Chemopreventive Metabolites Are Correlated with a Change in Intestinal Microbiota Measured in A-T Mice and Decreased Carcinogenesis

PLoS ONE

Volumn 11, Issue 4, 2016, Pages

  Cheema, Amrita K ^a   Maier, Irene ^b   Dowdy, Tyrone ^a   Wang, Yiwen ^a   Singh, Rajbir ^a   Ruegger, Paul M ^c   Borneman, James ^c   Fornace, Albert J ^a   Schiestl, Robert H ^b,d  

^a GEORGETOWN UNIVERSITY MEDICAL CENTER   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c UNIVERSITY OF CALIFORNIA   (United States)

^d UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

3 METHYLADENINE; 3 METHYLBUTYROLACTONE; ANTINEOPLASTIC AGENT; DRUG METABOLITE; KYNEURENIC ACID; UNCLASSIFIED DRUG; 3-METHYLADENINE; 3-METHYLBUTYROLACTONE; ADENINE; GAMMA BUTYROLACTONE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTINEOPLASTIC ACTIVITY; ARTICLE; ATAXIA TELANGIECTASIA; CANCER PREVENTION; CARCINOGENESIS; CONTROLLED STUDY; DRUG DETERMINATION; DRUG EFFECT; DRUG MECHANISM; DRUG RESPONSE; FECES ANALYSIS; INTESTINE FLORA; MALE; MALIGNANT NEOPLASTIC DISEASE; MASS SPECTROMETRY; METABOLOMICS; MOUSE; NONHUMAN; PHENOTYPE; SPECIES COMPOSITION; URINALYSIS; ANALOGS AND DERIVATIVES; ANIMAL; CELL TRANSFORMATION; INTESTINE TUMOR; KNOCKOUT MOUSE; METABOLISM;

4-BUTYROLACTONE; ADENINE; ANIMALS; CELL TRANSFORMATION, NEOPLASTIC; GASTROINTESTINAL MICROBIOME; INTESTINAL NEOPLASMS; MICE; MICE, KNOCKOUT;

EID: 84963864991     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0151190     Document Type: Article

References (69)

1. Meyn MS. Ataxia-telangiectasia, cancer and the pathobiology of the ATM gene. Clin Genet. 1999; 55 (5):289-304. Epub 1999/07/28. PMID: 10422797.
2. Peterson RD, Funkhouser JD, Tuck-Muller CM, Gatti RA. Cancer susceptibility in ataxia-telangiectasia. Leukemia. 1992; 6 Suppl 1:8-13. PMID: 1548942.
3. Hecht F, Hecht BK. Cancer in ataxia-telangiectasia patients. Cancer Genet Cytogenet. 1990; 46(1):9-19. PMID: 2184934.
4. Morrell D, Cromartie E, Swift M. Mortality and cancer incidence in 263 patients with ataxia-telangiectasia. J Natl Cancer Inst. 1986; 77(1):89-92. PMID: 3459930
5. Sandoval C, Swift M. Treatment of lymphoid malignancies in patients with ataxia-telangiectasia. Med Pediatr Oncol. 1998; 31(6):491-7. PMID: 9835901.
6. Taylor AM, Metcalfe JA, Thick J, Mak YF. Leukemia and lymphoma in ataxia telangiectasia. Blood. 1996; 87(2):423-38. PMID: 8555463.
7. Boder E. Ataxia-telangiectasia: Some historic, clinical and pathologic observations. Birth Defects Orig Artic Ser. 1975; 11(1):255-70. PMID: 1096982.
8. Crawford TO, Skolasky RL, Fernandez R, Rosquist KJ, Lederman HM. Survival probability in ataxia telangiectasia. Arch Dis Child. 2006; 91(7):610-1. PMID: 16790721.
