Polysaccharides from Lichens: Structural Characteristics and Biological Activity

Abstract

Lichens have been used for medicinal purposes throughout the ages, and beneficial claims have to some extent been correlated with their polysaccharide content. Of 13,500 lichen species growing worldwide, less than 100 species have been investigated for polysaccharide content. Lichen polysaccharides are mainly of three different structural types: β-glucans, α-glucans, and galactomannans. In addition, a few complex heteroglycans have recently been described, such as thamnolan, a water-soluble, immunologically active heteroglycan with a novel rhamnopyranosylgalactofuranan type of structure. A number of investigations have been carried out on biological effects of lichen polysaccharides, most notably antitumour, immunomodulating, antiviral, and memory-enhancing effects. The current review summarizes present knowledge on the structural characteristics and biological activity of lichen polysaccahrides.

Key words

Lichens - polysaccharides - structural characteristics - antitumour activity - immunological activity - biological activity

References

• 1 Huneck S, Yoshimura I. Identification of Lichen Substances. Berlin; Springer Verlag 1996
• 2 Gorin P AJ, Baron M, Silva M LC, Teixeira A ZA, Iacomini M. Lichen carbohydrates.  Ciencia e Cultura (Journal of the Brazilian Association for the Advancement of Science). 1993;  45 27-36
• 3 Barreto-Bergter E. Chemical Structure, Immunology and Application of Polysaccharides of Fungi and Lichens. In: Atta-ur-Rahman, editor Studies in Natural Products Chemistry Vol. 5, Structure Elucidation (Part B). Amsterdam; Elsevier 1989: 275-340
• 4 Gorin P AJ, Baron M, Iacomini M. Storage Products of Lichens. In: Galun M, editor CRC Handbook of Lichenology Vol. 3. Florida; CRC Press 1988: 9-23
• 5 Gorin P AJ, Barreto-Bergter E. The Chemistry of Polysaccharides of Fungi and Lichens. In: Aspinall GO, editor The Polysaccharides Vol. 2. New York; Academic Press 1983: 389-94
• 6 Olafsdottir E S, Omarsdottir S, Smestad Paulsen B, Jurcic K, Wagner H. Rhamnopyranosylgalactofuranan, a new immunologically active polysaccharide from Thamnolia subuliformis .  Phytomedicine. 1999;  6 (4) 273-9
• 7 Iacomini M, Zanin S MW, Fontana J D. Isolation and characterization of β-D-glucan, heteropolysaccharide, and trehalose components of the Basidiomycetous lichen Cora pavonia .  Carbohydrate Research. 1987;  168 55-65
• 8 Common R S. The distribution and taxonomic significance of lichenan and isolichenan in the Parmeliaceae (lichenized Ascomycotina), as determined by iodine reactions. I. Introduction and methods. II. The genus Alectoria and associated taxa.  Mycotaxon. 1991;  XLI 67-112
• 9 Teixeira A ZA, Iacomini M, Gorin P AJ. Chemotypes of mannose-containing polysaccharides of lichen mycobionts: a possible aid in classification and identification.  Carbohydrate Research. 1995;  266 309-14
• 10 Takahashi K, Takeda T, Shibata S. Polysaccharides of lichen symbionts.  Chemical & Pharmaceutical Bulletin. 1979;  27 (1) 238-41
• 11 Konig J, Pevelung E. Cell wall of the phycobiont Trebouxia and Pseudotrebouxia: Constituents and their localization.  Lichenologist. 1984;  16 129-44
• 12 Stone B A, Clarke A E. Chemistry and Biology of (1-3)-β-Glucans. Victoria, Australia; La Trobe University Press 1992: 60-75, 283 - 358
• 13 Vartia K O. Antibiotics from Lichens. In: Ahmadjian V, Hale MS, editors The Lichens. New York; Academic Press 1973: 547
• 14 Ingólfsdóttir K. Bioactive Compounds in Iceland Moss. In: Smestad-Paulsen B, editor Bioactive Carbohydrate Polymers, Proceedings Phytochemical Society of Europe. Dordrecht; Kluwer Academic Publishers 2000: 25-36
• 15 Baron M, Iacomini M, Fanta E, Gorin P AJ. Galactomannan, lichenan and isolichenan from the polysaccharide-rich lichen Newropogon aurantiago-ater .  Phytochemistry. 1991;  30 3125-6
• 16 Smith A L. Lichens. Cambridge University Press 1921
• 17 Takeda T, Funatsu M, Shibata S, Fukuoka F. Polysaccharides of lichens and fungi V. Antitumor active polysaccharides of Evernia, pacroscyphus and Alectoria species.  Chemical & Pharmaceutical Bulletin. 1972;  20 2445-9
