Molecular pathology in real time

Cancer and Metastasis Reviews

Volumn 35, Issue 1, 2016, Pages 129-140

  Ryška, Aleš ^a  

^a CHARLES UNIVERSITY   (Czech Republic)

Author keywords

Evolution; Limitation; Liquid biopsy; Molecular pathology; Predictive marker; Resistance; Targeted therapy; Tumor heterogeneity

Indexed keywords

ARTICLE; BREAST CANCER; CIRCULATING TUMOR CELL; COLORECTAL CANCER; ENDOSCOPIC BIOPSY; HUMAN; MALIGNANT NEOPLASTIC DISEASE; MOLECULAR PATHOLOGY; NEEDLE BIOPSY; NON SMALL CELL LUNG CANCER; PHENOTYPE; PRIMARY TUMOR; PRIORITY JOURNAL; STOMACH CANCER; SYSTEMIC THERAPY; TREATMENT FAILURE; TUMOR BIOPSY; TUMOR VOLUME; GENETIC HETEROGENEITY; GENETICS; NEOPLASMS; PATHOLOGY; PROCEDURES; TUMOR EMBOLISM;

DNA; TUMOR MARKER;

BIOMARKERS, TUMOR; DNA, NEOPLASM; GENETIC HETEROGENEITY; HUMANS; NEOPLASMS; NEOPLASTIC CELLS, CIRCULATING; PATHOLOGY, MOLECULAR;

EID: 84959386597     PISSN: 01677659     EISSN: 15737233     Source Type: Journal    
DOI: 10.1007/s10555-016-9607-3     Document Type: Article

References (112)

1. Burrell, R. A., & Swanton, C. (2014). Tumour heterogeneity and the evolution of polyclonal drug resistance. Molecular Oncology, 8(6), 1095–1111. doi:10.1016/j.molonc.2014.06.005.
2. Swanton, C. (2012). Intratumor heterogeneity: evolution through space and time. Cancer Research, 72(19), 4875–4882. doi:10.1158/0008-5472.can-12-2217.
3. Gerlinger, M., & Swanton, C. (2010). How Darwinian models inform therapeutic failure initiated by clonal heterogeneity in cancer medicine. British Journal of Cancer, 103(8), 1139–1143. doi:10.1038/sj.bjc.6605912.
4. Gerlinger, M., Rowan, A. J., Horswell, S., Larkin, J., Endesfelder, D., Gronroos, E., et al. (2012). Intratumor heterogeneity and branched evolution revealed by multiregion sequencing. New England Journal of Medicine, 366(10), 883–892. doi:10.1056/NEJMoa1113205.
5. Sighoko, D., Liu, J., Hou, N., Gustafson, P., & Huo, D. (2014). Discordance in hormone receptor status among primary, metastatic, and second primary breast cancers: biological difference or misclassification? The Oncologist, 19(6), 592–601. doi:10.1634/theoncologist.2013-0427.
6. Santinelli, A., Pisa, E., Stramazzotti, D., & Fabris, G. (2008). HER-2 status discrepancy between primary breast cancer and metastatic sites. Impact on target therapy. International Journal of Cancer, 122(5), 999–1004. doi:10.1002/ijc.23051.
7. Bachmann, C., Grischke, E. M., Fehm, T., Staebler, A., Schittenhelm, J., & Wallwiener, D. (2013). CNS metastases of breast cancer show discordant immunohistochemical phenotype compared to primary. Journal of Cancer Research and Clinical Oncology, 139(4), 551–556. doi:10.1007/s00432-012-1358-0.
8. Houssami, N., Macaskill, P., Balleine, R. L., Bilous, M., & Pegram, M. D. (2011). HER2 discordance between primary breast cancer and its paired metastasis: tumor biology or test artefact? Insights through meta-analysis. Breast Cancer Research and Treatment, 129(3), 659–674. doi:10.1007/s10549-011-1632-x.
9. Mittendorf, E. A., Wu, Y., Scaltriti, M., Meric-Bernstam, F., Hunt, K. K., Dawood, S., et al. (2009). Loss of HER2 amplification following trastuzumab-based neoadjuvant systemic therapy and survival outcomes. Clinical Cancer Research, 15(23), 7381–7388. doi:10.1158/1078-0432.ccr-09-1735.
10. Guarneri, V., Dieci, M. V., Barbieri, E., Piacentini, F., Omarini, C., Ficarra, G., et al. (2013). Loss of HER2 positivity and prognosis after neoadjuvant therapy in HER2-positive breast cancer patients. Annals of Oncology, 24(12), 2990–2994. doi:10.1093/annonc/mdt364.
11. Sekido, Y., Umemura, S., Takekoshi, S., Suzuki, Y., Tokuda, Y., Tajima, T., et al. (2003). Heterogeneous gene alterations in primary breast cancer contribute to discordance between primary and asynchronous metastatic/recurrent sites: HER2 gene amplification and p53 mutation. International Journal of Oncology, 22(6), 1225–1232.
