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TRiC/CCT Chaperonin: Structure and Function

  • Mingliang Jin
  • Caixuan Liu
  • Wenyu Han
  • Yao CongEmail author
Chapter
Part of the Subcellular Biochemistry book series (SCBI, volume 93)

Abstract

The eukaryotic group II chaperonin TRiC/CCT assists the folding of 10% of cytosolic proteins including many key structural and regulatory proteins. TRiC plays an essential role in maintaining protein homeostasis, and dysfunction of TRiC is closely related to human diseases including cancer and neurodegenerative diseases. TRiC consists of eight paralogous subunits, each of which plays a specific role in the assembly, allosteric cooperativity, and substrate recognition and folding of this complex macromolecular machine. TRiC-mediated substrate folding is regulated through its ATP-driven conformational changes. In recent years, progresses have been made on the structure, subunit arrangement, conformational cycle, and substrate folding of TRiC. Additionally, accumulating evidences also demonstrate the linkage between TRiC oligomer or monomer and diseases. In this review, we focus on the TRiC structure itself, TRiC assisted substrate folding, TRiC and disease, and the potential therapeutic application of TRiC in various diseases.

Keywords

Chaperonin TRiC/CCT Structure Function Substrate folding ATP-driven conformational changes Cryo-EM 

References

  1. Adato A, Weil D, Kalinski H, Pel-Or Y, Ayadi H, Petit C, Korostishevsky M, Bonne-Tamir B (1997) Mutation profile of all 49 exons of the human myosin VIIA gene, and haplotype analysis, in Usher 1B families from diverse origins. Am J Hum Genet 61(4):813–821.  https://doi.org/10.1086/514899CrossRefPubMedPubMedCentralGoogle Scholar
  2. 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(3):532–543.  https://doi.org/10.1016/j.jmb.2010.06.037CrossRefPubMedGoogle Scholar
  3. Antonova SV, Haffke M, Corradini E, Mikuciunas M, Low TY, Signor L, van Es RM, Gupta K, Scheer E, Vos HR, Tora L, Heck AJR, Timmers HTM, Berger I (2018) Chaperonin CCT checkpoint function in basal transcription factor TFIID assembly. Nat Struct Mol Biol.  https://doi.org/10.1038/s41594-018-0156-z
  4. Bai XC, Rajendra E, Yang G, Shi Y, Scheres SH (2015) Sampling the conformational space of the catalytic subunit of human gamma-secretase. Elife 4.  https://doi.org/10.7554/elife.11182
  5. Bakthavatsalam D, Soung RH, Tweardy DJ, Chiu W, Dixon RA, Woodside DG (2014) Chaperonin-containing TCP-1 complex directly binds to the cytoplasmic domain of the LOX-1 receptor. FEBS Lett 588(13):2133–2140.  https://doi.org/10.1016/j.febslet.2014.04.049CrossRefPubMedPubMedCentralGoogle Scholar
  6. Balchin D, Hayer-Hartl M, Hartl FU (2016) In vivo aspects of protein folding and quality control. Science 353(6294):aac4354.  https://doi.org/10.1126/science.aac4354
  7. Balchin D, Milicic G, Strauss M, Hayer-Hartl M, Hartl FU (2018) Pathway of actin folding directed by the eukaryotic chaperonin TRiC. Cell.  https://doi.org/10.1016/j.cell.2018.07.006
  8. Bassiouni R, Nemec KN, Iketani A, Flores O, Showalter A, Khaled AS, Vishnubhotla P, Sprung RW Jr, Kaittanis C, Perez JM, Khaled AR (2016) Chaperonin containing TCP-1 protein level in breast cancer cells predicts therapeutic application of a cytotoxic peptide. Clin Cancer Res 22(17):4366–4379.  https://doi.org/10.1158/1078-0432.CCR-15-2502CrossRefPubMedPubMedCentralGoogle Scholar
  9. Beck M, Baumeister W (2016) Cryo-Electron tomography: can it reveal the molecular sociology of cells in atomic detail? Trends Cell Biol 26(11):825–837.  https://doi.org/10.1016/j.tcb.2016.08.006CrossRefPubMedGoogle Scholar
  10. Behrends C, Langer CA, Boteva R, Bottcher UM, Stemp MJ, Schaffar G, Rao BV, Giese A, Kretzschmar H, Siegers K, Hartl FU (2006) Chaperonin TRiC promotes the assembly of polyQ expansion proteins into nontoxic oligomers. Mol Cell 23(6):887–897.  https://doi.org/10.1016/j.molcel.2006.08.017CrossRefPubMedGoogle Scholar
  11. Berger J, Berger S, Li M, Jacoby AS, Arner A, Bavi N, Stewart AG, Currie PD (2018) In vivo function of the chaperonin TRiC in alpha-actin folding during sarcomere assembly. Cell Rep 22(2):313–322.  https://doi.org/10.1016/j.celrep.2017.12.069CrossRefPubMedGoogle Scholar
  12. Bonné-Tamir B, Korostishevsky M, Kalinsky H, Seroussi E, Beker R, Weiss S, Godel V (1994) Genetic mapping of the gene for usher syndrome: linkage analysis in a large samaritan kindred. Genomics 20(1):36–42.  https://doi.org/10.1006/geno.1994.1124CrossRefPubMedGoogle Scholar
  13. Booth CR, Meyer AS, Cong Y, Topf M, Sali A, Ludtke SJ, Chiu W, Frydman J (2008) Mechanism of lid closure in the eukaryotic chaperonin TRiC/CCT. Nat Struct Mol Biol 15(7):746–753.  https://doi.org/10.1038/nsmb.1436CrossRefPubMedPubMedCentralGoogle Scholar
  14. Bouhouche A, Benomar A, Bouslam N, Chkili T, Yahyaoui M (2006) Mutation in the epsilon subunit of the cytosolic chaperonin-containing t-complex peptide-1 (Cct5) gene causes autosomal recessive mutilating sensory neuropathy with spastic paraplegia. J Med Genet 43(5):441–443.  https://doi.org/10.1136/jmg.2005.039230CrossRefPubMedPubMedCentralGoogle Scholar
  15. Broadley SA, Hartl FU (2009) The role of molecular chaperones in human misfolding diseases. FEBS Lett 583(16):2647–2653.  https://doi.org/10.1016/j.febslet.2009.04.029CrossRefPubMedGoogle Scholar
  16. 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(1):87–100.  https://doi.org/10.1016/s1097-2765(03)00244-2CrossRefPubMedGoogle Scholar
  17. Carr AC, Khaled AS, Bassiouni R, Flores O, Nierenberg D, Bhatti H, Vishnubhotla P, Perez JM, Santra S, Khaled AR (2017) Targeting chaperonin containing TCP1 (CCT) as a molecular therapeutic for small cell lung cancer. Oncotarget 8(66):110273–110288.  https://doi.org/10.18632/oncotarget.22681
