Female mice lacking p47phox have altered adipose tissue gene expression and are protected against high fat-induced obesity

Physiological Genomics

Volumn 45, Issue 9, 2013, Pages 351-366

  Ronis, Martin J J ^a,b   Sharma, Neha ^a   Vantrease, Jamie ^a   Borengasser, Sarah J ^a,b   Ferguson, Matthew ^a   Mercer, Kelly E ^b   Cleves, Mario A ^a,b   Gomez Acevedo, Horacio ^a,b   Badger, Thomas M ^a,b  

^a UNIVERSITY OF ARKANSAS FOR MEDICAL SCIENCES   (United States)

^b UNIVERSITY OF ARKANSAS FOR MEDICAL SCIENCES   (United States)

Author keywords

Adipose; Metabolism; NADPH oxidase; Obesity; p47phox

Indexed keywords

ADIPONECTIN; CD36 ANTIGEN; CHOLESTEROL; ESTRADIOL; FAT; FATTY ACID; LEPTIN; LIPOPROTEIN LIPASE; MESSENGER RNA; MITOCHONDRIAL TRANSCRIPTION FACTOR A; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA; PREF 1 PROTEIN; PROTEIN; PROTEIN P47; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE 2; TRIACYLGLYCEROL; UNCLASSIFIED DRUG; UNCOUPLING PROTEIN 2;

ADIPOCYTE; ADIPOSE TISSUE; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL DIFFERENTIATION; CELL SIZE; CONTROLLED STUDY; CYTOSOL; ENERGY EXPENDITURE; ENERGY METABOLISM; FATTY LIVER; FEMALE; GENE EXPRESSION; GENOTYPE; HOMEOSTASIS; HYPERGLYCEMIA; LIPID DIET; MALE; METABOLISM; MICROARRAY ANALYSIS; MOUSE; NONHUMAN; OBESITY; PRIORITY JOURNAL; TRIACYLGLYCEROL BLOOD LEVEL;

ADIPOSE; METABOLISM; NADPH-OXIDASE; OBESITY; P47PHOX;

ADIPOGENESIS; ADIPOSE TISSUE; ANIMALS; BODY COMPOSITION; BODY WEIGHT; CELL SEPARATION; DIET, HIGH-FAT; ENERGY METABOLISM; ESTRADIOL; FATTY ACIDS; FEEDING BEHAVIOR; FEMALE; GENE EXPRESSION REGULATION; GROWTH AND DEVELOPMENT; HYDROGEN PEROXIDE; MAGNETIC RESONANCE SPECTROSCOPY; MALE; MICE; MITOCHONDRIA, LIVER; NADPH OXIDASE; OBESITY; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; ORGAN SIZE; SEX CHARACTERISTICS; TETRADECANOYLPHORBOL ACETATE;

MUS;

EID: 84878634688     PISSN: 10948341     EISSN: 15312267     Source Type: Journal    
DOI: 10.1152/physiolgenomics.00148.2012     Document Type: Article

References (46)

