Complement opsonization of HIV-1 results in decreased antiviral and inflammatory responses in immature dendritic cells via CR3

Journal of Immunology

Volumn 193, Issue 9, 2014, Pages 4590-4601

  Ellegård, Rada ^a   Crisci, Elisa ^a   Burgener, Adam ^b,c   Sjöwall, Christopher ^d   Birse, Kenzie ^b,c   Westmacott, Garrett ^c   Hinkula, Jorma ^a   Lifson, Jeffrey D ^e   Larsson, Marie ^a  

^a LINKÖPING UNIVERSITY   (Sweden)

^b UNIVERSITY OF MANITOBA   (Canada)

^c PUBLIC HEALTH AGENCY OF CANADA   (Canada)

^d Autoimmunity and Immune Regulation Unit   (Sweden)

^e FREDERICK NATIONAL LABORATORY FOR CANCER RESEARCH   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BETA INTERFERON; COMPLEMENT RECEPTOR; COMPLEMENT RECEPTOR 3; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERFERON REGULATORY FACTOR 1; INTERFERON REGULATORY FACTOR 3; INTERLEUKIN 1BETA; INTERLEUKIN 6; MITOGEN ACTIVATED PROTEIN KINASE; MITOGEN ACTIVATED PROTEIN KINASE P38; MYXOVIRUS RESISTANCE PROTEIN A; PHOSPHATIDYLINOSITOL 3 KINASE; PROTEIN KINASE LYN; TOLL LIKE RECEPTOR 8; TUMOR NECROSIS FACTOR ALPHA; UNCLASSIFIED DRUG; CD11B ANTIGEN; COMPLEMENT; LYN PROTEIN-TYROSINE KINASE; MESSENGER RNA; PROTEIN TYROSINE KINASE;

ANTIINFLAMMATORY ACTIVITY; ANTIVIRAL ACTIVITY; ARTICLE; CELL NUCLEUS; CONTROLLED STUDY; DENDRITIC CELL; HUMAN; HUMAN CELL; HUMAN IMMUNODEFICIENCY VIRUS 1; NONHUMAN; OPSONIZATION; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; SIGNAL TRANSDUCTION; ANTAGONISTS AND INHIBITORS; BIOLOGICAL MODEL; GENE EXPRESSION PROFILING; GENETICS; HUMAN IMMUNODEFICIENCY VIRUS INFECTION; IMMUNOLOGY; INFLAMMATION; INNATE IMMUNITY; METABOLISM; PHOSPHORYLATION; PROTEIN TRANSPORT; VIROLOGY;

COMPLEMENT SYSTEM PROTEINS; DENDRITIC CELLS; EXTRACELLULAR SIGNAL-REGULATED MAP KINASES; GENE EXPRESSION PROFILING; HIV INFECTIONS; HIV-1; HUMANS; IMMUNITY, INNATE; INFLAMMATION; INTERFERON REGULATORY FACTOR-1; INTERFERON REGULATORY FACTOR-3; MACROPHAGE-1 ANTIGEN; MODELS, BIOLOGICAL; NF-KAPPA B; P38 MITOGEN-ACTIVATED PROTEIN KINASES; PHOSPHATIDYLINOSITOL 3-KINASES; PHOSPHORYLATION; PROTEIN TRANSPORT; RNA, MESSENGER; SIGNAL TRANSDUCTION; SRC-FAMILY KINASES; TOLL-LIKE RECEPTOR 8;

EID: 84908131727     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1401781     Document Type: Article

References (64)

