European Journal of Cancer
Volume 41, Issue 13 , Pages 1941-1954 , September 2005

Beer constituents as potential cancer chemopreventive agents

Received 24 March 2005 ,Accepted 1 April 2005.

References 

  1. Piendl A. Über den Stellenwert des Biers in der heutigen Ernährung. Brauwelt. 1989;14:546–552
  2. Stevens JF, Miranda CL, Buhler DR, et al. Chemistry and biology of hop flavonoids. J Am Soc Brew Chem. 1998;56:136–145
  3. De Keukeleire D, De Cooman L, Rong H, et al. Functional properties of hop polyphenols. In: Gross , et al. editor. Plant polyphenols 2: chemistry, biology, pharmacology, ecology. New York: Kluwer Academics/Plenum Publishers; 1999;p. 739–760
  4. Taylor AW, Barofsky E, Kennedy JA, et al. Hop (Humulus lupulus L.) proanthocyanidins characterized by mass spectrometry, acid catalysis, and gel permeation chromatography. J Agric Food Chem. 2003;51:4101–4110
  5. De Keukeleire D. Fundamentals of beer and hop chemistry. Quím Nova. 2000;23:108–112
  6. De Keukeleire J, Ooms G, Heyerick A, et al. Formation and accumulation of alpha-acids, beta-acids, desmethylxanthohumol, and xanthohumol during flowering of hops (Humulus lupulus L.). J Agric Food Chem. 2003;51:4436–4441
  7. Knorr F. Über Polyphenole im Brauprozess. Z Lebens Unters-Forsch. 1978;166:228–233
  8. Madigan D, McMurrough I, Smyth MR. Determination of proanthocyanidins and catechins in beer and barley by high-performance liquid chromatography with dual-electrode electrochemical detection. Analyst. 1994;119:863–868
  9. McMurrough I, Baert T. Identification of proanthocyanidins in beer and their direct measurement with a dual electrode electrochemical detector. J Inst Brew. 1994;100:409–416
  10. Friedrich W, Eberhardt A, Galensa R. Investigation of proanthocyanidins by HPLC with electrospray ionization mass spectrometry. Eur Food Res Technol. 2000;211:56–64
  11. Doll R, Peto R, Hall E, et al. Mortality in relation to consumption of alcohol: 13 years’ observations on male British doctors. Br Med J. 1994;309:911–918
  12. Thun MJ, Peto R, Lopez AD, et al. Alcohol consumption and mortality among middle-aged and elderly U.S. adults. N Engl J Med. 1997;337:1705–1714
  13. Chou SP, Grant BF, Dawson DA. Alcoholic beverage preference and risks of alcohol-related medical consequences: a preliminary report from the National Longitudinal Alcohol Epidemiologic Survey. Alcohol Clin Exp Res. 1998;22:1450–1455
