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

详细信息    查看全文

• 作者：Haiyan Zhu ; Xiaoyun Fang ; Dongmei Zhang ; Weicheng Wu ; Miaomiao Shao ; Lan Wang…
• 关键词：HSPs ; Apoptosis ; Cytokine expression ; DC maturation ; Cross ; presentation ; LOX ; 1
• 刊名：Apoptosis
• 出版年：2016
• 出版时间：January 2016
• 年：2016
• 卷：21
• 期：1
• 页码：96-109
• 全文大小：4,600 KB
• 参考文献：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 PubMed PubMedCentral CrossRef
  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 PubMed PubMedCentral CrossRef
  4.Li MO, Sarkisian MR, Mehal WZ, Rakic P, Flavell RA (2003) Phosphatidylserine receptor is required for clearance of apoptotic cells. Science 302(5650):1560–1563PubMed CrossRef
  5.Moffatt OD, Devitt A, Bell ED, Simmons DL, Gregory CD (1999) Macrophage recognition of ICAM-3 on apoptotic leukocytes. J Immunol 162(11):6800–6810PubMed
  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 PubMed CrossRef
  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 PubMed PubMedCentral CrossRef
  8.Lindquist S, Craig EA (1988) The heat-shock proteins. Annu Rev Genet 22:631–677. doi:10.​1146/​annurev.​ge.​22.​120188.​003215 PubMed CrossRef
  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):6–12PubMed PubMedCentral CrossRef
  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 PubMed CrossRef
  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):1587–1594PubMed CrossRef
  12.Srivastava P (2002) Roles of heat-shock proteins in innate and adaptive immunity. Nat Rev Immunol 2(3):185–194PubMed CrossRef
  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 PubMed PubMedCentral CrossRef
  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):15028–15034PubMed CrossRef
  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):20847–20853PubMed CrossRef
  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 PubMed CrossRef
  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 PubMed PubMedCentral CrossRef
  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 PubMed CrossRef
  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 PubMed PubMedCentral CrossRef
  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 PubMed CrossRef
  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):3821–3830PubMed CrossRef
  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 PubMed PubMedCentral CrossRef
  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 PubMed CrossRef
  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 PubMed PubMedCentral CrossRef
  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):349–355PubMed CrossRef
  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 PubMed PubMedCentral CrossRef
  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):353–362PubMed CrossRef
  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 PubMed CrossRef
  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):9535–9540PubMed PubMedCentral CrossRef
  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):5108–5114PubMed CrossRef
  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):107–115PubMed PubMedCentral CrossRef
  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 PubMed CrossRef
  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 PubMed CrossRef
  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 PubMed CrossRef
  35.Binder RJ (2009) Hsp receptors: the cases of identity and mistaken identity. Curr Opin Mol Ther 11(1):62–71PubMed
  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):8604–8611PubMed CrossRef
  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 PubMed CrossRef
  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 CrossRef
  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 PubMed CrossRef
  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 PubMed PubMedCentral CrossRef
  42.Meier P, Finch A, Evan G (2000) Apoptosis in development. Nature 407(6805):796–801. doi:10.​1038/​35037734 PubMed CrossRef
  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 PubMed CrossRef
  44.Caminschi I, Lahoud MH, Shortman K (2009) Enhancing immune responses by targeting antigen to DC. Eur J Immunol 39(4):931–938PubMed CrossRef
  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):1711–1720PubMed CrossRef
  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 PubMed CrossRef
  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 PubMed PubMedCentral CrossRef
  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 PubMed PubMedCentral CrossRef
  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):4108–4115PubMed CrossRef
  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 PubMed
  51.Tsan MF, Gao B (2009) Heat shock proteins and immune system. J Leukoc Biol 85(6):905–910. doi:10.​1189/​jlb.​0109005 PubMed CrossRef
  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 PubMed CrossRef
  
• 作者单位：Haiyan Zhu (1)
  Xiaoyun Fang (2)
  Dongmei Zhang (3)
  Weicheng Wu (1)
  Miaomiao Shao (1)
  Lan Wang (1)
  Jianxin Gu (1)
  
  1. Key Laboratory of Glycoconjugate Research, School of Basic Medical Sciences, Fudan University, Shanghai, 200032, China
  2. Jiangsu Patent Examination Assistance Center Under Sipo, Suzhou, Jiangsu, 215163, China
  3. Department of Pathogen Biology, Medical College, Nantong University, Nantong, 226001, China
  
• 刊物类别：Medicine
• 刊物主题：Medicine & Public Health
  Oncology
  Cancer Research
  Cell Biology
  Biochemistry
  Virology
  
• 出版者：Springer Netherlands
• ISSN：1573-675X

文摘

Heat shock proteins (HSPs) were originally identified as stress-responsive proteins and serve as molecular chaperones in different intracellular compartments. Translocation of HSPs to the cell surface and release of HSPs into the extracellular space have been observed during the apoptotic process and in response to a variety of cellular stress. Here, we report that UV irradiation and cisplatin treatment rapidly induce the expression of membrane-bound Hsp60, Hsp70, and Hsp90 upstream the phosphatidylserine exposure. Membrane-bound Hsp60, Hsp70 and Hsp90 could promote the release of IL-6 and IL-1β as well as DC maturation by the evaluation of CD80 and CD86 expression. On the other hand, Hsp60, Hsp70 and Hsp90 on cells could facilitate the uptake of dying cells by bone marrow-derived dendritic cells. Lectin-like oxidized LDL receptor-1 (LOX-1), as a common receptor for Hsp60, Hsp70, and Hsp90, is response for their recognition and mediates the uptake of dying cells. Furthermore, membrane-bound Hsp60, Hsp70 and Hsp90 could promote the cross-presentation of OVA antigen from E.G7 cells and inhibition of the uptake of dying cells by LOX-1 decreases the cross-presentation of cellular antigen. Therefore, the rapid exposure of HSPs on dying cells at the early stage allows for the recognition by and confers an activation signal to the immune system. Keywords HSPs Apoptosis Cytokine expression DC maturation Cross-presentation LOX-1