Hyperglycemia and diabetes downregulate the functional expression of TRPV4 channels in retinal microvascular endothelium

PLoS ONE

Volumn 10, Issue 6, 2015, Pages

  Monaghan, Kevin ^a   McNaughten, Jennifer ^a   McGahon, Mary K ^a   Kelly, Catriona ^a   Kyle, Daniel ^a   Yong, Phaik Har ^a   McGeown, J Graham ^a   Curtis, Tim M ^a  

^a QUEEN'S UNIVERSITY BELFAST   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

4ALPHA PHORBOL DIDECANOATE; CALCIUM ION; CYCLOPIAZONIC ACID; GLUCOSE; SMALL INTERFERING RNA; VANILLOID RECEPTOR 4; CALCIUM; TRPV4 PROTEIN, RAT; VANILLOID RECEPTOR;

ANIMAL CELL CULTURE; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CALCIUM TRANSPORT; CONTROLLED STUDY; DIABETES MELLITUS; DOWN REGULATION; ELECTROPHYSIOLOGY; ENDOTHELIUM CELL; EXTRACELLULAR CALCIUM; FUNCTIONAL PROTEOMICS; HYPERGLYCEMIA; IMMUNOHISTOCHEMISTRY; MALE; MEMBRANE CURRENT; MEMBRANE TRANSPORT; MICROFLUOROMETRY; NONHUMAN; PIGMENT EPITHELIUM; POLYMERASE CHAIN REACTION; PROTEIN EXPRESSION; PROTEIN FUNCTION; QUANTITATIVE ANALYSIS; RAT; RETINA MICROVASCULAR EPITHELIUM; STREPTOZOTOCIN-INDUCED DIABETES MELLITUS; VOLTAGE CLAMP TECHNIQUE; ANIMAL; BOVINE; CELL CULTURE; EXPERIMENTAL DIABETES MELLITUS; GENETICS; METABOLISM; MICROVASCULATURE; PATHOLOGY; SPRAGUE DAWLEY RAT; VASCULAR ENDOTHELIUM;

BOVINAE; RATTUS;

ANIMALS; CALCIUM; CATTLE; CELLS, CULTURED; DIABETES MELLITUS, EXPERIMENTAL; DOWN-REGULATION; ENDOTHELIUM, VASCULAR; HYPERGLYCEMIA; MALE; MICROVESSELS; RATS, SPRAGUE-DAWLEY; TRPV CATION CHANNELS;

EID: 84934998953     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0128359     Document Type: Article

References (55)

