Multi-marker analysis of circulating cell-free DNA toward personalized medicine for colorectal cancer

Molecular Oncology

Volumn 8, Issue 5, 2014, Pages 927-941

  Mouliere, Florent ^a   El Messaoudi, Safia ^a   Pang, Dalong ^b   Dritschilo, Anatoly ^b   Thierry, Alain R ^a  

^a INSTITUT DE RECHERCHE EN CANCÉROLOGIE DE MONTPELLIER   (France)

^b GEORGETOWN UNIVERSITY   (United States)

Author keywords

Circulating cell free DNA; Colorectal cancer; Multi marker analysis; qPCR

Indexed keywords

B RAF KINASE; CIRCULATING CELL FREE DNA; DNA; UNCLASSIFIED DRUG; TUMOR MARKER; BIOLOGICAL MARKER;

ALLELE; ALLELE SPECIFIC BLOCKER QUANTITATIVE POLYMERASE CHAIN REACTION; AREA UNDER THE CURVE; ARTICLE; ATOMIC FORCE MICROSCOPY; BLOOD SAMPLING; CANCER DIAGNOSIS; CANCER PATIENT; COLORECTAL CANCER; CONTROLLED CLINICAL TRIAL; CONTROLLED STUDY; DIAGNOSTIC TEST ACCURACY STUDY; DNA DETERMINATION; DNA FRAGMENTATION; DNA INTEGRITY INDEX; GENETIC PARAMETERS; HUMAN; MAJOR CLINICAL STUDY; ONCOGENE; ONCOGENE B RAF KINASE; ONCOGENE K RAS; PERSONALIZED MEDICINE; POINT MUTATION; POLYMERASE CHAIN REACTION; POLYMERASE CHAIN REACTION SYSTEM; PRIORITY JOURNAL; QUANTITATIVE ASSAY; RECEIVER OPERATING CHARACTERISTIC; SENSITIVITY AND SPECIFICITY; BLOOD; COLON; COLORECTAL TUMOR; GENETICS; METABOLISM; PATHOLOGY; PROCEDURES; RECTUM; ULTRASTRUCTURE; VALIDATION STUDY; GENE MUTATION; HUMAN CELL;

BIOMARKERS, TUMOR; COLON; COLORECTAL NEOPLASMS; DNA FRAGMENTATION; DNA, NEOPLASM; HUMANS; MICROSCOPY, ATOMIC FORCE; POLYMERASE CHAIN REACTION; PRECISION MEDICINE; RECTUM;

EID: 84903549166     PISSN: 15747891     EISSN: 18780261     Source Type: Journal    
DOI: 10.1016/j.molonc.2014.02.005     Document Type: Article

References (48)

