Gallium nitrate is efficacious in murine models of tuberculosis and inhibits key bacterial fe-dependent enzymes

Antimicrobial Agents and Chemotherapy

Volumn 57, Issue 12, 2013, Pages 6074-6080

  Olakanmi, Oyebode ^a,b   Kesavalu, Banurekha ^a   Pasula, Rajamouli ^a,b   Abdalla, Maher Y ^c,d,e   Schlesinger, Larry S ^f   Britigan, Bradley E ^c,d,e  

^a UNIVERSITY OF CINCINNATI MEDICAL CENTER   (United States)

^b UNIVERSITY OF CINCINNATI COLLEGE OF MEDICINE   (United States)

^c VA NEBRASKA WESTERN IOWA HEALTH CARE SYSTEM   (United States)

^d Pathology and Microbiology Department   (United States)

^e UNIVERSITY OF NEBRASKA MEDICAL CENTER   (United States)

^f THE OHIO STATE UNIVERSITY COLLEGE OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACONITATE HYDRATASE; BACTERIAL ENZYME; DNA; GALLIUM; GALLIUM NITRATE; IRON; RIBONUCLEOTIDE REDUCTASE; SODIUM CHLORIDE; SODIUM NITRATE; ANTIMETABOLITE; BACTERIAL PROTEIN; TUBERCULOSTATIC AGENT;

ANIMAL EXPERIMENT; ANTIBACTERIAL ACTIVITY; ARTICLE; BACTERIAL GROWTH; BACTERIAL STRAIN; COLONY FORMING UNIT; CONTROLLED STUDY; DNA REPLICATION; DRUG EFFICACY; DRUG INHIBITION; ENZYME ACTIVITY; GROWTH INHIBITION; HUMAN; HUMAN CELL; INFECTION; LIVER; LUNG; LUNG TUBERCULOSIS; MACROPHAGE; MOUSE; MYCOBACTERIUM TUBERCULOSIS; NONHUMAN; PRIORITY JOURNAL; SPLEEN; SURVIVAL RATE; ANIMAL; ANTAGONISTS AND INHIBITORS; BACTERIAL COUNT; BAGG ALBINO MOUSE; DISEASE MODEL; DRUG EFFECTS; GROWTH, DEVELOPMENT AND AGING; METABOLISM; MICROBIOLOGY; MORTALITY; PATHOLOGY; SCID MOUSE; SURVIVAL; TUBERCULOSIS, PULMONARY;

ACONITATE HYDRATASE; ANIMALS; ANTIMETABOLITES; ANTITUBERCULAR AGENTS; BACTERIAL PROTEINS; COLONY COUNT, MICROBIAL; DISEASE MODELS, ANIMAL; GALLIUM; IRON; LIVER; LUNG; MICE; MICE, INBRED BALB C; MICE, SCID; MYCOBACTERIUM TUBERCULOSIS; RIBONUCLEOTIDE REDUCTASES; SPLEEN; SURVIVAL ANALYSIS; TUBERCULOSIS, PULMONARY;

EID: 84887479723     PISSN: 00664804     EISSN: 10986596     Source Type: Journal    
DOI: 10.1128/AAC.01543-13     Document Type: Article

References (40)

