handbook of seafood quality, safety and health applications (alasalvar/handbook of seafood quality,...

P1: SFK/UKS P2: SFKc42 BLBK298-Alasalvar August 5, 2010 18:25 Trim: 244mm×172mm

42 Functional and nutraceutical ingredientsfrom marine macroalgae

Tao Wang, Guðrun Olafsdottir, Rosa Jonsdottir,Hordur G. Kristinsson, and Ragnar Johannsson

42.1 Introduction

Accumulating scientific evidence on the relationship between diet and health has demon-strated that food products with beneficial components can improve the state of well-beingand reduce the risk of common diseases. A growing number of health conscious consumershave created a demand for food products with health promoting benefits. Therefore, searchfor new ingredients with biological activity from natural resources is gaining great interestamong researchers.

Marine macroalgae have a long history of use as food and folk medicine in Asia and aretraditionally well-known for their versatile health benefits. Marine algae are not only a richsource of dietary fibre, proteins, vitamins, and minerals, but also contain a great variety ofsecondary metabolites with diverse biological activities, which cannot be found in terrestrialplants. Therefore, the potential application of seaweed as a source of functional additives withhealth beneficial properties is a new target for exploration. In recent years, a number of potentantioxidant compounds have been isolated and identified from different types of edible sea-weeds. In particular, phlorotannins (polyphloroglucinol phenolics) derived from brown algaehave been shown to possess multiple physiological activities such as antioxidant, anticarcino-genic, antibacterial, anti-inflammatory, and anti-allergic properties (Table 42.1). Other bioac-tive compounds of importance in macroalgae are sulphated polysaccharides, dietary fibre,polyunsaturated fatty acids (PUFA), sterols, carotenoids, and �-tocopherol [1]. This chapterdiscusses recent investigations on functional and nutraceutical ingredients from marine algae,with emphasis on the biological activities of algal polyphenols and sulphated polysaccharides.

42.2 Functional and nutraceutical propertiesof polyphenols from marine algae

42.2.1 Occurrence and chemical structure of algal polyphenols

Marine macroalgae are a rich source of polyphenols. A series of phenolic compounds suchas catechins (e.g. gallocatechin, epicatechin, and catechin gallate), flavonols, and flavonol

Handbook of Seafood Q uality, Safety and Health Applications

Edited by Cesarettin Alasalvar, Fereidoon Shahidi, Kazuo Miyashita and Udaya Wanasundara

© 2011 Blackwell Publishing Ltd. ISBN: 978-1-405-18070-2


Ingredients from marine macroalgae 509

Tab

le42.1

Som

eex

ampl

esof

bioa

ctiv

ein

gred

ient

sis

olat

edfr

omm

arin

eal

gae

and

thei

rm

ultif

unct

iona

lpro

pert

ies

Bio

act

ive

ing

red

ien

tsA

lga

esp

eci

es

Bio

act

ivit

yR

efe

ren

ce

Phlo

rota

nnin

sP

ha

eop

hyc

ea

e:

Eckl

onia

cava

,Eck

loni

aku

rom

e,Ec

klon

iast

olon

ifera

,Eis

enia

bicy

clis

,Eis

enia

Arb

orea

,Fuc

usve

sicu

losu

s,Fu

cus

spira

lis,F

ucus

serr

atus

,Asc

ophy

llum

nodo

sum

,Sa

rgas

sum

kjel

lman

ianu

m,S

arga

ssum

ringg

oldi

anum

,Sa

rgas

sum

siliq

uast

rum

,Ish

ige

okam

urae

Ant

ioxi

dant

,ant

i-in

flam

mat

ory,

anti-

alle

rgic

,an

ti-tu

mou

r,an

ti-di

abet

ic,a

ntib

acte

rial,

HIV

-1re

vers

etr

ansc

ripta

sean

dpr

otea

sein

hibi

tory

activ

ities

,che

mop

reve

ntio

nag

ains

tsev

eral

vasc

ular

dise

ases

[8,1

6,17

,19,

45,4

6]

Sulp

hate

dpo

lysa

ccha

rides

Ph

aeop

hyc

ea

e:

Lam

inar

iaja

poni

ca,E

cklo

nia

cava

,Eck

loni

aku

rom

e,U

ndar

iapi

nnat

ifida

,Fuc

usve

sicu

losu

s,Fu

cus

evan

esce

ns,A

scop

hyllu

mno

dosu

m,P

adin

agy

mno

spor

a,D

icty

ota

men

stru

alis

,Spa

togl

ossu

msc

hroe

deri,

Sarg

assu

mfu

sifo

rme,

Sarg

assu

mth

unbe

rgii,

Sarg

assu

mst

enop

hyllu

m,

Surg

assu

mla

tifol

ium

,Sar

gass

umfu

lvel

lum

Rh

od

op

hyc

ea

e:

Gig

artin

ask

otts

berg

ii,C

hond

rus

ocel

latu

s,Po

rphy

raha

itane

sis,

Gra

cila

riaco

rnea

,Gra

telo

upia

filic

ina,

Gra

telo

upia

long

ifolia

Ch

loro

ph

ycea

e:

Ulv

ape

rtus

a,U

lva

cong

loba

ta,C

odiu

mpu

gnifo

rmis

,Cod

ium

cylin

dric

um,M

onos

trom

aan

gica

va,

Mon

ostr

oma

latis

sim

um,M

onos

trom

ani

tidum

Ant

ioxi

dant

,ant

icoa

gula

nt,a

nti-

infla

mm

ator

y,an

tivira

l,an

tibac

teria

l,an

ti-tu

mou

r,an

tivas

culo

geni

c,an

tithr

ombo

tic,

imm

unom

odul

ator

y,ra

diop

rote

ctiv

eac

tiviti

es

[21,

23,2

4,26

–30,

47,4

8]

Fuco

xant

hin

Ph

aeop

hyc

ea

e:

