Oxygen Concentration controls epigenetic effects in models of familial paraganglioma

PLoS ONE

Volumn 10, Issue 5, 2015, Pages

  Her, Yeng F ^a,b   Nelson Holte, Molly ^a   Maher, Louis James ^a  

^a MAYO GRADUATE SCHOOL   (United States)

^b MAYO CLINIC   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

2 OXOGLUTARIC ACID; DIOXYGENASE; DNA; HISTONE; HYPOXIA INDUCIBLE FACTOR 1ALPHA; HYPOXIA INDUCIBLE FACTOR 2ALPHA; OXYGEN; SUCCINATE DEHYDROGENASE; SUCCINIC ACID; 5-HYDROXYMETHYLCYTOSINE; ALPHA-KETOGLUTARIC ACID; CYTOSINE;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; CELL CULTURE; CONTROLLED STUDY; DISEASE ASSOCIATION; DNA METHYLATION; ENZYME DEFICIENCY; ENZYME INHIBITION; EPIGENETICS; HISTONE METHYLATION; HUMAN; HUMAN CELL; HUMAN TISSUE; HYPOTHESIS; HYPOXIA; MOUSE; NONHUMAN; PARAGANGLIOMA; ANALOGS AND DERIVATIVES; ANIMAL; ANTAGONISTS AND INHIBITORS; BIOLOGICAL MODEL; C57BL MOUSE; CASE CONTROL STUDY; DRUG EFFECTS; FIBROBLAST; GENE SILENCING; GENETIC EPIGENESIS; GENETICS; HEK293 CELL LINE; METABOLISM;

ANIMALS; CASE-CONTROL STUDIES; CYTOSINE; DIOXYGENASES; DNA METHYLATION; EPIGENESIS, GENETIC; FIBROBLASTS; GENE KNOCKDOWN TECHNIQUES; HEK293 CELLS; HISTONES; HUMANS; HYPOXIA-INDUCIBLE FACTOR 1, ALPHA SUBUNIT; KETOGLUTARIC ACIDS; MICE, INBRED C57BL; MODELS, BIOLOGICAL; OXYGEN; PARAGANGLIOMA; SUCCINATE DEHYDROGENASE; SUCCINIC ACID;

EID: 84930674809     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0127471     Document Type: Article

References (76)

1. Astuti D, Latif F, Dallol A, Dahia PL, Douglas F, George E, 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: 49-54. PMID: 11404820
2. Baysal BE, Ferrell RE, Willett-Brozick JE, Lawrence EC, Myssiorek D, Bosch A, et al. (2000) Mutations in SDHD, a mitochondrial complex II gene, in hereditary paraganglioma. Science 287: 848-51. PMID: 10657297
3. Baysal BE, Willett-Brozick JE, Lawrence EC, Drovdlic CM, Savul SA, McLeod DR, et al. (2002) Prevalence of SDHB, SDHC, and SDHD germline mutations in clinic patients with head and neck paragangliomas. J Med Genet 39: 178-83. PMID: 11897817
4. Hao HX, Khalimonchuk O, Schraders M, Dephoure N, Bayley JP, Kunst H, et al. (2009) SDH5, a gene required for flavination of succinate dehydrogenase, is mutated in paraganglioma. Science 325: 1139-42. doi: 10.1126/science.1175689 PMID: 19628817
5. Burnichon N, Briere JJ, Libe R, Vescovo L, Riviere J, Tissier F, et al. (2010) SDHA is a tumor suppressor gene causing paraganglioma. Hum Mol Genet 19: 3011-20. doi: 10.1093/hmg/ddq206 PMID: 20484225
6. Niemann S, Muller U (2000) Mutations in SDHC cause autosomal dominant paraganglioma, type 3. Nat Genet 26: 268-70. PMID: 11062460
7. Guzy RD, Sharma B, Bell E, Chandel NS, Schumacker PT (2008) 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: 718-31. PMID: 17967865
8. Pollard PJ, Briere JJ, Alam NA, Barwell J, Barclay E, Wortham NC, 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: 2231-9. PMID: 15987702
9. Selak MA, Armour SM, MacKenzie ED, Boulahbel H, Watson DG, Mansfield KD, et al. (2005) Succinate links TCA cycle dysfunction to oncogenesis by inhibiting HIF-alpha prolyl hydroxylase. Cancer Cell 7: 77-85. PMID: 15652751
