Metallobiology of host-pathogen interactions: An intoxicating new insight

Trends in Microbiology

Volumn 20, Issue 3, 2012, Pages 106-112

  Botella, Hélène ^a,b   Stadthagen, Gustavo ^a,b   Lugo Villarino, Geanncarlo ^a,b   de Chastellier, Chantal ^c   Neyrolles, Olivier ^a,b  

^a INSTITUT DE PHARMACOLOGIE ET DE BIOLOGIE STRUCTURALE   (France)

^b UNIVERSITÉ DE TOULOUSE   (France)

^c CENTRE D IMMUNOLOGIE DE MARSEILLE LUMINY   (France)

Author keywords

CtpC; Macrophage killing mechanism; Mycobacteria; NRAMP1; P type ATPase; Transition metal

Indexed keywords

ADENOSINE TRIPHOSPHATASE; COPPER; NATURAL RESISTANCE ASSOCIATED MACROPHAGE PROTEIN 1; ZINC;

COPPER METABOLISM; HEAVY METAL POISONING; HOMEOSTASIS; HOST PATHOGEN INTERACTION; HOST RESISTANCE; INNATE IMMUNITY; MICROBIAL GROWTH; MICROBIAL IMMUNITY; MOLECULAR PHYLOGENY; MYCOBACTERIUM TUBERCULOSIS; NONHUMAN; PHAGOCYTE; PRIORITY JOURNAL; REVIEW; ZINC METABOLISM;

BACTERIAL PROTEINS; CATION TRANSPORT PROTEINS; COPPER; HOST-PATHOGEN INTERACTIONS; HUMANS; IRON; MYCOBACTERIUM TUBERCULOSIS; TUBERCULOSIS;

BACTERIA (MICROORGANISMS); CORYNEBACTERINEAE; MYCOBACTERIUM TUBERCULOSIS; VERTEBRATA;

EID: 84858002232     PISSN: 0966842X     EISSN: 18784380     Source Type: Journal    
DOI: 10.1016/j.tim.2012.01.005     Document Type: Review

References (54)

