Skip to main content
NCBI home page
Biochemical Journal logoLink to Biochemical Journal
. 1996 Aug 15;318(Pt 1):1–14. doi: 10.1042/bj3180001

The lipocalin protein family: structure and function.

D R Flower 1
PMCID: PMC1217580  PMID: 8761444

Abstract

The lipocalin protein family is a large group of small extracellular proteins. The family demonstrates great diversity at the sequence level; however, most lipocalins share three characteristic conserved sequence motifs, the kernel lipocalins, while a group of more divergent family members, the outlier lipocalins, share only one. Belying this sequence dissimilarity, lipocalin crystal structures are highly conserved and comprise a single eight-stranded continuously hydrogen-bonded antiparallel beta-barrel, which encloses an internal ligand-binding site. Together with two other families of ligand-binding proteins, the fatty-acid-binding proteins (FABPs) and the avidins, the lipocalins form part of an overall structural superfamily: the calycins. Members of the lipocalin family are characterized by several common molecular-recognition properties: the ability to bind a range of small hydrophobic molecules, binding to specific cell-surface receptors and the formation of complexes with soluble macromolecules. The varied biological functions of the lipocalins are mediated by one or more of these properties. In the past, the lipocalins have been classified as transport proteins; however, it is now clear that the lipocalins exhibit great functional diversity, with roles in retinol transport, invertebrate cryptic coloration, olfaction and pheromone transport, and prostaglandin synthesis. The lipocalins have also been implicated in the regulation of cell homoeostasis and the modulation of the immune response, and, as carrier proteins, to act in the general clearance of endogenous and exogenous compounds.

Full Text

The Full Text of this article is available as a PDF (777.4 KB).

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Achen M. G., Harms P. J., Thomas T., Richardson S. J., Wettenhall R. E., Schreiber G. Protein synthesis at the blood-brain barrier. The major protein secreted by amphibian choroid plexus is a lipocalin. J Biol Chem. 1992 Nov 15;267(32):23170–23174. [PubMed] [Google Scholar]
  2. Akerström B., Bratt T., Enghild J. J. Formation of the alpha 1-microglobulin chromophore in mammalian and insect cells: a novel post-translational mechanism? FEBS Lett. 1995 Mar 27;362(1):50–54. doi: 10.1016/0014-5793(95)00206-o. [DOI] [PubMed] [Google Scholar]
  3. Akerström B., Lögdberg L. Alpha 1-microglobulin glycopeptides inhibit antigen-specific stimulation of human peripheral blood leucocytes. Scand J Immunol. 1984 Dec;20(6):559–563. doi: 10.1111/j.1365-3083.1984.tb01039.x. [DOI] [PubMed] [Google Scholar]
  4. Akerström B., Lögdberg L. An intriguing member of the lipocalin protein family: alpha 1-microglobulin. Trends Biochem Sci. 1990 Jun;15(6):240–243. doi: 10.1016/0968-0004(90)90037-c. [DOI] [PubMed] [Google Scholar]
  5. Akerström B. Role of alpha 1-microglobulin in immune response and inflammation. Folia Histochem Cytobiol. 1992;30(4):183–186. [PubMed] [Google Scholar]
  6. Arnaud P., Miribel L., Roux A. F. Alpha 1-acid glycoprotein. Methods Enzymol. 1988;163:418–430. doi: 10.1016/0076-6879(88)63040-0. [DOI] [PubMed] [Google Scholar]
  7. Arruda L. K., Vailes L. D., Hayden M. L., Benjamin D. C., Chapman M. D. Cloning of cockroach allergen, Bla g 4, identifies ligand binding proteins (or calycins) as a cause of IgE antibody responses. J Biol Chem. 1995 Dec 29;270(52):31196–31201. doi: 10.1074/jbc.270.52.31196. [DOI] [PubMed] [Google Scholar]
  8. Babiker-Mohamed H., Akerström B., Lögdberg L. Mitogenic effect of alpha 1-microglobulin on mouse lymphocytes. Evidence of T- and B-cell cooperation, B-cell proliferation, and a low-affinity receptor on mononuclear cells. Scand J Immunol. 1990 Jul;32(1):37–44. doi: 10.1111/j.1365-3083.1990.tb02889.x. [DOI] [PubMed] [Google Scholar]
  9. Babiker-Mohamed H., Forsberg M., Olsson M. L., Winquist O., Nilson B. H., Lögdberg L., Akerström B. Characterization of monoclonal anti-alpha 1-microglobulin antibodies: binding strength, binding sites, and inhibition of lymphocyte stimulation. Scand J Immunol. 1991 Nov;34(5):655–666. doi: 10.1111/j.1365-3083.1991.tb01589.x. [DOI] [PubMed] [Google Scholar]
  10. Babiker-Mohamed H., Olsson M. L., Boketoft A., Lögdberg L., Akerström B. Alpha 1-microglobulin is mitogenic to human peripheral blood lymphocytes. Regulation by both enhancing and suppressive serum factors. Immunobiology. 1990 Feb;180(2-3):221–234. doi: 10.1016/S0171-2985(11)80330-X. [DOI] [PubMed] [Google Scholar]
