ANNALS OF THE NEW YORK ACADEMY OF SCIENCES

Valume 1126

The Maillard Reaction

Recent Advances in Food and Biom.edical Sciences

Edited by ERWIN SCHLEICHER, VERONIKA SOMOZA, AND PET ER SCHIEBERLE

Published by Blackwell Publishing on behalf of the Neu' lork Acaden~v of Seienefs Boston, Massachusetts

2008

ANNALS OF THE NEW YORK ACADEMY OF SCIENCES

Volume 1126 April 2008

The Maillard Reaction

Recent Advances in Food and Biorn.edical Sciences

Editors ERWIN SCHLEICHER, VERONIKA SOMOZA, AND PETER SCHIEBERLE

This volume is the result of the 9th International SYDlposhuIl on the Maillard Reaction, held September 1-5, 2007 in Munieh, Germany.

CONTENTS

Preface. By Erwin Schleicher, Veronika Somoza, and Peter Schieb erle

Part I. Keynote Papers

The Sense ofSmell: Reception ofFlavors. ßy H. Breer ... " .................. .

Receptor far Advanced Glycation End Products: Fundamental Roles in thc Inflammatory Response: Winding the Way to the Pathogenesis of Endothelial Dysfunction and Atherosclerosis. By Ravichandran Ramasamy, Shi Fang Yan,

Xlll

Kevan Herold, Raphael Clynes, and Ann Marie Schmidt ................. 7

Central Nervous System Regulation ofEnergy Metabolism: Ghrelin versus Leptin. By Ruben Nogueiras, Matthias H. Tschöp, andJeffrey M. Zigman .. 14-

Determination of .N'-(Carboxymethyl)lysine in Foods and Related Systems. By Jennifer M. Ames . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 20

Part 11. Plenary Lectures

Food Anoxia and the Formation of Either Flavar ar Toxic Compounds by Amino Acid Degradation Initiated by Oxidized Lipids. ßy FranciscoJ. Hidalgo and Rosario Zamora ........... , ......... " ....................... " . .. . . . . 25

Post-Schiff Base Chemistry ofthe Maillard Reaction: Mechanism ofImine Isomerization. By Fong Lam Chu and Varoujan A. Yaylayan .............. 30

vii

viii Annals of the New York Academy of Sciences

Usefulness of Antibodics for E\'alliating thc Biological Significancc oL\(; Es, l!r Ryoji Nagai, Yukio Fuji\\'ara, Kat~lImi ~1~Ta, ~eita. ~l.()t(}ml.lra: . Yasunori Iwao, Keiichiro TsUrllShlllla, ~ IlllH' :\ agal, KaZlIlllJ'O Ltkco. Makiko Yoshitomi, ~Iasaki Otagiri, allel 'lSlIyoshi Ikcela ., . , , , .. , ....... , , .

Receptor for Advanceel Glycation End Proeluct E~pressi()n in Experimental Diabetic Retinopathy. ß.r Vumei "'ang, Franziska \U!11 HagcIL Frederick Pfister, Angelika Bicrhaus, Vuxi Feng, Rcinholel Gans, ami Hans-Peter Hammes .................................................. .

Advanced Glvcation End Product Homcostasis: Exogenous Oxielants ancl Innate Defenses: By Helen Vlassara, jaime Cribarri, \\'cijing Cai, ami Gar) Strikcr

Formation 1Iechanisms of11elanoidins and Fluoresccnt P\Tielinilim Compollnds as Aelvanced Glycation End Products. ß.)' Fumitaka H~l)asc, Tcrll)lIki Csui, Yoriyuki Ono, Yoshinobu Shirahashi, Tomomi '\lachida, Takashi lto, Nozomu Nishitani, Kazuhito Shimohira, and Hirohito "'atanahc , ........ .

Advanced Glycation as a Basis for ünelcrstanding Retinal Aging anel :'\()nill\'as~\'(' Risk Preeliction. By Anna 11. Pawlak, joscphine V GlcllJl, Jalllcs R. Ikattw, johnJ McGarvey, and Alan W. Stitt .................................... .

