Alterations of metabolic genes and metabolites in cancer

Seminars in Cell and Developmental Biology

Volumn 23, Issue 4, 2012, Pages 370-380

  Oermann, Eric K ^a,b   Wu, Jing ^a,b   Guan, Kun Liang ^c,d   Xiong, Yue ^a,b,c  

^a UNIVERSITY OF NORTH CAROLINA   (United States)

^b UNIVERSITY OF NORTH CAROLINA SCHOOL OF MEDICINE   (United States)

^c FUDAN UNIVERSITY   (China)

^d UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Cancer; Metabolism; Oncometabolite; Tumorigenesis; Warburg

Indexed keywords

2 OXOGLUTARIC ACID; B RAF KINASE; FUMARATE HYDRATASE; GLUCOSE TRANSPORTER 1; GLUTAMINASE; HYDROXYMETHYLGLUTARYL COENZYME A REDUCTASE KINASE; HYPOXIA INDUCIBLE FACTOR 1ALPHA; ISOCITRATE DEHYDROGENASE 1; ISOCITRATE DEHYDROGENASE 2; K RAS PROTEIN; LACTATE DEHYDROGENASE; MAMMALIAN TARGET OF RAPAMYCIN; MYC PROTEIN; PHOSPHOENOLPYRUVATE; PROTEIN KINASE B; PROTEIN P53; PYRUVATE KINASE; SUCCINATE DEHYDROGENASE;

3' UNTRANSLATED REGION; ACUTE GRANULOCYTIC LEUKEMIA; ACUTE LYMPHOBLASTIC LEUKEMIA; ANGIOIMMUNOBLASTIC T CELL LYMPHOMA; BILE DUCT CARCINOMA; CARCINOGENESIS; CARTILAGE TUMOR; CATALYSIS; CLINICAL FEATURE; COLORECTAL CARCINOMA; CYSTADENOMA; GASTROINTESTINAL STROMAL TUMOR; GENE MUTATION; GLIOMA; GLUCOSE TRANSPORT; HUMAN; KIDNEY CARCINOMA; LEIOMYOMA; LEYDIG CELL TUMOR; LUNG ADENOCARCINOMA; MELANOMA; MERKEL CELL TUMOR; METABOLIC REGULATION; METABOLISM; METABOLITE; NEOPLASM; ONCOGENE K RAS; PARAGANGLIOMA; PHENOTYPE; PHEOCHROMOCYTOMA; PROSTATE CANCER; PROTEIN PROCESSING; REVIEW; SERIAL ANALYSIS OF GENE EXPRESSION; SIGNAL TRANSDUCTION; T CELL LYMPHOMA; THYROID CARCINOMA; TUMOR GENE; UPREGULATION;

EID: 84862776612     PISSN: 10849521     EISSN: 10963634     Source Type: Journal    
DOI: 10.1016/j.semcdb.2012.01.013     Document Type: Review

References (102)

