From the nucleus to the plasma membrane: Translocation of the nuclear proteins histone H3 and lamin B1 in apoptotic microglia

Apoptosis

Volumn 19, Issue 5, 2014, Pages 759-775

  Klein, Barbara ^a,b   Lütz Meindl, Ursula ^a   Kerschbaum, Hubert H ^a  

^a UNIVERSITY OF SALZBURG   (Austria)

^b PARACELSUS MEDICAL UNIVERSITY   (Austria)

Author keywords

Apoptosis; Histone; Lamin; Microglia; Ultrastructure

Indexed keywords

CARBOBENZOXY VALYL ALANYL ASPARTYL [O METHYL] FLUOROMETHYLKETONE); CASPASE INHIBITOR; HISTONE H3; LAMIN B; LAMIN B1; PHOSPHORUS; UNCLASSIFIED DRUG;

ANIMAL CELL; APOPTOSIS; ARTICLE; CELL LINE; CELL MEMBRANE; CELL MEMBRANE PERMEABILITY; CELL NUCLEUS; CELL SURFACE; CELLULAR DISTRIBUTION; CHROMATIN CONDENSATION; CONCENTRATION (PARAMETERS); CONFOCAL MICROSCOPY; CONTROLLED STUDY; CYTOPLASM; ELECTRON ENERGY LOSS SPECTROSCOPY; IMMUNOGOLD LABELING; MICROGLIA; MOUSE; NONHUMAN; NUCLEAR LAMINA; PRIORITY JOURNAL; PROTEIN ANALYSIS; TRANSMISSION ELECTRON MICROSCOPY; ULTRASTRUCTURE; ULTRAVIOLET IRRADIATION;

AMINO ACID CHLOROMETHYL KETONES; ANIMALS; APOPTOSIS; CASPASE INHIBITORS; CASPASES; CELL MEMBRANE; CELL NUCLEUS; CELLS, CULTURED; CHROMATIN; CHROMATIN ASSEMBLY AND DISASSEMBLY; CYTOPLASM; HISTONES; LAMIN TYPE B; MICE; MICE, INBRED C57BL; MICROGLIA; MICROSCOPY, ELECTRON, TRANSMISSION; PROTEIN TRANSPORT;

EID: 84898865216     PISSN: 13608185     EISSN: 1573675X     Source Type: Journal    
DOI: 10.1007/s10495-014-0970-7     Document Type: Article

References (92)

