Intracellular complement − the complosome − in immune cell regulation

Molecular Immunology

Volumn 89, Issue , 2017, Pages 2-9

  Arbore, Giuseppina ^a   Kemper, Claudia ^a,b   Kolev, Martin ^a  

^a GUY S HOSPITAL   (United Kingdom)

^b NATIONAL HEART LUNG AND BLOOD INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CELL PROTEIN; COMPLEMENT; COMPLEMENT COMPONENT C1Q; COMPLEMENT COMPONENT C3; COMPLEMENT COMPONENT C3 COMPLOSOME; COMPLEMENT COMPONENT C5; COMPLEMENT COMPONENT C5 COMPLOSOME; COMPLOSOME; OXYGEN; TUMOR NECROSIS FACTOR; UNCLASSIFIED DRUG;

CELL LEVEL; CELL PROLIFERATION; CELL REGULATION; CELL SURVIVAL; CELLULAR IMMUNITY; CELLULAR, SUBCELLULAR AND MOLECULAR BIOLOGICAL PHENOMENA AND FUNCTIONS; COMPLEMENT ACTIVATION; HUMAN; IMMUNOCOMPETENT CELL; IMMUNOMODULATION; INFECTIOUS AGENT; METABOLISM; NONHUMAN; NUTRIENT; PRIORITY JOURNAL; REVIEW; ADAPTIVE IMMUNITY; ANIMAL; BIOLOGICAL MODEL; CYTOPLASM; IMMUNOLOGY; INNATE IMMUNITY; T LYMPHOCYTE;

ADAPTIVE IMMUNITY; ANIMALS; COMPLEMENT ACTIVATION; COMPLEMENT SYSTEM PROTEINS; CYTOPLASM; HUMANS; IMMUNITY, CELLULAR; IMMUNITY, INNATE; MODELS, IMMUNOLOGICAL; T-LYMPHOCYTES;

EID: 85020462081     PISSN: 01615890     EISSN: 18729142     Source Type: Journal    
DOI: 10.1016/j.molimm.2017.05.012     Document Type: Review

References (83)

1. Abdul-Aziz, M., Tsolaki, A.G., Kouser, L., Carroll, M.V., Al-Ahdal, M.N., Sim, R.B., Kishore, U., Complement factor H interferes with Mycobacterium bovis BCG entry into macrophages and modulates the pro-inflammatory cytokine response. Immunobiology 221:9 (2016), 944–952.
2. Afrookhteh, A., Emamgholipour, S., Alipoor, B., Moradi, N., Meshkani, R., Nasli-Esfahani, E., Rahimipour, A., Shanaki, M., The circulating levels of complement-C1q/TNF-related protein 13 (CTRP13) in patients with type 2 diabetes and its association with insulin resistance. Clin. Lab. 63:2 (2017), 327–333.
3. Appledorn, D.M., McBride, A., Seregin, S., Scott, J.M., Schuldt, N., Kiang, A., Godbehere, S., Amalfitano, A., Complex interactions with several arms of the complement system dictate innate and humoral immunity to adenoviral vectors. Gene Ther. 15:24 (2008), 1606–1617.
4. + T cells. Science, 352(6292), 2016, aad1210.
5. Asgari, E., Le Friec, G., Yamamoto, H., Perucha, E., Sacks, S.S., Köhl, J., Cook, H.T., Kemper, C., C3a modulates IL-1β secretion in human monocytes by regulating ATP efflux and subsequent NLRP3 inflammasome activation. Blood 122:20 (2013), 3473–3481.
6. Astier, A., Trescol-Biémont, M.C., Azocar, O., Lamouille, B., Rabourdin-Combe, C., Cutting edge: CD46, a new costimulatory molecule for T cells, that induces p120CBL and LAT phosphorylation. J. Immunol. 164:12 (2000), 6091–6095.
7. Astier, A.L., Meiffren, G., Freeman, S., Hafler, D.A., Alterations in CD46-mediated Tr1 regulatory T cells in patients with multiple sclerosis. J. Clin. Invest. 116:12 (2006), 3252–3257.
8. Bai, B., Ban, B., Liu, Z., Zhang, M.M., Tan, B.K., Chen, J., Circulating C1q complement/TNF-related protein (CTRP) 1, CTRP9, CTRP12 and CTRP13 concentrations in Type 2 diabetes mellitus: in vivo regulation by glucose. PLoS One, 12(2), 2017, e0172271.
