Circulating tumor DNA analysis as a real-time method for monitoring tumor burden in melanoma patients undergoing treatment with immune checkpoint blockade

Journal for ImmunoTherapy of Cancer

Volumn 2, Issue 1, 2014, Pages

  Lipson, Evan J ^a   Velculescu, Victor E ^a   Pritchard, Theresa S ^a   Sausen, Mark ^b   Pardoll, Drew M ^a   Topalian, Suzanne L ^a   Diaz, Luis A ^a  

^a JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b Personal Genome Diagnostics   (United States)

Author keywords

Anti PD 1; Biomarker; Checkpoint blockade; Circulating tumor DNA; Immunotherapy; Ipilimumab

Indexed keywords

B RAF KINASE; BMS 936559; CIRCULATING TUMOR DNA; DNA; IPILIMUMAB; STEM CELL FACTOR RECEPTOR; TELOMERASE REVERSE TRANSCRIPTASE; UNCLASSIFIED DRUG;

ADULT; AGED; ARTICLE; BIOPSY; CLINICAL ARTICLE; DISEASE COURSE; DNA DETERMINATION; FEMALE; GENE; HUMAN; LYMPHADENOPATHY; MALE; MELANOMA; MIDDLE AGED; MUTATION; NRAS GENE; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; RADIOGRAPHY; SEQUENCE ANALYSIS; TUMOR REGRESSION; TUMOR VOLUME;

EID: 84977068103     PISSN: None     EISSN: 20511426     Source Type: Journal    
DOI: 10.1186/s40425-014-0042-0     Document Type: Article

References (32)

