In vitro hypoxia-conditioned colon cancer cell lines derived from HCT116 and HT29 exhibit altered apoptosis susceptibility and a more angiogenic profile in vivo

British Journal of Cancer

Volumn 93, Issue 12, 2005, Pages 1356-1363

  Yao, K ^a   Gietema, J A ^b   Shida, S ^a   Selvakumaran, M ^a   Fonrose, X ^a   Haas, N B ^c   Testa, J ^c   O'Dwyer, P J ^a  

^a UNIVERSITY OF PENNSYLVANIA   (United States)

^b UNIVERSITY MEDICAL CENTER GRONINGEN   (Netherlands)

^c FOX CHASE CANCER CENTER   (United States)

Author keywords

Angiogenesis; Apoptosis; Cisplatin; Colon cancer; Hypoxia

Indexed keywords

ANGIOGENESIS INHIBITOR; CISPLATIN; DNA; OXYGEN;

ADAPTATION; ANGIOGENESIS; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; APOPTOSIS; ARTICLE; CANCER CELL; CANCER CELL CULTURE; CANCER RESISTANCE; CELL STRAIN HCT116; CELL STRAIN HT29; CELL SURVIVAL; COLON CANCER; COLON CARCINOMA; CONTROLLED STUDY; DNA DAMAGE; DRUG SENSITIVITY; EXPOSURE; FEMALE; HUMAN; HUMAN CELL; HYPOXIA; IMMUNE DEFICIENCY; IN VITRO STUDY; IN VIVO STUDY; MOUSE; NONHUMAN; PRIORITY JOURNAL; SENSITIVITY ANALYSIS; SIGNAL TRANSDUCTION; TUMOR XENOGRAFT; VASCULARIZATION;

ADAPTATION, PHYSIOLOGICAL; ANIMALS; APOPTOSIS; CELL HYPOXIA; CELL PROLIFERATION; CELL SURVIVAL; COLONIC NEOPLASMS; DNA DAMAGE; DRUG RESISTANCE, NEOPLASM; FEMALE; HUMANS; IMMUNOHISTOCHEMISTRY; IN SITU NICK-END LABELING; MICE; MICE, SCID; NEOVASCULARIZATION, PATHOLOGIC; TRANSPLANTATION, HETEROLOGOUS; TUMOR CELLS, CULTURED;

EID: 28644437424     PISSN: 00070920     EISSN: 15321827     Source Type: Journal    
DOI: 10.1038/sj.bjc.6602864     Document Type: Article

References (57)

