Вы находитесь на странице: 1из 13

doi:10.

101 7/S0043 93391300 0366

__ _ _ _ _____ _
_ __ _ _ _ _ __ _ _ _ _ _ _ _ __
___ __ __
_ __ _ _ _____ _ ________ _ _ _ _ _ ____ __ _ __
__________

_ __ _ _ _ _ ___ _____

___

Biologically active peptides derived from


n___________ _____ _____ _______
egg proteins
____
______
E. ECKERT , A.___
ZAMBROWICZ
*, M. POKORA , A. POLANOWSKI ,
1

1
A SKI 2and
J. CHRZANOWSKA ,M.SZOLTYSIK ,A.D B R O W S KA , H. R
1
T. TRZISZKA
1

1
0___________
!"#$%_&!'#(")_*+,-*,_.!'"-/#_0_.'-,___1_
Dept. of Animal
Products Technology and Quality Management, Wroclaw
2
UniversityofEnvironmentalandLifeSciences,Wroclaw,Poland;
TheStateSchool
+
2
____3__
___1____0_$!+__1__1_1__________1_____44
of Higher Professional Education, Krosno, Poland
*Corresponding author: graszkiewicz@o2.pl

cations,
During food processing, proteins are subjected to different
modi of which
most
are the result of proteolytic enzyme
*+
(/(+!-
",/$ activity. Due to these mild and easily
cation has been commonly
controlled reaction conditions, this method of modi
_applied in producing high quality food
_4 products. Processingaffects the
conformation of the molecule and its biological activity. Limited hydrolysis leads
toimprovementofboththefunctionalandnutritionalpropertiesofproteins,aswell
organoleptic characteristics. Proteolytic enzymes release peptides that
_as their0____
__+-*#'$+-5_
c biological activities. Bioactive peptides govern
frequently show different speci
the function of other compounds in the bloodstream, digestive, immune and
__ &
__6of_ bioactive peptides exhibiting anti-hypertensive,
nervous/_systems.
Food_ sources
sh.
anti-tumour,
antioxidant
or
antimicrobial
activities include milk, eggs
and
' _ 7___ _ _8 _ __ _ _ _ _
Biopeptides with speci
c biological activities can be used in pharmaceutical,
cosmetic
food industries
as natural
___or
___
&'9#+*/(+!-
___
_*+(/(+!-
___ substances which prevent adverse changes,
ned
ts to the
as food additives or as functional food ingredients with
de bene
consumer.,,
The
following
paper
reviews
the
role
of
hens
eggs
as
a source of
_ &"!3 + #,
bioactive peptides, and how these can be used in functional foods.
/ _ $ __ ive pepti
__6 des; hydrol ysis; eggs; antioxidan t; imm unostim ulation
Keywords:bioact
_ __ _ ' __ 7___ _ _8 _
__ ,7 _ _
2:
___&'9#+*/(+!-___
___
_*+(/(+!-___

Introduction

,, _ &"!3
+ #, s are mix tures of pepti des of varying molecular weights and
Dietary prote in hydrol
ysate
free amino acids , which show a higher absorp tion rate compa red to native prote ins. They
arewi delyusedin themanuf actur of
ingdietarysupplement
andfoodfor
s
particula r
nutriti onal u ses (C lemente, 2000). Enzymat ic h ydrolysis of protein is mai nly carried out
under industri al condition s. Process es catal ysed by enzym es
c, are
andhighl
their y speci
progre ss can be fully controlle d. Protei n hydrolysat es wi th a certain degree of hydrol ysis

W orld's Poultry Science Associa tion 2013


/7________ 2__/_
__&
_
W orld's Poult ry Sc ience Journa l, V ol. 69, June 2013
"_____7________!__ ______1_
Received for publication August 6, 2012
Accepted for publication October 12, 2012
375

__6_

Bioactive peptides from food proteins: E. Eckert et al.


are a valuable source of p eptides that are characte rised by high biol ogical acti vity and
nutriti onal value (Cleme nte, 2000; Hartm an and Mies el, 2007).
Diethasa vitalrolein shapi ng
thehealt o
h fthebody Bioact
.
ive
peptides
aregood
examp les of substanc es that e xert diff erent health effects. The y are relea sed from food
prote ins by the action of prote olytic enzy mes (Hartman and Miesel, 2007). Distinguis hed
ed as compo unds
opioidpepti des
havebeenidenti
with immunos timula ting,
blood
press ure
loweri ng,plat elet
aggrega tion
inhi biting,
anti microbiaantioxidat
l,
ion
and
mineralabsorp tion-enhanc
proper
ing ties (Miand
ne Kova cs-Nolan , 2006;
Hartm an
and
Miese l, 2 007). The cspeci
activity of peptides is de termined by the type and location of
aminoacidresid ues
contai ned
in thei p
r rimarystructure(Parket
s
al., 2001).Proteins
from food mat erial are the precur sors of biopep tides. This prote in may be either of animal
or plantorigi nsuchas mil kproteins(casein,wheyprote in),
musc le
proteins(myosin,
inin,
collag en), soy prote in (glyc
-congl
ycini n) whea t (gluten) prote in or egg (ovalb umin,
conalb umin)
(T suge,
1991;Ibrahi m
et al., 1998;Pelle grini
et al., 2000;Saigaet al.,
2003; Gibbs
et al., 2004; ; Kimet al., 2007 ; Kong
et al., 20 07; Liet al., 2007).

Enzymatic hydrolysis of proteins


Hydro lysis of prote ins is a proces s of decom position into indi vidual ami no acids and/or
peptid es that occurs with the participa tion of enzy mes. The rate of hydrol ysis depends on
many factors such as enzymceity
speci
and c oncentrati on, subst rate concent ration, the
rateof masstransfer
in theenzym e/sub strate
syst em,
thedegreeof denatu ring
of the
prote in in the subst rate, pH, temperat ure, ionic strength in the react ion medium and the
akow(Ko
presen ce of activator s and inhi bitors
ski
et al., 2005). The hydrol ysis proces s
eds,
can proceed accordi ng to two mechanism
asone-byclass i one
orzipper
. During
theinitialstageof the react ion
typeone-by- one
(determining
theoveral levelof
l
hydrol ysis) it is necess ary to partiall y unfol d native protein mol ecules. As a result, the
prote in loses its stabili ty , more peptide bonds are exposed on the outside of the molecule
(interm ediate product s) an d the enzym e has ac cess to the hydrol yzed peptide bond. In a
furtherstep,intermed iate
products
areveryrapid ly
degradetdosmallpepti des.
If the
react ion equilibrium is on
the side
native
, then the prote in mol ecules are degrade d one
by one,so thereare no signicantquanti ties
of intermed iate
product s;
only nati ve
prote ins
andnal productarepresen
s
In
t. thezipper
typereact ion,
nati ve
prote in
is
veryrapidlyconverted
to intermed iate
products,
andhydrolysi os findi rect
formsof
nal product s occurs very slowly (Ku nst, 2003).
prote in in the
Proteo lysis
may occurby the on e-ortwo-stepsystem.In the caseof one-st ep
hydrol ysis,
the pH of the mix ture
is changed
automati cally as a result
of thereaction,
or is maintai nedaatconst ant
level by the
addit ion
of acidsor bases.
Thathydrol ysis
takes place in a continuous manne r . However, during the tw o-stage hydrolysi s, the pH of
thereact ion
varie sin subseq uent
stagesof prote olysis
throu gh
theuseof

