Proposed megakaryocytic regulon of p53: The genes engaged to control cell cycle and apoptosis during megakaryocytic differentiation

Physiological Genomics

Volumn 44, Issue 12, 2012, Pages 638-650

  Apostolidis, Pani A ^a,b   Lindsey, Stephan ^b   Miller, William M ^a   Papoutsakis, Eleftherios T ^a,b  

^a Northwestern University   (United States)

^b UNIVERSITY OF DELAWARE   (United States)

Author keywords

Megakaryocytic; Microarray; p53; Polyploidization

Indexed keywords

ACTA2 PROTEIN; CASP8 PROTEIN; CELL PROTEIN; CKS1B PROTEIN; CYCLIN DEPENDENT KINASE INHIBITOR 1A; DRAM1 PROTEIN; FAS ANTIGEN; GTSE1 PROTEIN; NOTCH1 RECEPTOR; PHLDA3 PROTEIN; POLO LIKE KINASE 2; PROTEIN BCL 2; PROTEIN P53; RRM2B PROTEIN; SESN1 PROTEIN; TNFRSF10B PROTEIN; TP53I3 PROTEIN; TP53INP1 PROTEIN; TP63 PROTEIN; UNCLASSIFIED DRUG; ZMAT3 PROTEIN;

APOPTOSIS; ARTICLE; CELL CYCLE ARREST; CELL CYCLE REGULATION; CELL DIFFERENTIATION; CELL LINE; CONTROLLED STUDY; CYTOSKELETON; DNA SYNTHESIS; GENE CONTROL; GENE EXPRESSION; GENE FUNCTION; GENE LOSS; GENE SILENCING; GENE TARGETING; HUMAN; HUMAN CELL; MEGAKARYOCYTE; MEGAKARYOPOIESIS; MICROARRAY ANALYSIS; MITOSIS; POLYPLOIDY; PRIORITY JOURNAL; REGULON; UPREGULATION; WILD TYPE;

APOPTOSIS; BASE SEQUENCE; CELL CYCLE; CELL DIFFERENTIATION; CELL LINE; DNA PRIMERS; GENES, P53; HUMANS; MEGAKARYOCYTES;

EID: 84862591309     PISSN: 10948341     EISSN: 15312267     Source Type: Journal    
DOI: 10.1152/physiolgenomics.00028.2012     Document Type: Article

References (72)

