MAPK phosphatase-1 is required for regulatory natural autoantibody-mediated inhibition of TLR responses

Proceedings of the National Academy of Sciences of the United States of America

Volumn 109, Issue 48, 2012, Pages 19745-19750

  Grönwall, Caroline ^a,b   Chen, Yifang ^b   Vas, Jaya ^a,b   Khanna, Sahil ^b   Thiel, Steffen ^c   Corr, Maripat ^b   Kono, Dwight H ^d   Silverman, Gregg J ^a,b  

^a NEW YORK UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF CALIFORNIA SAN DIEGO   (United States)

^c AARHUS UNIVERSITY   (Denmark)

^d SCRIPPS RESEARCH INSTITUTE   (United States)

Author keywords

Apoptotic cell; Autoimmunity; Dusp 1; Inflammation; MBL

Indexed keywords

COMPLEMENT COMPONENT C1Q; COMPLEMENT FACTOR; IMMUNOGLOBULIN G; IMMUNOGLOBULIN M ANTIBODY; MANNOSE BINDING LECTIN; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; MITOGEN ACTIVATED PROTEIN KINASE P38; MITOGEN ACTIVATED PROTEIN KINASE PHOSPHATASE 1; STRESS ACTIVATED PROTEIN KINASE; TOLL LIKE RECEPTOR; TOLL LIKE RECEPTOR AGONIST;

ADAPTIVE IMMUNITY; ANIMAL CELL; ANTIGEN RECOGNITION; APOPTOSIS; ARTICLE; BONE MARROW CELL; DENDRITIC CELL; INNATE IMMUNITY; MOUSE; NONHUMAN; NUCLEAR LOCALIZATION SIGNAL; PRIORITY JOURNAL; PROTEIN EXPRESSION; UPREGULATION;

ANIMALS; AUTOANTIBODIES; DUAL SPECIFICITY PHOSPHATASE 1; IMMUNOGLOBULIN M; MICE; MICE, INBRED C57BL; TOLL-LIKE RECEPTORS; UP-REGULATION;

EID: 84870327137     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1211868109     Document Type: Article

References (46)

