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Planta Med 2015; 81(02): 130-137
DOI: 10.1055/s-0034-1383411
Biological and Pharmacological Activity
Original Papers
Georg Thieme Verlag KG Stuttgart · New York

Polysaccharides of Dendrobium officinale Induce Aquaporin 5 Translocation by Activating M3 Muscarinic Receptors

Xiang Lin
1   School of Chinese Medicine, The University of Hong Kong, Pokfulam, Hong Kong, China
,
Jingyi Liu
1   School of Chinese Medicine, The University of Hong Kong, Pokfulam, Hong Kong, China
,
Wingyan Chung
1   School of Chinese Medicine, The University of Hong Kong, Pokfulam, Hong Kong, China
,
Stephen Cho-Wing Sze
1   School of Chinese Medicine, The University of Hong Kong, Pokfulam, Hong Kong, China
,
Haiyan Li
2   Foshan University, Department of Pharmacy, Foshan, China
3   Guangdong Guofang Medical Technology Co. Ltd., Dongguan, China
,
Lixing Lao
1   School of Chinese Medicine, The University of Hong Kong, Pokfulam, Hong Kong, China
,
Yanbo Zhang
1   School of Chinese Medicine, The University of Hong Kong, Pokfulam, Hong Kong, China
› Author Affiliations
Further Information

Publication History

received 28 April 2014
revised 16 November 2014

accepted 22 November 2014

Publication Date:
15 January 2015 (online)

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Abstract

Dendrobium officinale is an herbal medicine that has been clinically used to promote body fluid production. Previous works demonstrated that D. officinale polysaccharides could ameliorate symptoms of salivary secretion of patients with Sjögrenʼs syndrome and in a respective mice model. In the present study, we investigated the underlying mechanism by which D. officinale polysaccharides activate M3 muscarinic receptors and induce extracellular calcium influx, leading to the translocation of aquaporin 5, a water channel protein, to the apical membrane of human submandibular gland epithelial cells. Enzymatic treatment of D. officinale polysaccharides suggested that they are hydrolyzed but do not permeate cell membranes. This finding supports the pharmacological activity of D. officinale polysaccharides to promote salivary secretion.

Key words

Dendrobium officinale - Orchidaceae - polysaccharides - M3 muscarinic receptor - aquaporin 5
 

