Adaptive landscapes and emergent phenotypes: Why do cancers have high glycolysis?

Journal of Bioenergetics and Biomembranes

Volumn 39, Issue 3, 2007, Pages 251-257

  Gillies, Robert J ^a   Gatenby, Robert A ^a  

^a UNIVERSITY OF ARIZONA   (United States)

Author keywords

Acid base; Aerobic glycolysis; Math models; Somatic evolution

Indexed keywords

ACID; ADENOSINE TRIPHOSPHATE; FLUORODEOXYGLUCOSE; HYDROGEN; HYPOXIA INDUCIBLE FACTOR 1ALPHA; MYC PROTEIN; REACTIVE OXYGEN METABOLITE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE; RIBOSE;

CANCER; CARCINOGENESIS; CELL DEATH; CELL PROLIFERATION; ENERGY YIELD; ENZYME LINKED IMMUNOSORBENT ASSAY; EPIGENETICS; GENETICS; GLUCOSE INTAKE; GLYCOLYSIS; HUMAN; MATHEMATICAL MODEL; METASTASIS; ONCOGENE; PENTOSE PHOSPHATE CYCLE; PHENOTYPE; POSITRON EMISSION TOMOGRAPHY; PREVALENCE; PROTO ONCOGENE; SHORT SURVEY; TUMOR SUPPRESSOR GENE;

ENERGY METABOLISM; GLUCOSE; GLYCOLYSIS; HUMANS; HYPOXIA-INDUCIBLE FACTOR 1, ALPHA SUBUNIT; MODELS, BIOLOGICAL; NEOPLASM INVASIVENESS; NEOPLASMS; OXYGEN CONSUMPTION; POSITRON-EMISSION TOMOGRAPHY;

EID: 35448940364     PISSN: 0145479X     EISSN: 15736881     Source Type: Journal    
DOI: 10.1007/s10863-007-9085-y     Document Type: Short Survey

References (63)

