User menu

Accès à distance ? S'identifier sur le proxy UCLouvain

The amphiphilic nature of saponins and their effects on artificial and biological membranes and potential consequences for red blood and cancer cells

Primary tabs

download
  • Open access
  • PDF
  • 2.30 M
Lorent, Joseph H. [UCL] Quetin-Leclercq, Joëlle [UCL] Mingeot-Leclercq, Marie-Paule [UCL]

Saponins, amphiphiles of natural origin with numerous biological activities, are widely used in the cosmetic and pharmaceutical industry. Some saponins exhibit relatively selective cytotoxic effects on cancer cells but the tendency of saponins to induce hemolysis limits their anticancer potential. This review focused on the effects of saponin activity on membranes and consequent implications for red blood and cancer cells. This activity seems to be strongly related to the amphiphilic character of saponins that gives them the ability to self-aggregate and interact with membrane components such as cholesterol and phospholipids. Membrane interactions of saponins with artificial membrane models, red blood and cancer cells are reviewed with respect to their molecular structures. The review considered the mechanisms of these membrane interactions and their consequences including the modulation of membrane dynamics, interaction with membrane rafts, and membrane lysis. We summarized current knowledge concerning the mechanisms involved in the interactions of saponins with membrane lipids and examined the structure activity relationship of saponins regarding hemolysis and cancer cell death. A critical analysis of these findings speculates on their potential to further develop new anticancer compounds.

Document type Article de périodique (Journal article) – Synthèse de littérature
Access type Accès libre
Publication date 2014
Language Anglais
Journal information "Organic & Biomolecular Chemistry" - Vol. 12, no.44, p. 8803-8822 (2014)
Peer reviewed yes
Publisher Royal Society of Chemistry ((United Kingdom) Cambridge)
issn 1477-0520
e-issn 1477-0539
Publication status Publié
Affiliation UCL - SSS/LDRI - Louvain Drug Research Institute
Links
  1. Abe H., Konishi H., Komiya H., Arichi S., Effects of Saikosaponins on Biological Membranes, 10.1055/s-2007-971655
  2. Afrose Sadia, Hossain Md. S., Maki Takaaki, Tsujii Hirotada, Karaya root saponin exerts a hypocholesterolemic response in rats fed a high-cholesterol diet, 10.1016/j.nutres.2009.05.008
  3. Akiyama Toshiyuki, Takagi Shigekazu, Sankawa Ushio, Inari Shoji, Saito Hazime, Saponin-cholesterol interaction in the multibilayers of egg yolk lecithin as studied by deuterium nuclear magnetic resonance: digitonin and its analogs, 10.1021/bi00550a027
  4. Armah C.N., Mackie A.R., Roy C., Price K., Osbourn A.E., Bowyer P., Ladha S., The Membrane-Permeabilizing Effect of Avenacin A-1 Involves the Reorganization of Bilayer Cholesterol, 10.1016/s0006-3495(99)77196-1
  5. Ashworth L. A. E., Green C., Plasma Membranes: Phospholipid and Sterol Content, 10.1126/science.151.3707.210
  6. Assa Y., Shany S., Gestetner B., Tencer Y., Birk Y., Bondi A., Interaction of alfalfa saponins with components of the erythrocyte membrane in hemolysis, 10.1016/0005-2736(73)90027-8
  7. Augustin Jörg M., Kuzina Vera, Andersen Sven B., Bak Søren, Molecular activities, biosynthesis and evolution of triterpenoid saponins, 10.1016/j.phytochem.2011.01.015
  8. Bachran Christopher, Bachran Silke, Sutherland Mark, Bachran Diana, Fuchs Hendrik, Saponins in Tumor Therapy, 10.2174/138955708784534445
  9. Balakrishnan S., Varughese S., Deshpande A. P., Micellar Characterisation of Saponin fromSapindus Mukorossi, 10.3139/113.100315
  10. BANGHAM A. D., HORNE R. W., Action of Saponin on Biological Cell Membranes, 10.1038/196952a0
  11. Barros L F, Kanaseki T, Sabirov R, Morishima S, Castro J, Bittner C X, Maeno E, Ando-Akatsuka Y, Okada Y, Apoptotic and necrotic blebs in epithelial cells display similar neck diameters but different kinase dependency, 10.1038/sj.cdd.4401236
  12. Baumann Eckehard, Stoya Gudrun, Völkner Andreas, Richter Walter, Lemke Cornelius, Linss Werner, Hemolysis of human erythrocytes with saponin affects the membrane structure, 10.1078/0065-1281-00534
