CHD5 is required for spermiogenesis and chromatin condensation

Mechanisms of Development

Volumn 131, Issue 1, 2014, Pages 35-46

  Zhuang, Tiangang ^a   Hess, Rex A ^b   Kolla, Venkatadri ^a   Higashi, Mayumi ^a   Raabe, Tobias D ^c   Brodeur, Garrett M ^a,d  

^a CHILDREN S HOSPITAL OF PHILADELPHIA   (United States)

^b UNIVERSITY OF ILLINOIS AT URBANA CHAMPAIGN   (United States)

^c UNIVERSITY OF PENNSYLVANIA   (United States)

^d UNIVERSITY OF PENNSYLVANIA   (United States)

Author keywords

CHD5; Chromatin condensation; Histone modification; Infertility; Spermatogenesis; Spermiogenesis

Indexed keywords

ANILINE; GENOMIC DNA; HISTONE; HISTONE H4; MESSENGER RNA; NUCLEAR PROTEIN; PROTEIN CHD5; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BRAIN; CELL TYPE; CHROMATIN CONDENSATION; CONTROLLED STUDY; ELECTRON MICROSCOPY; EMBRYONIC STEM CELL; EPIDIDYMIS; EPITHELIUM; FEMALE; GENE TARGETING; GERM CELL; IMMUNOHISTOCHEMISTRY; KNOCKOUT MOUSE; MALE; MORPHOLOGY; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN ANALYSIS; REAL TIME POLYMERASE CHAIN REACTION; SEMINIFEROUS TUBULE; SPERM; SPERMATID; SPERMATOGENESIS; TESTIS;

MUS;

CHD5; CHROMATIN CONDENSATION; HISTONE MODIFICATION; INFERTILITY; SPERMATOGENESIS; SPERMIOGENESIS;

ANIMALS; CHROMATIN; DNA HELICASES; HISTONES; INFERTILITY, MALE; MALE; MICE; MICE, KNOCKOUT; MICROSCOPY, ELECTRON; SPERMATIDS; SPERMATOGENESIS; SPERMATOZOA; TESTIS;

EID: 84892372838     PISSN: 09254773     EISSN: 18726356     Source Type: Journal    
DOI: 10.1016/j.mod.2013.10.005     Document Type: Article

References (64)