9. Bar-Peled, L., Schweitzer, L.D., Zoncu, R., Sabatini, D.M., Ragulator is a GEF for the rag GTPases that signal amino acid levels to mTORC1. Cell 150:6 (2012), 1196–1208.
10. Basu, R., Pajvani, U.B., Rizza, R.A., Scherer, P.E., Selective downregulation of the high molecular weight form of adiponectin in hyperinsulinemia and in type 2 diabetes: differential regulation from nondiabetic subjects. Diabetes 56:8 (2007), 2174–2177.
11. Baudino, L., Sardini, A., Ruseva, M.M., Fossati-Jimack, L., Cook, H.T., Scott, D., Simpson, E., Botto, M., C3 opsonization regulates endocytic handling of apoptotic cells resulting in enhanced T-cell responses to cargo-derived antigens. Proc. Natl. Acad. Sci. U. S. A. 111:4 (2014), 1503–1508.
12. Cardone, J., Le Friec, G., Vantourout, P., Roberts, A., Fuchs, A., Jackson, I., Suddason, T., Lord, G., Atkinson, J.P., Cope, A., Hayday, A., Kemper, C., Complement regulator CD46 temporally regulates cytokine production by conventional and unconventional T cells. Nat. Immunol. 11:9 (2010), 862–871.
13. Chang, C.H., Curtis, J.D., Maggi, L.B., Faubert, B., Villarino, A.V., O'Sullivan, D., Huang, S.C., van der Windt, G.J., Blagih, J., Qiu, J., Weber, J.D., Pearce, E.J., Jones, R.G., Pearce, E.L., Posttranscriptional control of T cell effector function by aerobic glycolysis. Cell 153:6 (2013), 1239–1251.
14. Chen, Z.L., Su, Y.J., Zhang, H.L., Gu, P.Q., Gao, L.J., The role of the globular heads of the C1q receptor in HPV-16 E2-induced human cervical squamous carcinoma cell apoptosis via a mitochondria-dependent pathway. J. Transl. Med., 12, 2014, 286.
15. Clarke, E.V., Weist, B.M., Walsh, C.M., Tenner, A.J., Complement protein C1q bound to apoptotic cells suppresses human macrophage and dendritic cell-mediated Th17 and Th1 T cell subset proliferation. J. Leukoc. Biol. 97:1 (2015), 147–160.
16. Cope, A., Le Friec, G., Cardone, J., Kemper, C., The Th1 life cycle: molecular control of IFN-γ to IL-10 switching. Trends Immunol. 32:6 (2011), 278–286.
17. Croker, D.E., Halai, R., Kaeslin, G., Wende, E., Fehlhaber, B., Klos, A., Monk, P.N., Cooper, M.A., C5a2 can modulate ERK1/2 signaling in macrophages via heteromer formation with C5a1 and β-arrestin recruitment. Immunol. Cell Biol. 92:7 (2014), 631–639.
18. Cudrici, C., Niculescu, F., Jensen, T., Zafranskaia, E., Fosbrink, M., Rus, V., Shin, M.L., Rus, H., C5b-9 terminal complex protects oligodendrocytes from apoptotic cell death by inhibiting caspase-8 processing and up-regulating FLIP. J. Immunol. 176:5 (2006), 3173–3180.
19. Doyle, S.L., Campbell, M., Ozaki, E., Salomon, R.G., Mori, A., Kenna, P.F., Farrar, G.J., Kiang, A.S., Humphries, M.M., Lavelle, E.C., O'Neill, L.A., Hollyfield, J.G., Humphries, P., NLRP3 has a protective role in age-related macular degeneration through the induction of IL-18 by drusen components. Nat. Med. 18:5 (2012), 791–798.
20. Drouin, S.M., Corry, D.B., Hollman, T.J., Kildsgaard, J., Wetsel, R.A., Absence of the complement anaphylatoxin C3a receptor suppresses Th2 effector functions in a murine model of pulmonary allergy. J. Immunol. 169:10 (2002), 5926–5933.
21. Elvington, M., Liszewski, M.K., Bertram, P., Kulkarni, H.S., Atkinson, J.P., A C3(H20) recycling pathway is a component of the intracellular complement system. J. Clin. Invest. 127:3 (2017), 970–981.