1. Amado R.G., Wolf M., Peeters M., Van Cutsem E., Siena S., Freeman D.J., Juan T., Sikorski R., Suggs S., Radinsky R., Patterson S.D., Chang D.D. Wild-type KRAS is required for panitumumab efficacy in patients with metastatic colorectal cancer. J. Clin. Oncol. 2008, 26(10):1626-1634. 10.1200/JCO.2007.14.7116.
2. Bamford S., Dawson E., Forbes S., Clements J., Pettett R., Dogan A., Flanagan A., Teague J., Futreal P.A., Stratton M.R., Wooster R. The COSMIC (catalogue of somatic mutations in cancer) database and website. Br. J. Cancer 2004, 91(2):355-358. DOI: 6601894, [pii] 10.1038/sj.bjc.6601894.
3. Bustin S.A., Benes V., Garson J.A., Hellemans J., Huggett J., Kubista M., Mueller R., Nolan T., Pfaffl M.W., Shipley G.L., Vandesompele J., Wittwer C.T. The MIQE guidelines: minimum information for publication of quantitative real-time PCR experiments. Clin. Chem. 2009, 55(4):611-622. [pii] 10.1373/clinchem.2008.112797, DOI: clinchem.2008.112797.
4. Chan K.C., Jiang P., Zheng Y.W., Liao G.J., Sun H., Wong J., Siu S.S., Chan W.C., Chan S.L., Chan A.T., Lai P.B., Chiu R.W., Lo Y.M. Cancer genome scanning in plasma: detection of tumor-associated copy number aberrations, single-nucleotide variants, and tumoral heterogeneity by massively parallel sequencing. Clin. Chem. 2013, 59(1):211-224. 10.1373/clinchem.2012.196014.
5. Dawson S.J., Tsui D.W., Murtaza M., Biggs H., Rueda O.M., Chin S.F., Dunning M.J., Gale D., Forshew T., Mahler-Araujo B., Rajan S., Humphray S., Becq J., Halsall D., Wallis M., Bentley D., Caldas C., Rosenfeld N. Analysis of circulating tumor DNA to monitor metastatic breast cancer. N. Engl. J. Med. 2013, 368(13):1199-1209. 10.1056/NEJMoa1213261.
6. Di Nicolantonio F., Arena S., Gallicchio M., Zecchin D., Martini M., Flonta S.E., Stella G.M., Lamba S., Cancelliere C., Russo M., Geuna M., Appendino G., Fantozzi R., Medico E., Bardelli A. Replacement of normal with mutant alleles in the genome of normal human cells unveils mutation-specific drug responses. Proc. Natl. Acad. Sci. U S A 2008, 105(52):20864-20869. DOI: 0808757105, [pii] 10.1073/pnas.0808757105.
7. Di Nicolantonio F., Martini M., Molinari F., Sartore-Bianchi A., Arena S., Saletti P., De Dosso S., Mazzucchelli L., Frattini M., Siena S., Bardelli A. Wild-type BRAF is required for response to panitumumab or cetuximab in metastatic colorectal cancer. J. Clin. Oncol. 2008, 26(35):5705-5712. DOI: JCO.2008.18.0786, [pii]10.1200/JCO.2008.18.0786.
8. Diehl F., Li M., Dressman D., He Y., Shen D., Szabo S., Diaz L.A., Goodman S.N., David K.A., Juhl H., Kinzler K.W., Vogelstein B. Detection and quantification of mutations in the plasma of patients with colorectal tumors. Proc. Natl. Acad. Sci. U S A 2005, 102(45):16368-16373. DOI: 0507904102, [pii] 10.1073/pnas.0507904102.
9. Diehl F., Schmidt K., Choti M.A., Romans K., Goodman S., Li M., Thornton K., Agrawal N., Sokoll L., Szabo S.A., Kinzler K.W., Vogelstein B., Diaz L.A. Circulating mutant DNA to assess tumor dynamics. Nat. Med. 2008, 14(9):985-990. DOI: nm.1789, [pii] 10.1038/nm.1789.
10. Diehl F., Schmidt K., Durkee K.H., Moore K.J., Goodman S.N., Shuber A.P., Kinzler K.W., Vogelstein B. Analysis of mutations in DNA isolated from plasma and stool of colorectal cancer patients. Gastroenterology 2008, 135(2):489-498. DOI: S0016-5085(08)00860-3, [pii] 10.1053/j.gastro.2008.05.039.
11. Douillard J.Y., Oliner K.S., Siena S., Tabernero J., Burkes R., Barugel M., Humblet Y., Bodoky G., Cunningham D., Jassem J., Rivera F., Kocákova I., Ruff P., Błasińska-Morawiec M., Šmakal M., Canon J.L., Rother M., Williams R., Rong A., Wiezorek J., Sidhu R., Patterson S.D. Panitumumab-FOLFOX4 treatment and RAS mutations in colorectal cancer. N. Engl. J. Med. 2013, 369(11):1023-1034. 10.1056/NEJMoa1305275.
