS; MOUSE; NONHUMAN; PROMOTER REGION; PROTEIN DNA BINDING; PROTEIN DNA INTERACTION; RAT; SEQUENCE ANALYSIS; SPERM; WEB BROWSER; ANIMAL; ENVIRONMENT; FEMALE; GENE EXPRESSION REGULATION; GENETIC EPIGENESIS; GENETICS; GENOME; GENOMICS; MALE; MUTATION; PROCEDURES; SPERMATOZOON;

ANIMALS; DNA METHYLATION; ENVIRONMENT; EPIGENESIS, GENETIC; FEMALE; GENE EXPRESSION REGULATION; GENOME; GENOMICS; MALE; MUTATION; RATS; SPERMATOZOA;

EID: 84903289499     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0100194     Document Type: Article

References (65)

1. Anway MD, Cupp AS, Uzumcu M, Skinner MK (2005) Epigenetic transgenerational actions of endocrine disruptors and male fertility. Science 308: 1466-1469. (Pubitemid 40791300)
2. Manikkam M, Tracey R, Guerrero-Bosagna C, Skinner MK (2012) Dioxin (TCDD) induces epigenetic transgenerational inheritance of adult onset disease and sperm epimutations. PLoS One 7: e46249.
3. Guerrero-Bosagna C, Settles M, Lucker B, Skinner M (2010) Epigenetic transgenerational actions of vinclozolin on promoter regions of the sperm epigenome. PLoS ONE 5: e13100.
4. Guerrero-Bosagna C, Covert T, Haque MM, Settles M, Nilsson EE, et al. (2012) Epigenetic Transgenerational Inheritance of Vinclozolin Induced Mouse Adult Onset Disease and Associated Sperm Epigenome Biomarkers. Reproductive Toxicology 34: 694-707.
5. Manikkam M, Tracey R, Guerrero-Bosagna C, Skinner M (2012) Pesticide and Insect Repellent Mixture (Permethrin and DEET) Induces Epigenetic Transgenerational Inheritance of Disease and Sperm Epimutations. Reproductive Toxicology 34: 708-719.
6. Manikkam M, Guerrero-Bosagna C, Tracey R, Haque MM, Skinner MK (2012) Transgenerational Actions of Environmental Compounds on Reproductive Disease and Epigenetic Biomarkers of Ancestral Exposures. PLoS ONE 7: e31901.
7. Skinner M, Guerrero-Bosagna C, Haque MM, Nilsson E, Bhandari R, et al. (2013) Environmentally Induced Transgenerational Epigenetic Reprogramming of Primordial Germ Cells and Subsequent Germline. PLoS ONE 8: e66318.
8. Tracey R, Manikkam M, Guerrero-Bosagna C, Skinner M (2013) Hydrocarbon (Jet Fuel JP-8) Induces Epigenetic Transgenerational Inheritance of Adult-Onset Disease and Sperm Epimutations. Reproductive Toxicology 36: 104-116.
9. Skinner MK, Mohan M, Haque MM, Zhang B, Savenkova MI (2012) Epigenetic transgenerational inheritance of somatic transcriptomes and epigenetic control regions. Genome Biol 13: R91.
10. Nilsson E, Larsen G, Manikkam M, Guerrero-Bosagna C, Savenkova MI, et al. (2012) Environmentally induced epigenetic transgenerational inheritance of ovarian disease. PLoS One 7: e36129.
11. Arico JK, Katz DJ, van der Vlag J, Kelly WG (2011) Epigenetic patterns maintained in early Caenorhabditis elegans embryos can be established by gene activity in the parental germ cells. PLoS Genet 7: e1001391.
12. Carone BR, Fauquier L, Habib N, Shea JM, Hart CE, et al. (2010) Paternally induced transgenerational environmental reprogramming of metabolic gene expression in mammals. Cell 143: 1084-1096.
