Mechanisms of ATP release by human trabecular meshwork cells, the enabling step in purinergic regulation of aqueous humor outflow

Journal of Cellular Physiology

Volumn 227, Issue 1, 2012, Pages 172-182

  Li, Ang ^a   Leung, Chi Ting ^a   Peterson Yantorno, Kim ^a   Stamer, W Daniel ^b   Mitchell, Claire H ^a   Civan, Mortimer M ^a  

^a UNIVERSITY OF PENNSYLVANIA   (United States)

^b UNIVERSITY OF ARIZONA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE TRIPHOSPHATE; CALCIUM ION; DITHIOTHREITOL; GAP JUNCTION PROTEIN; IONOMYCIN; MEMBRANE PROTEIN; PANNEXIN 1; PROBENECID; PURINERGIC P2X7 RECEPTOR; UNCLASSIFIED DRUG;

AQUEOUS HUMOR OUTFLOW; ARTICLE; CELL FUNCTION; CELL STRAIN HEK293; CELL SWELLING; CONTROLLED STUDY; HUMAN; HUMAN CELL; MUSCLE HYPOTONIA; NUCLEOTIDE TRANSPORT; OXIDATION; PRIORITY JOURNAL; PROTEIN EXPRESSION; TRABECULAR MESHWORK;

ADENOSINE; ADENOSINE TRIPHOSPHATE; AQUEOUS HUMOR; BLOTTING, WESTERN; CONNEXINS; GLAUCOMA; HEK293 CELLS; HUMANS; INTRAOCULAR PRESSURE; LUMINESCENT MEASUREMENTS; MICROSCOPY, CONFOCAL; NERVE TISSUE PROTEINS; REAL-TIME POLYMERASE CHAIN REACTION; RECEPTORS, PURINERGIC P2X7; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; TRABECULAR MESHWORK;

EID: 80054954153     PISSN: 00219541     EISSN: 10974652     Source Type: Journal    
DOI: 10.1002/jcp.22715     Document Type: Article

References (72)

