Transcriptome characterization uncovers the molecular response of hematopoietic cells to ionizing radiation

Radiation Research

Volumn 175, Issue 1, 2011, Pages 66-82

  Pawlik, Alexandre ^a   Alibert, Olivier ^b   Baulande, Sylvain ^c   Vaigot, Pierre ^b   Roux, Diana Tronik Le ^d,e  

^a INSTITUT PASTEUR   (France)

^b DIF   (France)

^c PartnerChip   (France)

^d INSTITUT DE RADIOPROTECTION ET DE SÛRETÉ NUCLÉAIRE   (France)

^e INSERM   (France)

Author keywords

[No Author keywords available]

Indexed keywords

PROTEIN P53; TRANSCRIPTOME;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; BIOINFORMATICS; BONE MARROW CELL; GENE EXPRESSION PROFILING; HEMATOPOIETIC CELL; HEMATOPOIETIC STEM CELL; IONIZING RADIATION; MALE; MICROARRAY ANALYSIS; MOUSE; NONHUMAN; NULL ALLELE; PRIORITY JOURNAL; RADIATION RESPONSE; RADIOSENSITIVITY; TRANSCRIPTION REGULATION; TRANSGENIC MOUSE;

ANIMALS; ANTIGENS, CD; BINDING SITES; CONNEXIN 43; GENE EXPRESSION PROFILING; HEMATOPOIETIC STEM CELLS; IMMUNOGLOBULINS; MALE; MEMBRANE GLYCOPROTEINS; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; RADIATION TOLERANCE; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; TUMOR SUPPRESSOR PROTEIN P53;

MUS;

EID: 78650587977     PISSN: 00337587     EISSN: None     Source Type: Journal    
DOI: 10.1667/RR2282.1     Document Type: Article

References (76)

