Metabolic dysregulation in monogenic disorders and cancer-finding method in madness

Nature Reviews Cancer

Volumn 15, Issue 7, 2015, Pages 440-448

  Erez, Ayelet ^a   Deberardinis, Ralph J ^b  

^a WEIZMANN INSTITUTE OF SCIENCE   (Israel)

^b UNIVERSITY OF TEXAS   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

2 HYDROXYGLUTARIC ACID; FUMARATE HYDRATASE; FUMARIC ACID; FUMARYLACETOACETASE; GLYCERALDEHYDE 3 PHOSPHATE DEHYDROGENASE; HEXOKINASE; HYPOXIA INDUCIBLE FACTOR; ISOCITRATE DEHYDROGENASE; PORPHOBILINOGEN DEAMINASE; SUCCINATE DEHYDROGENASE; SUCCINIC ACID; UROPORPHYRINOGEN DECARBOXYLASE; IDH1 PROTEIN, HUMAN; ISOCITRATE DEHYDROGENASE 2, HUMAN; PHOSPHOGLYCERATE DEHYDROGENASE;

ACUTE MYELOBLASTIC LEUKEMIA; ALPHA 1 ANTITRYPSIN DEFICIENCY; CANCER DIAGNOSIS; FABRY DISEASE; FAMILIAL CANCER; GAUCHER DISEASE; GENE EXPRESSION; GENE MUTATION; GLYCOGEN STORAGE DISEASE TYPE 1; GLYCOLYSIS; HEMOCHROMATOSIS; HUMAN; LIVER CELL CARCINOMA; METABOLIC DISORDER; MITOCHONDRIAL DNA DEPLETION SYNDROME; MONOGENIC DISORDER; NEOPLASM; PORPHYRIA CUTANEA TARDA; PRIORITY JOURNAL; RARE DISEASE; REVIEW; TYROSINEMIA; WILSON DISEASE; ANIMAL; COMPLICATION; INBORN ERROR OF METABOLISM; METABOLISM; NEOPLASMS; PHYSIOLOGY;

ANIMALS; GLYCOLYSIS; HUMANS; ISOCITRATE DEHYDROGENASE; METABOLISM, INBORN ERRORS; NEOPLASMS; PHOSPHOGLYCERATE DEHYDROGENASE;

EID: 84933279481     PISSN: 1474175X     EISSN: 14741768     Source Type: Journal    
DOI: 10.1038/nrc3949     Document Type: Review

References (122)

