Blockade of Notch1 signaling alleviates murine lupus via blunting macrophage activation and M2b polarization

Journal of Immunology

Volumn 184, Issue 11, 2010, Pages 6465-6478

  Zhang, Weijuan ^a   Xu, Wei ^a   Xiong, Sidong ^a,b  

^a FUDAN UNIVERSITY   (China)

^b SOOCHOW UNIVERSITY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

DNA; GAMMA SECRETASE INHIBITOR; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; MITOGEN ACTIVATED PROTEIN KINASE; NOTCH1 RECEPTOR; PHOSPHATIDYLINOSITOL 3 KINASE; PROTEIN P50;

ANIMAL CELL; ANIMAL MODEL; ARTICLE; CELL INFILTRATION; CELL NUCLEUS; CONTROLLED STUDY; FEMALE; GENE TRANSLOCATION; IMMUNIZATION; IN VITRO STUDY; IN VIVO STUDY; LYMPHOCYTE ACTIVATION; MACROPHAGE; MACROPHAGE ACTIVATION; MOUSE; NEPHRITIS; NONHUMAN; POLARIZATION; PRIORITY JOURNAL; SIGNAL TRANSDUCTION; SYSTEMIC LUPUS ERYTHEMATOSUS; UPREGULATION; ANIMAL; BAGG ALBINO MOUSE; CELL SEPARATION; ENZYME LINKED IMMUNOSORBENT ASSAY; FLOW CYTOMETRY; GENETIC TRANSFECTION; IMMUNOLOGY; METABOLISM; PROTEIN TRANSPORT; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; WESTERN BLOTTING;

1-PHOSPHATIDYLINOSITOL 3-KINASE; ANIMALS; BLOTTING, WESTERN; CELL SEPARATION; ENZYME-LINKED IMMUNOSORBENT ASSAY; EXTRACELLULAR SIGNAL-REGULATED MAP KINASES; FEMALE; FLOW CYTOMETRY; LUPUS ERYTHEMATOSUS, SYSTEMIC; MACROPHAGE ACTIVATION; MACROPHAGES; MICE; MICE, INBRED BALB C; NF-KAPPA B P50 SUBUNIT; PROTEIN TRANSPORT; RECEPTOR, NOTCH1; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION; TRANSFECTION;

EID: 77953474634     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.0904016     Document Type: Article

References (70)

