Drosophila NUAK functions with Starvin/BAG3 in autophagic protein turnover
Autoři:
David Brooks aff001; Fawwaz Naeem aff001; Marta Stetsiv aff001; Samantha C. Goetting aff001; Simranjot Bawa aff001; Nicole Green aff001; Cheryl Clark aff001; Arash Bashirullah aff002; Erika R. Geisbrecht aff001
Působiště autorů:
Department of Biochemistry and Molecular Biophysics, Kansas State University, Manhattan, KS, United States of America
aff001; Division of Pharmaceutical Sciences, University of Wisconsin-Madison, Madison, WI, United States of America
aff002
Vyšlo v časopise:
Drosophila NUAK functions with Starvin/BAG3 in autophagic protein turnover. PLoS Genet 16(4): e32767. doi:10.1371/journal.pgen.1008700
Kategorie:
Research Article
doi:
https://doi.org/10.1371/journal.pgen.1008700
Souhrn
The inability to remove protein aggregates in post-mitotic cells such as muscles or neurons is a cellular hallmark of aging cells and is a key factor in the initiation and progression of protein misfolding diseases. While protein aggregate disorders share common features, the molecular level events that culminate in abnormal protein accumulation cannot be explained by a single mechanism. Here we show that loss of the serine/threonine kinase NUAK causes cellular degeneration resulting from the incomplete clearance of protein aggregates in Drosophila larval muscles. In NUAK mutant muscles, regions that lack the myofibrillar proteins F-actin and Myosin heavy chain (MHC) instead contain damaged organelles and the accumulation of select proteins, including Filamin (Fil) and CryAB. NUAK biochemically and genetically interacts with Drosophila Starvin (Stv), the ortholog of mammalian Bcl-2-associated athanogene 3 (BAG3). Consistent with a known role for the co-chaperone BAG3 and the Heat shock cognate 71 kDa (HSC70)/HSPA8 ATPase in the autophagic clearance of proteins, RNA interference (RNAi) of Drosophila Stv, Hsc70-4, or autophagy-related 8a (Atg8a) all exhibit muscle degeneration and muscle contraction defects that phenocopy NUAK mutants. We further demonstrate that Fil is a target of NUAK kinase activity and abnormally accumulates upon loss of the BAG3-Hsc70-4 complex. In addition, Ubiquitin (Ub), ref(2)p/p62, and Atg8a are increased in regions of protein aggregation, consistent with a block in autophagy upon loss of NUAK. Collectively, our results establish a novel role for NUAK with the Stv-Hsc70-4 complex in the autophagic clearance of proteins that may eventually lead to treatment options for protein aggregate diseases.
Klíčová slova:
Drosophila melanogaster – Larvae – Muscle contraction – Muscle functions – Muscle proteins – Muscle tissue – RNA interference – Sarcomeres
Zdroje
1. Jia B, Wu Y, Zhou Y. 14-3-3 and aggresome formation: implications in neurodegenerative diseases. Prion. 2014;8(2). Epub 2014/02/18. doi: 10.4161/pri.28123 24549097; PubMed Central PMCID: PMC4189886.
2. Takalo M, Salminen A, Soininen H, Hiltunen M, Haapasalo A. Protein aggregation and degradation mechanisms in neurodegenerative diseases. Am J Neurodegener Dis. 2013;2(1):1–14. Epub 2013/03/08. 23516262; PubMed Central PMCID: PMC3601466.
3. Shamsi TN, Athar T, Parveen R, Fatima S. A review on protein misfolding, aggregation and strategies to prevent related ailments. Int J Biol Macromol. 2017;105(Pt 1):993–1000. Epub 2017/07/23. doi: 10.1016/j.ijbiomac.2017.07.116 28743576.
4. Klaips CL, Jayaraj GG, Hartl FU. Pathways of cellular proteostasis in aging and disease. J Cell Biol. 2018;217(1):51–63. Epub 2017/11/10. doi: 10.1083/jcb.201709072 29127110; PubMed Central PMCID: PMC5748993.
