Abstract
Heat Shock Protein 60 (HSP60) is primarily a chaperone protein responsible for refolding proteins in the mitochondria. Nevertheless it has numerous other pro- and anti-apoptotis and signalling functions which it achieves through a variety of post-translational modifications (PTMs). Increasing evidence indicates that in disease states from cancer to systemic inflammation, such modifications become dysregulated, and as a result HSP60 cannot perform its functions. Understanding the biological role of these PTMs in healthy and disease states, the context in which they are generated and removed, as well as the mechanisms by which they can be targetted and modulated extraneously will help to provide better therapeutic solutions to deal with a wide range of conditions driven by stress-related processes.
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Abbreviations
- ADAM:
-
A Disintegrin And Metalloproteinase
- aDMA:
-
asymmetric N,N-di-methylarginine
- AdoMet:
-
S-adenosyl-L-methioinine
- Akt:
-
protein kinase B
- APCs:
-
antigen-presenting cells
- ATP:
-
adenosine triphosphate
- β-O-GlyNAcylation:
-
O-linked N-acetylglucosamine
- Bak:
-
BCL2 Antagonist/Killer 1
- Bax:
-
BCL2-Associated X Protein
- BCL2:
-
B-Cell Chronic Lymphocytic Leukemia/Lymphoma 2
- BCL2-L1:
-
Bcl-2-Like Protein 1
- CD:
-
cluster of differentiation
- CLEC:
-
C-type lectin
- DNA:
-
deoxyribonucleic acid
- Dox:
-
Doxorubicin
- E1s:
-
ubiquitin-activating enzymes
- E2s:
-
ubiquitin-conjugating enzymes
- E3s:
-
ubiquitin ligases
- ER:
-
endoplasmic reticulum
- ERB:
-
eukaryotic ribosome biogenesis protein
- ETF:
-
electron transfer flavoprotein
- ExAC:
-
Exome Aggregation Consortium
- GA:
-
Geldanamycin
- GPI anchor:
-
Glycosylphosphatidylinositol anchor
- H2B:
-
histone 2B
- HATs:
-
histone acetyltransferases
- HDACis:
-
Histone deacetylase inhibitors
- HDACs:
-
histone deacetylases
- HSE:
-
heat shock response element
- HSF1:
-
heat shock factor 1
- HSP:
-
heat shock protein/s
- IL-1b:
-
interleukin-1b
- iNOS:
-
inducible nitric oxide synthase
- K:
-
lysine
- KATs:
-
lysine acetyltransferases
- KDACs:
-
lysine deacetylases
- KO:
-
knock-out
- M:
-
methionine
- METTL:
-
Methyltransferase-like
- MHC:
-
major histocompatibility complex
- MIRKO:
-
muscle insulin receptor knockout
- MMPs:
-
matrix metalloproteases
- N:
-
asparagine
- NAC:
-
N-acetyl-cysteine
- NATs:
-
N-terminal acetyltransferases
- NF-kB:
-
Nuclear Factor kappa-light-chain-enhancer of activated B cells
- NKG2D:
-
Natural killer group 2 member D receptor
- NO:
-
nitric oxide
- NSP4:
-
nonstructural protein 4
- PKA-I:
-
protein kinase A, type 1
- PKMTs:
-
protein lysine methyltransferases
- PRL-3:
-
phosphatase of Regenerating Liver 3
- PRMTs:
-
protein arginine methyltransferases
- PTMs:
-
post-translational modifications
- RNS:
-
reactive nitrogen species
- ROS:
-
reactive oxygen species
- S:
-
serine
- SAHA:
-
Suberoylanilide hydroxamic acid
- SET:
-
Su(var)3-9, Enhancer-of-zeste and Trithorax
- SIRT:
-
sirtuin
- SNP:
-
single nucleotide polymorphism
- Src:
-
sarcoma
- T:
-
threonine
- TLR:
-
toll-like-receptor
- ULBP2:
-
UL16 binding protein 2
- Y:
-
tyrosine
References
Abdelmegeed MA, Song BJ (2014) Functional roles of protein nitration in acute and chronic liver diseases. Oxidative Med Cell Longev 2014:149627
Abello N, Kerstjens HA, Postma DS, Bischoff R (2009) Protein tyrosine nitration: selectivity, physicochemical and biological consequences, denitration, and proteomics methods for the identification of tyrosine-nitrated proteins. J Proteome Res 8(7):3222–3238
Akimoto Y, Kreppel LK, Hirano H, Hart GW (2001) Hyperglycemia and the O-GlcNAc transferase in rat aortic smooth muscle cells: elevated expression and altered patterns of O-GlcNAcylation. Arch Biochem Biophys 389(2):166–175
Al-Aidaroos AQO, Zeng Q (2010) PRL-3 phosphatase and cancer metastasis. J Cell Biochem 111(5):1087–1098
Alexandraki K, Piperi C, Kalofoutis C, Singh J, Alaveras A, Kalofoutis A (2006) Inflammatory process in type 2 diabetes. Ann N Y Acad Sci 1084(1):89–117
Alrob OA, Sankaralingam S, Ma C, Wagg CS, Fillmore N, Jaswal JS, Sack MN, Lehner R, Gupta MP, Michelakis ED, Padwal RS (2014) Obesity-induced lysine acetylation increases cardiac fatty acid oxidation and impairs insulin signalling. Cardiovasc Res 103(4):485–497
Altieri P, Spallarossa P, Barisione C, Garibaldi S, Garuti A, Fabbi P, Ghigliotti G, Brunelli C (2012) Inhibition of doxorubicin-induced senescence by PPARδ activation agonists in cardiac muscle cells: cooperation between PPARδ and Bcl6. PLoS One 7(9):e46126
Ande SR, Moulik S, Mishra S (2009) Interaction between O-GlcNAc modification and tyrosine phosphorylation of prohibitin: implication for a novel binary switch. PLoS One 4(2):e4586
Arias AE, Vélez-Granell CS, Mayer G, Bendayan M (2000) Colocalization of chaperone Cpn60, proinsulin and convertase PC1 within immature secretory granules of insulin-secreting cells suggests a role for Cpn60 in insulin processing. J Cell Sci 113(11):2075–2083
Asquith KL, Baleato RM, McLaughlin EA, Nixon B, Aitken RJ (2004) Tyrosine phosphorylation activates surface chaperones facilitating sperm-zona recognition. J Cell Sci 117(16):3645–3657
Avidan A, Perlmutter M, Tal S, Oraki O, Kapp T, Krelin Y, Elkabets M, Dotan S, Apte RN, Lichtenstein RG (2009) Differences in the sialylation patterns of membrane stress proteins in chemical carcinogen-induced tumors developed in BALB/c and IL-1α deficient mice. Glycoconj J 26(9):1181
