Characterization and Comparison of the Structural Features, Immune-Modulatory and Anti-Avian Influenza Virus Activities Conferred by Three Algal Sulfated Polysaccharides
"> Figure 1
<p>FT-IR spectra of three extracted sulfated polysaccharides. GFP, <span class="html-italic">Grateloupia filicina</span>; UPP, <span class="html-italic">Ulva Pertusa</span>; SQP, <span class="html-italic">Sargassum qingdaoens</span>.</p> "> Figure 2
<p>Mouse spleen cell proliferation effects of GFP, UPP and SQP. Mock treated with PBS instead of polysaccharides as a negative control. Values with different letters in the same column (a–d) are significantly different (<span class="html-italic">p</span> < 0.05) from each other. Data are shown as the Mean + SD and are fully representative of the individual experiment.</p> "> Figure 3
<p>Avian influenza virus (AIV)-specific antibody titer detection. Kunming mice were immunized with an AIV vaccine and polysaccharides, following the prime-boost vaccination programme (days 0 and 14), respectively. (<b>A</b>) GFP; (<b>B</b>) UPP; (<b>C</b>) SQP. Values with different letters in the same column (a–d) are significantly different (<span class="html-italic">p</span> < 0.05) from each other. Data are shown as the Mean + SD and are fully representative of an individual experiment.</p> "> Figure 4
<p>Cytokine production stimulating effect of GFP, UPP and SQP. Kunming mice were immunized with an AIV vaccine and polysaccharides, and sera were collected on day 28 after two immunizations to detect the cytokines IFN-γ (<b>A</b>) and IL-4 (<b>B</b>). Values with different letters in the same column (a–d) are significantly different (<span class="html-italic">p</span> < 0.05) from each other. Data are shown as the Mean + SD and are fully representative for the individual experiment.</p> "> Figure 5
<p>T-cell subpopulation tests. The blood cells of the treated mice were collected and analyzed with flow cytometry. (<b>A</b>) CD3+CD4+. (<b>B</b>) CD3+CD8+. Values with different letters in the same column (a–d) are significantly different (<span class="html-italic">p</span> < 0.05) from each other. Data are shown as the Mean + SD and are fully representative of the individual experiment.</p> "> Figure 6
<p>Haemagglutination test (HA) of the cell culture and relative expression of H9N2. Antiviral activity <span class="html-italic">in vitro</span> was measured with a HA test (<b>A</b>) and RT-PCR (<b>B</b>). Data from samples without polysaccharides were used as a basic control. Values with different letters in the same column (a–c) are significantly different (<span class="html-italic">p</span> < 0.05) from each other. Data are shown as the Mean + SD and are fully representative of the individual experiment.</p> ">
Abstract
:1. Introduction
Author | Phylum | Species | Bioactivities |
---|---|---|---|
Qi, et al., 2005 [14] | Chlorophyta | Ulva pertusa | Antioxidant activity |
Zhang et al., 2010 [2] | Ulva pertusa | Antioxidant activity | |
Enteromorpha linza | |||
Bryopsis plumose | |||
Cho et al., 2010 [15] | Enteromorpha prolifera | Antitumor and immunomodulating activities | |
Jiao et al., 2010 [16] | Enteromorpha intestinalis | Antitumor and immunomodulating activities | |
Tabarsa et al., 2012 [17] | Ulva pertusa | Immunomodulatory, anticancer activities | |
Zhang et al., 2013 [18] | Enteromorpha linza | Immunological and antioxidant activities | |
Aguilar-Briseño et al., 2015 [19] | Ulva clathrata | Antiviral activity | |
Zhang et al., 2010 [2] | Ochrophyta | Laminaria japonica | Antioxidant activity |
Ye et al., 2008 [20] | Sargassum pallidum | Antitumor and antioxidant activities | |
Wang et al., 2011 [21] | Laminaria japonica | Anticoagulant activity | |
Li et al., 2012 [22] | Sargassum pallidum | Immune responses | |
