Optogenetic delivery of trophic signals in a genetic model of Parkinson’s disease
Autoři:
Alvaro Ingles-Prieto aff001; Nikolas Furthmann aff002; Samuel H. Crossman aff003; Alexandra-Madelaine Tichy aff003; Nina Hoyer aff005; Meike Petersen aff005; Vanessa Zheden aff001; Julia Biebl aff001; Eva Reichhart aff001; Attila Gyoergy aff001; Daria E. Siekhaus aff001; Peter Soba aff005; Konstanze F. Winklhofer aff002; Harald Janovjak aff001
Působiště autorů:
Institute of Science and Technology Austria (IST Austria), Klosterneuburg, Austria
aff001; Molecular Cell Biology, Institute of Biochemistry and Pathobiochemistry, Ruhr University Bochum, Bochum, Germany
aff002; Australian Regenerative Medicine Institute (ARMI), Faculty of Medicine, Nursing and Health Sciences, Monash University, Clayton/Melbourne, Australia
aff003; European Molecular Biology Laboratory Australia (EMBL Australia), Monash University, Clayton/Melbourne, Australia
aff004; Center for Molecular Neurobiology (ZMNH), University Medical Center Hamburg-Eppendorf, Hamburg, Germany
aff005
Vyšlo v časopise:
Optogenetic delivery of trophic signals in a genetic model of Parkinson’s disease. PLoS Genet 17(4): e1009479. doi:10.1371/journal.pgen.1009479
Kategorie:
Research Article
doi:
https://doi.org/10.1371/journal.pgen.1009479
Souhrn
Optogenetics has been harnessed to shed new mechanistic light on current and future therapeutic strategies. This has been to date achieved by the regulation of ion flow and electrical signals in neuronal cells and neural circuits that are known to be affected by disease. In contrast, the optogenetic delivery of trophic biochemical signals, which support cell survival and are implicated in degenerative disorders, has never been demonstrated in an animal model of disease. Here, we reengineered the human and Drosophila melanogaster REarranged during Transfection (hRET and dRET) receptors to be activated by light, creating one-component optogenetic tools termed Opto-hRET and Opto-dRET. Upon blue light stimulation, these receptors robustly induced the MAPK/ERK proliferative signaling pathway in cultured cells. In PINK1B9 flies that exhibit loss of PTEN-induced putative kinase 1 (PINK1), a kinase associated with familial Parkinson’s disease (PD), light activation of Opto-dRET suppressed mitochondrial defects, tissue degeneration and behavioral deficits. In human cells with PINK1 loss-of-function, mitochondrial fragmentation was rescued using Opto-dRET via the PI3K/NF-кB pathway. Our results demonstrate that a light-activated receptor can ameliorate disease hallmarks in a genetic model of PD. The optogenetic delivery of trophic signals is cell type-specific and reversible and thus has the potential to inspire novel strategies towards a spatio-temporal regulation of tissue repair.