12. Aurilio, G., Disalvatore, D., Pruneri, G., Bagnardi, V., Viale, G., Curigliano, G., et al. (2014). A meta-analysis of oestrogen receptor, progesterone receptor and human epidermal growth factor receptor 2 discordance between primary breast cancer and metastases. European Journal of Cancer, 50(2), 277–289. doi:10.1016/j.ejca.2013.10.004.
13. Kalkman, S., Barentsz, M. W., & van Diest, P. J. (2014). The effects of under 6 hours of formalin fixation on hormone receptor and HER2 expression in invasive breast cancer: a systematic review. American Journal of Clinical Pathology, 142(1), 16–22. doi:10.1309/ajcp96ydqstybxwu.
14. Khoury, T., Sait, S., Hwang, H., Chandrasekhar, R., Wilding, G., Tan, D., et al. (2009). Delay to formalin fixation effect on breast biomarkers. Modern Pathology, 22(11), 1457–1467. doi:10.1038/modpathol.2009.117.
15. Nofech-Mozes, S., Vella, E. T., Dhesy-Thind, S., Hagerty, K. L., Mangu, P. B., Temin, S., et al. (2012). Systematic review on hormone receptor testing in breast cancer. Applied Immunohistochemistry and Molecular Morphology, 20(3), 214–263. doi:10.1097/PAI.0b013e318234aa12.
16. Qiu, J., Kulkarni, S., Chandrasekhar, R., Rees, M., Hyde, K., Wilding, G., et al. (2010). Effect of delayed formalin fixation on estrogen and progesterone receptors in breast cancer: a study of three different clones. American Journal of Clinical Pathology, 134(5), 813–819. doi:10.1309/ajcpvcx83jwmsbno.
17. Tong, L. C., Nelson, N., Tsourigiannis, J., & Mulligan, A. M. (2011). The effect of prolonged fixation on the immunohistochemical evaluation of estrogen receptor, progesterone receptor, and HER2 expression in invasive breast cancer: a prospective study. The American Journal of Surgical Pathology, 35(4), 545–552. doi:10.1097/PAS.0b013e31820e6237.
18. Uy, G. B., Laudico, A. V., Carnate, J. M., Jr., Lim, F. G., Fernandez, A. M., Rivera, R. R., et al. (2010). Breast cancer hormone receptor assay results of core needle biopsy and modified radical mastectomy specimens from the same patients. Clinical Breast Cancer, 10(2), 154–159. doi:10.3816/CBC.2010.n.021.
19. Yildiz-Aktas, I. Z., Dabbs, D. J., & Bhargava, R. (2012). The effect of cold ischemic time on the immunohistochemical evaluation of estrogen receptor, progesterone receptor, and HER2 expression in invasive breast carcinoma. Modern Pathology, 25(8), 1098–1105. doi:10.1038/modpathol.2012.59.
20. Huang, S. C., Ng, K. F., Lee, S. E., Chen, K. H., Yeh, T. S., & Chen, T. C. (2014). HER2 testing in paired biopsy and excision specimens of gastric cancer: the reliability of the scoring system and the clinicopathological factors relevant to discordance. Gastric Cancer. doi:10.1007/s10120-014-0453-0.
21. Bang, Y. J., Van Cutsem, E., Feyereislova, A., Chung, H. C., Shen, L., Sawaki, A., et al. (2010). Trastuzumab in combination with chemotherapy versus chemotherapy alone for treatment of HER2-positive advanced gastric or gastro-oesophageal junction cancer (ToGA): a phase 3, open-label, randomised controlled trial. Lancet, 376(9742), 687–697. doi:10.1016/S0140-6736(10)61121-X.
22. Yan, B., Yau, E. X., Choo, S. N., Ong, C. W., Yong, K. J., Pang, B., et al. (2011). Dual-colour HER2/chromosome 17 chromogenic in situ hybridisation assay enables accurate assessment of HER2 genomic status in gastric cancer and has potential utility in HER2 testing of biopsy samples. Journal of Clinical Pathology, 64(10), 880–883. doi:10.1136/jclinpath-2011-200009.
23. Ruschoff, J., Dietel, M., Baretton, G., Arbogast, S., Walch, A., Monges, G., et al. (2010). HER2 diagnostics in gastric cancer-guideline validation and development of standardized immunohistochemical testing. Virchows Archiv, 457(3), 299–307. doi:10.1007/s00428-010-0952-2.
24. Warneke, V. S., Behrens, H. M., Boger, C., Becker, T., Lordick, F., Ebert, M. P., et al. (2013). Her2/neu testing in gastric cancer: evaluating the risk of sampling errors. Annals of Oncology, 24(3), 725–733. doi:10.1093/annonc/mds528.
