The endocytic receptor megalin binds the iron transporting neutrophil-gelatinase-associated lipocalin with high affinity and mediates its cellular uptake

FEBS Letters

Volumn 579, Issue 3, 2005, Pages 773-777

  Hvidberg, Vibeke ^a   Jacobsen, Christian ^a   Strong, Roland K ^b   Cowland, Jack B ^c   Moestrup, Søren K ^a   Borregaard, Niels ^c  

^a AARHUS UNIVERSITY   (Denmark)

^b Fred Hutchinson Cancer Research Center   (United States)

^c Rigshospitalet   (Denmark)

Author keywords

Iron; Lipocalin; Megalin; NGAL; Siderophore

Indexed keywords

ANTIBODY; BACTERIAL PROTEIN; GELATINASE; LIPOCALIN; LOW DENSITY LIPOPROTEIN RECEPTOR; MEGALIN; SIDEROPHORE;

ANIMAL CELL; ARTICLE; BACTERIAL STRAIN; BINDING AFFINITY; CELL TRANSPORT; CONTROLLED STUDY; ENDOCYTOSIS; EPITHELIUM CELL; IRON TRANSPORT; NEUTROPHIL; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; RAT; SURFACE PLASMON RESONANCE;

ACUTE-PHASE PROTEINS; ENDOCYTOSIS; HUMANS; IRON; LDL-RECEPTOR RELATED PROTEIN 2; ONCOGENE PROTEINS; PROTEIN BINDING; PROTO-ONCOGENE PROTEINS; RECOMBINANT PROTEINS; SURFACE PLASMON RESONANCE;

BACTERIA (MICROORGANISMS);

EID: 12744272449     PISSN: 00145793     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.febslet.2004.12.031     Document Type: Article

References (38)