• 18 Chanda N B, Hirst E L, Manners D J. A comparison of isolichenin and lichenin from Iceland moss (Cetraria islandica).  Journal of Chemical Society. 1957;  1951-8
• 19 Peat S, Whelan W J, Turvey J R, Morgan K. The structure of isolichenin.  Journal of Chemical Society. 1961;  623-9
• 20 Olafsdottir E S, Ingolfsdottir K, Barsett H, Smestad Paulsen B, Jurcic K, Wagner H. Immunologically active (1→3)-(1→4)-α-D-glucan from Cetraria islandica .  Phytomedicine. 1999;  6 (1) 33-9
• 21 Ulander A, Tollens B. Untersuchungen über die Kohlenhydrate der Flechten.  Berichte der deutschen chemischen Gesellschaft. 1906;  39 401
• 22 Preston J F, Gander J E. Isolation and partial characterization of the extracellular polysaccharides of Penicillium charlesii .  Archives of Biochemistry and Biophysics. 1968;  124 504-12
• 23 Prado S RT, Gorin P AJ, Stuelp P M, Honda N K, Iacomini M. An unusual juxtaposition of polysaccharide components of Collema leptosporum .  Carbohydrate Polymers. 1999;  40 271-6
• 24 Ingolfsdottir K, Jurcic K, Fischer B, Wagner H. Immunologically active polysaccharide from Cetraria islandica .  Planta Medica. 1994;  60 527-31
• 25 Iacomini M, Schneider C L, Gorin P AJ. Comparative studies on the polysaccharides of Cladonia alphestris (Reindeer moss), Cladonia confusa and Cladonia amaurocraea .  Carbohydrate Research. 1985;  142 237-51
• 26 Shibata S. Polysaccharides of lichens.  Journal of the National Science Council of Sri Lanka. 1973;  1 183-8
• 27 Woranovicz-Barreira S M, Gorin P AJ, Sassaki G L, Tischer C A, Ahti T, Iacomini M. Chemotyping glucans from lichens of the genus Cladonia .  Phytochemistry. 1999;  52 1069-74
• 28 Nishikawa Y, Ohki K, Takahashi K, Kurono G, Fukuoka F, Emori M. Studies on the water soluble constituents of lichens. II. Antitumor polysaccharides of Lasallia, Usnea and Cladonia Species.  Chemical & Pharmaceutical Bulletin. 1974;  22 2692-702
• 29 Woranovicz-Barreira S M, Pinto B M, Gorin P AJ, Iacomini M. Novel structures in galactomannans of the lichens Cladonia substellata and Cladonia ibitipocae: Significance as chemotypes.  Phytochemistry. 1999;  51 395-402
• 30 Gorshkova R P, Nazarenko E L, Zubkov V A, Stepanenko L S, Isakov V V. Structural study of polysaccharides from Cetraria cucullata and Cetraria islandica lichens.  Russian Journal of Bioorganic Chemistry. 1997;  23 (2) 122-5
• 31 Gorin P A, Iacomini M. Polysaccharides of the lichens Cetraria islandica and Ramalina usnea .  Carbohydr. Res.. 1984;  128 119-32
• 32 Mittal O P, Neelakantan S, Seshadri T R. Chemical investigations of Indian lichens. Part XIV.  Journal of Scientific and Industrial Research (India). 1952;  11B 386-7
• 33 Yokota I, Shibata S, Saito H. A ¹³C-n.m.r. analysis of linkages in lichen polysaccharides: an approach to chemical taxonomy of lichens.  Carbohydrate Research. 1979;  69 252-8
• 34 Teixeira A ZA, Iacomini M, Gorin P AJ. An unusual glucomannan from Tornabenia incarnata .  Phytochemistry. 1992;  31 3467-70
• 35 Micovic V M, Hranisavljevic-Jakovljevic M, Miljkovic-Stojanovic J. Structural study of polysaccharides from the oak lichen Evernia prunastri (L.)  Ach. Carbohydrate Research. 1969;  10 525-33
• 36 Iacomini M, Gorin P AJ, Baron M, Tulloch A P, Mazurek M. Novel D-glucans obtained by dimethyl sulphoxide extraction of the lichens Letharia vulpina, Actinogyra muehlenbergii and an Usnea sp.  Carbohydrate Research. 1988;  176 117-26
• 37 Gorin P AJ, Iacomini M. Structural diversity of galactomannan components isolated from lichens having Ascomycetous mycosymbionts.  Carbohydrate Research. 1985;  142 253-67
• 38 Takeda T, Nishikawa Y, Shibata S. A new α-glucan from the lichen Parmelia caperata (L.)  Ach. Chemical & Pharmaceutical Bulletin. 1970;  18 (5) 1074-5
• 39 Smriga M, Saito H, Shibata S, Narui T, Okuyama T, Nishiyama N. PC-2, linear homoglucan with α-linkages, peripherally enhanches the hippocampal long-term potentiation.  Pharmaceutical Research. 1996;  13 (9) 1322-6
• 40 Olafsdottir E S. Unpublished results. 
