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Circulating nucleic acids as liquid biopsies for disease prediction, screening and diagnosis

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Abstract

Liquid biopsy used molecular information in body liquid to perform early diagnosis, screening, monitoring, prognosis, and treatment of various diseases. Circulating free nucleic acids (cfNA) are important diagnostic biomarkers, providing a window to accurately and immediately observe the body’s vital activity status. With the development of gene sequencing technology and bioinformatics technology, genetic, epigenetic, and fragtomics alterations that can be detected in cfDNA, as well as the expression level of miRNA and cf-mRNA can be quantified, this can reflect its tissue origin, gene regulation, genome evolution, and disease pathogenesis. This review focuses on the clinical utility of cfNA in different body liquids (blood, urine, bile), and discusses the diagnostic efficacy and accuracy of cfNA as diagnostic biomarkers in a variety of diseases. Blood is widely used to diagnose various tissue lesions for liquid biopsies as a body fluid circulating throughout the body, reflecting the state of the entire body. Bile and urine, as local circulating body fluids, can better reflect the changing state of tissues around the biliary tract and tissues around the bladder, respectively. In addition, normalized sample preservation, cfNA extraction, and detection procedures will help the practical application of cfNA in the clinic.

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References

  1. Heitzer E, Haque IS, Roberts CES, Speicher MR. Nat Rev Genet, 2019, 20: 71–88

    Article  CAS  PubMed  Google Scholar 

  2. Gardner L, Kostarelos K, Mallick P, Dive C, Hadjidemetriou M. Nat Rev Clin Oncol, 2022, 19: 551–561

    Article  PubMed  Google Scholar 

  3. Underwood JJ, Quadri RS, Kalva SP, Shah H, Sanjeeviah AR, Beg MS, Sutphin PD. Radiology, 2020, 294: 5–17

    Article  PubMed  Google Scholar 

  4. Schwarzenbach H, Hoon DSB, Pantel K. Nat Rev Cancer, 2011, 11: 426–437

    Article  CAS  PubMed  Google Scholar 

  5. Jahr S, Hentze H, Englisch S, Hardt D, Fackelmayer FO, Hesch RD, Knippers R. Cancer Res, 2001, 61: 1659–1665

    CAS  PubMed  Google Scholar 

  6. Tsui NB, Ng EK, Lo YD. Clin Chem, 2002, 48: 1647–1653

    Article  CAS  PubMed  Google Scholar 

  7. Fleischhacker M, Schmidt B. Biochim Biophys Acta Rev Cancer, 2007, 1775: 181–232

    Article  CAS  Google Scholar 

  8. Zaporozhchenko IA, Ponomaryova AA, Rykova EY, Laktionov PP. Expert Rev Mol Diagnostics, 2018, 18: 133–145

    Article  CAS  Google Scholar 

  9. Abbosh C, Birkbak NJ, Wilson GA, Jamal-Hanjani M, Constantin T, Salari R, Le Quesne J, Moore DA, Veeriah S, Rosenthal R, Marafioti T, Kirkizlar E, Watkins TBK, McGranahan N, Ward S, Martinson L, Riley J, Fraioli F, Al Bakir M, Grönroos E, Zambrana F, Endozo R, Bi WL, Fennessy FM, Sponer N, Johnson D, Laycock J, Shafi S, Czyzewska-Khan J, Rowan A, Chambers T, Matthews N, Turajlic S, Hiley C, Lee SM, Forster MD, Ahmad T, Falzon M, Borg E, Lawrence D, Hayward M, Kolvekar S, Panagiotopoulos N, Janes SM, Thakrar R, Ahmed A, Blackhall F, Summers Y, Hafez D, Naik A, Ganguly A, Kareht S, Shah R, Joseph L, Marie Quinn A, Crosbie PA, Naidu B, Middleton G, Langman G, Trotter S, Nicolson M, Remmen H, Kerr K, Chetty M, Gomersall L, Fennell DA, Nakas A, Rathinam S, Anand G, Khan S, Russell P, Ezhil V, Ismail B, Irvin-Sellers M, Prakash V, Lester JF, Kornaszewska M, Attanoos R, Adams H, Davies H, Oukrif D, Akarca AU, Hartley JA, Lowe HL, Lock S, Iles N, Bell H, Ngai Y, Elgar G, Szallasi Z, Schwarz RF, Herrero J, Stewart A, Quezada SA, Peggs KS, Van Loo P, Dive C, Lin CJ, Rabinowitz M, Aerts HJWL, Hackshaw A, Shaw JA, Zimmermann BG, Swanton C. Nature, 2017, 545: 446–451

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  10. Sadeh R, Sharkia I, Fialkoff G, Rahat A, Gutin J, Chappleboim A, Nitzan M, Fox-Fisher I, Neiman D, Meler G, Kamari Z, Yaish D, Peretz T, Hubert A, Cohen JE, Salah A, Temper M, Grinshpun A, Maoz M, Abu-Gazala S, Ben Ya’acov A, Shteyer E, Safadi R, Kaplan T, Shemer R, Planer D, Galun E, Glaser B, Zick A, Dor Y, Friedman N. Nat Biotechnol, 2021, 39: 586–598

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  11. Ulz P, Thallinger GG, Auer M, Graf R, Kashofer K, Jahn SW, Abete L, Pristauz G, Petru E, Geigl JB, Heitzer E, Speicher MR. Nat Genet, 2016, 48: 1273–1278