1. P. Mauch, L. Constine, J. Greenberger, W. Knospe, J. Sullivan, J. L. Liesveld and H. J. Deeg, Hematopoietic stem cell compartment: acute and late effects of radiation therapy and chemotherapy. Int. J. Radiat. Oncol. Biol. Phys. 31, 1319-1339 (1995).
2. A. J. Simonnet, J. Nehme, P. Vaigot, V. Barroca, P. Leboulch and D. Tronik-Le Roux, Phenotypic and functional changes induced in hematopoietic stem/progenitor cells after gamma-ray radiation exposure. Stem Cells 27, 1400-1409 (2009).
3. A. V. Gudkov and E. A. Komarova, The role of p53 in determining sensitivity to radiotherapy. Nat. Rev. Cancer 3, 117-129 (2003).
4. S. Alvarez, P. Drane, A. Meiller, M. Bras, V. Deguin-Chambon, V. Bouvard and E. May, A comprehensive study of p53 transcriptional activity in thymus and spleen of gamma irradiated mouse: high sensitivity of genes involved in the two main apoptotic pathways. Int. J. Radiat. Biol. 82, 761-770 (2006).
5. P. Fei, E. J. Bernhard and W. S. El-Deiry, Tissue-specific induction of p53 targets in vivo. Cancer Res. 62, 7316-7327 (2002).
6. W. Qiu, E. B. Carson-Walter, H. Liu, M. Epperly, J. S. Greenberger, G. P. Zambetti, L. Zhang and J. Yu, PUMA regulates intestinal progenitor cell radiosensitivity and gastrointestinal syndrome. Cell Stem Cell 2, 576-583 (2008).
7. A. Pawlik, P. Delmar, S. Bosse, L. Sainz, C. Petat, G. Pietu, D. Thierry and D. Tronik-Le Roux, Changes in transcriptome after in vivo exposure to ionising radiation reveal a highly specialised liver response. Int. J. Radiat. Biol. 85, 656-671 (2009).
8. L. Enns, R. D. Barley, M. C. Paterson and R. Mirzayans, Radiosensitivity in ataxia telangiectasia fibroblasts is not associated with deregulated apoptosis. Radiat. Res. 150, 11-16 (1998).
9. C. H. Westphal, S. Rowan, C. Schmaltz, A. Elson, D. E. Fisher and P. Leder, Atm and p53 cooperate in apoptosis and suppression of tumorigenesis, but not in resistance to acute radiation toxicity. Nat. Genet. 16, 397-401 (1997).
10. z lymphocytes. Strahlenther. Onkol. 181, 326-335 (2005).
11. T. F. Burns and W. S. El-Deiry, Microarray analysis of p53 target gene expression patterns in the spleen and thymus in response to ionizing radiation. Cancer Biol. Ther. 2, 431-443 (2003).
12. K. Y. Jen and V. G. Cheung, Transcriptional response of lymphoblastoid cells to ionizing radiation. Genome Res. 13, 2092-2100 (2003).
13. J. K. Sax, A. Stoddard, M. E. Murphy, L. Chodosh and W. S. El-Deiry, Microarray expression profiling of p53-dependent transcriptional changes in an immortalized mouse embryo fibroblast cell line. Cancer Biol. Ther. 2, 416-430 (2003).
14. A. Gudkov, Microarray analysis of p53-mediated transcription: multi-thousand piece puzzle or invitation to collective thinking. Cancer Biol. Ther. 2, 444-445 (2003).
15. G. Gruel, C. Lucchesi, A. Pawlik, V. Frouin, O. Alibert, T. Kortulewski, A. Zarour, B. Jacquelin, X. Gidrol and D. Tronik-Le Roux, Novel microarray-based method for estimating exposure to ionizing radiation. Radiat. Res. 166, 746-756 (2006).
16. E. Hubbell, W. M. Liu and R. Mei, Robust estimators for expression analysis. Bioinformatics 18, 1585-1592 (2002).
17. L. J. Heyer, S. Kruglyak and S. Yooseph, Exploring expression data: identification and analysis of coexpressed genes. Genome Res. 9, 1106-1115 (1999).
18. M. W. Pfaffl, A new mathematical model for relative quantification in real-time RT- PCR. Nucleic Acids Res. 29, E45 (2001).
19. B. Jacquelin, T. Kortulewski, P. Vaigot, A. Pawlik, G. Gruel, O. Alibert, P. Soularue, C. Joubert, X. Gidrol and D. Tronik-Le Roux, Novel pathway for megakaryocyte production after in vivo conditional eradication of integrin alphaIIb-expressing cells. Blood 106, 1965-1974 (2005).
