Tissue-Selective, Bidirectional Regulation of PEX11α and Perilipin Genes through a Common Peroxisome Proliferator Response Element

Molecular and Cellular Biology

Volumn 24, Issue 3, 2004, Pages 1313-1323

  Shimizu, Makoto ^a   Takeshita, Ayumi ^a   Tsukamoto, Toshiro ^a,c   Gonzalez, Frank J ^b   Osumi, Takashi ^a  

^a UNIVERSITY OF HYOGO   (Japan)

^b NATIONAL CANCER INSTITUTE   (United States)

^c UTSUNOMIYA UNIVERSITY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

CIS ACTING ELEMENT; PERILIPIN; PEROXISOME PROLIFERATOR; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR ALPHA; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA 2; RETINOID X RECEPTOR ALPHA; UNCLASSIFIED DRUG;

ADIPOCYTE; ANIMAL CELL; ARTICLE; CHROMATIN; DNA RESPONSIVE ELEMENT; GENE; GENE ACTIVATION; GENE CLUSTER; GENE CONTROL; GENE INDUCTION; GENETIC TRANSFECTION; HUMAN; HUMAN CELL; LIVER CELL; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; PEROXISOME; PEROXISOME PROLIFERATOR RESPONSE ELEMENT; PEX11ALPHA GENE; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN EXPRESSION; RECEPTOR UPREGULATION;

ANIMALS; BASE SEQUENCE; CONSERVED SEQUENCE; DIMERIZATION; GENES, REGULATOR; GENES, REPORTER; HUMANS; MEMBRANE PROTEINS; MICE; MOLECULAR SEQUENCE DATA; ORGAN SPECIFICITY; PHOSPHOPROTEINS; RECEPTORS, CYTOPLASMIC AND NUCLEAR; RECEPTORS, RETINOIC ACID; RETINOID X RECEPTORS; TRANSCRIPTION FACTORS; TRANSFECTION;

ANIMALIA;

EID: 1642458359     PISSN: 02707306     EISSN: None     Source Type: Journal    
DOI: 10.1128/MCB.24.3.1313-1323.2004     Document Type: Article

References (77)

