Chlorogenic Acid Differentially Alters Hepatic and Small Intestinal Thiol Redox Status Without Protecting Against Azoxymethane-Induced Colon Carcinogenesis in Mice

REFERENCES

• US Cancer Statistics Working Group . 2005 . United States Cancer Statistics: 1999–2002 Incidence and Mortality Web-Based Report Version , Atlanta, GA : Department of Health and Human Services, Centers for Disease Control and Prevention, and National Cancer Institute . Available from: http://www.cdc.gov/cancer/npcr/uscs/index.htmAccessed August 21, 2008
   Google Scholar
• American Cancer Society . 2006 . Overview: colon and rectum. What is colon cancer? , Atlanta, GA : American Cancer Society, Inc. .
   Google Scholar
• Doyle , V C . 2007 . Nutrition and colorectal cancer risk: a literature review . Gastroenterol Nurs , 30 : 178 – 182 . 182 – 173 .
   PubMed Web of Science ®Google Scholar
• Schatzkin , A , Mouw , T , Park , Y , Subar , A F Kipnis , V . 2007 . Dietary fiber and whole-grain consumption in relation to colorectal cancer in the NIH–AARP Diet and Health Study . Am J Clin Nutr , 85 : 1353 – 1360 .
   PubMed Web of Science ®Google Scholar
• Larsson , S C and Wolk , A . 2006 . Meat consumption and risk of colorectal cancer: a meta-analysis of prospective studies . Int J Cancer , 119 : 2657 – 2664 .
   PubMed Web of Science ®Google Scholar
• Michels , K B , Giovannucci , E , Chan , A T , Singhania , R Fuchs , C S . 2006 . Fruit and vegetable consumption and colorectal adenomas in the Nurses' Health Study . Cancer Res , 66 : 3942 – 3953 .
   PubMed Web of Science ®Google Scholar
• Napolitano , A , Cascone , A , Graziani , G , Ferracane , R Scalfi , L . 2004 . Influence of variety and storage on the polyphenol composition of apple flesh . J Agric Food Chem , 52 : 6526 – 6531 .
   PubMed Web of Science ®Google Scholar
• Adhami , V M , Ahmad , N and Mukhtar , H . 2003 . Molecular targets for green tea in prostate cancer prevention . J Nutr , 133 : 2417S – 2424S .
   PubMed Web of Science ®Google Scholar
• Tessitore , L , Davit , A , Sarotto , I and Caderni , G . 2000 . Resveratrol depresses the growth of colorectal aberrant crypt foci by affecting bax and p21(CIP) expression . Carcinogenesis , 21 : 1619 – 1622 .
   PubMed Web of Science ®Google Scholar
• Knekt , P , Kumpulainen , J , Jarvinen , R , Rissanen , H Heliovaara , M . 2002 . Flavonoid intake and risk of chronic diseases . Am J Clin Nutr , 76 : 560 – 568 .
   PubMed Web of Science ®Google Scholar
• Olsson , M E , Gustavsson , K E , Andersson , S , Nilsson , A and Duan , R D . 2004 . Inhibition of cancer cell proliferation in vitro by fruit and berry extracts and correlations with antioxidant levels . J Agric Food Chem , 52 : 7264 – 7271 .
   PubMed Web of Science ®Google Scholar
• Gonthier , M P , Verny , M A , Besson , C , Remesy , C and Scalbert , A . 2003 . Chlorogenic acid bioavailability largely depends on its metabolism by the gut microflora in rats . J Nutr , 133 : 1853 – 1859 .
   PubMed Web of Science ®Google Scholar
• Scalbert , A and Williamson , G . 2000 . Dietary intake and bioavailability of polyphenols . J Nutr , 130 : 2073S – 2085S .
   PubMed Web of Science ®Google Scholar
• Feng , R , Lu , Y , Bowman , L L , Qian , Y Castranova , V . 2005 . Inhibition of activator protein-1, NF-kappaB, and MAPKs and induction of phase 2 detoxifying enzyme activity by chlorogenic acid . J Biol Chem , 280 : 27888 – 27895 .
   PubMed Web of Science ®Google Scholar
• Zhang , J , Stanley , R A , Adaim , A , Melton , L D and Skinner , M A . 2006 . Free radical scavenging and cytoprotective activities of phenolic antioxidants . Mol Nutr Food Res , 50 : 996 – 1005 .
