Caenorhabditis elegans reveals a FxNPxY-independent low-density lipoprotein receptor internalization mechanism mediated by epsin1

Molecular Biology of the Cell

Volumn 24, Issue 3, 2013, Pages 308-318

  Kang, Yuan Lin ^a   Yochem, John ^b   Bell, Leslie ^b   Sorensen, Erika B ^c   Chen, Lihsia ^a   Conner, Sean D ^a  

^a UNIVERSITY OF MINNESOTA MEDICAL SCHOOL   (United States)

^b UNIVERSITY OF WYOMING   (United States)

^c UNIVERSITY OF WISCONSIN MADISON   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CLATHRIN; EPSIN; EPSIN 1; LOW DENSITY LIPOPROTEIN RECEPTOR; MEGALIN; UBIQUITIN; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; CAENORHABDITIS ELEGANS; CHEMICAL ANALYSIS; COMPLEX FORMATION; CONTROLLED STUDY; DAB1 GENE; ENDOCYTOSIS; EPN1 GENE; GENE; GENETIC ANALYSIS; GENETIC ASSOCIATION; INTERNALIZATION; LOSS OF FUNCTION MUTATION; MAMMAL CELL; NONHUMAN; PRIORITY JOURNAL; PROTEIN INTERACTION; PROTEIN TRANSPORT; RNA INTERFERENCE; UBIQUITINATION;

ADAPTOR PROTEINS, VESICULAR TRANSPORT; AMINO ACID MOTIFS; AMINO ACID SUBSTITUTION; ANIMALS; CAENORHABDITIS ELEGANS; CAENORHABDITIS ELEGANS PROTEINS; ENDOCYTOSIS; GENE KNOCKDOWN TECHNIQUES; HELA CELLS; HUMANS; LOW DENSITY LIPOPROTEIN RECEPTOR-RELATED PROTEIN-1; MOLECULAR SEQUENCE DATA; PROTEIN STABILITY; PROTEIN TRANSPORT; RNA INTERFERENCE; UBIQUITINATION;

EID: 84873384710     PISSN: 10591524     EISSN: 19394586     Source Type: Journal    
DOI: 10.1091/mbc.E12-02-0163     Document Type: Article

References (66)

