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Identification and characterization of AtCASP, a plant transmembrane Golgi matrix protein

Plant Molecular Biology volume 58, pages 109–122 (2005)Cite this article

Abstract

Golgins are a family of coiled-coil proteins that are associated with the Golgi apparatus. They are necessary for tethering events in membrane fusion and may act as structural support for Golgi cisternae. Here we report on the identification of an Arabidopsis golgin which is a homologue of CASP, a known transmembrane mammalian and yeast golgin. Similar to its homologues, the plant CASP contains a long N-terminal coiled-coil region protruding into the cytosol and a C-terminal transmembrane domain with amino acid residues which are highly conserved across species. Through fluorescent protein tagging experiments, we show that plant CASP localizes at the plant Golgi apparatus and that the C-terminus of this protein is sufficient for its localization, as has been shown for its mammalian counterpart. In addition, we demonstrate that the plant CASP is able to localize at the mammalian Golgi apparatus. However, mutagenesis of a conserved tyrosine in the transmembrane domain revealed that it is necessary for ER export and Golgi localization of the Arabidopsis CASP in mammalian cells, but is not required for its correct localization in plant cells. These data suggest that mammalian and plant cells have different mechanisms for concentrating CASP in the Golgi apparatus.

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References

  • C. Alvarez R. Garcia-Mata H.P. Hauri E. Sztul (2001) ArticleTitleThe p115-interactive proteins GM130 and giantin participate in endoplasmic reticulum-Golgi traffic J. Biol. Chem 276 IssueID4 2693–2700

    Google Scholar 

  • F.A. Barr (1999) ArticleTitleA novel Rab6-interacting domain defines a family of Golgi-targeted coiled-coil proteins Curr. Biol 9 IssueID7 381–384

    Google Scholar 

  • F.A. Barr N. Nakamura G. Warren (1998) ArticleTitleMapping the interaction between GRASP65 and GM130, components of a protein complex involved in the stacking of Golgi cisternae EMBO J 17 IssueID12 3258–3268

    Google Scholar 

  • F.A. Barr B. Short (2003) ArticleTitleGolgins in the structure and dynamics of the Golgi apparatus Curr. Opin. Cell Biol 15 IssueID4 405–413

    Google Scholar 

  • R.A. Bascom S. Srinivasan R.L. Nussbaum (1999) ArticleTitleIdentification and characterization of golgin-84, a novel Golgi integral membrane protein with a cytoplasmic coiled-coil domain J. Biol. Chem 274 IssueID5 2953–2962

    Google Scholar 

  • H. Batoko H.Q. Zheng C. Hawes I. Moore (2000) ArticleTitleA Rab1 GTPase is required for transport between the endoplasmic reticulum and Golgi apparatus and for normal Golgi movement in plants Plant Cell 12 IssueID11 2201–2218

    Google Scholar 

  • B. Berger D.B. Wilson E. Wolf T. Tonchev M. Milla P.S. Kim (1995) ArticleTitlePredicting coiled coils by use of pairwise residue correlations Proc. Natl. Acad. Sci. USA 92 IssueID18 8259–8263

    Google Scholar 

  • P. Boevink K. Oparka S. Santa Cruz B. Martin A. Betteridge C. Hawes (1998) ArticleTitleStacks on tracks: the plant Golgi apparatus traffics on an actin/ER network Plant J 15 IssueID3 441–447

    Google Scholar 

  • S. Bolte S. Brown B. Satiat-Jeunemaitre (2004) ArticleTitleThe N-myristoylated Rab-GTPase m-Rabmc is involved in post-Golgi trafficking events to the lytic vacuole in plant cells J. Cell Sci 117 IssueID6 943–954

    Google Scholar 

  • F. Brandizzi E.L. Snapp A.G. Roberts J. Lippincott- Schwartz C. Hawes (2002a) ArticleTitleMembrane protein transport between the endoplasmic reticulum and the Golgi in tobacco leaves is energy dependent but cytoskeleton independent: evidence from selective photobleaching Plant Cell 14 IssueID6 1293–1309

    Google Scholar 

  • F. Brandizzi N. Frangne S. Marc-Martin C. Hawes J.M. Neuhaus N. Paris (2002b) ArticleTitleIn plants the destination for single pass membrane proteins is markedly influenced by the length of the hydrophobic domain Plant Cell 14 IssueID5 1077–1092

