The PC6B cytoplasmic domain contains two acidic clusters that direct sorting to distinct trans-Golgi network/endosomal compartments

Molecular Biology of the Cell

Volumn 11, Issue 4, 2000, Pages 1257-1273

  Xiang, Yang ^a   Molloy, Sean S ^a   Thomas, Laurel ^a   Thomas, Gary ^a  

^a OREGON HEALTH AND SCIENCE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

FURIN; SERINE PROTEINASE;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CELLULAR DISTRIBUTION; CYTOPLASM; ENDOCYTOSIS; ENZYME ANALYSIS; ENZYME LOCALIZATION; GOLGI COMPLEX; MUTATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN TARGETING; RAT;

ANIMALIA; MAMMALIA;

EID: 0034077580     PISSN: 10591524     EISSN: None     Source Type: Journal    
DOI: 10.1091/mbc.11.4.1257     Document Type: Article

References (41)

1. Alconada, A., Bauer, U., and Hoflack, B. (1996). A tyrosine-based motif and a casein kinase II phosphorylation site regulate the intracellular trafficking of the varicella-zoster virus glycoprotein I, a protein localized in the trans-Golgi network. EMBO J. 15, 6096-6110.
2. Boker, C., von Figura, K., and Hille-Rehfeld, A. (1997). The carboxy-terminal peptides of 46 kDa and 300 kDa mannose 6-phosphate receptors share partial sequence homology and contain information for sorting in the early endosomal pathway. J. Cell Sci. 110, 1023-1032.
3. Bosshart, H., Humphrey, J., Deignan, E., Davidson, J., Drazba, J., Yuan, L., Oorschor, V., Peters, P.J., and Bonifacino, J.S. (1994). The cytoplasmic domain mediates localization of furin to the trans-Golgi network en route to the endosomal/lysosomal system. J. Cell Biol. 126, 1157-1172.
4. Bresnahan, P.A., Leduc, R., Thomas, L., Thorner, J., Gibson, H.L., Brake, A.J., Barr, P.J., and Thomas, G. (1990). Human fur gene encodes a yeast KEX2-like endoprotease that cleaves Pro-β-NGF in vivo. J. Cell Biol. 111, 2851-2859.
5. Chapman, R.E., and Munro, S. (1994). Retrieval of TGN proteins from the cell surface requires endosomal acidification. EMBO J. 13, 2305-2312.
6. Chen, H.J., Remmler, J., Delaney, J.C., Messner, D.J., and Lobel, P. (1993). Mutational analysis of the cation-independent mannose 6-phosphate/insulin-like growth factor II receptor: a consensus casein kinase II site followed by 2 leucines near the carboxyl terminus is important for intracellular targeting of lysosomal enzymes. J. Biol. Chem. 268, 22338-22346.
7. Cui, Y., Jean, F., Thomas, G., and Christian, J.L. (1998). BMP-4 is proteolytically activated by furin and/or PC6 during vertebrate embryonic development. EMBO J. 17, 4735-4743.
8. De Bie, I., Marcinkiewicz, M., Malide, D., Lazure, C., Nakayama, K., Bendayan, M., and Seidah, N.G. (1996). The isoforms of proprotein convertase PC5 are sorted to different subcellular compartments. J. Cell Biol. 135, 1261-1275.
9. Dittié, A.S., Thomas, L., Thomas, G., and Tooze, S.A. (1997). Interaction of furin in immature secretory granules from neuroendocrine cells with the AP-1 adaptor complex is modulated by casein kinase II phosphorylation. EMBO J. 16, 4859-4870.
10. Eng, F.J., Varlamov, O., and Fricker, L.D. (1999). Sequences within the cytoplasmic domain of Gp180/carboxypeptidase D mediate localization to the trans-Golgi network. Mol. Biol. Cell 10, 35-46.
11. Hayflick, J.S., Wolfgang, W.J., Forte, M.A., and Thomas, G. (1992). A unique Kex2-like endoprotease from Drosophila melanogaster is expressed in the central nervous system during early embryogenesis. J. Neurosci. 12, 705-717.
