Monocyte expressed macromolecular C1 and C1q receptors as molecular sensors of danger: Implications in SLE

Frontiers in Immunology

Volumn 5, Issue JUN, 2014, Pages

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

^a STONY BROOK UNIVERSITY   (United States)

^b MEMORIAL SLOAN KETTERING CANCER CENTER   (United States)

Author keywords

C1q; C1q and C1q receptors; C1q in autoimmunity; C1q in SLE; DC and C1; Monocyte C1

Indexed keywords

EID: 84905656603     PISSN: None     EISSN: 16643224     Source Type: Journal    
DOI: 10.3389/fimmu.2014.00278     Document Type: Review

References (66)

1. Swirski FK, Nahrendorf M, Etzrodt M, Wildgruber M, Cortez-Retamozo V, Panizzi P, et al. Identification of splenic reservoir monocytes and their deployment to inflammatory sites. Science (2009) 325:612-6. doi: 10.1126/science.1175202
2. Ziegler-Heitbrock L, Ancuta P, Crowe S, Dalod M, Grau V, Hart DN, et al. Nomenclature of monocytes and dendritic cells in blood. Blood (2010) 116:74-80. doi:10.1182/blood-2010-02-258558
3. Medzhitov R. Toll-like receptors and innate immunity. Nat Rev Immunol (2001) 1:135-45. doi:10.1038/35100529
4. Ghebrehiwet B, Peerschke EI. cC1qR (calreticulin) and gC1qR/p33: ubiquitously expressed multi-ligand binding cellular proteins involved in inflammation and infection. Mol Immunol (2004) 41:173-83. doi:10.1016/j.molimm.2004.03.014
5. Ghebrehiwet B, Hosszu KK, Valentino A, Peerschke EI. The C1q family of proteins: insights into the emerging non-traditional functions. Front Immunol (2012) 3:52. doi:10.3389/fimmu.2012.00052
6. Randazzo BP, Dattwyler RJ, Kaplan AP, Ghebrehiwet B. Synthesis of C1 inhibitor (C1-INA) by a human monocyte-like cell line, U937. J Immunol (1985) 135:1313-9.
7. Hosszu KK, Valentino A, Ji Y, Matkovic M, Pednekar L, Rehage N, et al. Cell surface expression and function of the macromolecular C1 complex on the surface of human monocytes. Front Immunol (2012) 3:38-43. doi:10.3389/fimmu.2012.00038
8. Inaba K, Pack M, Inaba M, Sakuta H, Isdell F, Steinman RM. High levels of major histocompatibility complex II-self peptide complex on dendritic cells from the T cell areas of lymph nodes. J Exp Med (1997) 186:665-72. doi:10.1084/jem.186.5.665
9. Banchereau J, Steinman R. Dendritic cells and the control of immunity. Nature (1998) 392:245-52. doi:10.1038/32588
10. Albert ML, Pearce SF, Francisco LM, Sauter B, Roy P, Silverstein RL, et al. Immature dendritic cells phagocytose apoptotic cells via alpha 5 and CD36, and cross-present antigens to cytotoxic T lymphocytes. J Exp Med (1998) 188:1359-68. doi:10.1084/jem.188.7.1359
11. Steinman RM, Turley S, Mellman I, Inaba K. The induction of tolerance by dendritic cells that have captured apoptotic cells. J Exp Med (2000) 191:411-6. doi:10.1084/jem.191.3.411
12. Kadowaki N, Ho S, Antonenko S, Malefyt RW, Kastelein RA, Bazan F, et al. Subsets of human dendritic cells precursors express different toll-like receptors and respond to different microbial antigens. J Exp Med (2001) 194:863-9. doi:10.1084/jem.194.6.863
13. Figdor CG, van Kooyk Y, Adema GJ. C-type lectin receptors on dendritic cells and Langerhans cells. Nat Rev Immunol (2002) 2:77-84. doi:10.1038/nri827
14. Steinman RM, Hawiger D, Nussensweig MC. Tolerogenic dendritic cells. Ann Rev Immunol (2003) 21:685-711. doi:10.1146/annurev.immunol.21.120601.141040
15. Pettit AR, Thomas R. Dendritic cells: the driving force behind autoimmunity in rheumatoid arthritis? Immunol Cell Biol (1999) 77:420-7. doi:10.1046/j.1440-1711.1999.00855.x
