The p53 pathway in hematopoiesis: lessons from mouse models, implications for humans

Surfing the p53 network

Vogelstein, B., Lane, D., & Levine, A. J. (2000) · Nature · doi:10.1038/35042675 · Cited by 6,607

Mice deficient for p53 are developmentally normal but susceptible to spontaneous tumours

Donehower, L. A., Harvey, M., Slagle, B. L., McArthur, M. J., Montgomery, C. A., Butel, J. S., & Bradley, A. (1992) · Nature · doi:10.1038/356215a0 · Cited by 4,649

Mdm2 promotes the rapid degradation of p53

Haupt, Y., Maya, R., Kazaz, A., & Oren, M. (1997) · Nature · doi:10.1038/387296a0 · Cited by 4,506

Germ Line p53 Mutations in a Familial Syndrome of Breast Cancer, Sarcomas, and Other Neoplasms

Malkin, D., Li, F. P., Strong, L. C., Fraumeni, J. F., Nelson, C. E., Kim, D. H., Kassel, J., Gryka, M. A., Bischoff, F. Z., Tainsky, M. A., et al. (1990) · Science · doi:10.1126/science.1978757 · Cited by 3,765

Regulation of p53 stability by Mdm2

Kubbutat, M. H. G., Jones, S. N., & Vousden, K. H. (1997) · Nature · doi:10.1038/387299a0 · Cited by 3,312

Live or let die: the cell's response to p53

Vousden, K. H., & Lü, X. (2002) · Nature reviews. Cancer · doi:10.1038/nrc864 · Cited by 3,231

SLAM Family Receptors Distinguish Hematopoietic Stem and Progenitor Cells and Reveal Endothelial Niches for Stem Cells

Kiel, M. J., Yilmaz, Ö. H., Iwashita, T., Yilmaz, O. H., Terhorst, C., & Morrison, S. J. (2005) · Cell · doi:10.1016/j.cell.2005.05.026 · Cited by 3,168

Blinded by the Light: The Growing Complexity of p53

Vousden, K. H., & Prives, C. (2009) · Cell · doi:10.1016/j.cell.2009.04.037 · Cited by 3,163

The mdm-2 oncogene product forms a complex with the p53 protein and inhibits p53-mediated transactivation

Momand, J., Zambetti, G. P., Olson, D. C., George, D., & Levine, A. J. (1992) · Cell · doi:10.1016/0092-8674(92)90644-r · Cited by 3,113

p53 is required for radiation-induced apoptosis in mouse thymocytes

Lowe, S. W., Schmitt, E. M., Smith, S. W., Osborne, B. A., & Jacks, T. (1993) · Nature · doi:10.1038/362847a0 · Cited by 2,864

A model for p53-induced apoptosis

Polyak, K., Xia, Y., Zweier, J. L., Kinzler, K. W., & Vogelstein, B. (1997) · Nature · doi:10.1038/38525 · Cited by 2,500

Thymocyte apoptosis induced by p53-dependent and independent pathways

Clarke, A. R., Purdie, C. A., Harrison, D. J., Morris, R. G., Bird, C. C., Hooper, M. L., & Wyllie, A. H. (1993) · Nature · doi:10.1038/362849a0 · Cited by 2,271

Long-Term Lymphohematopoietic Reconstitution by a Single CD34-Low/Negative Hematopoietic Stem Cell

Osawa, M., Hanada, K., Hamada, H., & Nakauchi, H. (1996) · Science · doi:10.1126/science.273.5272.242 · Cited by 2,141

Tumor spectrum analysis in p53-mutant mice

Jacks, T., Remington, L., Williams, B. O., Schmitt, E. M., Halachmi, S., Bronson, R. T., & Weinberg, R. A. (1994) · Current Biology · doi:10.1016/s0960-9822(00)00002-6 · Cited by 2,051

Activation of the ATM Kinase by Ionizing Radiation and Phosphorylation of p53

Canman, C. E., Lim, D.-S., Cimprich, K. A., Taya, Y., Tamai, K., Sakaguchi, K., Appella, E., Kastan, M. B., & Siliciano, J. D. (1998) · Science · doi:10.1126/science.281.5383.1677 · Cited by 2,042

Oncoprotein MDM2 is a ubiquitin ligase E3 for tumor suppressor p53

Honda, R., Tanaka, H., & Yasuda, H. (1997) · FEBS Letters · doi:10.1016/s0014-5793(97)01480-4 · Cited by 1,951

Amplification of a gene encoding a p53-associated protein in human sarcomas

Oliner, J. D., Kinzler, K. W., Meltzer, P. S., George, D. L., & Vogelstein, B. (1992) · Nature · doi:10.1038/358080a0 · Cited by 1,949

Enhanced Phosphorylation of p53 by ATM in Response to DNA Damage

Banin, S., Moyal, L., Shieh, S.-Y., Taya, Y., Anderson, C. W., Chessa, L., Smorodinsky, N. I., Prives, C., Reiss, Y., Shiloh, Y., et al. (1998) · Science · doi:10.1126/science.281.5383.1674 · Cited by 1,797

Senescence in premalignant tumours

Collado, M., Gil, J., Efeyan, A., Guerra, C., Schuhmacher, A. J., Barradas, M., Benguría, A., Zaballos, A., Flores, J. M., Barbacid, M., et al. (2005) · Nature · doi:10.1038/436642a · Cited by 1,482

p53 mutant mice that display early ageing-associated phenotypes

Tyner, S. D., Venkatachalam, S., Choi, J., Jones, S., Ghebranious, N., Igelmann, H., Lu, X., Soron, G., Cooper, B., Brayton, C., et al. (2002) · Nature · doi:10.1038/415045a · Cited by 1,459

Rescue of early embryonic lethality in mdm2-deficient mice by deletion of p53

de Oca Luna, R. M., Wagner, D. S., & Lozano, G. (1995) · Nature · doi:10.1038/378203a0 · Cited by 1,420