  13. Becher Anja, White Julia H., McIlhinney R. A. Jeffrey, The γ-aminobutyric acid receptor B, but not the metabotropic glutamate receptor type-1, associates with lipid rafts in the rat cerebellum : GABAB receptor associates with rafts, 10.1046/j.1471-4159.2001.00614.x
  14. Böttger Stefan, Hofmann Katja, Melzig Matthias F., Saponins can perturb biologic membranes and reduce the surface tension of aqueous solutions: A correlation?, 10.1016/j.bmc.2012.03.032
  15. British Standard Institution , Nanoparticles – Vocabulary , PAS 71:2011BSI Standards Publication , London, UK , 2011
  16. J. Bruneton , Pharmacognosie, Phytochimie, Plantes Médicinales , Lavoisier , Paris , 4 edn, 2009
  17. Cao, Zhongguo Zhongyao Zazhi, 35, 439 (2010)
  18. Cerneus, J. Biol. Chem., 268, 3150 (1993)
  19. Chaigne-Delalande Benjamin, Moreau Jean-François, Legembre Patrick, Rewinding the DISC, 10.1007/s00005-008-0002-9
  20. Choi Jung-Hye, Lee Heon-Woo, Park Hee-Juhn, Kim Sung-Hoon, Lee Kyung-Tae, Kalopanaxsaponin A induces apoptosis in human leukemia U937 cells through extracellular Ca2+ influx and caspase-8 dependent pathways, 10.1016/j.fct.2008.08.026
  21. Chu Patrick, Sadullah Shalal, The current role of amphotericin B lipid complex in managing systemic fungal infections, 10.1185/03007990903379077
  22. Chwalek Martin, Lalun Nathalie, Bobichon Hélène, Plé Karen, Voutquenne-Nazabadioko Laurence, Structure–activity relationships of some hederagenin diglycosides: Haemolysis, cytotoxicity and apoptosis induction, 10.1016/j.bbagen.2006.05.004
  23. Ciechomska Iwona A., Tolkovsky Aviva M., Non-Autophagic GFP-LC3 Puncta Induced by Saponin and Other Detergents, 10.4161/auto.4843
  24. Coleman Jeffrey J., Okoli Ikechukwu, Tegos George P., Holson Edward B., Wagner Florence F., Hamblin Michael R., Mylonakis Eleftherios, Characterization of Plant-Derived Saponin Natural Products againstCandida albicans, 10.1021/cb900243b
  25. Dai Xingxing, Shi Xinyuan, Yin Qianqian, Ding Haiou, Qiao Yanjiang, Multiscale study on the interaction mechanism between ginsenoside biosurfactant and saikosaponin a, 10.1016/j.jcis.2013.01.017
  26. Daines Alison M., Greatrex Ben W., Hayman Colin M., Hook Sarah M., McBurney Warren T., Rades Thomas, Rendle Phillip M., Sims Ian M., Mannosylated saponins based on oleanolic and glycyrrhizic acids. Towards synthetic colloidal antigen delivery systems, 10.1016/j.bmc.2009.05.043
  27. Danloy S., Quetin-Leclercq J., Coucke P., De Pauw-Gillet M.-Cl., Elias R., Balansard G., Angenot L., Bassleer R., Effects of α-Hederin, a Saponin Extracted from Hedera helix, on Cells Culturedin vitro, 10.1055/s-2006-959406
  28. de Ven H. Van, Van Dyck L., Weyenberg W., Maes L., Ludwig A., Nanosuspensions of chemically modified saponins: Reduction of hemolytic side effects and potential tool in drug targeting strategy, 10.1016/j.jconrel.2010.07.093
  29. Demana Patrick H., Davies Nigel M., Hook Sarah, Rades Thomas, Analysis of Quil A–phospholipid mixtures using drift spectroscopy, 10.1016/j.ijpharm.2007.04.030
  30. Demana Patrick H, Davies Nigel M, Vosgerau Uwe, Rades Thomas, Pseudo-ternary phase diagrams of aqueous mixtures of Quil A, cholesterol and phospholipid prepared by the lipid-film hydration method, 10.1016/j.ijpharm.2003.10.020
  31. Detmers Patricia A, Patel Sushma, Hernandez Melba, Montenegro Judy, Lisnock JeanMarie, Pikounis Bill, Steiner Mark, Kim Dooseop, Sparrow Carl, Chao Yu-Sheng, Wright Samuel D, A target for cholesterol absorption inhibitors in the enterocyte brush border membrane, 10.1016/s1388-1981(00)00068-8
  32. Dickens Laura S., Powley Ian R., Hughes Michelle A., MacFarlane Marion, The ‘complexities’ of life and death: Death receptor signalling platforms, 10.1016/j.yexcr.2012.04.005
  33. Dinda Biswanath, Debnath Sudhan, Mohanta Bikas Chandra, Harigaya Yoshihiro, Naturally Occurring Triterpenoid Saponins, 10.1002/cbdv.200800070
  34. Elias P M, Friend D S, Goerke J, Membrane sterol heterogeneity. Freeze-fracture detection with saponins and filipin., 10.1177/27.9.479568
  35. Ellington A. A., Induction of macroautophagy in human colon cancer cells by soybean B-group triterpenoid saponins, 10.1093/carcin/bgh297
  36. Francis George, Kerem Zohar, Makkar Harinder P. S., Becker Klaus, The biological action of saponins in animal systems: a review, 10.1079/bjn2002725
