Inferring mutational timing and reconstructing tumour evolutionary histories

Biochimica et Biophysica Acta - Reviews on Cancer

Volumn 1855, Issue 2, 2015, Pages 264-275

  Turajlic, Samra ^a   McGranahan, Nicholas ^a   Swanton, Charles ^a,b  

^a THE FRANCIS CRICK INSTITUTE   (United Kingdom)

^b UNIVERSITY COLLEGE LONDON   (United Kingdom)

Author keywords

Cancer evolution; Intratumour heterogeneity; Mutational timing; Subclonal mutations; Treatment resistance

Indexed keywords

ACUTE GRANULOCYTIC LEUKEMIA; BAYES THEOREM; BREAST CANCER; CANCER RESISTANCE; CHRONIC LYMPHATIC LEUKEMIA; COLORECTAL CANCER; COMPUTER ANALYSIS; COMPUTER PROGRAM; COPY NUMBER VARIATION; FOLLICULAR LYMPHOMA; GENE FREQUENCY; GENE MUTATION; GENE SEQUENCE; GLIOBLASTOMA; HUMAN; KIDNEY CARCINOMA; LUNG ADENOCARCINOMA; MALIGNANT NEOPLASTIC DISEASE; MELANOMA; MOLECULAR EVOLUTION; MYELODYSPLASTIC SYNDROME; NEXT GENERATION SEQUENCING; NONHUMAN; OVARY CANCER; PANCREAS CANCER; PHARMACOGENETICS; PRIORITY JOURNAL; REVIEW; TUMOR MICROENVIRONMENT; EVOLUTION, MOLECULAR; GENETICS; HIGH-THROUGHPUT NUCLEOTIDE SEQUENCING; HUMANS; MUTATION; MUTATION RATE; NEOPLASMS; PATHOLOGY; PROGNOSIS; SIGNAL TRANSDUCTION;

EVOLUTION, MOLECULAR; HIGH-THROUGHPUT NUCLEOTIDE SEQUENCING; HUMANS; MUTATION; MUTATION RATE; NEOPLASMS; PROGNOSIS; SIGNAL TRANSDUCTION;

EID: 84926434303     PISSN: 0304419X     EISSN: 18792561     Source Type: Journal    
DOI: 10.1016/j.bbcan.2015.03.005     Document Type: Review

References (119)

1. Burrell R.A., McGranahan N., Bartek J., Swanton C. The causes and consequences of genetic heterogeneity in cancer evolution. Nature 2013, 501:338-345.
2. Yates L.R., Campbell P.J. Evolution of the cancer genome. Nat. Rev. Genet. 2012, 13:795-806.
3. Navin N.E., Hicks J. Tracing the tumor lineage. Mol. Oncol. 2010, 4:267-283.
4. Sottoriva A., Kang H., Ma Z., Graham T.A., Salomon M.P., Zhao J., Marjoram P., Siegmund K., Press M.F., Shibata D., Curtis C. A Big Bang model of human colorectal tumor growth. Nat. Genet. 2015, 47:209-216.
5. Gerlinger M., Horswell S., Larkin J., Rowan A.J., Salm M.P., Varela I., Fisher R., McGranahan N., Matthews N., Santos C.R., Martinez P., Phillimore B., Begum S., Rabinowitz A., Spencer-Dene B., Gulati S., Bates P.A., Stamp G., Pickering L., Gore M., Nicol D.L., Hazell S., Futreal P.A., Stewart A., Swanton C. Genomic architecture and evolution of clear cell renal cell carcinomas defined by multiregion sequencing. Nat. Genet. 2014, 46:225-233.
6. Tomasetti C., Vogelstein B., Parmigiani G. Half or more of the somatic mutations in cancers of self-renewing tissues originate prior to tumor initiation. Proc. Natl. Acad. Sci. U. S. A. 2013, 110:1999-2004.
7. Weaver J.M., Ross-Innes C.S., Shannon N., Lynch A.G., Forshew T., Barbera M., Murtaza M., Ong C.A., Lao-Sirieix P., Dunning M.J., Smith L., Smith M.L., Anderson C.L., Carvalho B., O'Donovan M., Underwood T.J., May A.P., Grehan N., Hardwick R., Davies J., Oloumi A., Aparicio S., Caldas C., Eldridge M.D., Edwards P.A., Rosenfeld N., Tavare S., Fitzgerald R.C., Consortium O. Ordering of mutations in preinvasive disease stages of esophageal carcinogenesis. Nat. Genet. 2014, 46:837-843.
8. Sato Y., Yoshizato T., Shiraishi Y., Maekawa S., Okuno Y., Kamura T., Shimamura T., Sato-Otsubo A., Nagae G., Suzuki H., Nagata Y., Yoshida K., Kon A., Suzuki Y., Chiba K., Tanaka H., Niida A., Fujimoto A., Tsunoda T., Morikawa T., Maeda D., Kume H., Sugano S., Fukayama M., Aburatani H., Sanada M., Miyano S., Homma Y., Ogawa S. Integrated molecular analysis of clear-cell renal cell carcinoma. Nat. Genet. 2013, 45:860-867.
9. Landau D.A., Carter S.L., Stojanov P., McKenna A., Stevenson K., Lawrence M.S., Sougnez C., Stewart C., Sivachenko A., Wang L., Wan Y., Zhang W., Shukla S.A., Vartanov A., Fernandes S.M., Saksena G., Cibulskis K., Tesar B., Gabriel S., Hacohen N., Meyerson M., Lander E.S., Neuberg D., Brown J.R., Getz G., Wu C.J. Evolution and impact of subclonal mutations in chronic lymphocytic leukemia. Cell 2013, 152:714-726.
10. Zhang J., Fujimoto J., Zhang J., Wedge D.C., Song X., Zhang J., Seth S., Chow C.W., Cao Y., Gumbs C., Gold K.A., Kalhor N., Little L., Mahadeshwar H., Moran C., Protopopov A., Sun H., Tang J., Wu X., Ye Y., William W.N., Lee J.J., Heymach J.V., Hong W.K., Swisher S., Wistuba P.A. Futreal, intratumor heterogeneity in localized lung adenocarcinomas delineated by multiregion sequencing. Science 2014, 346:256-259.
11. Maley C.C., Rustgi A.K. Barrett's esophagus and its progression to adenocarcinoma. J. Natl. Compr. Cancer Netw. 2006, 4:367-374.
12. Ortmann C.A., Kent D.G., Nangalia J., Silber Y., Wedge D.C., Grinfeld J., Baxter E.J., Massie C.E., Papaemmanuil E., Menon S., Godfrey A.L., Dimitropoulou D., Guglielmelli P., Bellosillo B., Besses C., Dohner K., Harrison C.N., Vassiliou G.S., Vannucchi A., Campbell P.J., Green A.R. Effect of mutation order on myeloproliferative neoplasms. N. Engl. J. Med. 2015, 372:601-612.
