Skip to main content
SpringerLink
Log in

Plant-specific 4/1 polypeptide interacts with an endoplasmic reticulum protein related to human BAP31

  • Original Article
  • Published:
Planta Aims and scope Submit manuscript

Abstract

Main conclusion

The plant-specific 4/1 protein interacts, both in yeast two-hybrid system and in vitro, and co-localizes in plant cells with plant BAP-like protein, the orthologue of human protein BAP31.

In yeast two-hybrid system, we identified a number of Nicotiana benthamiana protein interactors of Nt-4/1, the protein known to affect systemic transport of potato spindle tuber viroid. For one of these interactors, an orthologue of human B-cell receptor-associated protein 31 (BAP31) termed plant BAP-like protein (PBL), the ability to interact with Nt-4/1 was studied in greater detail. Analyses of purified proteins expressed in bacterial cells carried out in vitro with the surface plasmon resonance (SPR) spectroscopy revealed that the N. tabacum PBL (NtPBL) was able to interact with Nt-4/1 with high-affinity, and that their complex can form at physiologically relevant concentrations of both proteins. Subcellular localization studies of 4/1-GFP and NtPBL-mRFP transiently co-expressed in plant cells revealed the co-localization of the two fusion proteins in endoplasmic reticulum-associated bodies, suggesting their interaction in vivo. The N-terminal region of the Nt-4/1 protein was found to be required for the specific subcellular targeting of the protein, presumably due to a predicted amphipathic helix mediating association of the Nt-4/1 protein with cell membranes. Additionally, this region was found to contain a trans-activator domain responsible for the Nt-4/1 ability to activate transcription of a reporter gene in yeast.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8

Similar content being viewed by others

Abbreviations

BAP31:

Human B-cell receptor-associated protein 31

PBL:

Plant BAP-like protein

GFP:

Green fluorescent protein

mRFP:

Monomeric red fluorescent protein

SPR:

Surface plasmon resonance

References

  • Breckenridge DG, Stojanovic M, Marcellus RC, Shore GC (2003) Caspase cleavage product of BAP31 induces mitochondrial fission through endoplasmic reticulum calcium signals, enhancing cytochrome c release to the cytosol. J Cell Biol 160:1115–1127

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chichkova NV, Tuzhikov AI, Taliansky M, Vartapetian AB (2012) Plant phytaspases and animal caspases: structurally unrelated death proteases with a common role and specificity. Physiol Plant 145:77–84

    Article  CAS  PubMed  Google Scholar 

  • Chou PY, Fasman GD (1974) Prediction of protein conformation. Biochemistry 13:222–245

    Article  CAS  PubMed  Google Scholar 

  • Cymer F, von Heijne G, White SH (2015) Mechanisms of integral membrane protein insertion and folding. J Mol Biol 427:999–1022

    Article  CAS  PubMed  Google Scholar 

  • Ducret A, Nguyen M, Breckenridge DG, Shore GC (2003) The resident endoplasmic reticulum protein, BAP31, associates with gamma-actin and myosin B heavy chain. Eur J Biochem 270:342–349

    Article  CAS  PubMed  Google Scholar 

  • Ernst WL, Shome K, Wu CC, Gong X, Frizzell RA, Aridor M (2016) VAMP-associated proteins (VAP) as receptors that couple cystic fibrosis transmembrane conductance regulator (CFTR) proteostasis with lipid homeostasis. J Biol Chem 291:5206–5220

    Article  CAS  PubMed  Google Scholar 

  • Formstecher E, Aresta S, Collura V, Hamburger A, Meil A, Trehin A, Reverdy C et al (2005) Protein interaction mapping: a Drosophila case study. Genome Res 15:376–384

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gautier R, Douguet D, Antonny B, Drin G (2008) HELIQUEST: a web server to screen sequences with specific α-helical properties. Bioinformatics 24:2101–2102

