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Current Protein & Peptide Science

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Mini-Review Article

Insights into The Function and Regulation of Jumonji C Lysine Demethylases as Hypoxic Responsive Enzymes

Author(s): Anand Chopra, Hemanta Adhikary, William G. Willmore* and Kyle K. Biggar*

Volume 21, Issue 7, 2020

Page: [642 - 654] Pages: 13

DOI: 10.2174/1389203721666191231104225

Price: $65

Abstract

Cellular responses to hypoxia (low oxygen) are governed by oxygen sensitive signaling pathways. Such pathways, in part, are controlled by enzymes with oxygen-dependent catalytic activity, of which the role of prolyl 4-hydroxylases has been widely reviewed. These enzymes inhibit hypoxic response by inducing the oxygen-dependent degradation of hypoxia-inducible factor 1α, the master regulator of the transcriptional hypoxic response. Jumonji C domain-containing lysine demethylases are similar enzymes which share the same oxygen-dependent catalytic mechanism as prolyl 4- hydroxylases. Traditionally, the role of lysine demethylases has been studied in relation to demethylation activity against histone substrates, however, within the past decade an increasing number of nonhistone protein targets have been revealed, some of which have a key role in survival in the hypoxic tumor microenvironment. Within this review, we highlight the involvement of methyllysine in the hypoxic response with a focus on the HIF signaling pathway, the regulation of demethylase activity by oxygen, and provide insights into notable areas of future hypoxic demethylase research.

Keywords: Hypoxia, hypoxia-inducible factor, methyllysine, lysine demethylase, Jumonji C, non-histone, hypoxic signaling, oxygen affinity.

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[1]
Embley, T.M.; Martin, W. Eukaryotic evolution, changes and challenges. Nature, 2006, 440(7084), 623-630.
[http://dx.doi.org/10.1038/nature04546] [PMID: 16572163]
[2]
Keeley, T.P.; Mann, G.E. Defining physiological normoxia for improved translation of cell physiology to animal models and humans. Physiol. Rev., 2019, 99(1), 161-234.
[http://dx.doi.org/10.1152/physrev.00041.2017] [PMID: 30354965]
[3]
Harris, A.L. Hypoxia--a key regulatory factor in tumour growth. Nat. Rev. Cancer, 2002, 2(1), 38-47.
[http://dx.doi.org/10.1038/nrc704] [PMID: 11902584]
[4]
Denko, N.C. Hypoxia, HIF1 and glucose metabolism in the solid tumour. Nat. Rev. Cancer, 2008, 8(9), 705-713.
[http://dx.doi.org/10.1038/nrc2468] [PMID: 19143055]
[5]
Courtnay, R.; Ngo, D.C.; Malik, N.; Ververis, K.; Tortorella, S.M.; Karagiannis, T.C. Cancer metabolism and the Warburg effect: the role of HIF-1 and PI3K. Mol. Biol. Rep., 2015, 42(4), 841-851.
[http://dx.doi.org/10.1007/s11033-015-3858-x] [PMID: 25689954]
[6]
Krock, B.L.; Skuli, N.; Simon, M.C. Hypoxia-induced angiogenesis: good and evil. Genes Cancer, 2011, 2(12), 1117-1133.
[http://dx.doi.org/10.1177/1947601911423654] [PMID: 22866203]
[7]
Ozer, A.; Bruick, R.K. Non-heme dioxygenases: cellular sensors and regulators jelly rolled into one? Nat. Chem. Biol., 2007, 3(3), 144-153.
[http://dx.doi.org/10.1038/nchembio863] [PMID: 17301803]
[8]
Lando, D.; Gorman, J.J.; Whitelaw, M.L.; Peet, D.J. Oxygen-dependent regulation of hypoxia-inducible factors by prolyl and asparaginyl hydroxylation. Eur. J. Biochem., 2003, 270(5), 781-790.
[http://dx.doi.org/10.1046/j.1432-1033.2003.03445.x] [PMID: 12603311]
[9]
Lando, D.; Peet, D.J.; Gorman, J.J.; Whelan, D.A.; Whitelaw, M.L.; Bruick, R.K. FIH-1 is an asparaginyl hydroxylase enzyme that regulates the transcriptional activity of hypoxia-inducible factor. Genes Dev., 2002, 16(12), 1466-1471.
[http://dx.doi.org/10.1101/gad.991402] [PMID: 12080085]
[10]
Lando, D.; Peet, D.J.; Whelan, D.A.; Gorman, J.J.; Whitelaw, M.L. Asparagine hydroxylation of the HIF transactivation domain a hypoxic switch. Science, 2002, 295(5556), 858-861.
[http://dx.doi.org/10.1126/science.1068592] [PMID: 11823643]
[11]
Biggar, K.K.; Li, S.S.C. Non-histone protein methylation as a regulator of cellular signalling and function. Nat. Rev. Mol. Cell Biol., 2015, 16(1), 5-17.
