Enterobacter sakazakii targets DC-SIGN to induce immunosuppressive responses in dendritic cells by modulating MAPKs

Journal of Immunology

Volumn 183, Issue 10, 2009, Pages 6588-6599

  Mittal, Rahul ^a   Bulgheresi, Silvia ^c   Emami, Claudia ^a   Prasadarao, Nemani V ^a,b  

^a CHILDREN S HOSPITAL LOS ANGELES   (United States)

^b UNIVERSITY OF SOUTHERN CALIFORNIA   (United States)

^c UNIVERSITY OF VIENNA   (Austria)

Author keywords

[No Author keywords available]

Indexed keywords

CD209 ANTIGEN; MITOGEN ACTIVATED PROTEIN KINASE; OUTER MEMBRANE PROTEIN A;

ARTICLE; CELL INTERACTION; CELL MATURATION; CONTROLLED STUDY; CYTOKINE PRODUCTION; DENDRITIC CELL; ENTEROBACTER SAKAZAKII; HELA CELL; HOST PATHOGEN INTERACTION; HUMAN; HUMAN CELL; IMMUNE RESPONSE; IMMUNOMODULATION; INTESTINE EPITHELIUM CELL; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; T LYMPHOCYTE;

ANIMALS; ANTHRACENES; BACTERIAL OUTER MEMBRANE PROTEINS; BUTADIENES; CELL ADHESION MOLECULES; CELL SURVIVAL; DENDRITIC CELLS; ENTEROBACTER SAKAZAKII; ENTEROBACTERIACEAE INFECTIONS; ENZYME INHIBITORS; EPITHELIAL CELLS; FLAVONOIDS; HELA CELLS; HUMANS; IMIDAZOLES; INTERLEUKIN-10; LECTINS, C-TYPE; LIPOPOLYSACCHARIDES; LYMPHOCYTE ACTIVATION; MICROSCOPY, ELECTRON, SCANNING; MICROSCOPY, ELECTRON, TRANSMISSION; MITOGEN-ACTIVATED PROTEIN KINASE KINASES; NITRILES; PYRIDINES; RATS; RECEPTORS, CELL SURFACE; TRANSFECTION; TRANSFORMING GROWTH FACTOR BETA;

EID: 77954222908     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.0902029     Document Type: Article

References (67)

