PE homeostasis rebalanced through mitochondria-ER lipid exchange prevents retinal degeneration in Drosophila
Autoři:
Haifang Zhao aff001; Tao Wang aff001
Působiště autorů:
National Institute of Biological Sciences, Beijing, China
aff001; Tsinghua Institute of Multidisciplinary Biomedical Research, Tsinghua University, Beijing, China
aff002
Vyšlo v časopise:
PE homeostasis rebalanced through mitochondria-ER lipid exchange prevents retinal degeneration in Drosophila. PLoS Genet 16(10): e32767. doi:10.1371/journal.pgen.1009070
Kategorie:
Research Article
doi:
https://doi.org/10.1371/journal.pgen.1009070
Souhrn
The major glycerophospholipid phosphatidylethanolamine (PE) in the nervous system is essential for neural development and function. There are two major PE synthesis pathways, the CDP-ethanolamine pathway in the endoplasmic reticulum (ER) and the phosphatidylserine decarboxylase (PSD) pathway in mitochondria. However, the role played by mitochondrial PE synthesis in maintaining cellular PE homeostasis is unknown. Here, we show that Drosophila pect (phosphoethanolamine cytidylyltransferase) mutants lacking the CDP-ethanolamine pathway, exhibited alterations in phospholipid composition, defective phototransduction, and retinal degeneration. Induction of the PSD pathway fully restored levels and composition of cellular PE, thus rescued the retinal degeneration and defective visual responses in pect mutants. Disrupting lipid exchange between mitochondria and ER blocked the ability of PSD to rescue pect mutant phenotypes. These findings provide direct evidence that the synthesis of PE in mitochondria contributes to cellular PE homeostasis, and suggest the induction of mitochondrial PE synthesis as a promising therapeutic approach for disorders associated with PE deficiency.
Klíčová slova:
Drosophila melanogaster – Eyes – Lipid analysis – Mitochondria – Phospholipids – Photoreceptors – Retina – Retinal degeneration
Zdroje
1. Anderson RE. Lipids of ocular tissues. IV. A comparison of the phospholipids from the retina of six mammalian species. Exp Eye Res. 1970;10(2):339–44. Epub 1970/10/01. doi: 10.1016/s0014-4835(70)80046-x 4320824.
2. Vance JE. Phosphatidylserine and phosphatidylethanolamine in mammalian cells: two metabolically related aminophospholipids. J Lipid Res. 2008;49(7):1377–87. doi: 10.1194/jlr.R700020-JLR200 18204094.
3. Verkleij AJ, Leunissen-Bijvelt J, de Kruijff B, Hope M, Cullis PR. Non-bilayer structures in membrane fusion. Ciba Foundation symposium. 1984;103:45–59. Epub 1984/01/01. doi: 10.1002/9780470720844.ch4 6561137.
4. Bottinger L, Horvath SE, Kleinschroth T, Hunte C, Daum G, Pfanner N, et al. Phosphatidylethanolamine and cardiolipin differentially affect the stability of mitochondrial respiratory chain supercomplexes. Journal of molecular biology. 2012;423(5):677–86. Epub 2012/09/14. doi: 10.1016/j.jmb.2012.09.001 22971339; PubMed Central PMCID: PMC3480645.
5. Tasseva G, Bai HD, Davidescu M, Haromy A, Michelakis E, Vance JE. Phosphatidylethanolamine deficiency in Mammalian mitochondria impairs oxidative phosphorylation and alters mitochondrial morphology. J Biol Chem. 2013;288(6):4158–73. doi: 10.1074/jbc.M112.434183 23250747; PubMed Central PMCID: PMC3567666.
6. Steenbergen R, Nanowski TS, Beigneux A, Kulinski A, Young SG, Vance JE. Disruption of the phosphatidylserine decarboxylase gene in mice causes embryonic lethality and mitochondrial defects. J Biol Chem. 2005;280(48):40032–40. Epub 2005/09/30. doi: 10.1074/jbc.M506510200 16192276; PubMed Central PMCID: PMC2888304.
