LABS: linear amplification-based bisulfite sequencing for ultrasensitive cancer detection from cell-free DNA.

Humans Neoplasms / genetics DNA Methylation Sequence Analysis, DNA / methods Sulfites Cell-Free Nucleic Acids Nucleic Acid Amplification Techniques / methods DNA Copy Number Variations DNA, Neoplasm / genetics Circulating Tumor DNA / genetics
Bisulfite sequencing Cancer detection Cell-free DNA Linear amplification Low-input DNA

Journal

Genome biology
ISSN: 1474-760X
Titre abrégé: Genome Biol
Pays: England
ID NLM: 100960660

Informations de publication

Date de publication:
14 Jun 2024
Historique:
received: 14 11 2023
accepted: 29 04 2024
medline: 15 6 2024
pubmed: 15 6 2024
entrez: 14 6 2024
Statut: epublish

Résumé

Methylation-based liquid biopsies show promises in detecting cancer using circulating cell-free DNA; however, current limitations impede clinical application. Most assays necessitate substantial DNA inputs, posing challenges. Additionally, underrepresented tumor DNA fragments may go undetected during exponential amplification steps of traditional sequencing methods. Here, we report linear amplification-based bisulfite sequencing (LABS), enabling linear amplification of bisulfite-treated DNA fragments in a genome-wide, unbiased fashion, detecting cancer abnormalities with sub-nanogram inputs. Applying LABS to 100 patient samples revealed cancer-specific patterns, copy number alterations, and enhanced cancer detection accuracy by identifying tissue-of-origin and immune cell composition.

Identifiants

DOI: 10.1186/s13059-024-03262-2 PMID: 38877540
pubmed: 38877540
doi: 10.1186/s13059-024-03262-2
pii: 10.1186/s13059-024-03262-2
doi:

Substances chimiques

Sulfites 0
Cell-Free Nucleic Acids 0
hydrogen sulfite OJ9787WBLU
DNA, Neoplasm 0
Circulating Tumor DNA 0

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Pagination

157

Subventions

Organisme : NHGRI NIH HHS
ID : R01 HG006827
Pays : United States
Organisme : NCI NIH HHS
ID : R33 CA269100
Pays : United States
Organisme : NIGMS NIH HHS
ID : R01 GM126553
Pays : United States
Organisme : NHGRI NIH HHS
ID : R01 HG011883
Pays : United States
Organisme : NCI NIH HHS
ID : U01 CA217078
Pays : United States

Informations de copyright

© 2024. The Author(s).

