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Cited by 13Cellular transport and secretionProtein Structure and DynamicsMicrotubule and mitosis dynamics

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Resurrecting Golgi proteins to grasp Golgi ribbon formation and self-association under stress

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Mendes, Luis F.S., Batista, Mariana R.B., Kava, Emanuel, Bleicher, Lucas, Micheletto, Mariana C., Costa-Filho, Antonio J.·2022·International Journal of Biological Macromolecules
DOI 10.1016/j.ijbiomac.2021.11.173

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Abstract

The Golgi complex is an essential organelle of the eukaryotic exocytic pathway. A subfamily of Golgi matrix proteins, called GRASPs, is central in stress-induced unconventional secretion, Golgi dynamics during mitosis/apoptosis, and Golgi ribbon formation. The Golgi ribbon is vertebrate-specific and correlates with the appearance of two GRASP paralogues and two Golgins (GM130/Golgin45), which form specific GRASP-Golgin pairs. The molecular details of their appearance only in Metazoans are unknown. Moreover, despite new functionalities supported by GRASP paralogy, little is known about their structural and evolutionary differences. Here, we used ancestor sequence reconstruction and biophysical/biochemical approaches to assess the evolution of GRASPs structure/dynamics, fibrillation, and how they started anchoring their Golgin partners. Our data showed that a GRASP ancestor anchored Golgins before gorasp gene duplication in Metazoans. After gene duplication, variations within the GRASP binding pocket determined which paralogue would recruit which Golgin. These interactions are responsible for their specific Golgi location and Golgi ribbon appearance. We also suggest that GRASPs have a long-standing capacity to form supramolecular structures, affecting their participation in stress-induced processes.

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Research works printed but not linked: 84

