Distribution and trafficking of MPR300 is normal in cells with cholesterol accumulated in late endocytic compartments: Evidence for early endosome-to-TGN trafficking of MPR300

Journal of Lipid Research

Volumn 44, Issue 10, 2003, Pages 1821-1832

  Umeda, Atsushi ^a   Fujita, Hideaki ^a   Kuronita, Toshio ^a   Hirosako, Kaori ^a   Himeno, Masaru ^a   Tanaka, Yoshitaka ^a  

^a KYUSHU UNIVERSITY   (Japan)

Author keywords

Cation independent mannose 6 phosphate IGF II receptor; Endosomes; Intracellular trafficking; Lysosomes; Niemann Pick type C fibroblasts; trans Golgi network

Indexed keywords

3BETA (2 DIETHYLAMINOETHOXY)ANDROST 5 EN 17 ONE; CATHEPSIN D; CHLOROQUINE; CHOLESTEROL; LYSOSOME ASSOCIATED MEMBRANE PROTEIN 2; MPR 300 PROTEIN; PROTEIN; TRANSFERRIN; UNCLASSIFIED DRUG;

ARTICLE; CELL COMPARTMENTALIZATION; CELL STRAIN; CHOLESTEROL METABOLISM; CHOLESTEROL TRANSPORT; CONTROLLED STUDY; ENDOCYTOSIS; ENDOSOME; ENZYME ACTIVITY; FIBROBLAST; GOLGI COMPLEX; HUMAN; HUMAN CELL; INTERNALIZATION; INTRACELLULAR TRANSPORT; LYSOSOME; MEMBRANE TRANSPORT; NIEMANN PICK TYPE C FIBROBLAST; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN LOCALIZATION; PROTEIN TARGETING; PROTEIN TRANSPORT;

EID: 0242322493     PISSN: 00222275     EISSN: None     Source Type: Journal    
DOI: 10.1194/jlr.M300153-JLR200     Document Type: Article

References (56)

