Detection of the epidermal growth factor receptor, amphiregulin and epiregulin in formalin-fixed paraffin-embedded human placenta tissue by matrix-assisted laser desorption/ionization mass spectrometry imaging

European Journal of Mass Spectrometry

Volumn 19, Issue 1, 2013, Pages 17-28

  Mahmoud, Khaled ^a,d   Cole, Laura M ^b   Newton, Jillian ^b   Mohamed, Sabah ^c   Al Enazi, Maher ^a   Quirke, Phil ^d   Clench, Malcolm R ^b  

^a JOUF UNIVERSITY   (Saudi Arabia)

^b SHEFFIELD HALLAM UNIVERSITY   (United Kingdom)

^c Ain Shams University   (Egypt)

^d UNIVERSITY OF LEEDS   (United Kingdom)

Author keywords

Amphiregulin; Cetuximab; Colorectal cancer; EGFR; Epiregulin; FFPE; Immunohistochemistry; Maldi; Panitumumab; Placenta; Recombinant cancer therapeutics; Targeted drugs; Tissue imaging

Indexed keywords

AMINO ACIDS; DESORPTION; DISEASES; DRUG PRODUCTS; FORMALDEHYDE; MASS SPECTROMETRY; PARAFFINS; PROTEINS;

AMPHIREGULIN; CANCER THERAPEUTICS; CETUXIMAB; COLORECTAL CANCER; EGFR; EPIREGULIN; FFPE; IMMUNOHISTOCHEMISTRY; MALDI; PANITUMUMAB; PLACENTA; TARGETED DRUGS; TISSUE IMAGING;

TISSUE;

AMPHIREGULIN; EPIDERMAL GROWTH FACTOR; EPIDERMAL GROWTH FACTOR RECEPTOR; EPIREGULIN; FORMALDEHYDE; GLYCOPROTEIN; PARAFFIN; SIGNAL PEPTIDE;

AMINO ACID SEQUENCE; ANTIBODY SPECIFICITY; ARTICLE; CHEMISTRY; ENZYMOLOGY; FEMALE; HUMAN; IMMUNOHISTOCHEMISTRY; MASS SPECTROMETRY; METHODOLOGY; MOLECULAR GENETICS; MOLECULAR IMAGING; PEPTIDE MAPPING; PLACENTA; PREGNANCY; TISSUE FIXATION;

AMINO ACID SEQUENCE; EPIDERMAL GROWTH FACTOR; FEMALE; FORMALDEHYDE; GLYCOPROTEINS; HUMANS; IMMUNOHISTOCHEMISTRY; INTERCELLULAR SIGNALING PEPTIDES AND PROTEINS; MOLECULAR IMAGING; MOLECULAR SEQUENCE DATA; ORGAN SPECIFICITY; PARAFFIN EMBEDDING; PEPTIDE MAPPING; PLACENTA; PREGNANCY; RECEPTOR, EPIDERMAL GROWTH FACTOR; SPECTROMETRY, MASS, MATRIX-ASSISTED LASER DESORPTION-IONIZATION; TISSUE FIXATION;

MLCS; MLOWN;

EID: 84878842043     PISSN: None     EISSN: 17516838     Source Type: Journal    
DOI: 10.1255/ejms.1212     Document Type: Article

References (61)