    Google Scholar 

  • X. Cao N. Ballew C. Barlowe (1998) ArticleTitleInitial docking of ER-derived vesicles requires Uso1p and Ypt1p but is independent of SNARE proteins EMBO J 17 IssueID8 2156–2165

    Google Scholar 

  • C.A. Chen H. Okayama (1988) ArticleTitleCalcium phosphate-mediated gene transfer: a highly efficient transfection system for stably transforming cells with plasmid DNA Biotechniques 6 IssueID7 632–638

    Google Scholar 

  • I. Contreras Y. Yang D.G. Robinson F. Aniento (2004) ArticleTitleSorting Signals in the Cytosolic Tail of Plant p24 Proteins Involved in the Interaction with the COPII Coat Plant Cell Physiol 45 IssueID12 1779–1786

    Google Scholar 

  • A.J. Crofts N. Leborgne-Castel S. Hillmer D.G. Robinson B. Phillipson L.E. Carlsson D.A. Ashford J. Denecke (1999) ArticleTitleSaturation of the endoplasmic reticulum retention machinery reveals anterograde bulk flow Plant Cell 11 IssueID11 2233–2248

    Google Scholar 

  • L.L. daSilva E.L. Snapp J. Denecke J. Lippincott-Schwartz C. Hawes F. Brandizzi (2004) ArticleTitleER export sites and Golgi bodies behave as single mobile secretory units in plant cells Plant Cell 16 IssueID7 1753–1771

    Google Scholar 

  • L.L. daSilva J.P. Taylor J.L. Hadlington S.L. Hanton C.J. Snowden S.J. Fox O. Foresti F. Brandizzi J. Denecke (2005) ArticleTitleReceptor salvage from the prevacuolar compartment is essential for efficient vacuolar protein targeting Plant Cell 17 IssueID1 132–148

    Google Scholar 

  • J. Denecke R. Rycke ParticleDe J. Botterman (1992) ArticleTitlePlant and mammalian sorting signals for protein retention in the endoplasmic reticulum contain a conserved epitope EMBO J 11 IssueID6 2345–2355

    Google Scholar 

  • J.G. Dohlman A. Lupas M. Carson (1993) ArticleTitleLong charge-rich alpha-helices in systemic autoantigens Biochem. Biophys. Res. Commun 195 IssueID2 686–696

    Google Scholar 

  • J.E. Drew D. Bown J.A. Gatehouse (1993) ArticleTitleSequence of a novel plant ras-related cDNA from Pisum sativum Plant Mol. Biol 21 IssueID6 1195–1199

    Google Scholar 

  • Y. Fridmann-Sirkis S. Siniossoglou H.R. Pelham (2004) ArticleTitleTMF is a golgin that binds Rab6 and influences Golgi morphology BMC Cell Biol 5 IssueID1 18

    Google Scholar 

  • A.K. Gillingham A.C. Pfeifer S. Munro (2002) ArticleTitleCASP, the alternatively spliced product of the gene encoding the CCAAT-displacement protein transcription factor, is a Golgi membrane protein related to giantin Mol. Biol. Cell 13 IssueID11 3761–3774

    Google Scholar 

  • A.K. Gillingham S. Munro (2003) ArticleTitleLong coiled-coil proteins and membrane traffic Biochim. Biophys. Acta 1641 IssueID2–3 71–85

    Google Scholar 

  • P.R. Gilson C.E. Vergara L. Kjer-Nielsen R.D. Teasdale A. Bacic P.A. Gleeson (2004) ArticleTitleIdentification of a Golgi-localised GRIP domain protein from Arabidopsis thaliana Planta 219 IssueID6 1050–1056

    Google Scholar 

  • M. Grebe J. Xu W. Mobius T. Ueda A. Nakano H.J. Geuze M.B. Rook B. Scheres (2003) ArticleTitleArabidopsis sterol endocytosis involves actin-mediated trafficking via ARA6-positive early endosomes Curr. Biol 13 IssueID16 1378–1387

    Google Scholar 

  • J. Haseloff K.R. Siemering D.C. Prasher S. Hodge (1997) ArticleTitleRemoval of a cryptic intron and subcellular localization of green fluorescent protein are required to mark transgenic Arabidopsis plants brightly Proc Natl Acad Sci USA 94 IssueID6 2122–2127

