Reviews of Physiology, Biochemistry and Pharmacology, Vol. 164 PDF
Preview Reviews of Physiology, Biochemistry and Pharmacology, Vol. 164
Reviews of Physiology, Biochemistry and Pharmacology 164 Reviews of Physiology, Biochemistry and Pharmacology Forfurther volumes: http://www.springer.com/series/112 ThiSisaFMBlankPage (cid:1) (cid:1) Bernd Nilius Susan G. Amara (cid:1) (cid:1) Thomas Gudermann Reinhard Jahn (cid:1) (cid:1) Roland Lill Stefan Offermanns Ole H. Petersen Editors Reviews of Physiology, Biochemistry and Pharmacology 164 Editors BerndNilius SusanG.Amara KatholiekeUniversiteitLeuven UniversityofPittsburgh Lab.Fysiologie SchoolofMedicine Herestraat49 DeptartmentofNeurobiology CampusGasthuisbergO&N BiomedicalScienceTower3 Belgium Pittsburgh,PA USA ThomasGudermann Ludwig-Maximilians-Universita¨tMu¨nchen ReinhardJahn MedizinischeFakulta¨t Max-Planck-InstituteforBiophysical Walther-Straub-Institutfu¨rPharmakologi Chemistry Mu¨nchen Go¨ttingen Germany Germany RolandLill StefanOffermanns UniversityofMarburg Max-Planck-Institutfu¨rHerzund Inst.ZytobiologieundZytopathologie Lungen Marburg AbteilungII Germany BadNauheim Germany OleH.Petersen SchoolofBiosciences CardiffUniversity MuseumAvenue Cardiff,UK ISSN0303-4240 ISSN1617-5786(electronic) ISBN978-3-319-00995-7 ISBN978-3-319-00996-4(eBook) DOI10.1007/978-3-319-00996-4 SpringerChamHeidelbergNewYorkDordrechtLondon #SpringerInternationalPublishingSwitzerland2013 Thisworkissubjecttocopyright.AllrightsarereservedbythePublisher,whetherthewholeorpartof the material is concerned, specifically the rights of translation, reprinting, reuse of illustrations, recitation,broadcasting,reproductiononmicrofilmsorinanyotherphysicalway,andtransmissionor informationstorageandretrieval,electronicadaptation,computersoftware,orbysimilarordissimilar methodologynowknownorhereafterdeveloped.Exemptedfromthislegalreservationarebriefexcerpts inconnectionwithreviewsorscholarlyanalysisormaterialsuppliedspecificallyforthepurposeofbeing enteredandexecutedonacomputersystem,forexclusiveusebythepurchaserofthework.Duplication ofthispublicationorpartsthereofispermittedonlyundertheprovisionsoftheCopyrightLawofthe Publisher’s location, in its current version, and permission for use must always be obtained from Springer.PermissionsforusemaybeobtainedthroughRightsLinkattheCopyrightClearanceCenter. 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Printedonacid-freepaper SpringerispartofSpringerScience+BusinessMedia(www.springer.com) Contents Spices:TheSavoryandBeneficialScienceofPungency .................... 1 BerndNiliusandGiovanniAppendino FreeFattyAcidReceptorsandTheirRoleinRegulationofEnergy Metabolism .................................................................... 77 TakafumiHara,IkuoKimura,DaisukeInoue,AtsuhikoIchimura, andAkiraHirasawa v Spices: The Savory and Beneficial Science of Pungency BerndNiliusandGiovanniAppendino “IntheBeginningWastheSpice.”S.Zweig,“Magellan”, 1938 Abstract Spicy food does not only provide an important hedonic input in daily life, buthas also been anedoctically associated tobeneficial effects on our health. In this context, the discovery ofchemesthetic trigeminal receptorsand their spicy ligands has provided the mechanistic basis and the pharmacological means to investigate this enticing possibility. This review discusses in molecular terms the connection between the neurophysiology of pungent spices and the “systemic” effectsassociatedtotheirtrigeminality.Itcommenceswithaculturalandhistorical overview on the Western fascination for spices, and, after analysing in detail the mechanismsunderlyingthetrigeminalityoffood,themaindietaryplayersfromthe transient receptor potential (TRP) family of cation channels are introduced, also discussing the “alien” distribution of taste receptors outside the oro-pharingeal cavity. The modulation of TRPV1 and TRPA1 by spices is next described, discussing how spicy sensations can be turned into hedonic pungency, and analyzing the mechanistic bases for the health benefits that have been associated totheconsumptionofspices.Theseinclude,inadditiontoabeneficialmodulation of gastro-intestinal and cardio-vascular function, slimming, the optimization of skeletal muscle performance, the reduction of chronic inflammation, and the pre- ventionofmetabolicsyndromeanddiabetes.Weconcludebyreviewingtheroleof electrophilicspiceconstituentsoncancerpreventioninthelightoftheiractionon B.Nilius(*) KULeuvenDepartmentofCellularandMolecularMedicine,LaboratoryofIonChannel Research,Leuven,Belgium e-mail:[email protected] G.Appendino DipartimentodiScienzedelFarmaco,Novara,Italy e-mail:[email protected] RevPhysiolBiochemPharmacol,doi:10.1007/112_2013_11, 1 #SpringerInternationalPublishingSwitzerland2013 2 B.NiliusandG.Appendino pro-inflammatory and pro-cancerogenic nuclear factors like NFκB, and on their interaction with the electrophile sensor protein Keap1 and the ensuing Nrf2- mediated transcriptional activity. Spicy compounds have a complex polyphar- macology, and just like any other bioactive agent, show a balance of beneficial and bad actions. However, at least for moderate consumption, the balance seems definitelyinfavourofthepositiveside,suggestingthataspicydiet,acaveman-era technology,couldbeseriouslyconsideredinadditiontocaloriccontrolandexercise as a measurement to prevent and control many chronic diseases associate to malnutritionfromaWesterndiet. Contents 1 Introduction................................................................................ 