13. Dunn GA, Bale TL (2011) Maternal high-fat diet effects on third-generation female body size via the paternal lineage. Endocrinology 152: 2228-2236.
14. Morgan CP, Bale TL (2011) Early prenatal stress epigenetically programs dysmasculinization in second-generation offspring via the paternal lineage. J Neurosci 31: 11748-11755.
15. Saze H (2012) Transgenerational inheritance of induced changes in the epigenetic state of chromatin in plants. Genes Genet Syst 87: 145-152.
16. Lees-Murdock DJ, Walsh CP (2008) DNA methylation reprogramming in the germ line. Epigenetics 3: 5-13. (Pubitemid 351540958)
17. Reik W, Dean W, Walter J (2001) Epigenetic reprogramming in mammalian development. Science 293: 1089-1093. (Pubitemid 32758081)
18. Smith ZD, Chan MM, Mikkelsen TS, Gu H, Gnirke A, et al. (2012) A unique regulatory phase of DNA methylation in the early mammalian embryo. Nature 484: 339-344.
19. Allegrucci C, Thurston A, Lucas E, Young L (2005) Epigenetics and the germline. Reproduction 129: 137-149. (Pubitemid 40340102)
20. Durcova-Hills G, Hajkova P, Sullivan S, Barton S, Surani MA, et al. (2006) Influence of sex chromosome constitution on the genomic imprinting of germ cells. Proc Natl Acad Sci U S A 103: 11184-11188. (Pubitemid 44156493)
21. Hackett JA, Zylicz JJ, Surani MA (2012) Parallel mechanisms of epigenetic reprogramming in the germline. Trends Genet 28: 164-174.
22. Skinner MK, Manikkam M, Guerrero-Bosagna C (2010) Epigenetic transgenerational actions of environmental factors in disease etiology. Trends Endocrinol Metab 21: 214-222.
23. Cowin PA, Gold E, Aleksova J, O'Bryan MK, Foster PM, et al. (2010) Vinclozolin exposure in utero induces postpubertal prostatitis and reduces sperm production via a reversible hormone-regulated mechanism. Endocrinology 151: 783-792.
24. Uzumcu M, Suzuki H, Skinner MK (2004) Effect of the anti-androgenic endocrine disruptor vinclozolin on embryonic testis cord formation and postnatal testis development and function. Reprod Toxicol 18: 765-774. (Pubitemid 38987963)
25. Webster KE, O'Bryan MK, Fletcher S, Crewther PE, Aapola U, et al. (2005) Meiotic and epigenetic defects in Dnmt3L-knockout mouse spermatogenesis. Proc Natl Acad Sci U S A 102: 4068-4073. (Pubitemid 40388556)
26. Stadler MB, Murr R, Burger L, Ivanek R, Lienert F, et al. (2011) DNA-binding factors shape the mouse methylome at distal regulatory regions. Nature 480: 490-495.
27. Molaro A, Hodges E, Fang F, Song Q, McCombie WR, et al. (2011) Sperm methylation profiles reveal features of epigenetic inheritance and evolution in primates. Cell 146: 1029-1041.
28. Filippova GN, Thienes CP, Penn BH, Cho DH, Hu YJ, et al. (2001) CTCF-binding sites flank CTG/CAG repeats and form a methylation-sensitive insulator at the DM1 locus. Nat Genet 28: 335-343. (Pubitemid 32702422)
29. Ichiyanagi K, Li Y, Watanabe T, Ichiyanagi T, Fukuda K, et al. (2011) Locusand domain-dependent control of DNA methylation at mouse B1 retrotransposons during male germ cell development. Genome Res 21: 2058-2066.
30. Wienholz BL, Kareta MS, Moarefi AH, Gordon CA, Ginno PA, et al. (2010) DNMT3L modulates significant and distinct flanking sequence preference for DNA methylation by DNMT3A and DNMT3B in vivo. PLoS Genet 6.
