The STRA6 receptor is essential for retinol-binding proteininduced insulin resistance but not for maintaining vitamin a homeostasis in tissues other than the eye

Journal of Biological Chemistry

Volumn 288, Issue 34, 2013, Pages 24528-24539

  Berry, Daniel C ^a,b   Jacobs, Hugues ^c,d   Marwarha, Gurdeep ^a   Gely Pernot, Aurore ^c   O'Byrne, Sheila M ^e   DeSantis, David ^b   Klopfenstein, Muriel ^c   Feret, Betty ^c   Dennefeld, Christine ^c   Blaner, William S ^e   Croniger, Colleen M ^b   Mark, Manuel ^c   Noy, Noa ^a,b   Ghyselinck, Norbert B ^c  

^a Department of Pharmacology ^*  (United States)

^b CASE WESTERN RESERVE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c UNIVERSITÉ DE STRASBOURG   (France)

^d INSTITUT CLINIQUE DE LA SOURIS   (France)

^e Columbia University ^*  (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BIOLOGICAL FUNCTIONS; INSULIN RESISTANCE; INSULIN SIGNALING; PHYSIOLOGICAL FUNCTIONS; PLASMA MEMBRANE PROTEIN; RETINOIC ACIDS; RETINOL-BINDING PROTEIN; SURFACE RECEPTORS;

ABLATION; BLOOD; CELL MEMBRANES; HISTOLOGY; INSULIN; MAMMALS; PHYSIOLOGY; SIGNALING; TISSUE HOMEOSTASIS;

TISSUE;

INSULIN; MEMBRANE PROTEIN; PROTEIN INHIBITOR; PROTEIN STRA6; RETINOIC ACID; RETINOID; RETINOL; RETINOL BINDING PROTEIN; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; EMBRYO; ENZYME ACTIVATION; ENZYME ACTIVITY; ENZYME REGULATION; ENZYME REPRESSION; EYE; FEMALE; FETUS; GENE; HOMEOSTASIS; IN VIVO STUDY; INSULIN RESISTANCE; INTRACELLULAR SIGNALING; MALE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; SIGNAL TRANSDUCTION; STRA6 GENE; VISUAL SYSTEM FUNCTION;

ADIPOKINES; INSULIN RESISTANCE; JAK KINASE; OBESITY; PHOSPHOLIPID; RBP4; STAT TRANSCRIPTION FACTOR; VITAMIN A;

3T3-L1 CELLS; ANIMALS; EYE; INSULIN; INSULIN RESISTANCE; MEMBRANE PROTEINS; MICE; MICE, KNOCKOUT; OBESITY; RETINOL-BINDING PROTEINS, PLASMA; SIGNAL TRANSDUCTION; VITAMIN A;

EID: 84883171546     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M113.484014     Document Type: Article

References (54)