1. Steinman, R. M. 2007. Lasker Basic Medical Research Award. Dendritic cells: versatile controllers of the immune system. Nat. Med. 13: 1155-1159.
2. Hladik, F., and M. J. McElrath. 2008. Setting the stage: host invasion by HIV. Nat. Rev. Immunol. 8: 447-457.
3. Lubong Sabado, R., D. G. Kavanagh, D. E. Kaufmann, K. Fru, E. Babcock, E. Rosenberg, B. Walker, J. Lifson, N. Bhardwaj, and M. Larsson. 2009. In vitro priming recapitulates in vivo HIV-1 specific T cell responses, revealing rapid loss of virus reactive CD4 T cells in acute HIV-1 infection. PLoS ONE 4: e4256.
4. Sewell, A. K., and D. A. Price. 2001. Dendritic cells and transmission of HIV-1. Trends Immunol. 22: 173-175.
5. Gringhuis, S. I., M. van der Vlist, L. M. van den Berg, J. den Dunnen, M. Litjens, and T. B. Geijtenbeek. 2010. HIV-1 exploits innate signaling by TLR8 and DC-SIGN for productive infection of dendritic cells. Nat. Immunol. 11: 419-426.
6. Carroll, M. C. 2004. The complement system in regulation of adaptive immunity. Nat. Immunol. 5: 981-986.
7. + T lymphocytes. J. Immunol. 178: 7581-7586.
8. Ochsenbein, A. F., D. D. Pinschewer, B. Odermatt, M. C. Carroll, H. Hengartner, and R. M. Zinkernagel. 1999. Protective T cell-independent antiviral antibody responses are dependent on complement. J. Exp. Med. 190: 1165-1174.
9. Favoreel, H. W., G. R. Van de Walle, H. J. Nauwynck, and M. B. Pensaert. 2003. Virus complement evasion strategies. J. Gen. Virol. 84: 1-15.
10. Stoiber, H., Z. Banki, D. Wilflingseder, and M. P. Dierich. 2008. Complement-HIV interactions during all steps of viral pathogenesis. Vaccine 26: 3046-3054.
11. Stoiber, H., M. Pruenster, C. G. Ammann, and M. P. Dierich. 2005. Complement-opsonized HIV: the free rider on its way to infection. Mol. Immunol. 42: 153-160.
12. Saifuddin, M., C. J. Parker, M. E. Peeples, M. K. Gorny, S. Zolla-Pazner, M. Ghassemi, I. A. Rooney, J. P. Atkinson, and G. T. Spear. 1995. Role of virion-associated glycosylphosphatidylinositol-linked proteins CD55 and CD59 in complement resistance of cell line-derived and primary isolates of HIV-1. J. Exp. Med. 182: 501-509.
13. Bajtay, Z., C. Speth, A. Erdei, and M. P. Dierich. 2004. Cutting edge: productive HIV-1 infection of dendritic cells via complement receptor type 3 (CR3, CD11b/CD18). J. Immunol. 173: 4775-4778.
14. Bouhlal, H., N. Chomont, M. Réquena, N. Nasreddine, H. Saidi, J. Legoff, M. D. Kazatchkine, L. Bélec, and H. Hocini. 2007. Opsonization of HIV with complement enhances infection of dendritic cells and viral transfer to CD4 T cells in a CR3 and DC-SIGN-dependent manner. J. Immunol. 178: 1086-1095.
15. Pruenster, M., D. Wilflingseder, Z. Bánki, C. G. Ammann, B. Muellauer, M. Meyer, C. Speth, M. P. Dierich, and H. Stoiber. 2005. C-type lectin-independent interaction of complement opsonized HIV with monocyte-derived dendritic cells. Eur. J. Immunol. 35: 2691-2698.
16. Tjomsland, V., R. Ellegård, A. Burgener, K. Mogk, K. F. Che, G. Westmacott, J. Hinkula, J. D. Lifson, and M. Larsson. 2013. Complement opsonization of HIV-1 results in a different intracellular processing pattern and enhanced MHC class I presentation by dendritic cells. Eur. J. Immunol. 43: 1470-1483.
17. Tjomsland, V., R. Ellegård, K. Che, J. Hinkula, J. D. Lifson, and M. Larsson. 2011. Complement opsonization of HIV-1 enhances the uptake by dendritic cells and involves the endocytic lectin and integrin receptor families. PLoS ONE 6: e23542.
18. Tan, E. M., A. S. Cohen, J. F. Fries, A. T. Masi, D. J. McShane, N. F. Rothfield, J. G. Schaller, N. Talal, and R. J. Winchester. 1982. The 1982 revised criteria for the classification of systemic lupus erythematosus. Arthritis Rheum. 25: 1271-1277.
