DOI QR코드

DOI QR Code

Poly (ADP-ribose) in the pathogenesis of Parkinson's disease

  • Lee, Yunjong (Neuroregeneration and Stem Cell Programs, Institute for Cell Engineering, the Johns Hopkins University School of Medicine) ;
  • Kang, Ho Chul (Neuroregeneration and Stem Cell Programs, Institute for Cell Engineering, the Johns Hopkins University School of Medicine) ;
  • Lee, Byoung Dae (Neurodegeneration Control Research Center, Department of Neuroscience, Kyung Hee University) ;
  • Lee, Yun-Il (Well Aging Research Center, Samsung Advanced Institute of Technology (SAIT)) ;
  • Kim, Young Pil (Department of Bio-Engineering, Life Science RD Center, Sinil Pharmaceutical Co.) ;
  • Shin, Joo-Ho (Neuroregeneration and Stem Cell Programs, Institute for Cell Engineering, the Johns Hopkins University School of Medicine)
  • Received : 2014.05.27
  • Published : 2014.08.31

Abstract

The defining feature of Parkinson's disease is a progressive and selective demise of dopaminergic neurons. A recent report on Parkinson's disease animal model demonstrates that poly (ADP-ribose) (PAR) dependent cell death, also named parthanatos, is accountable for selective dopaminergic neuronal loss. Parthanatos is a programmed necrotic cell death, characterized by PARP1 activation, apoptosis inducing factor (AIF) nuclear translocation, and large scale DNA fragmentation. Besides cell death regulation via interaction with AIF, PAR molecule mediates diverse cellular processes including genomic stability, cell division, transcription, epigenetic regulation, and stress granule formation. In this review, we will discuss the roles of PARP1 activation and PAR molecules in the pathological processes of Parkinson's disease. Potential interaction between PAR molecule and Parkinson's disease protein interactome are briefly introduced. Finally, we suggest promising points of therapeutic intervention in the pathological PAR signaling cascade to halt progression in Parkinson's disease.

Keywords

References

  1. Lang, A. E. and Lozano, A. M. (1998) Parkinson's disease. Second of two parts. N. Engl. J. Med. 339, 1130-1143. https://doi.org/10.1056/NEJM199810153391607
  2. Lang, A. E. and Lozano, A. M. (1998) Parkinson's disease. First of two parts. N. Engl. J. Med. 339, 1044-1053. https://doi.org/10.1056/NEJM199810083391506
  3. Galluzzi, L., Aaronson, S. A., Abrams, J., Alnemri, E. S., Andrews, D. W., Baehrecke, E. H., Bazan, N. G., Blagosklonny, M. V., Blomgren, K., Borner, C., Bredesen, D. E., Brenner, C., Castedo, M., Cidlowski, J. A., Ciechanover, A., Cohen, G. M., De Laurenzi, V., De Maria, R., Deshmukh, M., Dynlacht, B. D., El-Deiry, W. S., Flavell, R. A., Fulda, S., Garrido, C., Golstein, P., Gougeon, M. L., Green, D. R., Gronemeyer, H., Hajnoczky, G., Hardwick, J. M., Hengartner, M. O., Ichijo, H., Jaattela, M., Kepp, O., Kimchi, A., Klionsky, D. J., Knight, R. A., Kornbluth, S., Kumar, S., Levine, B., Lipton, S. A., Lugli, E., Madeo, F., Malomi, W., Marine, J. C., Martin, S. J., Medema, J. P., Mehlen, P., Melino, G., Moll, U. M., Morselli, E., Nagata, S., Nicholson, D. W., Nicotera, P., Nunez, G., Oren, M., Penninger, J., Pervaiz, S., Peter, M. E., Piacentini, M., Prehn, J. H., Puthalakath, H., Rabinovich, G. A., Rizzuto, R., Rodrigues, C. M., Rubinsztein, D. C., Rudel, T., Scorrano, L., Simon, H. U., Steller, H., Tschopp, J., Tsujimoto, Y., Vandenabeele, P., Vitale, I., Vousden, K. H., Youle, R. J., Yuan, J., Zhivotovsky, B. and Kroemer, G. (2009) Guidelines for the use and interpretation of assays for monitoring cell death in higher eukaryotes. Cell Death. Differ. 16, 1093-1107. https://doi.org/10.1038/cdd.2009.44
  4. Schreiber, V., Dantzer, F., Ame, J. C. and de Murcia, G. (2006) Poly(ADP-ribose): novel functions for an old molecule. Nat. Rev. Mol. Cell Biol. 7, 517-528. https://doi.org/10.1038/nrm1963
  5. Szabo, C. and Dawson, V. L. (1998) Role of poly(ADP-ribose) synthetase in inflammation and ischaemia-reperfusion. Trends. Pharmacol. Sci. 19, 287-298. https://doi.org/10.1016/S0165-6147(98)01193-6
  6. Wang, H., Shimoji, M., Yu, S. W., Dawson, T. M. and Dawson, V. L. (2003) Apoptosis inducing factor and PARP-mediated injury in the MPTP mouse model of Parkinson's disease. Ann. N. Y. Acad. Sci. 991, 132-139.
