Cellular models, genomic technologies and clinical practice: a synthesis of knowledge for the study of the mechanisms, diagnostics and treatment of Parkinson's disease



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Abstract

Nowadays we approached the turn, when the molecular genetics and the cell biology with its extensive baggage of methods and data, allow us to work with information about nucleotide sequences of whole genomes, to edit the nucleotide sequence of the genomes of laboratory animals and cultured human cells and also explore functions and interactions of genetic elements in health and in disease. The use of these instruments opens up huge possibilities for the study of severe human genetic abnormalities. In various laboratories around world an extensive work is carried out in this area by searching links between genetic elements and diseases, using the latest technology of genome editing and reprogramming somatic mature cells to a pluripotent stem condition. The most progressively developing area of research is the study of neurodegenerative diseases. In this review we discussed about possibilities and problems of using new techniques and instruments of cell biology, genetics and genomics in studying molecular and genetic basis of the pathogenesis of Parkinson's disease.

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About the authors

V. R Kovalenko

Federal Research Centre of the Institute of Cytology and Genetics, the Siberian Branch of the RAS; Institute of Chemical Biology and Fundamental Medicine, the Siberian Branch of the RAS; State Research Institute of Circulation Pathology

E. A Khabarova

Federal Center of Neurosurgery

D. A Rzaev

Federal Center of Neurosurgery

S. P Medvedev

Federal Research Centre of the Institute of Cytology and Genetics, the Siberian Branch of the RAS; Institute of Chemical Biology and Fundamental Medicine, the Siberian Branch of the RAS; State Research Institute of Circulation Pathology; National Research Novosibirsk State University