1. Rahman, A., and D. A. Isenberg. 2008. Systemic lupus erythematosus. N. Engl. J. Med. 358: 929-939.
2. Kotzin, B. L. 1996. Systemic lupus erythematosus. Cell 85: 303-306.
3. Teachey, D. T., A. E. Seif, V. I. Brown, M. Bruno, R. M. Bunte, Y. J. Chang, J. K. Choi, J. D. Fish, J. Hall, G. S. Reid, et al. 2008. Targeting Notch signaling in autoimmune and lymphoproliferative disease. Blood 111: 705-714.
4. Davidson, A., and B. Diamond. 2001. Autoimmune diseases. N. Engl. J. Med. 345: 340-350.
5. Desai, D. D., M. R. Krishnan, J. T. Swindle, andT. N. Marion. 1993. Antigen-specific induction of antibodies against native mammalian DNA in nonautoimmune mice. J. Immunol. 151: 1614-1626.
6. Vinuesa, C. G., and C. C. Goodnow. 2002. Immunology: DNA drives autoimmunity. Nature 416: 595-598.
7. Pisetsky, D. S. 1996. The immunologic properties of DNA. J. Immunol. 156: 421-423.
8. Leadbetter, E. A., I. R. Rifkin, A. M. Hohlbaum, B. C. Beaudette, M. J. Shlomchik, and A. Marshak-Rothstein. 2002. Chromatin-IgG complexes activate B cells by dual engagement of IgM and Toll-like receptors. Nature 416: 603-607.
9. Qiao, B., J. Wu, Y. W. Chu, Y. Wang, D. P. Wang, H. S. Wu, andS. D. Xiong. 2005. Induction of systemic lupus erythematosus-like syndrome in syngeneic mice by immunization with activated lymphocyte-derived DNA. Rheumatology (Oxford) 44: 1108-1114.
10. Wen, Z. K., W. Xu, L. Xu, Q. H. Cao, Y. Wang, Y. W. Chu, andS. D. Xiong. 2007. DNA hypomethylation is crucial for apoptotic DNA to induce systemic lupus erythematosus-like autoimmune disease in SLE-non-susceptible mice. Rheumatology (Oxford) 46: 1796-1803.
11. Schiffer, L., R. Bethunaickan, M. Ramanujam, W. Huang, M. Schiffer, H. Tao, M. P. Madaio, M. M. Madaio, E. P. Bottinger, and A. Davidson. 2008. Activated renal macrophages are markers of disease onset and disease remission in lupus nephritis. [Published erratum in 2008. J. Immunol. 180: 3613.] J. Immunol. 180: 1938-1947.
12. Liu, K., and C. Mohan. 2006. What do mouse models teach us about human SLE? Clin. Immunol. 119: 123-130. (Pubitemid 43786185)
13. Paulson, J. C. 2007. Innate immune response triggers lupus-like autoimmune disease. Cell 130: 589-591. (Pubitemid 47268067)
14. Green, R. S., E. L. Stone, M. Tenno, E. Lehtonen, M. G. Farquhar, andJ. D. Marth. 2007. Mammalian N-glycan branching protects against innate immune self-recognition and inflammation in autoimmune disease pathogenesis. Immunity 27: 308-320.
15. Hutcheson, J., J. C. Scatizzi, A. M. Siddiqui, G. K. Haines, 3rd, T. Wu, Q. Z. Li, L. S. Davis, C. Mohan, and H. Perlman. 2008. Combined deficiency of proapoptotic regulators Bim and Fas results in the early onset of systemic autoimmunity. Immunity 28: 206-217. (Pubitemid 351215233)
16. Hill, G. S., M. Delahousse, D. Nochy, P. Rémy, F. Mignon, J. P. Méry, andJ. Bariéty. 2001. Predictive power of the second renal biopsy in lupus nephritis: significance of macrophages. Kidney Int. 59: 304-316.
17. Jothy, S., andR. J. Sawka. 1981. Presence of monocytes in systemic lupus erythematosus-associated glomerulonephritis: marker study and significance. Arch. Pathol. Lab. Med. 105: 590-593.
18. Kobayashi, M., A. Koyama, M. Narita, and H. Shigematsu. 1991. Intra-glomerular monocytes in human glomerulonephritis. Nephron 59: 580-585.
19. Lan, H. Y., D. J. Nikolic-Paterson, W. Mu, andR. C. Atkins. 1995. Local macrophage proliferation in the progression of glomerular and tubulointerstitial injury in rat anti-GBM glomerulonephritis. Kidney Int. 48: 753-760.
20. Mosser, D. M., andJ. P. Edwards. 2008. Exploring the full spectrum of macrophage activation. Nat. Rev. Immunol. 8: 958-969.
21. Mantovani, A., A. Sica, andM. Locati. 2005. Macrophage polarization comes of age. Immunity 23: 344-346.