1. Amellem O, Stokke T, Sandvik JA, Smedshammer L, Pettersen EO (1997) Hypoxia-induced apoptosis in human cells with normal p53 status and function, without any alteration in the nuclear protein level. Exp Cell Res 232: 361-370
2. Bhattacharyya NP, Skandalis A, Ganesh A, Groden J, Meuth M (1994) Mutator phenotypes in human colorectal carcinoma cell lines. Proc Natl Acad Sci USA 91: 6319-6323
3. Brizel DM, Sibley GS, Prosnitz LR, Scher RL, Dewhirst MW (1997) Tumor hypoxia adversely effects the prognosis of carcinoma of the head and neck. Int J Radiat Oncol Biol Phys 38: 285-289
4. Brown JM, Koong A (1991) Therapeutic advantage of hypoxic cells in tumors: a theoretical study. J Natl Cancer Inst 83: 178-185
5. Brown JM (1999) The hypoxic cell: a target for selective cancer therapy - eighteenth Bruce F. Cain Memorial Award lecture. Cancer Res 59: 5863-5870
6. Buller AL, Clapper ML, Tew KD (1987) Glutathione S-transferases in nitrogen mustard-resistant and - sensitive cell lines. Mol Pharmacol 31: 575-578
7. 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: 263-269
8. Bush RS, Jenkin RDT, Allt WEC (1978) Definitive evidence for hypoxic cells influencing cure in cancer therapy. Br J Cancer 37(Supp III): 302-306
9. Carmeliet P, Dor Y, Herbert JM, Fukumura D, Brusselmans K, Dewerchin M, Neeman M, Bono F, Abramovitch R, Maxwell P, Koch CJ, Ratcliffe P, Moons L, Jain RK, Collen D, Keshert E (1998) Role of HIF-1alpha in hypoxia-mediated apoptosis, cell proliferation and tumour angiogenesis. Nature 394: 485-490
10. Castro-Rivera E, Ran S, Thorpe P, Minna JD (2004) Semaphorin 3B (SEMA3B) induces apoptosis in lung and breast cancer, whereas VEGF165 antagonizes this effect. Proc Natl Acad Sci USA 101: 11432-11437
11. Chaplin DJ, Hill SA (2002) Selective induction of tumor ischemia: development of vascular targeting agents for cancer therapy. Curr Opin Investig Drugs 3: 1381-1384
12. Coussens LM, Fingleton B, Matrisian LM (2002) Matrix metalloproteinase inhibitors and cancer: trials and tribulations. Science 295: 2387-2392
13. Dong Z, Wang J (2004) Hypoxia selection of death-resistant cells: a role for Bcl-XL. J Biol Chem. 279: 9215-9221
14. Egeblad M, Werb Z (2002) New functions for the matrix metalloproteinases in cancer progression. Nat Rev Cancer 2: 161-174
15. Forsythe JA, Jiang BH, Iyer NV, Agani F, Leung SW, Koos RD, Semenza GL (1996) Activation of vascular endothelial growth factor gene transcription by hypoxia-inducible factor 1. Mol Cell Biol 16: 4604-4613
16. Garay M, Gaarde W, Monia BP, Nero P, Cioffi CL (2000) Inhibition of hypoxia/reoxygenation-induced apoptosis by an antisense of oligonucleotide targeted to JNK1 in human kidney cells. Biochem Pharmacol 59: 1033-1043
17. Gibelli N, Zibera C, Asti A, Kaestri L, Bacchella L, Pedrazzoli P, Calligaro A, Robustelli della Cuna G (1996) CG5/Dx human breast cancer cell lines: characterization of a new doxorubicin-resistant variant. Anticancer Res 16: 1675-1681
18. Godwin A, Meister A, O'Dwyer PJ, Huang C, Hamilton T, Anderson M (1992) High resistance to cisplatin in human ovarian cancer cell lines is associated with marked increase of glutathione synthesis. Proc Natl Acad Sci USA 89: 3070-3074
19. Graeber TG, Osmanian C, Jacks T, Housman DE, Koch CJ, Lowe SW, Giaccia AJ (1996) Hypoxia-mediated selection of cells with diminished apoptotic potential in solid tumours. Nature 379: 88-91
