Central role of lactic acidosis in cancer cell resistance to glucose deprivation-induced cell death

Journal of Pathology

Volumn 227, Issue 2, 2012, Pages 189-199

  Wu, Hao ^a   Ding, Zonghui ^a   Hu, Danqing ^a   Sun, Feifei ^a   Dai, Chunyan ^a   Xie, Jiansheng ^a   Hu, Xun ^a  

^a ZHEJIANG UNIVERSITY   (China)

Author keywords

apoptosis; autophagy; cell cycle; glucose deprivation; lactic acidosis

Indexed keywords

GLUCOSE; LACTATE SODIUM;

ARTICLE; AUTOPHAGY; CANCER CELL; CANCER RESISTANCE; CANCER SURVIVAL; CELL CYCLE ARREST; CELL CYCLE G0 PHASE; CELL DEATH; CELL PROLIFERATION; CELL VIABILITY; CONTROLLED STUDY; G1 PHASE CELL CYCLE CHECKPOINT; HUMAN; HUMAN CELL; LACTIC ACIDOSIS; PRIORITY JOURNAL; TUMOR MICROENVIRONMENT;

ACIDOSIS, LACTIC; ANIMALS; APOPTOSIS; AUTOPHAGY; CELL LINE, TUMOR; CELL SURVIVAL; G1 PHASE CELL CYCLE CHECKPOINTS; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, NEOPLASTIC; GLUCOSE; HUMANS; HYDROGEN-ION CONCENTRATION; MICE; NEOPLASMS; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; TIME FACTORS; TUMOR MICROENVIRONMENT;

EID: 84862800709     PISSN: 00223417     EISSN: 10969896     Source Type: Journal    
DOI: 10.1002/path.3978     Document Type: Article

References (63)

