Apoptosis in Carcinogenesis and Chemotherapy – Esophageal Cancer

  • Yan Li
  • Robert C.G. Martin

Abstract

Esophageal cancer is the sixth most common cause of cancer-related death. Esophageal carcinoma can be divided in squamous cell carcinoma and adenocarcinoma by histopathology, and these two main histologic types of esophageal cancer are quite different in many aspects. Apoptosis in esophageal cancer has been extensively studied, and a recognized mechanism for the development of esophageal cancer is an imbalance between cell renewal and cell death, with apoptosis being inhibited. The inability of esophageal cancer to undergo apoptosis when presented with an insult is an important indicator of the propensity for the esophageal malignant transformation. Many of the molecular events necessary for activation, amplification and execution of the apoptotic process in esophageal cancer, and it is evident that diverse drugs can kill esophageal tumor cells through activating common apoptotic pathways. In the last decade, it has been demonstrated that resistance to apoptotic stimuli is a hallmark feature of esophageal cancer and a complex network of pro- and anti-apoptotic proteins that governs the tight regulation along apoptotic pathways in regards of esophageal carcinogenesis and chemotherapy is revealed, and these findings could lead to the identification of several new molecular targets for chemoprevention and chemotherapy in esophageal cancer.

Keywords

Apoptosis Chemoprevention Esophageal Carcinoma 

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. Alderson MR, Tough TW, Davis-Smith T, Braddy S, Falk B, Schooley KA, Goodwin RG, Smith CA, Ramsdell F, Lynch DH (1995) Fas ligand mediates activation-induced cell death in human T lymphocytes. J Exp Med 181:71–77PubMedGoogle Scholar
  2. Altorki NK, Oliveria S, Schrump DS (1997) Epidemiology and molecular biology of Barrett’s adenocarcinoma. Seminars in Surgical Oncology 13:270–280PubMedGoogle Scholar
  3. Anani PA, Gardiol D, Savary M, Monnier P (1991) An extensive morphological and comparative study of clinically early and obvious squamous cell carcinoma of the esophagus. Pathol Res Pract 187:214–219PubMedGoogle Scholar
  4. Ashkenazi A (2002) Targeting death and decoy receptors of the tumour-necrosis factor superfamily. Nat Rev Cancer 2:420–430PubMedGoogle Scholar
  5. Ashkenazi A, Dixit VM (1998) Death receptors: signaling and modulation. Science 281:1305–1308Google Scholar
  6. Ashkenazi A, Pai RC, Fong S, Leung S, Lawrence DA, Marsters SA, Blackie C, Chang L, McMurtrey AE, Hebert A, DeForge L, Koumenis IL, Lewis D, Harris L, Bussiere J, Koeppen H, Shahrokh Z, Schwall RH (1999) Safety and antitumor activity of recombinant soluble Apo2 ligand. J Clin Invest 104:155–162PubMedGoogle Scholar
  7. Azmi S, Dinda AK, Chopra P, Chattopadhyay TK, Singh N (2000) Bcl-2 expression is correlated with low apoptotic index and associated with histopathological grading in esophageal squamous cell carcinomas. Tumour Biol 21:3–10PubMedGoogle Scholar
  8. Beer DG, Stoner GD (1998) Clinical models of chemoprevention for the esophagus. Hematology-Oncology Clinics of North America 12:1055–1077Google Scholar
  9. Bennett MW, O’Connell J, O’Sullivan GC, Brady C, Roche D, Collins JK, Shanahan F (1998) The Fas counterattack in vivo: apoptotic depletion of tumor-infiltrating lymphocytes associated with Fas ligand expression by human esophageal carcinoma, J Immunol 160:5669–5675PubMedGoogle Scholar
  10. Bennett MW, O’Connell J, O’Sullivan GC, Roche D, Brady C, Collins JK, Shanahan F (1999) Fas ligand and Fas receptor are coexpressed in normal human esophageal epithelium: a potential mechanism of apoptotic epithelial turnover. Dis Esophagus 12:90–98PubMedGoogle Scholar
  11. Bian YS, Osterheld MC, Bosman FT, Benhattar J, Fontolliet C (2001) p53 gene mutation and protein accumulation during neoplastic progression in Barrett’s esophagus. Mod Pathol 14:397–403PubMedGoogle Scholar
  12. Blot WJ, Devesa SS, Kneller RW, Fraumeni JF (1991) Rising incidence of adenocarcinoma of the esophagus and gastric cardia. Jama-Journal of the American Medical Association 265:1287–1289Google Scholar
  13. Bunz F, Hwang PM, Torrance C, Waldman T, Zhang Y, Dillehay L, Williams J, Lengauer C, Kinzler KW, Vogelstein B (1999) Disruption of p53 in human cancer cells alters the responses to therapeutic agents. J Clin Invest 104:263–269Google Scholar
  14. Cameron AJ (1997) Barrett’s esophagus: Does the incidence of adenocarcinoma matter? Am J Gastroenterol 92:193–194Google Scholar