2 2 AHistoricalCulturalSojourn:TheRoleofSpicesinHistory.......................... 3 3 TheTasteMachinery...................................................................... 8 4 TheAlienTasteReceptors................................................................ 16 5 TheChemestheticSystem................................................................ 21 6 SpicyPlants............................................................................... 23 6.1 TheCaseofTRPV1................................................................. 26 6.2 “Irritant”Pungency:TRPA1ANewPlayer....................................... 29 6.3 AGustatoryandBeneficialTRPM5Connection.................................. 33 7 Spices,TRPsandHealth.................................................................. 34 7.1 SpicesandObesity................................................................. 35 7.2 ASkeletalMuscleConnection.................................................... 39 7.3 SpicesAgainstPain................................................................ 41 7.4 SpicesAgainstCancer............................................................. 43 7.5 ACytoprotectiveandAnti-inflammatoryActionofSpices...................... 48 7.6 AntimicrobicActionofSpices.................................................... 50 7.7 SpicesinGastro-intestinalDiseases.............................................. 52 7.8 DoSpicesGoCardio-vascular?................................................... 53 7.9 TRPA1andCough................................................................. 55 7.10 ASpicyPancreasConnection?.................................................... 56 7.11 AnActionofSpicyChannelActivatorsintheBrain?........................... 57 7.12 ABoneConnection?............................................................... 58 8 ConcludingRemarks...................................................................... 61 References........................................................................................ 62 1 Introduction Chemesthesis is the sensation induced by the chemical activation of gustatory receptorsothersthanthosefortasteandodor. Thesereceptors mediatepain,touch, texture (mechanical), and thermal perception, substantially modifying what is perceived as “food taste”. The notion that the same food tastes differently when warmorcold,whenshreddedorcoarse,whenplainorseasonedwithtiny(catalytic, in the lingo of chemistry) amounts of spices may seem a truism, but its molecular basesanditsimplicationsarenot.Ingeneral,theacceptanceoffooddependsnotonly on taste, but also on olfactory, tactile and visual cues, as well as on memories of Spices:TheSavoryandBeneficialScienceofPungency 3 previous, similar experiences and social expectations. Food palatability and its hedonic value play therefore a central role in nutrition, and one of the most fascinatingaspectsoftheserelationshipsishowfoodtasteismodifiedbyreceptors thatmainlyprovideaspicyflavor.Humansaretheonlyanimalswhichdeliberately and systematically consume spices with a pungent, “hot”, or even slightly painful note, raising the issue of the biological significance of this behavior, and what its possible evolutionary impact might have been. If, during evolution, taste has determined the discrimination between beneficial and harmful nutrients, chemesthesis has probably added another quality, namely, a hedonic experience associated to some health benefits. While there is no shortage of review articles and even books on the beneficial effects of spices, the molecular bases of their perceptionassuchhasreceivedlittleattentionoutsidetherealmofneurophysiology, where spice constituents have provided the tools to identify a series of sensory receptors of wide biomedical relevance. This review tries to fill this gap, summarizing the relationships between the basic mechanisms of taste and those ofchemesthesis.ThemechanismsbywhichchemestheticTRPchannelscontrolthe intake of a host of spicy, often electrophilic, food compounds will be analyzed, discussinghowspicesmightprovideasensorycluetopotentiallybeneficialhealth effects. 