Evaluation of systemic markers of inflammation in atomic-bomb survivors with special reference to radiation and age effects

FASEB Journal

Volumn 26, Issue 11, 2012, Pages 4765-4773

  Hayashi, Tomonori ^a   Morishita, Yukari ^a   Khattree, Ravindra ^a   Misumi, Munechika ^b   Sasaki, Keiko ^a   Hayashi, Ikue ^c   Yoshida, Kengo ^a   Kajimura, Junko ^a   Kyoizumi, Seishi ^a   Imai, Kazue ^a   Kusunoki, Yoichiro ^a   Nakachi, Kei ^a  

^a RADIATION EFFECTS RESEARCH FOUNDATION   (Japan)

^b OAKLAND UNIVERSITY   (United States)

^c HIROSHIMA UNIVERSITY   (Japan)

Author keywords

Cytokines; Immunosenescence; Reactive oxygen species

Indexed keywords

BIOLOGICAL MARKER; C REACTIVE PROTEIN; CD4 ANTIGEN; IMMUNOGLOBULIN; INTERLEUKIN 10; INTERLEUKIN 4; INTERLEUKIN 6; REACTIVE OXYGEN METABOLITE; TUMOR NECROSIS FACTOR ALPHA;

AGED; AGING; ARTICLE; ATOMIC BOMB; ATOMIC BOMB SURVIVOR; CD4+ T LYMPHOCYTE; DOSIMETRY; ERYTHROCYTE SEDIMENTATION RATE; FEMALE; HUMAN; INFLAMMATION; MAJOR CLINICAL STUDY; MALE; PRIORITY JOURNAL; RADIATION EXPOSURE; WHOLE BODY RADIATION;

AGED; AGING; BIOLOGICAL MARKERS; CYTOKINES; FEMALE; HUMANS; INFLAMMATION; JAPAN; LINEAR MODELS; MALE; MIDDLE AGED; NUCLEAR WARFARE; NUCLEAR WEAPONS; RADIATION DOSAGE; RADIATION INJURIES; REACTIVE OXYGEN SPECIES;

EID: 84868271201     PISSN: None     EISSN: 15306860     Source Type: Journal    
DOI: 10.1096/fj.12-215228     Document Type: Article

References (57)