19. Enocsson, H., J. Wetterö, T. Skogh, and C. Sjöwall. 2013. Soluble urokinase plasminogen activator receptor levels reflect organ damage in systemic lupus erythematosus. Transl. Res. 162: 287-296.
20. Sabado, R. L., E. Babcock, D. G. Kavanagh, V. Tjomsland, B. D. Walker, J. D. Lifson, N. Bhardwaj, and M. Larsson. 2007. Pathways utilized by dendritic cells for binding, uptake, processing and presentation of antigens derived from HIV-1. Eur. J. Immunol. 37: 1752-1763.
21. Rossio, J. L., M. T. Esser, K. Suryanarayana, D. K. Schneider, J. W. Bess, Jr., G. M. Vasquez, T. A. Wiltrout, E. Chertova, M. K. Grimes, Q. Sattentau, et al. 1998. Inactivation of human immunodeficiency virus type 1 infectivity with preservation of conformational and functional integrity of virion surface proteins. J. Virol. 72: 7992-8001.
22. Vandesompele, J., K. De Preter, F. Pattyn, B. Poppe, N. Van Roy, A. De Paepe, and F. Speleman. 2002. Accurate normalization of real-time quantitative RT-PCR data by geometric averaging of multiple internal control genes. Genome Biol. 3: research0034.
23. Rieu, I., and S. J. Powers. 2009. Real-time quantitative RT-PCR: design, calculations, and statistics. Plant Cell 21: 1031-1033.
24. Burgener, A., K. Mogk, G. Westmacott, F. Plummer, B. Ball, K. Broliden, and K. Hasselrot. 2012. Salivary basic proline-rich proteins are elevated in HIVexposed seronegative men who have sex with men. AIDS 26: 1857-1867.
25. Elkord, E., P. E. Williams, H. Kynaston, and A. W. Rowbottom. 2005. Human monocyte isolation methods influence cytokine production from in vitro generated dendritic cells. Immunology 114: 204-212.
26. Wilflingseder, D., Z. Banki, E. Garcia, M. Pruenster, G. Pfister, B. Muellauer, D. S. Nikolic, C. Gassner, C. G. Ammann, M. P. Dierich, et al. 2007. IgG opsonization of HIV impedes provirus formation in and infection of dendritic cells and subsequent long-term transfer to T cells. J. Immunol. 178: 7840-7848.
27. Tjomsland, V., R. Ellegård, P. Kjölhede, N. B. Wodlin, J. Hinkula, J. D. Lifson, and M. Larsson. 2013. Blocking of integrins inhibits HIV-1 infection of human cervical mucosa immune cells with free and complement-opsonized virions. Eur. J. Immunol. 43: 2361-2372.
28. Harman, A. N., J. Lai, S. Turville, S. Samarajiwa, L. Gray, V. Marsden, S. K. Mercier, K. Jones, N. Nasr, A. Rustagi, et al. 2011. HIV infection of dendritic cells subverts the IFN induction pathway via IRF-1 and inhibits type 1 IFN production. Blood 118: 298-308.
29. Brown, J., H. Wang, G. N. Hajishengallis, and M. Martin. 2011. TLR-signaling networks: an integration of adaptor molecules, kinases, and cross-talk. J. Dent. Res. 90: 417-427.
30. Weichhart, T., and M. D. Säemann. 2008. The PI3K/Akt/mTOR pathway in innate immune cells: emerging therapeutic applications. Ann. Rheum. Dis. 67 (Suppl. 3): iii70-iii74.
31. Sabbah, A., T. H. Chang, R. Harnack, V. Frohlich, K. Tominaga, P. H. Dube, Y. Xiang, and S. Bose. 2009. Activation of innate immune antiviral responses by Nod2. Nat. Immunol. 10: 1073-1080.
32. Uematsu, S., and S. Akira. 2007. Toll-like receptors and Type I interferons. J. Biol. Chem. 282: 15319-15323.
33. Kuznik, A., M. Bencina, U. Svajger, M. Jeras, B. Rozman, and R. Jerala. 2011. Mechanism of endosomal TLR inhibition by antimalarial drugs and imidazo-quinolines. J. Immunol. 186: 4794-4804.
34. Dai, S., M. V. Rajaram, H. M. Curry, R. Leander, and L. S. Schlesinger. 2013. Fine tuning inflammation at the front door: macrophage complement receptor 3-mediates phagocytosis and immune suppression for Francisella tularensis. PLoS Pathog. 9: e1003114.