1. Friedemann, M. 2007. Enterobacter sakazakii in food and beverages (other than infant formula and milk powder). Int. J. Food. Microbiol. 116: 1-10.
2. Kim, H., Y. Lee, L. R. Beuchat, B. J. Yoon, and J. H. Ryu. 2009. Microbiological examination of vegetable seed sprouts in Korea. J. Food Prot. 72: 856-859.
3. Baumgartner, A., M. Grand, M. Liniger, and C. Iversen. 2009. Detection and frequency of Cronobacter spp. (Enterobacter sakazakii) in different categories of ready-to-eat foods other than infant formula. Int. J. Food Microbiol. In press.
4. Kandhai, M. C., M. W. Reij, L. G. Gorris, O. Guillaume-Gentil, and M. van Schothorst. 2004. Occurrence of Enterobacter sakazakii in food production environments and households. Lancet 363: 39-40.
5. Drudy, D., N. R. Mullane, T. Quinn, P. G. Wall, and S. Fanning. 2006. Enterobacter sakazakii: an emerging pathogen in powdered infant formula. Clin. Infect. Dis. 42: 996-1002.
6. Giovannini, M., E. Verduci, D. Ghisleni, E. Salvatici, E. Riva, and C. Agostoni. 2008. Enterobacter sakazakii: an emerging problem in paediatric nutrition. J. Int. Med. Res. 36: 394-399.
7. International Commission on Microbiological Specifications for Foods. 2002. Microorganisms in Food 7. Microbiological Testing in Food Safety Management. Kluwer Academic/Plenum Publishers: New York.
8. Riedel, K., and Lehner, A. 2007. Identification of proteins involved in osmotic stress response in Enterobacter sakazakii by proteomics. Proteomics 7: 1217-1231.
9. Hunter, C. J., M. Petrosyan, H. R. Ford, and N. V. Prasadarao. 2008. Enterobacter sakazakii: an emerging pathogen in infants and neonates. Surg. Infect. 9: 533-539.
10. Skovgaard, N. 2007. New trends in emerging pathogens. Int. J. Food Microbiol. 120: 217-224.
11. Mullane, N. R., C. Iversen, B. Healy, C. Walsh, P. Whyte, P. G. Wall, T. Quinn, and S. Fanning. 2007. Enterobacter sakazakii an emerging bacterial pathogen with implications for infant health. Minerva Pediatr. 59: 137-148.
12. Bowen, A. B., and C. R. Braden. 2006. Invasive Enterobacter sakazakii disease in infants. Emerg. Infect. Dis. 12: 1185-1189.
13. Willis, J., and J. E. Robinson. 1988. Enterobacter sakazakii meningitis in neonates. Pediatr. Infect. Dis. J. 7: 196-199.
14. Nazarowec-White, M., and J. M. Farber. 1997. Enterobacter sakazakii: a review. Int. J. Food Microbiol. 34: 103-113.
15. Mittal, R., Y. Wang, C. J. Hunter, I. Gonzalez-Gomez, and N. V. Prasadarao. 2009. Brain damage in newborn rat model of meningitis by Enterobacter sakazakii: a role for outer membrane protein A. Lab. Invest. 89: 263-277.
16. Hunter, C. J., M. Williams, M. Petrosyan, Y. Guner, R. Mittal, D. Mock, J. S. Upperman, H. R. Ford, and N. V. Prasadarao. 2009. Lactobacillus bulgaricus prevents intestinal epithelial cell injury caused by Enterobacter sakazakiiinduced nitric oxide both in vitro and in the newborn rat model of necrotizing enterocolitis. Infect. Immun. 77: 1031-1043.
17. Hunter, C. J., V. K. Singamsetty, N. K. Chokshi, P. Boyle, V. Camerini, A. V. Grishin, J. S. Upperman, H. R. Ford, and N. V. Prasadarao. 2008. Enterobacter sakazakii enhances epithelial cell injury by inducing apoptosis in a rat model of necrotizing enterocolitis. J. Infect. Dis. 198: 586-593.
18. Steinman, R. M. 2007. Dendritic cells: understanding immunogenicity. Eur. J. Immunol. 37(Suppl. 1): S53-S60.
