TRPC6 channel-mediated neurite outgrowth in PC12 cells and hippocampal neurons involves activation of RAS/MEK/ERK, PI3K, and CAMKIV signaling

Journal of Neurochemistry

Volumn 127, Issue 3, 2013, Pages 303-313

  Heiser, Jeanine H ^a   Schuwald, Anita M ^a   Sillani, Giacomo ^a   Ye, Lian ^b   Müller, Walter E ^a   Leuner, Kristina ^b  

^a GOETHE UNIVERSITY   (Germany)

^b UNIVERSITY OF ERLANGEN NUREMBERG   (Germany)

Author keywords

calcium; hyperforin; neuritic outgrowth; synaptic plasticity; TRPC6 channels

Indexed keywords

CALCIUM CALMODULIN DEPENDENT PROTEIN KINASE IV; CYCLIC AMP RESPONSIVE ELEMENT BINDING PROTEIN; MITOGEN ACTIVATED PROTEIN KINASE; PHOSPHATIDYLINOSITOL 3 KINASE; PROTEIN KINASE B; RAS PROTEIN; TRANSIENT RECEPTOR POTENTIAL CHANNEL 6;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BRAIN NERVE CELL; CALCIUM CELL LEVEL; CALCIUM TRANSPORT; CELL DIFFERENTIATION; CELL TYPE; CONTROLLED STUDY; DOWN REGULATION; HIPPOCAMPAL CA1 REGION; NERVE CELL PLASTICITY; NERVE FIBER GROWTH; NONHUMAN; PC12 CELL; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; PROTEIN TARGETING; RAT; SIGNAL TRANSDUCTION;

CALCIUM; HYPERFORIN; NEURITIC OUTGROWTH; SYNAPTIC PLASTICITY; TRPC6 CHANNELS;

ANIMALS; ANTI-BACTERIAL AGENTS; BLOTTING, WESTERN; CALCIUM-CALMODULIN-DEPENDENT PROTEIN KINASE TYPE 2; CALCIUM-CALMODULIN-DEPENDENT PROTEIN KINASE TYPE 4; CYCLIC AMP RESPONSE ELEMENT-BINDING PROTEIN; ENZYME ACTIVATION; ENZYME-LINKED IMMUNOSORBENT ASSAY; EXTRACELLULAR SIGNAL-REGULATED MAP KINASES; GENES, RAS; HIPPOCAMPUS; MAP KINASE SIGNALING SYSTEM; NEURITES; NEURONS; ONCOGENE PROTEIN V-AKT; PC12 CELLS; PHLOROGLUCINOL; PHOSPHATIDYLINOSITOL 3-KINASES; PHOSPHORYLATION; PRIMARY CELL CULTURE; RATS; TERPENES; TRPC CATION CHANNELS;

EID: 84886020200     PISSN: 00223042     EISSN: 14714159     Source Type: Journal    
DOI: 10.1111/jnc.12376     Document Type: Article

References (54)

