Asian-Australasian Journal of Animal Sciences

Asian Australasian Association of Animal Production Societies (아세아태평양축산학회)
권호 표지
DOI QR코드

DOI QR Code

Cloning, Expression, and Regulation of Bovine Cellular Retinoic Acid-binding Protein-II (CRABP-II) during Adipogenesis

  • Jeong, Young Hee (Department of Food and Nutrition, Osaka City University) ;
  • Lee, Sang Mi (Department of Animal Science, Chonnam National University) ;
  • Kim, Hye-Min (Department of Animal Science, Chonnam National University) ;
  • Park, Hyo Young (Department of Animal Science, Chonnam National University) ;
  • Yoon, Duhak (National Livestock Research Institute, Rural Development Administration) ;
  • Moon, Seung Ju (Department of Animal Science, Chonnam National University) ;
  • Hosoda, Akemi (Department of Food and Nutrition, Osaka City University) ;
  • Kim, Dong-Ho (Department of Food and Nutrition, Osaka City University) ;
  • Saeki, Shigeru (Department of Food and Nutrition, Osaka City University) ;
  • Kang, Man-Jong (Department of Animal Science, Chonnam National University)
  • Received : 2007.09.18
  • Accepted : 2008.02.15
  • Published : 2008.11.01
Download PDF
⟨ Previous Next ⟩

Abstract

The mammalian cellular retinoic acid-binding proteins, CRABP-I and CRABP-II, bind retinoic acid which acts as an inducer of differentiation in several biological systems. To investigate a possible role for CRABP-II in bovine adipogenesis, we have cloned bovine CRABP-II cDNA and the coding region for CRABP-I. The predicted amino acid sequences of CRABP-II were highly conserved among several animal species (human, mouse, and rat at 97%, 93%, and 93%, respectively). The expression pattern of bovine CRABP-II was examined in greater details by applying RT-PCR to various bovine tissues. CRABP-II mRNA was expressed in most adipose-containing tissues. Moreover, the expression of CRABP-I and -II mRNA dramatically increased during the differentiation of adipocytes from bovine intramuscular fibroblast-like cells. The effects of retinoic acid on adipocyte differentiation of bovine intramuscular fibroblast-like cells were concentration-dependent. Retinoic acid activated the formation of lipid droplets at a level of 1 nM, whereas inhibition was observed at a level of $1{\mu}M$. CRABP-I gene was up-regulated and CRABP-II gene down-regulated by retinoic acid during adipocyte differentiation. These results suggest that CRABPs may play an important role in the regulation of intracellular retinoic acid concentrations during adipogenesis.