[http://dx.doi.org/10.1038/nrm3915] [PMID: 25491103]
[12]
Hamamoto, R.; Saloura, V.; Nakamura, Y. Critical roles of non-histone protein lysine methylation in human tumorigenesis. Nat. Rev. Cancer, 2015, 15(2), 110-124.
[http://dx.doi.org/10.1038/nrc3884] [PMID: 25614009]
[13]
Carlson, S.M.; Gozani, O. Nonhistone lysine methylation in the regulation of cancer pathways. Cold Spring Harb. Perspect. Med., 2016, 6(11)a026435
[http://dx.doi.org/10.1101/cshperspect.a026435] [PMID: 27580749]
[14]
Han, D.; Huang, M.; Wang, T.; Li, Z.; Chen, Y.; Liu, C.; Lei, Z.; Chu, X. Lysine methylation of transcription factors in cancer. Cell Death Dis., 2019, 10(4), 290.
[http://dx.doi.org/10.1038/s41419-019-1524-2] [PMID: 30926778]
[15]
Klose, R.J.; Kallin, E.M.; Zhang, Y. JmjC-domain-containing proteins and histone demethylation. Nat. Rev. Genet., 2006, 7(9), 715-727.
[http://dx.doi.org/10.1038/nrg1945] [PMID: 16983801]
[16]
Shi, Y.; Lan, F.; Matson, C.; Mulligan, P.; Whetstine, J.R.; Cole, P.A.; Casero, R.A.; Shi, Y. Histone demethylation mediated by the nuclear amine oxidase homolog LSD1. Cell, 2004, 119(7), 941-953.
[http://dx.doi.org/10.1016/j.cell.2004.12.012] [PMID: 15620353]
[17]
Majello, B.; Gorini, F.; Saccà, C.D.; Amente, S. Expanding the role of the histone lysine-specific demethylase LSD1 in cancer. Cancers (Basel), 2019, 11(3)E324
[http://dx.doi.org/10.3390/cancers11030324] [PMID: 30866496]
[18]
Ramadoss, S.; Guo, G.; Wang, C.Y. Lysine demethylase KDM3A regulates breast cancer cell invasion and apoptosis by targeting histone and the non-histone protein p53. Oncogene, 2017, 36(1), 47-59.
[http://dx.doi.org/10.1038/onc.2016.174] [PMID: 27270439]
[19]
Yang, L.; Lin, C.; Liu, W.; Zhang, J.; Ohgi, K.A.; Grinstein, J.D.; Dorrestein, P.C.; Rosenfeld, M.G. ncRNA- and Pc2 methylation-dependent gene relocation between nuclear structures mediates gene activation programs. Cell, 2011, 147(4), 773-788.
[http://dx.doi.org/10.1016/j.cell.2011.08.054] [PMID: 22078878]
[20]
Koehntop, K.D.; Emerson, J.P.; Que, L., Jr The 2-His-1-carboxylate facial triad: a versatile platform for dioxygen activation by mononuclear non-heme iron(II) enzymes. J. Biol. Inorg. Chem., 2005, 10(2), 87-93.
[http://dx.doi.org/10.1007/s00775-005-0624-x] [PMID: 15739104]
[21]
Zhou, J.; Gunsior, M.; Bachmann, B.O.; Townsend, C.A.; Solomon, E.I. Substrate binding to the α-ketoglutarate-dependent non-heme iron enzyme clavaminate synthase 2: Coupling mechanism of oxidative decarboxylation and hydroxylation. J. Am. Chem. Soc., 1989, 120(51), 13539-13540.
[http://dx.doi.org/10.1021/ja983534x]
[22]
Walport, L.J.; Hopkinson, R.J.; Chowdhury, R.; Schiller, R.; Ge, W.; Kawamura, A.; Schofield, C.J. Arginine demethylation is catalysed by a subset of JmjC histone lysine demethylases. Nat. Commun., 2016, 7, 11974.
[http://dx.doi.org/10.1038/ncomms11974] [PMID: 27337104]
[23]
Meng, Y.; Li, H.; Liu, C.; Zheng, L.; Shen, B. Jumonji domain-containing protein family: the functions beyond lysine demethylation. J. Mol. Cell Biol., 2018, 10(4), 371-373.
[http://dx.doi.org/10.1093/jmcb/mjy010] [PMID: 29659917]
[24]
Zhang, J.; Jing, L.; Li, M.; He, L.; Guo, Z. Regulation of histone arginine methylation/demethylation by methylase and demethylase. (Review) Mol. Med. Rep., 2019, 19(5), 3963-3971.
[http://dx.doi.org/10.3892/mmr.2019.10111] [PMID: 30942418]
[25]
Unoki, M.; Masuda, A.; Dohmae, N.; Arita, K.; Yoshimatsu, M.; Iwai, Y.; Fukui, Y.; Ueda, K.; Hamamoto, R.; Shirakawa, M.; Sasaki, H.; Nakamura, Y. Lysyl 5-hydroxylation, a novel histone modification, by Jumonji domain containing 6 (JMJD6). J. Biol. Chem., 2013, 288(9), 6053-6062.
