An African-specific polymorphism in the TP53 gene impairs p53 tumor suppressor function in a mouse model

Genes and Development

Volumn 30, Issue 8, 2016, Pages 918-930

  Jennis, Matthew ^a,b   Kung, Che Pei ^a   Basu, Subhasree ^a   Budina Kolomets, Anna ^a   Leu, Julia I Ju ^c   Khaku, Sakina ^a   Scott, Jeremy P ^a   Cai, Kathy Q ^d   Campbell, Michelle R ^e   Porter, Devin K ^e   Wang, Xuting ^e   Bell, Douglas A ^e   Li, Xiaoxian ^f   Garlick, David S ^a   Liu, Qin ^a   Hollstein, Monica ^g   George, Donna L ^c   Murphy, Maureen E ^a  

^a WISTAR INSTITUTE   (United States)

^b DREXEL UNIVERSITY COLLEGE OF MEDICINE   (United States)

^c UNIVERSITY OF PENNSYLVANIA   (United States)

^d FOX CHASE CANCER CENTER   (United States)

^e NATIONAL INSTITUTE OF ENVIRONMENTAL HEALTH SCIENCES   (United States)

^f EMORY UNIVERSITY SCHOOL OF MEDICINE   (United States)

^g UNIVERSITY OF LEEDS   (United Kingdom)

Author keywords

Ferroptosis; Metabolism; P53; Polymorphism; Ser46 phosphorylation; Tumor suppression

Indexed keywords

CISPLATIN; PROTEIN P53; TUMOR SUPPRESSOR PROTEIN; CODON; PROTEIN BINDING;

AFRICAN; ANIMAL EXPERIMENT; ANIMAL MODEL; APOPTOSIS; ARTICLE; CANCER RISK; GENETIC POLYMORPHISM; GENETIC TRANSCRIPTION; GENETIC VARIABILITY; GENOTOXICITY; HUMAN; HUMAN CELL; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; TRANSACTIVATION; ANIMAL; BLACK PERSON; C57BL MOUSE; CELL DEATH; CELL LINE; CHEMISTRY; CODON; DISEASE MODEL; DRUG EFFECTS; GENETICS; LIVER CELL CARCINOMA; METABOLISM; NEOPLASM; RISK FACTOR; SINGLE NUCLEOTIDE POLYMORPHISM; TRANSCRIPTION INITIATION; TUMOR SUPPRESSOR GENE;

AFRICAN CONTINENTAL ANCESTRY GROUP; ANIMALS; CARCINOMA, HEPATOCELLULAR; CELL DEATH; CELL LINE; CISPLATIN; CODON; DISEASE MODELS, ANIMAL; GENES, P53; HUMANS; MICE; MICE, INBRED C57BL; NEOPLASMS; POLYMORPHISM, SINGLE NUCLEOTIDE; PROTEIN BINDING; RISK FACTORS; TRANSCRIPTIONAL ACTIVATION; TUMOR SUPPRESSOR PROTEIN P53;

EID: 84963814113     PISSN: 08909369     EISSN: 15495477     Source Type: Journal    
DOI: 10.1101/gad.275891.115     Document Type: Article

References (41)