    Article  CAS  PubMed  Google Scholar 

  12. Liu MC, Oxnard GR, Klein EA, Swanton C, Seiden MV, Liu MC, Oxnard GR, Klein EA, Smith D, Richards D, Yeatman TJ, Cohn AL, Lapham R, Clement J, Parker AS, Tummala MK, McIntyre K, Sekeres MA, Bryce AH, Siegel R, Wang X, Cosgrove DP, Abu-Rustum NR, Trent J, Thiel DD, Becerra C, Agrawal M, Garbo LE, Giguere JK, Michels RM, Harris RP, Richey SL, McCarthy TA, Waterhouse DM, Couch FJ, Wilks ST, Krie AK, Balaraman R, Restrepo A, Meshad MW, Rieger-Christ K, Sullivan T, Lee CM, Greenwald DR, Oh W, Tsao CK, Fleshner N, Kennecke HF, Khalil MF, Spigel DR, Manhas AP, Ulrich BK, Kovoor PA, Stokoe C, Courtright JG, Yimer HA, Larson TG, Swanton C, Seiden MV, Cummings SR, Absalan F, Alexander G, Allen B, Amini H, Aravanis AM, Bagaria S, Bazargan L, Beausang JF, Berman J, Betts C, Blocker A, Bredno J, Calef R, Cann G, Carter J, Chang C, Chawla H, Chen X, Chien TC, Civello D, Davydov K, Demas V, Desai M, Dong Z, Fayzullina S, Fields AP, Filippova D, Freese P, Fung ET, Gnerre S, Gross S, Halks-Miller M, Hall MP, Hartman AR, Hou C, Hubbell E, Hunkapiller N, Jagadeesh K, Jamshidi A, Jiang R, Jung B, Kim TH, Klausner RD, Kurtzman KN, Lee M, Lin W, Lipson J, Liu H, Liu Q, Lopatin M, Maddala T, Maher MC, Melton C, Mich A, Nautiyal S, Newman J, Newman J, Nicula V, Nicolaou C, Nikolic O, Pan W, Patel S, Prins SA, Rava R, Ronaghi N, Sakarya O, Satya RV, Schellenberger J, Scott E, Sehnert AJ, Shaknovich R, Shanmugam A, Shashidhar KC, Shen L, Shenoy A, Shojaee S, Singh P, Steffen KK, Tang S, Toung JM, Valouev A, Venn O, Williams RT, Wu T, Xu HH, Yakym C, Yang X, Yecies J, Yip AS, Youngren J, Yue J, Zhang J, Zhang L, Zhang LQ, Zhang N, Curtis C, Berry DA. Ann Oncol, 2020, 31: 745–759

    Article  CAS  PubMed  Google Scholar 

  13. Cristiano S, Leal A, Phallen J, Fiksel J, Adleff V, Bruhm DC, Jensen SØ, Medina JE, Hruban C, White JR, Palsgrove DN, Niknafs N, Anagnostou V, Forde P, Naidoo J, Marrone K, Brahmer J, Woodward BD, Husain H, van Rooijen KL, Ørntoft MBW, Madsen AH, van de Velde CJH, Verheij M, Cats A, Punt CJA, Vink GR, van Grieken NCT, Koopman M, Fijneman RJA, Johansen JS, Nielsen HJ, Meijer GA, Andersen CL, Scharpf RB, Velculescu VE. Nature, 2019, 570: 385–389

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  14. Wan JCM, Massie C, Garcia-Corbacho J, Mouliere F, Brenton JD, Caldas C, Pacey S, Baird R, Rosenfeld N. Nat Rev Cancer, 2017, 17: 223–238

    Article  CAS  PubMed  Google Scholar 

  15. Schwarzenbach H, Nishida N, Calin GA, Pantel K. Nat Rev Clin Oncol, 2014, 11: 145–156

    Article  CAS  PubMed  Google Scholar 

  16. Zhang Y, Yao Y, Xu Y, Li L, Gong Y, Zhang K, Zhang M, Guan Y, Chang L, Xia X, Li L, Jia S, Zeng Q. Nat Commun, 2021, 12: 1048

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  17. Chen X, Gole J, Gore A, He Q, Lu M, Min J, Yuan Z, Yang X, Jiang Y, Zhang T, Suo C, Li X, Cheng L, Zhang Z, Niu H, Li Z, Xie Z, Shi H, Zhang X, Fan M, Wang X, Yang Y, Dang J, McConnell C, Zhang J, Wang J, Yu S, Ye W, Gao Y, Zhang K, Liu R, Jin L. Nat Commun, 2020, 11: 3475

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  18. McDonald BR, Contente-Cuomo T, Sammut SJ, Odenheimer-Bergman A, Ernst B, Perdigones N, Chin SF, Farooq M, Mejia R, Cronin PA, Anderson KS, Kosiorek HE, Northfelt DW, McCullough AE, Patel BK, Weitzel JN, Slavin TP, Caldas C, Pockaj BA, Murtaza M. Sci Transl Med, 2019, 11: eaax7392

    Article  PubMed  PubMed Central  Google Scholar 

  19. Bratman SV, Yang SYC, Iafolla MAJ, Liu Z, Hansen AR, Bedard PL, Lheureux S, Spreafico A, Razak AA, Shchegrova S, Louie M, Billings P, Zimmermann B, Sethi H, Aleshin A, Torti D, Marsh K, Eagles J, Cirlan I, Hanna Y, Clouthier DL, Lien SC, Ohashi PS, Xu W, Siu LL, Pugh TJ. Nat Cancer, 2020, 1: 873–881

