La Deletion from Mouse Brain Alters Pre-tRNA Metabolism and Accumulation of Pre-5.8S rRNA, with Neuron Death and Reactive Astrocytosis

REFERENCES

• Lerner MR, Boyle JA, Hardin JA, Steitz JA. 1981. Two novel classes of small ribo-nucleoproteins detected by antibodies associated with lupus erythematosus. Science 211:400–402. https://doi.org/10.1126/science.6164096.
   PubMed Web of Science ®Google Scholar
• Bousquet-Antonelli C, Deragon JM. 2009. A comprehensive analysis of the La-motif protein superfamily. RNA 15:750–764. https://doi.org/10.1261/rna.1478709.
   PubMed Web of Science ®Google Scholar
• Rinke J, Steitz JA. 1982. Precursor molecules of both human 5S ribosomal RNA and tRNAs are bound by a cellular protein reactive with anti-La lupus antibodies. Cell 29:149–159. https://doi.org/10.1016/0092-8674(82)90099-X.
   PubMed Web of Science ®Google Scholar
• Stefano JE. 1984. Purified lupus antigen La recognizes an oligouridylate stretch common to the 3′ termini of RNA polymerase III transcripts. Cell 36:145–154. https://doi.org/10.1016/0092-8674(84)90083-7.
   PubMed Web of Science ®Google Scholar
• Teplova M, Yuan Y-R, Ilin S, Malinina L, Phan AT, Teplov A, Patel DJ. 2006. Structural basis for recognition and sequestration of UUU-OH 3′-termini of nascent RNA pol III transcripts by La, a rheumatic disease autoantigen. Mol Cell 21:75–85. https://doi.org/10.1016/j.molcel.2005.10.027.
   PubMed Web of Science ®Google Scholar
• Bayfield MA, Kaiser TE, Intine RV, Maraia RJ. 2007. Conservation of a masked nuclear export activity of La proteins and its effects on tRNA maturation. Mol Cell Biol 27:3303–3312. https://doi.org/10.1128/MCB.00026-07.
   PubMed Web of Science ®Google Scholar
• Bayfield MA, Yang R, Maraia R. 2010. Conserved and divergent features of structure and function of La and La-related proteins (LARPs). Biochim Biophys Acta 1799:365–378. https://doi.org/10.1016/j.bbagrm.2010.01.011.
   PubMed Web of Science ®Google Scholar
• Chakshusmathi G, Kim SD, Rubinson DA, Wolin SL. 2003. A La protein requirement for efficient pre-tRNA folding. EMBO J 22:6562–6572. https://doi.org/10.1093/emboj/cdg625.
   PubMed Web of Science ®Google Scholar
• Copela LA, Chakshusmathi G, Sherrer RL, Wolin SL. 2006. The La protein functions redundantly with tRNA modification enzymes to ensure tRNA structural stability. RNA 12:644–654. https://doi.org/10.1261/rna.2307206.
   PubMed Web of Science ®Google Scholar
• Huang Y, Bayfield MA, Intine RV, Maraia RJ. 2006. Separate RNA-binding surfaces on the multifunctional La protein mediate distinguishable activities in tRNA maturation. Nat Struct Mol Biol 13:611–618. https://doi.org/10.1038/nsmb1110.
   PubMed Web of Science ®Google Scholar
• Intine RV, Dundr M, Misteli T, Maraia RJ. 2002. Aberrant nuclear trafficking of La protein leads to disordered processing of associated precursor tRNAs. Mol Cell 9:1113–1123. https://doi.org/10.1016/S1097-2765(02)00533-6.
   PubMed Web of Science ®Google Scholar
• Intine RVA, Sakulich AL, Koduru SB, Huang Y, Pierstorrf E, Goodier JL, Phan L, Maraia RJ. 2000. Control of transfer RNA maturation by phosphorylation of the human La antigen on serine 366. Mol Cell 6:339–348. https://doi.org/10.1016/S1097-2765(00)00034-4.
   PubMed Web of Science ®Google Scholar
• Maraia RJ. 2001. La protein and the trafficking of nascent RNA polymerase III transcripts. J Cell Biol 153:F13–F17. https://doi.org/10.1083/jcb.153.4.F13.
   PubMedGoogle Scholar
• Wolin SL, Cedervall T. 2002. The La protein. Annu Rev Biochem 71:375–403. https://doi.org/10.1146/annurev.biochem.71.090501.150003.
   PubMed Web of Science ®Google Scholar
• Yoo CJ, Wolin SL. 1997. The yeast La protein is required for the 3′ endonucleolytic cleavage that matures tRNA precursors. Cell 89:393–402. https://doi.org/10.1016/S0092-8674(00)80220-2.
   PubMed Web of Science ®Google Scholar
• Kucera NJ, Hodsdon ME, Wolin SL. 2011. An intrinsically disordered C terminus allows the La protein to assist the biogenesis of diverse noncoding RNA precursors. Proc Natl Acad Sci U S A 108:1308–1313. https://doi.org/10.1073/pnas.1017085108.
   PubMed Web of Science ®Google Scholar
• Wolin SL, Wurtmann EJ. 2006. Molecular chaperones and quality control in noncoding RNA biogenesis. Cold Spring Harbor Symp Quant Biol 71:505–511. https://doi.org/10.1101/sqb.2006.71.051.
   PubMedGoogle Scholar
• Bayfield MA, Maraia RJ. 2009. Precursor-product discrimination by La protein during tRNA metabolism. Nat Struct Mol Biol 16:430–437. https://doi.org/10.1038/nsmb.1573.
   PubMed Web of Science ®Google Scholar
• Copela LA, Fernandez CF, Sherrer RL, Wolin SL. 2008. Competition between the Rex1 exonuclease and the La protein affects both Trf4p-mediated RNA quality control and pre-tRNA maturation. RNA 14:1214–1227. https://doi.org/10.1261/rna.1050408.
   PubMed Web of Science ®Google Scholar
• Bai C, Tolias PP. 2000. Genetic analysis of a La homolog in Drosophila melanogaster. Nucleic Acids Res 28:1078–1084. https://doi.org/10.1093/nar/28.5.1078.
   PubMed Web of Science ®Google Scholar
• Park JM, Kohn MJ, Bruinsma MW, Vech C, Intine RV, Fuhrmann S, Grinberg A, Mukherjee I, Love PE, Ko MS, DePamphilis ML, Maraia RJ. 2006. The multifunctional RNA-binding protein La is required for mouse development and for the establishment of embryonic stem cells. Mol Cell Biol 26:1445–1451. https://doi.org/10.1128/MCB.26.4.1445-1451.2006.
   PubMed Web of Science ®Google Scholar
• Ali N, Pruijn GJ, Kenan DJ, Keene JD, Siddiqui A. 2000. Human La antigen is required for the hepatitis C virus internal ribosome entry site (IRES)-mediated translation. J Biol Chem 275:27531–27540.