1. 2+, and calmodulin. Cell. Signal. 14, 649-654.
2. Alonso M., Medina J. H., and, Pozzo-Miller L., (2004) ERK1/2 activation is necessary for BDNF to increase dendritic spine density in hippocampal CA1 pyramidal neurons. Learn. Mem. 11, 172-178.
3. Amaral M. D., and, Pozzo-Miller L., (2007) TRPC3 channels are necessary for brain-derived neurotrophic factor to activate a nonselective cationic current and to induce dendritic spine formation. J. Neurosci. 27, 5179-5189.
4. Beitner-Johnson D., Leibold J., and, Millhorn D. E., (1998) Hypoxia regulates the cAMP- and Ca2+/calmodulin signaling systems in PC12 cells. Biochem. Biophys. Res. Commun. 242, 61-66.
5. Brunn G. J., Williams J., Sabers C., Wiederrecht G., Lawrence J. C., and, Abraham R. T., (1996) Direct inhibition of the signaling functions of the mammalian target of rapamycin by the phosphoinositide 3-kinase inhibitors, wortmannin and LY294002. EMBO J. 15, 5256-5267.
6. Chen A. C. H., Shirayama Y., Shin K. H., Neve R. L., and, Duman R. S., (2001) Expression of the cAMP response element binding protein (CREB) in hippocampus produces an antidepressant effect. Biol. Psychiatry 49, 753-762.
7. Chung J. H., Kubota H., Ozaki Y., Uda S., and, Kuroda S,. (2010) Timing-dependent actions of NGF required for cell differentiation. PLoS ONE 5, e9011. doi: 10.1371.
8. Cowen D. S., (2007) Serotonin and neuronal growth factors-a convergence of signaling pathways. J. Neurochem. 101, 1161-1171.
9. Cullen P. J., (2006) Decoding complex Ca2+ signals through the modulation of Ras signaling. Curr. Opin. Cell Biol. 18, 157-161.
10. Cullen P. J., and, Lockyer P. J., (2002) Integration of calcium and Ras signalling. Nat. Rev. Mol. Cell Biol. 3, 339-348.
11. Dinamarca M. C., Cerpa W., Garrido J., Hancke J. L., and, Inestrosa N. C., (2006) Hyperforin prevents beta-amyloid neurotoxicity and spatial memory impairments by disaggregation of Alzheimer's amyloid-beta-deposits. Mol. Psychiatry 11, 1032-1048.
12. Dolmetsch R. E., Pajvani U., Fife K., Spotts J. M., and, Greenberg M. E., (2001) Signaling to the nucleus by an L-type calcium channel-calmodulin complex through the MAP kinase pathway. Science 294, 333-339.
13. Du W., Huang J., Yao H., Zhou K., Duan B., and, Wang Y., (2010) Inhibition of TRPC6 degradation suppresses ischemic brain damage in rats. J. Clin. Invest. 120, 3480-3492.
14. Duman C. H., Schlesinger L., Kodama M., Russell D. S., and, Duman R. S., (2007) A role for MAP kinase signaling in behavioral models of depression and antidepressant treatment. Biol. Psychiatry 61, 661-670.
15. Duric V., Banasr M., Licznerski P., Schmidt H. D., Stockmeier C. A., Simen A. A., Newton S. S., and, Duman R. S., (2010) A negative regulator of MAP kinase causes depressive behavior. Nat. Med. 16, 1328-1332.
16. El Hassar L., Hagenston A. M., D'Angelo L. B., and, Yeckel M. F., (2011) Metabotropic glutamate receptors regulate hippocampal CA1 pyramidal neuron excitability via Ca(2) wave-dependent activation of SK and TRPC channels. J. Physiol. 589, 3211-3229.
17. Favata M. F., Horiuchi K. Y., Manos E. J., et al,. (1998) Identification of a novel inhibitor of mitogen-activated protein kinase kinase. J. Biol. Chem. 273, 18623-18632.
18. Fukushima H., Maeda R., Suzuki R., et al,. (2008) Upregulation of calcium/calmodulin-dependent protein kinase IV improves memory formation and rescues memory loss with aging. J. Neurosci. 28, 9910-9919.
19. Gibon J., Tu P., and, Bouron A., (2010) Store-depletion and hyperforin activate distinct types of Ca(2+)-conducting channels in cortical neurons. Cell Calcium 47, 538-543.
