AMN directs endocytosis of the intrinsic factor-vitamin B12 receptor cubam by engaging ARH or Dab2

Traffic

Volumn 11, Issue 5, 2010, Pages 706-720

  Pedersen, Gitte Albinus ^a   Chakraborty, Souvik ^b   Steinhauser, Amie L ^b   Traub, Linton M ^b   Madsen, Mette ^a  

^a AARHUS UNIVERSITY   (Denmark)

^b UNIVERSITY OF PITTSBURGH SCHOOL OF MEDICINE   (United States)

Author keywords

FY NPX FY sorting signal; Amnionless; ARH; Clathrin; Cubilin; Dab2; Endocytosis; Internalization; Receptor; Vitamin B12

Indexed keywords

AMNIONLESS PROTEIN; AUTOSOMAL RECESSIVE HYPERCHOLESTEROLEMIA PROTEIN; BINDING PROTEIN; CUBAM; CUBILIN; DISABLED 2 PROTEIN; MUTANT PROTEIN; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; CONTROLLED STUDY; ENDOCYTOSIS; HUMAN; HUMAN CELL; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN FAMILY; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; SIGNAL TRANSDUCTION; YEAST;

ADAPTOR PROTEINS, VESICULAR TRANSPORT; ANIMALS; APOLIPOPROTEIN A-I; CRICETINAE; ENDOCYTOSIS; HUMANS; HYPERCHOLESTEROLEMIA; INTRINSIC FACTOR; MUTATION; PROTEIN BINDING; PROTEIN TRANSPORT; PROTEINS; RECEPTORS, CELL SURFACE; RECEPTORS, LDL; SIGNAL TRANSDUCTION; VITAMIN B 12; VITAMIN D-BINDING PROTEIN;

EID: 77953152356     PISSN: 13989219     EISSN: 16000854     Source Type: Journal    
DOI: 10.1111/j.1600-0854.2010.01042.x     Document Type: Article

References (65)