1. Hanahan D, Weinberg RA,. Hallmarks of cancer: the next generation. Cell 2011; 144: 646-674.
2. Kroemer G, Pouyssegur J,. Tumor cell metabolism: cancer's Achilles' heel. Cancer Cell 2008; 13: 472-482.
3. Annibaldi A, Widmann C,. Glucose metabolism in cancer cells. Curr Opin Clin Nutr Metab Care 2010; 13: 466-470.
4. Gatenby RA, Gillies RJ,. Why do cancers have high aerobic glycolysis? Nature Rev Cancer 2004; 4: 891-899.
5. Warburg O,. On the origin of cancer cells. Science 1956; 123: 309-314.
6. Bergers G, Benjamin LE,. Tumorigenesis and the angiogenic switch. Nature Rev Cancer 2003; 3: 401-410.
7. Tredan O, Galmarini CM, Patel K, et al., Drug resistance and the solid tumor microenvironment. J Natl Cancer Inst 2007; 99: 1441-1454.
8. Fukumura D, Jain RK,. Tumor microvasculature and microenvironment: targets for anti-angiogenesis and normalization. Microvasc Res 2007; 74: 72-84.
9. Skinner SA, Tutton PJ, O'Brien PE,. Microvascular architecture of experimental colon tumors in the rat. Cancer Res 1990; 50: 2411-2417.
10. Denko NC,. Hypoxia, HIF1 and glucose metabolism in the solid tumour. Nature Rev Cancer 2008; 8: 705-713.
11. Chen JL, Lucas JE, Schroeder T, et al., The genomic analysis of lactic acidosis and acidosis response in human cancers. PLoS Genet 2008; 4: e1000293.
12. Irizarry RA, Hobbs B, Collin F, et al., Exploration, normalization, and summaries of high density oligonucleotide array probe level data. Biostatistics 2003; 4: 249-264.
13. Tusher VG, Tibshirani R, Chu G,. Significance analysis of microarrays applied to the ionizing radiation response. Proc Natl Acad Sci U S A 2001; 98: 5116-5121.
14. Saeed AI, Sharov V, White J, et al., TM4: a free, open-source system for microarray data management and analysis. Biotechniques 2003; 34: 374-378.
15. Han W, Li L, Qiu S, et al., Shikonin circumvents cancer drug resistance by induction of a necroptotic death. Mol Cancer Ther 2007; 6: 1641-1649.
16. Trimboli AJ, Waite BM, Atsumi G, et al., Influence of coenzyme A-independent transacylase and cyclooxygenase inhibitors on the proliferation of breast cancer cells. Cancer Res 1999; 59: 6171-6177.
17. Gibon Y, Larher F,. Cycling assay for nicotinamide adenine dinucleotides: NaCl precipitation and ethanol solubilization of the reduced tetrazolium. Anal Biochem 1997; 251: 153-157.
18. Knudsen ES, Knudsen KE,. Tailoring to RB: tumour suppressor status and therapeutic response. Nature Rev Cancer 2008; 8: 714-724.
19. Chu IM, Hengst L, Slingerland JM,. The Cdk inhibitor p27 in human cancer: prognostic potential and relevance to anticancer therapy. Nature Rev Cancer 2008; 8: 253-267.
20. Nakayama KI, Nakayama K,. Ubiquitin ligases: cell-cycle control and cancer. Nature Rev Cancer 2006; 6: 369-381.
21. Toczyski DP, Galgoczy DJ, Hartwell LH,. CDC5 and CKII control adaptation to the yeast DNA damage checkpoint. Cell 1997; 90: 1097-1106.
22. Lobrich M, Jeggo PA,. The impact of a negligent G2/M checkpoint on genomic instability and cancer induction. Nature Rev Cancer 2007; 7: 861-869.
23. Levine B, Klionsky DJ,. Development by self-digestion: molecular mechanisms and biological functions of autophagy. Dev Cell 2004; 6: 463-477.
24. Mathew R, Karantza-Wadsworth V, White E,. Role of autophagy in cancer. Nature Rev Cancer 2007; 7: 961-967.
25. Jin S, DiPaola RS, Mathew R, et al., Metabolic catastrophe as a means to cancer cell death. J Cell Sci 2007; 120: 379-383.
26. Liang J, Shao SH, Xu ZX, et al., The energy sensing LKB1-AMPK pathway regulates p27(kip1) phosphorylation mediating the decision to enter autophagy or apoptosis. Nature Cell Biol 2007; 9: 218-224.
27. Tanaka Y, Guhde G, Suter A, et al., Accumulation of autophagic vacuoles and cardiomyopathy in LAMP-2-deficient mice. Nature 2000; 406: 902-906.
28. Huynh KK, Eskelinen EL, Scott CC, et al., LAMP proteins are required for fusion of lysosomes with phagosomes. EMBO J 2007; 26: 313-324.
29. Lee YJ, Galoforo SS, Berns CM, et al., Glucose deprivation-induced cytotoxicity in drug resistant human breast carcinoma MCF-7/ADR cells: role of c-myc and bcl-2 in apoptotic cell death. J Cell Sci 1997; 110: 681-686.
30. Caro-Maldonado A, Tait SW, Ramirez-Peinado S, et al., Glucose deprivation induces an atypical form of apoptosis mediated by caspase-8 in Bax-, Bak-deficient cells. Cell Death Differ 2010; 17: 1335-1344.
31. Galonek HL, Hardwick JM,. Upgrading the BCL-2 network. Nature Cell Biol 2006; 8: 1317-1319.
32. Degenhardt K, Mathew R, Beaudoin B, et al., Autophagy promotes tumor cell survival and restricts necrosis, inflammation, and tumorigenesis. Cancer Cell 2006; 10: 51-64.
33. Karantza-Wadsworth V, Patel S, Kravchuk O, et al., Autophagy mitigates metabolic stress and genome damage in mammary tumorigenesis. Genes Dev 2007; 21: 1621-1635.
34. Amaravadi R, Thompson CB,. The survival kinases Akt and Pim as potential pharmacological targets. J Clin Invest 2005; 115: 2618-2624.
35. Irmler M, Thome M, Hahne M, et al., Inhibition of death receptor signals by cellular FLIP. Nature 1997; 388: 190-195.
