[advances in food and nutrition research] marine carbohydrates: fundamentals and applications, part...

CHAPTER ONE

Marine-Derived Polysaccharidesfor Regulation of AllergicResponsesThanh-Sang Vo*, Se-Kwon Kim*,†,1*Marine Bioprocess Research Center, Pukyong National University, Busan, South Korea†Department of Chemistry, Pukyong National University, Busan, South Korea1Corresponding author: e-mail address: [email protected]

Contents

1. Introduction 22. Marine Polysaccharides 3

2.1 Alginate 32.2 Porphyran 42.3 Fucoidans 42.4 Chitin and its derivatives 5

3. Pharmacological Properties of Marine Polysaccharides for Modulation of AllergicResponses 63.1 Alginic acid 63.2 Porphyran 73.3 Fucoidans 73.4 Chitin 83.5 Chitosan nanoparticles 93.6 Chitooligosaccharides 10

4. Conclusion 10References 11

Abstract

Polysaccharides are macromolecules made up of many monosaccharides joinedtogether by glycosidic bonds. Polysaccharides from marine sources are widely distrib-uted as the principle component in cell wall structures of seaweeds or exoskeletonsof crustaceans. So far, marine polysaccharides have been used in many fields of bio-materials, food, cosmetic, and pharmacology. Especially, numerous pharmaceuticalproperties of marine polysaccharides have been revealed such as antioxidant, anti-inflammatory, antiallergic, antitumor, antiobesity, antidiabetes, anticoagulant,antiviral, immunomodulatory, cardioprotective, antihepatopathy, antiuropathy, andantirenalpathy activities. Recently, several marine polysaccharides such alginate,porphyran, fucoidan, and chitin and its derivatives have been found as modulatorsof allergic responses due to enhancing innate immune system, altering Th1/Th2

Advances in Food and Nutrition Research, Volume 73 # 2014 Elsevier Inc.ISSN 1043-4526 All rights reserved.http://dx.doi.org/10.1016/B978-0-12-800268-1.00001-9

1

http://dx.doi.org/10.1016/B978-0-12-800268-1.00001-9

balance, inhibiting IgE production, and suppressing mast cell degranulation. This con-tribution, therefore, focuses specially on the immunomodulatory effect of marinepolysaccharides and emphasizes their potential application as candidates of pharma-ceuticals as well as nutraceuticals to prevent allergic disorders.

1. INTRODUCTION

Allergy is a disorder of the immune system due to an exaggerated reac-

tion of the immune system to harmless environmental substances, such as

animal dander, house dust mites, foods, pollen, insects, and chemical agents

(Milian & Dıaz, 2004). It can cause runny nose, sneezing, itching, rashes,

swelling, or asthma (Kay, 2000). It is noteworthy that the allergic diseases

are among the commonest causes of chronic ill-health. The prevalence,

severity, and complexity of these diseases are rapidly rising and considerably

adding to the burden of health-care costs (Kay, 2000). Substantially, allergic

reaction is characterized by the excessive activation of mast cells and baso-

phils by immunoglobulin E (IgE), resulting in an extreme inflammatory

response (Galli, Tsai, & Piliponsky, 2008). Acute allergic sensitization in

individuals is involved in the generation of allergen-specific CD4+ Th2 cells.

These cells secrete various cytokines, including IL-4, IL-5, IL-9, and IL-13,

as well as chemokines such as thymus, leading to further Th2 cell recruit-

ment and the production of allergen-specific IgE by B cells. Subsequently,

IgE circulates and binds surface receptors onmast cells and basophils. Further

exposure to allergen results in crosslinking of IgE on mast cells and basophils

causing cell degranulation, releasing histamine, proteases, chemokines, pros-

taglandins, leukotrienes, and a host of other mediators. This results in

bronchoconstriction and recruitment of activated eosinophils, neutrophils,

lymphocytes, and macrophages (Larche, 2007; Larche, Robinson, & Kay,

2003). These allergic cascades are considered as a source of molecular targets

for regulation of type I allergic reaction and management of allergic diseases.

Recently, the role of marine organisms-derived compounds as antiallergic

agents has been determined in vitro and in vivo by many researchers. Simul-

taneously, numerous marine compounds have been found to be efficient for

antiallergic therapeutics via modulation of Th1/Th2 balance, inhibition of

IgE production, and suppression of mast cell degranulation.

