Mechanism of the AAA+ ATPases Pontin and Reptin in the Biogenesis of H/ACA RNPs

Overview

Journal RNA

Specialty Molecular Biology

Date 2012 Aug 28

PMID 22923768

Citations 52

Authors

Rosario Machado-Pinilla

Dominique Liger

Nicolas Leulliot

U Thomas Meier

Affiliations

Soon will be listed here.

Abstract

The AAA+ ATPases pontin and reptin function in a staggering array of cellular processes including chromatin remodeling, transcriptional regulation, DNA damage repair, and assembly of macromolecular complexes, such as RNA polymerase II and small nucleolar (sno) RNPs. However, the molecular mechanism for all of these AAA+ ATPase associated activities is unknown. Here we document that, during the biogenesis of H/ACA RNPs (including telomerase), the assembly factor SHQ1 holds the pseudouridine synthase NAP57/dyskerin in a viselike grip, and that pontin and reptin (as components of the R2TP complex) are required to pry NAP57 from SHQ1. Significantly, the NAP57 domain captured by SHQ1 harbors most mutations underlying X-linked dyskeratosis congenita (X-DC) implicating the interface between the two proteins as a target of this bone marrow failure syndrome. Homing in on the essential first steps of H/ACA RNP biogenesis, our findings provide the first insight into the mechanism of action of pontin and reptin in the assembly of macromolecular complexes.

Citing Articles

The multi-faceted roles of R2TP complex span across regulation of gene expression, translation, and protein functional assembly.

Luthuli S, Shonhai A Biophys Rev. 2024; 15(6):1951-1965.

PMID: 38192347 PMC: 10771493. DOI: 10.1007/s12551-023-01127-9.

Advances in understanding telomerase assembly.

Klump B, Schmidt J Biochem Soc Trans. 2023; 51(6):2093-2101.

PMID: 38108475 PMC: 10754283. DOI: 10.1042/BST20230269.

Extract2Chip-Bypassing Protein Purification in Drug Discovery Using Surface Plasmon Resonance.

Paiva A, Lemos A, Busse P, Martins M, Silva D, Freitas M Biosensors (Basel). 2023; 13(10).

PMID: 37887106 PMC: 10605449. DOI: 10.3390/bios13100913.

The C-terminal extension of dyskerin is a dyskeratosis congenita mutational hotspot that modulates interaction with telomerase RNA and subcellular localization.

Qin J, Garus A, Autexier C Hum Mol Genet. 2023; 33(4):318-332.

PMID: 37879098 PMC: 10840380. DOI: 10.1093/hmg/ddad180.

Maturation of small nucleolar RNAs: from production to function.

Webster S, Ghalei H RNA Biol. 2023; 20(1):715-736.

PMID: 37796118 PMC: 10557570. DOI: 10.1080/15476286.2023.2254540.

References

Meier U . The many facets of H/ACA ribonucleoproteins. Chromosoma. 2005; 114(1):1-14. PMC: 4313906. DOI: 10.1007/s00412-005-0333-9. View

Jha S, Dutta A . RVB1/RVB2: running rings around molecular biology. Mol Cell. 2009; 34(5):521-33. PMC: 2733251. DOI: 10.1016/j.molcel.2009.05.016. View

Huber O, Menard L, Haurie V, Nicou A, Taras D, Rosenbaum J . Pontin and reptin, two related ATPases with multiple roles in cancer. Cancer Res. 2008; 68(17):6873-6. DOI: 10.1158/0008-5472.CAN-08-0547. View

Torreira E, Jha S, Lopez-Blanco J, Arias-Palomo E, Chacon P, Canas C . Architecture of the pontin/reptin complex, essential in the assembly of several macromolecular complexes. Structure. 2008; 16(10):1511-20. PMC: 2577609. DOI: 10.1016/j.str.2008.08.009. View

Gallant P . Control of transcription by Pontin and Reptin. Trends Cell Biol. 2007; 17(4):187-92. DOI: 10.1016/j.tcb.2007.02.005. View

Grozdanov P, Fernandez-Fuentes N, Fiser A, Meier U . Pathogenic NAP57 mutations decrease ribonucleoprotein assembly in dyskeratosis congenita. Hum Mol Genet. 2009; 18(23):4546-51. PMC: 2773269. DOI: 10.1093/hmg/ddp416. View

