Peroxisome proliferator-activated receptor α mediates enhancement of gene expression of cerebroside sulfotransferase in several murine organs

Glycoconjugate Journal

Volumn 30, Issue 6, 2013, Pages 553-560

  Nakajima, Takero ^a   Kamijo, Yuji ^a,b   Yuzhe, Huang ^a,c   Kimura, Takefumi ^a,b   Tanaka, Naoki ^a   Sugiyama, Eiko ^a,d   Nakamura, Kozo ^e   Kyogashima, Mamoru ^f   Hara, Atsushi ^a   Aoyama, Toshifumi ^a  

^a SHINSHU UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

^b SHINSHU UNIVERSITY SCHOOL OF MEDICINE   (Japan)

^c HEBEI MEDICAL UNIVERSITY   (China)

^d Nagano Prefectural College   (Japan)

^e SHINSHU UNIVERSITY   (Japan)

^f NIHON PHARMACEUTICAL UNIVERSITY   (Japan)

Author keywords

CST; Fenofibrate; PPAR ; Sphingoglycolipid; Sulfoglycolipid

Indexed keywords

ARYLSULFATASE; CEREBROSIDE SULFOTRANSFERASE; FENOFIBRATE; MESSENGER RNA; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR ALPHA; SULFATIDE; SULFOTRANSFERASE; UNCLASSIFIED DRUG; GALACTOSYLCERAMIDE SULFOTRANSFERASE;

AMINO ACID SEQUENCE; ANIMAL TISSUE; ARTICLE; BRAIN TISSUE; CATALYSIS; COLON; CONTROLLED STUDY; CST GENE; GENE; GENE CONTROL; GENE EXPRESSION; GENE LOCATION; HEART; KIDNEY PARENCHYMA; LIPOGENESIS; LIVER; MALE; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN DNA BINDING; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; PROTEIN TARGETING; SMALL INTESTINE; TISSUE SECTION; WILD TYPE; AGONISTS; ANIMAL; ANTIBODY SPECIFICITY; BRAIN; GENETIC TRANSCRIPTION; GENETICS; HEART MUSCLE; INTESTINE; KIDNEY; KNOCKOUT MOUSE; METABOLISM;

MAMMALIA; MURINAE; MUS;

ANIMALS; BRAIN; FENOFIBRATE; INTESTINES; KIDNEY; LIVER; MICE; MICE, KNOCKOUT; MYOCARDIUM; ORGAN SPECIFICITY; PPAR ALPHA; RNA, MESSENGER; SULFOGLYCOSPHINGOLIPIDS; SULFOTRANSFERASES; TRANSCRIPTION, GENETIC;

EID: 84880924974     PISSN: 02820080     EISSN: 15734986     Source Type: Journal    
DOI: 10.1007/s10719-012-9454-6     Document Type: Article

References (53)