1. Kerr JF, Wyllie AH, Currie AR (1972) Apoptosis: a basic biological phenomenon with wide-ranging implications in tissue kinetics. Br J Cancer 26(4):239-257
2. Rao L, Perez D, White E (1996) Lamin proteolysis facilitates nuclear events during apoptosis. J Cell Biol 135(6 Pt 1):1441-1455 (Pubitemid 26427643)
3. Croft DR, Coleman ML, Li S, Robertson D, Sullivan T, Stewart CL, Olson MF (2005) Actin-myosin-based contraction is responsible for apoptotic nuclear disintegration. J Cell Biol 168(2):245-255. doi: 10.1083/jcb.200409049 (Pubitemid 40248222)
4. Lazebnik YA, Takahashi A, Moir RD, Goldman RD, Poirier GG, Kaufmann SH, Earnshaw WC (1995) Studies of the lamin proteinase reveal multiple parallel biochemical pathways during apoptotic execution. Proc Natl Acad Sci USA 92(20):9042-9046
5. Slee EA, Adrain C, Martin SJ (2001) Executioner caspase-3, -6, and -7 perform distinct, non-redundant roles during the demolition phase of apoptosis. J Biol Chem 276(10):7320-7326. doi: 10.1074/jbc.M008363200M008363200
6. Casciola-Rosen LA, Anhalt G, Rosen A (1994) Autoantigens targeted in systemic lupus erythematosus are clustered in two populations of surface structures on apoptotic keratinocytes. J Exp Med 179(4):1317-1330 (Pubitemid 24091790)
7. Radic M, Marion T, Monestier M (2004) Nucleosomes are exposed at the cell surface in apoptosis. J Immunol 172(11):6692-6700 (Pubitemid 38669105)
8. Ravichandran KS (2011) Beginnings of a good apoptotic meal: the find-me and eat-me signaling pathways. Immunity 35(4):445-455. doi: 10.1016/j.immuni. 2011.09.004
9. Gaipl US, Munoz LE, Grossmayer G, Lauber K, Franz S, Sarter K, Voll RE, Winkler T, Kuhn A, Kalden J, Kern P, Herrmann M (2007) Clearance deficiency and systemic lupus erythematosus (SLE). J Autoimmun 28(2-3):114-121. doi: 10.1016/j.jaut.2007.02.005 (Pubitemid 46680499)
10. Savill J, Dransfield I, Gregory C, Haslett C (2002) A blast from the past: clearance of apoptotic cells regulates immune responses. Nat Rev Immunol 2(12):965-975. doi: 10.1038/nri957nri957 (Pubitemid 37323217)
11. Elliott MR, Ravichandran KS (2010) Clearance of apoptotic cells: implications in health and disease. J Cell Biol 189(7):1059-1070. doi: 10.1083/jcb.201004096
12. Erwig LP, Henson PM (2007) Immunological consequences of apoptotic cell phagocytosis. Am J Pathol 171(1):2-8. doi: 10.2353/ajpath.2007.070135 (Pubitemid 47339220)
13. Nagata S, Hanayama R, Kawane K (2010) Autoimmunity and the clearance of dead cells. Cell 140(5):619-630. doi: 10.1016/j.cell.2010.02.014
14. Shao WH, Cohen PL (2011) Disturbances of apoptotic cell clearance in systemic lupus erythematosus. Arthritis research & therapy 13(1):202. doi: 10.1186/ar3206
15. Decker P (2006) Nucleosome autoantibodies. Clin Chim Acta 366(1-2):48-60. doi: 10.1016/j.cca.2005.11.009 (Pubitemid 43330966)
16. Gomez-Puerta JA, Burlingame RW, Cervera R (2008) Anti-chromatin (anti-nucleosome) antibodies: diagnostic and clinical value. Autoimmun Rev 7(8):606-611. doi: 10.1016/j.autrev.2008.06.005
17. Rumore PM, Steinman CR (1990) Endogenous circulating DNA in systemic lupus erythematosus. Occurrence as multimeric complexes bound to histone. J Clin Invest 86(1):69-74. doi: 10.1172/JCI114716 (Pubitemid 20226976)