Dore et al., 2013 [10] | Sargassum vulgare | Anticoagulant, antithrombotic, antioxidant and anti-inflammatory effects | |
Suresh et al., 2013 [23] | Sargassum plagiophyllum | Anticancer and antioxidant activities | |
Imbs et al., 2014 [24] | Fucus evanescens | Antioxidant activity | |
Hwang et al., 2015 [25] | Sargassum hemiphyllum | Anti-inflammatory | |
Wen et al., 2014 [26] | Sargassum horneri | Antioxidant activity | |
Shao et al., 2014 [27] | Sargassum horneri | Antioxidant and antitumor activities | |
Shobharani et al., 2014 [28] | Sargassum sp. | Antioxidant and anticoagulant activities | |
Aguilar-Briseño et al., 2015 [19] | Cladosiphon okamuranus | Antiviral activity | |
Zhang et al., 2014 [29] | Ascophyllum nodosum | Induces Th1 and Tc1 Immune Responses | |
Yuan et al., 2015 [30] | Ascophyllum nodosum | Antioxidant activity | |
Ammar et al., 2015 [31] | Cystoseira sedoides, | Anti-radical, anti-inflammatory and gastroprotective activities | |
Cystoseira compressa, | |||
Cystoseira crinita | |||
Shao et al., 2015 [32] | Sargassum horneri | Antioxidant and moisture-preserving activities | |
Athukorala et al., 2005 [33] | Rhodophyta | Grateloupia filicina | Antioxidant activity, protecting ability for H2O2-induced DNA damage |
Wang et al., 2007 [34] | Grateloupia longifolia | Anti-virus activity | |
Grateloupia filicina | |||
Zhang et al., 2010 [2] | Porphyra haitanensis | Antioxidant activity | |
Yu et al., 2012 [35] | Eucheuma denticulatum | Anti-virus activity | |
Shi et al., 2014 [36] | Porphyra haitanensis | Anti-allergic activity | |
Chen et al., 2015 [37] | Grateloupia filicina | Anticoagulant activity | |
Fleita et al., 2015 [38] | Pterocladia capillacea | Antioxidant activity |
2. Results
2.1. Chemical Characterization of Three Sulfated Polysaccharides
2.1.1. Chemical Analysis
Sample | Yield (%) | Total Sugar (%) | Sulfate (%) | Monosaccharides Composition (Molar Ratio) | ||||||
---|---|---|---|---|---|---|---|---|---|---|
Man | Rha | Glc A | Glc | Gal | Xyl | Fuc | ||||
UPP | 12.1 | 53.13 | 13.54 | 0.06 | 1 | 0.53 | 0.19 | 0.09 | 0.39 | 0.02 |
GFP | 19.7 | 40.9 | 19.89 | 0.01 | - | 0.02 | 0.07 | 1 | 0.1 | 0.05 |
SQP | 7.2 | 20.81 | 5.64 | 0.56 | - | 0.13 | 0.37 | 0.6 | - | 1 |
2.1.2. FT-IR Spectrometric Characterization
2.2. Cytotoxic Activity of the Polysaccharides
2.3. Immunologic Modulation of Three Sulfated Polysaccharides in Vitro
2.4. Immune-Modulation of Three Sulfated Polysaccharides in Vivo
2.4.1. H9N2-Specific Antibody Titer
2.4.2. Effect on Cytokine Production Stimulation
2.4.3. T-Cell Subpopulation
2.5. Anti-H9N2 Effect of Three Sulfated Polysaccharides in Vitro
3. Discussion
4. Materials and Methods
4.1. Algal Samples
4.2. Extraction of Water-Soluble Sulfated Algal Polysaccharide
4.3. Chemical Characterization
4.4. Animals and Maintenance
4.5. Cell Lines, Virus, and Tissue Culture
4.6. Cytotoxic Activity Evaluation
4.7. Immuno-Modulatory Effect
4.7.1. Mouse Splenic Lymphocyte Proliferation Assay
4.7.2. Animals Grouping and Treatment
4.7.3 AIV-Specific Antibody Titer Detection
4.7.4. Cytokines Production
4.7.5. T-Cell Subpopulation and Flow Cytometry
4.8. Anti-AIV Effect in Vitro
4.8.1. Virus Titers Assay
4.8.2. Relative Expression of Viruses
4.9. Statistical Analysis
5. Conclusions
Acknowledgments
Author Contributions
Conflicts of Interest
Appendix
Conc (mg/mL) | 10 | 5 | 2.5 | 1.25 | 0.625 | 0.3125 | 0.156 | 0.078 |
---|---|---|---|---|---|---|---|---|
UPP | 0.82 | 1.03 | 1.16 | 1.09 | 1.05 | 1.08 | 1.06 | 1.02 |
GFP | 0.74 | 0.81 | 0.89 | 0.9 | 0.95 | 0.92 | 1.01 | 1.13 |
SQP | 0.78 | 0.96 | 1.01 | 1 | 0.97 | 1.05 | 0.99 | 1.03 |
References
- Bohn, J.A.; Bemiller, J.N. (1→3)-β-d-Glucans as Biological Response Modifiers: A Review of Structure-Functional Activity Relationships. Carbohydr. Polym. 1995, 28, 3–14. [Google Scholar] [CrossRef]
