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Regulation of the p53 tumor suppressor protein

Gannon, H., Shen, Q., Donehower, L.A., Lyle, S., and Jones, S.N. (2011) Mdm2-p53 signaling regulates epidermal stem cell senescence and premature aging phenotypes in mouse skin. Dev. Biology (in press).

Regeling, A., Armata, H.L., Gallant, J., Jones, S.N., and Sluss, HK (2010) Mice defective in p53 nuclear localization signal 1 exhibit exencephaly. Transgenic Res. (in press).

Mason, E.F., Zhao, Y., Gorksha-Hicks, P., Coloff, J.L., Gannon, H., Jones, S.N. and Rathmell, J.C. (2010). Aerobic glycolysis suppresses p53 activity to provide selective protection from apoptosis upon loss of growth signals or inhibition of BCR-Abl. Cancer Res. 70:8066-76.

Sluss, H.K., Gannon, H., Shen, Q., Coles, A.H., Eischen, C.M., and Jones, S.N. (2010) Phosphorylation of p53 serine 18 upregulates apoptosis to suppress Myc-induced tumorigenesis. Mol. Cancer Res. 8: 216-222. [PMC2829875]

Li, S., Ezhevsky, S., Dewing, A., Cato, M., Scortegagna, M., Bhoumik, A., Brietwiewer, W., Braddock, D., Eroshkin, A., Qi, J., Chen, M., Kim, J., Jones, S., Jones, N., Rickert, RT., and Ronai, Z. (2010) Radiation sensitivity and genomic instability in ATM phospho-mutant ATF2 mice. Genes and Cancer Apr 1;1(4):316-330.

Zhang X., Lin, L., Guo, H., Yang, J., Jones, S.N., Jochemsen, A. and Lu, X. (2009) Phosphorylation and degradation of MdmX is inhibited by Wip1 phosphatase in the DNA damage response. Cancer Res. 69:7960-7968. [PMC2763051]

Matijasevic, Z., Krzywicka-Racka, A., Sluder, G., and Jones, S.H. (2008) MdmX regulates transformation and chromosomal stability in p53-deficient cells. Cell Cycle 7:2967-2973. [PMC2716213]

Mudhasani, R., Zhu, Z., Hutvagner, G., Eischen, C.M., Lyle, S., Hall, L., Lawrence, J., Imbalzano, A.N. and Jones, S.N. (2008) Loss of miRNA biogenesis induces p19-p53 signaling and senescence in primary cells. J. Cell Biology 181: 1055-1063. [PMC2442212]

Matijasevic, Z., Steinman, H.A., Hoover, K. and Jones, S.N. (2008) Mdm4 suppresses transformation and tumorigenesis in p53-deficient cells and mice by preventing spindle multipolarity and chromosome loss. Mol. Cell. Biol. 28:1265-1273. [PMC2258754]

Chang, L., Zhou, B., Hu, S., Guo, R., Liu, X., Jones, S.N., and Yen, Y. (2008) ATM-mediated serine 72 phosphorylation stabilizes ribonucleotide reductase small subunit p53R2 protein against MDM2 in DNA damage. Proc. Nat’l. Acad. Sci. USA. 105:18519-18524. [PMC2587585]

Wang, P., Lushnikova, T., Greiner, T.C., Jones, S.N. and Eischen, C.M. (2008) Elevated Mdm2 expression induces chromosomal instability and confers survival and growth advantage to B cells. Oncogene 27(11):1590-1598.

Armata, H.L., Garlick, D.S., Jones, S.N.* and Sluss, H.K.* (2007) The Ataxia-telangiectasia-mutated target site ser18 is required for p53-mediated tumor suppression. Cancer Res. 67:11696-11703. (*shared senior authorship).

Lu, X., Ma. O., Ngyuen, T-A., Jones, S.N., Oren, M., and Donehower, L.A. (2007) The Wip1 phosphatase acts as a gatekeeper in the p53-Mdm2 autoregulatory loop. Cancer Cell 12:342-354.

