Accessible Requires Authentication Published by De Gruyter February 25, 2015

Team work at its best – TAPL and its two domains

Tina Zollmann, Christoph Bock, Philipp Graab and Rupert Abele
From the journal Biological Chemistry

Abstract

The transporter associated with antigen processing (TAPL, ABCB9) is a homodimeric ABC transporter, shuttling cytosolic polypeptides into the lumen of lysosomes energized by ATP hydrolysis. Here we give a short overview of the superfamily of ABC transporters and summarize the current state of knowledge on TAPL in detail. The architecture of TAPL and its substrate specificity are described and we discuss the function of an extra N-terminal transmembrane domain, called TMD0, in respect of subcellular targeting and interaction with proteins, contributing to long-term stability. As TAPL shows – besides a ubiquitous basal expression – an elevated expression in antigen presenting cells, we present models of TAPL function in adaptive immunity.


Corresponding author: Rupert Abele, Institute of Biochemistry, Biocenter, Goethe University Frankfurt, Max-von-Laue-Str. 9, D-60438 Frankfurt/Main, Germany, e-mail:

Acknowledgments

This work was supported by the German Research Foundation via SFB807 – Transport and Communication across Membranes (R.A.) and Fond der Chemischen Industrie (T.Z. and R.A.)

References

Ambudkar, S.V., Cardarelli, C.O., Pashinsky, I., and Stein, W.D. (1997). Relation between the turnover number for vinblastine transport and for vinblastine-stimulated ATP hydrolysis by human P-glycoprotein. J. Biol. Chem. 272, 21160–21166. Search in Google Scholar

Andrejewski, N., Punnonen, E.L., Guhde, G., Tanaka, Y., Lullmann-Rauch, R., Hartmann, D., von Figura, K., and Saftig, P. (1999). Normal lysosomal morphology and function in LAMP-1-deficient mice. J. Biol. Chem. 274, 12692–12701. Search in Google Scholar

Bandler, P.E., Westlake, C.J., Grant, C.E., Cole, S.P., and Deeley, R.G. (2008). Identification of regions required for apical membrane localization of human multidrug resistance protein 2. Mol. Pharmacol. 74, 9–19. Search in Google Scholar

Biemans-Oldehinkel, E., Doeven, M.K., and Poolman, B. (2006). ABC transporter architecture and regulatory roles of accessory domains. FEBS Lett. 580, 1023–1035. Search in Google Scholar

Borst, P. and Elferink, R.O. (2002). Mammalian ABC transporters in health and disease. Annu. Rev. Biochem. 71, 537–592. Search in Google Scholar

Chan, K.W., Zhang, H., and Logothetis, D.E. (2003). N-terminal transmembrane domain of the SUR controls trafficking and gating of Kir6 channel subunits. EMBO J. 22, 3833–3843. Search in Google Scholar

Chen, Z.S. and Tiwari, A.K. (2011). Multidrug resistance proteins (MRPs/ABCCs) in cancer chemotherapy and genetic diseases. FEBS J. 278, 3226–3245. Search in Google Scholar

Chicz, R.M., Urban, R.G., Gorga, J.C., Vignali, D.A., Lane, W.S., and Strominger, J.L. (1993). Specificity and promiscuity among naturally processed peptides bound to HLA-DR alleles. J. Exp. Med. 178, 27–47. Search in Google Scholar

Cuervo, A.M. and Dice, J.F. (1996). A receptor for the selective uptake and degradation of proteins by lysosomes. Science 273, 501–503. Search in Google Scholar

Cui, J. and Davidson, A.L. (2011). ABC solute importers in bacteria. Essays Biochem. 50, 85–99. Search in Google Scholar

Dani, A., Chaudhry, A., Mukherjee, P., Rajagopal, D., Bhatia, S., George, A., Bal, V., Rath, S., and Mayor, S. (2004). The pathway for MHCII-mediated presentation of endogenous proteins involves peptide transport to the endo-lysosomal compartment. J. Cell Sci. 117, 4219–4230. Search in Google Scholar

