Cited by 282Immune Response and InflammationCell death mechanisms and regulationPhagocytosis and Immune Regulation

The immune response to secondary necrotic cells

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Sachet, Monika, Liang, Ying Yu, Oehler, Rudolf·2017·Apoptosis

Abstract

When apoptotic cells are not cleared in an efficient and timely manner, they progress to secondary necrosis and lose their membrane integrity. This results in a leakage of immunostimulatory, danger associated molecular patterns (DAMPs), similar to accidental (or primary) necrosis. However, primary necrosis is a sudden event with an inadvertent release of almost unmodified DAMPs. Secondary necrotic cells, in contrast, have gone through various modifications during the process of apoptosis. Recent research revealed that the molecules released from the cytoplasm or exposed on the cell surface differ between primary necrosis, secondary necrosis, and regulated necrosis such as necroptosis. This review gives an overview of these differences and focusses their effects on the immune response. The implications to human physiology and diseases are manifold and will be discussed in the context of cancer, neurodegenerative disorders and autoimmunity.

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  • Initial cell death of transplanted cells can cause release of molecules that initiate other immune responses, further exacerbating the issue by causing other transplanted cells to exhibit stress responses.

    “This initial cell death of transplanted cells can also cause release of molecules that initiate other immune responses, further exacerbating the issue by causing other transplanted cells to exhibit stress responses.”

    From Developments in stem cell-derived islet replacement therapy for treating type 1 diabetes (2023) · cites this paper as [141]

    The Introduction (page unavailable) says dying cells release DAMPs that activate innate immune cells and induce inflammation. The Summary and concluding remarks says neighboring cells can show different responses to stress, but does not establish that molecules released by dying cells cause stress responses in other cells. The paper does not address this proposed chain of events in transplanted cells. (LLM, conf=0.85)

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  1. [1]Fulda S Gorman a M Hori O Samali a Cellular stress responses: cell survival and cell death Int J Cell Biol 2010 PMC2825543 20182529
  2. [2]Tyedmers J Mogk A Bukau B Cellular strategies for controlling protein aggregation Nat Rev Mol Cell Biol 2010 11 777 788 10.1038/nrm2993 20944667 · DOI
  3. [3]Long JS Ryan KM New frontiers in promoting tumour cell death: targeting apoptosis, necroptosis and autophagy Oncogene 2012 31 5045 5060 10.1038/onc.2012.7 22310284 · DOI
  4. [4]Pasparakis M Vandenabeele P Necroptosis and its role in inflammation Nature 2015 517 311 320 10.1038/nature14191 25592536 · DOI · Paper page
  5. [5]Galluzzi L Vitale I Abrams JM Molecular definitions of cell death subroutines: recommendations of the Nomenclature Committee on Cell Death 2012 Cell Death Differ 2012 19 107 120 10.1038/cdd.2011.96 21760595 PMC3252826 · DOI · Paper page
  6. [6]Green DR Cell death and the immune system: getting to how and why Immunol Rev 2017 277 4 8 10.1111/imr.12553 28462522 · DOI
