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administration of hydrogen-saturated drinking water

Hepatic Oxidoreduction-Related Genes Are Upregulated by Administration of Hydrogen-Saturated Drinking Water

Yuji N AKAI ,1;y Bunpei S ATO ,2Shota U SHIAMA ,1Shinji O KADA ,1Keiko A BE ,1;3and Soichi A RAI 3;4

Graduate School of Agricultural and Life Sciences,The University of Tokyo,1-1-1Yayoi,Bunkyo-ku,Tokyo 113-8657,Japan 2

MiZ Co.,Ltd.,1-16-5Zengyo,Fujisawa,Kanagawa 251-0871,Japan 3

Food Safety and Reliability Project,Kanagawa Academy of Science and Technology,KSP EAST 301,3-2-1Sakado,Takatsu-ku,Kawasaki,Kanagawa 213-0012,Japan 4

Department of Nutritional Science,Faculty of Applied Bioscience,Tokyo University of Agriculture,1-1-1Sakuragaoka,Setagaya-ku,Tokyo 156-8502,Japan

Received November 19,2010;Accepted December 27,2010;Online Publication,April 22,2011[doi:10.1271/bbb.100819]

The e?ects of the administration of molecular hydro-gen-saturated drinking water (hydrogen water)on hepatic gene expression were investigated in https://www.wendangku.net/doc/f514158868.html,ing DNA microarrays,548upregulated and 695downregu-lated genes were detected in the liver after 4weeks of administration of hydrogen water.Gene Ontology analysis revealed that genes for oxidoreduction-related proteins,including hydroxymethylglutaryl CoA reduc-tase,were signi?cantly enriched in the upregulated genes.Key words:

hydrogen-saturated water;DNA microarray;rat;liver;oxidation-reduction

Molecular hydrogen has a potent antioxidant e?ect against hydroxyl radicals,which may be involved in tissue protection from oxidative stress in vivo .1,2)Drinking molecular hydrogen-saturated water (hydrogen water)prevented atherosclerosis development in apoli-poprotein E knockout mice,3)but its e?ect on gene expression in normal animals is still unclear.To determine the e?ects of hydrogen water consumption on gene expression comprehensively,we conducted experiments using DNA microarray technology.

The animal experiments were performed by Mercian Cleantec (Fujisawa,Japan).In brief,4-week-old male Sprague-Dawley rats were acclimatized for 4d in a room maintained at 24?3 C at a relative humidity of 55?15%under a 12-h light-dark cycle (lights on at 7:00,o?at 19:00),and were fed a commercial diet ad libitum (MF,Oriental Yeast,Yokohama,Japan).After acclimatization,the rats were divided into two groups (n ?8per group)with similar mean body weights.During a period of 4weeks,one group (control group)was supplied sterilized distilled water and the other (HW group),hydrogen water produced by MiZ Co.,Ltd.(Fujisawa,Japan),which contains 0.7m M dissolved hydrogen (pH 7.4).All the animals drank water ad libitum .After 4weeks,the rats were anesthetized with diethyl ether and blood samples were collected from the

abdominal aorta.The liver was then immediately excised,frozen in liquid nitrogen,and stored at à80 C until use.All the animal experiment protocols were in accordance with the ‘‘Guidelines for Animal Experimentation of the Japanese Association for Labo-ratory Animal Science,’’and were approved by the Animal Use and Care Committee of Mercian Cleantec Corporation.

Body weight and water intake showed no signi?cant between-group di?erences during the 4-week adminis-tration period (data not shown).As an index of hepatic and plasmic lipid peroxidation,thiobarbituric acid reactive substances (TBARS)were measured by the Material Research Center (Kisarazu,Japan)using a Bioxytech LPO-586kit (Percipio Biosciences,Foster City,CA),and were compared across groups.The values were represented as mean ?SE (n ?8),and di?erences were examined by Student’s t -test at a signi?cance threshold of p <0:05.TBARS were sig-ni?cantly lower in the HW group (0:177?0:006nmol malondialdehyde/mg protein)than in the control group (0:217?0:016nmol malondialdehyde/mg protein),suggesting that oxidative stress was reduced in the HW group.In addition,plasmic TBARS values,0:176?0:028m M and 0:151?0:021m M in the control and the HW group respectively,were not signi?cantly di?erent from each other at p <0:05.Four liver samples with approximately average levels of hepatic TBARS were selected from each group and subjected to DNA microarray analysis.