Bioactive peptides from food proteins: E. Eckert et al.


sh protein
emulsif ying and foam ing properties of wheat glut
etal.
en
, 2008)
(Agyare
and
(Shahi di
et at., 1995).Rapeseed
prote in
hydrol ysates
havemuchbette emul
r
sifying
proper ties
an dwater-bi nding
capaci ty
thanthe startingsubst rate.
While the use of
sequent ially
alkalaseandexopept idase
allowsfor highl ysolub le
h ydrolysatewhi
s, ch
can be used as compo nents of speci alized high- protein liquids
et al., 1999).
(V ioque

Non-speci
c, far-reachi
ng hydrol ysis may lead to loss of funct ional properties and the
appearan ce of bitter peptides. The bitter tast e of prote in hydrolysat es can be reduced to an
accept able level by means
of
ltr ultr
ation,
a activated carbon proces sing and utilis ing the
plastein react ion (C lemente, 2000). It has been p roven that, by using certa in enzym es in
cantlymask ed (FitzGerald
the hy drolysis
proces s, the bitter
peptides
canbe signi
and
O'Cuin n,
2000).Thedevelo pment
of biot echnol ogical
solut ions
to obtai n hydroly sates
without a bitter aftertast e is alrea dy in progre ss.
Protein hydrolysat es are produce d on a large scale from various source s such as milk,
legumes, meat, and potatoes (Schaafs ma, 2009). Their valuab le proper ties
sh,eggs,
rice,
make them excellent ingre dients for incre asing the share of n itrogen in specialty d rinks,
manuf acturing specialist foods for pregnan t wom en, nutriti onal and cosmetic ingre dients
and in diet ary supplement s. The y can also be found in foods for pe ople with impaired
diges tion,
for athletes
and
in hypoal lerge product
nic
(Schaafsma,
s
2009).In addition,
hydrol ysates
areusefulas a growthmedi a
for a varie ty
of desir able
microorga nisms.
Several studies havermed
c on the positive imp act of the fraction of pepti des adde d to
mediain orderto improvethe grow thof microorga nisms
or in the production
of
recom binant prote ins (Duarte de Holanda and Netto, 20 06).
Thesedayshydrol ysate
deriv
s ed
from mari ne
product havebecom
s
p
earti cularly
popula r,
mainlydueto thefactthattheycontai a
n highamountof c omplete
ami no
acids (Crdova -Muretal.
ueta
, 2007). Over the years, techniques have been develo ped in
the use and recover y of va luable by-pro ducts in biopolym
et al.
ers
, 1996).
(Ferrer

Bioactive peptides - sources and application


The presen ce of biopep tide s in hydrolysat es ha s arouse d great interest amongst scientis ts
(Parket
, 2001;
al.
Korhonen and Pihla nto, 2003; Hartm an and Mies el, 2007). Bio active
peptid es are fragm ents of prote ins that are not active in the sequenc e o f the precursors.
After enzym atic release they inte ract with the corres pondin g receptors to regul ate the body
and its functions (Ko
a kowski
et al., 2005). The y cause vario us health effects, acti ng as
human horm ones o n the circu latory , digestiv e, nervous , and immune syst ems (Ha rtman
c acti vity of a pep tide is deter mined by the type
and Miesel, 2007)
Table
( 1
). The speci
and locat ion of amino acid residues contained in thei r primary
etal.
stru
, 2001).
cture (Park
Among the bioact ive pe ptides, simple and compl ex dipeptides , linear or cycli c oligo-and
polype ptides exist whic h may exhibi t various a ctivities (Mi ne and Kovacs Nol an, 2006;
Hartm an
andMies el,2007).Moreo ver,
somebioactivepeptides
exhibitchemotact ic
proper ties,
embr yotoxic
propertieshemolyti
,
p
c roper ties,
inhi bitoryacti vitycause
,
smoo th musc le contracti ons by stimulati ng the synthesis of red blood cell s a nd regulate
theactivityof thestomac mucosa
h
andthe ow of ions(Koakow skiet al., 2005).
T ypically , pepti des have mul tiple biological acti vities (Korhonen and Pihlanto, 2003).

Antioxidant activity
Oxidati ve react ions und erlie the advers e changes in food product s (ranci dity , odour and
colour change) and most p athologica l condition s (cardiovasc ular disea ses, d egenerative
W orld's Poultry Science Journa l, V ol. 69, June 2013
377

Bioactive peptides from food proteins: E. Eckert et al.


changes ) (Saiga
et, al.
2003). Current ly , great attentio n is paid to compo unds of natural
origin,e.g. in the potentialtherap eutic
role of antioxidan ts,
which are offse tb y
unfavou rable
ch anges
resul ting
from the actionof oxygenfree radic als.
Natural
source s opowerful
f
antioxidansuch
ts as protein
hydrol ysates
areconsi dered
usefulin
prevent ing disea se caused by oxidative stress, such a s colon cancer, Alzheim er's d isease
and Parkin son's d iseaseet
(Park
al., 2001).
Table 1 Examples of bioactive peptides derived from food.
Effect

Source of
peptides

Encrypting
protein(s)