9. Gatti RA, Becker-Catania S, Chun HH, Sun X, Mitui M, Lai CH, et al. The pathogenesis of ataxia-telangiectasia. Learning from a Rosetta Stone. Clin Rev Allergy Immunol. 2001; 20(1):87-108. Epub 2001/03/28. CRIAI:20:1:87 [pii] doi: 10.1385/CRIAI:20:1:87 PMID: 11269230.
10. Lim DS, Kim ST, Xu B, Maser RS, Lin J, Petrini JH, et al. ATM phosphorylates p95/nbs1 in an S-phase checkpoint pathway. Nature. 2000; 404(6778):613-7. doi: 10.1038/35007091 PMID: 10766245.
11. Bakkenist CJ, Kastan MB. DNA damage activates ATM through intermolecular autophosphorylation and dimer dissociation. Nature. 2003; 421(6922):499-506. doi: 10.1038/nature01368 PMID: 12556884.
12. Barlow C, Hirotsune S, Paylor R, Liyanage M, Eckhaus M, Collins F, et al. Atm-deficient mice: A paradigm of ataxia telangiectasia. Cell. 1996; 86(1):159-71. PMID: 8689683.
13. Elson A, Wang Y, Daugherty CJ, Morton CC, Zhou F, Campos-Torres J, et al. Pleiotropic defects in ataxia-telangiectasia protein-deficient mice. Proc Natl Acad Sci U S A. 1996; 93(23):13084-9. PMID: 8917548
14. Xu Y, Ashley T, Brainerd EE, Bronson RT, Meyn MS, Baltimore D. Targeted disruption of ATM leads to growth retardation, chromosomal fragmentation during meiosis, immune defects, and thymic lymphoma. Genes Dev. 1996; 10(19):2411-22. Epub 1996/10/01. PMID: 8843194.
15. Xu Y, Baltimore D. Dual roles of ATM in the cellular response to radiation and in cell growth control. Genes Dev. 1996; 10(19):2401-10. Epub 1996/10/01. PMID: 8843193.
16. Liyanage M, Weaver Z, Barlow C, Coleman A, Pankratz DG, Anderson S, et al. Abnormal rearrangement within the alpha/delta T-cell receptor locus in lymphomas from Atm-deficient mice. Blood. 2000; 96(5):1940-6. Epub 2000/08/29. PMID: 10961898.
17. Borghesani PR, Alt FW, Bottaro A, Davidson L, Aksoy S, Rathbun GA, et al. Abnormal development of Purkinje cells and lymphocytes in Atm mutant mice. Proc Natl Acad Sci U S A. 2000; 97(7):3336-41. PMID: 10716718.
18. Petiniot LK, Weaver Z, Vacchio M, Shen R, Wangsa D, Barlow C, et al. RAG-mediated V(D)J recombination is not essential for tumorigenesis in Atm-deficient mice. Mol Cell Biol. 2002; 22(9):3174-7. PMID: 11940674.
19. Reliene R, Schiestl RH. Antioxidant N-acetyl cysteine reduces incidence and multiplicity of lymphoma in Atm deficient mice. DNA Repair (Amst). 2006; 5(7):852-9. Epub 2006/06/20. S1568-7864(06) 00120-0 [pii] doi: 10.1016/j.dnarep.2006.05.003 PMID: 16781197.
20. Schubert R, Erker L, Barlow C, Yakushiji H, Larson D, Russo A, et al. Cancer chemoprevention by the antioxidant tempol in Atm-deficient mice. Hum Mol Genet. 2004; 13(16):1793-802. Epub 2004/06/24. doi: 10.1093/hmg/ddh189 ddh189 [pii]. PMID: 15213104.
21. Yamamoto ML, Maier I, Dang AT, Berry D, Liu J, Ruegger PM, et al. Intestinal bacteria modify lymphoma incidence and latency by affecting systemic inflammatory state, oxidative stress, and leukocyte genotoxicity. Cancer Res. 2013; 73(14):4222-32. Epub 2013/07/19. doi: 10.1158/0008-5472.CAN-13-0022 PMID: 23860718; PubMed Central PMCID: PMC3718495.