  11. Bacchini A., Gaetani E., Cavaggioni A. Pheromone binding proteins of the mouse, Mus musculus. Experientia. 1992 Apr 15;48(4):419–421. doi: 10.1007/BF01923448. [DOI] [PubMed] [Google Scholar]
  12. Balbín M., Freije J. M., Fueyo A., Sánchez L. M., López-Otín C. Apolipoprotein D is the major protein component in cyst fluid from women with human breast gross cystic disease. Biochem J. 1990 Nov 1;271(3):803–807. doi: 10.1042/bj2710803. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Bartsch S., Tschesche H. Cloning and expression of human neutrophil lipocalin cDNA derived from bone marrow and ovarian cancer cells. FEBS Lett. 1995 Jan 9;357(3):255–259. doi: 10.1016/0014-5793(94)01303-i. [DOI] [PubMed] [Google Scholar]
  14. Bedard P. A., Yannoni Y., Simmons D. L., Erikson R. L. Rapid repression of quiescence-specific gene expression by epidermal growth factor, insulin, and pp60v-src. Mol Cell Biol. 1989 Mar;9(3):1371–1375. doi: 10.1128/mcb.9.3.1371. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Bell S. C. Purification of human secretory pregnancy-associated endometrial alpha 2-globulin (alpha 2-PEG) from cytosol of first trimester pregnancy endometrium. Hum Reprod. 1986 Aug;1(5):313–318. doi: 10.1093/oxfordjournals.humrep.a136412. [DOI] [PubMed] [Google Scholar]
  16. Bell S. C. Secretory endometrial and decidual proteins: studies and clinical significance of a maternally derived group of pregnancy-associated serum proteins. Hum Reprod. 1986 Apr;1(3):129–143. doi: 10.1093/oxfordjournals.humrep.a136369. [DOI] [PubMed] [Google Scholar]
  17. Bennett M., Schmid K. Immunosuppression by human plasma alpha 1-acid glycoprotein: importance of the carbohydrate moiety. Proc Natl Acad Sci U S A. 1980 Oct;77(10):6109–6113. doi: 10.1073/pnas.77.10.6109. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Berman P., Gray P., Chen E., Keyser K., Ehrlich D., Karten H., LaCorbiere M., Esch F., Schubert D. Sequence analysis, cellular localization, and expression of a neuroretina adhesion and cell survival molecule. Cell. 1987 Oct 9;51(1):135–142. doi: 10.1016/0092-8674(87)90018-3. [DOI] [PubMed] [Google Scholar]
  19. Bignetti E., Cattaneo P., Cavaggioni A., Damiani G., Tirindelli R. The pyrazine-binding protein and olfaction. Comp Biochem Physiol B. 1988;90(1):1–5. doi: 10.1016/0305-0491(88)90029-6. [DOI] [PubMed] [Google Scholar]
  20. Bishop R. E., Penfold S. S., Frost L. S., Höltje J. V., Weiner J. H. Stationary phase expression of a novel Escherichia coli outer membrane lipoprotein and its relationship with mammalian apolipoprotein D. Implications for the origin of lipocalins. J Biol Chem. 1995 Sep 29;270(39):23097–23103. doi: 10.1074/jbc.270.39.23097. [DOI] [PubMed] [Google Scholar]
  21. Blanco-Vaca F., Via D. P., Yang C. Y., Massey J. B., Pownall H. J. Characterization of disulfide-linked heterodimers containing apolipoprotein D in human plasma lipoproteins. J Lipid Res. 1992 Dec;33(12):1785–1796. [PubMed] [Google Scholar]
  22. Blaner W. S. Retinol-binding protein: the serum transport protein for vitamin A. Endocr Rev. 1989 Aug;10(3):308–316. doi: 10.1210/edrv-10-3-308. [DOI] [PubMed] [Google Scholar]
  23. Blomhoff R., Green M. H., Berg T., Norum K. R. Transport and storage of vitamin A. Science. 1990 Oct 19;250(4979):399–404. doi: 10.1126/science.2218545. [DOI] [PubMed] [Google Scholar]
  24. Bolton A. E., Pockley A. G., Clough K. J., Mowles E. A., Stoker R. J., Westwood O. M., Chapman M. G. Identification of placental protein 14 as an immunosuppressive factor in human reproduction. Lancet. 1987 Mar 14;1(8533):593–595. doi: 10.1016/s0140-6736(87)90235-2. [DOI] [PubMed] [Google Scholar]
  25. Borghoff S. J., Miller A. B., Bowen J. P., Swenberg J. A. Characteristics of chemical binding to alpha 2u-globulin in vitro--evaluating structure-activity relationships. Toxicol Appl Pharmacol. 1991 Feb;107(2):228–238. doi: 10.1016/0041-008x(91)90205-s. [DOI] [PubMed] [Google Scholar]
  26. Borghoff S. J., Short B. G., Swenberg J. A. Biochemical mechanisms and pathobiology of alpha 2u-globulin nephropathy. Annu Rev Pharmacol Toxicol. 1990;30:349–367. doi: 10.1146/annurev.pa.30.040190.002025. [DOI] [PubMed] [Google Scholar]
  27. Boyles J. K., Notterpek L. M., Anderson L. J. Accumulation of apolipoproteins in the regenerating and remyelinating mammalian peripheral nerve. Identification of apolipoprotein D, apolipoprotein A-IV, apolipoprotein E, and apolipoprotein A-I. J Biol Chem. 1990 Oct 15;265(29):17805–17815. [PubMed] [Google Scholar]
  28. Brooks D. E. The major androgen-regulated secretory proteins of the rat epididymis bear sequence homology with members of the alpha 2u-globulin superfamily. Biochem Int. 1987 Feb;14(2):235–240. [PubMed] [Google Scholar]
