The origin and properties of extracellular DNA: From PAMP to DAMP

Clinical Immunology

Volumn 144, Issue 1, 2012, Pages 32-40

  Pisetsky, David S ^a,b  

^a DURHAM VA MEDICAL CENTER   (United States)

^b DUKE UNIVERSITY MEDICAL CENTER   (United States)

Author keywords

Anti DNA; Apoptosis; DNA; HMGB1; Immune complexes; Systemic lupus erythematosus

Indexed keywords

BACTERIAL DNA; CELL DNA; CELL NUCLEUS DNA; DNA; DNA ANTIBODY; EXTRACELLULAR DNA; EXTRACHROMOSOMAL DNA; HIGH MOBILITY GROUP B1 PROTEIN; INTERFERON; TOLL LIKE RECEPTOR 9; UNCLASSIFIED DRUG;

ANTIGEN ANTIBODY COMPLEX; APOPTOSIS; CELLULAR DISTRIBUTION; CPG ISLAND; CYTOKINE PRODUCTION; DNA STRUCTURE; HUMAN; IMMUNOSTIMULATION; INJURY; LUNG INFARCTION; MALIGNANT NEOPLASTIC DISEASE; NONHUMAN; NUCLEOSOME; PLASMACYTOID DENDRITIC CELL; PREGNANCY; PRIORITY JOURNAL; REVIEW; SEPSIS; SYSTEMIC LUPUS ERYTHEMATOSUS; TOXIC HEPATITIS;

ANIMALS; DNA; HMGB1 PROTEIN; HUMANS;

EID: 84861558147     PISSN: 15216616     EISSN: 15217035     Source Type: Journal    
DOI: 10.1016/j.clim.2012.04.006     Document Type: Review

References (88)

