A role for EHD4 in the regulation of early endosomal transport

Traffic

Volumn 9, Issue 6, 2008, Pages 995-1018

  Sharma, Mahak ^a   Naslavsky, Naava ^a   Caplan, Steve ^a,b  

^a UNIVERSITY OF NEBRASKA MEDICAL CENTER   (United States)

^b UNIVERSITY OF NEBRASKA MEDICAL CENTER   (United States)

Author keywords

Early endosome; EHD1; EHD4; Rab5

Indexed keywords

ADENOSINE DIPHOSPHATE RIBOSYLATION FACTOR 6; CARBOXY TERMINAL EPS15 HOMOLOGY DOMAIN PROTEIN 1; CARBOXY TERMINAL EPS15 HOMOLOGY DOMAIN PROTEIN 4; EARLY ENDOSOME ANTIGEN 1; GUANOSINE TRIPHOSPHATE; LOW DENSITY LIPOPROTEIN; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 1; PEPTIDE ANTIBODY; POLYCLONAL ANTIBODY; RAB PROTEIN; RAB5 PROTEIN; REGULATOR PROTEIN; SHORT HAIRPIN RNA; SMALL INTERFERING RNA; TRANSFERRIN;

ARTICLE; CELL COMPARTMENTALIZATION; CELLULAR DISTRIBUTION; CONTROLLED STUDY; DOWN REGULATION; ENDOCYTOSIS; ENDOSOME; GENE EXPRESSION REGULATION; HUMAN; HUMAN CELL; INTERNALIZATION; INTRACELLULAR TRANSPORT; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN PROTEIN INTERACTION; PROTEIN TRANSPORT;

BIOLOGICAL TRANSPORT; DNA-BINDING PROTEINS; ENDOSOMES; HELA CELLS; HUMANS; NUCLEAR PROTEINS; PROTEIN BINDING; PROTEIN TRANSPORT; RAB5 GTP-BINDING PROTEINS; RNA INTERFERENCE; RNA, SMALL INTERFERING; TIME FACTORS; VESICULAR TRANSPORT PROTEINS;

EID: 43149116767     PISSN: 13989219     EISSN: 16000854     Source Type: Journal    
DOI: 10.1111/j.1600-0854.2008.00732.x     Document Type: Article

References (58)