  29. Båvik C. O., Busch C., Eriksson U. Characterization of a plasma retinol-binding protein membrane receptor expressed in the retinal pigment epithelium. J Biol Chem. 1992 Nov 15;267(32):23035–23042. [PubMed] [Google Scholar]
  30. Böcskei Z., Groom C. R., Flower D. R., Wright C. E., Phillips S. E., Cavaggioni A., Findlay J. B., North A. C. Pheromone binding to two rodent urinary proteins revealed by X-ray crystallography. Nature. 1992 Nov 12;360(6400):186–188. doi: 10.1038/360186a0. [DOI] [PubMed] [Google Scholar]
  31. Cavaggioni A., Findlay J. B., Tirindelli R. Ligand binding characteristics of homologous rat and mouse urinary proteins and pyrazine-binding protein of calf. Comp Biochem Physiol B. 1990;96(3):513–520. doi: 10.1016/0305-0491(90)90049-y. [DOI] [PubMed] [Google Scholar]
  32. Cavaggioni A., Sorbi R. T., Keen J. N., Pappin D. J., Findlay J. B. Homology between the pyrazine-binding protein from nasal mucosa and major urinary proteins. FEBS Lett. 1987 Feb 23;212(2):225–228. doi: 10.1016/0014-5793(87)81349-2. [DOI] [PubMed] [Google Scholar]
  33. Cavaggioni A., Sorbi R. T., Keen J. N., Pappin D. J., Findlay J. B. Homology between the pyrazine-binding protein from nasal mucosa and major urinary proteins. FEBS Lett. 1987 Feb 23;212(2):225–228. doi: 10.1016/0014-5793(87)81349-2. [DOI] [PubMed] [Google Scholar]
  34. Cogan U., Kopelman M., Mokady S., Shinitzky M. Binding affinities of retinol and related compounds to retinol binding proteins. Eur J Biochem. 1976 May 17;65(1):71–78. doi: 10.1111/j.1432-1033.1976.tb10390.x. [DOI] [PubMed] [Google Scholar]
  35. Costello M., Fiedel B. A., Gewurz H. Inhibition of platelet aggregation by native and desialised alpha-1 acid glycoprotein. Nature. 1979 Oct 25;281(5733):677–678. doi: 10.1038/281677a0. [DOI] [PubMed] [Google Scholar]
  36. Cowan S. W., Newcomer M. E., Jones T. A. Crystallographic refinement of human serum retinol binding protein at 2A resolution. Proteins. 1990;8(1):44–61. doi: 10.1002/prot.340080108. [DOI] [PubMed] [Google Scholar]
  37. De Graaf T. W., Van der Stelt M. E., Anbergen M. G., van Dijk W. Inflammation-induced expression of sialyl Lewis X-containing glycan structures on alpha 1-acid glycoprotein (orosomucoid) in human sera. J Exp Med. 1993 Mar 1;177(3):657–666. doi: 10.1084/jem.177.3.657. [DOI] [PMC free article] [PubMed] [Google Scholar]
  38. Descalzi Cancedda F., Asaro D., Molina F., Cancedda R., Caruso C., Camardella L., Negri A., Ronchi S. The amino terminal sequence of the developmentally regulated Ch21 protein shows homology with amino terminal sequences of low molecular weight proteins binding hydrophobic molecules. Biochem Biophys Res Commun. 1990 May 16;168(3):933–938. doi: 10.1016/0006-291x(90)91118-c. [DOI] [PubMed] [Google Scholar]
  39. Descalzi Cancedda F., Manduca P., Tacchetti C., Fossa P., Quarto R., Cancedda R. Developmentally regulated synthesis of a low molecular weight protein (Ch 21) by differentiating chondrocytes. J Cell Biol. 1988 Dec;107(6 Pt 1):2455–2463. doi: 10.1083/jcb.107.6.2455. [DOI] [PMC free article] [PubMed] [Google Scholar]
  40. Dodin G., Andrieux M., al Kabbani H. Binding of ellipticine to beta-lactoglobulin. A physico-chemical study of the specific interaction of an antitumor drug with a transport protein. Eur J Biochem. 1990 Nov 13;193(3):697–700. doi: 10.1111/j.1432-1033.1990.tb19389.x. [DOI] [PubMed] [Google Scholar]
  41. Dufour E., Marden M. C., Haertlé T. Beta-lactoglobulin binds retinol and protoporphyrin IX at two different binding sites. FEBS Lett. 1990 Dec 17;277(1-2):223–226. doi: 10.1016/0014-5793(90)80850-i. [DOI] [PubMed] [Google Scholar]
  42. Escribano J., Grubb A., Calero M., Méndez E. The protein HC chromophore is linked to the cysteine residue at position 34 of the polypeptide chain by a reduction-resistant bond and causes the charge heterogeneity of protein HC. J Biol Chem. 1991 Aug 25;266(24):15758–15763. [PubMed] [Google Scholar]
  43. Escribano J., Grubb A., Méndez E. Identification of retinol as one of the protein HC chromophores. Biochem Biophys Res Commun. 1988 Sep 30;155(3):1424–1429. doi: 10.1016/s0006-291x(88)81300-7. [DOI] [PubMed] [Google Scholar]
  44. FINLAYSON J. S., POTTER M., RUNNER C. R. ELECTROPHORETIC VARIATION AND SEX DIMORPHISM OF THE MAJOR URINARY PROTEIN COMPLEX IN INBRED MICE: A NEW GENETIC MARKER. J Natl Cancer Inst. 1963 Jul;31:91–107. [PubMed] [Google Scholar]
  45. Falkenberg C., Allhorn M., Thøgersen I. B., Valnickova Z., Pizzo S. V., Salvesen G., Akerström B., Enghild J. J. alpha 1-Microglobulin destroys the proteinase inhibitory activity of alpha 1-inhibitor-3 by complex formation. J Biol Chem. 1995 Mar 3;270(9):4478–4483. doi: 10.1074/jbc.270.9.4478. [DOI] [PubMed] [Google Scholar]