   PubMed Web of Science ®Google Scholar
• Tavani , A and La Vecchia , C . 2004 . Coffee, decaffeinated coffee, tea, and cancer of the colon and rectum: a review of epidemiological studies, 1990-2003 . Cancer Causes Control , 15 : 743 – 757 .
   PubMed Web of Science ®Google Scholar
• Kono , Y , Shibata , H , Kodama , Y and Sawa , Y . 1995 . The suppression of the N-nitrosating reaction by chlorogenic acid . Biochem J , 312 : 947 – 953 . (Pt 3)
   PubMed Web of Science ®Google Scholar
• Matsunaga , K , Katayama , M , Sakata , K , Kuno , T Yoshida , K . 2002 . Inhibitory effects of chlorogenic acid on azoxymethane-induced colon carcinogenesis in male F344 rats . Asian Pac J Cancer Prev , 3 : 163 – 166 .
   PubMedGoogle Scholar
• Stensvold , I and Jacobsen , B K . 1994 . Coffee and cancer: a prospective study of 43,000 Norwegian men and women . Cancer Causes Control , 5 : 401 – 408 .
   PubMed Web of Science ®Google Scholar
• Brown , S R , Cann , P A and Read , N W . 1990 . Effect of coffee on distal colon function . Gut , 31 : 450 – 453 .
   PubMed Web of Science ®Google Scholar
• Tavani , A and La Vecchia , C . 2000 . Coffee and cancer: a review of epidemiological studies, 1990-1999 . Eur J Cancer Prev , 9 : 241 – 256 .
   PubMed Web of Science ®Google Scholar
• Michels , K B , Willett , W C , Fuchs , C S and Giovannucci , E . 2005 . Coffee, tea, and caffeine consumption and incidence of colon and rectal cancer . J Natl Cancer Inst , 97 : 282 – 292 .
   PubMed Web of Science ®Google Scholar
• Higdon , J V and Frei , B . 2006 . Coffee and health: a review of recent human research . Crit Rev Food Sci Nutr , 46 : 101 – 123 .
   PubMed Web of Science ®Google Scholar
• La Vecchia , C and Tavani , A . 2007 . Coffee and cancer risk: an update . Eur J Cancer Prev , 16 : 385 – 389 .
   PubMed Web of Science ®Google Scholar
• Giovannucci , E . 1998 . Meta-analysis of coffee consumption and risk of colorectal cancer . Am J Epidemiol , 147 : 1043 – 1052 .
   PubMed Web of Science ®Google Scholar
• Lee , K J , Inoue , M , Otani , T , Iwasaki , M , Sasazuki , S and Tsugane , S . 2007 . Coffee consumption and risk of colorectal cancer in a population-based prospective cohort of Japanese men and women . Int J Cancer , 121 : 1312 – 1318 .
   PubMed Web of Science ®Google Scholar
• Mori , H , Kawabata , K , Matsunaga , K , Ushida , J , Fujii , K , Hara , A , Tanaka , T and Murai , H . 2000 . Chemopreventive effects of coffee bean and rice constituents on colorectal carcinogenesis . Biofactors , 12 : 101 – 105 .
   PubMed Web of Science ®Google Scholar
• Tao , K S , Wang , W , Wang , L , Cao , D Y , Li , Y Q , Wu , S X and Dou , K F . 2008 . The multifaceted mechanisms for coffee's anti-tumorigenic effect on liver . Med Hypotheses ,
   Google Scholar
• Chen , Y , Jungsuwadee , P , Vore , M , Butterfield , D A and St. Clair , D K . 2007 . Collateral damage in cancer chemotherapy: oxidative stress in nontargeted tissues . Mol Interv , 7 : 147 – 156 .
   PubMed Web of Science ®Google Scholar
• Rosenberg , D W and Mankowski , D C . 1994 . Induction of cyp2e-1 protein in mouse colon . Carcinogenesis , 15 : 73 – 78 .
   PubMed Web of Science ®Google Scholar
• Dolara , P , Luceri , C , De Filippo , C , Femia , A P , Giovannelli , L , Caderni , G , Cecchini , C , Silvi , S , Orpianesi , C and Cresci , A . 2005 . Red wine polyphenols influence carcinogenesis, intestinal microflora, oxidative damage and gene expression profiles of colonic mucosa in F344 rats . Mutat Res , 591 : 237 – 246 .