1. D.R. Flower The lipocalin protein family: structure and function Biochem. J. 318 1996 1 14
2. M.D. Ganfornina, G. Gutierrez, M. Bastiani, and D. Sanchez A phylogenetic analysis of the lipocalin protein family Mol. Biol. Evol. 17 2000 114 126
3. R.C. Patel, D. Lange, W.J. McConathy, Y.C. Patel, and S.C. Patel Probing the structure of the ligand binding cavity of lipocalins by fluorescence spectroscopy Protein Eng. 10 1997 621 625
4. B. Akerstrom, D.R. Flower, and J.P. Salier Lipocalins: unity in diversity Biochim. Biophys. Acta 1482 2000 1 8
5. D.R. Flower Beyond the superfamily: the lipocalin receptors Biochim. Biophys. Acta 1482 2000 327 336
6. P. Wojnar, M. Lechner, and B. Redl Antisense down-regulation of lipocalin-interacting membrane receptor expression inhibits cellular internalization of lipocalin-1 in human NT2 cells J. Biol. Chem. 278 2003 16209 16215
7. P. Wojnar, M. Lechnar, P. Merschak, and B. Redl Molecular cloning of a novel lipocalin-1 interacting human cell membrane receptor using phage display J. Biol. Chem. 276 2001 20206 20212
8. A. Saito, S. Pietromonaco, A.K. Loo, and M.G. Farquhar 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 1994 9725 9729
9. S.K. Moestrup, and P.J. Verroust Megalin- and cubilin-mediated endocytosis of protein-bound vitamins, lipids, and hormones in polarized epithelia Annu. Rev. Nutr. 21 2001 407 428
10. J.R. Leheste, B. Rolinski, H. Vorum, J. Hilpert, A. Nykjaer, C. Jacobsen, P. Aucouturier, J.O. Moskaug, A. Otto, E.I. Christensen, and T.E. Willnow Megalin knockout mice as an animal model of low molecular weight proteinuria Am. J. Pathol. 155 1999 1361 1370
11. J.B. Cowland, and N. Borregaard Molecular characterization and pattern of tissue expression of the gene for neutrophil gelatinase-associated lipocalin from humans Genomics 45 1997 17 23
12. J.B. Cowland, O.E. Sorensen, M. Sehested, and N. Borregaard Neutrophil gelatinase-associated lipocalin Is up-regulated in human epithelial cells by IL-1beta, but not by TNF-alpha J. Immunol. 171 2003 6630 6639
13. B.S. Nielsen, N. Borregaard, J.R. Bundgaard, S. Timshel, M. Sehested, and L. Kjeldsen Induction of NGAL synthesis in epithelial cells of human colorectal neoplasia and inflammatory bowel disease Gut 38 1996 414 420
14. L. Mallbris, K.P. O'Brien, A. Hulthen, B. Sandstedt, J.B. Cowland, N. Borregaard, and M. Stahle-Backdahl Neutrophil gelatinase-associated lipocalin is a marker for dysregulated keratinocyte differentiation in human skin Exp. Dermatol. 11 2002 584 591
15. D.H. Goetz, M.A. Holmes, N. Borregaard, M.E. Bluhm, K.N. Raymond, and R.K. Strong The neutrophil lipocalin NGAL is a bacteriostatic agent that interferes with siderophore-mediated iron acquisition Mol. Cell. 10 2002 1033 1043
16. T.H. Flo, K.D. Smith, S. Sato, D.J. Rodriguez, M.A. Holmes, R.K. Strong, S. Akira, and A. Aderem Lipocalin 2 mediates an innate immune response to bacterial infection by sequestrating iron Nature 2004
17. J.B. Neilands Siderophores: structure and function of microbial iron transport compounds J. Biol. Chem. 270 1995 26723 26726
18. L. Kjeldsen, A.H. Johnsen, H. Sengeløv, and N. Borregaard Isolation and primary structure of NGAL, a novel protein associated with human neutrophil gelatinase J. Biol. Chem. 268 1993 10425 10432
19. J. Yang, D. Goetz, J.Y. Li, W. Wang, K. Mori, D. Setlik, T. Du, H. Erdjument-Bromage, P. Tempst, R. Strong, and J. Barasch An iron delivery pathway mediated by a lipocalin Mol. Cell. 10 2002 1045 1056
20. J. Yang, K. Mori, J.Y. Li, and J. Barasch Iron, lipocalin, and kidney epithelia Am. J. Physiol. Renal Physiol. 285 2003 F9 F18
21. L. Axelsson, M. Bergenfeldt, and K. Ohlsson Studies of the release and turnover of a human neutrophil lipocalin Scand. J. Clin. Lab. Invest. 55 1995 577 588
22. L.R. Devireddy, J.G. Teodoro, F.A. Richard, and M.R. Green Induction of apoptosis by a secreted lipocalin that is transcriptionally regulated by IL-3 deprivation Science 293 2001 829 834
