High glucose enhances intracellular Ca2+ responses triggered by purinergic stimulation in retinal neurons and microglia

Brain Research

Volumn 1316, Issue , 2010, Pages 129-138

  Pereira, Tiago de Oliveira Simões ^a   da Costa, Gabriel Nascimento Ferreira ^a   Santiago, Ana Raquel Sarabando ^a,c   Ambrósio, António Francisco ^a,c   dos Santos, Paulo Fernando Martins ^a,b  

^a UNIVERSITY OF COIMBRA   (Portugal)

^b UNIVERSITY OF COIMBRA   (Portugal)

^c IBILI   (Portugal)

Author keywords

Diabetes; Intracellular calcium; Purinergic system; Retina

Indexed keywords

CALCIUM ION; GLUCOSE; PURINERGIC P2 RECEPTOR; VOLTAGE GATED CALCIUM CHANNEL;

ANIMAL CELL; ARTICLE; CALCIUM CELL LEVEL; CALCIUM SIGNALING; CALCIUM TRANSPORT; CONTROLLED STUDY; EVOKED RESPONSE; MEDIATOR RELEASE; MICROGLIA; MOLECULAR IMAGING; NERVE CELL CULTURE; NERVE CELL NECROSIS; NERVE CELL STIMULATION; NEUROTRANSMITTER RELEASE; NEWBORN; NONHUMAN; PRIORITY JOURNAL; RAT; RETINA NERVE CELL;

ADENOSINE TRIPHOSPHATE; ANIMALS; CALCIUM; CALCIUM CHANNELS; CELLS, CULTURED; GLUCOSE; INTRACELLULAR SPACE; MICROGLIA; RATS; RATS, WISTAR; RECEPTORS, PURINERGIC P2; RETINA; RETINAL NEURONS; SODIUM;

RATTUS;

EID: 75349097992     PISSN: 00068993     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.brainres.2009.12.034     Document Type: Article

References (60)