Hiji

kia

fusi

form

is, U

ndar

iapi

nnat

ifida

,La

min

aria

japo

nica

Ant

ioxi

dant

,ant

icar

cino

geni

c,an

ti-ob

esity

,an

ti-di

abet

es,a

nti-

infla

mm

ator

yac

tiviti

es[3

3–35

,37,

38]

Ster

ols

Ph

aeop

hyc

ea

e:

Pelv

etia

siliq

uosa

,Sar

gass

umca

rpop

hyllu

m,

Sarg

assu

mm

utic

um,S

arga

ssum

parv

ives

icul

osum

,Eck

loni

ast

olon

ifera

Ch

loro

ph

ycea

e:

Ulv

ala

ctuc

a

Ant

ioxi

dant

,ant

i-di

abet

es,a

nti-

infla

mm

ator

y,an

ti-tu

mou

r,an

tibac

teria

l,nh

ibiti

onin

Alz

heim

er’s

dise

ase

[40,

41,4

9]

Bioa

ctiv

epe

ptid

esP

ha

eop

hyc

ea

e:

Ura

daria

pinn

atifi

da,S

arga

ssum

carp

ophy

llum

,Sar

gass

umfu

lvel

lum

,Sar

gass

umho

rner

i,Sa

rgas

sum

core

anum

,Ish

ige

okam

urae

,Eck

loni

aca

vaR

hod

op

hyc

ea

e:

Porp

hyra

yezo

ensi

sC

hlo

rop

hyc

ea

e:

Chl

orel

lapy

reno

idos

a

Ant

ihyp

erte

nsiv

e,an

tioxi

dant

,ant

imic

robi

al,

min

eral

-bin

ding

,im

mun

omod

ulat

ory,

antic

arci

noge

nic,

antiv

iral,

opio

idac

tiviti

es

[42–

44]

PUFA

(n-3

)P

ha

eop

hyc

ea

e:

Und

aria

pinn

atifi

da,H

izik

iafu

sifo

rme,

Him

anth

alia

elon

gata

,Lam

inar

iaoc

hrol

euca

Rh

od

op

hyc

ea

e:

Porp

hyra

spp.

,Pal

mar

iast

enog

ona,

Poly

siph

onia

urce

olat

a,Pa

chym

enio

psis

lanc

eola

ta,G

elid

ium

aman

sii,

Cho

ndria

cras

sica

ulis

Ch

loro

ph

ycea

e:

Ulv

afe

nest

rate

Ant

i-in

flam

mat

ory,

anti-

tum

our,

antiv

iral,

antim

icro

bial

activ

ities

,pre

vent

ion

ofco

rona

ryhe

artd

isea

se,t

hrom

bosi

s,at

hero

scle

rosi

s

[1,5

0,51

]


510 Seafood Quality, Safety and Health Applications

glycosides have been identified from methanol extracts of red and brown algae [2–4].Phlorotannins, the largest group of polyphenols in marine brown algae, exhibit many in-teresting physiological activities (Table 42.1). They have been identified from Eckloniacava, Ecklonia stolonifera, Eisenia bicyclis, Sargassum kjellmanianum, Sargassum ring-goldianum, Fucus vesiculosus, Fucus serratus, and Ascophyllum nodosum.

Based on the type of structural linkages between the phloroglucinol sub-units(diphenylethers or biphenyls) and on the number of additional hydroxyl groups, phlorotan-nins can be systematically classified into six major subclasses: phlorethols, fucols, fuhalols,fucophlorethols, isofuhalols, and eckols [5,6]. The chemical structures of common algalphlorotannins are presented in Fig. 42.1.

Fucols are phlorotannin polymers in which the phloroglucinol units are connected only byC–C (aryl–aryl) bonds. The phloroglucinol units in phlorethols are linked only by C–O–C(aryl–ether) bonds. Fucophlorethols contain both biaryl and aryl–ether linkages. Fuhalolsare connected exclusively via ether bonds. Eckols are characterized by the occurrence ofat least one three-ring moiety with a dibenzo-1,4-dioxin unit substituted by a phenoxylgroup at the C-4 position. Isofuhalols and endofucophlorethols are small, specialized groupsisolated from specific algal genera. Moreover, some phlorotannins can also be sulphated orhalogenated [5].

42.2.2 Antioxidant activity of algal polyphenols

42.2.2.1 In vitro antioxidant properties of algal polyphenols

Different species of seaweed display varying degrees of antioxidant activity. Brown seaweedsgenerally show better antioxidant capacities than green and red seaweeds. In particular, somespecies such as F. vesiculosus, E. cava, and S. ringgoldianum have been reported to possessremarkably high antioxidant potential. Fifty percent ethanol extracts of 25 common seaweedspecies from the Japanese coast were screened for their antioxidant activities [7]. The highestradical scavenging effect was obtained for S. ringgoldianum. The chemical structure of thephlorotannin was identified as a bifuhalol oligomer based on matrix-assisted laser desorp-tion/ionization time-of-flight mass spectrometry (MALDI-TOF MS) analysis. The partiallypurified phlorotannin-rich fraction exhibited significant scavenging potencies on superoxideanion radicals, which were around five times higher than that of catechin. Recently, the au-thors studied the potential antioxidant activities of water and 70% acetone extracts from tenspecies of Icelandic seaweeds [8]. The results of this screening experiment showed that thedifferent seaweed species contained different levels of total phenolics and possessed diverseantioxidant properties. Three fucoid species (F. vesiculosus, F. serratus, and A. nodosum)exhibited the greatest scavenging activities against 2,2-diphenyl-1-picrylhydrazyl (DPPH)and peroxyl radicals as well as considerable ferrous ion-chelating abilities.

Previous studies have shown that phenolic compounds are the main contributors to theantioxidant activity of various seaweeds. A positive correlation has been well documentedbetween total phenolic content (TPC) and antioxidant activity of different seaweed extractsby many researchers. However, some studies reported poor or low correlation coefficientsbetween TPC and antioxidant activities of several seaweed extracts. Other active compounds,such as fucoxanthin and sterols in solvent extracts and water-soluble sulphated polysaccha-rides, proteins or peptides, ascorbic acid, and glutathione (GSH) in water and enzymaticextracts, could also contribute partially to the overall antioxidant activity.



