Multiple organelle-targeting signals in the N-terminal portion of peroxisomal membrane protein PMP70

Journal of Biochemistry

Volumn 147, Issue 4, 2010, Pages 581-590

  Iwashita, Shohei ^a   Tsuchida, Masashi ^a   Tsukuda, Miwa ^a   Yamashita, Yukari ^a   Emi, Yoshikazu ^a   Kida, Yuichiro ^a   Komori, Masayuki ^b   Kashiwayama, Yoshinori ^c   Imanaka, Tsuneo ^c   Sakaguchi, Masao ^a,b  

^a UNIVERSITY OF HYOGO   (Japan)

^b Osaka Prefecture University   (Japan)

^c UNIVERSITY OF TOYAMA   (Japan)

Author keywords

ABC transporter; Membrane protein; Peroxisome; Signal sequence; Topogenesis

Indexed keywords

AMINO ACID; ENHANCED GREEN FLUORESCENT PROTEIN; MEMBRANE PROTEIN; PEROXISOMAL MEMBRANE PROTEIN 70; UNCLASSIFIED DRUG;

AMINO TERMINAL SEQUENCE; ANIMAL CELL; ARTICLE; CELL ORGANELLE; CELL STRAIN COS1; CONTROLLED STUDY; ENDOPLASMIC RETICULUM; NONHUMAN; PEROXISOME; SIGNAL TRANSDUCTION;

AMINO ACID SEQUENCE; ANIMALS; ATP-BINDING CASSETTE TRANSPORTERS; CERCOPITHECUS AETHIOPS; COS CELLS; ENDOPLASMIC RETICULUM; GLYCOSYLATION; GREEN FLUORESCENT PROTEINS; HUMANS; HYDROPHOBICITY; INTRACELLULAR MEMBRANES; MICE; MICROSCOPY, FLUORESCENCE; MITOCHONDRIAL MEMBRANES; MOLECULAR SEQUENCE DATA; MUTANT PROTEINS; PEROXISOMES; PROTEASOME ENDOPEPTIDASE COMPLEX; PROTEIN INTERACTION DOMAINS AND MOTIFS; PROTEIN SORTING SIGNALS; PROTEIN TRANSPORT; RECOMBINANT FUSION PROTEINS;

EID: 77950604267     PISSN: 0021924X     EISSN: 17562651     Source Type: Journal    
DOI: 10.1093/jb/mvp205     Document Type: Article

References (36)

