The STRIPAK signaling complex regulates dephosphorylation of GUL1, an RNA-binding protein that shuttles on endosomes

Autoři: Valentina Stein aff001;  Bernhard Blank-Landeshammer aff002;  Kira Müntjes aff003;  Ramona Märker aff001;  Ines Teichert aff001;  Michael Feldbrügge aff003;  Albert Sickmann aff002;  Ulrich Kück aff001
Působiště autorů: Allgemeine und Molekulare Botanik, Ruhr-Universität, Bochum, Germany aff001;  Leibniz-Institut für Analytische Wissenschaften-ISAS-e.V., Dortmund, Germany aff002;  Institut für Mikrobiologie, Cluster of Excellence on Plant Sciences, Heinrich-Heine-Universität, Düsseldorf, Germany aff003
Vyšlo v časopise: The STRIPAK signaling complex regulates dephosphorylation of GUL1, an RNA-binding protein that shuttles on endosomes. PLoS Genet 16(9): e32767. doi:10.1371/journal.pgen.1008819
Kategorie: Research Article


The striatin-interacting phosphatase and kinase (STRIPAK) multi-subunit signaling complex is highly conserved within eukaryotes. In fungi, STRIPAK controls multicellular development, morphogenesis, pathogenicity, and cell-cell recognition, while in humans, certain diseases are related to this signaling complex. To date, phosphorylation and dephosphorylation targets of STRIPAK are still widely unknown in microbial as well as animal systems. Here, we provide an extended global proteome and phosphoproteome study using the wild type as well as STRIPAK single and double deletion mutants (Δpro11, Δpro11Δpro22, Δpp2Ac1Δpro22) from the filamentous fungus Sordaria macrospora. Notably, in the deletion mutants, we identified the differential phosphorylation of 129 proteins, of which 70 phosphorylation sites were previously unknown. Included in the list of STRIPAK targets are eight proteins with RNA recognition motifs (RRMs) including GUL1. Knockout mutants and complemented transformants clearly show that GUL1 affects hyphal growth and sexual development. To assess the role of GUL1 phosphorylation on fungal development, we constructed phospho-mimetic and -deficient mutants of GUL1 residues. While S180 was dephosphorylated in a STRIPAK-dependent manner, S216, and S1343 served as non-regulated phosphorylation sites. While the S1343 mutants were indistinguishable from wild type, phospho-deficiency of S180 and S216 resulted in a drastic reduction in hyphal growth, and phospho-deficiency of S216 also affects sexual fertility. These results thus suggest that differential phosphorylation of GUL1 regulates developmental processes such as fruiting body maturation and hyphal morphogenesis. Moreover, genetic interaction studies provide strong evidence that GUL1 is not an integral subunit of STRIPAK. Finally, fluorescence microscopy revealed that GUL1 co-localizes with endosomal marker proteins and shuttles on endosomes. Here, we provide a new mechanistic model that explains how STRIPAK-dependent and -independent phosphorylation of GUL1 regulates sexual development and asexual growth.

Klíčová slova:

Endosomes – Fungi – Phosphoproteins – Phosphorylation – Protein kinase signaling cascade – Proteomes – RNA-binding proteins – Yeast


1. Rogers S, McCloy R, Watkins DN, Burgess A. Mechanisms regulating phosphatase specificity and the removal of individual phosphorylation sites during mitotic exit. Bioessays. 2016;38 Suppl 1:S24–32.

2. Schuhmacher D, Sontag JM, Sontag E. Protein phosphatase 2A: More than a passenger in the regulation of epithelial cell-cell junctions. Front Cell Dev Biol. 2019;7:30. doi: 10.3389/fcell.2019.00030 30895176

3. Goudreault M, D'Ambrosio LM, Kean MJ, Mullin MJ, Larsen BG, Sanchez A, et al. A PP2A phosphatase high density interaction network identifies a novel striatin-interacting phosphatase and kinase complex linked to the cerebral cavernous malformation 3 (CCM3) protein. Mol Cell Proteomics. 2009;8(1):157–71. doi: 10.1074/mcp.M800266-MCP200 18782753