10. rd (2007) Succinate Inhibition of alpha-Ketoglutarate-Dependent Enzymes in a Yeast Model of Paraganglioma. Hum Mol Genet 16: 3136-48. PMID: 17884808
11. Xiao M, Yang H, Xu W, Ma S, Lin H, Zhu H, et al. (2012) Inhibition of alpha-KG-dependent histone and DNA demethylases by fumarate and succinate that are accumulated in mutations of FH and SDH tumor suppressors. Genes Dev 26: 1326-38. doi: 10.1101/gad.191056.112 PMID: 22677546
12. Letouze E, Martinelli C, Loriot C, Burnichon N, Abermil N, Ottolenghi C, et al. (2013) SDH mutations establish a hypermethylator phenotype in paraganglioma. Cancer Cell 23: 739-52. doi: 10.1016/j.ccr.2013.04.018 PMID: 23707781
13. Bardella C, Pollard PJ, Tomlinson I (2011) SDH mutations in cancer. Biochim Biophys Acta 1807: 1432-43. doi: 10.1016/j.bbabio.2011.07.003 PMID: 21771581
14. MacKenzie ED, Selak MA, Tennant DA, Payne LJ, Crosby S, Frederiksen CM, et al. (2007) Cell-permeating alpha-ketoglutarate derivatives alleviate pseudohypoxia in succinate dehydrogenase-deficient cells. Mol Cell Biol 27: 3282-9. PMID: 17325041
15. Richter S, Peitzsch M, Rapizzi E, Lenders JW, Qin N, de Cubas AA, et al. (2014) Krebs cycle metabolite profiling for identification and stratification of pheochromocytomas/paragangliomas due to succinate dehydrogenase deficiency. J Clin Endocrinol Metab 99: 3903-11. doi: 10.1210/jc.2014-2151 PMID: 25014000
16. Lendvai N, Pawlosky R, Bullova P, Eisenhofer G, Patocs A, Veech RL, et al. (2014) Succinate-to-fumarate ratio as a new metabolic marker to detect the presence of SDHB/D-related paraganglioma: initial experimental and ex vivo findings. Endocrinology 155: 27-32. doi: 10.1210/en.2013-1549 PMID: 24189137
17. Pollard PJ, El-Bahrawy M, Poulsom R, Elia G, Killick P, Kelly G, et al. (2006) Expression of HIF-1alpha, HIF-2alpha (EPAS1), and their target genes in paraganglioma and pheochromocytoma with VHL and SDH mutations. J Clin Endocrinol Metab 91: 4593-8. PMID: 16954163
18. Gimenez-Roqueplo AP, Favier J, Rustin P, Rieubland C, Kerlan V, Plouin PF, et al. (2002) Functional consequences of a SDHB gene mutation in an apparently sporadic pheochromocytoma. J Clin Endocrinol Metab 87: 4771-4. PMID: 12364472
19. Gimenez-Roqueplo AP, Favier J, Rustin P, Mourad JJ, Plouin PF, Corvol P, et al. (2001) The R22X mutation of the SDHD gene in hereditary paraganglioma abolishes the enzymatic activity of complex II in the mitochondrial respiratory chain and activates the hypoxia pathway. Am J Hum Genet 69: 1186-97. PMID: 11605159
20. Favier J, Briere JJ, Burnichon N, Riviere J, Vescovo L, Benit P, et al. (2009) The warburg effect is genetically determined in inherited pheochromocytomas. PLoS ONE 4: e7094. doi: 10.1371/journal.pone.0007094 PMID: 19763184
21. Koh MY, Lemos R Jr, Liu X, Powis G (2011) The hypoxia-associated factor switches cells from HIF-1alpha- to HIF-2alpha-dependent signaling promoting stem cell characteristics, aggressive tumor growth and invasion. Cancer Res 71: 4015-27. doi: 10.1158/0008-5472.CAN-10-4142 PMID: 21512133
22. Briere JJ, Favier J, Benit P, El Ghouzzi V, Lorenzato A, Rabier D, et al. (2005) Mitochondrial succinate is instrumental for HIF1alpha nuclear translocation in SDHA-mutant fibroblasts under normoxic conditions. Hum Mol Genet 14: 3263-9. PMID: 16195397