16. Kapsenberg ML. Dendritic-cell control of pathogen-driven T-cell polarization. Nat Rev Immunol (2003) 3:984-93. doi:10.1038/nri1246
17. Moser M. Dendritic cells in immunity and tolerance - do they display opposite functions? Immunity (2003) 19:5-8. doi:10.1016/S1074-7613(03)00182-1
18. Scandella E, Ludewig B. Dendritic cells and autoimmunity. Transfus Med Hemother (2005) 32:363-8. doi:10.1159/000089124
19. Bensa JC, Reboul A, Colomb MG. Biosynthesis in vitro of complement subcomponents C1q, C1s and C1 inhibitor by resting and stimulated human monocytes. Biochem J (1983) 216:385-92.
20. Tenner AJ, Volkin DB. Complement subcomponent C1q secreted by cultured human monocytes has a subunit structure identical with that of serum C1q. Biochem J (1986) 233:451-8.
21. Drouet C, Reboul A. Biosynthesis of C1r and C1s subcomponents. Behring Inst Mitt (1989) 84:80-8.
22. Gulati P, Lemercier C, Guc D, Lappin D, Whaley K. Regulation of the synthesis of C1 subcomponents and C1-inhibitor. Behring Inst Mitt (1993) 93:196-203.
23. Lu J, Le Y, Kon OL, Chan J, Lee SH. Biosynthesis of human ficolin, an Escherichia coli-binding protein, by monocytes: comparison with the synthesis of two macrophage-specific proteins, C1q and the mannose receptor. Immunology (1996) 89:289-94.
24. Moosig F, Damm F, Knorr-Spahr A, Ritgen M, Zeuner RA, Kneba M, et al. Reduced expression of C1q-mRNA in monocytes from patients with systemic lupus erythematosus. Clin Exp Immunol (2006) 146:409-16. doi:10.1111/j.1365-2249.2006.03225.x
25. Loos M. Biosynthesis of the collagen-like C1q molecule and its receptor function for Fc and polyanionic molecules on macrophages. Curr Top Microb Immuno (1983) 102:1-56.
26. Kaul M, Loos M. Collagen-like complement component C1q is a membrane protein of human monocyte-derived macrophages that mediates endocytosis. J Immunol (1995) 155:5795-802.
27. Kaul M, Loos M. Expression of membrane C1q in human monocyte-derived macrophages is developmentally regulated and enhanced by interferon-gamma. FEBS Lett (2001) 500:91-8. doi:10.1016/S0014-5793(01)02592-3
28. Vegh Z, Goyarts EC, Rozengarten K, Mazumder A, Ghebrehiwet B. Maturation-dependent expression of C1q-binding proteins on the cell surface of human monocyte-derived dendritic cells. Int Immunopharmacol (2003) 3:345-57. doi:10.1016/S1567-5769(02)00211-4
29. Castellano G, Woltman AM, Nauta AJ, Roos A, Trouw LA, Seelen MA, et al. Maturation of dendritic cells abrogates C1q production in vivo and in vitro. Blood (2004) 103:3813-20. doi:10.1182/blood-2003-09-3046
30. Hosszu KK, Valentino A, Vinayagasundaram U, Vinayagasundaram R, Joyce MG, Ji Y, et al. DC-SIGN, C1q and gC1qR form a tri-molecular receptor complex on the surface of monocyte-derived immature dendritic cells. Blood (2012) 120:1228-36. doi:10.1182/blood-2011-07-369728
31. Walport MJ, Davies KA, Botto M. C1q and systemic lupus erythematosus. Immunobiology (1998) 199:265-85. doi:10.1016/S0171-2985(98)80032-6
32. Walport MJ. Complement and systemic lupus erythematosus. Arthritis Res (2002) 4(Suppl 3):S279-93. doi:10.1186/ar586
33. Pickering MC, Botto M, Taylor PR, Lachmann PJ, Walport MJ. Systemic lupus erythematosus, complement deficiency, and apoptosis. Adv Immunol (2000) 76:227-34. doi:10.1016/S0065-2776(01)76021-X
34. Ghebrehiwet B, Peerschke EI. Role of C1q and C1q receptors in the pathogenesis of systemic lupus erythematosus. Curr Dir Autoimmun (2004) 7:87-97. doi:10.1159/000075688
