DOI QR코드

DOI QR Code

Tat-indoleamine 2,3-dioxygenase 1 elicits neuroprotective effects on ischemic injury

  • Park, Jung Hwan (Department of Biomedical Science and Research Institute of Bioscience and Biotechnology, Hallym University) ;
  • Kim, Dae Won (Department of Biochemistry and Molecular Biology, Research Institute of Oral Sciences, College of Dentistry, Gangneung-Wonju National University) ;
  • Shin, Min Jea (Department of Biomedical Science and Research Institute of Bioscience and Biotechnology, Hallym University) ;
  • Park, Jinseu (Department of Biomedical Science and Research Institute of Bioscience and Biotechnology, Hallym University) ;
  • Han, Kyu Hyung (Department of Biomedical Science and Research Institute of Bioscience and Biotechnology, Hallym University) ;
  • Lee, Keun Wook (Department of Biomedical Science and Research Institute of Bioscience and Biotechnology, Hallym University) ;
  • Park, Jong Kook (Department of Biomedical Science and Research Institute of Bioscience and Biotechnology, Hallym University) ;
  • Choi, Yeon Joo (Department of Biomedical Science and Research Institute of Bioscience and Biotechnology, Hallym University) ;
  • Yeo, Hyeon Ji (Department of Biomedical Science and Research Institute of Bioscience and Biotechnology, Hallym University) ;
  • Yeo, Eun Ji (Department of Biomedical Science and Research Institute of Bioscience and Biotechnology, Hallym University) ;
  • Sohn, Eun Jeong (Department of Biomedical Science and Research Institute of Bioscience and Biotechnology, Hallym University) ;
  • Kim, Hyoung-Chun (Neuropsychopharmacology and Toxicology Program, BK21 PLUS Project, College of Pharmacy, Kangwon National University) ;
  • Shin, Eun-Joo (Neuropsychopharmacology and Toxicology Program, BK21 PLUS Project, College of Pharmacy, Kangwon National University) ;
  • Cho, Sung-Woo (Department of Biochemistry and Molecular Biology, University of Ulsan College of Medicine) ;
  • Kim, Duk-Soo (Department of Anatomy and BK21 Plus Center, College of Medicine, Soonchunhyang University) ;
  • Cho, Yong-Jun (Department of Neurosurgery, Hallym University Medical Center) ;
  • Eum, Won Sik (Department of Biomedical Science and Research Institute of Bioscience and Biotechnology, Hallym University) ;
  • Choi, Soo Young (Department of Biomedical Science and Research Institute of Bioscience and Biotechnology, Hallym University)
  • Received : 2020.05.28
  • Accepted : 2020.06.30
  • Published : 2020.11.30

Abstract

It is well known that oxidative stress participates in neuronal cell death caused production of reactive oxygen species (ROS). The increased ROS is a major contributor to the development of ischemic injury. Indoleamine 2,3-dioxygenase 1 (IDO-1) is involved in the kynurenine pathway in tryptophan metabolism and plays a role as an anti-oxidant. However, whether IDO-1 would inhibit hippocampal cell death is poorly known. Therefore, we explored the effects of cell permeable Tat-IDO-1 protein against oxidative stress-induced HT-22 cells and in a cerebral ischemia/reperfusion injury model. Transduced Tat-IDO-1 reduced cell death, ROS production, and DNA fragmentation and inhibited mitogen-activated protein kinases (MAPKs) activation in H2O2 exposed HT-22 cells. In the cerebral ischemia/reperfusion injury model, Tat-IDO-1 transduced into the brain and passing by means of the blood-brain barrier (BBB) significantly prevented hippocampal neuronal cell death. These results suggest that Tat-IDO-1 may present an alternative strategy to improve from the ischemic injury.