22. Benoit, M., B. Desnues, andJ. L. Mege. 2008. Macrophage polarization in bacterial infections. J. Immunol. 181: 3733-3739.
23. Martinez, F. O., L. Helming, andS. Gordon. 2009. Alternative activation of macrophages: an immunologic functional perspective. Annu. Rev. Immunol. 27: 451-483.
24. Mantovani, A., A. Sica, S. Sozzani, P. Allavena, A. Vecchi, andM. Locati. 2004. The chemokine system in diverse forms of macrophage activation and polarization. Trends Immunol. 25: 677-686. (Pubitemid 39457982)
25. Li, K., W. Xu, Q. Guo, Z. Jiang, P. Wang, Y. Yue, andS. Xiong. 2009. Differential macrophage polarization in male and female BALB/c mice infected with coxsackievirus B3 defines susceptibility to viral myocarditis. Circ. Res. 105: 353-364.
26. Gordon, S. 2003. Alternative activation of macrophages. Nat. Rev. Immunol. 3: 23-35.
27. Artavanis-Tsakonas, S., M. D. Rand, andR. J. Lake. 1999. Notch signaling: cell fate control and signal integration in development. Science 284: 770-776.
28. Maillard, I., T. Fang, andW. S. Pear. 2005. Regulation of lymphoid development, differentiation, and function by the Notch pathway. Annu. Rev. Immunol. 23: 945-974.
29. Tanigaki, K., andT. Honjo. 2007. Regulation of lymphocyte development by Notch signaling. Nat. Immunol. 8: 451-456.
30. Ohishi, K., B. Varnum-Finney, R. E. Serda, C. Anasetti, and I. D. Bernstein. 2001. The Notch ligand, Delta-1, inhibits the differentiation of monocytes into macrophages but permits their differentiation into dendritic cells. Blood 98: 1402-1407.
31. Hu, X., A. Y. Chung, I. Wu, J. Foldi, J. Chen, J. D. Ji, T. Tateya, Y. J. Kang, J. Han, M. Gessler, et al. 2008. Integrated regulation of Toll-like receptor responses by Notch and interferon-gamma pathways. Immunity 29: 691-703.
32. Palaga, T., C. Buranaruk, S. Rengpipat, A. H. Fauq, T. E. Golde, S. H. Kaufmann, and B. A. Osborne. 2008. Notch signaling is activated by TLR stimulation and regulates macrophage functions. Eur. J. Immunol. 38: 174-183.
33. Narayana, Y., andK. N. Balaji. 2008. NOTCH1 up-regulation and signaling involved in Mycobacterium bovis BCG-induced SOCS3 expression in macrophages. J. Biol. Chem. 283: 12501-12511.
34. Monsalve, E., M. A. Pérez, A. Rubio, M. J. Ruiz-Hidalgo, V. Baladrón, J. J. García-Ramírez, J. C. Gómez, J. Laborda, andM. J. Díaz-Guerra. 2006. Notch-1 up-regulation and signaling following macrophage activation modulates gene expression patterns known to affect antigen-presenting capacity and cytotoxic activity. J. Immunol. 176: 5362-5373.
35. Ito, T., M. Schaller, C. M. Hogaboam, T. J. Standiford, M. Sandor, N. W. Lukacs, S. W. Chensue, andS. L. Kunkel. 2009. TLR9 regulates the mycobacteria-elicited pulmonary granulomatous immune response in mice through DC-derived Notch ligand delta-like 4. J. Clin. Invest. 119: 33-46.
36. Sato, M., H. Suemori, N. Hata, M. Asagiri, K. Ogasawara, K. Nakao, T. Nakaya, M. Katsuki, S. Noguchi, N. Tanaka, andT. Taniguchi. 2000. Distinct and essential roles of transcription factors IRF-3 and IRF-7 in response to viruses for IFN-alpha/beta gene induction. Immunity 13: 539-548.
37. Takaoka, A., H. Yanai, S. Kondo, G. Duncan, H. Negishi, T. Mizutani, S. Kano, K. Honda, Y. Ohba, T. W. Mak, andT. Taniguchi. 2005. Integral role of IRF-5 in the gene induction programme activated by Toll-like receptors. Nature 434: 243-249. (Pubitemid 40388058)
38. Capozzo, A. V., K. Ramírez, J. M. Polo, J. Ulmer, E. M. Barry, M. M. Levine, andM. F. Pasetti. 2006. Neonatal immunization with a Sindbis virus-DNA measles vaccine induces adult-like neutralizing antibodies and cell-mediated immunity in the presence of maternal antibodies. J. Immunol. 176: 5671-5681.