7. Vaz FM, McDermott JH, Alders M, Wortmann SB, Kolker S, Pras-Raves ML, et al. Mutations in PCYT2 disrupt etherlipid biosynthesis and cause a complex hereditary spastic paraplegia. Brain. 2019;142(11):3382–97. Epub 2019/10/23. doi: 10.1093/brain/awz291 31637422; PubMed Central PMCID: PMC6821184.
8. Kennedy EP, Weiss SB. The function of cytidine coenzymes in the biosynthesis of phospholipides. J Biol Chem. 1956;222(1):193–214. Epub 1956/09/01. 13366993.
9. Percy AK, Moore JF, Carson MA, Waechter CJ. Characterization of brain phosphatidylserine decarboxylase: localization in the mitochondrial inner membrane. Archives of biochemistry and biophysics. 1983;223(2):484–94. Epub 1983/06/01. doi: 10.1016/0003-9861(83)90613-6 6859873.
10. Zborowski J, Dygas A, Wojtczak L. Phosphatidylserine decarboxylase is located on the external side of the inner mitochondrial membrane. FEBS Lett. 1983;157(1):179–82. Epub 1983/06/27. doi: 10.1016/0014-5793(83)81141-7 6862014.
11. Horvath SE, Bottinger L, Vogtle FN, Wiedemann N, Meisinger C, Becker T, et al. Processing and topology of the yeast mitochondrial phosphatidylserine decarboxylase 1. J Biol Chem. 2012;287(44):36744–55. doi: 10.1074/jbc.M112.398107 22984266; PubMed Central PMCID: PMC3481278.
12. Fullerton MD, Hakimuddin F, Bakovic M. Developmental and metabolic effects of disruption of the mouse CTP:phosphoethanolamine cytidylyltransferase gene (Pcyt2). Molecular and cellular biology. 2007;27(9):3327–36. Epub 2007/02/28. doi: 10.1128/MCB.01527-06 17325045; PubMed Central PMCID: PMC1899976.
13. Leonardi R, Frank MW, Jackson PD, Rock CO, Jackowski S. Elimination of the CDP-ethanolamine pathway disrupts hepatic lipid homeostasis. J Biol Chem. 2009;284(40):27077–89. Epub 2009/08/12. doi: 10.1074/jbc.M109.031336 19666474; PubMed Central PMCID: PMC2785637.
14. Kainu V, Hermansson M, Hanninen S, Hokynar K, Somerharju P. Import of phosphatidylserine to and export of phosphatidylethanolamine molecular species from mitochondria. Biochim Biophys Acta. 2013;1831(2):429–37. doi: 10.1016/j.bbalip.2012.11.003 23159415.
15. Shiao YJ, Lupo G, Vance JE. Evidence that phosphatidylserine is imported into mitochondria via a mitochondria-associated membrane and that the majority of mitochondrial phosphatidylethanolamine is derived from decarboxylation of phosphatidylserine. J Biol Chem. 1995;270(19):11190–8. Epub 1995/05/12. doi: 10.1074/jbc.270.19.11190 7744750.
16. Vance JE, Aasman EJ, Szarka R. Brefeldin A does not inhibit the movement of phosphatidylethanolamine from its sites for synthesis to the cell surface. J Biol Chem. 1991;266(13):8241–7. Epub 1991/05/05. 2022641.
17. Camici O, Corazzi L. Import of phosphatidylethanolamine for the assembly of rat brain mitochondrial membranes. The Journal of membrane biology. 1995;148(2):169–76. Epub 1995/11/01. doi: 10.1007/BF00207272 8606365.
18. Bleijerveld OB, Brouwers JF, Vaandrager AB, Helms JB, Houweling M. The CDP-ethanolamine pathway and phosphatidylserine decarboxylation generate different phosphatidylethanolamine molecular species. J Biol Chem. 2007;282(39):28362–72. Epub 2007/08/04. doi: 10.1074/jbc.M703786200 17673461.