  7. [7]Weinlich R Oberst A Beere HM Green DR Necroptosis in development, inflammation and disease Nat Rev Mol Cell Biol 2016 18 127 136 10.1038/nrm.2016.149 27999438 · DOI · Paper page
  8. [8]Blander JM The many ways tissue phagocytes respond to dying cells Immunol Rev 2017 277 158 173 10.1111/imr.12537 28462530 PMC5721677 · DOI · Paper page
  9. [9]Wyllie AH Kerr JFR Currie AR Cell death: the significance of apoptosis Int Rev Cytol 1980 7014501
  10. [10]Silva MT Secondary necrosis: the natural outcome of the complete apoptotic program FEBS Lett 2010 584 4491 4499 10.1016/j.febslet.2010.10.046 20974143 · DOI
  11. [11]Garg AD Romano E Rufo N Agostinis P Immunogenic versus tolerogenic phagocytosis during anticancer therapy: mechanisms and clinical translation Cell Death Differ 2016 23 938 951 10.1038/cdd.2016.5 26891691 PMC4987738 · DOI
  12. [12]Mahajan A Herrmann M Muñoz LE Clearance deficiency and cell death pathways: a model for the pathogenesis of SLE Front Immunol 2016 7 35 10.3389/fimmu.2016.00035 26904025 PMC4745266 · DOI
  13. [14]Birge RB Boeltz S Kumar S Phosphatidylserine is a global immunosuppressive signal in efferocytosis, infectious disease, and cancer Cell Death Differ 2016 23 962 978 10.1038/cdd.2016.11 26915293 PMC4987730 · DOI
  14. [16]Lotze MT Zeh HJ Rubartelli A The grateful dead: damage-associated molecular pattern molecules and reduction/oxidation regulate immunity Immunol Rev 2007 220 60 81 10.1111/j.1600-065X.2007.00579.x 17979840 · DOI
  15. [17]Matzinger P Tolerance, danger, and the extended family Annu Rev Immunol 1994 12 991 1045 10.1146/annurev.iy.12.040194.005015 8011301 · DOI
  16. [18]Schaefer L Complexity of danger: the diverse nature of damage-associated molecular patterns J Biol Chem 2014 289 35237 35245 10.1074/jbc.R114.619304 25391648 PMC4271212 · DOI
  17. [19]Cocco RE Ucker DS Distinct modes of macrophage recognition for apoptotic and necrotic cells are not specified exclusively by phosphatidylserine exposure Mol Biol Cell 2001 12 919 930 10.1091/mbc.12.4.919 11294896 PMC32276 · DOI
  18. [20]Crawford ED Wells JA Caspase substrates and cellular remodeling Annu Rev Biochem 2011 80 1055 1087 10.1146/annurev-biochem-061809-121639 21456965 · DOI
  19. [21]Vanden Berghe T Vanlangenakker N Parthoens E Necroptosis, necrosis and secondary necrosis converge on similar cellular disintegration features Cell Death Differ 2010 17 922 930 10.1038/cdd.2009.184 20010783 · DOI · Paper page
  20. [22]Vanden Berghe T Grootjans S Goossens V Determination of apoptotic and necrotic cell death in vitro and in vivo Methods 2013 61 117 129 10.1016/j.ymeth.2013.02.011 23473780 · DOI
  21. [23]Krysko DV Vanden Berghe T D’Herde K Vandenabeele P Apoptosis and necrosis: detection, discrimination and phagocytosis Methods 2008 44 205 221 10.1016/j.ymeth.2007.12.001 18314051 · DOI
  22. [24]Tixeira R Caruso S Paone S Defining the morphologic features and products of cell disassembly during apoptosis Apoptosis 2017 22 475 477 10.1007/s10495-017-1345-7 28102458 · DOI
  23. [25]Wickman GR Julian L Mardilovich K Blebs produced by actin-myosin contraction during apoptosis release damage-associated molecular pattern proteins before secondary necrosis occurs Cell Death Differ 2013 20 1293 1305 10.1038/cdd.2013.69 23787996 PMC3770329 · DOI
