Biological activities and potential cosmeceutical applications of bioactive components from brown...

13
Biological activities and potential cosmeceutical applications of bioactive components from brown seaweeds: a review W. A. J. P. Wijesinghe You-Jin Jeon Received: 6 April 2011 / Accepted: 9 June 2011 / Published online: 17 June 2011 Ó Springer Science+Business Media B.V. 2011 Abstract Seaweeds are the primary producers of all aquatic ecosystems. Chemical constituents isolated from diverse classes of seaweeds exert a wide range of nutritional, functional and biological activities. Unique metabolites of seaweeds possess specific biological properties that make them potential ingre- dients of many industrial applications such as func- tional foods, pharmaceuticals and cosmeceuticals. Cosmeceuticals of natural origin are becoming more popular than synthetic cosmetics. Hence, the inves- tigation of new seaweeds derived functional compo- nents, a different source of natural products, has proven to be a promising area of cosmeceutical studies. Brown seaweeds also produce a range of active components including unique secondary metabolites such as phlorotannins and many of which have specific biological activities that give possibil- ities for their economic utilization. Brown seaweeds derived active compounds have been shown various functional properties including, antioxidant, antiwrin- kling, whitening, antiinflammatory and antiallergy. It is well-known that these kind of biological effects are closely associated with cosmeceutical prepara- tions. This communication reviews the current knowledge on brown seaweeds derived metabolites with various biological activities and the potential use as cosmeceutical ingredients. It is hoped that the reviewed literature on multifunctional properties of brown seaweeds will improve access to the seaweed based natural products specially the ability to incor- porate these functional properties in cosmeceutical applications. Keywords Biological properties Natural products Phaeophyceae Phytochemicals Secondary metabolites Introduction Seaweeds belong to a group of organisms that has enormous ecological importance and represent a significant proportion of the world’s biodiversity. They are large and diverse group of organisms which play vital ecological roles in marine communities. It falls into three broad categories as brown, red and green seaweed based on pigmentation (Dawczynski et al. 2007). Seaweeds have always been of great interest in Asian culture as marine food sources (Rioux et al. 2009). In contrast, seaweeds represent an important economical resource mostly in the W. A. J. P. Wijesinghe Y.-J. Jeon (&) School of Marine Biomedical Sciences, Jeju National University, Jeju 690-756, Republic of Korea e-mail: [email protected] Y.-J. Jeon Marine and Environmental Research Institute, Jeju National University, Hamdok, Jeju 695-814, Republic of Korea 123 Phytochem Rev (2011) 10:431–443 DOI 10.1007/s11101-011-9214-4

Transcript of Biological activities and potential cosmeceutical applications of bioactive components from brown...

Biological activities and potential cosmeceutical applicationsof bioactive components from brown seaweeds: a review

W. A. J. P. Wijesinghe • You-Jin Jeon

Received: 6 April 2011 / Accepted: 9 June 2011 / Published online: 17 June 2011

� Springer Science+Business Media B.V. 2011

Abstract Seaweeds are the primary producers of all

aquatic ecosystems. Chemical constituents isolated

from diverse classes of seaweeds exert a wide range

of nutritional, functional and biological activities.

Unique metabolites of seaweeds possess specific

biological properties that make them potential ingre-

dients of many industrial applications such as func-

tional foods, pharmaceuticals and cosmeceuticals.

Cosmeceuticals of natural origin are becoming more

popular than synthetic cosmetics. Hence, the inves-

tigation of new seaweeds derived functional compo-

nents, a different source of natural products, has

proven to be a promising area of cosmeceutical

studies. Brown seaweeds also produce a range of

active components including unique secondary

metabolites such as phlorotannins and many of which

have specific biological activities that give possibil-

ities for their economic utilization. Brown seaweeds

derived active compounds have been shown various

functional properties including, antioxidant, antiwrin-

kling, whitening, antiinflammatory and antiallergy.

It is well-known that these kind of biological effects

are closely associated with cosmeceutical prepara-

tions. This communication reviews the current

knowledge on brown seaweeds derived metabolites

with various biological activities and the potential use

as cosmeceutical ingredients. It is hoped that the

reviewed literature on multifunctional properties of

brown seaweeds will improve access to the seaweed

based natural products specially the ability to incor-

porate these functional properties in cosmeceutical

applications.

Keywords Biological properties � Natural

products � Phaeophyceae � Phytochemicals �Secondary metabolites

Introduction

Seaweeds belong to a group of organisms that has

enormous ecological importance and represent a

significant proportion of the world’s biodiversity.

They are large and diverse group of organisms which

play vital ecological roles in marine communities. It

falls into three broad categories as brown, red and

green seaweed based on pigmentation (Dawczynski

et al. 2007). Seaweeds have always been of great

interest in Asian culture as marine food sources

(Rioux et al. 2009). In contrast, seaweeds represent

an important economical resource mostly in the

W. A. J. P. Wijesinghe � Y.-J. Jeon (&)

School of Marine Biomedical Sciences, Jeju National

University, Jeju 690-756, Republic of Korea

e-mail: [email protected]

Y.-J. Jeon

Marine and Environmental Research Institute,

Jeju National University, Hamdok, Jeju 695-814,

Republic of Korea

123

Phytochem Rev (2011) 10:431–443

DOI 10.1007/s11101-011-9214-4

countries of East and south Asia where they are not

only largely harvested but also intensively and

largely employed in the human nutrition (Caliceti

et al. 2002). Seaweeds or marine macro algae are

potential renewable resource in the marine environ-

ment and known to be extremely rich source of

bioactive compounds (Chandini et al. 2008; Kladi

et al. 2004). Therefore, algae can be a very interesting

natural source of new metabolites with various

biological activities that could be used as functional

ingredients (Kashman and Rudi 2004; Plaza et al.

2008). Biological activities are correlated to the

presence of chemical compounds, particularly sec-

ondary metabolites. The presence of these com-

pounds may assist in predicting some traditional uses

of medicinal plants (Kamatou et al. 2008). However,

novel potential areas have to be explored in order to

maximize the effective utilization of seaweeds.

The Phaeophyceae or brown seaweeds are a large

group of multicellular algae, and they play an

important role in marine environments both as food,

and for the habitats they form. Most brown

seaweeds contain the pigment fucoxanthin and

various pheophycean tannins which are responsible

for the distinctive greenish-brown colour as the

name indicated. Worldwide there are about 1,500

species of brown seaweeds and they produce vast

numbers of useful active components (Davis et al.

2003; Reddy and Urban 2009). Some species are of

sufficient commercial importance, such that they

have become subjects of extensive research in their

own right.

The term cosmeceutical is now commonly used to

describe a cosmetic product that exerts a pharmaceu-

tical therapeutic benefit (Choi and Berson 2006).

