Deficiency of the complex i of the mitochondrial respiratory chain but improved adenylate control over succinate-dependent respiration are human gastric cancer-specific phenomena

Molecular and Cellular Biochemistry

Volumn 370, Issue 1-2, 2012, Pages 69-78

  Puurand, Marju ^a   Peet, Nadežda ^a   Piirsoo, Andres ^a   Peetsalu, Margot ^a   Soplepmann, Jaan ^a   Sirotkina, Meeli ^b   Peetsalu, Ants ^a   Hemminki, Akseli ^c   Seppet, Enn ^a  

^a UNIVERSITY OF TARTU   (Estonia)

^b TARTU UNIVERSITY HOSPITAL   (Estonia)

^c UNIVERSITY OF HELSINKI   (Finland)

Author keywords

Gastric cancer; Gastric cancer cell line; Gastric mucosa; Oxidative phosphorylation; Respiratory chain

Indexed keywords

ADENOSINE PHOSPHATE; SAPONIN; SUCCINIC ACID;

AGED; ARTICLE; CANCER CELL CULTURE; CANCER TISSUE; CELL MEMBRANE PERMEABILITY; CLINICAL ARTICLE; FEMALE; HISTOPATHOLOGY; HUMAN; HUMAN CELL; HUMAN CELL CULTURE; HUMAN TISSUE; MALE; MALIGNANT TRANSFORMATION; MITOCHONDRIAL RESPIRATION; MITOCHONDRIAL RESPIRATORY CHAIN COMPLEX I; OXIDATIVE PHOSPHORYLATION; STOMACH CANCER; STOMACH MUCOSA; TRANSMISSION ELECTRON MICROSCOPY;

ADENOSINE DIPHOSPHATE; AGED; CELL LINE, TUMOR; CELL RESPIRATION; ELECTRON TRANSPORT; ELECTRON TRANSPORT COMPLEX I; FEMALE; GASTRIC MUCOSA; HUMANS; MALE; MITOCHONDRIA; OXIDATIVE PHOSPHORYLATION; STOMACH NEOPLASMS; SUCCINIC ACID;

EID: 84867334412     PISSN: 03008177     EISSN: 15734919     Source Type: Journal    
DOI: 10.1007/s11010-012-1399-3     Document Type: Article

References (54)