Frese K.K., Latorre, I., Chung S., Caruana G., Bernstein A., Justice M., Jones S.N., Donehower L.A., Garner C.C., and Javier R.T. (2006). Oncogenic Function for the Dlg1 Mammalian Homologue of the Drosophila Discs-Large Tumor Suppressor. EMBO J. 25:1406-1417.

Lengner, C.J., Steinman, H.A., Gagnon, J., Smith, T.W., Henderson, J.E., Kream B.E., Stein, G.S., Lian, J.B. and Jones, S.N. (2006). Osteoblast differentiation and skeletal development are regulated by Mdm2-p53 signaling. J. Cell Biology172:909-921. [PMC2063734]

Steinman, H.A, Hoover, K, Sands, A.T. and Jones, S.N. (2005). Rescue of Mdmx deficient mice by Mdm2 reveals overlapping functions of Mdm2 and Mdm4 during development. Oncogene 24:7935-7940.

Liang, H., Atkins, H., Abdel-Fattah, R, Jones, S.N. and Lunec, J. (2004). Genomic organization of the human MDM2 oncogene and its relationship to alternatively spliced mRNAs. Gene 338:217-223.

Rogoff, H., Pickering, M.T., Frame, F., Sanchez, Y., Jones, S., and Kowalik, T. (2004). Apoptosis associated with deregulated E2F activity is dependent on E2F1 and ATM/Nbs1/Chk2. Mol. Cell Biol. 24:2968-2977.

Sluss, H.K., Armata, H., Gallant, J., Zhu, Z., and Jones, S.N. (2004). Phosphorylation of serine 18 regulates distinct p53 functions in mice. Mol. Cell. Biol. 24:976-984.

Steinman, H., Burstein, E., Lengner, C., Gosselin, J., Pihan, G., Duckett, C.S. and Jones, S.N. (2004). An alternative splice form of Mdm2 induces p53-independent cell growth and tumorigenesis. J. Biol. Chem. 279:4877-4886.

Steinman, H., Sluss, H.K., Pihan, G., Sands, A., and Jones, S.N. (2004). Absence of p21 partially rescues Mdm4 loss and uncovers an anti-proliferative effect of Mdm4 on cell growth. Oncogene 23:303-306.

Moore, L., Venkatachalam. S., Vogel, H., Watt, J., Wu, C.-L., Steinman, H., Jones, S.N., and Donehower, L.A. (2003). Cooperativity of p19(Arf), Mdm2, and p53 in murine tumorigenesis. Oncogene 22:7831-7837.

Sluss, H and Jones, S.N. (2003). Analyzing p53 tumor suppressor functions in mice. Expert Opinion on Therapeutic Targets 7: 89-99.

Jones, S.N. and Donehower, L.A. (2002). Functional analysis of tumor suppressor genes in mice. Book chapter in Methods in Molecular Medicine: Tumor Suppressor Genes (ed. W. El-Deiry) Humana Press USA. 223:283-314.

Schonoff, C.M., Daou, M.C., Jones, S.N., Schiffer, C.A., and Ross, A.H. (2002). Nitric oxide mediated inhibition of Hdm2-p53 binding. Biochemistry 41:13570-13574.

Rogoff, H.A., Pickering, M.T., Debatis, M.E., Jones, S.N. and Kowalik, T.F. (2002). E2F1 Induces Phosphorylation of p53 that is Coincident with p53 Accumulation and Apoptosis. Mol. Cell Biol. 22:5308-5318

Steinman, H., and Jones, S.N. (2002). Generation of an Mdm2 conditional allele in mice. Genesis 32:142-144.

Tyner, S.D., Venkatachalam, S., Choi, J., Jones, S., Ghebranious, N., Igelmann, H., Lu, X., Soron, G., Cooper, B., Brayton, C., Karsenty, G., Bradley, A., and Donehower, L.A. (2002) p53 mutant mice that display early ageing-associated phenotypes. (2002). Nature 415: 45-53.

