Mast cells and ionizing radiation induce a synergistic expression of inflammatory genes in endothelial cells by a Mechanism involving p38α MAP Kinase and (p65) NF-κB activation

Radiation Research

Volumn 178, Issue 6, 2012, Pages 556-567

  Blirando, Karl ^a   Hneino, Mohammad ^a   Martelly, Isabelle ^b   Benderitter, Marc ^a   Milliat, Fabien ^a   François, Agnès ^a  

^a INSTITUT DE RADIOPROTECTION ET DE SÛRETÉ NUCLÉAIRE IRSN   (France)

^b UNIVERSITÉ PARIS EST CRÉTEIL   (France)

Author keywords

[No Author keywords available]

Indexed keywords

CXCL2 CHEMOKINE; ENDOTHELIAL LEUKOCYTE ADHESION MOLECULE 1; INTERLEUKIN 6; INTERLEUKIN 8; MEPYRAMINE; MITOGEN ACTIVATED PROTEIN KINASE 14; TRANSCRIPTION FACTOR RELA;

ARTICLE; CELL ACTIVATION; CELL INTERACTION; CONTROLLED STUDY; DRUG EFFECT; ENDOTHELIUM CELL; ENZYME INHIBITION; GENE EXPRESSION; HUMAN; HUMAN CELL; INFLAMMATION; IONIZING RADIATION; MAST CELL; PRIORITY JOURNAL;

CDC42 GTP-BINDING PROTEIN; CELL LINE, TUMOR; CULTURE MEDIA, CONDITIONED; ENZYME ACTIVATION; GENE EXPRESSION REGULATION; GENE SILENCING; HISTAMINE; HUMAN UMBILICAL VEIN ENDOTHELIAL CELLS; HUMANS; INFLAMMATION; INTERLEUKIN-6; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; MAST CELLS; P38 MITOGEN-ACTIVATED PROTEIN KINASES; PHOSPHORYLATION; PROTEIN KINASE INHIBITORS; PROTEIN-SERINE-THREONINE KINASES; TRANSCRIPTION FACTOR RELA;

EID: 84870914919     PISSN: 00337587     EISSN: 19385404     Source Type: Journal    
DOI: 10.1667/RR3058.1     Document Type: Article

References (47)