35. Hajishengallis, G., M. A. Shakhatreh, M. Wang, and S. Liang. 2007. Complementreceptor 3 blockade promotes IL-12-mediated clearance of Porphyromonas gingivalis and negates its virulence in vivo. J. Immunol. 179: 2359-2367.
36. Zhou, Y., J. Wu, D. F. Kucik, N. B. White, D. T. Redden, A. J. Szalai, D. C. Bullard, and J. C. Edberg. 2013. Multiple lupus-associated ITGAM variants alter Mac-1 functions on neutrophils. Arthritis Rheum. 65: 2907-2916.
37. Rhodes, B., B. G. Furnrohr, A. L. Roberts, G Tzircotis, G. Schett, T. D. Spector, and T. J. Vyse. 2012. The rs1143679 (R77H) lupus associated variant of ITGAM (CD11b) impairs complement receptor 3 mediated functions in human monocytes. Ann. Rheum. Dis. 71: 2028-2034.
38. Gjelstrup, L. C, S. H. Andersen, S. V. Petersen, J. J. Enghild, A. M. Blom, T. Vorup-Jensen, and S. Thiel. 2011. The role of higher-order protein structure in supporting binding by heteroclitic monoclonal antibodies: the monoclonal antibody KIM185 to CD18 also binds C4-binding protein. Mol. Immunol. 49: 38-47.
39. Thornton, B. P., V. Vetvicka, M. Pitman, R. C. Goldman, and G. D. Ross. 1996. Analysis of the sugar specificity and molecular location of the beta-glucan-binding lectin site of complement receptor type 3 (CD11b/CD18). J. Immunol. 156: 1235-1246.
40. Cummings, K. L., S. N. Waggoner, R. Tacke, and Y. S. Hahn. 2007. Role of complement in immune regulation and its exploitation by virus. Viral Immunol. 20: 505-524.
41. Sohn, J. H., P. S. Bora, H. J. Suk, H. Molina, H. J. Kaplan, and N. S. Bora. 2003. Tolerance is dependent on complement C3 fragment iC3b binding to antigen-presenting cells. Nat. Med. 9: 206-212.
42. Skoberne, M., S. Somersan, W Almodovar, T. Truong, K. Petrova, P. M. Henson, and N. Bhardwaj. 2006. The apoptotic-cell receptor CR3, but not αvβ5, is a regulator of human dendritic-cell immunostimulatory function. Blood 108: 947-955.
43. Amarilyo, G., I. Verbovetski, M. Atallah, A. Grau, G Wiser, O. Gil, Y Ben-Neriah, and D. Mevorach. 2010. iC3b-opsonized apoptotic cells mediate a distinct anti-inflammatory response and transcriptional NF-κB-dependent blockade. Eur. J. Immunol. 40: 699-709.
44. Verbovetski, I., H. Bychkov, U. Trahtemberg, I. Shapira, M. Hareuveni, O. Ben-Tal, I. Kutikov, O. Gill, and D. Mevorach. 2002. Opsonization of apoptotic cells by autologous iC3b facilitates clearance by immature dendritic cells, down-regulates DR and CD86, and up-regulates CC chemokine receptor 7. J. Exp. Med. 196: 1553-1561.
45. Pontillo, A., L. T Silva, T. M. Oshiro, C. Finazzo, S. Crovella, and A. J. Duarte. 2012. HIV-1 induces NALP3-inflammasome expression and interleukin-1β secretion in dendritic cells from healthy individuals but not from HIV-positive patients. AIDS 26: 11-18.
46. Lu, B., T. Nakamura, K. Inouye, J. Li, Y Tang, P. Lundbäck, S. I. Valdes-Ferrer, P. S. Olofsson, T Kalb, J. Roth, et al. 2012. Novel role of PKR in inflammasome activation and HMGB1 release. Nature 488: 670-674.
47. Taganov, K. D., M. P. Boldin, K. J. Chang, and D. Baltimore. 2006. NF-κB-dependent induction of microRNA miR-146, an inhibitor targeted to signaling proteins of innate immune responses. Proc. Natl. Acad. Sci. USA 103: 12481-12486.
48. Anand, A. R., A. Prasad, R. R. Bradley, Y S. Deol, T. Nagaraja, X. Ren, E. F Terwilliger, and R. K. Ganju. 2009. HIV-1 gp120-induced migration of dendritic cells is regulated by a novel kinase cascade involving Pyk2, p38 MAP kinase, and LSP1. Blood 114: 3588-3600.