Klíčová slova:
Mitochondria – Optogenetics – Drosophila melanogaster – Light – Parkinson disease – Retina – Signal processing – Transfection
Zdroje
1. Johnson HE, Toettcher JE. Illuminating developmental biology with cellular optogenetics. Curr Opin Biotechnol. 2018;52: 42–8. doi: 10.1016/j.copbio.2018.02.003 29505976
2. Guglielmi G, Falk HJ, De Renzis S. Optogenetic control of protein function: From intracellular processes to tissue morphogenesis. Trends Cell Biol. 2016;26(11): 864–74. doi: 10.1016/j.tcb.2016.09.006 27727011
3. Deisseroth K. Optogenetics: 10 years of microbial opsins in neuroscience. Nat Neurosci. 2015;18(9): 1213–25. doi: 10.1038/nn.4091 26308982
4. Bugaj LJ, Sabnis AJ, Mitchell A, Garbarino JE, Toettcher JE, Bivona TG, et al. Cancer mutations and targeted drugs can disrupt dynamic signal encoding by the Ras-Erk pathway. Science. 2018;361(6405). doi: 10.1126/science.aao3048 30166458
5. Wilson MZ, Ravindran PT, Lim WA, Toettcher JE. Tracing information flow from erk to target gene induction reveals mechanisms of dynamic and combinatorial control. Mol Cell. 2017;67(5): 757–69 e5. doi: 10.1016/j.molcel.2017.07.016 28826673
6. Agus V, Janovjak H. Optogenetic methods in drug screening: technologies and applications. Curr Opin Biotechnol. 2017;48: 8–14. doi: 10.1016/j.copbio.2017.02.006 28273648
7. Ordaz JD, Wu W, Xu XM. Optogenetics and its application in neural degeneration and regeneration. Neural Regen Res. 2017;12(8): 1197–209. doi: 10.4103/1673-5374.213532 28966628
8. Tye KM, Deisseroth K. Optogenetic investigation of neural circuits underlying brain disease in animal models. Nat Rev Neurosci. 2012;13(4): 251–66. doi: 10.1038/nrn3171 22430017
9. Gradinaru V, Mogri M, Thompson KR, Henderson JM, Deisseroth K. Optical deconstruction of parkinsonian neural circuitry. Science. 2009;324(5925): 354–9. doi: 10.1126/science.1167093 19299587
10. Steinbeck JA, Choi SJ, Mrejeru A, Ganat Y, Deisseroth K, Sulzer D, et al. Optogenetics enables functional analysis of human embryonic stem cell-derived grafts in a Parkinson’s disease model. Nat Biotechnol. 2015;33(2): 204–9. doi: 10.1038/nbt.3124 25580598
11. Busskamp V, Duebel J, Balya D, Fradot M, Viney TJ, Siegert S, et al. Genetic reactivation of cone photoreceptors restores visual responses in retinitis pigmentosa. Science. 2010;329(5990): 413–7. doi: 10.1126/science.1190897 20576849
12. Kleinlogel S, Vogl C, Jeschke M, Neef J, Moser T. Emerging Approaches for Restoration of Hearing and Vision. Physiol Rev. 2020;100(4): 1467–525. doi: 10.1152/physrev.00035.2019 32191560
13. Bryson JB, Machado CB, Crossley M, Stevenson D, Bros-Facer V, Burrone J, et al. Optical control of muscle function by transplantation of stem cell-derived motor neurons in mice. Science. 2014;344(6179): 94–7. doi: 10.1126/science.1248523 24700859
14. Bruegmann T, Malan D, Hesse M, Beiert T, Fuegemann CJ, Fleischmann BK, et al. Optogenetic control of heart muscle in vitro and in vivo. Nat Methods. 2010;7(11): 897–900. doi: 10.1038/nmeth.1512 20881965
15. Grusch M, Schelch K, Riedler R, Reichhart E, Differ C, Berger W, et al. Spatio-temporally precise activation of engineered receptor tyrosine kinases by light. EMBO J. 2014;33(15): 1713–26. doi: 10.15252/embj.201387695 24986882