  1. Palade, 1975, Intracellular aspects of process of protein-synthesis, Science, 189, 347, 10.1126/science.1096303 · DOI
  2. Rabouille, 2017, Pathways of unconventional protein secretion, Trends Cell Biol., 27, 230, 10.1016/j.tcb.2016.11.007 · DOI
  3. Kinseth, 2007, The golgi-associated protein GRASP is required for unconventional protein secretion during development, Cell, 130, 524, 10.1016/j.cell.2007.06.029 · DOI
  4. Fontana, 2018, The yeast GRASP Grh1 displays a high polypeptide backbone mobility along with an amyloidogenic behavior, Sci. Rep., 8, 10.1038/s41598-018-33955-1 · DOI
  5. Chiritoiu, 2019, GRASP55 and UPR control Interleukin-1 beta aggregation and secretion, Dev. Cell, 49, 145-+, 10.1016/j.devcel.2019.02.011 · DOI
  6. Gee, 2011, Rescue of delta F508-CFTR trafficking via a GRASP-dependent unconventional secretion pathway, Cell, 146, 746, 10.1016/j.cell.2011.07.021 · DOI
  7. Schotman, 2008, dGRASP-mediated noncanonical integrin secretion is required for drosophila epithelial remodeling, Dev. Cell, 14, 171, 10.1016/j.devcel.2007.12.006 · DOI
  8. Bruns, 2011, Biogenesis of a novel compartment for autophagosome-mediated unconventional protein secretion, J. Cell Biol., 195, 979, 10.1083/jcb.201106098 · DOI
  9. Son, 2016, Insulin-degrading enzyme secretion from astrocytes is mediated by an autophagy-based unconventional secretory pathway in alzheimer disease, Autophagy, 12, 784, 10.1080/15548627.2016.1159375 · DOI
  10. Ahat, 2019, New insights into the golgi stacking proteins, Front. Cell Dev. Biol., 7, 10.3389/fcell.2019.00131 · DOI
  11. Mendes, 2020, The exquisite structural biophysics of the golgi reassembly and stacking proteins, Int. J. Biol. Macromol., 164, 3632, 10.1016/j.ijbiomac.2020.08.203 · DOI
  12. Wu, 2020, GRASP55: a multifunctional protein, Curr. Protein Pept. Sci., 21, 544, 10.2174/1389203721666200218105302 · DOI
  13. Zhang, 2020, Nonredundant roles of GRASP55 and GRASP65 in the golgi apparatus and beyond, Trends Biochem. Sci., 45, 1065, 10.1016/j.tibs.2020.08.001 · DOI
  14. Rabouille, 2016, GRASP: a multitasking tether, Front. Cell Dev. Biol., 4, 10.3389/fcell.2016.00001 · DOI
  15. Zhang, 2016, GRASPs in golgi structure and function, Front. Cell Dev. Biol., 3, 10.3389/fcell.2015.00084 · DOI
  16. Mendes, 2019, The GRASP domain in golgi reassembly and stacking proteins: differences and similarities between lower and higher eukaryotes, FEBS J., 286, 3340, 10.1111/febs.14869 · DOI
  17. Vinke, 2011, The multiple facets of the golgi reassembly stacking proteins, Biochem. J., 433, 423, 10.1042/BJ20101540 · DOI
  18. Barr, 1998, Mapping the interaction between GRASP65 and GM130, components of a protein complex involved in the stacking of golgi cisternae, EMBO J., 17, 3258, 10.1093/emboj/17.12.3258 · DOI
  19. Barr, 1997, GRASP65, a protein involved in the stacking of golgi cisternae, Cell, 91, 253, 10.1016/S0092-8674(00)80407-9 · DOI
  20. Shorter, 1999, GRASP55, a second mammalian GRASP protein involved in the stacking of golgi cisternae in a cell-free system, EMBO J., 18, 4949, 10.1093/emboj/18.18.4949 · DOI
  21. Zhang, 2020, Rapid degradation of GRASP55 and GRASP65 reveals their immediate impact on the golgi structure, J. Cell Biol., 220
  22. Grond, 2020, The function of GORASPs in golgi apparatus organization in vivo, J. Cell Biol., 219
  23. Feng, 2013, Structural insight into golgi membrane stacking by GRASP65 and GRASP55 proteins, J. Biol. Chem., 288, 28418, 10.1074/jbc.M113.478024 · DOI
  24. Mendes, 2020, Conformational flexibility of GRASPs and their constituent PDZ subdomains reveals structural basis of their promiscuous interactome, FEBS J., 287, 3255, 10.1111/febs.15206 · DOI
  25. Mendes, 2016, New structural insights into golgi reassembly and stacking protein (GRASP) in solution, Sci. Rep., 6, 10.1038/srep29976 · DOI
  26. Mendes, 2018, Disorder-to-order transitions in the molten globule-like golgi reassembly and stacking protein, Biochim. Biophys. Acta, Gen. Subj., 1862, 855, 10.1016/j.bbagen.2018.01.009 · DOI
  27. Ayala, 2018, GRASP65-mediated control of the golgi structure is crucial for G2/M transition, Mol. Biol. Cell, 29
  28. Tang, 2010, The role of GRASP65 in golgi cisternal stacking and cell cycle progression, Traffic, 11, 827, 10.1111/j.1600-0854.2010.01055.x · DOI
  29. Lane, 2002, Caspase-mediated cleavage of the stacking protein GRASP65 is required for golgi fragmentation during apoptosis, J. Cell Biol., 156, 495, 10.1083/jcb.200110007 · DOI
