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Article

A Hypertension-Associated tRNAAla Mutation Alters tRNA Metabolism and Mitochondrial Function

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Pages 1920-1930 | Received 21 Apr 2016, Accepted 04 May 2016, Published online: 17 Mar 2023

REFERENCES

  • Messerli FH, Williams B, Ritz E. 2007. Essential hypertension. Lancet 370:591–603. http://dx.doi.org/10.1016/S0140-6736(07)61299-9.
  • Wu Y, Huxley R, Li L, Anna V, Xie G, Yao C, Woodward M, Li X, Chalmers J, Gao R, Kong L, Yang X, China NNHS Steering Committee, China NNHS Working Group. 2008. Prevalence, awareness, treatment, and control of hypertension in China: data from the China National Nutrition and Health Survey 2002. Circulation 118:2679–2686. http://dx.doi.org/10.1161/CIRCULATIONAHA.108.788166.
  • Lifton RP, Gharavi AG, Geller DS. 2001. Molecular mechanisms of human hypertension. Cell 104:545–556. http://dx.doi.org/10.1016/S0092-8674(01)00241-0.
  • Dromparis P, Michelakis ED. 2013. Mitochondria in vascular health and disease. Annu Rev Physiol 75:95–126. http://dx.doi.org/10.1146/annurev-physiol-030212-183804.
  • Wilson FH, Hariri A, Farhi A, Zhao H, Petersen KF, Toka HR, Nelson-Williams C, Raja KM, Kashgarian M, Shulman GI, Scheinman SJ, Lifton RP. 2004. A cluster of metabolic defects caused by mutation in a mitochondrial tRNA. Science 306:1190–1194. http://dx.doi.org/10.1126/science.1102521.
  • Marian AJ. 2011. Mitochondrial genetics and human systemic hypertension. Circ Res 108:784–786. http://dx.doi.org/10.1161/CIRCRESAHA.111.242768.
  • Andrews RM, Kubacka I, Chinnery PF, Lightowlers RN, Turnbull DM, Howell N. 1999. Reanalysis and revision of the Cambridge reference sequence for human mitochondrial DNA. Nat Genet 23:147. http://dx.doi.org/10.1038/13779.
  • Ojala D, Montoya J, Attardi G. 1981. tRNA punctuation model of RNA processing in human mitochondria. Nature 290:470–474. http://dx.doi.org/10.1038/290470a0.
  • Guan MX, Enriquez JA, Fischel-Ghodsian N, Puranam RS, Lin CP, Maw MA, Attardi G. 1998. The deafness-associated mitochondrial DNA mutation at position 7445, which affects tRNASer(UCN) precursor processing, has long-range effects on NADH dehydrogenase subunit ND6 gene expression. Mol Cell Biol 18:5868–5879. http://dx.doi.org/10.1128/MCB.18.10.5868.
  • Abbott JA, Francklyn CS, Robey-Bond SM. 2014. Transfer RNA and human disease. Front Genet 5:158. http://dx.doi.org/10.3389/fgene.2014.00158.
  • Ruiz-Pesini E, Wallace DC. 2006. Evidence for adaptive selection acting on the tRNA and rRNA genes of human mitochondrial DNA. Hum Mutat 27:1072–1081. http://dx.doi.org/10.1002/humu.20378.
  • Qin Y, Xue L, Jiang P, Xu M, He Y, Shi S, Huang Y, He J, Mo JQ, Guan MX. 2014. Mitochondrial tRNA variants in Chinese subjects with coronary heart disease. J Am Heart Assoc 3:e000437. http://dx.doi.org/10.1161/JAHA.113.000437.
  • Li R, Liu Y, Li Z, Yang L, Wang S, Guan MX. 2009. Failures in mitochondrial tRNAMet and tRNAGln metabolism caused by the novel 4401A>G mutation are involved in essential hypertension in a Han Chinese family. Hypertension 54:329–337. http://dx.doi.org/10.1161/HYPERTENSIONAHA.109.129270.
  • Liu Y, Li R, Li Z, Wang XJ, Yang L, Wang S, Guan MX. 2009. Mitochondrial transfer RNAMet 4435A>G mutation is associated with maternally inherited hypertension in a Chinese pedigree. Hypertension 53:1083–1090. http://dx.doi.org/10.1161/HYPERTENSIONAHA.109.128702.
  • Wang S, Li R, Fettermann A, Li Z, Qian Y, Liu Y, Wang X, Zhou A, Mo JQ, Yang L, Jiang P, Taschner A, Rossmanith W, Guan MX. 2011. Maternally inherited essential hypertension is associated with the novel 4263A>G mutation in the mitochondrial tRNAIle gene in a large Han Chinese family. Circ Res 108:862–870. http://dx.doi.org/10.1161/CIRCRESAHA.110.231811.
