The non-classical functions of the classical complement pathway recognition subcomponent C1q

Immunology Letters

Volumn 131, Issue 2, 2010, Pages 139-150

  Nayak, Annapurna ^a   Ferluga, Janez ^a   Tsolaki, Anthony G ^a   Kishore, Uday ^a  

^a BRUNEL UNIVERSITY   (United Kingdom)

Author keywords

Adaptive immunity; Apoptotic cells; C1q; Coagulation; Development; Immune cells; Innate immunity

Indexed keywords

ALPHA INTERFERON; COMPLEMENT COMPONENT C1Q; PENTRAXIN 3; TUMOR NECROSIS FACTOR ALPHA;

ADAPTIVE IMMUNITY; APOPTOSIS; ARTICLE; B LYMPHOCYTE; BLOOD CLOTTING; CELL ACTIVATION; CELL INTERACTION; CELL MATURATION; CELL MIGRATION; COMPLEMENT CLASSICAL PATHWAY; CYTOKINE PRODUCTION; DENDRITIC CELL; HUMAN; LYMPHOCYTE DIFFERENTIATION; MICROGLIA; NONHUMAN; PATHOGENESIS; PREGNANCY; PRION DISEASE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN STRUCTURE; T LYMPHOCYTE; ANIMAL; CELL COMMUNICATION; DEFICIENCY; DEGENERATIVE DISEASE; FEMALE; IMMUNOLOGY; INNATE IMMUNITY; METABOLISM; PREGNANCY COMPLICATION; SYSTEMIC LUPUS ERYTHEMATOSUS;

ADAPTIVE IMMUNITY; ANIMALS; APOPTOSIS; BLOOD COAGULATION; CELL COMMUNICATION; COMPLEMENT C1Q; COMPLEMENT PATHWAY, CLASSICAL; FEMALE; HUMANS; IMMUNITY, INNATE; LUPUS ERYTHEMATOSUS, SYSTEMIC; NEURODEGENERATIVE DISEASES; PREGNANCY; PREGNANCY COMPLICATIONS;

EID: 77953712553     PISSN: 01652478     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.imlet.2010.03.012     Document Type: Article

References (126)