23. Saldana MJ, Salem LE, Travezan R (1973) High altitude hypoxia and chemodectomas. Hum Pathol 4: 251-63. PMID: 4706179
24. Arias-Stella J, Bustos F (1976) Chronic hypoxia and chemodectomas in bovines at high altitudes. Arch Pathol Lab Med 100: 636-9. PMID: 187143
25. Astrom K, Cohen JE, Willett-Brozick JE, Aston CE, Baysal BE (2003) Altitude is a phenotypic modifier in hereditary paraganglioma type 1: evidence for an oxygen-sensing defect. Hum Genet 113: 228-37. PMID: 12811540
26. Ayala-Ramirez M, Habra MA, Busaidy N, Cote G, Rich T, Waguespack S, et al. (2010) A catecholamine crisis on Mount Kilimanjaro: a hypoxia effect? J Travel Med 17: 424-6. doi: 10.1111/j.1708-8305.2010.00463.x PMID: 21050326
27. Kasaliwal R, Sarathi V, Pandit R, Budyal SR, Bukan A, Kakade H, et al. (2014) Pheochromocytoma and tetralogy of fallot: a rare but potentially dangerous combination. Endocr Pract 20: e80-5. doi: 10.4158/EP13408.CR PMID: 24449673
28. Folger GM Jr, Roberts WC, Mehrizi A, Shah KD, Glancy DL, Carpenter CC, et al. (1964) Cyanotic Malformations of the Heart with Pheochromocytoma. A Report of Five Cases. Circulation 29: 750-7. PMID: 14156866
29. Kita T, Imamura T, Date H, Kitamura K, Moriguchi S, Sato Y, et al. (2003) Two cases of pheochromocytoma associated with tetralogy of Fallot. Hypertens Res 26: 433-7. PMID: 12887136
30. Opotowsky AR, Moko L, Ginns J, Rosenbaum M, Greutmann M, Aboulhosn J, et al. (2015) Pheochromocytoma and Paraganglioma in Cyanotic Congenital Heart Disease. J Clin Endocrinol Metab: jc20143863.
31. Bancos I, Bida JP, Tian D, Bundrick M, John K, Holte MN, et al. (2013) High-throughput screening for growth inhibitors using a yeast model of familial paraganglioma. PLoS One 8: e56827. doi: 10.1371/journal.pone.0056827 PMID: 23451094
32. Miest T, Saenz D, Meehan A, Llano M, Poeschla EM (2009) Intensive RNAi with lentiviral vectors in mammalian cells. Methods 47: 298-303. doi: 10.1016/j.ymeth.2008.11.001 PMID: 19041944
33. Baker DJ, Jeganathan KB, Cameron JD, Thompson M, Juneja S, Kopecka A, et al. (2004) BubR1 insufficiency causes early onset of aging-associated phenotypes and infertility in mice. Nat Genet 36: 744-9. PMID: 15208629
34. Ricke RM, Jeganathan KB, Malureanu L, Harrison AM, van Deursen JM (2012) Bub1 kinase activity drives error correction and mitotic checkpoint control but not tumor suppression. J Cell Biol 199: 931-49. doi: 10.1083/jcb.201205115 PMID: 23209306
35. Tevethia MJ (1984) Immortalization of primary mouse embryo fibroblasts with SV40 virions, viral DNA, and a subgenomic DNA fragment in a quantitative assay. Virology 137: 414-21. PMID: 6091337
36. Aaronson SA, Todaro GJ (1968) Development of 3T3-like lines from Balb-c mouse embryo cultures: transformation susceptibility to SV40. J Cell Physiol 72: 141-8. PMID: 4301006
37. Koek MM, Muilwijk B, van der Werf MJ, Hankemeier T (2006) Microbial metabolomics with gas chromatography/mass spectrometry. Anal Chem 78: 1272-81. PMID: 16478122
38. Sandhu J, Kaur B, Armstrong C, Talbot CJ, Steward WP, Farmer PB, et al. (2009) Determination of 5-methyl-2′-deoxycytidine in genomic DNA using high performance liquid chromatography-ultraviolet detection. J Chromatogr B 877: 1957-61.