25. Watson, S., Validire, P., Cervera, P., Zorkani, N., Scriva, A., Lemay, F., et al. (2013). Combined HER2 analysis of biopsies and surgical specimens to optimize detection of trastuzumab-eligible patients in eso-gastric adenocarcinoma: a GERCOR study. Annals of Oncology, 24(12), 3035–3039. doi:10.1093/annonc/mdt393.
26. Kimura, M., Tsuda, H., Morita, D., Shinto, E., Tanimoto, T., Ichikura, T., et al. (2005). Usefulness and limitation of multiple endoscopic biopsy sampling for epidermal growth factor receptor and c-erbB-2 testing in patients with gastric adenocarcinoma. Japanese Journal of Clinical Oncology, 35(6), 324–331. doi:10.1093/jjco/hyi089.
27. Gumusay, O., Benekli, M., Ekinci, O., Baykara, M., Ozet, A., Coskun, U., et al. (2015). Discordances in HER2 status between primary gastric cancer and corresponding metastatic sites. Japanese Journal of Clinical Oncology, 45(5), 416–421. doi:10.1093/jjco/hyv020.
28. Selcukbiricik, F., Erdamar, S., Buyukunal, E., Serrdengecti, S., & Demirelli, F. (2014). Is her-2 status in the primary tumor correlated with matched lymph node metastases in patients with gastric cancer undergoing curative gastrectomy? Asian Pacific Journal of Cancer Prevention, 15(24), 10607–10611.
29. Yan, B., Yau, E. X., Bte Omar, S. S., Ong, C. W., Pang, B., Yeoh, K. G., et al. (2010). A study of HER2 gene amplification and protein expression in gastric cancer. Journal of Clinical Pathology, 63(9), 839–842. doi:10.1136/jcp.2010.076570.
30. Liang, J. W., Zhang, J. J., Zhang, T., & Zheng, Z. C. (2014). Clinicopathological and prognostic significance of HER2 overexpression in gastric cancer: a meta-analysis of the literature. Tumour Biology, 35(5), 4849–4858. doi:10.1007/s13277-014-1636-3.
31. Gomez-Martin, C., Plaza, J. C., Pazo-Cid, R., Salud, A., Pons, F., Fonseca, P., et al. (2013). Level of HER2 gene amplification predicts response and overall survival in HER2-positive advanced gastric cancer treated with trastuzumab. Journal of Clinical Oncology, 31(35), 4445–4452. doi:10.1200/JCO.2013.48.9070.
32. Ieni, A., Barresi, V., Caltabiano, R., Caleo, A., Bonetti, L. R., Lanzafame, S., et al. (2014). Discordance rate of HER2 status in primary gastric carcinomas and synchronous lymph node metastases: a multicenter retrospective analysis. International Journal of Molecular Sciences, 15(12), 22331–22341. doi:10.3390/ijms151222331.
33. Blanco-Calvo, M., Concha, A., Figueroa, A., Garrido, F., & Valladares-Ayerbes, M. (2015). Colorectal cancer classification and cell heterogeneity: a systems oncology approach. International Journal of Molecular Sciences, 16(6), 13610–13632. doi:10.3390/ijms160613610.
34. Pino, M. S., & Chung, D. C. (2010). The chromosomal instability pathway in colon cancer. Gastroenterology, 138(6), 2059–2072. doi:10.1053/j.gastro.2009.12.065.
35. Leggett, B., & Whitehall, V. (2010). Role of the serrated pathway in colorectal cancer pathogenesis. Gastroenterology, 138(6), 2088–2100. doi:10.1053/j.gastro.2009.12.066.
36. Pinheiro, M., Pinto, C., Peixoto, A., Veiga, I., Lopes, P., Henrique, R., et al. (2015). Target gene mutational pattern in Lynch syndrome colorectal carcinomas according to tumour location and germline mutation. British Journal of Cancer, 113(4), 686–692. doi:10.1038/bjc.2015.281.
37. Chen, J., Etzel, C. J., Amos, C. I., Zhang, Q., Viscofsky, N., Lindor, N. M., et al. (2009). Genetic variants in the cell cycle control pathways contribute to early onset colorectal cancer in Lynch syndrome. Cancer Causes & Control, 20(9), 1769–1777. doi:10.1007/s10552-009-9416-x.
38. Martin-Lopez, J. V., & Fishel, R. (2013). The mechanism of mismatch repair and the functional analysis of mismatch repair defects in Lynch syndrome. Familial Cancer, 12(2), 159–168. doi:10.1007/s10689-013-9635-x.
39. Poulogiannis, G., Frayling, I. M., & Arends, M. J. (2010). DNA mismatch repair deficiency in sporadic colorectal cancer and Lynch syndrome. Histopathology, 56(2), 167–179. doi:10.1111/j.1365-2559.2009.03392.x.
40. Barana, D., van der Klift, H., Wijnen, J., Longa, E. D., Radice, P., Cetto, G. L., et al. (2004). Spectrum of genetic alterations in Muir-Torre syndrome is the same as in HNPCC. American Journal of Medical Genetics. Part A, 125A(3), 318–319. doi:10.1002/ajmg.a.20523.