  14. Denke MA. Nutritional and health benefits of beer. Am J Med Sci. 2000;320:320–326
  15. Klatsky AL, Friedman GD, Armstrong MA, et al. Wine, liquor, beer, and mortality. Am J Epidemiol. 2003;158:585–595
  16. Potter J, et al. Food, Nutrition and the Prevention of Cancer: a global perspective. WCRF/AICR Report, 1997.
  17. Spiegelhalder B, Eisenbrand G, Preussman R. Occurrence of volatile nitrosamines in food. In:  Walker EA,  Griciute L,  Castegnaro M editor. N-nitroso compounds: analysis, formation, and occurrence (Publ. No. 105). Lyon, France: IRAC; 1980;p. 467–479
  18. Lijinsky W. N-nitroso compounds in the diet. Mut Res. 1999;443:129–138
  19. Bandera EV, Freudenheim JL, Vena JE. Alcohol consumption and lung cancer: a review of the epidemiologic evidence. Cancer Epidemiol Biomarkers Prev. 2001;10:813–821
  20. Grønbæk M, Becker U, Johansen D, et al. Type of alcohol consumed and mortality from all causes, coronary heart disease, and cancer. Ann Intern Med. 2000;133:411–419
  21. Longnecker MP, Orza MJ, Adams ME, et al. A meta-analysis of alcoholic beverage consumption in relation to risk of colorectal cancer. Cancer Causes Control. 1990;1:59–68
  22. Kune GA, Vitetta L. Alcohol consumption and the etiology of colorectal cancer: a review of the scientific evidence from 1957 to 1991. Nutr Cancer. 1992;18:97–111
  23. Ruf JC. Overview of epidemiological studies on wine, health and mortality. Drugs Exp Clin Res. 2003;29:173–179
  24. Kaerlev L, Teglbjaerg PS, Sabroe S, et al. Is there an association between alcohol intake or smoking and small bowel adenocarcinoma? Results from a European multi-center case-control study. Cancer Causes Control. 2000;11:791–797
  25. Jain MG, Hislop GT, Howe GR, et al. Alcohol and other beverage use and prostate cancer risk among Canadian men. Int J Cancer. 1998;78:707–711
  26. Mahabir S, Leitzmann MF, Virtanen MJ, et al. Prospective study of alcohol drinking and renal cell cancer risk in a cohort of finnish male smokers. Cancer Epidemiol Biomarkers Prev. 2005;14:170–175
  27. Nelson RL, Samelson SL. Neither dietary ethanol nor beer augments experimental colon carcinogenesis in rats. Dis Colon Rectum. 1985;28:460–462
  28. Hamilton SR, Hyland J, McAvinchey D, et al. Effects of chronic dietary beer and ethanol consumption on experimental colonic carcinogenesis by azoxymethane in rats. Cancer Res. 1987;47:1551–1559
  29. Nozawa H, Yoshida A, Tajima O, et al. Intake of beer inhibits azoxymethane-induced colonic carcinogenesis in male Fischer 344 rats. Int J Cancer. 2004;108:404–411
  30. Anonymous . Good news for beer drinkers. Science. 1996;274:1309–1310
  31. Arimoto-Kobayashi S, Sugiyama C, Harada N, et al. Inhibitory effects of beer and other alcoholic beverages on mutagenesis and DNA adduct formation induced by several carcinogens. Agric Food Chem. 1999;47:221–230
  32. Kimura S, Hayatsu H, Arimoto-Kobayashi S. Glycine betaine in beer as an antimutagenic substance against 2-chloro-4-methylthiobutanoic acid, the sanma-fish mutagen. Mutat Res. 1999;39:267–276
  33. Arimoto-Kobayashi S, Takata J, Nakandakari N, et al. Inhibitory effects of heterocyclic amine-induced DNA adduct formation in mouse liver and lungs by beer. J Agric Food Chem. 2005;53:812–815
  34. Vinson JA, Mandarano M, Hirst M, et al. Phenol antioxidant quantity and quality in foods: beers and the effect of two types of beer on an animal model of atherosclerosis. J Agric Food Chem. 2003;51:5528–5533
  35. Ghiselli A, Natella F, Guidi A, et al. Beer increases plasma antioxidant capacity in humans. J Nutr Biochem. 2000;11:76–80
  36. Leupold G, Drawert F. Zur Analytik phenolischer Verbindungen im Bier. Brauwissenschaften. 1981;34:205–210
