Novel role for the δ-opioid receptor in hypoxic preconditioning in rat retinas

Journal of Neurochemistry

Volumn 108, Issue 3, 2009, Pages 741-754

  Peng, Pai Huei ^b   Huang, Ho Shiang ^c   Lee, Yih Jing ^a   Chen, Yih Sharng ^c   Ma, Ming Chieh ^a  

^a FU JEN CATHOLIC UNIVERSITY   (Taiwan)

^b SHIN KONG WU HO SU MEMORIAL HOSPITAL   (Taiwan)

^c NATIONAL TAIWAN UNIVERSITY HOSPITAL   (Taiwan)

Author keywords

opioid receptor; Extracellular signal regulated kinase; Hypoxia inducible factor 1 ; Hypoxic preconditioning; Intraocular pressure; Oxidative stress

Indexed keywords

8 ISOPROSTAGLANDIN F2 ALPHA; CASPASE 3; CATALASE; COPPER ZINC SUPEROXIDE DISMUTASE; DELTA OPIATE RECEPTOR; GLUTATHIONE PEROXIDASE; HYPOXIA INDUCIBLE FACTOR 1ALPHA; LEUCINE ENKEPHALIN; MANGANESE SUPEROXIDE DISMUTASE; MITOGEN ACTIVATED PROTEIN KINASE; NALTRINDOLE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE 2; SMALL INTERFERING RNA; SUPEROXIDE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; CONTROLLED STUDY; ENZYME ACTIVITY; EYE PROTECTION; FEMALE; HYPOXIA; INTRAOCULAR PRESSURE; NONHUMAN; NUCLEOTIDE SEQUENCE; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; REPERFUSION INJURY; RETINA ISCHEMIA; UPREGULATION;

ANIMALS; ANOXIA; ANTIOXIDANTS; BLOTTING, WESTERN; DINOPROST; ENKEPHALIN, LEUCINE; HYPOXIA-INDUCIBLE FACTOR 1, ALPHA SUBUNIT; IMMUNOHISTOCHEMISTRY; INTRAOCULAR PRESSURE; ISCHEMIC PRECONDITIONING; LIPID PEROXIDATION; MALE; NALTREXONE; NARCOTIC ANTAGONISTS; OXIDATIVE STRESS; RATS; RATS, WISTAR; RECEPTORS, OPIOID, DELTA; RETINA; RETINAL VESSELS; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, SMALL INTERFERING; SIGNAL TRANSDUCTION; SPECTROMETRY, FLUORESCENCE; SUPEROXIDES;

RATTUS;

EID: 58149358815     PISSN: 00223042     EISSN: 14714159     Source Type: Journal    
DOI: 10.1111/j.1471-4159.2008.05807.x     Document Type: Article

References (51)

