Biophysical Reviews

, Volume 11, Issue 6, pp 1007–1015 | Cite as

Plasmodium falciparum R2TP complex: driver of parasite Hsp90 function

  • Thiago V. Seraphim
  • Graham Chakafana
  • Addmore ShonhaiEmail author
  • Walid A. HouryEmail author


Heat shock protein 90 (Hsp90) is essential for the development of the main malaria agent, Plasmodium falciparum. Inhibitors that target Hsp90 function are known to not only kill the parasite, but also reverse resistance of the parasite to traditional antimalarials such as chloroquine. For this reason, Hsp90 has been tagged as a promising antimalarial drug target. As a molecular chaperone, Hsp90 facilitates folding of proteins such as steroid hormone receptors and kinases implicated in cell cycle and development. Central to Hsp90 function is its regulation by several co-chaperones. Various co-chaperones interact with Hsp90 to modulate its co-operation with other molecular chaperones such as Hsp70 and to regulate its interaction with substrates. The role of Hsp90 in the development of malaria parasites continues to receive research attention, and several Hsp90 co-chaperones have been mapped out. Recently, focus has shifted to P. falciparum R2TP proteins, which are thought to couple Hsp90 to a diverse set of client proteins. R2TP proteins are generally known to form a complex with Hsp90, and this complex drives multiple cellular processes central to signal transduction and cell division. Given the central role that the R2TP complex may play, the current review highlights the structure-function features of Hsp90 relative to R2TPs of P. falciparum.


Plasmodium falciparum Heat shock protein 90 R2TP proteins 


Funding information

TVS was supported by a CNPq-Brazil fellowship (202192/2015-6). This work was supported by a CIHR Project grant (PJT-148564) to WAH. This project was supported through a grant (PR1099/4-1) provided to A.S. by the Deutsche Forchungsgemeinshaft (DFG) under the theme, “German–African Cooperation Projects in Infectiology.” We are grateful to the Department of Science and Technology/National Research Foundation (NRF) of South Africa for providing an equipment grant (UID, 75464) and NRF mobility grant (UID, 92598) awarded to A.S.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical approval

This article does not contain any studies with human participants or animals performed by any of the authors.