5. Kaushik S, Cuervo AM. Chaperones in autophagy. Pharmacol Res. 2012;66(6):484–93. Epub 2012/10/08. doi: 10.1016/j.phrs.2012.10.002 23059540; PubMed Central PMCID: PMC3502706.
6. Klimek C, Kathage B, Wördehoff J, Höhfeld J. BAG3-mediated proteostasis at a glance. J Cell Sci. 2017;130(17):2781–8. Epub 2017/08/14. doi: 10.1242/jcs.203679 28808089.
7. Stürner E, Behl C. The Role of the Multifunctional BAG3 Protein in Cellular Protein Quality Control and in Disease. Front Mol Neurosci. 2017;10:177. Epub 2017/06/21. doi: 10.3389/fnmol.2017.00177 28680391; PubMed Central PMCID: PMC5478690.
8. Kettern N, Dreiseidler M, Tawo R, Höhfeld J. Chaperone-assisted degradation: multiple paths to destruction. Biol Chem. 2010;391(5):481–9. doi: 10.1515/BC.2010.058 20302520.
9. Ulbricht A, Höhfeld J. Tension-induced autophagy: may the chaperone be with you. Autophagy. 2013;9(6):920–2. Epub 2013/03/21. doi: 10.4161/auto.24213 23518596; PubMed Central PMCID: PMC3672301.
10. Ulbricht A, Arndt V, Höhfeld J. Chaperone-assisted proteostasis is essential for mechanotransduction in mammalian cells. Commun Integr Biol. 2013;6(4):e24925. Epub 2013/06/11. doi: 10.4161/cib.24925 23986815; PubMed Central PMCID: PMC3737759.
11. Arndt V, Dick N, Tawo R, Dreiseidler M, Wenzel D, Hesse M, et al. Chaperone-assisted selective autophagy is essential for muscle maintenance. Curr Biol. 2010;20(2):143–8. Epub 2010/01/07. doi: 10.1016/j.cub.2009.11.022 20060297.
12. Ulbricht A, Eppler FJ, Tapia VE, van der Ven PF, Hampe N, Hersch N, et al. Cellular mechanotransduction relies on tension-induced and chaperone-assisted autophagy. Curr Biol. 2013;23(5):430–5. Epub 2013/02/21. doi: 10.1016/j.cub.2013.01.064 23434281.
13. Ulbricht A, Gehlert S, Leciejewski B, Schiffer T, Bloch W, Höhfeld J. Induction and adaptation of chaperone-assisted selective autophagy CASA in response to resistance exercise in human skeletal muscle. Autophagy. 2015;11(3):538–46. doi: 10.1080/15548627.2015.1017186 25714469; PubMed Central PMCID: PMC4502687.
14. Fürst DO, Goldfarb LG, Kley RA, Vorgerd M, Olivé M, van der Ven PF. Filamin C-related myopathies: pathology and mechanisms. Acta Neuropathol. 2013;125(1):33–46. Epub 2012/10/30. doi: 10.1007/s00401-012-1054-9 23109048; PubMed Central PMCID: PMC5127197.
15. Razinia Z, Mäkelä T, Ylänne J, Calderwood DA. Filamins in mechanosensing and signaling. Annu Rev Biophys. 2012;41:227–46. Epub 2012/02/23. doi: 10.1146/annurev-biophys-050511-102252 22404683; PubMed Central PMCID: PMC5508560.
16. Gamerdinger M, Kaya AM, Wolfrum U, Clement AM, Behl C. BAG3 mediates chaperone-based aggresome-targeting and selective autophagy of misfolded proteins. EMBO Rep. 2011;12(2):149–56. Epub 2011/01/21. doi: 10.1038/embor.2010.203 21252941; PubMed Central PMCID: PMC3049430.