39. Perez, O. D., and G. P. Nolan. 2002. Simultaneous measurement of multiple active kinase states using polychromatic flow cytometry. Nat. Biotechnol. 20: 155-162.
40. Lumeng, C. N., J. L. Bodzin, and A. R. Saltiel. 2007. Obesity induces a phenotypic switch in adipose tissue macrophage polarization. J. Clin. Invest. 117: 175-184.
41. Gao, B., Z. Duan, W. Xu, andS. Xiong. 2009. Tripartite motif-containing 22 inhibits the activity of hepatitis B virus core promoter, which is dependent on nuclear-located RING domain. Hepatology 50: 424-433.
42. Minhajuddin, M., F. Fazal, K. M. Bijli, M. R. Amin, and A. Rahman. 2005. Inhibition of mammalian target of rapamycin potentiates thrombin-induced intercellular adhesion molecule-1 expression by accelerating and stabilizing NF-kappa B activation in endothelial cells. J. Immunol. 174: 5823-5829. (Pubitemid 40593227)
43. Chung, E. Y., J. Liu, Y. Homma, Y. Zhang, A. Brendolan, M. Saggese, J. Han, R. Silverstein, L. Selleri, andX. Ma. 2007. Interleukin-10 expression in macrophages during phagocytosis of apoptotic cells is mediated by homeodomain proteins Pbx1 and Prep-1. Immunity 27: 952-964.
44. Guan, E., J. Wang, J. Laborda, M. Norcross, P. A. Baeuerle, andT. Hoffman. 1996. T cell leukemia-associated human Notch/translocation-associated Notch homologue has I kappa B-like activity and physically interacts with nuclear factor-kappa B proteins in T cells. J. Exp. Med. 183: 2025-2032.
45. Rosati, E., R. Sabatini, G. Rampino, A. Tabilio, M. Di Ianni, K. Fettucciari, A. Bartoli, S. Coaccioli, I. Screpanti, andP. Marconi. 2009. Constitutively activated Notch signaling is involved in survival and apoptosis resistance of B-CLL cells. Blood 113: 856-865.
46. McKenzie, G., G. Ward, Y. Stallwood, E. Briend, S. Papadia, A. Lennard, M. Turner, B. Champion, and G. E. Hardingham. 2006. Cellular Notch responsiveness is defined by phosphoinositide 3-kinase-dependent signals. BMC Cell Biol. 7: 10.
47. Liu, Z. J., M. Xiao, K. Balint, K. S. Smalley, P. Brafford, R. Qiu, C. C. Pinnix, X. Li, andM. Herlyn. 2006. Notch1 signaling promotes primary melanoma progression by activating mitogen-activated protein kinase/phosphatidylinositol 3-kinase-Akt pathways and up-regulating N-cadherin expression. Cancer Res. 66: 4182-4190.
48. Sade, H., S. Krishna, and A. Sarin. 2004. The anti-apoptotic effect of Notch-1 requires p56lck-dependent, Akt/PKB-mediated signaling in T cells. J. Biol. Chem. 279: 2937-2944.
49. Savill, J., I. Dransfield, C. Gregory, and C. Haslett. 2002. A blast from the past: clearance of apoptotic cells regulates immune responses. Nat. Rev. Immunol. 2: 965-975.
50. Okabe, Y., K. Kawane, S. Akira, T. Taniguchi, andS. Nagata. 2005. Toll-like receptor-independent gene induction program activated by mammalian DNA escaped from apoptotic DNA degradation. J. Exp. Med. 202: 1333-1339.
51. Mukundan, L., J. I. Odegaard, C. R. Morel, J. E. Heredia, J. W. Mwangi, R. R. Ricardo-Gonzalez, Y. P. Goh, A. R. Eagle, S. E. Dunn, J. U. Awakuni, et al. 2009. PPAR-delta senses and orchestrates clearance of apoptotic cells to promote tolerance. Nat. Med. 15: 1266-1272.
52. Napirei, M., H. Karsunky, B. Zevnik, H. Stephan, H. G. Mannherz, andT. Möröy. 2000. Features of systemic lupus erythematosus in Dnase1-deficient mice. Nat. Genet. 25: 177-181.
53. Bickerstaff, M. C., M. Botto, W. L. Hutchinson, J. Herbert, G. A. Tennent, A. Bybee, D. A. Mitchell, H. T. Cook, P. J. Butler, M. J. Walport, andM. B. Pepys. 1999. Serum amyloid P component controls chromatin degradation and prevents antinuclear autoimmunity. Nat. Med. 5: 694-697.