  37. Fukuda Kayoko, Utsumi Hideo, Soda Seiji, Shoji Junzo, Hamada Akira, Specific interaction of arabinose residue in ginsenoside with egg phosphatidylcholine vesicles, 10.1016/0005-2736(87)90341-5
  38. Gajate Consuelo, Mollinedo Faustino, Lipid Rafts and Fas/CD95 Signaling in Cancer Chemotherapy, 10.2174/157489211796957766
  39. Galluzzi L, Vitale I, Abrams J M, Alnemri E S, Baehrecke E H, Blagosklonny M V, Dawson T M, Dawson V L, El-Deiry W S, Fulda S, Gottlieb E, Green D R, Hengartner M O, Kepp O, Knight R A, Kumar S, Lipton S A, Lu X, Madeo F, Malorni W, Mehlen P, Nuñez G, Peter M E, Piacentini M, Rubinsztein D C, Shi Y, Simon H-U, Vandenabeele P, White E, Yuan J, Zhivotovsky B, Melino G, Kroemer G, Molecular definitions of cell death subroutines: recommendations of the Nomenclature Committee on Cell Death 2012, 10.1038/cdd.2011.96
  40. Gao Jian, Li Xia, Gu Guofeng, Sun Bin, Cui Min, Ji Mei, Lou Hong-Xiang, Efficient synthesis of trisaccharide saponins and their tumor cell killing effects through oncotic necrosis, 10.1016/j.bmcl.2010.12.046
  41. Gauthier Charles, Legault Jean, Girard-Lalancette Karl, Mshvildadze Vakhtang, Pichette André, Haemolytic activity, cytotoxicity and membrane cell permeabilization of semi-synthetic and natural lupane- and oleanane-type saponins, 10.1016/j.bmc.2009.01.022
  42. K. Gawrisch , The Dynamics of Membrane Lipids , CRC Press LLC , Boca Raton , 2005 , ch. 4, pp. 147–171
  43. George Kimberly S., Wu Shiyong, Lipid raft: A floating island of death or survival, 10.1016/j.taap.2012.01.007
  44. Gerkens, Anticancer Res., 27, 2529 (2007)
  45. Gilabert-Oriol Roger, Mergel Katharina, Thakur Mayank, von Mallinckrodt Benedicta, Melzig Matthias F., Fuchs Hendrik, Weng Alexander, Real-time analysis of membrane permeabilizing effects of oleanane saponins, 10.1016/j.bmc.2013.01.061
  46. Gögelein Heinz, Hüby Afra, Interaction of saponin and digitonin with black lipid membranes and lipid monolayers, 10.1016/0005-2736(84)90547-9
  47. Guan Fuqin, Shan Yu, Zhao Xingzeng, Zhang Dongmei, Wang Ming, Peng Feng, Xia Bing, Feng Xu, Apoptosis and membrane permeabilisation induced by macranthoside B on HL-60 cells, 10.1080/14786411003752086
  48. Guo Lian Yu, Joo Eun Ji, Son Kun Ho, Jeon Su Jin, Jang Sehyun, Shin Eun Myoung, Zhou Hong Yu, Kim Yeong Shik, Cimiside E arrests cell cycle and induces cell apoptosis in gastric cancer cells, 10.1007/s12272-009-2007-2
  49. Harada Shinji, The broad anti-viral agent glycyrrhizin directly modulates the fluidity of plasma membrane and HIV-1 envelope, 10.1042/bj20051069
  50. Haridas Valsala, Li Xiaoxian, Mizumachi Takatsugu, Higuchi Masahiro, Lemeshko Viktor V., Colombini Marco, Gutterman Jordan U., Avicins, a novel plant-derived metabolite lowers energy metabolism in tumor cells by targeting the outer mitochondrial membrane, 10.1016/j.mito.2006.12.005
  51. HASE JUNICHI, KOBASHI KYOICHI, MITSUI KENICHIRO, NAMBA TSUNEO, YOSHIZAKI MASAO, TOMIMORI TSUYOSHI, The structure-hemolysis relationship of oleanolic acid derivatives and inhibition of the saponin-induced hemolysis with sapogenins., 10.1248/bpb1978.4.833
  52. Haslam Ruth M., Klyne W., The precipitation of 3β-hydroxysteroids by digitonin, 10.1042/bj0550340
  53. Haslewood G. A. D., Precipitation of steroid ketones with digitonin, 10.1042/bj0410639
  54. Heffer-Lauc Marija, Viljetić Barbara, Vajn Katarina, Schnaar Ronald L., Lauc Gordan, Effects of Detergents on the Redistribution of Gangliosides and GPI-anchored Proteins in Brain Tissue Sections, 10.1369/jhc.7a7195.2007
  55. Heiner Anne L., Gibbons Elizabeth, Fairbourn Jeremy L., Gonzalez Laurie J., McLemore Chisako O., Brueseke Taylor J., Judd Allan M., Bell John D., Effects of Cholesterol on Physical Properties of Human Erythrocyte Membranes: Impact on Susceptibility to Hydrolysis by Secretory Phospholipase A2, 10.1529/biophysj.107.118356
  56. Hu, Nanoparticulate Quillaja saponin induces apoptosis in human leukemia cell lines with a high therapeutic index, 10.2147/ijn.s7879
  57. Hu Mei, Konoki Keiichi, Tachibana Kazuo, Cholesterol-independent membrane disruption caused by triterpenoid saponins, 10.1016/0005-2760(95)00214-6
  58. Hunter Douglas R., Haworth Robert A., The Ca2+-induced membrane transition in mitochondria, 10.1016/0003-9861(79)90371-0
  59. Hunter Douglas R., Haworth Robert A., The Ca2+-induced membrane transition in mitochondria, 10.1016/0003-9861(79)90373-4