19. Balla T, Sengupta N, Kim YJ. Lipid synthesis and transport are coupled to regulate membrane lipid dynamics in the endoplasmic reticulum. Biochim Biophys Acta Mol Cell Biol Lipids. 2020;1865(1). doi: 10.1016/j.bbalip.2019.05.005 31108203; PubMed Central PMCID: PMC6858525.
20. Zhao T, Goedhart CM, Sam PN, Sabouny R, Lingrell S, Cornish AJ, et al. PISD is a mitochondrial disease gene causing skeletal dysplasia, cataracts, and white matter changes. Life Sci Alliance. 2019;2(2). doi: 10.26508/lsa.201900353 30858161; PubMed Central PMCID: PMC6412922.
21. Girisha KM, von Elsner L, Neethukrishna K, Muranjan M, Shukla A, Bhavani GS, et al. The homozygous variant c.797G>A/p.(Cys266Tyr) in PISD is associated with a Spondyloepimetaphyseal dysplasia with large epiphyses and disturbed mitochondrial function. Hum Mutat. 2019;40(3):299–309. doi: 10.1002/humu.23693 30488656.
22. Peter VG, Quinodoz M, Pinto-Basto J, Sousa SB, Di Gioia SA, Soares G, et al. The Liberfarb syndrome, a multisystem disorder affecting eye, ear, bone, and brain development, is caused by a founder pathogenic variant in thePISD gene. Genet Med. 2019;21(12):2734–43. Epub 2019/07/03. doi: 10.1038/s41436-019-0595-x 31263216; PubMed Central PMCID: PMC6892740.
23. Senturk M, Bellen HJ. Genetic strategies to tackle neurological diseases in fruit flies. Curr Opin Neurobiol. 2018;50:24–32. Epub 2017/11/13. doi: 10.1016/j.conb.2017.10.017 29128849; PubMed Central PMCID: PMC5940587.
24. Wang T, Montell C. Phototransduction and retinal degeneration in Drosophila. Pflugers Arch. 2007;454(5):821–47. Epub 2007/05/10. doi: 10.1007/s00424-007-0251-1 17487503.
25. Tsai JW, Kostyleva R, Chen PL, Rivas-Serna IM, Clandinin MT, Meinertzhagen IA, et al. Transcriptional Feedback Links Lipid Synthesis to Synaptic Vesicle Pools in Drosophila Photoreceptors. Neuron. 2019;101(4):721–37 e4. doi: 10.1016/j.neuron.2019.01.015 30737130.
26. Midorikawa R, Yamamoto-Hino M, Awano W, Hinohara Y, Suzuki E, Ueda R, et al. Autophagy-dependent rhodopsin degradation prevents retinal degeneration in Drosophila. The Journal of neuroscience: the official journal of the Society for Neuroscience. 2010;30(32):10703–19. Epub 2010/08/13. doi: 10.1523/jneurosci.2061-10.2010 20702701; PubMed Central PMCID: PMC6634698.
27. Zhao H, Wang J, Wang T. The V-ATPase V1 subunit A1 is required for rhodopsin anterograde trafficking in Drosophila. Molecular biology of the cell. 2018;29(13):1640–51. Epub 2018/05/10. doi: 10.1091/mbc.E17-09-0546 29742016; PubMed Central PMCID: PMC6080656.
28. Xiong L, Zhang L, Yang Y, Li N, Lai W, Wang F, et al. ER complex proteins are required for rhodopsin biosynthesis and photoreceptor survival in Drosophila and mice. Cell Death Differ. 2019. Epub 2019/07/03. doi: 10.1038/s41418-019-0378-6 31263175.
29. Sundler R. Ethanolaminephosphate cytidylyltransferase. Purification and characterization of the enzyme from rat liver. J Biol Chem. 1975;250(22):8585–90. Epub 1975/11/25. 241749.
30. Sundler R, Akesson B. Biosynthesis of phosphatidylethanolamines and phosphatidylcholines from ethanolamine and choline in rat liver. The Biochemical journal. 1975;146(2):309–15. Epub 1975/02/01. doi: 10.1042/bj1460309 168873; PubMed Central PMCID: PMC1165307.
