Complement protein C1q bound to apoptotic cells suppresses human macrophage and dendritic cell-mediated Th17 and Th1 T cell subset proliferation

Journal of Leukocyte Biology

Volumn 97, Issue 1, 2015, Pages 147-160

  Clarke, Elizabeth V ^a,b   Weist, Brian M ^c   Walsh, Craig M ^a,b   Tenner, Andrea J ^a,b  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Autoimmunity; Inflammation; Phagocytosis

Indexed keywords

CD40 ANTIGEN; CD86 ANTIGEN; COMPLEMENT COMPONENT C1Q; RESIQUIMOD; TOLL LIKE RECEPTOR 4; TOLL LIKE RECEPTOR 7; TOLL LIKE RECEPTOR 8;

APOPTOSIS; ARTICLE; CELL PROLIFERATION; DENDRITIC CELL; HUMAN; HUMAN CELL; IMMUNE SYSTEM; MACROPHAGE; PRIORITY JOURNAL; REGULATORY T LYMPHOCYTE; SIGNAL TRANSDUCTION; SYSTEMIC LUPUS ERYTHEMATOSUS; T LYMPHOCYTE SUBPOPULATION; TH1 CELL; TH17 CELL; FLOW CYTOMETRY; IMMUNOLOGY; LYMPHOCYTE ACTIVATION; MIXED LYMPHOCYTE CULTURE; PHAGOCYTOSIS;

ERAGROSTIS TEF;

APOPTOSIS; CELL PROLIFERATION; COMPLEMENT C1Q; DENDRITIC CELLS; FLOW CYTOMETRY; HUMANS; LUPUS ERYTHEMATOSUS, SYSTEMIC; LYMPHOCYTE ACTIVATION; LYMPHOCYTE CULTURE TEST, MIXED; MACROPHAGES; PHAGOCYTOSIS; TH1 CELLS; TH17 CELLS;

EID: 84925287332     PISSN: 07415400     EISSN: 19383673     Source Type: Journal    
DOI: 10.1189/jlb.3A0614-278R     Document Type: Article

References (84)

1. Walport, M. Davies, K. A., Botto, M. (1998) Clq and systemic lupus erythematosus. Immunobiology 199, 265-285.
2. Botto, M., Dell'Agnola, C., Bygrave, A. E., Thompson, E. M., Cook, H. T., Petiy, F., Loos, M., Pandolfi, P. P., Walport, M. J. (1998) Homozygous Clq deficiency causes glomerulonephritis associated with multiple apoptotic bodies. Nat. Genet. 19, 56-59.
3. Mitchell, D. A., Pickering, M. C., Warren, J., Fossati-Jimack, L., Cortes-Hernandez, J., Cook, H. T., Botto, M., Walport, M. J. (2002) Clq deficiency and autoimmunity: the effects of genetic background on disease expression. J. Immunol. 168, 2538-2543.
4. Miura-Shimura, V., Nakamura, K., Ohtsuji, M., Tomita, H., Jiang, Y., Abe, M., Zhang, O., Hamano, Y., Tsuda, H., Hashimoto, H., Nishimura, H., Taki, S., Shirai, T., Hirose, S. (2002) Clq regulatory region polymorphism down-regulating murine clq protein levels with linkage to lupus nephritis. J. Immunol. 169, 1334-1339.
5. Galvan, M. D., Foreman, D. B., Zeng, E., Tan. J. C., Bohlson, S. S. (2012) Complement component Clq regulates macrophage expression of Mer tyrosine kinase to promote clearance of apoptotic cells. J. Immunol 188 3716-3723.
6. Zizzo, G., Hilliard, B. A., Monestier, M., Cohen, P. L. (2012) Efficient clearance of early apoptotic cells by human macrophages requires M2c polarization and MerTK induction. J. Immunol. 189, 3508-3520.