4. Castets F, Bartoli M, Barnier JV, Baillat G, Salin P, Moqrich A, et al. A novel calmodulin-binding protein, belonging to the WD-repeat family, is localized in dendrites of a subset of CNS neurons. J Cell Biol. 1996;134(4):1051–62. doi: 10.1083/jcb.134.4.1051 8769426

5. Pöggeler S, Kück U. A WD40 repeat protein regulates fungal cell differentiation and can be replaced functionally by the mammalian homologue striatin. Eukaryot Cell. 2004;3(1):232–40. doi: 10.1128/ec.3.1.232-240.2004 14871953

6. Hwang J, Pallas DC. STRIPAK complexes: structure, biological function, and involvement in human diseases. Int J Biochem Cell Biol. 2014;47:118–48. doi: 10.1016/j.biocel.2013.11.021 24333164

7. Shi Z, Jiao S, Zhou Z. STRIPAK complexes in cell signaling and cancer. Oncogene. 2016;35(35):4549–57. doi: 10.1038/onc.2016.9 26876214

8. Kück U, Beier AM, Teichert I. The composition and function of the striatin-interacting phosphatases and kinases (STRIPAK) complex in fungi. Fungal Genet Biol. 2016;90:31–8. doi: 10.1016/j.fgb.2015.10.001 26439752

9. Kück U, Radchenko D, Teichert I. STRIPAK, a highly conserved signaling complex, controls multiple eukaryotic cellular and developmental processes and is linked with human diseases. Biol Chem. 2019;400(8):1005–22.

10. Elramli N, Karahoda B, Sarikaya-Bayram O, Frawley D, Ulas M, Oakley CE, et al. Assembly of a heptameric STRIPAK complex is required for coordination of light-dependent multicellular fungal development with secondary metabolism in Aspergillus nidulans. PLoS Genet. 2019;15(3):e1008053. doi: 10.1371/journal.pgen.1008053 30883543

11. Green KA, Becker Y, Fitzsimons HL, Scott B. An Epichloë festucae homologue of MOB3, a component of the STRIPAK complex, is required for the establishment of a mutualistic symbiotic interaction with Lolium perenne. Mol Plant Pathol. 2016;17(9):1480–92. doi: 10.1111/mpp.12443 27277141

12. Herzog S, Schumann MR, Fleissner A. Cell fusion in Neurospora crassa. Curr Opin Microbiol. 2015;28:53–9. doi: 10.1016/j.mib.2015.08.002 26340439

13. Fischer MS, Glass NL. Communicate and fuse: how filamentous fungi establish and maintain an Interconnected mycelial network. Front Microbiol. 2019;10:619. doi: 10.3389/fmicb.2019.00619 31001214

14. Frey S, Reschka EJ, Pöggeler S. Germinal center kinases SmKIN3 and SmKIN24 are associated with the Sordaria macrospora striatin-interacting phosphatase and kinase (STRIPAK) complex. PLoS One. 2015;10(9):e0139163. doi: 10.1371/journal.pone.0139163 26418262

15. Heilig Y, Dettmann A, Mouriño-Pérez RR, Schmitt K, Valerius O, Seiler S. Proper actin ring formation and septum constriction requires coordinated regulation of SIN and MOR pathways through the germinal centre kinase MST-1. PLoS Genet. 2014;10(4):e1004306. doi: 10.1371/journal.pgen.1004306 24762679

16. Radchenko D, Teichert I, Pöggeler S, Kück U. A Hippo pathway-related GCK controls both sexual and vegetative developmental processes in the fungus Sordaria macrospora. Genetics. 2018;210(1):137–53. doi: 10.1534/genetics.118.301261 30012560

17. Teichert I, Pöggeler S, Nowrousian M. Sordaria macrospora: 25 years as a model organism for studying the molecular mechanisms of fruiting body development. Appl Microbiol Biotechnol. 2020; 104(9):3691–3704. doi: 10.1007/s00253-020-10504-3

18. Beier A, Teichert I, Krisp C, Wolters DA, Kück U. Catalytic subunit 1 of protein phosphatase 2A is a subunit of the STRIPAK complex and governs fungal sexual development. mBio. 2016;7(3):e00870–16. doi: 10.1128/mBio.00870-16 27329756

