Fcγ receptor i alpha chain (CD64) expression in macrophages is critical for the onset of meningitis by Escherichia coli K1

PLoS Pathogens

Volumn 6, Issue 11, 2010, Pages

  Mittal, Rahul ^a   Sukumaran, Sunil K ^a   Selvaraj, Suresh K ^a   Wooster, David G ^a   Madan Babu, M ^b   Schreiber, Alan D ^c   Sjef Verbeek, J ^d   Prasadarao, Nemani V ^a,e  

^a CHILDREN S HOSPITAL LOS ANGELES   (United States)

^b MRC LABORATORY OF MOLECULAR BIOLOGY   (United Kingdom)

^c UNIVERSITY OF PENNSYLVANIA   (United States)

^d LEIDEN UNIVERSITY MEDICAL CENTER   (Netherlands)

^e UNIVERSITY OF SOUTHERN CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CD64 ANTIGEN; COMPLEMENT RECEPTOR; IMMUNOGLOBULIN G; IMMUNOGLOBULIN G2A; OUTER MEMBRANE PROTEIN A; CD11B ANTIGEN; FC RECEPTOR; MESSENGER RNA; NITRIC OXIDE; OMPA OUTER MEMBRANE PROTEINS; OUTER MEMBRANE PROTEIN;

ADOPTIVE TRANSFER; ALPHA CHAIN; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIGEN EXPRESSION; ARTICLE; BACTERIAL CLEARANCE; BACTERIAL MENINGITIS; BACTERIAL SURVIVAL; CARBOXY TERMINAL SEQUENCE; CELL STRAIN COS1; CONTROLLED STUDY; ESCHERICHIA COLI; ESCHERICHIA COLI K1; GENE OVEREXPRESSION; HUMAN; HUMAN CELL; IN VITRO STUDY; INFECTION RESISTANCE; INFECTION SENSITIVITY; MOUSE; NEWBORN; NONHUMAN; OPSONIZATION; PERITONEUM MACROPHAGE; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; ANIMAL; BINDING COMPETITION; BRAIN; C57BL MOUSE; CERCOPITHECUS; FLOW CYTOMETRY; GENETICS; GROWTH, DEVELOPMENT AND AGING; IMMUNOLOGY; IMMUNOPRECIPITATION; MACROPHAGE; METABOLISM; MICROBIOLOGY; MOUSE MUTANT; PATHOGENICITY; PATHOLOGY; PHAGOCYTOSIS; PHOSPHORYLATION; PHYSIOLOGY; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; WESTERN BLOTTING;

ANIMALIA; BACTERIA (MICROORGANISMS); ESCHERICHIA COLI; MUS;

ANIMALS; ANIMALS, NEWBORN; BACTERIAL OUTER MEMBRANE PROTEINS; BINDING, COMPETITIVE; BLOTTING, WESTERN; BRAIN; CERCOPITHECUS AETHIOPS; COS CELLS; ESCHERICHIA COLI; FLOW CYTOMETRY; HUMANS; IMMUNOGLOBULIN G; IMMUNOPRECIPITATION; MACROPHAGE-1 ANTIGEN; MACROPHAGES; MENINGITIS, ESCHERICHIA COLI; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; NITRIC OXIDE; PHAGOCYTOSIS; PHOSPHORYLATION; RECEPTORS, IGG; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, MESSENGER;

EID: 79251509551     PISSN: 15537366     EISSN: 15537374     Source Type: Journal    
DOI: 10.1371/journal.ppat.1001203     Document Type: Article

References (73)