Bailey LM, Wallace JC, Polyak SW (2010) Holocarboxylase synthetase: correlation of protein localisation with biological function. Arch Biochem Biophys 496(1):45–52
Bao B, Wijeratne SS, Rodriguez-Melendez R, Zempleni J (2011) Human holocarboxylase synthetase with a start site at methionine-58 is the predominant nuclear variant of this protein and has catalytic activity. Biochem Biophys Res Commun 412(1):115–120
Barazi HO, Zhou L, Templeton NS, Krutzsch HC, Roberts DD (2002) Identification of heat shock protein 60 as a molecular mediator of α3β1 integrin activation. Cancer Res 62(5):1541–1548
Baron B (2015) Lysine methylation of non-histone proteins. Biochem Mod Appl 1:1–2
Baron B (2018) The diagnostic and prognostic application of heat shock proteins and their post-translational modifications from liquid biopsies. IntechOpen [Online First]
Barone R, Rappa F, Macaluso F, Bavisotto CC, Sangiorgi C, Di Paola G, Tomasello G, Di Felice V, Marcianò V, Farina F, Zummo G (2016) Alcoholic liver disease: a mouse model reveals protection by Lactobacillus fermentum. Clin Transl Gastroenterol 7(1):e138
Bateman A, Coin L, Durbin R, Finn RD, Hollich V, Griffiths-Jones S, Khanna A, Marshall M, Moxon S, Sonnhammer EL, Studholme DJ (2004) The Pfam protein families database. Nucleic Acids Res 32(Suppl 1):D138–D141
Bernkopf M, Webersinke G, Tongsook C, Koyani CN, Rafiq MA, Ayaz M, Müller D, Enzinger C, Aslam M, Naeem F, Schmidt K (2014) Disruption of the methyltransferase-like 23 gene METTL23 causes mild autosomal recessive intellectual disability. Hum Mol Genet 23(15):4015–4023
Bessette DC, Qiu D, Pallen CJ (2008) PRL PTPs: mediators and markers of cancer progression. Cancer Metastasis Rev 27(2):231–252
Bhowmick R, Halder UC, Chattopadhyay S, Chanda S, Nandi S, Bagchi P, Nayak MK, Chakrabarti O, Kobayashi N, Chawla-Sarkar M (2012) Rotaviral enterotoxin nonstructural protein 4 targets mitochondria for activation of apoptosis during infection. J Biol Chem 287(42):35004–35020
Bie AS, Fernandez-Guerra P, Birkler RI, Nisemblat S, Pelnena D, Lu X, Deignan JL, Lee H, Dorrani N, Corydon TJ, Palmfeldt J (2016) Effects of a mutation in the HSPE1 gene encoding the mitochondrial co-chaperonin HSP10 and its potential association with a neurological and developmental disorder. Front Mol Biosci 3:65
Braig M, Lee S, Loddenkemper C, Rudolph C, Peters AH, Schlegelberger B, Stein H, Dörken B, Jenuwein T, Schmitt CA (2005) Oncogene-induced senescence as an initial barrier in lymphoma development. Nature 436(7051):660
Brocchieri L, Karlin S (2000) Conservation among HSP60 sequences in relation to structure, function, and evolution. Protein Sci 9(3):476–486
Bross P, Fernandez-Guerra P (2016) Disease-associated mutations in the HSPD1 gene encoding the large subunit of the mitochondrial HSP60/HSP10 chaperonin complex. Front Mol Biosci 3:49
Brudzynski K, Martinez V (1993) Synaptophysin-containing microvesicles transport heat-shock protein hsp60 in insulin-secreting beta cells. Cytotechnology 11(1):23–33
Bukau B, Horwich AL (1998) The Hsp70 and Hsp60 chaperone machines. Cell 92(3):351–366
Buse MG (2006) Hexosamines, insulin resistance, and the complications of diabetes: current status. Am J Physiol-Endocrinol Metab 290(1):E1–E8
Butler LM, Agus DB, Scher HI, Higgins B, Rose A, Cordon-Cardo C, Thaler HT, Rifkind RA, Marks PA, Richon VM (2000) Suberoylanilide hydroxamic acid, an inhibitor of histone deacetylase, suppresses the growth of prostate cancer cells in vitro and in vivo. Cancer Res 60(18):5165–5170
Campanella C, Marino Gammazza A, Mularoni L, Cappello F, Zummo G, Di Felice V (2009) A comparative analysis of the products of GROEL-1 gene from chlamydia trachomatis serovar D and the HSP60 var1 transcript from Homo sapiens suggests a possible autoimmune response. Int J Immunogenet 36(1):73–78
Campanella C, Bucchieri F, Merendino AM, Fucarino A, Burgio G, Corona DF, Barbieri G, David S, Farina F, Zummo G, de Macario EC (2012) The odyssey of Hsp60 from tumor cells to other destinations includes plasma membrane-associated stages and Golgi and exosomal protein-trafficking modalities. PLoS One 7(7):e42008
Campanella C, Bavisotto CC, Gammazza AM, Nikolic D, Rappa F, David S, Cappello F, Bucchieri F, Fais S (2014) Exosomal heat shock proteins as new players in tumour cell-to-cell communication. J Circulating Biomark 3:4
Campanella C, Rappa F, Sciumè C, Marino Gammazza A, Barone R, Bucchieri F, David S, Curcurù G, Caruso Bavisotto C, Pitruzzella A, Geraci G (2015) Heat shock protein 60 levels in tissue and circulating exosomes in human large bowel cancer before and after ablative surgery. Cancer 121(18):3230–3239
Campanella C, D'Anneo A, Gammazza AM, Bavisotto CC, Barone R, Emanuele S, Cascio FL, Mocciaro E, Fais S, De Macario EC, Macario AJ (2016) The histone deacetylase inhibitor SAHA induces HSP60 nitration and its extracellular release by exosomal vesicles in human lung-derived carcinoma cells. Oncotarget 7(20):28849
Cao XJ, Arnaudo AM, Garcia BA (2013) Large-scale global identification of protein lysine methylation in vivo. Epigenetics 8(5):477–485
Cappello F, Zummo G (2005) HSP60 expression during carcinogenesis: a molecular “Proteus” of carcinogenesis? Cell Stress Chaperones 10(4):263