35. Hosszu KK, Santiago-Schwarz F, Peerschke EI, Ghebrehiwet B. Evidence that a C1q/C1qR system regulates monocyte-derived dendritic cell differentiation at the interface of innate and acquired immunity. Innate Immun (2010) 16:115-27. doi:10.1177/1753425909339815
36. Lahita RG. Systemic Lupus Erythematosus. 3rd ed. San Diego, CA: Academic Press (1999).
37. Liu C-C, Navratil JS, Sabine JM, Ahearn JM. Apoptosis, complement and systemic lupus erythematosus: a mechanistic view. In: Tsokos GC, editor. Complement in Autoimmunity. (Vol. 7), Basel: Karger (2004). p. 49-86.
38. Nishino H, Shibuya K, Nishida Y, Mushimoto M. Lupus erythematosus-like syndrome with selective C1q complete deficiency of C1q. Ann Intern Med (1981) 95:322-4. doi:10.7326/0003-4819-95-3-322
39. Komatsu A, Komazawa M, Murakami M, Nagaki Y. A case of selective C1q-deficiency with SLE-like symptoms. J Jpn Pediatr Soc (1982) 86:23-6.
40. Botto M. C1q knockout mice for the study of complement deficiency in autoimmune disease. Exp Clin Immunogenet (1998) 15:231-4. doi:10.1159/000019076
41. Kishore U, Kojouharova MS, Reid KBM. Recent progress in the understanding of the structure-function relationships of the globular head region of C1q. Immunobiology (2002) 205:355-64. doi:10.1078/0171-2985-00138
42. Nauta AJ, Trouw LA, Daha MR, Tijsma O, Nieuwland R, Schwaeble WJ, et al. Direct binding of C1q to apoptotic cells and cell blebs induces complement activation. Eur J Immunol (2002) 32:1726-36. doi:10.1002/1521-4141(200206)32:6>1726::AID-IMMU1726>3.0.CO;2-R
43. Gaboriaud C, Païdassi H, Frachet P, Tacnet-Delorme P, Thielens NM, Arlaud GJ. C1q: a versatile pattern recognition molecule and sensor of altered self. In: Kilpatrick D, editor. Collagen-Related Lectins in Innate Immunity. (Vol. 81), New York: Research Signpost (2007). p. 1-15.
44. Païdassi H, Tacnet P, Garlatti V, Darnault C, Ghebrehiwet B, Gaboriaud C, et al. C1q binds phosphatidylserine and likely acts as a multiligand bridging molecule in apoptotic cell recognition. J Immunol (2008) 180:2329-38. doi:10.4049/jimmunol.180.4.2329
45. Bally I, Ancelet S, Moriscot C, Gonnet F, Mantovani A, Daniel R, et al. Expression of recombinant human complement C1q allows identification of the C1r/C1s-binding sites. Proc Natl Acad Sci U S A (2013) 110:8650-5. doi:10.1073/pnas.1304894110
46. Casciola-Rosen LA, Anhalt G, Rosen A. Autoantigens targeted in systemic lupus erythematosus are clustered in two populations of surface structures on apoptotic keratinocytes. J Exp Med (1994) 179:1317-30. doi:10.1084/jem.179.4.1317
47. Korb LC, Ahearn JM. C1q binds directly and specifically to surface blebs of apoptotic human keratinocytes: complement deficiency and systemic lupus erythematosus revisited. J Immunol (1997) 158:4527-9.
48. Ogden CA, deCathelineau A, Hoffmann PR, Braton D, Ghebrehiwet B, Fadok VA, et al. C1q and mannose binding lectin (MBL) engagement of cell surface calreticulin and CD91 initiates macropinocytosis and uptake of apoptotic cells. J Exp Med (2001) 194:781-95. doi:10.1084/jem.194.6.781
49. Vandivier RW, Ogden CA, Fadok VA, Hoffmann PR, Brown KK, Botto M, et al. 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 (2002) 169:3978-86. doi:10.4049/jimmunol.169.7.3978
50. Nauta AJ, Castellano G, Xu W, Woltman AM, Borrias MC, Daha MR, et al. Opsonization with C1q and mannose-binding lectin targets apoptotic cells to dendritic cells. J Immunol (2004) 173:3044-50. doi:10.4049/jimmunol.173.5.3044