19. Steinman, R. M., L. Bonifaz, S. Fujii, K. Liu, D. Bonnyay, S. Yamazaki, M. Pack, D. Hawiger, T. Iyoda, K. Inaba, and M. C. Nussenzweig. 2005. The innate functions of dendritic cells in peripheral lymphoid tissues. Adv. Exp. Med. Biol. 560: 83-97.
20. Rossi, M., and J. W. Young. 2005. Human dendritic cells: potent antigen-presenting cells at the crossroads of innate and adaptive immunity. J. Immunol. 175: 1373-1381.
21. Bousso, P. 2008. T cell activation by dendritic cells in the lymph node: lessons from the movies. Nat. Rev. Immunol. 8: 675-684.
22. Banchereau, J., and R. M. Steinman. 1998. Dendritic cells and the control of immunity. Nature 392: 245-252.
23. Steinman, R. M. 2003. Some interfaces of dendritic cell biology. APMIS 111: 675-697.
24. Banchereau, J., F. Briere, C. Caux, J. Davoust, S. Lebecque, Y. J. Liu, B. Pulendran, and K. Palucka. 2000. Immunobiology of dendritic cells. Annu. Rev. Immunol. 18: 767-811.
25. Moutaftsi, M., A. M. Mehl, L. K. Borysiewicz, and Z. Tabi. 2002. Human cytomegalovirus inhibits maturation and impairs function of monocyte-derived dendritic cells. Blood 99: 2913-2921.
26. Gelderblom, H. C., L. E. Nijhuis, E. C. de Jong, A. A. te Velde, D. Pajkrt, H. W. Reesink, M. G. Beld, S. J. van Deventer, and P. L. Jansen. 2007. Monocyte-derived dendritic cells from chronic HCV patients are not infected but show an immature phenotype and aberrant cytokine profile. Liver Int. 27: 944-953.
27. Bueno, S. M., J. A. Tobar, M. I. Iruretagoyena, and A. M. Kalergis. 2005. Molecular interactions between dendritic cells and Salmonella: escape from adaptive immunity and implications on pathogenesis. Crit. Rev. Immunol. 25: 389-403.
28. van Kooyk, Y. 2008. C-type lectins on dendritic cells: key modulators for the induction of immune responses. Biochem. Soc. Trans. 36: 1478-1481.
29. den Dunnen, J., S. I. Gringhuis, and T. B. Geijtenbeek. 2009. Innate signaling by the C-type lectin DC-SIGN dictates immune responses. Cancer Immunol. Immunother. 58: 1149-1157.
30. Zhou, T., Y. Chen, L. Hao, and Y. Zhang. 2006. DC-SIGN and immunoregulation. Cell. Mol. Immunol. 3: 279-283.
31. Geijtenbeek, T. B., and Y. van Kooyk. 2003. DC-SIGN: a novel HIV receptor on DCs that mediates HIV-1 transmission. Curr. Top. Microbiol. Immunol. 276: 31-54.
32. Wu, L., and V. N. KewalRamani. 2006. Dendritic-cell interactions with HIV: infection and viral dissemination. Nat. Rev. Immunol. 6: 859-868.
33. Yu Kimata, M. T., M. Cella, J. E. Biggins, C. Rorex, R. White, S. Hicks, J. M. Wilson, P. G. Patel, J. S. Allan, M. Colonna, and J. T. Kimata. 2002. Capture and transfer of simian immunodeficiency virus by macaque dendritic cells is enhanced by DC-SIGN. J. Virol. 76: 11827-11836.
34. Zhang, P., S. Snyder, P. Feng, P. Azadi, S. Zhang, S. Bulgheresi, K. E. Sanderson, J. He, J. Klena, and T. Chen. 2006. Role of N-acetylglucosamine within core lipopolysaccharide of several species of gram-negative bacteria in targeting the DC-SIGN (CD209). J. Immunol. 177: 4002-4011.
35. van Kooyk, Y., B. Appelmelk, and T. B. Geijtenbeek. 2003. A fatal attraction: Mycobacterium tuberculosis and HIV-1 target DC-SIGN to escape immune surveillance. Trends Mol. Med. 9: 153-159.
36. Tailleux, L., O. Schwartz, J. L. Herrmann, E. Pivert, M. Jackson, A. Amara, L. Legres, D. Dreher, L. P. Nicod, J. C. Gluckman, et al. 2003. DC-SIGN is the major Mycobacterium tuberculosis receptor on human dendritic cells. J. Exp. Med. 197: 121-127.
