Structural elucidation of novel saponins in the sea cucumber Holothuria lessoni

Marine Drugs

Volumn 12, Issue 8, 2014, Pages 4439-4473

  Bahrami, Yadollah ^a,b,c   Zhang, Wei ^a,b   Chataway, Tim ^a   Franco, Chris ^a,b  

^a FLINDERS UNIVERSITY   (Australia)

^b Australian Seafood Cooperative Research Centre   (Australia)

^c KERMANSHAH UNIVERSITY OF MEDICAL SCIENCES   (Iran)

Author keywords

Bioactive compounds; Echinodermata; ESI; Holothurian; HPCPC; MALDI; Marine invertebrate; Mass spectrometry; Saponins; Sea cucumber viscera; Structure elucidation; Triterpene glycosides

Indexed keywords

AGLYCONE; ALCOHOL; HOLOTHURIN D; HOLOTHURIN E; HOLOTHURINOSIDE X; HOLOTHURINOSIDE Y; HOLOTHURINOSIDE Z; SAPONIN; SUGAR; UNCLASSIFIED DRUG; GLYCOSIDE; TRITERPENE;

ADSORPTION CHROMATOGRAPHY; ANIMAL TISSUE; ARTICLE; BIOLOGICAL ACTIVITY; CONTROLLED STUDY; ELECTROSPRAY MASS SPECTROMETRY; EXTRACTION AND EXTRACTS; HIGH PERFORMANCE CENTRIFUGAL PARTITION CHROMATOGRAPHY; ISOLATION AND PURIFICATION; MASS SPECTROMETRY; MATRIX ASSISTED LASER DESORPTION IONIZATION MASS SPECTROMETRY; NONHUMAN; PARTITION CHROMATOGRAPHY; PARTITION COEFFICIENT; SEA CUCUMBER; STRUCTURE ACTIVITY RELATION; STRUCTURE ANALYSIS; TANDEM MASS SPECTROMETRY; VISCERA; ANIMAL; CHEMISTRY; HOLOTHURIA; ISOMERISM;

ANIMALS; GLYCOSIDES; HOLOTHURIA; ISOMERISM; SAPONINS; SEA CUCUMBERS; TRITERPENES; VISCERA;

EID: 84908024980     PISSN: None     EISSN: 16603397     Source Type: Journal    
DOI: 10.3390/md12084439     Document Type: Article

References (110)

