Postconditioning with Inhaled Carbon Monoxide Counteracts Apoptosis and Neuroinflammation in the Ischemic Rat Retina

PLoS ONE

Volumn 7, Issue 9, 2012, Pages

  Schallner, Nils ^a   Fuchs, Matthias ^a   Schwer, Christian I ^a   Loop, Torsten ^a   Buerkle, Hartmut ^a   Lagrèze, Wolf Alexander ^a   van Oterendorp, Christian ^a   Biermann, Julia ^a   Goebel, Ulrich ^a  

^a UNIVERSITY OF FREIBURG   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

CARBON MONOXIDE; CASPASE 3; HEME OXYGENASE 1; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE P38; PROTEIN BAX; PROTEIN BCL 2;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIINFLAMMATORY ACTIVITY; APOPTOSIS; ARTICLE; CELL MIGRATION; CELL PROTECTION; CONTROLLED STUDY; ENZYME INHIBITION; ENZYME PHOSPHORYLATION; FEMALE; ISCHEMIC POSTCONDITIONING; MACROPHAGE; MALE; MICROGLIA; MUELLER CELL; NERVOUS SYSTEM INFLAMMATION; NEUROPROTECTION; NONHUMAN; PROTEIN EXPRESSION; RAT; REPERFUSION INJURY; RETINA GANGLION CELL; RETINA ISCHEMIA;

ADMINISTRATION, INHALATION; ANIMALS; ANTI-INFLAMMATORY AGENTS; APOPTOSIS; BCL-2-ASSOCIATED X PROTEIN; CARBON MONOXIDE; CASPASE 3; CELL MOVEMENT; ENZYME ACTIVATION; FEMALE; GENE EXPRESSION; HEME OXYGENASE-1; ISCHEMIA; MALE; MITOGEN-ACTIVATED PROTEIN KINASES; NEUROGLIA; NEUROPROTECTIVE AGENTS; NF-KAPPA B; PHOSPHORYLATION; PROTEIN PROCESSING, POST-TRANSLATIONAL; PROTO-ONCOGENE PROTEINS C-BCL-2; RATS; RATS, SPRAGUE-DAWLEY; REPERFUSION INJURY; RETINA; RETINAL GANGLION CELLS; RETINAL VESSELS; RETINITIS;

RATTUS;

EID: 84867011823     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0046479     Document Type: Article

References (49)