  60. ILANGUMARAN Subburaj, HOESSLI Daniel C., Effects of cholesterol depletion by cyclodextrin on the sphingolipid microdomains of the plasma membrane, 10.1042/bj3350433
  61. INAMITSU Tetsuaki, OHTSUKI Iwao, Characterization of ATP-dependent Ca2+ uptake by canine brain microsomes with saponin, 10.1111/j.1432-1033.1984.tb08529.x
  62. Ioffe D V, Sterols as Complex-forming Species, 10.1070/rc1986v055n02abeh003177
  63. Ishida Hideyuki, Hirota Yuki, Nakazawa Hiroe, Effect of sub-skinning concentrations of saponin on intracellular Ca2+ and plasma membrane fluidity in cultured cardiac cells, 10.1016/0005-2736(93)90381-9
  64. J. N. Israelachvili , Intermolecular and Surface Forces , Academic Press, Elsevier , Amsterdam , 3rd edn, 2011
  65. Israelachvili Jacob N., Mitchell D.John, Ninham Barry W., Theory of self-assembly of lipid bilayers and vesicles, 10.1016/0005-2736(77)90099-2
  66. Jacobson Ken, Mouritsen Ole G., Anderson Richard G. W., Lipid rafts: at a crossroad between cell biology and physics, 10.1038/ncb0107-7
  67. Jian Hong-lei, Liao Xiao-xia, Zhu Li-wei, Zhang Wei-ming, Jiang Jian-xin, Synergism and foaming properties in binary mixtures of a biosurfactant derived from Camellia oleifera Abel and synthetic surfactants, 10.1016/j.jcis.2011.04.038
  68. Jiang, Int. J. Mol. Med., 26, 787 (2010)
  69. Jin Zhaoyu, El-Deiry Wafik S., Overview of cell death signaling pathways, 10.4161/cbt.4.2.1508
  70. Jones PJH, MacDougall D E, Ntanios F, Vanstone C A, Dietary phytosterols as cholesterol-lowering agents in humans, 10.1139/y97-011
  71. Kersten Gideon F.A., Crommelin Daan J.A., Liposomes and ISCOMS as vaccine formulations, 10.1016/0304-4157(95)00002-9
  72. Keukens Erik A.J., de Vrije Truus, van den Boom Claudia, de Waard Pieter, Plasman Henk H., Thiel Felix, Chupin Vladimir, Jongen Wim M.F., de Kruijff Ben, Molecular basis of glycoalkaloid induced membrane disruption, 10.1016/0005-2736(95)00186-7
  73. King Frank W., Fong Sylvia, Griffin Chandi, Shoemaker Mark, Staub Rick, Zhang Yan-Ling, Cohen Isaac, Shtivelman Emma, Timosaponin AIII Is Preferentially Cytotoxic to Tumor Cells through Inhibition of mTOR and Induction of ER Stress, 10.1371/journal.pone.0007283
  74. KO Hyeonseok, KIM Young-Joo, PARK Jin-Soo, PARK Jeong Hill, YANG Hyun Ok, Autophagy Inhibition Enhances Apoptosis Induced by Ginsenoside Rk1 in Hepatocellular Carcinoma Cells, 10.1271/bbb.90250
  75. Kostetsky Eduard Y, Sanina Nina M, Mazeika Andrey N, Tsybulsky Alexander V, Vorobyeva Natalia S, Shnyrov Valery L, Tubular immunostimulating complex based on cucumarioside A2-2 and monogalactosyldiacylglycerol from marine macrophytes, 10.1186/1477-3155-9-35
  76. Kowaltowski Alicia J., Castilho Roger F., Vercesi Anibal E., Opening of the mitochondrial permeability transition pore by uncoupling or inorganic phosphate in the presence of Ca2+is dependent on mitochondrial-generated reactive oxygen species, 10.1016/0014-5793(95)01449-7
  77. Kroemer G., Galluzzi L., Brenner C., Mitochondrial Membrane Permeabilization in Cell Death, 10.1152/physrev.00013.2006
  78. Kroemer G, Galluzzi L, Vandenabeele P, Abrams J, Alnemri E S, Baehrecke E H, Blagosklonny M V, El-Deiry W S, Golstein P, Green D R, Hengartner M, Knight R A, Kumar S, Lipton S A, Malorni W, Nuñez G, Peter M E, Tschopp J, Yuan J, Piacentini M, Zhivotovsky B, Melino G, Classification of cell death: recommendations of the Nomenclature Committee on Cell Death 2009, 10.1038/cdd.2008.150
  79. Kumar, Int. J. Mol. Med., 24, 381 (2009)
  80. Kwon Hyog-Young, Kim Eun-Hye, Kim Seung-Whan, Kim Su-Nam, Park Jong-Dae, Rhee Dong-Kwon, Selective toxicity of ginsenoside Rg3 on multidrug resistant cells by membrane fluidity modulation, 10.1007/s12272-001-1137-y
  81. Lange Yvonne, Ye Jin, Duban Mark-Eugene, Steck Theodore L., Activation of Membrane Cholesterol by 63 Amphipaths, 10.1021/bi900951r
  82. Lange Yvonne, Ye Jin, Steck Theodore L., Activation of Membrane Cholesterol by Displacement from Phospholipids, 10.1074/jbc.m507149200
  83. Launikonis B. S., Stephenson D. George, Effects of β-escin and saponin on the transverse-tubular system and sarcoplasmic reticulum membranes of rat and toad skeletal muscle, 10.1007/s004240050867
  84. Lee, Mol. Cell. Biomech., 3, 185 (2006)