19. Bloemendal S, Bernhards Y, Bartho K, Dettmann A, Voigt O, Teichert I, et al. A homologue of the human STRIPAK complex controls sexual development in fungi. Mol Microbiol. 2012;84(2):310–23. doi: 10.1111/j.1365-2958.2012.08024.x 22375702

20. Bloemendal S, Lord KM, Rech C, Hoff B, Engh I, Read ND, et al. A mutant defective in sexual development produces aseptate ascogonia. Eukaryot Cell. 2010;9(12):1856–66. doi: 10.1128/EC.00186-10 20952581

21. Märker R, Blank-Landeshammer B, Beier-Rosberger A, Sickmann A, Kück U. Phosphoproteomic analysis of STRIPAK mutants identifies a conserved serine phosphorylation site in PAK kinase CLA4 to be important in fungal sexual development and polarized growth. Mol Microbiol. 2020; 113(6):1053–1069. doi: 10.1111/mmi.14475

22. Schönberg A, Rödiger A, Mehwald W, Galonska J, Christ G, Helm S, et al. Identification of STN7/STN8 kinase targets reveals connections between electron transport, metabolism and gene expression. Plant J. 2017;90(6):1176–86. doi: 10.1111/tpj.13536 28295753

23. Roitinger E, Hofer M, Köcher T, Pichler P, Novatchkova M, Yang J, et al. Quantitative phosphoproteomics of the ataxia telangiectasia-mutated (ATM) and ataxia telangiectasia-mutated and rad3-related (ATR) dependent DNA damage response in Arabidopsis thaliana. Mol Cell Proteomics. 2015;14(3):556–71. doi: 10.1074/mcp.M114.040352 25561503

24. Gordon J, Hwang J, Carrier KJ, Jones CA, Kern QL, Moreno CS, et al. Protein phosphatase 2a (PP2A) binds within the oligomerization domain of striatin and regulates the phosphorylation and activation of the mammalian Ste20-Like kinase Mst3. BMC Biochem. 2011;12:54. doi: 10.1186/1471-2091-12-54 21985334

25. Terenzi HF, Reissig JL. Modifiers of the cot gene in Neurospora: the gulliver mutants. Genetics. 1967;56(2):321–9. 6068178

26. Yarden O, Plamann M, Ebbole DJ, Yanofsky C. cot-1, a gene required for hyphal elongation in Neurospora crassa, encodes a protein kinase. EMBO J. 1992;11(6):2159–66. 1534751

27. Seiler S, Vogt N, Ziv C, Gorovits R, Yarden O. The STE20/germinal center kinase POD6 interacts with the NDR kinase COT1 and is involved in polar tip extension in Neurospora crassa. Mol Biol Cell. 2006;17(9):4080–92. doi: 10.1091/mbc.e06-01-0072 16822837

28. Herold I, Yarden O. Regulation of Neurospora crassa cell wall remodeling via the cot-1 pathway is mediated by gul-1. Curr Genet. 2017;63(1):145–59. doi: 10.1007/s00294-016-0625-z 27363849

29. Herold I, Kowbel D, Delgado-Álvarez DL, Garduño-Rosales M, Mouriño-Pérez RR, Yarden O. Transcriptional profiling and localization of GUL-1, a COT-1 pathway component, in Neurospora crassa. Fungal Genet Biol. 2019;126:1–11. doi: 10.1016/j.fgb.2019.01.010 30731203

30. Sutton A, Immanuel D, Arndt KT. The SIT4 protein phosphatase functions in late G1 for progression into S phase. Mol Cell Biol. 1991;11(4):2133–48. doi: 10.1128/mcb.11.4.2133 1848673

31. Uesono Y, Toh-e A, Kikuchi Y. Ssd1p of Saccharomyces cerevisiae associates with RNA. J Biol Chem. 1997;272(26):16103–9. doi: 10.1074/jbc.272.26.16103 9195905

