Host-Microbe Co-metabolism Dictates Cancer Drug Efficacy in C. elegans

Cell

Volumn 169, Issue 3, 2017, Pages 442-456.e18

  Scott, Timothy A ^a   Quintaneiro, Leonor M ^a,b   Norvaisas, Povilas ^a   Lui, Prudence P ^a   Wilson, Matthew P ^b   Leung, Kit Yi ^b   Herrera Dominguez, Lucia ^c   Sudiwala, Sonia ^b   Pessia, Alberto ^d   Clayton, Peter T ^b   Bryson, Kevin ^a   Velagapudi, Vidya ^d   Mills, Philippa B ^b   Typas, Athanasios ^c   Greene, Nicholas D E ^b   Cabreiro, Filipe ^a  

^a UNIVERSITY COLLEGE LONDON   (United Kingdom)

^b UNIVERSITY COLLEGE LONDON   (United Kingdom)

^c EUROPEAN MOLECULAR BIOLOGY LABORATORY   (Germany)

^d UNIVERSITY OF HELSINKI   (Finland)

Author keywords

5 FU; autophagy; C. elegans; cancer; chemical genomics; co metabolism; E. coli; holobiont; Keio; nucleotide metabolism

Indexed keywords

ANTINEOPLASTIC AGENT; CAPECITABINE; DAMINOZIDE; DEOXYRIBONUCLEOTIDE; FLOXURIDINE; FLUCYTOSINE; FLUOROOROTIC ACID; FLUOROPYRIMIDINE DERIVATIVE; FLUOROURACIL; NUCLEOSIDE DIPHOSPHATE KINASE; PYRIDOXINE; GLYCOSYLTRANSFERASE; URACIL PHOSPHORIBOSYLTRANSFERASE;

ANTIPROLIFERATIVE ACTIVITY; ARTICLE; AUTOPHAGY; BACTERIAL METABOLISM; CAENORHABDITIS ELEGANS; CARBON METABOLISM; CELL DEATH; DRUG ACTIVATION; DRUG EFFECT; DRUG EFFICACY; DRUG MECHANISM; DRUG POTENCY; HIGH THROUGHPUT SCREENING; HOST; HOST CELL; HUMAN; IMMUNE RESPONSE; INTESTINE FLORA; NONHUMAN; PRIORITY JOURNAL; SURVIVAL; ANIMAL; ANIMAL MODEL; COLORECTAL NEOPLASMS; DIET; ENZYMOLOGY; ESCHERICHIA COLI; GENETICS; METABOLISM;

ANIMALS; ANTINEOPLASTIC AGENTS; AUTOPHAGY; CAENORHABDITIS ELEGANS; CELL DEATH; COLORECTAL NEOPLASMS; DIET; ESCHERICHIA COLI; FLUOROURACIL; GASTROINTESTINAL MICROBIOME; HUMANS; MODELS, ANIMAL; PENTOSYLTRANSFERASES;

EID: 85018528514     PISSN: 00928674     EISSN: 10974172     Source Type: Journal    
DOI: 10.1016/j.cell.2017.03.040     Document Type: Article

References (35)

