The retinol esterifying enzyme LRAT supports cell signaling by retinol-binding protein and its receptor STRA6

FASEB Journal

Volumn 28, Issue 1, 2014, Pages 26-34

  Marwarha, Gurdeep ^a   Berry, Daniel C ^a,b   Croniger, Colleen M ^a   Noy, Noa ^a  

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

^b UNIVERSITY OF TEXAS SOUTHWESTERN MEDICAL CENTER   (United States)

Author keywords

Cytokine receptors; Insulin receptor; JAK; Obesity; STAT; Vitamin A metabolism

Indexed keywords

CYTOKINE RECEPTOR; JANUS KINASE 2; LECITHIN RETINOL ACYLTRANSFERASE; LEPTIN RECEPTOR; PROTEIN KINASE B; RETINOL BINDING PROTEIN; STAT5 PROTEIN; STRA6 PROTEIN; SUPPRESSOR OF CYTOKINE SIGNALING 3; UNCLASSIFIED DRUG; ACYLTRANSFERASE; INSULIN RECEPTOR; LECITHIN-RETINOL ACYLTRANSFERASE; MEMBRANE PROTEIN; RETINOL; SOCS3 PROTEIN, MOUSE; STRA6 PROTEIN, HUMAN; STRA6 PROTEIN, MOUSE; STRA6 PROTEIN, RAT; SUPPRESSOR OF CYTOKINE SIGNALING;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; CONTROLLED STUDY; ENZYME ACTIVATION; ENZYME PHOSPHORYLATION; ESTERIFICATION; FOOD INTAKE; GLUCOSE TOLERANCE TEST; HUMAN; HUMAN CELL; INSULIN RESISTANCE; INSULIN RESPONSE; INTRACELLULAR SIGNALING; LIVER; MALE; MOUSE; NONHUMAN; OBESITY; PRIORITY JOURNAL; PROTEIN BLOOD LEVEL; PROTEIN EXPRESSION; PROTEIN FUNCTION; SIGNAL TRANSDUCTION; SKELETAL MUSCLE; UPREGULATION; VITAMIN METABOLISM; WHITE ADIPOSE TISSUE; ANIMAL; CELL STRAIN 3T3; CELL STRAIN HEPG2; CYTOKINE RECEPTORS; EATING; GENETICS; JAK; METABOLISM; PHYSIOLOGY; REAL TIME POLYMERASE CHAIN REACTION; STAT; VITAMIN A METABOLISM;

CYTOKINE RECEPTORS; INSULIN RECEPTOR; JAK; OBESITY; STAT; VITAMIN A METABOLISM;

ACYLTRANSFERASES; ANIMALS; EATING; GLUCOSE TOLERANCE TEST; HEP G2 CELLS; HUMANS; MEMBRANE PROTEINS; MICE; NIH 3T3 CELLS; REAL-TIME POLYMERASE CHAIN REACTION; RETINOL-BINDING PROTEINS; SUPPRESSOR OF CYTOKINE SIGNALING PROTEINS; VITAMIN A;

EID: 84894537681     PISSN: 08926638     EISSN: 15306860     Source Type: Journal    
DOI: 10.1096/fj.13-234310     Document Type: Article

References (36)