Hematopoietic Stem Cell Quiescence Maintained by p21 cip1/waf1

Cheng, T., Rodrigues, N., Shen, H., Yang, Y.-G., Dombkowski, D., Sykes, M., & Scadden, D. T. (2000) · Science · doi:10.1126/science.287.5459.1804 · Cited by 1,339

p53- and Drug-Induced Apoptotic Responses Mediated by BH3-Only Proteins Puma and Noxa

Villunger, A., Michalak, E. M., Coultas, L., Müllauer, F., Böck, G., Ausserlechner, M. J., Adams, J. M., & Strasser, A. (2003) · Science · doi:10.1126/science.1090072 · Cited by 1,327

DNA Damage-Induced Activation of p53 by the Checkpoint Kinase Chk2

Hirao, A., Kong, Y., Matsuoka, S., Wakeham, A. C., Ruland, J., Yoshida, H., Liu, D., Elledge, S. J., & Mak, T. W. (2000) · Science · doi:10.1126/science.287.5459.1824 · Cited by 1,311

Mutant p53 gain of function in two mouse models of Li-Fraumeni syndrome

Olive, K. P., Tuveson, D. A., Ruhe, Z. C., Yin, B., Willis, N. A., Bronson, R. T., Crowley, D., & Jacks, T. (2004) · Cell · doi:10.1016/j.cell.2004.11.004 · Cited by 1,308

Suppression of induced pluripotent stem cell generation by the p53–p21 pathway

Hong, H., Takahashi, K., Ichisaka, T., Aoi, T., Kanagawa, O., Nakagawa, M., Okita, K., & Yamanaka, S. (2009) · Nature · doi:10.1038/nature08235 · Cited by 1,301

Regulating the p53 pathway: in vitro hypotheses, in vivo veritas

Toledo, F., & Wahl, G. M. (2006) · Nature reviews. Cancer · doi:10.1038/nrc2012 · Cited by 1,286

Rescue of embryonic lethality in Mdm2-deficient mice by absence of p53

Jones, S. N., Roe, A. E., Donehower, L. A., & Bradley, A. (1995) · Nature · doi:10.1038/378206a0 · Cited by 1,280

Germ-line transmission of a mutated p53 gene in a cancer-prone family with Li–Fraumeni syndrome

Srivastava, S. K., Zou, Z., Pirollo, K. F., Blattner, W. A., & Chang, E. H. (1990) · Nature · doi:10.1038/348747a0 · Cited by 1,210

The antioxidant function of the p53 tumor suppressor

Sablina, A. A., Budanov, A. V., Ilyinskaya, G. V., Agapova, L. S., Kravchenko, J. E., & Chumakov, P. M. (2005) · Nature Medicine · doi:10.1038/nm1320 · Cited by 1,137

Linking the p53 tumour suppressor pathway to somatic cell reprogramming

Kawamura, T., Suzuki, J., Wang, Y. V., Menendez, S., Morera, L. B., Raya, A., Wahl, G. M., & Belmonte, J. C. I. (2009) · Nature · doi:10.1038/nature08311 · Cited by 1,115

Gain of function of a p53 hot spot mutation in a mouse model of Li-Fraumeni syndrome

Lang, G. A., Iwakuma, T., Suh, Y.-A., Liu, G., Rao, V. A., Parant, J. M., Valentin-Vega, Y. A., Terzian, T., Caldwell, L. C., Strong, L. C., et al. (2004) · Cell · doi:10.1016/j.cell.2004.11.006 · Cited by 1,069

Identification of RPS14 as a 5q- syndrome gene by RNA interference screen

Ebert, B. L., Pretz, J. L., Bosco, J., Chang, C. Y., Tamayo, P., Galili, N., Raza, A., Root, D. E., Attar, E. C., Ellis, S. R., et al. (2008) · Nature · doi:10.1038/nature06494 · Cited by 953

Puma is an essential mediator of p53-dependent and -independent apoptotic pathways

Jeffers, J. R., Parganas, E., Lee, Y., Yang, C., Wang, J., Brennan, J. A., Maclean, K. H., Han, J., Chittenden, T., Ihle, J. N., et al. (2003) · Cancer Cell · doi:10.1016/s1535-6108(03)00244-7 · Cited by 880

Ribosomopathies: human disorders of ribosome dysfunction

Narla, A., & Ebert, B. L. (2010) · Blood · doi:10.1182/blood-2009-10-178129 · Cited by 841

The gene encoding ribosomal protein S19 is mutated in Diamond-Blackfan anaemia

Draptchinskaia, N., Gustavsson, P., Andersson, B., Pettersson, M., Willig, T.-N., Dianzani, I., Ball, S., Tchernia, G., Klar, J., Matsson, H., et al. (1999) · Nature Genetics · doi:10.1038/5951 · Cited by 795

The Biology of Hematopoietic Stem Cells

Morrison, S. J., Uchida, N., & Weissman, I. L. (1995) · Annual Review of Cell and Developmental Biology · doi:10.1146/annurev.cb.11.110195.000343 · Cited by 794

Association of Spindle Assembly Checkpoint Component XMAD2 with Unattached Kinetochores

Chen, R., Waters, J. C., Salmon, E. D., & Murray, A. W. (1996) · Science · doi:10.1126/science.274.5285.242 · Cited by 783

The Tumor Suppressor p53 Regulates Polarity of Self-Renewing Divisions in Mammary Stem Cells

Cicalese, A., Bonizzi, G., Pasi, C. E., Faretta, M., Ronzoni, S., Giulini, B., Brisken, C., Minucci, S., Fiore, P. P. D., & Pelicci, P. G. (2009) · Cell · doi:10.1016/j.cell.2009.06.048 · Cited by 713

MDMX: a novel p53‐binding protein with some functional properties of MDM2.

