Ion Channels in Regulation of Neuronal Regenerative Activities

Translational Stroke Research

Volumn 5, Issue 1, 2014, Pages 156-162

  Chen, Dongdong ^a   Yu, Shan Ping ^a   Wei, Ling ^a  

^a EMORY UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Ion channels; Migration; Neurogenesis; Proliferation; Stroke

Indexed keywords

ION CHANNEL;

ARTICLE; CELL DIFFERENTIATION; CELL MIGRATION; CELL PROLIFERATION; CEREBROVASCULAR ACCIDENT; GROWTH CONE; HUMAN; MYELINATION; NERVE REGENERATION; NERVOUS SYSTEM DEVELOPMENT; OLIGODENDROGLIA; PRIORITY JOURNAL; REGENERATIVE ABILITY; STEM CELL TRANSPLANTATION;

ANIMALS; CELL DIFFERENTIATION; CELL PROLIFERATION; HUMANS; ION CHANNELS; MICE; NEURONS; REGENERATION; STEM CELL TRANSPLANTATION; STEM CELLS;

EID: 84893744430     PISSN: 18684483     EISSN: 1868601X     Source Type: Journal    
DOI: 10.1007/s12975-013-0320-z     Document Type: Article

References (105)

1. Steward MM, Sridhar A, Meyer JS. Neural regeneration. Curr Top Microbiol Immunol. 2013;367: 163-91.
2. Horner PJ, Gage FH. Regenerating the damaged central nervous system. Nature. 2000;407(6807): 963-70.
3. Springer JE. Apoptotic cell death following traumatic injury to the central nervous system. J Biochem Mol Biol. 2002;35(1): 94-105.
4. Wei L et al. Necrosis, apoptosis and hybrid death in the cortex and thalamus after barrel cortex ischemia in rats. Brain Res. 2004;1022(1-2): 54-61.
5. Bahr M, Bonhoeffer F. Perspectives on axonal regeneration in the mammalian CNS. Trends Neurosci. 1994;17(11): 473-9.
6. Horner PJ, Gage FH. Regeneration in the adult and aging brain. Arch Neurol. 2002;59(11): 1717-20.
7. Kahle MP, Bix GJ. Neuronal restoration following ischemic stroke: influences, barriers, and therapeutic potential. Neurorehabil Neural Repair. 2013;27(5): 469-78.
8. Snyder EY et al. Multipotent neural precursors can differentiate toward replacement of neurons undergoing targeted apoptotic degeneration in adult mouse neocortex. Proc Natl Acad Sci U S A. 1997;94(21): 11663-8.
9. Drury-Stewart D et al. Highly efficient differentiation of neural precursors from human embryonic stem cells and benefits of transplantation after ischemic stroke in mice. Stem Cell Res Ther. 2013;4(4): 93.
10. Mohamad O et al. Vector-free and transgene-free human iPS cells differentiate into functional neurons and enhance functional recovery after ischemic stroke in mice. PLoS One. 2013;8(5): e64160.
11. Song M et al. Restoration of intracortical and thalamocortical circuits after transplantation of bone marrow mesenchymal stem cells into the ischemic brain of mice. Cell Transplant. 2012;22(11): 2001-15.
12. Wei N et al. Delayed intranasal delivery of hypoxic-preconditioned bone marrow mesenchymal stem cells enhanced cell homing and therapeutic benefits after ischemic stroke in mice. Cell Transplant. 2013;22(6): 977-91.
13. Wei L et al. Transplantation of hypoxia preconditioned bone marrow mesenchymal stem cells enhances angiogenesis and neurogenesis after cerebral ischemia in rats. Neurobiol Dis. 2012;46(3): 635-45.
14. Wei L et al. Transplantation of embryonic stem cells overexpressing bcl-2 promotes functional recovery after transient cerebral ischemia. Neurobiol Dis. 2005;19(1-2): 183-93.
15. Theus MH et al. In vitro hypoxic preconditioning of embryonic stem cells as a strategy of promoting cell survival and functional benefits after transplantation into the ischemic rat brain. Exp Neurol. 2008;210(2): 656-70.
