Membrane-bound heat shock proteins facilitate the uptake of dying cells and cross-presentation of cellular antigen

Apoptosis

Volumn 21, Issue 1, 2016, Pages 96-109

  Zhu, Haiyan ^a   Fang, Xiaoyun ^b   Zhang, Dongmei ^c   Wu, Weicheng ^a   Shao, Miaomiao ^a   Wang, Lan ^a   Gu, Jianxin ^a  

^a FUDAN UNIVERSITY   (China)

^b Jiangsu Patent Examination Assistance Center under Sipo   (China)

^c NANTONG MEDICAL COLLEGE   (China)

Author keywords

Apoptosis; Cross presentation; Cytokine expression; DC maturation; HSPs; LOX 1

Indexed keywords

CD86 ANTIGEN; CELL ANTIGEN; CHAPERONIN 60; CISPLATIN; HEAT SHOCK PROTEIN; HEAT SHOCK PROTEIN 70; HEAT SHOCK PROTEIN 90; INTERLEUKIN 1BETA; INTERLEUKIN 4; INTERLEUKIN 6; MEMBRANE PROTEIN; OXIDIZED LOW DENSITY LIPOPROTEIN RECEPTOR 1; PHOSPHATIDYLSERINE; B7 ANTIGEN; CD86 PROTEIN, MOUSE; HSPD1 PROTEIN, MOUSE; INTERLEUKIN-6, MOUSE; MITOCHONDRIAL PROTEIN; OLR1 PROTEIN, MOUSE; OVALBUMIN; PROTEIN BINDING;

ANIMAL CELL; ANTIGEN PRESENTATION; ANTIGEN PRESENTING CELL; APOPTOSIS; ARTICLE; BONE MARROW DERIVED DENDRITIC CELL; CELL MATURATION; CELL MEMBRANE; CELL SURFACE; CHO CELL LINE; CONFOCAL MICROSCOPY; CONTROLLED STUDY; CROSS PRESENTATION; CYTOMETRY; FEMALE; HL 60 CELL LINE; HUMAN; HUMAN CELL; MOUSE; NONHUMAN; PHAGOCYTOSIS; PRIORITY JOURNAL; PROTEIN EXPRESSION; ULTRAVIOLET IRRADIATION; ANIMAL; C57BL MOUSE; CRICETULUS; CYTOLOGY; DENDRITIC CELL; DRUG EFFECTS; GENE EXPRESSION REGULATION; GENETICS; HL-60 CELL LINE; IMMUNOLOGY; METABOLISM; SIGNAL TRANSDUCTION;

ANIMALS; ANTIGENS, CD80; ANTIGENS, CD86; APOPTOSIS; CELL MEMBRANE; CHAPERONIN 60; CHO CELLS; CRICETULUS; CROSS-PRIMING; DENDRITIC CELLS; GENE EXPRESSION REGULATION; HL-60 CELLS; HSP70 HEAT-SHOCK PROTEINS; HSP90 HEAT-SHOCK PROTEINS; HUMANS; INTERLEUKIN-1BETA; INTERLEUKIN-6; MICE; MICE, INBRED C57BL; MITOCHONDRIAL PROTEINS; OVALBUMIN; PHOSPHATIDYLSERINES; PROTEIN BINDING; SCAVENGER RECEPTORS, CLASS E; SIGNAL TRANSDUCTION;

EID: 84953310911     PISSN: 13608185     EISSN: 1573675X     Source Type: Journal    
DOI: 10.1007/s10495-015-1187-0     Document Type: Article

References (52)