1. Bettegowda C, Sausen M, Leary RJ, Kinde I, Wang Y, Agrawal N, Bartlett BR, Wang H, Luber B, Alani RM, Antonarakis ES, Azad NS, Bardelli A, Brem H, Cameron JL, Lee CC, Fecher LA, Gallia GL, Gibbs P, Le D, Giuntoli RL, Goggins M, Hogarty MD, Holdhoff M, Hong SM, Jiao Y, Juhl HH, Kim JJ, Siravegna G, Laheru D, et al. Detection of circulating tumor DNA in early- and late-stage human malignancies. Sci Transl Med 2014, 6:224ra24. 10.1126/scitranslmed.3007094, 24553385.
2. Leary RJ, Sausen M, Kinde I, Papadopoulos N, Carpten JD, Craig D, O'Shaughnessy J, Kinzler KW, Parmigiani G, Vogelstein B, Diaz LA, Velculescu VE. Detection of chromosomal alterations in the circulation of cancer patients with whole-genome sequencing. Sci Transl Med 2012, 4:162ra154. 10.1126/scitranslmed.3004742, 23197571.
3. Newman AM, Bratman SV, To J, Wynne JF, Eclov NC, Modlin LA, Liu CL, Neal JW, Wakelee HA, Merritt RE, Shrager JB, Loo BW, Alizadeh AA, Diehn M. An ultrasensitive method for quantitating circulating tumor DNA with broad patient coverage. Nat Med 2014, 20:548-554. 10.1038/nm.3519, 24705333.
4. Forshew T, Murtaza M, Parkinson C, Gale D, Tsui DW, Kaper F, Dawson SJ, Piskorz AM, Jimenez-Linan M, Bentley D, Hadfield J, May AP, Caldas C, Brenton JD, Rosenfeld N. Noninvasive identification and monitoring of cancer mutations by targeted deep sequencing of plasma DNA. Sci Transl Med 2012, 4:136ra68. 10.1126/scitranslmed.3003726, 22649089.
5. Diehl F, Li M, Dressman D, He Y, Shen D, Szabo S, Diaz LA, Goodman SN, David KA, Juhl H, Kinzler KW, Vogelstein B. Detection and quantification of mutations in the plasma of patients with colorectal tumors. Proc Natl Acad Sci U S A 2005, 102:16368-16373. 10.1073/pnas.0507904102, 16258065.
6. Dawson SJ, Tsui DW, Murtaza M, Biggs H, Rueda OM, Chin SF, Dunning MJ, 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, 368:1199-1209. 10.1056/NEJMoa1213261, 23484797.
7. Diehl F, Schmidt K, Choti MA, Romans K, Goodman S, Li M, Thornton K, Agrawal N, Sokoll L, Szabo SA, Kinzler KW, Vogelstein B, Diaz LA. Circulating mutant DNA to assess tumor dynamics. Nat Med 2008, 14:985-990. 10.1038/nm.1789, 18670422.
8. Momtaz P, Gaskell AA, Merghoub T, Viale A, Chapman PB. Correlation of tumor-derived circulating cell free DNA (cfDNA) measured by digital PCR (DigPCR) with tumor burden measured radiographically in patients (pts) with BRAFV600Emutated melanoma (mel) treated with RAF inhibitor (RAFi) and/or ipilimumab (Ipi). ASCO Meeting Abstracts 2014, 32:9085.
9. Pardoll DM. The blockade of immune checkpoints in cancer immunotherapy. Nat Rev Cancer 2012, 12:252-264. 10.1038/nrc3239, 22437870.
10. Wolchok JD, Hoos A, O'Day S, Weber JS, Hamid O, Lebbe C, Maio M, Binder M, Bohnsack O, Nichol G, Humphrey R, Hodi FS. Guidelines for the evaluation of immune therapy activity in solid tumors: immune-related response criteria. Clin Cancer Res 2009, 15:7412-7420. 10.1158/1078-0432.CCR-09-1624, 19934295.
11. Saenger YM, Wolchok JD. The heterogeneity of the kinetics of response to ipilimumab in metastatic melanoma: patient cases. Cancer Immun 2008, 8:1. 18198818.
12. Eisenhauer EA, Therasse P, Bogaerts J, Schwartz LH, Sargent D, Ford R, Dancey J, Arbuck S, Gwyther S, Mooney M, Rubinstein L, Shankar L, Dodd L, Kaplan R, Lacombe D, Verweij J. New response evaluation criteria in solid tumours: revised RECIST guideline (version 1.1). Eur J Cancer 2009, 45:228-247. 10.1016/j.ejca.2008.10.026, 19097774.
13. Lipson EJ, Sharfman WH, Drake CG, Wollner I, Taube JM, Anders RA, Xu H, Yao S, Pons A, Chen L, Pardoll DM, Brahmer JR, Topalian SL. Durable cancer regression off-treatment and effective reinduction therapy with an anti-PD-1 antibody. Clin Cancer Res 2013, 19:462-468. 10.1158/1078-0432.CCR-12-2625, 23169436.
14. Brahmer JR, Tykodi SS, Chow LQ, Hwu WJ, Topalian SL, Hwu P, Drake CG, Camacho LH, Kauh J, Odunsi K, Pitot HC, Hamid O, Bhatia S, Martins R, Eaton K, Chen S, Salay TM, Alaparthy S, Grosso JF, Korman AJ, Parker SM, Agrawal S, Goldberg SM, Pardoll DM, Gupta A, Wigginton JM. Safety and activity of anti-PD-L1 antibody in patients with advanced cancer. N Engl J Med 2012, 366:2455-2465. 10.1056/NEJMoa1200694, 22658128.
15. Hodi FS, O'Day SJ, McDermott DF, Weber RW, Sosman JA, Haanen JB, Gonzalez R, Robert C, Schadendorf D, Hassel JC, Akerley W, van den Eertwegh AJ, Lutzky J, Lorigan P, Vaubel JM, Linette GP, Hogg D, Ottensmeier CH, Lebbe C, Peschel C, Quirt I, Clark JI, Wolchok JD, Weber JS, Tian J, Yellin MJ, Nichol GM, Hoos A, Urba WJ. Improved survival with ipilimumab in patients with metastatic melanoma. N Engl J Med 2010, 363:711-723. 10.1056/NEJMoa1003466, 20525992.
16. Topalian SL, Sznol M, McDermott DF, Kluger HM, Carvajal RD, Sharfman WH, Brahmer JR, Lawrence DP, Atkins MB, Powderly JD, Leming PD, Lipson EJ, Puzanov I, Smith DC, Taube JM, Wigginton JM, Kollia GD, Gupta A, Pardoll DM, Sosman JA, Hodi FS. Survival, durable tumor remission, and long-term safety in patients with advanced melanoma receiving nivolumab. J Clin Oncol 2014, 32:1020-1030. 10.1200/JCO.2013.53.0105, 24590637.