16. Kim N, Kim JM, Lee M, Kim CY, Chang KY, Heo WD. Spatiotemporal control of fibroblast growth factor receptor signals by blue light. Chem Biol. 2014;21(7): 903–12. doi: 10.1016/j.chembiol.2014.05.013 24981772
17. Krishnamurthy VV, Khamo JS, Mei W, Turgeon AJ, Ashraf HM, Mondal P, et al. Reversible optogenetic control of kinase activity during differentiation and embryonic development. Development. 2016;143(21): 4085–94. doi: 10.1242/dev.140889 27697903
18. Huang P, Liu A, Song Y, Hope JM, Cui B, Duan L. Optical Activation of TrkB Signaling. J Mol Biol. 2020;432(13): 3761–70. doi: 10.1016/j.jmb.2020.05.002 32422149
19. Bunnag N, Tan QH, Kaur P, Ramamoorthy A, Sung ICH, Lusk J, et al. An optogenetic method to study signal transduction in intestinal stem cell homeostasis. J Mol Biol. 2020;432(10): 3159–76. doi: 10.1016/j.jmb.2020.03.019 32201167
20. Takahashi M, Ritz J, Cooper GM. Activation of a novel human transforming gene, ret, by DNA rearrangement. Cell. 1985;42(2): 581–8. doi: 10.1016/0092-8674(85)90115-1 2992805
21. Bjorklund A, Kirik D, Rosenblad C, Georgievska B, Lundberg C, Mandel RJ. Towards a neuroprotective gene therapy for Parkinson’s disease: use of adenovirus, AAV and lentivirus vectors for gene transfer of GDNF to the nigrostriatal system in the rat Parkinson model. Brain Res. 2000;886(1–2): 82–98. doi: 10.1016/s0006-8993(00)02915-2 11119690
22. Olanow CW, Bartus RT, Volpicelli-Daley LA, Kordower JH. Trophic factors for Parkinson’s disease: To live or let die. Movement disorders: official journal of the Movement Disorder Society. 2015;30(13): 1715–24. doi: 10.1002/mds.26426 26769457
23. Warren Olanow C, Bartus RT, Baumann TL, Factor S, Boulis N, Stacy M, et al. Gene delivery of neurturin to putamen and substantia nigra in Parkinson disease: A double-blind, randomized, controlled trial. Annals of neurology. 2015;78(2): 248–57. doi: 10.1002/ana.24436 26061140
24. Marks WJ Jr., Bartus RT, Siffert J, Davis CS, Lozano A, Boulis N, et al. Gene delivery of AAV2-neurturin for Parkinson’s disease: a double-blind, randomised, controlled trial. Lancet Neurol. 2010;9(12): 1164–72. doi: 10.1016/S1474-4422(10)70254-4 20970382
25. Manfredsson FP, Tumer N, Erdos B, Landa T, Broxson CS, Sullivan LF, et al. Nigrostriatal rAAV-mediated GDNF overexpression induces robust weight loss in a rat model of age-related obesity. Mol Ther. 2009;17(6): 980–91. doi: 10.1038/mt.2009.45 19277011
26. Georgievska B, Kirik D, Bjorklund A. Aberrant sprouting and downregulation of tyrosine hydroxylase in lesioned nigrostriatal dopamine neurons induced by long-lasting overexpression of glial cell line derived neurotrophic factor in the striatum by lentiviral gene transfer. Exp Neurol. 2002;177(2): 461–74. doi: 10.1006/exnr.2002.8006 12429192
27. Kirik D, Rosenblad C, Bjorklund A, Mandel RJ. Long-term rAAV-mediated gene transfer of GDNF in the rat Parkinson’s model: intrastriatal but not intranigral transduction promotes functional regeneration in the lesioned nigrostriatal system. J Neurosci. 2000;20(12): 4686–700. doi: 10.1523/JNEUROSCI.20-12-04686.2000 10844038
28. Barroso-Chinea P, Cruz-Muros I, Afonso-Oramas D, Castro-Hernandez J, Salas-Hernandez J, Chtarto A, et al. Long-term controlled GDNF over-expression reduces dopamine transporter activity without affecting tyrosine hydroxylase expression in the rat mesostriatal system. Neurobiology of disease. 2016;88: 44–54. doi: 10.1016/j.nbd.2016.01.002 26777664
