Comparison of Immunomodulating Activities of Dendrobium devonianum and...

[Full title: Comparison of Immunomodulating Activities of Dendrobium devonianum and Dendrobium officinale In vitro and In vivo]

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OPEN ACCESS International Journal of Pharmacology ISSN 1811-7775 DOI: 10.3923/ijp.2019.441.448 Research Article Comparison of Immunomodulating Activities of Dendrobium devonianum and Dendrobium officinale In vitro and In vivo 1 Zheng-Rong Zhao, 1 Shi-Fang Xu, 1 Ping Zhang, 1 Hua Liu, 1 Yue-Guo Wu, 2 Gui-Jiao Zhou, 2 Yi-Heng Cai, 3 Ju-Run Zhao and 2 Feng-Yang Chen 1 Institute of Materia Medica, Zhejiang Academy of Medical Sciences, Hangzhou, China 2 School of Basic Medical Sciences and Forensic Medicine, Hangzhou Medical College, Binwen Road 481, Hangzhou, Zhejiang, 310053, China 3 Longling Institute of Dendrobium, Baoshan, China Abstract Background and Objective: Dendrobium devonianum and Dendrobium officinale are widely used as Chinese medicinal materials and health foods. These two species have similar appearances and chemical constitutions. However, their immunomodulating activities have never been compared. This study aims to investigate and compare the immunomodulating activities of D. devonianum and D. officinale Materials and Methods: Ten batches of D. devonianum and D. officinale were collected from different regions. The botanical origins of the species were authenticated by DNA sequence analysis and the total polysaccharide contents were determined to guarantee the quality of each batch. Their immunomodulating activities were evaluated and compared in vitro and in vivo by splenocytes proliferation and hydrocortisone-induced immunosuppressed mice, respectively. Results: The two species have significant different sequences of DNA ITS region but with very close polysaccharide contents. In vitro study showed that the aqueous extracts of the 10 batches of D. devonianum and D. officinale significantly stimulated splenocyte proliferation with no differences in efficiencies. Furthermore, oral administration of D. devonianum or D. officinale not only significantly alleviated hydrocortisone-induced leukopenia and spleen and thymus atrophy but also significantly increased macrophage phagocytosis and delayed-type hypersensitivity response (DTH) in mice Conclusion: Dendrobium devonianum and D. officinale regulated the innate and adaptive immune responses in vitro and in vivo with no differences in efficiencies Key words: D. devonianum, D. officinale, immunomodulating activity, innate immunity, adaptive immunity Received: December 18, 2018 Accepted: January 30, 2019 Published: March 15, 2019 Citation: Zheng-Rong Zhao, Shi-Fang Xu, Ping Zhang, Hua Liu, Yue-Guo Wu, Gui-Jiao Zhou, Yi-Heng Cai, Ju-Run Zhao and Feng-Yang Chen, 2019 Comparison of immunomodulating activities of Dendrobium devonianum and Dendrobium officinale In vitro and In vivo. Int. J. Pharmacol., 15: 441-448 Corresponding Author: Feng-Yang Chen, School of Basic Medical Sciences and Forensic Medicine, Hangzhou Medical College, Binwen Road 481, Hangzhou, Zhejiang, 310053, China Tel/Fax: +86 571 8769 2775 Yue-Guo Wu, Institute of Materia Medica, Zhejiang Academy of Medical Sciences, Tianmushan Road 182, Hangzhou, Zhejiang, 310013, China Tel/Fax: +86 571 8821 5630 Copyright: © 2019 Zheng-Rong Zhao et al. This is an open access article distributed under the terms of the creative commons attribution License, which permits unrestricted use, distribution and reproduction in any medium, provided the original author and source are credited. Competing Interest: The authors have declared that no competing interest exists Data Availability: All relevant data are within the paper and its supporting information files.