Cappello F, Bellafiore M, David S, Anzalone R, Zummo G (2003) Ten kilodalton heat shock protein (HSP10) is overexpressed during carcinogenesis of large bowel and uterine exocervix. Cancer Lett 196(1):35–41
Cappello F, David S, Rappa F, Bucchieri F, Marasà L, Bartolotta TE, Farina F, Zummo G (2005) The expression of HSP60 and HSP10 in large bowel carcinomas with lymph node metastase. BMC Cancer 5(1):139
Cappello F, Bellafiore M, Palma A, David S, Marcianà V, Bartolotta T, Sciumà C, Modica G, Farina F, Zummo G, Bucchieri F (2009) 60KDa chaperonin (HSP60) is over-expressed during colorectal carcinogenesis. Eur J Histochem 47(2):105–110
Cappello F, Marino Gammazza A, Palumbo Piccionello A, Campanella C, Pace A, Conway de Macario E, Macario AJ (2014) Hsp60 chaperonopathies and chaperonotherapy: targets and agents. Expert Opin Ther Targets 18(2):185–208
Chandra D, Choy G, Tang DG (2007) Cytosolic accumulation of Hsp60 during apoptosis with or without apparent mitochondrial release evidence that its pro-apoptotic or pro-survival functions involve differential interactions with caspase-3. J Biol Chem 282(43):31289–31301
Chao CC, Sun FC, Wang CH, Lo CW, Chang YS, Chang KC, Chang MDT, Lai YK (2008) Concerted actions of multiple transcription elements confer differential transactivation of HSP90 isoforms in geldanamycin-treated 9L rat gliosarcoma cells. J Cell Biochem 104(4):1286–1296
Chapman-Smith A, Cronan JE Jr (1999) Molecular biology of biotin attachment to proteins. J Nutr 129(2):477S–484S
Chattopadhyay S, Mukherjee A, Patra U, Bhowmick R, Basak T, Sengupta S, Chawla-Sarkar M (2017) Tyrosine phosphorylation modulates mitochondrial chaperonin Hsp60 and delays rotavirus NSP4-mediated apoptotic signaling in host cells. Cell Microbiol 19(3):e12670
Chavarría C, Souza JM (2013) Oxidation and nitration of α-synuclein and their implications in neurodegenerative diseases. Arch Biochem Biophys 533(1–2):25–32
Chen W, Syldath U, Bellmann K, Burkart V, Kolb H (1999) Human 60-kDa heat-shock protein: a danger signal to the innate immune system. J Immunol 162(6):3212–3219
Chen W, Wang J, Shao C, Liu S, Yu Y, Wang Q, Cao X (2006) Efficient induction of antitumor T cell immunity by exosomes derived from heat-shocked lymphoma cells. Eur J Immunol 36(6):1598–1607
Chen S, Zhao Y, Gou WF, Zhao S, Takano Y, Zheng HC (2013) The anti-tumor effects and molecular mechanisms of suberoylanilide hydroxamic acid (SAHA) on the aggressive phenotypes of ovarian carcinoma cells. PLoS One 8(11):e79781
Cheng X, Cole RN, Zaia J, Hart GW (2000) Alternative O-glycosylation/O-phosphorylation of the murine estrogen receptor β. Biochemistry 39(38):11609–11620
Chew YC, Camporeale G, Kothapalli N, Sarath G, Zempleni J (2006) Lysine residues in N-terminal and C-terminal regions of human histone H2A are targets for biotinylation by biotinidase. J Nutr Biochem 17(4):225–233
Choudhary C, Kumar C, Gnad F, Nielsen ML, Rehman M, Walther TC, Olsen JV, Mann M (2009) Lysine acetylation targets protein complexes and co-regulates major cellular functions. Science 325(5942):834–840
Christensen JH, Nielsen MN, Hansen J, Füchtbauer A, Füchtbauer EM, West M, Corydon TJ, Gregersen N, Bross P (2010) Inactivation of the hereditary spastic paraplegia-associated Hspd1 gene encoding the Hsp60 chaperone results in early embryonic lethality in mice. Cell Stress Chaperones 15(6):851–863
Cloutier P, Lavallée-Adam M, Faubert D, Blanchette M, Coulombe B (2013) A newly uncovered group of distantly related lysine methyltransferases preferentially interact with molecular chaperones to regulate their activity. PLoS Genet 9(1):e1003210
Comer FI, Hart GW (2001) Reciprocity between O-GlcNAc and O-phosphate on the carboxyl terminal domain of RNA polymerase II. Biochemistry 40(26):7845–7852
Copeland RJ, Bullen JW Jr, Hart GW (2008) Crosstalk between GlcNAcylation and phosphorylation: roles in insulin resistance and glucose toxicity. Am J Physiol-Endocrinol Metab 295:E17–E28
Corbett JA, McDaniel ML (1995) Intraislet release of interleukin 1 inhibits beta cell function by inducing beta cell expression of inducible nitric oxide synthase. J Exp Med 181(2):559–568
Cosman D, Müllberg J, Sutherland CL, Chin W, Armitage R, Fanslow W, Kubin M, Chalupny NJ (2001) ULBPs, novel MHC class I–related molecules, bind to CMV glycoprotein UL16 and stimulate NK cytotoxicity through the NKG2D receptor. Immunity 14(2):123–133
Czarnecka AM, Campanella C, Zummo G, Cappello F (2006) Mitochondrial chaperones in cancer: from molecular biology to clinical diagnostics. Cancer Biol Ther 5(7):714–720
Davis CW, Hawkins BJ, Ramasamy S, Irrinki KM, Cameron BA, Islam K, Daswani VP, Doonan PJ, Manevich Y, Madesh M (2010) Nitration of the mitochondrial complex I subunit NDUFB8 elicits RIP1-and RIP3-mediated necrosis. Free Radic Biol Med 48(2):306–317
De Bellis F, Carafa V, Conte M, Rotili D, Petraglia F, Matarese F, Françoijs KJ, Ablain J, Valente S, Castellano R, Goubard A (2014) Context-selective death of acute myeloid leukemia cells triggered by the novel hybrid retinoid-HDAC inhibitor MC2392. Cancer Res 74(8):2328–2339
Dentin R, Hedrick S, Xie J, Yates J, Montminy M (2008) Hepatic glucose sensing via the CREB coactivator CRTC2. Science 319(5868):1402–1405
Drazic A, Myklebust LM, Ree R, Arnesen T (2016) The world of protein acetylation. Biochim Biophys Acta (BBA)-Proteins Proteomics 1864(10):1372–1401
Eren MK, Kilincli A, Eren Ö (2015) Resveratrol induced premature senescence is associated with DNA damage mediated SIRT1 and SIRT2 down-regulation. PLoS One 10(4):e0124837