32. Kurischko C, Kuravi VK, Herbert CJ, Luca FC. Nucleocytoplasmic shuttling of Ssd1 defines the destiny of its bound mRNAs. Mol Microbiol. 2011;81(3):831–49. doi: 10.1111/j.1365-2958.2011.07731.x 21762218

33. Kurischko C, Broach JR. Phosphorylation and nuclear transit modulate the balance between normal function and terminal aggregation of the yeast RNA-binding protein Ssd1. Mol Biol Cell. 2017;28(22):3057–69. doi: 10.1091/mbc.E17-02-0100 28877986

34. Kurischko C, Kim HK, Kuravi VK, Pratzka J, Luca FC. The yeast Cbk1 kinase regulates mRNA localization via the mRNA-binding protein Ssd1. J Cell Biol. 2011;192(4):583–98. doi: 10.1083/jcb.201011061 21339329

35. Nordzieke S, Zobel T, Franzel B, Wolters DA, Kück U, Teichert I. A fungal sarcolemmal membrane-associated protein (SLMAP) homolog plays a fundamental role in development and localizes to the nuclear envelope, endoplasmic reticulum, and mitochondria. Eukaryot Cell. 2015;14(4):345–58. doi: 10.1128/EC.00241-14 25527523

36. Niessing D, Jansen RP, Pohlmann T, Feldbrügge M. mRNA transport in fungal top models. Wiley Interdiscip Rev RNA. 2018;9(1):e1453. doi: 10.1002/wrna.1453

37. Dettmann A, Heilig Y, Valerius O, Ludwig S, Seiler S. Fungal communication requires the MAK-2 pathway elements STE-20 and RAS-2, the NRC-1 adapter STE-50 and the MAP kinase scaffold HAM-5. PLoS Genet. 2014;10(11):e1004762. doi: 10.1371/journal.pgen.1004762 25411845

38. Jonkers W, Leeder AC, Ansong C, Wang Y, Yang F, Starr TL, et al. HAM-5 functions as a MAP kinase scaffold during cell fusion in Neurospora crassa. PLoS Genet. 2014;10(11):e1004783. doi: 10.1371/journal.pgen.1004783 25412208

39. Nowrousian M, Stajich JE, Chu M, Engh I, Espagne E, Halliday K, et al. De novo assembly of a 40 Mb eukaryotic genome from short sequence reads: Sordaria macrospora, a model organism for fungal morphogenesis. PLoS Genet. 2010;6(4):e1000891. doi: 10.1371/journal.pgen.1000891 20386741

40. Kämper J, Kahmann R, Bölker M, Ma LJ, Brefort T, Saville BJ, et al. Insights from the genome of the biotrophic fungal plant pathogen Ustilago maydis. Nature. 2006;444(7115):97–101. doi: 10.1038/nature05248 17080091

41. Nowrousian M. Next-generation sequencing techniques for eukaryotic microorganisms: sequencing-based solutions to biological problems. Eukaryot Cell. 2010;9(9):1300–10. doi: 10.1128/EC.00123-10 20601439

42. Nowrousian M, Teichert I, Masloff S, Kück U. Whole-genome sequencing of Sordaria macrospora mutants identifies developmental genes. G3 (Bethesda). 2012;2(2):261–70. doi: 10.1534/g3.111.001479 22384404

43. Blank-Landeshammer B, Teichert I, Märker R, Nowrousian M, Kück U, Sickmann A. Combination of proteogenomics with peptide de novo sequencing identifies new genes and hidden posttranscriptional modifications. mBio. 2019;10(5):e02367–19. doi: 10.1128/mBio.02367-19 31615963

44. Gouw M, Michael S, Samano-Sanchez H, Kumar M, Zeke A, Lang B, et al. The eukaryotic linear motif resource—2018 update. Nucleic Acids Res. 2018;46(D1):D428–D34. doi: 10.1093/nar/gkx1077 29136216

45. Galzitskaya OV. Repeats are one of the main characteristics of RNA-binding proteins with prion-like domains. Mol Biosyst. 2015;11(8):2210–8. doi: 10.1039/c5mb00273g 26022110

