Gastroenterology
Volume 127, Issue 6 , Pages 1787-1797 , December 2004

Translational regulation of XIAP expression and cell survival during hypoxia in human cholangiocarcinoma

  • Carla Marienfeld

      Affiliations

    • Scott and White Clinic, Texas A&M University System Health Science Center College of Medicine, Temple, Texas
  • ,
  • Yoko Yamagiwa

      Affiliations

    • Scott and White Clinic, Texas A&M University System Health Science Center College of Medicine, Temple, Texas
  • ,
  • Yoshiyuki Ueno

      Affiliations

    • Division of Gastroenterology, Tohoku University School of Medicine, Aobaku, Sendai, Japan
  • ,
  • Valorie Chiasson

      Affiliations

    • Scott and White Clinic, Texas A&M University System Health Science Center College of Medicine, Temple, Texas
  • ,
  • Linda Brooks

      Affiliations

    • Scott and White Clinic, Texas A&M University System Health Science Center College of Medicine, Temple, Texas
  • ,
  • Fanyin Meng

      Affiliations

    • Scott and White Clinic, Texas A&M University System Health Science Center College of Medicine, Temple, Texas
  • ,
  • Tushar Patel

      Affiliations

    • Scott and White Clinic, Texas A&M University System Health Science Center College of Medicine, Temple, Texas
    • Corresponding Author InformationAddress requests for reprints to: Tushar Patel, MD, Division of Gastroenterology, Scott and White Clinic, Texas A&M University Health Science Center, 2401 South 31st Street, Temple, Texas 76502. fax: (254) 724-8276.

Received 8 August 2003 ,Accepted 26 August 2004.