Davidson, A.L., Dassa, E., Orelle, C., and Chen, J. (2008). Structure, function, and evolution of bacterial ATP-binding cassette systems. Microbiol. Mol. Biol. Rev. 72, 317–364. Search in Google Scholar

Dawson, R.J. and Locher, K.P. (2006). Structure of a bacterial multidrug ABC transporter. Nature 443, 180–185. Search in Google Scholar

Dean, M. (2005). The genetics of ATP-binding cassette transporters. Methods Enzymol. 400, 409–429. Search in Google Scholar

Dean, M. and Annilo, T. (2005). Evolution of the ATP-binding cassette (ABC) transporter superfamily in vertebrates. Annu. Rev. Genomics Hum. Genet. 6, 123–142. Search in Google Scholar

Demirel, Ö., Bangert, I., Tampé, R., and Abele, R. (2010). Tuning the cellular trafficking of the lysosomal peptide transporter TAPL by its N-terminal domain. Traffic 11, 383–393. Search in Google Scholar

Demirel, Ö., Jan, I., Wolters, D., Blanz, J., Saftig, P., Tampé, R., and Abele, R. (2012). The lysosomal polypeptide transporter TAPL is stabilized by interaction with LAMP-1 and LAMP-2. J. Cell Sci. 125, 4230–4240. Search in Google Scholar

Demirel, Ö., Waibler, Z., Kalinke, U., Grünebach, F., Appel, S., Brossart, P., Hasilik, A., Tampé, R., and Abele, R. (2007). Identification of a lysosomal peptide transport system induced during dendritic cell development. J. Biol. Chem. 282, 37836–37843. Search in Google Scholar

Denzer, K., Kleijmeer, M.J., Heijnen, H.F., Stoorvogel, W., and Geuze, H.J. (2000). Exosome: from internal vesicle of the multivesicular body to intercellular signaling device. J. Cell Sci. 113, 3365–3374. Search in Google Scholar

Dongre, A.R., Kovats, S., deRoos, P., McCormack, A.L., Nakagawa, T., Paharkova-Vatchkova, V., Eng, J., Caldwell, H., Yates, J.R., and Rudensky, A.Y. (2001). In vivo MHC class II presentation of cytosolic proteins revealed by rapid automated tandem mass spectrometry and functional analyses. Eur. J. Immunol. 31, 1485–1494. Search in Google Scholar

Eggensperger, S., Fisette, O., Parcej, D., Schäfer, L.V., and Tampé, R. (2014). An annular lipid belt is essential for allosteric coupling and viral inhibition of the antigen translocation complex TAP (transporter associated with antigen processing). J. Biol. Chem. 289, 33098–33108. Search in Google Scholar

Escola, J.M., Kleijmeer, M.J., Stoorvogel, W., Griffith, J.M., Yoshie, O., and Geuze, H.J. (1998). Selective enrichment of tetraspan proteins on the internal vesicles of multivesicular endosomes and on exosomes secreted by human B-lymphocytes. J. Biol. Chem. 273, 20121–20127. Search in Google Scholar

Eskelinen, E.L., Tanaka, Y., and Saftig, P. (2003). At the acidic edge: emerging functions for lysosomal membrane proteins. Trends Cell Biol. 13, 137–145. Search in Google Scholar

Eytan, G.D., Regev, R., and Assaraf, Y.G. (1996). Functional reconstitution of P-glycoprotein reveals an apparent near stoichiometric drug transport to ATP hydrolysis. J. Biol. Chem. 271, 3172–3178. Search in Google Scholar

George, A.M. and Jones, P.M. (2012). Perspectives on the structure-function of ABC transporters: the Switch and Constant Contact models. Prog. Biophys. Mol. Biol. 109, 95–107. Search in Google Scholar

Gerber, S., Comellas-Bigler, M., Goetz, B.A., and Locher, K.P. (2008). Structural basis of trans-inhibition in a molybdate/tungstate ABC transporter. Science 321, 246–250. Search in Google Scholar

