New horizons for lipoprotein receptors: Communication by β-propellers

Journal of Lipid Research

Volumn 54, Issue 10, 2013, Pages 2763-2774

  Andersen, Olav M ^a   Dagil, Robert ^b   Kragelund, Birthe B ^b  

^a AARHUS UNIVERSITY   (Denmark)

^b UNIVERSITY OF COPENHAGEN   (Denmark)

Author keywords

Endocytosis; Internalisation; Ligand recognition motif; Ligand release; Structure; Tyr Trp Thr Asp propeller

Indexed keywords

LIPOPROTEIN RECEPTOR;

AMINO TERMINAL SEQUENCE; ARTICLE; BETA PROPELLER; BETA SHEET; BINDING SITE; DISULFIDE BOND; LIGAND BINDING; MOLECULAR RECOGNITION; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN DOMAIN; PROTEIN FOLDING; PROTEIN INTERACTION; PROTEIN MOTIF; PROTEIN STRUCTURE; RECEPTOR BINDING; SEQUENCE ALIGNMENT; SEQUENCE ANALYSIS; SIGNAL TRANSDUCTION; STRUCTURE ACTIVITY RELATION;

ENDOCYTOSIS; INTERNALISATION; LIGAND RECOGNITION MOTIF; LIGAND RELEASE; STRUCTURE; TYR-TRP-THR-ASP Β-PROPELLER;

AMINO ACID SEQUENCE; HUMANS; HYDROGEN-ION CONCENTRATION; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; PROTEIN INTERACTION DOMAINS AND MOTIFS; PROTEIN STRUCTURE, SECONDARY; RECEPTORS, LIPOPROTEIN; SEQUENCE HOMOLOGY, AMINO ACID; SIGNAL TRANSDUCTION; STRUCTURAL HOMOLOGY, PROTEIN;

EID: 84884147067     PISSN: 00222275     EISSN: 15397262     Source Type: Journal    
DOI: 10.1194/jlr.M039545     Document Type: Article

References (82)

