Structure and Inhibition of Microbiome β-Glucuronidases Essential to the Alleviation of Cancer Drug Toxicity

Chemistry and Biology

Volumn 22, Issue 9, 2015, Pages 1238-1249

  Wallace, Bret D ^a   Roberts, Adam B ^b   Pollet, Rebecca M ^a   Ingle, James D ^a   Biernat, Kristen A ^a   Pellock, Samuel J ^a   Venkatesh, Madhu Kumar ^c   Guthrie, Leah ^c   O'Neal, Sara K ^d   Robinson, Sara J ^a   Dollinger, Makani ^a   Figueroa, Esteban ^a   McShane, Sarah R ^a   Cohen, Rachel D ^a   Jin, Jian ^d   Frye, Stephen V ^d   Zamboni, William C ^d   Pepe Ranney, Charles ^e   Mani, Sridhar ^c   Kelly, Libusha ^c   Redinbo, Matthew R ^a,b   more..

^a The University of North Carolina at Chapel Hill   (United States)

^b UNIVERSITY OF NORTH CAROLINA SCHOOL OF MEDICINE   (United States)

^c ALBERT EINSTEIN COLLEGE OF MEDICINE   (United States)

^d UNIVERSITY OF NORTH CAROLINA   (United States)

^e NONE   (United States)

Author keywords

chemotherapy induced diarrhea; irinotecan; microbiota; NSAIDs

Indexed keywords

BETA GLUCURONIDASE; IRINOTECAN; ANTINEOPLASTIC AGENT; BACTERIAL PROTEIN; CAMPTOTHECIN; ENZYME INHIBITOR;

ANIMAL EXPERIMENT; ARTICLE; BACTEROIDES FRAGILIS; CATALYSIS; CLOSTRIDIUM PERFRINGENS; CONFORMATIONAL TRANSITION; CRYSTAL STRUCTURE; DRUG BLOOD LEVEL; DRUG METABOLISM; ENZYME INHIBITION; ESCHERICHIA COLI; FIRMICUTES; GASTROINTESTINAL TOXICITY; IN VITRO STUDY; IN VIVO STUDY; MAXIMUM PLASMA CONCENTRATION; MICROBIOME; MOUSE; NONHUMAN; PHARMACOKINETIC PARAMETERS; PRIORITY JOURNAL; STREPTOCOCCUS AGALACTIAE; TIME TO MAXIMUM PLASMA CONCENTRATION; AMINO ACID SEQUENCE; ANALOGS AND DERIVATIVES; ANIMAL; ANTAGONISTS AND INHIBITORS; BAGG ALBINO MOUSE; CHEMISTRY; DRUG EFFECTS; DRUG SCREENING; ENZYMOLOGY; METABOLISM; MICROFLORA; MOLECULAR GENETICS; MOLECULAR MODEL;

AMINO ACID SEQUENCE; ANIMALS; ANTINEOPLASTIC AGENTS; BACTERIAL PROTEINS; BACTEROIDES FRAGILIS; CAMPTOTHECIN; CLOSTRIDIUM PERFRINGENS; DRUG SCREENING ASSAYS, ANTITUMOR; ENZYME INHIBITORS; ESCHERICHIA COLI; GLUCURONIDASE; MICE; MICE, INBRED BALB C; MICROBIOTA; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; STREPTOCOCCUS AGALACTIAE;

EID: 84941938693     PISSN: 10745521     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.chembiol.2015.08.005     Document Type: Article

References (43)

