Telephone: 608-265-2543; Fax: 608-263-5267
Embryonic Stem Cells/Induced Pluripotent Stem Cells
Article first published online: 1 SEP 2009
Copyright © 2009 AlphaMed Press
Volume 27, Issue 12, pages 2906–2916, December 2009
How to Cite
Weick, J. P., Austin Johnson, M. and Zhang, S.-C. (2009), Developmental Regulation of Human Embryonic Stem Cell-Derived Neurons by Calcium Entry via Transient Receptor Potential Channels. STEM CELLS, 27: 2906–2916. doi: 10.1002/stem.212
Author contributions: J.P.W. and M.A.J.: conception and design, collection and/or assembly of data, data analysis and interpretation, manuscript writing, final approval of manuscript; J.P.W. and M.A.J. contributed equally to this work; S.-C.Z.: conception and design, financial support, data analysis and interpretation, manuscript writing, final approval of manuscript.
First published online in STEM CELLS EXPRESS September 1, 2009.
Disclosure of potential conflicts of interest is found at the end of this article.
- Issue published online: 14 DEC 2009
- Article first published online: 1 SEP 2009
- Accepted manuscript online: 1 SEP 2009 12:00AM EST
- Manuscript Accepted: 16 AUG 2009
- Manuscript Received: 29 MAY 2009
- NINDS, NS. Grant Number: 045926
- Waisman Center from the National Institute of Child Health and Human Development. Grant Number: HD03352
- Rath Distinguished Graduate Student Fellowship
- NIH Stem Cell Training Grant. Grant Number: NIH T32AG027566-01
- 1Spontaneous neuronal calcium spikes and waves during early differentiation. J Neurosci 1994; 14: 6325– 6335., , .
- 2Ca2+ influx through mechanosensitive channels inhibits neurite outgrowth in opposition to other influx pathways and release from intracellular stores. J Neurosci 2006; 26: 5656–5664., , et al.
- 3Intracellular Ca2+ fluctuations modulate the rate of neuronal migration. Neuron 1996; 17: 275–285., .
- 4L-type calcium channel activation controls the in vivo transduction of the neuralizing signal in the amphibian embryos. Mech Dev 1997; 64: 105–110., , et al.
- 5Calcium waves propagate through radial glial cells and modulate proliferation in the developing neocortex. Neuron 2004; 43: 647–661., , et al.
- 6Patterns of intracellular calcium fluctuation in precursor cells of the neocortical ventricular zone. J Neurosci 1998; 18: 5374–5388., .
- 7Local calcium signaling in neurons. Neuron 2003; 40: 331–346., , .
- 8Transient receptor potential cation channels in disease. Physiol Rev 2007; 87: 165–217., , et al.
- 9Trp, a novel mammalian gene family essential for agonist-activated capacitative Ca2+ entry. Cell 1996; 85: 661–671., , et al.
- 10[Ca2+]i inhibition of Ca2+ release-activated Ca2+ influx underlies agonist- and thapsigargin-induced [Ca2+]i oscillations in salivary acinar cells. J Biol Chem 1994; 269: 31525–31532., .
- 11Repetitive transient rises in cytoplasmic free calcium in hormone-stimulated hepatocytes. Nature 1986; 319: 600–602., , .
- 12TRP channels as cellular sensors. Nature 2003; 426: 517–524..
- 13Essential role for TRPC5 in amygdala function and fear-related behavior. Cell 2009; 137: 761–772., , et al.
- 14A point mutation in TRPC3 causes abnormal Purkinje cell development and cerebellar ataxia in moonwalker mice. Proc Natl Acad Sci U S A 2009; 106: 6706–6711., , et al.
- 15Canonical transient receptor potential 1 plays a role in basic fibroblast growth factor (bFGF)/FGF receptor-1-induced Ca2+ entry and embryonic rat neural stem cell proliferation. J Neurosci 2005; 25: 2687–2701., , et al.
- 16TRPC5 is a regulator of hippocampal neurite length and growth cone morphology. Nat Neurosci 2003; 6: 837–845., , et al.
- 17TRPC4 in rat dorsal root ganglion neurons is increased after nerve injury and is necessary for neurite outgrowth. J Biol Chem 2008; 283: 416–426., , et al.
- 18The molecular basis for calcium-dependent axon pathfinding. Nat Rev Neurosci 2006; 7: 115–125., .
- 19Functional neural development from human embryonic stem cells: Accelerated synaptic activity via astrocyte coculture. J Neurosci 2007; 27: 3069–3077., , et al.
- 20In vitro differentiation of transplantable neural precursors from human embryonic stem cells. Nat Biotechnol 2001; 19: 1129–1133., , et al.
- 21Signaling from synapse to nucleus: Postsynaptic CREB phosphorylation during multiple forms of hippocampal synaptic plasticity. Neuron 1996; 16: 89–101., , .
- 22Specification of motoneurons from human embryonic stem cells. Nat Biotechnol 2005; 23: 215–221., , et al.
