Swelling and eicosanoid metabolites differentially gate TRPV4 channels in retinal neurons and glia

Journal of Neuroscience

Volumn 34, Issue 47, 2014, Pages 15689-15700

  Ryskamp, Daniel A ^a,b   Jo, Andrew O ^a   Frye, Amber M ^a   Vazquez Chona, Felix ^a   MaCaulay, Nanna ^c   Thoreson, Wallace B ^d,e   Križaj, David ^a,b  

^a UNIVERSITY OF UTAH SCHOOL OF MEDICINE   (United States)

^b University of Copenhagen ^*  (United States)

^c UNIVERSITY OF COPENHAGEN   (Denmark)

^d UNIVERSITY OF NEBRASKA MEDICAL CENTER   (United States)

^e UNIVERSITY OF NEBRASKA MEDICAL CENTER   (United States)

Author keywords

Ganglion cell; M ller glia; Osmoregulation; Retina; TRP channels

Indexed keywords

ARACHIDONIC ACID; CALCIUM; CYTOCHROME P450; ICOSANOID; PHOSPHOLIPASE A2; VANILLOID RECEPTOR 4; TRPV4 PROTEIN, MOUSE; VANILLOID RECEPTOR;

ANIMAL CELL; ARTICLE; CALCIUM TRANSPORT; CELL PERMEABILIZATION; CHANNEL GATING; CONTROLLED STUDY; ELECTROPHYSIOLOGY; FEMALE; FLUORESCENCE IMAGING; GLIA; GLIOSIS; IMMUNOFLUORESCENCE; MALE; MOUSE; MUELLER CELL; NONHUMAN; OSMOSIS; RETINA NERVE CELL; SPIKE WAVE; ANIMAL; C57BL MOUSE; CYTOLOGY; GENETICS; IN VITRO STUDY; KNOCKOUT MOUSE; METABOLISM; NERVE CELL; OSMOLARITY; PATCH CLAMP TECHNIQUE; PATHOLOGY; PHYSIOLOGY; RETINA; RETINA GANGLION CELL;

ANIMALS; EICOSANOIDS; GLIOSIS; IN VITRO TECHNIQUES; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; NEUROGLIA; NEURONS; OSMOLAR CONCENTRATION; PATCH-CLAMP TECHNIQUES; PHOSPHOLIPASES A2; RETINA; RETINAL GANGLION CELLS; TRPV CATION CHANNELS;

EID: 84911444207     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.2540-14.2014     Document Type: Article

References (61)

