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Published in: Virchows Archiv 5/2009

01-05-2009 | Review and Perspective

Mitochondria and cancer

Authors: Valdemar Máximo, Jorge Lima, Paula Soares, Manuel Sobrinho-Simões

Published in: Virchows Archiv | Issue 5/2009

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Abstract

The authors review the role played by mutations in mitochondrial DNA and in nuclear genes encoding mitochondrial proteins in cancer development, with an emphasis on the alterations of the oxidative phosphorylation system and glycolysis.
Literature
2.
go back to reference Warburg O (1930) The metabolism of tumours. London Constable, London Warburg O (1930) The metabolism of tumours. London Constable, London
3.
go back to reference Warburg O, Wind F, Negelein E (1927) The metabolism of tumors in the body. J Gen Physiol 8:519–530CrossRefPubMed Warburg O, Wind F, Negelein E (1927) The metabolism of tumors in the body. J Gen Physiol 8:519–530CrossRefPubMed
4.
go back to reference Baysal BE, Ferrell RE, Willett-Brozick JE et al (2000) Mutations in SDHD, a mitochondrial complex II gene, in hereditary paraganglioma. Science 287:848–851PubMedCrossRef Baysal BE, Ferrell RE, Willett-Brozick JE et al (2000) Mutations in SDHD, a mitochondrial complex II gene, in hereditary paraganglioma. Science 287:848–851PubMedCrossRef
5.
go back to reference Astuti D, Latif F, Dallol A et al (2001) Gene mutations in the succinate dehydrogenase subunit SDHB cause susceptibility to familial pheochromocytoma and to familial paraganglioma. Am J Hum Genet 69:49–54PubMedCrossRef Astuti D, Latif F, Dallol A et al (2001) Gene mutations in the succinate dehydrogenase subunit SDHB cause susceptibility to familial pheochromocytoma and to familial paraganglioma. Am J Hum Genet 69:49–54PubMedCrossRef
6.
go back to reference Niemann S, Muller U (2000) Mutations in SDHC cause autosomal dominant paraganglioma, type 3. Nat Genet 26:268–270PubMedCrossRef Niemann S, Muller U (2000) Mutations in SDHC cause autosomal dominant paraganglioma, type 3. Nat Genet 26:268–270PubMedCrossRef
7.
go back to reference Horvath R, Abicht A, Holinski-Feder E et al (2006) Leigh syndrome caused by mutations in the flavoprotein (Fp) subunit of succinate dehydrogenase (SDHA). J Neurol Neurosurg Psychiatry 77:74–76PubMedCrossRef Horvath R, Abicht A, Holinski-Feder E et al (2006) Leigh syndrome caused by mutations in the flavoprotein (Fp) subunit of succinate dehydrogenase (SDHA). J Neurol Neurosurg Psychiatry 77:74–76PubMedCrossRef
9.
go back to reference Wallace DC (2005) A mitochondrial paradigm of metabolic and degenerative diseases, aging, and cancer: a dawn for evolutionary medicine. Annu Rev Genet 39:359–407PubMedCrossRef Wallace DC (2005) A mitochondrial paradigm of metabolic and degenerative diseases, aging, and cancer: a dawn for evolutionary medicine. Annu Rev Genet 39:359–407PubMedCrossRef
10.
go back to reference Rohren EM, Turkington TG, Coleman RE (2004) Clinical applications of PET in oncology. Radiology 231:305–332PubMedCrossRef Rohren EM, Turkington TG, Coleman RE (2004) Clinical applications of PET in oncology. Radiology 231:305–332PubMedCrossRef
11.
go back to reference Habano W, Sugai T, Nakamura SI et al (2000) Microsatellite instability and mutation of mitochondrial and nuclear DNA in gastric carcinoma. Gastroenterology 118:835–841PubMedCrossRef Habano W, Sugai T, Nakamura SI et al (2000) Microsatellite instability and mutation of mitochondrial and nuclear DNA in gastric carcinoma. Gastroenterology 118:835–841PubMedCrossRef
12.
go back to reference Richard SM, Bailliet G, Paez GL et al (2000) Nuclear and mitochondrial genome instability in human breast cancer. Cancer Res 60:4231–4237PubMed Richard SM, Bailliet G, Paez GL et al (2000) Nuclear and mitochondrial genome instability in human breast cancer. Cancer Res 60:4231–4237PubMed
13.
go back to reference Maximo V, Soares P, Seruca R et al (2001) Microsatellite instability, mitochondrial DNA large deletions, and mitochondrial DNA mutations in gastric carcinoma. Genes Chromosomes Cancer 32:136–143PubMedCrossRef Maximo V, Soares P, Seruca R et al (2001) Microsatellite instability, mitochondrial DNA large deletions, and mitochondrial DNA mutations in gastric carcinoma. Genes Chromosomes Cancer 32:136–143PubMedCrossRef
14.
go back to reference Burgart LJ, Zheng J, Shu Q et al (1995) Somatic mitochondrial mutation in gastric cancer. Am J Pathol 147:1105–1111PubMed Burgart LJ, Zheng J, Shu Q et al (1995) Somatic mitochondrial mutation in gastric cancer. Am J Pathol 147:1105–1111PubMed
15.
go back to reference Habano W, Sugai T, Yoshida T et al (1999) Mitochondrial gene mutation, but not large-scale deletion, is a feature of colorectal carcinomas with mitochondrial microsatellite instability. Int J Cancer 83:625–629PubMedCrossRef Habano W, Sugai T, Yoshida T et al (1999) Mitochondrial gene mutation, but not large-scale deletion, is a feature of colorectal carcinomas with mitochondrial microsatellite instability. Int J Cancer 83:625–629PubMedCrossRef
16.
go back to reference Polyak K, Li Y, Zhu H et al (1998) Somatic mutations of the mitochondrial genome in human colorectal tumours. Nat Genet 20:291–293PubMedCrossRef Polyak K, Li Y, Zhu H et al (1998) Somatic mutations of the mitochondrial genome in human colorectal tumours. Nat Genet 20:291–293PubMedCrossRef
17.
go back to reference Fliss MS, Usadel H, Caballero OL et al (2000) Facile detection of mitochondrial DNA mutations in tumors and bodily fluids. Science 287:2017–2019PubMedCrossRef Fliss MS, Usadel H, Caballero OL et al (2000) Facile detection of mitochondrial DNA mutations in tumors and bodily fluids. Science 287:2017–2019PubMedCrossRef
18.