  30. Lee, 2014, Membrane adhesion dictates Golgi stacking and cisternal morphology, Proc. Natl. Acad. Sci. U. S. A., 111, 1849, 10.1073/pnas.1323895111 · DOI
  31. Seemann, 2000, Matrix proteins can generate the higher order architecture of the Golgi apparatus, Nature, 407, 1022, 10.1038/35039538 · DOI
  32. Rebane, 2020, Liquid-liquid phase separation of the Golgi matrix protein GM130, FEBS Lett., 594, 1132, 10.1002/1873-3468.13715 · DOI
  33. Reddy, 2020, Nucleation-dependent amyloid fibrillation of human GRASP55 in aqueous solution, Eur. Biophys. J. Biophys. Lett., 49, 133, 10.1007/s00249-019-01419-7 · DOI
  34. Eme, 2014, On the age of eukaryotes: evaluating evidence from fossils and molecular clocks, Cold Spring Harb. Perspect. Biol., 6, 10.1101/cshperspect.a016139 · DOI · Paper page
  35. Barlow, 2018, A sophisticated, differentiated Golgi in the ancestor of eukaryotes, BMC Biol., 16
  36. Uversky, 2021, The protein disorder cycle, Biophys. Rev., 10.1007/s12551-021-00853-2 · DOI
  37. Kyte, 1982, A simple method for displaying the hydropathic character of a protein, J. Mol. Biol., 157, 105, 10.1016/0022-2836(82)90515-0 · DOI
  38. Cilia, 2013, From protein sequence to dynamics and disorder with DynaMine, Nat. Commun., 4, 10.1038/ncomms3741 · DOI
  39. Cilia, 2014, The DynaMine webserver: predicting protein dynamics from sequence, Nucleic Acids Res., 42, W264, 10.1093/nar/gku270 · DOI
  40. Ferreiro, 2007, Localizing frustration in native proteins and protein assemblies, Proc. Natl. Acad. Sci. U. S. A., 104, 19819, 10.1073/pnas.0709915104 · DOI
  41. Ferreiro, 2011, On the role of frustration in the energy landscapes of allosteric proteins, Proc. Natl. Acad. Sci. U. S. A., 108, 3499, 10.1073/pnas.1018980108 · DOI
  42. Zhao, 2017, Structural Basis for the Interaction between Golgi Reassembly-stacking Protein GRASP55 and Golgin45, J. Biol. Chem., 292, 2956, 10.1074/jbc.M116.765990 · DOI
  43. Hu, 2015, Structural basis for the interaction between the golgi reassembly-stacking protein GRASP65 and the Golgi matrix protein GM130, J. Biol. Chem., 290, 26373, 10.1074/jbc.M115.657940 · DOI
  44. Parra, 2016, Protein frustratometer 2: a tool to localize energetic frustration in protein molecules, now with electrostatics, Nucleic Acids Res., 44, W356, 10.1093/nar/gkw304 · DOI
  45. Ashkenazy, 2016, ConSurf 2016: an improved methodology to estimate and visualize evolutionary conservation in macromolecules, Nucleic Acids Res., 44, W344, 10.1093/nar/gkw408 · DOI · Paper page
  46. Bologna, 2004, N-Terminal myristoylation predictions by ensembles of neural networks, Proteomics, 4, 1626, 10.1002/pmic.200300783 · DOI
  47. Bachert, 2010, Dual anchoring of the GRASP membrane tether promotes trans pairing, J. Biol. Chem., 285, 16294, 10.1074/jbc.M110.116129 · DOI
  48. Kava, 2021, Myristoylation and its effects on the human Golgi reassembly and stacking protein 55, Biophys. Chem., 279, 10.1016/j.bpc.2021.106690 · DOI
  49. Reddy, 2020, Biophysical characterization of intrinsically disordered human Golgi matrix protein GRASP65, Int. J. Biol. Macromol., 162, 1982, 10.1016/j.ijbiomac.2020.08.126 · DOI
  50. Boyko, 2020, Regulatory mechanisms of tau protein fibrillation under the conditions of liquid-liquid phase separation, Proc. Natl. Acad. Sci. U. S. A., 117, 31882, 10.1073/pnas.2012460117 · DOI
  51. Babinchak, 2019, The role of liquid-liquid phase separation in aggregation of the TDP-43 low-complexity domain, J. Biol. Chem., 294, 6306, 10.1074/jbc.RA118.007222 · DOI
  52. Ray, 2020, alpha-Synuclein aggregation nucleates through liquid-liquid phase separation, Nat. Chem., 12, 10.1038/s41557-020-0465-9 · DOI · Paper page
  53. Wegmann, 2018, Tau protein liquid-liquid phase separation can initiate tau aggregation, EMBO J., 37, 10.15252/embj.201798049 · DOI · Paper page
  54. Fuxreiter, 2021, Generic nature of the condensed states of proteins, Nat. Cell Biol., 23, 587, 10.1038/s41556-021-00697-8 · DOI
  55. Ziaunys, 2019, Exploring the potential of deep-blue autofluorescence for monitoring amyloid fibril formation and dissociation, Peerj, 7, 10.7717/peerj.7554 · DOI
  56. Guptasarma, 2008, Solution-state characteristics of the ultraviolet A-induced visible fluorescence from proteins, Arch. Biochem. Biophys., 478, 127, 10.1016/j.abb.2008.08.002 · DOI
  57. Chan, 2013, Protein amyloids develop an intrinsic fluorescence signature during aggregation, Analyst, 138, 2156, 10.1039/c3an36798c · DOI
