Ocean and Polar Research

  • 제38권2호
  • /
  • Pages.129-137
  • /
  • 2016
  • /
  • 1598-141X(pISSN)
  • /
  • 2234-7313(eISSN)
한국해양과학기술원 (Korea Institute of Ocean Science & Technology)
권호 표지
DOI QR코드

DOI QR Code

Anticancer Activity of Sulfated Polysaccharides Isolated from the Antarctic Red Seaweed Iridaea cordata

  • Kim, Hak Jun (Department of Chemistry, College of Engineering, Pukyong National University) ;
  • Kim, Woo Jung (Biocenter, Gyeonggi Institute of Science and Technology Promotion) ;
  • Koo, Bon-Won (Department of Chemistry, College of Engineering, Pukyong National University) ;
  • Kim, Dong-Woo (Department of Chemistry, College of Engineering, Pukyong National University) ;
  • Lee, Jun Hyuck (Division of Polar Biology, Korea Polar Research Institute) ;
  • Nugroho, Wahyu Sri Kunto (Department of Chemistry, College of Engineering, Pukyong National University)
  • 투고 : 2016.03.24
  • 심사 : 2016.06.07
  • 발행 : 2016.06.30
PDF 다운로드
⟨ 이전 논문 다음 논문 ⟩

초록

This study aimed to isolate and characterize sulfated polysaccharides (SPs) from Iridaea cordata and evaluate their anticancer activity. SPs of the Antarctic red seaweed were obtained by $CaCl_2$ (SP1) and ethanol precipitations (SP2) following diluted acid extraction at room temperature. Yields of SP1 and SP2 were approximately 14% and 23%, respectively, of the dry weight of red seaweed. The average molecular mass of the SP1 and SP2 was estimated about $1.84{\times}10^3$ and $1.42{\times}10^3kDa$, respectively, by size-fractionation High-Performance Liquid Chromatography (HPLC). From the High-Performance Anion-Exchange Chromatography-Pulsed Amperometric Detection (HPAEC-PAD) analysis, the main monosaccharide was galactose with glucose and fucose as minor components. The sulfate content of SP2 (40.4%) was slightly higher than that of SP1 (33.8%). The FT-IR spectra also showed characteristic band of carrageenan-like sulfated polysaccharides. Taken together the SPs are thought to be carrageenan-like sulfated galactan. The polysaccharides (SPs) from I. cordata exhibited weak antitumor activity against PC-3 (prostate cancer), HeLa (cervical cancer), and HT-29 (human colon adenocarcinoma). To our knowledge, this is the first data on biological activity of the Antarctic red seaweed I. cordata.