51. Chen A, Gaddipati S, Volkman DJ, Peerschke EIB, Ghebrehiwet B. Human T cells possess specific receptors for C1q: role in activation and proliferation. J Immunol (1994) 153:1430-40.
52. Szabo J, Cervenak L, Toth FD, Prohaszka Z, Horvath L, Kerekes K, et al. Soluble gC1q-R/p33, a cell protein that binds to the globular "heads" of C1q, effectively inhibits the growth of HIV-1 strains in cell cultures. Clin Immunol (2001) 99:222-31. doi:10.1006/clim.2001.5013
53. Kittlesen DJ, Chianese-Bullock KA, Yao ZQ, Braciale TJ, Hahn YS. Interaction between complement receptor gC1qR and hepatitis C virus core protein inhibits T-lymphocyte proliferation. J Clin Immunol (2000) 106:1239-49.
54. Gardai SJ, Xiao YQ, Dickinson M, Nick JA, Voelker DR, Greene KE, et al. By binding SIRPalpha or calreticulin/CD91, lung collectins act as dual function surveillance molecules to suppress or enhance inflammation. Cell (2003) 115:13-23. doi:10.1016/S0092-8674(03)00758-X
55. Ghebrehiwet B, Jesty J, Vinayagasundaram U, Vinayagasundaram R, Ji Y, Valentino A, et al. Targeting gC1qR domains for therapy against infection and inflammation. Adv Exp Med Biol (2013) 735:97-110. doi:10.1007/978-1-4614-4118-2_6
56. Steino A, Jorgensen CS, Laursen I, Houen G. Interaction of C1q with the receptor calreticulin requires a conformational change in C1q. Scand J Immunol (2004) 59:485-95. doi:10.1111/j.0300-9475.2004.01425.x
57. Shortman K, Caux C. Dendritic cell development: multiple pathways to nature's adjuvants. Stem Cells (1997) 15:409-19. doi:10.1002/stem.150409
58. Banchereau J, Briere F, Caux C, Davoust J, Lebecque S, Liu Y-J, et al. Immunobiology of dendritic cells. Annu Rev Immunol (2000) 18:767-811. doi:10.1146/annurev.immunol.18.1.767
59. Reid SD, Penna G, Adorini L. The control of T cell responses by dendritic cell subsets. Curr Opin Immunol (2000) 12:114-21. doi:10.1016/S0952-7915(99)00059-X
60. Csomor E, Bajtay Z, Sandor N, Krsitof K, Arlaud GJ, Thiel S, et al. Complement protein C1q induces maturation of human dendritic cells. Mol Immunol (2007) 44:3389-97. doi:10.1016/j.molimm.2007.02.014
61. Pastva AM, Wright JR, Williams KL. Immunomodulatory roles of surfactant proteins A and D: implications in lung disease. Proc Am Thorac Soc (2007) 4:252-7. doi:10.1513/pats.200701-018AW
62. Yamada M, Oritani K, Kaisho T, Ishikawa J, Yoshida H, Takahashi I, et al. Complement C1q regulates LPS-induced cytokine production in bone marrow-derived dendritic cells. Eur J Immunol (2004) 34:221-30. doi:10.1002/eji.200324026
63. Baruah P, Dumitriu IE, Malik TH, Cook HT, Dyson J, Scott D, et al. C1q enhances IFN-? production by antigen specific T cells via the CD40 co-stimulatory pathway on dendritic cells. Blood (2009) 113:3485-93. doi:10.1182/blood-2008-06-164392
64. Waggoner SN, Cruise MW, Kassel R, Hahn YS. gC1q receptor ligation selectively down-regulates human IL-12 production through activation of the phosphoinositide 3-kinase pathway. J Immunol (2005) 175:4706-14. doi:10.4049/jimmunol.175.7.4706
65. Gringhuis SI, den Dunnen J, Litjens M, van Het Hof B, van Kooyk Y, Geijtenbeek TB. C-type lectin DC-SIGN modulates toll-like receptor signaling via Raf-1 kinase-dependent acetylation of transcription factor NF-kappaB. Immunity (2007) 26:605-16. doi:10.1016/j.immuni.2007.03.012
66. Caparros E, Munoz P, Sierra-Filardi E, Serrano-Gomez D, Puig-Kröger A, Rodriguez-Fernandez JL, et al. DC-SIGN ligation on dendritic cells results in ERK and PI3K activation and modulates cytokine production. Blood (2006) 107:3950-8. doi:10.1182/blood-2005-03-1252