The clathrin adaptor proteins ARH, Dab2, and numb play distinct roles in Niemann-Pick C1-Like 1 versus low density lipoprotein receptor-mediated cholesterol uptake

Journal of Biological Chemistry

Volumn 289, Issue 48, 2014, Pages 33689-33700

  Wei, Jian ^a   Fu, Zhen Yan ^b   Li, Pei Shan ^a   Miao, Hong Hua ^a   Li, Bo Liang ^a   Ma, Yi Tong ^b   Song, Bao Liang ^a,c  

^a INSTITUTE OF GEOLOGY AND GEOPHYSICS   (China)

^b XINJIANG MEDICAL UNIVERSITY   (China)

^c WUHAN UNIVERSITY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

LIPOPROTEINS; MACHINERY; MOLECULAR BIOLOGY;

ADAPTOR PROTEINS; CHOLESTEROL ABSORPTION; CHOLESTEROL UPTAKES; CLATHRIN-DEPENDENT ENDOCYTOSIS; ENDOCYTIC MACHINERY; LOW DENSITY LIPOPROTEIN RECEPTORS; LOW DENSITY LIPOPROTEINS; PHOSPHOTYROSINE BINDINGS;

CHOLESTEROL;

CLATHRIN; LOW DENSITY LIPOPROTEIN RECEPTOR; MEMBRANE PROTEIN; NIEMANN PICK C1 LIKE 1; PHOSPHOTYROSINE; PROTEIN ARH; PROTEIN DAB2; PROTEIN NUMB; UNCLASSIFIED DRUG; DAB2 PROTEIN, HUMAN; LDLR PROTEIN, HUMAN; LDLRAP1 PROTEIN, HUMAN; LOW DENSITY LIPOPROTEIN CHOLESTEROL; NERVE PROTEIN; NPC1L1 PROTEIN, HUMAN; NUMB PROTEIN, HUMAN; SIGNAL TRANSDUCING ADAPTOR PROTEIN; TUMOR SUPPRESSOR PROTEIN;

AMINO ACID SUBSTITUTION; ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BILE; BINDING AFFINITY; CHOLESTEROL TRANSPORT; CONTROLLED STUDY; ENDOCYTOSIS; ENZYME REGULATION; HUMAN; HUMAN TISSUE; LIPID ABSORPTION; LIVER; MOUSE; NONHUMAN; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN INTERACTION; PROTEIN POLYMORPHISM; PROTEIN TRANSPORT; RAT; ACTIVE TRANSPORT; ANIMAL; GENETICS; METABOLISM; MISSENSE MUTATION; PHYSIOLOGY; TUMOR CELL LINE;

ADAPTOR PROTEINS, SIGNAL TRANSDUCING; AMINO ACID SUBSTITUTION; ANIMALS; BIOLOGICAL TRANSPORT, ACTIVE; CELL LINE, TUMOR; CHOLESTEROL, LDL; ENDOCYTOSIS; HUMANS; MEMBRANE PROTEINS; MUTATION, MISSENSE; NERVE TISSUE PROTEINS; RATS; RECEPTORS, LDL; TUMOR SUPPRESSOR PROTEINS;

EID: 84912122936     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M114.593764     Document Type: Article

References (41)