Therefore, cosmeceuticals are cosmetic products with

biologically active ingredients purporting to have

medical or drug-like benefits. Dermatological

research suggests that the bioactive ingredients used

in cosmeceuticals do indeed have benefits beyond the

traditional cosmetics such as creams, lotions, and

ointments (Chen et al. 2005; Schurch et al. 2008).

There are a number of synthetic components have

been extensively used as ingredients for cosmetics.

The interactions between cosmetics and skin are

complex (Gao et al. 2008). Therefore, during the past

decades the toxicological safety of cosmetics and

their ingredients has attracted increasing attention

(Nohynek et al. 2010). Today, there is a growing

consumer demand for personal care products con-

taining natural ingredients without any adverse

effects (Antignac et al. 2011). In response, there has

been a dramatic growth in the sales of natural

personal care products. As a result, recent investiga-

tions have focused on natural substances derived

from plant materials which could be incorporated in

cosmeceutical products instead of synthetic materials.

The active components of seaweeds are varied.

Focusing on natural products, recent trends in

cosmeceutical research from natural sources suggest

that seaweeds are a promising group to novel

biochemically active substances (Heo et al. 2009).

Moreover, seaweed extracts or pure compounds

isolated from seaweeds have a growing role to play

in the cosmeceutical field. The purpose of this paper

is to review the current findings on biological

properties of brown seaweeds with their potential

cosmeceutical applications. In addition, attempts

have also been made to update the information

covered in recent articles on the subject and present

communication therefore aims towards the assess-

ment of biologically active components from brown

seaweeds with reference to cosmeceutical

applications.

Skin care and cosmeceuticals of different

categories

Unlike other organs, skin is in direct contact with the

environment and therefore undergoes aging as a

consequence of environmental damage (Fisher et al.

2002). Sun-exposed or photoaged skin is typically

coarse and rough with deep lines and wrinkles and

irregular pigmentation (Jenkins 2002). In addition,

Free radical damage causes wrinkles by activating the

metalloproteinases that break down collagen. There

are several factors that start this cascading process

including exposure to UV radiation in sunlight,

smoking and exposure to air pollution. A number of

factors including adverse environmental conditions

can cause skin dryness. Therefore, well accepted

practice is that dry skin can be improved by hydrating

the outermost layer of the skin with a humectant or

occlusive agent, smoothing the rough surface with an

emollient, and normalizing the stratum corneum by

moisturization.

432 Phytochem Rev (2011) 10:431–443

123

Being a vital organ, the skin must be nourished and

nowadays various types of skin care cosmeceutical

products are proliferating in the market. This is due to

demand of consumers all over the world. Cellulites,

wrinkles, acne, rashes, dermatitis, and other skin

ailments are just some of the skin problems that need

to look out for. Skincare products are manufactured

with the sole purpose of taking care of the skin.

Cosmeceuticals are category of cosmetic products

claimed to have biologically active ingredients with

medicinal or drug like benefits (Gao et al. 2008). They

are topically applied products that are more than

merely cosmetic, yet are not true drugs that have

undergone rigorous placebo controlled studies for

safety and efficacy (Reszko et al. 2009). Furthermore,

they satisfy the needs of beauty and health. At present,

a wide range of cosmetic products with biologically

active ingredients have been developed and marketed.

Protection, whitening or depigmenting, tanning, anti-

wrinkling, deodorant, antiaging and moisturizing are

the main intended activities of skin care cosmeceuti-

cals. Chemically synthesized synthetic substances or

extracted substances from plants or animals can be

used as functional ingredients in the production of

functional cosmetics (Gao et al. 2008). Important

biological effects of brown seaweeds which related to

cosmeceutical applications are illustrated in Fig. 1.

Bioactive compounds from brown seaweeds

with various functional properties

as cosmeceutical ingredients

Phlorotannins (brown algal polyphenols)

As many of polyphenols are found in plants, they are

also described as phytochemicals. Polyphenolic com-

pounds are large and diverse group of naturally

occurring compounds containing phenolic function-

ality are secondary metabolites which exist both in

terrestrial and aquatic environments (Shibata et al.

2002; Susanto et al. 2009). Since these naturally

occurring polyphenols are known to have numerous

biological activities, they are found to be potential

candidates for various industrial applications such as

functional foods, pharmaceuticals, nutraceuticals and

cosmeceuticals. Tannins are defined as naturally

occurring plant polyphenolic compounds and are

widespread among terrestrial and marine plants. In

contrast to terrestrial tannins, phlorotannins have

been found only in marine brown seaweeds. They are

structurally less complex than terrestrial tannins, and

are produced entirely by polymerization of phloro-

glucinol (Glombitza and Hauperich 1997; Kang et al.

2007; Koivikko et al. 2005; Wang et al. 2008). Over

the years, the roles and functions of phlorotannins

Fig. 1 Schematic showing

cosmeceutical properties of

brown algae

Phytochem Rev (2011) 10:431–443 433

123

have been the subject of many studies. In addition, a

number of phlotrotannin compounds were isolated

from different brown seaweeds such as E. cava,

E. radiata, E. bicyclis and E. kurome. Figure 2 shows

the chemical formulae of important phlorotannins

isolated from brown seaweeds.

Fucoxanthin

Fucoxanthin (Fig. 3a) is a natural pigment that falls

under the broad category of carotenoids (Satomi and

Nishino 2009). Among the carotenoids, fucoxanthin

is one of the major xanthophyll variants in brown

seaweeds (Kim et al. 2010b). It is found in edible

brown algae such as U. pinnatifida, S. fulvellum,

L. japonica and H. fusiformis along with h-carotene,

is one of the most abundant carotenoids found in

nature (Hosokawa et al. 2004; Woo et al. 2010). The

presence of fucoxanthin in all algae species can be

readily externally determined by examining their

colour. It is found as an accessory pigment in the

chloroplasts of brown algae and most other hetero-

konts, giving them a brown or olive-green colour as

the name suggests. Currently, much research is being

conducted on how to extract fucoxanthin from certain

species of brown algae, which would allow use of the

substance in many functional applications. Some

metabolic and nutritional studies carried out on rats

and mice at Hokkaido University indicate that

fucoxanthin promotes fat burning within fat cells in

white adipose tissue by increasing the expression of

thermogenin (Maeda et al. 2005). In addition, fuco-

xanthin was found to exhibit number of biological

functions including antiinflammatory and antioxidant

effects (Shang et al. 2010).

Fig. 2 The chemical

formulae of phlorotannin

compounds isolated from

the marine brown seaweeds

434 Phytochem Rev (2011) 10:431–443

123

Bioactive polysaccharides

Over the years, bioactive polysaccharides isolated

from natural sources have attracted much attention in

the field of pharmacology (Yang and Zhang 2009).

Seaweeds contain a significant amount of soluble

polysaccharides, and have potential function as

dietary fiber. Specially, brown seaweeds are known

to produce functional polysaccharides such as algi-

nates and fucoidans (Lee et al. 2008). Fucans and

alginic acid derivatives exhibit different biological

properties including anticoagulant, antiinflammatory,

antiviral and antitumoral activities (Boisson-Vidal

et al. 1995; Costa et al. 2010).