Antioxidant

egg

lecithin-free egg
yolk
Ovalbumin
-lactalbumin
-lactoglobu lin
germ protein
ovotransferin
ovalbumin

egg
milk
wheat
ACE inhibitory/ egg
Hypotensive
milk
sh

Antitumour

egg
sh

Antimicrobial

egg

Metal binding

egg
milk

Immunomodulatory

milk
egg

Antithrombotic milk
pork

Name/remarks/sequence
(in single-letter code)
Reference

LMSYMWSTSM
Parket al.(2001)
LELHKLRSSHWFSRR
AHK, VHH, VHHANEN
T suge
et al.(1991)
MHIRL, YVEEL,
Hernandez-Le desma
WYSLAMAA SDI
et al.(2005)
ed
peptides not speci
Zhuet al.(2006)
KVREGTTY
Leeet al.(2006)
ovokinin (FRADHPPL)
Miguel and
ovokinin (f 7)
2
Aleixandre (2006)
(KVREGTTY)
-lactalbumin
lactokinins
Mizushimaet al.
-lactoglobu lin, (e.g.WLAHK, LRP , LKP) (2004)
, , -casein
casokinins
miobryllar
(e.g.FFV AP , F ALPQY , Hartman and Miesel
protein
VPP)
(2007)
bryllar
hydrolysates
oligopeptide LKPNio
protein hydrolysates
Phosvitin
phosphooligopeptides Picotet al.(2006)
ed
miobrillar
peptides not speci
Mine and Kovacsprotein
Nolan (2006)
hydrolysates
Pellegriniet al.
(2004)
ovotransferrin
OT AP-92 (f 109
200)
Choiet al., 2005
ed
lysozyme
peptides not speci
ovalbumin
penta-, hexa- and
oktapeptides
Phosvitin
phosphooligopeptides Crosset al.(2007)
Miquel and Farre
(2007)
-, - casein
caseinophosphopeptidesGauthier
et al.
(2006)
-, -, - casein, immunopeptide.g.aS1es (
Mine and Kovacs-lactalbumin
immunocasokinin)
Nolan (2006)
(TTMPL W)
ed
Ovalbumin
peptides not speci
Iwaniak and
Minkiewicz (2007)
Qianet al.(1995)
-casein
caseinoglycopeptide
Chavakiset al.
(CGP) (f 106-171)
(2002)
miobryllar
FK633, His-Gly-L ys
protein
hydrolysates

The anti oxidant


activityof prote in
hydrol ysates
depends
largelyon thedegreeof
hydrol ysis
(% DH) andthetypeof prote ases
usedfor enzym atic
degrada tion
(Ko ng
andXiong,2006).The crucialfactoris theweight,typeandpositionof aminoacid
378

W orld's Poult ry Sc ience Journa l, V ol. 69, June 2013

Bioactive peptides from food proteins: E. Eckert et al.


residu es contained
in thestructure
of the peptide s (Park
et al., 2001). Marcu se (1962)
demon strated that antioxidan t proper ties are deter mined by the presen ce in hydrol ysates
of severalaminoacids s, uchas tryptophan,
methioni ne,
histidine,lysi ne,glyci ne.
Kawash ima
et al.(1979)foundthatthearomatic
aminoacids,presen t in some
di-an d
tri-pept ides, exhibit strong free radic al scaveng ing properties . This is due to the abil ity of
theseami no
acids(tyro sine,
tryptophan
andhistidi ne)
to readilycleavehy drogen
- an
electron donor to free radicals seeki ng to adopt a stabl e form through their pairing (Park
et al., 2001;Dava ls
et al., 2004).The mecha nism
o fanti oxidative
hydroly sates
and
peptid es
maybe manifest ed
as thescaveng ing
of freeradicals,chelation
of trans ition
c o xidants
metals,reduct ion
of hydrope roxideenzymatic
s,
elimin ation
of speci
or
inhibit ion of lipid peroxi dation in food syst ems
et al.
(Elia
, 2008).
s
Many antioxidanpteptides
havebeenprepar ed
from whea (L
t iyana-P athirana
and
Shahidi , 2007), mai ze (Kong and Xiong, 2006), pig blood haemo globi
et al.,n (Chang
2007), or eggs. For example, two pepti des with aromatic resi dues, which wer e o b tained
from egg yolk proteins under the
uence
in of Alcalase have the potential to inhib it the
oxidat ion of lino leic acidetal.
(P ark
, 200 1). Ovalbum in is the source of three antio xidant
peptid es contai ning sequenc es in the second position the rest of the histidine
et
(T suge
al., 1991).A charact eristic
featu re
of thesepeptides
is thepresen ce
of theresto fthe
leucin e at position N-term inal, condition ing their bioactivi
etal., 2001).
ty (Park
A sim ilar
effect has anti oxidant p reparation obtai ned by the action of bacterial prote olytic enzym es
(Bacil lus
sp) on theyolk protein,co nsisting
of a fract ion
of pepti des
wi thmolecular
weights not exceedi ng 1 kDa (Sakanaka
et al., 2004).
Furthe r peptides with antioxidan t activity are product s resultin g from the hydroly sis of
ovalbu min wi th pepsin, which have the abil ity to scaveng e free radic als AAPH (Davals
, et
2004).
al. Many valuab le anti oxidant peptides wer e also obtained from ph osvitin - a
highly phospho rylat glycoprotei
ed
n,
represents
the maj orfract ionof egg yolk
phospho protePeptides
ins.
deriv ed
fromphosvi tin
arecha racterise
byda highcon tent
of phospho rus
andaminoacidssuchas histidi ne,
methioni ne
andtyrosine(Xu et al.,
2007).It's alsobeenshow nthatph osvitin
products,
by inhibit ing
iron-dependeion
nt
formati on
reactionof the mostreactivehydroxy free
l
radic als,
are linke dto DNA
prote ctive proper ties (Matoba
et al., 1999).
Studi es
in recentyearsconrm thatsomeproteinhydrol ysates
andpeptides
exhibit
-toco
better anti oxidan t acti vity
thanpherol and may even exceed the activity of potent
synth etic
antioxidan (BHA,
ts
BHT) usedin the food industry(Je et al., 2007).In
addition,manyanti oxidan
pepti
t
des
havea mul tifunctional
charact er,
showingother
proper ties
suchas an tihyperte nsive,
opioi d,an ti-thrombot
andhypoch
ic
olesterolemi c
which makes these compo unds more useful as dietary ingredient s in prom oting human
health (Da vals
et al., 2004).