The world’s oceans, covering more than 70% of the earth’s surface, rep-

resent an enormous resource for the discovery of promising therapeutic

agents. Due to the unusual diversity of chemical structures, marine

2 Thanh-Sang Vo and Se-Kwon Kim

organisms have received much attention in screening marine natural prod-

ucts for their biomedical potential (Haefner, 2003; Molinski, Dalisay,

Lievens, & Saludes, 2009; Newman & Cragg, 2004). During the last

decades, marine organisms such as algae, tunicates, sponges, soft corals, bryo-

zoans, sea slugs, mollusks, echinoderms, fishes, microorganisms, etc., have

been subjected for isolation of numerous novel compounds. They have sig-

nificant amounts of lipid, protein, peptide, acid amine, polysaccharides,

chlorophyll, carotenoids, vitamins, minerals, and unique pigments (Blunt,

Copp, Munro, Northcote, & Prinsep, 2006; Faulkner, 2001, 2002). Nota-

bly, marine polysaccharides have been known as potential promising mate-

rials for a variety of uses in food, medicine, pharmaceutical, and nutraceutical

industries due to their biological properties and activities. This contribution,

therefore, focuses specially on the immunomodulatory effect of marine

polysaccharides and emphasizes their potential application as candidates of

pharmaceuticals as well as nutraceuticals to prevent allergic disorders.

2. MARINE POLYSACCHARIDES

Polysaccharides from marine sources offer diverse therapeutic func-

tions due to their biocompatible, biodegradable to harmless products, non-

toxic, and physiologically inert. Moreover, most of them are capable of

forming hydrogels because of their remarkable hydrophilicity, which helps

them to bind to proteins and other compounds. Several marine polysaccha-

rides such as alginate, porphyran, fucoidan, and chitin and its derivatives

have been found and extracted from various sources, especially seaweed

and crustacean. In recent years, numerous polysaccharides have been used

in many fields of biomaterials, food, cosmetic, and pharmacology.

2.1. AlginateAlginates are quite abundant in nature as structural component in marine

brown algae (Phaeophyceae) and as capsular polysaccharides in soil bacteria

(Laurienzo, 2010). The function of alginates in algae is primarily skeletal,

with the gel located in the cell wall and intercellular matrix conferring

the strength and flexibility necessary to withstand the force of water in which

the seaweed grows (D’Ayala, Malinconico, & Laurienzo, 2008). Alginate is a

linear, anionic block copolymer heteropolysaccharide consisting of β-D-mannuronic acid (M) and α-L-guluronic acid (G). The relative amount

and sequential distribution of homogeneous M–M segments (M-blocks),

homogeneous G–G segments (G-blocks), and alternating M–G segments

3Antiallergic Properties of Marine Polysaccharides

(MG-blocks), which represent the primary structure of alginate, depend on

the producing species, and for marine sources, on seasonal and geographical

variations (D’Ayala et al., 2008). Alginates may be prepared with a wide

range of average molecular weights (50–100,000 residues) to suit the appli-

cation. The process of the isolation of alginates from brown algae includes

the pre-extraction with hydrochloric acid, followed by washing, filtration,

and neutralization with alkali. Sodium alginate is precipitated from the solu-

tion by alcohol (isopropanol or ethanol) and usually reprecipitated in the

same way (Laurienzo, 2010). Over the last few years, medical and pharma-

ceutical industries have shown an increased interest in alginates due to effi-

cient treatment of esophageal reflux, creates multiquality calcium fibers for

dermatology, and wound healing. Alginate is an effective natural dis-

integrant, tablet binder and offers an attractive alternative for sustained-

release systems. It offers advantages over synthetic polymers as it forms

hydrogels under relatively mild pH and temperature and is generally reg-

arded as nontoxic, biocompatible, biodegradable, less expensive, and abun-

dantly available in nature. Accordingly, alginates are considered to be useful

materials for biomedical applications, especially for controlled delivery of

drugs and other biologically active compounds and for the encapsulation

of cells (D’Ayala et al., 2008).

2.2. PorphyranPorphyran is a sulfated polysaccharide isolated from seaweeds of order

Bangiales especially from the genera Porphyra. It is obtained from red algae

of KingdomRhodophyta. Chemically, porphyran is related to agarose, con-

sists of linear backbone of alternating 3-linked β-D-galactose and 4-linked

3,6-anhydro-α-L-galactose units. The L residues are mainly composed of

α-L-galactosyl 6-sulfate units, and the 3,6-anhydrogalactosyl units are minor.