1. Wong GY, Warner DO, Schroeder DR, Offord KP, Warner MA, et al. (2000) Risk of surgery and anesthesia for ischemic stroke. Anesthesiology 92: 425-432.
2. Mashour GA, Shanks AM, Kheterpal S, (2011) Perioperative stroke and associated mortality after noncardiac, nonneurologic surgery. Anesthesiology 114: 1289-1296.
3. O'Collins VE, Macleod MR, Donnan GA, Horky LL, van der Worp BH, et al. (2006) 1,026 experimental treatments in acute stroke. Ann Neurol 59: 467-477.
4. Otterbein LE, Bach FH, Alam J, Soares M, Tao Lu H, et al. (2000) Carbon monoxide has anti-inflammatory effects involving the mitogen-activated protein kinase pathway. Nat Med 6: 422-428.
5. Zhang X, Shan P, Otterbein LE, Alam J, Flavell RA, et al. (2003) Carbon monoxide inhibition of apoptosis during ischemia-reperfusion lung injury is dependent on the p38 mitogen-activated protein kinase pathway and involves caspase 3. J Biol Chem 278: 1248-1258.
6. Goebel U, Siepe M, Mecklenburg A, Stein P, Roesslein M, et al. (2008) Carbon monoxide inhalation reduces pulmonary inflammatory response during cardiopulmonary bypass in pigs. Anesthesiology 108: 1025-1036.
7. Vieira HL, Queiroga CS, Alves PM, (2008) Pre-conditioning induced by carbon monoxide provides neuronal protection against apoptosis. J Neurochem 107: 375-384.
8. Biermann J, Lagreze WA, Dimitriu C, Stoykow C, Goebel U, (2010) Preconditioning with inhalative carbon monoxide protects rat retinal ganglion cells from ischemia/reperfusion injury. Invest Ophthalmol Vis Sci 51: 3784-3791.
9. Zuckerbraun BS, Chin BY, Bilban M, d'Avila JC, Rao J, et al. (2007) Carbon monoxide signals via inhibition of cytochrome c oxidase and generation of mitochondrial reactive oxygen species. Faseb J 21: 1099-1106.
10. Otterbein LE, Otterbein SL, Ifedigbo E, Liu F, Morse DE, et al. (2003) MKK3 mitogen-activated protein kinase pathway mediates carbon monoxide-induced protection against oxidant-induced lung injury. Am J Pathol 163: 2555-2563.
11. Morse D, Pischke SE, Zhou Z, Davis RJ, Flavell RA, et al. (2003) Suppression of inflammatory cytokine production by carbon monoxide involves the JNK pathway and AP-1. J Biol Chem 278: 36993-36998.
12. Goebel U, Mecklenburg A, Siepe M, Roesslein M, Schwer CI, et al. (2009) Protective effects of inhaled carbon monoxide in pig lungs during cardiopulmonary bypass are mediated via an induction of the heat shock response. Br J Anaesth 103: 173-184.
13. Zeynalov E, Dore S, (2009) Low doses of carbon monoxide protect against experimental focal brain ischemia. Neurotox Res 15: 133-137.
14. Kamphuis W, Dijk F, van Soest S, Bergen AA, (2007) Global gene expression profiling of ischemic preconditioning in the rat retina. Mol Vis 13: 1020-1030.
15. Li SY, Fu ZJ, Ma H, Jang WC, So KF, et al. (2009) Effect of lutein on retinal neurons and oxidative stress in a model of acute retinal ischemia/reperfusion. Invest Ophthalmol Vis Sci 50: 836-843.
16. Wang L, Li C, Guo H, Kern TS, Huang K, et al. (2011) Curcumin inhibits neuronal and vascular degeneration in retina after ischemia and reperfusion injury. PLoS One 6: e23194.
17. Jehle T, Wingert K, Dimitriu C, Meschede W, Lasseck J, et al. (2008) Quantification of ischemic damage in the rat retina: a comparative study using evoked potentials, electroretinography, and histology. Invest Ophthalmol Vis Sci 49: 1056-1064.
18. Fischer D, Pavlidis M, Thanos S, (2000) Cataractogenic lens injury prevents traumatic ganglion cell death and promotes axonal regeneration both in vivo and in culture. Invest Ophthalmol Vis Sci 41: 3943-3954.
19. Villegas-Perez MP, Vidal-Sanz M, Bray GM, Aguayo AJ, (1988) Influences of peripheral nerve grafts on the survival and regrowth of axotomized retinal ganglion cells in adult rats. J Neurosci 8: 265-280.
20. Danias J, Shen F, Goldblum D, Chen B, Ramos-Esteban J, et al. (2002) Cytoarchitecture of the retinal ganglion cells in the rat. Invest Ophthalmol Vis Sci 43: 587-594.
21. Weber J, Remonda L, Mattle HP, Koerner U, Baumgartner RW, et al. (1998) Selective intra-arterial fibrinolysis of acute central retinal artery occlusion. Stroke 29: 2076-2079.
22. Jaissle GB, Szurman P, Feltgen N, Spitzer B, Pielen A, et al. (2011) Predictive factors for functional improvement after intravitreal bevacizumab therapy for macular edema due to branch retinal vein occlusion. Graefes Arch Clin Exp Ophthalmol 249: 183-192.
23. Goebel U, Siepe M, Schwer CI, Schibilsky D, Brehm K, et al. (2011) Postconditioning of the lungs with inhaled carbon monoxide after cardiopulmonary bypass in pigs. Anesth Analg 112: 282-291.
24. Zhang X, Shan P, Alam J, Davis RJ, Flavell RA, et al. (2003) Carbon monoxide modulates Fas/Fas ligand, caspases, and Bcl-2 family proteins via the p38alpha mitogen-activated protein kinase pathway during ischemia-reperfusion lung injury. J Biol Chem 278: 22061-22070.