31. Rosenbaum EE, Hardie RC, Colley NJ. Calnexin Is Essential for Rhodopsin Maturation, Ca2+ Regulation, and Photoreceptor Cell Survival. Neuron. 2006;49(2):229–41. doi: 10.1016/j.neuron.2005.12.011 16423697
32. Chyb S, Raghu P, Hardie RC. Polyunsaturated fatty acids activate the Drosophila light-sensitive channels TRP and TRPL. Nature. 1999;397(6716):255–9. Epub 1999/02/04. doi: 10.1038/16703 9930700.
33. Leung HT, Tseng-Crank J, Kim E, Mahapatra C, Shino S, Zhou Y, et al. DAG lipase activity is necessary for TRP channel regulation in Drosophila photoreceptors. Neuron. 2008;58(6):884–96. Epub 2008/06/27. doi: 10.1016/j.neuron.2008.05.001 18579079; PubMed Central PMCID: PMC2459341.
34. Raghu P, Usher K, Jonas S, Chyb S, Polyanovsky A, Hardie RC. Constitutive activity of the light-sensitive channels TRP and TRPL in the Drosophila diacylglycerol kinase mutant, rdgA. Neuron. 2000;26(1):169–79. Epub 2000/05/08. doi: 10.1016/s0896-6273(00)81147-2 10798401.
35. Inoue H, Yoshioka T, Hotta Y. Diacylglycerol kinase defect in a Drosophila retinal degeneration mutant rdgA. J Biol Chem. 1989;264(10):5996–6000. Epub 1989/04/05. 2538432.
36. Garcia-Murillas I, Pettitt T, Macdonald E, Okkenhaug H, Georgiev P, Trivedi D, et al. lazaro Encodes a Lipid Phosphate Phosphohydrolase that Regulates Phosphatidylinositol Turnover during Drosophila Phototransduction. Neuron. 2006;49(4):533–46. doi: 10.1016/j.neuron.2006.02.001 16476663
37. Kwon Y, Montell C. Dependence on the Lazaro phosphatidic acid phosphatase for the maximum light response. Current biology: CB. 2006;16(7):723–9. Epub 2006/03/04. doi: 10.1016/j.cub.2006.02.057 16513351.
38. Ly CV, Verstreken P. Mitochondria at the synapse. The Neuroscientist: a review journal bringing neurobiology, neurology and psychiatry. 2006;12(4):291–9. Epub 2006/07/15. doi: 10.1177/1073858406287661 16840705.
39. 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. Epub 2006/05/05. doi: 10.1038/nature04788 16672980.
40. Vance JE. MAM (mitochondria-associated membranes) in mammalian cells: Lipids and beyond. Biochimica et Biophysica Acta (BBA)—Molecular and Cell Biology of Lipids. 2014;1841(4):595–609. doi: 10.1016/j.bbalip.2013.11.014 24316057
41. Krols M, Bultynck G, Janssens S. ER-Mitochondria contact sites: A new regulator of cellular calcium flux comes into play. J Cell Biol. 2016;214(4):367–70. Epub 2016/08/17. doi: 10.1083/jcb.201607124 27528654; PubMed Central PMCID: PMC4987300.
42. Modi S, Lopez-Domenech G, Halff EF, Covill-Cooke C, Ivankovic D, Melandri D, et al. Miro clusters regulate ER-mitochondria contact sites and link cristae organization to the mitochondrial transport machinery. Nat Commun. 2019;10(1):4399. Epub 2019/09/29. doi: 10.1038/s41467-019-12382-4 31562315; PubMed Central PMCID: PMC6764964.
43. de Brito OM, Scorrano L. Mitofusin 2 tethers endoplasmic reticulum to mitochondria. Nature. 2008;456(7222):605–10. Epub 2008/12/05. doi: 10.1038/nature07534 19052620.
44. Szabadkai G, Bianchi K, Varnai P, De Stefani D, Wieckowski MR, Cavagna D, et al. Chaperone-mediated coupling of endoplasmic reticulum and mitochondrial Ca2+ channels. J Cell Biol. 2006;175(6):901–11. Epub 2006/12/21. doi: 10.1083/jcb.200608073 17178908; PubMed Central PMCID: PMC2064700.