1. Abifadel, M., Varret, M., Rabès, J. P., Allard, D., Ouguerram, K., Devillers, M., Cruaud, C., Benjannet, S., Wickham, L., Erlich, D., Derré, A., Villéger, L., Farnier, M., Beucler, I., Bruckert, E., Chambaz, J., Chanu, B., Lecerf, J. M., Luc, G., Moulin, P., Weissenbach, J., Prat, A., Krempf, M., Junien, C., Seidah, N. G., and Boileau, C. (2003) Mutations in PCSK9 cause autosomal dominant hypercholesterolemia. Nat. Genet. 34, 154-156
2. Brown, M. S., and Goldstein, J. L. (1999) A proteolytic pathway that controls the cholesterol content of membranes, cells, and blood. Proc. Natl. Acad. Sci. U.S.A. 96, 11041-11048
3. Ge, L., Wang, J., Qi, W., Miao, H. H., Cao, J., Qu, Y. X., Li, B. L., and Song, B. L. (2008) The cholesterol absorption inhibitor ezetimibe acts by blocking the sterol-induced internalization of NPC1L1. Cell Metab. 7, 508-519
4. Goldstein, J. L., and Brown, M. S. (2009) The LDL receptor. Arterioscler. Thromb. Vasc. Biol. 29, 431-438
5. Brown, M. S., and Goldstein, J. L. (1986) A receptor-mediated pathway for cholesterol homeostasis. Science 232, 34-47
6. Chen, W. J., Goldstein, J. L., and Brown, M. S. (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, 3116-3123
7. Davis, C. G., Lehrman, M. A., Russell, D. W., Anderson, R. G., Brown, M. S., and Goldstein, J. L. (1986) The J.D. mutation in familial hypercholesterolemia: amino acid substitution in cytoplasmic domain impedes internalization of LDL receptors. Cell 45, 15-24
8. Garcia, C. K., Wilund, K., Arca, M., Zuliani, G., Fellin, R., Maioli, M., Calandra, S., Bertolini, S., Cossu, F., Grishin, N., Barnes, R., Cohen, J. C., and Hobbs, H. H. (2001) Autosomal recessive hypercholesterolemia caused by mutations in a putative LDL receptor adaptor protein. Science 292, 1394-1398
9. He, G., Gupta, S., Yi, M., Michaely, P., Hobbs, H. H., and Cohen, J. C. (2002) ARH is a modular adaptor protein that interacts with the LDL receptor, clathrin, and AP-2. J. Biol. Chem. 277, 44044-44049
10. Maurer, M. E., and Cooper, J. A. (2006) The adaptor protein Dab2 sorts LDL receptors into coated pits independently of AP-2 and ARH. J. Cell Sci. 119, 4235-4246
11. Jones, C., Hammer, R. E., Li, W. P., Cohen, J. C., Hobbs, H. H., and Herz, J. (2003) Normal sorting but defective endocytosis of the low density lipoprotein receptor in mice with autosomal recessive hypercholesterolemia. J. Biol. Chem. 278, 29024-29030
12. Zuliani, G., Arca, M., Signore, A., Bader, G., Fazio, S., Chianelli, M., Bellosta, S., Campagna, F., Montali, A., Maioli, M., Pacifico, A., Ricci, G., and Fellin, R. (1999) Characterization of a new form of inherited hypercholesterolemia: familial recessive hypercholesterolemia. Arterioscler. Thromb. Vasc. Biol. 19, 802-809
13. Altmann, S. W., Davis, H. R., Jr., Zhu, L. J., Yao, X., Hoos, L. M., Tetzloff, G., Iyer, S. P., Maguire, M., Golovko, A., Zeng, M., Wang, L., Murgolo, N., and Graziano, M. P. (2004) Niemann-Pick C1 Like 1 protein is critical for intestinal cholesterol absorption. Science 303, 1201-1204
14. Wang, L. J., and Song, B. L. (2012) Niemann-Pick C1-Like 1 and cholesterol uptake. Biochim. Biophys. Acta 1821, 964-972
15. Li, P. S., Fu, Z. Y., Zhang, Y. Y., Zhang, J. H., Xu, C. Q., Ma, Y. T., Li, B. L., and Song, B. L. (2014) The clathrin adaptor Numb regulates intestinal cholesterol absorption through dynamic interaction with NPC1L1. Nat. Med. 20, 80-86
16. Traub, L. M. (2009) Tickets to ride: selecting cargo for clathrin-regulated internalization. Nat. Rev. Mol. Cell Biol. 10, 583-596
17. Uhlik, M. T., Temple, B., Bencharit, S., Kimple, A. J., Siderovski, D. P., and Johnson, G. L. (2005) Structural and evolutionary division of phosphotyrosine binding (PTB) domains. J. Mol. Biol. 345, 1-20
18. Nishimura, T., and Kaibuchi, K. (2007) Numb controls integrin endocytosis for directional cell migration with aPKC and PAR-3. Dev. Cell 13, 15-28
19. Teckchandani, A., Toida, N., Goodchild, J., Henderson, C., Watts, J., Wollscheid, B., and Cooper, J. A. (2009) Quantitative proteomics identifies a Dab2/integrin module regulating cell migration. J. Cell Biol. 186, 99-111
20. Gulino, A., Di Marcotullio, L., and Screpanti, I. (2010) The multiple functions of Numb. Exp. Cell Res. 316, 900-906
21. Goldstein, J. L., Basu, S. K., and Brown, M. S. (1983) Receptor-mediated endocytosis of low-density lipoprotein in cultured cells. Methods Enzymol. 98, 241-260
22. Fang, L., Garuti, R., Kim, B. Y., Wade, J. B., and Welling, P. A. (2009) The ARH adaptor protein regulates endocytosis of the ROMK potassium secretory channel in mouse kidney. J. Clin. Invest. 119, 3278-3289
