The human antimicrobial protein calgranulin C participates in control of helicobacter pylori growth and regulation of virulence

Infection and Immunity

Volumn 83, Issue 7, 2015, Pages 2944-2956

  Haley, Kathryn P ^b   Delgado, Alberto G ^b   Piazuelo, M Blanca ^b   Mortensen, Brittany L ^c   Correa, Pelayo ^b,c   Damo, Steven M ^b,c,d   Chazin, Walter J ^b,c   Skaar, Eric P ^a,c   Gaddy, Jennifer A ^a,b  

^a Veteran's Affairs Tennessee Valley Healthcare System   (United States)

^b VANDERBILT UNIVERSITY   (United States)

^c VANDERBILT UNIVERSITY SCHOOL OF MEDICINE   (United States)

^d FISK UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CALGRANULIN; CALGRANULIN A; CALGRANULIN B; CALGRANULIN C; INTERLEUKIN 8; PROTEIN S 100; UNCLASSIFIED DRUG; ZINC; S100A12 PROTEIN, HUMAN;

ARTICLE; BACTERIAL GROWTH; BACTERIAL VIRULENCE; BINDING AFFINITY; BIOGENESIS; CONTROLLED STUDY; FIELD EMISSION; HELICOBACTER INFECTION; HELICOBACTER PYLORI; HUMAN; HUMAN CELL; HUMAN TISSUE; IN VITRO STUDY; INFECTION; PHENOTYPE; PRIORITY JOURNAL; SCANNING ELECTRON MICROSCOPY; STOMACH BIOPSY; TYPE IV SECRETION SYSTEM; ADULT; BIOPSY; GROWTH, DEVELOPMENT AND AGING; IMMUNOLOGY; METABOLISM; MICROBIAL VIABILITY; MICROBIOLOGY; PATHOGENICITY; PATHOLOGY; PHYSIOLOGY; STOMACH MUCOSA; VIRULENCE;

ADULT; BIOPSY; GASTRIC MUCOSA; HELICOBACTER INFECTIONS; HELICOBACTER PYLORI; HUMANS; MICROBIAL VIABILITY; MICROSCOPY, ELECTRON, SCANNING; S100 PROTEINS; S100A12 PROTEIN; VIRULENCE; ZINC;

EID: 84930995029     PISSN: 00199567     EISSN: 10985522     Source Type: Journal    
DOI: 10.1128/IAI.00544-15     Document Type: Article

References (78)

