Family of pentatricopeptide repeat proteins in non-plant organisms

Katarzyna Dorota Raczynska, Pawel Czubak

Abstract


Pentatricopeptide repeat (PPR) proteins belong to the large family of nucleic acid binding proteins. Their name is defined by the presence of the so-called pentatricopeptide repeat (PPR), a degenerate 35-amino acid motif tandemly repeated 2–26 times per protein. The PPR protein family includes some of the major mediators of organelle post-transcriptional control. These proteins localize mainly to mitochondria and chloroplasts, where they are involved in different steps of RNA metabolism: transcription, splicing, editing, polyadenylation, RNA stability and translation. Some of them can also act as adaptors in protein-protein interactions. PPR protein genes were discovered in many eukaryotic genomes, but they are especially abundant in plants. In humans, some PPR proteins are implicated in human diseases, such as cancer, Alzheimer’s disease and Parkinson’s disease.


Keywords


PPR motif, RNA binding proteins, organella, human diseases

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References


Small ID, Peeters N. The PPR motif - a TPR-related motif prevalent in plant organellar proteins. Trends Biochem Sci. 2000;25(2):46-7.

Schmitz-Linneweber C, Small I. Pentatricopeptide repeat proteins: a socket set for organelle gene expression. Trends Plant Sci. 2008;13(12):663-70.

Dong Y, Yoshitomi T, Hu JF, Cui J. Long noncoding RNAs coordinate functions between mitochondria and the nucleus. Epigenetics Chromatin. 2017;10(1):41.

Moore MJ. From birth to death: the complex lives of eukaryotic mRNAs. Science. 2005;309(5740):1514-8.

Dreyfuss G, Kim VN, Kataoka N. Messenger-RNA-binding proteins and the messages they carry. Nat Rev Mol Cell Biol. 2002;3(3):195-205.

Keene JD. RNA regulons: coordination of post-transcriptional events. Nat Rev Genet. 2007;8(7):533-43.

Lipinski KA, Puchta O, Surendranath V, Kudla M, Golik P. Revisiting the yeast PPR proteins--application of an Iterative Hidden Markov Model algorithm reveals new members of the rapidly evolving family. Mol Biol Evol. 2011;28(10):2935-48.

Shikanai T. RNA editing in plant organelles: machinery, physiological function and evolution. Cell Mol Life Sci. 2006;63(6):698-708.

Manna S, Brewster J, Barth C. Identification of Pentatricopeptide Repeat Proteins in the Model Organism Dictyostelium discoideum. Int J Genomics. 2013;2013:586498.

Barkan A, Small I. Pentatricopeptide repeat proteins in plants. Annu Rev Plant Biol. 2014;65:415-42.

O'Toole N, Hattori M, Andres C, Iida K, Lurin C, Schmitz-Linneweber C, et al. On the expansion of the pentatricopeptide repeat gene family in plants. Mol Biol Evol. 2008;25(6):1120-8.

Raczynska KD, Augustyniak H. [Family of pentatricopeptide repeat proteins]. Postepy Biochem. 2005;51(4):440-6.

Hassani D, Khalid M, Bilal M, Zhang YD, Huang D. Pentatricopeptide repeat-directed RNA editing and their

biomedical applications. International Journal of Pharmacology. 2017;13(7):762-72.

Filipovska A, Rackham O. Pentatricopeptide repeats: modular blocks for building RNA-binding proteins. RNA Biol. 2013;10(9):1426-32.

Lurin C, Andres C, Aubourg S, Bellaoui M, Bitton F, Bruyere C, et al. Genome-wide analysis of Arabidopsis pentatricopeptide repeat proteins reveals their essential role in organelle biogenesis. Plant Cell. 2004;16(8):2089-103.

Cazalet C, Gomez-Valero L, Rusniok C, Lomma M, Dervins-Ravault D, Newton HJ, et al. Analysis of the Legionella longbeachae genome and transcriptome uncovers unique strategies to cause Legionnaires' disease. PLoS Genet. 2010;6(2):e1000851.

Choudhary M, Zanhua X, Fu YX, Kaplan S. Genome analyses of three strains of Rhodobacter sphaeroides: evidence of rapid evolution of chromosome II. J Bacteriol. 2007;189(5):1914-21.

