Adaptation to hypoxia and acidosis in carcinogenesis and tumor progression

Seminars in Cancer Biology

Volumn 18, Issue 5, 2008, Pages 330-337

  Fang, Jennifer S ^a   Gillies, Robert D ^b   Gatenby, Robert A ^b  

^a UNIVERSITY OF ARIZONA COLLEGE OF MEDICINE   (United States)

^b H LEE MOFFITT CANCER CENTER AND RESEARCH INSTITUTE   (United States)

Author keywords

Acidosis; Carcinogenesis; Glycolysis; HIF1 ; Hypoxia

Indexed keywords

CARBONATE DEHYDRATASE; GLUCOSE TRANSPORTER 1; GLUCOSE TRANSPORTER 2; GLUCOSE TRANSPORTER 3; GLUCOSE TRANSPORTER 4; HISTONE ACETYLTRANSFERASE PCAF; HYPOXIA INDUCIBLE FACTOR 1ALPHA; HYPOXIA INDUCIBLE FACTOR 1BETA; LACTATE DEHYDROGENASE; MITOGEN ACTIVATED PROTEIN KINASE; NICOTINAMIDE ADENINE DINUCLEOTIDE; PENTOSE PHOSPHATE; SODIUM PROTON EXCHANGE PROTEIN 1; UBIQUITIN; UBIQUITIN PROTEIN LIGASE;

ACIDOSIS; BASEMENT MEMBRANE; CANCER CELL; CANCER INVASION; CANCER MODEL; CARCINOGENESIS; CELL HYPOXIA; CELL PROLIFERATION; ENVIRONMENTAL FACTOR; ENZYME PHOSPHORYLATION; EPIGENETICS; GENE EXPRESSION; GLYCOLYSIS; HUMAN; IMMUNOHISTOCHEMISTRY; MALIGNANT NEOPLASTIC DISEASE; METASTASIS; NONHUMAN; ONCOGENE C MYC; PHENOTYPE; PRECANCER; REVIEW; TUMOR GROWTH; UPREGULATION;

ADAPTATION, BIOLOGICAL; CELL HYPOXIA; CELL PROLIFERATION; DISEASE PROGRESSION; HUMANS; HYDROGEN-ION CONCENTRATION; NAD; NEOPLASMS; TRANSCRIPTION FACTORS;

EID: 48349111944     PISSN: 1044579X     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.semcancer.2008.03.011     Document Type: Review

References (62)

