The menagerie of human lipocalins: A natural protein scaffold for molecular recognition of physiological compounds

Accounts of Chemical Research

Volumn 48, Issue 4, 2015, Pages 976-985

  Schiefner, André ^a   Skerra, Arne ^a  

^a TECHNICAL UNIVERSITY OF MUNICH   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

LIPOCALIN;

AMINO ACID SEQUENCE; CHEMICAL STRUCTURE; CHEMISTRY; HUMAN; HYDROGEN BOND; METABOLISM; MOLECULAR GENETICS;

AMINO ACID SEQUENCE; HUMANS; HYDROGEN BONDING; LIPOCALINS; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA;

EID: 84928334296     PISSN: 00014842     EISSN: 15204898     Source Type: Journal    
DOI: 10.1021/ar5003973     Document Type: Article

References (77)

1. 1-acid glycoprotein and serum retinol-binding protein and its relatives FASEB J. 1987, 1, 209-214
2. Necomer, M. E.; Jones, T. A.; Åqvist, J.; Sundelin, J.; Eriksson, U.; Rask, L.; Peterson, P. A. The three-dimensional structure of retinol-binding protein EMBO J. 1984, 3, 1451-1454
3. Floer, D. R. Experimentally determined lipocalin structures Biochim. Biophys. Acta 2000, 1482, 46-56
4. Floer, D. R. The lipocalin protein family: Structure and function Biochem. J. 1996, 318, 1-14
5. Sánchez, D.; Ganfornina, M. D.; Gutiérrez, G.; Marín, A. Exon-intron structure and evolution of the Lipocalin gene family Mol. Biol. Evol. 2003, 20, 775-783
6. Breustedt, D. A.; Schönfeld, D. L.; Skerra, A. Comparative ligand-binding analysis of ten human lipocalins Biochim. Biophys. Acta 2006, 1764, 161-173
7. Coan, S. .; Necomer, M. E.; Jones, T. A. Crystallographic refinement of human serum retinol binding protein at 2 Å resolution Proteins 1990, 8, 44-61
8. Motani, A.; ang, Z.; Conn, M.; Siegler, K.; Zhang, Y.; Liu, Q.; Johnstone, S.; Xu, H.; Thibault, S.; ang, Y.; Fan, P.; Connors, R.; Le, H.; Xu, G.; alker, N.; Shan, B.; Coard, P. Identification and characterization of a non-retinoid ligand for retinol-binding protein 4 hich loers serum retinol-binding protein 4 levels in vivo J. Biol. Chem. 2009, 284, 7673-7680
9. Zanotti, G.; Folli, C.; Cendron, L.; Alfieri, B.; Nishida, S. K.; Gliubich, F.; Pasquato, N.; Negro, A.; Berni, R. Structural and mutational analyses of protein-protein interactions beteen transthyretin and retinol-binding protein FEBS J. 2008, 275, 5841-5854
10. Necomer, M. E.; Ong, D. E. Plasma retinol binding protein: Structure and function of the prototypic lipocalin Biochim. Biophys. Acta 2000, 1482, 57-64
11. Sun, H.; Kaaguchi, R. The membrane receptor for plasma retinol-binding protein, a ne type of cell-surface receptor Int. Rev. Cell Mol. Biol. 2011, 288, 1-41
12. 1-Acid glycoprotein: An acute phase protein ith inflammatory and immunomodulating properties Cytokine Groth Factor Rev. 2003, 14, 25-34
13. Dente, L.; Pizza, M. G.; Metspalu, A.; Cortese, R. Structure and expression of the genes coding for human α1-acid glycoprotein EMBO J. 1987, 6, 2289-2296
14. 1-glycoprotein and its interactions ith drugs Drug Metab. Rev. 2001, 33, 161-235
15. 1-acid glycoprotein (Orosomucoid) solved by UV RIP reveals the broad drug-binding activity of this human plasma lipocalin J. Mol. Biol. 2008, 384, 393-405
16. 1-acid glycoprotein genetic variants, the A and F1∗S forms J. Biol. Chem. 2011, 286, 14427-14434