  1. Absalon S, Robbins JA, Dvorin JD (2016) An essential malaria protein defines the architecture of blood-stage and transmission-stage parasites. Nat Commun 7:11449PubMedPubMedCentralGoogle Scholar
  2. Ahmad M, Tuteja R (2013a) Plasmodium falciparum RuvB1 is an active DNA helicase and translocates in the 5'-3' direction. Gene 515:99–109PubMedGoogle Scholar
  3. Ahmad M, Tuteja R (2013b) Plasmodium falciparum RuvB2 translocates in 5'-3' direction, relocalizes during schizont stage and its enzymatic activities are up regulated by RuvB3 of the same complex. Biochim Biophys Acta 1834:2795–2811PubMedGoogle Scholar
  4. Ahmad M, Singh S, Afrin F, Tuteja R (2012) Novel RuvB nuclear ATPase is specific to intraerythrocytic mitosis during schizogony of Plasmodium falciparum. Mol Biochem Parasitol 185:58–65PubMedGoogle Scholar
  5. Ahmad M, Afrin F, Tuteja R (2013) Identification of R2TP complex of Leishmania donovani and Plasmodium falciparum using genome wide in-silico analysis. Commun Integr Biol 6:e26005PubMedPubMedCentralGoogle Scholar
  6. Ammelburg M, Frickey T, Lupas AN (2006) Classification of AAA+ proteins. J Struct Biol 156:2–11PubMedGoogle Scholar
  7. Back R, Dominguez C, Rothe B, Bobo C, Beaufils C, Morera S, Meyer P, Charpentier B, Branlant C, Allain FH et al (2013) High-resolution structural analysis shows how Tah1 tethers Hsp90 to the R2TP complex. Structure 21:1834–1847PubMedGoogle Scholar
  8. Banumathy G, Singh V, Pavithra SR, Tatu U (2003) Heat shock protein 90 is essential for Plasmodium falciparum growth in human erythrocytes. J Biol Chem 278:18336–18345PubMedGoogle Scholar
  9. Benbahouche Nel H, Iliopoulos I, Torok I, Marhold J, Henri J, Kajava AV, Farkas R, Kempf T, Schnolzer M, Meyer P et al (2014) Drosophila Spag is the homolog of RNA polymerase II-associated protein 3 (RPAP3) and recruits the heat shock proteins 70 and 90 (Hsp70 and Hsp90) during the assembly of cellular machineries. J Biol Chem 289:6236–6247PubMedGoogle Scholar
  10. Bizarro J, Dodre M, Huttin A, Charpentier B, Schlotter F, Branlant C, Verheggen C, Massenet S, Bertrand E (2015) NUFIP and the HSP90/R2TP chaperone bind the SMN complex and facilitate assembly of U4-specific proteins. Nucleic Acids Res 43:8973–8989PubMedPubMedCentralGoogle Scholar
  11. Boulon S, Marmier-Gourrier N, Pradet-Balade B, Wurth L, Verheggen C, Jady BE, Rothe B, Pescia C, Robert MC, Kiss T et al (2008) The Hsp90 chaperone controls the biogenesis of L7Ae RNPs through conserved machinery. J Cell Biol 180:579–595PubMedPubMedCentralGoogle Scholar
  12. Boulon S, Pradet-Balade B, Verheggen C, Molle D, Boireau S, Georgieva M, Azzag K, Robert MC, Ahmad Y, Neel H et al (2010) HSP90 and its R2TP/Prefoldin-like cochaperone are involved in the cytoplasmic assembly of RNA polymerase II. Mol Cell 39:912–924PubMedPubMedCentralGoogle Scholar
  13. Cai Y, Jin J, Tomomori-Sato C, Sato S, Sorokina I, Parmely TJ, Conaway RC, Conaway JW (2003) Identification of new subunits of the multiprotein mammalian TRRAP/TIP60-containing histone acetyltransferase complex. J Biol Chem 278:42733–42736PubMedGoogle Scholar
  14. Chua CS, Low H, Lehming N, Sim TS (2012) Molecular analysis of Plasmodium falciparum co-chaperone Aha1 supports its interaction with and regulation of Hsp90 in the malaria parasite. Int J Biochem Cell Biol 44:233–245PubMedGoogle Scholar
  15. Cloutier P, Poitras C, Durand M, Hekmat O, Fiola-Masson E, Bouchard A, Faubert D, Chabot B, Coulombe B (2017) R2TP/Prefoldin-like component RUVBL1/RUVBL2 directly interacts with ZNHIT2 to regulate assembly of U5 small nuclear ribonucleoprotein. Nat Commun 8:15615PubMedPubMedCentralGoogle Scholar
  16. Corey VC, Lukens AK, Istvan ES, MCS L, Franco V, Magistrado P, Coburn-Flynn S-KT, Fuchs O, Gnädig NF (2016) A broad analysis of resistance development in the malaria parasite. Nat Commun 7:11901PubMedPubMedCentralGoogle Scholar