Shvarts, A., Steegenga, W. T., Riteco, N., van Laar, T., Dekker, P., Bazuine, M., van Ham, R. C., van der Houven van Oordt, W., Hateboer, G., van der Eb, A. J., et al. (1996) · The EMBO Journal · doi:10.1002/j.1460-2075.1996.tb00919.x · Cited by 648

Inactivation of the p53 pathway in retinoblastoma

Laurie, N. A., Donovan, S. L., Shih, C.-S., Zhang, J., Mills, N., Fuller, C., Teunisse, A., Lam, S., Ramos, Y., Mohan, A., et al. (2006) · Nature · doi:10.1038/nature05194 · Cited by 595

The role of p53 in determining sensitivity to radiotherapy

Gudkov, A. V., & Komarova, E. A. (2003) · Nature reviews. Cancer · doi:10.1038/nrc992 · Cited by 581

p53 Regulates Hematopoietic Stem Cell Quiescence

Liu, Y., Elf, S. E., Miyata, Y., Sashida, G., Liu, Y., Huang, G., Di Giandomenico, S., Lee, J. M., Deblasio, A., Menendez, S., et al. (2009) · Cell Stem Cell · doi:10.1016/j.stem.2008.11.006 · Cited by 547

Gfi-1 restricts proliferation and preserves functional integrity of haematopoietic stem cells

Hock, H., Hamblen, M. J., Rooke, H. M., Schindler, J. W., Saleque, S., Fujiwara, Y., & Orkin, S. H. (2004) · Nature · doi:10.1038/nature02994 · Cited by 541

'Super p53' mice exhibit enhanced DNA damage response, are tumor resistant and age normally

García‐Cao, I., García‐Cao, M., Martín‐Caballero, J., Criado, L. M., Klatt, P., Flores, J. M., Weill, J., Blasco, M. A., & Serrano, M. (2002) · The EMBO Journal · doi:10.1093/emboj/cdf595 · Cited by 529

Rescue of embryonic lethality in Mdm4-null mice by loss of Trp53 suggests a nonoverlapping pathway with MDM2 to regulate p53

Parant, J., Chavez-Reyes, A., Little, N. A., Yan, W., Reinke, V., Jochemsen, A. G., & Lozano, G. (2001) · Nature Genetics · doi:10.1038/ng714 · Cited by 517

P53 and radiation responses

Fei, P., & El‐Deiry, W. S. (2003) · Oncogene · doi:10.1038/sj.onc.1206677 · Cited by 503

IARC Database of p53 gene mutations in human tumors and cell lines: updated compilation, revised formats and new visualisation tools

Hainaut, P. L. (1998) · Nucleic Acids Research · doi:10.1093/nar/26.1.205 · Cited by 446

Distinct haematological disorder with deletion of long arm of No. 5 chromosome

BERGHE, H. V. D., Cassiman, J., David, G., Fryns, J., Michaux, J., & SOKAL, G. (1974) · Nature · doi:10.1038/251437a0 · Cited by 442

p53 suppresses the self-renewal of adult neural stem cells

Meletis, K., Wirta, V., Hede, S., Nistér, M., Lundeberg, J., & Frisén, J. (2005) · Development · doi:10.1242/dev.02208 · Cited by 422

Haploinsufficiency for ribosomal protein genes causes selective activation of p53 in human erythroid progenitor cells

Dutt, S., Narla, A., Lin, K. I., Mullally, A., Abayasekara, N., Megerdichian, C., Wilson, F. H., Currie, T., Khanna‐Gupta, A., Berliner, N., et al. (2010) · Blood · doi:10.1182/blood-2010-07-295238 · Cited by 410

p53 at a glance

Brady, C. A., & Attardi, L. D. (2010) · Journal of Cell Science · doi:10.1242/jcs.064501 · Cited by 400

Overexpression of Mdm2 in mice reveals a p53-independent role for Mdm2 in tumorigenesis

Jones, S. N., Hancock, A. R., Vogel, H., Donehower, L. A., & Bradley, A. (1998) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.95.26.15608 · Cited by 386

The pathological response to DNA damage does not contribute to p53-mediated tumour suppression

Christophorou, M. A., Ringshausen, I., Finch, A. J., Swigart, L. B., & Evan, G. I. (2006) · Nature · doi:10.1038/nature05077 · Cited by 382

p53-deficient mice are extremely susceptible to radiation-induced tumorigenesis

Kemp, C. J., Wheldon, T. E., & Balmain, A. (1994) · Nature Genetics · doi:10.1038/ng0994-66 · Cited by 370

A p53-dependent mechanism underlies macrocytic anemia in a mouse model of human 5q– syndrome

Barlow, J. L., Drynan, L. F., Hewett, D. R., Holmes, L. R., Lorenzo-Abalde, S., Lane, A. L., Jolin, H. E., Pannell, R., Middleton, A. J., Wong, S. H., et al. (2009) · Nature Medicine · doi:10.1038/nm.2063 · Cited by 349

Transcription factor Gfi1 regulates self‐renewal and engraftment of hematopoietic stem cells

Zeng, H., Yücel, R., Kosan, C., Klein‐Hitpaß, L., & Möröy, T. (2004) · The EMBO Journal · doi:10.1038/sj.emboj.7600419 · Cited by 346

p53-Mediated Hematopoietic Stem and Progenitor Cell Competition

Bondar, T., & Medzhitov, R. (2010) · Cell Stem Cell · doi:10.1016/j.stem.2010.03.002 · Cited by 342

Chromosome stability, in the absence of apoptosis, is critical for suppression of tumorigenesis in Trp53 mutant mice

Liu, G., Parant, J. M., Lang, G., Chau, P., Chavez-Reyes, A., El-Naggar, A. K., Multani, A., Chang, S., & Lozano, G. (2004) · Nature Genetics · doi:10.1038/ng1282 · Cited by 325

Mdm4 (Mdmx) regulates p53-induced growth arrest and neuronal cell death during early embryonic mouse development

Migliorini, D., Denchi, E. L., Danovi, D., Jochemsen, A., Capillo, M., Gobbi, A., Helin, K., Pelicci, P. G., & Marine, J.-C. (2002) · Molecular and Cellular Biology · doi:10.1128/mcb.22.15.5527-5538.2002 · Cited by 313

