TY - JOUR
T1 - Gallium disrupts bacterial iron metabolism and has therapeutic effects in mice and humans with lung infections
AU - Goss, Christopher H.
AU - Kaneko, Yukihiro
AU - Khuu, Lisa
AU - Anderson, Gail D.
AU - Ravishankar, Sumedha
AU - Aitken, Moira L.
AU - Lechtzin, Noah
AU - Zhou, Guolin
AU - Czyz, Daniel M.
AU - McLean, Kathryn
AU - Olakanmi, Oyebode
AU - Shuman, Howard A.
AU - Teresi, Mary
AU - Wilhelm, Ellen
AU - Caldwell, Ellen
AU - Salipante, Stephen J.
AU - Hornick, Douglas B.
AU - Siehnel, Richard J.
AU - Becker, Lev
AU - Britigan, Bradley E.
AU - Singh, Pradeep K.
N1 - Funding Information:
The study was supported by NIH [UM1HL119073, R01HL085868, P30DK089507, and K24HL102246; Clinical and Translational Science Awards (CTSA) program Ignition Award], the Cystic Fibrosis Foundation (GOSS09A0 and SINGH15R0), the Arcadia Foundation, the Burroughs Wellcome Fund (BWF1006700), and the University of Washington's Institute of Translational Health Sciences. Study drug was donated by Genta Inc.
Publisher Copyright:
Copyright © 2018 The Authors.
PY - 2018/9/26
Y1 - 2018/9/26
N2 - The lack of new antibiotics is among the most critical challenges facing medicine. The problem is particularly acute for Gram-negative bacteria. An unconventional antibiotic strategy is to target bacterial nutrition and metabolism. The metal gallium can disrupt bacterial iron metabolism because it substitutes for iron when taken up by bacteria. We investigated the antibiotic activity of gallium ex vivo, in a mouse model of airway infection, and in a phase 1 clinical trial in individuals with cystic fibrosis (CF) and chronic Pseudomonas aeruginosa airway infections. Our results show that micromolar concentrations of gallium inhibited P. aeruginosa growth in sputum samples from patients with CF. Ex vivo experiments indicated that gallium inhibited key iron-dependent bacterial enzymes and increased bacterial sensitivity to oxidants. Furthermore, gallium resistance developed slowly, its activity was synergistic with certain antibiotics, and gallium did not diminish the antibacterial activity of host macrophages. Systemic gallium treatment showed antibiotic activity in murine lung infections. In addition, systemic gallium treatment improved lung function in people with CF and chronic P. aeruginosa lung infection in a preliminary phase 1 clinical trial. These findings raise the possibility that human infections could be treated by targeting iron metabolism or other nutritional vulnerabilities of bacterial pathogens.
AB - The lack of new antibiotics is among the most critical challenges facing medicine. The problem is particularly acute for Gram-negative bacteria. An unconventional antibiotic strategy is to target bacterial nutrition and metabolism. The metal gallium can disrupt bacterial iron metabolism because it substitutes for iron when taken up by bacteria. We investigated the antibiotic activity of gallium ex vivo, in a mouse model of airway infection, and in a phase 1 clinical trial in individuals with cystic fibrosis (CF) and chronic Pseudomonas aeruginosa airway infections. Our results show that micromolar concentrations of gallium inhibited P. aeruginosa growth in sputum samples from patients with CF. Ex vivo experiments indicated that gallium inhibited key iron-dependent bacterial enzymes and increased bacterial sensitivity to oxidants. Furthermore, gallium resistance developed slowly, its activity was synergistic with certain antibiotics, and gallium did not diminish the antibacterial activity of host macrophages. Systemic gallium treatment showed antibiotic activity in murine lung infections. In addition, systemic gallium treatment improved lung function in people with CF and chronic P. aeruginosa lung infection in a preliminary phase 1 clinical trial. These findings raise the possibility that human infections could be treated by targeting iron metabolism or other nutritional vulnerabilities of bacterial pathogens.
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U2 - 10.1126/scitranslmed.aat7520
DO - 10.1126/scitranslmed.aat7520
M3 - Article
C2 - 30257953
AN - SCOPUS:85054057700
SN - 1946-6234
VL - 10
JO - Science Translational Medicine
JF - Science Translational Medicine
IS - 460
M1 - eaat7520
ER -