1. Abe, I., and Y. Fujiki. 1998. cDNA cloning and characterization of constitutively expressed isoform of the human peroxin Pex11p. Biochem. Biophys. Res. Commun. 252:529-533.
2. Abe, I., K. Okumoto, S. Tamura, and Y. Fujiki. 1998. Clofibrate-inducible, 28-kDa peroxisomal integral membrane protein is encoded by PEX11. FEBS Lett. 431:468-472.
3. Adachi, N., and M. R. Lieber. 2002. Bidirectional gene organization: a common architectural feature of the human genome. Cell 109:807-809.
4. Aldridge, T. C., J. D. Tugwood, and S. Green. 1995. Identification and characterization of DNA elements implicated in the regulation of CYP4A1 transcription. Biochem. J. 306:473-479.
5. Amri, E. Z., F. Bonino, G. Ailhaud, N. A. Abumrad, and P. A. Grimaldi. 1995. Cloning of a protein that mediates transcriptional effects of fatty acids in preadipocytes. Homology to peroxisome proliferator-activated receptors. J. Biol. Chem. 270:2367-2371.
6. Banerji, J., S. Rusconi, and W. Schaffner. 1981. Expression of a beta-globin gene is enhanced by remote SV40 DNA sequences. Cell 27:299-308.
7. Barak, Y., D. Liao, W. He, E. S. Ong, M. C. Nelson, J. M. Olefsky, R. Boland, and R. M. Evans. 2002. Effects of peroxisome proliferator-activated receptor delta on placentation, adiposity, and colorectal cancer. Proc. Natl. Acad. Sci. USA 99:303-308.
8. Berger, J., and D. E. Moller. 2002. The mechanisms of action of PPARs. Annu. Rev. Med. 53:409-435.
9. Blackwood, E. M., and J. T. Kadonaga. 1998. Going the distance: a current view of enhancer action. Science 281:61-63.
10. Braissant, O., F. Foufelle, C. Scotto, M. Dauca, and W. Wahli. 1996. Differential expression of peroxisome proliferator-activated receptors (PPARs): tissue distribution of PPAR-alpha, -beta, and -gamma in the adult rat. Endocrinology 137:354-366.
11. Carter, D., L. Chakalova, C. S. Osborne, Y. F. Dai, and P. Fraser. 2002. Long-range chromatin regulatory interactions in vivo. Nat. Genet. 32:623-626.
12. Chang, C. C., S. South, D. Warren, J. Jones, A. B. Moser, H. W. Moser, and S. J. Gould. 1999. Metabolic control of peroxisome abundance. J. Cell Sci. 112:1579-1590.
13. Clifford, G. M., C. Londos, F. B. Kraemer, R. G. Vernon, and S. J. Yeaman. 2000. Translocation of hormone-sensitive lipase and perilipin upon lipolytic stimulation of rat adipocytes. J. Biol. Chem. 275:5011-5015.
14. Desvergne, B., and W. Wahli. 1999. Peroxisome proliferator-activated receptors: nuclear control of metabolism. Endocr. Rev. 20:649-688.
15. Distel, B., R. Erdmann, S. J. Gould, G. Blobel, D. I. Crane, J. M. Cregg, G. Dodt, Y. Fujiki, J. M. Goodman, W. W. Just, J. A. Kiel, W. H. Kunau, P. B. Lazarow, G. P. Mannaerts, H. W. Moser, T. Osumi, R. A. Rachubinski, A. Roscher, S. Subramani, H. F. Tabak, T. Tsukamoto, D. Valle, I. van der Klei, P. P. van Veldhoven, and M. Veenhuis. 1996. A unified nomenclature for peroxisome biogenesis factors. J. Cell Biol. 135:1-3.
16. Dodgson, J. B., J. Strommer, and J. D. Engel. 1979. Isolation of the chicken beta-globin gene and a linked embryonic beta-like globin gene from a chicken DNA recombinant library. Cell 17:879-887.
17. Dolan, M., B. J. Sugarman, J. B. Dodgson, and J. D. Engel. 1981. Chromosomal arrangement of the chicken beta-type globin genes. Cell 24:669-677.
18. Dreyer, C., G. Krey, H. Keller, F. Givel, G. Helftenbein, and W. Wahli. 1992. Control of the peroxisomal beta-oxidation pathway by a novel family of nuclear hormone receptors. Cell 68:879-887.