1. T. Hunter and B. M. Sefton, "Transforming gene product of Rous sarcoma virus phosphorylates tyrosine", Proc. Natl. Acad. Sci. USA 77, 1311 (1980). doi: 10.1073/pnas.77.3.1311
2. P. Blume-Jensen and T. Hunter, "Oncogenic kinase signaling", Nature 411, 355 (2001). doi: 10.1038/35077225 (Pubitemid 32467045)
3. T. Pawson and N. Warner, "Oncogenic re-wiring of cellular signaling pathways", Oncogene 26, 1268 (2007). doi: 10.1038/sj.onc.1210255 (Pubitemid 46328468)
4. D. Hanahan and R. A. Weinberg, "Hallmarks of cancer: the next generation", Cell 144, 646 (2011). doi: 10.1016/j. cell.2011.02.013
5. F. Ciardiello and G. Tortora, "A novel approach in the treatment of cancer: targeting the epidermal growth factor receptor", Clin. Cancer Res. 7, 2958 (2001).
6. J. T. Hartmann, M. Haap, H. G. Kop and H. P. Lipp, "Tyrosine kinase inhibitors - a review on pharmacology, metabolism and side effects", Current Drug Metabolism 5, 470 (2009). doi: 10.2174/138920009788897975
7. M. Moroni, S. Veronese, S. Benvenuti, G. Marrapese, A. Sartore-Bianchi, F. Di Nicolantonio, M. Gambacorta, S. Siena and A. Bardelli, "Gene copy number for epidermal growth factor receptor (EGFR) and clinical response to anti-EGFR treatment in colorectal cancer: a cohort study", Lancet Oncology 5, 279 (2005). doi: 10.1016/S1470-2045 (05) 70102-9
8. J. A. Engelman and P. A. Janne, "Factors predicting response to EGFR tyrosine kinase inhibitors", Semin. Resp. Crit. Care Med. 26, 314 (2005). doi: 10.1055/s-2005-871990 (Pubitemid 40980880)
9. N. Personeni, A. Hendlisz, J. Gallez, M. G. Galdon, D. Larsimont, J. L. Van Laethem, N. Nagy, M. Barette, M. Paesmans, F. Cardoso and H. Bleiberg, "Correlation between the response to cetuximab alone or in combination with irinotecan and the activated/phosphorylated epidermal growth factor receptor in metastatic colorectal cancer", Semin. Oncol. 32(Suppl 9), S59 (2005). doi: 10.1053/j.seminoncol.2005.04.029 (Pubitemid 43080918)
10. A. Lièvre, J. B. Bachet, D. Le Corre, V. Boige, B. Landi, J. F. Emile, J. F. Côté, G. Tomasic, C. Penna, M. Ducreux, P. Rougier, F. Penault-Llorca and P. Laurent-Puig, "KRAS mutation status is predictive of response to cetuximab therapy in colorectal cancer", Cancer Res. 66, 3992 (2006). doi: 10.1158/0008-5472. CAN-06-0191
11. A. Sartore-Bianchi, M. Moroni, S. Veronese, C. Carnaghi, E. Bajetta, G. Luppi, A. Sobrero, C. Barone, S. Cascinu, G. Colucci, E. Cortesi, M. Nichelatti, M. Gambacorta and S. Siena, "Epidermal growth factor receptor gene copy number and clinical outcome of metastatic colorectal cancer treated with panitumumab", J. Clin. Oncol. 25, 3238-3245 (2007). doi: 10.1200/JC0.2007.11.5956 (Pubitemid 47325607)
12. R. G. Amado, M. Wolf, M. Peeters, E. Van Cutsem, S. Siena, D. J. Freeman, T. Juan, R. Sikorski, S. Suggs, R. Radinsky, S. D. Patterson and D. D. Chang, "Wild-type KRAS is required for panitumumab efficacy in patients with metastatic colorectal cancer", J. Clin. Oncol. 26, 1626 (2008). doi: 10.1200/JC0.2007.14.7116
13. S. Siena, A. Sartore-Bianchi, F. Di Nicolantonio, J. Balfour and A. Bardelli, "Biomarkers predicting clinical outcome of epidermal growth factor receptor-targeted therapy in metastatic colorectal cancer", J. Natl. Cancer Inst. 101, 1308 (2009). doi: 10.1093/inci/dip280
14. Z. Y. Chen, W. Z. Zhong, X. C. Zhang, J. Su, X. N. Yang, Z. H. Chen, J. J. Yang, Q. Zhou, H. H. Yan, S. J. An, H. J. Chen, B. Y. Jiang, T. S. Mok and Y. L. Wu, "EGFR mutation heterogeneity and the mixed response to EGFR tyrosine kinase inhibitors of lung adenocarcinomas", Oncologist 17, 978 (2012). doi: 10.1634/theoncologist.2011-0385
