Cholesterol level regulates endosome motility via rab proteins

Biophysical Journal

Volumn 94, Issue 4, 2008, Pages 1508-1520

  Chen, Hongtao ^a   Yang, Jun ^a   Low, Philip S ^a,b   Cheng, Ji Xin ^a,b,c  

^a PURDUE UNIVERSITY   (United States)

^b Purdue University   (United States)

^c PURDUE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CHOLESTEROL; MOLECULAR MOTOR; RAB PROTEIN;

ARTICLE; ENDOCYTOSIS; ENDOSOME; HELA CELL; HUMAN; METABOLISM; PHYSIOLOGY;

CHOLESTEROL; ENDOCYTOSIS; ENDOSOMES; HELA CELLS; HUMANS; MOLECULAR MOTOR PROTEINS; RAB GTP-BINDING PROTEINS;

EID: 38949156866     PISSN: 00063495     EISSN: 15420086     Source Type: Journal    
DOI: 10.1529/biophysj.106.099366     Document Type: Article

References (70)

1. Mukherjee, S., R. N. Ghosh, and F. R. Maxfield. 1997. Endocytosis. Physiol. Rev. 77:759-803.
2. Helms, J. B., and C. Zurzolo. 2004. Lipids as targeting signals: lipid rafts and intracellular trafficking. Traffic. 5:247-254.
3. Maxfield, F. R., and D. Wustner. 2002. Intracellular cholesterol transport. J. Clin. Invest. 110:891-898.
4. Gruenberg, J. 2001. The endocytic pathway: a mosaic of domains. Nat. Rev. Mol. Cell Biol. 2:721-730.
5. Chatterjee, S., and S. Mayor. 2001. The GPI-anchor and protein sorting. Cell. Mol. Life Sci. 58:1969-1987.
6. Fivaz, M., F. Vilbois, S. Thurnheer, C. Pasquali, L. Abrami, P. E. Bickel, R. G. Parton, and F. G. van der Goot. 2002. Differential sorting and fate of endocytosed GPI-anchored proteins. EMBO J. 21:3989-4000.
7. Abrami, L., S. Liu, P. Cosson, S. H. Leppla, and F. G. van der Goot. 2003. Anthrax toxin triggers endocytosis of its receptor via a lipid raftmediated clathrin-dependent process. J. Cell Biol. 160:321-328.
8. Zhang, M., N. K. Dwyer, D. C. Love, A. Cooney, M. Comly, E. 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.
9. Karten, B. A., D. E. Vance, R. B. Campenot, and J. E. Vance. 2003. Trafficking of cholesterol from cell bodies to distal axons in Niemann Pick C1-deficient neurons. J. Biol. Chem. 278:4168-4175.
10. Pagano, R. E. 2003. Endocytic trafficking of glycosphingolipids in sphingolipid storage diseases. Philos. Trans. R. Soc. Lond. B Biol. Sci. 358:885-891.
11. Kamen, B. A., M. T. Wang, A. J. Streckfuss, X. Peryea, and R. G. Anderson. 1988. Deliveryoffolates to the cytoplasm of MA104 cells is mediated by a surface membrane receptor that recycles. J. Biol. Chem. 263:13602-13609.
12. Kamen, B. A., and A. K. Smith. 2004. A review of folate receptor alpha cycling and 5-methyltetrahydrofolate accumulation with an emphasis on cell models in vitro. Adv. Drug Deliv. Rev. 56:1085-1097.
13. Mayor, S., and H. Riezman. 2004. Sorting GPI-anchored proteins. Nat. Rev. Mol. Cell Biol. 5:110-120.
14. Varma, R., and S. Mayor. 1998. GPI-anchored proteins are organized in submicron domains at the cell surface. Nature. 394:798-801.
15. Ikonen, E. 2001. Roles of lipid rafts in membrane transport. Curr. Opin. Cell Biol. 13:470-477.
16. Rothberg, K. G., Y. S. Ying, J. F. Kolhouse, B. A. Kamen, and R. G. Anderson. 1990. The glycophospholipid-linked folate receptor internalizes folate without entering the clathrin-coated pit endocytic pathway. J. Cell Biol. 110:637-649.
17. Anderson, R. G., B. A. Kamen, K. G. Romberg, and S. W. Lacey. 1992. Potocytosis: sequestration and transport of small molecules by caveolae. Science. 255:410-411.
