Pathogen response-like recruitment and activation of neutrophils by sterile immunogenic dying cells drives neutrophil-mediated residual cell killing

Cell Death and Differentiation

Volumn 24, Issue 5, 2017, Pages 832-843

  Garg, Abhishek D ^a,b   Vandenberk, Lien ^c   Fang, Shentong ^b   Fasche, Tekele ^b   Van Eygen, Sofie ^a   Maes, Jan ^d   Van Woensel, Matthias ^e,f   Koks, Carolien ^c   Vanthillo, Niels ^d   Graf, Norbert ^g   De Witte, Peter ^d   Van Gool, Stefaan ^h   Salven, Petri ^b   Agostinis, Patrizia ^a  

^a LABORATORY OF MOLECULAR AND CELLULAR SIGNALING   (Belgium)

^b UNIVERSITY OF HELSINKI   (Finland)

^c UNIVERSITY OF LEUVEN   (Belgium)

^d DEPARTMENT OF PHARMACEUTICAL AND PHARMACOLOGICAL SCIENCES   (Belgium)

^e KU LEUVEN UNIVERSITY OF LEUVEN   (Belgium)

^f UNIVERSITÉ LIBRE DE BRUXELLES   (Belgium)

^g SAARLAND UNIVERSITY   (Germany)

^h Immunologisch Onkologisches Zentrum Koln IOZK   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE TRIPHOSPHATE; CALRETICULIN; CHEMOKINE; CXCL1 CHEMOKINE; GAMMA INTERFERON INDUCIBLE PROTEIN 10; HYDROGEN PEROXIDE; MONOCYTE CHEMOTACTIC PROTEIN 1; MYELOID DIFFERENTIATION FACTOR 88; NITRIC OXIDE; NUCLEIC ACID; PATHOGEN ASSOCIATED MOLECULAR PATTERN; PATHOGEN RESPONSE LIKE CHEMOKINE; PURINERGIC RECEPTOR; TOLL LIKE RECEPTOR; TOLL LIKE RECEPTOR 7; TOLL LIKE RECEPTOR 8; TOLL LIKE RECEPTOR 9; UNCLASSIFIED DRUG; BETA CHEMOKINE; CCL18 PROTEIN, HUMAN; TLR7 PROTEIN, HUMAN;

ANIMAL CELL; APOPTOSIS; ARTICLE; CANCER CELL; CELL KILLING; CONTROLLED STUDY; FEMALE; IMMUNOGENICITY; IN VIVO STUDY; INNATE IMMUNITY; LEUKOCYTE ACTIVATION; MALE; MOUSE; NEUTROPHIL; NEUTROPHIL CHEMOTAXIS; NONHUMAN; PATHOGENESIS; PHAGOCYTOSIS; PRIORITY JOURNAL; RESPIRATORY BURST; SIGNAL TRANSDUCTION; ZEBRA FISH; ANIMAL; C57BL MOUSE; COCULTURE; CYTOLOGY; CYTOTOXICITY; EPITHELIUM CELL; GENE EXPRESSION REGULATION; GENETICS; GLIA; HUMAN; IMMUNOLOGY; MELANOCYTE; PATHOLOGY; TRANSGENIC ANIMAL; TUMOR CELL LINE;

ANIMALS; ANIMALS, GENETICALLY MODIFIED; APOPTOSIS; CELL LINE, TUMOR; CHEMOKINE CCL2; CHEMOKINE CXCL1; CHEMOKINE CXCL10; CHEMOKINES, CC; COCULTURE TECHNIQUES; CYTOTOXICITY, IMMUNOLOGIC; EPITHELIAL CELLS; FEMALE; GENE EXPRESSION REGULATION; HUMANS; MALE; MELANOCYTES; MICE; MICE, INBRED C57BL; MYELOID DIFFERENTIATION FACTOR 88; NEUROGLIA; NEUTROPHILS; SIGNAL TRANSDUCTION; TOLL-LIKE RECEPTOR 7; ZEBRAFISH;