Porphyran has been reported to possess various pharmaceutical properties

such as antioxidant, antitumor, immunostimulant, hypotensive, antifatigue,

antibacterial, anticoagulant, anticancer, antiviral, antihyperlipidemic, and

hepatoprotective activity (Bhatia et al., 2008).

2.3. FucoidansFucoidans are a complex series of sulfated polysaccharides found widely in

the cell walls of brown seaweeds. In recent years, different brown algae were

analyzed for their content of fucoidans. The low-molecular-weight fractions

of algal fucoidans (less than 30 kDa) obtained by depolymerization have


been shown to exhibit some heparin-like properties, with less side effects

(Karim et al., 2011). Such polysaccharides do not occur in other divisions

of algae and in land plants. However, the related biopolymers were found

in marine invertebrates such as sea cucumbers or sea urchins. These polysac-

charides are simpler than fucoidans derived frommarine brown algae and are

referred to as sulfated fucans. The seaweed fucoidans are heterogenic and

represent the mixtures of structurally related polysaccharides with certain

variations of the content of carbohydrate units and noncarbohydrate substit-

uents (Cumashi et al., 2007). Fucoidans are mainly composed of fucose and

sulfate. Besides, they also contain other monosaccharides (mannose, galac-

tose, glucose, xylose, etc.) and uronic acids, even acetyl groups and protein.

The fucoidans of most algae consist of sulfated L-fucose with major fucose

components. However, some fucoidans have minor fucose components and

major other monosaccharides like galactose or uronic acids (Vo & Kim,

2013). According to Cumashi et al. (2007), the polysaccharide backbones

in fucoidans are known as type I or type II chains. The type I chains are

found to contain the repeating (1!3)-linked α-L-fucopyranose residues,

whereas type II chains contain the alternating (1!3)- and (1!4)-linked

α-L-fucopyranose residues. During the last decades, numerous pharmaceu-

tical properties of fucoidans have been revealed due to their antioxidant,

anti-inflammatory, antiallergic, antitumor, antiobesity, antidiabetes, antico-

agulant, antiviral, antihepatopathy, antiuropathy, and antirenalpathy effects

(Vo &Kim, 2013). These special properties of fucoidans have supported it to

be applied to functional foods for disease prevention and health promotion.

2.4. Chitin and its derivativesChitin is a linear polysaccharide consisting of β-(1–4)-N-acetyl

D-glucosamine residues. It is widely distributed in nature and is the second

most abundant polysaccharide in nature after cellulose. It may be regarded as

cellulose with hydroxyl at position C-2 replaced by an acetamino group.

Chitin is a white, hard, inelastic, nitrogenous polysaccharide found in the

cell walls of bacteria and fungi, mushrooms, exoskeleton of crustaceans

and insects, the microfilarial sheath of parasitic nematodes, and the lining

of the digestive tracts of many insect. These organisms use chitin to protect

the invader from the harsh conditions inside the animal or plant host (Elias,

Homer, Hamid, & Lee, 2005). Chitin is highly hydrophobic and it insoluble

in water and most organic solvents. It exists mainly in two forms including

α-chitin and β-chitin. α-Chitin consists of sheets of tightly packed


alternating parallel and antiparallel chains (Minke & Blackwell, 1978).

Meanwhile, β-chitin is arranged in parallel (Gardner & Blackwell, 1975),

which occurs less frequently in nature than α-chitin. Being nontoxic and

environmentally safe, chitin has become of great interest not only as a

utilized resource but also a new functional biomaterial of high potential

in many fields such as medical, agricultural, and cosmetic applications. It

is readily obtained for commercial use from crustacean shell waste products

generated by the seafood industry (Kumar, 2000; Kurita, 2006). Chitosan, a

partially deacetylated polymer of N-acetylglucosamine, is produced com-

mercially by deacetylation of chitin (Dutta, Dutta, & Tripathi, 2004).

During the past decades, chitosan has received considerable attention

due to its biodegradable, nontoxic, and nonallergenic properties, which

made it possible to be used in many fields including food, cosmetics, bio-

medicine, agriculture, and environmental protection (Kim & Rajapaksea,

2005). Recent studies have focused on the conversion of chitosan to

chitooligosaccharides (COS) since COS are not only water soluble and

possess higher oral absorption but also have various biological effects,

including antimicrobial, antitumor, anticancer, antioxidant, anti-

inflammatory, and antiangiotensin-I-converting enzyme activities

(Kim & Rajapaksea, 2005). Especially, chitin and its derivatives have been

determined to be protective agents against allergic diseases.

