IFN priming is necessary but not sufficient to turn on a migratory dendritic cell program in lupus monocytes

Journal of Immunology

Volumn 192, Issue 12, 2014, Pages 5586-5598

  Rodriguez Pla, Alicia ^a   Patel, Pinakeen ^a   Maecker, Holden T ^b   Rossello Urgell, Jose ^a   Baldwin, Nicole ^a   Bennett, Lynda ^a   Cantrell, Victoria ^a   Baisch, Jeanine ^a   Punaro, Marilynn ^c,d   Gotte, Alisa ^c,d   Nassi, Lorien ^c,d   Wright, Tracey ^c,d   Palucka, Anna Karolina ^a   Banchereau, Jacques ^a   Pascual, Virginia ^a,c  

^a BAYLOR INSTITUTE FOR IMMUNOLOGY RESEARCH   (United States)

^b STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c TEXAS SCOTTISH RITE HOSPITAL FOR CHILDREN   (United States)

^d UNIVERSITY OF TEXAS SOUTHWESTERN MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CHEMOKINE RECEPTOR CCR7; INTERFERON; INTERLEUKIN 1BETA; INTERLEUKIN 6;

ADULT; ARTICLE; CD4+ T LYMPHOCYTE; CELL FUNCTION; CELL INTERACTION; CHILD; CONTROLLED STUDY; CYTOKINE RESPONSE; DENDRITIC CELL; FEMALE; HUMAN; HUMAN CELL; IN VITRO STUDY; MAJOR CLINICAL STUDY; MALE; MONOCYTE; NUCLEAR REPROGRAMMING; PHENOTYPE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; SIGNAL TRANSDUCTION; SYSTEMIC LUPUS ERYTHEMATOSUS; TRANSCRIPTION REGULATION;

ADOLESCENT; ADULT; CELL MOVEMENT; CHILD; CYTOKINES; DENDRITIC CELLS; FEMALE; HUMANS; INTERFERON TYPE I; LIPOPOLYSACCHARIDES; LUPUS ERYTHEMATOSUS, SYSTEMIC; RECEPTORS, CCR7; TOLL-LIKE RECEPTORS;

EID: 84902212735     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1301319     Document Type: Article

References (71)

