Recognition of dileucine-based sorting signals from HIV-1 Nef and LIMP-II by the AP-1 {gamma}-{sigma}1 and AP-3 {delta}-{sigma}3 hemicomplexes

doi:10.1083/jcb.200307157

Published 22 December 2003. doi:10.1083/jcb.200307157

This Article

	Full Text
	Full Text (PDF, 433K)
	PPT slides of all figures
	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 Janvier, K.
	Articles by Bonifacino, J. S.
	Search for Related Content

PubMed

	PubMed Citation
	Articles by Janvier, K.
	Articles by Bonifacino, J. S.


Social Bookmarking

	What's this?

© The Rockefeller University Press, 0021-9525/2003/12/1281 $8.00
The Journal of Cell Biology, Volume 163, Number 6, 1281-1290

Article

Recognition of dileucine-based sorting signals from HIV-1 Nef and LIMP-II by the AP-1 ${gamma}$ – ${sigma}$ 1 and AP-3 ${delta}$ – ${sigma}$ 3 hemicomplexes

Katy Janvier¹, Yukio Kato¹, Markus Boehm¹, Jeremy R. Rose², José A. Martina¹, Bong-Yoon Kim¹, Sundararajan Venkatesan² and Juan S. Bonifacino¹

¹ Cell Biology and Metabolism Branch, National Institute of Child Health and Human Development
² Laboratory of Molecular Microbiology, National Institute of Allergy and Infectious Diseases, National Institutes of Health, Bethesda, MD 20892

Address correspondence to Juan S. Bonifacino, Cell Biology and Metabolism Branch, National Institute of Child Health and Human Development, National Institutes of Health, Building 18T, Rm. 101, Bethesda, MD 20892. Tel.: (301) 496-6368. Fax: (301) 402-0078. email: juan{at}helix.nih.gov

The sorting of transmembrane proteins to endosomes and lysosomesis mediated by signals present in the cytosolic tails of theproteins. A subset of these signals conform to the [DE]XXXL[LI]consensus motif and mediate sorting via interactions with heterotetramericadaptor protein (AP) complexes. However, the identity of theAP subunits that recognize these signals remains controversial.We have used a yeast three-hybrid assay to demonstrate that[DE]XXXL[LI]-type signals from the human immunodeficiency virusnegative factor protein and the lysosomal integral membraneprotein II interact with combinations of the ${gamma}$ and ${sigma}$ 1 subunitsof AP-1 and the ${delta}$ and ${sigma}$ 3 subunits of AP-3, but not the analogouscombinations of AP-2 and AP-4 subunits. The sequence requirementsfor these interactions are similar to those for binding to thewhole AP complexes in vitro and for function of the signalsin vivo. These observations reveal a novel mode of recognitionof sorting signals involving the ${gamma}$ / ${delta}$ and ${sigma}$ subunits of AP-1 andAP-3.

Key Words: clathrin; adaptors; coats; endocytosis; endosomes

Y. Kato's present address is Faculty of Pharmaceutical Sciences,Kanazawa University, 13-1 Takara-machi, Kanazawa, 920-0934,Japan.

M. Boehm's present address is ALTANA Pharma AG, Byk-Gulden-Strasse2, 78467 Konstanz, Germany.

Abbreviations used in this paper: 3AT, 3-aminotriazole; AP,adaptor protein; CD-MPR, cation-dependent MPR; CI-MPR, cation-independentMPR; GAL4AD, GAL4, transcription activation domain; GAL4BD,GAL4 DNA binding domain; GGAs, Golgi-localized, ${gamma}$ -ear–containing,Arf-binding proteins; HIV, human immunodeficiency virus; LIMP-II,lysosomal integral membrane protein II; MPR, mannose 6-phosphatereceptor; Nef, negative factor; SIV, simian immunodeficiencyvirus; VHS, Vps27, Hrs, and Stam.