46. Hao Y, Chun A, Cheung K, Rashidi B, Yang X. Tumor suppressor LATS1 is a negative regulator of oncogene YAP. J Biol Chem. 2008;283(9):5496–509. doi: 10.1074/jbc.M709037200 18158288

47. Costanzo M, Baryshnikova A, Bellay J, Kim Y, Spear ED, Sevier CS, et al. The genetic landscape of a cell. Science. 2010;327(5964):425–31. doi: 10.1126/science.1180823 20093466

48. Costanzo M, Baryshnikova A, Myers CL, Andrews B, Boone C. Charting the genetic interaction map of a cell. Curr Opin Biotechnol. 2011;22(1):66–74. doi: 10.1016/j.copbio.2010.11.001 21111604

49. VanderSluis B, Costanzo M, Billmann M, Ward HN, Myers CL, Andrews BJ, et al. Integrating genetic and protein-protein interaction networks maps a functional wiring diagram of a cell. Curr Opin Microbiol. 2018;45:170–9. doi: 10.1016/j.mib.2018.06.004 30059827

50. Baumann S, Pohlmann T, Jungbluth M, Brachmann A, Feldbrügge M. Kinesin-3 and dynein mediate microtubule-dependent co-transport of mRNPs and endosomes. J Cell Sci. 2012;125(Pt 11):2740–52. doi: 10.1242/jcs.101212 22357951

51. Pohlmann T, Baumann S, Haag C, Albrecht M, Feldbrügge M. A FYVE zinc finger domain protein specifically links mRNA transport to endosome trafficking. Elife. 2015;4:e06041.

52. Müller J, Pohlmann T, Feldbrügge M. Core components of endosomal mRNA transport are evolutionarily conserved in fungi. Fungal Genet Biol. 2019;126:12–6. doi: 10.1016/j.fgb.2019.01.013 30738139

53. Kück U, Pöggeler S, Nowrousian M, Nolting N, Engh I. Sordaria macrospora, a model system for fungal development. In: Anke T, editor. THE MYCOTA XV. Heidelberg, New York, Tokyo: Springer Verlag; 2009. p. 17–39.

54. Schumacher DI, Lütkenhaus R, Altegoer F, Teichert I, Kück U, Nowrousian M. The transcription factor PRO44 and the histone chaperone ASF1 regulate distinct aspects of multicellular development in the filamentous fungus Sordaria macrospora. BMC Genet. 2018;19(1):112. doi: 10.1186/s12863-018-0702-z 30545291

55. Galagan JE, Calvo SE, Borkovich KA, Selker EU, Read ND, Jaffe D, et al. The genome sequence of the filamentous fungus Neurospora crassa. Nature. 2003;422(6934):859–68. doi: 10.1038/nature01554 12712197

56. Jankowski S, Pohlmann T, Baumann S, Müntjes K, Devan SK, Zander S, et al. The multi PAM2 protein Upa2 functions as novel core component of endosomal mRNA transport. EMBO Rep. 2019;20(9):e47381. doi: 10.15252/embr.201847381 31338952

57. Dean RA, Talbot NJ, Ebbole DJ, Farman ML, Mitchell TK, Orbach MJ, et al. The genome sequence of the rice blast fungus Magnaporthe grisea. Nature. 2005;434(7036):980–6. doi: 10.1038/nature03449 15846337

58. Thammahong A, Dhingra S, Bultman KM, Kerkaert JD, Cramer RA. An Ssd1 homolog impacts trehalose and chitin biosynthesis and contributes to virulence in Aspergillus fumigatus. mSphere. 2019;4(3):e00244–19. doi: 10.1128/mSphere.00244-19 31068436

59. Muzzey D, Schwartz K, Weissman JS, Sherlock G. Assembly of a phased diploid Candida albicans genome facilitates allele-specific measurements and provides a simple model for repeat and indel structure. Genome Biol. 2013;14(9):R97. doi: 10.1186/gb-2013-14-9-r97 24025428

60. Olgeiser L, Haag C, Boerner S, Ule J, Busch A, Koepke J, et al. The key protein of endosomal mRNP transport Rrm4 binds translational landmark sites of cargo mRNAs. EMBO Rep. 2019;20(1):e46588. doi: 10.15252/embr.201846588 30552148

