Metabolic alteration in tumorigenesis

Science China Life Sciences

Volumn 56, Issue 12, 2013, Pages 1067-1075

  Yang, Hui ^a   Xiong, Yue ^a,b   Guan, KunLiang ^a,c  

^a FUDAN UNIVERSITY   (China)

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

^c UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

epigenetic; metabolite; tumorigenesis

Indexed keywords

2 HYDROXYGLUTARIC ACID; 2 OXOGLUTARIC ACID; ALPHA-HYDROXYGLUTARATE; ALPHA-KETOGLUTARIC ACID; FUMARATE HYDRATASE; GLUTARIC ACID DERIVATIVE; ISOCITRATE DEHYDROGENASE; SUCCINATE DEHYDROGENASE;

CARCINOGENESIS; CELL PROLIFERATION; GENETIC EPIGENESIS; GENETICS; HUMAN; METABOLISM; MUTATION; NEOPLASM; PATHOLOGY; REVIEW;

CARCINOGENESIS; CELL PROLIFERATION; EPIGENESIS, GENETIC; FUMARATE HYDRATASE; GLUTARATES; HUMANS; ISOCITRATE DEHYDROGENASE; KETOGLUTARIC ACIDS; METABOLIC NETWORKS AND PATHWAYS; MUTATION; NEOPLASMS; SUCCINATE DEHYDROGENASE;

EID: 84889661553     PISSN: 16747305     EISSN: None     Source Type: Journal    
DOI: 10.1007/s11427-013-4549-2     Document Type: Review

References (86)