    Article  CAS  PubMed  Google Scholar 

  20. Leal A, van Grieken NCT, Palsgrove DN, Phallen J, Medina JE, Hruban C, Broeckaert MAM, Anagnostou V, Adleff V, Bruhm DC, Canzoniero JV, Fiksel J, Nordsmark M, Warmerdam FARM, Verheul HMW, van Spronsen DJ, Beerepoot LV, Geenen MM, Portielje JEA, Jansen EPM, van Sandick J, Meershoek-Klein Kranenbarg E, van Laarhoven HWM, van der Peet DL, van de Velde CJH, Verheij M, Fijneman R, Scharpf RB, Meijer GA, Cats A, Velculescu VE. Nat Commun, 2020, 11: 525

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  21. Yeh YM, Lin PC, Lee CT, Chen SH, Lin BW, Lin SC, Chen PC, Chan RH, Shen MR. Mol Cancer, 2020, 19: 150

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  22. Wan JCM, Heider K, Gale D, Murphy S, Fisher E, Mouliere F, Ruiz-Valdepenas A, Santonja A, Morris J, Chandrananda D, Marshall A, Gill AB, Chan PY, Barker E, Young G, Cooper WN, Hudecova I, Marass F, Mair R, Brindle KM, Stewart GD, Abraham JE, Caldas C, Rassl DM, Rintoul RC, Alifrangis C, Middleton MR, Gallagher FA, Parkinson C, Durrani A, McDermott U, Smith CG, Massie C, Corrie PG, Rosenfeld N. Sci Transl Med, 2020, 12: eaaz8084

    Article  CAS  PubMed  Google Scholar 

  23. Kingston B, Cutts RJ, Bye H, Beaney M, Walsh-Crestani G, Hrebien S, Swift C, Kilburn LS, Kernaghan S, Moretti L, Wilkinson K, Wardley AM, Macpherson IR, Baird RD, Roylance R, Reis-Filho JS, Hubank M, Faull I, Banks KC, Lanman RB, Garcia-Murillas I, Bliss JM, Ring A, Turner NC. Nat Commun, 2021, 12: 4479

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  24. Martignano F, Munagala U, Crucitta S, Mingrino A, Semeraro R, Del Re M, Petrini I, Magi A, Conticello SG. Mol Cancer, 2021, 20: 32

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  25. Shen SY, Burgener JM, Bratman SV, De Carvalho DD. Nat Protoc, 2019, 14: 2749–2780

    Article  CAS  PubMed  Google Scholar 

  26. Kurtz DM, Soo J, Co Ting Keh L, Alig S, Chabon JJ, Sworder BJ, Schultz A, Jin MC, Scherer F, Garofalo A, Macaulay CW, Hamilton EG, Chen B, Olsen M, Schroers-Martin JG, Craig AFM, Moding EJ, Esfahani MS, Liu CL, Dührsen U, Hüttmann A, Casasnovas RO, Westin JR, Roschewski M, Wilson WH, Gaidano G, Rossi D, Diehn M, Alizadeh AA. Nat Biotechnol, 2021, 39: 1537–1547

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  27. De Vlaminck I, Valantine HA, Snyder TM, Strehl C, Cohen G, Luikart H, Neff NF, Okamoto J, Bernstein D, Weisshaar D, Quake SR, Khush KK. Sci Transl Med, 2014, 6: 241ra277

    Article  Google Scholar 

  28. Blauwkamp TA, Thair S, Rosen MJ, Blair L, Lindner MS, Vilfan ID, Kawli T, Christians FC, Venkatasubrahmanyam S, Wall GD, Cheung A, Rogers ZN, Meshulam-Simon G, Huijse L, Balakrishnan S, Quinn JV, Hollemon D, Hong DK, Vaughn ML, Kertesz M, Bercovici S, Wilber JC, Yang S. Nat Microbiol, 2019, 4: 663–674

    Article  CAS  PubMed  Google Scholar 

  29. Caggiano C, Celona B, Garton F, Mefford J, Black BL, Henderson R, Lomen-Hoerth C, Dahl A, Zaitlen N. Nat Commun, 2021, 12: 2717

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  30. Fedyuk V, Erez N, Furth N, Beresh O, Andreishcheva E, Shinde A, Jones D, Zakai BB, Mavor Y, Peretz T, Hubert A, Cohen JE, Salah A, Temper M, Grinshpun A, Maoz M, Zick A, Ron G, Shema E. Nat Biotechnol, 2023, 41: 212–221

    Article  CAS  PubMed  Google Scholar 

  31. Wang P, Song Q, Ren J, Zhang W, Wang Y, Zhou L, Wang D, Chen K, Jiang L, Zhang B, Chen W, Qu C, Zhao H, Jiao Y. Sci Transl Med, 2022, 14: abp8704

    Article  Google Scholar 

  32. Guler GD, Ning Y, Ku CJ, Phillips T, McCarthy E, Ellison CK, Bergamaschi A, Collin F, Lloyd P, Scott A, Antoine M, Wang W, Chau K, Ashworth A, Quake SR, Levy S. Nat Commun, 2020, 11: 5270

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  33. Lo YMD, Han DSC, Jiang P, Chiu RWK. Science, 2021, 372: eaaw3616

    Article  CAS  PubMed  Google Scholar 

  34. Yu SCY, Jiang P, Peng W, Cheng SH, Cheung YTT, Tse OYO, Shang H, Poon LC, Leung TY, Chan KCA, Chiu RWK, Lo YMD. Proc Natl Acad Sci USA, 2021, 118: e2114937118

    Article  PubMed  PubMed Central  Google Scholar 

  35. Sin STK, Jiang P, Deng J, Ji L, Cheng SH, Dutta A, Leung TY, Chan KCA, Chiu RWK, Lo YMD. Proc Natl Acad Sci USA, 2020, 117: 1658–1665

