Triterpenoids Amplify Anti-Tumoral Effects of Mistletoe Extracts on Murine B16.F10 Melanoma In Vivo

PLoS ONE

Volumn 8, Issue 4, 2013, Pages

  Strüh, Christian M ^a,b,f   Jäger, Sebastian ^d,e,f   Kersten, Astrid ^c   Schempp, Christoph M ^a   Scheffler, Armin ^e,f   Martin, Stefan F ^a  

^a UNIVERSITY OF FREIBURG   (Germany)

^b UNIVERSITY OF FREIBURG   (Germany)

^c DermatoHistologisches Labor Dr Laaff   (Germany)

^d Betulin Institute   (Germany)

^e Birken AG   (Germany)

^f Carl Gustav Carus Institut   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

CASPASE 3; CD31 ANTIGEN; CYCLODEXTRIN; TRITERPENOID; VISCUM ALBUM EXTRACT;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIANGIOGENIC ACTIVITY; ANTINEOPLASTIC ACTIVITY; APOPTOSIS; AQUEOUS SOLUTION; ARTICLE; CANCER GROWTH; CANCER REGRESSION; CANCER SURVIVAL; CONTROLLED STUDY; DRUG EFFICACY; DRUG ISOLATION; ENZYME ACTIVITY; HISTOPATHOLOGY; IN VIVO STUDY; MALE; MELANOMA B16; MOUSE; NICK END LABELING; NONHUMAN; SURVIVAL TIME; VISCUM ALBUM;

ANIMALS; ANTINEOPLASTIC AGENTS, PHYTOGENIC; MELANOMA, EXPERIMENTAL; MICE; MICE, INBRED C57BL; NEOVASCULARIZATION, PATHOLOGIC; OLEANOLIC ACID; PHYTOTHERAPY; PLANT EXTRACTS; TRITERPENES; VISCUM ALBUM;

MURINAE; MUS;

EID: 84876221574     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0062168     Document Type: Article

References (54)