    Article  CAS  PubMed  Google Scholar 

  • Grigoriev II, Senin II, Tikhomirova NK, Komolov KE, Permyakov SE, Zernii EY, Koch KW, Philippov PP (2012) Synergetic effect of recoverin and calmodulin on regulation of rhodopsin kinase. Front Mol Neurosci 5:28

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Heath-Engel HM, Wang B, Shore GC (2012) Bcl2 at the endoplasmic reticulum protects against a Bax/Bak-independent paraptosis-like cell death pathway initiated via p20Bap31. Biochim Biophys Acta 1823:335–347

    Article  CAS  PubMed  Google Scholar 

  • Hemsley PA (2015) The importance of lipid modified proteins in plants. New Phytol 205:476–489

    Article  CAS  PubMed  Google Scholar 

  • Kazakov AS, Sokolov AS, Vologzhannikova AA, Permyakova ME, Khorn PA, Ismailov RG, Denessiouk KA, Denesyuk AI, Rastrygina VA, Baksheeva VE, Zernii EY, Zinchenko DV, Glazatov VV, Uversky VN, Mirzabekov TA, Permyakov EA, Permyakov SE (2016) Interleukin-11 binds specific EF-hand proteins via their conserved structural motifs. J Biomol Struct Dyn 8:1–14

    Google Scholar 

  • Kim KM, Adachi T, Nielsen PJ, Terashima M, Lamers MC, Köhler G, Reth M (1994) Two new proteins preferentially associated with membrane immunoglobulin D. EMBO J 13:3793–3800

    CAS  PubMed  PubMed Central  Google Scholar 

  • Kim WT, Seo Choi H, Min Lee H, Jang YJ, Ryu CJ (2014) B-cell receptor-associated protein 31 regulates human embryonic stem cell adhesion, stemness, and survival via control of epithelial cell adhesion molecule. Stem Cells 32:2626–2641

    Article  CAS  PubMed  Google Scholar 

  • Kyte J, Doolittle RF (1982) A simple method for displaying the hydropathic character of a protein. J Mol Biol 157:105–132

    Article  CAS  PubMed  Google Scholar 

  • Lazareva EA, Lezzhov AA, Komarova TV, Morozov SY, Heinlein M, Solovyev AG (2016) A novel block of plant virus movement genes. Mol Plant Pathol. doi:10.1111/mpp.12418

    PubMed  Google Scholar 

  • Lupas A, Van Dyke M, Stock J (1991) Predicting coiled coils from protein sequences. Science 252:1162–1164

    Article  CAS  PubMed  Google Scholar 

  • Makarova SS, Minina EA, Makarov VV, Semenyuk PI, Kopertekh L, Schiemann J, Serebryakova MV, Erokhina TN, Solovyev AG, Morozov SY (2011) Orthologues of a plant-specific At-4/1 gene in the genus Nicotiana and the structural properties of bacterially expressed 4/1 protein. Biochimie 93:1770–1778

    Article  CAS  PubMed  Google Scholar 

  • Makarova SS, Solovyev AG, Morozov SY (2014) RNA-binding properties of the plant protein Nt-4/1. Biochemistry (Mosc) 79:717–726

    Article  CAS  Google Scholar 

  • Minina EA, Erokhina TN, Garushyants SK, Solovyev AG, Morozov SY (2009) Subcellular localization of the new plant protein 4/1 and analysis of heterologous protein-protein interactions indicate its ability for nuclear-cytoplasmic transport. Dokl Biochem Biophys 429:296–300

    Article  CAS  PubMed  Google Scholar 

  • Morozov SY, Makarova SS, Erokhina TN, Kopertekh L, Schiemann J, Owens RA, Solovyev AG (2014) Plant 4/1 protein: potential player in intracellular, cell-to-cell and long-distance signaling. Front Plant Sci 5:26

    Article  PubMed  PubMed Central  Google Scholar 

  • Morozov SY, Milyutina IA, Bobrova VK, Ryazantsev DY, Erokhina TN, Zavriev SK, Agranovsky AA, Solovyev AG, Troitsky AV (2015a) Structural evolution of the 4/1 genes and proteins in non-vascular and lower vascular plants. Biochimie 119:125–136

