The role of the molecular chaperone CCT in protein folding and mediation of cytoskeleton-associated processes: implications for cancer cell biology.
Actin
Cancer
Chaperonin
Cytoskeleton
Tubulin
Journal
Cell stress & chaperones
ISSN: 1466-1268
Titre abrégé: Cell Stress Chaperones
Pays: Netherlands
ID NLM: 9610925
Informations de publication
Date de publication:
01 2019
01 2019
Historique:
received:
13
07
2018
accepted:
09
11
2018
revised:
02
11
2018
pubmed:
7
12
2018
medline:
19
6
2019
entrez:
4
12
2018
Statut:
ppublish
Résumé
The chaperonin-containing tailless complex polypeptide 1 (CCT) is required in vivo for the folding of newly synthesized tubulin and actin proteins and is thus intrinsically connected to all cellular processes that rely on the microtubule and actin filament components of the cytoskeleton, both of which are highly regulated and dynamic assemblies. In addition to CCT acting as a protein folding oligomer, further modes of CCT action mediated either by the CCT oligomer itself or via CCT subunits in their monomeric forms can influence processes associated with assembled actin filaments and microtubules. Thus, there is an extended functional role for CCT with regard to its major folding substrates with a complex interplay between CCT as folding machine for tubulin/actin and as a modulator of processes involving the assembled cytoskeleton. As cell division, directed cell migration, and invasion are major drivers of cancer development and rely on the microtubule and actin filament components of the cytoskeleton, CCT activity is fundamentally linked to cancer. Furthermore, the CCT oligomer also folds proteins connected to cell cycle progression and interacts with several other proteins that are linked to cancer such as tumor-suppressor proteins and regulators of the cytoskeleton, while CCT monomer function can influence cell migration. Thus, understanding CCT activity is important for many aspects of cancer cell biology and may reveal new ways to target tumor growth and invasion.
Identifiants
pubmed: 30506376
doi: 10.1007/s12192-018-0949-3
pii: 10.1007/s12192-018-0949-3
pmc: PMC6363620
doi:
Substances chimiques
Chaperonin Containing TCP-1
EC 3.6.1.-
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Review
Langues
eng
Sous-ensembles de citation
IM
Pagination
17-27Références
Amit M, Weisberg SJ, Nadler-Holly M, McCormack EA, Feldmesser E, Kaganovich D, Willison KR, Horovitz A (2010) Equivalent mutations in the eight subunits of the chaperonin CCT produce dramatically different cellular and gene expression phenotypes. J Mol Biol 401:532–543. https://doi.org/10.1016/j.jmb.2010.06.037
doi: 10.1016/j.jmb.2010.06.037
pubmed: 20600117
Brackley KI, Grantham J (2010) Subunits of the chaperonin CCT interact with F-actin and influence cell shape and cytoskeletal assembly. Exp Cell Res 316:543–553. https://doi.org/10.1016/j.yexcr.2009.11.003
doi: 10.1016/j.yexcr.2009.11.003
pubmed: 19913534
Brackley KI, Grantham J (2011) Interactions between the actin filament capping and severing protein gelsolin and the molecular chaperone CCT: evidence for nonclassical substrate interactions. Cell Stress Chaperones 16:173–179. https://doi.org/10.1007/s12192-010-0230-x
doi: 10.1007/s12192-010-0230-x
pubmed: 20890741
