Metabolism and its sequelae in cancer evolution and therapy

Cancer Journal (United States)

Volumn 21, Issue 2, 2015, Pages 88-96

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

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

Author keywords

aerobic glycolysis; carcinogenesis; metabolic phenotypes; metastasis; process of environmental selection; selected phenotypes; Warburg effect

Indexed keywords

ANTIOXIDANT; GLUCOSE; LACTIC ACID; OXYGEN;

ACIDIFICATION; ANAEROBIC GLYCOLYSIS; BIOLOGY; CANCER CELL; CANCER GROWTH; CANCER PREVENTION; CANCER PROGNOSIS; CANCER SURVIVAL; CANCER THERAPY; CARCINOGENESIS; ENZYME SUBSTRATE; EXTRACELLULAR SPACE; FERMENTATION; HEREDITY; HUMAN; INTRADUCTAL CARCINOMA; METABOLISM; METASTASIS; MICROENVIRONMENT; MOLECULAR EVOLUTION; NEOPLASM; NONHUMAN; PH; PHENOTYPE; PRIMARY TUMOR; PRIORITY JOURNAL; REVIEW; SPECIES; TUMOR IMMUNITY; ANIMAL; ANOXIA; CELL TRANSFORMATION; DISEASE COURSE; ENERGY METABOLISM; GENETICS; NEOPLASMS; PATHOLOGY; TUMOR INVASION; TUMOR MICROENVIRONMENT;

ANIMALS; ANOXIA; CELL TRANSFORMATION, NEOPLASTIC; DISEASE PROGRESSION; ENERGY METABOLISM; HUMANS; NEOPLASM INVASIVENESS; NEOPLASMS; PHENOTYPE; TUMOR MICROENVIRONMENT;

EID: 84926669244     PISSN: 15289117     EISSN: 1540336X     Source Type: Journal    
DOI: 10.1097/PPO.0000000000000102     Document Type: Review

References (73)