7. Korb, L. C., Ahearn, J. M. (1997) Clq hinds directly and specifically to surface blebs of apoptotic human keratinocytes: complement deficiency and systemic lupus erythematosus revisited. J. Immunol. 158, 4525-4528.
8. Botto, M., Walport, M. J. (2002) Clq, autoimmunity and apoptosis. Immunobiology 205, 395-406.
9. Elkon, K. B., Santer, D. M. (2012) Complement, interferon and lupus. Cun. Opin. Immunol. 24, 665-670.
10. Abdulahad, D. A., Westra, J., Limburg, P. C., Kallenberg, C. G., Bijl, M. (2010) HMGB1 in systemic lupus erythematosus: its role in cutaneous lesions development. Autoimmun. Rev. 9, 661-665.
11. Santer, D. M., Wiedeman, A E., Teal, T. H., Ghosh, P., Elkon, K. B. (2012) Plasmacytoid dendritic cells and Clq differentially regulate inflammatory gene induction by lupus immune complexes. J. Immunol. 188, 902-915.
12. Lu. J. H., Teh, B. K., Wang, Ld., Wang, Y. N., Tan, Y. S., Lai, M. C., Reid, K. B. M. (2008) The classical and regulatory functions of Clq in immunity and autoimmunity. Cell. Mol. Immunol. 5, 9-21.
13. Fraser, D. A., Laust, A. K., Nelson, E. L., Tenner, A. J. (2009) Clq differentially modulates phagocytosis and cytokine responses during ingestion of apoptotic cells by human monocytes, macrophages, and dendritic cells. J. Immunol. 183, 6175-6185.
14. Castellano, G., Woltman, A M., Schena, F. P., Roos, A., Daha, M. R., van Kooten, C. (2004) Dendritic cells and complement: at the cross road of innate and adaptive immunity. Mol. Immunol. 41, 133-140.
15. Teh, B. K., Yeo, J. G., Chern, L. M., Lu, J. (2011) Clq regulation of dendritic cell development from monocytes with distinct cytokine production and T cell stimulation. Mol. Immunol. 48, 1128-1138.
16. Fraser, D. A., Arora, M., Bohlson, S. S., Lozano, F., Tenner, A. J. (2007) Generation of inhibitory NF-κB complexes and phosphorylated cAMP response element-binding protein correlates with the anti-inflaminatory activity of complement protein Clq in human monocytes. J. Biol Chnii 282, 7360-7367.
17. Benoit, M. E., Clarke, E. V., Morgado, P., Fraser, D. A., Tenner, A. J. (2012) Complement protein Clq directs macrophage polarization and limits inflammasome activity during the uptake of apoptotic cells. J. Immunol. 188, 5682-5693.
18. Tsokos, G. C. (2011) Systemic lupus erythematosus. N. End. J. Med 2110-2121.
19. Peng, X., Kasran, A., Warmerdam, P. A., de Boer, M., Ceuppens, J. L. (1996) Accessory signaling by CD40 for T cell activation: induction of Till and Th2 cytokines and synergy with interleukin-12 for interferon-gamma production. Eur. J. Immunol 26, 1621-1627.
20. Lichtcnegger, F. S., Mueller, K., Otte, B., Beck, B., Hiddemann, W. Schendel, D. J., Subklewe, M. (2012) CD86 and IL-12p70 are key players for T helper 1 polarization and natural killer cell activation by Toll-like receptor-induced dendritic cells. PLoS ONE 7, e44266.
21. Kang, H. K., Liu, M., Datta, S. K. (2007) Low-dose peptide tolerance therapy of lupus generates plasmacytoid dendritic cells that cause expansion of autoantigen-specifìc regulatory T cells and contraction of inflammatory Thl7 cells. J. Immunol. 178, 7849-7858.
22. Ding, Y., Li, j., Wu, Q., Yang, P., Luo, B., Xie, S., Druey, K. M., Zajac, A. T, Hsu, H. C., Mountz. J. D. (2013) IM7RA is essential for optimal localization of follicular Th cells in the germinal center light zone to promote autoantibody-producing B cells. J. Immunol. 191, 1614-1624.