17. Shaid S, Brandts CH, Serve H, Dikic I. Ubiquitination and selective autophagy. Cell Death Differ. 2013;20(1):21–30. Epub 2012/06/22. doi: 10.1038/cdd.2012.72 22722335; PubMed Central PMCID: PMC3524631.
18. Tanaka Y, Guhde G, Suter A, Eskelinen EL, Hartmann D, Lüllmann-Rauch R, et al. Accumulation of autophagic vacuoles and cardiomyopathy in LAMP-2-deficient mice. Nature. 2000;406(6798):902–6. doi: 10.1038/35022595 10972293.
19. Sun X, Gao L, Chien HY, Li WC, Zhao J. The regulation and function of the NUAK family. J Mol Endocrinol. 2013;51(2):R15–22. doi: 10.1530/JME-13-0063 23873311.
20. Hawley SA, Boudeau J, Reid JL, Mustard KJ, Udd L, Mäkelä TP, et al. Complexes between the LKB1 tumor suppressor, STRAD alpha/beta and MO25 alpha/beta are upstream kinases in the AMP-activated protein kinase cascade. J Biol. 2003;2(4):28. Epub 2003/09/24. doi: 10.1186/1475-4924-2-28 14511394; PubMed Central PMCID: PMC333410.
21. Lefebvre DL, Rosen CF. Regulation of SNARK activity in response to cellular stresses. Biochim Biophys Acta. 2005;1724(1–2):71–85. Epub 2005/04/08. doi: 10.1016/j.bbagen.2005.03.015 15893879.
22. Koh HJ, Toyoda T, Fujii N, Jung MM, Rathod A, Middelbeek RJ, et al. Sucrose nonfermenting AMPK-related kinase (SNARK) mediates contraction-stimulated glucose transport in mouse skeletal muscle. Proc Natl Acad Sci U S A. 2010;107(35):15541–6. doi: 10.1073/pnas.1008131107 20713714; PubMed Central PMCID: PMC2932588.
23. Lessard SJ, Rivas DA, So K, Koh HJ, Queiroz AL, Hirshman MF, et al. The AMPK-related kinase SNARK regulates muscle mass and myocyte survival. J Clin Invest. 2016;126(2):560–70. doi: 10.1172/JCI79197 26690705; PubMed Central PMCID: PMC4731174.
24. Fisher JS, Ju JS, Oppelt PJ, Smith JL, Suzuki A, Esumi H. Muscle contractions, AICAR, and insulin cause phosphorylation of an AMPK-related kinase. Am J Physiol Endocrinol Metab. 2005;289(6):E986–92. Epub 2005/07/19. doi: 10.1152/ajpendo.00335.2004 16030062; PubMed Central PMCID: PMC1350986.
25. Hirano M, Kiyonari H, Inoue A, Furushima K, Murata T, Suda Y, et al. A new serine/threonine protein kinase, Omphk1, essential to ventral body wall formation. Dev Dyn. 2006;235(8):2229–37. doi: 10.1002/dvdy.20823 16715502.
26. Inazuka F, Sugiyama N, Tomita M, Abe T, Shioi G, Esumi H. Muscle-specific knock-out of NUAK family SNF1-like kinase 1 (NUAK1) prevents high fat diet-induced glucose intolerance. J Biol Chem. 2012;287(20):16379–89. doi: 10.1074/jbc.M111.302687 22418434; PubMed Central PMCID: PMC3351321.
27. Tsuchihara K, Ogura T, Fujioka R, Fujii S, Kuga W, Saito M, et al. Susceptibility of Snark-deficient mice to azoxymethane-induced colorectal tumorigenesis and the formation of aberrant crypt foci. Cancer Sci. 2008;99(4):677–82. Epub 2007/02/27. doi: 10.1111/j.1349-7006.2008.00734.x 18307533.
28. Hoppe PE, Chau J, Flanagan KA, Reedy AR, Schriefer LA. Caenorhabditis elegans unc-82 encodes a serine/threonine kinase important for myosin filament organization in muscle during growth. Genetics. 2010;184(1):79–90. doi: 10.1534/genetics.109.110189 19901071; PubMed Central PMCID: PMC2815932.
