Berries and Cancer Prevention
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3 Berries and Cancer Prevention
4 Gary D. Stoner Navindra P. Seeram Editors Berries and Cancer Prevention 123
5 Editors Gary D. Stoner, Ph.D Department of Medicine Medical College of Wisconsin Milwaukee, WI 53226, USA Navindra P. Seeram, Ph.D Department of Biomedical and Pharmaceutical Sciences University of Rhode Island Kingston, RI 02881, USA ISBN e-isbn DOI / Springer New York Dordrecht Heidelberg London Springer Science+Business Media, LLC 2011 All rights reserved. This work may not be translated or copied in whole or in part without the written permission of the publisher (Springer Science+Business Media, LLC, 233 Spring Street, New York, NY 10013, USA), except for brief excerpts in connection with reviews or scholarly analysis. Use in connection with any form of information storage and retrieval, electronic adaptation, computer software, or by similar or dissimilar methodology now known or hereafter developed is forbidden. The use in this publication of trade names, trademarks, service marks, and similar terms, even if they are not identified as such, is not to be taken as an expression of opinion as to whether or not they are subject to proprietary rights. While the advice and information in this book are believed to be true and accurate at the date of going to press, neither the authors nor the editors nor the publisher can accept any legal responsibility for any errors or omissions that may be made. The publisher makes no warranty, express or implied, with respect to the material contained herein. Printed on acid-free paper Springer is part of Springer Science+Business Media (
6 Preface Among colorful fruits, berries and their derived products command an overwhelming and rapidly growing body of scientific data to support their ability to prevent, delay and potentially treat certain types of human cancers. Given that the worldwide incidence of cancer is rapidly increasing, intervention with foodstuffs, such as berries and berry formulations, provide an attractive strategy to cancer prevention. Like many other fruits, berries contain micro- and macronutrients such as vitamins, minerals, and fiber. However, berries also contain a multitude of plant secondary metabolites (phytochemicals) that exhibit a diverse array of chemical structures. It has become apparent that multiple berry constituents, through additive, complementary, and/or synergistic interactions, exhibit chemopreventive effects superior to any single component alone. This book provides focused and timely discussions on berries and cancer. The chapters presented here are collected from a multi-disciplinary team of international researchers. Thus, the fifteen chapters are organized into four sections. The first section consists of three chapters, examining the overall theme of berry composition, bioavailability, metabolism and biological effects. The second section examines the antioxidant effects of berry components which are presented in a single chapter. The third section, groups eight chapters which examine the chemopreventive effects of berries and berry components in animal model systems. The fourth and last section comprises three chapters that individually discuss cancer prevention studies with berries and berry formulations in human subjects. We think this collection of writings is the first of many to come in the future regarding the role of berries and their components as preventative agents for cancer. We thank all authors for their contributions towards making this book a success. Also, Sophia O. Tolliver for her invaluable assistance in coordinating this project. Milwaukee, WI, USA Kingston, RI, USA Gary D. Stoner Navindra P. Seeram v
7 Contents Part I Berry Composition, Bioavailability, Metabolism and Biological Effects 1 Contribution of Berry Anthocyanins to Their Chemopreventive Properties... 3 Pu Jing and M. Monica Giusti 2 Ursolic Acid and Other Pentacyclic Triterpenoids: Anticancer Activities and Occurrence in Berries Catherine C. Neto 3 The Effects of Berry Extracts on Cell Signaling Pathways: Leading to Cellular Transformation Tongjian Cai and Chuanshu Huang Part II Antioxidant Capacity of Berry Components 4 Correlation of Antioxidants and Antioxidant Enzymes to Oxygen Radical Scavenging Activities in Berries Shiow Y. Wang Part III Chemopreventive Effects of Berries and Berry Components in Animal Model Systems 5 Berries in the Prevention of Esophageal Adenocarcinoma Laura A. Kresty, Amy Exum, and Bree Zeyzus-Johns 6 Endothelial Cell Tumor Prevention with Berry Extracts: Clinical Problems, Molecular Mechanisms and Therapeutic Opportunities Gayle M. Gordillo and Chandan K. Sen 7 Effects of Black Raspberries on UV-Induced Cutaneous Inflammation and Tumor Development Tatiana Oberyszyn vii
