The C1q family of proteins: Insights into the emerging non-traditional functions

Frontiers in Immunology

Volumn 3, Issue APR, 2012, Pages

  Ghebrehiwet, Berhane ^a   Hosszu, Kinga K ^a   Valentino, Alisa ^a   Peerschke, Ellinor I B ^b  

^a STONY BROOK UNIVERSITY   (United States)

^b MEMORIAL SLOAN KETTERING CANCER CENTER   (United States)

Author keywords

C1q and cancer; Emerging role of C1q; Functions of C1q; Role of C1q in inflammation and autoimmunity

Indexed keywords

EID: 84865417273     PISSN: None     EISSN: 16643224     Source Type: Journal    
DOI: 10.3389/fimmu.2012.00052     Document Type: Review

References (116)

1. Agostinis, C., Bulla, R., Tripodo, C., Gismondi, A., Stabile, H., Bossi, F., Guarnotta, C., Garlanda, C., De Seta, F., Spessotto, P., Santoni, A., Ghebrehiwet, B., Girardi, G., and Tedesco, F. (2010). An alternative role of C1q in cell migration and tissue remodelling: contribution to trophoblast invasion and placental development. J. Immunol. 185, 4420-4429.
2. Arlaud, G. J., Gaboriaud, C., Thielens, N. M., Rossi, V., Bersch, B., Hernandez, J.-F., and Fontecilla-Camps, J. C. (2001). Structural biology of C1: dissection of a complex molecular machinery. Immunol. Rev. 180, 136-145.
3. Armbrust, T., Nordmann, B., Kreissig, M., and Ramadori, G. (1997). C1q synthesis by tissue mononuclear phagocytes from normal and from damaged rat liver: up-regulation by dexamethasone, down-regulation by interferon gamma, and lipopolysaccharide. Hepatology 26, 98-106.
4. Bensa, J. C., Reboul, A., and Colomb, M. G. (1983). Biosynthesis in vitro of complement subcomponents C1q, C1s and C1-inhibitor by resting and stimulated human monocytes. Biochem. J. 216, 385-392.
5. Berg, A. H., Combs, T. P., Du, X., Brownlee, M., and Scherer, P. (2001). The adipocyte-secreted protein Acrp30 enhances hepatic insulin action. Nat. Med. 7, 947-953.
6. Bobak, D. A., Gaither, T. A., Frank, M. M., and 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.
7. Bogin, O., Kvansakul, M., Rom, E., Singer, J., Yayon, A., and Hohenester, E. (2002). Insight into Schmid metaphyseal chondrodysplasia from the crystal structure of the collagen X NCI domain trimer. Structure 10, 165-173.
8. Bordin, S., Ghebrehiwet, B., and Page, R. C. (1990). Participation of C1q and its receptor in adherence of human diploid fibroblasts. J. Immunol. 145, 2520-2526.
9. Bossi, F., Rizzi, L., Bulla, R., Tripodo, C., Guarnota, C., Novati, F., Ghebrehiwet, B., and Tedesco, F. (2011). C1q induces in vivo angiogenesis, and wound healing. Mol. Immunol. 48, abstr. 1676.
10. Botto, M., Dell'Angola, C., Bygrave, A. E., Thompson, E. M., Cook, H. T., Petry, F., Loos, M., Pandolfi, P. P., and Walport, M. J. (1998). Homozygous C1q deficiency causes glomerulonephritis associated with multiple apoptotic bodies. Nat. Genet. 19, 56-59.
11. Brodsky-Doyle, B., Leonhard, K. R., and Reid, K. B. M. (1976). Circulardichroism and electron microscopy studies of human subcomponent C1q before and after limited proteolysis by pepsin. Biochem. J. 159, 279.
12. Bulla, R., Agostinis, C., Bossi, F., Rizzi, L., Debeus, A., Tripodo, C., Radillo, O., DeSeta, F., Ghebrehiwet, B., and Tedesco, F. (2008). Decidual endothelial cells express surface bound C1q as a molecular bridge between endovascular trophoblast and decidual endothelium. Mol. Immunol. 45, 2629-2640.
13. Calcott, M. A., and Müller-Eberhard, H. J. (1972). C1q protein of human complement. Biochemistry 11, 3443.
14. Casciola-Rosen, L. A., Anhalt, G., and Rosen, A. (1994). Autoantigens targeted in systemic lupus erythematosus are clustered in two populations of surface structures on apoptotic keratinocytes. J. Exp. Med. 179. 1317-1330.