  24. [26]Liang YY Rainprecht D Eichmair E Serum-dependent processing of late apoptotic cells and their immunogenicity Apoptosis 2015 20 1444 1456 10.1007/s10495-015-1163-8 26341352 · DOI
  25. [27]Krysko DV Denecker G Festjens N Macrophages use different internalization mechanisms to clear apoptotic and necrotic cells Cell Death Differ 2006 13 2011 2022 10.1038/sj.cdd.4401900 16628234 · DOI
  26. [28]Zeerleder S Zwart B te Velthuis H Nucleosome-releasing factor: a new role for factor VII-activating protease (FSAP) FASEB J 2008 22 4077 4084 10.1096/fj.08-110429 18753248 · DOI
  27. [29]Stephan F Marsman G Bakker LM Cooperation of factor VII–activating protease and serum DNase I in the release of nucleosomes from necrotic cells Arthritis Rheum. 2014 66 686 693 10.1002/art.38265 24574229 · DOI
  28. [30]Liang YY Arnold T Michlmayr A Serum-dependent processing of late apoptotic cells for enhanced efferocytosis Cell Death Dis 2014 PMC4047901 24874736
  29. [31]Nauta AJ Trouw LA Daha MR Direct binding of C1q to apoptotic cells and cell blebs induces complement activation Eur J Immunol 2002 32 1726 1736 10.1002/1521-4141(200206)32:6<1726::AID-IMMU1726>3.0.CO;2-R 12115656 · DOI
  30. [32]Fraser DA Laust AK Nelson EL Tenner AJ C1q differentially modulates phagocytosis and cytokine responses during ingestion of apoptotic cells by human monocytes, macrophages, and dendritic cells J Immunol 2009 183 6175 6185 10.4049/jimmunol.0902232 19864605 PMC2843563 · DOI
  31. [34]Napirei M Karsunky H Zevnik B Features of systemic lupus erythematosus in Dnase1-deficient mice Nat Genet 2000 25 177 181 10.1038/76032 10835632 · DOI
  32. [35]Clarke EV Weist BM Walsh CM Tenner AJ Complement protein C1q bound to apoptotic cells suppresses human macrophage and dendritic cell-mediated Th17 and Th1 T cell subset proliferation J Leukoc Biol 2015 97 147 160 10.1189/jlb.3A0614-278R 25381385 PMC4377823 · DOI
  33. [36]Maueröder C, Chaurio RA, Dumych T et al (2016) A blast without power – cell death induced by the tuberculosis-necrotizing toxin fails to elicit adequate immune responses. Cell Death Differ 1016–1025. doi:10.1038/cdd.2016.4 PMC4987737 26943324 · DOI
  34. [37]Urbonaviciute V Furnrohr BG Meister S Induction of inflammatory and immune responses by HMGB1-nucleosome complexes: implications for the pathogenesis of SLE J Exp Med 2008 205 3007 3018 10.1084/jem.20081165 19064698 PMC2605236 · DOI
  35. [38]Janko C Filipović M Munoz LE redox modulation of HMGB1-related signaling Antioxid Redox Signal 2014 20 1075 1085 10.1089/ars.2013.5179 23373897 PMC3928832 · DOI
  36. [39]Shi Y Evans JE Rock KL Molecular identification of a danger signal that alerts the immune system to dying cells Nature 2003 425 516 521 10.1038/nature01991 14520412 · DOI · Paper page
  37. [40]Lauber K Ernst A Orth M Dying cell clearance and its impact on the outcome of tumor radiotherapy Front Oncol 2012 22973558 PMC3438527
  38. [41]Popa-Nita O Naccache PH Crystal-induced neutrophil activation Immunol Cell Biol 2010 88 32 40 10.1038/icb.2009.98 19949421 · DOI
  39. [42]Martinon F Mechanisms of uric acid crystal-mediated autoinflammation Immunol Rev 2010 233 218 232 10.1111/j.0105-2896.2009.00860.x 20193002 · DOI
  40. [43]Galvan MD Foreman DB Zeng E Complement component C1q regulates macrophage expression of Mer tyrosine kinase to promote clearance of apoptotic cells J Immunol 2012 188 3716 3723 10.4049/jimmunol.1102920 22422887 PMC3324645 · DOI