  15. Casson AG (1998) Molecular biology of Barrett’s esophagus and esophageal cancer: role of p53. World J Gastroenterol 4:277–279PubMedGoogle Scholar
  16. Casson AG, Mukhopadhyay T, Cleary KR, Ro JY, Levin B, Roth JA (1991) p53 gene mutations in Barrett’s epithelium and esophageal cancer. Cancer Res 51:4495–4499PubMedGoogle Scholar
  17. Chan KW, Lee PY, Lam AK, Law S, Wong J, Srivastava G (2006) Clinical relevance of Fas expression in oesophageal squamous cell carcinoma. J Clin Pathol 59:101–104PubMedGoogle Scholar
  18. Chang MS, Lee HS, Lee BL, Kim YT, Lee JS, Kim WH (2005) Differential protein expression between esophageal squamous cell carcinoma and dysplasia, and prognostic significance of protein markers. Pathol Res Pract 201:417–425PubMedGoogle Scholar
  19. Chatzopoulos D, Kyrgidis A, Kountouras J, Zavos C, Molyvas E, Venizelos I (2007) Bax upregulation may provide a rationale for the low incidence of esophageal adenocarcinoma in a Greek cohort of patients with Barrett’s esophagus. Hepatogastroenterology 54:705–709PubMedGoogle Scholar
  20. Chen XX, Yang CS (2001) Esophageal adenocarcinoma: a review and perspectives on the mechanism of carcinogenesis and chemoprevention. Carcinogenesis 22:1119–1129PubMedGoogle Scholar
  21. Cheng EH, Wei MC, Weiler S, Flavell RA, Mak TW, Lindsten T, Korsmeyer SJ (2001) BCL-2, BCL-X(L) sequester BH3 domain-only molecules preventing BAX- and BAK-mediated mitochondrial apoptosis. Mol Cell 8:705–711PubMedGoogle Scholar
  22. Chung SM, Kao J, Hyjek E, Chen YT (2007) p53 in esophageal adenocarcinoma: a critical reassessment of mutation frequency and identification of 72Arg as the dominant allele. Int J Oncol 31:1351–1355PubMedGoogle Scholar
  23. Clark GW, Smyrk TC, Burdiles P, Hoeft SF, Peters JH, Kiyabu M, Hinder RA, Bremner CG, Demeester TR (1994) Is Barrett’s metaplasia the source of adenocarcinomas of the cardia? Arch Surg 129:609–614Google Scholar
  24. Clem RJ, Sheu TT, Richter BW, He WW, Thornberry NA, Duckett CS, Hardwick JM (2001) c-IAP1 is cleaved by caspases to produce a proapoptotic C-terminal fragment. J Biol Chem 276:7602–7608PubMedGoogle Scholar
  25. Cleveland JL, Ihle JN (1995) Contenders in FasL/TNF death signaling. Cell 81:479–482PubMedGoogle Scholar
  26. Coggi G, Bosari S, Roncalli M, Graziani D, Bossi P, Viale G, Buffa R, Ferrero S, Piazza M, Blandamura S, Segalin A, Bonavina L, Peracchia A (1997) p53 protein accumulation and p53 gene mutation in esophageal carcinoma. A molecular and immunohistochemical study with clinicopathologic correlations. Cancer 79:425–432Google Scholar
  27. Degterev A, Boyce M, Yuan J (2003) A decade of caspases. Oncogene 22:8543–8567PubMedGoogle Scholar
  28. Deveraux QL, Stennicke HR, Salvesen GS, Reed JC (1999) Endogenous inhibitors of caspases. J Clin Immunol 19:388–398PubMedGoogle Scholar
  29. Djalilvand A, Pal R, Goldman H, Antonioli D, Kocher O (2004) Evaluation of p53 mutations in premalignant esophageal lesions and esophageal adenocarcinoma using laser capture microdissection. Mod Pathol 17:1323–1327PubMedGoogle Scholar
  30. Doak SH, Jenkins GJ, Parry EM, Griffiths AP, Shah V, Baxter JN, Parry JM (2003) Characterisation of p53 status at the gene, chromosomal and protein levels in oesophageal adenocarcinoma. Br J Cancer 89:1729–1735PubMedGoogle Scholar
  31. Dolan K, Walker SJ, Gosney J, Field JK, Sutton R (2003) TP53 mutations in malignant and premalignant Barrett’s esophagus. Dis Esophagus 16:83–89PubMedGoogle Scholar
  32. Duhaylongsod FG, Gottfried MR, Iglehart JD, Vaughn AL, Wolfe WG (1995) The significance of c-erb B-2 and p53 immunoreactivity in patients with adenocarcinoma of the esophagus. Ann Surg 221:677–683PubMedGoogle Scholar
  33. Egashira A, Morita M, Kakeji Y, Sadanaga N, Oki E, Honbo T, Ohta M, Maehara Y (2007) p53 gene mutations in esophageal squamous cell carcinoma and their relevance to etiology and pathogenesis: results in Japan and comparisons with other countries. Cancer Sci 98:1152–1156PubMedGoogle Scholar
  34. El Deiry WS, Tokino T, Velculescu VE, Levy DB, Parsons R, Trent JM, Lin D, Mercer WE, Kinzler KW, Vogelstein B (1993) WAF1, a potential mediator of p53 tumor suppression. Cell 75:817–825PubMedGoogle Scholar
  35. el Serag HB (2002) The epidemic of esophageal adenocarcinoma. Gastroenterol Clin North Am 31:421–440, viiiPubMedGoogle Scholar
  36. Enzinger PC, Mayer RJ (2003) Esophageal cancer. N Engl J Med 349:2241–2252PubMedGoogle Scholar