1. Warburg O. On the origin of cancer cells. Science, 1956, 123: 309-314.
2. Warburg O. Über den stoffwechsel der carcinomzelle. J Mol Med, 1925, 4: 534-536.
3. Avril N, Dose J, Jänicke F, et al. Metabolic characterization of breast tumors with positron emission tomography using f-18 fluorodeoxyglucose. J Clin Oncol, 1996, 14: 1848-1857.
4. 18fluoro-deoxy-d-glucose positron emission tomography is a reliable predictor for viable tumor in postchemotherapy seminoma: An update of the prospective multicentric sempet trial. J Clin Oncol, 2004, 22: 1034-1039.
5. Oermann E K, Wu J, Guan K L, et al. Alterations of metabolic genes and metabolites in cancer. Semin Cell Dev Biol, 2012, 23: 370-380.
6. Hsu P P, Sabatini D M. Cancer cell metabolism: Warburg and beyond. Cell, 2008, 134: 703-707.
7. Vander Heiden M G, Cantley L C, Thompson C B. Understanding the warburg effect: The metabolic requirements of cell proliferation. Sci Signal, 2009, 324: 1029.
8. Wise D R, Thompson C B. Glutamine addiction: A new therapeutic target in cancer. Trends Biochem Sci, 2010, 35: 427-433.
9. Daye D, Wellen K E. Metabolic reprogramming in cancer: Unraveling the role of glutamine in tumorigenesis. Semin Cell Dev Biol, 2012, 23: 362-369.
10. Le A, Lane A N, Hamaker M, et al. Glucose-independent glutamine metabolism via TCA cycling for proliferation and survival in B cells. Cell Metab, 2012, 15: 110-121.
11. Metallo C M, Gameiro P A, Bell E L, et al. Reductive glutamine metabolism by IDH1 mediates lipogenesis under hypoxia. Nature, 2011, 481: 380-384.
12. Mullen A R, Wheaton W W, Jin E S, et al. Reductive carboxylation supports growth in tumour cells with defective mitochondria. Nature, 2011, 481: 385-388.
13. Wise D R, Ward P S, Shay J E, et al. Hypoxia promotes isocitrate dehydrogenase-dependent carboxylation of α-ketoglutarate to citrate to support cell growth and viability. Proc Natl Acad Sci USA, 2011, 108: 19611-19616.
14. Fuchs B C, Bode B P. Amino acid transporters ASCT2 and LAT1 in cancer: Partners in crime? Semin Cancer Biol, 2005, 15: 254-266.
15. Fuchs B C, Finger R E, Onan M C, et al. ASCT2 silencing regulates mammalian target-of-rapamycin growth and survival signaling in human hepatoma cells. Am J Physiol Cell Physiol, 2007, 293: C55-C63.
16. Hu W, Zhang C, Wu R, et al. Glutaminase 2, a novel p53 target gene regulating energy metabolism and antioxidant function. Sci Signal, 2010, 107: 7455.
17. Suzuki S, Tanaka T, Poyurovsky M V, et al. Phosphate-activated glutaminase (GLS2), a p53-inducible regulator of glutamine metabolism and reactive oxygen species. Sci Signal, 2010, 107: 7461.
18. Hao H X, Khalimonchuk O, Schraders M, et al. SDH5, a gene required for flavination of succinate dehydrogenase, is mutated in paraganglioma. Science, 2009, 325: 1139-1142.
19. Baysal B E, Ferrell R E, Willett-Brozick J E, et al. Mutations in SDHD, a mitochondrial complex II gene, in hereditary paraganglioma. Science, 2000, 287: 848-851.
20. Gimm O, Armanios M, Dziema H, et al. Somatic and occult germline mutations in SDHD, a mitochondrial complex II gene, in nonfamilial pheochromocytoma. Cancer Res, 2000, 60: 6822-6825.
21. McWhinney S R, Pasini B, Stratakis C A. Familial gastrointestinal stromal tumors and germ-line mutations. N Engl J Med, 2007, 357: 1054-1056.
22. Ricketts C, Woodward E R, Killick P, et al. Germline SDHB mutations and familial renal cell carcinoma. J Nat Cancer Inst, 2008, 100: 1260-1262.
23. Bardella C, Pollard P J, Tomlinson I. SDH mutations in cancer. Biochim Biophys Acta Bioenerg, 2011, 1807: 1432-1443.
24. Timmers H J, Kozupa A, Eisenhofer G, et al. Clinical presentations, biochemical phenotypes, and genotype-phenotype correlations in patients with succinate dehydrogenase subunit B-associated pheochromocytomas and paragangliomas. J Clin Endocrinol Metab, 2007, 92: 779-786.