1. Aguilar RC et al. (2006). Epsin N-terminal homology domains perform an essential function regulating Cdc42 through binding Cdc42 GTPase-activating proteins. Proc Natl Acad Sci USA 103, 4116-4121.
2. Anderson RG, Goldstein JL, Brown MS (1977). A mutation that impairs the ability of lipoprotein receptors to localise in coated pits on the cell surface of human fibroblasts. Nature 270, 695-699.
3. Balklava Z, Pant S, Fares H, Grant BD (2007). Genome-wide analysis identifies a general requirement for polarity proteins in endocytic traffic. Nat Cell Biol 9, 1066-1072.
4. Boucrot E, Saffarian S, Zhang R, Kirchhausen T (2010). Roles of AP-2 in clathrin-mediated endocytosis. PLoS One 5, e10597.
5. Brady RJ, Wen Y, O'Halloran TJ (2008). The ENTH and C-terminal domains of Dictyostelium epsin cooperate to regulate the dynamic interaction with clathrin-coated pits. J Cell Sci 121, 3433-3444.
6. Brenner S (1974). The genetics of Caenorhabditis elegans. Genetics 77, 71-94.
7. Chen C, Zhuang X (2008). Epsin 1 is a cargo-specific adaptor for the clathrin-mediated endocytosis of the influenza virus. Proc Natl Acad Sci USA 105, 11790-11795.
8. Chen H et al. (2009). Embryonic arrest at midgestation and disruption of Notch signaling produced by the absence of both epsin 1 and epsin 2 in mice. Proc Natl Acad Sci USA 106, 13838-13842.
9. Chen H, Fre S, Slepnev VI, Capua MR, Takei K, Butler MH, Di Fiore PP, De Camilli P (1998). Epsin is an EH-domain-binding protein implicated in clathrin-mediated endocytosis. Nature 394, 793-797.
10. Chen WJ, Goldstein JL, Brown MS (1990). NPXY, a sequence often found in cytoplasmic tails, is required for coated pit-mediated internalization of the low density lipoprotein receptor. J Biol Chem 265, 3116-3122.
11. Chen X, Zhang B, Fischer JA (2002). A specific protein substrate for a deubiquitinating enzyme: liquid facets is the substrate of fat facets. Genes Dev 16, 289-294.
12. Damke H, Baba T, van der Bliek AM, Schmid SL (1995). Clathrin-independent pinocytosis is induced in cells overexpressing a temperature-sensitive mutant of dynamin. J Cell Biol 131, 69-80.
13. Dores MR, Schnell JD, Maldonado-Baez L, Wendland B, Hicke L (2009). The function of yeast epsin and ede1 ubiquitin-binding domains during receptor internalization. Traffic 11, 151-160.
14. Drake MT, Downs MA, Traub LM (2000). Epsin binds to clathrin by associating directly with the clathrin-terminal domain. Evidence for cooperative binding through two discrete sites. J Biol Chem 275, 6479-6489.
15. Edeling MA, Mishra SK, Keyel PA, Steinhauser AL, Collins BM, Roth R, Heuser JE, Owen DJ, Traub LM (2006). Molecular switches involving the AP-2 β2 appendage regulate endocytic cargo selection and clathrin coat assembly. Dev Cell 10, 329-342.
16. Eden ER, Patel DD, Sun XM, Burden JJ, Themis M, Edwards M, Lee P, Neuwirth C, Naoumova RP, Soutar AK (2002). Restoration of LDL receptor function in cells from patients with autosomal recessive hypercholesterolemia by retroviral expression of ARH1. J Clin Invest 110, 1695-1702.
17. Frand AR, Russel S, Ruvkun G (2005). Functional genomic analysis of C. elegans molting. PLoS Biol 3, e312.
18. Fraser AG, Kamath RS, Zipperlen P, Martinez-Campos M, Sohrmann M, Ahringer J (2000). Functional genomic analysis of C. elegans chromosome I by systematic RNA interference. Nature 408, 325-330.
19. Garcia CK et al. (2001). Autosomal recessive hypercholesterolemia caused by mutations in a putative LDL receptor adaptor protein. Science 292, 1394-1398.
20. Gravotta D, Carvajal-Gonzalez JM, Mattera R, Deborde S, Banfelder JR, Bonifacino JS, Rodriguez-Boulan E (2012). The clathrin adaptor AP-1A mediates basolateral polarity. Dev Cell 22, 811-822.
21. Hawryluk MJ, Keyel PA, Mishra SK, Watkins SC, Heuser JE, Traub LM (2006). Epsin 1 is a polyubiquitin-selective clathrin-associated sorting protein. Traffic 7, 262-281.
22. Henne WM, Boucrot E, Meinecke M, Evergren E, Vallis Y, Mittal R, McMahon HT (2010). FCHo proteins are nucleators of clathrin-mediated endocytosis. Science 328, 1281-1284.