18. Mayor, S., K. G. Romberg, and F. R. Maxfield. 1994. Sequestration of GPI-anchored proteins in caveolae triggered by cross-linking. Science. 264:1948-1951.
19. Wu, M., J. Fan, W. Gunning, and M. Ratnam. 1997. Clustering of GPI-anchored folate receptor independent of both cross-linking and association with caveolin. J. Membr. Biol. 159:137-147.
20. Ritter, T. E., O. Fajardo, H. Matsue, R. G. W. Anderson, and S. W. Lacey. 1995. Folate receptors targeted to clathrin-coated pits cannot regulate vitamin uptake. Proc. Natl. Acad. Sci. USA. 92:3824-3828.
21. Sabharanjak, S., P. Sharma, R. G. Parton, and S. Mayor. 2002. GPI-anchored proteins are delivered to recycling endosomes via a distinct cdc42-regulated, clathrin-independent pinocytic pathway. Dev. Cell. 2:411-423.
22. Mayor, S., S. Sabharanjak, and F. R. Maxfield. 1998. Cholesterol- dependent retention of GPI-anchored proteins in endosomes. EMBO J. 17:4626-4638.
23. Turek, J. J., C. P. Leamon, and P. S. Low. 1993. Endocytosis of folate-protein conjugates: ultrastructural localization in KB cells. J. Cell Sci. 106:423-430.
24. Yang, J., H. Chen, I. R. Vlahov, J.-X. Cheng, and P. S. Low. 2006. Evaluation of disulfide reduction during receptor-mediated endocytosis by using FRET imaging. Proc. Natl. Acad. Sci. USA. 103:13872-13877.
25. Paulos, C. M., J. A. Reddy, C. P. Leamon, M. J. Turk, and P. S. Low. 2004. Ligand binding and kinetics of folate receptor recycling in vivo: impact on receptor-mediated drug delivery. Mol. Pharmacol. 66: 1406-1414.
26. H folate receptor-containing endosomes and the rate of hydrolysis of internalized acid-labile folate-drug conjugates. J. Pharmacol. Exp. Ther. 321:462-468.
27. Chatterjee, S., E. R. Smith, K. Hanada, V. L. Stevens, and S. Mayor. 2001. GPI anchoring leads to sphingolipid-dependent retention of endocytosed proteins in the recycling endosomal compartment. EMBO J. 20:1583-1592.
28. Saxton, M. J., and K. Jacobson. 1997. Single-particle tracking: applications to membrane dynamics. Annu. Rev. Biophys. Biomol. Struct. 26:373-399.
29. Lakadamyali, M., M. J. Rust, H. P. Babcock, and X. Zhuang. 2003. Visualizing infection of individual influenza viruses. Proc. Natl. Acad. Sci. USA. 100:9280-9285.
30. Yvon, A.-M. C., P. Wadsworth, and M. A. Jordan. 1999. Taxol suppresses dynamics of individual microtubules in living human tumor cells. Mol. Biol. Cell. 10:947-959.
31. Crocker, J. C., and D. G. Grier. 1996. Methods of digital video microscopy for colloidal studies. J. Colloid Interface Sci. 179:298-310.
32. Johnson, L. S., K. W. Dunn, B. Pytowski, and T. E. McGraw. 1993. Endosome acidification and receptor trafficking: bafilomycin A1 slows receptor externalization by a mechanism involving the receptor's internalization motif. Mol. Biol. Cell. 4:1251-1266.
33. Lin, S. X., G. G. Gundersen, and F. R. Maxfield. 2002. Export from pericentriolar endocytic recycling compartment to cell surface depends on stable, detyrosinated (Glu) microtubules and kinesin. Mol. Biol. Cell. 13:96-109.
34. Mukherjee, S., X. Zha, I. Tabas, and F. R. Maxfield. 1998. Cholesterol distribution in living cells: fluorescence imaging using dehydroergosterol as a fluorescent cholesterol analog. Biophys. J. 75:1915-1925.