22. Maier I, Berry DM, Schiestl RH. Intestinal microbiota reduces genotoxic endpoints induced by highenergy protons. Radiation research. 2014; 181(1):45-53. doi: 10.1667/RR13352.1 PMID: 24397477.
23. 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 microbiota. J Immunol. 2008; 180(9):5843-52. Epub 2008/04/22. 180/9/5843 [pii]. PMID: 18424703.
24. Westbrook AM, Wei B, Braun J, Schiestl RH. Intestinal mucosal inflammation leads to systemic genotoxicity in mice. Cancer research. 2009; 69(11):4827-34. Epub 2009/06/03. 69/11/4827 [pii] doi: 10. 1158/0008-5472.CAN-08-4416 PMID: 19487293; PubMed Central PMCID: PMC2709766.
25. Zitvogel L, Galluzzi L, Viaud S, Vetizou M, Daillere R, Merad M, et al. Cancer and the gut microbiota: An unexpected link. Sci Transl Med. 2015; 7(271):271ps1. doi: 10.1126/scitranslmed.3010473 PMID: 25609166.
26. Cani PD, Delzenne NM. The role of the gut microbiota in energy metabolism and metabolic disease. Curr Pharm Des. 2009; 15(13):1546-58. PMID: 19442172.
27. Delzenne NM, Neyrinck AM, Cani PD. Gut microbiota and metabolic disorders: How prebiotic can work? Br J Nutr. 2013; 109 Suppl 2:S81-5. doi: 10.1017/S0007114512004047 PMID: 23360884.
28. Bowling FG, Thomas M. Analyzing the metabolome. Methods in molecular biology. 2014; 1168:31-45. doi: 10.1007/978-1-4939-0847-9-3 PMID: 24870129.
29. Blow N. Metabolomics: Biochemistry's new look. Nature. 2008; 455(7213):697-700. doi: 10.1038/455697a PMID: 18833281.
30. Xie G, Zhang S, Zheng X, Jia W. Metabolomics approaches for characterizing metabolic interactions between host and its commensal microbes. Electrophoresis. 2013; 34(19):2787-98. doi: 10.1002/elps. 201300017 PMID: 23775228.
31. Clavel T, Desmarchelier C, Haller D, Gerard P, Rohn S, Lepage P, et al. Intestinal microbiota in metabolic diseases: From bacterial community structure and functions to species of pathophysiological relevance. Gut microbes. 2014; 5(4). PMID: 25003516.
32. Swann JR, Claus SP. Nutrimetabonomics: Nutritional applications of metabolic profiling. Science progress. 2014; 97(Pt 1):41-7. PMID: 24800468.
33. Ursell LK, Haiser HJ, Van TreurenW, Garg N, Reddivari L, Vanamala J, et al. The intestinal metabolome: An intersection between microbiota and host. Gastroenterology. 2014; 146(6):1470-6. doi: 10. 1053/j.gastro.2014.03.001 PMID: 24631493.
34. Cheema AK, Timofeeva O, Varghese R, Dimtchev A, Shiekh K, Shulaev V, et al. Integrated analysis of ATM mediated gene and protein expression impacting cellular metabolism. Journal of proteome research. 2011; 10(5):2651-7. doi: 10.1021/pr101243j PMID: 21322649.
35. Schwabe RF, Jobin C. The microbiome and cancer. Nature reviews Cancer. 2013; 13(11):800-12. Epub 2013/10/18. doi: 10.1038/nrc3610 PMID: 24132111.
36. Rakoff-Nahoum S, Paglino J, Eslami-Varzaneh F, Edberg S, Medzhitov R. Recognition of commensal microflora by toll-like receptors is required for intestinal homeostasis. Cell. 2004; 118(2):229-41. Epub 2004/07/21. doi: 10.1016/j.cell.2004.07.002 S0092867404006610 [pii]. PMID: 15260992.
