Liver retinol transporter and receptor for serum retinol-binding protein (RBP4)

Journal of Biological Chemistry

Volumn 288, Issue 2, 2013, Pages 1250-1265

  Alapatt, Philomena ^a,b   Guo, Fangjian ^a,b,d   Komanetsky, Susan M ^a,b,e   Wang, Shuping ^a,b   Cai, Jinjin ^a,b   Sargsyan, Ashot ^a,b   Díaz, Eduardo Rodríguez ^a,b   Bacon, Brandon T ^a,b   Aryal, Pratik ^c   Graham, Timothy E ^a,b  

^a UNIVERSITY OF UTAH SCHOOL OF MEDICINE   (United States)

^b VETERANS AFFAIRS MEDICAL CENTER   (United States)

^c BETH ISRAEL DEACONESS MEDICAL CENTER   (United States)

^d UNIVERSITY OF ALABAMA AT BIRMINGHAM   (United States)

^e PURDUE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADIPOSE TISSUE; CULTURED CELL; HIGH AFFINITY; HIGH-AFFINITY BINDING SITES; IN-VIVO; METABOLIC ACTION; OBESE MICE; RETINOIC ACIDS; RETINOL-BINDING PROTEIN; SMALL INTESTINE; VITAMIN A;

BODY FLUIDS; HISTOLOGY; PROTEINS;

TISSUE;

CARRIER PROTEIN; MEMBRANE PROTEIN; RETINOIC ACID; RETINOL; RETINOL BINDING PROTEIN 4; RETINOL BINDING PROTEIN 4 RECEPTOR 2; STIMULATED BY RETINOIC ACID 6 PROTEIN; UNCLASSIFIED DRUG;

3' UNTRANSLATED REGION; 5' UNTRANSLATED REGION; ADIPOSE TISSUE; AMINO ACID SEQUENCE; ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BINDING AFFINITY; CELL CULTURE; CONTROLLED STUDY; CORRELATION ANALYSIS; FEMALE; GENE SILENCING; GENETIC CONSERVATION; HUMAN; HUMAN CELL; IN VIVO STUDY; INTESTINE; LIVER; MALE; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; OBESITY; OPEN READING FRAME; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN STRUCTURE; PROTEIN TRANSPORT; VERTEBRATE;

AMINO ACID SEQUENCE; ANIMALS; BASE SEQUENCE; CARRIER PROTEINS; CELL LINE; CLONING, MOLECULAR; DNA PRIMERS; HUMANS; LIVER; MEMBRANE PROTEINS; MICE; MICE, INBRED C57BL; MOLECULAR SEQUENCE DATA; POLYMERASE CHAIN REACTION; PROMOTER REGIONS, GENETIC; RETINOL-BINDING PROTEINS, PLASMA; SEQUENCE HOMOLOGY, AMINO ACID; TRANSCRIPTOME;

MUS; VERTEBRATA;

EID: 84872297784     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M112.369132     Document Type: Article

References (76)

