Siderocalins: Siderophore binding proteins evolved for primary pathogen host defense

Current Opinion in Chemical Biology

Volumn 17, Issue 2, 2013, Pages 150-157

  Sia, Allyson K ^a   Allred, Benjamin E ^a   Raymond, Kenneth N ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BINDING PROTEIN; ENTEROCHELIN; LIPOCALIN; SIDEROCALIN; SIDEROPHORE; UNCLASSIFIED DRUG;

BACTERIAL GROWTH; BACTERIAL SURVIVAL; CHICKEN; EMBRYO DEVELOPMENT; HOST RESISTANCE; HUMAN; INFLAMMATION; NEOPLASM; NONHUMAN; QUAIL; REVIEW; TEAR FILM;

ANIMALS; BACTERIAL INFECTIONS; CARRIER PROTEINS; HOST-PATHOGEN INTERACTIONS; HUMANS; IRON; LIPOCALINS; PROTEIN BINDING; SIDEROPHORES;

ANIMALIA; BACTERIA (MICROORGANISMS); GALLUS GALLUS; PHASIANIDAE;

EID: 84876703848     PISSN: 13675931     EISSN: 18790402     Source Type: Journal    
DOI: 10.1016/j.cbpa.2012.11.014     Document Type: Review

References (63)

1. Crichton R.R. Iron Metabolism-From Molecular Mechanisms to Clinical Consequences 2009, John Wiley & Sons Ltd.
2. Miethke M., Marahiel M.A. Siderophore-based iron acquisition and pathogen control. Microbiol Mol Biol Rev 2007, 71:413-451.
3. Raymond K.N., Dertz E.A. Biochemical and physical properties of siderophores. Iron Transport in Bacteria 2004, 3-17. ASM Press. J.H. Crosa, A.R. Mey, S.M. Payne (Eds.).
4. Clifton M.C., Corrent C., Strong R.K. Siderocalins: siderophore-binding proteins of the innate immune system. Biometals 2009, 22:557-564.
5. åkerstrom B., Flower D.R., Salier J.-P. Lipocalins: unity in diversity. Biochim Biophys Acta (BBA)-Protein Structure and Molecular Enzymolog 2000, 1482:1-8.
6. Flo T.H., Smith K.D., Sato S., Rodriguez D.J., Holmes M.A., Strong R.K., Akira S., Aderem A. Lipocalin 2 mediates an innate immune response to bacterial infection by sequestrating iron. Nature 2004, 432:917-921.
7. Goetz D.H., Holmes M.A., Borregaard N., Bluhm M.E., Raymond K.N., Strong R.K. The neutrophil lipocalin NGAL is a bacteriostatic agent that interferes with siderophore-mediated iron acquisition. Mol Cell 2002, 10:1033-1043.
8. Faurschou M., Borregaard N. Neutrophil granules and secretory vesicles in inflammation. Microbes Infect 2003, 5:1317-1327.
9. Cho H., Kim J.-H. Lipocalin2 expressions correlate significantly with tumor differentiation in epithelial ovarian cancer. J Histochem Cytochem 2009, 57:513-521.
10. Wang H.-J., He X.-J., Ma Y.-Y., Jiang X.-T., Xia Y.-J., Ye Z.-Y., Zhao Z.-S., Tao H.-Q. Expressions of neutrophil gelatinase-associated lipocalin in gastric cancer: a potential biomarker for prognosis and an ancillary diagnostic test. Anat Rec (Hoboken) 2010, 293:1855-1863.
11. Han W.K., Wagener G., Zhu Y., Wang S., Lee H.T. Urinary biomarkers in the early detection of acute kidney injury after cardiac surgery. Clin J Am Soc Nephrol 2009, 4:873-882.
12. Mallbris L., O'Brien K.P., Hulthén A., Sandstedt B., Cowland J.B., Borregaard N., Ståhle-Bäckdahl M. Neutrophil gelatinase-associated lipocalin is a marker for dysregulated keratinocyte differentiation in human skin. Exp Dermatol 2002, 11:584-591.
13. Bao G., Clifton M., Hoette T.M., Mori K., Deng S.-X., Qiu A., Viltard M., Williams D., Paragas N., Leete T., et al. Iron traffics in circulation bound to a siderocalin (Ngal)-catechol complex. Nat Chem Biol 2010, 6:602-609.
14. Yang J., Goetz D., Li J.Y., Wang W., Mori K., Setlik D., Du T., Erdjument-Bromage H., Tempst P., Strong R., et al. An iron delivery pathway mediated by a lipocalin. Mol Cell 2002, 10:1045-1056.