Phloroglucinol Triphlorethol A

Tetrafucol A Tetrafuhalol A

OH

HO

OH

OH

OH

O

OO

OH

OH

O

HO OH

O

Phlorofucofuroeckol Dieckol

OH

OHHO

OH

OH

OH

OHHO

OH

OH

OO

OH

O

O

OH

OH

O

HO OH

HO

O

OH

O

O

OH

OH

O

OH

OH

OH

OH

OHHOOH

OH

HO

HO

OHHO OH

OH

HO

OH

HO

O

HO

OHOHO

O

HO

HO

HO

OHHO

Fig. 42.1 Chemical structures of common algal phlorotannins.



42.2.2.2 Antioxidant mechanism and structure-antioxidant activityrelationship of algal polyphenols

Plant and algal derived phenolic compounds have been shown to act as potent antioxidantsin various systems, although some plant phenolics have sometimes been found to havepro-oxidant properties under certain conditions [9–10]. However, neither the antioxidantmechanism nor the structure-activity relationship of algal polyphenols has been fully eluci-dated up to date. The putative mechanisms have been associated with free radical scavenging,singlet oxygen quenching, transition metal ion chelation, and reducing power.

Many studies have demonstrated that phenolic compounds are potent free radical scav-engers [9,11]. However, there are contradictory reports in the literature regarding metalchelating abilities of polyphenols. Some studies have shown that polyphenols derived frombrown algae are potent ferrous ion chelators [12,13]. In contrast, other authors have reportedthat metal chelation played a minor role in the overall antioxidant activities of several plant-derived phenolic compounds [14]. In agreement with this, our study on various seaweedsusing different antioxidant assays indicated that ferrous ion-chelating ability of seaweedextracts correlated neither with TPC nor with DPPH radical scavenging activity or oxygenradical absorbance capacity (ORAC). Therefore, the major role of algal polyphenols ap-peared to be as potent radical scavengers and primary, chain-breaking antioxidants [8]. Othercomponents such as polysaccharides, proteins, or peptides may be more important for theobserved chelating effects of the extracts.

Several studies have reported that high molecular weight (HMW) phlorotannins exhibitmore potent antioxidant activities than the monomer phloroglucinol. It was postulated thatoligomerization of phloroglucinol may be crucial for the enhancement of the radical scav-enging activity. However, no clear correlation was found between the antioxidant activityand structural characterization of the polymer.

Yan et al. [15] reported that HMW phlorotannins from S. kjellmanianum were moreeffective than those of their low molecular weight (LMW) counterparts to prevent rancidityin fish oil. The antioxidant activity of HMW phlorotannins at a concentration of 1% wasabout 2.6 times higher than that of 0.02% butylated hydroxytoluene (BHT).

Recently, Shibata et al. [16] isolated and identified several phlorotannins, including eckol,phlorofucofuroeckol A, dieckol, and 8,8′-bieckol from the Japanese Laminariaceous brownalgae (E. bicyclis, E. cava, and Ecklonia kurome). All phloroglucinol oligomers displayedpotent DPPH radical scavenging activity and were approximately twice as effective ascatechin, ascorbic acid, and �-tocopherol. With the exception of eckol, all phlorotanninsexhibited extraordinary superoxide anion radical scavenging ability, which were around 2 to10 times more effective than ascorbic acid and �-tocopherol. The varying radical scavengingproperties of phlorotannin polymers may be contributed by the phenolic hydroxy groupsattached to the eckol skeleton.

42.2.3 Other biological activities of algal polyphenols

Recent studies have revealed that algal polyphenols, especially phlorotannins derived frombrown algae not only exhibit potent antioxidant activities but also possess many other biologi-cal activities, including anti-inflammatory, anti-allergic, anti-tumour, anti-diabetic, antibacte-rial, HIV-1 reverse transcriptase, and protease inhibitory activities as well as chemopreventionagainst several vascular diseases (Table 42.1). Their multiple physiological activities offer



many advantages for potential applications in nutraceutical, pharmaceutical, and cosmeticindustries.

42.2.3.1 Angiotensin I-converting enzyme (ACE) inhibitory propertiesof algal polyphenols

Jung et al. [17] studied the ACE inhibitory properties of ethanol extracts from 10 edibleKorean seaweeds, including five Phaeophyceae (E. stolonifera, E. cava, Pelvetia siliqu-osa, Hizikia fusifome, and Undaria pinnatifida), four Rhodophyceae (Gigartina tenella,Gelidium amansii, Chondria crassicaulis, and Porphyra tenera) and one Chlorophyceae(Capsosiphon fulvescens). E. stolonifera and E. cava possessed the highest inhibitory activi-ties. Six phlorotannin compounds were further isolated from E. stolonifera. The compoundsphlorofucofuroeckol A, eckol and dieckol, showed remarkably high inhibitory activities,whereas phloroglucinol showed no activity within the tested concentrations (163.93 �g/mL).Although the structure–activity relationship of the phlorotannins has not yet been established,a closed-ring dibenzo-1,4-dioxin moiety in the molecular skeleton seems to be crucial fortheir ACE inhibitory properties. Moreover, the presence of another dibenzofuran ring mayalso enhance the inhibitory effects.