39. rd (2013) Mechanical properties of DNA-like polymers. Nucleic Acids Res 41: 10593-604. doi: 10.1093/nar/gkt808 PMID: 24013560
40. Gimenez-Roqueplo AP, Favier J, Rustin P, Rieubland C, Crespin M, Nau V, et al. (2003) Mutations in the SDHB gene are associated with extra-adrenal and/or malignant phaeochromocytomas. Cancer Res 63: 5615-21. PMID: 14500403
41. King KS, Prodanov T, Kantorovich V, Fojo T, Hewitt JK, Zacharin M, et al. (2011) Metastatic pheochromocytoma/paraganglioma related to primary tumor development in childhood or adolescence: significant link to SDHB mutations. J Clin Oncol 29: 4137-42. doi: 10.1200/JCO.2011.34.6353 PMID: 21969497
42. Amar L, Baudin E, Burnichon N, Peyrard S, Silvera S, Bertherat J, et al. (2007) Succinate dehydrogenase B gene mutations predict survival in patients with malignant pheochromocytomas or paragangliomas. J Clin Endocrinol Metab 92: 3822-8. PMID: 17652212
43. van Nederveen FH, Gaal J, Favier J, Korpershoek E, Oldenburg RA, de Bruyn EM, et al. (2009) An immunohistochemical procedure to detect patients with paraganglioma and phaeochromocytoma with germline SDHB, SDHC, or SDHD gene mutations: a retrospective and prospective analysis. Lancet Oncol 10: 764-71. doi: 10.1016/S1470-2045(09)70164-0 PMID: 19576851
44. Gill AJ, Benn DE, Chou A, Clarkson A, Muljono A, Meyer-Rochow GY, et al. (2010) Immunohistochemistry for SDHB triages genetic testing of SDHB, SDHC, and SDHD in paraganglioma-pheochromocytoma syndromes. Hum Pathol 41: 805-14. doi: 10.1016/j.humpath.2009.12.005 PMID: 20236688
45. Isaacs JS, Jung YJ, Mole DR, Lee S, Torres-Cabala C, Chung YL, et al. (2005) HIF overexpression correlates with biallelic loss of fumarate hydratase in renal cancer: novel role of fumarate in regulation of HIF stability. Cancer Cell 8: 143-53. PMID: 16098467
46. Myllyla R, Tuderman L, Kivirikko KI (1977) Mechanism of the prolyl hydroxylase reaction. 2. Kinetic analysis of the reaction sequence. Eur J Biochem 80: 349-57. PMID: 200425
47. Tuderman L, Myllyla R, Kivirikko KI (1977) Mechanism of the prolyl hydroxylase reaction. 1. Role of cosubstrates. Eur J Biochem 80: 341-8. PMID: 200424
48. Hirsila M, Koivunen P, Gunzler V, Kivirikko KI, Myllyharju J (2003) Characterization of the human prolyl 4-hydroxylases that modify the hypoxia-inducible factor. J Biol Chem 278: 30772-80. PMID: 12788921
49. Koivunen P, Hirsila M, Remes AM, Hassinen IE, Kivirikko KI, Myllyharju J (2007) Inhibition of hypoxiainducible factor (HIF) hydroxylases by citric acid cycle intermediates - Possible links between cell metabolism and stabilization of HIF. J Biol Chem 282: 4524-32. PMID: 17182618
50. Whalen WJ, Ganfield R, Nair P (1970) Effects of breathing O2 or O2 plus CO2 and of the injection of neurohumors on the PO2 of cat cerebral cortex. Stroke 1: 194-200. PMID: 4399607