29. Tenenbaum L, Humbert-Claude M. Glial cell line-derived neurotrophic factor gene delivery in Parkinson’s disease: A delicate balance between neuroprotection, trophic effects, and unwanted compensatory mechanisms. Front Neuroanat. 2017;11: 29. doi: 10.3389/fnana.2017.00029 28442998
30. Axelsen TM, Woldbye DPD. Gene therapy for Parkinson’s disease, an update. J Parkinsons Dis. 2018;8(2): 195–215. doi: 10.3233/JPD-181331 29710735
31. Hahn M, Bishop J. Expression pattern of Drosophila ret suggests a common ancestral origin between the metamorphosis precursors in insect endoderm and the vertebrate enteric neurons. Proc Natl Acad Sci USA. 2001;98(3): 1053–8. doi: 10.1073/pnas.021558598 11158593
32. Sugaya R, Ishimaru S, Hosoya T, Saigo K, Emori Y. A Drosophila homolog of human proto-oncogene ret transiently expressed in embryonic neuronal precursor cells including neuroblasts and CNS cells. Mech Dev. 1994;45(2): 139–45. doi: 10.1016/0925-4773(94)90027-2 8199050
33. Myers L, Perera H, Alvarado MG, Kidd T. The Drosophila Ret gene functions in the stomatogastric nervous system with the Maverick TGFbeta ligand and the Gfrl co-receptor. Development. 2018;145(3). doi: 10.1242/dev.157446 29361562
34. Puschmann A, Fiesel FC, Caulfield TR, Hudec R, Ando M, Truban D, et al. Heterozygous PINK1 p.G411S increases risk of Parkinson’s disease via a dominant-negative mechanism. Brain. 2017;140(1): 98–117. doi: 10.1093/brain/aww261 27807026
35. Valente EM, Abou-Sleiman PM, Caputo V, Muqit MM, Harvey K, Gispert S, et al. Hereditary early-onset Parkinson’s disease caused by mutations in PINK1. Science. 2004;304(5674): 1158–60. doi: 10.1126/science.1096284 15087508
36. Valente EM, Salvi S, Ialongo T, Marongiu R, Elia AE, Caputo V, et al. PINK1 mutations are associated with sporadic early-onset parkinsonism. Annals of neurology. 2004;56(3): 336–41. doi: 10.1002/ana.20256 15349860
37. Hewitt VL, Whitworth AJ. Mechanisms of Parkinson’s disease: lessons from Drosophila. Curr Top Dev Biol. 2017;121: 173–200. doi: 10.1016/bs.ctdb.2016.07.005 28057299
38. Voigt A, Berlemann LA, Winklhofer KF. The mitochondrial kinase PINK1: functions beyond mitophagy. J Neurochem. 2016;139 Suppl 1: 232–9. doi: 10.1111/jnc.13655 27251035
39. Vos M, Verstreken P, Klein C. Stimulation of electron transport as potential novel therapy in Parkinson’s disease with mitochondrial dysfunction. Biochem Soc Trans. 2015;43(2): 275–9. doi: 10.1042/BST20140325 25849929
40. Schlee S, Carmillo P, Whitty A. Quantitative analysis of the activation mechanism of the multicomponent growth-factor receptor Ret. Nat Chem Biol. 2006;2(11): 636–44. doi: 10.1038/nchembio823 17013378
41. Jing S, Wen D, Yu Y, Holst PL, Luo Y, Fang M, et al. GDNF-induced activation of the ret protein tyrosine kinase is mediated by GDNFR-alpha, a novel receptor for GDNF. Cell. 1996;85(7): 1113–24. doi: 10.1016/s0092-8674(00)81311-2 8674117
42. Asai N, Iwashita T, Matsuyama M, Takahashi M. Mechanism of activation of the ret proto-oncogene by multiple endocrine neoplasia 2A mutations. Mol Cell Biol. 1995;15(3): 1613–9. doi: 10.1128/mcb.15.3.1613 7532281
