AIM2 facilitates the apoptotic DNA-induced systemic lupus erythematosus via arbitrating macrophage functional maturation

Journal of Clinical Immunology

Volumn 33, Issue 5, 2013, Pages 925-937

  Zhang, Weijuan ^a   Cai, Yanxing ^a   Xu, Wei ^b   Yin, Zhinan ^c   Gao, Xiaoming ^b   Xiong, Sidong ^a,b  

^a FUDAN UNIVERSITY   (China)

^b SOOCHOW UNIVERSITY   (China)

^c NANKAI UNIVERSITY   (China)

Author keywords

AIM2; DNA sensor; inflammation; lupus nephritis; macrophage activation; SLE

Indexed keywords

ABSENT IN MELANOMA 2 PROTEIN; APOPTOTIC DNA; CELL RECEPTOR; CYTOPLASM PROTEIN; DNA; INFLAMMASOME; SMALL INTERFERING RNA; UNCLASSIFIED DRUG;

ADOLESCENT; ADULT; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL MATURATION; CLINICAL ARTICLE; CONTROLLED STUDY; DISEASE COURSE; DISEASE SEVERITY; FEMALE; HUMAN; HUMAN CELL; IMMUNOPATHOGENESIS; IMMUNOSENSOR; IN VITRO STUDY; IN VIVO STUDY; INFLAMMATION; MACROPHAGE ACTIVATION; MACROPHAGE FUNCTION; MALE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; SYSTEMIC LUPUS ERYTHEMATOSUS;

ADOLESCENT; ADULT; ANIMALS; ANTIBODIES, ANTINUCLEAR; APOPTOSIS; CELLS, CULTURED; DNA; FEMALE; HUMANS; INFLAMMASOMES; LUPUS ERYTHEMATOSUS, SYSTEMIC; LUPUS NEPHRITIS; MACROPHAGE ACTIVATION; MACROPHAGES; MALE; MELANOMA; MICE; MICE, INBRED BALB C; MIDDLE AGED; NEGOTIATING; NUCLEAR PROTEINS; RECEPTORS, CELL SURFACE; YOUNG ADULT;

EID: 84879205728     PISSN: 02719142     EISSN: 15732592     Source Type: Journal    
DOI: 10.1007/s10875-013-9881-6     Document Type: Article

References (53)