  37. Faried A, Faried LS, Kimura H, Sohda M, Nakajima M, Miyazaki T, Kato H, Kanuma T, Kuwano H (2006) Differential sensitivity of paclitaxel-induced apoptosis in human esophageal squamous cell carcinoma cell lines. Cancer Chemother Pharmacol 57:301–308PubMedGoogle Scholar
  38. Faried A, Faried LS, Nakagawa T, Yamauchi T, Kitani M, Sasabe H, Nishimura T, Usman N, Kato H, Asao T, Kuwano H, Yazawa S (2007) Chemically synthesized sugar-cholestanols possess a preferential anticancer activity involving promising therapeutic potential against human esophageal cancer. Cancer Sci 98:1358–1367PubMedGoogle Scholar
  39. Farrow DC, Vaughan TL (1996) Determinants of survival following the diagnosis of esophageal adenocarcinoma (United States) Cancer Causes & Control 7:322–327Google Scholar
  40. Fitzgerald RC, Triadafilopoulos G (1998) Recent developments in the molecular characterization of Barrett’s esophagus. Digestive Diseases 16:63–80PubMedGoogle Scholar
  41. Fridman JS, Lowe SW (2003) Control of apoptosis by p53. Oncogene 22:9030–9040PubMedGoogle Scholar
  42. Gleeson CM, Sloan JM, McGuigan JA, Ritchie AJ, Russell SE (1995) Base transitions at CpG dinucleotides in the p53 gene are common in esophageal adenocarcinoma. Cancer Res 55:3406–3411PubMedGoogle Scholar
  43. Gleeson CM, Sloan JM, McManus DT, Maxwell P, Arthur K, McGuigan JA, Ritchie AJ, Russell SE (1998) Comparison of p53 and DNA content abnormalities in adenocarcinoma of the oesophagus and gastric cardia. Br J Cancer 77:277–286PubMedGoogle Scholar
  44. Goldblum JR, Rice TW (1995) bcl-2 protein expression in the Barrett’s metaplasia-dysplasia-carcinoma sequence. Mod Pathol 8:866–869PubMedGoogle Scholar
  45. Gonzalez MV, Artimez ML, Rodrigo L, Lopez-Larrea C, Menendez MJ, Alvarez V, Perez R, Fresno MF, Perez MJ, Sampedro A, Coto E (1997) Mutation analysis of the p53, APC, and p16 genes in the Barrett’s oesophagus, dysplasia, and adenocarcinoma. J Clin Pathol 50:212–217PubMedGoogle Scholar
  46. Gratas C, Tohma Y, Barnas C, Taniere P, Hainaut P, Ohgaki H (1998) Up-regulation of Fas (APO-1/CD95) ligand and down-regulation of Fas expression in human esophageal cancer. Cancer Res 58:2057–2062PubMedGoogle Scholar
  47. Greenawalt DM, Duong C, Smyth GK, Ciavarella ML, Thompson NJ, Tiang T, Murray WK, Thomas RJ, Phillips WA (2007) Gene expression profiling of esophageal cancer: comparative analysis of Barrett’s esophagus, adenocarcinoma, and squamous cell carcinoma. Int J Cancer 120:1914–1921PubMedGoogle Scholar
  48. Guicciardi ME, Gores GJ (2005) Apoptosis: a mechanism of acute and chronic liver injury. Gut 54:1024–1033PubMedGoogle Scholar
  49. Hamelin R, Flejou JF, Muzeau F, Potet F, Laurent-Puig P, Fekete F, Thomas G (1994) TP53 gene mutations and p53 protein immunoreactivity in malignant and premalignant Barrett’s esophagus. Gastroenterology 107:1012–1018PubMedGoogle Scholar
  50. Han U, Can OI, Han S, Kayhan B, Onal BU (2007) Expressions of p53, VEGF C, p21: could they be used in preoperative evaluation of lymph node metastasis of esophageal squamous cell carcinoma? Dis Esophagus 20:379–385Google Scholar
  51. Hanahan D, Weinberg RA (2000) The hallmarks of cancer. Cell 100:57–70PubMedGoogle Scholar
  52. Heeren PA, Kloppenberg FW, Hollema H, Mulder NH, Nap RE, Plukker JT (2004) Predictive effect of p53 and p21 alteration on chemotherapy response and survival in locally advanced adenocarcinoma of the esophagus. Anticancer Res 24:2579–2583PubMedGoogle Scholar
  53. Herr I, Debatin KM (2001) Cellular stress response and apoptosis in cancer therapy. Blood 98:2603–2614PubMedGoogle Scholar
  54. Hollstein M, Sidransky D, Vogelstein B, Harris CC (1991) p53 mutations in human cancers. Science 253:49–53PubMedGoogle Scholar
  55. Holmes RS, Vaughan TL (2007) Epidemiology and pathogenesis of esophageal cancer. Semin Radiat Oncol 17:2–9PubMedGoogle Scholar
  56. Hong MK, Laskin WB, Herman BE, Johnston MH, Vargo JJ, Steinberg SM, Allegra CJ, Johnston PG (1995) Expansion of the Ki-67 proliferative compartment correlates with degree of dysplasia in Barretts esophagus. Cancer 75:423–429PubMedGoogle Scholar
  57. Hong WK, Sporn MB (1997) Recent advances in chemoprevention of cancer. Science 278:1073–1077PubMedGoogle Scholar
  58. Houston A, O’Connell J (2004) The Fas signalling pathway and its role in the pathogenesis of cancer. Curr Opin Pharmacol 4:321–326PubMedGoogle Scholar
  59. Hsia JY, Chen CY, Chen JT, Hsu CP, Shai SE, Yang SS, Chuang CY, Wang PY, Miaw J (2003) Prognostic significance of caspase-3 expression in primary resected esophageal squamous cell carcinoma. Eur J Surg Oncol 29:44–48PubMedGoogle Scholar