1. Warburg O. On respiratory impairment in cancer cells. Science 1956, 124:269-270.
2. Warburg O. On the origin of cancer cells. Science 1956, 123:309-314.
3. Hsu P.P., Sabatini D.M. Cancer cell metabolism: Warburg and beyond. Cell 2008, 134:703-707.
4. Vander Heiden M.G., Cantley L.C., Thompson C.B. Understanding the Warburg effect: the metabolic requirements of cell proliferation. Science 2009, 324:1029-1033.
5. DeBerardinis R.J., Lum J.J., Hatzivassiliou G., Thompson C.B. The biology of cancer: metabolic reprogramming fuels cell growth and proliferation. Cell Metabolism 2008, 7:11-20.
6. Manning B.D., Cantley L.C. AKT/PKB signaling: navigating downstream. Cell 2007, 129:1261-1274.
7. Zoncu R., Efeyan A., Sabatini D.M. mTOR: from growth signal integration to cancer, diabetes and ageing. Nature Reviews Molecular Cell Biology 2011, 12:21-35.
8. Flier J.S., Mueckler M.M., Usher P., Lodish H.F. Elevated levels of glucose transport and transporter messenger RNA are induced by ras or src oncogenes. Science 1987, 235:1492-1495.
9. Yun J., Rago C., Cheong I., Pagliarini R., Angenendt P., Rajagopalan H., et al. Glucose deprivation contributes to the development of KRAS pathway mutations in tumor cells. Science 2009, 325:1555-1559.
10. Chen C., Pore N., Behrooz A., Ismail-Beigi F., Maity A. Regulation of glut1 mRNA by hypoxia-inducible factor-1. Interaction between H-ras and hypoxia. The Journal of Biological Chemistry 2001, 276:9519-9525.
11. Airley R., Loncaster J., Davidson S., Bromley M., Roberts S., Patterson A., et al. Glucose transporter glut-1 expression correlates with tumor hypoxia and predicts metastasis-free survival in advanced carcinoma of the cervix. Clinical Cancer Research: An Official Journal of the American Association for Cancer Research 2001, 7:928-934.
12. Lewis B.C., Shim H., Li Q., Wu C.S., Lee L.A., Maity A., et al. Identification of putative c-Myc-responsive genes: characterization of rcl, a novel growth-related gene. Molecular and Cellular Biology 1997, 17:4967-4978.
13. Shim H., Dolde C., Lewis B.C., Wu C.S., Dang G., Jungmann R.A., et al. c-Myc transactivation of LDH-A: implications for tumor metabolism and growth. Proceedings of the National Academy of Sciences of the United States of America 1997, 94:6658-6663.
14. Semenza G.L., Jiang B.H., Leung S.W., Passantino R., Concordet J.P., Maire P., et al. Hypoxia response elements in the aldolase A, enolase 1, and lactate dehydrogenase A gene promoters contain essential binding sites for hypoxia-inducible factor 1. The Journal of Biological Chemistry 1996, 271:32529-32537.
15. Goldman R.D., Kaplan N.O., Hall T.C. Lactic dehydrogenase in human neoplastic tissues. Cancer Research 1964, 24:389-399.
16. Fantin V.R., 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.
17. Le A., Cooper C.R., Gouw A.M., Dinavahi R., Maitra A., Deck L.M., et al. Inhibition of lactate dehydrogenase A induces oxidative stress and inhibits tumor progression. Proceedings of the National Academy of Sciences of the United States of America 2010, 107:2037-2042.
18. Xie H., Valera V.A., Merino M.J., Amato A.M., Signoretti S., Linehan W.M., et al. LDH-A inhibition, a therapeutic strategy for treatment of hereditary leiomyomatosis and renal cell cancer. Molecular Cancer Therapeutics 2009, 8:626-635.