41. Kruse, R., Rutten, A., Lamberti, C., Hosseiny-Malayeri, H. R., Wang, Y., Ruelfs, C., et al. (1998). Muir-Torre phenotype has a frequency of DNA mismatch-repair-gene mutations similar to that in hereditary nonpolyposis colorectal cancer families defined by the Amsterdam criteria. American Journal of Human Genetics, 63(1), 63–70. doi:10.1086/301926.
42. Suspiro, A., Fidalgo, P., Cravo, M., Albuquerque, C., Ramalho, E., Leitao, C. N., et al. (1998). The Muir-Torre syndrome: a rare variant of hereditary nonpolyposis colorectal cancer associated with hMSH2 mutation. The American Journal of Gastroenterology, 93(9), 1572–1574. doi:10.1111/j.1572-0241.1998.00487.x.
43. Bapat, B., Xia, L., Madlensky, L., Mitri, A., Tonin, P., Narod, S. A., et al. (1996). The genetic basis of Muir-Torre syndrome includes the hMLH1 locus. American Journal of Human Genetics, 59(3), 736–739.
44. Kacerovska, D., Kazakov, D. V., Cerna, K., Hadravsky, L., Michal, M., Jr., Dostal, J., et al. (2010). Muir-Torre syndrome—a phenotypic variant of Lynch syndrome. Ceskoslovenská Patologie, 46(4), 86–94.
45. Greenson, J. K., Bonner, J. D., Ben-Yzhak, O., Cohen, H. I., Miselevich, I., Resnick, M. B., et al. (2003). Phenotype of microsatellite unstable colorectal carcinomas: well-differentiated and focally mucinous tumors and the absence of dirty necrosis correlate with microsatellite instability. The American Journal of Surgical Pathology, 27(5), 563–570.
46. Kocarnik, J. M., Shiovitz, S., & Phipps, A. I. (2015). Molecular phenotypes of colorectal cancer and potential clinical applications. Gastroenterol Report (Oxf), 3(4), 269–276. doi:10.1093/gastro/gov046.
47. Lievre, A., Bachet, J. B., Boige, V., Cayre, A., Le Corre, D., Buc, E., et al. (2008). KRAS mutations as an independent prognostic factor in patients with advanced colorectal cancer treated with cetuximab. Journal of Clinical Oncology, 26(3), 374–379. doi:10.1200/JCO.2007.12.5906.
48. Lievre, A., Bachet, J. B., Le Corre, D., Boige, V., Landi, B., Emile, J. F., et al. (2006). KRAS mutation status is predictive of response to cetuximab therapy in colorectal cancer. Cancer Research, 66(8), 3992–3995. doi:10.1158/0008-5472.CAN-06-0191.
49. Schubbert, S., Shannon, K., & Bollag, G. (2007). Hyperactive Ras in developmental disorders and cancer. Nature Reviews. Cancer, 7(4), 295–308. doi:10.1038/nrc2109.
50. Baas, J. M., Krens, L. L., Guchelaar, H. J., Morreau, H., & Gelderblom, H. (2011). Concordance of predictive markers for EGFR inhibitors in primary tumors and metastases in colorectal cancer: a review. The Oncologist, 16(9), 1239–1249. doi:10.1634/theoncologist.2011-0024.
51. Vignot, S., Lefebvre, C., Frampton, G. M., Meurice, G., Yelensky, R., Palmer, G., et al. (2015). Comparative analysis of primary tumour and matched metastases in colorectal cancer patients: evaluation of concordance between genomic and transcriptional profiles. European Journal of Cancer, 51(7), 791–799. doi:10.1016/j.ejca.2015.02.012.
52. Santini, D., Loupakis, F., Vincenzi, B., Floriani, I., Stasi, I., Canestrari, E., et al. (2008). High concordance of KRAS status between primary colorectal tumors and related metastatic sites: implications for clinical practice. The Oncologist, 13(12), 1270–1275. doi:10.1634/theoncologist.2008-0181.
53. Siyar Ekinci, A., Demirci, U., Cakmak Oksuzoglu, B., Ozturk, A., Esbah, O., Ozatli, T., et al. (2015). KRAS discordance between primary and metastatic tumor in patients with metastatic colorectal carcinoma. Journal of BUON, 20(1), 128–135.
54. Neumann, J., Wehweck, L., Maatz, S., Engel, J., Kirchner, T., & Jung, A. (2013). Alterations in the EGFR pathway coincide in colorectal cancer and impact on prognosis. Virchows Archiv, 463(4), 509–523. doi:10.1007/s00428-013-1450-0.
55. Cejas, P., Lopez-Gomez, M., Aguayo, C., Madero, R., Moreno-Rubio, J., de Castro Carpeno, J., et al. (2012). Analysis of the concordance in the EGFR pathway status between primary tumors and related metastases of colorectal cancer patients: implications for cancer therapy. Current Cancer Drug Targets, 12(2), 124–131.
