Ascorbic acid deficiency affects genes for oxidation-reduction and lipid metabolism in livers from SMP30/GNL knockout mice

Biochimica et Biophysica Acta - General Subjects

Volumn 1840, Issue 7, 2014, Pages 2289-2298

  Takahashi, Keita ^a,b   Kishimoto, Yuki ^a,b   Konishi, Tomokazu ^c   Fujita, Yasunori ^a   Ito, Masafumi ^a   Shimokado, Kentaro ^b   Maruyama, Naoki ^a   Ishigami, Akihito ^a  

^a TOKYO METROPOLITAN INSTITUTE OF GERONTOLOGY   (Japan)

^b TOKYO MEDICAL AND DENTAL UNIVERSITY   (Japan)

^c AKITA PREFECTURAL UNIVERSITY   (Japan)

Author keywords

Ascorbic acid; Bile acid; Cyp7a1; Lipid metabolism; Microarray; Nrf2

Indexed keywords

ASCORBIC ACID; BILE ACID; CHOLESTEROL; CHOLESTEROL 7ALPHA MONOOXYGENASE; FATTY ACID; GLUCONOLACTONASE; IRON; LIPID; PHOSPHOLIPID; REACTIVE OXYGEN METABOLITE; REGUCALCIN; TRANSCRIPTION FACTOR NRF2; TRANSCRIPTOME; TRIACYLGLYCEROL;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; ASCORBIC ACID DEFICIENCY; BILE ACID SYNTHESIS; BODY WEIGHT; CONTROLLED STUDY; CYP7A1 GENE; ENZYME ACTIVATION; ENZYME ACTIVE SITE; FEMALE; GALLBLADDER; GENE; GENE EXPRESSION; IN VIVO STUDY; KNOCKOUT MOUSE; LIPID METABOLISM; LIVER; MALE; MICROARRAY ANALYSIS; MOUSE; NONHUMAN; NRF2 GENE; OXIDATION REDUCTION REACTION; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; SMP30 GNL KNOCKOUT MOUSE; WESTERN BLOTTING;

ASCORBIC ACID; BILE ACID; CYP7A1; LIPID METABOLISM; MICROARRAY; NRF2;

ANIMALS; ASCORBIC ACID; ASCORBIC ACID DEFICIENCY; CALCIUM-BINDING PROTEINS; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; LIPID METABOLISM; LIVER; MICE; MICE, KNOCKOUT; MICROARRAY ANALYSIS; OXIDATION-REDUCTION; TRANSCRIPTOME;

EID: 84899887766     PISSN: 03044165     EISSN: 18728006     Source Type: Journal    
DOI: 10.1016/j.bbagen.2014.03.019     Document Type: Article

References (68)

