Breaking immunological tolerance in systemic lupus erythematosus

Frontiers in Immunology

Volumn 5, Issue APR, 2014, Pages

  Pieterse, Elmar ^a   van der Vlag, Johan ^a  

^a RADBOUD UNIVERSITY MEDICAL CENTER   (Netherlands)

Author keywords

Apoptosis; Histone modifications; NETosis; Neutrophil; Systemic lupus erythematosus

Indexed keywords

ALPHA INTERFERON; AUTOANTIGEN; C REACTIVE PROTEIN; CATHELICIDIN ANTIMICROBIAL PEPTIDE LL 37; CD34 ANTIGEN; CITRULLINE; COMPLEMENT COMPONENT C1Q; FAS LIGAND; HIGH MOBILITY GROUP B1 PROTEIN; HISTONE ACETYLTRANSFERASE; HISTONE DEACETYLASE; IMMUNOGLOBULIN G; INTERLEUKIN 17; INTERLEUKIN 1BETA; INTERLEUKIN 8; MANNOSE BINDING LECTIN; NICOTINAMIDE ADENINE DINUCLEOTIDE ADENOSINE DIPHOSPHATE RIBOSYLTRANSFERASE; PROTEIN ARGININE DEIMINASE; THROMBOCYTE ACTIVATING FACTOR; TOLL LIKE RECEPTOR; TUMOR NECROSIS FACTOR ALPHA; TUMOR NECROSIS FACTOR RELATED APOPTOSIS INDUCING LIGAND; UBIQUITIN; URATE;

ANTIGEN PRESENTATION; APOPTOSIS; AUTOIMMUNITY; DEAMINATION; DNA TRANSCRIPTION; FOLLICULAR DENDRITIC CELL; HISTONE ACETYLATION; HISTONE METHYLATION; HISTONE MODIFICATION; HISTONE UBIQUITINATION; HUMAN; IMMUNE COMPLEX DEPOSITION; IMMUNOLOGICAL TOLERANCE; INFLAMMATION; KERATINIZATION; MACROPHAGE; NEUTROPHIL; REVIEW; SYSTEMIC LUPUS ERYTHEMATOSUS; TELOMERE HOMEOSTASIS;

EID: 84900859409     PISSN: None     EISSN: 16643224     Source Type: Journal    
DOI: 10.3389/fimmu.2014.00164     Document Type: Review

References (94)

1. Ippolito A, Wallace DJ, Gladman D, Fortin PR, Urowitz M, Werth V, et al. Autoantibodies in systemic lupus erythematosus: comparison of historical and current assessment of seropositivity. Lupus (2011) 20:250-5. doi: 10.1177/0961203310385738.
2. Pradhan VD, Badakere SS, Bichile LS, Almeida AF. Anti-neutrophil cytoplasmic antibodies (ANCA) in systemic lupus erythematosus: prevalence, clinical associations and correlation with other autoantibodies. J Assoc Physicians India (2004) 52:533-7.
3. Bouts YM, Wolthuis DF, Dirkx MF, Pieterse E, Simons EM, Van Boekel AM, et al. Apoptosis and NET formation in the pathogenesis of SLE. Autoimmunity (2012) 45:597-601. doi:10.3109/08916934.2012.719953.
4. Munoz LE, Van Bavel C, Franz S, Berden J, Herrmann M, Van Der Vlag J. Apoptosis in the pathogenesis of systemic lupus erythematosus. Lupus (2008) 17:371-5. doi:10.1177/0961203308089990.
5. Saraste A, Pulkki K. Morphologic and biochemical hallmarks of apoptosis. Cardiovasc Res (2000) 45:528-37. doi:10.1016/S0008-6363(99)00384-3.
6. Rosen A, Casciola-Rosen L, Ahearn J. Novel packages of viral and self-antigens are generated during apoptosis. J Exp Med (1995) 181:1557-61. doi:10.1084/jem.181.4.1557.
7. 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) 179:1317-30. doi:10.1084/jem.179.4.1317.
