As part of a high-throughput subcellular localisation project, the protein encoded by the RIKEN mouse cDNA 2610528J11 was expressed and identified to be associated with both endosomes and the plasma membrane. Based on this, we have assigned the name TEMP for Type III Endosome Membrane Protein. TEMP encodes a short protein of 111 amino acids with a single, alpha-helical transmembrane domain. Experimental analysis of its membrane topology demonstrated it is a Type III membrane protein with the amino-terminus in the lumenal, or extracellular region, and the carboxy-terminus in the cytoplasm. In addition to the plasma membrane TEMP was localized to Rab5 positive early endosomes, Rab5/Rab11 positive recycling endosomes but not Rab7 positive late endosomes. Video microscopy in living cells confirmed TEMP's plasma membrane localization and identified the intracellular endosome compartments to be tubulovesicular. Overexpression of TEMP resulted in the early/recycling endosomes clustering at the cell periphery that was dependent on the presence of intact microtubules. The cellular function of TEMP cannot be inferred based on bioinformatics comparison, but its cellular distribution between early/recycling endosomes and the plasma membrane suggests a role in membrane transport.
References
[1]
Aturaliya, R.N.; Fink, J.L.; Davis, M.J.; Teasdale, M.S.; Hanson, K.A.; Miranda, K.C.; Forrest, A.R.; Grimmond, S.M.; Suzuki, H.; Kanamori, M.; et al. Subcellular localization of mammalian type ii membrane proteins. Traffic 2006, 7, 613–625, doi:10.1111/j.1600-0854.2006.00407.x.
Forrest, A.R.; Taylor, D.F.; Fink, J.L.; Gongora, M.M.; Flegg, C.; Teasdale, R.D.; Suzuki, H.; Kanamori, M.; Kai, C.; Hayashizaki, Y.; et al. Phosphoregdb: The tissue and sub-cellular distribution of mammalian protein kinases and phosphatases. BMC bioinformatics 2006, 7, 82, doi:10.1186/1471-2105-7-82.
[4]
Locate—subcellular localisation database. Available online: http://www.locate.imb.uq.edu.au (accessed on 30 October 2012).
Goder, V.; Spiess, M. Topogenesis of membrane proteins: Determinants and dynamics. FEBS Lett. 2001, 504, 87–93, doi:10.1016/S0014-5793(01)02712-0.
[8]
Suzuki, H.; Forrest, A.R.; van Nimwegen, E.; Daub, C.O.; Balwierz, P.J.; Irvine, K.M.; Lassmann, T.; Ravasi, T.; Hasegawa, Y.; de Hoon, M.J., et al. The transcriptional network that controls growth arrest and differentiation in a human myeloid leukemia cell line. Nat. Genet 2009, 41, 553–562, doi:10.1038/ng.375.
[9]
Davis, M.J.; Zhang, F.; Yuan, Z.; Teasdale, R.D. Memo: A consensus approach to the annotation of a protein's membrane organization. In Silico Biol. 2006, 6, 387–399.
[10]
Chai, L.; Dai, L.; Che, Y.; Xu, J.; Liu, G.; Zhang, Z.; Yang, R. Lrrc19, a novel member of the leucine-rich repeat protein family, activates nf-kappab and induces expression of proinflammatory cytokines. Biochem. Biophys. Res. Commun. 2009, 388, 543–548, doi:10.1016/j.bbrc.2009.08.043.
[11]
McMahon, H.T.; Mills, I.G. Cop and clathrin-coated vesicle budding: Different pathways, common approaches. Curr. Opin. Cell. Biol. 2004, 16, 379–391, doi:10.1016/j.ceb.2004.06.009.
[12]
Su, A.I.; Cooke, M.P.; Ching, K.A.; Hakak, Y.; Walker, J.R.; Wiltshire, T.; Orth, A.P.; Vega, R.G.; Sapinoso, L.M.; Moqrich, A.; et al. Large-scale analysis of the human and mouse transcriptomes. Proc. Natl. Acad. Sci. USA 2002, 99, 4465–4470.
[13]
Wu, C.; Orozco, C.; Boyer, J.; Leglise, M.; Goodale, J.; Batalov, S.; Hodge, C.L.; Haase, J.; Janes, J.; Huss, J.W., 3rd; et al. Biogps: An extensible and customizable portal for querying and organizing gene annotation resources. Genome Biol. 2009, 10, R130, doi:10.1186/gb-2009-10-11-r130.