15. Mori K., Lee H.T., Rapoport D., Drexler I.R., Foster K., Yang J., Schmidt-Ott K.M., Chen X., Li J.Y., Weiss S., et al. Endocytic delivery of lipocalin-siderophore-iron complex rescues the kidney from ischemia-reperfusion injury. J Clin Invest 2005, 115:610-621.
16. Owen H.C., Roberts S.J., Ahmed S.F., Farquharson C. Dexamethasone-induced expression of the glucocorticoid response gene lipocalin 2 in chondrocytes. Am J Physiol Endocrinol Metab 2008, 294:E1023-E1034.
17. Landrø L., Damås J.K., Flo T.H., Heggelund L., Ueland T., Tjønnfjord G.E., Espevik T., Aukrust P., Frøland S.S. Decreased serum lipocalin-2 levels in human immunodeficiency virus-infected patients: increase during highly active anti-retroviral therapy. Clin Exp Immunol 2008, 152:57-63.
18. Cowland J.B., Sørensen O.E., Sehested M., Borregaard N. Neutrophil gelatinase-associated lipocalin is up-regulated in human epithelial cells by IL-1 beta, but not by TNF-alpha. J Immunol 2003, 171:6630-6639.
19. Tan B.K., Adya R., Shan X., Syed F., Lewandowski K.C., O'Hare J.P., Randeva H.S. Ex vivo and in vivo regulation of lipocalin-2, a novel adipokine, by insulin. Diabetes Care 2009, 32:129-131.
20. Bu D., Hemdahl A.-L., Gabrielsen A., Fuxe J., Zhu C., Eriksson P., Yan Z. Induction of neutrophil gelatinase-associated lipocalin in vascular injury via activation of nuclear factor-kappaB. Am J Pathol 2006, 169:2245-2253.
21. Seth P., Porter D., Lahti-Domenici J., Geng Y., Richardson A., Polyak K. Cellular and molecular targets of estrogen in normal human breast tissue. Cancer Res 2002, 62:4540-4544.
22. Bando M., Hiroshima Y., Kataoka M., Shinohara Y., Herzberg M.C., Ross K.F., Nagata T., Kido J. Interleukin-1alpha regulates antimicrobial peptide expression in human keratinocytes. Immunol Cell Biol 2007, 85:532-537.
23. Sørensen O.E., Cowland J.B., Theilgaard-Mönch K., Liu L., Ganz T., Borregaard N. Wound healing and expression of antimicrobial peptides/polypeptides in human keratinocytes, a consequence of common growth factors. J Immunol 2003, 170:5583-5589.
24. Ziegler S., Röhrs S., Tickenbrock L., Langerak A., Chu S.-T., Feldmann I., Jakubowski N., Müller O. Lipocalin 24p3 is regulated by the Wnt pathway independent of regulation by iron. Cancer Genet Cytogenet 2007, 174:16-23.
25. Hoette T.M., Abergel R.J., Xu J., Strong R.K., Raymond K.N. The role of electrostatics in siderophore recognition by the immunoprotein siderocalin. J Am Chem Soc 2008, 130:17584-17592.
26. Hoette T.M., Clifton M.C., Zawadzka A.M., Holmes M.A., Strong R.K., Raymond K.N. Immune interference in Mycobacterium tuberculosis intracellular iron acquisition through siderocalin recognition of carboxymycobactins. ACS Chem Biol 2011, 6:1327-1331.
27. Earhart C.F. Uptake and metabolism of iron and molybdenum. Escherichia coli and Salmonella: Cellular and Molecular Biology 1996, 1075-1090. ASM Press. F.C. Neidhardt (Ed.).
28. Hantke K., Nicholson G., Rabsch W., Winkelmann G. Salmochelins, siderophores of Salmonella enterica and uropathogenic Escherichia coli strains, are recognized by the outer membrane receptor IroN. Proc Natl Acad Sci U S A 2003, 100:3677-3682.
29. Abergel R.J., Wilson M.K., Arceneaux J.E.L., Hoette T.M., Strong R.K., Byers B.R., Raymond K.N. Anthrax pathogen evades the mammalian immune system through stealth siderophore production. Proc Natl Acad Sci U S A 2006, 103:18499-18503.