3. PHARMACOLOGICAL PROPERTIES OF MARINEPOLYSACCHARIDES FOR MODULATION OF ALLERGICRESPONSES

3.1. Alginic acidAlginic acid, a naturally occurring hydrophilic colloidal polysaccharide

obtained from the several species of brown seaweeds, exhibited different

effects against hyaluronidase activity and histamine release from mast cells

(Asada et al., 1997). In the in vivo conditions, alginic acid inhibited com-

pound 48/80-induced systemic anaphylaxis with doses of 0.25–1 g/kg

and significantly inhibited passive cutaneous anaphylaxis by 54.8% at

1 g/kg for 1 h pretreatment ( Jeong et al., 2006). Besides, alginic acid was

found to have a maximum suppression rate (60.8%) on histamine release

from rat peritoneal mast cells at concentration of 0.01 μg/ml. Furthermore,

the antiallergic activities of alginic acid were also observed due to its suppres-

sive effects on activity and expression of histidine decarboxylase, production

of IL-1β and TNF-α, and protein level of nuclear factor (NF)-κB/Rel A in


PMA plus A23187-stimulated HMC-1 cells ( Jeong et al., 2006). Notice-

ably, alginic acid oligosaccharide (ALGO), a lyase lysate of alginic acid,

has been revealed to be able to reduce IgE production in the serum of

BALB/c mice immunized with β-lactoglobulin (Uno, Hattori, &

Yoshida, 2006; Yoshida, Hirano, Wada, Takahashi, & Hattori, 2004).

Moreover, antigen-induced Th2 development was blocked by ALGO treat-

ment via enhancing the production of IFN-γ and IL-12, and down-

regulating IL-4 production in splenocytes of mice (Yoshida et al., 2004).

3.2. PorphyranPorphyran, a sulfated polysaccharide isolated from red seaweeds, has been

recognized to be effective against different allergic responses. According to

Ishihara, Oyamada, Matsushima, Murata, and Muraoka (2005), porphyran

of red algae Porphyra tenera and P. yezoensiswere capable to inhibit the con-

tact hypersensitivity reaction induced by 2,4,6-trinitrochlorobenzene via

decreasing the serum level of IgE in Balb/c mice. Moreover, Yoshizawa

and colleagues have revealed that polysaccharide fractions from

P. yezoensis possessed the ability to activate macrophages in vitro and in vivo

via enhancing glucose consumption, the production of nitrite and tumor

necrosis factor (TNF), secretion of IL-1 from macrophages and carbon

clearance activity of phagocytes from mice injected intraperitoneally. It

has been indicated that porphyran is responsible for these effects and its sul-

fate group contributes to the macrophage stimulating activities (Yoshizawa

et al., 1995, Yoshizawa, Enomoto, Todoh, Ametani, & Kaminogawa,

1993). In addition, oral administration of porphyran from Porphyra

vietnamensis evoked a significant increase in weight of the thymus, spleen

and lymphoid organ cellularity, and total leucocyte and lymphocyte

(Bhatia et al., 2013).

3.3. FucoidansRecently, algal fucoidans have been found to be effective in suppression of

IgE and Th2 cytokine production in vitro and in vivo. Fucoidan fromUndaria

pinnatifida reduced the concentrations of both IL-4 and IL-13 in

bronchoalveolar lavage fluid (BALF) and inhibited the increase of

antigen-specific IgE in OVA-induced mouse airway hypersensitivity

(Maruyama, Tamauchi, Hashimoto, & Nakano, 2005). In the recent study,

Yanase et al. (2009) have reported that the peritoneal injection of fucoidan

caused an alleviative effect of plasma IgE level by suppressing a number of


IgE-expressing and IgE-secreting B cells fromOVA-sensitized mice. On the

other hand, the inhibitory effect of fucoidan on IgE production was deter-

mined due to preventing Cε germline transcription and NF-κB p52 trans-

location in B cells (Oomizu, Yanase, Suzuki, Kameyoshi, & Hide, 2006).

Yet, the inhibitory activity of fucoidan has been not observed if B cells were

prestimulated with IL-4 and anti-CD40 antibody before the administration

of fucoidan. Thus, it suggested that fucoidan may not prevent a further

increase of IgE in patients who have already developed allergic diseases

and high levels of serum IgE. However, Iwamoto et al. (2011) have recently

determined that fucoidan effectively reduced IgE production in both

peripheral blood mononuclear cells from atopic dermatitis patients and

healthy donors. These findings indicated that fucoidan suppresses IgE pro-

duction by inhibiting immunoglobulin class-switching to IgE in human

B cells, even after the onset of atopic dermatitis.