Alginic acid (Fig. 3b), is a gelling polysaccharide

contains 1, 4-linked b-D-mannuronic and a-L-gulu-

ronic acid residues arranged in a non-regular, block-

wise order along the chain (Andrade et al. 2004;

Moore et al. 2004). It is also called algin or alginate,

and this naturally occurring hydrophilic colloidal

polysaccharide distributed widely in the cell walls

and intracellular material of the marine brown

seaweeds. In addition, it is the major structural

polysaccharide of brown seaweeds (Leal et al. 2008).

Acid polysaccharides found in brown algal cell wall

are mainly composed of alginic acid and fucoidan.

Alginate produced by brown seaweeds is widely used

in various pharmaceutical preparations and also it is a

useful additive in food industry for preparation of

thickening drinks, jellies and ice cream (Cardozo

et al. 2007; Yamasaki et al. 2005) Cosmetic industry

uses alginic acid as a thickening and water-binding

agent because, alginate absorbs water quickly, which

makes it useful as an additive in cosmetic

formulations.

Fucoidan (Fig. 3c) refers to a type of polysaccha-

ride which contains substantial percentages of

L-fucose and sulfate ester groups, found mainly in

various species of brown seaweeds (Matou et al.

2002; Li et al. 2008). It is a sulfated polysaccharide

found in the cell-wall matrix of brown seaweeds

(Kim et al. 2010a; Teruya et al. 2007). Among the

sulfated polysaccharides, often called fucoidans

found in marine brown algae, are well-known to

have potent biological activities such as antiinflam-

matory and antioxidant (Jiang et al. 2010). Biological

activities of fucoidans seem to be determined by their

high degree of sulfation, although, these activities

depend on the fine structure and molecular weight

(Zvyagintseva et al. 2003). The fucoidan is capable of

exhibiting skin cosmeticizing effects. Therefore, it is

an interesting functional ingredient with potential for

topical cosmetic formulations. Polygalactosides react

with the protective outer surface of the skin and the

ion–ion interaction form a protective moisturizing

complex, while the fucose polymers are hygroscopic

and act as hydrating agents. Fucus contains abundant

non-essential and essential amino acids, such as

proline, glycine and lacing all of which are found in

the elastic fibers in the skin. With this in mind, the

brown algal sulfated polysaccharide fucoidan would

be helpful for the maintenance of the skin’s elasticity

by increasing hydration and thereby improving the

skin’s elasticity.

Biological activities of brown seaweeds

with special focuses on cosmeceutical applications

Antioxidants

Antioxidants are compounds that protect cells against

the damaging effects of reactive oxygen species

(ROS), such as single oxygen, superoxide, peroxyl

radicals, and hydroxyl radicals. An imbalance

between antioxidants and ROS results in oxidative

stress, leading to cellular damage. Oxidative stress

has been linked to cancer, aging and inflammation.

Fig. 3 Chemical structures of (a) Fucoxanthin, (b) Alginic

acids, (c) Fucoidans

Phytochem Rev (2011) 10:431–443 435

123

Antioxidants protect skin against damaging effects

from ROS (Weber et al. 1997). Therefore, antioxi-

dants have the great popularity as primary ingredients

in cosmetics as functional ingredients (Lupo 2001).

In the recent times many researchers were given

attention on natural antioxidant sources which can be

utilized in many industrial applications. Therefore,

natural antioxidant extracts have attracted increasing

interest in cosmeceutical applications (Sun and Ho

2005).

Three phlorotannins purified from brown seaweed

E. cava namely phloroglucinol, eckol and dieckol

found to possess antioxidant activities (Ahn et al.

2007). In the study, antioxidant activities were

measured by electron spin resonance spectrometry

(ESR) technique for scavenging effects of free

radicals and comet assay was used to determine the

protecting effects against H2O2-mediated DNA dam-

age. In another recent study, eckol protects V79-4

cells against oxidative damage by enhancing the

cellular antioxidant activity and modulating cellular

signal pathway (Kang et al. 2005). In addition,

promising antioxidant properties of E. cava were

reported with novel phlorotannin derivatives (Li et al.

2009). By contrast, they have reported the profound

antioxidant properties of 6,60-bieckol, dieckol and

fucodiphloroethol among the isolated compounds. A

recent study suggests that, triphlorethol-A a phloro-

tannin found in E. cava, protects V79-4 cells against

oxidative stress induced cell death through up

regulation of HO-1 (Kang et al. 2007). In addition,

triphlorethol-A protects cells against oxidative dam-

age induced by radiation through reducing ROS

(Kang et al. 2006). In another study, an antioxidant

phloroglucinol was isolated and the isolated com-

pound found to possess similar antioxidant activity

with L-ascorbic acid (Lee et al. 1996). One of our

previous works demonstrated the antioxidant effect of

fermented E. cava processing by-product (Wijesinghe

et al. 2011). Further we reported that, the antioxidant

activity of E. cava processing by-product mainly due

to the phlorotannins in the extract.

Experimental finding revealed that cytoprotective

effect of fucoxanthin, a natural carotenoid isolated

from brown seaweed S. siliquastrum (Heo et al.

2008). A protective effect against oxidative stress-

induced cell apoptosis was also demonstrated via

nuclear staining with Hoechst dye. The findings

clearly indicate that fucoxanthin isolated from

S. siliquastrum possesses prominent antioxidant

activity.

In vitro antioxidant activities of three selected

Indian brown seaweeds namely S. marginatum, P.

tetrastomatica and T. conoides were reported (Chan-

dini et al. 2008). Turbinaria conoides had signif-

icantly higher phenol content compared to the other

two species. In vitro antioxidant activity of metha-

nolic extracts from all the three seaweeds showed in a

dose dependent manner. In another recent study, in

vitro and cellular antioxidant activities of methanolic

extracts of brown seaweeds were reported (O’Sulli-

van et al. 2011). As they reported brown seaweeds

F. vesiculosus and F. serratus extracts were seen to

be the most effective extracts in terms of antioxidant

activity.

It is anticipated that the antioxidant effects of

brown seaweeds could be used for cosmeceutical

preparations. Free radical damage is one of the

principal mechanisms of aging. Skin suffers addi-

tional free radical damage from sunlight to pollu-

tants. When it comes to wrinkles, free radical

damage causes collagen and other vital skin func-

tions to break down. Topical antioxidants provide

some protection against environmental damage to

the skin and may be effective in slowing down the

skin aging because treatment with some antioxi-

dants, such as ascorbic acid, tocopherols, and

polyphenols, should be effective to enhance resis-

tance to oxidative stress and prevent skin aging

(Masaki 2010).