19. Erdmann, R., and G. Blobel. 1995. Giant peroxisomes in oleic acid-induced Saccharomyces cerevisiae lacking the peroxisomal membrane protein Pmp27p. J. Cell Biol. 128:509-523.
20. Galetto, R., M. Albajar, J. I. Polanco, M. M. Zakin, and J. C. Rodriguez-Rey. 2001. Identification of a peroxisome-proliferator-activated-receptor response element in the apolipoprotein E gene control region. Biochem. J. 357:521-527.
21. Godbout, R., R. Ingram, and S. M. Tilghman. 1986. Multiple regulatory elements in the intergenic region between the α-fetoprotein and albumin genes. Mol. Cell. Biol. 6:477-487.
22. Greenberg, A. S., J. J. Egan, S. A. Wek, N. B. Garty, E. J. Blanchette-Mackie, and C. Londos. 1991. Perilipin, a major hormonally regulated adipocyte-specific phosphoprotein associated with the periphery of lipid storage droplets. J. Biol. Chem. 266:11341-11346.
23. Helledie, T., L. Grontved, S. S. Jensen, P. Kiilericb, L. Rietveld, T. Albrektsen, M. S. Boysen, J. Nohr, L. K. Larsen, J. Fleckner, H. G. Stunnenberg, K. Kristiansen, and S. Mandrup. 2002. The gene encoding the Acyl-CoA-binding protein is activated by peroxisome proliferator-activated receptor gamma through an intronic response element functionally conserved between humans and rodents. J. Biol. Chem. 277:26821-26830.
24. Hess, R., W. Staubli, and W. Riess. 1965. Nature of the hepatomegatic effect produced by ethyl-chlorophenoxy-isobutyrate in the rat. Nature 208:856-858.
25. Hochheimer, A., and R. Tjian. 2003. Diversified transcription initiation complexes expand promoter selectivity and tissue-specific gene expression. Genes Dev. 17:1309-1320.
26. Hoepfner, D., M. van den Berg, P. Philippsen, H. F. Tabak, and E. H. Hettema. 2001. A role for Vps1p, actin, and the Myo2p motor in peroxisome abundance and inheritance in Saccharomyces cerevisiae. J. Cell Biol. 155: 979-990.
27. Hsu, M. H., U. Savas, K. J. Griffin, and E. F. Johnson. 2001. Identitication of peroxisome proliferator-responsive human genes by elevated expression of the peroxisome proliferator-activated receptor alpha in HepG2 cells. J. Biol. Chem. 276:27950-27958.
28. Ijpenberg, A., E. Jeannin, W. Wahli, and B. Desvergne. 1997. Polarity and specific sequence requirements of peroxisome proliferator-activated receptor (PPAR)/retinoid X receptor heterodimer binding to DNA. A functional analysis of the malic enzyme gene PPAR response clement. J. Biol. Chem. 272:20108-20117.
29. Issemann, I., and S. Green. 1990. Activation of a member of the steroid hormone receptor superfamily by peroxisome proliferators. Nature 347:645-650.
30. Jack, J., D. Dorsett, Y. Delotto, and S. Liu. 1991. Expression of the cut locus in the Drosophila wing margin is required for cell type specification and is regulated by a distant enhancer. Development 113:735-747.
31. Juge-Aubry, C., A. Pernin, T. Favez, A. G. Burger, W. Wahll, C. A. Meier, and B. Desvergne. 1997. DNA binding properties of peroxisome proliferator-activated receptor subtypes on various natural peroxisome proliferator response elements. Importance of the 5′-flanking region. J. Biol. Chem. 272: 25252-25259.
32. Kliewer, S. A., K. Umesono, D. J. Noonan, R. A. Heyman, and R. M. Evans. 1992. Convergence of 9-cis retinoic acid and peroxisome proliferator signalling pathways through heterodimer formation of their receptors. Nature 358:771-774.