17. Ribas A, Chmielowski B, Glaspy JA. Do we need a different set of response assessment criteria for tumor immunotherapy?. Clin Cancer Res 2009, 15:7116-7118. 10.1158/1078-0432.CCR-09-2376, 19934296.
18. Weber JS, Kahler KC, Hauschild A. Management of immune-related adverse events and kinetics of response with ipilimumab. J Clin Oncol 2012, 30:2691-2697. 10.1200/JCO.2012.41.6750, 22614989.
19. Huang FW, Hodis E, Xu MJ, Kryukov GV, Chin L, Garraway LA. Highly recurrent TERT promoter mutations in human melanoma. Science 2013, 339:957-959. 10.1126/science.1229259, 23348506.
20. Wood LD, Parsons DW, Jones S, Lin J, Sjoblom T, Leary RJ, Shen D, Boca SM, Barber T, Ptak J, Silliman N, Szabo S, Dezso Z, Ustyanksky V, Nikolskaya T, Nikolsky Y, Karchin R, Wilson PA, Kaminker JS, Zhang Z, Croshaw R, Willis J, Dawson D, Shipitsin M, Willson JK, Sukumar S, Polyak K, Park BH, Pethiyagoda CL, Pant PV, et al. The genomic landscapes of human breast and colorectal cancers. Science 2007, 318:1108-1113. 10.1126/science.1145720, 17932254.
21. Parsons DW, Jones S, Zhang X, Lin JC, Leary RJ, Angenendt P, Mankoo P, Carter H, Siu IM, Gallia GL, Olivi A, McLendon R, Rasheed BA, Keir S, Nikolskaya T, Nikolsky Y, Busam DA, Tekleab H, Diaz LA, Hartigan J, Smith DR, Strausberg RL, Marie SK, Shinjo SM, Yan H, Riggins GJ, Bigner DD, Karchin R, Papadopoulos N, Parmigiani G, Vogelstein B, Velculescu VE, Kinzler KW. An integrated genomic analysis of human glioblastoma multiforme. Science 2008, 321:1807-1812. 10.1126/science.1164382, 18772396.
22. Jones S, Zhang X, Parsons DW, Lin JC, Leary RJ, Angenendt P, Mankoo P, Carter H, Kamiyama H, Jimeno A, Hong SM, Fu B, Lin MT, Calhoun ES, Kamiyama M, Walter K, Nikolskaya T, Nikolsky Y, Hartigan J, Smith DR, Hidalgo M, Leach SD, Klein AP, Jaffee EM, Goggins M, Maitra A, Iacobuzio-Donahue C, Eshleman JR, Kern SE, Hruban RH, Karchin R, Papadopoulos N, Parmigiani G, Vogelstein B, Velculescu VE, Kinzler KW. Core signaling pathways in human pancreatic cancers revealed by global genomic analyses. Science 2008, 321:1801-1806. 10.1126/science.1164368, 18772397.
23. Sausen M, Leary RJ, Jones S, Wu J, Reynolds CP, Liu X, Blackford A, Parmigiani G, Diaz LA, Papadopoulos N, Vogelstein B, Kinzler KW, Velculescu VE, Hogarty MD. Integrated genomic analyses identify ARID1A and ARID1B alterations in the childhood cancer neuroblastoma. Nat Genet 2013, 45:12-17. 10.1038/ng.2493, 23202128.
24. Diehl F, Li M, He Y, Kinzler KW, Vogelstein B, Dressman D. BEAMing: single-molecule PCR on microparticles in water-in-oil emulsions. Nat Methods 2006, 3:551-559. 10.1038/nmeth898, 16791214.
25. Kinde I, Wu J, Papadopoulos N, Kinzler KW, Vogelstein B. Detection and quantification of rare mutations with massively parallel sequencing. Proc Natl Acad Sci U S A 2011, 108:9530-9535. 10.1073/pnas.1105422108, 21586637.
26. Hodis E, Watson I, Kryukov G, Arold S, Imielinski M, Theurillat J, Nickerson E, Auclair D, Li L, Place C, DiCara D, Ramos A, Lawrence M, Cibulskis K, Sivachenko A, Voet D, Saksena G, Stransky N, Onofrio R, Winckler W, Ardlie K, Wagle N, Wargo J, Chong K, Morton D, Stemke-Hale K, Chen G, Noble M, Meyerson M, Ladbury J, Davies M, Gershenwald J, Wagner S, Hoon DB, Schadendorf D, Lander E, Gabriel S, Getz G, Garraway L, Chin L. A Landscape of Driver Mutations in Melanoma. Cell 2012, 150:251-263. 10.1016/j.cell.2012.06.024, 22817889.
27. Griewank KG, Murali R, Puig-Butille JA, Schilling B, Livingstone E, Potrony M, Carrera C, Schimming T, Moller I, Schwamborn M, Sucker A, Hillen U, Badenas C, Malvehy J, Zimmer L, Scherag A, Puig S, Schadendorf D. TERT promoter mutation status as an independent prognostic factor in cutaneous melanoma. J Natl Cancer Inst 2014, 106:dju246. 10.1093/jnci/dju246, 25217772.
28. Diaz LA, Bardelli A. Liquid Biopsies: Genotyping Circulating Tumor DNA. J Clin Oncol 2014, 32:579-586. 10.1200/JCO.2012.45.2011, 24449238.
29. Haber DA, Velculescu VE. Blood-based analyses of cancer: circulating tumor cells and circulating tumor DNA. Cancer Discov 2014, 4:650-661. 10.1158/2159-8290.CD-13-1014, 24801577.
30. Mir M, Chan CS, Khan F, Krishnan B, Orengo I, Rosen T. The rate of melanoma transection with various biopsy techniques and the influence of tumor transection on patient survival. J Am Acad Dermatol 2013, 68:452-458. 10.1016/j.jaad.2012.08.005, 22967665.
31. Martires KJ, Nandi T, Honda K, Cooper KD, Bordeaux JS. Prognosis of patients with transected melanomas. Dermatol Surg 2013, 39:605-615. 10.1111/dsu.12124, 23379583.
32. Mills JK, White I, Diggs B, Fortino J, Vetto JT. Effect of biopsy type on outcomes in the treatment of primary cutaneous melanoma. Am J Surg 2013, 205:585-590. 10.1016/j.amjsurg.2013.01.023, 23592167.