15. Castellano, G., Woltman, A. M., Nauta, A. J., Roos, A., Trouw, L. A., Seelen, M., Schena, F. B., Daha, M. R., and van Kooten, C. (2004a). Maturation of dendritic cells abrogates C1q production in vivo and in vitro. Blood 103, 3813-3820.
16. Castellano, G., Woltman, A. M., Schena, F. P., Roos, A., Daha, M. R., and van Kooten, C. (2004b). Dendritic cells and complement: at the crossroad of innate and adaptive immunity. Mol. Immunol. 41, 133-140.
17. Chen, A., Gaddipati, S., Volkman, D. J., Peerschke, E. I. B., and Ghebrehiwet, B. (1994). Human T cells possess specific receptors for C1q: role in activation and proliferation. J. Immunol. 153, 1430-1440.
18. Colten, H. R. (1976). Biosynthesis of complement. Adv. Immunol. 22, 67-118.
19. Cooper, N. R. (1985). The classical complement pathway: activation and regulation of the first complement component. Adv. Immunol. 37, 151-216.
20. Ebenbichler, C. F., Thielens, N. M., Vornhagen, R., Marschang, P., Arlaud, G. J., and Dierich, M. P. (1991). Human immunodeficiency virus type 1 activates the classical pathway of complement by direct binding through specific sites in the transmembrane glycoprotein gp41. J. Exp. Med. 174, 1417-1424.
21. Farber, K., Cheung, G., Mitchell, D., Wallis, R., Weihe, E., Schwaeble, W., and Kettenmann, H. (2009). C1q, the recognition subcomponent of the classical pathway of complement, drives microglial activation. J. Neurosci. Res. 87, 644-652.
22. Feng, F., Tonnesen, M. G., Peerschke, E. I. B., and Ghebrehiwet, B. (2002). Cooperation of C1q receptors and integrins in C1q-mediated endothelial cell adhesion and spreading. J. Immunol. 168, 2441-2448.
23. Fogal, V., Zhang, L., Krajewski, S., and Ruoslahti, E. (2008). Mitochondrial/cell-surface protein p32/gC1qR as a molecular target in tumor cells and tumor stroma. Cancer Res. 68, 7210-7218.
24. Gaboriaud, C., Juanhuix, J., Gruez, A., Lacroix, M., Darnault, C., Pignol, D., Verger, D., Fontecilla-Camps, J. C., and Arlaud, G. (2009). The crystal structure of the globular head of complement protein C1q provides a basis for its versatile recognition properties. J. Biol. Chem. 278, 46974-46982.
25. Gaboriaud, C., Païdassi, H., Frachet, P., Tacnet-Delorme, P., Thielens, N. M., and Arlaud, G. J. (2007). "C1q: a versatile pattern recognition molecule and sensor of altered self," in Collagen-Related Lectins in Innate Immunity, Vol. 81, ed. D. Kilpatrick (Research Signpost), 1-15.
26. Gadjeva, M. S., Rouseva, M. M., Zlatarova, A. S., Reid, K. B., Kishore, U., and Kojouharova, M. S. (2008). Interaction of human C1q with IgG and IgM: revisited. Biochemistry 47, 13093-13102.
27. Gardai, S. J., Xiao, Y. Q., Dickinson, M., Nick, J. A., Voelker, D. R., Greene, K. E., and Henson, P. M. (2003). By binding SIRPalpha or calreticulin/CD91, lung collectins act as dual function surveillance molecules to suppress or enhance inflammation. Cell 115, 13-23.
28. Gewurz, H., Ying, S.-C., Jiang, H., and Lint, T. F. (1993). Nonimmune activation of the classical complement pathway. Behring Inst. Mitt. 93, 138-147.
29. Ghai, R., Waters, P., Roumenina, L. T., Gadjeva, M., Kojouharova, M. S., Sim, R. S., Reid, K. B. M., and Kishore, U. (2007). C1q and its growing family. Immunobiology 212, 253-266.
30. Ghebrehiwet, B., Gruber, B., Kew, R. R., Marchese, M. J., Peerschke, E. I. B., and Reid, K. B. M. (1995). Murine mast cells express two types of C1q receptors that are involved in the induction of chemotaxis and chemokinesis. J. Immunol. 155, 2614-2619.
