C1q and MBL, components of the innate immune system, influence monocyte cytokine expression

Journal of Leukocyte Biology

Volumn 80, Issue 1, 2006, Pages 107-116

  Fraser, Deborah A ^a   Bohlson, Suzanne S ^a   Jasinskiene, Nijole ^a   Rawal, Nenoo ^b   Palmarini, Gail ^a   Ruiz, Sol ^a,d   Rochford, Rosemary ^c   Tenner, Andrea J ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF TEXAS HEALTH CENTER   (United States)

^c State University of New York Upstate Medical University: College of Medicine   (United States)

^d Division of Pharmacoepidemiology and Pharmacovigilance   (Spain)

Author keywords

Complement; Human; Macrophages

Indexed keywords

CHEMOATTRACTANT; COLLAGEN; COMPLEMENT COMPONENT C1Q; CYTOKINE; INTERLEUKIN 1; INTERLEUKIN 1 ALPHA; INTERLEUKIN 1 BETA; INTERLEUKIN 1 RECEPTOR BLOCKING AGENT; INTERLEUKIN 10; INTERLEUKIN 12P70; INTERLEUKIN 6; LIPOPOLYSACCHARIDE; MANNOSE BINDING LECTIN; MESSENGER RNA; MONOCYTE CHEMOTACTIC PROTEIN 1; SYNAPSIN I;

APOPTOSIS; ARTICLE; AUTOIMMUNITY; CONTROLLED STUDY; CYTOKINE PRODUCTION; HUMAN; HUMAN CELL; IMMUNE RESPONSE; IN VITRO STUDY; IN VIVO STUDY; INNATE IMMUNITY; KNOCKOUT MOUSE; LUPUS LIKE SYNDROME; MACROPHAGE; MONOCYTE; PATHOGENESIS; PERIPHERAL BLOOD MONONUCLEAR CELL; PHAGOCYTOSIS; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN FAMILY; SIGNAL TRANSDUCTION; UPREGULATION;

ANIMALS; COMPLEMENT C1Q; CYTOKINES; HUMANS; IMMUNITY, NATURAL; LIPOPOLYSACCHARIDES; MANNOSE-BINDING LECTIN; MICE; MICE, KNOCKOUT; MONOCYTES; RNA, MESSENGER; UP-REGULATION;

EID: 33750429108     PISSN: 07415400     EISSN: None     Source Type: Journal    
DOI: 10.1189/jlb.1105683     Document Type: Article

References (81)

