Using targeted transgenic reporter mice to study promoter-specific p53 transcriptional activity

Proceedings of the National Academy of Sciences of the United States of America

Volumn 109, Issue 5, 2012, Pages 1685-1690

  Goh, Amanda M ^a   Lim, Chin Yan ^b   Chiam, Poh Cheang ^a   Li, Ling ^a   Mann, Michael B ^c,d   Mann, Karen M ^c,d   Menendez, Sergio ^a   Lane, David P ^a  

^a AGENCY FOR SCIENCE   (Singapore)

^b INSTITUTE OF MEDICAL BIOLOGY   (Singapore)

^c INSTITUTE OF MOLECULAR AND CELL BIOLOGY   (Singapore)

^d HOUSTON METHODIST RESEARCH INSTITUTE   (United States)

Author keywords

Embryonic development; Reporter mouse models

Indexed keywords

ENHANCED GREEN FLUORESCENT PROTEIN; PROTEIN P21; PROTEIN P53; PUMA PROTEIN;

ANIMAL TISSUE; APOPTOSIS; ARTICLE; CELL CYCLE ARREST; EMBRYO; EMBRYO DEVELOPMENT; EMBRYONAL TISSUE; IN VITRO STUDY; IN VIVO STUDY; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; SENESCENCE; TRANSCRIPTION INITIATION; TRANSGENIC MOUSE;

ANIMALS; BLOTTING, WESTERN; EMBRYONIC DEVELOPMENT; FLOW CYTOMETRY; GENES, ERBB-1; GENES, P53; GENES, REPORTER; MICE; MICE, TRANSGENIC; PROMOTER REGIONS, GENETIC;

MUS;

EID: 84863177576     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1114173109     Document Type: Article

References (58)