  60. Hsia JY, Chen CY, Hsu CP, Shai SE, Yang SS, Chuang CY, Wang PY, Chen JT (2001) Expression of apoptosis-regulating proteins p53, Bcl-2, and Bax in primary resected esophageal squamous cell carcinoma. Neoplasma 48:483–488PubMedGoogle Scholar
  61. Hughes SJ, Nambu Y, Soldes OS, Hamstra D, Rehemtulla A, Iannettoni MD, Orringer MB, Beer DG (1997) Fas/APO-1 (CD95) is not translocated to the cell membrane in esophageal adenocarcinoma. Cancer Res 57:5571–5578PubMedGoogle Scholar
  62. Ikeguchi M, Maeta M, Kaibara N (2001) Bax expression as a prognostic marker of postoperative chemoradiotherapy for patients with esophageal cancer. Int J Mol Med 7:413–417PubMedGoogle Scholar
  63. Imoto I, Yang ZQ, Pimkhaokham A, Tsuda H, Shimada Y, Imamura M, Ohki M, Inazawa J (2001) Identification of cIAP1 as a candidate target gene within an amplicon at 11q22 in esophageal squamous cell carcinomas. Cancer Res 61:6629–6634PubMedGoogle Scholar
  64. Ireland AP, Shibata DK, Chandrasoma P, Lord RV, Peters JH, Demeester TR (2000) Clinical significance of p53 mutations in adenocarcinoma of the esophagus and cardia. Ann Surg 231:179–187PubMedGoogle Scholar
  65. Isolauri J, Luostarinen M, Isolauri E, Reinikainen P, Viljakka M, Keyrilainen O (1997) Natural course of gastroesophageal reflux disease: 17–22 year follow-up of 60 patients. Am J Gastroenterol 92:37–41PubMedGoogle Scholar
  66. Jankowski JA, Wright NA, Meltzer SJ, Triadafilopoulos G, Geboes K, Casson AG, Kerr D, Young LS (1999) Molecular evolution of the metaplasia-dysplasia-adenocarcinoma sequence in the esophagus. Am J Pathol 154:965–973PubMedGoogle Scholar
  67. Jemal A, Murray T, Ward E, Samuels A, Tiwari RC, Ghafoor A, Feuer EJ, Thun MJ (2005) Cancer statistics, 2005. CA Cancer J Clin 55:10–30PubMedGoogle Scholar
  68. Jo M, Kim TH, Seol DW, Esplen JE, Dorko K, Billiar TR, Strom SC (2000) Apoptosis induced in normal human hepatocytes by tumor necrosis factor-related apoptosis-inducing ligand. Nat Med 6:564–567PubMedGoogle Scholar
  69. Kan T, Shimada Y, Sato F, Maeda M, Kawabe A, Kaganoi J, Itami A, Yamasaki S, Imamura M (2001) Gene expression profiling in human esophageal cancers using cDNA microarray. Biochem Biophys Res Commun 286:792–801PubMedGoogle Scholar
  70. Kanemitsu S, Ihara K, Saifddin A, Otsuka T, Takeuchi T, Nagayama J, Kuwano M, Hara T (2002) A functional polymorphism in fas (CD95/APO-1) gene promoter associated with systemic lupus erythematosus. J Rheumatol 29:1183–1188PubMedGoogle Scholar
  71. Katada N, Hinder RA, Smyrk TC, Hirabayashi N, Perdikis G, Lund RJ, Woodward T, Klingler PJ (1997) Apoptosis is inhibited early in the dysplasia-carcinoma sequence of Barrett esophagus. Arch Surg 132:728–733PubMedGoogle Scholar
  72. Kato J, Kuwabara Y, Mitani M, Shinoda N, Sato A, Toyama T, Mitsui A, Nishiwaki T, Moriyama S, Kudo J, Fujii Y (2001) Expression of survivin in esophageal cancer: correlation with the prognosis and response to chemotherapy. Int J Cancer 95:92–95PubMedGoogle Scholar
  73. Kerr JF, Wyllie AH, Currie AR (1972) Apoptosis: a basic biological phenomenon with wide-ranging implications in tissue kinetics. Br J Cancer 26:239–257PubMedGoogle Scholar
  74. Kim SH, Kim K, Kwagh JG, Dicker DT, Herlyn M, Rustgi AK, Chen Y, El Deiry WS (2004) Death induction by recombinant native TRAIL and its prevention by a caspase 9 inhibitor in primary human esophageal epithelial cells. J Biol Chem 279:40044–40052PubMedGoogle Scholar
  75. Kondo K, Yamasaki S, Inoue N, Sugie T, Teratani N, Kan T, Shimada Y (2006a) Prospective antitumor effects of the combination of tumor necrosis factor-related apoptosis-inducing ligand (TRAIL) and cisplatin against esophageal squamous cell carcinoma. Surg Today 36:966–974Google Scholar
  76. Kondo K, Yamasaki S, Sugie T, Teratani N, Kan T, Imamura M, Shimada Y (2006b) Cisplatin-dependent upregulation of death receptors 4 and 5 augments induction of apoptosis by TNF-related apoptosis-inducing ligand against esophageal squamous cell carcinoma. Int J Cancer 118:230–242Google Scholar
  77. Kozlowski M, Kowalczuk O, Sulewska A, Dziegielewski P, Lapuc G, Laudanski W, Niklinska W, Chyczewski L, Niklinski J, Laudanski J (2007) Serum soluble Fas ligand (sFasL) in patients with primary squamous cell carcinoma of the esophagus. Folia Histochem Cytobiol 45:199–204Google Scholar
  78. Kroemer G (1997) The proto-oncogene Bcl-2 and its role in regulating apoptosis. Nat Med 3:614–620PubMedGoogle Scholar