- Zhang, Z.; Wang, F.; Wang, X.; Liu, X.; Hou, Y.; Zhang, Q. Extraction of the Polysaccharides from Five Algae and Their Potential Antioxidant Activity in vitro. Carbohydr. Polym. 2010, 82, 118–121. [Google Scholar] [CrossRef]
- Nikapitiya, C.; De Zoysa, Mahanama; Jeon, Y.-J.; Lee, J.; Jee, Y.H. Isolation of Sulfated Anticoagulant Compound from Fermented Red Seaweed Grateloupia Filicina. J. World Aquac. Soc. 2007, 38, 407–417. [Google Scholar] [CrossRef]
- Genovese, G.; Faggio, C.; Gugliandolo, C.; Torre, A.; Spanò, A.; Morabito, M.; Maugeri, T.L. In vitro Evaluation of Antibacterial Activity of Asparagopsis Taxiformis from the Straits of Messina Against Pathogens Relevant in Aquaculture. Mar. Environ. Res. 2012, 73, 1–6. [Google Scholar] [CrossRef] [PubMed]
- Bordbar, S.; Saari, F.A.N. High-value Components and Bioactives from Sea Cucumbers for Functional Foods—A Review. Mar. Drugs 2011, 9, 1761–1805. [Google Scholar] [CrossRef] [PubMed]
- Pomin, V.H. Fucanomics and Galactanomics: Marine Distribution, Medicinal Impact, Conceptions, and Challenges. Mar. Drugs 2012, 10, 793–811. [Google Scholar] [CrossRef] [PubMed]
- Faggio, C.; Morabito, M.; Minicante, S.A.; Piano, G.L.; Pagano, M.; Genovese, G. Potential Use of Polysaccharides from the Brown Alga Undaria Pinnatifida as Anticoagulants. Braz. Arch. Biol. Technol. 2015, 58. [Google Scholar] [CrossRef]
- Wang, L.; Wang, X.; Wu, H.; Liu, R. Overview on Biological Activities and Molecular Characteristics of Sulfated Polysaccharides from Marine Green Algae in Recent Years. Mar. Drugs 2014, 12, 4984–5020. [Google Scholar] [CrossRef] [PubMed]
- Qi, X.; Mao, W.; Gao, Y.; Chen, Y.; Chen, Y.; Zhao, C.; Li, N.; Wang, C.; Yan, M.; Lin, C. Chemical Characteristic of an Anticoagulant-Active Sulfated Polysaccharide from Enteromorpha Clathrata. Carbohydr. Polym. 2012, 90, 1804–1810. [Google Scholar] [CrossRef] [PubMed]
- Dore, C.M.; das, C.F.A.M.G.; Will, L.S.; Costa, T.G.; Sabry, D.A.; de Souza Rego, L.A.; Accardo, C.M.; Rocha, H.A.; Filgueira, L.G.; Leite, E.L. A Sulfated Polysaccharide, Fucans, Isolated from Brown Algae Sargassum Vulgare with Anticoagulant, Antithrombotic, Antioxidant and Anti-Inflammatory Effects. Carbohydr. Polym. 2013, 91, 467–475. [Google Scholar] [CrossRef] [PubMed]
- Seo, Y.; Kang, S.H.; Lee, H.J.; You, A.K.; Youn, H.J.; Lee, B.J.; Chung, H. In vitro Screening of Seaweed Extract on the Proliferation of Mouse Spleen and Thymus Cell. Biotechnol. Bioprocess Eng. 2006, 11, 160–163. [Google Scholar] [CrossRef]
- Ping, S.; Jia, L.; Chen, X.; Fang, Z.; Sun, P. Structural Features and Antitumor Activity of a Purified Polysaccharide Extracted from Sargassum Horneri. Int. J. Biol. Macromol. 2015, 73, 124–130. [Google Scholar]
- Murad, H.; Ghannam, A.; Al-Ktaifani, M.; Abbas, A.; Hawat, M. Algal Sulfated Carrageenan Inhibits Proliferation of Mda-Mb-231 Cells via Apoptosis Regulatory Genes. Mol. Med. Rep. 2015, 11, 2153–2158. [Google Scholar] [CrossRef] [PubMed]
- Qi, H.; Zhang, Q.; Zhao, T.; Rong, C.; Hong, Z.; Niu, X.; Li, Z. Antioxidant Activity of Different Sulfate Content Derivatives of Polysaccharide Extracted from Ulva Pertusa (Chlorophyta) in vitro. Int. J. Biol. Macromol. 2005, 37, 195–199. [Google Scholar] [CrossRef] [PubMed]
- Cho, M.L.; Yang, C.; Sang, M.K.; You, S.G. Molecular Characterization and Biological Activities of Water-Soluble Sulfated Polysaccharides from Enteromorpha Prolifera. Food Sci. Biotechnol. 2010, 19, 525–533. [Google Scholar] [CrossRef]
- Jiao, L.; Xia, L.; Li, T.; Peng, J.; Zhang, L.; Wu, M.; Zhang, L. Characterization and Anti-Tumor Activity of Alkali-Extracted Polysaccharide from Enteromorpha Intestinalis. Int. Immunopharmacol. 2009, 9, 324–329. [Google Scholar] [CrossRef] [PubMed]
- Tabarsa, M.; Han, J.H.; Kim, C.Y.; You, S.G. Molecular Characteristics and Immunomodulatory Activities of Water-Soluble Sulfated Polysaccharides from Ulva Pertusa. J. Med. Food 2012, 15, 135–144. [Google Scholar] [CrossRef] [PubMed]