1. Anikumar N, Weber R, Zhang M, Brewer A, Shah AM. Nox4 and Nox2 NADPH oxidases mediate distinct cellular redox signaling responses to agonist stimulation. Arterioscler Thromb Vasc Biol 28: 1347-1354, 2008.
2. Borengasser SJ, Lau F, Kang P, Blackburn ML, Ronis MJJ, Badger TM, Shankar K. Exposure to maternal obesity during gestation impairs fatty acid oxidation and mitochondrial SIRT3 expression in the offspring at weaning. PLos One 6: e24068, 2011.
3. Chaible LM, Sanches DS, Cogliati B, Mennecier G, Dagli ML. Delayed osteoblastic differentiation and bone development in Cx43 knockout mice. Toxicol Pathol 39: 1046-1055, 2011.
4. Chen JR, Lazarenko OP, Blackburn ML, Badger TM, Ronis MJ. A role for ethanol-induced oxidative stress in controlling lineage commitment of mesenchymal stromal cells through inhibition of Wnt/beta catenin signaling. J Bone Miner Res 25: 1117-1127, 2010.
5. Chen JR, Lazarenko OP, Haley RL, Blackburn ML, Badger TM, Ronis MJJ. Ethanol impairs estrogen receptor signaling and activates senescence pathways in osteoblasts. Protection by estradiol. J Bone Miner Res 24: 221-230, 2009.
6. Cross AR, Segal AW. The NADPH oxidase of professional phagocytes-prototype of the NOX electron transport chain systems. Biochim Biophys Acta 1657: 1-22, 2004.
7. 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 114: 1752-1761, 2004.
8. Gibbons JD, Chakraboti S. Nonparametric Statistical Inference (5th Ed.). Boca Raton, FL: Chipman & Hall/CRC, 2011.
9. Govoni KE, Baylink DJ, Chen J, Mohan S. Disruption of four and a half LIM 2 decreases bone mineral content and bone mineral density in femur and tibia bones of female mice. Calcif Tissue Int 79: 112-117, 2006.
10. Gunther T, Schinke T. Mouse genetics have uncovered new paradigms in bone biology. Trends Endocrinol Metab 11: 189-193, 2000.
11. Haesegawa T, Kikuyama M, Sakurai K, Kambayashi Y, Adachi M, Saniabadi AR, Kuwano H, Nakano M. Mechanism of superoxide anion production by hepatic sinusoidal epithelial cells and Kupffer cells during short term ethanol perfusion in the liver. Liver 22: 321-329, 2002.
12. Horvath TL, Andrews ZB, Diano S. Fuel utilization by hypothalamic neurons: role for ROS. Trends Endocrinol Metab 20: 78-87, 2009.
13. Kanda Y, Hinata T, Kang SW, Watanabe Y. Reactive oxygen species mediate adipocyte differentiation in mesenchymal stem cells. Life Sci 89: 250-258, 2011.
14. Kennedy DJ, Kashyap SR. Pathogenic role of scavenger receptor CD36 in the metabolic syndrome and diabetes. Metab Syndr Relat Disord 9: 239-245, 2011.
15. Kim KS, Choi HW, Yoon HE, Kim IY. Reactive oxygen species generated by NADPH oxidase 2 and 4 are required for chondrogenic differentiation. J Biol Chem 285: 40294-40302, 2010.
16. Lai CF, Bai S, Uthgenannt BA, Halstead LR, McLoughlin P, Schafer BW, Chu PH, Chen J, Otey CA, Cao X, Cheng SL. Four and half lim protein 2 (FHL2) stimulates osteoblast differentiation. J Bone Miner Res 21: 17-28, 2006.
17. Lee OH, Seo MJ, Choi HS, Lee BY. Pycnogenol inhibits lipid accumulation in 3T3-L1 adipocytes with the modulation of reactive oxygen species (ROS) production associated with antioxidant enzyme responses. Phytother Res 26: 403-411, 2012.
18. Lee YH, Nair S, Rousseau E, Allison DB, Page GP, Tataranni PA, Bogardus C, Permana PA. Microarray profiling of isolated abdominal subcutaneous adipocytes from obese vs. non-obese Pima Indians: increased expression of inflammation-related genes. Diabetologia 48: 1776-1783, 2005.
19. Leto TL, Morand S, Hurt D, Ueyama T. Targeting and regulation of reactive oxygen species generation by Nox family NADPH oxidases. Antioxid Redox Signal 11: 2607-2619, 2009.
20. Levin I, Petrasek J, Szabo G. The presence of p47phox in liver parenchymal cells is a key mediator in the pathogenesis of alcoholic liver steatosis. Alc Clin Exp Res 36: 1397-1406, 2012.
21. Li Y, Mouche S, Sajic T, Veyrat-Durebex C, Supale R, Pierroz D, Ferrari S, Negro F, Hasler U, Feraille E, Moll S, Meda P, Deffert C, Montet X, Krause KH, Szanto I. Deficiency in the NADPH oxidase 4 predisposes towards diet-induced obesity. Int J Obesity 36: 1503-1513, 2012.
22. Li Z, Zhou Z, Saunders MM, Donahue HJ. Modulation of connexin43 alters expression of osteoblastic differentiation markers. Am J Physiol Cell Physiol 290: C1248-C1255, 2006.
23. Lin L, Pang W, Chen K, Wang F, Gengler J, Sun Y, Tong Q. Adipocyte expression of PU.1 transcription factor causes insulin resistance through upregulation of inflammatory cytokine gene expression and ROS production. Am J Physiol Endocrinol Metab 302: E1550-E1559, 2012.
24. Longo N, Amat di San Filippo C, Pasquali M. Disorders of carnitine transport and the carnitine cycle. Am J Med Genet C Semin Med Genet 142C: 77-85, 2006.