Henne, W.M., Buchkovich, N.J., and Emr, S.D. (2011). The ESCRT pathway. Dev. Cell 21, 77–91. Search in Google Scholar

Jones, P.M. and George, A.M. (2004). The ABC transporter structure and mechanism: perspectives on recent research. Cell. Mol. Life Sci. 61, 682–699. Search in Google Scholar

Kamakura, A., Fujimoto, Y., Motohashi, Y., Ohashi, K., Ohashi-Kobayashi, A., and Maeda, M. (2008). Functional dissection of transmembrane domains of human TAP-like (ABCB9). Biochem. Biophys. Res. Commun. 377, 847–851. Search in Google Scholar

Kang, J., Hwang, J.U., Lee, M., Kim, Y.Y., Assmann, S.M., Martinoia, E., and Lee, Y. (2010). PDR-type ABC transporter mediates cellular uptake of the phytohormone abscisic acid. Proc. Natl. Acad. Sci. USA 107, 2355–2360. Search in Google Scholar

Kawai, H., Tanji, T., Shiraishi, H., Yamada, M., Iijima, R., Inoue, T., Kezuka, Y., Ohashi, K., Yoshida, Y., Tohyama, K., et al. (2009). Normal formation of a subset of intestinal granules in Caenorhabditis elegans requires ATP-binding cassette transporters HAF-4 and HAF-9, which are highly homologous to human lysosomal peptide transporter TAP-like. Mol. Biol. Cell 20, 2979–2990. Search in Google Scholar

Kobayashi, A., Kasano, M., Maeda, T., Hori, S., Motojima, K., Suzuki, M., Fujiwara, T., Takahashi, E., Yabe, T., Tanaka, K., et al. (2000). A half-type ABC transporter TAPL is highly conserved between rodent and man, and the human gene is not responsive to interferon-gamma in contrast to TAP1 and TAP2. J. Biochem. 128, 711–718. Search in Google Scholar

Kobayashi, A., Hori, S., Suita, N., and Maeda, M. (2003). Gene organization of human transporter associated with antigen processing-like (TAPL, ABCB9): analysis of alternative splicing variants and promoter activity. Biochem. Biophys. Res. Commun. 309, 815–822. Search in Google Scholar

Koch, J., Guntrum, R., Heintke, S., Kyritsis, C., and Tampé, R. (2004). Functional dissection of the transmembrane domains of the transporter associated with antigen processing (TAP). J. Biol. Chem. 279, 10142–10147. Search in Google Scholar

Koopmann, J.O., Post, M., Neefjes, J.J., Hämmerling, G.J., and Momburg, F. (1996). Translocation of long peptides by transporters associated with antigen processing (TAP). Eur. J. Immunol. 26, 1720–1728. Search in Google Scholar

Lee, M., Choi, Y., Burla, B., Kim, Y.Y., Jeon, B., Maeshima, M., Yoo, J.Y., Martinoia, E., and Lee, Y. (2008). The ABC transporter AtABCB14 is a malate importer and modulates stomatal response to CO2. Nat. Cell Biol. 10, 1217–1223. Search in Google Scholar

Leveson-Gower, D.B., Michnick, S.W., and Ling, V. (2004). Detection of TAP family dimerizations by an in vivo assay in mammalian cells. Biochemistry 43, 14257–14264. Search in Google Scholar

Li, L., He, S., Sun, J.M., and Davie, J.R. (2004). Gene regulation by Sp1 and Sp3. Biochem. Cell Biol. 82, 460–471. Search in Google Scholar

Locher, K.P. (2009). Review. Structure and mechanism of ATP-binding cassette transporters. Philos. Trans. R. Soc. Lond. B. Biol. Sci. 364, 239–245. Search in Google Scholar

Locher, K.P., Lee, A.T., and Rees, D.C. (2002). The E. coli BtuCD structure: a framework for ABC transporter architecture and mechanism. Science 296, 1091–1098. Search in Google Scholar