42.2.3.2 Human immunodeficiency virus (HIV) inhibitory propertiesof algal polyphenols

A large-scale screening experiment was carried out to study the inhibitory activities of 47types of Korean seaweeds on HIV type 1 (HIV-1) reverse transcriptase (RT) and HIV-1integrase (IN) [18]. One of the 4 Chlorophyceae, 8 of the 17 Phaeophyceae, and 6 of the 26Rhodophyceae showed inhibitory activities against HIV-1 RT. Five brown algae possessedinhibitory effects on the 3′-processing activity of HIV-1 IN. In particular, the ethyl acetate(EtOAc) fraction of E. cava strongly inhibited both the HIV-1 RT and IN activities. Inanother study, they further isolated four phlorotannin compounds from the EtOAc fractionof E. cava and evaluated their inhibitory activities against HIV-1 RT and protease [19]. Thecompounds 8,8′-bieckol and 8,4′′′-dieckol had strong inhibitory effects on the HIV-1 RTactivity, whereas eckol and phlorofucofuroeckol A did not exhibit anti-HIV-1 RT activity.Furthermore, the inhibitory activity against HIV-1 RT of 8,8′-bieckol was 10-fold higherthan that of 8,4′′′-dieckol. The difference in the inhibition potential of these two compoundsappears to be related to the steric hindrance of the hydroxyl and aryl groups near the biaryllinkage of 8,8′-bieckol.

42.3 Functional and nutraceutical properties of sulphatedpolysaccharides from marine algae

Over the past decade, many studies have demonstrated that the sulphated polysaccha-rides from marine algae possess excellent biological properties, including antioxidant,anticoagulant, anti-inflammatory, antiviral, antibacterial, anti-tumour, antivasculogenic,antithrombotic, immunomodulatory, and radio-protective activities (Table 42.1). Particularlyfucoidans, a unique class of sulphated fucans, have been extensively studied due to theirdiverse biological activities. They have been isolated mainly from several orders of brown



algae (Phaeophyceae) such as Fucales and Laminariales, but also from Chordariales,Dictyotales, Dictyosiphonales, Ectocarpales, and Scytosiphonales [20].

42.3.1 Antioxidant activity of sulphated polysaccharides

Sulphated polysaccharides derived from Laminaria japonica, E. kurome, F. vesiculosus, andUlva pertusa have been found to possess excellent antioxidant potency. Due to their HMWand heterogeneous structures, the correlation between the structure and antioxidant activityof sulphated polysaccharides has not been fully characterized. However, their antioxidantactivity seems to be highly related to several structural parameters such as the degree ofsulphation (DS), the sulphation position, the molecular size, monosaccharide composition,and glycosidic branching. Type of linkage and molecular geometry are also involved inexhibited antioxidant activity [21].

Tsipali et al. [22] compared the free radical scavenging activities of glucan and nonglucanpolymers. Phosphated and sulphated glucan exhibited higher antioxidant potentials thanglucan and other neutral polysaccharides. Moreover, the monosaccharide constitution alsohas an impact on the free radical scavenging activity of a variety of carbohydrate polymers.When the monosaccharides were arrayed in a polymer molecule, enhanced antioxidant abilitywas observed [22].

Qi et al. [21] reported that polysaccharides from U. pertusa with high sulphate contentand LMW exhibited stronger reducing power and radical scavenging activities than othersulphated polysaccharides. Zhao et al. [23] also observed that LMW sulphated polysaccha-rides (8,000–10,000 Da) from brown algae, L. japonica possessed high scavenging abilitiesagainst superoxide, hydroxyl, and hypochlorous acid radicals. More recently, they furtherdemonstrated that the chemical composition such as glucuronic acid and fucose contentcould also influence the scavenging effects [24].

42.3.2 Other functional properties of sulphated polysaccharides

42.3.2.1 Anticoagulant activities of sulphated polysaccharides

Anticoagulant activities are one of the most intensely studied properties of sulphated polysac-charides. Sulphated polysaccharides derived from marine algae are effective coagulationmodulators and have the potential to be used as alternatives to heparin, a conventional an-ticoagulant drug. Different sulphated polysaccharides with potent anticoagulant activitieshave been isolated from several brown algae such as F. vesiculosus, A. nodosum, Pad-ina gymnospora, Dictyota menstrualis, and Spatoglossum schroederi, red algae Gigartinaskottsbergii, and green algae Codium cylindricum, Ulva conglobata, Monostroma nitidum,and Monostroma latissimum (Table 42.1).

Fucoidans have been reported to possess powerful in vitro and in vivo anticoagulantproperties, which have many advantages over cattle-derived heparin. Fucoidans purified fromF. vesiculosus and A. nodosum have been patented as anticoagulant drugs. The anticoagulantactivities of fucoidans can be attributed to direct fucan-thrombin interaction and are highlyrelated to DS and MW. Colliec et al. [25] observed that the anticoagulant activity of fucoidanwas reduced with a decrease in the MW. A HMW fraction (58 kDa) was found to possessrather high thrombin inhibitory property, while a LMW of 21 kDa only showed moderateactivity. The anticoagulant activity of fucoidan is believed to be mediated by heparin cofactor



II and/or antithrombin III. Fucoidan also enhances plasma clot lysis and the activation ofplasminogen by tissue-type plasminogen activator (t-PA) or urokinase.

Sulphated polysaccharides isolated from several Monostroma species (Chlorophyceae)also show potent anticoagulant activities. Two different sulphated polysaccharides fromM. latissimum and M. nitidum have been reported to exhibit stronger antithrombin activitiesthan that of heparin or dermatan sulphate [26]. Recently, Zhang et al. [27] compared thethrombin inhibitory effects of a sulphated polysaccharide from M. latissimum and its frag-ments with different MW. The MW had profound influence on the anticoagulant activity.A relatively longer saccharide chain length is required for better thrombin inhibition. Thesulphated polysaccharides with high sulphate content have also been found to be desired foranticoagulant activity.