The Aroma Siele of the Maillard Reaction. l!Ji Christoph (:(TJlY ............... .

Methylglyoxal: Its Presence in Bcvcrages anel Potcnt ial SCa\·cJlgcrs. 1!J' Di TlIl, Yu Wang, Chih-Yu Lo, Shengmin Sang, ami Chi-Tang Ho ............... .

The RAGE Pathway: Activation and PcrpctuatioJl ill thc Pat!Jogcllcsis of Dialwtic Neuropathy. By Ivan K. Lukic, Per ~L Humpert, Peter l~ Nawroth, ami Angelika Bierhaus .................................................... .

The Role of the Amadori Product in the Complications of Diabetes. ß.r Vincent M. Monnier, David R. SeIl, Zhenyu Dai, Ina Nemet, Francois Collard, andJianye Zhang .................................... .

Mitigation Strategies to Reduce Acrylamide Formation in Fried Potato Products. By Francisco Morales, Edoardo Capuano, and Vincenzo Fogliano ......... .

Therapeutic Interruption of Advanced Glycation in Diabetic Nephropathy: Do All Roads Lead to Rome? By Karly C. Sourris,josephine M. Forbes, and Mark E. Cooper ...................................................... .

The Other Side ofthe Maillard Reaction. By Ram H. Nagaraj, Ashis Bis\vas, Antonia Miller, Tomoko Oya-Ito, and Manjunatha Bhat ................. .

Dicarbonyls Stimulate Cellular Protection Systems in Primary Rat Hepatocytes and Show Anti-inftammatory Properties. By Timo M. Buetlcr, HeIia Latado, Alexandra Baumeyer, and Thierry Delatour ............................ .

N-terminal Glycation of Proteins and Peptides in Foods and in Vivo: Evaluation of N-(2-Furoylmethyl)Valine in Acid Hydrolyzates ofHuman Hemoglobin. By Ilka Penndorf, Changhao Li, Uwe Schwarzenbolz, and Thomas Henle .....

The Dicar?onyl ~rot~ome: Proteins Susceptible to Dicarbonyl Glycation at FunctlOnal Sltes 111 Health, Aging, and Disease. By Naila Rabbani and Paul]. Thornalley .................................................... .

Peroxyl R~dicals A~e Essential Reagents in the Oxidation Steps of the Maillard ReactlOn Lead111g to Generation of Advanced Glycation End Products. By Gerhard Spiteller ..................................................... .

Applica~ion. of Mass Spectrometry for the Detection of Glycation and OXldatlOn Products in Milk Proteins. By Jasmin Meltretter and Monika Pischetsrieder ................................................. .

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Contents ix

Inhibition of Advanced Glycation End Products: An Implicit Goal in Clinical Medicine for the Treatment ofDiabctic Nephropathy? By Toshio Miyata and Yuko Izuhara . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 141

Inflammation and thc Rcdox-sensitive AGE-RAGE Pathway as a Therapeutic Target in Alzheimer's Disease. By Annette Maczurek, Kirubakaran Shanmugam, and Gerald Münch . . . . . . . . . . . . . . . . . . . . . . . . . . . 147

Part IH. Oral Presentations

Some Natural Compounds Enhance .JVE-(Carboxymethyl)lysine Formation. By Yukio Fujiwara, Naoko Kiyota, Keita Motomura, Katsumi .Mera, Motohiro Takeya, Tsuyoshi Ikeda, and Ryoji Nagai .......... '" . . . .. .. . . . 152

Immunological Detection of NW-(Carboxymethyl)arginine by a Spccific Antibody. By ~atsum~ Mera, Yukio Fujiwara, Masaki Otagiri, Noriyuki Sakata, and RYOJI Nagal ........................................................... 155

Isolation and Partial Characterization of Four Fluorophores Formed by Nonenzymatic Browning ofMethylglyoxal and Glutamine-derivcd Ammonia. By Celine Niquet, Serge Pilard, David Mathiron, and FredericJ. Tcssicr 158

