The tale of tail-anchored proteins: coming from the cytosol and looking for a membrane

doi:10.1083/jcb.200303069

Published 23 June 2003. doi:10.1083/jcb.200303069

This Article

	Full Text
	PDF (Full Text)
	Alert me when this article is cited
	Citation Map

Services

	Email this article
	Similar articles in this journal
	Similar articles in PubMed
	Alert me to new content in the JCB
	Download to citation manager

Citing Articles

	Citing Articles via HighWire
	Citing Articles via CrossRef
	Citing Articles via Google Scholar

Google Scholar

	Articles by Borgese, N.
	Articles by Pedrazzini, E.
	Search for Related Content

PubMed

	PubMed Citation
	Articles by Borgese, N.
	Articles by Pedrazzini, E.


Social Bookmarking

	What's this?

© The Rockefeller University Press, 0021-9525/2003/6/1013 $5.00
The Journal of Cell Biology, Volume 161, Number 6, 1013-1019

Mini-Review

The tale of tail-anchored proteins : coming from the cytosol and looking for a membrane

Nica Borgese¹^,2, Sara Colombo¹ and Emanuela Pedrazzini³

¹ Consiglio Nazionale delle Ricerche Institute for Neuroscience, Cellular and Molecular Pharmacology Section, and Department of Medical Pharmacology, University of Milan, 20129 Milano, Italy
² Faculty of Pharmacy, University of Catanzaro Magna Graecia, 88021 Roccelletta di Borgia (CZ), Italy
³ Consiglio Nazionale delle Ricerche Istituto di Biologia e Biotecnologia Agraria, 20133 Milano, Italy

Address correspondence to Nica Borgese, CNR Institute for Neuroscience, Cellular and Molecular Pharmacology Section, via Vanvitelli 32, 20129 Milano, Italy. Tel.: 3902-50316971. Fax: 3902-7490574. E-mail: n.borgese{at}in.cnr.it

A group of integral membrane proteins, known as C-tail anchored,is defined by the presence of a cytosolic NH₂-terminal domainthat is anchored to the phospholipid bilayer by a single segmentof hydrophobic amino acids close to the COOH terminus. The modeof insertion into membranes of these proteins, many of whichplay key roles in fundamental intracellular processes, is obligatorilyposttranslational, is highly specific, and may be subject toregulatory processes that modulate the protein's function. Althoughrecent work has elucidated structural features in the tail regionthat determine selection of the correct target membrane, themolecular machinery involved in interpreting this information,and in modulating tail-anchored protein localization, has notbeen identified yet.

Key Words: endoplasmic reticulum; membrane traffic; mitochondrial outer membrane; protein targeting and translocation; transmembrane domain

^* Abbreviations used in this paper: MOM, mitochondrial outer membrane;SNARE, soluble N-ethylmaledimide–sensitive factor attachmentprotein receptor; SRP, signal recognition particle; TA, tail-anchored;TMD, transmembrane domain; TOM, translocase of the outer mitochondrialmembrane; UBC6, ubiquitin conjugating enzyme 6.

Add to CiteULike CiteULike Add to Complore Complore Add to Connotea Connotea Add to Del.icio.us Del.icio.us Add to Digg Digg Add to Reddit Reddit Add to Technorati Technorati What's this?

This article has been cited by other articles:

Kemper, C., Habib, S. J., Engl, G., Heckmeyer, P., Dimmer, K. S., Rapaport, D. (2008). Integration of tail-anchored proteins into the mitochondrial outer membrane does not require any known import components. J. Cell Sci. 121: 1990-1998 [Abstract] [Full Text]
Favaloro, V., Spasic, M., Schwappach, B., Dobberstein, B. (2008). Distinct targeting pathways for the membrane insertion of tail-anchored (TA) proteins. J. Cell Sci. 121: 1832-1840 [Abstract] [Full Text]
Corcoran, C. A., He, Q., Ponnusamy, S., Ogretmen, B., Huang, Y., Sheikh, M. S. (2008). Neutral Sphingomyelinase-3 Is a DNA Damage and Nongenotoxic Stress-Regulated Gene That Is Deregulated in Human Malignancies. Mol Cancer Res 6: 795-807 [Abstract] [Full Text]
Rehman, R. U., Stigliano, E., Lycett, G. W., Sticher, L., Sbano, F., Faraco, M., Dalessandro, G., Di Sansebastiano, G.-P. (2008). Tomato Rab11a Characterization Evidenced a Difference Between SYP121-Dependent and SYP122-Dependent exocytosis. Plant Cell Physiol 49: 751-766 [Abstract] [Full Text]
Ronchi, P., Colombo, S., Francolini, M., Borgese, N. (2008). Transmembrane domain-dependent partitioning of membrane proteins within the endoplasmic reticulum. J. Cell Biol. 181: 105-118 [Abstract] [Full Text]
Schepetilnikov, M. V., Solovyev, A. G., Gorshkova, E. N., Schiemann, J., Prokhnevsky, A. I., Dolja, V. V., Morozov, S. Y. (2008). Intracellular Targeting of a Hordeiviral Membrane-Spanning Movement Protein: Sequence Requirements and Involvement of an Unconventional Mechanism. J. Virol. 82: 1284-1293 [Abstract] [Full Text]
Becker, T., Pfannschmidt, S., Guiard, B., Stojanovski, D., Milenkovic, D., Kutik, S., Pfanner, N., Meisinger, C., Wiedemann, N. (2008). Biogenesis of the Mitochondrial TOM Complex: Mim1 PROMOTES INSERTION AND ASSEMBLY OF SIGNAL-ANCHORED RECEPTORS. J. Biol. Chem. 283: 120-127 [Abstract] [Full Text]
Banadyga, L., Gerig, J., Stewart, T., Barry, M. (2007). Fowlpox Virus Encodes a Bcl-2 Homologue That Protects Cells from Apoptotic Death through Interaction with the Proapoptotic Protein Bak. J. Virol. 81: 11032-11045 [Abstract] [Full Text]
Ko, J.-K., Choi, K.-H., Pan, Z., Lin, P., Weisleder, N., Kim, C.-W., Ma, J. (2007). The tail-anchoring domain of Bfl1 and HCCS1 targets mitochondrial membrane permeability to induce apoptosis. J. Cell Sci. 120: 2912-2923 [Abstract] [Full Text]
Abell, B. M., Rabu, C., Leznicki, P., Young, J. C., High, S. (2007). Post-translational integration of tail-anchored proteins is facilitated by defined molecular chaperones. J. Cell Sci. 120: 1743-1751 [Abstract] [Full Text]
Moise, A. R., Golczak, M., Imanishi, Y., Palczewski, K. (2007). Topology and Membrane Association of Lecithin: Retinol Acyltransferase. J. Biol. Chem. 282: 2081-2090 [Abstract] [Full Text]
Brambillasca, S., Yabal, M., Makarow, M., Borgese, N. (2006). Unassisted translocation of large polypeptide domains across phospholipid bilayers. J. Cell Biol. 175: 767-777 [Abstract] [Full Text]
Foresti, O., daSilva, L. L.P., Denecke, J. (2006). Overexpression of the Arabidopsis Syntaxin PEP12/SYP21 Inhibits Transport from the Prevacuolar Compartment to the Lytic Vacuole in Vivo. Plant Cell 18: 2275-2293 [Abstract] [Full Text]
Halbach, A., Landgraf, C., Lorenzen, S., Rosenkranz, K., Volkmer-Engert, R., Erdmann, R., Rottensteiner, H. (2006). Targeting of the tail-anchored peroxisomal membrane proteins PEX26 and PEX15 occurs through C-terminal PEX19-binding sites. J. Cell Sci. 119: 2508-2517 [Abstract] [Full Text]
Yang, X., Xu, P., Xiao, Y., Xiong, X., Xu, T. (2006). Domain Requirement for the Membrane Trafficking and Targeting of Syntaxin 1A. J. Biol. Chem. 281: 15457-15463 [Abstract] [Full Text]
Krut, O., Wiegmann, K., Kashkar, H., Yazdanpanah, B., Kronke, M. (2006). Novel Tumor Necrosis Factor-responsive Mammalian Neutral Sphingomyelinase-3 Is a C-tail-anchored Protein. J. Biol. Chem. 281: 13784-13793 [Abstract] [Full Text]
Ceppi, P., Colombo, S., Francolini, M., Raimondo, F., Borgese, N., Masserini, M. (2005). Two tail-anchored protein variants, differing in transmembrane domain length and intracellular sorting, interact differently with lipids. Proc. Natl. Acad. Sci. USA 102: 16269-16274 [Abstract] [Full Text]