  • References

  • 1 Paulsen DF. Histology & cell biology: Examination and board review. New York: Lange Medical Books/McGraw-Hill; 2000
    Google Scholar
  • 2 Verkman AS. More than just water channels: unexpected cellular roles of aquaporins. J Cell Sci 2005; 118: 3225-3232
    CrossrefPubMedGoogle Scholar
  • 3 Gresz V, Kwon TH, Hurley PT, Varga G, Zelles T, Nielsen S, Case RM, Steward MC. Identification and localization of aquaporin water channels in human salivary glands. Am J Physiol Gastrointest Liver Physiol 2001; 281: G247-G254
    PubMedGoogle Scholar
  • 4 Gresz V, Kwon TH, Gong H, Agre P, Steward MC, King LS, Nielsen S. Immunolocalization of AQP-5 in rat parotid and submandibular salivary glands after stimulation or inhibition of secretion in vivo . Am J Physiol Gastrointest Liver Physiol 2004; 287: G151-G161
    CrossrefPubMedGoogle Scholar
  • 5 Ishikawa Y, Skowronski MT, Ishida H. Persistent increase in the amount of aquaporin-5 in the apical plasma membrane of rat parotid acinar cells induced by a muscarinic agonist SNI-2011. FEBS Lett 2000; 477: 253-257
    CrossrefPubMedGoogle Scholar
  • 6 Steinfeld SD, Delporte C. Distribution of salivary aquaporin-5 in Sjogrenʼs syndrome. Lancet 2002; 359: 1777-1778 (author reply 1778)
    PubMedGoogle Scholar
  • 7 Melvin JE, Yule D, Shuttleworth T, Begenisich T. Regulation of fluid and electrolyte secretion in salivary gland acinar cells. Annu Rev Physiol 2005; 67: 445-469
    CrossrefPubMedGoogle Scholar
  • 8 Ma T, Song Y, Gillespie A, Carlson EJ, Epstein CJ, Verkman AS. Defective secretion of saliva in transgenic mice lacking aquaporin-5 water channels. J Biol Chem 1999; 274: 20071-20074
    CrossrefPubMedGoogle Scholar
  • 9 Baum BJ. Principles of saliva secretion. Ann N Y Acad Sci 1993; 694: 17-23
    CrossrefPubMedGoogle Scholar
  • 10 Steinfeld S, Cogan E, King LS, Agre P, Kiss R, Delporte C. Abnormal distribution of aquaporin-5 water channel protein in salivary glands from Sjogrenʼs syndrome patients. Lab Invest 2001; 81: 143-148
    CrossrefPubMedGoogle Scholar
  • 11 Beroukas D, Goodfellow R, Hiscock J, Jonsson R, Gordon TP, Waterman SA. Up-regulation of M3-muscarinic receptors in labial salivary gland acini in primary Sjogrenʼs syndrome. Lab Invest 2002; 82: 203-210
    CrossrefPubMedGoogle Scholar
  • 12 Kovacs L, Feher E, Bodnar I, Marczinovits I, Nagy GM, Somos J, Boda V. Demonstration of autoantibody binding to muscarinic acetylcholine receptors in the salivary gland in primary Sjogrenʼs syndrome. Clin Immunol 2008; 128: 269-276
    CrossrefPubMedGoogle Scholar
  • 13 Lee BH, Gauna AE, Perez G, Park YJ, Pauley KM, Kawai T, Cha S. Autoantibodies against muscarinic type 3 receptor in Sjogrenʼs syndrome inhibit aquaporin 5 trafficking. PLoS One 2013; 8: e53113
    CrossrefPubMedGoogle Scholar
  • 14 Takakura K, Takaki S, Takeda I, Hanaue N, Kizu Y, Tonogi M, Yamane GY. Effect of cevimeline on radiation-induced salivary gland dysfunction and AQP5 in submandibular gland in mice. Bull Tokyo Dent Coll 2007; 48: 47-56
    CrossrefPubMedGoogle Scholar
  • 15 Felder CC. Muscarinic acetylcholine receptors: signal transduction through multiple effectors. FASEB J 1995; 9: 619-625
    PubMedGoogle Scholar
  • 16 Ishikawa Y, Inoue N, Zhenfang Y, Nakae Y. Molecular mechanisms and drug development in aquaporin water channel diseases: the translocation of aquaporin-5 from lipid rafts to the apical plasma membranes of parotid glands of normal rats and the impairment of it in diabetic or aged rats. J Pharmacol Sci 2004; 96: 271-275
    CrossrefPubMedGoogle Scholar
  • 17 Ishikawa Y, Eguchi T, Skowronski MT, Ishida H. Acetylcholine acts on M3 muscarinic receptors and induces the translocation of aquaporin5 water channel via cytosolic Ca2+ elevation in rat parotid glands. Biochem Biophys Res Commun 1998; 245: 835-840
    CrossrefPubMedGoogle Scholar
  • 18 Luo A, He X, Zhou S, Fan Y, He T, Chun Z. In vitro antioxidant activities of a water-soluble polysaccharide derived from Dendrobium nobile Lindl. extracts. Int J Biol Macromol 2009; 45: 359-363
    CrossrefPubMedGoogle Scholar
  • 19 Li B, Wang BC, Liang YL, Tang K, Shu KX, Liu WQ. [Effect of polysaccharides content of tissue culturing seedlings on Dendrobium candidium under sound wave stimulation]. Zhong Yao Cai 2006; 29: 645-647