Receptor for Advanced Glycation End Product Polymorphisms and Type 2 Diabetes: The CODAM Study. By Katrien HJ. Gacns, CarlaJ.H. van der Kallen, Marleen MJ. van Greevenbroek, EdithJ. Feskens, Coen D.A. Stehouwcr, and Casper G. Schalkwijk . . . . . . . . . . . . . . . . . . . . . . . . . 162

Pentosidine Effects on Human Osteoblasts in Vitra. By Roberta Sanguineti, Daniela Storace, Fiammetta Monacelli, Alberto Federici, and Patrizio Odetti . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 166

Strategy for the Study ofthe Hcalth Impact ofDietary ~1aillard Products in Clinical Studies: The Example of the ICARE Clinical Study on Healthy Adults. By Philippe Pouillart, Helene Mauprivez, Lamia Ait-Ameur, Amelie Cayzeelc,Jean-Michel Lecerf, FredcricJ. Tessier, and 1. Birloucz-Aragon . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 173

Plasma Conccntration and Urinary Excretion of.JVE-(Carboxymt'thyl)lysine in Breast Milk-- and Formula-fC:d Infants. By Katarina Sebekova, GiscHc Saavedra, Cornelia Zumpe, Veronika Somoza, Kristina KlenovicsO\'a, and Ines Birlouez-Aragon .............................................. 177

Maillard Rcaction Products in the Escherichia coli-derived Therapeutic Protein Interferon Alfacon-l. By Roumyana ~1ironova, Angelina Sredovska, Ivan Ivanov, and Toshimitsu Niwa ...................................... 181

Acrolein Induccs Inflammatory Response Underlying Endothelial Dysfunction: A Risk Faetor for Atherosclerosis. By Yong Seek Park and Naoyuki Taniguchi .................................................... 185

Oxidative Stress and Advanced Glycation in Diabetic Nephropathy. 1!J1 Melinda T. Coughlan, Amy L. Mibus, andJosephine M. Forbes . . . . . . . . . . . . 190

Vitamin C-mediatcd Maillard Reaction in the Lens Probed in a Transgenic-mouse Model. By Xingjun -Fan and Vincent M. Monnic'}' . . . . . . . 194

.JVE-(Carboxymethyl)lysine during the Early Development ofHypcrtension. ~)I Marcus Baumann, Coen Stehouwcr,Jcan Scheijen, Uwe Hccmann, Harry Struijker Boudier, and Casper Schalkwijk . . . . . . . . . . . . . . . . . . . . . . . . . . 201

x Annals of the New York Academy of Sciences

Aging, Diabetes, and Renal Failurc Catalyzc thl' Oxicl,~tioll of Ly~yl Rcsiclucs to 2-Aminoadipic Acid in Human Skin (:ol!agen: Enc\cllcc for :"\letal-catalyzcd Oxidation Mediated bv a-Dicarbonds. 1$)' Dm'id R. SclL Christophcr :"\1. Strauch, Wei Shen, and Vincent :"\1.\10,lnicr ............................ 205

a-Dicarbonyl Compounds--Key Intermediates for the Formation of . Carbohvdrate-based ~lelanoidins. B), Lothar \\'. Kroh, Thorsten Frecller. and Janine Wagner ................... ~ . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 210

Approaches to Wine Aroma: Cl Transfer du ring the Reaction bet\\een Diacetyl and Cysteine. By John Almy and Gilles dl' Revel . . . . . . . . . . . . . . . . . . . . . . . . .. 216

Antioxidant Activity and Chemical Properties of Crude and Fractionated Maillard Reaction Products Derived from Four Sugar-Amino Acid :"\laillard Reaction Model Systems. By Xiu-~Iin Chen and Da\'id D. Kitts ........... 220

Advanced Glycation Endproducts in Chronic Hcart Failure. l~)' Andries.J. Smit, Jasper W L. Hartog, Adriaan A. Voors, and Dirk.J. van Vclclhuiscn ........ 225