   PubMed Web of Science ®Google Scholar
• Brenet F, Dussault N, Borch J, Ferracci G, Delfino C, Roepstorff P, Miquelis R, Ouafik L. 2005. Mammalian peptidylglycine alpha-amidating monooxygenase mRNA expression can be modulated by the La autoantigen. Mol Cell Biol 25:7505–7521. https://doi.org/10.1128/MCB.25.17.7505-7521.2005.
   PubMed Web of Science ®Google Scholar
• Cardinali B, Carissimi C, Gravina P, Pierandrei-Amaldi P. 2003. La protein is associated with terminal oligopyrimidine mRNAs in actively translating polysomes. J Biol Chem 278:35145–35151. https://doi.org/10.1074/jbc.M300722200.
   PubMed Web of Science ®Google Scholar
• Costa-Mattioli M, Svitkin Y, Sonenberg N. 2004. La autoantigen is necessary for optimal function of the poliovirus and hepatitis C virus internal ribosome entry site in vivo and in vitro. Mol Cell Biol 24:6861–6870. https://doi.org/10.1128/MCB.24.15.6861-6870.2004.
   PubMed Web of Science ®Google Scholar
• Crosio C, Boyl PP, Loreni F, Pierandrei-Amaldi P, Amaldi F. 2000. La protein has a positive effect on the translation of TOP mRNAs in vivo. Nucleic Acids Res 28:2927–2934. https://doi.org/10.1093/nar/28.15.2927.
   PubMed Web of Science ®Google Scholar
• Intine RV, Tenenbaum SA, Sakulich AS, Keene JD, Maraia RJ. 2003. Differential phosphorylation and subcellular localization of La RNPs associated with precursor tRNAs and translation-related mRNAs. Mol Cell 12:1301–1307. https://doi.org/10.1016/S1097-2765(03)00429-5.
   PubMed Web of Science ®Google Scholar
• Meerovitch K, Svitkin YV, Lee HS, Lejbkowicz F, Kenan DJ, Chan EK, Agol VI, Keene JD, Sonenberg N. 1993. La autoantigen enhances and corrects aberrant translation of poliovirus RNA in reticulocyte lysate. J Virol 67:3798–3807.
   PubMed Web of Science ®Google Scholar
• Pudi R, Abhiman S, Srinivasan N, Das S. 2003. Hepatitis C virus internal ribosome entry site-mediated translation is stimulated by specific interaction of independent regions of human La autoantigen. J Biol Chem 278:12231–12240. https://doi.org/10.1074/jbc.M210287200.
   PubMedGoogle Scholar
• Schwartz E, Intine RV, Maraia RJ. 2004. CK2 is responsible for phosphorylation of human La protein serine-366 and can modulate 5′TOP mRNA metabolism. Mol Cell Biol 24:9580–9591. https://doi.org/10.1128/MCB.24.21.9580-9591.2004.
   PubMed Web of Science ®Google Scholar
• Svitkin YV, Ovchinnikov LP, Dreyfuss G, Sonenberg N. 1996. General RNA binding proteins render translation cap dependent. EMBO J 15:7147–7155.
   PubMed Web of Science ®Google Scholar
• Ohndorf UM, Steegborn C, Knijff R, Sondermann P. 2001. Contributions of the individual domains in La protein to its RNA 3′-end binding activity. J Biol Chem 276:27188–27196. https://doi.org/10.1074/jbc.M102891200.
   PubMed Web of Science ®Google Scholar
• Yoo CJ, Wolin SL. 1994. La proteins from Drosophila melanogaster and Saccharomyces cerevisiae: a yeast homolog of the La autoantigen is dispensable for growth. Mol Cell Biol 14:5412–5424. https://doi.org/10.1128/MCB.14.8.5412.
   PubMed Web of Science ®Google Scholar
• Martino L, Pennell S, Kelly G, Bui TT, Kotik-Kogan O, Smerdon SJ, Drake AF, Curry S, Conte MR. 2012. Analysis of the interaction with the hepatitis C virus mRNA reveals an alternative mode of RNA recognition by the human La protein. Nucleic Acids Res 40:1381–1394. https://doi.org/10.1093/nar/gkr890.
   PubMed Web of Science ®Google Scholar
• Gottlieb E, Steitz JA. 1989. The RNA binding protein La influences both the accuracy and the efficiency of RNA polymerase III transcription in vitro. EMBO J 8:841–850.
   PubMedGoogle Scholar
• Intine RV, Dundr M, Vassilev A, Schwartz E, Zhao Y, Depamphilis ML, Maraia RJ. 2004. Nonphosphorylated human La antigen interacts with nucleolin at nucleolar sites involved in rRNA biogenesis. Mol Cell Biol 24:10894–10904. https://doi.org/10.1128/MCB.24.24.10894-10904.2004.
   PubMed Web of Science ®Google Scholar
• Sommer G, Dittmann J, Kuehnert J, Reumann K, Schwartz PE, Will H, Coulter BL, Smith MT, Heise T. 2011. The RNA-binding protein La contributes to cell proliferation and CCND1 expression. Oncogene 30:434–444. https://doi.org/10.1038/onc.2010.425.
   PubMed Web of Science ®Google Scholar
• Tang J, Zhang ZH, Huang M, Heise T, Zhang J, Liu GL. 2013. Phosphorylation of human La protein at Ser 366 by casein kinase II contributes to hepatitis B virus replication and expression in vitro. J Viral Hepat 20:24–33. https://doi.org/10.1111/j.1365-2893.2012.01636.x.
   PubMed Web of Science ®Google Scholar
• Brenet F, Socci N, Sonenberg N, Holland E. 2009. Akt phosphorylation of La regulates specific mRNA translation in glial progenitors. Oncogene 28:128–139. https://doi.org/10.1038/onc.2008.376.
   PubMed Web of Science ®Google Scholar
• Kuehnert J, Sommer G, Zierk AW, Fedarovich A, Brock A, Fedarovich D, Heise T. 2015. Novel RNA chaperone domain of RNA-binding protein La is regulated by AKT phosphorylation. Nucleic Acids Res 43:581–594. https://doi.org/10.1093/nar/gku1309.
   PubMed Web of Science ®Google Scholar
• Fan H, Sakulich AL, Goodier JL, Zhang X, Qin J, Maraia RJ. 1997. Phosphorylation of the human La antigen on serine 366 can regulate recycling of RNA polymerase III transcription complexes. Cell 88:707–715. https://doi.org/10.1016/S0092-8674(00)81913-3.
   PubMed Web of Science ®Google Scholar
• Allain FH, Bouvet P, Dieckmann T, Feigon J. 2000. Molecular basis of sequence-specific recognition of pre-ribosomal RNA by nucleolin. EMBO J 19:6870–6881. https://doi.org/10.1093/emboj/19.24.6870.
