RECQL4 regulates p53 function in vivo during skeletogenesis

Journal of Bone and Mineral Research

Volumn 30, Issue 6, 2015, Pages 1077-1089

  Lu, Linchao ^a   Harutyunyan, Karine ^a   Jin, Weidong ^a   Wu, Jianhong ^a   Yang, Tao ^b   Chen, Yuqing ^c,d   Joeng, Kyu Sang ^c   Bae, Yangjin ^c   Tao, Jianning ^c   Dawson, Brian C ^c,d   Jiang, Ming Ming ^c,d   Lee, Brendan ^c,d   Wang, Lisa L ^a  

^a TEXAS CHILDREN S CANCER CENTER   (United States)

^b VAN ANDEL RESEARCH INSTITUTE   (United States)

^c BAYLOR COLLEGE OF MEDICINE   (United States)

^d HOWARD HUGHES MEDICAL INSTITUTE   (United States)

Author keywords

cartilage; genetic animal models; RECQL4; Rothmund Thomson syndrome; skeletal development

Indexed keywords

ATM PROTEIN; ATR PROTEIN; CYCLIN DEPENDENT KINASE INHIBITOR 1A; HISTONE H2AX; PROTEIN MDM2; PROTEIN P53; RECQ HELICASE; RECQL4 HELICASE; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; BONE DEVELOPMENT; CANCER RISK; CARTILAGE CELL; CELL PROLIFERATION; CONTROLLED STUDY; CRANIOFACIAL SYNOSTOSIS; DNA DAMAGE; EMBRYO; FEMUR; FORELIMB; GENE MUTATION; GENOMIC INSTABILITY; GROWTH PLATE; IN VIVO STUDY; LIMB DEVELOPMENT; LIMB MALFORMATION; MESENCHYMAL STEM CELL; MOUSE; NONHUMAN; OSTEOSARCOMA; PROTEIN PHOSPHORYLATION; RIB CARTILAGE; ROTHMUND THOMSON SYNDROME; SENESCENCE; ANAL CANAL; ANIMAL; CONGENITAL MALFORMATION; DWARFISM; GENETICS; HEART SEPTUM DEFECT; HUMAN; METABOLISM; MUTATION; PATELLA; PATHOLOGY; RADIUS; TRANSGENIC MOUSE;

ANAL CANAL; ANIMALS; BONE DEVELOPMENT; CRANIOSYNOSTOSES; DWARFISM; HEART SEPTAL DEFECTS, ATRIAL; HUMANS; LIMB DEFORMITIES, CONGENITAL; MICE; MICE, TRANSGENIC; MUTATION; PATELLA; RADIUS; RECQ HELICASES; ROTHMUND-THOMSON SYNDROME; TUMOR SUPPRESSOR PROTEIN P53;

EID: 84929353694     PISSN: 08840431     EISSN: 15234681     Source Type: Journal    
DOI: 10.1002/jbmr.2436     Document Type: Article

References (45)