1. Agarwal ML, Agarwal A, Taylor WR, Stark GR. p53 controls both the G2/M and the G1 cell cycle checkpoints and mediates reversible growth arrest in human fibroblasts. Proc Natl Acad Sci USA 92: 8493-8497, 1995.
2. Ando K, Ajchenbaum-Cymbalista F, Griffin JD. Regulation of G1/S transition by cyclins D2 and D3 in hematopoietic cells. Proc Natl Acad Sci USA 90: 9571-9575, 1993.
3. Apostolidis PA, Woulfe DS, Chavez M, Miller WM, Papoutsakis ET. Role of tumor suppressor p53 in megakaryopoiesis and platelet function. Exp Hematol 40: 131-142, 2012.
4. Archambault V, Glover DM. Polo-like kinases: conservation and divergence in their functions and regulation. Nat Rev Mol Cell Biol 10: 265-275, 2009.
5. Baccini V, Roy L, Vitrat N, Chagraoui H, Sabri S, Le Couedic JP, Debili N, Wendling F, Vainchenker W. Role of p21(Cip1/Waf1) in cell-cycle exit of endomitotic megakaryocytes. Blood 98: 3274-3282, 2001.
6. Baker SJ, Markowitz S, Fearon ER, Willson JK, Vogelstein B. Suppression of human colorectal carcinoma cell growth by wild-type p53. Science 249: 912-915, 1990.
7. Bassini A, Pierpaoli S, Falcieri E, Vitale M, Guidotti L, Capitani S, Zauli G. Selective modulation of the cyclin B/CDK1 and cyclin D/CDK4 complexes during in vitro human megakaryocyte development. Br J Haematol 104: 820-828, 1999.
8. Beckerman R, Prives C. Transcriptional regulation by p53. Cold Spring Harb Perspect Biol 2: a000935, 2010.
9. Bensaad K, Tsuruta A, Selak MA, Vidal MN, Nakano K, Bartrons R, Gottlieb E, Vousden KH. TIGAR, a p53-inducible regulator of glycolysis and apoptosis. Cell 126: 107-120, 2006.
10. Bermejo R, Vilaboa N, Cales C. Regulation of CDC6, geminin, and CDT1 in human cells that undergo polyploidization. Mol Biol Cell 13: 3989-4000, 2002.
11. + current. Am J Physiol Cell Physiol 289: C49-C57, 2005.
12. Chen C, Fuhrken PG, Huang LT, Apostolidis P, Wang M, Paredes CJ, Miller WM, Papoutsakis ET. A systems-biology analysis of isogenic megakaryocytic and granulocytic cultures identifies new molecular components of megakaryocytic apoptosis. BMC Genomics 8: 384, 2007.
13. Chitu V, Pixley FJ, Macaluso F, Larson DR, Condeelis J, Yeung YG, Stanley ER. The PCH family member MAYP/PSTPIP2 directly regulates F-actin bundling and enhances filopodia formation and motility in macrophages. Mol Biol Cell 16: 2947-2959, 2005.
14. Churchill GA. Fundamentals of experimental design for cDNA microar-rays. Nat Genet 32, Suppl: 490-495, 2002.
15. Chylicki K, Ehinger M, Svedberg H, Bergh G, Olsson I, Gullberg U. p53-mediated differentiation of the erythroleukemia cell line K562. Cell Growth Differ 11: 315-324, 2000.
16. Clarke MC, Savill J, Jones DB, Noble BS, Brown SB. Compartmentalized megakaryocyte death generates functional platelets committed to caspase-independent death. J Cell Biol 160: 577-587, 2003.
17. Conacci-Sorrell M, Zhurinsky J, Ben-Ze'ev A. The cadherin-catenin adhesion system in signaling and cancer. J Clin Invest 109: 987-991, 2002.
18. Crighton D, Wilkinson S, O'Prey J, Syed N, Smith P, Harrison PR, Gasco M, Garrone O, Crook T, Ryan KM. DRAM, a p53-induced modulator of autophagy, is critical for apoptosis. Cell 126: 121-134, 2006.
19. Datta NS, Long MW. Modulation of MDM2/p53 and cyclin-activating kinase during the megakaryocyte differentiation of human erythroleukemia cells. Exp Hematol 30: 158-165, 2002.
20. Duriez C, Falette N, Audoynaud C, Moyret-Lalle C, Bensaad K, Courtois S, Wang Q, Soussi T, Puisieux A. The human BTG2/TIS21/ PC3 gene: genomic structure, transcriptional regulation and evaluation as a candidate tumor suppressor gene. Gene 282: 207-214, 2002.