1. Bandele OJ, Wang X, Campbell MR, Pittman GS, Bell DA. 2011. Human single-nucleotide polymorphisms alter p53 sequence-specific binding at gene regulatory elements. Nucleic Acids Res 39: 178-189.
2. Brady CA, Jiang D, Mello SS, Johnson TM, Jarvis LA, Kozak MM, Kenzelmann Broz D, Basak S, Park EJ, McLaughlin ME, et al. 2011. Distinct p53 transcriptional programs dictate acute DNA-damage responses and tumor suppression. Cell 145: 571-583.
3. Budanov AV. 2014. The role of tumor suppressor p53 in the antioxidant defense and metabolism. Subcell Biochem 85: 337-358.
4. Bulavin DV, Saito S, Hollander MC, Sakaguchi K, Anderson CW, Appella E, Fornace AJ Jr. 1999. Phosphorylation of human p53 by p38 kinase coordinates N-terminal phosphorylation and apoptosis in response to UV radiation. EMBO J 18: 6845-6854.
5. Dixon SJ, Stockwell BR. 2014. The role of iron and reactive oxygen species in cell death. Nat Chem Biol 10: 9-17.
6. Dixon SJ, Lemberg KM, Lamprecht MR, Skouta R, Zaitsev EM, Gleason CE, Patel DN, Bauer AJ, Cantley AM, Yang WS, et al. 2012. Ferroptosis: an iron-dependent form of nonapoptotic cell death. Cell 149: 1060-1072.
7. Dixon SJ,Winter GE, Musavi LS, Lee ED, Snijder B, Rebsamen M, Superti-Furga G, Stockwell BR. 2015. Human haploid cell genetics reveals roles for lipid metabolism genes in nonapoptotic cell death. ACS Chem Biol 10: 1604-1609.
8. Donehower LA, Harvey M, Slagle BL, McArthur MJ, Montgomery CA Jr, Butel JS, Bradley A. 1992. Mice deficient for p53 are developmentally normal but susceptible to spontaneous tumours. Nature 356: 215-221.
9. D'Orazi G, Cecchinelli B, Bruno T, Manni I, Higashimoto Y, Saito S,Gostissa M, Coen S, Marchetti A, Del Sal G, et al. 2002. Homeodomain-interacting protein kinase-2 phosphorylates p53 at Ser 46 and mediates apoptosis. Nat Cell Biol 4: 11-19.
10. Felley-Bosco E, Weston A, Cawley HM, Bennett WP, Harris CC. 1993. Functional studies of a germ-line polymorphism at codon 47 within the p53 gene. Am J Hum Genet 53: 752-759.
11. Feng L, Hollstein M, Xu Y. 2006. Ser46 phosphorylation regulates p53-dependent apoptosis and replicative senescence. Cell Cycle 5: 2812-2819.
12. Follis AV, Llambi F, Merritt P, Chipuk JE, Green DR, Kriwacki RW. 2015. Pin1-induced proline isomerization in cytosolic p53 mediates BAX activation and apoptosis. Mol Cell 59: 677-684.
13. Frank AK, Leu JI, Zhou Y, Devarajan K, Nedelko T, Klein-Szanto A,Hollstein M, Murphy ME. 2011. The codon 72 polymorphism of p53 regulates interaction with NF-κB and transactivation of genes involved in immunity and inflammation. Mol Cell Biol 31: 1201-1213.
14. Gao M, Monian P, Quadri N, Ramasamy R, Jiang X. 2015. Glutaminolysis and transferrin regulate ferroptosis. Mol Cell 59: 298-308.
15. Grochola LF, Zeron-Medina J, Meriaux S, Bond GL. 2010. Singlenucleotide polymorphisms in the p53 signaling pathway. Cold Spring Harb Perspect Biol 2: a001032.
16. Hernandez Losa J, Parada Cobo C, Guinea Viniegra J, Sanchez-Arevalo Lobo VJ, Ramon Y, Cajal S, Sanchez-Prieto R. 2003. Role of the p38 MAPK pathway in cisplatin-based therapy. Oncogene 22: 3998-4006.
17. Hofmann TG, Moller A, Sirma H, Zentgraf H, Taya Y, Droge W, Will H, Schmitz ML. 2002. Regulation of p53 activity by its interaction with homeodomain-interacting protein kinase-2. Nat Cell Biol 4: 1-10.
18. Hollstein M, Sidransky D, Vogelstein B, Harris CC. 1991. p53 mutations in human cancers. Science 253: 49-53.
19. Humbey O, Pimkina J, Zilfou JT, Jarnik M, Dominguez-Brauer C, Burgess DJ, Eischen CM, Murphy ME. 2008. The ARF tumor suppressor can promote the progression of some tumors. Cancer Res 68: 9608-9613.
20. Jiang L, Kon N, Li T, Wang SJ, Su T, Hibshoosh H, Baer R, GuW. 2015. Ferroptosis as a p53-mediated activity during tumour suppression. Nature 520: 57-62.
21. Kenzelmann Broz D, Spano Mello S, Bieging KT, Jiang D, Dusek RL, Brady CA, Sidow A, Attardi LD. 2013. Global genomic profiling reveals an extensive p53-regulated autophagy program contributing to key p53 responses. Genes Dev 27: 1016-1031.