Hallam SJ, Putnam N, Preston CM, Detter JC, Rokhsar D, Richardson PM, et al. Reverse methanogenesis: testing the hypothesis with environmental genomics. Science. 2004;305(5689):1457-62.

Schallenberg-Rudinger M, Lenz H, Polsakiewicz M, Gott JM, Knoop V. A survey of PPR proteins identifies DYW domains like those of land plant RNA editing factors in diverse eukaryotes. RNA Biol. 2013;10(9):1549-56.

Ke J, Chen RZ, Ban T, Zhou XE, Gu X, Tan MH, et al. Structural basis for RNA recognition by a dimeric PPR-protein complex. Nat Struct Mol Biol. 2013;20(12):1377-82.

Yin P, Li Q, Yan C, Liu Y, Liu J, Yu F, et al. Structural basis for the modular recognition of single-stranded RNA by PPR proteins. Nature. 2013;504(7478):168-71.

Barkan A, Rojas M, Fujii S, Yap A, Chong YS, Bond CS, et al. A combinatorial amino acid code for RNA recognition by pentatricopeptide repeat proteins. PLoS Genet. 2012;8(8):e1002910.

Yagi Y, Hayashi S, Kobayashi K, Hirayama T, Nakamura T. Elucidation of the RNA recognition code for pentatricopeptide repeat proteins involved in organelle RNA editing in plants. PLoS One. 2013;8(3):e57286.

Main ER, Stott K, Jackson SE, Regan L. Local and long-range stability in tandemly arrayed tetratricopeptide repeats. Proc Natl Acad Sci U S A. 2005;102(16):5721-6.

Kobe B, Kajava AV. When protein folding is simplified to protein coiling: the continuum of solenoid protein structures. Trends Biochem Sci. 2000;25(10):509-15.

Delannoy E, Stanley WA, Bond CS, Small ID. Pentatricopeptide repeat (PPR) proteins as sequence-specificity factors in post-transcriptional processes in organelles. Biochem Soc Trans. 2007;35(Pt 6):1643-7.

Williams-Carrier R, Kroeger T, Barkan A. Sequence-specific binding of a chloroplast pentatricopeptide repeat protein to its native group II intron ligand. RNA. 2008;14(9):1930-41.

Okuda K, Myouga F, Motohashi R, Shinozaki K, Shikanai T. Conserved domain structure of pentatricopeptide repeat proteins involved in chloroplast RNA editing. Proc Natl Acad Sci U S A. 2007;104(19):8178-83.

Abbas YM, Pichlmair A, Gorna MW, Superti-Furga G, Nagar B. Structural basis for viral 5'-PPP-RNA recognition by human IFIT proteins. Nature. 2013;494(7435):60-4.

Pichlmair A, Lassnig C, Eberle CA, Gorna MW, Baumann CL, Burkard TR, et al. IFIT1 is an antiviral protein that recognizes 5'-triphosphate RNA. Nat Immunol. 2011;12(7):624-30.

Manna S. An overview of pentatricopeptide repeat proteins and their applications. Biochimie. 2015;113:93-9.

Herbert CJ, Golik P, Bonnefoy N. Yeast PPR proteins, watchdogs of mitochondrial gene expression. RNA Biol. 2013;10(9):1477-94.

Hall TM. De-coding and re-coding RNA recognition by PUF and PPR repeat proteins. Curr Opin Struct Biol. 2016;36:116-21.

Gobert A, Gutmann B, Taschner A, Gossringer M, Holzmann J, Hartmann RK, et al. A single Arabidopsis organellar protein has RNase P activity. Nat Struct Mol Biol. 2010;17(6):740-4.

Takenaka M, Zehrmann A, Verbitskiy D, Kugelmann M, Hartel B, Brennicke A. Multiple organellar RNA editing factor (MORF) family proteins are required for RNA editing in mitochondria and plastids of plants. Proc Natl Acad Sci U S A. 2012;109(13):5104-9.

Ringel R, Sologub M, Morozov YI, Litonin D, Cramer P, Temiakov D. Structure of human mitochondrial RNA polymerase. Nature. 2011;478(7368):269-73.

Coquille S, Filipovska A, Chia T, Rajappa L, Lingford JP, Razif MF, et al. An artificial PPR scaffold for programmable RNA recognition. Nat Commun. 2014;5:5729.

Fujii S, Small I. The evolution of RNA editing and pentatricopeptide repeat genes. New Phytol. 2011;191(1):37-47.