1. Bentzen SM. Preventing or reducing late side effects of radiation therapy: radiobiology meets molecular pathology. Nature Rev Cancer 2006; 6(9):702-13. Epub 2006/08/25.
2. Wang J, Boerma M, Fu Q, Hauer-Jensen M. Significance of endothelial dysfunction in the pathogenesis of early and delayed radiation enteropathy. World J Gastroenterol 2007; 13(22): 3047-55. Epub 2007/06/26.
3. Meeren AV, Bertho JM, Vandamme M, Gaugler MH. Ionizing radiation enhances IL-6 and IL-8 production by human endothelial cells. Mediat Inflam 1997; 6(3):185-93. Epub 1997/01/01.
4. Gaugler MH, Squiban C, van der Meeren A, Bertho JM, Vandamme M, Mouthon MA. Late and persistent up-regulation of intercellular adhesion molecule-1 (ICAM-1) expression by ionizing radiation in human endothelial cells in vitro. Int J Radiat Biol 1997; 72(2):201-9. Epub 1997/08/01.
5. Chang CC, Lerman OZ, Thanik VD, Scharf CL, Greives MR, Schneider RJ, et al. Dose-dependent effect of radiation on angiogenic and angiostatic CXC chemokine expression in human endothelial cells. Cytokine 2009; 48(3):295-302. Epub 2009/09/29.
6. Soloviev AI, Tishkin SM, Parshikov AV, Ivanova IV, Goncharov EV, Gurney AM. Mechanisms of endothelial dysfunction after ionized radiation: selective impairment of the nitric oxide component of endothelium-dependent vasodilation. Br J Pharmacol 2003; 138(5):837-44. Epub 2003/03/19.
7. Milliat F, Sabourin JC, Tarlet G, Holler V, Deutsch E, Buard V, et al. Essential role of plasminogen activator inhibitor type-1 in radiation enteropathy. Am J Pathol 2008;172(3):691-701.
8. Verheij M, Dewit LG, van Mourik JA. The effect of ionizing radiation on endothelial tissue factor activity and its cellular localization. Thromb Haemost 1995; 73(5):894-5. Epub 1995/05/01.
9. Zhou Q, Zhao Y, Li P, Bai X, Ruan C. Thrombomodulin as a marker of radiation-induced endothelial cell injury. Radiat Res 1992; 131(3):285-9. Epub 1992/09/01.
10. Van der Meeren A, Vandamme M, Squiban C, Gaugler MH, Mouthon MA. Inflammatory reaction and changes in expression of coagulation proteins on lung endothelial cells after total-body irradiation in mice. Radiat Res 2003; 160(6):637-46. Epub 2003/12/04.
11. Chon BH, Loeffler JS. The effect of nonmalignant systemic disease on tolerance to radiation therapy. Oncologist 2002; 7(2): 136-43.
12. Bourgier C, Vozenin MC, Deutsch E. Reirradiation des tissus sains: donnees radiobiologiques precliniques. (Reirradiation of normal tissues: preclinical radiobiological data.) Cancer radiotherapie. J Soc Franc Radiother Oncol 2010; 14(6-7):412-5. Epub 2010/08/24.
13. Denham JW, Hauer-Jensen M. The radiotherapeutic injury - a complex 'wound'. Radiother Oncol 2002; 63(2):129-45.
14. Hofmann AM, Abraham SN. New roles for mast cells in modulating allergic reactions and immunity against pathogens. Curr Opin Immunol 2009; 21(6):679-86. Epub 2009/10/16.
15. Moon TC, St Laurent CD, Morris KE, Marcet C, Yoshimura T, Sekar Y, et al. Advances in mast cell biology: new understanding of heterogeneity and function. Mucosal Immunol 2010; 3(2): 111-28. Epub 2010/01/01.
16. Gilfillan AM, Tkaczyk C. Integrated signalling pathways for mast-cell activation. Nature Rev Immunol 2006; 6(3):218-30. Epub 2006/02/14.
17. Lindsberg PJ, Strbian D, Karjalainen-Lindsberg ML. Mast cells as early responders in the regulation of acute blood-brain barrier changes after cerebral ischemia and hemorrhage. J Cerebral Blood Flow Metabol 2010; 30(4):689-702. Epub 2010/01/21.
18. Li Y, Stechschulte AC, Smith DD, Lindsley HB, Stechschulte DJ, Dileepan KN. Mast cell granules potentiate endotoxin-induced interleukin-6 production by endothelial cells. J Leuko Bio 1997; 62(2):211-6. Epub 1997/08/01.
19. Chou CH, Chen SU, Cheng JC. Radiation-induced interleukin-6 expression through MAPK/p38/NF-kappaB signaling pathway and the resultant antiapoptotic effect on endothelial cells through Mcl-1 expression with sIL6-Ralpha. Int J Radiat Oncol Biol Phys 2009; 75(5):1553-61. Epub 2009/11/26.
20. Blirando K, Milliat F, Martelly I, Sabourin JC, Benderitter M, Francois A. Mast cells are an essential component of human radiation proctitis and contribute to experimental colorectal damage in mice. Am J Pathol 178(2):640-51. Epub 2011/02/02.
21. Pober JS, Sessa WC. Evolving functions of endothelial cells in inflammation. Nature Rev Immunol 2007; 7(10):803-15. Epub 2007/09/26.
22. Gaugler MH. A unifying system: does the vascular endothelium have a role to play in multi-organ failure following radiation exposure? BJR supplement/BIR 2005; 27:100-5. Epub 2005/06/ 25.
23. Matsumoto T, Mugishima H. Signal transduction via vascular endothelial growth factor (VEGF) receptors and their roles in atherogenesis. J Athero Thromb 2006; 13(3):130-5. Epub 2006/07/13.
24. Ghosh S, Hayden MS. New regulators of NF-kappaB in inflammation. Nature Rev Immunol 2008; 8(11):837-48. Epub 2008/10/18.