1. Knudson AG Jr. Mutation and cancer in man. Cancer. 1977;39(4 suppl): 1882-1886.
2. Nowell PC. The clonal nature of neoplasia. Cancer Cells. 1989;1:29-30.
3. Suva ML, Riggi N, Bernstein BE. Epigenetic reprogramming in cancer. Science. 2013;339:1567-1570.
4. Dawson MA, Kouzarides T. Cancer epigenetics: from mechanism to therapy. Cell. 2012;150:12-27.
5. Whitesell L, Lindquist SL. HSP90 and the chaperoning of cancer. Nat Rev Cancer. 2005;5:761-772.
6. Lee AS. Glucose-regulated proteins in cancer: molecular mechanisms and therapeutic potential. Nat Rev Cancer. 2014;14:263-276.
7. Gatenby RA, Gillies RJ, Brown JS. Of cancer and cave fish. Nat Rev Cancer. 2011;11:237-238.
8. Igney FH, Krammer PH. Death and anti-death: tumour resistance to apoptosis. Nat Rev Cancer. 2002;2:277-288.
9. Gillies RJ, Gatenby RA. Adaptive landscapes and emergent phenotypes: why do cancers have high glycolysis? J Bioenerg Biomembr. 2007;39: 251-257.
10. Gillies RJ, Gatenby RA. Hypoxia and adaptive landscapes in the evolution of carcinogenesis. Cancer Metastasis Rev. 2007;26:311-317.
11. Chmielecki J, Foo J, Oxnard GR, et al. Optimization of dosing for EGFRmutant non-small cell lung cancer with evolutionary cancer modeling. Sci Transl Med. 2011;3(90):90ra59.
12. Whelan KA, Schwab LP, Karakashev SV, et al. The oncogene HER2/neu (ERBB2) requires the hypoxia-inducible factor HIF-1 for mammary tumor growth and anoikis resistance. J Biol Chem. 2013;288:15865-15877.
13. Park SH, Riley Pt, Frisch SM. Regulation of anoikis by deleted in breast cancer-1 (DBC1) through NF-kappaB. Apoptosis. 2013;18:949-962.
14. Carmeliet P, Jain RK. Angiogenesis in cancer and other diseases. Nature. 2000;407:249-257.
15. Gatenby RA, Gillies RJ. Why do cancers have high aerobic glycolysis? Nat Rev Cancer. 2004;4:891-899.
16. Wykoff CC, Beasley NJP, Watson PH, et al. Hypoxia-inducible expression of tumor-associated carbonic anhydrases. Cancer Res. 2000;60: 7075-7083.
17. Gillies RJ, Verduzco D, Gatenby RA. Evolutionary dynamics of carcinogenesis and why targeted therapy does not work. Nat Rev Cancer. 2012; 12:487-493.
18. Graeber TG, Osmanian C, Jacks T, et al. Hypoxia-mediated selection of cells with diminished apoptotic potential in solid tumours. Nature. 1996; 379:88-91.
19. Verduzco D, Xu L, lloyd MC, et al. Intermittent hypoxia selects for genotypes and phenotypes that increase survival, invasion, and therapy resistance. PLoS One. 2015. In press.
20. Bensaad K, Tsuruta A, Selak MA, et al. TIGAR, a p53-inducible regulator of glycolysis and apoptosis. Cell. 2006;126:107-120.
21. Gatenby RA, Gillies RJ. A microenvironmental model of carcinogenesis. Nat Rev Cancer. 2008;8:56-61.
22. Yun J, Rago C, Cheong I, et al. Glucose deprivation contributes to the development of KRAS pathway mutations in tumor cells. Science. 2009; 325:1555-1559.
23. Burke K, Tang P, Brown E. Second harmonic generation reveals matrix alterations during breast tumor progression. J Biomed Opt. 2013;18:31106.
24. Kakkad SM, Penet MF, Akhbardeh A, et al. Hypoxic tumor environments exhibit disrupted collagen I fibers and lowmacromolecular transport. PLoS One. 2013;8:e81869.
25. Riemann A, Ihling A, Thomas J, et al. Acidic environment activates inflammatory programs in fibroblasts via a cAMP-MAPK pathway. Biochim Biophys Acta. 2014;1853:299-307.
26. Luddy KA, Robertson-Tessi M, Tafreshi NK, et al. The role of toll-like receptors in colorectal cancer progression: evidence for epithelial to leucocytic transition. Front Immunol. 2014;5:429.
27. ChowMT, Moller A, SmythMJ. Inflammation and immune surveillance in cancer. Semin Cancer Biol. 2012;22:23-32.