- Zhang, Z.; Wang, X.; Zhao, M.; Yu, S.; Qi, H. The Immunological and Antioxidant Activities of Polysaccharides Extracted from Enteromorpha Linza. Int. J. Biol. Macromol. 2013, 57, 45–49. [Google Scholar] [CrossRef] [PubMed]
- Aguilar-Briseño, J.A.; Cruz-Suarez, L.E.; Sassi, J.-F.; Ricque-Marie, D.; Zapata-Benavides, P.; Mendoza-Gamboa, E.; Rodríguez-Padilla, C.; Trejo-Avila, L.M. Sulphated Polysaccharides from Ulva Clathrata and Cladosiphon Okamuranus Seaweeds both Inhibit Viral Attachment/Entry and Cell-Cell Fusion, in NDV Infection. Mar. Drugs 2015, 13, 697–712. [Google Scholar] [CrossRef] [PubMed]
- Ye, H.; Wang, K.; Zhou, C.; Liu, J.; Zeng, X. Purification, Antitumor and Antioxidant Activities in vitro of Polysaccharides from the Brown Seaweed Sargassum Pallidum. Food Chem. 2008, 111, 428–432. [Google Scholar] [CrossRef] [PubMed]
- Wang, J.; Zhang, Q.B.; Zhang, Z.S.; Hou, Y.; Zhang, H. In-vitro Anticoagulant Activity of Fucoidan Derivatives from Brown Seaweed Laminaria Japonica. Chin. J. Oceanol. Limn. 2011, 29, 679–685. [Google Scholar] [CrossRef]
- Li, L.J.; Li, M.Y.; Li, Y.T.; Feng, J.J.; Hao, F.Q.; Lun, Z. Adjuvant Activity of Sargassum Pallidum Polysaccharides Against Combined Newcastle Disease, Infectious Bronchitis and Avian Influenza Inactivated Vaccines. Mar. Drugs 2012, 10, 2648–2660. [Google Scholar] [CrossRef] [PubMed]
- Suresh, V.; Senthilkumar, N.; Thangam, R.; Rajkumar, M.; Anbazhagan, C.; Rengasamy, R.; Gunasekaran, P.; Kannan, S.; Palani, P. Separation, Purification and Preliminary Characterization of Sulfated Polysaccharides from Sargassum Plagiophyllum and its in vitro Anticancer and Antioxidant Activity. Process Biochem. 2013, 48, 364–373. [Google Scholar] [CrossRef]
- Imbs, T.I.; Skriptsova, A.V.; Zvyagintseva, T.N. Antioxidant Activity of Fucose-Containing Sulfated Polysaccharides Obtained from Fucus Evanescens by Different Extraction Methods. J. Appl. Phycol. 2014, 27, 1–9. [Google Scholar] [CrossRef]
- Hwang, P.A.; Hung, Y.L.; Chien, S.Y. Inhibitory Activity of Sargassum Hemiphyllum Sulfated Polysaccharide in Arachidonic Acid-Induced Animal Models of Inflammation. J. Food Drug Anal. 2015, 23, 49–56. [Google Scholar] [CrossRef]
- Wen, Z.S.; Liu, L.J.; Ouyang, X.K.; Qu, Y.L.; Yin, C.; Ding, G.F. Protective Effect of Polysaccharides from Sargassum Horneri Against Oxidative Stress in Raw264.7 Cells. Int. J. Biol. Macromol. 2014, 68, 98–106. [Google Scholar] [CrossRef] [PubMed]
- Ping, S.; Chen, X.; Sun, P. Chemical Characterization, Antioxidant and Antitumor Activity of Sulfated Polysaccharide from Sargassum Horneri. Carbohyd. Polym. 2014, 105, 260–269. [Google Scholar]
- Shobharani, P.; Nanishankar, V.H.; Halami, P.M.; Sachindra, N.M. Antioxidant and Anticoagulant Activity of Polyphenol and Polysaccharides from Fermented Sargassum Sp. Int. J. Biol. Macromol. 2014, 65, 542–548. [Google Scholar] [CrossRef] [PubMed]
- Zhang, W.; Du, J.Y.; Jiang, Z.D.; Okimura, T.; Oda, T.; Yu, Q.; Jin, J.-O. Ascophyllan Purified from Ascophyllum Nodosum Induces Th1 and Tc1 Immune Responses by Promoting Dendritic Cell Maturation. Mar. Drugs 2014, 12, 4148–4164. [Google Scholar]
- Yuan, Y.; Macquarrie, D. Microwave Assisted Extraction of Sulfated Polysaccharides (fucoidan) from Ascophyllum Nodosum and its Antioxidant Activity. Carbohyd. Polym. 2015, 129, 101–107. [Google Scholar] [CrossRef] [PubMed]
- Ammar, H.H.; Lajili, S.; Said, R.B.; Cerf, D.L.; Bouraoui, A.; Majdoub, H. Physico-Chemical Characterization and Pharmacological Evaluation of Sulfated Polysaccharides from Three Species of Mediterranean Brown Algae of the Genus Cystoseira. Daru J. Pharm. Sci. 2015, 23, 1–8. [Google Scholar] [CrossRef] [PubMed]