1. Complement regulatory proteins 1994, Academic Press. B.P. Morgan, C.L. Harris (Eds.).
2. Klaus Rother G.O. The complement system 1997, Springer.
3. Kishore U., Ghai R., Greenhough T.J., Shrive A.K., Bonifati D.M., Gadjeva M.G., et al. Structural and functional anatomy of the globular domain of the the complement protein C1q. Immunol Lett 2004, 95:113-128.
4. Rabs U., Martin H., Hitschold T., Golan M.D., Heinz H.P., Loos M. Isolation and characterization of macrophage-derived C1q and its similarities to serum C1q. Eur J Immunol 1986, 16:1183-1186.
5. Sontheimer R.D., Racila E., Racila M.D. C1q: its functions within the innate and adaptive immune responses and its role in lupus autoimmunity. J Invest Dermatol 2005, 125:14-23.
6. De Bracco M.M., Manni J.A. Serum levels of C1q, C1r and C1s in normal and pathologic sera. Arthritis Rheum 1974, 17:121-128.
7. Kishore U., Gaboriaud C., Waters P., Shrive A.K., Greenhough T.J., Reid K.B. C1q and tumor necrosis factor superfamily: modularity and versatility. Trends Immunol 2004, 25:551-561.
8. van de Wetering K., van Golde M.G.L., Batenburg J. Collectins: Players of the innate immune system. Eur J Biochem 2004, 271:1229-1249.
9. Shapiro L., Scherer P.E. The crystal structure of a C1q family protein suggests an evolutionary link to tumor necrosis factor. Curr Biol 1998, 8:335-338.
10. Sim R., Kishore U., Villiers C.L., Marche P.N., Mitchell D.A. C1q binding and complement activation by prions and amyloids. Immunobiology 2007, 212:355-362.
11. Banchereau J., Steinman R.M. Dendritic cells and the control of immunity. Nature 1998, 392:245-252.
12. 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.
13. Castellano G., Woltman A.M., Schlagwein N., Xu W., Schena F.P., Daha M.R., et al. Immune modulation of human dendritic cells by complement. Eur J Immunol 2007, 37:2803-2811.
14. Castellano G., Woltman A.M., Nauta A.J., Roos A., Trouw L.A., Seelen M.A., et al. Maturation of dendritic cells abrogates C1q production in vivo and in vitro. Blood 2004, 103:3813-3820.
15. Vegh Z., Goyarts E.C., 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, 3:39-51.
16. Csomor E., Bajtay Z., Sándor N., Kristóf K., Arlaud G.J., Thiel S., et al. Complement protein C1q induces maturation of human dendritic cells. Mol Immunol 2007, 44:3389-3397.
17. Tada Y., Asahina A., Fujita H., Mitsui H., Torii H., Watanabe T., et al. Differential effects of LPS and TGF-β on the production of IL-6 and IL-12 by Langerhans cells, splenic dendritic cells, and macrophages. Cytokine 2004, 25:155-161.
18. Reis E.S., Barbuto J.A., Isaac L. Complement components, regulators and receptors are produced by human monocyte-derived dendritic cells. Immunobiology 2007, 212:151-157.
19. Lood C., Gullstrand B., Truedsson L., Olin A.I., Alm G.V., Rönnblom L., et al. C1q inhibits immune complex-induced interferon-alpha production in plasmacytoid dendritic cells: a novel link between C1q deficiency and systemic lupus erythematosus pathogenesis. Arthritis Rheum 2009, 60:3081-3090.
20. Agrawal A., Singh P.P., Bottazzi B., Garlanda C., Mantovani A. Pattern recognition by pentraxins. Adv Exp Med Biol 2009, 653:98-116.
21. Baruah P., Dumitriu I.E., Peri G., Russo V., Mantovani A., Manfredi A.A., et al. The tissue pentraxin PTX3 limits C1q-mediated complement activation and phagocytosis of apoptotic cells by dendritic cells. J Leukoc Biol 2006, 80:87-95.
22. Oiki S., Okada Y. C1q induces chemotaxis and K+ conductance activation coupled to increased cytosolic Ca2+ in mouse fibroblasts. J Immunol 1988, 141:3177-3185.
23. Bordin S., Ghebrehiwet B., Page R.C. Participation of C1q and its receptor in adherence of human diploid fibroblast. J Immunol 1990, 145:2520-2526.
24. Ghebrehiwet B., Kew R.R., Gruber B.L., Marchese M.J., Peerschke E.I., Reid K.B. Murine mast cells express two types of C1q receptors that are involved in the induction of chemotaxis and chemokinesis. J Immunol 1995, 155:2614-2619.