[http://dx.doi.org/10.1074/jbc.M112.433284] [PMID: 23303181]
[26]
Webby, C.J.; Wolf, A.; Gromak, N.; Dreger, M.; Kramer, H.; Kessler, B.; Nielsen, M.L.; Schmitz, C.; Butler, D.S.; Yates, J.R., III; Delahunty, C.M.; Hahn, P.; Lengeling, A.; Mann, M.; Proudfoot, N.J.; Schofield, C.J.; Böttger, A. Jmjd6 catalyses lysyl-hydroxylation of U2AF65, a protein associated with RNA splicing. Science, 2009, 325(5936), 90-93.
[http://dx.doi.org/10.1126/science.1175865] [PMID: 19574390]
[27]
Markolovic, S.; Zhuang, Q.; Wilkins, S.E.; Eaton, C.D.; Abboud, M.I.; Katz, M.J.; McNeil, H.E.; Leśniak, R.K.; Hall, C.; Struwe, W.B.; Konietzny, R.; Davis, S.; Yang, M.; Ge, W.; Benesch, J.L.P.; Kessler, B.M.; Ratcliffe, P.J.; Cockman, M.E.; Fischer, R.; Wappner, P.; Chowdhury, R.; Coleman, M.L.; Schofield, C.J. The Jumonji-C oxygenase JMJD7 catalyzes (3S)-lysyl hydroxylation of TRAFAC GTPases. Nat. Chem. Biol., 2018, 14(7), 688-695.
[http://dx.doi.org/10.1038/s41589-018-0071-y] [PMID: 29915238]
[28]
Liu, X.; Chen, Z.; Xu, C.; Leng, X.; Cao, H.; Ouyang, G.; Xiao, W. Repression of hypoxia-inducible factor α signaling by Set7-mediated methylation. Nucleic Acids Res., 2015, 43(10), 5081-5098.
[http://dx.doi.org/10.1093/nar/gkv379] [PMID: 25897119]
[29]
Kim, Y.; Nam, H.J.; Lee, J.; Park, D.Y.; Kim, C.; Yu, Y.S.; Kim, D.; Park, S.W.; Bhin, J.; Hwang, D.; Lee, H.; Koh, G.Y.; Baek, S.H. Methylation-dependent regulation of HIF-1α stability restricts retinal and tumour angiogenesis. Nat. Commun., 2016, 7, 10347.
[http://dx.doi.org/10.1038/ncomms10347] [PMID: 26757928]
[30]
Lee, J.Y.; Park, J.H.; Choi, H.J.; Won, H.Y.; Joo, H.S.; Shin, D.H.; Park, M.K.; Han, B.; Kim, K.P.; Lee, T.J.; Croce, C.M.; Kong, G. LSD1 demethylates HIF1α to inhibit hydroxylation and ubiquitin-mediated degradation in tumor angiogenesis. Oncogene, 2017, 36(39), 5512-5521.
[http://dx.doi.org/10.1038/onc.2017.158] [PMID: 28534506]
[31]
Bao, L.; Chen, Y.; Lai, H.T.; Wu, S.Y.; Wang, J.E.; Hatanpaa, K.J.; Raisanen, J.M.; Fontenot, M.; Lega, B.; Chiang, C.M.; Semenza, G.L.; Wang, Y.; Luo, W. Methylation of hypoxia-inducible factor (HIF)-1α by G9a/GLP inhibits HIF-1 transcriptional activity and cell migration. Nucleic Acids Res., 2018, 46(13), 6576-6591.
[http://dx.doi.org/10.1093/nar/gky449] [PMID: 29860315]
[32]
Xiao, B.; Jing, C.; Wilson, J.R.; Walker, P.A.; Vasisht, N.; Kelly, G.; Howell, S.; Taylor, I.A.; Blackburn, G.M.; Gamblin, S.J. Structure and catalytic mechanism of the human histone methyltransferase SET7/9. Nature, 2003, 421(6923), 652-656.
[http://dx.doi.org/10.1038/nature01378] [PMID: 12540855]
[33]
Couture, J.F.; Collazo, E.; Hauk, G.; Trievel, R.C. Structural basis for the methylation site specificity of SET7/9. Nat. Struct. Mol. Biol., 2006, 13(2), 140-146.
[http://dx.doi.org/10.1038/nsmb1045] [PMID: 16415881]
[34]
Dhayalan, A.; Kudithipudi, S.; Rathert, P.; Jeltsch, A. Specificity analysis-based identification of new methylation targets of the SET7/9 protein lysine methyltransferase. Chem. Biol., 2011, 18(1), 111-120.
[http://dx.doi.org/10.1016/j.chembiol.2010.11.014] [PMID: 21276944]
[35]
Yang, Y.; Bedford, M.T. Titivated for destruction: the methyl degron. Mol. Cell, 2012, 48(4), 487-488.