1. Warburg O. On the origin of cancer cells. Science 123, 309-314 (1956
2. De Berardinis R. J., Sayed N., Ditsworth D. & Thompson C. B. Brick by brick: metabolism and tumor cell growth. Curr. Opin. Genet. Dev. 18, 54-61 (2008
3. Boroughs L. K. & DeBerardinis R. J. Metabolic pathways promoting cancer cell survival and growth. Nat. Cell Biol. 17, 351-359 (2015
4. Hanahan D. & Weinberg R. A. Hallmarks of cancer: the next generation. Cell 144, 646-674 (2011
5. Garrod A. The Croonian lectures on inborn errors of metabolism, lecture II: alkaptonuria. Lancet 2, 73-79 (1908
6. Garrod A. E. The incidence of alkaptonuria: a study in chemical individuality. 1902. Mol. Med. 2, 274-282 (1996
7. Beadle G. W. & Tatum E. L. Genetic control of biochemical reactions in Neurospora. Proc. Natl Acad. Sci. USA 27, 499-506 (1941
8. Hamosh A., et al. Online Mendelian Inheritance in Man (OMIM), a knowledgebase of human genes and genetic disorders. Nucleic Acids Res. 30, 52-55 (2002
9. Pampols T. Inherited metabolic rare disease. Adv. Exp. Med. Biol. 686, 397-431 (2010
10. Dipple K. M. & McCabe E. R. Phenotypes of patients with simple Mendelian disorders are complex traits: thresholds, modifiers, and systems dynamics. Am. J. Hum. Genet. 66, 1729-1735 (2000
11. Lanpher B., Brunetti-Pierri N. & Lee B. Inborn errors of metabolism: the flux from Mendelian to complex diseases. Nat. Rev. Genet. 7, 449-460 (2006
12. Jeffery C. J. Moonlighting proteins - an update. Mol. Biosyst. 5, 345-350 (2009
13. Erez A., Shchelochkov O. A., Plon S. E., Scaglia F. & Lee B. Insights into the pathogenesis and treatment of cancer from inborn errors of metabolism. Am. J. Hum. Genet. 88, 402-421 (2011
14. Baysal B. E., et al. Prevalence of SDHB, SDHC, and SDHD germline mutations in clinic patients with head and neck paragangliomas. J. Med. Genet. 39, 178-183 (2002
15. Burnichon N., et al. SDHA is a tumor suppressor gene causing paraganglioma. Hum. Mol. Genet. 19, 3011-3020 (2010
16. Guzy R. D., Sharma B., Bell E., Chandel N. S. & Schumacker P. T. Loss of the SdhB, but not the SdhA, subunit of complex II triggers reactive oxygen species-dependent hypoxia-inducible factor activation and tumorigenesis. Mol. Cell. Biol. 28, 718-731 (2008
17. Kaelin W. G. Jr. SDH5 mutations and familial paraganglioma: somewhere Warburg is smiling. Cancer Cell 16, 180-182 (2009
18. Ricketts C. J., et al. Tumor risks and genotype- phenotype-proteotype analysis in 358 patients with germline mutations in SDHB and SDHD. Hum. Mutat. 31, 41-51 (2010
19. 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 Med. Genet. 9, 20 (2008
20. Zheng L., et al. Fumarate induces redox-dependent senescence by modifying glutathione metabolism. Nat. Commun. 6, 6001 (2015
21. Wellen K. E. & Thompson C. B. A two-way street: reciprocal regulation of metabolism and signalling. Nat. Rev. Mol. Cell Biol. 13, 270-276 (2012
22. Garber J. E. & Offit K. Hereditary cancer predisposition syndromes. J. Clin. Oncol. 23, 276-292 (2005
23. Samuel N., Villani A., Fernandez C. V. & Malkin D. Management of familial cancer: sequencing, surveillance and society. Nat. Rev. Clin. Oncol. 11, 723-731 (2014
24. Cizmarova M., et al. Rasopathies - dysmorphic syndromes with short stature and risk of malignancy. Endocr. Regul. 47, 217-222 (2013
25. Schiffman J. D., et al. Update on pediatric cancer predisposition syndromes. Pediatr. Blood Cancer 60, 1247-1252 (2013
26. Levy P. A. An overview of newborn screening. J. Dev. Behav. Pediatr. 31, 622-631 (2010
27. Gottlieb E. & Tomlinson I. P. Mitochondrial tumour suppressors: a genetic and biochemical update. Nat. Rev. Cancer 5, 857-866 (2005
28. Litten J. B. & Tomlinson G. E. Liver tumors in children. Oncologist 13, 812-820 (2008