17. 1-Microglobulin: A yello-bron lipocalin Biochim. Biophys. Acta 2000, 1482, 172-184
18. Åkerström, B.; Gram, M. A1M, an extravascular tissue cleaning and housekeeping protein Free Radical Biol. Med. 2014, 74, 274-282
19. 1-microglobulin as first- and early second-trimester predictive biomarkers for preeclampsia Am. J. Obstet. Gynecol. 2011, 204, 520.e1-520.e5
20. 1-microglobulin excretion as biomarker of renal toxicity in trichloroethylene-exposed persons Int. Arch. Occup. Environ. Health 2004, 77, 186-190
21. 1-microglobulin reveals a potential haem-binding site Biochem. J. 2012, 445, 175-182
22. Zhang, Y.; Gao, Z.; Guo, Z.; Zhang, H.; Zhang, Z.; Luo, M.; Hou, H.; Huang, A.; Dong, Y.; ang, D. The crystal structure of human protein α1M reveals a chromophore-binding site and to putative protein-protein interfaces Biochem. Biophys. Res. Commun. 2013, 439, 346-350
23. Flo, T. H.; Smith, K. D.; Sato, S.; Rodriguez, D. J.; Holmes, M. A.; Strong, R. K.; Akira, S.; Aderem, A. Lipocalin 2 mediates an innate immune response to bacterial infection by sequestrating iron Nature 2004, 432, 917-921
24. Goetz, D. H.; Holmes, M. A.; Borregaard, N.; Bluhm, M. E.; Raymond, K. N.; Strong, R. K. The neutrophil lipocalin NGAL is a bacteriostatic agent that interferes ith siderophore-mediated iron acquisition Mol. Cell 2002, 10, 1033-1043
25. Kjeldsen, L.; Johnsen, A. H.; Sengelov, H.; Borregaard, N. Isolation and primary structure of NGAL, a novel protein associated ith human neutrophil gelatinase J. Biol. Chem. 1993, 268, 10425-10432
26. Abergel, R. J.; Clifton, M. C.; Pizarro, J. C.; arner, J. A.; Shuh, D. K.; Strong, R. K.; Raymond, K. N. The siderocalin/enterobactin interaction: A link beteen mammalian immunity and bacterial iron transport J. Am. Chem. Soc. 2008, 130, 11524-11534
27. Miethke, M.; Skerra, A. Neutrophil gelatinase-associated lipocalin expresses antimicrobial activity by interfering ith l -norepinephrine-mediated bacterial iron acquisition Antimicrob. Agents Chemother. 2010, 54, 1580-1589
28. Esser, A. F. The membrane attack complex of complement. Assembly, structure and cytotoxic activity Toxicology 1994, 87, 229-247
29. Ng, S. C.; Sodetz, J. M. Biosynthesis of C8 by hepatocytes. Differential expression and intracellular association of the α-γ- and β-subunits J. Immunol. 1987, 139, 3021-3027
30. Chisell, B.; Lovelace, L. L.; Brannen, C.; Ortlund, E. A.; Lebioda, L.; Sodetz, J. M. Structural features of the ligand binding site on human complement protein C8γ: A member of the lipocalin family Biochim. Biophys. Acta 2007, 1774, 637-644
31. Lovelace, L. L.; Cooper, C. L.; Sodetz, J. M.; Lebioda, L. Structure of human C8 protein provides mechanistic insight into membrane pore formation by complement J. Biol. Chem. 2011, 286, 17585-17592
32. Ortlund, E.; Parker, C. L.; Schreck, S. F.; Ginell, S.; Minor, W.; Sodetz, J. M.; Lebioda, L. Crystal structure of human complement protein C8γ at 1.2 Å resolution reveals a lipocalin fold and a distinct ligand binding site Biochemistry 2002, 41, 7030-7037
33. Milne, R.; Rassart, E.; Marcel, Y. L. Molecular biology of apolipoprotein D Curr. Opin. Lipidol. 1993, 4, 100-106