1. Anderson ARA (2005) A hybrid mathematical model of solid tumour invasion: the importance of cell adhesion. Math Med Biol 22:163-186
2. Baudelet C et al (2004) Physiological noise in murine solid tumors using T2*-weighted gradient echo imaging: a marker for tumor acute hypoxia? Phys Med Biol 49:3389-3411
3. Beckner ME et al (2005) Glycolytic glioma cells with active glycogen synthase are sensitive to PTEN and inhibitors of P13K and gluconeogenesis. Lab Invest 85:1457-1470
4. Bhujwalla ZM et al (2001) The physiological environment in cancer vascularization, invasion and metastasis. Novartis Found Symp 240:23-38
5. Bhujwalla ZM et al (2002) Combined vascular and extracellular pH imaging of solid tumors. NMR in Biomed 15(2):114-119
6. Bos R (2002) Biologic correlates of (18) fluorodeoxyglucose uptake in human breast cancer measured by positron emission tomography. J Clin Oncol 20:379-387
7. Braun RD, Lanzel JL, Dewhirst MW (1999) Fourier analysis of fluctuations of oxygen tension and blood flow in R3230Ac tumors and muscle in rats. Am J Physiol 277:t-68
8. Brown JM, Giaccia AJ (1998) The unique physiology of solid tumors: opportunities (and problems) for cancer theraphy. Cancer Res 58:1408-1416
9. Brurberg KG, Thuen M, Ruud EB, Rofstad EK (2006) Fluctuations in p02 in irradiated human melanoma xenografts. Radiat Res 165:16-25
10. Cherk MH et al. (2006) Lack of correlation of hypoxic cell fraction and angiogenesis with glucose metabolic rate in non-small cell lung cancer assessed by 18F-fluoromisonidazole and 18F-FDG PET. J Nucl Med 47:1921-1926
11. Czernin J, Phelps ME (2002) Positron emission tomography scanning: current and future applications. Ann Rev Med 53:89-112
12. Dang CV, Semenza GL (1999) Oncogenic alterations of metabolism. Trends Biochem Sci 24:68-72
13. Dang CV, Lewis BC, Dolde C, Dang G, Shim H (1997) Oncogenes in tumor metabolism, tumorigenesis, and apoptosis. J Bioenerg Biomembranes 29:345-354
14. De Jaeger K et al (1998) Heterogeneity of tumor oxygenation: relationship to tumor necrosis, tumor size, and metastasis. Int J Radiat Oncol Biol Phys 42:717-721
15. Elstrom, RL et al (2004) Akt stimulates aerobic glycolysis in cancer cells. Cancer Res. 64:3892-3899
16. Fearon ER, Vogelstein B (1990) A genetic model for colorectal tumorigenesis. Cell 61:759-767
17. Folkman J, Folkman J (2003) Fundamental concepts of the angiogenic process. Curr Mol Med 3:643-651
18. Fyles A et al (2002) Tumor hypoxia has independent predictor impact only in patients with node-negative cervix cancer. [see comment]. J Clin Oncol 20:680-687
19. Fyles AW, Milosevic M, Pintilie M, Hill RP (1998) Cervix cancer oxygenation measured following external radiation therapy. Int J Radiat Oncol Biol Phys 42:751-753
20. Garcia M et al (1996) Biological and clinical significance of cathepsin D in breast cancer metastasis. Stem Cells 14:642-650
21. Gatenby RA (1998) Mathematical models of tumor-host interactions. Cancer J 11:2-6
22. Gatenby RA, Gawlinski ET (1996) A reaction-diffusion model of cancer invasion. Cancer Res 56:5745-5753
23. Gatenby RA, Gawlinski ET, Gmitro AF, Kaylor B, Gillies RJ (2006) Acidmediated tumor invasion: a multidisciplinary study. Cancer Res 66:5216-5223
24. Gatenby RA, Gillies RJ (2004) Why do cancers have high aerobic glycolysis? Nat Rev Cancer 4:891-899
25. Gatenby RA, Vincent TL (2003) An evolutionary model of carcinogenesis. Cancer Res 63:6212-6220
26. Gillies RJ, Raghunand N, Karczmar GA, Bhujwalla ZM (2002) MR Imaging of the tumor microenvironment. J Magn Reson Imag 15
27. Green SL, Giaccia AJ (1998) Tumor hypoxia and the cell cycle: implications for malignant progression and response to therapy.Cancer J Sci Am 4:218-223
28. Griffiths JR, McIntyre DJ, Howe FA, Stubbs M (2001) Why are cancers acidic? A carrier-mediated diffusion model for H+ transport in the interstitial fluid. Novartis Found Symp 240:46-62; discussion 62-7, 152-3
29. Griguer CE et al (2005) Glucose metabolism heterogeneity in human and mouse malignant glioma cell lines. J Neuro-Oncol 74:123-133
30. Guppy M et al (2002) Contribution by different fuels and metabolic pathways to the total ATP turnover of proliferating MCF-7 breast cancer cells. Biochem J 364:309-315
31. Haugland HK et al (2002) Expression of hypoxia-inducible factor-1alpha in cervical carcinomas: correlation with tumor oxygenation. Int J Radiat Oncol Biol Phys 53:854-861
32. Hawkins RA, Phelps ME (1988) PET in clinical oncology. Cancer Metastasis Rev 7:119-142
33. Helmlinger G, Yuan F, Dellian M, Jain RK (1997) Interstitial pH and pO2 gradients in solid tumors in vivo: high-resolution measurements reveal a lack of correlation. Nat Med 3:177-182