25. Leigh L.E., Ghebrehiwet B., Perera T.P., Bird I.N., Strong P., Kishore U., et al. C1q-mediated chemotaxis by human neutrophils: involvement of gClqR and G-protein signalling mechanisms. Biochem J 1998, 330:247-254.
26. Kantrow S.P., Shen Z., Jagneaux T., Zhang P., Nelson S. Neutrophil-mediated lung permeability and host defense proteins. Am J Physiol Lung Cell Mol Physiol 2009, 297:738-745.
27. Goodman E.B., Anderson D.C., Tenner A.J. C1q triggers neutrophil superoxide production by a unique CD18-dependent mechanism. J Leukoc Biol 1995, 58:168-176.
28. van den Berg R.H., Faber-Krol M.C., van Wetering S., Hiemstra P.S., Daha M.R. Inhibition of activation of the classical pathway of complement by human neutrophil defensins. Blood 1998, 92:3898-3903.
29. Groeneveld T.W., Ramwadhdoebé T.H., Trouw L.A., van den Ham D.L., van der Borden V., Drijfhout J.W., et al. Human neutrophil peptide-1 inhibits both the classical and the lectin pathway of complement activation. Mol Immunol 2007, 44:3608-3614.
30. Chen A., Gaddipati S., Hong Y., Volkman D.J., Peerschke E.I., Ghebrehiwet B. Human T cells express specific binding sites for C1q. Role in T cell activation and proliferation. J Immunol 1994, 153:1430-1440.
31. van Montfoort N., de Jong J.M., Schuurhuis D.H., van der Voort E.I., Camps M.G., Huizinga T.W., et al. A novel role of complement factor C1q in augmenting the presentation of antigen captured in immune complexes to CD8+ T lymphocytes. J Immunol 2007, 178:7581-7586.
32. Cutler A.J., Botto M., van Essen D., Rivi R., Davies K.A., Gray D., et al. T cell-dependent immune response in C1q-deficient mice: defective interferon gamma production by antigen-specific T cells. J Exp Med 1998, 187:1789-1797.
33. Young K.R., Ambrus J.L., Malbran A., Fauci A.S., Tenner A.J. Complement subcomponent C1q stimulates Ig production by human B lymphocytes. J Immunol 1991, 146:3356-3364.
34. Ferry H., Potter P.K., Crockford T.L., Nijnik A., Ehrenstein M.R., Walport M.J., et al. Increased positive selection of B1 cells and reduced B cell tolerance to intracellular antigens in c1q-deficient mice. J Immunol 2007, 178:2916-2922.
35. Cutler A.J., Cornall R.J., Ferry H., Manderson A.P., Botto M., Walport M.J. Intact B cell tolerance in the absence of the first component of the classical complement pathway. Eur J Immunol 2001, 2087-2093.
36. Yurasov S., Wardemann H., Hammersen J., Tsuiji M., Meffre E., Pascual V., et al. Defective B cell tolerance checkpoints in systemic lupus erythematosus. J Exp Med 2005, 201:703-711.
37. Färber K., Cheung G., Mitchell D., Wallis R., Weihe E., Schwaeble W., et al. C1q, the recognition subcomponent of the classical pathway of complement, drives microglial activation. J Neurosci Res 2009, 87:644-652.
38. Walport M.J., Davies K.A., Botto M. C1q and systemic lupus erythematosus. Immunobiol 1998, 199:265-285.
39. Korb L.C., Ahearn J.M. C1q binds directly and specifically to surface blebs of apoptotic human keratinocytes: complement deficiency and systemic lupus erythematosus revisited. J Immunol 1997, 158:4525-4528.
40. Ogden C.A., deCathelineau A., Hoffmann P.R., Bratton D., Ghebrehiwet B., Fadok V.A., et al. C1q and mannose binding lectin engagement of cell surface calreticulin and CD91 initiates macropinocytosis and uptake of apoptotic cells. J Exp Med 2001, 194:781-796.
41. Navratil J.S., Watkins S.C., Wisnieski J.J., Ahearn J.M. The globular heads of C1q specifically recognize surface blebs of apoptotic vascular endothelial cells. J Immunol 2001, 166:3231-3239.
42. Nauta A.J., Trouw L.A., Daha M.R., Tijsma O., Nieuwland R., Schwaeble W.J., et al. Direct binding of C1q to apoptotic cells and cell blebs induces complement activation. Eur J Immunol 2002, 32:1726-1736.
43. Fraser D.A., Laust A.K., Nelson E.L., Tenner A.J. C1q differentially modulates phagocytosis and cytokine responses during ingestion of apoptotic cells by human monocytes, macrophages, and dendritic cells. J Immunol 2009, 183:6175-6185.