15. R. Bianco, T. Troiani, G. Tortora and F. Ciardiello, "Intrinsic and acquired resistance to EGFR inhibitors in Human cancer therapy", Endocr-Relat. CancerSuppl. 1, S159 (2005).
16. F. Morgillo, M. A. Bareschino, R. Bianco, G. Tortora and F. Ciardiello, "Primary and acquired resistance to anti-EGFR targeted drugs in cancer therapy", Differentiation 75, 788 (2007). doi: 10.1111/j.1432-0436.2007. 00200.x (Pubitemid 350086168)
17. J. K. Rho, Y. J. Choi, J. K. Lee, B. Y. Ryoo, I. I. Na, S. H. Yang, S. S. Lee, C. H. Kim, Y. D. Yoo and J. C. Lee, "The role of MET activation in determining the sensitivity to epidermal growth factor receptor tyrosine kinase inhibitors", Mol. Cancer Res. 10, 1736 (2009). doi: 10.1158/1541-7786. MCR-08-0504
18. D. L. Wheeler, E. F. Dunn and P. M. Harari, "Understanding resistance to EGFR inhibitors-impact on future treatment strategies", Natl. Rev. Clin. Oncol. 9, 493 (2010) 7.
19. L. Bonanno, A. Jirillo and A. Favaretto, "Mechanisms of acquired resistance to epidermal growth factor receptor tyrosine kinase inhibitors and new therapeutic perspectives in non small cell lung cancer", Curr. Drug Targets 12, 922 (2011). doi: 10.2174/138945011795528958
20. K. Suda, H. Mizuuchi, Y. Maehara and T. Mitsudomi, "Acquired resistance mechanisms to tyrosine kinase inhibitors in lung cancer with activating epidermal growth factor receptor mutation-diversity, ductility, and destiny", Cancer Metast. Rev. 31, 807 (2012). doi: 10.1007/s10555-012-9391- 7
21. K. Tabara, R. Kanda, K. Sonoda, T. Kubo, Y. Murakami, A. Kawahara, K. Azuma, H. Abe, M. Kage, A. Yoshinaga, T. Tahira, K. Hayashi, T. Arao, K. Nishio, R. Rosell, M. Kuwano and M. Ono, "Loss of activating EGFR mutant gene contributes to acquired resistance to EGFR tyrosine kinase inhibitors in lung cancer cells", PLoS One 7, e41017 (2012). doi: 10.1371/journal.pone.0041017
22. J, Baselga, "Does epidermal growth factor receptor status predict activity of cetuximab in colorectal cancer patients?", Natl. Clin. Pract. Oncol. 2, 284 (2005). doi: 10.1371/journal.pone.0041017
23. D. Cunningham, Y. Humblet, S. Siena, D. Khayat, H. Bleiberg, A. Santoro, D. Bets, M. Mueser, A. Harstrick, C. Verslype, I. Chau and V. Cutsem, "Cetuximab monotherapy and cetuximab plus irinotecan in irinotecan-refractory metastatic colorectal cancer", New Engl. J. Med. 351, 337 (2004). doi: 10.1056/NEJMoa033025 (Pubitemid 38944402)
24. J. R. Hecht, A. Patnaik, J. Berlin, A. Venook, I. Malik, S. Tchekmedyian, L. Navale, R. G. Amado and N. J. Meropol, "Panitumumab monotherapy in patients with previously treated metastatic colorectal cancer", Cancer 110, 980 (2007). doi: 10.1002/cncr. 22915
25. K. Y. Chung, J. Shia, N. E. Kemeny, M. Shah, G. K. Schwartz, A. Tse, A. Hamilton, D. Pan, D. Schrag, L. Schwartz, D. S. Klimstra, D. Fridman, D. P. Kelsen and L. B. Saltz, "Cetuximab shows activity in colorectal cancer patients with tumors that do not express the epidermal growth factor receptor by immunohistochemistry", J. Clin. Oncol. 23, 1803 (2005). doi: 10.1200/JC0.2005.08.037
26. M. Moroni, S. Veronese, A. Sartore-Bianchi, S. Artale and S. Siena, "Controversial evaluation of EGFR protein and gene status in predicting response to anti-EGFR monoclonal antibodies in metastatic colorectal cancer: a case report and review of the literature", Target. Oncol. 3, 127 (2008). doi: 10.1007/s11523-008-0073-x
27. B. A. Gusterson and K. D. Hunter, "Should we be surprised at the paucity of response to EGFR inhibitors?", Lancet Oncol. 10, 522 (2009). doi: 10.1016/S1470-2045 (09) 70034-8