20. Hamilton TC, Winker MA, Louie KG, Batist G, Behrens BC, Tsuruo T, Grotzinger KR, McKoy WM, Young RC, Ozols RF (1985) Augmentation of adriamycin, melphalan, and cisplatin cytotoxicity in drug-resistant and -sensitive human ovarian carcinoma cell lines by buthionine sulfoximine mediated glutathione depletion. Biochem Pharmacol 34: 2583-2586
21. Harris AL (2001) Hypoxia - a key regulatory factor in tumor growth. Nat Rev Cancer 2: 38-46
22. Hochachka PW, Rupert JL, Goldenberg L, Gleave M, Kozlowski P (2002) Going malignant: the hypoxia-cancer connection in the prostate. Bioessays 24: 749-757
23. Hockel M, Schlenger K, Aral B, Mitze M, Schaffer U, Vaupel P (1996) Association between tumor hypoxia and malignant progression in advanced cancer of the uterine cervix. Cancer Res 56: 4509-4515
24. Holmbeck K, Bianco P, Birkedal-Hansen H (2003) MT1-mmp: a collagenase essential for tumor cell invasive growth. Cancer Cell 4: 83-84
25. Johnson SW, Laub PB, Beesley JS, Ozols RF, Hamilton TC (1997) Increased platinum-DNA damage tolerance is associated with cisplatin resistance and cross-resistance to various chemotherapeutic agents in unrelated human ovarian cancer cell lines. Cancer Res 57: 850-856
26. Johnstone RW, Ruefli AA, Lowe SW (2002) Apoptosis: a link between cancer genetics and chemotherapy. Cell 108: 153-164
27. Kartner N, Shales M, Riordan JR, Ling V (1983) Daunorubicin-resistant Chinese hamster ovary cells expressing multidrug resistance and a cell-surface P-glycoprotein. Cancer Res 43: 4413-4419
28. Kennedy KA, Teicher BA, Rockwell S, Sartorelli AC (1980) The hypoxic tumor cell: a target for selective cancer chemotherapy. Biochem Pharmacol 29: 1-8
29. Kim CY, Tsai MH, Osmanian C, Graeber TG, Lee JE, Giffard RG, DiPaolo JA, Peehl DM, Giaccia AJ (1997) Selection of human cervical epithelial cells that possess reduced apoptotic potential to low-oxygen conditions. Cancer Res 57: 4200-4204
30. Koong AC, Denko NC, Hudson KM, Schindler C, Swiersz L, Koch C, Evans S, Ibrahim H, Le QT, Terris DJ, Giaccia AJ (2000) Candidate genes for the hypoxic tumor phenotype. Cancer Res 60: 883-887
31. Leker RR, Aharonowiz M, Greig NH, Ovadia H (2004) The role of p53-induced apoptosis in cerebral ischemia: effects of the p53 inhibitor pifithrin alpha. Exp Neurol 187: 478-486
32. Ling V, Kartner N, Sudo T, Siminovitch L, Riordan JR (1983) Multidrug-resistance phenotype in Chinese hamster ovary cells. Cancer Treat Rep 67: 869-874
33. Liotta LA, Thorgeirsson UP, Garbisa S (1982) Role of collagenases in tumor cell invasion. Cancer Metast Rev 1: 277-288
34. Louie KG, Hamilton TC, Shoemaker RH, Young RC, Ozols RF (1992) Evaluation of in vitro drug screening leads using experimental models of human ovarian cancer. Invest New Drugs 10: 73-78
35. Melchiori A, Albini A, Ray JM, Stetler-Stevenson WG (1992) Inhibition of tumor cell invasion by a highly-conserved peptide sequence from the matrix metalloproteinase enzyme prosegment. Cancer Res 52: 2353-2356
36. Mitelman F (ed). (1995) An international System for Human Cytogenetic Normenclature. S. Karger, Basel, ISCN
37. Mosmann T (1983) Rapid colorimetric assay for cellular growth and survival: application to proliferations and cytotoxicity assays. J Immune Methods 65: 55-63
38. Moulder JE, Rockwell S (1984) Hypoxic fractions of solid tumors: experimental techniques, methods of analysis, and a survey of existing data. Int J Radiat Oncol Biol Phys 10: 695-712