키워드

참고문헌

  1. Amsler CD, McClintock JB, Baker BJ (1998) Chemical defense against herbivory in the Antarctic marine macroalgae Iridaea cordata and Phyllophora antarctica (Rhodophyceae). J Phycol 34(1):53-59. doi:10.1046/j.1529-8817.1998.340053.x
  2. Barabanova AO, Yermak IM, Glazunov VP, Isakov VV, Titlyanov EA, Solov'eva TF (2005) Comparative study of carrageenans from reproductive and sterile forms of Tichocarpus crinitus (Gmel.) Rupr (rhodophyta, tichocarpaceae). Biochem 70(3):350-356. doi:10.1007/s10541-005-0121-4
  3. Bitter T, Muir HM (1962) A modified uronic acid carbazole reaction. Anal Biochem 4(4):330-334 https://doi.org/10.1016/0003-2697(62)90095-7
  4. Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72(1-2):248-254 https://doi.org/10.1016/0003-2697(76)90527-3
  5. Brito TV, Neto JP, Prudencio RS, Batista JA, Junior JS, Silva RO, Franco AX, Aragao KS, Soares PM, Souza MH, Chaves LS, Freitas AL, Medeiros JV, Barbosa AL (2014) Sulfated-polysaccharide fraction extracted from red algae Gracilaria birdiae ameliorates trinitrobenzenesulfonic acid-induced colitis in rats. J Pharm Pharmacol 66(8):1161-1170. doi:10.1111/jphp.12231
  6. Campo VL, Kawano DFF, Silva Jr DB da, Carvalho I, Braz da SD (2009) Carrageenans: biological properties, chemical modifications and structural analysis - A review. Carbohydr Polym 77:167-180. doi:10.1016/j.carbpol.2009.01.020
  7. Clayton MN, Wiencke C, Kloser H (1997) New records of temperate and sub-Antarctic marine benthic macroalgae from Antarctica. Polar Biol 17(2):141-149. doi:10.1007/s003000050116
  8. Coombe DR, Parish CR, Ramshaw IA, Snowden JM (1987) Analysis of the inhibition of tumour metastasis by sulphated polysaccharides. Int J Cancer 39(1):82-88 https://doi.org/10.1002/ijc.2910390115
  9. Cormaci M, Furnari G, Scammacca B, Alongi G (1996) Summer biomass of a population of Iridaea cordata (Gigartinaceae, Rhodophyta) from Antarctica. Hydrobiologia 326-327(1):267-272. doi:10.1007/BF00047817
  10. Dhargalkar VK (1990) Benthic marine algae of the inshore water at the Vestfold Hills, Antarctica. Ind J Mar Sci 19:110-114
  11. Dhargalkar VK, Verlecar XN (2009) Southern Ocean seaweeds: A resource for exploration in food and drugs. Aquaculture 287(3-4):229-242. doi:10.1016/j.aquaculture.2008.11.013
  12. Dubois M, Gilles KA, Hamilton JK, Rebers Pa, Smith F (1956) Colorimetric method for determination of sugars and related substances. Anal Chem 28(3):350-356 https://doi.org/10.1021/ac60111a017
  13. Falshaw R, Furneaux RH, Stevenson DE (2005) Structural analysis of carrageenans from the red alga, Callophyllis hombroniana Mont. Kutz (Kallymeniaceae, Rhodophyta). Carbohydr Res 340(6):1149-1158. doi:10.1016/j.carres.2005.01.019
  14. Fenoradosoa TA, Delattre C, Laroche C, Wadouachi A, Dulong V, Picton L, Andriamadio P, Michaud P (2009) Highly sulphated galactan from Halymenia durvillei (Halymeniales, Rhodophyta), a red seaweed of Madagascar marine coasts. Int J Biol Macromol 45(2):140-145. doi:10.1016/j.ijbiomac.2009.04.015
  15. Ghosh T, Pujol CA, Damonte EB, Sinha S, Ray B (2009) Sulfated xylomannans from the red seaweed Sebdenia polydactyla: structural features, chemical modification and antiviral activity. Antivir Chem Chemother 19(6):235-242 https://doi.org/10.1177/095632020901900603
  16. Hu X, Jiang X, Aubree E, Boulenguer P, Critchley AT (2006) Preparation and In Vivo. Antitumor Activity of ${\kappa}$-Carrageenan Oligosaccharides. Pharm Biol 44(9):646-650. doi:10.1080/13880200601006848
  17. Jerez JR, Matsuhiro B, Urzua CC (1997) Chemical modifications of the xylan from Palmaria decipiens. Carbohydr Polym 32:155-159. doi:10.1016/S0144-8617(96)00119-1
  18. Jiao G, Yu G, Zhang J, Ewart HS (2011) Chemical structures and bioactivities of sulfated polysaccharides from marine algae. Mar Drugs 9(2):196-233. doi:10.3390/md9020196
  19. Kim DS, Suh HH, Lim DJ, Moon SH, Park YI (2004) Purification of fucoidan from Korean sea tangle (Laminaria religosa) and isolation of fucoidan degrading microorganisms. Korean J Microbiol Biotechnol 32(4):362-365
  20. Knutsen SH, Murano E, D'Amato M, Toffanin R, Rizzo R, Paoletti S (1995) Modified procedures for extraction and analysis of carrageenan applied to the red alga Hypnea musciformis. J Appl Phycol 7(6):565-576. doi:10.1007/BF00003944