1. Awe S., Renkawitz-Pohl R. Histone H4 acetylation is essential to proceed from a histone- to a protamine-based chromatin structure in spermatid nuclei of Drosophila melanogaster. Syst. Biol. Reprod. Med. 2010, 56:44-61.
2. Bagchi A., Papazoglu C., Wu Y., Capurso D., Brodt M., Francis D., Bredel M., Vogel H., Mills A.A. CHD5 is a tumor suppressor at human 1p36. Cell 2007, 128:459-475.
3. Bajpai R., Chen D.A., Rada-Iglesias A., Zhang J., Xiong Y., Helms J., Chang C.P., Zhao Y., Swigut T., Wysocka J. CHD7 cooperates with PBAF to control multipotent neural crest formation. Nature 2010, 463:958-962.
4. Beardsley A., Robertson D.M., O'Donnell L. A complex containing alpha6beta1-integrin and phosphorylated focal adhesion kinase between Sertoli cells and elongated spermatids during spermatid release from the seminiferous epithelium. J. Endocrinol. 2006, 190:759-770.
5. Cheng C.Y., Mruk D.D. Regulation of spermiogenesis, spermiation and blood-testis barrier dynamics: novel insights from studies on Eps8 and Arp3. Biochem. J. 2011, 435:553-562.
6. Chung S.S., Wang X., Wolgemuth D.J. Male sterility in mice lacking retinoic acid receptor alpha involves specific abnormalities in spermiogenesis. Differentiation 2005, 73:188-198.
7. D'Souza R., Pathak S., Upadhyay R., Gaonkar R., D'Souza S., Sonawane S., Gill-Sharma M., Balasinor N.H. Disruption of tubulobulbar complex by high intratesticular estrogens leading to failed spermiation. Endocrinology 2009, 150:1861-1869.
8. Dass B., Tardif S., Park J.Y., Tian B., Weitlauf H.M., Hess R.A., Carnes K., Griswold M.D., Small C.L., Macdonald C.C. Loss of polyadenylation protein tauCstF-64 causes spermatogenic defects and male infertility. Proc. Natl. Acad. Sci. USA 2007, 104:20374-20379.
9. Egan C.M., Nyman U., Skotte J., Streubel G., Turner S., O'Connell D.J., Rraklli V., Dolan M.J., Chadderton N., Hansen K., Farrar G.J., Helin K., Holmberg J., Bracken A.P. CHD5 is required for neurogenesis and has a dual role in facilitating gene expression and polycomb gene repression. Dev. Cell 2013, 26:223-236.
10. Forgione N., Vogl A.W., Varmuza S. Loss of protein phosphatase 1c{gamma} (PPP1CC) leads to impaired spermatogenesis associated with defects in chromatin condensation and acrosome development: an ultrastructural analysis. Reproduction 2010, 139:1021-1029.
11. Fujita T., Igarashi J., Okawa E.R., Gotoh T., Manne J., Kolla V., Kim J., Zhao H., Pawel B.R., London W.B., Maris J.M., White P.S., Brodeur G.M. CHD5, a tumor suppressor gene deleted from 1p36.31 in neuroblastomas. J. Natl. Cancer Inst. 2008, 100:940-949.
12. Garcia I., Mayol G., Rodriguez E., Sunol M., Gershon T.R., Rios J., Cheung N.K., Kieran M.W., George R.E., Perez-Atayde A.R., Casala C., Galvan P., de Torres C., Mora J., Lavarino C. Expression of the neuron-specific protein CHD5 is an independent marker of outcome in neuroblastoma. Mol. Cancer 2010, 9:277.
13. Gill-Sharma M.K., Choudhuri J., D'Souza S. Sperm chromatin protamination: an endocrine perspective. Protein Pept. Lett. 2011, 18:786-801.
14. Hall J.A., Georgel P.T. CHD proteins: a diverse family with strong ties. Biochem. Cell Biol. 2007, 85:463-476.
15. Hammadeh M.E., al-Hasani S., Doerr S., Stieber M., Rosenbaum P., Schmidt W., Diedrich K. Comparison between chromatin condensation and morphology from testis biopsy extracted and ejaculated spermatozoa and their relationship to ICSI outcome. Hum. Reprod. 1999, 14:363-367.
16. Hammoud S., Liu L., Carrell D.T. Protamine ratio and the level of histone retention in sperm selected from a density gradient preparation. Andrologia 2009, 41:88-94.
17. Hess R.A., Renato de Franca L. Spermatogenesis and cycle of the seminiferous epithelium. Adv. Exp. Med. Biol. 2008, 636:1-15.
18. Hong W., Nakazawa M., Chen Y.Y., Kori R., Vakoc C.R., Rakowski C., Blobel G.A. FOG-1 recruits the NuRD repressor complex to mediate transcriptional repression by GATA-1. EMBO J. 2005, 24:2367-2378.
19. Kashiwabara S., Noguchi J., Zhuang T., Ohmura K., Honda A., Sugiura S., Miyamoto K., Takahashi S., Inoue K., Ogura A., Baba T. Regulation of spermatogenesis by testis-specific, cytoplasmic poly(A) polymerase TPAP. Science 2002, 298:1999-2002.
20. Kierszenbaum A.L., Rivkin E., Tres L.L. Molecular biology of sperm head shaping. Soc. Reprod. Fertil. Suppl. 2007, 65:33-43.
