Role of human epidermal growth factor receptor 2 in gastric cancer: Biological and pharmacological aspects

World Journal of Gastroenterology

Volumn 20, Issue 16, 2014, Pages 4526-4535

  Jørgensen, Jan Trøst ^a  

^a Dx Rx Institute   (Denmark)

Author keywords

Ado trastuzumab emtansine; Companion diagnostics; Gastric cancer; Human epidermal growth factor receptor 2; Lapatinib; Pertuzumab; Prognostic; Trastuzumab

Indexed keywords

AFATINIB; CAPECITABINE; CISPLATIN; DACOMITINIB; EPIDERMAL GROWTH FACTOR RECEPTOR 2; FLUOROURACIL; LAPATINIB; PERTUZUMAB; TRASTUZUMAB; TRASTUZUMAB EMTANSINE; ANTINEOPLASTIC AGENT; EGFR PROTEIN, HUMAN; EPIDERMAL GROWTH FACTOR RECEPTOR; PROTEIN KINASE INHIBITOR; TUMOR MARKER;

ARTICLE; BIOLOGICAL FUNCTIONS; CANCER DIAGNOSIS; CANCER PROGNOSIS; CANCER STAGING; DISEASE COURSE; FLUORESCENCE IN SITU HYBRIDIZATION; GENE AMPLIFICATION; GENE OVEREXPRESSION; HUMAN; IMMUNOHISTOCHEMISTRY; LOWER ESOPHAGUS SPHINCTER; MULTICENTER STUDY (TOPIC); OVERALL SURVIVAL; PHASE 1 CLINICAL TRIAL (TOPIC); PHASE 2 CLINICAL TRIAL (TOPIC); PHASE 3 CLINICAL TRIAL (TOPIC); PREVALENCE; RANDOMIZED CONTROLLED TRIAL (TOPIC); STOMACH ADENOCARCINOMA; STOMACH CANCER; ADENOCARCINOMA; ANTAGONISTS AND INHIBITORS; DRUG EFFECTS; ENZYMOLOGY; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; MOLECULARLY TARGETED THERAPY; MORTALITY; PATHOLOGY; SIGNAL TRANSDUCTION; STOMACH NEOPLASMS; TREATMENT OUTCOME;

ADENOCARCINOMA; ANTINEOPLASTIC COMBINED CHEMOTHERAPY PROTOCOLS; ESOPHAGOGASTRIC JUNCTION; GENE AMPLIFICATION; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; MOLECULAR TARGETED THERAPY; PROTEIN KINASE INHIBITORS; RECEPTOR, EPIDERMAL GROWTH FACTOR; SIGNAL TRANSDUCTION; STOMACH NEOPLASMS; TREATMENT OUTCOME; TUMOR MARKERS, BIOLOGICAL;

EID: 84899645435     PISSN: 10079327     EISSN: 22192840     Source Type: Journal    
DOI: 10.3748/wjg.v20.i16.4526     Document Type: Article

References (59)

