Activation of the TRPV1 cation channel contributes to stress-induced astrocyte migration

GLIA

Volumn 62, Issue 9, 2014, Pages 1435-1451

  Ho, Karen W ^a   Lambert, Wendi S ^b   Calkins, David J ^a,b  

^a VANDERBILT UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b VANDERBILT UNIVERSITY MEDICAL CENTER   (United States)

Author keywords

Astrocytes; Calcium; Migration; Reactivity; TRPV1

Indexed keywords

CALCIUM; TRPV1 PROTEIN, MOUSE; TRPV1 PROTEIN, RAT; VANILLOID RECEPTOR;

AGONISTS; ANIMAL; ANTAGONISTS AND INHIBITORS; ASTROCYTE; C57BL MOUSE; CELL CULTURE; CELL MOTION; CULTURE TECHNIQUE; CYTOSKELETON; DRUG EFFECTS; EXTRACELLULAR SPACE; INTRACELLULAR SPACE; MECHANICAL STRESS; METABOLISM; PHYSIOLOGY; RETINA; SPRAGUE DAWLEY RAT;

ANIMALS; ASTROCYTES; CALCIUM; CELL CULTURE TECHNIQUES; CELL MOVEMENT; CELLS, CULTURED; CYTOSKELETON; EXTRACELLULAR SPACE; INTRACELLULAR SPACE; MICE, INBRED C57BL; RATS, SPRAGUE-DAWLEY; RETINA; STRESS, MECHANICAL; TRPV CATION CHANNELS;

EID: 84904392608     PISSN: 08941491     EISSN: 10981136     Source Type: Journal    
DOI: 10.1002/glia.22691     Document Type: Article

References (93)