28. Hamai A, Benlalam H, Meslin F, et al. Immune surveillance of human cancer: if the cytotoxic T-lymphocytes play the music, does the tumoral system call the tune? Tissue Antigens. 2010;75:1-8.
29. Lardner A. The effects of extracellular pH on immune function. J Leukoc Biol. 2001;69:522-530.
30. Calcinotto A, Filipazzi P, Grioni M, et al.Modulation of microenvironment acidity reverses anergy in human and murine tumor-infiltrating T lymphocytes. Cancer Res. 2012;72:2746-2756.
31. Gillies RJ, Schornack PA, Secomb TW, et al. Causes and effects of heterogeneous perfusion in tumors. Neoplasia. 1999;1:197-207.
32. Porporato PE, Dhup S, Dadhich RK, et al. Anticancer targets in the glycolytic metabolism of tumors: a comprehensive review. Front Pharmacol. 2011;2:49.
33. Gatenby RA, Gawlinski ET, Gmitro AF, et al. Acid-mediated tumor invasion: a multidisciplinary study. Cancer Res. 2006;66:5216-5223.
34. Estrella V, Chen T, Lloyd M, et al. Acidity generated by the tumor microenvironment drives local invasion [published online ahead of print January 5, 2013]. In: Cancer Res. 2013.
35. Fukumura D, Xu L, Chen Y, et al. Hypoxia and acidosis independently upregulate vascular endothelial growth factor transcription in brain tumors in vivo. Cancer Res. 2001;61:6020-6024.
36. Xu L, Fukumura D, Jain RK. Acidic extracellular pH induces vascular endothelial growth factor (VEGF) in human glioblastoma cells via ERK1/2 MAPK signaling pathway: mechanism of low pH-induced VEGF. J Biol Chem. 2002;277:11368-11374.
37. Stubbs M, McSheehy PM, Griffiths JR, et al. Causes and consequences of tumour acidity and implications for treatment. MolMed Today. 2000;6:15-19.
38. Gillies RJ, Liu Z, Bhujwalla Z. 31P-MRS measurements of extracellular pH of tumors using 3-aminopropylphosphonate. Am J Physiol. 1994;267: C195-203.
39. van Sluis R, Bhujwalla ZM, Raghunand N, et al. In vivo imaging of extracellular pH using 1H MRSI. Magn Reson Med. 1999;41:743-750.
40. Lora-Michiels M, Yu D, Sanders L, et al. Extracellular pH and P-31 magnetic resonance spectroscopic variables are related to outcome in canine soft tissue sarcomas treated with thermoradiotherapy. Clin Cancer Res. 2006;12:5733-5740.
41. Rozhin J, Sameni M, Ziegler G, et al. Pericellular pH affects distribution and secretion of cathepsin B in malignant cells. Cancer Res. 1994;54:6517-6525.
42. Robey IF, Baggett BK, Kirkpatrick ND, et al. Bicarbonate increases tumor pH and inhibits spontaneous metastases. Cancer Res. 2009;69:2260-2268.
43. Rofstad EK, Mathiesen B, Kindem K, et al. Acidic extracellular pH promotes experimental metastasis of human melanoma cells in athymic nude mice. Cancer Res. 2006;66:6699-6707.
44. Chambers AF, Matrisian LM. Changing views of the role of matrix metalloproteinases in metastasis. J Natl Cancer Inst. 1997;89:1260-1270.
45. Sloane BF, Moin K, Krepela E, et al. Cathepsin B and its endogenous inhibitors: the role in tumor malignancy. Cancer Metastasis Rev. 1990;9.
46. Rochefort H, Liaudet-Coopman E. Cathepsin D in cancer metastasis: a protease and a ligand. APMIS. 1999;107:86-95.
47. Gatenby RA, Gawlinski ET. A reaction-diffusion model of cancer invasion. Cancer Res. 1996;56:5745-5753.
48. Moellering RE, Black KC, Krishnamurty C, et al. Acid treatment of melanoma cells selects for invasive phenotypes. Clin Exp Metastasis. 2008;25: 411-425.
49. Schlappack OK, Zimmermann A, Hill RP. Glucose starvation and acidosis: effect on experimental metastatic potential, DNA content and MTX resistance of murine tumour cells. Br J Cancer. 1991;64:663-670.
50. Robertson-Tessi M, Gillies RJ, Gatenby RA, et al. The impact of heterogeneity on tumor growth, invasion and treatment outcomes. Cancer Res. 2015. In press.