- Shao, P.; Chen, X.; Sun, P. Improvement of Antioxidant and Moisture-Preserving Activities of Sargassum Horneri Polysaccharide Enzymatic Hydrolyzates. Int. J. Biol. Macromol. 2015, 74, 420–427. [Google Scholar] [CrossRef] [PubMed]
- Athukorala, Y.; Lee, K.W.; Park, E.J.; Heo, M.S.; Yeo, I.K.; Lee, Y.D.; Jeon, Y.J. Reduction of Lipid Peroxidation and H2O2-Mediated DNA Damage by a Red Alga (Grateloupia Filicina) Methanolic Extract. J. Sci. Food Agr. 2005, 85, 2341–2348. [Google Scholar] [CrossRef]
- Wang, S.C.; Bligh, S.W.; Shi, S.S.; Wang, Z.T.; Hu, Z.B.; Crowder, J.; Branford-White, C.; Vella, C. Structural Features and Anti-HIV-1 Activity of Novel Polysaccharides from Red Algae Grateloupia Longifolia and Grateloupia Filicina. Int. J. Biol. Macromol. 2007, 41, 369–375. [Google Scholar] [CrossRef] [PubMed]
- Yu, G.; Li, M.; Wang, W.; Liu, X.; Zhao, X.; Lv, Y.; Li, G.; Jiao, G.; Zhao, X. Structure and Anti-Influenza A (H1N1) Virus Activity of Three Polysaccharides from Eucheuma Denticulatum. J. Ocean U. China 2012, 11, 527–532. [Google Scholar] [CrossRef]
- Shi, C.; Pan, T.; Cao, M.J.; Liu, Q.M.; Zhang, L.J.; Liu, G.M. Suppression of Th2 Immune Responses by the Sulfated Polysaccharide from Porphyra Haitanensis in Tropomyosin-Sensitized Mice. Int. Immunopharmacol. 2015, 24, 211–218. [Google Scholar] [CrossRef] [PubMed]
- Chen, X.; Yang, S.; Wang, J.; Song, L.; Xing, R.; Liu, S.; Yu, H.; Li, P. Sulfated Polysaccharides Isolated from Cloned Grateloupia Filicina and their Anticoagulant Activity. Biomed Res. Int. 2015, 2015, 1–5. [Google Scholar]
- Fleita, D.; El-Sayed, M.; Rifaat, D. Evaluation of the Antioxidant Activity of Enzymatically-Hydrolyzed Sulfated Polysaccharides Extracted from Red Algae; Pterocladia Capillacea. LWT—Food Sci. Technol. 2015, 63, 1236–1244. [Google Scholar] [CrossRef]
- Karnjanapratum, S.; You, S.G. Molecular Characteristics of Sulfated Polysaccharides from Monostroma Nitidum and their in vitro Anticancer and Immunomodulatory Activities. Int. J. Biol. Macromol. 2011, 48, 311–318. [Google Scholar] [CrossRef] [PubMed]
- Komatsu, T.; Kido, N.; Sugiyama, T.; Yokochi, T. Antiviral Activity of Acidic Polysaccharides from Coccomyxa Gloeobotrydiformi, a Green Alga, Against An in vitro Human Influenza A Virus Infection. Immunopharmacology Immunotoxicology 2012, 35, 1–7. [Google Scholar] [CrossRef] [PubMed]
- Kwon, J.S.; Lee, H.J.; Lee, D.H.; Lee, Y.J.; Mo, I.P.; Nahm, S.S.; Kim, M.J.; Lee, J.B.; Park, S.Y.; Choi, I.S. Immune Responses and Pathogenesis in Immunocompromised Chickens in Response to Infection with the H9N2 Low Pathogenic Avian Influenza Virus. Virus Res. 2008, 133, 187–194. [Google Scholar] [CrossRef] [PubMed]
- Lee, D.H.; Park, J.K.; Lee, Y.N.; Song, J.M.; Kang, S.M.; Lee, J.B.; Park, S.Y.; Choi, I.S.; Song, C.S. H9N2 Avian Influenza Virus-Like Particle Vaccine Provides Protective Immunity and a Strategy for the Differentiation of Infected from Vaccinated Animals. Vaccine 2011, 29, 4003–4007. [Google Scholar] [CrossRef] [PubMed]
- Yuan, J.; Xu, L.; Bao, L.; Yao, Y.; Deng, W.; Li, F.; Lv, Q.; Gu, S.; Wei, Q.; Qin, C. Characterization of an H9N2 Avian Influenza Virus from a Fringilla Montifringilla Brambling in Northern China. Virology 2015, 476, 289–297. [Google Scholar] [CrossRef] [PubMed]
- Kallon, S.; Li, X.; Ji, J.; Chen, C.; Xi, Q.; Shuang, C.; Xue, C.; Ma, J.; Xie, Q.; Zhang, Y. Astragalus Polysaccharide Enhances Immunity and Inhibits H9N2 Avian Influenza Virus in vitro and in vivo. J. Anim. Sci. Biotechnol. 2013, 4, 325–335. [Google Scholar] [CrossRef] [PubMed]
- Lv, J.; Wei, B.; Yang, Y.; Yao, M.; Cai, Y.; Gao, Y.; Xia, X.; Zhao, X.; Liu, Z.; Li, X.; et al. Experimental Transmission in Guinea Pigs of H9N2 Avian Influenza Viruses from Indoor Air of Chicken Houses. Virus Res. 2012, 170, 102–108. [Google Scholar] [CrossRef] [PubMed]