25. Gimenez-Roqueplo A P, Favier J, Rustin P, et al. Mutations in the SDHB gene are associated with extra-adrenal and/or malignant phaeochromocytomas. Cancer Res, 2003, 63: 5615-5621.
26. Amar L, Baudin E, Burnichon N, et al. Succinate dehydrogenase B gene mutations predict survival in patients with malignant pheochromocytomas or paragangliomas. J Clin Endocrinol Metab, 2007, 92: 3822-3828.
27. Pollard P, Briere J, Alam N, et al. Accumulation of Krebs cycle intermediates and over-expression of hif1α in tumours which result from germline FH and SDH mutations. Hum Mol Genet, 2005, 14: 2231-2239.
28. Xiao M, Yang H, Xu W, et al. Inhibition of α-kg-dependent histone and DNA demethylases by fumarate and succinate that are accumulated in mutations of FH and SDH tumor suppressors. Genes Dev, 2012, 26: 1326-1338.
29. Tomlinson I P, Alam N A, Rowan A J, et al. Germline mutations in FH predispose to dominantly inherited uterine fibroids, skin leiomyomata and papillary renal cell cancer. Nat Genet, 2002, 30: 406-410.
30. Campione E, Terrinoni A, Orlandi A, et al. Cerebral cavernomas in a family with multiple cutaneous and uterine leiomyomas associated with a new mutation in the fumarate hydratase gene. J Invest Dermatol, 2007, 127: 2271-2273.
31. Carvajal-Carmona L G, Alam N A, Pollard P J, et al. Adult leydig cell tumors of the testis caused by germline fumarate hydratase mutations. J Clin Endocrinol Metab, 2006, 91: 3071-3075.
32. Ylisaukko-oja S K, Cybulski C, Lehtonen R, et al. Germline fumarate hydratase mutations in patients with ovarian mucinous cystadenoma. Eur J Hum Genet, 2006, 14: 880-883.
33. Yang H, Ye D, Guan K L, et al. IDH1 and IDH2 mutations in tumorigenesis: Mechanistic insights and clinical perspectives. Clin Cancer Res, 2012, 18: 5562-5571.
34. Parsons D W, Jones S, Zhang X, et al. An integrated genomic analysis of human glioblastoma multiforme. Science, 2008, 321: 1807-1812.
35. Mardis E R, Ding L, Dooling D J, et al. Recurring mutations found by sequencing an acute myeloid leukemia genome. N Engl J Med, 2009, 361: 1058-1066.
36. Balss J, Meyer J, Mueller W, et al. Analysis of the IDH1 codon 132 mutation in brain tumors. Acta Neuropathol, 2008, 116: 597-602.
37. Bleeker F E, Lamba S, Leenstra S, et al. IDH1 mutations at residue p. R132 (idh1r132) occur frequently in high-grade gliomas but not in other solid tumors. Hum Mutat, 2009, 30: 7-11.
38. Hartmann C, Meyer J, Balss J, et al. Type and frequency of IDH1 and IDH2 mutations are related to astrocytic and oligodendroglial differentiation and age: A study of 1010 diffuse gliomas. Acta Neuropathol, 2009, 118: 469-474.
39. Watanabe T, Nobusawa S, Kleihues P, et al. IDH1 mutations are early events in the development of astrocytomas and oligodendrogliomas. Am J Pathol, 2009, 174: 1149-1153.
40. Yan H, Parsons D W, Jin G, et al. IDH1 and IDH2 mutations in gliomas. N Engl J Med, 2009, 360: 765-773.
41. Chou W C, Hou H A, Chen C Y, et al. Distinct clinical and biologic characteristics in adult acute myeloid leukemia bearing the isocitrate dehydrogenase 1 mutation. Blood, 2010, 115: 2749-2754.
42. Dang L, Jin S, Su S M. IDH mutations in glioma and acute myeloid leukemia. Trends Mol Med, 2010, 16: 387-397.
43. Gravendeel L A M, Kloosterhof N K, Bralten L B C, et al. Segregation of non-p. R132h mutations in IDH1 in distinct molecular subtypes of glioma. Hum Mutat, 2010, 31: E1186-E1199.
44. Gross S, Cairns R A, Minden M D, et al. Cancer-associated metabolite 2-hydroxyglutarate accumulates in acute myelogenous leukemia with isocitrate dehydrogenase 1 and 2 mutations. J Exp Med, 2010, 207: 339-344.