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Int. J. Pharmacol., 15 (3): 441-448, 2019 INTRODUCTION Dendrobium is among the largest genera in the Orchidaceae family, with 1500 of the currently described species distributed mainly in the tropical and subtropical regions 1 . A total of 74 Dendrobium species and 2 variants are found in China (Flora of China, http://frps.eflora.cn/frps/ Dendrobium). The stems of approximately 30 species are used as Chinese medicinal materials to promote the production of body fluids, benefit the stomach, moisten the lungs and relieve cough and other yin-deficiency diseases. Among all these medicinal Dendrobium species, D. officinale Kimura et Migo is considered to have the best and widest medicinal applications. Its ethnopharmacological use, phytochemistry, pharmacology and industrialization have been widely explored and reported. This species has been used solely or combined with other Chinese materia medicas to treat many diseases, such as Sjogrenʼs syndrome, gastric ulcer, alcoholic liver injury, chronic obstructive pulmonary disease, diabetes and hypertensive stroke 2 . Among these activities, the immunomodulating effects of D. officinale have attracted considerable attention 3 In addition to D. officinale , three other Dendrobium species, namely, Dendrobium nobile , Dendrobium chrysotoxum and Dendrobium fimbriatum are listed in the Chinese Pharmacopoeia as Chinese medicinal materials 4 Yu et al 3 compared the immunomodulating activities of these four Dendrobium species (each contained only a single sample) in healthy mice and cyclophosphamide-induced immunosuppressed mice. The results showed that all species promoted lymphocyte proliferation, enhanced phagocytic function of macrophage and increased the number of peripheral white blood cell and leukocytes. However, only D. officinale was found to increase the number of neutrophils in the peripheral blood of mice Dendrobium devonianum Paxt. is another widely consumed Dendrobium species, although it has not been listed in the Chinese Pharmacopoeia. Contrary to D. officinale , which is distributed mainly in China, D. devonianum is distributed widely in Bhutan, India, Burma, Thailand, Vietnam and China (Flora of China, http://frps.eflora.cn/frps/ Dendrobium). Similar to D. officinale , D. devonianum is also used as Chinese medicinal material, health food and nutrient in southwestern China 5 . These two species have similar appearances and chemical constitutions 6,7 . Both species are mass-produced in China by tissue cultivation. However, limited studies on the immunomodulating effects of D. devonianum have been conducted . Especially, the immunomodulating activities of D. devonianum and D. officinale have never been compared previously Therefore, to compare the immunomodulating activities between D. devonianum and D. officinale , in the present study, 10 batches of D. devonianum and D. officinale were collected from different regions. The botanical origins of these materials were first authenticated by DNA sequence analysis and the total polysaccharide contents were determined to guarantee the quality of each batch. Then, their immunomodulating effects were evaluated in vitro through splenocyte proliferation assay. In addition, hydrocortisone-induced immunosuppressed mice were used to further compare the immunomodulating effects between D. devonianum and D. officinale in vivo MATERIALS AND METHODS DNA sequence analysis: Ten samples of D. devonianum and D. officinale (Fig. 1, Table 1) were collected (during Nov., 2016 to Jan. 2017) from different regions in China, mainly in and around Yunnan or Zhejiang province. The voucher specimens were deposited at the Laboratory of Natural Drugs, Institute of Materia Medica, Zhejiang Academy of Medical Sciences, China Table 1: Sources, rDNA ITS sequence identification and polysaccharide content of Dendrobium samples Accession Sequence Polysaccharide Sample ID Locality Voucher number Match species number identity (%) E-value content (%) Dv 1 Longling, Yunnan D 20161130 D. devonianum KP 743545.1 100 0.0 42.5 Dv 2 Pingbian, Yunnan D 20161213 D. devonianum KP 743545.1 99 0.0 35.4 Dv 3 Bannan, Yunnan D 20161107 D. devonianum KJ 210443.1 99 0.0 44.1 Dv 4 Lianghe, Yunnan D 20170109 D. devonianum KJ 210443.1 99 0.0 42.0 Dv 5 Jinping, Yunnan D 20161226 D. devonianum KP 743545.1 98 0.0 44.2 Oc 1 Panan, Zhejiang O 20170106 D. officinale MH 198114.1 100 0.0 39.9 Oc 2 Ruian, Zhejiang O 20161221 D. officinale MH 198114.1 100 0.0 36.1 Oc 3 Guangnan, Yunnan O 20161201 D. officinale MH 198108.1 99 0.0 34.3 Oc 4 Shangrao, Jiangxi O 20161215 D. officinale MH 198114.1 100 0.0 32.5 Oc 5 Wujiang, Jiangsu O 20161216 D. officinale MH 198114.1 99 0.0 43.5 The species identity was confirmed by NCBI-BLAST search program based on rDNA ITS sequence. Total polysaccharide content in each Dendrobium sample was determined by phenol-sulfuric acid colorimetric method 442

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Int. J. Pharmacol., 15 (3): 441-448, 2019 Fig. 1: Representative photographs of 10 Dendrobium samples. Clustering map was made by MEGA-phylogeny reconstruction program based on rDNA ITS sequence Total genomic DNA was isolated by Hi-DNA secure Plant Kit (TIANGEN Biotech, China). The ITS region (ITS 1-5.8 S rDNA-ITS 2) of the nuclear rDNA was amplified and sequenced as previously described 8 . The DNA sequences were aligned using Clustal W and MEGA 9 . The botanical origin of each sample was deduced by the direct comparison with ITS sequences of Dendrobium in the Genbank and analyzed with the National Center for Biotechnology Information (NCBI) BLAST sequence analysis search algorithm Measurement of polysaccharide contents: Total polysaccharide contents in the D. devonianum and D. officinale samples were determined by phenol-sulfuric acid colorimetric method as described in the Chinese Pharmacopoeia 4 . Preparation of aqueous extracts of D. devonianum and D. officinale : The processed dried stems of the samples were first cut into small pieces. Then, the pieces (10 g) were extracted thrice with 500 mL of water under boiling for 3 h Finally, the extract was filtered through Whatman filter paper and the filtrate was concentrated to 100 mL in a rotary evaporator under reduced pressure Experimental animals: Female C 57 BL/6 mice (6 weeks old) were purchased from the Shanghai Slac Laboratory Animal Co., Ltd. (Shanghai, China). Male ICR mice (6 weeks old) were purchased from the Experimental Animals Center of Zhejiang province (Hangzhou, China). The animals were acclimatized for 7 days before use. All procedures were in strict accordance with the P.R. China legislation on the use and care of laboratory animals and with the guidelines established by the Experimental Animals Center of Zhejiang province Moreover, the procedures were approved by the Animal Care and Use Committee of Zhejiang Academy of Medical Sciences, China. Splenocyte proliferation assay: Splenocytes proliferation assay was tested by MTT assay as previously described 10 443 Dv 1 Dv 2 Dv 3 Dv 4 Dv 5 Oc 1 Oc 4 Oc 2 Oc 1 Oc 5 Oc 3 Dv 4 Dv 5 Dv 3 Dv 2 Dv 1 D. devonianum D. officinale Dv 1 Dv 2 Dv 3 Dv 4 Dv 5 Oc 1 Oc 2 Oc 3 Oc 4 Oc 5 Dv 1 Dv 2 Dv 3 Dv 5 Dv 4 Oc 3 Oc 5 Oc 1 Oc 2 Oc 4 D. devonianum D. officinale

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Int. J. Pharmacol., 15 (3): 441-448, 2019 Hydrocortisone-induced immunosuppressed mice and treatment protocols: The model of hydrocortisone-induced immunosuppressed mice was established as previously described 11 . Aqueous extracts of D. devonianum (Dv 1) or D. officinale (Oc 3), its 3 and 9 times dilution were designated as high, medium and low doses, respectively. Mice were orally treated with them once daily for 25 days. The phagocytic activity of monocyte-macrophages was assessed by carbon clearance method 12 . The DTH reaction was elicited by sheep red blood cells (SRBC) and evaluated as previously described 11 Statistical analysis: The data were expressed as mean±standard