21. Kierszenbaum A.L., Tres L.L. The acrosome-acroplaxome-manchette complex and the shaping of the spermatid head. Arch. Histol. Cytol. 2004, 67:271-284.
22. Kolla V., Higashi M., Zhuang T., Brodeur G.M. CHD5 (chromodomain helicase DNA binding protein 5). Atlas Genet. Cytogenet. Oncol. Haematol. 2012, 16:392-395.
23. Kunert N., Brehm A. Novel Mi-2 related ATP-dependent chromatin remodelers. Epigenetics 2009, 4:209-211.
24. Kurtz K., Saperas N., Ausio J., Chiva M. Spermiogenic nuclear protein transitions and chromatin condensation. Proposal for an ancestral model of nuclear spermiogenesis. J. Exp. Zool. B Mol. Dev. Evol. 2009, 312B:149-163.
25. Lahn B.T., Tang Z.L., Zhou J., Barndt R.J., Parvinen M., Allis C.D., Page D.C. Previously uncharacterized histone acetyltransferases implicated in mammalian spermatogenesis. Proc. Natl. Acad. Sci. USA 2002, 99:8707-8712.
26. Lie P.P., Mruk D.D., Lee W.M., Cheng C.Y. Epidermal growth factor receptor pathway substrate 8 (Eps8) is a novel regulator of cell adhesion and the blood-testis barrier integrity in the seminiferous epithelium. Faseb J. 2009, 23:2555-2567.
27. Lin Y.H., Chou C.K., Hung Y.C., Yu I.S., Pan H.A., Lin S.W., Kuo P.L. SEPT12 deficiency causes sperm nucleus damage and developmental arrest of preimplantation embryos. Fertil. Steril. 2011, 95:363-365.
28. Mali P., Kaipia A., Kangasniemi M., Toppari J., Sandberg M., Hecht N.B., Parvinen M. Stage-specific expression of nucleoprotein mRNAs during rat and mouse spermiogenesis. Reprod. Fertil. Dev. 1989, 1:369-382.
29. Marfella C.G., Imbalzano A.N. The Chd family of chromatin remodelers. Mutat. Res. 2007, 618:30-40.
30. McLachlan R.I., Wreford N.G., O'Donnell L., de Kretser D.M., Robertson D.M. The endocrine regulation of spermatogenesis: independent roles for testosterone and FSH. J. Endocrinol. 1996, 148:1-9.
31. Meistrich M.L., Trostle-Weige P.K., Russell L.D. Abnormal manchette development in spermatids of azh/azh mutant mice. Am. J. Anat. 1990, 188:74-86.
32. Mulero-Navarro S., Esteller M. Chromatin remodeling factor CHD5 is silenced by promoter CpG island hypermethylation in human cancer. Epigenetics 2008, 3:210-215.
33. O'Bryan M.K., Takada S., Kennedy C.L., Scott G., Harada S., Ray M.K., Dai Q., Wilhelm D., de Kretser D.M., Eddy E.M., Koopman P., Mishina Y. Sox8 is a critical regulator of adult Sertoli cell function and male fertility. Dev. Biol. 2008, 316:359-370.
34. O'Donnell L., Pratis K., Stanton P.G., Robertson D.M., McLachlan R.I. Testosterone-dependent restoration of spermatogenesis in adult rats is impaired by a 5alpha-reductase inhibitor. J. Androl. 1999, 20:109-117.
35. Okada Y., Tateishi K., Zhang Y. Histone demethylase JHDM2A is involved in male infertility and obesity. J. Androl. 2010, 31:75-78.
36. Oliva F. Protamines and male infertility. Hum. Reprod. Update 2006, 12:417-435.
37. Ouvrier A., Cadet R., Vernet P., Laillet B., Chardigny J.M., Lobaccaro J.M., Drevet J.R., Saez F. LXR and ABCA1 control cholesterol homeostasis in the proximal mouse epididymis in a cell-specific manner. J. Lipid Res. 2009, 50:1766-1775.
38. Perdrix A., Travers A., Chelli M.H., Escalier D., Do Rego J.L., Milazzo J.P., Mousset-Simeon N., Mace B., Rives N. Assessment of acrosome and nuclear abnormalities in human spermatozoa with large vacuoles. Hum. Reprod. 2011, 26:47-58.
39. Polychronidou, M., Grobhans, J., 2011. Determining nuclear shape: the role of farnesylated nuclear membrane proteins. Nucleus (Austin, Tex.) 2, 17-23.
40. Potts R.C., Zhang P., Wurster A.L., Precht P., Mughal M.R., Wood W.H., Zhang Y., Becker K.G., Mattson M.P., Pazin M.J. CHD5, a brain-specific paralog of Mi2 chromatin remodeling enzymes, regulates expression of neuronal genes. PLoS One 2011, 6:e24515.
41. Roest H.P., van Klaveren J., de Wit J., van Gurp C.G., Koken M.H., Vermey M., van Roijen J.H., Hoogerbrugge J.W., Vreeburg J.T., Baarends W.M., Bootsma D., Grootegoed J.A., Hoeijmakers J.H. Inactivation of the HR6B ubiquitin-conjugating DNA repair enzyme in mice causes male sterility associated with chromatin modification. Cell 1996, 86:799-810.
42. Russell L.D., Russell J.A., MacGregor G.R., Meistrich M.L. Linkage of manchette microtubules to the nuclear envelope and observations of the role of the manchette in nuclear shaping during spermiogenesis in rodents. Am. J. Anat. 1991, 192:97-120.
43. Sadek A., Almohamdy A.S., Zaki A., Aref M., Ibrahim S.M., Mostafa T. Sperm chromatin condensation in infertile men with varicocele before and after surgical repair. Fertil. Steril. 2011, 95:1705-1708.