1. Douple, E. B., Mabuchi, K., Cullings, H. M., Preston, D. L., Kodama, K., Shimizu, Y., Fujiwara, S., and Shore, R. E. (2011) Long-term radiation-related health effects in a unique human population: lessons learned from the atomic bomb survivors of Hiroshima and Nagasaki. Disaster Med. Public Health Prep. 5(Suppl. 1), S122-S133
2. Kodama, K., Sasaki, H., and Shimizu, Y. (1990) Trend of coronary heart disease and its relationship to risk factors in a Japanese population: a 26-year follow-up, Hiroshima/Nagasaki study. Jpn. Circ. J. 54, 414-421
3. Pierce, D. A., Shimizu, Y., Preston, D. L., Vaeth, M., and Mabuchi, K. (1996) Studies of the mortality of atomic bomb survivors. Report 12, Part I. Cancer: 1950-1990. Radiat. Res. 146, 1-27
4. Sharp, G. B., Mizuno, T., Cologne, J. B., Fukuhara, T., Fujiwara, S., Tokuoka, S., and Mabuchi, K. (2003) Hepatocellular carcinoma among atomic bomb survivors: significant interaction of radiation with hepatitis C virus infections. Int. J. Cancer 103, 531-537
5. Preston, D. L., Ron, E., Tokuoka, S., Funamoto, S., Nishi, N., Soda, M., Mabuchi, K., and Kodama, K. (2007) Solid cancer incidence in atomic bomb survivors: 1958-1998. Radiat. Res. 168, 1-64
6. Ozasa, K., Shimizu, Y., Suyama, A., Kasagi, F., Soda, M., Grant, E. J., Sakata, R., Sugiyama, H., and Kodama, K. (2012) Studies of the mortality of atomic bomb survivors, Report 14, 1950-2003: an overview of cancer and noncancer diseases. Radiat. Res. 177, 229-243
7. Bretz, W. A., Weyant, R. J., Corby, P. M., Ren, D., Weissfeld, L., Kritchevsky, S. B., Harris, T., Kurella, M., Satterfield, S., Visser, M., and Newman, A. B. (2005) Systemic inflammatory markers, periodontal diseases, and periodontal infections in an elderly population. J. Am. Geriatr. Soc. 53, 1532-1537
8. Ungvari, Z., Csiszar, A., and Kaley, G. (2004) Vascular inflammation in aging. Herz. 29, 733-740
9. Krabbe, K. S., Pedersen, M., and Bruunsgaard, H. (2004) Inflammatory mediators in the elderly. Exp. Gerontol. 39, 687-699
10. Harris, T. B., Ferrucci, L., Tracy, R. P., Corti, M. C., Wacholder, S., Ettinger, W. H., Jr., Heimovitz, H., Cohen, H. J., and Wallace, R. (1999) Associations of elevated interleukin-6 and C-reactive protein levels with mortality in the elderly. Am. J. Med. 106, 506-512
11. Van der Meide, P. H., and Schellekens, H. (1996) Cytokines and the immune response. Biotherapy 8, 243-249
12. Pannen, B. H., and Robotham, J. L. (1995) The acute-phase response. New Horiz. 3, 183-197
13. Lu, Z. Y., Brailly, H., Wijdenes, J., Bataille, R., Rossi, J. F., and Klein, B. (1995) Measurement of whole body interleukin-6 (IL-6) production: prediction of the efficacy of anti-IL-6 treatments. Blood 86, 3123-3131
14. Fey, G. H., Hattori, M., Hocke, G., Brechner, T., Baffet, G., Baumann, M., Baumann, H., and Northemann, W. (1991) Gene regulation by interleukin 6. Biochimie (Paris) 73, 47-50
15. Tracey, K. J. (2002) The inflammatory reflex. Nature 420, 853-859
16. Dinarello, C. A. (1991) Interleukin-1 and interleukin-1 antagonism. Blood 77, 1627-1652
17. Papadaki, H. A., Eliopoulos, D. G., Ponticoglou, C., and Eliopoulos, G. D. (2001) Increased frequency of monoclonal gammopathy of undetermined significance in patients with nonimmune chronic idiopathic neutropenia syndrome. Int. J. Hematol. 73, 339-345
18. Roxburgh, C. S., and McMillan, D. C. (2010) Role of systemic inflammatory response in predicting survival in patients with primary operable cancer. Future Oncol. 6, 149-163
19. Macarthur, M., Hold, G. L., and El-Omar, E. M. (2004) Inflammation and Cancer II. Role of chronic inflammation and cytokine gene polymorphisms in the pathogenesis of gastrointestinal malignancy. Am. J. Physiol. Gastrointest. Liver Physiol. 286, G515-G520
20. Willcox, J. K., Ash, S. L., and Catignani, G. L. (2004) Antioxidants and prevention of chronic disease. Crit. Rev. Food Sci. Nutr. 44, 275-295