13. Sottoriva A., Graham T. A Pan-cancer Signature of Neutral Tumor Evolution 2015, bioRxiv.
14. Lohr J.G., Stojanov P., Carter S.L., Cruz-Gordillo P., Lawrence M.S., Auclair D., Sougnez C., Knoechel B., Gould J., Saksena G., Cibulskis K., McKenna A., Chapman M.A., Straussman R., Levy J., Perkins L.M., Keats J.J., Schumacher S.E., Rosenberg M., C.Multiple Myeloma Research, Getz G., Golub T.R. Widespread genetic heterogeneity in multiple myeloma: implications for targeted therapy. Cancer Cell 2014, 25:91-101.
15. Keats J.J., Chesi M., Egan J.B., Garbitt V.M., Palmer S.E., Braggio E., Van Wier S., Blackburn P.R., Baker A.S., Dispenzieri A., Kumar S., Rajkumar S.V., Carpten J.D., Barrett M., Fonseca R., Stewart A.K., Bergsagel P.L. Clonal competition with alternating dominance in multiple myeloma. Blood 2012, 120:1067-1076.
16. Egan J.B., Shi C.X., Tembe W., Christoforides A., Kurdoglu A., Sinari S., Middha S., Asmann Y., Schmidt J., Braggio E., Keats J.J., Fonseca R., Bergsagel P.L., Craig D.W., Carpten J.D., Stewart A.K. Whole-genome sequencing of multiple myeloma from diagnosis to plasma cell leukemia reveals genomic initiating events, evolution, and clonal tides. Blood 2012, 120:1060-1066.
17. Bolli N., Avet-Loiseau H., Wedge D.C., Van Loo P., Alexandrov L.B., Martincorena I., Dawson K.J., Iorio F., Nik-Zainal S., Bignell G.R., Hinton J.W., Li Y., Tubio J.M., McLaren S., O.M.S, Butler A.P., Teague J.W., Mudie L., Anderson E., Rashid N., Tai Y.T., Shammas M.A., Sperling A.S., Fulciniti M., Richardson P.G., Parmigiani G., Magrangeas F., Minvielle S., Moreau P., Attal M., Facon T., Futreal P.A., Anderson K.C., Campbell P.J., Munshi N.C. Heterogeneity of genomic evolution and mutational profiles in multiple myeloma. Nat. Commun. 2014, 5:2997.
18. Romano E., Pradervand S., Paillusson A., Weber J., Harshman K., Muehlethaler K., Speiser D., Peters S., Rimoldi D., Michielin O. Identification of multiple mechanisms of resistance to vemurafenib in a patient with BRAFV600E-mutated cutaneous melanoma successfully rechallenged after progression. Clin. Cancer Res. 2013, 19:5749-5757.
19. Sanchez-Laorden B., Viros A., Girotti M.R., Pedersen M., Saturno G., Zambon A., Niculescu-Duvaz D., Turajlic S., Hayes A., Gore M., Larkin J., Lorigan P., Cook M., Springer C., Marais R. BRAF inhibitors induce metastasis in RAS mutant or inhibitor-resistant melanoma cells by reactivating MEK and ERK signaling. Sci. Signal. 2014, 7:ra30.
20. Gibney G.T., Messina J.L., Fedorenko I.V., Sondak V.K., Smalley K.S. Paradoxical oncogenesis-the long-term effects of BRAF inhibition in melanoma. Nat. Rev. Clin. Oncol. 2013, 10:390-399.
21. Turke A.B., Zejnullahu K., Wu Y.L., Song Y., Dias-Santagata D., Lifshits E., Toschi L., Rogers A., Mok T., Sequist L., Lindeman N.I., Murphy C., Akhavanfard S., Yeap B.Y., Xiao Y., Capelletti M., Iafrate A.J., Lee C., Christensen J.G., Engelman J.A., Janne P.A. Preexistence and clonal selection of MET amplification in EGFR mutant NSCLC. Cancer Cell 2010, 17:77-88.
22. Marusyk A., Tabassum D.P., Altrock P.M., Almendro V., Michor F., Polyak K. Non-cell-autonomous driving of tumour growth supports sub-clonal heterogeneity. Nature 2014, 514:54-58.
23. Inda M.M., Bonavia R., Mukasa A., Narita Y., Sah D.W., Vandenberg S., Brennan C., Johns T.G., Bachoo R., Hadwiger P., Tan P., Depinho R.A., Cavenee W., Furnari F. Tumor heterogeneity is an active process maintained by a mutant EGFR-induced cytokine circuit in glioblastoma. Genes Dev. 2010, 24:1731-1745.
24. Ding L., Ellis M.J., Li S., Larson D.E., Chen K., Wallis J.W., Harris C.C., McLellan M.D., Fulton R.S., Fulton L.L., Abbott R.M., Hoog J., Dooling D.J., Koboldt D.C., Schmidt H., Kalicki J., Zhang Q., Chen L., Lin L., Wendl M.C., McMichael J.F., Magrini V.J., Cook L., McGrath S.D., Vickery T.L., Appelbaum E., Deschryver K., Davies S., Guintoli T., Lin L., Crowder R., Tao Y., Snider J.E., Smith S.M., Dukes A.F., Sanderson G.E., Pohl C.S., Delehaunty K.D., Fronick C.C., Pape K.A., Reed J.S., Robinson J.S., Hodges J.S., Schierding W., Dees N.D., Shen D., Locke D.P., Wiechert M.E., Eldred J.M., Peck J.B., Oberkfell B.J., Lolofie J.T., Du F., Hawkins A.E., O'Laughlin M.D., Bernard K.E., Cunningham M., Elliott G., Mason M.D., Thompson D.M., Ivanovich J.L., Goodfellow P.J., Perou C.M., Weinstock G.M., Aft R., Watson M., Ley T.J., Wilson R.K., Mardis E.R. Genome remodelling in a basal-like breast cancer metastasis and xenograft. Nature 2010, 464:999-1005.
25. Campbell P.J., Yachida S., Mudie L.J., Stephens P.J., Pleasance E.D., Stebbings L.A., Morsberger L.A., Latimer C., McLaren S., Lin M.L., McBride D.J., Varela I., Nik-Zainal S.A., Leroy C., Jia M., Menzies A., Butler A.P., Teague J.W., Griffin C.A., Burton J., Swerdlow H., Quail M.A., Stratton M.R., Iacobuzio-Donahue C., Futreal P.A. The patterns and dynamics of genomic instability in metastatic pancreatic cancer. Nature 2010, 467:1109-1113.
26. Ding L., Kim M., Kanchi K.L., Dees N.D., Lu C., Griffith M., Fenstermacher D., Sung H., Miller C.A., Goetz B., Wendl M.C., Griffith O., Cornelius L.A., Linette G.P., McMichael J.F., Sondak V.K., Fields R.C., Ley T.J., Mule J.J., Wilson R.K., Weber J.S. Clonal architectures and driver mutations in metastatic melanomas. PLoS ONE 2014, 9:e111153.