34. Yang, C. Y.; Gu, Z. .; Blanco-Vaca, F.; Gaskell, S. J.; Yang, M.; Massey, J. B.; Gotto, A. M., Jr.; Ponall, H. J. Structure of human apolipoprotein D: Locations of the intermolecular and intramolecular disulfide links Biochemistry 1994, 33, 12451-12455
35. Rassart, E.; Bedirian, A.; Do Carmo, S.; Guinard, O.; Sirois, J.; Terrisse, L.; Milne, R. Apolipoprotein D Biochim. Biophys. Acta 2000, 1482, 185-198
36. Hall, R. E.; Horsfall, D. J.; Stahl, J.; Vivekanandan, S.; Ricciardelli, C.; Stapleton, A. M.; Scardino, P. T.; Neufing, P.; Tilley, D. Apolipoprotein-D: A novel cellular marker for HGPIN and prostate cancer Prostate 2004, 58, 103-108
37. Miranda, E.; Vizoso, F.; Martín, A.; Quintela, I.; Corte, M. D.; Seguí, M. E.; Ordiz, I.; Merino, A. M. Apolipoprotein D expression in cutaneous malignant melanoma J. Surg. Oncol. 2003, 83, 99-105
38. Patel, S. C.; Asotra, K.; Patel, Y. C.; McConathy, J.; Patel, R. C.; Suresh, S. Astrocytes synthesize and secrete the lipophilic ligand carrier apolipoprotein D Neuroreport 1995, 6, 653-657
39. Thomas, E. A.; Copolov, D. L.; Sutcliffe, J. G. From pharmacotherapy to pathophysiology: Emerging mechanisms of apolipoprotein D in psychiatric disorders Curr. Mol. Med. 2003, 3, 408-418
40. Eichinger, A.; Nasreen, A.; Kim, H. J.; Skerra, A. Structural insight into the dual ligand specificity and mode of high density lipoprotein association of apolipoprotein D J. Biol. Chem. 2007, 282, 31068-31075
41. Christoffersen, C.; Ahnström, J.; Axler, O.; Christensen, E. I.; Dahlbäck, B.; Nielsen, L. B. The signal peptide anchors apolipoprotein M in plasma lipoproteins and prevents rapid clearance of apolipoprotein M from plasma J. Biol. Chem. 2008, 283, 18765-18772
42. Faber, K.; Axler, O.; Dahlbäck, B.; Nielsen, L. B. Characterization of apoM in normal and genetically modified mice J. Lipid Res. 2004, 45, 1272-1278
43. Xu, N.; Dahlbäck, B. A novel human apolipoprotein (apoM) J. Biol. Chem. 1999, 274, 31286-31290
44. Christoffersen, C.; Jauhiainen, M.; Moser, M.; Porse, B.; Ehnholm, C.; Boesl, M.; Dahlbäck, B.; Nielsen, L. B. Effect of apolipoprotein M on high density lipoprotein metabolism and atherosclerosis in lo density lipoprotein receptor knock-out mice J. Biol. Chem. 2008, 283, 1839-1847
45. olfrum, C.; Poy, M. N.; Stoffel, M. Apolipoprotein M is required for preβ-HDL formation and cholesterol efflux to HDL and protects against atherosclerosis Nat. Med. 2005, 11, 418-422
46. Christoffersen, C.; Obinata, H.; Kumarasamy, S. B.; Galvani, S.; Ahnström, J.; Sevvana, M.; Egerer-Sieber, C.; Muller, Y. A.; Hla, T.; Nielsen, L. B.; Dahlbäck, B. Endothelium-protective sphingosine-1-phosphate provided by HDL-associated apolipoprotein M Proc. Natl. Acad. Sci. U.S.A. 2011, 108, 9613-9618
47. Sevvana, M.; Ahnström, J.; Egerer-Sieber, C.; Lange, H. A.; Dahlbäck, B.; Muller, Y. A. Serendipitous fatty acid binding reveals the structural determinants for ligand recognition in apolipoprotein M J. Mol. Biol. 2009, 393, 920-936
48. Urade, Y.; Hayaishi, O. Biochemical, structural, genetic, physiological, and pathophysiological features of lipocalin-type prostaglandin D synthase Biochim. Biophys. Acta 2000, 1482, 259-271
