A G-quadruplex DNA structure resolvase, RHAU, is essential for spermatogonia differentiation

Cell Death and Disease

Volumn 6, Issue 1, 2015, Pages

  Gao, X ^a   Ma, W ^b   Nie, J ^a   Zhang, C ^b   Zhang, J ^a   Yao, G ^b   Han, J ^a   Xu, J ^a   Hu, B ^a   Du, Y ^a   Shi, Q ^c   Yang, Z ^a   Huang, X ^a   Zhang, Y ^b,d  

^a NANJING UNIVERSITY   (China)

^b INSTITUTE OF BIOCHEMISTRY AND CELL BIOLOGY   (China)

^c UNIVERSITY OF SCIENCE AND TECHNOLOGY OF CHINA   (China)

^d SHANGHAI INSTITUTE OF PLANNED PARENTHOOD RESEARCH   (China)

Author keywords

[No Author keywords available]

Indexed keywords

G QUADRUPLEX DNA STRUCTURE RESOLVASE; GUANINE QUADRUPLEX; RESOLVASE; RNA HELICASE; UNCLASSIFIED DRUG; ADENOSINE TRIPHOSPHATE; DEAD BOX PROTEIN; DHX36 PROTEIN, MOUSE; DNA; PROTEIN BINDING; RECOMBINASE; STEM CELL FACTOR RECEPTOR;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; AU RICH ELEMENT; AZOOSPERMIA; CELL DIFFERENTIATION; CELL PROLIFERATION; CONTROLLED STUDY; DNA STRUCTURE; DOWN REGULATION; FLOW CYTOMETRY; GENE EXPRESSION; IMMUNOFLUORESCENCE; IMMUNOHISTOCHEMISTRY; MOUSE; NONHUMAN; NUCLEOTIDE MOTIF; PRIORITY JOURNAL; PROTEIN LOCALIZATION; QUANTITATIVE ANALYSIS; REAL TIME POLYMERASE CHAIN REACTION; RNA HELICASE ASSOCIATED WITH AU RICH ELEMENT; SPERMATOGONIUM; TESTIS DEVELOPMENT; WESTERN BLOTTING; ANIMAL; APOPTOSIS; CHEMISTRY; CYTOLOGY; DEFICIENCY; ENZYMOLOGY; GENE DELETION; GENE EXPRESSION REGULATION; GENETICS; KNOCKOUT MOUSE; MALE; MEIOSIS; METABOLISM; MOLECULAR GENETICS; NUCLEOTIDE SEQUENCE; PATHOLOGY; PROMOTER REGION; STEM CELL; TESTIS;

ADENOSINE TRIPHOSPHATE; ANIMALS; APOPTOSIS; AZOOSPERMIA; BASE SEQUENCE; CELL DIFFERENTIATION; CELL PROLIFERATION; DEAD-BOX RNA HELICASES; DNA; G-QUADRUPLEXES; GENE DELETION; GENE EXPRESSION REGULATION; MALE; MEIOSIS; MICE; MICE, KNOCKOUT; MOLECULAR SEQUENCE DATA; NUCLEOTIDE MOTIFS; PROMOTER REGIONS, GENETIC; PROTEIN BINDING; PROTO-ONCOGENE PROTEINS C-KIT; RECOMBINASES; SPERMATOGONIA; STEM CELLS; TESTIS;

EID: 84927644246     PISSN: None     EISSN: 20414889     Source Type: Journal    
DOI: 10.1038/cddis.2014.571     Document Type: Article

References (70)