1. Pisetsky D.S. Immune activation by bacterial DNA: a new genetic code. Immunity 1996, 5:303-310.
2. Griffith T.S., Ferguson T.A. Cell death in the maintenance and abrogation of tolerance: the five Ws of dying cells. Immunity 2011, 35:456-466.
3. Hansen J.D., Vojtech L.N., Laing K.J. Sensing disease and danger: a survey of vertebrate PRRs and their origins. Dev. Comp. Immunol. 2011, 35:886-897.
4. Kawasaki T., Kawai T., Akira S. Recognition of nucleic acids by pattern-recognition receptors and its relevance in autoimmunity. Immunol. Rev. 2011, 243:61-73.
5. Ranjin P., Bowzard J.B., Schwerzmann J.W., Jeisy-Scott V., Fujita T., Sambhara S. Cytoplasmic nucleic acid sensors in antiviral immunity. Trends Mol. Med. 2009, 15:359-368.
6. Theofilopoulos A.N., Kono D.H., Beutler B., Baccala R. Intracellular nucleic acid sensors and autoimmunity. J. Interferon Cytokine Res. 2011, 31:867-886.
7. Brinkmann V., Zychlinsky A. Beneficial suicide: why neutrophils die to make NETs. Nat. Rev. Microbiol. 2007, 5:577-582.
8. Fuchs T.A., Abed U., Goosmann C., Hurwitz R., Schulze I., Wahn V., Weinrauch Y., Brinkmann V., Zyclinsky A. Novel cell death program leads to neutrophil extracellular traps. J. Cell Biol. 2007, 176:231-241.
9. Papayannopoulos V., Metzler K.D., Hakkim A., Zychlinsky A. Neutrophil elastase and myeloperoxidase regulate the formation of neutrophil extracellular traps. J. Cell Biol. 2010, 191:677-691.
10. Khorasanizadeh S. The nucleosome: from genomic organization to genomic regulation. Cell 2004, 116:259-272.
11. Brown D.G., Sun X.-M., Cohen G.M. Dexamethasone-induced apoptosis involves cleavage of DNA to large fragments prior to internucleosomal fragmentation. J. Biol. Chem. 1993, 268:3037-3039.
12. Enari M., Sakahira H., Yokoyama H., Okawa K., Iwamatsu A., Nagata S. A caspase-activated DNase that degrades DNA during apoptosis, and its inhibitor ICAD. Nature 1998, 391:43-50.
13. Nagata S. Apoptotic DNA fragmentation. Exp. Cell Res. 2000, 256:12-18.
14. Samejima K., Earnshaw W.C. Trashing the genome: the role of nucleases during apoptosis. Nat. Rev. Mol. Cell Biol. 2005, 6:677-688.
15. Napirei M., Karsunky H., Zevnik B., Stephean H., Mannherz H.G., Möröy T. Features of systemic lupus erythematosus in Dnase1-deficient mice. Nat. Genet. 2000, 25:177-181.
16. Zykova S.N., Tveita A.A., Rekvig O.P. Renal Dnase1 enzyme activity and protein expression is selectively shut down in murine and human membranoproliferative lupus nephritis. PLoS One 2010, 10:e12096.
17. Jog N.R., Frisoni L., Monestier M., Hernandez S., Craft J., Prak E.T., Caricchio R. Caspase-activated Dnase is required for maintenance of tolerance to lupus nuclear autoantigens. Arthritis Rheum. 2012, 64:1247-1256.
18. Jahr S., Hentze H., Englisch S., Hardt D., Fackelmayer F.O., Hesch R.-D., Knippers R. DNA fragments in the blood plasma of cancer patients: quantitations and evidence for their origin from apoptotic and necrotic cells. Cancer Res. 2001, 61:1659-1665.
19. Björkman L., Reich C.F., Pisetsky D.S. The use of fluorometric assays to assess the immune response to DNA in murine systemic lupus erythematosus. Scand. J. Immunol. 2003, 57:525-533.
20. Holdenrieder S., Stieber P., Chan L.Y.S., Geiger S., Kremer A., Nagel D., Dennis Lo Y.M. Cell-free DNA in serum and plasma: comparison of ELISA and quantitative PCR. Clin. Chem. 2005, 1544-1546.
21. Jung K., Fleischhacker M., Rabien A. Cell-free DNA in the blood as a solid tumor-biomarker-a critical appraisal of the literature. Clin. Chim. Acta 2010, 411:1611-1624.
22. Holdenrieder S., Stieber P. Clinical use of circulating nucleosomes. Crit. Rev. Clin. Lab. Sci. 2009, 46:1-24.
23. Moussion C., Ortega N., Girard J.P. The IL-1-like cytokine IL-33 is constitutively expressed in the nucleus of endothelial cells and epithelial cells in vivo: a novel 'alarmin'?. PLoS One 2008, 6:e3331.
24. Cohen I., Rider P., Carmi Y., Braiman A., Dotan S., White M.R., Voronov E., Martin M.U., Dinarello C.A., Apte R.N. Differential release of chromatin-bound IL-1a discriminates between necrotic and apoptotic cell death by the ability to induce sterile inflammation. Proc. Natl. Acad. Sci. U. S. A. 2010, 107:2574-2579.