[14]
Kurten, R.C.; Cadena, D.L.; Gill, G.N. Enhanced degradation of egf receptors by a sorting nexin, snx1. Science 1996, 272, 1008–1010.
[15]
Nakamura, N.; Sun-Wada, G.H.; Yamamoto, A.; Wada, Y.; Futai, M. Association of mouse sorting nexin 1 with early endosomes. J. Biochem. (Tokyo) 2001, 130, 765–771.
[16]
Haft, C.R.; de la Luz Sierra, M.; Barr, V.A.; Haft, D.H.; Taylor, S.I. Identification of a family of sorting nexin molecules and characterization of their association with receptors. Mol. Cell. Biol. 1998, 18, 7278–7287.
[17]
Schnatwinkel, C.; Christoforidis, S.; Lindsay, M.R.; Uttenweiler-Joseph, S.; Wilm, M.; Parton, R.G.; Zerial, M. The rab5 effector rabankyrin-5 regulates and coordinates different endocytic mechanisms. PLoS Biol. 2004, 2, E261, doi:10.1371/journal.pbio.0020261.
[18]
Mohrmann, K.; van der Sluijs, P. Regulation of membrane transport through the endocytic pathway by rabgtpases. Mol. Membr. Biol. 1999, 16, 81–87, doi:10.1080/096876899294797.
Zerial, M.; McBride, H. Rab proteins as membrane organizers. Nat. Rev. Mol. Cell. Biol. 2001, 2, 107–117, doi:10.1038/35052055.
[21]
Gorvel, J.P.; Chavrier, P.; Zerial, M.; Gruenberg, J. Rab5 controls early endosome fusion in vitro. Cell 1991, 64, 915–925, doi:10.1016/0092-8674(91)90316-Q.
[22]
Bucci, C.; Parton, R.G.; Mather, I.H.; Stunnenberg, H.; Simons, K.; Hoflack, B.; Zerial, M. The small gtpase rab5 functions as a regulatory factor in the early endocytic pathway. Cell 1992, 70, 715–728, doi:10.1016/0092-8674(92)90306-W.
[23]
Roberts, R.L.; Barbieri, M.A.; Pryse, K.M.; Chua, M.; Morisaki, J.H.; Stahl, P.D. Endosome fusion in living cells overexpressing gfp-rab5. J. Cell. Sci. 1999, 112 (Pt 21), 3667–3675.
[24]
Rink, J.; Ghigo, E.; Kalaidzidis, Y.; Zerial, M. Rab conversion as a mechanism of progression from early to late endosomes. Cell 2005, 122, 735–749, doi:10.1016/j.cell.2005.06.043.
[25]
Sonnichsen, B.; De Renzis, S.; Nielsen, E.; Rietdorf, J.; Zerial, M. Distinct membrane domains on endosomes in the recycling pathway visualized by multicolor imaging of rab4, rab5, and rab11. J. Cell. Biol. 2000, 149, 901–914, doi:10.1083/jcb.149.4.901.
[26]
Sheff, D.R.; Daro, E.A.; Hull, M.; Mellman, I. The receptor recycling pathway contains two distinct populations of early endosomes with different sorting functions. J. Cell. Biol. 1999, 145, 123–139, doi:10.1083/jcb.145.1.123.
[27]
Trischler, M.; Stoorvogel, W.; Ullrich, O. Biochemical analysis of distinct rab5- and rab11-positive endosomes along the transferrin pathway. J. Cell. Sci. 1999, 112 (Pt 24), 4773–4783.
[28]
van der Sluijs, P.; Hull, M.; Webster, P.; Male, P.; Goud, B.; Mellman, I. The small gtp-binding protein rab4 controls an early sorting event on the endocytic pathway. Cell 1992, 70, 729–740, doi:10.1016/0092-8674(92)90307-X.
[29]
Ullrich, O.; Reinsch, S.; Urbe, S.; Zerial, M.; Parton, R.G. Rab11 regulates recycling through the pericentriolar recycling endosome. J. Cell. Biol. 1996, 135, 913–924, doi:10.1083/jcb.135.4.913.
[30]
Krogh, A.; Larsson, B.; von Heijne, G.; Sonnhammer, E.L. Predicting transmembrane protein topology with a hidden markov model: Application to complete genomes. J. Mol. Biol. 2001, 305, 567–580, doi:10.1006/jmbi.2000.4315.