8 viii Contents 8 Chemopreventive Effects of Berries and Berry Components in the Rodent Esophagus Claire M. Seguin, Li-Shu Wang, and Gary D. Stoner 9 Chemopreventive Effects of Berries and Berry Components in Animal Models: Prevention of Estrogen-Mediated Mammary Tumors in ACI Rats by Berries Harini Aiyer, Srivani Ravoori, and Ramesh Gupta 10 Inhibition of Oral Cancer in Animal Models by Black Raspberries and Berry Components Bruce C. Casto, Thomas J. Knobloch, and Christopher M. Weghorst 11 Prevention of Cancer with Pomegranate and Pomegranate Anthocyanins Vaqar Mustafa Adhami, Naghma Khan, and Hasan Mukhtar 12 Chemoprevention of Chronic Inflammatory Bowel Disease-Induced Carcinogenesis in Rodent Models by Berries Allison Yang, Haonan Li, WanYing Zhang, Yeon Tae Chung, Jie Liao, and Guang-Yu Yang Part IV Berry Chemoprevention in High-Risk Populations 13 Cancer Prevention in Humans at High-Risk for Development of Cancer: Prevention of Oral Dysplasia in Humans by Berry Formulations Susan R. Mallery and Meng Tong 14 Cancer Prevention in Populations High At-Risk for the Development of Oral Cancer: Clinical Trials with Black Raspberries Thomas J. Knobloch, Bruce C. Casto, Amit Agrawal, Steven K. Clinton, and Christopher M. Weghorst 15 Effects of Black Raspberries on Cellular and Epigenetic Biomarkers of Colon Cancer Development in Humans Gary D. Stoner, Li-Shu Wang, Christine Sardo, Mark Arnold, Edward Martin, Wendy Frankel, and Dennis Pearl Index
9 Contributors Vaqar Mustafa Adhami Department of Dermatology, University of Wisconsin, Madison, WI 53706, USA Amit Agrawal Department of Otolaryngology, The Ohio State University College of Medicine, Columbus, OH 43210, USA Harini Aiyer James Graham Brown Cancer Center, University of Louisville, Louisville, KY 40202, USA; Department of Surgery, University of Louisville, Louisville, KY 40202, USA Mark Arnold Department of Surgery, The Ohio State University College of Medicine, Columbus, OH 43210, USA Tongjian Cai Nelson Institute of Environmental Medicine, New York University School of Medicine, Tuxedo, NY 10987, USA Bruce C. Casto Division of Environmental Health Sciences, College of Public Health, The Ohio State University, Columbus, OH 43210, USA Yeon Tae Chung Department of Pathology, Northwestern University Feinberg School of Medicine, Chicago, IL 60611, USA Steven K. Clinton Division of Hematology and Oncology, The Ohio State University College of Medicine, Columbus, OH 43210, USA Amy Exum Department of Epidemiology and Public Health, Miller School of Medicine, University of Miami Sylvester Cancer Center, Miami, FL 33136, USA Wendy Frankel Department of Pathology, The Ohio State University College of Medicine, Columbus, OH 43210, USA M. Monica Giusti Department of Food Science and Technology, The Ohio State University, Columbus, OH 43210, USA Gayle M. Gordillo Division of Plastic Surgery, Davis Heart Lung Research Institute, The Ohio State University, Columbus, OH 43212, USA ix
10 x Contributors Ramesh Gupta James Graham Brown Cancer Center, University of Louisville, Louisville, KY 40202, USA; Department of Pharmacology and Toxicology, University of Louisville, Louisville, KY 40202, USA Chuanshu Huang Nelson Institute of Environmental Medicine, New York University School of Medicine, Tuxedo, NY 10987, USA Pu Jing Institute of Food and Nutraceutical Science, School of Agriculture and Biology, Shanghai Jiao Tong University, Shanghai , P.R. China Naghma Khan Department of Dermatology, University of Wisconsin, Madison, WI 53706, USA Thomas J. Knobloch Division of Environmental Health Sciences, College of Public Health, The Ohio State University, Columbus, OH 43210, USA Laura A. Kresty Department of Epidemiology and Public Health, Miller School of Medicine, University of Miami Sylvester Cancer Center, Miami, FL 33136, USA Haonan Li Department of Pathology, Northwestern University Feinberg School of Medicine, Chicago, IL 60611, USA Jie Liao Department of Pathology, Northwestern University Feinberg School of Medicine, Chicago, IL 60611, USA Susan R. Mallery Division of Oral Maxillofacial Surgery, Pathology and Anesthesiology, College of Dentistry, The Ohio State University, Columbus, OH 43210, USA Edward Martin Department of Surgery, The Ohio State University College of Medicine, Columbus, OH 43210, USA Hasan Mukhtar Department of Dermatology, University of Wisconsin, Madison, WI 53706, USA Catherine C. Neto Department of Chemistry and Biochemistry, University of Massachusetts Dartmouth, North Dartmouth, MA 02747, USA Tatiana Oberyszyn Department of Pathology, The Ohio State University, Columbus, OH 43201, USA Dennis Pearl Department of Statistics, The Ohio State University, Columbus, OH 43210, USA Srivani Ravoori James Graham Brown Cancer Center, University of Louisville, Louisville, KY 40202, USA Christine Sardo Comprehensive Cancer Center, The Ohio State University College of Medicine, Columbus, OH 43210, USA Claire M. Seguin Comprehensive Cancer Center, The Ohio State University College of Medicine, Columbus, OH 43210, USA
