Vancomycin Analogue Restores Meropenem Activity against NDM-1 Gram-Negative Pathogens

ACS Infectious Diseases

Volumn 4, Issue 7, 2018, Pages 1093-1101

  Yarlagadda, Venkateswarlu ^a   Sarkar, Paramita ^a   Samaddar, Sandip ^a   Manjunath, Goutham Belagula ^a   Mitra, Susweta Das ^b   Paramanandham, Krishnamoorthy ^b   Shome, Bibek Ranjan ^b   Haldar, Jayanta ^a  

^a JAWAHARLAL NEHRU CENTRE FOR ADVANCED SCIENTIFIC RESEARCH   (India)

^b ICAR NATIONAL INSTITUTE OF VETERINARY EPIDEMIOLOGY AND DISEASE INFORMATICS   (India)

Author keywords

antibacterial activity; antibiotic resistance; glycopeptide antibiotics; meropenem; NDM 1 Gram negative bacteria; vancomycin

Indexed keywords

BETA LACTAMASE INHIBITOR; COLISTIN; DIPICOLYL VANCOMYCIN; MEROPENEM; METAL ION; UNCLASSIFIED DRUG; VANCOMYCIN DERIVATIVE; ANTIINFECTIVE AGENT; BETA LACTAMASE; BETA-LACTAMASE NDM-1; VANCOMYCIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIBACTERIAL ACTIVITY; ARTICLE; BACTERIUM ISOLATE; CONTROLLED STUDY; ENZYME ACTIVE SITE; ENZYME INACTIVATION; ESCHERICHIA COLI; FEMALE; GRAM NEGATIVE BACTERIUM; KLEBSIELLA PNEUMONIAE; MOUSE; NONHUMAN; OUTER MEMBRANE; PRIORITY JOURNAL; SEPSIS; ANIMAL; BETA-LACTAM RESISTANCE; CELL MEMBRANE PERMEABILITY; CHEMICAL STRUCTURE; DRUG EFFECT; DRUG POTENTIATION; ENZYME ACTIVATION; GENE EXPRESSION REGULATION; GENETICS; KLEBSIELLA INFECTION; METABOLISM; MICROBIOLOGY; SYNTHESIS;

ANIMALS; ANTI-BACTERIAL AGENTS; BETA-LACTAM RESISTANCE; BETA-LACTAMASES; CELL MEMBRANE PERMEABILITY; DRUG SYNERGISM; ENZYME ACTIVATION; FEMALE; GENE EXPRESSION REGULATION, BACTERIAL; GRAM-NEGATIVE BACTERIA; KLEBSIELLA INFECTIONS; KLEBSIELLA PNEUMONIAE; MEROPENEM; MICE; MOLECULAR STRUCTURE; VANCOMYCIN;

EID: 85046634810     PISSN: None     EISSN: 23738227     Source Type: Journal    
DOI: 10.1021/acsinfecdis.8b00011     Document Type: Article

References (49)