49. Mase, M.; Yamada, K.; Shimazu, N.; Seiki, K.; Oda, H.; Nakau, H.; Inui, T.; Li, W.; Eguchi, N.; Urade, Y. Lipocalin-type prostaglandin D synthase (β-trace) in cerebrospinal fluid: A useful marker for the diagnosis of normal pressure hydrocephalus Neurosci. Res. 2003, 47, 455-459
50. Kume, S.; Lee, Y. H.; Miyamoto, Y.; Fukada, H.; Goto, Y.; Inui, T. Systematic interaction analysis of human lipocalin-type prostaglandin D synthase ith small lipophilic ligands Biochem. J. 2012, 446, 279-289
51. Lim, S. M.; Chen, D.; Teo, H.; Roos, A.; Jansson, A. E.; Nyman, T.; Trésaugues, L.; Pervushin, K.; Nordlund, P. Structural and dynamic insights into substrate binding and catalysis of human lipocalin prostaglandin D synthase J. Lipid Res. 2013, 54, 1630-1643
52. Perduca, M.; Bovi, M.; Bertinelli, M.; Bertini, E.; Destefanis, L.; Carrizo, M. E.; Capaldi, S.; Monaco, H. L. High-resolution structures of mutants of residues that affect access to the ligand-binding cavity of human lipocalin-type prostaglandin D synthase Acta Crystallogr., Sect. D: Biol. Crystallogr. 2014, 70, 2125-2138
53. Zhou, Y.; Sha, N.; Li, Y.; Zhao, Y.; Zhang, R.; Liu, Z.-J. Structure-function analysis of human L-prostaglandin D synthase bound ith fatty acid molecules FASEB J. 2010, 24, 4668-4677
54. Seppälä, M.; Koistinen, H.; Koistinen, R. Glycodelins Trends Endocrinol. Metab. 2001, 12, 111-117
55. Dell, A.; Morris, H. R.; Easton, R. L.; Panico, M.; Patankar, M.; Oehniger, S.; Koistinen, R.; Koistinen, H.; Seppälä, M.; Clark, G. F. Structural analysis of the oligosaccharides derived from glycodelin, a human glycoprotein ith potent immunosuppressive and contraceptive activities J. Biol. Chem. 1995, 270, 24116-24126
56. Morris, H. R.; Dell, A.; Easton, R. L.; Panico, M.; Koistinen, H.; Koistinen, R.; Oehninger, S.; Patankar, M. S.; Seppälä, M.; Clark, G. F. Gender-specific glycosylation of human glycodelin affects its contraceptive activity J. Biol. Chem. 1996, 271, 32159-32167
57. Schiefner, A.; Rodeald, F.; Neumaier, I.; Skerra, A. The dimeric crystal structure of the human fertility lipocalin glycodelin reveals a protein scaffold for the presentation of complex glycans Biochem. J. 2015, 466, 95-104
58. Kontopidis, G.; Holt, C.; Sayer, L. β-Lactoglobulin: Binding properties, structure, and function J. Dairy Sci. 2004, 87, 785-796
59. Redl, B. Human tear lipocalin Biochim. Biophys. Acta 2000, 1482, 241-248
60. Gasymov, O. K.; Abduragimov, A. R.; Yusifov, T. N.; Glasgo, B. J. Binding studies of tear lipocalin: The role of the conserved tryptophan in maintaining structure, stability and ligand affinity Biochim. Biophys. Acta 1999, 1433, 307-320
61. Glasgo, B. J.; Abduragimov, A. R.; Farahbakhsh, Z. T.; Faull, K. F.; Hubbell, L. Tear lipocalins bind a broad array of lipid ligands Curr. Eye Res. 1995, 14, 363-372
62. Fluckinger, M.; Haas, H.; Merschak, P.; Glasgo, B. J.; Redl, B. Human tear lipocalin exhibits antimicrobial activity by scavenging microbial siderophores Antimicrob. Agents Chemother. 2004, 48, 3367-3372
63. ojnar, P.; Lechner, M.; Merschak, P.; Redl, B. Molecular cloning of a novel lipocalin-1 interacting human cell membrane receptor using phage display J. Biol. Chem. 2001, 276, 20206-20212
64. Breustedt, D. A.; Chatell, L.; Skerra, A. A ne crystal form of human tear lipocalin reveals high flexibility in the loop region and induced fit in the ligand cavity Acta Crystallogr., Sect. D: Biol. Crystallogr. 2009, 65, 1118-1125