1. Abbracchio M.P., Burnstock G., Boeynaems J.M., Barnard E.A., Boyer J.L., Kennedy C., Knight G.E., Fumagalli M., Gachet C., Jacobson K.A., and Weisman G.A. International Union of Pharmacology LVIII: update on the P2Y G protein-coupled nucleotide receptors: from molecular mechanisms and pathophysiology to therapy. Pharmacol. Rev. 58 (2006) 281-341
2. Alderton W.K., Cooper C.E., and Knowles R.G. Nitric oxide synthases: structure, function and inhibition. Biochem. J. 357 (2001) 593-615
3. Azuma M., and Shearer T.R. The role of calcium-activated protease calpain in experimental retinal pathology. Surv. Ophthalmol. 53 (2008) 150-163
4. Barber A.J., Lieth E., Khin S.A., Antonetti D.A., Buchanan A.G., and Gardner T.W. Neural apoptosis in the retina during experimental and human diabetes. Early onset and effect of insulin. J. Clin. Invest. 102 (1998) 783-791
5. Brandle U., Guenther E., Irrle C., and Wheeler-Schilling T.H. Gene expression of the P2X receptors in the rat retina. Brain Res. Mol. Brain Res. 59 (1998) 269-272
6. Bringmann A., Pannicke T., Moll V., Milenkovic I., Faude F., Enzmann V., Wolf S., and Reichenbach A. Up-regulation of P2X(7) receptor currents in Muller glial cells during proliferative vitreoretinopathy. Invest. Ophthalmol. Vis. Sci. 42 (2001) 860-867
7. Burnstock G. Introduction: P2 receptors. Curr. Top. Med. Chem. 4 (2004) 793-803
8. Burnstock G. Purine and pyrimidine receptors. Cell. Mol. Life Sci. 64 (2007) 1471-1483
9. Carmo A., Cunha-Vaz J.G., Carvalho A.P., and Lopes M.C. Nitric oxide synthase activity in retinas from non-insulin-dependent diabetic Goto-Kakizaki rats: correlation with blood-retinal barrier permeability. Nitric Oxide 4 (2000) 590-596
10. Carrasquero L.M., Delicado E.G., Bustillo D., Gutierrez-Martin Y., Artalejo A.R., and Miras-Portugal M.T. P2X7 and P2Y13 purinergic receptors mediate intracellular calcium responses to BzATP in rat cerebellar astrocytes. J. Neurochem. 110 (2009) 879-889
11. Costa G., Pereira T., Neto A.M., Cristovao A.J., Ambrosio A.F., and Santos P.F. High glucose changes extracellular adenosine triphosphate levels in rat retinal cultures. J. Neurosci. Res. 87 (2009) 1375-1380
12. Demircan N., Safran B.G., Soylu M., Ozcan A.A., and Sizmaz S. Determination of vitreous interleukin-1 (IL-1) and tumour necrosis factor (TNF) levels in proliferative diabetic retinopathy. Eye 20 (2006) 1366-1369
13. 2+]i regulation by glutamate receptor agonists in cultured chick retina cells. Vis. Res. 36 (1996) 1091-1102
14. Duarte C.B., Ferreira I.L., Santos P.F., Carvalho A.L., Agostinho P.M., and Carvalho A.P. Glutamate in life and death of retinal amacrine cells. Gen. Pharmacol. 30 (1998) 289-295
15. Duarte J.M., Oses J.P., Rodrigues R.J., and Cunha R.A. Modification of purinergic signaling in the hippocampus of streptozotocin-induced diabetic rats. Neuroscience 149 (2007) 382-391
16. Erb L., Liao Z., Seye C.I., and Weisman G.A. P2 receptors: intracellular signaling. Pflugers Arch. 452 (2006) 552-562
17. Fries J.E., Wheeler-Schilling T.H., Guenther E., and Kohler K. Expression of P2Y1, P2Y2, P2Y4, and P2Y6 receptor subtypes in the rat retina. Invest. Ophthalmol. Vis. Sci. 45 (2004) 3410-3417
18. Fries J.E., Goczalik I.M., Wheeler-Schilling T.H., Kohler K., Guenther E., Wolf S., Wiedemann P., Bringmann A., Reichenbach A., Francke M., and Pannicke T. Identification of P2Y receptor subtypes in human Muller glial cells by physiology, single cell RT-PCR, and immunohistochemistry. Invest. Ophthalmol. Vis. Sci. 46 (2005) 3000-3007
19. Gardner T.W., Antonetti D.A., Barber A.J., LaNoue K.F., and Levison S.W. Diabetic retinopathy: more than meets the eye. Surv. Ophthalmol. 47 Suppl. 2 (2002) S253-S262
20. Gaucher D., Chiappore J.A., Paques M., Simonutti M., Boitard C., Sahel J.A., Massin P., and Picaud S. Microglial changes occur without neural cell death in diabetic retinopathy. Vis. Res. 47 (2007) 612-623