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  36. Larson MH, Pan W, Kim HJ, Mauntz RE, Stuart SM, Pimentel M, Zhou Y, Knudsgaard P, Demas V, Aravanis AM, Jamshidi A. Nat Commun, 2021, 12: 2357

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  37. Ibarra A, Zhuang J, Zhao Y, Salathia NS, Huang V, Acosta AD, Aballi J, Toden S, Karns AP, Purnajo I, Parks JR, Guo L, Mason J, Sigal D, Nova TS, Quake SR, Nerenberg M. Nat Commun, 2020, 11: 400

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  38. Ngo TTM, Moufarrej MN, Rasmussen MLH, Camunas-Soler J, Pan W, Okamoto J, Neff NF, Liu K, Wong RJ, Downes K, Tibshirani R, Shaw GM, Skotte L, Stevenson DK, Biggio JR, Elovitz MA, Melbye M, Quake SR. Science, 2018, 360: 1133–1136

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  39. Rasmussen M, Reddy M, Nolan R, Camunas-Soler J, Khodursky A, Scheller NM, Cantonwine DE, Engelbrechtsen L, Mi JD, Dutta A, Brundage T, Siddiqui F, Thao M, Gee EPS, La J, Baruch-Gravett C, Santillan MK, Deb S, Ame SM, Ali SM, Adkins M, DePristo MA, Lee M, Namsaraev E, Gybel-Brask DJ, Skibsted L, Litch JA, Santillan DA, Sazawal S, Tribe RM, Roberts JM, Jain M, Høgdall E, Holzman C, Quake SR, Elovitz MA, McElrath TF. Nature, 2022, 601: 422–427

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  40. Toden S, Zhuang J, Acosta AD, Karns AP, Salathia NS, Brewer JB, Wilcock DM, Aballi J, Nerenberg M, Quake SR, Ibarra A. Sci Adv, 2020, 6: eabb1654

    Article  PubMed  PubMed Central  Google Scholar 

  41. Miyoshi J, Zhu Z, Luo A, Toden S, Zhou X, Izumi D, Kanda M, Takayama T, Parker IM, Wang M, Gao F, Zaidi AH, Baba H, Kodera Y, Cui Y, Wang X, Liu Z, Goel A. Mol Cancer, 2022, 21: 44

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  42. Rose Brannon A, Jayakumaran G, Diosdado M, Patel J, Razumova A, Hu Y, Meng F, Haque M, Sadowska J, Murphy BJ, Baldi T, Johnson I, Ptashkin R, Hasan M, Srinivasan P, Rema AB, Rijo I, Agarunov A, Won H, Perera D, Brown DN, Samoila A, Jing X, Gedvilaite E, Yang JL, Stephens DP, Dix JM, DeGroat N, Nafa K, Syed A, Li A, Lebow ES, Bowman AS, Ferguson DC, Liu Y, Mata DA, Sharma R, Yang SR, Bale T, Benhamida JK, Chang JC, Dogan S, Hameed MR, Hechtman JF, Moung C, Ross DS, Vakiani E, Vanderbilt CM, Yao JJ, Razavi P, Smyth LM, Chandarlapaty S, Iyer G, Abida W, Harding JJ, Krantz B, O’Reilly E, Yu HA, Li BT, Rudin CM, Diaz L, Solit DB, Arcila ME, Ladanyi M, Loomis B, Tsui D, Berger MF, Zehir A, Benayed R. Nat Commun, 2021, 12: 3770

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  43. Vandekerkhove G, Lavoie JM, Annala M, Murtha AJ, Sundahl N, Walz S, Sano T, Taavitsainen S, Ritch E, Fazli L, Hurtado-Coll A, Wang G, Nykter M, Black PC, Todenhöfer T, Ost P, Gibb EA, Chi KN, Eigl BJ, Wyatt AW. Nat Commun, 2021, 12: 184

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  44. Vermeirssen V, Deleu J, Morlion A, Everaert C, De Wilde J, Anckaert J, Durinck K, Nuytens J, Rishfi M, Speleman F, Van Droogenbroeck H, Verniers K, Baietti MF, Albersen M, Leucci E, Post E, Best MG, Van Maerken T, De Wilde B, Vandesompele J, Decock A. NAR Cancer, 2022, 4: zcac037

    Article  PubMed  PubMed Central  Google Scholar 

  45. Oshi M, Murthy V, Takahashi H, Huyser M, Okano M, Tokumaru Y, Rashid OM, Matsuyama R, Endo I, Takabe K. Cancers, 2021, 13: 2652

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  46. Bulterys MA, Wagner B, Redard-Jacot M, Suresh A, Pollock NR, Moreau E, Denkinger CM, Drain PK, Broger T. J Clin Med, 2019, 9: 111

    Article  PubMed  PubMed Central  Google Scholar 

  47. Yeasmin S, Ammanath G, Onder A, Yan E, Yildiz UH, Palaniappan A, Liedberg B. TrAC Trends Anal Chem, 2022, 157: 116786

    Article  CAS  Google Scholar 

  48. Palmer BF, Clegg DJ. Clin J Am Soc Nephrol, 2019, 14: 306–316

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  49. Salfer B, Li F, Wong DTW, Zhang L. Clin Chem, 2022, 68: 1493–1501

    Article  PubMed  PubMed Central  Google Scholar 

  50. Bryzgunova OE, Laktionov PP. Acta Naturae, 2015, 7: 48–54

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  51. Oreskovic A, Brault ND, Panpradist N, Lai JJ, Lutz BR. J Mol Diagnostics, 2019, 21: 1067–1078

    Article  CAS  Google Scholar 

  52. Greytak SR, Engel KB, Parpart-Li S, Murtaza M, Bronkhorst AJ, Pertile MD, Moore HM. Clin Cancer Res, 2020, 26: 3104–3109

