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1.

Fumarate is an epigenetic modifier that elicits epithelial-to-mesenchymal transition.

Sciacovelli M, Gonçalves E, Johnson TI, Zecchini VR, da Costa AS, Gaude E, Drubbel AV, Theobald SJ, Abbo SR, Tran MG, Rajeeve V, Cardaci S, Foster S, Yun H, Cutillas P, Warren A, Gnanapragasam V, Gottlieb E, Franze K, Huntly B, Maher ER, Maxwell PH, Saez-Rodriguez J, Frezza C.

Nature. 2016 Aug 31;537(7621):544-547. doi: 10.1038/nature19353. Erratum in: Nature. 2016 Dec 1;540(7631):150.

2.

Aberrant succination of proteins in fumarate hydratase-deficient mice and HLRCC patients is a robust biomarker of mutation status.

Bardella C, El-Bahrawy M, Frizzell N, Adam J, Ternette N, Hatipoglu E, Howarth K, O'Flaherty L, Roberts I, Turner G, Taylor J, Giaslakiotis K, Macaulay VM, Harris AL, Chandra A, Lehtonen HJ, Launonen V, Aaltonen LA, Pugh CW, Mihai R, Trudgian D, Kessler B, Baynes JW, Ratcliffe PJ, Tomlinson IP, Pollard PJ.

J Pathol. 2011 Sep;225(1):4-11. doi: 10.1002/path.2932. Epub 2011 Jun 1.

PMID:
21630274
3.

Expression profiling in progressive stages of fumarate-hydratase deficiency: the contribution of metabolic changes to tumorigenesis.

Ashrafian H, O'Flaherty L, Adam J, Steeples V, Chung YL, East P, Vanharanta S, Lehtonen H, Nye E, Hatipoglu E, Miranda M, Howarth K, Shukla D, Troy H, Griffiths J, Spencer-Dene B, Yusuf M, Volpi E, Maxwell PH, Stamp G, Poulsom R, Pugh CW, Costa B, Bardella C, Di Renzo MF, Kotlikoff MI, Launonen V, Aaltonen L, El-Bahrawy M, Tomlinson I, Pollard PJ.

Cancer Res. 2010 Nov 15;70(22):9153-65. doi: 10.1158/0008-5472.CAN-10-1949. Epub 2010 Oct 26.

4.

Genetic and functional analyses of FH mutations in multiple cutaneous and uterine leiomyomatosis, hereditary leiomyomatosis and renal cancer, and fumarate hydratase deficiency.

Alam NA, Rowan AJ, Wortham NC, Pollard PJ, Mitchell M, Tyrer JP, Barclay E, Calonje E, Manek S, Adams SJ, Bowers PW, Burrows NP, Charles-Holmes R, Cook LJ, Daly BM, Ford GP, Fuller LC, Hadfield-Jones SE, Hardwick N, Highet AS, Keefe M, MacDonald-Hull SP, Potts ED, Crone M, Wilkinson S, Camacho-Martinez F, Jablonska S, Ratnavel R, MacDonald A, Mann RJ, Grice K, Guillet G, Lewis-Jones MS, McGrath H, Seukeran DC, Morrison PJ, Fleming S, Rahman S, Kelsell D, Leigh I, Olpin S, Tomlinson IP.

Hum Mol Genet. 2003 Jun 1;12(11):1241-52.

PMID:
12761039
5.

Fumarate induces redox-dependent senescence by modifying glutathione metabolism.

Zheng L, Cardaci S, Jerby L, MacKenzie ED, Sciacovelli M, Johnson TI, Gaude E, King A, Leach JD, Edrada-Ebel R, Hedley A, Morrice NA, Kalna G, Blyth K, Ruppin E, Frezza C, Gottlieb E.

Nat Commun. 2015 Jan 23;6:6001. doi: 10.1038/ncomms7001.

6.

A role for cytosolic fumarate hydratase in urea cycle metabolism and renal neoplasia.

Adam J, Yang M, Bauerschmidt C, Kitagawa M, O'Flaherty L, Maheswaran P, Özkan G, Sahgal N, Baban D, Kato K, Saito K, Iino K, Igarashi K, Stratford M, Pugh C, Tennant DA, Ludwig C, Davies B, Ratcliffe PJ, El-Bahrawy M, Ashrafian H, Soga T, Pollard PJ.

Cell Rep. 2013 May 30;3(5):1440-8. doi: 10.1016/j.celrep.2013.04.006. Epub 2013 May 2.

7.

Haem oxygenase is synthetically lethal with the tumour suppressor fumarate hydratase.

Frezza C, Zheng L, Folger O, Rajagopalan KN, MacKenzie ED, Jerby L, Micaroni M, Chaneton B, Adam J, Hedley A, Kalna G, Tomlinson IP, Pollard PJ, Watson DG, Deberardinis RJ, Shlomi T, Ruppin E, Gottlieb E.

Nature. 2011 Aug 17;477(7363):225-8. doi: 10.1038/nature10363.

PMID:
21849978
8.

Dysregulation of hypoxia pathways in fumarate hydratase-deficient cells is independent of defective mitochondrial metabolism.

O'Flaherty L, Adam J, Heather LC, Zhdanov AV, Chung YL, Miranda MX, Croft J, Olpin S, Clarke K, Pugh CW, Griffiths J, Papkovsky D, Ashrafian H, Ratcliffe PJ, Pollard PJ.

Hum Mol Genet. 2010 Oct 1;19(19):3844-51. doi: 10.1093/hmg/ddq305. Epub 2010 Jul 21.

9.

Fumarase tumor suppressor gene and MET oncogene cooperate in upholding transformation and tumorigenesis.