18. Ramage AE, Fox PT, Brey RL, Narayana S, Cykowski MD, Naqibuddin M, Sampedro M, Holliday SL, Franklin C, Wallace DJ, Weisman MH, Petri M (2011) Neuroimaging evidence of white matter inflammation in newly diagnosed systemic lupus erythematosus. Arthritis Rheum 63(10):3048-3057. doi: 10.1002/art.30458
19. Sciascia S, Bertolaccini ML, Baldovino S, Roccatello D, Khamashta MA, Sanna G (2013) Central nervous system involvement in systemic lupus erythematosus: overview on classification criteria. Autoimmun Rev 12(3):426-429. doi: 10.1016/j.autrev.2012.08.014
20. Barned S, Goodman AD, Mattson DH (1995) Frequency of anti-nuclear antibodies in multiple sclerosis. Neurology 45(2):384-385
21. Collard RC, Koehler RP, Mattson DH (1997) Frequency and significance of antinuclear antibodies in multiple sclerosis. Neurology 49(3):857-861 (Pubitemid 27428036)
22. Dore-Duffy P, Donaldson JO, Rothman BL, Zurier RB (1982) Antinuclear antibodies in multiple sclerosis. Arch Neurol 39(8):504-506 (Pubitemid 12089651)
23. Yukitake M, Sueoka E, Sueoka-Aragane N, Sato A, Ohashi H, Yakushiji Y, Saito M, Osame M, Izumo S, Kuroda Y (2008) Significantly increased antibody response to heterogeneous nuclear ribonucleoproteins in cerebrospinal fluid of multiple sclerosis patients but not in patients with human T-lymphotropic virus type I-associated myelopathy/tropical spastic paraparesis. J Neurovirol 14(2):130-135. doi: 10.1080/13550280701883840 (Pubitemid 351619266)
24. Comabella M, Rentzsch K, Rio J, Bustamante MF, Borowski K, Stoecker W, Montalban X (2013) Treatment with interferon-beta does not induce anti-nuclear and anti-neuronal serum autoantibodies in multiple sclerosis patients. J Neuroimmunol 255(1-2):102-104. doi: 10.1016/j.jneuroim.2012.10.016
25. Fukazawa T, Kikuchi S, Sasaki H, Hamada K, Hamada T, Miyasaka K, Tashiro K (1997) Anti-nuclear antibodies and the optic-spinal form of multiple sclerosis. J Neurol 244(8):483-488 (Pubitemid 27424785)
26. Szmyrka-Kaczmarek M, Pokryszko-Dragan A, Pawlik B, Gruszka E, Korman L, Podemski R, Wiland P, Szechinski J (2012) Antinuclear and antiphospholipid antibodies in patients with multiple sclerosis. Lupus 21(4):412-420. doi: 10.1177/0961203311427550
27. Solomon AJ, Hills W, Chen Z, Rosenbaum J, Bourdette D, Whitham R (2013) Autoantibodies and Sjogren's syndrome in multiple sclerosis, a reappraisal. PLoS ONE 8(6):e65385. doi: 10.1371/journal.pone.0065385
28. Mecocci P, Ekman R, Parnetti L, Senin U (1993) Antihistone and anti-dsDNA autoantibodies in Alzheimer's disease and vascular dementia. Biol Psychiatry 34(6):380-385 (Pubitemid 23295754)
29. Lopez OL, Rabin BS, Huff FJ, Rezek D, Reinmuth OM (1992) Serum autoantibodies in patients with Alzheimer's disease and vascular dementia and in nondemented control subjects. Stroke 23(8):1078-1083
30. Ginhoux F, Greter M, Leboeuf M, Nandi S, See P, Gokhan S, Mehler MF, Conway SJ, Ng LG, Stanley ER, Samokhvalov IM, Merad M (2010) Fate mapping analysis reveals that adult microglia derive from primitive macrophages. Science 330(6005):841-845. doi: 10.1126/science.1194637
31. Greter M, Merad M (2013) Regulation of microglia development and homeostasis. Glia 61(1):121-127. doi: 10.1002/glia.22408
32. Jung S, Schwartz M (2012) Non-identical twins - microglia and monocyte-derived macrophages in acute injury and autoimmune inflammation. Front Immunol 3:89. doi: 10.3389/fimmu.2012.00089