1. Barber, C., W. L. Gold, and P. R. Fortin. 2011. Infections in the lupus patient: perspectives on prevention. Curr. Opin. Rheumatol. 23:358-365.
2. Sallusto, F., and A. Lanzavecchia. 1994. Efficient presentation of soluble antigen by cultured human dendritic cells is maintained by granulocyte/macrophage colony-stimulating factor plus interleukin 4 and downregulated by tumor necrosis factor alpha. J. Exp. Med. 179:1109-1118.
3. Romani, N., S. Gruner, D. Brang, E. Kämpgen, A. Lenz, B. Trockenbacher, G. Konwalinka, P. O. Fritsch, R. M. Steinman, and G. Schuler. 1994. Proliferating dendritic cell progenitors in human blood. J. Exp. Med. 180:83-93.
4. Randolph, G. J., S. Beaulieu, S. Lebecque, R. M. Steinman, and W. A. Muller. 1998. Differentiation of monocytes into dendritic cells in a model of transendothelial trafficking. Science 282:480-483.
5. Serbina, N. V., T. M. Hohl, M. Cherny, and E. G. Pamer. 2009. Selective expansion of the monocytic lineage directed by bacterial infection. J. Immunol. 183:1900-1910.
6. Cheong, C., I. Matos, J. H. Choi, D. B. Dandamudi, E. Shrestha, M. P. Longhi, K. L. Jeffrey, R. M. Anthony, C. Kluger, G. Nchinda, et al. 2010. Microbial stimulation fully differentiates monocytes to DC-SIGN/CD209+ dendritic cells for immune T cell areas. Cell 143:416-429.
7. Segura, E., M. Touzot, A. Bohineust, A. Cappuccio, G. Chiocchia, A. Hosmalin, M. Dalod, V. Soumelis, and S. Amigorena. 2013. Human inflammatory dendritic cells induce Th17 cell differentiation. Immunity 38:336-348.
8. Blanco, P., A. K. Palucka, M. Gill, V. Pascual, and J. Banchereau. 2001. Induction of dendritic cell differentiation by IFN-a in systemic lupus erythematosus. Science 294:1540-1543.
9. Banchereau, J., V. Pascual, and A. K. Palucka. 2004. Autoimmunity through cytokine-induced dendritic cell activation. Immunity 20:539-550.
10. Joo, H., C. Coquery, Y. Xue, I. Gayet, S. R. Dillon, M. Punaro, G. Zurawski, J. Banchereau, V. Pascual, and S. Oh. 2012. Serum from patients with SLE instructs monocytes to promote IgG and IgA plasmablast differentiation. J. Exp. Med. 209:1335-1348.
11. Fuss, I. J., Kanof, M. E., Smith, P. D. and Zola, H. 2009. Isolation of whole mononuclear cells from peripheral blood and cord blood. Curr. Protoc. Immunol. Chapter 7: Unit 7.1.doi:10.1002/0471142735.im0701s85
12. Kronenberger, B., B. Rüster, R. Elez, S. Weber, A. Piiper, J. H. Lee, W. K. Roth, and S. Zeuzem. 2001. Interferon alfa down-regulates CD81 in patients with chronic hepatitis C. Hepatology 33:1518-1526.
13. Frleta, D., C. E. Ochoa, H. B. Kramer, S. A. Khan, A. R. Stacey, P. Borrow, B. M. Kessler, B. F. Haynes, and N. Bhardwaj. 2012. HIV-1 infection-induced apoptotic microparticles inhibit human DCs via CD44. J. Clin. Invest. 122:4685-4697.
14. Steinberger, P., A. Szekeres, S. Wille, J. Stöckl, N. Selenko, E. Prager, G. Staffler, O. Madic, H. Stockinger, and W. Knapp. 2002. Identification of human CD93 as the phagocytic C1q receptor (C1qRp) by expression cloning. J. Leukoc. Biol. 71:133-140.
15. McGreal, E. P., N. Ikewaki, H. Akatsu, B. P. Morgan, and P. Gasque. 2002. Human C1qRp is identical with CD93 and the mNI-11 antigen but does not bind C1q. J. Immunol. 168:5222-5232.
16. Norsworthy, P. J., L. Fossati-Jimack, J. Cortes-Hernandez, P. R. Taylor, A. E. Bygrave, R. D. Thompson, S. Nourshargh, M. J. Walport, and M. Botto. 2004. Murine CD93 (C1qRp) contributes to the removal of apoptotic cells in vivo but is not required for C1q-mediated enhancement of phagocytosis. J. Immunol. 172:3406-3414.
17. Kato, M., S. Khan, E. D'Aniello, K. J. McDonald, and D. N. Hart. 2007. The novel endocytic and phagocytic C-type lectin receptor DCL-1/CD302 on macrophages is colocalized with F-actin, suggesting a role in cell adhesion and migration. J. Immunol. 179:6052-6063.
18. Mezyk-Kopeć, R., M. Bzowska, K. Stalińska, T. Chełmicki, M. Podkalicki, J. Jucha, K. Kowalczyk, P. Mak, and J. Bereta. 2009. Identification of ADAM10 as a major TNF sheddase in ADAM17-deficient fibroblasts. Cytokine 46:309-315.