• 41 Nishikawa Y, Takeda T, Shibata S, Fukuoka F. Polysaccharides in lichens and fungi III. Further investigation on the structures and the antitumor activity of the polysaccharides from Gyrophora esculenta Miyoshi and Lasailla papulosa (Ach.) Llano.  Chemical & Pharmaceutical Bulletin. 1969;  17 1910-6
• 42 Periera E C, Nascimento S C, Lima R C, Silva N H, Oliveira A F, Bandeira E, Boitard M, Beriel H, Vicente C, Legaz M E. Analysis of Usnea fasciata crude extracts with antineoplastic activity.  Tokai Journal of Experimental and Clinical Medicine. 1994;  19 47-52
• 43 Mittal O P, Seshadri T R. Chemical investigation of Indian lichens XVI. Purification and composition of lichenin and isolichenin from Indian lichens.  Journal of Scientific and Industrial Research (India). 1954;  13B 244-5
• 44 Shibata S, Nishikawa Y, Takeda T, Tanaka M, Fukuoka F, Nakanishi M. Studies on the chemical structures of the new glucans isolated from Gyrophora esculenta Miyoshi and Lasailla papulosa (Ach.) Llano and their inhibiting effect on implanted sarcoma 180 in mice.  Chemical & Pharmaceutical Bulletin. 1968;  16 1639-41
• 45 Nishikawa Y, Tanaka M, Shibata S, Fukooka F. Polysaccharides of lichens and fungi IV. Antitumor active O-acetylated pustulan-type glucans from lichens of Umbilicaria species.  Chemical & Pharmaceutical Bulletin. 1970;  18 1431-4
• 46 Lindberg B, McPherson J. Studies on the chemistry of lichens VI. The structure of pustulan.  Acta Chemica Scandinavica. 1954;  8 985
• 47 Kjölberg O, Kvernheim A L. Studies on the polysaccharides III. The structure of alkali-soluble polysaccharides in Umbilicaria pustulata (L.) Hoffm. and Umbilicaria spodochroa (Arch.) Hoffm.  Acta Chemica Scandinavica. 1989;  43 280-5
• 48 Stuelp P M, Carneiro Leao A MA, Gorin P AJ, Iacomini M. The glucans of Ramalina celastri: Relation with chemotypes of other lichens.  Carbohydrate Research. 1999;  40 101-6
• 49 Miceno A M, Gorin P AJ, Iacomini M. Galactomannan and isolichenan components of the carbohydrate-rich lichen Ramalina ecklonii .  Agricultural and Biological Chemistry. 1991;  55 1391-2
• 50 Takahashi K, Kon K, Yokota I, Shibata S. Chemotaxonomic studies on the polysaccharides of lichens.  Polysaccharides of Stereocaulaceous lichens.. Carbohydrate Research. 1981;  89 166-73
• 51 Yokota I, Shibata S. A polysaccharide of the lichen Stereocaulon japonicum .  Chemical & Pharmaceutical Bulletin. 1978;  26 2668-70
• 52 Hauan E, Kjölberg O. Studies on the polysaccharides of lichens. I. The structure of a water-soluble polysaccharide in Stereocaulon paschale (L.) Fr.  Acta Chemica Scandinavica. 1971;  25 2622-8
• 53 Baron M, Gorin P, Iacomini M. Structural studies on the galactomannan isolated from the lichen Stereocaulon ramulosum .  Agricultural and Biological Chemistry. 1989;  53 1751-8
• 54 Baron M, Gorin P AJ, Iacomini M. Isolation and identification of a linear (1→3)-linked β-D-glucan and other carbohydrate components of the lichen Stereocaulon ramulosum (Sw.) Rausch.  Carbohydrate Research. 1988;  177 235-9
• 55 Corradi da Silva M DL, Iacomini M, Jablonski E, Gorin P AJ. Carbohydrate, glycopeptide and protein components of the lichen Sticta sp. and effect of storage.  Phytochemistry. 1993;  33 547-52
• 56 Krämer P, Wincierz U, Grüber G, Tschakert J, Voelter W, Mayer H. Rational approach to fractionation, isolation and characterization of poylsaccharides from the lichen Cetraria islandica .  Arzneimittel - Forschung/Drug Research. 1995;  45 (I) 726-31
• 57 Whistler R L, Bushway A A, Singh P P. Noncytotoxic, antitumour polysaccharides.  Advances in Carbohydrate Chemistry and Biochemistry. 1976;  32 235-75
• 58 Wagner H. Immunomodulatory agents from plants. Progress in Inflammation Research. Parnham M, series editor Basel; Birkhauser Verlag 1999