1. Hornef MW, Wick MJ, Rhen M, Normark S (2002) Bacterial strategies for overcoming host innate and adaptive immune responses. Nat Immunol 3: 1033-1040.
2. Sansonetti PJ (2000) Phagocytosis, a cell biology view. J Cell Sci 113: 3355-3356.
3. Underhill DM, Ozinsky A (2002) Phagocytosis of microbes: complexity in action. Annu Rev Immunol 20: 825-852.
4. Koedel U, Pfister HW (1999) Models of experimental bacterial meningitis. Role and limitations. Infect Dis Clin North Am 13: 549-577.
5. Leib SL, Tauber MG (1999) Pathogenesis of bacterial meningitis. Infect Dis Clin North Am 13: 527-548.
6. Pong A, Bradley JS (1999) Bacterial meningitis and the newborn infant. Infect Dis Clin North Am 13: 711-733.
7. Stoll BJ, Hansen N, Fanaroff AA, Wright LL, Carlo WA, et al. (2002) Changes in pathogens causing early-onset sepsis in very-low-birth-weight infants. N Engl J Med 347: 240-247.
8. Dubois D, Prasadarao NV, Mittal R, Bret L, Roujou-Gris M, et al. (2009) CTXM beta-lactamase production and virulence of Escherichia coli K1. Emerg Infect Dis 15: 1988-1990.
9. Prasadarao NV, Blom AM, Villoutreix BO, Linsangan LC (2002) A novel interaction of outer membrane protein A with C4b binding protein mediates serum resistance of Escherichia coli K1. J Immunol 169: 6352-6360.
10. Wooster DG, Maruvada R, Blom AM, Prasadarao NV (2006) Logarithmic phase Escherichia coli K1 efficiently avoids serum killing by promoting C4bpmediated C3b and C4b degradation. Immunology 117: 482-493.
11. Maruvada R, Blom AM, Prasadarao NV (2008) Effects of complement regulators bound to Escherichia coli K1 and Group B Streptococcus on the interaction with host cells. Immunology 124: 265-276.
12. Dale DC, Boxer L, Liles WC (2008) The phagocytes: neutrophils and monocytes. Blood 112: 935-945.
13. Mukhopadhyay S, Pluddemann A, Gordon S (2009) Macrophage pattern recognition receptors in immunity, homeostasis and self tolerance. Adv Exp Med Biol 653: 1-14.
14. Sukumaran SK, Shimada H, Prasadarao NV (2003) Entry and intracellular replication of Escherichia coli K1 in macrophages require expression of outer membrane protein A. Infect Immun 71: 5951-5961.
15. Barth E, Fischer G, Schneider EM, Wollmeyer J, Georgieff M, et al. (2001) Differences in the expression of CD64 and mCD14 on polymorphonuclear cells and on monocytes in patients with septic shock. Cytokine 14: 299-302.
16. Brandtzaeg P, van Deuren M (2002) Current concepts in the role of the host response in Neisseria meningitidis septic shock. Curr Opin Infect Dis 15: 247-252.
17. Hoffmann JJ (2009) Neutrophil CD64: a diagnostic marker for infection and sepsis. Clin Chem Lab Med 47: 903-916.
18. Amigorena S, Bonnerot C (1999) Fc receptor signaling and trafficking: a connection for antigen processing. Immunol Rev 172: 279-284.
19. Gessner JE, Heiken H, Tamm A, Schmidt RE (1998) The IgG Fc receptor family. Ann Hematol 76: 231-248.
20. Isakov N (1997) ITIMs and ITAMs. The Yin and Yang of antigen and Fc receptor-linked signaling machinery. Immunol Res 16: 85-100.
21. McKenzie SE, Schreiber AD (1998) Fc gamma receptors in phagocytes. Curr Opin Hematol 5: 16-21.
22. Raghavan M, Bjorkman PJ (1996) Fc receptors and their interactions with immunoglobulins. Annu Rev Cell Dev Biol 12: 181-220.
23. Ravetch JV (1997) Fc receptors. Curr Opin Immunol 9: 121-125.
24. Indik ZK, Park JG, Hunter S, Schreiber AD (1995) Structure/function relationships of Fc gamma receptors in phagocytosis. Semin Immunol 7: 45-54.
25. Beekman JM, Bakema JE, van de Winkel JG, Leusen JH (2004) Direct interaction between FcgammaRI (CD64) and periplakin controls receptor endocytosis and ligand binding capacity. Proc Natl Acad Sci U S A 101: 10392-10397.
26. Beekman JM, Bakema JE, van der Linden J, Tops B, Hinten M, et al. (2004) Modulation of FcgammaRI (CD64) ligand binding by blocking peptides of periplakin. J Biol Chem 279: 33875-33881.
27. Goldmann O, Rohde M, Chhatwal GS, Medina E (2004) Role of macrophages in host resistance to group A streptococci. Infect Immun 72: 2956-2963.