1. Springer, T. A. 1998. An extracellular beta-propeller module predicted in lipoprotein and scavenger receptors, tyrosine kinases, epidermal growth factor precursor, and extracellular matrix components. J. Mol. Biol. 283: 837-862.
2. Bazan, J. F. 1990. Structural design and molecular evolution of a cytokine receptor superfamily. Proc. Natl. Acad. Sci. USA. 87: 6934-6938.
3. Jacobsen, L., P. Madsen, S. K. Moestrup, A. H. Lund, N. Tommerup, A. Nykjaer, L. Sottrup-Jensen, J. Gliemann, and C. M. Petersen. 1996. Molecular characterization of a novel human hybrid-type receptor that binds the alpha2-macroglobulin receptor-associated protein. J. Biol. Chem. 271: 31379-31383.
4. Russell, D. W., M. S. Brown, and J. L. Goldstein. 1989. Different combinations of cysteine-rich repeats mediate binding of low density lipoprotein receptor to two different proteins. J. Biol. Chem. 264: 21682-21688.
5. Herz, J., and D. K. Strickland. 2001. LRP: a multifunctional scavenger and signaling receptor. J. Clin. Invest. 108: 779-784.
6. Jeon, H., W. Meng, J. Takagi, M. J. Eck, T. A. Springer, and S. C. Blacklow. 2001. Implications for familial hypercholesterolemia from the structure of the LDL receptor YWTD-EGF domain pair. Nat. Struct. Biol. 8: 499-504.
7. Takagi, J., Y. Yang, J. H. Liu, J. H. Wang, and T. A. Springer. 2003. Complex between nidogen and laminin fragments reveals a paradigmatic beta-propeller interface. Nature. 424: 969-974.
8. Rudenko, G., L. Henry, K. Henderson, K. Ichtchenko, M. S. Brown, J. L. Goldstein, and J. Deisenhofer. 2002. Structure of the LDL receptor extracellular domain at endosomal pH. Science. 298: 2353-2358.
9. Bourhis, E., W. Wang, C. Tam, J. Hwang, Y. Zhang, D. Spittler, O. W. Huang, Y. Gong, A. Estevez, I. Zilberleyb, et al. 2011. Wnt antagonists bind through a short peptide to the first b-propeller domain of LRP5/6. Structure. 19: 1433-1442.
10. Cheng, Z., T. Biechele, Z. Wei, S. Morrone, R. T. Moon, L. Wang, and W. Xu. 2011. Crystal structures of the extracellular domain of LRP6 and its complex with DKK1. Nat. Struct. Mol. Biol. 18: 1204-1210.
11. Ahn, V. E., M. L. Chu, H. J. Choi, D. Tran, A. Abo, and W. I. Weis. 2011. Structural basis of Wnt signaling inhibition by Dickkopf binding to LRP5/6. Dev. Cell. 21: 862-873.
12. Hammes, A., T. K. Andreassen, R. Spoelgen, J. Raila, N. Hubner, H. Schulz, J. Metzger, F. J. Schweigert, P. B. Luppa, A. Nykjaer, et al. 2005. Role of endocytosis in cellular uptake of sex steroids. Cell. 122: 751-762.
13. Nykjær, A., D. Dragun, D. Walther, H. Vorum, C. Jacobsen, J. Herz, F. Melsen, E. I. Christensen, and T. E. Willnow. 1999. An endocytic pathway essential for renal uptake and activation of the steroid 25- (OH) vitamin D 3. Cell. 96: 507-515.
14. Semenov, M. V., K. Tamai, B. K. Brott, M. Kuhl, S. Sokol, and X. He. 2001. Head inducer Dickkopf-1 is a ligand for Wnt coreceptor LRP6. Curr. Biol. 11: 951-961.
15. Brott, B. K., and S. Y. Sokol. 2002. Regulation of Wnt/LRP signaling by distinct domains of Dickkopf proteins. Mol. Cell. Biol. 22: 6100-6110.
16. Mao, B., and C. Niehrs. 2003. Kremen2 modulates Dickkopf2 activity during Wnt/LRP6 signaling. Gene. 302: 179-183.
17. Li, L., J. Mao, L. Sun, W. Liu, and D. Wu. 2002. Second cysteinerich domain of Dickkopf-2 activates canonical Wnt signaling pathway via LRP-6 independently of dishevelled. J. Biol. Chem. 277: 5977-5981.
18. McCarthy, R. A., J. L. Barth, M. R. Chintalapudi, C. Knaak, and W. S. Argraves. 2002. Megalin functions as an endocytic sonic hedgehog receptor. J. Biol. Chem. 277: 25660-25667.