  85. Legembre P., Daburon S., Moreau P., Ichas F., de Giorgi F., Moreau J.-F., Taupin J.-L., Amplification of Fas-Mediated Apoptosis in Type II Cells via Microdomain Recruitment, 10.1128/mcb.25.15.6811-6820.2005
  86. Lemeshko Victor V., Haridas Valsala, Quijano Pérez Jairo C., Gutterman Jordan U., Avicins, natural anticancer saponins, permeabilize mitochondrial membranes, 10.1016/j.abb.2006.08.008
  87. Leung Yuk-Man, Ou Yi-Jun, Kwan Chiu-Yin, Loh Tatt-Tuck, Specific interaction between tetrandrine and Quillaja saponins in promoting permeabilization of plasma membrane in human leukemic HL-60 cells, 10.1016/s0005-2736(97)00002-3
  88. Levin S., Korenstein R., Membrane fluctuations in erythrocytes are linked to MgATP-dependent dynamic assembly of the membrane skeleton, 10.1016/s0006-3495(91)82104-x
  89. Li Xiao Xian, Davis Bridgette, Haridas Valsala, Gutterman Jordan U., Colombini Marco, Proapoptotic Triterpene Electrophiles (Avicins) Form Channels in Membranes: Cholesterol Dependence, 10.1529/biophysj.104.049403
  90. Li Ying Chun, Park Mi Jung, Ye Sang-Kyu, Kim Chul-Woo, Kim Yong-Nyun, Elevated Levels of Cholesterol-Rich Lipid Rafts in Cancer Cells Are Correlated with Apoptosis Sensitivity Induced by Cholesterol-Depleting Agents, 10.2353/ajpath.2006.050959
  91. Lin Fu, Wang Renxiao, Hemolytic mechanism of dioscin proposed by molecular dynamics simulations, 10.1007/s00894-009-0523-0
  92. Lin X., Ma L., Racette S. B., Anderson Spearie C. L., Ostlund R. E., Phytosterol glycosides reduce cholesterol absorption in humans, 10.1152/ajpgi.00001.2009
  93. Lingwood D., Simons K., Lipid Rafts As a Membrane-Organizing Principle, 10.1126/science.1174621
  94. Liu Guo-Yu, Bu Xuexian, Yan Hang, Jia William W.-G., 20S-Protopanaxadiol-Induced Programmed Cell Death in Glioma Cells through Caspase-Dependent and -Independent Pathways, 10.1021/np060313t
  95. Liu Wei, Huang Xue-Feng, Qi Qi, Dai Qin-Sheng, Yang Li, Nie Fei-Fei, Lu Na, Gong Dan-Dan, Kong Ling-Yi, Guo Qing-Long, Asparanin A induces G2/M cell cycle arrest and apoptosis in human hepatocellular carcinoma HepG2 cells, 10.1016/j.bbrc.2009.02.124
  96. London Erwin, How principles of domain formation in model membranes may explain ambiguities concerning lipid raft formation in cells, 10.1016/j.bbamcr.2005.09.002
  97. Lorent Joseph, Le Duff Cécile S., Quetin-Leclercq Joelle, Mingeot-Leclercq Marie-Paule, Induction of Highly Curved Structures in Relation to Membrane Permeabilization and Budding by the Triterpenoid Saponins, α- and δ-Hederin, 10.1074/jbc.m112.407635
  98. Lorent Joseph, Lins Laurence, Domenech Òscar, Quetin-Leclercq Joelle, Brasseur Robert, Mingeot-Leclercq Marie-Paule, Domain Formation and Permeabilization Induced by the Saponin α-Hederin and Its Aglycone Hederagenin in a Cholesterol-Containing Bilayer, 10.1021/la4049902
  99. Madsen Henriette Baun, Ifversen Peter, Madsen Flemming, Brodin Birger, Hausser Ingrid, Nielsen Hanne Mørck, In Vitro Cutaneous Application of ISCOMs on Human Skin Enhances Delivery of Hydrophobic Model Compounds Through the Stratum Corneum, 10.1208/s12248-009-9149-5
  100. Mahapatro Anil, Singh Dinesh K, Biodegradable nanoparticles are excellent vehicle for site directed in-vivo delivery of drugs and vaccines, 10.1186/1477-3155-9-55
  101. Man Shuli, Gao Wenyuan, Zhang Yanjun, Huang Luqi, Liu Changxiao, Chemical study and medical application of saponins as anti-cancer agents, 10.1016/j.fitote.2010.06.004
  102. Mazzucchelli Gabriel D., Cellier Nicolas A., Mshviladzade Vakhtang, Elias Riad, Shim Yong-Ho, Touboul David, Quinton Loïc, Brunelle Alain, Laprévote Olivier, De Pauw Edwin A., De Pauw-Gillet Marie-Claire A., Pores Formation on Cell Membranes by Hederacolchiside A1 Leads to a Rapid Release of Proteins for Cytosolic Subproteome Analysis, 10.1021/pr7006973
  103. Mitra Shuman, Dungan Stephanie R., Micellar Properties of Quillaja Saponin. 1. Effects of Temperature, Salt, and pH on Solution Properties, 10.1021/jf960349z
  104. Mitra Shuman, Dungan Stephanie R, Micellar properties of quillaja saponin. 2. Effect of solubilized cholesterol on solution properties, 10.1016/s0927-7765(99)00088-0
  105. Mitra Shuman, Dungan Stephanie R., Cholesterol Solubilization in Aqueous Micellar Solutions of Quillaja Saponin, Bile Salts, or Nonionic Surfactants, 10.1021/jf000568r