1. Pfeffer SR. Rab GTPases: Specifying and deciphering organelle identity and function. Trends Cell Biol 2001;11:487-491.
2. Zerial M, McBride H. Rab proteins as membrane organizers. Nat Rev Mol Cell Biol 2001;2:107-117.
3. Grosshans BL, Ortiz D, Novick P. Rabs and their effectors: Achieving specificity in membrane traffic. Proc Natl Acad Sci U S A 2006;103:11821-11827.
4. Gorvel JP, Chavrier P, Zerial M, Gruenberg J. Rab5 controls early endosome fusion in vitro. Cell 1991;64:915-925.
5. Stenmark H, Valencia A, Martinez O, Ullrich O, Goud B, Zerial M. Distinct structural elements of rab5 define its functional specificity. EMBO J 1994;13:575-583.
6. Daro E, van der Sluijs P, Galli T, Mellman I. Rab4 and cellubrevin define different early endosome populations on the pathway of transferrin receptor recycling. Proc Natl Acad Sci U S A 1996;93:9559-9564.
7. Sheff DR, Daro EA, 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.
8. Ren M, Xu G, Zeng J, De Lemos-Chiarandini C, Adesnik M, Sabatini DD. Hydrolysis of GTP on rab11 is required for the direct delivery of transferrin from the pericentriolar recycling compartment to the cell surface but not from sorting endosomes. Proc Natl Acad Sci U S A 1998;95:6187-6192.
9. Casanova JE, Wang X, Kumar R, Bhartur SG, Navarre J, Woodrum JE, Altschuler Y, Ray GS, Goldenring JR. Association of Rab25 and Rab11a with the apical recycling system of polarized Madin-Darby canine kidney cells. Mol Biol Cell 1999;10:47-61.
10. Simpson JC, Griffiths G, Wessling-Resnick M, Fransen JA, Bennett H, Jones AT. A role for the small GTPase Rab21 in the early endocytic pathway. J Cell Sci 2004;117:6297-6311.
11. Pellinen T, Arjonen A, Vuoriluoto K, Kallio K, Fransen JA, Ivaska J. Small GTPase Rab21 regulates cell adhesion and controls endosomal traffic of {beta}1-integrins. J Cell Biol 2006;173:767-780.
12. Weigert R, Donaldson JG. Fluorescent microscopy-based assays to study the role of Rab22a in clathrin-independent endocytosis. Methods Enzymol 2005;403:243-253.
13. Mesa R, Salomon C, Roggero M, Stahl PD, Mayorga LS. Rab22a affects the morphology and function of the endocytic pathway. J Cell Sci 2001;114:4041-4049.
14. Kauppi M, Simonsen A, Bremnes B, Vieira A, Callaghan J, Stenmark H, Olkkonen VM. The small GTPase Rab22 interacts with EEA1 and controls endosomal membrane trafficking. J Cell Sci 2002;115:899-911.
15. Babbey CM, Ahktar N, Wang E, Chen CC, Grant BD, Dunn KW. Rab10 regulates membrane transport through early endosomes of polarized Madin-Darby canine kidney cells. Mol Biol Cell 2006; 17: 3156-3175.
16. Schuck S, Gerl MJ, Ang A, Manninen A, Keller P, Mellman I, Simons K. Rab10 is involved in basolateral transport in polarized Madin-Darby canine kidney cells. Traffic 2007;8:47-60.
17. Chen CC, Schweinsberg PJ, Vashist S, Mareiniss DP, Lambie EJ, Grant BD. RAB-10 is required for endocytic recycling in the Caenorhabditis elegans intestine. Mol Biol Cell 2006;17:1286-1297.
18. Novick P, Medkova M, Dong G, Hutagalung A, Reinisch K, Grosshans B. Interactions between Rabs, tethers, SNAREs and their regulators in exocytosis. Biochem Soc Trans 2006;34:683-686.
19. Naslavsky N, Caplan S. C-terminal EH-domain-containing proteins: consensus for a role in endocytic trafficking, EH? J Cell Sci 2005;118:4093-4101.
20. Mintz L, Galperin E, Pasmanik-Chor M, Tulzinsky S, Bromberg Y, Kozak CA, Joyner A, Fein A, Horowitz M. EHD1 -an EH-domain-containing protein with a specific expression pattern. Genomics 1999;59:66-76.