1. Murray PJ, Wynn TA. Protective and pathogenic functions of macrophage subsets. Nat Rev Immunol. 2011;11(11):723-37.
2. Triantafyllopoulou A, Franzke CW, Seshan SV, Perino G, Kalliolias GD, Ramanujam M, et al. Proliferative lesions and metalloproteinase activity in murine lupus nephritis mediated by type I interferons and macrophages. Proc Natl Acad Sci USA. 2010;107(7):3012-7.
3. Schiffer L, Bethunaickan R, Ramanujam M, Huang W, Schiffer M, Tao H, et al. Activated renal macrophages are markers of disease onset and disease remission in lupus nephritis. J Immunol. 2008;180(3):1938-47.
4. Bethunaickan R, Berthier CC, Ramanujam M, Sahu R, Zhang W, Sun Y, et al. A unique hybrid renal mononuclear phagocyte activation phenotype in murine systemic lupus erythematosus nephritis. J Immunol. 2011;186(8):4994-5003.
5. Wada T, Yokoyama H, Su SB, Mukaida N, Iwano M, Dohi K, et al. Monitoring urinary levels of monocyte chemotactic and activating factor reflects disease activity of lupus nephritis. Kidney Int. 1996;49(3):761-7.
6. Hill GS, Delahousse M, Nochy D, Remy P, Mignon F, Mery JP, et al. Predictive power of the second renal biopsy in lupus nephritis: significance of macrophages. Kidney Int. 2001;59(1):304-16.
7. Sean Eardley K, Cockwell P. Macrophages and progressive tubulointerstitial disease. Kidney Int. 2005;68(2):437-55.
8. Qiao B, Wu J, Chu YW, Wang Y, Wang DP, Wu HS, et al. Induction of systemic lupus erythematosus-like syndrome in syngeneic mice by immunization with activated lymphocyte-derived DNA. Rheumatology (Oxford). 2005;44(9):1108-14.
9. Wen ZK, Xu W, Xu L, Cao QH, Wang Y, Chu YW, et al. DNA hypomethylation is crucial for apoptotic DNA to induce systemic lupus erythematosus-like autoimmune disease in SLE-non-susceptible mice. Rheumatology (Oxford). 2007;46(12):1796-803.
10. Zhang W, Xu W, Xiong S. Blockade of Notch1 signaling alleviates murine lupus via blunting macrophage activation and M2b polarization. J Immunol. 2010;184(11):6465-78.
11. Zhang W, Xu W, Xiong S. Macrophage differentiation and polarization via phosphatidylinositol 3-Kinase/Akt-ERK signaling pathway conferred by serum amyloid P component. J Immunol. 2011;187(4):1764-77.
12. Evans CJ, Aguilera RJ. DNase II: genes, enzymes and function. Gene. 2003;322:1-15.
13. Yoshida H, Kawane K, Koike M, Mori Y, Uchiyama Y, Nagata S. Phosphatidylserine-dependent engulfment by macrophages of nuclei from erythroid precursor cells. Nature. 2005;437(7059):754-8.
14. Yoshida H, Okabe Y, Kawane K, Fukuyama H, Nagata S. Lethal anemia caused by interferon-beta produced in mouse embryos carrying undigested DNA. Nat Immunol. 2005;6(1):49-56.
15. Okabe Y, Kawane K, Akira S, Taniguchi T, Nagata S. Toll-like receptor-independent gene induction program activated by mammalian DNA escaped from apoptotic DNA degradation. J Exp Med. 2005;202(10):1333-9.
16. Barbalat R, Ewald SE, Mouchess ML, Barton GM. Nucleic Acid recognition by the innate immune system. Annu Rev Immunol. 2011;29:185-214.
17. Hornung V, Latz E. Intracellular DNA recognition. Nat Rev Immunol. 2010;10(2):123-30.
18. Kahlenberg JM, Thacker SG, Berthier CC, Cohen CD, Kretzler M, Kaplan MJ. Inflammasome activation of IL-18 results in endothelial progenitor cell dysfunction in systemic lupus erythematosus. J Immunol. 2011;187(11):6143-56.
19. Hornung V, Ablasser A, Charrel-Dennis M, Bauernfeind F, Horvath G, Caffrey DR, et al. AIM2 recognizes cytosolic dsDNA and forms a caspase-1-activating inflammasome with ASC. Nature. 2009;458(7237):514-8.
20. Roberts TL, Idris A, Dunn JA, Kelly GM, Burnton CM, Hodgson S, et al. HIN-200 proteins regulate caspase activation in response to foreign cytoplasmic DNA. Science. 2009;323(5917):1057-60.
21. Fernandes-Alnemri T, Yu JW, Datta P, Wu J, Alnemri ES. AIM2 activates the inflammasome and cell death in response to cytoplasmic DNA. Nature. 2009;458(7237):509-13.
22. Panchanathan R, Duan X, Arumugam M, Shen H, Liu H, Choubey D. Cell type and gender-dependent differential regulation of the p202 and Aim2 proteins: implications for the regulation of innate immune responses in SLE. Mol Immunol. 2011;49(1-2):273-80.
23. Choubey D. DNA-responsive inflammasomes and their regulators in autoimmunity. Clin Immunol. 2012;142(3):223-31.
24. Li K, Xu W, Guo Q, Jiang Z, Wang P, Yue Y, et al. Differential macrophage polarization in male and female BALB/c mice infected with coxsackievirus B3 defines susceptibility to viral myocarditis. Circ Res. 2009;105(4):353-64.
25. Ito T, Schaller M, Hogaboam CM, Standiford TJ, Sandor M, Lukacs NW, et al. TLR9 regulates the mycobacteria-elicited pulmonary granulomatous immune response in mice through DC-derived Notch ligand delta-like 4. J Clin Invest. 2009;119(1):33-46.
26. Zhang W, Cai Y, Xu W, Xiong S. C-reactive protein functions as a negative regulator of macrophage activation induced by apoptotic DNA. Protein Cell. 2011;2(8):672-9.
27. Xu J, Yun X, Jiang J, Wei Y, Wu Y, Zhang W, et al. Hepatitis B virus X protein blunts senescence-like growth arrest of human hepatocellular carcinoma by reducing Notch1 cleavage. Hepatology. 2010;52(1):142-54.
