Cell cycle kinase inhibitor expression and hypoxia-induced cell cycle arrest in human cancer cell lines

Carcinogenesis

Volumn 25, Issue 12, 2004, Pages 2325-2335

  Box, Adrian Harold ^a   Demetrick, Douglas James ^a,b  

^a CALGARY LABORATORY SERVICES   (Canada)

^b UNIVERSITY OF CALGARY   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

HYPOXIA INDUCIBLE FACTOR 1ALPHA; LITHIUM CHLORIDE; NUCLEAR PROTEIN; PHOSPHOTRANSFERASE INHIBITOR; PROTEIN KINASE B; PROTEIN P16; PROTEIN P27;

APOPTOSIS; ARTICLE; BREAST CARCINOMA; BREAST EPITHELIUM; CANCER CELL CULTURE; CELL CYCLE; CELL CYCLE G1 PHASE; CELL CYCLE S PHASE; ENZYME ACTIVITY; FIBROBLAST; FLOW CYTOMETRY; HELA CELL; HUMAN; HUMAN CELL; HYPOXIA; LIVER CELL CARCINOMA; PHENOTYPE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; SIGNAL TRANSDUCTION; UPREGULATION; UTERINE CERVIX CARCINOMA;

APOPTOSIS; CARCINOMA, HEPATOCELLULAR; CELL CYCLE PROTEINS; CELL HYPOXIA; CYCLIN-DEPENDENT KINASE INHIBITOR P16; CYCLIN-DEPENDENT KINASE INHIBITOR P27; ENZYME ACTIVATION; FIBROBLASTS; G1 PHASE; GLYCOGEN SYNTHASE KINASE 3; HELA CELLS; HUMANS; HYPOXIA-INDUCIBLE FACTOR 1, ALPHA SUBUNIT; LIVER NEOPLASMS; PHOSPHORYLATION; PROTEIN-SERINE-THREONINE KINASES; PROTO-ONCOGENE PROTEINS; PROTO-ONCOGENE PROTEINS C-AKT; RNA, MESSENGER; S PHASE; TRANSCRIPTION FACTORS; TUMOR CELLS, CULTURED; TUMOR SUPPRESSOR PROTEINS;

EID: 10344240885     PISSN: 01433334     EISSN: None     Source Type: Journal    
DOI: 10.1093/carcin/bgh274     Document Type: Article

References (74)