1. Abd-el-Basset EM, Ahmed I, Fedoroff S. 1991. Actin and actin-binding proteins in differentiating astroglia in tissue culture. J Neurosci Res 30:1-17.
2. Abd-El-Basset EM, Fedoroff S. 1997. Upregulation of F-actin and alpha-actinin in reactive astrocytes. J Neurosci Res 49:608-616.
3. Agapova OA, Ricard CS, Salvador-Silva M, Hernandez MR. 2001. Expression of matrix metalloproteinases and tissue inhibitors of metalloproteinases in human optic nerve head astrocytes. Glia 33:205-216.
4. Argaw AT, Asp L, Zhang J, Navrazhina K, Pham T, Mariani JN, Mahase S, Dutta DJ, Seto J, Kramer EG, Ferrara N, Sofroniew MV, John GR. 2012. Astrocyte-derived VEGF-A drives blood-brain barrier disruption in CNS inflammatory disease. J Clin Invest 122:2454-2468.
5. Bevan S, Hothi S, Hughes G, James IF, Rang HP, Shah K, Walpole CS, Yeats JC. 1992. Capsazepine: A competitive antagonist of the sensory neurone excitant capsaicin. Br J Pharmacol 107:544-552.
6. Bouvard D, Block MR. 1998. Calcium/calmodulin-dependent protein kinase II controls integrin alpha5beta1-mediated cell adhesion through the integrin cytoplasmic domain associated protein-1alpha. Biochem Biophys Res Commun 252:46-50.
7. Caterina MJ, Leffler A, Malmberg AB, Martin WJ, Trafton J, Petersen-Zeitz KR, Koltzenburg M, Basbaum AI, Julius D. 2000. Impaired nociception and pain sensation in mice lacking the capsaicin receptor. Science 288:306-313.
8. Caterina MJ, Schumacher MA, Tominaga M, Rosen TA, Levine JD, Julius D. 1997. The capsaicin receptor: a heat-activated ion channel in the pain pathway. Nature 389:816-824.
9. Chen Y, Willcockson HH, Valtschanoff JG. 2009. Influence of the vanilloid receptor TRPV1 on the activation of spinal cord glia in mouse models of pain. Exp Neurol 220:383-390.
10. Collin L, Schlessinger K, Hall A. 2008. APC nuclear membrane association and microtubule polarity. Biol Cell 100:243-252.
11. Cong X, Zhang Y, Yang NY, Li J, Ding C, Ding QW, Su YC, Mei M, Guo XH, Wu LL, Yu GY. 2013. Occludin is required for TRPV1-modulated paracellular permeability in the submandibular gland. J Cell Sci 126:1109-1121.
12. Correll CC, Phelps PT, Anthes JC, Umland S, Greenfeder S. 2004. Cloning and pharmacological characterization of mouse TRPV1. Neurosci Lett 370:55-60.
13. Crish SD, Sappington RM, Inman DM, Horner PJ, Calkins DJ. 2010. Distal axonopathy with structural persistence in glaucomatous neurodegeneration. Proc Natl Acad Sci USA 107:5196-5201.
14. Damann N, Owsianik G, Li S, Poll C, Nilius B. 2009. The calcium-conducting ion channel transient receptor potential canonical 6 is involved in macrophage inflammatory protein-2-induced migration of mouse neutrophils. Acta Physiol (Oxf) 195:3-11.
15. DeNiro M, Al-Mohanna FH, Al-Mohanna FA. 2011. Inhibition of reactive gliosis prevents neovascular growth in the mouse model of oxygen-induced retinopathy. PLoS One 6:e22244.
16. Doly S, Fischer J, Salio C, Conrath M. 2004. The vanilloid receptor-1 is expressed in rat spinal dorsal horn astrocytes. Neurosci Lett 357:123-126.
17. Etienne-Manneville S, Hall A. 2001. Integrin-mediated activation of Cdc42 controls cell polarity in migrating astrocytes through PKCzeta. Cell 106:489-498.
18. Gagelin C, Pierre M, Gavaret JM, Toru-Delbauffe D. 1995. Rapid TGF beta 1 effects on actin cytoskeleton of astrocytes: comparison with other factors and implications for cell motility. Glia 13:283-293.
19. Gao K, Wang CR, Jiang F, Wong AY, Su N, Jiang JH, Chai RC, Vatcher G, Teng J, Chen J, Jiang YW, Yu AC. 2013. Traumatic scratch injury in astrocytes triggers calcium influx to activate the JNK/c-Jun/AP-1 pathway and switch on GFAP expression. Glia 61:2063-2077.