- 23Interaction between TRPC channel subunits in endothelial cells. J Recept Signal Transduct Res 2006; 26: 225–240., , et al.
- 24Glutamate enhances proliferation and neurogenesis in human neural progenitor cell cultures derived from the fetal cortex. Eur J Neurosci 2006; 24: 645–653., , et al.
- 25Human embryonic stem cell-derived motor neurons expressing SOD1 mutants exhibit typical signs of motor neuron degeneration linked to ALS. Dis Model Mech 2009; 2: 189–195., , et al.
- 26Directed neural differentiation of human embryonic stem cells via an obligated primitive anterior stage. Stem Cells 2007; 25: 1511–1520., , et al.
- 27Transgenes delivered by lentiviral vector are suppressed in human embryonic stem cells in a promoter-dependent manner. Stem Cells Dev 2007; 16: 167–176., , et al.
- 28Human ES cell-derived neural rosettes reveal a functionally distinct early neural stem cell stage. Genes Dev 2008; 22: 152–165., , et al.
- 29Human cortical neurons originate from radial glia and neuron-restricted progenitors. J Neurosci 2007; 27: 4132–4145., , et al.
- 30Dividing precursor cells of the embryonic cortical ventricular zone have morphological and molecular characteristics of radial glia. J Neurosci 2002; 22: 3161–3173., , et al.
- 31Elusive radial glial cells: Historical and evolutionary perspective. Glia 2003; 43: 19–32..
- 32ThermoTRP channels and beyond: Mechanisms of temperature sensation. Nat Rev Neurosci 2003; 4: 529–539., , et al.
- 33Activation of TRPV4 channels (hVRL-2/mTRP12) by phorbol derivatives. J Biol Chem 2002; 277: 13569–13577., , et al.
- 34Activation of the TRPC1 cation channel by metabotropic glutamate receptor mGluR1. Nature 2003; 426: 285–291., , et al.
- 35Requirement of TRPC channels in netrin-1-induced chemotropic turning of nerve growth cones. Nature 2005; 434: 898–904., .
- 36Hippocampal astrocytes in situ exhibit calcium oscillations that occur independent of neuronal activity. J Neurophysiol 2002; 87: 528–537., , .
- 37ATP released via gap junction hemichannels from the pigment epithelium regulates neural retinal progenitor proliferation. Neuron 2005; 46: 731–744., , et al.
- 38Directed differentiation of ventral spinal progenitors and motor neurons from human embryonic stem cells by small molecules. Stem Cells 2008; 26: 886–893., , et al.
- 39Endogenous TRPC1, TRPC3, and TRPC7 proteins combine to form native store-operated channels in HEK-293 cells. J Biol Chem 2005; 280: 29559–29569., , .
- 40Guiding neuronal growth cones using Ca2+ signals. Trends Cell Biol 2004; 14: 320–330., .
- 41Translocation of calmodulin to the nucleus supports CREB phosphorylation in hippocampal neurons. Nature 1998; 392: 198–202., , .
- 42Buffering of calcium in the vicinity of a channel pore. Cell Calcium 1992; 13: 183–192..
- 43Rescue of the Drosophila phototransduction mutation trp by germline transformation. Science 1985; 230: 1040–1043., , et al.
- 44A transient receptor potential-like channel mediates synaptic transmission in rod bipolar cells. J Neurosci 2009; 29: 6088–6093., , et al.
- 45TRPC channels promote cerebellar granule neuron survival. Nat Neurosci 2007; 10: 559–567., , et al.
- 46Calcium transients and neural induction in vertebrates. Cell Calcium 2005; 37: 375–385., , et al.
- 47Endothelin-1-mediated wave-like [Ca2+]i oscillations in intact rabbit inferior vena cava. J Vasc Res 2007; 44: 495–503., , et al.
- 48Asynchronous Ca(2+) waves in intact venous smooth muscle. Circ Res 2000; 86: E72–E79., , et al.
- 49TRPM4 regulates calcium oscillations after T cell activation. Science 2004; 306: 1374–1377., , et al.
- 50Transient receptor potential 1 regulates capacitative Ca(2+) entry and Ca(2+) release from endoplasmic reticulum in B lymphocytes. J Exp Med 2002; 195: 673–681., , et al.
- 51Translating developmental time across mammalian species. Neuroscience 2001; 105: 7–17., , .
- 52Cell-cycle control and cortical development. Nat Rev Neurosci 2007; 8: 438–450., .
- 53TRPC1 forms the stretch-activated cation channel in vertebrate cells. Nat Cell Biol 2005; 7: 179–185., , et al.
- 54Calcium channel modulation as an all-purpose mechanism for short-term synaptic plasticity. Neuron 2008; 57: 171–172., .
- 55TRPC1 and TRPC5 form a novel cation channel in mammalian brain. Neuron 2001; 29: 645–655., , et al.
- 56Essential role of filopodia in chemotropic turning of nerve growth cone induced by a glutamate gradient. J Neurosci 1996; 16: 1140–1149., , .
