The Clustered, Regularly Interspaced, Short Palindromic Repeats-associated endonuclease 9 (CRISPR/Cas9)-created MDM2 T309G mutation enhances vitreous-induced expression of MDM2 and proliferation and survival of cells

Journal of Biological Chemistry

Volumn 291, Issue 31, 2016, Pages 16339-16347

  Duan, Yajian ^a,b,d   Ma, Gaoen ^a,b   Huang, Xionggao ^a,b   D'Amore, Patricia A ^a,b   Zhang, Feng ^c   Lei, Hetian ^a,b  

^a SCHEPENS EYE RESEARCH INSTITUTE   (United States)

^b HARVARD MEDICAL SCHOOL   (United States)

^c HARVARD UNIVERSITY   (United States)

^d Shanxi Eye Hospital   (China)

Author keywords

[No Author keywords available]

Indexed keywords

ALDEHYDES; CELL PROLIFERATION; CYTOLOGY; GENES; MAMMALS; VIRUSES;

ADENO-ASSOCIATED VIRUS; ENDONUCLEASES; GENOMIC LOCUS; MAMMALIAN CELLS; MULTIPLE NUCLEOTIDES; NEXT-GENERATION SEQUENCING; RETINAL PIGMENT EPITHELIAL; STREPTOCOCCUS PYOGENES;

CELLS;

CLUSTERED REGULARLY INTERSPACED SHORT PALINDROMIC REPEAT ASSOCIATED ENDONUCLEASE 9; ENDONUCLEASE; PARVOVIRUS VECTOR; PROTEIN MDM2; PROTEIN P53; UNCLASSIFIED DRUG; MDM2 PROTEIN, HUMAN; TP53 PROTEIN, HUMAN;

ARTICLE; CELL PROLIFERATION; CELL SURVIVAL; CONTROLLED STUDY; GENE LOCUS; GENE MUTATION; GENOTYPE; HUMAN; HUMAN CELL; MDM2 GENE; NEXT GENERATION SEQUENCING; PRIORITY JOURNAL; PROTEIN EXPRESSION; RETINAL PIGMENT EPITHELIUM; SINGLE NUCLEOTIDE POLYMORPHISM; VITREOUS BODY; AMINO ACID SUBSTITUTION; ANIMAL; BIOSYNTHESIS; CRISPR CAS SYSTEM; DEPENDOPARVOVIRUS; ENZYMOLOGY; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; MISSENSE MUTATION; MOUSE; PATHOLOGY; VITREORETINOPATHY;

AMINO ACID SUBSTITUTION; ANIMALS; CELL PROLIFERATION; CRISPR-CAS SYSTEMS; DEPENDOVIRUS; GENE EXPRESSION REGULATION, ENZYMOLOGIC; HUMANS; MICE; MUTATION, MISSENSE; POLYMORPHISM, SINGLE NUCLEOTIDE; PROTO-ONCOGENE PROTEINS C-MDM2; RETINAL PIGMENT EPITHELIUM; TUMOR SUPPRESSOR PROTEIN P53; VITREORETINOPATHY, PROLIFERATIVE;

EID: 84979752539     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M116.729467     Document Type: Article

References (47)