  41. [44]Graham DK DeRyckere D Davies KD Earp HS The TAM family: phosphatidylserine-sensing receptor tyrosine kinases gone awry in cancer Nat Rev Cancer 2014 14 769 785 10.1038/nrc3847 25568918 · DOI
  42. [46]Martin M Leffler J Blom AM Annexin A2 and a5 serve as new ligands for c1q on apoptotic cells J Biol Chem 2012 287 33733 33744 10.1074/jbc.M112.341339 22879587 PMC3460470 · DOI
  43. [47]Cai Y Teo BHD Yeo JG Lu J C1q protein binds to the apoptotic nucleolus and causes C1 protease degradation of nucleolar proteins J Biol Chem 2015 290 22570 22580 10.1074/jbc.M115.670661 26231209 PMC4566231 · DOI
  44. [48]Molineros JE Maiti AK Sun C Admixture mapping in lupus identifies multiple functional variants within IFIH1 associated with apoptosis, inflammation, and autoantibody production PLoS Genet 2013 23441136 PMC3575474
  45. [49]Blume KE Soeroes S Waibel M Cell surface externalization of annexin A1 as a failsafe mechanism preventing inflammatory responses during secondary necrosis J Immunol 2009 183 8138 8147 10.4049/jimmunol.0902250 20007579 · DOI
  46. [50]Blume KE Soeroes S Keppeler H Cleavage of annexin A1 by ADAM10 during secondary necrosis generates a monocytic “find-me” signal J Immunol 2012 188 135 145 10.4049/jimmunol.1004073 22116825 · DOI
  47. [51]Bournazou I Pound JD Duffin R Apoptotic human cells inhibit migration of granulocytes via release of lactoferrin J Clin Invest 2009 119 20 32 19033648 PMC2613454
  48. [52]Huang Q Li F Liu X Caspase 3-mediated stimulation of tumor cell repopulation during cancer radiotherapy Nat Med 2011 17 860 866 10.1038/nm.2385 21725296 PMC3132290 · DOI · Paper page
  49. [53]Voss JJLP Ford CA Petrova S Modulation of macrophage antitumor potential by apoptotic lymphoma cells Cell Death Differ 2017 28157210 PMC5442466
  50. [54]Cayrol C Girard J-P The IL-1-like cytokine IL-33 is inactivated after maturation by caspase-1 Proc Natl Acad Sci USA 2009 106 9021 9026 10.1073/pnas.0812690106 19439663 PMC2690027 · DOI · Paper page
  51. [55]Adinolfi E Capece M Amoroso F Emerging roles of P2X receptors in cancer Curr Med Chem 2015 22 878 890 10.2174/0929867321666141012172913 25312206 · DOI
  52. [56]Krysko DV Garg AD Kaczmarek A Immunogenic cell death and DAMPs in cancer therapy Nat Rev Cancer 2012 12 860 875 10.1038/nrc3380 23151605 · DOI · Paper page
  53. [57]Young A Mittal D Stagg J Smyth MJ Targeting cancer-derived adenosine:new therapeutic approaches Cancer Discov 2014 4 879 888 10.1158/2159-8290.CD-14-0341 25035124 · DOI
  54. [58]Sciorati C Rigamonti E Manfredi AA Rovere-Querini P Cell death, clearance and immunity in the skeletal muscle Cell Death Differ 2016 23 927 937 10.1038/cdd.2015.171 26868912 PMC4987728 · DOI
  55. [59]Bosurgi L Manfredi AA Rovere-Querini P Macrophages in injured skeletal muscle:a perpetuum mobile causing and limiting fibrosis, prompting or restricting resolution and regeneration Front Immunol 2011 22566851 PMC3341990
  56. [61]Mevorach D Clearance of dying cells and systemic lupus erythematosus:the role of C1q and the complement system Apoptosis 2010 15 1114 1123 10.1007/s10495-010-0530-8 20683667 · DOI
  57. [62]Fernandez-Boyanapalli RF Falcone EL Zerbe CS Impaired efferocytosis in human chronic granulomatous disease is reversed by pioglitazone treatment J Allergy Clin Immunol 2015 136 1399-401-3 10.1016/j.jaci.2015.07.034 26386811 PMC4640967 · DOI