- Lin, Y.P.; Shaw, M.; Gregory, V.; Cameron, K.; Lim, W.; Klimov, A.; Subbarao, K.; Guan, Y.; Krauss, S.; Shortridge, K. Avian-to-human Transmission of H9N2 Subtype Influenza a Viruses: Relationship Between H9N2 and H5N1 Human Isolates. Proc. Natl. Acad. Sci. 2000, 97, 9654–9658. [Google Scholar] [CrossRef] [PubMed]
- Xu, C.; Fan, W.; Wei, R.; Zhao, H. Isolation and Identification of Swine Influenza Recombinant a/Swine/Shandong/1/2003(H9N2) Virus. Microbes Infect. 2004, 6, 919–925. [Google Scholar] [CrossRef] [PubMed]
- Wan, H.; Sorrell, E.M.; Song, H.; Hossain, M.J.; Ramirez-Nieto, G.; Monne, I.; Stevens, J.; Cattoli, G.; Capua, I.; Chen, L.-M.; et al. Replication and transmission of H9N2 Influenza Viruses in Ferrets: Evaluation of Pandemic Potential. PLoS ONE 2008, 3. [Google Scholar] [CrossRef] [PubMed]
- Richard, M.; Schrauwen, E.J.A.; de Graaf, M.; Bestebroer, T.M.; Spronken, M.I.J.; van Boheemen, S.; de Meulder, D.; Lexmond, P.; Linster, M.; Herfst, S. Limited Airborne Transmission of H7N9 Influenza a Virus Between Ferrets. Nature 2013, 501, 560–563. [Google Scholar] [CrossRef] [PubMed]
- Dalby, A.R.; Iqbal, M. A Global Phylogenetic Analysis in Order to Determine the Host Species and Geography Dependent Features Present in the Evolution of Avian H9N2 Influenza Hemagglutinin. PeerJ 2014, 2. [Google Scholar] [CrossRef] [PubMed]
- Lam, T.-Y.; Wang, J.; Shen, Y.Y.; Zhou, B.P.; Duan, L.; Cheung, C.-L.; Ma, C.; Lycett, S.J.; Leung, Y.H.; Chen, X.C.; et al. The Genesis and Source of the H7N9 Influenza Viruses Causing Human Infections in China. Nature 2013, 502, 241–244. [Google Scholar] [CrossRef] [PubMed]
- Peiris, M.; Yuen, K.Y.; Leung, C.W.; Chan, K.H.; lp, P.L.; Lai, R.W.; Orr, W.K.; Shortridge, K.F. Human Infection with Influenza H9N2. Lancet 1999, 354, 916–917. [Google Scholar] [CrossRef]
- Westenius, V.; Mäkelä, S.M.; Ziegler, T.; Julkunen, I.; Osterlund, P. Efficient Replication and Strong Induction of Innate Immune Responses by H9N2 Avian Influenza Virus in Human Dendritic Cells. Virology 2014, 471, 38–48. [Google Scholar] [CrossRef] [PubMed]
- Bouhlal, R.; Haslin, C.; Chermann, J.C.; Colliec-Jouault, S.; Sinquin, C.; Simon, G.; Cerantola, S.; Riadi, H.; Bourgougnon, N. Antiviral Activities of Sulfated Polysaccharides Isolated from Sphaerococcus Coronopifolius (Rhodophytha, Gigartinales) and Boergeseniella Thuyoides (Rhodophyta, Ceramiales). Mar. Drugs 2011, 9, 1187–1209. [Google Scholar] [CrossRef] [PubMed]
- Kim, M.; Yim, J.H.; Kim, S.Y.; Kim, H.S.; Lee, W.G.; Kim, S.J.; Kang, P.S.; Lee, C.K. In vitro Inhibition of Influenza a Virus Infection by Marine Microalga-Derived Sulfated Polysaccharide P-Kg03. Antivir. Res. 2012, 93, 253–259. [Google Scholar] [CrossRef] [PubMed]
- Pujol, C.A.; Ray, S.; Ray, B.; Damonte, E.B. Antiviral Activity Against Dengue Virus of Diverse Classes of Algal Sulfated Polysaccharides. Int. J. Biol. Macromol. 2012, 51, 412–416. [Google Scholar] [CrossRef] [PubMed]
- Fang, X.B.; Chen, X.E. Structure Elucidation and Immunological Activity of a Novel Pectic Polysaccharide from the Stems of Avicennia Marina. Eur. Food Res. Technol. 2013, 236, 243–248. [Google Scholar] [CrossRef]
- Liu, C.; Chen, J.; Li, E.; Fan, Q.; Wang, D.; Li, P.; Li, X.; Chen, X.; Qiu, S.; Gao, Z.; et al. The Comparison of Antioxidative and Hepatoprotective Activities of Codonopsis Pilosula Polysaccharide (CP) and Sulfated CP. Int. Immunopharmacol. 2015, 24, 299–305. [Google Scholar] [CrossRef] [PubMed]
- Tabarsa, M.; Lee, S.J.; You, S. Structural Analysis of Immunostimulating Sulfated Polysaccharides from Ulva Pertusa. Carbohydr. Res. 2012, 361, 141–147. [Google Scholar] [CrossRef] [PubMed]
- Wang, X.; Chen, Y.; Wang, J.; Liu, Z.; Zhao, S. Antitumor Activity of a Sulfated Polysaccharide from Enteromorpha Intestinalis Targeted Against Hepatoma through Mitochondrial Pathway. Tumor Biol. 2013, 35, 1641–1647. [Google Scholar] [CrossRef] [PubMed]