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

This article has been cited by other articles:

Tazeh, N. N., Silverman, J. S., Schwartz, K. J., Sevova, E. S., Sutterwala, S. S., Bangs, J. D. (2009). Role of AP-1 in Developmentally Regulated Lysosomal Trafficking in Trypanosoma brucei. Eukaryot Cell 8: 1352-1361 [Abstract] [Full Text]
Ma, Y., Takeuchi, M., Sugiura, R., Sio, S. O., Kuno, T. (2009). Deletion mutants of AP-1 adaptin subunits display distinct phenotypes in fission yeast. GENES CELLS 14: 1015-1028 [Abstract] [Full Text]
Subramanya, A. R., Liu, J., Ellison, D. H., Wade, J. B., Welling, P. A. (2009). WNK4 Diverts the Thiazide-sensitive NaCl Cotransporter to the Lysosome and Stimulates AP-3 Interaction. J. Biol. Chem. 284: 18471-18480 [Abstract] [Full Text]
daSilva, L. L. P., Sougrat, R., Burgos, P. V., Janvier, K., Mattera, R., Bonifacino, J. S. (2009). Human Immunodeficiency Virus Type 1 Nef Protein Targets CD4 to the Multivesicular Body Pathway. J. Virol. 83: 6578-6590 [Abstract] [Full Text]
Chaudhuri, R., Mattera, R., Lindwasser, O. W., Robinson, M. S., Bonifacino, J. S. (2009). A Basic Patch on {alpha}-Adaptin Is Required for Binding of Human Immunodeficiency Virus Type 1 Nef and Cooperative Assembly of a CD4-Nef-AP-2 Complex. J. Virol. 83: 2518-2530 [Abstract] [Full Text]
Sitaram, A., Piccirillo, R., Palmisano, I., Harper, D. C., Dell'Angelica, E. C., Schiaffino, M. V., Marks, M. S. (2009). Localization to Mature Melanosomes by Virtue of Cytoplasmic Dileucine Motifs Is Required for Human OCA2 Function. Mol. Biol. Cell 20: 1464-1477 [Abstract] [Full Text]
Laguette, N., Benichou, S., Basmaciogullari, S. (2009). Human Immunodeficiency Virus Type 1 Nef Incorporation into Virions Does Not Increase Infectivity. J. Virol. 83: 1093-1104 [Abstract] [Full Text]
Keyel, P. A., Thieman, J. R., Roth, R., Erkan, E., Everett, E. T., Watkins, S. C., Heuser, J. E., Traub, L. M. (2008). The AP-2 Adaptor {beta}2 Appendage Scaffolds Alternate Cargo Endocytosis. Mol. Biol. Cell 19: 5309-5326 [Abstract] [Full Text]
Mitchell, R. S., Chaudhuri, R., Lindwasser, O. W., Tanaka, K. A., Lau, D., Murillo, R., Bonifacino, J. S., Guatelli, J. C. (2008). Competition Model for Upregulation of the Major Histocompatibility Complex Class II-Associated Invariant Chain by Human Immunodeficiency Virus Type 1 Nef. J. Virol. 82: 7758-7767 [Abstract] [Full Text]
Vince, J. E., Tull, D. L., Spurck, T., Derby, M. C., McFadden, G. I., Gleeson, P. A., Gokool, S., McConville, M. J. (2008). Leishmania Adaptor Protein-1 Subunits Are Required for Normal Lysosome Traffic, Flagellum Biogenesis, Lipid Homeostasis, and Adaptation to Temperatures Encountered in the Mammalian Host. Eukaryot Cell 7: 1256-1267 [Abstract] [Full Text]
Jin, Y.-J., Cai, C. Y., Zhang, X., Burakoff, S. J. (2008). Lysine 144, a Ubiquitin Attachment Site in HIV-1 Nef, Is Required for Nef-Mediated CD4 Down-Regulation. J. Immunol. 180: 7878-7886 [Abstract] [Full Text]
Styers, M. L., O'Connor, A. K., Grabski, R., Cormet-Boyaka, E., Sztul, E. (2008). Depletion of {beta}-COP reveals a role for COP-I in compartmentalization of secretory compartments and in biosynthetic transport of caveolin-1. Am. J. Physiol. Cell Physiol. 294: C1485-C1498 [Abstract] [Full Text]