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  53. Johansson G, Andersson D, Filges S, Li J, Muth A, Godfrey TE, Ståhlberg A. Biomol Detection Quantif, 2019, 17: 100078

    Article  CAS  Google Scholar 

  54. Werner B, Warton K, Ford CE. Cancers, 2022, 14: 1309

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  55. Botezatu I, Serdyuk O’, Potapova G, Shelepov V, Alechina R, Molyaka Y, Anan’ev V, Bazin I, Garin A, Narimanov M, Knysh V, Melkonyan H, Umansky S, Lichtenstein A. Clin Chem, 2000, 46: 1078–1084

    Article  CAS  PubMed  Google Scholar 

  56. Kopreski MS, Benko FA, Kwak LW, Gocke CD. Clin Cancer Res, 1999, 5: 1961–1965

    CAS  PubMed  Google Scholar 

  57. Chen XQ, Bonnefoi H, Pelte MF, Lyautey J, Lederrey C, Movarekhi S, Schaeffer P, Mulcahy HE, Meyer P, Stroun M, Anker P. Clin Cancer Res, 2000, 6: 3823–3826

    CAS  PubMed  Google Scholar 

  58. Takahashi H, Yasui T, Baba Y. Chem Lett, 2021, 50: 1244–1253

    Article  CAS  Google Scholar 

  59. van der Vaart M, Pretorius PJ. Ann New York Acad Sci, 2008, 1137: 18–26

    Article  CAS  Google Scholar 

  60. Vo JN, Cieslik M, Zhang Y, Shukla S, Xiao L, Zhang Y, Wu YM, Dhanasekaran SM, Engelke CG, Cao X, Robinson DR, Nesvizhskii AI, Chinnaiyan AM. Cell, 2019, 176: 869–881.e13

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  61. Fleischhacker M. Int J Mol Sci, 2016, 1–4

  62. Giri B, Seamon M, Banerjee A, Chauhan S, Purohit S, Morgan J, Baban B, Wakade C. Metab Brain Dis, 2022, 37: 1687–1696

    Article  CAS  PubMed  Google Scholar 

  63. Shekhtman EM, Anne K, Melkonyan HS, Robbins DJ, Warsof SL, Umansky SR. Clin Chem, 2009, 55: 723–729

    Article  CAS  PubMed  Google Scholar 

  64. Kim WT, Kim YH, Jeong P, Seo SP, Kang HW, Kim YJ, Yun SJ, Lee SC, Moon SK, Choi YH, Lee GT, Kim IY, Kim WJ. Oncotarget, 2018, 9: 14354–14365

    Article  PubMed  PubMed Central  Google Scholar 

  65. Urquidi V, Netherton M, Gomes-Giacoia E, Serie D, Eckel-Passow J, Rosser CJ, Goodison S. Oncotarget, 2016, 7: 38731–38740

    Article  PubMed  PubMed Central  Google Scholar 

  66. Piao XM, Jeong P, Kim YH, Byun YJ, Xu Y, Kang HW, Ha YS, Kim WT, Lee JY, Woo SH, Kwon TG, Kim IY, Moon SK, Choi YH, Cha EJ, Yun SJ, Kim WJ. Int J Cancer, 2019, 144: 380–388

    Article  CAS  PubMed  Google Scholar 

  67. Guo J, Yang J, Zhang X, Feng X, Zhang H, Chen L, Johnson H, Persson JL, Xiao K. Anticancer Res, 2018, 38: 1471–1477

    CAS  PubMed  Google Scholar 

  68. Woo HK, Park J, Ku JY, Lee CH, Sunkara V, Ha HK, Cho YK. Lab Chip, 2019, 19: 87–97

    Article  CAS  Google Scholar 

  69. Ngamdee T, Chalermwatanachai T, Siriwan C, Warachit O, Rijiravanich P, Surareungchai W. Anal Bioanal Chem, 2022, 414: 5695–5707

    Article  CAS  PubMed  Google Scholar 

  70. Saha S, Araf Y, Promon SK. J Egypt Natl Canc Inst, 2022, 34: 8

    Article  PubMed  Google Scholar 

  71. Zmrzljak UP, Košir R, Krivokapic Z, Radojković D, Nikolić A. Genes, 2021, 12: 289

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  72. Ståhlberg A, Krzyzanowski PM, Jackson JB, Egyud M, Stein L, Godfrey TE. Nucleic Acids Res, 2016, 44: e105

    Article  PubMed  PubMed Central  Google Scholar 

  73. Ståhlberg A, Krzyzanowski PM, Egyud M, Filges S, Stein L, Godfrey TE. Nat Protoc, 2017, 12: 664–682

    Article  PubMed  Google Scholar 

  74. Lei R, Huo R, Mohan C. Expert Rev Mol Diagnostics, 2020, 20: 69–84

    Article  CAS  Google Scholar 

  75. Jordaens S, Zwaenepoel K, Tjalma W, Deben C, Beyers K, Vankerckhoven V, Pauwels P, Vorsters A. Intl J Cancer, 2023, 152: 2186–2205

    Article  CAS  Google Scholar 

  76. Bryzgunova OE, Skvortsova TE, Kolesnikova EV, Starikov AV, Rykova EY, Vlassov VV, Laktionov PP. Ann New York Acad Sci, 2006, 1075: 334–340

    Article  CAS  Google Scholar 

  77. Chen C, Lu C, Qian Y, Li H, Tan Y, Cai L, Weng H. Sci Rep, 2017, 7: 17737

    Article  PubMed  PubMed Central  Google Scholar 

  78. Sidransky D, Von Eschenbach A, Tsai Y, Jones P, Summerhayes I, Marshall F, Paul M, Green P, Hamilton P, Frost P, et A. Science, 1991, 252: 706–709