8. Brinkmann V, Reichard U, Goosmann C, Fauler B, Uhlemann Y, Weiss DS, et al. Neutrophil extracellular traps kill bacteria. Science (2004) 303:1532-5. doi:10.1126/science.1092385.
9. Knight JS, Carmona-Rivera C, Kaplan MJ. Proteins derived from neutrophil extracellular traps may serve as self-antigens and mediate organ damage in autoimmune diseases. Front Immunol (2012) 3:380. doi:10.3389/fimmu.2012.00380.
10. Jenne CN, Wong CH, Zemp FJ, Mcdonald B, Rahman MM, Forsyth PA, et al. Neutrophils recruited to sites of infection protect from virus challenge by releasing neutrophil extracellular traps. Cell Host Microbe (2013) 13:169-80. doi:10.1016/j.chom.2013.01.005.
11. Urban CF, Reichard U, Brinkmann V, Zychlinsky A. Neutrophil extracellular traps capture and kill Candida albicans yeast and hyphal forms. Cell Microbiol (2006) 8:668-76. doi:10.1111/j.1462-5822.2005.00659.x.
12. Abi Abdallah DS, Denkers EY. Neutrophils cast extracellular traps in response to protozoan parasites. Front Immunol (2012) 3:382. doi:10.3389/fimmu.2012.00382.
13. Goldmann O, Medina E. The expanding world of extracellular traps: not only neutrophils but much more. Front Immunol (2012) 3:420. doi:10.3389/fimmu.2012.00420.
14. Remijsen Q, Kuijpers TW, Wirawan E, Lippens S, Vandenabeele P, Vanden Berghe T. Dying for a cause: NETosis, mechanisms behind an antimicrobial cell death modality. Cell Death Differ (2011) 18:581-8. doi:10.1038/cdd.2011.1.
15. Andrews BS, Eisenberg RA, Theofilopoulos AN, Izui S, Wilson CB, Mcconahey PJ, et al. Spontaneous murine lupus-like syndromes. Clinical and immunopathological manifestations in several strains. J Exp Med (1978) 148:1198-215. doi:10.1084/jem.148.5.1198.
16. Dhir V, Singh AP, Aggarwal A, Naik S, Misra R. Increased T-lymphocyte apoptosis in lupus correlates with disease activity and may be responsible for reduced T-cell frequency: a cross-sectional and longitudinal study. Lupus (2009) 18:785-91. doi:10.1177/0961203309103152.
17. Courtney PA, Crockard AD, Williamson K, Irvine AE, Kennedy RJ, Bell AL. Increased apoptotic peripheral blood neutrophils in systemic lupus erythematosus: relations with disease activity, antibodies to double stranded DNA, and neutropenia. Ann Rheum Dis (1999) 58:309-14. doi:10.1136/ard.58.5.309.
18. Ren Y, Tang J, Mok MY, Chan AW, Wu A, Lau CS. Increased apoptotic neutrophils and macrophages and impaired macrophage phagocytic clearance of apoptotic neutrophils in systemic lupus erythematosus. Arthritis Rheum (2003) 48:2888-97. doi:10.1002/art.11237.
19. Shoshan Y, Shapira I, Toubi E, Frolkis I, Yaron M, Mevorach D. Accelerated Fas-mediated apoptosis of monocytes and maturing macrophages from patients with systemic lupus erythematosus: relevance to in vitro impairment of interaction with iC3b-opsonized apoptotic cells. J Immunol (2001) 167:5963-9.
20. Bengtsson AA, Sturfelt G, Gullstrand B, Truedsson L. 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 (2004) 135:535-43. doi:10.1111/j.1365-2249.2003.02386.x.
21. Kaplan MJ, Lewis EE, Shelden EA, Somers E, Pavlic R, Mccune WJ, et al. The apoptotic ligands TRAIL, TWEAK, and Fas ligand mediate monocyte death induced by autologous lupus T cells. J Immunol (2002) 169:6020-9.