Email: medvedev@bionet.nsc.ru

References

  1. Thomas B., Beal M.F. Parkinson's disease. Hum. Mol. Genet. 2007; 16(R2): R183-94.
  2. Suppa A., Bologna M., Conte A. et al. The effect of L-dopa in Parkinson' s disease as revealed by neurophysiological studies of motor and sensory functions. Expert Rev. Neurother. 2017; 17(2): 181-92.
  3. Lees A.J. Unresolved issues relating to the Shaking Palsy on the celebration of James Parkinson's 250th birthday. Mov. Disord. 2007; 22(S17): S327-34.
  4. Goedert M., Spillantini M.G., Del Tredici K. et al. 100 years of Lewy pathology. Nat. Rev. Neurol. 2012; 9(1): 13-24.
  5. Ikeda K., Ikeda S., Yoshimura T. et al. Idiopathic Parkinsonism with Lewy-type inclusions in cerebral cortex. A case report. Acta Neuropathol. 1978; 41(2): 165-8.
  6. Wakabayashi K., Toyoshima Y., Awamori K. et al. Restricted occurrence of Lewy bodies in the dorsal vagal nucleus in a patient with late-onset parkinsonism. J. Neurol. Sci. 1999; 165(2): 188-91.
  7. Polymeropoulos M.H., Lavedan C., Leroy E. et al. Mutation in the alpha-synuclein gene identified in families with Parkinson's disease. Science 1997; 276(5321): 2045-7.
  8. Spillantini M.G., Schmidt M.L., Lee V.M. et al. α-Synuclein in Lewy bodies. Nature 1997; 388(6645): 839-40.
  9. Spillantini M.G., Crowther R.A., Jakes R. et al. Filamentous alpha-synuclein inclusions link multiple system atrophy with Parkinson's disease and dementia with Lewy bodies. Neurosci. Lett. 1998; 251(3): 205-8.
  10. Wakabayashi K., Yoshimoto M., Tsuji S. et al. Alpha-synuclein immunoreactivity in glial cytoplasmic inclusions in multiple system atrophy. Neurosci. Lett. 1998; 249(2-3): 180-2.
  11. Gelb D.J., Oliver E., Gilman S. Diagnostic criteria for Parkinson disease. Arch. Neurol. 1999; 56(1): 33-9.
  12. Poewe W., Antonini A., Zijlmans J.C. et al. Levodopa in the treatment of Parkinson's disease: an old drug still going strong. Clin. Interv. Aging 2010; 5: 229-38.
  13. Шток В.Н., Федорова Н.В. Болезнь Паркинсона. В: Шток В.Н., Иванова-Смоленская И.А., Левин О.С., редакторы. Экстрапирамидные расстройства. Руководство по диагностике и лечению. Москва: МЕДпресс-информ; 2002. с. 87-124.
  14. Contin M., Riva R., Albani F. et al. Pharmacokinetic optimisation in the treatment of Parkinson's disease. Clin. Pharmacokinet. 1996; 30(6): 463-81.
  15. Ciesielska A., Sharma N., Beyer J. et al. Carbidopa-based modulation of the functional effect of the AAV2-hAADC gene therapy in 6-OHDA lesioned rats. PLoS One 2015; 10(4): 1-14.
  16. Forsayeth J.R., Eberling J.L., Sanftner L.M. et al. A Dose-ranging study of AAV-hAADC therapy in parkinsonian monkeys. Mol. Ther. 2009; 14(4): 571-7.
  17. Christine C.W., Starr P.A., Larson P.S. et al. Safety and tolerability of putaminal AADC gene therapy for Parkinson disease. Neurology 2009; 73(20): 1662-9.
  18. Mittermeyer G., Christine C.W., Rosenbluth K.H. et al. Long-term evaluation of a phase 1 study of AADC gene therapy for Parkinson's disease. Hum. Gene Ther. 2012; 23(4): 377-81.
  19. Князькина Ю.А. Оценка эффективности терапии пирибедилом пациентов с болезнью Паркинсона при моторных флуктуациях и лекарственных дискинезиях. В: Иллариошкин С.Н., Левин О.С., редакторы. Болезнь Паркинсона и расстройство движений. Москва: ЗАО «рКи Соверо пресс»; 2014. с. 195-7.
  20. Goetz C.G., Poewe W., Rascol O. et al. Evidence-based medical review update: Pharmacological and surgical treatments of Parkinson's disease: 2001 to 2004. Mov. Disord. 2005; 20(5): 523-39.