45. Ho P A, Alonzo T A, Kopecky K J, et al. Molecular alterations of the IDH1 gene in AML: A children's oncology group and southwest oncology group study. Leukemia, 2010, 24: 909-913.
46. Tefferi A, Lasho T L, Abdel-Wahab O, et al. IDH1 and IDH2 mutation studies in 1473 patients with chronic-, fibrotic- or blast-phase essential thrombocythemia, polycythemia vera or myelofibrosis. Leukemia, 2010, 24: 1302-1309.
47. Wagner K, Damm F, Gohring G, et al. Impact of IDH1 R132 mutations and an IDH1 single nucleotide polymorphism in cytogenetically normal acute myeloid leukemia: SNP rs11554137 is an adverse prognostic factor. J Clin Oncol, 2010, 28: 2356-2364.
48. Ward P S, Patel J, Wise D R, et al. The common feature of leukemia-associated IDH1 and IDH2 mutations is a neomorphic enzyme activity converting α-ketoglutarate to 2-hydroxyglutarate. Cancer Cell, 2010, 17: 225-234.
49. Amary M F, Bacsi K, Maggiani F, et al. IDH1 and IDH2 mutations are frequent events in central chondrosarcoma and central and periosteal chondromas but not in other mesenchymal tumours. J Pathol, 2011, 224: 334-343.
50. Amary M F, Damato S, Halai D, et al. Ollier disease and maffucci syndrome are caused by somatic mosaic mutations of IDH1 and IDH2. Nat Genet, 2011, 43: 1262-1265.
51. Pansuriya T C, van Eijk R, d'Adamo P, et al. Somatic mosaic IDH1 and IDH2 mutations are associated with enchondroma and spindle cell hemangioma in ollier disease and maffucci syndrome. Nat Genet, 2011, 43: 1256-1261.
52. Borger D R, Tanabe K K, Fan K C, et al. Frequent mutation of isocitrate dehydrogenase (IDH)1 and IDH2 in cholangiocarcinoma identified through broad-based tumor genotyping. Oncologist, 2011, 17: 72-79.
53. Wang P, Dong Q, Zhang C, et al. Mutations in isocitrate dehydrogenase 1 and 2 occur frequently in intrahepatic cholangiocarcinomas and share hypermethylation targets with glioblastomas. Oncogene, 2013, 32: 3091-3100.
54. Hemerly J P, Bastos A U, Cerutti J M. Identification of several novel non-p. R132 IDH1 variants in thyroid carcinomas. Eur J Endocrinol, 2010, 163: 747-755.
55. Murugan A K, Bojdani E, Xing M. Identification and functional characterization of isocitrate dehydrogenase 1 (IDH1) mutations in thyroid cancer. Biochem Biophys Res Commun, 2010, 393: 555-559.
56. Kang M R, Kim M S, Oh J E, et al. Mutational analysis of IDH1 codon 132 in glioblastomas and other common cancers. Int J Cancer, 2009, 125: 353-355.
57. Gaal J, Burnichon N, Korpershoek E, et al. Isocitrate dehydrogenase mutations are rare in pheochromocytomas and paragangliomas. J Clin Endocrinol Metab, 2010, 95: 1274-1278.
58. Pusch S S F, Meyer J, Mittelbronn M, et al. Glioma IDH1 mutation patterns off the beaten track. Neuropathol Appl Neurobiol, 2011, 37: 428-430.
59. Zhao S, Lin Y, Xu W, et al. Glioma-derived mutations in IDH1 dominantly inhibit IDH1 catalytic activity and induce HIF-1α. Science's STKE, 2009, 324: 261.
60. Dang L, White D W, Gross S, et al. Cancer-associated IDH1 mutations produce 2-hydroxyglutarate. Nature, 2009, 462: 739-744.
61. Figueroa M E, Abdel-Wahab O, Lu C, 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.
62. Ward P, Cross J, Lu C, et al. Identification of additional IDH mutations associated with oncometabolite R(-)-2-hydroxyglutarate production. Oncogene, 2012, 31: 2491-2498.
63. Xu W, Yang H, Liu Y, et al. Oncometabolite 2-hydroxyglutarate is a competitive inhibitor of α-ketoglutarate-dependent dioxygenases. Cancer Cell, 2011, 19: 17-30.
64. Jalbert L, Elkhaled A, Phillips J, et al. Presence of 2-hydroxyglutarate in IDH1 mutated low-grade glioma using ex vivo proton hr-mas spectroscopy. Proc Intl Soc Mag Reson Med, 2011, 19: 183.