21. Hall K.E., Sima A.A., and Wiley J.W. Voltage-dependent calcium currents are enhanced in dorsal root ganglion neurones from the Bio Bred/Worchester diabetic rat. J. Physiol. 486 Pt 2 (1995) 313-322
22. Hartwick A.T., Hamilton C.M., and Baldridge W.H. Glutamatergic calcium dynamics and deregulation of rat retinal ganglion cells. J. Physiol. 586 (2008) 3425-3446
23. Heidelberger R. Mechanisms of tonic, graded release: lessons from the vertebrate photoreceptor. J. Physiol. 585 (2007) 663-667
24. Holback S., Adlerz L., Gatsinzi T., Jacobsen K.T., and Iverfeldt K. PI3-K- and PKC-dependent up-regulation of APP processing enzymes by retinoic acid. Biochem. Biophys. Res. Commun. 365 (2008) 298-303
25. Ishii K., Kaneda M., Li H., Rockland K.S., and Hashikawa T. Neuron-specific distribution of P2X7 purinergic receptors in the monkey retina. J. Comp. Neurol. 459 (2003) 267-277
26. Kaneda M., Ishii K., Morishima Y., Akagi T., Yamazaki Y., Nakanishi S., and Hashikawa T. OFF-cholinergic-pathway-selective localization of P2X2 purinoceptors in the mouse retina. J. Comp. Neurol. 476 (2004) 103-111
27. Kern T.S. Contributions of inflammatory processes to the development of the early stages of diabetic retinopathy. Exp. Diabetes Res. 2007 (2007) 95103
28. Kern T.S., and Barber A.J. Retinal ganglion cells in diabetes. J. Physiol. 586 (2008) 4401-4408
29. Kowluru R.A. Diabetes-induced elevations in retinal oxidative stress, protein kinase C and nitric oxide are interrelated. Acta Diabetol. 38 (2001) 179-185
30. Kruglikov I., Gryshchenko O., Shutov L., Kostyuk E., Kostyuk P., and Voitenko N. Diabetes-induced abnormalities in ER calcium mobilization in primary and secondary nociceptive neurons. Pflugers Arch. 448 (2004) 395-401
31. Leal E.C., Manivannan A., Hosoya K., Terasaki T., Cunha-Vaz J., Ambrosio A.F., and Forrester J.V. Inducible nitric oxide synthase isoform is a key mediator of leukostasis and blood-retinal barrier breakdown in diabetic retinopathy. Invest. Ophthalmol. Vis. Sci. 48 (2007) 5257-5265
32. McKernan D.P., Guerin M.B., O'Brien C.J., and Cotter T.G. A key role for calpains in retinal ganglion cell death. Invest. Ophthalmol. Vis. Sci. 48 (2007) 5420-5430
33. Morigiwa K., Quan M., Murakami M., Yamashita M., and Fukuda Y. P2 Purinoceptor expression and functional changes of hypoxia-activated cultured rat retinal microglia. Neurosci. Lett. 282 (2000) 153-156
34. Pannicke T., Fischer W., Biedermann B., Schadlich H., Grosche J., Faude F., Wiedemann P., Allgaier C., Illes P., Burnstock G., and Reichenbach A. P2X7 receptors in Muller glial cells from the human retina. J. Neurosci. 20 (2000) 5965-5972
35. Ramsey D.J., Ripps H., and Qian H. Streptozotocin-induced diabetes modulates GABA receptor activity of rat retinal neurons. Exp. Eye Res. 85 (2007) 413-422
36. Reddy A.B., Ramana K.V., Srivastava S., Bhatnagar A., and Srivastava S.K. Aldose reductase regulates high glucose-induced ectodomain shedding of tumor necrosis factor (TNF)-alpha via protein kinase C-delta and TNF-alpha converting enzyme in vascular smooth muscle cells. Endocrinology 150 (2009) 63-74
37. Resta V., Novelli E., Vozzi G., Scarpa C., Caleo M., Ahluwalia A., Solini A., Santini E., Parisi V., Di Virgilio F., and Galli-Resta L. Acute retinal ganglion cell injury caused by intraocular pressure spikes is mediated by endogenous extracellular ATP. Eur. J. Neurosci. 25 (2007) 2741-2754
38. Santiago A.R., Pereira T.S., Garrido M.J., Cristovao A.J., Santos P.F., and Ambrosio A.F. High glucose and diabetes increase the release of [3H]-d-aspartate in retinal cell cultures and in rat retinas. Neurochem. Int. 48 (2006) 453-458
39. Santiago A.R., Rosa S.C., Santos P.F., Cristovao A.J., Barber A.J., and Ambrosio A.F. Elevated glucose changes the expression of ionotropic glutamate receptor subunits and impairs calcium homeostasis in retinal neural cells. Invest. Ophthalmol. Vis. Sci. 47 (2006) 4130-4137