27. de Bruin E.C., McGranahan N., Mitter R., Salm M., Wedge D.C., Yates L., Jamal-Hanjani M., Shafi S., Murugaesu N., Rowan A.J., Gronroos E., Muhammad M.A., Horswell S., Gerlinger M., Varela I., Jones D., Marshall J., Voet T., Van Loo P., Rassl D.M., Rintoul R.C., Janes S.M., Lee S.M., Forster M., Ahmad T., Lawrence D., Falzon M., Capitanio A., Harkins T.T., Lee C.C., Tom W., Teefe E., Chen S.C., Begum S., Rabinowitz A., Phillimore B., Spencer-Dene B., Stamp G., Szallasi Z., Matthews N., Stewart A., Campbell P., Swanton C. Spatial and temporal diversity in genomic instability processes defines lung cancer evolution. Science 2014, 346:251-256.
28. Yachida S., Jones S., Bozic I., Antal T., Leary R., Fu B., Kamiyama M., Hruban R.H., Eshleman J.R., Nowak M.A., Velculescu V.E., Kinzler K.W., Vogelstein B., Iacobuzio-Donahue C.A. Distant metastasis occurs late during the genetic evolution of pancreatic cancer. Nature 2010, 467:1114-1117.
29. Kostadinov R.L., Kuhner M.K., Li X., Sanchez C.A., Galipeau P.C., Paulson T.G., Sather C.L., Srivastava A., Odze R.D., Blount P.L., Vaughan T.L., Reid B.J., Maley C.C. NSAIDs modulate clonal evolution in Barrett's esophagus. PLoS Genet. 2013, 9:e1003553.
30. Aktipis C.A., Kwan V.S., Johnson K.A., Neuberg S.L., Maley C.C. Overlooking evolution: a systematic analysis of cancer relapse and therapeutic resistance research. PLoS ONE 2011, 6:e26100.
31. Gerlinger M., Rowan A.J., Horswell S., Larkin J., Endesfelder D., Gronroos E., Martinez P., Matthews N., Stewart A., Tarpey P., Varela I., Phillimore B., Begum S., McDonald N.Q., Butler A., Jones D., Raine K., Latimer C., Santos C.R., Nohadani M., Eklund A.C., Spencer-Dene B., Clark G., Pickering L., Stamp G., Gore M., Szallasi Z., Downward J., Futreal P.A., Swanton C. Intratumor heterogeneity and branched evolution revealed by multiregion sequencing. N. Engl. J. Med. 2012, 366:883-892.
32. Sottoriva A., Spiteri I., Piccirillo S.G., Touloumis A., Collins V.P., Marioni J.C., Curtis C., Watts C., Tavare S. Intratumor heterogeneity in human glioblastoma reflects cancer evolutionary dynamics. Proc. Natl. Acad. Sci. U. S. A. 2013, 110:4009-4014.
33. Zare H., Wang J., Hu A., Weber K., Smith J., Nickerson D., Song C., Witten D., Blau C.A., Noble W.S. Inferring clonal composition from multiple sections of a breast cancer. PLoS Comput. Biol. 2014, 10:e1003703.
34. Turajlic S., Furney S.J., Lambros M.B., Mitsopoulos C., Kozarewa I., Geyer F.C., Mackay A., Hakas J., Zvelebil M., Lord C.J., Ashworth A., Thomas M., Stamp G., Larkin J., Reis-Filho J.S., Marais R. Whole genome sequencing of matched primary and metastatic acral melanomas. Genome Res. 2012, 22:196-207.
35. Xie T., Cho Y.B., Wang K., Huang D., Hong H.K., Choi Y.L., Ko Y.H., Nam D.H., Jin J., Yang H., Fernandez J., Deng S., Rejto P.A., Lee W.Y., Mao M. Patterns of somatic alterations between matched primary and metastatic colorectal tumors characterized by whole-genome sequencing. Genomics 2014, 104:234-241.
36. Lee S.Y., Haq F., Kim D., Jun C., Jo H.J., Ahn S.M., Lee W.S. Comparative genomic analysis of primary and synchronous metastatic colorectal cancers. PLoS ONE 2014, 9:e90459.
37. Ouyang L., Lee J., Park C.K., Mao M., Shi Y., Gong Z., Zheng H., Li Y., Zhao Y., Wang G., Fu H., Kim J., Lim H.Y. Whole-genome sequencing of matched primary and metastatic hepatocellular carcinomas. BMC Med. Genet. 2014, 7:2.
38. Huang Y., Gao S., Wu S., Song P., Sun X., Hu X., Zhang S., Yu Y., Zhu J., Li C., Qin Z., Xie L., Yao Q., Tang A., Li Z., Guo G., Wan S., Dong P., Sun L., Li W., Wang D., Gui Y., Yang H., Zhou F., Zhang X., Cai Z. Multilayered molecular profiling supported the monoclonal origin of metastatic renal cell carcinoma. Int. J. Cancer 2014, 135:78-87.
39. De Mattos-Arruda L., Bidard F.C., Won H.H., Cortes J., Ng C.K., Peg V., Nuciforo P., Jungbluth A.A., Weigelt B., Berger M.F., Seoane J., Reis-Filho J.S. Establishing the origin of metastatic deposits in the setting of multiple primary malignancies: the role of massively parallel sequencing. Mol. Oncol. 2014, 8:150-158.
40. Bashashati A., Ha G., Tone A., Ding J., Prentice L.M., Roth A., Rosner J., Shumansky K., Kalloger S., Senz J., Yang W., McConechy M., Melnyk N., Anglesio M., Luk M.T., Tse K., Zeng T., Moore R., Zhao Y., Marra M.A., Gilks B., Yip S., Huntsman D.G., McAlpine J.N., Shah S.P. Distinct evolutionary trajectories of primary high-grade serous ovarian cancers revealed through spatial mutational profiling. J. Pathol. 2013, 231:21-34.
41. Shah S.P., Morin R.D., Khattra J., Prentice L., Pugh T., Burleigh A., Delaney A., Gelmon K., Guliany R., Senz J., Steidl C., Holt R.A., Jones S., Sun M., Leung G., Moore R., Severson T., Taylor G.A., Teschendorff A.E., Tse K., Turashvili G., Varhol R., Warren R.L., Watson P., Zhao Y., Caldas C., Huntsman D., Hirst M., Marra M.A., Aparicio S. Mutational evolution in a lobular breast tumour profiled at single nucleotide resolution. Nature 2009, 461:809-813.