  7. Yu, S. W., Wang, H., Dawson, T. M. and Dawson, V. L. (2003) Poly(ADP-ribose) polymerase-1 and apoptosis inducing factor in neurotoxicity. Neurobiol. Dis. 14, 303-317. https://doi.org/10.1016/j.nbd.2003.08.008
  8. Strosznajder, J. B., Czapski, G. A., Adamczyk, A. and Strosznajder, R. P. (2012) Poly(ADP-ribose) polymerase-1 in amyloid beta toxicity and Alzheimer's disease. Mol. Neurobiol. 46, 78-84. https://doi.org/10.1007/s12035-012-8258-9
  9. Martire, S., Fuso, A., Rotili, D., Tempera, I., Giordano, C., De Zottis, I., Muzi, A., Vernole, P., Graziani, G., Lococo, E., Faraldi, M., Maras, B., Scarpa, S., Mosca, L. and d'Erme, M. (2013) PARP-1 modulates amyloid beta peptide- induced neuronal damage. PLoS One. 8, e72169. https://doi.org/10.1371/journal.pone.0072169
  10. Mashimo, M., Kato, J. and Moss, J. (2013) ADP-ribosyl-acceptor hydrolase 3 regulates poly (ADP-ribose) degradation and cell death during oxidative stress. Proc. Natl. Acad. Sci. U. S. A. 110, 18964-18969. https://doi.org/10.1073/pnas.1312783110
  11. Fatokun, A. A., Dawson, V. L. and Dawson, T. M. (2014) Parthanatos: mitochondrial-linked mechanisms and therapeutic opportunities. Br. J. Pharmacol. 171, 2000-2016. https://doi.org/10.1111/bph.12416
  12. Burkle, A. (2005) Poly(ADP-ribose). The most elaborate metabolite of NAD+. FEBS J. 272, 4576-4589. https://doi.org/10.1111/j.1742-4658.2005.04864.x
  13. Gagne, J. P., Rouleau, M. and Poirier, G. G. (2012) Structural biology. PARP-1 activation--bringing the pieces together. Science 336, 678-679. https://doi.org/10.1126/science.1221870
  14. Luo, X. and Kraus, W. L. (2012) On PAR with PARP: cellular stress signaling through poly(ADP-ribose) and PARP-1. Genes Dev. 26, 417-432. https://doi.org/10.1101/gad.183509.111
  15. Vyas, S., Chesarone-Cataldo, M., Todorova, T., Huang, Y. H. and Chang, P. (2013) A systematic analysis of the PARP protein family identifies new functions critical for cell physiology. Nat. Commun. 4, 2240.