11 Contributors xi Chandan K. Sen Department of Surgery, Davis Heart Lung Research Institute, The Ohio State University, Columbus, OH 43212, USA Gary D. Stoner Department of Medicine, Medical College of Wisconsin, Milwaukee, WI 53226, USA Meng Tong Division of Oral Maxillofacial Surgery, Pathology and Anesthesiology, College of Dentistry, The Ohio State University, Columbus, OH 43210, USA Li-Shu Wang Comprehensive Cancer Center, The Ohio State University College of Medicine, Columbus, OH 43210, USA Shiow Y. Wang Genetic Improvement of Fruits and Vegetables Lab, US Department of Agriculture, ARS, Beltsville, MD 20705, USA Christopher M. Weghorst Division of Environmental Health Sciences, College of Public Health, The Ohio State University, Columbus, OH 43210, USA Allison Yang Department of Pathology, Northwestern University Feinberg School of Medicine, Chicago, IL 60611, USA Guang-Yu Yang Department of Pathology, Northwestern University Feinberg School of Medicine, Chicago, IL 60611, USA Bree Zeyzus-Johns Department of Epidemiology and Public Health, Miller School of Medicine, University of Miami Sylvester Cancer Center, Miami, FL 33136, USA WanYing Zhang Department of Pathology, Northwestern University Feinberg School of Medicine, Chicago, IL 60611, USA
12 Part I Berry Composition, Bioavailability, Metabolism and Biological Effects
13 Chapter 1 Contribution of Berry Anthocyanins to Their Chemopreventive Properties Pu Jing and M. Monica Giusti Abstract Interest in berry fruits has intensified worldwide because of the multiple health-promoting phytochemicals present. Anthocyanins represent a major class of phytochemicals present in most colorful berries, and are of interest to nutritionists because of their postulated health benefits, as well as to food processors because of their colorful character and their use as natural colorants. This chapter presents an overview of the role of anthocyanins in the chemoprotective effects of berries. We will review incidence of anthocyanins in berries, their chemistry and concentration, as well as the reported literature regarding in vitro and in vivo chemoprotective studies, structure/chemoprotection relationship, bioavailability, and the interaction of berry anthocyanins with other phytochemicals. The data presented suggests that anthocyanins play a major role in the chemoprotective effects of many berry fruits. Keywords Berry Anthocyanin Concentration Structure Chemoprevention Bioavailability Interaction effect Structure-bioactivity relationship 1 Introduction Berries are popularly consumed in North America both in fresh or frozen forms and in a variety of processed foods such as yogurts, beverages, jams, canned fruits, jellies, et al. Recently, interest in berry fruits has intensified around the world because of the multiple health-promoting phytochemicals found in berries. Berry extracts are being commercialized as nutraceuticals and as dietary supplements to meet consumers demands. M.M. Giusti (B) Department of Food Science and Technology, The Ohio State University, Columbus, OH 43210, USA giusti.6@osu.edu G.D. Stoner, N.P. Seeram (eds.), Berries and Cancer Prevention, DOI / _1, C Springer Science+Business Media, LLC
14 4 P. Jing and M.M. Giusti Anthocyanins represent one of major phytochemicals present in most colorful berries and are of interest to nutritionists because of their postulated health benefits, as well as to food processors because of their colorful character as a natural alternative to the use of synthetic dyes. This chapter will present an overview of the incidence of anthocyanins in berries, their chemistry and concentration, as well as the reported literature regarding in vitro and in vivo chemoprotective studies, structure/chemoprotection relationship, bioavailability, and the interaction of berry anthocyanins with other phytochemicals. 