Home LiteratureArticle Details
PMID: 26898182 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't Review

VAP, a Versatile Access Point for the Endoplasmic Reticulum: Review and analysis of FFAT-like motifs in the VAPome.

Biochimica et biophysica acta ·Vol. 1861 ·No. 8 Pt B ·2016-08-00 ·Pages 952-961

Murphy SE, Levine TP

Abstract

Dysfunction of VAMP-associated protein (VAP) is associated with neurodegeneration, both Amyotrophic Lateral Sclerosis and Parkinson's disease. Here we summarize what is known about the intracellular interactions of VAP in humans and model organisms. VAP is a simple, small and highly conserved protein on the cytoplasmic face of the endoplasmic reticulum (ER). It is the sole protein on that large organelle that acts as a receptor for cytoplasmic proteins. This may explain the extremely wide range of interacting partners of VAP, with components of many cellular pathways binding it to access the ER. Many proteins that bind VAP also target other intracellular membranes, so VAP is a component of multiple molecular bridges at membrane contact sites between the ER and other organelles. So far approximately 100 proteins have been identified in the VAP interactome (VAPome), of which a small minority have a "two phenylalanines in an acidic tract" (FFAT) motif as it was originally defined. We have analyzed the entire VAPome in humans and yeast using a simple algorithm that identifies many more FFAT-like motifs. We show that approximately 50% of the VAPome binds directly or indirectly via the VAP-FFAT interaction. We also review evidence on pathogenesis in genetic disorders of VAP, which appear to arise from reduced overall VAP levels, leading to ER stress. It is not possible to identify one single interaction that underlies disease. This article is part of a Special Issue entitled: The cellular lipid landscape edited by Tim P. Levine and Anant K. Menon.