28. Liu H, Xu J, Zhou L, Yun X, Chen L, Wang S, et al. Hepatitis B virus large surface antigen promotes liver carcinogenesis by activating the Src/PI3K/Akt pathway. Cancer Res. 2011;71:7547-57.
29. Xu J, Liu H, Chen L, Wang S, Zhou L, Yun X, et al. Hepatitis B virus X protein confers resistance of hepatoma cells to anoikis by up-regulating and activating p21-activated kinase 1. Gastroenterology. 2012;143(1):199-212.
30. Chen M, Zhang W, Xu W, Zhang F, Xiong S. Blockade of TLR9 signaling in B cells impaired anti-dsDNA antibody production in mice induced by activated syngenic lymphocyte-derived DNA immunization. Mol Immunol. 2011;48(12-13):1532- 9.
31. Zhang W, Wu J, Qiao B, Xu W, Xiong S. Amelioration of lupus nephritis by serum amyloid p component gene therapy with distinct mechanisms varied from different stage of the disease. PLoS One. 2011;6(7):e22659.
32. Hale MB, Krutzik PO, Samra SS, Crane JM, Nolan GP. Stage dependent aberrant regulation of cytokine-STAT signaling in murine systemic lupus erythematosus. PLoS One. 2009;4(8):e6756.
33. Casciola-Rosen LA, Anhalt G, Rosen A. Autoantigens targeted in systemic lupus erythematosus are clustered in two populations of surface structures on apoptotic keratinocytes. J Exp Med. 1994;179(4):1317-30.
34. Mevorach D, Zhou JL, Song X, Elkon KB. Systemic exposure to irradiated apoptotic cells induces autoantibody production. J Exp Med. 1998;188(2):387-92.
35. Rahman A, Isenberg DA. Systemic lupus erythematosus. N Engl J Med. 2008;358(9):929-39.
36. Papatriantafyllou M. Macrophages: support from the locals. Nat Rev Immunol. 2011;11(7):442.
37. Shi C, Pamer EG. Monocyte recruitment during infection and inflammation. Nat Rev Immunol. 2011;11(11):762-74.
38. Hemmi H, Takeuchi O, Kawai T, Kaisho T, Sato S, Sanjo H, et al. A Toll-like receptor recognizes bacterial DNA. Nature. 2000;408(6813):740-5.
39. Takaoka A, Wang Z, Choi MK, Yanai H, Negishi H, Ban T, et al. DAI (DLM-1/ZBP1) is a cytosolic DNA sensor and an activator of innate immune response. Nature. 2007;448(7152):501-5.
40. Chiu YH, Macmillan JB, Chen ZJ. RNA polymerase III detects cytosolic DNA and induces type I interferons through the RIG-I pathway. Cell. 2009;138(3):576-91.
41. Ablasser A, Bauernfeind F, Hartmann G, Latz E, Fitzgerald KA, Hornung V. RIG-I-dependent sensing of poly(dA:dT) through the induction of an RNA polymerase III-transcribed RNA intermediate. Nat Immunol. 2009;10(10):1065-72.
42. Unterholzner L, Keating SE, Baran M, Horan KA, Jensen SB, Sharma S, et al. IFI16 is an innate immune sensor for intracellular DNA. Nat Immunol. 2010;11(11):997-1004.
43. Yang P, An H, Liu X, Wen M, Zheng Y, Rui Y, et al. The cytosolic nucleic acid sensor LRRFIP1 mediates the production of type I interferon via a beta-catenin-dependent pathway. Nat Immunol. 2010;11(6):487-94.
44. Zhang Z, Yuan B, Bao M, Lu N, Kim T, Liu YJ. The helicase DDX41 senses intracellular DNA mediated by the adaptor STING in dendritic cells. Nat Immunol. 2011;12(10):959-65.
45. Yanai H, Ban T, Wang Z, Choi MK, Kawamura T, Negishi H, et al. HMGB proteins function as universal sentinels for nucleic-acid-mediated innate immune responses. Nature. 2009;462(7269):99-103.
46. Keating SE, Baran M, Bowie AG. Cytosolic DNA sensors regulating type I interferon induction. Trends Immunol. 2011;32(12):574-81.
47. Kimkong I, Avihingsanon Y, Hirankarn N. Expression profile of HIN200 in leukocytes and renal biopsy of SLE patients by real-time RT-PCR. Lupus. 2009;18(12):1066-72.
48. Panchanathan R, Duan X, Shen H, Rathinam VA, Erickson LD, Fitzgerald KA, et al. Aim2 deficiency stimulates the expression of IFN-inducible Ifi202, a lupus susceptibility murine gene within the Nba2 autoimmune susceptibility locus. J Immunol. 2010;185(12):7385-93.
49. Panchanathan R, Shen H, Bupp MG, Gould KA, Choubey D. Female and male sex hormones differentially regulate expression of Ifi202, an interferon-inducible lupus susceptibility gene within the Nba2 interval. J Immunol. 2009;183(11):7031-8.
50. Panchanathan R, Shen H, Duan X, Rathinam VA, Erickson LD, Fitzgerald KA, et al. Aim2 deficiency in mice suppresses the expression of the inhibitory Fcgamma receptor (FcgammaRIIB) through the induction of the IFN-inducible p202, a lupus susceptibility protein. J Immunol. 2011;186(12):6762-70.
51. Jorgensen TN, Alfaro J, Enriquez HL, Jiang C, Loo WM, Atencio S, et al. Development of murine lupus involves the combined genetic contribution of the SLAM and FcgammaR intervals within the Nba2 autoimmune susceptibility locus. J Immunol. 2010;184(2):775-86.
52. Choubey D, Panchanathan R, Shen H, Duan X. Comment on "Development of murine lupus involves the combined genetic contribution of the SLAM and Fc gamma R intervals within the Nba2 autoimmune susceptibility locus". J Immunol. 2010;184(8):4051-2. author reply 2.
53. Choubey D, Panchanathan R, Duan X, Liu H. Emerging roles for the interferon-inducible p200-family proteins in sex bias in systemic lupus erythematosus. J Interferon Cytokine Res. 2011;31(12):893-906.