16. Azevedo-Pereira RL, Daadi MM. Isolation and purification of self-renewable human neural stem cells for cell therapy in experimental model of ischemic stroke. Methods Mol Biol. 2013;1059: 157-67.
17. Kim SU, Lee HJ, Kim YB. Neural stem cell-based treatment for neurodegenerative diseases. Neuropathology. 2013;33: 491-504.
18. Marchionini DM et al. Reassessment of caspase inhibition to augment grafted dopamine neuron survival. Cell Transplant. 2004;13(3): 273-82.
19. Sortwell CE. Strategies for the augmentation of grafted dopamine neuron survival. Front Biosci. 2003;8: s522-32.
20. Sortwell CE et al. Effects of ex vivo transduction of mesencephalic reaggregates with bcl-2 on grafted dopamine neuron survival. Brain Res. 2007;1134(1): 33-44.
21. Tam RY et al. Regenerative therapies for central nervous system diseases: a biomaterials approach. Neuropsychopharmacology. 2013. doi: 10. 1038/npp. 2013. 237.
22. Park KI. Transplantation of neural stem cells: cellular & gene therapy for hypoxic-ischemic brain injury. Yonsei Med J. 2000;41(6): 825-35.
23. Lindvall O, Kokaia Z, Martinez-Serrano A. Stem cell therapy for human neurodegenerative disorders-how to make it work. Nat Med. 2004;10(Suppl): S42-50.
24. Hu X et al. Hypoxic preconditioning enhances bone marrow mesenchymal stem cell migration via Kv2. 1 channel and FAK activation. Am J Physiol Cell Physiol. 2011;301(2): C362-72.
25. Zhou X et al. Potential role of KCNQ/M-channels in regulating neuronal differentiation in mouse hippocampal and embryonic stem cell-derived neuronal cultures. Exp Neurol. 2011;229(2): 471-83.
26. Yu SP, Canzoniero LM, Choi DW. Ion homeostasis and apoptosis. Curr Opin Cell Biol. 2001;13(4): 405-11.
27. Purves DAG, Fitzpatrick D. Channels and transporter. In: Purves D, Augustine GJ, Fitzpatrick D, Katz LC, LaMantia A-S, McNamara JO, Williams SM, editors. Neuroscience. 2nd ed. Sunderland: Sinauer Associates, Inc; 2011.
28. Krupp JJ. Role of ion channels in neurological disorders. CNS Neurol Disord Drug Targets. 2008;7(2): 120-1.
29. Swayne LA, Wicki-Stordeur L. Ion channels in postnatal neurogenesis: potential targets for brain repair. Channels (Austin). 2012;6(2): 69-74.
30. Simanov D et al. The flatworm Macrostomum lignano is a powerful model organism for ion channel and stem cell research. Stem Cells Int. 2012;2012: 167265.
31. DeCoursey TE et al. Voltage-gated K+ channels in human T lymphocytes: a role in mitogenesis? Nature. 1984;307(5950): 465-8.
32. Wang E et al. Physiological electric fields control the G1/S phase cell cycle checkpoint to inhibit endothelial cell proliferation. FASEB J. 2003;17(3): 458-60.
33. Valero ML et al. TRPM8 ion channels differentially modulate proliferation and cell cycle distribution of normal and cancer prostate cells. PLoS One. 2012;7(12): e51825.
34. Cidad P et al. Kv1. 3 channels can modulate cell proliferation during phenotypic switch by an ion-flux independent mechanism. Arterioscler Thromb Vasc Biol. 2012;32(5): 1299-307.
35. Becchetti A. Ion channels and transporters in cancer. Ion channels and cell proliferation in cancer. Am J Physiol Cell Physiol. 2011;301(2): C255-65.
36. Lang F et al. Cell volume regulatory ion channels in cell proliferation and cell death. Methods Enzymol. 2007;428: 209-25.
37. Lang F et al. Ion channels in cell proliferation and apoptotic cell death. J Membr Biol. 2005;205(3): 147-57.
38. Scheffler B et al. Phenotypic and functional characterization of adult brain neuropoiesis. Proc Natl Acad Sci U S A. 2005;102(26): 9353-8.