- 57A critical importance of polyamine site in NMDA receptors for neurite outgrowth and fasciculation at early stages of P19 neuronal differentiation. Exp Cell Res 2008; 314: 2603–2617., , et al.
- 58Regulation of nerve growth mediated by inositol 1,4,5-trisphosphate receptors in growth cones. Science 1998; 282: 1705–1708., , et al.
- 59Human embryonic stem cell-derived dopaminergic neurons reverse functional deficit in Parkinsonian rats. Stem Cells 2008; 26: 55–63., , et al.
- 60Functional engraftment of human ES cell-derived dopaminergic neurons enriched by coculture with telomerase-immortalized midbrain astrocytes. Nat Med 2006; 12: 1259–1268., , et al.
- 61TRPC5 as a candidate for the nonselective cation channel activated by muscarinic stimulation in murine stomach. Am J Physiol Gastrointest Liver Physiol 2003; 284: G604–G616., , et al.
- 622APB, 2-aminoethoxydiphenyl borate, a membrane-penetrable modulator of Ins(1,4,5)P3-induced Ca2+ release. J Biochem 1997; 122: 498–505., , et al.
- 63Inhibition of the transient receptor potential cation channel TRPM2 by 2-aminoethoxydiphenyl borate (2-APB). Br J Pharmacol 2008; 153: 1324–1330., , .
- 64Nociceptor and hair cell transducer properties of TRPA1, a channel for pain and hearing. J Neurosci 2005; 25: 4052–4061., , et al.
- 65Molecular pathophysiology of mucolipidosis type IV: pH dysregulation of the mucolipin-1 cation channel. Hum Mol Genet 2004; 13: 617–627., , et al.
- 66Quinoxalinediones: Potent competitive non-NMDA glutamate receptor antagonists. Science 1988; 241: 701–703., , et al.
- 67Synaptic plasticity and learning: Selective impairment of learning rats and blockade of long-term potentiation in vivo by the N-methyl-D-aspartate receptor antagonist AP5. J Neurosci 1989; 9: 3040–3057..
- 68Expression and modulation of voltage-gated calcium channels after RNA injection in Xenopus oocytes. Science 1986; 231: 1147–1150., , et al.
- 69A neuronal nicotinic acetylcholine receptor subunit (α 7) is developmentally regulated and forms a homo-oligomeric channel blocked by α-BTX. Neuron 1990; 5: 847–856., , et al.
- 70Synaptic transmission at nicotinic acetylcholine receptors in rat hippocampal organotypic cultures and slices. J Physiol 1999; 515( Pt 3): 769–776., , et al.
- 71Flufenamic acid is a pH-dependent antagonist of TRPM2 channels. Neuropharmacology 2004; 47: 450–460., , et al.
- 72The transient receptor potential protein homologue TRP6 is the essential component of vascular α(1)-adrenoceptor-activated Ca(2+)-permeable cation channel. Circ Res 2001; 88: 325–332., , et al.
- 73Comparison of functional properties of the Ca2+-activated cation channels TRPM4 and TRPM5 from mice. Cell Calcium 2005; 37: 267–278., , et al.
- 74Stretch-activated cation channels of leech neurons exhibit two activity modes. Eur J Neurosci 2001; 13: 503–511., , .
- 75Identification of a peptide toxin from Grammostola spatulata spider venom that blocks cation-selective stretch-activated channels. J Gen Physiol 2000; 115: 583–598., , et al.
- 76The actions of orally active GABAB receptor antagonists on GABAergic transmission in vivo and in vitro. Eur J Pharmacol 1993; 233: 179–186., , et al.
- 77The effect of picrotoxin on peripheral inhibition in the crayfish. J Physiol 1958; 143: 541–552., .
- 78Localised calcium release events in cells from the muscle of guinea-pig gastric fundus. J Physiol 2004; 554: 687–705., .
- 79Regulation of a TRPM7-like current in rat brain microglia. J Biol Chem 2003; 278: 42867–42876., , .
- 80Polyunsaturated fatty acids activate the Drosophila light-sensitive channels TRP and TRPL. Nature 1999; 397: 255–259., , .
- 81Anandamide and arachidonic acid use epoxyeicosatrienoic acids to activate TRPV4 channels. Nature 2003; 424: 434–438., , et al.
- 82The role of endogenous human Trp4 in regulating carbachol-induced calcium oscillations in HEK-293 cells. J Biol Chem 2002; 277: 13597–13608., , et al.
- 83Activation of human TRPC6 channels by receptor stimulation. J Biol Chem 2004; 279: 22047–22056., , et al.
- 84Regulation of canonical transient receptor potential (TRPC) channel function by diacylglycerol and protein kinase C. J Biol Chem 2003; 278: 29031–29040., , .
- 85Activation of the melastatin-related cation channel TRPM3 by D-erythro-sphingosine [corrected]. Mol Pharmacol 2005; 67: 798–805., , et al.