Références

Schwarzenbach H, Hoon DSB, Pantel K. Cell-free nucleic acids as biomarkers in cancer patients. Nat Rev Cancer. 2011;11:426–37.
doi: 10.1038/nrc3066 pubmed: 21562580
Alix-Panabières C, Pantel K. Clinical applications of circulating tumor cells and circulating tumor DNA as liquid biopsy. Cancer Discov. 2016;6:479–91.
doi: 10.1158/2159-8290.CD-15-1483 pubmed: 26969689
Lo YMD, Han DSC, Jiang P, Chiu RWK. Epigenetics, fragmentomics, and topology of cell-free DNA in liquid biopsies. Science. 2021;372:eaaw3616.
doi: 10.1126/science.aaw3616 pubmed: 33833097
Murtaza M, Dawson S-J, Tsui DWY, Gale D, Forshew T, Piskorz AM, Parkinson C, Chin S-F, Kingsbury Z, Wong ASC, et al. Non-invasive analysis of acquired resistance to cancer therapy by sequencing of plasma DNA. Nature. 2013;497:108–12.
doi: 10.1038/nature12065 pubmed: 23563269
Bettegowda C, Sausen M, Leary RJ, Kinde I, Wang Y, Agrawal N, Bartlett BR, Wang H, Luber B, Alani RM, et al. Detection of circulating tumor DNA in early- and late-stage human malignancies. Sci Transl Med. 2014;6:224ra224.
doi: 10.1126/scitranslmed.3007094
Feng H, Jin P, Wu H. Disease prediction by cell-free DNA methylation. Brief Bioinform. 2018;20:585–97.
doi: 10.1093/bib/bby029 pmcid: 6556903
Chan KCA, Jiang P, Chan CWM, Sun K, Wong J, Hui EP, Chan SL, Chan WC, Hui DSC, Ng SSM, et al. Noninvasive detection of cancer-associated genome-wide hypomethylation and copy number aberrations by plasma DNA bisulfite sequencing. Proc Natl Acad Sci. 2013;110:18761–8.
doi: 10.1073/pnas.1313995110 pubmed: 24191000 pmcid: 3839703
Guo S, Diep D, Plongthongkum N, Fung H-L, Zhang K, Zhang K. Identification of methylation haplotype blocks aids in deconvolution of heterogeneous tissue samples and tumor tissue-of-origin mapping from plasma DNA. Nat Genet. 2017;49:635–42.
doi: 10.1038/ng.3805 pubmed: 28263317 pmcid: 5374016
Kang S, Li Q, Chen Q, Zhou Y, Park S, Lee G, Grimes B, Krysan K, Yu M, Wang W, et al. CancerLocator: non-invasive cancer diagnosis and tissue-of-origin prediction using methylation profiles of cell-free DNA. Genome Biol. 2017;18:53.
doi: 10.1186/s13059-017-1191-5 pubmed: 28335812 pmcid: 5364586
Xu RH, Wei W, Krawczyk M, Wang W, Luo H, Flagg K, Yi S, Shi W, Quan Q, Li K, et al. Circulating tumour DNA methylation markers for diagnosis and prognosis of hepatocellular carcinoma. Nat Mater. 2017;16:1155–61.
doi: 10.1038/nmat4997 pubmed: 29035356
Li W, Li Q, Kang S, Same M, Zhou Y, Sun C, Liu C-C, Matsuoka L, Sher L, Wong WH, et al. CancerDetector: ultrasensitive and non-invasive cancer detection at the resolution of individual reads using cell-free DNA methylation sequencing data. Nucleic Acids Res. 2018;46:e89–e89.
doi: 10.1093/nar/gky423 pubmed: 29897492 pmcid: 6125664
Liu MC, Oxnard GR, Klein EA, Swanton C, Seiden MV, Liu MC, Oxnard GR, Klein EA, Smith D, Richards D, et al. Sensitive and specific multi-cancer detection and localization using methylation signatures in cell-free DNA. Ann Oncol. 2020;31:745–59.
doi: 10.1016/j.annonc.2020.02.011 pubmed: 33506766
Siejka-Zielińska P, Cheng J, Jackson F, Liu Y, Soonawalla Z, Reddy S, Silva M, Puta L, McCain MV, Culver EL, et al. Cell-free DNA TAPS provides multimodal information for early cancer detection. Sci Adv. 2021;7:eabh0534.
doi: 10.1126/sciadv.abh0534 pubmed: 34516908 pmcid: 8442905
Jones PA. Functions of DNA methylation: islands, start sites, gene bodies and beyond. Nat Rev Genet. 2012;13:484–92.
doi: 10.1038/nrg3230 pubmed: 22641018
Neri F, Rapelli S, Krepelova A, Incarnato D, Parlato C, Basile G, Maldotti M, Anselmi F, Oliviero S. Intragenic DNA methylation prevents spurious transcription initiation. Nature. 2017;543:72–7.
doi: 10.1038/nature21373 pubmed: 28225755
Lister R, Pelizzola M, Dowen RH, Hawkins RD, Hon G, Tonti-Filippini J, Nery JR, Lee L, Ye Z, Ngo Q-M, et al. Human DNA methylomes at base resolution show widespread epigenomic differences. Nature. 2009;462:315–22.
doi: 10.1038/nature08514 pubmed: 19829295 pmcid: 2857523