  21. Федорова Н.В., Шток В.Н. Стратегия и тактика лечения болезни Паркинсона. Cons. Medicum 2001; 5: 237-40.
  22. Яхно Н.Н., Нодель М. Современные принципы терапии болезни Паркинсона. РМЖ 2010; 10: 418.
  23. Rodriguez R.L., Fernandez H.H., Haq I. et al. Pearls in Patient Selection for Deep Brain Stimulation. Neurologist 2007; 13(5): 253-60.
  24. Shih L.C., Tarsy D. Deep brain stimulation for the treatment of atypical parkinsonism. Mov. Disord. 2007; 22(15): 2149-55.
  25. Li Z., Lin Q., Huang W. et al. Target gene capture sequencing in Chinese population of sporadic Parkinson disease. Medicine (Baltimore) 2015; 94(20): e836.
  26. Nuytemans K., Bademci G., Inchausti V. et al. Whole exome sequencing of rare variants in EIF4G1 and VPS35 in Parkinson disease. Neurology 2013; 80(11): 982-9.
  27. Dansithong W., Paul S., Scoles D.R. et al. Generation of SNCA Cell Models Using Zinc Finger Nuclease (ZFN) Technology for Efficient High-Throughput Drug Screening. PLoS One 2015; 10(8): e0136930.
  28. Soldner F., Laganière J., Cheng A.W. et al. Generation of isogenic pluripotent stem cells differing exclusively at two early onset Parkinson point mutations. Cell 2011; 146(2): 318-31.
  29. Dow L.E., Fisher J., O'Rourke K.P. et al. Inducible in vivo genome editing with CRISPR-Cas9. Nat. Biotechnol. 2015; 33(4): 390-4.
  30. Zhou X., Xin J., Fan N. et al. Generation of CRISPR/Cas9-mediated gene-targeted pigs via somatic cell nuclear transfer. Cell. Mol. Life Sci. 2015; 72(6): 1175-84.
  31. Wang X., Cao C., Huang J. et al. One-step generation of triple gene- targeted pigs using CRISPR/Cas9 system. Sci. Rep. 2016; 9(6): 1-7.
  32. Soldner F., Stelzer Y., Shivalila C.S. et al. Parkinson-associated risk variant in distal enhancer of а-synuclein modulates target gene expression. Nature 2016; 533(7601): 95-9.
  33. Nalls M.A., Pankratz N., Lill C.M. et al. Large-scale metaanalysis of genome-wide association data identifies six new risk loci for Parkinson's disease. Nat. Genet. 2014; 46(9): 989-93.
  34. Abeliovich A., Rhinn H. Parkinson's disease: Guilt by genetic association. Nature 2016; 533(7601): 40-1.
  35. Devine M.J., Gwinn K., Singleton A. et al. Parkinson's disease and а-synuclein expression. Mov. Disord. 2011; 26(12): 2160-8.
  36. Liu Z., Wang X., Yu Y. et al. A Drosophila model for LRRK2-linked parkinsonism. PNAS USA 2008; 105(7): 2693-8.
  37. Feany M.B., Bender W.W. A Drosophila model of Parkinson's disease. Nature 2000; 404(6776): 394-8.
  38. McGurk L., Berson A., Bonini N.M. Drosophila as an In Vivo Model for Human Neurodegenerative Disease. Genetics 2015; 201(2): 377-402.
  39. Yao C., El Khoury R., Wang W. et al. LRRK2-mediated neurodegeneration and dysfunction of dopaminergic neurons in a Caenorhabditis elegans model of Parkinson's disease. Neurobiol. Dis. 2010; 40(1): 73-81.
  40. Fu R.H., Harn H.J., Liu S.P. et al. n-butylidenephthalide protects against dopaminergic neuron degeneration and α-synuclein accumulation in Caenorhabditis elegans models of Parkinson's disease. PLoS One 2014; 9(1): e85305.
  41. Vera E., Studer L. When rejuvenation is a problem: challenges of modeling late-onset neurodegenerative disease. Development 2015; 142(18): 3085-9.
  42. Bombardier J.P., Munson M. Three steps forward, two steps back: Mechanistic insights into the assembly and disassembly of the SNARE complex. Curr. Opin. Chem. Biol. 2015; 29: 66-71.