Keywords
Amyotrophic Lateral Sclerosis/genetics Biological Transport Endoplasmic Reticulum/*metabolism Intracellular Membranes/*metabolism Motor Neurons/*metabolism Vesicular Transport Proteins/genetics/*metabolism
MeSH Terms
Amino Acid Motifs Amino Acid Sequence Animals Endoplasmic Reticulum/metabolism Humans Molecular Sequence Data Protein Binding Protein Interaction Domains and Motifs/physiology Protein Interaction Maps Vesicular Transport Proteins/chemistry,metabolism,physiology
Chemicals
VAPA protein, human VAPB protein, human Vesicular Transport Proteins
Authors & Affiliations
2 authors, click to expand affiliations / ORCID
Murphy Sarah E
Department of Cell Biology, UCL Institute of Ophthalmology, 11-43 Bath Street, UK EC1V 9EL.
Levine Tim P
Department of Cell Biology, UCL Institute of Ophthalmology, 11-43 Bath Street, UK EC1V 9EL. Electronic address: [email protected].
References (57)
57 references, click to expand
  1. A bacterial control circuit integrates polar localization and proteolysis of key regulatory proteins with a phospho-signaling cascade.
    Proc Natl Acad Sci U S A. 2008 Oct 28;105(43):16602-7 PMID: 18946044
  2. A dual binding site for integration host factor and the response regulator CtrA inside the Caulobacter crescentus replication origin.
    J Bacteriol. 2003 Sep;185(18):5563-72 PMID: 12949109
  3. Getting in the loop: regulation of development in Caulobacter crescentus.
    Microbiol Mol Biol Rev. 2010 Mar;74(1):13-41 PMID: 20197497
  4. Functions of the CckA histidine kinase in Caulobacter cell cycle control.
    Mol Microbiol. 2003 Mar;47(5):1279-90 PMID: 12603734
  5. The chromosome partitioning protein, ParB, is required for cytokinesis in Caulobacter crescentus.
    Mol Microbiol. 2001 Nov;42(3):741-55 PMID: 11722739
  6. Cell cycle-dependent polar localization of chromosome partitioning proteins in Caulobacter crescentus.
    Cell. 1997 Mar 7;88(5):675-84 PMID: 9054507
  7. Cell-cycle progression and the generation of asymmetry in Caulobacter crescentus.
    Nat Rev Microbiol. 2004 Apr;2(4):325-37 PMID: 15031731
  8. Analysis of nonmotile mutants of the dimorphic bacterium Caulobacter crescentus.
    J Bacteriol. 1979 Jan;137(1):627-34 PMID: 762024
  9. Structure and signaling mechanism of Per-ARNT-Sim domains.
    Structure. 2009 Oct 14;17(10):1282-94 PMID: 19836329
  10. Cytokinesis signals truncation of the PodJ polarity factor by a cell cycle-regulated protease.
    EMBO J. 2006 Jan 25;25(2):377-86 PMID: 16395329
  11. Cell type-specific phosphorylation and proteolysis of a transcriptional regulator controls the G1-to-S transition in a bacterial cell cycle.
    Cell. 1997 Aug 8;90(3):415-24 PMID: 9267022
  12. Comparative analysis of Caulobacter chromosome replication origins.
    Microbiology. 2009 Apr;155(Pt 4):1215-25 PMID: 19332823
  13. Cell cycle transition from S-phase to G1 in Caulobacter is mediated by ancestral virulence regulators.
    Nat Commun. 2014 Jun 18;5:4081 PMID: 24939058
  14. Cloning of a factor required for activity of the Ah (dioxin) receptor.
    Science. 1991 May 17;252(5008):954-8 PMID: 1852076
  15. Integration of cell cycle signals by multi-PAS domain kinases.
    Proc Natl Acad Sci U S A. 2018 Jul 24;115(30):E7166-E7173 PMID: 29987042
  16. Control of chromosome replication in caulobacter crescentus.
    Annu Rev Microbiol. 2002;56:625-56 PMID: 12142494
  17. Branched signal wiring of an essential bacterial cell-cycle phosphotransfer protein.
    Structure. 2013 Sep 3;21(9):1590-601 PMID: 23932593
  18. A cell-type-specific protein-protein interaction modulates transcriptional activity of a master regulator in Caulobacter crescentus.
    Mol Cell. 2010 Aug 13;39(3):455-67 PMID: 20598601
  19. Signal transduction in histidine kinases: insights from new structures.
    Structure. 2015 Jun 2;23(6):981-94 PMID: 25982528
  20. Spatial and temporal control of differentiation and cell cycle progression in Caulobacter crescentus.
    Annu Rev Microbiol. 2003;57:225-47 PMID: 14527278
  21. The BAM complex subunit BamE (SmpA) is required for membrane integrity, stalk growth and normal levels of outer membrane {beta}-barrel proteins in Caulobacter crescentus.
    Microbiology. 2010 Mar;156(Pt 3):742-56 PMID: 19959579
  22. Dynamics of two Phosphorelays controlling cell cycle progression in Caulobacter crescentus.
    J Bacteriol. 2009 Dec;191(24):7417-29 PMID: 19783630
  23. NIH Image to ImageJ: 25 years of image analysis.
    Nat Methods. 2012 Jul;9(7):671-5 PMID: 22930834
  24. Cyclic di-GMP acts as a cell cycle oscillator to drive chromosome replication.
    Nature. 2015 Jul 9;523(7559):236-9 PMID: 25945741
  25. Identification and cell cycle control of a novel pilus system in Caulobacter crescentus.
    EMBO J. 2000 Jul 3;19(13):3223-34 PMID: 10880436
  26. Polar localization of the CckA histidine kinase and cell cycle periodicity of the essential master regulator CtrA in Caulobacter crescentus.
    J Bacteriol. 2010 Jan;192(2):539-52 PMID: 19897656
  27. Direct observation of extension and retraction of type IV pili.
    Proc Natl Acad Sci U S A. 2001 Jun 5;98(12):6901-4 PMID: 11381130
  28. The Caulobacter crescentus chromosome replication origin evolved two classes of weak DnaA binding sites.
    Mol Microbiol. 2011 Oct;82(2):312-26 PMID: 21843309
  29. Genes directly controlled by CtrA, a master regulator of the Caulobacter cell cycle.
    Proc Natl Acad Sci U S A. 2002 Apr 2;99(7):4632-7 PMID: 11930012