1. Becker D, Blase C, Bereiter-Hahn J, Jendrach M (2005) TRPV4 exhibits a functional role in cell-volume regulation. J Cell Sci 118:2435-2440. CrossRef Medline
2. Benfenati V, Caprini M, Dovizio M, Mylonakou MN, Ferroni S, Ottersen OP, Amiry-Moghaddam M (2011) An aquaporin-4/transient receptor potential vanilloid 4 (AQP4/TRPV4) complex is essential for cell-volume control in astrocytes. Proc Natl Acad Sci U S A 108:2563-2568. CrossRef Medline
3. Butenko O, Dzamba D, Benesova J, Honsa P, Benfenati V, Rusnakova V, Ferroni S, AnderovaM (2012) The increased activity of TRPV4 channel in the astrocytes of the adult rat hippocampus after cerebral hypoxia/ ischemia. PLoS One 7:e39959. CrossRef Medline
4. Da T, Verkman AS (2004) Aquaporin-4 gene disruption in mice protects against impaired retinal function and cell death after ischemia. Invest Ophthalmol Vis Sci 45:4477- 4483. CrossRef Medline
5. Da Silva N, Herron CE, Stevens K, Jollimore CA, Barnes S, Kelly ME (2008) Metabotropic receptor-activated calcium increases and store-operated calcium influx in mouse Müller cells. Invest Ophthalmol Vis Sci 49:3065- 3073. CrossRef Medline
6. Della Santina L, Inman DM, Lupien CB, Horner PJ, Wong RO (2013) Differential progression of structural and functional alterations in distinct retinal ganglion cell types in a mouse model of glaucoma. J Neurosci 33:17444 -17457. CrossRef Medline
7. 2+ release in astrocytic endfeet and amplify neurovascular coupling responses. Proc Natl Acad Sci U S A 110: 6157-6162. CrossRef Medline
8. Dyer MA, Cepko CL (2000) Control of Müller glial cell proliferation and activation following retinal injury. Nat Neurosci 3:873- 880. CrossRef Medline
9. Feng L, Zhao Y, Yoshida M, Chen H, Yang JF, Kim TS, Cang J, Troy JB, Liu X (2013) Sustained ocular hypertension induces dendritic degeneration of mouse retinal ganglion cells that depends on cell type and location. Invest Ophthalmol Vis Sci 54:1106 -1117. CrossRef Medline
10. Fernández JM, Di Giusto G, Kalstein M, Melamud L, Rivarola V, Ford P, Capurro C (2013) Cell volume regulation in cultured human retinal Müller cells is associated with changes in transmembrane potential. PLoS One 8:e57268. CrossRef Medline
11. Gaiano N, Nye JS, Fishell G (2000) Radial glial identity is promoted by Notch1 signaling in the murine forebrain. Neuron 26:395- 404. CrossRef Medline
12. 2+ indicators with greatly improved fluorescence properties. J Biol Chem 260: 3440-3450. Medline
13. Ho KW, Lambert WS, Calkins DJ (2014) Activation of the TRPV1 cation channel contributes to stress-induced astrocyte migration. Glia 62:1435- 1451. CrossRef Medline
14. Hoffmann EK, Lambert IH, Pedersen SF (2009) Physiology of cell volume regulation in vertebrates. Physiol Rev 89:193-277. CrossRef Medline
15. Huang W, Xing W, Ryskamp DA, Punzo C, Krizaj D (2011) Localization and phenotype-specific expression of ryanodine calcium release channels in C57BL6 and DBA/2J mouse strains. Exp Eye Res 93:700 -709. CrossRef Medline
16. Inman DM, Horner PJ (2007) Reactive nonproliferative gliosis predominates in a chronic mouse model of glaucoma. Glia 55:942-953. CrossRef Medline
17. Jang Y, Jung J, Kim H, Oh J, Jeon JH, Jung S, Kim KT, Cho H, Yang DJ, Kim SM, Kim IB, Song MR, Oh U (2012) Axonal neuropathy-associated TRPV4 regulates neurotrophic factor-derived axonal growth. J Biol Chem 287:6014-6024. CrossRef Medline
18. Jo AO, Ryskamp DA, Redmon S, Krizaj D (2014) Nonretrograde endocannabinoid signaling modulates retinal ganglon cell calcium homeostasis through the TRPV1 cation channel. Soc Neurosci Abstr 55:E- 3021.
19. Keirstead SA, Miller RF (1995) Calcium waves in dissociated retinal glial (Müller) cells are evoked by release of calcium from intracellular stores. Glia 14:14 -22. CrossRef Medline
20. Koplas PA, Rosenberg RL, Oxford GS (1997) The role of calcium in the desensitization of capsaicin responses in rat dorsal root ganglion neurons. J Neurosci 17:3525-3537. Medline