1. Fyfe JC, Madsen M, Hojrup P, Christensen EI, Tanner SM, de la Chapelle A, He Q, Moestrup SK. The functional cobalamin (vitamin B-12)-intrinsic factor receptor is a novel complex of cubilin and amnionless. Blood 2004, 103:1573-1579.
2. Sahali D, Mulliez N, Chatelet F, Dupuis R, Ronco P, Verroust P. Characterization of a 280-kD protein restricted to the coated pits of the renal brush border and the epithelial cells of the yolk sac. Teratogenic effect of the specific monoclonal antibodies. J Exp Med 1988, 167:213-218.
3. Seetharam B, Christensen EI, Moestrup SK, Hammond TG, Verroust PJ. Identification of rat yolk sac target protein of teratogenic antibodies, gp280, as intrinsic factor-cobalamin receptor. J Clin Invest 1997, 99:2317-2322.
4. Strope S, Rivi R, Metzger T, Manova K, Lacy E. Mouse amnionless, which is required for primitive streak assembly, mediates cell-surface localization and endocytic function of cubilin on visceral endoderm and kidney proximal tubules. Development 2004, 131:4787-4795.
5. Birn H, Fyfe JC, Jacobsen C, Mounier F, Verroust PJ, Orskov H, Willnow TE, Moestrup SK, Christensen EI. Cubilin is an albumin binding protein important for renal tubular albumin reabsorption. J Clin Invest 2000, 105:1353-1361.
6. Kozyraki R, Fyfe J, Verroust PJ, Jacobsen C, Dautry-Varsat A, Gburek J, Willnow TE, Christensen EI, Moestrup SK. Megalin-dependent cubilin-mediated endocytosis is a major pathway for the apical uptake of transferrin in polarized epithelia. Proc Natl Acad Sci U S A 2001, 98:12491-12496.
7. Kozyraki R, Fyfe J, Kristiansen M, Gerdes C, Jacobsen C, Cui S, Christensen EI, Aminoff M, de la Chapelle A, Krahe R, Verroust PJ, Moestrup SK. The intrinsic factor-vitamin B12 receptor, cubilin, is a high-affinity apolipoprotein A-I receptor facilitating endocytosis of high-density lipoprotein. Nat Med 1999, 5:656-661.
8. Nykjaer A, Fyfe JC, Kozyraki R, Leheste JR, Jacobsen C, Nielsen MS, Verroust PJ, Aminoff M, de la Chapelle A, Moestrup SK, Ray R, Gliemann J, Willnow TE, Christensen EI. Cubilin dysfunction causes abnormal metabolism of the steroid hormone 25(OH) vitamin D3. Proc Natl Acad Sci U S A 2001, 98:13895-13900.
9. Kozyraki R, Kristiansen M, Silahtaroglu A, Hansen C, Jacobsen C, Tommerup N, Verroust PJ, Moestrup SK. The human intrinsic factor-vitamin B12 receptor, cubilin: molecular characterization and chromosomal mapping of the gene to 10p within the autosomal recessive megaloblastic anemia (MGA1) region. Blood 1998, 91:3593-3600.
10. Moestrup SK, Kozyraki R, Kristiansen M, Kaysen JH, Rasmussen HH, Brault D, Pontillon F, Goda FO, Christensen EI, Hammond TG, Verroust PJ. The intrinsic factor-vitamin B12 receptor and target of teratogenic antibodies is a megalin-binding peripheral membrane protein with homology to developmental proteins. J Biol Chem 1998, 273:5235-5242.
11. Kalantry S, Manning S, Haub O, Tomihara-Newberger C, Lee HG, Fangman J, Disteche CM, Manova K, Lacy E. The amnionless gene, essential for mouse gastrulation, encodes a visceral-endoderm-specific protein with an extracellular cysteine-rich domain. Nat Genet 2001, 27:412-416.
12. Tanner SM, Aminoff M, Wright FA, Liyanarachchi S, Kuronen M, Saarinen A, Massika O, Mandel H, Broch H, de la Chapelle A. Amnionless, essential for mouse gastrulation, is mutated in recessive hereditary megaloblastic anemia. Nat Genet 2003, 33:426-429.
13. Chen WJ, Goldstein JL, Brown MS. NPXY, a sequence often found in cytoplasmic tails, is required for coated pit-mediated internalization of the low density lipoprotein receptor. J Biol Chem 1990, 265:3116-3123.
14. Bonifacino JS, Traub LM. Signals for sorting of transmembrane proteins to endosomes and lysosomes. Annu Rev Biochem 2003, 72:395-447.
15. Traub LM. Tickets to ride: selecting cargo for clathrin-regulated internalization. Nat Rev Mol Cell Biol 2009, 10:583-596.
16. Stolt PC, Bock HH. Modulation of lipoprotein receptor functions by intracellular adaptor proteins. Cell Signal 2006, 18:1560-1571.
17. He G, Gupta S, Yi M, Michaely P, Hobbs HH, Cohen JC. ARH is a modular adaptor protein that interacts with the LDL receptor, clathrin, and AP-2. J Biol Chem 2002, 277:44044-44049.
18. Maurer ME, Cooper JA. Endocytosis of megalin by visceral endoderm cells requires the Dab2 adaptor protein. J Cell Sci 2005, 118:5345-5355.
19. Nagai M, Meerloo T, Takeda T, Farquhar MG. The adaptor protein ARH escorts megalin to and through endosomes. Mol Biol Cell 2003, 14:4984-4996.