    Article  CAS  PubMed  Google Scholar 

  79. Hessels D, Klein Gunnewiek JMT, van Oort I, Karthaus HFM, van Leenders GJL, van Balken B, Kiemeney LA, Witjes JA, Schalken JA. Eur Urol, 2003, 44: 8–16

    Article  CAS  PubMed  Google Scholar 

  80. Groskopf J, Aubin SM, Deras IL, Blase A, Bodrug S, Clark C, Brentano S, Mathis J, Pham J, Meyer T, Cass M, Hodge P, Macairan ML, Marks LS, Rittenhouse H. Clin Chem, 2006, 52: 1089–1095

    Article  CAS  PubMed  Google Scholar 

  81. Lin SY, Dhillon V, Jain S, Chang TT, Hu CT, Lin YJ, Chen SH, Chang KC, Song W, Yu L, Block TM, Su YH. J Mol Diagn, 2011, 13: 474–484

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  82. Su YH, Wang M, Brenner DE, Norton PA, Block TM. Ann New York Acad Sci, 2008, 1137: 197–206

    Article  CAS  Google Scholar 

  83. Chen S, Zhao J, Cui L, Liu Y. Clin Transl Oncol, 2017, 19: 332–340

    Article  CAS  PubMed  Google Scholar 

  84. Zhang J, Zhang X, Shen S. Future Oncol, 2020, 16: 849–858

    Article  CAS  PubMed  Google Scholar 

  85. Nuzzo PV, Berchuck JE, Korthauer K, Spisak S, Nassar AH, Abou Alaiwi S, Chakravarthy A, Shen SY, Bakouny Z, Boccardo F, Steinharter J, Bouchard G, Curran CR, Pan W, Baca SC, Seo JH, Lee GSM, Michaelson MD, Chang SL, Waikar SS, Sonpavde G, Irizarry RA, Pomerantz M, De Carvalho DD, Choueiri TK, Freedman ML. Nat Med, 2020, 26: 1041–1043

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  86. Bach S, Paulis I, Sluiter NR, Tibbesma M, Martin I, van de Wiel MA, Tuynman JB, Bahce I, Kazemier G, Steenbergen RDM. Sci Rep, 2021, 11: 2363

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  87. Zhou Z, Cheng SH, Ding SC, Heung MMS, Xie T, Cheng THT, Lam WKJ, Peng W, Teoh JYC, Chiu PKF, Ng CF, Jiang P, Chan KCA, Chiu RWK, Lo YMD. Clin Chem, 2021, 67: 621–630

    Article  PubMed  Google Scholar 

  88. Kim WT, Jeong P, Yan C, Kim YH, Lee IS, Kang HW, Kim YJ, Lee SC, Kim SJ, Kim YT, Moon SK, Choi YH, Kim IY, Yun SJ, Kim WJ. Oncotarget, 2016, 7: 58193–58202

    Article  PubMed  PubMed Central  Google Scholar 

  89. Bartel DP. Cell, 2004, 116: 281–297

    Article  CAS  PubMed  Google Scholar 

  90. Mall C, Rocke DM, Durbin-Johnson B, Weiss RH. Biomarkers Med, 2013, 7: 623–631

    Article  CAS  Google Scholar 

  91. Hung PS, Chen CY, Chen WT, Kuo CY, Lo SS. PLoS One, 2017, 12: e0177346

    Article  PubMed  PubMed Central  Google Scholar 

  92. Kapranov P, Cheng J, Dike S, Nix DA, Duttagupta R, Willingham AT, Stadler PF, Hertel J, Hackermuller J, Hofacker IL, Bell I, Cheung E, Drenkow J, Dumais E, Patel S, Helt G, Ganesh M, Ghosh S, Piccolboni A, Sementchenko V, Tammana H, Gingeras TR. Science, 2007, 316: 1484–1488

    Article  CAS  PubMed  Google Scholar 

  93. Iyer MK, Niknafs YS, Malik R, Singhal U, Sahu A, Hosono Y, Barrette TR, Prensner JR, Evans JR, Zhao S, Poliakov A, Cao X, Dhanasekaran SM, Wu YM, Robinson DR, Beer DG, Feng FY, Iyer HK, Chinnaiyan AM. Nat Genet, 2015, 47: 199–208

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  94. Bussemakers MJG, van Bokhoven A, Verhaegh GW, Smit FP, Karthaus HF, Schalken JA, Debruyne FM, Ru N, Isaacs WB. Cancer Res, 1999, 59: 5975–5979

    CAS  PubMed  Google Scholar 

  95. Hansen TB, Jensen TI, Clausen BH, Bramsen JB, Finsen B, Damgaard CK, Kjems J. Nature, 2013, 495: 384–388

    Article  CAS  PubMed  Google Scholar 

  96. Guarnerio J, Bezzi M, Jeong JC, Paffenholz SV, Berry K, Naldini MM, Lo-Coco F, Tay Y, Beck AH, Pandolfi PP. Cell, 2016, 165: 289–302

    Article  CAS  PubMed  Google Scholar 

  97. Zhang S, Zeng X, Ding T, Guo L, Li Y, Ou S, Yuan H. Sci Rep, 2018, 8: 2878

    Article  PubMed  PubMed Central  Google Scholar 

  98. Kristiansen TZ, Maitra A, Pandey A. Proteomics of human bile. In: Proteomics of Human Body Fluids. Totowa: Humana Press, 2007. 399–414