  46. Falkenberg C., Enghild J. J., Thøgersen I. B., Salvesen G., Akerström B. Isolation and characterization of fibronectin-alpha 1-microglobulin complex in rat plasma. Biochem J. 1994 Aug 1;301(Pt 3):745–751. doi: 10.1042/bj3010745. [DOI] [PMC free article] [PubMed] [Google Scholar]
  47. Fernandez-Luna J. L., Leyva-Cobian F., Mollinedo F. Identification of the protein HC receptor. FEBS Lett. 1988 Aug 29;236(2):471–474. doi: 10.1016/0014-5793(88)80079-6. [DOI] [PubMed] [Google Scholar]
  48. Flower D. R. FOLD: integrated analysis and display of protein secondary structure. J Mol Graph. 1995 Dec;13(6):377–384. doi: 10.1016/0263-7855(95)00072-0. [DOI] [PubMed] [Google Scholar]
  49. Flower D. R. Improved ribbon-drawing programs. J Mol Graph. 1991 Dec;9(4):257-8, 248. doi: 10.1016/0263-7855(91)80021-q. [DOI] [PubMed] [Google Scholar]
  50. Flower D. R. Multiple molecular recognition properties of the lipocalin protein family. J Mol Recognit. 1995 May-Jun;8(3):185–195. doi: 10.1002/jmr.300080304. [DOI] [PubMed] [Google Scholar]
  51. Flower D. R., North A. C., Attwood T. K. Mouse oncogene protein 24p3 is a member of the lipocalin protein family. Biochem Biophys Res Commun. 1991 Oct 15;180(1):69–74. doi: 10.1016/s0006-291x(05)81256-2. [DOI] [PubMed] [Google Scholar]
  52. Flower D. R., North A. C., Attwood T. K. Structure and sequence relationships in the lipocalins and related proteins. Protein Sci. 1993 May;2(5):753–761. doi: 10.1002/pro.5560020507. [DOI] [PMC free article] [PubMed] [Google Scholar]
  53. Flower D. R., Sansom C. E., Beck M. E., Attwood T. K. The first prokaryotic lipocalins. Trends Biochem Sci. 1995 Dec;20(12):498–499. doi: 10.1016/s0968-0004(00)89116-1. [DOI] [PubMed] [Google Scholar]
  54. Flower D. R. Structural relationship of streptavidin to the calycin protein superfamily. FEBS Lett. 1993 Oct 25;333(1-2):99–102. doi: 10.1016/0014-5793(93)80382-5. [DOI] [PubMed] [Google Scholar]
  55. Flower D. R. The lipocalin protein family: a role in cell regulation. FEBS Lett. 1994 Oct 31;354(1):7–11. doi: 10.1016/0014-5793(94)01078-1. [DOI] [PubMed] [Google Scholar]
  56. Francone O. L., Gurakar A., Fielding C. Distribution and functions of lecithin:cholesterol acyltransferase and cholesteryl ester transfer protein in plasma lipoproteins. Evidence for a functional unit containing these activities together with apolipoproteins A-I and D that catalyzes the esterification and transfer of cell-derived cholesterol. J Biol Chem. 1989 Apr 25;264(12):7066–7072. [PubMed] [Google Scholar]
  57. Ganfornina M. D., Sánchez D., Bastiani M. J. Lazarillo, a new GPI-linked surface lipocalin, is restricted to a subset of neurons in the grasshopper embryo. Development. 1995 Jan;121(1):123–134. doi: 10.1242/dev.121.1.123. [DOI] [PubMed] [Google Scholar]
  58. Glasgow B. J., Abduragimov A. R., Farahbakhsh Z. T., Faull K. F., Hubbell W. L. Tear lipocalins bind a broad array of lipid ligands. Curr Eye Res. 1995 May;14(5):363–372. doi: 10.3109/02713689508999934. [DOI] [PubMed] [Google Scholar]
  59. Grubb A., Méndez E., Fernandez-Luna J. L., López C., Mihaesco E., Vaerman J. P. The molecular organization of the protein HC-IgA complex (HC-IgA). J Biol Chem. 1986 Oct 25;261(30):14313–14320. [PubMed] [Google Scholar]
  60. Haefliger J. A., Jenne D., Stanley K. K., Tschopp J. Structural homology of human complement component C8 gamma and plasma protein HC: identity of the cysteine bond pattern. Biochem Biophys Res Commun. 1987 Dec 16;149(2):750–754. doi: 10.1016/0006-291x(87)90431-1. [DOI] [PubMed] [Google Scholar]
  61. Haefliger J. A., Peitsch M. C., Jenne D. E., Tschopp J. Structural and functional characterization of complement C8 gamma, a member of the lipocalin protein family. Mol Immunol. 1991 Jan-Feb;28(1-2):123–131. doi: 10.1016/0161-5890(91)90095-2. [DOI] [PubMed] [Google Scholar]
  62. Hase J., Kobashi K., Nakai N., Onosaka S. Binding of retinol-binding protein obtained from human urine with vitamin A derivatives and terpenoids. J Biochem. 1976 Feb;79(2):373–380. doi: 10.1093/oxfordjournals.jbchem.a131080. [DOI] [PubMed] [Google Scholar]
  63. Henzel W. J., Rodriguez H., Singer A. G., Stults J. T., Macrides F., Agosta W. C., Niall H. The primary structure of aphrodisin. J Biol Chem. 1988 Nov 15;263(32):16682–16687. [PubMed] [Google Scholar]
  64. Holden H. M., Rypniewski W. R., Law J. H., Rayment I. The molecular structure of insecticyanin from the tobacco hornworm Manduca sexta L. at 2.6 A resolution. EMBO J. 1987 Jun;6(6):1565–1570. doi: 10.1002/j.1460-2075.1987.tb02401.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  65. Hollenberg M. D. Protease-mediated signalling: new paradigms for cell regulation and drug development. Trends Pharmacol Sci. 1996 Jan;17(1):3–6. doi: 10.1016/0165-6147(96)81562-8. [DOI] [PubMed] [Google Scholar]