1. Pasare, C., Medzhitov, R. (2004) Toll-like receptors: linking innate and adaptive immunity. Microbes Infect. 6, 1382-1387.
2. Tenner, A. J. (1999) Membrane receptors for soluble defense collagens. Curr. Opin. Immunol. 11, 34-42.
3. Ma, Y. G., Cho, M. Y., Zhao, M., Park, J. W., Matsushita, M., Fujita, T., Lee, B. L. (2004) Human mannose-binding lectin and L-ficolin function as specific pattern recognition proteins in the lectin activation pathway of complement. J. Biol. Chem. 279, 25307-25312.
4. Sim, R. B., Tsiftsoglou, S. A. (2004) Proteases of the complement system. Biochem. Soc. Trans. 32, 21-27.
5. Bobak, D. A., Gaither, T. G., Frank, M. M., Tenner, A. J. (1987) Modulation of FcR function by complement: subcomponent C1q enhances the phagocytosis of IgG-opsonized targets by human monocytes and culture-derived macrophages. J. Immunol. 138, 1150-1156.
6. Hartshorn, K. L., Sastry, K., White, M. R., Anders, E. M., Super, M., Ezekowitz, R. A., Tauber, A. I. (1993) Human mannose-binding protein functions as an opsonin for influenza A viruses. J. Clin. Invest. 91, 1414-1420.
7. Tenner, A. J., Robinson, S. L., Borchelt, J., Wright, J. R. (1989) Human pulmonary surfactant protein (SP-A), a protein structurally homologous to C1q, can enhance FcR- and CR1-mediated phagocytosis. J. Biol. Chem. 264, 13923-13928.
8. Bobak, D. A., Frank, M. M., Tenner, A. J. (1988) C1q acts synergistically with phorbol dibutyrate to activate CR1-mediated phagocytosis by human mononuclear phagocytes. Eur. J. Immunol. 18, 2001-2007.
9. Bobak, D. A., Washburn, R. G., Frank, M. M. (1988) C1q enhances the phagocytosis of cryptococcus neoformans blastospores by human monocytes. J. Immunol. 141, 592-597.
10. Arora, M., Munoz, E., Tenner, A. J. (2001) Identification of a site on mannan-binding lectin critical for enhancement of phagocytosis. J. Biol. Chem. 276, 43087-43094.
11. Webster, S. D., Galvan, M. D., Ferran, E., Garzon-Rodriguez, W., Glabe, C. G., Tenner, A. J. (2001) Antibody-mediated phagocytosis of the amyloid β-peptide in microglia is differentially modulated by C1q. J. Immunol. 166, 7496-7503.
12. Alan, R., Ezekowitz, B. (1991) Ante-antibody immunity. Curr. Biol. 1, 60-62.
13. Nauta, A. J., Daha, M. R., van Kooten, C., Roos, A. (2003) Recognition and clearance of apoptotic cells: a role for complement and pentraxins. Trends Immunol. 24, 148-154.
14. Nauta, A. J., Raaschou-Jensen, N., Roos, A., Daha, M. R., Madsen, H. O., Borrias-Essers, M. C., Ryder, L. P., Koch, C., Garred, P. (2003) Mannose-binding lectin engagement with late apoptotic and necrotic cells. Eur. J. Immunol. 33, 2853-2863.
15. Ogden, C. A., deCathelineau, A., Hoffmann, P. R., Bratton, D., Ghebrehiwet, B., Fadok, V. A., Henson, P. M. (2001) C1q and mannose binding lectin engagement of cell surface calreticulin and CD91 initiates macropinocytosis and uptake of apoptotic cells. J. Exp. Med. 194, 781-796.
16. Vandivier, R. W., Ogden, C. A., Fadok, V. A., Hoffmann, P. R., Brown, K. K., Botto, M., Walport, M. J., Fisher, J. H., Henson, P. M., Greene, K. E. (2002) Role of surfactant proteins A, D, and C1q in the clearance of apoptotic cells in vivo and in vitro: calreticulin and CD91 as a common collectin receptor complex. J. Immunol. 169, 3978-3986.
17. Korb, L. C., Ahearn, J. M. (1997) C1q binding directly and specifically to surface blebs of apoptotic human keratinocytes. J. Immunol. 158, 4525-4528.
18. Navratil, J. S., Watkins, S. C., Wisnieski, J. J., Ahearn, J. M. (2001) The globular heads of C1q specifically recognize surface blebs of apoptotic vascular endothelial cells. J. Immunol. 166, 3231-3239.
19. Botto, M., Dell'agnola, C., Bygrave, A. E., Thompson, E. M., Cook, H. T., Petry, F., Loos, M., Pandolfi, P. P., Walport, M. J. (1998) Homozygous C1q deficiency causes glomerulonephritis associated with multiple apoptotic bodies. Nat. Genet. 19, 56-59.
20. Stuart, L. M., Takahashi, K., Shi, L., Savill, J., Ezekowitz, R. A. (2005) Mannose-binding lectin-deficient mice display defective apoptotic cell clearance but no autoimmune phenotype. J. Immunol. 174, 3220-3226.