20. Oleinikov AV, Zhao J, Makker SP. Cytosolic adaptor protein Dab2 is an intracellular ligand of endocytic receptor gp600/megalin. Biochem J 2000, 347:613-621.
21. Mameza MG, Lockard JM, Zamora E, Hillefors M, Lavina ZS, Kaplan BB. Characterization of the adaptor protein ARH expression in the brain and ARH molecular interactions. J Neurochem 2007, 103:927-941.
22. Morris SM, Cooper JA. Disabled-2 colocalizes with the LDLR in clathrin-coated pits and interacts with AP-2. Traffic 2001, 2:111-123.
23. Davis CG, van Driel IR, Russell DW, Brown MS, Goldstein JL. The low density lipoprotein receptor. Identification of amino acids in cytoplasmic domain required for rapid endocytosis. J Biol Chem 1987, 262:4075-4082.
24. Coudroy G, Gburek J, Kozyraki R, Madsen M, Trugnan G, Moestrup SK, Verroust PJ, Maurice M. Contribution of cubilin and amnionless to processing and membrane targeting of cubilin-amnionless complex. J Am Soc Nephrol 2005, 16:2330-2337.
25. He Q, Madsen M, Kilkenney A, Gregory B, Christensen EI, Vorum H, Højrup P, Schäffer AA, Kirkness EF, Tanner SM, de la Chapelle A, Giger U, Moestrup SK, Fyfe JC. Amnionless function is required for cubilin brush-border expression and intrinsic factor-cobalamin (vitamin B12) absorption in vivo. Blood 2005, 106:1447-1453.
26. Hawryluk MJ, Keyel PA, Mishra SK, Watkins SC, Heuser JE, Traub LM. Epsin 1 is a polyubiquitin-selective clathrin-associated sorting protein. Traffic 2006, 7:262-281.
27. Humphrey JS, Peters PJ, Yuan LC, Bonifacino JS. Localization of TGN38 to the trans-Golgi network: involvement of a cytoplasmic tyrosine-containing sequence. J Cell Biol 1993, 120:1123-1135.
28. Eden ER, Sun XM, Patel DD, Soutar AK. Adaptor protein Disabled-2 modulates low density lipoprotein receptor synthesis in fibroblasts from patients with autosomal recessive hypercholesterolaemia. Hum Mol Gen 2007, 16:2751-2759.
29. Keyel PA, Mishra SK, Roth R, Heuser JE, Watkins SC, Traub LM. A single common portal for clathrin-mediated endocytosis of distinct cargo governed by cargo-selective adaptors. Mol Biol Cell 2006, 17:4300-4317.
30. Maurer ME, Cooper JA. The adaptor protein Dab2 sorts LDL receptors into coated pits independently of AP-2 and ARH. J Cell Sci 2006, 119:4235-4246.
31. Davis CG, Lehrman MA, Russell DW, Anderson RG, Brown MS, Goldstein JL. The J. D. mutation in familial hypercholesterolemia: Amino acid substitution in cytoplasmic domain impedes internalization of LDL receptors. Cell 1986, 45:15-24.
32. Hopps HE, Bernheim BC, Nisalak A, Tjio JH, Smadel JE. Biologic characteristics of a continuous kidney cell line derived from the african green monkey. J Immunol 1963, 91:416-424.
33. Mishra SK, Watkins SC, Traub LM. The autosomal recessive hypercholesterolemia (ARH) protein interfaces directly with the clathrin-coat machinery. Proc Natl Acad Sci U S A 2002, 99:16099-16104.
34. Abera AB, Marais AD, Raal FJ, Leisegang F, Jones S, George P, Henderson HE. Autosomal recessive hypercholesterolaemia: discrimination of ARH protein and LDLR function in the homozygous FH phenotype. Clin Chim Acta 2007, 378:33-37.
35. Garcia CK, Wilund K, Arca M, Zuliani G, Fellin R, Maioli M, Calandra S, Bertolini S, Cossu F, Grishin N, Barnes R, Cohen JC, Hobbs HH. Autosomal recessive hypercholesterolemia caused by mutations in a putative LDL receptor adaptor protein. Science 2001, 292:1394-1398.
36. Warren RA, Green FA, Stenberg PE, Enns CA. Distinct saturable pathways for the endocytosis of different tyrosine motifs. J Biol Chem 1998, 273:17056-17063.
37. Marks MS, Woodruff L, Ohno H, Bonifacino JS. Protein targeting by tyrosine- and di-leucine-based signals: evidence for distinct saturable components. J Cell Biol 1996, 135:341-354.
38. Pandey MS, Harris EN, Weigel JA, Weigel PH. The cytoplasmic domain of the hyaluronan receptor for endocytosis (HARE) contains multiple endocytic motifs targeting coated pit-mediated internalization. J Biol Chem 2008, 283:21453-21461.
39. Kelly BT, McCoy AJ, Spate K, Miller SE, Evans PR, Honing S, Owen DJ. A structural explanation for the binding of endocytic dileucine motifs by the AP2 complex. Nature 2008, 456:976-979.
40. Ohno H, Stewart J, Fournier MC, Bosshart H, Rhee I, Miyatake S, Saito T, Gallusser A, Kirchhausen T, Bonifacino JS. Interaction of tyrosine-based sorting signals with clathrin-associated proteins. Science 1995, 269:1872-1875.
41. Owen DJ, Evans PR. A structural explanation for the recognition of tyrosine-based endocytotic signals. Science 1998, 282:1327-1332.
