199
Views
5
CrossRef citations to date
0
Altmetric
Original Research

Temozolomide induces the expression of the glioma Big Potassium (gBK) ion channel, while inhibiting fascin-1 expression: possible targets for glioma therapy

, , , , , & show all
Pages 1155-1167 | Received 14 Jun 2016, Accepted 28 Jun 2016, Published online: 13 Jul 2016

References

  • Stupp R, Hegi ME, Mason WP, et al. Effects of radiotherapy with concomitant and adjuvant temozolomide versus radiotherapy alone on survival in glioblastoma in a randomised phase III study: 5-year analysis of the EORTC-NCIC trial. Lancet Oncol. 2009;10(5):459–466.
  • Denny BJ, Wheelhouse RT, Stevens MFG, et al. NMR and molecular modeling investigation of the mechanism of activation of the antitumor drug temozolomide and its interaction with DNA. Biochemistry. 1994;33(31):9045–9051.
  • Kaina B, Christmann M, Naumann S, et al. MGMT: Key node in the battle against genotoxicity, carcinogenicity and apoptosis induced by alkylating agents. DNA Repair. 2007;6(8):1079–1099.
  • Kitange GJ, Carlson BL, Schroeder MA, et al. Induction of MGMT expression is associated with temozolomide resistance in glioblastoma xenografts. Neuro Oncol. 2009;11(3):281–291.
  • Hegi ME, Diserens A-C, Gorlia T, et al. MGMT gene silencing and benefit from temozolomide in glioblastoma. N Engl J Med. 2005;352(10):997–1003.
  • Roos WP, Batista LF, Naumann SC, et al. Apoptosis in malignant glioma cells triggered by the temozolomide-induced DNA lesion O6-methylguanine. Oncogene. 2007;26(2):186–197.
  • Kanzawa T, Germano IM, Komata T, et al. Role of autophagy in temozolomide-induced cytotoxicity for malignant glioma cells. Cell Death Differ. 2004;11(4):448–457.
  • Hirose Y, Berger MS, Pieper RO. Abrogation of the Chk1-mediated G(2) checkpoint pathway potentiates temozolomide-induced toxicity in a p53-independent manner in human glioblastoma cells. Cancer Res. 2001;61(15):5843–5849.
  • Natelson EA, Pyatt D. Temozolomide-induced myelodysplasia. Adv Hematol. 2010;2010:1–5.
  • Schwarzberg AB, Stover EH, Sengupta T, et al. Selective lymphopenia and opportunistic infections in neuroendocrine tumor patients receiving temozolomide. Cancer Invest. 2007;25(4):249–255.
  • Su Y-W, Chang M-C, Chiang M-F, et al. Treatment-related myelodysplastic syndrome after temozolomide for recurrent high-grade glioma. J Neurooncol. 2005;71(3):315–318.
  • Bauer M, Goldstein M, Heylmann D, et al. Human monocytes undergo excessive apoptosis following temozolomide activating the ATM/ATR pathway while dendritic cells and macrophages are resistant. PLoS One. 2012;7(6):e39956.
  • Banissi C, Ghiringhelli F, Chen L, et al. Treg depletion with a low-dose metronomic temozolomide regimen in a rat glioma model. Cancer Immunol Immunother. 2009;58(10):1627–1634.
  • Xu X, Stockhammer F, Schmitt A, et al. Therapeutical doses of temozolomide do not impair the function of dendritic cells and CD8+ T cells. Int J Oncol. 2012;40(3):764–772.
  • Kim C-H, Woo S-J, Park J-S, et al. Enhanced antitumour immunity by combined use of temozolomide and TAT-survivin pulsed dendritic cells in a murine glioma. Immunology. 2007;122(4):615–622.
  • De Vleeschouwer S, Van Calenbergh F, Demaerel P, et al. Transient local response and persistent tumor control in a child with recurrent malignant glioma: treatment with combination therapy including dendritic cell therapy. Case report. J Neurosurg. 2004;100(5 Suppl Pediatrics):492–497.
  • Liu G, Akasaki Y, Khong HT, et al. Cytotoxic T cell targeting of TRP-2 sensitizes human malignant glioma to chemotherapy. Oncogene. 2005;24(33):5226–5234.