19. Aringer, M., E. Feierl, G. Steiner, G. H. Stummvoll, E. Höfler, C. W. Steiner, I. Radda, J. S. Smole, and W. B. Graninger. 2002. Increased bioactive TNF in human systemic lupus erythematosus: associations with cell death. Lupus 11:102-108.
20. Gabay, C., N. Cakir, F. Moral, P. Roux-Lombard, O. Meyer, J. M. Dayer, T. Vischer, H. Yazici, and P. A. Guerne. 1997. Circulating levels of tumor necrosis factor soluble receptors in systemic lupus erythematosus are significantly higher than in other rheumatic diseases and correlate with disease activity. J. Rheumatol. 24:303-308.
21. Studnicka-Benke, A., G. Steiner, P. Petera, and J. S. Smolen. 1996. Tumour necrosis factor a and its soluble receptors parallel clinical disease and autoimmune activity in systemic lupus erythematosus. Br. J. Rheumatol. 35:1067-1074.
22. Sabry, A., S. R. Elbasyouni, H. A. Sheashaa, A. A. Alhusseini, K. Mahmoud, S. K. George, E. A. Kaleek, H. Abo-Zena, A. M. Kalil, T. Mohsen, et al. 2006. Correlation between levels of TNF-α and IL-6 and hematological involvement in SLE Egyptian patients with lupus nephritis. Int. Urol. Nephrol. 38:731-737.
23. Akilesh, S., A. Koziell, and A. S. Shaw. 2007. Basic science meets clinical medicine: identification of a CD2AP-deficient patient. Kidney Int. 72:1181-1183.
24. Chavan, S. S., W. Tian, K. Hsueh, D. Jawaheer, P. K. Gregersen, and C. C. Chu. 2002. Characterization of the human homolog of the IL-4 induced gene-1 (Fig1). Biochim. Biophys. Acta 1576:70-80.
25. Su, L., and M. David. 2000. Distinct mechanisms of STAT phosphorylation via the interferon-a/b receptor. Selective inhibition of STAT3 and STAT5 by piceatannol. J. Biol. Chem. 275:12661-12666.
26. Yang, C. H., A. Murti, S. J. Baker, M. Frangou-Lazaridis, A. B. Vartapetian, K. G. Murti, and L. M. Pfeffer. 2004. Interferon induces the interaction of prothymosin - a with STAT3 and results in the nuclear translocation of the complex. Exp. Cell Res. 298:197-206.
27. Snyder, M., X. Y. Huang, and J. J. Zhang. 2011. Signal transducers and activators of transcription 3 (STAT3) directly regulates cytokine-induced fascin expression and is required for breast cancer cell migration. J. Biol. Chem. 286:38886-38893.
28. Bennett, L., A. K. Palucka, E. Arce, V. Cantrell, J. Borvak, J. Banchereau, and V. Pascual. 2003. Interferon and granulopoiesis signatures in systemic lupus erythematosus blood. J. Exp. Med. 197:711-723.
29. Grage-Griebenow, E., H. D. Flad, M. Ernst, M. Bzowska, J. Skrzeczyñska, and J. Pryjma. 2000. Human MO subsets as defined by expression of CD64 and CD16 differ in phagocytic activity and generation of oxygen intermediates. Immunobiology 202:42-50.
30. Langlet, C., S. Tamoutounour, S. Henri, H. Luche, L. Ardouin, C. Grégoire, B. Malissen, and M. Guilliams. 2012. CD64 expression distinguishes monocytederived and conventional dendritic cells and reveals their distinct role during intramuscular immunization. J. Immunol. 188:1751-1760.
31. Crighton, D., S. Wilkinson, J. O'Prey, N. Syed, P. Smith, P. R. Harrison, M. Gasco, O. Garrone, T. Crook, and K. M. Ryan. 2006. DRAM, a p53-induced modulator of autophagy, is critical for apoptosis. Cell 126:121-134.
32. Sepulveda, F. E., S. Maschalidi, R. Colisson, L. Heslop, C. Ghirelli, E. Sakka, A. M. Lennon-Duménil, S. Amigorena, L. Cabanie, and B. Manoury. 2009. Critical role for asparagine endopeptidase in endocytic Toll-like receptor signaling in dendritic cells. Immunity 31:737-748.
33. Ewald, S. E., A. Engel, J. Lee, M. Wang, M. Bogyo, and G. M. Barton. 2011. Nucleic acid recognition by Toll-like receptors is coupled to stepwise processing by cathepsins and asparagine endopeptidase. J. Exp. Med. 208:643-651.
34. Granucci, F., F. Petralia, M. Urbano, S. Citterio, F. Di Tota, L. Santambrogio, and P. Ricciardi-Castagnoli. 2003. The scavenger receptor MARCO mediates cytoskeleton rearrangements in dendritic cells and microglia. Blood 102:2940-2947.