37. Presley LL, Wei B, Braun J, Borneman J. Bacteria associated with immunoregulatory cells in mice. Appl Environ Microbiol. 2010; 76(3):936-41. Epub 2009/12/17. AEM.01561-09 [pii] doi: 10.1128/AEM. 01561-09 PMID: 20008175; PubMed Central PMCID: PMC2813032.
38. Ruegger PM, Clark RT, Weger JR, Braun J, Borneman J. Improved resolution of bacteria by high throughput sequence analysis of the rRNA internal transcribed spacer. Journal ofmicrobiologicalmethods. 2014; 105:82-7. doi: 10.1016/j.mimet.2014.07.001 PMID: 25034229; PubMed Central PMCID: PMC4160368.
39. Kaur P, Rizk N, Ibrahim S, Luo Y, Younes N, Perry B, et al. Quantitative metabolomic and lipidomic profiling reveals aberrant amino acid metabolism in type 2 diabetes. Molecular bioSystems. 2013; 9 (2):307-17. doi: 10.1039/c2mb25384d PMID: 23247761.
40. Varghese RS, Cheema A, Cheema P, Bourbeau M, Tuli L, Zhou B, et al. Analysis of LC-MS data for characterizing the metabolic changes in response to radiation. Journal of proteome research. 9 (5):2786-93. Epub 2010/03/25. doi: 10.1021/pr100185b PMID: 20329776.
41. Want EJ, Wilson ID, Gika H, Theodoridis G, Plumb RS, Shockcor J, et al. Global metabolic profiling procedures for urine using UPLC-MS. Nat Protoc. 2010; 5(6):1005-18. doi: 10.1038/nprot.2010.50 PMID: 20448546.
42. Smith CA, Want EJ, O'Maille G, Abagyan R, Siuzdak G. XCMS: Processing mass spectrometry data for metabolite profiling using nonlinear peak alignment, matching, and identification. Anal Chem. 2006; 78 (3):779-87. Epub 2006/02/02. doi: 10.1021/ac051437y PMID: 16448051.
43. Xia J, Mandal R, Sinelnikov IV, Broadhurst D, Wishart DS. MetaboAnalyst 2.0-a comprehensive server for metabolomic data analysis. Nucleic acids research. 2012; 40(Web Server issue):W127-33. Epub 2012/05/04. gks374 [pii] doi: 10.1093/nar/gks374 PMID: 22553367; PubMed Central PMCID: PMC3394314.
44. Storey JD. A direct approach to false discovery rates. Journal of the Royal Statistical Society: Series B (Statistical Methodology). 2002; 64(3):479-98.
45. Patterson AD, Li H, Eichler GS, Krausz KW, Weinstein JN, Fornace AJ Jr, et al. UPLC-ESI-TOFMSbased metabolomics and gene expression dynamics inspector self-organizing metabolomic maps as tools for understanding the cellular response to ionizing radiation. Anal Chem. 2008; 80(3):665-74. doi: 10.1021/ac701807v PMID: 18173289; PubMed Central PMCID: PMC2254319.
46. Ciappio ED, KrauszKW, Rochman M, Furusawa T, Bonzo JA, Tessarollo L, et al. Metabolomics Reveals a Role for the Chromatin-Binding Protein HMGN5 in Glutathione Metabolism. PLoS One. 2014; 9(1): E84583. doi: 10.1371/journal.pone.0084583 PMID: 24392144; PubMed Central PMCID: PMC3879345.
47. Cheema AK, Suman S, Kaur P, Singh R, Fornace AJ Jr, Datta K. Long-Term Differential Changes in Mouse Intestinal Metabolomics after gamma and Heavy Ion Radiation Exposure. PLoS One. 2014; 9(1): E87079. doi: 10.1371/journal.pone.0087079 PMID: 24475228; PubMed Central PMCID: PMC3903607.
