Host-Mediated Bioactivation of Pyrazinamide: Implications for Efficacy, Resistance, and Therapeutic Alternatives

ACS Infectious Diseases

Volumn 1, Issue 5, 2015, Pages 203-214

  Via, Laura E ^a   Savic, Rada ^b   Weiner, Danielle M ^a   Zimmerman, Matthew D ^c   Prideaux, Brendan ^c   Irwin, Scott M ^d   Lyon, Eddie ^d   O'Brien, Paul ^c   Gopal, Pooja ^e   Eum, Seokyong ^f   Lee, Myungsun ^f   Lanoix, Jean Philippe ^g   Dutta, Noton K ^g   Shim, TaeSun ^h   Cho, Jeong Su ⁱ   Kim, Wooshik ^j   Karakousis, Petros C ^g   Lenaerts, Anne ^d   Nuermberger, Eric ^g   Barry, Clifton E ^a   Dartois, Véronique ^c   more..

^a NATIONAL INSTITUTE OF ALLERGY AND INFECTIOUS DISEASES   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c PUBLIC HEALTH RESEARCH INSTITUTE   (United States)

^d Department of Environmental and Radiological Health Sciences   (United States)

^e NATIONAL UNIVERSITY OF SINGAPORE   (Singapore)

^f International Tuberculosis Research Center   (South Korea)

^g JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^h Asan Medical Center   (South Korea)

ⁱ Pusan National University Hospital   (South Korea)

^j National Medical Center   (South Korea)

more..

Author keywords

bioactivation; host metabolism; Mycobacterium tuberculosis; pyrazinamide; pyrazinoic acid

Indexed keywords

ALLOPURINOL; PYRAZINAMIDE; PYRAZINOIC ACID;

ADULT; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CLINICAL ARTICLE; COMPARATIVE STUDY; CONCENTRATION RESPONSE; CONTROLLED STUDY; DISEASE RESISTANCE; DRUG BIOAVAILABILITY; DRUG BLOOD LEVEL; DRUG EFFICACY; DRUG EXPOSURE; DRUG INDICATION; DRUG PENETRATION; DRUG POTENCY; DRUG SENSITIVITY; FEMALE; GOUT; GRANULOMA; GROWTH INHIBITION; HOST; HUMAN; IN VITRO STUDY; IN VIVO STUDY; LUNG LESION; LUNG PARENCHYMA; MALE; NONHUMAN; PATHOGENESIS; PRIORITY JOURNAL; SALVAGE THERAPY; TUBERCULOSIS;

EID: 84969255804     PISSN: None     EISSN: 23738227     Source Type: Journal    
DOI: 10.1021/id500028m     Document Type: Article

References (64)