12. El Messaoudi S., Rolet F., Mouliere F., Thierry A.R. Circulating cell free DNA: preanalytical considerations. Clin. Chim. Acta 2013, 424(11):222-230. 10.1016/j.cca.2013.05.022.
13. Ellinger J., Wittkamp V., Albers P., Perabo F.G., Mueller S.C., von Ruecker A., Bastian P.J. Cell-free circulating DNA: diagnostic value in patients with testicular germ cell cancer. J. Urol. 2009, 181(1):363-371. DOI: S0022-5347(08)02410-5, [pii] 10.1016/j.juro.2008.08.118.
14. Fleischhacker M., Schmidt B., Weickmann S., Fersching D.M., Leszinski G.S., Siegele B., Stötzer O.J., Nagel D., Holdenrieder S. Methods for isolation of cell-free plasma DNA strongly affect DNA yield. Clin. Chim. Acta 2011, 412(23-24):2085-2088. DOI: S0009-8981(11)00409-8, [pii] 10.1016/j.cca.2011.07.011.
15. Forshew T., Murtaza M., Parkinson C., Gale D., Tsui D.W., Kaper F., Dawson S.J., Piskorz A.M., Jimenez-Linan M., Bentley D., Hadfield J., May A.P., Caldas C., Brenton J.D., Rosenfeld N. Noninvasive identification and monitoring of cancer mutations by targeted deep sequencing of plasma DNA. Sci. Transl Med. 2012, 4(136):136ra68. DOI: 4/136/136ra68, [pii] 10.1126/scitranslmed.3003726.
16. García-Olmo D.C., Domínguez C., García-Arranz M., Anker P., Stroun M., García-Verdugo J.M., García-Olmo D. Cell-free nucleic acids circulating in the plasma of colorectal cancer patients induce the oncogenic transformation of susceptible cultured cells. Cancer Res. 2010, 70(2):560-567. DOI: 0008-5472.CAN-09-3513, [pii] 10. 1158/0008-5472.CAN-09-3513.
17. Gorges T.M., Schiller J., Schmitz A., Schuetzmann D., Schatz C., Zollner T.M., Krahn T., von Ahsen O. Cancer therapy monitoring in xenografts by quantitative analysis of circulating tumor DNA. Biomarkers 2012, 17(6):498-506. 10.3109/1354750X.2012.689133.
18. Guha M., Castellanos-Rizaldos E., Liu P., Mamon H., Makrigiorgos G.M. Differential strand separation at critical temperature: a minimally disruptive enrichment method for low-abundance unknown DNA mutations. Nucleic Acids Res. 2013, 41(3):e50. 10.1093/nar/gks1250.
19. Heitzer E., Auer M., Gasch C., Pichler M., Ulz P., Hoffmann E.M., Lax S., Waldispuehl-Geigl J., Mauermann O., Lackner C., Höfler G., Eisner F., Sill H., Samonigg H., Pantel K., Riethdorf S., Bauernhofer T., Geigl J.B., Speicher M.R. Complex tumor genomes inferred from single circulating tumor cells by array-CGH and next-generation sequencing. Cancer Res. 2013, 73(10):2965-2975. 10.1158/0008-5472.CAN-12-4140.
20. Holohan C., Van Schaeybroeck S., Longley D.B., Johnston P.G. Cancer drug resistance: an evolving paradigm. Nat. Rev. Cancer 2013, Oct, 13(10):714-726. 10.1038/nrc3599.
21. Jung K., Fleischhacker M., Rabien A. Cell-free DNA in the blood as a solid tumor biomarker - a critical appraisal of the literature. Clin. Chim. Acta 2010, 411(21-22):1611-1624. DOI: S0009-8981(10)00491-2, [pii] 10.1016/j.cca.2010.07.032.
22. Leon S.A., Shapiro B., Sklaroff D.M., Yaros M.J. Free DNA in the serum of cancer patients and the effect of therapy. Cancer Res. 1977, 37(3):646-650.
23. Lièvre A., Bachet J.B., Le Corre D., Boige V., Landi B., Emile J.F., CÔté J.F., Tomasic G., Penna C., Ducreux M., Rougier P., Penault-Llorca F., Laurent-Puig P. KRAS mutation status is predictive of response to cetuximab therapy in colorectal cancer. Cancer Res. 2006, 66(8):3992-3995. DOI: 66/8/3992, [pii] 10. 1158/0008-5472.CAN-06-0191.