43. Freche B, Guillaumot P, Charmetant J, Pelletier L, Luquain C, Christiansen D, et al. Inducible dimerization of RET reveals a specific AKT deregulation in oncogenic signaling. J Biol Chem. 2005;280(44): 36584–91. doi: 10.1074/jbc.M505707200 16123037
44. Read RD, Goodfellow PJ, Mardis ER, Novak N, Armstrong JR, Cagan RL. A Drosophila model of multiple endocrine neoplasia type 2. Genetics. 2005;171(3): 1057–81. doi: 10.1534/genetics.104.038018 15965261
45. Abrescia C, Sjostrand D, Kjaer S, Ibanez CF. Drosophila RET contains an active tyrosine kinase and elicits neurotrophic activities in mammalian cells. FEBS Lett. 2005;579(17): 3789–96. doi: 10.1016/j.febslet.2005.05.075 15978587
46. Takahashi F, Yamagata D, Ishikawa M, Fukamatsu Y, Ogura Y, Kasahara M, et al. AUREOCHROME, a photoreceptor required for photomorphogenesis in stramenopiles. Proc Natl Acad Sci U S A. 2007;104(49): 19625–30. doi: 10.1073/pnas.0707692104 18003911
47. Toyooka T, Hisatomi O, Takahashi F, Kataoka H, Terazima M. Photoreactions of aureochrome-1. Biophys J. 2011;100(11): 2801–9. doi: 10.1016/j.bpj.2011.02.043 21641326
48. Reichhart E, Ingles-Prieto A, Tichy AM, McKenzie C, Janovjak H. A phytochrome sensory domain permits receptor activation by red light. Angew Chem Int Ed Engl. 2016;55(21): 6339–42. doi: 10.1002/anie.201601736 27101018
49. Kennedy MJ, Hughes RM, Peteya LA, Schwartz JW, Ehlers MD, Tucker CL. Rapid blue-light-mediated induction of protein interactions in living cells. Nat Methods. 2010;7(12): 973–5. doi: 10.1038/nmeth.1524 21037589
50. Zoltowski BD, Vaccaro B, Crane BR. Mechanism-based tuning of a LOV domain photoreceptor. Nat Chem Biol. 2009;5(11): 827–34. doi: 10.1038/nchembio.210 19718042
51. Sako K, Pradhan SJ, Barone V, Ingles-Prieto A, Muller P, Ruprecht V, et al. Optogenetic control of nodal signaling reveals a temporal pattern of nodal signaling regulating cell fate specification during gastrulation. Cell Rep. 2016;16(3): 866–77. doi: 10.1016/j.celrep.2016.06.036 27396324
52. Li XZ, Yan J, Huang SH, Zhao L, Wang J, Chen ZY. Identification of a key motif that determines the differential surface levels of RET and TrkB tyrosine kinase receptors and controls depolarization enhanced RET surface insertion. J Biol Chem. 2012;287(3): 1932–45. doi: 10.1074/jbc.M111.283457 22128160
53. Paratcha G, Ledda F, Baars L, Coulpier M, Besset V, Anders J, et al. Released GFRalpha1 potentiates downstream signaling, neuronal survival, and differentiation via a novel mechanism of recruitment of c-Ret to lipid rafts. Neuron. 2001;29(1): 171–84. doi: 10.1016/s0896-6273(01)00188-x 11182089
54. Takahashi M, Asai N, Iwashita T, Murakami H, Ito S. Mechanisms of development of multiple endocrine neoplasia type 2 and Hirschsprung’s disease by ret mutations. Rec Res Cancer Res. 1998;154: 229–36. doi: 10.1007/978-3-642-46870-4_14 10027003
55. Baker NE, Yu SY. The EGF receptor defines domains of cell cycle progression and survival to regulate cell number in the developing Drosophila eye. Cell. 2001;104(5): 699–708. doi: 10.1016/s0092-8674(01)00266-5 11257224
56. Freeman M. Reiterative use of the EGF receptor triggers differentiation of all cell types in the Drosophila eye. Cell. 1996;87(4): 651–60. doi: 10.1016/s0092-8674(00)81385-9 8929534
57. Cagan RL, Ready DF. The emergence of order in the Drosophila pupal retina. Dev Biol. 1989;136(2): 346–62. doi: 10.1016/0012-1606(89)90261-3 2511048