  21. Kolender AA, Matulewicz MC (2002) Sulfated polysaccharides from the red seaweed Georgiella confluens. Carbohydr Res 337(1):57-68. doi:10.1016/S0008-6215(01)00283-X
  22. Lahaye M (2001) Developments on gelling algal galactans, their structure and physico-chemistry. J Appl Phycol 13(2):173-184. doi:10.1023/A:1011142124213
  23. Lee Y-K, Lim D-J, Lee Y-H, Park Y-I (2006) Variation in fucoidan contents and monosaccharide compositions of Korean Undaria pinnatifida (Harvey) Suringar (Phaeophyta). 21(1):157-160 https://doi.org/10.4490/ALGAE.2006.21.1.157
  24. Lim B-L, Ryu I-H (2009) Purification, structural characterization, and antioxidant activity of antioxidant substance from the red seaweed Gloiopeltis tenax. J Med Food 12(2):442-451 https://doi.org/10.1089/jmf.2007.0688
  25. Lins KO, Bezerra DP, Alves AP, Alencar NM, Lima MW, Torres VM, Farias WR, Pessoa C, de Moraes MO, Costa-Lotufo LV (2009) Antitumor properties of a sulfated polysaccharide from the red seaweed Champia feldmannii (Diaz-Pifferer). J Appl Toxicol 29(1):20-26 https://doi.org/10.1002/jat.1374
  26. Marinho-Soriano E, Bourret E (2005) Polysaccharides from the red seaweed Gracilaria dura (Gracilariales, Rhodophyta). Bioresour Technol 96(3):379-382. doi:10.1016/j.biortech.2004.04.012
  27. Matsuhiro B, Urzua CC (1996) The acidic polysaccharide from Palmaria decipiens (Palmariales, Rhodophyta). Hydrobiologia 326-327(1):491-495. doi:10.1007/BF00047850
  28. McCandless EL, Craigie JS, Walter JA (1973) Carrageenans in the gametophytic and sporophytic stages of Chondrus crispus. Planta 112(3):201-212. doi:10.1007/BF00385324
  29. Melo MRS, Feitosa JPA, Freitas ALP, De Paula RCM (2002) Isolation and characterization of soluble sulfated polysaccharide from the red seaweed Gracilaria cornea. Carbohydr Polym 49(4):491-498. doi:10.1016/S0144-8617(02)00006-1
  30. Mendes GS, Duarte MER, Colodi FG, Noseda MD, Ferreira LG, Berte SD, Cavalcanti JF, Santos N, Romanos MT V (2014) Structure and anti-metapneumovirus activity of sulfated galactans from the red seaweed Cryptonemia seminervis. Carbohydr Polym 101(1):313-323. doi:10.1016/j.carbpol.2013.09.026
  31. Pereira L, Amado AM, Critchley AT, van de Velde F, Ribeiro-Claro PJA (2009) Identification of selected seaweed polysaccharides (phycocolloids) by vibrational spectroscopy (FTIR-ATR and FT-Raman). Food Hydrocoll 23(7):1903-1909. doi:10.1016/j.foodhyd.2008.11.014
  32. Pereira L, Sousa A, Coelho H, Amado AM, Ribeiro-Claro PJA (2003) Use of FTIR, FT-Raman and 13C-NMR spectroscopy for identification of some seaweed phycocolloids. Biomol Eng 20(4-6):223-228. doi:10.1016/S1389-0344(03)00058-3
  33. Peters KJ, Amsler CD, Amsler MO, McClintock JB, Dunbar RB, Baker BJ (2005a) A comparative analysis of the nutritional and elemental composition of macroalgae from the western Antarctic Peninsula. Phycologia 44(4):453-463. doi:10.2216/0031-8884(2005)44[453:ACAOTN]2.0.CO;2
  34. Piriz ML, Cerezo AS (1991) Seasonal variation of carrageenans in tetrasporic, cystocarpic and "sterile" stages of Gigartina skottsbergii S. et G. (Rhodophyta, Gigartinales). Hydrobiologia 226(2):65-69 https://doi.org/10.1007/BF00006807
  35. Qiu X, Amarasekara A, Doctor V (2006) Effect of oversulfation on the chemical and biological properties of fucoidan. Carbohydr Polym 63(2):224-228 https://doi.org/10.1016/j.carbpol.2005.08.064
  36. Schoenrock KM, Amsler CD, McClintock JB, Baker BJ (2015) Life history bias in endophyte infection of the Antarctic rhodophyte, Iridaea cordata. Bot Mar 58(1):1-8. doi:10.1515/bot-2014-0085
  37. Sekkal M, Legrand P (1993) A spectroscopic investigation of the carrageenans and agar in the $1500-100cm^{-1}$ spectral range. Spectrochim Acta Part A Mol Spectrosc 49(2):209-221 https://doi.org/10.1016/0584-8539(93)80176-B
  38. Sekkal M, Legrand P, Huvenne JP, Verdus MC (1993) The use of FTIR microspectrometry as a new tool for the identification in situ of polygalactanes in red seaweeds. J Mol Struct 294:227-230. doi:10.1016/0022-2860(93)80356-Z
  39. Silvestri LJ, Hurst RE, Simpson L, Settine JM (1982) Analysis of sulfate in complex carbohydrates. Anal Biochem 123(2):303-309 https://doi.org/10.1016/0003-2697(82)90450-X