  79. Kurabayashi A, Furihata M, Matsumoto M, Ohtsuki Y, Sasaguri S, Ogoshi S (2001) Expression of Bax and apoptosis-related proteins in human esophageal squamous cell carcinoma including dysplasia. Mod Pathol 14:741–747PubMedGoogle Scholar
  80. Kuwano H, Watanabe M, Sadanaga N, Ikebe M, Mori M, Sugimachi K (1993) Squamous epithelial dysplasia associated with squamous cell carcinoma of the esophagus. Cancer Lett 72:141–147PubMedGoogle Scholar
  81. Lam KY, Law S, Ma LT, Ong SK, Wong J (1997) Pre-operative chemotherapy for squamous cell carcinoma of the oesophagus: do histological assessment and p53 overexpression predict chemo-responsiveness? Eur J Cancer 33:1221–1225Google Scholar
  82. Lane DP (1994) p53 and human cancers. Br Med Bull 50:582–599PubMedGoogle Scholar
  83. Levine AJ, Momand J, Finlay CA (1991) The p53 tumour suppressor gene. Nature 351:453–456PubMedGoogle Scholar
  84. Li WD, Wang MJ, Ding F, Yin DL, Liu ZH (2005) Cytotoxic effect of a non-peptidic small molecular inhibitor of the p53-HDM2 interaction on tumor cells. World J Gastroenterol 11:2927–2931PubMedGoogle Scholar
  85. Liston P, Fong WG, Korneluk RG (2003) The inhibitors of apoptosis: there is more to life than Bcl2. Oncogene 22:8568–8580PubMedGoogle Scholar
  86. Lowe SW, Lin AW (2000) Apoptosis in cancer. Carcinogenesis 21:485–495PubMedGoogle Scholar
  87. Lutter M, Fang M, Luo X, Nishijima M, Xie X, Wang X (2000) Cardiolipin provides specificity for targeting of tBid to mitochondria. Nat Cell Biol 2:754–761PubMedGoogle Scholar
  88. Ma G, Yang C, Qu Y, Wei H, Zhang T, Zhang N (2007) The flavonoid component isorhamnetin in vitro inhibits proliferation and induces apoptosis in Eca-109 cells. Chem Biol Interact 167:153–160PubMedGoogle Scholar
  89. MacFarlane M, Ahmad M, Srinivasula SM, Fernandes-Alnemri T, Cohen GM, Alnemri ES (1997) Identification and molecular cloning of two novel receptors for the cytotoxic ligand TRAIL. J Biol Chem 272:25417–25420PubMedGoogle Scholar
  90. Michel P, Magois K, Robert V, Chiron A, Lepessot F, Bodenant C, Roque I, Seng SK, Frebourg T, Paillot B (2002) Prognostic value of TP53 transcriptional activity on p21 and bax in patients with esophageal squamous cell carcinomas treated by definitive chemoradiotherapy. Int J Radiat Oncol Biol Phys 54:379–385PubMedGoogle Scholar
  91. Mir MM, Dar NA, Gochhait S, Zargar SA, Ahangar AG, Bamezai RN (2005) p53 mutation profile of squamous cell carcinomas of the esophagus in Kashmir (India): a high-incidence area. Int J Cancer 116:62–68PubMedGoogle Scholar
  92. Muro K, Ohtsu A, Boku N, Chin K, Oda Y, Fujii T, Hosokawa K, Yoshida S, Hasebe T (1996) Association of p53 protein expression with responses and survival of patients with locally advanced esophageal carcinoma treated with chemoradiotherapy. Jpn J Clin Oncol 26:65–69PubMedGoogle Scholar
  93. Nabeya Y, Loganzo F, Jr., Maslak P, Lai L, de Oliveira AR, Schwartz GK, Blundell ML, Altorki NK, Kelsen DP, Albino AP (1995) The mutational status of p53 protein in gastric and esophageal adenocarcinoma cell lines predicts sensitivity to chemotherapeutic agents. Int J Cancer 64:37–46PubMedGoogle Scholar
  94. Nachmias B, Ashhab Y, Bucholtz V, Drize O, Kadouri L, Lotem M, Peretz T, Mandelboim O, Ben Yehuda D (2003) Caspase-mediated cleavage converts Livin from an antiapoptotic to a proapoptotic factor: implications for drug-resistant melanoma. Cancer Res 63:6340–6349PubMedGoogle Scholar
  95. Nagata S (1997) Apoptosis by death factor. Cell 88:355–365PubMedGoogle Scholar
  96. Nakashima S, Natsugoe S, Matsumoto M, Kijima F, Takebayashi Y, Okumura H, Shimada M, Nakano S, Kusano C, Baba M, Takao S, Aikou T (2000) Expression of p53 and p21 is useful for the prediction of preoperative chemotherapeutic effects in esophageal carcinoma. Anticancer Res. 20:1933–1937PubMedGoogle Scholar
  97. Natsugoe S, Matsumoto M, Okumura H, Nakashima S, Sakamoto F, Sakita H, Baba M, Takao S, Aikou T (2001) Bax and Bcl-X(L) expression are not related to prognosis in patients with advanced esophageal squamous cell carcinoma. Cancer Lett 174:91–97PubMedGoogle Scholar
  98. Nebel OT, Fornes MF, Castell DO (1976) Symptomatic gastroesophageal reflux – incidence and precipitating factors. Am J Digest Dis 21:953–956PubMedGoogle Scholar
  99. Nemoto T, Kitagawa M, Hasegawa M, Ikeda S, Akashi T, Takizawa T, Hirokawa K, Koike M (2004) Expression of IAP family proteins in esophageal cancer. Exp Mol Pathol 76:253–259PubMedGoogle Scholar