   PubMed Web of Science ®Google Scholar
• Ginisty H, Amalric F, Bouvet P. 1998. Nucleolin functions in the first step of ribosomal RNA processing. EMBO J 17:1476–1486. https://doi.org/10.1093/emboj/17.5.1476.
   PubMed Web of Science ®Google Scholar
• Ginisty H, Sicard H, Roger B, Bouvet P. 1999. Structure and functions of nucleolin. J Cell Sci 112:761–772.
   PubMed Web of Science ®Google Scholar
• Gerbi SA, Borovjagin AV, Lange TS. 2003. The nucleolus: a site of ribonucleoprotein maturation. Curr Opin Cell Biol 15:318–325. https://doi.org/10.1016/S0955-0674(03)00049-8.
   PubMed Web of Science ®Google Scholar
• Gaidamakov S, Maximova OA, Chon H, Blewett NH, Wang H, Crawford AK, Day A, Tulchin N, Crouch RJ, Morse HC, III, Blitzer RD, Maraia RJ. 2014. Targeted deletion of the gene encoding the La protein SSB autoantigen in B cells or cerebral cortex causes extensive tissue loss. Mol Cell Biol 34:123–131. https://doi.org/10.1128/MCB.01010-13.
   PubMed Web of Science ®Google Scholar
• Maraia RJ, Lamichhane TN. 2011. 3′ Processing of eukaryotic precursor tRNAs. WIRES RNA 2:362–375. https://doi.org/10.1002/wrna.64.
   Google Scholar
• Hanada T, Weitzer S, Mair B, Bernreuther C, Wainger BJ, Ichida J, Hanada R, Orthofer M, Cronin SJ, Komnenovic V, Minis A, Sato F, Mimata H, Yoshimura A, Tamir I, Rainer J, Kofler R, Yaron A, Eggan KC, Woolf CJ, Glatzel M, Herbst R, Martinez J, Penninger JM. 2013. CLP1 links tRNA metabolism to progressive motor-neuron loss. Nature 495:474–480. https://doi.org/10.1038/nature11923.
   PubMed Web of Science ®Google Scholar
• Ishimura R, Nagy G, Dotu I, Zhou H, Yang XL, Schimmel P, Senju S, Nishimura Y, Chuang JH, Ackerman SL. 2014. RNA function. Ribosome stalling induced by mutation of a CNS-specific tRNA causes neurodegeneration. Science 345:455–459. https://doi.org/10.1126/science.1249749.
   PubMed Web of Science ®Google Scholar
• Thiffault I, Wolf NI, Forget D, Guerrero K, Tran LT, Choquet K, Lavallee-Adam M, Poitras C, Brais B, Yoon G, Sztriha L, Webster RI, Timmann D, van de Warrenburg BP, Seeger J, Zimmermann A, Mate A, Goizet C, Fung E, van der Knaap MS, Fribourg S, Vanderver A, Simons C, Taft RJ, Yates JR, III, Coulombe B, Bernard G. 2015. Recessive mutations in POLR1C cause a leukodystrophy by impairing biogenesis of RNA polymerase III. Nat Commun 6:7623. https://doi.org/10.1038/ncomms8623.
   PubMed Web of Science ®Google Scholar
• Arimbasseri AG, Maraia RJ. 2016. RNA Polymerase III advances: structural and tRNA functional views. Trends Biochem Sci 41:546–559. https://doi.org/10.1016/j.tibs.2016.03.003.
   PubMed Web of Science ®Google Scholar
• Watkins NJ, Lemm I, Ingelfinger D, Schneider C, Hossbach M, Urlaub H, Luhrmann R. 2004. Assembly and maturation of the U3 snoRNP in the nucleoplasm in a large dynamic multiprotein complex. Mol Cell 16:789–798. https://doi.org/10.1016/j.molcel.2004.11.012.
   PubMed Web of Science ®Google Scholar
• Watkins NJ, Lemm I, Luhrmann R. 2007. Involvement of nuclear import and export factors in U8 box C/D snoRNP biogenesis. Mol Cell Biol 27:7018–7027. https://doi.org/10.1128/MCB.00516-07.
   PubMedGoogle Scholar
• Mullineux ST, Lafontaine DL. 2012. Mapping the cleavage sites on mammalian pre-rRNAs: where do we stand? Biochimie 94:1521–1532. https://doi.org/10.1016/j.biochi.2012.02.001.
   PubMed Web of Science ®Google Scholar
• Peculis BA, Steitz JA. 1993. Disruption of U8 nucleolar snRNA inhibits 5.8S and 28S rRNA processing in the Xenopus oocyte. Cell 73:1233–1245. https://doi.org/10.1016/0092-8674(93)90651-6.
   PubMed Web of Science ®Google Scholar
• Farrar JE, Nater M, Caywood E, McDevitt MA, Kowalski J, Takemoto CM, Talbot CC, Jr, Meltzer P, Esposito D, Beggs AH, Schneider HE, Grabowska A, Ball SE, Niewiadomska E, Sieff CA, Vlachos A, Atsidaftos E, Ellis SR, Lipton JM, Gazda HT, Arceci RJ. 2008. Abnormalities of the large ribosomal subunit protein, Rpl35a, in Diamond-Blackfan anemia. Blood 112:1582–1592. https://doi.org/10.1182/blood-2008-02-140012.
   PubMed Web of Science ®Google Scholar
• Wang X, Zhang C, Szabo G, Sun QQ. 2013. Distribution of CaMKIIalpha expression in the brain in vivo, studied by CaMKIIalpha-GFP mice. Brain Res 1518:9–25. https://doi.org/10.1016/j.brainres.2013.04.042.
   PubMedGoogle Scholar
• Lerner EA, Lerner MR, Janeway CA, Jr, Steitz JA. 1981. Monoclonal antibodies to nucleic acid-containing cellular constituents: probes for molecular biology and autoimmune disease. Proc Natl Acad Sci U S A 78:2737–2741. https://doi.org/10.1073/pnas.78.5.2737.
   PubMed Web of Science ®Google Scholar
• Mili S, Steitz JA. 2004. Evidence for reassociation of RNA-binding proteins after cell lysis: implications for the interpretation of immunoprecipitation analyses. RNA 10:1692–1694. https://doi.org/10.1261/rna.7151404.
   PubMed Web of Science ®Google Scholar
• Mazan S, Bachellerie JP. 1988. Structure and organization of mouse U3B RNA functional genes. J Biol Chem 263:19461–19467.
   PubMedGoogle Scholar
• Tyc K, Steitz JA. 1992. A new interaction between the mouse 5′ external transcribed spacer of pre-rRNA and U3 snRNA detected by psoralen crosslinking. Nucleic Acids Res 20:5375–5382. https://doi.org/10.1093/nar/20.20.5375.
   PubMed Web of Science ®Google Scholar
• Phizicky EM, Hopper AK. 2010. tRNA biology charges to the front. Genes Dev 24:1832–1860. https://doi.org/10.1101/gad.1956510.