23. Crispin, J. C., Tsokos, G. C. (2010) Interleukin-17-producing T cells in lupus. Curr. Opin. Rheumatol. 22, 499-503.
24. Mascanfroni, I. D., Yeste, A., Vieira, S. M., Burns, E. J., Patel, B., Sloma, I Wu, Y., Mayo, L., Ben-Hamo, R., Efroni, S., Kuchroo, V. K., Robson, S. C., Quintana, F. J. (2013) IL-27 acts on DCs to suppress the T cell response and autoimmunity by inducing expression of the immunoregulatory molecule CD39. Nat. Immunol. 14, 1054-1063.
25. Diveu, C., McGeachy, M. J., Boniface, K., Stumhofer. J. S., Sathe, M. Joyce-Shaikh, B., Chen, Y., Tato, C. M., McClanahan, T. K., de Waal Malcfyt, R., Hunter, C. A., Cua, D. J., Kastclein, R. A. (2009) IL-27 blocks RORc expression to inhibit lineage commitment of Thl7 cells J. Immunol. 182, 5748-5756.
26. Kido, M., Takeuchi, S., Sugiyama, N., Esaki, H., Nakashitna, H., Yoshida H., Furue, M. (2011) T cell-specific overexpression of interleukin-27 receptor α subunit (WSX-1) prevents spontaneous skin inflammation in MRL/lpr mice. Br. J. Dermatol. 164, 1214-1220.
27. Sugiyama, N., Nakashima, H., Yoshiinura, T., Sadanaga, A., Shimizu, S Masutani, K., Igawa, T., Akahoshi, M., Miyake, K., Takeda, A., Yoshiinura A., Hamano, S., Yoshida, H. (2008) Amelioration of human lupus-like phenotypes in MRL/lpr mice by overexpression of interleukin 27 receptor alpha (WSX-1). Ann. Rheum. Dis. 67, 1461-1467.
28. Iyer, S. S., Ghaffari, A. A., Cheng, G. (2010) Lipopolysaccharide-mediated IL-10 transcriptional regulation requires sequential induction of type I IFNs and IL-27 in macrophages. J. Immunol. 185, 6599-6607.
29. Guarda, G., Braun, M., Staehli, F., Tardivel, A., Mattmann, C., Forster, I., Farlik, M., Decker, T., Du Pasquier, R. A., Romero, P., Tschopp, J. (2011) Type I interferon inhibits interleukin-1 production and inflammasome activation. Immunity 34, 213-223.
30. Karakhanova, S., Bedke, T., Enk, A. H., Mahnke, K. (2011) IL-27 renders DC immunosuppressive by induction of B7-H1. J. Leukoc. Biol. 89, 837-845.
31. Huber, S., Hoffmann, R., Muskens, F., Voehringer, D. (2010) Alternatively activated macrophages inhibit T-cell proliferation by Stat6-dependent expression of PD-L2. Blood 116, 3311-3320.
32. Fife, B. T., Pauken, K. E., Eagar, T. N., Obu, T., Wu, J., Tang, Q., Azuma, M., Krummel, M. F., Bluestone, J. A. (2009) Interactions between PD-1 and PD-L1 promote tolerance by blocking the TCR-induced stop signal. Nat. Immunol. 10, 1185-1192.
33. Latchman, Y., Wood, C. R., Chernova, T., Chaudhary, D., Borde, M., Chernova, I., Iwai, Y., Long, A. J., Brown, J. A., Nunes, R., Greenfield, F. A., Bourque, K., Boussiotis, V. A., Carter, L. L., Carreno, B. M., Malenkovich, N., Nishimura, H., Okazaki. T., Honjo, T. Sharpe. A. H. Freeman, G. J. (2001) PD-L2 is a second ligand for PD-1 and inhibits T cell activation. Nat. Immunol. 2, 261-268.