  17. Daniyan MO, Przyborski JM, Shonhai A (2019) Partners in mischief: functional networks of heat shock proteins of Plasmodium falciparum and their influence on parasite virulence. Biomolecules 9:295PubMedCentralGoogle Scholar
  18. Elnatan D, Betegon M, Liu Y, Ramelot T, Kennedy MA, Agard DA (2017) Symmetry broken and rebroken during the ATP hydrolysis cycle of the mitochondrial Hsp90 TRAP1. e25235.
  19. Gangwar D, Kalita MK, Gupta D, Chauhan VS, Mohmmed A (2009) A systematic classification of Plasmodium falciparum P-loop NTPases: structural and functional correlation. Malar J 8:69PubMedPubMedCentralGoogle Scholar
  20. Gitau GW, Mandal P, Blatch GL, Przyborski J, Shonhai A (2012) Characterization of the Plasmodium falciparum Hsp70-Hsp90 organising protein (PfHop). Cell Stress Chaperones 17:191–202PubMedGoogle Scholar
  21. Gonzales FA, Zanchin NI, Luz JS, Oliveira CC (2005) Characterization of Saccharomyces cerevisiae Nop17p, a novel Nop58p-interacting protein that is involved in Pre-rRNA processing. J Mol Biol 346:437–455PubMedGoogle Scholar
  22. Gorynia S, Bandeiras TM, Pinho FG, CE MV, Vonrhein C, Round A, Svergun DI, Donner P, Matias PM, Carrondo MA (2011) Structural and functional insights into a dodecameric molecular machine - the RuvBL1/RuvBL2 complex. J Struct Biol 176:279–291PubMedGoogle Scholar
  23. Halpin JC, Huang B, Sun M, Street TO (2016) Crowding activates heat shock protein 90. J Biol Chem 291:6447–6455PubMedPubMedCentralGoogle Scholar
  24. Horejsi Z, Takai H, Adelman CA, Collis SJ, Flynn H, Maslen S, Skehel JM, de Lange T, Boulton SJ (2010) CK2 phospho-dependent binding of R2TP complex to TEL2 is essential for mTOR and SMG1 stability. Mol Cell 39:839–850PubMedGoogle Scholar
  25. Horejsi Z, Stach L, Flower TG, Joshi D, Flynn H, Skehel JM, O’Reilly NJ, Ogrodowicz RW, Smerdon SJ, Boulton SJ (2014) Phosphorylation-dependent PIH1D1 interactions define substrate specificity of the R2TP cochaperone complex. Cell reports 7:19–26PubMedPubMedCentralGoogle Scholar
  26. Hoter A, El-Sabban ME, Naim HY (2018) The Hsp90 family: structure, regulation, function, and implications in health and disease. Int J Mol Sci 19:2560PubMedCentralGoogle Scholar
  27. Ismail HM, Barton V, Phanchana M, Charoensutthivarakul S, Wong MH, Hemingway J, Biagini GA, O’Neill PM, Ward SA (2016) Artemisinin activity-based probes identify multiple molecular targets within the asexual stage of the malaria parasites Plasmodium falciparum 3D7. Proc Natl Acad Sci USA 113:2080–2085PubMedGoogle Scholar
  28. Iyer LM, Leipe DD, Koonin EV, Aravind L (2004) Evolutionary history and higher order classification of AAA+ ATPases. J Struct Biol 146:11–31PubMedGoogle Scholar
  29. Izumi N, Yamashita A, Iwamatsu A, Kurata R, Nakamura H, Saari B, Hirano H, Anderson P, Ohno S (2010) AAA+ proteins RUVBL1 and RUVBL2 coordinate PIKK activity and function in nonsense-mediated mRNA decay. Sci Signal 3:27Google Scholar
  30. Jimenez B, Ugwu F, Zhao R, Orti L, Makhnevych T, Pineda-Lucena A, Houry WA (2012) Structure of minimal tetratricopeptide repeat domain protein Tah1 reveals mechanism of its interaction with Pih1 and Hsp90. J Biol Chem 287:5698–5709PubMedGoogle Scholar
  31. Jin J, Cai Y, Yao T, Gottschalk AJ, Florens L, Swanson SK, Gutierrez JL, Coleman MK, Workman JL, Mushegian A et al (2005) A mammalian chromatin remodeling complex with similarities to the yeast INO80 complex. J Biol Chem 280:41207–41212PubMedGoogle Scholar
  32. Johnson JL, Brown C (2009) Plasticity of the Hsp90 chaperone machine in divergent eukaryotic organisms. Cell Stress Chaperones 14:83–94PubMedGoogle Scholar
