Carbonic anhydrase III regulates peroxisome proliferator-activated receptor-γ2

Experimental Cell Research

Volumn 318, Issue 8, 2012, Pages 877-886

  Mitterberger, Maria C ^a   Kim, Geumsoo ^b   Rostek, Ursula ^a   Levine, Rodney L ^b   Zwerschke, Werner ^a  

^a ERICH SCHMID INSTITUTE OF MATERIALS SCIENCE   (Austria)

^b NATIONAL HEART LUNG AND BLOOD INSTITUTE   (United States)

Author keywords

Adipocyte; Adipogenesis; Aging; Caloric restriction; Carbonic anhydrase III; FABP4; Oxidative stress; PPAR 2; Preadipocyte

Indexed keywords

CARBONATE DEHYDRATASE III; CCAAT ENHANCER BINDING PROTEIN ALPHA; FATTY ACID BINDING PROTEIN 4; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA 2; TRIACYLGLYCEROL;

ADIPOGENESIS; ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; CELL STRAIN 3T3; CONTROLLED STUDY; DOWN REGULATION; EMBRYO CELL; FIBROBLAST; GENE EXPRESSION; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROADIPOCYTE; RNA INTERFERENCE;

MUS;

EID: 84859157159     PISSN: 00144827     EISSN: 10902422     Source Type: Journal    
DOI: 10.1016/j.yexcr.2012.02.011     Document Type: Article

References (49)