  58. [63]Manoussakis MN Fragoulis GE Vakrakou AG Moutsopoulos HM Impaired clearance of early apoptotic cells mediated by inhibitory IgG antibodies in patients with primary Sjögren’s syndrome PLoS ONE 2014 9 e112100 10.1371/journal.pone.0112100 25396412 PMC4232361 · DOI
  59. [64]Hamon R Homan CC Tran HB Zinc and zinc transporters in macrophages and their roles in efferocytosis in COPD PLoS ONE 2014 9 e110056 10.1371/journal.pone.0110056 25350745 PMC4211649 · DOI
  60. [65]Simpson JL Gibson PG Yang IA Impaired macrophage phagocytosis in non-eosinophilic asthma Clin Exp Allergy 2013 43 29 35 10.1111/j.1365-2222.2012.04075.x 23278878 · DOI
  61. [66]Liang YY, Schwarzinger I, Simonitsch-Klupp I et al (2017) Impaired efferocytosis by monocytes in multiple myeloma. Oncol Lett (in press) PMC6006325 29928429
  62. [67]Avagyan H Goldenson B Tse E Immune blood biomarkers of Alzheimer disease patients J Neuroimmunol 2009 210 67 72 10.1016/j.jneuroim.2009.02.015 19329192 · DOI
  63. [69]Cash JG Kuhel DG Basford JE Apolipoprotein E4 impairs macrophage efferocytosis and potentiates apoptosis by accelerating endoplasmic reticulum stress J Biol Chem 2012 287 27876 27884 10.1074/jbc.M112.377549 22730380 PMC3431692 · DOI
  64. [70]Fiala M Liu PT Espinosa-Jeffrey A Innate immunity and transcription of MGAT-III and Toll-like receptors in Alzheimer’s disease patients are improved by bisdemethoxycurcumin Proc Natl Acad Sci USA 2007 104 12849 12854 10.1073/pnas.0701267104 17652175 PMC1937555 · DOI
  65. [71]Casares N Pequignot MO Tesniere A Caspase-dependent immunogenicity of doxorubicin-induced tumor cell death J Exp Med 2005 202 1691 1701 10.1084/jem.20050915 16365148 PMC2212968 · DOI · Paper page
  66. [72]Obeid M Tesniere A Ghiringhelli F Calreticulin exposure dictates the immunogenicity of cancer cell death Nat Med 2007 13 54 61 10.1038/nm1523 17187072 · DOI · Paper page
  67. [73]Kepp O Senovilla L Vitale I Consensus guidelines for the detection of immunogenic cell death Oncoimmunology 2014 3 1 19 10.4161/21624011.2014.955691 PMC4292729 25941621 · DOI · Paper page
  68. [74]Poon IKH, Chiu Y-HH, Armstrong AJ et al (2014) Unexpected link between an antibiotic, pannexin channels and apoptosis. Nature 507:329–334. doi:10.1038/nature13147. http://www.nature.com/nature/journal/vaop/ncurrent/abs/nature13147.html#supplementary-information PMC4078991 24646995 · DOI
  69. [75]Faivre S Chan D Salinas R DNA strand breaks and apoptosis induced by oxaliplatin in cancer cells Biochem Pharmacol 2003 66 225 237 10.1016/S0006-2952(03)00260-0 12826265 · DOI
  70. [76]Aresvik DM Pettersen RD Abrahamsen TG Wright MS 5-fluorouracil-induced death of Jurkat T-Cells - a role for caspases and MCL-1 Anticancer Res 2010 30 3879 3887 21036698
  71. [77]Ferraro C Quemeneur L Fournel S The topoisomerase inhibitors camptothecin and etoposide induce a CD95-independent apoptosis of activated peripheral lymphocytes Cell Death Differ 2000 7 197 206 10.1038/sj.cdd.4400595 10713734 · DOI
  72. [78]Tesniere A Schlemmer F Boige V Immunogenic death of colon cancer cells treated with oxaliplatin Oncogene 2010 29 482 491 10.1038/onc.2009.356 19881547 · DOI
  73. [79]Krysko DV Vandenabeele P From regulation of dying cell engulfment to development of anti-cancer therapy Cell Death Differ 2008 15 29 38 10.1038/sj.cdd.4402271 18007662 · DOI