    Google Scholar 

  • T. Inaba Y. Nagano T. Nagasaki Y. Sasaki (2002) ArticleTitleDistinct localization of two closely related Ypt3/Rab11 proteins on the trafficking pathway in higher plants J. Biol. Chem 277 IssueID11 9183–9188

    Google Scholar 

  • A. Jakymiw E. Raharjo J.B. Rattner T. Eystathioy E.K. Chan D.J. Fujita (2000) ArticleTitleIdentification and characterization of a novel Golgi protein, golgin-67 J. Biol. Chem 275 IssueID6 4137–4144

    Google Scholar 

  • G Jürgens (2004) ArticleTitleMembrane trafficking in plants Annu. Rev. Cell Dev. Biol 20 481–504

    Google Scholar 

  • L. Kjer-Nielsen R.D. Teasdale C. Vliet Particlevan P.A. Gleeson (1999) ArticleTitleA novel Golgi-localisation domain shared by a class of coiled-coil peripheral membrane proteins Curr. Biol 9 IssueID7 385–388

    Google Scholar 

  • A.M. Kotzer F. Brandizzi U. Neumann N. Paris I. Moore C. Hawes (2004) ArticleTitleAtRabF2b (Ara7) acts on the vacuolar trafficking pathway in tobacco leaf epidermal cells J. Cell Sci 117 IssueID26 6377–6389

    Google Scholar 

  • A. Krogh B. Larsson G. Heijne Particlevon E.L Sonnhammer (2001) ArticleTitlePredicting transmembrane protein topology with a hidden Markov model: application to complete genomes J. Mol. Biol 305 IssueID3 567–580

    Google Scholar 

  • G.M. Lesa J. Seemann J. Shorter J. Vandekerckhove G. Warren (2000) ArticleTitleThe amino-terminal domain of the golgi protein giantin interacts directly with the vesicle-tethering protein p115 J. Biol. Chem 275 IssueID4 2831–2836

    Google Scholar 

  • A.D. Linstedt H.P. Hauri (1993) ArticleTitleGiantin, a novel conserved Golgi membrane protein containing a cytoplasmic domain of at least 350 kDa Mol. Biol. Cell 4 IssueID7 679–693

    Google Scholar 

  • R. Lu V. Misra (2000) ArticleTitlePotential role for luman, the cellular homologue of herpes simplex virus VP16 (alpha gene trans-inducing factor), in herpesvirus latency J. Virol 74 IssueID2 934–943

    Google Scholar 

  • M. Mansour S.Y. Lee B Pohajdak (2002) ArticleTitleThe N-terminal coiled coil domain of the cytohesin/ARNO family of guanine nucleotide exchange factors interacts with the scaffolding protein CASP J. Biol. Chem 277 IssueID35 32302–32309

    Google Scholar 

  • Y. Misumi M. Sohda A. Tashiro H. Sato Y. Ikehara (2001) ArticleTitleAn essential cytoplasmic domain for the Golgi localization of coiled-coil proteins with a COOH-terminal membrane anchor J. Biol. Chem 276 IssueID9 6867–6873

    Google Scholar 

  • B.D. Moyer B.B. Allan W.E. Balch (2001) ArticleTitleRab1 interaction with a GM130 effector complex regulates COPII vesicle cis-Golgi tethering Traffic 2 IssueID4 268–276

    Google Scholar 

  • S. Munro (1995) ArticleTitleAn investigation into the role of trans-membrane domains in Golgi protein retention EMBO J 14 IssueID19 4695–4704

    Google Scholar 

  • S. Munro B.J. Nichols (1999) ArticleTitleThe GRIP domain -- a novel Golgi-targeting domain found in several coiled-coil proteins Curr. Biol 9 IssueID7 377–380

    Google Scholar 

  • M.Y. Nahm S.W. Kim D. Yun S.Y. Lee M.J. Cho J.D. Bahk (2003) ArticleTitleMolecular and biochemical analyses of OsRab7, a rice Rab7 homolog Plant Cell Physiol 44 IssueID12 1341–1349