  58. Sormanni, 2019, Protein solubility predictions using the camsol method in the study of protein homeostasis, Cold Spring Harb. Perspect. Biol., 11, 10.1101/cshperspect.a033845 · DOI
  59. Joshi, 2014, A beta-induced Golgi fragmentation in Alzheimer's disease enhances A beta production, Proc. Natl. Acad. Sci. U. S. A., 111, E1230, 10.1073/pnas.1320192111 · DOI
  60. Wang, 2019, Golgi reassembly and stacking protein 65 downregulation is required for the anti-cancer effect of dihydromyricetin on human ovarian cancer cells, PLoS One, 14, 10.1371/journal.pone.0225450 · DOI
  61. Nüchel, 2021, An mTORC1-GRASP55 signaling axis controls unconventional secretion to reshape the extracellular proteome upon stress, Mol. Cell, 81, 3275, 10.1016/j.molcel.2021.06.017 · DOI
  62. Zhang, 2018, The Golgi stacking protein GORASP2/GRASP55 serves as an energy sensor to promote autophagosome maturation under glucose starvation, Autophagy, 14, 1649, 10.1080/15548627.2018.1491214 · DOI
  63. Zhang, 2018, GRASP55 senses glucose deprivation through O-GlcNAcylation to, Dev. Cell, 45, 245-+, 10.1016/j.devcel.2018.03.023 · DOI
  64. Tang, 2016, Mena-GRASP65 interaction couples actin polymerization to Golgi ribbon linking, Mol. Biol. Cell, 27, 137, 10.1091/mbc.E15-09-0650 · DOI
  65. Li, 2019, DjA1 maintains Golgi integrity via interaction with GRASP65, Mol. Biol. Cell, 30, 478, 10.1091/mbc.E18-10-0613 · DOI
  66. Cheng, 2010, Caspase cleavage of the Golgi stacking factor GRASP65 is required for Fas/CD95-mediated apoptosis, Cell Death Dis., 1, 10.1038/cddis.2010.59 · DOI
  67. Sutterlin, 2005, The Golgi-associated protein GRASP65 regulates spindle dynamics and is essential for cell division, Mol. Biol. Cell, 16, 3211, 10.1091/mbc.e04-12-1065 · DOI
  68. Ayala, 2019, GRASP65 controls Golgi position and structure during G2/M transition by regulating the stability of microtubules, Traffic, 20, 785, 10.1111/tra.12682 · DOI
  69. Wei, 2010, Unraveling the Golgi Ribbon, Traffic, 11, 1391, 10.1111/j.1600-0854.2010.01114.x · DOI
  70. Xiang, 2013, Regulation of protein glycosylation and sorting by the Golgi matrix proteins GRASP55/65, Nat. Commun., 4
  71. Zhang, 2017, GRASP55 senses energy deprivation through O-GlcNAcylation to promote autophagosome-lysosome fusion, Mol. Biol. Cell, 28
  72. Sammut, 2008, Pfam 10 years on: 10 000 families and still growing, Brief. Bioinform., 9, 210, 10.1093/bib/bbn010 · DOI
  73. Mistry, 2021, Pfam: The protein families database in 2021, Nucleic Acids Res., 49, D412, 10.1093/nar/gkaa913 · DOI · Paper page
  74. Sievers, 2018, Clustal Omega for making accurate alignments of many protein sequences, Protein Sci., 27, 135, 10.1002/pro.3290 · DOI · Paper page
  75. Madeira, 2019, The EMBL-EBI search and sequence analysis tools APIs in 2019, Nucleic Acids Res., 47, W636, 10.1093/nar/gkz268 · DOI · Paper page
  76. Liu, 2010, MSAProbs: multiple sequence alignment based on pair hidden Markov models and partition function posterior probabilities, Bioinformatics, 26, 1958, 10.1093/bioinformatics/btq338 · DOI
  77. Stamatakis, 2005, RAxML-III: a fast program for maximum likelihood-based inference of large phylogenetic trees, Bioinformatics, 21, 456, 10.1093/bioinformatics/bti191 · DOI
  78. Hanson-Smith, 2016, PhyloBot: a web portal for automated phylogenetics, ancestral sequence reconstruction, and exploration of mutational trajectories, PLoS Comput. Biol., 12, 10.1371/journal.pcbi.1004976 · DOI
  79. Yang, 2007, PAML 4: phylogenetic analysis by maximum likelihood, Mol. Biol. Evol., 24, 1586, 10.1093/molbev/msm088 · DOI · Paper page
  80. Hanson-Smith, 2010, Robustness of ancestral sequence reconstruction to phylogenetic uncertainty, Mol. Biol. Evol., 27, 1988, 10.1093/molbev/msq081 · DOI
  81. Fonseca, 2020, CONAN: a web application to detect specificity determinants and functional sites by amino acids co-variation network analysis, Bioinformatics, 37, 1026, 10.1093/bioinformatics/btaa713 · DOI
  82. Tumminello, 2011, Statistically validated networks in bipartite complex systems, PLoS One, 6, 10.1371/journal.pone.0017994 · DOI
  83. Yang, 2015, I-TASSER server: new development for protein structure and function predictions, Nucleic Acids Res., 43, W174, 10.1093/nar/gkv342 · DOI
  84. Waterhouse, 2018, SWISS-MODEL: homology modelling of protein structures and complexes, Nucleic Acids Res., 46, W296, 10.1093/nar/gky427 · DOI