51. Sridhar KS, Plasse TF, Holland JF, Shapiro M, Ohnuma T (1983) Effects of physiological oxygen concentration on human tumor colony growth in soft agar. Cancer Res 43: 4629-31. PMID: 6883320
52. Wolfle D, Jungermann K (1985) Long-term effects of physiological oxygen concentrations on glycolysis and gluconeogenesis in hepatocyte cultures. Eur J Biochem 151: 299-303. PMID: 4029136
53. Yu DY, Cringle SJ (2005) Retinal degeneration and local oxygen metabolism. Exp Eye Res 80: 745-51. PMID: 15939030
54. Tennant DA, Frezza C, MacKenzie ED, Nguyen QD, Zheng L, Selak MA, et al. (2009) Reactivating HIF prolyl hydroxylases under hypoxia results in metabolic catastrophe and cell death. Oncogene 28: 4009-21. doi: 10.1038/onc.2009.250 PMID: 19718054
55. Killian JK, Kim SY, Miettinen M, Smith C, Merino M, Tsokos M, et al. (2013) Succinate dehydrogenase mutation underlies global epigenomic divergence in gastrointestinal stromal tumor. Cancer Discov 3: 648-57. doi: 10.1158/2159-8290.CD-13-0092 PMID: 23550148
56. Mariani CJ, Vasanthakumar A, Madzo J, Yesilkanal A, Bhagat T, Yu Y, et al. (2014) TET1-mediated hydroxymethylation facilitates hypoxic gene induction in neuroblastoma. Cell Rep 7: 1343-52. doi: 10.1016/j.celrep.2014.04.040 PMID: 24835990
57. Yan H, Parsons DW, Jin G, McLendon R, Rasheed BA, Yuan W, et al. (2009) IDH1 and IDH2 Mutations in Gliomas. New England J Med 360: 765-73. doi: 10.1056/NEJMoa0808710 PMID: 19228619
58. Dang L, White DW, Gross S, Bennett BD, Bittinger MA, Driggers EM, et al. (2009) Cancer-associated IDH1 mutations produce 2-hydroxyglutarate. Nature 462: 739-44. doi: 10.1038/nature08617 PMID: 19935646
59. Figueroa ME, Abdel-Wahab O, Lu C, Ward PS, Patel J, Shih A, et al. (2010) Leukemic IDH1 and IDH2 mutations result in a hypermethylation phenotype, disrupt TET2 function, and impair hematopoietic differentiation. Cancer Cell 18: 553-67. doi: 10.1016/j.ccr.2010.11.015 PMID: 21130701
60. Kaelin WG Jr (2011) Cancer and altered metabolism: potential importance of hypoxia-inducible factor and 2-oxoglutarate-dependent dioxygenases. Cold Spring Harb Symp Quant Biol 76: 335-45. doi: 10.1101/sqb.2011.76.010975 PMID: 22089927
61. Salnikow K, Donald SP, Bruick RK, Zhitkovich A, Phang JM, Kasprzak KS (2004) Depletion of intracellular ascorbate by the carcinogenic metals nickel and cobalt results in the induction of hypoxic stress. J Biol Chem 279: 40337-44. PMID: 15271983
62. Losman JA, Looper RE, Koivunen P, Lee S, Schneider RK, McMahon C, et al. (2013) (R)-2-hydroxyglutarate is sufficient to promote leukemogenesis and its effects are reversible. Science 339: 1621-5. doi: 10.1126/science.1231677 PMID: 23393090