21. Köttgen M, Buchholz B, Garcia-Gonzalez MA, Kotsis F, Fu X, Doerken M, Boehlke C, Steffl D, Tauber R, Wegierski T, Nitschke R, Suzuki M, Kramer-Zucker A, Germino GG, Watnick T, Prenen J, Nilius B, Kuehn EW, WalzG (2008) TRPP2 and TRPV4 form a polymodal sensory channel complex. J Cell Biol 182:437- 447. CrossRef Medline
22. KrižajD, Ryskamp DA, Tian N, Tezel G, Mitchell CH, Slepak VZ, Shestopalov VI (2014) From mechanosensitivity to inflammatory responses: new players in the pathology of glaucoma. Curr Eye Res 39:105-119. CrossRef Medline
23. Kunert-Keil C, Bisping F, Krüger J, Brinkmeier H (2006) Tissue-specific expression of TRP channel genes in the mouse and its variation in three different mouse strains. BMC Genomics 7:159. CrossRef Medline
24. Kurth-Nelson ZL, Mishra A, Newman EA (2009) Spontaneous glial calcium waves in the retina develop over early adulthood. J Neurosci 29:11339- 11346. CrossRef Medline
25. Lechner SG, Markworth S, Poole K, Smith ES, Lapatsina L, Frahm S, May M, Pischke S, Suzuki M, Ibañez-Tallon I, Luft FC, Jordan J, LewinGR (2011) The molecular and cellular identity of peripheral osmoreceptors. Neuron 69:332-344. CrossRef Medline
26. −/− mice. Proc Natl Acad Sci U S A 100:13698-13703. CrossRef Medline
27. Lindqvist N, Liu Q, Zajadacz J, Franze K, Reichenbach A (2010) Retinal glial (Müller) cells: sensing and responding to tissue stretch. Invest Ophthalmol Vis Sci 51:1683-1690. CrossRef Medline
28. Liu X, Bandyopadhyay B, Nakamoto T, Singh B, Liedtke W, Melvin JE, Ambudkar I (2006) A role for AQP5 in activation of TRPV4 by hypotonic- ity: concerted involvement of AQP5 and TRPV4 in regulation of cell volume recovery. J Biol Chem 281:15485-15495. CrossRef Medline
29. Loukin SH, Su Z, Kung C (2009) Hypotonic shocks activate rat TRPV4 in yeast in the absence of polyunsaturated fatty acids. FEBS Lett 583:754- 758. CrossRef Medline
30. Loukin S, Zhou X, Su Z, Saimi Y, Kung C (2010) Wild-type and brachyolmia-causing mutant TRPV4 channels respond directly to stretch force. J Biol Chem 285:27176 -27181. CrossRef Medline
31. Loukin S, Su Z, Kung C (2011) Increased basal activity is a key determinant in the severity of human skeletal dysplasia caused by TRPV4 mutations. PLoS One 6:e19533. CrossRef Medline
32. Lu YB, Franze K, Seifert G, Steinhäuser C, Kirchhoff F, Wolburg H, Guck J, Janmey P, Wei EQ, Käs J, Reichenbach A (2006) Viscoelastic properties of individual glial cells and neurons in the CNS. Proc Natl Acad Sci U S A 103:17759 -17764. CrossRef Medline
33. 2+) entry in vascular endothelial cells. Cell Calcium 50:502-559. CrossRef Medline
34. Marc RE (1999) Mapping glutamatergic drive in the vertebrate retina with a channel-permeant organic cation. J Comp Neurol 407:47- 64. CrossRef Medline
35. Matthews BD, Thodeti CK, Tytell JD, Mammoto A, Overby DR, Ingber DE (2010) Ultra-rapid activation of TRPV4 ion channels by mechanical forces applied to cell surface beta1 integrins. Integr Biol (Camb) 2:435- 442. CrossRef Medline
36. Meves H (2008) Arachidonic acid and ion channels: an update. Br J Pharmacol 155:4 -16. CrossRef Medline
37. Molnar T, Barabas P, Birnbaumer L, Punzo C, Kefalov V, Križaj D (2012) Store-operated channels regulate intracellular calcium in mammalian rods. J Physiol 590:3465-3481. CrossRef Medline
38. Nagelhus EA, Veruki ML, Torp R, Haug FM, Laake JH, Nielsen S, Agre P, Ottersen OP (1998) Aquaporin-4 water channel protein in the rat retina and optic nerve: polarized expression in Müller cells and fibrous astrocytes. J Neurosci 18:2506 -2519. Medline
39. Nedergaard M, Rodríguez JJ, Verkhratsky A (2010) Glial calcium and diseases of the nervous system. Cell Calcium 47:140 -149. CrossRef Medline
40. Newman EA, Zahs KR (1998) Modulation of neuronal activity by glial cells in the retina. J Neurosci 18:4022- 4028. Medline
41. Nilius B, Voets T (2013) The puzzle of TRPV4 channelopathies. EMBO Rep 14:152-163. CrossRef Medline
