Caudal regression in adrenocortical dysplasia (acd) mice is caused by telomere dysfunction with subsequent p53-dependent apoptosis

Developmental Biology

Volumn 334, Issue 2, 2009, Pages 418-428

  Vlangos, Christopher N ^a   O'Connor, Bridget C ^a   Morley, Madeleine J ^a   Krause, Andrea S ^a   Osawa, Gail A ^a   Keegan, Catherine E ^a  

^a UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

Author keywords

Apoptosis; Caudal regression; Development; p53; Rescue; Telomere

Indexed keywords

PROTEIN P53;

ADRENAL CORTEX INSUFFICIENCY; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; APOPTOSIS; ARTICLE; BIRTH DEFECT; CELL MUTANT; CELL PROLIFERATION; CONTROLLED STUDY; EMBRYO; FEMALE; GENE DOSAGE; GENOMIC INSTABILITY; LIMB MALFORMATION; MALE; MOUSE; NONHUMAN; PHENOTYPE; POLYDACTYLY; PRIORITY JOURNAL; SIGNAL TRANSDUCTION; SKELETON MALFORMATION; TELOMERE; VERTEBRA MALFORMATION;

MUS;

EID: 70349270554     PISSN: 00121606     EISSN: 1095564X     Source Type: Journal    
DOI: 10.1016/j.ydbio.2009.07.038     Document Type: Article

References (61)