22. Ma CY, Jiao YL, Zhang J, Yang QR, Zhang ZF, Shen YJ, et al. Elevated plasma level of HMGB1 is associated with disease activity and combined alterations with IFN-alpha and TNF-alpha in systemic lupus erythematosus. Rheumatol Int (2012) 32:395-402. doi:10.1007/s00296-010-1636-6.
23. Vordenbaumen S, Fischer-Betz R, Timm D, Sander O, Chehab G, Richter J, et al. Elevated levels of human beta-defensin 2 and human neutrophil peptides in systemic lupus erythematosus. Lupus (2010) 19:1648-53. doi:10.1177/0961203310377089.
24. Sthoeger ZM, Bezalel S, Chapnik N, Asher I, Froy O. High alpha-defensin levels in patients with systemic lupus erythematosus. Immunology (2009) 127:116-22. doi:10.1111/j.1365-2567.2008.02997.x.
25. Khandpur R, Carmona-Rivera C, Vivekanandan-Giri A, Gizinski A, Yalavarthi S, Knight JS, et al. NETs are a source of citrullinated autoantigens and stimulate inflammatory responses in rheumatoid arthritis. Sci Transl Med (2013) 5:178ra140. doi:10.1126/scitranslmed.3005580.
26. Mitroulis I, Kambas K, Chrysanthopoulou A, Skendros P, Apostolidou E, Kourtzelis I, et al. Neutrophil extracellular trap formation is associated with IL-1beta and autophagy-related signaling in gout. PLoS One (2011) 6:e29318. doi:10.1371/journal.pone.0029318.
27. Gupta AK, Hasler P, Holzgreve W, Gebhardt S, Hahn S. Induction of neutrophil extracellular DNA lattices by placental microparticles and IL-8 and their presence in preeclampsia. Hum Immunol (2005) 66:1146-54. doi:10.1016/j.humimm.2005.11.003.
28. Niewold TB, Clark DN, Salloum R, Poole BD. Interferon alpha in systemic lupus erythematosus. J Biomed Biotechnol (2010) 2010:948364. doi:10.1155/2010/948364.
29. Martinelli S, Urosevic M, Daryadel A, Oberholzer PA, Baumann C, Fey MF, et al. Induction of genes mediating interferon-dependent extracellular trap formation during neutrophil differentiation. J Biol Chem (2004) 279:44123-32. doi:10.1074/jbc.M405883200.
30. Bosch X. Systemic lupus erythematosus and the neutrophil. N Engl J Med (2011) 365:758-60. doi:10.1056/NEJMcibr1107085.
31. Kaplan MJ. Neutrophils in the pathogenesis and manifestations of SLE. Nat Rev Rheumatol (2011) 7:691-9. doi:10.1038/nrrheum.2011.132.
32. Garcia-Romo GS, Caielli S, Vega B, Connolly J, Allantaz F, Xu Z, et al. Netting neutrophils are major inducers of type I IFN production in pediatric systemic lupus erythematosus. Sci Transl Med (2011) 3:73ra20. doi:10.1126/scitranslmed.3001201.
33. Denny MF, Yalavarthi S, Zhao W, Thacker SG, Anderson M, Sandy AR, et al. A distinct subset of proinflammatory neutrophils isolated from patients with systemic lupus erythematosus induces vascular damage and synthesizes type I IFNs. J Immunol (2010) 184:3284-97. doi:10.4049/jimmunol.0902199.
34. Elliott MR, Ravichandran KS. Clearance of apoptotic cells: implications in health and disease. J Cell Biol (2010) 189:1059-70. doi:10.1083/jcb.201004096.
35. Fransen JH, Berden JH, Koeter CM, Adema GJ, Van Der Vlag J, Hilbrands LB. Effect of administration of apoptotic blebs on disease development in lupus mice. Autoimmunity (2012) 45:290-7. doi:10.3109/08916934.2012.664668.
36. Liu CL, Tangsombatvisit S, Rosenberg JM, Mandelbaum G, Gillespie EC, Gozani OP, et al. Specific post-translational histone modifications of neutrophil extracellular traps as immunogens and potential targets of lupus autoantibodies. Arthritis Res Ther (2012) 14:R25. doi:10.1186/ar3933.