29. Nelson R. L., Davis F. G., Persky V. & Becker E. Risk of neoplastic and other diseases among people with heterozygosity for hereditary hemochromatosis. Cancer 76, 875-879 (1995
30. Lithner F. & Wetterberg L. Hepatocellular carcinoma in patients with acute intermittent porphyria. Acta Med. Scand. 215, 271-274 (1984
31. Savas N., et al. Hepatocellular carcinoma in Wilson's disease: a rare association in childhood. Pediatr. Transplant. 10, 639-643 (2006
32. Yin P. H., et al. Alteration of the copy number and deletion of mitochondrial DNA in human hepatocellular carcinoma. Br. J. Cancer 90, 2390-2396 (2004
33. Cassiman D., et al. Bilateral renal cell carcinoma development in long-term Fabry disease. J. Inherit. Metab. Dis. 30, 830-831 (2007
34. Xu R., et al. Hepatocellular carcinoma in type 1 Gaucher disease: a case report with review of the literature. Semin. Liver Dis. 25, 226-229 (2005
35. Osborne N. J., et al. HFE C282Y homozygotes are at increased risk of breast and colorectal cancer. Hepatology 51, 1311-1318 (2010
36. Harrison S. A. & Bacon B. R. Relation of hemochromatosis with hepatocellular carcinoma: epidemiology, natural history, pathophysiology, screening, treatment, and prevention. Med. Clin. North Am. 89, 391-409 (2005
37. Bartlett D. C., Lloyd C., McKiernan P. J. & Newsome P. N. Early nitisinone treatment reduces the need for liver transplantation in children with tyrosinaemia type 1 and improves post-transplant renal function. J. Inherit. Metab. Dis. 37, 745-752 (2014
38. Yang M., Soga T. & Pollard P. J. Oncometabolites: linking altered metabolism with cancer. J. Clin. Invest. 123, 3652-3658 (2013
39. Selak M. A., et al. Succinate links TCA cycle dysfunction to oncogenesis by inhibiting HIF-α prolyl hydroxylase. Cancer Cell 7, 77-85 (2005
40. Tuppen H. A., Blakely E. L., Turnbull D. M. & Taylor R. W. Mitochondrial DNA mutations and human disease. Biochim. Biophys. Acta 1797, 113-128 (2010
41. Figueroa M. E., et al. DNA methylation signatures identify biologically distinct subtypes in acute myeloid leukemia. Cancer Cell 17, 13-27 (2010
42. Rakheja D., Medeiros L. J., Bevan S. & Chen W. The emerging role of d-2 hydroxyglutarate as an oncometabolite in hematolymphoid and central nervous system neoplasms. Front. Oncol. 3, 169 (2013
43. Letouze E., et al. SDH mutations establish a hypermethylator phenotype in paraganglioma. Cancer Cell 23, 739-752 (2013
44. Sullivan L. B., et al. The proto-oncometabolite fumarate binds glutathione to amplify ROS-dependent signaling. Mol. Cell 51, 236-248 (2013
45. Ooi A., et al. An antioxidant response phenotype shared between hereditary and sporadic type 2 papillary renal cell carcinoma. Cancer Cell 20, 511-523 (2011
46. Adam J., 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 20, 524-537 (2011
47. Singh A. K., Pandey P., Tewari M., Pandey H. P. & Shukla H. S. Human mitochondrial genome flaws and risk of cancer. Mitochondrial DNA 25, 329-334 (2014
48. Carew J. S. & Huang P. Mitochondrial defects in cancer. Mol. Cancer 1, 9 (2002
49. Scheers I., Bachy V., Stephenne X. & Sokal E. M. Risk of hepatocellular carcinoma in liver mitochondrial respiratory chain disorders. J. Pediatr. 146, 414-417 (2005
50. Kunz B. A. Mutagenesis and deoxyribonucleotide pool imbalance. Mutat. Res. 200, 133-147 (1988
51. Kulawiec M., et al. Tumorigenic transformation of human breast epithelial cells induced by mitochondrial DNA depletion. Cancer Biol. Ther. 7, 1732-1743 (2008
52. Dimmock D., et al. Citrin deficiency, a perplexing global disorder. Mol. Genet. Metab. 96, 44-49 (2009
53. Nagasaka H., et al. Sustaining hypercitrullinemia, hypercholesterolemia and augmented oxidative stress in Japanese children with aspartate/glutamate carrier isoform 2 citrin-deficiency even during the silent period. Mol. Genet. Metab. 97, 21-26 (2009