1. Petitjean A, Achatz MI, Borresen-Dale AL, Hainaut P, Olivier M (2007) TP53 mutations in human cancers: Functional selection and impact on cancer prognosis and outcomes. Oncogene 26:2157-2165. (Pubitemid 46536647)
2. Jackson JG, Post SM, Lozano G (2011) Regulation of tissue- and stimulus-specific cell fate decisions by p53 in vivo. J Pathol 223:127-136.
3. Macleod KF, et al. (1995) p53-dependent and independent expression of p21 during cell growth, differentiation, and DNA damage. Genes Dev 9:935-944.
4. el-Deiry WS, et al. (1993) WAF1, a potential mediator of p53 tumor suppression. Cell 75:817-825.
5. Xiong Y, et al. (1993) p21 is a universal inhibitor of cyclin kinases. Nature 366:701-704. (Pubitemid 24036020)
6. Jackson JG, Pereira-Smith OM (2006) p53 is preferentially recruited to the promoters of growth arrest genes p21 and GADD45 during replicative senescence of normal human fibroblasts. Cancer Res 66:8356-8360. (Pubitemid 44449144)
7. Yu J, Zhang L, Hwang PM, Kinzler KW, Vogelstein B (2001) PUMA induces the rapid apoptosis of colorectal cancer cells. Mol Cell 7:673-682. (Pubitemid 32706358)
8. Nakano K, Vousden KH (2001) PUMA, a novel proapoptotic gene, is induced by p53. Mol Cell 7:683-694. (Pubitemid 32706359)
9. Han J, et al. (2001) Expression of bbc3, a pro-apoptotic BH3-only gene, is regulated by diverse cell death and survival signals. Proc Natl Acad Sci USA 98:11318-11323. (Pubitemid 32928726)
10. Yu J, Wang Z, Kinzler KW, Vogelstein B, Zhang L (2003) PUMA mediates the apoptotic response to p53 in colorectal cancer cells. Proc Natl Acad Sci USA 100:1931-1936. (Pubitemid 36254551)
11. Villunger A, et al. (2003) p53- and drug-induced apoptotic responses mediated by BH3-only proteins puma and noxa. Science 302:1036-1038. (Pubitemid 37386194)
12. Hemann MT, et al. (2004) Suppression of tumorigenesis by the p53 target PUMA. Proc Natl Acad Sci USA 101:9333-9338. (Pubitemid 38812876)
13. Jeffers JR, et al. (2003) Puma is an essential mediator of p53-dependent and -independent apoptotic pathways. Cancer Cell 4:321-328. (Pubitemid 37329796)
14. Qiu W, et al. (2008) PUMA regulates intestinal progenitor cell radiosensitivity and gastrointestinal syndrome. Cell Stem Cell 2:576-583. (Pubitemid 351729214)
15. Fei P, Bernhard EJ, El-Deiry WS (2002) Tissue-specific induction of p53 targets in vivo. Cancer Res 62:7316-7327. (Pubitemid 36025255)
16. Resnick-Silverman L, St Clair S, Maurer M, Zhao K, Manfredi JJ (1998) Identification of a novel class of genomic DNA-binding sites suggests a mechanism for selectivity in target gene activation by the tumor suppressor protein p53. Genes Dev 12: 2102-2107. (Pubitemid 28348033)
17. Bronson SK, et al. (1996) Single-copy transgenic mice with chosen-site integration. Proc Natl Acad Sci USA 93:9067-9072. (Pubitemid 26282019)
18. Palais G, et al. (2009) Targeted transgenesis at the HPRT locus: An efficient strategy to achieve tightly controlled in vivo conditional expression with the tet system. Physiol Genomics 37:140-146.
19. Jasin M, Moynahan ME, Richardson C (1996) Targeted transgenesis. Proc Natl Acad Sci USA 93:8804-8808. (Pubitemid 26281970)
20. Ménendez S, et al. (2011) MDM4 downregulates p53 transcriptional activity and response to stress during differentiation. Cell Cycle 10:1100-1108.
21. Vassilev LT, et al. (2004) In vivo activation of the p53 pathway by small-molecule antagonists of MDM2. Science 303:844-848. (Pubitemid 38174664)
22. Attardi LD, de Vries A, Jacks T (2004) Activation of the p53-dependent G1 checkpoint response in mouse embryo fibroblasts depends on the specific DNA damage inducer. Oncogene 23:973-980. (Pubitemid 38250943)
23. Gudkov AV, Komarova EA (2003) The role of p53 in determining sensitivity to radiotherapy. Nat Rev Cancer 3:117-129. (Pubitemid 37328879)
24. Bunz F, et al. (1999) Disruption of p53 in human cancer cells alters the responses to therapeutic agents. J Clin Invest 104:263-269.
25. Spike BT, Wahl GM (2011) p53, stem cells, and reprogramming: Tumor suppression beyond guarding the genome. Genes Cancer 2:404-419.
26. Gottlieb E, et al. (1997) Transgenic mouse model for studying the transcriptional activity of the p53 protein: Age- and tissue-dependent changes in radiation-induced activation during embryogenesis. EMBO J 16:1381-1390. (Pubitemid 27136103)
27. Hamstra DA, et al. (2006) Real-time evaluation of p53 oscillatory behavior in vivo using bioluminescent imaging. Cancer Res 66:7482-7489. (Pubitemid 44289202)
28. Komarova EA, et al. (1997) Transgenic mice with p53-responsive lacZ: p53 activity varies dramatically during normal development and determines radiation and drug sensitivity in vivo. EMBO J 16:1391-1400. (Pubitemid 27136104)
29. Wang W, El-Deiry WS (2003) Bioluminescent molecular imaging of endogenous and exogenous p53-mediated transcription in vitro and in vivo using an HCT116 human colon carcinoma xenograft model. Cancer Biol Ther 2:196-202.