Merzougui, N., Kratzer, R., Saveanu, L., and van Endert, P. (2011). A proteasome-dependent, TAP-independent pathway for cross-presentation of phagocytosed antigen. EMBO Rep. 12, 1257–1264. Search in Google Scholar

Mizushima, N. and Levine, B. (2010). Autophagy in mammalian development and differentiation. Nat. Cell Biol. 12, 823–830. Search in Google Scholar

Neumann, L. and Tampé, R. (1999). Kinetic analysis of peptide binding to the TAP transport complex: evidence for structural rearrangements induced by substrate binding. J. Mol. Biol. 294, 1203–1213. Search in Google Scholar

Nishimura, M. and Naito, S. (2005). Tissue-specific mRNA expression profiles of human ATP-binding cassette and solute carrier transporter superfamilies. Drug Metab. Pharmacokinet. 20, 452–477. Search in Google Scholar

Nürenberg, E. and Tampé, R. (2013). Tying up loose ends: ribosome recycling in eukaryotes and archaea. Trends Biochem. Sci. 38, 64–74. Search in Google Scholar

Oldham, M.L., Khare, D., Quiocho, F.A., Davidson, A.L., and Chen, J. (2007). Crystal structure of a catalytic intermediate of the maltose transporter. Nature 450, 515–521. Search in Google Scholar

Parcej, D. and Tampé, R. (2010). ABC proteins in antigen translocation and viral inhibition. Nat. Chem. Biol. 6, 572–580. Search in Google Scholar

Patzlaff, J.S., van der Heide, T., and Poolman, B. (2003). The ATP/substrate stoichiometry of the ATP-binding cassette (ABC) transporter OpuA. J. Biol. Chem. 278, 29546–29551. Search in Google Scholar

Powis, S.J., Townsend, A.R., Deverson, E.V., Bastin, J., Butcher, G.W., and Howard, J.C. (1991). Restoration of antigen presentation to the mutant cell line RMA-S by an MHC-linked transporter. Nature 354, 528–531. Search in Google Scholar

Ramos, M.S., Abele, R., Nagy, R., Grotemeyer, M.S., Tampé, R., Rentsch, D., and Martinoia, E. (2011). Characterization of a transport activity for long-chain peptides in barley mesophyll vacuoles. J. Exp. Bot. 62, 2403–2410. Search in Google Scholar

Rice, A.J., Park, A., and Pinkett, H.W. (2014). Diversity in ABC transporters: Type I, II and III importers. Crit. Rev. Biochem. Mol. Biol. 49, 426–437. Search in Google Scholar

Rudensky, AYu, Preston-Hurlburt, P., Hong, S.C., Barlow, A., and Janeway, C.A. (1991). Sequence analysis of peptides bound to MHC class II molecules. Nature 353, 622–627. Search in Google Scholar

Schmitt, L. and Tampé, R. (2002). Structure and mechanism of ABC transporters. Curr. Opin. Struct. Biol. 12, 754–760. Search in Google Scholar

Schuette, V. and Burgdorf, S. (2014). The ins-and-outs of endosomal antigens for cross-presentation. Curr. Opin. Immunol. 26, 63–68. Search in Google Scholar

Sun, H. (2012). Membrane receptors and transporters involved in the function and transport of vitamin A and its derivatives. Biochim. Biophys. Acta 1821, 99–112. Search in Google Scholar

Tanaka, Y., Guhde, G., Suter, A., Eskelinen, E.L., Hartmann, D., Lullmann-Rauch, R., Janssen, P.M., Blanz, J., von Figura, K., and Saftig, P. (2000). Accumulation of autophagic vacuoles and cardiomyopathy in LAMP-2-deficient mice. Nature 406, 902–906. Search in Google Scholar

Tanji, T., Nishikori, K., Shiraishi, H., Maeda, M., and Ohashi-Kobayashi, A. (2013). Co-operative function and mutual stabilization of the half ATP-binding cassette transporters HAF-4 and HAF-9 in Caenorhabditis elegans. Biochem. J. 452, 467–475. Search in Google Scholar

Tanno, H. and Komada, M. (2013). The ubiquitin code and its decoding machinery in the endocytic pathway. J. Biochem. 153, 497–504. Search in Google Scholar