  • Prins RM, Soto H, Konkankit V, et al. Gene expression profile correlates with T-cell infiltration and relative survival in glioblastoma patients vaccinated with dendritic cell immunotherapy. Clin Cancer Res. 2011;17(6):1603–1615.
  • Weaver AK, Liu X, Sontheimer H. Role for calcium-activated potassium channels (BK) in growth control of human malignant glioma cells. J Neurosci Res. 2004;78(2):224–234.
  • Ransom CB, Sontheimer H. BK channels in human glioma cells. J Neurophysiol. 2001;85(2):790–803.
  • Sontheimer H. An unexpected role for ion channels in brain tumor metastasis. Exp Biol Med (Maywood). 2008;233(7):779–791.
  • Debska G, Kicinska A, Dobrucki J, et al. Large-conductance K+ channel openers NS1619 and NS004 as inhibitors of mitochondrial function in glioma cells. Biochem Pharmacol. 2003;65(11):1827–1834.
  • Liu X, Chang Y, Reinhart PH, et al. Cloning and characterization of glioma BK, a novel BK channel isoform highly expressed in human glioma cells. J Neurosci. 2002;22(5):1840–1849.
  • Ge L, Hoa NT, Wilson Z, et al. Big Potassium (BK) ion channels in biology, disease and possible targets for cancer immunotherapy. Int Immunopharmacol. 2014;22(2):427–443.
  • Ge L, Hoa NT, Cornforth AN, et al. Glioma big potassium channel expression in human cancers and possible T cell epitopes for their immunotherapy. J Immunol. 2012;189(5):2625–2634.
  • Hoa NT, Ge L, Tajhya RB, et al. Small cell lung cancer cells express the late stage gBK tumor antigen: a possible immunotarget for the terminal disease. Am J Transl Res. 2014;6(3):188–205.
  • Hoa N, Ge L, Kuznetsov Y, et al. Glioma cells display complex cell surface topographies that resist the actions of cytolytic effector lymphocytes. J Immunol. 2010;185(8):4793–4803.
  • Dang AQ, Hoa NT, Ge L, et al. Using REMBRANDT to paint in the details of glioma biology: applications for future immunotherapy. In: Lichtor T, editor. Evolution of the Molecular Biology of Brain Tumors and the Therapeutic Implications. InTech; 2013. p. 167–200. doi:10.5772/50198
  • Arismendi-Morillo G, Hoa NT, Ge L, et al. Mitochondrial network in glioma’s invadopodia displays an activated state both in situ and in vitro: potential functional implications. Ultrastruct Pathol. 2012;36(6):409–414.
  • Nakada M, Nakamura H, Ikeda E, et al. Expression and tissue localization of membrane-type 1, 2, and 3 matrix metalloproteinases in human astrocytic tumors. Am J Pathol. 1999;154(2):417–428.
  • Fillmore HL, VanMeter TE, Broaddus WC. Membrane-type matrix metalloproteinases (MT-MMPs): expression and function during glioma invasion. J Neurooncol. 2001;53(2):187–202.
  • Thorns V, Walter GF, Thorns C. Expression of MMP-2, MMP-7, MMP-9, MMP-10 and MMP-11 in human astrocytic and oligodendroglial gliomas. Anticancer Res. 2003;23(5a):3937–3944.
  • Zhao H, Sokabe M. Tuning the mechanosensitivity of a BK channel by changing the linker length. Cell Res. 2008;18(8):871–878.
  • Steinle M, Palme D, Misovic M, et al. Ionizing radiation induces migration of glioblastoma cells by activating BK K(+) channels. Radiother Oncol. 2011;101(1):122–126.
  • Adams JC. Roles of fascin in cell adhesion and motility. Curr Opin Cell Biol. 2004;16(5):590–596.
  • Peraud A, Mondal S, Hawkins C, et al. Expression of fascin, an actin-bundling protein, in astrocytomas of varying grades. Brain Tumor Pathol. 2003;20(2):53–58.
  • Roma AA, Prayson RA. Fascin expression in 90 patients with glioblastoma multiforme. Ann Diagn Pathol. 2005;9(6):307–311.