28. C. J. Allegra, J. M. Jessup, M. R. Somerfield, S. R. Hamilton, E. H. Hammond, D. F. Hayes, P. K. McAllister, R. F. Morton and R. L. Schilsky, "American Society of Clinical Oncology provisional clinical opinion: testing for KRAS gene mutations in patients with metastatic colorectal carcinoma to predict response to antiepidermal growth factor receptor monoclonal antibody therapy", J. Clin. Oncol. 27, 2091 (2009). doi: 10.1200/JC0.2009.21.9170
29. M. Jhawer, S. Goel, A. J. Wilson, C. Montagna, Y. H. Ling, D. S. Byun, S. Nasser, D. Arango, J. Shin, L. Klampfer, L. H. Augenlicht, R. Perez-Soler and J. M. Mariadason, "PIK3CA mutation/PTEN expression status predicts response of colon cancer cells to the epidermal growth factor receptor inhibitor cetuximab", Cancer Res. 68, 1953-1961 (2008). doi: 10.1158/0008-5472. CAN-07-5659 (Pubitemid 351416582)
30. L. Bonanno, M. Schiavon, G. Nardo, R. Bertorelle, L. Bonaldi, A. Galligioni, S. Indraccolo, G. Pasello, F. Rea and A. Favaretto, "Prognostic and predictive implications of EGFR mutations, EGFR copy number and KRAS mutations in advanced stage lung adenocarcinoma" Anticancer Res. 30, 5121 (2010).
31. J. Tol, J. R. Dijkstra, M. Klomp, S. Teerenstra, M. Dommerholt, M. E. Vink-Borger, P. H. van Cleef, J. H. van Krieken, C. J. Punt and I. D. Nagtegaal, "Markers for EGFR pathway activation as predictor of outcome in metastatic colorectal cancer patients treated with or without cetuximab", Eur. J. Cancer 46, 1997 (2010). doi: 10.1016/j.ejca.2010.03.036
32. A. Lièvre, J.-B. Bachet, V. Boige, A. Cayre, D. Le Corre, E. Buc, M. Ychou, O. Bouche, B. Landi, C. Louvet, T. Andre, F. Bibeau, M.-D. Diebold, P. Rougier, M. Ducreux, G. Tomasic, J.-F. Emile, F. Penault-Llorca and P. Laurent-Puig, "KRAS mutations as an independent prognostic factor in patients with advanced colorectal cancer treated with cetuximab", J. Clin. Oncol. 26, 374 (2008). doi: 10.1200/JC0.2007.12.5906
33. F. Cappuzzo, G. Finocchiaro, E. Rossi, P. A. Janne, C. Carnaghi, C. Calandri, K. Bencardino, C. Ligorio, F. Ciardiello, T. Pressiani, A. Destro, M. Roncalli, L. Crino, W. A. Franklin, A. Santoro and M. Varella-Garcia, "EGFR FISH assay predicts for response to cetuximab in chemotherapy refractory colorectal cancer patients", Ann. Oncol. 19, 717 (2008). doi: 10.1093/annonc/mdm492 (Pubitemid 351461042)
34. S. Ichih ara, S. Toyooka, Y. Fujiwara, K. Hotta, H. Shigematsu, M. Tokumo, J. Soh, H. Asano, K. Ichimura, K. Aoe, M. Aoe, K. Kiura, K. Shimizu, H. Date and N. Shimizu, "The impact of epidermal growth factor receptor gene status on gefitinib-treated Japanese patients with non-small-cell lung cancer", Int. J. Cancer 120, 1239 (2007). doi: 10.1002/iic.22513
35. F. Cappuzzo, "EGFR FISH versus mutation: Different tests, different end-points", Lung Cancer 60, 160 (2008). doi: 10.1016/j.lungcan. 2008.02.008
36. A. Italiano, P. Follana, F. X. Caroli, J. L. Badetti, D. Benchimol, G. Garnier, J. Gugenheim, J. Haudebourg, F. Keslair, G. Lesbats, G. Lledo, J. F. Roussel, F. Pedeutour and E. François, "Cetuximab shows activity in colorectal cancer patients with tumors for which FISH analysis does not detect an increase in EGFR gene copy number", Ann. Surg. Oncol. 15, 649 (2008). doi: 10.1245/s10434-007-9667-2
37. S. Khambata-Ford, C. R. Garrett, N. J. Meropol, M. Basik, C. T. Harbison, S. Wu, T. W. Wong, X. Huang, C. H. Takimoto, A. K. Godwin, B. R. Tan, S. S. Krishnamurthi, H. A. Burris, 3rd, E. A. Poplin, M. Hidalgo, J. Baselga, E. A. Clark and D. J. Mauro, "Expression of epiregulin and amphiregulin and K-ras mutation status predict disease control in metastatic colorectal cancer patients treated with cetuximab", J. Clin. Oncol. 25, 3230-3237 (2007). doi: 10.1200/JC0.2006.10.5437 (Pubitemid 47325606)