20. Giaume C, Koulakoff A, Roux L, Holcman D, Rouach N. 2010. Astroglial networks: A step further in neuroglial and gliovascular interactions. Nat Rev Neurosci 11:87-99.
21. Glenney JR, Jr., Tack B, Powell MA. 1987. Calpactins: Two distinct Ca++-regulated phospholipid- and actin-binding proteins isolated from lung and placenta. J Cell Biol 104:503-511.
22. Goswami C, Dreger M, Otto H, Schwappach B, Hucho F. 2006. Rapid disassembly of dynamic microtubules upon activation of the capsaicin receptor TRPV1. J Neurochem 96:254-266.
23. Goswami C, Hucho T. 2007. TRPV1 expression-dependent initiation and regulation of filopodia. J Neurochem 103:1319-1333.
24. Goswami C, Schmidt H, Hucho F. 2007. TRPV1 at nerve endings regulates growth cone morphology and movement through cytoskeleton reorganization. FEBS J 274:760-772.
25. Gremm D, Wegner A. 2000. Gelsolin as a calcium-regulated actin filament-capping protein. Eur J Biochem 267:4339-4345.
26. Hamilton NB, Attwell D. 2010. Do astrocytes really exocytose neurotransmitters? Nat Rev Neurosci 11:227-238.
27. Han P, McDonald HA, Bianchi BR, Kouhen RE, Vos MH, Jarvis MF, Faltynek CR, Moreland RB. 2007. Capsaicin causes protein synthesis inhibition and microtubule disassembly through TRPV1 activities both on the plasma membrane and intracellular membranes. Biochem Pharmacol 73:1635-1645.
28. Hartwig JH, Thelen M, Rosen A, Janmey PA, Nairn AC, Aderem A. 1992. MARCKS is an actin filament crosslinking protein regulated by protein kinase C and calcium-calmodulin. Nature 356:618-622.
29. Ho KW, Ward NJ, Calkins DJ. 2012. TRPV1: A stress response protein in the central nervous system. Am J Neurodegener Dis 1:1-14.
30. Holinstat M, Mehta D, Kozasa T, Minshall RD, Malik AB. 2003. Protein kinase Calpha-induced p115RhoGEF phosphorylation signals endothelial cytoskeletal rearrangement. J Biol Chem 278:28793-28798.
31. Huang C, Hu ZL, Wu WN, Yu DF, Xiong QJ, Song JR, Shu Q, Fu H, Wang F, Chen JG. 2010. Existence and distinction of acid-evoked currents in rat astrocytes. Glia 58:1415-1424.
32. Inman DM, Horner PJ. 2007. Reactive nonproliferative gliosis predominates in a chronic mouse model of glaucoma. Glia 55:942-953.
33. Jayadev R, Kuk CY, Low SH, Murata-Hori M. 2012. Calcium sensitivity of alpha-actinin is required for equatorial actin assembly during cytokinesis. Cell Cycle 11:1929-1937.
34. Lau CL, O'Shea RD, Broberg BV, Bischof L, Beart PM. 2011. The Rho kinase inhibitor Fasudil up-regulates astrocytic glutamate transport subsequent to actin remodelling in murine cultured astrocytes. Br J Pharmacol 163:533-545.
35. Lawson MA, Maxfield FR. 1995. Ca(2+)- and calcineurin-dependent recycling of an integrin to the front of migrating neutrophils. Nature 377:75-79.
36. Le Clainche C, Carlier MF. 2008. Regulation of actin assembly associated with protrusion and adhesion in cell migration. Physiol Rev 88:489-513.
37. Leonelli M, Martins DO, Britto LR. 2010. TRPV1 receptors are involved in protein nitration and Muller cell reaction in the acutely axotomized rat retina. Exp Eye Res 91:755-768.
38. Leonelli M, Martins DO, Kihara AH, Britto LR. 2009. Ontogenetic expression of the vanilloid receptors TRPV1 and TRPV2 in the rat retina. Int J Dev Neurosci 27:709-718.
39. Lepekhin EA, Eliasson C, Berthold CH, Berezin V, Bock E, Pekny M. 2001. Intermediate filaments regulate astrocyte motility. J Neurochem 79:617-625.
40. Li Y, Li D, Ibrahim A, Raisman G. 2012. Repair involves all three surfaces of the glial cell. Prog Brain Res 201:199-218.
41. Lilja J, Lindegren H, Forsby A. 2007. Surfactant-induced TRPV1 activity-A novel mechanism for eye irritation? Toxicol Sci 99:174-180.
