The PERKs of damage-associated molecular patterns mediating cancer immunogenicity: From sensor to the plasma membrane and beyond

Seminars in Cancer Biology

Volumn 33, Issue , 2015, Pages 74-85

  van Vliet, A R ^a   Martin, S ^a   Garg, A D ^a   Agostinis, P ^a  

^a LABORATORY OF MOLECULAR AND CELLULAR SIGNALING   (Belgium)

Author keywords

Cancer; Damage associated molecular patterns; ER stress; Immunogenic cell death; Trafficking pathways

Indexed keywords

ACTIVATING TRANSCRIPTION FACTOR 6; ADENOSINE TRIPHOSPHATE; BLEOMYCIN; BORTEZOMIB; CALRETICULIN; CHAPERONE; CHEMOKINE RECEPTOR CXCR1; CYCLOPHOSPHAMIDE; DOXORUBICIN; EPIRUBICIN; EPOTHILONE B; GAMMA INTERFERON; HEAT SHOCK PROTEIN 70; HEAT SHOCK PROTEIN 90; HIGH MOBILITY GROUP B1 PROTEIN; INITIATION FACTOR 2ALPHA; INOSITOL REQUIRING ENZYME 1; INTERLEUKIN 17; INTERLEUKIN 8; MITOXANTRONE; ONCOLYTIC VIRUS; OXALIPLATIN; OXYGEN REGULATED PROTEIN 150; PROTEIN KINASE R; PROTEIN KINASE R LIKE ENDOPLASMIC RETICULUM KINASE; SHIKONIN; TUMOR NECROSIS FACTOR RECEPTOR ASSOCIATED FACTOR 2; UNCLASSIFIED DRUG; VORINOSTAT; WOGONIN; CALCIUM; CALRETICULIN, HUMAN; REACTIVE OXYGEN METABOLITE;

ANTIGEN PRESENTATION; ANTIGEN PRESENTING CELL; ANTITUMOR GENE; AUTOPHAGY; CALCIUM SIGNALING; CALCIUM TRANSPORT; CANCER GROWTH; CD4+ T LYMPHOCYTE; CELL DEATH; CELL MEMBRANE; CELL SELECTION; ENDOPLASMIC RETICULUM ASSOCIATED DEGRADATION; ENDOPLASMIC RETICULUM STRESS; EXOCYTOSIS; HUMAN; IMMUNOGENICITY; IMMUNOMODULATION; IMMUNOSTIMULATION; LIVER CARCINOGENESIS; OXIDATION REDUCTION REACTION; PHAGOCYTOSIS; PHOTODYNAMIC THERAPY; PROTEIN DEGRADATION; PROTEIN HOMEOSTASIS; PROTEIN PHOSPHORYLATION; REVIEW; SIGNAL TRANSDUCTION; TUMOR IMMUNITY; UNFOLDED PROTEIN RESPONSE; VIROTHERAPY; ANIMAL; APOPTOSIS; ENDOPLASMIC RETICULUM; IMMUNOLOGY; INFLAMMATION; METABOLISM; NEOPLASMS; OXIDATIVE STRESS; PATHOLOGY;

ADENOSINE TRIPHOSPHATE; ANIMALS; APOPTOSIS; CALCIUM; CALRETICULIN; CELL MEMBRANE; ENDOPLASMIC RETICULUM; ENDOPLASMIC RETICULUM STRESS; HUMANS; INFLAMMATION; MOLECULAR CHAPERONES; NEOPLASMS; OXIDATION-REDUCTION; OXIDATIVE STRESS; REACTIVE OXYGEN SPECIES; SIGNAL TRANSDUCTION; UNFOLDED PROTEIN RESPONSE;

EID: 84938215240     PISSN: 1044579X     EISSN: 10963650     Source Type: Journal    
DOI: 10.1016/j.semcancer.2015.03.010     Document Type: Review

References (141)

1. Ron D., Walter P. Signal integration in the endoplasmic reticulum unfolded protein response. Nat Rev Mol Cell Biol 2007, 8:519-529.
2. Harding H.P., Zhang Y., Ron D. Protein translation and folding are coupled by an endoplasmic-reticulum-resident kinase. Nature 1999, 397:271-274.
3. Schroder M., Kaufman R.J. The mammalian unfolded protein response. Annu Rev Biochem 2005, 74:739-789.
4. Han J., Back S.H., Hur J., Lin Y.H., Gildersleeve R., Shan J., et al. ER-stress-induced transcriptional regulation increases protein synthesis leading to cell death. Nat Cell Biol 2013, 15:481-490.