1. Wilson, J. G., Roth, C. B., and Warkany, J. (1953) An analysis of the syndrome of malformations induced by maternal vitamin A deficiency. Effects of restoration of vitamin A at various times during gestation. Am. J. Anat. 92, 189-217
2. Wald, G. (1968) The molecular basis of visual excitation. Nature 219, 800-807
3. Mark, M., Ghyselinck, N. B., and Chambon, P. (2006) Function of retinoid nuclear receptors: lessons from genetic and pharmacological dissections of the retinoic acid signaling pathway during mouse embryogenesis. Annu. Rev. Pharmacol. Toxicol. 46, 451-480
4. Schug, T. T., Berry, D. C., Shaw, N. S., Travis, S. N., and Noy, N. (2007) Opposing effects of retinoic acid on cell growth result from alternate activation of two different nuclear receptors. Cell 129, 723-733
5. Quadro, L., Hamberger, L., Colantuoni, V., Gottesman, M. E., and Blaner, W. S. (2003) Understanding the physiological role of retinol-binding protein in vitamin A metabolism using transgenic and knockout mouse models. Mol. Aspects Med. 24, 421-430
6. Quadro, L., Blaner, W. S., Salchow, D. J., Vogel, S., Piantedosi, R., Gouras, P., Freeman, S., Cosma, M. P., Colantuoni, V., and Gottesman, M. E. (1999) Impaired retinal function and vitamin A availability in mice lacking retinol-binding protein. EMBO J. 18, 4633-4644
7. Ghyselinck, N. B., Vernet, N., Dennefeld, C., Giese, N., Nau, H., Chambon, P., Viville, S., and Mark, M. (2006) Retinoids and spermatogenesis: lessons from mutant mice lacking the plasma retinol-binding protein. Dev. Dyn. 235, 1608-1622
8. Quadro, L., Hamberger, L., Gottesman, M. E., Wang, F., Colantuoni, V., Blaner, W. S., and Mendelsohn, C. L. (2005) Pathways of vitamin A delivery to the embryo: insights from a new tunable model of embryonic vitamin A deficiency. Endocrinology 146, 4479-4490
9. 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 4 contributes to insulin resistance in obesity and type 2 diabetes. Nature 436, 356-362
10. Noy, N. (2000) Retinoid-binding proteins: mediators of retinoid action. Biochem. J. 348, 481-495
11. Fex, G., and Johannesson, G. (1988) Retinol transfer across and between phospholipid bilayer membranes. Biochim. Biophys. Acta 944, 249-255
12. Noy, N., and Xu, Z. J. (1990) Kinetic parameters of the interactions of retinol with lipid bilayers. Biochemistry 29, 3883-3888
13. Heller, J. (1975) Interactions of plasma retinol-binding protein with its receptor. Specific binding of bovine and human retinol-binding protein to pigment epithelium cells from bovine eyes. J. Biol. Chem. 250, 3613-3619
14. Shingleton, J. L., Skinner, M. K., and Ong, D. E. (1989) Characteristics of retinol accumulation from serum retinol-binding protein by cultured Sertoli cells. Biochemistry 28, 9641-9647
15. 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
16. 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
17. 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
18. 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
19. 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-E681
20. Biesalski, H. K., Frank, J., Beck, S. C., Heinrich, F., Illek, B., Reifen, R., Gollnick, H., Seeliger, M. W., Wissinger, B., and Zrenner, E. (1999) Biochemical but not clinical vitamin A deficiency results from mutations in the gene for retinol-binding protein. Am. J. Clin. Nutr. 69, 931-936
21. 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
22. 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
23. Berry, D. C., Croniger, C. M., Ghyselinck, N. B., and Noy, N. (2012) Transthyretin blocks retinol uptake and cell signalling by the holo-retinol-binding protein receptor STRA6. Mol. Cell. Biol. 32, 3851-3859
24. Berry, D. C., O'Byrne, S. M., Vreeland, A. C., Blaner, W. S., and Noy, N. (2012) Cross talk between signaling and vitamin A transport by the retinol-binding protein receptor STRA6. Mol. Cell. Biol. 32, 3164-3175
25. Starr, R., Willson, T. A., Viney, E. M., Murray, L. J., Rayner, J. R., Jenkins, B. J., Gonda, T. J., Alexander, W. S., Metcalf, D., Nicola, N. A., and Hilton, D. J. (1997) A family of cytokine-inducible inhibitors of signalling. Nature 387, 917-921
26. Ruiz, A., Mark, M., Jacobs, H., Klopfenstein, M., Hu, J., Lloyd, M., Habib, S., Tosha, C., Radu, R. A., Ghyselinck, N. B., Nusinowitz, S., and Bok, D. (2012) Retinoid content, visual responses, and ocular morphology are compromised in the retinas of mice lacking the retinol-binding protein receptor, STRA6. Invest. Ophthalmol. Vis. Sci. 53, 3027-3039
27. Rodríguez, C. I., Buchholz, F., Galloway, J., Sequerra, R., Kasper, J., Ayala, R., Stewart, A. F., and Dymecki, S. M. (2000) High-efficiency deleter mice show that FLPe is an alternative to Cre-loxP. Nat. Genet. 25, 139-140