56. Siravegna, G., Mussolin, B., Buscarino, M., Corti, G., Cassingena, A., Crisafulli, G., et al. (2015). Clonal evolution and resistance to EGFR blockade in the blood of colorectal cancer patients. Nature Medicine, 21(7), 795–801. doi:10.1038/nm.3870.
57. Das, A., Kunkel, M., Joudeh, J., Dicker, D. T., Scicchitano, A., Allen, J. E., et al. (2015). Clinico-pathological correlation of serial measurement of circulating tumor cells in 24 metastatic colorectal cancer patients receiving chemotherapy reveals interpatient heterogeneity correlated with CEA levels but independent of KRAS and BRAF mutation. Cancer Biology & Therapy, 16(5), 709–713. doi:10.1080/15384047.2015.1030555.
58. Lyberopoulou, A., Aravantinos, G., Efstathopoulos, E. P., Nikiteas, N., Bouziotis, P., Isaakidou, A., et al. (2015). Mutational analysis of circulating tumor cells from colorectal cancer patients and correlation with primary tumor tissue. PLoS One, 10(4), e0123902. doi:10.1371/journal.pone.0123902.
59. Raimondi, C., Nicolazzo, C., Gradilone, A., Giannini, G., De Falco, E., Chimenti, I., et al. (2014). Circulating tumor cells: exploring intratumor heterogeneity of colorectal cancer. Cancer Biology & Therapy, 15(5), 496–503. doi:10.4161/cbt.28020.
60. Sequist, L. V., Heist, R. S., Shaw, A. T., Fidias, P., Rosovsky, R., Temel, J. S., et al. (2011). Implementing multiplexed genotyping of non-small-cell lung cancers into routine clinical practice. Annals of Oncology, 22(12), 2616–2624. doi:10.1093/annonc/mdr489.
61. Popper, H. H., Ryska, A., Timar, J., & Olszewski, W. (2014). Molecular testing in lung cancer in the era of precision medicine. Translational Lung Cancer Research, 3(5), 291–300. doi:10.3978/j.issn.2218-6751.2014.10.01.
62. Travis, W. D., Brambilla, E., Nicholson, A. G., Yatabe, Y., Austin, J. H., Beasley, M. B., et al. (2015). The 2015 World Health Organization classification of lung tumors: impact of genetic, clinical and radiologic advances since the 2004 classification. Journal of Thoracic Oncology, 10(9), 1243–1260. doi:10.1097/JTO.0000000000000630.
63. Popper, H. H., Timar, J., Ryska, A., & Olszewski, W. (2014). Minimal requirements for the molecular testing of lung cancer. Translational Lung Cancer Research, 3(5), 301–304. doi:10.3978/j.issn.2218-6751.2014.10.02.
64. Linardou, H., Dahabreh, I. J., Kanaloupiti, D., Siannis, F., Bafaloukos, D., Kosmidis, P., et al. (2008). Assessment of somatic k-RAS mutations as a mechanism associated with resistance to EGFR-targeted agents: a systematic review and meta-analysis of studies in advanced non-small-cell lung cancer and metastatic colorectal cancer. The Lancet Oncology, 9(10), 962–972. doi:10.1016/S1470-2045(08)70206-7.
65. Nguyen, K. S., Kobayashi, S., & Costa, D. B. (2009). Acquired resistance to epidermal growth factor receptor tyrosine kinase inhibitors in non-small-cell lung cancers dependent on the epidermal growth factor receptor pathway. Clinical Lung Cancer, 10(4), 281–289. doi:10.3816/CLC.2009.n.039.
66. Popat, S., Wotherspoon, A., Nutting, C. M., Gonzalez, D., Nicholson, A. G., & O’Brien, M. (2013). Transformation to “high grade” neuroendocrine carcinoma as an acquired drug resistance mechanism in EGFR-mutant lung adenocarcinoma. Lung Cancer, 80(1), 1–4. doi:10.1016/j.lungcan.2012.12.019.
67. Sequist, L. V., Waltman, B. A., Dias-Santagata, D., Digumarthy, S., Turke, A. B., Fidias, P., et al. (2011). Genotypic and histological evolution of lung cancers acquiring resistance to EGFR inhibitors. Science Translational Medicine, 3(75), 75ra26. doi:10.1126/scitranslmed.3002003.
68. Suda, K., Murakami, I., Sakai, K., Mizuuchi, H., Shimizu, S., Sato, K., et al. (2015). Small cell lung cancer transformation and T790M mutation: complimentary roles in acquired resistance to kinase inhibitors in lung cancer. Scientific Reports, 5, 14447. doi:10.1038/srep14447.
69. Takezawa, K., Pirazzoli, V., Arcila, M. E., Nebhan, C. A., Song, X., de Stanchina, E., et al. (2012). HER2 amplification: a potential mechanism of acquired resistance to EGFR inhibition in EGFR-mutant lung cancers that lack the second-site EGFRT790M mutation. Cancer Discovery, 2(10), 922–933. doi:10.1158/2159-8290.CD-12-0108.