  • Li Z, Liu Y, Yang L, Wang S, Guan MX. 2008. Maternally inherited hypertension is associated with the mitochondrial tRNAIle A4295G mutation in a Chinese family. Biochem Biophys Res Commun 367:906–911. http://dx.doi.org/10.1016/j.bbrc.2007.12.150.
  • Suzuki T, Nagao A. 2011. Human mitochondrial tRNAs: biogenesis, function, structural aspects, and diseases. Annu Rev Genet 45:299–329. http://dx.doi.org/10.1146/annurev-genet-110410-132531.
  • Zheng J, Ji Y, Guan MX. 2012. Mitochondrial tRNA mutations associated with deafness. Mitochondrion 12:406–413. http://dx.doi.org/10.1016/j.mito.2012.04.001.
  • Holzmann J, Frank P, Loffler E, Bennett KL, Gerner C, Rossmanith W. 2008. RNase P without RNA: identification and functional reconstitution of the human mitochondrial tRNA processing enzyme. Cell 135:462–474. http://dx.doi.org/10.1016/j.cell.2008.09.013.
  • Qu J, Li R, Zhou X, Tong Y, Lu F, Qian Y, Hu Y, Mo JQ, West CE, Guan MX. 2006. The novel A4435G mutation in the mitochondrial tRNAMet may modulate the phenotypic expression of the LHON-associated ND4 G11778A mutation in a Chinese family. Invest Ophthalmol Vis Sci 47:475–483. http://dx.doi.org/10.1167/iovs.05-0665.
  • Suzuki T, Suzuki T. 2014. A complete landscape of post-transcriptional modifications in mammalian mitochondrial tRNAs. Nucleic Acids Res 42:7346–7357. http://dx.doi.org/10.1093/nar/gku390.
  • Mercer TR, Neph S, Dinger ME, Crawford J, Smith MA, Shearwood AM, Haugen E, Bracken CP, Rackham O, Stamatoyannopoulos JA, Filipovska A, Mattick JS. 2011. The human mitochondrial transcriptome. Cell 146:645–658. http://dx.doi.org/10.1016/j.cell.2011.06.051.
  • Hällberg BM, Larsson NG. 2014. Making proteins in the powerhouse. Cell Metab 20:226–240. http://dx.doi.org/10.1016/j.cmet.2014.07.001.
  • King MP, Attardi G. 1996. Mitochondria-mediated transformation of human rho(0) cells. Methods Enzymol 264:313–334. http://dx.doi.org/10.1016/S0076-6879(96)64030-0.
  • Guan MX, Fischel-Ghodsian N, Attardi G. 2001. Nuclear background determines biochemical phenotype in the deafness-associated mitochondrial 12S rRNA mutation. Hum Mol Genet 10:573–580. http://dx.doi.org/10.1093/hmg/10.6.573.
  • Qiu Q, Li R, Jiang P, Xue L, Lu Y, Song Y, Han J, Lu Z, Zhi S, Mo JQ, Guan MX. 2012. Mitochondrial tRNA mutations are associated with maternally inherited hypertension in two Han Chinese pedigrees. Hum Mutat 33:1285–1293. http://dx.doi.org/10.1002/humu.22109.
  • Lu Z, Chen H, Meng Y, Wang Y, Xue L, Zhi S, Qiu Q, Yang L, Mo JQ, Guan MX. 2011. The tRNAMet 4435A>G mutation in the mitochondrial haplogroup G2a1 is responsible for maternally inherited hypertension in a Chinese pedigree. Eur J Hum Genet 19:1181–1186. http://dx.doi.org/10.1038/ejhg.2011.111.
  • Joint National Committee on Prevention Detection Evaluation and Treatment of High Blood pressure. 1997. The sixth report of the Joint National Committee on prevention, detection, evaluation and treatment of high blood pressure. Arch Intern Med 157:2413–2446. http://dx.doi.org/10.1001/archinte.1997.00440420033005.
  • Rieder MJ, Taylor SL, Tobe VO, Nickerson DA. 1998. Automating the identification of DNA variations using quality-based fluorescence re-sequencing: analysis of the human mitochondrial genome. Nucleic Acids Res 26:967–973. http://dx.doi.org/10.1093/nar/26.4.967.
  • Miller G, Lipman M. 1973. Release of infectious Epstein-Barr virus by transformed marmoset leukocytes. Proc Natl Acad Sci U S A 70:190–194. http://dx.doi.org/10.1073/pnas.70.1.190.
  • King MP, Attardi G. 1993. Post-transcriptional regulation of the steady-state levels of mitochondrial tRNAs in HeLa cells. J Biol Chem 268:10228–10237.