23. Huang F, Khvorova A, Marshall W, Sorkin A (2004). Analysis of clathrin-mediated endocytosis of epidermal growth factor receptor by RNA interference. J Biol Chem 279, 16657-16661.
24. Itoh T, Koshiba S, Kigawa T, Kikuchi A, Yokoyama S, Takenawa T (2001). Role of the ENTH domain in phosphatidylinositol-4,5-bisphosphate binding and endocytosis. Science 291, 1047-1051.
25. Jakobsson J, Gad H, Andersson F, Low P, Shupliakov O, Brodin L (2008). Role of epsin 1 in synaptic vesicle endocytosis. Proc Natl Acad Sci USA 105, 6445-6450.
26. Kamath RS, Ahringer J (2003). Genome-wide RNAi screening in Caenorhabditis elegans. Methods 30, 313-321.
27. Kamikura DM, Cooper JA (2003). Lipoprotein receptors and a disabled family cytoplasmic adaptor protein regulate EGL-17/FGF export in C. elegans. Genes Dev 17, 2798-2811.
28. Kamikura DM, Cooper JA (2006). Clathrin interaction and subcellular localization of Ce-DAB-1, an adaptor for protein secretion in Caenorhabditis elegans. Traffic 7, 324-336.
29. Kazazic M, Bertelsen V, Pedersen KW, Vuong TT, Grandal MV, Rodland MS, Traub LM, Stang E, Madshus IH (2009). Epsin 1 is involved in recruitment of ubiquitinated EGF receptors into clathrin-coated pits. Traffic 10, 235-245.
30. Keyel PA, Mishra SK, Roth R, Heuser JE, Watkins SC, Traub LM (2006). A single common portal for clathrin-mediated endocytosis of distinct cargo governed by cargo-selective adaptors. Mol Biol Cell 17, 4300-4317.
31. Kingsley DM, Krieger M (1984). Receptor-mediated endocytosis of low density lipoprotein: somatic cell mutants define multiple genes required for expression of surface-receptor activity. Proc Natl Acad Sci USA 81, 5454-5458.
32. Legendre-Guillemin V, Wasiak S, Hussain NK, Angers A, McPherson PS (2004). ENTH/ANTH proteins and clathrin-mediated membrane budding. J Cell Sci 117, 9-18.
33. Maldonado-Baez L, Wendland B (2006). Endocytic adaptors: recruiters, coordinators and regulators. Trends Cell Biol 16, 505-512.
34. Martin PJ, Ledbetter JA, Clark EA, Beatty PG, Hansen JA (1984). Epitope mapping of the human surface suppressor/cytotoxic T cell molecule Tp32. J Immunol 132, 759-765.
35. Maurer ME, Cooper JA (2006). The adaptor protein Dab2 sorts LDL receptors into coated pits independently of AP-2 and ARH. J Cell Sci 119, 4235-4246.
36. Mettlen M, Loerke D, Yarar D, Danuser G, Schmid SL (2010). Cargo-and adaptor-specific mechanisms regulate clathrin-mediated endocytosis. J Cell Biol 188, 919-932.
37. Michaely P, Zhao Z, Li WP, Garuti R, Huang LJ, Hobbs HH, Cohen JC (2007). Identification of a VLDL-induced, FDNPVY-independent internalization mechanism for the LDLR. EMBO J 26, 3273-3282.
38. Mishra SK, Keyel PA, Hawryluk MJ, Agostinelli NR, Watkins SC, Traub LM (2002). Disabled-2 exhibits the properties of a cargo-selective endocytic clathrin adaptor. EMBO J 21, 4915-4926.
39. Morris SM, Cooper JA (2001). Disabled-2 colocalizes with the LDLR in clathrin-coated pits and interacts with AP-2. Traffic 2, 111-122.
40. Motley A, Bright NA, Seaman MN, Robinson MS (2003). Clathrin-mediated endocytosis in AP-2-depleted cells. J Cell Biol 162, 909-918.
41. Mulkearns EE, Cooper JA (2012). FCH domain only-2 organizes clathrin-coated structures and interacts with Disabled-2 for low-density lipoprotein receptor endocytosis. Mol Biol Cell 23, 1330-1342.
42. Oldham CE, Mohney RP, Miller SL, Hanes RN, O'Bryan JP (2002). The ubiquitin-interacting motifs target the endocytic adaptor protein epsin for ubiquitination. Curr Biol 12, 1112-1116.
43. Overstreet E, Chen X, Wendland B, Fischer JA (2003). Either part of a Drosophila epsin protein, divided after the ENTH domain, functions in endocytosis of delta in the developing eye. Curr Biol 13, 854-860.
44. Reusch U, Bernhard O, Koszinowski U, Schu P (2002). AP-1A and AP-3A lysosomal sorting functions. Traffic 3, 752-761.
45. Robinson MS (2004). Adaptable adaptors for coated vesicles. Trends Cell Biol 14, 167-174.