Hematopoietic cells from mice deficient in wild-type p53 are more resistant to induction of apoptosis by some agents

Lotem, J., & Sachs, L. (1993) · Blood · doi:10.1182/blood.v82.4.1092.1092 · Cited by 301

Differential Expression of Novel Potential Regulators in Hematopoietic Stem Cells

Forsberg, E. C., Prohaska, S. S., Katzman, S. J., Heffner, G. C., Stuart, J. M., & Weissman, I. L. (2005) · PLoS Genetics · doi:10.1371/journal.pgen.0010028 · Cited by 296

Ribosomal Protein S24 Gene Is Mutated in Diamond-Blackfan Anemia

Gazda, H. T., Grabowska, A. K., de Long, L. M., Latawiec, E., Schneider, H. E., Lipton, J. M. M., Vlachos, A., Atsidaftos, E., Ball, S. E., Orfali, K. A., et al. (2006) · The American Journal of Human Genetics · doi:10.1086/510020 · Cited by 276

Transgenic mice with p53‐responsive lacZ: p53 activity varies dramatically during normal development and determines radiation and drug sensitivity in vivo

Komarova, E. A., Chernov, M. V., Franks, R., Wang, K., Armin, G., Zelnick, C. R., Chin, D. M., Bacus, S. S., Stark, G. R., & Gudkov, A. V. (1997) · The EMBO Journal · doi:10.1093/emboj/16.6.1391 · Cited by 274

The promises and perils of p53

Krizhanovsky, V., & Lowe, S. W. (2009) · Nature · doi:10.1038/4601085a · Cited by 274

Mouse hematopoietic stem-cell antigen Sca-1 is a member of the Ly-6 antigen family.

van de Rijn, M., Heimfeld, S., Spangrude, G. J., & Weissman, I. L. (1989) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.86.12.4634 · Cited by 265

Declining p53 function in the aging process: A possible mechanism for the increased tumor incidence in older populations

Feng, Z., Hu, W., Teresky, A. K., Hernando, E., Cordon-Cardo, C., & Levine, A. J. (2007) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0708043104 · Cited by 264

Do reactive oxygen species play a role in myeloid leukemias?

Hole, P. S., Darley, R. L., & Tonks, A. (2011) · Blood · doi:10.1182/blood-2011-01-326025 · Cited by 261

Mdm2 is critically and continuously required to suppress lethal p53 activity in vivo

Ringshausen, I., O'Shea, C. C., Finch, A. J., Swigart, L. B., & Evan, G. I. (2006) · Cancer Cell · doi:10.1016/j.ccr.2006.10.010 · Cited by 256

Mdm2 Regulates p53 mRNA Translation through Inhibitory Interactions with Ribosomal Protein L26

Ofir-Rosenfeld, Y., Boggs, K., Michael, D., Kastan, M. B., & Oren, M. (2008) · Molecular Cell · doi:10.1016/j.molcel.2008.08.031 · Cited by 255

The impact of altered p53 dosage on hematopoietic stem cell dynamics during aging

Dumble, M. L., Moore, L. M., Chambers, S. M., Geiger, H., Zant, G. E. V., Goodell, M. A., & Donehower, L. A. (2006) · Blood · doi:10.1182/blood-2006-03-010413 · Cited by 249

p53 Controls Radiation-Induced Gastrointestinal Syndrome in Mice Independent of Apoptosis

Kirsch, D. G., Santiago, P. M., di Tomaso, E., Sullivan, J. M., Hou, W.-S., Dayton, T. L., Jeffords, L. B., Sodha, P., Mercer, K. L., Cohen, R., et al. (2009) · Science · doi:10.1126/science.1166202 · Cited by 245

Abnormalities of the large ribosomal subunit protein, Rpl35a, in Diamond-Blackfan anemia

Farrar, J. E., Nater, M., Caywood, E., McDevitt, M. A., Kowalski, J., Takemoto, C. M., Talbot, C. C., Meltzer, P. S., Esposito, D., Beggs, A. H., et al. (2008) · Blood · doi:10.1182/blood-2008-02-140012 · Cited by 239

mdm2 Is Critical for Inhibition of p53 during Lymphopoiesis and the Response to Ionizing Irradiation

Mendrysa, S. M., McElwee, M. K., Michalowski, J., O'Leary, K. A., Young, K. M., & Perry, M. E. (2003) · Molecular and Cellular Biology · doi:10.1128/mcb.23.2.462-473.2003 · Cited by 234

Tumor suppressor genes in normal and malignant hematopoiesis

Krug, U. O., Ganser, A., & Koeffler, H. P. (2002) · Oncogene · doi:10.1038/sj.onc.1205322 · Cited by 232

p53-family proteins and their regulators: hubs and spokes in tumor suppression

Collavin, L., Lunardi, A., & Sal, G. D. (2010) · Cell Death and Differentiation · doi:10.1038/cdd.2010.35 · Cited by 225

Ribosomal protein S17 gene (RPS17) is mutated in Diamond-Blackfan anemia

Čmejla, R., Čmejlová, J., Handrková, H., Petrák, J., & Pospı́šilová, D. (2007) · Human Mutation · doi:10.1002/humu.20608 · Cited by 220

p53 Lesions in Leukemic Transformation

Harutyunyan, A. S., Klampfl, T., Cazzola, M., & Královics, R. (2011) · New England Journal of Medicine · doi:10.1056/nejmc1012718 · Cited by 211

Tumor suppression and normal aging in mice with constitutively high p53 activity

Mendrysa, S. M., O'Leary, K. A., McElwee, M. K., Michalowski, J., Eisenman, R. N., Powell, D. A., & Perry, M. E. (2006) · Genes & Development · doi:10.1101/gad.1378506 · Cited by 210

Progression of interleukin-2 (IL-2)-dependent rat T cell lymphoma lines to IL-2-independent growth following activation of a gene (Gfi-1) encoding a novel zinc finger protein.