30. Abergel R.J., Zawadzka A.M., Raymond K.N. Petrobactin-mediated iron transport in pathogenic bacteria: coordination chemistry of an unusual 3,4-catecholate/citrate siderophore. J Am Chem Soc 2008, 130:2124-2125.
31. Yang J., Mori K., Li J.Y., Barasch J. Iron, lipocalin, and kidney epithelia. Am J Physiol Renal Physiol 2003, 285:F9-F18.
32. Correnti C., Richardson V., Sia A.K., Bandaranayake A.D., Ruiz M., Suryo Rahmanto Y., Kovačević Z., Clifton M.C., Holmes M.A., Kaiser B.K., et al. Siderocalin/Lcn2/NGAL/24p3 does not drive apoptosis through gentisic acid mediated iron withdrawal in hematopoietic cell lines. PLoS One 2012, 7:e43696.
33. Devireddy L.R., Hart D.O., Goetz D.H., Green M.R. A mammalian siderophore synthesized by an enzyme with a bacterial homolog involved in enterobactin production. Cell 2010, 141:1006-1017.
34. Yusifov T.N., Abduragimov A.R., Narsinh K., Gasymov O.K., Glasgow B.J. Tear lipocalin is the major endonuclease in tears. Mol Vis 2008, 14:180-188.
35. Wojnar P., van't Hof W., Merschak P., Lechner M., Redl B. The N-terminal part of recombinant human tear lipocalin/von Ebner's gland protein confers cysteine proteinase inhibition depending on the presence of the entire cystatin-like sequence motifs. Biol Chem 2001, 382:1515-1520.
36. van't Hof W., Blankenvoorde M.F., Veerman E.C., Amerongen A.V. The salivary lipocalin von Ebner's gland protein is a cysteine proteinase inhibitor. J Biol Chem 1997, 272:1837-1841.
37. Fluckinger M., Haas H., Merschak P., Glasgow B.J., Redl B. Human tear lipocalin exhibits antimicrobial activity by scavenging microbial siderophores. Antimicrob Agents Chemother 2004, 48:3367-3372.
38. Yusifov T.N., Abduragimov A.R., Gasymov O.K., Glasgow B.J. Endonuclease activity in lipocalins. Biochem J 2000, 347:815-819.
39. Dartt D.A. Tear lipocalin: structure and function. Ocul Surf 2011, 9:126-138.
40. Wojnar P., Dirnhofer S., Ladurner P., Berger P., Redl B. Human lipocalin-1, a physiological scavenger of lipophilic compounds, is produced by corticotrophs of the pituitary gland. J Histochem Cytochem 2002, 50:433-435.
41. Redl B. Human tear lipocalin. Biochim Biophys Acta 2000, 1482:241-248.
42. Holzfeind P., Merschak P., Rogatsch H., Culig Z., Feichtinger H., Klocker H., Redl B. Expression of the gene for tear lipocalin/von Ebner's gland protein in human prostate. FEBS Lett 1996, 395:95-98.
43. Breustedt D.A., Chatwell L., Skerra A. A new crystal form of human tear lipocalin reveals high flexibility in the loop region and induced fit in the ligand cavity. Acta Crystallogr D: Biol Crystallogr 2009, 65:1118-1125.
44. Gasymov O.K., Abduragimov A.R., Glasgow B.J. Intracavitary ligand distribution in tear lipocalin by site-directed tryptophan fluorescence. Biochemistry 2009, 48:7219-7228.
45. Glasgow B.J., Gasymov O.K. Focus on molecules: tear lipocalin. Exp Eye Res 2011, 92:242-243.
46. Descalzi Cancedda F., Manduca P., Tacchetti C., Fossa P., Quarto R., Cancedda R. Developmentally regulated synthesis of a low molecular weight protein (Ch 21) by differentiating chondrocytes. J Cell Biol 1988, 107:2455-2463.
47. Correnti C., Clifton M.C., Abergel R.J., Allred B., Hoette T.M., Ruiz M., Cancedda R., Raymond K.N., Descalzi F., Strong R.K. Galline Ex-FABP is an antibacterial siderocalin and a lysophosphatidic acid sensor functioning through dual ligand specificities. Structure 2011, 19:1796-1806.
48. Bojan B., Bischoff D., Nicholson G.J., Valdebenito M., Schneider K., Winkelmann G., Hantke K., Sussmuth R.D. The structure of salmochelins: C-glucosylated enterobactins of Salmonella enterica. Biometals 2004, 17:471-481.