1. M. Nishikimi, T. Koshizaka, T. Ozawa, and K. Yagi Occurrence in humans and guinea pigs of the gene related to their missing enzyme L-gulono-γ- lactone oxidase Arch. Biochem. Biophys. 267 1988 842 846
2. E. Magiorkinis, A. Beloukas, and A. Diamantis Scurvy: past, present and future Eur. J. Intern. Med. 22 2011 147 152
3. M.E. Rice Ascorbate regulation and its neuroprotective role in the brain Trends Neurosci. 23 2000 209 216
4. M. Nishikimi Oxidation of ascorbic acid with superoxide anion generated by the xanthine-xanthine oxidase system Biochem. Biophys. Res. Commun. 63 1975 463 468
5. R.S. Bodannes, and P.C. Chan Ascorbic acid as a scavenger of singlet oxygen FEBS Lett. 105 1979 195 196
6. B.H. Bielski, H.W. Richter, and P.C. Chan Some properties of the ascorbate free radical Ann. N. Y. Acad. Sci. 258 1975 231 237
7. Z. Radak, Z. Zhao, S. Goto, and E. Koltai Age-associated neurodegeneration and oxidative damage to lipids, proteins and DNA Mol. Aspects Med. 32 2011 305 315
8. B.A. Eipper, R.E. Mains, and C.C. Glembotski Identification in pituitary tissue of a peptide α-amidation activity that acts on glycine-extended peptides and requires molecular oxygen, copper, and ascorbic acid Proc. Natl. Acad. Sci. U. S. A. 80 1983 5144 5148
9. V. May, and B.A. Eipper Regulation of peptide amidation in cultured pituitary cells J. Biol. Chem. 260 1985 16224 16231
10. S. Friedman, and S. Kaufman 3,4-Dihydroxyphenylethylamine β-hydroxylase. Physical properties, copper content, and role of copper in the catalytic activity J. Biol. Chem. 240 1965 4763 4773
11. M. Levine, K. Morita, and H. Pollard Enhancement of norepinephrine biosynthesis by ascorbic acid in cultured bovine chromaffin cells J. Biol. Chem. 260 1985 12942 12947
12. M. Levine New concepts in the biology and biochemistry of ascorbic acid N. Engl. J. Med. 314 1986 892 902
13. K.I. Kivirikko, and J. Myllyharju Prolyl 4-hydroxylases and their protein disulfide isomerase subunit Matrix Biol. 16 1998 357 368
14. R. Myllyla, V. Gunzler, K.I. Kivirikko, and D.D. Kaska Modification of vertebrate and algal prolyl 4-hydroxylases and vertebrate lysyl hydroxylase by diethyl pyrocarbonate. Evidence for histidine residues in the catalytic site of 2-oxoglutarate-coupled dioxygenases Biochem. J. 286 1992 923 927
15. B. Peterkofsky, and S. Udenfriend Enzymatic hydroxylation of proline in microsomal polypeptide leading to formation of collagen Proc. Natl. Acad. Sci. U. S. A. 53 1965 335 342
16. K. Hirota, and G.L. Semenza Regulation of hypoxia-inducible factor 1 by prolyl and asparaginyl hydroxylases Biochem. Biophys. Res. Commun. 338 2005 610 616
17. M.C. Vissers, S.P. Gunningham, M.J. Morrison, G.U. Dachs, and M.J. Currie Modulation of hypoxia-inducible factor-1 α in cultured primary cells by intracellular ascorbate Free Radic. Biol. Med. 42 2007 765 772
18. T. Mori, A. Ishigami, K. Seyama, R. Onai, S. Kubo, K. Shimizu, N. Maruyama, and Y. Fukuchi Senescence marker protein-30 knockout mouse as a novel murine model of senile lung Pathol. Int. 54 2004 167 173
19. A. Ishigami, and N. Maruyama Significance of SMP30 in gerontology Geriatr. Gerontol. Int. 7 2007 316 325
20. N. Maruyama, A. Ishigami, and Y. Kondo Pathophysiological significance of senescence marker protein-30 Geriatr. Gerontol. Int. 10 2010 S88 S98
21. Y. Kondo, Y. Inai, Y. Sato, S. Handa, S. Kubo, K. Shimokado, S. Goto, M. Nishikimi, N. Maruyama, and A. Ishigami Senescence marker protein 30 functions as gluconolactonase in l-ascorbic acid biosynthesis, and its knockout mice are prone to scurvy Proc. Natl. Acad. Sci. U. S. A. 103 2006 5723 5728