[http://dx.doi.org/10.1016/j.molcel.2012.11.007] [PMID: 23200121]
[36]
Lee, J.M.; Lee, J.S.; Kim, H.; Kim, K.; Park, H.; Kim, J.Y.; Lee, S.H.; Kim, I.S.; Kim, J.; Lee, M.; Chung, C.H.; Seo, S.B.; Yoon, J.B.; Ko, E.; Noh, D.Y.; Kim, K.I.; Kim, K.K.; Baek, S.H. EZH2 generates a methyl degron that is recognized by the DCAF1/DDB1/CUL4 E3 ubiquitin ligase complex. Mol. Cell, 2012, 48(4), 572-586.
[http://dx.doi.org/10.1016/j.molcel.2012.09.004] [PMID: 23063525]
[37]
Lim, J.H.; Lee, Y.M.; Chun, Y.S.; Chen, J.; Kim, J.E.; Park, J.W. Sirtuin 1 modulates cellular responses to hypoxia by deacetylating hypoxia-inducible factor 1α. Mol. Cell, 2010, 38(6), 864-878.
[http://dx.doi.org/10.1016/j.molcel.2010.05.023] [PMID: 20620956]
[38]
Lee, J.S.; Kim, Y.; Kim, I.S.; Kim, B.; Choi, H.J.; Lee, J.M.; Shin, H.J.; Kim, J.H.; Kim, J.Y.; Seo, S.B.; Lee, H.; Binda, O.; Gozani, O.; Semenza, G.L.; Kim, M.; Kim, K.I.; Hwang, D.; Baek, S.H. Negative regulation of hypoxic responses via induced Reptin methylation. Mol. Cell, 2010, 39(1), 71-85.
[http://dx.doi.org/10.1016/j.molcel.2010.06.008] [PMID: 20603076]
[39]
Lee, J.S.; Kim, Y.; Bhin, J.; Shin, H.J.; Nam, H.J.; Lee, S.H.; Yoon, J.B.; Binda, O.; Gozani, O.; Hwang, D.; Baek, S.H. Hypoxia-induced methylation of a pontin chromatin remodeling factor. Proc. Natl. Acad. Sci. USA, 2011, 108(33), 13510-13515.
[http://dx.doi.org/10.1073/pnas.1106106108] [PMID: 21825155]
[40]
Kim, J.H.; Kim, B.; Cai, L.; Choi, H.J.; Ohgi, K.A.; Tran, C.; Chen, C.; Chung, C.H.; Huber, O.; Rose, D.W.; Sawyers, C.L.; Rosenfeld, M.G.; Baek, S.H. Transcriptional regulation of a metastasis suppressor gene by Tip60 and β-catenin complexes. Nature, 2005, 434(7035), 921-926.
[http://dx.doi.org/10.1038/nature03452] [PMID: 15829968]
[41]
Kim, J.H.; Choi, H.J.; Kim, B.; Kim, M.H.; Lee, J.M.; Kim, I.S.; Lee, M.H.; Choi, S.J.; Kim, K.I.; Kim, S.I.; Chung, C.H.; Baek, S.H. Roles of sumoylation of a reptin chromatin-remodelling complex in cancer metastasis. Nat. Cell Biol., 2006, 8(6), 631-639.
[http://dx.doi.org/10.1038/ncb1415] [PMID: 16699503]
[42]
Liu, Y.V.; Semenza, G.L. RACK1 vs. HSP90: competition for HIF-1 α degradation vs. stabilization. Cell Cycle, 2007, 6(6), 656-659.
[http://dx.doi.org/10.4161/cc.6.6.3981] [PMID: 17361105]
[43]
Yang, S.J.; Park, Y.S.; Cho, J.H.; Moon, B.; An, H.J.; Lee, J.Y.; Xie, Z.; Wang, Y.; Pocalyko, D.; Lee, D.C.; Sohn, H.A.; Kang, M.; Kim, J.Y.; Kim, E.; Park, K.C.; Kim, J.A.; Yeom, Y.I. Regulation of hypoxia responses by flavin adenine dinucleotide-dependent modulation of HIF-1α protein stability. EMBO J., 2017, 36(8), 1011-1028.
[http://dx.doi.org/10.15252/embj.201694408] [PMID: 28279976]
[44]
Song, H.; Feng, X.; Zhang, M.; Jin, X.; Xu, X.; Wang, L.; Ding, X.; Luo, Y.; Lin, F.; Wu, Q.; Liang, G.; Yu, T.; Liu, Q.; Zhang, Z. Crosstalk between lysine methylation and phosphorylation of ATG16L1 dictates the apoptosis of hypoxia/reoxygenation-induced cardiomyocytes. Autophagy, 2018, 14(5), 825-844.
[http://dx.doi.org/10.1080/15548627.2017.1389357] [PMID: 29634390]
[45]
Kunizaki, M.; Hamamoto, R.; Silva, F.P.; Yamaguchi, K.; Nagayasu, T.; Shibuya, M.; Nakamura, Y.; Furukawa, Y. The lysine 831 of vascular endothelial growth factor receptor 1 is a novel target of methylation by SMYD3. Cancer Res., 2007, 67(22), 10759-10765.