3.4. ChitinChitin has been evidenced as a potent innate immune stimulator of macro-

phages and other innate immune cells, and thus chitin is able to suppress

allergen-induced type 2 allergic responses. Indeed, Shibata and colleagues

have determined the immunological effects of chitin in vivo and in vitro using

phagocytosable small-sized chitin particles. It has shown that intravenous

administration of fractionated chitin particles into the lung activated alveolar

macrophages to express cytokines such as IL-12, TNF-α, and IL-18, leadingto INF-γ production mainly by NK cells (Shibata, Foster, Metzger, &

Myrvik, 1997). The production of cytokines induced by chitin is identified

to be mediated by a mannose receptor (Shibata, Metzger, & Myrvik, 1997).

In another study, Lee and colleagues have determined that chitin stimulates

macrophages by interacting with different cell surface receptors such as mac-

rophage mannose receptor, toll-like receptor-2, C-type lectin receptor

Dectin-1, and leukotriene 134 receptor (BLT1) (Lee, 2009). These studies

have shown the direct interactions between chitin and its cell surface recep-

tors and thus chitin regulates the specific signaling pathways in immune

responses.

In the further study of Shibata and colleagues, the suppressive effect of

Th2 responses has been confirmed when chitin was given orally in BALB/c

and C57BL/6 mice (Shibata, Foster, Bradfield, & Myrvik, 2000). It was

observed that chitin treatment resulted in decreases of serum IgE levels

and lung eosinophil numbers in both strains. The inhibitory mechanisms


of Th2 responses by chitin was found due to decreases of Th2 cytokines

including IL-4, IL-5, and IL-10 levels and the production of Th1 cytokine

IFN-gamma in spleen cells isolated from the ragweed-immunized mice.

These results indicated that the immune responses were redirected toward

a Th1 response by chitin treatment, and thus downregulating Th2-facilitated

IgE production and lung eosinophilia in the allergic mouse. Moreover, the

Th1 adjuvant role of chitin has been determined via upregulating Th1

immunity induced by heat-killed Mycobacterium bovis and downregulating

Th2 immunity induced by mycobacterial protein (Shibata et al., 2001).

Likewise, Hamajima et al. (2003) has also reported the Th1 adjuvant effect

of chitin microparticles in inducing viral specific immunity.

Notably, the effectiveness of chitin microparticles when given intrana-

sally as a treatment for the symptoms of respiratory allergy and allergy asthma

has been tested in two different mouse models of allergy, namely to

Dermatophagoids pteronyssinus and Aspergillus fumigates (Strong, Clark, &

Reid, 2002). The intranasal application of microgram doses of chitin micro-

particles substantially reduced the allergen-induced serum IgE levels,

peripheral eosinophilia, airway hyperresponsiveness, and lung inflammation

in both allergy models. This effectiveness was found due to the increase

in Th1 cytokines IL-12, IFN-γ, and TNF-α and decrease in IL-4 produc-

tion during allergen challenge. The immunostimulatory properties of chitin

microparticles could offer a novel and natural approach to treating allergic

disease in humans.

3.5. Chitosan nanoparticlesIn the most recent study, chitosan nanoparticles have been determined as an

adjuvant agent via promoting immune response in ovalbumin (OVA)-

challenged mice (Wen, Xu, Zou, & Xu, 2011). Mice were immunized sub-

cutaneously with 25 μg OVA alone or with 25 μg OVA dissolved in saline

containing Quil A (10 μg), chitosan (50 μg), or chitosan nanoparticles (12.5,50, or 200 μg) on days 1 and 15. It was found that the serum OVA-specific

IgG, IgG1, IgG2a, and IgG2b antibody titers and Con A-, LPS-, and OVA-

induced splenocyte proliferation were significantly enhanced by chitosan

nanoparticles as compared with OVA and chitosan groups. Notably,

chitosan nanoparticles also significantly promoted the production of IL-2

and IFN-γ cytokines and upregulated the mRNA expression of IL-2,

IFN-γ cytokines in splenocytes from the immunized mice compared with

OVA and chitosan groups. Besides, chitosan nanoparticles remarkably


increased the killing activities of NK cells activity. The results suggested that

chitosan nanoparticles had a strong potential to increase both cellular and

humoral immune responses.