  43. Burré J., Sharma M., Tsetsenis T. et al. Alpha-synuclein promotes SNARE-complex assembly in vivo and in vitro. Science 2010; 329(5999): 1663-7.
  44. Bungeroth M., Appenzeller S., Regulin A. et al. Differential aggregation properties of alpha-synuclein isoforms. Neurobiol. Aging 2014; 35(8): 1913-9.
  45. Eckermann K., Kügler S., Bähr M. Dimerization propensities of Synucleins are not predictive for Synuclein aggregation. Biochim. Biophys. Acta - Mol. Basis Dis. 2015; 1852(8): 1658-64.
  46. Lopez de Maturana R., Aguila J.C., Sousa A. et al. Leucine-rich repeat kinase 2 modulates cyclooxygenase 2 and the inflammatory response in idiopathic and genetic Parkinson's disease. Neurobiol. Aging 2014; 35(5): 1116-24.
  47. Lippolis R., Siciliano R.A., Pacelli C. et al. Altered protein expression pattern in skin fibroblasts from parkin-mutant early-onset Parkinson's disease patients. Biochim. Biophys. Acta - Mol. Basis Dis. 2015; 1852(9): 1960-70.
  48. Amano T., Papanikolaou T., Sung L.Y. et al. Nuclear Transfer Embryonic Stem Cells Provide an In Vitro Culture Model for Parkinson's Disease. Cloning Stem Cells 2009; 11(1): 77-88.
  49. Friling S., Andersson E., Thompson L.H. et al. Efficient production of mesencephalic dopamine neurons by Lmx1a expression in embryonic stem cells. PNAS USA 2009; 106(18): 7613-8.
  50. Tian L.P., Zhang S., Zhang Y.J. et al. Lmx1b can promote the differentiation of embryonic stem cells to dopaminergic neurons associated with Parkinson's disease. Biotechnol. Lett. 2012; 34(7): 1167-74.
  51. Kim D.W., Chung S., Hwang M. et al. Stromal Cell-Derived Inducing Activity, Nurr1, and Signaling Molecules Synergistically Induce Dopaminergic Neurons from Mouse Embryonic Stem Cells. Stem Cells 2006; 24(3): 557-67.
  52. Chung S., Hedlund E., Hwang M. et al. The homeodomain transcription factor Pitx3 facilitates differentiation of mouse embryonic stem cells into AHD2-expressing dopaminergic neurons. Mol. Cell. Neurosci. 2005; 28(2): 241-52.
  53. Park I.H., Arora N., Huo H. et al. Disease-specific induced pluripotent stem cells. Cell 2008; 134(5): 877-86.
  54. Sanders L.H., Laganière J., Cooper O. et al. LRRK2 mutations cause mitochondrial DNA damage in iPSC-derived neural cells from Parkinson's disease patients: reversal by gene correction. Neurobiol. Dis. 2014; 62: 381-6.
  55. Liu G.H., Qu J., Suzuki K. et al. Progressive degeneration of human neural stem cells caused by pathogenic LRRK2. Nature 2012; 491(7425): 603-7.
  56. Cooper O., Seo H., Andrabi S. et al. Familial Parkinson's disease iPSCs show cellular deficits in mitochondrial responses that can be pharmacologically rescued. Sci. Transl. Med. 2012; 4(141): 141ra90.
  57. Imaizumi Y., Okada Y., Akamatsu W. et al. Mitochondrial dysfunction associated with increased oxidative stress and α-synuclein accumulation in PARK2 iPSC-derived neurons and postmortem brain tissue. Mol. Brain 2012; 5(1): 35.
  58. Sánchez-Danés A., Richaud-Patin Y., Carballo-Carbajal I. et al. Disease-specific phenotypes in dopamine neurons from human iPS-based models of genetic and sporadic Parkinson's disease. EMBO Mol. Med. 2012; 4(5): 380-95.
  59. Nguyen H.N., Byers B., Cord B. et al. LRRK2 mutant iPSC-derived DA neurons demonstrate increased susceptibility to oxidative stress. Cell Stem Cell 2011; 8(3): 267-80.