21. Botto, M., Walport, M. J. (2002) C1q, autoimmunity and apoptosis. Immunobiology 205, 395-406.
22. Garred, P., Voss, A., Madsen, H. O., Junker, P. (2001) Association of mannose-binding lectin gene variation with disease severity and infections in a population-based cohort of systemic lupus erythematosus patients. Genes Immun. 2, 442-450.
23. Mitchell, D. A., Pickering, M. C., Warren, J., Fossati-Jimack, L., Cortes-Hernandez, J., Cook, H. T., Botto, M., Walport, M. J. (2002) C1q deficiency and autoimmunity: the effects of genetic background on disease expression. J. Immunol. 168, 2538-2543.
24. Miura-Shimura, Y., Nakamura, K., Ohtsuji, M., Tomita, H., Jiang, Y., Abe, M., Zhang, D., Hamano, Y., Tsuda, H., Hashimoto, H., Nishimura, H., Taki, S., Shirai, T., Hirose, S. (2002) C1q regulatory region polymorphism down-regulating murine C1q protein levels with linkage to lupus nephritis. J. Immunol. 169, 1334-1339.
25. Potter, P. K., Cortes-Hernandez, J., Quartier, P., Botto, M., Walport, M. J. (2003) Lupus-prone mice have an abnormal response to thioglycolate and an impaired clearance of apoptotic cells. J. Immunol. 170, 3223-3232.
26. Matzinger, P. (1994) Tolerance, danger, and the extended family. Annu. Rev. Immunol. 12, 991-1045.
27. Matzinger, P. (2002) The danger model: a renewed sense of self. Science 296, 301-305.
28. LeVine, A. M., Whitsett, J. A., Gwozdz, J. A., Richardson, T. R., Fisher, J. H., Burhans, M. S., Korfhagen, T. R. (2000) Distinct effects of surfactant protein A or D deficiency during bacterial infection on the lung. J. Immunol. 165, 3934-3940.
29. Restrepo, C. I., Dong, Q., Savov, J., Mariencheck, W. I., Wright, J. R. (1999) Surfactant protein D stimulates phagocytosis of Pseudomonas aeruginosa by alveolar macrophages. Am. J. Respir. Cell Mol. Biol. 21, 576-585.
30. Greene, K. E., King Jr., T. E., Kuroki, Y., Bucher-Bartelson, B., Hunninghake, G. W., Newman, L. S., Nagae, H., Mason, R. J. (2002) Serum surfactant proteins-A and -D as biomarkers in idiopathic pulmonary fibrosis. Eur. Respir. J. 19, 439-446.
31. Wright, J. R. (2005) Immunoregulatory functions of surfactant proteins. Nat. Rev. Immunol. 5, 58-68.
32. Savill, J., Dransfield, I., Gregory, C., Haslett, C. (2002) A blast from the past: clearance of apoptotic cells regulates immune responses. Nat. Rev. Immunol. 2, 965-975.
33. Voll, R. E., Herrmann, M., Roth, E. A., Stach, C., Kalden, J. R., Girkontaite, I. (1997) Immunosuppressive effects of apoptotic cells. Nature 390, 350-351.
34. Fadok, V. A., Bratton, D. L., Konowal, A., Freed, P. W., Westcott, J. Y., Henson, P. M. (1998) Macrophages that have ingested apoptotic cells in vitro inhibit proinflammatory cytokine production through autocrine/paracrine mechanisms involving TGF-β, PGE2, and PAF. J. Clin. Invest. 101, 890-898.
35. Nauta, A. J., Castellano, G., Xu, W., Woltman, A. M., Borrias, M. C., Daha, M. R., van Kooten, C., Roos, A. (2004) Opsonization with C1q and mannose-binding lectin targets apoptotic cells to dendritic cells. J. Immunol. 173, 3044-3050.
36. Gardai, S. J., Xiao, Y. Q., Dickinson, M., Nick, J. A., Voelker, D. R., Greene, K. E., Henson, P. M. (2003) By binding SIRPα or calreticulin/CD91, lung collectins act as dual function surveillance molecules to suppress or enhance inflammation. Cell 115, 13-23.
37. Tenner, A. J., Lesavre, P. H., Cooper, N. R. (1981) Purification and radiolabeling of human C1q. J. Immunol. 127, 648-653.
38. Young, K. R., Ambrus Jr., J. L., Malbran, A., Fauci, A. S., Tenner, A. J. (1991) Complement subcomponent C1q stimulates immunoglobulin production by human B lymphocytes. J. Immunol. 146, 3356-3364.
39. Reid, K. B. M., Lowe, D. M., Porter, R. R. (1972) Isolation and characterization of C1q, a subcomponent of the first component of complement, from human and rabbit sera. Biochem. J. 130, 749-763.
40. Tan, S. M., Chung, M. C. M., Kon, O. L., Thiel, S., Lee, S. H., Lu, J. (1996) Improvements on the purification of mannon-binding lectin and demonstration of its Ca2+ independent association with a C1s-like serine protease. Biochem. J. 319, 329-332.