19. Christ, A., A. Christa, E. Kur, O. Lioubinski, S. Bachmann, T. E. Willnow, and A. Hammes. 2012. LRP2 is an auxiliary SHH receptor required to condition the forebrain ventral midline for inductive signals. Dev. Cell. 22: 268-278.
20. Spoelgen, R., A. Hammes, U. Anzenberger, D. Zechner, O. M. Andersen, B. Jerchow, and T. E. Willnow. 2005. LRP2/megalin is required for patterning of the ventral telencephalon. Development. 132: 405-414.
21. Gajera, C. R., H. Emich, O. Lioubinski, A. Christ, R. Beckervordersandforth-Bonk, K. Yoshikawa, S. Bachmann, E. I. Christensen, M. Gotz, G. Kempermann, et al. 2010. LRP2 in ependymal cells regulates BMP signaling in the adult neurogenic niche. J. Cell Sci. 123: 1922-1930.
22. Sonoda, I., I. Imoto, J. Inoue, T. Shibata, Y. Shimada, K. Chin, M. Imamura, T. Amagasa, J. W. Gray, S. Hirohashi, et al. 2004. Frequent silencing of low density lipoprotein receptor-related protein 1B (LRP1B) expression by genetic and epigenetic mechanisms in esophageal squamous cell carcinoma. Cancer Res. 64: 3741-3747.
23. Prazeres, H., J. Torres, F. Rodrigues, M. Pinto, M. C. Pastoriza, D. Gomes, J. Cameselle-Teijeiro, A. Vidal, T. C. Martins, M. Sobrinho-Simoes, et al. 2011. Chromosomal, epigenetic and microRNA-mediated inactivation of LRP1B, a modulator of the extracellular environment of thyroid cancer cells. Oncogene. 30: 1302-1317.
24. Cowin, P. A., J. George, S. Fereday, E. Loehrer, P. Van Loo, C. Cullinane, D. Etemadmoghadam, S. Ftouni, L. Galletta, M. S. Anglesio, et al. 2012. LRP1B deletion in high-grade serous ovarian cancers is associated with acquired chemotherapy resistance to liposomal doxorubicin. Cancer Res. 72: 4060-4073.
25. Lo Surdo, P., M. J. Bottomley, A. Calzetta, E. C. Settembre, A. Cirillo, S. Pandit, Y. G. Ni, B. Hubbard, A. Sitlani, and A. Carfi. 2011. Mechanistic implications for LDL receptor degradation from the PCSK9/LDLR structure at neutral pH. EMBO Rep. 12: 1300-1305.
26. Kim, D. H., Y. Inagaki, T. Suzuki, R. X. Ioka, S. Z. Yoshioka, K. Magoori, M. J. Kang, Y. Cho, A. Z. Nakano, Q. Liu, et al. 1998. A new low density lipoprotein receptor related protein, LRP5, is expressed in hepatocytes and adrenal cortex, and recognizes apolipoprotein E. J. Biochem. 124: 1072-1076.
27. UniProt Consortium. 2012. Reorganizing the protein space at the Universal Protein Resource (UniProt). Nucleic Acids Res. 40: D71 - D75.
28. Letunic, I., T. Doerks, and P. Bork. 2012. SMART 7: recent updates to the protein domain annotation resource. Nucleic Acids Res. 40: D302 - D305.
29. Schultz, J., F. Milpetz, P. Bork, and C. P. Ponting. 1998. SMART, a simple modular architecture research tool: identification of signaling domains. Proc. Natl. Acad. Sci. USA. 95: 5857-5864.
30. Notredame, C., D. G. Higgins, and J. Heringa. 2000. T-Coffee: a novel method for fast and accurate multiple sequence alignment. J. Mol. Biol. 302: 205-217.
31. Arnold, K., L. Bordoli, J. Kopp, and T. Schwede. 2006. The SWISSMODEL workspace: a web-based environment for protein structure homology modelling. Bioinformatics. 22: 195-201.
32. Mayer, U., E. Kohfeldt, and R. Timpl. 1998. Structural and genetic analysis of laminin-nidogen interaction. Ann. N. Y. Acad. Sci. 857: 130-142.
33. Willem, M., N. Miosge, W. Halfter, N. Smyth, I. Jannetti, E. Burghart, R. Timpl, and U. Mayer. 2002. Specific ablation of the nidogenbinding site in the laminin gamma1 chain interferes with kidney and lung development. Development. 129: 2711-2722.
34. Andersen, O. M., R. Reiche, V. Schmidt, M. Gotthardt, R. Spoelgen, J. Behlke, C. A. Von Arnim, T. Breiderhoff, P. Jansen, X. Wu, et al. 2005. SorLA/LR11, a neuronal sorting receptor that regulates processing of the amyloid precursor protein. Proc. Natl. Acad. Sci. USA. 102: 13461-13466.