  • Gong S, Peng Y, Jiang P, Wang M, Fan M, Wang X, Zhou H, Li H, Yan Q, Huang T, Guan MX. 2014. A deafness-associated tRNAHis mutation alters the mitochondrial function, ROS production and membrane potential. Nucleic Acids Res 42:8039–8048. http://dx.doi.org/10.1093/nar/gku466.
  • Li X, Fischel-Ghodsian N, Schwartz F, Yan Q, Friedman RA, Guan MX. 2004. Biochemical characterization of the mitochondrial tRNASer(UCN) T7511C mutation associated with nonsyndromic deafness. Nucleic Acids Res 32:867–877. http://dx.doi.org/10.1093/nar/gkh226.
  • Jiang P, Jin X, Peng Y, Wang M, Liu H, Liu X, Zhang Z, Ji Y, Zhang J, Liang M, Zhao F, Sun YH, Zhang M, Zhou X, Chen Y, Mo JQ, Huang T, Qu J, Guan MX. 2016. The exome sequencing identified the mutation in YARS2 encoding the mitochondrial tyrosyl-tRNA synthetase as a nuclear modifier for the phenotypic manifestation of Leber's hereditary optic neuropathy-associated mitochondrial DNA mutation. Hum Mol Genet 25:584–596. http://dx.doi.org/10.1093/hmg/ddv498.
  • Enriquez JA, Attardi G. 1996. Analysis of aminoacylation of human mitochondrial tRNAs. Methods Enzymol 264:183–196. http://dx.doi.org/10.1016/S0076-6879(96)64019-1.
  • Enriquez JA, Chomyn A, Attardi G. 1995. MtDNA mutation in MERRF syndrome causes defective aminoacylation of tRNALys and premature translation termination. Nat Genet 10:47–55. http://dx.doi.org/10.1038/ng0595-47.
  • Dranka BP, Benavides GA, Diers AR, Giordano S, Zelickson BR, Reily C, Zou L, Chatham JC, Hill BG, Zhang J, Landar A, Darley-Usmar VM. 2011. Assessing bioenergetic function in response to oxidative stress by metabolic profiling. Free Radic Biol Med 51:1621–1635. http://dx.doi.org/10.1016/j.freeradbiomed.2011.08.005.
  • Birch-Machin MA, Turnbull DM. 2001. Assaying mitochondrial respiratory complex activity in mitochondria isolated from human cells and tissues. Methods Cell Biol 65:97–117. http://dx.doi.org/10.1016/S0091-679X(01)65006-4.
  • Zhang J, Jiang P, Jin X, Liu X, Zhang M, Xie S, Gao M, Zhang S, Sun YH, Zhu J, Ji Y, Wei QP, Tong Y, Guan MX. 2014. Leber's hereditary optic neuropathy caused by the homoplasmic ND1 m.3635G>A mutation in nine Han Chinese families. Mitochondrion 18:18–26. http://dx.doi.org/10.1016/j.mito.2014.08.008.
  • Yu J, Zheng J, Zhao X, Liu J, Mao Z, Ling Y, Chen D, Chen C, Hui L, Cui L, Chen Y, Jiang P, Guan MX. 2014. Aminoglycoside stress together with the 12S rRNA 1494C>T mutation leads to mitophagy. PLoS One 9:e114650. http://dx.doi.org/10.1371/journal.pone.0114650.
  • Mukhopadhyay P, Rajesh M, Haskó G, Hawkins BJ, Madesh M, Pacher P. 2007. Simultaneous detection of apoptosis and mitochondrial superoxide production in live cells by flow cytometry and confocal microscopy. Nat Protoc 2:2295–2301. http://dx.doi.org/10.1038/nprot.2007.327.
  • Kong QP, Bandelt HJ, Sun C, Yao YG, Salas A, Achilli A, Wang CY, Zhong L, Zhu CL, Wu SF, Torroni A, Zhang YP. 2006. Updating the East Asian mtDNA phylogeny: a prerequisite for the identification of pathogenic mutations. Hum Mol Genet 15:2076–2086. http://dx.doi.org/10.1093/hmg/ddl130.
  • Zhou X, Qian Y, Zhang J, Tong Y, Jiang P, Liang M, Dai X, Zhou H, Zhao F, Ji Y, Mo JQ, Qu J, Guan MX. 2012. Leber's hereditary optic neuropathy is associated with the T3866C mutation in mitochondrial ND1 gene in three Han Chinese families. Invest Ophthalmol Vis Sci 53:4586–4594. http://dx.doi.org/10.1167/iovs.11-9109.
  • Florentz C, Sohm B, Tryoen-Toth P, Putz J, Sissler M. 2003. Human mitochondrial tRNAs in health and disease. Cell Mol Life Sci 60:1356–1375. http://dx.doi.org/10.1007/s00018-003-2343-1.