Burtnick LD, Robinson RC, Choe S (2001) Structure and function of gelsolin. Results Probl Cell Differ 32:201–211
doi: 10.1007/978-3-540-46560-7_14
Camasses A, Bogdanova A, Shevchenko A, Zachariae W (2003) The CCT chaperonin promotes activation of the anaphase-promoting complex through the generation of functional Cdc20. Mol Cell 12:87–100
doi: 10.1016/S1097-2765(03)00244-2
Chen L, Sigler PB (1999) The crystal structure of a GroEL/peptide complex: plasticity as a basis for substrate diversity. Cell 99:757–768
doi: 10.1016/S0092-8674(00)81673-6
Cong Y, Baker ML, Jakana J, Woolford D, Miller EJ, Reissmann S, Kumar RN, Redding-Johanson AM, Batth TS, Mukhopadhyay A, Ludtke SJ, Frydman J, Chiu W (2010) 4.0-A resolution cryo-EM structure of the mammalian chaperonin TRiC/CCT reveals its unique subunit arrangement. Proc Natl Acad Sci U S A 107:4967–4972. https://doi.org/10.1073/pnas.0913774107
doi: 10.1073/pnas.0913774107
pubmed: 20194787
pmcid: 2841888
Cunningham C, Stossel T, Kwiatkowski D (1991) Enhanced motility in NIH 3T3 fibroblasts that overexpress gelsolin. Science 251(4998):1233–1236
Dekker C, Roe SM, McCormack EA, Beuron F, Pearl LH, Willison KR (2011) The crystal structure of yeast CCT reveals intrinsic asymmetry of eukaryotic cytosolic chaperonins. EMBO J 30:3078–3090. https://doi.org/10.1038/emboj.2011.208
doi: 10.1038/emboj.2011.208
pubmed: 21701561
pmcid: 3160183
Dekker C, Stirling PC, McCormack EA, Filmore H, Paul A, Brost RL, Costanzo M, Boone C, Leroux MR, Willison KR (2008) The interaction network of the chaperonin CCT. EMBO J 27:1827–1839. https://doi.org/10.1038/emboj.2008.108
doi: 10.1038/emboj.2008.108
pubmed: 18511909
pmcid: 2486426
Dixit R, Levy JR, Tokito M, Ligon LA, Holzbaur EL (2008) Regulation of dynactin through the differential expression of p150Glued isoforms. J Biol Chem 283:33611–33619. https://doi.org/10.1074/jbc.M804840200
doi: 10.1074/jbc.M804840200
pubmed: 18812314
pmcid: 2586252
Echbarthi M, Vallin J, Grantham J (2018) Interactions between monomeric CCTdelta and p150(Glued): a novel function for CCTdelta at the cell periphery distinct from the protein folding activity of the molecular chaperone CCT. Exp Cell Res 370:137–149. https://doi.org/10.1016/j.yexcr.2018.06.018
doi: 10.1016/j.yexcr.2018.06.018
pubmed: 29913154
Elliott KL, Svanstrom A, Spiess M, Karlsson R, Grantham J (2015) A novel function of the monomeric CCTepsilon subunit connects the serum response factor pathway to chaperone-mediated actin folding. Mol Biol Cell 26:2801–2809. https://doi.org/10.1091/mbc.E15-01-0048
doi: 10.1091/mbc.E15-01-0048
pubmed: 26063733
pmcid: 4571339
Feldman DE, Thulasiraman V, Ferreyra RG, Frydman J (1999) Formation of the VHL-elongin BC tumor suppressor complex is mediated by the chaperonin. TRiC Mol Cell 4:1051–1061
doi: 10.1016/S1097-2765(00)80233-6
Grantham J (2010) The eukaryotic chaperonin CCT (TRiC):structure, mechanisms of action and substrate diversity. In: Durante P, Colucci L (eds) Molecular chaperones: roles structures and mechanisms. Nova Science Publishing, New York
Grantham J, Brackley KI, Willison KR (2006) Substantial CCT activity is required for cell cycle progression and cytoskeletal organization in mammalian cells. Exp Cell Res 312:2309–2324. https://doi.org/10.1016/j.yexcr.2006.03.028