1. Ishizuka, I.: Chemistry and functional distribution of sulfoglycolipids. Prog. Lipid Res. 36, 245-319 (1997)
2. Takahashi, T., Suzuki, T.: Role of sulfatide in normal and pathological cells and tissues. J. Lipid Res. 53, 1437-1450 (2012)
3. Honke, K., Hirahara, Y., Dupree, J., Suzuki, K., Popko, B., Fukushima, K., Fukushima, J., Nagasawa, T., Yoshida, N., Wada, Y., Taniguchi, N.: Paranodal junction formation and spermatogenesis require sulfoglycolipids. Proc. Natl. Acad. Sci. U. S. A. 99, 4227-4232 (2002)
4. Zhang, X., Nakajima, T., Kamijo, Y., Li, G., Hu, R., Kannagi, R., Kyogashima, M., Aoyama, T., Hara, A.: Acute kidney injury induced by protein-overload nephropathy down-regulates gene expression of hepatic cerebroside sulfotransferase in mice, resulting in reduction of liver and serum sulfatides. Biochem. Biophys. Res. Commun. 390, 1382-1388 (2009)
5. Sheng, X., Nakajima, T., Wang, L., Zhang, X., Kamijo, Y., Takahashi, K., Tanaka, N., Sugiyama, E., Kyogashima, M., Aoyama, T., Hara, A.: Attenuation of kidney injuries maintains serum sulfatide levels dependent on hepatic synthetic ability: a possible involvement of oxidative stress. Tohoku J. Exp. Med. 227, 1-12 (2012)
6. Hirahara, Y., Tsuda, M., Wada, Y., Honke, K.: cDNA cloning, genomic cloning, and tissue-specific regulation of mouse cerebroside sulfotransferase. Eur. J. Biochem. 267, 1909-1916 (2000)
7. Podvinec, M., Kaufmann, M.R., Handschin, C., Meyer, U.A.: NUBIScan, an in silico approach for prediction of nuclear receptor response elements. Mol. Endocrinol. 16, 1269-1279 (2002)
8. Kimura, T., Nakajima, T., Kamijo, Y., Tanaka, N., Wang, L., Hara, A., Sugiyama, E., Tanaka, E., Gonzalez, F.J., Aoyama, T.: Hepatic cerebroside sulfotransferase is induced by PPARα activation in mice. PPAR Res. 2012, 174932 (2012)
9. Lee, S.S., Pineau, T., Drago, J., Lee, E.J., Owens, J.W., Kroetz, D.L., Fernandez-Salguero, P.M., Westphal, H., Gonzalez, F.J.: Targeted disruption of the α isoform of the peroxisome proliferator-activated receptor gene in mice results in abolishment of the pleiotropic effects of peroxisome proliferators. Mol. Cell. Biol. 15, 3012-3022 (1995)
10. Akiyama, T.E., Nicol, C.J., Fievet, C., Staels, B., Ward, J.M., Auwerx, J., Lee, S.S., Gonzalez, F.J., Peters, J.M.: Peroxisome proliferator-activated receptor-α regulates lipid homeostasis, but is not associated with obesity. J. Biol. Chem. 276, 39088-39093 (2001)
11. Aoyama, T., Peters, J.M., Iritani, N., Nakajima, T., Furihata, K., Hashimoto, T., Gonzalez, F.J.: Altered constitutive expression of fatty acid-metabolizing enzymes in mice lacking the peroxisome proliferator-activated receptor α (PPARα). J. Biol. Chem. 273, 5678-5684 (1998)
12. Takahashi, K., Kamijo, Y., Hora, K., Hashimoto, K., Higuchi, M., Nakajima, T., Ehara, T., Shigematsu, H., Gonzalez, F.J., Aoyama, T.: Pretreatment by low-dose fibrates protects against acute free fatty acid-induced renal tubule toxicity by counteracting PPARα deterioration. Toxicol. Appl. Pharmacol. 252, 237-249 (2011)
13. Hashimoto, K., Kamijo, Y., Nakajima, T., Harada, M., Higuchi, M., Ehara, T., Shigematsu, H., Aoyama, T.: PPARα activation protects against anti-Thy1 nephritis by suppressing glomerular NF-κB signaling. PPAR Res. 2012, 976089 (2012)
14. Nakajima, T., Tanaka, N., Kanbe, H., Hara, A., Kamijo, Y., Zhang, X., Gonzalez, F.J., Aoyama, T.: Bezafibrate at clinically relevant doses decreases serum/liver triglycerides via down-regulation of sterol regulatory element-binding protein-1c in mice: a novel peroxisome proliferator-activated receptor α-independent mechanism. Mol. Pharmacol. 75, 782-792 (2009)
15. Nakajima, T., Tanaka, N., Li, G., Hu, R., Kamijo, Y., Hara, A., Aoyama, T.: Effect of bezafibrate on hepatic oxidative stress: comparison between conventional experimental doses and clinically-relevant doses in mice. Redox Rep. 15, 123-130 (2010)
16. Hara, A., Radin, N.S.: Lipid extraction of tissues with a low-toxicity solvent. Anal. Biochem. 90, 420-426 (1978)
17. Li, G., Hu, R., Kamijo, Y., Nakajima, T., Aoyama, T., Inoue, T., Node, K., Kannagi, R., Kyogashima, M., Hara, A.: Establishment of a quantitative, qualitative, and high-throughput analysis of sulfatides from small amounts of sera by matrix-assisted laser desorption ionization-time of flight mass spectrometry. Anal. Biochem. 362, 1-7 (2007)