3.6. ChitooligosaccharidesIn the regard of COS on in vitro allergic responses, Vo, Kong, and Kim

(2011) and Vo, Kim, Ngo, Kong, and Kim (2012) have investigated the

inhibitory effect of COS on mast cell activation induced by calcium

ionophore A23187 or antigen. The pretreatment of COS causes signifi-

cant inhibition on mast cell degranulation via reducing histamine and

β-hexosaminidase release and intracellular Ca2+ elevation in RBL-2H3

mast cells. Moreover, the inhibitory effects of COS on expression as well

as production of various cytokines such as TNF-α, IL-1β, IL-4, and IL-6

were also evidenced. Notably, the protective effect of COS (<1 kDa)

against OVA-induced lung inflammation in asthma model mice was also

examined (Chung, Park, & Park, 2012). Oral administration of COS

(16 mg/kg body weight/day) resulted in a significant reduction in both

mRNA and protein levels of interleukin IL-4, IL-5, IL-13, and TNF-αin the lung tissue and BALF. The protein levels of IL-4, IL-13, and

TNF-α in BALF were decreased by 5.8-fold, 3.0-fold, and 9.9-fold,

respectively, compared to those in the OVA-sensitized/challenged asthma

control group. Collectively, these results indicate that COS can contribute

to attenuation of allergic reactions and might be a promising candidate for

novel inhibitor of allergic reaction.

4. CONCLUSION

Marine polysaccharides are considered as promising biomaterials that

are the focus of biomedical research today. Notably, many experimental

results clearly indicated that marine polysaccharides such as alginate,

porphyran, fucoidan, and chitin and its derivatives are exciting agents for

modulation of allergic responses via enhance of innate immune system, reg-

ulation of Th1/Th2 balance toward Th1 dominance, decrease in IgE pro-

duction, and inhibition of mast cell degranulation. Accordingly, marine

polysaccharides can be used as safety and efficacy biomaterials for the devel-

opment of food, pharmaceutical, and nutraceutical industries in prevention

and/or treatment of allergic disorders. The possibility of producing a variety

of chemically modified derivatives makes these polysaccharides versatile bio-

materials in almost all fields of biomedical interest.


REFERENCESAsada, M., Sugie, M., Inoue, M., Nakagomi, K., Hongo, S., Murata, K., et al. (1997). Inhib-

itory effect of alginic acids on hyaluronidase and on histamine release from mast cells.Bioscience Biotechnology and Biochemistry, 61, 1030–1032.

Bhatia, S., Rathee, P., Sharma, K., Chaugule, B. B., Kar, N., & Bera, T. (2013). Immuno-modulation effect of sulphated polysaccharide (porphyran) from Porphyra vietnamensis.International Journal of Biological Macromolecules, 57, 50–56.

Bhatia, S., Sharma, A., Sharma, K., Kavale, M., Chaugule, B. B., Dhalwal, K., et al. (2008).Novel algal polysaccharides from marine source: Porphyran. Pharmacognosy Reviews, 2,271–276.

Blunt, J. W., Copp, B. R., Munro, M. H. G., Northcote, P. T., & Prinsep, M. R. (2006).Marine natural products. Natural Product Reports, 23, 26–78.

Chung, M. J., Park, J. K., & Park, Y. I. (2012). Anti-inflammatory effects of low-molecularweight chitosan oligosaccharides in IgE-antigen complex-stimulated RBL-2H3 cells andasthma model mice. International Immunopharmacology, 12, 453–459.

Cumashi, A., Ushakova, N. A., Preobrazhenskaya, M. E., D’Incecco, A., Piccoli, A.,Totani, L., et al. (2007). A comparative study of the anti-inflammatory, anticoagulant,antiangiogenic, and antiadhesive activities of nine different fucoidans from brown sea-weeds. Glycobiology, 17, 541–552.

D’Ayala, G. G., Malinconico, M., & Laurienzo, P. (2008). Marine derived polysaccharidesfor biomedical applications: chemical modification approaches. Molecules, 13,2069–2106.

Dutta, P. K., Dutta, J., & Tripathi, V. S. (2004). Chitin and chitosan: Chemistry, propertiesand applications. Journal of Scientific and Industrial Research, 63, 20–31.