42.3.2.2 Anti-tumour activities of sulphated polysaccharides

Sulphated polysaccharides from marine algae have been found to have potent anti-tumouractivities as well as lower side-effects. These sulphated polysaccharides including fucoidanisolated from brown algae L. japonica, U. pinnatifida, Sargassum thunbergii, and Fu-cus evanescens, �-carrageenan polysaccharides from red algae Chondrus ocellatus, and�-carrageenan oligosaccharides from Kappaphycus striatum. However, contradictory re-ports can be found in the literature regarding the biochemical and molecular principles ofthese anti-tumour polysaccharides. Some studies showed that only HMW fractions (MW�16,000 Da) of partially hydrolyzed glucan polysaccharides had anti-tumour activity. Incontrast, other authors reported that the anti-tumour activity was dependent upon their basicstructure-oligosaccharide unit. The heptasaccharides present in the polysaccharides exhib-ited even higher activity than the polysaccharides themselves [28]. The study conductedby Yuan and Song [29] showed that the MW had great impact on the anti-tumour ac-tivity of carrageenan polysaccharides. Degradation of kappa-carrageenan polysaccharidesinto oligosaccharides could enhance the biological activity. The tumour inhibitory activitiesof carrageenan oligosaccharides may be attributed to their recognition or interaction withthe tumour-specific oligosaccharide molecules. Further studies are needed to elucidate therelationship between structural features and anti-tumour activities.

42.3.2.3 Antiviral activities of sulphated polysaccharides

Sulphated polysaccharides derived from different brown and red algae have been demon-strated to possess remarkable antiviral activities against viruses responsible for human in-fectious diseases, including herpes simplex virus (HSV) types 1 and 2, respiratory syncytialvirus (RSV), human cytomegalovirus (HCMV), influenza virus, and bovine viral diarrhoeavirus. Furthermore, most of the algal polysaccharides have very low cytotoxic activities to-wards mammalian cells, which represent a potential new source for the development of saferantiviral agent.

Sulphated polysaccharides obtained from different brown algae such as Caulerpa spp.,Corallina spp., Hypnea charoides, Padina arborescens, and Sargassum patens have shownpotent antiviral activities against HSV types 1 and 2 with low levels of cytotoxicity. Partic-ularly, fucoidans have demonstrated an extraordinary antiviral activity towards HSV types1 and 2, RSV, and HCMV. The antiviral mechanism seems to be related to their inhibitioneffects on the binding of the viral particle to the host cell [30]. Other sulphated polysaccha-rides from red algae, such as galactan sulphate and sulphated xylomannan, are also good



C

OCOCH3HO

H

HO

O

O

Fucoxanthin

Fucoxanthinol

H

C

OHHO

HO

O

O

Fig. 42.2 Structure of fucoxanthin and fucoxanthinol.

candidates for further development of novel antiviral drugs. These polysaccharides have beenfound to be active during the initial stage of the RNA virus replication when the virus adsorbsonto the surface of the host cell [30].

42.4 Functional and nutraceutical propertiesof fucoxanthin from marine algae

Fucoxanthin, along with �-carotene, is one of the most abundant carotenoids found in nature.In marine macroalgae, high concentrations have been found in several edible brown algaesuch as Hijikia fusiformis, U. pinnatifida, and Sargassum fulvellum. However, it is absentin green and red algae. Fucoxanthin has a unique structure including an unusual allenicbond and 5,6-monoepoxide in its molecule [31] (Fig. 42.2). It can easily be converted tofucoxanthinol in human intestinal cells and mice. Therefore, fucoxanthinol may be the activeform in the biological system [32]. Recently, the potential application of fucoxanthin inpharmaceutical and nutraceutical fields has attracted an increasing interest due to its multi-functional properties including antioxidant, anticarcinogenic, anti-obesity, anti-diabetes, andanti-inflammatory activities (Table 42.1).

42.4.1 Antioxidant activities of fucoxanthin

Similar to other carotenoids, fucoxanthin derived from brown algae is well-known for itsantioxidant properties. Yan et al. [33] reported that the major carotenoid with DPPH radicalscavenging activities in brown alga H. fusiformis was all-trans-fucoxanthin. The quenchingof free radicals by fucoxanthin might stem from its ability to donate electron. More recently,a comprehensive study was carried out to evaluate the antioxidant activities of fucoxan-thin and its metabolites, fucoxanthinol and halocynthiaxanthin [34]. The radical scavengingand singlet quenching activities of fucoxanthin and fucoxanthinol were comparable or evensuperior to that of �-tocopherol. Interestingly, fucoxanthin exhibited considerable DPPH



radical scavenging activity, even under anoxic conditions, whereas other carotenoids includ-ing �-carotene, �-cryptoxanthin, zeaxanthin, and lutein generally had no activities [35]. Thesuperior radical quenching ability of fucoxanthin under anoxic conditions may be attributedto the presence of six oxygen atoms in its molecular skeleton, which ensures better interac-tion with free radicals. This distinct property is of great importance for the development ofnovel fucoxanthin-based antioxidant agent, since most tissues under physiological conditionsgenerally have low oxygen presence.

42.4.2 Anti-obesity effects of fucoxanthin

The seaweed carotenoid, fucoxanthin, has recently been found to possess potent anti-obesityeffects [36]. Feeding with fucoxanthin from edible brown algae U. pinnatifida significantlyreduced the weight of abdominal white adipose tissues (WAT) of both rats and mice [37].The mechanism of their anti-obesity properties may be related to the up-regulation of theexpression of the fat-burning protein UCP1 (uncoupling protein 1 or thermogenin) in WATaround the internal organs [38]. Fucoxanthin-induced expression of UCP1 in WAT resultsin the oxidation of fatty acids and heat generation, which directly reduce abdominal fat inanimals [39].

42.5 Functional and nutraceutical properties of sterolsfrom marine algae

Sterols are another class of interesting constituents of marine algae. Brown algae generallycontain higher level of sterols than red algae. Fucosterol and fucosterol derivatives are thepredominant sterols of brown algae. The major sterol in red algae is cholesterol. However,some species contain mainly demosterol or 22-dehydrocholesterol. Sterol composition ofgreen algae is much more complex and varied. Isofucosterol, cholesterol, chondrillasterol,poriferasterol, and ergosterol have been found to be the major sterols in various green algae.In recent years, sterols isolated from marine algae have been reported to exhibit diversebiological properties including antioxidant, anti-diabetes, anti-inflammation, anti-tumour,antibacterial, and inhibition in Alzheimer’s disease (Table 42.1).