deviation. Statistical analyses were performed using one-way ANOVA and Studentʼs t-test with SPSS data analysis software (version 13.0). The p-values less than 0.05 were regarded as statistically significant RESULTS DNA sequence analysis and species identification: The samples of Dendrobium species (Fig. 1, Table 1) were collected from 10 different regions in China. We extracted the genomic DNAs and analyzed the nucleotide sequences of the ITS region of the 10 samples to guarantee their botanical origin. Significant differences were found between samples Dv 1-5 and samples Oc 1-5 (Fig. 2) The sequences were aligned using MEGA-Clustal W and Phylogeny Reconstruction program and the results showed that Dv 1 and Dv 2, Dv 3 and Dv 5, Oc 2 and Oc 4 and Oc 3 and Oc 5 displayed the highest similarity (Fig. 1). Using NCBI-BLAST search program, samples Dv 1-5 were found to be identical to the sequence of D. devonianum (sequence identity >98%) and samples Oc 1-5 were identical to the sequence of D. officinale (sequence identity >99%) (Table 1). These results clearly indicated that samples Dv 1-5 belong to D. devonianum and samples Oc 1-5 belong to D. officinale Total polysaccharide content: The results are shown in Table 1. The polysaccharide content in each sample exceeded 25%. The total polysaccharide contents of five samples of D. devonianum were close to those of D. officinale , with corresponding average values of 41.6 and 37.3%. These results suggested that all Dendrobium samples have very close polysaccharide contents. D. devonianum and D. officinale stimulated splenocytes proliferation in vitro : The results were showed in Fig. 3, five D. devonianum samples and five D. officinale samples significantly stimulated splenocyte proliferation in a concentration-dependent manner (p<.05, p<.01 or p<.001). Moreover, no obvious differences were observed in the efficiency between D. devonianum and D. officinale . This result indicated that D. devonianum exhibited similar immunomodulating capacities to D. officinale in vitro D. devonianum and D. officinale alleviated hydrocortisone-induced immunosuppression in mice: The results were shown in Fig. 4 and 5. Compared with the normal control group, injection with hydrocortisone significantly reduced peripheral white blood cell number (Fig. 4 a) and spleen and thymus indices (Fig. 4 b, c) (p<0.01). Furthermore, the rate of blood carbon clearance (Fig. 5 a) and phagocytic index (Fig. 5 b) showed that hydrocortisone inhibited the phagocytic activity of monocyte-macrophages (p<0.01). Hydrocortisone also inhibited the DTH response as represented by footpad swelling (Fig. 5 c) (p<0.01). However, oral administration of D. devonianum or D. officinale at medium and high doses significantly alleviated hydrocortisone-induced leukopenia (Fig. 4 a) and spleen (Fig. 4 b) and thymus atrophy (Fig. 4 c) (p<0.05 or p<0.01) Dendrobium devonianum or D. officinale also significantly increased the phagocytic function of monocyte-macrophages (Fig. 5 a, b) and DTH response (Fig. 5 c), compared with the hydrocortisone only-treated group (p<0.05, p<0.01 or p<0.001). These results suggested that D. devonianum or D. officinale improved innate and adaptive immune responses and counteracted hydrocortisone-induced immunosuppression in vivo . Moreover, in agreement with the results of splenocyte proliferation in vitro , D. devonianum and D. officinale exhibited similar immunomodulating effects in hydrocortisone-induced immunosuppressed mice DISCUSSION In this study, the immunomodulating activities of D. devonianum and D. officinale were compared for the first time. Despite the slight differences in their appearances (Fig. 1) and chemical constitutions 6,7 , there are significant differences of DNA ITS region between D. devonianum and D. officinale as showed by earlier reports 8 and these present studies (Fig. 2). The present results showed that the aqueous extracts of D. officinale stimulated splenocyte proliferation in vitro , as well as alleviated hydrocortisone-induced leukopenia, spleen and thymus atrophy, decrease of macrophages phagocytic function and DTH response in mice, which are in accordance with previous studies on cyclophosphamide-induced immunosuppressed mice 3,13 . In addition, the five batches of D. devonianum and five batches 444