doi: 10.1016/j.yexcr.2006.03.028
pubmed: 16765944
Grantham J, Lassing I, Karlsson R (2012) Controlling the cortical actin motor Protoplasma 249:1001–1015 https://doi.org/10.1007/s00709-012-0403-9
Grantham J, Ruddock LW, Roobol A, Carden MJ (2002) Eukaryotic chaperonin containing T-complex polypeptide 1 interacts with filamentous actin and reduces the initial rate of actin polymerization in vitro. Cell Stress Chaperones 7:235–242
doi: 10.1379/1466-1268(2002)007<0235:ECCTCP>2.0.CO;2
Gruber R, Levitt M, Horovitz A (2017) Sequential allosteric mechanism of ATP hydrolysis by the CCT/TRiC chaperone is revealed through Arrhenius analysis. Proc Natl Acad Sci U S A 114:5189–5194. https://doi.org/10.1073/pnas.1617746114
doi: 10.1073/pnas.1617746114
pubmed: 28461478
pmcid: 5441784
Guest ST, Kratche ZR, Bollig-Fischer A, Haddad R, Ethier SP (2015) Two members of the TRiC chaperonin complex, CCT2 and TCP1 are essential for survival of breast cancer cells and are linked to driving oncogenes. Exp Cell Res 332:223–235. https://doi.org/10.1016/j.yexcr.2015.02.005
doi: 10.1016/j.yexcr.2015.02.005
pubmed: 25704758
Joachimiak LA, Walzthoeni T, Liu CW, Aebersold R, Frydman J (2014) The structural basis of substrate recognition by the eukaryotic chaperonin TRiC/CCT. Cell 159:1042–1055. https://doi.org/10.1016/j.cell.2014.10.042
doi: 10.1016/j.cell.2014.10.042
pubmed: 25416944
pmcid: 4298165
Kabir MA et al (2005) Physiological effects of unassembled chaperonin Cct subunits in the yeast Saccharomyces cerevisiae. Yeast 22:219–239. https://doi.org/10.1002/yea.1210
doi: 10.1002/yea.1210
pubmed: 15704212
Kaisari S, Sitry-Shevah D, Miniowitz-Shemtov S, Teichner A, Hershko A (2017) Role of CCT chaperonin in the disassembly of mitotic checkpoint complexes. Proc Natl Acad Sci U S A 114:956–961. https://doi.org/10.1073/pnas.1620451114
doi: 10.1073/pnas.1620451114
pubmed: 28096334
pmcid: 5293070
Kalisman N, Adams CM, Levitt M (2012) Subunit order of eukaryotic TRiC/CCT chaperonin by cross-linking, mass spectrometry, and combinatorial homology modeling. Proc Natl Acad Sci U S A 109:2884–2889. https://doi.org/10.1073/pnas.1119472109
doi: 10.1073/pnas.1119472109
pubmed: 22308438
pmcid: 3287007
Kasembeli M, Lau WC, Roh SH, Eckols TK, Frydman J, Chiu W, Tweardy DJ (2014) Modulation of STAT3 folding and function by TRiC/CCT chaperonin. PLoS Biol 12:e1001844. https://doi.org/10.1371/journal.pbio.1001844
doi: 10.1371/journal.pbio.1001844
pubmed: 24756126
pmcid: 3995649
Kim S, Willison KR, Horwich AL (1994) Cystosolic chaperonin subunits have a conserved ATPase domain but diverged polypeptide-binding domains. Trends Biochem Sci 19:543–548
doi: 10.1016/0968-0004(94)90058-2
Leitner A, Joachimiak LA, Bracher A, Mönkemeyer L, Walzthoeni T, Chen B, Pechmann S, Holmes S, Cong Y, Ma B, Ludtke S, Chiu W, Hartl FU, Aebersold R, Frydman J (2012) The molecular architecture of the eukaryotic chaperonin TRiC/CCT. Structure 20:814–825. https://doi.org/10.1016/j.str.2012.03.007
doi: 10.1016/j.str.2012.03.007
pubmed: 22503819
pmcid: 3350567
Liou AK, Willison KR (1997) Elucidation of the subunit orientation in CCT (chaperonin containing TCP1) from the subunit composition of CCT micro-complexes. EMBO J 16:4311–4316
doi: 10.1093/emboj/16.14.4311