37. Cambi, A., K. Gijzen, J. M. de Vries, R. Torensma, B. Joosten, G. J. Adema, M. G. Netea, B. J. Kullberg, L. Romani, and C. G. Figdor. 2003. The C-type lectin DC-SIGN (CD209) is an antigen-uptake receptor for Candida albicans on dendritic cells. Eur. J. Immunol. 33: 532-538.
38. Zhang, P., M. Skurnik, S. S. Zhang, O. Schwartz, R. Kalyanasundaram, S. Bulgheresi, J. J. He, J. D. Klena, B. J. Hinnebusch, and T. Chen. 2008. Human dendritic cell-specific intercellular adhesion molecule-grabbing nonintegrin (CD209) is a receptor for Yersinia pestis that promotes phagocytosis by dendritic cells. Infect. Immun. 76: 2070-2079.
39. Zhang, P., O. Schwartz, M. Pantelic, G. Li, Q. Knazze, C. Nobile, M. Radovich, J. He, S. C. Hong, J. Klena, and T. Chen. 2006. DC-SIGN (CD209) recognition of Neisseria gonorrhoeae is circumvented by lipooligosaccharide variation. J. Leukocyte Biol. 79: 731-738.
40. Bulgheresi, S., I. Schabussova, T. Chen, N. P. Mullin, R. M. Maizels, and J. A. Ott. 2006. A new C-type lectin similar to the human immunoreceptor DCSIGN mediates symbiont acquisition by a marine nematode. Appl. Environ. Microbiol. 72: 2950-2956.
41. Pöhlmann, S., F. Baribaud, B. Lee, G. J. Leslie, M. D. Sanchez, K. Hiebenthal-Millow, J. Münch, F. Kirchhoff, and R. W. Doms. 2001. DC-SIGN interactions with human immunodeficiency virus type 1, type 2 and simian immunodeficiency virus. J. Virol. 75: 4664-4672.
42. Jameson, B., F. Baribaud, S. Pöhlmann, D. Ghavimi, F. Mortari, R. W. Doms, and A. Iwasaki. 2002. Expression of DC-SIGN by dendritic cells of intestinal and genital mucosae in humans and rhesus macaques. J. Virol. 76: 1866-1875.
43. Singamsetty, V. K., Y. Wang, H. Shimada, and N. V. Prasadarao. 2008. Outer membrane protein A expression in Enterobacter sakazakii is required to induce microtubule condensation in human brain microvascular endothelial cells for invasion. Microb. Pathog. 45: 181-191.
44. Dixon, G. L., P. J. Newton, B. M. Chain, D. Katz, S. R. Andersen, S. Wong, P. van der Ley, N. Klein, and R. E. Callard. 2001. Dendritic cell activation and cytokine production induced by group B Neisseria meningitidis: interleukin-12 production depends on lipopolysaccharide expression in intact bacteria. Infect. Immun. 69: 4351-4357.
45. Jones, H. E., H. Uronen-Hansson, R. E. Callard, N. Klein, and G. L. J. Dixon. 2007. The differential response of human dendritic cells to live and killed Neisseria meningitides. Cell. Microbiol. 9: 2856-2869.
46. Banks, K. E., T. L. Humphreys, W. Li, B. P. Katz, D. S. Wilkes, and S. M. Spinola. 2007. Haemophilus ducreyi partially activates human myeloid dendritic cells. Infect. Immun. 75: 5678-5685.
47. SolFoulon, N., A. Moris, C. Nobile, C. Boccaccio, A. Engering, J. P. Abastado, J. M. Heard, Y. van Kooyk, and O. Schwartz. 2002. HIV-1 Nef-induced upregulation of DC-SIGN in dendritic cells promotes lymphocyte clustering and viral spread. Immunity 16: 145-155.
48. Schulz, K. R., E. A. Danna, P. O. Krutzik, and G. P. Nolan. 2007. Single-cell phospho-protein analysis by flow cytometry. Curr. Protoc. Immunol. Chapter 8:Unit 8.17.
49. Krutzik, P. O., and G. P. Nolan. 2003. Intracellular phospho-protein staining techniques for flow cytometry: monitoring single cell signaling events. Cytometry A 55: 61-70.
50. Hanekom, W. A., M. Mendillo, C. Manca, P. A. Haslett, M. R. Siddiqui, C. Barry III, and G. Kaplan. 2003. Mycobacterium tuberculosis inhibits maturation of human monocyte-derived dendritic cells in vitro. J. Infect. Dis. 188: 257-266.