- Yu, Q.; Yan, J.; Wang, S.; Ji, L.; Ding, K.; Vella, C.; Wang, Z.; Hu, Z. Antiangiogenic Effects of GFP08, an Agaran-Type Polysaccharide Isolated from Grateloupia Filicina. Glycobiology 2012, 22, 1343–1352. [Google Scholar] [CrossRef] [PubMed]
- Faggio, C.; Pagano, M.; Dottore, A.; Genovese, G.; Morabito, M. Evaluation of Anticoagulant Activity of Two Algal Polysaccharides. Nat. Prod. Res. 2015. [Google Scholar] [CrossRef] [PubMed]
- Wang, Y.; Huang, M.; Sun, R.; Pan, L. Extraction, Characterization of a Ginseng Fruits Polysaccharide and its Immune Modulating Activities in Rats with Lewis Lung Carcinoma. Carbohydr. Polym. 2015, 127, 215–221. [Google Scholar] [CrossRef] [PubMed]
- Turan, K.; Nagata, K.; Kuru, A. Antiviral effect of Sanicula Europaea L. Leaves Extract on Influenza Virus-Infected Cells. Biochem. Biophys. Res. Commun. 1996, 225, 22–26. [Google Scholar] [CrossRef] [PubMed]
- Li, D.Y.; Xue, M.Y.; Wang, C.; Wang, J.B.; Chen, P.Y. Bursopentine as a Novel Immunoadjuvant Enhances Both Humoral and Cell-Mediated Immune Responses to Inactivated H9N2 Avian Influenza Virus in Chickens. Clin. Vaccine Immunol. CVI 2011, 18, 1497–1502. [Google Scholar] [CrossRef] [PubMed]
- Zhang, J.J.; Zhang, Q.B.; Wang, J.; Shi, X.L.; Zhang, Z.S. Analysis of the Monosaccharide Composition of Fucoidan by Precolumn Derivation HPLC. Chin. J. Oceanol. Limnol. 2009, 27, 578–582. [Google Scholar] [CrossRef]
- Zhang, W.; Oda, T.; Yu, Q.; Jin, J.O. Fucoidan from Macrocystis Pyrifera has Powerful Immune-Modulatory Effects Compared to Three Other Fucoidans. Mar. Drugs 2015, 13, 1084–1104. [Google Scholar] [CrossRef] [PubMed]
- Thelen, T.; Hao, Y.; Medeiros, A.I.; Curtis, J.L.; Serezani, C.H.; Kobzik, L.; Harris, L.H.; Aronoff, D.M. The Class A Scavenger Receptor, Macrophage Receptor with Collagenous Structure, is the Major Phagocytic Receptor for Clostridium Sordellii Expressed by Human Decidual Macrophages. J. Immunol. 2010, 185, 4328–4335. [Google Scholar] [CrossRef] [PubMed]
- Jin, J.-O.; Zhang, W.; Du, J.-Y.; Wong, K.-W.; Oda, T.; Yu, Q. Fucoidan can Function as an Adjuvant in vivo to Enhance Dendritic Cell Maturation and Function and Promote Antigen-Specific T Cell Immune Responses. PLoS ONE 2014, 9. [Google Scholar] [CrossRef] [PubMed]
- de Godoi, A. M.; Faccin-Galhardi, L.C.; Lopes, N.; Rechenchoski, D.Z.; de Almeida, R.R.; Ricardo, N.M.P.S.; Nozawa, C.; Linhares, R.E.C. Antiviral Activity of Sulfated Polysaccharide of Adenanthera Pavonina Against Poliovirus in Hep-2 Cells. Evid. Based Complement. Alternat. Med. 2014, 2014. [Google Scholar] [CrossRef] [PubMed]
- Chen, Y.; Xiong, W.; Zeng, L.; Wang, D.; Liu, J.; Wu, Y.; Hu, Y. Comparison of Bush Sophora Root Polysaccharide and its Sulfate's Anti-Duck Hepatitis A Virus Activity and Mechanism. Carbohydr. Polym. 2014, 102, 333–340. [Google Scholar] [CrossRef] [PubMed]
- Chen, Y.; Song, M.; Wang, Y.; Xiong, W.; Zeng, L.; Zhang, S.; Xu, M.; Du, H.; Liu, J.; Wang, D.; et al. The Anti-DHAV Activities of Astragalus Polysaccharide and its Sulfate Compared with those of BSRPs and its Sulfate. Carbohydr. Polym. 2015, 117, 339–345. [Google Scholar] [CrossRef] [PubMed]
- Shang, R.F.; Liang, J.P.; Na, Z.Y.; Yang, H.J.; Lu, Y.; Hua, L.Y.; Guo, W.Z.; Cui, Y.; Wang, L. In vivo Inhibition of NAS Preparation on H9N2 Subtype Aiv. Virol. Sin. 2010, 25, 145–150. [Google Scholar] [CrossRef] [PubMed]
- Dubois, M.; Gilles, K.A.; Hamilton, J.K.; Rebers, P.A.; Smith, F. Colorimetric Method For Determination of Sugars and Related Substances. Anal. Chem. 1956, 28, 350–356. [Google Scholar] [CrossRef]
- Yan, W.; Niu, Y.; Lv, J.; Xie, Z.; Jin, L.; Yao, W.; Gao, X.; Yu, L.L. Characterization of a Heteropolysaccharide Isolated from Diploid Gynostemma Pentaphyllum Makino. Carbohydr. Polym. 2013, 92, 2111–2117. [Google Scholar] [CrossRef] [PubMed]
- Kawai, Y.; Seno, N.; Anno, K. A Modified Method for Chondrosulfatase Assay. Anal. Biochem. 1969, 32, 314–321. [Google Scholar] [CrossRef]