  18. Chen X, Sullivan DS, Huffaker TC (1994) Two yeast genes with similarity to TCP-1 are required for microtubule and actin function in vivo. Proc Natl Acad Sci USA 91(19):9111–9115.  https://doi.org/10.1073/pnas.91.19.9111
  19. Chen L, Zhang Z, Qiu J, Zhang L, Luo X, Jang J (2014) Chaperonin CCT-mediated AIB1 folding promotes the growth of ERalpha-positive breast cancer cells on hard substrates. PLoS ONE 9(5):e96085.  https://doi.org/10.1371/journal.pone.0096085CrossRefPubMedPubMedCentralGoogle Scholar
  20. Coghlin C, Carpenter B, Dundas SR, Lawrie LC, Telfer C, Murray GI (2006) Characterization and over-expression of chaperonin t-complex proteins in colorectal cancer. J Pathol 210(3):351–357.  https://doi.org/10.1002/path.2056CrossRefPubMedGoogle Scholar
  21. 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 Nat Acad Sci USA 107(11):4967–4972.  https://doi.org/10.1073/pnas.0913774107
  22. Cong Y, Schroder GF, Meyer AS, Jakana J, Ma B, Dougherty MT, Schmid MF, Reissmann S, Levitt M, Ludtke SL, Frydman J, Chiu W (2012) Symmetry-free cryo-EM structures of the chaperonin TRiC along its ATPase-driven conformational cycle. EMBO J 31(3):720–730.  https://doi.org/10.1038/emboj.2011.366CrossRefPubMedGoogle Scholar
  23. Counts JT, Hester TM, Rouhana L (2017) Genetic expansion of chaperonin-containing TCP-1 (CCT/TRiC) complex subunits yields testis-specific isoforms required for spermatogenesis in planarian flatworms. Mol Reprod Dev 84(12):1271–1284.  https://doi.org/10.1002/mrd.22925CrossRefPubMedPubMedCentralGoogle Scholar
  24. Cuellar J, Martin-Benito J, Scheres SH, Sousa R, Moro F, Lopez-Vinas E, Gomez-Puertas P, Muga A, Carrascosa JL, Valpuesta JM (2008) The structure of CCT-Hsc70 NBD suggests a mechanism for Hsp70 delivery of substrates to the chaperonin. Nat Struct Mol Biol 15(8):858–864.  https://doi.org/10.1038/nsmb.1464CrossRefPubMedPubMedCentralGoogle Scholar
  25. Cuéllar J, Ludlam WG, Tensmeyer NC, Aoba T, Dhavale M, Santiago C, Bueno-Carrasco MT, Mann MJ, Plimpton RL, Makaju A, Franklin S, Willardson BM, Valpuesta JM (2019) Structural and functional analysis of the role of the chaperonin CCT in mTOR complex assembly. Nat Commun 10(1)Google Scholar
  26. Cui X, Hu ZP, Li Z, Gao PJ, Zhu JY (2015) Overexpression of chaperonin containing TCP1, subunit 3 predicts poor prognosis in hepatocellular carcinoma. World J Gastroenterol 21(28):8588–8604.  https://doi.org/10.3748/wjg.v21.i28.8588CrossRefPubMedPubMedCentralGoogle Scholar
  27. Cyrne L, Guerreiro P, Cardoso AC, RodriguesPousada C, Soares H (1996) The Tetrahymena chaperonin subunit CCT eta gene is coexpressed with CCT gamma gene during cilia biogenesis and cell sexual reproduction. FEBS Lett 383(3):277–283.  https://doi.org/10.1016/0014-5793(96)00240-2CrossRefPubMedGoogle Scholar
  28. Darrow MC, Sergeeva OA, Isas JM, Galaz-Montoya JG, King JA, Langen R, Schmid MF, Chiu W (2015) Structural mechanisms of mutant huntingtin aggregation suppression by the synthetic chaperonin-like CCT5 complex explained by cryoelectron tomography. J Biol Chem 290(28):17451–17461.  https://doi.org/10.1074/jbc.M115.655373CrossRefPubMedPubMedCentralGoogle Scholar
  29. 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(15):3078–3090.  https://doi.org/10.1038/emboj.2011.208CrossRefPubMedPubMedCentralGoogle Scholar
  30. Ditzel L, Lowe J, Stock D, Stetter KO, Huber H, Huber R, Steinbacher S (1998) Crystal structure of the thermosome, the archaeal chaperonin and homolog of CCT. Cell 93(1):125–138.  https://doi.org/10.1016/s0092-8674(00)81152-6CrossRefGoogle Scholar
  31. Dunn AY, Melville MW, Frydman J (2001) Review: cellular substrates of the eukaryotic chaperonin TRiC/CCT. J Struct Biol 135(2):176–184.  https://doi.org/10.1006/jsbi.2001.4380CrossRefPubMedGoogle Scholar
  32. Erdo F, Trapp T, Mies G, Hossmann KA (2004) Immunohistochemical analysis of protein expression after middle cerebral artery occlusion in mice. Acta Neuropathol 107(2):127–136.  https://doi.org/10.1007/s00401-003-0789-8CrossRefPubMedGoogle Scholar
  33. Farr GW, Scharl EC, Schumacher RJ, Sondek S, Horwich AL (1997) Chaperonin-mediated folding in the eukaryotic cytosol proceeds through rounds of release of native and nonnative forms. Cell 89(6):927–937.  https://doi.org/10.1016/S0092-8674(00)80278-0CrossRefPubMedGoogle Scholar
  34. 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(6):1051–1061CrossRefGoogle Scholar
  35. Feldman DE, Spiess C, Howard DE, Frydman J (2003) Tumorigenic mutations in VHL disrupt folding in vivo by interfering with chaperonin binding. Mol Cell 12(5):1213–1224CrossRefGoogle Scholar
  36. Fernandez-Fernandez MR, Sot B, Valpuesta JM (2016) Molecular chaperones: functional mechanisms and nanotechnological applications. Nanotechnology 27(32):324004.  https://doi.org/10.1088/0957-4484/27/32/324004CrossRefPubMedGoogle Scholar
  37. Fiorica JV (1992) Breast disease. Curr Opin Obstet Gynecol 4(6):897–903CrossRefGoogle Scholar
  38. Fontanella B, Birolo L, Infusini G, Cirulli C, Marzullo L, Pucci P, Turco MC, Tosco A (2010) The co-chaperone BAG3 interacts with the cytosolic chaperonin CCT: new hints for actin folding. Int J Biochem Cell Biol 42(5):641–650.  https://doi.org/10.1016/j.biocel.2009.12.008CrossRefPubMedGoogle Scholar
  39. Frank J, Ourmazd A (2016) Continuous changes in structure mapped by manifold embedding of single-particle data in cryo-EM. Methods 100:61–67.  https://doi.org/10.1016/j.ymeth.2016.02.007CrossRefPubMedGoogle Scholar
  40. Freund A, Zhong FL, Venteicher AS, Meng Z, Veenstra TD, Frydman J, Artandi SE (2014) Proteostatic control of telomerase function through TRiC-mediated folding of TCAB1. Cell 159(6):1389–1403.  https://doi.org/10.1016/j.cell.2014.10.059CrossRefPubMedPubMedCentralGoogle Scholar