35. Sappington, T. W., and A. S. Raikhel. 1998. Ligand-binding domains in vitellogenin receptors and other LDL-receptor family members share a common ancestral ordering of cysteine-rich repeats. J. Mol. Evol. 46: 476-487.
36. Kwon, H. J., T. A. Lagace, M. C. McNutt, J. D. Horton, and J. Deisenhofer. 2008. Molecular basis for LDL receptor recognition by PCSK9. Proc. Natl. Acad. Sci. USA. 105: 1820-1825.
37. Marzolo, M. P., and P. Farfán. 2011. New insights into the roles of megalin/LRP2 and the regulation of its functional expression. Biol. Res. 44: 89-105.
38. Jensen, G. A., O. M. Andersen, A. M. Bonvin, I. Bjerrum-Bohr, M. Etzerodt, H. C. Thogersen, C. O'Shea, F. M. Poulsen, and B. B. Kragelund. 2006. Binding site structure of one LRP-RAP complex: implications for a common ligand-receptor binding motif. J. Mol. Biol. 362: 700-716.
39. Andersen, O. M., F. P. Schwarz, E. Eisenstein, C. Jacobsen, S. K. Moestrup, M. Etzerodt, and H. C. Thøgersen. 2001. Dominant thermodynamic role of the third independent receptor binding site in the receptor-associated protein RAP. Biochemistry. 40: 15408-15417.
40. Skeldal, S., J. V. Larsen, K. E. Pedersen, H. H. Petersen, R. Egelund, A. Christensen, J. K. Jensen, J. Gliemann, and P. A. Andreasen. 2006. Binding areas of urokinase-type plasminogen activator-plasminogen activator inhibitor-1 complex for endocytosis receptors of the low-density lipoprotein receptor family, determined by sitedirected mutagenesis. FEBS J. 273: 5143-5159.
41. Guttman, M., J. H. Prieto, J. E. Croy, and E. A. Komives. 2010. Decoding of lipoprotein-receptor interactions: properties of ligand binding modules governing interactions with apolipoprotein E. Biochemistry. 49: 1207-1216.
42. Yasui, N., T. Nogi, T. Kitao, Y. Nakano, M. Hattori, and J. Takagi. 2007. Structure of a receptor-binding fragment of reelin and mutational analysis reveal a recognition mechanism similar to endocytic receptors. Proc. Natl. Acad. Sci. USA. 104: 9988-9993.
43. Yasui, N., T. Nogi, and J. Takagi. 2010. Structural basis for specific recognition of reelin by its receptors. Structure. 18: 320-331.
44. Verdaguer, N., I. Fita, M. Reithmayer, R. Moser, and D. Blaas. 2004. X-ray structure of a minor group human rhinovirus bound to a fragment of its cellular receptor protein. Nat. Struct. Mol. Biol. 11: 429-434.
45. Fisher, C., N. Beglova, and S. C. Blacklow. 2006. Structure of an LDLR-RAP complex reveals a general mode for ligand recognition by lipoprotein receptors. Mol. Cell. 22: 277-283.
46. Lee, C. J., A. De Biasio, and N. Beglova. 2010. Mode of interaction between 2GPI and lipoprotein receptors suggests mutually exclusive binding of 2GPI to the receptors and anionic phospholipids. Structure. 18: 366-376.
47. Guttman, M., J. H. Prieto, T. M. Handel, P. J. Domaille, and E. A. Komives. 2010. Structure of the minimal interface between ApoE and LRP. J. Mol. Biol. 398: 306-319.
48. Dagil, R., C. O'Shea, A. Nykjaer, A. M. Bonvin, and B. B. Kragelund. 2013. Gentamicin binds to the megalin receptor as a competitive inhibitor using the common ligand binding motif of complement type repeats: insight from the NMR structure of the 10th complement type repeat domain alone and in complex with gentamicin. J. Biol. Chem. 288: 4424-4435.
49. Andersen, O. M., P. A. Christensen, L. L. Christensen, C. Jacobsen, S. K. Moestrup, M. Etzerodt, and H. C. Thøgersen. 2000. Specific binding of -macroglobulin to complement-type repeat CR4 of the low density lipoprotein receptor-related protein. Biochemistry. 39: 10627-10633.