1. Adam J., Deans B., and Thacker J. A role for Xrcc2 in the early stages of mouse development. DNA Repair (Amst). 6 (2007) 224-234
2. Alter B.P., Rosenberg P.S., and Brody L.C. Clinical and molecular features associated with biallelic mutations in FANCD1/BRCA2. J. Med. Genet. 44 (2007) 1-9
3. Armstrong J.F., Kaufman M.H., Harrison D.J., and Clarke A.R. High-frequency developmental abnormalities in p53-deficient mice. Curr. Biol. 5 (1995) 931-936
4. Aulehla A., and Herrmann B.G. Segmentation in vertebrates: clock and gradient finally joined. Genes Dev. 18 (2004) 2060-2067
5. Aulehla A., Wehrle C., Brand-Saberi B., Kemler R., Gossler A., Kanzler B., and Herrmann B.G. Wnt3a plays a major role in the segmentation clock controlling somitogenesis. Dev. Cell 4 (2003) 395-406
6. Baatout S., Jacquet P., Michaux A., Buset J., Vankerkom J., Derradji H., Yan J., von Suchodoletz H., de Saint-Georges L., Desaintes C., and Mergeay M. Developmental abnormalities induced by X-irradiation in p53 deficient mice. In Vivo 16 (2002) 215-221
7. Beamer W.G., Sweet H.O., Bronson R.T., Shire J.G., Orth D.N., and Davisson M.T. Adrenocortical dysplasia: a mouse model system for adrenocortical insufficiency. J. Endocrinol. 141 (1994) 33-43
8. Bekaert S., Derradji H., De Meyer T., Michaux A., Buset J., Neefs M., Mergeay M., Jacquet P., Van Oostveldt P., and Baatout S. Telomere shortening is associated with malformation in p53-deficient mice after irradiation during specific stages of development. DNA Repair (Amst). 4 (2005) 1028-1037
9. Blasco M.A., Lee H.W., Hande M.P., Samper E., Lansdorp P.M., DePinho R.A., and Greider C.W. Telomere shortening and tumor formation by mouse cells lacking telomerase RNA. Cell 91 (1997) 25-34
10. Bohring A., Lewin S.O., Reynolds J.F., Voigtlander T., Rittinger O., Carey J.C., Kopernik M., Smith R., Zackai E.H., Leonard N.J., Gritter H.L., Bamforth J.S., Okun N., McLeod D.R., Super M., Powell P., Mundlos S., Hennekam R.C., van Langen I.M., Viskochil D.H., Wiedemann H.R., and Opitz J.M. Polytopic anomalies with agenesis of the lower vertebral column. Am. J. Med. Genet. 87 (1999) 99-114
11. Boreham D.R., Dolling J.A., Misonoh J., and Mitchel R.E. Radiation-induced teratogenic effects in fetal mice with varying Trp53 function: influence of prior heat stress. Radiat. Res. 158 (2002) 449-457
12. Celli G.B., and de Lange T. DNA processing is not required for ATM-mediated telomere damage response after TRF2 deletion. Nat. Cell Biol. 7 (2005) 712-718
13. Chiang Y.J., Hemann M.T., Hathcock K.S., Tessarollo L., Feigenbaum L., Hahn W.C., and Hodes R.J. Expression of telomerase RNA template, but not telomerase reverse transcriptase, is limiting for telomere length maintenance in vivo. Mol. Cell. Biol. 24 (2004) 7024-7031
14. Chiang Y.J., Kim S.H., Tessarollo L., Campisi J., and Hodes R.J. Telomere-associated protein TIN2 is essential for early embryonic development through a telomerase-independent pathway. Mol. Cell. Biol. 24 (2004) 6631-6634
15. Chin L., Artandi S.E., Shen Q., Tam A., Lee S.L., Gottlieb G.J., Greider C.W., and DePinho R.A. p53 deficiency rescues the adverse effects of telomere loss and cooperates with telomere dysfunction to accelerate carcinogenesis. Cell 97 (1999) 527-538
16. de Lange T. Shelterin: the protein complex that shapes and safeguards human telomeres. Genes Dev. 19 (2005) 2100-2110
17. Dubrulle J., and Pourquie O. Coupling segmentation to axis formation. Development 131 (2004) 5783-5793
18. Dubrulle J., McGrew M.J., and Pourquie O. FGF signaling controls somite boundary position and regulates segmentation clock control of spatiotemporal Hox gene activation. Cell 106 (2001) 219-232
19. Else T., Theisen B.K., Wu Y., Hutz J.E., Keegan C.E., Hammer G.D., and Ferguson D.O. Tpp1/Acd maintains genomic stability through a complex role in telomere protection. Chromosome Res. 15 (2007) 1001-1013
20. Frank K.M., Sharpless N.E., Gao Y., Sekiguchi J.M., Ferguson D.O., Zhu C., Manis J.P., Horner J., DePinho R.A., and Alt F.W. DNA ligase IV deficiency in mice leads to defective neurogenesis and embryonic lethality via the p53 pathway. Mol. Cell 5 (2000) 993-1002