1. Dewhirst,M.W., Ong,E.T., Rosner,G.L., Rehmus,S.W., Shan,S., Braun,R.D., Brizel,D.M. and Secomb,T.W. (1996) Arteriolar oxygenation in tumour and subcutaneous arterioles: effects of inspired air oxygen content. Br. J. Cancer Suppl., 27, S241-246.
2. Brizel,D.M., Scully,S.P., Harrelson,J.M., Layfield,L.J., Bean,J.M., Prosnitz,L.R. and Dewhirst,M.W. (1996) Tumor oxygenation predicts for the likelihood of distant metastases in human soft tissue sarcoma. Cancer Res., 56, 941-943.
3. Gatenby,R.A., Kessler,H.B., Rosenblum,J.S., Coia,L.R., Moldofsky,P.J., Hartz,W.H. and Broder,G.J. (1988) Oxygen distribution in squamous cell carcinoma metastases and its relationship to outcome of radiation therapy. Int. J. Radiat. Oncol. Biol. Phys., 14, 831-838.
4. Schwickert,G., Walenta,S., Sundfor,K., Rofstad,E.K. and Mueller-Klieser,W. (1995) Correlation of high lactate levels in human cervical cancer with incidence of metastasis. Cancer Res., 55 4757-4759.
5. Tomida,A. and Tsuruo,T. (1999) Drug resistance mediated by cellular stress response to the microenvironment of solid tumors. Anticancer Drug Des., 14, 169-177.
6. Wang,G.L. and Semenza,G.L.(1993) Characterization of hypoxia-inducible factor 1 and regulation of DNA binding activity by hypoxia. J. Biol. Chem., 268, 21513-21518.
7. Semenza,G.L. and Wang,G.L. (1992) A nuclear factor induced by hypoxia via de novo protein synthesis binds to the human erythropoietin gene enhancer at a site required for transcriptional activation. Mol. Cell. Biol., 12, 5447-5454.
8. Wang,G.L., Jiang,B.H., Rue,E.A. and Semenza,G.L. (1995) Hypoxia-inducible factor 1 is a basic-helix-loop-helix-PAS heterodimer regulated by cellular O2 tension. Proc. Natl Acad. Sci. USA, 92 5510-5514.
9. Salceda,S. and Caro,J. (1997) Hypoxia-inducible factor 1alpha (HIF-1alpha) protein is rapidly degraded by the ubiquitin-proteasome system under normoxic conditions. Its stabilization by hypoxia depends on redox-induced changes. J. Biol. Chem., 272, 22642-22647.
10. Huang,L.E., Gu,J., Schau,M. and Bunn,H.F. (1998) Regulation of hypoxia-inducible factor 1alpha is mediated by an O2-dependent degradation domain via the ubiquitin-proteasome pathway. Proc. Natl Acad. Sci. USA, 95, 7987-7992.
11. Chen,C., Pore,N., Behrooz,A., Ismail-Beigi,F. and Maity,A. (2001) Regulation of glut1 mRNA by hypoxia-inducible factor-1. Interaction between H-ras and hypoxia. J. Biol. Chem., 276, 9519-9525.
12. Semenza,G.L., Jiang,B.H., Leung,S.W., Passantino,R., Concordet,J.P., Maire,P. and Giallongo,A. (1996) Hypoxia response elements in the aldolase A, enolase 1 and lactate dehydrogenase A gene promoters contain essential binding sites for hypoxia-inducible factor 1. J. Biol. Chem., 271, 32529-32537.
13. Semenza,G.L., Roth,P.H., Fang,H.M. and Wang,G.L. (1994) Transcriptional regulation of genes encoding glycolytic enzymes by hypoxia-inducible factor 1. J. Biol. Chem., 269, 23757-23763.
14. Liu,Y., Cox,S.R., Morita,T. and Kourembanas,S. (1995) Hypoxia regulates vascular endothelial growth factor gene expression in endothelial cells. Identification of a 5′ enhancer. Circ. Res., 77, 638-643.
15. Forsythe,J.A., Jiang,B.H., Iyer,N.V., Agani,F., Leung,S.W., Koos,R.D. and Semenza,G.L. (1996) Activation of vascular endothelial growth factor gene transcription by hypoxia-inducible factor 1. Mol. Cell. Biol., 16, 4604-4613.
16. Amellem,O. and Pettersen,E.O. (1991) Cell inactivation and cell cycle inhibition as induced by extreme hypoxia: the possible role of cell cycle arrest as a protection against hypoxia-induced lethal damage. Cell Prolif., 24, 127-141.
17. Krtolica,A. and Ludlow,J.W. (1996) Hypoxia arrests ovarian carcinoma cell cycle progression, but invasion is unaffected. Cancer Res., 56, 1168-1173.