1. Cover TL, Blaser MJ. 2009. Helicobacter pylori in health and disease. Gastroenterology 136:1863-1873. http://dx.doi.org/10.1053/j.gastro.2009.01.073.
2. Atherton J, Blaser MJ. 2009. Coadaptation of Helicobacter pylori and humans: ancient history, modern implications. J Clin Invest 119:2475- 2487. http://dx.doi.org/10.1172/JCI38605.
3. Algood HMS, Cover T. 2006. Helicobacter pylori persistence: an overview of interactions between H. pylori and host immune defenses. Clin Microbiol Rev 19:597-613. http://dx.doi.org/10.1128/CMR.00006-06.
4. Stolte M. 1992. Helicobacter pylori gastritis and gastric MALT-lymphoma. Lancet 339:745-746. http://dx.doi.org/10.1016/0140-6736(92)90645-J.
5. Ding SZ, Goldberg JB, Hatakeyama M. 2010. Helicobacter pylori infection, oncogenic pathways and epigenetic mechanisms in gastric carcinogenesis. Future Oncol 6:851-862. http://dx.doi.org/10.2217/fon.10.37.
6. Posselt G, Backert S, Wessler S. 2013. The functional interplay of Helicobacter pylori factors with gastric epithelial cells induces a multi-step process in pathogenesis. Cell Commun SIgnal 11:77. http://dx.doi.org/10.1186/1478-811X-11-77.
7. Sugiyama T, Asaka M. 2004. Helicobacter pylori infection and gastric cancer. Med Electron Microsc 37:149-157. http://dx.doi.org/10.1007/s00795-004-0250-7.
8. Stein M, Ruggiero P, Rappouli R, Bagnoli F. 2013. Helicobacter pylori CagA: from pathogenic mechanisms to use as an anti-cancer vaccine. Front Immunol 4:328. http://dx.doi.org/10.3389/fimmu.2013.00328.
9. Tan S, Noto JM, Romero-Gallo J, Peek RM, Jr, Amieva MR. 2011. Helicobacter pylori perturbs iron trafficking in the epithelium to grow on the cell surface. PLoS Pathog 7:e1002050. http://dx.doi.org/10.1371/journal.ppat.1002050.
10. Tummuru MK, Sharma SA, Blaser MJ. 1995. Helicobacter pylori picB, a homologue of the Bordetella pertussis toxin secretion protein is required for induction of IL-8 in gastric epithelial cells. Mol Microbiol 18:867-876. http://dx.doi.org/10.1111/j.1365-2958.1995.18050867.x.
11. Detmers PA, Lo SK, Olsen-Egbert E, Walz A, Baggiolini M, Cohn ZA. 1990. Neutrophil-activating protein 1/interlukin 8 stimulates the binding activity of the leukocyte adhesion receptor CD11b/CD18 on human neutrophils. J Exp Med 171:1155-1162. http://dx.doi.org/10.1084/jem.171.4.1155.
12. Mayadas TN, Cullerre X, Lowell CA. 2014. The multifaceted functions of neutrophils. Annu Rev Pathol 9:181-218. http://dx.doi.org/10.1146/annurev-pathol-020712-164023.
13. Fialkow L, Wang Y, Downey GP. 2007. Reactive oxygen and nitrogen species as signaling molecules regulating neutrophil function. Free Radic Biol Med 42:153-164. http://dx.doi.org/10.1016/j.freeradbiomed.2006.09.030.
14. Pietzsch J, Hoppmann S. 2009. Human S100A12: a novel key player in inflammation? Amino Acids 36:381-389. http://dx.doi.org/10.1007/s00726-008-0097-7.
15. Fritz G, Botelho HM, Morozova-Roche LA, Gomes CM. 2010. Natural and amyloid self-assembly of S100 proteins: structural basis for functional diversity. FEBS J 277:4578-4590. http://dx.doi.org/10.1111/j.1742-4658.2010.07887.x.
16. Sohnle PG, Hunter MJ, Hahn B, Chazin WJ. 2000. Zinc-reversible antimicrobial activity of recombinant calprotectin (migration inhibitory factor-related proteins 8 and 14). J Infect Dis 182:1272-1275. http://dx.doi.org/10.1086/315810.
17. Santamaria-Kisiel L, Rintala-Dempsey AC, Shaw GS. 2006. Calciumdependent and -independent interactions of the S100 protein family. Biochem J 396:201-214. http://dx.doi.org/10.1042/BJ20060195.
18. Diaz-Ochoa VE, Jellbauer S, Klaus S, Raffatellu M. 2014. Transition metal ions at the crossroads of mucosal immunology and microbial pathogenesis. Front Cell Infect Microbiol 4:2. http://dx.doi.org/10.3389/fcimb.2014.00002.