Matsushima Y, Hirofuji Y, Aihara M, Yue S, Uchiumi T, Kaguni LS, et al. Drosophila protease ClpXP specifically degrades DmLRPPRC1 controlling mitochondrial mRNA and translation. Sci Rep. 2017;7(1):8315.

Barros MH, Tzagoloff A. Aep3p-dependent translation of yeast mitochondrial ATP8. Mol Biol Cell. 2017;28(11):1426-34.

Aphasizheva I, Maslov D, Wang X, Huang L, Aphasizhev R. Pentatricopeptide repeat proteins stimulate mRNA adenylation/uridylation to activate mitochondrial translation in trypanosomes. Mol Cell. 2011;42(1):106-17.

Aphasizheva I, Maslov DA, Qian Y, Huang L, Wang Q, Costello CE, et al. Ribosome-associated pentatricopeptide repeat proteins function as translational activators in mitochondria of trypanosomes. Mol Microbiol. 2016;99(6):1043-58.

Ridlon L, Skodova I, Pan S, Lukes J, Maslov DA. The importance of the 45 S ribosomal small subunit-related complex for mitochondrial translation in Trypanosoma brucei. J Biol Chem. 2013;288(46):32963-78.

Herrmann JM, Woellhaf MW, Bonnefoy N. Control of protein synthesis in yeast mitochondria: the concept of translational activators. Biochim Biophys Acta. 2013;1833(2):286-94.

Richter-Dennerlein R, Dennerlein S, Rehling P. Integrating mitochondrial translation into the cellular context. Nat Rev Mol Cell Biol. 2015;16(10):586-92.

Sasarman F, Brunel-Guitton C, Antonicka H, Wai T, Shoubridge EA, Consortium L. LRPPRC and SLIRP interact in a ribonucleoprotein complex that regulates posttranscriptional gene expression in mitochondria. Mol Biol Cell. 2010;21(8):1315-23.

Bratic A, Wredenberg A, Gronke S, Stewart JB, Mourier A, Ruzzenente B, et al. The bicoid stability factor controls polyadenylation and expression of specific mitochondrial mRNAs in Drosophila melanogaster. PLoS Genet. 2011;7(10):e1002324.

Ruzzenente B, Metodiev MD, Wredenberg A, Bratic A, Park CB, Camara Y, et al. LRPPRC is necessary for polyadenylation and coordination of translation of mitochondrial mRNAs. EMBO J. 2012;31(2):443-56.

Chujo T, Ohira T, Sakaguchi Y, Goshima N, Nomura N, Nagao A, et al. LRPPRC/SLIRP suppresses PNPase-mediated mRNA decay and promotes polyadenylation in human mitochondria. Nucleic Acids Res. 2012;40(16):8033-47.

Cooper MP, Qu L, Rohas LM, Lin J, Yang W, Erdjument-Bromage H, et al. Defects in energy homeostasis in Leigh syndrome French Canadian variant through PGC-1alpha/LRP130 complex. Genes Dev. 2006;20(21):2996-3009.

Manna S, Barth C. Identification of a novel pentatricopeptide repeat subfamily with a C-terminal domain of bacterial origin acquired via ancient horizontal gene transfer. BMC Res Notes. 2013;6:525.

Rackham O, Filipovska A. The role of mammalian PPR domain proteins in the regulation of mitochondrial gene expression. Biochim Biophys Acta. 2012;1819(9-10):1008-16.

Siira SJ, Spahr H, Shearwood AJ, Ruzzenente B, Larsson NG, Rackham O, et al. LRPPRC-mediated folding of the mitochondrial transcriptome. Nat Commun. 2017;8(1):1532.

Perks KL, Ferreira N, Richman TR, Ermer JA, Kuznetsova I, Shearwood AJ, et al. Adult-onset obesity is triggered by impaired mitochondrial gene expression. Sci Adv. 2017;3(8):e1700677.

Lightowlers RN, Chrzanowska-Lightowlers ZM. Human pentatricopeptide proteins: only a few and what do they do? RNA Biol. 2013;10(9):1433-8.

Rossmanith W. Of P and Z: mitochondrial tRNA processing enzymes. Biochim Biophys Acta. 2012;1819(9-10):1017-26.