41. Thiel, S., Holmskov, U., Hviid, L., Laursen, S. B., Jensenius, J. C. (1992) The concentration of the C-type lectin, mannan-binding protein, in human plasma increases during an acute phase response. Clin. Exp. Immunol. 90, 31-35.
42. Lionetti, F. J., Hunt, S. M., Valeri, C. R. (1980) Methods of Cell Separation, New York, NY, Plenum, 141.
43. Bobak, D. A., Frank, M. M., Tenner, A. J. (1986) Characterization of C1q receptor expression on human phagocytic cells: effects of PDBu and fMLP. J. Immunol. 136, 4604-4610.
44. Guan, E., Robinson, S. L., Goodman, E. B., Tenner, A. J. (1994) Cell surface protein identified on phagocytic cells modulates the C1q-mediated enhancement of phagocytosis. J. Immunol. 152, 4005-4016.
45. Nepomuceno, R. R., Tenner, A. J. (1998) C1qRp, the C1q receptor that enhances phagocytosis, is detected specifically in human cells of myeloid lineage, endothelial cells, and platelets. J. Immunol. 160, 1929-1935.
46. Fonseca, M. I., Carpenter, P. M., Park, M., Palmarini, G., Nelson, E. L., Tenner, A. J. (2001) C1qR(P), a myeloid cell receptor in blood, is predominantly expressed on endothelial cells in human tissue. J. Leukoc. Biol. 70, 793-800.
47. Bohlson, S. S., Zhang, M., Ortiz, C. E., Tenner, A. J. (2005) CD93 interacts with the PDZ domain-containing adaptor protein GIPC: implications in the modulation of phagocytosis. J. Leukoc. Biol. 77, 80-89.
48. Bohnsack, J. F., Kleinman, H. K., Takahashi, T., O'Shea, J. J., Brown, E. J. (1985) Connective tissue proteins and phagocytic cell function laminin enhances complement and Fc-mediated phagocytosis by cultured human macrophages. J. Exp. Med. 161, 912-923.
49. r component of the C1q receptor. Immunity 3, 485-493.
50. r cell surface "C1q receptor". 33, 65.
51. Nepomuceno, R. R., Ruiz, S., Park, M., Tenner, A. J. (1999) C1qRP is a heavily O-glycosylated cell surface protein involved in the regulation of phagocytic activity. J. Immunol. 162, 3583-3589.
52. Tenner, A. J., Cooper, N. R. (1982) Stimulation of a human polymorphonuclear leukocyte oxidative response by the C1q subunit of the first complement component. J. Immunol. 128, 2547-2552.
53. Hoebe, K., Janssen, E., Beutler, B. (2004) The interface between innate and adaptive immunity. Nat. Immunol. 5, 971-974.
54. Underhill, D. M., Ozinsky, A. (2002) Phagocytosis of microbes: complexity in action. Annu. Rev. Immunol. 20, 825-852.
55. Dinarello, C. A. (1996) Biologic basis for interleukin-1 in disease. Blood 87, 2095-2147.
56. De Waal Malefyt, R., Abrams, R., Bennett, B., Figdor, C. G., De Vries, J. E. (1991) Interleukin 10 (IL-10) inhibits cytokine synthesis by human monocytes: an autoregulatory role of IL-10 produced by monocytes. J. Exp. Med. 174, 1209-1220.
57. Bogdan, C., Vodovotz, Y., Nathan, C. (1991) Macrophage deactivation by interleukin 10. J. Exp. Med. 174, 1549-1555.
58. Gazzinelli, R. T., Oswald, I. P., James, S. L., Sher, A. (1992) IL-10 inhibits parasite killing and nitrogen oxide production by IFN-γ-activated macrophages. J. Immunol. 148, 1792-1796.
59. Silva, J. S., Morrissey, P. J., Grabstein, K. H., Mohler, K. M., Anderson, D., Reed, S. G. (1992) Interleukin 10 and interferon γ regulation of experimental Trypanosoma cruzi infection. J. Exp. Med. 175, 169-174.
60. Capsoni, F., Minonzio, F., Ongari, A. M., Carbonelli, V., Galli, A., Zanussi, C. (1995) IL-10 up-regulates human monocyte phagocytosis in the presence of IL-4 and IFN-γ. J. Leukoc. Biol. 58, 351-358.
61. Berg, D. J., Kuhn, R., Rajewsky, K., Muller, W., Menon, S., Davidson, N., Grunig, G., Rennick, D. (1995) Interleukin-10 is a central regulator of the response to LPS in murine models of endotoxic shock and the Shwartzman reaction but not endotoxin tolerance. J. Clin. Invest. 96, 2339-2347.
62. Kuhn, R., Lohler, J., Rennick, D., Rajewsky, K., Muller, W. (1993) Interleukin-10-deficient mice develop chronic enterocolitis. Cell 75, 263-274.
63. Gunn, M. D., Nelken, N. A., Liao, X., Williams, L. T. (1997) Monocyte chemoattractant protein-1 is sufficient for the chemotaxis of monocytes and lymphocytes in transgenic mice but requires an additional stimulus for inflammatory activation. J. Immunol. 158, 376-383.