Tarling, E.J., de Aguiar Vallim, T.Q., and Edwards, P.A. (2013). Role of ABC transporters in lipid transport and human disease. Trends Endocrinol. Metab. 24, 342–350. Search in Google Scholar

ter Beek, J., Guskov, A., and Slotboom, D.J. (2014). Structural diversity of ABC transporters. J. Gen. Physiol. 143, 419–435. Search in Google Scholar

Thiele, F., Tao, S., Zhang, Y., Muschaweckh, A., Zollmann, T., Protzer, U., Abele, R., and Drexler, I. (2015). Modified vaccinia virus Ankara-infected dendritic cells present CD4+ T-cell epitopes by endogenous major histocompatibility complex class II presentation pathways. J. Virol. 89, 2698–2709. Search in Google Scholar

Uebel, S., Kraas, W., Kienle, S., Wiesmuller, K.H., Jung, G., and Tampé, R. (1997). Recognition principle of the TAP transporter disclosed by combinatorial peptide libraries. Proc. Natl. Acad. Sci. USA 94, 8976–8981. Search in Google Scholar

Uinuk-ool, T.S., Mayer, W.E., Sato, A., Takezaki, N., Benyon, L., Cooper, M.D., and Klein, J. (2003). Identification and characterization of a TAP-family gene in the lamprey. Immunogenetics 55, 38–48. Search in Google Scholar

van Endert, P.M., Tampé, R., Meyer, T.H., Tisch, R., Bach, J.-F., and McDevitt, H.O. (1994). A sequential model for peptide binding and transport by the transporters associated with antigen processing. Immunity 1, 491–500. Search in Google Scholar

Virgin, H.W. and Levine, B. (2009). Autophagy genes in immunity. Nat. Immunol. 10, 461–470. Search in Google Scholar

Wolters, J.C., Abele, R., and Tampé, R. (2005). Selective and ATP-dependent translocation of peptides by the homodimeric ATP binding cassette transporter TAP-like (ABCB9). J. Biol. Chem. 280, 23631–23636. Search in Google Scholar

Yamaguchi, Y., Kasano, M., Terada, T., Sato, R., and Maeda, M. (1999). An ABC transporter homologous to TAP proteins. FEBS Lett. 457, 231–236. Search in Google Scholar

Yamaguchi, Y., Iseoka, H., Kobayashi, A., and Maeda, M. (2004). The carboxyl terminal sequence of rat transporter associated with antigen processing (TAP)-like (ABCB9) is heterogeneous due to splicing of its mRNA. Biol. Pharm. Bull. 27, 100–104. Search in Google Scholar

Zhang, P. (2013). Structure and mechanism of energy-coupling factor transporters. Trends Microbiol. 21, 652–659. Search in Google Scholar

Zhang, F., Zhang, W., Liu, L., Fisher, C.L., Hui, D., Childs, S., Dorovini-Zis, K., and Ling, V. (2000). Characterization of ABCB9, an ATP binding cassette protein associated with lysosomes. J. Biol. Chem. 275, 23287–23294. Search in Google Scholar

Zhao, C., Tampé, R., and Abele, R. (2006). TAP and TAP-like – brothers in arms? Naunyn-Schmiedeberg’s Arch. Pharmacol. 372, 444–450. Search in Google Scholar

Zhao, C., Haase, W., Tampé, R., and Abele, R. (2008). Peptide specificity and lipid activation of the lysosomal transport complex ABCB9 (TAPL). J. Biol. Chem. 283, 17083–17091. Search in Google Scholar

Zollmann, T., Moiset, G., Tumulka, F., Tampé, R., Poolman, B., and Abele, R. (2015). Single liposome analysis of peptide translocation by the ABC transporter TAPL. Proc. Natl. Acad. Sci. USA 112, 2046–2051. Search in Google Scholar

Received: 2014-12-23
Accepted: 2015-2-20
Published Online: 2015-2-25
Published in Print: 2015-9-1

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