Xu F, Ackerley C, Maj MC, Addis JB, Levandovskiy V, Lee J, et al. Disruption of a mitochondrial RNA-binding protein gene results in decreased cytochrome b expression and a marked reduction in ubiquinol-cytochrome c reductase activity in mouse heart mitochondria. Biochem J. 2008;416(1):15-26.

Rorbach J, Minczuk M. The post-transcriptional life of mammalian mitochondrial RNA. Biochem J. 2012;444(3):357-73.

Seo DC, Sung JM, Cho HJ, Yi H, Seo KH, Choi IS, et al. Gene expression profiling of cancer stem cell in human lung adenocarcinoma A549 cells. Mol Cancer. 2007;6:75.

Tian T, Ikeda J, Wang Y, Mamat S, Luo W, Aozasa K, et al. Role of leucine-rich pentatricopeptide repeat motif-containing protein (LRPPRC) for anti-apoptosis and tumourigenesis in cancers. Eur J Cancer. 2012;48(15):2462-73.

Siegel R, Naishadham D, Jemal A. Cancer statistics, 2013. CA Cancer J Clin. 2013;63(1):11-30.

Jiang X, Li X, Huang H, Jiang F, Lin Z, He H, et al. Elevated levels of mitochondrion-associated autophagy inhibitor LRPPRC are associated with poor prognosis in patients with prostate cancer. Cancer. 2014;120(8):1228-36.

Mootha VK, Lepage P, Miller K, Bunkenborg J, Reich M, Hjerrild M, et al. Identification of a gene causing human cytochrome c oxidase deficiency by integrative genomics. Proc Natl Acad Sci U S A. 2003;100(2):605-10.

Mourier A, Ruzzenente B, Brandt T, Kuhlbrandt W, Larsson NG. Loss of LRPPRC causes ATP synthase deficiency. Hum Mol Genet. 2014;23(10):2580-92.

Sasarman F, Nishimura T, Antonicka H, Weraarpachai W, Shoubridge EA, Consortium L. Tissue-specific responses to the LRPPRC founder mutation in French Canadian Leigh Syndrome. Hum Mol Genet. 2015;24(2):480-91.

Xu F, Morin C, Mitchell G, Ackerley C, Robinson BH. The role of the LRPPRC (leucine-rich pentatricopeptide repeat cassette) gene in cytochrome oxidase assembly: mutation causes lowered levels of COX (cytochrome c oxidase) I and COX III mRNA. Biochem J. 2004;382(Pt 1):331-6.

Chouliaras L, Sierksma AS, Kenis G, Prickaerts J, Lemmens MA, Brasnjevic I, et al. Erratum: gene-environment interaction research and transgenic mouse models of Alzheimer's disease. Int J Alzheimers Dis. 2011;2010:356862.

Day JJ, Sweatt JD. Cognitive neuroepigenetics: a role for epigenetic mechanisms in learning and memory. Neurobiol Learn Mem. 2011;96(1):2-12.

Minati L, Edginton T, Bruzzone MG, Giaccone G. Current concepts in Alzheimer's disease: a multidisciplinary review. Am J Alzheimers Dis Other Demen. 2009;24(2):95-121.

Hosp F, Vossfeldt H, Heinig M, Vasiljevic D, Arumughan A, Wyler E, et al. Quantitative interaction proteomics of neurodegenerative disease proteins. Cell Rep. 2015;11(7):1134-46.

Acharya NK, Nagele EP, Han M, Coretti NJ, DeMarshall C, Kosciuk MC, et al. Neuronal PAD4 expression and protein citrullination: possible role in production of autoantibodies associated with neurodegenerative disease. J Autoimmun. 2012;38(4):369-80.

Jankovic J. Parkinson's disease: clinical features and diagnosis. J Neurol Neurosurg Psychiatry. 2008;79(4):368-76.

Zimprich A, Biskup S, Leitner P, Lichtner P, Farrer M, Lincoln S, et al. Mutations in LRRK2 cause autosomal-dominant parkinsonism with pleomorphic pathology. Neuron. 2004;44(4):601-7.

Gaweda-Walerych K, Mohagheghi F, Zekanowski C, Buratti E. Parkinson's disease-related gene variants influence pre-mRNA splicing processes. Neurobiol Aging. 2016;47:127-38.

Samii A, Nutt JG, Ransom BR. Parkinson's disease. Lancet. 2004;363(9423):1783-93.




DOI: http://dx.doi.org/10.18103/imr.v4i3.657

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