Relationship between the Structures and the Antitumor Activities of Tannins
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1 814 Vol. 35 (1987) Chem. Pharm. Bull. 35 (2) (1987) Relationship between the Structures and the Antitumor Activities of Tannins KENICHI MIYAMOTO,*,a NOBUHARU KISHI,a RYOZO KOSHIURA,a TAKASHI YOSHIDA,b TSUTOMU HATANOb and TAKUO OKUDAb Department of Pharmacology, Hokuriku University School of Pharmacy,a Kanagawa-machi, Kanazawa , Japan and Faculty of Pharmaceutical Sciences, Okayama University,b Tsushima, Okayama 700, Japan (Received August 19, 1986) Sixty-three tannins and related polyphenols were intraperitoneally injected into mice at 4 d before intraperitoneal sarcoma-180 cell inoculation, and their antitumor activities were evaluated. The condensed tannins and related compounds all showed negligible activity. As regards the hydrolyzable tannins, active compounds were found among ellagitannins. In particular, dimeric ellagitannins such as oenothein B, rugosin E, rugosin D, gemin A and coriariin A showed significantly higher antitumor activity than agrimoniin, which we previously reported as an antitumor tannin. Coriariin A, which has four galloyl groups instead of two hexahydroxydiphenoyl groups of agrimoniin, showed the strongest activity. It seems to be essential for marked antitumor activity that ellagitannins should possess a dimeric structure with several galloyl groups on the glucose core. Keywords tannin; antitumor activity; sarcoma-180; mice; structure-activity relationship; hydrolyzable tannin; ellagitannin; dimeric ellagitannin; coriariin A A number of medicinal plants have been traditionally used for treatment of various ailments, and it has been suggested that tannins may be the active principles of many of them. Since it has recently become possible to isolate pure tannins from plants, we can now examine the characters and activities of each tannin. As regards biological activities of tannins, inhibition of lipid peroxidation,1) decrease of mutagenicity of several mutagens,2) antiviral activity,3) decrease of blood urea-nitrogen content,4) inhibition of plasmin activity,5) various effects on lipolysis in fat cells,6) and several others have been presented. However, there are very few reports on the antitumor activity of tannins, and on the correlation of their structures with the antitumor activities. Recently, we have reported that the methanol extract from roots of Agrimonia pilosa LEDEB. showed some host-mediated antitumor activities,7) and we showed that the main antitumor constituent in the plant is agrimoniin,8) which is also contained in Agrimonia pilosa japonica and Potentilla kleiniana.9) The present paper deals with the antitumor activities of various types of tannins, and discusses the relationship between structure and antitumor activity. Experimental Materials Sixty-three tannins and related polyphenols were isolated from plants according to the cited methods (indicated in the right-hand column of Table I). OK-432, a streptococcal preparation, was obtained from Chugai Pharmaceutical Co. and used as a positive control.12) Materials were dissolved in sterilized physiological saline before use.
2 No Antitumor Experiments Sarcoma-180 was maintained by intraperitoneal passage at weekly intervals in female ddy mice (Shizuoka Laboratory Animal Center). Six female mice (6-weeks old) in a group were intraperitoneally administered with 5 or 10 mg/kg of a test compound once at 4 d before intraperitoneal inoculation of the tumor cells (1 ~ 105), because agrimoniin, a dimeric ellagitannin, was more effective when given by intraperitoneal injection once at 4 d before the tumor cell inoculation than three times on 1, 4 and 7 d after the inoculation.8) Sixty days after the tumor cell