5. Szegezdi E., Logue S.E., Gorman A.M., Samali A. Mediators of endoplasmic reticulum stress-induced apoptosis. EMBO Rep 2006, 7:880-885.
6. Sano R., Reed J.C. ER stress-induced cell death mechanisms. Biochim Biophys Acta 2013, 1833:3460-3470.
7. Urra H., Dufey E., Lisbona F., Rojas-Rivera D., Hetz C. When ER stress reaches a dead end. Biochim Biophys Acta 2013, 1833:3507-3517.
8. Urano F., Wang X., Bertolotti A., Zhang Y., Chung P., Harding H.P., et al. Coupling of stress in the ER to activation of JNK protein kinases by transmembrane protein kinase IRE1. Science 2000, 287:664-666.
9. Verfaillie T., Rubio N., Garg A.D., Bultynck G., Rizzuto R., Decuypere J.P., et al. PERK is required at the ER-mitochondrial contact sites to convey apoptosis after ROS-based ER stress. Cell Death Differ 2012, 19:1880-1891.
10. Yoneda T., Imaizumi K., Oono K., Yui D., Gomi F., Katayama T., et al. Activation of caspase-12, an endoplastic reticulum (ER) resident caspase, through tumor necrosis factor receptor-associated factor 2-dependent mechanism in response to the ER stress. J Biol Chem 2001, 276:13935-13940.
11. Xu C., Bailly-Maitre B., Reed J.C. Endoplasmic reticulum stress: cell life and death decisions. J Clin Invest 2005, 115:2656-2664.
12. Kim I., Xu W., Reed J.C. Cell death and endoplasmic reticulum stress: disease relevance and therapeutic opportunities. Nat Rev Drug Discov 2008, 7:1013-1030.
13. Rao R.V., Ellerby H.M., Bredesen D.E. Coupling endoplasmic reticulum stress to the cell death program. Cell Death Differ 2004, 11:372-380.
14. Dejeans N., Manie S., Hetz C., Bard F., Hupp T., Agostinis P., et al. Addicted to secrete - novel concepts and targets in cancer therapy. Trends Mol Med 2014, 20:242-250.
15. Garg A.D., Krysko D.V., Verfaillie T., Kaczmarek A., Ferreira G.B., 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. Luo B., Lee A.S. The critical roles of endoplasmic reticulum chaperones and unfolded protein response in tumorigenesis and anticancer therapies. Oncogene 2013, 32:805-818.
17. Nakagawa H., Umemura A., Taniguchi K., Font-Burgada J., Dhar D., Ogata H., et al. ER stress cooperates with hypernutrition to trigger TNF-dependent spontaneous HCC development. Cancer Cell 2014, 26:331-343.
18. Kroemer G., Galluzzi L., Kepp O., Zitvogel L. Immunogenic cell death in cancer therapy. Annu Rev Immunol 2013, 31:51-72.
19. Begovic M., Herberman R., Gorelik E. Increase in immunogenicity and sensitivity to natural cell-mediated cytotoxicity following in vitro exposure of MCA105 tumor cells to ultraviolet radiation. Cancer Res 1991, 51:5153-5159.
20. Chang C.L., Hsu Y.T., Wu C.C., Yang Y.C., Wang C., Wu T.C., et al. Immune mechanism of the antitumor effects generated by bortezomib. J Immunol 2012, 189:3209-3220.
21. Ma Y., Conforti R., Aymeric L., Locher C., Kepp O., Kroemer G., et al. How to improve the immunogenicity of chemotherapy and radiotherapy. Cancer Metastasis Rev 2011, 30:71-82.
22. West A.C., Mattarollo S.R., Shortt J., Cluse L.A., Christiansen A.J., Smyth M.J., et al. An intact immune system is required for the anticancer activities of histone deacetylase inhibitors. Cancer Res 2013, 73:7265-7276.
23. Garg A.D., Martin S., Golab J., Agostinis P. Danger signalling during cancer cell death: origins, plasticity and regulation. Cell Death Differ 2014, 21:26-38.
24. Matzinger P. Tolerance, danger, and the extended family. Annu Rev Immunol 1994, 12:991-1045.
25. Koks C., Garg A.D., 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 2014, 10.1002/ijc.29202.
26. Pawaria S., Binder R.J. CD91-dependent programming of T-helper cell responses following heat shock protein immunization. Nat Commun 2011, 2:521.