28. Mittal R, Gonzalez-Gomez I, Goth KA, Prasadarao NV (2010) Inhibition of inducible nitric oxide controls pathogen load and brain damage by enhancing phagocytosis of Escherichia coli K1 in neonatal meningitis. Am J Pathol 176: 1292-305.
29. Thomson AW, Fowler EF (1981) Carrageenan: a review of its effects on the immune system. Agents Actions 11: 265-273.
30. Loike JD, Silverstein SC (1983) A fluorescence quenching technique using trypan blue to differentiate between attached and ingested glutaraldehyde-fixed red blood cells in phagocytosing murine macrophages. J Immunol Methods 57: 373-379.
31. Antal JM, Cunningham JV, Goodrum KJ (1992) Opsonin-independent phagocytosis of group B streptococci: role of complement receptor type three. Infect Immun 60: 1114-1121.
32. Goodrum KJ, McCormick LL, Schneider B (1994) Group B streptococcus-induced nitric oxide production in murine macrophages is CR3 (CD11b/CD18) dependent. Infect Immun 62: 3102-3107.
33. Noel GJ, Katz SL, Edelson PJ (1991) The role of C3 in mediating binding and ingestion of group B streptococcus serotype III by murine macrophages. Pediatr Res 30: 118-123.
34. Prasadarao NV, Wass CA, Weiser JN, Stins MF, Huang SH, et al. (1996) Outer membrane protein A of Escherichia coli contributes to invasion of brain microvascular endothelial cells. Infect Immun 64: 146-153.
35. Drevets DA, Leenen PJ, Campbell PA (1993) Complement receptor type 3 (CD11b/CD18) involvement is essential for killing of Listeria monocytogenes by mouse macrophages. J Immunol 151: 5431-5439.
36. Gafa V, Manches O, Pastor A, Drouet E, Ambroise-Thomas P, et al. (2005) Human cytomegalovirus downregulates complement receptors (CR3, CR4) and decreases phagocytosis by macrophages. J Med Virol 76: 361-366.
37. Drevets DA, Leenen PJ, Campbell PA (1996) Complement receptor type 3 mediates phagocytosis and killing of Listeria monocytogenes by a TNF-alpha- and IFN-gamma-stimulated macrophage precursor hybrid. Cell Immunol 169: 1-6.
38. Mosser D (1994) Receptors on phagocytic cells involved in microbial recognition. Immunol Ser 60: 99-114.
39. Watanabe I, Ichiki M, Shiratsuchi A, Nakanishi Y (2007) TLR2-mediated survival of Staphylococcus aureus in macrophages: a novel bacterial strategy against host innate immunity. J Immunol 178: 4917-4925.
40. Taylor PR, Martinez-Pomares L, Stacey M, Lin HH, Brown GD, et al. (2005) Macrophage receptors and immune recognition. Annu Rev Immunol 23: 901-944.
41. Weiss DJ, Souza CD, Evanson OA, Sanders M, Rutherford M (2008) Bovine monocyte TLR2 receptors differentially regulate the intracellular fate of Mycobacterium avium subsp. paratuberculosis and Mycobacterium avium subsp. avium. J Leukoc Biol 83: 48-55.
42. Higgins SC, Jarnicki AG, Lavelle EC, Mills KH (2006) TLR4 mediates vaccineinduced protective cellular immunity to Bordetella pertussis: role of IL-17- producing T cells. J Immunol 177: 7980-7989.
43. Diacovich L, Gorvel JP (2010) Bacterial manipulation of innate immunity to promote infection. Nat Rev Microbiol 8: 117-128.
44. Aderem A, Underhill DM (1999) Mechanisms of phagocytosis in macrophages. Annu Rev Immunol 17: 593-623.
45. Flannagan RS, Cosío G, Grinstein S (2009) Antimicrobial mechanisms of phagocytes and bacterial evasion strategies. Nat Rev Microbiol 7: 355-366.
46. Lam GY, Brumell JH (2008) Cell biology: A Listeria escape trick. Nature 455: 1186-1187.
47. Sjodahl J (1977) Structural studies on the four repetitive Fc-binding regions in protein A from Staphylococcus aureus. Eur J Biochem 78: 471-490.
48. Sulica A, Medesan C, Laky M, Onica D, Sjoquist J, et al. (1979) Effect of protein A of Staphylococcus aureus on the binding of monomeric and polymeric IgG to Fc receptor-bearing cells. Immunology 38: 173-179.
49. Wang Y (2002) The function of OmpA in Escherichia coli. Biochem Biophys Res Commun 292: 396-401.
50. Smith SG, Mahon V, Lambert MA, Fagan RP (2007) A molecular Swiss army knife: OmpA structure, function and expression. FEMS Microbiol Lett 273: 1-11.
51. Celli J, Finlay BB (2002) Bacterial avoidance of phagocytosis. Trends Microbiol 10: 232-237.
52. Ernst JD (2000) Bacterial inhibition of phagocytosis. Cell Microbiol 2: 379-386.