1. Anonymous (1981) Controlled trial of four thrice-weekly regimens and a daily regimen all given for 6 months for pulmonary tuberculosis Lancet 1, 171-174
2. Controlled clinical trial of 4 short-course regimens of chemotherapy (three 6-month and one 8-month) for pulmonary tuberculosis: final report. East and Central African/British Medical Research Council Fifth Collaborative Study, Tubercle 1986, 67, 5-15. 10.1016/0041-3879(86)90027-9
3. Combs, D. L., O'Brien, R. J., and Geiter, L. J. (1990) USPHS Tuberculosis Short-Course Chemotherapy Trial 21: effectiveness, toxicity, and acceptability. The report of final results Ann. Int. Med. 112, 397-406 10.7326/0003-4819-76-3-112-6-397
4. Nolan, C. M. (1990) Incorporation of pyrazinamide into community-wide treatment of tuberculosis Am. J. Public Health 80, 1525-1526 10.2105/AJPH.80.12.1525
5. Zhang, Y., Yew, W. W., and Barer, M. R. (2012) Targeting persisters for tuberculosis control Antimicrob. Agents Chemother. 56, 2223-2230 10.1128/AAC.06288-11
6. Ahmad, Z., Fraig, M. M., Bisson, G. P., Nuermberger, E. L., Grosset, J. H., and Karakousis, P. C. (2011) Dose-dependent activity of pyrazinamide in animal models of intracellular and extracellular tuberculosis infections Antimicrob. Agents Chemother. 55, 1527-1532 10.1128/AAC.01524-10
7. Diacon, A. H., Dawson, R., von Groote-Bidlingmaier, F., Symons, G., Venter, A., Donald, P. R., van Niekerk, C., Everitt, D., Winter, H., Becker, P., Mendel, C. M., and Spigelman, M. K. (2012) 14-day bactericidal activity of PA-824, bedaquiline, pyrazinamide, and moxifloxacin combinations: a randomised trial Lancet. 380, 986-993 10.1016/S0140-6736(12)61080-0
8. Ibrahim, M., Andries, K., Lounis, N., Chauffour, A., Truffot-Pernot, C., Jarlier, V., and Veziris, N. (2007) Synergistic activity of R207910 combined with pyrazinamide against murine tuberculosis Antimicrob. Agents Chemother. 51, 1011-1015 10.1128/AAC.00898-06
9. Tasneen, R., Li, S. Y., Peloquin, C. A., Taylor, D., Williams, K. N., Andries, K., Mdluli, K. E., and Nuermberger, E. L. (2011) Sterilizing activity of novel TMC207- and PA-824-containing regimens in a murine model of tuberculosis Antimicrob. Agents Chemother. 55, 5485-5492 10.1128/AAC.05293-11
10. Gopal, P. and Dick, T. (2014) Reactive dirty fragments: implications for tuberculosis drug discovery Curr. Opin. Microbiol. 21C, 7-12 10.1016/j.mib.2014.06.015
11. Solotorovsky, M., Gregory, F. J., Ironson, E. J., Bugie, E. J., O'Neill, R. C., and Pfister, R., III. (1952) Pyrazinoic acid amide; an agent active against experimental murine tuberculosis Proc. Soc. Exp. Biol. Med. 79, 563-565 10.3181/00379727-79-19447
12. Speirs, R. J., Welch, J. T., and Cynamon, M. H. (1995) Activity of n-propyl pyrazinoate against pyrazinamide-resistant Mycobacterium tuberculosis: investigations into mechanism of action of and mechanism of resistance to pyrazinamide Antimicrob. Agents Chemother. 39, 1269-1271 10.1128/AAC.39.6.1269
13. Salfinger, M. and Heifets, L. B. (1988) Determination of pyrazinamide MICs for Mycobacterium tuberculosis at different pHs by the radiometric method Antimicrob. Agents Chemother. 32, 1002-1004 10.1128/AAC.32.7.1002