Cosmeceuticals are commercially available prod-

ucts that can not only improve the appearance of the

skin but also benefit to the health of the skin because

of their antioxygenation (Guan et al. 2005). A great

skincare product, whether it comes in a liquid, gel,

serum, lotion, or cream, should contain a potent

assortment of stable antioxidants to interrupt free

radical damage and keep it from harming the skin. It

is easy to realize that one of the most effective

ingredients of cosmeceuticals is the antioxidant

which can interrupt the radical-chain processes, help

the skin to repair systems. According to the above

mentioned research findings, brown seaweeds could

be considered as very good natural source of

antioxidants. In contrast, antioxidant effects of

phlorotannins ideally coupled with cosmeceuticals

because free radical damage is one of the major

causes of skin aging.

436 Phytochem Rev (2011) 10:431–443

123

Protective effect against UV light-induced skin

damage

Ultraviolet radiation, the most biologically active

component of sunlight, is the major environmental

risk factor for all skin cancers (Xu et al. 2000). In

addition, sunlight has a profound effect on the skin

causing premature skin aging, and a host of skin

changes. UV-B radiation is responsible for a wide

range of potentially damaging human and animal

health effects, primarily related to the skin, eyes, and

immune system. There is evidence that UVB radia-

tion interacts directly with cellular targets like DNA

(de la Coba et al. 2009). Human exposure to UV-B

depends upon an individual’s location, the duration

and timing of outdoor activities and precautionary

behavior such as the use of sunscreen, sunglasses, or

protective clothing. An individual’s skin colour and

age can influence the occurrence and severity of some

of the health effects from exposure to UV-B. Topical

application of sunscreens is widely advocated for

prevention of UV induced sunburn, photoaging, and

skin cancer (Torres et al. 2006). Recent studies have

focused on marine organisms as a source of natural

bioactive molecules and some UV-absorbing algal

compounds are under investigation as candidates for

new natural sunscreens (de la Coba et al. 2009).

Therefore, in this report here we discuss the protec-

tive effect of active components from brown sea-

weeds against UV damage.

Fucoxanthin, a natural carotenoids isolated from

the marine brown alga S. siliquastrum has the ability

to protect against oxidative stress induced by UV-B

radiation and which might be applied to antioxidant

and cosmeceutical industries (Heo and Jeon 2009). In

contrast, they investigated and confirmed the protec-

tive effect of fucoxanthin on UV-B induced cell

injury in human fibroblasts. In addition fucoxanthin

significantly scavenged the ROS generated by expo-

sure to UV-B radiation.

Polyphenolic compounds of brown seaweeds

found to involve in protection mechanisms, against

UV damage (Connan et al. 2007). Dieckol, isolated

from a brown alga E. cava exhibited prominent

protective effect against photo-oxidative stress

induced by UV-B radiation (Heo et al. 2009; Ko

et al. 2010). Dieckol, phenolic moiety, is a kind of

phlorotannin which consists of six phloroglucinol

units (hexamer) and functional hydroxyl groups.

In another recent experiment carmalol derivative,

diphlorethohydroxycarmalol isolated from the brown

algae I. okamurae showed strong protective effect

against intracellular ROS induced by UV-B radiation

(Heo et al. 2010).

Over-exposure to UV radiation provokes acute

sunburn reaction (Thiele et al. 1997). Skin is the

preferred target of oxidative stress as continuously

exposed to UV radiation from sunlight to environ-

mental oxidizing pollutants. As mentioned in the

previous reports with phlorotannins, they represent an

interesting class of active polyphenolic compounds in

the protection of UV light-induced skin damage.

Together with the scientific evidence that do support

their use in cosmeceutical preparations.

Tyrosinase inhibitory activity and inhibition

of melanin synthesis

Melanin is a pigment which is primarily responsible

for the colour of skin, eyes and hair. Melanocytes are

melanin-producing cells located in the bottom layer

of the skin’s epidermis and the middle layer of the

eye. Through a process called melanogenesis, these

cells produce melanin. Exposure to UV-B radiation

causes an increased melanogenesis as a response to

DNA photodamage (Agar and Young 2005). Tyros-

inase is an enzyme which is required for melanocytes

to produce melanin from the amino acid tyrosine. In

addition, tyrosinase is the key enzyme for the

synthesis of melanin pigment is completed by a

series of oxidative reactions (Gao et al. 2008). Thus,

in mammals tyrosinase is responsible for pigmenta-

tion of the skin, eyes and hair (Likhitwitayawuid

2008). The study of tyrosinase inhibitory activity

became of interest in recent years because of the

significant industrial and economic impact of the

inhibitors of this protein (Fails et al. 2009). In

contrast, inhibition of tyrosinase activity might be

useful in cosmeceutical applications for depigmenta-

tion. Up to date a number of tyrosinase and melano-

genesis inhibitors, from both natural and synthetic

sources, have been identified (Sima et al. 2011).

One of the previous reports indicated that, extracts

of marine brown algae E. cava and S. silquastrum

reduced melanin synthesis and tyrosinase activity

both in vitro and zebra fish animal model (Cha et al.

2010). Hence, the results provided that the both

brown algal extracts could be used as an ingredient in

Phytochem Rev (2011) 10:431–443 437

123

whitening cosmetics. The inhibitory effect of phloro-

tannins isolated from E. cava on mushroom tyrosi-

nase activity and melanin formation in mouse

B16F10 melanoma cells was reported (Yoon et al.

2009). They assessed the feasibility of phlorotannins

isolated from E. cava as an inhibitor of melanin

formation and the results suggested that 7-phloroec-

kol might prove useful as a novel inhibitor of melanin

formation in cosmetic applications.

Ecklonia stolonifera OKAMURA (Laminariaceae)

belonging to brown algae, showed high tyrosinase

inhibitory activity (Kang et al. 2004). Their work

showed that phloroglucinol derivatives, isolated from

E. stolonifera OKAMURA, could be involved in the

control of pigmentation in plants and other organisms

through inhibition of tyrosinase activity. In another

recent experiment suggested that dieckol, phlorotan-

nin isolated from E. cava has an ability to inhibit

tyrosinase activity in relatively higher manner than a

commercial tyrosinase inhibitor kojic acid (Heo et al.

2009). The results also proved the ability of the

specific phlorotannin compound to use in cosmeceu-

tical applications. Potential inhibitory effect of

marine brown algae I. okamurae on melanogenesis

was assessed via tyrosinase inhibitory effect (Heo

et al. 2010). Interestingly according to the results the

active compound diphlorethohydroxycarmalol exhib-

ited higher levels of activity than that of commercial

whitening agent.

It now appears that important actions can be

attributed to some secondary metabolites of brown

algae, and evidence indicates that their potential

whitening effect which could be employed in

cosmeceutical applications. In addition, it is well-

known that oxidative stress caused by free radicals

leads to hyperpigmentation. Therefore, the antioxi-

dant properties of brown seaweeds also an additional

benefit for depigmentation.