35. Campanella, G. S., E. M. Lee, J. Sun, and A. D. Luster. 2003. CXCR3 and heparin binding sites of the chemokine IP-10 (CXCL10). J. Biol. Chem. 278:17066-17074.
36. Ben-Sasson, S. Z., A. Hogg, J. Hu-Li, P. Wingfield, X. Chen, M. Crank, S. Caucheteux, M. Ratner-Hurevich, J. A. Berzofsky, R. Nir-Paz, and W. E. Paul. 2013. IL-1 enhances expansion, effector function, tissue localization, and memory response of antigen-specific CD8 T cells. J. Exp. Med. 210:491-502.
37. Dzionek, A., A. Fuchs, P. Schmidt, S. Cremer, M. Zysk, S. Miltenyi, D. W. Buck, and J. Schmitz. 2000. BDCA-2, BDCA-3, and BDCA-4: three markers for distinct subsets of dendritic cells in human peripheral blood. J. Immunol. 165:6037-6046.
38. Patterson, S., H. Donaghy, P. Amjadi, B. Gazzard, F. Gotch, and P. Kelleher. 2005. Human BDCA-1-positive blood dendritic cells differentiate into phenotypically distinct immature and mature populations in the absence of exogenous maturational stimuli: differentiation failure in HIV infection. J. Immunol. 174:8200-8209.
39. Geissmann, F., S. Jung, and D. R. Littman. 2003. Blood monocytes consist of two principal subsets with distinct migratory properties. Immunity 19:71-82.
40. Auffray, C., D. Fogg, M. Garfa, G. Elain, O. Join-Lambert, S. Kayal, S. Sarnacki, A. Cumano, G. Lauvau, and F. Geissmann. 2007. Monitoring of blood vessels and tissues by a population ofmonocyteswith patrolling behavior. Science 317:666-670.
41. Serbina, N. V., and E. G. Pamer. 2008. Coordinating innate immune cells to optimize microbial killing. Immunity 29:672-674.
42. Serbina, N. V., T. P. Salazar-Mather, C. A. Biron, W. A. Kuziel, and E. G. Pamer. 2003. TNF/iNOS-producing dendritic cells mediate innate immune defense against bacterial infection. Immunity 19:59-70.
43. Zigmond, E., and S. Jung. 2013. Intestinal macrophages: well educated exceptions from the rule. Trends Immunol. 34:162-168.
44. Steinbach, F., F. Henke, B. Krause, B. Thiele, G. R. Burmester, and F. Hiepe. 2000. Monocytes from systemic lupus erythematous patients are severely altered in phenotype and lineage flexibility. Ann. Rheum. Dis. 59:283-288.
45. + monocytes in coronary artery disease and their relationship to serum TNF-α levels. Thromb. Haemost. 92:419-424.
46. +, peripheral blood monocytes in severe asthmatic patients. Clin. Immunol. 130:338-346.
47. Heron, M., J. C. Grutters, H. Van Velzen-Blad, M. Veltkamp, A. M. Claessen, and J. M. Van Den Bosch. 2008. Increased expression of CD16, CD69, and very late antigen-1 on blood monocytes in active sarcoidosis. Chest 134:1001-1008.
48. + monocyte subset is expanded in rheumatoid arthritis and promotes expansion of the Th17 cell population. Arthritis Rheum. 64:671-677.
49. Lorenz, H. M., M. Grünke, T. Hieronymus, M. Herrmann, A. Kühnel, B. Manger, and J. R. Kalden. 1997. In vitro apoptosis and expression of apoptosis-related molecules in lymphocytes from patients with systemic lupus erythematosus and other autoimmune diseases. Arthritis Rheum. 40:306-317.
50. Klint, C., L. Truedsson, A. Andreasson, I. Johansson, and G. Sturfelt. 2000. Toxic effects of SLE serum on normal monocytes in vitro: cell death induced by apoptosis related to complement dysfunction. Lupus 9:278-287.
51. Bengtsson, A. A., G. Sturfelt, B. Gullstrand, and L. Truedsson. 2004. Induction of apoptosis in monocytes and lymphocytes by serum from patients with systemic lupus erythematosus: an additional mechanism to increased autoantigen load? Clin. Exp. Immunol. 135:535-543.
52. Xu, W., H. Joo, S. Clayton, M. Dullaers, M. C. Herve, D. Blankenship, M. T. De La Morena, R. Balderas, C. Picard, J. L. Casanova, et al. 2012. Macrophages induce differentiation of plasma cells through CXCL10/IP-10. J. Exp. Med. 209:1813-1823.
53. Narumi, S., T. Takeuchi, Y. Kobayashi, and K. Konishi. 2000. Serum levels of IFN-inducible protein-10 relating to the activity of systemic lupus erythematosus. Cytokine 12:1561-1565.