14. Gumbo, T., Chigutsa, E., Pasipanodya, J., Visser, M., van Helden, P. D., Sirgel, F. A., and McIlleron, H. (2014) The pyrazinamide susceptibility breakpoint above which combination therapy fails J. Antimicrob. Chemother. 69, 2420-2425 10.1093/jac/dku136
15. Alsultan, A. and Peloquin, C. A. (2014) Therapeutic drug monitoring in the treatment of tuberculosis: an update Drugs 74, 839-854 10.1007/s40265-014-0222-8
16. Heifets, L. and Lindholm-Levy, P. (1989) Comparison of bactericidal activities of streptomycin, amikacin, kanamycin, and capreomycin against Mycobacterium avium and M. tuberculosis Antimicrob. Agents Chemother. 33, 1298-1301 10.1128/AAC.33.8.1298
17. Zhang, Y., Permar, S., and Sun, Z. (2002) Conditions that may affect the results of susceptibility testing of Mycobacterium tuberculosis to pyrazinamide J. Med. Microbiol. 51, 42-49
18. Shi, W., Zhang, X., Jiang, X., Yuan, H., Lee, J. S., Barry, C. E., 3rd, Wang, H., Zhang, W., and Zhang, Y. (2011) Pyrazinamide inhibits trans-translation in Mycobacterium tuberculosis Science 333, 1630-1632 10.1126/science.1208813
19. Mc, D. W. and Tompsett, R. (1954) Activation of pyrazinamide and nicotinamide in acidic environments in vitro Am. Rev. Tuberc. 70, 748-754
20. Hirano, K., Takahashi, M., Kazumi, Y., Fukasawa, Y., and Abe, C. (1997) Mutation in pncA is a major mechanism of pyrazinamide resistance in Mycobacterium tuberculosis Tuber Lung Dis. 78, 117-122 10.1016/S0962-8479(98)80004-X
21. Scorpio, A. and Zhang, Y. (1996) Mutations in pncA, a gene encoding pyrazinamidase/nicotinamidase, cause resistance to the antituberculous drug pyrazinamide in tubercle bacillus Nat. Med. 2, 662-667 10.1038/nm0696-662
22. Zimhony, O., Cox, J. S., Welch, J. T., Vilcheze, C., and Jacobs, W. R., Jr. (2000) Pyrazinamide inhibits the eukaryotic-like fatty acid synthetase I (FASI) of Mycobacterium tuberculosis Nat. Med. 6, 1043-1047 10.1038/79558
23. Wade, M. M. and Zhang, Y. (2006) Effects of weak acids, UV and proton motive force inhibitors on pyrazinamide activity against Mycobacterium tuberculosis in vitro J. Antimicrob. Chemother. 58, 936-941 10.1093/jac/dkl358
24. Zhang, S., Chen, J., Shi, W., Liu, W., Zhang, W., and Zhang, Y. (2013) Mutations in panD encoding aspartate decarboxylase are associated with pyrazinamide resistance in Mycobacterium tuberculosis Emerging Microbes Infect. e34 10.1038/emi.2013.38
25. Dillon, N. A., Peterson, N. D., Rosen, B. C., and Baughn, A. D. (2014) Pantothenate and pantetheine antagonize the anti-tubercular activity of pyrazinamide Antimicrob. Agents Chemother. 58, 7258-7263 10.1128/AAC.04028-14
26. Manca, C., Koo, M. S., Peixoto, B., Fallows, D., Kaplan, G., and Subbian, S. (2013) Host targeted activity of pyrazinamide in Mycobacterium tuberculosis infection PloS one 8, e74082 10.1371/journal.pone.0074082
27. Mendez, S., Traslavina, R., Hinchman, M., Huang, L., Green, P., Cynamon, M. H., and Welch, J. T. (2009) The antituberculosis drug pyrazinamide affects the course of cutaneous leishmaniasis in vivo and increases activation of macrophages and dendritic cells Antimicrob. Agents Chemother. 53, 5114-5121 10.1128/AAC.01146-09
28. Zhang, Y., Scorpio, A., Nikaido, H., and Sun, Z. (1999) Role of acid pH and deficient efflux of pyrazinoic acid in unique susceptibility of Mycobacterium tuberculosis to pyrazinamide J. Bacteriol. 181, 2044-2049