33. Koch, A., M. Thiemann, M. Grabenbauer, Y. Yoon, M. A. McNiven, and M. Schrader. 2003. Dynamin-like protein 1 is involved in peroxisomal fission. J. Biol. Chem. 278:8597-8605.
34. Lawrence, J. W., Y. Li, S. Chen, J. G. DeLuca, J. P. Berger, D. R. Umbenhauer, D. E. Moller, and G. Zhou. 2001. Differential gene regulation in human versus rodent hepatocytes by peroxisome proliferator-activated receptor (PPAR) alpha. PPAR alpha fails to induce peroxisome proliferation-associated genes in human cells independently of the level of receptor expresson. J. Biol. Chem. 276:31521-31527.
35. Lazarow, P. B., and Y. Fujiki. 1985. Biogenesis of peroxisomes. Annu. Rev. Cell Biol. 1:489-530.
36. Lee, S. S., T. Pineau, J. Drago, E. J. Lee, J. W. Owens, D. L. Kroetz, P. M. Fernandez-Salguero, H. Westphal, and F. J. Gonzalez. 1995. Targeted disruption of the alpha 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.
37. Li, X., E. Baumgart, G. X. Dong, J. C. Morrell, G. Jimenez-Sanchez, D. Valle, K. D. Smith, and S. J. Gould. 2002. PEX11α is required for peroxisome proliferation in response to 4-phenylbutyrate but is dispensable for peroxisome proliferator-activated receptor alpha-mediated peroxisome proliferation. Mol. Cell. Biol. 22:8226-8240.
38. Li, X., and S. J. Gould. 2003. The dynamin-like GTPase DLP1 is essential for peroxisome division and is recruited to peroxisomes in part by PEX11. J. Biol. Chem. 278:17012-17020.
39. Li, X., and S. J. Gould. 2002. PEX11 promotes peroxisome division independently of peroxisome metabolism. J. Cell Biol. 156:643-651.
40. Lock, E. A., A. M. Mitchell, and C. R. Elcombe. 1989. Biochemical mechanisms of induction of hepatic peroxisome proliferation. Annu. Rev. Pharmacol. Toxicol. 29:145-163.
41. MacGregor, G. R., and C. T. Caskey. 1989. Construction of plasmids that express E. coli beta-galactosidase in mammalian cells. Nucleic Acids Res. 17:2365.
42. Marshall, P. A., Y. I. Krimkevich, R. H. Lark, J. M. Dyer, M. Veenhuis, and J. M. Goodman. 1995. Pmp27 promotes peroxisomal proliferation. J. Cell Biol. 129:345-355.
43. Matsumoto, N., S. Tamura, and Y. Fujiki. 2003. The pathogenic peroxin Pex26p recruits the Pex1p-Pex6p AAA ATPase complexes to peroxisomes. Nat. Cell Biol. 5:454-460.
44. Nickol, J. M., and G. Felsenfeld. 1988. Bidirectional control of the chicken beta- and epsilon-globin genes by a shared enhancer. Proc. Natl. Acad. Sci. USA 85:2548-2552.
45. Nicolas-Frances, V., V. K. Dasari, E. Abruzzi, T. Osumi, and N. Latruffe. 2000. The peroxisome proliferator response element (PPRE) present at positions-681/-669 in the rat liver 3-ketoacyl-CoA thiolase B gene functionally interacts differently with PPARalpha and HNF-4. Biochem. Biophys. Res. Commun. 269:347-351.
46. Osada, S., T. Tsukamoto, M. Takiguchi, M. Mori, and T. Osumi. 1997. Identification of an extended half-site motif required for the function of peroxisome proliferator-activated receptor alpha. Genes Cells 2:315-327.
47. Osumi, T., J. K. Wen, and T. Hashimoto. 1991. Two cis-acting regulatory sequences in the peroxisome proliferator-responsive enhancer region of rat acyl-CoA oxidase gene. Biochem. Biophys. Res. Commun. 175:866-871.
48. Osumi, T., S. Yokota, and T. Hashimoto. 1990. Proliferation of peroxisomes and induction of peroxisomal beta-oxidation enzymes in rat hepatoma H4IIEC3 by ciprofibrate. J. Biochem. (Tokyo) 108:614-621.