[http://dx.doi.org/10.1158/0008-5472.CAN-07-1132] [PMID: 18006819]
[46]
Rahimi, N. Vascular endothelial growth factor receptors: molecular mechanisms of activation and therapeutic potentials. Exp. Eye Res., 2006, 83(5), 1005-1016.
[http://dx.doi.org/10.1016/j.exer.2006.03.019] [PMID: 16713597]
[47]
Franke, K.; Gassmann, M.; Wielockx, B. Erythrocytosis: the HIF pathway in control. Blood, 2013, 122(7), 1122-1128.
[http://dx.doi.org/10.1182/blood-2013-01-478065] [PMID: 23733342]
[48]
Salminen, A.; Kaarniranta, K.; Kauppinen, A. Hypoxia-inducible histone lysine demethylases: Impact on the aging process and age-related diseases. Aging Dis., 2016, 7(2), 180-200.
[http://dx.doi.org/10.14336/AD.2015.0929] [PMID: 27114850]
[49]
Choudhry, H.; Harris, A.L. Advances in hypoxia-inducible factor biology. Cell Metab., 2018, 27(2), 281-298.
[http://dx.doi.org/10.1016/j.cmet.2017.10.005] [PMID: 29129785]
[50]
Melvin, A.; Rocha, S. Chromatin as an oxygen sensor and active player in the hypoxia response. Cell. Signal., 2012, 24(1), 35-43.
[http://dx.doi.org/10.1016/j.cellsig.2011.08.019] [PMID: 21924352]
[51]
Hancock, R.L.; Dunne, K.; Walport, L.J.; Flashman, E.; Kawamura, A. Epigenetic regulation by histone demethylases in hypoxia. Epigenomics, 2015, 7(5), 791-811.
[http://dx.doi.org/10.2217/epi.15.24] [PMID: 25832587]
[52]
Park, H. Hypoxia suffocates histone demethylases to change gene expression: a metabolic control of histone methylation. BMB Rep., 2017, 50(11), 537-538.
[http://dx.doi.org/10.5483/BMBRep.2017.50.11.200] [PMID: 29065972]
[53]
Batie, M.; Rocha, S. JmjC histone demethylases act as chromatin oxygen sensors. Mol. Cell. Oncol., 2019, 6(4)1608501
[http://dx.doi.org/10.1080/23723556.2019.1608501] [PMID: 31211238]
[54]
Shmakova, A.; Batie, M.; Druker, J.; Rocha, S. Chromatin and oxygen sensing in the context of JmjC histone demethylases. Biochem. J., 2014, 462(3), 385-395.
[http://dx.doi.org/10.1042/BJ20140754] [PMID: 25145438]
[55]
Pollard, P.J.; Loenarz, C.; Mole, D.R.; McDonough, M.A.; Gleadle, J.M.; Schofield, C.J.; Ratcliffe, P.J. Regulation of Jumonji-domain-containing histone demethylases by hypoxia-inducible factor (HIF)-1α. Biochem. J., 2008, 416(3), 387-394.
[http://dx.doi.org/10.1042/BJ20081238] [PMID: 18713068]
[56]
Wellmann, S.; Bettkober, M.; Zelmer, A.; Seeger, K.; Faigle, M.; Eltzschig, H.K.; Bührer, C. Hypoxia upregulates the histone demethylase JMJD1A via HIF-1. Biochem. Biophys. Res. Commun., 2008, 372(4), 892-897.
[http://dx.doi.org/10.1016/j.bbrc.2008.05.150] [PMID: 18538129]
[57]
Krieg, A.J.; Rankin, E.B.; Chan, D.; Razorenova, O.; Fernandez, S.; Giaccia, A.J. Regulation of the histone demethylase JMJD1A by hypoxia-inducible factor 1 alpha enhances hypoxic gene expression and tumor growth. Mol. Cell. Biol., 2010, 30(1), 344-353.
[http://dx.doi.org/10.1128/MCB.00444-09] [PMID: 19858293]
[58]
Wan, W.; Peng, K.; Li, M.; Qin, L.; Tong, Z.; Yan, J.; Shen, B.; Yu, C. Histone demethylase JMJD1A promotes urinary bladder cancer progression by enhancing glycolysis through coactivation of hypoxia inducible factor 1α. Oncogene, 2017, 36(27), 3868-3877.
[http://dx.doi.org/10.1038/onc.2017.13] [PMID: 28263974]
[59]
Yang, J.; Jubb, A.M.; Pike, L.; Buffa, F.M.; Turley, H.; Baban, D.; Leek, R.; Gatter, K.C.; Ragoussis, J.; Harris, A.L. The histone demethylase JMJD2B is regulated by estrogen receptor alpha and hypoxia, and is a key mediator of estrogen induced growth. Cancer Res., 2010, 70(16), 6456-6466.