Olova N, Krueger F, Andrews S, Oxley D, Berrens RV, Branco MR, Reik W. Comparison of whole-genome bisulfite sequencing library preparation strategies identifies sources of biases affecting DNA methylation data. Genome Biol. 2018;19:33.
doi: 10.1186/s13059-018-1408-2 pubmed: 29544553 pmcid: 5856372
Hariharan R, Jenkins M. Utility of the methylated SEPT9 test for the early detection of colorectal cancer: a systematic review and meta-analysis of diagnostic test accuracy. BMJ Open Gastroenterol. 2020;7:e000355.
doi: 10.1136/bmjgast-2019-000355 pubmed: 32128229 pmcid: 7039590
Moss J, Magenheim J, Neiman D, Zemmour H, Loyfer N, Korach A, Samet Y, Maoz M, Druid H, Arner P, et al. Comprehensive human cell-type methylation atlas reveals origins of circulating cell-free DNA in health and disease. Nat Commun. 2018;9:5068.
doi: 10.1038/s41467-018-07466-6 pubmed: 30498206 pmcid: 6265251
Loyfer N, Magenheim J, Peretz A, Cann G, Bredno J, Klochendler A, Fox-Fisher I, Shabi-Porat S, Hecht M, Pelet T, et al. A DNA methylation atlas of normal human cell types. Nature. 2023;613:355–64.
doi: 10.1038/s41586-022-05580-6 pubmed: 36599988 pmcid: 9811898
Cui X-L, Nie J, Ku J, Dougherty U, West-Szymanski DC, Collin F, Ellison CK, Sieh L, Ning Y, Deng Z, et al. A human tissue map of 5-hydroxymethylcytosines exhibits tissue specificity through gene and enhancer modulation. Nat Commun. 2020;11:6161.
doi: 10.1038/s41467-020-20001-w pubmed: 33268789 pmcid: 7710742
Sun K, Jiang P, Chan KCA, Wong J, Cheng YKY, Liang RHS, Chan WK, Ma ESK, Chan SL, Cheng SH, et al. Plasma DNA tissue mapping by genome-wide methylation sequencing for noninvasive prenatal, cancer, and transplantation assessments. Proc Natl Acad Sci. 2015;112:E5503-12.
doi: 10.1073/pnas.1508736112 pubmed: 26392541 pmcid: 4603482
Yin F, Zhao R, Gorja DR, Fu X, Lu N, Huang H, Xu B, Chen H, Shim J-H, Liu K, et al. Novel dual inhibitor for targeting PIM1 and FGFR1 kinases inhibits colorectal cancer growth in vitro and patient-derived xenografts in vivo. Acta Pharmaceutica Sinica B. 2022;12:4122–37.
doi: 10.1016/j.apsb.2022.07.005 pubmed: 36386480 pmcid: 9643289
Luan Y, Li X, Luan Y, Zhao R, Li Y, Liu L, Hao Y, Oleg Vladimir B, Jia L. Circulating lncRNA UCA1 promotes malignancy of colorectal cancer via the miR-143/MYO6 axis. Mol Ther Nucleic Acids. 2020;19:790–803.
doi: 10.1016/j.omtn.2019.12.009 pubmed: 31955010
Rahaman MH, Lam F, Zhong L, Teo T, Adams J, Yu M, Milne RW, Pepper C, Lokman NA, Ricciardelli C, et al. Targeting CDK9 for treatment of colorectal cancer. Mol Oncol. 2019;13:2178–93.
doi: 10.1002/1878-0261.12559 pubmed: 31398271 pmcid: 6763784
Chen C, Xing D, Tan L, Li H, Zhou G, Huang L, Xie XS. Single-cell whole-genome analyses by linear amplification via transposon insertion (LIANTI). Science. 2017;356:189–94.
doi: 10.1126/science.aak9787 pubmed: 28408603 pmcid: 5538131
Zheng SC, Breeze CE, Beck S, Teschendorff AE. Identification of differentially methylated cell types in epigenome-wide association studies. Nat Methods. 2018;15:1059–66.
doi: 10.1038/s41592-018-0213-x pubmed: 30504870 pmcid: 6277016
R Core Team R: R: a language and environment for statistical computing. 2013.
Cui X-L, Nie J, Zhu H, Kowitwanich K, Beadell AV, West-Szymanski DC, Zhang Zhou Z, Dougherty U, Kwesi A, Deng Z, et al: LABS: linear amplification-based bisulfite sequencing for ultrasensitive cancer detection from cell-free DNA. GSE186007. Gene Expression Omnibus. https://www.ncbi.nlm.nih.gov/geo/query/acc.cgi?acc=GSE186007 . (2024)
Cui X-L, Nie J, Zhu H, Kowitwanich K, Beadell AV, West-Szymanski DC, Zhang Zhou Z, Dougherty U, Kwesi A, Deng Z, et al: LABS: linear amplification-based bisulfite sequencing for ultrasensitive cancer detection from cell-free DNA. Github. https://github.com/xlcui/LABS . (2024)
Cui X-L, Nie J, Zhu H, Kowitwanich K, Beadell AV, West-Szymanski DC, Zhang Zhou Z, Dougherty U, Kwesi A, Deng Z, et al: LABS: linear amplification-based bisulfite sequencing for ultrasensitive cancer detection from cell-free DNA. Zenodo. https://zenodo.org/doi/10.5281/zenodo.11061161 . (2024)