1. Purcell, S. W.; Samyn, Y.; Conand, C. Commercially Important Sea Cucumbers of the World; FAO Species Catalogue for Fishery Purposes. No. 6; FAO: Rome, Italy, 2012; p. 150.
2. Waller, G. R.; Yamasaki, K. Saponins Used in Food and Agriculture; Plenum Press: New York, NY, USA, 1996; Volume 405.
3. Hostettmann, K.; Marston, A. Saponins; Cambridge University Press: Cambridge, UK, 1995.
4. Elbandy, M.; Rho, J.; Afifi, R. Analysis of saponins as bioactive zoochemicals from the marine functional food sea cucumber Bohadschia cousteaui. Eur. Food Res. Technol. 2014, 238, 1-19.
5. Venugopal, V. Marine Products for Healthcare: Functional and Bioactive Nutraceutical Compounds from the Ocean; CRC Press Taylor & Francis Group: New York, NY, USA, 2009; Volume 13.
6. Ridzwan, B. H. Sea Cucumbers, a Malaysian Heritage, 1st ed.; Research Centre of International Islamic University Malaysia (IIUM), Kuala Lumpur Wilayah Persekutuan: Kuala Lumpur, Malaysia, 2007; pp. 1-15, 89-128.
7. Toral-Granda, V. The Biological and Trade Status of Sea Cucumbers in the Families Holothuriidae and Stichopodidae; Convention on International Trade in Endangered Species of Wild Flora and Fauna: Hague, The Netherlands, 2006.
8. Zhong, Y.; Khan, M. A.; Shahidi, F. Compositional characteristics and antioxidant properties of fresh and processed sea cucumber Cucumaria frondosa. J. Agric. Food Chem. 2007, 55, 1188-1192.
9. Kiew, P. L.; Don, M. M. Jewel of the seabed: Sea cucumbers as nutritional and drug candidates. Int. J. Food Sci. Nutr. 2012, 63, 616-136.
10. Lovatelli, A.; Conand, C. Advances in Sea Cucumber Aquaculture and Management; FAO: Rome, Italy, 2004.
11. Bordbar, S.; Anwar, F.; Saari, N. High-value components and bioactives from sea cucumbers for functional foods-A review. Mar. Drugs 2011, 9, 1761-805.
12. Bahrami, Y.; Zhang, W.; Franco, C. Discovery of novel saponins from the viscera of the sea cucumber Holothuria lessoni. Mar. Drugs 2014, 12, 2633-2667.
13. Caulier, G.; Van Dyck, S.; Gerbaux, P.; Eeckhaut, I.; Flammang, P. Review of saponin diversity in sea cucumbers belonging to the family Holothuriidae. SPC Beche-de-mer Inf. Bull. 2011, 31, 48-54.
14. Dong, P.; Xue, C.; Du, Q. Separation of two main triterpene glycosides from sea cucumber Pearsonothuria graeffei by high-speed countercurrent chromatography. Acta Chromatogr. 2008, 20, 269-276.
15. Han, H.; Zhang, W.; Yi, Y. H.; Liu, B. S.; Pan, M. X.; Wang, X. H. A novel sulfated holostane glycoside from sea cucumber Holothuria leucospilota. Chem. Biodivers. 2010, 7, 1764-1769.
16. Naidu, A. S. Natural Food Antimicrobial Systems; CRC Press: New York, NY, USA, 2000.
17. Zhang, S. L.; Li, L.; Yi, Y. H.; Sun, P. Philinopsides E and F, two new sulfated triterpene glycosides from the sea cucumber Pentacta quadrangularis. Nat. Prod. Res. 2006, 20, 399-407.
18. Zhang, S. Y.; Yi, Y. H.; Tang, H. F.; Li, L.; Sun, P.; Wu, J. Two new bioactive triterpene glycosides from the sea cucumber Pseudocolochirus violaceus. J. Asian Nat. Prod. Res. 2006, 8, 1-8.
19. Zhang, S. L.; Li, L.; Yi, Y. H.; Zou, Z. R.; Sun, P. Philinopgenin A, B, and C, three new triterpenoid aglycones from the sea cucumber Pentacta quadrangulasis. Mar. Drugs 2004, 2, 185-191.