21. Pohl U, Smith JS, Tachibana I, Ueki K, Lee HK, Ramaswamy S, Wu Q, Mohrenweiser HW, Jenkins RB, Louis DN. EHD2, EHD3, and EHD4 encode novel members of a highly conserved family of EH domain-containing proteins. Genomics 2000;63:255-262.
22. Grant B, Zhang Y, Paupard MC, Lin SX, Hall DH, Hirsh D. Evidence that RME-1, a conserved C. elegans EH-domain protein, functions in endocytic recycling. Nat Cell Biol 2001;3:573-579.
23. Lin SX, Grant B, Hirsh D, Maxfield FR. Rme-1 regulates the distribution and function of the endocytic recycling compartment in mammalian cells. Nat Cell Biol 2001;3:567-572.
24. Lee DW, Zhao X, Scarselletta S, Schweinsberg PJ, Eisenberg E, Grant BD, Greene LE. ATP binding regulates oligomerization and endosome association of RME-1 family proteins. J Biol Chem 2005;280:280-290.
25. Naslavsky N, Rahajeng J, Sharma M, Jovic M, Caplan S. Interactions between EHD proteins and Rab11-FIP2: A role for EHD3 in early endosomal transport. Mol Biol Cell 2006;17:163-177.
26. Daumke O, Lundmark R, Vallis Y, Martens S, Butler PJ, McMahon HT. Architectural and mechanistic insights into an EHD ATPase involved in membrane remodelling. Nature 2007;449:923-927.
27. Kieken F, Jovic M, Naslavsky N, Caplan S, Sorgen PL. EH domain of EHD1. J Biomol NMR 2007;39:232-329.
28. Naslavsky N, Boehm M, Backlund PS Jr, Caplan S. Rabenosyn-5 and EHD1 interact and sequentially regulate protein recycling to the plasma membrane. Mol Biol Cell 2004;15:2410-2422.
29. Rapaport D, Auerbach W, Naslavsky N, Pasmanik-Chor M, Galperin E, Fein A, Caplan S, Joyner AL, Horowitz M. Recycling to the plasma membrane is delayed in EHD1 knockout mice. Traffic 2006;7:52-60.
30. Caplan S, Naslavsky N, Hartnell LM, Lodge R, Polishchuk RS, Donaldson JG, Bonifacino JS. A tubular EHD1-containing compartment involved in the recycling of major histocompatibility complex class I molecules to the plasma membrane. EMBO J 2002;21:2557-2567.
31. Picciano JA, Ameen N, Grant BD, Bradbury NA. Rme-1 regulates the recycling of the cystic fibrosis transmembrane conductance regulator. Am J Physiol Cell Physiol 2003;285:C1009-C1018.
32. Guilherme A, Soriano NA, Furcinitti PS, Czech MP. Role of EHD1 and EHBP1 in perinuclear sorting and insulin-regulated GLUT4 recycling in 3T3-L1 adipocytes. J Biol Chem 2004;279:40062-40075.
33. Park M, Penick EC, Edwards JG, Kauer JA, Ehlers MD. Recycling endosomes supply AMPA receptors for LTP. Science 2004;305:1972-1975.
34. Jovic M, Naslavsky N, Rapaport D, Horowitz M, Caplan S. EHD1 regulates beta1 integrin endosomal transport: Effects on focal adhesions, cell spreading and migration. J Cell Sci 2007;120:802-814.
35. Hao M, Lin SX, Karylowski OJ, Wustner D, McGraw TE, Maxfield FR. Vesicular and non-vesicular sterol transport in living cells. The endocytic recycling compartment is a major sterol storage organelle. J Biol Chem 2002;277:609-617.
36. Naslavsky N, Rahajeng J, Rapaport D, Horowitz M, Caplan S. EHD1 regulates cholesterol homeostasis and lipid droplet storage. Biochem Biophys Res Commun 2007;357:792-799.
37. Gokool S, Tattersall D, Seaman MN. EHD1 interacts with retromer to stabilise SNX1-tubules and facilitate endosome-to-Golgi retrieval. Traffic 2007;8:1873-1886.
38. Rotem-Yehudar R, Galperin E, Horowitz M. Association of insulin-like growth factor 1 receptor with EHD1 and SNAP29. J Biol Chem 2001;276:33054-33060.
39. Braun A, Pinyol R, Dahlhaus R, Koch D, Fonarev P, Grant BD, Kessels MM, Qualmann B. EHD proteins associate with syndapin I and II and such interactions play a crucial role in endosomal recycling. Mol Biol Cell 2005;16:3642-3658.
