TGS1 mediates 2,2,7-trimethyl guanosine capping of the human telomerase RNA to direct telomerase dependent telomere maintenance.


Journal

Nature communications
ISSN: 2041-1723
Titre abrégé: Nat Commun
Pays: England
ID NLM: 101528555

Informations de publication

Date de publication:
28 04 2022
Historique:
received: 09 11 2020
accepted: 25 03 2022
entrez: 28 4 2022
pubmed: 29 4 2022
medline: 3 5 2022
Statut: epublish

Résumé

Pathways that direct the selection of the telomerase-dependent or recombination-based, alternative lengthening of telomere (ALT) maintenance pathway in cancer cells are poorly understood. Using human lung cancer cells and tumor organoids we show that formation of the 2,2,7-trimethylguanosine (TMG) cap structure at the human telomerase RNA 5' end by the Trimethylguanosine Synthase 1 (TGS1) is central for recruiting telomerase to telomeres and engaging Cajal bodies in telomere maintenance. TGS1 depletion or inhibition by the natural nucleoside sinefungin impairs telomerase recruitment to telomeres leading to Exonuclease 1 mediated generation of telomere 3' end protrusions that engage in RAD51-dependent, homology directed recombination and the activation of key features of the ALT pathway. This indicates a critical role for 2,2,7-TMG capping of the RNA component of human telomerase (hTR) in enforcing telomerase-dependent telomere maintenance to restrict the formation of telomeric substrates conductive to ALT. Our work introduces a targetable pathway of telomere maintenance that holds relevance for telomere-related diseases such as cancer and aging.

Identifiants

pubmed: 35484160
doi: 10.1038/s41467-022-29907-z
pii: 10.1038/s41467-022-29907-z
pmc: PMC9050681
doi:

Substances chimiques

telomerase RNA 0
Guanosine 12133JR80S
RNA 63231-63-0
Telomerase EC 2.7.7.49

Types de publication

Journal Article Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

2302

Informations de copyright

© 2022. The Author(s).

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Auteurs

Valentina Buemi (V)

Dipartimento di Scienze della Vita, Università degli Studi di Trieste, Via E. Weiss 2, 34127, Trieste, Italy.
Cancer Research UK Cancer Therapeutics Unit, The Institute of Cancer Research, London, SM2 5NG, United Kingdom.

Odessa Schillaci (O)

Dipartimento di Scienze della Vita, Università degli Studi di Trieste, Via E. Weiss 2, 34127, Trieste, Italy.

Mariangela Santorsola (M)

Dipartimento di Scienze della Vita, Università degli Studi di Trieste, Via E. Weiss 2, 34127, Trieste, Italy.

Deborah Bonazza (D)

Struttura Complessa di Anatomia ed Istologia Patologica, Azienda Sanitaria Universitaria Giuliano Isontina (ASUGI) Trieste, Strada di Fiume 447, 34149, Trieste, Italy.

Pamela Veneziano Broccia (PV)

Dipartimento di Scienze della Vita, Università degli Studi di Trieste, Via E. Weiss 2, 34127, Trieste, Italy.

Annie Zappone (A)

Dipartimento di Scienze della Vita, Università degli Studi di Trieste, Via E. Weiss 2, 34127, Trieste, Italy.

Cristina Bottin (C)

Dipartimento Universitario Clinico di Scienze Mediche Chirurgiche e della Salute, Università degli Studi di Trieste, Ospedale di Cattinara - Strada di Fiume 447, 34149, Trieste, Italy.

Giulia Dell'Omo (G)

IFOM Foundation-FIRC Institute of Molecular Oncology Foundation, Milan, 20139, Italy.

Sylvie Kengne (S)

Dipartimento di Scienze della Vita, Università degli Studi di Trieste, Via E. Weiss 2, 34127, Trieste, Italy.

Stefano Cacchione (S)

Dipartimento di Biologia e Biotecnologie, Sapienza Università di Roma, Roma, Italy.

Grazia Daniela Raffa (GD)

Dipartimento di Biologia e Biotecnologie, Sapienza Università di Roma, Roma, Italy.

Silvano Piazza (S)

International Centre for Genetic Engineering and Biotechnology (ICGEB), Area Science Park - Padriciano, 34149, Trieste, Italy.

Fabrizio d'Adda di Fagagna (FD)

IFOM Foundation-FIRC Institute of Molecular Oncology Foundation, Milan, 20139, Italy.
Istituto di Genetica Molecolare, Consiglio Nazionale delle Ricerche (IGM-CNR), Pavia, 27100, Italy.

Roberta Benetti (R)

Dipartimento di Area Medica (Dame), Università degli Studi di Udine, p.le Kolbe 4, 33100, Udine, Italy.

Maurizio Cortale (M)

Struttura Complessa di Chirurgia Toracica, Azienda Sanitaria Universitaria Giuliano Isontina (ASUGI) Trieste, Strada di Fiume 447, 34149, Trieste, Italy.

Fabrizio Zanconati (F)

Struttura Complessa di Anatomia ed Istologia Patologica, Azienda Sanitaria Universitaria Giuliano Isontina (ASUGI) Trieste, Strada di Fiume 447, 34149, Trieste, Italy.
Dipartimento Universitario Clinico di Scienze Mediche Chirurgiche e della Salute, Università degli Studi di Trieste, Ospedale di Cattinara - Strada di Fiume 447, 34149, Trieste, Italy.

Giannino Del Sal (G)

Dipartimento di Scienze della Vita, Università degli Studi di Trieste, Via E. Weiss 2, 34127, Trieste, Italy.
IFOM Foundation-FIRC Institute of Molecular Oncology Foundation, Milan, 20139, Italy.
International Centre for Genetic Engineering and Biotechnology (ICGEB), Area Science Park - Padriciano, 34149, Trieste, Italy.

Stefan Schoeftner (S)

Dipartimento di Scienze della Vita, Università degli Studi di Trieste, Via E. Weiss 2, 34127, Trieste, Italy. sschoeftner@units.it.

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