42. Schuh A., Becq J., Humphray S., Alexa A., Burns A., Clifford R., Feller S.M., Grocock R., Henderson S., Khrebtukova I., Kingsbury Z., Luo S., McBride D., Murray L., Menju T., Timbs A., Ross M., Taylor J., Bentley D. Monitoring chronic lymphocytic leukemia progression by whole genome sequencing reveals heterogeneous clonal evolution patterns. Blood 2012, 120:4191-4196.
43. Wu X., Northcott P.A., Dubuc A., Dupuy A.J., Shih D.J., Witt H., Croul S., Bouffet E., Fults D.W., Eberhart C.G., Garzia L., Van Meter T., Zagzag D., Jabado N., Schwartzentruber J., Majewski J., Scheetz T.E., Pfister S.M., Korshunov A., Li X.N., Scherer S.W., Cho Y.J., Akagi K., MacDonald T.J., Koster J., McCabe M.G., Sarver A.L., Collins V.P., Weiss W.A., Largaespada D.A., Collier L.S., Taylor M.D. Clonal selection drives genetic divergence of metastatic medulloblastoma. Nature 2012, 482:529-533.
44. Ding L., Ley T.J., Larson D.E., Miller C.A., Koboldt D.C., Welch J.S., Ritchey J.K., Young M.A., Lamprecht T., McLellan M.D., McMichael J.F., Wallis J.W., Lu C., Shen D., Harris C.C., Dooling D.J., Fulton R.S., Fulton L.L., Chen K., Schmidt H., Kalicki-Veizer J., Magrini V.J., Cook L., McGrath S.D., Vickery T.L., Wendl M.C., Heath S., Watson M.A., Link D.C., Tomasson M.H., Shannon W.D., Payton J.E., Kulkarni S., Westervelt P., Walter M.J., Graubert T.A., Mardis E.R., Wilson R.K., DiPersio J.F. Clonal evolution in relapsed acute myeloid leukaemia revealed by whole-genome sequencing. Nature 2012, 481:506-510.
45. Johnson B.E., Mazor T., Hong C., Barnes M., Aihara K., McLean C.Y., Fouse S.D., Yamamoto S., Ueda H., Tatsuno K., Asthana S., Jalbert L.E., Nelson S.J., Bollen A.W., Gustafson W.C., Charron E., Weiss W.A., Smirnov I.V., Song J.S., Olshen A.B., Cha S., Zhao Y., Moore R.A., Mungall A.J., Jones S.J., Hirst M., Marra M.A., Saito N., Aburatani H., Mukasa A., Berger M.S., Chang S.M., Taylor B.S., Costello J.F. Mutational analysis reveals the origin and therapy-driven evolution of recurrent glioma. Science 2014, 343:189-193.
46. Haffner M.C., Mosbruger T., Esopi D.M., Fedor H., Heaphy C.M., Walker D.A., Adejola N., Gurel M., Hicks J., Meeker A.K., Halushka M.K., Simons J.W., Isaacs W.B., De Marzo A.M., Nelson W.G., Yegnasubramanian S. Tracking the clonal origin of lethal prostate cancer. J. Clin. Invest. 2013, 123:4918-4922.
47. Juric D., Castel P., Griffith M., Griffith O.L., Won H.H., Ellis H., Ebbesen S.H., Ainscough B.J., Ramu A., Iyer G., Shah R.H., Huynh T., Mino-Kenudson M., Sgroi D., Isakoff S., Thabet A., Elamine L., Solit D.B., Lowe S.W., Quadt C., Peters M., Derti A., Schegel R., Huang A., Mardis E.R., Berger M.F., Baselga J., Scaltriti M. Convergent loss of PTEN leads to clinical resistance to a PI(3)Kalpha inhibitor. Nature 2015, 518:240-244.
48. Shapiro E., Biezuner T., Linnarsson S. Single-cell sequencing-based technologies will revolutionize whole-organism science. Nat. Rev. Genet. 2013, 14:618-630.
49. Xu X., Hou Y., Yin X., Bao L., Tang A., Song L., Li F., Tsang S., Wu K., Wu H., He W., Zeng L., Xing M., Wu R., Jiang H., Liu X., Cao D., Guo G., Hu X., Gui Y., Li Z., Xie W., Sun X., Shi M., Cai Z., Wang B., Zhong M., Li J., Lu Z., Gu N., Zhang X., Goodman L., Bolund L., Wang J., Yang H., Kristiansen K., Dean M., Li Y., Wang J. Single-cell exome sequencing reveals single-nucleotide mutation characteristics of a kidney tumor. Cell 2012, 148:886-895.
50. Wang Y., Waters J., Leung M.L., Unruh A., Roh W., Shi X., Chen K., Scheet P., Vattathil S., Liang H., Multani A., Zhang H., Zhao R., Michor F., Meric-Bernstam F., Navin N.E. Clonal evolution in breast cancer revealed by single nucleus genome sequencing. Nature 2014, 512:155-160.
51. Potter N.E., Ermini L., Papaemmanuil E., Cazzaniga G., Vijayaraghavan G., Titley I., Ford A., Campbell P., Kearney L., Greaves M. Single-cell mutational profiling and clonal phylogeny in cancer. Genome Res. 2013, 23:2115-2125.
52. Navin N., Kendall J., Troge J., Andrews P., Rodgers L., McIndoo J., Cook K., Stepansky A., Levy D., Esposito D., Muthuswamy L., Krasnitz A., McCombie W.R., Hicks J., Wigler M. Tumour evolution inferred by single-cell sequencing. Nature 2011, 472:90-94.
53. Hou Y., Song L., Zhu P., Zhang B., Tao Y., Xu X., Li F., Wu K., Liang J., Shao D., Wu H., Ye X., Ye C., Wu R., Jian M., Chen Y., Xie W., Zhang R., Chen L., Liu X., Yao X., Zheng H., Yu C., Li Q., Gong Z., Mao M., Yang X., Yang L., Li J., Wang W., Lu Z., Gu N., Laurie G., Bolund L., Kristiansen K., Wang J., Yang H., Li Y., Zhang X., Wang J. Single-cell exome sequencing and monoclonal evolution of a JAK2-negative myeloproliferative neoplasm. Cell 2012, 148:873-885.
54. Miller C.A., White B.S., Dees N.D., Griffith M., Welch J.S., Griffith O.L., Vij R., Tomasson M.H., Graubert T.A., Walter M.J., Ellis M.J., Schierding W., DiPersio J.F., Ley T.J., Mardis E.R., Wilson R.K., Ding L. SciClone: inferring clonal architecture and tracking the spatial and temporal patterns of tumor evolution. PLoS Comput. Biol. 2014, 10:e1003665.
55. Hajirasouliha I., Mahmoody A., Raphael B.J. A combinatorial approach for analyzing intra-tumor heterogeneity from high-throughput sequencing data. Bioinformatics 2014, 30:i78-i86.