Anti-hypertensive activity
Amongthe mostincre asing
lifestylediseases,
includingthosestem ming
from an
unheal thy
lifestyle,cardi ovasculdisea
ar se
and hypert ension
are
o f key imp ortan ce.
Pepti des can be consi dered natur al antihypert ensive pharm acological compo unds. The y
inhibit the activityof angiot ensinogen
I-conv erting
enzym e(ACE ), a peptidyldipept idase
that can cleave a dipept ide
from the angiotensi In (decapep tide:
DR VY IHPFHL)C-termina whichcauses
l,
its convers ion
to angiotensiII,n a blood
press urebooster I.nact ivation
of the enzym eby inhi bitorsmeansbradyki nin
stimul ation
also, whi chlowers blood press ure(Miguel et al., 2006
). These

W orld's Poultry Science Journa l, V ol. 69, June 2013


379

Bioactive peptides from food proteins: E. Eckert et al.


antihy pertensive
precur sors of peptides
are prominent ly found in egg album in (Miguel
and Aleixan dre, 2006; Har tman and Miesel, 2007).
Great interestin biological lyactivepeptidesh asbeen generat ed
from wor k
inves tigating
ovalbu min
presenint eggwhite.Whenthewholeegg
i.e.theprote ins
uence
is eaten, ovalbu min is transform ed into octape ptide
underofthe
pepsi
in n called
ovokin in, representi ng fragm ent (f 358-365 ) o f ovalbu
etal., min
1995;
(Fujita
Davis and
Reeve s,
2002).In addition,underthe inuenceof chymo trypsovokin
in,
in(2-7)is
relea sed
(Matoba,1999).The sepeptides
act by loweri ng
systolicbloodpress ure
in
rats,in a dose-d ependent
manne(Fujitaet
r
al., 1995).In thediges tive
syst em,
these
cation
peptid es undergo immediate
emulsiand are well ab sorbed by the intestine (Davis
and Reeves, 2002).

Anti-tumour activity

Evidence of the
tsbene
of consuming bioact ive pepti des has been recognized in the case
of neo plastic
changes
(Erdma nn
et al., 2008).Epidem iolo gical
studiesshowthatthe
incide nce
of tum ours
in differentpartsof the humandiges tive
systemis stro ngly
condit ioned
by thediet(Roseet al., 2007).Studi es
showthattherisk of color ectal
uence
cancer may be reduced under
the inof hydrol ysate s from egg yolk protein (Azuma
et al., 2000;Belob rajdic
et al., 2003),wher eby
inges tion
inhi bits
theprolifera tion
of
tumou r cell s in the colon of ratsc. Sp
prote
ecictive effect s agains t the prolifera tion of
cancer cell s have been attr ibuted to phosvi tin, as this prote in and its peptides, have strong
antiox idant properties
in vitro(Ishikaw etal.,
a
2004) and in human inte stinal epit helium
(Katayamet
,a200
al. 6). In addition, they regul ate the level of the e nzymes respon sible
for biosy nthes is of glutathio ne (GSH), which plays a key role in the mecha nism of cell
death (Richman and Meister, 1975). Studi es have show n that oligopept ides relea sed from
phosvi tin
ha vethe abil ityto incre ase
intr acellular
GSH activityand regul ate
the
expres sion
of -glutamy cysteine
in intesti nal
epithe lial
cell s,which catal yses
the
synth esis
of GSH (Ka tayama
et al., 2006;2007).Phospho- oligopept obtai
ides ned
from phosvi tin also have the abil ity to regulate the levels of antioxidan t enzy mes such
as catalase and glut athione reduct ase. For this reason they can be consi dered as anticancer
agents in the c olon.
The precursors of anti -cancer peptides are presen t in the egg ovomu cin. The a ction of
pronas enzy
e
mes
fromStreptomyces griseus
on bothfactions and of theproteins,
), 120 (fof)220
)
relea sed highl y glycosylat ed o ligopeptides with masses
and(f70 (f
kDa. Direct treatmen t of the mice tumours with these oligopept ides effectivel y inhi bited
tumou r grow th (W atanabe
et al., 1998).

Antimicrobial activity
Pepti des
deriv ed
from food proteinhydrolysat es
can exhibi tantimi crobial
ac tivity ,
especi ally
thosecontaining
tryptophan
andargin ine.
The presen ce
of argin ine
in the
peptid e
sequenc allows
e
the moleculeto give a positivecharge,which form sa
hydroge bondwiththeanionic
n
compo nents
of thecell membrane,
impacti ng
on the
peptid e - cy toplasm ic mem brane (Powers and Hanc ock, 2003). However, the presen ce of
tryptophan
prom otes
thefoldi ngof peptides
in aqueoussolution bs ecause
it hasan
afnityto thecell mem brane.
This provi des
thestructure
of theamphiphi lic
peptides
necess ary for their trans port across the cytoplasm ic membrane
et al., 2006).
(Chan
Thereareseveramecha
l
nism
of sactionof peptides
againsmicrobia
t
cells.Oneof
l
380

W orld's Poult ry Sc ience Journa l, V ol. 69, June 2013

Bioactive peptides from food proteins: E. Eckert et al.


them, whi ch is used particula rly in relation to gram -negat ive bacter ia, is due to the abil ity
of pepti des
to bindto thecell lipopolys acchariwal
del.As a resul of
t aggrega tion
of
peptid es
in thecytopl asmic
membrane,
channelareform
s
ed
thatcausedesta bilisation,
leadin g to cell death. An examp le of a peptide show ing this acti vity is lact oferricin B.
Pepti de
precur sors
with antimi crobial
proper ties
includeo valbumin
themajo
,
regg
prote in.
Bovinetrypsinis usedto relea se
of thisprote in
as well as penta-hexa-an
,
d
oktape ptides
which exhibi tstrongbacterici dal
activ ityagains Bacillus
t
subtilis
. In
contr ast,
peptidesformed by the action of bovine chymo trypsin
demon strate
bacter icidal
activity againstGra m-posit ive
bacter ia,such as Bacillus subtilis
,
Micrococcus luteus
, Staphylococcus aureus
, Streptococcus epidermidis
, Streptococcus
zooepidermicus
and theGra m-ne gative
bacter Bordetella
ia
bronchiseptica
, Escherichia
coli, Klebsiella pneumoniale
, Pseudomonas aeruginosa
andSerratia marcesens
, as well
as fungi, such as
Candida albicans
(Pellegri ni
et al., 2004). The antimi crobia l acti vity
shows that the 9.9 kDa fragm ent (f 109 -200) of conalb umi n (OT AP 92) is active against
G+ and G- bacteria. The OT AP pepti de 92 obtain ed from the N-te rminal fragm ent of the
polype ptide chain and has a cati onic c haracter . The same featu res have been observ ed in
peptid es
relea sed
by pepsin,of lact oferrin
in humanmilk andcow'smilk,or peptides
formed during hydrol ysis of basic pancreat ic tryps in inhibit or by clostripain,
et (Ibra him
al., 2000).Moreo ver,
theOT AP-9 2
p eptide
showsanti-vir ulence
proper ties
whi
, chis
effective in the inactivat ion of Marek 's disease virus in chicke ns.
L ysozyme
is anotheprecur
r
sor
of a ntimicrobia
peptides.
l
Partialhydrol ysis
of this
prote in
usingpepsingivesrise to a mix ture
of peptidesexhibi ting
activityagainst
bacter ia
of thegenusBacillus
. Thesepeptides
retai nacti vity
evenafter30 minutes
heatin g
at 95C in a pH rangefrom 4.5 to 7, makingthemusefula natur al
preser vatives in proces sed food et
(Abdou
al., 2007).