1. Jørgensen JT. Targeted HER2 treatment in advanced gastric cancer. Oncology 2010; 78: 26-33. [PMID: 20185938 DOI: 10.1159/000288295]
2. Ross JS, Slodkowska EA, Symmans WF, Pusztai L, Ravdin PM, Hortobagyi GN. The HER-2 receptor and breast cancer: ten years of targeted anti-HER-2 therapy and personalized medicine. Oncologist 2009; 14: 320-368. [PMID: 19346299 DOI: 10.1634/theoncologist.2008-0230]
3. Yamamoto T, Ikawa S, Akiyama T, Semba K, Nomura N, Miyajima N, Saito T, Toyoshima K. Similarity of protein encoded by the human c-erb-B-2 gene to epidermal growth factor receptor. Nature 1986; 319: 230-234. [PMID: 3003577 DOI: 10.1038/319230a0]
4. Fukushige S, Matsubara K, Yoshida M, Sasaki M, Suzuki T, Semba K, Toyoshima K, Yamamoto T. Localization of a novel v-erbB-related gene, c-erbB-2, on human chromosome 17 and its amplification in a gastric cancer cell line. Mol Cell Biol 1986; 6: 955-958. [PMID: 2430175]
5. Sakai K, Mori S, Kawamoto T, Taniguchi S, Kobori O, Morioka Y, Kuroki T, Kano K. Expression of epidermal growth factor receptors on normal human gastric epithelia and gastric carcinomas. J Natl Cancer Inst 1986; 77: 1047-1052. [PMID: 3464796]
6. Jørgensen JT, Hersom M. HER2 as a Prognostic Marker in Gastric Cancer - A Systematic Analysis of Data from the Literature. J Cancer 2012; 3: 137-144. [PMID: 22481979 DOI: 10.7150/jca.4090]
7. Hu B, El Hajj N, Sittler S, Lammert N, Barnes R, Meloni-Ehrig A. Gastric cancer: Classification, histology and application of molecular pathology. J Gastrointest Oncol 2012; 3: 251-261. [PMID: 22943016 DOI: 10.3978/j.issn.2078-6891]
8. Kamangar F, Dores GM, Anderson WF. Patterns of cancer incidence, mortality, and prevalence across five continents: defining priorities to reduce cancer disparities in different geographic regions of the world. J Clin Oncol 2006; 24: 2137-2150. [PMID: 16682732 DOI: 10.1200/JCO.2005.05.2308]
9. Ohtsu A. Chemotherapy for metastatic gastric cancer: past, present, and future. J Gastroenterol 2008; 43: 256-264. [PMID: 18458840 DOI: 10.1007/s00535-008-2177-6]
10. Bang YJ, Van Cutsem E, Feyereislova A, Chung HC, Shen L, Sawaki A, Lordick F, Ohtsu A, Omuro Y, Satoh T, Aprile G, Kulikov E, Hill J, Lehle M, Rüschoff J, Kang YK. Trastuzumab in combination with chemotherapy versus chemotherapy alone for treatment of HER2-positive advanced gastric or gastro-oesophageal junction cancer (ToGA): a phase 3, openlabel, randomised controlled trial. Lancet 2010; 376: 687-697. [PMID: 20728210 DOI: 10.1016/S0140-6736(10)61121-X]
11. Bang YJ, Chung HC, Xu JM, Lordick F, Sawaki A, Lipatov O, Al-Sakaff N, See CG, Rueschoff J, Van Cutsem E. Pathological features of advanced gastric cancer: relationship to human epidermal growth factor receptor 2 positivity in the global screening programme of the ToGA trial. J Clin Oncol 2009; 27 Suppl: Abstract 4556
12. Hofmann M, Stoss O, Shi D, Büttner R, van de Vijver M, Kim W, Ochiai A, Rüschoff J, Henkel T. Assessment of a HER2 scoring system for gastric cancer: results from a validation study. Histopathology 2008; 52: 797-805. [PMID: 18422971 DOI: 10.1111/j.1365-2559.2008.03028.x]