39. Nahle Z, Polakoff J, Davuluri RV, McCurrach ME, Jacobson MD, Narita M, Zhang MQ, Lazebnik Y, Bar-Sagi D, Lowe SW (2002) Direct coupling of the cell cycle and cell death machinery by E2F. Nat Cell Biol 4: 859-864
40. North S, Moenner M, Bikfalvi A (2005) Recent developments in the regulation of the angiogenic switch by cellular stress factors in tumors. Cancer Lett 218: 1-14
41. O'Dwyer PJ, Yao KS, Ford P, Godwin AK, Claytin M (1994) Effects of hypoxia upon detoxicating enzyme activity and expression in HT29 colon adenocarcinoma cells. Cancer Res 54: 3082-3087
42. Pandey P, Avraham S, Kumar S, Nakazawa A, Place A, Ghanem L, Rana A, Kumar V, Majumder PK, Avraham H, Davis RJ, Kharbanda S (1999) Activation of p38 mitogen-activated protein kinase by PYK2/related adhesion focal tyrosine kinase-dependent mechanism. J Biol Chem 274: 10140-10144
43. Rice GC, Hoy C, Schimke RT (1986) Transient hypoxia enhances the frequency of dihydrofolate reductase gene amplification in Chinese hamster ovary cell. Proc Natl Acad Sci USA 83: 5978-5982
44. Rodrigues NR, Rowan A, Smith ME, Kerr IB, Bodmer WF, Gannon JV, Lane DP (1990) p53 mutations in colorectal cancer. Proc Natl Acad Sci USA 87: 7555-7559
45. Sakata K, Kwok TT, Murphy BJ, Laderoute KR, Gordon GR, Sutherland RM (1991) Hypoxia-induced drug resistance: comparison to P-glycoprotein-associated drug resistance. Br J Cancer 64: 809-814
46. Semenza GL (2003) Targeting HIF-1α for cancer therapy. Nat Rev Cancer 3: 721-732
47. Shimizu S, Eguchi Y, Kamiike W, Itoh Y, Hasegawa J, Yamabe K, Otsuki Y, Matsuda H, Tsujimoto Y (1996) Induction of apoptosis as well as necrosis by hypoxia and predominant prevention of apoptosis by Bcl-2 and Bcl-XL. Cancer Res 56: 2161-2166
48. Stephan S, Datta K, Wang E, Li J, Brekken RA, Parangi S, Thorpe PE, Mukhopadhyay D (2004) Effect of rapamycin alone and in combination with antiangiogenesis therapy in an orthotopic model of human pancreatic cancer. Clinical Cancer Res 10: 6993-7000
49. Tannock I, Guttman P (1981) Response of Chinese hamster ovary cells to anticancer drugs under aerobic and hypoxic conditions. Br J Cancer 42: 245-248
50. Teicher BA, Holden SA, Al-Achi A, Herman TS (1990) Classification of antineoplastic treatments by their differential toxicity toward putative oxygenated and hypoxic tumor subpopulations in vivo in the FSaIIC murine fibrosarcoma. Cancer Res 50: 3339-3344
51. Vasilevskaya I, O'Dwyer PJ (1999) Effects of geldanamycin on signaling through AP-1 in hypoxic HT29 human colon adenocarcinoma cells. Cancer Res 59: 3935-3940
52. Vaupel P, Kallinowski F, Okunief F (1989) Blood flow, oxygen and nutrient supply, and metabolic microenvironment of humors: A review. Cancer Res 49: 6449-6465
53. Wang AL, Tew KD (1985) Increased glutathione-S-transferase activity in a cell line with acquired resistance to nitrogen mustards. Cancer Treat Rep 69: 677-682
54. Yao KS, Clayton M, O'Dwyer PJ (1995) Apoptosis in human adenocarcinoma HT29 cells induced by exposure to hypoxia. J Natl Cancer Inst 87: 117-122
55. Yao KS, O'Dwyer PJ (1995) Involvement of NF-êB in the induction of NAD(P)H: quinone oxidoreductase (DT-diaphorase) by hypoxia, oltipraz andmitomycin C. Biochem Pharmacol 49: 275-282
56. Yao KS, Xanthoudakis S, Curran T, O'Dwyer PJ (1994) Activation of AP-1 and of a nuclear redox factor ref-1 in the response of HT29 colon cancer cells to hypoxia. Mol Cell Biol 14: 5997-6003
57. Zhang L, Hill RP (2004) Hypoxia enhances metastatic efficiency by upregulating mdm2 KHT cells and increasing resistance to apoptosis. Cancer Res 64: 4180-4189