21. Gao Y., Ferguson D.O., Xie W., Manis J.P., Sekiguchi J., Frank K.M., Chaudhuri J., Horner J., DePinho R.A., and Alt F.W. Interplay of p53 and DNA-repair protein XRCC4 in tumorigenesis, genomic stability and development. Nature 404 (2000) 897-900
22. Greco T.L., Takada S., Newhouse M.M., McMahon J.A., McMahon A.P., and Camper S.A. Analysis of the vestigial tail mutation demonstrates that Wnt-3a gene dosage regulates mouse axial development. Genes Dev. 10 (1996) 313-324
23. Guillemot F., and Joyner A.L. Dynamic expression of the murine Achaete-Scute homologue Mash-1 in the developing nervous system. Mech. Dev. 42 (1993) 171-185
24. Guo X., Deng Y., Lin Y., Cosme-Blanco W., Chan S., He H., Yuan G., Brown E.J., and Chang S. Dysfunctional telomeres activate an ATM-ATR-dependent DNA damage response to suppress tumorigenesis. EMBO J. 26 (2007) 4709-4719
25. Harrington L., and Robinson M.O. Telomere dysfunction: multiple paths to the same end. Oncogene 21 (2002) 592-597
26. He H., Wang Y., Guo X., Ramchandani S., Ma J., Shen M.F., Garcia D.A., Deng Y., Multani A.S., You M.J., and Chang S. Pot1b deletion and telomerase haploinsufficiency in mice initiate an ATR-dependent DNA damage response and elicit phenotypes resembling dyskeratosis congenita. Mol. Cell. Biol. 29 (2009) 229-240
27. Herrera E., Samper E., and Blasco M.A. Telomere shortening in mTR-/- embryos is associated with failure to close the neural tube. EMBO J. 18 (1999) 1172-1181
28. Herrmann B.G., Labeit S., Poustka A., King T.R., and Lehrach H. Cloning of the T gene required in mesoderm formation in the mouse. Nature 343 (1990) 617-622
29. Hockemeyer D., Daniels J.P., Takai H., and de Lange T. Recent expansion of the telomeric complex in rodents: two distinct POT1 proteins protect mouse telomeres. Cell 126 (2006) 63-77
30. Hockemeyer D., Palm W., Else T., Daniels J.P., Takai K.K., Ye J.Z., Keegan C.E., de Lange T., and Hammer G.D. Telomere protection by mammalian Pot1 requires interaction with Tpp1. Nat. Struct. Mol. Biol. 14 (2007) 754-761
31. Hockemeyer D., Palm W., Wang R.C., Couto S.S., and de Lange T. Engineered telomere degradation models dyskeratosis congenita. Genes Dev. 22 (2008) 1773-1785
32. Jones S.N., Roe A.E., Donehower L.A., and Bradley A. Rescue of embryonic lethality in Mdm2-deficient mice by absence of p53. Nature 378 (1995) 206-208
33. Jouve C., Palmeirim I., Henrique D., Beckers J., Gossler A., Ish-Horowicz D., and Pourquie O. Notch signalling is required for cyclic expression of the hairy-like gene HES1 in the presomitic mesoderm. Development 127 (2000) 1421-1429
34. Ju Z., and Rudolph K.L. Telomere dysfunction and stem cell ageing. Biochimie 90 (2008) 24-32
35. Kallen K., Mastroiacovo P., Castilla E.E., Robert E., and Kallen B. VATER non-random association of congenital malformations: study based on data from four malformation registers. Am. J. Med. Genet. 101 (2001) 26-32
36. Karlseder J., Kachatrian L., Takai H., Mercer K., Hingorani S., Jacks T., and de Lange T. Targeted deletion reveals an essential function for the telomere length regulator Trf1. Mol. Cell. Biol. 23 (2003) 6533-6541
37. Keegan C.E., Hutz J.E., Else T., Adamska M., Shah S.P., Kent A.E., Howes J.M., Beamer W.G., and Hammer G.D. Urogenital and caudal dysgenesis in adrenocortical dysplasia (acd) mice is caused by a splicing mutation in a novel telomeric regulator. Hum. Mol. Genet. 14 (2005) 113-123
38. Kimmel C.A., and Trammell C. A rapid procedure for routine double staining of cartilage and bone in fetal and adult animals. Stain Technol. 56 (1981) 271-273
39. Lee H.W., Blasco M.A., Gottlieb G.J., Horner II J.W., Greider C.W., and DePinho R.A. Essential role of mouse telomerase in highly proliferative organs. Nature 392 (1998) 569-574
40. Leitges M., Neidhardt L., Haenig B., Herrmann B.G., and Kispert A. The paired homeobox gene Uncx4.1 specifies pedicles, transverse processes and proximal ribs of the vertebral column. Development 127 (2000) 2259-2267