51. Wojtkowiak JW, Rothberg JF, Kumar VK, et al. Chronic autophagy is a cellular adaptation to tumor acidic pH microenvironments. Cancer Res. 2012; 72:3938-3947
52. Chiche J, Ilc K, Laferriere J, et al. Hypoxia-inducible carbonic anhydrase IX and XII promote tumor cell growth by counteracting acidosis through the regulation of the intracellular pH. Cancer Res. 2009;69:358-368.
53. Ivanov S, Liao SY, Ivanova A, et al. Expression of hypoxia-inducible cellsurface transmembrane carbonic anhydrases in human cancer. Am J Pathol. 2001;158:905-919.
54. Gatenby RA. The potential role of transformation-induced metabolic changes in tumor-host interaction. Cancer Res. 1995;55:4151-4156.
55. Steffan JJ, Snider JL, Skalli O, et al. Na+/H+ exchangers and RhoA regulate acidic extracellular pH-induced lysosome trafficking in prostate cancer cells. Traffic. 2009;10:737-753.
56. GlundeK,Guggino SE, Solaiyappan M, et al. Extracellular acidification alters lysosomal trafficking in human breast cancer cells. Neoplasia. 2003;5: 533-545.
57. Raghunand N, He X, van Sluis R, et al. Enhancement of chemotherapy by manipulation of tumour pH. Br J Cancer. 1999;80:1005-1011.
58. Chen LQ, Howison CM, Jeffery JJ, et al. Evaluations of extracellular pH within in vivo tumors using acidoCEST MRI. Magn Reson Med. 2014; 72:1408-1417.
59. Andreev OA, Dupuy AD, SegalaM, et al. Mechanism and uses of a membrane peptide that targets tumors and other acidic tissues in vivo. Proc Natl Acad Sci U S A. 2007;104:7893-7898.
60. Mahoney BP, Raghunand N, Baggett B, et al. Tumor acidity, ion trapping and chemotherapeutics. I. Acid pH affects the distribution of chemotherapeutic agents in vitro. Biochem Pharmacol. 2003;66:1207-1218.
61. Raghunand N, Mahoney BP, Gillies RJ. Tumor acidity, ion trapping and chemotherapeutics. II. pH-dependent partition coefficients predict importance of ion trapping on pharmacokinetics of weakly basic chemotherapeutic agents. Biochem Pharmacol. 2003;66:1219-1229.
62. Ibrahim-Hashim A, Cornnell HH, Coelho Ribeiro Mde L, et al. Reduction of metastasis using a nonvolatile buffer. Clin Exp Metastasis. 2011;28: 841-849.
63. Ribeiro M, Silva AS, Bailey K, et al. Buffer therapy for cancer. J Nutr Food Sci. 2012;S2:1-7.
64. Ibrahim-Hashim A, Cornnell HH, Abrahams D, et al. Systemic buffers inhibit carcinogenesis in TRAMP mice. J Urol. 2012;188:624-631.
65. Yachida S, Jones S, Bozic I, et al. Distant metastasis occurs late during the genetic evolution of pancreatic cancer. Nature. 2010;467:1114-1117.
66. Gerlinger M, Rowan AJ, Horswell S, et al. Intratumor heterogeneity and branched evolution revealed by multiregion sequencing. N Engl J Med. 2012;366:883-892.
67. Sottoriva A, Spiteri I, Piccirillo SG, et al. Intratumor heterogeneity in human glioblastoma reflects cancer evolutionary dynamics. Proc Natl Acad Sci U S A. 2013;110:4009-4014.
68. Winge O. Zytologische untersuchungen uber die natur maligner tumoren. II. Teerkarzinome bei mausen. Z Zellforsch Mikrosk Anat. 1930;10: 683-735.
69. Allred DC, Brown P, Medina D. The origins of estrogen receptor alpha-positive and estrogen receptor alpha-negative human breast cancer. Breast Cancer Res. 2004;6:240-245.
70. Gatenby RA, Grove O, Gillies RJ. Quantitative imaging in cancer evolution and ecology. Radiology. 2013;269:8-15.
71. Alfarouk KO, Ibrahim ME, Gatenby RA, et al. Riparian ecosystems in human cancers. Evol Appl. 2013;6:46-53.
72. Aerts HJ, Velazquez ER, Leijenaar RT, et al. Decoding tumour phenotype by noninvasive imaging using a quantitative radiomics approach. Nat Commun. 2014;5:4006.
73. Lambin P, Rios-Velazquez E, Leijenaar R, et al. Radiomics: extractingmore information from medical images using advanced feature analysis. Eur J Cancer. 2012;48:441-446.