Total RNA was prepared from the liver samples,and DNA microarray analysis was performed as described previously.4)The raw microarray data (CEL ?les)were quanti?ed using Factor Analysis for Robust Microarray Summarization (FARMS)5)with the statis-tical language R 6)and Bioconductor.7)All microarray data were submitted to the National Center for Bio-technology Information (NCBI)Gene Expression Om-nibus (https://www.wendangku.net/doc/f514158868.html,/geo/,GEO Series ID GSE26363).Hierarchical clustering analysis revealed

To whom correspondence should be addressed.Tel:+81-3-5841-1128;Fax:+81-3-5841-1127;E-mail:aynakai@mail.ecc.u-tokyo.ac.jp

Abbreviations :DEGs,di?erentially expressed genes;FARMS,factor analysis for robust microarray summarization;FDR,false discovery rate;GO,Gene Ontology;HMG,hydroxymethylglutaryl;RP,rank products;TBARS,thiobarbituric acid reactive

substances

Biosci.Biotechnol.Biochem.,75(4),774–776,2011

Note

that each group formed a distinct cluster (Fig.1),indicating that the gene expression pro?les di?ered between the HW and the control group.

To determine the speci?c e?ects of hydrogen water on gene expression,di?erentially expressed genes (DEGs)between the two groups were identi?ed by applying the rank products (RP)method 8)to the FARMS quanti?ed data.A recent study reported that the RP method together with a FARMS preprocessing algo-rithm was one of the best combinations for accurate DEG detection.9)With the false discovery rate (FDR)signi?cance <0:05,548upregulated and 695down-regulated genes were selected.

To identify over-represented Gene Ontology (GO)terms in the selected genes,a functional annotation tool of the Database for Annotation,Visualization,and Integrated Discovery (DAVID;https://www.wendangku.net/doc/f514158868.html,/)10)and QuickGO 11)were used.GO terms with Benjamini and Hochberg FDR 12)-corrected p -values <0:1were regarded as signi?cantly https://www.wendangku.net/doc/f514158868.html,ing these criteria,no signi?cantly enriched GO terms were present in the downregulated gene set.The signi?cantly enriched GO terms for genes that were upregulated by hydrogen water treatment are summa-rized in Table 1.The enriched GO term with the lowest p -value was oxidation-reduction,which re?ects many genes that encode oxidoreductase proteins involved in steroid metabolism,such as Cyp27a1,Hsd17b6,and Sc5dl,and amino acid metabolism,such as Cdo1,Glud1,and Prodh (Fig.2).Moreover,genes related to the sterol biosynthetic process,cellular carbohydrate biosynthetic process,glycogen metabolic process,and coenzyme metabolic process were also over-represented in the upregulated gene set (Table 1).These GO terms shared genes for key proteins,including Gck,G6pc,and Hmgcr (Fig.2).Notably,the genes involved in the cholesterol biosynthetic pathway,including rate-limiting enzyme hydroxymethylglutaryl (HMG)-CoA reductase (Hmgcr),were also signi?cantly upregulated (Fig.2).Administration of hydrogen water to apolipoprotein E-knockout mice has been reported to suppress atherosclerosis,perhaps due to delayed very low-and low-density lipoprotein oxidation and phagocytosis.3)Decreases in serum cholesterol might also induce upregulation of the sterol synthesis genes.For example,rats fed soybean protein-containing diets showed decreased serum cholesterol levels and signi?cantly increased hepatic expression of the genes encoding sterol-catabolic proteins,including HMG-CoA reduc-tase.13)Actually,we observed that primary bile acid synthesis pathway-and steroid hormone biosynthesis pathway-related genes such as Cyp27a1,Cyp3a2,and Hsd17b6(Fig.2)were upregulated in the HW group.This result suggests that cholesterol catabolism was promoted by hydrogen water administration,resulting in upregulation of the genes for cholesterol synthesis.Our major ?nding in the present study was that drinking of hydrogen water altered the hepatic gene expression pro?le.Taken together with previous studies,the hepatic oxidoreduction-related gene upregulation observed in this study appears to con?rm the ?ndings reported to date 1–3)concerning the antioxidant e?ect of

H W 3

H W 1

H W 2

H W 4

C 3

C 1

C 2

C 4

0.008

0.010

0.012

0.0140.0160.0180.020

Fig.1.Hierarchical Clustering Dendrograms from FARMS-Quanti-?ed DNA Microarray Data.