Metal binding peptides


Of great imp ortance, especiall y i n the food and pharm aceutical indus tries, are the metal
ion bindingpeptides.
The ycanserveas carri ers
of micronut rients,
facilit ating
thei r
c transport
absorp tion,
d ueto thespeci
systemsfor shortpeptides
in thediges tive
system(C lemente,
2000).Pe ptides
withchelat ing
abilitymaytherefore
be usefulfor
incre asing
the bioava ilability
of min erals
a n dto prevent ing
the oxidationof food
product whi
s, lstretainingthevisualcharacter
andquali tyof food.Phosphop epti des,
deriv ed
from milk prote ins,
havech elating
proper ties
for metalssuchas calcium
(Crosset al., 2007),zinc(Miqu el and
Farre,2007)andiron(Bouhal lab
et al., 2002).
Similareffectsareseenwi thpep tides
deriv ed
fromeggyolk phosvi tin,
whi chmay
incre ase
thebioava ilability
of calcium(Choi et al., 2005
). Phosvi tin
contai ns
more
serine resi dues than casei n. In addition, the high phospho rus content gives this protein
ogical proper ties. It has been proven that the pepti des from phosvi tin
some speci
c biol
incre ase calci um absorp tion in rats
et al.
(Choi
, 2005). Other studies indi cate that when
these pepti des are obtained by hydrol ysis with tryps in, it incre ases the bindi ng of calcium
in the bones and prevens the formati on of insolubl e calcium phospha te (Jia ng and Mine ,
2001). As a resul t, phospho pepti des, deriv ed from phosvi tin, contai n a large amoun t of
phospho seri ne and can be widely used as nutri tional supplement s and pharm acolog ical
prepar ations for people suffe ring from osteo porosis. Che lating pepti des, by prote cting the
bodyagainsfreeradic
t
als,
mayalsoimp rove
theperfor mance
of physic al
andmental
activity and delay the aging proces s in human s (Hartman and Mies el, 2007).

W orld's Poultry Science Journa l, V ol. 69, June 2013


381

Bioactive peptides from food proteins: E. Eckert et al.

Immunostimulating activity
Theimmunesystemhasa decis ive
inuenceon theequil ibrium
stateof healt h in
the
body which determin es its ho meostasis. One possi ble stra tegy to increase natural immune
prote ction is the use of a balanc ed diet rich in p robiotics and funct ional foods
et (Na kano
, 2001).
al. In recent years the role of reduci ng the risk of chroni c diseases and enhaci ng
immune prote ction has been attribut ed to bioact ive p eptides deriv ed from food proteins
(Ma et al., 2006).
The mechanism of action of biopep tides may rely on direc t inte raction with pathog ens
as well as suppre ssion or sti mulatio n o f certain immune respon ses (Ha ncock and Sahl,
2006).Studiesshowthatbothimm unosupp ression
and immu nostimu lation
maybe
importanint prevent ing
andghtin g
variouspathologica
condition
l
os fthebody and
,
ammati
peptid es have an immunom odulat ing effect that can be used
to reduce
on inin
autoimm une diseases, prevent transplant rejec tion and improve overall health
et (Gauthi er
al., 2006).The reare numero us
examplesin the literat ure
of such inte ractions
ius et al., 2006), howe ver most are deriv ed from milk.
(Bizi ulevi
Prevent ion of diseases associ ated with the current way of life, such as ather oscle rosis,
myoca rdial
infarcti on
or strokeis veryimp ortant
andnecess ary
in manydevelo ped
countr ies.
The useof anti-pept ide
seemsto be a prom ising
strategy
for reducingthe
risk of thrombot ic disea se in health y people and assi st or even repla ce the currently used
thera peutic agents .

Conclusions
There is a growing inte rest in the food, pharm aceutical and cosmetic indus tries in the use
of biopep tide
prepar ations.
Researche rs
are looking for unc onventional
high,
c
perfor mance
enzym es,
andmet hods
andtechno logies
areb eingdevelo ped
for speci
hydrol ytic proces sing. An examp le of this focus are the studies carried out in the project
OVO CURA withi ntheconsor tium
of theUni versity
of Life SciencesandMedical
Acad emy in Wroclaw .
Unde rstanding
the relat ionship
betweenphysi cochem ical
proper ties
of protein
hydrol ysates
and theirfunct ionalitcan
y lead to imp roved
qualityand stabi lity
of
nutriti onal
formulat ions
basedon the product of
s hydrol ysis
(Panyamand Kilara,
ned and repeat able
1996).Many potentialhydrol ysate
requi
s rewel l-de
en zymatic
degrada tion
proces ses.
Because
minordiff erences
in thehydrol ysis
leadto changes
in
biolog ical acti vity , the need for careful contr ol of the proces s is param ount. Moreo ver,
edphysiologi cal properties
mostof theidenti
of bioact ive peptihave
des been
studied
only in vitro or in animalmodel s.
Clinicaltri alson human arelimitedor
s
arenot
perfor med
at all, bec ause
it is difcultto determinthelevelof
e
bioact ive
peptides
in
serum It. shouldalso be notedthat,despi te
the greatvarie ty
o fbioact ive
pepti des
generat ed by the proces s of digestion in the human body , only the di- and tri-peptides
are absorb ed by the intestinal epit helial cells and transport ed by erythrocyt es (Jones and
Tung, 19 83).
ciency
One o f the probl ems concern ing
the efof biopep tides is thei r oral appli cation.
T o get into the bloods tream, they must ove rcome the body' s natur al barriers, such as a
highly acidi cstomachenvir onment,
pepsi nand pancreatic
enzym es
an dinte stinal
absorp tion.
The refore,
it is necess ary
to conductfurtherresear ch
to ident ifythe
potent ial
therapeu role
tic of bioactivepepti des,
deriv ed
fromvario us
source s,
on the
human body .

382

W orld's Poult ry Sc ience Journa l, V ol. 69, June 2013

Bioactive peptides from food proteins: E. Eckert et al.