49. Caza M., Lépine F., Dozois C.M. Secretion, but not overall synthesis, of catecholate siderophores contributes to virulence of extraintestinal pathogenic Escherichia coli. Mol Microbiol 2011, 80:266-282.
50. Caza M., Lépine F., Milot S., Dozois C.M. Specific roles of the iroBCDEN genes in virulence of an avian pathogenic Escherichia coli O78 strain and in production of salmochelins. Infect Immun 2008, 76:3539-3549.
51. Gao Q., Wang X., Xu H., Xu Y., Ling J., Zhang D., Gao S., Liu X. Roles of iron acquisition systems in virulence of extraintestinal pathogenic Escherichia coli: salmochelin and aerobactin contribute more to virulence than heme in a chicken infection model. BMC Microbiol 2012, 12:143.
52. Fricke W.F., McDermott P.F., Mammel M.K., Zhao S., Johnson T.J., Rasko D.A., Fedorka-Cray P.J., Pedroso A., Whichard J.M., Leclerc J.E., et al. Antimicrobial resistance-conferring plasmids with similarity to virulence plasmids from avian pathogenic Escherichia coli strains in Salmonella enterica serovar Kentucky isolates from poultry. Appl Environ Microbiol 2009, 75:5963-5971.
53. Guérin-Dubiard C., Pasco M., Mollé D., Désert C., Croguennec T., Nau F. Proteomic analysis of hen egg white. J Agric Food Chem 2006, 54:3901-3910.
54. Dozin B., Descalzi F., Briata L., Hayashi M., Gentili C., Hayashi K., Quarto R., Cancedda R. Expression, regulation, and tissue distribution of the Ch21 protein during chicken embryogenesis. J Biol Chem 1992, 267:2979-2985.
55. Cao Z., Han Z., Shao Y., Geng H., Kong X., Liu S. Proteomic analysis of chicken embryonic trachea and kidney tissues after infection in ovo by avian infectious bronchitis coronavirus. Proteome Sci 2011, 9:11.
56. Cermelli S., Zerega B., Carlevaro M., Gentili C., Thorp B., Farquharson C., Cancedda R., Cancedda F.D. Extracellular fatty acid binding protein (Ex-FABP) modulation by inflammatory agents: physiological acute phase response in endochondral bone formation. Eur J Cell Biol 2000, 79:155-164.
57. Gentili C., Tutolo G., Zerega B., Di Marco E., Cancedda R., Cancedda F.D. Acute phase lipocalin Ex-FABP is involved in heart development and cell survival. J Cell Physiol 2005, 202:683-689.
58. Descalzi Cancedda F., Dozin B., Zerega B., Cermelli S., Cancedda R. Ex-FABP: a fatty acid binding lipocalin developmentally regulated in chicken endochondral bone formation and myogenesis. Biochim Biophys Acta 2000, 1482:127-135.
59. Zhao Z., Zhang L., Du B., Cao N., Jiang X., Tian W., Li S., Wu W., Ye C. Polymorphisms in chicken extracellular fatty acid binding protein gene. Mol Biol Rep 2012, 39:2677-2682.
60. Hartl M., Matt T., Schüler W., Siemeister G., Kontaxis G., Kloiber K., Konrat R., Bister K. Cell transformation by the v-myc oncogene abrogates c-Myc/Max-mediated suppression of a C/EBP beta-dependent lipocalin gene. J Mol Biol 2003, 333:33-46.
61. Coudevylle N., Geist L., Hötzinger M., Hartl M., Kontaxis G., Bister K., Konrat R. The v-myc-induced Q83 lipocalin is a siderocalin. J Biol Chem 2010, 285:41646-41652.
62. Coudevylle N., Hoetzinger M., Geist L., Kontaxis G., Hartl M., Bister K., Konrat R. Lipocalin Q83 reveals a dual ligand binding mode with potential implications for the functions of siderocalins. Biochemistry 2011, 50:9192-9199.
63. Coudevylle N., Geist L., Hoetzinger M., Tollinger M., Konrat R. Siderocalin Q83 exhibits differential slow dynamics upon ligand binding. J Biomol NMR 2011, 51:83-88.