  60. Orenstein S.J., Kuo S.H., Tasset I. et al. Interplay of LRRK2 with chaperone-mediated autophagy. Nat. Neurosci. 2013; 16(4): 394-406.
  61. Reinhardt P., Schmid B., Burbulla L.F. et al. Genetic Correction of a LRRK2 Mutation in Human iPSCs Links Parkinsonian Neurodegeneration to ERK-Dependent Changes in Gene Expression. Cell Stem Cell 2013; 12(3): 354-67.
  62. Некрасов Е.Д., Лебедева О.С., Честков И.В. и соавт. Получение и характеристика индуцированных плюрипотентных стволовых клеток человека из фибробластов кожи пациентов с нейродегенеративными заболеваниями. Клеточная трансплантология и тканевая инженерия 2011; 6(4): 82-8.
  63. Ветчинова А.С., Коновалова Е.В., Волчков П.Ю. и соавт. Редактирование генома на клеточной модели генетической формы болезни Паркинсона. Гены и Клетки 2016; 11(2): 114-8.
  64. Лебедева О.С., Лагарькова М.А., Киселев С.Л. и соавт. Морфофункциональные свойства индуцированных плюрипотентных стволовых клеток, полученных из фибробластов кожи человека и дифференцированных в дофаминергические нейроны. Нейрохимия 2013; 30(3): 233-41.
  65. Haugarvoll K., Rademakers R., Kachergus J.M. et al. Lrrk2 R1441C parkinsonism is clinically similar to sporadic Parkinson disease. Neurology 2008; 70tIssue 16, Part 2): 1456-60.
  66. Atashrazm F., Dzamko N. LRRK2 inhibitors and their potential in the treatment of Parkinson's disease: current perspectives. Clin. Pharmacol. 2016; 8: 177-189.
  67. Greggio E., Jain S., Kingsbury A. et al. Kinase activity is required for the toxic effects of mutant LRRK2/dardarin. Neurobiol. Dis. 2006; 23(2): 329-41.
  68. Heo H.Y., Park J.M., Kim C.H. et al. LRRK2 enhances oxidative stress-induced neurotoxicity via its kinase activity. Exp. Cell Res. 2010; 316(4): 649-56.
  69. Liu Z., Wang X., Yu Y. et al. A Drosophila model for LRRK2-linked parkinsonism. PNAS USA 2008; 105(7): 2693-8.
  70. Yao C., El Khoury R., Wang W. et al. LRRK2-mediated neurodegeneration and dysfunction of dopaminergic neurons in a Caenorhabditis elegans model of Parkinson's disease. Neurobiol. Dis. 2010; 40(1): 73-81.
  71. Ramonet D., Daher J.P., Lin B.M. et al. Dopaminergic Neuronal Loss, Reduced Neurite Complexity and Autophagic Abnormalities in Transgenic Mice Expressing G2019S Mutant LRRK2. PLoS One 2011; 6(4): e18568.
  72. Estrada A.A., Chan B.K., Baker-Glenn C. et al. Discovery of Highly Potent, Selective, and Brain-Penetrant Aminopyrazole Leucine-Rich Repeat Kinase 2 (LRRK2) Small Molecule Inhibitors. J. Med. Chem. 2014; 57(3): 921-36.
  73. Fuji R.N., Flagella M., Baca M. et al. Effect of selective LRRK2 kinase inhibition on nonhuman primate lung. Sci. Transl. Med. 2015; 7(273): 273ra15.
  74. Fell M.J., Mirescu C., Basu K. et al. MLi-2, a Potent, Selective, and Centrally Active Compound for Exploring the Therapeutic Potential and Safety of LRRK2 Kinase Inhibition. J. Pharmacol. Exp. Ther. 2015; 355(3): 397-409.
  75. Russo I., Bubacco L., Greggio E. LRRK2 and neuroinflammation: partners in crime in Parkinson's disease? J. Neuroinflammation 2014; 11(1): 52.
  76. Umeno J., Asano K., Matsushita T. et al. Meta-analysis of published studies identified eight additional common susceptibility loci for Crohn's disease and ulcerative colitis. Inflamm. Bowel Dis. 2011; 17(12): 2407-15.
  77. Zhang F.R., Huang W., Chen S.M. et al. Genomewide association study of leprosy. N. Engl. J. Med. 2009; 361(27): 2609-18.