1. Taubes, G. (2008) The bacteria fight back. Science 321, 356-361, 10.1126/science.321.5887.356
2. Bush, K., Courvalin, P., Dantas, G., Davies, J., Eisenstein, B., Huovinen, P., Jacoby, G. A., Kishony, R., Kreiswirth, B. N., Kutter, E., Lerner, S. A., Levy, S., Lewis, K., Lomovskaya, O., Miller, J. H., Mobashery, S., Piddock, L. J., Projan, S., Thomas, C. M., Tomasz, A. Z., Tulkens, P. M., Walsh, T. R., Watson, J. D., Witkowski, J., Witte, W., Wright, G., Yeh, P., and Zgurskaya, H. I. (2011) Tackling antibiotic resistance. Nat. Rev. Microbiol. 9, 894-896, 10.1038/nrmicro2693
3. Piddock, L. J. (2012) The crisis of no new antibiotics-what is the way forward?. Lancet Infect. Dis. 12, 249-253, 10.1016/S1473-3099(11)70316-4
4. World Health Organization. (2014) Antimicrobial resistance: global report on surveillance, World Health Organization, Geneva, Switzerland, http://www.who.int/drugresistance/documents/surveillancereport/en/ (accessed 9th May 2014).
5. Arpin, C., Noury, P., Boraud, D., Coulange, L., Manetti, A., Andre, C., M'Zali, F., and Quentin, C. (2012) NDM-1-Producing Klebsiella pneumoniae resistant to colistin in a French community patient without history of foreign travel. Antimicrob. Agents Chemother. 56, 3432-3434, 10.1128/AAC.00230-12
6. Bush, K. and Jacoby, G. A. (2010) Updated functional classification of β-lactamases. Antimicrob. Agents Chemother. 54, 969-976, 10.1128/AAC.01009-09
7. Mattei, P. J., Neves, D., and Dessen, A. (2010) Bridging cell wall biosynthesis and bacterial morphogenesis. Curr. Opin. Struct. Biol. 20, 749-575, 10.1016/j.sbi.2010.09.014
8. Cox, G. and Wright, G. D. (2013) Intrinsic antibiotic resistance: mechanisms, origins, challenges and solutions. Int. J. Med. Microbiol. 303, 287-292, 10.1016/j.ijmm.2013.02.009
9. Butler, M. S., Blaskovich, M. A. T., and Cooper, M. A. (2017) Antibiotics in the clinical pipeline in 2015. J. Antibiot. 70, 3-24, 10.1038/ja.2016.72
10. Walsh, T. R., Toleman, M. A., Poirel, L., and Nordmann, P. (2005) Metallo-β-lactamases: the quiet before the storm?. Clin. Microbiol. Rev. 18, 306-325, 10.1128/CMR.18.2.306-325.2005
11. Mao, W., Xia, L., and Xie, H. (2017) Detection of carbapenemase-producing organisms with a carbapenem-based fluorogenic probe. Angew. Chem., Int. Ed. 56, 4468-4472, 10.1002/anie.201612495
12. Cornaglia, G., Giamarellou, H., and Rossolini, G. M. (2011) Metallo-β-lactamases: a last frontier for β-lactams?. Lancet Infect. Dis. 11, 381-393, 10.1016/S1473-3099(11)70056-1
13. Page, M. I. and Badarau, A. (2008) The mechanisms of catalysis by metallo β-lactamases. Bioinorg. Chem. Appl. 2008, 576297, 10.1155/2008/576297
14. Spencer, J., Read, J., Sessions, R. B., Howell, S., Blackburn, G. M., and Gamblin, S. J. (2005) Antibiotic recognition by binuclear metallo-beta-lactamases revealed by X-ray crystallography. J. Am. Chem. Soc. 127, 14439-14444, 10.1021/ja0536062
15. Ehmann, D. E., Jahic, C., Ross, P. L., Gu, R. F., Hu, J., Durand-Reville, T. F., Lahiri, S., Thresher, J., Livchak, S., Gao, N., Palmer, T., Walkup, G. K., and Fisher, S. L. (2013) Kinetics of avibactam inhibition against class A, C, and D β-lactamases. J. Biol. Chem. 288, 27960-27971, 10.1074/jbc.M113.485979
16. Durand-Réville, T. F., Guler, S., Comita-Prevoir, J., Chen, B., Bifulco, N., Huynh, H., Lahiri, S., Shapiro, A. B., McLeod, S. M., Carter, N. M., Moussa, S. H., Velez-Vega, C., Olivier, N. B., McLaughlin, R., Gao, N., Thresher, J., Palmer, T., Andrews, B., Giacobbe, R. A., Newman, J. V., Ehmann, D. E., de Jonge, B., O'Donnell, J., Mueller, J. P., Tommasi, R. A., and Miller, A. A. (2017) ETX2514 is a broad-spectrum β-lactamase inhibitor for the treatment of drug-resistant Gram-negative bacteria including Acinetobacter baumannii. Nat. Microbiol. 2, 17104, 10.1038/nmicrobiol.2017.104
17. Crowder, M. W., Spencer, J., and Vila, A. J. (2006) Metallo-β-lactamases: novel weaponry for antibiotic resistance in bacteria. Acc. Chem. Res. 39, 721-728, 10.1021/ar0400241
18. González, L. J., Bahr, G., Nakashige, T. G., Nolan, E. M., Bonomo, R. A., and Vila, A. J. (2016) Membrane anchoring stabilizes and favors secretion of New Delhi metallo-β-lactamase. Nat. Chem. Biol. 12, 516-522, 10.1038/nchembio.2083