42. Collins BM, McCoy AJ, Kent HM, Evans PR, Owen DJ. Molecular architecture and functional model of the endocytic AP2 complex. Cell 2002, 109:523-535.
43. Robinson MS. Adaptable adaptors for coated vesicles. Trends Cell Biol 2004, 14:167-174.
44. Maldonado-Baez L, Wendland B. Endocytic adaptors: recruiters, coordinators and regulators. Trends Cell Biol 2006, 16:505-513.
45. Schmid EM, McMahon HT. Integrating molecular and network biology to decode endocytosis. Nature 2007, 448:883-888.
46. Anzenberger U, Bit-Avragim N, Rohr S, Rudolph F, Dehmel B, Willnow TE, Abdelilah-Seyfried S. Elucidation of megalin/LRP2-dependent endocytic transport processes in the larval zebrafish pronephros. J Cell Sci 2006, 119:2127-2137.
47. Covassin L, Amigo JD, Suzuki K, Teplyuk V, Straubhaar J, Lawson ND. Global analysis of hematopoietic and vascular endothelial gene expression by tissue specific microarray profiling in zebrafish. Dev Biol 2006, 299:551-562.
48. Jones C, Hammer RE, Li WP, Cohen JC, Hobbs HH, Herz J. Normal sorting but defective endocytosis of the low density lipoprotein receptor in mice with autosomal recessive hypercholesterolemia. J Biol Chem 2003, 278:29024-29030.
49. Morris SM, Tallquist MD, Rock CO, Cooper JA. Dual roles for the Dab2 adaptor protein in embryonic development and kidney transport. EMBO J 2002, 21:1555-1564.
50. Ruan J, Li H, Chen Z, Coghlan A, Coin LJ, Guo Y, Hériché JK, Hu Y, Kristiansen K, Li R, Liu T, Moses A, Qin J, Vang S, Vilella AJ. TreeFam: 2008 Update. Nucleic Acids Res 2008, 36:D735-D740.
51. Warren WC, Hillier LW, Marshall Graves JA, Birney E, Ponting CP, Grützner F, Belov K, Miller W, Clarke L, Chinwalla AT, Yang SP, Heger A, Locke DP, Miethke P, Waters PD. Genome analysis of the platypus reveals unique signatures of evolution. Nature 2008, 453:175-183.
52. Rohrer J, Schweizer A, Russell D, Kornfeld S. The targeting of Lamp1 to lysosomes is dependent on the spacing of its cytoplasmic tail tyrosine sorting motif relative to the membrane. J Cell Biol 1996, 132:565-576.
53. Leheste JR, Rolinski B, Vorum H, Hilpert J, Nykjaer A, Jacobsen C, Aucouturier P, Moskaug JO, Otto A, Christensen EI, Willnow TE. Megalin knockout mice as an animal model of low molecular weight proteinuria. Am J Pathol 1999, 155:1361-1370.
54. Nagai J, Christensen EI, Morris SM, Willnow TE, Cooper JA, Nielsen R. Mutually dependent localization of megalin and Dab2 in the renal proximal tubule. Am J Physiol Renal Physiol 2005, 289:F569-F576.
55. Mishra SK, Keyel PA, Hawryluk MJ, Agostinelli NR, Watkins SC, Traub LM. Disabled-2 exhibits the properties of a cargo-selective endocytic clathrin adaptor. EMBO J 2002, 21:4915-4926.
56. Mishra SK, Keyel PA, Edeling MA, Dupin AL, Owen DJ, Traub LM. Functional dissection of an AP-2 β2 appendage-binding sequence within the autosomal recessive hypercholesterolemia protein. J Biol Chem 2005, 280:19270-19280.
57. Edeling MA, Mishra SK, Keyel PA, Steinhauser AL, Collins BM, Roth R, Heuser JE, Owen DJ, Traub LM. Molecular switches involving the AP-2 β2 appendage regulate endocytic cargo selection and clathrin coat assembly. Dev Cell 2006, 10:329-342.
58. Schmid EM, Ford MG, Burtey A, Praefcke GJ, Peak-Chew SY, Mills IG, Benmerah A, McMahon HT. Role of the AP2 β-appendage hub in recruiting partners for clathrin-coated vesicle assembly. PLoS Biol 2006, 4:e262.
59. Soutar AK, Naoumova RP. Mechanisms of disease: genetic causes of familial hypercholesterolemia. Nat Clin Pract Cardiovasc Med 2007, 4:214-225.
60. Fang L, Garuti R, Kim BY, Wade JB, Welling PA. The ARH adaptor protein regulates endocytosis of the ROMK potassium secretory channel in mouse kidney. J Clin Invest 2009, 119:3278-3289.
61. Nathke IS, Heuser J, Lupas A, Stock J, Turck CW, Brodsky FM. Folding and trimerization of clathrin subunits at the triskelion hub. Cell 1992, 68:899-910.
62. Ahle S, Mann A, Eichelsbacher U, Ungewickell E. Structural relationships between clathrin assembly proteins from the Golgi and the plasma membrane. EMBO J 1988, 7:919-929.
63. Traub LM, Bannykh SI, Rodel JE, Aridor M, Balch WE, Kornfeld S. AP-2-containing clathrin coats assemble on mature lysosomes. J Cell Biol 1996, 135:1801-1814.
64. Chiu J, March PE, Lee R, Tillett D. Site-directed, ligase-independent mutagenesis (SLIM): a single-tube methodology approaching 100% efficiency in 4 h. Nucl Acids Res 2004, 32:e174.
65. Elbashir SM, Harborth J, Lendeckel W, Yalcin A, Weber K, Tuschl T. Duplexes of 21-nucleotide RNAs mediate RNA interference in cultured mammalian cells. Nature 2001, 411:494-498.