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Int. J. Pharmacol., 15 (3): 441-448, 2019 445 D.d evon ia num .D. o ffic in ale D. dev onianum .D. o ffi cina le D.dev oni anum .D. o ffic ina le D. dev onianum .D. offi cina le Fig. 2: Partial r D NA ITS seque nces of ten D e ndrobium samples. Se q ue nce va riation site s were aligne d by MEG A -clust al W program

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Int. J. Pharmacol., 15 (3): 441-448, 2019 2.5 2.0 1.5 1.0 0.5 0.0 R e la ti v e p ro lifer at io n i n dex Control Dv 1 Dv 2 Dv 3 Dv 4 Dv 5 Oc 1 Oc 2 Oc 3 Oc 4 Oc 5 Low concentration Medium concentration High concentration a c c a a c c b c a b c a c a c c c c c c c c b c (b) 24 18 12 6 0 e a b a b Th y m e in d ex (c) 50 40 30 20 10 0 e a b a a Sp le en i n d e x Normal group Model group D. devonianum D. off icinale (a) 8 6 4 2 0 P er ip h e ral w h it e b lo o d c e ll c o u nt s (1 0 c e ll s k g b .w t ) HG 12 1 e a b a b Low concentration Medium concentration High concentration Fig. 3: Dendrobium devonianum and D. officinale stimulated splenocytes proliferation in vitro The values are presented as Means±SD (n = 4). Significant differences with control group were designated as a p<0.05, b p<0.01 or c p<0.001 Fig. 4(a-c): Dendrobium devonianum and D. officinale alleviated hydrocortisone-induced (a) Leukopenia and (b) Thymus and (c) Spleen atrophy in mice The values are presented as Means±SD (n = 10). Significant differences with model group were designated as a p<0.05 or b p<0.01, with normal control group were designated as e p<0.001 of D. officinale stimulated splenocyte proliferation with the same levels of efficiency Furthermore, similar to D. officinale and D. devonianum exhibited comparable immunomodulating activities on hydrocortisone-induced immunosuppressed mice Polysaccharides are the richest constituents of D. devonianum and D. officinale . According to the Chinese Pharmacopoeia, polysaccharide in D. officinale should not be less 4 than 25%. The monosaccharide compositions of both species were previously reported to be mainly composed of glucose and mannose 14 . In this study, the results showed that the total polysaccharide contents in 5 batches of D. devonianum were very close to those in five batches of D. devonianum (Table 1). Therefore, we infer that the comparable activities of D. devonianum and D. officinale could be mainly ascribed to their similar contents and constitutions of polysaccharides. The constitutions and immunomodulating effects of polysaccharides from D. officinale have been investigated widely 6,15-19 . However, contrary to D. officinale , the constitutions and immunomodulating activities of polysaccharides from D. devonianum are seldom reported. Only in this year, Deng et al 20 identified a polysaccharide with globular conformation from D. devonianum and found that this compound could promote the NO release and phagocytosis of macrophages. Thus, further studies are necessary to elucidate the structures and bioactivities of polysaccharides from D. devonianum This study showed that D. devonianum and D. officinale influenced the peripheral white blood cell number, spleen and thymus indices, splenocyte proliferation, macrophage phagocytosis and T cell-mediated DTH response, indicating they regulated both innate and adaptive immune responses. Polysaccharides from Dendrobium plants may directly or indirectly regulate many immunocytes, such as T cells, B cells, 446