53. Rosenberger CM, Finlay BB (2003) Phagocyte sabotage: disruption of macrophage signalling by bacterial pathogens. Nat Rev Mol Cell Biol 4: 385-396.
54. Taylor PR, Martinez-Pomares L, Stacey M, Lin HH, Brown GD, et al. (2005) Macrophage receptors and immune recognition. Annu Rev Immunol 23: 901-944.
55. Kumar H, Kawai T, Akira S (2009) Toll-like receptors and innate immunity. Biochem Biophys Res Commun 388: 621-625.
56. Drevets DA, Leenen PJ, Campbell PA (1993) Complement receptor type 3 (CD11b/CD18) involvement is essential for killing of Listeria monocytogenes by mouse macrophages. J Immunol 151: 5431-5439.
57. Drevets DA, Leenen PJ, Campbell PA (1996) Complement receptor type 3 mediates phagocytosis and killing of Listeria monocytogenes by a TNF-alpha- and IFN-gamma-stimulated macrophage precursor hybrid. Cell Immunol 169: 1-6.
58. Gafa V, Manches O, Pastor A, Drouet E, Ambroise-Thomas P, et al. (2005) Human cytomegalovirus downregulates complement receptors (CR3. CR4) and decreases phagocytosis by macrophages. J Med Virol 76: 361-366.
59. Watanabe I, Ichiki M, Shiratsuchi A, Nakanishi Y (2007) TLR2-mediated survival of Staphylococcus aureus in macrophages: a novel bacterial strategy against host innate immunity. J Immunol 178: 4917-4925.
60. Higgins SC, Jarnicki AG, Lavelle EC, Mills KH (2006) TLR4 mediates vaccineinduced protective cellular immunity to Bordetella pertussis: role of IL-17- producing T cells. J Immunol 177: 7980-7989.
61. Mittal R, Gonzalez-Gomez I, Panigrahy A, Goth K, Bonnet R, et al. (2010) IL- 10 administration reduces PGE-2 levels and promotes CR3-mediated clearance of Escherichia coli K1 by phagocytes in meningitis. J Exp Med 207: 1307-1319.
62. Demangel C, Bertolino P, Britton WJ (2002) Autocrine IL-10 impairs dendritic cell (DC)-derived immune responses to mycobacterial infection by suppressing DC trafficking to draining lymph nodes and local IL-12 production. Eur J Immunol 32: 994-1002.
63. Edberg JC, Qin H, Gibson AW, Yee AM, Redecha PB, et al. (2002) The CY domain of the Fcgamma RIa alpha-chain (CD64) alters gamma-chain tyrosinebased signaling and phagocytosis. J Biol Chem 277: 41287-41293.
64. Qin H, Edberg JC, Gibson AW, Page GP, Teng L, et al. (2004) Differential gene expression modulated by the cytoplasmic domain of Fc gamma RIa (CD64) alpha-chain. J Immunol 173: 6211-6219.
65. Kedzierska K, Ellery P, Mak J, Lewin SR, Crowe SM, et al. (2002) HIV-1 downmodulates gamma signaling chain of Fc gamma R in human macrophages: a possible mechanism for inhibition of phagocytosis. J Immunol 168: 2895-2903.
66. Indik ZK, Hunter S, Huang MM, Pan XQ, Chien P, et al. (1994) The high affinity Fc gamma receptor (CD64) induces phagocytosis in the absence of its cytoplasmic domain: the gamma subunit of Fc gamma RIIIA imparts phagocytic function to Fc gamma RI. Exp Hematol 22: 599-606.
67. Maruvada R, Prasadarao NV, Rubens CE (2009) Acquisition of factor H by a novel surface protein on group B Streptococcus promotes complement degradation. Faseb J 23: 3967-3977.
68. Prasadarao NV (2002) Identification of Escherichia coli outer membrane protein A receptor on human brain microvascular endothelial cells. Infect Immun 70: 4556-4563.
69. Mittal R, Aggarwal S, Sharma S, Chhibber S, Harjai K (2009) Contribution of macrophage secretory products to urovirulence of Pseudomonas aeruginosa. FEMS Immunol Med Microbiol 57: 156-164.
70. Mittal R, Sharma S, Chhibber S, Harjai K (2006) Effect of macrophage secretory products on elaboration of virulence factors by planktonic and biofilm cells of Pseudomonas aeruginosa. Comp Immunol Microbiol Infect Dis 29: 12-26.
71. Stanley ER (1997) Murine bone marrow-derived macrophages. Methods Mol Biol 75: 301-304.
72. Mittal R, Sharma S, Chhibber S, Harjai K (2008) Contribution of free radicals to Pseudomonas aeruginosa induced acute pyelonephritis. Microb Pathog 45: 323-330.
73. Mittal R, Prasadarao NV (2010) Nitric oxide/cGMP signaling induces Escherichia coli K1 receptor expression and modulates the permeability in human brain endothelial cell monolayers during invasion. Cell Microbiol 12: 67-83.