Farrugia M, Baron B (2017) The role of Toll-like receptors in autoimmune diseases through failure of the self-recognition mechanism. Int J Inflamm 2017:8391230
Fiskus W, Ren Y, Mohapatra A, Bali P, Mandawat A, Rao R, Herger B, Yang Y, Atadja P, Wu J, Bhalla K (2007) Hydroxamic acid analogue histone deacetylase inhibitors attenuate estrogen receptor-α levels and transcriptional activity: a result of hyperacetylation and inhibition of chaperone function of heat shock protein 90. Clin Cancer Res 13(16):4882–4890
Fritz KS, Galligan JJ, Hirschey MD, Verdin E, Petersen DR (2012) Mitochondrial acetylome analysis in a mouse model of alcohol-induced liver injury utilizing SIRT3 knockout mice. J Proteome Res 11(3):1633–1643
Gammazza AM, Campanella C, Barone R, Bavisotto CC, Gorska M, Wozniak M, Carini F, Cappello F, D'Anneo A, Lauricella M, Zummo G (2017) Doxorubicin anti-tumor mechanisms include Hsp60 post-translational modifications leading to the Hsp60/p53 complex dissociation and instauration of replicative senescence. Cancer Lett 385:75–86
Ghosh JC, Dohi T, Kang BH, Altieri DC (2008) Hsp60 regulation of tumor cell apoptosis. J Biol Chem 283(8):5188–5194
Ghosh JC, Siegelin MD, Dohi T, Altieri DC (2010) Heat shock protein 60 regulation of the mitochondrial permeability transition pore in tumor cells. Cancer Res 70(22):8988–8993
Glickman MH, Ciechanover A (2002) The ubiquitin-proteasome proteolytic pathway: destruction for the sake of construction. Physiol Rev 82(2):373–428
Glozak MA, Sengupta N, Zhang X, Seto E (2005) Acetylation and deacetylation of non-histone proteins. Gene 363:15–23
Gorska M, Gammazza AM, Zmijewski MA, Campanella C, Cappello F, Wasiewicz T, Kuban-Jankowska A, Daca A, Sielicka A, Popowska U, Knap N (2013) Geldanamycin-induced osteosarcoma cell death is associated with hyperacetylation and loss of mitochondrial pool of heat shock protein 60 (hsp60). PLoS One 8(8):e71135
Greening DW, Gopal SK, Xu R, Simpson RJ, Chen W (2015) Exosomes and their roles in immune regulation and cancer. Semin Cell Dev Biol 40:72–81. Academic Press
Gu TL, Deng X, Huang F, Tucker M, Crosby K, Rimkunas V, Wang Y, Deng G, Zhu L, Tan Z, Hu Y (2011a) Survey of tyrosine kinase signaling reveals ROS kinase fusions in human cholangiocarcinoma. PLoS One 6(1):e15640
Gu Y, Ande SR, Mishra S (2011b) Altered O-GlcNAc modification and phosphorylation of mitochondrial proteins in myoblast cells exposed to high glucose. Arch Biochem Biophys 505(1):98–104
Gueugnon F, Cartron PF, Charrier C, Bertrand P, Fonteneau JF, Gregoire M, Blanquart C (2014) New histone deacetylase inhibitors improve cisplatin antitumor properties against thoracic cancer cells. Oncotarget 5(12):4504
Guo K, Li J, Ping Tang J, Bobby Tan CP, Wang H, Wang H, Zeng Q (2008) Monoclonal antibodies target intracellular PRL phosphatases to inhibit cancer metastases in mice. Cancer Biol Ther 7(5):750–757
Guo X, Keyes WM, Papazoglu C, Zuber J, Li W, Lowe SW, Vogel H, Mills AA (2009) TAp63 induces senescence and suppresses tumorigenesis in vivo. Nat Cell Biol 11(12):1451
Gupta S, Knowlton AA (2002) Cytosolic heat shock protein 60, hypoxia, and apoptosis. Circulation 106(21):2727–2733
Gupta S, Knowlton AA (2005) HSP60, Bax, apoptosis and the heart. J Cell Mol Med 9(1):51–58
Ha K, Fiskus W, Choi DS, Bhaskara S, Cerchietti L, Devaraj SG, Shah B, Sharma S, Chang JC, Melnick AM, Hiebert S (2014) Histone deacetylase inhibitor treatment induces ‘BRCAness’ and synergistic lethality with PARP inhibitor and cisplatin against human triple negative breast cancer cells. Oncotarget 5(14):5637
Haaland I, Opsahl JA, Berven FS, Reikvam H, Fredly HK, Haugse R, Thiede B, McCormack E, Lain S, Bruserud Ø, Gjertsen BT (2014) Molecular mechanisms of nutlin-3 involve acetylation of p53, histones and heat shock proteins in acute myeloid leukemia. Mol Cancer 13(1):116
Hageman J, Rujano MA, Van Waarde MA, Kakkar V, Dirks RP, Govorukhina N, Oosterveld-Hut HM, Lubsen NH, Kampinga HH (2010) A DNAJB chaperone subfamily with HDAC-dependent activities suppresses toxic protein aggregation. Mol Cell 37(3):355–369
Han JY, Lee SH, Lee GK, Yun T, Lee YJ, Hwang KH, Kim JY, Kim HT (2015) Phase I/II study of gefitinib (Iressa®) and vorinostat (IVORI) in previously treated patients with advanced non-small cell lung cancer. Cancer Chemother Pharmacol 75(3):475–483
Hansen JJ, Dürr A, Cournu-Rebeix I, Georgopoulos C, Ang D, Nielsen MN, Davoine CS, Brice A, Fontaine B, Gregersen N, Bross P (2002) Hereditary spastic paraplegia SPG13 is associated with a mutation in the gene encoding the mitochondrial chaperonin Hsp60. Am J Hum Genet 70(5):1328–1332
Hayes GR, Williams A, Costello CE, Enns CA, Lucas JJ (1995) The critical glycosylation site of human transferrin receptor contains a high-mannose oligosaccharide. Glycobiology 5(2):227–232
Hayoun D, Kapp T, Edri-Brami M, Ventura T, Cohen M, Avidan A, Lichtenstein RG (2012) HSP60 is transported through the secretory pathway of 3-MCA-induced fibrosarcoma tumour cells and undergoes N-glycosylation. FEBS J 279(12):2083–2095
Helenius A, Aebi M (2001) Intracellular functions of N-linked glycans. Science 291(5512):2364–2369
Hilpert J, Grosse-Hovest L, Grünebach F, Buechele C, Nuebling T, Raum T, Steinle A, Salih HR (2012) Comprehensive analysis of NKG2D ligand expression and release in leukemia: implications for NKG2D-mediated NK cell responses. J Immunol 189(3):1360–1371