40. Xu Y, Shi H, Wei S, Wong SH, Hong W. Mutually exclusive interactions of EHD1 with GS32 and syndapin II. Mol Membr Biol 2004;21:269-277.
41. Shi A, Pant S, Balklava Z, Chen CC, Figueroa V, Grant BD. A novel requirement for C. elegans Alix/ALX-1 in RME-1-mediated membrane transport. Curr Biol 2007;17:1913-1924.
42. Galperin E, Benjamin S, Rapaport D, Rotem-Yehudar R, Tolchinsky S, Horowitz M. EHD3: A protein that resides in recycling tubular and vesicular membrane structures and interacts with EHD1. Traffic 2002;3:575-589.
43. Park SY, Ha BG, Choi GH, Ryu J, Kim B, Jung CY, Lee W. EHD2 interacts with the insulin-responsive glucose transporter (GLUT4) in rat adipocytes and may participate in insulin-induced GLUT4 recruitment. Biochemistry 2004;43:7552-7562.
44. Guilherme A, Soriano NA, Bose S, Holik J, Bose A, Pomerleau DP, Furcinitti P, Leszyk J, Corvera S, Czech MP. EHD2 and the novel EH domain binding protein EHBP1 couple endocytosis to the actin cytoskeleton. J Biol Chem 2004;279:10593-10605.
45. Blume JJ, Halbach A, Behrendt D, Paulsson M, Plomann M. EHD proteins are associated with tubular and vesicular compartments and interact with specific phospholipids. Exp Cell Res 2007;313:219-231.
46. George M, Ying G, Rainey MA, Solomon A, Parikh PT, Gao Q, Band V, Band H. Shared as well as distinct roles of EHD proteins revealed by biochemical and functional comparisons in mammalian cells and C. elegans. BMC Cell Biol 2007;8:3.
47. Kuo HJ, Tran NT, Clary SA, Morris NP, Glanville RW. Characterization of EHD4, an EH domain-containing protein expressed in the extracellular matrix. J Biol Chem 2001;276:43103-43110.
48. Shao Y, Akmentin W, Toledo-Aral JJ, Rosenbaum J, Valdez G, Cabot JB, Hilbush BS, Halegoua S. Pincher, a pinocytic chaperone for nerve growth factor/TrkA signaling endosomes. J Cell Biol 2002;157:679-691.
49. Smith CA, Dho SE, Donaldson J, Tepass U, McGlade CJ. The cell fate determinant numb interacts with EHD/Rme-1 family proteins and has a role in endocytic recycling. Mol Biol Cell 2004;15:3698-3708.
50. Bucci C, Parton RG, Mather IH, 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.
51. Stenmark H, Parton RG, Steele-Mortimer O, Lutcke A, Gruenberg J, Zerial M. Inhibition of rab5 GTPase activity stimulates membrane fusion in endocytosis. EMBO J 1994;13:1287-1296.
52. Galperin E, Sorkin A. Visualization of Rab5 activity in living cells by FRET microscopy and influence of plasma-membrane-targeted Rab5 on clathrin-dependent endocytosis. J Cell Sci 2003;116:4799-4810.
53. Gaullier JM, Simonsen A, D'Arrigo A, Bremnes B, Stenmark H, Aasland R. FYVE fingers bind PtdIns(3)P. Nature 1998;394:432-433.
54. Corvera S, D'Arrigo A, Stenmark H. Phosphoinositides in membrane traffic. Curr Opin Cell Biol 1999;11:460-465.
55. Caplan S, Hartnell LM, Aguilar RC, Naslavsky N, Bonifacino JS. Human Vam6p promotes lysosome clustering and fusion in vivo. J Cell Biol 2001;154:109-122.
56. Bolte S, Cordelieres FP. A guided tour into subcellular colocalization analysis in light microscopy. J Microsc 2006;224:213-232.
57. Manders EM, Stap J, Brakenhoff GJ, van Driel R, Aten JA. Dynamics of three-dimensional replication patterns during the S-phase, analysed by double labelling of DNA and confocal microscopy. J Cell Sci 1992;103:857-862.
58. Naslavsky N, Rahajeng J, Chenavas S, Sorgen PL, Caplan S. EHD1 and Eps15 interact with phosphatidylinositols via their Eps15 homology domains. J Biol Chem 2007;282:16612-16622.