Fertility and Sterility
Volume 94, Issue 5 , Pages 1728-1733 , October 2010

Alterations in sperm DNA methylation patterns at imprinted loci in two classes of infertility

  • Saher Sue Hammoud, B.S.

      Affiliations

    • Andrology and IVF Laboratories, Division of Urology, Department of Surgery, School of Medicine, University of Utah, Salt Lake City, Utah
    • Department of Physiology, School of Medicine, University of Utah, Salt Lake City, Utah
  • ,
  • Jahnvi Purwar, B.S.

      Affiliations

    • Department of Oncological Sciences, Huntsman Cancer Institute, University of Utah, Salt Lake City, Utah
  • ,
  • Christian Pflueger, M.S.

      Affiliations

    • Department of Oncological Sciences, Huntsman Cancer Institute, University of Utah, Salt Lake City, Utah
  • ,
  • Bradley R. Cairns, Ph.D.

      Affiliations

    • Department of Oncological Sciences, Huntsman Cancer Institute, University of Utah, Salt Lake City, Utah
    • Howard Hughes Medical Institute, University of Utah School of Medicine, Salt Lake City, Utah
  • ,
  • Douglas T. Carrell, Ph.D.

      Affiliations

    • Andrology and IVF Laboratories, Division of Urology, Department of Surgery, School of Medicine, University of Utah, Salt Lake City, Utah
    • Department of Physiology, School of Medicine, University of Utah, Salt Lake City, Utah
    • Department of Obstetrics and Gynecology, School of Medicine, University of Utah, Salt Lake City, Utah
    • Corresponding Author InformationReprint requests: Douglas T. Carrell, Ph.D., University of Utah IVF and Andrology Laboratories, 675 Arapeen Drive, Suite 205, Salt Lake City, UT 84108 (FAX: 801-581-6127).

Received 8 April 2009 ,Revised 5 August 2009 ,Accepted 8 September 2009.