29. Konno, K., Feldmann, F. M., and McDermott, W. (1967) Pyrazinamide susceptibility and amidase activity of tubercle bacilli Am. Rev. Respir. Dis. 95, 461-469
30. Kamal, N., Mukerji, P. K., Kishore, K., Kumar, S., and Khanna, B. K. (1976) Serum levels of pyrazinamide and pyrazinoic acid following long term administration of pyrazinamide orally Ind. J. Tub. 23, 19-25
31. Lacroix, C., Hoang, T. P., Nouveau, J., Guyonnaud, C., Laine, G., Duwoos, H., and Lafont, O. (1989) Pharmacokinetics of pyrazinamide and its metabolites in healthy subjects Eur. J. Clin. Pharmacol. 36, 395-400 10.1007/BF00558302
32. Wilkins, J. J., Langdon, G., McIlleron, H., Pillai, G. C., Smith, P. J., and Simonsson, U. S. (2006) Variability in the population pharmacokinetics of pyrazinamide in South African tuberculosis patients Eur. J. Clin Pharmacol. 62, 727-735
33. Jassal, M. S., Nedeltchev, G. G., Osborne, J., and Bishai, W. R. (2011) A modified scoring system to describe gross pathology in the rabbit model of tuberculosis BMC Microbiol. 11, 49 10.1186/1471-2180-11-49
34. Manabe, Y. C., Dannenberg, A. M., Jr., Tyagi, S. K., Hatem, C. L., Yoder, M., Woolwine, S. C., Zook, B. C., Pitt, M. L., and Bishai, W. R. (2003) Different strains of Mycobacterium tuberculosis cause various spectrums of disease in the rabbit model of tuberculosis Infect. Immun. 71, 6004-6011 10.1128/IAI.71.10.6004-6011.2003
35. Dutta, N. K., Alsultan, A., Gniadek, T. J., Belchis, D. A., Pinn, M. L., Mdluli, K. E., Nuermberger, E. L., Peloquin, C. A., and Karakousis, P. C. (2013) Potent rifamycin-sparing regimen cures guinea pig tuberculosis as rapidly as the standard regimen Antimicrob. Agents Chemother. 57, 3910-3916 10.1128/AAC.00761-13
36. Magis-Escurra, C., Later-Nijland, H. M., Alffenaar, J. W., Broeders, J., Burger, D. M., van Crevel, R., Boeree, M. J., Donders, A. R., van Altena, R., van der Werf, T. S., and Aarnoutse, R. E. (2014) Population pharmacokinetics and limited sampling strategy for first-line tuberculosis drugs and moxifloxacin Int. J. Antimicrob. Agents 44, 229-234 10.1016/j.ijantimicag.2014.04.019
37. Xu, J., Jin, H., Zhu, H., Zheng, M., Wang, B., Liu, C., Chen, M., Zhou, L., Zhao, W., Fu, L., and Lu, Y. (2013) Oral bioavailability of rifampicin, isoniazid, ethambutol, and pyrazinamide in a 4-drug fixed-dose combination compared with the separate formulations in healthy Chinese male volunteers Clin. Ther. 35, 161-168 10.1016/j.clinthera.2013.01.003
38. Pasipanodya, J., McIlleron, H., Burger, A., Wash, P., Smith, P., and Gumbo, T. (2013) Serum drug concentrations predictive of pulmonary tuberculosis outcomes J. Infect Dis 208, 1464-1473 10.1093/infdis/jit352
39. Weiner, I. M. and Tinker, J. P. (1972) Pharmacology of pyrazinamide: metabolic and renal function studies related to the mechanism of drug-induced urate retention J. Pharmacol. Exp. Ther. 180, 411-434
40. Yamamoto, T., Moriwaki, Y., Takahashi, S., Hada, T., and Higashino, K. (1987) In vitro conversion of pyrazinamide into 5-hydroxypyrazinamide and that of pyrazinoic acid into 5-hydroxypyrazinoic acid by xanthine oxidase from human liver Biochem. Pharmacol. 36, 3317-3318 10.1016/0006-2952(87)90654-X
41. Pacher, P., Nivorozhkin, A., and Szabo, C. (2006) Therapeutic effects of xanthine oxidase inhibitors: renaissance half a century after the discovery of allopurinol Pharmacol. Rev. 58, 87-114 10.1124/pr.58.1.6