21. Peters, T., Weiss, J. M., Sindrilaru, A., Wang, H., Oreshkova, T., Wlaschek, M., Maity, P., Reimann, J., and Scharffetter-Kochanek, K. (2009) Reactive oxygen intermediate-induced pathomechanisms contribute to immunosenescence, chronic inflammation and autoimmunity. Mech. Ageing Dev. 130, 564-587
22. Federico, A., Morgillo, F., Tuccillo, C., Ciardiello, F., and Loguercio, C. (2007) Chronic inflammation and oxidative stress in human carcinogenesis. Int. J. Cancer. 121, 2381-2386
23. Chung, J., Lee, H. S., Chung, H. Y., Yoon, T. R., and Kim, H. K. (2008) Salicylideneamino-2-thiophenol inhibits inflammatory mediator genes (RANTES, MCP-1, IL-8 and HIF-1alpha) expression induced by tert-butyl hydroperoxide via MAPK pathways in rat peritoneal macrophages. Biotechnol. Lett. 30, 1553-1558
24. Papa, S., Zazzeroni, F., Pham, C. G., Bubici, C., and Franzoso, G. (2004) Linking JNK signaling to NF-kappaB: a key to survival. J. Cell Sci. 117, 5197-5208
25. Papa, S., Bubici, C., Zazzeroni, F., Pham, C. G., Kuntzen, C., Knabb, J. R., Dean, K., and Franzoso, G. (2006) The NF-kappaBmediated control of the JNK cascade in the antagonism of programmed cell death in health and disease. Cell Death Differ. 13, 712-729
26. Wullaert, A., Heyninck, K., and Beyaert, R. (2006) Mechanisms of crosstalk between TNF-induced NF-kappaB and JNK activation in hepatocytes. Biochem. Pharmacol. 72, 1090-1101
27. Bubici, C., Papa, S., Dean, K., and Franzoso, G. (2006) Mutual cross-talk between reactive oxygen species and nuclear factorkappa B: molecular basis and biological significance. Oncogene 25, 6731-6748
28. Goossens, V., De Vos, K., Vercammen, D., Steemans, M., Vancompernolle, K., Fiers, W., Vandenabeele, P., and Grooten, J. (1999) Redox regulation of TNF signaling. Biofactors 10, 145-156
29. Sone, H., Akanuma, H., and Fukuda, T. (2010) Oxygenomics in environmental stress. Redox Rep. 15, 98-114
30. Cullings, H. M., Fujita, S., Funamoto, S., Grant, E. J., Kerr, G. D., and Preston, D. L. (2006) Dose estimation for atomic bomb survivor studies: its evolution and present status. Radiat. Res. 166, 219-254
31. Hayashi, I., Morishita, Y., Imai, K., Nakamura, M., Nakachi, K., and Hayashi, T. (2007) High-throughput spectrophotometric assay of reactive oxygen species in serum. Mutat. Res. 631, 55-61
32. Hayashi, T., Morishita, Y., Kubo, Y., Kusunoki, Y., Hayashi, I., Kasagi, F., Hakoda, M., Kyoizumi, S., and Nakachi, K. (2005) Long-term effects of radiation dose on inflammatory markers in atomic bomb survivors. Am. J. Med. 118, 83-86
33. Neriishi, K., Nakashima, E., and Delongchamp, R. R. (2001) Persistent subclinical inflammation among A-bomb survivors. Int. J. Radiat. Biol. 77, 475-482
34. Kusunoki, Y., Kyoizumi, S., Hirai, Y., Suzuki, T., Nakashima, E., Kodama, K., and Seyama, T. (1998) Flow cytometry measurements of subsets of T, B and NK cells in peripheral blood lymphocytes of atomic bomb survivors. Radiat. Res. 150, 227-236
35. Khattree, R., and Naik, D. N. (1999) Applied Multivariate Statistics with SAS Software, SAS Press/Wiley, Cary, NC, USA
36. Khattree, R., and Naik, D. N. (2000) Multivariate Data Reduction and Discrimination with SAS Software, SAS Press/Wiley, Cary, NC, USA
37. Bishop, Y. M., Fienberg, S. E., Holland, P. W., and Light, R. J. (2007) Discrete Multivariate Analysis: Theory and Practice, Springer, London
38. Hayashi, T., Kusunoki, Y., Hakoda, M., Morishita, Y., Kubo, Y., Maki, M., Kasagi, F., Kodama, K., Macphee, D. G., and Kyoizumi, S. (2003) Radiation dose-dependent increases in inflammatory response markers in A-bomb survivors. Int. J. Radiat. Biol. 79, 129-136
39. Lambeth, J. D. (2004) NOX enzymes and the biology of reactive oxygen. Nat. Rev. Immunol. 4, 181-189