Gilks, C. B., Bear, S. E., Grimes, H. L., & Tsichlis, P. N. (1993) · Molecular and Cellular Biology · doi:10.1128/mcb.13.3.1759 · Cited by 207

Ribosomal Protein S7 Is Both a Regulator and a Substrate of MDM2

Zhu, Y. Y., Poyurovsky, M. V., Li, Y., Biderman, L., Stahl, J., Jacq, X., & Prives, C. L. (2009) · Molecular Cell · doi:10.1016/j.molcel.2009.07.014 · Cited by 206

Human RPS19, the gene mutated in Diamond-Blackfan anemia, encodes a ribosomal protein required for the maturation of 40S ribosomal subunits

Flygare, J., Aspesi, A., Bailey, J. C., Miyake, K., Caffrey, J. M., Karlsson, S., & Ellis, S. R. (2006) · Blood · doi:10.1182/blood-2006-07-038232 · Cited by 201

Dysfunction of the TP53 tumor suppressor gene in lymphoid malignancies

Xu-Monette, Z. Y., Medeiros, L. J., Li, Y., Orlowski, R. Z., Andreeff, M., Bueso-Ramos, C., Greiner, T. C., McDonnell, T. J., & Young, K. H. (2012) · Blood · doi:10.1182/blood-2011-11-366062 · Cited by 190

Single Adult Human CD34+/Lin−/CD38− Progenitors Give Rise to Natural Killer Cells, B-Lineage Cells, Dendritic Cells, and Myeloid Cells

Miller, J. S., McCullar, V., Punzel, M., Lemischka, I. R., & Moore, K. A. (1999) · Blood · doi:10.1182/blood.v93.1.96.401k13_96_106 · Cited by 186

Long-term haematopoietic reconstitution by Trp53-/-p16Ink4a-/-p19Arf-/- multipotent progenitors

Akala, O. O., Park, I.-K., Qian, D., Pihalja, M., Becker, M. W., & Clarke, M. F. (2008) · Nature · doi:10.1038/nature06869 · Cited by 173

Ribosomal protein S3: A multi-functional protein that interacts with both p53 and MDM2 through its KH domain

Yadavilli, S., Mayo, L. D., Higgins, M., Laı́n, S., Hegde, V. K., & Deutsch, W. A. (2009) · DNA repair · doi:10.1016/j.dnarep.2009.07.003 · Cited by 165

Low Doses of Radiation Increase the Latency of Spontaneous Lymphomas and Spinal Osteosarcomas in Cancer-Prone, Radiation-SensitiveTrp53Heterozygous Mice

Mitchel, R. E. J., Jackson, J. S., Morrison, D. P., & Carlisle, S. M. (2003) · Radiation Research · doi:10.1667/0033-7587(2003)159[0320:ldorit]2.0.co;2 · Cited by 159

The prognostic impact of 17p (p53) deletion in 2272 adults with acute myeloid leukemia

Seifert, H., Mohr, B., Thiede, C., Oelschlägel, U., Schäkel, U., Illmer, T., Soucek, S., Ehninger, G., Schaich, M. A., & on behalf of the Study Alliance Leukemia (SAL) (2009) · Leukemia · doi:10.1038/leu.2008.375 · Cited by 158

Ser18 and 23 phosphorylation is required for p53‐dependent apoptosis and tumor suppression

Chao, C., Herr, D., Chun, J., & Xu, Y. (2006) · The EMBO Journal · doi:10.1038/sj.emboj.7601167 · Cited by 158

Targeted Disruption of the Ribosomal Protein S19 Gene Is Lethal Prior to Implantation

Matsson, H., Davey, E. J., Draptchinskaia, N., Hamaguchi, I., Ooka, A., Levéen, P., Forsberg, E., Karlsson, S., & Dahl, N. (2004) · Molecular and Cellular Biology · doi:10.1128/mcb.24.9.4032-4037.2004 · Cited by 156

Phosphorylation of Serine 18 Regulates Distinct p53 Functions in Mice

Sluss, H. K., Armata, H., Gallant, J., & Jones, S. N. (2004) · Molecular and Cellular Biology · doi:10.1128/mcb.24.3.976-984.2004 · Cited by 152

Irradiation selects for p53-deficient hematopoietic progenitors.

Marusyk, A., Porter, C. C., Zaberezhnyy, V., & DeGregori, J. (2010) · PLoS Biology · doi:10.1371/journal.pbio.1000324 · Cited by 151

Establishment of a Normal Hematopoietic and Leukemia Stem Cell HierarchyPreprint

Chao, M. P., Seita, J., & Weissman, I. L. (2008) · Cold Spring Harbor Symposia on Quantitative Biology · doi:10.1101/sqb.2008.73.031 · Cited by 146

Mdm2 Is Required for Survival of Hematopoietic Stem Cells/Progenitors via Dampening of ROS-Induced p53 Activity

Abbas, H. A., Macció, D. R., Coşkun, S., Jackson, J. G., Hazen, A. L., Sills, T., You, M. J., Hirschi, K. K., & Lozano, G. (2010) · Cell stem cell · doi:10.1016/j.stem.2010.09.013 · Cited by 144

Deletion of Puma protects hematopoietic stem cells and confers long-term survival in response to high-dose γ-irradiation

Yu, H. M., Shen, H., Yuan, Y., XuFeng, R., Hu, X., Garrison, S. P., Zhang, L., Yu, J., Zambetti, G. P., & Cheng, T. (2010) · Blood · doi:10.1182/blood-2009-10-248278 · Cited by 144

Expansion of hematopoietic stem cell phenotype and activity in Trp53-null mice

TeKippe, M., Harrison, D. E., & Chen, J. (2003) · Experimental Hematology · doi:10.1016/s0301-472x(03)00072-9 · Cited by 135

Heterodimerization of Mdm2 and Mdm4 is critical for regulating p53 activity during embryogenesis but dispensable for p53 and Mdm2 stability