61. Baumann S, Zander S, Weidtkamp-Peters S, Feldbrügge M. Live cell imaging of septin dynamics in Ustilago maydis. Methods Cell Biol. 2016;136:143–59. doi: 10.1016/bs.mcb.2016.03.021 27473908

62. Zander S, Baumann S, Weidtkamp-Peters S, Feldbrügge M. Endosomal assembly and transport of heteromeric septin complexes promote septin cytoskeleton formation. J Cell Sci. 2016;129(14):2778–92. doi: 10.1242/jcs.182824 27252385

63. Cioni JM, Lin JQ, Holtermann AV, Koppers M, Jakobs MAH, Azizi A, et al. Late endosomes act as mRNA translation platforms and sustain mitochondria in axons. Cell. 2019;176(1–2):56–72 e15. doi: 10.1016/j.cell.2018.11.030 30612743

64. Garza AE, Pojoga LH, Moize B, Hafiz WM, Opsasnick LA, Siddiqui WT, et al. Critical role of striatin in blood pressure and vascular responses to dietary sodium intake. Hypertension. 2015;66(3):674–80. doi: 10.1161/HYPERTENSIONAHA.115.05600 26169051

65. Neisch AL, Neufeld TP, Hays TS. A STRIPAK complex mediates axonal transport of autophagosomes and dense core vesicles through PP2A regulation. J Cell Biol. 2017;216(2):441–61. doi: 10.1083/jcb.201606082 28100687

66. Jerpseth B, Greener A, Short J, Viola J, Kretz P. XL1-blue MRF = E. coli cells: mcrA-, mcrCB-, mcrF-, mmr-, hsdR- derivative of XL1-blue cells. Strateg Mol Biol. 1992;5:81–3.

67. Sambrook J, Russel D. Molecular cloning: a laboratory manual. NY: Cold Spring Harbor Laboratory Press; 2001.

68. James P, Halladay J, Craig EA. Genomic libraries and a host strain designed for highly efficient two-hybrid selection in yeast. Genetics. 1996;144(4):1425–36. 8978031

69. Colot HV, Park G, Turner GE, Ringelberg C, Crew CM, Litvinkova L, et al. A high-throughput gene knockout procedure for Neurospora reveals functions for multiple transcription factors. Proc Natl Acad Sci U S A. 2006;103(27):10352–7. doi: 10.1073/pnas.0601456103 16801547

70. Becker D, Lundblad V. Introduction of DNA into yeast cells. Curr Protoc Mol Biol 1994;27:13–7.

71. Engh I, Würtz C, Witzel-Schlömp K, Zhang HY, Hoff B, Nowrousian M, et al. The WW domain protein PRO40 is required for fungal fertility and associates with woronin bodies. Eukaryot Cell. 2007;6(5):831–43. doi: 10.1128/EC.00269-06 17351077

72. Dirschnabel DE, Nowrousian M, Cano-Domínguez N, Aguirre J, Teichert I, Kück U. New insights into the roles of NADPH oxidases in sexual development and ascospore germination in Sordaria macrospora. Genetics. 2014;196(3):729–44. doi: 10.1534/genetics.113.159368 24407906

73. Burkhart JM, Premsler T, Sickmann A. Quality control of nano-LC-MS systems using stable isotope-coded peptides. Proteomics. 2011;11(6):1049–57. doi: 10.1002/pmic.201000604 21328538

74. Engholm-Keller K, Birck P, Størling J, Pociot F, Mandrup-Poulsen T, Larsen MR. TiSH-a robust and sensitive global phosphoproteomics strategy employing a combination of TiO2, SIMAC, and HILIC. J Proteomics. 2012;75(18):5749–61. doi: 10.1016/j.jprot.2012.08.007 22906719

75. Gonczarowska-Jorge H, Zahedi RP, Sickmann A. The proteome of baker's yeast mitochondria. Mitochondrion. 2017;33:15–21. doi: 10.1016/j.mito.2016.08.007 27535110