Methylglyoxal and Methylglyoxal-argininc Adducts Do l'\O( Dircctly Inhibit Endothelial Nitric Oxide Synthase. I~y Olaf Brouwcrs, Tom Tccrlink, Jan van Bezu, Rob Barto, Coen D.A. StchOUWlT, ,md Caspcr G Schalkwijk ............................................................ 2:3 1

Kinetic Study ofthe Reaction ofGlycolalckhyck with Two (;I~Ta(ion 'Lu'ge( Models. By Miquel Adrover, Bartolomt'· Vilanov<l, Francisco :\Iur\oz, ,md Josefa Donoso ......................................................... 235

Origin and Yields of Acetic Acid in Pentose-bascd Maillarcl Rcaction Systems. I'!y Tomas Davidek, Elisabeth Gouezec, Stephanie Devaud, and ll11r(' Blank ... 241

The Peptide-catalyzed Maillard Reaction: Characterization of l'C Reductones. By Leif Alexander Garbe, Alexander Würtz, Christian T Piechotta, and Roland Tressl ......................................................... , 244

Model Studies on Pro tein Glycation: Influence of Cysteine on the Reactivity of Arginine and Lysine Residues toward Glyoxal. By Uwe Schwarzenbolz, Susann Mende, and Thomas Henle ..................................... 248

Analysis of Amadori Peptides Enriched by Boronic Acid Affinity Chromatography. By Andrej Frolov and Ralf Hoffmann .................. , 253

Induetion of Heat Shock Proteins and the Proteasome System by Casein-N"-(Carboxymethyl)lysine and N"-(Carboxymethyl)lysine in Caco-2 Cells. By Karoline Schmid, Martin Haslbeck, Johannes Buehner, and Veronika Somoza ..................................................... , 257

Reversal of Hyperglycemia-induced Angiogenesis Deficit of Human Endothelial Cell~ by Overexpression ofGlyoxalase 1 in Vitra. By Usman Ahmed, Dann Dobler, Sarah]. Larkin, Naila Rabbani, and Paul]. Thornalley . . . . . . 262

Pathophysiol<:>gical Rol~ ofthe Glyoxalase System in Renal Hypoxie Injury. By Takanon Kumagm, Masaomi Nangaku, and Reiko Inagi .. , .............. , 265

A419C (ElllA) Polymorphism ofthe Glyoxalase I Gene and Vascular Complications in Chronic Hemodialysis Patients. By Marta Kalousova, Alex~~dr.a Germanova, MarieJachymova, Oto Mestek, Vladimir Tesar, and Tomas Zlma .......................................................... 268

Suceination of Proteins by Fumarate: Mechanism of Inaetivation of Glyceraldehyde-3-Phosphate Dehydrogenase in Diabetes. By Matthew Blatnik, Suzanne R. Thorpe, andJohn W Baynes ............... 272

Contents xi

Dietary Advanced Glycation Endproducts and Oxidative Stress: In Vivo Effects on Endothelial Function and Adipokines. By Alin Stirban, Monica Negrean, Christian Götting,Jaime Uribarri, Thomas Gawlowski, Bernd Stratmann, Knut Kleesiek, Theodor Koschinsky, Helen Vlassara, and Diethelm Tschoepe .................................................... 276

Preparation of N ucleotide Advanced Glycation Endproducts-Imidazopurinone Adducts Formed by Glycation of Deoxyguanosine with Glyoxal and Methylglyoxal. By Thomas Fleming, Naila Rabbani, and PaulJ. Thornalley . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .. 280

Maillard Products as Biomarkers in Cancer. By Beatrice E. Bachmeier, Andreas G. Nerlich, Helmut Rohrbach, Erwin D. Schleicher, and Ulrich Friess . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 283

Glycation of Plasma Lipoprotein Lipid Membrane and Screening for Lipid Glycation Inhibitor. By Kiyotaka Nakagawa, Daigo Ibusuki, Shinji Yamashita, and Teruo Miyazawa . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .. 288