42. Workman, P. and White, R. A. (1982) Effects of the xanthine oxidase inhibitor allopurinol on the renal clearance of nitroimidazoles Biochem. Pharmacol. 31, 3041-3046 10.1016/0006-2952(82)90077-6
43. Nakamura, K., Natsugoe, S., Kumanohoso, T., Shinkawa, T., Kariyazono, H., Yamada, K., Baba, M., Yoshinaka, H., Fukumoto, T., and Aikou, T. (1996) Prophylactic action of allopurinol against chemotherapy-induced stomatitis - inhibition of superoxide dismutase and proteases Anti-Cancer Drugs 7, 235-239 10.1097/00001813-199605000-00001
44. Davies, P. D. (2003) The role of DOTS in tuberculosis treatment and control Am. J. Respir Med. 2, 203-209 10.1007/BF03256649
45. Aono, A., Chikamatsu, K., Yamada, H., Kato, T., and Mitarai, S. (2014) Association between pncA gene mutations, pyrazinamidase activity, and pyrazinamide susceptibility testing in Mycobacterium tuberculosis Antimicrob. Agents Chemother. 58, 4928-4930 10.1128/AAC.02394-14
46. Miotto, P., Cabibbe, A. M., Feuerriegel, S., Casali, N., Drobniewski, F., Rodionova, Y., Bakonyte, D., Stakenas, P., Pimkina, E., Augustynowicz-Kopec, E., Degano, M., Ambrosi, A., Hoffner, S., Mansjo, M., Werngren, J., Rusch-Gerdes, S., Niemann, S., and Cirillo, D. M. (2014) Mycobacterium tuberculosis Pyrazinamide Resistance Determinants: a Multicenter Study mBio 5, e01819-14 10.1128/mBio.01819-14
47. Feuerriegel, S., Koser, C. U., and Niemann, S. (2014) Phylogenetic polymorphisms in antibiotic resistance genes of the Mycobacterium tuberculosis complex J. Antimicrob. Chemother. 69, 1205-1210 10.1093/jac/dkt535
48. Simons, S. O., van Ingen, J., van der Laan, T., Mulder, A., Dekhuijzen, P. N., Boeree, M. J., and van Soolingen, D. (2012) Validation of pncA gene sequencing in combination with the mycobacterial growth indicator tube method to test susceptibility of Mycobacterium tuberculosis to pyrazinamide J. Clin. Microbiol. 50, 428-434 10.1128/JCM.05435-11
49. WHO. Tuberculosis MDR-TB & XDR-TB 2011 Progress Report.
50. Ellard, G. A. (1969) Absorption, metabolism and excretion of pyrazinamide in man Tubercle 50, 144-158 10.1016/0041-3879(69)90020-8
51. Klemens, S. P., Sharpe, C. A., and Cynamon, M. H. (1996) Activity of pyrazinamide in a murine model against Mycobacterium tuberculosis isolates with various levels of in vitro susceptibility Antimicrob. Agents Chemother. 40, 14-16
52. Ahuja, S. D., Ashkin, D., Avendano, M., Banerjee, R., Bauer, M., Bayona, J. N., Becerra, M. C., Benedetti, A., Burgos, M., Centis, R., Chan, E. D., Chiang, C. Y., Cox, H., D'Ambrosio, L., DeRiemer, K., Dung, N. H., Enarson, D., Falzon, D., Flanagan, K., Flood, J., Garcia-Garcia, M. L., Gandhi, N., Granich, R. M., Hollm-Delgado, M. G., Holtz, T. H., Iseman, M. D., Jarlsberg, L. G., Keshavjee, S., Kim, H. R., Koh, W. J., Lancaster, J., Lange, C., de Lange, W. C., Leimane, V., Leung, C. C., Li, J., Menzies, D., Migliori, G. B., Mishustin, S. P., Mitnick, C. D., Narita, M., O'Riordan, P., Pai, M., Palmero, D., Park, S. K., Pasvol, G., Pena, J., Perez-Guzman, C., Quelapio, M. I., Ponce-de-Leon, A., Riekstina, V., Robert, J., Royce, S., Schaaf, H. S., Seung, K. J., Shah, L., Shim, T. S., Shin, S. S., Shiraishi, Y., Sifuentes-Osornio, J., Sotgiu, G., Strand, M. J., Tabarsi, P., Tupasi, T. E., van Altena, R., Van der Walt, M., Van der Werf, T. S., Vargas, M. H., Viiklepp, P., Westenhouse, J., Yew, W. W., and Yim, J. J. (2012) Multidrug resistant pulmonary tuberculosis treatment regimens and patient outcomes: an individual patient data meta-analysis of 9,153 patients PLoS Med. 9, e1001300 10.1371/journal.pmed.1001300