19. Aghili M., Zahedi F., Rafiee E. Hydroxyglutaric aciduria and malignant brain tumor: a case report and literature review. Journal of Neuro-Oncology 2009, 91:233-236.
20. Gao P., Tchernyshyov I., Chang T.C., Lee Y.S., Kita K., Ochi T., et al. c-Myc suppression of miR-23a/b enhances mitochondrial glutaminase expression and glutamine metabolism. Nature 2009, 458:762-765.
21. Wang J.B., Erickson J.W., Fuji R., Ramachandran S., Gao P., Dinavahi R., et al. Targeting mitochondrial glutaminase activity inhibits oncogenic transformation. Cancer Cell 2010, 18:207-219.
22. Vousden K.H., Prives C. Blinded by the light: the growing complexity of p53. Cell 2009, 137:413-431.
23. Mathupala S.P., Heese C., Pedersen P.L. Glucose catabolism in cancer cells. The type II hexokinase promoter contains functionally active response elements for the tumor suppressor p53. The Journal of Biological Chemistry 1997, 272:22776-22780.
24. Bensaad K., Tsuruta A., Selak M.A., Vidal M.N., Nakano K., Bartrons R., et al. TIGAR, a p53-inducible regulator of glycolysis and apoptosis. Cell 2006, 126:107-120.
25. Li H., Jogl G. Structural and biochemical studies of TIGAR (TP53-induced glycolysis and apoptosis regulator). The Journal of Biological Chemistry 2009, 284:1748-1754.
26. Suzuki S., Tanaka T., Poyurovsky M.V., Nagano H., Mayama T., Ohkubo S., et al. Phosphate-activated glutaminase (GLS2), a p53-inducible regulator of glutamine metabolism and reactive oxygen species. Proceedings of the National Academy of Sciences of the United States of America 2010, 107:7461-7466.
27. Lu W., Pelicano H., Huang P. Cancer metabolism: is glutamine sweeter than glucose. Cancer Cell 2010, 18:199-200.
28. Hu W., Zhang C., Wu R., Sun Y., Levine A., Feng Z. Glutaminase 2, a novel p53 target gene regulating energy metabolism and antioxidant function. Proceedings of the National Academy of Sciences of the United States of America 2010, 107:7455-7460.
29. Mazurek S. Pyruvate kinase type M2: a key regulator of the metabolic budget system in tumor cells. The International Journal of Biochemistry & Cell Biology 2010.
30. Noguchi T., Yamada K., Inoue H., Matsuda T., Tanaka T. The L-R-type isozymes of rat pyruvate kinase are produced from a single gene by use of different promoters. The Journal of Biological Chemistry 1987, 262:14366-14371.
31. Noguchi T., Inoue H., Tanaka T. The M1-M2-type isozymes of rat pyruvate kinase are produced from the same gene by alternative RNA splicing. The Journal of Biological Chemistry 1986, 261:13807-13812.
32. Yamada K., Noguchi T. Alteration of isozyme gene expression during cell differentiation and oncogenesis. Nippon Rinsho 1995, 53:1112-1118.
33. Mazurek S., Boschek C.B., Hugo F., Eigenbrodt E. Pyruvate kinase type M2 and its role in tumor growth and spreading. Seminars in Cancer Biology 2005, 15:300-308.
34. Wellen K.E., Thompson C.B. Cellular metabolic stress: considering how cells respond to nutrient excess. Molecular Cell 2010, 40:323-332.
35. Luo W., Hu H., Chang R., Zhong J., Knabel M., O'Meally R., et al. Pyruvate kinase M2 is a PHD3-stimulated coactivator for hypoxia-inducible factor 1. Cell 2011, 145:732-744.
36. Yang W., Xia Y., Ji H., Zheng Y., Liang J., Huang W., et al. Nuclear PKM2 regulates beta-catenin transactivation upon EGFR activation. Nature 2011.
37. David C.J., Chen M., Assanah M., Canoll P., Manley J.L. HnRNP proteins controlled by c-Myc deregulate pyruvate kinase mRNA splicing in cancer. Nature 2010, 463:364-368.