  66. Holzfeind P., Merschak P., Dieplinger H., Redl B. The human lacrimal gland synthesizes apolipoprotein D mRNA in addition to tear prealbumin mRNA, both species encoding members of the lipocalin superfamily. Exp Eye Res. 1995 Oct;61(4):495–500. doi: 10.1016/s0014-4835(05)80145-9. [DOI] [PubMed] [Google Scholar]
  67. Hraba-Renevey S., Türler H., Kress M., Salomon C., Weil R. SV40-induced expression of mouse gene 24p3 involves a post-transcriptional mechanism. Oncogene. 1989 May;4(5):601–608. [PubMed] [Google Scholar]
  68. Huber R., Schneider M., Epp O., Mayr I., Messerschmidt A., Pflugrath J., Kayser H. Crystallization, crystal structure analysis and preliminary molecular model of the bilin binding protein from the insect Pieris brassicae. J Mol Biol. 1987 May 20;195(2):423–434. doi: 10.1016/0022-2836(87)90661-9. [DOI] [PubMed] [Google Scholar]
  69. Huber R., Schneider M., Mayr I., Müller R., Deutzmann R., Suter F., Zuber H., Falk H., Kayser H. Molecular structure of the bilin binding protein (BBP) from Pieris brassicae after refinement at 2.0 A resolution. J Mol Biol. 1987 Dec 5;198(3):499–513. doi: 10.1016/0022-2836(87)90296-8. [DOI] [PubMed] [Google Scholar]
  70. Hänsch G. M. The homologous species restriction of the complement attack: structure and function of the C8 binding protein. Curr Top Microbiol Immunol. 1989;140:109–118. doi: 10.1007/978-3-642-73911-8_9. [DOI] [PubMed] [Google Scholar]
  71. Itoh Y., Kawai T. Human alpha 1-microglobulin: its measurement and clinical significance. J Clin Lab Anal. 1990;4(5):376–384. doi: 10.1002/jcla.1860040511. [DOI] [PubMed] [Google Scholar]
  72. Julkunen M., Seppälä M., Jänne O. A. Complete amino acid sequence of human placental protein 14: a progesterone-regulated uterine protein homologous to beta-lactoglobulins. Proc Natl Acad Sci U S A. 1988 Dec;85(23):8845–8849. doi: 10.1073/pnas.85.23.8845. [DOI] [PMC free article] [PubMed] [Google Scholar]
  73. Kasik J. W., Rice E. J. An increase in expression of the lipocalin 24p3 is found in mouse uterus coincident with birth. Am J Obstet Gynecol. 1995 Aug;173(2):613–617. doi: 10.1016/0002-9378(95)90291-0. [DOI] [PubMed] [Google Scholar]
  74. Keen J. N., Caceres I., Eliopoulos E. E., Zagalsky P. F., Findlay J. B. Complete sequence and model for the A2 subunit of the carotenoid pigment complex, crustacyanin. Eur J Biochem. 1991 Apr 23;197(2):407–417. doi: 10.1111/j.1432-1033.1991.tb15925.x. [DOI] [PubMed] [Google Scholar]
  75. Kjeldsen L., Johnsen A. H., Sengeløv H., Borregaard N. Isolation and primary structure of NGAL, a novel protein associated with human neutrophil gelatinase. J Biol Chem. 1993 May 15;268(14):10425–10432. [PubMed] [Google Scholar]
  76. Knopf J. L., Gallagher J. F., Held W. A. Differential, multihormonal regulation of the mouse major urinary protein gene family in the liver. Mol Cell Biol. 1983 Dec;3(12):2232–2240. doi: 10.1128/mcb.3.12.2232. [DOI] [PMC free article] [PubMed] [Google Scholar]
  77. Kock K., Morley S. D., Mullins J. J., Schmale H. Denatonium bitter tasting among transgenic mice expressing rat von Ebner's gland protein. Physiol Behav. 1994 Dec;56(6):1173–1177. doi: 10.1016/0031-9384(94)90362-x. [DOI] [PubMed] [Google Scholar]
  78. Kremer J. M., Wilting J., Janssen L. H. Drug binding to human alpha-1-acid glycoprotein in health and disease. Pharmacol Rev. 1988 Mar;40(1):1–47. [PubMed] [Google Scholar]
  79. Lee K. H., Wells R. G., Reed R. R. Isolation of an olfactory cDNA: similarity to retinol-binding protein suggests a role in olfaction. Science. 1987 Feb 27;235(4792):1053–1056. doi: 10.1126/science.3493528. [DOI] [PubMed] [Google Scholar]
  80. Liu H. M., Lei H. Y., Schmid K. Alpha 1-acid glycoprotein and peripheral nerve injury, studied with a wound chamber. Lab Invest. 1993 May;68(5):577–583. [PubMed] [Google Scholar]
  81. Liu Q., Nilsen-Hamilton M. Identification of a new acute phase protein. J Biol Chem. 1995 Sep 22;270(38):22565–22570. doi: 10.1074/jbc.270.38.22565. [DOI] [PubMed] [Google Scholar]
  82. López-Boado Y. S., Tolivia J., López-Otín C. Apolipoprotein D gene induction by retinoic acid is concomitant with growth arrest and cell differentiation in human breast cancer cells. J Biol Chem. 1994 Oct 28;269(43):26871–26878. [PubMed] [Google Scholar]
  83. Lögdberg L., Akerström B., Shevach E. M. Alpha 1-microglobulin is mitogenic for guinea pig lymphocytes. Scand J Immunol. 1986 Nov;24(5):575–581. doi: 10.1111/j.1365-3083.1986.tb02173.x. [DOI] [PubMed] [Google Scholar]