1. Norum, K. R., and Blomhoff, R. (1992) McCollum Award Lecture, 1992. Vitamin A absorption, transport, cellular uptake, and storage. Am. J. Clin. Nutr. 56, 735-744
2. Tanumihardjo, S. A. (2011) Vitamin A. Biomarkers of nutrition for development. Am. J. Clin. Nutr. 94, 658S-665S
3. Chambon, P. (1996) A decade of molecular biology of retinoic acid receptors. FASEB J. 10, 940-954
4. McGrane, M. M. (2007) Vitamin A regulation of gene expression. Molecular mechanism of a prototype gene. J. Nutr. Biochem. 18, 497-508
5. Mendoza-Parra, M. A., Walia, M., Sankar, M., and Gronemeyer, H. (2011) Dissecting the retinoid-induced differentiation of F9 embryonal stem cells by integrative genomics. Mol. Syst. Biol. 7, 538
6. Shirakami, Y., Lee, S. A., Clugston, R. D., and Blaner, W. S. (2012) Hepatic metabolism of retinoids and disease associations. Biochim. Biophys. Acta 1821, 124-136
7. Tsutsumi, C., Okuno, M., Tannous, L., Piantedosi, R., Allan, M., Goodman, D. S., and Blaner, W. S. (1992) Retinoids and retinoid-binding protein expression in rat adipocytes. J. Biol. Chem. 267, 1805-1810
8. Blaner, W. S. (1989) Retinol-binding protein. The serum transport protein for vitamin A. Endocr. Rev. 10, 308-316
9. Zanotti, G., and Berni, R. (2004) Plasma retinol-binding protein. Structure and interactions with retinol, retinoids, and transthyretin. Vitam. Horm. 69, 271-295 (Pubitemid 39753925)
10. Lewis, K. C., Green, M. H., Green, J. B., and Zech, L. A. (1990) Retinol metabolism in rats with low vitamin A status. A compartmental model. J. Lipid Res. 31, 1535-1548 (Pubitemid 20321715)
11. Gjøen, T., Bjerkelund, T., Blomhoff, H. K., Norum, K. R., Berg, T., and Blomhoff, R. (1987) Liver takes up retinol-binding protein from plasma. J. Biol. Chem. 262, 10926-10930
12. Smeland, S., Bjerknes, T., Malaba, L., Eskild, W., Norum, K. R., and Blomhoff, R. (1995) Tissue distribution of the receptor for plasma retinol-binding protein. Biochem. J. 305, 419-424
13. Blomhoff, R., Norum, K. R., and Berg, T. (1985) Hepatic uptake of [3H]retinol bound to the serum retinol-binding protein involves both parenchymal and perisinusoidal stellate cells. J. Biol. Chem. 260, 13571-13575 (Pubitemid 16192309)
14. Yamamoto, Y., Yoshizawa, T., Kamio, S., Aoki, O., Kawamata, Y., Masushige, S., and Kato, S. (1997) Interactions of transthyretin (TTR) and retinol-binding protein (RBP) in the uptake of retinol by primary rat hepatocytes. Exp. Cell Res. 234, 373-378 (Pubitemid 27335180)
15. Quadro, L., Blaner, W. S., Hamberger, L., Novikoff, P. M., Vogel, S., Piantedosi, R., Gottesman, M. E., and Colantuoni, V. (2004) The role of extrahepatic retinol binding protein in the mobilization of retinoid stores. J. Lipid Res. 45, 1975-1982 (Pubitemid 40990891)
16. Kawaguchi, R., Yu, J., Honda, J., Hu, J., Whitelegge, J., Ping, P., Wiita, P., Bok, D., and Sun, H. (2007) A membrane receptor for retinol binding protein mediates cellular uptake of vitamin A. Science 315, 820-825
17. Kawaguchi, R., Yu, J., Wiita, P., Ter-Stepanian, M., and Sun, H. (2008) Mapping the membrane topology and extracellular ligand binding domains of the retinol binding protein receptor. Biochemistry 47, 5387-5395 (Pubitemid 351656982)
18. Bouillet, P., Sapin, V., Chazaud, C., Messaddeq, N., Décimo, D., Dollé, P., and Chambon, P. (1997) Developmental expression pattern of Stra6, a retinoic acid-responsive gene encoding a new type of membrane protein. Mech. Dev. 63, 173-186 (Pubitemid 27272702)