21. Even-Ram S, Yamada KM. Of mice and men: relevance of cellular and molecular characterizations of myosin IIA to MYH9-related human disease. Cell Adh Migr 1: 152-155, 2007.
22. Faradji F, Bloyer S, Dardalhon-Cumenal D, Randsholt NB, Peronnet F. Drosophila melanogaster cyclin G coordinates cell growth and cell proliferation. Cell Cycle 10: 805-818, 2011.
23. Fuhrken PG, Apostolidis PA, Lindsey S, Miller WM, Papoutsakis ET. Tumor suppressor protein p53 regulates megakaryocytic polyploidization and apoptosis. J Biol Chem 283: 15589-15600, 2008.
24. Fuhrken PG, Chen C, Apostolidis PA, Wang M, Miller WM, Papoutsakis ET. Gene Ontology-driven transcriptional analysis of CD34+ cell-initiated megakaryocytic cultures identifies new transcriptional regulators of megakaryopoiesis. Physiol Genomics 33: 159-169, 2008.
25. Fuhrken PG, Chen C, Miller WM, Papoutsakis ET. Comparative, genome-scale transcriptional analysis of CHRF-288-11 and primary human megakaryocytic cell cultures provides novel insights into lineage-specific differentiation. Exp Hematol 35: 476-489, 2007.
26. Gaiddon C, Lokshin M, Ahn J, Zhang T, Prives C. A subset of tumor-derived mutant forms of p53 down-regulate p63 and p73 through a direct interaction with the p53 core domain. Mol CellBiol 21: 1874-1887, 2001.
27. Giammona LM, Panuganti S, Kemper JM, Apostolidis PA, Lindsey S, Papoutsakis ET, Miller WM. Mechanistic studies on the effects of nicotinamide on megakaryocytic polyploidization and the roles of NAD + levels and SIRT inhibition. Exp Hematol 37: 1340-1352, 2009.
28. Heminger K, Markey M, Mpagi M, Berberich SJ. Alterations in gene expression and sensitivity to genotoxic stress following HdmX or Hdm2 knockdown in human tumor cells harboring wild-type p53. Aging (Albany NY) 1: 89-108, 2009.
29. Hoogenraad CC, Akhmanova A, Howell SA, Dortland BR, De Zeeuw CI, Willemsen R, Visser P, Grosveld F, Galjart N. Mammalian Golgi-associated bicaudal-D2 functions in the dynein-dynactin pathway by interacting with these complexes. EMBO J 20: 4041-4054, 2001.
30. Horvath MM, Wang X, Resnick MA, Bell DA. Divergent evolution of human p53 binding sites: cell cycle versus apoptosis. PLoS Genet 3: e127, 2007.
31. Ishiko E, Matsumura I, Ezoe S, Gale K, Ishiko J, Satoh Y, Tanaka H, Shibayama H, Mizuki M, Era T, Enver T, Kanakura Y. Notch signals inhibit the development of erythroid/megakaryocytic cells by suppressing GATA-1 activity through the induction of HES1. J Biol Chem 280: 4929-4939, 2005.
32. Jiang F, Jia Y, Cohen I. Fibronectin- and protein kinase C-mediated activation of ERK/MAPK are essential for proplateletlike formation. Blood 99: 3579-3584, 2002.
33. Jiang PH, Motoo Y, Iovanna JL, Pebusque MJ, Xie MJ, Okada G, Sawabu N. Tumor protein p53-induced nuclear protein 1 (TP53INP1) in spontaneous chronic pancreatitis in the WBN/Kob rat: drug effects on its expression in the pancreas. JOP 5: 205-216, 2004.
34. Jurak Begonja A, Hoffmeister KM, Hartwig JH, Falet H. FlnA-null megakaryocytes prematurely release large and fragile platelets that circulate poorly. Blood 118: 2285-2295, 2011.
35. Kaushansky K. Determinants of platelet number and regulation of throm-bopoiesis. Hematology Am Soc Hematol Educ Program: 147-152, 2009.
36. Kaushansky K. Historical review: megakaryopoiesis and thrombopoiesis. Blood 111: 981-986, 2008.
37. Kawasaki A, Matsumura I, Miyagawa J, Ezoe S, Tanaka H, Terada Y, Tatsuka M, Machii T, Miyazaki H, Furukawa Y, Kanakura Y. Downregulation of an AIM-1 kinase couples with megakaryocytic polyploidization of human hematopoietic cells. J Cell Biol 152: 275-287, 2001.
