Asiatic acid induces endoplasmic reticulum stress and apoptotic death in glioblastoma multiforme cells both in vitro and in vivo

Molecular Carcinogenesis

Volumn 54, Issue 11, 2015, Pages 1417-1429

  Kavitha, Chandagirikoppal V ^a   Jain, Anil K ^a   Agarwal, Chapla ^a,b   Pierce, Angela ^c   Keating, Amy ^c   Huber, Kendra M ^b,d   Serkova, Natalie J ^b,d   Wempe, Michael F ^a,b   Agarwal, Rajesh ^a,b   Deep, Gagan ^a,b  

^a UNIVERSITY OF COLORADO   (United States)

^b UNIVERSITY OF COLORADO CANCER CENTER   (United States)

^c University of Colorado Denver and Children s Hospital Colorado   (United States)

^d UNIVERSITY OF COLORADO SCHOOL OF MEDICINE   (United States)

Author keywords

Apoptosis; Asiatic acid; Calcium; ER stress; Glioblastoma multiforme

Indexed keywords

ASIATIC ACID; CALCIUM; CALNEXIN; CALPAIN; CASPASE; GLUCOSE REGULATED PROTEIN 78; PROTEIN BCL 2; PROTEIN IRE1; SURVIVIN; TEMOZOLOMIDE; APOPTOSIS REGULATORY PROTEIN; DACARBAZINE; PENTACYCLIC TRITERPENE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; BLOOD BRAIN BARRIER; CALCIUM CELL LEVEL; CALCIUM SIGNALING; CANCER INHIBITION; CELL VIABILITY; DRUG EFFICACY; ENDOPLASMIC RETICULUM STRESS; GLIOBLASTOMA; GLIOMA CELL; HUMAN; HUMAN CELL; IN VITRO STUDY; IN VIVO CULTURE; INTRACELLULAR SIGNALING; MITOCHONDRION; MOUSE; NONHUMAN; NUCLEAR MAGNETIC RESONANCE IMAGING; PRIORITY JOURNAL; PROTEIN EXPRESSION; TUMOR VOLUME; ANALOGS AND DERIVATIVES; ANIMAL; BRAIN NEOPLASMS; DRUG EFFECTS; DRUG SCREENING; GENE EXPRESSION REGULATION; GENETICS; MALE; METABOLISM; NUDE MOUSE; PROCEDURES; TUMOR CELL LINE;

ANIMALS; APOPTOSIS; APOPTOSIS REGULATORY PROTEINS; BRAIN NEOPLASMS; CELL LINE, TUMOR; DACARBAZINE; ENDOPLASMIC RETICULUM STRESS; GENE EXPRESSION REGULATION, NEOPLASTIC; GLIOBLASTOMA; HUMANS; MALE; MICE; MICE, NUDE; PENTACYCLIC TRITERPENES; TUMOR BURDEN; XENOGRAFT MODEL ANTITUMOR ASSAYS;

EID: 84945199647     PISSN: 08991987     EISSN: 10982744     Source Type: Journal    
DOI: 10.1002/mc.22220     Document Type: Article

References (47)