44. Mevorach D., Mascarenhas J.O., Gershov D., Elkon K.B. Complement-dependent clearance of apoptotic cells by human macrophages. J Exp Med 1998, 188:2313-2320.
45. Zwart B., Ciurana C., Rensink I., Manoe R., Hack C.E., Aarden L.A. Complement activation by apoptotic cells occurs predominantly via IgM and is limited to late apoptotic (secondary necrotic) cells. Autoimmunity 2004, 37:95-102.
46. Ogden C.A., Kowalewski R., Peng Y., Montenegro V., Elkon K.B. IgM is required for efficient complement mediated phagocytosis of apoptotic cells in vivo. Autoimmunity 2005, 38:259-264.
47. Walport M.J. Complement - Second of two parts. N Engl J Med 2001, 344:1140-1144.
48. Botto M., Dell'Agnola C., Bygrave A.E., Thompson E.M., Cook H.T., Petry F., et al. Homozygous C1q deficiency causes glomerulonephritis associated with multiple apoptotic bodies. Nat Genet 1998, 19:56-59.
49. Casciola-Rosen L., Rosen A., Petri M., Schlissel M. Surface blebs on apoptotic cells are sites of enhanced procoagulant activity: implications for coagulation events and antigenic spread in systemic lupus erythematosus. Proc Natl Acad Sci USA 1996, 93:1624-1629.
50. Rosen A., Casciola-Rosen L., Ahearn J. Novel packages of viral and self-antigens are generated during apoptosis. J Exp Med 1995, 181:1557-1561.
51. Jesus A.A., Silva C.A., Carneiro-Sampaio M., Sheinberg M., Mangueira C.L., Marie S.K., et al. Anti-C1q antibodies in juvenile-onset systemic lupus erythematosus. Ann NY Acad Sci 2009, 1173:235-238.
52. Moura C.G., Lima I., Barbosa L., Athanazio D., Reis E., Reis M., et al. Anti-C1q antibodies: association with nephritis and disease activity in systemic lupus erythematosus. J Clin Lab Anal 2009, 23:19-23.
53. Mosca M., Chimenti D., Pratesi F., Baldini C., Anzilotti C., Bombardieri S., et al. Prevalence and clinico-serological correlations of anti-alpha-enolase, anti-C1q, and anti-dsDNA antibodies in patients with systemic lupus erythematosus. J Rheumatol 2006, 33:695-697.
54. Trouw L.A., Groeneveld T.W., Seelen M.A., Duijs J.M., Bajema I.M., Prins F.A., et al. Anti-C1q autoantibodies deposit in glomeruli but are only pathogenic in combination with glomerular C1q-containing immune complexes. J Clin Invest 2004, 114:679-688.
55. Bigler C., Schaller M., Perahud I., Osthoff M., Trendelenburg M. Autoantibodies against complement C1q specifically target C1q bound on early apoptotic cells. J Immunol 2009, 183:3512-3521.
56. Fraser D.A., Pisalyaput K., Tenner A.J. C1q enhances microglial clearance of apoptotic neurons and neuronal blebs, and modulates subsequent inflammatory cytokine production. J Neurochem 2010, 112:733-743.
57. Unterberger U., Voigtlander T., Budka H. Pathogenesis of prion diseases. Acta Neuropathol 2005, 109:32-48.
58. Klein M.A., Kaeser P.S., Schwarz P., Weyd H., Xenarios I., Zinkernagel R.M., et al. Complement facilitates early prion pathogenesis. Nat Med 2001, 488-492.
59. Mabbott N.A., Bruce M.E., Botto M., Walport M.J., Pepys M.B. Temporary depletion of complement component C3 or genetic deficiency of C1q significantly delays onset of scrapie. Nat Med 2001, 7:485-487.
60. Ishii T., Haga S., Yagishita S., Tateishi J. The presence of complement in amyloid plaques of Creutzfeldt-Jakob disease and Gerstmann-Straussler-Scheinker disease. Appl Pathol 1984, 2:370-379.
61. Mitchell D.A., Kirby L., Paulin S.M., Villiers C.L., Sim R.B. Prion protein activates and fixes complement directly via the classical pathway: implications for the mechanism of scrapie agent propagation in lymphoid tissue. Mol Immunol 2007, 44:2997-3004.
62. Flores-Langarica A., Sebti Y., Mitchell D.A., Sim R.B., MacPherson G.G. Scrapie pathogenesis: the role of complement C1q in scrapie agent uptake by conventional dendritic cells. J Immunol 2009, 182:1305-1313.
63. Klickstein L.B., Barbashov S.F., Liu T., Jack R.M., Nicholson-Weller A. Complement receptor type 1 (CR1, CD35) is a receptor for C1q. Immunity 1997, 7:345-355.
