Intestinal microbiota reduces genotoxic endpoints induced by high-energy protons

Radiation Research

Volumn 181, Issue 1, 2014, Pages 45-53

  Maier, Irene ^a   Berry, David M ^b   Schiestl, Robert H ^a,c  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF VIENNA   (Austria)

^c UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

GLUTATHIONE; HISTONE H2AX; RIBOSOME RNA;

ADAPTIVE IMMUNITY; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BACTEROIDES; BARNESIELLA INTESTIHOMINIS; CHROMOSOME ABERRATION; CONTROLLED STUDY; COSMIC RADIATION; DNA DAMAGE; DNA REPAIR; DNA STRAND BREAKAGE; FEMALE; GENE SEQUENCE; GENOTOXICITY; HELICOBACTER HEPATICUS; INNATE IMMUNITY; INTESTINE FLORA; IONIZING RADIATION; LINEAR ENERGY TRANSFER; MALE; MOUSE; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; PROTON RADIATION; RADIATION CARCINOGENESIS; RADIATION ENERGY; RADIATION EXPOSURE; RADIATION INJURY; WHOLE BODY RADIATION;

ANIMALS; CHROMOSOME ABERRATIONS; DNA BREAKS, DOUBLE-STRANDED; ENDPOINT DETERMINATION; EXTRATERRESTRIAL ENVIRONMENT; FECES; FEMALE; INTESTINES; LINEAR ENERGY TRANSFER; MALE; MICE; MICROBIOTA; MUTAGENICITY TESTS; OXIDATIVE STRESS; PROTONS; T-LYMPHOCYTES;

EID: 84893702319     PISSN: 00337587     EISSN: 19385404     Source Type: Journal    
DOI: 10.1667/RR13352.1     Document Type: Article

References (62)