13. Rüschoff J, Hanna W, Bilous M, Hofmann M, Osamura RY, Penault-Llorca F, van de Vijver M, Viale G. HER2 testing in gastric cancer: a practical approach. Mod Pathol 2012; 25: 637-650. [PMID: 22222640 DOI: 10.1038/modpathol.2011.198]
14. Food and Drug Administration. HercepTest-Summary of Safety and Effectiveness Data (SSED), October 20, 2010 Available from: URL: http://www.accessdata.fda.gov/cdrh_docs/pdf/P980018S010b.pdf
15. Ishikawa T, Kobayashi M, Mai M, Suzuki T, Ooi A. Amplification of the c-erbB-2 (HER-2/neu) gene in gastric cancer cells. Detection by fluorescence in situ hybridization. Am J Pathol 1997; 151: 761-768. [PMID: 9284825]
16. Yonemura Y, Ninomiya I, Tsugawa K, Fushida S, Fujimura T, Miyazaki I, Uchibayashi T, Endou Y, Sasaki T. Prognostic significance of c-erbB-2 gene expression in the poorly differentiated type of adenocarcinoma of the stomach. Cancer Detect Prev 1998; 22: 139-146. [PMID: 9544434 DOI: 10.1046/j.1525-1500.1998.CDOA02.x]
17. Lee KE, Lee HJ, Kim YH, Yu HJ, Yang HK, Kim WH, Lee KU, Choe KJ, Kim JP. Prognostic significance of p53, nm23, PCNA and c-erbB-2 in gastric cancer. Jpn J Clin Oncol 2003; 33: 173-179. [PMID: 12810831 DOI: 10.1093/jjco/hyg039]
18. Barros-Silva JD, Leitão D, Afonso L, Vieira J, Dinis-Ribeiro M, Fragoso M, Bento MJ, Santos L, Ferreira P, Rêgo S, Brandão C, Carneiro F, Lopes C, Schmitt F, Teixeira MR. Association of ERBB2 gene status with histopathological parameters and disease-specific survival in gastric carcinoma patients. Br J Cancer 2009; 100: 487-493. [PMID: 19156142 DOI: 10.1038/sj.bjc.6604885]
19. Song HS, Do YR, Kim IH, Sohn SS, Kwon KY. Prognostic significance of immunohistochemical expression of EGFR and C-erbB-2 oncoprotein in curatively resected gastric cancer. Cancer Res Treat 2004; 36: 240-245. [PMID: 20368841 DOI: 10.4143/crt.2004.36.4.240]
20. Fan XS, Chen JY, Li CF, Zhang YF, Meng FQ, Wu HY, Feng AN, Huang Q. Differences in HER2 over-expression between proximal and distal gastric cancers in the Chinese population. World J Gastroenterol 2013; 19: 3316-3323. [PMID: 23745034 DOI: 10.3748/wjg.v19.i21.3316]
21. Tanner M, Hollmén M, Junttila TT, Kapanen AI, Tommola S, Soini Y, Helin H, Salo J, Joensuu H, Sihvo E, Elenius K, Isola J. Amplification of HER-2 in gastric carcinoma: association with Topoisomerase IIalpha gene amplification, intestinal type, poor prognosis and sensitivity to trastuzumab. Ann Oncol 2005; 16: 273-278. [PMID: 15668283 DOI: 10.1093/annonc/mdi064]
22. Polkowski W, van Sandick JW, Offerhaus GJ, ten Kate FJ, Mulder J, Obertop H, van Lanschot JJ. Prognostic value of Laurén classification and c-erbB-2 oncogene overexpression in adenocarcinoma of the esophagus and gastroesophageal junction. Ann Surg Oncol 1999; 6: 290-297. [PMID: 10340889 DOI: 10.1007/s10434-999-0290-2]
23. Ohguri T, Sato Y, Koizumi W, Saigenji K, Kameya T. An immunohistochemical study of c-erbB-2 protein in gastric carcinomas and lymph-node metastases: is the c-erbB-2 protein really a prognostic indicator? Int J Cancer 1993; 53: 75-79. [PMID: 8093216 DOI: 10.1002/ijc.2910530115]
24. Chariyalertsak S, Sugano K, Ohkura H, Mori Y. Comparison of c-erbB-2 oncoprotein expression in tissue and serum of patients with stomach cancer. Tumour Biol 1994; 15: 294-303. [PMID: 7991990 DOI: 10.1159/000217904]