56. Cibulskis K., Lawrence M.S., Carter S.L., Sivachenko A., Jaffe D., Sougnez C., Gabriel S., Meyerson M., Lander E.S., Getz G. Sensitive detection of somatic point mutations in impure and heterogeneous cancer samples. Nat. Biotechnol. 2013, 31:213-219.
57. Pleasance E.D., Cheetham R.K., Stephens P.J., McBride D.J., Humphray S.J., Greenman C.D., Varela I., Lin M.L., Ordonez G.R., Bignell G.R., Ye K., Alipaz J., Bauer M.J., Beare D., Butler A., Carter R.J., Chen L., Cox A.J., Edkins S., Kokko-Gonzales P.I., Gormley N.A., Grocock R.J., Haudenschild C.D., Hims M.M., James T., Jia M., Kingsbury Z., Leroy C., Marshall J., Menzies A., Mudie L.J., Ning Z., Royce T., Schulz-Trieglaff O.B., Spiridou A., Stebbings L.A., Szajkowski L., Teague J., Williamson D., Chin L., Ross M.T., Campbell P.J., Bentley D.R., Futreal P.A., Stratton M.R. A comprehensive catalogue of somatic mutations from a human cancer genome. Nature 2010, 463:191-196.
58. Durinck S., Ho C., Wang N.J., Liao W., Jakkula L.R., Collisson E.A., Pons J., Chan S.W., Lam E.T., Chu C., Park K., Hong S.W., Hur J.S., Huh N., Neuhaus I.M., Yu S.S., Grekin R.C., Mauro T.M., Cleaver J.E., Kwok P.Y., LeBoit P.E., Getz G., Cibulskis K., Aster J.C., Huang H., Purdom E., Li J., Bolund L., Arron S.T., Gray J.W., Spellman P.T., Cho R.J. Temporal dissection of tumorigenesis in primary cancers. Cancer Discov. 2011, 1:137-143.
59. Dewhurst S.M., McGranahan N., Burrell R.A., Rowan A.J., Gronroos E., Endesfelder D., Joshi T., Mouradov D., Gibbs P., Ward R.L., Hawkins N.J., Szallasi Z., Sieber O.M., Swanton C. Tolerance of whole-genome doubling propagates chromosomal instability and accelerates cancer genome evolution. Cancer Discov. 2014, 4:175-185.
60. Beerenwinkel N., Schwarz R.F., Gerstung M., Markowetz F. Cancer evolution: mathematical models and computational inference. Syst. Biol. 2015, 64:e1-e25.
61. Nik-Zainal S., Van Loo P., Wedge D.C., Alexandrov L.B., Greenman C.D., Lau K.W., Raine K., Jones D., Marshall J., Ramakrishna M., Shlien A., Cooke S.L., Hinton J., Menzies A., Stebbings L.A., Leroy C., Jia M., Rance R., Mudie L.J., Gamble S.J., Stephens P.J., McLaren S., Tarpey P.S., Papaemmanuil E., Davies H.R., Varela I., McBride D.J., Bignell G.R., Leung K., Butler A.P., Teague J.W., Martin S., Jonsson G., Mariani O., Boyault S., Miron P., Fatima A., Langerod A., Aparicio S.A., Tutt A., Sieuwerts A.M., Borg A., Thomas G., Salomon A.V., Richardson A.L., Borresen-Dale A.L., Futreal P.A., Stratton M.R., Campbell P.J., C.Breast Cancer Working Group of the International Cancer Genome The life history of 21 breast cancers. Cell 2012, 149:994-1007.
62. Roth A., Khattra J., Yap D., Wan A., Laks E., Biele J., Ha G., Aparicio S., Bouchard-Cote A., Shah S.P. PyClone: statistical inference of clonal population structure in cancer. Nat. Methods 2014, 11:396-398.
63. Hughes A.E., Magrini V., Demeter R., Miller C.A., Fulton R., Fulton L.L., Eades W.C., Elliott K., Heath S., Westervelt P., Ding L., Conrad D.F., White B.S., Shao J., Link D.C., DiPersio J.F., Mardis E.R., Wilson R.K., Ley T.J., Walter M.J., Graubert T.A. Clonal architecture of secondary acute myeloid leukemia defined by single-cell sequencing. PLoS Genet. 2014, 10:e1004462.
64. Fischer A., Vazquez-Garcia I., Illingworth C.J., Mustonen V. High-definition reconstruction of clonal composition in cancer. Cell Rep. 2014, 7:1740-1752.
65. Jiao W., Vembu S., Deshwar A.G., Stein L., Morris Q. Inferring clonal evolution of tumors from single nucleotide somatic mutations. BMC Bioinformatics 2014, 15:35.
66. Strino F., Parisi F., Micsinai M., Kluger Y. TrAp: a tree approach for fingerprinting subclonal tumor composition. Nucleic Acids Res. 2013, 41:e165.
67. Qiao Y., Quinlan A.R., Jazaeri A.A., Verhaak R.G., Wheeler D.A., Marth G.T. SubcloneSeeker: a computational framework for reconstructing tumor clone structure for cancer variant interpretation and prioritization. Genome Biol. 2014, 15:443.
68. Hoglund M., Frigyesi A., Sall T., Gisselsson D., Mitelman F. Statistical behavior of complex cancer karyotypes. Genes Chromosomes Cancer 2005, 42:327-341.
69. Attolini C.S., Cheng Y.K., Beroukhim R., Getz G., Abdel-Wahab O., Levine R.L., Mellinghoff I.K., Michor F. A mathematical framework to determine the temporal sequence of somatic genetic events in cancer. Proc. Natl. Acad. Sci. U. S. A. 2010, 107:17604-17609.
70. Fearon E.R., Vogelstein B. A genetic model for colorectal tumorigenesis. Cell 1990, 61:759-767.
71. Desper R., Jiang F., Kallioniemi O.P., Moch H., Papadimitriou C.H., Schaffer A.A. Inferring tree models for oncogenesis from comparative genome hybridization data. J. Comput. Biol. 1999, 6:37-51.
72. Beerenwinkel N., Rahnenfuhrer J., Daumer M., Hoffmann D., Kaiser R., Selbig J., Lengauer T. Learning multiple evolutionary pathways from cross-sectional data. J. Comput. Biol. 2005, 12:584-598.
73. Cheng Y.K., Beroukhim R., Levine R.L., Mellinghoff I.K., Holland E.C., Michor F. A mathematical methodology for determining the temporal order of pathway alterations arising during gliomagenesis. PLoS Comput. Biol. 2012, 8:e1002337.
74. Mazzarella L., Riva L., Luzi L., Ronchini C., Pelicci P.G. The genomic and epigenomic landscapes of AML. Semin. Hematol. 2014, 51:259-272.