1. Durante M, Cucinotta FA. Heavy ion carcinogenesis and human space exploration. Nat Rev Cancer 2008; 8:465-72.
2. Cucinotta FA, Schimmerling W, Wilson JW, Peterson LE, Saganti PB, Dicello JF. Uncertainities in estimates of the risks of late effects from space radiation. Adv Space Res 2004; 34:1383-9.
3. Durante M, George K, Wu H, Cucinotta FA. Karyotypes of human lymphocytes exposed to high-energy iron ions. Radiat Res 2002; 158:581-90.
4. Desai N, Davis E, O'Neill P, Durante M, Cucinotta FA, Wu H. Immunofluorescence detection of clustered gamma-H2AX foci induced by HZE-particle radiation. Radiat Res 2005; 164:518-22.
5. Rithidech KN, Honikel L, Whorton EB. mFish analysis of chromosomal damage in bone marrow cells collected from CBA/CaJ mice following whole body exposure to heavy ions (56Fe ions). Radiat Environ Biophys 2007; 46:137-45.
6. Asaithamby A, Uematsu N, Chatterjee A, Story, MD, Burma S, Chen DJ. Repair of HZE-particle-induced DNA double-strand breaks in normal human fibroblasts. Radiat Res 2008; 169:437-46.
7. Gridley DS, Pecaut MJ, Green LM, Sanchez MC, Kadhim MA. Strain-related differences and radiation quality effects on mouse leukocytes: gamma-rays and protons (with and without aluminum shielding). In Vivo 2011; 25:871-80.
8. Durante M, George K, Cucinotta FA. Chromosomes lacking telomeres are present in the progeny of human lymphocytes exposed to heavy ions. Radiat Res 2006; 165:51-58.
9. Trovati S, Ballarini F, Battistoni G, Cerutti F, Fasso A, Ferrari A, et al. Human exposure to space radiation: role of primary and secondary particles. Radiat Prot Dosimetry 2006; 122:362-66.
10. Yang H, Magpayo N, Rusek A, Chiang IH, Sivertz M, Held KD. Effects of very low fluences of high-energy protons or iron ions on irradiated and bystander cells. Radiat Res 2011; 176:695-705.
11. Sutherland BM, Cuomo NC, Bennett PV. Induction of anchorageindependent growth in primary human cells exposed to protons or HZE ions separately or in dual exposures. Radiat Res 2005; 164:493-6.
12. Stisova V, Abele WH, Thompson KH, Bennett PV, Sutherland BM. Response of primary human fibroblasts exposed to solar particle event protons. Radiat Res 2011; 176:217-25.
13. Evans MD, Dizdaroglu M, Cooke MS. Oxidative DNA damage and disease: induction, repair and significance. Mutat Res 2004; 567:1-61.
14. Jang JH, Surh YJ. Bcl-2 attenuation of oxidative cell death is associated with up-regulation of gamma-glutamylcysteine ligase via constitutive NF-kappaB activation. J Biol Chem 2004; 279:38779-86.
15. Rugo RE, Schiestl RH. Increases in oxidative stress in the progeny of X-irradiated cells. Radiat Res 2004; 162:416-25.
16. Ballatori N, Krance SM, Notenboom S, Shi S, Tieu K, Hammond CL. Glutathione dysregulation and the etiology and progression of human diseases. Biol Chem 2009; 390:191-214.
17. Boisio ML, Merlo F, Martines H, Esposito M. Blood levels of reduced and oxidized glutathione in malignant and non-malignant human colorectal lesions. Eur J Cancer 1990; 26:89-91.
18. Andarawewa KL, Erickson AC, Chou WS, Costes SV, Gascard P, Mott JD, et al. Ionizing radiation predisposes nonmalignant human mammary epithelial cells to undergo transforming growth factor beta induced epithelial to mesenchymal transition. Cancer Res 2007; 67:8662-70.
19. Nougayrede JP, Homburg S, Taieb F, Boury M, Brzuszkiewicz E, Gottschalk G, et al. Escherichia coli induces DNA double-strand breaks in eukaryotic cells. Science 2006; 313:848-51.
20. Mazmanian SK, Liu CH, Tzianabos AO, Kasper DL. An immunomodulatory molecule of symbiotic bacteria directs maturation of the host immune system. Cell 2005; 122:107-18.
21. Feng T, Wang L, Schoeb TR, Elson CO, Cong Y. Microbiota innate stimulation is a prerequisite for T cell spontaneous proliferation and induction of experimental colitis. J Exp Med 2010; 207:1321-32.