70. Tanizaki, J., Okamoto, I., Okabe, T., Sakai, K., Tanaka, K., Hayashi, H., et al. (2012). Activation of HER family signaling as a mechanism of acquired resistance to ALK inhibitors in EML4-ALK-positive non-small cell lung cancer. Clinical Cancer Research, 18(22), 6219–6226. doi:10.1158/1078-0432.CCR-12-0392.
71. Kobayashi, S., Boggon, T. J., Dayaram, T., Janne, P. A., Kocher, O., Meyerson, M., et al. (2005). EGFR mutation and resistance of non-small-cell lung cancer to gefitinib. New England Journal of Medicine, 352(8), 786–792. doi:10.1056/NEJMoa044238.
72. Pao, W., Miller, V. A., Politi, K. A., Riely, G. J., Somwar, R., Zakowski, M. F., et al. (2005). Acquired resistance of lung adenocarcinomas to gefitinib or erlotinib is associated with a second mutation in the EGFR kinase domain. PLoS Medicine, 2(3), e73. doi:10.1371/journal.pmed.0020073.
73. Maheswaran, S., Sequist, L. V., Nagrath, S., Ulkus, L., Brannigan, B., Collura, C. V., et al. (2008). Detection of mutations in EGFR in circulating lung-cancer cells. New England Journal of Medicine, 359(4), 366–377. doi:10.1056/NEJMoa0800668.
74. Ohashi, K., Sequist, L. V., Arcila, M. E., Moran, T., Chmielecki, J., Lin, Y. L., et al. (2012). Lung cancers with acquired resistance to EGFR inhibitors occasionally harbor BRAF gene mutations but lack mutations in KRAS, NRAS, or MEK1. Proceedings of the National Academy of Sciences of the United States of America, 109(31), E2127–2133. doi:10.1073/pnas.1203530109.
75. Piotrowska, Z., Niederst, M. J., Karlovich, C. A., Wakelee, H. A., Neal, J. W., Mino-Kenudson, M., et al. (2015). Heterogeneity underlies the emergence of EGFRT790 wild-type clones following treatment of T790M-positive cancers with a third-generation EGFR inhibitor. Cancer Discovery, 5(7), 713–722. doi:10.1158/2159-8290.CD-15-0399.
76. Sorensen, B. S., Wu, L., Wei, W., Tsai, J., Weber, B., Nexo, E., et al. (2014). Monitoring of epidermal growth factor receptor tyrosine kinase inhibitor-sensitizing and resistance mutations in the plasma DNA of patients with advanced non-small cell lung cancer during treatment with erlotinib. Cancer, 120(24), 3896–3901. doi:10.1002/cncr.28964.
77. Hata, A., Katakami, N., Yoshioka, H., Kaji, R., Masago, K., Fujita, S., et al. (2015). Spatiotemporal T790M heterogeneity in individual patients with EGFR-mutant non-small-cell lung cancer after acquired resistance to EGFR-TKI. Journal of Thoracic Oncology, 10(11), 1553–1559. doi:10.1097/JTO.0000000000000647.
78. Turke, A. B., Zejnullahu, K., Wu, Y. L., Song, Y., Dias-Santagata, D., Lifshits, E., et al. (2010). Preexistence and clonal selection of MET amplification in EGFR mutant NSCLC. Cancer Cell, 17(1), 77–88. doi:10.1016/j.ccr.2009.11.022.
79. Galluzzi, L., Vacchelli, E., Bravo-San Pedro, J. M., Buque, A., Senovilla, L., Baracco, E. E., et al. (2014). Classification of current anticancer immunotherapies. Oncotarget, 5(24), 12472–12508.
80. Garon, E. B., Rizvi, N. A., Hui, R., Leighl, N., Balmanoukian, A. S., Eder, J. P., et al. (2015). Pembrolizumab for the treatment of non-small-cell lung cancer. New England Journal of Medicine, 372(21), 2018–2028. doi:10.1056/NEJMoa1501824.
81. Ribas, A., Puzanov, I., Dummer, R., Schadendorf, D., Hamid, O., Robert, C., et al. (2015). Pembrolizumab versus investigator-choice chemotherapy for ipilimumab-refractory melanoma (KEYNOTE-002): a randomised, controlled, phase 2 trial. The Lancet Oncology, 16(8), 908–918. doi:10.1016/s1470-2045(15)00083-2.
82. Larkin, J., Chiarion-Sileni, V., Gonzalez, R., Grob, J. J., Cowey, C. L., Lao, C. D., et al. (2015). Combined nivolumab and ipilimumab or monotherapy in untreated melanoma. New England Journal of Medicine, 373(1), 23–34. doi:10.1056/NEJMoa1504030.
83. Postow, M. A., Chesney, J., Pavlick, A. C., Robert, C., Grossmann, K., McDermott, D., et al. (2015). Nivolumab and ipilimumab versus ipilimumab in untreated melanoma. New England Journal of Medicine, 372(21), 2006–2017. doi:10.1056/NEJMoa1414428.