19. Corbin BD, Seeley EH, Raab A, Feldmann J, Miller MR, Torres VJ, Anderson KL, Dattilo BM, Dunman PM, Gerads R, Caprioli RM, Nacken W, Chazin WJ, Skaar EP. 2008. Metal chelation and inhibition of bacterial growth in tissue abscesses. Science 319:962-965. http://dx.doi.org/10.1126/science.1152449.
20. Damo S, Kehl-Fie TE, Sugitani N, Holt ME, Rathi S, Murphy WJ, Zhang Y, Betz C, Hench L, Fritz G, Skaar EP, Chazin WJ. 2013. Molecular basis for manganese sequestration by calprotectin and its role in the innate immune response to invading bacterial pathogens. Proc Natl Acad Sci U S A 110:3841-3846. http://dx.doi.org/10.1073/pnas.1220341110.
21. Hood MI, Mortensen BL, Moore JL, Zhang Y, Kehl-Fie TE, Sugitani N, Chazin WJ, Caprioli RM, Skaar EP. 2012. Identification of an Acinetobacter baumannii zinc acquisition system that facilitates resistance to calprotectin- mediated zinc sequestration. PLoS Pathog 8:e1003068. http://dx.doi.org/10.1371/journal.ppat.1003068.
22. Liu JZ, Jellbauer S, Poe AJ, Ton V, Pesciaroli M, Kehl-Fie TE, Restrepo NA, Hosking MP, Edwards RA, Battistoni A, Pasquali P, Lane TE, Chazin WJ, Vogl T, Roth J, Skaar EP, Raffatellu M. 2012. Zinc sequestration by the neutrophil protein calprotectin enhances Salmonella growth in the inflamed gut. Cell Host Microbe 11:227-239. http://dx.doi.org/10.1016/j.chom.2012.01.017.
23. Loomans HJ, Hahn BL, Li QQ, Phadnis SH, Sohnle PG. 1998. Histidinebased zinc-binding sequences and the antimicrobial activity of calprotectin. J Infect Dis 177:812-814. http://dx.doi.org/10.1086/517816.
24. Lusitani D, Malawista SE, Montgomery RR. 2003. Calprotectin, an abundant cytosolic protein from human polymorphonuclear leukocytes, inhibits the growth of Borrelia burgdorferi. Infect Immun 71:4711-4716. http://dx.doi.org/10.1128/IAI.71.8.4711-4716.2003.
25. Steinbakk M, Naess-Andresen CF, Lingaas E, Dale I, Brandtzaeg P, Fagerhol MK. 1990. Antimicrobial actions of calcium binding leucocyte L1 protein, calprotectin. Lancet 336:763-765. http://dx.doi.org/10.1016/0140-6736(90)93237-J.
26. Zaia AA, Sappington KJ, Nisapakultorn K, Chazin WJ, Dietrich EA, Ross KF, Herzberg MC. 2009. Subversion of antimicrobial calprotectin (S100A8/S100A9 complex) in the cytoplasm of TR146 epithelial cells after invasion by Listeria monocytogenes. Mucosal Immunol 2:43-53. http://dx.doi.org/10.1038/mi.2008.63.
27. Gaddy JA, Radin JN, Loh JT, Piazuelo MB, Kehl-Fie TE, Delgado AG, Ilca FT, Peek RM, Cover TL, Chazin WJ, Skaar EP, Scott Algood HM. 2014. The host protein calprotectin modulates the Helicobacter pylori cag type IV secretion system via zinc sequestration. PLoS Pathog 10:e1004450. http://dx.doi.org/10.1371/journal.ppat.1004450.
28. Leach ST, Mitchell HM, Geczy CL, Sherman PM, Day AS. 2008. S100 calgranulin proteins S100A8, S100A9 and S100A12 are expressed in the inflamed gastric mucosa of Helicobacter pylori-infected children. Can J Gastroenterol 22:461-464.
29. van de Logt F, Day AS. 2013. S100A12: a noninvasive marker of inflammation in inflammatory bowel disease. J Dig Dis 14:62-67. http://dx.doi.org/10.1111/1751-2980.12012.
30. Goyette J, Geczy CL. 2011. Inflammation-associated S100 proteins: new mechanisms that regulate function. Amino Acids 41:821-842. http://dx.doi.org/10.1007/s00726-010-0528-0.
31. Kehl-Fie TE, Chitayat S, Hood MI, Damo S, Restrepo N, Garcia C, Munro KA, Chazin WJ, Skaar EP. 2011. Nutrient metal sequestration by calprotectin inhibits bacterial superoxide defense, enhancing neutrophil killing of Staphylococcus aureus. Cell Host Microbe 10:158-164. http://dx.doi.org/10.1016/j.chom.2011.07.004.
32. Hunter MJ, Chazin WJ. 1998. High level expression and dimer characterization of the S100 EF-hand proteins, migration inhibitory factorrelated proteins 8 and 14. J Biol Chem 273:12427-12435. http://dx.doi.org/10.1074/jbc.273.20.12427.