27. Panaretakis T., Kepp O., Brockmeier U., Tesniere A., Bjorklund A.C., Chapman D.C., et al. Mechanisms of pre-apoptotic calreticulin exposure in immunogenic cell death. EMBO J 2009, 28:578-590.
28. Martins I., Wang Y., Michaud M., Ma Y., Sukkurwala A.Q., Shen S., et al. Molecular mechanisms of ATP secretion during immunogenic cell death. Cell Death Differ 2014, 21:79-91.
29. Apetoh L., Ghiringhelli F., Tesniere A., Criollo A., Ortiz C., Lidereau R., et al. The interaction between HMGB1 and TLR4 dictates the outcome of anticancer chemotherapy and radiotherapy. Immunol Rev 2007, 220:47-59.
30. Spisek R., Charalambous A., Mazumder A., Vesole D.H., Jagannath S., Dhodapkar M.V. Bortezomib enhances dendritic cell (DC)-mediated induction of immunity to human myeloma via exposure of cell surface heat shock protein 90 on dying tumor cells: therapeutic implications. Blood 2007, 109:4839-4845.
31. Dudek-Peric A.M., Ferreira G.B., Muchowicz A., Wouters J., Prada N., Matrin S., et al. Anti-tumor immunity triggered by melphalan is potentiated by melanoma cell surface associated calreticulin. Cancer Res 2015, 75(8):1603-1614. 10.1158/0008-5472.
32. Martin S., Dudek-Peric A.M., Maes H., Garg A.D., Gabrysiak M., Demirsoy S., et al. Concurrent MEK and autophagy inhibition is required to restore cell death associated danger-signalling in Vemurafenib-resistant melanoma cells. Biochem Pharmacol 2015, 93:290-304.
33. Garg A.D., Dudek A.M., Ferreira G.B., Verfaillie T., Vandenabeele P., Krysko D.V., et al. ROS-induced autophagy in cancer cells assists in evasion from determinants of immunogenic cell death. Autophagy 2013, 9:1292-1307.
34. Zitvogel L., Kepp O., Senovilla L., Menger L., Chaput N., Kroemer G. Immunogenic tumor cell death for optimal anticancer therapy: the calreticulin exposure pathway. Clin Cancer Res 2010, 16:3100-3104.
35. Udono H., Levey D.L., Srivastava P.K. Cellular requirements for tumor-specific immunity elicited by heat shock proteins: tumor rejection antigen gp96 primes CD8+ T cells in vivo. Proc Natl Acad Sci U S A 1994, 91:3077-3081.
36. Berwin B., Reed R.C., Nicchitta C.V. Virally induced lytic cell death elicits the release of immunogenic GRP94/gp96. J Biol Chem 2001, 276:21083-21088.
37. Wang H., Pezeshki A.M., Yu X., Guo C., Subjeck J.R., Wang X.Y. The endoplasmic reticulum chaperone GRP170: from immunobiology to cancer therapeutics. Front Oncol 2014, 4:377.
38. Zhang Y., Liu R., Ni M., Gill P., Lee A.S. Cell surface relocalization of the endoplasmic reticulum chaperone and unfolded protein response regulator GRP78/BiP. J Biol Chem 2010, 285:15065-15075.
39. Rondas D., Crevecoeur I., D'Hertog W., Ferreira G.B., Staes A., Garg A.D., et al. Citrullinated glucose-regulated protein 78 is an autoantigen in type 1 diabetes. Diabetes 2014, 10.2337/db14-0621.
40. Garg A.D., Krysko D.V., Vandenabeele P., Agostinis P. Hypericin-based photodynamic therapy induces surface exposure of damage-associated molecular patterns like HSP70 and calreticulin. Cancer Immunol Immunother 2012, 61:215-221.
41. Madeo F., Durchschlag M., Kepp O., Panaretakis T., Zitvogel L., Frohlich K.U., et al. Phylogenetic conservation of the preapoptotic calreticulin exposure pathway from yeast to mammals. Cell Cycle 2009, 8:639-642.
42. Nakamura M., Moriya M., Baba T., Michikawa Y., Yamanobe T., Arai K., et al. An endoplasmic reticulum protein, calreticulin, is transported into the acrosome of rat sperm. Exp Cell Res 1993, 205:101-110.
43. Park B.J., Lee D.G., Yu J.R., Jung S.K., Choi K., Lee J., et al. Calreticulin, a calcium-binding molecular chaperone, is required for stress response and fertility in Caenorhabditis elegans. Mol Biol Cell 2001, 12:2835-2845.