84. Robert, C., Schachter, J., Long, G. V., Arance, A., Grob, J. J., Mortier, L., et al. (2015). Pembrolizumab versus ipilimumab in advanced melanoma. New England Journal of Medicine, 372(26), 2521–2532. doi:10.1056/NEJMoa1503093.
85. Wolchok, J. D., Kluger, H., Callahan, M. K., Postow, M. A., Rizvi, N. A., Lesokhin, A. M., et al. (2013). Nivolumab plus ipilimumab in advanced melanoma. New England Journal of Medicine, 369(2), 122–133. doi:10.1056/NEJMoa1302369.
86. Brtnicky, T., Fialova, A., Lastovicka, J., Rob, L., & Spisek, R. (2015). Clinical relevance of regulatory T cells monitoring in the peripheral blood of ovarian cancer patients. Human Immunology, 76(2–3), 187–191. doi:10.1016/j.humimm.2014.12.004.
87. Minarik, I., Lastovicka, J., Budinsky, V., Kayserova, J., Spisek, R., Jarolim, L., et al. (2013). Regulatory T cells, dendritic cells and neutrophils in patients with renal cell carcinoma. Immunology Letters, 152(2), 144–150. doi:10.1016/j.imlet.2013.05.010.
88. Xu, H., Mao, Y., Dai, Y., Wang, Q., & Zhang, X. (2009). CD4CD25+ regulatory T cells in patients with advanced gastrointestinal cancer treated with chemotherapy. Onkologie, 32(5), 246–252. doi:10.1159/000210023.
89. McLaughlin, J., Han, G., Schalper, K. A., Carvajal-Hausdorf, D., Pelakanou, V., Rehman, J., et al. (2015). Quantitative assessment of the heterogeneity of PD-L1 expression in non-small-cell lung cancer. JAMA Oncology. doi:10.1001/jamaoncol.2015.3638. 1–9.
90. Teixido, C., Karachaliou, N., Gonzalez-Cao, M., Morales-Espinosa, D., & Rosell, R. (2015). Assays for predicting and monitoring responses to lung cancer immunotherapy. Cancer Biology & Medicine, 12(2), 87–95. doi:10.7497/j.issn.2095-3941.2015.0019.
91. Ilie, M., Long-Mira, E., Bence, C., Butori, C., Lassalle, S., Bouhlel, L., et al. (2015). Comparative study of the PD-L1 status between surgically resected specimens and matched biopsies of NSCLC patients reveal major discordances: a potential issue for anti-PD-L1 therapeutic strategies. Annals of Oncology. doi:10.1093/annonc/mdv489.
92. Kerr, K. M., Tsao, M. S., Nicholson, A. G., Yatabe, Y., Wistuba, I. I., & Hirsch, F. R. (2015). Programmed death-ligand 1 immunohistochemistry in lung cancer: in what state is this art? Journal of Thoracic Oncology, 10(7), 985–989. doi:10.1097/jto.0000000000000526.
93. Bunger, S., Zimmermann, M., & Habermann, J. K. (2015). Diversity of assessing circulating tumor cells (CTCs) emphasizes need for standardization: a CTC Guide to design and report trials. Cancer Metastasis Reviews, 34(3), 527–545. doi:10.1007/s10555-015-9582-0.
94. Freidin, M. B., Freydina, D. V., Leung, M., Montero Fernandez, A., Nicholson, A. G., & Lim, E. (2015). Circulating tumor DNA outperforms circulating tumor cells for KRAS mutation detection in thoracic malignancies. Clinical Chemistry, 61(10), 1299–1304. doi:10.1373/clinchem.2015.242453.
95. Mostert, B., Jiang, Y., Sieuwerts, A. M., Wang, H., Bolt-de Vries, J., Biermann, K., et al. (2013). KRAS and BRAF mutation status in circulating colorectal tumor cells and their correlation with primary and metastatic tumor tissue. International Journal of Cancer, 133(1), 130–141. doi:10.1002/ijc.27987.
96. Morgan, S. R., Whiteley, J., Donald, E., Smith, J., Eisenberg, M. T., Kallam, E., et al. (2012). Comparison of KRAS mutation assessment in tumor DNA and circulating free DNA in plasma and serum samples. Clinical Medicine Insights: Pathology, 5, 15–22. doi:10.4137/CPath.S8798.
97. Bettegowda, C., Sausen, M., Leary, R. J., Kinde, I., Wang, Y., Agrawal, N., et al. (2014). Detection of circulating tumor DNA in early- and late-stage human malignancies. Science Translational Medicine, 6(224), 224ra224. doi:10.1126/scitranslmed.3007094.