33. Zabaleta J, Camargo MC, Ritchie MD, Piazuelo MB, Sierra RA, Turner SD, Delgado A, Fontham ET, Schneider BG, Correa P, Ochoa AC. 2011. Association of haplotypes of inflammation-related genes with gastric preneoplastic lesions in African Americans and Caucasians. Int J Cancer 128: 668-675. http://dx.doi.org/10.1002/ijc.25385.
34. Loh JT, Friedman DB, Piazuelo MB, Bravo LE, Wilson KT, Peek RM, Jr, Correa P, Cover TL. 2012. Analysis of Helicobacter pylori cagA promoter elements required for salt-induced upregulation of CagA expression. Infect Immun 80:3094-3106. http://dx.doi.org/10.1128/IAI.00232-12.
35. Akpek EK, Liu SH, Thompson R, Gottsch JD. 2002. Identification of paramyosin as a binding protein for calgranulin C in experimental helminthic keratitis. Invest Ophthalmol Vis Sci 43:2677-2684.
36. Moroz OV, Blagova EV, Wilkinson AJ, Wilson KS, Bronstein IB. 2009. The crystal structures of human S100A12 in apo form and in complex with zinc: new insights into S100A12 oligomerisation. J Mol Biol 391:536-551. http://dx.doi.org/10.1016/j.jmb.2009.06.004.
37. Shaffer CL, Gaddy JA, Loh JT, Johnson EM, Hill S, Hennig EE, McClain MS, McDonald WH, Cover TL. 2011. Helicobacter pylori exploits a unique repertoire of type IV secretion system components for pilus assembly at the bacteria-host cell interface. PLoS Pathog 7:e1002237. http://dx.doi.org/10.1371/journal.ppat.1002237.
38. Loh JT, Torres VJ, Cover TL. 2007. Regulation of Helicobacter pylori cagA expression in response to salt. Cancer Res 67:4709-4715. http://dx.doi.org/10.1158/0008-5472.CAN-06-4746.
39. Backert S, Moese S, Selbach M, Brinkmann V, Meyer TF. 2001. Phosphorylation of tyrosine 972 of the Helicobacter pylori CagA protein is essential for induction of a scattering phenotype in gastric epithelial cells. Mol Microbiol 42:631-644.
40. Foell D, Wittkowski H, Vogl T, Roth J. 2007. S100 proteins expressed in phagocytes: a novel group of damage-associated molecular pattern molecules. J Leukoc Biol 81:28-37.
41. van Zoelen MA, Achouiti A, van der Poll T. 2011. The role of receptor for advanced glycation end products (RAGE) in infection. Crit Care 15: 208. http://dx.doi.org/10.1186/cc9990.
42. Kang JH, Hwang SM, Chung IY. 2015. S100A8, S100A9, and S100A12 activate airway epithelial cells to produce MUC5AC via ERK and NF-κB pathways. Immunology 144:79 -90. http://dx.doi.org/10.1111/imm.12352.
43. Foell D, Wittkowski H, Kessel C, Lüken A, Weinhage T, Varga G, Vogl T, Wirth T, Viemann D, Björk P, van Zoelen MA, Gohar F, Srikrishna G, Kraft M, Roth J. 2013. Proinflammatory S100A12 can activate human monocytes via Toll-like receptor 4. Am J Respir Crit Care Med 187:1324- 1334. http://dx.doi.org/10.1164/rccm.201209-1602OC.
44. Fagerhol MK, Dale I, Anderson T. 1980. Release and quantitation of a leucocyte derived protein. Scand J Haematol 24:393-398.
45. Nakashima E, Okano Y, Niimi K, Takahashi E. 2013. Detection of calprotectin and apoptotic activity in the colon of marmosets with chronic diarrhea. J Vet Med Sci 75:1633-1636. http://dx.doi.org/10.1292/jvms.13-0257.
46. Sidler MA, Leach ST, Day AS. 2008. Fecal S100A12 and fecal calprotectin as noninvasive markers for inflammatory bowel disease in children. Inflamm Bowel Dis 14:359-366. http://dx.doi.org/10.1002/ibd.20336.
47. Burri E, Beglinger C. 2014. The use of fecal calprotectin as a biomarker in gastrointestinal disease. Expert Rev Gastroenterol Hepatol 8:197-210. http://dx.doi.org/10.1586/17474124.2014.869476.
48. Kaiser T, Langhorst J, Wittkowski H, Becker K, Friedrich AW, Rueffer A, Dobos GJ, Roth J, Foell D. 2007. Faecal S100A12 as a non-invasive marker distinguishing inflammatory bowel disease from irritable bowel syndrome. Gut 56:1706 -1713. http://dx.doi.org/10.1136/gut.2006.113431.
49. Sun B, Karin M. 2014. The therapeutic value of targeting inflammation in gastrointestinal cancers. Trends Phamacol Sci 35:349-357. http://dx.doi.org/10.1016/j.tips.2014.04.011.