18. Green,S.L., Freiberg,R.A. and Giaccia,A.J. (2001) p21 (Cip1) and p27 (Kip1) regulate cell cycle reentry after hypoxic stress but are not necessary for hypoxia-induced arrest. Mol. Cell. Biol., 21 1196-1206.
19. Swanton,C. (2004) Cell-cycle targeted therapies. Lancet Oncol., 5, 27-36.
20. Ekholm,S.V. and Reed,S.I. (2000) Regulation of G (1) cyclin-dependent kinases in the mammalian cell cycle. Curr. Opin. Cell. Biol., 12, 676-684.
21. Bartek,J., Bartkova,J. and Lukas,J. (1996) The retinoblastoma protein pathway and the restriction point. Curr. Opin. Cell. Biol., 8, 805-814.
22. Serrano,M., Hannon,G.J. and Beach,D. (1993) A new regulatory motif in cell-cycle control causing specific inhibition of cyclin D/CDK4. Nature, 366, 704-707.
23. Okamoto,A., Demetrick,D.J., Spillare,E.A. et al. (1994) Mutations and altered expression of p16INK4 in human cancer. Proc. Natl Acad. Sci. USA, 91, 11045-11049.
24. Nobori,T., Miura,K., Wu,D.J., Lois,A., Takabayashi,K. and Carson,D.A. (1994) Deletions of the cyclin-dependent kinase-4 inhibitor gene in multiple human cancers. Nature, 368, 753-756.
25. Kamb,A., Gruis,N.A., Weaver-Feldhaus,J., Liu,Q., Harshman,K., Tavtigian,S.V., Stockert,E., Day,R.S. 3rd, Johnson,B.E. and Skolnick,M.H. (1994) A cell cycle regulator potentially involved in genesis of many tumor types. Science, 264, 436-440.
26. Serrano,M., Lee,H., Chin,L., Cordon-Cardo,C., Beach,D. and DePinho,R.A. (1996) Role of the INK4a locus in tumor suppression and cell mortality. Cell, 85, 27-37.
27. Hannon,G.J. and Beach,D. (1994) p15INK4B is a potential effector of TGF-beta-induced cell cycle arrest. Nature, 371, 257-261.
28. Hirai,H., Roussel,M.F., Kato,J.Y., Ashmun,R.A. and Sherr,C.J. (1995) Novel INK4 proteins, p19 and p18, are specific inhibitors of the cyclin D-dependent kinases CDK4 and CDK6. Mol. Cell. Biol., 15 2672-2681.
29. Alcorta,D.A., Xiong,Y., Phelps,D., Hannon,G., Beach,D. and Barrett,J.C. (1996) Involvement of the cyclin-dependent kinase inhibitor p16 (INK4a) in replicative senescence of normal human fibroblasts. Proc. Natl Acad. Sci. USA, 93, 13742-13747.
30. Wieser,R.J., Faust,D., Dietrich,C. and Oesch,F. (1999) p16INK4 mediates contact-inhibition of growth. Oncogene, 18, 277-281.
31. Roussel,M.F. (1999) The INK4 family of cell cycle inhibitors in cancer. Oncogene, 18, 5311-5317.
32. Latres,E., Malumbres,M., Sotillo,R., Martin,J., Ortega,S., Martin-Caballero,J., Flores,J.M., Cordon-Cardo,C. and Barbacid,M. (2000) Limited overlapping roles of P15 (INK4b) and P18 (INK4c) cell cycle inhibitors in proliferation and tumorigenesis. EMBO J., 19, 3496-3506.
33. El-Diery,W.S., Tokino,T., Velculescu,V.E., Levy,D.B., Parsons,R., Trent,J.M., Lin,D., Mercer,W.E., Kinzler,K.W. and Vogelstein,B. (1993) WAF1, a potential mediator of p53 tumour suppression. Cell, 75, 817-825.
34. Xiong,Y., Hannon,G.J., Zhang,H., Casso,D., Kobayashi,R. and Beach,D. (1993) p21 is a universal inhibitor of cyclin kinases. Nature 366, 701-704.
35. Gu,Y., Turck,C.W. and Morgan,D.O. (1993) Inhibition of cdk2 activity in vivo by an associated 20K regulatory subunit. Nature 366, 707-710.
36. Polyak,K., Lee,M.H., Erdjument-Bromage,H., Koff,A., Roberts,J.M., Tempst,P. and Massague,J. (1994) Cloning of p27Kip1, a cyclin-dependent kinase inhibitor and a potential mediator of extracellular antimitogenic signals. Cell, 78, 59-66.
37. Matsuoka,S., Edwards,M.C., Bai,C., Parker,S., Zhang,P., Baldini,A., Harper,J.W. and Elledge,S.J. (1995) p57KIP2, a structurally distinct member of the p21CIP1 Cdk inhibitor family, is a candidate tumor suppressor gene. Genes Dev., 9, 650-662.
38. Krtolica,A., Krucher,N.A. and Ludlow,J.W. (1999) Molecular analysis of selected cell cycle regulatory proteins during aerobic and hypoxic maintenance of human ovarian carcinoma cells. Br. J. Cancer 80, 1875-1883.