31. Ghebrehiwet, B., Habicht, G. S., and Beck, G. (1990). Interaction of C1q with its receptors on cultured cell lines induces an antiproliferative response. Clin. Immunol. Immunopathol. 54, 148-160.
32. Ghebrehiwet, B., Lim, B.-L., Feng, X., and Peerschke, E. I. B. (2001). gC1q-R/p33, a member of a new class of multifunctional and multicompartmental cellular proteins, is involved in inflammation and infection. Immunol. Rev. 180, 65-77.
33. Ghebrehiwet, B., and Peerschke, E. I. B. (2004a). cC1q-R (calreticulin) and gC1q-R/p33: ubiquitously expressed multi-ligand binding cellular proteins involved in inflammation and infection. Mol. Immunol. 41, 173-183.
34. Ghebrehiwet, B., and Peerschke, E. I. B. (2004b). "Role of C1q and C1q receptors in the pathogenesis of systemic lupus erythematosus,"in Complement in Autoimmunity, Vol. 7, ed. G. C. Tsokos (Basel: S. Karger AG), 87.
35. Ghebrehiwet, B., Tantral, L., Titmus, M. A., Panessa-Warren, B. J., Tortora, G. T., Wong, S. S., and Warren, J. B. (2009). The exosporium of B. cereus contains a binding site for gc1qr/p33: implication in spore attachment and/or entry. Adv. Exp. Med. Biol. 598, 181-187.
36. Gulati, P., Lemercier, C., Guc, D., and Whaley, K. (1993). Regulation of the synthesis of C1 subcomponents and C1-inhibitor. Behring Inst. Mitt. 93, 196-203.
37. Hakansson, K., and Reid, K. B. M. (2000). Collectin structure: a review. Protein Sci. 9, 1607-1617.
38. Hayward, C. P., Hassell, J. A., Denomme, G. A., Rachubinski, R. A., Brown, C., and Kelton, J. G. (1995). The cDNA sequence of human endothelial cell multimerin. a unique protein with RGDS, coiled-coil, and epidermal growth factor-like domains and a carboxyl terminus similar to the globular domain of complement C1q and collagen type VIII and X. J. Biol. Chem. 270, 18246-18251.
39. Hoekzema, R., Brouwer, M. C., de Graeff-Meeder, E. R., van Helden, H. T. P., and Hack, C. E. (1989). Biosynthesis of normal and low-molecularmass complement component C1q by cultured human monocytes and macrophages. Biochem. J. 257, 477-486.
40. Hoekzema, R., Brouwer, M. C., and Hack, C. E. (1987). Production of LWM-C1q by monocytes from SLE patients and normal individuals. Complement 4, 169.
41. Hoekzema, R., Hannema, A. J., Swaak, T. J. G., Paardekooper, J. Q., and Hack, C. E. (1985). Low molecular weight C1q in systemic lupus erythematosus. J. Immunol. 135, 265-271.
42. Hong, Q., Sze, C.-I., Lin, S.-R., Lee, M.H., He, R.-Y., Schultz, L., Chang, J.Y., Chen, S.-J., Boackle, R. J., Hsu, L.-J., and Chang, N.-S. (2009). Complement C1q activates tumor suppressor wwox to induce apoptosis in prostate cancer cells. PLoS ONE 4, e5755. doi:10.1371/journal.pone.0005755.
43. Hoppe, H.-J., and Reid, K. B. M. (1994). Trimeric C-type lectin domains in host defence. Curr. Biol. 2, 1129.
44. Hosszu, K. K., Santiago-Schwarz, F., Peerschke, E. I., and Ghebrehiwet, B. (2008). C1q is a molecular switch dictating the monocyte to dendritic cell (DC) transition and arrests DCs in an immature phenotype. FASEB J. 22, 673.1.
45. Hosszu, K. K., Santiago-Schwarz, F., Peerschke, E. I. B., and Ghebrehiwet, B. (2010). Evidence that a C1q/C1qR system regulates monocyte-derived dendritic cell differentiation at the interface of innate and acquired immunity. Int. Immunol. 16, 115-127.
46. Hu, E., Liang, P., and Spiegelman, P. M. (1996). AdipoQ is a novel adiposespecific gene dysregulated in obesity. J. Biol. Chem. 271, 10697-10703.