33. Kettenmann H, Hanisch UK, Noda M, Verkhratsky A (2011) Physiology of microglia. Physiol Rev 91(2):461-553. doi: 10.1152/physrev.00011.2010
34. Parkhurst CN, Gan WB (2010) Microglia dynamics and function in the CNS. Curr Opin Neurobiol 20(5):595-600. doi: 10.1016/j.conb.2010.07.002
35. Graeber MB (2010) Changing face of microglia. Science 330(6005):783-788. doi: 10.1126/science.1190929
36. Polazzi E, Monti B (2010) Microglia and neuroprotection: from in vitro studies to therapeutic applications. Prog Neurobiol 92(3):293-315. doi: 10.1016/j.pneurobio.2010.06.009
37. Sierra A, Abiega O, Shahraz A, Neumann H (2013) Janus-faced microglia: beneficial and detrimental consequences of microglial phagocytosis. Front Cell Neurosci 7:6. doi: 10.3389/fncel.2013.00006
38. Aguzzi A, Barres BA, Bennett ML (2013) Microglia: scapegoat, saboteur, or something else? Science 339(6116):156-161. doi: 10.1126/science.1227901
39. Rawji KS, Yong VW (2013) The benefits and detriments of macrophages/microglia in models of multiple sclerosis. Clinical Dev Immunol 2013:948976. doi: 10.1155/2013/948976
40. Lee P, Lee J, Kim S, Lee MS, Yagita H, Kim SY, Kim H, Suk K (2001) NO as an autocrine mediator in the apoptosis of activated microglial cells: correlation between activation and apoptosis of microglial cells. Brain Res 892(2):380-385 (Pubitemid 32141226)
41. Ladeby R, Wirenfeldt M, Garcia-Ovejero D, Fenger C, Dissing-Olesen L, Dalmau I, Finsen B (2005) Microglial cell population dynamics in the injured adult central nervous system. Brain Res Brain Res Rev 48(2):196-206. doi: 10.1016/j.brainresrev.2004.12.009 (Pubitemid 40585750)
42. Lee J, Hur J, Lee P, Kim JY, Cho N, Kim SY, Kim H, Lee MS, Suk K (2001) Dual role of inflammatory stimuli in activation-induced cell death of mouse microglial cells. Initiation of two separate apoptotic pathways via induction of interferon regulatory factor-1 and caspase-11. J Biol Chem 276(35):32956-32965. doi: 10.1074/jbc.M104700200-M104700200
43. Liu B, Wang K, Gao HM, Mandavilli B, Wang JY, Hong JS (2001) Molecular consequences of activated microglia in the brain: overactivation induces apoptosis. J Neurochem 77(1):182-189 (Pubitemid 32245092)
44. Mayo L, Jacob-Hirsch J, Amariglio N, Rechavi G, Moutin MJ, Lund FE, Stein R (2008) Dual role of CD38 in microglial activation and activation-induced cell death. J Immunol 181(1):92-103
45. Bonetti B, Pohl J, Gao YL, Raine CS (1997) Cell death during autoimmune demyelination: effector but not target cells are eliminated by apoptosis. J Immunol 159(11):5733-5741 (Pubitemid 127470105)
46. Kohji T, Matsumoto Y (2000) Coexpression of Fas/FasL and Bax on brain and infiltrating T cells in the central nervous system is closely associated with apoptotic cell death during autoimmune encephalomyelitis. J Neuroimmunol 106(1-2):165-171 (Pubitemid 30256089)
47. White CA, McCombe PA, Pender MP (1998) Microglia are more susceptible than macrophages to apoptosis in the central nervous system in experimental autoimmune encephalomyelitis through a mechanism not involving Fas (CD95). Int Immunol 10(7):935-941 (Pubitemid 28325609)
48. Ransohoff RM, Engelhardt B (2012) The anatomical and cellular basis of immune surveillance in the central nervous system. Nat Rev Immunol 12(9):623-635. doi: 10.1038/nri3265