  41. Frydman J, Nimmesgern E, Erdjument-Bromage H, Wall JS, Tempst P, Hartl FU (1992) Function in protein folding of TRiC, a cytosolic ring complex containing TCP-1 and structurally related subunits. EMBO J 11(13):4767–4778.  https://doi.org/10.1002/j.1460-2075.1992.tb05582.x  
  42. Frydman J, Nimmesgern E, Ohtsuka K, Hartl FU (1994) Folding of nascent polypeptide chains in a high molecular mass assembly with molecular chaperones. Nature 370(6485):111–117.  https://doi.org/10.1038/370111a0CrossRefPubMedGoogle Scholar
  43. Gao YJ, Thomas JO, Chow RL, Lee GH, Cowan NJ (1992) A cytoplasmic chaperonin that catalyzes beta-actin folding. Cell 69(6):1043–1050.  https://doi.org/10.1016/0092-8674(92)90622-JCrossRefGoogle Scholar
  44. Gao HJ, Zheng M, Sun SJ, Wang HW, Yue ZG, Zhu Y, Han XC, Yang JQ, Zhou YQ, Cai YR, Hu WN (2017) Chaperonin containing TCP1 subunit 5 is a tumor associated antigen of non-small cell lung cancer. Oncotarget 8(38):64170–64179.  https://doi.org/10.18632/oncotarget.19369
  45. Gestaut D, Roh SH, Ma B, Pintilie G, Joachimiak LA, Leitner A, Walzthoeni T, Aebersold R, Chiu W, Frydman J (2019) The chaperonin TRiC/CCT associates with prefoldin through a conserved electrostatic interface essential for cellular proteostasis. Cell 177(3):751–765.e15Google Scholar
  46. 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(12):2309–2324.  https://doi.org/10.1016/j.yexcr.2006.03.028CrossRefPubMedGoogle Scholar
  47. Guenther MG, Yu JJ, Kao GD, Yen TJ, Lazar MA (2002) Assembly of the SMRT-histone deacetylase 3 repression complex requires the TCP-1 ring complex. Genes Dev 16(24):3130–3135.  https://doi.org/10.1101/gad.1037502CrossRefPubMedPubMedCentralGoogle Scholar
  48. 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(2):223–235.  https://doi.org/10.1016/j.yexcr.2015.02.005CrossRefPubMedGoogle Scholar
  49. Guo Q, Lehmer C, Martinez-Sanchez A, Rudack T, Beck F, Hartmann H, Perez-Berlanga M, Frottin F, Hipp MS, Hartl FU, Edbauer D, Baumeister W, Fernandez-Busnadiego R (2018) In situ structure of neuronal C9orf72 Poly-GA aggregates reveals proteasome recruitment. Cell.  https://doi.org/10.1016/j.cell.2017.12.030
  50. Hanafy KA, Martin E, Murad F (2004) CCTeta, a novel soluble guanylyl cyclase-interacting protein. J Biol Chem 279(45):46946–46953.  https://doi.org/10.1074/jbc.M404134200CrossRefPubMedGoogle Scholar
  51. Harker WG, Sikic BI (1985) Multidrug (pleiotropic) resistance in doxorubicin-selected variants of the human sarcoma cell line MES-SA. Cancer Res 45(9):4091–4096PubMedGoogle Scholar
  52. Horwich AL, Willison KR (1993) Protein folding in the cell: functions of two families of molecular chaperone, hsp 60 and TF55-TCP1. Philos Trans R Soc Lond B Biol Sci 339(1289):313–325; discussion 325–316.  https://doi.org/10.1098/rstb.1993.0030
  53. Huang X, Wang X, Cheng C, Cai J, He S, Wang H, Liu F, Zhu C, Ding Z, Huang X, Zhang T, Zhang Y (2014) Chaperonin containing TCP1, subunit 8 (CCT8) is upregulated in hepatocellular carcinoma and promotes HCC proliferation. APMIS 122(11):1070–1079.  https://doi.org/10.1111/apm.12258CrossRefPubMedGoogle Scholar
  54. Humrich J, Bermel C, Bunemann M, Harmark L, Frost R, Quitterer U, Lohse MJ (2005) Phosducin-like protein regulates G-protein betagamma folding by interaction with tailless complex polypeptide-1alpha: dephosphorylation or splicing of PhLP turns the switch toward regulation of Gbetagamma folding. J Biol Chem 280(20):20042–20050.  https://doi.org/10.1074/jbc.M409233200CrossRefPubMedGoogle Scholar
  55. Hunziker M, Barandun J, Petfalski E, Tan D, Delan-Forino C, Molloy KR, Kim KH, Dunn-Davies H, Shi Y, Chaker-Margot M, Chait BT, Walz T, Tollervey D, Klinge S (2016) UtpA and UtpB chaperone nascent pre-ribosomal RNA and U3 snoRNA to initiate eukaryotic ribosome assembly. Nat Commun 7:12090.  https://doi.org/10.1038/ncomms12090CrossRefPubMedPubMedCentralGoogle Scholar
  56. Jiang Y, Douglas NR, Conley NR, Miller EJ, Frydman J, Moerner WE (2011) Sensing cooperativity in ATP hydrolysis for single multisubunit enzymes in solution. Proc Natl Acad Sci USA 108(41):16962–16967.  https://doi.org/10.1073/pnas.1112244108CrossRefPubMedGoogle Scholar
  57. Jiang XD, Mao WJ, Yang ZY, Zeng J, Zhang Y, Song Y, Kong Y, Ren SY, Zuo YF (2015) Silencing P2X7 receptor downregulates the expression of TCP-1 involved in lymphoma lymphatic metastasis. Oncotarget 6(39):42105–42117.  https://doi.org/10.18632/oncotarget.5870
  58. 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(5):1042–1055.  https://doi.org/10.1016/j.cell.2014.10.042CrossRefPubMedPubMedCentralGoogle Scholar
  59. Kaelin WG Jr (2002) Molecular basis of the VHL hereditary cancer syndrome. Nat Rev Cancer 2(9):673–682.  https://doi.org/10.1038/nrc885CrossRefPubMedGoogle Scholar
  60. 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 USA 114(5):956–961.  https://doi.org/10.1073/pnas.1620451114CrossRefPubMedGoogle Scholar
  61. 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 USA 109(8):2884–2889.  https://doi.org/10.1073/pnas.1119472109CrossRefPubMedGoogle Scholar
  62. Kalisman N, Schroder GF, Levitt M (2013) The crystal structures of the eukaryotic chaperonin CCT reveal its functional partitioning. Structure 21(4):540–549.  https://doi.org/10.1016/j.str.2013.01.017CrossRefPubMedPubMedCentralGoogle Scholar
  63. 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(4):e1001844.  https://doi.org/10.1371/journal.pbio.1001844CrossRefPubMedPubMedCentralGoogle Scholar
  64. Khabirova E, Moloney A, Marciniak SJ, Williams J, Lomas DA, Oliver SG, Favrin G, Sattelle DB, Crowther DC (2014) The TRiC/CCT chaperone is implicated in Alzheimer’s disease based on patient GWAS and an RNAi screen in Abeta-expressing Caenorhabditis elegans. PLoS One 9(7):e102985.  https://doi.org/10.1371/journal.pone.0102985CrossRefPubMedPubMedCentralGoogle Scholar