  40. Sousa NA, Barros FC, Araujo TS, Costa DS, Souza LK, Sousa FB, Leodido AC, Pacífico DM, Araujo Sd, Bezerra FF, Freitas AL, Medeiros JV (2016) The efficacy of a sulphated polysaccharide fraction from Hypnea musciformis against diarrhea in rodents. Int J Biol Macromol 86:865-875. doi:10.1016/j.ijbiomac.2016.02.028
  41. Souza BWS, Cerqueira MA, Bourbon AI, Pinheiro AC, Martins JT, Teixeira JA, Coimbra MA, Vicente AA (2012) Chemical characterization and antioxidant activity of sulfated polysaccharide from the red seaweed Gracilaria birdiae. Food Hydrocoll 27(2):287-292. doi:10.1016/j.foodhyd.2011.10.005
  42. Souza MCR, Marques CT, Dore CMG, Silva FRF, Rocha HAO, Leite EL (2007) Antioxidant activities of sulfated polysaccharides from brown and red seaweeds. J Appl Phycol 19(2):153-160 https://doi.org/10.1007/s10811-006-9121-z
  43. Synytsya A, Copikova J, Matejka P, Machovic V (2003) Fourier transform Raman and infrared spectroscopy of pectins. Carbohydr Polym 54(1):97-106 https://doi.org/10.1016/S0144-8617(03)00158-9
  44. Talarico LB, Damonte EB (2007) Interference in dengue virus adsorption and uncoating by carrageenans. Virology 363(2):473-485 https://doi.org/10.1016/j.virol.2007.01.043
  45. Talarico LB, Duarte ME, Zibetti RG, Noseda MD, Damonte EB (2007) An algal-derived DL-galactan hybrid is an efficient preventing agent for in vitro dengue virus infection. Planta Med 73(14):1464-1468 https://doi.org/10.1055/s-2007-990241
  46. Talarico LB, Pujol CA, Zibetti RGM, Faria PCS, Noseda MD, Duarte MER, Damonte EB (2005) The antiviral activity of sulfated polysaccharides against dengue virus is dependent on virus serotype and host cell. Antiviral Res 66(2):103-110 https://doi.org/10.1016/j.antiviral.2005.02.001
  47. Tsuji RF, Hoshino K, Noro Y, Tsuji NM, Kurokawa T, Masuda T, Akira S, Nowak B (2003) Suppression of allergic reaction by lambda-carrageenan: Toll-like receptor 4/MyD88-dependent and -independent modulation of immunity. Clin Exp Allergy 33(2):249-258. doi:10.1046/j.1365-2222.2003.01575.x
  48. Usov AI (2011) Polysaccharides of the red algae. Adv Carbohydr Chem Biochem 65:115-217. doi:10.1016/B978-0-12-385520-6.00004-2
  49. Wiencke C, Amsler CD (2012) Seaweeds and their communities in polar regions. Seaweed Biology. Seaweeds and their communities in polar regions. Springer, pp 265-291
  50. Wiencke C, Clayton MN, Wagele JW (2002) Antarctic seaweeds. ARG Gantner Verlag KG Ruggell, 239 p
  51. Witvrouw M, De Clercq E (1997) Sulfated polysaccharides extracted from sea algae as potential antiviral drugs. Gen Pharmacol Vasc Syst 29(4):497-511 https://doi.org/10.1016/S0306-3623(96)00563-0
  52. Yamada T, Ogamo A, Saito T, Watanabe J, Uchiyama H, Nakagawa Y (1997) Preparation and anti-HIV activity of low-molecular-weight carrageenans and their sulfated derivatives. Carbohydr Polym 32(1):51-55. doi:10.1016/S0144-8617(96)00128-2
  53. Yu G, Hu Y, Yang B, Zhao X, Wang P, Ji G, Wu J, Guan H (2010) Extraction, isolation and structural characterization of polysaccharides from a red alga Gloiopeltis furcata. J Ocean Univ China 9(2):193-197. doi:10.1007/s11802-010-0193-7
  54. Yuan H, Song J, Li X, Li N, Dai J (2006) Immunomodulation and antitumor activity of ${\kappa}$-carrageenan oligosaccharides. Cancer Lett 243(2):228-234 https://doi.org/10.1016/j.canlet.2005.11.032
  55. Zacher K, Roleda MY, Wulff A, Hanelt D, Wiencke C (2009) Responses of Antarctic Iridaea cordata (Rhodophyta) tetraspores exposed to ultraviolet radiation. Phycol Res 57(3):186-193. doi:10.1111/j.1440-1835.2009.00538.x
  56. Zhou G, Sun Y, Xin H, Zhang Y, Li Z, Xu Z (2004) In vivo antitumor and immunomodulation activities of different molecular weight lambda-carrageenans from Chondrus ocellatus. Pharmacol Res 50(1):47-53 https://doi.org/10.1016/j.phrs.2003.12.002
  57. Zhou G, Xin H, Sheng W, Sun Y, Li Z, Xu Z (2005) In vivo growth-inhibition of S180 tumor by mixture of 5-Fu and low molecular $\lambda$-carrageenan from Chondrus ocellatus. Pharmacol Res 51(2):153-157 https://doi.org/10.1016/j.phrs.2004.07.003

피인용 문헌

  1. Macroalgae Extracts From Antarctica Have Antimicrobial and Anticancer Potential vol.9, pp.1664-302X, 2018, https://doi.org/10.3389/fmicb.2018.00412
  2. Antileishmanial activity of the Antarctic red algae Iridaea cordata (Gigartinaceae; Rhodophyta) pp.1573-5176, 2019, https://doi.org/10.1007/s10811-018-1592-1