• 59 Franz G. Polysaccharides in pharmacy: Current applications and future concepts.  Planta Medica. 1989;  55 493-7
• 60 Fukuoka F. et al. Polysaccharides in lichens and fungi. II. Antitumor activities on sarcoma-180 of the polysaccharide preparations from Gyrophora esculenta Miyoshi, Cetraria islandica (L.). Ach. var. Orientalis Asahina, and some other lichens.  GANN Japanese Journal of Cancer Research. 1968;  59 421-32
• 61 Nishikawa Y, Ohno H. Studies on the water-soluble constituents of lichens. IV. Effect of antitumor lichen-glucans and related derivatives on the phagocytic activity of the reticuloendothelial system in mice.  Chemical & Pharmaceutical Bulletin. 1981;  29 (11) 3407-10
• 62 Takahashi K, Takeda T, Shibata S, Inomata M, Fukuoka F. Polysaccharides of lichens and fungi. VI. Antitumour active polysaccharides of lichens of Stictaceae.  Chemical & Pharmaceutical Bulletin. 1974;  22 (2) 404-8
• 63 Konopa J, Privett O S, Jenkin H M, Goldin A. Polysaccharides as stimulators of nonspecific immunological response against syngeneic tumors in mice. In: Sigienthaler W, Luthy R, editors Current Chemotherapy: Proceedings of the 10^th International Congress of Chemotherapy. Washington D.C.; American Society for Microbiology 1978: 1095-7
• 64 Watanabe M, Iwai K, Shibata S, Takahashi K, Narui T, Tashiro T. Purification and characterization of mouse α₁-acid glycoprotein and its possible role in the antitumor activity of some lichen polysaccharides.  Chemical & Pharmaceutical Bulletin. 1986;  34 (6) 2532-41
• 65 Tokuzen R, Nakahara W, Fukuoka F, Shibata S, Nishikawa Y. Liver changes in mice treated with lichen polysaccharides.  Toxicology and Applied Pharmacology. 1970;  17 529-37
• 66 Ingólfsdóttir K, Jurcic K, Wagner H. Immunomodulating polysaccharides from aqueous extracts of Iceland moss.  Phytomedicine. 1998;  5 (5) 333-9
• 67 Leao A MAC, Buchi D F, Iacomini M, Gorin P AJ, Oliveira M BM. Cytotoxic effect against HeLA cells of polysaccharides from the lichen Ramalina celastri .  Journal of Submicroscopic Cytology and Pathology. 1997;  29 (4) 503-9
• 68 Stübler D, Buchenauer H. Antiviral activity of the glucan lichenan (poly-β-(1→3,1→4)-D-anhydroglucose). I. Biological activity in tobacco plants.  Journal of Phytopathology. 1996;  144 37-43
• 69 Stübler D, Buchenauer H. Antiviral activity of the glucan lichenan (poly-β-(1→3,1→4)-D-anhydroglucose). II. Studies on the mode of action.  Journal of Phytopathology. 1996;  144 45-52
• 70 Smriga M, Chen J, Zhang J-T, Narui T, Shibata S, Hirano E, Saito H. Isolichenan, an α-glucan isolated from the lichen Cetrariella islandica, repairs impaired learning behaviour and facilitates hippocampal synaptic plasticity.  Proceedings Japan Academie. 1999;  75, Ser. B 219-23
• 71 Smriga M, Saito H. Effect of selected thallophytic glucans on learning behaviour and short-term potentiation.  Phytotherapy Research. 2000;  14 (3) 153-5
• 72 Nishikawa Y. et al. Studies on the water-soluble constituents of lichens. III. Changes in antitumor effect caused by modifications of pustulan- and lichenan-type glucans.  Chemical & Pharmaceutical Bulletin. 1979;  27 (9) 2065-72
• 73 Hirabayashi K, Iwata S, Ito M, Shigeta S, Narui T, Mori T, Shibata S. Inhibitory effect of a lichen polysaccharide sulfate, GE-3-S, on the replication of human immuno-deficiency virus (HIV) in vitro .  Chemical & Pharmaceutical Bulletin. 1989;  37 (9) 2410-12
• 74 Bohn J A, BeMiller J N. (1→3)-β-D-Glucans as biological response modifiers.  Carbohydrate Polymers. 1995;  28 3-14
• 75 Maeda Y Y, Chihara G. Lentinan and other antitumoural polysaccharides. In: Wagner H, editor Immunomodulatory Agents from Plants. Basel; Birkhauser Verlag 1999: 203-23