Mishra, S. K., Jha, A., Steinhauser, A. L., Kokoza, V. A., Washabaugh, C. H., Raikhel, A. S., Foster, W. A., Traub, L. M. (2008). Internalization of LDL-receptor superfamily yolk-protein receptors during mosquito oogenesis involves transcriptional regulation of PTB-domain adaptors. J. Cell Sci. 121: 1264-1274 [Abstract] [Full Text]
Craige, B., Salazar, G., Faundez, V. (2008). Phosphatidylinositol-4-Kinase Type II Alpha Contains an AP-3-sorting Motif and a Kinase Domain That Are Both Required for Endosome Traffic. Mol. Biol. Cell 19: 1415-1426 [Abstract] [Full Text]
Lindwasser, O. W., Smith, W. J., Chaudhuri, R., Yang, P., Hurley, J. H., Bonifacino, J. S. (2008). A Diacidic Motif in Human Immunodeficiency Virus Type 1 Nef Is a Novel Determinant of Binding to AP-2. J. Virol. 82: 1166-1174 [Abstract] [Full Text]
Noviello, C. M., Benichou, S., Guatelli, J. C. (2008). Cooperative Binding of the Class I Major Histocompatibility Complex Cytoplasmic Domain and Human Immunodeficiency Virus Type 1 Nef to the Endosomal AP-1 Complex via Its {micro} Subunit. J. Virol. 82: 1249-1258 [Abstract] [Full Text]
Cancino, J., Torrealba, C., Soza, A., Yuseff, M. I., Gravotta, D., Henklein, P., Rodriguez-Boulan, E., Gonzalez, A. (2007). Antibody to AP1B Adaptor Blocks Biosynthetic and Recycling Routes of Basolateral Proteins at Recycling Endosomes. Mol. Biol. Cell 18: 4872-4884 [Abstract] [Full Text]
Hubner, W., Chen, P., Portillo, A. D., Liu, Y., Gordon, R. E., Chen, B. K. (2007). Sequence of Human Immunodeficiency Virus Type 1 (HIV-1) Gag Localization and Oligomerization Monitored with Live Confocal Imaging of a Replication-Competent, Fluorescently Tagged HIV-1. J. Virol. 81: 12596-12607 [Abstract] [Full Text]
Lubben, N. B., Sahlender, D. A., Motley, A. M., Lehner, P. J., Benaroch, P., Robinson, M. S. (2007). HIV-1 Nef-induced Down-Regulation of MHC Class I Requires AP-1 and Clathrin but Not PACS-1 and Is Impeded by AP-2. Mol. Biol. Cell 18: 3351-3365 [Abstract] [Full Text]
Li, C., Hao, M., Cao, Z., Ding, W., Graves-Deal, R., Hu, J., Piston, D. W., Coffey, R. J. (2007). Naked2 Acts as a Cargo Recognition and Targeting Protein to Ensure Proper Delivery and Fusion of TGF-{alpha} containing Exocytic Vesicles at the Lower Lateral Membrane of Polarized MDCK Cells. Mol. Biol. Cell 18: 3081-3093 [Abstract] [Full Text]
Copic, A., Starr, T. L., Schekman, R. (2007). Ent3p and Ent5p Exhibit Cargo-specific Functions in Trafficking Proteins between the Trans-Golgi Network and the Endosomes in Yeast. Mol. Biol. Cell 18: 1803-1815 [Abstract] [Full Text]
Doray, B., Lee, I., Knisely, J., Bu, G., Kornfeld, S. (2007). The {gamma}/{sigma}1 and {alpha}/{sigma}2 Hemicomplexes of Clathrin Adaptors AP-1 and AP-2 Harbor the Dileucine Recognition Site. Mol. Biol. Cell 18: 1887-1896 [Abstract] [Full Text]
Chaudhuri, R., Lindwasser, O. W., Smith, W. J., Hurley, J. H., Bonifacino, J. S. (2007). Downregulation of CD4 by Human Immunodeficiency Virus Type 1 Nef Is Dependent on Clathrin and Involves Direct Interaction of Nef with the AP2 Clathrin Adaptor. J. Virol. 81: 3877-3890 [Abstract] [Full Text]
Setty, S. R. G., Tenza, D., Truschel, S. T., Chou, E., Sviderskaya, E. V., Theos, A. C., Lamoreux, M. L., Di Pietro, S. M., Starcevic, M., Bennett, D. C., Dell'Angelica, E. C., Raposo, G., Marks, M. S. (2007). BLOC-1 Is Required for Cargo-specific Sorting from Vacuolar Early Endosomes toward Lysosome-related Organelles. Mol. Biol. Cell 18: 768-780 [Abstract] [Full Text]