   PubMed Web of Science ®Google Scholar
• Walsh JG, Muruve DA, Power C. 2014. Inflammasomes in the CNS. Nat Rev Neurosci 15:84–97. https://doi.org/10.1038/nrn3638.
   PubMed Web of Science ®Google Scholar
• Liu XB, Jones EG. 1996. Localization of alpha type II calcium calmodulin-dependent protein kinase at glutamatergic but not gamma-aminobutyric acid (GABAergic) synapses in thalamus and cerebral cortex. Proc Natl Acad Sci U S A 93:7332–7336. https://doi.org/10.1073/pnas.93.14.7332.
   PubMed Web of Science ®Google Scholar
• Arvieux J, Yssel H, Colomb MG. 1988. Antigen-bound C3b and C4b enhance antigen-presenting cell function in activation of human T-cell clones. Immunology 65:229–235.
   PubMed Web of Science ®Google Scholar
• Bryan KJ, Zhu X, Harris PL, Perry G, Castellani RJ, Smith MA, Casadesus G. 2008. Expression of CD74 is increased in neurofibrillary tangles in Alzheimer's disease. Mol Neurodegener 3:13. https://doi.org/10.1186/1750-1326-3-13.
   PubMedGoogle Scholar
• Lotteau V, Teyton L, Peleraux A, Nilsson T, Karlsson L, Schmid SL, Quaranta V, Peterson PA. 1990. Intracellular transport of class II MHC molecules directed by invariant chain. Nature 348:600–605. https://doi.org/10.1038/348600a0.
   PubMed Web of Science ®Google Scholar
• Morris P, Shaman J, Attaya M, Amaya M, Goodman S, Bergman C, Monaco JJ, Mellins E. 1994. An essential role for HLA-DM in antigen presentation by class II major histocompatibility molecules. Nature 368:551–554. https://doi.org/10.1038/368551a0.
   PubMed Web of Science ®Google Scholar
• Roche PA, Cresswell P. 1990. Invariant chain association with HLA-DR molecules inhibits immunogenic peptide binding. Nature 345:615–618. https://doi.org/10.1038/345615a0.
   PubMed Web of Science ®Google Scholar
• Durrenberger PF, Fernando FS, Kashefi SN, Bonnert TP, Seilhean D, Nait-Oumesmar B, Schmitt A, Gebicke-Haerter PJ, Falkai P, Grunblatt E, Palkovits M, Arzberger T, Kretzschmar H, Dexter DT, Reynolds R. 2015. Common mechanisms in neurodegeneration and neuroinflammation: a BrainNet Europe gene expression microarray study. J Neural Transm (Vienna) 122:1055–1068. https://doi.org/10.1007/s00702-014-1293-0.
   PubMed Web of Science ®Google Scholar
• Griffin WS, Stanley LC, Ling C, White L, MacLeod V, Perrot LJ, White CL, III, Araoz C. 1989. Brain interleukin 1 and S-100 immunoreactivity are elevated in Down syndrome and Alzheimer disease. Proc Natl Acad Sci U S A 86:7611–7615. https://doi.org/10.1073/pnas.86.19.7611.
   PubMed Web of Science ®Google Scholar
• Moynagh PN, Williams DC, O'Neill LA. 1994. Activation of NF-kappa B and induction of vascular cell adhesion molecule-1 and intracellular adhesion molecule-1 expression in human glial cells by IL-1. Modulation by antioxidants. J Immunol 153:2681–2690.
   PubMed Web of Science ®Google Scholar
• Meyuhas O, Kahan T. 2015. The race to decipher the top secrets of TOP mRNAs. Biochim Biophys Acta 1849:801–811. https://doi.org/10.1016/j.bbagrm.2014.08.015.
   PubMed Web of Science ®Google Scholar
• Yoshihama M, Uechi T, Asakawa S, Kawasaki K, Kato S, Higa S, Maeda N, Minoshima S, Tanaka T, Shimizu N, Kenmochi N. 2002. The human ribosomal protein genes: sequencing and comparative analysis of 73 genes. Genome Res 12:379–390. https://doi.org/10.1101/gr.214202.
   PubMed Web of Science ®Google Scholar
• Pellizzoni L, Cardinali B, Lin-Marq N, Mercanti D, Pierandrei-Amaldi P. 1996. A Xenopus homologue of La autoantigen binds the pyrimidine tract of 5′ UTR of ribosomal protein mRNAs in vitro: implication of a protein factor in complex formation. J Mol Biol 259:904–915. https://doi.org/10.1006/jmbi.1996.0368.
   PubMed Web of Science ®Google Scholar
• Zhu J, Hayakawa A, Kakegawa T, Kaspar RL. 2001. Binding of the La autoantigen to the 5′ untranslated region of a chimeric human translation elongation factor 1A reporter mRNA inhibits translation in vitro. Biochim Biophys Acta 1521:19–29. https://doi.org/10.1016/S0167-4781(01)00277-9.
   PubMed Web of Science ®Google Scholar
• Gunapala KM, Chang D, Hsu CT, Manaye K, Drenan RM, Switzer RC, Steele AD. 2010. Striatal pathology underlies prion infection-mediated hyperactivity in mice. Prion 4:302–315. https://doi.org/10.4161/pri.4.4.13721.
   PubMed Web of Science ®Google Scholar
• Ziebell JM, Taylor SE, Cao T, Harrison JL, Lifshitz J. 2012. Rod microglia: elongation, alignment, and coupling to form trains across the somatosensory cortex after experimental diffuse brain injury. J Neuroinflammation 9:247. https://doi.org/10.1186/1742-2094-9-247.
   PubMed Web of Science ®Google Scholar
• Diedrich J, Wietgrefe S, Zupancic M, Staskus K, Retzel E, Haase AT, Race R. 1987. The molecular pathogenesis of astrogliosis in scrapie and Alzheimer's disease. Microb Pathog 2:435–442. https://doi.org/10.1016/0882-4010(87)90050-7.
   PubMedGoogle Scholar
• Janeczko K. 1988. The proliferative response of astrocytes to injury in neonatal rat brain. A combined immunocytochemical and autoradiographic study. Brain Res 456:280–285.
   PubMed Web of Science ®Google Scholar
• Le Prince G, Delaere P, Fages C, Duyckaerts C, Hauw JJ, Tardy M. 1993. Alterations of glial fibrillary acidic protein mRNA level in the aging brain and in senile dementia of the Alzheimer type. Neurosci Lett 151:71–73. https://doi.org/10.1016/0304-3940(93)90048-P.
   PubMed Web of Science ®Google Scholar
• Ling EA, Wong WC. 1993. The origin and nature of ramified and amoeboid microglia: a historical review and current concepts. Glia 7:9–18. https://doi.org/10.1002/glia.440070105.