20. Chludil, H. D.; Muniain, C. C.; Seldes, A. M.; Maier, M. S. Cytotoxic and antifungal triterpene glycosides from the Patagonian sea cucumber Hemoiedema spectabilis. J. Nat. Prod. 2002, 65, 860-865.
21. Maier, M. S.; Roccatagliata, A. J.; Kuriss, A.; Chludil, H.; Seldes, A. M.; Pujol, C. A.; Damonte, E. B. Two new cytotoxic and virucidal trisulfated triterpene glycosides from the Antarctic sea cucumber Staurocucumis liouvillei. J. Nat. Prod. 2001, 64, 732-736.
22. Osbourn, A.; Goss, R. J. M.; Field, R. A. The saponins-polar isoprenoids with important and diverse biological activities. Nat. Prod. Rep. 2011, 28, 1261-1268.
23. Francis, G.; Kerem, Z.; Makkar, H. P.; Becker, K. The biological action of saponins in animal systems: A review. Br. J. Nutr. 2002, 88, 587-605.
24. Liu, J.; Yang, X.; He, J.; Xia, M.; Xu, L.; Yang, S. Structure analysis of triterpene saponins in Polygala tenuifolia by electrospray ionization ion trap multiple-stage mass spectrometry. J. Mass Spectrom. 2007, 42, 861-873.
25. Kalinin, V. I.; Aminin, D. L.; Avilov, S. A.; Silchenko, A. S.; Stonik, V. A. Triterpene glycosides from sea cucucmbers (Holothurioidea, Echinodermata). Biological activities and functions. Stud. Nat. Prod. Chem. 2008, 35, 135-196.
26. Jha, R. K.; Zi-rong, X. Biomedical Compounds from Marine organisms. Mar. Drugs 2004, 2, 123-146.
27. Friess, S.; Standaert, F.; Whitcomb, E.; Nigrelli, R.; Chanley, J.; Sobotka, H. Some pharmacologic properties of holothurin, an active neurotoxin from the sea cucumber. J. Pharmacol. Exp. Ther. 1959, 126, 323-329.
28. Kim, S. K.; Himaya, S. W.; kang, K. H. Sea cucumber saponins realization of their anticancer effects. In Marine Pharmacognosy: Trends and Applications; Kim, S. K., Ed.; CRC Press: New York, NY, USA, 2012; pp. 119-128.
29. Aminin, D. L.; Pislyagin, E. A.; Menchinskaya, E. S.; Silchenko, A. S.; Avilov, S. A.; Kalinin, V. I. Immunomodulatory and anticancer activity of sea cucumber triterpene glycosides. Stud. Nat. Prod. Chem. 2014, 41, 75-94.
30. Sarhadizadeh, N.; Afkhami, M.; Ehsanpour, M. Evaluation bioactivity of a sea cucumber, Stichopus hermanni from Persian Gulf. Eur. J. Exp. Biol. 2014, 4, 254-258.
31. Mokhlesi, A.; Saeidnia, S.; Gohari, A. R.; Shahverdi, A. R.; Nasrolahi, A.; Farahani, F.; Khoshnood, R.; Es' Haghi, N. Biological activities of the sea cucumber Holothuria leucospilota. Asian J. Anim. Vet. Adv. 2012, 7, 243-249.
32. Mohammadizadeh, F.; Ehsanpor, M.; Afkhami, M.; Mokhlesi, A.; Khazaali, A.; Montazeri, S. Antibacterial, antifungal and cytotoxic effects of a sea cucumber Holothuria leucospilota, from the north coast of the Persian Gulf. J. Mar. Biol. Assoc. UK 2013, 93, 1401-1405.
33. Mohammadizadeh, F.; Ehsanpor, M.; Afkhami, M.; Mokhlesi, A.; Khazaali, A.; Montazeri, S. Evaluation of antibacterial, antifungal and cytotoxic effects of Holothuria scabra from the north coast of the Persian Gulf. J. Med. Mycol. 2013, 23, 225-229.
34. Yamanouchi, T. On the poisonous substance contained in holothurians. Publ. Seto Mar. Biol. Lab. 1955, 4, 183-203.