25. Mizutani T, Onda M, Tokunaga A, Yamanaka N, Sugisaki Y. Relationship of C-erbB-2 protein expression and gene amplification to invasion and metastasis in human gastric cancer. Cancer 1993; 72: 2083-2088. [PMID: 8397058]
26. Yonemura Y, Ninomiya I, Yamaguchi A, Fushida S, Kimura H, Ohoyama S, Miyazaki I, Endou Y, Tanaka M, Sasaki T. Evaluation of immunoreactivity for erbB-2 protein as a marker of poor short term prognosis in gastric cancer. Cancer Res 1991; 51: 1034-1038. [PMID: 1670998]
27. Chung H, Bang Y, Xu J, Lordick F, Sawaki A, Lipatov O, Lehle M, Pickl M, Rueschoff J, Van Cutsem E. Human epidermal growth factor receptor 2 (HER2) in gastric cancer (GC): results of the ToGA trial screening programme and recommendations for HER2 testing. ECCO 15-34th ESMO Multidisciplinary Congress. Berlin, Germany: ECCO, 2009
28. Trosman JR, Weldon CB, Tsongalis GJ, Schink JC, Benson AB. What are NCI-designated cancer centers using for gastric and esophageal cancer HER2 testing? J Clin Oncol 2013; 31 Suppl: Abstract e15010
29. Slamon DJ, Clark GM, Wong SG, Levin WJ, Ullrich A, Mc-Guire WL. Human breast cancer: correlation of relapse and survival with amplification of the HER-2/neu oncogene. Science 1987; 235: 177-182. [PMID: 3798106 DOI: 10.1126/science.3798106]
30. Roh JK, Paik S, Chung HC, Yang W, Kim HK, Choi IJ, Kim J, Koh E, Lee KS, Min JS. Overexpression of erbB-2 protein in gastric adenocarcinoma--a potential role in therapeutic response to adjuvant 5-FU-doxorubicin regimen. Gan To Kagaku Ryoho 1992; 19: 1207-1219. [PMID: 1355336]
31. Chua TC, Merrett ND. Clinicopathologic factors associated with HER2-positive gastric cancer and its impact on survival outcomes--a systematic review. Int J Cancer 2012; 130: 2845-2856. [PMID: 21780108 DOI: 10.1002/ijc.26292]
32. Fornaro L, Lucchesi M, Caparello C, Vasile E, Caponi S, Ginocchi L, Masi G, Falcone A. Anti-HER agents in gastric cancer: from bench to bedside. Nat Rev Gastroenterol Hepatol 2011; 8: 369-383. [PMID: 21647199 DOI: 10.1038/nrgastro.2011.81.]
33. Jain S, Filipe MI, Gullick WJ, Linehan J, Morris RW. c-erbB-2 proto-oncogene expression and its relationship to survival in gastric carcinoma: an immunohistochemical study on archival material. Int J Cancer 1991; 48: 668-671. [PMID: 1676988 DOI: 10.1002/ijc.2910480506]
34. Janjigian YY, Werner D, Pauligk C, Steinmetz K, Kelsen DP, Jäger E, Altmannsberger HM, Robinson E, Tafe LJ, Tang LH, Shah MA, Al-Batran SE. Prognosis of metastatic gastric and gastroesophageal junction cancer by HER2 status: a European and USA International collaborative analysis. Ann Oncol 2012; 23: 2656-2662. [PMID: 22689179 DOI: 10.1093/annonc/mds104]
35. ClinicalTrials. gov. Available from: URL: http://www.clinicaltrials.gov/ct2/results?term=GastricCancerANDHER2&pg=3
36. Gonzales AJ, Hook KE, Althaus IW, Ellis PA, Trachet E, Delaney AM, Harvey PJ, Ellis TA, Amato DM, Nelson JM, Fry DW, Zhu T, Loi CM, Fakhoury SA, Schlosser KM, Sexton KE, Winters RT, Reed JE, Bridges AJ, Lettiere DJ, Baker DA, Yang J, Lee HT, Tecle H, Vincent PW. Antitumor activity and pharmacokinetic properties of PF-00299804, a secondgeneration irreversible pan-erbB receptor tyrosine kinase inhibitor. Mol Cancer Ther 2008; 7: 1880-1889. [PMID: 18606718 DOI: 10.1158/1535-7163.MCT-07-2232]