38. Integrated genomic analyses of ovarian carcinoma. Nature 2011, 474:609-615.
39. Baysal B.E., Ferrell R.E., Willett-Brozick J.E., Lawrence E.C., Myssiorek D., Bosch A., et al. Mutations in SDHD, a mitochondrial complex II gene, in hereditary paraganglioma. Science 2000, 287:848-851.
40. Niemann S., Muller U. Mutations in SDHC cause autosomal dominant paraganglioma, type 3. Nature Genetics 2000, 26:268-270.
41. Astuti D., Douglas F., Lennard T.W., Aligianis I.A., Woodward E.R., Evans D.G., et al. Germline SDHD mutation in familial phaeochromocytoma. Lancet 2001, 357:1181-1182.
42. Hao H.X., Khalimonchuk O., Schraders M., Dephoure N., Bayley J.P., Kunst H., et al. SDH5, a gene required for flavination of succinate dehydrogenase, is mutated in paraganglioma. Science 2009, 325:1139-1142.
43. Bayley J.P., Devilee P., Taschner P.E. The SDH mutation database: an online resource for succinate dehydrogenase sequence variants involved in pheochromocytoma, paraganglioma and mitochondrial complex II deficiency. BMC Medical Genetics 2005, 6:39.
44. Burnichon N., Briere J.J., Libe R., Vescovo L., Riviere J., Tissier F., et al. SDHA is a tumor suppressor gene causing paraganglioma. Human Molecular Genetics 2010, 19:3011-3020.
45. Pantaleo M.A., Astolfi A., Indio V., Moore R., Thiessen N., Heinrich M.C., et al. SDHA loss-of-function mutations in KIT-PDGFRA wild-type gastrointestinal stromal tumors identified by massively parallel sequencing. Journal of the National Cancer Institute 2011, 103:983-987.
46. Korpershoek E., Favier J., Gaal J., Burnichon N., van Gessel B., Oudijk L., et al. SDHA immunohistochemistry detects germline SDHA gene mutations in apparently sporadic paragangliomas and pheochromocytomas. The Journal of Clinical Endocrinology and Metabolism 2011, 96:E1472-E1476.
47. Bardella C., Pollard P.J., Tomlinson I. SDH mutations in cancer. Biochimica et Biophysica Acta 2011, 1807:1432-1443.
48. Weaver T.M., Levitt D.G., Donnelly M.I., Stevens P.P., Banaszak L.J. The multisubunit active site of fumarase C from Escherichia coli. Nature Structural Biology 1995, 2:654-662.
49. Tomlinson I.P., Alam N.A., Rowan A.J., Barclay E., Jaeger E.E., Kelsell D., et al. Germline mutations in FH predispose to dominantly inherited uterine fibroids, skin leiomyomata and papillary renal cell cancer. Nature Genetics 2002, 30:406-410.
50. Bayley J.P., Launonen V., Tomlinson I.P. The FH mutation database: an online database of fumarate hydratase mutations involved in the MCUL (HLRCC) tumor syndrome and congenital fumarase deficiency. BMC Medical Genetics 2008, 9:20.
51. Alam N.A., Olpin S., Rowan A., Kelsell D., Leigh I.M., Tomlinson I.P., et al. Missense mutations in fumarate hydratase in multiple cutaneous and uterine leiomyomatosis and renal cell cancer. Journal of Molecular Diagnostics 2005, 7:437-443.
52. Parsons D.W., Jones S., Zhang X., Lin J.C., Leary R.J., Angenendt P., et al. An integrated genomic analysis of human glioblastoma multiforme. Science 2008, 321:1807-1812.
53. Dang L., Jin S., Su S.M. IDH mutations in glioma and acute myeloid leukemia. Trends in Molecular Medicine 2010, 16:387-397.
54. Mardis E.R., Ding L., Dooling D.J., Larson D.E., McLellan M.D., Chen K., et al. Recurring mutations found by sequencing an acute myeloid leukemia genome. New England Journal of Medicine 2009, 361:1058-1066.