1. 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
2. Shklyar B, Shklover J, Kurant E (2013) Live imaging of apoptotic cell clearance during Drosophila embryogenesis. J Vis Exp (78). doi: 10.3791/50151
3. Hoffmann PR, deCathelineau AM, Ogden CA, Leverrier Y, Bratton DL, Daleke DL, Ridley AJ, Fadok VA, Henson PM (2001) Phosphatidylserine (PS) induces PS receptor-mediated macropinocytosis and promotes clearance of apoptotic cells. J Cell Biol 155(4):649-659. doi: 10.1083/jcb.200108080
4. Li MO, Sarkisian MR, Mehal WZ, Rakic P, Flavell RA (2003) Phosphatidylserine receptor is required for clearance of apoptotic cells. Science 302(5650):1560-1563
5. Moffatt OD, Devitt A, Bell ED, Simmons DL, Gregory CD (1999) Macrophage recognition of ICAM-3 on apoptotic leukocytes. J Immunol 162(11):6800-6810
6. 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/nri957
7. Ucker DS, Jain MR, Pattabiraman G, Palasiewicz K, Birge RB, Li H (2012) Externalized glycolytic enzymes are novel, conserved, and early biomarkers of apoptosis. J Biol Chem 287(13):10325-10343. doi: 10.1074/jbc.M111.314971
8. Lindquist S, Craig EA (1988) The heat-shock proteins. Annu Rev Genet 22:631-677. doi: 10.1146/annurev.ge.22.120188.003215
9. Poccia F, Piselli P, Vendetti S, Bach S, Amendola A, Placido R, Colizzi V (1996) Heat-shock protein expression on the membrane of T cells undergoing apoptosis. Immunology 88(1):6-12
10. Lancaster GI, Febbraio MA (2005) Exosome-dependent trafficking of HSP70: a novel secretory pathway for cellular stress proteins. J Biol Chem 280(24):23349-23355. doi: 10.1074/jbc.M502017200
11. Pfister G, Stroh CM, Perschinka H, Kind M, Knoflach M, Hinterdorfer P, Wick G (2005) Detection of HSP60 on the membrane surface of stressed human endothelial cells by atomic force and confocal microscopy. J Cell Sci 118(Pt 8):1587-1594
12. Srivastava P (2002) Roles of heat-shock proteins in innate and adaptive immunity. Nat Rev Immunol 2(3):185-194
13. Murshid A, Theriault J, Gong J, Calderwood SK (2011) Investigating receptors for extracellular heat shock proteins. Methods Mol Biol 787:289-302. doi: 10.1007/978-1-61779-295-3-22
14. Asea A, Rehli M, Kabingu E, Boch JA, Bare O, Auron PE, Stevenson MA, Calderwood SK (2002) Novel signal transduction pathway utilized by extracellular HSP70: role of toll-like receptor (TLR) 2 and TLR4. J Biol Chem 277(17):15028-15034
15. Vabulas RM, Braedel S, Hilf N, Singh-Jasuja H, Herter S, Ahmad-Nejad P, Kirschning CJ, Da Costa C, Rammensee HG, Wagner H, Schild H (2002) The endoplasmic reticulum-resident heat shock protein Gp96 activates dendritic cells via the Toll-like receptor 2/4 pathway. J Biol Chem 277(23):20847-20853
16. Ghosh AK, Sinha D, Mukherjee S, Biswas R, Biswas T (2015) LPS stimulates and Hsp70 down-regulates TLR4 to orchestrate differential cytokine response of culture-differentiated innate memory CD8(+) T cells. Cytokine 73(1):44-52. doi: 10.1016/j.cyto.2015.01.018
17. Green DR, Ferguson T, Zitvogel L, Kroemer G (2009) Immunogenic and tolerogenic cell death. Nat Rev Immunol 9(5):353-363. doi: 10.1038/nri2545
18. Baruah P, Propato A, Dumitriu IE, Rovere-Querini P, Russo V, Fontana R, Accapezzato D, Peri G, Mantovani A, Barnaba V, Manfredi AA (2006) The pattern recognition receptor PTX3 is recruited at the synapse between dying and dendritic cells, and edits the cross-presentation of self, viral, and tumor antigens. Blood 107(1):151-158. doi: 10.1182/blood-2005-03-1112
19. Desch AN, Randolph GJ, Murphy K, Gautier EL, Kedl RM, Lahoud MH, Caminschi I, Shortman K, Henson PM, Jakubzick CV (2011) CD103+ pulmonary dendritic cells preferentially acquire and present apoptotic cell-associated antigen. J Exp Med 208(9):1789-1797. doi: 10.1084/jem.20110538