Matrix metalloproteinases (MMPs) inhibitory

activity

Matrix metalloproteinases (MMPs) are zinc-depen-

dent endopeptidases. The MMPs belong to a larger

family of proteases known as the metzincin super-

family. Collectively they are capable of degrading all

kinds of extracellular matrix proteins, but also can

process a number of bioactive molecules. The

functional properties of skin depend on the integrity

of collagen in the dermis. Moreover, collagen is

tightly controlled by matrix metalloproteinases (Fujii

et al. 2008). Cellular changes as well as qualitative

and quantitative alterations of dermal extracellular

matrix proteins are involved, resulting in loss of

recoil capacity and tensile strength with wrinkle

formation (Kochanek et al. 2000). The skin matrix is

responsible for the skin’s mechanical properties,

including firmness, strength, suppleness and elastic-

ity. To a large degree, the signs of skin aging reflect

the condition of the skin matrix, the weaker and less

regular the matrix, the more wrinkles and roughness.

With increasing age, collagen synthesis becomes

lower and MMP-1 (Interstitial collagenase) levels

become higher in naturally aged human skin, and

these alterations cause changes such as skin wrinkling

and loss of elasticity (Moon et al. 2004). Therefore,

control of collagen metabolism might be one of the

important properties in functional cosmetics.

Kim et al. (2006) reported the inhibitory effects of

E. cava extract on MMP activities. For the first time

they reported a detailed study on the inhibitory

effects of phlorotannins in brown algae, E. cava on

MMP activities in cultured human cell lines. Further,

E. cava extract did not exert any cytotoxic effect on

the used cell line at tested concentrations anticipating

its potential use as a safe MMP inhibitor which can

be utilized in cosmeceutical applications.

Antiinflammatories and antiallergies

Inflammation is the complex biological response of

vascular tissues to harmful stimuli and inflammation

is a protective attempt by the organism to remove

the injurious stimuli as well as initiate the healing

process for the tissue. Macrophages are key players

in inflammation (Kazlowska et al. 2010). Oxidative

stress induced inflammation is mediated by the

activation of NF-kB and AP-1. The undesired

effects of oxidative stress have been found to be

controlled by the antioxidant and/or antiinflamma-

tory effects of dietary polyphenols (Han et al. 2007).

Antiallergic agents can be used to treat allergic

reactions and most of these agents act by preventing

the release of inflammatory mediators or inhibiting

the actions of released mediators on their target

cells. To date there have been recent investigations

supporting the antiinflammatory properties of brown

seaweeds.

438 Phytochem Rev (2011) 10:431–443

123

The potent effect of the phlorotannin compounds

from E. cava; eckol, 2 dieckol, 6,60-bieckol and

1-(30,50-dihydroxyphenoxy)-7-(200,400,600-trihydroxy-

phenoxy)—2,4,9-trihydroxydibenzo-1,4,-dioxin on

a host of commonly occurring diseases which possess

an inflammatory component, including osteoarthri-

tis, atherosclerosis and cancer were reported (Ryu

et al. 2008). Further, they reported that, these

compounds not only inhibited the proinflammatory

cytokines induced expression of MMP-1, -3 and -13

in MG-63 human osteoblasts but also exhibited

conversely regulate activation of ERK and p38

MAP kinases in NO-induced differentiation. In

addition, Jung et al. (2009) reported that ethanolic

extracts of E. cava inhibited LPS-induced nitric

oxide (NO) and prostaglandin E2 (PGE2) production

in a concentration-dependent manner and inhibit

inducible nitric oxide (iNOS) and cyclooxygenase

(COX)-2 in BV2 microglia. According to their results

further they have reported that E. cava extracts exert

antiinflammatory effects by suppressing proinflam-

matory cytokines. In another recent study revealed

Table 1 Summary of the biological activities of brown seaweeds with reference to cosmeceutical applications

Brown seaweed Active component Activity Potential cosmeceutical

application

References

E. cava Eckol Antioxidant Anti aging Ahn et al. (2007),

Kang et al. (2005)

E. cava 6,60-Bieckol, dieckol and

fucodiphloroethol

Antioxidant Anti aging Li et al. (2009)

E. cava Triphlorethol-A Antioxidant Anti aging Kang et al. (2007)

E. cava Triphlorethol-A Antioxidant Anti aging Kang et al. (2006)

E. cava Phlorotannins Antioxidant Anti aging Wijesinghe et al. (2011)

S. siliquastru Fucoxanthin Antioxidant Cytoprotective Heo et al. (2008)

S. marginatum,

P. tetrastomaticaand T. conoides

Polyphenols Antioxidant Anti aging Chandini et al. (2008)

F. vesiculosusand F. serratus

Polyphenols Antioxidant Anti aging O’Sullivan et al. (2011)

E. cava Phlorotannins Anti inflammatory Ryu et al. (2008)

E. cava Phlorotannins Anti-allergic Lee et al. (2009)

S. siliquastrum Fucoxanthin Antioxidant Protect against oxidative

stress induced by UV-B

Heo and Jeon (2009)

E. cava Dieckol Antioxidant Protective effect against

photo-oxidative stress

Heo et al. (2009),

Ko et al. (2010)

I. okamurae Diphlorethohydroxycarmalol Antioxidant Protective effect against

UV light-induced skin

damage

Heo et al. (2010)

E. cava and

S. silquastrumReduce melanin

synthesis and

tyrosinase activity

Whitening Cha et al. (2010)

E. cava 7-Phloroeckol Inhibition of

melanin

formation

Whitening Yoon et al. (2009)

E. cava Dieckol Tyrosinase inhibitor Whitening Heo et al. (2009)

I. okamurae Diphlorethohydroxycarmalol Tyrosinase inhibitor Whitening Heo et al. (2010)

E.cava Phlorotannins MMP inhibitor Anti wrinkling Kim et al. (2006)

E.cava Ethanolic extracts Anti inflammatory Jung et al. (2009)

E. stolonifera Phlorotannins Tyrosinase inhibitor Whitening Kang et al. (2004)

E. stolonifera Phloroglucinol Antioxidant Anti aging Lee et al. (1996)

Phytochem Rev (2011) 10:431–443 439

123

that dieckol and 6,60-bieckol; phlorotannins isolated

from brown alga E. cava, showed prominent antial-

lergic activities (Le et al. 2009). Furthermore, they

have suggested the potential antiallergic mechanism

with the results of flow cytometric analysis, as the

suppression of binding activity between IgE and

FceRI.

Today, in the modern market, there is an increasing

number of novel cosmeceutical products are available

with the functional ingredients such as fucoidan and

alginate from brown seaweeds. As natural marine

products, these extracts are ideal for inclusion in

cosmeceuticals (Fitton et al. 2007). The preparations

could be facilitated to maintain the skin health in

many ways. However, cosmeceutical industries are

still waiting for some exciting development to happen.

Formulation of cosmeceuticals involves an effective

use of scientific findings and selection of appropriate

combination of functional ingredients in the formula.