46. Shafaq-Zadah M, Brocard L, Solari F, Michaux G (2012). AP-1 is required for the maintenance of apico-basal polarity in the C. elegans intestine. Development 139, 2061-2070.
47. Shih SC, Katzmann DJ, Schnell JD, Sutanto M, Emr SD, Hicke L (2002). Epsins and Vps27p/Hrs contain ubiquitin-binding domains that function in receptor endocytosis. Nat Cell Biol 4, 389-392.
48. Sigismund S, Woelk T, Puri C, Maspero E, Tacchetti C, Transidico P, Di Fiore PP, Polo S (2005). Clathrin-independent endocytosis of ubiquitinated cargos. Proc Natl Acad Sci USA 102, 2760-2765.
49. Sirinian MI et al. (2005). Adaptor protein ARH is recruited to the plasma membrane by low density lipoprotein (LDL) binding and modulates endocytosis of the LDL/LDL receptor complex in hepatocytes. J Biol Chem 280, 38416-38422.
50. Sorensen EB, Conner SD (2010). γ secretase-dependent cleavage initiates Notch signaling from the plasma membrane. Traffic 11, 1234-1245.
51. Soutar AK, Naoumova RP (2007). Mechanisms of disease: genetic causes of familial hypercholesterolemia. Nat Clin Pract Cardiovasc Med 4, 214-225.
52. Sugiyama S, Kishida S, Chayama K, Koyama S, Kikuchi A (2005). Ubiquitin-interacting motifs of Epsin are involved in the regulation of insulin-dependent endocytosis. J Biochem 137, 355-364.
53. Teckchandani A, Mulkearns EE, Randolph TW, Toida N, Cooper JA (2012). The clathrin adaptor Dab2 recruits EH domain scaffold proteins to regulate integrin β1 endocytosis. Mol Biol Cell 23, 2905-2916.
54. Tian X, Hansen D, Schedl T, Skeath JB (2004). Epsin potentiates Notch pathway activity in Drosophila and C. elegans. Development 131, 5807-5815.
55. van Driel IR, Davis CG, Goldstein JL, Brown MS (1987). Self-association of the low density lipoprotein receptor mediated by the cytoplasmic domain. J Biol Chem 262, 16127-16134.
56. Wang W, Struhl G (2004). Drosophila Epsin mediates a select endocytic pathway that DSL ligands must enter to activate Notch. Development 131, 5367-5380.
57. Wendland B, Steece KE, Emr SD (1999). Yeast epsins contain an essential N-terminal ENTH domain, bind clathrin and are required for endocytosis. EMBO J 18, 4383-4392.
58. Xie X, Cho B, Fischer JA (2012). Drosophila Epsin's role in Notch ligand cells requires three Epsin protein functions: the lipid binding function of the ENTH domain, a single ubiquitin interaction motif, and a subset of the C-terminal protein binding modules. Dev Biol 363, 399-412.
59. Xu J, Toops KA, Diaz F, Carvajal-Gonzalez JM, Gravotta D, Mazzoni F, Schreiner R, Rodriguez-Boulan E, Lakkaraju A (2012). Mechanism of polarized lysosome exocytosis in epithelial cells. J Cell Sci, doi:10.1242/jcs.109421.
60. Yochem J, Greenwald I (1993). A gene for a low density lipoprotein receptor-related protein in the nematode Caenorhabditis elegans. Proc Natl Acad Sci USA 90, 4572-4576.
61. Yochem J, Tuck S, Greenwald I, Han M (1999). A gp330/megalin-related protein is required in the major epidermis of Caenorhabditis elegans for completion of molting. Development 126, 597-606.
62. Yoshida H, Yokode M, Yamamoto A, Masaki R, Murayama T, Horiuchi H, Kita T (1999). Compensated endocytosis of LDL by hamster cells co-expressing the two distinct mutant LDL receptors defective in endocytosis and ligand binding. J Lipid Res 40, 814-822.
63. Yun M, Keshvara L, Park CG, Zhang YM, Dickerson JB, Zheng J, Rock CO, Curran T, Park HW (2003). Crystal structures of the Dab homology domains of mouse disabled 1 and 2. J Biol Chem 278, 36572-36581.
64. Zelcer N, Hong C, Boyadjian R, Tontonoz P (2009). LXR regulates cholesterol uptake through Idol-dependent ubiquitination of the LDL receptor. Science 325, 100-104.
65. Zhang H, Kim A, Abraham N, Khan LA, Hall DH, Fleming JT, Gobel V (2012). Clathrin and AP-1 regulate apical polarity and lumen formation during C. elegans tubulogenesis. Development 139, 2071-2082.
66. Zou P, Ting AY (2011). Imaging LDL receptor oligomerization during endocytosis using a co-internalization assay. ACS Chem Biol 6, 308-312.