19. Golzio, C., Martinovic-Bouriel, J., Thomas, S., Mougou-Zrelli, S., Grattagliano-Bessieres, B., Bonniere, M., Delahaye, S., Munnich, A., Encha- Razavi, F., Lyonnet, S., Vekemans, M., Attie-Bitach, T., and Etchevers, H. C. (2007) Matthew-Wood syndrome is caused by truncating mutations in the retinol-binding protein receptor gene STRA6. Am. J. Hum. Genet. 80, 1179-1187 (Pubitemid 47579353)
20. Pasutto, F., Sticht, H., Hammersen, G., Gillessen-Kaesbach, G., Fitzpatrick, D. R., Nürnberg, G., Brasch, F., Schirmer-Zimmermann, H., Tolmie, J. L., Chitayat, D., Houge, G., Fernández-Martínez, L., Keating, S., Mortier, G., Hennekam, R. C., von der Wense, A., Slavotinek, A., Meinecke, P., Bitoun, P., Becker, C., Nürnberg, P., Reis, A., and Rauch, A. (2007) Mutations in STRA6 cause a broad spectrum of malformations including anophthalmia, congenital heart defects, diaphragmatic hernia, alveolar capillary dysplasia, lung hypoplasia, and mental retardation. Am. J. Hum. Genet. 80, 550-560
21. Chassaing, N., Golzio, C., Odent, S., Lequeux, L., Vigouroux, A., Martinovic-Bouriel, J., Tiziano, F. D., Masini, L., Piro, F., Maragliano, G., Delezoide, A. L., Attié-Bitach, T., Manouvrier-Hanu, S., Etchevers, H. C., and Calvas, P. (2009) Phenotypic spectrum of STRA6 mutations. From Matthew-Wood syndrome to non-lethal anophthalmia. Hum. Mutat. 30, E673-681
22. Chitayat, D., Sroka, H., Keating, S., Colby, R. S., Ryan, G., Toi, A., Blaser, S., Viero, S., Devisme, L., Boute-Bénéjean, O., Manouvrier-Hanu, S., Mortier, G., Loeys, B., Rauch, A., and Bitoun, P. (2007) The PDAC syndrome (pulmonary hypoplasia/agenesis, diaphragmatic hernia/eventration, anophthalmia/ microphthalmia, and cardiac defect) (Spear syndrome, Matthew- Woodsyndrome). Report of eight cases including a living child and further evidence for autosomal recessive inheritance. Am. J. Med. Genet. A 143A, 1268-1281 (Pubitemid 46870092)
23. Slavotinek, A. M. (2011) Eye development genes and known syndromes. Mol. Genet. Metab. 104, 448-456
24. Schnitzer, J. J. (2004) Control and regulation of pulmonary hypoplasia associated with congenital diaphragmatic hernia. Semin. Pediatr. Surg. 13, 37-43
25. Rhinn, M., and Dollé, P. (2012) Retinoic acid signalling during development. Development 139, 843-858
26. Paschaki, M., Lin, S. C., Wong, R. L., Finnell, R. H., Dollé, P., and Niederreither, K. (2012) Retinoic acid-dependent signaling pathways and lineage events in the developing mouse spinal cord. PLoS One 7, e32447
27. Robinson, J. F., Verhoef, A., Pennings, J. L., Pronk, T. E., and Piersma, A. H. (2012) A comparison of gene expression responses in rat whole embryo culture and in vivo. Time-dependent retinoic acid-induced teratogenic response. Toxicol. Sci. 126, 242-254
28. Dereeper, A., Guignon, V., Blanc, G., Audic, S., Buffet, S., Chevenet, F., Dufayard, J. F., Guindon, S., Lefort, V., Lescot, M., Claverie, J. M., and Gascuel, O. (2008) Phylogeny.fr. Robust phylogenetic analysis for the nonspecialist. Nucleic Acids Res. 36, W465-W469
29. Dereeper, A., Audic, S., Claverie, J. M., and Blanc, G. (2010) BLAST-EXPLORER helps you building datasets for phylogenetic analysis. BMC Evol. Biol. 10, 8
30. Venable, C. L., Frevert, E. U., Kim, Y. B., Fischer, B. M., Kamatkar, S., Neel, B. G., and Kahn, B. B. (2000) Overexpression of protein-tyrosine phosphatase-1B in adipocytes inhibits insulin-stimulated phosphoinositide 3-kinase activity without altering glucose transport or Akt/protein kinase B activation. J. Biol. Chem. 275, 18318-18326 (Pubitemid 30414787)