1. Ludwig, T., H. Munier-Lehmann, U. Bauer, M. Hollinshead, C. Ovitt, P. Lobel, and B. Hoflack. 1994. Differential sorting of lysosomal enzymes in mannose 6-phosphate receptor-deficient fibroblasts. EMBO J. 13: 3430-3437.
2. Pohlmann, R., M. Wendland, C. Boeker, and K. von Figura. 1995. The two mannose 6-phosphate receptors transport distinct complements of lysosomal enzymes. J. Biol. Chem. 270: 27311-27318.
3. Kornfeld, S. 1992. Structure and function of the mannose 6-phosphate/insulinlike growth factor II receptors. Annu. Rev. Biochem. 61: 307-330.
4. Hille-Rehfeld, A. 1995. Mannose 6-phosphate receptors in sorting and transport of lysosomal enzymes. Biochim. Biophys. Acta. 1241: 177-194.
5. Dell'Angelica, E. C., and G. S. Payne. 2001. Intracellular cycling of lysosomal enzyme receptors: cytoplasmic tails' tales. Cell. 106: 395-398.
6. Boehm, M., and J. S. Bonifacino. 2001. Adaptins: the final recount. Mol. Biol. Cell. 12: 2907-2920.
7. Puertollano, R., R. C. Aguilar, I. Gorshkova, R.J. Crouch, and J. S. Bonifacino. 2001. Sorting of mannose 6-phosphate receptors mediated by the GGAs. Science. 292: 1712-1716.
8. Zhu, Y., B. Doray, A. Poussu, V-P. Lehto, and S. Kornfeld. 2001. Binding of GGA2 to the lysosomal enzyme sorting motif of the mannose 6-phosphate receptor. Science. 292: 1716-1718.
9. Crump, C. M., Y. Xiang, L. Thomas, F. Gu, C. Austin, S. A. Tooze, and G. Thomas. 2001. PACS-1 binding to adaptors is required for acidic cluster motif-mediated protein traffic. EMBO J. 20: 2191-2201.
10. Wan, L., S. S. Molloy, L. Thomas, G. Liu, Y. Xiang, S. L. Rybak, and G. Thomas. 1998. PACS-1 defines a novel gene family of cytosolic sorting proteins required for trans-Golgi network localization. Cell. 94: 205-216.
11. Meyer, C., D. Zizioli, S. Lausmann, E-L. Eskelinen, J. Hamann, P. Saftig, K. von Figura, and P. Schu. 2000. μ1A-adaptin-deficient mice: lethality, loss of AP-1 binding and rerouting of mannose 6-phosphate receptors. EMBO J. 19: 2193-2203.
12. Diaz, E., and S. R. Pfeffer. 1998. TIP47: a cargo selection device for mannose 6-phosphate receptor trafficking. Cell. 93: 433-443.
13. Carroll, K. S., J. Hanna, I. Simon, J. Krise, P. Barbero, and S. R. Pfeffer. 2001. Role of rab9 GTPase in facilitating receptor recruitment by TIP47. Science. 292: 1373-1376.
14. Kobayashi, T., M-H. Beuchat, M. Lindsay, S. Frias, R. D. Palmiter, H. Sakuraba, R. G. Parton, and J. Gruenberg. 1999. Late endosomal membranes rich in lysobisphosphatidic acid regulate cholesterol transport. Nat. Cell Biol. 1: 113-118.
15. Ohashi, M., I. Miwako, A. Yamamoto, and K. Nagayama. 2000. Arrested late endosome-lysosome intermediate aggregate observed in a Chinese hamster ovary cell mutant, LEX2, isolated by repeated flow-cytometric cell sorting. J. Cell Sci. 113: 2187-2205.
16. Miwako, I., A. Yamamoto, T. Kitamura, K. Nagayama, and M. Ohashi. 2001. Cholesterol requirement for cation-independent mannose 6-phosphate receptor exit from multivesicular late endosomes to the Golgi. J. Cell Sci. 114: 1765-1776.
17. Ory, D. S. 2000. Niemann-Pick type C: a disorder of cellular cholesterol trafficking. Biochim. Biophys. Acta. 1529: 331-339.
18. Liscum, L. 2000. Niemann-Pick type C mutations cause lipid traffic jam. Traffic. 1: 218-225.
19. Brown, W. J., D. B. DeWald, S. D. Emr, H. Plutner, and W. E. Balch. 1995. Role for phosphatidylinositol 3-kinase in the sorting and transport of newly synthesized lysosomal enzymes in mammalian cells. J. Cell Biol. 130: 781-796.
20. Davidson, H. W. 1995. Wortmannin causes mistargeting of procathepsin D. Evidence for the involvement of a phosphatidylinositol 3-kinase in vesicle transport to lysosomes. J. Cell Biol. 130: 797-805.
21. Row, P. E., B. J. Reaves, J. Domin, J. P. Luzio, and H. W. Davidson. 2001. Overexpression of a rat kinase-deficient phosphatidylinositide 3-kinase, Vps34p, inhibits cathepsin D maturation. Biochem. J. 353: 655-661.