49. Palmer, C. N., M. H. Hsu, H. J. Griffin, and E. F. Johnson. 1995. Novel sequence determinants in peroxisome proliferator signaling. J. Biol. Chem. 270:16114-16121.
50. Passreiter, M., M. Anton, D. Lay, R. Frank, C. Harter, F. T. Wieland, K. Gorgas, and W. W. Just. 1998. Peroxisome biogenesis: involvement of ARF and coatomer. J. Cell Biol. 141:373-383.
51. Peters, J. M., S. S. Lee, W. Li, J. M. Ward, O. Gavrilova, C. Everett, M. L. Reitman, L. D. Hudson, and F. J. Gonzalez. 2000. Growth, adipose, brain, and skin alterations resulting from targeted disruption of the mouse peroxisome proliferator-activated receptor β(δ). Mol. Cell. Biol. 20:5119-5128.
52. Poll-The, B. T., F. Roels, H. Ogier, J. Scotto, J. Vamecq, R. B. Schutgens, R. J. Wanders, C. W. van Roermund, M. J. van Wijland, A. W. Schram, et al. 1988. A new peroxisomal disorder with enlarged peroxisomes and a specific deficiency of acyl-CoA oxidase (pseudo-neonatal adrenoleukodystrophy). Am. J. Hum. Genet. 42:422-434.
53. Purdue, P. E., and P. B. Lazarow. 2001. Peroxisome biogenesis. Annu. Rev. Cell Dev. Biol. 17:701-752.
54. Qi, C., Y. Zhu, J. Pan, N. Usuda, N. Maeda, A. V. Yeldandi, M. S. Rao, T. Hashimoto, and J. K. Reddy. 1999. Absence of spontaneous peroxisome proliferation in enoyl-CoA hydratase/L-3-hydroxyacyl-CoA dehydrogenase-deficient mouse liver. Further support for the role of fatty acyl CoA oxidase in PPARα ligand metabolism. J. Biol. Chem. 274:15775-15780.
55. Reddy, J. K., and T. Hashimoto. 2001. Peroxisomal beta-oxidation and peroxisome prolilerator-activated receptor alpha: an adaptive metabolic system. Annu. Rev. Nutr. 21:193-230.
56. Rosenbaum, S. E., and A. S. Greenberg. 1998. The short- and long-term effects of tumor necrosis factor-alpha and BRL 49653 on peroxisome proliferator-activated receptor (PPAR)gamma2 gene expression and other adipocyte genes. Mol. Endocrinol. 12:1150-1160.
57. Rubin, C. S., A. Hirsch, C. Fung, and O. M. Rosen. 1978. Development of hormone receptors and hormonal responsiveness in vitro. Insulin receptors and insulin sensitivity in the preadipocyte and adipocyte forms of 3T3-LI cells. J. Biol. Chem. 253:7570-7578.
58. Sakai, Y., P. A. Marshall, A. Saiganji, K. Takabe, H. Saiki, N. Kato, and J. M. Goodman. 1995. The Candida boidinii peroxisomal membrane protein Pmp30 has a role in peroxisomal proliferation and is functionally homologous to Pmp27 from Saccharomyces cerevisiae. J. Bacteriol. 177:6773-6781.
59. Sambrook, J., E. F. Fritsch, and T. Maniatis. 1989. Molecular cloning: a laboratory manual, p. 16.32-16.36. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, N.Y.
60. Schoonjans, K., J. Peinado-Onsurbe, A. M. Lefehvre, R. A. Heyman, M. Briggs, S. Deeb, B. Staels, and J. Auwerx. 1996. PPARalpha and PPAR-gamma activators direct a distinct tissue-specific transcriptional response via a PPRE in the lipoprotein lipase gene. EMBO J. 15:5336-5348.
61. Schrader, M., B. E. Reuher, J. C. Morrell, G. Jimenez-Sanchez, C. Ohie, T. A. Stroh, D. Valle, T. A. Schroer, and S. J. Gould. 1998. Expression of PEX11beta mediates peroxisome proliferation in the absence of extracellular stimuli. J. Biol. Chem. 273:29607-29614.
62. Servetnick, D. A., D. L. Brasaemle, J. Gruia-Gray, A. R. Kimmel, J. Wolff, and C. Londos. 1995. Perilipins are associated with cholesteryl ester droplets in steroidogenic adrenal cortical and Leydig cells. J. Biol. Chem. 270:16970-16973.