  16. Gagne, J. P., Isabelle, M., Lo, K. S., Bourassa, S., Hendzel, M. J., Dawson, V. L., Dawson, T. M. and Poirier, G. G. (2008) Proteome-wide identification of poly(ADP-ribose) binding proteins and poly(ADP-ribose)-associated protein complexes. Nucleic Acids Res. 36, 6959-6976. https://doi.org/10.1093/nar/gkn771
  17. Gagne, J. P., Pic, E., Isabelle, M., Krietsch, J., Ethier, C., Paquet, E., Kelly, I., Boutin, M., Moon, K. M., Foster, L. J. and Poirier, G. G. (2012) Quantitative proteomics profiling of the poly(ADP-ribose)-related response to genotoxic stress. Nucleic Acids Res. 40, 7788-7805. https://doi.org/10.1093/nar/gks486
  18. Wang, Z., Michaud, G. A., Cheng, Z., Zhang, Y., Hinds, T. R., Fan, E., Cong, F. and Xu, W. (2012) Recognition of the iso-ADP-ribose moiety in poly(ADP-ribose) by WWE domains suggests a general mechanism for poly(ADP-ribosyl) ation-dependent ubiquitination. Genes. Dev. 26, 235-240. https://doi.org/10.1101/gad.182618.111
  19. Slade, D., Dunstan, M. S., Barkauskaite, E., Weston, R., Lafite, P., Dixon, N., Ahel, M., Leys, D. and Ahel, I. (2011) The structure and catalytic mechanism of a poly(ADP-ribose) glycohydrolase. Nature 477, 616-620. https://doi.org/10.1038/nature10404
  20. Kim, M. Y., Zhang, T. and Kraus, W. L. (2005) Poly(ADPribosyl) ation by PARP-1: 'PAR-laying' NAD+ into a nuclear signal. Genes. Dev. 19, 1951-1967. https://doi.org/10.1101/gad.1331805
  21. Menissier de Murcia, J., Ricoul, M., Tartier, L., Niedergang, C., Huber, A., Dantzer, F., Schreiber, V., Ame, J. C., Dierich, A., LeMeur, M., Sabatier, L., Chambon, P. and de Murcia, G. (2003) Functional interaction between PARP-1 and PARP-2 in chromosome stability and embryonic development in mouse. EMBO J. 22, 2255-2263. https://doi.org/10.1093/emboj/cdg206
  22. Cortes, U., Tong, W. M., Coyle, D. L., Meyer-Ficca, M. L., Meyer, R. G., Petrilli, V., Herceg, Z., Jacobson, E. L., Jacobson, M. K. and Wang, Z. Q. (2004) Depletion of the 110-kilodalton isoform of poly(ADP-ribose) glycohydrolase increases sensitivity to genotoxic and endotoxic stress in mice. Mol. Cell Biol. 24, 7163-7178. https://doi.org/10.1128/MCB.24.16.7163-7178.2004
  23. Herceg, Z. and Wang, Z. Q. (2001) Functions of poly(ADP-ribose) polymerase (PARP) in DNA repair, genomic integrity and cell death. Mutat. Res. 477, 97-110. https://doi.org/10.1016/S0027-5107(01)00111-7
  24. Virag, L. and Szabo, C. (2002) The therapeutic potential of poly(ADP-ribose) polymerase inhibitors. Pharmacol. Rev. 54, 375-429. https://doi.org/10.1124/pr.54.3.375
  25. Andrabi, S. A., Dawson, T. M. and Dawson, V. L. (2008) Mitochondrial and nuclear cross talk in cell death: parthanatos. Ann. N. Y. Acad. Sci. 1147, 233-241. https://doi.org/10.1196/annals.1427.014
  26. Lee, Y., Karuppagounder, S. S., Shin, J. H., Lee, Y. I., Ko, H. S., Swing, D., Jiang, H., Kang, S. U., Lee, B. D., Kang, H. C., Kim, D., Tessarollo, L., Dawson, V. L. and Dawson, T. M. (2013) Parthanatos mediates AIMP2-activated age-dependent dopaminergic neuronal loss. Nat. Neurosci. 16, 1392-1400. https://doi.org/10.1038/nn.3500