37. Nam HJ, Ching KA, Kan J, Kim HP, Han SW, Im SA, Kim TY, Christensen JG, Oh DY, Bang YJ. Evaluation of the antitumor effects and mechanisms of PF00299804, a pan-HER inhibitor, alone or in combination with chemotherapy or targeted agents in gastric cancer. Mol Cancer Ther 2012; 11: 439-451. [PMID: 22135232 DOI: 10.1158/1535-7163.MCT-11-0494]
38. Oh DY, Lee KW, Cho J Y, Kang WK, Rha SY, Bang YJ. Aphase II open-label trial of dacomitinib monotherapy in patients with HER2-positive advanced gastric cancer after failure of at least one prior chemotherapy regimen. J Clin Oncol 2012; 30 suppl 4: Abstract 54
39. Kwak E. The role of irreversible HER family inhibition in the treatment of patients with non-small cell lung cancer. Oncologist 2011; 16: 1498-1507. [PMID: 22016476 DOI: 10.1634/theoncologist]
40. Food and Drug Administration. Afatinib. July 12, 2013. Available from: URL: http://www.fda.gov/Drugs/InformationOnDrugs/ApprovedDrugs/ucm360574.htm
41. Janjigian YY, Viola-Villegas N, Holland JP, Divilov V, Carlin SD, Gomes-DaGama EM, Chiosis G, Carbonetti G, de Stanchina E, Lewis JS. Monitoring afatinib treatment in HER2-positive gastric cancer with 18F-FDG and 89Zr-trastuzumab PET. J Nucl Med 2013; 54: 936-943. [PMID: 23578997 DOI: 10.2967/jnumed.112.110239]
42. Janjigian YY, Capanu M, Gromisch CM, Kelsen DP, Ku GY, Brown KT, Schattner M, Ilson DH, Solit DB, Berger MF, Vakiani E. A phase II study of afatinib in patients (pts) with metastatic human epidermal growth factor receptor (HER2)-positive trastuzumab-refractory esophagogastric (EG) cancer. J Clin Oncol 2013; 31 suppl: Abstract e15017
43. Food and Drug Administration. TYKERB (lapatinib) tablets. Prescribing Information. February 2012. Available from: URL: http://www.accessdata.fda.gov/drugsatfda_docs/label/2012/022059s013lbl.pdf
44. Kim JW, Kim HP, Im SA, Kang S, Hur HS, Yoon YK, Oh DY, Kim JH, Lee DS, Kim TY, Bang YJ. The growth inhibitory effect of lapatinib, a dual inhibitor of EGFR and HER2 tyrosine kinase, in gastric cancer cell lines. Cancer Lett 2008; 272: 296-306. [PMID: 18774637 DOI: 10.1016/j.canlet.2008.07.018]
45. Iqbal S, Goldman B, Fenoglio-Preiser CM, Lenz HJ, Zhang W, Danenberg KD, Shibata SI, Blanke CD. Southwest Oncology Group study S0413: a phase II trial of lapatinib (GW572016) as first-line therapy in patients with advanced or metastatic gastric cancer. Ann Oncol 2011; 22: 2610-2615. [PMID: 21415234 DOI: 10.1093/annonc/mdr021]
46. Hecht JR, Bang YJ, Qin S, Chung HC, Xu JM, Park JO, Jeziorski K, Shparyk Y, Hoff PM, Sobrero AF, Salman P, Li J, Protsenko S, Buyse ME, Afenjar K, Kaneko T, Kemner A, Santillana S, Press MF, Slamon DJ. Lapatinib in combination with capecitabine plus oxaliplatin (CapeOx) in HER2-positive advanced or metastatic gastric, esophageal, or gastroesophageal adenocarcinoma (AC): The TRIO-013/LOGiCTrial. J Clin Oncol 2013; 31 suppl: Abstract LBA4001
47. Satoh T, Bang Y, Wang J, Xu J, Chung HC, Yeh K, Chen J, Mukaiyama A, Yoshida P, Ohtsu A. Interim safety analysis from TYTAN: A phase III Asian study of lapatinib in combination with paclitaxel as second-line therapy in gastric cancer. J Clin Oncol 2010; 28 Suppl: Abstract 4057