2 A Historical Cultural Sojourn: The Role of Spices in History The detection of eatable food was dramatically changed when our ancestors stood up on 2 ft. Not anymore close with their nose to earth, they complemented the decrease of anterograde olfaction with sight, taste and retrograde olfaction (Shepherd2012),developinganticipativetasteexperiencestocontrolfoodintake, often a decision of life or death (Wrangham 2009). In consideration of the brain neuronal network associated to food intake, neuronutrition might be a justified neologismforthe“neurological”integrationoftheinputsfromtaste,olfaction,and chemesthesis into a decision on the palatability of a specific food source. Spices havethepotentialtoupregulateourresponsetofood,andthisexplains,inpart,the role they have played in human history. The amazing, pantagruelic appetite of Europe for spices was not only a matter of culinary taste, but also of social and emotional reasons. We are amazed when we read that the Roman Emperor Heliogabalus, thequintessenceofdepravation,wasseasoninghisroastswithgold powder,buthiscontemporarieswouldhavebeenevenmorestartledbyseeingthe profligacybywhichspiceslikecinnamon,pepper,andclovesarenowadaysusedin cuisine and even in soft drinks. Thus, ginger ale contains ginger, Coca Cola is rumored to contain a huge variety of spices like a smo¨rga˚sbord that includes cinnamon and nutmeg, and spices are used in profligacy to fortify energy drinks. Incidentally,wehavemanagedtooutperformHeliogabalus,sincenotonlygold,but also edible silver and even platinum are now commercially available for culinary use, and are claimed to improve brain function (see the site eat gold and also the moonhill.jpwebsite). 4 B.NiliusandG.Appendino There is convincing evidence for the trade of cloves from the remote and minuscule Spice Islands in Indonesia, where Syzygium aromaticum (L.) Merril & Perryisendemic,totheMiddleEastasearlyasin1700BC(Turner2004),andmost spiceswerewellknownintheAncientWorld.Thus,weknowthatcinnamonwas more valuable than gold in the ancient Egypt (2000 BC), and a plethora of spices are mentioned in the Egyptian Ebers Papyrus (1550 BC), a description of 700 natural agents used for medical purposes and the oldest example of a pharmaco- poeia. Over 1,000 years later, Hippocrates of Cos (460–377 BC) described the use of spices (out of 400 natural agents) as remedies for digestion disturbances (in Corpus Hippocratium) (Ji et al. 2009), also suggesting that broccoli, which contain activators of the ion channel TRPA1, can be useful to treat, inter alia, headache. The ancient literature is full of “anticipations” of modern discoveries, generally vaguely expressed and better recognized a posteriori. For instance, wormwood(ArtemisiaabsinthiumL.)wasalreadyrecommendedasananti-malaria remedy,probablybecauseofitsapocalypticbitterness(Touwaide2012),andeven clues on the molecular mechanism of action of spices can be identified in the ancient literature. Thus, in his De Anima (translated as “The soul” in English, DAII.7–11),Aristotle(384BC–322BC),whilediscussingsenses(inthefollowing order:sight,sound,smell,taste,andtouch–onechapterforeach,and,incidentally, giving more relevance to touch than to olfaction) (Hamlyn 1968; Sachs 2011), mergedheat,coldandtouchtogether,anticipatingthecriticalinvolvementofTRPs inallthesesensations. After the Romans discovered the burning and irritating taste of the Oriental ingredients during their expeditions and wars, the Western World could not miss anymorethe“especerias”fromIndiaandArabia,thatbecameapleasureandnota necessity to survive. The Roman cuisine made abundant use of many herbs and spices, to the point that the Greek historian Plutarch (c. 45–120 AD), bemoaning the need touse somanyspices totreat meat, commented that: “we mixoil, wine, honey,fishpaste,vinegar,withSyrianandArabianspices,asthoughwewerereally embalming a corpse for burial”. On the other hand, the frugal Roman statesman Cato the Elder (234–149 BC) recommended his Roman citizens to cultivate broccoli,andtousethemasaremedyagainstgastro-intestinaldiseases(Touwaide 2012).AlthoughmodernEuropeansassociatespiceswithIndiaandtheFarEast,the most celebrated and expensive spice of the ancient world was silphion, a product coming from the Mediterranean area. Silphion is a gum-resin, obtained from a FerulaspeciesthatgrewexclusivelyaroundCyrene,intoday’sLibya.Silphionwas moreexpensivethansilverandgold,andacquiredasortofstatussymbolallover the Greek-Roman world. After centuries of over-exploitation, gastronomic merits andallegedaphrodisiacpropertieseventuallycondemnedSilphiontoextinctionin the first century AD. Silphion is considered the first documented case of the extinction of a plant by humans (McGee 2001). The replacement of Silphium cyrenaicumwiththecheaperSilphiumparticum(asafetida,a.k.a.Stercumdiabuli) suggeststhat,justliketheinfamousgarumbasedonfermentedfish.Alsosilphium hadaratherstrongflavor.Interestingly,someMediterraneanFerulaspeciescontain high concentration of ferutinin, one of the most potent phytoestrogens known,
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