1. Correa P (1992) Human gastric carcinogenesis: a multistep and multifactorial processFirst American Cancer Society Award Lecture on Cancer Epidemiology and Prevention. Cancer Res 52:6735-6740
2. Correa P (2004) The biological model of gastric carcinogenesis. IARC Scientific Publication, pp 301-310
3. Warburg O (1956) On the origin of cancer cells. Science 123:309-314
4. Weinhouse S (1956) On respiratory impairment in cancer cells. Science 124:267-269
5. Zu XL, Guppy M (2004) Cancer metabolism: facts, fantasy, and fiction. Biochem Biophys Res Commun 313:459-465
6. Moreno-Sánchez R, Rodríguez-Enríquez S, Saavedra E et al (2009) The bioenergetics of cancer: is glycolysis the main ATP supplier in all tumor cells? BioFactors 35:209-225. doi: 10.1002/biof.31
7. Rodríguez-Enríquez S, Torres-Márquez ME, Moreno-Sánchez R (2000) Substrate oxidation and ATP supply in AS-30D hepatoma cells. Arch Biochem Biophys 375:21-30. doi: 10.1006/abbi.1999.1582
8. Fogal V, Richardson AD, Karmali PP et al (2010) Mitochondrial p32 protein is a critical regulator of tumor metabolism via maintenance of oxidative phosphorylation. Mol Cell Biol 30:1303-1318. doi: 10.1128/MCB.01101-09
9. Gough DJ, Corlett A, Schlessinger K et al (2009) Mitochondrial STAT3 supports Ras-dependent oncogenic transformation. Science 324:1713-1716. doi: 10.1126/science.1171721
10. Moreno-Sánchez R, Rodríguez-Enríquez S, Marín-Hernández A, Saavedra E (2007) Energy metabolism in tumor cells. FEBS J 274:1393-1418. doi: 10.1111/j.1742-4658.2007.05686.x
11. Sonveaux P, Végran F, Schroeder T et al (2008) Targeting lactate-fueled respiration selectively kills hypoxic tumor cells in mice. J Clin Invest 118:3930-3942. doi: 10.1172/JCI36843
12. Tomitsuka E, Kita K, Esumi H (2010) The NADH-fumarate reductase system, a novel mitochondrial energy metabolism, is a new target for anticancer therapy in tumor microenvironments. Ann N Y Acad Sci 1201:44-49. doi: 10.1111/j.1749-6632.2010.05620.x
13. Morrish F, Isern N, Sadilek M et al (2009) c-Myc activates multiple metabolic networks to generate substrates for cell-cycle entry. Oncogene 28:2485-2491. doi: 10.1038/onc.2009.112
14. Gruno M, Peet N, Tein A et al (2008) Atrophic gastritis: deficient complex I of the respiratory chain in the mitochondria of corpus mucosal cells. J Gastroenterol 43:780-788. doi: 10.1007/s00535-008-2231-4
15. Gruno M, Peet N, Seppet E et al (2006) Oxidative phosphorylation and its coupling to mitochondrial creatine and adenylate kinases in human gastric mucosa. Am J Physiol Regul Integr Comp Physiol 291:R936-R946. doi: 10.1152/ajpregu.00162.2006
16. Dixon MF, Genta RM, Yardley JH, Correa P (1996) Classification and grading of gastritis. The updated Sydney System. International workshop on the histopathology of gastritis, Houston 1994. Am J Surg Pathol 20:1161-1181
17. Peetsalu A, Maaroos HI, Sipponen P, Peetsalu M (1991) Long-term effect of vagotomy on gastric mucosa and Helicobacter pylori in duodenal ulcer patients. Scand J Gastroenterol Suppl 186:77-83
18. World Medical Association (1997) Declaration of Helsinki. Recommendations guiding physicians in biomedical research involving human subjects. Cardiovasc Res 35:2-3
19. Motoyama T, Hojo H, Watanabe H (1986) Comparison of seven cell lines derived from human gastric carcinomas. Acta Pathol Jpn 36:65-83
20. Eimre M, Paju K, Pelloux S et al (2008) Distinct organization of energy metabolism in HL-1 cardiac cell line and cardiomyocytes. Biochim Biophys Acta 1777:514-524. doi: 10.1016/j.bbabio.2008.03.019
21. Lim HY, Ho QS, Low J et al (2011) Respiratory competent mitochondria in human ovarian and peritoneal cancer. Mitochondrion 11:437-443. doi: 10.1016/j.mito.2010.12.015
22. Hawkins BJ, Levin MD, Doonan PJ et al (2010) Mitochondrial complex II prevents hypoxic but not calcium- and proapoptotic Bcl-2 protein-induced mitochondrial membrane potential loss. J Biol Chem 285:26494-26505. doi: 10.1074/jbc.M110.143164
23. Gellerich FN, Deschauer M, Chen Y et al (2002) Mitochondrial respiratory rates and activities of respiratory chain complexes correlate linearly with heteroplasmy of deleted mtDNA without threshold and independently of deletion size. Biochim Biophys Acta 1556:41-52
24. Rustin P, Chretien D, Bourgeron T et al (1991) Assessment of the mitochondrial respiratory chain. Lancet 338:60
25. Vahsen N, Candé C, Brière J-J et al (2004) AIF deficiency compromises oxidative phosphorylation. EMBO J 23:4679-4689. doi: 10.1038/sj.emboj.7600461
26. Yin G-Y, Zhang W-N, Shen X-J et al (2003) Ultrastructure and molecular biological changes of chronic gastritis, gastric cancer and gastric precancerous lesions: a comparative study. World J Gastroenterol 9:851-857
27. Matoba S, Kang J-G, Patino WD et al (2006) p53 regulates mitochondrial respiration. Science 312:1650-1653. doi: 10.1126/science.1126863
28. Levine AJ, Feng Z, Mak TW et al (2006) Coordination and communication between the p53 and IGF-1-AKT-TOR signal transduction pathways. Genes Dev 20:267-275. doi: 10.1101/gad.1363206
29. Kondoh H, Lleonart ME, Gil J et al (2005) Glycolytic enzymes can modulate cellular life span. Cancer Res 65:177-185