Ultimately the typical components of the cosmeceu-

ticals needed to achieve the expected performance

such as anti aging, anti wrinkling and whitening. The

use of these brown algal extracts or compounds sit

well with the recent trend for natural product formu-

lations and provide the opportunity to offer a cosme-

ceutical solution from systemic to a topical approach.

Brown seaweeds representing the candidate ingredi-

ents of cosmeceuticals with their potential cosmeceu-

tical applications are summarized in the Table 1.

Conclusion

Marine organisms are rich sources of structurally

novel and biologically active metabolites with valu-

able industrial potentials. Therefore, this review

refers to extracts of brown seaweeds, and chemically

defined compounds of natural origin showing various

biological effects. In contrast, brown seaweeds pro-

duce a variety of remarkable polyphenolic com-

pounds (phlorotannins), polysaccharides and

carotenoids collectively referred to as bioactive

components. The relevant substances are diverse in

their chemical structure and physiological functions.

It is interesting to note that functional metabolites

from brown seaweeds offer a promising approach for

the cosmeceutical preparations. In conclusion, brown

seaweeds have been identified as potential and easily

accessible producers of a wide spectrum of natural

substances of vital cosmeceutical needs. The potent

biological activities of certain active components

isolated from brown seaweeds may represent an

interesting advance in the search for novel functional

ingredients.

Conflicts of interest The authors declare that there are no

conflicts of interest.

References

Agar N, Young AR (2005) Melanogenesis: a photoprotective

response to DNA damage. Mutat Res 571:121–132

Ahn GN, Kim KN, Cha SH, Son CB, Lee J, Heo MS, Yeo IK,

Lee NH, Jee YH, Kim JS, Heu MS, Jeon YJ (2007)

Antioxidant activities of phlorotannins purified from

E. cava on free radical scavenging using ESR and H2O2-

mediated DNA damage. Eur Food Res Technol 226:71–79

Andrade LR, Salgado LT, Farina M, Pereira MS, Mourao PAS,

Amado-Filho GM (2004) Ultrastructure of acidic poly-

saccharides from the cell walls of brown algae. J Struct

Biol 145:216–225

Antignac E, Nohynec GJ, Re T, Clouzeau J, Toutain H (2011)

Safety of botanical ingredients in personal care products/

cosmetics. Food Chem Toxicol 49:324–341

Boisson-Vidal C, Haroun F, Ellouali M, Blondin C, Fischer

AM, de Agostini A, Josefonvicz J (1995) Biological

activities of polysaccharides from marine algae. Drugs

Futur 20:1237–1249

Caliceti M, Argese E, Sfriso A, Pavoni B (2002) Heavy metal

contamination in the seaweeds of the Venice lagoon.

Chemosphere 47:4436–4454

Cardozo KHM, Guaratini T, Barros MP, Falcao VR, Tonon

AP, Lopes NP, Campos S, Torres MA, Souza AO,

Colepicolo P, Pinto E (2007) Metabolites from algae with

economical impact. Comp Biochem Phys C146:60–78

Cha SH, Ko SC, Kim D, Jeon YJ (2010) Screening of marine

algae for potential tyrosinase inhibitor: those inhibitors

reduced tyrosinase activity and melanin synthesis in zebra

fish. J Dermatol 37:1–10

Chandini SK, Ganesa P, Bhaskar N (2008) In vitro antioxidant

activities of three selected seaweeds of India. Food Chem

107:707–713

Chen Z, Seo JY, Kim YK, Lee SR, Kim KH, Cho KH, Eun HC,

Chung JH (2005) Heat modulation of tropoelastin, fibril-

lin-1, and matrixmetalloproteinase-12 in human skin in

vivo. J Invest Dermatol 124:70–78

Choi CM, Berson DS (2006) Cosmeceuticals. Semin Cutan

Med Surg 25:163–168

Connan S, Deslandes E, Gall EA (2007) Influence of day-night

and tidal cycles on phenol content and antioxidant

capacity in three temperate intertidal brown seaweeds. J

Exp Mar Biol Ecol 349:359–369

Costa LS, Fidelis GP, Cordeiro SL, Oliveira RM, Sabry DA,

Camara RB, Nobre LT, Costa MS, Almeida-Lima J,

Farias EH, Leite EL, Rocha HA (2010) Biological activ-

ities of sulfated polysaccharides from tropical seaweeds.

Biomed Pharmacother 64:21–28

440 Phytochem Rev (2011) 10:431–443

123

Davis TA, Volesky B, Mucci A (2003) A review of the bio-

chemistry of heavy metal biosorption by brown algae.

Water Res 37:4311–4330

Dawczynski C, Schubert R, Jahreis G (2007) Amino acids,

fatty acids, and dietary fibre in edible seaweed products.

Food Chem 103:891–899

de la Coba F, Aguilera J, de Galves MV, Alvarez M, Figueroa

FL, Herrera E (2009) Prevention of ultraviolet effects on

clinical and histopathological changes, as well as the heat

shock protein-70 expression in mouse skin by topical

application of algal UV-absorbing compounds. J Dermatol

Sci 55:161–169

Fails A, Corda M, Era B, Fadda MB, Matos MJ, Quezada E,

Santana L, Picciau C, Podda G, Delogu G (2009) Tyros-

inase inhibitor activity of coumarin-resveratrol hybrids.

Molecules 14:2514–2520

Fisher GJ, Kang S, Varani J, Csorgo ZB, Wan Y, Datta S,

Voorhees JJ (2002) Mechanisms of photoaging and

chronological skin aging. Arch Dermatol 138:1462–1470

Fitton JH, Irhimeh M, Falk N (2007) Macroalgal fucoidan

extracts: a new opportunity for marine cosmetics. Cosmet

Toilet 122:55–64

Fujii T, Wakaizumi M, Ikami T, Saito M (2008) Amla (E.officinalis Gaertn.) extract procollagen production and

inhibits matrix metalloproteinase-1 in human skin fibro-

blasts. J Etnopharmacol 119:53–57

Gao XH, Zhang L, Wei H, Chen HD (2008) Efficiency and

safety of innovative cosmeceuticals. Clin Dermatol

26:367–374

Glombitza KW, Hauperich S (1997) Phlorotannins from the

brown alga C. torulosa. Phytochemistry 46:735–740

Guan Y, Chu Q, Fu L, Ye J (2005) Determination of antioxi-

dants in cosmetics by micellar electrokinetics capillary

chromatography with electrochemical detection. J Chro-

matogr A 1074:201–204

Han X, Shen T, Lou H (2007) Dietary polyphenols and their

biological significance. Int J Mol Sci 8:950–988

Heo SJ, Jeon YJ (2009) Protective effect of fucoxanthin iso-

lated from S. siliquastrum on UV-B induced cell damage.

J Photoch Photobiol B 95:101–107

Heo SJ, Ko SC, Kang SM, Kang HS, Kim JP, Kim SH, Lee

KW, Kim JP, Kim SH, Lee KW, Cho MG, Jeon YJ (2008)

Cytoprotective effect of fucoxanthin isolated from brown

algae S. siliquastrum against H2O2-induced cell damage.