Keywords

References

  1. Tas SW, Vervoordeldonk MJ, Hajji N et al (2007) Noncanonical NF-kappaB signaling in dendritic cells is required for indoleamine 2,3-dioxygenase (IDO) induction and immune regulation. Blood 1, 1540-1549
  2. Uyttenhove C, Pilotte L, Theate I et al (2003) Evidence for a tumoral immune resistance mechanism based on tryptophan degradation by indoleamine 2,3-dioxygenase. Nat Med 9, 1269-1274 https://doi.org/10.1038/nm934
  3. Wang XF, Wang HS, Wang H et al (2014) The role of indoleamine 2,3-dioxygenase (IDO) in immune tolerance: focus on macrophage polarization of THP-1 cells. Cell Immunol 289, 42-48 https://doi.org/10.1016/j.cellimm.2014.02.005
  4. Hirata F, Ohnishi T and Hayaish O (1977) Intracellular utilization of superoxide anion by indoleamine 2,3-dioxygenase of rabbit enterocytes. J Biol Chem 252, 2774-1776 https://doi.org/10.1016/S0021-9258(17)40524-2
  5. Chen Y and Guillemin GJ (2009) Kynurenine pathway metabolites in humans: Disease and healthy states. Int J Tryptophan Res 2, 1-19
  6. Lugo-Huitron R, Blanco-Ayala T, Ugalde-Muniz P et al (2011) On the antioxidant properties of kynurenic acid: free radical scavenging activity and inhibition of oxidative stress. Neurotoxicol Teratol 33, 538-547 https://doi.org/10.1016/j.ntt.2011.07.002
  7. Takikawa O (2005) Biochemical and medical aspects of the indoleamine 2,3-dioxygenase-initiated L-tryptophan metabolism. Biochem Biophys Res Commun 338, 12-19 https://doi.org/10.1016/j.bbrc.2005.09.032
  8. Liu H, Liu L and Visner GA (2007) Nonviral gene delivery with indoleamine 2,3-dioxygenase targeting pulmonary endothelium protects against ischemia-reperfusion injury. Am J Transplant 10, 2291-2300
  9. Yun TJ, Lee JS, Machmach K et al (2016) Indoleamine 2,3-dioxygenase-expressing aortic plasmacytoid dendritic cells protect against atherosclerosis by induction of regulatory T cells. Cell Metab 23, 852-866 https://doi.org/10.1016/j.cmet.2016.04.010
  10. Chen X, Guo C and Kong J (2012) Oxidative stress in neurodegenerative diseases. Neural Regen Res 7, 376-385 https://doi.org/10.3969/j.issn.1673-5374.2012.05.009
  11. Kim GH, Kim JE, Rhie SJ and Yoon S (2015) The role of oxidative stress in neurodegenerative diseases. Exp Neurobiol 24, 325-340 https://doi.org/10.5607/en.2015.24.4.325
  12. Ashafaq M, Raza SS, Khan MM et al (2012) Catechin hydrate ameliorates redox imbalance and limits inflammatory response in focal cerebral ischemia. Neurochem Res 37, 1747-1760 https://doi.org/10.1007/s11064-012-0786-1
  13. Lei C, Deng J, Wang B et al (2011) Reactive oxygen species scavenger inhibits STAT3 activation after transient focal cerebral ischemia-reperfusion injury in rats. Anesth Analg 113, 153-159 https://doi.org/10.1213/ane.0b013e31821a9fbe
  14. Jeong HJ, Yoo DY, Kim DW et al (2014) Neuroprotective effect of PEP-1-peroxiredoxin2 on CA1 regions in the hippocampus against ischemic insult. Biochim Biophys Acta 1840, 2321-2330 https://doi.org/10.1016/j.bbagen.2014.03.003
  15. Kim SM, Hwang IK, Yoo DY et al (2015) Tat-antioxidant 1 protects against stress-induced hippocampal TH-22 cell death and ischemic insult in animal model. J Cell Mol Med 19, 1333-1345 https://doi.org/10.1111/jcmm.12513
  16. Cheng J, Wang F, Yu DF, Wu PF and Chen JG (2011) The cytotoxic mechanism of malondialdehyde and protective effect of carnosine via protein cross-linking/ mitochondrial dysfunction/reactive oxygen species/MAPK pathway in neurons. Eur J Pharmacol 650, 184-194 https://doi.org/10.1016/j.ejphar.2010.09.033
