CXC chemokines exhibit bactericidal activity against multidrug-resistant gram-negative pathogens

mBio

Volumn 8, Issue 6, 2017, Pages

  Crawford, Matthew A ^a   Fisher, Debra J ^a   Leung, Lisa M ^b   Lomonaco, Sara ^c   Lascols, Christine ^d   Cannatelli, Antonio ^e   Giani, Tommaso ^e   Rossolini, Gian Maria ^f,g   Doi, Yohei ^h   Goodlett, David R ⁱ   Allard, Marc W ^c   Sharma, Shashi K ^c   Khan, Erum ^j   Ernst, Robert K ^b   Hughes, Molly A ^a  

^a UNIVERSITY OF VIRGINIA   (United States)

^b UNIVERSITY OF MARYLAND DENTAL SCHOOL   (United States)

^c CENTER FOR DRUG EVALUATION AND RESEARCH   (United States)

^d NATIONAL CENTER FOR EMERGING AND ZOONOTIC INFECTIOUS DISEASES   (United States)

^e UNIVERSITY OF SIENA   (Italy)

^f UNIVERSITY OF FLORENCE   (Italy)

^g CAREGGI UNIVERSITY HOSPITAL   (Italy)

^h UNIVERSITY OF PITTSBURGH SCHOOL OF MEDICINE   (United States)

ⁱ UNIVERSITY OF MARYLAND SCHOOL OF PHARMACY   (United States)

^j AGA KHAN UNIVERSITY   (Pakistan)

more..

Author keywords

Antimicrobial resistance; Carbapenem; Chemokine; Colistin; Gram negative

Indexed keywords

ARABINOSE; BACTERIAL PROTEIN; CARBAPENEM; COLISTIN; CXCL9 CHEMOKINE; GAMMA INTERFERON INDUCIBLE PROTEIN 10; LIPID A; LIPOPOLYSACCHARIDE; MCR 1 PROTEIN; PHOSPHOETHANOLAMINE; UNCLASSIFIED DRUG; ANTIINFECTIVE AGENT; CXCL10 PROTEIN, HUMAN; CXCL9 PROTEIN, HUMAN; PHOP PROTEIN, BACTERIA; PHOQ PROTEIN, BACTERIA;

ANTIMICROBIAL ACTIVITY; ARTICLE; BACTERIAL GENE; BACTERIAL GROWTH; BACTERIAL STRAIN; BACTERICIDAL ACTIVITY; BACTERIUM ISOLATE; BACTERIUM ISOLATION; CONTROLLED STUDY; DRUG EFFECT; DRUG EFFICACY; DRUG MECHANISM; ENTEROBACTERIACEAE; GENE MUTATION; GRAM NEGATIVE BACTERIUM; KLEBSIELLA PNEUMONIAE; MGRB GENE; MULTIDRUG RESISTANCE; NONHUMAN; PRIORITY JOURNAL; GENETICS; HUMAN; METABOLISM; MICROBIAL VIABILITY; PHYSIOLOGY;

ANTI-BACTERIAL AGENTS; BACTERIAL PROTEINS; CHEMOKINE CXCL10; CHEMOKINE CXCL9; ENTEROBACTERIACEAE; HUMANS; MICROBIAL VIABILITY;

EID: 85039911192     PISSN: 21612129     EISSN: 21507511     Source Type: Journal    
DOI: 10.1128/mBio.01549-17     Document Type: Article

References (40)