Acknowledgements
Projec tInnova tive
techno logies
of product ion
of biopr eparations
basedon new
generat ion
eggs
EconomyOper ational
Prog ramme
Prior ity1.3.1,them atic
Innovat ive
areaBio Co-nan ced
by European
Uni onthroughEuropean
Reg ional
Deve lopment
Fund withi n the Innovat ive Eco nomy Oper ational Program me, 2007-20 13.

References
(2007)
ABDOU, A.M., HIGASHIGUCHI, S., ABOUELEININ, A.M., KIM, M. and IBRAHIM, H.R.
Antimicrobial
peptides
derivedfrom henegglysozym with
e
inhibitoryeffectagainstBacillusspecies.
Food Control18: 173-178 .
uence of salt and pH on the solubility and structural
(2008) In
AGYARE,K.K.,XIONG,Y.L.andADDO,K.
characterist ics of transglutaminase-treate d wheat gluten
Food
hydrolysate.
Chemistry
: 1131
1137
.
107(3)
(2000)
AZUMA, N., SUDA, H., IWASAKI, H., YAMAGATA, N., SAEKI, T. and KANAMOTO, R.
Antitumourigenic
effectsof severalfood proteinsin a rat modelwith coloncancerandtheirreverse
correlation with plasma bile acid concentration
Journal of
. Nutritional Science & Vitaminology
46: 91-6.
BELOBRAJDIC, D.P., MCINTOSH, G.H. and OWENS, J.A. (2003) Whey proteins protect more than red
meat against azoxymethane induced ACF in wistar
Cancer
rats.
Letters
198: 43-51.
UKAIT, V. (2006)FoodBIZIULEVI IUS, G.A., KISLUKHINA, O.V., KAZLAUSKAIT, J. and
protein enzymatic
hydrolysates
possess
both antimicrobial
andimmunostimulatory
activities:
a cause and
effect
lity . Immunology and Medical Microbiology
: 131-138.
theory of bifunctionaFEMS
46(1)
BOUHALLAB, S., CINGA, V., AIT-OUKHATAR, N., BUREAU, F., NEUVILLE, D. and ARHAN, P.
uence of various phosphop eptides of caseins on iron
(2002) In
JournalofAgriculturalandFood
absorption.
Chemistry
7130.
50: 7127
CRDOVA-MURUETA,J.H., NAVARRETE-DEL-TORO, M.A. and GARCIA-CARRENO, F.L. (2007)
Concentrate ssh
of protein from by catch species produced by various drying
Food
processes.
Chemistry
100:05711.
(2006)Tr yptophanand arginine-rich antimicrobial
CHAN, D.I., PRENNER, E.J. and VOGEL, H.J.
peptides:
Structures
andmechanisms
o faction.Biochimica et Biophysica Acta (BBA) - Biomembranes
: 1 184-1202.
1758
properties
andproteincompositions
of
CHANG, C.Y., WU, K.C. and CHIANG, S.H. (2007)Antioxidant
porcine hemoglo bin hydrolysates.
Food Chemistry
1543.
100: 1537
CHAVAKIS, T., BOECKEL, N., SANTOSO, S., VOSS, R., ISORIDA-SALAS, I. and PIXLEY, R.A.
(2002)Inhibitionof plateletadhesion
andaggregatiobnya denedregion(Gly-486-L ys
502)of high
molecular weight kininogen.
Journal of Biological Chemistry
277:5764.
(2005)Effectiveness
of phosvitinpeptides
on
CHOI, I., JUNG, C., CHOI, H., KIM, C. and HA, H.
enhancing bioavailabil ity of calcium and its accumulation
Food
in bones.
Chemistry
93: 577-583.
CLEMENTE, A. (2000)Enzymaticproteinhydrolysateins humannutrition.Trends in Food Science &
Technology
11(7): 254-262 .
CROSS, K.J., HUQ, N.L. and REYNOLDS, E.C. (2007) Casein phosphopeptides in oral health-chemis try
and clinical applications.
Current Pharmaceutical Design
13: 793800.
DAVALS, A., MIGIEL, M., BARTOLOME, B. and LPEZ FANDI O, R. (2004) Antioxidant activity
of peptides derived from egg white proteins by enzymaticJournal
hydrolysis.
of Food Products
67: 19391944.
DAVIS, C. and REEVES, R. (2002) High value opportunities from the chicken egg. A report for the Rural
Industries Research and Development Corporation 02/094.
(2006)Recoveryof components
from shrimp
DUARTE DE HOLANDA, H. and NETTO, F.M.
(Xiphopenaeuskroyeri
) processing waste by enzymatic hydrolys
JournalofFoodScience
is.
: 298303.
71(5)
ELIAS, R.J., KELLERBY, S.S. and DECKER, E.A. (2008) Antioxidant activity of proteins and peptides.
Critical Reviews in Food Science and Nutrition
48: 430441.
(2008) The possible roles of food-derived peptides
ERDMAN,K.,CHEUNG,B.W.Y.andSCHRDER,H.
in reducing in the risk of cardiovascular disease.
Journal of Nutritional Biochemistry
19: 643-654.
(1996) Acid
FERRER, J.,PAEZ, G.,MARMOL,Z., RAMONES, E., GARCIA,H.andFORSTER, C.F.
hydrolysis of shrimp-shell wastes and the production of single cell protein from
Bioresource
the hydrolysate .
Technology
57:5560.
(2000)Enzymaticdebittering
of food proteinhydrolysates.
FITZGERALD, R.J. and O'CUINN, G.
Biotechnology Advances
: 234-237.
24(2)

W orld's Poultry Science Journa l, V ol. 69, June 2013


383

Bioactive peptides from food proteins: E. Eckert et al.


of theantihypertensive
activityof
FUJITA, H., SASAKI, R. and YOSHIKAWA, M. (1995)Potentiation
cationin egg
orallyadministered
ovokinin,a vasorelaxing
peptidederivedfromovalbum in,
by emulsi
phosphatidylc holine.
Bioscience Biotechnology & Biochemistry
: 2344-2345.
59(12)
GAUTHIER, S.F., POULIOT, Y. and SAINT-SAUVEUR, D. (2006) Immuno modulatory peptides obtained
by the enzymatic hydrolysis of whey proteins.
International Dairy Journal
: 1315-13 23.
16(11)
GIBBS, B.F., ZOUGMAN, A.,MASSE, R.and MULLIGAN, C. (2004) Production and characterizatio n of
bioactive peptides from soy hydrolys ate
and soy food.
FoodResearchInternational
fermented
37: 123131.
HANCOCK, R.E.W. and SAHL, H.G. (2006) Antimicrobia l and hostdefens e peptides as new anti-infective
therapeutic strategies.
Nature Biotechnology
: 1551-15 57.
24(12)
HARTMAN,R.andMIESEL,H. (2007) Food-derived peptides with biological activity: from research to food
applications
Current
.
Opinion in Biotechnology
18: 163-169.
(2005) Preparation of
HERNANDEZ-LEDESMA,B.,DAVALOS,A.,BARTOLOME, B.andAMIGO,L.
cationof active
antioxidant
enzymatic
hydrolys ates
fromalpha-lactalb umin
andbeta-lactoglob ulin.
Identi
peptides by HPLC-MS/MJournal
S.
of Agricultural and Food Chemistry
53: 588-593.
cationof a distinct
(1998)Identi
IBRAHIM, H.R., IWAMORI, E., SUGIMOTO, Y. and AOKI, T.
antibacterial
domainwithin the N-lobe of ovotransfe rrin.
Biochimica et Biophysica Acta (BBA)