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Int. J. Pharmacol., 15 (3): 441-448, 2019 (a) 0.024 0.018 0.012 0.006 0.000 R a te o f ca rb o n cl e ar an c e ( K ) e a a a b Low concentration Medium concentration High concentration (b) 6 4 2 0 e a b a b P h a g oc y ti c i n d ex ( a) (c) 1.6 1.2 0.8 0.4 0.0 e b c c c F o ot p a d s w el li n g (m m ) Normal group Model group D. devonianum D. off icinale a a Fig. 5(a-c): Dendrobium devonianum and D. officinale increased (a-b) Macrophages phagocytosis and (c) T cells-mediated DTH response in hydrocortisone-induced immunosuppressed mice The values are presented as Means±SD (n = 10). Significant differences with model group were designated as a p<0.05, b p<.01 or c p<0.001, with normal control group were designated as e p<0.001 macrophages, granulocytes, dendritic cells and NK cells 21 However, their definite molecular mechanisms have been rarely explored and deserve further study In addition to the immunomodulating activities, D. officinale is used clinically to treat many chronic diseases, such as Sjogrenʼs syndrome, gastric ulcer, alcoholic liver injury, chronic obstructive pulmonary disease, diabetes and hypertensive stroke 2 . This study indicated that D. devonianum and D. officinale possess comparable immunomodulating activities . Given the slight differences in their chemical constitutions and contents 7 , it is possible that D. devonianum may display other bioactivities as D. officinale , such as anti-fatigue, anti-neoplastic, anti-oxidative and anti-mutagenic activities CONCLUSION By ten batches of D. devonianum and D. officinale , this study discovered that D. devonianum and D. officinale have significant different sequences of DNA ITS region but with very close polysaccharide contents. They regulated the innate and adaptive immune responses in vitro and in vivo with no differences in efficiencies. The similar contents and constitutions of polysaccharides may be responsible for their comparable immunomodulating activities. SIGNIFICANCE STATEMENT This study firstly compared the immunomodulating activities between D. devonianum and D. officinale The findings are beneficial for better using of D. devonianum and D. officinale as Chinese medicinal materials or health foods for immunocompromised people ACKNOWLEDGMENTS We appreciated helpful discussions with Prof. Yan-Fei Xin from Zhejiang Academy of Medical Sciences. The work was supported by Grant-in Aid from Zhejiang Provincial Medicinal Health Program of China (2017 KY 039). REFERENCES 1 Da Silva, J.A.T., X. Jin, J. Dobranszki, J. Lu and H. Wang et al ., 2016. Advances in Dendrobium molecular research: Applications in genetic variation, identification and breeding. Mol. Phylogenet. Evol., 95: 196-216 2 Tang, H., T. Zhao, Y. Sheng, T. Zheng, L. Fu and Y. Zhang, 2017 Dendrobium officinale Kimura et Migo: A review on its ethnopharmacology, phytochemistry, pharmacology and industrialization. Evidence-Based Complement. Altern. Med., Vol. 2017. 10.1155/2017/7436259 3 Yu, Q., P.J. Mao, J.M. Jiang and Z.H. Jin, 2017. Comparison of the effects of four medicinal species of Dendrobium on improving immunological functions on mice. Chin. J. Mod. Applied Pharm., 34: 191-195 4 Chinese Pharmacopoeia Commission, 2015. Chinese Pharmacopoeia. Vol. 1, Chinese Medical Science and Technology Press, Beijing, China 447

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Int. J. Pharmacol., 15 (3): 441-448, 2019 5 Cheng, L.L., F.J. Yang, H.Y. Wang, W. Li and M. Li, 2015. Latest research progress on Dendrobium devonianum . Asia-Pac Tradit. Med., 11: 31-33 6 Wei, W., L. Feng, W.R. Bao, D.L. Ma, C.H. Leung, S.P. Nie and Q.B. Han, 2016. Structure characterization and immunomodulating effects of polysaccharides isolated from Dendrobium officinale . J. Agric. Food Chem., 64: 881-889 7 Ye, Z., J.R. Dai, C.G. Zhang, Y. Lu and L.L. Wu et al ., 2017 Chemical differentiation of Dendrobium officinale and Dendrobium devonianum by using HPLC fingerprints, HPLC-ESI-MS and HPTLC analyses. Evidence-Based Complement. Altern. Med., Vol. 2017. 