  • Lovato MA, Chihade JW, Schimmel P. 2001. Translocation within the acceptor helix of a major tRNA identity determinant. EMBO J 20:4846–4853. http://dx.doi.org/10.1093/emboj/20.17.4846.
  • Giege R, Sissler M, Florentz C. 1998. Universal rules and idiosyncratic features in tRNA identity. Nucleic Acids Res 26:5017–5035. http://dx.doi.org/10.1093/nar/26.22.5017.
  • Jia Z, Wang X, Qin Y, Xue L, Jiang P, Meng Y, Shi S, Wang Y, Mo J, Guan MX. 2013. Coronary heart disease is associated with a mutation in mitochondrial tRNA. Hum Mol Genet 22:4064–4073. http://dx.doi.org/10.1093/hmg/ddt256.
  • Wang X, Lu J, Zhu Y, Yang A, Yang L, Li R, Chen B, Qian Y, Tang X, Wang J, Zhang X, Guan MX. 2008. Mitochondrial tRNAThr G15927A mutation may modulate the phenotypic manifestation of ototoxic 12S rRNA A1555G mutation in four Chinese families. Pharmacogenet Genomics 18:1059–1070. http://dx.doi.org/10.1097/FPC.0b013e3283131661.
  • Li R, Guan MX. 2010. Human mitochondrial leucyl-tRNA synthetase corrects mitochondrial dysfunctions due to the tRNALeu(UUR) A3243G mutation, associated with mitochondrial encephalomyopathy, lactic acidosis, and stroke-like symptoms and diabetes. Mol Cell Biol 30:2147–2154. http://dx.doi.org/10.1128/MCB.01614-09.
  • Scheffler IE. 2015. Mitochondrial disease associated with complex I (NADH-CoQ oxidoreductase) deficiency. J Inherit Metab Dis 38:405–415. http://dx.doi.org/10.1007/s10545-014-9768-6.
  • Wallace DC. 2005. A mitochondrial paradigm of metabolic and degenerative diseases, aging, and cancer: a dawn for evolutionary medicine. Annu Rev Genet 39:359–407. http://dx.doi.org/10.1146/annurev.genet.39.110304.095751.
  • de Andrade PB, Rubi B, Frigerio F, van den Ouweland JM, Maassen JA, Maechler P. 2006. Diabetes-associated mitochondrial DNA mutation A3243G impairs cellular metabolic pathways necessary for beta cell function. Diabetologia 49:1816–1826. http://dx.doi.org/10.1007/s00125-006-0301-9.
  • St-Pierre J, Buckingham JA, Roebuck SJ, Brand MD. 2002. Topology of superoxide production from different sites in the mitochondrial electron transport chain. J Biol Chem 277:44784–44790. http://dx.doi.org/10.1074/jbc.M207217200.
  • Addabbo F, Montagnani M, Goligorsky MS. 2009. Mitochondria and reactive oxygen species. Hypertension 53:885–892. http://dx.doi.org/10.1161/HYPERTENSIONAHA.109.130054.
  • Eirin A, Lerman A, Lerman LO. 2015. Mitochondria: a pathogenic paradigm in hypertensive renal disease. Hypertension 65:264–270. http://dx.doi.org/10.1161/HYPERTENSIONAHA.114.04598.
  • Raimundo N, Song L, Shutt TE, McKay SE, Cotney J, Guan MX, Gilliland TC, Hohuan D, Santos-Sacchi J, Shadel GS. 2012. Mitochondrial stress engages E2F1 apoptotic signaling to cause deafness. Cell 148:716–726. http://dx.doi.org/10.1016/j.cell.2011.12.027.
  • Vasan RS, Beiser A, Seshadri S, Larson MG, Kannel WB, D'Agostino RB, Levy D. 2002. Residual lifetime risk for developing hypertension in middle-aged women and men: The Framingham Heart Study. JAMA 287:1003–1010.
  • Archer SL, Marsboom G, Kim GH, Zhang HJ, Toth PT, Svensson EC, Dyck JR, Gomberg-Maitland M, Thebaud B, Husain AN, Cipriani N, Rehman J. 2010. Epigenetic attenuation of mitochondrial superoxide dismutase 2 in pulmonary arterial hypertension: a basis for excessive cell proliferation and a new therapeutic target. Circulation 121:2661–2671. http://dx.doi.org/10.1161/CIRCULATIONAHA.109.916098.
  • Dittmar KA, Goodenbour JM, Pan T. 2006. Tissue-specific differences in human transfer RNA expression. PLoS Genet 2:e221. http://dx.doi.org/10.1371/journal.pgen.0020221.

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