29. Schiller NR, Duchesneau CD, Lane LS, Reedy AR, Manzon ER, Hoppe PE. The Role of the UNC-82 Protein Kinase in Organizing Myosin Filaments in Striated Muscle of. Genetics. 2017;205(3):1195–213. Epub 2016/12/30. doi: 10.1534/genetics.116.193029 28040740; PubMed Central PMCID: PMC5340333.
30. Amin N, Khan A, St Johnston D, Tomlinson I, Martin S, Brenman J, et al. LKB1 regulates polarity remodeling and adherens junction formation in the Drosophila eye. Proc Natl Acad Sci U S A. 2009;106(22):8941–6. doi: 10.1073/pnas.0812469106 19443685; PubMed Central PMCID: PMC2690039.
31. Couderc JL, Richard G, Vachias C, Mirouse V. Drosophila LKB1 is required for the assembly of the polarized actin structure that allows spermatid individualization. PLoS One. 2017;12(8):e0182279. Epub 2017/08/02. doi: 10.1371/journal.pone.0182279 28767695; PubMed Central PMCID: PMC5540607.
32. LaBeau-DiMenna EM, Clark KA, Bauman KD, Parker DS, Cripps RM, Geisbrecht ER. Thin, a Trim32 ortholog, is essential for myofibril stability and is required for the integrity of the costamere in Drosophila. Proc Natl Acad Sci U S A. 2012;109(44):17983–8. doi: 10.1073/pnas.1208408109 23071324; PubMed Central PMCID: PMC3497806.
33. Clark KA, Bland JM, Beckerle MC. The Drosophila muscle LIM protein, Mlp84B, cooperates with D-titin to maintain muscle structural integrity. J Cell Sci. 2007;120(Pt 12):2066–77. doi: 10.1242/jcs.000695 17535853.
34. Green N, Odell N, Zych M, Clark C, Wang ZH, Biersmith B, et al. A Common Suite of Coagulation Proteins Function in Drosophila Muscle Attachment. Genetics. 2016. Epub 2016/08/31. doi: 10.1534/genetics.116.189787 27585844; PubMed Central PMCID: PMC5105843.
35. Fogerty FJ, Fessler LI, Bunch TA, Yaron Y, Parker CG, Nelson RE, et al. Tiggrin, a novel Drosophila extracellular matrix protein that functions as a ligand for Drosophila alpha PS2 beta PS integrins. Development. 1994;120(7):1747–58. 7924982.
36. Wang L, Evans J, Andrews HK, Beckstead RB, Thummel CS, Bashirullah A. A genetic screen identifies new regulators of steroid-triggered programmed cell death in Drosophila. Genetics. 2008;180(1):269–81. Epub 2008/08/30. doi: 10.1534/genetics.108.092478 18757938; PubMed Central PMCID: PMC2535680.
37. Bate M. The embryonic development of larval muscles in Drosophila. Development. 1990;110(3):791–804. 2100994.
38. Tatum EL, Beadle GW. DEVELOPMENT OF EYE COLORS IN DROSOPHILA: SOME PROPERTIES OF THE HORMONES CONCERNED. J Gen Physiol. 1938;22(2):239–53. doi: 10.1085/jgp.22.2.239 19873102; PubMed Central PMCID: PMC2141983.
39. Wójtowicz I, Jabłońska J, Zmojdzian M, Taghli-Lamallem O, Renaud Y, Junion G, et al. Drosophila small heat shock protein CryAB ensures structural integrity of developing muscles, and proper muscle and heart performance. Development. 2015;142(5):994–1005. doi: 10.1242/dev.115352 25715399.
40. Zagórska A, Deak M, Campbell DG, Banerjee S, Hirano M, Aizawa S, et al. New roles for the LKB1-NUAK pathway in controlling myosin phosphatase complexes and cell adhesion. Sci Signal. 2010;3(115):ra25. doi: 10.1126/scisignal.2000616 20354225.