55. Hemerly J.P., Bastos A.U., Cerutti J.M. Identification of several novel non-p.R132 IDH1 variants in thyroid carcinomas. European Journal of Endocrinology 2010, 163:747-755.
56. Murugan A.K., Bojdani E., Xing M. Identification and functional characterization of isocitrate dehydrogenase 1 (IDH1) mutations in thyroid cancer. Biochemical and Biophysical Research Communications 2010, 393:555-559.
57. Amary M.F., Bacsi K., Maggiani F., Damato S., Halai D., Berisha F., et al. IDH1 and IDH2 mutations are frequent events in central chondrosarcoma and central and periosteal chondromas but not in other mesenchymal tumours. The Journal of Pathology 2011, 224:334-343.
58. Amary M.F., Damato S., Halai D., Eskandarpour M., Berisha F., Bonar F., et al. Ollier disease and Maffucci syndrome are caused by somatic mosaic mutations of IDH1 and IDH2. Nature Genetics 2011.
59. Pansuriya T.C., van Eijk R., d'Adamo P., van Ruler M.A., Kuijjer M.L., Oosting J., et al. Somatic mosaic IDH1 and IDH2 mutations are associated with enchondroma and spindle cell hemangioma in Ollier disease and Maffucci syndrome. Nature Genetics 2011.
60. Shibata T., Kokubu A., Miyamoto M., Sasajima Y., Yamazaki N. Mutant IDH1 confers an in vivo growth in a melanoma cell line with BRAF mutation. The American Journal of Pathology 2011, 178:1395-1402.
61. Gaal J., Burnichon N., Korpershoek E., Roncelin I., Bertherat J., Plouin P.F., et al. Isocitrate dehydrogenase mutations are rare in pheochromocytomas and paragangliomas. Journal of Clinical Endocrinology and Metabolism 2010, 95:1274-1278.
62. Kang M.R., Kim M.S., Oh J.E., Kim Y.R., Song S.Y., Seo S.I., et al. Mutational analysis of IDH1 codon 132 in glioblastomas and other common cancers. International Journal of Cancer 2009, 125:353-355.
63. Cairns R.A., Iqbal J., Lemonnier F., Kucuk C., de Leval L., Jais J.P., et al. IDH2 mutations are frequent in angioimmunoblastic T-cell lymphoma. Blood 2012.
64. Borger D.R., Tanabe K.K., Fan K.C., Lopez H.U., Fantin V.R., Straley K.S., et al. Frequent mutation of Isocitrate Dehydrogenase (IDH)1 and IDH2 in cholangiocarcinoma identified through broad-based tumor genotyping. The Oncologist 2011.
65. Eng C., Kiuru M., Fernandez M.J., Aaltonen L.A. A role for mitochondrial enzymes in inherited neoplasia and beyond. Nature Reviews Cancer 2003, 3:193-202.
66. Gottlieb E., Tomlinson I.P. Mitochondrial tumour suppressors: a genetic and biochemical update. Nature Reviews Cancer 2005, 5:857-866.
67. Hausinger R.P. FeII/alpha-ketoglutarate-dependent hydroxylases and related enzymes. Critical Reviews in Biochemistry and Molecular Biology 2004, 39:21-68.
68. Loenarz C., Schofield C.J. Expanding chemical biology of 2-oxoglutarate oxygenases. Nature Chemical Biology 2008, 4:152-156.
69. Iyer L.M., Tahiliani M., Rao A., Aravind L. Prediction of novel families of enzymes involved in oxidative and other complex modifications of bases in nucleic acids. Cell Cycle 2009, 8:1698-1710.
70. Pollard P.J., Briere J.J., Alam N.A., Barwell J., Barclay E., Wortham N.C., et al. Accumulation of Krebs cycle intermediates and over-expression of HIF1alpha in tumours which result from germline FH and SDH mutations. Human Molecular Genetics 2005, 14:2231-2239.
71. Selak M.A., Armour S.M., MacKenzie E.D., Boulahbel H., Watson D.G., Mansfield K.D., et al. Succinate links TCA cycle dysfunction to oncogenesis by inhibiting HIF-alpha prolyl hydroxylase. Cancer Cell 2005, 7:77-85.