Liu X, Lin CY, Lei M, Yan S, Zhou T, Erikson RL (2005) CCT chaperonin complex is required for the biogenesis of functional Plk1. Mol Cell Biol 25:4993–5010. https://doi.org/10.1128/MCB.25.12.4993-5010.2005
doi: 10.1128/MCB.25.12.4993-5010.2005
pubmed: 15923617
pmcid: 1140568
Llorca O, Martin-Benito J, Grantham J, Ritco-Vonsovici M, Willison KR, Carrascosa JL, Valpuesta JM (2001) The ‘sequential allosteric ring’ mechanism in the eukaryotic chaperonin-assisted folding of actin and tubulin. EMBO J 20:4065–4075. https://doi.org/10.1093/emboj/20.15.4065
doi: 10.1093/emboj/20.15.4065
pubmed: 11483510
pmcid: 149171
Llorca O et al (2000) Eukaryotic chaperonin CCT stabilizes actin and tubulin folding intermediates in open quasi-native conformations. EMBO J 19:5971–5979. https://doi.org/10.1093/emboj/19.22.5971
doi: 10.1093/emboj/19.22.5971
pubmed: 305829
pmcid: 305829
Llorca O, McCormack EA, Hynes G, Grantham J, Cordell J, Carrascosa JL, Willison KR, Fernandez JJ, Valpuesta JM (1999) Eukaryotic type II chaperonin CCT interacts with actin through specific subunits. Nature 402:693–696. https://doi.org/10.1038/45294
doi: 10.1038/45294
pubmed: 10604479
Lundin VF, Srayko M, Hyman AA, Leroux MR (2008) Efficient chaperone-mediated tubulin biogenesis is essential for cell division and cell migration in C. elegans. Dev Biol 313:320–334. https://doi.org/10.1016/j.ydbio.2007.10.022
doi: 10.1016/j.ydbio.2007.10.022
pubmed: 18062952
Matalon O, Horovitz A, Levy ED (2014) Different subunits belonging to the same protein complex often exhibit discordant expression levels and evolutionary properties. Curr Opin Struct Biol 26:113–120. https://doi.org/10.1016/j.sbi.2014.06.001
doi: 10.1016/j.sbi.2014.06.001
pubmed: 24997301
Melville MW, McClellan AJ, Meyer AS, Darveau A, Frydman J (2003) The Hsp70 and TRiC/CCT chaperone systems cooperate in vivo to assemble the von Hippel-Lindau tumor suppressor complex. Mol Cell Biol 23:3141–3151
doi: 10.1128/MCB.23.9.3141-3151.2003
Mielnicki LM, Ying AM, Head KL, Asch HL, Asch BB (1999) Epigenetic Regulation of Gelsolin Expression in Human Breast Cancer Cells. Exp Cell Res 249(1):161–176
Munoz IG et al (2011) Crystal structure of the open conformation of the mammalian chaperonin CCT in complex with tubulin. Nat Struct Mol Biol 18:14–19. https://doi.org/10.1038/nsmb.1971
doi: 10.1038/nsmb.1971
pubmed: 21151115
Olson MF, Sahai E (2009) The actin cytoskeleton in cancer cell motility. Clin Exp Metastasis 26:273–287. https://doi.org/10.1007/s10585-008-9174-2
doi: 10.1007/s10585-008-9174-2
pubmed: 18498004
Pappenberger G, Wilsher JA, Roe SM, Counsell DJ, Willison KR, Pearl LH (2002) Crystal structure of the CCTgamma apical domain: implications for substrate binding to the eukaryotic cytosolic chaperonin. J Mol Biol 318:1367–1379
doi: 10.1016/S0022-2836(02)00190-0
Reissmann S, Joachimiak LA, Chen B, Meyer AS, Nguyen A, Frydman J (2012) A gradient of ATP affinities generates an asymmetric power stroke driving the chaperonin TRIC/CCT folding cycle. Cell Rep 2:866–877. https://doi.org/10.1016/j.celrep.2012.08.036
doi: 10.1016/j.celrep.2012.08.036
pubmed: 23041314
pmcid: 23041314
Roobol A, Sahyoun ZP, Carden MJ (1999) Selected subunits of the cytosolic chaperonin associate with microtubules assembled in vitro. J Biol Chem 274:2408–2415