1. Kim G., Lee T.H., Wetzel P., Geers C., Robinson M.A., Myers T.G., Owens J.W., Wehr N.B., Eckhaus M.W., Gros G., Wynshaw-Boris A., Levine R.L. Carbonic anhydrase III is not required in the mouse for normal growth, development, and life span. Mol. Cell. Biol. 2004, 24:9942-9947.
2. Supuran C.T. Carbonic anhydrases: novel therapeutic applications for inhibitors and activators. Nat. Rev. Drug Discov. 2008, 7:168-181.
3. Sanyal G., Swenson E.R., Pessah N.I., Maren T.H. The carbon dioxide hydration activity of skeletal muscle carbonic anhydrase. Inhibition by sulfonamides and anions. Mol. Pharmacol. 1982, 22:211-220.
4. Chai Y.C., Jung C.H., Lii C.K., Ashraf S.S., Hendrich S., Wolf B., Sies H., Thomas J.A. Identification of an abundant S-thiolated rat liver protein as carbonic anhydrase III; characterization of S-thiolation and dethiolation reactions. Arch. Biochem. Biophys. 1991, 284:270-278.
5. Lii C.K., Chai Y.C., Zhao W., Thomas J.A., Hendrich S. S-thiolation and irreversible oxidation of sulfhydryls on carbonic anhydrase III during oxidative stress: a method for studying protein modification in intact cells and tissues. Arch. Biochem. Biophys. 1994, 308:231-239.
6. Thomas J.A., Poland B., Honzatko R. Protein sulfhydryls and their role in the antioxidant function of protein S-thiolation. Arch. Biochem. Biophys. 1995, 319:1-9.
7. Cabiscol E., Levine R.L. Carbonic anhydrase III. Oxidative modification in vivo and loss of phosphatase activity during aging. J. Biol. Chem. 1995, 270:14742-14747.
8. Raisanen S.R., Lehenkari P., Tasanen M., Rahkila P., Harkonen P.L., Vaananen H.K. Carbonic anhydrase III protects cells from hydrogen peroxide-induced apoptosis. FASEB J. 1999, 13:513-522.
9. Cabiscol E., Levine R.L. The phosphatase activity of carbonic anhydrase III is reversibly regulated by glutathiolation. Proc. Natl. Acad. Sci. U. S. A. 1996, 93:4170-4174.
10. Mallis R.J., Hamann M.J., Zhao W., Zhang T., Hendrich S., Thomas J.A. Irreversible thiol oxidation in carbonic anhydrase III: protection by S-glutathiolation and detection in aging rats. Biol. Chem. 2002, 383:649-662.
11. Thomas J.A., Mallis R.J. Aging and oxidation of reactive protein sulfhydryls. Exp. Gerontol. 2001, 36:1519-1526.
12. Chen C.N., Ferrington D.A., Thompson L.V. Carbonic anhydrase III and four-and-a-half LIM protein 1 are preferentially oxidized with muscle unloading. J. Appl. Physiol. 2008, 105:1554-1561.
13. Harman D. Aging: a theory based on free radical and radiation chemistry. J. Gerontol. 1956, 11:298-300.
14. Lyons G.E., Buckingham M.E., Tweedie S., Edwards Y.H. Carbonic anhydrase III, an early mesodermal marker, is expressed in embryonic mouse skeletal muscle and notochord. Development 1991, 111:233-244.
15. Tashian R.E. The carbonic anhydrases: widening perspectives on their evolution, expression and function. Bioessays 1989, 10:186-192.
16. Rosen E.D., Spiegelman B.M. Adipocytes as regulators of energy balance and glucose homeostasis. Nature 2006, 444:847-853.
17. Spicer S.S., Ge Z.H., Tashian R.E., Hazen-Martin D.J., Schulte B.A. Comparative distribution of carbonic anhydrase isozymes III and II in rodent tissues. Am. J. Anat. 1990, 187:55-64.
18. Lynch C.J., Brennan W.A., Vary T.C., Carter N., Dodgson S.J. Carbonic anhydrase III in obese Zucker rats. Am. J. Physiol. 1993, 264:E621-E630.
19. Lynch C.J., Hazen S.A., Horetsky R.L., Carter N.D., Dodgson S.J. Differentiation-dependent expression of carbonic anhydrase II and III in 3T3 adipocytes. Am. J. Physiol. 1993, 265:C234-C243.
20. Gabrielsson B.L., Carlsson B., Carlsson L.M. Partial genome scale analysis of gene expression in human adipose tissue using DNA array. Obes. Res. 2000, 8:374-384.
21. Bolduc C., Larose M., Lafond N., Yoshioka M., Rodrigue M.A., Morissette J., Labrie C., Raymond V., St-Amand J. Adipose tissue transcriptome by serial analysis of gene expression. Obes. Res. 2004, 12:750-757.
22. Spiegelman B.M., Flier J.S. Obesity and the regulation of energy balance. Cell 2001, 104:531-543.
23. Haslam D.W., James W.P. Obesity. Lancet 2005, 366:1197-1209.
24. Furukawa S., Fujita T., Shimabukuro M., Iwaki M., Yamada Y., Nakajima Y., Nakayama O., Makishima M., Matsuda M., Shimomura I. Increased oxidative stress in obesity and its impact on metabolic syndrome. J. Clin. Invest. 2004, 114:1752-1761.
25. Urakawa H., Katsuki A., Sumida Y., Gabazza E.C., Murashima S., Morioka K., Maruyama N., Kitagawa N., Tanaka T., Hori Y., Nakatani K., Yano Y., Adachi Y. Oxidative stress is associated with adiposity and insulin resistance in men. J. Clin. Endocrinol. Metab. 2003, 88:4673-4676.
26. Yun Z., Maecker H.L., Johnson R.S., Giaccia A.J. Inhibition of PPAR gamma 2 gene expression by the HIF-1-regulated gene DEC1/Stra13: a mechanism for regulation of adipogenesis by hypoxia. Dev. Cell 2002, 2:331-341.