35. Avilov, S. A.; Drozdova, O. A.; Kalinin, V. I.; Kalinovsky, A. I.; Stonik, V. A.; Gudimova, E. N.; Riguera, R.; Jimenez, C. Frondoside C, a new nonholostane triterpene glycoside from the sea cucumber Cucumaria frondosa: Structure and cytotoxicity of its desulfated derivative. Can. J. Chem. 1998, 76, 137-141.
36. Han, H.; Yi, Y.; Xu, Q.; La, M.; Zhang, H. Two new cytotoxic triterpene glycosides from the sea cucumber Holothuria scabra. Planta Med. 2009, 75, 1608-1612.
37. Kalinin, V. I.; Avilov, S. A.; Kalinina, E. Y.; Korolkova, O. G.; Kalinovsky, A. I.; Stonik, V. A.; Riguera, R.; Jimenez, C. Structure of eximisoside A, a novel triterpene glycoside from the Far-Eastern sea cucumber Psolus eximius. J. Nat. Prod. 1997, 60, 817-819.
38. Kitagawa, I.; Yamanaka, H.; Kobayashi, M.; Nishino, T.; Yosioka, I.; Sugawara, T. Saponin and sapogenol. XXVII. Revised structures of holotoxin A and holotoxin B, two antifungal oligoglycosides from the sea cucumber Stichopus japonicus Selenka. Chem. Pharm. Bull. (Tokyo) 1978, 26, 3722-3731.
39. Miyamoto, T.; Togawa, K.; Higuchi, R.; Komori, T.; Sasaki, T. Structures of four new triterpenoid oligoglycosides: DS-penaustrosides A, B, C, and D from the sea cucumber Pentacta australis. J. Nat. Prod. 1992, 55, 940-946.
40. Liu, B. S.; Yi, Y. H.; Li, L.; Sun, P.; Yuan, W. H.; Sun, G. Q.; Han, H.; Xue, M. Argusides B and C, two new cytotoxic triterpene glycosides from the sea cucumber Bohadschia argus Jaeger. Chem. Biodivers. 2008, 5, 1288-1297.
41. Girard, M.; Bélanger, J.; Ap Simon, J. W.; Garneau, F. X.; Harvey, C.; Brisson, J. R. Frondoside A. A novel triterpene glycoside from the holothurian Cucumaria frondosa. Can. J. Chem. 1990, 68, 11-18.
42. Thompson, J.; Walker, R.; Faulkner, D. Screening and bioassays for biologically-active substances from forty marine sponge species from San Diego, California, USA. Mar. Biol. 1985, 88, 11-21.
43. Campagnuolo, C.; Fattorusso, E.; Taglialatela-Scafati, O. Feroxosides A-B, two norlanostane tetraglycosides from the Caribbean sponge Ectyoplasia ferox. Tetrahedron 2001, 57, 4049-4055.
44. Dang, N. H.; Thanh, N. V.; Kiem, P. V.; Huong le, M.; Minh, C. V.; Kim, Y. H. Two new triterpene glycosides from the Vietnamese sea cucumber Holothuria scabra. Arch. Pharm. Res. 2007, 30, 1387-1391.
45. Kerr, R. G.; Chen, Z. In vivo and in vitro biosynthesis of saponins in sea cucumbers. J. Nat. Prod. 1995, 58, 172-176.
46. Kim, S. K.; Himaya, S. W. Triterpene glycosides from sea cucumbers and their biological activities. Adv. Food Nutr. Res. 2012, 65, 297-319.
47. Stonik, V. A.; Kalinin, V. I.; Avilov, S. A. Toxins from sea cucumbers (holothuroids): Chemical structures, properties, taxonomic distribution, biosynthesis and evolution. J. Nat. Toxins 1999, 8, 235-248.
48. Chludil, H. D.; Murray, A. P.; Seldes, A. M.; Maier, M. S. Biologically active triterpene glycosides from sea cucumbers (Holothuroidea, Echinodermata). Stud. Nat. Prod. Chem. 2003, 28, 587-615.
49. Kalinin, V. I.; Silchenko, A. S.; Avilov, S. A.; Stonik, V. A.; Smirnov, A. V. Sea cucumbers triterpene glycosides, the recent progress in structural elucidation and chemotaxonomy. Phytochem. Rev. 2005, 4, 221-236.