  27. Mandir, A. S., Przedborski, S., Jackson-Lewis, V., Wang, Z. Q., Simbulan-Rosenthal, C. M., Smulson, M. E., Hoffman, B. E., Guastella, D. B., Dawson, V. L. and Dawson, T. M. (1999) Poly(ADP-ribose) polymerase activation mediates 1-methyl-4-phenyl-1, 2,3,6-tetrahydropyridine (MPTP)-induced parkinsonism. Proc. Natl. Acad. Sci. U. S. A. 96, 5774-5779. https://doi.org/10.1073/pnas.96.10.5774
  28. Bai, P. and Canto, C. (2012) The role of PARP-1 and PARP-2 enzymes in metabolic regulation and disease. Cell Metab. 16, 290-295. https://doi.org/10.1016/j.cmet.2012.06.016
  29. Andrabi, S. A., Kim, N. S., Yu, S. W., Wang, H., Koh, D. W., Sasaki, M., Klaus, J. A., Otsuka, T., Zhang, Z., Koehler, R. C., Hurn, P. D., Poirier, G. G., Dawson, V. L. and Dawson, T. M. (2006) Poly(ADP-ribose) (PAR) polymer is a death signal. Proc. Natl. Acad. Sci. U. S. A. 103, 18308-18313. https://doi.org/10.1073/pnas.0606526103
  30. Hanai, S., Kanai, M., Ohashi, S., Okamoto, K., Yamada, M., Takahashi, H. and Miwa, M. (2004) Loss of poly(ADP-ribose) glycohydrolase causes progressive neurodegeneration in Drosophila melanogaster. Proc. Natl. Acad. Sci. U. S. A. 101, 82-86. https://doi.org/10.1073/pnas.2237114100
  31. Cohen-Armon, M., Visochek, L., Katzoff, A., Levitan, D., Susswein, A. J., Klein, R., Valbrun, M. and Schwartz, J. H. (2004) Long-term memory requires polyADP-ribosylation. Science 304, 1820-1822. https://doi.org/10.1126/science.1096775
  32. Cohen-Armon, M., Visochek, L., Rozensal, D., Kalal, A., Geistrikh, I., Klein, R., Bendetz-Nezer, S., Yao, Z. and Seger, R. (2007) DNA-independent PARP-1 activation by phosphorylated ERK2 increases Elk1 activity: a link to histone acetylation. Mol. Cell 25, 297-308. https://doi.org/10.1016/j.molcel.2006.12.012
  33. Goldberg, S., Visochek, L., Giladi, E., Gozes, I. and Cohen-Armon, M. (2009) PolyADP-ribosylation is required for long-term memory formation in mammals. J. Neurochem. 111, 72-79. https://doi.org/10.1111/j.1471-4159.2009.06296.x
  34. Guastafierro, T., Cecchinelli, B., Zampieri, M., Reale, A., Riggio, G., Sthandier, O., Zupi, G., Calabrese, L. and Caiafa, P. (2008) CCCTC-binding factor activates PARP-1 affecting DNA methylation machinery. J. Biol. Chem. 283, 21873-21880. https://doi.org/10.1074/jbc.M801170200
  35. Severin, J., Lizio, M., Harshbarger, J., Kawaji, H., Daub, C. O., Hayashizaki, Y., Consortium, F., Bertin, N. and Forrest, A. R. (2014) Interactive visualization and analysis of large-scale sequencing datasets using ZENBU. Nat. Biotechnol. 32, 217-219. https://doi.org/10.1038/nbt.2840
  36. Ohmiya, H., Vitezic, M., Frith, M. C., Itoh, M., Carninci, P., Forrest, A. R., Hayashizaki, Y., Lassmann, T. and Consortium, F. (2014) RECLU: a pipeline to discover reproducible transcriptional start sites and their alternative regulation using capped analysis of gene expression (CAGE). BMC Genomics. 15, 269. https://doi.org/10.1186/1471-2164-15-269
  37. Guzman, J. N., Sanchez-Padilla, J., Chan, C. S. and Surmeier, D. J. (2009) Robust pacemaking in substantia nigra dopaminergic neurons. J. Neurosci. 29, 11011-11019. https://doi.org/10.1523/JNEUROSCI.2519-09.2009
  38. Guzman, J. N., Sanchez-Padilla, J., Wokosin, D., Kondapalli, J., Ilijic, E., Schumacker, P. T. and Surmeier, D. J. (2010) Oxidant stress evoked by pacemaking in dopaminergic neurons is attenuated by DJ-1. Nature 468, 696-700. https://doi.org/10.1038/nature09536