20. C. F. Bender, M. L. Sikes, R. Sullivan, L. E. Huye, M. M. Le Beau, D. B. Roth, O. K. Mirzoeva, E. M. Oltz and J. H. Petrini, Cancer predisposition and hematopoietic failure in Rad50(S/S) mice. Genes Dev. 16, 2237-2251 (2002).
21. M. B. Kastan and J. Bartek, Cell-cycle checkpoints and cancer. Nature 432, 316-323 (2004).
22. S. L. Wolin and T. Cedervall, The La protein. Annu. Rev. Biochem. 71, 375-403 (2002).
23. F. M. Uckun, K. G. Waddick, S. Mahajan, X. Jun, M. Takata, J. Bolen and T. Kurosaki, BTK as a mediator of radiation-induced apoptosis in DT-40 lymphoma B cells. Science 273, 1096-1100 (1996).
24. C. J. Johnston, J. P. Williams, P. Okunieff and J. N. Finkelstein, Radiation-induced pulmonary fibrosis: examination of chemo-kine and chemokine receptor families. Radiat. Res. 157, 256-265 (2002).
25. F. D'Agnillo and A. I. Alayash, Redox cycling of diaspirin cross-linked hemoglobin induces G2/M arrest and apoptosis in cultured endothelial cells. Blood 98, 3315-3323 (2001).
26. S. Y. Kim and Y. Kim, Genome-wide prediction of transcrip-tional regulatory elements of human promoters using gene expression and promoter analysis data. BMC Bioinformatics 7, 330-742 (2006).
27. C. Sarkar and A. Maitra, Deciphering the cis-regulatory elements of co-expressed genes in PCOS by in silico analysis. Gene 408, 72-84 (2008)
28. K. Ushizawa, T. Takahashi, M. Hosoe, H. Ishiwata, K.Kaneyama, K. Kizaki and K. Hashizume, Global gene expression analysis and regulation of the principal genes expressed in bovine placenta in relation to the transcription factor AP-2 family. Reprod. Biol. Endocrinol. 5, 17-34 (2007).
29. S. Veerla and M. Hoglund, Analysis of promoter regions of co-expressed genes identified by microarray analysis. BMC Bioinformatics 7, 384-399 (2006).
30. Y. Feng, X. Wang, L. Xu, H. Pan, S. Zhu, Q. Liang, B. Huang and J. Lu, The transcription factor ZBP-89 suppresses p16 expression through a histone modification mechanism to affect cell senescence. FEBS J. 276, 4197-4206 (2009).
31. K. Ohneda, S. Ohmori, Y. Ishijima, M. Nakano and M. Yamamoto, Characterization of a functional ZBP-89 binding site that mediates Gata1 gene expression during hematopoietic development. J. Biol. Chem. 284, 30187-99 (2009).
32. A. J. Woo, T. B. Moran, Y. L. Schindler, S. K. Choe, N. B. Langer, M. R. Sullivan, Y. Fujiwara, B. H. Paw and A. B. Cantor, Identification of ZBP-89 as a novel GATA-1-associated transcription factor involved in megakaryocytic and erythroid development. Mol. Cell Biol. 28, 2675-2689 (2008).
33. L. Bai and J. L. Merchant, Transcription factor ZBP-89 cooperates with histone acetyltransferase p300 during butyrate activation of p21waf1 transcription in human cells. J. Biol. Chem. 275, 30725-30733 (2000)
34. L. Bai and J. L. Merchant, ZBP-89 promotes growth arrest through stabilization of p53. Mol. Cell Biol. 21, 4670-4683 (2001).
35. X. Wang, R. C. Southard, C. D. Allred, D. R. Talbert, M. E. Wilson and M. W. Kilgore, MAZ drives tumor-specific expression of PPAR gamma 1 in breast cancer cells. Breast Cancer Res. Treat. 111, 103-111 (2008).
36. E. Myslinski, M. A. Gerard, A. Krol and P. Carbon, A genome scale location analysis of human Staf/ZNF143-binding sites suggests a widespread role for human Staf/ZNF143 in mammalian promoters. J. Biol. Chem. 281, 39953-39962 (2006).
37. M. Schaub, E. Myslinski, C. Schuster, A. Krol and P. Carbon, Staf, a promiscuous activator for enhanced transcription by RNA polymerases II and III. EMBO J. 16, 173-181 (1997).
38. G. Zheng and Y. C. Yang, ZNF76, a novel transcriptional repressor targeting TATA-binding protein, is modulated by sumoylation. J Biol. Chem. 279, 42410-42421 (2004).
39. S. Kondo, Apoptotic repair of genotoxic tissue damage and the role of p53 gene. Mutat. Res. 402, 311-319 (1998).