12. 1-Antitrypsin Portland, a bioengineered serpin highly selective for furin: application as an antipathogenic agent. Proc. Natl. Acad. Sci. USA 95, 7293-7298.
13. Jones, B.G., Thomas, L., Molloy, S.S., Thulin, C.D., Fry, M.D., Walsh, K.A., and Thomas, G. (1995). Intracellular trafficking of furin is modulated by the phosphorylation state of a casein kinase II site in its cytoplasmic tail. EMBO J. 14, 5869-5883.
14. Liu, G., Thomas, L., Warren, R.A., Enns, C.A., Cunningham, C.C., Hartwig, J.H., and Thomas, G. (1997). Cytoskeletal protein ABP-280 directs the intracellular trafficking of furin and modulates proprotein processing in the endocytic pathway. J. Cell Biol. 139, 1719-1733.
15. Marks, M.S., Ohno, H., Kirchhausen, T., and Bonifacino, J.S. (1997). Protein sorting by tyrosine-based signals. Trends Cell Biol. 7, 124-128.
16. Matter, K., Yamamoto, E.M., and Mellman, I. (1994). Structural requirements and sequence motifs for polarized sorting and endocytosis of LDL and Fc receptors in MDCK cells. J. Cell Biol. 126, 991-1004.
17. Mauxion, F., Le Borgne, R., Munier-Lehmann, H., and Hoflack, B. (1996). A casein kinase II phosphorylation site in the cytoplasmic domain of the cation-dependent mannose 6-phosphate receptor determines the high affinity interaction of the AP-1 Golgi assembly proteins with membranes. J. Biol. Chem. 271, 2171-2178.
18. Mbikay, M., et al. (1997). Impaired fertility in mice deficient for the testicular germ-cell protease PC4. Proc. Natl. Acad. Sci. USA 94, 6842-6846.
19. Milgram, S.L., Kho, S.T., Martin, G.V., Mains, R.E., and Eipper, B.A. (1997). Localization of integral membrane peptidylglycine alpha-amidating monooxygenase in neuroendocrine cells. J. Cell Sci. 110, 695-706.
20. Molloy, S.S., Anderson, E., Jean, F., and Thomas, G. (1999). Bicycling the furin pathway: from TGN localization to pathogen activation and embryogenesis. Trends Cell Biol. 9, 28-35.
21. Molloy, S.S., Thomas, L., Kamibayashi, C., Mumby, M.C., and Thomas, G. (1998). Regulation of endosome sorting by a specific PP2A isoform. J. Cell Biol. 142, 1399-1411.
22. Molloy, S.S., Thomas, L., VanSlyke, J.K., Stenberg, P.E., and Thomas, G. (1994). Intracellular trafficking and activation of the furin pro-protein convertase: localization to the TGN and recycling from the cell surface. EMBO J. 13, 18-33.
23. Nakagawa, T., Murakami, K., and Nakayama, K. (1993). Identification of an isoform with an extremely large Cys-rich region of PC6, a Kex2-like processing endoprotease. FEBS Lett. 327, 165-171.
24. Nakayama, K. (1997). Furin: a mammalian subtilisin/Kex2p-like endoprotease involved in processing of a wide variety of precursor proteins. Biochem. J. 327, 625-635.
25. Piguet, V., Wan, L., Borel, C., Mangasarian, A., Demaurex, N., Thomas, G., and Trono, D. (2000). HIV-1 Nef protein binds to the cellular protein PACS-1 to downregulate class I major histocompatibility complexes. Nat. Cell Biol. 2, 163-167.
26. Roebroek, A.J., Umans, L., Pauli, I.G., Robertson, E.J., van Leuven, F., van de Yen, W.J., and Constam, D.B. (1998). Failure of ventral closure and axial rotation in embryos lacking the proprotein convertase furin. Development 125, 4863-4876.
27. Sariola, M., Saraste, J., and Kuismanen, E. (1995). Communication of post-Golgi elements with early endocytic pathway: regulation of endoproteolytic cleavage of Semliki Forest virus p62 precursor. J. Cell Sci. 108, 2465-2475.