1. Ehrenstein MR, Notley CA (2010) The importance of natural IgM: Scavenger, protector and regulator. Nat Rev Immunol 10(11):778-786.
2. Chou MY, et al. (2009) Oxidation-specific epitopes are dominant targets of innate natural antibodies in mice and humans. J Clin Invest 119(5):1335-1349.
3. Baumgarth N, Tung JW, Herzenberg LA (2005) Inherent specificities in natural antibodies: A key to immune defense against pathogen invasion. Springer Semin Immunopathol 26(4):347-362.
4. Cancro MP, Sigal NH, Klinman NR (1978) Differential expression of an equivalent clonotype among BALB/c and C57BL/6 mice. J Exp Med 147(1):1-12.
5. Satow Y, Cohen GH, Padlan EA, Davies DR (1986) Phosphocholine binding immunoglobulin Fab McPC603: An X-ray diffraction study at 2.7 A. J Mol Biol 190(4):593-604.
6. Binder CJ, Silverman GJ (2005) Natural antibodies and the autoimmunity of atherosclerosis. Springer Semin Immunopathol 26(4):385-404.
7. Shaw PX, Goodyear CS, Chang MK, Witztum JL, Silverman GJ (2003) The autoreactivity of anti-phosphorylcholine antibodies for atherosclerosis- associated neo-antigens and apoptotic cells. J Immunol 170(12):6151-6157.
8. Silverman GJ (2011) Regulatory natural autoantibodies to apoptotic cells: Pallbearers and protectors. Arthritis Rheum 63(3):597-602.
9. Chen Y, Park YB, Patel E, Silverman GJ (2009) IgM antibodies to apoptosis-associated determinants recruit C1q and enhance dendritic cell phagocytosis of apoptotic cells. J Immunol 182(10):6031-6043.
10. Ogden CA, Kowalewski R, Peng Y, Montenegro V, Elkon KB (2005) IGM is required for efficient complement mediated phagocytosis of apoptotic cells in vivo. Autoimmunity 38(4):259-264.
11. Quartier P, Potter PK, Ehrenstein MR, Walport MJ, Botto M (2005) Predominant role of IgM-dependent activation of the classical pathway in the clearance of dying cells by murine bone marrow-derived macrophages in vitro. Eur J Immunol 35(1):252-260.
12. Chen Y, et al. (2009) Regulation of dendritic cells and macrophages by an anti-apoptotic cell natural antibody that suppresses TLR responses and inhibits inflammatory arthritis. J Immunol 183(2):1346-1359.
13. Steinman RM, Hawiger D, Nussenzweig MC (2003) Tolerogenic dendritic cells. Annu Rev Immunol 21:685-711.
14. Kim S, Elkon KB, Ma X (2004) Transcriptional suppression of interleukin-12 gene expression following phagocytosis of apoptotic cells. Immunity 21(5):643-653.
15. Baccala R, et al. (2009) Sensors of the innate immune system: Their mode of action. Nat Rev Rheumatol 5(8):448-456.
16. Vas J, Grönwall C, Marshak-Rothstein A, Silverman GJ (2012) Natural antibody to apoptotic cell membranes inhibits the proinflammatory properties of lupus autoantibody immune complexes. Arthritis Rheum 64(10):3388-3398.
17. Liu Y, Shepherd EG, Nelin LD (2007) MAPK phosphatases: Regulating the immune response. Nat Rev Immunol 7(3):202-212.
18. Sun H, Charles CH, Lau LF, Tonks NK (1993) MKP-1 (3CH134), an immediate early gene product, is a dual specificity phosphatase that dephosphorylates MAP kinase in vivo. Cell 75(3):487-493.
19. Chen P, et al. (2002) Restraint of proinflammatory cytokine biosynthesis by mitogenactivated protein kinase phosphatase-1 in lipopolysaccharide- stimulated macrophages. J Immunol 169(11):6408-6416.
20. Hu JH, et al. (2007) Feedback control of MKP-1 expression by p38. Cell Signal 19(2): 393-400.
21. Bohlson SS, Fraser DA, Tenner AJ (2007) Complement proteins C1q and MBL are pattern recognition molecules that signal immediate and long-term protective immune functions. Mol Immunol 44(1-3):33-43.
22. Reiser V, Ammerer G, Ruis H (1999) Nucleocytoplasmic traffic of MAP kinases. Gene Expr 7(4-6):247-254.
23. Lasa M, Abraham SM, Boucheron C, Saklatvala J, Clark AR (2002) Dexamethasone causes sustained expression of mitogen-activated protein kinase (MAPK) phosphatase 1 and phosphatase-mediated inhibition of MAPK p38. Mol Cell Biol 22(22):7802-7811.
24. Sigal NH, Pickard AR, Metcalf ES, Gearhart PJ, Klinman NR (1977) Expression of phosphorylcholine- specific B cells during murine development. J Exp Med 146(4):933-948.
25. Dorfman K, et al. (1996) Disruption of the erp/mkp-1 gene does not affect mouse development: normal MAP kinase activity in ERP/MKP-1-deficient fibroblasts. Oncogene 13(5):925-931.
26. Salojin KV, et al. (2006) Essential role of MAPK phosphatase-1 in the negative control of innate immune responses. J Immunol 176(3):1899-1907.
27. Maier JV, et al. (2007) Dual specificity phosphatase 1 knockout mice show enhanced susceptibility to anaphylaxis but are sensitive to glucocorticoids. Mol Endocrinol 21 (11):2663-2671.
28. Kuwano Y, et al. (2008) MKP-1 mRNA stabilization and translational control by RNAbinding proteins HuR and NF90. Mol Cell Biol 28(14):4562-4575.
29. Brondello JM, Pouysségur J, McKenzie FR (1999) Reduced MAP kinase phosphatase-1 degradation after p42/p44MAPK-dependent phosphorylation. Science 286(5449): 2514-2517.
30. CaoW, Bao C, Padalko E, Lowenstein CJ (2008) Acetylation of mitogen-activated protein kinase phosphatase-1 inhibits Toll-like receptor signaling. J ExpMed 205(6):1491-1503.
31. Lemaitre B, Nicolas E, Michaut L, Reichhart JM, Hoffmann JA (1996) The dorsoventral regulatory gene cassette spätzle/Toll/cactus controls the potent antifungal response in Drosophila adults. Cell 86(6):973-983.
32. Asai T, et al. (2002) MAP kinase signalling cascade in Arabidopsis innate immunity. Nature 415(6875):977-983.
33. Moncho-Amor V, Galardi-Castilla M, Perona R, Sastre L (2011) The dual-specificity protein phosphatase MkpB, homologous to mammalian MKP phosphatases, is required for D. discoideum post-aggregative development and cisplatin response. Differentiation 81(3):199-207.
34. Zhao Q, et al. (2006) MAP kinase phosphatase 1 controls innate immune responses and suppresses endotoxic shock. J Exp Med 203(1):131-140.
35. Arnold JN, Dwek RA, Rudd PM, Sim RB (2006) Mannan binding lectin and its interaction with immunoglobulins in health and in disease. Immunol Lett 106(2):103-110.
36. Boes M, et al. (2000) Accelerated development of IgG autoantibodies and autoimmune disease in the absence of secreted IgM. Proc Natl Acad Sci USA 97(3):1184-1189.
37. Botto M, et al. (1998) Homozygous C1q deficiency causes glomerulonephritis associated with multiple apoptotic bodies. Nat Genet 19(1):56-59.
38. Ehrenstein MR, O'Keefe TL, Davies SL, Neuberger MS (1998) Targeted gene disruption reveals a role for natural secretory IgM in the maturation of the primary immune response. Proc Natl Acad Sci USA 95(17):10089-10093.
39. Stuart LM, Takahashi K, Shi L, Savill J, Ezekowitz RA (2005) Mannose-binding lectindeficient mice display defective apoptotic cell clearance but no autoimmune phenotype. J Immunol 174(6):3220-3226.
40. Matsushita M, et al. (2004) Origin of the classical complement pathway: Lamprey orthologue of mammalian C1q acts as a lectin. Proc Natl Acad Sci USA 101(27):10127-10131.
41. Ogden CA, et al. (2001) C1q and mannose binding lectin engagement of cell surface calreticulin and CD91 initiates macropinocytosis and uptake of apoptotic cells. J Exp Med 194(6):781-795.
42. Shaw PX, et al. (2000) Natural antibodies with the T15 idiotype may act in atherosclerosis, apoptotic clearance, and protective immunity. J Clin Invest 105(12):1731-1740.
43. Binder CJ, et al. (2003) Pneumococcal vaccination decreases atherosclerotic lesion formation: molecular mimicry between Streptococcus pneumoniae and oxidized LDL. Nat Med 9(6):736-743.
44. Grönwall C, et al. (2012) IgM autoantibodies to distinct apoptosis-associated antigens correlate with protection from cardiovascular events and renal disease in patients with SLE. Clin Immunol 142(3):390-398.
45. Su J, et al. (2008) Natural antibodies against phosphorylcholine as potential protective factors in SLE. Rheumatology (Oxford) 47(8):1144-1150.
46. Griffin DO, Holodick NE, Rothstein TL (2011) Human B1 cells in umbilical cord and adult peripheral blood express the novel phenotype CD20+ CD27+ CD43+ CD70-.J Exp Med 208(1):67-80.