   PubMed Web of Science ®Google Scholar
• Vidovic M, Sparacio SM, Elovitz M, Benveniste EN. 1990. Induction and regulation of class II major histocompatibility complex mRNA expression in astrocytes by interferon-gamma and tumor necrosis factor-alpha. J Neuroimmunol 30:189–200. https://doi.org/10.1016/0165-5728(90)90103-T.
   PubMedGoogle Scholar
• Mumaw CL, Levesque S, McGraw C, Robertson S, Lucas S, Stafflinger JE, Campen MJ, Hall P, Norenberg JP, Anderson T, Lund AK, McDonald JD, Ottens AK, Block ML. 2016. Microglial priming through the lung-brain axis: the role of air pollution-induced circulating factors. FASEB J 30:1880–1891. https://doi.org/10.1096/fj.201500047.
   PubMed Web of Science ®Google Scholar
• Taetzsch T, Levesque S, McGraw C, Brookins S, Luqa R, Bonini MG, Mason RP, Oh U, Block ML. 2015. Redox regulation of NF-kappaB p50 and M1 polarization in microglia. Glia 63:423–440. https://doi.org/10.1002/glia.22762.
   PubMed Web of Science ®Google Scholar
• Frautschy SA, Yang F, Irrizarry M, Hyman B, Saido TC, Hsiao K, Cole GM. 1998. Microglial response to amyloid plaques in APPsw transgenic mice. Am J Pathol 152:307–317.
   PubMed Web of Science ®Google Scholar
• Matsumoto Y, Ohmori K, Fujiwara M. 1992. Microglial and astroglial reactions to inflammatory lesions of experimental autoimmune encephalomyelitis in the rat central nervous system. J Neuroimmunol 37:23–33. https://doi.org/10.1016/0165-5728(92)90152-B.
   PubMedGoogle Scholar
• Kreutzberg GW. 1996. Microglia: a sensor for pathological events in the CNS. Trends Neurosci 19:312–318. https://doi.org/10.1016/0166-2236(96)10049-7.
   PubMed Web of Science ®Google Scholar
• Block ML, Zecca L, Hong JS. 2007. Microglia-mediated neurotoxicity: uncovering the molecular mechanisms. Nat Rev Neurosci 8:57–69. https://doi.org/10.1038/nrn2038.
   PubMed Web of Science ®Google Scholar
• Pais TF, Figueiredo C, Peixoto R, Braz MH, Chatterjee S. 2008. Necrotic neurons enhance microglial neurotoxicity through induction of glutaminase by a MyD88-dependent pathway. J Neuroinflammation 5:43. https://doi.org/10.1186/1742-2094-5-43.
   PubMed Web of Science ®Google Scholar
• Rudy B, Fishell G, Lee S, Hjerling-Leffler J. 2011. Three groups of interneurons account for nearly 100% of neocortical GABAergic neurons. Dev Neurobiol 71:45–61. https://doi.org/10.1002/dneu.20853.
   PubMed Web of Science ®Google Scholar
• Sik A, Hajos N, Gulacsi A, Mody I, Freund TF. 1998. The absence of a major Ca2+ signaling pathway in GABAergic neurons of the hippocampus. Proc Natl Acad Sci U S A 95:3245–3250. https://doi.org/10.1073/pnas.95.6.3245.
   PubMedGoogle Scholar
• Ayukawa K, Taniguchi S, Masumoto J, Hashimoto S, Sarvotham H, Hara A, Aoyama T, Sagara J. 2000. La autoantigen is cleaved in the COOH terminus and loses the nuclear localization signal during apoptosis. J Biol Chem 275:34465–34470. https://doi.org/10.1074/jbc.M003673200.
   PubMed Web of Science ®Google Scholar
• Huang M, Ida H, Kamachi M, Iwanaga N, Izumi Y, Tanaka F, Aratake K, Arima K, Tamai M, Hida A, Nakamura H, Origuchi T, Kawakami A, Ogawa N, Sugai S, Utz PJ, Eguchi K. 2005. Detection of apoptosis-specific autoantibodies directed against granzyme B-induced cleavage fragments of the SS-B (La) autoantigen in sera from patients with primary Sjogren's syndrome. Clin Exp Immunol 142:148–154. https://doi.org/10.1111/j.1365-2249.2005.02888.x.
   PubMedGoogle Scholar
• Rutjes SA, Utz PJ, der Heijden A, Broekhuis C, van Venrooij WJ, Pruijn GJ. 1999. The La (SS-B) autoantigen, a key protein in RNA biogenesis, is dephosphorylated and cleaved early during apoptosis. Cell Death Differ 6:976–986. https://doi.org/10.1038/sj.cdd.4400571.
   PubMedGoogle Scholar
• Tran HB, Ohlsson M, Beroukas D, Hiscock J, Bradley J, Buyon JP, Gordon TP. 2002. Subcellular redistribution of La/SS-B autoantigen during physiologic apoptosis in the fetal mouse heart and conduction system: a clue to the pathogenesis of congenital heart block. Arthritis Rheum 46:202–208. https://doi.org/10.1002/1529-0131(200201)46:1<202::AID-ART10062>3.0.CO;2-Y.
   PubMedGoogle Scholar
• Stennicke HR, Jurgensmeier JM, Shin H, Deveraux Q, Wolf BB, Yang X, Zhou Q, Ellerby HM, Ellerby LM, Bredesen D, Green DR, Reed JC, Froelich CJ, Salvesen GS. 1998. Pro-caspase-3 is a major physiologic target of caspase-8. J Biol Chem 273:27084–27090. https://doi.org/10.1074/jbc.273.42.27084.
   PubMed Web of Science ®Google Scholar
• Filippi-Chiela EC, Oliveira MM, Jurkovski B, Callegari-Jacques SM, da Silva VD, Lenz G. 2012. Nuclear morphometric analysis (NMA): screening of senescence, apoptosis and nuclear irregularities. PLoS One 7:e42522. https://doi.org/10.1371/journal.pone.0042522.
   PubMed Web of Science ®Google Scholar
• Heise T, Kota V, Brock A, Morris AB, Rodriguez RM, Zierk AW, Howe PH, Sommer G. 2016. The La protein counteracts cisplatin-induced cell death by stimulating protein synthesis of anti-apoptotic factor Bcl2. Oncotarget 7:29664–29676. https://doi.org/10.18632/oncotarget.8819.
   PubMedGoogle Scholar
• Holcik M, Korneluk RG. 2000. Functional characterization of the X-linked inhibitor of apoptosis (XIAP) internal ribosome entry site element: role of La autoantigen in XIAP translation. Mol Cell Biol 20:4648–4657. https://doi.org/10.1128/MCB.20.13.4648-4657.2000.
   PubMed Web of Science ®Google Scholar
• Nakatake M, Monte-Mor B, Debili N, Casadevall N, Ribrag V, Solary E, Vainchenker W, Plo I. 2012. JAK2(V617F) negatively regulates p53 stabilization by enhancing MDM2 via La expression in myeloproliferative neoplasms. Oncogene 31:1323–1333. https://doi.org/10.1038/onc.2011.313.