  39. Clark, I. E., Dodson, M. W., Jiang, C., Cao, J. H., Huh, J. R., Seol, J. H., Yoo, S. J., Hay, B. A. and Guo, M. (2006) Drosophila pink1 is required for mitochondrial function and interacts genetically with parkin. Nature 441, 1162-1166. https://doi.org/10.1038/nature04779
  40. Park, J., Lee, S. B., Lee, S., Kim, Y., Song, S., Kim, S., Bae, E., Kim, J., Shong, M., Kim, J. M. and Chung, J. (2006) Mitochondrial dysfunction in Drosophila PINK1 mutants is complemented by parkin. Nature 441, 1157-1161. https://doi.org/10.1038/nature04788
  41. Ziviani, E., Tao, R. N. and Whitworth, A. J. (2010) Drosophila parkin requires PINK1 for mitochondrial translocation and ubiquitinates mitofusin. Proc. Natl. Acad. Sci. U. S. A. 107, 5018-5023. https://doi.org/10.1073/pnas.0913485107
  42. Collier, T. J., Kanaan, N. M. and Kordower, J. H. (2011) Ageing as a primary risk factor for Parkinson's disease: evidence from studies of non-human primates. Nat. Rev. Neurosci. 12, 359-366. https://doi.org/10.1038/nrn3039
  43. Corti, O., Hampe, C., Koutnikova, H., Darios, F., Jacquier, S., Prigent, A., Robinson, J. C., Pradier, L., Ruberg, M., Mirande, M., Hirsch, E., Rooney, T., Fournier, A. and Brice, A. (2003) The p38 subunit of the aminoacyl-tRNA synthetase complex is a Parkin substrate: linking protein biosynthesis and neurodegeneration. Hum. Mol. Genet. 12, 1427-1437. https://doi.org/10.1093/hmg/ddg159
  44. Ko, H. S., von Coelln, R., Sriram, S. R., Kim, S. W., Chung, K. K., Pletnikova, O., Troncoso, J., Johnson, B., Saffary, R., Goh, E. L., Song, H., Park, B. J., Kim, M. J., Kim, S., Dawson, V. L. and Dawson, T. M. (2005) Accumulation of the authentic parkin substrate aminoacyl- tRNA synthetase cofactor, p38/JTV-1, leads to catecholaminergic cell death. J. Neurosci. 25, 7968-7978. https://doi.org/10.1523/JNEUROSCI.2172-05.2005
  45. Ko, H. S., Lee, Y., Shin, J. H., Karuppagounder, S. S., Gadad, B. S., Koleske, A. J., Pletnikova, O., Troncoso, J. C., Dawson, V. L. and Dawson, T. M. (2010) Phosphorylation by the c-Abl protein tyrosine kinase inhibits parkin's ubiquitination and protective function. Proc. Natl. Acad. Sci. U.S.A. 107, 16691-16696. https://doi.org/10.1073/pnas.1006083107
  46. Imam, S. Z., Zhou, Q., Yamamoto, A., Valente, A. J., Ali, S. F., Bains, M., Roberts, J. L., Kahle, P. J., Clark, R. A. and Li, S. (2011) Novel regulation of parkin function through c-Abl-mediated tyrosine phosphorylation: implications for Parkinson's disease. J. Neurosci. 31, 157-163. https://doi.org/10.1523/JNEUROSCI.1833-10.2011
  47. Moore, D. J., West, A. B., Dawson, V. L. and Dawson, T. M. (2005) Molecular pathophysiology of Parkinson's disease. Annu. Rev. Neurosci. 28, 57-87. https://doi.org/10.1146/annurev.neuro.28.061604.135718
  48. Martin, I., Dawson, V. L. and Dawson, T. M. (2011) Recent advances in the genetics of Parkinson's disease. Annu. Rev. Genomics. Hum. Genet. 12, 301-325. https://doi.org/10.1146/annurev-genom-082410-101440
  49. Stark, C., Breitkreutz, B. J., Reguly, T., Boucher, L., Breitkreutz, A. and Tyers, M. (2006) BioGRID: a general repository for interaction datasets. Nucleic Acids Res. 34, D535-539. https://doi.org/10.1093/nar/gkj109