75. Welch J.S., Ley T.J., Link D.C., Miller C.A., Larson D.E., Koboldt D.C., Wartman L.D., Lamprecht T.L., Liu F., Xia J., Kandoth C., Fulton R.S., McLellan M.D., Dooling D.J., Wallis J.W., Chen K., Harris C.C., Schmidt H.K., Kalicki-Veizer J.M., Lu C., Zhang Q., Lin L., O'Laughlin M.D., McMichael J.F., Delehaunty K.D., Fulton L.A., Magrini V.J., McGrath S.D., Demeter R.T., Vickery T.L., Hundal J., Cook L.L., Swift G.W., Reed J.P., Alldredge P.A., Wylie T.N., Walker J.R., Watson M.A., Heath S.E., Shannon W.D., Varghese N., Nagarajan R., Payton J.E., Baty J.D., Kulkarni S., Klco J.M., Tomasson M.H., Westervelt P., Walter M.J., Graubert T.A., DiPersio J.F., Ding L., Mardis E.R., Wilson R.K. The origin and evolution of mutations in acute myeloid leukemia. Cell 2012, 150:264-278.
76. Welch J.S. Mutation position within evolutionary subclonal architecture in AML. Semin. Hematol. 2014, 51:273-281.
77. Klco J.M., Spencer D.H., Miller C.A., Griffith M., Lamprecht T.L., O'Laughlin M., Fronick C., Magrini V., Demeter R.T., Fulton R.S., Eades W.C., Link D.C., Graubert T.A., Walter M.J., Mardis E.R., Dipersio J.F., Wilson R.K., Ley T.J. Functional heterogeneity of genetically defined subclones in acute myeloid leukemia. Cancer Cell 2014, 25:379-392.
78. Walter M.J., Shen D., Ding L., Shao J., Koboldt D.C., Chen K., Larson D.E., McLellan M.D., Dooling D., Abbott R., Fulton R., Magrini V., Schmidt H., Kalicki-Veizer J., O'Laughlin M., Fan X., Grillot M., Witowski S., Heath S., Frater J.L., Eades W., Tomasson M., Westervelt P., DiPersio J.F., Link D.C., Mardis E.R., Ley T.J., Wilson R.K., Graubert T.A. Clonal architecture of secondary acute myeloid leukemia. N. Engl. J. Med. 2012, 366:1090-1098.
79. Walter M.J., Shen D., Shao J., Ding L., White B.S., Kandoth C., Miller C.A., Niu B., McLellan M.D., Dees N.D., Fulton R., Elliot K., Heath S., Grillot M., Westervelt P., Link D.C., DiPersio J.F., Mardis E., Ley T.J., Wilson R.K., Graubert T.A. Clonal diversity of recurrently mutated genes in myelodysplastic syndromes. Leukemia 2013, 27:1275-1282.
80. Wong T.N., Ramsingh G., Young A.L., Miller C.A., Touma W., Welch J.S., Lamprecht T.L., Shen D., Hundal J., Fulton R.S., Heath S., Baty J.D., Klco J.M., Ding L., Mardis E.R., Westervelt P., DiPersio J.F., Walter M.J., Graubert T.A., Ley T.J., Druley T.E., Link D.C., Wilson R.K. Role of TP53 mutations in the origin and evolution of therapy-related acute myeloid leukaemia. Nature 2015, 518:552-555.
81. Genovese G., Kahler A.K., Handsaker R.E., Lindberg J., Rose S.A., Bakhoum S.F., Chambert K., Mick E., Neale B.M., Fromer M., Purcell S.M., Svantesson O., Landen M., Hoglund M., Lehmann S., Gabriel S.B., Moran J.L., Lander E.S., Sullivan P.F., Sklar P., Gronberg H., Hultman C.M., McCarroll S.A. Clonal hematopoiesis and blood-cancer risk inferred from blood DNA sequence. N. Engl. J. Med. 2014, 371:2477-2487.
82. Jaiswal S., Fontanillas P., Flannick J., Manning A., Grauman P.V., Mar B.G., Lindsley R.C., Mermel C.H., Burtt N., Chavez A., Higgins J.M., Moltchanov V., Kuo F.C., Kluk M.J., Henderson B., Kinnunen L., Koistinen H.A., Ladenvall C., Getz G., Correa A., Banahan B.F., Gabriel S., Kathiresan S., Stringham H.M., McCarthy M.I., Boehnke M., Tuomilehto J., Haiman C., Groop L., Atzmon G., Wilson J.G., Neuberg D., Altshuler D., Ebert B.L. Age-related clonal hematopoiesis associated with adverse outcomes. N. Engl. J. Med. 2014, 371:2488-2498.
83. Papaemmanuil E., Gerstung M., Malcovati L., Tauro S., Gundem G., Van Loo P., Yoon C.J., Ellis P., Wedge D.C., Pellagatti A., Shlien A., Groves M.J., Forbes S.A., Raine K., Hinton J., Mudie L.J., McLaren S., Hardy C., Latimer C., Della Porta M.G., O'Meara S., Ambaglio I., Galli A., Butler A.P., Walldin G., Teague J.W., Quek L., Sternberg A., Gambacorti-Passerini C., Cross N.C., Green A.R., Boultwood J., Vyas P., Hellstrom-Lindberg E., Bowen D., Cazzola M., Stratton M.R., Campbell P.J., C.Chronic Myeloid Disorders Working Group of the International Cancer Genome Clinical and biological implications of driver mutations in myelodysplastic syndromes. Blood 2013, 122:3616-3627. (quiz 3699).
84. Melchor L., Brioli A., Wardell C.P., Murison A., Potter N.E., Kaiser M.F., Fryer R.A., Johnson D.C., Begum D.B., Hulkki Wilson S., Vijayaraghavan G., Titley I., Cavo M., Davies F.E., Walker B.A., Morgan G.J. Single-cell genetic analysis reveals the composition of initiating clones and phylogenetic patterns of branching and parallel evolution in myeloma. Leukemia 2014, 28:1705-1715.
85. Bohn O.L., Hsu K., Hyman D.M., Pignataro D.S., Giralt S., Teruya-Feldstein J. BRAF V600E mutation and clonal evolution in a patient with relapsed refractory myeloma with plasmablastic differentiation. Clin. Lymphoma Myeloma Leuk. 2014, 14:e65-e68.
86. Green M.R., Gentles A.J., Nair R.V., Irish J.M., Kihira S., Liu C.L., Kela I., Hopmans E.S., Myklebust J.H., Ji H., Plevritis S.K., Levy R., Alizadeh A.A. Hierarchy in somatic mutations arising during genomic evolution and progression of follicular lymphoma. Blood 2013, 121:1604-1611.
87. Bodor C., Grossmann V., Popov N., Okosun J., O'Riain C., Tan K., Marzec J., Araf S., Wang J., Lee A.M., Clear A., Montoto S., Matthews J., Iqbal S., Rajnai H., Rosenwald A., Ott G., Campo E., Rimsza L.M., Smeland E.B., Chan W.C., Braziel R.M., Staudt L.M., Wright G., Lister T.A., Elemento O., Hills R., Gribben J.G., Chelala C., Matolcsy A., Kohlmann A., Haferlach T., Gascoyne R.D., Fitzgibbon J. EZH2 mutations are frequent and represent an early event in follicular lymphoma. Blood 2013, 122:3165-3168.