EID: 85013810275     PISSN: 13509047     EISSN: 14765403     Source Type: Journal    
DOI: 10.1038/cdd.2017.15     Document Type: Article

References (34)

1. Poon IK, Lucas CD, Rossi AG, Ravichandran KS. Apoptotic cell clearance: Basic biology and therapeutic potential. Nat Rev Immunol 2014; 14: 166-180.
2. Zitvogel L, Kepp O, Kroemer G. Decoding cell death signals in inflammation and immunity. Cell 2010; 140: 798-804.
3. Garg AD, Galluzzi L, Apetoh L, Baert T, Birge RB, Bravo-San Pedro JM, et al. Molecular and translational classifications of DAMPs in immunogenic cell death. Front Immunol 2015; 6: 588.
4. Medzhitov R, Janeway CA Jr. Decoding the patterns of self and nonself by the innate immune system. Science 2002; 296: 298-300.
5. Matzinger P. The danger model: A renewed sense of self. Science 2002; 296: 301-305.
6. Jozefowski S. The danger model: Questioning an unconvincing theory. Immunol Cell Biol 2016; 94: 164-168.
7. Chen CJ, Kono H, Golenbock D, Reed G, Akira S, Rock KL. Identification of a key pathway required for the sterile inflammatory response triggered by dying cells. Nat Med 2007; 13: 851-856.
8. Kepp O, Senovilla L, Vitale I, Vacchelli E, Adjemian S, Agostinis P, et al. Consensus guidelines for the detection of immunogenic cell death. Oncoimmunology 2014; 3: E955691.
9. Garg AD, Vandenberk L, Koks C, Verschuere T, Boon L, Van Gool SW, et al. Dendritic cell vaccines based on immunogenic cell death elicit danger signals and T cell-driven rejection of high-grade glioma. Sci Transl Med 2016; 8: 328ra327.
10. Aaes TL, Kaczmarek A, Delvaeye T, De Craene B, De Koker S, Heyndrickx L, et al. Vaccination with necroptotic cancer cells induces efficient anti-tumor immunity. Cell Rep 2016; 15: 274-287.
11. Janeway C. Immunobiology: The Immune System in Health and Disease, 6th edn. Garland Science: New York, USA, 2005.
12. Kolaczkowska E, Kubes P. Neutrophil recruitment and function in health and inflammation. Nat Rev Immunol 2013; 13: 159-175.
13. Moser B, Wolf M, Walz A, Loetscher P. Chemokines: Multiple levels of leukocyte migration control. Trends Immunol 2004; 25: 75-84.
14. Miest TS, Cattaneo R. New viruses for cancer therapy: Meeting clinical needs. Nat Rev Microbiol 2014; 12: 23-34.
15. Garg AD, Krysko DV, Verfaillie T, Kaczmarek A, Ferreira GB, Marysael T, et al. A novel pathway combining calreticulin exposure and ATP secretion in immunogenic cancer cell death. EMBO J 2012; 31: 1062-1079.
16. Obeid M, Tesniere A, Ghiringhelli F, Fimia GM, Apetoh L, Perfettini JL, et al. Calreticulin exposure dictates the immunogenicity of cancer cell death. Nat Med 2007; 13: 54-61.
17. Garg AD, Elsen S, Krysko DV, Vandenabeele P, de Witte P, Agostinis P. Resistance to anticancer vaccination effect is controlled by a cancer cell-autonomous phenotype that disrupts immunogenic phagocytic removal. Oncotarget 2015; 6: 26841-26860.
18. Casares N, Pequignot MO, Tesniere A, Ghiringhelli F, Roux S, Chaput N, et al. Caspasedependent immunogenicity of doxorubicin-induced tumor cell death. J Exp Med 2005; 202: 1691-1701.