22. Kuronita, T., E-L. Eskelinen, H. Fujita, P. Saftig, M. Himeno, and Y. Tanaka. 2002. A role for the lysosomal membrane protein LGP85 in the biogenesis and maintenance of endosomal and lysosomal morphology. J. Cell Sci. 115: 4117-4131.
23. Sahagian, G. G., J. Distler, and G. W. Jourdian. 1982. Membrane receptor for phosphomannosyl residues. Methods Enzymol. 83: 392-396.
24. Köster, A., K. von Figura, and R. Pohlmann. 1994. Mistargeting of lysosomal enzymes in Mr 46000 mannose 6-phosphate receptor-deficient mice is compensated by carbohydrate-specific endocytotic receptors. Eur. J. Biochem. 224: 685-689.
25. Porter, M. T., A. L. Fluharty, and H. Kihara. 1969. Metachromatic leukodystrophy: arylsulfatase-A deficiency in skin fibroblast cultures. Proc. Natl. Acad. Sci. USA. 62: 887-891.
26. Barrett, A. J., and H. Kirschke. 1981. Cathepsin B, cathepsin H, and cathepsin L. Methods Enzymol. 80: 535-561.
27. Tanaka, Y., R. Tanaka, T. Kawabata, Y. Noguchi, and M. Himeno. 2000. Lysosomal cysteine protease, cathepsin B, is targeted to lysosomes by the mannose 6-phosphate-independent pathway in rat hepatocytes: site-specific phosphorylation in oligosaccharides of the proregion. J. Biochem. 128: 39-48.
28. Tanaka, Y., R. Tanaka, and M. Himeno. 2000. Lysosomal cysteine protease, cathepsin H, is targeted to lysosomes by the mannose 6-phosphate-independent system in rat hepatocytes. Biol. Pharm. Bull. 23: 805-809.
29. Laemmli, U. K. 1970. Cleavage of structural protein during the assembly of the head of bacteriophage T4. Nature. 227: 680-685.
30. Besley, G. T. N., and S. E. Moss. 1983. Studies of sphingomyelinase and β-glucosidase activities in Niemann-Pick disease variants: phosphodiesterase activities measured with natural and artificial substrates. Biochim. Biophys. Acta. 752: 54-64.
31. Thomas, G. H., C. M. Tuck-Muller, C. S. Miller, and L. W. Reynolds. 1989. Correction of sphingomyelinase deficiency in Niemann-Pick type C fibroblasts by removal of lipoprotein fraction from culture media. J. Inherit. Metab. Dis. 12: 139-151.
32. Rohrer, J., A. Schweizer, K. F. Johnson, and S. Kornfeld. 1995. A determinant in the cytoplasmic tail of the cation-dependent mannose 6-phosphate receptor prevents trafficking to lysosomes. J. Cell Biol. 130: 1297-1306.
33. Liscum, L., and J. R. Faust. 1989. The intracellular transport of low density, lipoprotein-derived cholesterol is inhibited in Chinese hamster ovary cells cultured with 3-beta-[2-(diethylamino)ethoxy] androst-5-en-17-one. J. Biol. Chem. 264: 11796-11806.
34. Neufeld, E. B., M. Wastney, S. Patel, S. Suresh, A. M. Cooney, N.K. Dwyer, C. F. Roff, K. Ohno, J. A. Morris, E. D. Carstea, J. P. Incardona, J. F. Strauss III, M. T. Vanier, M. C. Patterson, R. O. Brady, P. G. Pentchev, and E. J. Blanchette-Mackie. 1999. The Niemann-Pick C1 protein resides in a vesicular compartment linked to retrograde transport of multiple lysosomal cargo. J. Biol. Chem. 274: 9627-9635.
35. Cruz, J. C., S. Sugii, C. Yu, and T. Y. Chang. 2000. Role of Niemann-Pick type C1 protein in intracellular trafficking of low density lipoprotein-derived cholesterol. J. Biol. Chem. 275: 4013-4021.
36. Lange, Y., J. Ye, M. Rigney, and T. Steck. 2000. Cholesterol movement in Niemann-Pick type C cells and in cells treated with amphiphiles. J. Biol. Chem. 275: 17468-17475.
37. Reaves, B. J., G. Banting, and J. P. Luzio. 1998. Lumenal and transmembrane domains play a role in sorting type I membrane proteins on endocytic pathways. Mol. Biol. Cell. 9: 1107-1122.
38. Rous, B. A., B. J. Reaves, G. Ihrke, J. A. G. Briggs, S. R. Gray, D. J. Stephens, G. Banting, and J. P. Luzio. 2002. Role of adaptor complex AP-3 in targeting wild-type and mutated CD63 to lysosomes. Mol. Biol. Cell. 13: 1071-1082.
39. Frolov, A., K. Srivastava, D. Daphna-Iken, L. M. Traub, J. E. Schaffer, and D. S. Ory. 2001. Cholesterol overload promotes morphogenesis of a Niemann-Pick C (NPC)-like compartment independent of inhibition of NPC1 or HE1/NPC2 function. J. Biol. Chem. 276: 46414-46426.