   PubMed Web of Science ®Google Scholar
• Trotta R, Vignudelli T, Pecorari L, Intine RV, Guerzoni C, Santilli G, Candini O, Byrom MW, Goldoni S, Ford LP, Caligiuri MA, Maraia R, Perrotti D, Calabretta B. 2003. BCR/ABL activates mdm2 mRNA translation via the La antigen. Cancer Cell 13:145–160. https://doi.org/10.1016/S1535-6108(03)00020-5.
   Google Scholar
• Kole AJ, Annis RP, Deshmukh M. 2013. Mature neurons: equipped for survival. Cell Death Dis 4:e689. https://doi.org/10.1038/cddis.2013.220.
   PubMedGoogle Scholar
• Tsien JZ, Chen DF, Gerber D, Tom C, Mercer EH, Anderson DJ, Mayford M, Kandel ER, Tonegawa S. 1996. Subregion- and cell type-restricted gene knockout in mouse brain. Cell 87:1317–1326. https://doi.org/10.1016/S0092-8674(00)81826-7.
   PubMed Web of Science ®Google Scholar
• Lafontaine DL. 2015. Noncoding RNAs in eukaryotic ribosome biogenesis and function. Nat Struct Mol Biol 22:11–19. https://doi.org/10.1038/nsmb.2939.
   PubMed Web of Science ®Google Scholar
• Maraia RJ, Intine RV. 2002. La protein and its associated small nuclear and nucleolar precursor RNAs. Gene Expr 10:41–57.
   PubMed Web of Science ®Google Scholar
• Maraia RJ, Intine RV. 2001. Recognition of nascent RNA by the human La antigen: Conserved and diverged features of structure and function. Mol Cell Biol 21:367–379. https://doi.org/10.1128/MCB.21.2.367-379.2001.
   PubMedGoogle Scholar
• Scheper GC, Voorma HO, Thomas AA. 1994. Basepairing with 18S ribosomal RNA in internal initiation of translation. FEBS Lett 352:271–275. https://doi.org/10.1016/0014-5793(94)00975-9.
   PubMedGoogle Scholar
• Boria I, Garelli E, Gazda HT, Aspesi A, Quarello P, Pavesi E, Ferrante D, Meerpohl JJ, Kartal M, Da Costa L, Proust A, Leblanc T, Simansour M, Dahl N, Frojmark AS, Pospisilova D, Cmejla R, Beggs AH, Sheen MR, Landowski M, Buros CM, Clinton CM, Dobson LJ, Vlachos A, Atsidaftos E, Lipton JM, Ellis SR, Ramenghi U, Dianzani I. 2010. The ribosomal basis of Diamond-Blackfan Anemia: mutation and database update. Hum Mutat 31:1269–1279. https://doi.org/10.1002/humu.21383.
   PubMed Web of Science ®Google Scholar
• Phipps KR, Charette J, Baserga SJ. 2011. The small subunit processome in ribosome biogenesis—progress and prospects. Wiley Interdiscip Rev RNA 2:1–21. https://doi.org/10.1002/wrna.57.
   PubMed Web of Science ®Google Scholar
• Briggs MW, Burkard KT, Butler JS. 1998. Rrp6p, the yeast homologue of the human PM-Scl 100-kDa autoantigen, is essential for efficient 5.8 S rRNA 3′ end formation. J Biol Chem 273:13255–13263. https://doi.org/10.1074/jbc.273.21.13255.
   PubMed Web of Science ®Google Scholar
• Thomson E, Tollervey D. 2010. The final step in 5.8S rRNA processing is cytoplasmic in Saccharomyces cerevisiae. Mol Cell Biol 30:976–984. https://doi.org/10.1128/MCB.01359-09.
   PubMedGoogle Scholar
• Waldron C, Lacroute F. 1975. Effect of growth rate on the amounts of ribosomal and transfer ribonucleic acids in yeast. J Bacteriol 122:855–865.
   PubMed Web of Science ®Google Scholar
• Ozanick SG, Wang X, Costanzo M, Brost RL, Boone C, Anderson JT. 2009. Rex1p deficiency leads to accumulation of precursor initiator tRNAMet and polyadenylation of substrate RNAs in Saccharomyces cerevisiae. Nucleic Acids Res 37:298–308. https://doi.org/10.1093/nar/gkn925.
   PubMed Web of Science ®Google Scholar
• Turowski TW, Tollervey D. 2015. Cotranscriptional events in eukaryotic ribosome synthesis. Wiley Interdiscip Rev RNA 6:129–139. https://doi.org/10.1002/wrna.1263.
   PubMed Web of Science ®Google Scholar
• Daneshvar DH, Goldstein LE, Kiernan PT, Stein TD, McKee AC. 2015. Post-traumatic neurodegeneration and chronic traumatic encephalopathy. Mol Cell Neurosci 66:81–90. https://doi.org/10.1016/j.mcn.2015.03.007.
   PubMed Web of Science ®Google Scholar
• De Chiara G, Marcocci ME, Sgarbanti R, Civitelli L, Ripoli C, Piacentini R, Garaci E, Grassi C, Palamara AT. 2012. Infectious agents and neurodegeneration. Mol Neurobiol 46:614–638. https://doi.org/10.1007/s12035-012-8320-7.
   PubMed Web of Science ®Google Scholar
• Wang X, Huang T, Bu G, Xu H. 2014. Dysregulation of protein trafficking in neurodegeneration. Mol Neurodegener 9:31. https://doi.org/10.1186/1750-1326-9-31.
   PubMed Web of Science ®Google Scholar
• Nalavade R, Griesche N, Ryan DP, Hildebrand S, Krauss S. 2013. Mechanisms of RNA-induced toxicity in CAG repeat disorders. Cell Death Dis 4:e752. https://doi.org/10.1038/cddis.2013.276.
   Google Scholar
• Heppner FL, Ransohoff RM, Becher B. 2015. Immune attack: the role of inflammation in Alzheimer disease. Nat Rev Neurosci 16:358–372. https://doi.org/10.1038/nrn3880.
   PubMed Web of Science ®Google Scholar
• Lull ME, Block ML. 2010. Microglial activation and chronic neurodegeneration. Neurotherapeutics 7:354–365. https://doi.org/10.1016/j.nurt.2010.05.014.
   PubMed Web of Science ®Google Scholar
• Maragakis NJ, Rothstein JD. 2006. Mechanisms of disease: astrocytes in neurodegenerative disease. Nat Clin Pract Neurol 2:679–689.
   PubMedGoogle Scholar
• Qin L, Wu X, Block ML, Liu Y, Breese GR, Hong JS, Knapp DJ, Crews FT. 2007. Systemic LPS causes chronic neuroinflammation and progressive neurodegeneration. Glia 55:453–462. https://doi.org/10.1002/glia.20467.