25. Hahn B.H. Antibodies to DNA. N. Engl. J. Med. 1998, 338:1359-1368.
26. Jang Y.J., Stollar B.D. Anti-DNA antibodies: aspects of structure and pathogenicity. Cell. Mol. Life Sci. 2003, 60:309-320.
27. Lui Y.Y.N., Lo Y.M.D. Circulating DNA in plasma and serum: biology, preanalytical issues and diagnostic applications. Clin. Chem. Lab. Med. 2002, 40:962-968.
28. Lam N.Y.L., Rainer T.H., Chan L.Y.S., Joynt G.J., Lo Y.M.D. Time course of early and late changes in plasma DNA in trauma patients. Clin. Chem. 2003, 49:1286-1291.
29. Wang B.G., Huang H.-Y., Chen Y.-C., Bristow R.E., Kassauei K., Cheng C.-C., Roden R., Sokill L.J., Chan D.W., Shih I.-M. Increased plasma DNA integrity in cancer patients. Cancer Res. 2003, 63:3966-3968.
30. Choi J.J., Reich C.F., Pisetsky D.S. Release of DNA from dead and dying lymphocyte and monocyte cell lines in vitro. Scand. J. Immunol. 2004, 60:159-166.
31. Choi J.J., Reich C.F., Pisetsky D.S. The role of macrophages in the in vitro generation of extracellular DNA from apoptotic and necrotic cells. Immunology 2005, 115:55-62.
32. Beyer C., Stearns N.A., Giessl A., Distler J.H., Schett G., Pisetsky D. The extracellular release of DNA and HMGB1 from Jurkat T cells during in vitro necrotic cell death. Innate Immun. Feb. 16 2012, [Epub ahead of print].
33. Jiang N., Reich C.F., Monestier M., Pisetsky D.S. The expression of plasma nucleosomes in mice undergoing in vivo apoptosis. Clin. Immunol. 2003, 106:139-147.
34. Jiang N., Reich C.F., Pisetsky D.S. Role of macrophages in the generation of circulating blood nucleosomes from dead and dying cells. Blood 2003, 102:2243-2250.
35. Pisetsky D.S., Jiang N. The generation of extracellular DNA in SLE: the role of death and sex. Scand. J. Immunol. 2006, 64:200-204.
36. Tran T.T., Groben P., Pisetsky D.S. The release of DNA into the plasma of mice following hepatic cell death by apoptosis and necrosis. Biomarkers 2008, 13:184-200.
37. Fourmé G.J., Lambert P.H., Meischer P.A. Release of DNA in circulating blood and induction of anti-DNA antibodies after injection of bacterial lipopolysaccharides. J. Exp. Med. 1974, 140:1189-1206.
38. Licht R., vanBruggen M.C., Oppers-Walgreen B., Rijke T.P., Berden J.H. Plasma levels of nucleosomes and nucleosome-autoantibody complexes in murine lupus: effects of disease progression and lipopolysaccharide administration. Arthritis Rheum. 2001, 44:1320-1330.
39. Xu J., Zhang X., Pelayo R., Monestier M., Ammollo C.T., Semararo F., Taylor F.B., Esmon N.L., Lupu F., Esmon C.T. Extracellular histones are major mediators of death in sepsis. Nat. Med. 2009, 15:1318-1322.
40. Harris H.E., Andersson U., Pisetsky D.S. HMGB1: a multifunctional alarmin driving autoimmune and inflammatory disease. Nat. Rev. Rheumatol. 2012, [Epub ahead of print]. 10.1038/nrrheum.2011.222.
41. Casciola-Rosen L.A., 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, 179:1317-1330.
42. Schiller M., Bekeredian-Ding I., Heyder P., Ho A.D., Lorenz H.M. Autoantigens are translocated into small apoptotic bodies during early stages of apoptosis. Cell Death Differ. 2008, 15:183-191.
43. Reich C.F., Pisetsky D.S. The content of DNA and RNA in microparticles released by Jurkat and HL-60 cells undergoing in vitro apoptosis. Exp. Cell Res. 2009, 315:760-768.
44. Mause S.F., Weber C. Microparticles: protagonists of a novel communication network for intercellular information exchange. Circ. Res. 2010, 107:1047-1057.
45. Pisetsky D.S., Ullal A.J., Gauley J., Ning T.C. Microparticles as mediators and biomarkers of rheumatic disease. Rheumatology Mar. 7 2012, [E pub ahead of print].
46. Ullal A.J., Reich C.F., Clowse M., Criscione-Schreiber L.G., Tochacek M., Monestier M., Pisetsky D.S. Microparticles as antigenic targets of antibodies to DNA and nucleosomes in systemic lupus erythematosus. J. Autoimmun. 2011, 36:173-180.
47. Radic M.Z., Weigert M. Genetic and structural evidence for antigen selection of anti-DNA antibodies. Annu. Rev. Immunol. 1994, 12:487-520.