1. Huppert JL. Structure, location and interactions of G-quadruplexes. The FEBS J 2010; 277: 3452-3458.
2. Bochman ML, Paeschke K, Zakian VA. DNA secondary structures: stability and function of G-quadruplex structures. Nat Rev Genet 2012; 13: 770-780.
3. Williamson JR, Raghuraman MK, Cech TR. Monovalent cation-induced structure of telomeric DNA: the G-quartet model. Cell 1989; 59: 871-880.
4. Wilson WD, Sugiyama H. First International Meeting on Quadruplex DNA. ACS Chem Biol 2007; 2: 589-594.
5. Gellert M, Lipsett MN, Davies DR. Helix formation by guanylic acid. Proc Natl Acad Sci USA 1962; 48: 2013-2018.
6. Biffi G, Tannahill D, McCafferty J, Balasubramanian S. Quantitative visualization of DNA G-quadruplex structures in human cells. Nat Chem 2013; 5: 182-186.
7. Henderson A, Wu Y, Huang YC, Chavez EA, Platt J, Johnson FB et al. Detection of G-quadruplex DNA in mammalian cells. Nucleic Acids Res 2014; 42: 860-869.
8. Eddy J, Maizels N. Gene function correlates with potential for G4 DNA formation in the human genome. Nucleic Acids Res 2006; 34: 3887-3896.
9. Eddy J, Maizels N. Conserved elements with potential to form polymorphic G-quadruplex structures in the first intron of human genes. Nucleic Acids Res 2008; 36: 1321-1333.
10. Huppert JL, Balasubramanian S. Prevalence of quadruplexes in the human genome. Nucleic Acids Res 2005; 33: 2908-2916.
11. Todd AK, Johnston M, Neidle S. Highly prevalent putative quadruplex sequence motifs in human DNA. Nucleic Acids Res 2005; 33: 2901-2907.
12. Cahoon LA, Seifert HS. An alternative DNA structure is necessary for pilin antigenic variation in Neisseria gonorrhoeae. Science 2009; 325: 764-767.
13. Cheung I, Schertzer M, Rose A, Lansdorp PM. Disruption of dog-1 in Caenorhabditis elegans triggers deletions upstream of guanine-rich DNA. Nat Genet 2002; 31: 405-409.
14. Rodriguez R, Miller KM, Forment JV, Bradshaw CR, Nikan M, Britton S et al. Smallmolecule-induced DNA damage identifies alternative DNA structures in human genes. Nat Chem Biol 2012; 8: 301-310.
15. Siddiqui-Jain A, Grand CL, Bearss DJ, Hurley LH. Direct evidence for a G-quadruplex in a promoter region and its targeting with a small molecule to repress c-MYC transcription. Proc Natl Acad Sci USA 2002; 99: 11593-11598.
16. Baran N, Pucshansky L, Marco Y, Benjamin S, Manor H. The SV40 large T-antigen helicase can unwind four stranded DNA structures linked by G-quartets. Nucleic Acids Res 1997; 25: 297-303.
17. Mohaghegh P, Karow JK, Brosh RM Jr., Bohr VA, Hickson ID. The Bloom's and Werner's syndrome proteins are DNA structure-specific helicases. Nucleic Acids Res 2001; 29: 2843-2849.
18. Creacy SD, Routh ED, Iwamoto F, Nagamine Y, Akman SA, Vaughn JP. G4 Resolvase 1 Binds Both DNA and RNA Tetramolecular Quadruplex with High Affinity and Is the Major Source of Tetramolecular Quadruplex G4-DNA and G4-RNA Resolving Activity in HeLa Cell Lysates. J Biol Chem 2008; 283: 34626-34634.
19. Vaughn JP, Creacy SD, Routh ED, Joyner-Butt C, Jenkins GS, Pauli S et al. The DEXH protein product of the DHX36 gene is the major source of tetramolecular quadruplex G4-DNA resolving activity in HeLa cell lysates. J Biol Chem 2005; 280: 38117-38120.
20. Chakraborty P, Grosse F. Human DHX9 helicase preferentially unwinds RNA-containing displacement loops (R-loops) and G-quadruplexes. DNA Repair 2011; 10: 654-665.