1. U.A. Boelsterli, M.R. Redinbo, and K. Saitta Multiple NSAID-induced hits injure the small intestine: underlying mechanisms and novel strategies Toxicol. Sci. 131 2012 654 667
2. K. Brune, and B. Hinz The discovery and development of antiinflammatory drugs Arthritis Rheum. 50 2004 2391 2399
3. G.G. Chabot Clinical pharmacology and pharmacodynamics of irinotecan Ann. N. Y. Acad. Sci. 803 1996 164 172
4. S. Chen, M.-F. Yueh, C. Bigo, O. Barbier, K. Wang, M. Karin, N. Nguyen, and R.H. Tukey Intestinal glucuronidation protects against chemotherapy-induced toxicity by irinotecan (CPT-11) Proc. Natl. Acad. Sci. USA 110 2013 19143 19148
5. I. Cho, S. Yamanishi, L. Cox, B.A. Methé, J. Zavadil, K. Li, Z. Gao, D. Mahana, K. Raju, I. Teitler, and et al. Antibiotics in early life alter the murine colonic microbiome and adiposity Nature 488 2012 621 626
6. T. Conroy, F. Desseigne, M. Ychou, O. Bouché, R. Guimbaud, Y. Bécouarn, A. Adenis, J.-L. Raoul, S. Gourgou-Bourgade, C. de la Fouchardière, and et al. FOLFIRINOX versus gemcitabine for metastatic pancreatic cancer N. Engl. J. Med. 364 2011 1817 1825
7. D. Cunningham, S. Pyrhönen, R.D. James, C.J. Punt, T.F. Hickish, R. Heikkila, T.B. Johannesen, H. Starkhammar, C.A. Topham, L. Awad, and et al. Randomised trial of irinotecan plus supportive care versus supportive care alone after fluorouracil failure for patients with metastatic colorectal cancer Lancet 352 1998 1413 1418
8. J.Y. Douillard, D. Cunningham, A.D. Roth, M. Navarro, R.D. James, P. Karasek, P. Jandik, T. Iveson, J. Carmichael, M. Alakl, and et al. Irinotecan combined with fluorouracil compared with fluorouracil alone as first-line treatment for metastatic colorectal cancer: a multicentre randomised trial Lancet 355 2000 1041 1047
9. G. Dranitsaris, J. Maroun, and A. Shah Severe chemotherapy-induced diarrhea in patients with colorectal cancer: a cost of illness analysis Support Care Cancer 13 2005 318 324
10. M. Fittkau, W. Voigt, H.-J. Holzhausen, and H.-J. Schmoll Saccharic acid 1.4-lactone protects against CPT-11-induced mucosa damage in rats J. Cancer Res. Clin. Oncol. 130 2004 388 394
11. K. Gloux, O. Berteau, H. Oumami El, F. Béguet, M. Leclerc, and J. Doré A metagenomic β-glucuronidase uncovers a core adaptive function of the human intestinal microbiome Proc. Natl. Acad. Sci. USA 108 Suppl 1 2011 4539 4546
12. E. Gupta, T.M. Lestingi, R. Mick, J. Ramirez, E.E. Vokes, and M.J. Ratain Metabolic fate of irinotecan in humans: correlation of glucuronidation with diarrhea Cancer Res. 54 1994 3723 3725
13. M.I. Hassan, A. Waheed, J.H. Grubb, H.E. Klei, S. Korolev, and W.S. Sly High resolution crystal structure of human beta-glucuronidase reveals structural basis of lysosome targeting PLoS One 8 2013 e79687
14. E. Holmes, J.V. Li, T. Athanasiou, H. Ashrafian, and J.K. Nicholson Understanding the role of gut microbiome-host metabolic signal disruption in health and disease Trends Microbiol. 19 2011 349 359
15. E.Y. Hsiao, S.W. McBride, S. Hsien, G. Sharon, E.R. Hyde, T. McCue, J.A. Codelli, J. Chow, S.E. Reisman, J.F. Petrosino, and et al. Microbiota modulate behavioral and physiological abnormalities associated with neurodevelopmental disorders Cell 155 2013 1451 1463
16. H. Hurwitz, L. Fehrenbacher, W. Novotny, T. Cartwright, J. Hainsworth, W. Heim, J. Berlin, A. Baron, S. Griffing, E. Holmgren, and et al. Bevacizumab plus irinotecan, fluorouracil, and leucovorin for metastatic colorectal cancer N. Engl. J. Med. 350 2004 2335 2342
17. S. Jain, W.B. Drendel, Z.W. Chen, F.S. Mathews, W.S. Sly, and J.H. Grubb Structure of human beta-glucuronidase reveals candidate lysosomal targeting and active-site motifs Nat. Struct. Biol. 3 1996 375 381
18. H. Kelly, and R.M. Goldberg Systemic therapy for metastatic colorectal cancer: current options, current evidence J. Clin. Oncol. 23 2005 4553 4560
19. R. Kong, T. Liu, X. Zhu, S. Ahmad, A.L. Williams, A.T. Phan, H. Zhao, J.E. Scott, L.-A. Yeh, and S.T.C. Wong Old drug new use - amoxapine and its metabolites as potent bacterial β-glucuronidase inhibitors for alleviating cancer drug toxicity Clin. Cancer Res. 20 2014 3521 3530
20. L. Laine, L.G. Connors, A. Reicin, C.J. Hawkey, R. Burgos-Vargas, T.J. Schnitzer, Q.F. Yu, and C. Bombardier Serious lower gastrointestinal clinical events with nonselective NSAID or coxib use Gastroenterology 124 2003 288 292