34. Hill RP, De Jaeger K, Jang A, Cairns R (2001) pH, hypoxia and metastasis. Novartis Found Symp 240:154-165
35. Jang A, Hill RP (1997) An examination of the effects of hypoxia, acidosis, and glucose starvation on the expression of metastasis-associated genes in murine tumor cells. Clin Exp Metastasis 15:469-483
36. Kapp DS, Giaccia AJ (1996) New directions for radiation biology research in cancer of the uterine cervix. J Natl Cancer Inst Monographs 131-139
37. Kavanagh MC, Sun A, Hu Q, Hill RP (1996) Comparing techniques of measuring tumor hypoxia in different murine tumors: eppendorf pO2 Histograph, [3H]misonidazole binding and paired survival assay. Radiat Res 145:491-500
38. Kelloff GJ et al (2005) Progress and promise of FDG-PET imaging for cancer patient management and oncologic drug development. Clin Cancer Res 11:2785-2808
39. Krogh A (1919a) The number and distribution of capillaries in muscles with calculations of the oxygen pressure head necessary for supplying the tissue. J Physiol 52:409-415
40. Krogh A (1919b) The rate of diffusion of gases through animal tissues, with some remarks on the coefficient of invasion. J Physiol 52:391-408
41. Langbein S et al (2006) Expression of transketolase TKTL1 predicts colon and urothelial cancer patient survival: Warburg effect reinterpreted. Br J Cancer 94:578-585
42. Le QT et al (2003) Identification of osteopontin as a prognostic plasma marker for head and neck squamous cell carcinomas. [see comment]. Clin Cancer Res 9:59-67
43. Montcourrier P et al (1994) Characterization of very acidic phagosomes in breast cancer cells and their association with invasion. J Cell Sci 107:2381-2391
44. Montcourrier P, Silver I, Farnoud R, Bird I, Rochefort H (1997) Breast cancer cells have a high capacity to acidify extracellular milieu by a dual mechanism. Clin Exp. Metastasis 15, 382-392
45. Naumov GN et al (2006) Role of angiogenesis in human tumor dormancy: animal models of the angiogenic switch. Cell Cycle 5:1779-1787
46. Osthus RC et al (2000) Deregulation of glucose transporter 1 and glycolytic gene expression by c-Myc. J Biol Chem 275:21797-21800
47. Patel AA et al. (2000) Cancer J
48. Pelicano H et al (2006) Glycolysis inhibition for anticancer treatment. Oncogene 25:4633-4646
49. Rajendran JG et al (2003) [(18)F]FMISO and [(18)F]FDG PET imaging in soft tissue sarcomas: correlation of hypoxia, metabolism and VEGF expression. Eur J Nuclear Med Mol Imag 30:695-704
50. Robey IF, Lien AD, Welsh SJ, Baggett BK, Gillies RJ (2005) Hypoxia-inducible factor-1alpha and the glycolytic phenotype in tumors. Neoplasia 7:324-330
51. Rochefort H, Liaudet E, Garcia M (1996) Alterations and role of human cathepsin D in cancer metastasis. Enzyme Protein 49:106-116
52. Rofstad EK et al (2006) Acidic extracellular pH promotes experimental metastasis of human melanoma cells in athymic nude mice. Can Res 66:6699-6707
53. Rozhin J, Sameni M, Ziegler G, Sloane BF (1994) Pericellular pH affects distribution and secretion of cathepsin B in Malignant Cells. Cancer Res 54:6517-6525
54. Schlappack OK, Zimmermann A, Hill RP (1991) Glucose starvation and acidosis: effect on experimental metastasic potential, DNA content and MTX resistance of murine tumour cells. Br J Cancer 64:663-670
55. Schornack PA, Gillies RJ (2003) Contributions of cell metabolism and H + diffusion to the acidic pH of tumors. Neoplasia (New York) 5:135-145
56. Semenza GL (2000) Hypoxia, clonal selection, and the role of HIF-1 in tumor progression. Crit Rev Biochem Mol Biol 35:71-103
57. Semenza GL et al (2001) 'The metabolism of tumours': 70 years later. Novartis Found Symp 240:251-260
58. Semenza GL (2002) Involvement of hypoxia-inducible factor 1 in human cancer. Internal Medicine 41:79-83
59. Serkova N, Boros LG, Serkova N, Boros LG (2005) Detection of resistance to imatinib by metabolic profiling: clinical and drug development implications. Am J PharmacoGenomics 5:293-302
60. Smallbone K, Gavaghan DJ, Gatenby RA, Maini PK (2005) The role of acidity in solid tumour growth and invasion. J Theor Biol 235:476-484
61. Thomlinson RH, Gray LH (1955) The histological structure of some human lung cancers and the possible implications for radiotherapy. Br J Cancer 9:539-549
62. Turner GA (1979) Increased release of tumour cells by collagenase at acidic pH: a possible mechanisms for metastasis. Experientia 35:1657-1658
63. Wykoff CC et al (2001) Expression of the hypoxia-inducible and tumor-associated carbonic anhydrases in ductal carcinoma in situ of the breast. Am J Pathol 158:1011-1019