64. Zabel M.D., Heikenwalder M., Prinz M., Arrighi I., Schwarz P., Kranich J., et al. Stromal complement receptor CD21/35 facilitates lymphoid prion colonization and pathogenesis. J Immunol 2007, 179:6144-6152.
65. Kovacs G.G., Gasque P., Ströbel T., Lindeck-Pozza E., Strohschneider M., Ironside J.W., et al. Complement activation in human prion disease. Neurobiol Dis 2004, 21-28.
66. Peuschel K.E. Pitfalls in prion research. Med Hypotheses 2000, 54:698-700.
67. Bulla R., Agostinis C., Bossi F., Rizzi L., Debeus A., Tripodo C., et al. Decidual endothelial cells express surface-bound C1q as a molecular bridge between endovascular trophoblast and decidual endothelium. Mol Immunol 2008, 45:2629-2640.
68. Mold C., Morris C.A. Complement activation by apoptotic endothelial cells following hypoxia/reoxygenation. Immunology 2001, 102:359-364.
69. Fischetti F., Tedesco F. Cross-talk between the complement system and endothelial cells in physiologic conditions and in vascular diseases. Autoimmunity 2006, 39:417-428.
70. Smyth A., Garovic V.D. Systemic lupus erythematosus and pregnancy. Miner Urol Nefrol 2009, 61:457-474.
71. Nepomuceno R.R., Tenner A.J. C1qRP, the C1q receptor that enhances phagocytosis, is detected specifically in human cells of myeloid lineage, endothelial cells, and platelets. J Immunol 1998, 160:1929-1935.
72. Peerschke E.I., Ghebrehiwet B. C1q augments platelet activation in response to aggregated Ig. J Immunol 1997, 159:5594-5598.
73. Peerschke E.I., Reid K.B., Ghebrehiwet B. Platelet activation by C1q results in the induction of alpha IIb/beta 3 integrins (GPIIb-IIIa) and the expression of P-selectin and procoagulant activity. J Exp Med 1993, 178:579-587.
74. Tiffany M.L., Penner J.A. Effect of complement on collagen-induced platelet aggregation. J Lab Clin Med 1980, 96:796-802.
75. Lu P.D., Galanakis D.K., Ghebrehiwet B., Peerschke E.I. The receptor for the globular " heads" of C1q, gC1q-R, binds to fibrinogen/fibrin and impairs its polymerization. Clin Immunol 1999, 90:360-367.
76. Skoglund C., Wetterö J., Skogh T., Sjöwall C., Tengvall P., Bengtsson T. C-reactive protein and C1q regulate platelet adhesion and activation on adsorbed immunoglobulin G and albumin. Immunol Cell Biol 2008, 86:466-474.
77. McGrath F.D., Brouwer M.C., Arlaud G.J., Daha M.R., Hack C.E., Roos A. Evidence that complement protein C1q interacts with C-reactive protein through its globular head region. J Immunol 2006, 176:2950-2957.
78. Wetterö J., Askendal A., Tengvall P., Bengtsson T. Interactions between surface-bound actin and complement, platelets, and neutrophils. J Biomed Mater Res A 2003, 66:162-175.
79. Arumugam T.V., Shiels I.A., Woodruff T.M., Granger D.N., Taylor S.M. The role of the complement system in ischemia-reperfusion injury. Shock 2004, 21:401-409.
80. Peerschke E.I., Yin W., Alpert D.R., Roubey R.A., Salmon J.E., Ghebrehiwet B. Serum complement activation on heterologous platelets is associated with arterial thrombosis in patients with systemic lupus erythematosus and antiphospholipid antibodies. Lupus 2009, 18:530-538.
81. Ghai R., Waters P., Roumenina L.T., Gadjeva M., Kojouharova M.S., Reid K.B., et al. C1q and its growing family. Immunobiology 2007, 212:253-266.
82. Stevens B., Allen N.J., Vazquez L.E., Howell G.R., Christopherson K.S., Nouri N., et al. The classical complement cascade mediates CNS synapse elimination. Cell 2007, 131:1164-1178.
83. Stevens B. Neuron-astrocyte signaling in the development and plasticity of neural circuits. Neurosignals 2008, 16:278-288.
84. Malinow R., Malenka R. AMPA receptor trafficking and synaptic plasticity. Annu Rev Neurosci 2002, 25:103-126.
85. Matsuda S., Miura E., Matsuda K., Kakegawa W., Kohda K., Watanabe M., et al. Accumulation of AMPA receptors in autophagosomes in neuronal axons lacking adaptor protein AP-4. Neuron 2008, 57:730-745.
86. Stellwagen D., Malenka R.C. Synaptic scaling mediated by glial TNF-alpha. Nature 2006, 440:1054-1059.