  37. Maillard MN, Berset C. Evolution of antioxidant activity during kilning: role of insoluble bound phenolic acids of barley and malt. J Agric Food Chem. 1995;43:1789–1793
  38. Gerhauser C, Alt AP, Klimo K, et al. Isolation and potential cancer chemopreventive activities of phenolic compounds of beer. Phytochem Rev. 2002;1:369–377
  39. Gerhauser C, Klimo K, Heiss E, et al. Mechanism-based in vitro screening of potential cancer chemopreventive agents. Mut Res. 2003;523–524:163–172
  40. Stevens JF, Page JE. Xanthohumol and related prenylflavonoids from hops and beer: to your good health!. Phytochemistry. 2004;65:1317–1330
  41. Stevens JF, Ivancic M, Hsu VL, et al. Prenylflavonoids from Humulus lupulus. Phytochemistry. 1997;44:1575–1585
  42. Stevens JF, Taylor AW, Clawson JE, et al. Fate of xanthohumol and related prenylflavonoids from hops to beer. J Agric Food Chem. 1999;47:2421–2428
  43. Gerhauser C, Frank N. New promising chemopreventive agents and mechanisms. In:  Vainio H editors. Handbook of experimental pharmacology. Heidelberg: Springer-Verlag; 2003;p. 289–305
  44. Jang M, Cai L, Udeani GO, et al. Cancer chemopreventive activity of resveratrol, a natural product derived from grapes. Science. 1997;275:218–220
  45. Gerhauser C, Alt A, Heiss E, et al. Cancer chemopreventive activity of xanthohumol, a natural product derived from hop. Mol Cancer Ther. 2002;1:959–969
  46. Henderson MC, Miranda CL, Stevens JF, et al. In vitro inhibition of human P450 enzymes by prenylated flavonoids from hop, Humulus lupulus. Xenobiotica. 2000;30:235–251
  47. Miranda CL, Yang YH, Henderson MC, et al. Prenylflavonoids from hops inhibit the metabolic activation of the carcinogenic heterocyclic amine 2-amino-3-methylimidazo[4,5-f]quinoline, mediated by cDNA-expressed human CYP1A2. Drug Metab Dispos. 2000;28:1297–1302
  48. Gross-Steinmeyer K, Stapleton PL, Liu F, et al. Phytochemical-induced changes in gene expression of carcinogen-metabolizing enzymes in cultured human primary hepatocytes. Xenobiotica. 2004;34:619–632
  49. Miranda CL, Aponso GL, Stevens JF, et al. Prenylated chalcones and flavanones as inducers of quinone reductase in mouse Hepa 1c1c7 cells. Cancer Lett. 2000;149:21–29
  50. Miranda CL, Stevens JF, Ivanov V, et al. Antioxidant and prooxidant actions of prenylated and nonprenylated chalcones and flavanones in vitro. J Agric Food Chem. 2000;48:3876–3884
  51. Rodriguez RJ, Miranda CL, Stevens JF, et al. Influence of prenylated and non-prenylated flavonoids on liver microsomal lipid peroxidation and oxidative injury in rat hepatocytes. Food Chem Toxicol. 2001;39:437–445
  52. Stevens JF, Miranda CL, Frei B, et al. Inhibition of peroxynitrite-mediated LDL oxidation by prenylated flavonoids: the alpha,beta-unsaturated keto functionality of 2′-hydroxychalcones as a novel antioxidant pharmacophore. Chem Res Toxicol. 2003;16:1277–1286
  53. Zhao F, Watanabe Y, Nozawa H, et al. Prenylflavonoids and phloroglucinol derivatives from hops (Humulus lupulus). J Nat Prod. 2005;68:43–49
  54. Zhao F, Nozawa H, Daikonnya A, et al. Inhibitors of nitric oxide production from hops (Humulus lupulus L.). Biol Pharm Bull. 2003;26:61–65
  55. Reid SE, Murthy MS, Kaufman M, et al. Endocrine and paracrine hormones in the promotion, progression and recurrence of breast cancer. Br J Surg. 1996;83:1037–1046
  56. Cos P, De Bruyne T, Apers S, et al. Phytoestrogens: recent developments. Planta Med. 2003;69:589–599
  57. Milligan SR, Kalita JC, Pocock V, et al. The endocrine activities of 8-prenylnaringenin and related hop (Humulus lupulus L.) flavonoids. J Clin Endocrinol Metab. 2000;85:4912–4915