References 

  1. Morison IM, Paton CJ, Cleverley SD. The imprinted gene and parent-of-origin effect database. Nucleic Acids Res. 2001;29:275–276
  2. Ferguson-Smith AC, Surani MA. Imprinting and the epigenetic asymmetry between parental genomes. Science. 2001;293:1086–1089
  3. Verona RI, Mann MR, Bartolomei MS. Genomic imprinting: intricacies of epigenetic regulation in clusters. Annu Rev Cell Dev Biol. 2003;19:237–259
  4. Spahn L, Barlow DP. An ICE pattern crystallizes. Nat Genet. 2003;35:11–12
  5. Morgan HD, Santos F, Green K, Dean W, Reik W. Epigenetic reprogramming in mammals. Hum Mol Genet. 2005;14 Spec No 1: R47–R58
  6. Jaenisch R, Bird A. Epigenetic regulation of gene expression: how the genome integrates intrinsic and environmental signals. Nat Genet. 2003;33;Suppl:245–54
  7. Royo H, Bortolin ML, Seitz H, Cavaille J. Small non-coding RNAs and genomic imprinting. Cytogenet Genome Res. 2006;113:99–108
  8. Seitz H, Royo H, Bortolin ML, Lin SP, Ferguson-Smith AC, Cavaille J. A large imprinted microRNA gene cluster at the mouse Dlk1-Gtl2 domain. Genome Res. 2004;14:1741–1748
  9. Bjornsson HT, Brown LJ, Fallin MD, Rongione MA, Bibikova M, Wickham E, et al. Epigenetic specificity of loss of imprinting of the IGF2 gene in Wilms tumors. J Natl Cancer Inst. 2007;99:1270–1273
  10. Chao W, D'Amore PA. IGF2: epigenetic regulation and role in development and disease. Cytokine Growth Factor Rev. 2008;19:111–120
  11. Cui H. Loss of imprinting of IGF2 as an epigenetic marker for the risk of human cancer. Dis Markers. 2007;23:105–112
  12. Hemberger M. Epigenetic landscape required for placental development. Cell Mol Life Sci. 2007;64:2422–2436
  13. Henckel A, Feil R. Differential epigenetic marking on imprinted genes and consequences in human diseases. Med Sci (Paris). 2008;24:747–752
  14. Lemeta S, Jarmalaite S, Pylkkanen L, Bohling T, Husgafvel-Pursiainen K. Preferential loss of the nonimprinted allele for the ZAC1 tumor suppressor gene in human capillary hemangioblastoma. J Neuropathol Exp Neurol. 2007;66:860–867
  15. Murrell A, Ito Y, Verde G, Huddleston J, Woodfine K, Silengo MC, et al. Distinct methylation changes at the IGF2-H19 locus in congenital growth disorders and cancer. PLoS ONE. 2008;3:e1849
  16. Nakano S, Murakami K, Meguro M, Soejima H, Higashimoto K, Urano T, et al. Expression profile of LIT1/KCNQ1OT1 and epigenetic status at the KvDMR1 in colorectal cancers. Cancer Sci. 2006;97:1147–1154
  17. Nowaczyk MJ, Carter MT, Xu J, Huggins M, Raca G, Das S, et al. Paternal deletion 6q24.3: a new congenital anomaly syndrome associated with intrauterine growth failure, early developmental delay and characteristic facial appearance. Am J Med Genet A. 2008;146:354–360
  18. Shin JY, Fitzpatrick GV, Higgins MJ. Two distinct mechanisms of silencing by the KvDMR1 imprinting control region. EMBO J. 2008;27:168–178
  19. Valleley EM, Cordery SF, Bonthron DT. Tissue-specific imprinting of the ZAC/PLAGL1 tumour suppressor gene results from variable utilization of monoallelic and biallelic promoters. Hum Mol Genet. 2007;16:972–981
  20. Yoshimizu T, Miroglio A, Ripoche MA, Gabory A, Vernucci M, Riccio A, et al. The H19 locus acts in vivo as a tumor suppressor. Proc Natl Acad Sci U S A. 2008;105:12417–12422
  21. Cox GF, Burger J, Lip V, Mau UA, Sperling K, Wu BL, et al. Intracytoplasmic sperm injection may increase the risk of imprinting defects. Am J Hum Genet. 2002;71:162–164
  22. Niemitz EL, DeBaun MR, Fallon J, Murakami K, Kugoh H, Oshimura M, et al. Microdeletion of LIT1 in familial Beckwith-Wiedemann syndrome. Am J Hum Genet. 2004;75:844–849
  23. DeBaun MR, Niemitz EL, Feinberg AP. Association of in vitro fertilization with Beckwith-Wiedemann syndrome and epigenetic alterations of LIT1 and H19. Am J Hum Genet. 2003;72:156–160
  24. Gosden R, Trasler J, Lucifero D, Faddy M. Rare congenital disorders, imprinted genes, and assisted reproductive technology. Lancet. 2003;361:1975–1977
  25. Kobayashi H, Sato A, Otsu E, Hiura H, Tomatsu C, Utsunomiya T, et al. Aberrant DNA methylation of imprinted loci in sperm from oligospermic patients. Hum Mol Genet. 2007;16:2542–2551
  26. Marques CJ, Carvalho F, Sousa M, Barros A. Genomic imprinting in disruptive spermatogenesis. Lancet. 2004;363:1700–1702
  27. Marques CJ, Costa P, Vaz B, Carvalho F, Fernandes S, Barros A, et al. Abnormal methylation of imprinted genes in human sperm is associated with oligozoospermia. Mol Hum Reprod. 2008;14:67–74
  28. Aoki VW, Emery BR, Liu L, Carrell DT. Protamine levels vary between individual sperm cells of infertile human males and correlate with viability and DNA integrity. J Androl. 2006;27:890–898
  29. Balhorn R, Reed S, Tanphaichitr N. Aberrant protamine 1/protamine 2 ratios in sperm of infertile human males. Experientia. 1988;44:52–55
  30. Aoki VW, Moskovtsev SI, Willis J, Liu L, Mullen JB, Carrell DT. DNA integrity is compromised in protamine-deficient human sperm. J Androl. 2005;26:741–748
  31. Aoki VW, Liu L, Jones KP, Hatasaka HH, Gibson M, Peterson CM, et al. Sperm protamine 1/protamine 2 ratios are related to in vitro fertilization pregnancy rates and predictive of fertilization ability. Fertil Steril. 2006;86:1408–1415
  32. Paldi A. Genomic imprinting: could the chromatin structure be the driving force?. Curr Top Dev Biol. 2003;53:115–138
  33. Rousseaux S, Caron C, Govin J, Lestrat C, Faure AK, Khochbin S. Establishment of male-specific epigenetic information. Gene. 2005;345:139–153
  34. Clark SJ, Harrison J, Paul CL, Frommer M. High sensitivity mapping of methylated cytosines. Nucleic Acids Res. 1994;22:2990–2997
  35. El-Maarri O, Seoud M, Coullin P, Herbiniaux U, Oldenburg J, Rouleau G, et al. Maternal alleles acquiring paternal methylation patterns in biparental complete hydatidiform moles. Hum Mol Genet. 2003;12:1405–1413
  36. Kamikihara T, Arima T, Kato K, Matsuda T, Kato H, Douchi T, et al. Epigenetic silencing of the imprinted gene ZAC by DNA methylation is an early event in the progression of human ovarian cancer. Int J Cancer. 2005;115:690–700
  37. Arima T, Kamikihara T, Hayashida T, Kato K, Inoue T, Shirayoshi Y, et al. ZAC, LIT1 (KCNQ1OT1) and p57KIP2 (CDKN1C) are in an imprinted gene network that may play a role in Beckwith-Wiedemann syndrome. Nucleic Acids Res. 2005;33:2650–2660
  38. Kagami M, Nagai T, Fukami M, Yamazawa K, Ogata T. Silver-Russell syndrome in a girl born after in vitro fertilization: partial hypermethylation at the differentially methylated region of PEG1/MEST. J Assist Reprod Genet. 2007;24:131–136

 S.S.H. has nothing to disclose. J.P. has nothing to disclose. C.P. has nothing to disclose. B.R.C. has nothing to disclose. D.T.C. has nothing to disclose.

 Saher Sue Hammoud and Jahnvi Purwar contributed equally.

PII: S0015-0282(09)03689-9

doi: 10.1016/j.fertnstert.2009.09.010

Fertility and Sterility
Volume 94, Issue 5 , Pages 1728-1733 , October 2010