22. Emmens, R.W., Baylan, U., Juffermans, L.J., Karia, R.V., Ylstra, B., Wouters, D., Zeerleder, S., Simsek, S., van Ham, M., Niessen, H.W., Krijnen, P.A., Endogenous C1-inhibitor production and expression in the heart after acute myocardial infarction. Cardiovasc. Pathol. 25:1 (2016), 33–39.
23. Feng, H., Wang, J.Y., Zheng, M., Zhang, C.L., An, Y.M., Li, L., Wu, L.L., CTRP3 promotes energy production by inducing mitochondrial ROS and up-expression of PGC-1(in vascular smooth muscle cells. Exp. Cell Res. 341:2 (2016), 177–186.
24. Fishelson, Z., Attali, G., Mevorach, D., Complement and apoptosis. Mol. Immunol. 38:2-3 (2001), 207–219.
25. Freeley, S., Kemper, C., Le Friec, G., The ins and outs of complement-driven immune responses. Immunol. Rev. 274:1 (2016), 16–32.
26. Hüttenrauch, F., Pollok-Kopp, B., Oppermann, M., G protein-coupled receptor kinases promote phosphorylation and beta-arrestin-mediated internalization of CCR5 homo- and hetero-oligomers. J. Biol. Chem. 280:45 (2005), 37503–37515.
27. Haggadone, M.D., Grailer, J.J., Fattahi, F., Zetoune, F.S., Ward, P.A., Bidirectional crosstalk between C5a receptors and the NLRP3 inflammasome in macrophages and monocytes. Mediators Inflamm., 2016, 2016, 1340156.
28. Hansen, A.S., Bundgaard, B.B., Møller, B.K., Höllsberg, P., Non-random pairing of CD46 isoforms with skewing towards BC2 and C2 in activated and memory/effector T cells. Sci. Rep., 6, 2016, 35406.
29. Heeger, P.S., Kemper, C., Novel roles of complement in T effector cell regulation. Immunobiology, 2011.
30. Hou, M., Liu, J., Liu, F., Liu, K., Yu, B., C1q tumor necrosis factor-related protein-3 protects mesenchymal stem cells against hypoxia- and serum deprivation-induced apoptosis through the phosphoinositide 3-kinase/Akt pathway. Int. J. Mol. Med. 33:1 (2014), 97–104.
31. Jung, H.S., Jeong, S.Y., Yang, J., Kim, S.D., Zhang, B., Yoo, H.S., Song, S.U., Jeon, M.S., Song, Y.S., Neuroprotective effect of mesenchymal stem cell through complement component 3 downregulation after transient focal cerebral ischemia in mice. Neurosci. Lett. 633 (2016), 227–234.
32. Köhl, J., Baelder, R., Lewkowich, I.P., Pandey, M.K., Hawlisch, H., Wang, L., Best, J., Herman, N.S., Sproles, A.A., Zwirner, J., Whitsett, J.A., Gerard, C., Sfyroera, G., Lambris, J.D., Wills-Karp, M., A regulatory role for the C5a anaphylatoxin in type 2 immunity in asthma. J. Clin. Invest. 116:3 (2006), 783–796.
33. Kalbitz, M., Fattahi, F., Grailer, J.J., Jajou, L., Malan, E.A., Zetoune, F.S., Huber-Lang, M., Russell, M.W., Ward, P.A., Complement-induced activation of the cardiac NLRP3 inflammasome in sepsis. FASEB J. 30:12 (2016), 3997–4006.
34. Katz, Y., Singer, L., Wetsel, R.A., Schlesinger, M., Fishelson, Z., Inherited complement C3 deficiency: a defect in C3 secretion. Eur. J. Immunol. 24:7 (1994), 1517–1522.
35. Kemper, C., Leung, M., Stephensen, C.B., Pinkert, C.A., Liszewski, M.K., Cattaneo, R., Atkinson, J.P., Membrane cofactor protein (MCP; CD46) expression in transgenic mice. Clin. Exp. Immunol. 124:2 (2001), 180–189.
36. Kim, K.H., Choi, B.K., Kim, Y.H., Han, C., Oh, H.S., Lee, D.G., Kwon, B.S., Extracellular stimulation of VSIG4/complement receptor Ig suppresses intracellular bacterial infection by inducing autophagy. Autophagy 12:9 (2016), 1647–1659.
37. King, B.C., Esguerra, J.L., Golec, E., Eliasson, L., Kemper, C., Blom, A.M., CD46 activation regulates miR-150-Mediated control of GLUT1 expression and cytokine secretion in human CD4+ t cells. J. Immunol. 196:4 (2016), 1636–1645.