58. Basler K, Christen B, Hafen E. Ligand-independent activation of the sevenless receptor tyrosine kinase changes the fate of cells in the developing Drosophila eye. Cell. 1991;64(6): 1069–81. doi: 10.1016/0092-8674(91)90262-w 2004416
59. Kramer JM, Staveley BE. GAL4 causes developmental defects and apoptosis when expressed in the developing eye of Drosophila melanogaster. Genet Mol Res. 2003;2(1): 43–7. 12917801
60. Wassle H, Riemann HJ. The mosaic of nerve cells in the mammalian retina. Proc R Soc Lond B Biol Sci. 1978;200(1141): 441–61. doi: 10.1098/rspb.1978.0026 26058
61. Cook JE. Spatial properties of retinal mosaics: an empirical evaluation of some existing measures. Vis Neurosci. 1996;13(1): 15–30. doi: 10.1017/s0952523800007094 8730986
62. Johnson HE, Goyal Y, Pannucci NL, Schupbach T, Shvartsman SY, Toettcher JE. The spatiotemporal limits of developmental Erk signaling. Dev Cell. 2017;40(2): 185–92. doi: 10.1016/j.devcel.2016.12.002 28118601
63. Patel AL, Yeung E, McGuire SE, Wu AY, Toettcher JE, Burdine RD, et al. Optimizing photoswitchable MEK. Proc Natl Acad Sci U S A. 2019;116(51): 25756–63. doi: 10.1073/pnas.1912320116 31796593
64. Park J, Lee SB, Lee S, Kim Y, Song S, Kim S, et al. Mitochondrial dysfunction in Drosophila PINK1 mutants is complemented by parkin. Nature. 2006;441(7097): 1157–61. doi: 10.1038/nature04788 16672980
65. Wang D, Qian L, Xiong H, Liu J, Neckameyer WS, Oldham S, et al. Antioxidants protect PINK1-dependent dopaminergic neurons in Drosophila. Proc Natl Acad Sci U S A. 2006;103(36): 13520–5. doi: 10.1073/pnas.0604661103 16938835
66. Yang Y, Gehrke S, Imai Y, Huang Z, Ouyang Y, Wang JW, et al. Mitochondrial pathology and muscle and dopaminergic neuron degeneration caused by inactivation of Drosophila Pink1 is rescued by Parkin. Proc Natl Acad Sci U S A. 2006;103(28): 10793–8. doi: 10.1073/pnas.0602493103 16818890
67. Clark IE, Dodson MW, Jiang C, Cao JH, Huh JR, Seol JH, et al. Drosophila pink1 is required for mitochondrial function and interacts genetically with parkin. Nature. 2006;441(7097): 1162–6. doi: 10.1038/nature04779 16672981
68. Ranganayakulu G, Elliott DA, Harvey RP, Olson EN. Divergent roles for NK-2 class homeobox genes in cardiogenesis in flies and mice. Development. 1998;125(16): 3037–48. 9671578
69. Lin YY, Wu MC, Hsiao PY, Chu LA, Yang MM, Fu CC, et al. Three-wavelength light control of freely moving Drosophila Melanogaster for less perturbation and efficient social-behavioral studies. Biomed Opt Express. 2015;6(2): 514–23. doi: 10.1364/BOE.6.000514 25780741
70. Hori M, Shibuya K, Sato M, Saito Y. Lethal effects of short-wavelength visible light on insects. Sci Rep. 2014;4: 7383. doi: 10.1038/srep07383 25488603
71. Greene JC, Whitworth AJ, Kuo I, Andrews LA, Feany MB, Pallanck LJ. Mitochondrial pathology and apoptotic muscle degeneration in Drosophila parkin mutants. Proc Natl Acad Sci U S A. 2003;100(7): 4078–83. doi: 10.1073/pnas.0737556100 12642658
72. Klein P, Muller-Rischart AK, Motori E, Schonbauer C, Schnorrer F, Winklhofer KF, et al. Ret rescues mitochondrial morphology and muscle degeneration of Drosophila Pink1 mutants. EMBO J. 2014;33(4): 341–55. doi: 10.1002/embj.201284290 24473149