39. Yasuda T, Bartlett PF, Adams DJ. K(ir) and K(v) channels regulate electrical properties and proliferation of adult neural precursor cells. Mol Cell Neurosci. 2008;37(2): 284-97.
40. Yasuda T, Cuny H, Adams DJ. Kv3. 1 channels stimulate adult neural precursor cell proliferation and neuronal differentiation. J Physiol. 2013;591(Pt 10): 2579-91.
41. Zhang YY et al. BK and hEag1 channels regulate cell proliferation and differentiation in human bone marrow-derived mesenchymal stem cells. J Cell Physiol. 2013;8(11): e79952.
42. Zhang J et al. Regulation of cell proliferation of human induced pluripotent stem cell-derived mesenchymal stem cells via ether-a-go-go 1 (hEAG1) potassium channel. Am J Physiol Cell Physiol. 2012;303(2): C115-25.
43. Linta L et al. Calcium activated potassium channel expression during human iPS cell-derived neurogenesis. Ann Anat. 2013;195(4): 303-11.
44. Kong H et al. AQP4 knockout impairs proliferation, migration and neuronal differentiation of adult neural stem cells. J Cell Sci. 2008;121(Pt 24): 4029-36.
45. Zheng GQ et al. Beyond water channel: aquaporin-4 in adult neurogenesis. Neurochem Int. 2010;56(5): 651-4.
46. Li M et al. A TRPC1-mediated increase in store-operated Ca2+ entry is required for the proliferation of adult hippocampal neural progenitor cells. Cell Calcium. 2012;51(6): 486-96.
47. Rosenberg SS, Spitzer NC. Calcium signaling in neuronal development. Cold Spring Harb Perspect Biol. 2011;3(10): a004259.
48. Henley JR et al. Calcium mediates bidirectional growth cone turning induced by myelin-associated glycoprotein. Neuron. 2004;44(6): 909-16.
49. Hong K et al. Calcium signalling in the guidance of nerve growth by netrin-1. Nature. 2000;403(6765): 93-8.
50. Shim S et al. XTRPC1-dependent chemotropic guidance of neuronal growth cones. Nat Neurosci. 2005;8(6): 730-5.
51. Tojima T. Intracellular signaling and membrane trafficking control bidirectional growth cone guidance. Neurosci Res. 2012;73(4): 269-74.
52. Michaelsen K, Lohmann C. Calcium dynamics at developing synapses: mechanisms and functions. Eur J Neurosci. 2010;32(2): 218-23.
53. Platel JC, Dave KA, Bordey A. Control of neuroblast production and migration by converging GABA and glutamate signals in the postnatal forebrain. J Physiol. 2008;586(16): 3739-43.
54. Li Y et al. Essential role of TRPC channels in the guidance of nerve growth cones by brain-derived neurotrophic factor. Nature. 2005;434(7035): 894-8.
55. Wang GX, Poo MM. Requirement of TRPC channels in netrin-1-induced chemotropic turning of nerve growth cones. Nature. 2005;434(7035): 898-904.
56. Greka A et al. TRPC5 is a regulator of hippocampal neurite length and growth cone morphology. Nat Neurosci. 2003;6(8): 837-45.
57. Li HS, Xu XZ, Montell C. Activation of a TRPC3-dependent cation current through the neurotrophin BDNF. Neuron. 1999;24(1): 261-73.
58. Shim S et al. Peptidyl-prolyl isomerase FKBP52 controls chemotropic guidance of neuronal growth cones via regulation of TRPC1 channel opening. Neuron. 2009;64(4): 471-83.
59. Kaczmarek JS, Riccio A, Clapham DE. Calpain cleaves and activates the TRPC5 channel to participate in semaphorin 3A-induced neuronal growth cone collapse. Proc Natl Acad Sci U S A. 2012;109(20): 7888-92.
60. Davare MA et al. Transient receptor potential canonical 5 channels activate Ca2+/calmodulin kinase Igamma to promote axon formation in hippocampal neurons. J Neurosci. 2009;29(31): 9794-808.