inoculation, survivors were killed and autopsied. The antitumor activity of each compound was evaluated in terms of the number of regressors and the percent increase in the life span (%ILS) calculated according to the following formula: (mean survival days of the vehicle control group)]/ (mean survival days of the vehicle control group) Results and Discussion The results on the in vivo antitumor activity of sixty-three tannins and related compounds are shown in Table I. The data for OK-432 as a positive control12) were obtained under similar experimental conditions. We have reported that agrimoniin (55) is an antitumor tannin.8) In this study, 55 gave sarcoma-180-bearing mice 75.3% and 108.8% ILS at 5 and 10 mg/kg, respectively. Thus, a value of %ILS > 70 was chosen as the minimum requirement for a compound to be considered as active. All the condensed tannins and the related polyphenols (1-7) were practically inactive. As regards the hydrolyzable tannins, caffeic Chart 1
3 816 Vol. 35 (1987) TABLE I. Antitumor Activities of Tannins and Related Compounds against Sarcoma-180 in Mice
4 No The vehicle control mice died d. a) Number of mice negative for tumor at 60 d after the tumor cell inoculation, out of six mice. ECG: ( - )-epicatechin gallate. HHDP: hexahydroxydiphenoyl. acids (8-10) and bergenin and its derivatives (11-13) showed low activities. 3-ƒÍ- Tetragalloylquinic acid (16) markedly prolonged the life span of mice and cured one out of six mice, but further galloylation. of 16 did not lead to an increase of the antitumor activity (17-19). Penta-ƒÍ-galloyl-ƒÀ-D-glucose (22), in which the glucose core is saturated with galloyl groups, was active compared with other galloylglucoses. Several monomeric ellagitannins showed relatively high antitumor activities. Tellimagrandin II (30) has more galloyl groups and showed higher activity than strictinin (27), gemin D (28) and tellimagrandin I (29). Rugosin A (31), which has a valloneic acid at the same location on the glucose core as a hexahydroxydiphenoyl (HHDP) group of 30, cured one mouse. A similar correlation was observed among a group of tannins; pedunculagin (32), casuarictin (33), praecoxin A (34) and rugosin C (35). Only negligible activity was shown by 32, but the other tannins prolonged the life span of mice by over 70% as compared with the control. On the other hand, alnusiin (36) showed relatively high activity, but punicalagin (37) and teroblongin (38) were almost inactive. Among dehydroellagitannins, mallotusinic acid (42) and furosinin (44) showed higher activities than geraniin (41), granatin B (43), dehydrogeraniin (45) and isoterchebin (46). In these cases, the enhancement of the antitumor activity is attributable to factors other than the presence of gallic acid. Compounds with the open chain form of glucose moiety (23-26) hardly showed any antitumor activity. Most of the oligomeric ellagitannins showed strong activities compared with the monomeric tannins. The addition of galloyl groups on the glucose core increased the antitumor activity: cornusiin A (48) and oenothein B (49) showed higher activities than campthothin A (47); rugosin E (51) and rugosin D (52) showed higher activities than coriariin E (50). Isorugosin D (53) cured two out of six mice. It seems therefore that the antitumor activity of tannins is not much influenced by the isomerism between 52 and 53. While