Fuchs, S.Y., Adler, V., Buschmann, T., Yin, Z., Wu, X., Jones, S.N. and Ronai, Z. (1998). JNK targets p53 ubiquitination and degradation in nonstressed cells. Genes & Dev. 12: 2658-2663.

Jones, S.N., Hancock, A.E., Vogel, H., Donehower, L.A. and Bradley, A. (1998). Overexpression of Mdm2 in transgenic mice reveals a p53-independent role for Mdm2 in tumorigenesis. Proc. Natl. Acad. Sci. USA. 95: 15608-15612.

Shi, Y.-P., Venkatachalam, S., Jones, S.N., Vogel, H., Bradley, A., Pinkel, D. and Donehower, L. A. (1998). Retention of the wild type p53 allele in tumors from p53 heterozygous mice: Is p53 an exception to the two hit hypothesis? EMBO J. 17: 4657-4667.

Kubbutat, M.H.G., Jones, S.N. and Vousden, K.H. (1997). Regulation of p53 stability by Mdm2. Nature 387: 299-303.

Jones, S.N., Sands, A., Hancock, A.E., Vogel, H., Donehower, L.A., Linke, S.P., Wahl, G.M. and Bradley, A. (1996). The tumorigenic potential and cell growth characteristics of p53-deficient cells are equivalent in the presence or absence of Mdm2. Proc. Natl. Acad. Sci. USA. 93: 14106-14111.

Jones, S.N., Ansari-Lari, M.A., Hancock, A.E., Jones, W.J., Gibbs, R.A., Donehower, L.A. and Bradley, A. (1996). Genomic organization of the mouse double minute 2 gene (Mdm2). Gene 175: 209-213.

Jones, S.N., Donehower, L.A., and Bradley, A. (1995). Analysis of tumor suppressor genes using transgenic mice. Methods: A Companion to Methods in Enzymology 8: 247-258. 

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.

Non-canonical Wnt signaling in development and cancer 

Liang, H., Coles, A.H., Zayas, ZJ, Jurecic, R., Kang, J. and Jones, S.N. (2007) Non-cannonical Wnt promotes apoptosis in thymocyte development. J. Exp. Med. 204:3077-3084. [PMC2150967]

Cha, K., Douglas, K., Potok, M.A., Liang, H., Jones, S.N., and Camper, S. (2004). Wingless signaling affects pituitary gland shape. Mech Dev. 121:183-194.

Liang, H., Chen, Q., Coles, A., Anderson, S., Pihan, G., Gerstein, R., Jureceic, R., and Jones, S.N. (2003). Wnt5a inhibits B cell proliferation and functions as a tumor suppressor in hematopoietic tissue. Cancer Cell 4:349-360.

Yamaguchi,T., Bradley, A., McMahon, A.E. and Jones, S. (1999). A Wnt5a pathway underlies outgrowth of multiple structures in the vertebrate embryo. Development 126: 1211-1223.

Epigenetic regulation of development and tumor suppressor functions

Mudhasani, R., Puri, V., Hoover, K., Czech, M., Imbalzano, A.N., and Jones, S.N. (2011) Dicer regulates white but not brown adipose formation in mice. J. Cell Phys. (in press).

Coles, A.H., Gannon, H., Cerny, A., Kurt-Jones, E. and Jones, S.N. (2010) Inhibitor of growth 4 promotes IkB promoter activation to suppress NFkB signaling and innate immunity. Proc. Natl. Acad. Sci. USA. 107:11423-11428.

Shin, J., Bossenz, M., Chung, Y., Ma, H., Bryon, M., Tanaguichi-Ishigaki, N., Jiao, B., Zhu, X., Jiao, B., Hall, L.L., Green, M.R., Jones, S.N., Hermans-Borgmeyer, I, Lawrence, J.B. and Bach, I. (2010). Maternal Rnf12/RLIM is required for imprinted X chromosome inactivation in mice. Nature 467:977-981.