  100. Neshat K, Sanchez CA, Galipeau PC, Blount PL, Levine DS, Joslyn G, Reid BJ (1994) p53 mutations in Barrett’s adenocarcinoma and high-grade dysplasia. Gastroenterology 106:1589–1595PubMedGoogle Scholar
  101. Ngan CY, Yamamoto H, Takagi A, Fujie Y, Takemasa I, Ikeda M, Takahashi-Yanaga F, Sasaguri T, Sekimoto M, Matsuura N, Monden M (2008) Oxaliplatin induces mitotic catastrophe and apoptosis in esophageal cancer cells. Cancer Sci 99:129–139PubMedGoogle Scholar
  102. O’Connell J, Bennett MW, O’Sullivan GC, Collins JK, Shanahan F (1999) Resistance to Fas (APO-1/CD95)-mediated apoptosis and expression of Fas ligand in esophageal cancer: the Fas counterattack. Dis Esophagus 12:83–89PubMedGoogle Scholar
  103. Ogunwobi OO, Beales IL (2008) Statins inhibit proliferation and induce apoptosis in barrett’s esophageal adenocarcinoma cells. Am J Gastroenterol 103:838–841Google Scholar
  104. Ouatu-Lascar R, Fitzgerald RC, Triadafilopoulos G (1999) Differentiation and proliferation in Barrett’s esophagus and the effects of acid suppression. Gastroenterology 117:327–335PubMedGoogle Scholar
  105. Pan G, Ni J, Yu G, Wei YF, Dixit VM (1998) TRUNDD, a new member of the TRAIL receptor family that antagonizes TRAIL signalling. FEBS Lett 424:41–45PubMedGoogle Scholar
  106. Parkin DM, Bray F, Ferlay J, Pisani P (2005) Global cancer statistics, 2002. CA Cancer J Clin 55:74–108PubMedGoogle Scholar
  107. Pera M, Cameron AJ, Trastek VF, Carpenter HA, Zinsmeister AR (1993) Increasing incidence of adenocarcinoma of the esophagus and esophagogastric junction. Gastroenterology 104:510–513PubMedGoogle Scholar
  108. Pera M, Manterola C, Vidal O, Grande L (2005) Epidemiology of esophageal adenocarcinoma. J Surg Oncol 92:151–159PubMedGoogle Scholar
  109. Popnikolov NK, Gatalica Z, Adegboyega PA, Norris BA, Pasricha PJ (2006) Downregulation of TNF-related apoptosis-inducing ligand (TRAIL)/Apo2L in Barrett’s esophagus with dysplasia and adenocarcinoma. Appl Immunohistochem Mol Morphol 14:161–165PubMedGoogle Scholar
  110. Poulaki V, Mitsiades CS, Mitsiades N (2001) The role of Fas and FasL as mediators of anticancer chemotherapy. Drug Resist Updat 4:233–242PubMedGoogle Scholar
  111. Puglisi F, Di Loreto C, Panizzo R, Avellini C, Fongione S, Cacitti V, Beltrami CA (1996) Expression of p53 and bcl-2 and response to preoperative chemotherapy and radiotherapy for locally advanced squamous cell carcinoma of the oesophagus. J Clin Pathol 49:456–459PubMedGoogle Scholar
  112. Raouf AA, Evoy DA, Carton E, Mulligan E, Griffin MM, Reynolds JV (2003) Loss of Bcl-2 expression in Barrett’s dysplasia and adenocarcinoma is associated with tumor progression and worse survival but not with response to neoadjuvant chemoradiation. Dis.Esophagus 16:17–23PubMedGoogle Scholar
  113. Ribeiro U Jr, Finkelstein SD, Safatle-Ribeiro AV, Landreneau RJ, Clarke MR, Bakker A, Swalsky PA, Gooding WE, Posner MC (1998) p53 sequence analysis predicts treatment response and outcome of patients with esophageal carcinoma. Cancer 83:7–18Google Scholar
  114. Robert V, Michel P, Flaman JM, Chiron A, Martin C, Charbonnier F, Paillot B, Frebourg T (2000) High frequency in esophageal cancers of p53 alterations inactivating the regulation of genes involved in cell cycle and apoptosis. Carcinogenesis 21:563–565PubMedGoogle Scholar
  115. Rowinsky EK (2005) Targeted induction of apoptosis in cancer management: the emerging role of tumor necrosis factor-related apoptosis-inducing ligand receptor activating agents. J Clin Oncol 23:9394–9407PubMedGoogle Scholar
  116. Ruoslahti E, Reed JC (1994) Anchorage dependence, integrins, and apoptosis. Cell 77:477–478PubMedGoogle Scholar
  117. Sarbia M, Bittinger F, Grabellus F, Verreet P, Dutkowski P, Willers R, Gabbert HE (1997) Expression of Bax, a pro-apoptotic member of the Bcl-2 family, in esophageal squamous cell carcinoma. Int J Cancer 73:508–513PubMedGoogle Scholar
  118. Sarbia M, Bittinger F, Porschen R, Verreet P, Dutkowski P, Willers R, Gabbert HE (1996) bcl-2 expression and prognosis in squamous-cell carcinomas of the esophagus. Int J Cancer 69:324–328PubMedGoogle Scholar
  119. Sarbia M, Stahl M, Fink U, Willers R, Seeber S, Gabbert HE (1998) Expression of apoptosis-regulating proteins and outcome of esophageal cancer patients treated by combined therapy modalities. Clin Cancer Res 4:2991–2997PubMedGoogle Scholar
  120. Schmitt CA (2003) Senescence, apoptosis and therapy – cutting the lifelines of cancer. Nat Rev Cancer 3:286–295PubMedGoogle Scholar