47. Jiang, H., Burdick, D., Glabe, C. G., Cotman, C. W., and Tenner, A. J. (1994). Beta amyloid activates complement by binding to a specific region of the collagen-like domain of the C1q A-chain. J. Immunol. 152, 5050-5059.
48. Jiang, H. X., Siegel, J. N., and Gewurz, H. (1991). Binding and complement activation by C-reactive protein via the collagen-like region of C1q and inhibition of these reactions by monoclonal antibodies to C-reactive protein and C1q. J. Immunol. 146, 2324-2330.
49. Kavety, B., Jenkins, N. A., Fletcher, C. F., Copeland, N. G., and Morgan, J. I. (1994). Genomic structure and mapping of precerebellin and a precerebellin-related gene. Brain Res. Mol. Brain Res. 27, 152-156.
50. Kim, K.-B., Yi, J.-S., Nguyen, N., Lee, J.-H., Kwon, Y.-C., Ahn, B.-Y., Cho, H., Kim, Y. K., Yoo, H.-J., Lee, J.S., and Ko, Y.-G. (2001). Cell-surface receptor for complement component C1q (gC1qR) is a key regulator for lamellipodia formation and cancer metastasis. J. Biol. Chem. 286, 23093-23101.
51. Kishore, U., Gaboriaud, C., Waters, P., Shrive, A. K., Greenhough, T. J., Reid, K. B. M., Sim, R. B., and Arlaud, G. J. (2004). C1q and tumor necrosis factor superfamily: modularity and versatility. Trends Immunol. 25, 551-561.
52. Kishore, U., Gupta, S. K., Perdikoulis, M. D., Kojouharova, M. S., Urban, B. C., and Reid, K. B. M. (2003). Modular organization of the carboxyterminal globular head region of human C1q A, B, and C chains. J. Immunol. 171, 812-820.
53. Kishore, U., Kojouharova, M. S., and Reid, K. B. M. (2002). Recent progress in the understanding of the structure-function relationships of the globular head region of C1q. Immunobiology 205, 355-364.
54. Kishore, U., and Reid, K. B. M. (1999). Modular organization of proteins containing C1q-like globular domain. Immunopharmacology 42, 15-21.
55. Kishore, U., and Reid, K. B. M. (2000). C1q: structure, function and receptors. Immunopharmacology 49, 159-170.
56. Knobel, H. R., Heuser, C., Rodrick, M. L., and Isliker, H. (1974). Enzymatic digestion of the first component of human complement C1q. J. Immunol. 112, 2094-2101.
57. Knobel, H. R., Villiger, W., and Isliker, H. (1975). Chemical analysis and electron microscopy studies of human C1q prepared by different methods. Eur. J. Immunol. 5, 78.
58. Kojouharova, M. S., Gadjeva, M. D., Tzacheva, I. G., Zlatorova, A., Roumenina, L. T., Tchorbadjieva, M. I., Atanasov, B. P., Waters, P., Urban, B. C., Sim, R. B., Reid, K. B. M., and Kishore, U. (2004). Mutational analyses of the recombinant globular regions of human C1qA, B and C chains suggest an essential role for arginine and histidine residues in the C1q-IgG interaction. J. Immunol. 172, 4351-4358.
59. Kojouharova, M. S., Tsacheva, I. G., Tchorbadjieva, M. I., Reid, K. B. M., and Kishore, U. (2003). Localization of ligand-binding sites on human C1q globular head region using recombinant globular head fragments and single-chain antibodies. Biochim. Biophys. Acta 1652, 64-74.
60. Kolosov, M., Kolosova, I., Zhou, A., and Leu, R. W. (1996). Autocrine induction of macrophage synthesis of complement subcomponent C1q by endogenous interferonalpha/beta. J. Interferon Cytokine Res. 16, 209-215.
61. Komatsu, A., Komazawa, M., Murakami, M., and Nagaki, Y. (1982). A case of selective C1qdeficiency with SLE-like symptoms. J. Jpn. Pediatr. Soc. 86, 23-27.
62. Korb, L. C., and Ahearn, J. M. (1997). C1q binds directly and specifically to surface blebs of apoptotic human keratinocytes: complement deficiency and systemic lupus erythematosus revisited. J. Immunol. 158, 4527-4529.
63. Kuna, P., Iyer, M., Peerschke, E. I. B., Kaplan, A. P., Reid, K. B. M., and Ghebrehiwet, B. (1996). Human C1q induces eosinophil migration. Clin. Immunol. Immunopathol. 81, 48-54.