  30. Genetics of Caulobacter crescentus.
    Methods Enzymol. 1991;204:372-84 PMID: 1658564
  31. Structural asymmetry in a conserved signaling system that regulates division, replication, and virulence of an intracellular pathogen.
    Proc Natl Acad Sci U S A. 2015 Jul 14;112(28):E3709-18 PMID: 26124143
  32. Cyclic di-GMP mediates a histidine kinase/phosphatase switch by noncovalent domain cross-linking.
    Sci Adv. 2016 Sep 16;2(9):e1600823 PMID: 27652341
  33. Coupling prokaryotic cell fate and division control with a bifunctional and oscillating oxidoreductase homolog.
    Dev Cell. 2010 Jan 19;18(1):90-101 PMID: 20152180
  34. MreB, the cell shape-determining bacterial actin homologue, co-ordinates cell wall morphogenesis in Caulobacter crescentus.
    Mol Microbiol. 2004 Mar;51(5):1321-32 PMID: 14982627
  35. Mutation of the sensor kinase chvG in Rhizobium leguminosarum negatively impacts cellular metabolism, outer membrane stability, and symbiosis.
    J Bacteriol. 2012 Feb;194(4):768-77 PMID: 22155778
  36. An essential transcription factor, SciP, enhances robustness of Caulobacter cell cycle regulation.
    Proc Natl Acad Sci U S A. 2010 Nov 2;107(44):18985-90 PMID: 20956288
  37. Regulation of the activity of the dual-function DnaA protein in Caulobacter crescentus.
    PLoS One. 2011;6(10):e26028 PMID: 22022497
  38. CtrA controls cell division and outer membrane composition of the pathogen Brucella abortus.
    Mol Microbiol. 2017 Mar;103(5):780-797 PMID: 27893179
  39. A cell cycle-controlled redox switch regulates the topoisomerase IV activity.
    Genes Dev. 2015 Jun 1;29(11):1175-87 PMID: 26063575
  40. A cell cycle kinase with tandem sensory PAS domains integrates cell fate cues.
    Nat Commun. 2016 Apr 27;7:11454 PMID: 27117914
  41. Temporal regulation of genes encoding the flagellar proximal rod in Caulobacter crescentus.
    J Bacteriol. 2001 Jan;183(2):725-35 PMID: 11133968
  42. Organization of the flaFG gene cluster and identification of two additional genes involved in flagellum biogenesis in Caulobacter crescentus.
    J Bacteriol. 1989 Mar;171(3):1544-53 PMID: 2921244
  43. The CtrA response regulator essential for Caulobacter crescentus cell-cycle progression requires a bipartite degradation signal for temporally controlled proteolysis.
    J Mol Biol. 2002 Nov 29;324(3):443-55 PMID: 12445780
  44. Cell cycle-dependent polar localization of an essential bacterial histidine kinase that controls DNA replication and cell division.
    Cell. 1999 Apr 2;97(1):111-20 PMID: 10199407
  45. Mutations in DivL and CckA rescue a divJ null mutant of Caulobacter crescentus by reducing the activity of CtrA.
    J Bacteriol. 2006 Apr;188(7):2473-82 PMID: 16547034
  46. Caulobacter chromosome segregation is an ordered multistep process.
    Proc Natl Acad Sci U S A. 2010 Aug 10;107(32):14194-8 PMID: 20660743
  47. The DivJ, CbrA and PleC system controls DivK phosphorylation and symbiosis in Sinorhizobium meliloti.
    Mol Microbiol. 2013 Oct;90(1):54-71 PMID: 23909720
  48. In-phase oscillation of global regulons is orchestrated by a pole-specific organizer.
    Proc Natl Acad Sci U S A. 2016 Nov 1;113(44):12550-12555 PMID: 27791133
  49. BIOLOGICAL PROPERTIES AND CLASSIFICATION OF THE CAULOBACTER GROUP.
    Bacteriol Rev. 1964 Sep;28:231-95 PMID: 14220656
  50. Regulation of the bacterial cell cycle by an integrated genetic circuit.
    Nature. 2006 Dec 14;444(7121):899-904 PMID: 17136100
  51. Visualizing autophosphorylation in histidine kinases.
    Nat Commun. 2014;5:3258 PMID: 24500224
  52. The dynamic interplay between a cell fate determinant and a lysozyme homolog drives the asymmetric division cycle of Caulobacter crescentus.
    Genes Dev. 2008 Jan 15;22(2):212-25 PMID: 18198338
  53. Getting organized--how bacterial cells move proteins and DNA.
    Nat Rev Microbiol. 2008 Jan;6(1):28-40 PMID: 18059290
  54. A membrane metalloprotease participates in the sequential degradation of a Caulobacter polarity determinant.
    Mol Microbiol. 2005 Feb;55(4):1085-103 PMID: 15686556
  55. CtrA, a global response regulator, uses a distinct second category of weak DNA binding sites for cell cycle transcription control in Caulobacter crescentus.
    J Bacteriol. 2009 Sep;191(17):5458-70 PMID: 19542275
  56. An essential protease involved in bacterial cell-cycle control.
    EMBO J. 1998 Oct 1;17(19):5658-69 PMID: 9755166
  57. Signal transduction mechanisms in Caulobacter crescentus development and cell cycle control.
    FEMS Microbiol Rev. 2000 Apr;24(2):177-91 PMID: 10717313
Article Info
Journal
Biochimica et biophysica acta
Abbr.
Biochim Biophys Acta
ISSN
0006-3002
Published
2016-08-00
Epub
2016-00-17
Pages
952-961
Language
English
Region
Netherlands
NLM ID
0217513
Subset
IM
Grants
Biotechnology and Biological Sciences Research Council · BB/M011801/1 · United Kingdom
Biotechnology and Biological Sciences Research Council · BB/L016028 · United Kingdom
Biotechnology and Biological Sciences Research Council · BB/M011801 · United Kingdom
Analysis Services
Analysis Services

Contact

No. 2 Wenbo Road, Zhangqiu District, Jinan, Shandong

Qilu Normal University · Genelibs Bioinformatics Lab

750 Shunhua Rd, Jinan

2F, Bldg F, University Science Park

Tel: 0531-88819269

WeChat Official Account

Follow our WeChat subscription account for real-time updates and the latest in medical and biological research.


Business Email

E-mail: [email protected]