  33. Jonsson ZO, Dhar SK, Narlikar GJ, Auty R, Wagle N, Pellman D, Pratt RE, Kingston R, Dutta A (2001) Rvb1p and Rvb2p are essential components of a chromatin remodeling complex that regulates transcription of over 5% of yeast genes. J Biol Chem 276:16279–16288PubMedGoogle Scholar
  34. Kakihara Y, Houry WA (2012) The R2TP complex: discovery and functions. Biochim Biophys Acta 1:101–107Google Scholar
  35. Karagoz GE, Rudiger SG (2015) Hsp90 interaction with clients. Trends Biochem Sci 40:117–125PubMedGoogle Scholar
  36. Kravats AN, Hoskins JR, Reidy M, Johnson JL, Doyle SM, Genest O, Masison DC, Wickner S (2018) Functional and physical interaction between yeast Hsp90 and Hsp70. Proc Natl Acad Sci USA 115(10):2210–2219Google Scholar
  37. Krysztofinska EM, Evans NJ, Thapaliya A, Murray JW, Morgan RML, Martinez-Lumbreras S, Isaacson RL (2017) Structure and interactions of the TPR domain of Sgt2 with yeast chaperones and Ybr137wp. Front Mol Biosci 4:68PubMedPubMedCentralGoogle Scholar
  38. Li J, Richter K, Reinstein J, Buchner J (2013) Integration of the accelerator Aha1 in the Hsp90 co chaperone cycle. Nat Struct Mol Biol 20:326–331PubMedGoogle Scholar
  39. Li T, Jiang HL, Tong YG, Lu JJ (2018) Targeting the Hsp90-Cdc37-client protein interaction to disrupt Hsp90 chaperone machinery. J Hematol Oncol 11:59PubMedPubMedCentralGoogle Scholar
  40. Liu K, Houry WA, Blatch GL, Shonhai A (2014) Chaperones and proteases of Plasmodium falciparum. In: Shonhai A, Blatch GL (eds) Heat Shock Proteins of Malaria. Springer, Dordrecht, pp 161–187Google Scholar
  41. Lopez-Perrote A, Munoz-Hernandez H, Gil D, Llorca O (2012) Conformational transitions regulate the exposure of a DNA-binding domain in the RuvBL1-RuvBL2 complex. Nucleic Acids Res. 40:11086–11099PubMedPubMedCentralGoogle Scholar
  42. Maier AG, Rug M, O’Neill MT, Brown M, Chakravorty S, Szestak T, Chesson J, Wu Y, Hughes K, Coppel RL (2008) Exported proteins required for virulence and rigidity of Plasmodium falciparum-infected human erythrocytes. Cell 134:48–61PubMedPubMedCentralGoogle Scholar
  43. Makhnevych T, Houry WA (2012) The role of Hsp90 in protein complex assembly. Biochim Biophys Acta. 1823:674–682PubMedGoogle Scholar
  44. Malinova A, Cvackova Z, Mateju D, Horejsi Z, Abeza C, Vandermoere F, Bertrand E, Stanek D, Verheggen C (2017) Assembly of the U5 snRNP component PRPF8 is controlled by the HSP90/R2TP chaperones. J Cell Biol 216:1579–1596PubMedPubMedCentralGoogle Scholar
  45. Martino F, Pal M, Munoz-Hernandez H, Rodriguez CF, Nunez-Ramirez R, Gil-Carton D, Degliesposti G, Skehel JM, Roe SM, Prodromou C et al (2018) RPAP3 provides a flexible scaffold for coupling HSP90 to the human R2TP co-chaperone complex. Nat Commun 9:1501PubMedPubMedCentralGoogle Scholar
  46. Matias PM, Gorynia S, Donner P, Carrondo MA (2006) Crystal structure of the human AAA+ protein RuvBL1. J Biol Chem 281:38918–38929PubMedGoogle Scholar
  47. Maurizy C, Quinternet M, Abel Y, Verheggen C, Santo PE, Bourguet M, ACF P, Bragantini B, Chagot ME, Robert MC et al (2018) The RPAP3-Cterminal domain identifies R2TP-like quaternary chaperones. Nat Commun. 9:2093PubMedPubMedCentralGoogle Scholar
  48. McKeegan KS, Debieux CM, Boulon S, Bertrand E, Watkins NJ (2007) A dynamic scaffold of pre-snoRNP factors facilitates human box C/D snoRNP assembly. Mol Cell Biol 27:6782–6793PubMedPubMedCentralGoogle Scholar
  49. McKeegan KS, Debieux CM, Watkins NJ (2009) Evidence that the AAA+ proteins TIP48 and TIP49 bridge interactions between 15.5K and the related NOP56 and NOP58 proteins during box C/D snoRNP biogenesis. Mol Cell Biol 29:4971–4981PubMedPubMedCentralGoogle Scholar
  50. Miao J, Fan Q, Cui L, Li X, Wang H, Ning G, Reese JC, Cui L (2010) The MYST family histone acetyltransferase regulates gene expression and cell cycle in malaria parasite Plasmodium falciparum. Mol Microbiol 78:883–902PubMedPubMedCentralGoogle Scholar
