Autophagy enhancement contributes to the synergistic effect of vitamin D in temozolomide‑based glioblastoma chemotherapy

Experimental and Therapeutic Medicine

Volumn 11, Issue 6, 2016, Pages 2153-2162

  Bak, Dong Ho ^a   Kang, Seong Hee ^a   Choi, Du Ri ^a   Gil, Mi Na ^a   Yu, Kwang Sik ^a   Jeong, Ji Heun ^a   Lee, Nam Seob ^a   Lee, Je Hun ^a   Jeong, Young Gil ^a   Kim, Dong Kwan ^a   Kim, Do Kyung ^a   Kim, Jwa Jin ^a   Han, Seung Yun ^a  

^a Konyang University   (South Korea)

Author keywords

Autophagy; Glioblastoma; Orthotopic xenograft; Temozolomide; Vitamin D

Indexed keywords

MICROTUBULE ASSOCIATED PROTEIN 1; TEMOZOLOMIDE; VITAMIN D;

ANIMAL CELL; ANTINEOPLASTIC ACTIVITY; APOPTOSIS; ARTICLE; AUTOPHAGY; CELL COUNTING; CELL VIABILITY ASSAY; CLONOGENIC ASSAY; CONFOCAL LASER MICROSCOPY; CONTROLLED STUDY; CYTOTOXICITY; FLOW CYTOMETRY; FLUORESCENCE; GLIOBLASTOMA; IC50; LIGHT CHAIN; MEDIAN SURVIVAL TIME; MTT ASSAY; NONHUMAN; NUCLEAR MAGNETIC RESONANCE IMAGING; PROTEIN EXPRESSION; RAT; TRANSMISSION ELECTRON MICROSCOPY; TUMOR VOLUME; WESTERN BLOTTING; WOUND HEALING;

EID: 84964018944     PISSN: 17920981     EISSN: 17921015     Source Type: Journal    
DOI: 10.3892/etm.2016.3196     Document Type: Article

References (46)