73. Lutz AK, Exner N, Fett ME, Schlehe JS, Kloos K, Lammermann K, et al. Loss of parkin or PINK1 function increases Drp1-dependent mitochondrial fragmentation. J Biol Chem. 2009;284(34): 22938–51. doi: 10.1074/jbc.M109.035774 19546216
74. Meka DP, Muller-Rischart AK, Nidadavolu P, Mohammadi B, Motori E, Ponna SK, et al. Parkin cooperates with GDNF/RET signaling to prevent dopaminergic neuron degeneration. The Journal of clinical investigation. 2015;125(5): 1873–85. doi: 10.1172/JCI79300 25822020
75. Mulligan LM. RET revisited: expanding the oncogenic portfolio. Nat Rev Cancer. 2014;14(3): 173–86. doi: 10.1038/nrc3680 24561444
76. Kramer ER, Liss B. GDNF-Ret signaling in midbrain dopaminergic neurons and its implication for Parkinson disease. FEBS Lett. 2015;589(24 Pt A): 3760–72. doi: 10.1016/j.febslet.2015.11.006 26555190
77. Miller DT, Cagan RL. Local induction of patterning and programmed cell death in the developing Drosophila retina. Development. 1998;125(12): 2327–35. 9584131
78. Guglielmi G, Barry JD, Huber W, De Renzis S. An optogenetic method to modulate cell contractility during tissue morphogenesis. Dev Cell. 2015;35(5): 646–60. doi: 10.1016/j.devcel.2015.10.020 26777292
79. Wang X, He L, Wu YI, Hahn KM, Montell DJ. Light-mediated activation reveals a key role for Rac in collective guidance of cell movement in vivo. Nat Cell Biol. 2010;12(6): 591–7. doi: 10.1038/ncb2061 20473296
80. Greene JC, Whitworth AJ, Andrews LA, Parker TJ, Pallanck LJ. Genetic and genomic studies of Drosophila parkin mutants implicate oxidative stress and innate immune responses in pathogenesis. Hum Mol Genet. 2005;14(6): 799–811. doi: 10.1093/hmg/ddi074 15689351
81. Valadas JS, Esposito G, Vandekerkhove D, Miskiewicz K, Deaulmerie L, Raitano S, et al. ER lipid defects in neuropeptidergic neurons impair sleep patterns in parkinson’s disease. Neuron. 2018;98(6): 1155–69 e6. doi: 10.1016/j.neuron.2018.05.022 29887339
82. Lee JJ, Sanchez-Martinez A, Zarate AM, Beninca C, Mayor U, Clague MJ, et al. Basal mitophagy is widespread in Drosophila but minimally affected by loss of Pink1 or parkin. J Cell Biol. 2018;217(5): 1613–22. doi: 10.1083/jcb.201801044 29500189
83. Vos M, Geens A, Bohm C, Deaulmerie L, Swerts J, Rossi M, et al. Cardiolipin promotes electron transport between ubiquinone and complex I to rescue PINK1 deficiency. J Cell Biol. 2017;216(3): 695–708. doi: 10.1083/jcb.201511044 28137779
84. Pogson JH, Ivatt RM, Sanchez-Martinez A, Tufi R, Wilson E, Mortiboys H, et al. The complex I subunit NDUFA10 selectively rescues Drosophila pink1 mutants through a mechanism independent of mitophagy. PLoS Genet. 2014;10(11): e1004815. doi: 10.1371/journal.pgen.1004815 25412178
85. Morais VA, Haddad D, Craessaerts K, De Bock PJ, Swerts J, Vilain S, et al. PINK1 loss-of-function mutations affect mitochondrial complex I activity via NdufA10 ubiquinone uncoupling. Science. 2014;344(6180): 203–7. doi: 10.1126/science.1249161 24652937
86. Vincow ES, Merrihew G, Thomas RE, Shulman NJ, Beyer RP, MacCoss MJ, et al. The PINK1-Parkin pathway promotes both mitophagy and selective respiratory chain turnover in vivo. Proc Natl Acad Sci U S A. 2013;110(16): 6400–5. doi: 10.1073/pnas.1221132110 23509287
87. Vos M, Esposito G, Edirisinghe JN, Vilain S, Haddad DM, Slabbaert JR, et al. Vitamin K2 is a mitochondrial electron carrier that rescues pink1 deficiency. Science. 2012;336(6086): 1306–10. doi: 10.1126/science.1218632 22582012