   PubMed Web of Science ®Google Scholar
• Jefferies , H , Bot , J , Coster , J , Khalil , A , Hall , J C and McCauley , R D . 2003 . The role of glutathione in intestinal dysfunction . J Invest Surg , 16 : 315 – 323 .
   PubMed Web of Science ®Google Scholar
• Jones , D P . 2006 . Redefining oxidative stress . Antioxid Redox Signal , 8 : 1865 – 1879 .
   PubMed Web of Science ®Google Scholar
• Giles , G I . 2006 . The redox regulation of thiol dependent signaling pathways in cancer . Curr Pharm Des , 12 : 4427 – 4443 .
   PubMed Web of Science ®Google Scholar
• Franco , R , Schoneveld , O J , Pappa , A and Panayiotidis , M I . 2007 . The central role of glutathione in the pathophysiology of human diseases . Arch Physiol Biochem , 113 : 234 – 258 .
   PubMedGoogle Scholar
• Huber , W W and Parzefall , W . 2007 . Thiols and the chemoprevention of cancer . Curr Opin Pharmacol , 7 : 404 – 409 .
   PubMed Web of Science ®Google Scholar
• Boateng , J , Verghese , M , Shackelford , L , Walker , L T Khatiwada , J . 2007 . Selected fruits reduce azoxymethane (AOM)-induced aberrant crypt foci (ACF) in Fisher 344 male rats . Food Chem Toxicol , 45 : 725 – 732 .
   PubMed Web of Science ®Google Scholar
• Williams , D , Verghese , M , Walker , L T , Boateng , J Shackelford , L . 2007 . Flaxseed oil and flax seed meal reduce the formation of aberrant crypt foci (ACF) in azoxymethane-induced colon cancer in Fisher 344 male rats . Food Chem Toxicol , 45 : 153 – 159 .
   PubMed Web of Science ®Google Scholar
• Boateng , J , Verghese , M , Chawan , C B , Shackelford , L Walker , L T . 2006 . Red palm oil suppresses the formation of azoxymethane (AOM) induced aberrant crypt foci (ACF) in Fisher 344 male rats . Food Chem Toxicol , 44 : 1667 – 1673 .
   PubMedGoogle Scholar
• Nambiar , P R , Girnun , G , Lillo , N A , Guda , K Whiteley , H E . 2003 . Preliminary analysis of azoxymethane induced colon tumors in inbred mice commonly used as transgenic/knockout progenitors . Int J Oncol , 22 : 145 – 150 .
   PubMed Web of Science ®Google Scholar
• Nambiar , P R , Nakanishi , M , Gupta , R , Cheung , E Firouzi , A . 2004 . Genetic signatures of high- and low-risk aberrant crypt foci in a mouse model of sporadic colon cancer . Cancer Res , 64 : 6394 – 6401 .
   PubMed Web of Science ®Google Scholar
• Reeves , P G , Nielsen , F H and Fahey , G C Jr. 1993 . AIN-93 purified diets for laboratory rodents: final report of the American Institute of Nutrition ad hoc writing committee on the reformulation of the AIN-76A rodent diet . J Nutr , 123 : 1939 – 1951 .
   PubMed Web of Science ®Google Scholar
• Clifford , M N . 1999 . Chlorogenic acids and other cinnamates—nature, occurrence, and dietary burden . J Sci Food Agric , 79 : 362 – 372 .
   Web of Science ®Google Scholar
• Wen , D , Li , C , Di , H , Liao , Y and Liu , H . 2005 . A universal HPLC method for the determination of phenolic acids in compound herbal medicines . J Agric Food Chem , 53 : 6624 – 6629 .
   PubMed Web of Science ®Google Scholar
• Bird , R P . 1987 . Observation and quantification of aberrant crypts in the murine colon treated with a colon carcinogen: preliminary findings . Cancer Lett , 37 : 147 – 151 .
   PubMed Web of Science ®Google Scholar
• Papanikolaou , A , Wang , Q S , Papanikolaou , D , Whiteley , H E and Rosenberg , D W . 2000 . Sequential and morphological analyses of aberrant crypt foci formation in mice of differing susceptibility to azoxymethane-induced colon carcinogenesis . Carcinogenesis , 21 : 1567 – 1572 .