  58. Kitaoka M, Kadokawa H, Sugano M, et al. Prenylflavonoids: a new class of non-steroidal phytoestrogen (Part 1). Isolation of 8-isopentenylnaringenin and an initial study on its structure–activity relationship. Planta Med. 1998;64:511–515
  59. Milligan SR, Kalita JC, Heyerick A, et al. Identification of a potent phytoestrogen in hops (Humulus lupulus L.) and beer. J Clin Endocrinol Metab. 1999;84:2249–2252
  60. Coldham NG, Horton R, Byford MF, et al. A binary screening assay for pro-oestrogens in food: metabolic activation using hepatic microsomes and detection with oestrogen sensitive recombinant yeast cells. Food Addit Contam. 2002;19:1138–1147
  61. Zierau O, Gester S, Schwab P, et al. Estrogenic activity of the phytoestrogens naringenin, 6-(1,1-dimethylallyl)naringenin and 8-prenylnaringenin. Planta Med. 2002;68:449–451
  62. Schaefer O, Humpel M, Fritzemeier KH, et al. 8-Prenyl naringenin is a potent ERalpha selective phytoestrogen present in hops and beer. J Steroid Biochem Mol Biol. 2003;84:359–360
  63. Bovee TF, Helsdingen RJ, Rietjens IM, et al. Rapid yeast estrogen bioassays stably expressing human estrogen receptors alpha and beta, and green fluorescent protein: a comparison of different compounds with both receptor types. J Steroid Biochem Mol Biol. 2004;91:99–109
  64. Miyamoto M, Matsushita Y, Kiyokawa A, et al. Prenylflavonoids: a new class of non-steroidal phytoestrogen (Part 2). Estrogenic effects of 8-isopentenylnaringenin on bone metabolism. Planta Med. 1998;64:516–519
  65. Milligan S, Kalita J, Pocock V, et al. Oestrogenic activity of the hop phyto-oestrogen, 8-prenylnaringenin. Reproduction. 2002;123:235–242
  66. Diel P, Thomae RB, Caldarelli A, et al. Regulation of gene expression by 8-prenylnaringenin in uterus and liver of Wistar rats. Planta Med. 2004;70:39–44
  67. Zierau O, Morrissey C, Watson RW, et al. Antiandrogenic activity of the phytoestrogens naringenin, 6-(1,1-dimethylallyl)naringenin and 8-prenylnaringenin. Planta Med. 2003;69:856–858
  68. Miranda CL, Stevens JF, Helmrich A, et al. Antiproliferative and cytotoxic effects of prenylated flavonoids from hops (Humulus lupulus) in human cancer cell lines. Food Chem Toxicol. 1999;37:271–285
  69. Goto K, Asai T, Hara S, et al. Enhanced antitumour activity of xanthohumol, a diacylglycerol acyltransferase inhibitor, under hypoxia. Cancer Lett. 2005;219:215–222
  70. Tabata N, Ito M, Tomoda H, et al. Xanthohumols, diacylglycerol acyltransferase inhibitors, from Humulus lupulus. Phytochemistry. 1997;46:683–687
  71. Casaschi A, Maiyoh GK, Rubio BK, et al. The chalcone xanthohumol inhibits triglyceride and apolipoprotein B secretion in HepG2 cells. J Nutr. 2004;134:1340–1346
  72. Tokalov SV, Henker Y, Schwab P, et al. Toxicity and cell cycle effects of synthetic 8-prenylnaringenin and derivatives in human cells. Pharmacology. 2004;71:46–56
  73. Sharma RA, Harris AL, Dalgleish AG, et al. Angiogenesis as a biomarker and target in cancer chemoprevention. Lancet Oncol. 2001;2:726–732
  74. Bertl E, Klimo K, Heiss E, et al. Identification of novel inhibitors of angiogenesis using a human in vitro anti-angiogenesis assay. Intern J Cancer Prev. 2004;1:47–61
  75. Bertl E, Herhaus C, Kapadia G, et al. Inhibition of endothelial cell functions by novel potential anti-angiogenic agents. Biochem Biophys Res Commun. 2004;325:287–295
  76. Bertl E. Inhibition of angiogenesis by potential cancer chemopreventive agents – Establishment of a human in vitro anti-angiogenesis assay and mechanistic evaluation of potent inhibitors. Ph.D. Thesis University of Heidelberg, 2005.