44. Sukkurwala A.Q., Martins I., Wang Y., Schlemmer F., Ruckenstuhl C., Durchschlag M., et al. Immunogenic calreticulin exposure occurs through a phylogenetically conserved stress pathway involving the chemokine CXCL8. Cell Death Differ 2014, 21:59-68.
45. Tutuncu L., Stein P., Ord T.S., Jorgez C.J., Williams C.J. Calreticulin on the mouse egg surface mediates transmembrane signaling linked to cell cycle resumption. Dev Biol 2004, 270:246-260.
46. Raghavan M., Wijeyesakere S.J., Peters L.R., Del Cid N. Calreticulin in the immune system: ins and outs. Trends Immunol 2013, 34:13-21.
47. Garcia M.A., Gil J., Ventoso I., Guerra S., Domingo E., Rivas C., et al. Impact of protein kinase PKR in cell biology: from antiviral to antiproliferative action. Microbiol Mol Biol Rev 2006, 70:1032-1060.
48. Kaufman R.J., Scheuner D., Schroder M., Shen X., Lee K., Liu C.Y., et al. The unfolded protein response in nutrient sensing and differentiation. Nat Rev Mol Cell Biol 2002, 3:411-421.
49. Duewell P., Steger A., Lohr H., Bourhis H., Hoelz H., Kirchleitner S.V., et al. RIG-I-like helicases induce immunogenic cell death of pancreatic cancer cells and sensitize tumors toward killing by CD8T cells. Cell Death Differ 2014, 21(12):1825-1837. 10.1038/cdd.2014.96.
50. Li H., Liu L., Xing D., Chen W.R. Inhibition of the JNK/Bim pathway by Hsp70 prevents Bax activation in UV-induced apoptosis. FEBS Lett 2010, 584:4672-4678.
51. Li M., Wang J., Jing J., Hua H., Luo T., Xu L., et al. Synergistic promotion of breast cancer cells death by targeting molecular chaperone GRP78 and heat shock protein 70. J Cell Mol Med 2009, 13:4540-4550.
52. Marcu M.G., Doyle M., Bertolotti A., Ron D., Hendershot L., Neckers L. Heat shock protein 90 modulates the unfolded protein response by stabilizing IRE1alpha. Mol Cell Biol 2002, 22:8506-8513.
53. Hiramatsu N., Joseph V.T., Lin J.H. Monitoring and manipulating mammalian unfolded protein response. Methods Enzymol 2011, 491:183-198.
54. Park M.A., Curiel D.T., Koumenis C., Graf M., Chen C.S., Fisher P.B., et al. PERK-dependent regulation of HSP70 expression and the regulation of autophagy. Autophagy 2008, 4:364-367.
55. Hartl F.U., Bracher A., Hayer-Hartl M. Molecular chaperones in protein folding and proteostasis. Nature 2011, 475:324-332.
56. Udono H., Srivastava P.K. Comparison of tumor-specific immunogenicities of stress-induced proteins gp96, hsp90, and hsp70. J Immunol 1994, 152:5398-5403.
57. Udono H., Srivastava P.K. Heat shock protein 70-associated peptides elicit specific cancer immunity. J Exp Med 1993, 178:1391-1396.
58. Ishii T., Udono H., Yamano T., Ohta H., Uenaka A., Ono T., et al. Isolation of MHC class I-restricted tumor antigen peptide and its precursors associated with heat shock proteins hsp70, hsp90, and gp96. J Immunol 1999, 162:1303-1309.
59. Howe C., Garstka M., Al-Balushi M., Ghanem E., Antoniou A.N., Fritzsche S., et al. Calreticulin-dependent recycling in the early secretory pathway mediates optimal peptide loading of MHC class I molecules. EMBO J 2009, 28:3730-3744.
60. Ma Y., Hendershot L.M. ER chaperone functions during normal and stress conditions. J Chem Neuroanat 2004, 28:51-65.
61. Papp E., Nardai G., Soti C., Csermely P. Molecular chaperones, stress proteins and redox homeostasis. Biofactors 2003, 17:249-257.
62. Seong S.Y., Matzinger P. Hydrophobicity: an ancient damage-associated molecular pattern that initiates innate immune responses. Nat Rev Immunol 2004, 4:469-478.
63. Garg A.D., Krysko D.V., Vandenabeele P., Agostinis P. DAMPs and PDT-mediated photo-oxidative stress: exploring the unknown. Photochem Photobiol Sci 2011, 10:670-680.