36. Yang QH, Church-Hajduk R, Ren J, et al., Omi/HtrA2 catalytic cleavage of inhibitor of apoptosis (IAP) irreversibly inactivates IAPs and facilitates caspase activity in apoptosis. Genes Dev 2003; 17: 1487-1496.
37. Ying W,. NAD+/NADH and NADP+/NADPH in cellular functions and cell death: regulation and biological consequences. Antioxid Redox Signal 2008; 10: 179-206.
38. Circu ML, Maloney RE, Aw TY,. Disruption of pyridine nucleotide redox status during oxidative challenge at normal and low-glucose states: implications for cellular adenosine triphosphate, mitochondrial respiratory activity, and reducing capacity in colon epithelial cells. Antioxid Redox Signal 2011; 14: 2151-2162.
39. Garcia-Nogales P, Almeida A, Bolanos JP,. Peroxynitrite protects neurons against nitric oxide-mediated apoptosis. A key role for glucose-6-phosphate dehydrogenase activity in neuroprotection. J Biol Chem 2003; 278: 864-874.
40. Hamaoka R, Fujii J, Miyagawa J, et al., Overexpression of the aldose reductase gene induces apoptosis in pancreatic beta-cells by causing a redox imbalance. J Biochem 1999; 126: 41-47.
41. Ivarsson R, Quintens R, Dejonghe S, et al., Redox control of exocytosis: regulatory role of NADPH, thioredoxin, and glutaredoxin. Diabetes 2005; 54: 2132-2142.
42. Pias EK, Aw TY,. Apoptosis in mitotic competent undifferentiated cells is induced by cellular redox imbalance independent of reactive oxygen species production. FASEB J 2002; 16: 781-790.
43. Ren JG, Seth P, Everett P, et al., Induction of erythroid differentiation in human erythroleukemia cells by depletion of malic enzyme 2. PLoS One 2010; 5: e12520.
44. Warburg O, Posener K, Negelein E,. Ueber den stoffwechsel der tumoren. Biochem Z 1924; 152: 319-344.
45. Vander Heiden MG, Cantley LC, Thompson CB,. Understanding the Warburg effect: the metabolic requirements of cell proliferation. Science 2009; 324: 1029-1033.
46. DeBerardinis RJ, Cheng T,. Q's next: the diverse functions of glutamine in metabolism, cell biology and cancer. Oncogene 2010; 29: 313-324.
47. Wise DR, DeBerardinis RJ, Mancuso A, et al., Myc regulates a transcriptional program that stimulates mitochondrial glutaminolysis and leads to glutamine addiction. Proc Natl Acad Sci U S A 2008; 105: 18782-18787.
48. Brizel DM, Schroeder T, Scher RL, et al., Elevated tumor lactate concentrations predict for an increased risk of metastases in head-and-neck cancer. Int J Radiat Oncol Biol Phys 2001; 51: 349-353.
49. Schwickert G, Walenta S, Sundfor K, et al., Correlation of high lactate levels in human cervical cancer with incidence of metastasis. Cancer Res 1995; 55: 4757-4759.
50. Walenta S, Wetterling M, Lehrke M, et al., High lactate levels predict likelihood of metastases, tumor recurrence, and restricted patient survival in human cervical cancers. Cancer Res 2000; 60: 916-921.
51. Walenta S, Salameh A, Lyng H, et al., Correlation of high lactate levels in head and neck tumors with incidence of metastasis. Am J Pathol 1997; 150: 409-415.
52. Yokota H, Guo J, Matoba M, et al., Lactate, choline, and creatine levels measured by vitro 1H-MRS as prognostic parameters in patients with non-small-cell lung cancer. J Magn Reson Imaging 2007; 25: 992-999.
53. Paschen W, Djuricic B, Mies G, et al., Lactate and pH in the brain: association and dissociation in different pathophysiological states. J Neurochem 1987; 48: 154-159.
54. Fantin VR, St-Pierre J, Leder P,. Attenuation of LDH-A expression uncovers a link between glycolysis, mitochondrial physiology, and tumor maintenance. Cancer Cell 2006; 9: 425-434.
55. Christofk HR, Vander Heiden MG, Harris MH, et al., The M2 splice isoform of pyruvate kinase is important for cancer metabolism and tumour growth. Nature 2008; 452: 230-233.
56. 2+ signals. Curr Biol 2008; 18: 781-785.
57. Xu L, Fidler IJ,. Acidic pH-induced elevation in interleukin 8 expression by human ovarian carcinoma cells. Cancer Res 2000; 60: 4610-4616.
58. Fukumura D, Xu L, Chen Y, et al., Hypoxia and acidosis independently up-regulate vascular endothelial growth factor transcription in brain tumors in vivo. Cancer Res 2001; 61: 6020-6024.
59. Shi Q, Le X, Wang B, et al., Regulation of vascular endothelial growth factor expression by acidosis in human cancer cells. Oncogene 2001; 20: 3751-3756.
60. Mekhail K, Gunaratnam L, Bonicalzi ME, et al., HIF activation by pH-dependent nucleolar sequestration of VHL. Nature Cell Biol 2004; 6: 642-647.
61. Graham RM, Frazier DP, Thompson JW, et al., A unique pathway of cardiac myocyte death caused by hypoxia-acidosis. J Exp Biol 2004; 207: 3189-3200.
62. Silva AS, Yunes JA, Gillies RJ, et al., The potential role of systemic buffers in reducing intratumoral extracellular pH and acid-mediated invasion. Cancer Res 2009; 69: 2677-2684.
63. Robey IF, Baggett BK, Kirkpatrick ND, et al., Bicarbonate increases tumor pH and inhibits spontaneous metastases. Cancer Res 2009; 69: 2260-2268.