34. Sakaguchi, S., Yamaguchi, T., Nomura, T., Ono, M. (2008) Regulatory T cells and immune tolerance. Cell 133, 775-787.
35. Cretney, E., Rallies, A., Nutt, S. L. (2013) Differentiation and function of Foxp3(+) effector regulatory T cells. Trends Immunol. 34, 74-80.
36. Mukheijce, S., Giamberardino, C., Thomas, J. M., Gowdy, K., Pastva, A. M., Wright, J. R. (2012) Surfactant protein A modulates induction of regulatory T cells via TGF-β. J. Immunol. 188, 4376-4384.
37. Bercs, A. J., Haribhai, D., Chadwick, A. C., Gonyo, P. J., Williams, C. B., Drobyski, W. R. (2012) CD8+ Foxp3+ regulator' T cells are induced during graft-versus-host disease and mitigate disease severity. J. Immunol. 189, 464-474.
38. Tenner, A. J., Lesavre, P. H., Cooper, N. R. (1981) Purification and radiolabeling of human Clq. J. Immunol. 127, 648-653.
39. Young, Jr., K. R., Ambrus, Jr., J. L., Malbran, A., Fauci, A. S., Tenner, A. J. (1991) Complement subcomponent Clq stimulates Ig production by human B lymphocytes. J. Immunol. 146, 3356-3364.
40. Yu, M., Wang, H., Ding, A., Golenbock, D. T., Latz, E., Czura, C. J., Fenton, M. J., Tracey, K. J., Yang, H. (2006) HMGB1 signals through tolllike receptor (TLR) 4 and TLR2. Shock 26, 174-179.
41. Chatzigeorgiou, A., Lyberi, M., Chatzilymperis, G., Nezos, A., Hamper, E. (2009) CD40/CD40L signaling and its implication in health and disease. Biofactors 35, 474-483.
42. Castellano, G., Woltman, A. M., Schlagwein, N., Xu, W., Schena, F. P., Daha, M. R., van Kooten, C. (2007) Immune modulation of human dendritic cells by complement. Eur. J. Immunol 37, 2803-2811.
43. Fraser, D. A., Bohlson, S. S. Jasinskiene, N., Rawal, N., Palmarini, G., Ruiz, S., Rochford, R., Tenner, A. J. (2006) Clq and MBL, components of the innate immune system, influence monocyte cytokine expression. J. Irukoc. Biol. 80, 107-116.
44. Vollger, L. W., Uittenbogaart, C. H. (1993) Interleukin-7 promotes the generation of phenotypically mature CD45RA positive human thymocytes in vitro. Cytokine 5, 157-168.
45. Rathmell, J. C., Farkash, E. A., Gao, W., Thompson, C. B. (2001) IL-7 enhances the survival and maintains the size of naive T cells. J. Immunol. 167, 6869-6876.
46. Bretschneider, I., Clemente, M. J., Meisel, C., Guerreiro, M., Streitz, M., Hopfenmūller, W., Maciejewski. J. P., Wlodarski, M. W., Volk, H. D. (2014) Discrimination of T-cell subsets and T-cell receptor repertoire distribution. Immunol. Res. 58, 20-27.
47. Shen, N., Fu, Q., Deng, Y., Qian, X., Zhao, J., Kaufman, K. M., Wu, Y. L., Yu, C. Y., Tang, Y., Chen, J. Y., Yang, W., Wong, M., Kawasaki, A., Tsuchiya, N., Sumida, T., Kawaguchi, Y., Howe, H. S., Mok, M. Y., Bang, S. Y., Liu, F. L., Chang, D. M., Takasaki, Y., Hashimoto, H., Harley, J. B., Guthridgc. J. M., Grossman, J. M., Cantor, R. M., Song, Y. W., Bae, Š. C., Chen, S., Hahn, B. H., Lau, Y. L., Tsao, B. P. (2010) Sex-specific association of X-linked Toll-like receptor 7 (TLR7) with male systemic lupus erythematosus. Proc. Natl. Acad. Sci. USA 107, 15838-15843.