64. Carta S., Castellani P., Delfino L., Tassi S., Vene R., Rubartelli A. DAMPs and inflammatory processes: the role of redox in the different outcomes. J Leukoc Biol 2009, 86:549-555.
65. Li G., Tang D., Lotze M.T. Menage a trois in stress: DAMPs, redox and autophagy. Semin Cancer Biol 2013, 23:380-390.
66. 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.
67. Capitani M., Sallese M. The KDEL receptor: new functions for an old protein. FEBS Lett 2009, 583:3863-3871.
68. Gupta S., McGrath B., Cavener D.R. PERK (EIF2AK3) regulates proinsulin trafficking and quality control in the secretory pathway. Diabetes 2010, 59:1937-1947.
69. Lemus L., Goder V. Regulation of endoplasmic reticulum-associated protein degradation (ERAD) by ubiquitin. Cells 2014, 3:824-847.
70. Williams D.B. Beyond lectins: the calnexin/calreticulin chaperone system of the endoplasmic reticulum. J Cell Sci 2006, 119:615-623.
71. Park S.H., Bolender N., Eisele F., Kostova Z., Takeuchi J., Coffino P., et al. The cytoplasmic Hsp70 chaperone machinery subjects misfolded and endoplasmic reticulum import-incompetent proteins to degradation via the ubiquitin-proteasome system. Mol Biol Cell 2007, 18:153-165.
72. Saibil H. Chaperone machines for protein folding, unfolding and disaggregation. Nat Rev Mol Cell Biol 2013, 14:630-642.
73. Donnelly B.F., Needham P.G., Snyder A.C., Roy A., Khadem S., Brodsky J.L., et al. Hsp70 and Hsp90 multichaperone complexes sequentially regulate thiazide-sensitive cotransporter endoplasmic reticulum-associated degradation and biogenesis. J Biol Chem 2013, 288:13124-13135.
74. Smalle J., Vierstra R.D. The ubiquitin 26S proteasome proteolytic pathway. Annu Rev Plant Biol 2004, 55:555-590.
75. Urbe S. Ubiquitin and endocytic protein sorting. Essays Biochem 2005, 41:81-98.
76. Yao T.P. The role of ubiquitin in autophagy-dependent protein aggregate processing. Genes Cancer 2010, 1:779-786.
77. Baou M., Kohlhaas S.L., Butterworth M., Vogler M., Dinsdale D., Walewska R., et al. Role of NOXA and its ubiquitination in proteasome inhibitor-induced apoptosis in chronic lymphocytic leukemia cells. Haematologica 2010, 95:1510-1518.
78. Ding W.X., Ni H.M., Chen X., Yu J., Zhang L., Yin X.M. A coordinated action of Bax, PUMA, and p53 promotes MG132-induced mitochondria activation and apoptosis in colon cancer cells. Mol Cancer Ther 2007, 6:1062-1069.
79. Befani C.D., Vlachostergios P.J., Hatzidaki E., Patrikidou A., Bonanou S., Simos G., et al. Bortezomib represses HIF-1alpha protein expression and nuclear accumulation by inhibiting both PI3K/Akt/TOR and MAPK pathways in prostate cancer cells. J Mol Med (Berl.) 2012, 90:45-54.
80. Zhou J., Schmid T., Brune B. Tumor necrosis factor-alpha causes accumulation of a ubiquitinated form of hypoxia inducible factor-1alpha through a nuclear factor-kappaB-dependent pathway. Mol Biol Cell 2003, 14:2216-2225.
81. McDade T.P., Perugini R.A., Vittimberga F.J., Callery M.P. Ubiquitin-proteasome inhibition enhances apoptosis of human pancreatic cancer cells. Surgery 1999, 126:371-377.
82. Li C., Chen S., Yue P., Deng X., Lonial S., Khuri F.R., et al. Proteasome inhibitor PS-341 (bortezomib) induces calpain-dependent IkappaB(alpha) degradation. J Biol Chem 2010, 285:16096-16104.
83. Yeung B.H., Huang D.C., Sinicrope F.A. PS-341 (bortezomib) induces lysosomal cathepsin B release and a caspase-2-dependent mitochondrial permeabilization and apoptosis in human pancreatic cancer cells. J Biol Chem 2006, 281:11923-11932.
84. Tsubuki S., Saito Y., Tomioka M., Ito H., Kawashima S. Differential inhibition of calpain and proteasome activities by peptidyl aldehydes of di-leucine and tri-leucine. J Biochem 1996, 119:572-576.