53. Chang, K. C., Leung, C. C., Yew, W. W., Leung, E. C., Leung, W. M., Tam, C. M., and Zhang, Y. (2012) Pyrazinamide may improve fluoroquinolone-based treatment of multidrug-resistant tuberculosis Antimicrob. Agents Chemother. 56, 5465-5475 10.1128/AAC.01300-12
54. Toida, I. (1973) Metabolism of pyrazinamide. Pyrazinamide deamidase of animal tissues Am. Rev. Resp. Dis. 107, 630-638
55. Richert, D. A. and Westerfeld, W. W. (1953) Vitamin E deficiency and xanthine oxidase in rabbits Exp. Biol. Med. 84, 468-470 10.3181/00379727-84-20680
56. Lacroix, C., Guyonnaud, C., Chaou, M., Duwoos, H., and Lafont, O. (1988) Interaction between allopurinol and pyrazinamide Eur. Respir. J. 1, 807-811
57. Mitchison, D. and Davies, G. (2012) The chemotherapy of tuberculosis: past, present and future Int. J. Tuberc. Lung Dis. 16, 724-732 10.5588/ijtld.12.0083
58. Shih, T. Y., Pai, C. Y., Yang, P., Chang, W. L., Wang, N. C., and Hu, O. Y. (2013) A novel mechanism underlies the hepatotoxicity of pyrazinamide Antimicrob. Agents Chemother. 57, 1685-1690 10.1128/AAC.01866-12
59. Subbian, S., Tsenova, L., O'Brien, P., Yang, G., Koo, M. S., Peixoto, B., Fallows, D., Zeldis, J. B., Muller, G., and Kaplan, G. (2011) Phosphodiesterase-4 inhibition combined with isoniazid treatment of rabbits with pulmonary tuberculosis reduces macrophage activation and lung pathology Am. J. Pathol. 179, 289-301 10.1016/j.ajpath.2011.03.039
60. Via, L. E., Lin, P. L., Ray, S. M., Carrillo, J., Allen, S. S., Eum, S. Y., Taylor, K., Klein, E., Manjunatha, U., Gonzales, J., Lee, E. G., Park, S. K., Raleigh, J. A., Cho, S. N., McMurray, D. N., Flynn, J. L., and Barry, C. E., III. (2008) Tuberculous Granulomas are Hypoxic in Guinea pigs, Rabbits, and Non-Human Primates Infect. Immun. 76, 2333-2340 10.1128/IAI.01515-07
61. Driver, E. R., Ryan, G. J., Hoff, D. R., Irwin, S. M., Basaraba, R. J., Kramnik, I., and Lenaerts, A. J. (2012) Evaluation of a mouse model of necrotic granuloma formation using C3HeB/FeJ mice for testing of drugs against Mycobacterium tuberculosis Antimicrob. Agents Chemother. 56, 3181-3195 10.1128/AAC.00217-12
62. Dutta, N. K., Alsultan, A., Peloquin, C. A., and Karakousis, P. C. (2013) Preliminary pharmacokinetic study of repeated doses of rifampin and rifapentine in guinea pigs Antimicrob. Agents Chemother. 57, 1535-1537 10.1128/AAC.01933-12
63. Zhang, Y., Wade, M. M., Scorpio, A., Zhang, H., and Sun, Z. (2003) Mode of action of pyrazinamide: disruption of Mycobacterium tuberculosis membrane transport and energetics by pyrazinoic acid J. Antimicrob. Chemother. 52, 790-795 10.1093/jac/dkg446
64. Raynaud, C., Laneelle, M. A., Senaratne, R. H., Draper, P., Laneelle, G., and Daffe, M. (1999) Mechanisms of pyrazinamide resistance in mycobacteria: importance of lack of uptake in addition to lack of pyrazinamidase activity Microbiology 145, 1359-1367 10.1099/13500872-145-6-1359