39. Ludlow,J.W., Howell,R.L. and Smith,H.C. (1993) Hypoxic stress induces reversible hypophosphorylation of pRB and reduction in cyclin A abundance independent of cell cycle progression. Oncogene, 8, 331-339.
40. Krtolica,A., Krucher,N.A. and Ludlow,J.W. (1998) Hypoxia-induced pRB hypophosphorylation results from downregulation of CDK and upregulation of PP1 activities. Oncogene, 17, 2295-2304.
41. Gardner,L.B., Li,Q., Park,M.S., Flanagan,W.M., Semenza,G.L. and Dang,C.V. (2001) Hypoxia inhibits G1/S transition through regulation of p27 expression. J. Biol. Chem., 276, 7919-7926.
42. Zygmunt,A., Tedesco,V.C., Udho,E. and Krucher,N.A. (2002) Hypoxia stimulates p16 expression and association with cdk4. Exp. Cell. Res., 278, 53-60.
43. Reynisdottir,I., Polyak,K., Iavarone,A. and Massague,J. (1995) Kip/Cip and Ink4 Cdk inhibitors cooperate to induce cell cycle arrest in response to TGF-beta. Genes Dev., 9, 1831-1845.
44. Parry,D., Mahony,D., Wills,K. and Lees,E. (1999) Cyclin D-CDK subunit arrangement is dependent on the availability of competing INK4 and p21 class inhibitors. Mol. Cell. Biol., 19, 1775-1783.
45. Grimison,B., Langan,T.A. and Sclafani,R.A. (2000) P16Ink4a tumor suppressor function in lung cancer cells involves cyclin-dependent kinase 2 inhibition by Cip/Kip protein redistribution. Cell Growth Differ., 11, 507-515.
46. Jiang,H., Chou,H.S. and Zhu,L. (1998) Requirement of cyclin E-Cdk2 inhibition in p16 (INK4a)-mediated growth suppression. Mol. Cell. Biol., 18, 5284-5290.
47. McConnell,B.B., Gregory,F.J., Stott,F.J., Hara,E. and Peters,G. (1999) Induced expression of p16 (INK4a) inhibits both CDK4- and CDK2-associated kinase activity by reassortment of cyclin-CDK-inhibitor complexes. Mol. Cell. Biol., 19, 1981-1989.
48. Chomczynski,P. (1993) A reagent for the single-step simultaneous isolation of RNA, DNA and proteins from cell and tissue samples. Biotechniques, 15, 532-534, 536-537.
49. Katchanov,J., Harms,C., Gertz,K. et al. (2001) Mild cerebral ischemia induces loss of cyclin-dependent kinase inhibitors and activation of cell cycle machinery before delayed neuronal cell death. J. Neurosci., 21, 5045-5053.
50. Mottet,D., Dumont,V., Deccache,Y., Demazy,C., Ninane,N., Raes,M. and Michiels,C. (2003) Regulation of hypoxia-inducible factor-1alpha protein level during hypoxic conditions by the phosphatidylinositol 3-kinase/Akt/glycogen synthase kinase 3beta pathway in HepG2 cells. J. Biol. Chem., 278, 31277-31285.
51. Taylor,W.G. and Camalier,R.F. (1982) Modulation of epithelial cell proliferation in culture by dissolved oxygen. J. Cell Physiol. 111, 21-27.
52. Sherr,C.J. (2000) The Pezcoller lecture: cancer cell cycles revisited. Cancer Res., 60, 3689-3695.
53. Lundberg,A.S. and Weinberg,R.A. (1998) Functional inactivation of the retinoblastoma protein requires sequential modification by at least two distinct cyclin-cdk complexes. Mol. Cell. Biol., 18, 753-761.
54. Sugikawa,E., Hosoi,T., Yazaki,N., Gamanuma,M., Nakanishi,N. and Ohashi,M. (1999) Mutant p53 mediated induction of cell cycle arrest and apoptosis at G1 phase by 9-hydroxyellipticine. Anticancer Res., 19, 3099-3108.
55. Morel,A.P., Unsal,K., Cagatay,T., Ponchel,F., Carr,B. and Ozturk,M. (2000) P53 but not p16INK4a induces growth arrest in retinoblastoma-deficient hepatocellular carcinoma cells. J. Hepatol. 33, 254-265.
56. Soucek,T., Pusch,O., Hengstschlager-Ottnad,E., Wawra,E., Bernaschek,G. and Hengstschlager,M. (1995) Expression of the cyclin-dependent kinase inhibitor p16 during the ongoing cell cycle. FEBS Lett., 373, 164-169.
57. Hara,E., Smith,R., Parry,D., Tahara,H., Stone,S. and Peters,G. (1996) Regulation of p16CDKN2 expression and its implications for cell immortalization and senescence. Mol. Cell. Biol., 16 859-867.