88. Okosun J., Bodor C., Wang J., Araf S., Yang C.Y., Pan C., Boller S., Cittaro D., Bozek M., Iqbal S., Matthews J., Wrench D., Marzec J., Tawana K., Popov N., O'Riain C., O'Shea D., Carlotti E., Davies A., Lawrie C.H., Matolcsy A., Calaminici M., Norton A., Byers R.J., Mein C., Stupka E., Lister T.A., Lenz G., Montoto S., Gribben J.G., Fan Y., Grosschedl R., Chelala C., Fitzgibbon J. Integrated genomic analysis identifies recurrent mutations and evolution patterns driving the initiation and progression of follicular lymphoma. Nat. Genet. 2014, 46:176-181.
89. Bai H., Wang Z., Wang Y., Zhuo M., Zhou Q., Duan J., Yang L., Wu M., An T., Zhao J., Wang J. Detection and clinical significance of intratumoral EGFR mutational heterogeneity in Chinese patients with advanced non-small cell lung cancer. PLoS ONE 2013, 8:e54170.
90. Chen Z.Y., Zhong W.Z., Zhang X.C., Su J., Yang X.N., Chen Z.H., Yang J.J., Zhou Q., Yan H.H., An S.J., Chen H.J., Jiang B.Y., Mok T.S., Wu Y.L. EGFR mutation heterogeneity and the mixed response to EGFR tyrosine kinase inhibitors of lung adenocarcinomas. Oncologist 2012, 17:978-985.
91. Yatabe Y., Matsuo K., Mitsudomi T. Heterogeneous distribution of EGFR mutations is extremely rare in lung adenocarcinoma. J. Clin. Oncol. 2011, 29:2972-2977.
92. Katayama R., Shaw A.T., Khan T.M., Mino-Kenudson M., Solomon B.J., Halmos B., Jessop N.A., Wain J.C., Yeo A.T., Benes C., Drew L., Saeh J.C., Crosby K., Sequist L.V., Iafrate A.J., Engelman J.A. Mechanisms of acquired crizotinib resistance in ALK-rearranged lung Cancers. Sci. Transl. Med. 2012, 4:120ra117.
93. Su K.Y., Chen H.Y., Li K.C., Kuo M.L., Yang J.C., Chan W.K., Ho B.C., Chang G.C., Shih J.Y., Yu S.L., Yang P.C. Pretreatment epidermal growth factor receptor (EGFR) T790M mutation predicts shorter EGFR tyrosine kinase inhibitor response duration in patients with non-small-cell lung cancer. J. Clin. Oncol. 2012, 30:433-440.
94. Pollock P.M., Harper U.L., Hansen K.S., Yudt L.M., Stark M., Robbins C.M., Moses T.Y., Hostetter G., Wagner U., Kakareka J., Salem G., Pohida T., Heenan P., Duray P., Kallioniemi O., Hayward N.K., Trent J.M., Meltzer P.S. High frequency of BRAF mutations in nevi. Nat. Genet. 2003, 33:19-20.
95. Poynter J.N., Elder J.T., Fullen D.R., Nair R.P., Soengas M.S., Johnson T.M., Redman B., Thomas N.E., Gruber S.B. BRAF and NRAS mutations in melanoma and melanocytic nevi. Melanoma Res. 2006, 16:267-273.
96. Lin J., Goto Y., Murata H., Sakaizawa K., Uchiyama A., Saida T., Takata M. Polyclonality of BRAF mutations in primary melanoma and the selection of mutant alleles during progression. Br. J. Cancer 2011, 104:464-468.
97. Yancovitz M., Litterman A., Yoon J., Ng E., Shapiro R.L., Berman R.S., Pavlick A.C., Darvishian F., Christos P., Mazumdar M., Osman I., Polsky D. Intra- and inter-tumor heterogeneity of BRAF(V600E) mutations in primary and metastatic melanoma. PLoS ONE 2012, 7:e29336.
98. Nazarian R., Shi H., Wang Q., Kong X., Koya R.C., Lee H., Chen Z., Lee M.K., Attar N., Sazegar H., Chodon T., Nelson S.F., McArthur G., Sosman J.A., Ribas A., Lo R.S. Melanomas acquire resistance to B-RAF(V600E) inhibition by RTK or N-RAS upregulation. Nature 2010, 468:973-977.
99. Fecher L.A., Cummings S.D., Keefe M.J., Alani R.M. Toward a molecular classification of melanoma. J. Clin. Oncol. 2007, 25:1606-1620.
100. Van Allen E.M., Wagle N., Sucker A., Treacy D.J., Johannessen C.M., Goetz E.M., Place C.S., Taylor-Weiner A., Whittaker S., Kryukov G.V., Hodis E., Rosenberg M., McKenna A., Cibulskis K., Farlow D., Zimmer L., Hillen U., Gutzmer R., Goldinger S.M., Ugurel S., Gogas H.J., Egberts F., Berking C., Trefzer U., Loquai C., Weide B., Hassel J.C., Gabriel S.B., Carter S.L., Getz G., Garraway L.A., Schadendorf D. Dermatologic Cooperative Oncology Group of Germany. The genetic landscape of clinical resistance to RAF inhibition in metastatic melanoma. Cancer Discov. 2014, 4:94-109.
101. Shi H., Hugo W., Kong X., Hong A., Koya R.C., Moriceau G., Chodon T., Guo R., Johnson D.B., Dahlman K.B., Kelley M.C., Kefford R.F., Chmielowski B., Glaspy J.A., Sosman J.A., van Baren N., Long G.V., Ribas A., Lo R.S. Acquired resistance and clonal evolution in melanoma during BRAF inhibitor therapy. Cancer Discov. 2014, 4:80-93.
102. Somasundaram R., Herlyn M. Relapse of melanoma after successful adoptive T-cell therapy: escape through inflammation-induced phenotypic melanoma cell plasticity. Pigment Cell Melanoma Res. 2013, 26:2-4.
103. Prandi D., Baca S.C., Romanel A., Barbieri C.E., Mosquera J.M., Fontugne J., Beltran H., Sboner A., Garraway L.A., Rubin M.A., Demichelis F. Unraveling the clonal hierarchy of somatic genomic aberrations. Genome Biol. 2014, 15:439.
104. Wang S.S., Gu Y.F., Wolff N., Stefanius K., Christie A., Dey A., Hammer R.E., Xie X.J., Rakheja D., Pedrosa I., Carroll T., McKay R.M., Kapur P., Brugarolas J. Bap1 is essential for kidney function and cooperates with Vhl in renal tumorigenesis. Proc. Natl. Acad. Sci. U. S. A. 2014, 111:16538-16543.