42. Lin CC, Hsieh HL, Shih RH, Chi PL, Cheng SE, Chen JC, Yang CM. 2012. NADPH oxidase 2-derived reactive oxygen species signal contributes to bradykinin-induced matrix metalloproteinase-9 expression and cell migration in brain astrocytes. Cell Commun Signal 10:35.
43. Liu XP, Zheng HY, Qu M, Zhang Y, Cao FY, Wang Q, Ke D, Liu GP, Wang JZ. 2012. Upregulation of astrocytes protein phosphatase-2A stimulates astrocytes migration via inhibiting p38 MAPK in tg2576 mice. Glia 60:1279-1288.
44. Luna G, Lewis GP, Banna CD, Skalli O, Fisher SK. 2010. Expression profiles of nestin and synemin in reactive astrocytes and Muller cells following retinal injury: A comparison with glial fibrillar acidic protein and vimentin. Mol Vis 16:2511-2523.
45. Mannari T, Morita S, Furube E, Tominaga M, Miyata S. 2013. Astrocytic TRPV1 ion channels detect blood-borne signals in the sensory circumventricular organs of adult mouse brains. Glia 61:957-971.
46. Marinelli S, Di Marzo V, Berretta N, Matias I, Maccarrone M, Bernardi G, Mercuri NB. 2003. Presynaptic facilitation of glutamatergic synapses to dopaminergic neurons of the rat substantia nigra by endogenous stimulation of vanilloid receptors. J Neurosci 23:3136-3144.
47. Marinelli S, Di Marzo V, Florenzano F, Fezza F, Viscomi MT, van der Stelt M, Bernardi G, Molinari M, Maccarrone M, Mercuri NB. 2007. N-arachidonoyl-dopamine tunes synaptic transmission onto dopaminergic neurons by activating both cannabinoid and vanilloid receptors. Neuropsychopharmacology 32:298-308.
48. Martin E, Dahan D, Cardouat G, Gillibert-Duplantier J, Marthan R, Savineau JP, Ducret T. 2012. Involvement of TRPV1 and TRPV4 channels in migration of rat pulmonary arterial smooth muscle cells. Pflugers Arch 464:261-272.
49. McIntyre P, McLatchie LM, Chambers A, Phillips E, Clarke M, Savidge J, Toms C, Peacock M, Shah K, Winter J, Weerasakera N, Webb M, Rang HP, Bevan S, James IF. 2001. Pharmacological differences between the human and rat vanilloid receptor 1 (VR1). Br J Pharmacol 132:1084-1094.
50. Moreels M, Vandenabeele F, Dumont D, Robben J, Lambrichts I. 2008. Alpha-smooth muscle actin (alpha-SMA) and nestin expression in reactive astrocytes in multiple sclerosis lesions: Potential regulatory role of transforming growth factor-beta 1 (TGF-beta1). Neuropathol Appl Neurobiol 34:532-546.
51. Nishio T, Kawaguchi S, Yamamoto M, Iseda T, Kawasaki T, Hase T. 2005. Tenascin-C regulates proliferation and migration of cultured astrocytes in a scratch wound assay. Neuroscience 132:87-102.
52. Pearce LV, Toth A, Ryu H, Kang DW, Choi HK, Jin MK, Lee J, Blumberg PM. 2008. Differential modulation of agonist and antagonist structure activity relations for rat TRPV1 by cyclosporin A and other protein phosphatase inhibitors. Naunyn Schmiedebergs Arch Pharmacol 377:149-157.
53. Pekny M, Johansson CB, Eliasson C, Stakeberg J, Wallen A, Perlmann T, Lendahl U, Betsholtz C, Berthold CH, Frisen J. 1999. Abnormal reaction to central nervous system injury in mice lacking glial fibrillary acidic protein and vimentin. J Cell Biol 145:503-514.
54. Phillips E, Reeve A, Bevan S, McIntyre P. 2004. Identification of species-specific determinants of the action of the antagonist capsazepine and the agonist PPAHV on TRPV1. J Biol Chem 279:17165-17172.
55. Raisinghani M, Pabbidi RM, Premkumar LS. 2005. Activation of transient receptor potential vanilloid 1 (TRPV1) by resiniferatoxin. J Physiol 567:771-786.
56. Renault-Mihara F, Okada S, Shibata S, Nakamura M, Toyama Y, Okano H. 2008. Spinal cord injury: emerging beneficial role of reactive astrocytes' migration. Int J Biochem Cell Biol 40:1649-1653.