23. K. Kamezaki, K. Shimoda, A. Numata, K. Aoki, K. Kato, K. Takase, H. Nakajima, K. Ihara, T. Haro, F. Ishikawa, R. Imamura, T. Miyamoto, K. Nagafuji, H. Gondo, T. Hara, and M. Harada The lipocalin 24p3, which is an essential molecule in IL-3 withdrawal-induced apoptosis, is not involved in the G-CSF withdrawal-induced apoptosis Eur. J. Haematol. 71 2003 412 417
24. R.K. Strong, T. Bratt, J.B. Cowland, N. Borregaard, F.C. Wiberg, and A.J. Ewald Expression, purification, crystallization and crystallographic characterization of dimeric and monomeric human neutrophil gelatinase associated lipocalin (NGAL) Acta Crystallogr. D. Biol. Crystallogr. 54 Pt 1 1998 93 95
25. J.R. Bundgaard, N. Borregaard, and L. Kjeldsen Molecular cloning and expression of a cDNA encoding NGAL: a lipocalin expressed in human neutrophils Biochem. Biophys. Res. Commun. 202 1994 1468 1475
26. L. Kjeldsen, C. Koch, K. Arnljots, and N. Borregaard Characterization of two ELISAs for NGAL, a newly described lipocalin in human neutrophils J. Immunol. Meth. 198 1996 155 164
27. S.K. Moestrup, T.L. Holtet, M. Etzerodt, H.C. Thogersen, A. Nykjaer, P.A. Andreasen, H.H. Rasmussen, L. Sottrup-Jensen, and J. Gliemann Alpha 2-macroglobulin-proteinase complexes, plasminogen activator inhibitor type-1-plasminogen activator complexes, and receptor-associated protein bind to a region of the alpha 2-macroglobulin receptor containing a cluster of eight complement-type repeats J. Biol. Chem. 268 1993 13691 13696
28. S.K. Moestrup, and J. Gliemann Analysis of ligand recognition by the purified alpha 2-macroglobulin receptor (low density lipoprotein receptor-related protein). Evidence that high affinity of alpha 2-macroglobulin-proteinase complex is achieved by binding to adjacent receptors J. Biol. Chem. 266 1991 14011 14017
29. S.K. Moestrup, H. Birn, P.B. Fischer, C.M. Petersen, P.J. Verroust, R.B. Sim, E.I. Christensen, and E. Nexo Megalin-mediated endocytosis of transcobalamin-vitamin-B12 complexes suggests a role of the receptor in vitamin-B12 homeostasis Proc. Natl. Acad. Sci. USA 93 1996 8612 8617
30. S. Le Panse, P. Verroust, and E.I. Christensen Internalization and recycling of glycoprotein 280 in BN/MSV yolk sac epithelial cells: a model system of relevance to receptor-mediated endocytosis in the renal proximal tubule Exp. Nephrol. 5 1997 375 383
31. D. Sahali, N. Mulliez, F. Chatelet, C. Laurent-Winter, D. Citadelle, C. Roux, P. Ronco, and P. Verroust Coexpression in humans by kidney and fetal envelopes of a 280 kDa-coated pit-restricted protein. Similarity with the murine target of teratogenic antibodies Am. J. Pathol. 140 1992 33 44
32. M.M. Hussain, D.K. Strickland, and A. Bakillah The mammalian low-density lipoprotein receptor family Annu. Rev. Nutr. 19 1999 141 172
33. S.P. Stoesz, A. Friedl, J.D. Haag, M.J. Lindstrom, G.M. Clark, and M.N. Gould Heterogeneous expression of the lipocalin NGAL in primary breast cancers Int. J. Cancer 79 1998 565 572
34. S.P. Stoesz, and M.N. Gould Overexpression of neu-related lipocalin (NRL) in neu-initiated but not ras or chemically initiated rat mammary carcinomas Oncogene 11 1995 2233 2241
35. M. Furutani, S. Arii, M. Mizumoto, M. Kato, and M. Imamura Identification of a neutrophil gelatinase-associated lipocalin mRNA in human pancreatic cancers using a modified signal sequence trap method Cancer Lett. 122 1998 209 214
36. T.E. Willnow, J.L. Goldstein, K. Orth, M.S. Brown, and J. Herz Low density lipoprotein receptor-related protein and gp330 bind similar ligands, including plasminogen activator-inhibitor complexes and lactoferrin, an inhibitor of chylomicron remnant clearance J. Biol. Chem. 267 1992 26172 26180
37. M. Meilinger, M. Haumer, K.A. Szakmary, F. Steinbock, B. Scheiber, H. Goldenberg, and M. Huettinger Removal of lactoferrin from plasma is mediated by binding to low density lipoprotein receptor-related protein/alpha 2-macroglobulin receptor and transport to endosomes FEBS Lett. 360 1995 70 74
38. S.K. Moestrup, R. Kozyraki, M. Kristiansen, J.H. Kaysen, H.H. Rasmussen, D. Brault, F. Pontillon, F.O. Goda, E.I. Christensen, T.G. Hammond, and P.J. Verroust 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. 273 1998 5235 5242