1. Zilberberg MD, Shorr AF, Micek ST, Vazquez-Guillamet C, Kollef MH. 2014. Multi-drug resistance, inappropriate initial antibiotic therapy and mortality in Gram-negative severe sepsis and septic shock: a retrospective cohort study. Crit Care 18:596. https://doi.org/10.1186/s13054-014-0596-8.
2. Ventola CL. 2015. The antibiotic resistance crisis: part 1: causes and threats. P T 40:277-283.
3. Liu Y-Y, Wang Y, Walsh TR, Yi L-X, Zhang R, Spencer J, Doi Y, Tian G, Dong B, Huang X, Yu L-F, Gu D, Ren H, Chen X, Lv L, He D, Zhou H, Liang Z, Liu J-H, Shen J. 2016. Emergence of plasmid-mediated colistin resistance mechanism MCR-1 in animals and human beings in China: a microbiological and molecular biological study. Lancet Infect Dis 16:161-168. https://doi.org/10.1016/S1473-3099(15)00424-7.
4. Olaitan AO, Morand S, Rolain JM. 2014. Mechanisms of polymyxin resistance: acquired and intrinsic resistance in bacteria. Front Microbiol 5:643. https://doi.org/10.3389/fmicb.2014.00643.
5. Crawford MA, Zhu Y, Green CS, Burdick MD, Sanz P, Alem F, O’Brien AD, Mehrad B, Strieter RM, Hughes MA. 2009. Antimicrobial effects of interferon-inducible CXC chemokines against Bacillus anthracis spores and bacilli. Infect Immun 77:1664-1678. https://doi.org/10.1128/IAI.01208-08.
6. Yung SC, Murphy PM. 2012. Antimicrobial chemokines. Front Immunol 3:276. https://doi.org/10.3389/fimmu.2012.00276.
7. Yang D, Chen Q, Hoover DM, Staley P, Tucker KD, Lubkowski J, Oppenheim JJ. 2003. Many chemokines including CCL20/MIP-3alpha display antimicrobial activity. J Leukoc Biol 74:448-455. https://doi.org/10.1189/jlb.0103024.
8. Crawford MA, Burdick MD, Glomski IJ, Boyer AE, Barr JR, Mehrad B, Strieter RM, Hughes MA. 2010. Interferon-inducible CXC chemokines directly contribute to host defense against inhalational anthrax in a murine model of infection. PLoS Pathog 6:e1001199. https://doi.org/10.1371/journal.ppat.1001199.
9. González LJ, Bahr G, Nakashige TG, Nolan EM, Bonomo RA, Vila AJ. 2016. Membrane anchoring stabilizes and favors secretion of New Delhi metallo-β-lactamase. Nat Chem Biol 12:516-522. https://doi.org/10.1038/nchembio.2083.
10. Paul D, Bhattacharjee A, Bhattacharjee D, Dhar D, Maurya AP, Chakravarty A. 2017. Transcriptional analysis of blaNDM-1 and copy number alteration under carbapenem stress. Antimicrob Resist Infect Control 6:26. https://doi.org/10.1186/s13756-017-0183-2.
11. Dortet L, Poirel L, Nordmann P. 2014. Worldwide dissemination of the NDM-type carbapenemases in Gram-negative bacteria. Biomed Res Int 2014:249856. https://doi.org/10.1155/2014/249856.
12. Schutte KM, Fisher DJ, Burdick MD, Mehrad B, Mathers AJ, Mann BJ, Nakamoto RK, Hughes MA. 2015. Escherichia coli pyruvate dehydrogenase complex is an important component of CXCL10-mediated antimicrobial activity. Infect Immun 84:320-328. https://doi.org/10.1128/IAI.00552-15.
13. Hieshima K, Ohtani H, Shibano M, Izawa D, Nakayama T, Kawasaki Y, Shiba F, Shiota M, Katou F, Saito T, Yoshie O. 2003. CCL28 has dual roles in mucosal immunity as a chemokine with broad-spectrum antimicrobial activity. J Immunol 170:1452-1461. https://doi.org/10.4049/jimmunol.170.3.1452.
14. Yu Z, Qin W, Lin J, Fang S, Qiu J. 2015. Antibacterial mechanisms of polymyxin and bacterial resistance. Biomed Res Int 2015:679109. https://doi.org/10.1155/2015/679109.