31. Alabert C, Groth A (2012) Chromatin replication and epigenome maintenance. Nat Rev Mol Cell Biol 13: 153-167.
32. Wen B, Wu H, Bjornsson H, Green RD, Irizarry R, et al. (2008) Overlapping euchromatin/heterochromatin- associated marks are enriched in imprinted gene regions and predict allele-specific modification. Genome Res 18: 1806-1813.
33. Das MK, Dai HK (2007) A survey of DNA motif finding algorithms. BMC Bioinformatics 8 Suppl 7: S21.
34. Stormo GD (2000) DNA binding sites: representation and discovery. Bioinformatics 16: 16-23.
35. Elnitski L, Jin VX, Farnham PJ, Jones SJ (2006) Locating mammalian transcription factor binding sites: a survey of computational and experimental techniques. Genome Res 16: 1455-1464. (Pubitemid 44878485)
36. Nardone J, Lee DU, Ansel KM, Rao A (2004) Bioinformatics for the 'bench biologist': how to find regulatory regions in genomic DNA. Nat Immunol 5: 768-774. (Pubitemid 39172966)
37. Wasserman WW, Sandelin A (2004) Applied bioinformatics for the identification of regulatory elements. Nat Rev Genet 5: 276-287. (Pubitemid 38435623)
38. Carroll JS, Meyer CA, Song J, Li W, Geistlinger TR, et al. (2006) Genome-wide analysis of estrogen receptor binding sites. Nat Genet 38: 1289-1297. (Pubitemid 44646291)
39. Kim TH, Abdullaev ZK, Smith AD, Ching KA, Loukinov DI, et al. (2007) Analysis of the vertebrate insulator protein CTCF-binding sites in the human genome. Cell 128: 1231-1245. (Pubitemid 46427876)
40. Feltus FA, Lee EK, Costello JF, Plass C, Vertino PM (2006) DNA motifs associated with aberrant CpG island methylation. Genomics 87: 572-579.
41. Frith MC, Saunders NF, Kobe B, Bailey TL (2008) Discovering sequence motifs with arbitrary insertions and deletions. PLoS Comput Biol 4: e1000071.
42. Bailey TL, Boden M, Buske FA, Frith M, Grant CE, et al. (2009) MEME SUITE: tools for motif discovery and searching. Nucleic Acids Res 37: W202-208.
43. Mahony S, Benos PV (2007) STAMP: a web tool for exploring DNA-binding motif similarities. Nucleic Acids Res 35: W253-258.
44. Nilsson E, Larsen G, Manikkam M, Guerrero-Bosagna C, Savenkova M, et al. (2012) Environmentally Induced Epigenetic Transgenerational Inheritance of Ovarian Disease. PLoS ONE 7: e36129.
45. Guerrero-Bosagna C, Savenkova M, Haque MM, Sadler-Riggleman I, Skinner MK (2013) Environmentally Induced Epigenetic Transgenerational Inheritance of Altered Sertoli Cell Transcriptome and Epigenome: Molecular Etiology of Male Infertility. PLoS ONE 8: e59922.
46. Manikkam M, Tracey R, Guerrero-Bosagna C, Skinner M (2013) Plastics Derived Endocrine Disruptors (BPA, DEHP and DBP) Induce Epigenetic Transgenerational Inheritance of Adult-Onset Disease and Sperm Epimutations. PLoS ONE 8: e55387.
47. Tamaru H, Selker EU (2003) Synthesis of signals for de novo DNA methylation in Neurospora crassa. Mol Cell Biol 23: 2379-2394. (Pubitemid 36351020)
48. Kumar P, Yadav VK, Baral A, Kumar P, Saha D, et al. (2011) Zinc-finger transcription factors are associated with guanine quadruplex motifs in human, chimpanzee, mouse and rat promoters genome-wide. Nucleic Acids Res 39: 8005-8016.
