Mesencephalic astrocyte-derived neurotrophic factor prevents neuron loss via inhibiting ischemia-induced apoptosis

Journal of the Neurological Sciences

Volumn 344, Issue 1-2, 2014, Pages 129-138

  Yang, Wen ^a   Shen, Yujun ^a   Chen, Ying ^a   Chen, Lu ^a   Wang, Le ^a   Wang, Haiping ^a   Xu, Shengchun ^a   Fang, Shengyun ^a   Fu, Yu ^a   Yu, Yongqiang ^a   Shen, Yuxian ^a  

^a ANHUI MEDICAL UNIVERSITY   (China)

Author keywords

Apoptosis; Cerebral ischemia; Endoplasmic reticulum stress; Mesencephalic astrocyte derived neurotrophic factor; Middle cerebral artery occlusion; Unfolded protein response

Indexed keywords

CASPASE 3; GLUCOSE REGULATED PROTEIN 78; GROWTH ARREST AND DNA DAMAGE INDUCIBLE PROTEIN 153; MESSENGER RNA; NEUROTROPHIC FACTOR; PROPIDIUM IODIDE; PROTEIN IRE1; RECOMBINANT MESENCEPHALIC ASTROCYTE DERIVED NEUROTROPHIC FACTOR; RECOMBINANT PROTEIN; UNCLASSIFIED DRUG; X BOX BINDING PROTEIN 1; DNA BINDING PROTEIN; ENOLASE; MANF PROTEIN, RAT; NERVE GROWTH FACTOR; NEUROPROTECTIVE AGENT; REGULATORY FACTOR X TRANSCRIPTION FACTORS; TRANSCRIPTION FACTOR;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; BRAIN CORTEX; BRAIN INFARCTION SIZE; BRAIN ISCHEMIA; BRAIN VENTRICLE; CONTROLLED STUDY; ENDOPLASMIC RETICULUM STRESS; HIPPOCAMPUS; MALE; MIDDLE CEREBRAL ARTERY OCCLUSION; NERVE CELL; NEUROPROTECTION; NICK END LABELING; NONHUMAN; PRIORITY JOURNAL; PROTEIN CLEAVAGE; PROTEIN EXPRESSION; RAT; UNFOLDED PROTEIN RESPONSE; ANIMAL; BRAIN INFARCTION; COMPLICATION; CONVALESCENCE; DISEASE MODEL; DRUG EFFECTS; GENETICS; HEK293 CELL LINE; HUMAN; INFARCTION, MIDDLE CEREBRAL ARTERY; METABOLISM; NUCLEAR MAGNETIC RESONANCE IMAGING; PATHOLOGY; RANDOMIZED CONTROLLED TRIAL; SPRAGUE DAWLEY RAT; TIME;

ANIMALS; APOPTOSIS; BRAIN INFARCTION; CASPASE 3; DISEASE MODELS, ANIMAL; DNA-BINDING PROTEINS; ENDOPLASMIC RETICULUM STRESS; HEK293 CELLS; HUMANS; INFARCTION, MIDDLE CEREBRAL ARTERY; MAGNETIC RESONANCE IMAGING; MALE; NERVE GROWTH FACTORS; NEUROPROTECTIVE AGENTS; PHOSPHOPYRUVATE HYDRATASE; RATS; RATS, SPRAGUE-DAWLEY; RECOVERY OF FUNCTION; RNA, MESSENGER; TIME FACTORS; TRANSCRIPTION FACTORS;

EID: 84922465046     PISSN: 0022510X     EISSN: 18785883     Source Type: Journal    
DOI: 10.1016/j.jns.2014.06.042     Document Type: Article

References (48)