25. Kim HP, Wang X, Zhang J, Suh GY, Benjamin IJ, et al. (2005) Heat shock protein-70 mediates the cytoprotective effect of carbon monoxide: involvement of p38 beta MAPK and heat shock factor-1. J Immunol 175: 2622-2629.
26. Bani-Hani MG, Greenstein D, Mann BE, Green CJ, Motterlini R, (2006) Modulation of thrombin-induced neuroinflammation in BV-2 microglia by carbon monoxide-releasing molecule 3. J Pharmacol Exp Ther 318: 1315-1322.
27. De Backer O, Elinck E, Blanckaert B, Leybaert L, Motterlini R, et al. (2009) Water-soluble CO-releasing molecules reduce the development of postoperative ileus via modulation of MAPK/HO-1 signalling and reduction of oxidative stress. Gut 58: 347-356.
28. Guo YL, Kang B, Han J, Williamson JR, (2001) p38beta MAP kinase protects rat mesangial cells from TNF-alpha-induced apoptosis. J Cell Biochem 82: 556-565.
29. Schallner N, Schwemmers S, Schwer CI, Froehlich C, Stoll P, et al. (2011) p38beta-regulated induction of the heat shock response by carbon monoxide releasing molecule CORM-2 mediates cytoprotection in lung cells in vitro. Eur J Pharmacol 670: 58-66.
30. Marra C, Gomes Moret D, de Souza Correa A, Chagas da Silva F, Moraes P, et al. (2011) Protein kinases JAK and ERK mediate protective effect of interleukin-2 upon ganglion cells of the developing rat retina. J Neuroimmunol 233: 120-126.
31. Nakanishi Y, Nakamura M, Mukuno H, Kanamori A, Seigel GM, et al. (2006) Latanoprost rescues retinal neuro-glial cells from apoptosis by inhibiting caspase-3, which is mediated by p44/p42 mitogen-activated protein kinase. Exp Eye Res 83: 1108-1117.
32. Applegate LA, Luscher P, Tyrrell RM, (1991) Induction of heme oxygenase: a general response to oxidant stress in cultured mammalian cells. Cancer Res 51: 974-978.
33. Dvoriantchikova G, Barakat D, Brambilla R, Agudelo C, Hernandez E, et al. (2009) Inactivation of astroglial NF-kappa B promotes survival of retinal neurons following ischemic injury. Eur J Neurosci 30: 175-185.
34. Williams AJ, Wei HH, Dave JR, Tortella FC, (2007) Acute and delayed neuroinflammatory response following experimental penetrating ballistic brain injury in the rat. J Neuroinflammation 4: 17.
35. Ganesh BS, Chintala SK, (2011) Inhibition of reactive gliosis attenuates excitotoxicity-mediated death of retinal ganglion cells. PLoS One 6: e18305.
36. Li SY, Yang D, Yeung CM, Yu WY, Chang RC, et al. (2011) Lycium barbarum polysaccharides reduce neuronal damage, blood-retinal barrier disruption and oxidative stress in retinal ischemia/reperfusion injury. PLoS One 6: e16380.
37. Neumann H, Kotter MR, Franklin RJ, (2009) Debris clearance by microglia: an essential link between degeneration and regeneration. Brain 132: 288-295.
38. Geller SF, Lewis GP, Anderson DH, Fisher SK, (1995) Use of the MIB-1 antibody for detecting proliferating cells in the retina. Invest Ophthalmol Vis Sci 36: 737-744.
39. Lewis G, Mervin K, Valter K, Maslim J, Kappel PJ, et al. (1999) Limiting the proliferation and reactivity of retinal Muller cells during experimental retinal detachment: the value of oxygen supplementation. Am J Ophthalmol 128: 165-172.
40. Zeiss CJ, Johnson EA, (2004) Proliferation of microglia, but not photoreceptors, in the outer nuclear layer of the rd-1 mouse. Invest Ophthalmol Vis Sci 45: 971-976.
41. Kohno H, Sakai T, Kitahara K, (2006) Induction of nestin, Ki-67, and cyclin D1 expression in Muller cells after laser injury in adult rat retina. Graefes Arch Clin Exp Ophthalmol 244: 90-95.
42. Wohl SG, Schmeer CW, Witte OW, Isenmann S, (2010) Proliferative response of microglia and macrophages in the adult mouse eye after optic nerve lesion. Invest Ophthalmol Vis Sci 51: 2686-2696.
43. Kee N, Sivalingam S, Boonstra R, Wojtowicz JM, (2002) The utility of Ki-67 and BrdU as proliferative markers of adult neurogenesis. J Neurosci 115: 97-105.
44. Naskar R, Wissing M, Thanos S, (2002) Detection of early neuron degeneration and accompanying microglial responses in the retina of a rat model of glaucoma. Invest Ophthalmol Vis Sci 43: 2962-2968.
45. Kaneko H, Nishiguchi KM, Nakamura M, Kachi S, Terasaki H, (2008) Characteristics of bone marrow-derived microglia in the normal and injured retina. Invest Ophthalmol Vis Sci 49: 4162-4168.
46. Yabluchanskiy A, Sawle P, Homer-Vanniasinkam S, Green CJ, Foresti R, et al. (2012) CORM-3, a carbon monoxide-releasing molecule, alters the inflammatory response and reduces brain damage in a rat model of hemorrhagic stroke. Crit Care Med 40: 544-552.
47. Takeuchi A, Vesely A, Rucker J, Sommer LZ, Tesler J, et al. (2000) A simple "new" method to accelerate clearance of carbon monoxide. Am J Respir Crit Care Med 161: 1816-1819.
48. Mayr FB, Spiel A, Leitner J, Marsik C, Germann P, et al. (2005) Effects of carbon monoxide inhalation during experimental endotoxemia in humans. Am J Respir Crit Care Med 171: 354-360.
49. Graham BL, Mink JT, Cotton DJ, (2002) Effects of increasing carboxyhemoglobin on the single breath carbon monoxide diffusing capacity. Am J Respir Crit Care Med 165: 1504-1510.