22. K. Koike, Y. Kondo, M. Sekiya, Y. Sato, K. Tobino, S.I. Iwakami, S. Goto, K. Takahashi, N. Maruyama, K. Seyama, and A. Ishigami Complete lack of vitamin C intake generates pulmonary emphysema in senescence marker protein-30 knockout mice Am. J. Physiol. Lung Cell. Mol. Physiol. 298 2010 L784 L792
23. Y. Ishikawa, K. Hashizume, S. Kishimoto, Y. Tezuka, H. Nishigori, N. Yamamoto, Y. Kondo, N. Maruyama, A. Ishigami, and D. Kurosaka Effect of vitamin C depletion on UVR-B induced cataract in SMP30/GNL knockout mice Exp. Eye Res. 94 2012 85 89
24. Y. Sato, K.Y. Arai, T. Nishiyama, Y. Nomura, Y. Kishimoto, S. Aizawa, N. Maruyama, and A. Ishigami Ascorbic acid deficiency leads to epidermal atrophy and UVB-induced skin pigmentation in SMP30/GNL knockout hairless mice J. Investig. Dermatol. 132 2012 2112 2115
25. K.Y. Arai, Y. Sato, Y. Kondo, C. Kudo, H. Tsuchiya, Y. Nomura, A. Ishigami, and T. Nishiyama Effects of vitamin C deficiency on the skin of the senescence marker protein-30 (SMP30) knockout mouse Biochem. Biophys. Res. Commun. 385 2009 478 483
26. Y. Kondo, T. Sasaki, Y. Sato, A. Amano, S. Aizawa, M. Iwama, S. Handa, N. Shimada, M. Fukuda, M. Akita, J. Lee, K.S. Jeong, N. Maruyama, and A. Ishigami Vitamin C depletion increases superoxide generation in brains of SMP30/GNL knockout mice Biochem. Biophys. Res. Commun. 377 2008 291 296
27. Y. Sato, S. Kajiyama, A. Amano, Y. Kondo, T. Sasaki, S. Handa, R. Takahashi, M. Fukui, G. Hasegawa, N. Nakamura, H. Fujinawa, T. Mori, M. Ohta, H. Obayashi, N. Maruyama, and A. Ishigami Hydrogen-rich pure water prevents superoxide formation in brain slices of vitamin C-depleted SMP30/GNL knockout mice Biochem. Biophys. Res. Commun. 375 2008 346 350
28. A. Amano, T. Aigaki, N. Maruyama, and A. Ishigami Ascorbic acid depletion enhances expression of the sodium-dependent vitamin C transporters, SVCT1 and SVCT2, and uptake of ascorbic acid in livers of SMP30/GNL knockout mice Arch. Biochem. Biophys. 496 2010 38 44
29. T.L. Duarte, M.S. Cooke, and G.D. Jones Gene expression profiling reveals new protective roles for vitamin C in human skin cells Free Radic. Biol. Med. 46 2009 78 87
30. Y. Jiao, J. Zhang, J. Yan, J. Stuart, G. Gibson, L. Lu, R. Willaims, Y.J. Wang, and W. Gu Differential gene expression between wild-type and Gulo-deficient mice supplied with vitamin C Genet. Mol. Biol. 34 2011 386 395
31. D.H. Yu, K.H. Lee, J.Y. Lee, S. Kim, D.M. Shin, J.H. Kim, Y.S. Lee, Y.S. Lee, S.K. Oh, S.Y. Moon, S.H. Lee, and Y.S. Lee Changes of gene expression profiles during neuronal differentiation of central nervous system precursors treated with ascorbic acid J. Neurosci. Res. 78 2004 29 37
32. S. Ikeda, F. Horio, and A. Kakinuma Ascorbic acid deficiency changes hepatic gene expression of acute phase proteins in scurvy-prone ODS rats J. Nutr. 128 1998 832 838
33. F. Horio, K. Kiyama, M. Kobayashi, K. Kawai, and T. Tsuda Ascorbic acid deficiency stimulates hepatic expression of inflammatory chemokine, cytokine-induced neutrophil chemoattractant-1, in scurvy-prone ODS rats J. Nutr. Sci. Vitaminol. 52 2006 28 32
34. A. Ishigami, T. Fujita, S. Handa, T. Shirasawa, H. Koseki, T. Kitamura, N. Enomoto, N. Sato, T. Shimosawa, and N. Maruyama Senescence marker protein-30 knockout mouse liver is highly susceptible to tumor necrosis factor-α- and Fas-mediated apoptosis Am. J. Pathol. 161 2002 1273 1281