37. Svensson B. Monocyte in vitro function in systemic lupus erythematosus (SLE). I. A clinical and immunological study. Scand J Rheumatol Suppl (1980) 31:29-41.
38. Herrmann M, Voll RE, Zoller OM, Hagenhofer M, Ponner BB, Kalden JR. Impaired phagocytosis of apoptotic cell material by monocyte-derived macrophages from patients with systemic lupus erythematosus. Arthritis Rheum (1998) 41:1241-50. doi:10.1002/1529-0131(199807)41:7<1241::AID-ART15>3.0.CO;2-H.
39. Tas SW, Quartier P, Botto M, Fossati-Jimack L. Macrophages from patients with SLE and rheumatoid arthritis have defective adhesion in vitro, while only SLE macrophages have impaired uptake of apoptotic cells. Ann Rheum Dis (2006) 65:216-21. doi:10.1136/ard.2005.037143.
40. Munoz LE, Lauber K, Schiller M, Manfredi AA, Herrmann M. The role of defective clearance of apoptotic cells in systemic autoimmunity. Nat Rev Rheumatol (2010) 6:280-9. doi:10.1038/nrrheum.2010.46.
41. Baumann I, Kolowos W, Voll RE, Manger B, Gaipl U, Neuhuber WL, et al. Impaired uptake of apoptotic cells into tingible body macrophages in germinal centers of patients with systemic lupus erythematosus. Arthritis Rheum (2002) 46:191-201. doi:10.1002/1529-0131(200201)46:1<191::AID-ART10027>3.0.CO;2-K.
42. Gaipl US, Munoz LE, Grossmayer G, Lauber K, Franz S, Sarter K, et al. Clearance deficiency and systemic lupus erythematosus (SLE). J Autoimmun (2007) 28:114-21. doi:10.1016/j.jaut.2007.02.005.
43. Cairns AP, Crockard AD, Mcconnell JR, Courtney PA, Bell AL. Reduced expression of CD44 on monocytes and neutrophils in systemic lupus erythematosus: relations with apoptotic neutrophils and disease activity. Ann Rheum Dis (2001) 60:950-5. doi:10.1136/ard.60.10.950.
44. Gronwall C, Vas J, Silverman GJ. Protective roles of natural IgM antibodies. Front Immunol (2012) 3:66. doi:10.3389/fimmu.2012.00066.
45. Panda AK, Parida JR, Tripathy R, Pattanaik SS, Ravindran B, Das BK. Mannose binding lectin: a biomarker of systemic lupus erythematosus disease activity. Arthritis Res Ther (2012) 14:R218. doi:10.1186/ar4057.
46. 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:e22659. doi:10.1371/journal.pone.0022659.
47. Rodriguez W, Mold C, Marnell LL, Hutt J, Silverman GJ, Tran D, et al. Prevention and reversal of nephritis in MRL/lpr mice with a single injection of C-reactive protein. Arthritis Rheum (2006) 54:325-35. doi:10.1002/art.21556.
48. Walport MJ, Davies KA, Botto M. C1q and systemic lupus erythematosus. Immunobiology (1998) 199:265-85. doi:10.1016/S0171-2985(98)80032-6.
49. Martens HA, Zuurman MW, De Lange AH, Nolte IM, Van Der Steege G, Navis GJ, et al. Analysis of C1q polymorphisms suggests association with systemic lupus erythematosus, serum C1q and CH50 levels and disease severity. Ann Rheum Dis (2009) 68:715-20. doi:10.1136/ard.2007.085688.
50. Russell AI, Cunninghame Graham DS, Shepherd C, Roberton CA, Whittaker J, Meeks J, et al. Polymorphism at the C-reactive protein locus influences gene expression and predisposes to systemic lupus erythematosus. Hum Mol Genet (2004) 13:137-47. doi:10.1093/hmg/ddh021.