24. Lièvre A., Bachet J.B., Boige V., Cayre A., Le Corre D., Buc E., Ychou M., Bouché O., Landi B., Louvet C., André T., Bibeau F., Diebold M.D., Rougier P., Ducreux M., Tomasic G., Emile J.F., Penault-Llorca F., Laurent-Puig P. KRAS mutations as an independent prognostic factor in patients with advanced colorectal cancer treated with cetuximab. J. Clin. Oncol. 2008, 26(3):374-379. DOI: 26/3/374, [pii] 10.1200/JCO.2007.12.5906.
25. Misale S., Yaeger R., Hobor S., Scala E., Janakiraman M., Liska D., Valtorta E., Schiavo R., Buscarino M., Siravegna G., Bencardino K., Cercek A., Chen C.T., Veronese S., Zanon C., Sartore-Bianchi A., Gambacorta M., Gallicchio M., Vakiani E., Boscaro V., Medico E., Weiser M., Siena S., Di Nicolantonio F., Solit D., Bardelli A. Emergence of KRAS mutations and acquired resistance to anti-EGFR therapy in colorectal cancer. Nature 2012, 486(7404):532-536. DOI: nature11156, [pii] 10.1038/nature11156.
26. Mouliere F., Thierry A.R. The importance of examining the proportion of circulating DNA originating from tumor, microenvironment and normal cells in colorectal cancer patients. Expert Opin. Biol. Ther. 2012, 12(Suppl. 1):S209-S215. 10.1517/14712598.2012.688023.
27. Mouliere F., Robert B., Peyrotte E.A., Del Rio M., Ychou M., Molina F., Gongora C., Thierry A.R. High fragmentation characterizes tumour-derived circulating DNA. Plos One 2011, 6(9). DOI: e23418 10.1371/journal.pone.0023418.
28. Mouliere F., El Messaoudi S., Gongora C., Guedj A.S., Robert B., Del Rio M., Molina F., Lamy P.J., Lopez-Crapez E., Mathonnet M., Ychou M., Pezet D., Thierry A.R. Circulating cell-free DNA from colorectal cancer patients may reveal high KRAS or BRAF mutation load. Transl Oncol. 2013, 6(3):319-328.
29. Murtaza M., Dawson S.J., Tsui D.W., Gale D., Forshew T., Piskorz A.M., Parkinson C., Chin S.F., Kingsbury Z., Wong A.S., Marass F., Humphray S., Hadfield J., Bentley D., Chin T.M., Brenton J.D., Caldas C., Rosenfeld N. Non-invasive analysis of acquired resistance to cancer therapy by sequencing of plasma DNA. Nature 2013, 497(7447):108-112. 10.1038/nature12065.
30. Narayan A., Carriero N.J., Gettinger S.N., Kluytenaar J., Kozak K.R., Yock T.I., Muscato N.E., Ugarelli P., Decker R.H., Patel A.A. Ultrasensitive measurement of hotspot mutations in tumor DNA in blood using error-suppressed multiplexed deep sequencing. Cancer Res. 2012, 72(14):3492-3498. 10.1158/0008-5472.CAN-11-4037.
31. Pang D., Winters T.A., Jung M., Purkayastha S., Cavalli L.R., Chasovkikh S., Haddad B.R., Dritschilo A. Radiation-generated short DNA fragments may perturb non-homologous end-joining and induce genomic instability. J. Radiat. Res. 2011, 52(3):309-319. DOI: JST.JSTAGE/jrr/10147, [pii].
32. Pascal Artru, Ducreux Michel, Lièvre Astrid, Guiu Michel, Merlin Jean-Louis, Sabourin Jean-Christophe, Viguier JérÔme, Bastie Anne, Seronde Audrey, Laurent-Puig Pierre Review of the current status of KRAS mutation testing in France in 2011: the flash-KRAS study. J. Clin. Oncol. 2012, 30(suppl.):e14129. abstr.
33. Perkins G., Yap T.A., Pope L., Cassidy A.M., Dukes J.P., Riisnaes R., Massard C., Cassier P.A., Miranda S., Clark J., Denholm K.A., Thway K., Gonzalez De Castro D., Attard G., Molife L.R., Kaye S.B., Banerji U., de Bono J.S. Multi-purpose utility of circulating plasma DNA testing in patients with advanced cancers. PLoS One 2012, 7(11):e47020. 10.1371/journal.pone.0047020.
34. Rykova E.Y., Morozkin E.S., Ponomaryova A.A., Loseva E.M., Zaporozhchenko I.A., Cherdyntseva N.V., Vlassov V.V., Laktionov P.P. Cell-free and cell-bound circulating nucleic acid complexes: mechanisms of generation, concentration and content. Expert Opin. Biol. Ther. 2012, 12(Suppl 1):S141-S153. 10.1517/14712598.2012.673577.