1. Chambon, P. (1996) A decade of molecular biology of retinoic acid receptors. FASEB J. 10, 940-954
2. Shaw, N., Elholm, M., and Noy, N. (2003) Retinoic acid is a high affinity selective ligand for the peroxisome proliferator-activated receptor beta/delta. J. Biol. Chem. 278, 41589-41592
3. 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
4. Raz, A., and Goodman, D. S. (1969) The interaction of thyroxine with human plasma prealbumin and with the prealbuminretinol- binding protein complex. J. Biol. Chem. 244, 3230-3237
5. Bellovino, D., Morimoto, T., Tosetti, F., and Gaetani, S. (1996) Retinol binding protein and transthyretin are secreted as a complex formed in the endoplasmic reticulum in HepG2 human hepatocarcinoma cells. Exp. Cell Res. 222, 77-83
6. 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
7. Noy, N. (2000) Retinoid-binding proteins: mediators of retinoid action. Biochem. J. 348(Pt. 3), 481-495
8. 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
9. Ghyselinck, N. B., Bavik, C., Sapin, V., Mark, M., Bonnier, D., Hindelang, C., Dierich, A., Nilsson, C. B., Hakansson, H., Sauvant, P., Azais-Braesco, V., Frasson, M., Picaud, S., and Chambon, P. (1999) Cellular retinol-binding protein I is essential for vitamin A homeostasis. EMBO J. 18, 4903-4914
10. Ong, D. E., MacDonald, P. N., and Gubitosi, A. M. (1988) Esterification of retinol in rat liver. Possible participation by cellular retinol-binding protein and cellular retinol-binding protein II. J. Biol. Chem. 263, 5789-5796
11. Napoli, J. L., Boerman, M. H., Chai, X., Zhai, Y., and Fiorella, P. D. (1995) Enzymes and binding proteins affecting retinoic acid concentrations. J. Steroid. Biochem. Mol. Biol. 53, 497-502
12. Jiang, W., and Napoli, J. L. (2013) The retinol dehydrogenase Rdh10 localizes to lipid droplets during acyl ester biosynthesis. J. Biol. Chem. 288, 589-597
13. Jiang, W., and Napoli, J. L. (2012) Reorganization of cellular retinol-binding protein type 1 and lecithin: retinol acyltransferase during retinyl ester biosynthesis. Biochim. Biophys. Acta 1820, 859-869
14. Yost, R. W., Harrison, E. H., and Ross, A. C. (1988) Esterification by rat liver microsomes of retinol bound to cellular retinolbinding protein. J. Biol. Chem. 263, 18693-18701
15. Posch, K. C., Burns, R. D., and Napoli, J. L. (1992) Biosynthesis of all-trans-retinoic acid from retinal. Recognition of retinal bound to cellular retinol binding protein (type I) as substrate by a purified cytosolic dehydrogenase. J. Biol. Chem. 267, 19676-19682
16. 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
17. 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 Metabol. 7, 258-268
18. 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
19. 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
20. Croker, B. A., Kiu, H., and Nicholson, S. E. (2008) SOCS regulation of the JAK/STAT signalling pathway. Semin. Cell. Dev. Biol. 19, 414-422
21. D'Ambrosio, D. N., Clugston, R. D., and Blaner, W. S. (2011) Vitamin A metabolism: an update. Nutrients 3, 63-103
22. 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
23. Batten, M. L., Imanishi, Y., Maeda, T., Tu, D. C., Moise, A. R., Bronson, D., Possin, D., Van Gelder, R. N., Baehr, W., and Palczewski, K. (2004) Lecithin-retinol acyltransferase is essential for accumulation of all-trans-retinyl esters in the eye and in the liver. J. Biol. Chem. 279, 10422-10432
24. 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
25. 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
26. Liu, L., and Gudas, L. J. (2005) Disruption of the lecithin: retinol acyltransferase gene makes mice more susceptible to vitamin A deficiency. J. Biol. Chem. 280, 40226-40234
27. Berry, D. C., Jacobs, H., Marwarha, G., Gely-Pernot, A., O'Byrne, S. M., D, D. E. S., Klopfenstein, M., Feret, B., Dennefeld, C., Blaner, W. S., Croniger, C. M., Mark, M., Noy, N., and Ghyselinck, N. B. (2013) The STRA6 receptor is essential for retinol-binding protein-induced insulin resistance but not for maintaining vitamin A homeostasis in tissues other than the eye. J. Biol. Chem.
28. Wang, C. Y., and Liao, J. K. (2012) A mouse model of dietinduced obesity and insulin resistance. Methods Mol. Biol. 821, 421-433
29. 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
30. Posch, K. C., Boerman, M. H., Burns, R. D., and Napoli, J. L. (1991) Holocellular retinol binding protein as a substrate for microsomal retinal synthesis. Biochemistry 30, 6224-6230
31. Orland, M. D., Anwar, K., Cromley, D., Chu, C. H., Chen, L., Billheimer, J. T., Hussain, M. M., and Cheng, D. (2005) Acyl coenzyme A dependent retinol esterification by acyl coenzyme A: diacylglycerol acyltransferase 1. Biochim. Biophys. Acta 1737, 76-82
32. Shih, M. Y., Kane, M. A., Zhou, P., Yen, C. L., Streeper, R. S., Napoli, J. L., and Farese, R. V., Jr. (2009) Retinol esterification by DGAT1 is essential for retinoid homeostasis in murine skin. J. Biol. Chem. 284, 4292-4299
33. Wongsiriroj, N., Piantedosi, R., Palczewski, K., Goldberg, I. J., Johnston, T. P., Li, E., and Blaner, W. S. (2008) The molecular basis of retinoid absorption: a genetic dissection. J. Biol. Chem. 283, 13510-13519
34. O'Byrne, S. M., Wongsiriroj, N., Libien, J., Vogel, S., Goldberg, I. J., Baehr, W., Palczewski, K., and Blaner, W. S. (2005) Retinoid absorption and storage is impaired in mice lacking lecithin: retinol acyltransferase (LRAT). J. Biol. Chem. 280, 35647-35657
35. Mody, N., Graham, T. E., Tsuji, Y., Yang, Q., and Kahn, B. B. (2008) Decreased clearance of serum retinol-binding protein and elevated levels of transthyretin in insulin-resistant ob/ ob mice. Am. J. Physiol. Endocrinol. Metabol. 294, E785-793
36. Bjorbaek, C., El-Haschimi, K., Frantz, J. D., and Flier, J. S. (1999) The role of SOCS-3 in leptin signaling and leptin resistance. J. Biol. Chem. 274, 30059-30065