go back to reference Yeh JJ, Lunetta KL, Van Orsouw NJ et al (2000) Somatic mitochondrial DNA (mtDNA) mutations in papillary thyroid carcinomas and differential mtDNA sequence variants in cases with thyroid tumours. Oncogene 19:2060–2066PubMedCrossRef Yeh JJ, Lunetta KL, Van Orsouw NJ et al (2000) Somatic mitochondrial DNA (mtDNA) mutations in papillary thyroid carcinomas and differential mtDNA sequence variants in cases with thyroid tumours. Oncogene 19:2060–2066PubMedCrossRef
19.
go back to reference Lewis PD, Baxter P, Paul GA et al (2000) Detection of damage to the mitochondrial genome in the oncocytic cells of Warthin's tumour. J Pathol 191:274–281PubMedCrossRef Lewis PD, Baxter P, Paul GA et al (2000) Detection of damage to the mitochondrial genome in the oncocytic cells of Warthin's tumour. J Pathol 191:274–281PubMedCrossRef
20.
go back to reference Tallini G, Ladanyi M, Rosai J et al (1994) Analysis of nuclear and mitochondrial DNA alterations in thyroid and renal oncocytic tumors. Cytogenet Cell Genet 66:253–259PubMedCrossRef Tallini G, Ladanyi M, Rosai J et al (1994) Analysis of nuclear and mitochondrial DNA alterations in thyroid and renal oncocytic tumors. Cytogenet Cell Genet 66:253–259PubMedCrossRef
21.
go back to reference Maximo V, Soares P, Lima J et al (2002) Mitochondrial DNA somatic mutations (point mutations and large deletions) and mitochondrial DNA variants in human thyroid pathology: a study with emphasis on Hurthle cell tumors. Am J Pathol 160:1857–1865PubMed Maximo V, Soares P, Lima J et al (2002) Mitochondrial DNA somatic mutations (point mutations and large deletions) and mitochondrial DNA variants in human thyroid pathology: a study with emphasis on Hurthle cell tumors. Am J Pathol 160:1857–1865PubMed
22.
go back to reference Abu-Amero KK, Alzahrani AS, Zou M et al (2005) High frequency of somatic mitochondrial DNA mutations in human thyroid carcinomas and complex I respiratory defect in thyroid cancer cell lines. Oncogene 24:1455–1460PubMedCrossRef Abu-Amero KK, Alzahrani AS, Zou M et al (2005) High frequency of somatic mitochondrial DNA mutations in human thyroid carcinomas and complex I respiratory defect in thyroid cancer cell lines. Oncogene 24:1455–1460PubMedCrossRef
23.
go back to reference 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 66:6087–6096PubMedCrossRef 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 66:6087–6096PubMedCrossRef
24.
go back to reference Lohrer HD, Hieber L, Zitzelsberger H (2002) Differential mutation frequency in mitochondrial DNA from thyroid tumours. Carcinogenesis 23:1577–1582PubMedCrossRef Lohrer HD, Hieber L, Zitzelsberger H (2002) Differential mutation frequency in mitochondrial DNA from thyroid tumours. Carcinogenesis 23:1577–1582PubMedCrossRef
25.
go back to reference Maximo V, Sobrinho-Simoes M (2000) Hurthle cell tumours of the thyroid. A review with emphasis on mitochondrial abnormalities with clinical relevance. Virchows Arch 437:107–115PubMedCrossRef Maximo V, Sobrinho-Simoes M (2000) Hurthle cell tumours of the thyroid. A review with emphasis on mitochondrial abnormalities with clinical relevance. Virchows Arch 437:107–115PubMedCrossRef
26.
go back to reference Maximo V, Lima J, Soares P et al (2005) Mitochondrial D-loop instability in thyroid tumours is not a marker of malignancy. Mitochondrion 5:333–340PubMedCrossRef Maximo V, Lima J, Soares P et al (2005) Mitochondrial D-loop instability in thyroid tumours is not a marker of malignancy. Mitochondrion 5:333–340PubMedCrossRef
27.
go back to reference Rogounovitch T, Saenko V, Yamashita S (2004) Mitochondrial DNA and human thyroid diseases. Endocr J 51:265–277PubMedCrossRef Rogounovitch T, Saenko V, Yamashita S (2004) Mitochondrial DNA and human thyroid diseases. Endocr J 51:265–277PubMedCrossRef
28.
go back to reference Savagner F, Franc B, Guyetant S et al (2001) Defective mitochondrial ATP synthesis in oxyphilic thyroid tumors. J Clin Endocrinol Metab 86:4920–4925PubMedCrossRef Savagner F, Franc B, Guyetant S et al (2001) Defective mitochondrial ATP synthesis in oxyphilic thyroid tumors. J Clin Endocrinol Metab 86:4920–4925PubMedCrossRef
29.
go back to reference Gasparre G, Porcelli AM, Bonora E et al (2007) Disruptive mitochondrial DNA mutations in complex I subunits are markers of oncocytic phenotype in thyroid tumors. Proc Natl Acad Sci U S A 104:9001–9006PubMedCrossRef Gasparre G, Porcelli AM, Bonora E et al (2007) Disruptive mitochondrial DNA mutations in complex I subunits are markers of oncocytic phenotype in thyroid tumors. Proc Natl Acad Sci U S A 104:9001–9006PubMedCrossRef
30.
go back to reference Gasparre G, Iommarini L, Porcelli AM et al (2008) An inherited mitochondrial DNA disruptive mutation shifts to homoplasmy in oncocytic tumor cells. Hum Mutat 30:391–396CrossRef Gasparre G, Iommarini L, Porcelli AM et al (2008) An inherited mitochondrial DNA disruptive mutation shifts to homoplasmy in oncocytic tumor cells. Hum Mutat 30:391–396CrossRef
31.
go back to reference Jeronimo C, Nomoto S, Caballero OL et al (2001) Mitochondrial mutations in early stage prostate cancer and bodily fluids. Oncogene 20:5195–5198PubMedCrossRef Jeronimo C, Nomoto S, Caballero OL et al (2001) Mitochondrial mutations in early stage prostate cancer and bodily fluids. Oncogene 20:5195–5198PubMedCrossRef
32.
go back to reference Zhou S, Kachhap S, Sun W et al (2007) Frequency and phenotypic implications of mitochondrial DNA mutations in human squamous cell cancers of the head and neck. Proc Natl Acad Sci U S A 104:7540–7545PubMedCrossRef Zhou S, Kachhap S, Sun W et al (2007) Frequency and phenotypic implications of mitochondrial DNA mutations in human squamous cell cancers of the head and neck. Proc Natl Acad Sci U S A 104:7540–7545PubMedCrossRef
33.