Elias, J. A., Homer, R. J., Hamid, Q., & Lee, C. G. (2005). Chitinases and chitinase-likeproteins in T(H)2 inflammation and asthma. Journal of Allergy and Clinical Immunology,116, 497–500.

Faulkner, D. J. (2001). Marine natural products. Natural Product Reports, 18, 1–49.Faulkner, D. J. (2002). Marine natural products. Natural Product Reports, 19, 1–48.Galli, S. J., Tsai, M., & Piliponsky, A. M. (2008). The development of allergic inflammation.

Nature, 454, 445–454.Gardner, K. H., & Blackwell, J. (1975). Refinement of structure of beta-chitin. Biopolymers,

14, 1581–1595.Haefner, B. (2003). Drugs from the deep: Marine natural products as drug candidates. Drug

Discovery Today, 8, 536–544.Hamajima, K., Kojima, Y., Matsui, K., Toda, Y., Jounai, N., Ozaki, T., et al. (2003). Chitin

micro-particles: A useful adjuvant for inducing viral specific immunity when deliveredintranasally with an HIV-DNA vaccine. Viral Immunology, 16, 541–547.

Ishihara, K., Oyamada, C., Matsushima, R., Murata, M., & Muraoka, T. (2005). Inhibitoryeffect of porphyran, prepared from dried Nori, on contact hypersensitivity in mice. Bio-science Biotechnology and Biochemistry, 69, 1824–1830.

Iwamoto, K., Hiragun, T., Takahagi, S., Yanase, Y., Morioke, S., Mihara, S., et al. (2011).Fucoidan suppresses IgE production in peripheral blood mononuclear cells from patientswith atopic dermatitis. Archives of Dermatology Research, 303, 425–431.

Jeong, H. J., Lee, S. A., Moon, P. D., Na, H. J., Park, R. K., Um, J. Y., et al. (2006). Alginicacid has anti-anaphylactic effects and inhibits inflammatory cytokine expression via sup-pression of nuclear factor-kappaB activation. Clinical and Experimental Allergy, 36,785–794.

Karim, S., Jessica, P., Farida, G., Christine, D., Corinne, S., Jacqueline, R., et al. (2011).Marine polysaccharides: A source of bioactive molecules for cell therapy and tissue engi-neering. Marine Drugs, 9, 1664–1681.

Kay, A. B. (2000). Overview of ‘Allergy and allergic diseases: With a view in the future’.British Medical Bulletin, 56, 843–864.


http://refhub.elsevier.com/B978-0-12-800268-1.00001-9/rf0005




















































Kim, S. K., & Rajapaksea, N. (2005). Enzymatic production and biological activities ofchitosan oligosaccharides (COS): A review. Carbohydrate Polymers, 62, 357–368.

Kumar, M. N. V. R. (2000). A review of chitin and chitosan applications. Reactive and Func-tional Polymers, 46, 1–27.

Kurita, K. (2006). Chitin and chitosan: Functional biopolymers from marine crustaceans.Marine Biotechnology, 8, 203–226.

Larche, M. (2007). Regulatory T cells in allergy and asthma. Chest, 132, 1007–1014.Larche, M., Robinson, D. S., & Kay, A. B. (2003). The role of T lymphocytes in the path-

ogenesis of asthma. Journal of Allergy and Clinical Immunology, 111, 450–463.Laurienzo, P. (2010). Marine polysaccharides in pharmaceutical applications: An overview.

Marine Drugs, 8, 2435–2465.Lee, C. G. (2009). Chitin, chitinases and chitinase-like proteins in allergic inflammation and

tissue remodeling. Yonsei Medical Journal, 50, 22–30.Maruyama, H., Tamauchi, H., Hashimoto, M., & Nakano, T. (2005). Suppression of Th2

immune responses by Mekabu fucoidan from Undaria pinnatifida Sporophylls. Interna-tional Archives of Allergy and Immunology, 137, 289–294.

Milian, E., & Dıaz, A. M. (2004). Allergy to house dust mites and asthma. Puerto Rico HealthSciences Journal, 23, 47–57.

Minke, R., & Blackwell, J. (1978). The structure of alpha-chitin. Journal Molecular Biology,120, 167–181.

Molinski, T. F., Dalisay, D. S., Lievens, S. L., & Saludes, J. P. (2009). Drug developmentfrom marine natural products. Natural Reviews Drug Discovery, 8, 69–85.

Newman, D. J., & Cragg, G. M. (2004). Marine natural products and related compounds inclinical and advanced preclinical trials. Journal of Natural Products, 67, 1216–1238.