1. Aga M, Bradley JM, Keller KE, Kelley MJ, Acott TS. 2008. Specialized podosome- or invadopodia-like structures (PILS) for focal trabecular meshwork extracellular matrix turnover. Invest Ophthalmol Vis Sci 49:5353-5365.
2. Al-Aswad LA, Gong H, Lee D, O'Donnell ME, Brandt JD, Ryan WJ, Schroeder A, Erickson KA. 1999. Effects of Na-K-2Cl cotransport regulators on outflow facility in calf and human eyes in vitro. Invest Ophthalmol Vis Sci 40:1695-1701.
3. Avila MY, Stone RA, Civan MM. 2001. A(1)-, A(2A)- and A(3)-subtype adenosine receptors modulate intraocular pressure in the mouse. Br J Pharmacol 134:241-245.
4. Bao L, Locovei S, Dahl G. 2004a. Pannexin membrane channels are mechanosensitive conduits for ATP. FEBS Lett 572:65-68.
5. Bao L, Sachs F, Dahl G. 2004b. Connexins are mechanosensitive. Am J Physiol Cell Physiol 287:C1389-C1395.
6. Baranova A, Ivanov D, Petrash N, Pestova A, Skoblov M, Kelmanson I, Shagin D, Nazarenko S, Geraymovych E, Litvin O, Tiunova A, Born TL, Usman N, Staroverov D, Lukyanov S, Panchin Y. 2004. The mammalian pannexin family is homologous to the invertebrate innexin gap junction proteins. Genomics 83:706-716.
7. Bergfeld GR, Forrester T. 1992. Release of ATP from human erythrocytes in response to a brief period of hypoxia and hypercapnia. Cardiovasc Res 26:40-47.
8. Bruzzone R, Barbe MT, Jakob NJ, Monyer H. 2005. Pharmacological properties of homomeric and heteromeric pannexin hemichannels expressed in Xenopus oocytes. J Neurochem 92:1033-1043.
9. Bunse S, Locovei S, Schmidt M, Qiu F, Zoidl G, Dahl G, Dermietzel R. 2009. The potassium channel subunit Kvb3 interacts with pannexin 1 and attenuates its sensitivity to changes in redox potentials. Febs J 276:6258-6270.
10. Chow J, Liton PB, Luna C, Wong F, Gonzalez P. 2007. Effect of cellular senescence on the P2Y-receptor mediated calcium response in trabecular meshwork cells. Mol Vis 13:1926-1933.
11. Collaborative Normal-Tension Glaucoma Study Group. 1998a. Comparison of glaucomatous progression between untreated patients with normal-tension glaucoma and patients with therapeutically reduced intraocular pressures. Am J Ophthalmol 126:487-497.
12. Collaborative Normal-Tension Glaucoma Study Group. 1998b. The effectiveness of intraocular pressure reduction in the treatment of normal-tension glaucoma. Am J Ophthalmol 126:498-505.
13. Crosson CE. 1992. Ocular hypotensive activity of the adenosine agonist (R)-phenylisopropyladenosine in rabbits. Curr Eye Res 11:453-458.
14. Crosson CE. 1995. Adenosine receptor activation modulates intraocular pressure in rabbits. J Pharmacol Exp Ther 273:320-326.
15. Crosson CE. 2001. Intraocular pressure responses to the adenosine agonist cyclohexyladenosine: Evidence for a dual mechanism of action. Invest Ophthalmol Vis Sci 42:1837-1840.
16. Crosson CE, Gray T. 1996. Characterization of ocular hypertension induced by adenosine agonists. Invest Ophthalmol Vis Sci 37:1833-1839.
17. Crosson CE, Yates PW, Bhat AN, Mukhin YV, Husain S. 2004. Evidence for multiple P2Y receptors in trabecular meshwork cells. J Pharmacol Exp Ther 309:484-489.
18. Crosson CE, Sloan CF, Yates PW., 2005. Modulation of conventional outflow facility by the adenosine A1 agonist N6-cyclohexyladenosine. Invest Ophthalmol Vis Sci 46:3795-3799.
19. Daines BS, Kent AR, McAleer MS, Crosson CE. 2003. Intraocular adenosine levels in normal and ocular-hypertensive patients. J Ocul Pharmacol Ther 19:113-119.
20. De Vuyst E, Decrock E, De Bock M, Yamasaki H, Naus CC, Evans WH, Leybaert L. 2007. Connexin hemichannels and gap junction channels are differentially influenced by lipopolysaccharide and basic fibroblast growth factor. Mol Biol Cell 18:34-46.
21. Ebihara L, Liu X, Pal JD. 2003. Effect of external magnesium and calcium on human connexin46 hemichannels. Biophys J 84:277-286.
22. Eskandari S, Zampighi GA, Leung DW, Wright EM, Loo DD. 2002. Inhibition of gap junction hemichannels by chloride channel blockers. J Membr Biol 185:93-102.
23. Ethier CR. 2002. The inner wall of Schlemm's canal. Exp Eye Res 74:161-172.
24. Evans DW, Hosking SL, Embleton SJ, Morgan AJ, Bartlett JD. 2002. Spectral content of the intraocular pressure pulse wave: Glaucoma patients versus normal subjects. Graefes Arch Clin Exp Ophthalmol 240:475-480.