  106. Montero J., Morales A., Llacuna L., Lluis J. M., Terrones O., Basanez G., Antonsson B., Prieto J., Garcia-Ruiz C., Colell A., Fernandez-Checa J. C., Mitochondrial Cholesterol Contributes to Chemotherapy Resistance in Hepatocellular Carcinoma, 10.1158/0008-5472.can-07-6161
  107. Morehouse, J. Lipid Res., 40, 464 (1999)
  108. Myschik Julia, Lendemans Dirk G., McBurney Warren T., Demana Patrick H., Hook Sarah, Rades Thomas, On the preparation, microscopic investigation and application of ISCOMs, 10.1016/j.micron.2006.03.016
  109. Nag Subhasree Ashok, Ginsenosides as anticancer agents: In vitro and in vivo activities, structure–activity relationships, and molecular mechanisms of action, 10.3389/fphar.2012.00025
  110. NANJUNDAN Meera, POSSMAYER Fred, Pulmonary lipid phosphate phosphohydrolase in plasma membrane signalling platforms, 10.1042/bj3580637
  111. Naruse Masahiro, Suetomo Hiroyuki, Matsubara Teruhiko, Sato Toshinori, Yanagawa Hiroshi, Hoshi Motonori, Matsumoto Midori, Acrosome reaction-related steroidal saponin, Co-ARIS, from the starfish induces structural changes in microdomains, 10.1016/j.ydbio.2010.08.019
  112. Nielsen Jens K., Nagao Tsuneatsu, Okabe Hikaru, Shinoda Tetsuro, Resistance in the Plant, Barbarea vulgaris, and Counter-Adaptations in Flea Beetles Mediated by Saponins, 10.1007/s10886-010-9758-6
  113. NISHIKAWA Masahiko, NOJIMA Shoshichi, AKIYAMA Toshiyuki, SANKAWA Ushio, INOUE Keizo, Interaction of Digitonin and Its Analogs with Membrane Cholesterol1, 10.1093/oxfordjournals.jbchem.a134941
  114. Oftedal Linn, Myhren Lene, Jokela Jouni, Gausdal Gro, Sivonen Kaarina, Døskeland Stein Ove, Herfindal Lars, The lipopeptide toxins anabaenolysin A and B target biological membranes in a cholesterol-dependent manner, 10.1016/j.bbamem.2012.07.015
  115. Ohsaki Yuki, Maeda Takashi, Fujimoto Toyoshi, Fixation and permeabilization protocol is critical for the immunolabeling of lipid droplet proteins, 10.1007/s00418-005-0061-5
  116. Okunade A, Natural antimycobacterial metabolites: current status, 10.1016/j.phytochem.2004.02.013
  117. Ota, Cancer Res., 47, 3863 (1987)
  118. Özel Muhsin, Hℷlund Stefan, Gelderblom Hans R., Morein Bror, Quaternary structure of the immunostimulating complex (Iscom), 10.1016/0889-1605(89)90018-9
  119. Papadopoulou K., Melton R. E., Leggett M., Daniels M. J., Osbourn A. E., Compromised disease resistance in saponin-deficient plants, 10.1073/pnas.96.22.12923
  120. Park E-K, Lee EJ, Lee S-H, Koo KH, Sung JY, Hwang EH, Park JH, Kim C-W, Jeong K-C, Park B-K, Kim Y-N, Induction of apoptosis by the ginsenoside Rh2 by internalization of lipid rafts and caveolae and inactivation of Akt : Rh2 affects raft internalization and Akt, 10.1111/j.1476-5381.2010.00768.x
  121. Patra, Biochim. Biophys. Acta, 1785, 182 (2008)
  122. Pillion Dennis J., Amsden Jennifer A., Kensil Charlotte R., Recchia Joanne, Structure—Function Relationship among Quillaja Saponins Serving as Excipients for Nasal and Ocular Delivery of Insulin, 10.1021/js9504651
  123. Popov, Zh. Evol. Biokhim. Fiziol., 39, 244 (2003)
  124. Raffa V., Vittorio O., Riggio C., Cuschieri A., Progress in nanotechnology for healthcare, 10.3109/13645706.2010.481095
  125. Rao, J. Nutr., 125, 717S (1995)
  126. Roddick James G., Complex formation between solanaceous steroidal glycoalkaloids and free sterols in vitro, 10.1016/s0031-9422(00)98476-0
  127. Róg Tomasz, Pasenkiewicz-Gierula Marta, Vattulainen Ilpo, Karttunen Mikko, Ordering effects of cholesterol and its analogues, 10.1016/j.bbamem.2008.08.022
  128. Romussi, Pharmazie, 35, 498 (1980)
  129. Ruckenstein Eli, Li Buqiang, A surface equation of state based on clustering of surfactant molecules of insoluble monolayers, 10.1021/la00009a037
  130. Sakamoto Seiichi, Nakahara Hiromichi, Uto Takuhiro, Shoyama Yukihiro, Shibata Osamu, Investigation of interfacial behavior of glycyrrhizin with a lipid raft model via a Langmuir monolayer study, 10.1016/j.bbamem.2013.01.006
  131. Sarnthein-Graf Carlo, La Mesa Camillo, Association of saponins in water and water–gelatine mixtures, 10.1016/j.tca.2003.11.044
  132. Scheidt Holger A., Huster Daniel, Gawrisch Klaus, Diffusion of Cholesterol and Its Precursors in Lipid Membranes Studied by 1H Pulsed Field Gradient Magic Angle Spinning NMR, 10.1529/biophysj.105.062018