38. Kolev, M., Kemper, C., Keeping it all going-complement meets metabolism. Front. Immunol., 8, 2017, 1.
39. Kolev, M., Le Friec, G., Kemper, C., The role of complement in CD4⁺ T cell homeostasis and effector functions. Semin. Immunol. 25:1 (2013), 12–19.
40. Kolev, M., Friec, G.L., Kemper, C., Complement − tapping into new sites and effector systems. Nat. Rev. Immunol. 14:12 (2014), 811–820.
41. Kolev, M., Dimeloe, S., Le Friec, G., Navarini, A., Arbore, G., Povoleri, G.A., Fischer, M., Belle, R., Loeliger, J., Develioglu, L., Bantug, G.R., Watson, J., Couzi, L., Afzali, B., Lavender, P., Hess, C., Kemper, C., Complement regulates nutrient influx and metabolic reprogramming during th1 cell responses. Immunity 42:6 (2015), 1033–1047.
42. Kolev, M., Dimeloe, S., Lavender, P., Hess, C., Cope, A., Kemper, C., Tissue extravasation induces ‘complement-licesning' required for immune cell effector function. Immunobiology, 221, 2016, 1196.
43. Kurihara, R., Yamaoka, K., Sawamukai, N., Shimajiri, S., Oshita, K., Yukawa, S., Tokunaga, M., Iwata, S., Saito, K., Chiba, K., Tanaka, Y., C5a promotes migration, proliferation, and vessel formation in endothelial cells. Inflamm. Res. 59:8 (2010), 659–666.
44. Lalli, P.N., Strainic, M.G., Yang, M., Lin, F., Medof, M.E., Heeger, P.S., Locally produced C5a binds to T cell-expressed C5aR to enhance effector T-cell expansion by limiting antigen-induced apoptosis. Blood 112:5 (2008), 1759–1766.
45. Le Friec, G., Sheppard, D., Whiteman, P., Karsten, C.M., Shamoun, S.A., Laing, A., Bugeon, L., Dallman, M.J., Melchionna, T., Chillakuri, C., Smith, R.A., Drouet, C., Couzi, L., Fremeaux-Bacchi, V., Köhl, J., Waddington, S.N., McDonnell, J.M., Baker, A., Handford, P.A., Lea, S.M., Kemper, C., The CD46-Jagged1 interaction is critical for human TH1 immunity. Nat. Immunol. 13:12 (2012), 1213–1221.
46. Le Friec, G., Köhl, J., Kemper, C., A complement a day keeps the Fox(p3) away. Nat. Immunol. 14:2 (2013), 110–112.
47. Lee, H., Whitfeld, P.L., Mackay, C.R., Receptors for complement C5a. The importance of C5aR and the enigmatic role of C5L2. Immunol. Cell Biol. 86:2 (2008), 153–160.
48. Li, D., Dong, B., Tong, Z., Wang, Q., Liu, W., Wang, Y., Chen, J., Xu, L., Chen, L., Duan, Y., MBL-mediated opsonophagocytosis of Candida albicans by human neutrophils is coupled with intracellular Dectin-1-triggered ROS production. PLoS One, 7(12), 2012, e50589.
49. Liszewski, M.K., Kolev, M., Le Friec, G., Leung, M., Bertram, P.G., Fara, A.F., Subias, M., Pickering, M.C., Drouet, C., Meri, S., Arstila, T.P., Pekkarinen, P.T., Ma, M., Cope, A., Reinheckel, T., Rodriguez de Cordoba, S., Afzali, B., Atkinson, J.P., Kemper, C., Intracellular complement activation sustains T cell homeostasis and mediates effector differentiation. Immunity 39:6 (2013), 1143–1157.
50. Longhi, M., Sivasankar, B., Omidvar, N., Morgan, B., Gallimore, A., Cutting edge: murine CD59a modulates antiviral CD4+ T cell activity in a complement-independent manner. J. Immunol. 175:11 (2005), 7098–7102.
51. Luo, Y., Tucker, S.C., Casadevall, A., Fc- and complement-receptor activation stimulates cell cycle progression of macrophage cells from G1 to S. J. Immunol. 174:11 (2005), 7226–7233.