87. Bjartmar L., Huberman A.D., Ullian E.M., Rentería R.C., Liu X., Xu W., et al. Neuronal pentraxins mediate synaptic refinement in the developing visual system. J Neurosci 2006, 26:6269-6281.
88. Nauta A.J., Bottazzi B., Mantovani A., Salvatori G., Kishore U., Schwaeble W.J., et al. Biochemical and functional characterization of the interaction between pentraxin 3 and C1q. Eur J Immunol 2003, 33:465-473.
89. Salès N., Hässig R., Rodolfo K., Di Giamberardino L., Traiffort E., Ruat M., et al. Developmental expression of the cellular prion protein in elongating axons. Eur J Neurosci 2002, 15:1163-1177.
90. Encalada S.E., Encalada S.E., Moya K.L., Lehmann S., Zahn R. The role of the prion protein in the molecular basis for synaptic plasticity and nervous system development. J Mol Neurosci 2008, 34:9-15.
91. Málaga-Trillo E., Solis G.P., Schrock Y., Geiss C., Luncz L., Thomanetz V., et al. Regulation of embryonic cell adhesion by the prion protein. PLoC Biol 2009, 7:576-590.
92. McLin V.A., Hu C.H., Shah R., Jamrich M. Expression of complement components coincides with early patterning and organogenesis in Xenopus laevis. Int J Dev Biol 2008, 52:1123-1133.
93. Li X., Madison B.B., Zacharias W., Kolterud A., States D., Gumucio D.L. Deconvoluting the intestine: molecular evidence for a major role of the mesenchyme in the modulation of signaling cross talk. Physiol Genomics 2007, 29:290-301.
94. Sim R.B., Moffatt B.E., Shaw J.M., Ferluga J. Complement control proteins: from FH to CR4. Molecular aspects of innate and adaptive immunity 2008, 84-104. RSC Publishing Cambridge. K.B.M. Reid, R.B. Sim (Eds.).
95. Coppolino M.G., Woodside M.J., Demaurex N., Grinstein S., St-Arnaud R., Dedhar S. Calreticulin is essential for integrin-mediated calcium signalling and cell adhesion. Nature 1997, 386:843-847.
96. Howe C., Garstka M., Al-Balushi M., Ghanem E., Antoniou A.N., Fritzsche S., et al. Calreticulin-dependent recycling in the early secretory pathway mediates optimal peptide loading of MHC class I molecules. EMBO J 2009, 28:3730-3744.
97. Arosa F.A., de Jesus O., Porto G., Carmo A.M., de Sousa M. Calreticulin is expressed on the cell surface of activated human peripheral blood T lymphocytes in association with major histocompatibility complex class I molecules. J Biol Chem 1999, 274:16917-16922.
98. Huh G.S., Boulanger L.M., Du H., Riquelme P.A., Brotz T.M., Shatz C.J. Functional requirement for Class I MHC in CNS development and plasticity. Science 2000, 290:2155-2159.
99. Wang Q., Zhuang G.L., Zhou C.Q., Li T.C., Li J., Xu Y.W., et al. Expression of certain HLA-I types in cleavage-stage embryos. Reprod Biomed Online 2009, 18:244-250.
100. Hosszu K.K., Santiago-Schwarz F., Peerschke E.I., Ghebrehiwet B. Evidence that a C1q/C1qR system regulates monocyte-derived dendritic cell differentiation at the interface of innate and acquired immunity. Innate Immun 2009, [Epub ahead of print].
101. Mei J., Zhang Q.Y., Li Z., Lin S., Gui J.F. C1q-like inhibits p53-mediated apoptosis and controls normal hematopoiesis during zebrafish embryogenesis. Dev Biol 2008, 319:273-284.
102. Mei J., Gui J. Bioinformatic identification of genes encoding C1q-domain-containing proteins in zebrafish. J Genet Genomics 2008, 35:17-24.
103. Moya K.L., Benowitz L.I., Schneider G.E., Allinquant B. The amyloid precursor protein is developmentally regulated and correlated with synaptogenesis. Dev Biol 1994, 161:597-603.
104. Claasen A.M., Guévremont D., Mason-Parker S.E., Bourne K., Tate W.P., Abraham W.C., et al. Secreted amyloid precursor protein-alpha upregulates synaptic protein synthesis by a protein kinase G-dependent mechanism. Neurosci Lett 2009, 460:92-96.
105. Nikolaev A., McLaughlin T., O'Leary D., Tessier-Lavigne M. N-APP binds DR6 to cause axon pruning and neuron death via distinct caspases. Nature 2009, 457:981-989.
106. Kishore U., Gupta S.K., Perdikoulis M.V., Kojouharova M.S., Urban B.C., Reid K.B. Modular organization of the carboxyl-terminal, globular head region of human C1q A, B, and C chains. J Immunol 2003, 171:812-820.