[http://dx.doi.org/10.1158/0008-5472.CAN-10-0413] [PMID: 20682797]
[60]
Bishop, T.; Ratcliffe, P.J. Signaling hypoxia by hypoxia-inducible factor protein hydroxylases: a historical overview and future perspectives. Hypoxia (Auckl.), 2014, 2, 197-213.
[PMID: 27774477]
[61]
Ehrismann, D.; Flashman, E.; Genn, D.N.; Mathioudakis, N.; Hewitson, K.S.; Ratcliffe, P.J.; Schofield, C.J. Studies on the activity of the hypoxia-inducible-factor hydroxylases using an oxygen consumption assay. Biochem. J., 2007, 401(1), 227-234.
[http://dx.doi.org/10.1042/BJ20061151] [PMID: 16952279]
[62]
Hirsilä, M.; Koivunen, P.; Günzler, V.; Kivirikko, K.I.; Myllyharju, J. Characterization of the human prolyl 4-hydroxylases that modify the hypoxia-inducible factor. J. Biol. Chem., 2003, 278(33), 30772-30780.
[http://dx.doi.org/10.1074/jbc.M304982200] [PMID: 12788921]
[63]
Cascella, B.; Mirica, L.M. Kinetic analysis of iron-dependent histone demethylases: α-ketoglutarate substrate inhibition and potential relevance to the regulation of histone demethylation in cancer cells. Biochemistry, 2012, 51(44), 8699-8701.
[http://dx.doi.org/10.1021/bi3012466] [PMID: 23067339]
[64]
Hancock, R.L.; Masson, N.; Dunne, K.; Flashman, E.; Kawamura, A. The activity of JmjC histone lysine demethylase KDM4A is highly sensitive to oxygen concentrations. ACS Chem. Biol., 2017, 12(4), 1011-1019.
[http://dx.doi.org/10.1021/acschembio.6b00958] [PMID: 28051298]
[65]
Chakraborty, A.A.; Laukka, T.; Myllykoski, M.; Ringel, A.E.; Booker, M.A.; Tolstorukov, M.Y.; Meng, Y.J.; Meier, S.R.; Jennings, R.B.; Creech, A.L.; Herbert, Z.T.; McBrayer, S.K.; Olenchock, B.A.; Jaffe, J.D.; Haigis, M.C.; Beroukhim, R.; Signoretti, S.; Koivunen, P.; Kaelin, W.G. Jr Histone demethylase KDM6A directly senses oxygen to control chromatin and cell fate. Science, 2019, 363(6432), 1217-1222.
[http://dx.doi.org/10.1126/science.aaw1026] [PMID: 30872525]
[66]
Black, J.C.; Atabakhsh, E.; Kim, J.; Biette, K.M.; Van Rechem, C.; Ladd, B.; Burrowes, P.D.; Donado, C.; Mattoo, H.; Kleinstiver, B.P.; Song, B.; Andriani, G.; Joung, J.K.; Iliopoulos, O.; Montagna, C.; Pillai, S.; Getz, G.; Whetstine, J.R. Hypoxia drives transient site-specific copy gain and drug-resistant gene expression. Genes Dev., 2015, 29(10), 1018-1031.
[http://dx.doi.org/10.1101/gad.259796.115] [PMID: 25995187]
[67]
Flashman, E.; Hoffart, L.M.; Hamed, R.B.; Bollinger, J.M., Jr; Krebs, C.; Schofield, C.J. Evidence for the slow reaction of hypoxia-inducible factor prolyl hydroxylase 2 with oxygen. FEBS J., 2010, 277(19), 4089-4099.
[http://dx.doi.org/10.1111/j.1742-4658.2010.07804.x] [PMID: 20840591]
[68]
Sánchez-Fernández, E.M.; Tarhonskaya, H.; Al-Qahtani, K.; Hopkinson, R.J.; McCullagh, J.S.O.; Schofield, C.J.; Flashman, E. Investigations on the oxygen dependence of a 2-oxoglutarate histone demethylase. Biochem. J., 2013, 449(2), 491-496.
[http://dx.doi.org/10.1042/BJ20121155] [PMID: 23092293]
[69]
Batie, M.; Frost, J.; Frost, M.; Wilson, J.W.; Schofield, P.; Rocha, S. Hypoxia induces rapid changes to histone methylation and reprograms chromatin. Science, 2019, 363(6432), 1222-1226.
[http://dx.doi.org/10.1126/science.aau5870] [PMID: 30872526]
[70]
Laukka, T.; Mariani, C.J.; Ihantola, T.; Cao, J.Z.; Hokkanen, J.; Kaelin, W.G., Jr; Godley, L.A.; Koivunen, P. Fumarate and succinate regulate expression of hypoxia-inducible genes via TET enzymes. J. Biol. Chem., 2016, 291(8), 4256-4265.
[http://dx.doi.org/10.1074/jbc.M115.688762] [PMID: 26703470]
[71]
Myllyharju, J.; Kivirikko, K.I. Characterization of the iron- and 2-oxoglutarate-binding sites of human prolyl 4-hydroxylase. EMBO J., 1997, 16(6), 1173-1180.