1. Chu WK, Hickson ID,. RecQ helicases: multifunctional genome caretakers. Nat Rev Cancer. 2009; 9 (9): 644-54.
2. Yu CE, Oshima J, Fu YH, et al., Positional cloning of the Werner's syndrome gene. Science. 1996; 272 (5259): 258-62.
3. Ellis NA, Groden J, FYe TZ, et al., The Bloom's syndrome gene product is homologous to RecQ helicases. Cell. 1995; 83 (4): 655-66.
4. Kitao S, Shimamoto A, Goto M, et al., Mutations in RECQL4 cause a subset of cases of Rothmund-Thomson syndrome. Nat Genet. 1999; 22 (1): 82-4.
5. Larizza L, Roversi G, Volpi L,. Rothmund-Thomson syndrome. Orphanet J Rare Dis. 2010; 5: 2.
6. Wang LL, Levy ML, Lewis RA, et al., Clinical manifestations in a cohort of 41 Rothmund-Thomson syndrome patients. Am J Med Genet. 2001; 102 (1): 11-17.
7. Mehollin-Ray AR, Kozinetz CA, Schlesinger AE, Guillerman RP, Wang LL,. Radiographic abnormalities in Rothmund-Thomson syndrome and genotype-phenotype correlation with RECQL4 mutation status. AJR Am J Roentgenol. 2008; 191 (2): W62-6.
8. Wang LL, Gannavarapu A, Kozinetz CA, et al., Association between osteosarcoma and deleterious mutations in the RECQL4 gene in Rothmund-Thomson syndrome. J Natl Cancer Inst. 2003; 95 (9): 669-74.
9. Siitonen HA, Kopra O, Kaariainen H, et al., Molecular defect of RAPADILINO syndrome expands the phenotype spectrum of RECQL diseases. Hum Mol Genet. 2003; 12 (21): 2837-44.
10. Siitonen HA, Sotkasiira J, Biervliet M, et al., The mutation spectrum in RECQL4 diseases. Eur J Hum Genet. 2008; 17 (2): 151-8.
11. Van Maldergem L, Siitonen HA, Jalkh N, et al., Revisiting the craniosynostosis-radial ray hypoplasia association: Baller-Gerold syndrome caused by mutations in the RECQL4 gene. J Med Genet. 2006; 43 (2): 148-52.
12. Bachrati CZ, Hickson ID,. RecQ helicases: suppressors of tumorigenesis premature aging. Biochem J. 2003; 374 (Pt 3): 577-606.
13. Croteau DL, Singh DK, Hoh FL, Lu H, Bohr VA,. RECQL4 in genomic instability and aging. Trends Genet. 2012; 28 (12): 624-31.
14. Sangrithi MN, Bernal JA, Madine M, et al., Initiation of DNA replication requires the RECQL4 protein mutated in Rothmund-Thomson syndrome. Cell. 2005; 121 (6): 887-98.
15. Thangavel S, Mendoza-Maldonado R, Tissino E, et al., Human RECQ1 and RECQ4 helicases play distinct roles in DNA replication initiation. Mol Cell Biol. 2010; 30 (6): 1382-96.
16. Xu X, Rochette PJ, Feyissa EA, Su TV, Liu Y,. MCM10 mediates RECQ4 association with MCM2-7 helicase complex during DNA replication. EMBO J. 2009; 28 (19): 2-7.
17. Fan W, Luo J,. RecQ4 facilitates UV light-induced DNA damage repair through interaction with nucleotide excision repair factor xeroderma pigmentosum group A (XPA). J Biol Chem. 2008; 283 (43): 29037-44.
18. Schurman SH, Hedayati M, Wang Z, et al., Direct and indirect roles of RECQL4 in modulating base excision repair capacity. Hum Mol Genet. 2009; 18 (18): 3470-83.
19. Singh DK, Karmakar P, Aamann M, et al., The involvement of human RECQL4 in DNA double-strand break repair. Aging Cell. 2010; 9 (3): 358-71.
20. Crevel G, Vo N, Crevel I, et al., Drosophila RecQ4 is directly involved in both DNA replication and the response to UV damage in S2 cells. PLoS One. 2012; 7 (11):e49505.
21. Ghosh AK, Rossi ML, Singh DK, et al., RECQL4, the protein mutated in Rothmund-Thomson syndrome, functions in telomere maintenance. J Biol Chem. 2012; 287 (1): 196-209.
22. Croteau DL, Rossi ML, Canugovi C, et al., RECQL4 localizes to mitochondria and preserves mitochondrial DNA integrity. Aging Cell. 2012; 11 (3): 456-66.
23. De S Kumari, Mudgal J, et al., RECQL4 is essential for the transport of p53 to mitochondria in normal human cells in the absence of exogenous stress. J Cell Sci. 2012; 125 (Pt 10): 2509-22.