  51. Morgan RM, Pal M, Roe SM, Pearl LH, Prodromou C (2015) Tah1 helix-swap dimerization prevents mixed Hsp90 co-chaperone complexes. Acta Crystallogr D Biol Crystallogr 71:1197–1206PubMedPubMedCentralGoogle Scholar
  52. Pal M, Morgan M, SEL P, Roe M, Parry-Morris S, Downs JA, Polier S, Pearl LH, Prodromou C (2014) Structural basis for phosphorylation-dependent recruitment of Tel2 to Hsp90 by Pih1. Structure 22:805–818PubMedPubMedCentralGoogle Scholar
  53. Pallavi R, Roy N, Nageshan RK, Talukdar P, Pavithra SR, Reddy R, Tatu U (2010) Heat shock protein 90 as a drug target against protozoan infections biochemical characterization of Hsp90 from Plasmodium falciparum and Trypanosoma evansi and evaluation of its inhibitor as a candidate drug. J Biol Chem 285:37964–37975PubMedPubMedCentralGoogle Scholar
  54. Panaretou B, Prodromou C, Roe SM, O'Brien R, Ladbury JE, Piper PW, Pearl LH (1998) ATP binding and hydrolysis are essential to the function of the Hsp90 molecular chaperone in vivo. EMBO J 17:4829–4836PubMedPubMedCentralGoogle Scholar
  55. Picard D (2002) Heat-shock protein 90, a chaperone for folding and regulation. Cell Mol Life Sci 59:1640–1648PubMedGoogle Scholar
  56. Prieto MB, Georg RC, Gonzales-Zubiate FA, Luz JS, Oliveira CC (2015) Nop17 is a key R2TP factor for the assembly and maturation of box C/D snoRNP complex. BMC Mol Biol 16:7PubMedPubMedCentralGoogle Scholar
  57. Puri T, Wendler P, Sigala B, Saibil H, Tsaneva IR (2007) Dodecameric structure and ATPase activity of the human TIP48/TIP49 complex. J Mol Biol 366:179–192PubMedGoogle Scholar
  58. Riggs DL, Roberts PJ, Chirillo SC, Cheung-Flynn J, Prapapanich V, Ratajczak T, Gaber R, Picard D, Smith DF (2003) The Hsp90-binding peptidylprolyl isomerase FKBP52 potentiates glucocorticoid signalling in vivo. EMBO J 22:1158–1167PubMedPubMedCentralGoogle Scholar
  59. Riggs D, Cox M, Cheung-Flynn J, Prapapanich V, Carrigan P, Smith D (2004) Functional specificity of co-chaperone interactions with Hsp90 client proteins. Crit Rev Biochem Mol Biol 39:279–295PubMedGoogle Scholar
  60. Rivera-Calzada A, Pal M, Munoz-Hernandez H, Luque-Ortega JR, Gil-Carton D, Degliesposti G, Skehel JM, Prodromou C, Pearl LH, Llorca O (2017) The structure of the R2TP complex defines a platform for recruiting diverse client proteins to the Hsp90 molecular chaperone system. Structure 25:1145–1152.e1144PubMedPubMedCentralGoogle Scholar
  61. Rowlands M, McAndrew C, Prodromou C, Pearl L, Kalusa A, Jones K, Workman P, Aherne W (2010) Detection of the ATPase activity of the molecular chaperones Hsp90 and Hsp72 using the Transcreener TM ADP assay kit. J Biomol Screen 15:279–286PubMedGoogle Scholar
  62. Santiago TC, Zufferey R, Mehra RS, Coleman RA, Mamoun CB (2004) The Plasmodium falciparum PfGatp is an endoplasmic reticulum membrane protein important for the initial step of malarial glycerolipid synthesis. J Biol Chem 279(10):9222–9232PubMedGoogle Scholar
  63. Scheufler C, Brinker A, Bourenkov G, Pegoraro S, Moroder L, Bartunik H, Hartl FU, Moarefi I (2000) Structure of TPR domain-peptide complexes: critical elements in the assembly of the Hsp70-Hsp90 multichaperone machine. Cell 101:199–210PubMedGoogle Scholar
  64. Sen U, Saxena H, Khurana J, Nayak A, Gupta A (2018) Plasmodium falciparum RUVBL3 protein: a novel DNA modifying enzyme and an interacting partner of essential HAT protein MYST. Sci Rep 8:10917PubMedPubMedCentralGoogle Scholar
  65. Seraphim TV, Ramos CHI, Borges JC (2014) The Interaction Networks of Hsp70 and Hsp90 in the Plasmodium and Leishmania parasites. In: Houry WA (ed) The molecular chaperones interaction networks in protein folding and degradation. New York, Springer New York, pp 445–481Google Scholar