21. Capo-Chichi JM, Bharti SK, Sommers JA, Yammine T, Chouery E, Patry L et al. Identification and biochemical characterization of a novel mutation in DDX11 Causing Warsaw Breakage Syndrome. Hum Mutat 2013; 34: 103-107.
22. Vannier JB, Pavicic-Kaltenbrunner V, Petalcorin MI, Ding H, Boulton SJ. RTEL1 dismantles T loops and counteracts telomeric G4-DNA to maintain telomere integrity. Cell 2012; 149: 795-806.
23. Ribeyre C, Lopes J, Boule JB, Piazza A, Guedin A, Zakian VA et al. The yeast Pif1 helicase prevents genomic instability caused by G-quadruplex-forming CEB1 sequences in vivo. PLoS Genet 2009; 5: e1000475.
24. Chester N, Kuo F, Kozak C, O'Hara CD, Leder P. Stage-specific apoptosis, developmental delay, and embryonic lethality in mice homozygous for a targeted disruption in the murine Bloom's syndrome gene. Genes Dev 1998; 12: 3382-3393.
25. Lebel M, Leder P. A deletion within the murine Werner syndrome helicase induces sensitivity to inhibitors of topoisomerase and loss of cellular proliferative capacity. Proc Natl Acad Sci USA 1998; 95: 13097-13102.
26. Inoue A, Li TY, Roby SK, Valentine MB, Inoue M, Boyd K et al. Loss of ChlR1 helicase in mouse causes lethality due to the accumulation of aneuploid cells generated by cohesion defects and placental malformation. Cell Cycle 2007; 6: 1646-1654.
27. Ding H, Schertzer M, Wu X, Gertsenstein M, Selig S, Kammori M et al. Regulation of murine telomere length by Rtel: an essential gene encoding a helicase-like protein. Cell 2004; 117: 873-886.
28. Bochman ML, Sabouri N, Zakian VA. Unwinding the functions of the Pif1 family helicases. DNA Repair 2010; 9: 237-249.
29. Latypov V, Rothenberg M, Lorenz A, Octobre G, Csutak O, Lehmann E et al. Roles of Hop1 and Mek1 in meiotic chromosome pairing and recombination partner choice in Schizosaccharomyces pombe. Mol Cell Biol 2010; 30: 1570-1581.
30. De Muyt A, Jessop L, Kolar E, Sourirajan A, Chen JH, Dayani Y et al. BLM helicase ortholog Sgs1 is a central regulator of meiotic recombination intermediate metabolism. Mol Cell 2012; 46: 43-53.
31. Fu JJ, Li LY, Lu GX. Molecular cloning and characterization of human DDX36 and mouse Ddx36 genes, new members of the DEAD/H box superfamily. Sheng wu hua xue yu sheng wu wu li xue bao Acta biochimica et biophysica Sinica 2002; 34: 655-661.
32. Lattmann S, Giri B, Vaughn JP, Akman SA, Nagamine Y. Role of the amino terminal RHAU-specific motif in the recognition and resolution of guanine quadruplex-RNA by the DEAH-box RNA helicase RHAU. Nucleic Acids Res 2010; 38: 6219-6233.
33. Lai JC, Ponti S, Pan D, Kohler H, Skoda RC, Matthias P et al. The DEAH-box helicase RHAU is an essential gene and critical for mouse hematopoiesis. Blood 2012; 119: 4291-4300.
34. Gallardo T, Shirley L, John GB, Castrillon DH. Generation of a germ cell-specific mouse transgenic Cre line, Vasa-Cre. Genesis 2007; 45: 413-417.
35. Rogakou EP, Boon C, Redon C, Bonner WM. Megabase chromatin domains involved in DNA double-strand breaks in vivo. J Cell Biol 1999; 146: 905-916.
36. Lammers JHM, Offenberg HH, Vanaalderen M, Vink ACG, Dietrich AJJ, Heyting C. The gene encoding a major component of the lateral elements of synaptonemal complexes of the rat is related to X-linked lymphocyte-regulated genes. Mol Cell Biol 1994; 14: 1137-1146.