Keywords

References

  1. Aso, H., H. Abe, I. Nakajima, K. Ozutsumi, T. Yamaguchi, Y. Takamori, A. Kodama, F. B. Hoshino and S. Takano. 1995. A preadipocyte clonal line from bovine intramuscular adipose tissue: nonexpression of Gult-4 protein during adipocyte differentiation. Biochem. Biophys. Res. Commun. 213:369-375. https://doi.org/10.1006/bbrc.1995.2141
  2. Astrom, A., A. Tavakkol, U. Pettersson, M. Cromie, J. T. Elder and J. J. Voorhees. 1991. Molecular cloning of two human cellular retinoic acid-binding proteins (CRABP). Retinoic acid-induced expression of CRABP-II but not CRABP-I in adult human skin in vivo and in skin fibroblasts in vitro. J. Biol. Chem. 266:17662-17666.
  3. Astrom, A., U. Pettersson and J. J. Voorhees. 1992. Structure of the human cellular retinoic acid-binding protein II gene. Early transcriptional regulation by retinoic acid. J. Biol. Chem. 267:25251-25255.
  4. Bastien, J., S. Adam-Stitah, J. L. Plassat, P. Chambon and C. Rochette-Egly. 2002. The phosphorylation site located in the A region of retinoic X receptor alpha is required for the antiproliferative effect of retinoic acid (RA) and the activation of RA target genes in F9 cells. J. Biol. Chem. 277:28683-28689. https://doi.org/10.1074/jbc.M203623200
  5. Bruck, N., J. Bastien, G. Bour, A. Tarrade, J. L. Plassat, A. Bauer, S. Adam-Stitah and C. Rochette-Egly. 2005. Phosphorylation of the retinoid x receptor at the omega loop, modulates the expression of retinoic-acid-target genes with a promoter context specificity. Cell Signal. 17:1229-1239. https://doi.org/10.1016/j.cellsig.2004.12.006
  6. Bucco, R. A., M. H. Melner, D. S. Gordon, S. Leers-Sucheta and D. E. Ong. 1995. Inducible expression of cellular retinoic acid-binding protein II in rat ovary: gonadotropin regulation during luteal development. Endocrinol. 136:2730-2740. https://doi.org/10.1210/en.136.6.2730
  7. Chambon, P. 1996. A decade of molecular biology of retinoic acid receptors. FASEB J. 10:940-954. https://doi.org/10.1096/fasebj.10.9.8801176
  8. Cowherd, R. M., R. E. Lyle and R. E. Jr. McGehee. 1999. Molecular regulation of adipocyte differentiation. Semin. Cell Dev. Biol. 10:3-10.
  9. Dani, C., A. G. Smith, S. Dessolin, P. Leroy, L. Staccini, P. Villageois, C. Darimont and G. Ailhaud. 1997. Differentiation of embryonic stem cells into adipocytes in vitro. J. Cell Sci. 110:1279-1285.
  10. Dong, D., S. E. Ruuska, D. J. Levinthal and N. Noy. 1999. Distinct roles for cellular retinoic acid-binding proteins I and II in regulating signaling by retinoic acid. J. Biol. Chem. 274:23695-23698. https://doi.org/10.1074/jbc.274.34.23695
  11. Giguere, V., S. Lyn, P. Yip, C. H. Siu and S. Amin. 1990. Molecular cloning of cDNA encoding a second cellular retinoic acid-binding protein. Proc. Natl. Acad. Sci. USA. 87:6233-6237. https://doi.org/10.1073/pnas.87.16.6233
  12. Gorocica-Buenfil, M. A., F. L. Fluharty, C. K. Reynolds and S. C. Loerch. 2007a. Effect of dietary vitamin A concentration and roistered soybean inclusion on marbling, adipose cellularity, and fatty acid composition of beef. J. Anim. Sci. 85:2230-2242. https://doi.org/10.2527/jas.2006-780
  13. Gorocica-Buenfil, M. A., F. L. Fluharty, C. K. Reynolds and S. C. Loerch. 2007b. Effect of dietary vitamin A restriction on marbling and conjugated linoleic acid content in Holstein steers. J. Anim. Sci. 85:2243-2255. https://doi.org/10.2527/jas.2006-781
  14. Gorocica-Buenfil, M. A., F. L. Fluharty, T. Bohn, S. J. Schwartz and S. C. Loerch. 2007c. Effect of low vitamin A diets with high-moisture or dry corn on marbling and adipose tissue fatty acid composition of beef steers. J. Anim. Sci. 85:3355-3366. https://doi.org/10.2527/jas.2007-0172
  15. Haq, R. and F. Chytil. 1991. Expression of nuclear retinoic acid receptors in rat adipose tissue. Biochem. Biophys. Res. Commun. 176:1539-1544. https://doi.org/10.1016/0006-291X(91)90462-G
  16. Kamei, Y., T. Kawada, R. Kazuki and E. Sugimoto. 1993. Retinoic acid receptor gamma 2 gene expression is up-regulated by retinoic acid in 3T3-L1 preadipocytes. Biochem. J. 293:807-812. https://doi.org/10.1042/bj2930807
  17. Kamei, Y., T. Kawada, J. Mizukami and E. Sugimoto. 1994. The prevention of adipose differentiation of 3T3-L1 cells caused by retinoic acid is elicited through retinoic acid receptor alpha. Life Sci. 55:307-312.
  18. Kawada, T., N. Aoki, Y. Kamei, K. Maeshige, S. Nishiu and E. Sugimoto. 1990. Comparative investigation of vitamins and their analogues on terminal differentiation, from preadipocytes to adipocytes, of 3T3-L1 cells. Comp. Biochem. Physiol. 96:323-326. https://doi.org/10.1016/0300-9629(90)90699-S