48. Guo W., Smith D., Aviszus K., Detanico T., Heiser R.A., Wysocki L.J. Somatic hypermutation as a generator of antinuclear antibodies in a murine model of systemic autoimmunity. J. Exp. Med. 2010, 207:2225-2237.
49. Krieg A.M. CpG motifs in bacterial DNA and their immune effects. Annu. Rev. Immunol. 2002, 20:709-760.
50. Berends E.T., Horswill A.R., haste N.M., Monestier M., Nizet V., von Köckritz-Blickwede M. Nuclease expression by Staphylococcus aureus facilitates escape from neutrophil extracellular traps. J. Innate Immun. 2010, 2:576-586.
51. Pisetsky D.S., Reich C.F. Inhibition of murine macrophage IL-12 production by natural and synthetic DNA. Clin. Immunol. 2000, 96:198-204.
52. Gursel I., Gursel M., Yamada H., Ishii K.J., Takeshita F., Klinman D.M. Repetitive elements in mammalian telomeres suppress bacterial DNA-induced immune activation. J. Immunol. 2003, 17:1393-1400.
53. Gilkeson G.S., Pippen A.M., Pisetsky D.S. Induction of cross-reactive anti-dsDNA antibodies in preautoimmune NZB/NZW mice by immunization with bacterial DNA. J. Clin. Invest. 1995, 95:1398-1402.
54. Hemmi H., Takeuchi O., Kawai T., Kaisho T., Sato S., Sanjo H., Matsumoto M., Hoshino K., Wagner H., Takeda K., Akira S. A toll-like receptor recognizes bacterial DNA. Nature 2000, 408:740-745.
55. Bauer S., Kirschning C.J., Häcker H., Redecke V., Hausmann S., Akira S., Wagner H., Lipford G.B. Human TLR9 confers responsiveness to bacterial DNA via species-specific CpG motif recognition. Proc. Natl. Acad. Sci. U. S. A. 2001, 98:9237-9242.
56. Rutz M., Metzger J., Gellert T., Luppa P., Lipford G.B., Wagner H., Bauer S. Toll-like receptor 9 binds single-stranded CpG-DNA in a sequence- and pH-dependent manner. Eur. J. Immunol. 2004, 34:2541-2550.
57. Akira S., Takeda K. Toll-like receptor signaling. Nat. Rev. Immunol. 2004, 4:499-511.
58. Lee S.J., Silverman E., Bargman J.M. The role of antimalarial agents in the treatment of SLE and lupus nephritis. Nat. Rev. Nephrol. 2011, 7:718-729.
59. Ben-Zvi I., Kivity S., Langevitz P., Shoenfeld Y. Hydroxychloroquine: from malaria to autoimmunity. Clin. Rev. Allergy Immunol. 2012, 42:145-153.
60. Pisetsky D.S., Reich C.F. Influence of backbone chemistry on immune activation by synthetic oligonucleotides. Biochem. Pharmacol. 1999, 58:1981-1988.
61. Klinman D., Shirota H., Tross D., Sato T., Klaschik S. Synthetic oligonucleotides as modulators of inflammation. J. Leukoc. Biol. 2008, 84:958-964.
62. Krieg A.M. CpG still rocks! Update on an accidental drug. Nucleic Acid. Ther. Feb. 21 2012, [Epub ahead of print].
63. Jiang W., Reich C.F., Pisetsky D.S. Mechanisms of activation of the RAW 264.7 macrophage cell line by transfected mammalian DNA. Cell. Immunol. 2004, 229:31-40.
64. Jiang W., Pisetsky D.S. The induction of HMGB1 release from RAW 264.7 cells by transfected DNA. Mol. Immunol. 2008, 45:2038-2044.
65. Choubey D. DNA-responsive inflammasomes and their regulators in autoimmunity. Clin. Immunol. 2012, 142:223-231.
66. Vallin H., Perers A., Alm G.V., Rönnblom L. Anti-double-stranded DNA antibodies and immunostimulatory plasmid DNA in combination mimic the endogenous IFN-α inducer in systemic lupus erythematosus. J. Immunol. 1999, 163:6306-6313.
67. Boulé M.W., Broughton C., Mackay F., Akira S., Marshak-Rothstein A., Rifkin I.R. Toll-like receptor 9-dependent and -independent dendritic cell activation by chromatin-immunoglobulin G complexes. J. Exp. Med. 2004, 199:1631-1640.
68. Tian J., Avalos A.M., Mao S.-Y., Chen B., Senthil K., Wu H., Parroche P., Drabic S., Golenbock D., Sirois C., Hua J., An L.L., Audoly L., LaRosa G., Bierhaus A., Naworth P., Marshak-Rothstein A., Crow M.K., Fitzgerald K.A., Latz E., Kiener P.A., Coyle A.J. Toll-like receptor 9-dependent activation by DNA-containing immune complexes is mediated by HMGB1 and RAGE. Nat. Immunol. 2007, 8:487-497.
69. Rönnblom L., Eloranta M.-L., Alm G.V. The type I interferon system in systemic lupus erythematosus. Arthritis Rheum. 2006, 54:408-420.
70. Lande R., Gregorio J., Facchinetti V., Chatterjee B., Wang Y.H., Homey B., Cao W., Wang Y.H., Su B., Nestle F.O., Zal T., Mellman I., Schröder J.M., Liu Y.J., Gilliet M. Plasmacytoid dendritic cells sense self-DNA coupled with antimicrobial peptide. Nature 2007, 449:564-569.