27. Carriere A., Carmona M.C., Fernandez Y., Rigoulet M., Wenger R.H., Penicaud L., Casteilla L. Mitochondrial reactive oxygen species control the transcription factor CHOP-10/GADD153 and adipocyte differentiation: a mechanism for hypoxia-dependent effect. J. Biol. Chem. 2004, 279:40462-40469.
28. Stanton L.W., Ponte P.A., Coleman R.T., Snyder M.A. Expression of CA III in rodent models of obesity. Mol. Endocrinol. 1991, 5:860-866.
29. Lynch C.J., McCall K.M., Billingsley M.L., Bohlen L.M., Hreniuk S.P., Martin L.F., Witters L.A., Vannucci S.J. Pyruvate carboxylase in genetic obesity. Am. J. Physiol. 1992, 262:E608-E618.
30. Spalding K.L., Arner E., Westermark P.O., Bernard S., Buchholz B.A., Bergmann O., Blomqvist L., Hoffstedt J., Naslund E., Britton T., Concha H., Hassan M., Ryden M., Frisen J., Arner P. Dynamics of fat cell turnover in humans. Nature 2008, 453:783-787.
31. Gesta S., Tseng Y.H., Kahn C.R. Developmental origin of fat: tracking obesity to its source. Cell 2007, 131:242-256.
32. Farmer S.R. Transcriptional control of adipocyte formation. Cell Metab. 2006, 4:263-273.
33. Cao Z., Umek R.M., McKnight S.L. Regulated expression of three C/EBP isoforms during adipose conversion of 3T3-L1 cells. Genes Dev. 1991, 5:1538-1552.
34. Tontonoz P., Graves R.A., Budavari A.I., Erdjument-Bromage H., Lui M., Hu E., Tempst P., Spiegelman B.M. Adipocyte-specific transcription factor ARF6 is a heterodimeric complex of two nuclear hormone receptors, PPAR gamma and RXR alpha. Nucleic Acids Res. 1994, 22:5628-5634.
35. Houstis N., Rosen E.D., Lander E.S. Reactive oxygen species have a causal role in multiple forms of insulin resistance. Nature 2006, 440:944-948.
36. Luo W., Cao J., Li J., He W. Adipose tissue-specific PPARgamma deficiency increases resistance to oxidative stress. Exp. Gerontol. 2008, 43:154-163.
37. Hogan B., Beddington R., Costantini F., Lacey E. Manipulating the Mouse Embryo: A Laboratory Manual 1994, Cold Spring Harbor Laboratory Press, New York.
38. Jodar L., Mercken E.M., Ariza J., Younts C., Gonzalez-Reyes J.A., Alcain F.J., Buron I., de Cabo R., Villalba J.M. Genetic deletion of Nrf2 promotes immortalization and decreases life span of murine embryonic fibroblasts. J. Gerontol. A Biol. Sci. Med. Sci. 2010, 66:247-256.
39. Peraldi P., Xu M., Spiegelman B.M. Thiazolidinediones block tumor necrosis factor-alpha-induced inhibition of insulin signaling. J. Clin. Invest. 1997, 100:1863-1869.
40. Wu Z., Rosen E.D., Brun R., Hauser S., Adelmant G., Troy A.E., McKeon C., Darlington G.J., Spiegelman B.M. Cross-regulation of C/EBP alpha and PPAR gamma controls the transcriptional pathway of adipogenesis and insulin sensitivity. Mol. Cell 1999, 3:151-158.
41. Imhoff B.R., Hansen J.M. Extracellular redox environments regulate adipocyte differentiation. Differentiation 2010, 80:31-39.
42. Takahashi T., Tabuchi T., Tamaki Y., Kosaka K., Takikawa Y., Satoh T. Carnosic acid and carnosol inhibit adipocyte differentiation in mouse 3T3-L1 cells through induction of phase2 enzymes and activation of glutathione metabolism. Biochem. Biophys. Res. Commun. 2009, 382:549-554.
43. Cho H.Y., Reddy S.P., Kleeberger S.R. Nrf2 defends the lung from oxidative stress. Antioxid. Redox Signal. 2006, 8:76-87.
44. Pi J., Leung L., Xue P., Wang W., Hou Y., Liu D., Yehuda-Shnaidman E., Lee C., Lau J., Kurtz T.W., Chan J.Y. Deficiency in the nuclear factor E2-related factor-2 transcription factor results in impaired adipogenesis and protects against diet-induced obesity. J. Biol. Chem. 2010, 285:9292-9300.
45. Reisman S.A., Csanaky I.L., Yeager R.L., Klaassen C.D. Nrf2 activation enhances biliary excretion of sulfobromophthalein by inducing glutathione-S-transferase activity. Toxicol. Sci. 2009, 109:24-30.
46. Chanas S.A., Jiang Q., McMahon M., McWalter G.K., McLellan L.L., Elcombe C.R., Henderson C.J., Wolf C.R., Moffat G.J., Itoh K., Yamamoto M., Hayes J.D. Loss of the Nrf2 transcription factor causes a marked reduction in constitutive and inducible expression of the glutathione S-transferase Gsta1, Gsta2, Gstm1, Gstm2, Gstm3 and Gstm4 genes in the livers of male and female mice. Biochem. J. 2002, 365:405-416.
47. Shin S., Wakabayashi N., Misra V., Biswal S., Lee G.H., Agoston E.S., Yamamoto M., Kensler T.M. NRF2 modulates aryl hydrocarbon receptor signaling: influence on adipogenesis. Mol. Cell. Biol. 2007, 27:7188-7197.
48. Tahara E.B., Navarete F.D., Kowaltowski A.J. Tissue-, substrate-, and site-specific characteristics of mitochondrial reactive oxygen species generation. Free Radic. Biol. Med. 2009, 46:1283-1297.
49. Wakabayashi K., Okamura M., Tsutsumi S., Nishikawa N.S., Tanaka T., Sakakibara I., Kitakami J., Ihara S., Hashimoto Y., Hamakubo T., Kodama T., Aburatani H., Sakai J. The peroxisome proliferator-activated receptor gamma/retinoid X receptor alpha heterodimer targets the histone modification enzyme PR-Set7/Setd8 gene and regulates adipogenesis through a positive feedback loop. Mol. Cell. Biol. 2009, 29:3544-3555.