Huang YC, Huang FI, Mehndiratta S, Lai SC, Liou JP, Yang CR (2015) Anticancer activity of MPT0G157, a derivative of indolylbenzenesulfonamide, inhibits tumor growth and angiogenesis. Oncotarget 6(21):18590
Hunter T (2007) The age of crosstalk: phosphorylation, ubiquitination, and beyond. Mol Cell 28(5):730–738
Jimenez-Feltstrom J, Lundquist I, Salehi A (2005) Glucose stimulates the expression and activities of nitric oxide synthases in incubated rat islets: an effect counteracted by GLP-1 through the cyclic AMP/PKA pathway. Cell Tissue Res 319(2):221–230
Jindal S, Dudani AK, Singh BHAG, Harley CB, Gupta RS (1989) Primary structure of a human mitochondrial protein homologous to the bacterial and plant chaperonins and to the 65-kilodalton mycobacterial antigen. Mol Cell Biol 9(5):2279–2283
Jing E, Emanuelli B, Hirschey MD, Boucher J, Lee KY, Lombard D, Verdin EM, Kahn CR (2011) Sirtuin-3 (Sirt3) regulates skeletal muscle metabolism and insulin signaling via altered mitochondrial oxidation and reactive oxygen species production. Proc Natl Acad Sci 108(35):14608–14613
Kamemura K, Hayes BK, Comer FI, Hart GW (2002) Dynamic interplay between O-glycosylation and O-phosphorylation of nucleocytoplasmic proteins alternative glycosylation/phosphorylation of THR-58, a known mutational hot spot of c-Myc in lymphomas, is regulated by mitogens. J Biol Chem 277(21):19229–19235
Karbowski M, Spodnik JH, Teranishi MA, Wozniak M, Nishizawa Y, Usukura J, Wakabayashi T (2001) Opposite effects of microtubule-stabilizing and microtubule-destabilizing drugs on biogenesis of mitochondria in mammalian cells. J Cell Sci 114(2):281–291
Kaul Z, Yaguchi T, Kaul SC, Wadhwa R (2006) Quantum dot-based protein imaging and functional significance of two mitochondrial chaperones in cellular senescence and carcinogenesis. Ann N Y Acad Sci 1067(1):469–473
Kennelly PJ, Krebs EG (1991) Consensus sequences as substrate specificity determinants for protein kinases and protein phosphatases. J Biol Chem 266(24):15555–15558
Khan IU, Wallin R, Gupta RS, Kammer GM (1998) Protein kinase A-catalyzed phosphorylation of heat shock protein 60 chaperone regulates its attachment to histone 2B in the T lymphocyte plasma membrane. Proc Natl Acad Sci 95(18):10425–10430
Kikuchi I, Nakayama Y, Morinaga T, Fukumoto Y, Yamaguchi N (2010) A decrease in cyclin B1 levels leads to polyploidization in DNA damage-induced senescence. Cell Biol Int 34(6):645–653
Kim HJ, Bae SC (2011) Histone deacetylase inhibitors: molecular mechanisms of action and clinical trials as anti-cancer drugs. Am J Transl Res 3(2):166
Kim HR, Kang HS, Do Kim H (1999) Geldanamycin induces heat shock protein expression through activation of HSF1 in K562 erythroleukemic cells. IUBMB Life 48(4):429–433
Kim HS, Kim EM, Lee J, Yang WH, Park TY, Kim YM, Cho JW (2006) Heat shock protein 60 modified with O-linked N-acetylglucosamine is involved in pancreatic β-cell death under hyperglycemic conditions. FEBS Lett 580(9):2311–2316
Kirschbaum M, Gojo I, Goldberg SL, Bredeson C, Kujawski LA, Yang A, Marks P, Frankel P, Sun X, Tosolini A, Eid JE (2014) A phase 1 clinical trial of vorinostat in combination with decitabine in patients with acute myeloid leukaemia or myelodysplastic syndrome. Br J Haematol 167(2):185–193
Koeck T, Corbett JA, Crabb JW, Stuehr DJ, Aulak KS (2009) Glucose-modulated tyrosine nitration in beta cells: targets and consequences. Arch Biochem Biophys 484(2):221–231
Koll H, Guiard B, Rassow J, Ostermann J, Horwich AL, Neupert W, Hartl FU (1992) Antifolding activity of hsp60 couples protein import into the mitochondrial matrix with export to the intermembrane space. Cell 68(6):1163–1175
Komander D, Rape M (2012) The ubiquitin code. Annu Rev Biochem 81:203–229
Kurz EU, Douglas P, Lees-Miller SP (2004) Doxorubicin activates ATM-dependent phosphorylation of multiple downstream targets in part through the generation of reactive oxygen species. J Biol Chem 279(51):53272–53281
Lai MT, Huang KL, Chang WM, Lai YK (2003) Geldanamycin induction of grp78 requires activation of reactive oxygen species via ER stress responsive elements in 9L rat brain tumour cells. Cell Signal 15(6):585–595
Lakey JR, Suarez-Pinzon WL, Strynadka K, Korbutt GS, Rajotte RV, Mabley JG, Szabó C, Rabinovitch A (2001) Peroxynitrite is a mediator of cytokine-induced destruction of human pancreatic islet β cells. Lab Investig 81(12):1683
Lauricella M, Ciraolo A, Carlisi D, Vento R, Tesoriere G (2012) SAHA/TRAIL combination induces detachment and anoikis of MDA-MB231 and MCF-7 breast cancer cells. Biochimie 94(2):287–299
Lee BC, Dikiy A, Kim HY, Gladyshev VN (2009) Functions and evolution of selenoprotein methionine sulfoxide reductases. Biochim Biophys Acta (BBA)-Gen Subj 1790(11):1471–1477
Lek M, Karczewski KJ, Minikel EV, Samocha KE, Banks E, Fennell T, O’Donnell-Luria AH, Ware JS, Hill AJ, Cummings BB, Tukiainen T (2016) Analysis of protein-coding genetic variation in 60,706 humans. Nature 536(7616):285
Letunic I, Copley RR, Schmidt S, Ciccarelli FD, Doerks T, Schultz J, Ponting CP, Bork P (2004) SMART 4.0: towards genomic data integration. Nucleic Acids Res 32(suppl_1):D142–D144
Leung WH, Vong QP, Lin W, Bouck D, Wendt S, Sullivan E, Li Y, Bari R, Chen T, Leung W (2015) PRL-3 mediates the protein maturation of ULBP2 by regulating the tyrosine phosphorylation of HSP60. J Immunol 194(6):2930–2941