  133. Schroeder Avi, Heller Daniel A., Winslow Monte M., Dahlman James E., Pratt George W., Langer Robert, Jacks Tyler, Anderson Daniel G., Treating metastatic cancer with nanotechnology, 10.1038/nrc3180
  134. Schroeder Roxann J., Ahmed Sharmin N., Zhu Yongze, London Erwin, Brown Deborah A., Cholesterol and Sphingolipid Enhance the Triton X-100 Insolubility of Glycosylphosphatidylinositol-anchored Proteins by Promoting the Formation of Detergent-insoluble Ordered Membrane Domains, 10.1074/jbc.273.2.1150
  135. Seeman P., TRANSIENT HOLES IN THE ERYTHROCYTE MEMBRANE DURING HYPOTONIC HEMOLYSIS AND STABLE HOLES IN THE MEMBRANE AFTER LYSIS BY SAPONIN AND LYSOLECITHIN, 10.1083/jcb.32.1.55
  136. Seeman P., STRUCTURE OF MEMBRANE HOLES IN OSMOTIC AND SAPONIN HEMOLYSIS, 10.1083/jcb.56.2.519
  137. Segal Ruth, Mansour M., Zaitschek D.V., Effect of ester groups on the haemolytic action of some saponins and sapogenins, 10.1016/0006-2952(66)90185-7
  138. Segal Ruth, Milo-Goldzweig Ilana, On the mechanism of saponin hemolysis—II, 10.1016/0006-2952(75)90317-2
  139. Segal Ruth, Milo-Goldzweig Ilana, The susceptibility of cholesterol-depleted erythrocytes to saponin and sapogenin hemolysis, 10.1016/0005-2736(78)90233-x
  140. Segal Ruth, Shatkovsky Puah, Milo-Goldzweig Ilana, On the mechanism of saponin hemolysis—I, 10.1016/0006-2952(74)90027-6
  141. Sehgal Pravin B., Guo Gary G., Shah Mehul, Kumar Vinita, Patel Kirit, Cytokine Signaling : STATS IN PLASMA MEMBRANE RAFTS, 10.1074/jbc.m200018200
  142. Shany Shraga, Bernheimer Alan W., Grushoff Phyllis S., Kim Kwang-Shin, Evidence for membrane cholesterol as the common binding site for cereolysin, streptolysin O and saponin, 10.1007/bf01686643
  143. Sidhu G. S., Oakenfull D. G., A mechanism for the hypocholesterolaemic activity of saponins, 10.1079/bjn19860070
  144. Sleep John, Wilson David, Simmons Robert, Gratzer Walter, Elasticity of the Red Cell Membrane and Its Relation to Hemolytic Disorders: An Optical Tweezers Study, 10.1016/s0006-3495(99)77139-0
  145. Song Saisai, Zhu Lizhong, Zhou Wenjun, Simultaneous removal of phenanthrene and cadmium from contaminated soils by saponin, a plant-derived biosurfactant, 10.1016/j.envpol.2008.06.018
  146. Song Xiaoming, Zang Liming, Hu Songhua, Amplified immune response by ginsenoside-based nanoparticles (ginsomes), 10.1016/j.vaccine.2009.02.040
  147. Stanimirova R., Marinova K., Tcholakova S., Denkov N. D., Stoyanov S., Pelan E., Surface Rheology of Saponin Adsorption Layers, 10.1021/la202860u
  148. Stine Keith J., Hercules Rachel K., Duff Joy D., Walker Barry W., Interaction of the Glycoalkaloid Tomatine with DMPC and Sterol Monolayers Studied by Surface Pressure Measurements and Brewster Angle Microscopy†, 10.1021/jp056139j
  149. Stohlman E. F., Smith Maurice I., Experimental Saponin Anemia in the Albino Rat, 10.2307/4581221
  150. Sun Hong-Xiang, Xie Yong, Ye Yi-Ping, Advances in saponin-based adjuvants, 10.1016/j.vaccine.2009.01.091
  151. Sun Hong-Xiang, Xie Yong, Ye Yi-Ping, ISCOMs and ISCOMATRIX™, 10.1016/j.vaccine.2009.05.032
  152. Sung M.-K., Kendall C.W.C., Rao A.V., Effect of soybean saponins and gypsophila saponin on morphology of colon carcinoma cells in culture, 10.1016/0278-6915(95)00007-o
  153. Huat Benny Tan Kwong, Swamy S. Muthu Kumara, 10.1023/a:1022807207948
  154. Sy L.-K., Yan S.-C., Lok C.-N., Man R. Y.K., Che C.-M., Timosaponin A-III Induces Autophagy Preceding Mitochondria-Mediated Apoptosis in HeLa Cancer Cells, 10.1158/0008-5472.can-08-1983
  155. Tadros, J. Egypt. Soc. Parasitol., 38, 585 (2008)
  156. Takechi Masayuki, Shimada Shigetoshi, Tanaka Yasuo, Time Course and Inhibition of Saponin-Induced Hemolysis, 10.1055/s-2006-961413
  157. Takechi Masayuki, Tanaka Yasuo, Haemolytic Time Course Differences between Steroid and Triterpenoid Saponins, 10.1055/s-2006-958006
  158. Takechi Masayuki, Uno Chikari, Tanaka Yasuo, Structure-activity relationships of synthetic saponins, 10.1016/0031-9422(95)00556-0
  159. Tanaka Osamu, Tamura Yukiyoshi, Masuda Hitoshi, Mizutani Kenji, Application of Saponins in Foods and Cosmetics: Saponins of Mohave Yucca and Sapindus Mukurossi, Advances in Experimental Medicine and Biology (1996) ISBN:9781461380412 p.1-11, 10.1007/978-1-4613-0413-5_1