Eur Food Technol 228Z:145–151

Heo SJ, Ko SC, Cha SH, Kang DH, Park HS, Choi YU, Kim D,

Jung WK, Jeon YJ (2009) Effect of phlorotannins isolated

from E. cava on melanogenesis and their protective effect

against photo-oxidative stress induced by UV-B radiation.

Toxicol In Vitro 23:1123–1130

Heo SJ, Ko SC, Kang SM, Cha SH, Lee SH, Kang DH, Jung

WK, Affan A, Oh C, Jeon YJ (2010) Inhibitory effect

against UV-B radiation-induced cell damage. Food Chem

Toxicol 48:1355–1361

Hosokawa M, Kudo M, Maeda H, Konho H, Tanaka T, Mi-

yashita K (2004) Fucoxanthin induces apoptosis and

enhances the antiproliferative effect of the PPARc ligand,

troglitazone, on colon cancer cells. Biochim Acta

1675:113–119

Jenkins G (2002) Molecular mechanisms of skin aging. Mech

Ageing Dev 123:801–810

Jiang Z, Okimura T, Yokose T, Yamasaki Y, Yamaguchi K,

Oda T (2010) Effect of sulfated, ascopphyllan, from the

brown alga A. nodosum on various cell lines: a compar-

ative study on ascophyllan and fucoidan. J Biosci Bioeng

110:113–117

Jung WK, Ahn YW, Lee SH, Choi YH, Kim SK, Yea SS, Choi

I, Park SG, Seo SK, Lee SW, Choi IW (2009) Eckloniacava ethanolic extracts inhibit lipopolysaccharide-induced

cyclooxygrnase-2 and inducible nitric oxide synthase

expression in BV2 microglia via the MMP kinase and NF-

jB patheays. Food Chem Toxicol 47:410–417

Kamatou GPP, Zyl RLV, Vuuren SFV, Figueiredo AC, Barr-

oso JG, Pedro LG, Viljoen AM (2008) Seasonal variation

in oil composition, oil toxicity and the biological activity

of solvent extracts of three South African Salvia species. S

Afr J Bot 74:230–237

Kang HS, Kim HR, Byun DS, Son BW, Nam TJ, Choi JS

(2004) Tyrosinase inhibitors isolated from the edible

brown alga E. stolonifera. Arch Pharm Res 27:1226–1232

Kang KA, Lee KH, Chae S, Zhang R, Jung MS, Lee Y, Kim

SY, Kim HS, Hong GJ, Park JW, Ham YM, Lee NH,

Hyun JW (2005) Eckol isolated from E. cava attenuates

oxidative stress induced cell damage in lung fibroblast

cells. FEBS Lett 579:6295–6304

Kang KA, Zhang R, Lee KH, Chae S, Kim BJ, Kwak YS, Park

JW, Lee NH, Hyun JW (2006) Protective effect of

Triphloretheol-A from E. cava against ionizing radiation

in vitro. J Radiat Res 47:61–68

Kang KA, Lee KH, Park JW, Lee NH, Na HK, Surh YJ, You

HJ, Chung MH, Hyun JW (2007) Triphlorethol-A induces

heme oxygenase-1 via activation of ERK and NF-E2nre-

lated factor 2 transcription factor. FEBS Lett 581:2000–

2008

Kashman Y, Rudi A (2004) On the biosynthesis of marine

isoprenoids. Phytochem Rev 3:309–323

Kazlowska K, Hsu T, Hou CC, Yang WC, Tsai GJ (2010)

Antiinflammatory properties of phenolic compounds and

crude extract from P. dentata. J Ethanopharmacol 128:

123–130

Kim MM, Ta QV, Mendis E, Rajapakse N, Jung WK, Byun

HG, Jeon YJ, Kim SK (2006) Phlorotannins in E. cavaextract inhibit matrix metalloproteinase activity. Life Sci

79:1436–1443

Kim KJ, Lee OH, Lee BY (2010a) Fucoidan, a sulfated poly-

saccharide, inhibits adipogenesis through the mitogen-

activated protein kinase pathway in 3T3–L1 preadipocytes.

Life Sci 86:791–797

Kim KM, Heo SJ, Kang SM, Ahn G, Jeon YJ (2010b) Fuco-

xanthin induces apoptosis in human leukemia HL-60 cells

through a ROS-mediated Bcl-xL pathway. Toxicol In

Vitro 24:1648–1654

Kladi M, Vagias C, Roussis V (2004) Volatile halogenated

metabolites from red algae. Phytochem Rev 3:337–366

Ko SC, Cha SH, Heo SJ, Lee SH, Kang SM, Jeon YJ (2010)

Protective effect of E. cava on UVB-induced oxidative

stress: in vitro and in vivo zebrafish model. J Appl Phycol

(in press). doi:10.1007/s10811-010-9565-z

Kochanek KS, Brenneisen P, Wenk J, Herrmann G, Ma W,

Kuhr L, Meewes C, Wlaschek M (2000) Photoaging of the

skin from phenotype to mechanisms. Exp Gerontol

35:307–316

Phytochem Rev (2011) 10:431–443 441

123

Koivikko R, Loponen J, Honkanen T, Jormalainen V (2005)

Contents of soluble, cell-wall-bound and exuded phloro-

tannins in the brown alga F. vesiculosus, with implica-

tions on their ecological aspects. J Chem Ecol 31:195–212

Le QT, Li Y, Qian ZJ, Kim MM, Kim SK (2009) Inhibitory

effects of polyphenols isolated from marine algae E. cavaon histamine release. Process Biochem 44:168–176

Leal D, Rossi M, Caruso F (2008) FT-IR spectra of alginic acid

block fractions in three species of brown seaweeds. Car-

bohyd Res 343:308–316

Lee JH, Park JC, Choi JS (1996) The antioxidant activity of

E. stolonifera. Arch Pharm Res 19:223–227

Lee NY, Ermakova SP, Zvyagintseva TN, Kang KW, Dong Z,

Choi S (2008) Inhibitory effects of fucoidan on activation

of epidermal growth factor receptor and cell transforma-

tion in JB6 C141 cells. Food Chem Toxicol 46:1793–1800

LI B, Lu F, Wei X, Zhao R (2008) Fucoidan: structure and

bioactivity. Molecules 13:1671–1695

Li Y, Quian ZJ, Ryu B, Lee SH, Kim MM, Kim SK (2009)