go back to reference Park JS, Sharma LK, Li HZ et al. (2009) A heteroplasmic, not homoplasmic, mitochondrial DNA mutation promotes tumorigenesis via alteration in reactive oxygen species generation and apoptosis. Hum Mol Genet (in press) Park JS, Sharma LK, Li HZ et al. (2009) A heteroplasmic, not homoplasmic, mitochondrial DNA mutation promotes tumorigenesis via alteration in reactive oxygen species generation and apoptosis. Hum Mol Genet (in press)
34.
go back to reference Lima J, Maximo V, Soares P et al (2009) Mitochondria and oncocytomas. In: Singh KK, Costello LC (eds) Mitochondria and cancer. Springer, New York, pp 193–209CrossRef Lima J, Maximo V, Soares P et al (2009) Mitochondria and oncocytomas. In: Singh KK, Costello LC (eds) Mitochondria and cancer. Springer, New York, pp 193–209CrossRef
35.
go back to reference Copeland WC, Wachsman JT, Johnson FM et al (2002) Mitochondrial DNA alterations in cancer. Cancer Invest 20:557–569PubMedCrossRef Copeland WC, Wachsman JT, Johnson FM et al (2002) Mitochondrial DNA alterations in cancer. Cancer Invest 20:557–569PubMedCrossRef
36.
go back to reference Czarnecka AM, Golik P, Bartnik E (2006) Mitochondrial DNA mutations in human neoplasia. J Appl Genet 47:67–78PubMed Czarnecka AM, Golik P, Bartnik E (2006) Mitochondrial DNA mutations in human neoplasia. J Appl Genet 47:67–78PubMed
37.
go back to reference Tamori A, Nishiguchi S, Nishikawa M et al (2004) Correlation between clinical characteristics and mitochondrial D-loop DNA mutations in hepatocellular carcinoma. J Gastroenterol 39:1063–1068PubMedCrossRef Tamori A, Nishiguchi S, Nishikawa M et al (2004) Correlation between clinical characteristics and mitochondrial D-loop DNA mutations in hepatocellular carcinoma. J Gastroenterol 39:1063–1068PubMedCrossRef
38.
go back to reference Petros JA, Baumann AK, Ruiz-Pesini E et al (2005) mtDNA mutations increase tumorigenicity in prostate cancer. Proc Natl Acad Sci U S A 102:719–724PubMedCrossRef Petros JA, Baumann AK, Ruiz-Pesini E et al (2005) mtDNA mutations increase tumorigenicity in prostate cancer. Proc Natl Acad Sci U S A 102:719–724PubMedCrossRef
39.
go back to reference Shidara Y, Yamagata K, Kanamori T et al (2005) Positive contribution of pathogenic mutations in the mitochondrial genome to the promotion of cancer by prevention from apoptosis. Cancer Res 65:1655–1663PubMedCrossRef Shidara Y, Yamagata K, Kanamori T et al (2005) Positive contribution of pathogenic mutations in the mitochondrial genome to the promotion of cancer by prevention from apoptosis. Cancer Res 65:1655–1663PubMedCrossRef
40.
go back to reference Pelicano H, Xu RH, Du M et al (2006) Mitochondrial respiration defects in cancer cells cause activation of Akt survival pathway through a redox-mediated mechanism. J Cell Biol 175:913–923PubMedCrossRef Pelicano H, Xu RH, Du M et al (2006) Mitochondrial respiration defects in cancer cells cause activation of Akt survival pathway through a redox-mediated mechanism. J Cell Biol 175:913–923PubMedCrossRef
41.
go back to reference Gottlieb E, Tomlinson IP (2005) Mitochondrial tumour suppressors: a genetic and biochemical update. Nat Rev Cancer 5:857–866PubMedCrossRef Gottlieb E, Tomlinson IP (2005) Mitochondrial tumour suppressors: a genetic and biochemical update. Nat Rev Cancer 5:857–866PubMedCrossRef
42.
go back to reference Lima J, Teixeira-Gomes J, Soares P et al (2003) Germline succinate dehydrogenase subunit D mutation segregating with familial non-RET C cell hyperplasia. J Clin Endocrinol Metab 88:4932–4937PubMedCrossRef Lima J, Teixeira-Gomes J, Soares P et al (2003) Germline succinate dehydrogenase subunit D mutation segregating with familial non-RET C cell hyperplasia. J Clin Endocrinol Metab 88:4932–4937PubMedCrossRef
43.
go back to reference Montani M, Schmitt AM, Schmid S et al (2005) No mutations but an increased frequency of SDHx polymorphisms in patients with sporadic and familial medullary thyroid carcinoma. Endocr Relat Cancer 12:1011–1016PubMedCrossRef Montani M, Schmitt AM, Schmid S et al (2005) No mutations but an increased frequency of SDHx polymorphisms in patients with sporadic and familial medullary thyroid carcinoma. Endocr Relat Cancer 12:1011–1016PubMedCrossRef
44.
go back to reference Cascon A, Cebrian A, Pollan M et al (2005) Succinate dehydrogenase D variants do not constitute a risk factor for developing C cell hyperplasia or sporadic medullary thyroid carcinoma. J Clin Endocrinol Metab 90:2127–2130PubMedCrossRef Cascon A, Cebrian A, Pollan M et al (2005) Succinate dehydrogenase D variants do not constitute a risk factor for developing C cell hyperplasia or sporadic medullary thyroid carcinoma. J Clin Endocrinol Metab 90:2127–2130PubMedCrossRef
45.
go back to reference Ricketts C, Woodward ER, Killick P et al (2008) Germline SDHB mutations and familial renal cell carcinoma. J Natl Cancer Inst 100:1260–1262PubMedCrossRef Ricketts C, Woodward ER, Killick P et al (2008) Germline SDHB mutations and familial renal cell carcinoma. J Natl Cancer Inst 100:1260–1262PubMedCrossRef
46.
go back to reference Tomlinson IP, Alam NA, Rowan AJ et al (2002) Germline mutations in FH predispose to dominantly inherited uterine fibroids, skin leiomyomata and papillary renal cell cancer. Nat Genet 30:406–410PubMedCrossRef Tomlinson IP, Alam NA, Rowan AJ et al (2002) Germline mutations in FH predispose to dominantly inherited uterine fibroids, skin leiomyomata and papillary renal cell cancer. Nat Genet 30:406–410PubMedCrossRef
47.