  65. Kim YE, Hipp MS, Bracher A, Hayer-Hartl M, Hartl FU (2013) Molecular chaperone functions in protein folding and proteostasis. Annu Rev Biochem 82(82):323–355.  https://doi.org/10.1146/annurev-biochem-060208-092442CrossRefPubMedGoogle Scholar
  66. Kitamura A, Kubota H, Pack CG, Matsumoto G, Hirayama S, Takahashi Y, Kimura H, Kinjo M, Morimoto RI, Nagata K (2006) Cytosolic chaperonin prevents polyglutamine toxicity with altering the aggregation state. Nat Cell Biol 8(10):1163–1170.  https://doi.org/10.1038/ncb1478CrossRefPubMedGoogle Scholar
  67. Klumpp M, Baumeister W, Essen LO (1997) Structure of the substrate binding domain of the thermosome, an archaeal group II chaperonin. Cell 91(2):263–270.  https://doi.org/10.1016/S0092-8674(00)80408-0CrossRefGoogle Scholar
  68. Knee KM, Sergeeva OA, King JA (2013) Human TRiC complex purified from HeLa cells contains all eight CCT subunits and is active in vitro. Cell Stress Chaperones 18(2):137–144.  https://doi.org/10.1007/s12192-012-0357-zCrossRefPubMedGoogle Scholar
  69. Kohl S, Baumann B, Rosenberg T, Kellner U, Lorenz B, Vadalà M, Jacobson SG, Wissinger B (2002) Mutations in the cone photoreceptor G-protein alpha-subunit gene GNAT2 in patients with achromatopsia. Am J Hum Genet 71(2):422–425.  https://doi.org/10.1086/341835CrossRefPubMedPubMedCentralGoogle Scholar
  70. Korobko I, Nadler-Holly M, Horovitz A (2016) Transient kinetic analysis of ATP hydrolysis by the CCT/TRiC chaperonin. J Mol Biol 428(22):4520–4527.  https://doi.org/10.1016/j.jmb.2016.09.017CrossRefPubMedGoogle Scholar
  71. Koulikovska M, Podskochy A, Fagerholm P (2005) The expression pattern of the subunit of chaperonin containing T-complex polypeptide 1 and its substrate, alpha-smooth muscle actin, during corneal wound healing. Acta Ophthalmol Scand 83(5):543–548.  https://doi.org/10.1111/j.1600-0420.2005.00482.xCrossRefPubMedGoogle Scholar
  72. Lee MJ, Stephenson DA, Groves MJ, Sweeney MG, Davis MB, An SF, Houlden H, Salih MAM, Timmerman V, de Jonghe P, Auer-Grumbach M, Di Maria E, Scaravilli F, Wood NW, Reilly MM (2003) Hereditary sensory neuropathy is caused by a mutation in the delta subunit of the cytosolic chaperonin-containing t-complex peptide-1 (Cct4) gene. Hum Mol Genet 12(15):1917–1925.  https://doi.org/10.1093/hmg/ddg198CrossRefPubMedGoogle Scholar
  73. Leitner A, Joachimiak LA, Bracher A, Monkemeyer 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(5):814–825.  https://doi.org/10.1016/j.str.2012.03.007CrossRefPubMedPubMedCentralGoogle Scholar
  74. Lewis VA, Hynes GM, Zheng D, Saibil H, Willison K (1992) T-complex polypeptide-1 is a subunit of a heteromeric particle in the eukaryotic cytosol. Nature 358(6383):249–252.  https://doi.org/10.1038/358249a0CrossRefPubMedGoogle Scholar
  75. Liebman SW, Meredith SC (2010) Protein folding: sticky N17 speeds huntingtin pile-up. Nat Chem Biol 6(1):7–8.  https://doi.org/10.1038/nchembio.279CrossRefPubMedGoogle Scholar
  76. Lin YF, Tsai WP, Liu HG, Liang PH (2009) Intracellular beta-tubulin/chaperonin containing TCP1-beta complex serves as a novel chemotherapeutic target against drug-resistant tumors. Cancer Res 69(17):6879–6888.  https://doi.org/10.1158/0008-5472.CAN-08-4700CrossRefPubMedGoogle Scholar
  77. 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(14):4311–4316.  https://doi.org/10.1093/emboj/16.14.4311CrossRefGoogle Scholar
  78. Liu BD, Larsson L, Caballero A, Hao XX, Oling D, Grantham J, Nystrom T (2010) The polarisome is required for segregation and retrograde transport of protein aggregates. Cell 140(2):257–267.  https://doi.org/10.1016/j.cell.2009.12.031CrossRefPubMedGoogle Scholar
  79. Llorca O, Smyth MG, Marco S, Carrascosa JL, Willison KR, Valpuesta JM (1998) ATP binding induces large conformational changes in the apical and equatorial domains of the eukaryotic chaperonin containing TCP-1 complex. J Biol Chem 273(17):10091–10094.  https://doi.org/10.1074/jbc.273.17.10091CrossRefPubMedGoogle Scholar
  80. 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(6762):693–696.  https://doi.org/10.1038/45294valpuesta1999.pdfCrossRefPubMedGoogle Scholar
  81. Llorca O, Martin-Benito J, Ritco-Vonsovici M, Grantham J, Hynes GM, Willison KR, Carrascosa JL, Valpuesta JM (2000) Eukaryotic chaperonin CCT stabilizes actin and tubulin folding intermediates in open quasi-native conformations. EMBO J 19(22):5971–5979.  https://doi.org/10.1093/emboj/19.22.5971CrossRefPubMedPubMedCentralGoogle Scholar
  82. Llorca O, Martin-Benito J, Gomez-Puertas P, Ritco-Vonsovici M, Willison KR, Carrascosa JL, Valpuesta JM (2001) Analysis of the interaction between the eukaryotic chaperonin CCT and its substrates actin and tubulin. J Struct Biol 135(2):205–218.  https://doi.org/10.1106/jsbi.2001.4359CrossRefPubMedGoogle Scholar
  83. Loktev AV, Zhang Q, Beck JS, Searby CC, Scheetz TE, Bazan JF, Slusarski DC, Sheffield VC, Jackson PK, Nachury MV (2008) A BBSome subunit links ciliogenesis, microtubule stability, and acetylation. Dev Cell 15(6):854–865.  https://doi.org/10.1016/j.devcel.2008.11.001CrossRefPubMedGoogle Scholar
  84. Lopez T, Dalton K, Frydman J (2015) The mechanism and function of group ii chaperonins. J Mol Biol 427(18):2919–2930.  https://doi.org/10.1016/j.jmb.2015.04.013CrossRefPubMedPubMedCentralGoogle Scholar
  85. Machida K, Masutani M, Kobayashi T, Mikami S, Nishino Y, Miyazawa A, Imataka H (2012) Reconstitution of the human chaperonin CCT by co-expression of the eight distinct subunits in mammalian cells. Protein Expr Purif 82(1):61–69.  https://doi.org/10.1016/j.pep.2011.11.010CrossRefPubMedGoogle Scholar
  86. Malcikova J, Tichy B, Damborsky J, Kabathova J, Trbusek M, Mayer J, Pospisilova S (2010) Analysis of the DNA-binding activity of p53 mutants using functional protein microarrays and its relationship to transcriptional activation. Biol Chem 391(2–3):197–205.  https://doi.org/10.1515/BC.2010.027CrossRefPubMedGoogle Scholar