72. Isaacs J.S., Jung Y.J., Mole D.R., Lee S., Torres-Cabala C., Chung Y.L., et al. HIF overexpression correlates with biallelic loss of fumarate hydratase in renal cancer: novel role of fumarate in regulation of HIF stability. Cancer Cell 2005, 8:143-153.
73. Winkler B.S., DeSantis N., Solomon F. Multiple NADPH-producing pathways control glutathione (GSH) content in retina. Experimental Eye Research 1986, 43:829-847.
74. Zhao S., Lin Y., Xu W., Jiang W., Zha Z., Wang P., et al. Glioma-derived mutations in IDH1 dominantly inhibit IDH1 catalytic activity and induce HIF-1alpha. Science 2009, 324:261-265.
75. Yan H., Parsons D.W., Jin G., McLendon R., Rasheed B.A., Yuan W., et al. IDH1 and IDH2 mutations in gliomas. New England Journal of Medicine 2009, 360:765-773.
76. Dang L., White D.W., Gross S., Bennett B.D., Bittinger M.A., Driggers E.M., et al. Cancer-associated IDH1 mutations produce 2-hydroxyglutarate. Nature 2009, 462:739-744.
77. Pope W.B., Prins R.M., Albert Thomas M., Nagarajan R., Yen K.E., Bittinger M.A., et al. Non-invasive detection of 2-hydroxyglutarate and other metabolites in IDH1 mutant glioma patients using magnetic resonance spectroscopy. Journal of Neuro-Oncology 2011.
78. Ward P.S., Patel J., Wise D.R., Abdel-Wahab O., Bennett B.D., Coller H.A., et al. The common feature of leukemia-associated IDH1 and IDH2 mutations is a neomorphic enzyme activity converting alpha-ketoglutarate to 2-hydroxyglutarate. Cancer Cell 2010, 17:225-234.
79. Gross S., Cairns R.A., Minden M.D., Driggers E.M., Bittinger M.A., Jang H.G., et al. Cancer-associated metabolite 2-hydroxyglutarate accumulates in acute myelogenous leukemia with isocitrate dehydrogenase 1 and 2 mutations. Journal of Experimental Medicine 2010, 207:339-344.
80. Andersson A.K., Miller D.W., Lynch J.A., Lemoff A.S., Cai Z., Pounds S.B., et al. IDH1 and IDH2 mutations in pediatric acute leukemia. Leukemia 2011, 25:1570-1577.
81. Figueroa M.E., Abdel-Wahab O., Lu C., Ward P.S., Patel J., Shih A., et al. Leukemic IDH1 and IDH2 mutations result in a hypermethylation phenotype, disrupt TET2 function, and impair hematopoietic differentiation. Cancer Cell 2010, 18:553-567.
82. Xu W., Yang H., Liu Y., Yang Y., Wang P., Kim S.H., et al. Oncometabolite 2-hydroxyglutarate is a competitive inhibitor of alpha-ketoglutarate-dependent dioxygenases. Cancer Cell 2011, 19:17-30.
83. Ward P.S., Cross J.R., Lu C., Weigert O., Abel-Wahab O., Levine R.L., et al. Identification of additional IDH mutations associated with oncometabolite R(-)-2-hydroxyglutarate production. Oncogene 2011.
84. Rzem R., Veiga-da-Cunha M., Noel G., Goffette S., Nassogne M.C., Tabarki B., et al. A gene encoding a putative FAD-dependent L-2-hydroxyglutarate dehydrogenase is mutated in L-2-hydroxyglutaric aciduria. Proceedings of the National Academy of Sciences of the United States of America 2004, 101:16849-16854.
85. Topcu M., Jobard F., Halliez S., Coskun T., Yalcinkayal C., Gerceker F.O., et al. L-2-Hydroxyglutaric aciduria: identification of a mutant gene C14orf160, localized on chromosome 14q22.1. Human Molecular Genetics 2004, 13:2803-2811.
86. Chowdhury R., Yeoh K.K., Tian Y.M., Hillringhaus L., Bagg E.A., Rose N.R., et al. The oncometabolite 2-hydroxyglutarate inhibits histone lysine demethylases. EMBO Reports 2011, 12:463-469.