45. Zhang K, Kaufman RJ. The unfolded protein response: a stress signaling pathway critical for health and disease. Neurology. 2006;66(2 Suppl 1):S102–9. Epub 2006/01/25. doi: 10.1212/01.wnl.0000192306.98198.ec 16432136.
46. Schopf K, Huber A. Membrane protein trafficking in Drosophila photoreceptor cells. Eur J Cell Biol. 2017;96(5):391–401. Epub 2016/12/15. doi: 10.1016/j.ejcb.2016.11.002 27964885.
47. Hardie RC, Juusola M. Phototransduction in Drosophila. Curr Opin Neurobiol. 2015;34:37–45. Epub 2015/02/02. doi: 10.1016/j.conb.2015.01.008 25638280.
48. Wang T, Montell C. A phosphoinositide synthase required for a sustained light response. The Journal of neuroscience: the official journal of the Society for Neuroscience. 2006;26(49):12816–25. Epub 2006/12/08. doi: 10.1523/jneurosci.3673-06.2006 17151285; PubMed Central PMCID: PMC6674829.
49. Parnas M, Katz B, Lev S, Tzarfaty V, Dadon D, Gordon-Shaag A, et al. Membrane lipid modulations remove divalent open channel block from TRP-like and NMDA channels. The Journal of neuroscience: the official journal of the Society for Neuroscience. 2009;29(8):2371–83. Epub 2009/02/27. doi: 10.1523/jneurosci.4280-08.2009 19244513; PubMed Central PMCID: PMC2672305.
50. Randall AS, Liu CH, Chu B, Zhang Q, Dongre SA, Juusola M, et al. Speed and sensitivity of phototransduction in Drosophila depend on degree of saturation of membrane phospholipids. The Journal of neuroscience: the official journal of the Society for Neuroscience. 2015;35(6):2731–46. Epub 2015/02/13. doi: 10.1523/jneurosci.1150-14.2015 25673862; PubMed Central PMCID: PMC4323538.
51. Hardie RC, Franze K. Photomechanical responses in Drosophila photoreceptors. Science. 2012;338(6104):260–3. Epub 2012/10/16. doi: 10.1126/science.1222376 23066080.
52. Rockenfeller P, Koska M, Pietrocola F, Minois N, Knittelfelder O, Sica V, et al. Phosphatidylethanolamine positively regulates autophagy and longevity. Cell Death Differ. 2015;22(3):499–508. doi: 10.1038/cdd.2014.219 25571976; PubMed Central PMCID: PMC4326582.
53. Birner R, Bürgermeister M, Schneiter R, Daum G. Roles of Phosphatidylethanolamine and of Its Several Biosynthetic Pathways in Saccharomyces cerevisiae. Molecular biology of the cell. 2001;12(4):997–1007. doi: 10.1091/mbc.12.4.997 11294902.
54. Burgermeister M, Birner-Grunberger R, Nebauer R, Daum G. Contribution of different pathways to the supply of phosphatidylethanolamine and phosphatidylcholine to mitochondrial membranes of the yeast Saccharomyces cerevisiae. Biochim Biophys Acta. 2004;1686(1–2):161–8. Epub 2004/11/04. doi: 10.1016/j.bbalip.2004.09.007 15522832.
55. Calzada E, Avery E, Sam PN, Modak A, Wang C, McCaffery JM, et al. Phosphatidylethanolamine made in the inner mitochondrial membrane is essential for yeast cytochrome bc1 complex function. Nature Communications. 2019;10(1). doi: 10.1038/s41467-019-09425-1 30926815
56. Trotter PJ, Voelker DR. Identification of a non-mitochondrial phosphatidylserine decarboxylase activity (PSD2) in the yeast Saccharomyces cerevisiae. J Biol Chem. 1995;270(11):6062–70. Epub 1995/03/17. doi: 10.1074/jbc.270.11.6062 7890739.