  50. Shannon, P., Markiel, A., Ozier, O., Baliga, N. S., Wang, J. T., Ramage, D., Amin, N., Schwikowski, B. and Ideker, T. (2003) Cytoscape: a software environment for integrated models of biomolecular interaction networks. Genome Res. 13, 2498-2504. https://doi.org/10.1101/gr.1239303
  51. Bindea, G., Mlecnik, B., Hackl, H., Charoentong, P., Tosolini, M., Kirilovsky, A., Fridman, W. H., Pages, F., Trajanoski, Z. and Galon, J. (2009) ClueGO: a Cytoscape plug-in to decipher functionally grouped gene ontology and pathway annotation networks. Bioinformatics 25, 1091-1093. https://doi.org/10.1093/bioinformatics/btp101
  52. Leung, A. K., Calabrese, J. M. and Sharp, P. A. (2006) Quantitative analysis of Argonaute protein reveals microRNA-dependent localization to stress granules. Proc. Natl. Acad. Sci. U. S. A. 103, 18125-18130. https://doi.org/10.1073/pnas.0608845103
  53. Anderson, P. and Kedersha, N. (2008) Stress granules: the Tao of RNA triage. Trends. Biochem. Sci. 33, 141-150. https://doi.org/10.1016/j.tibs.2007.12.003
  54. Leung, A. K., Vyas, S., Rood, J. E., Bhutkar, A., Sharp, P. A. and Chang, P. (2011) Poly(ADP-ribose) regulates stress responses and microRNA activity in the cytoplasm. Mol. Cell 42, 489-499. https://doi.org/10.1016/j.molcel.2011.04.015
  55. Gehrke, S., Imai, Y., Sokol, N. and Lu, B. (2010) Pathogenic LRRK2 negatively regulates microRNA-mediated translational repression. Nature 466, 637-641. https://doi.org/10.1038/nature09191
  56. Okamura, H., Yoshida, K., Amorim, B. R. and Haneji, T. (2008) Histone H1.2 is translocated to mitochondria and associates with Bak in bleomycin-induced apoptotic cells. J. Cell Biochem. 103, 1488-1496. https://doi.org/10.1002/jcb.21537

Cited by

  1. JNK Activation Contributes to Oxidative Stress-Induced Parthanatos in Glioma Cells via Increase of Intracellular ROS Production vol.54, pp.5, 2017, https://doi.org/10.1007/s12035-016-9926-y
  2. PARP-1 overexpression contributes to Cadmium-induced death in rat proximal tubular cells via parthanatos and the MAPK signalling pathway vol.7, pp.1, 2017, https://doi.org/10.1038/s41598-017-04555-2
  3. Regulation of necrotic cell death: p53, PARP1 and cyclophilin D-overlapping pathways of regulated necrosis? vol.73, pp.11-12, 2016, https://doi.org/10.1007/s00018-016-2202-5
  4. Programmed cell death in aging vol.23, 2015, https://doi.org/10.1016/j.arr.2015.04.002
  5. 23rd Annual Meeting of Chinese Society of AnesthesiologyProtective effect of haemopexin in rats subjected to focal cerebral ischaemia–reperfusion injuryRemifentanil preconditioning confers cardioprotection via glycogen synthase kinase-3β associated with ERK and JNK pathways in rats with heart failureProtective effects of hydrogen-rich medium on high-glucose-induced oxidative stress and poly(ADP-ribose)polymerase-1-dependent cell death (parthanatos) in rat Schwann cellsin vitroEffect of c-Src kinase-mediated ventilator-induced lung injury in ratsProtective effects of hydrogen on intestinal epithelial barrier against lipopolysaccharidein vitroand the regulation of Rho kinasePharmacokinetics and pharmacodynamics of dexmedetomidine applied to patients with end-stage renal failure and secondary hyperparathyroidism undergoing general anaesthesiaRole of microRNA-133b-5p in cardioprotection