18. Aoyama, T., Yamano, S., Waxman, D.J., Lapenson, D.P., Meyer, U.A., Fischer, V., Tyndale, R., Inaba, T., Kalow, W., Gelboin, H.V.: Cytochrome P-450 hPCN3, a novel cytochrome P-450 IIIA gene product that is differentially expressed in adult human liver. cDNA and deduced amino acid sequence and distinct specificities of cDNA-expressed hPCN1 and hPCN3 for the metabolism of steroid hormones and cyclosporine. J. Biol. Chem. 264, 10388-10395 (1989)
19. Aoyama, T., Uchida, Y., Kelley, R.I., Marble, M., Hofman, K., Tonsgard, J.H., Rhead, W.J., Hashimoto, T.: A novel disease with deficiency of mitochondrial very-long-chain acyl-CoA dehydrogenase. Biochem. Biophys. Res. Commun. 191, 1369-1372 (1993)
20. Aoyama, T., Ueno, I., Kamijo, T., Hashimoto, T.: Rat very-long-chain acyl-CoA dehydrogenase, a novel mitochondrial acyl-CoA dehydrogenase gene product, is a rate-limiting enzyme in long-chain fatty acid β-oxidation system. cDNA and deduced amino acid sequence and distinct specificities of the cDNA-expressed protein. J. Biol. Chem. 269, 19088-19094 (1994)
21. Desvergne, B., Wahli, W.: Peroxisome proliferator-activated receptors: nuclear control of metabolism. Endocr. Rev. 20, 649-688 (1999)
22. Braissant, O., Foufelle, F., Scotto, C., Dauça, M., Wahli, W.: Differential expression of peroxisome proliferator-activated receptors (PPARs): tissue distribution of PPAR-α, -β, and -γ in the adult rat. Endocrinology 137, 354-366 (1996)
23. Rakhshandehroo, M., Knoch, B., Müller, M., Kersten, S.: Peroxisome proliferator-activated receptor alpha target genes. PPAR Res. 2010, 612089 (2010)
24. Honke, K., Zhang, Y., Cheng, X., Kotani, N., Taniguchi, N.: Biological roles of sulfoglycolipids and pathophysiology of their deficiency. Glycoconj. J. 21, 59-62 (2004)
25. Bosio, A., Binczek, E., Stoffel, W.: Functional breakdown of the lipid bilayer of the myelin membrane in central and peripheral nervous system by disrupted galactocerebroside synthesis. Proc. Natl. Acad. Sci. U. S. A. 93, 13280-13285 (1996)
26. Schoonjans, K., Peinado-Onsurbe, J., Lefebvre, A.M., Heyman, R.A., Briggs, M., Deeb, S., Staels, B., Auwerx, J.: PPARα and PPARγ activators direct a distinct tissue-specific transcriptional response via a PPRE in the lipoprotein lipase gene. EMBO J. 15, 5336-5348 (1996)
27. Martin, G., Schoonjans, K., Lefebvre, A.M., Staels, B., Auwerx, J.: Coordinate regulation of the expression of the fatty acid transport protein and acyl-CoA synthetase genes by PPARα and PPARγ activators. J. Biol. Chem. 272, 28210-28217 (1997)
28. Motojima, K., Passilly, P., Peters, J.M., Gonzalez, F.J., Latruffe, N.: Expression of putative fatty acid transporter genes are regulated by peroxisome proliferator-activated receptor α and γ activators in a tissue- and inducer-specific manner. J. Biol. Chem. 273, 16710-16714 (1998)
29. Schinkel, A.H., Smit, J.J., van Tellingen, O., Beijnen, J.H., Wagenaar, E., van Deemter, L., Mol, C.A., van der Valk, M.A., Robanus-Maandag, E.C., te Riele, H.P., Berns, A.J., Borst, P.: Disruption of the mouse mdr1a P-glycoprotein gene leads to a deficiency in the blood-brain barrier and to increased sensitivity to drugs. Cell 77, 491-502 (1994)
30. Berger, J., Albet, S., Bentejac, M., Netik, A., Holzinger, A., Roscher, A.A., Bugaut, M., Forss-Petter, S.: The four murine peroxisomal ABC-transporter genes differ in constitutive, inducible and developmental expression. Eur. J. Biochem. 265, 719-727 (1999)
31. Mogi, M., Abe, S., Hayashi, T., Tsutsumi, S.: Studies on the metabolic fate of fenofibrate (1). Absorption, distribution and excretion after the single and repeated administration to rats. Jpn. Pharmacol. Ther. 23, S1117-S1133 (1995)
32. Breimer, M.E., Hansson, G.C., Karlsson, K.A., Leffler, H.: The preparative separation of sialic acid-containing lipids from sulphate group-containing glycolipids from small intestine of different animals. Analysis by thin-layer chromatography and detection of novel species. J. Biochem. 93, 1473-1485 (1983)
33. 3- sulfogangliotetraosylceramide, demonstrated by negative ion fast atom bombardment mass spectrometry. J. Biol. Chem. 261, 1440-1444 (1986)