1. Garbe C, Eigentler TK, Keilholz U, Hauschild A, Kirkwood JM, (2011) Systematic review of medical treatment in melanoma: current status and future prospects. Oncologist 16: 5-24.
2. Flaherty KT, Puzanov I, Kim KB, Ribas A, McArthur GA, et al. (2010) Inhibition of mutated, activated BRAF in metastatic melanoma. N Engl J Med 363: 809-819.
3. Nazarian R, Shi H, Wang Q, Kong X, Koya RC, et al. (2010) Melanomas acquire resistance to B-RAF(V600E) inhibition by RTK or N-RAS upregulation. Nature 468: 973-977.
4. Newman DJ, Cragg GM, (2007) Natural products as sources of new drugs over the last 25 years. J Nat Prod 70: 461-477.
5. Foote M, (2007) Using nanotechnology to improve the characteristics of antineoplastic drugs: improved characteristics of nab-paclitaxel compared with solvent-based paclitaxel. Biotechnol Annu Rev 13: 345-357.
6. Rostock M, Huber R, Greiner T, Fritz P, Scheer R, et al. (2005) Anticancer activity of a lectin-rich mistletoe extract injected intratumorally into human pancreatic cancer xenografts. Anticancer Res 25: 1969-1975.
7. Seifert G, Jesse P, Laengler A, Reindl T, Lüth M, et al. (2008) Molecular mechanisms of mistletoe plant extract-induced apoptosis in acute lymphoblastic leukemia in vivo and in vitro. Cancer Lett 264: 218-228.
8. Horneber MA, Bueschel G, Huber R, Linde K, Rostock M (2008) Mistletoe therapy in oncology. Cochrane Database Syst Rev: CD003297.
9. Kienle GS, Glockmann A, Schink M, Kiene H, (2009) Viscum album L. extracts in breast and gynaecological cancers: a systematic review of clinical and preclinical research. J Exp Clin Cancer Res 28: 79.
10. Legnani W, (2008) Mistletoe in conventional oncological practice: exemplary cases. Integr Cancer Ther 7: 162-171.
11. Nabrotzki M, Scheffler A (2001) Komplette Remission nach intratumoraler Misteltherapie eines Duodenum-Karzinom-Rezidivs. In: Scheer R BR, Becher H, Berg PA, Fintelmann V, editor. Die Mistel in der Tumortherapie, Grundlagenforschung und Klinik. Essen: KVC Verlag. pp. 413-422.
12. Kleeberg UR, Suciu S, Brocker EB, Ruiter DJ, Chartier C, et al. (2004) Final results of the EORTC 18871/DKG 80-1 randomised phase III trial. rIFN-alpha2b versus rIFN-gamma versus ISCADOR M versus observation after surgery in melanoma patients with either high-risk primary (thickness >3 mm) or regional lymph node metastasis. Eur J Cancer 40: 390-402.
13. Augustin M, Bock PR, Hanisch J, Karasmann M, Schneider B, (2005) Safety and efficacy of the long-term adjuvant treatment of primary intermediate- to high-risk malignant melanoma (UICC/AJCC stage II and III) with a standardized fermented European mistletoe (Viscum album L.) extract. Results from a multicenter, comparative, epidemiological cohort study in Germany and Switzerland. Arzneimittelforschung 55: 38-49.
14. Thies A, Nugel D, Pfüller U, Moll I, Schumacher U, (2005) Influence of mistletoe lectins and cytokines induced by them on cell proliferation of human melanoma cells in vitro. Toxicology 207: 105-116.
15. Thies A, Dautel P, Meyer A, Pfüller U, Schumacher U, (2008) Low-dose mistletoe lectin-I reduces melanoma growth and spread in a scid mouse xenograft model. Br J Cancer 98: 106-112.
16. Büssing A, Schietzel M, (1999) Apoptosis-inducing properties of Viscum album L. extracts from different host trees, correlate with their content of toxic mistletoe lectins. Anticancer Res 19: 23-28.
17. Janssen O, Scheffler A, Kabelitz D, (1993) In vitro effects of mistletoe extracts and mistletoe lectins. Cytotoxicity towards tumor cells due to the induction of programmed cell death (apoptosis). Arzneimittelforschung 43: 1221-1227.
18. Müthing J, Meisen I, Kniep B, Haier J, Senninger N, et al. (2005) Tumor-associated CD75s gangliosides and CD75s-bearing glycoproteins with Neu5Acalpha2-6Galbeta1-4GlcNAc-residues are receptors for the anticancer drug rViscumin. FASEB J 19: 103-105.
19. Beuth J, (1997) Clinical relevance of immunoactive mistletoe lectin-I. Anticancer Drugs 8Suppl 1: S53-55.
20. Jäger S, Winkler K, Pfüller U, Scheffler A, (2007) Solubility studies of oleanolic acid and betulinic acid in aqueous solutions and plant extracts of Viscum album L. Planta Med. 73: 157-162.
21. Laszczyk MN, (2009) Pentacyclic triterpenes of the lupane, oleanane and ursane group as tools in cancer therapy. Planta Med 75: 1549-1560.
22. Jäger S, Trojan H, Kopp T, Laszczyk MN, Scheffler A, (2009) Pentacyclic triterpene distribution in various plants- rich sources for a new group of multi-potent plant extracts. Molecules 14: 2016-2031.
23. Pisha E, Chai H, Lee IS, Chagwedera TE, Farnsworth NR, et al. (1995) Discovery of betulinic acid as a selective inhibitor of human melanoma that functions by induction of apoptosis. Nat Med 1: 1046-1051.
24. Kanjoormana M, Kuttan G, (2010) Antiangiogenic activity of ursolic acid. Integr Cancer Ther 9: 224-235.
25. Place AE, Suh N, Williams CR, Risingsong R, Honda T, et al. (2003) The novel synthetic triterpenoid, CDDO-imidazolide, inhibits inflammatory response and tumor growth in vivo. Clin Cancer Res 9: 2798-2806.
26. Juan ME, Planas JM, Ruiz-Gutierrez V, Daniel H, Wenzel U, (2008) Antiproliferative and apoptosis-inducing effects of maslinic and oleanolic acids, two pentacyclic triterpenes from olives, on HT-29 colon cancer cells. Br J Nutr 100: 36-43.
27. Martin R, Carvalho J, Ibeas E, Hernandez M, Ruiz-Gutierrez V, et al. (2007) Acidic triterpenes compromise growth and survival of astrocytoma cell lines by regulating reactive oxygen species accumulation. Cancer Res 67: 3741-3751.
