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High resolution long-read telomere sequencing reveals dynamic mechanisms in aging and cancer

Author

Listed:
  • Tobias T. Schmidt

    (Salk Institute for Biological Studies)

  • Carly Tyer

    (Inc.)

  • Preeyesh Rughani

    (Inc.)

  • Candy Haggblom

    (Salk Institute for Biological Studies)

  • Jeffrey R. Jones

    (Salk Institute for Biological Studies)

  • Xiaoguang Dai

    (Inc.)

  • Kelly A. Frazer

    (University of California, San Diego)

  • Fred H. Gage

    (Salk Institute for Biological Studies)

  • Sissel Juul

    (Inc.)

  • Scott Hickey

    (Inc.)

  • Jan Karlseder

    (Salk Institute for Biological Studies)

Abstract

Telomeres are the protective nucleoprotein structures at the end of linear eukaryotic chromosomes. Telomeres’ repetitive nature and length have traditionally challenged the precise assessment of the composition and length of individual human telomeres. Here, we present Telo-seq to resolve bulk, chromosome arm-specific and allele-specific human telomere lengths using Oxford Nanopore Technologies’ native long-read sequencing. Telo-seq resolves telomere shortening in five population doubling increments and reveals intrasample, chromosome arm-specific, allele-specific telomere length heterogeneity. Telo-seq can reliably discriminate between telomerase- and ALT-positive cancer cell lines. Thus, Telo-seq is a tool to study telomere biology during development, aging, and cancer at unprecedented resolution.

Suggested Citation

  • Tobias T. Schmidt & Carly Tyer & Preeyesh Rughani & Candy Haggblom & Jeffrey R. Jones & Xiaoguang Dai & Kelly A. Frazer & Fred H. Gage & Sissel Juul & Scott Hickey & Jan Karlseder, 2024. "High resolution long-read telomere sequencing reveals dynamic mechanisms in aging and cancer," Nature Communications, Nature, vol. 15(1), pages 1-11, December.
    • Handle: RePEc:nat:natcom:v:15:y:2024:i:1:d:10.1038_s41467-024-48917-7
    DOI: 10.1038/s41467-024-48917-7
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    1. Joe Nassour & Lucia Gutierrez Aguiar & Adriana Correia & Tobias T. Schmidt & Laura Mainz & Sara Przetocka & Candy Haggblom & Nimesha Tadepalle & April Williams & Maxim N. Shokhirev & Semih C. Akincila, 2023. "Telomere-to-mitochondria signalling by ZBP1 mediates replicative crisis," Nature, Nature, vol. 614(7949), pages 767-773, February.
    2. Suneet Agarwal & Yuin-Han Loh & Erin M. McLoughlin & Junjiu Huang & In-Hyun Park & Justine D. Miller & Hongguang Huo & Maja Okuka & Rosana Maria dos Reis & Sabine Loewer & Huck-Hui Ng & David L. Keefe, 2010. "Telomere elongation in induced pluripotent stem cells from dyskeratosis congenita patients," Nature, Nature, vol. 464(7286), pages 292-296, March.
    3. Tsung-Po Lai & Ning Zhang & Jungsik Noh & Ilgen Mender & Enzo Tedone & Ejun Huang & Woodring E. Wright & Gaudenz Danuser & Jerry W. Shay, 2017. "A method for measuring the distribution of the shortest telomeres in cells and tissues," Nature Communications, Nature, vol. 8(1), pages 1-14, December.
    4. Riham Smoom & Catherine Lee May & Vivian Ortiz & Mark Tigue & Hannah M. Kolev & Melissa Rowe & Yitzhak Reizel & Ashleigh Morgan & Nachshon Egyes & Dan Lichtental & Emmanuel Skordalakes & Klaus H. Kaes, 2023. "Telomouse—a mouse model with human-length telomeres generated by a single amino acid change in RTEL1," Nature Communications, Nature, vol. 14(1), pages 1-18, December.
    5. Wen-Wei Liao & Mobin Asri & Jana Ebler & Daniel Doerr & Marina Haukness & Glenn Hickey & Shuangjia Lu & Julian K. Lucas & Jean Monlong & Haley J. Abel & Silvia Buonaiuto & Xian H. Chang & Haoyu Cheng , 2023. "A draft human pangenome reference," Nature, Nature, vol. 617(7960), pages 312-324, May.
    6. Ting Wang & Lucinda Antonacci-Fulton & Kerstin Howe & Heather A. Lawson & Julian K. Lucas & Adam M. Phillippy & Alice B. Popejoy & Mobin Asri & Caryn Carson & Mark J. P. Chaisson & Xian Chang & Robert, 2022. "The Human Pangenome Project: a global resource to map genomic diversity," Nature, Nature, vol. 604(7906), pages 437-446, April.
    7. Joe Nassour & Robert Radford & Adriana Correia & Javier Miralles Fusté & Brigitte Schoell & Anna Jauch & Reuben J. Shaw & Jan Karlseder, 2019. "Autophagic cell death restricts chromosomal instability during replicative crisis," Nature, Nature, vol. 565(7741), pages 659-663, January.
    8. Karen H. Miga & Sergey Koren & Arang Rhie & Mitchell R. Vollger & Ariel Gershman & Andrey Bzikadze & Shelise Brooks & Edmund Howe & David Porubsky & Glennis A. Logsdon & Valerie A. Schneider & Tamara , 2020. "Telomere-to-telomere assembly of a complete human X chromosome," Nature, Nature, vol. 585(7823), pages 79-84, September.
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