50. Habermehl, G.; Volkwein, G. Aglycones of the toxins from the Cuvierian organs of Holothuria forskali and a new nomenclature for the aglycones from Holothurioideae. Toxicon 1971, 9, 319-326.
51. Zhang, S. Y.; Tang, H. F.; Yi, Y. H. Cytotoxic triterpene glycosides from the sea cucumber Pseudocolochirus violaceus. Fitoterapia 2007, 78, 283-287.
52. Stonik, V. A.; Elyakov, G. B. Secondary metabolites from echinoderms as chemotaxonomic markers. Bioorg. Mar. Chem. 1988, 2, 43-86.
53. 5, two minor disulphated tetraosides containing 3-O-methylquinovose as terminal monosaccharide units from the sea cucumber Staurocucumis liouvillei (Vaney). Nat. Prod. Res. 2011, 25, 1324-1333.
54. 1, triterpene glycosides from the sea cucumber Synapta maculata containing 3-O-methylglucuronic acid and their cytotoxic activity against tumor cells. J. Nat. Prod. 2008, 71, 525-531.
55. 2 from the sea cucumber Staurocucumis liouvillei: New procedure for separation of highly polar glycoside fractions and taxonomic revision. J. Nat. Prod. 2008, 71, 1677-1685.
56. Aminin, D. L.; Chaykina, E. L.; Agafonova, I. G.; Avilov, S. A.; Kalinin, V. I.; Stonik, V. A. Antitumor activity of the immunomodulatory lead Cumaside. Int. Immunopharmacol. 2010, 10, 648-654.
57. Iniguez-Martinez, A. M.; Guerra-Rivas, G.; Rios, T.; Quijano, L. Triterpenoid oligoglycosides from the sea cucumber Stichopus parvimensis. J. Nat. Prod. 2005, 68, 1669-1673.
58. Xu, R.; Ye, Y.; Zhao, W. Saponins. In Introduction to Natural Products Chemistry; CRC Press: Boca Raton, FL, USA, 2012; pp. 125-145.
59. Van Dyck, S.; Gerbaux, P.; Flammang, P. Qualitative and quantitative saponin contents in five sea cucumbers from the Indian Ocean. Mar. Drugs 2010, 8, 173-189.
60. Avilov, S. A.; Antonov, A. S.; Drozdova, O. A.; Kalinin, V. I.; Kalinovsky, A. I.; Stonik, V. A.; Riguera, R.; Lenis, L. A.; Jiménez, C. Triterpene glycosides from the far-eastern sea cucumber Pentamera calcigera. 1. Monosulfated glycosides and cytotoxicity of their unsulfated derivatives. J. Nat. Prod. 2000, 63, 65-71.
61. Avilov, S. A.; Kalinovsky, A. I.; Kalinin, V. I.; Stonik, V. A.; Riguera, R.; Jiménez, C. Koreoside A, a new nonholostane triterpene glycoside from the sea cucumber Cucumaria koraiensis. J. Nat. Prod. 1997, 60, 808-810.
62. Avilov, S. A.; Antonov, A. S.; Drozdova, O. A.; Kalinin, V. I.; Kalinovsky, A. I.; Riguera, R.; Lenis, L. A.; Jimenez, C. Triterpene glycosides from the far eastern sea cucumber Pentamera calcigera II: Disulfated glycosides. J. Nat. Prod. 2000, 63, 1349-1355.
63. Avilov, S. A.; Antonov, A. S.; Silchenko, A. S.; Kalinin, V. I.; Kalinovsky, A. I.; Dmitrenok, P. S.; Stonik, V. A.; Riguera, R.; Jimenez, C. Triterpene glycosides from the far eastern sea cucumber Cucumaria conicospermium. J. Nat. Prod. 2003, 66, 910-916.
64. Zhang, S. Y.; Yi, Y. H.; Tang, H. F. Bioactive triterpene glycosides from the sea cucumber Holothuria fuscocinerea. J. Nat. Prod. 2006, 69, 1492-1495.