1. Kempen JH, O'Colmain BJ, Leske MC, Haffner SM, Klein R, Moss SE, et al. The prevalence of diabetic retinopathy among adults in the United States. Arch Ophthalmol. 2004; 122: 552-563. PMID: 15078674
2. Wong TY, Klein R, Islam FM, Cotch MF, Folsom AR, Klein BE, et al. Diabetic retinopathy in a multi-ethnic cohort in the United States. Am J Ophthalmol. 2006; 141: 446-455. PMID: 16490489
3. Antonetti DA, Barber AJ, Bronson SK, Freeman WM, Gardner TW, Jefferson LS, et al. Diabetic retinopathy: seeing beyond glucose-induced microvascular disease. Diabetes. 2006; 55: 2401-2411. PMID: 16936187
4. Chakravarthy U, Harding SP, Rogers CA, Downes SM, Lotery AJ, Culliford LA, et al. Alternative treatments to inhibit VEGF in age-related choroidal neovascularisation: 2-year findings of the IVAN randomised controlled trial. Lancet. 2013; 382: 1258-1267. doi: 10.1016/S0140-6736(13)61501-9 PMID: 23870813
5. Gardiner TA, Archer DB, Curtis TM, Stitt AW. Arteriolar involvement in the microvascular lesions of diabetic retinopathy: implications for pathogenesis. Microcirculation. 2007; 14: 25-38. PMID: 17365659
6. Aiello LP, Cahill MT, Wong JS. Systemic considerations in the management of diabetic retinopathy. Am J Ophthalmol. 2001; 132: 760-776. PMID: 11704039
7. Blum M, Kloos C, Gunther S, Hunger-Dathe W, Muller UA. Improved metabolic control results in better myogenic response of retinal arterioles in patients with diabetes mellitus type 1. Ophthalmologica. 2008; 222: 373-377. doi: 10.1159/000151278 PMID: 18698147
8. Ernest JT, Goldstick TK, Engerman RL. Hyperglycemia impairs retinal oxygen autoregulation in normal and diabetic dogs. Invest Ophthalmol Vis Sci. 1983; 24: 985-989. PMID: 6862799
9. Mandecka A, Dawczynski J, Blum M, Muller N, Kloos C, Wolf G, et al. Influence of flickering light on the retinal vessels in diabetic patients. Diabetes Care. 2007; 30: 3048-3052. PMID: 17728481
10. Nguyen TT, Kawasaki R, Wang JJ, Kreis AJ, Shaw J, Vilser W, et al. Flicker light-induced retinal vasodilation in diabetes and diabetic retinopathy. Diabetes Care. 2009; 32: 2075-2080. doi: 10.2337/dc09-0075 PMID: 19641162
11. Patel V, Rassam SM, Chen HC, Kohner EM. Oxygen reactivity in diabetes mellitus: effect of hypertension and hyperglycaemia. Clin Sci (Lond). 1994; 86: 689-695. PMID: 8062505
12. Pournaras CJ, Rungger-Brandle E, Riva CE, Hardarson SH, Stefansson E. Regulation of retinal blood flow in health and disease. Prog Retin Eye Res. 2008; 27: 284-330. doi: 10.1016/j.preteyeres.2008.02.002 PMID: 18448380
13. Sinclair SH, Grunwald JE, Riva CE, Braunstein SN, Nichols CW, Schwartz SS. Retinal vascular autoregulation in diabetes mellitus. Ophthalmology. 1982; 89: 748-750. PMID: 7122050
14. Nilius B, Vriens J, Prenen J, Droogmans G, Voets T. TRPV4 calcium entry channel: a paradigm for gating diversity. Am J Physiol Cell Physiol. 2004; 286: C195-C205. PMID: 14707014
15. Bagher P, Beleznai T, Kansui Y, Mitchell R, Garland CJ, Dora KA. Low intravascular pressure activates endothelial cell TRPV4 channels, local Ca2+ events, and IKCa channels, reducing arteriolar tone. Proc Natl Acad Sci U S A. 2012; 109: 18174-18179. doi: 10.1073/pnas.1211946109 PMID: 23071308
16. Bubolz AH, Mendoza SA, Zheng X, Zinkevich NS, Li R, Gutterman DD, et al. Activation of endothelial TRPV4 channels mediates flow-induced dilation in human coronary arterioles: role of Ca2+ entry and mitochondrial ROS signaling. Am J Physiol Heart Circ Physiol. 2012; 302: H634-H642. doi: 10.1152/ajpheart.00717.2011 PMID: 22140047
17. Hartmannsgruber V, Heyken WT, Kacik M, Kaistha A, Grgic I, Harteneck C, et al. Arterial response to shear stress critically depends on endothelial TRPV4 expression. PLoS One. 2007; 2: e827- PMID: 17786199
18. Kohler R, Heyken WT, Heinau P, Schubert R, Si H, Kacik M, et al. Evidence for a functional role of endothelial transient receptor potential V4 in shear stress-induced vasodilatation. Arterioscler Thromb Vasc Biol. 2006; 26: 1495-1502. PMID: 16675722
19. Loot AE, Popp R, Fisslthaler B, Vriens J, Nilius B, Fleming I. Role of cytochrome P450-dependent transient receptor potential V4 activation in flow-induced vasodilatation. Cardiovasc Res. 2008; 80: 445-452. doi: 10.1093/cvr/cvn207 PMID: 18682435