Auteurs

Xiao-Long Cui (XL)

Department of Chemistry, Department of Biochemistry and Molecular Biology, Institute for Biophysical Dynamics, The University of Chicago, Chicago, IL, USA.
Howard Hughes Medical Institute, The University of Chicago, Chicago, IL, USA.
Department of Preventive Medicine, Northwestern University Feinberg School of Medicine, Chicago, IL, USA.

Ji Nie (J)

Department of Chemistry, Department of Biochemistry and Molecular Biology, Institute for Biophysical Dynamics, The University of Chicago, Chicago, IL, USA.
Howard Hughes Medical Institute, The University of Chicago, Chicago, IL, USA.

Houxiang Zhu (H)

Department of Medicine, The University of Chicago, Chicago, IL, USA.
Department of Human Genetics, The University of Chicago, Chicago, IL, USA.

Krissana Kowitwanich (K)

Department of Chemistry, Department of Biochemistry and Molecular Biology, Institute for Biophysical Dynamics, The University of Chicago, Chicago, IL, USA.
Howard Hughes Medical Institute, The University of Chicago, Chicago, IL, USA.

Alana V Beadell (AV)

Department of Chemistry, Department of Biochemistry and Molecular Biology, Institute for Biophysical Dynamics, The University of Chicago, Chicago, IL, USA.
Howard Hughes Medical Institute, The University of Chicago, Chicago, IL, USA.

Diana C West-Szymanski (DC)

Department of Chemistry, Department of Biochemistry and Molecular Biology, Institute for Biophysical Dynamics, The University of Chicago, Chicago, IL, USA.
Howard Hughes Medical Institute, The University of Chicago, Chicago, IL, USA.
Department of Medicine, The University of Chicago, Chicago, IL, USA.

Zhou Zhang (Z)

Department of Preventive Medicine, Northwestern University Feinberg School of Medicine, Chicago, IL, USA.

Urszula Dougherty (U)

Department of Medicine, The University of Chicago, Chicago, IL, USA.

Akushika Kwesi (A)

Department of Medicine, The University of Chicago, Chicago, IL, USA.

Zifeng Deng (Z)

Department of Medicine, The University of Chicago, Chicago, IL, USA.

Yan Li (Y)

Department of Medicine, The University of Chicago, Chicago, IL, USA.
Department of Human Genetics, The University of Chicago, Chicago, IL, USA.

Danqing Meng (D)

Department of Molecular Biosciences, Northwestern University, Evanston, IL, USA.

Kevin Roggin (K)

Department of Surgery, The University of Chicago, Chicago, IL, USA.

Teresa Barry (T)

Department of Medicine, The University of Chicago, Chicago, IL, USA.

Ryan Owyang (R)

Department of Chemistry, Department of Biochemistry and Molecular Biology, Institute for Biophysical Dynamics, The University of Chicago, Chicago, IL, USA.
Howard Hughes Medical Institute, The University of Chicago, Chicago, IL, USA.

Ben Fefferman (B)

Department of Chemistry, Department of Biochemistry and Molecular Biology, Institute for Biophysical Dynamics, The University of Chicago, Chicago, IL, USA.
Howard Hughes Medical Institute, The University of Chicago, Chicago, IL, USA.

Chang Zeng (C)

Department of Preventive Medicine, Northwestern University Feinberg School of Medicine, Chicago, IL, USA.

Lu Gao (L)

Department of Chemistry, Department of Biochemistry and Molecular Biology, Institute for Biophysical Dynamics, The University of Chicago, Chicago, IL, USA.
Howard Hughes Medical Institute, The University of Chicago, Chicago, IL, USA.
Department of Medicine, The University of Chicago, Chicago, IL, USA.

Carolyn W T Zhao (CWT)

Department of Chemistry, Department of Biochemistry and Molecular Biology, Institute for Biophysical Dynamics, The University of Chicago, Chicago, IL, USA.
Howard Hughes Medical Institute, The University of Chicago, Chicago, IL, USA.

Yuri Malina (Y)

Department of Chemistry, Department of Biochemistry and Molecular Biology, Institute for Biophysical Dynamics, The University of Chicago, Chicago, IL, USA.
Howard Hughes Medical Institute, The University of Chicago, Chicago, IL, USA.

Jiangbo Wei (J)

Department of Chemistry, Department of Biochemistry and Molecular Biology, Institute for Biophysical Dynamics, The University of Chicago, Chicago, IL, USA.
Howard Hughes Medical Institute, The University of Chicago, Chicago, IL, USA.