48. Kelley, J., Johnson, M. R., Alarcon, G. S., Kimberly, R. P., Edberg. J. C. (2007) Variation in the relative copy number of the TLR7 gene in patients with systemic lupus erythematosus and healthy control subjects. Arthritis Rheum. 56, 3375-3378.
49. Alunno, A., Bartoloni, E., Bistoni. O., Nocentini, G., Ronchetti, S., Caterbi, S., Valentini, V., Riccardi, C, Gerli, R. (2012) Balance between regulatory T and Th 17 cells in systemic lupus erythematosus: the old and the new. Clin. Dev. Immunol. 2012, 823085.
50. Shin, M. S., Lee, N., Kang, I. (2011) Effector T-cell subsets in systemic lupus erythematosus: update focusing on Thl7 cells. Curr. Opin. Rheumatol. 23, 444-448.
51. Lazarevic, V., Chen, X., Shim, J. H., Hwang. E. S. Jang, F. Bolni. A. N. Oukka, M., Kuchroo, V. K., Glimcher, I. H. (2011) í-bet represses T(H)17 differentiation by preventing Runxl-mediated activation of the gene encoding RORyt. Nat. Immunol. 12, 96-104.
52. Krieg, A. M. Vollmer, J. (2007) Toll-like receptors 7, 8, and 9: linking innate immunity to autoimmunity. Immunol, Rev. 220, 251-269.
53. Nauta, A. J., Castellano. G., Xu, W., Woltman, A. M., Borrias, M. C., Daha. M. R., van Kooten, C., Roos, A. (2004) Opsonization with Glq and mannose-binding lectin targets apoptotic cells to dendritic cells. J. Immunol. 173, 3044-3050.
54. Batten, M., Li, J., Yi, S., Kljavin, N. M., Danilenko, D. M., Lucas, S., Lee, J., de Sauvage, F. J., Ghilardi, N. (2006) Interleukin 27 limits autoimmune encephalomyelitis by suppressing the development of interleukin 17-producing T cells. Nat. Immunol. 7, 929-936.
55. Stumhofcr, J. S., Hunter, C A. (2008) Advances in understanding the anti-inflammatory properties of IL-27. Immunol. Utt. 117, 123-130.
56. Hirahara, K., Ghoreschi, K., Yang, X. P., Takahashi, H., Laurence, A., Vahedi, G., Sciumè, G., Hall, A. O., Dupont, C. D., Francisco, L. M., Chen, Q., Tanaka, M., Kanno, Y., Sun, H. W., Sharpe, A. H., Hunter, C. A., O'Shea, J. J. (2012) Interleukin-27 priming of T cells controls 11.-17 production in trans via induction of the ligand PD-L1. Immunity 36, 1017-1030.
57. Baruah, P., Dumitriu, I. E., Malik, T. H., Cook, H. T., Dyson, J., Scott, D., Simpson, E., Botto, M. (2009) Clq enhances IFN-gamma production by antigen-specific T cells via the CD40 costimulatory pathway on dendritic cells. Blood 113, 3485-3493.
58. Nold, M. F., Nold-Petry, C. A., Zepp, J. A., Palmer, B. F. Bufler, P., Dinarello. C. A. (2010) 11.-37 is a fundamental inhibitor of innate immunity. Nat. Immunol. 11, 1014-1022.
59. Hsieh, C. S., Macatonia, S. F. Tripp, C. S., Wolf, S. F., O'Garra. A., Murphy, K. M. (1993) Development of TH1 CD4+ T cells through IL-12 produced by Usteria-induced macrophages. Science 260, 547-549.
60. Ghoreschi, K., Laurence, A., Yang, X. P., Hirahara, K., O'Shea, J. J. (2011) T helper 17 cell heterogeneity and pathogenicity in autoimmune disease. Trends Immunol. 32, 395-401.