48. Tyburski JB, Patterson AD, Krausz KW, Slavik J, Fornace AJ Jr, Gonzalez FJ, et al. Radiation metabolomics. 2. Dose-and time-dependent urinary excretion of deaminated purines and pyrimidines after sublethal gamma-radiation exposure in mice. Radiation research. 2009; 172(1):42-57. Epub 2009/07/08 doi: 10.1667/RR1703.1 PMID: 19580506; PubMed Central PMCID: PMC2794378.
49. Zhou B, Wang J, Ressom HW. MetaboSearch: Tool for mass-based metabolite identification using multiple databases. PLoS One. 7(6):e40096. Epub 2012/07/07. doi: 10.1371/journal.pone.0040096 PONE-D-12-06701 [pii]. PMID: 22768229; PubMed Central PMCID: PMC3387018.
50. Huang T, Wei B, Velazquez P, Borneman J, Braun J. Commensal microbiota alter the abundance and TCR responsiveness of splenic naive CD4+ T lymphocytes. Clin Immunol. 2005; 117(3):221-30. Epub 2005/11/18. S1521-6616(05)00337-2 [pii] doi: 10.1016/j.clim.2005.09.012 PMID: 16290233.
51. Wei B, Su TT, Dalwadi H, Stephan RP, Fujiwara D, Huang TT, et al. Resident enteric microbiota and CD8+ T cells shape the abundance of marginal zone B cells. Eur J Immunol. 2008; 38(12):3411-25. Epub 2008/11/15. doi: 10.1002/eji.200838432 PMID: 19009526; PubMed Central PMCID: PMC2734463.
52. Johnson RK, Inouye T, Goldin A, Stark GR. Antitumor activity of N-(phosphonacetyl)-L-aspartic acid, a transition-state inhibitor of aspartate transcarbamylase. Cancer Res. 1976; 36(8):2720-5. PMID: 1064466.
53. Walczak K, Turski WA, Rzeski W. Kynurenic acid enhances expression of p21 Waf1/Cip1 in colon cancer HT-29 cells. Pharmacological reports: PR. 2012; 64(3):745-50. PMID: 22814028.
54. Guo Z, Kozlov S, Lavin MF, Person MD, Paull TT. ATM activation by oxidative stress. Science. 2010; 330(6003):517-21. Epub 2010/10/23. 330/6003/517 [pii] doi: 10.1126/science.1192912 PMID: 20966255.
55. Iida N, Dzutsev A, Stewart CA, Smith L, Bouladoux N, Weingarten RA, et al. Commensal bacteria control cancer response to therapy by modulating the tumor microenvironment. Science. 2013; 342 (6161):967-70. Epub 2013/11/23. doi: 10.1126/science.1240527 PMID: 24264989.
56. Viaud S, Saccheri F, Mignot G, Yamazaki T, Daillere R, Hannani D, et al. The intestinal microbiota modulates the anticancer immune effects of cyclophosphamide. Science. 2013; 342(6161):971-6. Epub 2013/11/23. doi: 10.1126/science.1240537 PMID: 24264990.
57. Kingma SD, Li N, Sun F, Valladares RB, Neu J, Lorca GL. Lactobacillus johnsonii N6.2 stimulates the innate immune response through Toll-like receptor 9 in Caco-2 cells and increases intestinal crypt Paneth cell number in biobreeding diabetes-prone rats. The Journal of nutrition. 2011; 141(6):1023-8. Epub 2011/04/15. doi: 10.3945/jn.110.135517 jn.110.135517 [pii]. PMID: 21490291.
58. Adlercreutz H, Bannwart C, Wahala K, Makela T, Brunow G, Hase T, et al. Inhibition of human aromatase by mammalian lignans and isoflavonoid phytoestrogens. J Steroid Biochem Mol Biol. 1993; 44 (2):147-53. PMID: 8382517.