  74. [80]Crawford J Dale DC Lyman GH Chemotherapy-induced neutropenia: risks, consequences, and new directions for its management Cancer 2004 100 228 237 10.1002/cncr.11882 14716755 · DOI
  75. [81]Arnold T Michlmayr A Baumann S Plasma HMGB-1 after the initial dose of epirubicin/docetaxel in cancer Eur J Clin Invest 2013 43 286 291 10.1111/eci.12043 23410002 · DOI
  76. [82]Exner R Sachet M Arnold T Prognostic value of HMGB1 in early breast cancer patients under neoadjuvant chemotherapy Cancer Med 2016 5 2350 2358 10.1002/cam4.827 27457217 PMC5055166 · DOI
  77. [83]Stoetzer OJ Wittwer C Lehner J Circulating nucleosomes and biomarkers of immunogenic cell death as predictive and prognostic markers in cancer patients undergoing cytotoxic therapy Expert Opin Biol Ther 2012 12 S217 S224 10.1517/14712598.2012.689280 22620489 · DOI
  78. [84]Stoetzer OJ Fersching DMI Salat C Circulating immunogenic cell death biomarkers HMGB1 and RAGE in breast cancer patients during neoadjuvant chemotherapy Tumor Biol 2013 34 81 90 10.1007/s13277-012-0513-1 22983919 · DOI
  79. [85]Wittwer C Boeck S Heinemann V Circulating nucleosomes and immunogenic cell death markers HMGB1, sRAGE and DNAse in patients with advanced pancreatic cancer undergoing chemotherapy Int J Cancer 2013 133 2619 2630 23729200
  80. [86]Fahmueller YN Nagel D Hoffmann RT Immunogenic cell death biomarkers HMGB1, RAGE, and DNAse indicate response to radioembolization therapy and prognosis in colorectal cancer patients Int J Cancer 2013 132 2349 2358 10.1002/ijc.27894 23047645 · DOI
  81. [87]Kohles N, Nagel D, Jüngst D et al (2012) Predictive value of immunogenic cell death biomarkers HMGB1, sRAGE, and DNase in liver cancer patients receiving transarterial chemoembolization therapy. Tumor Biol 1–9. doi:10.1007/s13277-012-0504-2 22965881 · DOI
  82. [88]Farkona S Diamandis EP Blasutig IM Cancer immunotherapy: the beginning of the end of cancer? BMC Med 2016 14 73 10.1186/s12916-016-0623-5 27151159 PMC4858828 · DOI
  83. [89]Ott PA Hodi FS Kaufman HL Combination immunotherapy: a road map J Immunother Cancer 2017 5 16 10.1186/s40425-017-0218-5 28239469 PMC5319100 · DOI
  84. [90]Fehr EM Spoerl S Heyder P Apoptotic-cell-derived membrane vesicles induce an alternative maturation of human dendritic cells which is disturbed in SLE J Autoimmun 2013 40 86 95 10.1016/j.jaut.2012.08.003 23031801 · DOI
  85. [91]Penteado LDA Dejani NN Verdan FF Distinctive role of efferocytosis in dendritic cell maturation and migration in sterile or infectious conditions Immunology 2017 151 304 313 10.1111/imm.12731 28267881 PMC5461093 · DOI
  86. [92]Bachleitner-Hofmann T Friedl J Hassler M Pilot trial of autologous dendritic cells loaded with tumor lysate(s) from allogeneic tumor cell lines in patients with metastatic medullary thyroid carcinoma Oncol Rep 2009 21 1585 1592 10.3892/or_00000391 19424640 · DOI
  87. [93]Dubsky P Hayden H Sachet M Allogeneic tumor lysate can serve as both antigen source and protein supplementation for dendritic cell culture Cancer Immunol Immunother 2008 57 859 870 10.1007/s00262-007-0422-0 18030468 PMC11030753 · DOI
  88. [94]Beer L Mildner M Gyöngyösi M Ankersmit HJ Peripheral blood mononuclear cell secretome for tissue repair Apoptosis 2016 21 1336 1353 10.1007/s10495-016-1292-8 27696124 PMC5082595 · DOI