  87. Martin-Benito J, Boskovic J, Gomez-Puertas P, Carrascosa JL, Simons CT, Lewis SA, Bartolini F, Cowan NJ, Valpuesta JM (2002) Structure of eukaryotic prefoldin and of its complexes with unfolded actin and the cytosolic chaperonin CCT. EMBO J 21(23):6377–6386.  https://doi.org/10.1093/emboj/cdf640CrossRefGoogle Scholar
  88. Masson N, Appelhoff RJ, Tuckerman JR, Tian YM, Demol H, Puype M, Vandekerckhove J, Ratcliffe PJ, Pugh CW (2004) The HIF prolyl hydroxylase PHD3 is a potential substrate of the TRiC chaperonin. FEBS Lett 570(1–3):166–170.  https://doi.org/10.1016/j.febslet.2004.06.040CrossRefPubMedGoogle Scholar
  89. Matsuda N, Mishina M (2004) Identification of chaperonin CCT gamma subunit as a determinant of retinotectal development by whole-genome subtraction cloning from zebrafish no tectal neuron mutant. Development 131(9):1913–1925.  https://doi.org/10.1242/dev.01085CrossRefPubMedGoogle Scholar
  90. Matus DQ, Li XY, Durbin S, Agarwal D, Chi Q, Weiss SJ, Sherwood DR (2010) In vivo identification of regulators of cell invasion across basement membranes. Sci Signal 3(120):ra35.  https://doi.org/10.1126/scisignal.2000654
  91. McClellan AJ, Scott MD, Frydman J (2005) Folding and quality control of the VHL tumor suppressor proceed through distinct chaperone pathways. Cell 121(5):739–748.  https://doi.org/10.1016/j.cell.2005.03.024CrossRefPubMedGoogle Scholar
  92. 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(9):3141–3151.  https://doi.org/10.1128/mcb.23.9.3141-3151.2003CrossRefPubMedPubMedCentralGoogle Scholar
  93. Meyer AS, Gillespie JR, Walther D, Millet IS, Doniach S, Frydman J (2003) Closing the folding chamber of the eukaryotic chaperonin requires the transition state of ATP hydrolysis. Cell 113(3):369–381.  https://doi.org/10.1016/S0092-8674(03)00307-6CrossRefGoogle Scholar
  94. Minegishi Y, Sheng X, Yoshitake K, Sergeev Y, Iejima D, Shibagaki Y, Monma N, Ikeo K, Furuno M, Zhuang W, Liu Y, Rong W, Hattori S, Iwata T (2016) CCT2 mutations evoke leber congenital amaurosis due to chaperone complex instability. Sci Rep 6:33742.  https://doi.org/10.1038/srep33742CrossRefPubMedPubMedCentralGoogle Scholar
  95. Minegishi Y, Nakaya N, Tomarev SI (2018) Mutation in the Zebrafish cct2 gene leads to abnormalities of cell cycle and cell death in the retina: a model of CCT2-related leber congenital amaurosis. Invest Ophthalmol Vis Sci 59(2):995–1004.  https://doi.org/10.1167/iovs.17-22919CrossRefPubMedPubMedCentralGoogle Scholar
  96. Miyata Y, Shibata T, Aoshima M, Tsubata T, Nishida E (2014) The molecular chaperone TRiC/CCT binds to the Trp-Asp 40 (WD40) repeat protein WDR68 and promotes its folding, protein kinase DYRK1A binding, and nuclear accumulation. J Biol Chem 289(48):33320–33332.  https://doi.org/10.1074/jbc.M114.586115CrossRefPubMedPubMedCentralGoogle Scholar
  97. Monzo K, Dowd SR, Minden JS, Sisson JC (2010) Proteomic analysis reveals CCT is a target of Fragile X mental retardation protein regulation in Drosophila. Dev Biol 340(2):408–418.  https://doi.org/10.1016/j.ydbio.2010.01.028CrossRefPubMedPubMedCentralGoogle Scholar
  98. Mosalaganti S, Kosinski J, Albert S, Schaffer M, Strenkert D, Salome PA, Merchant SS, Plitzko JM, Baumeister W, Engel BD, Beck M (2018) In situ architecture of the algal nuclear pore complex. Nat Commun 9(1):2361.  https://doi.org/10.1038/s41467-018-04739-yCrossRefPubMedPubMedCentralGoogle Scholar
  99. Muchowski PJ, Wacker JL (2005) Modulation of neurodegeneration by molecular chaperones. Nat Rev Neurosci 6:11.  https://doi.org/10.1038/nrn1587CrossRefPubMedGoogle Scholar
  100. Munoz IG, Yebenes H, Zhou M, Mesa P, Serna M, Park AY, Bragado-Nilsson E, Beloso A, de Carcer G, Malumbres M, Robinson CV, Valpuesta JM, Montoya G (2011) Crystal structure of the open conformation of the mammalian chaperonin CCT in complex with tubulin. Nat Struct Mol Biol 18(1):14–19.  https://doi.org/10.1038/nsmb.1971CrossRefPubMedGoogle Scholar
  101. Nachury MV, Loktev AV, Zhang Q, Westlake CJ, Peranen J, Merdes A, Slusarski DC, Scheller RH, Bazan JF, Sheffield VC, Jackson PK (2007) A core complex of BBS proteins cooperates with the GTPase Rab8 to promote ciliary membrane biogenesis. Cell 129(6):1201–1213.  https://doi.org/10.1016/j.cell.2007.03.053CrossRefPubMedGoogle Scholar
  102. Noormohammadi A, Khodakarami A, Gutierrez-Garcia R, Lee HJ, Koyuncu S, Konig T, Schindler C, Saez I, Fatima A, Dieterich C, Vilchez D (2016) Somatic increase of CCT8 mimics proteostasis of human pluripotent stem cells and extends C. elegans lifespan. Nat Commun 7:13649.  https://doi.org/10.1038/ncomms13649
  103. Ooe A, Kato K, Noguchi S (2007) Possible involvement of CCT5, RGS3, and YKT6 genes up-regulated in p53-mutated tumors in resistance to docetaxel in human breast cancers. Breast Cancer Res Treat 101(3):305–315.  https://doi.org/10.1007/s10549-006-9293-xCrossRefPubMedGoogle Scholar
  104. Pappenberger G, McCormack EA, Willison KR (2006) Quantitative actin folding reactions using yeast CCT purified via an internal tag in the CCT3/gamma subunit. J Mol Biol 360(2):484–496.  https://doi.org/10.1016/j.jmb.2006.05.003CrossRefPubMedGoogle Scholar
  105. Pavel M, Imarisio S, Menzies FM, Jimenez-Sanchez M, Siddiqi FH, Wu X, Renna M, O’Kane CJ, Crowther DC, Rubinsztein DC (2016) CCT complex restricts neuropathogenic protein aggregation via autophagy. Nat Commun 7:13821.  https://doi.org/10.1038/ncomms13821CrossRefPubMedPubMedCentralGoogle Scholar
  106. Pereira JH, Ralston CY, Douglas NR, Meyer D, Knee KM, Goulet DR, King JA, Frydman J, Adams PD (2010) Crystal structures of a group II chaperonin reveal the open and closed states associated with the protein folding cycle. J Biol Chem 285(36):27958–27966.  https://doi.org/10.1074/jbc.M110.125344CrossRefPubMedPubMedCentralGoogle Scholar