1. Mahaley MS, Mettlin C, Natarajan N, Laws ER Jr and Peace BB: National survey of patterns of care for brain‑tumor patients. J Neurosurg 71: 826‑836, 1989.
2. Avgeropoulos NG and Batchelor TT: New treatment strategies for malignant gliomas. Oncologist 4: 209‑224, 1999.
3. Bower M, Newlands ES, Bleehen NM, Brada M, Begent RJ, Calvert H, Colquhoun I, Lewis P and Brampton MH: Multicentre CRC phase II trial of temozolomide in recurrent or progressive high‑grade glioma. Cancer Chemother Pharmacol 40: 484‑488, 1997.
4. Yung WK, Prados MD, Yaya‑Tur R, Rosenfeld SS, Brada M, Friedman HS, Albright R, Olson J, Chang SM, O'Neill AM, et al: Multicenter phase II trial of temozolomide in patients with anaplastic astrocytoma or anaplastic oligoastrocytoma at first relapse. J Clin Oncol 17: 2762‑2771, 1999.
5. Newlands ES, Blackledge GR, Slack JA, Rustin GJ, Smith DB, Stuart NS, Quarterman CP, Hoffman R, Stevens MF and Brampton MH: Phase I trial of temozolomide (CCRG 81045: M&B 39831: NSC 362856). Br J Cancer 65: 287‑291, 1992.
6. Dehdashti AR, Hegi ME, Regli L, Pica A and Stupp R: New trends in the medical management of glioblastoma multiforme: The role of temozolomide chemotherapy. Neurosurg Focus 20: E6, 2006.
7. Zhang J, Stevens MF and Bradshaw TD: Temozolomide: Mechanisms of action, repair and resistance. Curr Mol Pharmacol 5: 102‑114, 2012.
8. Begemann M, Kashimawo SA, Lunn RM, Delohery T, Choi YJ, Kim S, Heitjan DF, Santella RM, Schiff PB, Bruce JN and Weinstein IB: Growth inhibition induced by Ro 31‑8220 and calphostin C in human glioblastoma cell lines is associated with apoptosis and inhibition of CDC2 kinase. Anticancer Res 18: 3139‑3152, 1998.
9. Gagliano N, Moscheni C, Torri C, Donetti E, Magnani I, Costa F, Nowicky W and Gioia M: Ukrain modulates glial fibrillary acidic protein, but not connexin 43 expression, and induces apoptosis in human cultured glioblastoma cells. Anticancer Drugs 18: 669‑676, 2007.
10. Kanzawa T, Bedwell J, Kondo Y, Kondo S and Germano IM: Inhibition of DNA repair for sensitizing resistant glioma cells to temozolomide. J Neurosurg 99: 1047‑1052, 2003.
11. Takeuchi H, Kondo Y, Fujiwara K, Kanzawa T, Aoki H, Mills GB and Kondo S: Synergistic augmentation of rapamycin‑induced autophagy in malignant glioma cells by phosphatidylinositol 3‑kinase/protein kinase B inhibitors. Cancer Res 65: 3336‑3346, 2005.
12. Takeuchi H, Kanzawa T, Kondo Y and Kondo S: Inhibition of platelet‑derived growth factor signalling induces autophagy in malignant glioma cells. Br J Cancer 90: 1069‑1075, 2004.
13. Kanzawa T, Germano IM, Komata T, Ito H, Kondo Y and Kondo S: Role of autophagy in temozolomide‑induced cytotoxicity for malignant glioma cells. Cell Death Differ 11: 448‑457, 2004.
14. Gutierrez MG, Master SS, Singh SB, Taylor GA, Colombo MI and Deretic V: Autophagy is a defense mechanism inhibiting BCG and Mycobacterium tuberculosis survival in infected macrophages. Cell 119: 753‑766, 2004.
15. Giovannucci E: Vitamin D and cardiovascular disease. Curr Atheroscler Rep 11: 456‑461, 2009.
16. Xie Z and Klionsky DJ: Autophagosome formation: Core machinery and adaptations. Nat Cell Biol 9: 1102‑1109, 2007.
17. Campbell GR and Spector SA: Hormonally active vitamin D3 (1alpha,25‑dihydroxycholecalciferol) triggers autophagy in human macrophages that inhibits HIV‑1 infection. J Biol Chem 286: 18890‑18902, 2011.
18. Picotto G, Liaudat AC, Bohl L and Tolosa de Talamoni N: Molecular aspects of vitamin D anticancer activity. Cancer Invest 308: 604‑614, 2012.
19. Høyer‑Hansen M and Jäättelä M: AMP‑activated protein kinase: A universal regulator of autophagy? Autophagy 3: 381‑383, 2007.
20. 2+/calmodulin‑dependent protein kinase kinase‑beta acts upstream of AMP‑activated protein kinase in mammalian cells. Cell Metab 2: 21‑33, 2005.
21. Hannigan AM and Gorski SM: Macroautophagy: The key ingredient to a healthy diet? Autophagy 5: 140‑151, 2009.
22. Zou J, Wang YX, Mu HJ, Xiang J, Wu W, Zhang B and Xie P: Down‑regulation of glutamine synthetase enhances migration of rat astrocytes after in vitro injury. Neurochem Int 58: 404‑413, 2011.
23. Tanida I, Ueno T, and Kominami E: LC3 and autophagy. Methods Mol Biol 445: 77‑88, 2008.
24. Kobayashi N, Allen N, Clendenon NR and Ko LW: An improved rat brain‑tumor model. J Neurosurg 53: 808‑815, 1980.