28. Schäfer, W., Stroh, A., Berghofer, S., Seiler, J., Vey, M., Kruse, M.L., Kern, H.F., Klenk, H.D., and Garten, W. (1995). Two independent targeting signals in the cytoplasmic domain determine trans-Golgi network localization and endosomal trafficking of the proprotein convertase furin. EMBO J. 14, 2424-2435.
29. Schweizer, A., Kornfeld, S., and Rohrer, J. (1997). Proper sorting of the cation-dependent mannose 6-phosphate receptor in endosomes depends on a pair of aromatic amino acids in its cytoplasmic tail. Proc. Natl. Acad. Sci. USA 94, 14471-14476.
30. Seidah, N.G., Benjannet, S., Pareek, S., Savaria, D., Hamelin, J., Goulet, B., Laliberte, J., Lazure, C., Chretien, M., and Murphy, R.A. (1996). Cellular processing of the nerve growth factor precursor by the mammalian pro-protein convertases. Biochem. J. 314, 951-960.
31. Seidah, N.G., Chretien, M., and Day, R. (1994). The family of subtilisin/kexin like pro-protein and pro-hormone convertases: divergent or shared functions. Biochimie 76, 197-209.
32. Simmen, T., Nobile, M., Bonifacino, J.S., and Hunziker, W. (1999). Cycling of furin occurs via the basolateral surface of MDCK cells and requires a phenylalanine-isoleucine motif together with an acidic amino acid cluster. Mol. Cell. Biol. 19, 3136-3144.
33. Steiner, D. (1998). The proprotein convertases. Curr. Opin. Chem. Biol. 2, 31-39.
34. Steiner, D.F., Smeekens, S.P., Ohagi, S., and Chan, S.J. (1992). The new enzymology of precursor processing endoproteases. J. Biol. Chem. 267, 23435-23438.
35. Takahashi, S., Nakagawa, T., Banno, T., Watanabe, T., Murakami, K., and Nakayama, K. (1995). Localization of furin to the trans-Golgi network and recycling from the cell surface involves Ser and Tyr residues within the cytoplasmic domain. J. Biol. Chem. 270, 28397-28401.
36. Thorne, B.A., Caton, L.W., and Thomas, G. (1989). Expression of mouse proopiomelanocortin in an insulinoma cell line: requirements for β-endorphin processing. J. Biol. Chem. 264, 3545-3552.
37. van de Loo, J.W., Creemers, J.W., Bright, N.A., Young, B.D., Roebroek, A.J., and Van de Ven, W.J. (1997). Biosynthesis, distinct post-translational modifications, and functional characterization of lymphoma proprotein convertase. J. Biol. Chem. 272, 27116-27123.
38. VanSlyke, J.K., Thomas, L., and Thomas, G. (1995). Use of vaccinia virus vectors to study neuropeptide processing. In: Peptidases and Neuropeptide Processing, vol. 23, ed. A.I. Smith, San Diego, CA: Academic Press, 45-64.
39. Voorhees, P., Deignan, E., van Donselaar, E., Humphrey, J., Marks, M.S., Peters, P.J., and Bonifacino, J.S. (1995). An acidic sequence within the cytoplasmic domain of furin functions as a determinant of trans-Golgi network localization and internalization from the cell surface. EMBO J. 14, 4961-4975.
40. Wan, L., Molloy, S.S., Thomas, L., Liu, G., Xiang, Y., Rybak, S.L., and Thomas, G. (1998). PACS-1 defines a novel gene family of cytosolic sorting proteins required for trans-Golgi network localization. Cell 94, 205-216.
41. Zhu, Z., Hao, Y., Gershon, M.D., Ambron, R.T., and Gershon, A.A. (1996). Targeting of glycoprotein 1 (gE) of varicella-zoster virus to the trans-Golgi network by an AYRV sequence and an acidic amino acid-rich patch in the cytosolic domain of the molecule. J. Virol. 70, 6563-6575.