    PubMedGoogle Scholar
  • 20 Wanqian L, Bochu W, Chuanren D, Biao L. A method for isolating functional RNA from callus of Dendrobium candidum contented rich polysaccharides. Colloids Surf B Biointerfaces 2005; 42: 259-262
    CrossrefPubMedGoogle Scholar
  • 21 Hsieh YS, Chien C, Liao SK, Liao SF, Hung WT, Yang WB, Lin CC, Cheng TJ, Chang CC, Fang JM, Wong CH. Structure and bioactivity of the polysaccharides in medicinal plant Dendrobium huoshanense . Bioorg Med Chem 2008; 16: 6054-6068
    CrossrefPubMedGoogle Scholar
  • 22 Fan Y, He X, Zhou S, Luo A, He T, Chun Z. Composition analysis and antioxidant activity of polysaccharide from Dendrobium denneanum . Int J Biol Macromol 2009; 45: 169-173
    CrossrefPubMedGoogle Scholar
  • 23 Zhao Y, Son YO, Kim SS, Jang YS, Lee JC. Antioxidant and anti-hyperglycemic activity of polysaccharide isolated from Dendrobium chrysotoxum Lindl. J Biochem Mol Biol 2007; 40: 670-677
    CrossrefPubMedGoogle Scholar
  • 24 Xiao L, Ng TB, Feng YB, Yao T, Wong JH, Yao RM, Li L, Mo FZ, Xiao Y, Shaw PC, Li ZM, Sze SC, Zhang KY. Dendrobium candidum extract increases the expression of aquaporin-5 in labial glands from patients with Sjogrenʼs syndrome. Phytomedicine 2011; 18: 194-198
    CrossrefPubMedGoogle Scholar
  • 25 Lin X, Sze SCW, Tong Y, Zhang Z, Feng Y, Chen JP, Ng TB, Lin X, Shaw P, Zhang KY. Protective effect of Dendrobium officinale polysaccharides on experimental Sjogrenʼs syndrome. J Compl Integr Med 2010; 7 DOI: 10.2202/1553-3840.1342. online
    PubMedGoogle Scholar
  • 26 Lin X, Shaw PC, Sze SC, Tong Y, Zhang Y. Dendrobium officinale polysaccharides ameliorate the abnormality of aquaporin 5, pro-inflammatory cytokines and inhibit apoptosis in the experimental Sjogrenʼs syndrome mice. Int Immunopharmacol 2011; 11: 2025-2032
    CrossrefPubMedGoogle Scholar
  • 27 Williams MR, Duncan G, Riach RA, Webb SF. Acetylcholine receptors are coupled to mobilization of intracellular calcium cultured human lens cells. Exp Eye Res 1993; 57: 381-384
    CrossrefPubMedGoogle Scholar
  • 28 Collison DJ, Coleman RA, James RS, Carey J, Duncan G. Characterization of muscarinic receptors in human lens cells by pharmacologic and molecular techniques. Invest Ophthalmol Vis Sci 2000; 41: 2633-2641
    PubMedGoogle Scholar
  • 29 Song P, Sekhon HS, Lu A, Arredondo J, Sauer D, Gravett C, Mark GP, Grando SA, Spindel ER. M3 muscarinic receptor antagonists inhibit small cell lung carcinoma growth and mitogen-activated protein kinase phosphorylation induced by acetylcholine secretion. Cancer Res 2007; 67: 3936-3944
    CrossrefPubMedGoogle Scholar
  • 30 Okuda T, Nishida M, Sameshima I, Kyoyama K, Hiramatsu K, Takehara Y, Kohriyama K. Determination of atropine in biological specimens by high-performance liquid chromatography. J Chromatogr 1991; 567: 141-149
    CrossrefPubMedGoogle Scholar
  • 31 Li X, Ding X, Chu B, Zhou Q, Ding G, Gu S. Genetic diversity analysis and conservation of the endangered Chinese endemic herb Dendrobium officinale Kimura et Migo (Orchidaceae) based on AFLP. Genetica 2008; 133: 159-166
    CrossrefPubMedGoogle Scholar
  • 32 Lv GY, Yan MQ, Chen SH. [Review of pharmacological activities of Dendrobium officinale based on traditional functions]. Zhongguo Zhong Yao Za Zhi 2013; 38: 489-493
    PubMedGoogle Scholar
  • 33 Gao J, Jin R, Wu Y, Zhang H, Zhang D, Chang Y, Hu Z. [Comparative study of tissue cultured Dendrobium protocorm with natural Dendrobium candidum on immunological function]. Zhong Yao Cai 2002; 25: 487-489
    PubMedGoogle Scholar
  • 34 Zhang X, Xu JK, Wang J, Wang NL, Kurihara H, Kitanaka S, Yao XS. Bioactive bibenzyl derivatives and fluorenones from Dendrobium nobile . J Nat Prod 2007; 70: 24-28
    CrossrefPubMedGoogle Scholar
  • 35 Zha XQ, Luo JP, Luo SZ, Jiang ST. Structure identification of a new immunostimulating polysaccharide from the stems of Dendrobium huoshanense . Carbohydrate Polymers 2007; 69: 86-93
    CrossrefPubMedGoogle Scholar
  • 36 Wang Q, Gong Q, Wu Q, Shi J. Neuroprotective effects of Dendrobium alkaloids on rat cortical neurons injured by oxygen-glucose deprivation and reperfusion. Phytomedicine 2010; 17: 108-115
    CrossrefPubMedGoogle Scholar