[http://dx.doi.org/10.1093/emboj/16.6.1173] [PMID: 9135134]
[72]
Lee, H.Y.; Yang, E.G.; Park, H. Hypoxia enhances the expression of prostate-specific antigen by modifying the quantity and catalytic activity of Jumonji C domain-containing histone demethylases. Carcinogenesis, 2013, 34(12), 2706-2715.
[http://dx.doi.org/10.1093/carcin/bgt256] [PMID: 23884959]
[73]
Beyer, S.; Kristensen, M.M.; Jensen, K.S.; Johansen, J.V.; Staller, P. The histone demethylases JMJD1A and JMJD2B are transcriptional targets of hypoxia-inducible factor HIF. J. Biol. Chem., 2008, 283(52), 36542-36552.
[http://dx.doi.org/10.1074/jbc.M804578200] [PMID: 18984585]
[74]
Chen, H.; Kluz, T.; Zhang, R.; Costa, M. Hypoxia and nickel inhibit histone demethylase JMJD1A and repress Spry2 expression in human bronchial epithelial BEAS-2B cells. Carcinogenesis, 2010, 31(12), 2136-2144.
[http://dx.doi.org/10.1093/carcin/bgq197] [PMID: 20881000]
[75]
Chang, S.; Yim, S.; Park, H. The cancer driver genes IDH1/2, JARID1C/KDM5C, and UTX/KDM6A: crosstalk between histone demethylation and hypoxic reprogramming in cancer metabolism. Exp. Mol. Med., 2019, 51(6), 66.
[http://dx.doi.org/10.1038/s12276-019-0230-6] [PMID: 31221981]
[76]
Tarhonskaya, H.; Nowak, R.P.; Johansson, C.; Szykowska, A.; Tumber, A.; Hancock, R.L.; Lang, P.; Flashman, E.; Oppermann, U.; Schofield, C.J.; Kawamura, A. Studies on the interaction of the histone demethylase KDM5B with tricarboxylic acid cycle intermediates. J. Mol. Biol., 2017, 429(19), 2895-2906.
[http://dx.doi.org/10.1016/j.jmb.2017.08.007] [PMID: 28827149]
[77]
Chowdhury, R.; Yeoh, K.K.; Tian, Y.M.; Hillringhaus, L.; Bagg, E.A.; Rose, N.R.; Leung, I.K.; Li, X.S.; Woon, E.C.; Yang, M.; McDonough, M.A.; King, O.N.; Clifton, I.J.; Klose, R.J.; Claridge, T.D.; Ratcliffe, P.J.; Schofield, C.J.; Kawamura, A. The oncometabolite 2-hydroxyglutarate inhibits histone lysine demethylases. EMBO Rep., 2011, 12(5), 463-469.
[http://dx.doi.org/10.1038/embor.2011.43] [PMID: 21460794]
[78]
Metzen, E.; Zhou, J.; Jelkmann, W.; Fandrey, J.; Brüne, B. Nitric oxide impairs normoxic degradation of HIF-1alpha by inhibition of prolyl hydroxylases. Mol. Biol. Cell, 2003, 14(8), 3470-3481.
[http://dx.doi.org/10.1091/mbc.e02-12-0791] [PMID: 12925778]
[79]
Hickok, J.R.; Vasudevan, D.; Antholine, W.E.; Thomas, D.D. Nitric oxide modifies global histone methylation by inhibiting Jumonji C domain-containing demethylases. J. Biol. Chem., 2013, 288(22), 16004-16015.
[http://dx.doi.org/10.1074/jbc.M112.432294] [PMID: 23546878]
[80]
Chen, H.; Costa, M. Iron- and 2-oxoglutarate-dependent dioxygenases: an emerging group of molecular targets for nickel toxicity and carcinogenicity. Biometals, 2009, 22(1), 191-196.
[http://dx.doi.org/10.1007/s10534-008-9190-3] [PMID: 19096759]
[81]
Chen, H.; Giri, N.C.; Zhang, R.; Yamane, K.; Zhang, Y.; Maroney, M.; Costa, M. Nickel ions inhibit histone demethylase JMJD1A and DNA repair enzyme ABH2 by replacing the ferrous iron in the catalytic centers. J. Biol. Chem., 2010, 285(10), 7374-7383.
[http://dx.doi.org/10.1074/jbc.M109.058503] [PMID: 20042601]
[82]
Perillo, B.; Ombra, M.N.; Bertoni, A.; Cuozzo, C.; Sacchetti, S.; Sasso, A.; Chiariotti, L.; Malorni, A.; Abbondanza, C.; Avvedimento, E.V. DNA oxidation as triggered by H3K9me2 demethylation drives estrogen-induced gene expression. Science, 2008, 319(5860), 202-206.
[http://dx.doi.org/10.1126/science.1147674] [PMID: 18187655]
[83]
Nair, S.S.; Nair, B.C.; Cortez, V.; Chakravarty, D.; Metzger, E.; Schüle, R.; Brann, D.W.; Tekmal, R.R.; Vadlamudi, R.K. PELP1 is a reader of histone H3 methylation that facilitates oestrogen receptor-α target gene activation by regulating lysine demethylase 1 specificity. EMBO Rep., 2010, 11(6), 438-444.