Pant, V., Xiong, S., Iwakuma, T., Quintás-Cardama, A., & Lozano, G. (2011) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1102241108 · Cited by 134

Mdm2 haplo‐insufficiency profoundly inhibits Myc‐induced lymphomagenesis

Alt, J. R., Greiner, T. C., Cleveland, J. L., & Eischen, C. M. (2003) · The EMBO Journal · doi:10.1093/emboj/cdg133 · Cited by 129

A High-Frequency Regulatory Polymorphism in the p53 Pathway Accelerates Tumor Development

Post, S. M., Quintás-Cardama, A., Pant, V., Iwakuma, T., Hamir, A., Jackson, J. G., Maccio, D. R., Bond, G. L., Johnson, D. G., Levine, A. J., et al. (2010) · Cancer Cell · doi:10.1016/j.ccr.2010.07.010 · Cited by 127

Mutation of ribosomal protein RPS24 in Diamond-Blackfan anemia results in a ribosome biogenesis disorder

Choesmel, V., Fribourg, S., Aguissa-Touré, A.-H., Pinaud, N., Legrand, P., Gazda, H. T., & Gleizes, P. (2008) · Human Molecular Genetics · doi:10.1093/hmg/ddn015 · Cited by 126

Defective apoptosis and B-cell lymphomas in mice with p53 point mutation at Ser 23

MacPherson, D., Kim, J., Kim, T., Rhee, B. K., van Oostrom, C. T., DiTullio, R. A., Venere, M., Halazonetis, T. D., Bronson, R., de Vries, A., et al. (2004) · The EMBO Journal · doi:10.1038/sj.emboj.7600363 · Cited by 124

A Limited Role for p21Cip1/Waf1 in Maintaining Normal Hematopoietic Stem Cell Functioning

van Os, R. P., Kamminga, L. M., Ausema, A., Bystrykh, L. V., Draijer, D. P., van Pelt, K., Dontje, B., & de Haan, G. (2006) · Stem Cells · doi:10.1634/stemcells.2006-0631 · Cited by 124

Prognostic factors identified three risk groups in the LRF CLL4 trial, independent of treatment allocation

Oscier, D. G., Wade, R. L., Davis, Z. A., Morilla, A. M., Best, G., Richards, S. M., Else, M., Matutes, E., & Catovsky, D. (2010) · Haematologica · doi:10.3324/haematol.2010.025338 · Cited by 122

Pathologies Associated with the p53 ResponsePreprint

Gudkov, A. V., & Komarova, E. A. (2010) · Cold Spring Harbor Perspectives in Biology · doi:10.1101/cshperspect.a001180 · Cited by 119

Flow cytometry analysis of murine hematopoietic stem cells

Mayle, A., Luo, M., Jeong, M., & Goodell, M. A. (2012) · Cytometry Part A · doi:10.1002/cyto.a.22093 · Cited by 118

Haploinsufficiency of Mdm2 and Mdm4 in Tumorigenesis and Development

Terzian, T., Wang, Y., Van Pelt, C. S., Box, N. F., Travis, E. L., & Lozano, G. (2007) · Molecular and Cellular Biology · doi:10.1128/mcb.00555-06 · Cited by 116

Puma is required for p53-induced depletion of adult stem cells

Liu, D., Ou, L. Y., Clemenson, G. D., Chao, C., Lutske, M. E., Zambetti, G. P., Gage, F. H., & Xu, Y. (2010) · Nature Cell Biology · doi:10.1038/ncb2100 · Cited by 114

Mechanisms controlling hematopoietic stem cell functions during normal hematopoiesis and hematological malignancies

Warr, M. R., Pietras, E. M., & Passegué, E. (2011) · WIREs Systems Biology and Medicine · doi:10.1002/wsbm.145 · Cited by 112

Development and aging of primitive hematopoietic stem cells in BALB/cBy mice

Chen, J., Astle, C. M., & Harrison, D. E. (1999) · Experimental Hematology · doi:10.1016/s0301-472x(99)00018-1 · Cited by 109

Enrichment of hematopoietic stem cells with SLAM and LSK markers for the detection of hematopoietic stem cell function in normal and Trp53 null mice

Chen, J., Ellison, F. M., Keyvanfar, K., Omokaro, S. O., Desierto, M. J., Eckhaus, M., & Young, N. S. (2008) · Experimental Hematology · doi:10.1016/j.exphem.2008.04.012 · Cited by 109

THE CLINICAL SIGNIFICANCE OF MUTATIONS OF THE P52 TUMOUR SUPPRESSOR GENE IN HAEMATOLOGICAL MALIGNANCIES

Preudhomme, C., & Fenaux, P. (1997) · British Journal of Haematology · doi:10.1046/j.1365-2141.1997.2403057.x · Cited by 106

Deletion of proapoptotic Puma selectively protects hematopoietic stem and progenitor cells against high-dose radiation

Shao, L., Sun, Y., Zhang, Z., Feng, W., Gao, Y., Cai, Z., Wang, Z., Look, A. T., & Wu, W. (2010) · Blood · doi:10.1182/blood-2009-10-248872 · Cited by 103

The Regulation of the p53-mediated Stress Response by MDM2 and MDM4Preprint

Perry, M. E. (2009) · Cold Spring Harbor Perspectives in Biology · doi:10.1101/cshperspect.a000968 · Cited by 100

Ribosomal protein L11 mutation in zebrafish leads to haematopoietic and metabolic defects

Danilova, N., Sakamoto, K. M., & Lin, S. (2010) · British Journal of Haematology · doi:10.1111/j.1365-2141.2010.08396.x · Cited by 99

Pluripotent hematopoietic stem cell development during embryogenesis

Cumano, A., & Godin, I. (2001) · Current Opinion in Immunology · doi:10.1016/s0952-7915(00)00200-4 · Cited by 98

A transgenic mouse model demonstrates a dominant negative effect of a point mutation in the RPS19 gene associated with Diamond-Blackfan anemia