50. Karl J, Wild N, Tacke M, Andres H, Garczarek U, Rollinger W, Zolg W. 2008. Improved diagnosis of colorectal cancer using a combination of fecal occult blood and novel fecal protein markers. Clin Gastroenterol Hepatol 6:1122-1128. http://dx.doi.org/10.1016/j.cgh.2008.04.021.
51. Ferrer A, Ollila J, Tobin G, Nagy B, Thunberg U, Aalto Y, Vihinen M, Vilpo J, Rosenquist R, Knuutila S. 2004. Different gene expression in immunoglobulin-mutated and immunoglobulin-unmutated forms of chronic lymphocytic leukemia. Cancer Genet Cytogenet 153:69-72. http://dx.doi.org/10.1016/j.cancergencyto.2003.12.016.
52. Niini T, Vettenranta K, Hollmén J, Larramendy ML, Aalto Y, Wikman H, Nagy B, Seppänen JK, Ferrer Salvador A, Mannila H, Saarinen- Pihkala UM, Knuutila S. 2002. Expression of myeloid-specific genes in childhood acute lymphoblastic leukemia-a cDNA array study. Leukemia 16:2213-2221. http://dx.doi.org/10.1038/sj.leu.2402685.
53. Huang X, Zeng Y, Xing X, Zeng J, Gao Y, Cai Z, Xu B, Liu X, Huang A, Liu J. 2014. Quantitative proteomics analysis of early recurrence/ metastasis of huge hepatocellular carcinoma following radical resection. Proteome Sci 12:22. http://dx.doi.org/10.1186/1477-5956-12-22.
54. Ning X, Sun S, Hong L, Liang J, Liu L, Han S, Liu Z, Shi Y, Li Y, Gong W, Zhang S, Chen Y, Guo X, Cheng Y, Wu K, Fan D. 2007. Calcyclinbinding protein inhibits proliferation, tumorigenicity, and invasion of gastric cancer. Mol Cancer Res 5:1254-1262. http://dx.doi.org/10.1158/1541-7786.MCR-06-0426.
55. Franco AT, Johnston E, Krishna U, Yamaoka Y, Israel DA, Nagy TA, Wroblewski LE, Piazuelo MB, Correa P, Peek RM, Jr. 2008. Regulation of gastric carcinogenesis by Helicobacter pylori virulence factors. Cancer Res 68:379-387. http://dx.doi.org/10.1158/0008-5472.CAN-07-0824.
56. Cole AM, Kim YH, Tahk S, Hong T, Weis P, Waring AJ, Ganz T. 2001. Calcitermin, a novel antimicrobial peptide isolated from human airway secretions. FEBS Lett 504:5-10. http://dx.doi.org/10.1016/S0014-5793(01)02731-4.
57. Brenaut P, Lefèvre L, Rau A, Laloë D, Pisoni G, Moroni P, Bevilacqua C, Martin P. 2014. Contribution of mammary epithelial cells to the immune response during early stages of a bacterial infection to Staphylococcus aureus. Vet Res 45:16. http://dx.doi.org/10.1186/1297-9716-45-16.
58. Mitterhuemer S, Petzl W, Krebs S, Mehne D, Klanner A, Wolf E, Zerbe H, Blum H. 2010. Escherichia coli infection induces distinct local and systemic transcriptome responses in the mammary gland.BMCGenomics 11:138. http://dx.doi.org/10.1186/1471-2164-11-138.
59. Liu K, Pichichero ME. 2012. Clinical significance of serum S100A12 in acute otitis media in young children. Pediatr Infect Dis J 31:56-58. http://dx.doi.org/10.1097/INF.0b013e31824672cb.
60. Achouiti A, Föll D, Vogl T, van Till JW, Laterre PF, Dugernier T, Wittebole X, Boermeester MA, Roth J, van der Poll T, van Zoelen MA. 2013. S100A12 and soluble receptor for advanced glycation end products levels during human severe sepsis. Shock 40:188-194. http://dx.doi.org/10.1097/SHK.0b013e31829fbc38.
61. Däbritz J, Jenke A, Wirth S, Foell D. 2012. Fecal phagocyte-specific S100A12 for diagnosing necrotizing enterocolitis. J Pediatr 161:1059- 1064. http://dx.doi.org/10.1016/j.jpeds.2012.06.003.
62. Jenke AC, Postberg J, Mariel B, Hensel K, Foell D, Däbritz J, Wirth S. 2013. S100A12 and hBD2 correlate with the composition of the fecal microflora in ELBW infants and expansion of E. coli is associated with NEC. Biomed. Res Int 2013:150372. http://dx.doi.org/10.1155/2013/150372.
63. Reis RA, Bortot LO, Caliri A. 2014. In silico assessment of S100A12 monomer and dimer structural dynamics: implications for the understanding of its metal-induced conformational changes. J Biol. Inorg Chem 19:1113-1120. http://dx.doi.org/10.1007/s00775-014-1149-y.