65. Zhang, S. Y.; Yi, Y. H.; Tang, H. F. Cytotoxic sulfated triterpene glycosides from the sea cucumber Pseudocolochirus violaceus. Chem. Biodivers. 2006, 3, 807-817.
66. Jia, L.; Qian, K. An evidence-based perspective of panax ginseng (Asian Ginseng) and panax quinquefolius (American Ginseng) as a preventing or supplementary therapy for cancer patients. In Evidence-based Anticancer Materia Medica; Springer Verlag: New York, NY, USA, 2011; pp. 85-96.
67. Caulier, G.; Flammang, P.; Gerbaux, P.; Eeckhaut, I. When a repellent becomes an attractant: Harmful saponins are kairomones attracting the symbiotic Harlequin crab. Sci. Rep. 2013, 3, 1-5.
68. Bakus, G. J. Defensive mechanisms and ecology of some tropical holothurians. Mar. Biol. 1968, 2, 23-32.
69. Bondoc, K. G. V.; Lee, H.; Cruz, L. J.; Lebrilla, C. B.; Juinio-Meñez, M. A. Chemical fingerprinting and phylogenetic mapping of saponin congeners from three tropical holothurian sea cucumbers. Comp Biochem. Physiol. B 2013, 166, 182-193.
70. Van Dyck, S.; Caulier, G.; Todesco, M.; Gerbaux, P.; Fournier, I.; Wisztorski, M.; Flammang, P. The triterpene glycosides of Holothuria forskali: Usefulness and efficiency as a chemical defense mechanism against predatory fish. J. Exp. Biol. 2011, 214, 1347-1356.
71. Kalyani, G. A.; Kakrani, H. K. N.; Hukkeri, V. I. Holothurin-A Review. Indian J. Nat. Prod. 1988, 4, 3-8.
72. Kobayashi, M.; Hori, M.; Kan, K.; Yasuzawa, T.; Matsui, M.; Suzuki, S.; Kitagawa, I. Marine natural products. XXVII: Distribution of lanostane-type triterpene oligoglycosides in ten kinds of Okinawan Sea cucumbers. Chem. Pharm. Bull. 1991, 39, 2282-2287.
73. Kalinin, V.; Anisimov, M.; Prokofieva, N.; Avilov, S.; Afiyatullov, S. S.; Stonik, V. Biological activities and biological role of triterpene glycosides from holothuroids (Echinodermata). Echinoderm Stud. 1996, 5, 139-181.
74. Kalinin, V. I.; Prokofieva, N. G.; Likhatskaya, G. N.; Schentsova, E. B.; Agafonova, I. G.; Avilov, S. A.; Drozdova, O. A. Hemolytic activities of triterpene glycosides from the holothurian order Dendrochirotida: Some trends in the evolution of this group of toxins. Toxicon 1996, 34, 475-483.
75. Mercier, A.; Sims, D. W.; Hamel, J. F. Advances in Marine Biology: Endogenous and Exogenous Control of Gametogenesis and Spawning in Echinoderms; Academic Press: New York, NY, USA, 2009; Volume 55.
76. Massin, C; Uthicke, S.; Purcell, S. W.; Rowe, F. W. E.; Samyn, Y. Taxonomy of the heavily exploited Indo-Pacific sandfish complex (Echinodermata: Holothuriidae). Zool. J. Linn. Soc. 2009, 155, 40-59.
77. Van Dyck, S.; Gerbaux, P.; Flammang, P. Elucidation of molecular diversity and body distribution of saponins in the sea cucumber Holothuria forskali (Echinodermata) by mass spectrometry. Comp. Biochem. Physiol. B 2009, 152, 124-134.
78. Matsuno, T.; Ishida, T. Distribution and seasonal variation of toxic principles of sea-cucumber (Holothuria leucospilota; Brandt). Cell. Mol. Life Sci. 1969, 25, 1261.
79. Elyakov, G. B.; Stonik, V. A.; Levina, E. V.; Slanke, V. P.; Kuznetsova, T. A.; Levin, V. S. Glycosides of marine invertebrates-I. A comparative study of the glycoside fractions of pacific sea cucumbers. Comp. Biochem. Physiol. B 1973, 44, 325-336.