42.5.1 Antioxidant activities of sterols from marine algae

In a study on antioxidant activities of fucosterol from brown algae P. siliquosa, it was ob-served that the serum transaminase activity was significantly decreased by fucosterol inCCl4-intoxicated rats [40]. It also induced an increase in the activities of different antioxi-dant enzymes including superoxide dismutase (SOD), catalase, and glutathione peroxidase.Therefore, fucosterol not only possesses antioxidant, but also hepatoprotective properties.

42.5.2 Anti-diabetic activities of sterols from marine algae

Fucosterol isolated from P. siliquosa was found to exhibit potent anti-diabetic potential [41].The hypoglycaemic effects of fucosterol is possibly due to the inhibition of hepatic glycogenbreakdown in the liver, the reduction of hepatic glyconeogenesis, and the enhanced peripheral



glucose consumption or the direct inhibition of insulin release in the liver. Further studiesare needed to elucidate the exact mechanisms of action.

42.6 Functional and nutraceutical properties of bioactivepeptides from marine algae

Over the years, many efforts have been made for the isolation, characterization, and identifica-tion of biologically active peptides from various food sources or protein hydrolysates. Thesepeptides have been found to possess multifunctional properties including antihypertensive,antioxidant, antimicrobial, mineral-binding, immunomodulatory, anticarcinogenic, antiviral,and opioid activities (Table 42.1). In this chapter, we have focused on the antihypertensiveactivities of the peptides derived from marine algae.

42.6.1 Antihypertensive effects of the peptides derivedfrom algae

Most peptides with antihypertensive activities are those derived from different food proteinsand processing by-products. Seaweeds have also proven to be good sources of antihyperten-sive peptides. In particular, peptides derived from the brown seaweed U. pinnatifida (wakame)and the red algae Porphyra yezoensis have been demonstrated to be potent inhibitor of ACE[42–43]. Controlled enzymatic hydrolysis is one of the most appropriate methods in theproduction of tailor-made peptides from parent protein with enhanced ACE inhibitory prop-erties. An earlier study conducted by Suetsuna and Nakano [44] showed that the peptidesfrom peptic hydrolysate of wakame had marked ACE inhibitory and antihypertensive activi-ties. Oral administration of these peptides significantly decreased the systolic blood pressureof spontaneously hypertensive rats (SHR). However, peptides of peptic digest of wakameshowed pronounced bitter taste, which limited their use as functional food ingredients. Inanother screening test, the authors compared the antihypertensive effects of 17 different pro-tease hydrolysates of wakame, among which the hydrolysate made with protease S ‘Amano’exhibited marked antihypertensive effect in both the single oral administration and long-termfeeding test to SHR [42]. Moreover, S ‘Amano’ was more effective than other enzymes toproduce a hydrolysate with improved sensory properties and high solubility in water.

42.7 Conclusions

Numerous scientific studies across many laboratories have demonstrated that marine algaecontain a great variety of components with diverse and unique biological activities, whichcannot be found in terrestrial plants. The claimed physiological activities include antioxi-dant, anticarcinogenic, anti-vasculogenic, antithrombotic, anti-diabetic, antiviral, antibacte-rial, anti-inflammatory, and anti-allergic, as well as immunomodulatory and radio-protectiveproperties. However, most of these studies have only been conducted at laboratory-scale andmainly use water or organic solvent extraction systems. These conventional techniques haveseveral drawbacks such as low selectivity, low extraction efficiency, solvent residue, andenvironmental pollution. Therefore, it is necessary to develop innovative technologies forextraction, separation, and purification of bioactive compounds from marine algae, including



supercritical fluid extraction, subcritical water extraction, pressurized fluid extraction,enzyme-assisted extraction, and membrane separation system. Further optimization andscale-up of these new technologies is crucial for successful commercial developments. Reli-able and high-throughput analytical techniques need to be developed for the qualitative andquantitative analysis of these compounds in different matrices. The claimed physiologicaleffects of some seaweed extracts or purified compounds have, so far, only been tested inrelatively fast and simple in vitro screening trials. Well-designed in vivo, animal, and humanclinical studies should be carried out to systematically evaluate the health benefits and po-tential risks of these bioactive ingredients. Studies on the impact of processing conditionson the stability and bioavailability of these compounds are scarce. The adverse interactionor complexation of seaweed extracts and purified compounds with other food ingredients(proteins, carbohydrates, and lipids) as well as the possible formation of toxic, allergenic, orcarcinogenic substances should also be addressed.

References

1. Plaza, M., Cifuentes, A. & Ibanez, E. (2008). In the search of new functional food ingredients fromalgae. Trends in Food Science & Technology, 19, 31–39.

2. Santoso, J., Yoshie, Y. & Suzuki, T. (2002). The distribution and profile of nutrients and catechins ofsome Indonesian seaweeds. Fisheries Science, 68(Suppl.), 1647–1648.

3. Yoshie, Y., Wang, W., Petillo, D. & Suzuki, T. (2000). Distribution of catechins in Japanese seaweeds.Fisheries Science, 66, 998–1000.

4. Yoshie-Stark, Y., Hsieh, Y.P. & Suzuki, T. (2003). Distribution of flavonoids and related compoundsfrom seaweeds in Japan. Journal of Tokyo University of Fisheries, 89, 1–6.

5. Ragan, M.A. & Glombitza, K.W. (1986). Phlorotannins, brown algal polyphenols. In: Progress inPhycological Research. Round, F.E. & Chapman, D.J. (eds), Biopress Ltd., Bristol, UK, pp. 129–241.

6. Targett, N.M. & Arnold, T.M. (1998). Minireview – predicting the effects of brown algal phlorotanninson marine herbivores in tropical and temperate oceans. Journal of Phycology, 34, 195–205.