  84. Malaba L., Smeland S., Senoo H., Norum K. R., Berg T., Blomhoff R., Kindberg G. M. Retinol-binding protein and asialo-orosomucoid are taken up by different pathways in liver cells. J Biol Chem. 1995 Jun 30;270(26):15686–15692. doi: 10.1074/jbc.270.26.15686. [DOI] [PubMed] [Google Scholar]
  85. Matuo Y., Nishi N., Tanaka Y., Muguruma Y., Tanaka K., Akatsuka Y., Matsui S. I., Sandberg A. A., Wada F. Changes of an androgen-dependent nuclear protein during functional differentiation and by dedifferentiation of the dorsolateral prostate of rats. Biochem Biophys Res Commun. 1984 Jan 30;118(2):467–473. doi: 10.1016/0006-291x(84)91326-3. [DOI] [PubMed] [Google Scholar]
  86. Meheus L. A., Fransen L. M., Raymackers J. G., Blockx H. A., Van Beeumen J. J., Van Bun S. M., Van de Voorde A. Identification by microsequencing of lipopolysaccharide-induced proteins secreted by mouse macrophages. J Immunol. 1993 Aug 1;151(3):1535–1547. [PubMed] [Google Scholar]
  87. Miyawaki A., Matsushita F., Ryo Y., Mikoshiba K. Possible pheromone-carrier function of two lipocalin proteins in the vomeronasal organ. EMBO J. 1994 Dec 15;13(24):5835–5842. doi: 10.1002/j.1460-2075.1994.tb06927.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  88. Monaco H. L., Rizzi M., Coda A. Structure of a complex of two plasma proteins: transthyretin and retinol-binding protein. Science. 1995 May 19;268(5213):1039–1041. doi: 10.1126/science.7754382. [DOI] [PubMed] [Google Scholar]
  89. Monaco H. L., Zanotti G. Three-dimensional structure and active site of three hydrophobic molecule-binding proteins with significant amino acid sequence similarity. Biopolymers. 1992 Apr;32(4):457–465. doi: 10.1002/bip.360320425. [DOI] [PubMed] [Google Scholar]
  90. Morais Cabral J. H., Atkins G. L., Sánchez L. M., López-Boado Y. S., López-Otin C., Sawyer L. Arachidonic acid binds to apolipoprotein D: implications for the protein's function. FEBS Lett. 1995 Jun 5;366(1):53–56. doi: 10.1016/0014-5793(95)00484-q. [DOI] [PubMed] [Google Scholar]
  91. Morel L., Dufaure J. P., Depeiges A. LESP, an androgen-regulated lizard epididymal secretory protein family identified as a new member of the lipocalin superfamily. J Biol Chem. 1993 May 15;268(14):10274–10281. [PubMed] [Google Scholar]
  92. Morrow D. M., Xiong N., Getty R. R., Ratajczak M. Z., Morgan D., Seppala M., Riittinen L., Gewirtz A. M., Tykocinski M. L. Hematopoietic placental protein 14. An immunosuppressive factor in cells of the megakaryocytic lineage. Am J Pathol. 1994 Dec;145(6):1485–1495. [PMC free article] [PubMed] [Google Scholar]
  93. Mucignat-Caretta C., Caretta A., Cavaggioni A. Acceleration of puberty onset in female mice by male urinary proteins. J Physiol. 1995 Jul 15;486(Pt 2):517–522. doi: 10.1113/jphysiol.1995.sp020830. [DOI] [PMC free article] [PubMed] [Google Scholar]
  94. Mägert H. J., Hadrys T., Cieslak A., Gröger A., Feller S., Forssmann W. G. cDNA sequence and expression pattern of the putative pheromone carrier aphrodisin. Proc Natl Acad Sci U S A. 1995 Mar 14;92(6):2091–2095. doi: 10.1073/pnas.92.6.2091. [DOI] [PMC free article] [PubMed] [Google Scholar]
  95. Nagata A., Suzuki Y., Igarashi M., Eguchi N., Toh H., Urade Y., Hayaishi O. Human brain prostaglandin D synthase has been evolutionarily differentiated from lipophilic-ligand carrier proteins. Proc Natl Acad Sci U S A. 1991 May 1;88(9):4020–4024. doi: 10.1073/pnas.88.9.4020. [DOI] [PMC free article] [PubMed] [Google Scholar]
  96. Nakano T., Graf T. Identification of genes differentially expressed in two types of v-myb-transformed avian myelomonocytic cells. Oncogene. 1992 Mar;7(3):527–534. [PubMed] [Google Scholar]
  97. Newcomer M. E., Ong D. E. Purification and crystallization of a retinoic acid-binding protein from rat epididymis. Identity with the major androgen-dependent epididymal proteins. J Biol Chem. 1990 Aug 5;265(22):12876–12879. [PubMed] [Google Scholar]
  98. Newcomer M. E. Structure of the epididymal retinoic acid binding protein at 2.1 A resolution. Structure. 1993 Sep 15;1(1):7–18. doi: 10.1016/0969-2126(93)90004-z. [DOI] [PubMed] [Google Scholar]
  99. North A. C. Three-dimensional arrangement of conserved amino acid residues in a superfamily of specific ligand-binding proteins. Int J Biol Macromol. 1989 Feb;11(1):56–58. doi: 10.1016/0141-8130(89)90041-x. [DOI] [PubMed] [Google Scholar]
  100. Noy N., Blaner W. S. Interactions of retinol with binding proteins: studies with rat cellular retinol-binding protein and with rat retinol-binding protein. Biochemistry. 1991 Jul 2;30(26):6380–6386. doi: 10.1021/bi00240a005. [DOI] [PubMed] [Google Scholar]