40. S. J. Kuerbitz, B. S. Plunkett, W. V. Walsh and M. B. Kastan, Wild-type p53 is a cell cycle checkpoint determinant following irradiation. Proc. Natl. Acad. Sci. USA 89, 7491-7495 (1992).
41. S. A. Lorimore, D. T. Goodhead and E. G. Wright, The effect of p53 status on the radiosensitivity of haemopoietic stem cells. Cell Death Differ. 2, 233-234 (1995).
42. V. Zuckerman, K. Wolyniec, R. V. Sionov, S. Haupt and Y. Haupt, Tumour suppression by p53: the importance of apoptosis and cellular senescence. J. Pathol. 219, 3-15 (2009).
43. W. S. el-Deiry, T. Tokino, V. E. Velculescu, D. B. Levy, R. Parsons, J. M. Trent, D. Lin, W. E. Mercer, K. W. Kinzler and B. Vogelstein, WAF1, a potential mediator of p53 tumor suppression. Cell 75, 817-825 (1993).
44. Z. Gu, C. Flemington, T. Chittenden and G. P. Zambetti, ei24, a p53 response gene involved in growth suppression and apoptosis. Mol. Cell. Biol. 20, 233-241 (2000).
45. T. Hettmann, K. Barton and J. M. Leiden, Microphthalmia due to p53-mediated apoptosis of anterior lens epithelial cells in mice lacking the CREB-2 transcription factor. Dev. Biol. 222, 110-123 (2000).
46. G. Yang, G. Zhang, M. R. Pittelkow, M. Ramoni and H. Tsao, Expression profiling of UVB response in melanocytes identifies a set of p53-target genes. J. Invest. Dermatol. 126, 2490-2506 (2006).
47. C. C. Chu and W. E. Paul, Fig1, an interleukin 4-induced mouse B cell gene isolated by cDNA representational difference analysis. Proc. Natl. Acad. Sci. USA 94, 2507-2512 (1997).
48. A. Carbonnelle-Puscian, C. Copie-Bergman, M. Baia, N. Martin-Garcia, Y. Allory, C. Haioun, A. Cremades, I. Abd-Alsamad, J. P. Farcet and V. Molinier-Frenkel, The novel immuno-suppressive enzyme IL4I1 is expressed by neoplastic cells of several B-cell lymphomas and by tumor-associated macrophages. Leukemia 23, 952-960 (2009).
49. A. A. Raibekas and V. Massey, Primary structure of the snake venom L-amino acid oxidase shows high homology with the mouse B cell interleukin 4-induced Fig1 protein. Biochem. Biophys. Res. Commun. 248, 476-478 (1998).
50. S. Torii, K. Yamane, T. Mashima, N. Haga, K. Yamamoto, J. W. Fox, M. Naito and T. Tsuruo, Molecular cloning and functional analysis of apoxin I, a snake venom-derived apoptosis-inducing factor with L-amino acid oxidase activity. Biochemistry 39, 3197-3205 (2000).
51. M. L. Boulland, J. Marquet, V. Molinier-Frenkel, P. Moller, C. Guiter, F. Lasoudris, C. Copie-Bergman, M. Baia, P. Gaulard and F. Castellano, Human IL4I1 is a secreted L-phenylalanine oxidase expressed by mature dendritic cells that inhibits T-lymphocyte proliferation. Blood 110, 220-227 (2007).
52. J. Abe and B. C. Berk, Fyn and JAK2 mediate Ras activation by reactive oxygen species. J. Biol. Chem. 274, 21003-21010 (1999).
53. M. Carballo, M. Conde, R. El Bekay, J. Martin-Nieto, M. J. Camacho, J. Monteseirin, J. Conde, F. J. Bedoya and F. Sobrino, Oxidative stress triggers STAT3 tyrosine phosphorylation and nuclear translocation in human lymphocytes. J. Biol. Chem. 274, 17580-17586 (1999).
54. B. Kretschmer, K. Luthje, S. Schneider, B. Fleischer and M. Breloer, Engagement of CD83 on B cells modulates B cell function in vivo. J. Immunol. 182, 2827-2834 (2009).
55. M. Lechmann, S. Berchtold, J. Hauber and A. Steinkasserer, CD83 on dendritic cells: more than just a marker for maturation. Trends Immunol. 23, 273-275 (2002).
56. E. C. Pietsch, S. M. Sykes, S. B. McMahon and M. E. Murphy, The p53 family and programmed cell death. Oncogene 27, 6507-6521 (2008).
57. W. S. Wu, S. Heinrichs, D. Xu, S. P. Garrison, G. P. Zambetti, J. M. Adams and A. T. Look, Slug antagonizes p53-mediated apoptosis of hematopoietic progenitors by repressing puma. Cell 123, 641-653 (2005).
58. J. Yu and L. Zhang, The transcriptional targets of p53 in apoptosis control. Biochem Biophys. Res. Commun. 331, 851-858 (2005).