Newell-Litwa, K., Seong, E., Burmeister, M., Faundez, V. (2007). Neuronal and non-neuronal functions of the AP-3 sorting machinery. J. Cell Sci. 120: 531-541 [Abstract] [Full Text]
Traub, L. M., Lukacs, G. L. (2007). Decoding ubiquitin sorting signals for clathrin-dependent endocytosis by CLASPs. J. Cell Sci. 120: 543-553 [Abstract] [Full Text]
Pak, Y., Glowacka, W. K., Bruce, M. C., Pham, N., Rotin, D. (2006). Transport of LAPTM5 to lysosomes requires association with the ubiquitin ligase Nedd4, but not LAPTM5 ubiquitination. JCB 175: 631-645 [Abstract] [Full Text]
Loomis, J. S., Courtney, R. J., Wills, J. W. (2006). Packaging Determinants in the UL11 Tegument Protein of Herpes Simplex Virus Type 1. J. Virol. 80: 10534-10541 [Abstract] [Full Text]
Grati, M., Aggarwal, N., Strehler, E. E., Wenthold, R. J. (2006). Molecular determinants for differential membrane trafficking of PMCA1 and PMCA2 in mammalian hair cells. J. Cell Sci. 119: 2995-3007 [Abstract] [Full Text]
Roeth, J. F., Collins, K. L. (2006). Human Immunodeficiency Virus Type 1 Nef: Adapting to Intracellular Trafficking Pathways. Microbiol. Mol. Biol. Rev. 70: 548-563 [Abstract] [Full Text]
Schmidt, U., Briese, S., Leicht, K., Schurmann, A., Joost, H.-G., Al-Hasani, H. (2006). Endocytosis of the glucose transporter GLUT8 is mediated by interaction of a dileucine motif with the {beta}2-adaptin subunit of the AP-2 adaptor complex. J. Cell Sci. 119: 2321-2331 [Abstract] [Full Text]
Valencia, J. C., Watabe, H., Chi, A., Rouzaud, F., Chen, K. G., Vieira, W. D., Takahashi, K., Yamaguchi, Y., Berens, W., Nagashima, K., Shabanowitz, J., Hunt, D. F., Appella, E., Hearing, V. J. (2006). Sorting of Pmel17 to melanosomes through the plasma membrane by AP1 and AP2: evidence for the polarized nature of melanocytes. J. Cell Sci. 119: 1080-1091 [Abstract] [Full Text]
Radtke, S., Jorissen, A., de Leur, H. S.-V., Heinrich, P. C., Behrmann, I. (2006). Three Dileucine-like Motifs within the Interbox1/2 Region of the Human Oncostatin M Receptor Prevent Efficient Surface Expression in the Absence of an Associated Janus Kinase. J. Biol. Chem. 281: 4024-4034 [Abstract] [Full Text]
Coleman, S. H., Madrid, R., Van Damme, N., Mitchell, R. S., Bouchet, J., Servant, C., Pillai, S., Benichou, S., Guatelli, J. C. (2006). Modulation of Cellular Protein Trafficking by Human Immunodeficiency Virus Type 1 Nef: Role of the Acidic Residue in the ExxxLL Motif. J. Virol. 80: 1837-1849 [Abstract] [Full Text]
Theos, A. C., Tenza, D., Martina, J. A., Hurbain, I., Peden, A. A., Sviderskaya, E. V., Stewart, A., Robinson, M. S., Bennett, D. C., Cutler, D. F., Bonifacino, J. S., Marks, M. S., Raposo, G. (2005). Functions of Adaptor Protein (AP)-3 and AP-1 in Tyrosinase Sorting from Endosomes to Melanosomes. Mol. Biol. Cell 16: 5356-5372 [Abstract] [Full Text]
Jin, Y.-J., Cai, C. Y., Zhang, X., Zhang, H.-T., Hirst, J. A., Burakoff, S. J. (2005). HIV Nef-Mediated CD4 Down-Regulation Is Adaptor Protein Complex 2 Dependent. J. Immunol. 175: 3157-3164 [Abstract] [Full Text]
Nie, Z., Fei, J., Premont, R. T., Randazzo, P. A. (2005). The Arf GAPs AGAP1 and AGAP2 distinguish between the adaptor protein complexes AP-1 and AP-3. J. Cell Sci. 118: 3555-3566 [Abstract] [Full Text]
Newton, E. E., Wu, Z., Simister, N. E. (2005). Characterization of basolateral-targeting signals in the neonatal Fc receptor. J. Cell Sci. 118: 2461-2469 [Abstract] [Full Text]