65. Kalinina J C A, Wang L, Yu Q, et al. Detection of "oncometabolite" 2-hydroxyglutarate by magnetic resonance analysis as a biomarker of IDH1/2 mutations in glioma. J Mol Med (Berl), 2012, 90: 1161-1171.
66. Hutton Jr J J, Kaplan A, Udenfriend S. Conversion of the amino acid sequence gly-pro-pro in protein to gly-pro-hyp by collagen proline hydroxylase. Arch Biochem Biophys, 1967, 121: 384-391.
67. Rose N R, McDonough M A, King O N F, et al. Inhibition of 2-oxoglutarate dependent oxygenases. Chem Soc Rev, 2011, 40: 4364.
68. Pollard P, Loenarz C, Mole D, et al. Regulation of Jumonji-domain-containing histone demethylases by hypoxia-inducible factor (HIF)-1alpha. Biochem J, 2008, 416: 387-394.
69. Hausinger R P. FeII/alpha-ketoglutarate-dependent hydroxylases and related enzymes. Crit Rev Biochem Mol Biol, 2004, 39: 21-68.
70. Loenarz C, Schofield C J. Expanding chemical biology of 2-oxoglutarate oxygenases. Nat Chem Biol, 2008, 4: 152-156.
71. Tuderman L, Myllylä R, Kivirikko K I. Mechanism of the prolyl hydroxylase reaction. Eur J Biochem, 1977, 80: 341-348.
72. Letouzé E, Martinelli C, Loriot C, et al. SDH mutations establish a hypermethylator phenotype in paraganglioma. Cancer Cell, 2013, 23: 739-752.
73. Killian J K, Kim S Y, Miettinen M, et al. Succinate dehydrogenase mutation underlies global epigenomic divergence in gastrointestinal stromal tumor. Cancer Discovery, 2013, 3: 648-657.
74. Mason E F, Hornick J L. Succinate dehydrogenase deficiency is associated with decreased 5-hydroxymethylcytosine production in gastrointestinal stromal tumors: Implications for mechanisms of tumorigenesis. Modern Pathol, 2013, doi: 10. 1038/modpathol. 2013. 86.
75. Chowdhury R, Yeoh K K, Tian Y M, et al. The oncometabolite 2-hydroxyglutarate inhibits histone lysine demethylases. EMBO Rep, 2011, 12: 463-469.
76. Lu C, Ward P S, Kapoor G S, et al. IDH mutation impairs histone demethylation and results in a block to cell differentiation. Nature, 2012, 483: 474-478.
77. Duncan C G, Barwick B G, Jin G, et al. A heterozygous IDH1R132H/WT mutation induces genome-wide alterations in DNA methylation. Genome Res, 2012, 22: 2339-2355.
78. Sasaki M, Knobbe C B, Munger J C, et al. IDH1 (R132H) mutation increases murine haematopoietic progenitors and alters epigenetics. Nature, 2012, 488: 656-659.
79. Kriaucionis S, Heintz N. The nuclear DNA base 5-hydroxyme-thylcytosine is present in purkinje neurons and the brain. Science, 2009, 324: 929-930.
80. Tahiliani M, Koh K P, Shen Y, et al. Conversion of 5-methylcytosine to 5-hydroxymethylcytosine in mammalian DNA by mll partner TET1. Science, 2009, 324: 930-935.
81. Ito S, D'Alessio A C, Taranova O V, et al. Role of Tet proteins in 5mC to 5hmC conversion, ES-cell self-renewal and inner cell mass specification. Nature, 2010, 466: 1129-1133.
82. He Y F, Li B Z, Li Z, et al. Tet-mediated formation of 5-carbo-xylcytosine and its excision by TDG in mammalian DNA. Science, 2011, 333: 1303-1307.
83. Ito S, Shen L, Dai Q, et al. Tet proteins can convert 5-methylcytosine to 5-formylcytosine and 5-carboxylcytosine. Science, 2011, 333: 1300-1303.
84. Noushmehr H, Weisenberger D J, Diefes K, et al. Identification of a CPG island methylator phenotype that defines a distinct subgroup of glioma. Cancer Cell, 2010, 17: 510-522.
85. Turcan S, Rohle D, Goenka A, et al. IDH1 mutation is sufficient to establish the glioma hypermethylator phenotype. Nature, 2012, 483: 479-483.
86. Hewitson K S, Liénard B M, McDonough M A, et al. Structural and mechanistic studies on the inhibition of the hypoxia-inducible transcription factor hydroxylases by tricarboxylic acid cycle intermediates. J Biol Chem, 2007, 282: 3293-3301.