19. Bushnell, G., Mitrani-Gold, F., and Mundy, L. M. (2013) Emergence of New Delhi metallo-β-lactamase type 1-producing enterobacteriaceae and non-enterobacteriaceae: Global case detection and bacterial surveillance. Int. J. Infect. Dis. 17, e325-e333, 10.1016/j.ijid.2012.11.025
20. Bush, K. (2013) Proliferation and significance of clinically relevant β-lactamases. Ann. N. Y. Acad. Sci. 1277, 84-90, 10.1111/nyas.12023
21. Shakil, S., Azhar, E. I., Tabrez, S., Kamal, M. A., Jabir, N. R., Abuzenadah, A. M., Damanhouri, G. A., and Alam, Q. (2011) New Delhi metallo-β-lactamase (NDM-1): An update. J. Chemother. 23, 263-265, 10.1179/joc.2011.23.5.263
22. Drawz, S. M., Papp-Wallace, K. M., and Bonomo, R. A. (2014) New β-lactamase inhibitors: A therapeutic renaissance in an MDR world. Antimicrob. Agents Chemother. 58, 1835-1846, 10.1128/AAC.00826-13
23. Fast, W. and Sutton, L. D. (2013) Metallo-β-lactamase: inhibitors and reporter substrates. Biochim. Biophys. Acta, Proteins Proteomics 1834, 1648-1659, 10.1016/j.bbapap.2013.04.024
24. Wright, G. D. (2016) Antibiotic adjuvants: rescuing antibiotics from resistance. Trends Microbiol. 24, 862-871, 10.1016/j.tim.2016.06.009
25. González, M. M., Kosmopoulou, M., Mojica, M. F., Castillo, V., Hinchliffe, P., Pettinati, I., Brem, J., Schofield, C. J., Mahler, G., Bonomo, R. A., Llarrull, L. I., Spencer, J., and Vila, A. J. (2015) Bisthiazolidines: a substrate-mimicking scaffold as an inhibitor of the NDM-1 carbapenemase. ACS Infect. Dis. 1, 544-554, 10.1021/acsinfecdis.5b00046
26. King, A. M., Reid-Yu, S. A., Wang, W., King, D. T., De Pascale, G., Strynadka, N. C., Walsh, T. R., Coombes, B. K., and Wright, G. D. (2014) Aspergillomarasmine A overcomes metallo-beta-lactamase antibiotic resistance. Nature 510, 503-506, 10.1038/nature13445
27. Falconer, S. B., Reid-Yu, S. A., King, A. M., Gehrke, S. S., Wang, W., Britten, J. F., Coombes, B. K., Wright, G. D., and Brown, E. D. (2015) Zinc chelation by a small-molecule adjuvant potentiates Meropenem activity in vivo against NDM-1-producing Klebsiella pneumoniae. ACS Infect. Dis. 1, 533-543, 10.1021/acsinfecdis.5b00033
28. Brem, J., van Berkel, S. S., Aik, W., Rydzik, A. M., Avison, M. B., Pettinati, I., Umland, K. D., Kawamura, A., Spencer, J., Claridge, T. D., McDonough, M. A., and Schofield, C. J. (2014) Rhodanine hydrolysis leads to potent thioenolate mediated metallo-β-lactamase inhibition. Nat. Chem. 6, 1084-1090, 10.1038/nchem.2110
29. Brackett, C. M., Melander, R. J., An, I. H., Krishnamurthy, A., Thompson, R. J., Cavanagh, J., and Melander, C. (2014) Small molecule suppression of β-lactam resistance in multi-drug resistant gram-negative pathogens. J. Med. Chem. 57, 7450-7458, 10.1021/jm501050e
30. Cahill, S. T., Cain, R., Wang, D. Y., Lohans, C. T., Wareham, D. W., Oswin, H. P., Mohammed, J., Spencer, J., Fishwick, C. W. G., McDonough, M. A., Schofield, C. J., and Brem, J. (2017) Cyclic boronates inhibit all classes of β-lactamase. Antimicrob. Agents Chemother. 61, e02260-16, 10.1128/AAC.02260-16
31. Tehrani, K. H. M. E. and Martin, N. I. (2017) Thiol-containing metallo-β-lactamase inhibitors resensitize resistant Gram-negative bacteria to Meropenem. ACS Infect. Dis. 3, 711-717, 10.1021/acsinfecdis.7b00094
32. Chen, A. Y., Thomas, P. W., Stewart, A. C., Bergstrom, A., Cheng, Z., Miller, C., Bethel, C. R., Marshall, S. H., Credille, C. V., Riley, C. L., Page, R. C., Bonomo, R. A., Crowder, M. W., Tierney, D. L., Fast, W., and Cohen, S. M. (2017) Dipicolinic acid derivatives as inhibitors of New Delhi metallo-β-lactamase-1. J. Med. Chem. 60, 7267-7283, 10.1021/acs.jmedchem.7b00407
33. Mikami, Y. and Suzuki, T. (1983) Novel microbial inhibitors of angiotensin-converting enzyme, aspergillomarasmines A and B. Agric. Biol. Chem. 47, 2693-2695, 10.1080/00021369.1983.10866020