65. Breustedt, D. A.; Korndörfer, I. P.; Redl, B.; Skerra, A. The 1.8-Å crystal structure of human tear lipocalin reveals an extended branched cavity ith capacity for multiple ligands J. Biol. Chem. 2005, 280, 484-493
66. Tegoni, M.; Pelosi, P.; Vincent, F.; Spinelli, S.; Campanacci, V.; Grolli, S.; Ramoni, R.; Cambillau, C. Mammalian odorant binding proteins Biochim. Biophys. Acta 2000, 1482, 229-240
67. Lacazette, E.; Gachon, A. M.; Pitiot, G. A novel human odorant-binding protein gene family resulting from genomic duplicons at 9q34: Differential expression in the oral and genital spheres Hum. Mol. Genet. 2000, 9, 289-301
68. Briand, L.; Eloit, C.; Nespoulous, C.; Bézirard, V.; Huet, J. C.; Henry, C.; Blon, F.; Trotier, D.; Pernollet, J. C. Evidence of an odorant-binding protein in the human olfactory mucus: Location, structural characterization, and odorant-binding properties Biochemistry 2002, 41, 7241-7252
69. IIa. Proteins, in press.
70. Clark, H. F.; Gurney, A. L.; Abaya, E.; Baker, K.; Baldin, D.; Brush, J.; Chen, J.; Cho, B.; Chui, C.; Croley, C.; Currell, B.; Deuel, B.; Dod, P.; Eaton, D.; Foster, J.; Grimaldi, C.; Gu, Q.; Hass, P. E.; Heldens, S.; Huang, A.; Kim, H. S.; Klimoski, L.; Jin, Y.; Johnson, S.; Lee, J.; Leis, L.; Liao, D.; Mark, M.; Robbie, E.; Sanchez, C.; Schoenfeld, J.; Seshagiri, S.; Simmons, L.; Singh, J.; Smith, V.; Stinson, J.; Vagts, A.; Vandlen, R.; atanabe, C.; ieand, D.; oods, K.; Xie, M. H.; Yansura, D.; Yi, S.; Yu, G.; Yuan, J.; Zhang, M.; Zhang, Z.; Goddard, A.; ood, I.; Godoski, P.; Gray, A. The secreted protein discovery initiative (SPDI), a large-scale effort to identify novel human secreted and transmembrane proteins: A bioinformatics assessment Genome Res. 2003, 13, 2265-2270
71. Hamil, K. G.; Liu, Q.; Sivashanmugam, P.; Anbalagan, M.; Yenugu, S.; Soundararajan, R.; Grossman, G.; Rao, A. J.; Birse, C. E.; Ruben, S. M.; Richardson, R. T.; Zhang, Y. L.; O'Rand, M. G.; Petrusz, P.; French, F. S.; Hall, S. H. LCN6, a novel human epididymal lipocalin Reprod. Biol. Endocrinol. 2003, 1, 112
72. Suzuki, K.; Lareyre, J. J.; Sánchez, D.; Gutierrez, G.; Araki, Y.; Matusik, R. J.; Orgebin-Crist, M. C. Molecular evolution of epididymal lipocalin genes localized on mouse chromosome 2 Gene 2004, 339, 49-59
73. Skerra, A. Lipocalins as a scaffold Biochim. Biophys. Acta 2000, 1482, 337-350
74. Richter, A.; Eggenstein, E.; Skerra, A. Anticalins: Exploiting a non-Ig scaffold ith hypervariable loops for the engineering of binding proteins FEBS Lett. 2014, 588, 213-218
75. Gebauer, M.; Skerra, A. Anticalins: Small engineered binding proteins based on the lipocalin scaffold Methods Enzymol. 2012, 503, 157-188
76. Mross, K.; Richly, H.; Fischer, R.; Scharr, D.; Buchert, M.; Stern, A.; Gille, H.; Audoly, L. P.; Scheulen, M. E. First-in-human phase I study of PRS-050 (Angiocal), an Anticalin targeting and antagonizing VEGF-A, in patients ith advanced solid tumors PLoS One 2013, 8 e83232
77. Braberg, H.; ebb, B. M.; Tjioe, E.; Pieper, U.; Sali, A.; Madhusudhan, M. S. SALIGN: A eb server for alignment of multiple protein sequences and structures Bioinformatics 2012, 28, 2072-2073