35. Gagescu, R., N. Demaurex, R. G. Parton, W. Hunziker, L. A. Huber, and J. Gruenberg. 2000. The recycling endosome of Madin-Darby canine kidney cells is a mildly acidic compartment rich in raft components. Mol. Biol. Cell. 11:2775-2791.
36. Murray, J. W., and A. W. Wolkoff. 2003. Roles of the cytoskeleton and motor proteins in endocytic sorting. Adv. Drug Deliv. Rev. 55: 1385-1403.
37. Fletcher, L. M., G. I. Welsh, P. B. Oatey, and J. M. Tavaré. 2000. Role for the microtubule cytoskeleton in GLUT4 vesicle trafficking and in the regulation ofinsulin-stimulated glucose uptake. Biochem. J. 352:267-276.
38. Lewis, C. M., A. K. Smith, and B. A. Kamen. 1998. Receptor-mediated folate uptake is positively regulated by disruption of the actin cytoskeleton. Cancer Res. 58:2952-2956.
39. Lippincott-Schwartz, J., N. B. Cole, A. Marotta, P. A. Conrad, and G. S. Bloom. 1995. Kinesin is the motor for microtubule-mediated Golgi-to-ER membrane traffic. J. Cell Biol. 128:293-306.
40. Ichikawa, T., M. Yamada, D. Homma, R. J. Cherry, I. E. G. Morrison, and S. Kawato. 2000. Digital fluorescence imaging of trafficking of endosomes containing low-density lipoprotein in brain astroglial cells. Biochem. Biophys. Res. Commun. 269:25-30.
41. Hirokawa, N. 1998. Kinesin and dynein superfamily proteins and the mechanism of organelle transport. Science. 279:519-526.
42. Hirokawa, N. 1996. Organelle transport along microtubules-the role of KIFs. Trends Cell Biol. 6:135-141.
43. Ma, S., and R. L. Chisholm. 2002. Cytoplasmic dynein-associated structures move bidirectionally in vivo. J. Cell Sci. 115:1453-1460.
44. McCaffrey, G., and R. D. Vale. 1989. Identification of a kinesin-like microtubule-based motor protein in Dictyostelium discoideum. EMBO J. 8:3229-3234.
45. Pollock, N., M. P. Koonce, E. L. de Hostos, and R. D. Vale. 1998. In vitro microtubule-based organelle transport in wild-type Dictyostelium and cells overexpressing a truncated dynein heavy chain. Cell Motil. Cytoskeleton. 40:304-314.
46. Habermann, A., T. A. Schroer, G. Griffiths, and J. K. Burkhardt. 2001. Immunolocalization of cytoplasmic dynein and dynactin subunits in cultured macrophages: enrichment on early endocytic organelles. J. Cell Sci. 114:229-240.
47. Welte, M. A., S. P. Gross, M. Postner, S. M. Block, and E. F. Wieschaus. 1998. Developmental regulation of vesicle transport in Drosophila embryos: forces and kinetics. Cell. 92:547-557.
48. Chang, W. J., K. G. Rothberg, B. A. Kamen, and R. G. Anderson. 1992. Lowering the cholesterol content of MA104 cells inhibits receptor-mediated transport of folate. J. Cell Biol. 118:63-69.
49. Novick, P., and M. Zerial. 1997. The diversity of Rab proteins in vesicle transport. Curr. Opin. Cell Biol. 9:496-504.
50. 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.
51. Lebrand, C., M. Corti, H. Goodson, P. Cosson, V. Cavalli, N. Mayran, J. Fauré, and J. Gruenberg. 2002. Late endosome motility depends on lipids via the small GTPase Rab7. EMBO J. 21:1289-1300.
52. Choudhury, A., D. K. Sharma, D. L. Marks, and R. E. Pagano. 2004. Elevated endosomal cholesterol levels in Niemann-Pick cells inhibit Rab4 and perturb membrane recycling. Mol. Biol. Cell. 15:4500-4511.
53. Lombardi, D., T. Soldati, M. A. Riederer, Y. Goda, M. Zerial, and S. R. Pfeffer. 1993. Rab9 functions in transport between late endosomes and the trans Golgi network. EMBO J. 12:677-682.