20. Dixon KO, O'Flynn J, van der Kooij SW, van Kooten C (2014) Phagocytosis of apoptotic or necrotic cells differentially regulates the transcriptional expression of IL-12 family members in dendritic cells. J Leukoc Biol 96(2):313-324. doi: 10.1189/jlb.3A1013-538RR
21. Nakayama M, Akiba H, Takeda K, Kojima Y, Hashiguchi M, Azuma M, Yagita H, Okumura K (2009) Tim-3 mediates phagocytosis of apoptotic cells and cross-presentation. Blood 113(16):3821-3830
22. Chiba S, Baghdadi M, Akiba H, Yoshiyama H, Kinoshita I, Dosaka-Akita H, Fujioka Y, Ohba Y, Gorman JV, Colgan JD, Hirashima M, Uede T, Takaoka A, Yagita H, Jinushi M (2012) Tumor-infiltrating DCs suppress nucleic acid-mediated innate immune responses through interactions between the receptor TIM-3 and the alarmin HMGB1. Nat Immunol 13(9):832-842. doi: 10.1038/ni.2376
23. Obeid M, Tesniere A, Ghiringhelli F, Fimia GM, Apetoh L, Perfettini JL, Castedo M, Mignot G, Panaretakis T, Casares N, Metivier D, Larochette N, van Endert P, Ciccosanti F, Piacentini M, Zitvogel L, Kroemer G (2007) Calreticulin exposure dictates the immunogenicity of cancer cell death. Nat Med 13(1):54-61. doi: 10.1038/nm1523
24. Murshid A, Gong J, Stevenson MA, Calderwood SK (2011) Heat shock proteins and cancer vaccines: developments in the past decade and chaperoning in the decade to come. Expert Rev Vaccines 10(11):1553-1568. doi: 10.1586/erv.11.124
25. Dunn S, Vohra RS, Murphy JE, Homer-Vanniasinkam S, Walker JH, Ponnambalam S (2008) The lectin-like oxidized low-density-lipoprotein receptor: a pro-inflammatory factor in vascular disease. Biochem J 409(2):349-355
26. Joo H, Li D, Dullaers M, Kim TW, Duluc D, Upchurch K, Xue Y, Zurawski S, Le Grand R, Liu YJ, Kuroda M, Zurawski G, Oh S (2014) C-type lectin-like receptor LOX-1 promotes dendritic cell-mediated class-switched B cell responses. Immunity 41(4):592-604. doi: 10.1016/j.immuni.2014.09.009
27. Delneste Y, Magistrelli G, Gauchat J, Haeuw J, Aubry J, Nakamura K, Kawakami-Honda N, Goetsch L, Sawamura T, Bonnefoy J, Jeannin P (2002) Involvement of LOX-1 in dendritic cell-mediated antigen cross-presentation. Immunity 17(3):353-362
28. Xie J, Zhu H, Guo L, Ruan Y, Wang L, Sun L, Zhou L, Wu W, Yun X, Shen A, Gu J (2010) Lectin-like oxidized low-density lipoprotein receptor-1 delivers heat shock protein 60-fused antigen into the MHC class I presentation pathway. J Immunol 185(4):2306-2313. doi: 10.4049/jimmunol.0903214
29. Oka K, Sawamura T, Kikuta K, Itokawa S, Kume N, Kita T, Masaki T (1998) Lectin-like oxidized low-density lipoprotein receptor 1 mediates phagocytosis of aged/apoptotic cells in endothelial cells. Proc Natl Acad Sci USA 95(16):9535-9540
30. Shimaoka T, Kume N, Minami M, Hayashida K, Sawamura T, Kita T, Yonehara S (2001) LOX-1 supports adhesion of Gram-positive and Gram-negative bacteria. J Immunol 166(8):5108-5114
31. Murphy JE, Tacon D, Tedbury PR, Hadden JM, Knowling S, Sawamura T, Peckham M, Phillips SE, Walker JH, Ponnambalam S (2006) LOX-1 scavenger receptor mediates calcium-dependent recognition of phosphatidylserine and apoptotic cells. Biochem J 393(Pt 1):107-115
32. Yang SH, Li YT, Du DY (2013) Oxidized low-density lipoprotein-induced CD147 expression and its inhibition by high-density lipoprotein on platelets in vitro. Thromb Res 132(6):702-711. doi: 10.1016/j.thromres.2013.10.003
33. Zhu H, Wang L, Ruan Y, Zhou L, Zhang D, Min Z, Xie J, Yu M, Gu J (2011) An efficient delivery of DAMPs on the cell surface by the unconventional secretion pathway. Biochem Biophys Res Commun 404(3):790-795. doi: 10.1016/j.bbrc.2010.12.061