49. Halder R, Halder K, Sharma P, Garg G, Sengupta S, et al. (2010) Guanine quadruplex DNA structure restricts methylation of CpG dinucleotides genome-wide. Mol Biosyst 6: 2439-2447.
50. Sarkies P, Reams C, Simpson LJ, Sale JE (2010) Epigenetic instability due to defective replication of structured DNA. Mol Cell 40: 703-713.
51. Skinner MK, Manikkam M, Tracey R, Nilsson E, Haque MM, et al. (2013) Ancestral DDT Exposures Promote Epigenetic Transgenerational Inheritance of Obesity BMC Medicine 11: 228.
52. Bostick M, Kim JK, Esteve PO, Clark A, Pradhan S, et al. (2007) UHRF1 plays a role in maintaining DNA methylation in mammalian cells. Science 317: 1760-1764. (Pubitemid 47461842)
53. Sasai N, Nakao M, Defossez PA (2010) Sequence-specific recognition of methylated DNA by human zinc-finger proteins. Nucleic Acids Res 38: 5015-5022.
54. Datta J, Kutay H, Nasser MW, Nuovo GJ, Wang B, et al. (2008) Methylation mediated silencing of MicroRNA-1 gene and its role in hepatocellular carcinogenesis. Cancer Res 68: 5049-5058.
55. Klose RJ, Sarraf SA, Schmiedeberg L, McDermott SM, Stancheva I, et al. (2005) DNA binding selectivity of MeCP2 due to a requirement for A/T sequences adjacent to methyl-CpG. Mol Cell 19: 667-678. (Pubitemid 41219442)
56. Paeschke K, Bochman ML, Garcia PD, Cejka P, Friedman KL, et al. (2013) Pif1 family helicases suppress genome instability at G-quadruplex motifs. Nature 497: 458-462.
57. Wong C, Kelce WR, Sar M, Wilson EM (1995) Androgen receptor antagonist versus agonist activities of the fungicide vinclozolin relative to hydroxyflutamide. J Biol Chem 270: 19998-20003.
58. Singh S, Li SS (2012) Bisphenol A and phthalates exhibit similar toxicogenomics and health effects. Gene 494: 85-91.
59. Brander SM, He G, Smalling KL, Denison MS, Cherr GN (2012) The in vivo estrogenic and in vitro anti-estrogenic activity of permethrin and bifenthrin. Environ Toxicol Chem 31: 2848-2855.
60. Tanaka J, Yonemoto J, Zaha H, Kiyama R, Sone H (2007) Estrogen-responsive genes newly found to be modified by TCDD exposure in human cell lines and mouse systems. Mol Cell Endocrinol 272: 38-49. (Pubitemid 46908022)
61. Reutman SR, LeMasters GK, Knecht EA, Shukla R, Lockey JE, et al. (2002) Evidence of reproductive endocrine effects in women with occupational fuel and solvent exposures. Environ Health Perspect 110: 805-811.
62. Pitteloud N, Dwyer AA, DeCruz S, Lee H, Boepple PA, et al. (2008) Inhibition of luteinizing hormone secretion by testosterone in men requires aromatization for its pituitary but not its hypothalamic effects: evidence from the tandem study of normal and gonadotropin-releasing hormone-deficient men. J Clin Endocrinol Metab 93: 784-791. (Pubitemid 351398554)
63. Robison AK, Schmidt WA, Stancel GM (1985) Estrogenic activity of DDT: estrogen-receptor profiles and the responses of individual uterine cell types following o,p'-DDT administration. J Toxicol Environ Health 16: 493-508. (Pubitemid 16153220)
64. Frith MC, Fu Y, Yu L, Chen JF, Hansen U, et al. (2004) Detection of functional DNA motifs via statistical over-representation. Nucleic Acids Res 32: 1372-1381. (Pubitemid 38854738)
65. Grant CE, Bailey TL, Noble WS (2011) FIMO: scanning for occurrences of a given motif. Bioinformatics 27: 1017-1018.