1. Morescalchi, F., Duse, S., Gambicorti, E., Romano, M. R., Costagliola, C., and Semeraro, F. (2013) Proliferative vitreoretinopathy after eye injuries: an overexpression of growth factors and cytokines leading to a retinal keloid. Mediators Inflamm. 2013, 269787
2. Pastor-Idoate, S., Rodríguez-Hernández, I., Rojas, J., Fernández, I., García-Gutiérrez, M. T., Ruiz-Moreno, J. M., Rocha-Sousa, A., Ramkissoon, Y., Harsum, S., MacLaren, R. E., Charteris, D., VanMeurs, J. C., González-Sarmiento, R., Pastor, J. C., and Genetics on PVR Study Group (2013) The T309G MDM2 gene polymorphism is a novel risk factor for proliferative vitreoretinopathy. PLoS ONE 8, e82283
3. Lei, H., Rheaume, M. A., Cui, J., Mukai, S., Maberley, D., Samad, A., Matsubara, J., and Kazlauskas, A. (2012) A novel function of p53: a gatekeeper of retinal detachment. Am. J. Pathol. 181, 866-874
4. Lei, H., Qian, C. X., Lei, J., Haddock, L. J., Mukai, S., and Kazlauskas, A. (2015) RasGAP promotes autophagy and thereby suppresses platelet-derived growth factor receptor-mediated signaling events, cellular responses, and pathology. Mol. Cell Biol. 35, 1673-1685
5. Casaroli-Marano, R. P., Pagan, R., and Vilaró, S. (1999) Epithelial-mesenchymal transition in proliferative vitreoretinopathy: intermediate filament protein expression in retinal pigment epithelial cells. Invest. Ophthalmol. Vis. Sci. 40, 2062-2072
6. Connor, T. B., Jr., Roberts, A. B., Sporn, M. B., Danielpour, D., Dart, L. L., Michels, R. G., de Bustros, S., Enger, C., Kato, H., and Lansing, M. (1989) Correlation of fibrosis and transforming growth factor-β type 2 levels in the eye. J. Clin. Invest. 83, 1661-1666
7. Leaver, P. K., and Billington, B. M. (1989) Vitrectomy and fluid/silicone-oil exchange for giant retinal tears: 5 years follow-up. Graefes Arch. Clin. Exp. Ophthalmol. 227, 323-327
8. Cui, J., Lei, H., Samad, A., Basavanthappa, S., Maberley, D., Matsubara, J., and Kazlauskas, A. (2009) PDGF receptors are activated in human epiretinal membranes. Exp. Eye Res. 88, 438-444
9. Haupt, Y., Maya, R., Kazaz, A., and Oren, M. (1997) Mdm2 promotes the rapid degradation of p53. Nature 387, 296-299
10. Oliner, J. D., Kinzler, K. W., Meltzer, P. S., George, D. L., and Vogelstein, B. (1992) Amplification of a gene encoding a p53-associated protein in human sarcomas. Nature 358, 80-83
11. Vassilev, L. T., Vu, B. T., Graves, B., Carvajal, D., Podlaski, F., Filipovic, Z., Kong, N., Kammlott, U., Lukacs, C., Klein, C., Fotouhi, N., and Liu, E. A. (2004) In vivo activation of the p53 pathway by small-molecule antagonists of MDM2. Science 303, 844-848
12. Jones, S. N., Roe, A. E., Donehower, L. A., and Bradley, A. (1995) Rescue of embryonic lethality in Mdm2-deficient mice by absence of p53. Nature 378, 206-208
13. Montes de Oca Luna, R., Wagner, D. S., and Lozano, G. (1995) Rescue of early embryonic lethality in mdm2-deficient mice by deletion of p53. Nature 378, 203-206
14. Lei, H., Velez, G., and Kazlauskas, A. (2011) Pathological signaling via platelet-derived growth factor receptor α involves chronic activation of Akt and suppression of p53. Mol. Cell Biol. 31, 1788-1799
15. Bond, G. L., Hu, W., Bond, E. E., Robins, H., Lutzker, S. G., Arva, N. C., Bargonetti, J., Bartel, F., Taubert, H., Wuerl, P., Onel, K., Yip, L., Hwang, S. J., Strong, L. C., Lozano, G., and Levine, A. J. (2004) A single nucleotide polymorphism in the MDM2 promoter attenuates the p53 tumor suppressor pathway and accelerates tumor formation in humans. Cell 119, 591-602