1. Baba, T., Ara, T., Hasegawa, M., Takai, Y., Okumura, Y., Baba, M., Datsenko, K.A., Tomita, M., Wanner, B.L., Mori, H., Construction of Escherichia coli K-12 in-frame, single-gene knockout mutants: The Keio collection. Mol. Syst. Biol., 2, 2006 2006.0008.
2. Cabreiro, F., Metformin joins forces with microbes. Cell Host Microbe 19 (2016), 1–3.
3. Cabreiro, F., Au, C., Leung, K.Y., Vergara-Irigaray, N., Cochemé, H.M., Noori, T., Weinkove, D., Schuster, E., Greene, N.D., Gems, D., Metformin retards aging in C. elegans by altering microbial folate and methionine metabolism. Cell 153 (2013), 228–239.
4. Chen, W., Zhang, L., Zhang, K., Zhou, B., Kuo, M.L., Hu, S., Chen, L., Tang, M., Chen, Y.R., Yang, L., et al. Reciprocal regulation of autophagy and dNTP pools in human cancer cells. Autophagy 10 (2014), 1272–1284.
5. Chi, C., Ronai, D., Than, M.T., Walker, C.J., Sewell, A.K., Han, M., Nucleotide levels regulate germline proliferation through modulating GLP-1/Notch signaling in C. elegans. Genes Dev. 30 (2016), 307–320.
6. Degnan, P.H., Taga, M.E., Goodman, A.L., Vitamin B12 as a modulator of gut microbial ecology. Cell Metab. 20 (2014), 769–778.
7. Fitzpatrick, T.B., Amrhein, N., Kappes, B., Macheroux, P., Tews, I., Raschle, T., Two independent routes of de novo vitamin B6 biosynthesis: Not that different after all. Biochem. J. 407 (2007), 1–13.
8. Footitt, E.J., Clayton, P.T., Mills, K., Heales, S.J., Neergheen, V., Oppenheim, M., Mills, P.B., Measurement of plasma B6 vitamer profiles in children with inborn errors of vitamin B6 metabolism using an LC-MS/MS method. J. Inherit. Metab. Dis. 36 (2013), 139–145.
9. Garcia-Gonzalez, A.P., Ritter, A.D., Shrestha, S., Andersen, E.C., Yilmaz, L.S., Walhout, A.J.M., Bacterial metabolism affects the C. elegans response to cancer chemotherapeutics. Cell 169 (2017), 431–441 this issue.
10. Haiser, H.J., Gootenberg, D.B., Chatman, K., Sirasani, G., Balskus, E.P., Turnbaugh, P.J., Predicting and manipulating cardiac drug inactivation by the human gut bacterium Eggerthella lenta. Science 341 (2013), 295–298.
11. Iida, N., Dzutsev, A., Stewart, C.A., Smith, L., Bouladoux, N., Weingarten, R.A., Molina, D.A., Salcedo, R., Back, T., Cramer, S., et al. Commensal bacteria control cancer response to therapy by modulating the tumor microenvironment. Science 342 (2013), 967–970.
12. Kim, S., Park, D.H., Shim, J., Thymidylate synthase and dihydropyrimidine dehydrogenase levels are associated with response to 5-fluorouracil in Caenorhabditis elegans. Mol. Cells 26 (2008), 344–349.
13. Koyama, F., Sawada, H., Hirao, T., Fujii, H., Hamada, H., Nakano, H., Combined suicide gene therapy for human colon cancer cells using adenovirus-mediated transfer of escherichia coli cytosine deaminase gene and Escherichia coli uracil phosphoribosyltransferase gene with 5-fluorocytosine. Cancer Gene Ther. 7 (2000), 1015–1022.
14. Kwon, Y.K., Lu, W., Melamud, E., Khanam, N., Bognar, A., Rabinowitz, J.D., A domino effect in antifolate drug action in Escherichia coli. Nat. Chem. Biol. 4 (2008), 602–608.
15. Laourdakis, C.D., Merino, E.F., Neilson, A.P., Cassera, M.B., Comprehensive quantitative analysis of purines and pyrimidines in the human malaria parasite using ion-pairing ultra-performance liquid chromatography-mass spectrometry. J. Chromatogr. B Analyt. Technol. Biomed. Life Sci. 967 (2014), 127–133.
16. Locasale, J.W., Serine, glycine and one-carbon units: Cancer metabolism in full circle. Nat. Rev. Cancer 13 (2013), 572–583.