80. Schöpke, T.; Thiele, H.; Wray, V.; Nimtz, M.; Hiller, K. Structure elucidation of a glycoside of 2β, 3β, t23-trihydroxy-16-oxoolean-12-en-28-oic acid from bellis bernardii using mass spectrometry for the sugar sequence determination. J. Nat. Prod. 1995, 58, 152-155.
81. Cui, M.; Song, F.; Zhou, Y.; Liu, Z.; Liu, S. Rapid identification of saponins in plant extracts by electrospray ionization multI-stage tandem mass spectrometry and liquid chromatography/tandem mass spectrometry. Rapid Commun. Mass Spectrom. 2000, 14, 1280-1286.
82. Liu, S.; Cui, M.; Liu, Z.; Song, F.; Mo, W. Structural analysis of saponins from medicinal herbs using electrospray ionization tandem mass spectrometry. J. Am. Soc. Mass Spectrom. 2004, 15, 133-141.
83. Wang, X.; Sakuma, T.; Asafu-Adjaye, E.; Shiu, G. K. Determination of ginsenosides in plant extracts from Panax ginseng and Panax quinquefolius L. by LC/MS/MS. Anal. Chem. 1999, 71, 1579-1584.
84. Wolfender, J. L.; Rodriguez, S.; Hostettmann, K. Liquid chromatography coupled to mass spectrometry and nuclear magnetic resonance spectroscopy for the screening of plant constituents. J. Chromatogr. 1998, 794, 299-316.
85. Bankefors, J.; Broberg, S.; Nord, L. I.; Kenne, L. Electrospray ionization ion-trap multiple-stage mass spectrometry of Quillaja saponins. J. Mass Spectrom. 2011, 46, 658-665.
86. 21 steroidal saponins in Cynanchum versicolor Bunge by electrospray ionization multi-stage tandem mass spectrometry and liquid chromatography/tandem mass spectrometry. Rapid Commun. Mass Spectrom. 2007, 21, 279-285.
87. Song, F.; Cui, M.; Liu, Z.; Yu, B.; Liu, S. Multiple-stage tandem mass spectrometry for differentiation of isomeric saponins. Rapid Commun. Mass Spectrom. 2004, 18, 2241-2248.
88. Van Setten, D. C.; Jan ten Hove, G.; Wiertz, E. J. H. J.; Kamerling, J. P.; van de Werken, G. Multiple-stage tandem mass spectrometry for structural characterization of saponins. Anal. Chem. 1998, 70, 4401-4409.
89. Rodriguez, J.; Castro, R.; Riguera, R. Holothurinosides: New antitumour non sulphated triterpenoid glycosides from the sea cucumber holothuria forskalii. Tetrahedron 1991, 47, 4753-4762.
90. Kitagawa, I.; Kobayashi, M.; Kyogoku, Y. Marine natural products. IX. Structural elucidation of triterpenoidal oligoglycosides from the Bahamean sea cucumber Actinopyga agassizi Selenka. Chem. Pharm. Bull. (Tokyo) 1982, 30, 2045-2050.
91. Liu, B. S.; Yi, Y. H.; Li, L.; Sun, P.; Han, H.; Sun, G. Q.; Wang, X. H.; Wang, Z. L. Argusides D and E, two new cytotoxic triterpene glycosides from the sea cucumber Bohadschia argus Jaeger. Chem. Biodivers. 2008, 5, 1425-1433.
92. Van Dyck, S.; Flammang, P.; Meriaux, C.; Bonnel, D.; Salzet, M.; Fournier, I.; Wisztorski, M. Localization of secondary metabolites in marine invertebrates: Contribution of MALDI MSI for the study of saponins in Cuvierian tubules of H. forskali. PLoS One 2010, 5, e13923.
93. Wu, J.; Yi, Y.; Zou, Z. Two new triterpene glycosides from sea cucumber Holothuria nobilis. Chin. Tradit. Herbal Drugs 2006, 37, 497.