64. Amano, H., Morimoto, K., Senba, M., Wang, H., Ishida, Y., Kumatori, A., Yoshimine, H., Oishi, K., Mukaida, N., Nagatake, T. (2004) Essential contribution of monocyte chemoattractant protein-1/C-C chemokine ligand-2 to resolution and repair processes in acute bacterial pneumonia. J. Immunol. 172, 398-409.
65. Santana, M. A., Rosenstein, Y. (2003) What it takes to become an effector T cell: the process, the cells involved, and the mechanisms. J. Cell. Physiol. 195, 392-401.
66. Kilmon, M. A., Rutan, J. A., Clarke, S. H., Vilen, B. J. (2005) Cutting edge: low-affinity, Smith antigen-specific B cells are tolerized by dendritic cells and macrophages. J. Immunol. 175, 37-41.
67. Chomarat, P., Banchereau, J., Davoust, J., Palucka, A. K. (2000) IL-6 switches the differentiation of monocytes from dendritic cells to macrophages. Nat. Immunol. 1, 510-514.
68. Alcorn, J. F., Wright, J. R. (2004) Surfactant protein A inhibits alveolar macrophage cytokine production by CD14-independent pathway. Am. J. Physiol Lung Cell. Mol. Physiol. 286, l129 -L136.
69. Rosseau, S., Hammerl, P., Maus, U., Gunther, A., Seeger, W., Grimminger, F., Lohmeyer, J. (1999) Surfactant protein A down-regulates proinflammatory cytokine production evoked by Candida albicans in human alveolar macrophages and monocytes. J. Immunol. 163, 4495-4502.
70. Soell, M., Lett, E., Holveck, F., Scholler, M., Wachsmann, D., Klein, J-P. (1995) Activation of human monocytes by streptococcal rhamnose glucose polymers is mediated by CD14 antigen, and mannan binding protein inhibits TNF-α release. J. Immunol. 154, 851-860.
71. Borron, P. J., Mostaghel, E. A., Doyle, C., Walsh, E. S., McHeyzer-Williams, M. G., Wright, J. R. (2002) Pulmonary surfactant proteins A and D directly suppress CD3+/CD4+ cell function: evidence for two shared mechanisms. J. Immunol. 169, 5844-5850.
72. Stamme, C., Walsh, E., Wright, J. R. (2000) Surfactant protein A differentially regulates IFN-γ- and LPS-induced nitrite production by rat alveolar macrophages. Am. J. Respir. Cell Mol. Biol. 23, 772-779.
73. Khalkhali-Ellis, Z., Bulla, G. A., Schlesinger, L. S., Kirschmann, D. A., Moore, T. L., Hendrix, M. J. (1999) C1q-containing immune complexes purified from sera of juvenile rheumatoid arthritis patients mediate IL-8 production by human synoviocytes: role of C1q receptors. J. Immunol. 163, 4612-4620.
74. Yamada, M., Oritani, K., Kaisho, T., Ishikawa, J., Yoshida, H., Takahashi, I., Kawamoto, S., Ishida, N., Ujiie, H., Masaie, H., Botto, M., Tomiyama, Y., Matsuzawa, Y. (2004) Complement C1q regulates LPS-induced cytokine production in bone marrow-derived dendritic cells. Eur. J. Immunol. 34, 221-230.
75. Nauta, A. J., Castellano, G., Xu, W., Woltman, A. M., Borrias, M. C., Daha, M. R., van Kooten, C., Roos, A. (2004) Opsonization with C1q and mannose-binding lectin targets apoptotic cells to dendritic cells. J. Immunol. 173, 3044-3050.
76. Stuart, L. M., Lucas, M., Simpson, C., Lamb, J., Savill, J., Lacy-Hulbert, A. (2002) Inhibitory effects of apoptotic cell ingestion upon endotoxin-driven myeloid dendritic cell maturation. J. Immunol. 168, 1627-1635.
77. Urban, B. C., Willcox, N., Roberts, D. J. (2001) A role for CD36 in the regulation of dendritic cell function. Proc. Natl. Acad. Sci. USA 98, 8750-8755.
78. Byrne, A., Reen, D. J. (2002) Lipopolysaccharide induces rapid production of IL-10 by monocytes in the presence of apoptotic neutrophils. J. Immunol. 168, 1968-1977.
79. Sutterwala, F. S., Noel, G. J., Clynes, R., Mosser, D. M. (1997) Selective suppression of interleukin-12 induction after macrophage receptor ligation. J. Exp. Med. 185, 1977-1985.
80. Sutterwala, F. S., Noel, G. J., Salgame, P., Mosser, D. M. (1998) Reversal of proinflammatory responses by ligating the macrophage Fcγ receptor type I. J. Exp. Med. 188, 217-222.
81. Lucas, M., Stuart, L. M., Savill, J., Lacy-Hulbert, A. (2003) Apoptotic cells and innate immune stimuli combine to regulate macrophage cytokine secretion. J. Immunol. 171, 2610-2615.