go back to reference Eng C, Kiuru M, Fernandez MJ et al (2003) A role for mitochondrial enzymes in inherited neoplasia and beyond. Nat Rev Cancer 3:193–202PubMedCrossRef Eng C, Kiuru M, Fernandez MJ et al (2003) A role for mitochondrial enzymes in inherited neoplasia and beyond. Nat Rev Cancer 3:193–202PubMedCrossRef
48.
go back to reference Pollard PJ, Briere JJ, Alam NA et al (2005) Accumulation of Krebs cycle intermediates and over-expression of HIF1alpha in tumours which result from germline FH and SDH mutations. Hum Mol Genet 14:2231–2239PubMedCrossRef Pollard PJ, Briere JJ, Alam NA et al (2005) Accumulation of Krebs cycle intermediates and over-expression of HIF1alpha in tumours which result from germline FH and SDH mutations. Hum Mol Genet 14:2231–2239PubMedCrossRef
49.
go back to reference Maximo V, Botelho T, Capela J et al (2005) Somatic and germline mutation in GRIM-19, a dual function gene involved in mitochondrial metabolism and cell death, is linked to mitochondrion-rich (Hurthle cell) tumours of the thyroid. Br J Cancer 92:1892–1898PubMedCrossRef Maximo V, Botelho T, Capela J et al (2005) Somatic and germline mutation in GRIM-19, a dual function gene involved in mitochondrial metabolism and cell death, is linked to mitochondrion-rich (Hurthle cell) tumours of the thyroid. Br J Cancer 92:1892–1898PubMedCrossRef
50.
go back to reference Huang G, Lu H, Hao A et al (2004) GRIM-19, a cell death regulatory protein, is essential for assembly and function of mitochondrial complex I. Mol Cell Biol 24:8447–8456PubMedCrossRef Huang G, Lu H, Hao A et al (2004) GRIM-19, a cell death regulatory protein, is essential for assembly and function of mitochondrial complex I. Mol Cell Biol 24:8447–8456PubMedCrossRef
51.
go back to reference Alchanati I, Nallar SC, Sun P et al (2006) A proteomic analysis reveals the loss of expression of the cell death regulatory gene GRIM-19 in human renal cell carcinomas. Oncogene 25:7138–7147PubMedCrossRef Alchanati I, Nallar SC, Sun P et al (2006) A proteomic analysis reveals the loss of expression of the cell death regulatory gene GRIM-19 in human renal cell carcinomas. Oncogene 25:7138–7147PubMedCrossRef
52.
53.
go back to reference Ramanathan A, Wang C, Schreiber SL (2005) Perturbational profiling of a cell-line model of tumorigenesis by using metabolic measurements. Proc Natl Acad Sci U S A 102:5992–5997PubMedCrossRef Ramanathan A, Wang C, Schreiber SL (2005) Perturbational profiling of a cell-line model of tumorigenesis by using metabolic measurements. Proc Natl Acad Sci U S A 102:5992–5997PubMedCrossRef
54.
go back to reference Matoba S, Kang JG, Patino WD et al (2006) p53 regulates mitochondrial respiration. Science 312:1650–1653PubMedCrossRef Matoba S, Kang JG, Patino WD et al (2006) p53 regulates mitochondrial respiration. Science 312:1650–1653PubMedCrossRef
55.
go back to reference Kaelin WG Jr, Ratcliffe PJ (2008) Oxygen sensing by metazoans: the central role of the HIF hydroxylase pathway. Mol Cell 30:393–402PubMedCrossRef Kaelin WG Jr, Ratcliffe PJ (2008) Oxygen sensing by metazoans: the central role of the HIF hydroxylase pathway. Mol Cell 30:393–402PubMedCrossRef
56.
go back to reference Gatenby RA, Gillies RJ (2004) Why do cancers have high aerobic glycolysis? Nat Rev Cancer 4:891–899PubMedCrossRef Gatenby RA, Gillies RJ (2004) Why do cancers have high aerobic glycolysis? Nat Rev Cancer 4:891–899PubMedCrossRef
57.
go back to reference Ishikawa K, Takenaga K, Akimoto M et al (2008) ROS-generating mitochondrial DNA mutations can regulate tumor cell metastasis. Science 320:661–664PubMedCrossRef Ishikawa K, Takenaga K, Akimoto M et al (2008) ROS-generating mitochondrial DNA mutations can regulate tumor cell metastasis. Science 320:661–664PubMedCrossRef
58.
go back to reference Piruat JI, Pintado CO, Ortega-Saenz P et al (2004) The mitochondrial SDHD gene is required for early embryogenesis, and its partial deficiency results in persistent carotid body glomus cell activation with full responsiveness to hypoxia. Mol Cell Biol 24:10933–10940PubMedCrossRef Piruat JI, Pintado CO, Ortega-Saenz P et al (2004) The mitochondrial SDHD gene is required for early embryogenesis, and its partial deficiency results in persistent carotid body glomus cell activation with full responsiveness to hypoxia. Mol Cell Biol 24:10933–10940PubMedCrossRef
59.
go back to reference Muller-Hocker J (1992) Random cytochrome-C-oxidase deficiency of oxyphil cell nodules in the parathyroid gland. A mitochondrial cytopathy related to cell ageing? Pathol Res Pract 188:701–706PubMed Muller-Hocker J (1992) Random cytochrome-C-oxidase deficiency of oxyphil cell nodules in the parathyroid gland. A mitochondrial cytopathy related to cell ageing? Pathol Res Pract 188:701–706PubMed
60.
go back to reference Rosai J, Carcangiu ML, DeLellis RA (1992) Tumours of the thyroid gland. Armed Force Institute of Pathology, Washington, DC Rosai J, Carcangiu ML, DeLellis RA (1992) Tumours of the thyroid gland. Armed Force Institute of Pathology, Washington, DC
61.
go back to reference Sobrinho-Simoes MA, Nesland JM, Holm R et al (1985) Hurthle cell and mitochondrion-rich papillary carcinomas of the thyroid gland: an ultrastructural and immunocytochemical study. Ultrastruct Pathol 8:131–142PubMedCrossRef Sobrinho-Simoes MA, Nesland JM, Holm R et al (1985) Hurthle cell and mitochondrion-rich papillary carcinomas of the thyroid gland: an ultrastructural and immunocytochemical study. Ultrastruct Pathol 8:131–142PubMedCrossRef
62.