41. Carrera AC, Alexandrov K, Roberts TM. The conserved lysine of the catalytic domain of protein kinases is actively involved in the phosphotransfer reaction and not required for anchoring ATP. Proc Natl Acad Sci U S A. 1993;90(2):442–6. doi: 10.1073/pnas.90.2.442 8421674; PubMed Central PMCID: PMC45679.
42. Reimann L, Wiese H, Leber Y, Schwäble AN, Fricke AL, Rohland A, et al. Myofibrillar Z-discs Are a Protein Phosphorylation Hot Spot with Protein Kinase C (PKCα) Modulating Protein Dynamics. Mol Cell Proteomics. 2017;16(3):346–67. Epub 2016/12/27. doi: 10.1074/mcp.M116.065425 28028127; PubMed Central PMCID: PMC5340999.
43. Deshmukh A, Coffey VG, Zhong Z, Chibalin AV, Hawley JA, Zierath JR. Exercise-induced phosphorylation of the novel Akt substrates AS160 and filamin A in human skeletal muscle. Diabetes. 2006;55(6):1776–82. doi: 10.2337/db05-1419 16731842.
44. Murray JT, Campbell DG, Peggie M, Mora A, Alfonso M, Cohen P. Identification of filamin C as a new physiological substrate of PKBalpha using KESTREL. Biochem J. 2004;384(Pt 3):489–94. doi: 10.1042/BJ20041058 15461588; PubMed Central PMCID: PMC1134134.
45. Brand AH, Perrimon N. Targeted gene expression as a means of altering cell fates and generating dominant phenotypes. Development. 1993;118(2):401–15. 8223268.
46. Coulson M, Robert S, Saint R. Drosophila starvin encodes a tissue-specific BAG-domain protein required for larval food uptake. Genetics. 2005;171(4):1799–812. Epub 2005/09/02. doi: 10.1534/genetics.105.043265 16143622; PubMed Central PMCID: PMC1456105.
47. Rosati A, Graziano V, De Laurenzi V, Pascale M, Turco MC. BAG3: a multifaceted protein that regulates major cell pathways. Cell Death Dis. 2011;2:e141. Epub 2011/04/07. doi: 10.1038/cddis.2011.24 21472004; PubMed Central PMCID: PMC3122056.
48. Knezevic T, Myers VD, Gordon J, Tilley DG, Sharp TE, Wang J, et al. BAG3: a new player in the heart failure paradigm. Heart Fail Rev. 2015;20(4):423–34. doi: 10.1007/s10741-015-9487-6 25925243; PubMed Central PMCID: PMC4463985.
49. Behl C. BAG3 and friends: co-chaperones in selective autophagy during aging and disease. Autophagy. 2011;7(7):795–8. doi: 10.4161/auto.7.7.15844 21681022.
50. Kabbage M, Dickman MB. The BAG proteins: a ubiquitous family of chaperone regulators. Cell Mol Life Sci. 2008;65(9):1390–402. doi: 10.1007/s00018-008-7535-2 18264803.
51. Takayama S, Xie Z, Reed JC. An evolutionarily conserved family of Hsp70/Hsc70 molecular chaperone regulators. J Biol Chem. 1999;274(2):781–6. doi: 10.1074/jbc.274.2.781 9873016.
52. Takayama S, Reed JC. Molecular chaperone targeting and regulation by BAG family proteins. Nat Cell Biol. 2001;3(10):E237–41. doi: 10.1038/ncb1001-e237 11584289.
53. Lamark T, Johansen T. Aggrephagy: selective disposal of protein aggregates by macroautophagy. Int J Cell Biol. 2012;2012:736905. Epub 2012/03/22. doi: 10.1155/2012/736905 22518139; PubMed Central PMCID: PMC3320095.
54. Lim J, Yue Z. Neuronal aggregates: formation, clearance, and spreading. Dev Cell. 2015;32(4):491–501. doi: 10.1016/j.devcel.2015.02.002 25710535; PubMed Central PMCID: PMC4376477.