  89. [95]Richards CH Mohammed Z Qayyum T The prognostic value of histological tumor necrosis in solid organ malignant disease: a systematic review Future Oncol 2011 7 1223 1235 10.2217/fon.11.99 21992733 · DOI
  90. [96]Gkogkou C Frangia K Saif MW Necrosis and apoptotic index as prognostic factors in non-small cell lung carcinoma: a review Springerplus 2014 3 120 10.1186/2193-1801-3-120 24634811 PMC3951652 · DOI
  91. [97]Zhang X Chen L The recent progress of the mechanism and regulation of tumor necrosis in colorectal cancer J Cancer Res Clin Oncol 2016 142 453 463 10.1007/s00432-015-1997-z 26094047 PMC11819303 · DOI
  92. [98]Levin S Bucci TJ Cohen SM The nomenclature of cell death: recommendations of an ad hoc Committee of the Society of Toxicologic Pathologists Toxicol Pathol 1999 27 484 490 10.1177/019262339902700419 10485836 · DOI
  93. [99]Elmore SA Dixon D Hailey JR Recommendations from the INHAND Apoptosis/Necrosis Working Group Toxicol Pathol 2016 44 173 188 10.1177/0192623315625859 26879688 PMC4785073 · DOI
  94. [100]Banfalvi G Methods to detect apoptotic cell death Apoptosis 2017 22 306 323 10.1007/s10495-016-1333-3 28035493 · DOI
  95. [102]do Vale A Costa-Ramos C Silva A Systemic macrophage and neutrophil destruction by secondary necrosis induced by a bacterial exotoxin in a Gram-negative septicaemia Cell Microbiol 2007 9 988 1003 10.1111/j.1462-5822.2006.00846.x 17381431 · DOI
  96. [103]Hentze H Schwoebel F Lund S In vivo and in vitro evidence for extracellular caspase activity released from apoptotic cells Biochem Biophys Res Commun 2001 283 1111 1117 10.1006/bbrc.2001.4918 11355887 · DOI
  97. [104]Holdenrieder S Eichhorn P Beuers U Nucleosomal DNA fragments in autoimmune diseases Ann NY Acad Sci 2006 1075 318 327 10.1196/annals.1368.043 17108227 · DOI
  98. [105]Abbas AK Lichtman AH Pillai S Cellular and molecular immunology 2012 7 Philadelphia Elsevier

Authors
Sachet, M., Liang, Y. Y., & Oehler, R.
Affiliations
  • Comprehensive Cancer Center Vienna (AT)
  • Karolinska Institutet (SE)
Corresponding author
Oehler, Rudolf
Venue
Apoptosis
Published
2017-08-31
Volume
22
Issue
10
Pages
1189-1204
ISSN
  • 1360-8185 (ISSN-L)
  • 1573-675X
OpenAlex
W2753327319
Cited by
282
References
111
Citations by year
2026: 14 · 2025: 33 · 2024: 36 · 2023: 33 · 2022: 36 · 2021: 43 · 2020: 43 · 2019: 29 · 2018: 12 · 2017: 3
FWCI
2.44
Type
journal article
Language
en
Open access
Locations
  • APOPTOSIS (publishedVersion, cc-by)
  • Europe PMC (PubMed Central) (publishedVersion, cc-by)
  • PubMed Central (publishedVersion, cc-by)
  • PubMed (publishedVersion)
Funders
  • Universität Wien
  • Medizinische Universität Wien
Topics
  • Life Sciences › Immunology and Microbiology › Immunology › Immune Response and Inflammation
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Cell death mechanisms and regulation
  • Life Sciences › Immunology and Microbiology › Immunology › Phagocytosis and Immune Regulation
Keywords
secondary necrosis, efferocytosis, damage-associated molecular patterns, regulated necrosis, necroptosis, immune response, immunostimulatory molecules, cancer, neurodegenerative diseases, autoimmunity
MeSH terms
Alarmins, Animals, Humans, Immunotherapy, Inflammation, Necrosis, Phagocytosis, Signal Transduction, Cell Death, Apoptosis

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