40. Santiago A.R., Cristovao A.J., Santos P.F., Carvalho C.M., and Ambrosio A.F. High glucose induces caspase-independent cell death in retinal neural cells. Neurobiol. Dis. 25 (2007) 464-472
41. Santiago A.R., Gaspar J.M., Baptista F.I., Cristovao A.J., Santos P.F., Kamphuis W., and Ambrosio A.F. Diabetes changes the levels of ionotropic glutamate receptors in the rat retina. Mol. Vis. 15 (2009) 1620-1630
42. Santos P.F., Santos M.S., Carvalho A.P., and Duarte C.B. Modulation of [3H]acetylcholine release from cultured amacrine-like neurons by adenosine A1 receptors. J. Neurochem. 71 (1998) 1086-1094
43. Santos P.F., Caramelo O.L., Carvalho A.P., and Duarte C.B. Characterization of ATP release from cultures enriched in cholinergic amacrine-like neurons. J. Neurobiol. 41 (1999) 340-348
44. Shigematsu Y., Shimoda Y., and Kaneda M. Distribution of immunoreactivity for P2X3, P2X5, and P2X6-purinoceptors in mouse retina. J. Mol. Histol. 38 (2007) 369-371
45. Solini A., Chiozzi P., Falzoni S., Morelli A., Fellin R., and Di Virgilio F. High glucose modulates P2X7 receptor-mediated function in human primary fibroblasts. Diabetologia 43 (2000) 1248-1256
46. Solini A., Iacobini C., Ricci C., Chiozzi P., Amadio L., Pricci F., Di Mario U., Di Virgilio F., and Pugliese G. Purinergic modulation of mesangial extracellular matrix production: role in diabetic and other glomerular diseases. Kidney Int. 67 (2005) 875-885
47. 2+-dependent regulation of phototransduction. Photochem. Photobiol. 84 (2008) 903-910
48. 2+-permeable P2X receptor channels in cultured rat retinal ganglion cells. J. Neurosci. 19 (1999) 3353-3366
49. 2+ channels in dorsal root ganglia from streptozotocin-induced diabetic mice. Life Sci. 79 (2006) 1995-2000
50. Voitenko N.V., Kostyuk E.P., Kruglikov I.A., and Kostyuk P.G. Changes in calcium signaling in dorsal horn neurons in rats with streptozotocin-induced diabetes. Neuroscience 94 (1999) 887-890
51. Wang X.L., Jiang X.D., and Liang P.J. Intracellular calcium concentration changes initiated by N-methyl-d-aspartic acid receptors in retinal horizontal cells. Neuroreport 19 (2008) 675-678
52. Ward M.M., Puthussery T., and Fletcher E.L. Localization and possible function of P2Y(4) receptors in the rodent retina. Neuroscience 155 (2008) 1262-1274
53. Warrier A., Borges S., Dalcino D., Walters C., and Wilson M. Calcium from internal stores triggers GABA release from retinal amacrine cells. J. Neurophysiol. 94 (2005) 4196-4208
54. Wheeler-Schilling T.H., Marquordt K., Kohler K., Jabs R., and Guenther E. Expression of purinergic receptors in bipolar cells of the rat retina. Brain Res. Mol. Brain Res. 76 (2000) 415-418
55. Wheeler-Schilling T.H., Marquordt K., Kohler K., Guenther E., and Jabs R. Identification of purinergic receptors in retinal ganglion cells. Brain Res. Mol. Brain Res. 92 (2001) 177-180
56. Yang L.P., Sun H.L., Wu L.M., Guo X.J., Dou H.L., Tso M.O., Zhao L., and Li S.M. Baicalein reduces inflammatory process in a rodent model of diabetic retinopathy. Invest. Ophthalmol. Vis. Sci. 50 (2009) 2319-2327
57. Yusaf S.P., Goodman J., Gonzalez I.M., Bramwell S., Pinnock R.D., Dixon A.K., and Lee K. Streptozocin-induced neuropathy is associated with altered expression of voltage-gated calcium channel subunit mRNAs in rat dorsal root ganglion neurones. Biochem. Biophys. Res. Commun. 289 (2001) 402-406
58. Zeng X.X., Ng Y.K., and Ling E.A. Neuronal and microglial response in the retina of streptozotocin-induced diabetic rats. Vis. Neurosci. 17 (2000) 463-471
59. 2+ and kills retinal ganglion cells. Invest. Ophthalmol. Vis. Sci. 46 (2005) 2183-2191
60. Zhang J., Wu Y., Jin Y., Ji F., Sinclair S.H., Luo Y., Xu G., Lu L., Dai W., Yanoff M., Li W., and Xu G.T. Intravitreal injection of erythropoietin protects both retinal vascular and neuronal cells in early diabetes. Invest. Ophthalmol. Vis. Sci. 49 (2008) 732-742