34. Li, G., Hu, R., Kamijo, Y., Nakajima, T., Aoyama, T., Ehara, T., Shigematsu, H., Kannagi, R., Kyogashima, M., Hara, A.: Kidney dysfunction induced by protein overload nephropathy reduces serum sulfatide levels in mice. Nephrology 14, 658-662 (2009)
35. Coles, L., Hay, J.B., Gray, G.M.: Factors affecting the glycosphingolipid composition of murine tissues. J. Lipid Res. 11, 158-163 (1970)
36. Farwanah, H., Kolter, T.: Lipidomics of glycosphingolipids. Metabolites 2, 134-164 (2012)
37. Honke, K., Yamane, M., Ishii, A., Kobayashi, T., Makita, A.: Purification and characterization of 3′-phosphoadenosine-5′-phosphosulfate: GalCer sulfotransferase from human renal cancer cells. J. Biochem. 119, 421-427 (1996)
38. Watanabe, K., Fujii, H., Takahashi, T., Kodama, M., Aizawa, Y., Ohta, Y., Ono, T., Hasegawa, G., Naito, M., Nakajima, T., Kamijo, Y., Gonzalez, F.J., Aoyama, T.: Constitutive regulation of cardiac fatty acid metabolism through peroxisome proliferator-activated receptor α associated with age-dependent cardiac toxicity. J. Biol. Chem. 275, 22293-22299 (2000)
39. Kamijo, Y., Hora, K., Tanaka, N., Usuda, N., Kiyosawa, K., Nakajima, T., Gonzalez, F.J., Aoyama, T.: Identification of functions of peroxisome proliferator-activated receptor α in proximal tubules. J. Am. Soc. Nephrol. 13, 1691-1702 (2002)
40. Nakajima, T., Kamijo, Y., Tanaka, N., Sugiyama, E., Tanaka, E., Kiyosawa, K., Fukushima, Y., Peters, J.M., Gonzalez, F.J., Aoyama, T.: Peroxisome proliferator-activated receptor α protects against alcohol-induced liver damage. Hepatology 40, 972-980 (2004)
41. Kamijo, Y., Hora, K., Nakajima, T., Kono, K., Takahashi, K., Ito, Y., Higuchi, M., Kiyosawa, K., Shigematsu, H., Gonzalez, F.J., Aoyama, T.: Peroxisome proliferator-activated receptor α protects against glomerulonephritis induced by long-term exposure to the plasticizer di-(2-ethylhexyl)phthalate. J. Am. Soc. Nephrol. 18, 176-188 (2007)
42. Kamijo, Y., Hora, K., Kono, K., Takahashi, K., Higuchi, M., Ehara, T., Kiyosawa, K., Shigematsu, H., Gonzalez, F.J., Aoyama, T.: PPARα protects proximal tubular cells from acute fatty acid toxicity. J. Am. Soc. Nephrol. 18, 3089-3100 (2007)
43. Tanaka, N., Moriya, K., Kiyosawa, K., Koike, K., Gonzalez, F.J., Aoyama, T.: PPARα activation is essential for HCV core protein-induced hepatic steatosis and hepatocellular carcinoma in mice. J. Clin. Invest. 118, 683-694 (2008)
44. Bikman, B.T., Summers, S.A.: Ceramides as modulators of cellular and whole-body metabolism. J. Clin. Invest. 121, 4222-4230 (2011)
45. Rivier, M., Castiel, I., Safonova, I., Ailhaud, G., Michel, S.: Peroxisome proliferator-activated receptor-α enhances lipid metabolism in a skin equivalent model. J. Invest. Dermatol. 114, 681-687 (2000)
46. Hanada, K.: Serine palmitoyltransferase, a key enzyme of sphingolipid metabolism. Biochim. Biophys. Acta 1632, 16-30 (2003)
47. Hara, A., Kutsukake, Y., Uemura, K.I., Taketomi, T.: Anticoagulant activity of sulfatide and its anti-thrombotic effect in rabbit. J. Biochem. 113, 781-785 (1993)
48. Hara, A., Uemura, K., Taketomi, T.: Sulfatide prolongs blood-coagulation time and bleeding time by forming a complex with fibrinogen. Glycoconj. J. 13, 187-194 (1996)
49. Kyogashima, M., Sakai, T., Onaya, J., Hara, A.: Roles of galactose and sulfate residues in sulfatides for their antagonistic functions in the blood coagulation system. Glycoconj. J. 18, 245-251 (2001)
50. Hara, A., Taketomi, T.: Occurrence of sulfatide as a major glycosphingolipid in WHHL rabbit serum lipoproteins. J. Biochem. 102, 83-92 (1987)
51. Hu, R., Li, G., Kamijo, Y., Aoyama, T., Nakajima, T., Inoue, T., Node, K., Kannagi, R., Kyogashima, M., Hara, A.: Serum sulfatides as a novel biomarker for cardiovascular disease in patients with end-stage renal failure. Glycoconj. J. 24, 565-571 (2007)
52. Wang, L., Kamijo, Y., Matsumoto, A., Nakajima, T., Higuchi, M., Kannagi, R., Kyogashima, M., Aoyama, T., Hara, A.: Kidney transplantation recovers the reduction level of serum sulfatide in ESRD patients via processes correlated to oxidative stress and platelet count. Glycoconj. J. 28, 125-135 (2011)
53. Kamijo, Y., Wang, L., Matsumoto, A., Nakajima, T., Hashimoto, K., Higuchi, M., Kyogashima, M., Aoyama, T., Hara, A.: Long-term improvement of oxidative stress via kidney transplantation ameliorates serum sulfatide levels. Clin. Exp. Nephrol. (in press)