    Google Scholar 

  • A. Nebenführ L.A. Gallagher T.G. Dunahay J.A. Frohlick A.M. Mazurkiewicz J.B. Meehl L.A. Staehelin (1999) ArticleTitleStop-and-go movements of plant Golgi stacks are mediated by the acto-myosin system Plant Physiol 121 IssueID4 1127–1142

    Google Scholar 

  • U. Neumann F. Brandizzi C. Hawes (2003) ArticleTitleProtein transport in plant cells: in and out of the Golgi Ann. Bot 92 IssueID2 167–180

    Google Scholar 

  • G. Palade (1975) ArticleTitleIntracellular aspects of the process of protein synthesis Science 189 IssueID4200 347–358

    Google Scholar 

  • B.A. Phillipson P. Pimpl L.L. daSilva A.J. Crofts J.P. Taylor A. Movafeghi D.G. Robinson J. Denecke (2001) ArticleTitleSecretory bulk flow of soluble proteins is efficient and COPII dependent Plant Cell 13 IssueID9 2005–2020

    Google Scholar 

  • P. Pimpl A. Movafeghi S. Coughlan J. Denecke S. Hillmer D.G. Robinson (2000) ArticleTitleIn situ localization and in vitro induction of plant COPI-coated vesicles Plant Cell 12 IssueID11 2219–2236

    Google Scholar 

  • M.L. Preuss J. Serna T.G. Falbel S.Y. Bednarek E. Nielsen (2004) ArticleTitleThe Arabidopsis Rab GTPase RabA4b localizes to the tips of growing root hair cells Plant Cell 16 IssueID6 1589–1603

    Google Scholar 

  • M.A. Puthenveedu A.D. Linstedt (2001) ArticleTitleEvidence that Golgi structure depends on a p115 activity that is independent of the vesicle tether components giantin and GM130 J Cell Biol 155 IssueID2 227–238

    Google Scholar 

  • A. Rose S. Manikantan S.J. Schraegle M.A. Maloy E.A. Stahlberg I. Meier (2004) ArticleTitleGenome-wide identification of Arabidopsis coiled-coil proteins and establishment of the ARABI-COIL database Plant Physiol 134 IssueID3 927–939

    Google Scholar 

  • S. Rutherford I. Moore (2002) ArticleTitleThe Arabidopsis Rab GTPase family: another enigma variation Curr. Opin. Plant. Biol 5 IssueID6 518–528

    Google Scholar 

  • C.M. Saint-Jore J. Evins H. Batoko F. Brandizzi I. Moore C. Hawes (2002) ArticleTitleRedistribution of membrane proteins between the Golgi apparatus and endoplasmic reticulum in plants is reversible and not dependent on cytoskeletal networks Plant J 29 IssueID5 661–678

    Google Scholar 

  • J. Sambrook E.F. Fritsch T. Maniatis (1989) Molecular Cloning: a laboratory manual Cold Spring Harbour Laboratory Press USA

    Google Scholar 

  • A.A. Sanderfoot V. Kovaleva D.C. Bassham N.V. Raikhel (2001) ArticleTitleInteractions between syntaxins identify at least five SNARE complexes within the Golgi/prevacuolar system of the Arabidopsis cell Mol. Biol. Cell 12 IssueID12 3733–3743

    Google Scholar 

  • J. Seemann E.J. Jokitalo G. Warren (2000) ArticleTitleThe role of the tethering proteins p115 and GM130 in transport through the Golgi apparatus in vivo Mol. Biol. Cell 11 IssueID2 635–645

    Google Scholar 

  • C.E. Shamu (1997) ArticleTitleSplicing together the unfolded-protein response Curr. Biol 7 IssueID2 R67–70

    Google Scholar 

  • B. Short C. Preisinger R. Korner R. Kopajtich O. Byron F.A. Barr (2001) ArticleTitleA GRASP55-rab2 effector complex linking Golgi structure to membrane traffic J. Cell Biol 155 877–883

    Google Scholar 

  • J. Shorter G. Warren (1999) ArticleTitleA role for the vesicle tethering protein, p115, in the post-mitotic stacking of reassembling Golgi cisternae in a cell-free system J. Cell Biol 146 57–70

    Google Scholar 

  • P. Slusarewicz T. Nilsson N. Hui R. Watson G. Warren (1994) ArticleTitleIsolation of a matrix that binds medial Golgi enzymes J. Cell Biol 124 IssueID4 405–413