1. Zumla A, Raviglione M, Hafner R, Fordham von Reyn C. 2013. Tuberculosis. N. Engl. J. Med. 368:745-755.
2. WHO. 2012. Tuberculosis. Fact sheet no 104, November 2011. WHO, Geneva, Switzerland. http://www.who.int/mediacentre/factsheets/fs104/en/index.html.
3. Bernstein LR. 1998. Mechanisms of therapeutic activity for gallium. Pharmacol. Rev. 50:665-682.
4. Gobin J, Moore CH, Reeve JR, Wong DK, Gibson BW, Horwitz MA. 1995. Iron acquisition by Mycobacterium tuberculosis: isolation and characterization of a family of iron-binding exochelins. Proc. Natl. Acad. Sci. U. S. A. 92:5189-5193.
5. Antunes LCS, Imperi F, Minandri F, Visca P. 2012. In vitro and in vivo antimicrobial activities of gallium nitrate against multidrug-resistant Acinetobacter baumannii. Antimicrob. Agents Chemother. 56:5961-5970.
6. Olakanmi O, Britigan BE, Schlesinger LS. 2000. Gallium disrupts iron metabolism of mycobacteria residing within human macrophages. Infect. Immun. 68:5619-5627.
7. Gomes MS, Boelaert JR, Appelberg R. 2001. Role of iron in experimental Mycobacterium avium infection. J. Clin. Virol. 20:117-122.
8. Gobin J, Horwitz MA. 1996. Exochelins of Mycobacterium tuberculosis remove iron from human iron-binding proteins and donate iron to mycobactins in the M. tuberculosis cell wall. J. Exp. Med. 183:1527-1532.
9. Lounis N, Truffot-Pernot C, Grosset J, Gordeuk VR, Boelaert JR. 2001. Iron and Mycobacterium tuberculosis infection. J. Clin. Virol. 20:123-126.
10. Rodriguez GM, Smith I. 2006. Identification of an ABC transporter required for iron acquisition and virulence in Mycobacterium tuberculosis. J. Bacteriol. 188:424-430.
11. Pandey R, Rodriguez GM. 2012. A ferritin mutant of Mycobacterium tuberculosis is highly susceptible to killing by antibiotics and is unable to establish a chronic infection in mice. Infect. Immun. 80:3650-3659.
12. Tullius MV, Harmston CA, Owens CP, Chim N, Morse RP, McMath LM, Iniguez A, Kimmey JM, Sawaya MR, Whitelegge JP, Horwitz MA, Goulding CW. 2011. Discovery and characterization of a unique mycobacterial heme acquisition system. Proc. Natl. Acad. Sci. U. S. A. 108: 5051-5056.
13. Cronje L, Bornman L. 2005. Iron overload and tuberculosis: a case for iron chelation therapy. Int. J. Tuberc. Lung Dis. 9:2-9.
14. Cronjé L, Edmondson N, Eisenach KD, Bornman L. 2005. Iron and iron chelating agents modulate Mycobacterium tuberculosis growth and monocyte-macrophage viability and effector functions. FEMS Immunol. Med. Microbiol. 45:103-112.
15. Bernstein LR. 2005. 31Ga therapeutic gallium compounds, p 259-277. In Gielen M, Tiekink ERT (ed), Metallotherapeutic drugs and metal-based diagnostic agents. John Wiley & Sons, Ltd, Chichester, United Kingdom.
16. Kaneko Y, Thoendel M, Olakanmi O, Britigan BE, Singh PK. 2007. The transition metal gallium disrupts Pseudomonas aeruginosa iron metabolism and has antimicrobial and antibiofilm activity. J. Clin. Invest. 117: 877-888.
17. Olakanmi O, Gunn JS, Su S, Soni S, Hassett DJ, Britigan BE. 2010. Gallium disrupts iron uptake by intracellular and extracellular Francisella strains and exhibits therapeutic efficacy in a murine pulmonary infection model. Antimicrob. Agents Chemother. 54:244-253.
18. Stojiljkovic I, Kumar V, Srinivasan N. 1999. Non-iron metalloporphyrins: potent antibacterial compounds that exploit haem/Hb uptake systems of pathogenic bacteria. Mol. Microbiol. 31:429-442.
19. Schlesinger LS, Bellinger-Kawahara CG, Payne NR, Horwitz MA. 1990. Phagocytosis of Mycobacterium tuberculosis is mediated by human monocyte complement receptors and complement component C3. J. Immunol. 144:2771-2780.