64. Moroz OV, Antson AA, Grist SJ, Maitland NJ, Dodson GG, Wilson KS, Lukanidin E, Bronstein IB. 2003. Structure of the human S100A12- copper complex: implications for host-parasite defence. Acta Crystallogr D Biol Crystallogr 59:859-867. http://dx.doi.org/10.1107/S0907444903004700.
65. Moroz OV, Burkitt W, Wittkowski H, He W, Ianoul A, Novitskaya V, Xie J, Polyakova O, Lednev IK, Shekhtman A, Derrick PJ, Bjoerk P, Foell D, Bronstein IB. 2009. Both Ca2+ and Zn2+ are essential for S100A12 protein oligomerization and function. BMC Biochem 10:11. http://dx.doi.org/10.1186/1471-2091-10-11.
66. Dell'Angelica EC, Schleicher CH, Santomé JA. 1994. Primary structure and binding properties of calgranulin C, a novel S100-like calciumbinding protein from pig granulocytes. J Biol Chem 269:28929-28936.
67. Wilkie-Grantham RP, Magon NJ, Harwood T, Kettle AJ, Vissers MC, Winterbourn CC, Hampton MB. 2015. Myeloperoxidase-dependent lipid peroxidation promotes the oxidative modification of cytosolic proteins in phagocytic neutrophils. J Biol Chem 290:9896-9905. http://dx.doi.org/10.1074/jbc.M114.613422.
68. Testerman TL, Conn PB, Mobley HL, McGee DJ. 2006. Nutritional requirements and antibiotic resistance patterns of Helicobacter species in chemically defined media. J Clin Microbiol 44:1650-1658. http://dx.doi.org/10.1128/JCM.44.5.1650-1658.2006.
69. Fuellen G, Foell D, Nacken W, Sorg C, Kerkhoff C. 2003. Absence of S100A12 in mouse: implications for RAGE-S100A12 interaction. Trends Immunol 24:622-624. http://dx.doi.org/10.1016/j.it.2003.10.004.
70. Becker KW, Skaar EP. 2014. Metal limitation and toxicity at the interface between host and pathogen. FEMS Microbiol Rev 38:1235-1249. http://dx.doi.org/10.1111/1574-6976.12087.
71. Gielda LM, DiRita VJ. 2012. Zinc competition among the intestinal microbiota. mBio 3:e00171-12. http://dx.doi.org/10.1128/mBio.00171-12.
72. Medeiros P, Bolick DT, Roche JK, Noronha F, Pinheiro C, Kolling GL, Lima A, Guerrant RL. 2013. The micronutrient zinc inhibits EAEC strain 042 adherence, biofilm formation, virulence gene expression, and epithelial cytokine responses benefiting the infected host. Virulence 4:624-633. http://dx.doi.org/10.4161/viru.26120.
73. Serafini A, Pisu D, Palù G, Rodriguez GM, Manganelli R. 2013. The ESX-3 secretion system is necessary for iron and zinc homeostasis in Mycobacterium tuberculosis. PLoS One 8:e78351. http://dx.doi.org/10.1371/journal.pone.0078351.
74. Rybniker J, Chen JM, Sala C, Hartkoorn RC, Vocat A, Benjak A, Boy-Röttger S, Zhang M, Székely R, Greff Z, Orfi L, Szabadkai I, Pató J, Kéri G, Cole ST. 2014. Anticytolytic screen identifies inhibitors of mycobacterial virulence protein secretion. Cell Host Microbe 16:538-548. http://dx.doi.org/10.1016/j.chom.2014.09.008.
75. Gal-Mor O, Gibson DL, Baluta D, Vallance BA, Finlay BB. 2008. A novel secretion pathway of Salmonella enterica acts as an antivirulence modulator during salmonellosis. PLoS Pathog 4:e1000036. http://dx.doi.org/10.1371/journal.ppat.1000036.
76. Mellies JL, Thomas K, Turvey M, Evans NR, Crane J, Boedeker E, Benison GC. 2012. Zinc-induced envelope stress diminishes type III secretion in enteropathogenic Escherichia coli. BMC Microbiol 12:123. http://dx.doi.org/10.1186/1471-2180-12-123.
77. Burtnick MN, Brett PJ. 2013. Burkholderia mallei and Burkholderia pseudomallei cluster 1 type VI secretion system gene expression is negatively regulated by iron and zinc. PLoS One 8:e76767. http://dx.doi.org/10.1371/journal.pone.0076767.
78. Prehna G, Li Y, Stoynov N, Okon M, Vuckovic M, McIntosh LP, Foster LJ, Finlay BB, Strynadka NC. 2012. The zinc regulated antivirulence pathway of Salmonella is a multiprotein immunoglobulin adhesion system. J Biol Chem 287:32324-32337. http://dx.doi.org/10.1074/jbc.M112.357210.