  107. Pereira JH, Ralston CY, Douglas NR, Kumar R, Lopez T, McAndrew RP, Knee KM, King JA, Frydman J, Adams PD (2012) Mechanism of nucleotide sensing in group II chaperonins. EMBO J 31(3):731–740.  https://doi.org/10.1038/emboj.2011.468CrossRefPubMedGoogle Scholar
  108. Pereira JH, McAndrew RP, Sergeeva OA, Ralston CY, King JA, Adams PD (2017) Structure of the human TRiC/CCT Subunit 5 associated with hereditary sensory neuropathy. Sci Rep 7(1):3673.  https://doi.org/10.1038/s41598-017-03825-3CrossRefPubMedPubMedCentralGoogle Scholar
  109. Pines A, Dijk M, Makowski M, Meulenbroek EM, Vrouwe MG, van der Weegen Y, Baltissen M, French PJ, van Royen ME, Luijsterburg MS, Mullenders LH, Vermeulen M, Vermeulen W, Pannu NS, van Attikum H (2018) TRiC controls transcription resumption after UV damage by regulating Cockayne syndrome protein A. Nat Commun 9(1):1040.  https://doi.org/10.1038/s41467-018-03484-6CrossRefPubMedPubMedCentralGoogle Scholar
  110. Plimpton RL, Cuellar J, Lai CW, Aoba T, Makaju A, Franklin S, Mathis AD, Prince JT, Carrascosa JL, Valpuesta JM, Willardson BM (2015) Structures of the Gbeta-CCT and PhLP1-Gbeta-CCT complexes reveal a mechanism for G-protein beta-subunit folding and Gbetagamma dimer assembly. Proc Natl Acad Sci USA 112(8):2413–2418.  https://doi.org/10.1073/pnas.1419595112CrossRefPubMedGoogle Scholar
  111. Posokhova E, Song H, Belcastro M, Higgins L, Bigley LR, Michaud NA, Martemyanov KA, Sokolov M (2011) Disruption of the chaperonin containing TCP-1 function affects protein networks essential for rod outer segment morphogenesis and survival. Mol Cell Proteomics 10(1):M110 000570.  https://doi.org/10.1074/mcp.m110.000570
  112. Qian-Lin Z, Ting-Feng W, Qi-Feng C, Min-Hua Z, Ai-Guo L (2010) Inhibition of cytosolic chaperonin CCTzeta-1 expression depletes proliferation of colorectal carcinoma in vitro. J Surg Oncol 102(5):419–423.  https://doi.org/10.1002/jso.21625CrossRefPubMedGoogle Scholar
  113. Qiu X, He X, Huang Q, Liu X, Sun G, Guo J, Yuan D, Yang L, Ban N, Fan S, Tao T, Wang D (2015) Overexpression of CCT8 and its significance for tumor cell proliferation, migration and invasion in glioma. Pathol Res Pract 211(10):717–725.  https://doi.org/10.1016/j.prp.2015.04.012CrossRefPubMedGoogle Scholar
  114. Rademacher F, Kehren V, Stoldt VR, Ernst JF (1998) A Candida albicans chaperonin subunit (CaCct8p) as a suppressor of morphogenesis and Ras phenotypes in C-albicans and Saccharomyces cerevisiae. Microbiol-Uk 144:2951–2960.  https://doi.org/10.1099/00221287-144-11-2951CrossRefGoogle Scholar
  115. 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 reports 2(4):866–877.  https://doi.org/10.1016/j.celrep.2012.08.036CrossRefPubMedPubMedCentralGoogle Scholar
  116. Rivenzon-Segal D, Wolf SG, Shimon L, Willison KR, Horovitz A (2005) Sequential ATP-induced allosteric transitions of the cytoplasmic chaperonin containing TCP-1 revealed by EM analysis. Nat Struct Mol Biol 12(3):233–237.  https://doi.org/10.1038/nsmb901CrossRefPubMedGoogle Scholar
  117. Roh SH, Kasembeli M, Bakthavatsalam D, Chiu W, Tweardy DJ (2015) Contribution of the type II chaperonin, TRiC/CCT, to oncogenesis. Int J Mol Sci 16(11):26706–26720.  https://doi.org/10.3390/ijms161125975CrossRefPubMedPubMedCentralGoogle Scholar
  118. Roh SH, Kasembeli M, Galaz-Montoya JG, Trnka M, Lau WC, Burlingame A, Chiu W, Tweardy DJ (2016a) Chaperonin TRiC/CCT modulates the folding and activity of leukemogenic fusion oncoprotein AML1-ETO. J Biol Chem 291(9):4732–4741.  https://doi.org/10.1074/jbc.M115.684878CrossRefPubMedGoogle Scholar
  119. Roh SH, Kasembeli MM, Galaz-Montoya JG, Chiu W, Tweardy DJ (2016b) Chaperonin TRiC/CCT recognizes fusion oncoprotein AML1-ETO through subunit-specific interactions. Biophys J 110(11):2377–2385.  https://doi.org/10.1016/j.bpj.2016.04.045CrossRefPubMedPubMedCentralGoogle Scholar
  120. 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(20):3095–3104.  https://doi.org/10.1091/mbc.E13-09-0530CrossRefPubMedPubMedCentralGoogle Scholar
  121. Satish L, Johnson S, Wang JH, Post JC, Ehrlich GD, Kathju S (2010) Chaperonin containing T-complex polypeptide subunit eta (CCT-eta) is a specific regulator of fibroblast motility and contractility. PLoS ONE 5(4):e10063.  https://doi.org/10.1371/journal.pone.0010063CrossRefPubMedPubMedCentralGoogle Scholar
  122. Satish L, O’Gorman DB, Johnson S, Raykha C, Gan BS, Wang JH, Kathju S (2013) Increased CCT-eta expression is a marker of latent and active disease and a modulator of fibroblast contractility in Dupuytren’s contracture. Cell Stress Chaperones 18(4):397–404.  https://doi.org/10.1007/s12192-012-0392-9CrossRefPubMedPubMedCentralGoogle Scholar
  123. Seixas C, Cruto T, Tavares A, Gaertig J, Soares H (2010) CCTalpha and CCTdelta chaperonin subunits are essential and required for cilia assembly and maintenance in Tetrahymena. PLoS ONE 5(5):e10704.  https://doi.org/10.1371/journal.pone.0010704CrossRefPubMedPubMedCentralGoogle Scholar
  124. Seo S, Baye LM, Schulz NP, Beck JS, Zhang Q, Slusarski DC, Sheffield VC (2010) BBS6, BBS10, and BBS12 form a complex with CCT/TRiC family chaperonins and mediate BBSome assembly. Proc Natl Acad Sci USA 107(4):1488–1493.  https://doi.org/10.1073/pnas.0910268107CrossRefPubMedGoogle Scholar
  125. Sergeeva OA, Chen B, Haase-Pettingell C, Ludtke SJ, Chiu W, King JA (2013) Human CCT4 and CCT5 chaperonin subunits expressed in Escherichia coli form biologically active homo-oligomers. J Biol Chem 288(24):17734–17744.  https://doi.org/10.1074/jbc.M112.443929CrossRefPubMedPubMedCentralGoogle Scholar