85. Kadlcikova J., Holecek M., Safranek R., Tilser I., Kessler B.M. Effects of proteasome inhibitors MG132, ZL3VS and AdaAhx3L3VS on protein metabolism in septic rats. Int J Exp Pathol 2004, 85:365-371.
86. Satpute-Krishnan P., Ajinkya M., Bhat S., Itakura E., Hegde R.S., Lippincott-Schwartz J. ER stress-induced clearance of misfolded GPI-anchored proteins via the secretory pathway. Cell 2014, 158:522-533.
87. Ghiran I., Klickstein L.B., Nicholson-Weller A. Calreticulin is at the surface of circulating neutrophils and uses CD59 as an adaptor molecule. J Biol Chem 2003, 278:21024-21031.
88. Hochstrasser M. Ubiquitin and intracellular protein degradation. Curr Opin Cell Biol 1992, 4:1024-1031.
89. Piper R.C., Dikic I., Lukacs G.L. Ubiquitin-dependent sorting in endocytosis. Cold Spring Harb Perspect Biol 2014, 6.
90. Rastogi N., Mishra D.P. Therapeutic targeting of cancer cell cycle using proteasome inhibitors. Cell Div 2012, 7:26.
91. Juhasz K., Lipp A.M., Nimmervoll B., Sonnleitner A., Hesse J., Haselgruebler T., et al. The complex function of hsp70 in metastatic cancer. Cancers (Basel) 2013, 6:42-66.
92. Mambula S.S., Calderwood S.K. Heat shock protein 70 is secreted from tumor cells by a nonclassical pathway involving lysosomal endosomes. J Immunol 2006, 177:7849-7857.
93. Nylandsted J., Jaattela M. Heat shock protein 70: an important survival factor for cancer cells. Ugeskr Laeger 2004, 166:3184-3186.
94. Evdonin A.L., Martynova M.G., Bystrova O.A., Guzhova I.V., Margulis B.A., Medvedeva N.D. The release of Hsp70 from A431 carcinoma cells is mediated by secretory-like granules. Eur J Cell Biol 2006, 85:443-455.
95. Vega V.L., Rodriguez-Silva M., Frey T., Gehrmann M., Diaz J.C., Steinem C., et al. Hsp70 translocates into the plasma membrane after stress and is released into the extracellular environment in a membrane-associated form that activates macrophages. J Immunol 2008, 180:4299-4307.
96. Fucikova J., Kralikova P., Fialova A., Brtnicky T., Rob L., Bartunkova J., et al. Human tumor cells killed by anthracyclines induce a tumor-specific immune response. Cancer Res 2011, 71:4821-4833.
97. Andrei C., Dazzi C., Lotti L., Torrisi M.R., Chimini G., Rubartelli A. The secretory route of the leaderless protein interleukin 1beta involves exocytosis of endolysosome-related vesicles. Mol Biol Cell 1999, 10:1463-1475.
98. Cattaneo M., Lotti L.V., Martino S., Alessio M., Conti A., Bachi A., et al. Secretion of novel SEL1L endogenous variants is promoted by ER stress/UPR via endosomes and shed vesicles in human cancer cells. PLoS ONE 2011, 6:e17206.
99. Yang C., Robbins P.D. The roles of tumor-derived exosomes in cancer pathogenesis. Clin Dev Immunol 2011, 2011:842849.
100. Schmid T.E., Multhoff G. Radiation-induced stress proteins - the role of heat shock proteins (HSP) in anti-tumor responses. Curr Med Chem 2012, 19:1765-1770.
101. Suh D.H., Kim M.K., Kim H.S., Chung H.H., Song Y.S. Unfolded protein response to autophagy as a promising druggable target for anticancer therapy. Ann N Y Acad Sci 2012, 1271:20-32.
102. Wang J., Kang R., Huang H., Xi X., Wang B., Wang J., et al. Hepatitis C virus core protein activates autophagy through EIF2AK3 and ATF6 UPR pathway-mediated MAP1LC3B and ATG12 expression. Autophagy 2014, 10:766-784.
103. Mizushima N., Komatsu M. Autophagy: renovation of cells and tissues. Cell 2011, 147:728-741.
104. Rubinsztein D.C., Codogno P., Levine B. Autophagy modulation as a potential therapeutic target for diverse diseases. Nat Rev Drug Discov 2012, 11:709-730.
105. Hou W., Zhang Q., Yan Z., Chen R., Zeh Iii H.J., Kang R., et al. Strange attractors: DAMPs and autophagy link tumor cell death and immunity. Cell Death Dis 2013, 4:e966.