Oomizu, S., Yanase, Y., Suzuki, H., Kameyoshi, Y., & Hide, M. (2006). Fucoidan preventsCε germline transcription and NF-κB p52 translocation for IgE production in B cells.Biochemical Biophysical Research Communications, 350, 501–507.

Shibata, Y., Foster, L. A., Bradfield, J. F., & Myrvik, Q. N. (2000). Oral administration ofchitin down-regulates serum IgE levels and lung eosinophilia in the allergic mouse. TheJournal of Immunology, 164, 1314–1321.

Shibata, Y., Foster, L. A., Metzger, W. J., & Myrvik, Q. N. (1997). Alveolar macrophagepriming by intravenous administration of chitin particles, polymers of N-acetyl-D-glucosamine, in mice. Infection & Immunity, 65, 1734–1741.

Shibata, Y., Honda, I., Justice, J. P., Van Scott, M. R., Nakamura, R. M., & Myrvik, Q. N.(2001). Th1 adjuvant N-acetyl-D-glucosamine polymer up-regulates Th1 immunity butdown-regulates Th2 immunity against a mycobacterial protein (MPB-59) in interleukin-10-knockout and wild-type mice. Infection & Immunity, 69, 6123–6130.

Shibata, Y., Metzger, W. J., & Myrvik, Q. N. (1997). Chitin particle-induced cell-mediatedimmunity is inhibited by soluble mannan: Mannose receptor-mediated phagocytosis ini-tiates IL-12 production. The Journal of Immunology, 159, 2462–2467.

Strong, P., Clark, H., & Reid, K. (2002). Intranasal application of chitin microparticlesdown-regulates symptoms of allergic hypersensitivity to Dermatophagoides pteronyssinusand Aspergillus fumigatus in murine models of allergy. Clinical & Experimental Allergy,32, 1794–1800.

Uno, T., Hattori, M., & Yoshida, T. (2006). Oral administration of alginic acid oligosaccha-ride suppresses IgE production and inhibits the induction of oral tolerance. Bioscience Bio-technology and Biochemistry, 70, 3054–3057.

Vo, T. S., & Kim, S. K. (2013). Fucoidans as a natural bioactive ingredient for functionalfoods. Journal of Functional Foods, 5, 16–27.

Vo, T. S., Kim, J. A., Ngo, D. H., Kong, C. S., & Kim, S. K. (2012). Protective effect ofchitosan oligosaccharides against FcεRI-mediated RBL-2H3 mast cell activation. ProcessBiochemistry, 47, 327–330.

























































Vo, T. S., Kong, C. S., & Kim, S. K. (2011). Inhibitory effects of chitooligosaccharides ondegranulation and cytokine generation in rat basophilic leukemia RBL-2H3 cells.Carbohydrate Polymers, 84, 649–655.

Wen, Z. S., Xu, Y. L., Zou, X. T., & Xu, Z. R. (2011). Chitosan nanoparticles act as anadjuvant to promote both Th1 and Th2 immune responses induced by ovalbumin inmice. Marine Drugs, 9, 1038–1055.

Yanase, Y., Hiragun, T., Uchida, K., Ishii, K., Oomizu, S., Suzuki, H., et al. (2009). Peri-toneal injection of fucoidan suppresses the increase of plasma IgE induced by OVA- sen-sitization. Biochemical Biophysical Research Communications, 387, 435–439.

Yoshida, T., Hirano, A., Wada, H., Takahashi, K., & Hattori, M. (2004). Alginic acid oli-gosaccharide suppresses Th2 development and IgE production by inducing IL-12 pro-duction. International Archives of Allergy and Immunology, 133, 239–247.

Yoshizawa, Y., Ametani, A., Tsunehiro, J., Nomura, K., Itoh, M., Fukui, F., et al. (1995).Macrophage stimulation activity of the polysaccharide fraction from a marine alga(Porphyra yezoensis): Structure-function relationships and improved solubility. BioscienceBiotechnology and Biochemistry, 59, 1933–1937.

Yoshizawa, Y., Enomoto, A., Todoh, H., Ametani, A., & Kaminogawa, S. (1993). Activa-tion of murine macrophages by polysaccharide fractions from marine algae (Porphyrayezoensis). Bioscience Biotechnology and Biochemistry, 57, 1862–1866.





















[advances in food and nutrition research] marine carbohydrates: fundamentals and applications, part...

Documents