54. Kimura A., et al. Histological findings in the livers of patients with neonatal intrahepatic cholestasis caused by citrin deficiency. Hepatol. Res. 40, 295-303 (2010
55. Fukuhara N., Tokiguchi S., Shirakawa K. & Tsubaki T. Myoclonus epilepsy associated with ragged-red fibres (mitochondrial abnormalities): disease entity or a syndrome? Light-and electron-microscopic studies of two cases and review of literature. J. Neurol. Sci. 47, 117-133 (1980
56. Holme E., et al. Multiple symmetric lipomas with high levels of mtDNA with the tRNA(Lys) A->G(8344) mutation as the only manifestation of disease in a carrier of myoclonus epilepsy and ragged-red fibers (MERRF) syndrome. Am. J. Hum. Genet. 52, 551-556 (1993
57. Bourgeron T., et al. Mutation of a nuclear succinate dehydrogenase gene results in mitochondrial respiratory chain deficiency. Nat. Genet. 11, 144-149 (1995
58. Kerrigan J. F., Aleck K. A., Tarby T. J., Bird C. R. & Heidenreich R. A. Fumaric aciduria: clinical and imaging features. Ann. Neurol. 47, 583-588 (2000
59. Gimenez-Roqueplo A. P. New advances in the genetics of pheochromocytoma and paraganglioma syndromes. Ann. NY Acad. Sci. 1073, 112-121 (2006
60. Tomlinson I. P., et al. Germline mutations in FH predispose to dominantly inherited uterine fibroids, skin leiomyomata and papillary renal cell cancer. Nat. Genet. 30, 406-410 (2002
61. Stratakis C. A. & Carney J. A. The triad of paragangliomas, gastric stromal tumours and pulmonary chondromas (Carney triad), and the dyad of paragangliomas and gastric stromal sarcomas (Carney- Stratakis syndrome): molecular genetics and clinical implications. J. Intern. Med. 266, 43-52 (2009
62. Pollard P. J., 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. 14, 2231-2239 (2005
63. Adam J., et al. A role for cytosolic fumarate hydratase in urea cycle metabolism and renal neoplasia. Cell Rep. 3, 1440-1448 (2013
64. Zheng L., et al. Reversed argininosuccinate lyase activity in fumarate hydratase-deficient cancer cells. Cancer Metab. 1, 12 (2013
65. Alam N. A., et al. Genetic and functional analyses of FH mutations in multiple cutaneous and uterine leiomyomatosis, hereditary leiomyomatosis and renal cancer, and fumarate hydratase deficiency. Hum. Mol. Genet. 12, 1241-1252 (2003
66. Losman J. A. & Kaelin W. G. Jr. What a difference a hydroxyl makes: mutant IDH, (R)-2 hydroxyglutarate, and cancer. Genes Dev. 27, 836-852 (2013
67. Rogers R. E., et al. Wilms tumor in a child with l-2 hydroxyglutaric aciduria. Pediatr. Dev. Pathol. 13, 408-411 (2010
68. Moroni I., et al. l-2 hydroxyglutaric aciduria and brain malignant tumors: a predisposing condition?. Neurology 62, 1882-1884 (2004
69. Van Schaftingen E., Rzem R. & Veiga da Cunha M. l-2 Hydroxyglutaric aciduria, a disorder of metabolite repair. J. Inherit. Metab. Dis. 32, 135-142 (2009
70. Kranendijk M., Struys E. A., Salomons G. S., Van der Knaap M. S. & Jakobs C. Progress in understanding 2 hydroxyglutaric acidurias. J. Inherit. Metab. Dis. 35, 571-587 (2012
71. Kranendijk M., et al. IDH2 mutations in patients with d-2 hydroxyglutaric aciduria. Science 330, 336 (2010
72. Nota B., et al. Deficiency in SLC25A1, encoding the mitochondrial citrate carrier, causes combined d-2- and l-2 hydroxyglutaric aciduria. Am. J. Hum. Genet. 92, 627-631 (2013
73. Koivunen P., et al. Transformation by the (R)-enantiomer of 2 hydroxyglutarate linked to EGLN activation. Nature 483, 484-488 (2012
74. Lei K. J., Shelly L. L., Pan C. J., Sidbury J. B. & Chou J. Y. Mutations in the glucose 6 phosphatase gene that cause glycogen storage disease type 1a. Science 262, 580-583 (1993