106. Michaud M., Martins I., Sukkurwala A.Q., Adjemian S., Ma Y., Pellegatti P., et al. Autophagy-dependent anticancer immune responses induced by chemotherapeutic agents in mice. Science 2011, 334:1573-1577.
107. Garg A.D., Dudek A.M., Agostinis P. Calreticulin surface exposure is abrogated in cells lacking, chaperone-mediated autophagy-essential gene, LAMP2A. Cell Death Dis 2013, 4:e826.
108. Mathew R., Khor S., Hackett S.R., Rabinowitz J.D., Perlman D.H., White E. Functional role of autophagy-mediated proteome remodeling in cell survival signaling and innate immunity. Mol Cell 2014, 55:916-930.
109. Jounai N., Takeshita F., Kobiyama K., Sawano A., Miyawaki A., Xin K.Q., et al. The Atg5 Atg12 conjugate associates with innate antiviral immune responses. Proc Natl Acad Sci U S A 2007, 104:14050-14055.
110. McKnight N.C., Zhong Y., Wold M.S., Gong S., Phillips G.R., Dou Z., et al. Beclin 1 is required for neuron viability and regulates endosome pathways via the UVRAG-VPS34 complex. PLoS Genet 2014, 10:e1004626.
111. Kim H.J., Zhong Q., Sheng Z.H., Yoshimori T., Liang C., Jung J.U. Beclin-1-interacting autophagy protein Atg14L targets the SNARE-associated protein Snapin to coordinate endocytic trafficking. J Cell Sci 2012, 125:4740-4750.
112. Puri C., Renna M., Bento C.F., Moreau K., Rubinsztein D.C. ATG16L1 meets ATG9 in recycling endosomes: additional roles for the plasma membrane and endocytosis in autophagosome biogenesis. Autophagy 2014, 10:182-184.
113. Puri C., Renna M., Bento C.F., Moreau K., Rubinsztein D.C. Diverse autophagosome membrane sources coalesce in recycling endosomes. Cell 2013, 154:1285-1299.
114. Hyttinen J.M., Niittykoski M., Salminen A., Kaarniranta K. Maturation of autophagosomes and endosomes: a key role for Rab7. Biochim Biophys Acta 2013, 1833:503-510.
115. Verfaillie T., van Vliet A., Garg A.D., Dewaele M., Rubio N., Gupta S., et al. Pro-apoptotic signaling induced by photo-oxidative ER stress is amplified by Noxa, not Bim. Biochem Biophys Res Commun 2013, 438:500-506.
116. Healy S.J., Gorman A.M., Mousavi-Shafaei P., Gupta S., Samali A. Targeting the endoplasmic reticulum-stress response as an anticancer strategy. Eur J Pharmacol 2009, 625:234-246.
117. Axten J.M., Medina J.R., Feng Y., Shu A., Romeril S.P., Grant S.W., et al. Discovery of 7-methyl-5-(1-{[3-(trifluoromethyl)phenyl]acetyl}-2,3-dihydro-1H-indol-5-yl)-7H-p yrrolo[2,3-d]pyrimidin-4-amine (GSK2606414), a potent and selective first-in-class inhibitor of protein kinase R (PKR)-like endoplasmic reticulum kinase (PERK). J Med Chem 2012, 55:7193-7207.
118. Axten J.M., Romeril S.P., Shu A., Ralph J., Medina J.R., Feng Y., et al. Discovery of GSK2656157: an optimized PERK inhibitor selected for preclinical development. ACS Med Chem Lett 2013, 4:964-968.
119. Flaherty D.P., Golden J.E., Liu C., Hedrick M., Gosalia P., Li Y., et al. Selective small molecule activator of the apoptotic arm of the UPRss 2010, Probe Reports from the NIH Molecular Libraries Program, Bethesda (MD).
120. Bobrovnikova-Marjon E., Grigoriadou C., Pytel D., Zhang F., Ye J., Koumenis C., et al. PERK promotes cancer cell proliferation and tumor growth by limiting oxidative DNA damage. Oncogene 2010, 29:3881-3895.
121. Blais J.D., Addison C.L., Edge R., Falls T., Zhao H., Wary K., et al. Perk-dependent translational regulation promotes tumor cell adaptation and angiogenesis in response to hypoxic stress. Mol Cell Biol 2006, 26:9517-9532.
122. Hetz C., Chevet E., Harding H.P. Targeting the unfolded protein response in disease. Nat Rev Drug Discov 2013, 12:703-719.