7. Nakai, M., Kageyama, N., Nakahara, K. & Miki, W. (2006). Phlorotannins as radical scavengers fromthe extract of Sargassum ringgoldianum. Marine Biotechnology, 8, 409–414.

8. Wang, T., Jonsdottir, R. & Olafsdottir, G. (2009). Total phenolic compounds, radical scavenging andmetal chelation of extracts from Icelandic seaweed. Food Chemistry, 116, 240–248.

9. Shahidi, F. & Naczk, M. (2004). Antioxidant properties of food phenolics. In: Phenolics in Food andNutraceuticals. Shahidi, F. & Naczk, M. (eds), CRC Press, Boca Raton, FL, pp. 403–442.

10. Wanasundara, U.N. & Shahidi, F. (1998). Antioxidant and pro-oxidant activity of green tea extracts inmarine oils. Food Chemistry, 63, 335–342.

11. Shahidi, F. & Naczk, M. (1995). Antioxidant properties of food phenolics. In: Food Phenolics: Sources,Chemistry, Effects, and Applications. Shahidi, F. & Naczk, M. (eds), Technomic Publishing CompanyInc., Lancaster, PA, pp. 235–273.

12. Chew, Y.L., Lim, Y.Y., Omar, M. & Khoo, K.S. (2008). Antioxidant activity of three edible seaweedsfrom two areas in South East Asia. LWT – Food Science and Technology, 41, 1067–1072.

13. Senevirathne, M., Kim, S.H., Siriwardhana, N., Ha, J.H., Lee, K.W. & Jeon, Y.J. (2006). Antioxidantpotential of Ecklonia cava on reactive oxygen species scavenging, metal chelating, reducing power andlipid peroxidation inhibition. Food Science and Technology International, 12, 27–38.

14. Rice-Evans, C.A., Miller, N.J. & Paganga, G. (1996). Structure-antioxidant activity relationships offlavonoids and phenolic acids. Free Radical Biology and Medicine, 20, 933–956.

15. Yan, X.J., Li, X.C., Zhou, C.X. & Fan, X. (1996). Preservation of fish oil rancidity by phlorotanninsfrom Sargassum kjellmanianum. Journal of Applied Phycology, 8, 201–203.

16. Shibata, T., Ishimaru, K., Kawaguchi, S., Yoshikawa, H. & Hama, Y. (2008). Antioxidant activities ofphlorotannins isolated from Japanese Laminariaceae. Journal of Applied Phycology, 20, 705–711.

17. Jung, H.A., Hyun, S.K., Kim, H.R. & Choi, J.S. (2006). Angiotensin-converting enzyme I inhibitoryactivity of phlorotannins from Ecklonia stolonifera. Fisheries Science, 72, 1292–1299.



18. Ahn, M.J., Yoon, K.D., Kim, C.Y. et al. (2002). Inhibition of HIV-1 reverse transcriptase and HIV-1integrase and antiviral activity of Korean seaweed extracts. Journal of Applied Phycology, 14, 325–329.

19. Ahn, M.J., Yoon, K.D., Min, S.Y. et al. (2004). Inhibition of HIV-1 reverse transcriptase and protease byphlorotannins from the brown alga Ecklonia cava. Biological and Pharmaceutical Bulletin, 27, 544–547.

20. Berteau, O. & Mulloy, B. (2003). Sulfated fucans, fresh perspectives: structures, functions, and biologicalproperties of sulfated fucans and an overview of enzymes active toward this class of polysaccharide.Glycobiology, 13, 29R–40R.

21. Qi, H.M., Zhang, Q.B., Zhao, T.T. et al. (2005). Antioxidant activity of different sulphate contentderivatives of polysaccharide extracted from Ulva pertusa (Chlorophyta) in vitro. International Journalof Biological Macromolecules, 37, 195–199.

22. Tsiapali, E., Whaley, S., Kalbfleisch, J., Ensley, H.E., Browder, I.W. & Williams, D.L. (2001). Glucansexhibit weak antioxidant activity, but stimulate macrophage free radical activity. Free Radical Biologyand Medicine, 30, 393–402.

23. Zhao, X., Xue, C.H., Li, Z.J., Cai, Y.P., Liu, H.Y. & Qi, H.T. (2004). Antioxidant and hepatoprotectiveactivities of low molecular weight sulphated polysaccharide from Laminaria japonica. Journal ofApplied Phycology, 16, 111–115.

24. Zhao, X., Xue, C.H. & Li, B.F. (2008). Study of antioxidant activities of sulphated polysaccharides fromLaminaria japonica. Journal of Applied Phycology, 20, 431–436.

25. Colliec, S., Boisson-Vidal, C. & Jozefonvicz, J. (1994). A low molecular weight fucoidan fraction fromthe brown seaweed Pelvetia canaliculata. Phytochemistry, 35, 697–700.

26. Hayakawa, Y., Hayashi, T., Lee, J.B. et al. (2000). Inhibition of thrombin by sulphated polysaccharidesisolated from green algae. Biochimica et Biophysica Acta, 1543, 86–94.

27. Zhang, H.J., Mao, W.J., Fang, F. et al. (2008). Chemical characteristics and anticoagulant activities of asulphated polysaccharide and its fragments from Monostroma latissimum. Carbohydrate Polymers, 71,428–434.

28. Yan, J., Zong, H.L., Shen, A.G. et al. (2003). The �-(1→6)-branched �-(1→3) glucohexaose and itsanalogues containing an �-(1→3) linked bond have similar stimulatory effects on the mouse spleen aslentinan. International Immunopharmacology, 3, 1861–1871.

29. Yuan, H.M. & Song, J.M. (2005). Preparation, structural characterization and in vitro anti-tumor ac-tivity of kappa-carrageenan oligosaccharide fraction from Kappaphycus striatum. Journal of AppliedPhycology, 17, 7–13.

30. Smit, A.J. (2004). Medicinal and pharmaceutical uses of seaweed natural products: a review. Journal ofApplied Phycology, 16, 245–262.