1. R. Shridhar, V. Shridhar, S. Rivard, J.M. Siegfried, H. Pietraszkiewicz, and J. Ensley et al. Mutations in the arginine-rich protein gene, in lung, breast, and prostate cancers, and in squamous cell carcinoma of the head and neck Cancer Res 56 1996 5576 5578
2. A. Apostolou, Y. Shen, Y. Liang, J. Luo, and S. Fang Armet, a UPR-upregulated protein, inhibits cell proliferation and ER stress-induced cell death Exp Cell Res 314 2008 2454 2467
3. V. Shridhar, S. Rivard, R. Shridhar, C. Mullins, L. Bostick, and W. Sakr et al. A gene from human chromosomal band 3p21.1 encodes a highly conserved arginine-rich protein and is mutated in renal cell carcinomas Oncogene 12 1996 1931 1939
4. P. Lindholm, M.H. Voutilainen, J. Lauren, J. Peranen, V.M. Leppanen, and J.O. Andressoo et al. Novel neurotrophic factor CDNF protects and rescues midbrain dopamine neurons in vivo Nature 448 2007 73 77
5. P. Petrova, A. Raibekas, J. Pevsner, N. Vigo, M. Anafi, and M.K. Moore et al. MANF: a new mesencephalic, astrocyte-derived neurotrophic factor with selectivity for dopaminergic neurons J Mol Neurosci 20 2003 173 188
6. M. Palgi, R. Lindstrom, J. Peranen, T.P. Piepponen, M. Saarma, and T.I. Heino Evidence that DmMANF is an invertebrate neurotrophic factor supporting dopaminergic neurons Proc Natl Acad Sci U S A 106 2009 2429 2434
7. Y.C. Chen, M. Sundvik, S. Rozov, M. Priyadarshini, and P. Panula MANF regulates dopaminergic neuron development in larval zebrafish Dev Biol 370 2012 237 249
8. C. Zhou, C. Xiao, J.W. Commissiong, K. Krnjevic, and J.H. Ye Mesencephalic astrocyte-derived neurotrophic factor enhances nigral gamma-aminobutyric acid release Neuroreport 17 2006 293 297
9. P. Lindholm, J. Peranen, J.O. Andressoo, N. Kalkkinen, Z. Kokaia, and O. Lindvall et al. MANF is widely expressed in mammalian tissues and differently regulated after ischemic and epileptic insults in rodent brain Mol Cell Neurosci 39 2008 356 371
10. N. Mizobuchi, J. Hoseki, H. Kubota, S. Toyokuni, J. Nozaki, and M. Naitoh et al. ARMET is a soluble ER protein induced by the unfolded protein response via ERSE-II element Cell Struct Funct 32 2007 41 50
11. A. Tadimalla, P.J. Belmont, D.J. Thuerauf, M.S. Glassy, J.J. Martindale, and N. Gude et al. Mesencephalic astrocyte-derived neurotrophic factor is an ischemia-inducible secreted endoplasmic reticulum stress response protein in the heart Circ Res 103 2008 1249 1258
12. C.C. Glembotski, D.J. Thuerauf, C. Huang, J.A. Vekich, R.A. Gottlieb, and S. Doroudgar Mesencephalic astrocyte-derived neurotrophic factor protects the heart from ischemic damage and is selectively secreted upon sarco/endoplasmic reticulum calcium depletion J Biol Chem 287 2012 25893 25904
13. C.L. Hartley, S. Edwards, L. Mullan, P.A. Bell, M. Fresquet, and R.P. Boot-Handford et al. Armet/Manf and Creld2 are components of a specialized ER stress response provoked by inappropriate formation of disulphide bonds: implications for genetic skeletal diseases Hum Mol Genet 10 2013 1093
14. Y.Q. Yu, L.C. Liu, F.C. Wang, Y. Liang, D.Q. Cha, and J.J. Zhang et al. Induction profile of MANF/ARMET by cerebral ischemia and its implication for neuron protection J Cereb Blood Flow Metab 30 2010 79 91
15. C.C. Glembotski Functions for the cardiomyokine, MANF, in cardioprotection, hypertrophy and heart failure J Mol Cell Cardiol 51 2011 512 517
16. Y. Shen, A. Sun, Y. Wang, D. Cha, H. Wang, and F. Wang et al. Upregulation of mesencephalic astrocyte-derived neurotrophic factor in glial cells is associated with ischemia-induced glial activation J Neuroinflammation 9 2012 254
17. M. Airavaara, M.J. Chiocco, D.B. Howard, K.L. Zuchowski, J. Peranen, and C. Liu et al. Widespread cortical expression of MANF by AAV serotype 7: localization and protection against ischemic brain injury Exp Neurol 225 2010 104 113
18. M. Airavaara, H. Shen, C.C. Kuo, J. Peranen, M. Saarma, and B. Hoffer et al. Mesencephalic astrocyte-derived neurotrophic factor reduces ischemic brain injury and promotes behavioral recovery in rats J Comp Neurol 515 2009 116 124
19. W. Yan, H. Zhang, X. Bai, Y. Lu, H. Dong, and L. Xiong Autophagy activation is involved in neuroprotection induced by hyperbaric oxygen preconditioning against focal cerebral ischemia in rats Brain Res 1402 2011 109 121