Dugast, M., Toussaint, H., Dousset, C., Benaroch, P. (2005). AP2 Clathrin Adaptor Complex, but Not AP1, Controls the Access of the Major Histocompatibility Complex (MHC) Class II to Endosomes. J. Biol. Chem. 280: 19656-19664 [Abstract] [Full Text]
Mishra, S. K., Keyel, P. A., Edeling, M. A., Dupin, A. L., Owen, D. J., Traub, L. M. (2005). Functional Dissection of an AP-2 {beta}2 Appendage-binding Sequence within the Autosomal Recessive Hypercholesterolemia Protein. J. Biol. Chem. 280: 19270-19280 [Abstract] [Full Text]
Kyttala, A., Yliannala, K., Schu, P., Jalanko, A., Luzio, J. P. (2005). AP-1 and AP-3 Facilitate Lysosomal Targeting of Batten Disease Protein CLN3 via Its Dileucine Motif. J. Biol. Chem. 280: 10277-10283 [Abstract] [Full Text]
Rose, J. J., Janvier, K., Chandrasekhar, S., Sekaly, R. P., Bonifacino, J. S., Venkatesan, S. (2005). CD4 Down-regulation by HIV-1 and Simian Immunodeficiency Virus (SIV) Nef Proteins Involves Both Internalization and Intracellular Retention Mechanisms. J. Biol. Chem. 280: 7413-7426 [Abstract] [Full Text]
Wernick, N. L. B., Haucke, V., Simister, N. E. (2005). Recognition of the Tryptophan-based Endocytosis Signal in the Neonatal Fc Receptor by the {micro} Subunit of Adaptor Protein-2. J. Biol. Chem. 280: 7309-7316 [Abstract] [Full Text]
Coleman, S. H., Van Damme, N., Day, J. R., Noviello, C. M., Hitchin, D., Madrid, R., Benichou, S., Guatelli, J. C. (2005). Leucine-Specific, Functional Interactions between Human Immunodeficiency Virus Type 1 Nef and Adaptor Protein Complexes. J. Virol. 79: 2066-2078 [Abstract] [Full Text]
Madrid, R., Janvier, K., Hitchin, D., Day, J., Coleman, S., Noviello, C., Bouchet, J., Benmerah, A., Guatelli, J., Benichou, S. (2005). Nef-induced Alteration of the Early/Recycling Endosomal Compartment Correlates with Enhancement of HIV-1 Infectivity. J. Biol. Chem. 280: 5032-5044 [Abstract] [Full Text]
Seong, E., Wainer, B. H., Hughes, E. D., Saunders, T. L., Burmeister, M., Faundez, V. (2005). Genetic Analysis of the Neuronal and Ubiquitous AP-3 Adaptor Complexes Reveals Divergent Functions in Brain. Mol. Biol. Cell 16: 128-140 [Abstract] [Full Text]
Storch, S., Pohl, S., Braulke, T. (2004). A Dileucine Motif and a Cluster of Acidic Amino Acids in the Second Cytoplasmic Domain of the Batten Disease-related CLN3 Protein Are Required for Efficient Lysosomal Targeting. J. Biol. Chem. 279: 53625-53634 [Abstract] [Full Text]
Roeth, J. F., Williams, M., Kasper, M. R., Filzen, T. M., Collins, K. L. (2004). HIV-1 Nef disrupts MHC-I trafficking by recruiting AP-1 to the MHC-I cytoplasmic tail. JCB 167: 903-913 [Abstract] [Full Text]
Jin, Y.-J., Zhang, X., Boursiquot, J. G., Burakoff, S. J. (2004). CD4 Phosphorylation Partially Reverses Nef Down-Regulation of CD4. J. Immunol. 173: 5495-5500 [Abstract] [Full Text]
Deora, A. A., Gravotta, D., Kreitzer, G., Hu, J., Bok, D., Rodriguez-Boulan, E. (2004). The Basolateral Targeting Signal of CD147 (EMMPRIN) Consists of a Single Leucine and Is Not Recognized by Retinal Pigment Epithelium. Mol. Biol. Cell 15: 4148-4165 [Abstract] [Full Text]
Stockli, J., Honing, S., Rohrer, J. (2004). The Acidic Cluster of the CK2 Site of the Cation-dependent Mannose 6-Phosphate Receptor (CD-MPR) but Not Its Phosphorylation Is Required for GGA1 and AP-1 Binding. J. Biol. Chem. 279: 23542-23549 [Abstract] [Full Text]