76. Thingholm TE, Palmisano G, Kjeldsen F, Larsen MR. Undesirable charge-enhancement of isobaric tagged phosphopeptides leads to reduced identification efficiency. J Proteome Res. 2010;9(8):4045–52. doi: 10.1021/pr100230q 20515019

77. Taus T, Köcher T, Pichler P, Paschke C, Schmidt A, Henrich C, et al. Universal and confident phosphorylation site localization using phosphoRS. J Proteome Res. 2011;10(12):5354–62. doi: 10.1021/pr200611n 22073976

78. Käll L, Canterbury JD, Weston J, Noble WS, MacCoss MJ. Semi-supervised learning for peptide identification from shotgun proteomics datasets. Nat Methods. 2007;4(11):923–5. doi: 10.1038/nmeth1113 17952086

79. Cheng A, Grant CE, Noble WS, Bailey TL. MoMo: discovery of statistically significant post-translational modification motifs. Bioinformatics. 2019;35(16):2774–82. doi: 10.1093/bioinformatics/bty1058 30596994

80. Pöggeler S, Kück U. Highly efficient generation of signal transduction knockout mutants using a fungal strain deficient in the mammalian ku70 ortholog. Gene. 2006;378:1–10. doi: 10.1016/j.gene.2006.03.020 16814491

81. Rech C, Engh I, Kück U. Detection of hyphal fusion in filamentous fungi using differently fluorescence-labeled histones. Curr Genet. 2007;52(5–6):259–66. doi: 10.1007/s00294-007-0158-6 17929020

82. Haag C, Pohlmann T, Feldbrügge M. The ESCRT regulator Did2 maintains the balance between long-distance endosomal transport and endocytic trafficking. PLoS Genet. 2017;13(4):e1006734. doi: 10.1371/journal.pgen.1006734 28422978

83. Vizcaíno JA, Deutsch EW, Wang R, Csordas A, Reisinger F, Rios D, et al. ProteomeXchange provides globally coordinated proteomics data submission and dissemination. Nat Biotechnol. 2014;32(3):223–6. doi: 10.1038/nbt.2839 24727771

84. Swaney DL, Beltrao P, Starita L, Guo AL, Rush J, Fields S, et al. Global analysis of phosphorylation and ubiquitylation cross-talk in protein degradation. Nature Methods. 2013;10(7):676–82. doi: 10.1038/nmeth.2519 23749301

85. Sancar C, Ha N, Yilmaz R, Tesorero R, Fisher T, Brunner M, et al. Combinatorial control of light induced chromatin remodeling and gene activation in Neurospora. PLoS Genet. 2015;11(3):e1005105. doi: 10.1371/journal.pgen.1005105 25822411

86. Birney E, Kumar S, Krainer AR. Analysis of the RNA-recognition motif and RS and RGG domains: conservation in metazoan pre-mRNA splicing factors. Nucleic Acids Res. 1993;21(25):5803–16. doi: 10.1093/nar/21.25.5803 8290338

Článek vyšel v časopise

PLOS Genetics

2020 Číslo 9
Nejčtenější tento týden
Nejčtenější v tomto čísle

Zvyšte si kvalifikaci online z pohodlí domova

Hypertenze a hypercholesterolémie – synergický efekt léčby
nový kurz
Autoři: prof. MUDr. Hana Rosolová, DrSc.

Multidisciplinární zkušenosti u pacientů s diabetem
Autoři: Prof. MUDr. Martin Haluzík, DrSc., prof. MUDr. Vojtěch Melenovský, CSc., prof. MUDr. Vladimír Tesař, DrSc.

Úloha kombinovaných preparátů v léčbě arteriální hypertenze
Autoři: prof. MUDr. Martin Haluzík, DrSc.

Autoři: MUDr. Ladislav Korábek, CSc., MBA

Terapie roztroušené sklerózy v kostce
Autoři: MUDr. Dominika Šťastná, Ph.D.

Všechny kurzy
Zapomenuté heslo

Zadejte e-mailovou adresu, se kterou jste vytvářel(a) účet, budou Vám na ni zaslány informace k nastavení nového hesla.


Nemáte účet?  Registrujte se