38. K. Yonesaka, K. Zejnullahu, N. Lindeman, A. J. Homes, D. M. Jackman, F. Zhao, A. M. Rogers, B. E. Johnson and P. A. Jänne, "Autocrine production of amphiregulin predicts sensitivity to both gefitinib and cetuximab in EGFR wild-type cancers", Clin. Cancer Res. 14, 6963 (2008). doi: 10.1158/1078-0432. CC R-08-0957
39. B. Jacobs, W. De Roock, H. Piessevaux, R. Van Oirbeek, B. Biesmans, J. De Schutter, S. Fieuws, J. Vandesompele, M. Peeters, J. L. Van Laethem, Y. Humblet, F. Pénault-Llorca, G. De Hertogh, P. Laurent-Puig, E. Van Cutsem and S. Tejpar, "Amphiregulin and epiregulin mRNA expression in primary tumors predicts outcome in metastatic colorectal cancer treated with cetuximab", J. Clin. Oncol. 27, 5068 (2009). doi: 10.1200/JC0.2008.21.3744
40. J. B. Baker, D. Dutta, D. Watson, T. Maddala, B. M. Munneke, S. Shak, E. K. Rowinsky, L. A. Xu, C. T. Harbison, E. A. Clark, D. J. Mauro and S. Khambata-Ford, "Tumour gene expression predicts response to cetuximab in patients with KRAS wild-type metastatic colorectal cancer", Brit. J. Cancer 104, 488-495 (2011). doi: 10.1038/sj.bjc.6606054
41. M. H. Chang, H. K. Ahn, J. Lee, C. K. Jung, Y. L. Choi, Y. H. Park, J. S. Ahn, K. Park, M. J. Ahn, "Clinical impact of amphiregulin expression in patients with epidermal growth factor receptor (EGFR) wild-type nonsmall cell lung cancer treated with EGFR-tyrosine kinase inhibitors", Cancer 117, 143 (2011). doi: 10.1002/cncr.25560
42. H. Kuramochi, G. Nakajima, Y. Kaneko, A. Nakamura, Y. Inoue, M. Yamamoto and K. Hayashi, "Amphiregulin and epiregulin mRNA expression in primary colorectal cancer and corresponding liver metastases", BMC Cancer 12, 88 (2012). doi: 10.1186/1471-2407-12-88
43. J. H. Park, S. W. Han, D. Y. Oh, S. A. Im, S. Y. Jeong, K. J. Park, T. Y. Kim, Y. J. Bang and J. G. Park, "Analysis of KRAS, BRAF, PTEN, IGF1R, EGFR intron 1 CA status in both primary tumors and paired metastases in determining benefit from cetuximab therapy in colon cancer", Cancer Chemoth. Pharm. 68, 1045 (2011). doi: 10.1007/s00280-011-1586-z
44. R. Le maire, A. Desmons, J. C. Tabet, R. Day, M. Salzet and I. Fournier, "Direct analysis and MALDI imaging of formalin-fixed, paraffin-embedded tissue sections", J. Proteome Res. 6, 1295 (2007). doi: 10.1021/pr060549i (Pubitemid 46724026)
45. M.-C. Djidja, E. Claude, M. Snell, P. Scriven, S. Francese, V. A. Carolan and M. R. Clench, "MALDI-ion mobility separation-mass spectrometry imaging of glucose-regulated protein 78 kDa (Grp78) in human formalin fixed paraffin embedded pancreatic adenocarcinoma tissue sections", J. Proteome Res. 8, 4876 (2009). doi: 10.1021/pr900522m
46. M.-C. Djidja, E. Claude, M. Snell, P. Scriven, V. A. Carolan and M. R. Clench, "Novel molecular tumour classification using MALDI-mass spectrometry imaging of tissue micro array", Anal. Bioanal. Chem. 397, 587 (2010). doi: 10.1007/s00216-010-3554-6
47. J. Jiang, C. E. Parker, K. A. Hoadley, C. M. Perou, G. Boysen and C. H. Borchers, "Development of an immuno tandem mass spectrometry (iMALDI) assay for EGFR diagnosis", Proteom. Clin. Appl. 1, 1651 (2007). doi: 10.1002/prca.200700009