  78. Gardet A., Benita Y., Li C. et al. LRRK2 is involved in the IFN-gamma response and host response to pathogens. J. Immunol. 2010; 185(9): 5577-85.
  79. Moehle M.S., Webber P.J., Tse T. et al. LRRK2 inhibition attenuates microglial inflammatory responses. J. Neurosci. 2012; 32(5): 1602-11.
  80. Liu Z., Lee J., Krummey S. et al. The kinase LRRK2 is a regulator of the transcription factor NFAT that modulates the severity of inflammatory bowel disease. Nat. Immunol. 2011; 12(11): 1063-70.
  81. Dai W., Zhang G., Makeyev E.V. RNA-binding protein HuR autoregulates its expression by promoting alternative polyadenylation site usage. Nucleic Acids Res. 2012; 40(2): 787-800.
  82. Khabar K.S. Post-transcriptional control during chronic inflammation and cancer: a focus on AU-rich elements. Cell. Mol. Life Sci. 2010; 67(17): 2937-55.
  83. Lorez de Maturana R., Lang V., Zubiarrain A. et al. Mutations in LRRK2 impair NF-к B pathway in iPSC-derived neurons. J. Neuroinflammation 2016; 13(1): 295.
  84. Marder K., Wang Y., Alcalay R.N. et al. Age-specific penetrance of LRRK2 G2019S in the Michael J. Fox Ashkenazi Jewish LRRK2 Consortium. Neurology 2015; 85(1): 89-95.
  85. Latourelle J.C., Sun M., Lew M.F. et al. The Gly2019Ser mutation in LRRK2 is not fully penetrant in familial Parkinson's disease: the GenePD study. BMC Med. 2008; 6: 32.
  86. Dächsel J.C., Behrouz B., Yue M. et al. A comparative study of Lrrk2 function in primary neuronal cultures. Parkinsonism Relat. Disord. 2010; 16(10): 650-5.
  87. Tong Y., Giaime E., Yamaguchi H. et al. Loss of leucine-rich repeat kinase 2 causes age-dependent bi-phasic alterations of the autophagy pathway. Mol. Neurodegener. 2012; 7(1): 2.
  88. Jacobs B.M. Stemming the Hype: What can we learn from iPSC models of parkinson's disease and how can we learn it? J. Parkinson's Dis. 2014; 4(1): 15-27.
  89. Lavedan C. The synuclein family. Genome Res. 1998; 8(9): 871-80.
  90. Stefanova N., Wenning G.K. Review: Multiple system atrophy: emerging targets for interventional therapies. Neuropathol. Appl. Neurobiol. 2016; 42(1): 20-32.
  91. Sonnen J.A., Postupna N., Larson E.B. et al. Pathologic correlates of dementia in individuals with Lewy body disease. Brain Pathol. 2010; 20(3): 654-9.
  92. Wang Q., Tian Q., Song X. et al. One-step generation of triple gene-targeted pigs using CRISPR/Cas9 system. J. Clin. Lab. Anal. 2016; 30(6): 1092-9.
  93. Singleton A.B., Farrer M., Johnson J. et al. а-Synuclein Locus Triplication Causes Parkinson's Disease. Science 2003; 302(5646): 841.
  94. Devine M.J., Ryten M., Vodicka P. et al. Parkinson's disease induced pluripotent stem cells with triplication of the а-synuclein locus. Nat. Commun. 2011; 2: 440.
  95. Byers B., Cord B., Nguyen H.N. et al. SNCA Triplication Parkinson's Patient's iPSC-derived DA Neurons Accumulate а-Synuclein and Are Susceptible to Oxidative Stress. PLoS One 2011; 6(11): e26159.
  96. Chung C.Y., Khurana V., Auluck P.K. et al. Identification and Rescue of -Synuclein Toxicity in Parkinson Patient-Derived Neurons. Science 2013; 342(6161): 983-7.
  97. Ryan S.D., Dolatabadi N., Chan S.F. et al. Isogenic Human iPSC Parkinson's Model Shows Nitrosative Stress-Induced Dysfunction in MEF2-PGC^ Transcription. Cell 2013; 155(6): 1351-64.
  98. Fakhree M.A., Zijlstra N., Raiss C.C. et al. The number of а-synuclein proteins per vesicle gives insights into its physiological function. Sci. Rep. 2016; 6: 30658.