37. Baker SM, Plug AW, Prolla TA, Bronner CE, Harris AC, Yao X et al. Involvement of mouse Mlh1 in DNA mismatch repair and meiotic crossing over. Nat Genet 1996; 13: 336-342.
38. Shin YH, Choi Y, Erdin SU, Yatsenko SA, Kloc M, Yang F et al. Hormad1 mutation disrupts synaptonemal complex formation, recombination, and chromosome segregation in mammalian meiosis. PLoS Genet 2010; 6: e1001190.
39. Habu T, Taki T, West A, Nishimune Y, Morita T. The mouse and human homologs of DMC1, the yeast meiosis-specific homologous recombination gene, have a common unique form of exon-skipped transcript in meiosis. Nucleic Acids Res 1996; 24: 470-477.
40. Keeney S, Giroux CN, Kleckner N. Meiosis-specific DNA double-strand breaks are catalyzed by Spo11, a member of a widely conserved protein family. Cell 1997; 88: 375-384.
41. Anderson EL, Baltus AE, Roepers-Gajadien HL, Hassold TJ, de Rooij DG, van Pelt AM et al. Stra8 and its inducer, retinoic acid, regulate meiotic initiation in both spermatogenesis and oogenesis in mice. Proc Natl Acad Sci USA 2008; 105: 14976-14980.
42. Ruan HB, Zhang N, Gao X. Identification of a novel point mutation of mouse proto-oncogene c-kit through N-ethyl-N-nitrosourea mutagenesis. Genetics 2005; 169: 819-831.
43. Mark M, Jacobs H, Oulad-Abdelghani M, Dennefeld C, Feret B, Vernet N et al. STRA8-deficient spermatocytes initiate, but fail to complete, meiosis and undergo premature chromosome condensation. J Cell Sci 2008; 121: 3233-3242.
44. Barrios F, Filipponi D, Campolo F, Gori M, Bramucci F, Pellegrini M et al. SOHLH1 and SOHLH2 control Kit expression during postnatal male germ cell development. J Cell Sci 2012; 125: 1455-1464.
45. Buaas FW, Kirsh AL, Sharma M, McLean DJ, Morris JL, Griswold MD et al. Plzf is required in adult male germ cells for stem cell self-renewal. Nat Genet 2004; 36: 647-652.
46. Costoya JA, Hobbs RM, Barna M, Cattoretti G, Manova K, Sukhwani M et al. Essential role of Plzf in maintenance of spermatogonial stem cells. Nat Genet 2004; 36: 653-659.
47. Wainwright EN, Wilhelm D. The game plan: cellular and molecular mechanisms of mammalian testis development. Curr Topics Dev Biol 2010; 90: 231-262.
48. Zheng K, Wu X, Kaestner KH, Wang PJ. The pluripotency factor LIN28 marks undifferentiated spermatogonia in mouse. BMC Dev Biol 2009; 9: 38.
49. Oatley JM, Brinster RL. Regulation of spermatogonial stem cell self-renewal in mammals. Annu Rev Cell Dev Biol 2008; 24: 263-286.
50. Mauduit C, Hamamah S, Benahmed M. Stem cell factor/c-kit system in spermatogenesis. Hum Reprod Update 1999; 5: 535-545.
51. Sikarwar AP, Reddy KV. siRNA-mediated silencing of c-kit in mouse primary spermatogonial cells induces cell cycle arrest. Oligonucleotides 2008; 18: 145-160.
52. Blume-Jensen P, Jiang G, Hyman R, Lee KF, O'Gorman S, Hunter T. Kit/stem cell factor receptor-induced activation of phosphatidylinositol 3'-kinase is essential for male fertility. Nat Genet 2000; 24: 157-162.
53. Zhang R, Lin Y, Zhang CT. Greglist: a database listing potential G-quadruplex regulated genes. Nucleic Acids Res 2008; 36: D372-D376.
54. Rankin S, Reszka AP, Huppert J, Zloh M, Parkinson GN, Todd AK et al. Putative DNA quadruplex formation within the human c-kit oncogene. J Am Chem Soc 2005; 127: 10584-10589.