38. Kawase T, Ohki R, Shibata T, Tsutsumi S, Kamimura N, Inazawa J, Ohta T, Ichikawa H, Aburatani H, Tashiro F, Taya Y. PH domain-only protein PHLDA3 is a p53-regulated repressor of Akt. Cell 136: 535-550, 2009.
39. Konopatskaya O, Gilio K, Harper MT, Zhao Y, Cosemans JM, Karim ZA, Whiteheart SW, Molkentin JD, Verkade P, Watson SP, Heem-skerk JW, Poole AW. PKCalpha regulates platelet granule secretion and thrombus formation in mice. J Clin Invest 119: 399-407, 2009.
40. Kostyak JC, Naik UP. Calcium- and integrin-binding protein 1 regulates endomitosis and its interaction with Polo-like kinase 3 is enhanced in endomitotic Dami cells. PLoS One 6: e14513, 2011.
41. Law JC, Ritke MK, Yalowich JC, Leder GH, Ferrell RE. Mutational inactivation of the p53 gene in the human erythroid leukemic K562 cell line. Leuk Res 17: 1045-1050, 1993.
42. Levine AJ, Hu W, Feng Z. The P53 pathway: what questions remain to be explored? Cell Death Differ 13: 1027-1036, 2006.
43. Li J, Tan J, Zhuang L, Banerjee B, Yang X, Chau JF, Lee PL, Hande MP, Li B, Yu Q. Ribosomal protein S27-like, a p53-inducible modulator of cell fate in response to genotoxic stress. Cancer Res 67: 11317-11326, 2007.
44. Liebermann DA, Hoffman B. Gadd45 in the response of hematopoietic cells to genotoxic stress. Blood Cells Mol Dis 39: 329-335, 2007.
45. Limb JK, Yoon S, Lee KE, Kim BH, Lee S, Bae YS, Jhon GJ, Kim J. Regulation of megakaryocytic differentiation of K562 cells by FosB, a member of the Fos family of AP-1 transcription factors. Cell Mol Life Sci 66: 1962-1973, 2009.
46. Liu XS, Li H, Song B, Liu X. Polo-like kinase 1 phosphorylation of G2 and S-phase-expressed 1 protein is essential for p53 inactivation during G2 checkpoint recovery. EMBO Rep 11: 626-632, 2010.
47. Lordier L, Chang Y, Jalil A, Aurade F, Garcon L, Lecluse Y, Larbret F, Kawashima T, Kitamura T, Larghero J, Debili N, Vainchenker W. Aurora B is dispensable for megakaryocyte polyploidization, but contributes to the endomitotic process. Blood 116: 2345-2355, 2010.
48. Maynard DM, Heijnen HF, Gahl WA, Gunay-Aygun M. The a-granule proteome: novel proteins in normal and ghost granules in gray platelet syndrome. J Thromb Haemost 8: 1786-1796, 2010.
49. McGowan KA, Pang WW, Bhardwaj R, Perez MG, Pluvinage JV, Glader BE, Malek R, Mendrysa SM, Weissman IL, Park CY, Barsh GS. Reduced ribosomal protein gene dosage and p53 activation in low-risk myelodysplastic syndrome. Blood 118: 3622-3633, 2011.
50. Melloni E, Secchiero P, Celeghini C, Campioni D, Grill V, Guidotti L, Zauli G. Functional expression of TRAIL and TRAIL-R2 during human megakaryocytic development. J Cell Physiol 204: 975-982, 2005.
51. Merkle CJ, Karnitz LM, Henry-Sanchez JT, Chen J. Cloning and characterization of hCTF18, hCTF8, and hDCC1. Human homologs of a Saccharomyces cerevisiae complex involved in sister chromatid cohesion establishment. J Biol Chem 278: 30051-30056, 2003.
52. Ramsborg CG, Papoutsakis ET. Global transcriptional analysis delineates the differential inflammatory response interleukin-15 elicits from cultured human T cells. Exp Hematol 35: 454-464, 2007.
53. Riley T, Sontag E, Chen P, Levine A. Transcriptional control of human p53-regulated genes. Nat Rev Mol Cell Biol 9: 402-412, 2008.
54. Ritchie A, Braun SE, He J, Broxmeyer HE. Thrombopoietin-induced conformational change in p53 lies downstream of the p44/p42 mitogen activated protein kinase cascade in the human growth factor-dependent cell line M07e. Oncogene 18: 1465-1477, 1999.
55. Ryan MC, Zeeberg BR, Caplen NJ, Cleland JA, Kahn AB, Liu H, Weinstein JN. SpliceCenter: a suite of web-based bioinformatic applications for evaluating the impact of alternative splicing on RT-PCR, RNAi, microarray, and peptide-based studies. BMC Bioinformatics 9: 313, 2008.