1. Pluddemann A., et al. Innate immunity to intracellular pathogens: macrophage receptors and responses to microbial entry. Immunol. Rev. 2011, 240:11-24.
2. Fortier A., et al. Single gene effects in mouse models of host: pathogen interactions. J. Leukoc. Biol. 2005, 77:868-877.
3. Solomons N.W. Malnutrition and infection: an update. Br. J. Nutr. 2007, 98(Suppl. 1):S5-S10.
4. Maggini S., et al. Selected vitamins and trace elements support immune function by strengthening epithelial barriers and cellular and humoral immune responses. Br. J. Nutr. 2007, 98(Suppl. 1):S29-S35.
5. White C., et al. A role for the ATP7A copper-transporting ATPase in macrophage bactericidal activity. J. Biol. Chem. 2009, 284:33949-33956.
6. Ward S.K., et al. CtpV: a putative copper exporter required for full virulence of Mycobacterium tuberculosis. Mol. Microbiol. 2010, 77:1096-1110.
7. Botella H., et al. Mycobacterial p(1)-type ATPases mediate resistance to zinc poisoning in human macrophages. Cell Host Microbe 2011, 10:248-259.
8. Russell D.G. The galvanizing of Mycobacterium tuberculosis: an antimicrobial mechanism. Cell Host Microbe 2011, 10:181-183.
9. Wolschendorf F., et al. Copper resistance is essential for virulence of Mycobacterium tuberculosis. Proc. Natl. Acad. Sci. U.S.A. 2011, 108:1621-1626.
10. Shafeeq S., et al. The cop operon is required for copper homeostasis and contributes to virulence in Streptococcus pneumoniae. Mol. Microbiol. 2011, 81:1255-1270.
11. Kehl-Fie T.E., Skaar E.P. Nutritional immunity beyond iron: a role for manganese and zinc. Curr. Opin. Chem. Biol. 2010, 14:218-224.
12. Vidal S., et al. The Ity/Lsh/Bcg locus: natural resistance to infection with intracellular parasites is abrogated by disruption of the Nramp1 gene. J. Exp. Med. 1995, 182:655-666.
13. Appelberg R. Macrophage nutriprive antimicrobial mechanisms. J. Leukoc. Biol. 2006, 79:1117-1128.
14. Nairz M., et al. Interferon-gamma limits the availability of iron for intramacrophage Salmonella typhimurium. Eur. J. Immunol. 2008, 38:1923-1936.
15. Moller M., Hoal E.G. Current findings, challenges and novel approaches in human genetic susceptibility to tuberculosis. Tuberculosis (Edinb.) 2010, 90:71-83.
16. North R.J., et al. Consequence of Nramp1 deletion to Mycobacterium tuberculosis infection in mice. Infect. Immun. 1999, 67:5811-5814.
17. Jabado N., et al. Natural resistance to intracellular infections: natural resistance-associated macrophage protein 1 (Nramp1) functions as a pH-dependent manganese transporter at the phagosomal membrane. J. Exp. Med. 2000, 192:1237-1248.
18. Forbes J.R., Gros P. Iron, manganese, and cobalt transport by Nramp1 (Slc11a1) and Nramp2 (Slc11a2) expressed at the plasma membrane. Blood 2003, 102:1884-1892.
19. +/bivalent cation antiporter. Biochem. J. 2001, 354(Pt 3):511-519.
20. De Voss J.J., et al. The salicylate-derived mycobactin siderophores of Mycobacterium tuberculosis are essential for growth in macrophages. Proc. Natl. Acad. Sci. U.S.A. 2000, 97:1252-1257.
21. Rodriguez G.M., Smith I. Identification of an ABC transporter required for iron acquisition and virulence in Mycobacterium tuberculosis. J. Bacteriol. 2006, 188:424-430.
22. Siegrist M.S., et al. Mycobacterial Esx-3 is required for mycobactin-mediated iron acquisition. Proc. Natl. Acad. Sci. U.S.A. 2009, 106:18792-18797.
23. Waldron K.J., Robinson N.J. How do bacterial cells ensure that metalloproteins get the correct metal?. Nat. Rev. Microbiol. 2009, 7:25-35.
24. Colvin R.A., et al. Cytosolic zinc buffering and muffling: their role in intracellular zinc homeostasis. Metallomics 2010, 2:306-317.
25. Jomova K., Valko M. Advances in metal-induced oxidative stress and human disease. Toxicology 2011, 283:65-87.
26. Liu T., et al. CsoR is a novel Mycobacterium tuberculosis copper-sensing transcriptional regulator. Nat. Chem. Biol. 2007, 3:60-68.
27. Tailleux L., et al. Probing host pathogen cross-talk by transcriptional profiling of both Mycobacterium tuberculosis and infected human dendritic cells and macrophages. PLoS ONE 2008, 3:e1403.