  • Hashimoto Y, Ito T, Inoue H, et al. Prognostic significance of fascin overexpression in human esophageal squamous cell carcinoma. Clin Cancer Res. 2005;11(7):2597–2605.
  • Yoder BJ, Tso E, Skacel M, et al. The expression of fascin, an actin-bundling motility protein, correlates with hormone receptor-negative breast cancer and a more aggressive clinical course. Clin Cancer Res. 2005;11(1):186–192.
  • Hwang JH, Smith CA, Salhia B, et al. The role of fascin in the migration and invasiveness of malignant glioma cells. Neoplasia. 2008;10(2):149–159.
  • Machesky LM, Li A. Fascin: invasive filopodia promoting metastasis. Commun Integr Biol. 2010;3(3):263–270.
  • Li A, Dawson JC, Forero-Vargas M, et al. The actin-bundling protein fascin stabilizes actin in invadopodia and potentiates protrusive invasion. Curr Biol. 2010;20(4):339–345.
  • Hoa NT, Ge L, Erickson KL, et al. Fascin-1 knock-down of human glioma cells reduces their microvilli/filopodia expression while improving their susceptibility to lymphocyte-mediated cytotoxicity. Amer J Trans Res. 2015;7(2):271–284.
  • Heidrick ML, Ryan WL. Adenosine 3’,5’-cyclic monophosphate and contact inhibition. Cancer Res. 1971;31(9):1313–1315.
  • Zhang JG, Kruse CA, Driggers L, et al. Tumor antigen precursor protein profiles of adult and pediatric brain tumors identify potential targets for immunotherapy. J Neurooncol. 2008;88(1):65–76.
  • Zhang JG, Eguchi J, Kruse CA, et al. Antigenic profiling of glioma cells to generate allogeneic vaccines or dendritic cell-based therapeutics. Clin Cancer Res. 2007;13(2 Pt 1):566–575.
  • Chan CE, Odde DJ. Traction dynamics of filopodia on compliant substrates. Science. 2008;322(5908):1687–1691.
  • Ricart BG, Yang MT, Hunter CA, et al. Measuring traction forces of motile dendritic cells on micropost arrays. Biophys J. 2011;101(11):2620–2628.
  • Li R, Li G, Deng L, et al. IL-6 augments the invasiveness of U87MG human glioblastoma multiforme cells via up-regulation of MMP-2 and fascin-1. Oncol Rep. 2010;23(6):1553–1559.
  • Liu Q, Li G, Li R, et al. IL-6 promotion of glioblastoma cell invasion and angiogenesis in U251 and T98G cell lines. J Neurooncol. 2010;100(2):165–176.
  • Happold C, Roth P, Wick W, et al. Distinct molecular mechanisms of acquired resistance to temozolomide in glioblastoma cells. J Neurochem. 2012;122(2):444–455.
  • Sun S, Wong TS, Zhang XQ, et al. Protein alterations associated with temozolomide resistance in subclones of human glioblastoma cell lines. J Neurooncol. 2012;107(1):89–100.
  • Kitange GJ, Carlson BL, Schroeder MA, et al. Expression of CD74 in high grade gliomas: a potential role in temozolomide resistance. J Neurooncol. 2010;100(2):177–186.
  • Bocangel DB, Finkelstein S, Schold SC, et al. Multifaceted resistance of gliomas to temozolomide. Clin Cancer Res. 2002;8(8):2725–2734.
  • Hafting T, Sand O. Purinergic activation of BK channels in clonal kidney cells (Vero cells). Acta Physiol Scand. 2000 Oct;170(2):99–109.
  • Furlow PW, Zhang S, Soong TD, et al. Mechanosensitive pannexin-1 channels mediate microvascular metastatic cell survival. Nat Cell Biol. 2015;17(7):943–952.
  • Bringmann A, Pannicke T, Weick M, et al. Activation of P2Y receptors stimulates potassium and cation currents in acutely isolated human Müller (glial) cells. Glia. 2002;37(2):139–152.
  • Sedwick C, Short B. Tubulin transport pumps up cilia [biosights video]. Sedwick C, editor and producer. New York (NY): The Rockefeller University Press; 2015. MP4 video: 6.5min., sound, color.

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.