25. Matsuzawa-Nagata N, Takamura T, Ando H, Nakamua S, Kurita S, Misu H, Ota T, Yokoyama M, Honda M, Miyamoto K, Kaneko S. Increased oxidative stress precedes the onset of high fat diet-induced insulin resistance and obesity. Metabolism 57: 1071-1077, 2008.
26. Park HS, Jin DK, Shin SM, Jang MK, Longo N, Park JW, Bae DS, Bae YS. Impaired generation of reactive oxygen species in leprechaunism through downregulation of Nox4. Diabetes 54; 3175-3181, 2005.
27. Peshavariya HM, Dusting GJ, Selemidis S. Analysis of dihydroethidium fluorescence for the detection of intracellular and extracellular superoxide produced by NADPH oxidase. Free Radic Res 41: 699-712, 2007.
28. Petry A, Djordjevic T, Weitnauer M, Kietzmann T, Hess J, Gorlach A. NOX2 and NOX4 mediate proliferative response in endothelial cells. Antioxid Redox Signal 8: 1473-1484, 2006.
29. Piccoli C, D'Aprile A, Scrima R, Ripoli M, Boffoli D, Tabilio A, Caitanio N. Role of reactive oxygen species as signal molecules in the pre-commitment phase of adult stem cells. Ital J Biochem 56: 295-301, 2007.
30. Ronis MJJ, Baumgardner JN, Marecki J, Hennings L, Wu X, Shankar K, Cleves MA, Gomez-Acevedo H, Badger TM. Dietary fat source alters hepatic gene expression profile and determines the type of liver pathology in rats overfed via total enteral nutrition, Physiol. Genomics 44: 1073-1089, 2012.
31. Ronis MJJ, Chen Y, Shankar K, Gomez-Acevedo H, Badeaux J, Blackburn ML, Badger TM. Formula feeding and protein source alter hepatic gene expression, iron and cholesterol homeostasis in neonatal piglets. Physiol Genomics 43: 1281-1293, 2011.
32. Ronis MJJ, Rowlands JC, Hakkak R, Badger TM. Altered inducibility of hepatic CYP1A enzymes by 3-methylcholanthrene and isosafrole in male rats fed diets containing casein, soy protein isolate or whey. J Nutr 131: 1180-1188, 2001.
33. Sasaki H, Yamamoto H, Toiminaga K, Masuda K, Kawai T, Teshima-Kondo S, Matsuno K, Yabe-Nishimura C, Rokutan K. Receptor activator of nuclear factor-kappaB ligand-induced mouse osteoclast differentiation is associated with switching between NADPH-oxidase homologues. Free Radic Biol Med 47: 189-199, 2009.
34. Schoonjans K, Staels B, Auwerx J. The peroxisome proliferator activated receptors (PPARs) and their effects on lipid metabolism and adipocytes differentiation. Biochim Biophys Acta 1302: 93-109, 1996.
35. Schroeder K, Wandzioch K, Helmcke I, Brandes RP. Nox4 acts as a switch between differentiation and proliferation in preadipocytes. Arterioscler Thromb Vasc Biol 29: 239-245, 2009.
36. Shankar K, Harrell A, Liu X, Gilcrist J, Ronis MJJ, Badger TM,. Maternal obesity at conception programs obesity in the offspring. Am J Physiol Regul Integr Comp Physiol 294: R528-R538, 2008.
37. Shankar K, Harrell A, Kang P, Zhong Y, Marecki JC, Ronis MJJ, Badger TM. Maternal overweight programs insulin and adiponectin signaling in the offspring. Endocrinology 151: 2577-2589, 2010.
38. Silver AE, Beske SD, Christu DD, Donato AJ, Moreau KL, Eskurza I, Gates PE, Seals DR. Overweight and obese humans demonstrate increased vascular endothelial NADP(H) oxidase-p47(phox) expression and evidence of endothelial oxidative stress. Circulation 115: 627-637, 2007.
39. Smas CM, Chen L, Zhao L, Latasa MJ, Sul HS. Transcriptional repression of pref-1 by glucocortiocoids promotes 3T3-L1 adipocyte differentiation. J Biol Chem 274: 12632-12641, 1999.
40. Wagoner B, Hausman DB, Harris RB. Direct and indirect effects of leptin on preadipocyte proliferation and differentiation. Am J Physiol Regul Integr Comp Physiol 290: R1557-R1564, 2006.
41. Wang Y, Kim KA, Kim-H, Sul HS. Pref-1, a preadipocyte secreted factor that inhibits adipogenesis. J Nutr 136: 2953-2956, 2006.
42. Xiong Y, Lei QY, Zhao S, Guan KL. Regulation of glycolysis and gluconeogenesis by acetylation of PKM and PEPCK. Cold Spring Har Symp Quant Biol 76: 285-289, 2011.
43. Xu X, Yavar Z, Verdin M, Ying Z, Mihai G, Kampfath T, Wang A, Zhong M, Lippmann M, Chen LC, Rajogopalan S, Sun Q. Effect of early particulate air pollution exposure on obesity in mice: role of P47phox. Arteroscler Thromb Vasc Biol 30: 2518-2527, 2010.
44. Yasmeen R, Reichert B, Deiuliis J, Yang F, Lynch A, Meyers J, Sharlach M, Shin S, Volz KS, Green KB, Lee K, Alder H, Duester G, Zechner R, Rajagopalan S, Ziouzenkova O. Autocrine function of aldehyde dehydrogenase 1 as a determinant of diet and sex-specific differences in visceral adiposity. Diabetes 62: 124-36, 2013.
45. Zechner R, Strauss J, Frank S, Wagner E, Hofmann W, Kratky D, Hiden M, Levak-Frank S. The role of lipoprotein lipase in adipose tissue development and metabolism. Int J Obes Relat Metab Disord 24: S53-S56, 2000.
46. Zhou J, Febbraio M, Wada T, Zhai Y, Kuruba R, He J, Lee JH, Khadem S, Ren S, Silverstein RL, Xie W. Hepatic fatty acid transporter CD36 is a common target of LXR, PXR and PPAR in promoting steatosis. Gastroenterology 134: 556-567, 2008.