   PubMed Web of Science ®Google Scholar
• Block ML, Hong JS. 2005. Microglia and inflammation-mediated neurodegeneration: multiple triggers with a common mechanism. Prog Neurobiol 76:77–98. https://doi.org/10.1016/j.pneurobio.2005.06.004.
   PubMed Web of Science ®Google Scholar
• Navarrete M, Araque A. 2014. The Cajal school and the physiological role of astrocytes: a way of thinking. Front Neuroanat 8:33. https://doi.org/10.3389/fnana.2014.00033.
   PubMedGoogle Scholar
• Davies JE, Huang C, Proschel C, Noble M, Mayer-Proschel M, Davies SJ. 2006. Astrocytes derived from glial-restricted precursors promote spinal cord repair. J Biol 5:7. https://doi.org/10.1186/jbiol35.
   PubMedGoogle Scholar
• Baldwin KT, Carbajal KS, Segal BM, Giger RJ. 2015. Neuroinflammation triggered by beta-glucan/dectin-1 signaling enables CNS axon regeneration. Proc Natl Acad Sci U S A 112:2581–2586. https://doi.org/10.1073/pnas.1423221112.
   PubMed Web of Science ®Google Scholar
• Chan PP, Lowe TM. 2016. GtRNAdb 2.0: an expanded database of transfer RNA genes identified in complete and draft genomes. Nucleic Acids Res 44:D184–D189. https://doi.org/10.1093/nar/gkv1309.
   PubMed Web of Science ®Google Scholar
• Aslett M, Aurrecoechea C, Berriman M, Brestelli J, Brunk BP, Carrington M, Depledge DP, Fischer S, Gajria B, Gao X, Gardner MJ, Gingle A, Grant G, Harb OS, Heiges M, Hertz-Fowler C, Houston R, Innamorato F, Iodice J, Kissinger JC, Kraemer E, Li W, Logan FJ, Miller JA, Mitra S, Myler PJ, Nayak V, Pennington C, Phan I, Pinney DF, Ramasamy G, Rogers MB, Roos DS, Ross C, Sivam D, Smith DF, Srinivasamoorthy G, Stoeckert CJ, Jr, Subramanian S, Thibodeau R, Tivey A, Treatman C, Velarde G, Wang H. 2010. TriTrypDB: a functional genomic resource for the Trypanosomatidae. Nucleic Acids Res 38:D457–D462. https://doi.org/10.1093/nar/gkp851.
   PubMed Web of Science ®Google Scholar
• Aurrecoechea C, Brestelli J, Brunk BP, Dommer J, Fischer S, Gajria B, Gao X, Gingle A, Grant G, Harb OS, Heiges M, Innamorato F, Iodice J, Kissinger JC, Kraemer E, Li W, Miller JA, Nayak V, Pennington C, Pinney DF, Roos DS, Ross C, Stoeckert CJ, Jr, Treatman C, Wang H. 2009. PlasmoDB: a functional genomic database for malaria parasites. Nucleic Acids Res 37:D539–D543. https://doi.org/10.1093/nar/gkn814.
   PubMed Web of Science ®Google Scholar
• Basu S, Fey P, Pandit Y, Dodson R, Kibbe WA, Chisholm RL. 2013. DictyBase 2013: integrating multiple Dictyostelid species. Nucleic Acids Res 41:D676–D683. https://doi.org/10.1093/nar/gks1064.
   PubMed Web of Science ®Google Scholar
• Eichinger L, Pachebat JA, Glockner G, Rajandream MA, Sucgang R, Berriman M, Song J, Olsen R, Szafranski K, Xu Q, Tunggal B, Kummerfeld S, Madera M, Konfortov BA, Rivero F, Bankier AT, Lehmann R, Hamlin N, Davies R, Gaudet P, Fey P, Pilcher K, Chen G, Saunders D, Sodergren E, Davis P, Kerhornou A, Nie X, Hall N, Anjard C, Hemphill L, Bason N, Farbrother P, Desany B, Just E, Morio T, Rost R, Churcher C, Cooper J, Haydock S, van Driessche N, Cronin A, Goodhead I, Muzny D, Mourier T, Pain A, Lu M, Harper D, Lindsay R, Hauser H, James K, Quiles M, Madan Babu M, Saito T, Buchrieser C, Wardroper A, Felder M, Simmonds M, Spiegler S, Tivey A, Sugano S, White B, Walker D, Woodward J, Weinstock G, Rosenthal A, Cox EC, Chisholm RL, Gibbs R, Loomis WF, Platzer M, Kay RR, Williams J, Dear PH, Noegel AA, Barrell B, Kuspa A. 2005. The genome of the social amoeba Dictyostelium discoideum. Nature 435:43–57. https://doi.org/10.1038/nature03481.
   PubMed Web of Science ®Google Scholar
• De Robertis EM, Olson MV. 1979. Transcription and processing of cloned yeast tyrosine tRNA genes microinjected into frog oocytes. Nature 278:137–143. https://doi.org/10.1038/278137a0.
   PubMed Web of Science ®Google Scholar
• Melton DA, De Robertis EM, Cortese R. 1980. Order and intracellular location of the events involved in the maturation of a spliced tRNA. Nature 284:143–148. https://doi.org/10.1038/284143a0.
   PubMed Web of Science ®Google Scholar
• Foretek D, Wu J, Hopper AK, Boguta M. 2016. Control of Saccharomyces cerevisiae pre-tRNA processing by environmental conditions. RNA 22:339–349. https://doi.org/10.1261/rna.054973.115.
   PubMed Web of Science ®Google Scholar
• Huang Y, Intine RV, Mozlin A, Hasson S, Maraia RJ. 2005. Mutations in the RNA polymerase III subunit Rpc11p that decrease RNA 3′ cleavage activity increase 3′-terminal oligo(U) length and La-dependent tRNA processing. Mol Cell Biol 25:621–636. https://doi.org/10.1128/MCB.25.2.621-636.2005.
   PubMed Web of Science ®Google Scholar
• Van Horn DJ, Yoo CJ, Xue D, Shi H, Wolin SL. 1997. The La protein in Schizosaccharomyces pombe: a conserved yet dispensable phosphoprotein that functions in tRNA maturation. RNA 3:1434–1443.
   PubMed Web of Science ®Google Scholar
• De Robertis EM, Black P, Nishikura K. 1981. Intranuclear location of the tRNA splicing enzymes. Cell 23:89–93. https://doi.org/10.1016/0092-8674(81)90273-7.
   PubMedGoogle Scholar
• Hopper AK, Shaheen HH. 2008. A decade of surprises for tRNA nuclear-cytoplasmic dynamics. Trends Cell Biol 18:98–104. https://doi.org/10.1016/j.tcb.2008.01.001.