    Chapter  Google Scholar 

  99. Housset C, Chrétien Y, Debray D, Chignard N. Compr Physiol, 2016, 6: 1549–1577

    Article  PubMed  Google Scholar 

  100. Farina A, Dumonceau JM, Lescuyer P. Expert Rev Proteomics, 2009, 6: 285–301

    Article  CAS  PubMed  Google Scholar 

  101. Esteller A. World J Gastroenterol, 2008, 14: 5641–5649

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  102. Driescher C, Fuchs K, Haeberle L, Goering W, Frohn L, Opitz FV, Haeussinger D, Knoefel WT, Keitel V, Esposito I. Cancers, 2020, 13: 39

    Article  PubMed  PubMed Central  Google Scholar 

  103. Li Z, Liu Y, Fu J, Mugaanyi J, Yan J, Lu C, Huang J. Front Oncol, 2022, 12: 961939

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  104. Han JY, Ahn KS, Kim TS, Kim YH, Cho KB, Shin DW, Baek WK, Suh SI, Jang BC, Kang KJ. Cancers, 2021, 13: 4581

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  105. Kinugasa H, Nouso K, Ako S, Dohi C, Matsushita H, Matsumoto K, Kato H, Okada H. Cancer Biol Ther, 2018, 19: 934–938

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  106. Shen N, Zhu B, Zhang W, Nian B, Xu X, Yu L, Ruan X, Chen S, Liu Y, Cao X, Shi X, Li Z, Huang X, Wang X, Chen C, Xiong L, Zhang D, Fu X, Zhang Y. Front Oncol, 2022, 12: 891917

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  107. Shen N, Zhang D, Yin L, Qiu Y, Liu J, Yu W, Fu X, Zhu B, Xu X, Duan A, Chen Z, Wang X, Cao X, Zhao T, Zhou Z, Yu L, Qin H, Fang Z, Li J, Liu Y, Xiong L, Yuan B, Li F, Zhang Y. Oncol Rep, 2019, doi: https://doi.org/10.3892/or.2019.7177

  108. Arechederra M, Rullán M, Amat I, Oyon D, Zabalza L, Elizalde M, Latasa MU, Mercado MR, Ruiz-Clavijo D, Saldaña C, Fernández-Urién I, Carrascosa J, Jusué V, Guerrero-Setas D, Zazpe C, González-Borja I, Sangro B, Herranz JM, Purroy A, Gil I, Nelson LJ, Vila JJ, Krawczyk M, Zieniewicz K, Patkowski W, Milkiewicz P, Cubero FJ, Alkorta-Aranburu G, G Fernandez-Barrena M, Urman JM, Berasain C, Avila MA. Gut, 2022, 71: 1141–1151

    Article  CAS  PubMed  Google Scholar 

  109. Roest HP, IJzermans JNM, van der Laan LJW. BMC Biotechnol, 2021, 21: 48

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  110. Valle JW, Kelley RK, Nervi B, Oh DY, Zhu AX. Lancet, 2021, 397: 428–444

    Article  CAS  PubMed  Google Scholar 

  111. Banales JM, Cardinale V, Carpino G, Marzioni M, Andersen JB, Invernizzi P, Lind GE, Folseraas T, Forbes SJ, Fouassier L, Geier A, Calvisi DF, Mertens JC, Trauner M, Benedetti A, Maroni L, Vaquero J, Macias RIR, Raggi C, Perugorria MJ, Gaudio E, Boberg KM, Marin JJG, Alvaro D. Nat Rev Gastroenterol Hepatol, 2016, 13: 261–280

    Article  PubMed  Google Scholar 

  112. Wang YF, Feng FL, Zhao XH, Ye ZX, Zeng HP, Li Z, Jiang XQ, Peng ZH. World J Gastroenterol, 2014, 20: 4085–4092

    Article  PubMed  PubMed Central  Google Scholar 

  113. Gou Q, Zhang CZ, Sun ZH, Wu LG, Chen Y, Mo ZQ, Mai QC, He J, Zhou ZX, Shi F, Cui W, Zou W, Lv L, Zhuang WH, Xu RD, Li WK, Zhang J, Du HW, Xiang JX, Wang HZ, Hou T, Li ST, Li Y, Chen XM, Zhou ZJ. ESMO Open, 2021, 6: 100275

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  114. Klump B, Hsieh CJ, Dette S, Holzmann K, Kieβlich R, Jung M, Sinn U, Ortner M, Porschen R, Gregor M. Clin Cancer Res, 2003, 9: 1773–1778

    CAS  PubMed  Google Scholar 

  115. Shin SH, Lee K, Kim BH, Cho NY, Jang JY, Kim YT, Kim D, Jang JJ, Kang GH. J Mol Diagn, 2012, 14: 256–263

    Article  CAS  PubMed  Google Scholar 

  116. Vedeld HM, Grimsrud MM, Andresen K, Pharo HD, von Seth E, Karlsen TH, Honne H, Paulsen V, Färkkilä MA, Bergquist A, Jeanmougin M, Aabakken L, Boberg KM, Folseraas T, Lind GE. Hepatology, 2022, 75: 59–73

    Article  CAS  PubMed  Google Scholar 

  117. He S, Zeng F, Yin H, Wang P, Bai Y, Song Q, Chu J, Huang Z, Liu Y, Liu H, Chen Q, Liu L, Zhou J, Hu H, Li X, Li T, Wang G, Cai J, Jiao Y, Zhao H. eClinicalMedicine, 2023, 55: 101736

    Article  PubMed  Google Scholar 

  118. Shigehara K, Yokomuro S, Ishibashi O, Mizuguchi Y, Arima Y, Kawahigashi Y, Kanda T, Akagi I, Tajiri T, Yoshida H. PLoS One, 2011, 6: e23584