57. Ridley AJ, Schwartz MA, Burridge K, Firtel RA, Ginsberg MH, Borisy G, Parsons JT, Horwitz AR. 2003. Cell migration: integrating signals from front to back. Science 302:1704-1709.
58. Saadoun S, Papadopoulos MC, Watanabe H, Yan D, Manley GT, Verkman AS. 2005. Involvement of aquaporin-4 in astroglial cell migration and glial scar formation. J Cell Sci 118:5691-5698.
59. Sakimoto S, Kidoya H, Naito H, Kamei M, Sakaguchi H, Goda N, Fukamizu A, Nishida K, Takakura N. 2012. A role for endothelial cells in promoting the maturation of astrocytes through the apelin/APJ system in mice. Development 139:1327-1335.
60. Sappington RM, Calkins DJ. 2008. Contribution of TRPV1 to microglia-derived IL-6 and NFkappaB translocation with elevated hydrostatic pressure. Invest Ophthalmol Vis Sci 49:3004-3017.
61. Sappington RM, Carlson BJ, Crish SD, Calkins DJ. 2010. The microbead occlusion model: a paradigm for induced ocular hypertension in rats and mice. Invest Ophthalmol Vis Sci 51:207-216.
62. Sappington RM, Chan M, Calkins DJ. 2006. Interleukin-6 protects retinal ganglion cells from pressure-induced death. Invest Ophthalmol Vis Sci 47:2932-2942.
63. Sappington RM, Sidorova T, Long DJ, Calkins DJ. 2009. TRPV1: Contribution to retinal ganglion cell apoptosis and increased intracellular Ca2+ with exposure to hydrostatic pressure. Invest Ophthalmol Vis Sci 50:717-728.
64. Saunders CI, Kunde DA, Crawford A, Geraghty DP. 2007. Expression of transient receptor potential vanilloid 1 (TRPV1) and 2 (TRPV2) in human peripheral blood. Mol Immunol 44:1429-1435.
65. Savidge J, Davis C, Shah K, Colley S, Phillips E, Ranasinghe S, Winter J, Kotsonis P, Rang H, McIntyre P. 2002. Cloning and functional characterization of the guinea pig vanilloid receptor 1. Neuropharmacology 43:450-456.
66. Schneider CA, Rasband WS, Eliceiri KW. 2012. NIH Image to ImageJ: 25 years of image analysis. Nat Methods 9:671-675.
67. Scott A, Powner MB, Gandhi P, Clarkin C, Gutmann DH, Johnson RS, Ferrara N, Fruttiger M. 2010. Astrocyte-derived vascular endothelial growth factor stabilizes vessels in the developing retinal vasculature. PLoS One 5:e11863.
68. Seabrook GR, Sutton KG, Jarolimek W, Hollingworth GJ, Teague S, Webb J, Clark N, Boyce S, Kerby J, Ali Z, Chou M, Middleton R, Kaczorowski G, Jones AB. 2002. Functional properties of the high-affinity TRPV1 (VR1) vanilloid receptor antagonist (4-hydroxy-5-iodo-3-methoxyphenylacetate ester) iodo-resiniferatoxin. J Pharmacol Exp Ther 303:1052-1060.
69. Shao H, Travers T, Camacho CJ, Wells A. 2013. The carboxyl tail of alpha-actinin-4 regulates its susceptibility to m-calpain and thus functions in cell migration and spreading. Int J Biochem Cell Biol 45:1051-1063.
70. Sofroniew MV. 2009. Molecular dissection of reactive astrogliosis and glial scar formation. Trends Neurosci 32:638-647.
71. Song ZH, Zhong M. 2000. CB1 cannabinoid receptor-mediated cell migration. J Pharmacol Exp Ther 294:204-209.
72. Sorci G, Agneletti AL, Bianchi R, Donato R. 1998. Association of S100B with intermediate filaments and microtubules in glial cells. Biochim Biophys Acta 1448:277-289.
73. Suh YG, Oh U. 2005. Activation and activators of TRPV1 and their pharmaceutical implication. Curr Pharm Des 11:2687-2698.
74. Sun D, Qu J, Jakobs TC. 2013. Reversible reactivity by optic nerve astrocytes. Glia 61:1218-1235.
75. Szallasi A, Blumberg PM. 1989. Resiniferatoxin, a phorbol-related diterpene, acts as an ultrapotent analog of capsaicin, the irritant constituent in red pepper. Neuroscience 30:515-520.