   PubMed Web of Science ®Google Scholar
• Ilsley , J N , Nakanishi , M , Flynn , C , Belinsky , G S De Guise , S . 2005 . Cytoplasmic phospholipase A2 deletion enhances colon tumorigenesis . Cancer Res , 65 : 2636 – 2643 .
   PubMedGoogle Scholar
• Fariss , M W and Reed , D J . 1987 . High-performance liquid chromatography of thiols and disulfides: dinitrophenol derivatives . Methods Enzymol , 143 : 101 – 109 .
   PubMed Web of Science ®Google Scholar
• Metayer , S , Seiliez , I , Collin , A , Duchene , S Mercier , Y . 2008 . Mechanisms through which sulfur amino acids control protein metabolism and oxidative status . J Nutr Biochem , 19 : 207 – 215 .
   PubMed Web of Science ®Google Scholar
• Sohn , O S , Fiala , E S , Requeijo , S P , Weisburger , J H and Gonzalez , F J . 2001 . Differential effects of CYP2E1 status on the metabolic activation of the colon carcinogens azoxymethane and methylazoxymethanol . Cancer Res , 61 : 8435 – 8440 .
   PubMed Web of Science ®Google Scholar
• Neufert , C , Becker , C and Neurath , M F . 2007 . An inducible mouse model of colon carcinogenesis for the analysis of sporadic and inflammation-driven tumor progression . Nat Protoc , 2 : 1998 – 2004 .
   PubMed Web of Science ®Google Scholar
• Guda , K , Marino , J N , Jung , Y , Crary , K Dong , M . 2007 . Strain-specific homeostatic responses during early stages of azoxymethane-induced colon tumorigenesis in mice . Int J Oncol , 31 : 837 – 842 .
   PubMedGoogle Scholar
• Bird , R P and Good , C K . 2000 . The significance of aberrant crypt foci in understanding the pathogenesis of colon cancer . Toxicol Lett , 112–113 : 395 – 402 .
   PubMed Web of Science ®Google Scholar
• Mori , H , Hata , K , Yamada , Y , Kuno , T and Hara , A . 2005 . Significance and role of early-lesions in experimental colorectal carcinogenesis . Chem Biol Interact , 155 : 1 – 9 .
   PubMed Web of Science ®Google Scholar
• Stevens , R G , Swede , H and Rosenberg , D W . 2006 . Epidemiology of colonic aberrant crypt foci: review and analysis of existing studies . Cancer Lett , 252 : 171 – 183 .
   PubMedGoogle Scholar
• Stevens , R G , Swede , H , Heinen , C D , Jablonski , M Grupka , M . 2006 . Aberrant crypt foci in patients with a positive family history of sporadic colorectal cancer . Cancer Lett , 248 : 262 – 268 .
   PubMedGoogle Scholar
• Dupas , C , Marsset Baglieri , A , Ordonaud , C , Tome , D and Maillard , M N . 2006 . Chlorogenic acid is poorly absorbed, independently of the food matrix: A Caco-2 cells and rat chronic absorption study . Mol Nutr Food Res , 50 : 1053 – 1060 .
   PubMed Web of Science ®Google Scholar
• Lafay , S , Morand , C , Manach , C , Besson , C and Scalbert , A . 2006 . Absorption and metabolism of caffeic acid and chlorogenic acid in the small intestine of rats . Br J Nutr , 96 : 39 – 46 .
   PubMed Web of Science ®Google Scholar
• Olthof , M R , Hollman , P C , Buijsman , M N , van Amelsvoort , J M and Katan , M B . 2003 . Chlorogenic acid, quercetin-3-rutinoside and black tea phenols are extensively metabolized in humans . J Nutr , 133 : 1806 – 1814 .
   PubMed Web of Science ®Google Scholar
• Davies , M J , Bowey , E A , Adlercreutz , H , Rowland , I R and Rumsby , P C . 1999 . Effects of soy or rye supplementation of high-fat diets on colon tumor development in azoxymethane-treated rats . Carcinogenesis , 20 : 927 – 931 .
   PubMedGoogle Scholar
• Lam , L K , Sparnins , V L and Wattenberg , L W . 1982 . Isolation and identification of kahweol palmitate and cafestol palmitate as active constituents of green coffee beans that enhance glutathione S-transferase activity in the mouse . Cancer Res , 42 : 1193 – 1198 .