20. Lechuga-Ballesteros D, Truong-Le V, Patzer EJ. 2009. Comment on: resistance of planktonic and biofilm-grown Burkholderia cepacia complex isolates to the transition metal gallium. J. Antimicrob. Chemother. 63:1078-1079.
21. Jong A, Yu K, Zhou B, Frgala T, Reynolds CP, Yen Y. 1998. A simple and sensitive ribonucleotide reductase assay. J. Biomed. Sci. 5:62-68.
22. Kennedy MC, Emptage MH, Dreyer JL, Beinert H. 1983. The role of iron in the activation-inactivation of aconitase. J. Biol. Chem. 258:11098-11105.
23. Thelander L, Reichard P. 1979. Reduction of ribonucleotides. Annu. Rev. Biochem. 48:133-158.
24. Dawes SS, Warner DF, Tsenova L, Timm J, McKinney JD, Kaplan G, Rubin H, Mizrahi V. 2003. Ribonucleotide reduction in Mycobacterium tuberculosis: function and expression of genes encoding class Ib and class II ribonucleotide reductases. Infect. Immun. 71:6124-6131.
25. Smith BD, Karp JE. 2003. Ribonucleotide reductase: an old target with new potential. Leuk. Res. 27:1075-1076.
26. Gardner PR. 2002. Aconitase: sensitive target and measure of superoxide. Methods Enzymol. 349:9-23.
27. Banerjee S, Nandyala AK, Raviprasad P, Ahmed N, Hasnain SE. 2007. Iron-dependent RNA-binding activity of Mycobacterium tuberculosis aconitase. J. Bacteriol. 189:4046-4052.
28. Chan ED, Iseman MD. 2008. Multidrug-resistant and extensively drugresistant tuberculosis: a review. Curr. Opin. Infect. Dis. 21:587-595.
29. Jurado RL. 1997. Iron, infections, and anemia of inflammation. Clin. Infect. Dis. 25:888-895.
30. Olakanmi O, Schlesinger LS, Ahmed A, Britigan BE. 2004. The nature of extracellular iron influences iron acquisition by Mycobacterium tuberculosis residing within human macrophages. Infect. Immun. 72:2022-2028.
31. Hedley DW, Tripp EH, Slowiaczek P, Mann GJ. 1988. Effect of gallium on DNA synthesis by human T-cell lymphoblasts. Cancer Res. 48:3014-3018.
32. Berggren MM, Burns LA, Abraham RT, Powis G. 1993. Inhibition of protein tyrosine phosphatase by the antitumor agent gallium nitrate. Cancer Res. 53:1862-1866.
33. Custer RP, Bosma GC, Bosma MJ. 1985. Severe combined immunodeficiency (SCID) in the mouse. Pathology, reconstitution, neoplasms. Am. J. Pathol. 120:464-477.
34. Bhardwaj V, Kanagawa O, Swanson PE, Unanue ER. 1998. Chronic Listeria infection in SCID mice: requirements for the carrier state and the dual role of T cells in transferring protection or suppression. J. Immunol. 160:376-384.
35. Fattorini L, Mattei M, Placido R, Li BO, Iona E, Agrimi U, Colizzi V, Orefici G. 1999. Mycobacterium avium infection in BALB/c and SCID mice. J. Med. Microbiol. 48:577-583.
36. North RJ, Jung Y-J. 2004. Immunity to tuberculosis. Annu. Rev. Immunol. 22:599-623.
37. Vilchèze C, Jacobs WR. 2012. The combination of sulfamethoxazole, trimethoprim, and isoniazid or rifampin is bactericidal and prevents the emergence of drug resistance in Mycobacterium tuberculosis. Antimicrob. Agents Chemother. 56:5142-5148.
38. de Léséleuc L, Harris G, KuoLee R, Chen W. 2012. In vitro and in vivo biological activities of iron chelators and gallium nitrate against Acinetobacter baumannii. Antimicrob. Agents Chemother. 56:5397-5400.
39. DeLeon K, Balldin F, Watters C, Hamood A, Griswold J, Sreedharan S, Rumbaugh KP. 2009. Gallium maltolate treatment eradicates Pseudomonas aeruginosa infection in thermally injured mice. Antimicrob. Agents Chemother. 53:1331-1337.
40. Harrington JR, Martens RJ, Cohen ND, Bernstein LR. 2006. Antimicrobial activity of gallium against virulent Rhodococcus equi in vitro and in vivo. J. Vet. Pharmacol. Ther. 29:121-127.