48. Cho HS, Mason K, Ramyar KX, Stanley AM, Gabelli SB, Denney DW, Leahy DJ. Structure of the extracellular region of HER2 alone and in complex with the Herceptin Fab. Nature 2003; 421: 756-760. [PMID: 12610629 DOI: 10.1038/nature01392]
49. Franklin MC, Carey KD, Vajdos FF, Leahy DJ, de Vos AM, Sliwkowski MX. Insights into ErbB signaling from the structure of the ErbB2-pertuzumab complex. Cancer Cell 2004; 5: 317-328. [PMID: 15093539 DOI: 10.1016/S1535-6108(04)00083-2]
50. Baselga J, Cortés J, Kim SB, Im SA, Hegg R, Im YH, Roman L, Pedrini JL, Pienkowski T, Knott A, Clark E, Benyunes MC, Ross G, Swain SM; CLEOPATRA Study Group. Pertuzumab plus trastuzumab plus docetaxel for metastatic breast cancer. N Engl J Med 2012; 366: 109-119. [PMID: 22149875 DOI: 10.1056/NEJMoa1113216]
51. Yamashita-Kashima Y, Iijima S, Yorozu K, Furugaki K, Kurasawa M, Ohta M, Fujimoto-Ouchi K. Pertuzumab in combination with trastuzumab shows significantly enhanced antitumor activity in HER2-positive human gastric cancer xenograft models. Clin Cancer Res 2011; 17: 5060-5070. [PMID: 21700765 DOI: 10.1158/1078-0432.CCR-10-2927]
52. ClinicalTrials.gov. A Study of Pertuzumab in Combination with Trastuzumab and Chemotherapy in Patients With HER2-Positive Advanced Gastric Cancer (NCT014610579). Available from: URL: http://clinicaltrials.gov/show/NCT014610579
53. ClinicalTrials.gov. A Study of Perjeta (Pertuzumab) in Combination with Herceptin (Trastuzumab) and Chemotherapy in Patients with HER2-Positive Metastatic Gastroesophageal Junction or Gastric Cancer (NCT01774786). Available from: URL: http://clinicaltrials.gov/show/NCT01774786
54. Tabernero J, Hoff PM, Shen L, Ohtsu A, Yu R, Eng-Wong J, Kang YK. Pertuzumab (P) with trastuzumab (T) and chemotherapy (CTX) in patients (pts) with HER2-positive metastatic gastric or gastroesophageal junction (GEJ) cancer: An international phase III study (JACOB). J Clin Oncol 2013; 31: Abstract TPS4150
55. Lewis Phillips GD, Li G, Dugger DL, Crocker LM, Parsons KL, Mai E, Blättler WA, Lambert JM, Chari RV, Lutz RJ, Wong WL, Jacobson FS, Koeppen H, Schwall RH, Kenkare-Mitra SR, Spencer SD, Sliwkowski MX. Targeting HER2-positive breast cancer with trastuzumab-DM1, an antibodycytotoxic drug conjugate. Cancer Res 2008; 68: 9280-9290. [PMID: 19010901 DOI: 10.1158/0008-5472]
56. Verma S, Miles D, Gianni L, Krop IE, Welslau M, Baselga J, Pegram M, Oh DY, Diéras V, Guardino E, Fang L, Lu MW, Olsen S, Blackwell K. Trastuzumab emtansine for HER2-positive advanced breast cancer. N Engl J Med 2012; 367: 1783-1791. [PMID: 23020162 DOI: 10.1056/NEJMoa1209124]
57. Barok M, Tanner M, Köninki K, Isola J. Trastuzumab-DM1 is highly effective in preclinical models of HER2-positive gastric cancer. Cancer Lett 2011; 306: 171-179. [PMID: 21458915 DOI: 10.1016/j.canlet.2011.03.002]
58. Yamashita-Kashima Y, Shu S, Harada N, Fujimoto-Ouchi K. Enhanced antitumor activity of trastuzumab emtansine (T-DM1) in combination with pertuzumab in a HER2-positive gastric cancer model. Oncol Rep 2013; 30: 1087-1093. [PMID: 23783223 DOI: 10.3892/or.2013.2547]
59. ClinicalTrials.gov. A Study of Trastuzumab Emtansine versus Taxane in Patients with Advanced Gastric Cancer. Available from: URL: http://clinicaltrials.gov/ct2/show/NCT01641939?term=Trastuzumabemtansine&rank=6