52. Luo, C., Chen, M., Xu, H., Complement gene expression and regulation in mouse retina and retinal pigment epithelium/choroid. Mol. Vis. 17 (2011), 1588–1597.
53. Martin, M., Leffler, J., Smoląg, K.I., Mytych, J., Björk, A., Chaves, L.D., Alexander, J.J., Quigg, R.J., Blom, A.M., Factor H uptake regulates intracellular C3 activation during apoptosis and decreases the inflammatory potential of nucleosomes. Cell Death Differ. 23:5 (2016), 903–911.
54. Meilinger, M., Gschwentner, C., Burger, I., Haumer, M., Wahrmann, M., Szollar, L., Nimpf, J., Huettinger, M., Metabolism of activated complement component C3 is mediated by the low density lipoprotein receptor-related protein/alpha(2)-macroglobulin receptor. J. Biol. Chem. 274:53 (1999), 38091–38096.
55. Morgan, B.P., Berg, C.W., Harris, C.L., Homologous restriction in complement lysis: roles of membrane complement regulators. Xenotransplantation 12:4 (2005), 258–265.
56. Ni Choileain, S., Astier, A.L., CD46 plasticity and its inflammatory bias in multiple sclerosis. Arch. Immunol. Ther. Exp. (Warsz) 59:1 (2011), 49–59.
57. Ni Choileain, S., Weyand, N.J., Neumann, C., Thomas, J., So, M., Astier, A.L., The dynamic processing of CD46 intracellular domains provides a molecular rheostat for T cell activation. PLoS One, 6(1), 2011, e16287.
58. Nishimoto, H., Yamamoto, A., Furukawa, S., Wakisaka, S., Maeda, T., C1q/TNF-related protein 3 expression and effects on adipocyte differentiation of 3T3-L1 cells. Cell Biol. Int. 41:2 (2017), 197–203.
59. Ricklin, D., Hajishengallis, G., Yang, K., Lambris, J.D., Complement: a key system for immune surveillance and homeostasis. Nat. Immunol. 11:9 (2010), 785–797.
60. Ruseva, M.M., Hughes, T.R., Donev, R.M., Sivasankar, B., Pickering, M.C., Wu, X., Harris, C.L., Morgan, B.P., Crry deficiency in complement sufficient mice: C3 consumption occurs without associated renal injury. Mol. Immunol. 46:5 (2009), 803–811.
61. Samstad, E.O., Niyonzima, N., Nymo, S., Aune, M.H., Ryan, L., Bakke, S.S., Lappegård, K.T., Brekke, O.L., Lambris, J.D., Damås, J.K., Latz, E., Mollnes, T.E., Espevik, T., Cholesterol crystals induce complement-dependent inflammasome activation and cytokine release. J. Immunol. 192:6 (2014), 2837–2845.
62. Sarma, J.V., Ward, P.A., New developments in C5a receptor signaling. Cell Health Cytoskelet. 4 (2012), 73–82.
63. Satyam, A., Kannan, L., Matsumoto, N., Geha, M., Lapchak, P.H., Bosse, R., Shi, G.P., Dalle Lucca, J.J., Tsokos, M.G., Tsokos, G.C., Intracellular activation of complement 3 is responsible for intestinal tissue damage during mesenteric ischemia. J. Immunol. 198:2 (2017), 788–797.
64. Schäffler, A., Buechler, C., CTRP family: linking immunity to metabolism. Trends Endocrinol. Metab. 23:4 (2012), 194–204.
65. Schmidt, C.Q., Lambris, J.D., Ricklin, D., Protection of host cells by complement regulators. Immunol. Rev. 274:1 (2016), 152–171.
66. Seya, T., Ballard, L.L., Bora, N.S., Kumar, V., Cui, W., Atkinson, J.P., Distribution of membrane cofactor protein of complement on human peripheral blood cells. An altered form is found on granulocytes. Eur. J. Immunol. 18:8 (1988), 1289–1294.
67. Shah, P.P., Wang, T., Kaletsky, R.L., Myers, M.C., Purvis, J.E., Jing, H., Huryn, D.M., Greenbaum, D.C., Smith, A.B., Bates, P., Diamond, S.L., A small-molecule oxocarbazate inhibitor of human cathepsin L blocks severe acute respiratory syndrome and ebola pseudotype virus infection into human embryonic kidney 293T cells. Mol. Pharmacol. 78:2 (2010), 319–324.