    Google Scholar 

  • B. Sonnichsen M. Lowe T. Levine E. Jamsa B. Dirac-Svejstrup G. Warren (1998) ArticleTitleA role for giantin in docking COPI vesicles to Golgi membranes J. Cell Biol 140 IssueID5 1013–1021

    Google Scholar 

  • L.A. Staehelin I. Moore (1995) ArticleTitleThe plant Golgi apparatus: structure, functional organization and trafficking mechanisms Annu. Rev. Plant Phys. Plant Mol. Biol 46 261–288

    Google Scholar 

  • B.L. Tang S.H. Wong X.L. Qi S.H. Low W. Hong (1993) ArticleTitleMolecular cloning, characterization, subcellular localization and dynamics of p23, the mammalian KDEL receptor J. Cell Biol 120 IssueID2 325–328

    Google Scholar 

  • T. Ueda T. Anai H. Tsukaya A. Hirata H. Uchimiya (1996) ArticleTitleCharacterization and subcellular localization of a small GTP-binding protein (Ara-4) from Arabidopsis: conditional expression under control of the promoter of the gene for heat-shock protein HSP81y1 Mol. Gen. Genet 250 IssueID5 533–539

    Google Scholar 

  • T. Ueda N. Matsuda H. Uchimiya A. Nakano (2000) ArticleTitleModes of interaction between the Arabidopsis Rab protein, Ara4, and its putative regulator molecules revealed by a yeast expression system Plant J 21 IssueID4 341–349

    Google Scholar 

  • T. Ueda M. Yamaguchi H. Uchimiya A. Nakano (2001) ArticleTitleAra6, a plant-unique novel type Rab GTPase, functions in the endocytic pathway of Arabidopsis thaliana Embo J 20 IssueID17 4730–4741

    Google Scholar 

  • R. Valsdottir H. Hashimoto K. Ashman T. Koda B. Storrie T. Nilsson (2001) ArticleTitleIdentification of rabaptin-5, rabex-5, and GM130 as putative effectors of rab33b, a regulator of retrograde traffic between the Golgi apparatus and ER FEBS Lett 508 IssueID2 201–209

    Google Scholar 

  • A. Volchuk M. Ravazzola A. Perrelet W.S. Eng M. Di Liberto O. Varlamov M. Fukasawa T. Engel T.H. Sollner J.E. Rothman L. Orci (2004) ArticleTitleCountercurrent distribution of two distinct SNARE complexes mediating transport within the Golgi stack Mol. Biol. Cell 15 IssueID4 1506–1518

    Google Scholar 

  • T.H. Ward F. Brandizzi (2004) ArticleTitleDynamics of proteins in Golgi membranes: comparisons between mammalian and plant cells highlighted by photobleaching techniques Cell Mol. Life Sci 61 IssueID2 172–185

    Google Scholar 

  • K. Yuasa K. Toyooka H. Fukuda K. Matsuoka (2005) ArticleTitleMembrane-anchored prolyl hydroxylase with an export signal from the endoplasmic reticulum Plant J 41 81–94

    Google Scholar 

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Authors and Affiliations

  1. Department of Biology, University of Saskatchewan, 112 Science Place, Saskatoon, SK, S7N 5E2, Canada

    Luciana Renna, Sally L. Hanton, Giovanni Stefano, Lauren Bortolotti & Federica Brandizzi

  2. Department of Veterinary Sciences, University of Saskatchewan, 52 Campus Drive, Saskatoon, SK, S7N 5B, Canada

    Vikram Misra

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  1. Luciana Renna
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  2. Sally L. Hanton
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  3. Giovanni Stefano
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  4. Lauren Bortolotti
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  5. Vikram Misra
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  6. Federica Brandizzi
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Correspondence to Federica Brandizzi.

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†These authors have contributed equally to the work

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Renna, L., Hanton, S.L., Stefano, G. et al. Identification and characterization of AtCASP, a plant transmembrane Golgi matrix protein. Plant Mol Biol 58, 109–122 (2005). https://doi.org/10.1007/s11103-005-4618-4

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  • DOI: https://doi.org/10.1007/s11103-005-4618-4

Keywords

  • CASP
  • membrane Golgi matrix proteins
  • plants