30. Matsuhashi N, Saio M, Matsuo A et al (2004) Expression of p53 protein as a predictor of the response to 5-fluorouracil and cisplatin chemotherapy in human gastrointestinal cancer cell lines evaluated with apoptosis by use of thin layer collagen gel. Int J Oncol 24:807-813
31. Wang F, Liu J, Robbins D et al (2011) Mutant p53 exhibits trivial effects on mitochondrial functions which can be reactivated by ellipticine in lymphoma cells. Apoptosis 16:301-310. doi: 10.1007/s10495-010-0559-8
32. Atsumi T, Kato K, Uno K et al (2007) Pathophysiological role of the activation of p38 mitogen-activated protein kinases in poorly differentiated gastric cancer. Pathol Int 57:635-644. doi: 10.1111/j.1440-1827.2007.02152.x
33. Fan M, Rhee J, St-Pierre J et al (2004) Suppression of mitochondrial respiration through recruitment of p160 myb binding protein to PGC-1alpha: modulation by p38 MAPK. Genes Dev 18:278-289. doi: 10.1101/gad.1152204
34. Cuezva JM, Krajewska M, de Heredia ML et al (2002) The bioenergetic signature of cancer: a marker of tumor progression. Cancer Res 62:6674-6681
35. Cuezva JM, Ortega AD, Willers I et al (2009) The tumor suppressor function of mitochondria: translation into the clinics. Biochim Biophys Acta 1792:1145-1158. doi: 10.1016/j.bbadis.2009.01.006
36. Wang X, Moraes CT (2011) Increases in mitochondrial biogenesis impair carcinogenesis at multiple levels. Mol Oncol 5:399-409. doi: 10.1016/j.molonc.2011.07.008
37. Simonnet H, Demont J, Pfeiffer K et al (2003) Mitochondrial complex I is deficient in renal oncocytomas. Carcinogenesis 24:1461-1466. doi: 10.1093/carcin/bgg109
38. Bonora E, Porcelli AM, Gasparre G et al (2006) Defective oxidative phosphorylation in thyroid oncocytic carcinoma is associated with pathogenic mitochondrial DNA mutations affecting complexes I and III. Cancer Res 66:6087-6096. doi: 10.1158/0008-5472.CAN-06-0171
39. Boitier E, Merad-Boudia M, Guguen-Guillouzo C et al (1995) Impairment of the mitochondrial respiratory chain activity in diethylnitrosamine-induced rat hepatomas: possible involvement of oxygen free radicals. Cancer Res 55:3028-3035
40. Griffiths EA, Pritchard SA, Valentine HR et al (2007) Hypoxia-inducible factor-1alpha expression in the gastric carcinogenesis sequence and its prognostic role in gastric and gastro-oesophageal adenocarcinomas. Br J Cancer 96:95-103. doi: 10.1038/sj.bjc.6603524
41. Griffiths EA, Pritchard SA, McGrath SM et al (2008) Hypoxia-associated markers in gastric carcinogenesis and HIF-2alpha in gastric and gastro-oesophageal cancer prognosis. Br J Cancer 98:965-973. doi: 10.1038/sj.bjc.6604210
42. Ralph SJ, Rodríguez-Enríquez S, Neuzil J et al (2010) The causes of cancer revisited: mitochondrial malignancy and ROS-induced oncogenic transformationwhy mitochondria are targets for cancer therapy. Mol Aspects Med 31:145-170. doi: 10.1016/j.mam.2010.02.008
43. Barrientos A, Moraes CT (1999) Titrating the effects of mitochondrial complex I impairment in the cell physiology. J Biol Chem 274:16188-16197
44. Brandon M, Baldi P, Wallace DC (2006) Mitochondrial mutations in cancer. Oncogene 25:4647-4662. doi: 10.1038/sj.onc.1209607
45. Lemarie A, Grimm S (2011) Mitochondrial respiratory chain complexes: apoptosis sensors mutated in cancer? Oncogene 30:3985-4003. doi: 10.1038/onc.2011.167
46. Baracca A, Chiaradonna F, Sgarbi G et al (2010) Mitochondrial complex I decrease is responsible for bioenergetic dysfunction in K-ras transformed cells. Biochim Biophys Acta 1797:314-323. doi: 10.1016/j.bbabio.2009.11.006
47. Yamamoto F, Perucho M (1984) Activation of a human c-K-ras oncogene. Nucleic Acids Res 12:8873-8885
48. Hu Y, Lu W, Chen G et al (2012) K-ras(G12V) transformation leads to mitochondrial dysfunction and a metabolic switch from oxidative phosphorylation to glycolysis. Cell Res 22:399-412. doi: 10.1038/cr.2011.145
49. Weinberg F, Hamanaka R, Wheaton WW et al (2010) Mitochondrial metabolism and ROS generation are essential for Kras-mediated tumorigenicity. Proc Natl Acad Sci USA 107:8788-8793. doi: 10.1073/pnas.1003428107
50. Chiaradonna F, Sacco E, Manzoni R et al (2006) Ras-dependent carbon metabolism and transformation in mouse fibroblasts. Oncogene 25:5391-5404. doi: 10.1038/sj.onc.1209528
51. Mitsushita J, Lambeth JD, Kamata T (2004) The superoxide-generating oxidase Nox1 is functionally required for Ras oncogene transformation. Cancer Res 64:3580-3585. doi: 10.1158/0008-5472.CAN-03-3909
52. Komatsu D, Kato M, Nakayama J et al (2008) NADPH oxidase 1 plays a critical mediating role in oncogenic Ras-induced vascular endothelial growth factor expression. Oncogene 27:4724-4732. doi: 10.1038/onc.2008.102
53. Arrington DD, Van Vleet TR, Schnellmann RG (2006) Calpain 10: a mitochondrial calpain and its role in calcium-induced mitochondrial dysfunction. Am J Physiol Cell Physiol 291:C1159-C1171. doi: 10.1152/ajpcell.00207.2006
54. Ralph SJ, Rodríguez-Enríquez S, Neuzil J, Moreno-Sánchez R (2010) Bioenergetic pathways in tumor mitochondria as targets for cancer therapy and the importance of the ROS-induced apoptotic trigger. Mol Aspects Med 31:29-59. doi: 10.1016/j.mam.2009.12.006