  126. Sergeeva OA, Tran MT, Haase-Pettingell C, King JA (2014) Biochemical characterization of mutants in chaperonin proteins CCT4 and CCT5 associated with hereditary sensory neuropathy. J Biol Chem 289(40):27470–27480.  https://doi.org/10.1074/jbc.M114.576033CrossRefPubMedPubMedCentralGoogle Scholar
  127. Shahmoradian SH, Galaz-Montoya JG, Schmid MF, Cong Y, Ma B, Spiess C, Frydman J, Ludtke SJ, Chiu W (2013) TRiC’s tricks inhibit huntingtin aggregation. Elife 2:e00710.  https://doi.org/10.7554/eLife.00710CrossRefPubMedPubMedCentralGoogle Scholar
  128. Siegers K, Bolter B, Schwarz JP, Bottcher UMK, Guha S, Hartl FU (2003) TRiC/CCT cooperates with different upstream chaperones in the folding of distinct protein classes (Retracted Article. See vol 27, 301 p, 2008). EMBO J 22(19):5230–5240.  https://doi.org/10.1093/emboj/cdg483
  129. Sinha S, Belcastro M, Datta P, Seo S, Sokolov M (2014) Essential role of the chaperonin CCT in rod outer segment biogenesis. Invest Ophth Vis Sci 55(6):3775–3784.  https://doi.org/10.1167/iovs.14-13889
  130. Skjaerven L, Cuellar J, Martinez A, Valpuesta JM (2015) Dynamics, flexibility, and allostery in molecular chaperonins. FEBS Lett 589(19 Pt A):2522–2532.  https://doi.org/10.1016/j.febslet.2015.06.019
  131. Sontag EM, Joachimiak LA, Tan Z, Tomlinson A, Housman DE, Glabe CG, Potkin SG, Frydman J, Thompson LM (2013) Exogenous delivery of chaperonin subunit fragment ApiCCT1 modulates mutant Huntingtin cellular phenotypes. Proc Natl Acad Sci USA 110(8):3077–3082.  https://doi.org/10.1073/pnas.1222663110CrossRefPubMedGoogle Scholar
  132. Sot B, Rubio-Munoz A, Leal-Quintero A, Martinez-Sabando J, Marcilla M, Roodveldt C, Valpuesta JM (2017) The chaperonin CCT inhibits assembly of alpha-synuclein amyloid fibrils by a specific, conformation-dependent interaction. Sci Rep 7:40859.  https://doi.org/10.1038/srep40859CrossRefPubMedPubMedCentralGoogle Scholar
  133. Soues S, Kann M-L, Fouquet J-P, Melki R (2003) The cytosolic chaperonin CCT associates to cytoplasmic microtubular structures during mammalian spermiogenesis and to heterochromatin in germline and somatic cells. Exp Cell Res 288(2):363–373.  https://doi.org/10.1016/s0014-4827(03)00248-9CrossRefPubMedGoogle Scholar
  134. Spiess C, Meyer AS, Reissmann S, Frydman J (2004) Mechanism of the eukaryotic chaperonin: protein folding in the chamber of secrets. Trends Cell Biol 14(11):598–604.  https://doi.org/10.1016/j.tcb.2004.09.015CrossRefPubMedPubMedCentralGoogle Scholar
  135. Srikakulam R, Winkelmann DA (1999) Myosin II folding is mediated by a molecular chaperonin. J Biol Chem 274(38):27265–27273.  https://doi.org/10.1074/jbc.274.38.27265CrossRefPubMedGoogle Scholar
  136. Stemp MJ, Guha S, Hartl FU, Barral JM (2005) Efficient production of native actin upon translation in a bacterial lysate supplemented with the eukaryotic chaperonin TRiC. Biol Chem 386(8):753–757.  https://doi.org/10.1515/BC.2005.088CrossRefPubMedGoogle Scholar
  137. Stirling PC, Cuellar J, Alfaro GA, El Khadali F, Beh CT, Valpuesta JM, Melki R, Leroux MR (2006) PhLP3 modulates CCT-mediated actin and tubulin folding via ternary complexes with substrates. J Biol Chem 281(11):7012–7021.  https://doi.org/10.1074/jbc.M513235200CrossRefPubMedGoogle Scholar
  138. 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(10):1155–1162.  https://doi.org/10.1038/ncb1477CrossRefPubMedPubMedCentralGoogle Scholar
  139. Tam S, Spiess C, Auyeung W, Joachimiak L, Chen B, Poirier MA, Frydman J (2009) The chaperonin TRiC blocks a huntingtin sequence element that promotes the conformational switch to aggregation. Nat Struct Mol Biol 16(12):1279–1285.  https://doi.org/10.1038/nsmb.1700CrossRefPubMedPubMedCentralGoogle Scholar
  140. Tracy CM, Kolesnikov AV, Blake DR, Chen CK, Baehr W, Kefalov VJ, Willardson BM (2015) Retinal cone photoreceptors require phosducin-like protein 1 for G protein complex assembly and signaling. PLoS ONE 10(2):e0117129.  https://doi.org/10.1371/journal.pone.0117129CrossRefPubMedPubMedCentralGoogle Scholar
  141. 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(6):805–817.  https://doi.org/10.1016/j.molcel.2013.05.002CrossRefPubMedPubMedCentralGoogle Scholar
  142. Ursic D, Culbertson MR (1991) The yeast homolog to mouse Tcp-1 affects microtubule-mediated processes. Mol Cell Biol 11(5):2629–2640.  https://doi.org/10.1128/mcb.11.5.2629CrossRefGoogle Scholar
  143. Vainberg IE, Lewis SA, Rommelaere H, Ampe C, Vandekerckhove J, Klein HL, Cowan NJ (1998) Prefoldin, a chaperone that delivers unfolded proteins to cytosolic chaperonin. Cell 93(5):863–873.  https://doi.org/10.1016/S0092-8674(00)81446-4
  144. van den Brink DM, Brites P, Haasjes J, Wierzbicki AS, Mitchell J, Lambert-Hamill M, de Belleroche J, Jansen GA, Waterham HR, Ronald Wanders JA (2003) Identification of PEX7 as the Second Gene Involved in Refsum Disease. Am J Human Genet 72(2):471–477.  https://doi.org/10.1086/346093CrossRefGoogle Scholar
  145. Vinh DBN, Drubin DG (1994) A yeast Tcp-1-like protein is required for actin function in-vivo. P Natl Acad Sci USA 91(19):9116–9120.  https://doi.org/10.1073/pnas.91.19.9116
  146. Voisine C, Pedersen JS, Morimoto RI (2010) Chaperone networks: tipping the balance in protein folding diseases. Neurobiol Dis 40(1):12–20.  https://doi.org/10.1016/j.nbd.2010.05.007CrossRefPubMedPubMedCentralGoogle Scholar
  147. Waldmann T, Lupas A, Kellermann J, Peters J, Baumeister W (1995) Primary structure of the thermosome from thermoplasma-acidophilum. Biol Chem H-S 376(2):119–126.  https://doi.org/10.1515/bchm3.1995.376.2.119CrossRefGoogle Scholar
  148. Wang H, Han W, Takagi J, Cong Y (2018) Yeast inner-subunit PA–NZ-1 labeling strategy for accurate subunit identification in a macromolecular complex through Cryo-EM analysis. J Mol Biol 430(10):1417–1425.  https://doi.org/10.1016/j.jmb.2018.03.026CrossRefPubMedGoogle Scholar