49. Wilflingseder, D., B. Müllauer, H. Schramek, Z. Banki, M. Pruenster, M. P. Dierich, and H. Stoiber. 2004. HIV-1-induced migration of monocyte-derived dendritic cells is associated with differential activation of MAPK pathways. J. Immunol. 173: 7497-7505.
50. Kim, N., S. Kukkonen, Mdel. P. Martinez-Viedma, S. Gupta, and A. Aldovini. 2013. Tat engagement of p38 MAP kinase and IRF7 pathways leads to activation of interferon-stimulated genes in antigen-presenting cells. Blood 121: 4090-4100.
51. Hiscott, J. 2007. Triggering the innate antiviral response through IRF-3 activation. J. Biol. Chem. 282: 15325-15329.
52. Okumura, A., T. Alce, B. Lubyova, H. Ezelle, K. Strebel, and P. M. Pitha. 2008. HIV-1 accessory proteins VPR and Vif modulate antiviral response by targeting IRF-3 for degradation. Virology 373: 85-97.
53. Hajishengallis, G., and J. D. Lambris. 2010. Crosstalk pathways between Tolllike receptors and the complement system. Trends Immunol. 31: 154-163.
54. Keck, S., M. Freudenberg, and M. Huber. 2010. Activation of murine macrophages via TLR2 and TLR4 is negatively regulated by a Lyn/PI3K module and promoted by SHIP1. J. Immunol. 184: 5809-5818.
55. Han, C., J. Jin, S. Xu, H. Liu, N. Li, and X. Cao. 2010. Integrin CD11b negatively regulates TLR-triggered inflammatory responses by activating Syk and promoting degradation of MyD88 and TRIF via Cbl-b. Nat. Immunol. 11: 734-742.
56. Harokopakis, E., M. H. Albzreh, M. H. Martin, and G. Hajishengallis. 2006. TLR2 transmodulates monocyte adhesion and transmigration via Rac1- and PI3K-mediated inside-out signaling in response to Porphyromonas gingivalis fimbriae. J. Immunol. 176: 7645-7656.
57. Fukao, T., and S. Koyasu. 2003. PI3K and negative regulation of TLR signaling. Trends Immunol. 24: 358-363.
58. Napolitani, G., N. Bortoletto, L. Racioppi, A. Lanzavecchia, and U. D'Oro. 2003. Activation of src-family tyrosine kinases by LPS regulates cytokine production in dendritic cells by controlling AP-1 formation. Eur. J. Immunol. 33: 2832-2841.
59. Johnsen, I. B., T. T. Nguyen, M. Ringdal, A. M. Tryggestad, O. Bakke, E. Lien, T. Espevik, and M. W. Anthonsen. 2006. Toll-like receptor 3 associates with c-Src tyrosine kinase on endosomes to initiate antiviral signaling. EMBO J. 25: 3335-3346.
60. Sanjuan, M. A., N. Rao, K. T. Lai, Y. Gu, S. Sun, A. Fuchs, W. P. Fung-Leung, M. Colonna, and L. Karlsson. 2006. CpG-induced tyrosine phosphorylation occurs via a TLR9-independent mechanism and is required for cytokine secretion. J. Cell Biol. 172: 1057-1068.
61. Scapini, P., Y. Hu, C. L. Chu, T. S. Migone, A. L. Defranco, M. A. Cassatella, and C. A. Lowell. 2010. Myeloid cells, BAFF, and IFN-γ establish an inflammatory loop that exacerbates autoimmunity in Lyn-deficient mice. J. Exp. Med. 207: 1757-1773.
62. Lamagna, C., P. Scapini, J. A. van Ziffle, A. L. DeFranco, and C. A. Lowell. 2013. Hyperactivated MyD88 signaling in dendritic cells, through specific deletion of Lyn kinase, causes severe autoimmunity and inflammation. Proc. Natl. Acad. Sci. USA 110: E3311-E3320.
63. Van Lint, C., C. A. Amella, S. Emiliani, M. John, T. Jie, and E. Verdin. 1997. Transcription factor binding sites downstream of the human immunodeficiency virus type 1 transcription start site are important for virus infectivity. J. Virol. 71: 6113-6127.
64. Baruah, P., E. Simpson, I. E. Dumitriu, K. Derbyshire, D. Coe, C. Addey, J. Dyson, J. G. Chai, T. Cook, D. Scott, and M. Botto. 2010. Mice lacking C1q or C3 show accelerated rejection of minor H disparate skin grafts and resistance to induction of tolerance. Eur. J. Immunol. 40: 1758-1767.