55. Lee YK, Lee JA. Role of the mammalian ATG8/LC3 family in autophagy: differential and compensatory roles in the spatiotemporal regulation of autophagy. BMB Rep. 2016;49(8):424–30. doi: 10.5483/BMBRep.2016.49.8.081 27418283; PubMed Central PMCID: PMC5070729.
56. Abdollahzadeh I, Schwarten M, Gensch T, Willbold D, Weiergräber OH. The Atg8 Family of Proteins-Modulating Shape and Functionality of Autophagic Membranes. Front Genet. 2017;8:109. Epub 2017/08/28. doi: 10.3389/fgene.2017.00109 28894458; PubMed Central PMCID: PMC5581321.
57. Erdi B, Nagy P, Zvara A, Varga A, Pircs K, Ménesi D, et al. Loss of the starvation-induced gene Rack1 leads to glycogen deficiency and impaired autophagic responses in Drosophila. Autophagy. 2012;8(7):1124–35. Epub 2012/05/07. doi: 10.4161/auto.20069 22562043; PubMed Central PMCID: PMC3429548.
58. Chintapalli VR, Wang J, Dow JA. Using FlyAtlas to identify better Drosophila melanogaster models of human disease. Nat Genet. 2007;39(6):715–20. doi: 10.1038/ng2049 17534367.
59. Vereshchagina N, Bennett D, Szöor B, Kirchner J, Gross S, Vissi E, et al. The essential role of PP1beta in Drosophila is to regulate nonmuscle myosin. Mol Biol Cell. 2004;15(10):4395–405. Epub 2004/07/21. doi: 10.1091/mbc.E04-02-0139 15269282; PubMed Central PMCID: PMC519135.
60. Mizuno T, Tsutsui K, Nishida Y. Drosophila myosin phosphatase and its role in dorsal closure. Development. 2002;129(5):1215–23. 11874917.
61. Kathage B, Gehlert S, Ulbricht A, Lüdecke L, Tapia VE, Orfanos Z, et al. The cochaperone BAG3 coordinates protein synthesis and autophagy under mechanical strain through spatial regulation of mTORC1. Biochim Biophys Acta. 2017;1864(1):62–75. Epub 2016/10/15. doi: 10.1016/j.bbamcr.2016.10.007 27756573.
62. Modarres HP, Mofradt MR. Filamin: a structural and functional biomolecule with important roles in cell biology, signaling and mechanics. Mol Cell Biomech. 2014;11(1):39–65. 25330623.
63. Puissant A, Fenouille N, Auberger P. When autophagy meets cancer through p62/SQSTM1. Am J Cancer Res. 2012;2(4):397–413. Epub 2012/06/28. 22860231; PubMed Central PMCID: PMC3410580.
64. Klionsky DJ, Abdelmohsen K, Abe A, Abedin MJ, Abeliovich H, Acevedo Arozena A, et al. Guidelines for the use and interpretation of assays for monitoring autophagy (3rd edition). Autophagy. 2016;12(1):1–222. doi: 10.1080/15548627.2015.1100356 26799652; PubMed Central PMCID: PMC4835977.
65. Dimauro I, Antonioni A, Mercatelli N, Caporossi D. The role of αB-crystallin in skeletal and cardiac muscle tissues. Cell Stress Chaperones. 2018;23(4):491–505. Epub 2017/11/30. doi: 10.1007/s12192-017-0866-x 29190034; PubMed Central PMCID: PMC6045558.
66. Fichna JP, Potulska-Chromik A, Miszta P, Redowicz MJ, Kaminska AM, Zekanowski C, et al. A novel dominant D109A CRYAB mutation in a family with myofibrillar myopathy affects αB-crystallin structure. BBA Clin. 2017;7:1–7. Epub 2016/11/11. doi: 10.1016/j.bbacli.2016.11.004 27904835; PubMed Central PMCID: PMC5124346.