28. Festa R.A., et al. A novel copper-responsive regulon in Mycobacterium tuberculosis. Mol. Microbiol. 2011, 79:133-148.
29. Gold B., et al. Identification of a copper-binding metallothionein in pathogenic mycobacteria. Nat. Chem. Biol. 2008, 4:609-616.
30. Schwan W.R., et al. Mutations in the cueA gene encoding a copper homeostasis P-type ATPase reduce the pathogenicity of Pseudomonas aeruginosa in mice. Int. J. Med. Microbiol. 2005, 295:237-242.
31. Rosch J.W., et al. Role of the manganese efflux system mntE for signalling and pathogenesis in Streptococcus pneumoniae. Mol. Microbiol. 2009, 72:12-25.
32. Veyrier F.J., et al. A novel metal transporter mediating manganese export (MntX) regulates the Mn to Fe intracellular ratio and Neisseria meningitidis virulence. PLoS Pathog. 2011, 7:e1002261.
33. Lansdown A.B. Metallothioneins: potential therapeutic aids for wound healing in the skin. Wound Repair Regen. 2002, 10:130-132.
34. Rofe A.M., et al. Trace metal, acute phase and metabolic response to endotoxin in metallothionein-null mice. Biochem. J. 1996, 314(Pt 3):793-797.
35. Wagner D., et al. Elemental analysis of Mycobacterium avium-, Mycobacterium tuberculosis-, and Mycobacterium smegmatis-containing phagosomes indicates pathogen-induced microenvironments within the host cell's endosomal system. J. Immunol. 2005, 174:1491-1500.
36. Kim B.E., et al. Mechanisms for copper acquisition, distribution and regulation. Nat. Chem. Biol. 2008, 4:176-185.
37. Lichten L.A., Cousins R.J. Mammalian zinc transporters: nutritional and physiologic regulation. Annu. Rev. Nutr. 2009, 29:153-176.
38. van den Berghe P.V., et al. Human copper transporter 2 is localized in late endosomes and lysosomes and facilitates cellular copper uptake. Biochem. J. 2007, 407:49-59.
39. Bertinato J., et al. Ctr2 is partially localized to the plasma membrane and stimulates copper uptake in COS-7 cells. Biochem. J. 2008, 409:731-740.
40. Rees E.M., et al. Mobilization of intracellular copper stores by the ctr2 vacuolar copper transporter. J. Biol. Chem. 2004, 279:54221-54229.
41. Prohaska J.R., Gybina A.A. Intracellular copper transport in mammals. J. Nutr. 2004, 134:1003-1006.
42. Fukada T., et al. Zinc homeostasis and signaling in health and diseases: zinc signaling. J. Biol. Inorg. Chem. 2011, 16:1123-1134.
43. Vasak M., Meloni G. Chemistry and biology of mammalian metallothioneins. J. Biol. Inorg. Chem. 2011, 16:1067-1078.
44. Maret W. Molecular aspects of human cellular zinc homeostasis: redox control of zinc potentials and zinc signals. Biometals 2009, 22:149-157.
45. Wellenreuther G., et al. The ligand environment of zinc stored in vesicles. Biochem. Biophys. Res. Commun. 2009, 380:198-203.
46. Aydemir T.B., et al. Zinc transporter ZIP8 (SLC39A8) and zinc influence IFN-gamma expression in activated human T cells. J. Leukoc. Biol. 2009, 86:337-348.
47. Kitamura H., et al. Toll-like receptor-mediated regulation of zinc homeostasis influences dendritic cell function. Nat. Immunol. 2006, 7:971-977.
48. Cao J., et al. Effects of intracellular zinc depletion on metallothionein and ZIP2 transporter expression and apoptosis. J. Leukoc. Biol. 2001, 70:559-566.
49. Begum N.A., et al. Mycobacterium bovis BCG cell wall and lipopolysaccharide induce a novel gene, BIGM103, encoding a 7-TM protein: identification of a new protein family having Zn-transporter and Zn-metalloprotease signatures. Genomics 2002, 80:630-645.
50. Axelsen K.B., Palmgren M.G. Evolution of substrate specificities in the P-type ATPase superfamily. J. Mol. Evol. 1998, 46:84-101.
51. Kuhlbrandt W. Biology, structure and mechanism of P-type ATPases. Nat. Rev. Mol. Cell Biol. 2004, 5:282-295.
52. Rensing C., et al. The zntA gene of Escherichia coli encodes a Zn(II)-translocating P-type ATPase. Proc. Natl. Acad. Sci. U.S.A. 1997, 94:14326-14331.
53. Rensing C., et al. CopA: an Escherichia coli Cu(I)-translocating P-type ATPase. Proc. Natl. Acad. Sci. U.S.A. 2000, 97:652-656.
54. Arguello J.M., et al. The structure and function of heavy metal transport P1B-ATPases. Biometals 2007, 20:233-248.