59. K. J. Lindsay, P. J. Coates, S. A. Lorimore and E. G. Wright, The genetic basis of tissue responses to ionizing radiation. Br. J. Radiol. 80 (Spec. No. 1), S2-S6 (2007).
60. D. Suciu, Protein composition of cells, nuclei and chromatin from some radiosensitive and radioresistant mouse tissues. Int. J. Radiat. Biol. Relat. Stud. Phys. Chem. Med. 39, 641-647 (1981). (Pubitemid 11112543)
61. B. Foss, T. Hervig and O. Bruserud, Connexins are active participants of hematopoietic stem cell regulation. Stem Cells Dev. 18, 807-812 (2009).
62. T. Krenacs and M. Rosendaal, Connexin43 gap junctions in normal, regenerating and cultured mouse bone marrow and in human leukemias: their possible involvement in blood formation. Am. J. Pathol. 152, 993-1004 (1998)
63. E. Montecino-Rodriguez, H. Leathers and K. Dorshkind, Expression of connexin 43 (Cx43) is critical for normal hematopoiesis. Blood 96, 917-924 (2000).
64. W. Wagner, F. Wein, C. Roderburg, R. Saffrich, A. Faber, U. Krause, M. Schubert, V. Benes, V. Eckstein and A. D. Ho, Adhesion of hematopoietic progenitor cells to human mesenchymal stem cells as a model for cell-cell interaction. Exp. Hematol. 35, 314-325 (2007).
65. D. Glover, J. B. Little, M. F. Lavin and N. Gueven, Low dose ionizing radiation-induced activation of connexin 43 expression. Int. J. Radiat. Biol. 79: 955-964 (2003).
66. E. I. Azzam, S. M. de Toledo and J. B. Little, Expression of CONNEXIN43 is highly sensitive to ionizing radiation and other environmental stresses. Cancer Res. 63, 7128-7135 (2003).
67. R. J. Francis and C. W. Lo, Primordial germ cell deficiency in the connexin 43 knockout mouse arises from apoptosis associated with abnormal p53 activation. Development 133, 3451-3460 (2006).
68. A. Rodriguez-Sinovas, A. Cabestrero, D. Lopez, I. Torre, M. Morente, A. Abellan, E. Miro, M. Ruiz-Meana and D. Garcia-Dorado, The modulatory effects of connexin 43 on cell death/ survival beyond cell coupling. Prog. Biophys. Mol. Biol. 94, 219-232 (2007).
69. W. Hu, Z. Feng, A. K. Teresky and A. J. Levine, p53 regulates maternal reproduction through LIF. Nature 450, 721-724 (2007).
70. H. Niwa, K. Ogawa, D. Shimosato and K. Adachi, A parallel circuit of LIF signalling pathways maintains pluripotency of mouse ES cells. Nature 460, 118-122 (2009).
71. E. J. Kim, J. I. Park and B. D. Nelkin, IFI16 is an essential mediator of growth inhibition, but not differentiation, induced by the leukemia inhibitory factor/JAK/STAT pathway in medullary thyroid carcinoma cells. J. Biol. Chem. 280, 4913-4920 (2005).
72. H. Slaets, D. Dumont, J. Vanderlocht, J. P. Noben, P. Leprince, J. Robben, J. Hendriks, P. Stinissen and N. Hellings, Leukemia inhibitory factor induces an antiapoptotic response in oligodendrocytes through Akt-phosphorylation and up-regulation of 14-3-3. Proteomics 8, 1237-1247 (2008).
73. A. Abdollahi, D. W. Griggs, H. Zieher, A. Roth, K. E. Lipson, R. Saffrich, H. J. Grone, D. E. Hallahan, R. A. Reisfeld and P.E. Huber, Inhibition of alpha(v)beta3 integrin survival signaling enhances antiangiogenic and antitumor effects of radiotherapy. Clin. Cancer Res. 11, 6270-6279 (2005).
74. E. Decrock, M. Vinken, E. De Vuyst, D. V. Krysko, K. D'Herde, T. Vanhaecke, P. Vandenabeele, V. Rogiers and L. Leybaert, Connexin-related signaling in cell death: to live or let die? Cell Death Differ. 16, 524-536 (2009).
75. M. R. Wilson, T. W. Close and J. E. Trosko, Cell population dynamics (apoptosis, mitosis and cell-cell communication) during disruption of homeostasis. Exp. Cell Res. 254, 257-268 (2000).
76. Y. Liu, S. E. Elf, Y. Miyata, G. Sashida, Y. Liu, G. Huang, S. Di Giandomenico, J. M. Lee, A. Deblasio and S. D. Nimer, p53 regulates hematopoietic stem cell quiescence. Cell Stem Cell 4, 37-48 (2009).