41. Mansouri A., Yokota Y., Wehr R., Copeland N.G., Jenkins N.A., and Gruss P. Paired-related murine homeobox gene expressed in the developing sclerotome, kidney, and nervous system. Dev. Dyn. 210 (1997) 53-65
42. Mansouri A., Voss A.K., Thomas T., Yokota Y., and Gruss P. Uncx4.1 is required for the formation of the pedicles and proximal ribs and acts upstream of Pax9. Development 127 (2000) 2251-2258
43. Martin-Rivera L., Herrera E., Albar J.P., and Blasco M.A. Expression of mouse telomerase catalytic subunit in embryos and adult tissues. Proc. Natl. Acad. Sci. U. S. A. 95 (1998) 10471-10476
44. Montes de Oca Luna R., Wagner D.S., and Lozano G. Rescue of early embryonic lethality in mdm2-deficient mice by deletion of p53. Nature 378 (1995) 203-206
45. Pani L., Horal M., and Loeken M.R. Rescue of neural tube defects in Pax-3-deficient embryos by p53 loss of function: implications for Pax-3-dependent development and tumorigenesis. Genes Dev. 16 (2002) 676-680
46. Parant J., Chavez-Reyes A., Little N.A., Yan W., Reinke V., Jochemsen A.G., and Lozano G. Rescue of embryonic lethality in Mdm4-null mice by loss of Trp53 suggests a nonoverlapping pathway with MDM2 to regulate p53. Nat. Genet. 29 (2001) 92-95
47. Quan L., and Smith D.W. The VATER association. Vertebral defects, anal atresia, T-E fistula with esophageal atresia, radial and renal dysplasia: a spectrum of associated defects. J. Pediatr. 82 (1973) 104-107
48. Rudolph K.L., Chang S., Lee H.W., Blasco M., Gottlieb G.J., Greider C., and DePinho R.A. Longevity, stress response, and cancer in aging telomerase-deficient mice. Cell 96 (1999) 701-712
49. Sah V.P., Attardi L.D., Mulligan G.J., Williams B.O., Bronson R.T., and Jacks T. A subset of p53-deficient embryos exhibit exencephaly. Nat. Genet. 10 (1995) 175-180
50. Sakai Y., Meno C., Fujii H., Nishino J., Shiratori H., Saijoh Y., Rossant J., and Hamada H. The retinoic acid-inactivating enzyme CYP26 is essential for establishing an uneven distribution of retinoic acid along the anterio-posterior axis within the mouse embryo. Genes Dev. 15 (2001) 213-225
51. Sun X., Mariani F.V., and Martin G.R. Functions of FGF signalling from the apical ectodermal ridge in limb development. Nature 418 (2002) 501-508
52. Takada S., Stark K.L., Shea M.J., Vassileva G., McMahon J.A., and McMahon A.P. Wnt-3a regulates somite and tailbud formation in the mouse embryo. Genes Dev. 8 (1994) 174-189
53. Truett G.E., Heeger P., Mynatt R.L., Truett A.A., Walker J.A., and Warman M.L. Preparation of PCR-quality mouse genomic DNA with hot sodium hydroxide and tris (HotSHOT). Biotechniques 29 52 (2000) 54
54. Van Maldergem L., Siitonen H.A., Jalkh N., Chouery E., De Roy M., Delague V., Muenke M., Jabs E.W., Cai J., Wang L.L., Plon S.E., Fourneau C., Kestila M., Gillerot Y., Megarbane A., and Verloes A. Revisiting the craniosynostosis-radial ray hypoplasia association: Baller-Gerold syndrome caused by mutations in the RECQL4 gene. J. Med. Genet. 43 (2006) 148-152
55. Wang B., Ohyama H., Haginoya K., Odaka T., Yamada T., and Hayata I. Prenatal radiation-induced limb defects mediated by Trp53-dependent apoptosis in mice. Radiat. Res. 154 (2000) 673-679
56. Wilson V., Rashbass P., and Beddington R.S. Chimeric analysis of T (Brachyury) gene function. Development 117 (1993) 1321-1331
57. Wu L., Multani A.S., He H., Cosme-Blanco W., Deng Y., Deng J.M., Bachilo O., Pathak S., Tahara H., Bailey S.M., Behringer R.R., and Chang S. Pot1 deficiency initiates DNA damage checkpoint activation and aberrant homologous recombination at telomeres. Cell 126 (2006) 49-62
58. Yamaguchi T.P., Takada S., Yoshikawa Y., Wu N., and McMahon A.P. T (Brachyury) is a direct target of Wnt3a during paraxial mesoderm specification. Genes Dev. 13 (1999) 3185-3190
59. Yang A., Kaghad M., Caput D., and McKeon F. On the shoulders of giants: p63, p73 and the rise of p53. Trends Genet. 18 (2002) 90-95
60. Zhivotovsky B., and Kroemer G. Apoptosis and genomic instability. Nat. Rev. Mol. Cell Biol. 5 (2004) 752-762
61. Zuzarte-Luis V., and Hurle J.M. Programmed cell death in the embryonic vertebrate limb. Semin. Cell Dev. Biol. 16 (2005) 261-269