51. Kanof, M. E. 2001. Isolation of T cells using rosetting procedures. Curr. Protoc. Immunol. Chapter 7: Unit 7.2.
52. Sojka, D. K., C. A. Lazarski, Y. H. Huang, I. Bromberg, A. Hughson, and D. J. Fowell. 2009. Regulation of immunity at tissue sites of inflammation. Immunol. Res. In press.
53. Zou, G. M., and Y. K. Tam. 2002. Cytokines in the generation and maturation of dendritic cells: recent advances. Eur. Cytokine Netw. 13: 186-199.
54. Lukacs-Kornek, V., D. Engel, F. Tacke, and C. Kurts. 2008. The role of chemokines and their receptors in dendritic cell biology. Front. Biosci. 13: 2238-2252.
55. Nakahara, T., H. Uchi, K. Urabe, Q. Chen, M. Furue, and Y. Moroi. 2004. Role of c-Jun N-terminal kinase on lipopolysaccharide induced maturation of human monocyte-derived dendritic cells. Int. Immunol. 16: 1701-1709.
56. Arrighi, J. F., M. Rebsamen, F. Rousset, V. Kindler, and C. Hauser. 2001. A critical role for p38 mitogen-activated protein kinase in the maturation of human blood-derived dendritic cells induced by lipopolysaccharide, TNF-α, and contact sensitizers. J. Immunol. 166: 3837-3845.
57. Miyazawa, M., Y. Ito, N. Kosaka, Y. Nukada, H. Sakaguchi, H. Suzuki, and N. Nishiyama. 2008. Role of MAPK signaling pathway in the activation of dendritic type cell line, THP-1, induced by DNCB and NiSO4. J. Toxicol. Sci. 33: 51-59.
58. Aicher, A., G. Shu, D. Magaletti, T. Mulvania, A. Pezzutto, A. Craxton, and E. A. Clark. 1999. Differential role for p38 mitogen-activated protein kinase in regulating CD40-induced gene expression in dendritic cells and B cells. J. Immunol. 163: 5786-5795.
59. Koch, F., U. Stanzl, P. Jennewein, K. Janke, C. Heufler, E. Kämpgen, N. Romani, and G. Schuler. 1996. High level IL-12 production by murine dendritic cells: up-regulation via MHC class II and CD40 molecules and down-regulation by IL-4 and IL-10. J. Exp. Med. 184: 741-746.
60. Akbari, O., R. H. DeKruyff, and D. T. Umetsu. 2001. Pulmonary dendritic cells producing IL-10 mediate tolerance induced by respiratory exposure to antigen. Nat. Immunol. 2: 725-731.
61. Ding, L., and E. M. Shevach. 1992. IL-10 inhibits mitogen-induced T cell proliferation by selectively inhibiting macrophage costimulatory function. J. Immunol. 148: 3133-3139.
62. Park, S. M., H. S. Kim, J. Choe, and T. H. Lee. 1999. Differential induction of cytokines genes and activation of mitogen-activated protein kinase family by soluble CD40 ligand and TNF in a human follicular dendritic cell line. J. Immunol. 163: 631-638.
63. Mäkelä, S. M., M. Strengell, T. E. Pietilä, P. Osterlund, and I. Julkunen. 2009. Multiple signaling pathways contribute to synergistic TLR ligand-dependent cytokine gene expression in human monocyte-derived macrophages and dendritic cells. J. Leukocyte Biol. 85: 664-672.
64. Rincón, M., R. A. Flavell, and R. A. Davis. 2000. The JNK and P38 MAP kinase signaling pathways in T cell-mediated immune responses. Free Radic. Biol. Med. 28: 1328-1337.
65. Cuenda, A., and S. Rousseau. 2007. p38 MAP-kinases pathway regulation, function and role in human diseases. Biochim. Biophys. Acta 1773: 1358-1375.
66. Zhang, Y. L., and C. Dong. 2005. MAP kinases in immune responses. Cell. Mol. Immunol. 2: 20-27.
67. Dong, C., R. J. Davis, and R. A. Flavell. 2002. MAP kinases in the immune response. Annu. Rev. Immunol. 20: 55-72.