Costa B, Dettori D, Lorenzato A, Bardella C, Coltella N, Martino C, Cammarata C, Carmeliet P, Olivero M, Di Renzo MF.

FASEB J. 2010 Aug;24(8):2680-8. doi: 10.1096/fj.09-146928. Epub 2010 Mar 30.

PMID:
20354140
10.

Adipose-Specific Deficiency of Fumarate Hydratase in Mice Protects Against Obesity, Hepatic Steatosis, and Insulin Resistance.

Yang H, Wu JW, Wang SP, Severi I, Sartini L, Frizzell N, Cinti S, Yang G, Mitchell GA.

Diabetes. 2016 Nov;65(11):3396-3409. Epub 2016 Aug 23.

11.

Cells lacking the fumarase tumor suppressor are protected from apoptosis through a hypoxia-inducible factor-independent, AMPK-dependent mechanism.

Bardella C, Olivero M, Lorenzato A, Geuna M, Adam J, O'Flaherty L, Rustin P, Tomlinson I, Pollard PJ, Di Renzo MF.

Mol Cell Biol. 2012 Aug;32(15):3081-94. doi: 10.1128/MCB.06160-11. Epub 2012 May 29.

12.

Fumarate is cardioprotective via activation of the Nrf2 antioxidant pathway.

Ashrafian H, Czibik G, Bellahcene M, Aksentijević D, Smith AC, Mitchell SJ, Dodd MS, Kirwan J, Byrne JJ, Ludwig C, Isackson H, Yavari A, Støttrup NB, Contractor H, Cahill TJ, Sahgal N, Ball DR, Birkler RI, Hargreaves I, Tennant DA, Land J, Lygate CA, Johannsen M, Kharbanda RK, Neubauer S, Redwood C, de Cabo R, Ahmet I, Talan M, Günther UL, Robinson AJ, Viant MR, Pollard PJ, Tyler DJ, Watkins H.

Cell Metab. 2012 Mar 7;15(3):361-71. doi: 10.1016/j.cmet.2012.01.017.

13.

Fumarate hydratase is a critical metabolic regulator of hematopoietic stem cell functions.

Guitart AV, Panagopoulou TI, Villacreces A, Vukovic M, Sepulveda C, Allen L, Carter RN, van de Lagemaat LN, Morgan M, Giles P, Sas Z, Gonzalez MV, Lawson H, Paris J, Edwards-Hicks J, Schaak K, Subramani C, Gezer D, Armesilla-Diaz A, Wills J, Easterbrook A, Coman D, So CW, O'Carroll D, Vernimmen D, Rodrigues NP, Pollard PJ, Morton NM, Finch A, Kranc KR.

J Exp Med. 2017 Mar 6;214(3):719-735. doi: 10.1084/jem.20161087. Epub 2017 Feb 15.

14.

SUMOylation regulates nuclear localization of Krüppel-like factor 5.

Du JX, Bialkowska AB, McConnell BB, Yang VW.

J Biol Chem. 2008 Nov 14;283(46):31991-2002. doi: 10.1074/jbc.M803612200. Epub 2008 Sep 9.

15.

Inhibition of α-KG-dependent histone and DNA demethylases by fumarate and succinate that are accumulated in mutations of FH and SDH tumor suppressors.

Xiao M, Yang H, Xu W, Ma S, Lin H, Zhu H, Liu L, Liu Y, Yang C, Xu Y, Zhao S, Ye D, Xiong Y, Guan KL.

Genes Dev. 2012 Jun 15;26(12):1326-38. doi: 10.1101/gad.191056.112. Epub 2012 Jun 7. Erratum in: Genes Dev. 2015 Apr 15;29(8):887.

16.

Renal cyst formation in Fh1-deficient mice is independent of the Hif/Phd pathway: roles for fumarate in KEAP1 succination and Nrf2 signaling.

Adam J, Hatipoglu E, O'Flaherty L, Ternette N, Sahgal N, Lockstone H, Baban D, Nye E, Stamp GW, Wolhuter K, Stevens M, Fischer R, Carmeliet P, Maxwell PH, Pugh CW, Frizzell N, Soga T, Kessler BM, El-Bahrawy M, Ratcliffe PJ, Pollard PJ.

Cancer Cell. 2011 Oct 18;20(4):524-37. doi: 10.1016/j.ccr.2011.09.006.

17.

From Nf1 to Sdhb knockout: Successes and failures in the quest for animal models of pheochromocytoma.

Lepoutre-Lussey C, Thibault C, Buffet A, Morin A, Badoual C, Bénit P, Rustin P, Ottolenghi C, Janin M, Castro-Vega LJ, Trapman J, Gimenez-Roqueplo AP, Favier J.

Mol Cell Endocrinol. 2016 Feb 5;421:40-8. doi: 10.1016/j.mce.2015.06.027. Epub 2015 Jun 27. Review.

PMID:
26123588
18.

Targeted inactivation of fh1 causes proliferative renal cyst development and activation of the hypoxia pathway.

Pollard PJ, Spencer-Dene B, Shukla D, Howarth K, Nye E, El-Bahrawy M, Deheragoda M, Joannou M, McDonald S, Martin A, Igarashi P, Varsani-Brown S, Rosewell I, Poulsom R, Maxwell P, Stamp GW, Tomlinson IP.

Cancer Cell. 2007 Apr;11(4):311-9.

20.

Applying gene expression, proteomics and single-nucleotide polymorphism analysis for complex trait gene identification.

Stylianou IM, Affourtit JP, Shockley KR, Wilpan RY, Abdi FA, Bhardwaj S, Rollins J, Churchill GA, Paigen B.

Genetics. 2008 Mar;178(3):1795-805. doi: 10.1534/genetics.107.081216. Epub 2008 Feb 3.

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