25. Cuadrado A, Nebreda AR. Mechanisms and functions of p38 MAPK signalling. Biochem J 2010; 429(3):403-17. Epub 2010/07/16.
26. Galli SJ, Kalesnikoff J, Grimbaldeston MA, Piliponsky AM, Williams CM, Tsai M. Mast cells as "tunable" effector and immunoregulatory cells: recent advances. Annu Rev Immunol 2005; 23:749-86. Epub 2005/03/18.
27. Cantarella G, Scollo M, Lempereur L, Saccani-Jotti G, Basile F, Bernardini R. Endocannabinoids inhibit release of nerve growth factor by inflammation-activated mast cells. Biochem Pharmacol 2011; 82(4):380-8. Epub 2011/05/24.
28. Zheng H, Wang J, Hauer-Jensen M. Role of mast cells in early and delayed radiation injury in rat intestine. Radiat Res 2000; 153(5): 533-9.
29. Thomas DM, Fox J, Haston CK. Imatinib therapy reduces radiation-induced pulmonary mast cell influx and delays lung disease in the mouse. Int J Radiat Biol 2010; 86(6):436-44. Epub 2010/05/18.
30. Li Y, Chi L, Stechschulte DJ, Dileepan KN. Histamine-induced production of interleukin-6 and interleukin-8 by human coronary artery endothelial cells is enhanced by endotoxin and tumor necrosis factor-alpha. Microvas Res 2001; 61(3):253-62. Epub 2001/05/05.
31. Moriyasu S, Yamamoto K, Kureyama N, Okamura K, Ikeda T, Yamatodani A. Involvement of histamine released from mast cells in acute radiation dermatitis in mice. J Pharmacol Sci 2007; 104(2):187-90.
32. MacGlashan D, Jr. Histamine: A mediator of inflammation. J Allergy Clin Immunol 2003; 112(4 Suppl):S53-9. Epub 2003/10/08.
33. Haase MG, Klawitter A, Geyer P, Alheit H, Baumann M, Kriegel TM, et al. Sustained elevation of NF-kappaB DNA binding activity in radiation-induced lung damage in rats. Int J Radiat Biol 2003;79(11):863-77. Epub 2003/12/31.
34. Halle M, Gabrielsen A, Paulsson-Berne G, Gahm C, Agardh HE, Farnebo F, et al. Sustained inflammation due to nuclear factorkappa B activation in irradiated human arteries. J Am Col Cardiol 2010; 55(12):1227-36. Epub 2010/03/20.
35. Wang Y, Meng A, Lang H, Brown SA, Konopa JL, Kindy MS, et al. Activation of nuclear factor kappaB in vivo selectively protects the murine small intestine against ionizing radiation-induced damage. Cancer Res 2004;64(17):6240-6.
36. Burdelya LG, Krivokrysenko VI, Tallant TC, Strom E, Gleiberman AS, Gupta D, et al. An agonist of toll-like receptor 5 has radioprotective activity in mouse and primate models. Science 2008; 320(5873):226-30. Epub 2008/04/12.
37. Pearson G, Robinson F, Beers Gibson T, Xu BE, Karandikar M, Berman K, et al. Mitogen-activated protein (MAP) kinase pathways: regulation and physiological functions. Endoc Rev 2001; 22(2):153-83. Epub 2001/04/11.
38. Dent P, Yacoub A, Fisher PB, Hagan MP, Grant S. MAPK pathways in radiation responses. Oncogene 2003; 22(37):5885-96. Epub 2003/08/30.
39. Mihaescu A, Santen S, Jeppsson B, Thorlacius H. p38 Mitogen-activated protein kinase signalling regulates vascular inflammation and epithelial barrier dysfunction in an experimental model of radiation-induced colitis. Br J Surg 2010; 97(2):226-34. Epub 2009/12/25.
40. Hommes D, van den Blink B, Plasse T, Bartelsman J, Xu C, Macpherson B, et al. Inhibition of stress-activated MAP kinases induces clinical improvement in moderate to severe Crohn's disease. Gastroenterology 2002; 122(1):7-14. Epub 2002/01/10.
41. Otsuka M, Kang YJ, Ren J, Jiang H, Wang Y, Omata M, et al. Distinct effects of p38alpha deletion in myeloid lineage and gut epithelia in mouse models of inflammatory bowel disease. Gastroenterology 2010; 138(4):1255-65. Epub 2010/01/19.
42. Kumar P, Miller AI, Polverini PJ. p38 MAPK mediates gamma-irradiation- induced endothelial cell apoptosis, and vascular endothelial growth factor protects endothelial cells through the phosphoinositide 3-kinase-Akt-Bcl-2 pathway. J Biol Chem 2004; 279(41):43352-60. Epub 2004/08/05.
43. Dean JL, Sully G, Clark AR, Saklatvala J. The involvement of AU-rich element-binding proteins in p38 mitogen-activated protein kinase pathway-mediated mRNA stabilisation. Cell Sign 2004; 16(10):1113-21. Epub 2004/07/09.
44. Zhao W, Liu M, Kirkwood KL. p38alpha stabilizes interleukin-6 mRNA via multiple AU-rich elements. J Biol Chem 2008; 283(4): 1778-85. Epub 2007/11/29.
45. Gorska MM, Liang Q, Stafford SJ, Goplen N, Dharajiya N, Guo L, et al. MK2 controls the level of negative feedback in the NF-kappaB pathway and is essential for vascular permeability and airway inflammation. J Experim Med 2007; 204(7):1637-52. Epub 2007/06/20.
46. Pan WW, Li JD, Huang S, Papadimos TJ, Pan ZK, Chen LY. Synergistic activation of NF-fkappagB by bacterial chemoattractant and TNFfalphag is mediated by p38 MAPK-dependent RelA acetylation. J Biol Chem 2010; 285(45):34348-54. Epub 2010/08/24.
47. Gaestel M, Mengel A, Bothe U, Asadullah K. Protein kinases as small molecule inhibitor targets in inflammation. Curr Medicinal Chem 2007; 14(21):2214-34. Epub 2007/09/28.