References 

  1. Hockel M , Vaupel P . Biological consequences of tumor hypoxia . Semin Oncol . 2001;28:36–41
  2. Hockel M , Vaupel P . Tumor hypoxia (definitions and current clinical, biologic, and molecular aspects) . J Natl Cancer Inst . 2001;93:266–276
  3. Bergers G , Benjamin LE . Tumorigenesis and the angiogenic switch . Nat Rev Cancer . 2003;3:401–410
  4. Ghafar MA, Anastasiadis AG, Chen MW, Burchardt M, Olsson LE, Xie H, et al. Acute hypoxia increases the aggressive characteristics and survival properties of prostate cancer cells . Prostate . 2003;54:58–67
  5. Subarsky P , Hill RP . The hypoxic tumour microenvironment and metastatic progression . Clin Exp Metastasis . 2003;20:237–250
  6. Batts KP . Ischemic cholangitis . Mayo Clin Proc . 1998;73:380–385
  7. de Groen PC , Gores GJ , LaRusso NF , Gunderson LL , Nagorney DM . Biliary tract cancers . N Engl J Med . 1999;341:1368–1378
  8. Gores GJ . Cholangiocarcinoma (current concepts and insights) . Hepatology . 2003;37:961–969
  9. Horiuchi A, Imai T, Shimizu M, Oka K, Wang C, Nikaido T, et al. Hypoxia-induced changes in the expression of VEGF, HIF-1 α, and cell cycle-related molecules in ovarian cancer cells . Anticancer Res . 2002;22:2697–2702
  10. Humar R , Kiefer FN , Berns H , Resink TJ , Battegay EJ . Hypoxia enhances vascular cell proliferation and angiogenesis in vitro via rapamycin (mTOR)-dependent signaling . FASEB J . 2002;16:771–780
  11. Dong Z, Nishiyama J, Yi X, Venkatachalam MA, Denton M, Gu S, et al. Gene promoter of apoptosis inhibitory protein IAP2 (identification of enhancer elements and activation by severe hypoxia) . Biochem J . 2002;364:413–421
  12. Yamagiwa Y , Marienfeld C , Tadlock L , Patel T . Translational regulation by p38 mitogen-activated protein kinase signaling during human cholangiocarcinoma growth . Hepatology . 2003;38:158–166
  13. Pain VM . Initiation of protein synthesis in eukaryotic cells . Eur J Biochem . 1996;236:747–771
  14. Pestova TV, Kolupaeva VG, Lomakin IB, Pilipenko EV, Shatsky IN, Agol VI, et al. Molecular mechanisms of translation initiation in eukaryotes . Proc Natl Acad Sci U S A . 2001;98:7029–7036
  15. Kraggerud SM , Sandvik JA , Pettersen EO . Regulation of protein synthesis in human cells exposed to extreme hypoxia . Anticancer Res . 1995;15:683–686
  16. Abraham RT . MTOR as a positive regulator of tumor cell responses to hypoxia . Curr Top Microbiol Immunol . 2004;279:299–319
  17. Gingras AC , Raught B , Sonenberg N . Control of translation by the target of rapamycin proteins . Prog Mol Subcell Biol . 2001;27:143–174
  18. Park J , Tadlock L , Gores GJ , Patel T . Inhibition of interleukin 6-mediated mitogen-activated protein kinase activation attenuates growth of a cholangiocarcinoma cell line . Hepatology . 1999;30:1128–1133
  19. Park J , Gores GJ , Patel T . Lipopolysaccharide induces cholangiocyte proliferation via an interleukin-6-mediated activation of p44/p42 mitogen-activated protein kinase . Hepatology . 1999;29:1037–1043
  20. Tadlock L , Yamagiwa Y , Marienfeld C , Patel T . Double-stranded RNA activates a p38 MAPK-dependent cell survival program in biliary epithelia . Am J Physiol Gastrointest Liver Physiol . 2003;284:G924–G932
  21. Yamagiwa Y , Marienfeld C , Meng F , Holcik M , Patel T . Translational regulation of x-linked inhibitor of apoptosis protein by interleukin-6 (a novel mechanism of tumor cell survival) . Cancer Res . 2004;64:1293–1298
  22. Tadlock L , Patel T . Involvement of p38 mitogen-activated protein kinase signaling in transformed growth of a cholangiocarcinoma cell line . Hepatology . 2001;33:43–51
  23. Arteel GE , Thurman RG , Yates JM , Raleigh JA . Evidence that hypoxia markers detect oxygen gradients in liver (pimonidazole and retrograde perfusion of rat liver) . Br J Cancer . 1995;72:889–895
  24. Matkowskyj KA , Cox R , Jensen RT , Benya RV . Quantitative immunohistochemistry by measuring cumulative signal strength accurately measures receptor number . J Histochem Cytochem . 2003;51:205–214
  25. Hansel DE, Rahman A, Hidalgo M, Thuluvath PJ, Lillemoe KD, Shulick R, et al. Identification of novel cellular targets in biliary tract cancers using global gene expression technology . Am J Pathol . 2003;163:217–229
  26. LaCasse EC , Baird S , Korneluk RG , MacKenzie AE . The inhibitors of apoptosis (IAPs) and their emerging role in cancer . Oncogene . 1998;17:3247–3259
  27. Holcik M , Yeh C , Korneluk RG , Chow T . Translational upregulation of X-linked inhibitor of apoptosis (XIAP) increases resistance to radiation induced cell death . Oncogene . 2000;19:4174–4177
  28. Berkel HJ , Turbat-Herrera EA , Shi R , de Benedetti A . Expression of the translation initiation factor eIF4E in the polyp- cancer sequence in the colon . Cancer Epidemiol Biomarkers Prev . 2001;10:663–666
  29. DeFatta RJ , Nathan CA , de Benedetti A . Antisense RNA to eIF4E suppresses oncogenic properties of a head and neck squamous cell carcinoma cell line . Laryngoscope . 2000;110:928–933
  30. DeFatta RJ , Turbat-Herrera EA , Li BD , Anderson W , de Benedetti A . Elevated expression of eIF4E in confined early breast cancer lesions (possible role of hypoxia) . Int J Cancer . 1999;80:516–522
  31. Gingras AC , Raught B , Sonenberg N . eIF4 initiation factors (effectors of mRNA recruitment to ribosomes and regulators of translation) . Annu Rev Biochem . 1999;68:913–963
  32. Graff JR , Zimmer SG . Translational control and metastatic progression (enhanced activity of the mRNA cap-binding protein eIF-4E selectively enhances translation of metastasis-related mRNAs) . Clin Exp Metastasis . 2003;20:265–273
  33. de Benedetti A , Rhoads RE . Overexpression of eukaryotic protein synthesis initiation factor 4E in HeLa cells results in aberrant growth and morphology . Proc Natl Acad Sci U S A . 1990;87:8212–8216
  34. de Benedetti A , Harris AL . eIF4E expression in tumors (its possible role in progression of malignancies) . Int J Biochem Cell Biol . 1999;31:59–72
  35. Tinton SA , Buc-Calderon PM . Hypoxia increases the association of 4E-binding protein 1 with the initiation factor 4E in isolated rat hepatocytes . FEBS Lett . 1999;446:55–59
  36. Holcik M , Lefebvre C , Yeh C , Chow T , Korneluk RG . A new internal-ribosome-entry-site motif potentiates XIAP-mediated cytoprotection . Nat Cell Biol . 1999;1:190–192
  37. Nevins TA , Harder ZM , Korneluk RG , Holcik M . Distinct regulation of internal ribosome entry site-mediated translation following cellular stress is mediated by apoptotic fragments of eIF4G translation initiation factor family members eIF4GI and p97/DAP5/NAT1 . J Biol Chem . 2003;278:3572–3579
  38. Bilim V , Kasahara T , Hara N , Takahashi K , Tomita Y . Role of XIAP in the malignant phenotype of transitional cell cancer (TCC) and therapeutic activity of XIAP antisense oligonucleotides against multidrug-resistant TCC in vitro . Int J Cancer . 2003;103:29–37
  39. Sasaki H , Sheng Y , Kotsuji F , Tsang BK . Down-regulation of X-linked inhibitor of apoptosis protein induces apoptosis in chemoresistant human ovarian cancer cells . Cancer Res . 2000;60:5659–5666
  40. Mansouri A , Zhang Q , Ridgway LD , Tian L , Claret FX . Cisplatin resistance in an ovarian carcinoma is associated with a defect in programmed cell death control through XIAP regulation . Oncol Res . 2003;13:399–404
  41. Li J, Feng Q, Kim JM, Schneiderman D, Liston P, Li M, et al. Human ovarian cancer and cisplatin resistance (possible role of inhibitor of apoptosis proteins) . Endocrinology . 2001;142:370–380
  42. Hu Y, Cherton-Horvat G, Dragowska V, Baird S, Korneluk RG, Durkin JP, et al. Antisense oligonucleotides targeting XIAP induce apoptosis and enhance chemotherapeutic activity against human lung cancer cells in vitro and in vivo . Clin Cancer Res . 2003;9:2826–2836

 Supported by the Scott and White Hospital Foundation, grant DK069370 from the National Institutes of Health (to T.P.), and Grant-in-Aid for Scientific Research C(16590573) (to Y.U.).

PII: S0016-5085(04)01571-9

doi: 10.1053/j.gastro.2004.09.002

Gastroenterology
Volume 127, Issue 6 , Pages 1787-1797 , December 2004