    Article  CAS  PubMed  Google Scholar 

  • Morozov SY, Solovyev AG, Troitsky AV (2015b) Phylogeny of the plant 4/1 proteins. Data Brief 6:8–11

    Article  PubMed  PubMed Central  Google Scholar 

  • Namba T, Tian F, Chu K, Hwang SY, Yoon KW, Byun S, Hiraki M, Mandinova A, Lee SW (2013) CDIP1-BAP31 complex transduces apoptotic signals from endoplasmic reticulum to mitochondria under endoplasmic reticulum stress. Cell Rep 5:331–339

    Article  CAS  PubMed  Google Scholar 

  • Ng FW, Nguyen M, Kwan T, Branton PE, Nicholson DW, Cromlish JA, Shore GC (1997) p28 Bap31, a Bcl-2/Bcl-XL- and procaspase-8-associated protein in the endoplasmic reticulum. J Cell Biol 139:327–338

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Orgel JP (2006) Surface-active helices in transmembrane proteins. Curr Protein Pept Sci 7:553–560

    Article  CAS  PubMed  Google Scholar 

  • Paape M, Solovyev AG, Erokhina TN, Minina EA, Schepetilnikov MV, Lesemann DE, Schiemann J, Morozov SY, Kellmann JW (2006) At-4/1, an interactor of the Tomato spotted wilt virus movement protein, belongs to a new family of plant proteins capable of directed intra- and intercellular trafficking. Mol Plant Microbe Interact 19:874–883

    Article  CAS  PubMed  Google Scholar 

  • Paquet ME, Cohen-Doyle M, Shore GC, Williams DB (2004) Bap29/31 influences the intracellular traffic of MHC class I molecules. J Immunol 172:7548–7555

    Article  CAS  PubMed  Google Scholar 

  • Piskacek S, Gregor M, Nemethova M, Grabner M, Kovarik P, Piskacek M (2007) Nine-amino-acid transactivation domain: establishment and prediction utilities. Genomics 89:756–768

    Article  CAS  PubMed  Google Scholar 

  • Quistgaard EM, Low C, Moberg P, Guettou F, Maddi K, Nordlund P (2013) Structural and biophysical characterization of the cytoplasmic domains of human BAP29 and BAP31. PLoS One 8:e71111

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Solovyev AG, Makarova SS, Remizowa MV, Lim HS, Hammond J, Owens RA, Kopertekh L, Schiemann J, Morozov SY (2013a) Possible role of the Nt-4/1 protein in macromolecular transport in vascular tissue. Plant Signal Behav 8:e25784

    Article  PubMed Central  Google Scholar 

  • Solovyev AG, Minina EA, Makarova SS, Erokhina TN, Makarov VV, Kaplan IB, Kopertekh L, Schiemann J, Richert-Pöggeler KR, Morozov SY (2013b) Subcellular localization and self-interaction of plant-specific Nt-4/1 protein. Biochimie 95:1360–1370

    Article  CAS  PubMed  Google Scholar 

  • Spiliotis ET, Manley H, Osorio M, Zúñiga MC, Edidin M (2000) Selective export of MHC class I molecules from the ER after their dissociation from TAP. Immunity 13:841–851

    Article  CAS  PubMed  Google Scholar 

  • Stojanovic M, Germain M, Nguyen M, Shore GC (2005) BAP31 and its caspase cleavage product regulate cell surface expression of tetraspanins and integrinmediated cell survival. J Biol Chem 280:30018–30024

    Article  CAS  PubMed  Google Scholar 

  • von Bargen S, Salchert K, Paape M, Piechulla B, Kellmann J-W (2001) Interactions between the tomato spotted wilt virus movement protein and plant proteins showing homologies to myosin, kinesin and DnaJ-like chaperones. Plant Physiol Biochem 39:1083–1093