17. Longley, D.B., Harkin, D.P., Johnston, P.G., 5-fluorouracil: Mechanisms of action and clinical strategies. Nat. Rev. Cancer 3 (2003), 330–338.
18. Maslowska, K.H., Makiela-Dzbenska, K., Fijalkowska, I.J., Schaaper, R.M., Suppression of the E. coli SOS response by dNTP pool changes. Nucleic Acids Res. 43 (2015), 4109–4120.
19. Merry, A., Qiao, M., Hasler, M., Kuwabara, P.E., RAD-6: Pyrimidine synthesis and radiation sensitivity in Caenorhabditis elegans. Biochem. J. 458 (2014), 343–353.
20. Midgley, R., Kerr, D., Colorectal cancer. Lancet 353 (1999), 391–399.
21. Nichols, R.J., Sen, S., Choo, Y.J., Beltrao, P., Zietek, M., Chaba, R., Lee, S., Kazmierczak, K.M., Lee, K.J., Wong, A., et al. Phenotypic landscape of a bacterial cell. Cell 144 (2011), 143–156.
22. Nicholson, J.K., Holmes, E., Kinross, J., Burcelin, R., Gibson, G., Jia, W., Pettersson, S., Host-gut microbiota metabolic interactions. Science 336 (2012), 1262–1267.
23. Nikkanen, J., Forsström, S., Euro, L., Paetau, I., Kohnz, R.A., Wang, L., Chilov, D., Viinamäki, J., Roivainen, A., Marjamäki, P., et al. Mitochondrial DNA replication defects disturb cellular dNTP pools and remodel one-carbon metabolism. Cell Metab. 23 (2016), 635–648.
24. O'Donnell, P.H., Dolan, M.E., Cancer pharmacoethnicity: Ethnic differences in susceptibility to the effects of chemotherapy. Clin. Cancer Res. 15 (2009), 4806–4814.
25. Offer, S.M., Diasio, R.B., Is It Finally Time for a Personalized Medicine Approach for Fluorouracil-Based Therapies?. J. Clin. Oncol. 34 (2016), 205–207.
26. Okuda, H., Nishiyama, T., Ogura, K., Nagayama, S., Ikeda, K., Yamaguchi, S., Nakamura, Y., Kawaguchi, Y., Watabe, T., Lethal drug interactions of sorivudine, a new antiviral drug, with oral 5-fluorouracil prodrugs. Drug Metab. Dispos. 25 (1997), 270–273.
27. Pai, Y.J., Leung, K.Y., Savery, D., Hutchin, T., Prunty, H., Heales, S., Brosnan, M.E., Brosnan, J.T., Copp, A.J., Greene, N.D., Glycine decarboxylase deficiency causes neural tube defects and features of non-ketotic hyperglycinemia in mice. Nat. Commun., 6, 2015, 6388.
28. Peregrín-Alvarez, J.M., Sanford, C., Parkinson, J., The conservation and evolutionary modularity of metabolism. Genome Biol., 10, 2009, R63.
29. Pinkston, J.M., Garigan, D., Hansen, M., Kenyon, C., Mutations that increase the life span of C. elegans inhibit tumor growth. Science 313 (2006), 971–975.
30. Rosenberg, E., Zilber-Rosenberg, I., Symbiosis and development: The hologenome concept. Birth Defects Res. C Embryo Today 93 (2011), 56–66.
31. SenGupta, T., Torgersen, M.L., Kassahun, H., Vellai, T., Simonsen, A., Nilsen, H., Base excision repair AP endonucleases and mismatch repair act together to induce checkpoint-mediated autophagy. Nat. Commun., 4, 2013, 2674.
32. Ser, Z., Gao, X., Johnson, C., Mehrmohamadi, M., Liu, X., Li, S., Locasale, J.W., Targeting one carbon metabolism with an antimetabolite disrupts pyrimidine homeostasis and induces nucleotide overflow. Cell Rep. 15 (2016), 2367–2376.
33. Spanogiannopoulos, P., Bess, E.N., Carmody, R.N., Turnbaugh, P.J., The microbial pharmacists within us: A metagenomic view of xenobiotic metabolism. Nat. Rev. Microbiol. 14 (2016), 273–287.
34. Watson, E., MacNeil, L.T., Ritter, A.D., Yilmaz, L.S., Rosebrock, A.P., Caudy, A.A., Walhout, A.J., Interspecies systems biology uncovers metabolites affecting C. elegans gene expression and life history traits. Cell 156 (2014), 759–770.
35. Zeng, X., Kinsella, T.J., Impact of autophagy on chemotherapy and radiotherapy mediated tumor cytotoxicity: “To live or not to live”. Front. Oncol., 1, 2011, 30.