20. Ma X, Du J, Zhang P, Deng J, Liu J, Lam FF, et al. Functional role of TRPV4-KCa2.3 signaling in vascular endothelial cells in normal and streptozotocin-induced diabetic rats. Hypertension. 2013; 62: 134-139. doi: 10.1161/HYPERTENSIONAHA.113.01500 PMID: 23648706
21. Sonkusare SK, Bonev AD, Ledoux J, Liedtke W, Kotlikoff MI, Heppner TJ, et al. Elementary Ca2+ signals through endothelial TRPV4 channels regulate vascular function. Science. 2012; 336: 597-601. doi: 10.1126/science.1216283 PMID: 22556255
22. Vriens J, Owsianik G, Fisslthaler B, Suzuki M, Janssens A, Voets T, et al. Modulation of the Ca2 permeable cation channel TRPV4 by cytochrome P450 epoxygenases in vascular endothelium. Circ Res. 2005; 97: 908-915. PMID: 16179585
23. Earley S, Pauyo T, Drapp R, Tavares MJ, Liedtke W, Brayden JE. TRPV4-dependent dilation of peripheral resistance arteries influences arterial pressure. Am J Physiol Heart Circ Physiol. 2009; 297: H1096-H1102. doi: 10.1152/ajpheart.00241.2009 PMID: 19617407
24. Mendoza SA, Fang J, Gutterman DD, Wilcox DA, Bubolz AH, Li R, et al. TRPV4-mediated endothelial Ca2+ influx and vasodilation in response to shear stress. Am J Physiol Heart Circ Physiol. 2010; 298: H466-H476. doi: 10.1152/ajpheart.00854.2009 PMID: 19966050
25. Earley S, Heppner TJ, Nelson MT, Brayden JE. TRPV4 forms a novel Ca2+ signaling complex with ryanodine receptors and BKCa channels. Circ Res. 2005; 97: 1270-1279. PMID: 16269659
26. Hamanaka K, Jian MY, Weber DS, Alvarez DF, Townsley MI, Al-Mehdi AB, et al. TRPV4 initiates the acute calcium-dependent permeability increase during ventilator-induced lung injury in isolated mouse lungs. Am J Physiol Lung Cell Mol Physiol. 2007; 293: L923-L932. PMID: 17660328
27. Fiorio PA, Ong HL, Cheng KT, Brossa A, Bussolati B, Lockwich T, et al. TRPV4 mediates tumor-derived endothelial cell migration via arachidonic acid-activated actin remodeling. Oncogene. 2012; 31: 200-212. doi: 10.1038/onc.2011.231 PMID: 21685934
28. Hatano N, Suzuki H, Itoh Y, Muraki K. TRPV4 partially participates in proliferation of human brain capillary endothelial cells. Life Sci. 2013; 92: 317-324. doi: 10.1016/j.lfs.2013.01.002 PMID: 23333822
29. Banumathi E, O'Connor A, Gurunathan S, Simpson DA, McGeown JG, Curtis TM. VEGF-induced retinal angiogenic signaling is critically dependent on Ca(2)(+) signaling by Ca(2)(+)/calmodulin-dependent protein kinase II. Invest Ophthalmol Vis Sci. 2011; 52: 3103-3111. doi: 10.1167/iovs.10-6574 PMID: 21310919
30. Curtis TM, Major EH, Trimble ER, Scholfield CN. Diabetes-induced activation of protein kinase C inhibits store-operated Ca2+ uptake in rat retinal microvascular smooth muscle. Diabetologia. 2003; 46: 1252-1259. PMID: 12898009
31. McGahon MK, Dash DP, Arora A, Wall N, Dawicki J, Simpson DA, et al. Diabetes downregulates large-conductance Ca2+-activated potassium beta 1 channel subunit in retinal arteriolar smooth muscle. Circ Res. 2007; 100: 703-711. PMID: 17293477
32. Ramakers C, Ruijter JM, Deprez RH, Moorman AF. Assumption-free analysis of quantitative real-time polymerase chain reaction (PCR) data. Neurosci Lett. 2003; 339: 62-66. PMID: 12618301
33. Berrout J, Jin M, Mamenko M, Zaika O, Pochynyuk O, O'Neil RG. Function of transient receptor potential cation channel subfamily V member 4 (TRPV4) as a mechanical transducer in flow-sensitive segments of renal collecting duct system. J Biol Chem. 2012; 287: 8782-8791. doi: 10.1074/jbc.M111.308411 PMID: 22298783
34. Vriens J, Appendino G, Nilius B. Pharmacology of vanilloid transient receptor potential cation channels. Mol Pharmacol. 2009; 75: 1262-1279. doi: 10.1124/mol.109.055624 PMID: 19297520
35. Watanabe H, Davis JB, Smart D, Jerman JC, Smith GD, Hayes P, et al. Activation of TRPV4 channels (hVRL-2/mTRP12) by phorbol derivatives. J Biol Chem. 2002; 277: 13569-13577. PMID: 11827975
36. Dunn KM, Hill-Eubanks DC, Liedtke WB, Nelson MT. TRPV4 channels stimulate Ca2+-induced Ca2+ release in astrocytic endfeet and amplify neurovascular coupling responses. Proc Natl Acad Sci U S A. 2013; 110: 6157-6162. doi: 10.1073/pnas.1216514110 PMID: 23530219
37. Ng LC, McCormack MD, Airey JA, Singer CA, Keller PS, Shen XM, et al. TRPC1 and STIM1 mediate capacitative Ca2+ entry in mouse pulmonary arterial smooth muscle cells. J Physiol. 2009; 587: 2429-2442. doi: 10.1113/jphysiol.2009.172254 PMID: 19332490