98. Akca, H., Demiray, A., Yaren, A., Bir, F., Koseler, A., Iwakawa, R., et al. (2013). Utility of serum DNA and pyrosequencing for the detection of EGFR mutations in non-small cell lung cancer. Cancer Genetics, 206(3), 73–80. doi:10.1016/j.cancergen.2013.01.005.
99. Kim, H. R., Lee, S. Y., Hyun, D. S., Lee, M. K., Lee, H. K., Choi, C. M., et al. (2013). Detection of EGFR mutations in circulating free DNA by PNA-mediated PCR clamping. Journal of Experimental & Clinical Cancer Research, 32(1), 50. doi:10.1186/1756-9966-32-50.
100. Zhang, H., Liu, D., Li, S., Zheng, Y., Yang, X., Li, X., et al. (2013). Comparison of EGFR signaling pathway somatic DNA mutations derived from peripheral blood and corresponding tumor tissue of patients with advanced non-small-cell lung cancer using liquidchip technology. The Journal of Molecular Diagnostics, 15(6), 819–826. doi:10.1016/j.jmoldx.2013.06.006.
101. Luo, J., Shen, L., & Zheng, D. (2014). Diagnostic value of circulating free DNA for the detection of EGFR mutation status in NSCLC: a systematic review and meta-analysis. Scientific Reports, 4, 6269. doi:10.1038/srep06269.
102. Goto, K., Ichinose, Y., Ohe, Y., Yamamoto, N., Negoro, S., Nishio, K., et al. (2012). Epidermal growth factor receptor mutation status in circulating free DNA in serum: from IPASS, a phase III study of gefitinib or carboplatin/paclitaxel in non-small cell lung cancer. Journal of Thoracic Oncology, 7(1), 115–121. doi:10.1097/JTO.0b013e3182307f98.
103. Diaz, L. A., Jr., Williams, R. T., Wu, J., Kinde, I., Hecht, J. R., Berlin, J., et al. (2012). The molecular evolution of acquired resistance to targeted EGFR blockade in colorectal cancers. Nature, 486(7404), 537–540. doi:10.1038/nature11219.
104. Olsson, E., Winter, C., George, A., Chen, Y., Howlin, J., Tang, M. H., et al. (2015). Serial monitoring of circulating tumor DNA in patients with primary breast cancer for detection of occult metastatic disease. EMBO Molecular Medicine, 7(8), 1034–1047. doi:10.15252/emmm.201404913.
105. Sundaresan, T. K., Sequist, L. V., Heymach, J. V., Riely, G. J., Janne, P. A., Koch, W. H., et al. (2015). Detection of T790M, the acquired resistance EGFR mutation, by tumor biopsy versus noninvasive blood-based analyses. Clinical Cancer Research. doi:10.1158/1078-0432.ccr-15-1031.
106. Jiang, T., Ren, S., & Zhou, C. (2015). Role of circulating-tumor DNA analysis in non-small cell lung cancer. Lung Cancer, 90(2), 128–134. doi:10.1016/j.lungcan.2015.09.013.
107. Marchetti, A., Palma, J. F., Felicioni, L., De Pas, T. M., Chiari, R., Del Grammastro, M., et al. (2015). Early prediction of response to tyrosine kinase inhibitors by quantification of EGFR mutations in plasma of NSCLC patients. Journal of Thoracic Oncology, 10(10), 1437–1443. doi:10.1097/JTO.0000000000000643.
108. Thress, K. S., Paweletz, C. P., Felip, E., Cho, B. C., Stetson, D., Dougherty, B., et al. (2015). Acquired EGFR C797S mutation mediates resistance to AZD9291 in non-small cell lung cancer harboring EGFR T790M. Nature Medicine, 21(6), 560–562. doi:10.1038/nm.3854.
109. Nakamura, T., Sueoka-Aragane, N., Iwanaga, K., Sato, A., Komiya, K., Abe, T., et al. (2011). A noninvasive system for monitoring resistance to epidermal growth factor receptor tyrosine kinase inhibitors with plasma DNA. Journal of Thoracic Oncology, 6(10), 1639–1648. doi:10.1097/JTO.0b013e31822956e8.
110. Francis, G., & Stein, S. (2015). Circulating cell-free tumour DNA in the management of cancer. International Journal of Molecular Sciences, 16(6), 14122–14142. doi:10.3390/ijms160614122.
111. Douillard, J. Y., Ostoros, G., Cobo, M., Ciuleanu, T., Cole, R., McWalter, G., et al. (2014). Gefitinib treatment in EGFR mutated Caucasian NSCLC: circulating-free tumor DNA as a surrogate for determination of EGFR status. Journal of Thoracic Oncology, 9(9), 1345–1353. doi:10.1097/JTO.0000000000000263.
112. Douillard, J. Y., Ostoros, G., Cobo, M., Ciuleanu, T., McCormack, R., Webster, A., et al. (2014). First-line gefitinib in Caucasian EGFR mutation-positive NSCLC patients: a phase-IV, open-label, single-arm study. British Journal of Cancer, 110(1), 55–62. doi:10.1038/bjc.2013.721.