61. Heo DK et al. Opposite regulatory effects of TRPC1 and TRPC5 on neurite outgrowth in PC12 cells. Cell Signal. 2012;24(4): 899-906.
62. Kumar S et al. Mechanisms controlling neurite outgrowth in a pheochromocytoma cell line: the role of TRPC channels. J Cell Physiol. 2012;227(4): 1408-19.
63. El Bejjani R, Hammarlund M. Neural regeneration in Caenorhabditis elegans. Annu Rev Genet. 2012;46: 499-513.
64. Subramanian N et al. Role of Na(v)1. 9 in activity-dependent axon growth in motoneurons. Hum Mol Genet. 2012;21(16): 3655-67.
65. Wu D et al. TRPC4 in rat dorsal root ganglion neurons is increased after nerve injury and is necessary for neurite outgrowth. J Biol Chem. 2008;283(1): 416-26.
66. Kulbatski I, Cook DJ, Tator CH. Calcium entry through L-type calcium channels is essential for neurite regeneration in cultured sympathetic neurons. J Neurotrauma. 2004;21(3): 357-74.
67. Weick JP, Austin Johnson M, Zhang SC. Developmental regulation of human embryonic stem cell-derived neurons by calcium entry via transient receptor potential channels. Stem Cells. 2009;27(12): 2906-16.
68. Ding F et al. Involvement of cationic channels in proliferation and migration of human mesenchymal stem cells. Tissue Cell. 2012;44(6): 358-64.
69. Schwab A et al. Role of ion channels and transporters in cell migration. Physiol Rev. 2012;92(4): 1865-913.
70. Schwab A. Function and spatial distribution of ion channels and transporters in cell migration. Am J Physiol Renal Physiol. 2001;280(5): F739-47.
71. Schwab A et al. Potassium channels keep mobile cells on the go. Physiology (Bethesda). 2008;23: 212-20.
72. Yu X et al. Hypoxic preconditioning with cobalt of bone marrow mesenchymal stem cells improves cell migration and enhances therapy for treatment of ischemic acute kidney injury. PLoS One. 2013;8(5): e62703.
73. Komuro H, Kumada T. Ca2+ transients control CNS neuronal migration. Cell Calcium. 2005;37(5): 387-93.
74. Betapudi V et al. Novel regulation and dynamics of myosin II activation during epidermal wound responses. Exp Cell Res. 2010;316(6): 980-91.
75. Franco SJ, Huttenlocher A. Regulating cell migration: calpains make the cut. J Cell Sci. 2005;118(Pt 17): 3829-38.
76. Easley CAT et al. CaMK-II promotes focal adhesion turnover and cell motility by inducing tyrosine dephosphorylation of FAK and paxillin. Cell Motil Cytoskeleton. 2008;65(8): 662-74.
77. Brundage RA et al. Calcium gradients underlying polarization and chemotaxis of eosinophils. Science. 1991;254(5032): 703-6.
78. Hahn K, DeBiasio R, Taylor DL. Patterns of elevated free calcium and calmodulin activation in living cells. Nature. 1992;359(6397): 736-8.
79. Schwab A et al. Intracellular Ca2+ distribution in migrating transformed epithelial cells. Pflugers Arch. 1997;434(1): 70-6.
80. Clapham DE. Calcium signaling. Cell. 2007;131(6): 1047-58.
81. Fabian A et al. TRPC1 channels regulate directionality of migrating cells. Pflugers Arch. 2008;457(2): 475-84.
82. Louhivuori LM et al. Role of low voltage activated calcium channels in neuritogenesis and active migration of embryonic neural progenitor cells. Stem Cells Dev. 2013;22(8): 1206-19.
83. Paez PM et al. Multiple kinase pathways regulate voltage-dependent Ca2+ influx and migration in oligodendrocyte precursor cells. J Neurosci. 2010;30(18): 6422-33.
84. Morgan PJ et al. Spontaneous calcium transients in human neural progenitor cells mediated by transient receptor potential channels. Stem Cells Dev. 2013;22(18): 2477-86.