Analysis of Amadori-glycated Phosphatidylethanolamine in the Plasma of Healthy Subjects and Diabetic Patients by Liquid Chromatography-Tandem Mass Spectrometry. By Teruo Miyazawa, Daigo Ibusuki, Shinji Yamashita, and Kiyotaka N akagawa ................................................... 291

Nonenzymatically Glycated Lipoprotein ApoA-I in Plasma ofDiabetic and Nephropathic Patients. By Annunziata Lapolla, Maura Brioschi, Cristina Banfi, Elena Tremoli, Chiara Cosma, Luciana Bonfante, Simone Cristoni, Roberta Seraglia, and Pietro Traldi ..................... 295

Evaluating the Extent of Pro tein Damage in Dairy Products: Simultaneous Determination of Early and Advanced Glycation-induced Lysine Modifications. ByJörg Hegele, Veronique Parisod,Janique Richoz, Anke Förster, Sarah Maurer, Rene Krause, Thomas Henle, Timo Bütler, and Thierry Delatour ...................................................... 300

A Novel Yellow Pigment, Furpipate, Derived from Lysine and Furfural. ~y Masatsune Murata, Hana Totsuka, and Hiroshi Ono ..................... 307

Time-dependent Componcnt-specific Regulation of Gastric Acid Secretion-related Proteins by Roastecl CofTee Constituents. ~Y M. Rubach, R. Lang, T. Hofmann, and V. Somoza .................. . . . . . . . . . . . . . . . . . 310

Maillard Reaction versus Other N onenzymatic Modifications in Neurodegenerative Processes. By Reinald Pamplona, Ekaterina Ilieva, Victoria Ayala, MariaJosep Bellmunt, Daniel Cacabelos, Esther Dalfo, Isidre Ferrer, and Manuel Portero-Otin .................................. 315

Suppression ofRenal a-Dicarbonyl Compounds Generated following Ureteral Obstruction by Kidney-Specific a-DicarbonyllL-Xylulosc Reductase. ~Y Hiroko Odani,Jun Asami, Aiko Ishii, Kayoko Oide, Takako Sudo, Atsushi Nakamura, Noriyuki Miyata, Noboru Otsuka, Kenji Maeda, and Junichi Nakagawa ..................................................... 320

Comparison of Pharmacokinetics between Highly and Mildly Modified AG E Proteins in Mice. By Ryoji Nagai, Katsumi Mera, Yukio Fujiwara, Mime Nagai, and Masaki Otagiri ....................................... 325

Modification ofVimentin: A General Mechanism ofNonenzymatic Glycation in Human Skin. By Thomas Kueper, Tilman Grune, Gesa-Meikc Muhl~ Holger Lenz, Klaus-Peter Wittern, Horst Wenck, :Franz Stäb, and Thomas Blatt. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .. 328

xii Annals of the New York Academy of Sciences

Erratum far Ann. N.Y Acad. Sei. lO72: 3Hti :)B8. Inflallllll<llol"\ Bowcl Disc<lsc: Geneties, Barrier Functiün, Immunologie ~kehanisms. ,tIl~1 ~liLT()bial Pathways. ............................................................. :)33

Erratum für Ann. )J.Y Aead. Sei. 1088::\ 1 .\ 1 O. :'\curocndocrinc anel Immune Crosstalk. ............................................................. 33+

Erratum far Ann. N.Y Aead. Sei. 1108: .10.1-51 +. :\utüimmunit\; Part D: Autoimmune Disease, Annus :\Iirabilis. .................................. 335

Errata for Ann. XY Acad. Sei. 1111: ++2-+5+. Coccidioiclomycosis: Sixth International Symposium. . .......................... .'................. 336

Index of Contributors 337

The l\ew York Academy or Sciel1ccs l>e!ic\"('s il has a rcsp()l1SilJilil\ lo prmidc all "pm limlll1 Ir))' discussion of scientific questi()ns. Thc positions laken by lhc particip<lnh in lhe rep0rled ("onkrellCl'S are their ()wn and not neccssarily those ofthc :\cadelll\'. Thc ,\cadelllY has no inlellt lo inlllH'lHT legislalif))l by providing such forums.