15. Liu YY, Chandler CE, Leung LM, McElheny CL, Mettus RT, Shanks RMQ, Liu JH, Goodlett DR, Ernst RK, Doi Y. 2017. Structural modification of lipopolysaccharide conferred by mcr-1 in Gram-negative ESKAPE pathogens. Antimicrob Agents Chemother 61:e00580-17. https://doi.org/10.1128/AAC.00580-17.
16. Gunn JS. 2008. The Salmonella PmrAB regulon: lipopolysaccharide modifications, antimicrobial peptide resistance and more. Trends Microbiol 16:284-290. https://doi.org/10.1016/j.tim.2008.03.007.
17. Kato A, Groisman EA. 2004. Connecting two-component regulatory systems by a protein that protects a response regulator from dephosphorylation by its cognate sensor. Genes Dev 18:2302-2313. https://doi.org/10.1101/gad.1230804.
18. Lippa AM, Goulian M. 2009. Feedback inhibition in the PhoQ/PhoP signaling system by a membrane peptide. PLoS Genet 5:e1000788. https://doi.org/10.1371/journal.pgen.1000788.
19. Cannatelli A, Giani T, D’Andrea MM, Di Pilato V, Arena F, Conte V, Tryfinopoulou K, Vatopoulos A, Rossolini GM, COLGRIT Study Group. 2014. MgrB inactivation is a common mechanism of colistin resistance in KPCproducing Klebsiella pneumoniae of clinical origin. Antimicrob Agents Chemother 58:5696-5703. https://doi.org/10.1128/AAC.03110-14.
20. Crawford MA, Timme R, Lomonaco S, Lascols C, Fisher DJ, Sharma SK, Strain E, Allard MW, Brown EW, McFarland MA, Croley T, Hammack TS, Weigel LM, Anderson K, Hodge DR, Pillai SP, Morse SA, Khan E, Hughes MA. 2016. Genome sequences of multidrug-resistant, colistin-susceptible and-resistant Klebsiella pneumoniae clinical isolates from Pakistan. Genome Announc 4:e01419-16. https://doi.org/10.1128/genomeA.01419-16.
21. Jayol A, Poirel L, Brink A, Villegas MV, Yilmaz M, Nordmann P. 2014. Resistance to colistin associated with a single amino acid change in protein PmrB among Klebsiella pneumoniae isolates of worldwide origin. Antimicrob Agents Chemother 58:4762-4766. https://doi.org/10.1128/AAC.00084-14.
22. Mitrophanov AY, Jewett MW, Hadley TJ, Groisman EA. 2008. Evolution and dynamics of regulatory architectures controlling polymyxin B resistance in enteric bacteria. PLoS Genet 4:e1000233. https://doi.org/10.1371/journal.pgen.1000233.
23. Zwir I, Shin D, Kato A, Nishino K, Latifi T, Solomon F, Hare JM, Huang H, Groisman EA. 2005. Dissecting the PhoP regulatory network of Escherichia coli and Salmonella enterica. Proc Natl Acad Sci U S A 102: 2862-2867. https://doi.org/10.1073/pnas.0408238102.
24. Cannatelli A, D’Andrea MM, Giani T, Di Pilato V, Arena F, Ambretti S, Gaibani P, Rossolini GM. 2013. In vivo emergence of colistin resistance in Klebsiella pneumoniae producing KPC-type carbapenemases mediated by insertional inactivation of the PhoQ/PhoP mgrB regulator. Antimicrob Agents Chemother 57:5521-5526. https://doi.org/10.1128/AAC.01480-13.
25. Needham BD, Trent MS. 2013. Fortifying the barrier: the impact of lipid A remodelling on bacterial pathogenesis. Nat Rev Microbiol 11:467-481. https://doi.org/10.1038/nrmicro3047.
26. Llobet E, Martínez-Moliner V, Moranta D, Dahlström KM, Regueiro V, Tomás A, Cano V, Pérez-Gutiérrez C, Frank CG, Fernández-Carrasco H, Insua JL, Salminen TA, Garmendia J, Bengoechea JA. 2015. Deciphering tissue-induced Klebsiella pneumoniae lipid A structure. Proc Natl Acad Sci U S A 112:E6369-E6378. https://doi.org/10.1073/pnas.1508820112.