1. Foulds L. The experimental study of tumor progression: a review. Cancer Res 14 (1954) 327-339
2. Gillies R.J., and Gatenby R.A. Adaptive landscapes and emergent phenotypes: why do cancers have high glycolysis?. J Bioenerg Biomembr 39 (2007) 251-257
3. Gatenby R.A., and Gillies R.J. A microenvironmental model of carcingenesis. Nat Rev Cancer 8 (2008) 56-61
4. Hanahan D., and Weinberg R.A. The hallmarks of cancer. Cell 100 (2000) 57-70
5. Krogh A. The number and distribution of capillaries in muscles with calculations of the oxygen pressure head necessary for supplying the tissue. J Physiol 20 (1919) 409-415
6. Thomlinson R.H., and Gray L.H. The histological structure of some human lung cancers and the possible implications for radiotherapy. Br J Cancer 9 (1955) 539-549
7. 2 gradients in solid tumors in vivo: high-resolution measurements reveal a lack of correlation. Nat Med 3 (1997) 177-182
8. Wykoff C.C., Beasley N., Watson P.H., Campo L., Chia S.K., English R., Pastorek J., Sly W.S., Ratcliffe P., and Harris A.L. Expression of the hypoxia-inducible and tumor-associated carbonic anhydrases in ductal carcinoma in situ of the breast. Am J Pathol 158 (2001) 1011-1019
9. Gatenby R.A., and Gillies R.J. Why do cancers have high aerobic glycolysis?. Nat Rev Cancer 4 (2004) 891-899
10. Ramaiah A., Hathaway J.A., and Atkinson D.D. Adenylate as a metabolic regulator. Effect on yeast phosphofructokinase kinetics. J Biol Chem 239 (1964) 3619-3622
11. Passonneau J.V., and Lowry O.H. Phosphofructokinase and the Pasteur effect. Biochem Biophys Res Commun 20 7 (1962) 10-15
12. Hardie D.G. Minireview: the AMP-activated protein kinase cascade: the key sensor of cellular energy status. Endocrinology 144 (2003) 5179-5183
13. Hardie D.G. Metabolic control: a new solution to an old problem. Curr Biol 9 10 (2000) R757-R759
14. Russell III R.R., Bergeron R., Shulman G.I., and Young L.H. Translocation of myocardial GLUT-4 and increased glucose uptake through activation of AMPK by AICAR. Am J Physiol 277 (1999) 643-649
15. Cerdan S., Rodrigues T.B., Sierra A., Benito M., Fonseca L.L., Fonseca C.P., and Garcia-Martin M.L. The redox switch/redox coupling hypothesis. Neurochem Int 48 (2006) 523-530
16. Warburg O. On the origin of cancer cells. Science 123 (1956) 309-314
17. Chesney J., Mitchell R., Benigni F., Bacher M., Spiegel L., Al Abed Y., Han J.H., Metz C., and Bucala R. An inducible gene product for 6-phosphofructo-2-kinase with an AU-rich instability element: role in tumor cell glycolysis and the Warburg effect. Proc Natl Acad Sci USA 96 (1999) 3047-3052
18. Liao D.J., and Dickson R.B. c-Myc in breast cancer. Endocr Relat Cancer 7 (2000) 143-164
19. Dang C.V., Resar L.M., Emison E., Kim S., Li Q., Prescott J.E., Wonsey D., and Zeller K. Function of the c-Myc oncogenic transcription factor. Exp Cell Res 253 (1999) 63-77
20. Land H., Chen A.C., Morgenstern J.P., Parada L.F., and Weinberg R.A. Behavior of myc and ras oncogenes in transformation of rat embryo fibroblasts. Mol Cell Biol 6 (1986) 1917-1925
21. Shim H., Dolde C., Lewis B.C., Wu C.S., Dang G., Jungmann R.A., Dalla-Favera R., and Dang C.V. c-Myc transactivation of LDH-A: implications for tumor metabolism and growth. Proc Natl Acad Sci USA 94 (1997) 6658-6663
22. Osthus R.C., Shim H., Kim S., Li Q., Reddy R., Mukherjee M., Xu Y., Wonsey D., Lee L.A., and Dang C.V. Deregulation of glucose transporter 1 and glycolytic gene expression by c-Myc. J Biol Chem 275 (2000) 21797-21800
23. 2 homeostasis by hypoxia-inducible factor 1. Annu Rev Cell Dev Biol 15 (1999) 551-578
24. Kallio P.J., Pongratz I., Gradin K., McGuire J., and Poellinger L. Activation of hypoxia-inducible factor 1alpha: posttranscriptional regulation and conformational change by recruitment of the Arnt transcription factor. Proc Natl Acad Sci USA 94 (1997) 5667-5672
25. 2 tension. Proc Natl Acad Sci USA 92 (1995) 5510-5514
26. Wang G.L., and Semenza G.L. General involvement of hypoxia-inducible factor 1 in transcriptional response to hypoxia. Proc Natl Acad Sci USA 90 (1993) 4304-4308
27. Bergeron M., Yu A.Y., Solway K.E., Semenza G.L., and Sharp F.R. Induction of hypoxia-inducible factor-1 (HIF-1) and its target genes following focal ischaemia in rat brain. Eur J Neurosci 11 (1999) 4159-4170
28. 2 tension. Am J Physiol 271 (1996) C1172-C1180
29. Jiang B.H., Rue E., Wang G.L., Roe R., and Semenza G.L. Dimerization, DNA binding, and transactivation properties of hypoxia-inducible factor 1. J Biol Chem 271 (1996) 17771-17778
30. Salceda S., and Caro J. 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 (1997) 22642-22647
31. Ke Q., and Costa M. Hypoxia-inducible factor-1 (HIF-1). Mol Pharmacol 70 (2006) 1469-1480
32. Metzen E., Berchner-Pfannschmidt U., Stengel P., Marxsen J.H., Stolze I., Klinger M., Huang W.Q., Wotzlaw C., Hellwig-Bürgel T., Jelkmann W., Acker H., and Fandrey J. Intracellular localisation of human HIF-1 alpha hydroxylases: implications for oxygen sensing. J Cell Sci 116 (2003) 1319-1326