2 Incidence of Anthocyanins in Berries Anthocyanins are responsible for most of the wonderful orange-red, red, purple, blue and even some deep black colors in berries. Visual appearance of fresh and processed berries is the first factor influencing acceptability and quality perception regarding flavor and texture by consumers. Anthocyanin-rich berries and anthocyanin pigments from berry fruits have been suggested as potential chemoprotective agents, and a large and growing body of evidence from in-vitro cell culture studies, in-vivo animal model tumor systems, as well as human epidemiological studies. However, color appearance and cancer preventive properties are closely associated with the concentration of the pigments as well as their chemical structures. Therefore, accurate data about anthocyanin content and distribution in berry fruits are important. The most commonly consumed berry fruits in North America include strawberries, blueberries, cranberries, red raspberries, blackberries, and black raspberries (Strik, 2007). In the following sections, we will discuss the types and concentration of anthocyanins in those berries and in other less common berries of growing interest. 2.1 Types of Anthocyanins Found in Berries Anthocyanins belong to the class of flavonoid compounds and are commonly known as plant polyphenols. The anthocyanin pigments consist of two or three main chemical units: the flavylium ring or aglycone base (anthocyanidin), sugars, and sometimes acylating groups. Anthocyanidins present the basic structure of a C6-C3- C6 carbon skeleton typical of flavonoids. They are polyhydroxy and polymethoxy derivatives of 2-phenylbenzoprylium or flavylium salts, differing in the number and position of their hydroxyl and methoxyl groups on the B ring (Fig. 1.1). There are 27 known anthocyanidins present in nature (Andersen and Jordheim, 2005), however, only six (cyanidin, pelargonidin, peonidin, delphinidin, petunidin, and malvidin) are commonly found in berries (Giusti and Jing, 2007). One of the unusual anthocyanidin structures found in berries was a 4-substituted aglycone, recently found in strawberries (Fragaria ananassa Duch.), a 5-carboxypryanopelargonidin 3- O- ß-glucopyranoside, although present only in small concentrations (Andersen et al., 2004).
15 1 Contribution of Berry Anthocyanins to Their Chemopreventive Properties 5 HO 7 A 5 OH O + C 3 OH R 1 3 B OH 4 5 R 2 Pelargonidin R 1 =H R 2 =H Cyanidin R 1 =OH R 2 =H Delphinidin R 1 =OH R 2 =OH Peonidin R 1 =OCH 3 R 2 =H Petunidin R 1 =OCH 3 R 2 =OH Malvidin R 1 =OCH 3 R 2 = OCH 3 Fig. 1.1 Chemical structures of anthocyanidins commonly found in berries Anthocyanidins rarely occur in their free form in nature because of their high reactivity. Anthocyanins are mainly glycosylated with one or more sugar moieties that enhance their stability and solubility (Harborne, 1979; Clifford, 2000; Giusti and Wrolstad, 2003). The most common sugar moieties found attached to the aglycone is glucose (Table 1.1), followed by galactose, rhamnose, xylose, arabinose. Anthocyanins can be glycosylated with one or more sugar units, typically up to 3, with some rare exceptions. The C 3 -hydroxyl position of the C-ring is the primary place for glycosylation, followed by the C 5 position of the A ring (Fig. 1.1). Less common sites of glycosylations are the C 7 position, and in rare cases, glycosylation has been reported on the B ring. Although not common in berries, some anthocyanins may be acylated. Acylated anthocyanins have acids attached to the sugar moiety, either aliphatic (such as acetic or malonic) acids or aromatic (such as p-coumaric or caffeic) acids. Acylated anthocyanins have been reported in boysenberries and marionberries. Different combinations of types and numbers of sugars and/or acids attached to the different type of aglycons lead to a wide range of different anthocyanins found in berries. However, the most predominant berry anthocyanin is cyanidin-3-glucoside. The anthocyanin composition in berries (Table 1.1) has been used as a botanical tool for taxonomic classification of plants, as the anthocyanin profile tends to be characteristic of a plant, similar to a fingerprint. Anthocyanin profiles vary largely among different species but tend to remain quite similar within the same species. Some profiles are rather simple, such as the cases of strawberry, where 80 90% of the pigment composition is just one pigment, pelaronidin-3-glucoside. Other berries are characterized for their complex anthocyanin profiles, such as Vaccinium corymbosum commonly known as highbush blueberries that exhibit 5 of the different aglycones (cy, dp, pt, mv and pn), 3 different glycosylating sugars (glu, gal, and ara), and also exhibit some acylated derivatives of these anthocyanins the acetylated monoglycosides. The most widespread anthocyanin in berries is cyanidin 3-glucoside. Differential anthocyanin profiles can be also used for the detection of adulteration in specific commodities of berry fruit products.
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