123. Maes H., Kuchnio A., Peric A., Moens S., Nys K., De Bock K., et al. Tumor vessel normalization by chloroquine independent of autophagy. Cancer Cell 2014, 26:190-206.
124. Zhou R., Yazdi A.S., Menu P., Tschopp J. A role for mitochondria in NLRP3 inflammasome activation. Nature 2011, 469:221-225.
125. Bobrovnikova-Marjon E., Pytel D., Riese M.J., Vaites L.P., Singh N., Koretzky G.A., et al. PERK utilizes intrinsic lipid kinase activity to generate phosphatidic acid, mediate Akt activation, and promote adipocyte differentiation. Mol Cell Biol 2012, 32:2268-2278.
126. Liu Y., Su Y., Wang X. Phosphatidic acid-mediated signaling. Adv Exp Med Biol 2013, 991:159-176.
127. Liu Z., Cai H., Zhu H., Toque H., Zhao N., Qiu C., et al. Protein kinase RNA-like endoplasmic reticulum kinase (PERK)/calcineurin signaling is a novel pathway regulating intracellular calcium accumulation which might be involved in ventricular arrhythmias in diabetic cardiomyopathy. Cell Signal 2014, 26:2591-2600.
128. 2+ dynamics in beta-cells are regulated by PERK (EIF2AK3) in concert with calcineurin. J Biol Chem 2013, 288:33824-33836.
129. Bollo M., Paredes R.M., Holstein D., Zheleznova N., Camacho P., Lechleiter J.D. Calcineurin interacts with PERK and dephosphorylates calnexin to relieve ER stress in mammals and frogs. PLoS ONE 2010, 5:e11925.
130. 2+ levels favors plasma membrane surface exposure of calreticulin. Cell Death Differ 2008, 15:274-282.
131. Munoz J.P., Ivanova S., Sanchez-Wandelmer J., Martinez-Cristobal P., Noguera E., Sancho A., et al. Mfn2 modulates the UPR and mitochondrial function via repression of PERK. EMBO J 2013, 32:2348-2361.
132. Simmen T., Aslan J.E., Blagoveshchenskaya A.D., Thomas L., Wan L., Xiang Y., et al. PACS-2 controls endoplasmic reticulum-mitochondria communication and Bid-mediated apoptosis. EMBO J 2005, 24:717-729.
133. van Vliet A.R., Verfaillie T., Agostinis P. New functions of mitochondria associated membranes in cellular signaling. Biochim Biophys Acta 2014, 1843:2253-2262.
134. Menger L., Vacchelli E., Adjemian S., Martins I., Ma Y., Shen S., et al. Cardiac glycosides exert anticancer effects by inducing immunogenic cell death. Sci Transl Med 2012, 4. 143ra199.
135. Dudek A.M., Garg A.D., Krysko D.V., De Ruysscher D., Agostinis P. Inducers of immunogenic cancer cell death. Cytokine Growth Factor Rev 2013, 24:319-333.
136. Senovilla L., Vitale I., Martins I., Tailler M., Pailleret C., Michaud M., et al. An immunosurveillance mechanism controls cancer cell ploidy. Science 2012, 337:1678-1684.
137. Yang Y., Li X.J., Chen Z., Zhu X.X., Wang J., Zhang L.B., et al. Wogonin induced calreticulin/annexin A1 exposure dictates the immunogenicity of cancer cells in a PERK/AKT dependent manner. PLoS ONE 2012, 7:e50811.
138. Garrido G., Rabasa A., Sanchez B., Lopez M.V., Blanco R., Lopez A., et al. Induction of immunogenic apoptosis by blockade of epidermal growth factor receptor activation with a specific antibody. J Immunol 2011, 187:4954-4966.
139. Bugaut H., Bruchard M., Berger H., Derangere V., Odoul L., Euvrard R., et al. Bleomycin exerts ambivalent antitumor immune effect by triggering both immunogenic cell death and proliferation of regulatory T cells. PLOS ONE 2013, 8:e65181.
140. Yu Z., Geng J., Zhang M., Zhou Y., Fan Q., Chen J. Treatment of osteosarcoma with microwave thermal ablation to induce immunogenic cell death. Oncotarget 2014, 5:6526-6539.
141. Vacchelli E., Eggermont A., Sautes-Fridman C., Galon J., Zitvogel L., Kroemer G., et al. Trial watch: oncolytic viruses for cancer therapy. Oncoimmunology 2013, 2:e24612.