10.1155/2017/8647212 8 Ding, X., L. Xu, Z. Wang, K. Zhou, H. Xu and Y. Wang, 2002. Authentication of stems of Dendrobium officinale by rDNA ITS region sequences. Planta Med., 68: 191-192 9 Hall, B.G., 2013. Building phylogenetic trees from molecular data with MEGA. Mol. Biol. Evol., 30: 1229-1235 10. Chen, F., Y. Ni, Y. Ye, H. Sun, X. Li and S. Xu, 2012 Stephanthraniline a inhibits the proliferation and activation of T cells in vitro and in vivo . Eur. J. Pharmacol., 685: 186-197 11. Yingjian, L., H. Junming, C. Min, L. Chenyue, Z. Dachao, H. Yuanhua and L. Zhi, 2013. A health food high-peptide meal alleviates immunosuppression induced by hydrocortisone and cyclophosphamide in mice. Food Funct., 4: 1352-1359 12. Ganeshpurkar, A. and A.K. Saluja, 2018. Protective effect of catechin on humoral and cell mediated immunity in rat model. Int. Immunopharmacol., 54: 261-266 13. Li, W., J. Zhang and W. Zhou, 2016. The effects of Dendrobium officinale on the immune response and cytokines production in immunosuppressed mice. J. Hyg. Res., 45: 137-139 14. Wang, D., B. Fan, Y. Wang, L. Zhang and F. Wang, 2018 Optimum extraction, characterization and antioxidant activities of polysaccharides from flowers of Dendrobium devonianum . Int. J. Anal. Chem., Vol. 2018 10.1155/2018/3013497 15. Cai, T.Y., Q.L. Liu, D. Li, A.Z. Chen and B.H. Huang et al ., 1989 Effects of Dendrobium officinale polysaccharides on the activities of T lymphocytes and macrophages. Acad. J. Sun Yat-sen Univ. Med. Sci., 10: 66-67 16. Huang, M.Q., T.Y. Cai and Q.L. Liu, 1996. Effects of polysaccharides from Dendrobium candidum on white blood cells and lymph cell moving inhibition factor of mice. Nat. Prod. Res. Dev., 8: 39-42 17. Xia, L., X. Liu, H. Guo, H. Zhang, J. Zhu and F. Ren, 2012. Partial characterization and immunomodulatory activity of polysaccharides from the stem of Dendrobium officinale (Tiepishihu) in vitro . J. Funct. Foods, 4: 294-301 18. Xie, S.Z., B. Liu, D.D. Zhang, X.Q. Zha, L.H. Pan and J.P. Luo, 2016. Intestinal immunomodulating activity and structural characterization of a new polysaccharide from stems of Dendrobium officinale . Food Funct., 7: 2789-2799 19. He, T.B., Y.P. Huang, L. Yang, T.T. Liu and W.Y. Gong et al ., 2016. Structural characterization and immunomodulating activity of polysaccharide from Dendrobium officinale Int. J. Biol. Macromol., 83: 34-41 20. Deng, Y., M. Li, L.X. Chen, X.Q. Chen, J.H. Lu, J. Zhao and S.P. Li, 2018. Chemical characterization and immunomodulatory activity of acetylated polysaccharides from Dendrobium devonianum . Carbohydr. Polym., 180: 238-245 21. Xing, X., S.W. Cui, S. Nie, G.O. Phillips, H.D. Goff and Q. Wang, 2013. A review of isolation process, structural characteristics and bioactivities of water-soluble polysaccharides from Dendrobium plants. Bioact. Carbohydr. Dietary Fibre, 1: 131-147 448

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Glucose, Chinese Materia Medica, Diabetes, Species identification, Statistical analysis, In vitro, One-way ANOVA, Aqueous extract, MTT assay, Chronic Obstructive Pulmonary Disease, Student's t test, Gastric ulcer, Statistical analyses, In vivo, Clinical use, T cell, Phagocytic activity, Immunomodulating effect, Leukopenia, Medicinal application, Molecular mechanism, Polysaccharide content, Rotary evaporator, Animal Care and Use Committee, Adaptive immune response, Innate immune response, Experimental animal, Genomic DNA, Lymphocyte proliferation, Hydrocortisone, Polysaccharide, NK cell, Phagocytic index, Nucleotide sequence, Neutrophil, Sjogren's syndrome, Anti-neoplastic, Orchidaceae family, Immunocompromised mice, Chemical constitution, DTH response, Health food, Anti-fatigue, Anti oxidative, Phagocytic function, Dendrobium, Splenocytes proliferation, Macrophage, National Center for Biotechnology Information, Chinese Pharmacopoeia, Macrophage phagocytosis, Monocyte-macrophages, B-cell, Dendritic cell, Anti-mutagenic, Splenocyte proliferation, Innate and adaptive, ICR mice, Sequence identity, DNA sequence analysis, Immunocompromised people, Medicinal material, Leukocyte, Mannose, Peripheral white blood cell, DTH reaction, Alcoholic liver injury, Healthy mice, ITS region, Innate and adaptive immune response.