Melanie Weigert (M)

Department of Obstetrics and Gynecology/Section of Gynecologic Oncology, The University of Chicago, Chicago, IL, USA.

Wenjun Kang (W)

Department of Medicine, The University of Chicago, Chicago, IL, USA.
Department of Human Genetics, The University of Chicago, Chicago, IL, USA.

Ajay Goel (A)

City of Hope Comprehensive Cancer Center, Duarte, CA, USA.

Brian C-H Chiu (BC)

Department of Public Health Sciences, The University of Chicago, Chicago, IL, USA.

Marc Bissonnette (M)

Department of Medicine, The University of Chicago, Chicago, IL, USA.

Wei Zhang (W)

Department of Preventive Medicine, Northwestern University Feinberg School of Medicine, Chicago, IL, USA. wei.zhang1@northwestern.edu.
The Robert H. Lurie Comprehensive Cancer Center, Northwestern University Feinberg School of Medicine, Chicago, IL, USA. wei.zhang1@northwestern.edu.

Mengjie Chen (M)

Department of Medicine, The University of Chicago, Chicago, IL, USA. mengjiechen@uchicago.edu.
Department of Human Genetics, The University of Chicago, Chicago, IL, USA. mengjiechen@uchicago.edu.

Chuan He (C)

Department of Chemistry, Department of Biochemistry and Molecular Biology, Institute for Biophysical Dynamics, The University of Chicago, Chicago, IL, USA. chuanhe@uchicago.edu.
Howard Hughes Medical Institute, The University of Chicago, Chicago, IL, USA. chuanhe@uchicago.edu.

Articles similaires

Comprehensive comparative analysis and development of molecular markers for Lasianthus species based on complete chloroplast genome sequences.

Yue Zhang, Meifang Song, Deying Tang et al.
1.00
Genome, Chloroplast Phylogeny Genetic Markers Base Composition High-Throughput Nucleotide Sequencing

[Redispensing of expensive oral anticancer medicines: a practical application].

Lisanne N van Merendonk, Kübra Akgöl, Bastiaan Nuijen
1.00
Humans Antineoplastic Agents Administration, Oral Drug Costs Counterfeit Drugs

Smoking Cessation and Incident Cardiovascular Disease.

Jun Hwan Cho, Seung Yong Shin, Hoseob Kim et al.
1.00
Humans Male Smoking Cessation Cardiovascular Diseases Female

Evaluation of Low-Value Services Across Major Medicare Advantage Insurers and Traditional Medicare.

Ciara Duggan, Adam L Beckman, Ishani Ganguli et al.
1.00
Humans United States Aged Cross-Sectional Studies Medicare Part C

Classifications MeSH

questionsmedicales.fr › Eucaryotes › Animaux › Chordés › Vertébrés › Mammifères › Eutheria › Primates › Haplorhini › Catarrhini › Hominidae › Humains › LABS: linear amplification-based bisulfite...
questionsmedicales.fr › Tumeurs › LABS: linear amplification-based bisulfite...
questionsmedicales.fr › Phénomènes génétiques › Méthylation de l'ADN › LABS: linear amplification-based bisulfite...
questionsmedicales.fr › Techniques d'investigation › Techniques génétiques › Analyse de séquence › Analyse de séquence d'ADN › LABS: linear amplification-based bisulfite...
questionsmedicales.fr › Produits chimiques inorganiques › Sulfites › LABS: linear amplification-based bisulfite...
questionsmedicales.fr › Acides nucléiques, nucléotides et nucléosides › Acides nucléiques › Acides nucléiques acellulaires › LABS: linear amplification-based bisulfite...
questionsmedicales.fr › Techniques d'investigation › Techniques génétiques › Techniques d'amplification d'acides nucléiques › LABS: linear amplification-based bisulfite...
questionsmedicales.fr › Phénomènes génétiques › Variation génétique › Polymorphisme génétique › Variation structurale du génome › Variations de nombre de copies de segment d'ADN › LABS: linear amplification-based bisulfite...
questionsmedicales.fr › Acides nucléiques, nucléotides et nucléosides › Acides nucléiques › ADN › ADN tumoral › LABS: linear amplification-based bisulfite...
questionsmedicales.fr › Acides nucléiques, nucléotides et nucléosides › Acides nucléiques › ADN › ADN tumoral › ADN tumoral circulant › LABS: linear amplification-based bisulfite...