Levy-Rimler G, Viitanen P, Weiss C, Sharkia R, Greenberg A, Niv A, Lustig A, Delarea Y, Azem A (2001) The effect of nucleotides and mitochondrial chaperonin 10 on the structure and chaperone activity of mitochondrial chaperonin 60. Eur J Biochem 268(12):3465–3472
Li XS, Xu Q, Fu XY, Luo WS (2014a) Heat shock protein 60 overexpression is associated with the progression and prognosis in gastric cancer. PLoS One 9(9):e107507
Li Y, Malkaram SA, Zhou J, Zempleni J (2014b) Lysine biotinylation and methionine oxidation in the heat shock protein HSP60 synergize in the elimination of reactive oxygen species in human cell cultures. J Nutr Biochem 25(4):475–482
Lianos GD, Alexiou GA, Mangano A, Mangano A, Rausei S, Boni L, Dionigi G, Roukos DH (2015) The role of heat shock proteins in cancer. Cancer Lett 360(2):114–118
Lim Y, Lee E, Lee J, Oh S, Kim S (2008) Down-regulation of asymmetric arginine methylation during replicative and H2O2-induced premature senescence in WI-38 human diploid fibroblasts. J Biochem 144(4):523–529
Lim Y, Hong E, Kwon D, Lee E (2010) Proteomic identification and comparative analysis of asymmetrically arginine-methylated proteins in immortalized, young and senescent cells. Electrophoresis 31(23–24):3823–3833
Liu K, Paterson AJ, Chin E, Kudlow JE (2000) Glucose stimulates protein modification by O-linked GlcNAc in pancreatic β cells: linkage of O-linked GlcNAc to β cell death. Proc Natl Acad Sci 97(6):2820–2825
Lombard DB, Alt FW, Cheng HL, Bunkenborg J, Streeper RS, Mostoslavsky R, Kim J, Yancopoulos G, Valenzuela D, Murphy A, Yang Y (2007) Mammalian Sir2 homolog SIRT3 regulates global mitochondrial lysine acetylation. Mol Cell Biol 27(24):8807–8814
Lu Z, Chen Y, Aponte AM, Battaglia V, Gucek M, Sack MN (2015) Prolonged fasting identifies heat shock protein 10 as a Sirtuin 3 substrate elucidating a new mechanism linking mitochondrial protein acetylation to fatty acid oxidation enzyme folding and function. J Biol Chem 290(4):2466–2476
Lupi R, Del Guerra S, Mancarella R, Novelli M, Valgimigli L, Pedulli GF, Paolini M, Soleti A, Filipponi F, Mosca F, Boggi U (2007) Insulin secretion defects of human type 2 diabetic islets are corrected in vitro by a new reactive oxygen species scavenger. Diabetes Metab 33(5):340–345
Macario AJ, de Macario Conway E (2007) Molecular chaperones: multiple functions, pathologies, and potential applications. Front Biosci 12:2588–2600
Maedler K, Sergeev P, Ris F, Oberholzer J, Joller-Jemelka HI, Spinas GA, Kaiser N, Halban PA, Donath MY (2002) Glucose-induced β cell production of IL-1β contributes to glucotoxicity in human pancreatic islets. J Clin Invest 110(6):851–860
Magen D, Georgopoulos C, Bross P, Ang D, Segev Y, Goldsher D, Nemirovski A, Shahar E, Ravid S, Luder A, Heno B (2008) Mitochondrial hsp60 chaperonopathy causes an autosomal-recessive neurodegenerative disorder linked to brain hypomyelination and leukodystrophy. Am J Hum Genet 83(1):30–42
Marks PA, Xu WS (2009) Histone deacetylase inhibitors: potential in cancer therapy. J Cell Biochem 107(4):600–608
Martin-Latil S, Mousson L, Autret A, Colbère-Garapin F, Blondel B (2007) Bax is activated during rotavirus-induced apoptosis through the mitochondrial pathway. J Virol 81(9):4457–4464
McDowell GS, Philpott A (2013) Non-canonical ubiquitylation: mechanisms and consequences. Int J Biochem Cell Biol 45(8):1833–1842
Merendino AM, Bucchieri F, Campanella C, Marcianò V, Ribbene A, David S, Zummo G, Burgio G, Corona DF, de Macario EC, Macario AJ (2010) Hsp60 is actively secreted by human tumor cells. PLoS One 5(2):e9247
Mirzayans R, Andrais B, Hansen G, Murray D (2012) Role of in replicative senescence and DNA damage-induced premature senescence in p53-deficient human cells. Biochem Res Int 2012:951574
Monzani E, Roncone R, Galliano M, Koppenol WH, Casella L (2004) Mechanistic insight into the peroxidase catalyzed nitration of tyrosine derivatives by nitrite and hydrogen peroxide. Eur J Biochem 271(5):895–906
Moskovitz J, Oien DB (2010) Protein carbonyl and the methionine sulfoxide reductase system. Antioxid Redox Signal 12(3):405–415
Nahleh Z, Tfayli A, Najm A, El Sayed A, Nahle Z (2012) Heat shock proteins in cancer: targeting the ‘chaperones’. Future Med Chem 4(7):927–935
Narang MA, Dumas R, Ayer LM, Gravel RA (2004) Reduced histone biotinylation in multiple carboxylase deficiency patients: a nuclear role for holocarboxylase synthetase. Hum Mol Genet 13(1):15–23
Nielsen KL, Cowan NJ (1998) A single ring is sufficient for productive chaperonin-mediated folding in vivo. Mol Cell 2(1):93–99
Nisemblat S, Yaniv O, Parnas A, Frolow F, Azem A (2015) Crystal structure of the human mitochondrial chaperonin symmetrical football complex. Proc Natl Acad Sci 112(19):6044–6049
Osterloh A, Meier-Stiegen F, Veit A, Fleischer B, von Bonin A, Breloer M (2004) Lipopolysaccharide-free heat shock protein 60 activates T cells. J Biol Chem 279(46):47906–47911
Pacher P, Beckman JS, Liaudet L (2007) Nitric oxide and peroxynitrite in health and disease. Physiol Rev 87(1):315–424
Pahlich S, Zakaryan RP, Gehring H (2006) Protein arginine methylation: cellular functions and methods of analysis. Biochim Biophys Acta (BBA)-Proteins Proteomics 1764(12):1890–1903
Pickart CM, Eddins MJ (2004) Ubiquitin: structures, functions, mechanisms. Biochim Biophys Acta (BBA)-Mol Cell Res 1695(1–3):55–72