64. Leigh, L. E., Ghebrehiwet, B., Perera, T. P., Bird, I. N., Strong, P., Kishore, U., Reid, K. B. M., and Eggleton, P. (1998). C1q-mediated chemotaxis by human neutrophils: involvement of gClqR and G-protein signalling mechanisms. Biochem. J. 330, 247-254.
65. Loos, M. (1983). Biosynthesis of the collagen-like C1q molecule and its receptor function for Fc and polyanionic molecules on macrophages. Curr. Top. Microb. Immunol. 102, 1-56.
66. Lu, J., Wiedemann, H., Timpl, R., and Reid, K. B. M. (1993). Similarity in structure between C1q and the collectins as judged by electron microscopy. Behring Inst. Mitt. 93, 6-16.
67. Lynch, N. J., Willis, C. L., Nolan, C. C., Roscher, S., Fowler, M. J., Weihe, E., Ray, D. E., and Schwaeble, W. J. (2004). Microglial activation and increased synthesis of complement component C1q precedes bloodbrain barrier dysfunction in rats. Mol. Immunol. 40, 709-716.
68. Malhotra, R., Lu, J., Thiel, S., Jensenius, J.-C., Willis, A. C., and Sim, R. B. (1992). C1q receptor (collectin receptor): primary structure, homology, and interaction with ligands. Immunobiology 184, 437.
69. Marques, G. J., Anton, L. C., Barrio, E., Sanchez, A., Ruiz, S., Gavilanes, F., and Vivanco, F. (1993). Arginine residues of the globular regions of human C1q involved in the interaction with immunoglobulin G. J. Biol Chem. 268, 10393-10402.
70. Martin, H., and Loos, M. (1988). Guinea pig macrophages synthesize a low molecular weight form of C1q with affinity for the C1r2C1s2-complex but which does not bind to Fc in immunoglobulin aggregates. Mol. Immunol. 25, 1231-1237.
71. Menzies, C. A., Habiel, D., Glassberg, P. F., Nguyen, P. P., Jesty, P., Peerschke, E. I. B., and Ghebrehiwet, B. (2008). Identification of C1q receptor associated surface molecules on the monocyte-like cell line U937. FASEB J. 22, abstr. 673.3.
72. Mizuochi, T., Yonemasu, K., Yamashita, K., and Kobata, A. (1979). The asparagine-linked sugar chains of subcomponent C1q of the first component of human complement. J. Biol. Chem. 253, 7407-7409.
73. Moosig, F., Damm, F., Knorr-Spar, A., Ritgen, M., Zeuner, R. A., Kneba, M., Emst, M., and Schröder, J. O. (2006). Reduced expression of C1qmRNA in monocytes from patients with systemic lupus erythematosus. Clin. Exp. Immunol. 146, 409-416.
74. Morris, K. M., Colten, H. R., and Bing, D. H. (1978). The first component of complement. a quantitative comparison of its biosynthesis in culture by human epithelial and mesenchymal cells. J. Exp. Med. 148, 1007-1019.
75. Nauta, A. J., Touw, L. A., Daha, M. R., Tijsma, O., Nieuwland, R., Schwaeble, W. J., Gingras, A. R., Mantovani, A., Hack, E. C., and Roos, A. (2002). Direct binding of C1q to apoptotic cells and cell blebs induces complement activation. Eur. J. Immunol. 32, 1726-1736.
76. Nayak, A., Ferluga, J., Tsolaki, A. G., and Kishore, U. (2010). The non-classical functions of the classical complement pathway recognition subcomponent C1q. Immunol. Lett. 131, 139-150.
77. Nepomuceno, R. R., Henschen, E. A., Burgess, W. H., and Tenner, A. J. (1997). cDNA cloning and primary structure analysis of C1qR (P), the human C1q/MBL/SPA receptor that mediates enhanced phagocytosis in vitro. Immunity 6, 119-129.
78. Nishino, H., Shibuya, K., Nishida, Y., and Mushimoto, M. (1981). Lupus erythematosus-like syndrome with selective C1q complete deficiency of C1q. Ann. Intern. Med. 95, 322-324.
79. Ogden, C. A., deCathelineau, A., Hoffmann, P. R., Braton, D., Ghebrehiwet, B., Fadok, V. A., and Henson, P. M. (2001). C1q and mannose binding lectin (MBL) engagement of cell surface calreticulin and CD91 initiates macropinocytosis and uptake of apoptotic cells. J. Exp. Med. 194, 781-795.