doi: 10.1074/jbc.274.4.2408
Saegusa K, Sato M, Sato K, Nakajima-Shimada J, Harada A, Sato K (2014) Caenorhabditis elegans chaperonin CCT/TRiC is required for actin and tubulin biogenesis and microvillus formation in intestinal epithelial cells. Mol Biol Cell 25:3095–3104. https://doi.org/10.1091/mbc.E13-09-0530
doi: 10.1091/mbc.E13-09-0530
pubmed: 25143409
pmcid: 4196862
Shi X, Cheng S, Wang W (2018) Suppression of CCT3 inhibits malignant proliferation of human papillary thyroid carcinoma cell. Oncol Lett 15:9202–9208. https://doi.org/10.3892/ol.2018.8496
doi: 10.3892/ol.2018.8496
pubmed: 29805652
pmcid: 5958781
Sotiropoulos A, Gineitis D, Copeland J, Treisman R (1999) Signal-regulated activation of serum response factor is mediated by changes in actin dynamics. Cell 98:159–169
doi: 10.1016/S0092-8674(00)81011-9
Spiess M, Echbarthi M, Svanstrom A, Karlsson R, Grantham J (2015) Over-expression analysis of all eight subunits of the molecular chaperone CCT in mammalian cells reveals a novel function for CCTdelta. J Mol Biol 427:2757–2764. https://doi.org/10.1016/j.jmb.2015.06.007
doi: 10.1016/j.jmb.2015.06.007
pubmed: 26101841
Sternlicht H, Farr GW, Sternlicht ML, Driscoll JK, Willison K, Yaffe MB (1993) The t-complex polypeptide 1 complex is a chaperonin for tubulin and actin in vivo. Proc Natl Acad Sci U S A 90:9422–9426
doi: 10.1073/pnas.90.20.9422
Stoldt V, Rademacher F, Kehren V, Ernst JF, Pearce DA, Sherman F (1996) Review: the Cct eukaryotic chaperonin subunits of Saccharomyces cerevisiae and other yeasts. Yeast 12:523–529 https://doi.org/10.1002/(SICI)1097-0061(199605)12:6<523::AID-YEA962>3.0.CO;2-C
Sun Q, Chen G, Streb JW, Long X, Yang Y, Stoeckert CJ Jr, Miano JM (2006) Defining the mammalian CArGome. Genome Res 16:197–207. https://doi.org/10.1101/gr.4108706
doi: 10.1101/gr.4108706
pubmed: 16365378
pmcid: 1361715
Svanstrom A, Grantham J (2016) The molecular chaperone CCT modulates the activity of the actin filament severing and capping protein gelsolin in vitro. Cell Stress Chaperones 21:55–62. https://doi.org/10.1007/s12192-015-0637-5
doi: 10.1007/s12192-015-0637-5
pubmed: 26364302
Tam S, Geller R, Spiess C, Frydman J (2006) The chaperonin TRiC controls polyglutamine aggregation and toxicity through subunit-specific interactions. Nat Cell Biol 8:1155–1162. https://doi.org/10.1038/ncb1477
doi: 10.1038/ncb1477
pubmed: 16980959
pmcid: 2829982
Thulasiraman V, Yang CF, Frydman J (1999) In vivo newly translated polypeptides are sequestered in a protected folding environment. EMBO J 18:85–95. https://doi.org/10.1093/emboj/18.1.85
doi: 10.1093/emboj/18.1.85
pubmed: 9878053
pmcid: 9878053
Tian G, Kong XP, Jaglin XH, Chelly J, Keays D, Cowan NJ (2008) A pachygyria-causing alpha-tubulin mutation results in inefficient cycling with CCT and a deficient interaction with TBCB. Mol Biol Cell 19:1152–1161. https://doi.org/10.1091/mbc.E07-09-0861
doi: 10.1091/mbc.E07-09-0861
pubmed: 18199681
pmcid: 2262973
Tracy CM, Gray AJ, Cuéllar J, Shaw TS, Howlett AC, Taylor RM, Prince JT, Ahn NG, Valpuesta JM, Willardson BM (2014) Programmed cell death protein 5 interacts with the cytosolic chaperonin containing tailless complex polypeptide 1 (CCT) to regulate beta-tubulin folding. J Biol Chem 289:4490–4502. https://doi.org/10.1074/jbc.M113.542159