63. Smith, J. J., M. Marelli, R. H. Christmas, F. J. Vizeacoumar, D. J. Dilworth, T. Ideker, T. Galitski, K. Dimitrov, R. A. Rachubinski, and J. D. Aitchison. 2002. Transcriptome profiling to identify genes involved in peroxisome assembly and function. J. Cell Biol. 158:259-271.
64. Tam, Y. Y., and R. A. Rachubinski. 2002. Yarrowia lipolytica cells mutant for the PEX24 gene encoding a peroxisomal membrane peroxin mislocalize peroxisomal proteins and accumulate membrane structures containing both peroxisomal matrix and membrane proteins. Mol. Biol. Cell 13:2681-2691.
65. Tanaka, A., K. Okumoto, and Y. Fujiki. 2003. cDNA cloning and characterization of the third isoform of human peroxin Pcx11p. Biochem. Biophys. Res. Commun. 300:819-823.
66. Titorenko, V. I., and R. A. Rachuhinski. 2001. The life cycle of the peroxisome. Nat. Rev. Mol. Cell Biol. 2:357-368.
67. Tolhuis, B., R. J. Palstra, E. Splinter, F. Grosveld, and W. de Laat. 2002. Looping and interaction between hypersensitive sites in the active beta-globin locus. Mol. Cell 10:1453-1465.
68. Tominaga, S., M. Morikawa, and T. Osumi. 2002. Growth hormone has dual stage-specific effects on the differentiation of 3T3-LI preadipocytes. J. Biochem. (Tokyo) 132:881-889.
69. Tontonoz, P., E. Hu, J. Devine, E. C. Beale, and B. M. Spiegelman. 1995. PPARγ2 regulates adipose expression of the phosphoenolpyruvate carboxylkinase gene. Mol. Cell. Biol. 15:351-357.
70. Tontonoz, P., E. Hu, R. A. Graves, A. I. Budavari, and B. M. Spiegelman. 1994. mPPAR gamma 2: tissue-specific regulator of an adipocyte enhancer. Genes Dev. 8:1224-1234.
71. Tontonoz, P., E. Hu, and B. M. Spiegelman. 1994. Stimulation of adipogenesis in fibroblasts by PPAR gamma 2, a lipid-activated transcription factor. Cell 79:1147-11456.
72. Tugwood, J. D., I. Issemann, R. G. Anderson, K. R. Bundell, W. L. McPheat, and S. Green. 1992. The mouse peroxisome proliferator activated receptor recognizes a response element in the 5′ flanking sequence of the rat acyl CoA oxidase gene. EMBO J. 11:433-439.
73. van Roermund, C. W., H. F. Tahak, M. van Den Berg, R. J. Wanders, and E. H. Hettema. 2000. Pex11p plays a primary role in medium-chain fatty acid oxidation, a process that affects peroxisome number and size in Sacchammyces cerevisiae. J. Cell Biol. 150:489-498.
74. Wang, Y. X., C. H. Lee, S. Tiep, R. T. Yu, J. Ham, H. Kang, and R. M. Evans. 2003. Peroxisome-proliferator-activated receptor delta activates fat metabolism to prevent obesity. Cell 113:159-170.
75. Winoto, A., and D. Baltimore. 1989. A novel, inducible and T cell-specific enhancer located at the 3′ end of the T cell receptor alpha locus. EMBO J. 8:729-733.
76. Zhang, B., S. L. Marcus, F. G. Sajjadi, K. Alvares, J. K. Reddy, S. Subramani, R. A. Rachubinski, and J. P. Capone. 1992. Identification of a peroxisome proliferator-responsive element upstream of the gene encoding rat peroxisomal enoyl-CoA hydratase/3-hydroxyacyl-CoA dehydrogenase. Proc. Natl. Acad. Sci. USA 89:7541-7545.
77. Zhu, Y., C. Qi, J. R. Korenberg, X. N. Chen, D. Noya, M. S. Rao, and J. K. Reddy. 1995. Structural organization of mouse peroxisome proliferator-activated receptor gamma (mPPAR gamma) gene: alternative promoter use and different splicing yield two mPPAR gamma isoforms. Proc. Natl. Acad. Sci. USA 92:7921-7925.