51. Lee YH, Witte T, Momot T, Schmidt RE, Kaufman KM, Harley JB, et al. The mannose-binding lectin gene polymorphisms and systemic lupus erythematosus: two case-control studies and a meta-analysis. Arthritis Rheum (2005) 52:3966-74. doi:10.1002/art.21484.
52. Shoenfeld Y, Szyper-Kravitz M, Witte T, Doria A, Tsutsumi A, Tatsuya A, et al. Autoantibodies against protective molecules-C1q, C-reactive protein, serum amyloid P, mannose-binding lectin, and apolipoprotein A1: prevalence in systemic lupus erythematosus. Ann N Y Acad Sci (2007) 1108:227-39. doi:10.1196/annals.1422.025.
53. Bassi N, Ghirardello A, Blank M, Zampieri S, Sarzi-Puttini P, Mantovani A, et al. IgG anti-pentraxin 3 antibodies in systemic lupus erythematosus. Ann Rheum Dis (2010) 69:1704-10. doi:10.1136/ard.2009.117804.
54. Napirei M, Karsunky H, Zevnik B, Stephan H, Mannherz HG, Moroy T. Features of systemic lupus erythematosus in Dnase1-deficient mice. Nat Genet (2000) 25:177-81. doi:10.1038/76032.
55. Skiljevic D, Jeremic I, Nikolic M, Andrejevic S, Sefik-Bukilica M, Stojimirovic B, et al. Serum DNase I activity in systemic lupus erythematosus: correlation with immunoserological markers, the disease activity and organ involvement. Clin Chem Lab Med (2013) 51:1083-91. doi:10.1515/cclm-2012-0521.
56. Shin HD, Park BL, Kim LH, Lee HS, Kim TY, Bae SC. Common DNase I polymorphism associated with autoantibody production among systemic lupus erythematosus patients. Hum Mol Genet (2004) 13:2343-50. doi:10.1093/hmg/ddh275.
57. Yeh TM, Chang HC, Liang CC, Wu JJ, Liu MF. Deoxyribonuclease-inhibitory antibodies in systemic lupus erythematosus. J Biomed Sci (2003) 10:544-51. doi:10.1007/BF02256116.
58. Hakkim A, Furnrohr BG, Amann K, Laube B, Abed UA, Brinkmann V, et al. Impairment of neutrophil extracellular trap degradation is associated with lupus nephritis. Proc Natl Acad Sci U S A (2010) 107:9813-8. doi:10.1073/pnas.0909927107.
59. Leffler J, Martin M, Gullstrand B, Tyden H, Lood C, Truedsson L, et al. Neutrophil extracellular traps that are not degraded in systemic lupus erythematosus activate complement exacerbating the disease. J Immunol (2012) 188:3522-31. doi:10.4049/jimmunol.1102404.
60. Farrera C, Fadeel B. Macrophage clearance of neutrophil extracellular traps is a silent process. J Immunol (2013) 191:2647-56. doi:10.4049/jimmunol.1300436.
61. Lande R, Ganguly D, Facchinetti V, Frasca L, Conrad C, Gregorio J, et al. Neutrophils activate plasmacytoid dendritic cells by releasing self-DNA-peptide complexes in systemic lupus erythematosus. Sci Transl Med (2011) 3:73ra19. doi:10.1126/scitranslmed.3001180.
62. Cline AM, Radic MZ. Apoptosis, subcellular particles, and autoimmunity. Clin Immunol (2004) 112:175-82. doi:10.1016/j.clim.2004.02.017.
63. Biermann M, Maueroder C, Brauner JM, Chaurio R, Janko C, Herrmann M, et al. Surface code-biophysical signals for apoptotic cell clearance. Phys Biol (2013) 10:065007. doi:10.1088/1478-3975/10/6/065007.
64. Tsumiyama K, Miyazaki Y, Shiozawa S. Self-organized criticality theory of autoimmunity. PLoS One (2009) 4:e8382. doi:10.1371/journal.pone.0008382.
65. Dieker J, Muller S. Epigenetic histone code and autoimmunity. Clin Rev Allergy Immunol (2010) 39:78-84. doi:10.1007/s12016-009-8173-7.