5 818 Vol. 35 (1987) 20: R1=R2=H 21: R1=G, R2=H 22: R1=R2=G 14: n=o 17: n=3 L 15: n=1 18: n=4 16: n=2 19: n=5 32: R1,R2=H2OH, R3 `R4=(s)-HHDP 33: R1=OG, R2=H, R4 `R4=(S)-HHDP 36: R1, R2=H2OH 31: R1 =OG, R2=H, R3=R4=G 27: R1=OG, R2=R3=R4=H 28: R1, R2= H, OH, R3= H, R4=C 34: R1,R2=H2OH, R; `R4=(s)-HHDP 35: R1=OG, R2=H, R3 `R4=(S)-HHDP 29: R1, R2=H2OH, R3=R4=G 30: R1 =OG, R2=H, R3=R4=G 37: R1,R2=H2OH, R3 `R4=Galg 38: R1=H, R2=OG, R3 `R4=Gatg Chart 2 medinillin B (60), nobotanin A (61) and nobotanin F (62) possess two, three and four galloyl groups in their molecule, respectively, all of them showed similar degrees of activity, and in this case, the correlation of the antitumor activity with the galloylation was not clear. On the other hand, it was observed that the antitumor activity of several tannins was potentiated by the conversion of one HHDP group into two galloyl groups (see the chart for a comparison of structures): rugosin F (54) < rugosin D (52); agrimoniin (55) < gemin A (56) < coriariin A (57). Coriariin C (59) which has a valloneic acid instead of an HHDP in 57 cured two mice, but its activity was lower than that of 57. The activity of 48, a dimeric tannin, was significantly higher than that of 29, a monomeric tannin, but the activity of cornusiin C (63), a trimeric tannin, was not higher than that of 48. These results suggest that the antitumor activity of tannins does not simply increase with the molecular weight. Nonacosa-ƒÍ-methylcoriariin A (58), in which the phenolic hydroxyl groups of 57 are completely methylated, was inactive, while 57 showed the strongest antitumor activity among tannins and the related polyphenols examined in this study. It is clear that the presence of free phenolic hydroxyl groups is essential for the antitumor activity. It has been thought that tannins show a number of pharmacological activities due to their astringent activity. Our previous report indicated that the binding activities of tannins with hemoglobin and methylene blue increased with increase of the molecular weight of tannins, particularly upon galloylation.13) We have also reported that the methanol extract from
6 No Chart 3 Agrimonia pilosa LEDEB. and agrimoniin showed cytocidal activity in vitro, but the activity was significantly decreased by the addition of calf serum to the culture; further, they increased macrophage-like cells with cytostatic activity and lymphocytes with growing ability in vivo:7,8) Tannins in this study were injected into the mice at 4 d before the tumor cell inoculation. Consequently, it is difficult to consider that the tannins acted directly on the tumor cells. It appears that a suitable molecular mass with a high level of galloylation may be essential for the antitumor activity of ellagitannins, and the stereochemical composition of free phenolic hydroxyl groups may also be an important factor. It is likely that these tannins show antitumor activity through potentiation of the immunity of host animals. References 1) a) T. Okuda, Y. Kimura, T. Yoshida, T. Hatano, H. Okuda and S. Arichi, Chem. Pharm. Bull., 31, 1625 (1983); b) Y. Kimura, H. Okuda, T. Okuda, T. Hatano, I. Agata and S. Arichi, Planta Medica, 50, 473 (1984); c) Idem, Chem. Pharm. Bull., 33, 2028 (1985). 2) T. Okuda, K. Mori and H. Hayatsu, Chem. Pharm. Bull., 32, 3755 (1984). 3) M. Takechi and Y. Tanaka, Planta Medica, 45, 252 (1982). 4) I. Nishioka, Yakugaku Zasshi, 103, 125 (1983). 5) T. Okuda, T. Yoshida, T. Hatano, M. Kuwahara and S. Iida, Proc. Symp. WAKAN-YAKU, 15, 111 (1982). 6) Y. Kimura, H. Okuda, T. Okuda, T. Yoshida, T. Hatano and S. Arichi, Chem. Pharm. Bull., 31, 2497, 2501 (1983); T. Okuda, Abstract of Papers, 104th Annual Meeting of the Pharmaceutical Society of Japan, Sendai,
7 820 Vol. 35 (1987)