55. Fernando H, Reszka AP, Huppert J, Ladame S, Rankin S, Venkitaraman AR et al. A conserved quadruplex motif located in a transcription activation site of the human c-kit oncogene. Biochemistry 2006; 45: 7854-7860.
56. Lattmann S, Stadler MB, Vaughn JP, Akman SA, Nagamine Y. The DEAH-box RNA helicase RHAU binds an intramolecular RNA G-quadruplex in TERC and associates with telomerase holoenzyme. Nucleic Acids Res 2011; 39: 9390-9404.
57. Sexton AN, Collins K. The 5' guanosine tracts of human telomerase RNA are recognized by the G-quadruplex binding domain of the RNA helicase DHX36 and function to increase RNA accumulation. Mol Cell Biol 2011; 31: 736-743.
58. Meier M, Patel TR, Booy EP, Marushchak O, Okun N, Deo S et al. Binding of G-quadruplexes to the N-terminal recognition domain of the RNA helicase associated with AU-rich Element (RHAU). J Biol Chem 2013; 288: 35014-35027.
59. Suzuki H, Ahn HW, Chu T, Bowden W, Gassei K, Orwig K et al. SOHLH1 and SOHLH2 coordinate spermatogonial differentiation. Dev Biol 2012; 361: 301-312.
60. Carlomagno G, van Bragt MP, Korver CM, Repping S, de Rooij DG, van Pelt AM. BMP4-induced differentiation of a rat spermatogonial stem cell line causes changes in its cell adhesion properties. Biol Reprod 2010; 83: 742-749.
61. Pellegrini M, Grimaldi P, Rossi P, Geremia R, Dolci S. Developmental expression of BMP4/ ALK3/SMAD5 signaling pathway in the mouse testis: a potential role of BMP4 in spermatogonia differentiation. J Cell Sci 2003; 116: 3363-3372.
62. Hao J, Yamamoto M, Richardson TE, Chapman KM, Denard BS, Hammer RE et al. Sohlh2 knockout mice are male-sterile because of degeneration of differentiating type A spermatogonia. Stem Cells 2008; 26: 1587-1597.
63. Schrans-Stassen BHGJ, Saunders PTK, Cooke HJ, de Rooij DG. Nature of the spermatogenic arrest in Dazl -/- mice. Biol Reprod 2001; 65: 771-776.
64. Yuan LB, Tian T, Chen Y, Yan SY, Xing XW, Zhang ZA et al. Existence of G-quadruplex structures in promoter region of oncogenes confirmed by G-quadruplex DNA cross-linking strategy. Sci Rep-Uk 2013; 3: 1811.
65. Litovkin KV, Ivanova OV, Bauer A, Hoheisel JD, Bubnov VV, Zaporozhan VN. Microarray study of gene expression in uterine leiomyoma. Exp Oncol 2008; 30: 106-111.
66. Huang W, Smaldino PJ, Zhang Q, Miller LD, Cao P, Stadelman K et al. Yin Yang 1 contains G-quadruplex structures in its promoter and 5'-UTR and its expression is modulated by G4 resolvase 1. Nucleic Acids Res 2012; 40: 1033-1049.
67. Rank G, Cerruti L, Simpson RJ, Moritz RL, Jane SM, Zhao Q. Identification of a PRMT5-dependent repressor complex linked to silencing of human fetal globin gene expression. Blood 2010; 116: 1585-1592.
68. Zhao Q, Rank G, Tan YT, Li H, Moritz RL, Simpson RJ et al. PRMT5-mediated methylation of histone H4R3 recruits DNMT3A, coupling histone and DNA methylation in gene silencing. Nat Struct Mol Biol 2009; 16: 304-311.
69. Ma W, Hu S, Yao G, Xie S, Ni M, Liu Q et al. An androgen receptor-microrna-29a regulatory circuitry in mouse epididymis. J Biol Chem 2013; 288: 29369-29381.
70. Giri B, Smaldino PJ, Thys RG, Creacy SD, Routh ED, Hantgan RR et al. G4 resolvase 1 tightly binds and unwinds unimolecular G4-DNA. Nucleic Acids Res 2011; 39: 7161-7178.