  121. Schmitt CA, Rosenthal CT, Lowe SW (2000) Genetic analysis of chemoresistance in primary murine lymphomas. Nat Med 6:1029–1035PubMedGoogle Scholar
  122. Schneider PM, Casson AG, Levin B, Garewal HS, Hoelscher AH, Becker K, Dittler HJ, Cleary KR, Troster M, Siewert JR, Roth JA (1996) Mutations of p53 in Barrett’s esophagus and Barrett’s cancer: a prospective study of ninety-eight cases. J Thorac Cardiovasc Surg 111:323–331PubMedGoogle Scholar
  123. Schneider PM, Stoeltzing O, Roth JA, Hoelscher AH, Wegerer S, Mizumoto S, Becker K, Dittler HJ, Fink U, Siewert JR (2000) P53 mutational status improves estimation of prognosis in patients with curatively resected adenocarcinoma in Barrett’s esophagus. Clin Cancer Res 6:3153–3158Google Scholar
  124. Schrump DS, Matthews W, Chen GA, Mixon A, Altorki NK (1998) Flavopiridol mediates cell cycle arrest and apoptosis in esophageal cancer cells. Clin Cancer Res 4:2885–2890PubMedGoogle Scholar
  125. Seitz JF, Perrier H, Monges G, Giovannini M, Gouvernet J (1995) Multivariate analysis of the prognostic and predictive factors of response to concomitant radiochemotherapy in epidermoid cancers of the esophagus. Value of immunodetection of protein p53. Gastroenterol Clin Biol 19:465–474PubMedGoogle Scholar
  126. Shao Y, Tan W, Zhang S (2008) P53 gene codon 72 polymorphism and risk of esophageal squamous cell carcinoma: a case/control study in a Chinese population. Dis Esophagus 21:139–143PubMedGoogle Scholar
  127. Sheikh MS, Huang Y, Fernandez-Salas EA, El Deiry WS, Friess H, Amundson S, Yin J, Meltzer SJ, Holbrook NJ, Fornace AJ Jr (1999) The antiapoptotic decoy receptor TRID/TRAIL-R3 is a p53-regulated DNA damage-inducible gene that is overexpressed in primary tumors of the gastrointestinal tract. Oncogene 18:4153–4159PubMedGoogle Scholar
  128. Shibakita M, Tachibana M, Dhar DK, Kotoh T, Kinugasa S, Kubota H, Masunaga R, Nagasue N (1999) Prognostic significance of Fas and Fas ligand expressions in human esophageal cancer. Clin Cancer Res 5:2464–2469PubMedGoogle Scholar
  129. Shibakita M, Tachibana M, Dhar DK, Ohno S, Kubota H, Yoshimura H, Kinugasa S, Masunaga R, Nagasue N (2000) Spontaneous apoptosis in advanced esophageal carcinoma: its relation to Fas expression. Clin Cancer Res 6:4755–4759PubMedGoogle Scholar
  130. Shimoyama S, Konishi T, Kawahara M, Aoki F, Harada N, Shimizu S, Murakami T, Kaminishi M (1998) Expression and alteration of p53 and p21(waf1/cip1) influence the sensitivity of chemoradiation therapy for esophageal cancer. Hepatogastroenterology 45:1497–1504PubMedGoogle Scholar
  131. Siewert JR, Ott K (2007) Are squamous and adenocarcinomas of the esophagus the same disease? Semin Radiat Oncol 17:38–44Google Scholar
  132. Stoner GD, Gupta A (2001) Etiology and chemoprevention of esophageal squamous cell carcinoma. Carcinogenesis 22:1737–1746PubMedGoogle Scholar
  133. Stoner GD, Wang LS, Chen T (2007) Chemoprevention of esophageal squamous cell carcinoma. Toxicol Appl Pharmacol 224:337–349PubMedGoogle Scholar
  134. Sun T, Miao X, Zhang X, Tan W, Xiong P, Lin D (2004) Polymorphisms of death pathway genes FAS and FASL in esophageal squamous-cell carcinoma. J Natl Cancer Inst 96:1030–1036PubMedGoogle Scholar
  135. Szumilo J, Chibowski D, browski D (2000) Assessment of the predictive value of clinical and histopathological factors as well as the immunoexpression of p53 and bcl-2 proteins in response to preoperative chemotherapy for esophageal squamous cell carcinoma. Dis Esophagus 13:191–197PubMedGoogle Scholar
  136. Takayama T, Nagao M, Sawada H, Yamada Y, Emoto K, Fujimoto H, Ueno M, Hirao S, Nakajima Y (2001) Bcl-X expression in esophageal squamous cell carcinoma: association with tumor progression and prognosis. J Surg Oncol 78:116–123PubMedGoogle Scholar
  137. Taniere P, Martel-Planche G, Maurici D, Lombard-Bohas C, Scoazec JY, Montesano R, Berger F, Hainaut P (2001) Molecular and clinical differences between adenocarcinomas of the esophagus and of the gastric cardia. Am J Pathol 158:33–40PubMedGoogle Scholar
  138. Teraishi F, Kagawa S, Watanabe T, Tango Y, Kawashima T, Umeoka T, Nisizaki M, Tanaka N, Fujiwara T (2005) ZD1839 (Gefitinib, ’Iressa’) an epidermal growth factor receptor-tyrosine kinase inhibitor, enhances the anti-cancer effects of TRAIL in human esophageal squamous cell carcinoma. FEBS Lett 579:4069–4075PubMedGoogle Scholar
  139. Tew WP, Kelsen DP, Ilson DH (2005) Targeted therapies for esophageal cancer. Oncologist 10:590–601Google Scholar