34. Sully, E. K., Geller, B. L., Li, L., Moody, C. M., Bailey, S. M., Moore, A. L., Wong, M., Nordmann, P., Daly, S. M., Sturge, C. R., and Greenberg, D. E. (2017) Peptide-conjugated phosphorodiamidate morpholino oligomer (PPMO) restores carbapenem susceptibility to NDM-1-positive pathogens in vitro and in vivo. J. Antimicrob. Chemother. 72, 782-790, 10.1093/jac/dkw476
35. Yarlagadda, V., Sarkar, P., Samaddar, S., and Haldar, J. (2016) A vancomycin derivate with a pyrophosphate binding group: a strategy to combat vancomycin-resistant bacteria. Angew. Chem., Int. Ed. 55, 7836-7840, 10.1002/anie.201601621
36. Shen, B., Yu, Y., Chen, H., Cao, X., Lao, X., Fang, Y., Shi, Y., Chen, J., and Zheng, H. (2013) Inhibitor discovery of full-length New Delhi metallo-β-lactamase-1 (NDM-1). PLoS One 8, e62955, 10.1371/journal.pone.0062955
37. Bulik, C. C., Fauntleroy, K. A., Jenkins, S. G., Abuali, M., LaBombardi, V. J., Nicolau, D. P., and Kuti, J. L. (2010) Comparison of Meropenem MICs and susceptibilities for carbapenemase-producing Klebsiella pneumoniae isolates by various testing methods. J. Clin. Microbiol. 48, 2402-2406, 10.1128/JCM.00267-10
38. Yarlagadda, V., Manjunath, G. B., Sarkar, P., Akkapeddi, P., Paramanandham, K., Shome, B. R., Ravikumar, R., and Haldar, J. (2016) Glycopeptide antibiotic to overcome the intrinsic resistance of Gram-negative bacteria. ACS Infect. Dis. 2, 132-139, 10.1021/acsinfecdis.5b00114
39. Kim, Y., Cunningham, M. A., Mire, J., Tesar, C., Sacchettini, J., and Joachimiak, A. (2013) NDM-1, the ultimate promiscuous enzyme: substrate recognition and catalytic mechanism. FASEB J. 27, 1917-1927, 10.1096/fj.12-224014
40. Nordmann, P., Cuzon, G., and Naas, T. (2009) The real threat of Klebsiella pneumoniae carbapenemase-producing bacteria. Lancet Infect. Dis. 9, 228-236, 10.1016/S1473-3099(09)70054-4
41. Livermore, D. M., Warner, M., Mushtaq, S., Doumith, M., Zhang, J., and Woodford, N. (2011) What remains against carbapenem-resistant Enterobacteriaceae? Evaluation of chloramphenicol, ciprofloxacin, colistin, fosfomycin, minocycline, nitrofurantoin, temocillin and tigecycline. Int. J. Antimicrob. Agents 37, 415-419, 10.1016/j.ijantimicag.2011.01.012
42. Uppu, D. S., Ghosh, C., and Haldar, J. (2015) Surviving sepsis in the era of antibiotic resistance: Are there any alternative approaches to antibiotic therapy?. Microb. Pathog. 80, 7-13, 10.1016/j.micpath.2015.02.001
43. Uppu, D. S., Manjunath, G. B., Yarlagadda, V., Kaviyil, J. E., Ravikumar, R., Paramanandham, K., Shome, B. R., and Haldar, J. (2015) Membrane-active macromolecules resensitize NDM-1 gram-negative clinical isolates to tetracycline antibiotics. PLoS One 10, e0119422, 10.1371/journal.pone.0119422
44. Yarlagadda, V., Akkapeddi, P., Manjunath, G. B., and Haldar, J. (2014) Membrane active vancomycin analogues: A strategy to combat bacterial resistance. J. Med. Chem. 57, 4558-4568, 10.1021/jm500270w
45. Yarlagadda, V., Konai, M. M., Manjunath, G. B., Ghosh, C., and Haldar, J. (2015) Tackling vancomycin-resistant bacteria with lipophilic-vancomycin-carbohydrate conjugates. J. Antibiot. 68, 302-312, 10.1038/ja.2014.144
46. Yarlagadda, V., Sarkar, P., Manjunath, G. B., and Haldar, J. (2015) Lipophilic vancomycin aglycon dimer with high activity against vancomycin-resistant bacteria. Bioorg. Med. Chem. Lett. 25, 5477-5580, 10.1016/j.bmcl.2015.10.083
47. Yarlagadda, V., Konai, M. M., Paramanandham, K., Nimita, V. C., Shome, B. R., and Haldar, J. (2015) In-vivo efficacy and pharmacological properties of a novel glycopeptide (YV4465) against vancomycin-intermediate Staphylococcus aureus (VISA). Int. J. Antimicrob. Agents 46, 446-450, 10.1016/j.ijantimicag.2015.05.014
48. Yarlagadda, V., Samaddar, S., Paramanandham, K., Shome, B. R., and Haldar, J. (2015) Membrane disruption and enhanced inhibition of cell wall biosynthesis: A synergistic approach to tackle vancomycin-resistant bacteria. Angew. Chem., Int. Ed. 54, 13644-13649, 10.1002/anie.201507567
49. Yarlagadda, V., Samaddar, S., and Haldar, J. (2016) Intracellular activity of a membrane-active glycopeptide antibiotic against methicillin-resistant Staphylococcus aureus infection. J. Glob. Antimicrob. Resist. 5, 71-74, 10.1016/j.jgar.2015.12.007