22. Lavelle EC, Murphy C, O'Neill LA, Creagh EM. The role of TLRs, NLRs, and RLRs in mucosal innate immunity and homeostasis. Mucosal Immunol 2010; 3:17-28.
23. Kastenbauer S, Ziegler-Heitbrock HW. NF-kappaB1 (p50) is upregulated in lipopolysaccharide tolerance and can block tumor necrosis factor gene expression. Infect Immun 1999; 67:1553-9.
24. Fink LN, Metzdorff SB, Zeuthen LH, Nellemann C, Kristensen MB, Licht TR, et al. Establishment of tolerance to commensal bacteria requires a complex microbiota and is accompanied by decreased intestinal chemokine expression. Am J Physiol Gastrointest Liver Physiol 2012; 302:G55-G65.
25. McKernan DP, Gaszner G, Quigley EM, Cryan JF, Dinan TG. Altered peripheral toll-like receptor responses in the irritable bowel syndrome. Aliment Pharmacol Ther 2011; 33:1045-52.
26. Chung H, Kasper DL. Microbiota-stimulated immune mechanisms to maintain gut homeostasis. Curr Opin Immunol 2010; 22:455-60.
27. Ye J, Lee JW, Presley LL, Bent E, Wei B, Braun J, et al. Bacteria and bacterial rRNA genes associated with the development of colitis in IL-10(-/-) mice. Inflamm Bowel Dis 2008; 14:1041-50.
28. Berry D, Schwab C, Milinovich G, Reichert J, Ben Mahfoudh K, Decker T, et al. Phylotype-level 16S rRNA analysis reveals new bacteria indicators of health state in acute murine colitis. Isme J 2012; 6:2091-106.
29. Klaunig JE, Kamendulis LM, Hocevar BA. Oxidative stress and oxidative damage in carcinogenesis. Toxicol Pathol 2010; 38:96-109.
30. Sanchez-Vargas FM, Abu-El-Haija MA, Gomez-Duarte OG. Salmonella infections: An update on epidemiology management, and prevention. Travel Med Infect Dis 2011; 9:263-77.
31. Fujiwara D, Wei B, Presley LL, Brewer S, McPherson M, Lewinski MA, et al. Systemic control of plasmacytoid dendritic cells by CD8\+ T cells and commensal bacteria. J Immunol 2008; 180:5843-52.
32. Wingender G, Stepniak D, Krebs P, Lin L, McBride S, Wei B, et al. Intestinal microbes affect phenotypes and functions of invariant natural killer T cells in mice. Gastroenterology 2012; 143:418-28.
33. Brigl M, Tatituri RV, Watts GF, Bhowruth V, Leadbetter EA, Barton N, et al. Innate and cytokine-driven signals, rather than microbial antigens, dominate in natural killer T cell activation during microbial infection. J Exp Med 2011; 208:1163-77.
34. Presley LL, Wei B, Braun J, Borneman J. Bacteria associated with immunoregulatory cells in mice. Appl Environ Microbiol 2010; 76:936-41.
35. Chu FF, Esworthy RS, Chu PG, Longmate JA, Huycke MM, Wilczynski S, et al. Bacteria-induced intestinal cancer in mice with disrupted Gpx1 and Gpx2 genes. Cancer Res 2004; 64:962-8.
36. Lam V, Moulder JE, Salzman NH, Dubinsky EA, Andersen GL, Baker JE. Intestinal microbiota as novel biomarkers of prior radiation exposure. Radiat Res 2012; 177:573-83.
37. Rakoff-Nahoum S, Paglino J, Eslami-Varzaneh F, Edberg S, Medzhintov R. Recognition of commensal microflora by toll-like receptors is required for intestinal homeostasis. Cell 2004; 118:229-41.
38. Westbrook AM, Wei B, Braun J, Schiestl RH. Intestinal mucosal inflammation leads to systemic genotoxicity in mice. Cancer Res 2009; 69:4827-34.
39. Olive PL, Banath JP. The comet assay: a method to measure DNA damage in individual cells. Nat Protoc 2006; 1:23-9.
40. Muslimovic A, Ismail IH, Gao Y, Hammarsten O. An optimized method for measurement of gamma-H2AX in blood mononuclear and cultured cells. Nat Protoc 2008; 3:1187-93.
41. Griffiths RI, Whiteley AS, O'Donnell AG, Bailey MJ. Rapid method for coextraction of DNA and RNA from natural environments for analysis of ribosomal DNA-and rRNA-based microbial community composition. Appl Environ Microbiol 2000; 66:5488-91.
42. Berry D, Ben Mahfoudh K, Wagner M, Loy A. Barcoded primers used in multiplex amplicon pyrosequencing bias amplification. Appl Environ Microbiol 2011; 77:7846-9.