  149. Wei PL, Huang CY, Tai CJ, Batzorig U, Cheng WL, Hunag MT, Chang YJ (2016) Glucose-regulated protein 94 mediates metastasis by CCT8 and the JNK pathway in hepatocellular carcinoma. Tumour Biol 37(6):8219–8227.  https://doi.org/10.1007/s13277-015-4669-3CrossRefPubMedGoogle Scholar
  150. Willardson BM, Howlett AC (2007) Function of phosducin-like proteins in G protein signaling and chaperone-assisted protein folding. Cell Signal 19(12):2417–2427.  https://doi.org/10.1016/j.cellsig.2007.06.013
  151. Willison KR (2018a) The structure and evolution of eukaryotic chaperonin-containing TCP-1 and its mechanism that folds actin into a protein spring. Biochem J 475(19):3009–3034.  https://doi.org/10.1042/bcj20170378
  152. Willison KR (2018b) The substrate specificity of eukaryotic cytosolic chaperonin CCT. Philos Trans R Soc Lond B Biol Sci 373(1749).  https://doi.org/10.1098/rstb.2017.0192
  153. Wu CZ, Chang LC, Lin YF, Hung YJ, Pei D, Chen JS (2015a) Chaperonin-containing t-complex protein-1 subunit beta as a possible biomarker for the phase of glomerular hyperfiltration of diabetic nephropathy. Dis Markers 2015:548101.  https://doi.org/10.1155/2015/548101CrossRefPubMedPubMedCentralGoogle Scholar
  154. Wu X, Zhang H, Chen D, Song Y, Qian R, Chen C, Mao X, Chen X, Zhang W, Shao B, Shen J, Yan Y, Wu X, Liu Y (2015b) Up-Regulation of CCT8 related to neuronal apoptosis after traumatic brain injury in adult rats. Neurochem Res 40(9):1882–1891.  https://doi.org/10.1007/s11064-015-1683-1CrossRefPubMedGoogle Scholar
  155. Xu XM, Wang J, Xuan ZY, Goldshmidt A, Borrill PGM, Hariharan N, Kim JY, Jackson D (2011) Chaperonins facilitate KNOTTED1 cell-to-cell trafficking and stem cell function. Science 333(6046):1141–1144.  https://doi.org/10.1126/science.1205727CrossRefPubMedGoogle Scholar
  156. 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(12):1255–1262.  https://doi.org/10.1038/nsmb.1515CrossRefPubMedPubMedCentralGoogle Scholar
  157. Yamamoto YY, Uno Y, Sha E, Ikegami K, Ishii N, Dohmae N, Sekiguchi H, Sasaki YC, Yohda M (2017) Asymmetry in the function and dynamics of the cytosolic group II chaperonin CCT/TRiC. PLoS ONE 12(5):e0176054.  https://doi.org/10.1371/journal.pone.0176054CrossRefPubMedPubMedCentralGoogle Scholar
  158. Yin H, Miao X, Wu Y, Wei Y, Zong G, Yang S, Chen X, Zheng G, Zhu X, Guo Y, Li C, Chen Y, Wang Y, He S (2016) The role of the Chaperonin containing t-complex polypeptide 1, subunit 8 (CCT8) in B-cell non-Hodgkin’s lymphoma. Leuk Res 45:59–67.  https://doi.org/10.1016/j.leukres.2016.04.010CrossRefPubMedGoogle Scholar
  159. Ying Z, Tian H, Li Y, Lian R, Li W, Wu S, Zhang HZ, Wu J, Liu L, Song J, Guan H, Cai J, Zhu X, Li J, Li M (2017) CCT6A suppresses SMAD2 and promotes prometastatic TGF-beta signaling. J Clin Invest 127(5):1725–1740.  https://doi.org/10.1172/JCI90439CrossRefPubMedPubMedCentralGoogle Scholar
  160. 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 Chaperon 6(4):345–350.  https://doi.org/10.1379/1466-1268(2001)006<0345:Ieoccc>2.0.Co;2
  161. 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(52):37070–37078.  https://doi.org/10.1074/jbc.274.52.37070
  162. Zang Y, Jin M, Wang H, Cui Z, Kong L, Liu C, Cong Y (2016) Staggered ATP binding mechanism of eukaryotic chaperonin TRiC (CCT) revealed through high-resolution cryo-EM. Nat Struct Mol Biol 23(12):1083–1091.  https://doi.org/10.1038/nsmb.3309CrossRefPubMedGoogle Scholar
  163. Zang Y, Wang H, Cui Z, Jin M, Liu C, Han W, Wang Y, Cong Y (2018) Development of a yeast internal-subunit eGFP labeling strategy and its application in subunit identification in eukaryotic group II chaperonin TRiC/CCT. Sci Rep 8(1):2374.  https://doi.org/10.1038/s41598-017-18962-yCrossRefPubMedPubMedCentralGoogle Scholar
  164. Zhang J, Baker ML, Schroder GF, Douglas NR, Reissmann S, Jakana J, Dougherty M, Fu CJ, Levitt M, Ludtke SJ, Frydman J, Chiu W (2010) Mechanism of folding chamber closure in a group II chaperonin. Nature 463(7279):379–383.  https://doi.org/10.1038/nature08701CrossRefPubMedPubMedCentralGoogle Scholar
  165. Zhang Q, Yu D, Seo S, Stone EM, Sheffield VC (2012) Intrinsic protein-protein interaction-mediated and chaperonin-assisted sequential assembly of stable bardet-biedl syndrome protein complex, the BBSome. J Biol Chem 287(24):20625–20635.  https://doi.org/10.1074/jbc.M112.341487CrossRefPubMedPubMedCentralGoogle Scholar
  166. 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(1):101–109.  https://doi.org/10.1016/j.canlet.2015.12.029CrossRefPubMedGoogle Scholar
  167. Zhao X, Chen XQ, Han E, Hu Y, Paik P, Ding Z, Overman J, Lau AL, Shahmoradian SH, Chiu W, Thompson LM, Wu C, Mobley WC (2016) TRiC subunits enhance BDNF axonal transport and rescue striatal atrophy in Huntington’s disease. Proc Natl Acad Sci USA 113(38):E5655–E5664.  https://doi.org/10.1073/pnas.1603020113CrossRefPubMedGoogle Scholar
  168. Zou Q, Yang ZL, Yuan Y, Li JH, Liang LF, Zeng GX, Chen SL (2013) Clinicopathological features and CCT2 and PDIA2 expression in gallbladder squamous/adenosquamous carcinoma and gallbladder adenocarcinoma. World J Surg Oncol 11:143.  https://doi.org/10.1186/1477-7819-11-143

Copyright information

© Springer Nature Switzerland AG 2019

Authors and Affiliations

  • Mingliang Jin
    • 1
  • Caixuan Liu
    • 1
  • Wenyu Han
    • 1
  • Yao Cong
    • 1
    • 2
    Email author
  1. 1.National Center for Protein Science Shanghai, State Key Laboratory of Molecular BiologyCAS Center for Excellence in Molecular Cell Science, Shanghai Institute of Biochemistry and Cell Biology, Chinese Academy of Sciences, University of Chinese Academy of SciencesShanghaiChina
  2. 2.Shanghai Science Research Center, Chinese Academy of SciencesShanghaiChina

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