doi: 10.1074/jbc.M113.542159
pubmed: 24375412
Trinidad AG, Muller PA, Cuellar J, Klejnot M, Nobis M, Valpuesta JM, Vousden KH (2013) Interaction of p53 with the CCT complex promotes protein folding and wild-type p53 activity. Mol Cell 50:805–817. https://doi.org/10.1016/j.molcel.2013.05.002
doi: 10.1016/j.molcel.2013.05.002
pubmed: 23747015
pmcid: 3699784
Vang S, Corydon TJ, Børglum AD, Scott MD, Frydman J, Mogensen J, Gregersen N, Bross P (2005) Actin mutations in hypertrophic and dilated cardiomyopathy cause inefficient protein folding and perturbed filament formation. FEBS J 272:2037–2049. https://doi.org/10.1111/j.1742-4658.2005.04630.x
doi: 10.1111/j.1742-4658.2005.04630.x
pubmed: 15819894
Wang W, Goswami S, Lapidus K, Wells AL, Wyckoff JB, Sahai E, Singer RH, Segall JE, Condeelis JS (2004) Identification and testing of a gene expression signature of invasive carcinoma cells within primary mammary tumors. Cancer Res 64:8585–8594. https://doi.org/10.1158/0008-5472.CAN-04-1136
doi: 10.1158/0008-5472.CAN-04-1136
pubmed: 15574765
Van den Abbeele A, De Corte V, Van Impe K, Bruyneel E, Boucherie C, Bracke M, Vandekerckhove J, Gettemans J (2007) Downregulation of gelsolin family proteins counteracts cancer cell invasion in vitro. Cancer Lett 255(1):57–70
Vartiainen MK, Guettler S, Larijani B, Treisman R (2007) Nuclear actin regulates dynamic subcellular localization and activity of the SRF cofactor MAL. Science 316:1749–1752. https://doi.org/10.1126/science.1141084
doi: 10.1126/science.1141084
pubmed: 17588931
Willison KR (2018) The substrate specificity of eukaryotic cytosolic chaperonin CCT. Philos Trans R Soc Lond Ser B Biol Sci 373:20170192. https://doi.org/10.1098/rstb.2017.0192
doi: 10.1098/rstb.2017.0192
Yam AY, Xia Y, Lin HT, Burlingame A, Gerstein M, Frydman J (2008) Defining the TRiC/CCT interactome links chaperonin function to stabilization of newly made proteins with complex topologies. Nat Struct Mol Biol 15:1255–1262. https://doi.org/10.1038/nsmb.1515
doi: 10.1038/nsmb.1515
pubmed: 2658641
pmcid: 2658641
Yokota S, Yamamoto Y, Shimizu K, Momoi H, Kamikawa T, Yamaoka Y, Yanagi H, Yura T, Kubota H (2001) Increased expression of cytosolic chaperonin CCT in human hepatocellular and colonic carcinoma. Cell Stress Chaperones 6:345–350
doi: 10.1379/1466-1268(2001)006<0345:IEOCCC>2.0.CO;2
Yokota S, Yanagi H, Yura T, Kubota H (1999) Cytosolic chaperonin is up-regulated during cell growth. Preferential expression and binding to tubulin at G(1)/S transition through early S phase. J Biol Chem 274:37070–37078
doi: 10.1074/jbc.274.52.37070
Zhang Y, Wang Y, Wei Y, Wu J, Zhang P, Shen S, Saiyin H, Wumaier R, Yang X, Wang C, Yu L (2016) Molecular chaperone CCT3 supports proper mitotic progression and cell proliferation in hepatocellular carcinoma cells. Cancer Lett 372:101–109. https://doi.org/10.1016/j.canlet.2015.12.029
doi: 10.1016/j.canlet.2015.12.029
pubmed: 26739059
Zhao M, Spiess M, Johansson HJ, Olofsson H, Hu J, Lehtio J, Stromblad S (2017) Identification of the PAK4 interactome reveals PAK4 phosphorylation of N-WASP and promotion of Arp2/3-dependent actin polymerization. Oncotarget 8:77061–77074. https://doi.org/10.18632/oncotarget.20352
doi: 10.18632/oncotarget.20352
pubmed: 29100370
pmcid: 5652764