43. Schloss PD, Gevers D, Westcott SL. Reducing the effects of PCR amplification and sequencing artifacts on 16S rRNA-based studies. PLoS One 2011; 6:e27310.
44. Edgar RC. Search and clustering orders of magnitude faster than BLAST. Bioinformatics 2010; 26:2460-1.
45. Haas BJ, Gevers D, Earl AM, Feldgarden M, Ward DV, Giannoukos, G, et al. Chimeric 16S rRNA sequence formation and detection in Sanger and 454-pyrosequenced PCR amplicons. Genome Res 2011; 21:494-504.
46. Wang Q, Garrity GM, Tiedje JM, Cole J.R. Na?̈ve Bayesian classifier for rapid assignment of rRNA sequences into the new bacterial taxonomy. Appl Environ Microbiol 2007; 73:5261-7.
47. Caporaso JG, Kuczynski J, Stombaugh J, Bittinger K, Bushman FD, Costello EK, et al. QIIME allows analysis of high-throughput community sequencing data. Nat Methods 2010; 7:335-6.
48. McHardy IH, Goudarzi M, Tong M, Ruegger PM, Schwager E, Weger JR, et al. Integrative analysis of the microbiome and metabolome of the human intestinal mucosal surface reveals exquisite inter-relationships. Microbiome 1:17.
49. Ng SC, Benjamin JL, McCarthy NE, Hedin CR, Koutsoumpas A, Plamondon S, et al. Relationship between human intestinal denritic cells, gut microbiota, and disease activity in Crohn's disease. Inflamm Bowel Dis 2011; 17:2027-37.
50. Horstmann M, Durante M, Johannes C, Pieper R, Obe G. Space radiation does not induce a significant increase of intrachromosomal exchanges in astronauts' lymphocytes. Radiat Environ Biophys 2005; 44:219-24.
51. Durante M. Biomarkers of space radiation risk. Radiat Res 2005; 164:467-73.
52. Green LM, Murray DK, Bant AM, Kazarians G, Moyers MF, Nelson GA, et al. Response of thyroid follicular cells to gamma irradiation compared to proton irradiation. I. Initial characterization of DNA damage, micronucleus formation, apoptosis, cell survival, and cell cycle phase redistribution. Radiat Res 2001; 155:32-42.
53. Tariq MA, Soedipe A, Ramesh G, Wu H, Zhang Y, Shishodia S, et al. The effect of acute dose charge particle radiation on expression of DNA repair genes in mice. Mol Cell Biochem 2011; 349:213-8.
54. Goto S, Watanabe M, Yatagai F. Delayed cell cycle progression in human lymphoblastoid cells after exposure to high-LET radiation correlates with extremely localized DNA damage. Radiat Res 2002; 158:678-86.
55. Liu IF, Annamalai T, Sutherland JH, Tse-Dinh YC. Hydroxyl radicals are involved in cell killing by the bacterial topoisomerase I cleavage complex. J Bacteriol 2009; 191:5315-9.
56. Wei B, Wingender G, Fujiwara D, Chen DY, McPherson M, Brewer S, et al. Commensal microbiota and CD8\+ T cells shape the formation of invariant NKT cells. J Immunol 2010; 184:1218-26.
57. Clarke TB, Davis KM, Lysenko ES, Zhou AY, Yu Y, Weiser JN. Recognition of peptidoglycan from the microbiota by Nod1 enhances systemic innate immunity. Nat Med 2010; 16:228-31.
58. Biswas A, Petnicki-Ocwieja T, Kobayashi KS. Nod2: a key regulator linking microbiota to intestinal mucosal immunity. J Mol Med (Berl) 2012; 90:15-24.
59. Benlloch M, Ortega A, Ferrer P, Segarra R, Obrador E, Asensi M, et al. Acceleration of glutathione efflux of gamma-glutamyltranspeptidase sensitize metastatic B16 melanoma cells to endotheliuminduced cytotoxicity. J Biol Chem 2005; 280:6950-9.
60. Sido B, Hack V, Hochlehnert A, Lipps H, Herfarth C, Droge W. Impairment of intestinal glutathione synthesis in patients with inflammatory bowel disease. Gut 1998; 42:485-92.
61. Round JL, Lee SM, Li J, Tran G, Jabri B, Chatila TA, et al. The toll-like receptor 2 pathway establishes colonization by a commensal of the human microbiota. Science 2011; 332:974-7.
62. Sekelja M, Berget I, Naes T, Rudi K. Unveiling an abundant core microbiota in the human adult colon by a phylogroup-independent searching approach. Isme J 2011; 5:519-31.