58. Shapiro,G.I., Park,J.E., Edwards,C.D., Mao,L., Merlo,A., Sidransky,D., Ewen,M.E. and Rollins,B.J. (1995) Multiple mechanisms of p16INK4A inactivation in non-small cell lung cancer cell lines. Cancer Res., 55, 6200-6209.
59. Alvarez-Tejado,M., Naranjo-Suarez,S., Jimenez,C., Carrera,A.C., Landazuri,M.O. and del Peso,L. (2001) Hypoxia induces the activation of the phosphatidylinositol 3-kinase/Akt cell survival pathway in PC12 cells: protective role in apoptosis. J. Biol. Chem., 276 22368-22374.
60. Beitner-Johnson,D., Rust,R.T., Hsieh,T.C. and Millhorn,D.E. (2001) Hypoxia activates Akt and induces phosphorylation of GSK-3 in PC12 cells. Cell Signal., 13, 23-27.
61. Chen,E.Y., Mazure,N.M., Cooper,J.A. and Giaccia,A.J. (2001) Hypoxia activates a platelet-derived growth factor receptor/phosphatidylinositol 3-kinase/Akt pathway that results in glycogen synthase kinase-3 inactivation. Cancer Res., 61, 2429-2433.
62. Tang,T.T. and Lasky,L.A. (2003) The forkhead transcription factor FOXO4 induces the down-regulation of hypoxia-inducible factor 1 alpha by a von Hippel-Lindau protein-independent mechanism. J. Biol. Chem., 278, 30125-30135.
63. Arsham,A.M., Howell,J.J. and Simon,M.C. (2003) A novel hypoxia-inducible factor-independent hypoxic response regulating mammalian target of rapamycin and its targets. J. Biol. Chem., 278, 29655-29660.
64. Arsham,A.M., Plas,D.R., Thompson,C.B. and Simon,M.C. (2002) Phosphatidylinositol 3-kinase/Akt signaling is neither required for hypoxic stabilization of HIF-1 alpha nor sufficient for HIF-1-dependent target gene transcription. J. Biol. Chem., 277, 15162-15170.
65. Alvarez-Tejado,M., Alfranca,A., Aragones,J., Vara,A., Landazuri,M.O. and del Peso,L. (2002) Lack of evidence for the involvement of the phosphoinositide 3-kinase/Akt pathway in the activation of hypoxia-inducible factors by low oxygen tension. J. Biol. Chem., 277, 13508-13517.
66. Rossig,L., Badorff,C., Holzmann,Y., Zeiher,A.M. and Dimmeler,S. (2002) Glycogen synthase kinase-3 couples AKT-dependent signaling to the regulation of p21Cip1 degradation. J. Biol. Chem., 277, 9684-9689.
67. Diehl,J.A., Cheng,M., Roussel,M.F. and Sherr,C.J. (1998) Glycogen synthase kinase-3beta regulates cyclin D1 proteolysis and subcellular localization. Genes Dev., 12, 3499-3511.
68. Scandurro,A.B., Weldon,C.W., Figueroa,Y.G., Alam,J. and Beckman,B.S. (2001) Gene microarray analysis reveals a novel hypoxia signal transduction pathway in human hepatocellular carcinoma cells. Int. J. Oncol., 19, 129-135.
69. Kobayashi,Y., Pang,T., Iwamoto,T., Wakabayashi,S. and Shigekawa,M. (2000) Lithium activates mammalian Na+/H+ exchangers: isoform specificity and inhibition by genistein. Pflugers Arch., 439, 455-462.
70. Patel,S., Yenush,L., Rodriguez,P.L., Serrano,R, and Blundell,T.L. (2002) Crystal structure of an enzyme displaying both inositol-polyphosphate-1-phosphatase and 3′-phosphoadenosine-5′-phosphate phosphatase activities: a novel target of lithium therapy. J. Mol. Biol., 315, 677-685.
71. Collado,M., Medema,R.H., Garcia-Cao,I., Dubuisson,M.L., Barradas,M., Glassford,J., Rivas,C., Burgering,B.M., Serrano,M. and Lam,E.W. (2000) Inhibition of the phosphoinositide 3-kinase pathway induces a senescence-like arrest mediated by p27Kip1. J. Biol. Chem. 275, 21960-21968.
72. Doble,B.W. and Woodgett,J.R. (2003) GSK-3: tricks of the trade for a multi-tasking kinase. J. Cell Sci., 116, 1175-1186.
73. Zundel,W., Schindler,C., Haas-Kogan,D. et al. (2000) Loss of PTEN facilitates HIF-1-mediated gene expression. Genes Dev. 14, 391-396.
74. Graeber,T.G., Osmanian,C., Jacks,T., Housman,D.E., Koch,C.J., Lowe,S.W. and Giaccia,A.J. (1996) Hypoxia-mediated selection of cells with diminished apoptotic potential in solid tumours [see comments]. Nature, 379, 88-91.