31. Testa, G., Schaft, J., van der Hoeven, F., Glaser, S., Anastassiadis, K., Zhang, Y., Hermann, T., Stremmel, W., and Stewart, A. F. (2004)Areliable lacZ expression reporter cassette for multipurpose, knockout-first alleles. Genesis 38, 151-158 (Pubitemid 38506853)
32. de Vries, W. N., Binns, L. T., Fancher, K. S., Dean, J., Moore, R., Kemler, R., and Knowles, B. B. (2000) Expression of Cre recombinase in mouse oocytes. A means to study maternal effect genes. Genesis 26, 110-112 (Pubitemid 30158090)
33. Shepherd, P. R., Gnudi, L., Tozzo, E., Yang, H., Leach, F., and Kahn, B. B. (1993) Adipose cell hyperplasia and enhanced glucose disposal in transgenic mice overexpressing GLUT4 selectively in adipose tissue. J. Biol. Chem. 268, 22243-22246 (Pubitemid 23318260)
34. Yang, Q., Graham, T. E., Mody, N., Preitner, F., Peroni, O. D., Zabolotny, J. M., Kotani, K., Quadro, L., and Kahn, B. B. (2005) Serum retinol-binding protein contributes to insulin resistance in obesity and type 2 diabetes. Nature 436, 356-362 (Pubitemid 41065039)
35. Kawaguchi, R., Yu, J., Ter-Stepanian, M., Zhong, M., Cheng, G., Yuan, Q., Jin, M., Travis, G. H., Ong, D., and Sun, H. (2011) Receptor-mediated cellular uptake mechanism that couples to intracellular storage. ACS Chem. Biol. 6, 1041-1051
36. Cham, B. E., and Knowles, B. R. (1976) A solvent system for delipidation of plasma or serum without protein precipitation. J. Lipid Res. 17, 176-181
37. Goodman, D. S., and Raz, A. (1972) Extraction and recombination studies of the interaction of retinol with human plasma retinol-binding protein. J. Lipid Res. 13, 338-347
38. Ganguly, J. (1989) Biochemistry of Vitamin A, pp. 63-85, CRC Press, Inc., Boca Raton, FL
39. Abelson, J. N., Simon, M. I., and Sies, H. (1990) Retinoids. Part A. Molecular and metabolic aspects. Methods Enzymol. 189, 3-536
40. Kane, M. A., Folias, A. E., and Napoli, J. L. (2008) HPLC/UV quantitation of retinal, retinol, and retinyl esters in serum and tissues. Anal. Biochem. 378, 71-79
41. Sun, H., and Kawaguchi, R. (2011) The membrane receptor for plasma retinol-binding protein, a new type of cell-surface receptor. Int. Rev. Cell Mol. Biol. 288, 1-41
42. Chen, C. C., and Heller, J. (1977) Uptake of retinol and retinoic acid from serum retinol-binding protein by retinal pigment epithelial cells. J. Biol. Chem. 252, 5216-5221 (Pubitemid 8168388)
43. Sivaprasadarao, A., and Findlay, J. B. (1988) The mechanism of uptake of retinol by plasma-membrane vesicles. Biochem. J. 255, 571-579
44. Vogel, S., Piantedosi, R., Frank, J., Lalazar, A., Rockey, D. C., Friedman, S. L., and Blaner, W. S. (2000) An immortalized rat liver stellate cell line (HSC-T6). A new cell model for the study of retinoid metabolism in vitro. J. Lipid Res. 41, 882-893 (Pubitemid 30434319)
45. Randolph, R. K., and Ross, A. C. (1991) Regulation of retinol uptake and esterification in MCF-7 and HepG2 cells by exogenous fatty acids. J. Lipid Res. 32, 809-820
46. Matsuura, T., and Ross, A. C. (1993) Regulation of hepatic lecithin. Retinol acyltransferase activity by retinoic acid. Arch. Biochem. Biophys. 301, 221-227 (Pubitemid 23214112)
47. Faraonio, R., Galdieri, M., and Colantuoni, V. (1993) Cellular retinoic-acid- binding-protein and retinol-binding-protein mRNA expression in the cells of the rat seminiferous tubules and their regulation by retinoids. Eur. J. Biochem. 211, 835-842 (Pubitemid 23050060)