21. A. Lanas A review of the gastrointestinal safety data - a gastroenterologist's perspective Rheumatology 49 2010 ii3 ii10
22. A. Lanas, and F. Sopena Nonsteroidal anti-inflammatory drugs and lower gastrointestinal complications Gastroenterol. Clin. North Am. 38 2009 333 352
23. A. LoGuidice, B.D. Wallace, L. Bendel, M.R. Redinbo, and U.A. Boelsterli Pharmacologic targeting of bacterial β-glucuronidase alleviates nonsteroidal anti-inflammatory drug-induced enteropathy in mice J. Pharmacol. Exp. Ther. 341 2012 447 454
24. M. Ma, and H. McLeod Lessons learned from the irinotecan metabolic pathway Curr. Med. Chem. 10 2003 41 49
25. S. Mani, U.A. Boelsterli, and M.R. Redinbo Interrogating and modulating mammalian-microbial communication for improved health Annu. Rev. Pharmacol. Toxicol. 55 2014 559 580
26. R.H.J. Mathijssen, R.J. van Alphen, J. Verweij, W.J. Loos, K. Nooter, G. Stoter, and A. Sparreboom Clinical pharmacokinetics and metabolism of irinotecan (CPT-11) Clin. Cancer Res. 7 2001 2182 2194
27. I. Matsumura, and A.D. Ellington In vitro evolution of beta-glucuronidase into a beta-galactosidase proceeds through non-specific intermediates J. Mol. Biol. 305 2001 331 339
28. B.A. Methé, K.E. Nelson, M. Pop, H.H. Creasy, M.G. Giglio, C. Huttenhower, D. Gevers, J.F. Petrosino, S. Abubucker, J.H. Badger, and et al. A framework for human microbiome research Nature 486 2012 215 221
29. X.C. Morgan, T.L. Tickle, H. Sokol, D. Gevers, K.L. Devaney, D.V. Ward, J.A. Reyes, S.A. Shah, N. LeLeiko, S.B. Snapper, and et al. Dysfunction of the intestinal microbiome in inflammatory bowel disease and treatment Genome Biol. 13 2012 R79
30. J.K. Nicholson, E. Holmes, J. Kinross, R. Burcelin, G. Gibson, W. Jia, and S. Pettersson Host-gut microbiota metabolic interactions Science 336 2012 1262 1267
31. C.S. Plottel, and M.J. Blaser Microbiome and malignancy Cell Host Microbe 10 2011 324 335
32. M.R. Redinbo The Microbiota, chemical symbiosis, and human disease J. Mol. Biol. 426 2014 3877 3891
33. A.B. Roberts, B.D. Wallace, M.K. Venkatesh, S. Mani, and M.R. Redinbo Molecular insights into microbial β-glucuronidase inhibition to abrogate CPT-11 toxicity Mol. Pharmacol. 84 2013 208 217
34. M.L. Rothenberg, N.J. Meropol, E.A. Poplin, E. Van Cutsem, and S. Wadler Mortality associated with irinotecan plus bolus fluorouracil/leucovorin: summary findings of an independent panel J. Clin. Oncol. 19 2001 3801 3807
35. K.S. Saitta, C. Zhang, K.K. Lee, K. Fujimoto, M.R. Redinbo, and U.A. Boelsterli Bacterial beta-glucuronidase inhibition protects mice against enteropathy induced by indomethacin, ketoprofen, or diclofenac: mode of action and pharmacokinetics Xenobiotica 44 2014 28 35
36. M.I. Smith, T. Yatsunenko, M.J. Manary, I. Trehan, R. Mkakosya, J. Cheng, A.L. Kau, S.S. Rich, P. Concannon, J.C. Mychaleckyj, and et al. Gut microbiomes of Malawian twin pairs discordant for kwashiorkor Science 339 2013 548 554
37. A. Stein, W. Voigt, and K. Jordan Chemotherapy-induced diarrhea: pathophysiology, frequency and guideline-based management Ther. Adv. Med. Oncol. 2 2010 51 63
38. The Human Microbiome Project Consortium Structure, function and diversity of the healthy human microbiome Nature 486 2012 207 214
39. P.J. Turnbaugh, R.E. Ley, M.A. Mahowald, V. Magrini, E.R. Mardis, and J.I. Gordon An obesity-associated gut microbiome with increased capacity for energy harvest Nature 444 2006 1027 1031
40. B.D. Wallace, and M.R. Redinbo The human microbiome is a source of therapeutic drug targets Curr. Opin. Chem. Biol. 17 2013 379 384
41. B.D. Wallace, H. Wang, K.T. Lane, J.E. Scott, J. Orans, J.S. Koo, M. Venkatesh, C. Jobin, L.-A. Yeh, S. Mani, and et al. Alleviating cancer drug toxicity by inhibiting a bacterial enzyme Science 330 2010 831 835
42. Z. Wang, E. Klipfell, B.J. Bennett, R. Koeth, B.S. Levison, B. Dugar, A.E. Feldstein, E.B. Britt, X. Fu, Y.-M. Chung, and et al. Gut flora metabolism of phosphatidylcholine promotes cardiovascular disease Nature 472 2011 57 63
43. P. Wenzl, L. Wong, K. Kwang-won, and R.A. Jefferson A functional screen identifies lateral transfer of beta-glucuronidase (GUS) from bacteria to fungi Mol. Biol. Evol. 22 2005 308 316