20. Gibon J., Deloulme J. C., Chevallier T., Ladeveze E., Abrous D. N., and, Bouron A., (2013) The antidepressant hyperforin increases the phosphorylation of CREB and the expression of TrkB in a tissue-specific manner. Int. J. Neuropsychopharmacol. 16, 189-198.
21. Greka A., Navarro B., Oancea E., Duggan A., and, Clapham D. E., (2003) TRPC5 is a regulator of hippocampal neurite length and growth cone morphology. Nat. Neurosci. 6, 837-845.
22. Ho N., Liauw J. A., Blaeser F., et al,. (2000) Impaired synaptic plasticity and cAMP response element-binding protein activation in Ca2+/calmodulin-dependent protein kinase type IV/Gr-deficient mice. J. Neurosci. 20, 6459-6472.
23. Hofmann T., Schaefer M., Schultz G., and, Gudermann T., (2002) Subunit composition of mammalian transient receptor potential channels in living cells. Proc. Natl Acad. Sci. USA 99, 7461-7466.
24. Jia Y., Zhou J., Tai Y., and, Wang Y., (2007) TRPC channels promote cerebellar granule neuron survival. Nat. Neurosci. 10, 559-567.
25. Jin S. X., and, Feig L. A., (2010) Long-term potentiation in the CA1 hippocampus induced by NR2A subunit-containing NMDA glutamate receptors is mediated by Ras-GRF2/Erk map kinase signaling. PLoS ONE 5, e11732.
26. Koch J. M., Hinze-Selch D., Huchzermeier C., Schulz-Du Bois A. C., and, Aldenhoff J. B., (2005) The association of CREB-phosphorylation and treatment-response in depression: Findings in pharmacological and non-pharmacological treatment. Pharmacopsychiatry 38, 255.
27. Koch J. M., Hinze-Selch D., Stingele K., Huchzermeier C., Goder R., Seeck-Hirschner M., and, Aldenhoff J. B., (2009) Changes in CREB phosphorylation and BDNF plasma levels during psychotherapy of depression. Psychother. Psychosom. 78, 187-192.
28. Koh Y. H., Ruiz-Canada C., Gorczyca M., and, Budnik V., (2002) The Ras1-mitogen-activated protein kinase signal transduction pathway regulates synaptic plasticity through fasciclin II-mediated cell adhesion. J. Neurosci. 22, 2496-2504.
29. Kumar V., Zhang M. X., Swank M. W., Kunz J., and, Wu G. Y., (2005) Regulation of dendritic morphogenesis by Ras-PI3K-Akt-mTOR and Ras-MAPK signaling pathways. J. Neurosci. 25, 11288-11299.
30. Leuner K., Kazanski V., Muller M., Essin K., Henke B., Gollasch M., Harteneck C., and, Muller W. E., (2007) Hyperforin a key constituent of St. John's wort specifically activates TRPC6 channels. FASEB J. 21, 4101-4111.
31. Leuner K., Heiser J. H., Derksen S., et al,. (2010) Simple 2,4-diacylphloroglucinols as classic transient receptor potential-6 activators-identification of a novel pharmacophore. Mol. Pharmacol. 77, 368-377.
32. Leuner K., Li W., Amaral M. D., Rudolph S., Calfa G., Schuwald A. M., Harteneck C., Inoue T., and, Pozzo-Miller L., (2013) Hyperforin modulates dendritic spine morphology in hippocampal pyramidal neurons by activating Ca(2+) -permeable TRPC6 channels. Hippocampus 23, 40-52.
33. Li Y., Jia Y. C., Cui K., Li N., Zheng Z. Y., Wang Y. Z., and, Yuan X. B., (2005) Essential role of TRPC channels in the guidance of nerve growth cones by brain-derived neurotrophic factor. Nature 434, 894-898.
34. Li Y., Calfa G., Inoue T., Amaral M. D., and, Pozzo-Miller L., (2010) Activity-dependent release of endogenous BDNF from mossy fibers evokes a TRPC3 current and Ca2+ elevations in CA3 pyramidal neurons. J. Neurophysiol. 103, 2846-2856.
35. Lin Y., Zhang J. C., Fu J., Chen F., Wang J., Wu Z. L., and, Yuan S. Y., (2013) Hyperforin attenuates brain damage induced by transient middle cerebral artery occlusion (MCAO) in rats via inhibition of TRPC6 channels degradation. J. Cereb. Blood Flow Metab. 33, 253-262.