1. Fan S, Sun Z, Jiang D, et al. BmKCT toxin inhibits glioma proliferation and tumor metastasis. Cancer Lett 2010; 291:158-166.
2. Friedman HS, Kerby T, Calvert H. Temozolomide and treatment of malignant glioma. Clin Cancer Res 2000; 6:2585-2597.
3. Brinkhaus B, Lindner M, Schuppan D, Hahn EG. Chemical, pharmacological and clinical profile of the East Asian medical plant Centella asiatica. Phytomedicine 2000; 7:427-448.
4. James JT, Dubery IA. Pentacyclic triterpenoids from the medicinal herb, Centella asiatica (L.) Urban. Molecules 2009; 14:3922-3941.
5. Shinomol GK, Muralidhara . Prophylactic neuroprotective property of Centella asiatica against 3-nitropropionic acid induced oxidative stress and mitochondrial dysfunctions in brain regions of prepubertal mice. Neurotoxicology 2008; 29:948-957.
6. Soumyanath A, Zhong YP, Henson E, et al. Centella asiatica extract improves behavioral deficits in a mouse model of alzheimer's disease: Investigation of a possible mechanism of action. Int J Alzheimers Dis 2012; 2012:381974.
7. Soumyanath A, Zhong YP, Gold SA, et al. Centella asiatica accelerates nerve regeneration upon oral administration and contains multiple active fractions increasing neurite elongation in-vitro. J Pharm Pharmacol 2005; 57:1221-1229.
8. Singh RH, Narsimhamurthy K, Singh G. Neuronutrient impact of Ayurvedic Rasayana therapy in brain aging. Biogerontology 2008; 9:369-374.
9. Krishnamurthy RG, Senut MC, Zemke D, et al. Asiatic acid, a pentacyclic triterpene from Centella asiatica, is neuroprotective in a mouse model of focal cerebral ischemia. J Neurosci Res 2009; 87:2541-2550.
10. Lee MK, Kim SR, Sung SH, et al. Asiatic acid derivatives protect cultured cortical neurons from glutamate-induced excitotoxicity. Res Commun Mol Pathol Pharmacol 2000; 108:75-86.
11. Xu MF, Xiong YY, Liu JK, Qian JJ, Zhu L, Gao J. Asiatic acid, a pentacyclic triterpene in Centella asiatica, attenuates glutamate-induced cognitive deficits in mice and apoptosis in SH-SY5Y cells. Acta Pharmacol Sin 2012; 33:578-587.
12. Tang XL, Yang XY, Jung HJ, et al. Asiatic acid induces colon cancer cell growth inhibition and apoptosis through mitochondrial death cascade. Biol Pharm Bull 2009; 32:1399-1405.
13. Hsu YL, Kuo PL, Lin LT, Lin CC. Asiatic acid, a triterpene, induces apoptosis and cell cycle arrest through activation of extracellular signal-regulated kinase and p38 mitogen-activated protein kinase pathways in human breast cancer cells. J Pharmacol Exp Ther 2005; 313:333-344.
14. Cho CW, Choi DS, Cardone MH, Kim CW, Sinskey AJ, Rha C. Glioblastoma cell death induced by asiatic acid. Cell Biol Toxicol 2006; 22:393-408.
15. Park BC, Bosire KO, Lee ES, Lee YS, Kim JA. Asiatic acid induces apoptosis in SK-MEL-2 human melanoma cells. Cancer Lett 2005; 218:81-90.
16. Gurfinkel DM, Chow S, Hurren R, et al. Disruption of the endoplasmic reticulum and increases in cytoplasmic calcium are early events in cell death induced by the natural triterpenoid Asiatic acid. Apoptosis 2006; 11:1463-1471.
17. Meng YQ, Li YY, Li FQ, et al. Synthesis and antitumor activity evaluation of new asiatic acid derivatives. J Asian Nat Prod Res 2012; 14:844-855.
18. Bunpo P, Kataoka K, Arimochi H, et al. Inhibitory effects of asiatic acid and CPT-11 on growth of HT-29 cells. J Med Invest 2005; 52:65-73.
19. Lee YS, Jin DQ, Kwon EJ, et al. Asiatic acid, a triterpene, induces apoptosis through intracellular Ca2+ release and enhanced expression of p53 in HepG2 human hepatoma cells. Cancer Lett 2002; 186:83-91.
20. Park BC, Paek SH, Lee YS, et al. Inhibitory effects of asiatic acid on 7, 12-dimethylbenz[a]anthracene and 12-O-tetradecanoylphorbol 13-acetate-induced tumor promotion in mice. Biol Pharm Bull 2007; 30:176-179.
21. Kavitha CV, Agarwal C, Agarwal R, Deep G. Asiatic acid inhibits pro-angiogenic effects of VEGF and human gliomas in endothelial cell culture models. PLoS One 2011; 6:e22745.
22. Igney FH, Krammer PH. Death and anti-death: tumour resistance to apoptosis. Nat Rev Cancer 2002; 2:277-288.
23. Riedl SJ, Salvesen GS. The apoptosome: signalling platform of cell death. Nat Rev Mol Cell Biol 2007; 8:405-413.
24. Cotter TG. Apoptosis and cancer: the genesis of a research field. Nat Rev Cancer 2009; 9:501-507.