Powers MV, Workman P (2007) Inhibitors of the heat shock response: biology and pharmacology. FEBS Lett 581(19):3758–3769
Pyhtila B, Zheng T, Lager PJ, Keene JD, Reedy MC, Nicchitta CV (2008) Signal sequence-and translation-independent mRNA localization to the endoplasmic reticulum. RNA 14(3):445–453
Quintana FJ, Cohen IR (2011) The HSP60 immune system network. Trends Immunol 32(2):89–95
Radi R (2004) Nitric oxide, oxidants, and protein tyrosine nitration. Proc Natl Acad Sci 101(12):4003–4008
Radi R (2012) Protein tyrosine nitration: biochemical mechanisms and structural basis of functional effects. Acc Chem Res 46(2):550–559
Rakonczay Z Jr, Boros I, Jarmay K, Hegyi P, Lonovics J, Takacs T (2003) Ethanol administration generates oxidative stress in the pancreas and liver, but fails to induce heat-shock proteins in rats. J Gastroenterol Hepatol 18(7):858–867
Rao R, Fiskus W, Ganguly S, Kambhampati S, Bhalla KN (2012) HDAC inhibitors and chaperone function. Adv Cancer Res 116:239–262. Academic Press
Rappa F, Farina F, Zummo G, David S, Campanella C, Carini F, Tomasello G, Damiani P, Cappello F, De Macario EC, Macario AJ (2012) HSP-molecular chaperones in cancer biogenesis and tumor therapy: an overview. Anticancer Res 32(12):5139–5150
Rardin MJ, Newman JC, Held JM, Cusack MP, Sorensen DJ, Li B, Schilling B, Mooney SD, Kahn CR, Verdin E, Gibson BW (2013) Label-free quantitative proteomics of the lysine acetylome in mitochondria identifies substrates of SIRT3 in metabolic pathways. Proc Natl Acad Sci 110(16):6601–6606
Raulet DH, Gasser S, Gowen BG, Deng W, Jung H (2013) Regulation of ligands for the NKG2D activating receptor. Annu Rev Immunol 31:413–441
Rhein VF, Carroll J, He J, Ding S, Fearnley IM, Walker JE (2014) Human METTL20 methylates lysine residues adjacent to the recognition loop of the electron transfer flavoprotein in mitochondria. J Biol Chem 289(35):24640–24651
Rikova K, Guo A, Zeng Q, Possemato A, Yu J, Haack H, Nardone J, Lee K, Reeves C, Li Y, Hu Y (2007) Global survey of phosphotyrosine signaling identifies oncogenic kinases in lung cancer. Cell 131(6):1190–1203
Roninson IB (2002) Oncogenic functions of tumour suppressor p21Waf1/Cip1/Sdi1: association with cell senescence and tumour-promoting activities of stromal fibroblasts. Cancer Lett 179(1):1–14
Salih HR, Rammensee HG, Steinle A (2002) Cutting edge: down-regulation of MICA on human tumors by proteolytic shedding. J Immunol 169(8):4098–4102
Sarangi U, Singh MK, Abhijnya KVV, Reddy LPA, Prasad BS, Pitke VV, Paithankar K, Sreedhar AS (2013) Hsp60 chaperonin acts as barrier to pharmacologically induced oxidative stress mediated apoptosis in tumor cells with differential stress response. Drug Target Insights 7:DTI-S12513
Schnell JD, Hicke L (2003) Non-traditional functions of ubiquitin and ubiquitin-binding proteins. J Biol Chem 278(38):35857–35860
Schwer B, North BJ, Frye RA, Ott M, Verdin E (2002) The human silent information regulator (Sir) 2 homologue hSIRT3 is a mitochondrial nicotinamide adenine dinucleotide–dependent deacetylase. J Cell Biol 158(4):647–657
Semba S, Mizuuchi E, Yokozaki H (2010) Requirement of phosphatase of regenerating liver-3 for the nucleolar localization of nucleolin during the progression of colorectal carcinoma. Cancer Sci 101(10):2254–2261
Shan YX, Liu TJ, Su HF, Samsamshariat A, Mestril R, Wang PH (2003) Hsp10 and Hsp60 modulate Bcl-2 family and mitochondria apoptosis signaling induced by doxorubicin in cardiac muscle cells. J Mol Cell Cardiol 35(9):1135–1143
Shi T, Wang F, Stieren E, Tong Q (2005) SIRT3, a mitochondrial sirtuin deacetylase, regulates mitochondrial function and thermogenesis in brown adipocytes. J Biol Chem 280(14):13560–13567
Sol EM, Wagner SA, Weinert BT, Kumar A, Kim HS, Deng CX, Choudhary C (2012) Proteomic investigations of lysine acetylation identify diverse substrates of mitochondrial deacetylase sirt3. PLoS One 7(12):e50545
Soltys BJ, Gupta RS (1996) Immunoelectron microscopic localization of the 60-kDa heat shock chaperonin protein (Hsp60) in mammalian cells. Exp Cell Res 222(1):16–27
Soltys BJ, Gupta RS (1997) Cell surface localization of the 60 kDa heat shock chaperonin protein (hsp60) in mammalian cells. Cell Biol Int 21(5):315–320
Song YS, Lee BY, Hwang ES (2005) Dinstinct ROS and biochemical profiles in cells undergoing DNA damage-induced senescence and apoptosis. Mech Ageing Dev 126(5):580–590
Spallarossa P, Altieri P, Aloi C, Garibaldi S, Barisione C, Ghigliotti G, Fugazza G, Barsotti A, Brunelli C (2009) Doxorubicin induces senescence or apoptosis in rat neonatal cardiomyocytes by regulating the expression levels of the telomere binding factors 1 and 2. Am J Phys Heart Circ Phys 297:H2169–H2181
Spiro RG (2002) Protein glycosylation: nature, distribution, enzymatic formation, and disease implications of glycopeptide bonds. Glycobiology 12(4):43R–56R
Stadtman ER (2006) Protein oxidation and aging. Free Radic Res 40(12):1250–1258
Straus DJ, Hamlin PA, Matasar MJ, Palomba ML, Drullinsky PR, Zelenetz AD, Gerecitano JF et al (2015) Phase I/II trial of vorinostat with rituximab, cyclophosphamide, etoposide and prednisone as palliative treatment for elderly patients with relapsed or refractory diffuse large B-cell lymphoma not eligible for autologous stem cell transplantation. Br J Haematol 168(5):663–670