105. Sankin A., Hakimi A.A., Mikkilineni N., Ostrovnaya I., Silk M.T., Liang Y., Mano R., Chevinsky M., Motzer R.J., Solomon S.B., Cheng E.H., Durack J.C., Coleman J.A., Russo P., Hsieh J.J. The impact of genetic heterogeneity on biomarker development in kidney cancer assessed by multiregional sampling. Cancer Med. 2014, 3:1485-1492.
106. Voss M.H., Hakimi A.A., Pham C.G., Brannon A.R., Chen Y.B., Cunha L.F., Akin O., Liu H., Takeda S., Scott S.N., Socci N.D., Viale A., Schultz N., Sander C., Reuter V.E., Russo P., Cheng E.H., Motzer R.J., Berger M.F., Hsieh J.J. Tumor genetic analyses of patients with metastatic renal cell carcinoma and extended benefit from mTOR inhibitor therapy. Clin. Cancer Res. 2014, 20:1955-1964.
107. Kanu N., Gronroos E., Martinez P., Burrell R.A., Yi Goh X., Bartkova J., Maya-Mendoza A., Mistrik M., Rowan A.J., Patel H., Rabinowitz A., East P., Wilson G., Santos C.R., McGranahan N., Gulati S., Gerlinger M., Birkbak N.J., Joshi T., Alexandrov L.B., Stratton M.R., Powles T., Matthews N., Bates P.A., Stewart A., Szallasi Z., Larkin J., Bartek J., Swanton C. SETD2 loss-of-function promotes renal cancer branched evolution through replication stress and impaired DNA repair. Oncogene 2015, (Epub ahead of print). 10.1038/onc.2015.24.
108. Snuderl M., Fazlollahi L., Le L.P., Nitta M., Zhelyazkova B.H., Davidson C.J., Akhavanfard S., Cahill D.P., Aldape K.D., Betensky R.A., Louis D.N., Iafrate A.J. Mosaic amplification of multiple receptor tyrosine kinase genes in glioblastoma. Cancer Cell 2011, 20:810-817.
109. Szerlip N.J., Pedraza A., Chakravarty D., Azim M., McGuire J., Fang Y., Ozawa T., Holland E.C., Huse J.T., Jhanwar S., Leversha M.A., Mikkelsen T., Brennan C.W. Intratumoral heterogeneity of receptor tyrosine kinases EGFR and PDGFRA amplification in glioblastoma defines subpopulations with distinct growth factor response. Proc. Natl. Acad. Sci. U. S. A. 2012, 109:3041-3046.
110. Francis J.M., Zhang C.Z., Maire C.L., Jung J., Manzo V.E., Adalsteinsson V.A., Homer H., Haidar S., Blumenstiel B., Pedamallu C.S., Ligon A.H., Love J.C., Meyerson M., Ligon K.L. EGFR variant heterogeneity in glioblastoma resolved through single-nucleus sequencing. Cancer Discov. 2014, 4:956-971.
111. Jones S., Chen W.D., Parmigiani G., Diehl F., Beerenwinkel N., Antal T., Traulsen A., Nowak M.A., Siegel C., Velculescu V.E., Kinzler K.W., Vogelstein B., Willis J., Markowitz S.D. Comparative lesion sequencing provides insights into tumor evolution. Proc. Natl. Acad. Sci. U. S. A. 2008, 105:4283-4288.
112. Brannon A., Vakiani E., Sylvester B.E., Scott S.N., McDermott G., Shah R.H., Kania K., Viale A., Oschwald D.M., Vacic V., Emde A.K., Cercek A., Yaeger R., Kemeny N.E., Saltz L.B., Shia J., Graham D.M., Weiser M.R., Solit D.B., Berger M.F. Comparative sequencing analysis reveals high genomic concordance between matched primary and metastatic colorectal cancer lesions. Genome Biol. 2014, 15:454.
113. Donna M.A., Graham M., Sukhai Mahadeo A., Letourneau Louis, Karimzadeh Mehran, Zhang Tong, Thomas Mariam, Roehrl Michael H.A., Xueyu Chen Eric, Krzyzanowska Monika K., Moore Malcolm J., Giesler Amanda, Yu Celeste, Bedard Philippe L., Kamel-Reid Suzanne, Siu Lillian L., Riazalhosseini Yasser Analysis of clonal evolution in colorectal cancer. J. Clin. Oncol. 2014, 32(5s).
114. Diaz L.A., Williams R.T., Wu J., Kinde I., Hecht J.R., Berlin J., Allen B., Bozic I., Reiter J.G., Nowak M.A., Kinzler K.W., Oliner K.S., Vogelstein B. The molecular evolution of acquired resistance to targeted EGFR blockade in colorectal cancers. Nature 2012, 486:537-540.
115. Greenman C.D., Pleasance E.D., Newman S., Yang F., Fu B., Nik-Zainal S., Jones D., Lau K.W., Carter N., Edwards P.A., Futreal P.A., Stratton M.R., Campbell P.J. Estimation of rearrangement phylogeny for cancer genomes. Genome Res. 2012, 22:346-361.
116. N.Cancer Genome Atlas Research Integrated genomic analyses of ovarian carcinoma. Nature 2011, 474:609-615.
117. Jamal-Hanjani M., Hackshaw A., Ngai Y., Shaw J., Dive C., Quezada S., Middleton G., de Bruin E., Le Quesne J., Shafi S., Falzon M., Horswell S., Blackhall F., Khan I., Janes S., Nicolson M., Lawrence D., Forster M., Fennell D., Lee S.M., Lester J., Kerr K., Muller S., Iles N., Smith S., Murugaesu N., Mitter R., Salm M., Stuart A., Matthews N., Adams H., Ahmad T., Attanoos R., Bennett J., Birkbak N.J., Booton R., Brady G., Buchan K., Capitano A., Chetty M., Cobbold M., Crosbie P., Davies H., Denison A., Djearman M., Goldman J., Haswell T., Joseph L., Kornaszewska M., Krebs M., Langman G., MacKenzie M., Millar J., Morgan B., Naidu B., Nonaka D., Peggs K., Pritchard C., Remmen H., Rowan A., Shah R., Smith E., Summers Y., Taylor M., Veeriah S., Waller D., Wilcox B., Wilcox M., Woolhouse I., McGranahan N., Swanton C. Tracking genomic cancer evolution for precision medicine: The Lung TRACERx Study. PLoS Biol. 2014, 12:e1001906.
118. Rivlin N., Brosh R., Oren M., Rotter V. Mutations in the p53 tumor suppressor gene: important milestones at the various steps of tumorigenesis. Genes Cancer 2011, 2:466-474.
119. Marusyk A., Almendro V., Polyak K. Intra-tumour heterogeneity: a looking glass for cancer?. Nat. Rev. Cancer 2012, 12:323-334.