59. Yang N, Kays JS, Skillman TR, Burris L, Seng TW, Hammond C. C75 [4-methylene-2-octyl-5-oxo-tetrahydro-furan-3-carboxylic acid] activates carnitine palmitoyltransferase-1 in isolated mitochondria and intact cells without displacement of bound malonyl CoA. The Journal of pharmacology and experimental therapeutics. 2005; 312(1):127-33. doi: 10.1124/jpet.104.074104 PMID: 15356215.
60. Kim JC, Kim SH, Kim JA, Choi SK, Park WW. Potential antitumor alpha-methylene-gamma-butyrolactone-bearing nucleic acid base. 3. Synthesis of 5'-methyl-5'-[(6-substituted-9H-purin-9-yl)methyl]-2'-oxo-3'-methylenetetrahydrofurans. Archives of Pharmacal Research. 1997; Volume 20(3):253-8.
61. Wu YT, Tan HL, Shui G, Bauvy C, Huang Q, Wenk MR, et al. Dual role of 3-methyladenine in modulation of autophagy via different temporal patterns of inhibition on class I and III phosphoinositide 3-kinase. J Biol Chem. 2010; 285(14):10850-61. doi: 10.1074/jbc.M109.080796 PMID: 20123989; PubMed Central PMCID: PMC2856291.
62. Heckmann BL, Yang X, Zhang X, Liu J. The autophagic inhibitor 3-methyladenine potently stimulates PKA-dependent lipolysis in adipocytes. British journal of pharmacology. 2013; 168(1):163-71. doi: 10. 1111/j.1476-5381.2012.02110.x PMID: 22817685; PubMed Central PMCID: PMC3570012.
63. Tran AT, Ramalinga M, Kedir H, Clarke R, Kumar D. Autophagy inhibitor 3-methyladenine potentiates apoptosis induced by dietary tocotrienols in breast cancer cells. European journal of nutrition. 2015; 54 (2):265-72. doi: 10.1007/s00394-014-0707-y PMID: 24830781; PubMed Central PMCID: PMC4233202.
64. Tan S, Peng X, Peng W, Zhao Y, Wei Y. Enhancement of oxaliplatin-induced cell apoptosis and tumor suppression by 3-methyladenine in colon cancer. Oncol Lett. 2015; 9(5):2056-62. doi: 10.3892/ol. 2015.2996 PMID: 26137012; PubMed Central PMCID: PMCPMC4467296.
65. Wang J, Simonavicius N, Wu X, Swaminath G, Reagan J, Tian H, et al. Kynurenic acid as a ligand for orphan G protein-coupled receptor GPR35. J Biol Chem. 2006; 281(31):22021-8. Epub 2006/06/07. M603503200 [pii] doi: 10.1074/jbc.M603503200 PMID: 16754668.
66. DiNatale BC, Murray IA, Schroeder JC, Flaveny CA, Lahoti TS, Laurenzana EM, et al. Kynurenic acid is a potent endogenous aryl hydrocarbon receptor ligand that synergistically induces interleukin-6 in the presence of inflammatory signaling. Toxicological sciences: An official journal of the Society of Toxicology. 2010; 115(1):89-97. doi: 10.1093/toxsci/kfq024 PMID: 20106948; PubMed Central PMCID: PMC2855350.
67. Urenjak J, Obrenovitch TP. Neuroprotective potency of kynurenic acid against excitotoxicity. Neuroreport. 2000; 11(6):1341-4. PMID: 10817618.
68. Li H, Jogl G. Structural and biochemical studies of TIGAR (TP53-induced glycolysis and apoptosis regulator). J Biol Chem. 2009; 284(3):1748-54. doi: 10.1074/jbc.M807821200 PMID: 19015259; PubMed Central PMCID: PMCPMC2615519.
69. Altschul SF, Madden TL, Schaffer AA, Zhang J, Zhang Z, Miller W, et al. Gapped BLAST and PSIBLAST: a new generation of protein database search programs. Nucleic acids research. 1997; 25 (17):3389-402. PMID: 9254694; PubMed Central PMCID: PMC146917.