76. Tezel G, Hernandez MR, Wax MB. 2001. In vitro evaluation of reactive astrocyte migration, a component of tissue remodeling in glaucomatous optic nerve head. Glia 34:178-189.
77. Toth A, Boczan J, Kedei N, Lizanecz E, Bagi Z, Papp Z, Edes I, Csiba L, Blumberg PM. 2005a. Expression and distribution of vanilloid receptor 1 (TRPV1) in the adult rat brain. Brain Res Mol Brain Res 135:162-168.
78. Toth A, Wang Y, Kedei N, Tran R, Pearce LV, Kang SU, Jin MK, Choi HK, Lee J, Blumberg PM. 2005b. Different vanilloid agonists cause different patterns of calcium response in CHO cells heterologously expressing rat TRPV1. Life Sci 76:2921-2932.
79. Wahl P, Foged C, Tullin S, Thomsen C. 2001. Iodo-resiniferatoxin, a new potent vanilloid receptor antagonist. Mol Pharmacol 59:9-15.
80. Walpole CS, Bevan S, Bovermann G, Boelsterli JJ, Breckenridge R, Davies JW, Hughes GA, James I, Oberer L, Winter J, Wrigglesworth R. 1994. The discovery of capsazepine, the first competitive antagonist of the sensory neuron excitants capsaicin and resiniferatoxin. J Med Chem 37:1942-1954.
81. Walter L, Franklin A, Witting A, Moller T, Stella N. 2002. Astrocytes in culture produce anandamide and other acylethanolamides. J Biol Chem 277:20869-20876.
82. Wang F, Smith NA, Xu Q, Fujita T, Baba A, Matsuda T, Takano T, Bekar L, Nedergaard M. 2012. Astrocytes modulate neural network activity by Ca(2)+-dependent uptake of extracellular K+. Sci Signal 5:ra26.
83. Wang JP, Tseng CS, Sun SP, Chen YS, Tsai CR, Hsu MF. 2005. Capsaicin stimulates the nonstore-operated Ca2+ entry but inhibits the store-operated Ca2+ entry in neutrophils. Toxicol Appl Pharmacol 209:134-144.
84. Waning J, Vriens J, Owsianik G, Stuwe L, Mally S, Fabian A, Frippiat C, Nilius B, Schwab A. 2007. A novel function of capsaicin-sensitive TRPV1 channels: Involvement in cell migration. Cell Calcium 42:17-25.
85. Watson MG, McDougall SR, Chaplain MA, Devlin AH, Mitchell CA. 2012. Dynamics of angiogenesis during murine retinal development: a coupled in vivo and in silico study. J R Soc Interface 9:2351-2364.
86. Wei C, Wang X, Chen M, Ouyang K, Song LS, Cheng H. 2009. Calcium flickers steer cell migration. Nature 457:901-905.
87. Wei C, Wang X, Zheng M, Cheng H. 2012. Calcium gradients underlying cell migration. Curr Opin Cell Biol 24:254-261.
88. Yang H, Wang Z, Capo-Aponte JE, Zhang F, Pan Z, Reinach PS. 2010. Epidermal growth factor receptor transactivation by the cannabinoid receptor (CB1) and transient receptor potential vanilloid 1 (TRPV1) induces differential responses in corneal epithelial cells. Exp Eye Res 91:462-471.
89. Zhang Y, Porat RM, Alon T, Keshet E, Stone J. 1999. Tissue oxygen levels control astrocyte movement and differentiation in developing retina. Brain Res Dev Brain Res 118:135-145.
90. Zhao Z, Ni Y, Chen J, Zhong J, Yu H, Xu X, He H, Yan Z, Scholze A, Liu D, Zhu Z, Tepel M. 2012. Increased migration of monocytes in essential hypertension is associated with increased transient receptor potential channel canonical type 3 channels. PLoS One 7:e32628.
91. Zhu D, Hu C, Sheng W, Tan KS, Haidekker MA, Sun AY, Sun GY, Lee JC. 2009. NAD(P)H oxidase-mediated reactive oxygen species production alters astrocyte membrane molecular order via phospholipase A2. Biochem J 421:201-210.
92. Zimov S, Yazulla S. 2004. Localization of vanilloid receptor 1 (TRPV1/VR1)-like immunoreactivity in goldfish and zebrafish retinas: restriction to photoreceptor synaptic ribbons. J Neurocytol 33:441-452.
93. Zygmunt PM, Petersson J, Andersson DA, Chuang H, Sorgard M, Di Marzo V, Julius D, Hogestatt ED. 1999. Vanilloid receptors on sensory nerves mediate the vasodilator action of anandamide. Nature 400:452-457.