68. Shao, Y., Li, C., Xu, W., Zhang, P., Zhang, W., Zhao, X., miR-31 links lipid metabolism and cell apoptosis in bacteria-challenged apostichopus japonicus via targeting CTRP9. Front. Immunol., 8, 2017, 263.
69. Singer, L., Whitehead, W.T., Akama, H., Katz, Y., Fishelson, Z., Wetsel, R.A., Inherited human complement C3 deficiency. An amino acid substitution in the beta-chain (ASP549 to ASN) impairs C3 secretion. J. Biol. Chem. 269:45 (1994), 28494–28499.
70. Soane, L., Rus, H., Niculescu, F., Shin, M.L., Inhibition of oligodendrocyte apoptosis by sublytic C5b-9 is associated with enhanced synthesis of bcl-2 and mediated by inhibition of caspase-3 activation. J. Immunol. 163:11 (1999), 6132–6138.
71. Strainic, M.G., Liu, J., Huang, D., An, F., Lalli, P.N., Muqim, N., Shapiro, V.S., Dubyak, G.R., Heeger, P.S., Medof, M.E., Locally produced complement fragments C5a and C3a provide both costimulatory and survival signals to naive CD4+ T cells. Immunity 28:3 (2008), 425–435.
72. Tam, J.C., Bidgood, S.R., McEwan, W.A., James, L.C., Intracellular sensing of complement C3 activates cell autonomous immunity. Science, 345(6201), 2014, 1256070.
73. Tan, Y.H., Gamage, A.M., Gan, Y.H., Complement-activated vitronectin enhances the invasion of nonphagocytic cells by bacterial pathogens Burkholderia and Klebsiella. Cell. Microbiol., 2017.
74. Turner, N.A., Sartain, S.E., Hui, S.K., Moake, J.L., Regulatory components of the alternative complement pathway in endothelial cell cytoplasm, factor H and factor I, are not packaged in Weibel-Palade bodies. PLoS One, 10(3), 2015, e0121994.
75. Wagner, C., Ochmann, C., Schoels, M., Giese, T., Stegmaier, S., Richter, R., Hug, F., Hänsch, G.M., The complement receptor 1, CR1 (CD35), mediates inhibitory signals in human T-lymphocytes. Mol. Immunol. 43:6 (2006), 643–651.
76. Walport, M., Complement. First of two parts. N. Engl. J. Med. 344:14 (2001), 1058–1066.
77. Wang, G., Liszewski, M.K., Chan, A.C., Atkinson, J.P., Membrane cofactor protein (MCP; CD46): isoform-specific tyrosine phosphorylation. J. Immunol. 164:4 (2000), 1839–1846.
78. Wang, R.Y., Bare, P., De Giorgi, V., Matsuura, K., Salam, K.A., Grandinetti, T., Schechterly, C., Alter, H.J., Preferential association of hepatitis C virus with CD19(+) B cells is mediated by complement system. Hepatology 64:6 (2016), 1900–1910.
79. Woodman, M.E., Worth, R.G., Wooten, R.M., Capsule influences the deposition of critical complement C3 levels required for the killing of Burkholderia pseudomallei via NADPH-oxidase induction by human neutrophils. PLoS One, 7(12), 2012, e52276.
80. Wu, L., Tan, X., Liang, L., Yu, H., Wang, C., Zhang, D., Kijlstra, A., Yang, P., The role of mitochondria-associated reactive oxygen species in the amyloid β induced production of angiogenic factors by ARPE-19 cells. Curr. Mol. Med., 2017.
81. Xu, L., Xiao, N., Liu, F., Ren, H., Gu, J., Inhibition of RIG-I and MDA5-dependent antiviral response by gC1qR at mitochondria. Proc. Natl. Acad. Sci. U. S. A. 106:5 (2009), 1530–1535.
82. Yao, Z.Q., Nguyen, D.T., Hiotellis, A.I., Hahn, Y.S., Hepatitis C virus core protein inhibits human T lymphocyte responses by a complement-dependent regulatory pathway. J. Immunol. 167:9 (2001), 5264–5272.
83. Zaffran, Y., Destaing, O., Roux, A., Ory, S., Nheu, T., Jurdic, P., Rabourdin-Combe, C., Astier, A.L., CD46/CD3 costimulation induces morphological changes of human T cells and activation of Vav, Rac, and extracellular signal-regulated kinase mitogen-activated protein kinase. J. Immunol. 167:12 (2001), 6780–6785.