25. Rubin JB, Kung AL, Klein RS, Chan JA, Sun Y, Schmidt K, Kieran MW, Luster AD and Segal RA: A small‑molecule antagonist of CXCR4 inhibits intracranial growth of primary brain tumors. Proc Natl Acad Sci USA 100: 13513‑13518, 2003.
26. Knizhnik AV, Roos WP, Nikolova T, Quiros S, Tomaszowski KH, Christmann M and Kaina B: Survival and death strategies in glioma cells: Autophagy, senescence and apoptosis triggered by a single type of temozolomide‑induced DNA damage. PLoS One 8: e55665, 2013.
27. Wilson EN, Bristol ML, Di X, Maltese WA, Koterba K, Beckman MJ and Gewirtz DA: A switch between cytopro-tective and cytotoxic autophagy in the radiosensitization of breast tumor cells by chloroquine and vitamin D. Horm Cancer 2: 272‑85, 2011.
28. Kabeya Y, Mizushima N, Ueno T, Yamamoto A, Kirisako T, Noda T, Kominami E, Ohsumi Y and Yoshimori T: LC3, a mammalian homologue of yeast Apg8p, is localized in autophagosome membranes after processing. EMBO J 19: 5720‑5728, 2000.
29. Mizushima N, Yamamoto A, Hatano M, Kobayashi Y, Kabeya Y, Suzuki K, Tokuhisa T, Ohsumi Y and Yoshimori T: Dissection of autophagosome formation using Apg5‑deficient mouse embryonic stem cells. J Cell Biol 152: 657‑668, 2001.
30. Xu HD, Wu D, Gu JH, Ge JB, Wu JC, Han R, Liang ZQ and Qin ZH: The pro‑survival role of autophagy depends on Bcl‑2 under nutrition stress conditions. PLoS One 8: e63232, 2013.
31. Kapoor GS and O'Rourke DM: Mitogenic signaling cascades in glial tumors. Neurosurgery 52: 1425‑1435, 2003.
32. Lefranc F, Brotchi J and 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 23: 2411‑2422, 2005.
33. Mizushima N, Ohsumi Y and Yoshimori T: Autophagosome formation in mammalian cells. Cell Struct Funct 27: 421‑429, 2002.
34. Levine B, Mizushima N and Virgin HW: Autophagy in immunity and inflammation. Nature 469: 323‑335, 2011.
35. Feng Y, Ke C, Tang Q, Dong H, Zheng X, Lin W2, Ke J, Huang J, Yeung SC, and Zhang H: Metformin promotes autophagy and apoptosis in esophageal squamous cell carcinoma by downregu-lating Stat3 signaling. Cell Death Dis 5: e1088, 2014.
36. Liu YQ, Cheng X, Guo LX, Mao C, Chen YJ, Liu HX, Xiao QC, Jiang S, Yao ZJ, and Zhou GB: Identification of an annonaceous acetogeninmimetic, AA005, as an AMPK activator and autophagy inducer in colon cancer cells. PLoS One 7:e47049, 2012.
37. Miracco C, Cosci E, Oliveri G, Luzi P, Pacenti L, Monciatti I, Mannucci S, De Nisi MC, Toscano M, Malagnino V, et al: Protein and mRNA expression of autophagy gene Beclin 1 in human brain tumours. Int J Oncol 30: 429‑436, 2007.
38. Huang X, Bai HM, Chen L, Li B and Lu YC: Reduced expression of LC3B‑II and Beclin 1 in glioblastoma multiforme indicates a down‑regulated autophagic capacity that relates to the progression of astrocytic tumors. J Clin Neurosci 17: 1515‑1519, 2010.
39. Aoki H, Kondo Y, Aldape K, Yamamoto A, Iwado E, Yokoyama T, Hollingsworth EF, Kobayashi R, Hess K, Shinojima N, et al: Monitoring autophagy in glioblastoma with antibody against isoform B of human microtubule‑associated protein 1 light chain 3. Autophagy 4: 467‑475, 2008.
40. Jain MV, Paczulla AM, Klonisch T, Dimgba FN, Rao SB, Roberg K, Schweizer F, Lengerke C, Davoodpour P, et al: Interconnections between apoptotic, autophagic and necrotic pathways: Implications for cancer therapy development. J Cell Mol Med 17: 12‑29, 2013.
41. Rubinsztein DC, Shpilka T and Elazar Z: Mechanisms of autophagosome biogenesis. Curr Biol 22: 29‑34, 2012.
42. Monastyrska I and Klionsky DJ: Autophagy in organelle homeostasis: peroxisome turnover. Mol Aspects Med 27: 483‑494, 2006.
43. Audo I, Darjatmoko SR, Schlamp CL, Lokken JM, Lindstrom MJ, Albert DM and Nickells RW: Vitamin D analogues increase p53, p21, and apoptosis in a xenograft model of human retinoblastoma. Invest Ophthalmol Vis Sci 44: 4192‑4199, 2003.
44. Bernardi RJ, Johnson CS, Modzelewski RA and Trump DL: Antiproliferative effects of 1alpha,25‑dihydroxyvitamin D(3) and vitamin D analogs on tumor‑derived endothelial cells. Endocrinology 143: 2508‑2514, 2002.
45. Alvarez‑Díaz S, Valle N, García JM, Peña C, Freije JM, Quesada V, Astudillo A, Bonilla F, López‑Otín C and Muñoz A: Cystatin D is a candidate tumor suppressor gene induced by vitamin D in human colon cancer cells. J Clin Invest 119: 2343‑2358, 2009.
46. Gorski SM, Chittaranjan S, Pleasance ED, Freeman JD, Anderson CL, Varhol RJ, Coughlin SM, Zuyderduyn SD, Jones SJ, Marra MA: A SAGE approach to discovery of genes involved in autophagic cell death. Curr Biol 13: 358‑363, 2003.