35. T. Fujita, J.L. Mandel, T. Shirasawa, O. Hino, T. Shirai, and N. Maruyama Isolation of cDNA clone encoding human homologue of senescence marker protein-30 (SMP30) and its location on the X chromosome Biochim. Biophys. Acta 1263 1995 249 252
36. Y. Sato, T. Uchiki, M. Iwama, Y. Kishimoto, R. Takahashi, and A. Ishigami Determination of dehydroascorbic acid in mouse tissues and plasma by using tris(2-carboxyethyl)phosphine hydrochloride as reductant in metaphosphoric acid/ethylenediaminetetraacetic acid solution Biol. Pharm. Bull. 33 2010 364 369
37. P. Chomczynski, and N. Sacchi Single-step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction Anal. Biochem. 162 1987 156 159
38. T. Konishi Data distribution of short oligonucleotide expression arrays and its application to the construction of a generalized intellectual framework Stat. Appl. Genet. Mol. Biol. 7 2008 (Article 25.)
39. T. Konishi Microarray test results should not be compensated for multiplicity of gene contents BMC Syst. Biol. 5 Suppl. 2 2011 S6
40. O.H. Lowry, N.J. Rosebrough, A.L. Farr, and R.J. Randall Protein measurement with the Folin phenol reagent J. Biol. Chem. 193 1951 265 275
41. U.K. Laemmli Cleavage of structural proteins during the assembly of the head of bacteriophage T4 Nature 227 1970 680 685
42. K. Asahina, H. Fujimori, K. Shimizu-Saito, Y. Kumashiro, K. Okamura, Y. Tanaka, K. Teramoto, S. Arii, and H. Teraoka Expression of the liver-specific gene Cyp7a1 reveals hepatic differentiation in embryoid bodies derived from mouse embryonic stem cells Genes Cells 9 2004 1297 1308
43. S.A. Reisman, D.B. Buckley, Y. Tanaka, and C.D. Klaassen CDDO-Im protects from acetaminophen hepatotoxicity through induction of Nrf2-dependent genes Toxicol. Appl. Pharmacol. 236 2009 109 114
44. 2-induced PC12 cell death via Nrf2/ARE activation Bioorg. Med. Chem. 18 2010 3133 3139
45. K. Hemanth Kumar, A. Tamatam, A. Pal, and F. Khanum Neuroprotective effects of Cyperus rotundus on SIN-1 induced nitric oxide generation and protein nitration: ameliorative effect against apoptosis mediated neuronal cell damage Neurotoxicology 34 2013 150 159
46. H.S. Um, E.B. Kang, J.H. Koo, H.T. Kim, L. Jin, E.J. Kim, C.H. Yang, G.Y. An, I.H. Cho, and J.Y. Cho Treadmill exercise represses neuronal cell death in an aged transgenic mouse model of Alzheimer's disease Neurosci. Res. 69 2011 161 173
47. G.T. Wondrak, N.F. Villeneuve, S.D. Lamore, A.S. Bause, T. Jiang, and D.D. Zhang The cinnamon-derived dietary factor cinnamic aldehyde activates the Nrf2-dependent antioxidant response in human epithelial colon cells Molecules 15 2010 3338 3355
48. R. Sato, J. Yang, X. Wang, M.J. Evans, Y.K. Ho, J.L. Goldstein, and M.S. Brown Assignment of the membrane attachment, DNA binding, and transcriptional activation domains of sterol regulatory element-binding protein-1 (SREBP-1) J. Biol. Chem. 269 1994 17267 17273
49. Y. Duan, Y. Chen, W. Hu, X. Li, X. Yang, X. Zhou, Z. Yin, D. Kong, Z. Yao, D.P. Hajjar, L. Liu, Q. Liu, and J. Han Peroxisome proliferator-activated receptor gamma activation by ligands and dephosphorylation induces proprotein convertase subtilisin kexin type 9 and low density lipoprotein receptor expression J. Biol. Chem. 287 2012 23667 23677
50. C.B. Campbell, C. McGuffie, and L.W. Powell The measurement of sulphated and non-sulphated bile acids in serum using gas-liquid chromatography Clin. Chim. Acta 63 1975 249 262