16. Uhrinova, S., Uhrin, D., Powers, H., Watt, K., Zheleva, D., Fischer, P., McInnes, C., and Barlow, P. N. (2005) Structure of free MDM2 N-terminal domain reveals conformational adjustments that accompany p53-binding. J. Mol. Biol. 350, 587-598
17. Boersma, B. J., Howe, T. M., Goodman, J. E., Yfantis, H. G., Lee, D. H., Chanock, S. J., and Ambs, S. (2006) Association of breast cancer outcome with status of p53 and MDM2 SNP309. J. Natl. Cancer Inst. 98, 911-919
18. Bougeard, G., Baert-Desurmont, S., Tournier, I., Vasseur, S., Martin, C., Brugieres, L., Chompret, A., Bressac-de Paillerets, B., Stoppa-Lyonnet, D., Bonaiti-Pellie, C., and Frebourg, T. (2006) Impact of the MDM2 SNP309 and p53 Arg72Pro polymorphism on age of tumour onset in Li-Fraumeni syndrome. J. Med. Genet. 43, 531-533
19. Yu, H., Huang, Y. J., Liu, Z., Wang, L. E., Li, G., Sturgis, E. M., Johnson, D. G., and Wei, Q. (2011) Effects of MDM2 promoter polymorphisms and p53 codon 72 polymorphism on risk and age at onset of squamous cell carcinoma of the head and neck. Mol. Carcinog. 50, 697-706
20. Wang, L. H., Wang, X., Xu, W. T., and Hu, Y. L. (2014) MDM2 rs2279744 polymorphism and endometrial cancer: a meta-analysis. Tumour Biol. 35, 3167-3170
21. Gao, J., Kang, A. J., Lin, S., Dai, Z. J., Zhang, S. Q., Liu, D., Zhao, Y., Yang, P. T., Wang, M., and Wang, X. J. (2014) Association between MDM2 rs 2279744 polymorphism and breast cancer susceptibility: a meta-analysis based on 9,788 cases and 11,195 controls. Ther. Clin. Risk Manag. 10, 269-277
22. Jansen, R., Embden, J. D., Gaastra, W., and Schouls, L. M. (2002) Identification of genes that are associated with DNA repeats in prokaryotes. Mol. Microbiol. 43, 1565-1575
23. Barrangou, R., Fremaux, C., Deveau, H., Richards, M., Boyaval, P., Moineau, S., Romero, D. A., and Horvath, P. (2007) CRISPR provides acquired resistance against viruses in prokaryotes. Science 315, 1709-1712
24. Jinek, M., Chylinski, K., Fonfara, I., Hauer, M., Doudna, J. A., and Charpentier, E. (2012) A programmable dual-RNA-guided DNA endonuclease in adaptive bacterial immunity. Science 337, 816-821
25. Wang, T., Wei, J. J., Sabatini, D. M., and Lander, E. S. (2014) Genetic screens in human cells using the CRISPR-Cas9 system. Science 343, 80-84
26. Maruyama, T., Dougan, S. K., Truttmann, M. C., Bilate, A. M., Ingram, J. R., and Ploegh, H. L. (2015) Increasing the efficiency of precise genome editing with CRISPR-Cas9 by inhibition of nonhomologous end joining. Nat. Biotechnol. 33, 538-542
27. Sander, J. D., and Joung, J. K. (2014) CRISPR-Cas systems for editing, regulating and targeting genomes. Nat. Biotechnol. 32, 347-355
28. Mali, P., Yang, L., Esvelt, K. M., Aach, J., Guell, M., DiCarlo, J. E., Norville, J. E., and Church, G. M. (2013) RNA-guided human genome engineering via Cas9. Science 339, 823-826
29. Hsu, P. D., Lander, E. S., and Zhang, F. (2014) Development and applications of CRISPR-Cas9 for genome engineering. Cell 157, 1262-1278
30. Swiech, L., Heidenreich, M., Banerjee, A., Habib, N., Li, Y., Trombetta, J., Sur, M., and Zhang, F. (2015) In vivo interrogation of gene function in the mammalian brain using CRISPR-Cas9. Nat. Biotechnol. 33, 102-106
31. Xue, W., Chen, S., Yin, H., Tammela, T., Papagiannakopoulos, T., Joshi, N. S., Cai, W., Yang, G., Bronson, R., Crowley, D. G., Zhang, F., Anderson, D. G., Sharp, P. A., and Jacks, T. (2014) CRISPR-mediated direct mutation of cancer genes in the mouse liver. Nature 514, 380-384