63. Lu C, Ward PS, Kapoor GS, Rohle D, Turcan S, Abdel-Wahab O, et al. (2012) IDH mutation impairs histone demethylation and results in a block to cell differentiation. Nature 483: 474-8. doi: 10.1038/nature10860 PMID: 22343901
64. Akbay EA, Moslehi J, Christensen CL, Saha S, Tchaicha JH, Ramkissoon SH, et al. (2014) D-2-hydroxyglutarate produced by mutant IDH2 causes cardiomyopathy and neurodegeneration in mice. Genes Dev 28: 479-90. doi: 10.1101/gad.231233.113 PMID: 24589777
65. Rao DD, Vorhies JS, Senzer N, Nemunaitis J (2009) siRNA vs. shRNA: Similarities and differences. Adv Drug Deliver Rev 61: 746-59. doi: 10.1016/j.addr.2009.04.004 PMID: 19389436
66. DiGiusto DL, Krishnan A, Li LJ, Li HT, Li S, Rao A, et al. (2010) RNA-Based Gene Therapy for HIV With Lentiviral Vector-Modified CD34(+) Cells in Patients Undergoing Transplantation for AIDS-Related Lymphoma. Sci Transl Med 2.
67. Favier J, Gimenez-Roqueplo AP (2010) Pheochromocytomas: The (pseudo)-hypoxia hypothesis. Best Pract Res Clin Endocrinol Metab 24: 957-68. doi: 10.1016/j.beem.2010.10.004 PMID: 21115164
68. Dahia PL, Ross KN, Wright ME, Hayashida CY, Santagata S, Barontini M, et al. (2005) A HIF1alpha regulatory loop links hypoxia and mitochondrial signals in pheochromocytomas. PLoS Genet 1: 72-80. PMID: 16103922
69. Qin Y, Buddavarapu K, Dahia PL (2009) Pheochromocytomas: from genetic diversity to new paradigms. Horm Metab Res 41: 664-71. doi: 10.1055/s-0029-1215590 PMID: 19391076
70. Qin N, de Cubas AA, Garcia-Martin R, Richter S, Peitzsch M, Menschikowski M, et al. (2014) Opposing effects of HIF1alpha and HIF2alpha on chromaffin cell phenotypic features and tumor cell proliferation: Insights from MYC-associated factor X. Int J Cancer 135: 2054-64. doi: 10.1002/ijc.28868 PMID: 24676840
71. Maxwell PH (2005) A common pathway for genetic events leading to pheochromocytoma. Cancer Cell 8: 91-3. PMID: 16098460
72. Khan Q, Heath D, Smith P, Norboo T (1988) The histology of the carotid bodies in highlanders from Ladakh. Int J Biometerol 32: 254-9. PMID: 3235211
73. Rodriguez-Cuevas S, Lopez-Garza J, Labastida-Almendaro S (1998) Carotid body tumors in inhabitants of altitudes higher than 2000 meters above sea level. Head Neck 20: 374-8. PMID: 9663663
74. Cerecer-Gil NY, Figuera LE, Llamas FJ, Lara M, Escamilla JG, Ramos R, et al. (2010) Mutation of SDHB is a Cause of Hypoxia-Related High-Altitude Paraganglioma. Clin Cancer Res 16: 4148-54. doi: 10.1158/1078-0432.CCR-10-0637 PMID: 20592014
75. Kumar P, Prabhakar NR (2012) Peripheral chemoreceptors: function and plasticity of the carotid body. Compr Physiol 2: 141-219. doi: 10.1002/cphy.c100069 PMID: 23728973
76. Hatfield SM, Kjaergaard J, Lukashev D, Schreiber TH, Belikoff B, Abbott R, et al. (2015) Immunological mechanisms of the antitumor effects of supplemental oxygenation. Sci Transl Med 7: 277ra30.