54. Familian, A., B. Zwart, H. G. Huisman, I. Rensink, D. Roem, P. L. Hordijk, L. A. Aarden, and C. E. Hack. 2001. Chromatin-independent binding of serum amyloid P component to apoptotic cells. J. Immunol. 167: 647-654.
55. Botto, M., C. Dell'Agnola, A. E. Bygrave, E. M. Thompson, H. T. Cook, F. Petry, M. Loos, P. P. Pandolfi, andM. J. Walport. 1998. Homozygous C1q deficiency causes glomerulonephritis associated with multiple apoptotic bodies. Nat. Genet. 19: 56-59.
56. Yu, C. C., H. W. Tsui, B. Y. Ngan, M. J. Shulman, G. E. Wu, and F. W. Tsui. 1996. B and T cells are not required for the viable motheaten phenotype. J. Exp. Med. 183: 371-380.
57. Radtke, F., A. Wilson, S. J. Mancini, and H. R. MacDonald. 2004. Notch regulation of lymphocyte development and function. Nat. Immunol. 5: 247-253.
58. Besseyrias, V., E. Fiorini, L. J. Strobl, U. Zimber-Strobl, A. Dumortier, U. Koch, M. L. Arcangeli, S. Ezine, H. R. Macdonald, and F. Radtke. 2007. Hierarchy of Notch-Delta interactions promoting T cell lineage commitment and maturation. J. Exp. Med. 204: 331-343.
59. Jenkinson, E. J., W. E. Jenkinson, S. W. Rossi, and G. Anderson. 2006. The thymus and T-cell commitment: the right niche for Notch? Nat. Rev. Immunol. 6: 551-555.
60. Fang, T. C., Y. Yashiro-Ohtani, C. Del Bianco, D. M. Knoblock, S. C. Blacklow, andW. S. Pear. 2007. Notch directly regulates Gata3 expression during T helper 2 cell differentiation. Immunity 27: 100-110.
61. Tu, L., T. C. Fang, D. Artis, O. Shestova, S. E. Pross, I. Maillard, andW. S. Pear. 2005. Notch signaling is an important regulator of type 2 immunity. J. Exp. Med. 202: 1037-1042.
62. Caton, M. L., M. R. Smith-Raska, and B. Reizis. 2007. Notch-RBP-J signaling controls the homeostasis of CD8- dendritic cells in the spleen. J. Exp. Med. 204: 1653-1664.
63. Zhou, J., P. Cheng, J. I. Youn, M. J. Cotter, and D. I. Gabrilovich. 2009. Notch and wingless signaling cooperate in regulation of dendritic cell differentiation. Immunity 30: 845-859.
64. Hertzog, P. 2008. A notch in the toll belt. Immunity 29: 663-665.
65. Gu, L., S. Tseng, R. M. Horner, C. Tam, M. Loda, and B. J. Rollins. 2000. Control of TH2 polarization by the chemokine monocyte chemoattractant protein-1. Nature 404: 407-411.
66. Urbonaviciute, V., B. G. Fürnrohr, S. Meister, L. Munoz, P. Heyder, F. De Marchis, M. E. Bianchi, C. Kirschning, H. Wagner, A. A. Manfredi, et al. 2008. Induction of inflammatory and immune responses by HMGB1-nucleosome complexes: implications for the pathogenesis of SLE. J. Exp. Med. 205: 3007-3018.
67. Tesch, G. H., S. Maifert, A. Schwarting, B. J. Rollins, andV. R. Kelley. 1999. Monocyte chemoattractant protein 1-dependent leukocytic infiltrates are responsible for autoimmune disease in MRL-Fas(lpr) mice. J. Exp. Med. 190: 1813-1824.
68. Shin, H. M., L. M. Minter, O. H. Cho, S. Gottipati, A. H. Fauq, T. E. Golde, G. E. Sonenshein, and B. A. Osborne. 2006. Notch1 augments NF-kappaB activity by facilitating its nuclear retention. EMBO J. 25: 129-138.
69. Schiffer, L., J. Sinha, X. Wang, W. Huang, G. von Gersdorff, M. Schiffer, M. P. Madaio, A. Davidson, and G. Von Gonsdorff. 2003. Short term administration of costimulatory blockade and cyclophosphamide induces remission of systemic lupus erythematosus nephritis in NZB/W F1 mice by a mechanism downstream of renal immune complex deposition. [Published erratum in 2003 J. Immunol. 171: 1610.] J. Immunol. 171: 489-497. (Pubitemid 36745324)
70. Triantafyllopoulou, A., C. W. Franzke, S. V. Seshan, G. Perino, G. D. Kalliolias, M. Ramanujam, N. van Rooijen, A. Davidson, and L. B. Ivashkiv. 2010. Proliferative lesions and metalloproteinase activity in murine lupus nephritis mediated by type I interferons and macrophages. Proc. Natl. Acad. Sci. U.S.A. 107: 3012-3017.