94. Han, H.; Yi, Y. H.; Li, L.; Liu, B. S.; La, M. P.; Zhang, H. W. Antifungal active triterpene glycosides from sea cucumber Holothuria scabra. Acta Pharm. Sin. 2009, 44, 620-624.
95. Han, H.; Li, L.; Yi, Y.-h.; Wang, X.-h.; Pan, M.-x. Triterpene glycosides from sea cucumber Holothuria scabra with cytotoxic activity. Chin. Herb. Med. 2012, 4, 183-188.
96. Kitagawa, I.; Nishino, T.; Kyogoku, Y. Structure of holothurin A a biologically active triterpene-oligoglycoside from the sea cucumber Holothuria leucospilota Brandt. Tetrahedron Lett. 1979, 20, 1419-1422.
97. Thanh, N. V.; Dang, N. H.; Kiem, P. V.; Cuong, N. X.; Huong, H. T.; Minh, C. V. A new triterpene glycoside from the sea cucumber Holothuria scabra collected in Vietnam. ASEAN J. Sci. Technol. Dev. 2006, 23, 253-259.
98. Yuan, W.; Yi, Y.; Tang, H.; Xue, M.; Wang, Z.; Sun, G.; Zhang, W.; Liu, B.; Li, L.; Sun, P. Two new holostan-type triterpene glycosides from the sea cucumber Bohadschia marmorata JAEGER. Chem. Pharm. Bull. (Tokyo) 2008, 56, 1207-1211.
99. Chanley, J. D.; Ledeen, R.; Wax, J.; Nigrelli, R. F.; Sobotka, H. Holothurin. I. The isolation, properties and sugar components of holothurin A. J. Am. Chem. Soc. 1959, 81, 5180-5183.
100. Elyakov, G. B.; Kuznetsova, T. A.; Stonik, V. A.; Levin, V. S.; Albores, R. Glycosides of marine invertebrates. IV. A comparative study of the glycosides from Cuban sublittoral holothurians. Comp. Biochem. Physiol. B 1975, 52, 413-417.
101. Yasumoto, T.; Nakamura, K.; Hashimoto, Y. A new saponin, holothurin B, isolated from sea-cucumber, Holothuria vagabunda and Holothuria lubrica. Agric. Biol. Chem. 1967, 31, 7-10.
102. Matsuno, T.; Iba, J. Studies on the saponins of the sea cucumber. Yakugaku Zasshi 1966, 86, 637-638.
103. 4, new triterpene glycosides from mediterranean sea cucumbers of the genus holothuria. J. Nat. Prod. 2005, 68, 564-567.
104. Sun, G. Q.; Li, L.; Yi, Y. H.; Yuan, W. H.; Liu, B. S.; Weng, Y. Y.; Zhang, S. L.; Sun, P.; Wang, Z. L. Two new cytotoxic nonsulfated pentasaccharide holostane (=20-hydroxylanostan-18-oic acid γ-lactone) glycosides from the sea cucumber Holothuria grisea. Helv. Chim. Acta 2008, 91, 1453-1460.
105. Zou, Z.; Yi, Y.; Wu, H.; Yao, X.; Du, L.; Jiuhong, W.; Liaw, C. C.; Lee, K. H. Intercedensides D-I, cytotoxic triterpene glycosides from the sea cucumber Mensamaria intercedens Lampert. J. Nat. Prod. 2005, 68, 540-546.
106. Sottorff, I.; Aballay, A.; Hernández, V.; Roa, L.; Muñoz, L. X.; Silva, M.; Becerra, J.; Astuya, A. Characterization of bioactive molecules isolated from sea cucumber Athyonidium chilensis. Rev. Biol. Mar. Oceanogr. 2013, 48, 23-35.
107. 2 and D, six new triterpene glycosides from the sea cucumber Cladolabes schmeltzii. Nat. Prod. Commun. 2013, 8, 1527-1534.
108. 4 from the sea cucumber Eupentacta fraudatrix. Nat. Prod. Res. 2012, 26, 1765-1774.
109. Kupchan, S. M.; Britton, R. W.; Ziegler, M. F.; Sigel, C. W. Bruceantin, a new potent antileukemic simaroubolide from Brucea antidysenterica. J. Org. Chem. 1973, 38, 178-179.
110. Oleszek, W.; Marston, A. Saponins in Food, Feedstuffs and Medicinal Plants; Springer: Dordrecht, The Netherlands, 2000; Volume 45.