50. Nielsen, K. L., T. L. Holtet, M. Etzerodt, S. K. Moestrup, J. Gliemann, L. Sottrup-Jensen, and H. C. Thøgersen. 1996. Identification of residues in -macroglobulins important for binding to the 2 - macroglobulin receptor/Low density lipoprotein receptor-related protein. J. Biol. Chem. 271: 12909-12912.
51. Rodenburg, K. W., L. Kjøller, H. H. Petersen, and P. A. Andreasen. 1998. Binding of urokinase-type plasminogen activator-plasminogen activator inhibitor-1 complex to the endocytosis receptors alpha2-macroglobulin receptor/low-density lipoprotein receptorrelated protein and very-low- density lipoprotein receptor involves basic residues in the inhibitor. Biochem. J. 329: 55-63.
52. Sarafanov, A. G., E. M. Makogonenko, O. M. Andersen, I. A. Mikhailenko, N. M. Ananyeva, A. V. Khrenov, M. Shima, D. K. Strickland, and E. L. Saenko. 2007. Localization of the low-density lipoprotein receptor-related protein regions involved in binding to the A2 domain of coagulation factor VIII. Thromb. Haemost. 98: 1170-1181.
53. Andersen, O. M., H. H. Petersen, C. Jacobsen, S. K. Moestrup, M. Etzerodt, P. A. Andreasen, and H. C. Thøgersen. 2001. Analysis of a two-domain binding site for the urokinase-type plasminogen activator - plasminogen activator inhibitor-1 complex in low density lipoprotein receptor-related protein. Biochem. J. 357: 289-296.
54. Bu, G., H. J. Geuze, G. J. Strous, and A. L. Schwartz. 1995. 39 kDa receptor-associated protein is an ER resident protein and molecular chaperone for LDL receptor-related protein. EMBO J. 14: 2269-2280.
55. Beisiegel, U., W. Weber, G. Ihrke, J. Herz, and K. K. Stanley. 1989. The LDL-receptor-related protein, LRP, is an apolipoprotein E-binding protein. Nature. 341: 162-164.
56. Brown, M. S., and J. L. Goldstein. 1986. A receptor-mediated pathway for cholesterol homeostasis. Science. 232: 34-47.
57. Beglova, N., and S. C. Blacklow. 2005. The LDL receptor: how acid pulls the trigger. Trends Biochem. Sci. 30: 309-317.
58. Edwards, T. A., B. D. Wilkinson, R. P. Wharton, and A. K. Aggarwal. 2003. Model of the brain tumor-Pumilio translation repressor complex. Genes Dev. 17: 2508-2513.
59. Scharff, E. I., J. Koepke, G. Fritzsch, C. Lucke, and H. Ruterjans. 2001. Crystal structure of diisopropylfluorophosphatase from Loligo vulgaris. Structure. 9: 493-502.
60. Harel, M., A. Aharoni, L. Gaidukov, B. Brumshtein, O. Khersonsky, R. Meged, H. Dvir, R. B. Ravelli, A. McCarthy, L. Toker, et al. 2004. Structure and evolution of the serum paraoxonase family of detoxifying and anti-atherosclerotic enzymes. Nat. Struct. Mol. Biol. 11: 412-419.
61. Huang, S., L. Henry, Y. K. Ho, H. J. Pownall, and G. Rudenko. 2010. Mechanism of LDL binding and release probed by structure-based mutagenesis of the LDL receptor. J. Lipid Res. 51: 297-308.
62. Zhao, Z., and P. Michaely. 2011. Role of an intramolecular contact on lipoprotein uptake by the LDL receptor. Biochim. Biophys. Acta. 1811: 397-408.
63. Zong, Y., B. Zhang, S. Gu, K. Lee, J. Zhou, G. Yao, D. Figueiredo, K. Perry, L. Mei, and R. Jin. 2012. Structural basis of agrin-LRP4-MuSK signaling. Genes Dev. 26: 247-258.
64. Holdsworth, G., P. Slocombe, C. Doyle, B. Sweeney, V. Veverka, K. Le Riche, R. J. Franklin, J. Compson, D. Brookings, J. Turner, et al. 2012. Characterization of the interaction of sclerostin with the low density lipoprotein receptor-related protein (LRP) family of Wnt co-receptors. J. Biol. Chem. 287: 26464-26477.
65. Chen, S., D. Bubeck, B. T. MacDonald, W. X. Liang, J. H. Mao, T. Malinauskas, O. Llorca, A. R. Aricescu, C. Siebold, X. He, et al. 2011. Structural and functional studies of LRP6 ectodomain reveal a platform for Wnt signaling. Dev. Cell. 21: 848-861.