57. Heden TD, Johnson JM, Ferrara PJ, Eshima H, Verkerke ARP, Wentzler EJ, et al. Mitochondrial PE potentiates respiratory enzymes to amplify skeletal muscle aerobic capacity. Sci Adv. 2019;5(9):eaax8352. Epub 2019/09/20. doi: 10.1126/sciadv.aax8352 31535029; PubMed Central PMCID: PMC6739096.
58. Friedman JR, Kannan M, Toulmay A, Jan CH, Weissman JS, Prinz WA, et al. Lipid Homeostasis Is Maintained by Dual Targeting of the Mitochondrial PE Biosynthesis Enzyme to the ER. Dev Cell. 2018;44(2):261–70 e6. doi: 10.1016/j.devcel.2017.11.023 29290583; PubMed Central PMCID: PMC5975648.
59. Kornmann B, Currie E, Collins SR, Schuldiner M, Nunnari J, Weissman JS, et al. An ER-mitochondria tethering complex revealed by a synthetic biology screen. Science. 2009;325(5939):477–81. Epub 2009/06/27. doi: 10.1126/science.1175088 19556461; PubMed Central PMCID: PMC2933203.
60. 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.
61. Hernandez-Alvarez MI, Sebastian D, Vives S, Ivanova S, Bartoccioni P, Kakimoto P, et al. Deficient Endoplasmic Reticulum-Mitochondrial Phosphatidylserine Transfer Causes Liver Disease. Cell. 2019;177(4):881–95 e17. doi: 10.1016/j.cell.2019.04.010 31051106.
62. Kagan VE, Mao G, Qu F, Angeli JP, Doll S, Croix CS, et al. Oxidized arachidonic and adrenic PEs navigate cells to ferroptosis. Nat Chem Biol. 2017;13(1):81–90. doi: 10.1038/nchembio.2238 27842066; PubMed Central PMCID: PMC5506843.
63. Fu S, Yang L, Li P, Hofmann O, Dicker L, Hide W, et al. Aberrant lipid metabolism disrupts calcium homeostasis causing liver endoplasmic reticulum stress in obesity. Nature. 2011;473(7348):528–31. doi: 10.1038/nature09968 21532591; PubMed Central PMCID: PMC3102791.
64. Li Z, Agellon LB, Allen TM, Umeda M, Jewell L, Mason A, et al. The ratio of phosphatidylcholine to phosphatidylethanolamine influences membrane integrity and steatohepatitis. Cell Metab. 2006;3(5):321–31. Epub 2006/05/09. doi: 10.1016/j.cmet.2006.03.007 16679290.
65. Mitsuhashi S, Ohkuma A, Talim B, Karahashi M, Koumura T, Aoyama C, et al. A congenital muscular dystrophy with mitochondrial structural abnormalities caused by defective de novo phosphatidylcholine biosynthesis. Am J Hum Genet. 2011;88(6):845–51. Epub 2011/06/15. doi: 10.1016/j.ajhg.2011.05.010 21665002; PubMed Central PMCID: PMC3113344.
66. Ni JQ, Zhou R, Czech B, Liu LP, Holderbaum L, Yang-Zhou D, et al. A genome-scale shRNA resource for transgenic RNAi in Drosophila. Nat Methods. 2011;8(5):405–7. Epub 2011/04/05. doi: 10.1038/nmeth.1592 21460824; PubMed Central PMCID: PMC3489273.
67. Xu Y, Wang T. CULD is required for rhodopsin and TRPL channel endocytic trafficking and survival of photoreceptor cells. J Cell Sci. 2016;129(2):394–405. Epub 2015/11/26. doi: 10.1242/jcs.178764 26598556; PubMed Central PMCID: PMC4732287.
68. Bozidis P, Williamson CD, Colberg-Poley AM. Isolation of endoplasmic reticulum, mitochondria, and mitochondria-associated membrane fractions from transfected cells and from human cytomegalovirus-infected primary fibroblasts. Curr Protoc Cell Biol. 2007;Chapter 3:Unit 3.27. Epub 2008/01/30. doi: 10.1002/0471143030.cb0327s37 18228515.