Chemical components and its antioxidant properties in

vitro: an edible marine brown alga, E. cava. Bioorg Med

Chem 17:1963–1973

Likhitwitayawuid K (2008) Stilbenes with tyrosinase inhibitory

activity. Curr Sci 94:44–52

Lupo MP (2001) Antioxidants and vitamins in cosmetics. Clin

Dermatol 19:467–473

Maeda H, Hosokawa M, Sashima T, Funayama K, Miyashita K

(2005) Fucoxanthin from edible seaweed, U. pinnatifida,

shows antiobesity effect through UCP1 expression in

white adipose tissues. Biochem Biophys Res Commun

332:392–397

Masaki H (2010) Role of antioxidants in the skin: anti-aging

effects. J Dermatol Sci 58:85–90

Matou S, Helley D, Chabut D, Bros A, Fisher AM (2002)

Effect of fucoidan on fibroblast growth factor-2-induced

angiogenesis in vitro. Thomb Res 106:213–221

Moon H, Chung JH, Lee JK, Zee OP (2004) Triterpenoid

saponin from V. hondoensis W. Becker, H. Boss and their

effect on MMP-1 and type 1 procollagen expressin. Arch

Pharm Res 27:730–733

Moore DE, Miao WG, Benikos C (2004) Quantitative deter-

mination of alginicacid in pharmaceutical formulations

using capillary electrophoresis. J Pharmaceut Biomed

34:233–238

Nohynek GI, Antignac E, Re T, Toutain H (2010) Safety

assessment of personal care products/cosmetics and their

ingredients. Toxicol Appl Pharmacol 243:239–259

O’Sullivan AM, O’Callaghan YC, O’Grady MN, Queguineur

B, Hanniffy D, Troy DJ, Kerry JP, O’Brien NM (2011) In

vitro and cellular antioxidant activities of seaweed

extracts prepared from five seaweeds harvested in spring

from the west coast of Ireland. Food Chem 126:1064–

1070

Plaza M, Cifuentes A, Ibanez E (2008) In the search of new

functional food ingredients from algae. Trends Food Sci

Tech 19:31–39

Reddy P, Urban S (2009) Meroditerpenoids from the southern

Australian marine brown alga S. fallax. Phytochemistry

70:250–255

Reszko AE, Berson D, Lupo MP (2009) Cosmeceuticals:

practical applications. Dermatol Clin 27:401–416

Rioux LE, Turgeon SL, Beaulieu M (2009) Effect of season on

the composition of bioactive polysaccharides from the

brown seaweed S. longicruris. Phytochemistry 70:1069–

1075

Ryu B, Li Y, Qian ZJ, Kim MM, Kim SK (2008) Exhibitory

effects of compounds from brown alga E. cava on the

human osteoblasts. Abstr J Biotechnol 136S:S588

Satomi Y, Nishino H (2009) Implication of mitogen-activated

protein kinase in the induction of G1 cell cycle arrests and

gadd45 expression by the carotenoid fucoxanthin in

human cancer cells. Biochem Biophys Acta 790:260–266

Schurch C, Blum P, Zulli F (2008) Potential plant cells in

culture for cosmetic application. Phytochem Rev 7:599–

605

Shang YF, Kim SM, Lee WJ, Um BH (2010) Pressurized liquid

method for fucoxanthin extraction from E. bicyclis (kjell-

man) setchell. J Biosci Bioeng (in press). doi:10.1016/

j.jbiosc

Shibata T, Yamaguchi K, Nagayama K, Kawagushi S,

Nakamura T (2002) Inhibitory activity of brown algal

phlorotannins against glycosidases from the viscera of the

turban shell T. cornutus. Eur J Phycol 37:493–500

Sima VH, Patris S, Aydogmus Z, Sarakbi A, Sandulescu R,

Kauffmann JM (2011) Tyosinase immobilized magnetic

nanobeads for the amperometric assay of enzyme inhibitors:

application to the skin whitening agents. Talanta 83:980–987

Sun T, Ho CT (2005) Antioxidant activities of buckwheat

extracts. Food Chem 90:743–749

Susanto S, Feng Y, Ulbricht M (2009) Fouling behavior of

aqueous solutions of polyphenolic compounds during

ultrafiltration. J Food Eng 91:333–340

Teruya T, Konishi T, Uechi S, Tamaki H, Tako M (2007) Anti-

proliferative activity of oversulfated fucoidan from com-

mercially cultured C. okamuranus TOKIDA in U937

cells. Int J Biol Macromol 41:221–226

Thiele JJ, Podda M, Packer L (1997) Tropospheric ozone an

emerging environmental stress to skin. Biol Chem

378:1299–1305

Torres A, Enk CD, Hochberg M, Srebnic M (2006) Porphyra-

334: a potential natural source for UVA protective

screens. Photochem Photobio S 5:432–435

Wang Y, Xu Z, Bach SJ, McAllister TA (2008) Effects of

phlorotanninsfrom A. nodosum (brown seaweed) on in

vitro ruminal digestion of mixed forage or barley rain.

Anim Feed Sci Tech 145:375–395

Weber C, Podda M, Rallis M, Thiele JJ, Traber MG, Packer L

(1997) Efficacy of topically applied tocopherols and to-

cotrienols in protection of murine skin from oxidative

damage induced by UV-irradiation. Free Radic Biol Med

22:761–769

Wijesinghe WAJP, Won-Woo L, Young-Mog K, Young-Tae

K, Se-Kwon K, Byong-Tae J, Jin-Soo K, Min-Soo H,

Won-Kyo J, Ahn G, Lee KW, Jeon YJ (2011) Value-

added fermentation of E. cava processing by-product and

its antioxidant effect. J Appl Phycol. doi:10.1007/s10811-

011-9668-1

Woo MN, Jeon SM, Kim HJ, Lee MK, Shin SK, Shin YC, Park

YB, Choi MS (2010) Fucoxanthin supplementation

improves plasma and hepatic metabolism and blood glu-

cose concentration in high-fat fed C57BL/6N mice. Chem

Biol Interact 186:316–322

442 Phytochem Rev (2011) 10:431–443

123

Xu G, Snellman E, Bykov VJ, Jansen CT, Hemminki K (2000)

Effect of age on the formation and repair of UV photo-

products in human skin situ. Mutat Res 459:195–202

Yamasaki M, Ogura K, Hashimoto W, Mikami B, Murata K

(2005) A structural basis for depolymerization of alginate

by polysaccharide lyase family-7. J Mol Biol 352:11–21

Yang L, Zhang LM (2009) Chemical structural and chain

conformational characterization of some bioactive poly-

saccharides isolated from natural sources. Carbohydr

Polym 76:349–361

Yoon NY, Eom TK, Kim MM, Kim SK (2009) Inhibitory

effect of phlorotannins isolated from E. cava on mush-

room tyrosinase activity and melanin formation in mouse

B16F10melanoma cells. J Agr Food Chem 57:4124–4129

Zvyagintseva TN, Shevchenko NM, Chizhov AO, Krupnova

TN, Sundukova EV, Isakov VV (2003) Water-soluble

polysaccharides of some far-eastern brown seaweeds.

Distribution, structure and their dependence on the devel-

opmental conditions. J Exp Mar Biol Ecol 294:1–13

Phytochem Rev (2011) 10:431–443 443

123