67. Markossian KA, Yudin IK, Kurganov BI. Mechanism of suppression of protein aggregation by α-crystallin. Int J Mol Sci. 2009;10(3):1314–45. Epub 2009/03/19. doi: 10.3390/ijms10031314 19399251; PubMed Central PMCID: PMC2672032.
68. Fujita M, Mitsuhashi H, Isogai S, Nakata T, Kawakami A, Nonaka I, et al. Filamin C plays an essential role in the maintenance of the structural integrity of cardiac and skeletal muscles, revealed by the medaka mutant zacro. Dev Biol. 2012;361(1):79–89. Epub 2011/10/14. doi: 10.1016/j.ydbio.2011.10.008 22020047.
69. Min JN, Whaley RA, Sharpless NE, Lockyer P, Portbury AL, Patterson C. CHIP deficiency decreases longevity, with accelerated aging phenotypes accompanied by altered protein quality control. Mol Cell Biol. 2008;28(12):4018–25. Epub 2008/04/14. doi: 10.1128/MCB.00296-08 18411298; PubMed Central PMCID: PMC2423116.
70. Morishima Y, Wang AM, Yu Z, Pratt WB, Osawa Y, Lieberman AP. CHIP deletion reveals functional redundancy of E3 ligases in promoting degradation of both signaling proteins and expanded glutamine proteins. Hum Mol Genet. 2008;17(24):3942–52. Epub 2008/09/10. doi: 10.1093/hmg/ddn296 18784277; PubMed Central PMCID: PMC2605787.
71. Kley RA, Maerkens A, Leber Y, Theis V, Schreiner A, van der Ven PF, et al. A combined laser microdissection and mass spectrometry approach reveals new disease relevant proteins accumulating in aggregates of filaminopathy patients. Mol Cell Proteomics. 2013;12(1):215–27. Epub 2012/10/31. doi: 10.1074/mcp.M112.023176 23115302; PubMed Central PMCID: PMC3536902.
72. Maerkens A, Kley RA, Olivé M, Theis V, van der Ven PF, Reimann J, et al. Differential proteomic analysis of abnormal intramyoplasmic aggregates in desminopathy. J Proteomics. 2013;90:14–27. Epub 2013/04/30. doi: 10.1016/j.jprot.2013.04.026 23639843; PubMed Central PMCID: PMC5120880.
73. Maerkens A, Olivé M, Schreiner A, Feldkirchner S, Schessl J, Uszkoreit J, et al. New insights into the protein aggregation pathology in myotilinopathy by combined proteomic and immunolocalization analyses. Acta Neuropathol Commun. 2016;4:8. Epub 2016/02/03. doi: 10.1186/s40478-016-0280-0 26842778; PubMed Central PMCID: PMC4739336.
74. Olivé M, Kley RA, Goldfarb LG. Myofibrillar myopathies: new developments. Curr Opin Neurol. 2013;26(5):527–35. doi: 10.1097/WCO.0b013e328364d6b1 23995273; PubMed Central PMCID: PMC5127196.
75. Béhin A, Salort-Campana E, Wahbi K, Richard P, Carlier RY, Carlier P, et al. Myofibrillar myopathies: State of the art, present and future challenges. Rev Neurol (Paris). 2015;171(10):715–29. Epub 2015/09/03. doi: 10.1016/j.neurol.2015.06.002 26342832.
76. Winter L, Goldmann WH. Biomechanical characterization of myofibrillar myopathies. Cell Biol Int. 2015;39(4):361–3. Epub 2014/12/03. doi: 10.1002/cbin.10384 25264173.
77. Kley RA, Olivé M, Schröder R. New aspects of myofibrillar myopathies. Curr Opin Neurol. 2016;29(5):628–34. doi: 10.1097/WCO.0000000000000357 27389816.