66. Sun XY, Shi J, Han L, Su Y, Li ZG. Anti-histones antibodies in systemic lupus erythematosus: prevalence and frequency in neuropsychiatric lupus. J Clin Lab Anal (2008) 22:271-7. doi:10.1002/jcla.20248.
67. + T cells. J Rheumatol (2008) 35:804-10.
68. Garcia BA, Busby SA, Shabanowitz J, Hunt DF, Mishra N. Resetting the epigenetic histone code in the MRL-lpr/lpr mouse model of lupus by histone deacetylase inhibition. J Proteome Res (2005) 4:2032-42. doi:10.1021/pr050188r.
69. Forster N, Gallinat S, Jablonska J, Weiss S, Elsasser HP, Lutz W. p300 protein acetyltransferase activity suppresses systemic lupus erythematosus-like autoimmune disease in mice. J Immunol (2007) 178:6941-8.
70. Dieker JW, Fransen JH, Van Bavel CC, Briand JP, Jacobs CW, Muller S, et al. Apoptosis-induced acetylation of histones is pathogenic in systemic lupus erythematosus. Arthritis Rheum (2007) 56:1921-33. doi:10.1002/art.22646.
71. van Bavel CC, Dieker J, Muller S, Briand JP, Monestier M, Berden JH, et al. Apoptosis-associated acetylation on histone H2B is an epitope for lupus autoantibodies. Mol Immunol (2009) 47:511-6. doi:10.1016/j.molimm.2009.08.009.
72. Boix-Chornet M, Fraga MF, Villar-Garea A, Caballero R, Espada J, Nunez A, et al. Release of hypoacetylated and trimethylated histone H4 is an epigenetic marker of early apoptosis. J Biol Chem (2006) 281:13540-7. doi:10.1074/jbc.M601136200.
73. van Bavel CC, Dieker JW, Kroeze Y, Tamboer WP, Voll R, Muller S, et al. Apoptosis-induced histone H3 methylation is targeted by autoantibodies in systemic lupus erythematosus. Ann Rheum Dis (2011) 70:201-7. doi:10.1136/ard.2010.129320.
74. West MH, Bonner WM. Histone 2B can be modified by the attachment of ubiquitin. Nucleic Acids Res (1980) 8:4671-80. doi:10.1093/nar/8.20.4671.
75. Plaue S, Muller S, Van Regenmortel MH. A branched, synthetic octapeptide of ubiquitinated histone H2A as target of autoantibodies. J Exp Med (1989) 169:1607-17. doi:10.1084/jem.169.5.1607.
76. Stockl F, Muller S, Batsford S, Schmiedeke T, Waldherr R, Andrassy K, et al. A role for histones and ubiquitin in lupus nephritis? Clin Nephrol (1994) 41:10-7.
77. Marushige Y, Marushige K. Disappearance of ubiquitinated histone H2A during chromatin condensation in TGF beta 1-induced apoptosis. Anticancer Res (1995) 15:267-72.
78. Mimnaugh EG, Kayastha G, Mcgovern NB, Hwang SG, Marcu MG, Trepel J, et al. Caspase-dependent deubiquitination of monoubiquitinated nucleosomal histone H2A induced by diverse apoptogenic stimuli. Cell Death Differ (2001) 8:1182-96. doi:10.1038/sj.cdd.4400924.
79. Kawasaki A, Ito I, Ito S, Hayashi T, Goto D, Matsumoto I, et al. Association of TNFAIP3 polymorphism with susceptibility to systemic lupus erythematosus in a Japanese population. J Biomed Biotechnol (2010) 2010:207578. doi:10.1155/2010/207578.
80. Jury EC, Kabouridis PS, Abba A, Mageed RA, Isenberg DA. Increased ubiquitination and reduced expression of LCK in T lymphocytes from patients with systemic lupus erythematosus. Arthritis Rheum (2003) 48:1343-54. doi:10.1002/art.10978.
81. Franceschini F, Cavazzana I. Anti-Ro/SSA and La/SSB antibodies. Autoimmunity (2005) 38:55-63. doi:10.1080/08916930400022954.