75. Rake J. P., et al. Glycogen storage disease type I: diagnosis, management, clinical course and outcome. Results of the European Study on Glycogen Storage Disease Type I (ESGSD I). Eur. J. Pediatr. 161, S20-S34 (2002
76. Chou J. Y. & Mansfield B. C. Mutations in the glucose 6 phosphatase-alpha (G6PC) gene that cause type Ia glycogen storage disease. Hum. Mutat. 29, 921-930 (2008
77. Di Rocco M., et al. Hepatocellular adenoma and metabolic balance in patients with type Ia glycogen storage disease. Mol. Genet. Metab. 93, 398-402 (2008
78. Park S. K., Haase V. H. & Johnson R. S. von Hippel Lindau tumor suppressor regulates hepatic glucose metabolism by controlling expression of glucose transporter 2 and glucose 6 phosphatase. Int. J. Oncol. 30, 341-348 (2007
79. Nicholson L. J., et al. Epigenetic silencing of argininosuccinate synthetase confers resistance to platinum-induced cell death but collateral sensitivity to arginine auxotrophy in ovarian cancer. Int. J. Cancer 125, 1454-1463 (2009
80. Dillon B. J., et al. Incidence and distribution of argininosuccinate synthetase deficiency in human cancers: a method for identifying cancers sensitive to arginine deprivation. Cancer 100, 826-833 (2004
81. Delage B., et al. Arginine deprivation and argininosuccinate synthetase expression in the treatment of cancer. Int. J. Cancer 126, 2762-2772 (2010
82. Yang H., Zhai G., Ji X., Su J. & Lin M. Reduced expression of argininosuccinate lyase is closely associated with postresectional survival in hepatocellular carcinoma: an immunohistochemistry study of 61 cases. Appl. Immunohistochem. Mol. Morphol. 20, 602-606 (2012
83. Kobayashi E., et al. Reduced argininosuccinate synthetase is a predictive biomarker for the development of pulmonary metastasis in patients with osteosarcoma. Mol. Cancer Ther. 9, 535-544 (2010
84. Syed N., et al. Epigenetic status of argininosuccinate synthetase and argininosuccinate lyase modulates autophagy and cell death in glioblastoma. Cell Death Dis. 4, e458 (2013
85. Lincet H. & Icard P. How do glycolytic enzymes favour cancer cell proliferation by nonmetabolic functions?. Oncogene http://dx.doi.org/10.1038/onc.2014.320 (2014
86. Erez A. Argininosuccinic aciduria: from a monogenic to a complex disorder. Genet. Med. 15, 251-257 (2013
87. Majewski N., et al. Hexokinase-mitochondria interaction mediated by Akt is required to inhibit apoptosis in the presence or absence of Bax and Bak. Mol. Cell 16, 819-830 (2004
88. Danial N. N., et al. BAD and glucokinase reside in a mitochondrial complex that integrates glycolysis and apoptosis. Nature 424, 952-956 (2003
89. Yang J., Li J. H., Wang J. & Zhang C. Y. Molecular modeling of BAD complex resided in a mitochondrion integrating glycolysis and apoptosis. J. Theor. Biol. 266, 231-241 (2010
90. Niinaka Y., Paku S., Haga A., Watanabe H. & Raz A. Expression and secretion of neuroleukin/phosphohexose isomerase/maturation factor as autocrine motility factor by tumor cells. Cancer Res. 58, 2667-2674 (1998
91. Fruman D. A. & Rommel C. PI3K and cancer: lessons, challenges and opportunities. Nat. Rev. Drug Discov. 13, 140-156 (2014
92. Guo C., Liu S. & Sun M. Z. Novel insight into the role of GAPDH playing in tumor. Clin. Transl. Oncol. 15, 167-172 (2013
93. Tristan C., Shahani N., Sedlak T. W. & Sawa A. The diverse functions of GAPDH: views from different subcellular compartments. Cell Signal. 23, 317-323 (2011
94. Iqbal M. A., Gupta V., Gopinath P., Mazurek S. & Bamezai R. N. Pyruvate kinase M2 and cancer: an updated assessment. FEBS Lett. 588, 2685-2692 (2014
95. Li B., et al. Fructose 1,6 bisphosphatase opposes renal carcinoma progression. Nature 513, 251-255 (2014
96. Giovannini M., Biasucci G., Luotti D., Fiori L. & Riva E. Nutrition in children affected by inherited metabolic diseases. Ann. Ist. Super. Sanita 31, 489-502 (1995