    Article  Google Scholar 

  • von Heijne G (2007) Formation of transmembrane helices in vivo—is hydrophobicity all that matters? J Gen Physiol 129:353–356

    Article  Google Scholar 

  • Wakana Y, Takai S, Nakajima K, Tani K, Yamamoto A, Watson P, Stephens DJ, Hauri HP, Tagaya M (2008) Bap31 is an itinerant protein that moves between the peripheral endoplasmic reticulum (ER) and a juxtanuclear compartment related to ER-associated degradation. Mol Biol Cell 19:1825–1836

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wang B, Heath-Engel H, Zhang D, Nguyen N, Thomas DY, Hanrahan JW, Shore GC (2008) BAP31 interacts with Sec61 translocons and promotes retrotranslocation of CFTRDeltaF508 via the derlin-1 complex. Cell 133:1080–1092

    Article  CAS  PubMed  Google Scholar 

  • Wilson JD, Barlowe C (2010) Yet1p and Yet3p, the yeast homologs of BAP29 and BAP31, interact with the endoplasmic reticulum translocation apparatus and are required for inositol prototrophy. J Biol Chem 285:18252–18261

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zamyatnin AA Jr, Solovyev AG, Sablina AA, Agranovsky AA, Katul L, Vetten HJ, Schiemann J, Hinkkanen AE, Lehto K, Morozov SY (2002) Dual-colour imaging of membrane protein targeting directed by poa semilatent virus movement protein TGBp3 in plant and mammalian cells. J Gen Virol 83:651–662

    Article  PubMed  Google Scholar 

  • Zen K, Utech M, Liu Y, Soto I, Nusrat A, Parkos CA (2004) Association of BAP31 with CD11b/CD18. Potential role in intracellular trafficking of CD11b/CD18 in neutrophils. J Biol Chem 279:44924–44930

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

We are grateful to Dr. S. S. Makarova for the help with subcellular fractionation experiments. The work of A. Pankratenko, A. Atabekova, E. Lazareva, V. Baksheeva, E. Zernii, A. Solovyev and S. Morozov was performed at Moscow State University with financial support of the Russian Science Foundation (Grant 14-14-00053). The work of O. Zhironkina was performed at Moscow State University with financial support of the Russian Foundation for Basic Research (Grant 15-54-78077). The confocal laser scanning microscopy and surface plasmon resonance facilities in Belozersky Institute were funded by Moscow State University Development Program (PNR 5.13).

Author information

Authors and Affiliations

  1. Department of Virology, Biological Faculty, Moscow State University, Moscow, 119992, Russia

    Anna V. Pankratenko, Anastasia K. Atabekova, Ekaterina A. Lazareva & Sergey Y. Morozov

  2. Belozersky Institute of Physico-Chemical Biology, Moscow State University, Moscow, 119992, Russia

    Viktoriia E. Baksheeva, Oxana A. Zhironkina, Evgeni Yu Zernii, Andrey G. Solovyev & Sergey Y. Morozov

  3. Molecular Plant Pathology Laboratory, USDA-ARS, Beltsville, MD, 20705, USA

    Robert A. Owens

  4. Institute of Molecular Medicine, Sechenov First Moscow State Medical University, Moscow, 119991, Russia

    Andrey G. Solovyev

Authors
  1. Anna V. Pankratenko
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Anastasia K. Atabekova
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Ekaterina A. Lazareva
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Viktoriia E. Baksheeva
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Oxana A. Zhironkina
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Evgeni Yu Zernii
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Robert A. Owens
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Andrey G. Solovyev
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Sergey Y. Morozov
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Sergey Y. Morozov.

Additional information

Robert A. Owens retired from Molecular Plant Pathology Laboratory, USDA-ARS.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Pankratenko, A.V., Atabekova, A.K., Lazareva, E.A. et al. Plant-specific 4/1 polypeptide interacts with an endoplasmic reticulum protein related to human BAP31. Planta 245, 193–205 (2017). https://doi.org/10.1007/s00425-016-2601-8

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00425-016-2601-8

Keywords

Search

Navigation