56. Saeed AI, Sharov V, White J, Li J, Liang W, Bhagabati N, Braisted J, Klapa M, Currier T, Thiagarajan M, Sturn A, Snuffin M, Rezantsev A, Popov D, Ryltsov A, Kostukovich E, Borisovsky I, Liu Z, Vinsavich A, Trush V, Quackenbush J. TM4: a free, open-source system for microarray data management and analysis. Biotechniques 34: 374-378, 2003.
57. Saxena S, Dutta A. Geminin and p53: deterrents to rereplication in human cancer cells. Cell Cycle 2: 283-286, 2003.
58. Serra-Pages C, Medley QG, Tang M, Hart A, Streuli M. Liprins, a family of LAR transmembrane protein-tyrosine phosphatase-interacting proteins. J Biol Chem 273: 15611-15620, 1998.
59. Shin JW, Swift J, Spinler KR, Discher DE. Myosin-II inhibition and soft 2D matrix maximize multinucleation and cellular projections typical of platelet-producing megakaryocytes. Proc Natl Acad Sci USA 108: 11458-11463, 2011.
60. Sigurjonsson OE, Gudmundsson KO, Haraldsdottir V, Rafnar T, Agnarsson BA, Gudmundsson S. Flt3/Flk-2 ligand in combination with thrombopoietin decreases apoptosis in megakaryocyte development. Stem Cells Dev 13: 183-191, 2004.
61. Smyth GK, Yang YH, Speed T. Statistical issues in cDNA microarray data analysis. Methods Mol Biol 224: 111-136, 2003.
62. Syed N, Coley HM, Sehouli J, Koensgen D, Mustea A, Szlosarek P, McNeish I, Blagden SP, Schmid P, Lovell DP, Hatzimichael E, Crook T. Polo-like kinase Plk2 is an epigenetic determinant of chemosensitivity and clinical outcomes in ovarian cancer. Cancer Res 71: 3317-3327, 2011.
63. Talos F, Nemajerova A, Flores ER, Petrenko O, Moll UM. p73 suppresses polyploidy and aneuploidy in the absence of functional p53. Mol Cell 27: 647-659, 2007.
64. Tarcea VG, Weymouth T, Ade A, Bookvich A, Gao J, Mahavisno V, Wright Z, Chapman A, Jayapandian M, Ozgur A, Tian Y, Cavalcoli J, Mirel B, Patel J, Radev D, Athey B, States D, Jagadish HV. Michigan molecular interactions r2: from interacting proteins to pathways. Nucleic Acids Res 37: D642-D646, 2009.
65. Tusher VG, Tibshirani R, Chu G. Significance analysis of microarrays applied to the ionizing radiation response. Proc Natl Acad Sci USA 98: 5116-5121, 2001.
66. Van Geet C, Izzi B, Labarque V, Freson K. Human platelet pathology related to defects in the G-protein signaling cascade. J Thromb Haemost 7, Suppl 1: 282-286, 2009.
67. van Zon W, Ogink J, ter Riet B, Medema RH, te Riele H, Wolthuis RM. The APC/C recruits cyclin B1-Cdk1-Cks in prometaphase before D box recognition to control mitotic exit. J Cell Biol 190: 587-602, 2010.
68. Wei CL, Wu Q, Vega VB, Chiu KP, Ng P, Zhang T, Shahab A, Yong HC, Fu Y, Weng Z, Liu J, Zhao XD, Chew JL, Lee YL, Kuznetsov VA, Sung WK, Miller LD, Lim B, Liu ET, Yu Q, Ng HH, Ruan Y. A global map of p53 transcription-factor binding sites in the human genome. Cell 124: 207-219, 2006.
69. Yang H, Haddad H, Tomas C, Alsaker K, Papoutsakis ET. A segmen-tal nearest neighbor normalization and gene identification method gives superior results for DNA-array analysis. Proc Natl Acad Sci USA 100: 1122-1127, 2003.
70. Zhao L, Gregoire F, Sul HS. Transient induction of ENC-1, a Kelch-related actin-binding protein, is required for adipocyte differentiation. J Biol Chem 275: 16845-16850, 2000.
71. Zhao Y, Lu S, Wu L, Chai G, Wang H, Chen Y, Sun J, Yu Y, Zhou W, Zheng Q, Wu M, Otterson GA, Zhu WG. Acetylation of p53 at lysine 373/382 by the histone deacetylase inhibitor depsipeptide induces expression of p21(Waf1/Cip1). Mol Cell Biol 26: 2782-2790, 2006.
72. Zhao Y, Zhang Y, Wang S, Hua Z, Zhang J. The clock gene Per2 is required for normal platelet formation and function. Thromb Res 127: 122-130, 2011.