mediated by morphine preconditioning in H9C2 myocardial cellsNecrostatin-1 inhibits receptor-interacting protein 1/3-mediated necroptosis and attenuates intestinal ischaemia–reperfusion injuryIntegrin β3 positively regulates Toll-like receptor (TLR)-triggered inflammatory responses by targeting CD14 expression via a TLR4/MyD88-dependent and TRIF-independent pathway in murine sepsisMechanical ventilation augments Poly(I:C)-induced lung injury via WISP1–integrin β3 signalling in miceEffect of ifenprodil on intrathecal morphine-induced pruritus and its mechanismSevoflurane postconditioning protects neurones against oxygen–glucose deprivation and resuscitation via downregulation of Bid, Bim, and Puma mediated by inhibition of the mitochondrial permeability transition poreRole of serotonergic neurones in dorsal raphe nucleus in the facilitative effect of orexinergic signal on emergence from isoflurane anaesthesiaNR2B-containing NMDA receptor contributes to remifentanil-induced hyperalgesia via activation of DMT1(−)IREOestrogen replacement-induced neuroprotection against brain ischaemia–reperfusion injury involves activation of astrocytes via oestrogen receptor βMorphine-induced conditioned place preference and alteration of NR2B subunit expression in offspring of rats that underwent late-gestational morphine exposureGoal-directed intraoperative fluid therapy guided by mini-fluid challenge in elective colorectal resection: a prospective randomized studyNovel combined left and right atrial pressure-monitoring catheter: a simple and reliable left atrial pressure-monitoring method in paediatric cardiac surgeryComparison of qCON and BIS monitoring hypnotic effect during general anaesthesiaCan sonographic measurements of mandibular condyle mobility predict difficult laryngoscopy?Laryngoscope and a new tracheal tube assist lightwand intubation in difficult airways resulting from an unstable cervical spineSimvastatin attenuates neuropathic pain by inhibiting the RhoA/LIMK/cofilin pathway vol.116, pp.6, 2016, https://doi.org/10.1093/bja/aev308
  6. Poly(ADP-ribose)polymerase-1 hyperactivation in neurodegenerative diseases: The death knell tolls for neurons vol.63, 2017, https://doi.org/10.1016/j.semcdb.2016.11.007
  7. FAF1 mediates regulated necrosis through PARP1 activation upon oxidative stress leading to dopaminergic neurodegeneration vol.23, pp.11, 2016, https://doi.org/10.1038/cdd.2016.99
  8. Prevention of the degeneration of human dopaminergic neurons in an astrocyte co-culture system allowing endogenous drug metabolism vol.172, pp.16, 2015, https://doi.org/10.1111/bph.13193
  9. Poly(ADP-ribosylation) and neurodegenerative disorders vol.24, 2015, https://doi.org/10.1016/j.mito.2015.07.005
  10. Deoxypodophyllotoxin triggers parthanatos in glioma cells via induction of excessive ROS vol.371, pp.2, 2016, https://doi.org/10.1016/j.canlet.2015.11.044
  11. Psoralidin Stimulates Expression of Immediate-Early Genes and Synapse Development in Primary Cortical Neurons vol.43, pp.12, 2018, https://doi.org/10.1007/s11064-018-2674-9
  12. 2-Pentadecyl-2-Oxazoline Reduces Neuroinflammatory Environment in the MPTP Model of Parkinson Disease pp.1559-1182, 2018, https://doi.org/10.1007/s12035-018-1064-2