49. Chastain EM, Duncan DS, Rodgers JM, Miller SD (2011) The role of antigen presenting cells in multiple sclerosis. Biochim Biophys Acta 1812(2):265-274. doi: 10.1016/j.bbadis.2010.07.008
50. Goverman JM (2011) Immune tolerance in multiple sclerosis. Immunol Rev 241(1):228-240. doi: 10.1111/j.1600-065X.2011.01016.x
51. Frisoni L, McPhie L, Colonna L, Sriram U, Monestier M, Gallucci S, Caricchio R (2005) Nuclear autoantigen translocation and autoantibody opsonization lead to increased dendritic cell phagocytosis and presentation of nuclear antigens: a novel pathogenic pathway for autoimmunity? J Immunol 175(4):2692-2701 (Pubitemid 41113885)
52. Frisoni L, McPhie L, Kang SA, Monestier M, Madaio M, Satoh M, Caricchio R (2007) Lack of chromatin and nuclear fragmentation in vivo impairs the production of lupus anti-nuclear antibodies. J Immunol 179(11):7959-7966
53. Gabler C, Blank N, Hieronymus T, Schiller M, Berden JH, Kalden JR, Lorenz HM (2004) Extranuclear detection of histones and nucleosomes in activated human lymphoblasts as an early event in apoptosis. Ann Rheum Dis 63(9):1135-1144. doi: 10.1136/ard.2003-011452-63/9/1135 (Pubitemid 39120368)
54. Konishi A, Shimizu S, Hirota J, Takao T, Fan Y, Matsuoka Y, Zhang L, Yoneda Y, Fujii Y, Skoultchi AI, Tsujimoto Y (2003) Involvement of histone H1.2 in apoptosis induced by DNA double-strand breaks. Cell 114(6):673-688 (Pubitemid 37186764)
55. Okamura H, Yoshida K, Amorim BR, Haneji T (2008) Histone H1.2 is translocated to mitochondria and associates with Bak in bleomycin-induced apoptotic cells. J Cell Biochem 103(5):1488-1496. doi: 10.1002/jcb.21537 (Pubitemid 351490717)
56. Schiller M, Bekeredjian-Ding I, Heyder P, Blank N, Ho AD, Lorenz HM (2008) Autoantigens are translocated into small apoptotic bodies during early stages of apoptosis. Cell Death Differ 15(1):183-191. doi: 10.1038/sj.cdd. 4402239 (Pubitemid 350286186)
57. Zierler S, Klein B, Furtner T, Bresgen N, Lütz-Meindl U, Kerschbaum HH (2006) Ultraviolet irradiation-induced apoptosis does not trigger nuclear fragmentation but translocation of chromatin from nucleus into cytoplasm in the microglial cell-line, BV-2. Brain Res 1121(1):12-21. doi: 10.1016/j.brainres. 2006.08.122 (Pubitemid 44708894)
58. Blasi E, Barluzzi R, Bocchini V, Mazzolla R, Bistoni F (1990) Immortalization of murine microglial cells by a v-raf/v-myc carrying retrovirus. J Neuroimmunol 27(2-3):229-237 (Pubitemid 20146292)
59. Giulian D, Baker TJ (1986) Characterization of ameboid microglia isolated from developing mammalian brain. J Neurosci 6(8):2163-2178 (Pubitemid 16043659)
60. Frei K, Bodmer S, Schwerdel C, Fontana A (1986) Astrocyte-derived interleukin 3 as a growth factor for microglia cells and peritoneal macrophages. J Immunol 137(11):3521-3527 (Pubitemid 17193310)
61. Lütz-Meindl U, Aichinger N (2004) Use of energy-filtering transmission electron microscopy for routine ultrastructural analysis of high-pressure-frozen or chemically fixed plant cells. Protoplasma 223:155-162. doi: 10.1007/s00709-003-0033-3 (Pubitemid 38893469)
62. Brack K, Frings W, Dotzauer A, Vallbracht A (1998) A cytopathogenic, apoptosis-inducing variant of hepatitis A virus. J Virol 72(4):3370-3376 (Pubitemid 28175582)