  77. Pepper MS, Hazel SJ, Humpel M, et al. 8-prenylnaringenin, a novel phytoestrogen, inhibits angiogenesis in vitro and in vivo. J Cell Physiol. 2004;199:98–107
  78. Rong H, Boterberg T, Maubach J, et al. 8-Prenylnaringenin, the phytoestrogen in hops and beer, upregulates the function of the E-cadherin/catenin complex in human mammary carcinoma cells. Eur J Cell Biol. 2001;80:580–585
  79. Buckwold VE, Wilson RJ, Nalca A, et al. Antiviral activity of hop constituents against a series of DNA and RNA viruses. Antiviral Res. 2004;61:57–62
  80. Wang Q, Ding ZH, Liu JK, et al. Xanthohumol, a novel anti-HIV-1 agent purified from hops Humulus lupulus. Antiviral Res. 2004;64:189–194
  81. Zierau O, Hauswald S, Schwab P, et al. Two major metabolites of 8-prenylnaringenin are estrogenic in vitro. J Steroid Biochem Mol Biol. 2004;92:107–110
  82. Yilmazer M, Stevens JF, Deinzer ML, et al. In vitro biotransformation of xanthohumo, a flavonoid from hops (Humulus lupulus), by rat liver microsomes. Drug Metab Dispos. 2001;29:223–231
  83. Yilmazer M, Stevens JF, Buhler DR. In vitro glucuronidation of xanthohumo, a flavonoid in hop and beer, by rat and human liver microsomes. FEBS Lett. 2001;491:252–256
  84. Herath WH, Ferreira D, Khan IA. Microbial transformation of XN. Phytochemistry. 2003;62:673–677
  85. Herath W, Ferreira D, Khan SI, et al. Identification and biological activity of microbial metabolites of xanthohumo. Chem Pharm Bull (Tokyo). 2003;51:1237–1240
  86. Nookandeh A, Frank N, Steiner F, et al. Xanthohumol metabolites in faeces of rats. Phytochemistry. 2004;65:561–570
  87. Nikolic D, Li Y, Chadwick LR, et al. Metabolism of xanthohumol and isoxanthohumol, prenylated flavonoids from hops (Humulus lupulus L.), by human liver microsomes. J Mass Spectrom. 2005;40:289–299
  88. Nookandeh A. Xanthohumol: Isolierung, Untersuchungen zur Stabilität, Metabolite, Bioverfügbarkeit und Pharmakokinetik. Ph.D. Thesis University of Saarbrücken, 2003.
  89. Avula B, Ganzera M, Warnick JE, et al. High-performance liquid chromatographic determination of xanthohumol in rat plasma, urine, and fecal samples. J Chromatogr Sci. 2004;42:378–382
  90. Wohlfart R. In: 5th ed..  Hänsel R,  Keller K,  Rimpler H,  Schneider G editor. Hagers Handbuch der Pharmazeutischen Praxis. Vol. 5:Berlin, Heidelberg: Springer; 1993;p. 447–458
  91. Schmalreck AF, Teuber M. Structural features determining the antibiotic potencies of natural and synthetic hop bitter resins, their precursors and derivatives. Can J Microbiol. 1975;21:205–212
  92. Tagashira M, Watanabe M, Uemitsu N. Antioxidative activity of hop bitter acids and their analogues. Biosci Biotechnol Biochem. 1995;59:740–742
  93. Tobe H, Muraki Y, Kitamura K, et al. Bone resorption inhibitors from hop extract. Biosci Biotechnol Biochem. 1997;61:158–159
  94. Yamamoto K, Wang J, Yamamoto S, et al. Suppression of cyclooxygenase-2 gene transcription by humulon of beer hop extract studied with reference to glucocorticoid. FEBS Lett. 2000;465:103–106
  95. Yasukawa K, Takeuchi M, Takido M. Humulon, a bitter in the hop, inhibits tumour promotion by 12-O-tetradecanoylphorbol-13-acetate in two-stage carcinogenesis in mouse skin. Oncology. 1995;52:156–158
  96. Honma Y, Tobe H, Makishima M, et al. Induction of differentiation of myelogenous leukaemia cells by humulone, a bitter in the hop. Leuk Res. 1998;22:605–610