Arrate, M.P., Vinvent, T., Odvody, J., Kar, R., Jones, S.N. and Eischen, C.M. (2010) MicroRNA biogenesis is required for Myc-induced B cell lymphoma development and survival. Cancer Res. 70:5083-5092.

Mallappa, C., Nasipak, B.T., Etheridge, L., Androphy, E.J., Jones, S.N., Sagerstrom, C., Ohkawa, Y., and Imbalzano, A.I. (2010) Myogenic microRNA expression requires ATP-dependent chromatin remodeling enzyme function. Mol. Cell. Biol. 30: 3176-3186.

Mudhasani, R., Imbalzano, A.N., and Jones, S.N. (2010) An essential role for Dicer in adipocyte differentiation. J. Cell. Biochem. 110:812-816.

Guar, T., Hussain, S., Mudhasani, R., Parulkar, I., van Wijnin, A.J., Stein J.L., Stein G.S., Jones, S.N., and Lian, J. (2010) Dicer inactivation in osteoprogenitor cells compromises fetal survival and bone formation, while excision in differentiated osteoblasts increases bone mass in the adult mouse. Dev. Biology 340:10-21.

Coles A.H. and Jones S.N. (2009) ING genes in the regulation of cell growth and tumorigenesis. J. Cell Physiology 218:45-57. [PMC2872195]

Coles, A.H., Marfella, C., Imbalzano, A.N., Steinman, H.A., Garlick, D.S., Gerstein, R.M. and Jones, S.N. (2008) p37Ing1 regulates B cell proliferation and cooperates with p53 to suppress diffuse large B cell lymphomas. Cancer Res. 68:8705-8714. [PMC287218]

Coles, A.H., Liang, H., Zhu, Z., Marfella, C., Kang, J., Imbalzano, A.N., and Jones, S.N. (2007) Deletion of p37Ing1 in mice reveals a p53-independent role for Ing1 in suppression of cell proliferation, apoptosis, and tumorigenesis. Cancer Res.67:2054-2061 [PMC287214]

Marfella, G.A., Ohkawa,Y., Coles, A.H., Garlick, D.S., Jones, S.N., and Imbalzano, A.N. (2006) Mutation of the SNF2 family member Chd2 affects mouse development and survival. J. Cell Phys. 209:162-171.

Guidi, C., Mudhasani. R., Hoover, K., Koff, A., Leav, I., Imbalzano, T., and Jones, SN. (2006) Functional interaction of the Rb and Ini1/Snf5 tumor suppressors in cell growth and pituitary tumorigenesis. Cancer Res. 66:8076-8082.

Doan, D.N., Veal, T.M., Yan, Z., Wang, W., Jones, S.N., and Imbalzano, A.N. (2004). Loss of the Ini1 tumor suppressor does not impair the expression of multiple Brg1-dependent genes or the assembly of Swi/Snf enzyme. Oncogene 23:3462-3473.

Guidi, C.J., Veal, T., Jones, S.N., and Imbalzano, A.N. (2004). Transcriptional compensation for loss of an allele of the Ini1 tumor suppressor. J. Biol. Chem. 279:4180-4185.

Imbalzano, A.N., and Jones, S.N. (2005). Snf5 tumor suppressor couples chromatin remodeling, checkpoint control, and chromosomal stability. Cancer Cell 7:294-295.

Guidi, C.J., Jones, S.N., and Imbalzano, A.N. (2002). Ini1 is essential for embryonic development and tumor suppression Chemtracts: Mol. Biol. & Biochem. 14:751-756. 

Guidi, C., Turner, T., Smith, T., Zambowski, B., Sands, A.S., Imbalzano, T., and Jones, S.N. (2001). Disruption of Ini1 leads to peri-implantation lethality and tumorigenesis in mice. Mol. Cell. Biol. 21:3598-3603.