87. Rose N.R., McDonough M.A., King O.N., Kawamura A., Schofield C.J. Inhibition of 2-oxoglutarate dependent oxygenases. Chemical Society Reviews 2011, 40:4364-4397.
88. Tahiliani M., Koh K.P., Shen Y., Pastor W.A., Bandukwala H., Brudno Y., et al. Conversion of 5-methylcytosine to 5-hydroxymethylcytosine in mammalian DNA by MLL partner TET1. Science 2009, 324:930-935.
89. Ito S., D'Alessio A.C., Taranova O.V., Hong K., Sowers L.C., Zhang Y. Role of Tet proteins in 5mC to 5hmC conversion, ES-cell self-renewal and inner cell mass specification. Nature 2010, 466:1129-1133.
90. He Y.F., Li B.Z., Li Z., Liu P., Wang Y., Tang Q., et al. Tet-mediated formation of 5-carboxylcytosine and its excision by TDG in mammalian DNA. Science 2011, 333:1303-1307.
91. Ito S., Shen L., Dai Q., Wu S.C., Collins L.B., Swenberg J.A., et al. Tet proteins can convert 5-methylcytosine to 5-formylcytosine and 5-carboxylcytosine. Science 2011, 333:1300-1303.
92. Verhaak R.G., Hoadley K.A., Purdom E., Wang V., Qi Y., Wilkerson M.D., et al. Integrated genomic analysis identifies clinically relevant subtypes of glioblastoma characterized by abnormalities in PDGFRA, IDH1, EGFR, and NF1. Cancer Cell 2010, 17:98-110.
93. Noushmehr H., Weisenberger D.J., Diefes K., Phillips H.S., Pujara K., Berman B.P., et al. Identification of a CpG island methylator phenotype that defines a distinct subgroup of glioma. Cancer Cell 2010, 17:510-522.
94. Delhommeau F., Dupont S., Della Valle V., James C., Trannoy S., Masse A., et al. Mutation in TET2 in myeloid cancers. The New England Journal of Medicine 2009, 360:2289-2301.
95. Langemeijer S.M., Kuiper R.P., Berends M., Knops R., Aslanyan M.G., Massop M., et al. Acquired mutations in TET2 are common in myelodysplastic syndromes. Nature Genetics 2009, 41:838-842.
96. Christensen B.C., Smith A.A., Zheng S., Koestler D.C., Houseman E.A., Marsit C.J., et al. DNA methylation, isocitrate dehydrogenase mutation, and survival in glioma. Journal of the National Cancer Institute 2011, 103:143-153.
97. Smith E.H., Janknecht R., Maher L.J. Succinate inhibition of alpha-ketoglutarate-dependent enzymes in a yeast model of paraganglioma. Human Molecular Genetics 2007, 16:3136-3148.
98. Adam J., Hatipoglu E., O'Flaherty L., Ternette N., Sahgal N., Lockstone H., et al. Renal cyst formation in Fh1-deficient mice is independent of the Hif/Phd pathway: roles for fumarate in KEAP1 succination and Nrf2 signaling. Cancer Cell 2011, 20:524-537.
99. Bardella C., El-Bahrawy M., Frizzell N., Adam J., Ternette N., Hatipoglu E., et al. Aberrant succination of proteins in fumarate hydratase-deficient mice and HLRCC patients is a robust biomarker of mutation status. Journal of Pathology 2011, 225:4-11.
100. Alderson N.L., Wang Y., Blatnik M., Frizzell N., Walla M.D., Lyons T.J., et al. S-(2-Succinyl)cysteine: a novel chemical modification of tissue proteins by a Krebs cycle intermediate. Archives of Biochemistry and Biophysics 2006, 450:1-8.
101. Ooi A., Wong J.C., Petillo D., Roossien D., Perrier-Trudova V., Whitten D., et al. An antioxidant response phenotype shared between hereditary and sporadic type 2 papillary renal cell carcinoma. Cancer Cell 2011, 20:511-523.
102. Jia G., Fu Y., Zhao X., Dai Q., Zheng G., Yang Y., et al. N6-Methyladenosine in nuclear RNA is a major substrate of the obesity-associated FTO. Nature Chemical Biology 2011, 7:885-887.