  17. Dhanasekaran DN and Reddy EP (2008) JNK signaling in apoptosis. Oncogene 27, 6245-6251 https://doi.org/10.1038/onc.2008.301
  18. Kim SD, Moon CK, Eun SY, Ryu PD and Jo SA (2005) Identification of ASK1, MKK4, JNK, c-Jun, and caspase-3 as a signaling cascade involved in cadmium-induced neuronal cell apoptosis. Biochem Biophys Res Commun 328, 326-334 https://doi.org/10.1016/j.bbrc.2004.11.173
  19. Ouyang M and Shen X (2006) Critical role of ASK1 in the 6-hydroxydopamine-induced apoptosis in human neuroblastoma SH-SY5Y cells. J Neurochem 97, 234-244 https://doi.org/10.1111/j.1471-4159.2006.03730.x
  20. Wadia JS and Dowdy SF (2002) Protein transduction technology. Curr Opin Biotechnol 13, 52-56 https://doi.org/10.1016/S0958-1669(02)00284-7
  21. Cerrato CP, Pirisinu M, Vlachos EN and Langel U (2015) Novel cell-penetrating peptide targeting mitochondria. FASEB J 29, 4589-4599 https://doi.org/10.1096/fj.14-269225
  22. Jo HS, Yeo EJ, Shin MJ et al (2017) Tat-DJ-1 enhances cell survival by inhibition of oxidative stress, NF-𝜅B and MAPK activation in HepG2 cells. Biotechnol Lett 39, 511-521 https://doi.org/10.1007/s10529-017-2286-5
  23. Kim MJ, Park M, Kim DW et al (2015) Transduced PEP-1-PON1 proteins regulate microglial activation and dopaminergic neuronal death in a Parkinson's disease model. Biomaterials 64, 45-56 https://doi.org/10.1016/j.biomaterials.2015.06.015
  24. Gellert L, Fuzik J, Goblos A et al (2011) Neuroprotection with a new kynurenic acid analog in the four-vessel occlusion model of ischemia. Eur J Pharmacol 667, 182-187 https://doi.org/10.1016/j.ejphar.2011.05.069
  25. Lovelace MD, Varney B, Sundaram G et al (2017) Recent evidence for an expanded role of the kynurenine pathway of tryptophan metabolism in neurological diseases. Neuropharmacol 112, 373-388 https://doi.org/10.1016/j.neuropharm.2016.03.024
  26. Duleu S, Mangas A, Sevin F, Veyret B, Bessede A and Geffard M (2010) Circulating antibodies to IDO/THO pathway metabolites in Alzheimer's disease. Int J Alzheimers Dis 2010, 6
  27. Hu P, Hunt NH, Arfuso F et al (2017) Increased indoleamine 2,3-dioxygenase and quinolinic acid expression in microglia and muller cells of diabetic human and rodent retina. Invest Ophthalmol Vis Sci 58, 5043-5055 https://doi.org/10.1167/iovs.17-21654
  28. Taniguchi T, Sono M, Hirata F et al (1979) Indoleamine 2,3-dioxygenase. Kinetic studies on the binding of superoxide anion and molecular oxygen to enzyme. J Biol Chem 254, 3288-3294 https://doi.org/10.1016/S0021-9258(18)50757-2
  29. Sun Y (1989) Indoleamine 2,3-dioxygenase-a new antioxidant enzyme. Mater Med Pol 21, 244-250
  30. Freewan M, Rees MD, Plaza TS et al (2013). Human indoleamine 2,3-dioxygenase is a catalyst of physiological heme peroxidase reactions: implications for the inhibition of dioxygenase activity by hydrogen peroxide. J Biol Chem 288, 1548-1567 https://doi.org/10.1074/jbc.M112.410993
  31. Ramsey JD and Flynn NH (2015) Cell-penetrating peptides transport therapeutics into cells. Pharmacol Ther 54, 78-86 https://doi.org/10.1016/j.pharmthera.2015.07.003
  32. Moon JI, Han MJ, Yu SH et al (2019) Enhanced delivery of protein fused to cell penetrating peptides to mammalian cells. BMB Rep 52, 324-329 https://doi.org/10.5483/bmbrep.2019.52.5.195
  33. Zhang X, Li Y, Cheng Y et al (2015) Tat PTD-endostatin: A novel anti-angiogenesis protein with ocular barrier permeability via eye-drops. Biochim Biophys Acta 1850, 1140-1149 https://doi.org/10.1016/j.bbagen.2015.01.019
  34. Shin MJ, Kim DW, Lee YP et al (2014) Tat-glyoxalase protein inhibits against ischemic neuronal cell damage and ameliorates ischemic injury. Free Radic Biol Med 67, 195-210 https://doi.org/10.1016/j.freeradbiomed.2013.10.815