Devlin, E. E., DaCosta, L., Mohandas, N., Elliott, G., & Bodine, D. M. (2010) · Blood · doi:10.1182/blood-2010-03-275776 · Cited by 97

Regulation of hematopoietic stem cell growth

Attar, E. C., & Scadden, D. T. (2004) · Leukemia · doi:10.1038/sj.leu.2403515 · Cited by 96

The p53 Tumor Suppressor Protein Does Not Regulate Expression of Its Own Inhibitor, MDM2, Except under Conditions of Stress

Mendrysa, S. M., & Perry, M. E. (2000) · Molecular and Cellular Biology · doi:10.1128/mcb.20.6.2023-2030.2000 · Cited by 87

P53 Gene Mutations in Lymphoid Diseases and Their Possible Relevance to Drug Resistance

Newcomb, E. W. (1995) · Leukemia & lymphoma/Leukemia and lymphoma · doi:10.3109/10428199509056825 · Cited by 85

Validation of MdmX as a therapeutic target for reactivating p53 in tumors

Garcia, D., Warr, M. R., Martins, C. P., Brown Swigart, L., Passegué, E., & Evan, G. I. (2011) · Genes & Development · doi:10.1101/gad.16722111 · Cited by 83

Spontaneous Tumorigenesis in Mice Overexpressing the p53-Negative Regulator Mdm4

Xiong, S., Pant, V., Suh, Y.-A., Van Pelt, C. S., Wang, Y., Valentin-Vega, Y. A., Post, S. M., & Lozano, G. (2010) · Cancer Research · doi:10.1158/0008-5472.can-10-1457 · Cited by 82

Increased Radioresistance and Accelerated B Cell Lymphomas in Mice with Mdmx Mutations that Prevent Modifications by DNA-Damage-Activated Kinases

Wang, Y. V., Leblanc, M., Wade, M., Jochemsen, A. G., & Wahl, G. M. (2009) · Cancer Cell · doi:10.1016/j.ccr.2009.05.008 · Cited by 79

Murine hematopoietic stem cell characterization and its regulation in BM transplantation

Zhao, Y., Lin, Y., Zhan, Y., Yang, G., Louie, J. P., Harrison, D. E., & Anderson, W. F. (2000) · Blood · doi:10.1182/blood.v96.9.3016 · Cited by 77

Necdin, a p53 target gene, regulates the quiescence and response to genotoxic stress of hematopoietic stem/progenitor cells

Asai, T., Liu, Y., Giandomenico, S. D., Bae, N., Ndiaye‐Lobry, D., DeBlasio, A., Menéndez, S., Antipin, Y., Reva, B. A., Wevrick, R., et al. (2012) · Blood · doi:10.1182/blood-2011-11-393983 · Cited by 70

Diamond Blackfan Anemia

Ball, S. E. (2011) · Hematology · doi:10.1182/asheducation-2011.1.487 · Cited by 69

Timed Somatic Deletion of p53 in Mice Reveals Age-Associated Differences in Tumor Progression

Hinkal, G. W., Parikh, N., & Donehower, L. A. (2009) · PLoS ONE · doi:10.1371/journal.pone.0006654 · Cited by 68

Chapter 8 Diamond Blackfan Anemia: A Disorder of Red Blood Cell Development

Ellis, S. R., & Lipton, J. M. M. (2008) · Current topics in developmental biology/Current Topics in Developmental Biology · doi:10.1016/s0070-2153(07)00008-7 · Cited by 67

Distinct roles of Mdm2 and Mdm4 in red cell production

Maetens, M., Doumont, G., Clercq, S. D., Francoz, S., Froment, P., Bellefroid, E., Klingmuller, U., Lozano, G., & Marine, J.-C. (2007) · Blood · doi:10.1182/blood-2006-03-013656 · Cited by 64

The p53–Mdm2 network in progenitor cell expansion during mouse postnatal development

Liu, G., Terzian, T., Xiong, S., Pelt, C. S. V., Audiffred, A., Box, N. F., & Lozano, G. (2007) · The Journal of Pathology · doi:10.1002/path.2238 · Cited by 62

Diamond Blackfan anemia 2008–2009: broadening the scope of ribosome biogenesis disorders

Lipton, J. M. M., & Ellis, S. R. (2010) · Current Opinion in Pediatrics · doi:10.1097/mop.0b013e328334573b · Cited by 59

Mutated and non‐mutated TP53 as targets in the treatment of leukaemia

Nahi, H., Selivanova, G., Lehmann, S., Möllgård, L., Bengtzén, S., Concha, H., Svensson, A., Wiman, K. G., Merup, M., & Paul, C. (2008) · British Journal of Haematology · doi:10.1111/j.1365-2141.2008.07046.x · Cited by 58

Loss of heterozygosity frequency at the Trp53 locus in p53-deficient (+/-) mouse tumors is carcinogen-and tissue-dependent

French, J. E. (2001) · Carcinogenesis · doi:10.1093/carcin/22.1.99 · Cited by 58

Role of p53 in Hematopoietic Recovery After Cytotoxic Treatment

Wlodarski, P. K., Wasik, M. A., Ratajczak, M. Z., Sevignani, C., Hoser, G., Kawiak, J., Gewirtz, A. M., Calabretta, B., & Skórski, T. (1998) · Blood · doi:10.1182/blood.v91.8.2998.2998_2998_3006 · Cited by 53

Fine-tuning p53 activity through C-terminal modification significantly contributes to HSC homeostasis and mouse radiosensitivity

Wang, Y. V., Leblanc, M., Fox, N., Mao, J.-H., Tinkum, K. L., Krummel, K., Engle, D., Piwnica-Worms, D., Piwnica-Worms, H., Balmain, A., et al. (2011) · Genes & Development · doi:10.1101/gad.2024411 · Cited by 53

Pathogenesis of the erythroid failure in Diamond Blackfan anaemia

Sieff, C. A., Yang, J. C., de Long, L. M., & Lodish, H. F. (2009) · British Journal of Haematology · doi:10.1111/j.1365-2141.2009.07993.x · Cited by 50