54. Lit, L. C., C. K. Wong, L. S. Tam, E. K. Li, and C. W. Lam. 2006. Raised plasma concentration and ex vivo production of inflammatory chemokines in patients with systemic lupus erythematosus. Ann. Rheum. Dis. 65:209-215.
55. Okamoto, H., N. Iikuni, S. Kamitsuji, T. Yoshio, S. Minota, and N. Kamatani. 2006. IP-10/MCP-1 ratio in CSF is an useful diagnostic marker of neuropsychiatric lupus patients. Rheumatology (Oxford) 45:232-234.
56. Kaneko, H., H. Ogasawara, T. Naito, H. Akimoto, S. Lee, T. Hishikawa, I. Sekigawa, Y. Tokano, Y. Takasaki, S. I. Hirose, and H. Hashimoto. 1999. Circulating levels of b-chemokines in systemic lupus erythematosus. J. Rheumatol. 26:568-573.
57. Iikuni, N., H. Okamoto, T. Yoshio, E. Sato, S. Kamitsuji, T. Iwamoto, S. Momohara, A. Taniguchi, H. Yamanaka, S. Minota, and N. Kamatani. 2006. Raised monocyte chemotactic protein-1 (MCP-1)/CCL2 in cerebrospinal fluid of patients with neuropsychiatric lupus. Ann. Rheum. Dis. 65:253-256.
58. Bhardwaj, V., and M. J. Colston. 1988. The processing and presentation of mycobacterial antigens by human monocytes. Eur. J. Immunol. 18:691-696.
59. Guarda, G., M. Braun, F. Staehli, A. Tardivel, C. Mattmann, I. Förster, M. Farlik, T. Decker, R. A. Du Pasquier, P. Romero, and J. Tschopp. 2011. Type I interferon inhibits interleukin-1 production and inflammasome activation. Immunity 34:213-223.
60. Kim, S. J., P. K. Gregersen, and B. Diamond. 2013. Regulation of dendritic cell activation by microRNA let-7c and BLIMP1. J. Clin. Invest. 123:823-833.
61. Vallin, H., A. Perers, G. V. Alm, and L. Rönnblom. 1999. Anti-double-stranded DNA antibodies and immunostimulatory plasmid DNA in combination mimic the endogenous IFN-a inducer in systemic lupus erythematosus. J. Immunol. 163:6306-6313.
62. Yu, S. L., W. P. Kuan, C. K. Wong, E. K. Li, and L. S. Tam. 2012. Immunopathological roles of cytokines, chemokines, signaling molecules, and patternrecognition receptors in systemic lupus erythematosus. Clin. Dev. Immunol. 2012:715190.
63. Graham, R. R., S. V. Kozyrev, E. C. Baechler, M. V. Reddy, R. M. Plenge, J. W. Bauer, W. A. Ortmann, T. Koeuth, M. F. González Escribano, B. Pons-Estel, et al; Argentine and Spanish Collaborative Groups. 2006. A common haplotype of interferon regulatory factor 5 (IRF5) regulates splicing and expression and is associated with increased risk of systemic lupus erythematosus. Nat. Genet. 38:550-555.
64. Sigurdsson, S., G. Nordmark, H. H. Göring, K. Lindroos, A. C. Wiman, G. Sturfelt, A. Jönsen, S. Rantapää-Dahlqvist, B. Möller, J. Kere, et al. 2005. Polymorphisms in the tyrosine kinase 2 and interferon regulatory factor 5 genes are associated with systemic lupus erythematosus. Am. J. Hum. Genet. 76:528-537.
65. Worbs, T., and R. Förster. 2007. A key role for CCR7 in establishing central and peripheral tolerance. Trends Immunol. 28:274-280.
66. Moschovakis, G. L., and R. Förster. 2012. Multifaceted activities of CCR7 regulate T-cell homeostasis in health and disease. Eur. J. Immunol. 42:1949-1955.
67. Van Lent, P. L., C. G. Figdor, P. Barrera, K. Van Ginkel, A. Slöetjes, W. B. Van Den Berg, and R. Torensma. 2003. Expression of the dendritic cell-associated C-type lectin DC-SIGN by inflammatory matrix metalloproteinaseproducing macrophages in rheumatoid arthritis synovium and interaction with intercellular adhesion molecule 3-positive T cells. Arthritis Rheum. 48:360-369.
68. Zandman-Goddard, G., and Y. Shoenfeld. 2003. SLE and infections. Clin. Rev. Allergy Immunol. 25:29-40.
69. Rodríguez-Pla, A., and J. H. Stone. 2006. Vasculitis and systemic infections. Curr. Opin. Rheumatol. 18:39-47.
70. Di Luzio, N. R., and T. J. Friedmann. 1973. Letter: bacterial endotoxins in the environment. Nature 244:49-51.
71. Fu, Y., C. Xie, J. Chen, J. Zhu, H. Zhou, J. Thomas, X. J. Zhou, and C. Mohan. 2006. Innate stimuli accentuate end-organ damage by nephrotoxic antibodies via Fc receptor and TLR stimulation and IL-1/TNF-α production. J. Immunol. 176:632-639