  101. Noy N., Xu Z. J. Interactions of retinol with binding proteins: implications for the mechanism of uptake by cells. Biochemistry. 1990 Apr 24;29(16):3878–3883. doi: 10.1021/bi00468a012. [DOI] [PubMed] [Google Scholar]
  102. Okamoto N., Uchida A., Takakura K., Kariya Y., Kanzaki H., Riittinen L., Koistinen R., Seppälä M., Mori T. Suppression by human placental protein 14 of natural killer cell activity. Am J Reprod Immunol. 1991 Dec;26(4):137–142. doi: 10.1111/j.1600-0897.1991.tb00713.x. [DOI] [PubMed] [Google Scholar]
  103. Papiz M. Z., Sawyer L., Eliopoulos E. E., North A. C., Findlay J. B., Sivaprasadarao R., Jones T. A., Newcomer M. E., Kraulis P. J. The structure of beta-lactoglobulin and its similarity to plasma retinol-binding protein. 1986 Nov 27-Dec 3Nature. 324(6095):383–385. doi: 10.1038/324383a0. [DOI] [PubMed] [Google Scholar]
  104. Peitsch M. C., Boguski M. S. Is apolipoprotein D a mammalian bilin-binding protein? New Biol. 1990 Feb;2(2):197–206. [PubMed] [Google Scholar]
  105. Pervaiz S., Brew K. Homology of beta-lactoglobulin, serum retinol-binding protein, and protein HC. Science. 1985 Apr 19;228(4697):335–337. doi: 10.1126/science.2580349. [DOI] [PubMed] [Google Scholar]
  106. Pevsner J., Reed R. R., Feinstein P. G., Snyder S. H. Molecular cloning of odorant-binding protein: member of a ligand carrier family. Science. 1988 Jul 15;241(4863):336–339. doi: 10.1126/science.3388043. [DOI] [PubMed] [Google Scholar]
  107. Pevsner J., Trifiletti R. R., Strittmatter S. M., Snyder S. H. Isolation and characterization of an olfactory receptor protein for odorant pyrazines. Proc Natl Acad Sci U S A. 1985 May;82(9):3050–3054. doi: 10.1073/pnas.82.9.3050. [DOI] [PMC free article] [PubMed] [Google Scholar]
  108. Provost P. R., Marcel Y. L., Milne R. W., Weech P. K., Rassart E. Apolipoprotein D transcription occurs specifically in nonproliferating quiescent and senescent fibroblast cultures. FEBS Lett. 1991 Sep 23;290(1-2):139–141. doi: 10.1016/0014-5793(91)81244-3. [DOI] [PubMed] [Google Scholar]
  109. Pérez M. D., Díaz de Villegas C., Sánchez L., Aranda P., Ena J. M., Calvo M. Interaction of fatty acids with beta-lactoglobulin and albumin from ruminant milk. J Biochem. 1989 Dec;106(6):1094–1097. doi: 10.1093/oxfordjournals.jbchem.a122971. [DOI] [PubMed] [Google Scholar]
  110. Redl B., Holzfeind P., Lottspeich F. cDNA cloning and sequencing reveals human tear prealbumin to be a member of the lipophilic-ligand carrier protein superfamily. J Biol Chem. 1992 Oct 5;267(28):20282–20287. [PubMed] [Google Scholar]
  111. Riley C. T., Barbeau B. K., Keim P. S., Kézdy F. J., Heinrikson R. L., Law J. H. The covalent protein structure of insecticyanin, a blue biliprotein from the hemolymph of the tobacco hornworm, Manduca sexta L. J Biol Chem. 1984 Nov 10;259(21):13159–13165. [PubMed] [Google Scholar]
  112. Roy A. K., Chatterjee B., Demyan W. F., Milin B. S., Motwani N. M., Nath T. S., Schiop M. J. Hormone and age-dependent regulation of alpha 2u-globulin gene expression. Recent Prog Horm Res. 1983;39:425–461. doi: 10.1016/b978-0-12-571139-5.50015-x. [DOI] [PubMed] [Google Scholar]
  113. Roy A. K., Neuhaus O. W. Proof of the hepatic synthesis of a sex-dependent protein in the rat. Biochim Biophys Acta. 1966 Sep 26;127(1):82–87. doi: 10.1016/0304-4165(66)90478-8. [DOI] [PubMed] [Google Scholar]
  114. Said H. M., Ong D. E., Shingleton J. L. Intestinal uptake of retinol: enhancement by bovine milk beta-lactoglobulin. Am J Clin Nutr. 1989 Apr;49(4):690–694. doi: 10.1093/ajcn/49.4.690. [DOI] [PubMed] [Google Scholar]
  115. Schmale H., Ahlers C., Bläker M., Kock K., Spielman A. I. Perireceptor events in taste. Ciba Found Symp. 1993;179:167–185. doi: 10.1002/9780470514511.ch11. [DOI] [PubMed] [Google Scholar]
  116. Schmale H., Holtgreve-Grez H., Christiansen H. Possible role for salivary gland protein in taste reception indicated by homology to lipophilic-ligand carrier proteins. Nature. 1990 Jan 25;343(6256):366–369. doi: 10.1038/343366a0. [DOI] [PubMed] [Google Scholar]
  117. Schubert D., LaCorbiere M., Esch F. A chick neural retina adhesion and survival molecule is a retinol-binding protein. J Cell Biol. 1986 Jun;102(6):2295–2301. doi: 10.1083/jcb.102.6.2295. [DOI] [PMC free article] [PubMed] [Google Scholar]
  118. Schubert D., LaCorbiere M. Isolation of a cell-surface receptor for chick neural retina adherons. J Cell Biol. 1985 Jan;100(1):56–63. doi: 10.1083/jcb.100.1.56. [DOI] [PMC free article] [PubMed] [Google Scholar]
  119. Schubert D., LaCorbiere M. Isolation of an adhesion-mediating protein from chick neural retina adherons. J Cell Biol. 1985 Sep;101(3):1071–1077. doi: 10.1083/jcb.101.3.1071. [DOI] [PMC free article] [PubMed] [Google Scholar]