33. Semenza G.L., Nejfelt M.K., Chi S.M., and Antonarakis S.E. Hypoxia-inducible nuclear factors bind to an enhancer element located 3′ to the human erythropoietin gene. Proc Natl Acad Sci USA 88 (1991) 5680-5684
34. Chen C., Pore N., Behrooz A., Ismail-Beigi F., and Maity A. Regulation of glut1 mRNA by hypoxia-inducible factor-1. Interaction between H-ras and hypoxia. J Biol Chem 276 (2001) 9519-9525
35. Lu H., Forbes R.A., and Verma A. Hypoxia-inducible factor 1 activation by aerobic glycolysis implicates the Warburg effect in carcinogenesis. J Biol Chem 277 (2002) 23111-23115
36. Folkman J. Angiogenesis. Annu Rev Med 57 (2006) 1-18
37. Nelson C.M., and Bissell M.J. Of extracellular matrix, scaffolds, and signaling: tissue architecture regulates development, homeostasis, and cancer. Annu Rev Cell Dev Biol 22 (2006) 287-309
38. Fearon E.R., and Vogelstein B. A genetic model for colorectal tumorigenesis. Cell 61 (1990) 759-767
39. Beckman R.A., and Loeb L.A. Genetic instability in cancer: theory and experiment. Semin Cancer Biol 15 (2005) 423-435
40. Gatenby R.A., Vincent T., and Gillies R. Evolutionary dynamics in carcinogenesis. Math. Models Methods Appl. Sci. 15 (2005) 1-20
41. Lamlum H., Papadopoulou A., Ilyas M., Rowan A., Gillet C., Hanby A., Talbot I., Bodmer W., and Tomlinson I. APC mutations are sufficient for the growth of early colorectal adenomas. Proc Natl Acad Sci USA 97 5 (2000) 2225-2228
42. Dubina M.V., Iatckii N.A., Popov D.E., Vasil'ev S.V., and Krutovskikh V.A. Connexin 43, but not connexin 32, is mutated at advanced stages of human sporadic colon cancer. Oncogene 21 (2002) 4992-4996
43. Hirschi K.K., Xu C.E., Tsukamoto T., and Sager R. Gap junction genes Cx26 and Cx43 individually suppress the cancer phenotype of human mammary carcinoma cells and restore differentiation potential. Cell Growth Differ 7 (1996) 861-870
44. Nahta R., and Esteva F.J. Bcl-2 antisense oligonucleotides: a potential novel strategy for the treatment of breast cancer. Semin Oncol 30 (2003) 143-149
45. Hayflick L. Mortality and immortality at the cellular level. A review. Biochemistry (Mosc) 62 (1997) 1180-1190
46. Gatenby R.A., Gawlinski E.T., Gmitro A.F., Kaylor B., and Gillies R.J. Acid-mediated tumor invasion: a multidisciplinary study. Cancer Res 66 (2006) 5216-5223
47. Raghunand N., and Gillies R.J. pH and drug resistance in tumors. Drug Resist Updat 3 (2000) 39-47
48. Morita T. Low pH leads to sister-chromatid exchanges and chromosomal aberrations, and its clastogenicity is S-dependent. Mutat Res 334 (1995) 301-308
49. Morita T., Nagaki T., Fukuda I., and Okumura K. Clastogenicity of low pH to various cultured mammalian cells. Mutat Res 268 (1992) 297-305
50. Cairns R.A., Kalliomaki T., and Hill R.P. Acute (cyclic) hypoxia enhances spontaneous metastasis of KHT murine tumors. Cancer Res 61 (2001) 8903-8908
51. Gimbrone Jr. M.A., Leapman S.B., Cotran R.S., and Folkman J. Tumor dormancy in vivo by prevention of neovascularization. J Exp Med 136 (1972) 261-276
52. Brem S., Brem H., Folkman J., Finkelstein D., and Patz A. Prolonged tumor dormancy by prevention of neovascularization in the vitreous. Cancer Res 36 (1976) 2807-2812
53. Schmaltz C., Hardenbergh P.H., Wells A., and Fisher D.E. Regulation of proliferation-survival decisions during tumor cell hypoxia. Mol Cell Biol 18 (1998) 2845-2854
54. Ribatti D., Conconi M.T., and Nussdorfer G.G. Nonclassic endogenous regulators of angiogenesis. Pharmacol Rev 59 (2007) 185-205
55. Kimura H., Braun R.D., Ong E.T., Hsu R., Secomb T.W., Papahadjopoulos D., Hong K., and Dewhirst M.W. Fluctuations in red cell flux in tumor microvessels can lead to transient hypoxia and reoxygenation in tumor parenchyma. Cancer Res 56 (1996) 5522-5528
56. Brizel D.M., Scully S.P., Harrelson J.M., Layfield L.J., Bean J.M., Prosnitz L.R., and Dewhirst M.W. Tumor oxygenation predicts for the likelihood of distant metastases in human soft tissue sarcoma. Cancer Res 56 (1996) 941-943
57. Young S.D., Marshall R.S., and Hill R.P. Hypoxia induces DNA overreplication and enhances metastatic potential of murine tumor cells. Proc Natl Acad Sci USA 85 (1988) 9533-9537
58. Stackpole C.W., Groszek L., and Kalbag S.S. Benign-to-malignant B16 melanoma progression induced in two stages in vitro by exposure to hypoxia. J Natl Cancer Inst 86 (1994) 361-367
59. Gatenby R.A., and Gillies R.J. Glycolysis in cancer: a potential target for therapy. Int J Biochem Cell Biol 39 (2007) 1358-1366
60. Gatenby R.A., Smallbone K., Maini P.K., Rose F., Averill J., Nagle R.B., Worrall L., and Gillies R.J. Cellular adaptations to hypoxia and acidosis during somatic evolution of breast cancer. Br J Cancer 97 5 (2007) 646-653
61. Gatenby R.A., and Vincent T.L. An evolutionary model of carcinogenesis. Cancer Res 63 (2003) 6212-6220
62. Kondoh H., Lleonart Me, Bernard D., and Gil J. Protection from oxidative stress by enhanced glycolysis; a possible mechanism of cellular immortalization. Histol Histopathol 22 1 (2007) 85-90