Brock, S. C., Heck, J. M., McGraw, P. A., Crowe, J. E. Jr. (2005). The Transmembrane Domain of the Respiratory Syncytial Virus F Protein Is an Orientation-Independent Apical Plasma Membrane Sorting Sequence. J. Virol. 79: 12528-12535 [Abstract] [Full Text]
Patton, S. M., Pinero, D. J., Surguladze, N., Beard, J., Connor, J. R. (2005). Subcellular localization of iron regulatory proteins to Golgi and ER membranes. J. Cell Sci. 118: 4365-4373 [Abstract] [Full Text]
Fetzer, C., Tews, B. A., Meyers, G. (2005). The Carboxy-Terminal Sequence of the Pestivirus Glycoprotein Erns Represents an Unusual Type of Membrane Anchor. J. Virol. 79: 11901-11913 [Abstract] [Full Text]
Vitale, A., Pedrazzini, E. (2005). Recombinant Pharmaceuticals from Plants: The Plant Endomembrane System as Bioreactor. Mol. Interv. 5: 216-225 [Abstract] [Full Text]
van Herpen, R. E. M. A., Oude Ophuis, R. J. A., Wijers, M., Bennink, M. B., van de Loo, F. A. J., Fransen, J., Wieringa, B., Wansink, D. G. (2005). Divergent Mitochondrial and Endoplasmic Reticulum Association of DMPK Splice Isoforms Depends on Unique Sequence Arrangements in Tail Anchors. Mol. Cell. Biol. 25: 1402-1414 [Abstract] [Full Text]
Stewart, T. L., Wasilenko, S. T., Barry, M. (2005). Vaccinia Virus F1L Protein Is a Tail-Anchored Protein That Functions at the Mitochondria To Inhibit Apoptosis. J. Virol. 79: 1084-1098 [Abstract] [Full Text]
Ahting, U., Waizenegger, T., Neupert, W., Rapaport, D. (2005). Signal-anchored Proteins Follow a Unique Insertion Pathway into the Outer Membrane of Mitochondria. J. Biol. Chem. 280: 48-53 [Abstract] [Full Text]
Moradpour, D., Brass, V., Bieck, E., Friebe, P., Gosert, R., Blum, H. E., Bartenschlager, R., Penin, F., Lohmann, V. (2004). Membrane Association of the RNA-Dependent RNA Polymerase Is Essential for Hepatitis C Virus RNA Replication. J. Virol. 78: 13278-13284 [Abstract] [Full Text]
Hwang, Y. T., Pelitire, S. M., Henderson, M. P.A., Andrews, D. W., Dyer, J. M., Mullen, R. T. (2004). Novel Targeting Signals Mediate the Sorting of Different Isoforms of the Tail-Anchored Membrane Protein Cytochrome b5 to Either Endoplasmic Reticulum or Mitochondria. Plant Cell 16: 3002-3019 [Abstract] [Full Text]
Frederick, R. L., McCaffery, J. M., Cunningham, K. W., Okamoto, K., Shaw, J. M. (2004). Yeast Miro GTPase, Gem1p, regulates mitochondrial morphology via a novel pathway. J. Cell Biol. 167: 87-98 [Abstract] [Full Text]
Davidson, C. E., Reese, B. E., Billingsley, M. L., Yun, J. K. (2004). Stannin, A Protein That Localizes to the Mitochondria and Sensitizes NIH-3T3 Cells to Trimethyltin and Dimethyltin Toxicity. Mol. Pharmacol. 66: 855-863 [Abstract] [Full Text]
Schwer, B., Ren, S., Pietschmann, T., Kartenbeck, J., Kaehlcke, K., Bartenschlager, R., Yen, T. S. B., Ott, M. (2004). Targeting of Hepatitis C Virus Core Protein to Mitochondria through a Novel C-Terminal Localization Motif. J. Virol. 78: 7958-7968 [Abstract] [Full Text]
Papini, N., Anastasia, L., Tringali, C., Croci, G., Bresciani, R., Yamaguchi, K., Miyagi, T., Preti, A., Prinetti, A., Prioni, S., Sonnino, S., Tettamanti, G., Venerando, B., Monti, E. (2004). The Plasma Membrane-associated Sialidase MmNEU3 Modifies the Ganglioside Pattern of Adjacent Cells Supporting Its Involvement in Cell-to-Cell Interactions. J. Biol. Chem. 279: 16989-16995 [Abstract] [Full Text]
Moise, A. R., Grant, J. R., Lippe, R., Gabathuler, R., Jefferies, W. A. (2004). The Adenovirus E3-6.7K Protein Adopts Diverse Membrane Topologies following Posttranslational Translocation. J. Virol. 78: 454-463 [Abstract] [Full Text]
Wilson-Annan, J., O'Reilly, L. A., Crawford, S. A., Hausmann, G., Beaumont, J. G., Parma, L. P., Chen, L., Lackmann, M., Lithgow, T., Hinds, M. G., Day, C. L., Adams, J. M., Huang, D. C.S. (2003). Proapoptotic BH3-only proteins trigger membrane integration of prosurvival Bcl-w and neutralize its activity. J. Cell Biol. 162: 877-888 [Abstract] [Full Text]