42. Nilius B, Vriens J, Prenen J, Droogmans G, Voets T (2004) TRPV4 calcium entry channel: a paradigm for gating diversity. Am J Physiol Cell Physiol 286:C195-C205. CrossRef Medline
43. Pannicke T, Iandiev I, Wurm A, Uckermann O, vom Hagen F, Reichenbach A, Wiedemann P, Hammes HP, Bringmann A (2006) Diabetes alters osmotic swelling characteristics and membrane conductance of glial cells in rat retina. Diabetes 55:633- 639. CrossRef Medline
44. Pasantes-Morales H, Cruz-Rangel S (2010) Brain volume regulation: osmolytes and aquaporin perspectives. Neuroscience 168:871-884. CrossRef Medline
45. Pinar-Sueiro S, Urcola H, Rivas MA, Vecino E (2011) Prevention of retinal ganglion cell swelling by systemic brimonidine in a rat experimental glaucoma model. Clin Exp Ophthalmol 39:799-807. CrossRef Medline
46. Puro DG (1991) Stretch-activated channels in human retinal Müller cells. Glia 4:456-460. CrossRef Medline
47. Reichenbach A, Bringmann A (2010) In: Müller cells in the healthy and diseased retina. New York: Springer.
48. Ryskamp DA, Witkovsky P, Barabas P, Huang W, Koehler C, Akimov NP, Lee SH, Chauhan S, Xing W, Rentería RC, Liedtke W, Križaj D (2011) The polymodal ion channel transient receptor potential vanilloid 4 modulates calcium flux, spiking rate, and apoptosis of mouse retinal ganglion cells. J Neurosci 31:7089 -7101. CrossRef Medline
49. Ryskamp DA, Redmon S, Jo AO, Križaj D (2014) TRPV1 and endocannabinoids: emerging molecular signals that modulate mammalian vision. Cells 3:914 -938. CrossRef Medline
50. Sofroniew MV (2009) Molecular dissection of reactive astrogliosis and glial scar formation. Trends Neurosci 32:638-647. CrossRef Medline
51. Staub F, Winkler A, Peters J, Kempski O, Kachel V, Baethmann A (1994) Swelling, acidosis, and irreversible damage of glial cells from exposure to arachidonic acid in vitro. J Cereb Blood Flow Metab 14:1030 -1039. CrossRef Medline
52. Strotmann R, Harteneck C, Nunnenmacher K, Schultz G, Plant TD (2000) OTRPC4, a nonselective cation channel that confers sensitivity to extracellular osmolarity. Nat Cell Biol 2:695-702. CrossRef Medline
53. Szikra T, Barabas P, Bartoletti TM, Huang W, Akopian A, Thoreson WB, Križaj D (2009) Calcium homeostasis and cone signaling are regulated by interactions between calcium stores and plasma membrane ion channels. PLoS One 4:e6723. CrossRef Medline
54. Tezel G, Chauhan BC, LeBlanc RP, Wax MB (2003) Immunohistochemical assessment of the glial mitogen-activated protein kinase activation in glaucoma. Invest Ophthalmol Vis Sci 44:3025-3033. CrossRef Medline
55. 2+ signaling events elicited by cerebral edema. Proc Natl Acad Sci U S A 108:846-851. CrossRef Medline
56. Tian W, Fu Y, Garcia-Elias A, Fernández-Fernández JM, Vicente R, Kramer PL, Klein RF, Hitzemann R, Orwoll ES, Wilmot B, McWeeney S, Valverde MA, Cohen DM (2009) A loss-of-function nonsynonymous polymorphism in the osmoregulatory TRPV4 gene is associated with human hyponatremia. Proc Natl Acad Sci U S A 106:14034 -14039. CrossRef Medline
57. Verkman AS, Ruiz-Ederra J, Levin MH (2008) Functions of aquaporins in the eye. Prog Retin Eye Res 27:420-433. CrossRef Medline
58. Vriens J, Watanabe H, Janssens A, Droogmans G, Voets T, Nilius B (2004) Cell swelling, heat, and chemical agonists use distinct pathways for the activation of the cation channel TRPV4. Proc Natl Acad Sci U S A 101: 396-401. CrossRef Medline
59. Ward NJ, Ho KW, Lambert WS, Weitlauf C, Calkins DJ (2014) Absence of transient receptor potential vanilloid-1 accelerates stress-induced axonopathy in the optic projection. J Neurosci 34:3161-3170. CrossRef Medline
60. Watanabe H, Vriens J, Prenen J, Droogmans G, Voets T, Nilius B (2003a) Anandamide and arachidonic acid use epoxyeicosatrienoic acids to activate TRPV4 channels. Nature 424:434-438. CrossRef Medline
61. 2+. Cell Calcium 33:489-495. CrossRef Medline