38. Zhang L, Papadopoulos P, Hamel E. Endothelial TRPV4 channels mediate dilation of cerebral arteries: impairment and recovery in cerebrovascular pathologies related to Alzheimer's disease. Br J Pharmacol. 2013; 170: 661-670. doi: 10.1111/bph.12315 PMID: 23889563
39. Ma X, Cheng KT, Wong CO, O'Neil RG, Birnbaumer L, Ambudkar IS, et al. Heteromeric TRPV4-C1 channels contribute to store-operated Ca(2+) entry in vascular endothelial cells. Cell Calcium. 2011; 50: 502-509. doi: 10.1016/j.ceca.2011.08.006 PMID: 21930300
40. Brayden JE, Earley S, Nelson MT, Reading S. Transient receptor potential (TRP) channels, vascular tone and autoregulation of cerebral blood flow. Clin Exp Pharmacol Physiol. 2008; 35: 1116-1120. doi: 10.1111/j.1440-1681.2007.04855.x PMID: 18215190
41. Vriens J, Watanabe H, Janssens A, Droogmans G, Voets T, Nilius B. Cell swelling, heat, and chemical agonists use distinct pathways for the activation of the cation channel TRPV4. Proc Natl Acad Sci U S A. 2004; 101: 396-401. PMID: 14691263
42. Watanabe H, Vriens J, Suh SH, Benham CD, Droogmans G, Nilius B. Heat-evoked activation of TRPV4 channels in a HEK293 cell expression system and in native mouse aorta endothelial cells. J Biol Chem. 2002; 277: 47044-47051. PMID: 12354759
43. Nilius B, Droogmans G. Ion channels and their functional role in vascular endothelium. Physiol Rev. 2001; 81: 1415-1459. PMID: 11581493
44. Guler AD, Lee H, Iida T, Shimizu I, Tominaga M, Caterina M. Heat-evoked activation of the ion channel, TRPV4. J Neurosci. 2002; 22: 6408-6414. PMID: 12151520
45. Kern TS, Miller CM, Tang J, Du Y, Ball SL, Berti-Matera L. Comparison of three strains of diabetic rats with respect to the rate at which retinopathy and tactile allodynia develop. Mol Vis. 2010; 16: 1629-1639. PMID: 20806092
46. Robinson R, Barathi VA, Chaurasia SS, Wong TY, Kern TS. Update on animal models of diabetic retinopathy: from molecular approaches to mice and higher mammals. Dis Model Mech. 2012; 5: 444-456. doi: 10.1242/dmm.009597 PMID: 22730475
47. Roy S, Tonkiss J, Roy S. Aging increases retinal vascular lesions characteristic of early diabetic retinopathy. Biogerontology. 2010; 11: 447-455. doi: 10.1007/s10522-010-9263-x PMID: 20119717
48. Sharma NK, Gardiner TA, Archer DB. A morphologic and autoradiographic study of cell death and regeneration in the retinal microvasculature of normal and diabetic rats. Am J Ophthalmol. 1985; 100: 51-60. PMID: 4014380
49. Curtis TM, Gardiner TA, Stitt AW. Microvascular lesions of diabetic retinopathy: clues towards understanding pathogenesis? Eye (Lond). 2009; 23: 1496-1508. doi: 10.1038/eye.2009.108 PMID: 19444297
50. Cioffi DL, Lowe K, Alvarez DF, Barry C, Stevens T. TRPing on the lung endothelium: calcium channels that regulate barrier function. Antioxid Redox Signal. 2009; 11: 765-776. doi: 10.1089/ARS.2008.2221 PMID: 18783312
51. Gao F, Wang DH. Hypotension induced by activation of the transient receptor potential vanilloid 4 channels: role of Ca2+-activated K+ channels and sensory nerves. J Hypertens. 2010; 28: 102-110. doi: 10.1097/HJH.0b013e328332b865 PMID: 19996988
52. Willette RN, Bao W, Nerurkar S, Yue TL, Doe CP, Stankus G, et al. Systemic activation of the transient receptor potential vanilloid subtype 4 channel causes endothelial failure and circulatory collapse: Part 2. J Pharmacol Exp Ther. 2008; 326: 443-452. doi: 10.1124/jpet.107.134551 PMID: 18499744
53. Wu S, Jian MY, Xu YC, Zhou C, Al-Mehdi AB, Liedtke W, et al. Ca2+ entry via alpha1G and TRPV4 channels differentially regulates surface expression of P-selectin and barrier integrity in pulmonary capillary endothelium. Am J Physiol Lung Cell Mol Physiol. 2009; 297: L650-L657. doi: 10.1152/ajplung.00015.2009 PMID: 19617313
54. Zhang DX, Mendoza SA, Bubolz AH, Mizuno A, Ge ZD, Li R, et al. Transient receptor potential vanilloid type 4-deficient mice exhibit impaired endothelium-dependent relaxation induced by acetylcholine in vitro and in vivo. Hypertension. 2009; 53: 532-538. doi: 10.1161/HYPERTENSIONAHA.108.127100 PMID: 19188524
55. Liedtke W, Friedman JM. Abnormal osmotic regulation in trpv4-/- mice. Proc Natl Acad Sci U S A. 2003; 100: 13698-13703. PMID: 14581612