48. F. Taguchi, B. Solomon, V. Gregorc, H. Roder, R. Gray, K. Kasahara, M. Nishio, J. Brahmer, A. Spreafico, V. Ludovini, P. P. Massion, R. Dziadziuszko, J. Schiller, J. Grigorieva, M. Tsypin, S. W. Hunsucker, R. Caprioli, M. W. Duncan, F. R. Hirsch, P. A. Bunn, Jr and D. P. Carbone, "Mass spectrometry to classify non-small-cell lung cancer patients for clinical outcome after treatment with epidermal growth factor receptor tyrosine kinase inhibitors: a multicohort cross-institutional study", J. Natl. Cancer Inst. 99, 11838 (2007). doi: 10.1093/jnci/djk195
49. H. Roder, M. Tsypin and J. Grigorieva, Monitoring Treatment of Colorectal Cancer Patients with Drugs Targeting EGFR Pathway Using Mass Spectrometry of Patient Samples, United States Patent No. US8, 119, 418 B2.
50. A. Hoekstra and J. D. Herscheid, "The placenta as a substitute for cancerous models", Med. Hypotheses 17, 299 (1985). doi: 10.1016/03 06-9877 (85) 90088-X
51. M. J. Murray and B. A. Lessey, "Embryo implantation and tumor metastasis: common pathways of invasion and angiogenesis", Semin. Reprod. Endocr. 17, 275 (1999). doi: 10.1055/s-2007-1016235
52. C. Ferretti, L. Bruni, V. Dangles-Marie, A. P. Pecking and D. Bellet, "Molecular circuits shared by placental and cancer cells, and their implications in the proliferative, invasive and migratory capacities of trophoblasts", Hum. Reprod. Update 13, 121 (2007). doi: 10.1093/humupd/dml048 (Pubitemid 46323191)
53. J. Mühlhauser, C. Crescimanno, P. Kaufmann, H. Höfler, D. Zaccheo and M. Castellucci, "Differentiation and proliferation patterns in human trophoblast revealed by c-erbB-2 oncogene product and EGF-R", J. Histochem. and Cytochem. 41, 165 (1993). doi: 10.1177/41.2.8093455
54. T. Maruo, H. Matsuo, T. Otani and M. Mochizuki, "Role of epidermal growth factor (EGF) and its receptor in the development of the human placenta", Reprod. Fert. Develop. 7, 1465 (1995). doi: 10.1071/RD9951465 (Pubitemid 26133258)
55. J. J. Lysiak, G. R. Johnson and P. K. Lala, "Localization of amphiregulin in the Human placenta and decidua throughout gestation: role in trophoblast growth", Placenta 16, 359 (1995). doi: 10.1016/0143-4004 (95) 90093-4
56. H. Toyoda, T. Komurasaki, D. Uchida and S. Morimoto, "Distribution of mRNA for human epiregulin, a differentially expressed member of the epidermal growth factor family", Biochem. J. 326, 69 (1997).
57. J. Stauber, L. MacaLeese, J. Franck, E. Claude, M. Snel, B. K. Kaletas, I. M. V. D. Wiel, M. Witztorski, I. Fournier and R. Heeren, "On-tissue protein identification and imaging by MALDI-ion mobility mass spectrometry", J. Am. Soc. Mass Spectrom. 21, 338 (2010). doi: 10.1016/i.iasms.2009.09.016
58. Y. Schober, T. Schramm, B. Spengler and A. Rompp, "Protein identification by accurate mass matrix-assisted laser desorption/ionization imaging of tryptic peptides", Rapid Commun. Mass Spectrom. 25, 2475 (2011). doi: 10.1002/rcm.5135
59. V. K. Anagnostou, A. W. Welsh, J. M. Giltnane, S. Siddiqui, C. Liceaga, M. Gustavson, K. N. Syrigos, J. L. Reiter and D. L. Rimm, "Analytic variability in immunohistochemistry biomarker studies", Cancer Epidem. Biomar 19, 982 (2010). doi: 10.1158/1055-9965. EPI-10-0097
60. M. C. Prewett, A. T. Hooper, R. Bassi, L. M. Ellis, H. W. Waksal and D. J. Hicklin, "Enhanced antitumor activity of anti-epidermal growth factor receptor monoclonal antibodyIMC-C225 in combination with irinotecan (CPT-11) against human colorectal tumor xenografts", Clin. Cancer Res. 8, 994 (2002).
61. S. Kopetz, G. J. Chang, M. J. Overman, C. Eng, D. J. Sargent, D. W. Larson, A. Grothey, J. N. Vauthey, D. M. Nagorney and R. R. McWilliams, "Improved survival in metastatic colorectal cancer is associated with adoption of hepatic resection and improved chemotherapy", J. Clin. Oncol. 27, 36 (2009). doi: 10.1200/JC0.2008.20.5278