  • 37 Komai K, Shiozawa K, Tanaka Y, Yoshihara R, Tanaka C, Sakai H, Yamane T, Murata M, Tsumiyama K, Hashiramoto A, Shiozawa S. Sjogrenʼs syndrome patients presenting with hypergammaglobulinemia are relatively unresponsive to cevimeline treatment. Mod Rheumatol 2009; 19: 416-419
    CrossrefPubMedGoogle Scholar
  • 38 Tomiita M, Takei S, Kuwada N, Nonaka Y, Saito K, Shimojo N, Kohno Y. Efficacy and safety of orally administered pilocarpine hydrochloride for patients with juvenile-onset Sjogrenʼs syndrome. Mod Rheumatol 2010; 20: 486-490
    CrossrefPubMedGoogle Scholar
  • 39 Carroll RC, Peralta EG. The m3 muscarinic acetylcholine receptor differentially regulates calcium influx and release through modulation of monovalent cation channels. EMBO J 1998; 17: 3036-3044
    CrossrefPubMedGoogle Scholar
  • 40 Falet H, Rendu F. Calcium mobilisation controls tyrosine protein phosphorylation independently of the activation of protein kinase C in human platelets. FEBS Lett 1994; 345: 87-91
    CrossrefPubMedGoogle Scholar
  • 41 Ishikawa Y, Iida H, Ishida H. The muscarinic acetylcholine receptor-stimulated increase in aquaporin-5 levels in the apical plasma membrane in rat parotid acinar cells is coupled with activation of nitric oxide/cGMP signal transduction. Mol Pharmacol 2002; 61: 1423-1434
    CrossrefPubMedGoogle Scholar
  • 42 Ishikawa Y, Yuan Z, Inoue N, Skowronski MT, Nakae Y, Shono M, Cho G, Yasui M, Agre P, Nielsen S. Identification of AQP5 in lipid rafts and its translocation to apical membranes by activation of M3 mAChRs in interlobular ducts of rat parotid gland. Am J Physiol Cell Physiol 2005; 289: C1303-C1311
    CrossrefPubMedGoogle Scholar
  • 43 Asari T, Maruyama K, Kusama H. Salivation triggered by pilocarpine involves aquaporin-5 in normal rats but not in irradiated rats. Clin Exp Pharmacol Physiol 2009; 36: 531-538
    CrossrefPubMedGoogle Scholar
  • 44 Ishikawa Y, Cho G, Yuan Z, Inoue N, Nakae Y. Aquaporin-5 water channel in lipid rafts of rat parotid glands. Biochim Biophys Acta 2006; 1758: 1053-1060
    CrossrefPubMedGoogle Scholar
  • 45 Wellner RB, Hong S, Cotrim AP, Swaim WD, Baum BJ. Modifying the NH2 and COOH termini of aquaporin-5: effects on localization in polarized epithelial cells. Tissue Eng 2005; 11: 1449-1458
    CrossrefPubMedGoogle Scholar
  • 46 Hulme EC, Birdsall NJ, Buckley NJ. Muscarinic receptor subtypes. Annu Rev Pharmacol Toxicol 1990; 30: 633-673
    CrossrefPubMedGoogle Scholar
  • 47 Kruse AC, Kobilka BK, Gautam D, Sexton PM, Christopoulos A, Wess J. Muscarinic acetylcholine receptors: novel opportunities for drug development. Nat Rev Drug Discov 2014; 13: 549-560
    CrossrefPubMedGoogle Scholar
  • 48 Kruse AC, Hu J, Pan AC, Arlow DH, Rosenbaum DM, Rosemond E, Green HF, Liu T, Chae PS, Dror RO, Shaw DE, Weis WI, Wess J, Kobilka BK. Structure and dynamics of the M3 muscarinic acetylcholine receptor. Nature 2012; 482: 552-556
    CrossrefPubMedGoogle Scholar
  • 49 Ding X, Wang Z, Zhou K, Xu L, Xu H, Wang Y. Allele-specific primers for diagnostic PCR authentication of Dendrobium officinale . Planta Med 2003; 69: 587-588
    Article in Thieme ConnectPubMedGoogle Scholar
  • 50 Cuesta G, Suarez N, Bessio MI, Ferreira F, Massaldi H. Quantitative determination of pneumococcal capsular polysaccharide serotype 14 using a modification of phenol-sulfuric acid method. J Microbiol Methods 2003; 52: 69-73
    PubMedGoogle Scholar
  • 51 Giard DJ, Aaronson SA, Todaro GJ, Arnstein P, Kersey JH, Dosik H, Parks WP. In vitro cultivation of human tumors: establishment of cell lines derived from a series of solid tumors. J Natl Cancer Inst 1973; 51: 1417-1423
    PubMedGoogle Scholar
  • 52 Gee KR, Brown KA, Chen WN, Bishop-Stewart J, Gray D, Johnson I. Chemical and physiological characterization of fluo-4 Ca(2+)-indicator dyes. Cell Calcium 2000; 27: 97-106
    CrossrefPubMedGoogle Scholar
  • 53 Stewart GD, Sexton PM, Christopoulos A. Detection of novel functional selectivity at M3 muscarinic acetylcholine receptors using a Saccharomyces cerevisiae platform. ACS Chem Biol 2010; 5: 365-375
    CrossrefPubMedGoogle Scholar
  • 54 Blethrow JD, Glavy JS, Morgan DO, Shokat KM. Covalent capture of kinase-specific phosphopeptides reveals Cdk1-cyclin B substrates. Proc Natl Acad Sci U S A 2008; 105: 1442-1447
    CrossrefPubMedGoogle Scholar