88. Kloo B, Nagel D, Pfeifer M, Grau M, Duwel M, Vincendeau M, et al. Critical role of PI3K signaling for NF-kappaB-dependent survival in a subset of activated B-cell-like diffuse large B-cell lymphoma cells. Proc Natl Acad Sci U S A. 2011;108(1): 272–7. doi: 10.1073/pnas.1008969108 21173233
89. Jeay S, Pianetti S, Kagan HM, Sonenshein GE. Lysyl oxidase inhibits ras-mediated transformation by preventing activation of NF-kappa B. Mol Cell Biol. 2003;23(7): 2251–63. doi: 10.1128/mcb.23.7.2251-2263.2003 12640111
90. Shi CS, Kehrl JH. PYK2 links G(q)alpha and G(13)alpha signaling to NF-kappa B activation. J Biol Chem. 2001;276(34): 31845–50. doi: 10.1074/jbc.M101043200 11435419
91. Volakakis N, Tiklova K, Decressac M, Papathanou M, Mattsson B, Gillberg L, et al. Nurr1 and retinoid X receptor ligands stimulate ret signaling in dopamine neurons and can alleviate alpha-synuclein disrupted gene expression. J Neurosci. 2015;35(42): 14370–85. doi: 10.1523/JNEUROSCI.1155-15.2015 26490873
92. Takayama H, LaRochelle WJ, Sharp R, Otsuka T, Kriebel P, Anver M, et al. Diverse tumorigenesis associated with aberrant development in mice overexpressing hepatocyte growth factor/scatter factor. Proc Natl Acad Sci U S A. 1997;94(2): 701–6. doi: 10.1073/pnas.94.2.701 9012848
93. Kharitonenkov A, Shiyanova TL, Koester A, Ford AM, Micanovic R, Galbreath EJ, et al. FGF-21 as a novel metabolic regulator. The Journal of clinical investigation. 2005;115(6): 1627–35. doi: 10.1172/JCI23606 15902306
94. Zioncheck TF, Richardson L, DeGuzman GG, Modi NB, Hansen SE, Godowski PJ. The pharmacokinetics, tissue localization, and metabolic processing of recombinant human hepatocyte growth factor after intravenous administration in rats. Endocrinology. 1994;134(4): 1879–87. doi: 10.1210/endo.134.4.8137756 8137756
95. Clackson T, Yang W, Rozamus LW, Hatada M, Amara JF, Rollins CT, et al. Redesigning an FKBP-ligand interface to generate chemical dimerizers with novel specificity. Proc Natl Acad Sci U S A. 1998;95(18): 10437–42. doi: 10.1073/pnas.95.18.10437 9724721
96. Ingles-Prieto A, Reichhart E, Muellner MK, Nowak M, Nijman SM, Grusch M, et al. Light-assisted small-molecule screening against protein kinases. Nat Chem Biol. 2015;11(12): 952–4. doi: 10.1038/nchembio.1933 26457372
97. Sun S, Elwood J, Greene WC. Both amino- and carboxyl-terminal sequences within I kappa B alpha regulate its inducible degradation. Mol Cell Biol. 1996;16(3): 1058–65. doi: 10.1128/mcb.16.3.1058 8622650
98. Caudron Q, Lyn-Adams C, Aston JAD, Frenguelli BG, Moffat KG. Quantitative assessment of ommatidial distortion in Drosophila melanogaster. Dros Inf Serv. 2013;96: 136–44.
99. Ali YO, Escala W, Ruan K, Zhai RG. Assaying locomotor, learning, and memory deficits in Drosophila models of neurodegeneration. J Vis Exp. 2011(49).
100. Heintz U, Schlichting I. Blue light-induced LOV domain dimerization enhances the affinity of Aureochrome 1a for its target DNA sequence. Elife. 2016;5: e11860. doi: 10.7554/eLife.11860 26754770
101. Mitra D, Yang X, Moffat K. Crystal structures of Aureochrome1 LOV suggest new design strategies for optogenetics. Structure. 2012;20(4): 698–706. doi: 10.1016/j.str.2012.02.016 22483116
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