  160. Taverna Elena, Saba Elena, Rowe Joanna, Francolini Maura, Clementi Francesco, Rosa Patrizia, Role of Lipid Microdomains in P/Q-type Calcium Channel (Cav2.1) Clustering and Function in Presynaptic Membranes, 10.1074/jbc.m308798200
  161. Trump, FASEB J., 9, 219 (1995)
  162. 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, 10.1242/jeb.050930
  163. van Meer Gerrit, Cellular lipidomics, 10.1038/sj.emboj.7600798
  164. Verdier Mireille, Jayat Chantal, Ratinaud Marie-Hel�ne, Troutaud Danielle, Optimization of cell permeabilization for multiparametric flow cytometric analysis with lectin staining, 10.1002/1097-0320(20000901)41:1<55::aid-cyto8>3.0.co;2-a
  165. Voutquenne Laurence, Lavaud Catherine, Massiot Georges, Men-Olivier Louisette Le, Structure-Activity Relationships of Haemolytic Saponins, 10.1076/phbi.40.4.253.8470
  166. Walker Barry W., Manhanke Nathan, Stine Keith J., Comparison of the interaction of tomatine with mixed monolayers containing phospholipid, egg sphingomyelin, and sterols, 10.1016/j.bbamem.2008.06.004
  167. Wang Guanghui, Chen Haifeng, Huang Minghui, Wang Naili, Zhang Jinchao, Zhang Yaou, Bai Ganrong, Fong Wang-Fun, Yang Mengsu, Yao Xinsheng, Methyl protodioscin induces G2/M cell cycle arrest and apoptosis in HepG2 liver cancer cells, 10.1016/j.canlet.2005.10.050
  168. Wang Gao-Xue, Jiang Dong-Xin, Li Jun, Han Jing, Liu You-Tao, Liu Xiao-Lin, Anthelmintic activity of steroidal saponins from Dioscorea zingiberensis C. H. Wright against Dactylogyrus intermedius (Monogenea) in goldfish (Carassius auratus), 10.1007/s00436-010-2010-z
  169. Wang Ying, Che Chi-Ming, Chiu Jen-Fu, He Qing-Yu, Dioscin (Saponin)-Induced Generation of Reactive Oxygen Species through Mitochondria Dysfunction: A Proteomic-Based Study, 10.1021/pr070399r
  170. Wang Yibing, Zhang Yichun, Zhu Ziyan, Zhu Shilei, Li Yingxia, Li Ming, Yu Biao, Exploration of the correlation between the structure, hemolytic activity, and cytotoxicity of steroid saponins, 10.1016/j.bmc.2007.01.058
  171. Wassler M, Jonasson I, Persson R, Fries E, Differential permeabilization of membranes by saponin treatment of isolated rat hepatocytes. Release of secretory proteins, 10.1042/bj2470407
  172. Wassler, Eur. J. Cell Biol., 51, 252 (1990)
  173. Williams John R., Gong Hua, Biological Activities and Syntheses of Steroidal Saponins: the Shark-Repelling Pavoninins, 10.1007/s11745-006-1002-3
  174. Xiong Jing, Guo Jianxin, Huang Luosheng, Meng Boyu, Ping Qineng, Self-micelle formation and the incorporation of lipid in the formulation affect the intestinal absorption of Panax notoginseng, 10.1016/j.ijpharm.2008.04.016
  175. Xu Zhi-Xiang, Ding Tian, Haridas Valsala, Connolly Fiona, Gutterman Jordan U., Avicin D, a Plant Triterpenoid, Induces Cell Apoptosis by Recruitment of Fas and Downstream Signaling Molecules into Lipid Rafts, 10.1371/journal.pone.0008532
  176. Xu Z-X, Liang J, Haridas V, Gaikwad A, Connolly F P, Mills G B, Gutterman J U, A plant triterpenoid, avicin D, induces autophagy by activation of AMP-activated protein kinase, 10.1038/sj.cdd.4402207
  177. Yi Jae-Sung, Choo Hyo-Jung, Cho Bong-Rae, Kim Hwan-Myung, Kim Yong-Nyun, Ham Young-Mi, Ko Young-Gyu, Ginsenoside Rh2 induces ligand-independent Fas activation via lipid raft disruption, 10.1016/j.bbrc.2009.05.028
  178. Zhang De-Fu, Xu Hui, Sun Bing-Bing, Li Jian-Qiu, Zhou Qian-Jin, Zhang Hong-Li, Du Ai-Fang, Adjuvant effect of ginsenoside-based nanoparticles (ginsomes) on the recombinant vaccine against Eimeria tenella in chickens, 10.1007/s00436-011-2784-7
  179. Zhou Xiao-Mian, Cao Ying-Lin, Dou De-Qiang, Protective Effect of Ginsenoside-Re against Cerebral Ischemia/Reperfusion Damage in Rats, 10.1248/bpb.29.2502
  180. Zhuang, Cancer Res., 62, 2227 (2002)
  181. Zhuang Meibao, Oltean Daniela I., Gómez Isabel, Pullikuth Ashok K., Soberón Mario, Bravo Alejandra, Gill Sarjeet S., Heliothis virescensandManduca sextaLipid Rafts Are Involved in Cry1A Toxin Binding to the Midgut Epithelium and Subsequent Pore Formation, 10.1074/jbc.m110057200
Bibliographic reference Lorent, Joseph H. ; Quetin-Leclercq, Joëlle ; Mingeot-Leclercq, Marie-Paule. The amphiphilic nature of saponins and their effects on artificial and biological membranes and potential consequences for red blood and cancer cells. In: Organic & Biomolecular Chemistry, Vol. 12, no.44, p. 8803-8822 (2014)
Permanent URL http://hdl.handle.net/2078.1/157170