61. Caux, C., Vanbervliet, B., Massacricr, C., Azuma, M., Okumura, K., Ianier, L. L., Banchereau, J. (1994) B70/B7-2 is identical tu CD86 ami is the major functional ligand for CD28 expressed on human dendritic cells. J. Exp. Med. 180, 1841-1847.
62. Villegas-Mendez, A., de Souza, J. B. Lavelle, S. W., Gwyer Findlay, F. Shaw, T. N., van Rooijen, N. Saris, C. J., Hunter, C. A., Riley, E. M., Couper, K. N. (2013) IL-27 receptor signalling restricts the formation of pathogenic, terminally differentiated Thl cells during malaria infection by repressing IL-12 dependent signals. PolS Pathog. 9, e1003293.
63. O'Shea, J. J., Paul, W. E. (2010) Mechanisms underlying lineage commitment and plasticity of helper CD4+ T cells. Science 327, 1098-1102.
64. Ito, S. Ansari, P., Sakatsumc, M., Dickensheets, H., Vazquez. N., Donnelly, R. P., Lamer, A. C., Finbloom. D. S. (1999) Interleukin-10 inhibits expression of both interferon alpha-and interferon gamma-induced genes by suppressing tyrosine phosphorylation of STAT1. Blood 93, 1456-1463.
65. Bell. C. W., Jiang, W., Reich III C. F., Pisetsky, D. S. (2006) The extracellular release of HMGBI during apoptotic cell death. Am. J. Physiol. Cell Physiol. 291, C1318-C1325.
66. Baruah, P., Simpson, E., Dumitriu. I. F., Derbyshire, K., Coe, D., Addey, C., Dyson, J., Chai, L. G., Cook, T., Scott, D., Botto, M. (2010) Mice lacking Clq or C3 show accelerated rejection of minor H disparate skin grafts and resistance to induction of tolerance. Eur. J. Immunol. 40, 1758-1767.
67. Sathaliyawala, T., Kubota, M., Yudanin, N. Turner, D., Camp, P., Thome, J. J., Bickham, K. L., Lerner, H., Goldstein, M., Sykes, M., Kato, T., Father, D. L. (2013) Distribution and compartmentalization of human circulating and tissue-resident memory T cell subsets. Immunity 38, 187-197.
68. Davies, I. C., Jenkins, S. J., Allen, J. F. Taylor, P. R. (2013) Tissue-resident macrophages. Nat. Immunol. 14, 986-995.
69. Fry, T. J., Mackall, C. L. (2002) Intcrleukin-7: from bench to clinic. Blood 99, 3892-3904.
70. Baudino, L., Sardini, A., Ruseva, M. M., Fossati-Jimack, I., Cook, H. T., Scott, D., Simpson, E., Botto, M. (2014) C3 opsonization regulates endocytic handling of apoptotic cells resulting in enhanced T-cell responses to cargo-derived antigens, Proc. Natl. Acad. Sci. USA 111, 1503-1508.
71. Amel Kashipaz, M. R., Huggins, M. I. Powell, R. J., Todd, I. (2002) Human autologous mixed lymphocyte reaction as an in vitro model for autoreactivity to apoptotic antigens. Immunology 107, 358-365.
72. Chernysheva, A. D., Kirou, K. A., Crow, M. K. (2002) T cell proliferation induced by autologous non-T cells is a response to apoptotic cells processed by dendritic cells. J. Immunol. 169, 1241-1250.
73. Mallone, R., Mannering, S. I., Brooks-Worrell, B. M., Durinovic-Bclló, I., Cilio, C. M., Wong, F. S., Silloot, N. C.; T-Cell Workshop Committee, Immunology of Diabetes Society. (2011) Isolation and preservation of peripheral blood mononuclear cells for analysis of islet antigen-reactive T cell responses: position statement of the T-Cell Workshop Committee of the Immunology of Diabetes Society. Clin. Exp. Immunol. 163, 33-49.