Biomembranes
: 289-303.
1401(3)
antimicrobial
peptide
(OT AP-92)
IBRAHIM, H.R., SUGIMOTO, Y. and AOKI, T. (2000)Ovotransferrin
kills bacteria through a membrane damage mechanism.
Biochimica et Biophysica Acta
: 196-205.
1523
ISHIKAWA, S., ASANO, T., TAKENOSHITA, S., NOZAWA, Y., ARIHARA, K. and ITOH, M. (2009)
Egg yolk proteins suppress azoxymethane-induced aberrant crypt foci formation and cell proliferation in the
colon of rats.
Nutrition Research
29:6469.
(2004)Egg yolk phosvitininhibitshydroxyl
ISHIKAWA, S., YANO, Y., ARIHARA, K. and ITOH, M.
radical formation from Fenton reaction.
Bioscience Biotechnology & Biochemistry
68: 1324-31.
(2007) Proteins as the source of physiologi cally and functionally active
IWANIAK,A.andMINKIEWICZ,P.
peptides.
ACTA Scientiarum Polonorum - Technologia Alimentaria
6(3): 5-15.
cation and characterizatio n of a n antioxidant
(2007) Puri
JE,J.Y.,QIAN,Z.J.,BYUN,H.G.andKIM,S.K.
peptide obtained from tuna backbone protein by enzymatic
Process
hydrolysis.
Biochemistry
42: 840846.
JIANG, B. and MINE, Y. (2001) Phosphopeptides derived from hen egg yolk phosvitin: effect of molecular
size on the calciumbinding properties.
Bioscience Biotechnology & Biochemistry
1190
.
65: 1187
(1983)Functionalproperties
of proteinof modied oil seedprotein
JONES, L.J. and TUNG, M.A.
concentrates and isolates.
Canadian Institute of Food Science and Technology16
Journal
:5762.
(2007) Oligophosphopeptides derived from egg
KATAYAMA,S.,ISHIKAWA,S.,FAN,M.Z.andMINE,Y.
yolk phosvitinup-regulate
gamma-glutamylcystein
synthetase
e
andantioxidant
enzymes
againstoxidative
stress in Caco-2 cells.
Journal of Agricultural and Food Chemistry
55: 28,29-35.
KATAYAMA, S., XU, X., FAN, M.Z. and MINE, Y. (2006) Antioxidativestressactivityof
oligophosphopeptides
derivedfromheneggyolk phosvitinin Caco-2cells.Journal of Agricultural and
Food Chemistry
54: 773-8.
(1979) Antioxidant properties of branchedKAWASHIMA,K.,ITOH,H.,MIYOSHI,M.andCHIBATA,I.
chain amino acid derivatives.
Chemical & Pharmaceutical Bulletin (Tokyo)
1916.
27: 1912
(2007) Separation of iron-binding
KIM,S.B.,SEO,I.S.,KHAN,M.A.,KI,K.S.,NAM,M.S.andKIM,H.S.
protein from whey trough enzymatic hydrolysis.
International Dairy Journal
17: 625-631.
adnikw
kacja sk
KO AKOWSKI, E., BEDNARSKI, W. and BIELECKI, S. (2005) Enzymatyczna mody
ywnoci. Wydaw. A. R. Szczecin
: 373-382 (in polish).
KONG,B.H.andXIONG,Y.L. (2006) Antioxidant activity of zein hydrolys ates in a liposome system and the
possible mode of action.
Journal of Agricultural and Food Chemistry
6068.
54: 6059
and
KONG, X., ZHOU, H. and QIAN, H. (2007)Enzymatichydrolysisof wheatglutenby proteases
properties of the resulting hydrolys
Food
ates.
Chemistry
102: 759-763.
opportunities for designing
KORHONEN, H. and PIHLANTO, A. (2003) Food-derived bioactive peptides
future foods.
Current Pharmaceutical Design
308.
9: 1297
cation to optimize functionality protein hydrolysates, in: WHIT AKER, J.R.,
KUNST, T. (2003) Protein modi
VORAGEN, A.G.J. & WONG, D.W .S. (Eds)
Handbook of Enzymology
, pp. 221-231 (New Y ork, Basel).
(2006)One peptidederivedfrom hen
LEE, N.Y., CHENG, J.T., ENOMOTO, T. and NAKANO, Y.
ovotransferras
inpro-drugto inhibitangiotensin
converting
enzyme.
Journal of Food and Drug Analysis
14: 31-35.
cation of antioxidative peptides
(2007) Isolation and identi
LI,B.,CHEN,F.,WANG,X.,JIB.andWU,Y.
from porcinecollagenhydrolys ate
by consecutive
chromatog raphy
and electrospray
ionization-m ass
spectrometry
Food
. Chemistry
.
1143
102: 1135
(2007) Antioxidant and free radical scavenging activities of
LIYANA-PATHIRANA,C.M.andSHAHIDI,F.
whole wheat and milling fractions.
Food Chemistry
.
1157
101: 1151

384

W orld's Poult ry Sc ience Journa l, V ol. 69, June 2013

Bioactive peptides from food proteins: E. Eckert et al.