- Cardozo, F.T.; Camelini, C.M.; Cordeiro, M.N.; Mascarello, A.; Malagoli, B.G.; Larsen, I.V.; Rossi, M.J.; Nunes, R.J.; Braga, F.C.; Brandt, C.R.; et al. Characterization and Cytotoxic Activity of Sulfated Derivatives of Polysaccharides from Agaricus Brasiliensis. Int. J. Biol. Macromol. 2013, 57, 265–272. [Google Scholar] [CrossRef] [PubMed]
- Miao, S.; Mao, X.; Pei, R.; Miao, S.; Xiang, C.; Lv, Y.; Yang, X.; Sun, J.; Jia, S.; Liu, Y. Antitumor Activity of Polysaccharides from Lepista Sordida Against Laryngocarcinoma in vitro and in vivo. Int. J. Biol. Macromol. 2013, 60, 235–240. [Google Scholar] [CrossRef] [PubMed]
- Pagano, M.; Faggio, C. The Use of Erythrocyte Fragility to Assess Xenobiotic Cytotoxicity. Cell Biochem. Funct. 2015, 33, 351–355. [Google Scholar] [CrossRef] [PubMed]
- Ma, G.X.; Yang, W.J.; Mariga, A.M.; Fang, Y.; Ma, N.; Pei, F.; Hu, Q.H. Purification, Characterization and Antitumor Activity of Polysaccharides from Pleurotus Eryngii Residue. Carbohydr. Polym. 2014, 114, 297–305. [Google Scholar] [CrossRef] [PubMed]
- Seo, Y.W.; Lee, H.J.; Kim, Y.A.; Youn, H.J.; Lee, B.-J. Effects of Several Salt Marsh Plants on Mouse Spleen and Thymus Cell Proliferation Using MTT Assay. Ocean Sci. J. 2005, 40, 209–212. [Google Scholar] [CrossRef]
- Huang, Y.; Jiang, C.; Hu, Y.; Zhao, X.; Shi, C.; Yu, Y.; Liu, C.; Tao, Y.; Pan, H.; Feng, Y.; et al. Immunoenhancement Effect of Rehmannia Glutinosa Polysaccharide on Lymphocyte Proliferation and Dendritic Cell. Carbohydr. Polym. 2013, 96, 516–521. [Google Scholar] [CrossRef] [PubMed]
- Feng, X.; Su, X.; Wang, F.; Wei, J.; Wang, F.; Cao, R.; Zhou, B.; Mao, X.; Zheng, Q.; Chen, P. Isolation and Potential Immunological Characterization of Tpsglvy, a Novel Bursal Septpeptide Isolated from the Bursa of Fabricius. Peptides 2010, 31, 1562–1568. [Google Scholar] [CrossRef] [PubMed]
- Liu, X.D.; Feng, X.L.; Zhou, B.; Cao, R.B.; Li, X.F.; Ma, Z.Y.; Chen, P.Y. Isolation, Modulatory Functions on Murine B Cell Development and Antigen-Specific Immune Responses of Bp11, a Novel Peptide from the Chicken Bursa of Fabricius. Peptides 2012, 35, 107–113. [Google Scholar] [CrossRef] [PubMed]
- Sokolova, E.V.; Byankina, A.O.; Kalitnik, A.A.; Kim, Y.H.; Bogdanovich, L.N.; Solov'eva, T.F.; Yermak, I.M. Influence of Red Algal Sulfated Polysaccharides on Blood Coagulation and Platelets Activation in vitro. J. Biomed. Mater. Res. Part A 2014, 102, 1431–1438. [Google Scholar] [CrossRef] [PubMed]
- Livak, K.J.; Schmittgen, T.D. Analysis of Relative Gene Expression Data Using Real-Time Quantitative PCR and the 2(-Delta Delta C(T)) Method. Methods 2001, 25, 402–408. [Google Scholar] [CrossRef] [PubMed]
© 2015 by the authors; licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons by Attribution (CC-BY) license (http://creativecommons.org/licenses/by/4.0/).
Share and Cite
Song, L.; Chen, X.; Liu, X.; Zhang, F.; Hu, L.; Yue, Y.; Li, K.; Li, P. Characterization and Comparison of the Structural Features, Immune-Modulatory and Anti-Avian Influenza Virus Activities Conferred by Three Algal Sulfated Polysaccharides. Mar. Drugs 2016, 14, 4. https://doi.org/10.3390/md14010004
Song L, Chen X, Liu X, Zhang F, Hu L, Yue Y, Li K, Li P. Characterization and Comparison of the Structural Features, Immune-Modulatory and Anti-Avian Influenza Virus Activities Conferred by Three Algal Sulfated Polysaccharides. Marine Drugs. 2016; 14(1):4. https://doi.org/10.3390/md14010004
Chicago/Turabian StyleSong, Lin, Xiaolin Chen, Xiaodong Liu, Fubo Zhang, Linfeng Hu, Yang Yue, Kecheng Li, and Pengcheng Li. 2016. "Characterization and Comparison of the Structural Features, Immune-Modulatory and Anti-Avian Influenza Virus Activities Conferred by Three Algal Sulfated Polysaccharides" Marine Drugs 14, no. 1: 4. https://doi.org/10.3390/md14010004