107. Lambert J.C., Heath S., Even G., Campion D., Sleegers K., Hiltunen M., et al. Genome-wide association study identifies variants at CLU and CR1 associated with Alzheimer's disease. Nat Genet 2009, 41:1094-1099.
108. Kojouharova M.S., Gadjeva M.G., Tsacheva I.G., Zlatarova A., Roumenina L.T., Tchorbadjieva M.I., et al. Mutational analyses of the recombinant globular regions of human C1q A, B, and C chains suggest an essential role for arginine and histidine residues in the C1q-IgG interaction. J Immunol 2004, 172:4351-4358.
109. Kishore U., Reid K.B. C1q: structure, function, and receptors. Immunopharmacology 2000, 49:159-170.
110. Albertí S., Marqués G., Hernández-Allés S., Rubires X., Tomás J.M., Vivanco F., et al. Interaction between complement subcomponent C1q and the Klebsiella pneumoniae porin OmpK36. Infect Immun 1996, 4719-4725.
111. Roumenina L.T., Popov K.T., Bureeva S.V., Kojouharova M., Gadjeva M., Rabheru S., et al. Interaction of the globular domain of human C1q with Salmonella typhimurium lipopolysaccharide. Biochim Biophys Acta 2008, 1784:1271-1276.
112. Peerschke E.I., Reid K.B., Ghebrehiwet B. Identification of a novel 33-kDa C1q-binding site on human blood platelets. J Immunol 1994, 152:5896-5901.
113. Pickering M.C., Botto M., Taylor P.R., Lachmann P.J., Walport M.J. Systemic lupus erythematosus, complement deficiency, and apoptosis. Adv Immunol 2000, 76:227-324.
114. Botto M., Dell'Agnola C., Bygrave A.E., Thompson E.M., Cook H.T., Petry F., et al. Homozygous C1q deficiency causes glomerulonephritis associated with multiple apoptotic bodies. Nat Genet 2008, 19:56-59.
115. Warren J., Mastroeni P., Dougan G., Noursadeghi M., Cohen J., Walport M.J., et al. Increased susceptibility of C1q-deficient mice to Salmonella enterica serovar typhimurium infection. Infect Immun 2002, 70:551-557.
116. Taylor P.R., Seixas E., Walport M.J., Langhorne J., Botto M. Complement contributes to protective immunity against reinfection by Plasmodium chabaudi parasites. Infect Immun 2001, 69:3853-3859.
117. Celik I., Stover C., Botto M., Thiel S., Tzima S., Künkel D., et al. Role of the classical pathway of complement activation in experimentally induced polymicrobial peritonitis. Infect Immun 2001, 69:7304-7309.
118. Vizjak A., Ferluga D., Rozic M., Hvala A., Lindic J., Levart T.K., et al. Pathology, clinical presentations, and outcomes of C1q nephropathy. J Am Soc Nephrol 2008, 19:2237-2244.
119. Kishore U., Bonifati D.M. Role of complement in neurodegeneration and neuroinflammation. Mol Immunol 2007, 44:999-1010.
120. Blanquet-Grossard F., Thielens N.M., Vendrely C., Jamin M., Arlaud G.J. Complement protein C1q recognizes a conformationally modified form of the prion protein. Biochemistry 2005, 44:4349-4356.
121. Hong Q., Sze C.I., Lin S.R., Lee M.H., He R.Y., Schultz L., et al. Complement C1q activates tumor suppressor WWOX to induce apoptosis in prostate cancer cells. PLoS One 2009, 4:e5755.
122. Shimono C., Manabe R.I., Yamada T., Fukuda S., Kawai J., Furutani Y., et al. Identification and characterization of nCLP2, a novel C1q family protein expressed in the central nervous system. J Biochem 2009, [Epub ahead of print].
123. Ten V.S., Yao J., Ratner V., Sosunov S., Fraser D.A., Botto M., et al. Complement component C1q mediates mitochondria-driven oxidative stress in neonatal hypoxic-ischemic brain injury. J Neurosci 2010, 30:2077-2087.
124. Kreutz R., Schulz A., Sietmann A., Stoll M., Daha M.R., de Heer E., et al. Induction of C1q expression in glomerular endothelium in a rat model with arterial hypertension and albuminuria. J Hypertens 2007, 25(11):2308-2316.
125. 1-42 globulomer) suppress spontaneous synaptic activity by inhibition of P/Q-type calcium currents. J Neurosci 2008, 28:788-797.
126. Laurén J., Gimbel D.A., Nygaard H.B., Gilbert J.W., Strittmatter S.M. Cellular prion protein mediates impairment of synaptic plasticity by amyloid-β oligomers. Nature 2009, 457:1128-1132.