69. Huang Y, Xie J, Wang T. A Fluorescence-Based Genetic Screen to Study Retinal Degeneration in Drosophila. PLoS One. 2015;10(12):e0144925. Epub 2015/12/15. doi: 10.1371/journal.pone.0144925 26659849; PubMed Central PMCID: PMC4684387.
70. Tian S, Ohtsuka J, Wang S, Nagata K, Tanokura M, Ohta A, et al. Human CTP:phosphoethanolamine cytidylyltransferase: enzymatic properties and unequal catalytic roles of CTP-binding motifs in two cytidylyltransferase domains. Biochem Biophys Res Commun. 2014;449(1):26–31. Epub 2014/05/08. doi: 10.1016/j.bbrc.2014.04.131 24802409.
71. Wang T, Wang X, Xie Q, Montell C. The SOCS box protein STOPS is required for phototransduction through its effects on phospholipase C. Neuron. 2008;57(1):56–68. Epub 2008/01/11. doi: 10.1016/j.neuron.2007.11.020 18184564; PubMed Central PMCID: PMC2253723.
72. Wang T, Jiao Y, Montell C. Dissecting independent channel and scaffolding roles of the Drosophila transient receptor potential channel. The Journal of cell biology. 2005;171(4):685–94. doi: 10.1083/jcb.200508030 16301334.
73. Xu Y, Wang T. LOVIT Is a Putative Vesicular Histamine Transporter Required in Drosophila for Vision. Cell Rep. 2019;27(5):1327–33 e3. Epub 2019/05/03. doi: 10.1016/j.celrep.2019.04.024 31042461.
74. Zhuang N, Li L, Chen S, Wang T. PINK1-dependent phosphorylation of PINK1 and Parkin is essential for mitochondrial quality control. Cell Death Dis. 2016;7(12):e2501. Epub 2016/12/03. doi: 10.1038/cddis.2016.396 27906179; PubMed Central PMCID: PMC5261015.
75. Xu H, Lee SJ, Suzuki E, Dugan KD, Stoddard A, Li HS, et al. A lysosomal tetraspanin associated with retinal degeneration identified via a genome-wide screen. Embo j. 2004;23(4):811–22. Epub 2004/02/14. doi: 10.1038/sj.emboj.7600112 14963491; PubMed Central PMCID: PMC381016.
76. Lam SM, Tong L, Duan X, Petznick A, Wenk MR, Shui G. Extensive characterization of human tear fluid collected using different techniques unravels the presence of novel lipid amphiphiles. J Lipid Res. 2014;55(2):289–98. Epub 2013/11/30. doi: 10.1194/jlr.M044826 24287120; PubMed Central PMCID: PMC3886667.
77. Shui G, Guan XL, Low CP, Chua GH, Goh JS, Yang H, et al. Toward one step analysis of cellular lipidomes using liquid chromatography coupled with mass spectrometry: application to Saccharomyces cerevisiae and Schizosaccharomyces pombe lipidomics. Mol Biosyst. 2010;6(6):1008–17. Epub 2010/05/21. doi: 10.1039/b913353d 20485745.
Článek vyšel v časopise
PLOS Genetics
2020 Číslo 10
- S diagnostikou Parkinsonovy nemoci může nově pomoci AI nástroj pro hodnocení mrkacího reflexu
- Proč při poslechu některé muziky prostě musíme tančit?
- Chůze do schodů pomáhá prodloužit život a vyhnout se srdečním chorobám
- Metamizol jako analgetikum první volby: kdy, pro koho, jak a proč?
- „Jednohubky“ z klinického výzkumu – 2024/44
Nejčtenější v tomto čísle
- Evaluation of both exonic and intronic variants for effects on RNA splicing allows for accurate assessment of the effectiveness of precision therapies
- RNA-directed DNA Methylation
- The DNA methylome of human sperm is distinct from blood with little evidence for tissue-consistent obesity associations
- Correction: Molecular predictors of brain metastasis-related microRNAs in lung adenocarcinoma