71. Döring Y., Manthey H.D., Dreschsler M., Lievens D., Megens R.T., Soehnien O., Busch M., Manca M., Koenen R.R., Pelisek J., Daemen M.J., Lutgens E., Zenke M., Binder C.J., Weber C., Zermecke Z. Auto-antigenic protein-DNA complexes stimulate plasmacytoid dendritic cells to promote atherosclerosis. Circulation 2012, 125:1673-1683.
72. Wang H., Bloom O., Zhang M., Vishnubhakat J.M., Ombrellino M., Che J., Frazier A., Yang H., Ivanova S., Borovikova L., Manogue K.R., Faist E., Abraham E., Andersson J., Andersson U., Molina P.E., Abumrad N.N., Sama A., Tracey K.J. HMG-1 as a late mediator of endotoxin lethality in mice. Science 1999, 285:248-251.
73. Andersson U., Harris H.E. The role of HMGB1 in the pathogenesis of rheumatic disease. Biochim. Biophys. Acta 2010, 1799:141-148.
74. Scaffidi P., Misteli T., Bianchi M.E. Release of chromatin protein HMGB1 by necrotic cells triggers inflammation. Nature 2002, 418:191-195.
75. Rovere-Querini P., Capobianco A., Scaffidi P., Valentinis B., Catalanotti F., Giazzon M., Dumitriu I.E., Múller S., Iannacone M., Traversari C., Bianchi M.E., Manfredi A.A. HMGB1 is an endogenous immune adjuvant released by necrotic cells. EMBO Rep. 2004, 5:825-830.
76. Yang H., Lundbäck P., Ottosson L., Erlandsson-Harris H., Venereau E., Bianchi M.E., Al-Abed Y., Andersson U., Tracey K.J., Antoine D.J. Redox modification of cysteine residues regulates the cytokine activity of HMGB1. Mol. Med. 2011, [Epub ahead of print]. 10.2119/molmed.2011.00389.
77. Hreggvidsodottir H.S., Ostberg T., Wähämaa H., Schierbeck H., Aveberger A.C., Klevenvall L., Palmblad K., Ottosson L., Andersson U., Harris H.E. The alarmin HMGB1 acts in synergy with endogenous and exogenous danger signals to promote inflammation. J. Leukoc. Biol. 2009, 86:655-662.
78. Wähämaa H., Schierbeck H., Hreggvidsdottir H.S., Palmblad K., Aveberger A.C., Andersoon U., Harris H.E. High mobility group box protein 1 in complex with lipopolysaccharide or IL-1 promotes an increased inflammatory phenotype in synovial fibroblasts. Arthritis Res. Ther. 2011, 13:R136.
79. Pisetsky D. Cell death in the pathogenesis of immune-mediated diseases: the role of HMGB1 and DAMP-PAMP complexes. Swiss Med. Wkly. 2011, 141:13256.
80. Bell C.W., Jiang W., Reich C.F., Pisetsky D.S. The extracellular release of HMGB1 during apoptotic cell death. Am. J. Physiol. Cell Physiol. 2006, 291:C1318-C1325.
81. Kazama H., Ricci J.E., Herndon J.M., Hoppe G., Green D.R., Ferguson T.A. Induction of immunological tolerance by apoptotic cells requires caspase-dependent oxidation of high-mobility group box-1 protein. Immunity 2008, 29:21-32.
82. Urbonaviciute V., Furnrohr B.G., Meister S., Munoz L., Heyder P., De marchis F., Bianchi M.E., Kirschning C., Wagner H., Manfredi A.A., Kalden J.R., Schett G., Rovere-Querini P., Hermann M., Voll R.E. Induction of inflammatory and immune responses by HMGB1-nucleosome complexes: implications for the pathogenesis of SLE. J. Exp. Med. 2008, 205:3007-3018.
83. Lande R., Ganguly D., Facchinetti V., Frasca L., Conrad C., Gregorio J., Meller S., Chamilos G., Sebasigari R., Ricceri V., Bassett R., Amuro H., Fukuhara S., Ito T., Liu Y.-J., Gilliet M. Neutrophils activate plasmacytoid dendritic cells by releasing self-DNA-peptide complexes in systemic lupus erythematosus. Sci. Transl. Med. 2011, 9:1-11.
84. Lee J., Sohn J.W., Zhang Y., Leong K.W., Pisetsky D., Sullenger B.A. Nucleic acid-binding polymers as anti-inflammatory agents. Proc. Natl. Acad. Sci. U. S. A. 2011, 108:14055-14060.
85. Andersson U., Tracey K.J. HMGB1 is a therapeutic target for sterile inflammation and infection. Annu. Rev. Immunol. 2011, 29:139-162.
86. Xu J., Zhang X., Monestier M., Esmon N.L., Esmon C.T. Extracellular histones are mediators of death through TLR2 and TLR4 in mouse fatal liver injury. J. Immunol. 2011, 187:2626-2631.
87. Mortensen E.S., Rekvig O.P. Nephritogenic potential of anti-DNA antibodies against necrotic nucleosomes. J. Am. Soc. Nephrol. 2009, 20:696-704.
88. Bianchi M.E. HMGB1 loves company. J. Leukoc. Biol. 2009, 86:573-576.