  97. Tobe H, Kubota M, Yamaguchi M, et al. Apoptosis to HL-60 by humulone. Biosci Biotechnol Biochem. 1997;61:1027–1029
  98. Chen WJ, Lin JK. Mechanisms of cancer chemoprevention by hop bitter acids (beer aroma) through induction of apoptosis mediated by Fas and caspase cascades. J Agric Food Chem. 2004;52:55–64
  99. Shimamura M, Hazato T, Ashino H, et al. Inhibition of angiogenesis by humulone, a bitter acid from beer hop. Biochem Biophys Res Commun. 2001;289:220–224
  100. Shindo S, Tomatsu M, Nakada T, et al. Inhibition of aldose reductase activity by extracts from hop. J Inst Brew. 2002;108:344–347
  101. Yajima H, Ikeshima E, Shiraki M, et al. Isohumulones, bitter acids derived from hops, activate both peroxisome proliferator-activated receptor alpha and gamma and reduce insulin resistance. J Biol Chem. 2004;279:33456–33462
  102. Auwerx J. PPARgamma, the ultimate thrifty gene. Diabetologia. 1999;42:1033–1049
  103. Kersten S, Desvergne B, Wahli W. Roles of PPARs in health and disease. Nature. 2000;405:421–424
  104. Koeffler HP. Peroxisome proliferator-activated receptor and cancers. Clin Cancer Res. 2003;1:1–9
  105. Chappel CI, Smith SY, Chagnon M. Subchronic toxicity study of tetrahydroisohumulone and hexahydroisohumulone in the beagle dog. Food Chem Toxicol. 1998;36:915–922
  106. Soderberg U, Wachtmeister CA. Pharmacological effects of humulone on cats and rabbits. Acta Physiol Scand. 1955;34:90–98
  107. Liegeois C, Lermusieau G, Collin S. Measuring antioxidant efficiency of wort, malt, and hops against the 2,2′-azobis (2-amidinopropane) dihydrochloride-induced oxidation of an aqueous dispersion of linoleic acid. J Agric Food Chem. 2000;48:1129–1134
  108. Morales F, Jiménez-Pérez S. Peroxyl radical scavenging activites of melanoidins in aqueous systems. Eur Food Res Technol. 2004;218:515–520
  109. Faist V, Lindenmeier M, Geisler C, et al. Influence of molecular weight fractions isolated from roasted malt. J Agric Food Chem. 2002;50:602–606
  110. Achilli G, Cellerino GP, Gamache PH, et al. Identification and determination of phenolic constituents in natural beverages and plant extracts by means of a coulorimetric electrode array system. J Chromatogr. 1993;632:111–117
  111. Moll M, Fonknechten G, Carnielo M, et al. Technical quarterly. Master Brew Assoc Am. 1984;21:79–87
  112. Bartolomé B, Peña-Neira A, Gómez-Cordovés C. Phenolics and related substances in alcohol-free beer. Eur Food Res Technol. 2000;210:419–423
  113. Stevens JF, Taylor AW, Deinzer ML. Quantitative analysis of xanthohumol and related prenylflavonoids in hops and beer by liquid chromatography-tandem mass spectrometry. J Chromatogr A. 1999;832:97–107
  114. Forster A, Massinger S, Schmidt R. Breakdown of hop bitter substances during storage of beer. Brauwelt Intern. 2004;2004/VI:426
  115. Vanhoenacker G, De Keukeleire D, Sandra P. Analysis of iso-alpha-acids and reduced iso-alpha-acids in beer by direct injection and liquid chromatography with ultraviolet absorbance detection or with mass spectrometry. J Chromatogr A. 2004;1035:53–61
  116. Walker CJ, Lence CF, Biendl M. Investigation into the high levels of xanthohumol found in stout and porter – style beers. Brauwelt Intern. 2004;2004/II:100–103

PII: S0959-8049(05)00330-8

doi: 10.1016/j.ejca.2005.04.012

European Journal of Cancer
Volume 41, Issue 13 , Pages 1941-1954 , September 2005

Article Tools

* Image Usage & Resolution