  99. Braun A.R., Sevcsik E., Chin P. et al. α-Synuclein Induces Both Positive Mean Curvature and Negative Gaussian Curvature in Membranes. J. Am. Chem. Soc. 2012; 134(5): 2613-20.
  100. Braun A.R., Lacy M.M., Ducas V.C. et al. а-Synuclein-Induced Membrane Remodeling Is Driven by Binding Affinity, Partition Depth, and Interleaflet Order Asymmetry. J. Am. Chem. Soc. 2014; 136(28): 9962-72.
  101. Varkey J., Isas J.M., Mizuno N. et al. Membrane curvature induction and tubulation are common features of synucleins and apolipoproteins. J. Biol. Chem. 2010; 285(42): 32486-93.
  102. Sidhu A., Wersinger C., Moussa C.E. et al. The role of а-synuclein in both neuroprotection and neurodegeneration. Ann. N. Y. Acad. Sci. 2004; 1035: 250-70.
  103. Mayer E.A., Padua D., Tillisch K. Altered brain-gut axis in autism: Comorbidity or causative mechanisms? BioEssays 2014; 36(10): 933-9.
  104. Sharon G., Sampson T.R., Geschwind D.H. et al. The Central Nervous System and the Gut Microbiome. Cell 2016; 167(4): 915-32.
  105. Schroeder B.O., Bäckhed F. Signals from the gut microbiota to distant organs in physiology and disease. Nat. Med. 2016; 22(10): 1079-89.
  106. Selkrig J., Wong P., Zhang X. et al. Metabolic tinkering by the gut microbiome. Gut Microbes 2014; 5(3): 369-80.
  107. Wall R., Cryan J.F., Ross R.P. et al. Bacterial Neuroactive Compounds Produced by Psychobiotics. Adv. Exp. Med. Biol. 2014; 817: 221-39.
  108. Sampson T.R., Debelius J.W., Thron T. et al. Gut Microbiota Regulate Motor Deficits and Neuroinflammation in a Model of Parkinson's Disease. Cell 2016; 167(6): 1469-80.
  109. Kannarkat G.T., Boss J.M., Tansey M.G. The role of innate and adaptive immunity in Parkinson's disease. J. Parkinson's Dis. 2013; 3(4): 493-514.
  110. Sanchez-Guajardo V., Barnum C.J., Tansey M.G. et al. Neuroimmunological processes in Parkinson's disease and their relation to а-synuclein: microglia as the referee between neuronal processes and peripheral immunity. ASN Neuro 2013; 5(2): 113-39.
  111. Gao H.M., Zhang F., Zhou H. et al. Neuroinflammation and а-Synuclein Dysfunction Potentiate Each Other, Driving Chronic Progression of Neurodegeneration in a Mouse Model of Parkinson's Disease. Environ. Health Perspect. 2011; 119(6): 807-14.
  112. Shimura H., Hattori N., Kubo S. et al. Familial Parkinson disease gene product, parkin, is a ubiquitin-protein ligase. Nat. Genet. 2000; 25(3): 302-5.
  113. Kalia L.V., Lang A.E. Parkinson's disease. Lancet 2015; 386(9996): 896-912.
  114. Rakovic A., Shurkewitsch K., Seibler P. et al. Phosphatase and tensin homolog (PTEN)-induced putative kinase 1 (PINK1)-dependent ubiquitination of endogenous Parkin attenuates mitophagy: study in human primary fibroblasts and induced pluripotent stem cell-derived neurons. J. Biol. Chem. 2013; 288(4): 2223-37.
  115. Seibler P., Graziotto J., Jeong H. et al. Mitochondrial Parkin recruitment is impaired in neurons derived from mutant PINK1 induced pluripotent stem cells. J. Neurosci. 2011; 31(16): 5970-6.
  116. de Lau L.M., Breteler M.M. Epidemiology of Parkinson's disease. Lancet Neurol. 2006; 5(6): 525-35.
  117. Jiang H., Ren Y., Yuen E.Y. et al. Parkin controls dopamine utilization in human midbrain dopaminergic neurons derived from induced pluripotent stem cells. Nat. Commun. 2012; 3: 668.
  118. Ren Y., Jiang H., Hu Z. et al. Parkin Mutations Reduce the Complexity of Neuronal Processes in iPSC-Derived Human Neurons. Stem Cells 2015; 33(1): 68-78.