97. Seyfried T. N., Flores R., Poff A. M., D'Agostino D. P. & Mukherjee P. Metabolic therapy: a new paradigm for managing malignant brain cancer. Cancer Lett. 356, 289-300 (2015
98. Klement R. J. Restricting carbohydrates to fight head and neck cancer - is this realistic?. Cancer Biol. Med. 11, 145-161 (2014
99. Yang Y., et al. Increased intake of vegetables, but not fruit, reduces risk for hepatocellular carcinoma: a meta-analysis. Gastroenterology 147, 1031-1042 (2014
100. Schwingshackl L. & Hoffmann G. Adherence to Mediterranean diet and risk of cancer: a systematic review and meta-analysis of observational studies. Int. J. Cancer 135, 1884-1897 (2014
101. Shils M. E. Principles of nutritional therapy. Cancer 43, 2093-2102 (1979
102. Wilcken B. An introduction to nutritional treatment in inborn errors of metabolism - different disorders, different approaches. Southeast Asian J. Trop. Med. Publ. Health 34 (Suppl. 3), 198-201 (2003
103. Nagamani S. C., et al. A randomized controlled trial to evaluate the effects of high-dose versus low-dose of arginine therapy on hepatic function tests in argininosuccinic aciduria. Mol. Genet. Metab. 107, 315-321 (2012
104. Walker V. Ammonia toxicity and its prevention in inherited defects of the urea cycle. Diabetes Obes. Metab. 11, 823-835 (2009
105. Locasale J. W., et al. Phosphoglycerate dehydrogenase diverts glycolytic flux and contributes to oncogenesis. Nat. Genet. 43, 869-874 (2011
106. Johnson S. C., et al. mTOR inhibition alleviates mitochondrial disease in a mouse model of Leigh syndrome. Science 342, 1524-1528 (2013
107. Folling I. The discovery of phenylketonuria. Acta Paediatr. Suppl. 407, 4-10 (1994
108. Guthrie R. & Susi A. A. Simple phenylalanine method for detecting phenylketonuria in large populations of newborn infants. Pediatrics 32, 338-343 (1963
109. Woo S. L., Lidsky A. S., Guttler F., Chandra T. & Robson K. J. Cloned human phenylalanine hydroxylase gene allows prenatal diagnosis and carrier detection of classical phenylketonuria. Nature 306, 151-155 (1983
110. Pearson P., et al. The status of online Mendelian inheritance in man (OMIM) medio 1994. Nucleic Acids Res. 22, 3470-3473 (1994
111. 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 235, 1492-1495 (1987
112. DiLella A. G., Huang W. M. & Woo S. L. Screening for phenylketonuria mutations by DNA amplification with the polymerase chain reaction. Lancet 1, 497-499 (1988
113. Goldwater R. S. Gaucher disease, enzyme replacement therapy, and the Patient Assistance Program. J. Intraven Nurs. 19, 83-88 (1996
114. Afaq A., Syed R. & Bomanji J. PET/MRI: a new technology in the field of molecular imaging. Br. Med. Bull. 108, 159-171 (2013
115. Gimm O., Armanios M., Dziema H., Neumann H. P. & Eng C. Somatic and occult germ-line mutations in SDHD, a mitochondrial complex II gene, in nonfamilial pheochromocytoma. Cancer Res. 60, 6822-6825 (2000
116. Desnick R. J. Enzyme replacement therapy for Fabry disease: lessons from two α-galactosidase A orphan products and one FDA approval. Expert Opin. Biol. Ther. 4, 1167-1176 (2004
117. Matoba S., et al. p53 regulates mitochondrial respiration. Science 312, 1650-1653 (2006
118. Rivkees S. A. The Newborn Screening Saves Lives Act - four million calls for support J. Pediatr. Endocrinol. Metab. 20, 457-458 (2007
119. Parsons D. W., et al. An integrated genomic analysis of human glioblastoma multiforme. Science 321, 1807-1812 (2008
120. Dang L., et al. Cancer-associated IDH1 mutations produce 2-hydroxyglutarate. Nature 462, 739-744 (2009
121. Yan H., et al. IDH1 and IDH2 mutations in gliomas. N. Engl. J. Med. 360, 765-773 (2009
122. Wang F., et al. Targeted inhibition of mutant IDH2 in leukemia cells induces cellular differentiation. Science 340, 622-626 (2013