30. Coates PJ, Lorimore SA, Rigat BA, Lane DP, Wright EG (2001) Induction of endogenous beta-galactosidase by ionizing radiation complicates the analysis of p53-LacZ transgenic mice. Oncogene 20:7096-7097. (Pubitemid 33052201)
31. Bouvard V, et al. (2000) Tissue and cell-specific expression of the p53-target genes: bax, fas, mdm2 and waf1/p21, before and following ionising irradiation in mice. Oncogene 19:649-660. (Pubitemid 30102916)
32. Burns TF, Bernhard EJ, El-Deiry WS (2001) Tissue specific expression of p53 target genes suggests a key role for KILLER/DR5 in p53-dependent apoptosis in vivo. Oncogene 20:4601-4612. (Pubitemid 32762432)
33. Coates PJ, Lorimore SA, Lindsay KJ, Wright EG (2003) Tissue-specific p53 responses to ionizing radiation and their genetic modification: The key to tissue-specific tumour susceptibility? J Pathol 201:377-388. (Pubitemid 37408258)
34. Murray-Zmijewski F, Slee EA, Lu X (2008) A complex barcode underlies the heterogeneous response of p53 to stress. Nat Rev Mol Cell Biol 9:702-712.
35. Vousden KH, Prives C (2009) Blinded by the light: The growing complexity of p53. Cell 137:413-431.
36. Veprintsev DB, Fersht AR (2008) Algorithm for prediction of tumour suppressor p53 affinity for binding sites in DNA. Nucleic Acids Res 36:1589-1598. (Pubitemid 351426111)
37. Weinberg RL, Veprintsev DB, Bycroft M, Fersht AR (2005) Comparative binding of p53 to its promoter and DNA recognition elements. J Mol Biol 348:589-596. (Pubitemid 40515671)
38. Melero R, et al. (2011) Electron microscopy studies on the quaternary structure of p53 reveal different binding modes for p53 tetramers in complex with DNA. Proc Natl Acad Sci USA 108:557-562.
39. Kenzelmann Broz D, Attardi LD (2010) In vivo analysis of p53 tumor suppressor function using genetically engineered mouse models. Carcinogenesis 31:1311-1318.
40. Tang Y, Zhao W, Chen Y, Zhao Y, Gu W (2008) Acetylation is indispensable for p53 activation. Cell 133:612-626. (Pubitemid 351636297)
41. Aladjem MI, et al. (1998) ES cells do not activate p53-dependent stress responses and undergo p53-independent apoptosis in response to DNA damage. Curr Biol 8: 145-155. (Pubitemid 28091572)
42. Hong Y, Stambrook PJ (2004) Restoration of an absent G1 arrest and protection from apoptosis in embryonic stem cells after ionizing radiation. Proc Natl Acad Sci USA 101: 14443-14448. (Pubitemid 39346768)
43. Solozobova V, Rolletschek A, Blattner C (2009) Nuclear accumulation and activation of p53 in embryonic stem cells after DNA damage. BMC Cell Biol 10:46.
44. Sabapathy K, Klemm M, Jaenisch R, Wagner EF (1997) Regulation of ES cell differentiation by functional and conformational modulation of p53. EMBO J 16: 6217-6229.
45. Xu D, et al. (2002) Ets1 is required for p53 transcriptional activity in UV-induced apoptosis in embryonic stem cells. EMBO J 21:4081-4093. (Pubitemid 34857440)
46. Schmid P, Lorenz A, Hameister H, Montenarh M (1991) Expression of p53 during mouse embryogenesis. Development 113:857-865. (Pubitemid 21900325)
47. Rinon A, et al. (2011) p53 coordinates cranial neural crest cell growth and epithelialmesenchymal transition/delamination processes. Development 138:1827-1838.
48. Martins CP, Brown-Swigart L, Evan GI (2006) Modeling the therapeutic efficacy of p53 restoration in tumors. Cell 127:1323-1334. (Pubitemid 44960417)
49. Ventura A, et al. (2007) Restoration of p53 function leads to tumour regression in vivo. Nature 445:661-665. (Pubitemid 46232887)
50. Xue W, et al. (2007) Senescence and tumour clearance is triggered by p53 restoration in murine liver carcinomas. Nature 445:656-660. (Pubitemid 46232886)
51. Issaeva N, et al. (2004) Small molecule RITA binds to p53, blocks p53-HDM-2 interaction and activates p53 function in tumors. Nat Med 10:1321-1328. (Pubitemid 40022713)
52. Shangary S, et al. (2008) Temporal activation of p53 by a specific MDM2 inhibitor is selectively toxic to tumors and leads to complete tumor growth inhibition. Proc Natl Acad Sci USA 105:3933-3938. (Pubitemid 351723502)
53. Christophorou MA, Ringshausen I, Finch AJ, Swigart LB, Evan GI (2006) The pathological response to DNA damage does not contribute to p53-mediated tumour suppression. Nature 443:214-217. (Pubitemid 44387609)
54. Feldser DM, et al. (2010) Stage-specific sensitivity to p53 restoration during lung cancer progression. Nature 468:572-575.
55. Junttila MR, et al. (2010) Selective activation of p53-mediated tumour suppression in high-grade tumours. Nature 468:567-571.
56. Jonkers J, et al. (2001) Synergistic tumor suppressor activity of BRCA2 and p53 in a conditional mouse model for breast cancer. Nat Genet 29:418-425. (Pubitemid 34326692)
57. Lewandoski M, Martin GR (1997) Cre-mediated chromosome loss in mice. Nat Genet 17:223-225.
58. Wong ES, et al. (2010) A simple procedure for the efficient derivation of mouse ES cells. Methods Enzymol 476:265-283.