25. Wlodkowic D, Skommer J, McGuinness D, Hillier C, Darzynkiewicz Z. ER-Golgi network-a future target for anti-cancer therapy. Leuk Res 2009; 33:1440-1447.
26. Ferri KF, Kroemer G. Organelle-specific initiation of cell death pathways. Nat Cell Biol 2001; 3:E255-263.
27. Hoyer-Hansen M, Jaattela M. Connecting endoplasmic reticulum stress to autophagy by unfolded protein response and calcium. Cell Death Differ 2007; 14:1576-1582.
28. Schwarze SR, Lin EW, Christian PA, Gayheart DT, Kyprianou N. Intracellular death platform steps-in: targeting prostate tumors via endoplasmic reticulum (ER) apoptosis. Prostate 2008; 68:1615-1623.
29. Boelens J, Lust S, Offner F, Bracke ME, Vanhoecke BW. Review. The endoplasmic reticulum: a target for new anticancer drugs. In Vivo 2007; 21:215-226.
30. Kraskiewicz H, FitzGerald U. InterfERing with endoplasmic reticulum stress. Trends Pharmacol Sci 2012; 33:53-63.
31. Oakes SA, Opferman JT, Pozzan T, Korsmeyer SJ, Scorrano L. Regulation of endoplasmic reticulum Ca2+ dynamics by proapoptotic BCL-2 family members. Biochem Pharmacol 2003; 66:1335-1340.
32. Zi X, Feyes DK, Agarwal R. Anticarcinogenic effect of a flavonoid antioxidant, silymarin, in human breast cancer cells MDA-MB 468: induction of G1 arrest through an increase in Cip1/p21 concomitant with a decrease in kinase activity of cyclin-dependent kinases and associated cyclins. Clin Cancer Res 1998; 4:1055-1064.
33. Singh RP, Deep G, Chittezhath M, et al. Effect of silibinin on the growth and progression of primary lung tumors in mice. J Natl Cancer Inst 2006; 98:846-855.
34. Singh RP, Deep G, Blouin MJ, Pollak MN, Agarwal R. Silibinin suppresses in vivo growth of human prostate carcinoma PC-3 tumor xenograft. Carcinogenesis 2007; 28:2567-2574.
35. Gu M, Singh RP, Dhanalakshmi S, Agarwal C, Agarwal R. Silibinin inhibits inflammatory and angiogenic attributes in photocarcinogenesis in SKH-1 hairless mice. Cancer Res 2007; 67:3483-3491.
36. Wick W, Weller M, Weiler M, Batchelor T, Yung AW, Platten M. Pathway inhibition: emerging molecular targets for treating glioblastoma. Neuro Oncol 2011; 13:566-579.
37. Hirose Y, Berger MS, Pieper RO. p53 effects both the duration of G2/M arrest and the fate of temozolomide-treated human glioblastoma cells. Cancer Res 2001; 61:1957-1963.
38. Yamini B, Yu X, Gillespie GY, Kufe DW, Weichselbaum RR. Transcriptional targeting of adenovirally delivered tumor necrosis factor alpha by temozolomide in experimental glioblastoma. Cancer Res 2004; 64:6381-6384.
39. Guicciardi ME, Gores GJ. Calpains can do it alone: implications for cancer therapy. Cancer Biol Ther 2003; 2:153-154.
40. Lefranc F, Sadeghi N, Camby I, Metens T, Dewitte O, Kiss R. Present and potential future issues in glioblastoma treatment. Expert Rev Anticancer Ther 2006; 6:719-732.
41. Tate MC, Aghi MK. Biology of angiogenesis and invasion in glioma. Neurotherapeutics 2009; 6:447-457.
42. Lefranc F, Brotchi J, Kiss R. Possible future issues in the treatment of glioblastomas: special emphasis on cell migration and the resistance of migrating glioblastoma cells to apoptosis. J Clin Oncol 2005; 23:2411-2422.
43. Zheng CJ, Qin LP. Chemical components of Centella asiatica and their bioactivities. Zhong Xi Yi Jie He Xue Bao 2007; 5:348-351.
44. Dhanasekaran M, Holcomb LA, Hitt AR, et al. Centella asiatica extract selectively decreases amyloid beta levels in hippocampus of Alzheimer's disease animal model. Phytother Res 2009; 23:14-19.
45. Zheng XC, Wang SH. Determination of asiatic acid in beagle dog plasma after oral administration of Centella asiatica extract by precolumn derivatization RP-HPLC. J Chromatogr B Analyt Technol Biomed Life Sci 2009; 877:477-481.
46. Grimaldi R, De Ponti F, D'Angelo L, et al. Pharmacokinetics of the total triterpenic fraction of Centella asiatica after single and multiple administrations to healthy volunteers. A new assay for asiatic acid. J Ethnopharmacol 1990; 28:235-241.
47. Hoh C, Boocock D, Marczylo T, et al. Pilot study of oral silibinin, a putative chemopreventive agent, in colorectal cancer patients: silibinin levels in plasma, colorectum, and liver and their pharmacodynamic consequences. Clin Cancer Res 2006; 12:2944-2950.