  119. Aharon-Peretz J., Rosenbaum H., Gershoni-Baruch R. Mutations in the glucocerebrosidase gene and Parkinson's disease in Ashkenazi Jews. N. Engl. J. Med. 2004; 351(19): 1972-7.
  120. Migdalska-Richards A., Schapira A.H. The relationship between glucocerebrosidase mutations and Parkinson disease. J. Neurochem. 2016; 139 Suppl 1: 77-90.
  121. Corti O., Lesage S., Brice A. What genetics tells us about the causes and mechanisms of Parkinson's disease. Physiol. Rev. 2011; 91(4): 1161-218.
  122. Panicker L.M., Miller D., Park T.S. et al. Induced pluripotent stem cell model recapitulates pathologic hallmarks of Gaucher disease. PNAS USA 2012; 109(44): 18054-9.
  123. Lesage S., Brice A. Parkinson's disease: from monogenic forms to genetic susceptibility factors. Hum. Mol. Genet. 2009; 18(R1): 48-59.
  124. Kang J.F., Tang B.S., Guo J.F. The Progress of Induced Pluripotent Stem Cells as Models of Parkinson's Disease. Stem Cells Int. 2016; 2016: 4126214.
  125. Olszewska D.A., Fearon C., Lynch T. Novel gene (TMEM230) linked to Parkinson's disease. J. Clin. Mov. Disord. 2016; 3: 17.
  126. Majidinia M., Mihanfar A., Rahbarghazi R. et al. The roles of non-coding RNAs in Parkinson's disease. Mol. Biol. Rep. 2016; 43(11): 1193-204.
  127. Bartel D.P. MicroRNAs: genomics, biogenesis, mechanism, and function. Cell 2004; 116(2): 281-97.
  128. Esteller M. Non-coding RNAs in human disease. Nat. Rev. Genet. 2011; 12(12): 861-74.
  129. Macrae I.J., Zhou K., Li F. et al. Structural basis for double-stranded RNA processing by Dicer. Science 2006; 311(5758): 195-8.
  130. Kim J., Inoue K., Ishii J. et al. A MicroRNA Feedback Circuit in Midbrain Dopamine Neurons. Science 2007; 317(5842): 1220-4.
  131. Doxakis E. Post-transcriptional regulation of alpha-synuclein expression by mir-7 and mir-153. J. Biol. Chem. 2010; 285(17): 12726-34.
  132. Junn E., Lee K.W., Jeong B.S. et al. Repression of -synuclein expression and toxicity by microRNA-7. PNAS Usa 2009; 106(31): 13052-7.
  133. Margis R., Margis R., Rieder C.R. Identification of blood microRNAs associated to Parkinsons disease. J. Biotechnol. 2011; 152(3): 96-101.
  134. Cardo L.F., Coto E., Mena L. et al. Profile of microRNAs in the plasma of Parkinson's disease patients and healthy controls. J. Neurol. 2013; 260(5): 1420-22.
  135. Soreq L., Salomonis N., Bronstein M. et al. Small RNA sequencing-microarray analyses in Parkinson leukocytes reveal deep brain stimulation-induced splicing changes that classify brain region transcriptomes. Front. Mol. Neurosci. 2013; 6: 10.
  136. Cho H.J., Liu G., Jin S.M. et al. MicroRNA-205 regulates the expression of Parkinson's disease-related leucine-rich repeat kinase 2 protein. Hum. Mol. Genet. 2013; 22(3): 608-20.
  137. Minones-Moyano E., Porta S., Escaramis G. et al. MicroRNA profiling of Parkinson's disease brains identifies early downregulation of miR-34b/c which modulate mitochondrial function. Hum. Mol. Genet. 2011; 20(15): 3067-78.
  138. Miller J.D., Ganat Y.M., Kishinevsky S. et al. Human iPSC-based modeling of late-onset disease via progerin-induced aging. Cell Stem Cell 2013; 13(6): 691-705.
  139. Mazzulli J.R., Xu Y.H., Sun Y. et al. Gaucher Disease Glucocerebrosidase and а-Synuclein Form a Bidirectional Pathogenic Loop in Synucleinopathies. Cell 2011; 146(1): 37-52.

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