78. Batonnet-Pichon S, Behin A, Cabet E, Delort F, Vicart P, Lilienbaum A. Myofibrillar Myopathies: New Perspectives from Animal Models to Potential Therapeutic Approaches. J Neuromuscul Dis. 2017;4(1):1–15. doi: 10.3233/JND-160203 28269794; PubMed Central PMCID: PMC5345645.
79. Fichna JP, Maruszak A, Żekanowski C. Myofibrillar myopathy in the genomic context. J Appl Genet. 2018;59(4):431–9. Epub 2018/09/10. doi: 10.1007/s13353-018-0463-4 30203143.
80. Schröder R. Protein aggregate myopathies: the many faces of an expanding disease group. Acta Neuropathol. 2013;125(1):1–2. doi: 10.1007/s00401-012-1071-8 23224320.
81. Carra S, Boncoraglio A, Kanon B, Brunsting JF, Minoia M, Rana A, et al. Identification of the Drosophila ortholog of HSPB8: implication of HSPB8 loss of function in protein folding diseases. J Biol Chem. 2010;285(48):37811–22. Epub 2010/09/21. doi: 10.1074/jbc.M110.127498 20858900; PubMed Central PMCID: PMC2988385.
82. Green N, Walker J, Bontrager A, Zych M, Geisbrecht ER. A tissue communication network coordinating innate immune response during muscle stress. J Cell Sci. 2018;131(24). Epub 2018/12/18. doi: 10.1242/jcs.217943 30478194; PubMed Central PMCID: PMC6307882.
83. Geisbrecht ER, Haralalka S, Swanson SK, Florens L, Washburn MP, Abmayr SM. Drosophila ELMO/CED-12 interacts with Myoblast city to direct myoblast fusion and ommatidial organization. Dev Biol. 2008;314(1):137–49. doi: 10.1016/j.ydbio.2007.11.022 18163987; PubMed Central PMCID: PMC2697615.
84. Sokol NS, Cooley L. Drosophila filamin encoded by the cheerio locus is a component of ovarian ring canals. Curr Biol. 1999;9(21):1221–30. doi: 10.1016/s0960-9822(99)80502-8 10556087.
85. Friedrich MV, Schneider M, Timpl R, Baumgartner S. Perlecan domain V of Drosophila melanogaster. Sequence, recombinant analysis and tissue expression. Eur J Biochem. 2000;267(11):3149–59. doi: 10.1046/j.1432-1327.2000.01337.x 10824099.
86. Wang ZH, Clark C, Geisbrecht ER. Drosophila Clueless is involved in Parkin-dependent mitophagy by promoting VCP-mediated Marf degradation. Hum Mol Genet. 2016. doi: 10.1093/hmg/ddw067 26931463.
87. Brooks DS, Vishal K, Kawakami J, Bouyain S, Geisbrecht ER. Optimization of wrMTrck to monitor Drosophila larval locomotor activity. J Insect Physiol. 2016;93–94:11–7. Epub 2016/07/16. doi: 10.1016/j.jinsphys.2016.07.007 27430166.
Článek vyšel v časopise
PLOS Genetics
2020 Číslo 4
- Distribuce a lokalizace speciálně upravených exosomů může zefektivnit léčbu svalových dystrofií
- Prof. Jan Škrha: Metformin je bezpečný, ale je třeba jej bezpečně užívat a léčbu kontrolovat
- FDA varuje před selfmonitoringem cukru pomocí chytrých hodinek. Jak je to v Česku?
- Masturbační chování žen v ČR − dotazníková studie
- Vánoční dárky s přidanou hodnotou pro zdraví – nechte se inspirovat a poraďte svým pacientům
Nejčtenější v tomto čísle
- Analysis of genes within the schizophrenia-linked 22q11.2 deletion identifies interaction of night owl/LZTR1 and NF1 in GABAergic sleep control
- High expression in maize pollen correlates with genetic contributions to pollen fitness as well as with coordinated transcription from neighboring transposable elements
- Molecular genetics of maternally-controlled cell divisions
- Spastin mutations impair coordination between lipid droplet dispersion and reticulum