27. Guo L, Lim KB, Poduje CM, Daniel M, Gunn JS, Hackett M, Miller SI. 1998. Lipid A acylation and bacterial resistance against vertebrate antimicrobial peptides. Cell 95:189-198. https://doi.org/10.1016/S0092-8674(00)81750-X.
28. Zasloff M. 2002. Antimicrobial peptides of multicellular organisms. Nature 415:389-395. https://doi.org/10.1038/415389a.
29. Ageitos JM, Sánchez-Pérez A, Calo-Mata P, Villa TG. 2017. Antimicrobial peptides (AMPs): ancient compounds that represent novel weapons in the fight against bacteria. Biochem Pharmacol 133:117-138. https://doi.org/10.1016/j.bcp.2016.09.018.
30. Crawford MA, Lowe DE, Fisher DJ, Stibitz S, Plaut RD, Beaber JW, Zemansky J, Mehrad B, Glomski IJ, Strieter RM, Hughes MA. 2011. Identification of the bacterial protein FtsX as a unique target of chemokine-mediated antimicrobial activity against Bacillus anthracis. Proc Natl Acad Sci U S A 108:17159-17164. https://doi.org/10.1073/pnas.1108495108.
31. Margulieux KR, Fox JW, Nakamoto RK, Hughes MA. 2016. CXCL10 acts as a bifunctional antimicrobial molecule against Bacillus anthracis. mBio 7:e00334-16. https://doi.org/10.1128/mBio.00334-16.
32. Cannatelli A, Giani T, Antonelli A, Principe L, Luzzaro F, Rossolini GM. 2016. First detection of the mcr-1 colistin resistance gene in Escherichia coli in Italy. Antimicrob Agents Chemother 60:3257-3258. https://doi.org/10.1128/AAC.00246-16.
33. CLSI. 2015. Methods for dilution antimicrobial susceptibility tests for bacteria that grow aerobically; Approved Standards, 10th ed. CLSI document m07-A10. CLSI, Wayne, PA.
34. CLSI. 2016. Performance standards for antimicrobial susceptibility testing; 26th informational supplement. CLSI document M100-S. CLSI, Wayne, PA.
35. EUCAST. 2016. Breakpoint tables for interpretation of MICs and zone diameters, version 6.0. EUCAST, Basel, Switzerland. http://www.eucast.org.
36. Lascols C, Hackel M, Marshall SH, Hujer AM, Bouchillon S, Badal R, Hoban D, Bonomo RA. 2011. Increasing prevalence and dissemination of NDM-1 metallo-β-lactamase in India: data from the SMART study (2009). J Antimicrob Chemother 66:1992-1997. https://doi.org/10.1093/jac/dkr240.
37. El Hamidi A, Tirsoaga A, Novikov A, Hussein A, Caroff M. 2005. Microextraction of bacterial lipid A: easy and rapid method for mass spectrometric characterization. J Lipid Res 46:1773-1778. https://doi.org/10.1194/jlr.D500014-JLR200.
38. Di Pilato V, Arena F, Tascini C, Cannatelli A, Henrici De Angelis L, Fortunato S, Giani T, Menichetti F, Rossolini GM. 2016. mcr-1.2, a new mcr variant carried on a transferable plasmid from a colistin-resistant KPC carbapenemase-producing Klebsiella pneumoniae strain of sequence type 512. Antimicrob Agents Chemother 60:5612-5615. https://doi.org/10.1128/AAC.01075-16.
39. Liu P, Li P, Jiang X, Bi D, Xie Y, Tai C, Deng Z, Rajakumar K, Ou HY. 2012. Complete genome sequence of Klebsiella pneumoniae subsp. Pneumonia HS11286, a multidrug-resistant strain isolated from human sputum. J Bacteriol 194:1841-1842. https://doi.org/10.1128/JB.00043-12.
40. Siguier P, Perochon J, Lestrade L, Mahillon J, Chandler M. 2006. ISfinder: the reference centre for bacterial insertion sequences. Nucleic Acids Res 34:D32-D36. https://doi.org/10.1093/nar/gkj014.