go back to reference Nesland JM, Sobrinho-Simoes MA, Holm R et al (1985) Hurthle-cell lesions of the thyroid: a combined study using transmission electron microscopy, scanning electron microscopy, and immunocytochemistry. Ultrastruct Pathol 8:269–290PubMedCrossRef Nesland JM, Sobrinho-Simoes MA, Holm R et al (1985) Hurthle-cell lesions of the thyroid: a combined study using transmission electron microscopy, scanning electron microscopy, and immunocytochemistry. Ultrastruct Pathol 8:269–290PubMedCrossRef
63.
go back to reference Ebner D, Rodel G, Pavenstaedt I et al (1991) Functional and molecular analysis of mitochondria in thyroid oncocytoma. Virchows Arch B Cell Pathol Incl Mol Pathol 60:139–144PubMedCrossRef Ebner D, Rodel G, Pavenstaedt I et al (1991) Functional and molecular analysis of mitochondria in thyroid oncocytoma. Virchows Arch B Cell Pathol Incl Mol Pathol 60:139–144PubMedCrossRef
64.
go back to reference Muller-Hocker J, Jacob U, Seibel P (1998) Hashimoto thyroiditis is associated with defects of cytochrome-c oxidase in oxyphil Askanazy cells and with the common deletion (4, 977) of mitochondrial DNA. Ultrastruct Pathol 22:91–100PubMed Muller-Hocker J, Jacob U, Seibel P (1998) Hashimoto thyroiditis is associated with defects of cytochrome-c oxidase in oxyphil Askanazy cells and with the common deletion (4, 977) of mitochondrial DNA. Ultrastruct Pathol 22:91–100PubMed
65.
go back to reference Ortmann M, Vierbuchen M, Koller G et al (1988) Renal oncocytoma. I. Cytochrome c oxidase in normal and neoplastic renal tissue as detected by immunohistochemistry—a valuable aid to distinguish oncocytomas from renal cell carcinomas. Virchows Arch B Cell Pathol Incl Mol Pathol 56:165–173PubMedCrossRef Ortmann M, Vierbuchen M, Koller G et al (1988) Renal oncocytoma. I. Cytochrome c oxidase in normal and neoplastic renal tissue as detected by immunohistochemistry—a valuable aid to distinguish oncocytomas from renal cell carcinomas. Virchows Arch B Cell Pathol Incl Mol Pathol 56:165–173PubMedCrossRef
66.
go back to reference Muller-Hocker J (2000) Expression of bcl-2, Bax and Fas in oxyphil cells of Hashimoto thyroiditis. Virchows Arch 436:602–607PubMedCrossRef Muller-Hocker J (2000) Expression of bcl-2, Bax and Fas in oxyphil cells of Hashimoto thyroiditis. Virchows Arch 436:602–607PubMedCrossRef
67.
go back to reference Muller-Hocker J, Aust D, Napiwotzky J et al (1996) Defects of the respiratory chain in oxyphil and chief cells of the normal parathyroid and in hyperfunction. Hum Pathol 27:532–541PubMedCrossRef Muller-Hocker J, Aust D, Napiwotzky J et al (1996) Defects of the respiratory chain in oxyphil and chief cells of the normal parathyroid and in hyperfunction. Hum Pathol 27:532–541PubMedCrossRef
68.
go back to reference Cheung CC, Ezzat S, Ramyar L et al (2000) Molecular basis off Hurthle cell papillary thyroid carcinoma. J Clin Endocrinol Metab 85:878–882PubMedCrossRef Cheung CC, Ezzat S, Ramyar L et al (2000) Molecular basis off Hurthle cell papillary thyroid carcinoma. J Clin Endocrinol Metab 85:878–882PubMedCrossRef
69.
go back to reference Sobrinho-Simoes M, Maximo V, Castro IV et al (2005) Hurthle (oncocytic) cell tumors of thyroid: etiopathogenesis, diagnosis and clinical significance. Int J Surg Pathol 13:29–35PubMedCrossRef Sobrinho-Simoes M, Maximo V, Castro IV et al (2005) Hurthle (oncocytic) cell tumors of thyroid: etiopathogenesis, diagnosis and clinical significance. Int J Surg Pathol 13:29–35PubMedCrossRef
70.
go back to reference Langhans T (1907) Über die epithelialen Formen der malignen Struma. Virchows Arch 189:69–153CrossRef Langhans T (1907) Über die epithelialen Formen der malignen Struma. Virchows Arch 189:69–153CrossRef
71.
go back to reference DeLellis RA LR, Heitz PU, Eng C (eds) (2004) World Health Organization classification of tumours. Pathology and genetics of tumours of endocrine glands. IARC, Lyon DeLellis RA LR, Heitz PU, Eng C (eds) (2004) World Health Organization classification of tumours. Pathology and genetics of tumours of endocrine glands. IARC, Lyon
72.
go back to reference Dominguez-Malagon H, Delgado-Chavez R, Torres-Najera M et al (1989) Oxyphil and squamous variants of medullary thyroid carcinoma. Cancer 63:1183–1188PubMedCrossRef Dominguez-Malagon H, Delgado-Chavez R, Torres-Najera M et al (1989) Oxyphil and squamous variants of medullary thyroid carcinoma. Cancer 63:1183–1188PubMedCrossRef
73.
go back to reference Volante M, La Rosa S, Castellano I et al (2006) Clinico-pathological features of a series of 11 oncocytic endocrine tumours of the pancreas. Virchows Arch 448:545–551PubMedCrossRef Volante M, La Rosa S, Castellano I et al (2006) Clinico-pathological features of a series of 11 oncocytic endocrine tumours of the pancreas. Virchows Arch 448:545–551PubMedCrossRef
74.
go back to reference Moran CA, Suster S (2000) Primary neuroendocrine carcinoma (thymic carcinoid) of the thymus with prominent oncocytic features: a clinicopathologic study of 22 cases. Mod Pathol 13:489–494PubMedCrossRef Moran CA, Suster S (2000) Primary neuroendocrine carcinoma (thymic carcinoid) of the thymus with prominent oncocytic features: a clinicopathologic study of 22 cases. Mod Pathol 13:489–494PubMedCrossRef
75.
go back to reference Baloch ZW, LiVolsi VA (1999) Oncocytic lesions of the neuroendocrine system. Semin Diagn Pathol 16:190–199PubMed Baloch ZW, LiVolsi VA (1999) Oncocytic lesions of the neuroendocrine system. Semin Diagn Pathol 16:190–199PubMed
76.