8 No : R= H 59: R= 60: R1,R2 =H,OH R3, R4= H,OH 61: R1,R2 = H,OH R3= OG. R4= H 62: R1 =R3 =OG R2 =R4 =H Chart 5 March 1984, p ) R. Koshiura, K. Miyamoto, Y. Ikeya and H. Taguchi, Jpn. J. Pharmacol., 38, 9 (1985). 8) a) K. Miyamoto, R. Koshiura, Y. Ikeya and H. Taguchi, Abstract of Papers, 105th Annual Meeting of the Pharmaceutical Society of Japan, Kanazawa, April 1985, p. 192; b) Idem, Chem. Pharm. Bull., 33, 3977 (1985). 9) T. Okuda, T. Yoshida, M. Kuwahara, M. U. Memon and T. Shingu, Chem. Pharm. Bull., 32, 2165 (1984). 10) a) T. Okuda, T. Hatano, M. Kuwahara, Y. Higashiyama and Y. Maruyama, Abstract of Papers, 101st Annual Meeting of the Pharmaceutical Society of Japan, Kumamoto, April 1981, p. 512; b) T. Hatano, K. Urita and T. Okuda, Abstract of Papers, 24th Annual Meeting of the Chugoku-Shikoku Branch of the Pharmaceutical Society of Japan, October 1985, p. 45; c) T. Okuda, T. Hatano, K. Sugimoto, I. Agata and S. Nishibe, Abstract of Papers, 105th Annual Meeting of the Pharmaceutical Society of Japan, Kanazawa, April 1985, p. 435; d) T. Yoshida, K. Seno, Y. Takama and T. Okuda, Phytochemistry, 21, 1180 (1982); e) T. Okuda, T. Hatano, M. Matsuda and M. Yoshizaki, Abstract of Papers, 105th Annual Meeting of the Pharmaceutical Society of Japan, Kanazawa, April 1985, p. 499; f) T. Okuda, T. Hatano, N. Ogawa, R. Kira and M. Matsuda, Chem. Pharm. Bull., 32, 4662 (1982); g) G. Britton, P. W. Crabtree, E. Haslam and J. E. Stangroom, J. Chem. Soc., 1966, 783; h) T. Okuda, T. Yoshida, M. Ashida and K. Yazaki, J. Chem. Soc., Perkin Trans. 1, 1983, 1765; i) T. Yoshida, K. Inoue, N. Sanou and T. Okuda, Abstract of Papers, 31st Annual Meeting of the Japanese Society of Pharmacognosy, Tokyo, October 1984, p. 44; j) T. Yoshida, Y. Maruyama, M. U. Memon, T. Shingu and T. Okuda, Phytochemistry, 24, 1041 (1985); k) T. Okuda, T. Hatano and T. Yasui, Heterocycles, 16, 1321 (1981); l) T. Okuda, T. Hatano, K. Yazaki and N. Ogawa, Chem. Pharm. Bull., 30, 4230 (1982); m) T. Yoshida, M. U. Memon and T. Okuda, Heterocycles, 16, 1085 (1981); n) T. Okuda, T. Yoshida, K. Mori and T. Hatano, ibid., 15, 1323 (1981); o) T. Okuda, T. Hatano, M. Matsuda and P. B. English, Abstract of Papers, 32nd Annual Meeting of the Japanese Society of Pharmacognosy, Okayama, October 1985, p. 9; p) T. Okuda, T. Yoshida and K. Mori, Phytochemistry, 14, 1877 (1975); q) T. Okuda, K. Mori and T. Hatano, Chem. Pharm. Bull., 33, 1424
9 822 Vol. 35 (1987) (1985); r) T. Okuda, T. Yoshida and T. Hatano, J. Chem. Soc., Perkin Trans. 1, 1982, 9; s) T. Okuda and K. Seno, Nippon Kagaku Kaishi, 1981, 671; t) T. Okuda, T. Hatano, H. Nitta and R. Fujii, Tetrahedron Lett., 21, 4361 (1980); u) T. Okuda, T. Hatano and K. Yazaki, Chem. Pharm. Bull., 30, 1113 (1982). 11) a) T. Yoshida, T. Hatano, M. Matsuda, T. Shingu and T. Okuda, Symposium Papers, 27th Symposium on the Chemistry of Natural Products, Hiroshima, October 1985, p. 718; b) S. Hattori,T. Hatano and T. Okuda, Abstract of Papers, 31st Annual Meeting of the Japanese Society of Pharmacognosy, Tokyo, October 1984, p. 45; c) T. Okuda, T. Hatano and N. Ogawa, Chem. Pharm. Bull., 30, 4234 (1982); d) T. Okuda, T. Hatano, R. Kira, T. Kaneda and M. Yoshizaki, Abstract of Papers, 32nd Annual Meeting of the Japanese Society of Pharmacognosy, Okayama, October 1985, p. 9; e) T. Yoshida, M. U. Memon, T. Shingu and T. Okuda, J. Chem. Soc., Perkin Trans. 1, 1985, 315; f) T. Okuda, T. Hatano and S. Hattori, Abstract of Papers, 103rd Annual Meeting of the Pharmaceutical Society of Japan, Tokyo, April 1983, p. 225; g) Idem, Abstract of Papers, 104th Annual Meeting of the Pharmaceutical Society of Japan, Sendai, March 1984, p. 179; h) T. Yoshida, Y. Ikeda, T. Okuda and T. Shingu, Abstract of Papers, 106th Annual Meeting of the Pharmaceutical Society of Japan, Chiba, April 1986, p. 239; i) T. Okuda, T. Hatano and R. Kira, Abstract of Papers, 104th Annual Meeting of the Pharmaceutical Society of Japan, Sendai, March 1984, p ) Y. Sakurai, S. Tsukagoshi, H. Satoh, T. Akiba, S. Suzuki and Y. Takagaki, Cancer Chemother. Rep., 56, 9 (1972). 13) T. Okuda, K. Mori and T. Hatano, Chem. Pharm. Bull., 33, 1424 (1985).
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