51. J. Folch, M. Lees, and G.H. Sloane Stanley A simple method for the isolation and purification of total lipids from animal tissues J. Biol. Chem. 226 1957 497 509
52. F. Mashige, N. Tanaka, A. Maki, S. Kamei, and M. Yamanaka Direct spectrophotometry of total bile acids in serum Clin. Chem. 27 1981 1352 1356
53. S. Shimizu, K. Yasui, Y. Tani, and H. Yamada Acyl-CoA oxidase from Candida tropicalis Biochem. Biophys. Res. Commun. 91 1979 108 113
54. C.C. Allain, L.S. Poon, C.S. Chan, W. Richmond, and P.C. Fu Enzymatic determination of total serum cholesterol Clin. Chem. 20 1974 470 475
55. R.W. Spayd, B. Bruschi, B.A. Burdick, G.M. Dappen, J.N. Eikenberry, T.W. Esders, J. Figueras, C.T. Goodhue, D.D. LaRossa, R.W. Nelson, R.N. Rand, and T.W. Wu Multilayer film elements for clinical analysis: applications to representative chemical determinations Clin. Chem. 24 1978 1343 1350
56. M. Takayama, S. Itoh, T. Nagasaki, and I. Tanimizu A new enzymatic method for determination of serum choline-containing phospholipids Clin. Chim. Acta 79 1977 93 98
57. F. Horio, K. Ozaki, H. Oda, S. Makino, Y. Hayashi, and A. Yoshida Effect of dietary ascorbic acid, cholesterol and PCB on cholesterol and bile acid metabolism in a rat mutant unable to synthesize ascorbic acid J. Nutr. 119 1989 409 415
58. H.Y. Cho, and S.R. Kleeberger Nrf2 protects against airway disorders Toxicol. Appl. Pharmacol. 244 2010 43 56
59. T. Rangasamy, C.Y. Cho, R.K. Thimmulappa, L. Zhen, S.S. Srisuma, T.W. Kensler, M. Yamamoto, I. Petrache, R.M. Tuder, and S. Biswal Genetic ablation of Nrf2 enhances susceptibility to cigarette smoke-induced emphysema in mice J. Clin. Invest. 114 2004 1248 1259
60. A.T. Dinkova-Kostova, and P. Talalay NAD(P)H:quinone acceptor oxidoreductase 1 (NQO1), a multifunctional antioxidant enzyme and exceptionally versatile cytoprotector Arch. Biochem. Biophys. 501 2010 116 123
61. D. Siegel, D.L. Gustafson, D.L. Dehn, J.Y. Han, P. Boonchoong, L.J. Berliner, and D. Ross NAD(P)H:quinone oxidoreductase 1: role as a superoxide scavenger Mol. Pharmacol. 65 2004 1238 1247
62. R.A. Davis, J.H. Miyake, T.Y. Hui, and N.J. Spann Regulation of cholesterol-7α-hydroxylase: BAREly missing a SHP J. Lipid Res. 43 2002 533 543
63. T. Spolitak, E.G. Funhoff, and D.P. Ballou Spectroscopic studies of the oxidation of ferric CYP153A6 by peracids: insights into P450 higher oxidation states Arch. Biochem. Biophys. 493 2010 184 191
64. W.S. Harris, B.A. Kottke, and M.T. Subbiah Bile acid metabolism in ascorbic acid-deficient guinea pigs Am. J. Clin. Nutr. 32 1979 1837 1841
65. D.E. Holloway, and J.M. Rivers Influence of chronic ascorbic acid deficiency and excessive ascorbic acid intake on bile acid metabolism and bile composition in the guinea pig J. Nutr. 111 1981 412 424
66. J.D. Horton, J.L. Goldstein, and M.S. Brown SREBPs: activators of the complete program of cholesterol and fatty acid synthesis in the liver J. Clin. Invest. 109 2002 1125 1131
67. A. Ishigami, Y. Kondo, R. Nanba, T. Ohsawa, S. Handa, S. Kubo, M. Akita, and N. Maruyama SMP30 deficiency in mice causes an accumulation of neutral lipids and phospholipids in the liver and shortens the life span Biochem. Biophys. Res. Commun. 315 2004 575 580
68. A. Ishigami, S. Handa, N. Maruyama, and P.C. Supakar Nuclear localization of senescence marker protein-30, SMP30, in cultured mouse hepatocytes and its similarity to RNA polymerase Biosci. Biotechnol. Biochem. 67 2003 158 160