   PubMedGoogle Scholar
• Yoshihisa T, Ohshima C, Yunoki-Esaki K, Endo T. 2007. Cytoplasmic splicing of tRNA in Saccharomyces cerevisiae. Genes Cells 12:285–297. https://doi.org/10.1111/j.1365-2443.2007.01056.x.
   PubMed Web of Science ®Google Scholar
• Yoshihisa T, Yunoki-Esaki K, Tanaka N, Endo T. 2003. Possibility of cytoplasmic pre-tRNA splicing: the yeast tRNA splicing endonuclease mainly localizes on the mitochondria. Mol Biol Cell 14:3266–3279. https://doi.org/10.1091/mbc.E02-11-0757.
   PubMed Web of Science ®Google Scholar
• Kramer EB, Hopper AK. 2013. Retrograde transfer RNA nuclear import provides a new level of tRNA quality control in Saccharomyces cerevisiae. Proc Natl Acad Sci U S A 110:21042–21047. https://doi.org/10.1073/pnas.1316579110.
   PubMed Web of Science ®Google Scholar
• Cook AG, Fukuhara N, Jinek M, Conti E. 2009. Structures of the tRNA export factor in the nuclear and cytosolic states. Nature 461:60–65. https://doi.org/10.1038/nature08394.
   PubMed Web of Science ®Google Scholar
• Trotta CR, Abelson J. 1999. tRNA splicing: an RNA world add-on or an ancient reaction?, p 561–584. InGesteland RF, Cech TR, Atkins JF (ed), The RNA world, 2nd ed. Cold Spring Harbor Press, Cold Spring Harbor, NY.
   Google Scholar
• Trotta CR, Miao F, Arn EA, Stevens SW, Ho CK, Rauhut R, Abelson JN. 1997. The yeast tRNA splicing endonuclease: a tetrameric enzyme with two active site subunits homologous to the archaeal tRNA endonucleases. Cell 89:849–858. https://doi.org/10.1016/S0092-8674(00)80270-6.
   PubMed Web of Science ®Google Scholar
• Trotta CR, Paushkin SV, Patel M, Li H, Peltz SW. 2006. Cleavage of pre-tRNAs by the splicing endonuclease requires a composite active site. Nature 441:375–377. https://doi.org/10.1038/nature04741.
   PubMedGoogle Scholar
• Karaca E, Weitzer S, Pehlivan D, Shiraishi H, Gogakos T, Hanada T, Jhangiani SN, Wiszniewski W, Withers M, Campbell IM, Erdin S, Isikay S, Franco LM, Gonzaga-Jauregui C, Gambin T, Gelowani V, Hunter JV, Yesil G, Koparir E, Bainbridge MN, Gezdirici A, Seven M, Muzny DM, Boerwinkle E, Ozen M, Baylor Hopkins Center for Mendelian Genetics, Clausen T, Tuschl T, Yuksel A, Hess A, Gibbs RA, Martinez J, Penninger JM, Lupski JR. 2014. Human CLP1 mutations alter tRNA biogenesis, affecting both peripheral and central nervous system function. Cell 157:636–650. https://doi.org/10.1016/j.cell.2014.02.058.
   PubMed Web of Science ®Google Scholar
• Schaffer AE, Eggens VR, Caglayan AO, Reuter MS, Scott E, Coufal NG, Silhavy JL, Xue Y, Kayserili H, Yasuno K, Rosti RO, Abdellateef M, Caglar C, Kasher PR, Cazemier JL, Weterman MA, Cantagrel V, Cai N, Zweier C, Altunoglu U, Satkin NB, Aktar F, Tuysuz B, Caksen H, Bilguvar K, Fu XD, Trotta CR, Gabriel S, Reis A, Gunel M, Baas F, Gleeson JG. 2014. CLP1 founder mutation links tRNA splicing and maturation to cerebellar development and neurodegeneration. Cell 157:651–663. https://doi.org/10.1016/j.cell.2014.03.049.
   PubMed Web of Science ®Google Scholar
• Battini R, D'Arrigo S, Cassandrini D, Guzzetta A, Fiorillo C, Pantaleoni C, Romano A, Alfei E, Cioni G, Santorelli FM. 2014. Novel mutations in TSEN54 in pontocerebellar hypoplasia type 2. J Child Neurol 29:520–525. https://doi.org/10.1177/0883073812470002.
   PubMedGoogle Scholar
• Breuss MW, Sultan T, James KN, Rosti RO, Scott E, Musaev D, Furia B, Reis A, Sticht H, Al-Owain M, Alkuraya FS, Reuter MS, Abou Jamra R, Trotta CR, Gleeson JG. 2016. Autosomal-recessive mutations in the tRNA splicing endonuclease subunit TSEN15 cause pontocerebellar hypoplasia and progressive microcephaly. Am J Hum Genet 99:228–235. https://doi.org/10.1016/j.ajhg.2016.05.023.
   PubMedGoogle Scholar
• Huang da W, Sherman BT, Lempicki RA. 2009. Bioinformatics enrichment tools: paths toward the comprehensive functional analysis of large gene lists. Nucleic Acids Res 37:1–13. https://doi.org/10.1093/nar/gkn923.
   PubMed Web of Science ®Google Scholar
• Mi H, Dong Q, Muruganujan A, Gaudet P, Lewis S, Thomas PD. 2010. PANTHER version 7: improved phylogenetic trees, orthologs and collaboration with the Gene Ontology Consortium. Nucleic Acids Res 38:D204–D210. https://doi.org/10.1093/nar/gkp1019.
   PubMed Web of Science ®Google Scholar
• Thomas PD, Campbell MJ, Kejariwal A, Mi H, Karlak B, Daverman R, Diemer K, Muruganujan A, Narechania A. 2003. PANTHER: a library of protein families and subfamilies indexed by function. Genome Res 13:2129–2141. https://doi.org/10.1101/gr.772403.
   PubMed Web of Science ®Google Scholar
• Wang J, Huang Q, Liu ZP, Wang Y, Wu LY, Chen L, Zhang XS. 2011. NOA: a novel network ontology analysis method. Nucleic Acids Res 39:e87. https://doi.org/10.1093/nar/gkr251.
   Google Scholar
• Preibisch S, Saalfeld S, Tomancak P. 2009. Globally optimal stitching of tiled 3D microscopic image acquisitions. Bioinformatics 25:1463–1465. https://doi.org/10.1093/bioinformatics/btp184.
   PubMed Web of Science ®Google Scholar
• Schneider CA, Rasband WS, Eliceiri KW. 2012. NIH Image to ImageJ: 25 years of image analysis. Nat Methods 9:671–675. https://doi.org/10.1038/nmeth.2089.
   PubMed Web of Science ®Google Scholar
• Livak KJ, Schmittgen TD. 2001. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) method. Methods 25:402–408. https://doi.org/10.1006/meth.2001.1262.
   PubMed Web of Science ®Google Scholar