[31]
Bendtsen, J.D.; Nielsen, H.; von Heijne, G.; Brunak, S. Improved prediction of signal peptides: Signalp 3.0. J. Mol. Biol. 2004, 340, 783–795, doi:10.1016/j.jmb.2004.05.028.
[32]
Mulder, N.J.; Apweiler, R.; Attwood, T.K.; Bairoch, A.; Bateman, A.; Binns, D.; Bork, P.; Buillard, V.; Cerutti, L.; Copley, R.; et al. New developments in the interpro database. Nucleic. Acids Res. 2007, 35, D224–D228, doi:10.1093/nar/gkl841.
[33]
Mulder, N.J.; Apweiler, R.; Attwood, T.K.; Bairoch, A.; Bateman, A.; Binns, D.; Bradley, P.; Bork, P.; Bucher, P.; Cerutti, L.; et al. Interpro, progress and status in 2005. Nucleic. Acids Res. 2005, 33, D201–D205, doi:10.1093/nar/gki158.
Martin, S.; Driessen, K.; Nixon, S.J.; Zerial, M.; Parton, R.G. Regulated localization of rab18 to lipid droplets: Effects of lipolytic stimulation and inhibition of lipid droplet catabolism. J. Biol. Chem. 2005, 280, 42325–42335, doi:10.1074/jbc.M506651200.
Ang, A.L.; Taguchi, T.; Francis, S.; Folsch, H.; Murrells, L.J.; Pypaert, M.; Warren, G.; Mellman, I. Recycling endosomes can serve as intermediates during transport from the golgi to the plasma membrane of mdck cells. J. Cell. Biol. 2004, 167, 531–543, doi:10.1083/jcb.200408165.
[43]
Lock, J.G.; Stow, J.L. Rab11 in recycling endosomes regulates the sorting and basolateral transport of e-cadherin. Mol. Biol. Cell. 2005, 16, 1744–1755, doi:10.1091/mbc.E04-10-0867.
[44]
Murray, R.Z.; Kay, J.G.; Sangermani, D.G.; Stow, J.L. A role for the phagosome in cytokine secretion. Science 2005, 310, 1492–1495, doi:10.1126/science.1120225.
[45]
Leung, S.M.; Rojas, R.; Maples, C.; Flynn, C.; Ruiz, W.G.; Jou, T.S.; Apodaca, G. Modulation of endocytic traffic in polarized madin-darby canine kidney cells by the small gtpase rhoa. Mol. Biol. Cell. 1999, 10, 4369–4384.
[46]
D'Souza-Schorey, C.; van Donselaar, E.; Hsu, V.W.; Yang, C.; Stahl, P.D.; Peters, P.J. Arf6 targets recycling vesicles to the plasma membrane: Insights from an ultrastructural investigation. J. Cell. Biol. 1998, 140, 603–616, doi:10.1083/jcb.140.3.603.
[47]
Prigent, M.; Dubois, T.; Raposo, G.; Derrien, V.; Tenza, D.; Rosse, C.; Camonis, J.; Chavrier, P. Arf6 controls post-endocytic recycling through its downstream exocyst complex effector. J. Cell. Biol. 2003, 163, 1111–1121, doi:10.1083/jcb.200305029.
D'Souza-Schorey, C.; Boshans, R.L.; McDonough, M.; Stahl, P.D.; Van Aelst, L. A role for por1, a rac1-interacting protein, in arf6-mediated cytoskeletal rearrangements. EMBO J. 1997, 16, 5445–5454, doi:10.1093/emboj/16.17.5445.
[50]
Niedergang, F.; Colucci-Guyon, E.; Dubois, T.; Raposo, G.; Chavrier, P. Adp ribosylation factor 6 is activated and controls membrane delivery during phagocytosis in macrophages. J. Cell. Biol. 2003, 161, 1143–1150, doi:10.1083/jcb.200210069.
[51]
Radhakrishna, H.; Klausner, R.D.; Donaldson, J.G. Aluminum fluoride stimulates surface protrusions in cells overexpressing the arf6 gtpase. J. Cell. Biol. 1996, 134, 935–947, doi:10.1083/jcb.134.4.935.
[52]
Zhang, Q.; Cox, D.; Tseng, C.C.; Donaldson, J.G.; Greenberg, S. A requirement for arf6 in fcgamma receptor-mediated phagocytosis in macrophages. J. Biol. Chem. 1998, 273, 19977–19981, doi:10.1074/jbc.273.32.19977.