1. Sakaguchi, M., Tomiyoshi, R., Kuroiwa, T., Mihara, K., and Omura, T. (1992) Functions of signal and signalanchor sequences are determined by the balance between the hydrophobic segment and the N-terminal charge. Proc. Natl Acad. Sci. USA 89, 16-19
2. Kida, Y., Morimoto, F., Mihara, K., and Sakaguchi, M. (2006) Function of positive charges following signalanchor sequences during translocation of the N-terminal domain. J. Biol. Chem. 281, 1152-1158
3. Sakaguchi, M. (2002) Autonomous and heteronomous positioning of transmembrane segments in multispanning membrane protein. Biochem. Biophys. Res. Commun. 296, 1-4
4. Kida, Y., Mihara, K., and Sakaguchi, M. (2005) Translocation of a long amino-terminal domain through ER membrane by following signal-anchor sequence. EMBO J. 24, 3202-3213
5. Kida, Y., Morimoto, F., and Sakaguchi, M. (2007) Two translocating hydrophilic segments of a nascent chain span the ER membrane during multispanning protein topogenesis. J. Cell Biol. 179, 1441-1452
6. Sadlish, H., Pitonzo, D., Johnson, A.E., and Skach, W.R. (2005) Sequential triage of transmembrane segments by Sec61alpha during biogenesis of a native multispanning membrane protein. Nat. Struct. Mol. Biol. 12, 879-878
7. Skach, W.R. (2009) Cellular mechanisms of membrane protein folding. Nat. Struct. Mol. Biol. 16, 606-612
8. Tusnády, G.E., Sarkadi, B., Simon, I., and Váradi, A. (2006) Membrane topology of human ABC proteins. FEBS Lett. 580, 1017-1022
9. Shirihai, O.S., Gregory, T., Yu, C., Orkin, S.H., and Weiss, M.J. (2000) ABC-me: a novel mitochondrial transporter induced by GATA-1 during erythroid differentiation. EMBO J. 19, 2492-2502
10. Graf, S.A., Haigh, S.E., Corson, E.D., and Shirihai, O.S. (2004) Targeting, import, and dimerization of a mammalian mitochondrial ATP binding cassette (ABC) transporter, ABCB10 (ABC-me). J. Biol. Chem. 279, 42954-42963
11. Miyazaki, E., Kida, Y., Mihara, K., and Sakaguchi, M. (2005) Switching the sorting mode of membrane proteins from cotranslational endoplasmic reticulum targeting to posttranslational mitochondrial import. Mol. Biol. Cell 16, 1785-1799
12. Honsho, M. and Fujiki, Y. (2001) Topogenesis of peroxisomal membrane protein requires a short, positively charged intervening-loop sequence and flanking hydrophobic segments. Study using human membrane protein PMP34. J. Biol. Chem. 276, 9375-9382
13. Jones, J.M., Morrell, J.C., and Gould, S.J. (2001) Multiple distinct targeting signals in integral peroxisomal membrane proteins. J. Cell Biol. 153, 1141-1150
14. Rottensteiner, H., Kramer, A., Lorenzen, S., Stein, K., Landgraf, C., Volkmer-Engert, R., and Erdmann, R. (2004) Peroxisomal membrane proteins contain common Pex19p-binding sites that are an integral part of their targeting signals. Mol. Biol. Cell 15, 3406-3417
15. Fransen, M., Wylin, T., Brees, C., Mannaerts, G.P., and Van Veldhoven, P.P. (2001) Human pex19p binds peroxisomal integral membrane proteins at regions distinct from their sorting sequences. Mol. Cell. Biol. 21, 4413-4424
16. Halbach, A., Lorenzen, S., Landgraf, C., Volkmer- Engert, R., Erdmann, R., and Rottensteiner, H. (2005) Function of the PEX19-binding site of human adrenoleukodystrophy protein as targeting motif in man and yeast. PMP targeting is evolutionarily conserved. J. Biol. Chem. 280, 21176-21182
17. Sacksteder, K.A., Jones, J.M., South, S.T., Li, X., Liu, Y., and Gould, S.J. (2000) PEX19 binds multiple peroxisomal membrane proteins, is predominantly cytoplasmic, and is required for peroxisome membrane synthesis. J. Cell Biol. 148, 931-944
18. Kikuchi, M., Hatano, N., Yokota, S., Shimozawa, N., Imanaka, T., and Taniguchi, H. (2004) Proteomic analysis of rat liver peroxisome: presence of peroxisomespecific isozyme of Lon protease. J. Biol. Chem. 279, 421-428
19. Kashiwayama, Y., Asahina, K., Shibata, H., Morita, M., Muntau, A.C., Roscher, A.A., Wanders, R.J., Shimozawa, N., Sakaguchi, M., Kato, H., and Imanaka, T. (2005) Role of Pex19p in the Targeting of PMP70 to Peroxisome. Biochim. Biophys. Acta 1746, 116-128