28. Dupé, V., Davenne, M., Brocard, J., Dollé, P., Mark, M., Dierich, A., Chambon, P., and Rijli, F. M. (1997) In vivo functional analysis of the Hoxa-1 3′-retinoic acid response element (3′RARE). Development 124, 399-410
29. Antal, C., Teletin, M., Wendling, O., Dgheem, M., Auwerx, J., and Mark, M. (2007) Tissue collection for systematic phenotyping in the mouse. Curr. Protoc. Mol. Biol. Chapter 29, Unit 29A.4
30. Vernet, N., Dennefeld, C., Guillou, F., Chambon, P., Ghyselinck, N. B., and Mark, M. (2006) Prepubertal testis development relies on retinoic acid but not rexinoid receptors in Sertoli cells. EMBO J. 25, 5816-5825
31. Sanes, J. R., Rubenstein, J. L., and Nicolas, J. F. (1986) Use of a recombinant retrovirus to study post-implantation cell lineage in mouse embryos. EMBO J. 5, 3133-3142
32. Wei, S., Episkopou, V., Piantedosi, R., Maeda, S., Shimada, K., Gottesman, M. E., and Blaner, W. S. (1995) Studies on the metabolism of retinol and retinol-binding protein in transthyretin-deficient mice produced by homologous recombination. J. Biol. Chem. 270, 866-870
33. Blaner, W. S., Das, S. R., Gouras, P., and Flood, M. T. (1987) Hydrolysis of 11-cis-and all-trans-retinyl palmitate by homogenates of human retinal epithelial cells. J. Biol. Chem. 262, 53-58
34. 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
35. Ruan, H., Zarnowski, M. J., Cushman, S. W., and Lodish, H. F. (2003) Standard isolation of primary adipose cells from mouse epididymal fat pads induces inflammatory mediators and down-regulates adipocyte genes. J. Biol. Chem. 278, 47585-47593
36. Ayala, J. E., Bracy, D. P., McGuinness, O. P., and Wasserman, D. H. (2006) Considerations in the design of hyperinsulinemic-euglycemic clamps in the conscious mouse. Diabetes 55, 390-397
37. 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
38. Alapatt, P., Guo, F., Komanetsky, S. M., Wang, S., Cai, J., Sargsyan, A., Rodríguez Díaz, E., Bacon, B. T., Aryal, P., and Graham, T. E. (2013) Liver retinol transporter and receptor for serum retinol-binding protein (RBP4). J. Biol. Chem. 288, 1250-1265
39. Mark, M., Teletin, M., Antal, C., Wendling, O., Auwerx, J., Heikkinen, S., Khetchoumian, K., Argmann, C. A., and Dgheem, M. (2007) Histopathology in mouse metabolic investigations. Curr. Protoc. Mol. Biol. Chapter 29, Unit 29B.4
40. Rossant, J., Zirngibl, R., Cado, D., Shago, M., and Giguère, V. (1991) Expression of a retinoic acid response element-hsplacZ transgene defines specific domains of transcriptional activity during mouse embryogenesis. Genes Dev. 5, 1333-1344
41. Niederreither, K., and Dollé, P. (2008) Retinoic acid in development: towardan integrated view. Nat. Rev. Genet. 9, 541-553
42. Duester, G. (2008) Retinoic acid synthesis and signaling during early organogenesis. Cell 134, 921-931
43. 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
44. Geelen, J. A. (1979) Hypervitaminosis A induced teratogenesis. CRC Crit. Rev. Toxicol. 6, 351-375
45. Kim, Y. K., Wassef, L., Hamberger, L., Piantedosi, R., Palczewski, K., Blaner, W. S., and Quadro, L. (2008) Retinyl ester formation by lecithin: retinol acyltransferase is a key regulator of retinoid homeostasis in mouse embryogenesis. J. Biol. Chem. 283, 5611-5621
46. Ruiz, A., Ghyselinck, N. B., Mata, N., Nusinowitz, S., Lloyd, M., Dennefeld, C., Chambon, P., and Bok, D. (2007) Somatic ablation of the Lrat gene in the mouse retinal pigment epithelium drastically reduces its retinoid storage. Invest. Ophthalmol. Vis. Sci. 48, 5377-5387
47. Soprano, D. R., Pickett, C. B., Smith, J. E., and Goodman, D. S. (1981) Biosynthesis of plasma retinol-binding protein in liver as a larger molecular weight precursor. J. Biol. Chem. 256, 8256-8258
48. Xie, Y., Lashuel, H. A., Miroy, G. J., Dikler, S., and Kelly, J. W. (1998) Recombinant human retinol-binding protein refolding, native disulfide formation, and characterization. Protein Expr. Purif. 14, 31-37
49. Green, H., and Kehinde, O. (1975) An established preadipose cell line and its differentiation in culture. II. Factors affecting the adipose conversion. Cell 5, 19-27
50. Green, H., and Meuth, M. (1974) An established pre-adipose cell line and its differentiation in culture. Cell 3, 127-133
51. Lehrke, M., and Lazar, M. A. (2005) The many faces of PPARγ. Cell 123, 993-999
52. Wang, C. Y., and Liao, J. K. (2012) A mouse model of diet-induced obesity and insulin resistance. Methods Mol. Biol. 821, 421-433
53. Gavrilova, R., Babovic, N., Lteif, A., Eidem, B., Kirmani, S., Olson, T., and Babovic-Vuksanovic, D. (2009) Vitamin A deficiency in an infant with PAGOD syndrome. Am. J. Med. Genet. A 149A, 2241-2247
54. Cirillo, D., Rachiglio, A. M., la Montagna, R., Giordano, A., and Normanno, N. (2008) Leptin signaling in breast cancer: an overview. J. Cell. Biochem. 105, 956-964