77.
go back to reference Soares P, Trovisco V, Rocha AS et al (2003) BRAF mutations and RET/PTC rearrangements are alternative events in the etiopathogenesis of PTC. Oncogene 22:4578–4580PubMedCrossRef Soares P, Trovisco V, Rocha AS et al (2003) BRAF mutations and RET/PTC rearrangements are alternative events in the etiopathogenesis of PTC. Oncogene 22:4578–4580PubMedCrossRef
78.
go back to reference Castro P, Rebocho AP, Soares RJ et al (2006) PAX8-PPARgamma rearrangement is frequently detected in the follicular variant of papillary thyroid carcinoma. J Clin Endocrinol Metab 91:213–220PubMedCrossRef Castro P, Rebocho AP, Soares RJ et al (2006) PAX8-PPARgamma rearrangement is frequently detected in the follicular variant of papillary thyroid carcinoma. J Clin Endocrinol Metab 91:213–220PubMedCrossRef
79.
go back to reference Trovisco V, Vieira DCI, Soares P et al (2004) BRAF mutations are associated with some histological types of papillary thyroid carcinoma. J Pathol 202:247–251PubMedCrossRef Trovisco V, Vieira DCI, Soares P et al (2004) BRAF mutations are associated with some histological types of papillary thyroid carcinoma. J Pathol 202:247–251PubMedCrossRef
80.
go back to reference Trovisco V, Soares P, Preto A et al (2005) Type and prevalence of BRAF mutations are closely associated with papillary thyroid carcinoma histotype and patients' age but not with tumour aggressiveness. Virchows Arch 446:589–595PubMedCrossRef Trovisco V, Soares P, Preto A et al (2005) Type and prevalence of BRAF mutations are closely associated with papillary thyroid carcinoma histotype and patients' age but not with tumour aggressiveness. Virchows Arch 446:589–595PubMedCrossRef
81.
go back to reference Carcangiu ML, Bianchi S, Savino D et al (1991) Follicular Hurthle cell tumors of the thyroid gland. Cancer 68:1944–1953PubMedCrossRef Carcangiu ML, Bianchi S, Savino D et al (1991) Follicular Hurthle cell tumors of the thyroid gland. Cancer 68:1944–1953PubMedCrossRef
82.
go back to reference Evans HL, Vassilopoulou-Sellin R (1998) Follicular and Hurthle cell carcinomas of the thyroid: a comparative study. Am J Surg Pathol 22:1512–1520PubMedCrossRef Evans HL, Vassilopoulou-Sellin R (1998) Follicular and Hurthle cell carcinomas of the thyroid: a comparative study. Am J Surg Pathol 22:1512–1520PubMedCrossRef
83.
go back to reference McDonald MP, Sanders LE, Silverman ML et al (1996) Hurthle cell carcinoma of the thyroid gland: prognostic factors and results of surgical treatment. Surgery 120:1000–1004PubMedCrossRef McDonald MP, Sanders LE, Silverman ML et al (1996) Hurthle cell carcinoma of the thyroid gland: prognostic factors and results of surgical treatment. Surgery 120:1000–1004PubMedCrossRef
84.
go back to reference Papotti M, Botto Micca F, Favero A et al (1993) Poorly differentiated thyroid carcinomas with primordial cell component. A group of aggressive lesions sharing insular, trabecular, and solid patterns. Am J Surg Pathol 17:291–301PubMedCrossRef Papotti M, Botto Micca F, Favero A et al (1993) Poorly differentiated thyroid carcinomas with primordial cell component. A group of aggressive lesions sharing insular, trabecular, and solid patterns. Am J Surg Pathol 17:291–301PubMedCrossRef
85.
go back to reference Watson RG, Brennan MD, Goellner JR et al (1984) Invasive Hurthle cell carcinoma of the thyroid: natural history and management. Mayo Clin Proc 59:851–855PubMed Watson RG, Brennan MD, Goellner JR et al (1984) Invasive Hurthle cell carcinoma of the thyroid: natural history and management. Mayo Clin Proc 59:851–855PubMed
86.
go back to reference Lang W, Choritz H, Hundeshagen H (1986) Risk factors in follicular thyroid carcinomas. A retrospective follow-up study covering a 14-year period with emphasis on morphological findings. Am J Surg Pathol 10:246–255PubMedCrossRef Lang W, Choritz H, Hundeshagen H (1986) Risk factors in follicular thyroid carcinomas. A retrospective follow-up study covering a 14-year period with emphasis on morphological findings. Am J Surg Pathol 10:246–255PubMedCrossRef
87.
go back to reference Valenta LJ, Michel-Bechet M, Warshaw JB et al (1974) Human thyroid tumors composed of mitochondrion-rich cells: electron microscopic and biochemical findings. J Clin Endocrinol Metab 39:719–733PubMedCrossRef Valenta LJ, Michel-Bechet M, Warshaw JB et al (1974) Human thyroid tumors composed of mitochondrion-rich cells: electron microscopic and biochemical findings. J Clin Endocrinol Metab 39:719–733PubMedCrossRef
88.
go back to reference Apel RL, Asa SL (2002) The parathyroid glands. In: LiVolsi V, Asa SL (eds) Endocrine pathology. Churchill Livingstone, Philadelphia, pp 103–137 Apel RL, Asa SL (2002) The parathyroid glands. In: LiVolsi V, Asa SL (eds) Endocrine pathology. Churchill Livingstone, Philadelphia, pp 103–137
89.
go back to reference Giorgadze T, Stratton B, Baloch ZW et al (2004) Oncocytic parathyroid adenoma: problem in cytological diagnosis. Diagn Cytopathol 31:276–280PubMedCrossRef Giorgadze T, Stratton B, Baloch ZW et al (2004) Oncocytic parathyroid adenoma: problem in cytological diagnosis. Diagn Cytopathol 31:276–280PubMedCrossRef
90.
go back to reference Erickson LA, Jin L, Papotti M et al (2002) Oxyphil parathyroid carcinomas: a clinicopathologic and immunohistochemical study of 10 cases. Am J Surg Pathol 26:344–349PubMedCrossRef Erickson LA, Jin L, Papotti M et al (2002) Oxyphil parathyroid carcinomas: a clinicopathologic and immunohistochemical study of 10 cases. Am J Surg Pathol 26:344–349PubMedCrossRef
91.