HW,hydrogen water group;C,control group.Numbers represent independent samples.The vertical scale represents between-cluster

distances.

Table 1.Signi?cantly Enriched GO Terms (p <0:1)Identi?ed among the Top 548Upregulated Genes GO-ID GO term

FDR-corrected p -value

GO terms with no p -value indicate no signi?cance.??FDR-corrected p -values of the categories appearing in the deepest hierarchy are shadowed.

E?ects of Hydrogen Water on Hepatic Gene Expression 775

hydrogen water.The present study focused speci?cally on transcriptomics.A more detailed investigation of this phenomenon has not yet been conducted.Further experimentation is necessary to understand its under-lying mechanisms better.

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Fig.2.Venn Diagrams Representing the Association of Hydrogen Water-Induced Upregulated Genes with Multiple GO Terms.

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776Y.N AKAI et al.

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缩略词英文全称中文全称 ALT alanine aminotransferase / 谷丙转氨酶/丙氨酸氨基转移酶glutamic pyruvic transaminase (GPT) Anti-HBe hepatitis B “e”antibody 乙型肝炎e 抗体 Anti-HBs hepatitis B surface antibody 乙型肝炎表面抗体 APC antigen presenting cell 抗原提呈细胞 APC allophycocyanin 异藻蓝蛋白 AST aspartate amino transferase / 谷草转氨酶/天冬氨酸氨基转移酶glutamic oxaloacetic transaminase (GOT) BTLA B and T lymphocyte attenuator B、T 淋巴细胞衰减子 CHB chronic hepatic B 慢性乙型肝炎 CK cytokine 细胞因子 CTL(Tc) cytotoxic T lymphocytes 细胞毒T 淋巴细胞 DC dendritic cell 树突状细胞 DEPC diethyl pyrocarbonate 二乙基焦磷酰胺 DMSO dimethyl sulfoxide 二甲基亚砜 DNA deoxyribonucleic acid 脱氧核糖核酸 dsRNA double-stranded RNA 双链RNA EDTA ethylene diamine tetraacetic acid 乙二胺四乙酸FCM flow cytometry 流式细胞仪 FCS fetal calf serum 胎牛血清 Fig Figure 图表 FITC fluorescent isothiocyante 异硫氰酸荧光素GAPDH glyceraldehydes phosphate dehydrogenase 磷酸甘油醛脱氢酶H hour 小时 HBV hepatitis B virus 乙型肝炎病毒 HBcAb hepatitis B core antibody 乙型肝炎核心抗体 HBeAg hepatitis B “e” antigen乙型肝炎e 抗原 HBsAg hepatitis B surface antigen 乙型肝炎表面抗原 HCC hepatocellular carcinoma 肝细胞癌 HCV hepatitis C virus 丙型肝炎病毒 HDV hepatitis D Virus 丁型肝炎病毒 HIV human immunodeficiency virus 人类免疫缺陷病毒 IFN-αinterferon-α干扰素α IFN-βinterferon-β干扰素β IFN-γinterferon-γ干扰素γ IL interleukin 白细胞介素 LAG-3 lymphocyte activation gene-3 淋巴细胞活化基因-3 LDT Telbivudine (Sebivo) 替比夫定（素比伏） LPS lipopolysaccharide 脂多糖1 ALT alanine aminotransferase / 谷丙转氨酶/丙氨酸氨基 glutamic pyruvic transaminase (GPT) Anti-HBe hepatitis B “e”antibody 乙型肝炎e 抗体 Anti-HBs hepatitis B surface antibody 乙型肝炎表面抗体

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