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  119. Macias RIR, Banales JM, Sangro B, Muntané J, Avila MA, Lozano E, Perugorria MJ, Padillo FJ, Bujanda L, Marin JJG. Biochim Biophys Acta Mol Basis Dis, 2018, 1864: 1468–1477

    Article  CAS  PubMed  Google Scholar 

  120. Voigtlander T, Gupta SK, Thum S, Fendrich J, Manns MP, Lankisch TO, Thum T. PLoS One, 2015, 10: e0139305

    Article  PubMed  PubMed Central  Google Scholar 

  121. Han HS, Kim MJ, Han JH, Yun J, Kim HK, Yang Y, Kim KB, Park SM. Hepatob Pancreat Dis Int, 2020, 19: 41–50

    Article  CAS  Google Scholar 

  122. Yoshida M, Yukawa H, Hayashi K, Naitoh I, Miyabe K, Hori Y, Natsume M, Jinno N, Kato A, Kachi K, Asano G, Sahashi H, Toyohara T, Kuno K, Kito Y, Kondo H, Hirano A, Okumura F, Anbe K, Baba Y, Kataoka H, Tanaka Y. Cancer Sci, 2023, 114: 295–305

    Article  CAS  PubMed  Google Scholar 

  123. Uchida N, Tsutsui K, Kobara H, Ezaki T, Fukuma H, Yachida M, Masaki T, Watanabe S, Nakatsu T, Nakano H, Kuriyama S. Endoscopy, 2003, 35: 185–188

    Article  CAS  PubMed  Google Scholar 

  124. Nagai K, Kuwatani M, Hirata K, Suda G, Hirata H, Takishin Y, Furukawa R, Kishi K, Yonemura H, Nozawa S, Sugiura R, Kawakubo K, Sakamoto N. Diagnostics, 2022, 12: 2704

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  125. De Mattos-Arruda L, Mayor R, Ng CKY, Weigelt B, Martínez-Ricarte F, Torrejon D, Oliveira M, Arias A, Raventos C, Tang J, Guerini-Rocco E, Martínez-Sáez E, Lois S, Marín O, de la Cruz X, Piscuoglio S, Towers R, Vivancos A, Peg V, Ramon y Cajal S, Carles J, Rodon J, González-Cao M, Tabernero J, Felip E, Sahuquillo J, Berger MF, Cortes J, Reis-Filho JS, Seoane J. Nat Commun, 2015, 6: 8839

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  126. Miller AM, Shah RH, Pentsova EI, Pourmaleki M, Briggs S, Distefano N, Zheng Y, Skakodub A, Mehta SA, Campos C, Hsieh WY, Selcuklu SD, Ling L, Meng F, Jing X, Samoila A, Bale TA, Tsui DWY, Grommes C, Viale A, Souweidane MM, Tabar V, Brennan CW, Reiner AS, Rosenblum M, Panageas KS, DeAngelis LM, Young RJ, Berger MF, Mellinghoff IK. Nature, 2019, 565: 654–658

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  127. Escudero L, Llort A, Arias A, Diaz-Navarro A, Martínez-Ricarte F, Rubio-Perez C, Mayor R, Caratù G, Martínez-Sáez E, Vázquez-Méndez É, Lesende-Rodríguez I, Hladun R, Gros L, Ramón y Cajal S, Poca MA, Puente XS, Sahuquillo J, Gallego S, Seoane J. Nat Commun, 2020, 11: 5376

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  128. Brunet-Vega A, Pericay C, Quílez ME, Ramírez-Lázaro MJ, Calvet X, Lario S. Anal Biochem, 2015, 488: 28–35

    Article  CAS  PubMed  Google Scholar 

  129. Reiter JG, Baretti M, Gerold JM, Makohon-Moore AP, Daud A, Iacobuzio-Donahue CA, Azad NS, Kinzler KW, Nowak MA, Vogelstein B. Nat Rev Cancer, 2019, 19: 639–650

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  130. Ignatiadis M, Sledge GW, Jeffrey SS. Nat Rev Clin Oncol, 2021, 18: 297–312

    Article  PubMed  Google Scholar 

  131. Li W, Zhang X, Lu X, You L, Song Y, Luo Z, Zhang J, Nie J, Zheng W, Xu D, Wang Y, Dong Y, Yu S, Hong J, Shi J, Hao H, Luo F, Hua L, Wang P, Qian X, Yuan F, Wei L, Cui M, Zhang T, Liao Q, Dai M, Liu Z, Chen G, Meckel K, Adhikari S, Jia G, Bissonnette MB, Zhang X, Zhao Y, Zhang W, He C, Liu J. Cell Res, 2017, 27: 1243–1257

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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Acknowledgements

This work was supported by the National Natural Science Foundation of China (92153303, 21721005, 91940000 to X. Z), and the National Science Foundation for Young Scientists of China (21907078 to S.P.).

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  1. These authors contributed equally to this work.

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  1. College of Chemistry and Molecular Sciences, Key Laboratory of Biomedical Polymers-Ministry of Education, Department of Hematology of Zhongnan Hospital, Taikang Center for Life and Medical Sciences, Wuhan University, Wuhan, 430072, China

    Yuqing Sun, Yongling Tang, Long Yu, Yuhao Wang, Shuang Peng & Xiang Zhou

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Sun, Y., Tang, Y., Yu, L. et al. Circulating nucleic acids as liquid biopsies for disease prediction, screening and diagnosis. Sci. China Chem. 66, 3006–3023 (2023). https://doi.org/10.1007/s11426-023-1727-9

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