  35. Yeo HJ, Shin MJ, Yeo EJ et al (2019) Tat-CIAPIN1 inhibits hippocampal neuronal cell damage through the MAPK and apoptotic signaling pathways. Free Radic Biol Med 135, 68-78 https://doi.org/10.1016/j.freeradbiomed.2019.02.028
  36. Nakashima M, Niwa M, Iwai T and Uematsu T (1999) Involvement of free radicals in cerebral vascular reperfusion injury evaluated in a transient focal cerebral ischemia model of rat. Free Radic Biol Med 26, 722-729 https://doi.org/10.1016/S0891-5849(98)00257-3
  37. Taguchi A, Hara A, Saito K et al (2008) Localization and spatiotemporal expression of IDO following transient forebrain ischemia in gerbils. Brain Res 1217, 78-85 https://doi.org/10.1016/j.brainres.2008.02.067
  38. Liang K, Ye Y, Wang Y, Zhang J and Li C (2014) Formononetin mediates neuroprotection against cerebral ischemia/reperfusion in rats via downregulation of the Bax/Bcl-2 ratio and upregulation PI3K/Akt signaling pathway. J Neurol Sci 344, 100-104 https://doi.org/10.1016/j.jns.2014.06.033
  39. Zhang X, Shan P, Otterbein LE et al (2002) 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 https://doi.org/10.1074/jbc.M208419200
  40. Ferrer I, Lopez E, Blanco R et al (1998) Bcl-2, Bax, and Bcl-x expression in the CA1 area of the hippocampus following transient forebrain ischemia in the adult gerbil. Exp Brain Res 121, 167-173 https://doi.org/10.1007/s002210050448
  41. Zhu N, Cai C, Zhou A, Zhao X, Xiang Y and Zeng C (2017) Schisandrin B prevents hind limb from ischemiareperfusion-induced oxidative stress and inflammation via MAPK/NF-kappaB pathways in Rats. Biomed Res Int 2017, 4237973
  42. Kwon SH, Hong SI, Kim JA et al (2011) The neuro-protective effects of Lonicera japonica THUNB. against hydrogen peroxide-induced apoptosis via phosphorylation of MAPKs and PI3K/Akt in SH-SY5Y cells. Food Chem Toxicol 49, 1011-1019 https://doi.org/10.1016/j.fct.2011.01.008
  43. Jia L, Chen Y, Tian YH and Zhang G (2018) MAPK pathway mediates the anti-oxidative effect of chicoric acid against cerebral ischemia-reperfusion injury in vivo. Exp Ther Med 15, 1640-1646
  44. Guillemin GJ, Smythe G, Takikawa O and Brew BJ (2005) Expression of indoleamine 2,3-dioxygenase and production of quinolinic acid by human microglia, astrocytes, and neurons. Glia 49, 15-23 https://doi.org/10.1002/glia.20090
  45. Grant RS, Naif H, Espinosa M and Kapoor V (2000) IDO induction in IFN-gamma activated astroglia: a role in improving cell viability during oxidative stress. Redox Rep 5, 101-104 https://doi.org/10.1179/135100000101535357
  46. Sugawara T, Lewen A, Noshita N, Gasche Y and Chan PH (2002) Effects of global ischemia duration on neuronal, astroglial, oligodendroglial, and microglial reactions in the vulnerable hippocampal CA1 subregion in rats. J Neurotrauma 19, 85-98 https://doi.org/10.1089/089771502753460268
  47. Chu K, Yin B, Wang J et al (2012) Inhibition of P2X7 receptor ameliorates transient global cerebral ischemia/reperfusion injury via modulating inflammatory responses in the rat hippocampus. J Neuroinflam 9, 69
  48. Morizawa YM, Hirayama Y, Ohno N et al (2017) Reactive astrocytes function as phagocytes after brain ischemia via ABCA1-mediated pathway. Nat Commun 8, 28 https://doi.org/10.1038/s41467-017-00037-1
  49. Annunziato L, Boscia F and Pignataro G (2013) Ionic transporter activity in astrocytes, microglia, and oligodendrocytes during brain ischemia. J Cereb Blood Flow Metab 33, 969-982 https://doi.org/10.1038/jcbfm.2013.44