go back to reference Yoo GH, Eisele DW, Askin FB et al (1994) Warthin's tumor: a 40-year experience at The Johns Hopkins Hospital. Laryngoscope 104:799–803PubMedCrossRef Yoo GH, Eisele DW, Askin FB et al (1994) Warthin's tumor: a 40-year experience at The Johns Hopkins Hospital. Laryngoscope 104:799–803PubMedCrossRef
92.
go back to reference Honda K, Kashima K, Daa T et al (2000) Clonal analysis of the epithelial component of Warthin's tumor. Hum Pathol 31:1377–1380PubMedCrossRef Honda K, Kashima K, Daa T et al (2000) Clonal analysis of the epithelial component of Warthin's tumor. Hum Pathol 31:1377–1380PubMedCrossRef
93.
go back to reference Kotwall CA (1992) Smoking as an etiologic factor in the development of Warthin's tumor of the parotid gland. Am J Surg 164:646–647PubMedCrossRef Kotwall CA (1992) Smoking as an etiologic factor in the development of Warthin's tumor of the parotid gland. Am J Surg 164:646–647PubMedCrossRef
94.
go back to reference Zambrano NR, Lubensky IA, Merino MJ et al (1999) Histopathology and molecular genetics of renal tumors toward unification of a classification system. J Urol 162:1246–1258PubMedCrossRef Zambrano NR, Lubensky IA, Merino MJ et al (1999) Histopathology and molecular genetics of renal tumors toward unification of a classification system. J Urol 162:1246–1258PubMedCrossRef
95.
go back to reference Kuroda N, Toi M, Hiroi M et al (2003) Review of renal oncocytoma with focus on clinical and pathobiological aspects. Histol Histopathol 18:935–942PubMed Kuroda N, Toi M, Hiroi M et al (2003) Review of renal oncocytoma with focus on clinical and pathobiological aspects. Histol Histopathol 18:935–942PubMed
96.
go back to reference Maximo V, Soares P, Rocha AS et al (1998) The common deletion of mitochondrial DNA is found in goiters and thyroid tumors with and without oxyphil cell change. Ultrastruct Pathol 22:271–273PubMedCrossRef Maximo V, Soares P, Rocha AS et al (1998) The common deletion of mitochondrial DNA is found in goiters and thyroid tumors with and without oxyphil cell change. Ultrastruct Pathol 22:271–273PubMedCrossRef
97.
go back to reference Maximo V, Sobrinho-Simoes M (2000) Mitochondrial DNA ‘common’ deletion in Hurthle cell lesions of the thyroid. J Pathol 192:561–562PubMedCrossRef Maximo V, Sobrinho-Simoes M (2000) Mitochondrial DNA ‘common’ deletion in Hurthle cell lesions of the thyroid. J Pathol 192:561–562PubMedCrossRef
98.
go back to reference Attardi G, Yoneda M, Chomyn A (1995) Complementation and segregation behavior of disease-causing mitochondrial DNA mutations in cellular model systems. Biochim Biophys Acta 1271:241–248PubMed Attardi G, Yoneda M, Chomyn A (1995) Complementation and segregation behavior of disease-causing mitochondrial DNA mutations in cellular model systems. Biochim Biophys Acta 1271:241–248PubMed
99.
go back to reference Heddi A, Faure-Vigny H, Wallace DC et al (1996) Coordinate expression of nuclear and mitochondrial genes involved in energy production in carcinoma and oncocytoma. Biochim Biophys Acta 1316:203–209PubMed Heddi A, Faure-Vigny H, Wallace DC et al (1996) Coordinate expression of nuclear and mitochondrial genes involved in energy production in carcinoma and oncocytoma. Biochim Biophys Acta 1316:203–209PubMed
100.
go back to reference Welter C, Kovacs G, Seitz G et al (1989) Alteration of mitochondrial DNA in human oncocytomas. Genes Chromosomes Cancer 1:79–82PubMedCrossRef Welter C, Kovacs G, Seitz G et al (1989) Alteration of mitochondrial DNA in human oncocytomas. Genes Chromosomes Cancer 1:79–82PubMedCrossRef
101.
go back to reference Brooks JD, Marshall FF, Isaacs WB et al (1999) Absence of HinfI restriction abnormalities in renal oncocytoma mitochondrial DNA. Mol Urol 3:1–3PubMed Brooks JD, Marshall FF, Isaacs WB et al (1999) Absence of HinfI restriction abnormalities in renal oncocytoma mitochondrial DNA. Mol Urol 3:1–3PubMed
102.
go back to reference Simonnet H, Alazard N, Pfeiffer K et al (2002) Low mitochondrial respiratory chain content correlates with tumor aggressiveness in renal cell carcinoma. Carcinogenesis 23:759–768PubMedCrossRef Simonnet H, Alazard N, Pfeiffer K et al (2002) Low mitochondrial respiratory chain content correlates with tumor aggressiveness in renal cell carcinoma. Carcinogenesis 23:759–768PubMedCrossRef
103.
go back to reference Simonnet H, Demont J, Pfeiffer K et al (2003) Mitochondrial complex I is deficient in renal oncocytomas. Carcinogenesis 24:1461–1466PubMedCrossRef Simonnet H, Demont J, Pfeiffer K et al (2003) Mitochondrial complex I is deficient in renal oncocytomas. Carcinogenesis 24:1461–1466PubMedCrossRef
104.
go back to reference Mayr JA, Meierhofer D, Zimmermann F et al (2008) Loss of complex I due to mitochondrial DNA mutations in renal oncocytoma. Clin Cancer Res 14:2270–2275PubMedCrossRef Mayr JA, Meierhofer D, Zimmermann F et al (2008) Loss of complex I due to mitochondrial DNA mutations in renal oncocytoma. Clin Cancer Res 14:2270–2275PubMedCrossRef
105.
go back to reference Savagner F, Chevrollier A, Loiseau D et al (2001) Mitochondrial activity in XTC.UC1 cells derived from thyroid oncocytoma. Thyroid 11:327–333PubMedCrossRef Savagner F, Chevrollier A, Loiseau D et al (2001) Mitochondrial activity in XTC.UC1 cells derived from thyroid oncocytoma. Thyroid 11:327–333PubMedCrossRef
106.