28. Strüh CM, Jäger S, Schempp CM, Scheffler A, Martin SF (2012) A novel triterpene extract from mistletoe induces rapid apoptosis in murine B16.F10 melanoma cells. Phytotherapy Research.
29. Feles M, Koehler R, Scheffler A (1991) Verfahren und Vorrichtung zur Herstellung von Presssaft aus Pflanzen. Europäisches Patent Nr 0288603. Europa: 0288603.
30. Jäger S, Beffert M, Hoppe K, Nadberezny D, Frank B, et al. (2011) Preparation of herbal tea as infusion or by maceration at room temperature using mistletoe tea as an example. Sci Pharm 79: 145-155.
31. Fidler IJ, (1975) Biological behavior of malignant melanoma cells correlated to their survival in vivo. Cancer Res 35: 218-224.
32. Dudda JC, Simon JC, Martin S, (2004) Dendritic cell immunization route determines CD8+ T cell trafficking to inflamed skin: role for tissue microenvironment and dendritic cells in establishment of T cell-homing subsets. J Immunol 172: 857-863.
33. Schempp CM, Kiss J, Kirkin V, Averbeck M, Simon-Haarhaus B, et al. (2005) Hyperforin acts as an angiogenesis inhibitor. Planta Med 71: 999-1004.
34. Augustine CK, Toshimitsu H, Jung SH, Zipfel PA, Yoo JS, et al. (2010) Sorafenib, a multikinase inhibitor, enhances the response of melanoma to regional chemotherapy. Mol Cancer Ther 9: 2090-2101.
35. Wack C, Becker JC, Bröcker EB, Lutz WK, Fischer WH, (2001) Chemoimmunotherapy for melanoma with dacarbazine and 2,4-dinitrochlorobenzene: results from a murine tumour model. Melanoma Res 11: 247-253.
36. Terheyden P, Kortum AK, Schulze HJ, Durani B, Remling R, et al. (2007) Chemoimmunotherapy for cutaneous melanoma with dacarbazine and epifocal contact sensitizers: results of a nationwide survey of the German Dermatologic Co-operative Oncology Group. J Cancer Res Clin Oncol 133: 437-444.
37. Wack C, Kirst A, Becker JC, Lutz WK, Bröcker EB, et al. (2002) Chemoimmunotherapy for melanoma with dacarbazine and 2,4-dinitrochlorobenzene elicits a specific T cell-dependent immune response. Cancer Immunol Immunother 51: 431-439.
38. Elluru SR, JP Vanh, Delignat S, Prost F, Heudes D, et al. (2009) Antiangiogenic properties of viscum album extracts are associated with endothelial cytotoxicity. Anticancer Res 29: 2945-2950.
39. Sohn KH, Lee HY, Chung HY, Young HS, Yi SY, et al. (1995) Anti-angiogenic activity of triterpene acids. Cancer Lett 94: 213-218.
40. Delebinski CI, Jäger S, Kemnitz-Hassanin K, Henze G, Lode HN, et al. (2012) A new development of triterpene acid-containing extracts from Viscum album L. displays synergistic induction of apoptosis in acute lymphoblastic leukaemia. Cell Proliferation.
41. Huber R, Rostock M, Goedl R, Ludtke R, Urech K, et al. (2005) Mistletoe treatment induces GM-CSF- and IL-5 production by PBMC and increases blood granulocyte- and eosinophil counts: a placebo controlled randomized study in healthy subjects. Eur J Med Res 10: 411-418.
42. Huber R, Barth H, Schmitt-Graff A, Klein R, (2000) Hypereosinophilia induced by high-dose intratumoral and peritumoral mistletoe application to a patient with pancreatic carcinoma. J Altern Complement Med 6: 305-310.
43. Gardin NE, (2009) Immunological response to mistletoe (Viscum album L.) in cancer patients: a four-case series. Phytother Res 23: 407-411.
44. Schöffski P, Riggert S, Fumoleau P, Campone M, Bolte O, et al. (2004) Phase I trial of intravenous aviscumine (rViscumin) in patients with solid tumors: a study of the European Organization for Research and Treatment of Cancer New Drug Development Group. Ann Oncol 15: 1816-1824.
45. Schöffski P, Breidenbach I, Krauter J, Bolte O, Stadler M, et al. (2005) Weekly 24 h infusion of aviscumine (rViscumin): a phase I study in patients with solid tumours. Eur J Cancer 41: 1431-1438.
46. Burger AM, Mengs U, Schüler JB, Fiebig HH, (2001) Anticancer activity of an aqueous mistletoe extract (AME) in syngeneic murine tumor models. Anticancer Res 21: 1965-1968.
47. Hsu HY, Yang JJ, Lin CC, (1997) Effects of oleanolic acid and ursolic acid on inhibiting tumor growth and enhancing the recovery of hematopoietic system postirradiation in mice. Cancer Lett 111: 7-13.
48. Saleem M, Maddodi N, Abu ZM, Khan N, Bin HB, et al. (2008) Lupeol inhibits growth of highly aggressive human metastatic melanoma cells in vitro and in vivo by inducing apoptosis. Clin Cancer Res 14: 2119-2127.
49. Jeong DW, Kim YH, Kim HH, Ji HY, Yoo SD, et al. (2007) Dose-linear pharmacokinetics of oleanolic acid after intravenous and oral administration in rats. Biopharm Drug Dispos 28: 51-57.
50. Ji HY, Shin BS, Jeong DW, Park EJ, Park ES, et al. (2009) Interspecies scaling of oleanolic acid in mice, rats, rabbits and dogs and prediction of human pharmacokinetics. Arch Pharm Res 32: 251-257.
51. Liby KT, Yore MM, Sporn MB, (2007) Triterpenoids and rexinoids as multifunctional agents for the prevention and treatment of cancer. Nat Rev Cancer 7: 357-369.
52. Franz H, Steffan AM, Kirn A, (1986) Interaction of mistletoe lectin I with Kupffer cells and endothelial cells of mouse liver. Acta Histochem 78: 123-129.
53. Stein GM (2000) Toxicology of mistletoe extracts and their components. In: Büssing A, editor. Mistletoe: The genus viscum. Amsterdam: Harwood Academic Publishers. pp. 183-194.
54. Liu J, (1995) Pharmacology of oleanolic acid and ursolic acid. J Ethnopharmacol 49: 57-68.