Abstract
Previous findings indicated that microtubule-binding protein tau and voltage-gated K+ (Kv) channels exhibit a regulatory role in cell proliferation. However, the possible interaction of tau with Kv channels remained obscure. In this report, transfection of tau plasmids into human neuroblastoma SK-N-SH cells caused a significant reduction in the messenger RNA (mRNA) levels of several Kv channels, including Kv2.1, Kv3.1, Kv5.1, Kv9.2, and KCNH4. Correspondingly, the Kv currents recorded using patch-clamp techniques were substantially declined in the tau-transfected SK-N-SH cells. Moreover, tau induction and treatment with the Kv channel blocker TEA (tetraethylammonium) were able to improve proliferation rates of SK-N-SH cells by 43.1 and 66.2 %, respectively. These data suggested that the tau-mediated alteration of Kv channels could be involved in its action on neural proliferation.
References
Arcangeli A, Bianchi L, Becchetti A, Faravelli L, Coronnello M, Mini E, Olivotto M, Wanke E (1995) A novel inward-rectifying K+ current with a cell-cycle dependence governs the resting potential of mammalian neuroblastoma cells. J Physiol 489(Pt 2):455–471
Avila J, Lucas JJ, Perez M, Hernandez F (2004) Role of tau protein in both physiological and pathological conditions. Physiol Rev 84(2):361–384. doi:10.1152/physrev.00024.2003
Brandt R, Leger J, Lee G (1995) Interaction of tau with the neural plasma membrane mediated by tau’s amino-terminal projection domain. J Cell Biol 131(5):1327–1340
Burg ED, Remillard CV, Yuan JX (2006) K+ channels in apoptosis. J Membr Biol 209(1):3–20. doi:10.1007/s00232-005-0838-4
Chetty CS, Vemuri MC, Reddy GR, Suresh C (2007) Protective effect of 17-beta-estradiol in human neurocellular models of lead exposure. Neurotoxicology 28(2):396–401. doi:10.1016/j.neuro.2006.03.012
Drechsel DN, Hyman AA, Cobb MH, Kirschner MW (1992) Modulation of the dynamic instability of tubulin assembly by the microtubule-associated protein tau. Mol Biol Cell 3(10):1141–1154
Ferreira A, Caceres A (1991) Estrogen-enhanced neurite growth: evidence for a selective induction of Tau and stable microtubules. J Neurosci 11(2):392–400
Fieber LA, Gonzalez DM, Wallace MR, Muir D (2003) Delayed rectifier K currents in NF1 Schwann cells. Pharmacological block inhibits proliferation. Neurobiol Dis 13(2):136–146
Guise S, Braguer D, Remacle-Bonnet M, Pommier G, Briand C (1999) Tau protein is involved in the apoptotic process induced by anti-microtubule agents on neuroblastoma cells. Apoptosis 4(1):47–58
Hong XP, Peng CX, Wei W, Tian Q, Liu YH, Yao XQ, Zhang Y, Cao FY, Wang Q, Wang JZ (2010) Essential role of tau phosphorylation in adult hippocampal neurogenesis. Hippocampus 20(12):1339–1349. doi:10.1002/hipo.20712
Ikeda H, Taira N, Hara F, Fujita T, Yamamoto H, Soh J, Toyooka S, Nogami T, Shien T, Doihara H, Miyoshi S (2010) The estrogen receptor influences microtubule-associated protein tau (MAPT) expression and the selective estrogen receptor inhibitor fulvestrant downregulates MAPT and increases the sensitivity to taxane in breast cancer cells. Breast Cancer Res 12(3):R43. doi:10.1186/bcr2598
Lang F, Foller M, Lang KS, Lang PA, Ritter M, Gulbins E, Vereninov A, Huber SM (2005) Ion channels in cell proliferation and apoptotic cell death. J Membr Biol 205(3):147–157. doi:10.1007/s00232-005-0780-5
Lee VM, Balin BJ, Otvos L Jr, Trojanowski JQ (1991) A68: a major subunit of paired helical filaments and derivatized forms of normal Tau. Science 251(4994):675–678
Moschner K, Sundermann F, Meyer H, da Graca AP, Appel N, Paululat A, Bakota L, Brandt R (2014) RNA protein granules modulate tau isoform expression and induce neuronal sprouting. J Biol Chem 289(24):16814–16825. doi:10.1074/jbc.M113.541425
Ouadid-Ahidouch H, Chaussade F, Roudbaraki M, Slomianny C, Dewailly E, Delcourt P, Prevarskaya N (2000) KV1.1 K+ channels identification in human breast carcinoma cells: involvement in cell proliferation. Biochem Biophys Res Commun 278(2):272–277. doi:10.1006/bbrc.2000.3790
Perez M, Santa-Maria I, Gomez de Barreda E, Zhu X, Cuadros R, Cabrero JR, Sanchez-Madrid F, Dawson HN, Vitek MP, Perry G, Smith MA, Avila J (2009) Tau—an inhibitor of deacetylase HDAC6 function. J Neurochem 109(6):1756–1766. doi:10.1111/j.1471-4159.2009.06102.x
Rouzaire-Dubois B, Dubois JM (1990) Tamoxifen blocks both proliferation and voltage-dependent K+ channels of neuroblastoma cells. Cell Signal 2(4):387–393
Rouzier R, Rajan R, Wagner P, Hess KR, Gold DL, Stec J, Ayers M, Ross JS, Zhang P, Buchholz TA, Kuerer H, Green M, Arun B, Hortobagyi GN, Symmans WF, Pusztai L (2005) Microtubule-associated protein tau: a marker of paclitaxel sensitivity in breast cancer. Proc Natl Acad Sci U S A 102(23):8315–8320. doi:10.1073/pnas.0408974102
Schoenfeld TA, Obar RA (1994) Diverse distribution and function of fibrous microtubule-associated proteins in the nervous system. Int Rev Cytol 151:67–137
Vest RS, Pike CJ (2013) Gender, sex steroid hormones, and Alzheimer’s disease. Horm Behav 63(2):301–307. doi:10.1016/j.yhbeh.2012.04.006
Witman GB, Cleveland DW, Weingarten MD, Kirschner MW (1976) Tubulin requires tau for growth onto microtubule initiating sites. Proc Natl Acad Sci U S A 73(11):4070–4074
Wonderlin WF, Strobl JS (1996) Potassium channels, proliferation and G1 progression. J Membr Biol 154(2):91–107
Wu WK, Li GR, Wong HP, Hui MK, Tai EK, Lam EK, Shin VY, Ye YN, Li P, Yang YH, Luo JC, Cho CH (2006) Involvement of Kv1.1 and Nav1.5 in proliferation of gastric epithelial cells. J Cell Physiol 207(2):437–444. doi:10.1002/jcp.20576
Yi BA, Minor DL Jr, Lin YF, Jan YN, Jan LY (2001) Controlling potassium channel activities: interplay between the membrane and intracellular factors. Proc Natl Acad Sci U S A 98(20):11016–11023. doi:10.1073/pnas.191351798
Acknowledgments
This work was supported by the grants from the research project of MOE of PRC [BZY13030].
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Hu, XM., Li, XQ. & Li, XT. The Tau-Induced Reduction of mRNA Levels of Kv Channels in Human Neuroblastoma SK-N-SH Cells. J Mol Neurosci 58, 306–311 (2016). https://doi.org/10.1007/s12031-015-0683-6
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s12031-015-0683-6