40. Kobayashi, T., E. Stang, K. S. Fang, P. de Moerloose, R. G. Parton, and J. Gruenberg. 1998. A lipid associated with the antiphospholipid syndrome regulates endosome structure and function. Nature. 392: 193-197.
41. Ko, D. C., M. D. Gordon, G. J. Jin, and M. P. Scott. 2001. Dynamic movements of organelles containing Niemann-Pick C1 protein: NPC1 involvement in late endocytic events. Mol. Biol. Cell. 12: 601-614.
42. Higgins, M. E., J. P. Davies, F. W. Chen, and Y. A. Ioannou. 1999. Niemann-Pick C1 is a late endosome-resident protein that transiently associates with lysosomes and the trans-Golgi nerwork. Mol. Genet. Metab. 68: 1-13.
43. Zhang, M., N. K. Dwyer, D. C. Love, A. Cooney, M. Comly, E. B. Neufeld, P. G. Pentchev, E. J. Blanchette-Mackie, and J. A. Hanover. 2001. Cessation of rapid late endosomal tubulovesicular trafficking in Niemann-Pick type C1 disease. Proc. Natl. Acad. Sci. USA. 98: 4466-4471.
44. Zhang, M., N. K. Dwyer, E. B. Neufeld, D. C. Love, A. Cooney, M. Comly, S. Patel, H. Watari, J. F. Strauss III, P. G. Pentchev, J. A. Hanover, and E. J. Blanchette-Mackie. 2001. Sterol-modulated glycolipid sorting occurs in Niemann-Pick C1 late endosomes. J. Biol. Chem. 276: 3417-3425.
45. Choudhury, A., M. Dominguez, V. Puri, D. K. Sharma, K. Narita, C. L. Wheatley, D. L. Marks, and R. E. Pagano. 2002. Rab proteins mediate Golgi transport of caveola-internalized glycosphingolipids and correct lipid trafficking in Niemann-Pick C cells. J. Clin. Invest. 109: 1541-1550.
46. Walter, M., J. P. Davies, and Y. A. Ioannou. 2003. Telomerase immortalization upregulates Rab9 expression and restores LDL cholesterol egress from Niemann-Pick C1 late endosomes. J. Lipid Res. 44: 243-253.
47. Hirst, J., and M. S. Robinson. 1998. Clathrin and adaptors. Biochim. Biophys. Acta. 1404: 173-193.
48. Futter, C. E., A. Gibson, E. H. Allchin, S. Maxwell, L. J. Ruddock, G. Odorizzi, D. Domingo, I. S. Trowbridge, and C. R. Hopkins. 1998. In polarized MDCK cells basolateral vesicles arise from clathrin-γ-adaptin-coated domains on endosomal tubules. J. Cell Biol. 141: 611-623.
49. Bock, J. B., R. C. Lin, and R. H. Scheller. 1996. A new syntaxin family member implicated in targeting of intracellular transport vesicies. J. Chem. 271: 17961-17965.
50. Bock, J. B., J. Klumperman, S. Davanger, and R. H. Scheller. 1997. Syntaxin 6 functions in trans-Golgi network vesicle trafficking. Mol. Biol. Cell. 8: 1261-1271.
51. Ghosh, R. N., W. G. Mallet, T. T. Soe, T. E. McGraw, and F. R. Maxfield. 1998. An endocytosed TGN38 chimeric protein is delivered to the TGN after trafficking through the endocytic recycling compartment in CHO cells. J. Cell Biol. 142: 923-936.
52. Mallard, F., D. Tenza, C. Antony, J. Salamero, B. Goud, and L. Johannes. 1998. Direct pathway from early/recycling endosomes to the Golgi apparatus revealed through the study of Shiga toxin B-fragment transport. J. Cell Biol. 143: 973-990.
53. Mallard, F., B. L. Tang, T. Galli, D. Tenza, A. Saint-Pol, X. Yue, C. Antony, W. Hong, B. Goud, and L. Johannes. 2002. Early/recycling endosomes-to-TGN transport involves two SNARE complexes and a Rab6 isoform. J. Cell Biol. 156: 653-664.
54. Hirst, J., C. E. Futter, and C. R. Hopkins. 1998. The kinetics of mannose 6-phosphate receptor trafficking in the endocytic pathway in Hep-2 cells: the receptor enters and rapidly leaves multivesicular endosomes without accumulating in a prelysosomal compartment. Mol. Biol. Cell. 9: 809-816.
55. Waguri, S., F. Dewitte, R. Le Borgne, Y. Rouillé, Y. Uchiyama, J-F. Dubremetz, and B. Hoflack. 2003. Visualization of TGN to endosome trafficking through fluorescently labeled MPR and AP-1 in living cells. Mol. Biol. Cell. 14: 142-155.
56. Griffiths, G., B. Hoflack, K. Simons, I. Mellman, and S. Kornfeld. 1988. The mannose 6-phosphate receptor and the biogenesis of lysosomes. Cell. 52: 329-341.