40. Kanayama, A., and Miyamoto, Y. (2007) Apoptosis triggered by phagocytosis-related oxidative stress through FLIPS down-regulation and JNK activation. J. Leukoc. Biol. 82, 1344-1352
41. Mantovani, G., Maccio, A., Madeddu, C., Mura, L., Gramignano, G., Lusso, M. R., Mulas, C., Mudu, M. C., Murgia, V., Camboni, P., Massa, E., Ferreli, L., Contu, P., Rinaldi, A., Sanjust, E., Atzei, D., and Elsener, B. (2002) Quantitative evaluation of oxidative stress, chronic inflammatory indices and leptin in cancer patients: correlation with stage and performance status. Int. J. Cancer 98, 84-91
42. Dobbs, R. J., Charlett, A., Purkiss, A. G., Dobbs, S. M., Weller, C., and Peterson, D. W. (1999) Association of circulating TNF-Alpha and IL-6 with ageing and parkinsonism. Acta Neurol. Scand. 100, 34-41
43. Ballou, S. P., Lozanski, F. B., Hodder, S., Rzewnicki, D. L., Mion, L. C., Sipe, J. D., Ford, A. B., and Kushner, I. (1996) Quantitative and qualitative alterations of acute-phase proteins in healthy elderly persons. Age Ageing 25, 224-230
44. Solana, R., and Mariani, E. (2000) NK and NK/T cells in human senescence. Vaccine 18, 1613-1620
45. Rink, L., Cakman, I., and Kirchner, H. (1998) Altered cytokine production in the elderly. Mech. Ageing Dev. 102, 199-209
46. Pedersen, B. K., and Bruunsgaard, H. (2003) Possible beneficial role of exercise in modulating low-grade inflammation in the elderly. Scand. J. Med. Sci. Sports 13, 56-62
47. Cubbon, R. M., Kahn, M. B., and Wheatcroft, S. B. (2009) Effects of insulin resistance on endothelial progenitor cells and vascular repair. Clin. Sci. (London) 117, 173-190
48. Galkina, E., and Ley, K. (2009) Immune and inflammatory mechanisms of atherosclerosis (*). Ann. Rev. Immunol. 27, 165-197
49. Ridker, P. M., Rifai, N., Stampfer, M. J., and Hennekens, C. H. (2000) Plasma concentration of interleukin-6 and the risk of future myocardial infarction among apparently healthy men. Circulation 101, 1767-1772
50. Griselli, M., Herbert, J., Hutchinson, W. L., Taylor, K. M., Sohail, M., Krausz, T., and Pepys, M. B. (1999) C-reactive protein and complement are important mediators of tissue damage in acute myocardial infarction. J. Exp. Med. 190, 1733-1740
51. Cesselli, D., Jakoniuk, I., Barlucchi, L., Beltrami, A. P., Hintze, T. H., Nadal-Ginard, B., Kajstura, J., Leri, A., and Anversa, P. (2001) Oxidative stress-mediated cardiac cell death is a major determinant of ventricular dysfunction and failure in dog dilated cardiomyopathy. Circ. Res. 89, 279-286
52. Ferrari, R., Guardigli, G., Mele, D., Percoco, G. F., Ceconi, C., and Curello, S. (2004) Oxidative stress during myocardial ischaemia and heart failure. Curr. Pharm. Des. 10, 1699-1711
53. Giordano, F. J. (2005) Oxygen, oxidative stress, hypoxia, and heart failure. J. Clin. Invest. 115, 500-508
54. Landmesser, U., Spiekermann, S., Dikalov, S., Tatge, H., Wilke, R., Kohler, C., Harrison, D. G., Hornig, B., and Drexler, H. (2002) Vascular oxidative stress and endothelial dysfunction in patients with chronic heart failure: role of xanthine-oxidase and extracellular superoxide dismutase. Circulation 106, 3073-3078
55. Li, J. M., and Shah, A. M. (2004) Endothelial cell superoxide generation: regulation and relevance for cardiovascular pathophysiology. Am. J. Physiol. 287, R1014-R1030
56. Kusunoki, Y., Yamaoka, M., Kasagi, F., Hayashi, T., Koyama, K., Kodama, K., MacPhee, D. G., and Kyoizumi, S. (2002) T cells of atomic bomb survivors respond poorly to stimulation by Staphylococcus aureus toxins in vitro: does this stem from their peripheral lymphocyte populations having a diminished naive CD4 T-cell content? Radiat. Res. 158, 715-724
57. Kusunoki, Y., Kyoizumi, S., Yamaoka, M., Kasagi, F., Kodama, K., and Seyama, T. (1999) Decreased proportion of CD4 T cells in the blood of atomic bomb survivors with myocardial infarction. Radiat. Res. 152, 539-543