63. Batista LF, Kaina B, Meneghini R, Menck CF (2009) How DNA lesions are turned into powerful killing structures: insights from UV-induced apoptosis. Mutat Res 681(2-3):197-208. doi: 10.1016/j.mrrev.2008.09.001
64. Ferrando-May E, Cordes V, Biller-Ckovric I, Mirkovic J, Gorlich D, Nicotera P (2001) Caspases mediate nucleoporin cleavage, but not early redistribution of nuclear transport factors and modulation of nuclear permeability in apoptosis. Cell Death Differ 8(5):495-505. doi: 10.1038/sj.cdd.4400837 (Pubitemid 32492770)
65. Faleiro L, Lazebnik Y (2000) Caspases disrupt the nuclear-cytoplasmic barrier. J Cell Biol 151(5):951-959
66. Bano D, Dinsdale D, Cabrera-Socorro A, Maida S, Lambacher N, McColl B, Ferrando-May E, Hengartner MO, Nicotera P (2010) Alteration of the nuclear pore complex in Ca(2+)-mediated cell death. Cell Death Differ 17(1):119-133. doi: 10.1038/cdd.2009.112
67. Patre M, Tabbert A, Hermann D, Walczak H, Rackwitz HR, Cordes VC, Ferrando-May E (2006) Caspases target only two architectural components within the core structure of the nuclear pore complex. J Biol Chem 281(2):1296-1304. doi: 10.1074/jbc.M511717200
68. Gilthorpe JD, Oozeer F, Nash J, Calvo M, Bennett DL, Lumsden A, Pini A (2013) Extracellular histone H1 is neurotoxic and drives a pro-inflammatory response in microglia. F1000Research 2. doi: 10.12688/f1000research.2-148.v1
69. Knight JS, Carmona-Rivera C, Kaplan MJ (2012) Proteins derived from neutrophil extracellular traps may serve as self-antigens and mediate organ damage in autoimmune diseases. Front Immunol 3:380. doi: 10.3389/fimmu.2012. 00380
70. Kaplan MJ, Radic M (2012) Neutrophil extracellular traps: double-edged swords of innate immunity. J Immunol 189(6):2689-2695. doi: 10.4049/jimmunol. 1201719
71. Darrah E, Andrade F (2012) NETs: the missing link between cell death and systemic autoimmune diseases? Front Immunol 3:428. doi: 10.3389/fimmu.2012.00428
72. Mantovani A, Cassatella MA, Costantini C, Jaillon S (2011) Neutrophils in the activation and regulation of innate and adaptive immunity. Nat Rev Immunol 11(8):519-531. doi: 10.1038/nri3024
73. Brinkmann V, Zychlinsky A (2012) Neutrophil extracellular traps: is immunity the second function of chromatin? J Cell Biol 198(5):773-783. doi: 10.1083/jcb.201203170
74. Goldmann O, Medina E (2012) The expanding world of extracellular traps: not only neutrophils but much more. Front Immunol 3:420. doi: 10.3389/fimmu.2012.00420
75. Amulic B, Hayes G (2011) Neutrophil extracellular traps. Curr Biol 21(9):R297-298. doi: 10.1016/j.cub.2011.03.021
76. Brinkmann V, Reichard U, Goosmann C, Fauler B, Uhlemann Y, Weiss DS, Weinrauch Y, Zychlinsky A (2004) Neutrophil extracellular traps kill bacteria. Science 303(5663):1532-1535. doi: 10.1126/science.1092385 (Pubitemid 38314426)
77. Yousefi S, Simon D, Simon HU (2012) Eosinophil extracellular DNA traps: molecular mechanisms and potential roles in disease. Curr Opin Immunol 24(6):736-739. doi: 10.1016/j.coi.2012.08.010
78. von Kockritz-Blickwede M, Goldmann O, Thulin P, Heinemann K, Norrby-Teglund A, Rohde M, Medina E (2008) Phagocytosis-independent antimicrobial activity of mast cells by means of extracellular trap formation. Blood 111(6):3070-3080. doi: 10.1182/blood-2007-07-104018