25. Fleischhauer JC, Mitchell CH, Stamer WD, Karl MO, Peterson-Yantorno K, Civan MM. 2003. Common actions of adenosine receptor agonists in modulating human trabecular meshwork cell transport. J Membr Biol 193:121-136.
26. Freddo TF, Johnson M. 2008. Aqueous humor outflow resistance. In: Civan MM, editor. The eye's aqueous humor, 2nd edition. San Diego: Elsevier. pp. 161-192.
27. Garré JM, Retamal MA, Cassina P, Barbeito L, Bukauskas FF, Sáez JC, Bennett MV, Abudara V. 2010. FGF-1 induces ATP release from spinal astrocytes in culture and opens pannexin and connexin hemichannels. Proc Natl Acad Sci USA 107:22659-22664.
28. Gong H, Tripathi RC, Tripathi BJ. 1996. Morphology of the aqueous outflow pathway. Microsc Res Tech 33:336-367.
29. Gual A, Llobet A, Gilabert R, Borras M, Pales J, Bergamini MV, Belmonte C. 1997. Effects of time of storage, albumin, and osmolality changes on outflow facility (C) of bovine anterior segment in vitro. Invest Ophthalmol Vis Sci 38:2165-2171.
30. Husain S, Shearer TW, Crosson CE. 2007. Mechanisms linking adenosine A1 receptors and extracellular signal-regulated kinase 1/2 activation in human trabecular meshwork cells. J Pharmacol Exp Ther 320:258-265.
31. Iglesias R, Spray DC, Scemes E. 2009. Mefloquine blockade of Pannexin1 currents: Resolution of a conflict. Cell Commun Adhes 16:131-137.
32. Johnson M, Erickson K. 2000. Mechanisms and routes of aqueous humor drainage. In: Albert DM, Jakobiec FA, editors. Principles and practice of ophthalmology. Philadelphia: WB Saunders. pp. 2577-2595.
33. Johnson M, Shapiro A, Ethier CR, Kamm RD. 1992. Modulation of outflow resistance by the pores of the inner wall endothelium. Invest Ophthalmol Vis Sci 33:1670-1675.
34. Johnstone MA. 1979. Pressure-dependent changes in nuclei and the process origins of the endothelial cells lining Schlemm's canal. Invest Ophthalmol Vis Sci 18:44-51.
35. Kass MA, Heuer DK, Higginbotham EJ, Johnson CA, Keltner JL, Miller JP, Parrish RK II, Wilson MR, Gordon MO. 2002. The Ocular Hypertension Treatment Study: A randomized trial determines that topical ocular hypotensive medication delays or prevents the onset of primary open-angle glaucoma. Arch Ophthalmol 120:701-713 (discussion 829-730).
36. Khakh BS, North RA. 2006. P2X receptors as cell-surface ATP sensors in health and disease. Nature 442:527-532.
37. Kimura S, Suzuki K, Sagara T, Nishida T, Yamamoto T, Kitazawa Y. 2000. Regulation of connexin phosphorylation and cell-cell coupling in trabecular meshwork cells. Invest Ophthalmol Vis Sci 41:2222-2228.
38. Krupin T, Civan MM. 1996. The physiologic basis of aqueous humor formation. In: Ritch R, Shields MB, Krupin T, editors. The glaucomas, 2nd edition. St Louis: Mosby. pp. 251-280.
39. Kumar J, Epstein DL. 2011. Rho GTPase-mediated cytoskeletal organization in Schlemm's canal cells play a critical role in the regulation of aqueous humor outflow facility. J Cell Biochem 112:600-606.
40. Lévesque SA, Lavoie EG, Lecka J, Bigonnesse F, Sévigny J. 2007. Specificity of the ecto-ATPase inhibitor ARL 67156 on human and mouse ectonucleotidases. Br J Pharmacol 152:141-150.
41. Li A, Leung CT, Peterson-Yantorno K, Mitchell CH, Civan MM. 2010. Pathways for ATP release by bovine ciliary epithelial cells, the initial step in purinergic regulation of aqueous humor inflow. Am J Physiol Cell Physiol 299:C1308-C1317.
42. Locovei S, Wang J, Dahl G. 2006. Activation of pannexin 1 channels by ATP through P2Y receptors and by cytoplasmic calcium. FEBS Lett 580:239-244.
43. Locovei S, Scemes E, Qiu F, Spray DC, Dahl G. 2007. Pannexin1 is part of the pore forming unit of the P2X(7) receptor death complex. FEBS Lett 581:483-488.
44. Lu Z, Overby DR, Scott PA, Freddo TF, Gong H. 2008. The mechanism of increasing outflow facility by rho-kinase inhibition with Y-27632 in bovine eyes. Exp Eye Res 86:271-281.
45. Luna C, Li G, Qiu J, Challa P, Epstein DL, Gonzalez P. 2009. Extracellular release of ATP mediated by cyclic mechanical stress leads to mobilization of AA in trabecular meshwork cells. Invest Ophthalmol Vis Sci 50:5805-5810.
46. Lütjen-Drecoll E, Rohen JW. 1996. Morphology of aqueous outflow pathways in normal and glaucomatous eyes. In: Ritch R, Shields MB, Krupin T, editors. The glaucomas, 2nd edition. St. Louis: Mosby. pp. 89-123.
47. Ma W, Hui H, Pelegrin P, Surprenant A. 2009. Pharmacological characterization of pannexin-1 currents expressed in mammalian cells. J Pharmacol Exp Ther 328:409-418.