35. Salvianti F., Pinzani P., Verderio P., Ciniselli C.M., Massi D., De Giorgi V., Grazzini M., Pazzagli M., Orlando C. Multiparametric analysis of cell-free DNA in melanoma patients. PLoS One 2012, 7(11):e49843. 10.1371/journal.pone.0049843.
36. Schmidt B., Weickmann S., Witt C., Fleischhacker M. Integrity of cell-free plasma DNA in patients with lung cancer and nonmalignant lung disease. Ann. N. Y Acad. Sci. 2008, 1137:207-213. DOI: NYAS1137034, [pii] 10.1196/annals.1448.034.
37. Schwartz S., Meshorer E., Ast G. Chromatin organization marks exon-intron structure. Nat. Struct. Mol. Biol. 2009, 16(9):990-995. DOI: nsmb.1659, [pii] 10.1038/nsmb.1659.
38. Schwarzenbach H., Hoon D.S., Pantel K. Cell-free nucleic acids as biomarkers in cancer patients. Nat. Rev. Cancer 2011, 11(6):426-437. DOI: nrc3066, [pii] 10.1038/nrc3066.
39. Spindler K.L., Pallisgaard N., Vogelius I., Jakobsen A. Quantitative cell-free DNA, KRAS, and BRAF mutations in plasma from patients with metastatic colorectal cancer during treatment with cetuximab and irinotecan. Clin. Cancer Res. 2012, 18(4):1177-1185. DOI: 1078-0432.CCR-11-0564, [pii] 10.1158/1078-0432.CCR-11-0564.
40. Stroun M., Anker P., Lyautey J., Lederrey C., Maurice P.A. Isolation and characterization of DNA from the plasma of cancer patients. Eur. J. Cancer Clin. Oncol. 1987, 23(6):707-712.
41. Stroun M., Lyautey J., Lederrey C., Olson-Sand A., Anker P. About the possible origin and mechanism of circulating DNA apoptosis and active DNA release. Clin. Chim. Acta 2001, 313(1-2):139-142. DOI: S0009898101006659, [pii].
42. Taly V., Pekin D., El Abed A., Laurent-Puig P. Detecting biomarkers with microdroplet technology. Trends Mol. Med. 2012, 18(7):405-416. 10.1016/j.molmed.2012.05.001.
43. Thierry A.R., Mouliere F., Gongora C., Ollier J., Robert B., Ychou M., Del Rio M., Molina F. Origin and quantification of circulating DNA in mice with human colorectal cancer xenografts. Nucleic Acids Res. 2010, 38(18):6159-6175. 10.1093/nar/gkq421.
44. Thierry A.R., Mouliere F., EL messaoudi S., Mollevi C., Lopez-Crapez E., Rolet F., Gillet B., Gongora C., Dechelotte P., Robert B., Del Rio M., Lamy P.J., Bibeau F., Nouaille M., Loriot V., Jarousse A.S., Molina F., Mathonnet M., Pezet D., Ychou M. Clinical validation of the detection of KRAS and BRAF mutations from circulating tumor DNA. Nat. Medicine 2014, 10.1038/nm.3511.
45. Van Cutsem E., Köhne C.H., Láng I., Folprecht G., Nowacki M.P., Cascinu S., Shchepotin I., Maurel J., Cunningham D., Tejpar S., Schlichting M., Zubel A., Celik I., Rougier P., Ciardiello F. Cetuximab plus irinotecan, fluorouracil, and leucovorin as first-line treatment for metastatic colorectal cancer: updated analysis of overall survival according to tumor KRAS and BRAF mutation status. J. Clin. Oncol. 2011, 29(15):2011-2019. DOI: JCO.2010.33.5091, [pii] 10.1200/JCO.2010.33.5091.
46. van der Vaart M., Pretorius P.J. Is the role of circulating DNA as a biomarker of cancer being prematurely overrated?. Clin. Biochem. 2010, 43(1-2):26-36. DOI: S0009-9120(09)00372-5, [pii] 10.1016/j.clinbiochem.2009.08.027.
47. West N.P., Dattani M., McShane P., Hutchins G., Grabsch J., Mueller W., Treanor D., Quirke P., Grabsch H. The proportion of tumour cells is an independent predictor for survival in colorectal cancer patients. Br. J. Cancer 2010, 102(10):1519-1523. 6605674 [pii] 10.1038/sj.bjc.6605674.
48. Whale A.S., Huggett J.F., Cowen S., Speirs V., Shaw J., Ellison S., Foy C.A., Scott D.J. Comparison of microfluidic digital PCR and conventional quantitative PCR for measuring copy number variation. Nucleic Acids Res. 2012, 40(11):e82. 10.1093/nar/gks203.