24. Ichikawa K, Noda T, Furuichi Y,. [Preparation of the gene targeted knockout mice for human premature aging diseases, Werner syndrome, and Rothmund-Thomson syndrome caused by the mutation of DNA helicases]. Nippon Yakurigaku Zasshi. 2002; 119 (4): 219-26.
25. Hoki Y, Araki R, Fujimori A, et al., Growth retardation and skin abnormalities of the Recql4-deficient mouse. Hum Mol Genet. 2003; 12 (18): 2293-9.
26. Mann MB, Hodges CA, Barnes E, et al., Defective sister-chromatid cohesion, aneuploidy and cancer predisposition in a mouse model of type II Rothmund-Thomson syndrome. Hum Mol Genet. 2005; 14 (6): 813-25.
27. Logan M, Martin JF, Nagy A, et al., Expression of Cre Recombinase in the developing mouse limb bud driven by a Prxl enhancer. Genesis. 2002; 33 (2): 77-80.
28. Ovchinnikov DA, Deng JM, Ogunrinu G, Behringer RR,. Col2a1-directed expression of Cre recombinase in differentiating chondrocytes in transgenic mice. Genesis. 2000; 26 (2): 145-46.
29. Ford-Hutchinson AF, Ali Z, Lines SE, et al., Inactivation of Pten in osteo-chondroprogenitor cells leads to epiphyseal growth plate abnormalities and skeletal overgrowth. J Bone Miner Res. 2007; 22 (8): 1245-59.
30. Wang W, Nyman JS, Ono K, et al., Mice lacking Nf1 in osteochondroprogenitor cells display skeletal dysplasia similar to patients with neurofibromatosis type I. Hum Mol Genet. 2011; 20 (20): 3910-24.
31. Jonkers J, Meuwissen R, van Der GH, et al., Synergistic tumor suppressor activity of BRCA2 and p53 in a conditional mouse model for breast cancer. Nat Genet. 2001; 29 (4): 418-25.
32. Engin F, Yao Z, Yang T, et al., Dimorphic effects of Notch signaling in bone homeostasis. Nat Med. 2008; 14 (3): 299-305.
33. Livak KJ, Schmittgen TD,. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. Methods. 2001; 25 (4): 402-8.
34. Seo HS, Serra R,. Tgfbr2 is required for development of the skull vault. Dev Biol. 2009; 334 (2): 481-90.
35. Mah LJ, El-Osta A, Karagiannis TC,. GammaH2AX: a sensitive molecular marker of DNA damage and repair. Leukemia. 2010; 24 (4): 679-86.
36. Canman CE, Lim DS, Cimprich KA, et al., Activation of the ATM kinase by ionizing radiation and phosphorylation of p53. Science. 1998; 281 (5383): 1677-9.
37. Banin S, Moyal L, Shieh S, et al., Enhanced phosphorylation of p53 by ATM in response to DNA damage. Science. 1998; 281 (5383): 1674-7.
38. Tibbetts RS, Brumbaugh KM, Williams JM, et al., A role for ATR in the DNA damage-induced phosphorylation of p53. Genes Dev. 1999; 13 (2): 152-7.
39. Shieh SY, Ikeda M, Taya Y, Prives C,. DNA damage-induced phosphorylation of p53 alleviates inhibition by MDM2. Cell. 1997; 91 (3): 325-34.
40. Lu H, Fang EF, Sykora P, et al., Senescence induced by RECQL4 dysfunction contributes to Rothmund-Thomson syndrome features in mice. Cell Death Dis. 2014; 5:e1226.
41. Donehower LA, Harvey M, Slagle BL, et al., Mice deficient for p53 are developmentally normal but susceptible to spontaneous tumours. Nature. 1992; 356 (6366): 215-21.
42. Lengner CJ, Steinman HA, Gagnon J, et al., Osteoblast differentiation and skeletal development are regulated by Mdm2-p53 signaling. J Cell Biol. 2006; 172 (6): 909-21.
43. Wang X, Kua HY, Hu Y, et al., P53 functions as a negative regulator of osteoblastogenesis, osteoblast-dependent osteoclastogenesis, and bone remodeling. J Cell Biol. 2006; 172 (1): 115-25.
44. Wise CA, Chiang LC, Paznekas WA, et al., TCOF1 gene encodes a putative nucleolar phosphoprotein that exhibits mutations in Treacher Collins Syndrome throughout its coding region. Proc Natl Acad Sci U S.A. 1997; 94 (7): 3110-5.
45. Jones NC, Lynn ML, Gaudenz K, et al., Prevention of the neurocristopathy Treacher Collins syndrome through inhibition of p53 function. Nat Med. 2008; 14 (2): 125-33.