48. Niederreither, K., McCaffery, P., Dräger, U. C., Chambon, P., and Dollé, P. (1997) Restricted expression and retinoic acid-induced downregulation of the retinaldehyde dehydrogenase type 2 (RALDH-2) gene during mouse development. Mech. Dev. 62, 67-78 (Pubitemid 27165381)
49. Wang, Y., Zolfaghari, R., and Ross, A. C. (2002) Cloning of rat cytochrome P450RAI (CYP26) cDNA and regulation of its gene expression by all-trans- retinoic acid in vivo. Arch. Biochem. Biophys. 401, 235-243 (Pubitemid 34848626)
50. Leid, M., Kastner, P., and Chambon, P. (1992) Multiplicity generates diversity in the retinoic acid signalling pathways. Trends Biochem. Sci. 17, 427-433
51. Capper, N. S. (1930) Carotene and vitamin A. The transformation of carotene into vitamin A as shown by a study of the absorption spectra of rat-liver oils. Biochem. J. 24, 980-982
52. Ahmad, B., and Drummond, J. C. (1930) The relative vitamin A value of the body and liver oils of certain fish. Biochem. J. 24, 27-36
53. Berry, D. C., Jin, H., Majumdar, A., and Noy, N. (2011) Signaling by vitamin A and retinol-binding protein regulates gene expression to inhibit insulin responses. Proc. Natl. Acad. Sci. U.S.A. 108, 4340-4345
54. Berry, D. C., and Noy, N. (2012) Signaling by vitamin A and retinol-binding protein in regulation of insulin responses and lipid homeostasis. Biochim. Biophys. Acta 1821, 168-176
55. Szeto, W., Jiang, W., Tice, D. A., Rubinfeld, B., Hollingshead, P. G., Fong, S. E., Dugger, D. L., Pham, T., Yansura, D. G., Wong, T. A., Grimaldi, J. C., Corpuz, R. T., Singh, J. S., Frantz, G. D., Devaux, B., Crowley, C. W., Schwall, R. H., Eberhard, D. A., Rastelli, L., Polakis, P., and Pennica, D. (2001) Overexpression of the retinoic acid-responsive gene Stra6 in human cancers and its synergistic induction by Wnt-1 and retinoic acid. Cancer Res. 61, 4197-4205 (Pubitemid 32724956)
56. Tice, D. A., Szeto, W., Soloviev, I., Rubinfeld, B., Fong, S. E., Dugger, D. L., Winer, J., Williams, P. M., Wieand, D., Smith, V., Schwall, R. H., Pennica, D., and Polakis, P. (2002) Synergistic induction of tumor antigens by Wnt-1 signaling and retinoic acid revealed by gene expression profiling. J. Biol. Chem. 277, 14329-14335 (Pubitemid 34968050)
57. Cifelli, C. J., Green, J. B., Wang, Z., Yin, S., Russell, R. M., Tang, G., and Green, M. H. (2008) Kinetic analysis shows that vitamin A disposal rate in humans is positively correlated with vitamin A stores. J. Nutr. 138, 971-977 (Pubitemid 351571600)
58. Pitot, H. C., Peraino, C., Morse, P. A., Jr., and Potter, V. R. (1964) Hepatomas in tissue culture compared with adapting liver in vivo. Natl. Cancer Inst. Monogr. 13, 229-245
59. Bernhard, H. P., Darlington, G. J., and Ruddle, F. H. (1973) Expression of liver phenotypes in cultured mouse hepatoma cells. Synthesis and secretion of serum albumin. Dev. Biol. 35, 83-96
60. St. George, S., Friedman, M., and Byers, S. O. (1954) Mass separation of reticuloendothelial and parenchymal cells of rat's liver. Science 120, 463-465
61. Senoo, H., Kojima, N., and Sato, M. (2007) Vitamin A-storing cells (stellate cells). Vitam. Horm. 75, 131-159
62. Blaner, W. S., O'Byrne, S. M., Wongsiriroj, N., Kluwe, J., D'Ambrosio, D. M., Jiang, H., Schwabe, R. F., Hillman, E. M., Piantedosi, R., and Libien, J. (2009) Hepatic stellate cell lipid droplets: a specialized lipid droplet for retinoid storage. Biochim. Biophys. Acta 1791, 467-473