36. Lonze B. E., and, Ginty D. D., (2002) Function and regulation of CREB family transcription factors in the nervous system. Neuron 35, 605-623.
37. Miranti C. K., Ginty D. D., Huang G., Chatila T., and, Greenberg M. E., (1995) Calcium activates serum response factor-dependent transcription by a Ras- and Elk-1-independent mechanism that involves a Ca2+/calmodulin-dependent kinase. Mol. Cell. Biol. 15, 3672-3684.
38. Muller W. E., (2003) Current St John's wort research from mode of action to clinical efficacy. Pharmacol. Res. 47, 101-109.
39. Pang L., Sawada T., Decker S. J., and, Saltiel A. R., (1995) Inhibition of Map kinase kinase blocks the differentiation of Pc-12 cells induced by nerve growth-factor. J. Biol. Chem. 270, 13585-13588.
40. Pittenger C., and, Duman R. S., (2008) Stress, depression, and neuroplasticity: a convergence of mechanisms. Neuropsychopharmacology 33, 88-109.
41. Riccio A., Medhurst A. D., Mattei C., Kelsell R. E., Calver A. R., Randall A. D., Benham C. D., and, Pangalos M. N., (2002) mRNA distribution analysis of human TRPC family in CNS and peripheral tissues. Mol. Brain Res. 109, 95-104.
42. Riese U., Ziegler E., and, Hamburger M., (2004) Militarinone A induces differentiation in PC12 cells via MAP and Akt kinase signal transduction pathways. FEBS Lett. 577, 455-459.
43. Sakai T., Furuyama T., Ohoka Y., Miyazaki N., Fujioka S., Sugimoto H., Amasaki M., Hattori S., Matsuya T., and, Inagaki S., (1999) Mouse semaphorin H induces PC12 cell neurite outgrowth activating Ras-mitogen-activated protein kinase signaling pathway via Ca(2+) influx. J. Biol. Chem. 274, 29666-29671.
44. Santos A. R., Comprido D., and, Duarte C. B., (2010) Regulation of local translation at the synapse by BDNF. Prog. Neurobiol. 92, 505-516.
45. Tai Y., Feng S., Ge R., Du W., Zhang X., He Z., and, Wang Y., (2008) TRPC6 channels promote dendritic growth via the CaMKIV-CREB pathway. J. Cell Sci. 121, 2301-2307.
46. Takao K., Tanda K., Nakamura K., et al,. (2010) Comprehensive behavioral analysis of calcium/calmodulin-dependent protein kinase IV knockout mice. PLoS ONE 5, e9460.
47. Takeda K., and, Ichijo H., (2002) Neuronal p38 MAPK signalling: an emerging regulator of cell fate and function in the nervous system. Genes Cells 7, 1099-1111.
48. Treiber K., Singer A., Henke B., and, Muller W. E., (2005) Hyperforin activates nonselective cation channels (NSCCs). Br. J. Pharmacol. 145, 75-83.
49. Trofimiuk E., Holownia A., and, Braszko J. J., (2010) Activation of CREB by St. John's wort may diminish deletorious effects of aging on spatial memory. Arch. Pharmacal Res. 33, 469-477.
50. Vaudry D., Stork P. J. S., Lazarovici P., and, Eiden L. E., (2002) Signaling pathways for PC12 cell differentiation: making the right connections. Science 296, 1648-1649.
51. Venkatachalam K., and, Montell C., (2007) TRP channels. Annu. Rev. Biochem. 76, 387-417.
52. Wayman G. A., Lee Y. S., Tokumitsu H., Silva A. J., and, Soderling T. R., (2008) Calmodulin-kinases: modulators of neuronal development and plasticity. Neuron 59, 914-931.
53. Wei F., Qiu C. S., Liauw J., Robinson D. A., Ho N., Chatila T., and, Zhuo M., (2002) Calcium calmodulin-dependent protein kinase IV is required for fear memory. Nat. Neurosci. 5, 573-579.
54. Zhou J., Du W., Zhou K., Tai Y., Yao H., Jia Y., Ding Y., and, Wang Y., (2008) Critical role of TRPC6 channels in the formation of excitatory synapses. Nat. Neurosci. 11, 741-743.