1. 2]deltorphin-I in amacrine cells of rat retina. Peptides 15, 49 54.
2. Abraham A. S., Kay J. M., Cole R. B. et al. (1971) Haemodynamic and pathological study of the effect of chronic hypoxia and subsequent recovery on the heart and pulmonary vasculature of the rat. Cardiovasc. Res. 5, 95 102.
3. Agardh C. D., Gustavsson C., Hagert P. et al. (2006) Expression of antioxidant enzymes in rat retinal ischemia followed by reperfusion. Metabolism 55, 892 898.
4. Benov L., Sztejnberg L. Fridovich I. (1998) Critical evaluation of the use of hydroethidine as a measure of superoxide anion radical. Free Radic. Biol. Med. 25, 826 831.
5. 2+/calmodulin- dependent transcriptional activation of delta-opioid receptor gene expression induced by membrane depolarization in NG108-15 cells. J. Neurochem. 70, 105 112.
6. Cao W., Drumheller A., Zaharia M. et al. (1993) Effects of experimentally induced ischemia on dopamine metabolism in rabbit retina. Invest. Ophthalmol. Vis. Sci. 34, 3140 3146.
7. Chauhan B. C., Pan J., Archibald M. L. et al. (2002) Effect of intraocular pressure on optic disc topography, electroretinography, and axonal loss in a chronic pressure-induced rat model of optic nerve damage. Invest. Ophthalmol. Vis. Sci. 43, 2969 2976.
8. Chen S. T., von Bussmann K. A., Garey L. J. et al. (1994) Protein gene product 9.5-immunoreactive retinal neurons in normal developing rats and rats with optic nerve or tract lesion. Brain Res. Dev. Brain Res. 78, 265 272.
9. Dong J. W., Zhu H. F., Zhu W. Z. et al. (2003) Intermittent hypoxia attenuates ischemia/reperfusion induced apoptosis in cardiac myocytes via regulating Bcl-2/Bax expression. Cell Res. 13, 385 391.
10. Feng N. H., Lee H. H., Shiang J. C. et al. (2008) Transient receptor potential vanilloid type 1 channels act as mechanoreceptors and cause substance P release and sensory activation in rat kidneys. Am. J. Physiol. Renal Physiol. 294, F316 F325.
11. Gosbell A. D., Stefanovic N., Scurr L. L. et al. (2006) Retinal light damage: structural and functional effects of the antioxidant glutathione peroxidase-1. Invest. Ophthalmol. Vis. Sci. 47, 2613 2622.
12. Grimm C., Wenzel A., Groszer M. et al. (2002) HIF-1-induced erythropoietin in the hypoxic retina protects against light-induced retinal degeneration. Nat. Med. 8, 718 724.
13. Grimm C., Hermann D. M., Bogdanova A. et al. (2005) Neuroprotection by hypoxic preconditioning: HIF-1 and erythropoietin protect from retinal degeneration. Semin. Cell Dev. Biol. 16, 531 538.
14. Grozdanic S. D., Sakaguchi D. S., Kwon Y. H. et al. (2003) Functional characterization of retina and optic nerve after acute ocular ischemia in rats. Invest. Ophthalmol. Vis. Sci. 44, 2597 2605.
15. Harada T., Harada C., Wang Y. L. et al. (2004) Role of ubiquitin carboxy terminal hydrolase-L1 in neural cell apoptosis induced by ischemic retinal injury in vivo. Am. J. Pathol. 164, 59 64.
16. Howells R. D., Groth J., Hiller J. M. et al. (1980) Opiate binding sites in the retina: properties and distribution. J. Pharmacol. Exp. Ther. 215, 60 64.
17. Huang W., Fileta J., Guo Y. et al. (2006) Downregulation of Thy1 in retinal ganglion cells in experimental glaucoma. Curr. Eye Res. 31, 265 271.
18. Ikeda Y., Miura T., Sakamoto J. et al. (2006) Activation of ERK and suppression of calcineurin are interacting mechanisms of cardioprotection afforded by delta-opioid receptor activation. Basic Res. Cardiol. 101, 418 426.
19. Kaur C., Sivakumar V. Foulds W. S. (2006) Early response of neurons and glial cells to hypoxia in the retina. Invest. Ophthalmol. Vis. Sci. 47, 1126 1141.
20. Lam T. T., Takahashi K. Tso M. O. (1994) The effects of naloxone on retinal ischemia in rats. J. Ocul. Pharmacol. 10, 481 492.
21. Leske M. C., Heijl A., Hussein M. et al. (2003) Factors for glaucoma progression and the effect of treatment: the early manifest glaucoma trial. Arch. Ophthalmol. 121, 48 56.
22. Luo J. M., Cen L. P., Zhang X. M. et al. (2007) PI3K/akt, JAK/STAT and MEK/ERK pathway inhibition protects retinal ganglion cells via different mechanisms after optic nerve injury. Eur. J. Neurosci. 26, 828 842.
23. Ma M. C., Qian H., Ghassemi F. et al. (2005) Oxygen sensitive δ-opioid receptor-regulated survival and death signals: novel insights into neuronal preconditioning and protection. J. Biol. Chem. 280, 16208 16218.
24. Mayfield K. P., Horvath R., Lai J. et al. (1995) Increased expression of opioid delta receptors by deoxy conformation heme proteins in NG108-15 cells. Brain Res. 676, 358 362.