80. Païdassi, H., Tacnet, P., Garlatti, V., Darnault, C., Ghebrehiwet, B., Gaboriaud, C., Arlaud, G. J., and Frachet, P. (2008). C1q binds phosphatidylserine and likely acts as a multiligand bridging molecule in apoptotic cell recognition. J. Immunol. 180, 2329-2338.
81. Païdassi, H., Tacnet-Delorme, P., Verneret, M., Gaboriaud, C., Houen, G., Duus, K., Ling, W. L., Arlaud, G. J., and Frachet, P. (2011). Investigations on the C1qcalreticulin-phosphatidylserine interactions yield new insights into apoptotic cell recognition. J. Mol. Biol. 408, 277-290.
82. Peerschke, E. I. B., Dembitzer, F. R., Kinoshita, Y., Burstein, D., Phelps, R., and Ghebrehiwet, B. (2011). Differential expression of gC1qR in normal and pathologic human tissue. Mol. Immunol. 48, abstr. 1718.
83. Peerschke, E. I. B., Minta, J. O., Zhou, S. Z., Bini, A., Gotlieb, A., Colman, R. W., and Ghebrehiwet, B. (2004). gC1q-R/p33 expression on human coronary artery atherosclerotic lesions. Mol. Immunol. 41, 759-766.
84. Pickering, M. C., Botto, M., Taylor, P. R., Lachmann, P. J., and Walport, M. J. (2000). Systemic lupus erythematosus, complement deficiency, and apoptosis. Adv. Immunol. 76, 227-234.
85. Reid, K. B. M. (1979). Complete amino acid sequences of the three collagenlike regions present in subcomponent C1q of the first component of human complement. Biochem. J. 179, 367-371.
86. Reid, K. B. M. (1985). Molecular cloning and characterization of the complementary DNA and gene coding for the B chain subcomponent C1q of the human complement system. Biochem. J. 231, 729.
87. Reid, K. B. M. (1989). C1q: genes, biosynthesis and biology. Behring Inst. Mitt. 84, 8-19.
88. Reid, K. B. M., Lowe, D. M., and 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.
89. Reid, K. B. M., and Solomon, E. (1977). Biosynthesis of the first component of complement by human fibroblasts. Biochem. J. 167, 647-660.
90. Reid, K. B. M., and Thompson, R. A. (1983). Characterization of nonfunctional form of C1q found in patients with genetically linked deficiency of C1q activity. Immunology 20, 1117-1125.
91. Rety, S., Salamitou, S., Garcia-Verdugo, I., Hulmes, D. J. S., Le Hagarat, F., Chaby, R., and Lewit-Bentley, A. (2005). The crystal structure of the Bacillus anthracis spore surface protein, BclA, shows remarkable similarity to mammalian proteins. J. Biol. Chem. 280, 43073-43078.
92. Rubinstein, D. B., Stortchevoi, A., Boosalis, M., Ashfaq, R., Ghebrehiwet, B., Peerschke, E. I. B., Calvo, F., and Gillaume, T. (2004). Receptor for the globular heads of C1q (gC1qR; p33; hyaluronan-binding protein) is preferentially expressed by adenocarcinoma cells. Int. J. Cancer 110, 741-750.
93. Scherer, P. E., Williams, S., Fogliano, M., Baldini, G., and Lodish, H. F. (1995). A novel serum protein similar to C1q, produced exclusively in adipocytes. J. Biol. Chem. 270, 26746-26749.
94. Schumaker, V. N., Zavodsky, P., and Poon, P. H. (1987). Activation of the first component of complement. Annu. Rev. Immunol. 5, 21-42.
95. Sellar, G. C., Blake, D. J., and Reid, K. B. M. (1991). Characterization and organization of the genes encoding the A-, B-, and Cchains of human complement subcomponent C1q. Biochem. J. 274, 481.
96. Shapiro, L., and Scherer, P. E. (1998). The crystal structure of a complement-1q family of protein suggests an evolutionary link to tumor necrosis factor. Curr. Biol. 8, 335-338.
97. Shelton, E., Yonemasu, K., and Stroud, R. M. (1972). Ultrastructure of the human complement component C1q. Proc. Natl. Acad. Sci. U.S.A. 69, 65-68.