  19. Lee, H. J., S. C. Lee, Y. K. Oh and In K. Han. 2000. Effects of vitamins on the differentiation of preadipocytes from Hanwoo cattle adipose tissues. Asian-Aust. J. Anim. Sci. 13:446-450. https://doi.org/10.5713/ajas.2000.446
  20. Li, E. and A. W. Norris. 1996. Structure/function of cytoplasmic vitamin A-binding proteins. Annu. Rev. Nutr. 16:205-234. https://doi.org/10.1146/annurev.nu.16.070196.001225
  21. Means, A. L., J. R. Thompson and L. J. Gudas. 2000. Transcriptional regulation of the cellular retinoic acid binding protein I gene in F9 teratocarcinoma cells. Cell Growth Differ. 11:71-82.
  22. Miano, J. M. and B. C. Berk. 2000. Retinoids: versatile biological response modifiers of vascular smooth muscle phenotype. Circ. Res. 87:355-362. https://doi.org/10.1161/01.RES.87.5.355
  23. Napoli, J. L. 1996. Retinoic acid biosynthesis and metabolism. FASEB J. 10:993-1001. https://doi.org/10.1096/fasebj.10.9.8801182
  24. Ohyama, M., K. Matsuda, S, Torii, T. Matsui, H. Yano, T. Kawada and T. Ishihara. 1998. The interation between vitamin A and thiazolidinedione on bovine adipocyte differentiation in primary culture. J. Anim. Sci. 76:61-65. https://doi.org/10.2527/1998.76161x
  25. Oka, A., Y. Maruo, T. Miki, T. Yamasaki and T. Saito. 1998. Influence of vitamin A on the quality of beef from the Tajima strain of Japanase black cattle. Meat Sci. 48:150-167
  26. Okuno, M., E. Arimoto, M. Nishizuka, T. Nishihara and M. Imagawa. 2002. Isolation of up- or down-regulated genes in $PPAR{\gamma}$-expressing NIH-3T3 cells during differentiation into adipocytes. FEBS Lett. 519:108-112. https://doi.org/10.1016/S0014-5793(02)02720-5
  27. Ong, D. E., M. E. Newcomer and F. Chytil. 1993. The retinoids, Vol. 2. Academic Press, New York. pp. 283-318.
  28. Safonova, I., C. Darimont, E. Z. Amri, P. Grimaldi, G. Ailhaud, U. Reichert and B. Shroot. 1994. Retinoids are positive effectors of adipose cell differentiation. Mol. Cell Endocrinol. 104:201-211. https://doi.org/10.1016/0303-7207(94)90123-6
  29. Suryawan, A. and C. Y. Hu. 1997. Effect of retinoic acid on differentiation of cultured pig preadipocytes. J. Anim. Sci. 75:112-117. https://doi.org/10.2527/1997.751112x
  30. Tontonoz, P., R. A. Graves, A. I. Budavari, H. Erdjument-Bromage, M. Lui, E. Hu, P. Tempst and B. M. Spiegelman. 1994. Adipocyte-specific transcription factor ARF6 is a heterodimeric complex of two nuclear hormone receptors, $PPAR{\gamma}$ and $RXR{\alpha}$. Nucleic. Acids Res. 22:5628-5634. https://doi.org/10.1093/nar/22.25.5628
  31. Tontonoz, P., S. Singer, B. M. Forman, P. Sarraf, J. A. Fletcher, C. D. Fletcher, R. P. Brun, E. Mueller, S. Altiok, H. Oppenheim, R. M. Evans and B. M. Spiegelman. 1997. Terminal differentiation of human liposarcoma cells induced by ligands for peroxisome proliferator-activated receptor gamma and the retinoid X receptor. Proc. Natl. Acad. Sci. USA. 94:237-241. https://doi.org/10.1073/pnas.94.1.237
  32. Wardlaw, S. A., R. A. Bucco, W. L. Zheng and D. E. Ong. 1997. Variable expression of cellular retinol-and cellular retinoic acid-binding proteins in the rat uterus and ovary during the estrous cycle. Biol. Reprod. 56:125-132. https://doi.org/10.1095/biolreprod56.1.125
  33. Xue, J. C., E. J. Schwarz, A. Chawla and M. A. Lazar. 1996. Distinct stages in adipogenesis revealed by retinoid inhibition of differentiation after induction of $PPAR{\gamma}$. Mol. Cell Biol. 16:1567-1575. https://doi.org/10.1128/MCB.16.4.1567
  34. Zheng, W. L. and D. E. Ong. 1998. Spatial and temporal patterns of expression of cellular retinol-binding protein and cellular retinoic acid-binding proteins in rat uterus during early pregnancy. Biol. Reprod. 58:963-970. https://doi.org/10.1095/biolreprod58.4.963

Cited by

  1. ‐Retinoic Acid Below Cytotoxic Levels Promotes Adipogenesis in 3T3‐L1 Cells pp.1558-9307, 2019, https://doi.org/10.1002/lipd.12123
  2. Effect of Nicotinamide on Proliferation, Differentiation, and Energy Metabolism in Bovine Preadipocytes vol.22, pp.9, 2008, https://doi.org/10.5713/ajas.2009.90091
  3. Identification of Differentially Expressed Genes Between Preadipocytes and Adipocytes Using Affymetrix Bovine Genome Array vol.51, pp.6, 2008, https://doi.org/10.5187/jast.2009.51.6.443
  4. Differential retention of duplicated retinoid-binding protein (crabp & rbp) genes in the rainbow trout genome after two whole genome duplications and their responses to dietary canola oil vol.549, pp.None, 2008, https://doi.org/10.1016/j.aquaculture.2021.737779