25. Merighi S., Benini A., Mirandola P. et al. (2006) Adenosine modulates vascular endothelial growth factor expression via hypoxia-inducible factor-1 in human glioblastoma cells. Biochem. Pharmacol. 72, 19 31.
26. Milano G., Corno A. F., Lippa S. et al. (2002) Chronic and intermittent hypoxia induce different degrees of myocardial tolerance to hypoxia-induced dysfunction. Exp. Biol. Med. (Maywood) 227, 389 397.
27. 2 production via NADH-derived superoxide. Am. J. Physiol. 270, H1044 H1053.
28. Mozaffarieh M., Grieshaber M. C. Flammer J. (2008) Oxygen and blood flow: players in the pathogenesis of glaucoma. Mol. Vis. 14, 224 233.
29. Narita M., Kuzumaki N., Miyatake M. et al. (2006) Role of delta-opioid receptor function in neurogenesis and neuroprotection. J. Neurochem. 97, 1494 1505.
30. Nash M. S. Osborne N. N. (1999) Assessment of Thy-1 mRNA levels as an index of retinal ganglion cell damage. Invest. Ophthalmol. Vis. Sci. 40, 1293 1298.
31. Ohira A., Tanito M., Kaidzu S. et al. (2003) Glutathione peroxidase induced in rat retinas to counteract photic injury. Invest. Ophthalmol. Vis. Sci. 44, 1230 1236.
32. Prabhakar N. R. (2001) Oxygen sensing during intermittent hypoxia: cellular and molecular mechanisms. J. Appl. Physiol. 90, 1986 1994.
33. Renshaw G. M. Dyson S. E. (1999) Increased nitric oxide synthase in the vasculature of the epaulette shark brain following hypoxia. Neuroreport 10, 1707 1712.
34. Renshaw G. M. C. Nikinmaa M. (2007) Oxygen sensors of the peripheral and central nervous system, in Handbook of Neurochemistry and Molecular Neurobiology (Lajtha A. Johnson D. A., eds pp. 272 288. Springer, New York.
35. Riazi-Esfahani M., Kiumehr S., Asadi-Amoli F. et al. (2008) Morphine pretreatment provides histologic protection against ischemia-reperfusion injury in rabbit retina. Retina 28, 511 517.
36. Roth S., Shaikh A. R., Hennelly M. M. et al. (2003) Mitogen-activated protein kinases and retinal ischemia. Invest. Ophthalmol. Vis. Sci. 44, 5383 5395.
37. Sellés-Navarro I., Villegas-Pérez M. P., Salvador-Silva M. et al. (1996) Retinal ganglion cell death after different transient periods of pressure-induced ischemia and survival intervals. A quantitative in vivo study. Invest. Ophthalmol. Vis. Sci. 37, 2002 2014.
38. Semenza G. L. (2000) HIF-1: mediator of physiological and pathophysiological responses to hypoxia. J. Appl. Physiol. 88, 1474 1480.
39. Stroka D. M., Burkhardt T., Desbaillets I. et al. (2001) HIF-1 is expressed in normoxic tissue and displays an organ specific regulation under systemic hypoxia. FASEB J. 15, 2445 2453.
40. Tanito M., Yoshida Y., Kaidzu S. et al. (2006) Detection of lipid peroxidation in light-exposed mouse retina assessed by oxidative stress markers, total hydroxyoctadecadienoic acid and 8-iso-prostaglandin F2alpha. Neurosci. Lett. 398, 63 68.
41. Tezel G. (2006) Oxidative stress in glaucomatous neurodegeneration: mechanisms and consequences. Prog. Retin. Eye Res. 25, 490 513.
42. Vidal-Sanz M., Lafuente M., Sobrado-Calvo P. et al. (2002) Death and neuroprotection of retinal ganglion cells after different types of injury. Neurotox. Res. 2, 215 227.
43. Voigt T. Wässle H. (1987) Dopaminergic innervation of A II amacrine cells in mammalian retina. J. Neurosci. 7, 4115 4128.
44. Wallace D. R., Dodson S. L., Nath A. et al. (2006) Delta opioid agonists attenuate TAT(1-72)-induced oxidative stress in SK-N-SH cells. Neurotoxicology 27, 101 107.
45. Wamsley J. K., Palacios J. M. Kuhar M. J. (1981) Autoradiographic localization of opioid receptors in the mammalian retina. Neurosci. Lett. 27, 19 24.
46. Wilkinson K. D., Lee K. M., Deshpande S. et al. (1989) The neuron-specific protein PGP 9.5 is a ubiquitin carboxyl-terminal hydrolase. Science 246, 670 673.
47. Williams A. F. Gagnon J. (1982) Neuronal cell Thy-1 glycoprotein: homology with immunoglobulin. Science 216, 696 703.
48. Yang C. C., Ma M. C., Chien C. T. et al. (2007) Hypoxic preconditioning attenuates endotoxin-induced oxidative stress in rat kidneys. J. Physiol. 582, 407 419.
49. Zhou Y., Pernet V., Hauswirth W. W. et al. (2005) Activation of the extracellular signal-regulated kinase 1/2 pathway by AAV gene transfer protects retinal ganglion cells in glaucoma. Mol. Ther. 12, 402 412.
50. Zhu Y., Zhang Y., Ojwang B. A. et al. (2007) Long-term tolerance to retinal ischemia by repetitive hypoxic preconditioning: role of HIF-1alpha and heme oxygenase-1. Invest. Ophthalmol. Vis. Sci. 48, 1735 1743.
51. Zou A. P., Li N. Cowley A. W. Jr. (2001) Production and actions of superoxide in the renal medulla. Hypertension 37, 547 553.