48. Mitchell CH, Carré DA, McGlinn AM, Stone RA, Civan MM. 1998. A release mechanism for stored ATP in ocular ciliary epithelial cells. Proc Natl Acad Sci U S A 95:7174-7178.
49. Orellana JA, Saez PJ, Shoji KF, Schalper KA, Palacios-Prado N, Velarde V, Giaume C, Bennett MV, Saez JC. 2009. Modulation of brain hemichannels and gap junction channels by pro-inflammatory agents and their possible role in neurodegeneration. Antioxid Redox Signal 11:369-399.
50. Overby D, Gong H, Qiu G, Freddo TF, Johnson M. 2002. The mechanism of increasing outflow facility during washout in the bovine eye. Invest Ophthalmol Vis Sci 43:3455-3464.
51. Panchin Y, Kelmanson I, Matz M, Lukyanov K, Usman N, Lukyanov S. 2000. A ubiquitous family of putative gap junction molecules. Curr Biol 10:R473-R474.
52. Pang IH, Shade DL, Clark AF, Steely HT, DeSantis L. 1994. Preliminary characterization of a transformed cell strain derived from human trabecular meshwork. Curr Eye Res 13:51-63.
53. Paper W, Kroeber M, Heersink S, Stephan DA, Fuchshofer R, Russell P, Tamm ER. 2008. Elevated amounts of myocilin in the aqueous humor of transgenic mice cause significant changes in ocular gene expression. Exp Eye Res 87:257-267.
54. Pedrigi RM, Simon D, Reed A, Stamer WD, Overby DR. 2011. A model of giant vacuole dynamics in human Schlemm's canal endothelial cells. Exp Eye Res 92:57-66.
55. 7 receptor. Embo J 25:5071-5082.
56. Pelegrin P, Surprenant A. 2007. Pannexin-1 couples to maitotoxin- and nigericin-induced interleukin-1beta release through a dye uptake-independent pathway. J Biol Chem 282:2386-2394.
57. Raviola G, Raviola E. 1981. Paracellular route of aqueous outflow in the trabecular meshwork and canal of Schlemm. A freeze-fracture study of the endothelial junctions in the sclerocorneal angel of the macaque monkey eye. Invest Ophthalmol Vis Sci 21:52-72.
58. Rohen JW. 1963. Experimental studies on the trabecular meshwork in primates. Arch Ophthalmol 69:91-105.
59. Scott PA, Overby DR, Freddo TF, Gong H. 2007. Comparative studies between species that do and do not exhibit the washout effect. Exp Eye Res 84:435-443.
60. Shearer TW, Crosson CE. 2002. Adenosine A1 receptor modulation of MMP-2 secretion by trabecular meshwork cells. Invest Ophthalmol Vis Sci 43:3016-3020.
61. Silverman W, Locovei S, Dahl G. 2008. Probenecid, a gout remedy, inhibits pannexin 1 channels. Am J Physiol Cell Physiol 295:C761-C767.
62. Stamer WD, Seftor RE, Williams SK, Samaha HA, Snyder RW. 1995. Isolation and culture of human trabecular meshwork cells by extracellular matrix digestion. Curr Eye Res 14:611-617.
63. Tamm ER. 2009. The trabecular meshwork outflow pathways: Structural and functional aspects. Exp Eye Res 88:648-655.
64. The AGIS investigators. 2000. The Advanced Glaucoma Intervention Study (AGIS): 7. The relationship between control of intraocular pressure and visual field deterioration. Am J Ophthalmol 130:429-440.
65. Tian B, Gabelt BT, Crosson CE, Kaufman PL. 1997. Effects of adenosine agonists on intraocular pressure and aqueous humor dynamics in cynomolgus monkeys. Exp Eye Res 64:979-989.
66. Tripathi RC. 1996. Clinical implications of aqueous humor growth factors in glaucoma. In: Ritch R, Shields MB, Krupin T, editors. The glaucomas, 2nd edition. St. Louis: Mosby. pp. 71-87.
67. Virginio C, MacKenzie A, North RA, Surprenant A. 1999. Kinetics of cell lysis, dye uptake and permeability changes in cells expressing the rat P2X7 receptor. J Physiol 519:335-346.
68. Wheaton WW, Chandel NS. 2011. Hypoxia. 2. Hypoxia regulates cellular metabolism. Am J Physiol Cell Physiol. 300:C385-393.
69. Yan Z, Li S, Liang Z, Tomic M, Stojilkovic SS. 2008. The P2X7 receptor channel pore dilates under physiological ion conditions. J Gen Physiol 132:563-573.
70. Yegutkin GG. 2008. Nucleotide- and nucleoside-converting ectoenzymes: Important modulators of purinergic signalling cascade. Biochim Biophys Acta 1783:673-694.
71. Zhuo YH, He Y, Leung KW, Hou F, Li YQ, Chai F, Ge J. 2010. Dexamethasone disrupts intercellular junction formation and cytoskeleton organization in human trabecular meshwork cells. Mol Vis 16:61-71.
72. Zimmermann H. 2000. Extracellular metabolism of ATP and other nucleotides. Naunyn Schmiedebergs Arch Pharmacol 362:299-309.