[http://dx.doi.org/10.1038/embor.2010.62] [PMID: 20448663]
[84]
Zhang, X.; Tanaka, K.; Yan, J.; Li, J.; Peng, D.; Jiang, Y.; Yang, Z.; Barton, M.C.; Wen, H.; Shi, X. Regulation of estrogen receptor α by histone methyltransferase SMYD2-mediated protein methylation. Proc. Natl. Acad. Sci. USA, 2013, 110(43), 17284-17289.
[http://dx.doi.org/10.1073/pnas.1307959110] [PMID: 24101509]
[85]
Ramadoss, S.; Sen, S.; Ramachandran, I.; Roy, S.; Chaudhuri, G.; Farias-Eisner, R. Lysine-specific demethylase KDM3A regulates ovarian cancer stemness and chemoresistance. Oncogene, 2017, 36(11), 1537-1545.
[http://dx.doi.org/10.1038/onc.2016.320] [PMID: 27694900]
[86]
Luo, W.; Chang, R.; Zhong, J.; Pandey, A.; Semenza, G.L. Histone demethylase JMJD2C is a coactivator for hypoxia-inducible factor 1 that is required for breast cancer progression. Proc. Natl. Acad. Sci. USA, 2012, 109(49), E3367-E3376.
[http://dx.doi.org/10.1073/pnas.1217394109] [PMID: 23129632]
[87]
Mimura, I.; Nangaku, M.; Kanki, Y.; Tsutsumi, S.; Inoue, T.; Kohro, T.; Yamamoto, S.; Fujita, T.; Shimamura, T.; Suehiro, J.; Taguchi, A.; Kobayashi, M.; Tanimura, K.; Inagaki, T.; Tanaka, T.; Hamakubo, T.; Sakai, J.; Aburatani, H.; Kodama, T.; Wada, Y. Dynamic change of chromatin conformation in response to hypoxia enhances the expression of GLUT3 (SLC2A3) by cooperative interaction of hypoxia-inducible factor 1 and KDM3A. Mol. Cell. Biol., 2012, 32(15), 3018-3032.
[http://dx.doi.org/10.1128/MCB.06643-11] [PMID: 22645302]
[88]
Yamane, K.; Toumazou, C.; Tsukada, Y.; Erdjument-Bromage, H.; Tempst, P.; Wong, J.; Zhang, Y. JHDM2A, a JmjC-containing H3K9 demethylase, facilitates transcription activation by androgen receptor. Cell, 2006, 125(3), 483-495.
[http://dx.doi.org/10.1016/j.cell.2006.03.027] [PMID: 16603237]
[89]
Goda, S.; Isagawa, T.; Chikaoka, Y.; Kawamura, T.; Aburatani, H. Control of histone H3 lysine 9 (H3K9) methylation state via cooperative two-step demethylation by Jumonji domain containing 1A (JMJD1A) homodimer. J. Biol. Chem., 2013, 288(52), 36948-36956.
[http://dx.doi.org/10.1074/jbc.M113.492595] [PMID: 24214985]
[90]
Lancaster, D.E.; McNeill, L.A.; McDonough, M.A.; Aplin, R.T.; Hewitson, K.S.; Pugh, C.W.; Ratcliffe, P.J.; Schofield, C.J. Disruption of dimerization and substrate phosphorylation inhibit factor inhibiting hypoxia-inducible factor (FIH) activity. Biochem. J., 2004, 383(Pt. 3), 429-437.
[http://dx.doi.org/10.1042/BJ20040735] [PMID: 15239670]
[91]
Marxsen, J.H.; Stengel, P.; Doege, K.; Heikkinen, P.; Jokilehto, T.; Wagner, T.; Jelkmann, W.; Jaakkola, P.; Metzen, E. Hypoxia-inducible factor-1 (HIF-1) promotes its degradation by induction of HIF-α-prolyl-4-hydroxylases. Biochem. J., 2004, 381(Pt 3), 761-767.
[http://dx.doi.org/10.1042/BJ20040620] [PMID: 15104534]
[92]
André, H.; Pereira, T.S. Identification of an alternative mechanism of degradation of the hypoxia-inducible factor-1α. J. Biol. Chem., 2008, 283(43), 29375-29384.
[http://dx.doi.org/10.1074/jbc.M805919200] [PMID: 18694926]
[93]
Masson, N.; Singleton, R.S.; Sekirnik, R.; Trudgian, D.C.; Ambrose, L.J.; Miranda, M.X.; Tian, Y.M.; Kessler, B.M.; Schofield, C.J.; Ratcliffe, P.J. The FIH hydroxylase is a cellular peroxide sensor that modulates HIF transcriptional activity. EMBO Rep., 2012, 13(3), 251-257.
[http://dx.doi.org/10.1038/embor.2012.9] [PMID: 22310300]

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