79. Chow OA, von Kockritz-Blickwede M, Bright AT, Hensler ME, Zinkernagel AS, Cogen AL, Gallo RL, Monestier M, Wang Y, Glass CK, Nizet V (2010) Statins enhance formation of phagocyte extracellular traps. Cell Host Microbe 8(5):445-454. doi: 10.1016/j.chom.2010.10.005
80. Aulik NA, Hellenbrand KM, Czuprynski CJ (2012) Mannheimia haemolytica and its leukotoxin cause macrophage extracellular trap formation by bovine macrophages. Infect Immun 80(5):1923-1933. doi: 10.1128/IAI.06120-11
81. Hellenbrand KM, Forsythe KM, Rivera-Rivas JJ, Czuprynski CJ, Aulik NA (2013) Histophilus somni causes extracellular trap formation by bovine neutrophils and macrophages. Microb Pathog 54:67-75. doi: 10.1016/j.micpath. 2012.09.007
82. Mohanan S, Horibata S, McElwee JL, Dannenberg AJ, Coonrod SA (2013) Identification of macrophage extracellular trap-like structures in mammary gland adipose tissue: a preliminary study. Front Immunol 4:67. doi: 10.3389/fimmu.2013.00067
83. Wong KW, Jacobs WR Jr (2013) Mycobacterium tuberculosis exploits human interferon gamma to stimulate macrophage extracellular trap formation and necrosis. J Infect Dis 208(1):109-119. doi: 10.1093/infdis/jit097
84. Hirsch JG (1958) Bactericidal action of histone. J Exp Med 108(6):925-944
85. Parseghian MH, Luhrs KA (2006) Beyond the walls of the nucleus: the role of histones in cellular signaling and innate immunity. Biochem Cell Biol 84(4):589-604. doi: 10.1139/o06-082 (Pubitemid 44703662)
86. Yipp BG, Petri B, Salina D, Jenne CN, Scott BN, Zbytnuik LD, Pittman K, Asaduzzaman M, Wu K, Meijndert HC, Malawista SE, de Boisfleury Chevance A, Zhang K, Conly J, Kubes P (2012) Infection-induced NETosis is a dynamic process involving neutrophil multitasking in vivo. Nat Med 18(9):1386-1393. doi: 10.1038/nm.2847
87. Fuchs TA, Abed U, Goosmann C, Hurwitz R, Schulze I, Wahn V, Weinrauch Y, Brinkmann V, Zychlinsky A (2007) Novel cell death program leads to neutrophil extracellular traps. J Cell Biol 176(2):231-241. doi: 10.1083/jcb.200606027 (Pubitemid 46143263)
88. Yousefi S, Gold JA, Andina N, Lee JJ, Kelly AM, Kozlowski E, Schmid I, Straumann A, Reichenbach J, Gleich GJ, Simon HU (2008) Catapult-like release of mitochondrial DNA by eosinophils contributes to antibacterial defense. Nat Med 14(9):949-953. doi: 10.1038/nm.1855
89. Yousefi S, Mihalache C, Kozlowski E, Schmid I, Simon HU (2009) Viable neutrophils release mitochondrial DNA to form neutrophil extracellular traps. Cell Death Differ 16(11):1438-1444. doi: 10.1038/cdd.2009.96
90. Senecal JL, Rauch J, Grodzicky T, Raynauld JP, Uthman I, Nava A, Guimond M, Raymond Y (1999) Strong association of autoantibodies to human nuclear lamin B1 with lupus anticoagulant antibodies in systemic lupus erythematosus. Arthritis Rheum 42(7):1347-1353. doi: 10.1002/1529-0131(199907)42:7<1347:: AID-ANR7>3.0.CO;2-# (Pubitemid 30265591)
91. Dieude M, Senecal JL, Rauch J, Hanly JG, Fortin P, Brassard N, Raymond Y (2002) Association of autoantibodies to nuclear lamin B1 with thromboprotection in systemic lupus erythematosus: lack of evidence for a direct role of lamin B1 in apoptotic blebs. Arthritis Rheum 46(10):2695-2707. doi: 10.1002/art.10552 (Pubitemid 36118934)
92. Moisan E, Girard D (2006) Cell surface expression of intermediate filament proteins vimentin and lamin B1 in human neutrophil spontaneous apoptosis. J Leukoc Biol 79(3):489-498. doi: 10.1189/jlb.0405190 (Pubitemid 44831226)