20. Kashiwayama, Y., Asahina, K., Morita, M., and Imanaka, T. (2007) Hydrophobic regions adjacent to transmembrane domains 1 and 5 are important for the targeting of the 70-kDa peroxisomal membrane protein. J. Biol. Chem. 282, 33831-33844
21. Kinoshita, N., Ghaedi, K., Shimozawa, N., Wanders, R.J., Matsuzono, Y., Imanaka, T., Okumoto, K., Suzuki, Y., Kondo, N., and Fujiki, Y. (1998) Newly identified Chinese hamster ovary cell mutants are defective in biogenesis of peroxisomal membrane vesicles (Peroxisomal ghosts), representing a novel complementation group in mammals. J. Biol. Chem. 273, 24122-24130
22. Shimozawa, N., Tsukamoto, T., Nagase, T., Takemoto, Y., Koyama, N., Suzuki, Y., Komori, M., Osumi, T., Jeannette, G., Wanders, R.J., and Kondo, N. (2004) Identification of a new complementation group of the peroxisome biogenesis disorders and PEX14 as the mutated gene. Hum. Mutat. 23, 552-558
23. Miyazaki, E., Sakaguchi, M., Wakabayashi, S., Shigekawa, M., and Mihara, K. (2001) NHE6 protein possesses a signal peptide destined for endoplasmic reticulum membrane and localizes in secretory organelles of the cell. J. Biol. Chem. 276, 49221-49227
24. Otera, H., Ohsakaya, S., Nagaura, Z., Ishihara, N., and Mihara, K. (2005) Export of mitochondrial AIF in response to proapoptotic stimuli depends on processing at the intermembrane space. EMBO J. 24, 1375-1386
25. Kamijo, K., Kamijo, N., Ueno, I., Osumi, T., and Hashimoto, T. (1992) Nucleotide sequence of the human 70 kDa peroxisomal membrane protein: a member of ATP-binding cassette transporters. Biochim. Biophys. Acta 1129, 323-327
26. Kanki, T., Sakaguchi, M., Kitamura, A., Sato, T., Mihara, K., and Hamasaki, N. (2002) The tenth membrane region of band 3 is initially exposed to the luminal side of the endoplasmic reticulum and then integrated into a partially folded band 3 intermediate. Biochemistry 41, 13973-13981
27. Kanaji, S., Iwahashi, J., Kida, Y., Sakaguchi, M., and Mihara, K. (2000) Characterization of the signal that directs Tom20 to the mitochondrial outer membrane. J. Cell Biol. 151, 277-288
28. Ikeda, M., Kida, Y., Ikushiro, S., and Sakaguchi, M. (2005) Manipulation of membrane protein topology on the endoplasmic reticulum by a specific ligand in living cells. J. Biochem. 138, 631-637
29. Fujiki, Y., Hubbard, A.L., Fowler, S., and Lazarow, P.B. (1982) Isolation intracellular membranes by means of sodium carbonate treatment: application to endoplasmic reticulum. J. Cell Biol. 93, 97-102
30. Sakaki, K., Sakaguchi, M., Ota, K., and Mihara, K. (1999) Membrane perturbing factor in reticulocyte lysate, which is transiently activated by proteases. FEBS Lett. 454, 345-348
31. Krishnamurthy, P.C., Du, G., Fukuda, Y., Sun, D., Sampath, J., Mercer, K.E., Wang, J., Sosa-Pineda, B., Murti, K.G., and Schuetz, J.D. (2006) Identification of a mammalian mitochondrial porphyrin transporter. Nature 443, 586-589
32. Tsuchida, M., Emi, Y., Kida, Y., and Sakaguchi, M. (2008) Human ABC transporter isoform B6 (ABCB6) localizes primarily in the Golgi apparatus. Biochem. Biophys. Res. Commun. 369, 369-375
33. Jalil, Y.A., Ritz, V., Jakimenko, A., Schmitz-Salue, C., Siebert, H., Awuah, D., Kotthaus, A., Kietzmann, T., Ziemann, C., and Hirsch-Ernst, K.I. (2008) Vesicular localization of the rat ATP-binding cassette half-transporter rAbcb6. Am. J. Physiol. Cell Physiol. 294, 579-590
34. Kashiwayama, Y., Seki, M., Yasui, A., Murasaki, Y., Morita, M., Yamashita, Y., Sakaguchi, M., Tanaka, Y., and Imanaka, T. (2009) 70-kDa peroxisomal membrane protein related protein (P70R/ABCD4) localizes to endoplasmic reticulum not peroxisomes, and NH2-terminal hydrophobic property determines the subcellular localization of ABC subfamily D proteins. Exp. Cell Res. 315, 199-205
35. Brett, C.L., Wei, Y., Donowitz, M., and Rao, R. (2002) Human Na(+)/H(+) exchanger isoform 6 is found in recycling endosomes of cells, not in mitochondria. Am. J. Physiol. Cell Physiol. 282, 1031-1041
36. Nakamura, N., Tanaka, S., Teko, Y., Mitsui, K., and Kanazawa, H. (2005) Four Na+/H+ exchanger isoforms are distributed to Golgi and post-Golgi compartments and are involved in organelle pH regulation. J. Biol. Chem. 280, 1561-1572