82. Kanai Y, Kawaminami Y, Miwa M, Matsushima T, Sugimura T. Naturally-occurring antibodies to poly(ADP-ribose) in patients with systemic lupus erythematosus. Nature (1977) 265:175-7. doi:10.1038/265175a0.
83. Okolie EE, Shall S. The significance of antibodies to poly(adenosine diphosphate-ribose) in systemic lupus erythematosus. Clin Exp Immunol (1979) 36:151-64.
84. Muller S, Briand JP, Barakat S, Lagueux J, Poirier GG, De Murcia G, et al. Autoantibodies reacting with poly(ADP-ribose) and with a zinc-finger functional domain of poly(ADP-ribose) polymerase involved in the recognition of damaged DNA. Clin Immunol Immunopathol (1994) 73:187-96. doi:10.1006/clin.1994.1187.
85. Decker P, Isenberg D, Muller S. Inhibition of caspase-3-mediated poly(ADP-ribose) polymerase (PARP) apoptotic cleavage by human PARP autoantibodies and effect on cells undergoing apoptosis. J Biol Chem (2000) 275:9043-6. doi:10.1074/jbc.275.12.9043.
86. Kanai Y, Sugimura T. Comparative studies on antibodies to poly(ADP-ribose) in rabbits and patients with systemic lupus erythematosus. Immunology (1981) 43:101-10.
87. Messner S, Altmeyer M, Zhao H, Pozivil A, Roschitzki B, Gehrig P, et al. PARP1 ADP-ribosylates lysine residues of the core histone tails. Nucleic Acids Res (2010) 38:6350-62. doi:10.1093/nar/gkq463.
88. Schellekens GA, Visser H, De Jong BA, Van Den Hoogen FH, Hazes JM, Breedveld FC, et al. The diagnostic properties of rheumatoid arthritis antibodies recognizing a cyclic citrullinated peptide. Arthritis Rheum (2000) 43:155-63. doi:10.1002/1529-0131(200001)43:1<155::AID-ANR20>3.0.CO;2-3.
89. Li P, Li M, Lindberg MR, Kennett MJ, Xiong N, Wang Y. PAD4 is essential for antibacterial innate immunity mediated by neutrophil extracellular traps. J Exp Med (2010) 207:1853-62. doi:10.1084/jem.20100239.
90. Skare TL, Nisihara R, Barbosa BB, Da Luz A, Utiyama S, Picceli V. Anti-CCP in systemic lupus erythematosus patients: a cross sectional study in Brazilian patients. Clin Rheumatol (2013) 32:1065-70. doi:10.1007/s10067-013-2213-7.
91. Taraborelli M, Inverardi F, Fredi M, Ceribelli A, Cavazzana I, Tincani A, et al. Anti-cyclic citrullinated peptide antibodies in systemic lupus erythematosus patients with articular involvement: a predictive marker for erosive disease? Reumatismo (2012) 64:321-5. doi:10.4081/reumatismo.2012.321.
92. Qing YF, Zhang QB, Zhou JG, Yuan GH, Wei J, Xing Y, et al. The detecting and clinical value of anti-cyclic citrullinated peptide antibodies in patients with systemic lupus erythematosus. Lupus (2009) 18:713-7. doi:10.1177/0961203309102817.
93. Romero V, Fert-Bober J, Nigrovic PA, Darrah E, Haque UJ, Lee DM, et al. Immune-mediated pore-forming pathways induce cellular hypercitrullination and generate citrullinated autoantigens in rheumatoid arthritis. Sci Transl Med (2013) 5:209ra150. doi:10.1126/scitranslmed.3006869.
94. Kilsgard O, Andersson P, Malmsten M, Nordin SL, Linge HM, Eliasson M, et al. Peptidylarginine deiminases present in the airways during tobacco smoking and inflammation can citrullinate the host defense peptide LL-37, resulting in altered activities. Am J Respir Cell Mol Biol (2012) 46:240-8. doi:10.1165/rcmb.2010-0500OC.