22. Kruse JP, Gu W. 2008. SnapShot: p53 posttranslational modifications. Cell 133: 930-931 e931.
23. Lang GA, Iwakuma T, Suh YA, Liu G, Rao VA, Parant JM, Valentin-Vega YA, Terzian T, Caldwell LC, Strong LC, et al. 2004. Gain of function of a p53 hot spot mutation in a mouse model of Li-Fraumeni syndrome. Cell 119: 861-872.
24. Li X, Dumont P, Della Pietra A, Shetler C, Murphy ME. 2005. The codon 47 polymorphism in p53 is functionally significant. J Biol Chem 280: 24245-24251.
25. Li M, He Y, DuboisW, Wu X, Shi J, Huang J. 2012a. Distinct regulatory mechanisms and functions for p53-activated and p53-repressed DNA damage response genes in embryonic stem cells. Mol Cell 46: 30-42.
26. Li T, Kon N, Jiang L, Tan M, Ludwig T, Zhao Y, Baer R, Gu W. 2012b. Tumor suppression in the absence of p53-mediated cell-cycle arrest, apoptosis, and senescence. Cell 149: 1269-1283.
27. Li Y, Liu J, McLaughlin N, Bachvarov D, Saifudeen Z, El-Dahr SS. 2013. Genome-wide analysis of the p53 gene regulatory network in the developing mouse kidney. Physiol Genomics 45: 948-964.
28. Liu J, Zhang C, Lin M, Zhu W, Liang Y, Hong X, Zhao Y, Young KH, Hu W, Feng Z. 2014. Glutaminase 2 negatively regulates the PI3K/AKT signaling and shows tumor suppression activity in human hepatocellular carcinoma. Oncotarget 5: 2635-2647.
29. Luo JL, Yang Q, Tong WM, Hergenhahn M, Wang ZQ, Hollstein M. 2001. Knock-in mice with a chimeric human/murine p53 gene develop normally and show wild-type p53 responses to DNAdamaging agents: a new biomedical research tool. Oncogene 20: 320-328.
30. Malkin D, Jolly KW, Barbier N, Look AT, Friend SH, Gebhardt MC, Andersen TI, Borresen AL, Li FP, Garber J, et al. 1992. Germline mutations of the p53 tumor-suppressor gene in children and young adults with second malignant neoplasms. N Engl J Med 326: 1309-1315.
31. Noureddine MA, Menendez D, Campbell MR, Bandele OJ, Horvath MM, Wang X, Pittman GS, Chorley BN, Resnick MA, Bell DA. 2009. Probing the functional impact of sequence variation on p53-DNA interactions using a novel microsphere assay for protein-DNA binding with human cell extracts. PLoS Genet 5: e1000462.
32. Oda K, Arakawa H, Tanaka T, Matsuda K, Tanikawa C, Mori T, Nishimori H, Tamai K, Tokino T, Nakamura Y, et al. 2000. p53AIP1, a potentialmediator of p53-dependent apoptosis, and its regulation by Ser-46-phosphorylated p53. Cell 102: 849-862.
33. Pietsch EC, Humbey O, Murphy ME. 2006. Polymorphisms in the p53 pathway. Oncogene 25: 1602-1611.
34. Reinbold M, Luo JL, Nedelko T, Jerchow B, Murphy ME, Whibley C, Wei Q, Hollstein M. 2008. Common tumour p53 mutations in immortalized cells from Hupki mice heterozygous at codon. Oncogene 27: 2788-2794.
35. Sprowl JA, Lancaster CS, Pabla N, Hermann E, Kosloske AM, Gibson AA, Li L, Zeeh D, Schlatter E, Janke LJ, et al. 2014. Cisplatin-induced renal injury is independently mediated by OCT2 and p53. Clin Cancer Res 20: 4026-4035.
36. Su D, Wang X, Campbell MR, Song L, Safi A, Crawford GE, Bell DA. 2015. Interactions of chromatin context, binding site sequence content, and sequence evolution in stress-induced p53 occupancy and transactivation. PLoS Genet 11: e1004885.
37. Taira N, Nihira K, Yamaguchi T, Miki Y, Yoshida K. 2007. DYRK2 is targeted to the nucleus and controls p53 via Ser46 phosphorylation in the apoptotic response to DNA damage. Mol Cell 25: 725-738.
38. Vogelstein B, Lane D, Levine AJ. 2000. Surfing the p53 network. Nature 408: 307-310.
39. Vousden KH, Prives C. 2009. Blinded by the light: the growing complexity of p53. Cell 137: 413-431.
40. Yang WS, SriRamaratnam R, Welsch ME, Shimada K, Skouta R, Viswanathan VS, Cheah JH, Clemons PA, Shamji AF, Clish CB, et al. 2014. Regulation of ferroptotic cancer cell death by GPX4. Cell 156: 317-331.
41. Zhu Y, Regunath K, Jacq X, Prives C. 2013. Cisplatin causes cell death via TAB1 regulation of p53/MDM2/MDMX circuitry. Genes Dev 27: 1739-1751.