66. Christensen, E. I., and H. Birn. 2001. Megalin and cubilin: synergistic endocytic receptors in renal proximal tubule. Am. J. Physiol. Renal Physiol. 280: F562 - F573.
67. Amsellem, S., J. Gburek, G. Hamard, R. Nielsen, T. E. Willnow, O. Devuyst, E. Nexo, P. J. Verroust, E. I. Christensen, and R. Kozyraki. 2010. Cubilin is essential for albumin reabsorption in the renal proximal tubule. J. Am. Soc. Nephrol. 21: 1859-1867.
68. Ahuja, R., R. Yammani, J. A. Bauer, S. Kalra, S. Seetharam, and B. Seetharam. 2008. Interactions of cubilin with megalin and the product of the amnionless gene (AMN): effect on its stability. Biochem. J. 410: 301-308.
69. Niehrs, C. 2012. The complex world of WNT receptor signalling. Nat. Rev. Mol. Cell Biol. 13: 767-779.
70. Mao, B., W. Wu, G. Davidson, J. Marhold, M. Li, B. M. Mechler, H. Delius, D. Hoppe, P. Stannek, C. Walter, et al. 2002. Kremen proteins are Dickkopf receptors that regulate Wnt/+ -catenin signalling. Nature. 417: 664-667.
71. Janda, C. Y., D. Waghray, A. M. Levin, C. Thomas, and K. C. Garcia. 2012. Structural basis of Wnt recognition by Frizzled. Science. 337: 59-64.
72. Bilic, J., Y. L. Huang, G. Davidson, T. Zimmermann, C. M. Cruciat, M. Bienz, and C. Niehrs. 2007. Wnt induces LRP6 signalosomes and promotes dishevelled-dependent LRP6 phosphorylation. Science. 316: 1619-1622.
73. Spoelgen, R., K. W. Adams, M. Koker, A. V. Thomas, O. M. Andersen, P. J. Hallett, K. K. Bercury, D. F. Joyner, M. Deng, W. H. Stoothoff, et al. 2009. Interaction of the apolipoprotein E receptors low density lipoprotein receptor-related protein and sorLA/LR11. Neuroscience. 158: 1460-1468.
74. D'Arcangelo, G., R. Homayouni, L. Keshvara, D. S. Rice, M. Sheldon, and T. Curran. 1999. Reelin is a ligand for lipoprotein receptors. Neuron. 24: 471-479.
75. Trommsdorff, M., M. Gotthardt, T. Hiesberger, J. Shelton, W. Stockinger, J. Nimpf, R. E. Hammer, J. A. Richardson, and J. Herz. 1999. Reeler/Disabled-like disruption of neuronal migration in knockout mice lacking the VLDL receptor and ApoE receptor 2. Cell. 97: 689-701.
76. Tufail, M., and M. Takeda. 2009. Insect vitellogenin/lipophorin receptors: molecular structures, role in oogenesis, and regulatory mechanisms. J. Insect Physiol. 55: 87-103.
77. Norton, P. A., R. O. Hynes, and D. J. Rees. 1990. Sevenless: seven found? Cell. 61: 15-16.
78. Herz, J., U. Hamann, S. Rogne, O. Myklebost, H. Gausepohl, and K. K. Stanley. 1988. Surface location and high affinity for calcium of a 500-kd liver membrane protein closely related to the LDLreceptor suggest a physiological role as lipoprotein receptor. EMBO J. 7: 4119-4127.
79. Liu, C-X., S. Musco, N. M. Lisitsina, S. Y. Yaklichkin, and N. A. Lisitsyn. 2000. Genomic organization of a new candidate tumor suppressor gene, LRP1B. Genomics. 69: 271-274.
80. Saito, A., S. Pietromonaco, A. K-C. Loo, and M. G. Farquhar. 1994. Complete cloning and sequencing of rat gp330/"megalin," a distinctive member of the low density lipoprotein receptor gene family. Proc. Natl. Acad. Sci. USA. 91: 9725-9729.
81. Van Hoof, D., K. W. Rodenburg, and D. J. Van der Horst. 2005. Intracellular fate of LDL receptor family members depends on the cooperation between their ligand-binding and EGF domains. J. Cell Sci. 118: 1309-1320.
82. Fernandez-Castaneda, A., S. Arandjelovic, T. L. Stiles, R. K. Schlobach, K. A. Mowen, S. L. Gonias, and A. Gaultier. 2013. Identification of the low density lipoprotein (LDL) receptor-related protein-1 interactome in central nervous system myelin suggests a role in the clearance of necrotic cell debris. J. Biol. Chem. 288: 4538-4548.