Mueller-Cajar O, Stotz M, Wendler P, Hartl F, Bracher A, Hayer-Hartl M . Structure and function of the AAA+ protein CbbX, a red-type Rubisco activase. Nature. 2011; 479(7372):194-9. DOI: 10.1038/nature10568. View

Colau G, Thiry M, Leduc V, Bordonne R, Lafontaine D . The small nucle(ol)ar RNA cap trimethyltransferase is required for ribosome synthesis and intact nucleolar morphology. Mol Cell Biol. 2004; 24(18):7976-86. PMC: 515057. DOI: 10.1128/MCB.24.18.7976-7986.2004. View

Hamma T, Ferre-DAmare A . The box H/ACA ribonucleoprotein complex: interplay of RNA and protein structures in post-transcriptional RNA modification. J Biol Chem. 2009; 285(2):805-9. PMC: 2801282. DOI: 10.1074/jbc.R109.076893. View

10.

Ye K . H/ACA guide RNAs, proteins and complexes. Curr Opin Struct Biol. 2007; 17(3):287-92. DOI: 10.1016/j.sbi.2007.05.012. View

11.

Kanemaki M, Makino Y, Yoshida T, Kishimoto T, Koga A, Yamamoto K . Molecular cloning of a rat 49-kDa TBP-interacting protein (TIP49) that is highly homologous to the bacterial RuvB. Biochem Biophys Res Commun. 1997; 235(1):64-8. DOI: 10.1006/bbrc.1997.6729. View

12.

Jonsson Z, Jha S, Wohlschlegel J, Dutta A . Rvb1p/Rvb2p recruit Arp5p and assemble a functional Ino80 chromatin remodeling complex. Mol Cell. 2004; 16(3):465-77. DOI: 10.1016/j.molcel.2004.09.033. View

13.

Yang P, Rotondo G, Porras T, Legrain P, Chanfreau G . The Shq1p.Naf1p complex is required for box H/ACA small nucleolar ribonucleoprotein particle biogenesis. J Biol Chem. 2002; 277(47):45235-42. DOI: 10.1074/jbc.M207669200. View

14.

Matera A, Terns R, Terns M . Non-coding RNAs: lessons from the small nuclear and small nucleolar RNAs. Nat Rev Mol Cell Biol. 2007; 8(3):209-20. DOI: 10.1038/nrm2124. View

15.

Kim J, Choi H, Kim B, Kim M, Lee J, Kim I . Roles of sumoylation of a reptin chromatin-remodelling complex in cancer metastasis. Nat Cell Biol. 2006; 8(6):631-9. DOI: 10.1038/ncb1415. View

16.

King T, Decatur W, Bertrand E, MAXWELL E, Fournier M . A well-connected and conserved nucleoplasmic helicase is required for production of box C/D and H/ACA snoRNAs and localization of snoRNP proteins. Mol Cell Biol. 2001; 21(22):7731-46. PMC: 99944. DOI: 10.1128/MCB.21.22.7731-7746.2001. View

17.

Aris J, Blobel G . Identification and characterization of a yeast nucleolar protein that is similar to a rat liver nucleolar protein. J Cell Biol. 1988; 107(1):17-31. PMC: 2115186. DOI: 10.1083/jcb.107.1.17. View

18.

Iyer L, Leipe D, Koonin E, Aravind L . Evolutionary history and higher order classification of AAA+ ATPases. J Struct Biol. 2004; 146(1-2):11-31. DOI: 10.1016/j.jsb.2003.10.010. View

19.

Huen J, Kakihara Y, Ugwu F, Cheung K, Ortega J, Houry W . Rvb1-Rvb2: essential ATP-dependent helicases for critical complexes. Biochem Cell Biol. 2010; 88(1):29-40. DOI: 10.1139/o09-122. View

20.

Jiang W, Middleton K, Yoon H, Fouquet C, Carbon J . An essential yeast protein, CBF5p, binds in vitro to centromeres and microtubules. Mol Cell Biol. 1993; 13(8):4884-93. PMC: 360124. DOI: 10.1128/mcb.13.8.4884-4893.1993. View