31. Maeda, H., Tsukui T., Sashima, T., Hosokawa, M. & Miyashita, K. (2008). Seaweed carotenoid, fucox-anthin, as a multi-functional nutrient. Asia Pacific Journal of Clinical Nutrition, 17(Suppl 1), 196–199.

32. Miyashita K. & Hosokawa, M. (2009). Anti-obesity effect of allenic carotenoid, fucoxanthin. In: Nu-trigenomics and Proteomics in Health and Disease: Food Factors and Gene Interactions. Mine, Y.,Miyashita, K. & Shahidi, F. (eds), Wiley-Blackwell, Ames, IA, pp. 145–160.

33. Yan, X.J., Chuda, Y., Suzuki, M. & Nagata, T. (1999). Fucoxanthin as the major antioxidant in Hizikiafusiformis, a common edible seaweed. Bioscience, Biotechnology and Biochemistry, 63, 605–607.

34. Sachindra, N.M., Sato, E., Maeda, H. et al. (2007). Radical scavenging and singlet oxygen quench-ing activity of marine carotenoid fucoxanthin and its metabolites. Journal of Agricultural and FoodChemistry, 55, 8516–8522.

35. Nomura, T., Kikuchi, M., Kubodera, A. & Kawakami, Y. (1997). Proton-donative antioxidant activ-ity of fucoxanthin with 1,1-diphenyl-2-picrylhydrazyl (DPPH). Biochemistry and Molecular BiologyInternational, 42, 361–370.

36. Miyashita, K. (2007). Anti-obesity by marine lipids. In: Obesity: Epidemiology, Pathophysiology, andPrevention. Bagchi, D. & Preuss, H.G. (eds), CRC Press, Taylor & Francis Group, Boca Raton, FL,pp. 463–475.

37. Maeda, H., Hosokawa, M., Sashima, T., Funayama, K. & Miyashita, K. (2005). Fucoxanthin from edibleseaweed, Undaria pinnatifida, shows antiobesity effect through UCP1 expression in white adiposetissues. Biochemical and Biophysical Research Communications, 332, 392–397.

38. Miyashita, K. & Hosokawa, M. (2008). Beneficial health effects of seaweed carotenoid, fucoxanthin.In: Marine Nutraceuticals and Functional Foods. Barrow, C. & Shahidi, F. (eds), CRC Press – Taylor& Francis Group, Boca Raton, FL, pp. 297–319.

39. Maeda, H., Hosokawa, M., Sashima, T., Funayama, K. & Miyashita, K. (2007). Effect of medium-chaintriacylglycerols on anti-obesity effect of fucoxanthin. Journal of Oleo science, 56, 615–621.



40. Lee, S.H., Lee, Y.S., Jung, S.H., Kang, S.S. & Shin, K.H. (2003). Anti-oxidant activities of fucosterolfrom the marine algae Pelvetia siliquosa. Archives of Pharmacal Research, 26, 719–722.

41. Lee, Y.S., Shin, K.H., Kim, B.K. & Lee, S.H. (2004). Anti-diabetic activities of fucosterol from Pelvetiasiliquosa. Archives of Pharmacal Research, 27, 1120–1122.

42. Sato, M., Oba, T., Yamaguchi, T. et al. (2002). Antihypertensive effects of hydrolysates of wakame(Undaria pinnatifida) and their angiotensin I-converting enzyme inhibitory activity. Annals of Nutritionand Metabolism, 46, 259–267.

43. Suetsuna, K. (1998). Purification and identification of angiotensin I-converting enzyme inhibitors fromthe red alga Porphyra yezoensis. Journal of Marine Biotechnology, 6, 163–167.

44. Suetsuna, K. & Nakano, T. (2000). Identification of an antihypertensive peptide from peptic digest ofwakame (Undaria pinnatifida). The Journal of Nutritional Biochemistry, 11, 450–454.

45. Kim, J.A., Lee, J.M., Shin, D.B. & Lee, N.H. (2004). The antioxidant activity and tyrosinase inhibitoryactivity of phlorotannins in Ecklonia cava. Food Science and Biotechnology, 13, 476–480.

46. Sugiura, Y., Matsuda, K., Yamada, Y. et al (2007). Anti-allergic phlorotannins from the edible brownalga, Eisenia arborea. Food Science and Technology Research, 13, 54–60.

47. Dias, P.F., Siqueira, J.M., Maraschin, M., Ferreira, A.G., Gagliardi, A.R. & Ribeiro-do-Valle, R.M.(2008). A polysaccharide isolated from the brown seaweed Sargassum stenophyllum exerts antivascu-logenic effects evidenced by modified morphogenesis. Microvascular Research, 75, 34–44.

48. Zhou, G.F., Sun, Y.P., Xin, H., Zhang, Y.N., Li, Z.E. & Xu, Z.H. (2004). In vivo anti-tumor and im-munomodulation activities of different molecular weight lambda-carrageenans from Chondrus ocellatus.Pharmacological Research, 50, 47–53.

49. Yoon, N.Y., Chung, H.Y., Kim, H.R. & Choi, J.S. (2008). Acetyl- and butyrylcholinesterase inhibitoryactivities of sterols and phlorotannins from Ecklonia stolonifera. Fisheries Science, 74, 200–207.

50. Khan, M.N.A., Cho, J.Y., Lee, M.C. et al. (2007). Isolation of two anti-inflammatory and one pro-inflammatory polyunsaturated fatty acids from the brown seaweed Undaria pinnatifida. Journal ofAgricultural and Food Chemistry, 55, 6984–6988.

51. Sanchez-Machado, D.I., Lopez-Cervantes, J., Lopez-Hernandez, J. & Paseiro-Losada, P. (2004). Fattyacids, total lipid, protein and ash contents of processed edible seaweeds. Food Chemistry, 85, 439–444.

handbook of seafood quality, safety and health applications (alasalvar/handbook of seafood quality,...

Documents