44. Saito M., Kumamoto K., Robles A.I., Horikawa I., Furusato B., Okamura S., Goto A., Yamashita T., Nagashima M., Lee T.L., Baxendale V.J., Rennert O.M., Takenoshita S., Yokota J., Sesterhenn I.A., Trivers G.E., Hussain S.P., Harris C.C. Targeted disruption of Ing2 results in defective spermatogenesis and development of soft-tissue sarcomas. PLoS One 2010, 5:e15541.
45. Shimi T., Butin-Israeli V., Adam S.A., Goldman R.D. Nuclear lamins in cell regulation and disease. Cold Spring Harb. Symp. Quant. Biol. 2010, 75:525-531.
46. Song N., Liu J., An S., Nishino T., Hishikawa Y., Koji T. Immunohistochemical analysis of histone H3 modifications in germ cells during mouse spermatogenesis. Acta Histochem. Cytochem. 2011, 44:183-190.
47. Sonnack V., Failing K., Bergmann M., Steger K. Expression of hyperacetylated histone H4 during normal and impaired human spermatogenesis. Andrologia 2002, 34:384-390.
48. Steilmann C., Cavalcanti M.C., Bergmann M., Kliesch S., Weidner W., Steger K. Aberrant mRNA expression of chromatin remodelling factors in round spermatid maturation arrest compared with normal human spermatogenesis. Mol. Hum. Reprod. 2010, 16:726-733.
49. Talebi A.R., Vahidi S., Aflatoonian A., Ghasemi N., Ghasemzadeh J., Firoozabadi R.D., Moein M.R. Cytochemical evaluation of sperm chromatin and DNA integrity in couples with unexplained recurrent spontaneous abortions. Andrologia 2012, 44:462-470. (Suppl 1). 10.1111/j.1439-0272.2011.01206.x.
50. Taranum S., Sur I., Muller R., Lu W., Rashmi R.N., Munck M., Neumann S., Karakesisoglou I., Noegel A.A. Cytoskeletal interactions at the nuclear envelope mediated by nesprins. Int. J. Cell Biol. 2012, 2012:736524.
51. Thompson B.A., Tremblay V., Lin G., Bochar D.A. CHD8 is an ATP-dependent chromatin remodeling factor that regulates beta-catenin target genes. Mol. Cell. Biol. 2008, 28:3894-3904.
52. Thompson P.M., Gotoh T., Kok M., White P.S., Brodeur G.M. CHD5, a new member of the chromodomain gene family, is preferentially expressed in the nervous system. Oncogene 2003, 22:1002-1011.
53. Vigodner M. Roles of small ubiquitin-related modifiers in male reproductive function. Int. Rev. Cell Mol. Biol. 2011, 288:227-259.
54. Wang J., Chen H., Fu S., Xu Z.M., Sun K.L., Fu W.N. The involvement of CHD5 hypermethylation in laryngeal squamous cell carcinoma. Oral Oncol. 2011, 47:601-608.
55. Wang X., Lau K.K., So L.K., Lam Y.W. CHD5 is down-regulated through promoter hypermethylation in gastric cancer. J. Biomed. Sci. 2009, 16:95.
56. Ward W.S. Function of sperm chromatin structural elements in fertilization and development. Mol. Hum. Reprod. 2010, 16:30-36.
57. Wong R.R., Chan L.K., Tsang T.P., Lee C.W., Cheung T.H., Yim S.F., Siu N.S., Lee S.N., Yu M.Y., Chim S.S., Wong Y.F., Chung T.K. CHD5 downregulation associated with poor prognosis in epithelial ovarian cancer. Gynecol. Obstet. Invest. 2011, 72(3):203-207. 10.1159/000323883.
58. Xia X., Cai H., Qin S., Xu C. Histone acetylase inhibitor curcumin impairs mouse spermiogenesis-an in vitro study. PLoS One 2012, 7:e48673.
59. Yan W. Male infertility caused by spermiogenic defects: lessons from gene knockouts. Mol. Cell. Endocrinol. 2009, 306:24-32.
60. Yan W., Si Y., Slaymaker S., Li J., Zheng H., Young D.L., Aslanian A., Saunders L., Verdin E., Charo I.F. Zmynd15 encodes a histone deacetylase-dependent transcriptional repressor essential for spermiogenesis and male fertility. J. Biol. Chem. 2010, 285:31418-31426.
61. Yap K.L., Zhou M.M. Structure and mechanisms of lysine methylation recognition by the chromodomain in gene transcription. Biochemistry 2011, 50:1966-1980.
62. Zhang Z., Shen X., Gude D.R., Wilkinson B.M., Justice M.J., Flickinger C.J., Herr J.C., Eddy E.M., Strauss J.F. MEIG1 is essential for spermiogenesis in mice. Proc. Natl. Acad. Sci. USA 2009, 106:17055-17060.
63. Zhao M., Shirley C.R., Hayashi S., Marcon L., Mohapatra B., Suganuma R., Behringer R.R., Boissonneault G., Yanagimachi R., Meistrich M.L. Transition nuclear proteins are required for normal chromatin condensation and functional sperm development. Genesis 2004, 38:200-213.
64. Zhuang T., Kashiwabara S., Noguchi J., Baba T. Transgenic expression of testis-specific poly(A) polymerase TPAP in wild-type and TPAP-deficient mice. J. Reprod. Dev. 2004, 50:207-213.