85. Paez PM et al. Golli myelin basic proteins regulate oligodendroglial progenitor cell migration through voltage-gated Ca2+ influx. J Neurosci. 2009;29(20): 6663-76.
86. Paez PM et al. Voltage-operated Ca(2+) and Na(+) channels in the oligodendrocyte lineage. J Neurosci Res. 2009;87(15): 3259-66.
87. Kuang CY et al. Knockdown of transient receptor potential canonical-1 reduces the proliferation and migration of endothelial progenitor cells. Stem Cells Dev. 2012;21(3): 487-96.
88. Moustakas A et al. The cytoskeleton in cell volume regulation. Contrib Nephrol. 1998;123: 121-34.
89. Pedersen SF, Hoffmann EK, Mills JW. The cytoskeleton and cell volume regulation. Comp Biochem Physiol A Mol Integr Physiol. 2001;130(3): 385-99.
90. Schwab A et al. Oscillating activity of a Ca(2+)-sensitive K+ channel. A prerequisite for migration of transformed Madin-Darby canine kidney focus cells. J Clin Invest. 1994;93(4): 1631-6.
91. Pettit EJ, Fay FS. Cytosolic free calcium and the cytoskeleton in the control of leukocyte chemotaxis. Physiol Rev. 1998;78(4): 949-67.
92. Yu SP. Regulation and critical role of potassium homeostasis in apoptosis. Prog Neurobiol. 2003;70(4): 363-86.
93. Schwab A et al. Migration of transformed renal epithelial cells is regulated by K+ channel modulation of actin cytoskeleton and cell volume. Pflugers Arch. 1999;438(3): 330-7.
94. Gendelman HE et al. Monocyte chemotactic protein-1 regulates voltage-gated K+ channels and macrophage transmigration. J NeuroImmune Pharm. 2009;4(1): 47-59.
95. Nutile-McMenemy N, Elfenbein A, Deleo JA. Minocycline decreases in vitro microglial motility, beta1-integrin, and Kv1. 3 channel expression. J Neurochem. 2007;103(5): 2035-46.
96. Schwab A et al. Subcellular distribution of calcium-sensitive potassium channels (IK1) in migrating cells. J Cell Physiol. 2006;206(1): 86-94.
97. Shao Z, Makinde TO, Agrawal DK. Calcium-activated potassium channel KCa3. 1 in lung dendritic cell migration. Am J Respir Cell Mol Biol. 2011;45(5): 962-8.
98. Su XL et al. Insulin-mediated upregulation of K(Ca)3. 1 channels promotes cell migration and proliferation in rat vascular smooth muscle. J Mol Cell Cardiol. 2011;51(1): 51-7.
99. Meng F, et al. Aqp1 enhances migration of bone marrow mesenchymal stem cells through regulation of FAK and beta-catenin. Stem Cells Dev. 2014;23(1): 66-75.
100. Yu SP, Wei Z, Wei L. Preconditioning strategy in stem cell transplantation therapy. Transl Stroke Res. 2013;4(1): 76-88.
101. Makri G et al. Transplantation of embryonic neural stem/precursor cells overexpressing BM88/Cend1 enhances the generation of neuronal cells in the injured mouse cortex. Stem Cells. 2010;28(1): 127-39.
102. Zhang S et al. Purified human bone marrow multipotent mesenchymal stem cells regenerate infarcted myocardium in experimental rats. Cell Transplant. 2005;14(10): 787-98.
103. Agbulut O et al. Can bone marrow-derived multipotent adult progenitor cells regenerate infarcted myocardium? Cardiovasc Res. 2006;72(1): 175-83.
104. Zhang ZG et al. Bone marrow-derived endothelial progenitor cells participate in cerebral neovascularization after focal cerebral ischemia in the adult mouse. Circ Res. 2002;90(3): 284-8.
105. Yoo J, et al. Enhanced recovery from chronic ischemic injury by bone marrow cells in a rat model of ischemic stroke. Cell Transplant. 2013. doi: 10. 3727/096368913X674666.