63. Isken, A., Golczak, M., Oberhauser, V., Hunzelmann, S., Driever, W., Imanishi, Y., Palczewski, K., and von Lintig, J. (2008) RBP4 disrupts vitamin A uptake homeostasis in a STRA6-deficient animal model for Matthew-Wood syndrome. Cell Metab. 7, 258-268 (Pubitemid 351285530)
64. Kawaguchi, R., Zhong, M., Kassai, M., Ter-Stepanian, M., and Sun, H. (2012) STRA6-catalyzed vitamin A influx, efflux, and exchange. J. Membr. Biol. 245, 731-745
65. Amengual, J., Golczak, M., Palczewski, K., and von Lintig, J. (2012) Lecithin: retinol acyltransferase is critical for cellular uptake of vitamin A from serum retinol-binding protein. J. Biol. Chem. 287, 24216-24227
66. Graham, T. E., Smith, U., and Kahn, B. B. (2006) Retinol-binding protein 4 and insulin resistance (authors' reply). N. Engl. J. Med. 355, 1394-1395 (Pubitemid 44465489)
67. Munkhtulga, L., Nakayama, K., Utsumi, N., Yanagisawa, Y., Gotoh, T., Omi, T., Kumada, M., Erdenebulgan, B., Zolzaya, K., Lkhagvasuren, T., and Iwamoto, S. (2007) Identification of a regulatory SNP in the retinol binding protein 4 gene associated with type 2 diabetes in Mongolia. Hum. Genet. 120, 879-888 (Pubitemid 46128843)
68. Klöting, N., Graham, T. E., Berndt, J., Kralisch, S., Kovacs, P., Wason, C. J., Fasshauer, M., Schön, M. R., Stumvoll, M., Blüher, M., and Kahn, B. B. (2007) Serum retinol-binding protein is more highly expressed in visceral than in subcutaneous adipose tissue and is a marker of intra-abdominal fat mass. Cell Metab. 6, 79-87
69. Kovacs, P., Geyer, M., Berndt, J., Klöting, N., Graham, T. E., Böttcher, Y., Enigk, B., Tönjes, A., Schleinitz, D., Schön, M. R., Kahn, B. B., Blüher, M., and Stumvoll, M. (2007) Effects of genetic variation in the human retinol binding protein-4 gene (RBP4) on insulin resistance and fat depot-specific mRNA expression. Diabetes 56, 3095-3100 (Pubitemid 350223647)
70. Graham, T. E., and Kahn, B. B. (2007) Tissue-specific alterations of glucose transport and molecular mechanisms of intertissue communication in obesity and type 2 diabetes. Horm. Metab. Res. 39, 717-721 (Pubitemid 350099818)
71. Hahn, S., Backhaus, M., Broecker-Preuss, M., Tan, S., Dietz, T., Kimmig, R., Schmidt, M., Mann, K., and Janssen, O. E. (2007) Retinol-binding protein 4 levels are elevated in polycystic ovary syndrome women with obesity and impaired glucose metabolism. Eur. J. Endocrinol. 157, 201-207 (Pubitemid 47233125)
72. Qi, Q., Yu, Z., Ye, X., Zhao, F., Huang, P., Hu, F. B., Franco, O. H., Wang, J., Li, H., Liu, Y., and Lin, X. (2007) Elevated retinol-binding protein 4 levels are associated with metabolic syndrome in Chinese people. J. Clin. Endocrinol. Metab. 92, 4827-4834 (Pubitemid 350223466)
73. van Hoek, M., Dehghan, A., Zillikens, M. C., Hofman, A., Witteman, J. C., and Sijbrands, E. J. (2008)AnRBP4 promoter polymorphism increases risk of type 2 diabetes. Diabetologia 51, 1423-1428
74. Wu, Y., Li, H., Loos, R. J., Qi, Q., Hu, F. B., Liu, Y., and Lin, X. (2009) RBP4 variants are significantly associated with plasma RBP4 levels and hypertriglyceridemia risk in Chinese Hans. J. Lipid Res. 50, 1479-1486
75. Ost, A., Danielsson, A., Lidén, M., Eriksson, U., Nystrom, F. H., and Strålfors, P. (2007) Retinol-binding protein-4 attenuates insulin-induced phosphorylation of IRS1 and ERK1/2 in primary human adipocytes. FASEB J. 21, 3696-3704 (Pubitemid 350075157)
76. Thompson, J. D., Higgins, D. G., and Gibson, T. J. (1994) CLUSTAL W. Improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties, and weight matrix choice. Nucleic Acids Res. 22, 4673-4680 (Pubitemid 24354800)