   PubMed Web of Science ®Google Scholar
• Cavin , C , Holzhauser , D , Constable , A , Huggett , A C and Schilter , B . 1998 . The coffee-specific diterpenes cafestol and kahweol protect against aflatoxin B1-induced genotoxicity through a dual mechanism . Carcinogenesis , 19 : 1369 – 1375 .
   PubMed Web of Science ®Google Scholar
• Morioka , T , Suzui , M , Nabandith , V , Inamine , M Aniya , Y . 2004 . The modifying effect of Peucedanum japonicum, a herb in the Ryukyu Islands, on azoxymethane-induced colon preneoplastic lesions in male F344 rats . Cancer Lett , 205 : 133 – 141 .
   PubMed Web of Science ®Google Scholar
• Morishita , Y , Yoshimi , N , Kawabata , K , Matsunaga , K Sugie , S . 1997 . Regressive effects of various chemopreventive agents on azoxymethane-induced aberrant crypt foci in the rat colon . Jpn J Cancer Res , 88 : 815 – 820 .
   PubMedGoogle Scholar
• Exon , J H , Magnuson , B A , South , E H and Hendrix , K . 1998 . Effect of dietary chlorogenic acid on multiple immune functions and formation of aberrant crypt foci in rats . J Toxicol Environ Health A , 53 : 375 – 384 .
   PubMed Web of Science ®Google Scholar
• Hariri , L P , Qiu , Z , Tumlinson , A R , Besselsen , D G Gerner , E W . 2007 . Serial endoscopy in azoxymethane treated mice using ultra-high resolution optical coherence tomography . Cancer Biol Ther , 6 : 1753 – 1762 .
   PubMed Web of Science ®Google Scholar
• Ilsley , J N , Belinsky , G S , Guda , K , Zhang , Q Huang , X . 2004 . Dietary iron promotes azoxymethane-induced colon tumors in mice . Nutr Cancer , 49 : 162 – 169 .
   PubMed Web of Science ®Google Scholar
• Bissahoyo , A , Pearsall , R S , Hanlon , K , Amann , V Hicks , D . 2005 . Azoxymethane is a genetic background-dependent colorectal tumor initiator and promoter in mice: effects of dose, route, and diet . Toxicol Sci , 88 : 340 – 345 .
   PubMed Web of Science ®Google Scholar
• Rosenberg , D W , Giardina , C and Tanaka , T . 2009 . Mouse models for the study of colon carcinogenesis . Carcinogenesis , 30 : 183 – 196 .
   PubMed Web of Science ®Google Scholar
• Lafay , S , Gil-Izquierdo , A , Manach , C , Morand , C Besson , C . 2006 . Chlorogenic acid is absorbed in its intact form in the stomach of rats . J Nutr , 136 : 1192 – 1197 .
   PubMed Web of Science ®Google Scholar
• Nardini , M , Cirillo , E , Natella , F and Scaccini , C . 2002 . Absorption of phenolic acids in humans after coffee consumption . J Agric Food Chem , 50 : 5735 – 5741 .
   PubMed Web of Science ®Google Scholar
• Azuma , K , Ippoushi , K , Nakayama , M , Ito , H Higashio , H . 2000 . Absorption of chlorogenic acid and caffeic acid in rats after oral administration . J Agric Food Chem , 48 : 5496 – 5500 .
   PubMed Web of Science ®Google Scholar
• Cenesiz , S , Devrim , A K , Kamber , U and Sozmen , M . 2008 . The effect of kefir on glutathione (GSH), malondialdehyde (MDA) and nitric oxide (NO) levels in mice with colonic abnormal crypt formation (ACF) induced by azoxymethane (AOM) . Dtsch Tierarztl Wochenschr , 115 : 15 – 19 .
   PubMedGoogle Scholar
• Moridani , M Y , Scobie , H , Jamshidzadeh , A , Salehi , P and O'Brien , P J . 2001 . Caffeic acid, chlorogenic acid, and dihydrocaffeic acid metabolism: glutathione conjugate formation . Drug Metab Dispos , 29 : 1432 – 1439 .
   PubMed Web of Science ®Google Scholar
• Panzella , L , Napolitano , A and d'Ischia , M . 2003 . Oxidative conjugation of chlorogenic acid with glutathione: structural characterization of addition products and a new nitrite-promoted pathway . Bioorg Med Chem , 11 : 4797 – 4805 .
   PubMed Web of Science ®Google Scholar