cation and identi
cation of angiotensin IMA, M.-S., BAE, I.Y., LEE, H.G. and YANG, C.B. (2006) Puri
converting enzyme inhibitory peptide from buckwheat (Fagopyrum esculentum
FoodChemistry
Moench).
96
(1):3642.
MARCUSE, R.(1962) The effect of some amino acids on the oxidation of linoleic acid and its methyl ester .
Journal of the American Oil Chemists Society
39:97103.
peptide
MATOBA, N., USUI, H., FUJITA, H. and YOSHIKAWA, M. (1999)A novelanti-hyperten sive
derived from ovalbum in induces nitric oxide-mediated vasorelaxation in a isolated SHR mesenteric artery .
FEBS Letter452: 181-184 .
Journalof
proteins.
MIGUEL,M.andALEIXANDRE,A. (2006) Antihypertensive peptides derived from egg
Nutrition136: 1457-14 60.
(2006) New insights in biologically active proteins and peptides derived
MINE,Y.andKOVACS-NOLAN,J.
from hen egg.
World's Poultry Science Journal
: 87-95.
62(1)
(2007)Effectsand futuretrendsof caseinphosphopep tides
on zinc
MIQUEL, E. and FARRE, R.
bioavailabil ity
Trends
.
in Food Science & Technology
18: 139143.
MIZUSHIMA, S., OHSHIGE, K., WATANABE, J., KIMURA, M., KADOWAKI, T., NAKAMURA, Y.,
TOCHIKUBO, O.andUESHIMA, H. (2004) Randomiz ed controlled trial of sour milk on blood pressure
in borderline hypertensive American
men.
Journal of Hypertension
17: 701-706.
NAKANO, Y., ANDO, K., NAKAMURA, S., HIRATA, M., YOSHIDA, T. and MATUNAGA, I. (2001)
Relationsh ips between lifestyle-re lated factors and immune parameters in middleJournal
aged male workers.
of Occupational Health
: 321-330 .
43(6)
(1996)Enhancin tghe functionality
of food proteinsby enzymatic
PANYAM, D. and KILARA, A.
modication.Trends in Food Science & Technology
7: 1205.
cation and characterizatio n
(2001) Puri
PARK,P.J.,JUNG,W.K.,NAM,K.S.,SHAHIDI,F.andKIM,S.K.
of antioxidative
peptidefromprotein
s
hydrolysate
of lectin-free
eggyolk. Journal of the American Oil
Chemists Society
: 651-656.
78(6)
(2004) Proteolytic fragments of
PELLEGRINI,A.,HULSMEIER,A.J.,HUNZIKER,P.andTHOMAS,U.
ovalbumin display antimicrobial activity
Biochimica
.
et Biophysica Acta
: 76-85.
1672
(2000) Effect
PELLEGRINI, A., THOMAS, U.,WIL, P.,SCHRANER, E.and VONFELLENBERG, R.
ed lysozyme fragments on DNA and RNA synthesis and membrane permeability of
of lysozyme or modi
Echerichia coli. Microbiological Research
155: 69-77.
PICOT, S. BORDENAVE, S., DIDELOT, I., FRUITIER-ARNAUDIN, F., SANNIER, G.,
THORKELSSON, J.P., BERGE, F., GUERARD, A. and CHABEAUD, J.M. (2006) Antiproliferative
activity ofsh protein hydrolysates o n human breast cancerBiochemistry
cell lines. 4: 1217
1222.
2003)The relationship
betweenpeptidestructureand
POWERS, J.P.S. and HANCOCK, R.E.W. (
antibacterial activity
Peptides
.
24: 1681-16 91.
QIAN, Z-Y., JOLLS, P., MIGLIORE-SAMOUR, D., SCHOENTGEN, F. and FIAT, A-M. ( 1995) Sheep
K-casein peptides inhibit platelet aggregation.
Biochimica et Biophysica Acta
: 41 1-417.
1244
(1975)Regulationof gamma-glut amyl-cysteine
synthetase
by
RICHMAN, P.G. and MEISTER, A.
nonallosteri c feedback inhibition by glutathione.
Journal of Biological Chemistry
250: 1422-6.
uence of dietary
ber
2007) In
ROSE,D.J.,DEMEO,M.T.,KESHAVARZIAN,A.andHAMAKER,B.R.(
on inammatory bowel disease and colon cancer: importance of fermentation
Nutritionpattern.
Reviews
65:
51-62.
(2003) Antioxidant activity of peptides obtained from porcine
SAIGA,A.,TANABE,S.andNISHIMURA,T.
myobrillar proteins by protease treatment.
Journal of Agricultural and Food Chemistry
51: 3661-36 67.
SAKANAKA, S., TACHIBANA, Y., ISHIHARA, N. and JUNEJAJA, L.R. (2004) Antioxidant activity of
egg-yolk protein hydrolysates in a linoleic acid oxidation
Food
system.
Chem
istry86, 99-103.
(2009) Safety of protein hydrolys ates, fractions there of and bioactive peptides in human
SCHAAFSMA, G.
nutrition.
European Journal of Clinical Nutrition
1168.
63: 1 161
(1995)Productionand characterist of
icsprotein
SHAHIDI, F., HAN, X. Q. and SYNOWIECKI, J.
hydrolysates from capelin
Mallotus
(
villosus
). Food Chemistry
53: 285293.
TSUGE, N., EIKAWA, Y., NOMURA, Y., YAMAMOTO, M. and SUGISAWA, K. (1991) Antioxidative
activity of peptides prepared by enzymatic hydrolysis of egg white
NipponNogeikagakuKuishi
albumin.
65:
1635-1641.
Journal of Parenteral and Enteral
VINNARS, E.and WILMORE,D. (2003) History of parenteral nutrition.
Nutrition27: 225232.
VIOQUE, J., SANCHEZ-VIOQUE, R., CLEMENTE, A., PEDROCHE, J., BAUTISTA, J. and
of an extensiverapeseed
proteinhydrolysate.
MILLAN, F. (1999)Productionand characterization
Journal of the American Oil Chemists Society
76: 81923.
WATANABE, K., TSUGE, Y., SHIMOYAMADA, M., OGAMA, N. and EBINA, T. (1998)Antitumour
effectsof pronase-treated
fragments,
glycopeptides,
fromovomucinin heneggwhitein a doublegrafted
tumour system.
Journal of Agricultural and Food Chemistry
: 3033-3038.
46(8)

W orld's Poultry Science Journa l, V ol. 69, June 2013


385

Bioactive peptides from food proteins: E. Eckert et al.


(2007)Antioxidant
activityof trypticdigestof heneggyolk
XU, X., KATAYAMA, S. and MINE, Y.
phosvitin.
Journal of the Science of Food and Agriculture
87: 2604-2608.
ZHU,K.X.,ZHOU,H.M.andQIAN,H.F. (2006) Antioxidant and free radical scavenging activities of wheat
germ protein hydrolysates (WGPH) prepared withProcess
alcalase.
Biochemistry
41: 1296-1302.

386

W orld's Poult ry Sc ience Journa l, V ol. 69, June 2013

Вам также может понравиться