98. Shinkai, H., and Yonemasu, K. (1979). Hydroxylysine-linked glycosides of human complement subcomponent C1q and of various collagens. Biochem. J. 177, 847-852.
99. Singh, J., Ahmed, A., and Girardi, G. (2011). Role of complement component C1q in the onset of preeclampsia in mice. Hypertension 58, 716-724.
100. Skok, J., Solomon, E., Reid, K. B. M., and Thompson, R. A. (1981). Distinct genes for fibroblast and serum C1q, Nature 292, 549-551.
101. Sontheimer, R. D., Racila, D., Racila, E., Eggleton, P., and Donnelly, S. (2003). "Calreticulin's role(s) in autoimmune disorders,"in Calreticulin, 2nd Edn, eds P. Eggleton and M. Michalak (New York: Eurekah.com and Kluwer Academic/Plenum Publishing), 180-192.
102. Sontheimer, R. D., Racila, E., and Racila, D. M. (2005). C1q: its functions within the innate and adaptive immune responses and its role in lupus autoimmunity. J. Invest. Dermatol. 125, 14-23.
103. Steinberger, A. S., Wille, S., Stöckl, J., Selenko, N., Prager, E., Staffler, G., Madic, O., Stockinger, H., and Knapp, W. (2002). Identification of human CD93 as the phagocytic C1q receptor (C1qRp) by expression cloning. J. Leukoc. Biol. 71, 133-140.
104. Svehag, S. E., Manheim, L., and Bloth, B. (1972). Ultrastructure of human C1q protein. Nature New Biol. 238, 117.
105. Sylvestre, P., Couture-Tosi, E., and Mock, M. (2002). A collagen-like surface structure glycoprotein is a structural component of the Bacillus anthracis exosporium. Mol. Microbiol. 45, 169-178.
106. Tacnet, P., Cheong, E. C. C., Goeltz, P., Ghebrehiwet, B., Arlaud, G. J., Liu, X.-Y., and Lesieur, C. (2008). Trimeric reassembly of the globular domain of human C1q. Biochim. Biophys. Acta 1784, 518-529.
107. Tacnet-Delorme, P., Chevallier, S., and Arlaud, G. J. (2001). Beta-amyloid fibrils activate the C1 complex of complement under physiological conditions: evidence for a binding site for A beta on the C1q globular regions. J. Immunol. 167, 6374-6638.
108. Tenner, A. J., and Cooper, N. R. (1982). Stimulation of a human polymorphonuclear leukocyte oxidative response by the C1q subunit of the first component of complement. J. Immunol. 128, 2547-2552.
109. Tenner, A. J., and Volkin, D. B. (1986). Complement subcomponent C1q secreted by cultured human monocytes has a subunit structure identical with that of serum C1q. Biochem. J. 233, 451-458.
110. Tosato, G., Yao, L., and Pike, S. E. (2003)."Calreticulin and tumor suppression," in Calreticulin, 2nd Edn, eds P. Eggleton and M. Michalak (New York: Eurekah.com and Kluwer Academic/Plenum Publishing), 161-179.
111. 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., and Greene, K. E. (2002). Role of surfactant proteinsA, 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.
112. Vegh, Z., Goyarts, E. C., Rozengarten, K., Mazumder, A., and Ghebrehiwet, B. (2003). Maturationdependent expression of C1q binding proteins on the cell surface of monocyte-derived dendritic cells. Int. Immunopharmacol. 3, 345-357.
113. Vegh, Z., Kew, R., Gruber, B., and Ghebrehiwet, B. (2005). Chemotaxis of human monocyte derived dendritic cells toward C1q is mediated by gC1qR and cC1qR. Mol. Immunol. 43, 1402-1407.
114. Walport, M. J., Davies, K. A., and Botto, M. (1998). C1q and systemic lupus erythematosus. Immunobiology 199, 265-285.
115. Wong, G. W., Wang, J., Hug, C., Tsao, T.-S., and Lodish, H. F. (2004). A family of Acrp30/adiponectin structural and functional paralogs. Proc. Natl. Acad. Sci. U.S.A. 101, 10302-10307.
116. Yonemasu, K., Stroud, R. M., Neidermeier, W., and Butler, W. T. (1971). Chemical studies on C1q a modulator of immunoglobulin biology. Biochem. Biophys. Res. Commun. 43, 1388-1394.