32. Yin, H., Xue, W., Chen, S., Bogorad, R. L., Benedetti, E., Grompe, M., Koteliansky, V., Sharp, P. A., Jacks, T., and Anderson, D. G. (2014) Genome editing with Cas9 in adult mice corrects a disease mutation and phenotype. Nat. Biotechnol. 32, 551-553
33. Maguire, A. M., Simonelli, F., Pierce, E. A., Pugh, E. N., Jr., Mingozzi, F., Bennicelli, J., Banfi, S., Marshall, K. A., Testa, F., Surace, E. M., Rossi, S., Lyubarsky, A., Arruda, V. R., Konkle, B., Stone, E., et al. (2008) Safety and efficacy of gene transfer for Leber's congenital amaurosis. N. Engl. J. Med. 358, 2240-2248
34. Zarrin, A. A., Malkin, L., Fong, I., Luk, K. D., Ghose, A., and Berinstein, N. L. (1999) Comparison of CMV, RSV, SV40 viral and Vλ1 cellular promoters in B and T lymphoid and non-lymphoid cell lines. Biochim. Biophys. Acta 1446, 135-139
35. Ran, F. A., Hsu, P. D., Lin, C. Y., Gootenberg, J. S., Konermann, S., Trevino, A. E., Scott, D. A., Inoue, A., Matoba, S., Zhang, Y., and Zhang, F. (2013) Double nicking by RNA-guided CRISPR Cas9 for enhanced genome editing specificity. Cell 154, 1380-1389
36. Scherer, S. E., Muzny, D. M., Buhay, C. J., Chen, R., Cree, A., Ding, Y., Dugan-Rocha, S., Gill, R., Gunaratne, P., Harris, R. A., Hawes, A. C., Hernandez, J., Hodgson, A. V., Hume, J., Jackson, A., et al. (2006) The finished DNA sequence of human chromosome 12. Nature 440, 346-351
37. Lander, E. S., Linton, L. M., Birren, B., Nusbaum, C., Zody, M. C., Baldwin, J., Devon, K., Dewar, K., Doyle, M., FitzHugh, W., Funke, R., Gage, D., Harris, K., Heaford, A., Howland, J., et al. (2001) Initial sequencing and analysis of the human genome. Nature 409, 860-921
38. Lowe, T. M., and Eddy, S. R. (1997) tRNAscan-SE: a program for improved detection of transfer RNA genes in genomic sequence. Nucleic Acids Res. 25, 955-964
39. Ran, F. A., Hsu, P. D., Wright, J., Agarwala, V., Scott, D. A., and Zhang, F. (2013) Genome engineering using the CRISPR-Cas9 system. Nat. Protoc. 8, 2281-2308
40. Wang, H., Yang, H., Shivalila, C. S., Dawlaty, M. M., Cheng, A. W., Zhang, F., and Jaenisch, R. (2013) One-step generation of mice carrying mutations in multiple genes by CRISPR/Cas-mediated genome engineering. Cell 153, 910-918
41. Yang, H., Wang, H., Shivalila, C. S., Cheng, A. W., Shi, L., and Jaenisch, R. (2013) One-step generation of mice carrying reporter and conditional alleles by CRISPR/Cas-mediated genome engineering. Cell 154, 1370-1379
42. Milanini-Mongiat, J., Pouysségur, J., and Pagès, G. (2002) Identification of two Sp1 phosphorylation sites for p42/p44 mitogen-activated protein kinases: their implication in vascular endothelial growth factor gene transcription. J. Biol. Chem. 277, 20631-20639
43. Guo, A., Salomoni, P., Luo, J., Shih, A., Zhong, S., Gu, W., and Pandolfi, P. P. (2000) The function of PML in p53-dependent apoptosis. Nat. Cell Biol. 2, 730-736
44. Knudson, A. G., Jr. (1971) Mutation and cancer: statistical study of retinoblastoma. Proc. Natl. Acad. Sci. U.S.A. 68, 820-823
45. Ofir-Rosenfeld, Y., Boggs, K., Michael, D., Kastan, M. B., and Oren, M. (2008) Mdm2 regulates p53 mRNA translation through inhibitory interactions with ribosomal protein L26. Mol. Cell 32, 180-189
46. Ogawara, Y., Kishishita, S., Obata, T., Isazawa, Y., Suzuki, T., Tanaka, K., Masuyama, N., and Gotoh, Y. (2002) Akt enhances Mdm2-mediated ubiquitination and degradation of p53. J. Biol. Chem. 277, 21843-21850
47. Cong, L., Ran, F. A., Cox, D., Lin, S., Barretto, R., Habib, N., Hsu, P. D., Wu, X., Jiang, W., Marraffini, L. A., and Zhang, F. (2013) Multiplex genome engineering using CRISPR/Cas systems. Science 339, 819-823