23. Brown, A. J., Sun, L., Feramisco, J. D., Brown, M. S., and Goldstein, J. L. (2002) Cholesterol addition to ER membranes alters conformation of SCAP, the SREBP escort protein that regulates cholesterol metabolism. Mol. Cell 10, 237-245
24. Luo, J., Deng, Z. L., Luo, X., Tang, N., Song, W. X., Chen, J., Sharff, K. A., Luu, H. H., Haydon, R. C., Kinzler, K. W., Vogelstein, B., and He, T. C. (2007) Aprotocol for rapid generation of recombinant adenoviruses using the AdEasy system. Nat. Protoc. 2, 1236-1247
25. Redgrave, T. G., Roberts, D. C., and West, C. E. (1975) Separation of plasma lipoproteins by density-gradient ultracentrifugation. Anal. Biochem. 65, 42-49
26. Pitas, R. E., Innerarity, T. L., Weinstein, J. N., and Mahley, R. W. (1981) Acetoacetylated lipoproteins used to distinguish fibroblasts from macrophages in vitro by fluorescence microscopy. Arteriosclerosis 1, 177-185
27. Ranganathan, S., Liu, C. X., Migliorini, M. M., Von Arnim, C. A., Peltan, I. D., Mikhailenko, I., Hyman, B. T., and Strickland, D. K. (2004) Serine and threonine phosphorylation of the low density lipoprotein receptor-related protein by protein kinase Cα regulates endocytosis and association with adaptor molecules. J. Biol. Chem. 279, 40536-40544
28. Verdi, J. M., Bashirullah, A., Goldhawk, D. E., Kubu, C. J., Jamali, M., Meakin, S. O., and Lipshitz, H. D. (1999) Distinct human NUMB isoforms regulate differentiation versus proliferation in the neuronal lineage. Proc. Natl. Acad. Sci. U.S.A. 96, 10472-10476
29. Davies, J. P., Scott, C., Oishi, K., Liapis, A., and Ioannou, Y. A. (2005) Inactivation of NPC1L1 causes multiple lipid transport defects and protects against diet-induced hypercholesterolemia. J. Biol. Chem. 280, 12710-12720
30. Temel, R. E., Tang, W., Ma, Y., Rudel, L. L., Willingham, M. C., Ioannou, Y. A., Davies, J. P., Nilsson, L. M., and Yu, L. (2007) Hepatic Niemann-Pick C1-like 1 regulates biliary cholesterol concentration and is a target of ezetimibe. J. Clin. Invest. 117, 1968-1978
31. Wang, L. J., Wang, J., Li, N., Ge, L., Li, B. L., and Song, B. L. (2011) Molecular characterization of the NPC1L1 variants identified from cholesterol low absorbers. J. Biol. Chem. 286, 7397-7408
32. Li, N., Wang, H., Yan, Z., Yao, X., Hong, J., and Zhou, L. (2012) Ethnic disparities in the clustering of risk factors for cardiovascular disease among the Kazakh, Uygur, Mongolian and Han populations of Xinjiang: a cross-sectional study. BMC Public Health 12, 499
33. Tao, J., Ma, Y. T., Xiang, Y., Xie, X., Yang, Y. N., Li, X. M., Fu, Z. Y., Ma, X., Liu, F., Chen, B. D., Yu, Z. X., and Chen, Y. (2013) Prevalence of major cardiovascular risk factors and adverse risk profiles among three ethnic groups in the Xinjiang Uygur Autonomous Region, China. Lipids Health Dis. 12, 185
34. Santolini, E., Puri, C., Salcini, A. E., Gagliani, M. C., Pelicci, P. G., Tacchetti, C., and Di Fiore, P. P. (2000) Numb is an endocytic protein. J. Cell Biol. 151, 1345-1352
35. Kim, K. K., Nam, J., Mukouyama, Y. S., and Kawamoto, S. (2013) Rbfox3- regulated alternative splicing of Numb promotes neuronal differentiation during development. J. Cell Biol. 200, 443-458
36. Li, S. C., Zwahlen, C., Vincent, S. J., McGlade, C. J., Kay, L. E., Pawson, T., and Forman-Kay, J. D. (1998) Structure of a Numb PTB domain-peptide complex suggests a basis for diverse binding specificity. Nat. Struct. Biol. 5, 1075-1083
37. Zwahlen, C., Li, S. C., Kay, L. E., Pawson, T., and Forman-Kay, J. D. (2000) Multiple modes of peptide recognition by the PTB domain of the cell fate determinant Numb. EMBO J. 19, 1505-1515
38. Zong, F. Y., Fu, X., Wei, W. J., Luo, Y. G., Heiner, M., Cao, L. J., Fang, Z., Fang, R., Lu, D., Ji, H., and Hui, J. (2014) The RNA-binding protein QKI suppresses cancer-associated aberrant splicing. PLoS Genet. 10, e1004289
39. Bechara, E. G., Sebestyén, E., Bernardis, I., Eyras, E., and Valcárcel, J. (2013) RBM5, 6, and 10 differentially regulate NUMB alternative splicing to control cancer cell proliferation. Mol. Cell 52, 720-733
40. Cohen, J., Pertsemlidis, A., Kotowski, I. K., Graham, R., Garcia, C. K., and Hobbs, H. H. (2005) Low LDL cholesterol in individuals of African descent resulting from frequent nonsense mutations in PCSK9. Nat. Genet. 37, 161-165
41. Kotowski, I. K., Pertsemlidis, A., Luke, A., Cooper, R. S., Vega, G. L., Cohen, J. C., and Hobbs, H. H. (2006) A spectrum of PCSK9 alleles contributes to plasma levels of low-density lipoprotein cholesterol. Am. J. Hum. Genet. 78, 410-422