Metadata

Authors
Mendes, L. F. S., Batista, M. R. B., Kava, E., Bleicher, L., Micheletto, M. C., & Costa-Filho, A. J.
Affiliations
  • Universidade de São Paulo (BR)
  • Universidade Federal de Minas Gerais (BR)
Corresponding author
Costa-Filho, Antonio J.
ORCID
Venue
International Journal of Biological Macromolecules
Publisher
Elsevier BV
Published
2022-01
Volume
194
Pages
264-275
ISSN
0141-8130 (ISSN-L)
DOI
10.1016/j.ijbiomac.2021.11.173
OpenAlex
W3216691600
Cited by
13
References
6
Citations by year
2026: 5 · 2025: 1 · 2024: 3 · 2023: 4
FWCI
0.91
Type
journal article
Language
en
Open access
Licence
Locations
  • International Journal of Biological Macromolecules (publishedVersion)
  • bioRxiv (Cold Spring Harbor Laboratory) (acceptedVersion, cc-by-nc-nd)
  • PubMed (publishedVersion)
  • Warwick Research Archive Portal (University of Warwick) (submittedVersion)
Funders
  • CNPq (306682/2018-4)
  • FAPESP (2012/20367-3, 2017/24669-8, 2015/50366-7, 2016/16328-3)
  • Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (88882.378790/2019-01, 15/16812-0, 2018/13016-6)
Topics
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Cell Biology › Cellular transport and secretion
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Protein Structure and Dynamics
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Cell Biology › Microtubule and mitosis dynamics
Keywords
Golgi ribbon, GRASP, golgins, GM130, gene duplication, protein evolution, protein fibrillation, Golgi dynamics, Golgi apparatus
MeSH terms
Golgi Matrix Proteins, Amino Acid Sequence, Golgi Apparatus, Models, Molecular, Phylogeny, Protein Binding, Protein Conformation, Stress, Physiological, Structure-Activity Relationship, Thermodynamics, Protein Transport, Hydrophobic and Hydrophilic Interactions

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