34. Liu A, Ming JY, Fiskesund R, Ninio E, Karabina SA, Bergmark C, Frostegard AG, Frostegard J (2015) Induction of dendritic cell-mediated T-cell activation by modified but not native low-density lipoprotein in humans and inhibition by annexin a5: involvement of heat shock proteins. Arterioscler Thromb Vasc Biol 35(1):197-205. doi: 10.1161/ATVBAHA.114.304342
35. Binder RJ (2009) Hsp receptors: the cases of identity and mistaken identity. Curr Opin Mol Ther 11(1):62-71
36. Theriault JR, Adachi H, Calderwood SK (2006) Role of scavenger receptors in the binding and internalization of heat shock protein 70. J Immunol 177(12):8604-8611
37. 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
38. Zhang D, Feng Y, Zhang Q, Su X, Lu X, Liu S, Zhong L (2015) Raman spectrum reveals the cell cycle arrest of Triptolide-induced leukemic T-lymphocytes apoptosis. Spectrochim Acta Part A Mol Biomol Spectrosc 141:216-222. doi: 10.1016/j.saa.2015.01.037
39. Dyugovskaya L, Berger S, Polyakov A, Lavie L (2014) The development of giant phagocytes in long-term neutrophil cultures. J Leukoc Biol 96(4):511-521. doi: 10.1189/jlb.0813437
40. Garg AD, Nowis D, Golab J, Vandenabeele P, Krysko DV (1805) Agostinis P (2010) Immunogenic cell death, DAMPs and anticancer therapeutics: an emerging amalgamation. Biochim Biophys Acta 1:53-71
41. Panaretakis T, Kepp O, Brockmeier U, Tesniere A, Bjorklund AC, Chapman DC, Durchschlag M, Joza N, Pierron G, van Endert P, Yuan J, Zitvogel L, Madeo F, Williams DB, Kroemer G (2009) Mechanisms of pre-apoptotic calreticulin exposure in immunogenic cell death. EMBO J 28(5):578-590. doi: 10.1038/emboj.2009.1
42. Meier P, Finch A, Evan G (2000) Apoptosis in development. Nature 407(6805):796-801. doi: 10.1038/35037734
43. Devitt A, Marshall LJ (2011) The innate immune system and the clearance of apoptotic cells. J Leukoc Biol 90(3):447-457. doi: 10.1189/jlb.0211095
44. Caminschi I, Lahoud MH, Shortman K (2009) Enhancing immune responses by targeting antigen to DC. Eur J Immunol 39(4):931-938
45. Johansson U, Walther-Jallow L, Smed-Sorensen A, Spetz AL (2007) Triggering of dendritic cell responses after exposure to activated, but not resting, apoptotic PBMCs. J Immunol 179(3):1711-1720
46. Hertoghs N, van der Aar AM, Setiawan LC, Kootstra NA, Gringhuis SI, Geijtenbeek TB (2015) SAMHD1 Degradation Enhances Active Suppression of Dendritic Cell Maturation by HIV-1. J Immunol 194(9):4431-4437. doi: 10.4049/jimmunol.1403016
47. Schaefer L (2014) Complexity of danger: the diverse nature of damage-associated molecular patterns. J Biol Chem 289(51):35237-35245. doi: 10.1074/jbc.R114.619304
48. Spisek R, Charalambous A, Mazumder A, Vesole DH, Jagannath S, Dhodapkar MV (2007) 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 109(11):4839-4845. doi: 10.1182/blood-2006-10-054221
49. Feng H, Zeng Y, Graner MW, Katsanis E (2002) Stressed apoptotic tumor cells stimulate dendritic cells and induce specific cytotoxic T cells. Blood 100(12):4108-4115
50. Fredly H, Ersvaer E, Gjertsen BT, Bruserud O (2011) Immunogenic apoptosis in human acute myeloid leukemia (AML): primary human AML cells expose calreticulin and release heat shock protein (HSP) 70 and HSP90 during apoptosis. Oncol Rep 25(6):1549-1556. doi: 10.3892/or.2011.1229
51. Tsan MF, Gao B (2009) Heat shock proteins and immune system. J Leukoc Biol 85(6):905-910. doi: 10.1189/jlb.0109005
52. Albert ML (2004) Death-defying immunity: do apoptotic cells influence antigen processing and presentation? Nat Rev Immunol 4(3):223-231. doi: 10.1038/nri11308