go back to reference Baris O, Savagner F, Nasser V et al (2004) Transcriptional profiling reveals coordinated up-regulation of oxidative metabolism genes in thyroid oncocytic tumors. J Clin Endocrinol Metab 89:994–1005PubMedCrossRef Baris O, Savagner F, Nasser V et al (2004) Transcriptional profiling reveals coordinated up-regulation of oxidative metabolism genes in thyroid oncocytic tumors. J Clin Endocrinol Metab 89:994–1005PubMedCrossRef
107.
go back to reference Jacques C, Baris O, Prunier-Mirebeau D et al (2005) Two-step differential expression analysis reveals a new set of genes involved in thyroid oncocytic tumors. J Clin Endocrinol Metab 90:2314–2320PubMedCrossRef Jacques C, Baris O, Prunier-Mirebeau D et al (2005) Two-step differential expression analysis reveals a new set of genes involved in thyroid oncocytic tumors. J Clin Endocrinol Metab 90:2314–2320PubMedCrossRef
108.
go back to reference Maximo V, Preto A, Crespo A et al (2004) Core I gene is overexpressed in Hurthle and non-Hurthle cell microfollicular adenomas and follicular carcinomas of the thyroid. BMC Cancer 4:12PubMedCrossRef Maximo V, Preto A, Crespo A et al (2004) Core I gene is overexpressed in Hurthle and non-Hurthle cell microfollicular adenomas and follicular carcinomas of the thyroid. BMC Cancer 4:12PubMedCrossRef
109.
go back to reference Sobrinho-Simoes M, Preto A, Rocha AS et al (2005) Molecular pathology of well-differentiated thyroid carcinomas. Virchows Arch 447:787–793PubMedCrossRef Sobrinho-Simoes M, Preto A, Rocha AS et al (2005) Molecular pathology of well-differentiated thyroid carcinomas. Virchows Arch 447:787–793PubMedCrossRef
110.
go back to reference Pedersen PL (2007) Warburg, me and Hexokinase 2: multiple discoveries of key molecular events underlying one of cancers' most common phenotypes, the “Warburg effect”, i.e., elevated glycolysis in the presence of oxygen. J Bioenerg Biomembr 39:211–222PubMedCrossRef Pedersen PL (2007) Warburg, me and Hexokinase 2: multiple discoveries of key molecular events underlying one of cancers' most common phenotypes, the “Warburg effect”, i.e., elevated glycolysis in the presence of oxygen. J Bioenerg Biomembr 39:211–222PubMedCrossRef
111.
go back to reference Ko YH, Pedersen PL, Geschwind JF (2001) Glucose catabolism in the rabbit VX2 tumor model for liver cancer: characterization and targeting hexokinase. Cancer Lett 173:83–91PubMedCrossRef Ko YH, Pedersen PL, Geschwind JF (2001) Glucose catabolism in the rabbit VX2 tumor model for liver cancer: characterization and targeting hexokinase. Cancer Lett 173:83–91PubMedCrossRef
112.
go back to reference Geschwind JF, Ko YH, Torbenson MS et al (2002) Novel therapy for liver cancer: direct intraarterial injection of a potent inhibitor of ATP production. Cancer Res 62:3909–3913PubMed Geschwind JF, Ko YH, Torbenson MS et al (2002) Novel therapy for liver cancer: direct intraarterial injection of a potent inhibitor of ATP production. Cancer Res 62:3909–3913PubMed
113.
go back to reference Bonnet S, Archer SL, Allalunis-Turner J et al (2007) A mitochondria-K+ channel axis is suppressed in cancer and its normalization promotes apoptosis and inhibits cancer growth. Cancer Cell 11:37–51PubMedCrossRef Bonnet S, Archer SL, Allalunis-Turner J et al (2007) A mitochondria-K+ channel axis is suppressed in cancer and its normalization promotes apoptosis and inhibits cancer growth. Cancer Cell 11:37–51PubMedCrossRef
114.
go back to reference Warburg O (1956) On respiratory impairment in cancer cells. Science 124:269–270PubMed Warburg O (1956) On respiratory impairment in cancer cells. Science 124:269–270PubMed
115.
go back to reference Pouyssegur J, Dayan F, Mazure NM (2006) Hypoxia signalling in cancer and approaches to enforce tumour regression. Nature 441:437–443PubMedCrossRef Pouyssegur J, Dayan F, Mazure NM (2006) Hypoxia signalling in cancer and approaches to enforce tumour regression. Nature 441:437–443PubMedCrossRef
116.
go back to reference Bristow RG, Hill RP (2008) Hypoxia and metabolism. Hypoxia, DNA repair and genetic instability. Nat Rev Cancer 8:180–192PubMedCrossRef Bristow RG, Hill RP (2008) Hypoxia and metabolism. Hypoxia, DNA repair and genetic instability. Nat Rev Cancer 8:180–192PubMedCrossRef
117.
go back to reference Higgins DF, Kimura K, Bernhardt WM et al (2007) Hypoxia promotes fibrogenesis in vivo via HIF-1 stimulation of epithelial-to-mesenchymal transition. J Clin Invest 117:3810–3820PubMed Higgins DF, Kimura K, Bernhardt WM et al (2007) Hypoxia promotes fibrogenesis in vivo via HIF-1 stimulation of epithelial-to-mesenchymal transition. J Clin Invest 117:3810–3820PubMed
118.
go back to reference Yang MH, Wu MZ, Chiou SH et al (2008) Direct regulation of TWIST by HIF-1alpha promotes metastasis. Nat Cell Biol 10:295–305PubMedCrossRef Yang MH, Wu MZ, Chiou SH et al (2008) Direct regulation of TWIST by HIF-1alpha promotes metastasis. Nat Cell Biol 10:295–305PubMedCrossRef
119.
120.
go back to reference Selak MA, Armour SM, MacKenzie ED et al (2005) Succinate links TCA cycle dysfunction to oncogenesis by inhibiting HIF-alpha prolyl hydroxylase. Cancer Cell 7:77–85PubMedCrossRef Selak MA, Armour SM, MacKenzie ED et al (2005) Succinate links TCA cycle dysfunction to oncogenesis by inhibiting HIF-alpha prolyl hydroxylase. Cancer Cell 7:77–85PubMedCrossRef
Metadata
Title
Mitochondria and cancer
Authors
Valdemar Máximo
Jorge Lima
Paula Soares
Manuel Sobrinho-Simões
Publication date
01-05-2009
Publisher
Springer-Verlag
Published in
Virchows Archiv / Issue 5/2009
Print ISSN: 0945-6317
Electronic ISSN: 1432-2307
DOI
https://doi.org/10.1007/s00428-009-0766-2

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