19. Koks CA, Garg AD, Ehrhardt M, Riva M, Vandenberk L, Boon L, et al. Newcastle disease virotherapy induces long-term survival and tumor-specific immune memory in orthotopic glioma through the induction of immunogenic cell death. Int J Cancer 2015; 136: E313-E325.
20. Elliott MR, Chekeni FB, Trampont PC, Lazarowski ER, Kadl A, Walk SF, et al. Nucleotides released by apoptotic cells act as a find-me signal to promote phagocytic clearance. Nature 2009; 461: 282-286.
21. DeVries ME, Kelvin AA, Xu L, Ran L, Robinson J, Kelvin DJ. Defining the origins and evolution of the chemokine/chemokine receptor system. J Immunol 2006; 176: 401-415.
22. Gray C, Loynes CA, Whyte MK, Crossman DC, Renshaw SA, Chico TJ. Simultaneous intravital imaging of macrophage and neutrophil behaviour during inflammation using a novel transgenic zebrafish. Thromb Haemost 2011; 105: 811-819.
23. Cambier CJ, Takaki KK, Larson RP, Hernandez RE, Tobin DM, Urdahl KB, et al. Mycobacteria manipulate macrophage recruitment through coordinated use of membrane lipids. Nature 2014; 505: 218-222.
24. 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.
25. Sistigu A, Yamazaki T, Vacchelli E, Chaba K, Enot DP, Adam J, et al. Cancer cellautonomous contribution of type I interferon signaling to the efficacy of chemotherapy. Nat Med 2014; 20: 1301-1309.
26. de Oliveira S, Rosowski EE, Huttenlocher A. Neutrophil migration in infection and wound repair: Going forward in reverse. Nat Rev Immunol 2016; 16: 378-391.
27. Thompson AJ, Locarnini SA. Toll-like receptors, RIG-I-like RNA helicases and the antiviral innate immune response. Immunol Cell Biol 2007; 85: 435-445.
28. Chiba S, Baghdadi M, Akiba H, Yoshiyama H, Kinoshita I, Dosaka-Akita H, et al. Tumorinfiltrating DCs suppress nucleic acid-mediated innate immune responses through interactions between the receptor TIM-3 and the alarmin HMGB1. Nat Immunol 2012; 13: 832-842.
29. Krysko DV, Kaczmarek A, Krysko O, Heyndrickx L, Woznicki J, Bogaert P, et al. TLR-2 and TLR-9 are sensors of apoptosis in a mouse model of doxorubicin-induced acute inflammation. Cell Death Differ 2011; 18: 1316-1325.
30. Granot Z, Henke E, Comen EA, King TA, Norton L, Benezra R. Tumor entrained neutrophils inhibit seeding in the premetastatic lung. Cancer Cell 2011; 20: 300-314.
31. Finisguerra V, Di Conza G, Di Matteo M, Serneels J, Costa S, Thompson AA, et al. MET is required for the recruitment of anti-tumoural neutrophils. Nature 2015; 522: 349-353.
32. Torraca V, Cui C, Boland R, Bebelman JP, van der Sar AM, Smit MJ, et al. The CXCR3-CXCL11 signaling axis mediates macrophage recruitment and dissemination of mycobacterial infection. Dis Model Mech 2015; 8: 253-269.
33. Vandenberk L, Garg AD, Verschuere T, Koks C, Belmans J, Beullens M, et al. Irradiation of necrotic cancer cells, employed for pulsing dendritic cells (DCs), potentiates DC vaccineinduced antitumor immunity against high-grade glioma. Oncoimmunology 2016; 5: E1083669.
34. Alkassar M, Gartner B, Roemer K, Graesser F, Rommelaere J, Kaestner L, et al. The combined effects of oncolytic reovirus plus Newcastle disease virus and reovirus plus parvovirus on U87 and U373 cells in vitro and in vivo. J Neurooncol 2011; 104: 715-727.