  66. Shahinas D, Folefoc A, Pillai D (2013) Targeting Plasmodium falciparum Hsp90: towards reversing antimalarial resistance. Pathogens 2:33–35PubMedPubMedCentralGoogle Scholar
  67. Shen X, Mizuguchi G, Hamiche A, Wu C (2000) A chromatin remodelling complex involved in transcription and DNA processing. Nature 406:541–544PubMedGoogle Scholar
  68. Shonhai A (2010) Plasmodial heat shock proteins: targets for chemotherapy. FEMS Immunol Med Microbiol 58:61–74PubMedGoogle Scholar
  69. Silva NSM, Bertolino-Reis DE, Dores-Silva PR, Anneta FB, Seraphim TV, Barbosa LRS, Borges JC (2019) Structural studies of the Hsp70/Hsp90 organizing protein of Plasmodium falciparum and its modulation of Hsp70 and Hsp90 ATPase activities. Biochim Biophys Acta.
  70. Takai H, Xie Y, de Lange T, Pavletich NP (2010) Tel2 structure and function in the Hsp90-dependent maturation of mTOR and ATR complexes. Genes Dev 24:2019–2030PubMedPubMedCentralGoogle Scholar
  71. Te J, Jia L, Rogers J, Miller A, Hartson SD (2007) Novel subunits of the mammalian Hsp90 signal transduction chaperone. J Proteome Res 6:1963–1973PubMedGoogle Scholar
  72. Tian S, Yu G, He H, Zhao Y, Liu P, Marshall AG, Demeler B, Stagg SM, Li H (2017) Pih1p-Tah1p puts a lid on hexameric AAA+ ATPases Rvb1/2p. Structure 25:1519–1529PubMedPubMedCentralGoogle Scholar
  73. Torreira E, Jha S, Lopez-Blanco JR, Arias-Palomo E, Chacon P, Canas C, Ayora S, Dutta A, Llorca O (2008) Architecture of the pontin/reptin complex, essential in the assembly of several macromolecular complexes. Structure 16:1511–1520PubMedPubMedCentralGoogle Scholar
  74. Venteicher AS, Meng Z, Mason PJ, Veenstra TD, Artandi SE (2008) Identification of ATPases pontin and reptin as telomerase components essential for holoenzyme assembly. Cell 132:945–957PubMedPubMedCentralGoogle Scholar
  75. Wang T, Mäser P, Picard D (2016) Inhibition of Plasmodium falciparum Hsp90 contributes to the antimalarial activities of aminoalcohol-carbazoles. J Med Chem 59(13):6344–6352PubMedGoogle Scholar
  76. Young JC, Moarefi I, Hartl FU (2001) Hsp90, a specialized but essential protein-folding tool. J Cell Biol 154(2):267–274PubMedPubMedCentralGoogle Scholar
  77. Zhao R, Davey M, Hsu YC, Kaplanek P, Tong A, Parsons AB, Krogan N, Cagney G, Mai D, Greenblatt J et al (2005) Navigating the chaperone network: an integrative map of physical and genetic interactions mediated by the hsp90 chaperone. Cell 120:715–727PubMedGoogle Scholar
  78. Zhao R, Kakihara Y, Gribun A, Huen J, Yang G, Khanna M, Costanzo M, Brost RL, Boone C, Hughes TR et al (2008) Molecular chaperone Hsp90 stabilizes Pih1/Nop17 to maintain R2TP complex activity that regulates snoRNA accumulation. J Cell Biol 180:563–578PubMedPubMedCentralGoogle Scholar
  79. Zininga T, Makumire S, Gitau GW, Njunge JM, Pooe OJ, Klimek H, Scheurr R, Raifer H, Prinsloo E, Przyborski JM et al (2015) Plasmodium falciparum Hop (PfHop) interacts with the Hsp70 chaperone in a nucleotide-dependent fashion and exhibits ligand selectivity. PLoS One 10:e0135326PubMedPubMedCentralGoogle Scholar
  80. Zur Lage P, Stefanopoulou P, Styczynska-Soczka K, Quinn N, Mali G, von Kriegsheim A, Mill P, Jarman AP (2018) Ciliary dynein motor preassembly is regulated by Wdr92 in association with HSP90 co-chaperone, R2TP. J Cell Biol 217:2583–2598PubMedPubMedCentralGoogle Scholar

Copyright information

© International Union for Pure and Applied Biophysics (IUPAB) and Springer-Verlag GmbH Germany, part of Springer Nature 2019

Authors and Affiliations

  1. 1.Department of Biochemistryniversity of TorontoTorontoCanada
  2. 2.Department of BiochemistryUniversity of VendaThohoyandouSouth Africa
  3. 3.Department of ChemistryUniversity of TorontoTorontoCanada

Personalised recommendations