Suarez J, Wang H, Ouyang K, Scott B (2014) Cardiac myocyte-specific deletion of heat shock protein 10 results in altered cytosolic and mitochondrial protein expression (699.6). FASEB J 28(1_supplement):699–696
Suarez-Pinzon WL, Szabó C, Rabinovitch A (1997) Development of autoimmune diabetes in NOD mice is associated with the formation of peroxynitrite in pancreatic islet β-cells. Diabetes 46(5):907–911
Szabó C, Mabley JG, Moeller SM, Shimanovich R, Pacher P, Virág L, Soriano FG, Van Duzer JH, Williams W, Salzman AL, Groves JT (2002) Part I: pathogenetic role of peroxynitrite in the development of diabetes and diabetic vascular complications: studies with FP15, a novel potent peroxynitrite decomposition catalyst. Mol Med 8(10):571–580
Tang H, Tian E, Liu C, Wang Q, Deng H (2013) Oxidative stress induces monocyte necrosis with enrichment of cell-bound albumin and overexpression of endoplasmic reticulum and mitochondrial chaperones. PLoS One 8(3):e59610
Théry C, Ostrowski M, Segura E (2009) Membrane vesicles as conveyors of immune responses. Nat Rev Immunol 9(8):581
Thomson L (2015) 3-nitrotyrosine modified proteins in atherosclerosis. Dis Markers 2015:708282
Tian P, Estes MK, Hu Y, Ball JM, Zeng CQ, Schilling WP (1995) The rotavirus nonstructural glycoprotein NSP4 mobilizes Ca2+ from the endoplasmic reticulum. J Virol 69(9):5763–5772
Tomasello G, Rodolico V, Zerilli M, Martorana A, Bucchieri F, Pitruzzella A, Gammazza AM, David S, Rappa F, Zummo G, Damiani P (2011) Changes in immunohistochemical levels and subcellular localization after therapy and correlation and colocalization with CD68 suggest a pathogenetic role of Hsp60 in ulcerative colitis. Appl Immunohistochem Mol Morphol 19(6):552–561
Touriol C, Bornes S, Bonnal S, Audigier S, Prats H, Prats AC, Vagner S (2003) Generation of protein isoform diversity by alternative initiation of translation at non-AUG codons. Biol Cell 95(3–4):169–178
Tsai YP, Teng SC, Wu KJ (2008) Direct regulation of HSP60 expression by c-MYC induces transformation. FEBS Lett 582(29):4083–4088
Tsai YP, Yang MH, Huang CH, Chang SY, Chen PM, Liu CJ, Teng SC, Wu KJ (2009) Interaction between HSP60 and β-catenin promotes metastasis. Carcinogenesis 30(6):1049–1057
Tu Y, Hershman DL, Bhalla K, Fiskus W, Pellegrino CM, Andreopoulou E, Makower D, Kalinsky K, Fehn K, Fineberg S, Negassa A (2014) A phase I-II study of the histone deacetylase inhibitor vorinostat plus sequential weekly paclitaxel and doxorubicin-cyclophosphamide in locally advanced breast cancer. Breast Cancer Res Treat 146(1):145–152
Van Eden W, Wick G, Albani S, Cohen I (2007) Stress, heat shock proteins, and autoimmunity. Ann N Y Acad Sci 1113(1):217–237
Waldhauer I, Steinle A (2006) Proteolytic release of soluble UL16-binding protein 2 from tumor cells. Cancer Res 66(5):2520–2526
Waldhauer I, Goehlsdorf D, Gieseke F, Weinschenk T, Wittenbrink M, Ludwig A, Stevanovic S, Rammensee HG, Steinle A (2008) Tumor-associated MICA is shed by ADAM proteases. Cancer Res 68(15):6368–6376
Walgren JL, Vincent TS, Schey KL, Buse MG (2003) High glucose/insulin promote O-GlcNAc modification of proteins including α-tubulin. Am J Physiol-Endocrinol Metab 284:E424–E434
Wang L, Shen Y, Song R, Sun Y, Xu J, Xu Q (2009) An anticancer effect of curcumin mediated by down-regulating phosphatase of regenerating liver-3 expression on highly metastatic melanoma cells. Mol Pharmacol 76(6):1238–1245
Whelan SA, Lane MD, Hart GW (2008) Regulation of the O-linked β-N-acetylglucosamine transferase by insulin signaling. J Biol Chem 283(31):21411–21417
Wolf SS (2009) The protein arginine methyltransferase family: an update about function, new perspectives and the physiological role in humans. Cell Mol Life Sci 66(13):2109–2121
Yamaguchi K, Chikumi H, Shimizu A, Takata M, Kinoshita N, Hashimoto K, Nakamoto M, Matsunaga S, Kurai J, Miyake N, Matsumoto S (2012) Diagnostic and prognostic impact of serum-soluble UL 16-binding protein 2 in lung cancer patients. Cancer Sci 103(8):1405–1413
Yang Y, Fiskus W, Yong B, Atadja P, Takahashi Y, Pandita TK, Wang HG, Bhalla KN (2013) Acetylated hsp70 and KAP1-mediated Vps34 SUMOylation is required for autophagosome creation in autophagy. Proc Natl Acad Sci 110(17):6841–6846
Yechoor VK, Patti ME, Ueki K, Laustsen PG, Saccone R, Rauniyar R, Kahn CR (2004) Distinct pathways of insulin-regulated versus diabetes-regulated gene expression: an in vivo analysis in MIRKO mice. Proc Natl Acad Sci 101(47):16525–16530
Yogev O, Pines O (2011) Dual targeting of mitochondrial proteins: mechanism, regulation and function. Biochim Biophys Acta (BBA)-Biomembr 1808(3):1012–1020
Zambrano JL, Díaz Y, Peña F, Vizzi E, Ruiz MC, Michelangeli F, Liprandi F, Ludert JE (2008) Silencing of rotavirus NSP4 or VP7 expression reduces alterations in Ca2+ homeostasis induced by infection of cultured cells. J Virol 82(12):5815–5824
Zanin-Zhorov A, Bruck R, Tal G, Oren S, Aeed H, Hershkoviz R, Cohen IR, Lider O (2005) Heat shock protein 60 inhibits Th1-mediated hepatitis model via innate regulation of Th1/Th2 transcription factors and cytokines. J Immunol 174(6):3227–3236
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Baron, B. (2019). Role of the Post-translational Modifications of HSP60 in Disease. In: Asea, A., Kaur, P. (eds) Heat Shock Protein 60 in Human Diseases and Disorders. Heat Shock Proteins, vol 18. Springer, Cham. https://doi.org/10.1007/978-3-030-23154-5_6
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