54. Nichols, B. J., A. K. Kenworthy, R. S. Polishchuk, R. Lodge, T. H. Roberts, K. Hirschberg, R. D. Phair, and J. Lippincott-Schwartz. 2001. Rapid cycling of lipid raft markers between the cell surface and Golgi complex. J. Cell Biol. 153:529-542.
55. Johansson, M., N. Rocha, W. Zwart, I. Jordens, L. Janssen, C. Kuijl, V. M. Olkkonen, and J. Neefjes. 2007. Activation of endosomal dynein motors by stepwise assembly of Rab7-RILP-p150Glued, ORP1L, and the receptor βIII spectrin. J. Cell Biol. 176:459-471.
56. McIlvain, J. M. Jr., J. K. Burkhardt, S. Hamm-Alvarez, Y. Argon, and M. P. Sheetz. 1994. Regulation of kinesin activity by phosphorylation of kinesin-associated proteins. J. Biol. Chem. 269:19176-19182.
57. Reilein, A. R., I. S. Tint, N. I. Peunova, G. N. Enikolopov, and V. I. Gelfand. 1998. Regulation of organelle movement in melanophores by protein kinase A (PKA), protein kinase C (PKC), and protein phosphatase 2A (PP2A). J. Cell Biol. 142:803-813.
58. Hammer 3rd, J. A., and X. S. Wu. 2002. Rabs grab motors: defining the connections between Rab GTPases and motor proteins. Curr. Opin. Cell Biol. 14:69-75.
59. Imamura, T., J. Huang, I. Usui, H. Satoh, J. Bever, and J. M. Olefsky. 2003. Insulin-induced GLUT4 translocation involves Protein Kinase C-l-mediated functional coupling between Rab4 and the motor protein kinesin. Mol. Cell. Biol. 23:4892-4900.
60. Bananis, E., S. Nath, K. Gordon, P. Satir, R. J. Stockert, J. W. Murray, and A. W. Wolkoff. 2004. Microtubule-dependent movement of late endocytic vesicles in vitro: requirements for dynein and kinesin. Mol. Biol. Cell. 15:3688-3697.
61. Tekotte, H., and I. Davis. 2002. Intracellular mRNA localization: motors move messages. Trends Genet. 18:636-642.
62. Jordens, I., M. Marsman, C. Kuijl, and J. Neefjes. 2005. Rab proteins, connecting transport and vesicle fusion. Traffic. 6:1070-1077.
63. Deneka, M., M. Neeft, andP. vanderSluijs. 2003. Regulation of membrane transport by Rab GTPases. Crit. Rev. Biochem. Mol. Biol. 38:121-142.
64. Tuvim, M. J., R. Adachi, S. Hoffenberg, and B. F. Dickey. 2001. Traffic control: Rab GTPases and the regulation of interorganellar transport. News Physiol. Sci. 16:56-61.
65. Sheff, D. R., E. A. Daro, M. Hull, and I. Mellman. 1999. The receptor recycling pathway contains two distinct populations of early endosomes with different sorting functions. J. Cell Biol. 145:123-139.
66. Sönnichsen, B., S. De Renzis, E. Nielsen, J. Rietdorf, and M. Zerial. 2000. Distinct membrane domains on endosomes in the recycling pathway visualized by multicolor imaging of Rab4, Rab5, and Rab11. J. Cell Biol. 149:901-914.
67. van der Sluijs, P., M. Hull, A. Zahraoui, A. Tavitian, B. Goud, and I. Mellman. 1991. The small GTP-binding protein Rab4 is associated with early endosomes. Proc. Natl. Acad. Sci. USA. 88:6313-6317.
68. Ullrich, O., S. Reinsch, S. Urbe, M. Zerial, and R. G. Parton. 1996. Rab11 regulates recycling through the pericentriolar recycling endosome. J. Cell Biol. 135:913-924.
69. van der Sluijs, P., M. Hull, P. Webster, P. Male, B. Goud, and I. Mellman. 1992. The small GTP-binding protein Rab4 controls an early sorting event on the endocytic pathway. Cell. 70:729-740.
70. Wu, X., B. Bowers, K. Rao, Q. Wei, and J. A. Hammer III. 1998. Visualization of melanosome dynamics within wild-type and dilute melanocytes suggests a paradigm for myosin V function in vivo. J. Cell Biol. 143:1899-1918.