  140. Thompson WG, Heaton KW (1982) Heartburn and globus in apparently healthy people. Can Med Assoc J 126:46–48PubMedGoogle Scholar
  141. Torzewski M, Sarbia M, Heep H, Dutkowski P, Willers R, Gabbert HE (1998) Expression of Bcl-X(L) an antiapoptotic member of the Bcl-2 family, in esophageal squamous cell carcinoma. Clin Cancer Res 4:577–583PubMedGoogle Scholar
  142. Tytgat GN (1995) Does endoscopic surveillance in esophageal columnar metaplasia (Barrett’s esophagus) have any real value? Endoscopy 27:19–26Google Scholar
  143. Vallbohmer D, Peters JH, Oh D, Kuramochi H, Shimizu D, Demeester SR, Hagen JA, Chandrasoma PT, Danenberg KD, Demeester TR, Danenberg P (2005) Survivin, a potential biomarker in the development of Barrett’s adenocarcinoma. Surgery 138:701–706PubMedGoogle Scholar
  144. van der Woude CJ, Jansen PL, Tiebosch AT, Beuving A, Homan M, Kleibeuker JH, Moshage H (2002) Expression of apoptosis-related proteins in Barrett’s metaplasia-dysplasia-carcinoma sequence: a switch to a more resistant phenotype. Hum Pathol 33:686–692PubMedGoogle Scholar
  145. Vollmers HP, Dammrich J, Hensel F, Ribbert H, Meyer-Bahlburg A, Ufken-Gaul T, von Korff M, Muller-Hermelink HK (1997) Differential expression of apoptosis receptors on diffuse and intestinal type stomach carcinoma. Cancer 79:433–440Google Scholar
  146. Walczak H, Miller RE, Ariail K, Gliniak B, Griffith TS, Kubin M, Chin W, Jones J, Woodward A, Le T, Smith C, Smolak P, Goodwin RG, Rauch CT, Schuh JC, Lynch DH (1999) Tumoricidal activity of tumor necrosis factor-related apoptosis-inducing ligand in vivo. Nat Med 5:157–163PubMedGoogle Scholar
  147. Wallace-Brodeur RR, Lowe SW (1999) Clinical implications of p53 mutations. Cell Mol Life Sci 55:64–75PubMedGoogle Scholar
  148. Wei MC, Zong WX, Cheng EH, Lindsten T, Panoutsakopoulou V, Ross AJ, Roth KA, MacGregor GR, Thompson CB, Korsmeyer SJ (2001) Proapoptotic BAX and BAK: a requisite gateway to mitochondrial dysfunction and death. Science 292:727–730PubMedGoogle Scholar
  149. Whittles CE, Biddlestone LR, Burton A, Barr H, Jankowski JAZ, Warner PJ, Shepherd NA (1999) Apoptotic and proliferative activity in the neoplastic progression of Barrett’s oesophagus: A comparative study. J Pathol 187:535–540PubMedGoogle Scholar
  150. Wu J, Metz C, Xu X, Abe R, Gibson AW, Edberg JC, Cooke J, Xie F, Cooper GS, Kimberly RP (2003) A novel polymorphic CAAT/enhancer-binding protein beta element in the FasL gene promoter alters Fas ligand expression: a candidate background gene in African American systemic lupus erythematosus patients. J Immunol 170:132–138PubMedGoogle Scholar
  151. Xue LY, Ren LQ, Luo W, Guan XJ, Zou SM, Zheng S, Bi R, Xie YQ, He ZG, Lu N (2007) [Expression of Fas, Fas ligand, Fas-associated death domain protein, caspase 8 and mutant P53 protein in esophageal squamous cell carcinoma]. Zhonghua Yi.Xue.Za Zhi 87:150–154PubMedGoogle Scholar
  152. Yang B, Rice TW, Adelstein DJ, Rybicki LA, Goldblum JR (1999) Overexpression of p53 protein associates decreased response to chemoradiotherapy in patients with esophageal carcinoma. Mod Pathol 12:251–256PubMedGoogle Scholar
  153. Yin XM (2000) Signal transduction mediated by Bid, a pro-death Bcl-2 family proteins, connects the death receptor and mitochondria apoptosis pathways. Cell Res 10:161–167PubMedGoogle Scholar
  154. Yokomakura N, Natsugoe S, Okumura H, Ikeda R, Uchikado Y, Mataki Y, Takatori H, Matsumoto M, Owaki T, Ishigami S, Aikou T (2007) Improvement in radiosensitivity using small interfering RNA targeting p53R2 in esophageal squamous cell carcinoma. Oncol Rep 18:561–567Google Scholar
  155. Younes M, Georgakis GV, Rahmani M, Beer D, Younes A (2006) Functional expression of TRAIL receptors TRAIL-R1 and TRAIL-R2 in esophageal adenocarcinoma. Eur J Cancer 42:542–547PubMedGoogle Scholar
  156. Younes M, Lechago J, Ertan A, Finnie D, Younes A (2000) Decreased expression of Fas (CD95/APO1) associated with goblet cell metaplasia in Barrett’s esophagus. Hum Pathol 31:434–438PubMedGoogle Scholar
  157. Younes M, Schwartz MR, Finnie D, Younes A (1999) Overexpression of Fas ligand (FasL) during malignant transformation in the large bowel and in Barrett’s metaplasia of the esophagus. Hum Pathol 30:1309–1313PubMedGoogle Scholar

Copyright information

© Springer Science+Business Media B.V. 2009

Authors and Affiliations

  • Yan Li
    • 1
  • Robert C.G. Martin
    • 1
  1. 1.Department of Surgery, Division of Surgical OncologyUniversity of Louisville School of MedicineLouisvilleUSA

Personalised recommendations