74. Son, M., Santiago-Schwarz, F., Al-Abed, Y., Diamond, B. (2012) Clq limits dendritic cell differentiation and activation by engaging LAIR-1. Proc Natl. Acad. Sri. USA 109, E3160-E3167.
75. Ramirez-Ortiz, Z. G., Pendergraft III, W. F., Prasad, A, Byrne, M. H., Iram, T., Blanchette, C. J., Luster, A. D., Hacohen, N., El Khoury, J., Means, T. K. (2013) The scavenger receptor SCARF1 mediates the clearance of apoptotic cells and prevents autoimmunity. Nat. Immunol. 14, 917-926.
76. Byrne, J. C., Ní Gabhann, J., Stacey, K. B., Coffey, B. M., McCarthy, E., Thomas, W., Jefferies, C. A. (2013) Bruton's tyrosine kinase is required for apoptotic cell uptake via regulating the phosphorylation and localization of calreticulin. J. Immunol. 190, 5207-5215.
77. Kemper, C., Köhl, J. (2013) Novel roles for complement receptors in T cell regulation and beyond. Mol. Immunol. 56, 181-190.
78. Cuder, A. J., Botto, M., van Essen, D., Rivi, R., Davies, K. A., Gray, D., Walport, M. J. (1998) T cell-dependent immune response in Clq-deficient mice: defective interferon gamma production by antigen-specific T cells. J. Exp. Med. 187, 1789-1797.
79. Seok, J., Warren, H. S., Cuenca, A. G., Mindrinos, M. N., Baker, H. V., Xu, W., Richards, D. R., McDonald-Smith, G. P., Gao, H., Hennessy, L., Finnerty, C. C., López, C. M., Honari, S., Moore, E. E., Minei, J. P., Cuschieri, J., Bankey, P. E., Johnson, J. L., Sperry, J., Naüiens, A B., Billiar, T. R., West, M. A., Jeschkc, M'. G., Klein, M. B. Gamelli, R. L., Gibran, N. S., Brownstein, B. H., Miller-Graziano, C., Calvano, S. E., Mason, P. H., Cobb, J. P., Rahme, L. G., Lowry, S. F., Maier, R. V., Moldawer, L. I., Herndon, D. N., Davis, R. W., Xiao, W., Tompkins, R. G., Inflammation and Host Response to Injury Large Scale Collaborative Research Program. (2013) Genomic responses in mouse models poorly mimic human inflammatory diseases. Proc. Natl. Acad. Sci. USA 110 3507-3512.
80. Osterburg, A. R., Hexley, P., Supp, D. M., Robinson, C. T., Noel, G., Ogle C., Boyce, S. T., Aronow, B. J., Babcock, G. F. (2013) Concerns over interspecies transcriptional comparisons in mice and humans after trauma. Proc. Natl. Acad. Sri. USA 110, E3370.
81. Mestas, J., Hughes, C. C. (2004) Of mice and not men: differences between mouse and human immunology. J. Immunol. 172, 2731-2738.
82. Skapenko, A., Leipe, J., Lipsky, P. E., Schulze-Koops, H. (2005) The role of the T cell in autoimmune inflammation. Arthritis Res. Thrr 7 (Suppl 2), S4-S14.
83. Bensa, J. C., Reboul, A., Colomb, M. G. (1983) Biosynthesis in vitro of complement subcomponents Clq, Cls and Cl inhibitor by resting and stimulated human monocytes. Riorhem. J. 216, 385-392.
84. Martens, H. A., Zuurman, M. W., de Iange, A. H., Nolte, I. M., van der Steege, G., Navis, G. J., Kallenberg, C. G., Seelen, M. A., Bijl, M. (2009) Analysis of Clq polymorphisms suggests association with systemic lupus erythematosus, serum Clq and CH50 levels and disease severity. Ann Rheum. Dis. 68, 715-720.