  120. Senoo H., Stang E., Nilsson A., Kindberg G. M., Berg T., Roos N., Norum K. R., Blomhoff R. Internalization of retinol-binding protein in parenchymal and stellate cells of rat liver. J Lipid Res. 1990 Jul;31(7):1229–1239. [PubMed] [Google Scholar]
  121. Seppälä M., Koistinen R., Rutanen E. M. Uterine endocrinology and paracrinology: insulin-like growth factor binding protein-1 and placental protein 14 revisited. Hum Reprod. 1994 May;9(5):917–925. doi: 10.1093/oxfordjournals.humrep.a138617. [DOI] [PubMed] [Google Scholar]
  122. Shaw P. H., Held W. A., Hastie N. D. The gene family for major urinary proteins: expression in several secretory tissues of the mouse. Cell. 1983 Mar;32(3):755–761. doi: 10.1016/0092-8674(83)90061-2. [DOI] [PubMed] [Google Scholar]
  123. Simard J., Veilleux R., de Launoit Y., Haagensen D. E., Labrie F. Stimulation of apolipoprotein D secretion by steroids coincides with inhibition of cell proliferation in human LNCaP prostate cancer cells. Cancer Res. 1991 Aug 15;51(16):4336–4341. [PubMed] [Google Scholar]
  124. Singer A. G., Macrides F., Clancy A. N., Agosta W. C. Purification and analysis of a proteinaceous aphrodisiac pheromone from hamster vaginal discharge. J Biol Chem. 1986 Oct 5;261(28):13323–13326. [PubMed] [Google Scholar]
  125. Sivaprasadarao A., Boudjelal M., Findlay J. B. Lipocalin structure and function. Biochem Soc Trans. 1993 Aug;21(3):619–622. doi: 10.1042/bst0210619. [DOI] [PubMed] [Google Scholar]
  126. Sivaprasadarao A., Findlay J. B. The mechanism of uptake of retinol by plasma-membrane vesicles. Biochem J. 1988 Oct 15;255(2):571–579. [PMC free article] [PubMed] [Google Scholar]
  127. Smeland S., Bjerknes T., Malaba L., Eskild W., Norum K. R., Blomhoff R. Tissue distribution of the receptor for plasma retinol-binding protein. Biochem J. 1995 Jan 15;305(Pt 2):419–424. doi: 10.1042/bj3050419. [DOI] [PMC free article] [PubMed] [Google Scholar]
  128. Snyder S. H., Sklar P. B., Pevsner J. Molecular mechanisms of olfaction. J Biol Chem. 1988 Oct 5;263(28):13971–13974. [PubMed] [Google Scholar]
  129. Sodetz J. M. Structure and function of C8 in the membrane attack sequence of complement. Curr Top Microbiol Immunol. 1989;140:19–31. doi: 10.1007/978-3-642-73911-8_3. [DOI] [PubMed] [Google Scholar]
  130. Spence A. M., Sheppard P. C., Davie J. R., Matuo Y., Nishi N., McKeehan W. L., Dodd J. G., Matusik R. J. Regulation of a bifunctional mRNA results in synthesis of secreted and nuclear probasin. Proc Natl Acad Sci U S A. 1989 Oct;86(20):7843–7847. doi: 10.1073/pnas.86.20.7843. [DOI] [PMC free article] [PubMed] [Google Scholar]
  131. Spreyer P., Schaal H., Kuhn G., Rothe T., Unterbeck A., Olek K., Müller H. W. Regeneration-associated high level expression of apolipoprotein D mRNA in endoneurial fibroblasts of peripheral nerve. EMBO J. 1990 Aug;9(8):2479–2484. doi: 10.1002/j.1460-2075.1990.tb07426.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  132. Suter F., Kayser H., Zuber H. The complete amino-acid sequence of the bilin-binding protein from Pieris brassicae and its similarity to a family of serum transport proteins like the retinol-binding proteins. Biol Chem Hoppe Seyler. 1988 Jun;369(6):497–505. doi: 10.1515/bchm3.1988.369.1.497. [DOI] [PubMed] [Google Scholar]
  133. Sánchez D., Ganfornina M. D., Bastiani M. J. Developmental expression of the lipocalin Lazarillo and its role in axonal pathfinding in the grasshopper embryo. Development. 1995 Jan;121(1):135–147. doi: 10.1242/dev.121.1.135. [DOI] [PubMed] [Google Scholar]
  134. Tejler L., Grubb A. O. A complex-forming glycoprotein heterogeneous in charge and present in human plasma, urine, and cerebrospinal fluid. Biochim Biophys Acta. 1976 Jul 19;439(1):82–94. doi: 10.1016/0005-2795(76)90164-1. [DOI] [PubMed] [Google Scholar]
  135. Triebel S., Bläser J., Reinke H., Tschesche H. A 25 kDa alpha 2-microglobulin-related protein is a component of the 125 kDa form of human gelatinase. FEBS Lett. 1992 Dec 21;314(3):386–388. doi: 10.1016/0014-5793(92)81511-j. [DOI] [PubMed] [Google Scholar]
  136. Urade Y., Nagata A., Suzuki Y., Fujii Y., Hayaishi O. Primary structure of rat brain prostaglandin D synthetase deduced from cDNA sequence. J Biol Chem. 1989 Jan 15;264(2):1041–1045. [PubMed] [Google Scholar]
  137. Zagalsky P. F., Eliopoulos E. E., Findlay J. B. The architecture of invertebrate carotenoproteins. Comp Biochem Physiol B. 1990;97(1):1–18. doi: 10.1016/0305-0491(90)90171-o. [DOI] [PubMed] [Google Scholar]
  138. Zagalsky P. F. Invertebrate carotenoproteins. Methods Enzymol. 1985;111:216–247. doi: 10.1016/s0076-6879(85)11011-6. [DOI] [PubMed] [Google Scholar]

Articles from Biochemical Journal are provided here courtesy of The Biochemical Society

RESOURCES