Animal Models of Diamond Blackfan Anemia

McGowan, K. A., & Mason, P. J. (2011) · Seminars in Hematology · doi:10.1053/j.seminhematol.2011.02.001 · Cited by 45

A small molecule inhibitor of p53 stimulates amplification of hematopoietic stem cells but does not promote tumor development in mice

Leonova, K. I., Shneyder, J., Antoch, M. P., Toshkov, I. A., Novototskaya, L. R., Komarov, P. G., Komarova, E. A., & Gudkov, A. V. (2010) · Cell Cycle · doi:10.4161/cc.9.7.11508 · Cited by 40

Erythropoiesis in the Rps19 disrupted mouse: Analysis of erythropoietin response and biochemical markers for Diamond-Blackfan anemia

Matsson, H., Davey, E. J., Fröjmark, A.-S., Miyake, K., Utsugisawa, T., Flygare, J., Zahou, E., Byman, I., Landin, B., Ronquist, G. K., et al. (2006) · Blood Cells Molecules and Diseases · doi:10.1016/j.bcmd.2005.12.002 · Cited by 40

High-Resolution Array-Based Comparative Genomic Hybridization of Bladder Cancers Identifies Mouse Double Minute 4 ( MDM4 ) as an Amplification Target Exclusive of MDM2 and TP53

Veerakumarasivam, A., Scott, H. E., Chin, S., Warren, A. Y., Wallard, M. J., Grimmer, D., Ichimura, K., Caldas, C., Collins, V. P., Neal, D. E., et al. (2008) · Clinical Cancer Research · doi:10.1158/1078-0432.ccr-07-4129 · Cited by 38

Rpl27a mutation in the sooty foot ataxia mouse phenocopies high p53 mouse models

Terzian, T., Dumble, M. L., Arbab, F., Christina Thaller, B., Donehower, L. A., Lozano, G., Justice, M. J., Roop, D. R., & Box, N. F. (2011) · The Journal of Pathology · doi:10.1002/path.2891 · Cited by 29

MDM4 (MDMX) is overexpressed in chronic lymphocytic leukaemia (CLL) and marks a subset of p53wild‐type CLL with a poor cytotoxic response to Nutlin‐3

Bo, M. D., Secchiero, P., Degan, M., Marconi, D., Bomben, R., Pozzato, G., Gaïdano, G., Poeta, G. D., Forconi, F., Zauli, G., et al. (2010) · British Journal of Haematology · doi:10.1111/j.1365-2141.2010.08185.x · Cited by 26

Apoptosis in bone marrow cells of mice with different p53 genotypes after gamma-rays irradiation in vitro.

Cui, Y., Zhou, P., Woolford, L. B., Lord, B. I., Hendry, J. H., & Wang, D. W. (1995) · PubMed · Cited by 25

Prognostic Impact of the MDM2SNP309 Allele in Leukemia and Lymphoma

Post, S. M., Pant, V., Abbas, H. A., & Quintás‐Cardama, A. (2010) · Oncotarget · doi:10.18632/oncotarget.123 · Cited by 11

Cellular senescence and cancer

(1999) · doi:10.1002/(sici)1096-9896(199901)187:1

Unravelling mechanisms of p53-mediated tumour suppression

Bieging-Rolett, K. T., Mello, S. S., & Attardi, L. D. (2014) · Nature reviews. Cancer · doi:10.1038/nrc3711 · Cited by 1,459

Uncovering the role of p53 splice variants in human malignancy: a clinical perspective

Bourdon, J., Surget, S., & Khoury, M. P. (2013) · OncoTargets and Therapy · doi:10.2147/ott.s53876 · Cited by 399

MDM2 inhibition: an important step forward in cancer therapy

Konopleva, M. Y., Martinelli, G., Daver, N. G., Papayannidis, C., Wei, A. H., Higgins, B., Ott, M., Mascarenhas, J. O., & Andreeff, M. (2020) · Leukemia · doi:10.1038/s41375-020-0949-z · Cited by 380

Deconstructing networks of p53-mediated tumor suppression in vivo

Kaiser, A. M., & Attardi, L. D. (2017) · Cell Death and Differentiation · doi:10.1038/cdd.2017.171 · Cited by 232

Natural course and biology of CML

Chereda, B., & Melo, J. V. (2015) · Annals of Hematology · doi:10.1007/s00277-015-2325-z · Cited by 226

The ups and downs of p53 regulation in hematopoietic stem cells

Abbas, H. A., Pant, V., & Lozano, G. (2011) · Cell Cycle · doi:10.4161/cc.10.19.17721 · Cited by 33

The p53 tumor suppressor protein is a critical regulator of hematopoietic stem cell behavior

Liu, Y., Elf, S., Asai, T., Miyata, Y., Liu, Y., Sashida, G., Huang, G., Giandomenico, S. D., Koff, A., & Nimer, S. D. (2009) · Cell Cycle · doi:10.4161/cc.8.19.9627 · Cited by 67

A new role of P53 in preventing early leukemic transformation of HSCS

Brown, A., Eiwen, K., Pospiech, J., Saçma, M., Moehrle, B., & Geiger, H. (2016) · Experimental Hematology · doi:10.1016/j.exphem.2016.06.099

p53 mediates loss of hematopoietic stem cell function and lymphopenia in Mysm1 deficiency

Belle, J. I., Langlais, D., Petrov, J. C., Pardo, M., Jones, R. G., Gros, P., & Nijnik, A. (2015) · Blood · doi:10.1182/blood-2014-05-574111 · Cited by 77

Repression of p53-target gene Bbc3/PUMA by MYSM1 is essential for the survival of hematopoietic multipotent progenitors and contributes to stem cell maintenance

Belle, J. I., Petrov, J. C., Langlais, D., Robert, F., Cencic, R., Shen, S., Pelletier, J., Gros, P., & Nijnik, A. (2016) · Cell Death and Differentiation · doi:10.1038/cdd.2015.140 · Cited by 62