20. P. Norlen, M. Kitano, E. Lindstrom, and R. Hakanson Anaesthetic agents inhibit gastrin-stimulated but not basal histamine release from rat stomach ECL cells Br J Pharmacol 130 2000 725 730
21. J.B. Bederson, L.H. Pitts, M. Tsuji, M.C. Nishimura, R.L. Davis, and H. Bartkowski Rat middle cerebral artery occlusion: evaluation of the model and development of a neurologic examination Stroke 17 1986 472 476
22. J.B. Bederson, L.H. Pitts, S.M. Germano, M.C. Nishimura, R.L. Davis, and H.M. Bartkowski Evaluation of 2,3,5-triphenyltetrazolium chloride as a stain for detection and quantification of experimental cerebral infarction in rats Stroke 17 1986 1304 1308
23. C.J. Stork, and Y.V. Li Rising zinc: a significant cause of ischemic neuronal death in the CA1 region of rat hippocampus J Cereb Blood Flow Metab 29 2009 1399 1408
24. M.H. Voutilainen, S. Back, E. Porsti, L. Toppinen, L. Lindgren, and P. Lindholm et al. Mesencephalic astrocyte-derived neurotrophic factor is neurorestorative in rat model of Parkinson's disease J Neurosci 29 2009 9651 9659
25. M. Palgi, D. Greco, R. Lindstrom, P. Auvinen, and T.I. Heino Gene expression analysis of Drosophilaa Manf mutants reveals perturbations in membrane traffic and major metabolic changes BMC Genomics 13 2012 134
26. S. Cox, B.K. Harvey, J.F. Sanchez, J.Y. Wang, and Y. Wang Mediation of BMP7 neuroprotection by MAPK and PKC in rat primary cortical cultures Brain Res 1010 1-2 2004 55 61
27. B.K. Harvey, A. Mark, J. Chou, G.J. Chen, B.J. Hoffer, and Y. Wang Neurotrophic effects of bone morphogenetic protein-7 in a rat model of Parkinson's disease Brain Res 1022 1-2 2004 88 95
28. A.C. Tomac, A.D. Agulnick, N. Haughey, C.F. Chang, Y. Zhang, and C. Bäckman et al. Effects of cerebral ischemia in mice deficient in Persephin Proc Natl Acad Sci U S A 99 14 2002 9521 9526
29. V. Parkash, P. Lindholm, J. Peranen, N. Kalkkinen, E. Oksanen, and M. Saarma et al. The structure of the conserved neurotrophic factors MANF and CDNF explains why they are bifunctional Protein Eng Des Sel 22 2009 233 241
30. J. Hoseki, H. Sasakawa, Y. Yamaguchi, M. Maeda, H. Kubota, and K. Kato et al. Solution structure and dynamics of mouse ARMET FEBS Lett 584 2010 1536 1542
31. M. Hellman, J. Peränen, M. Saarma, and P. Permi 1H, 13C and 15N resonance assignments of the human mesencephalic astrocyte-derived neurotrophic factor Biomol NMR Assign 4 2010 215 217
32. M. Hellman, U. Arumae, L.Y. Yu, P. Lindholm, J. Peranen, and M. Saarma et al. Mesencephalic astrocyte-derived neurotrophic factor (MANF) has a unique mechanism to rescue apoptotic neurons J Biol Chem 286 2011 2675 2680
33. L. Aravind, and E.V. Koonin SAP - a putative DNA-binding motif involved in chromosomal organization Trends Biochem Sci 25 2000 112 114
34. J.R. Walker, R.A. Corpina, and J. Goldberg Structure of the Ku heterodimer bound to DNA and its implications for double-strand break repair Nature 412 2001 607 614
35. M. Sawada, W. Sun, P. Hayes, K. Leskov, D.A. Boothman, and S. Matsuyama Ku70 suppresses the apoptotic translocation of Bax to mitochondria Nat Cell Biol 5 2003 320 329
36. M. Sawada, P. Hayes, and S. Matsuyama Cytoprotective membrane-permeable peptides designed from the Bax-binding domain of Ku70 Nat Cell Biol 5 2003 352 357
37. T. Sugawara, N. Noshita, A. Lewen, G.W. Kim, and P.H. Chan Neuronal expression of the DNA repair protein Ku 70 after ischemic preconditioning corresponds to tolerance to global cerebral ischemia Stroke 32 2001 2388 2393
38. P. Lindholm, and M. Saarma Novel CDNF/MANF family of neurotrophic factors Dev Neurobiol 70 2010 360 371
39. D. Ron, and P. Walter Signal integration in the endoplasmic reticulum unfolded protein response Nat Rev Mol Cell Biol 8 2007 519 529
40. R.J. Kaufman, D. Scheuner, M. Schroder, X.H. Shen, K. Lee, and C.Y. Liu et al. The unfolded protein response in nutrient sensing and differentiation Nat Rev Mol Cell Biol 3 2002 411 421
41. J.D. Malhotra, and R.J. Kaufman The endoplasmic reticulum and the unfolded protein response Semin Cell Dev Biol 18 2007 716 731
42. S.J. Marciniak, and D. Ron Endoplasmic reticulum stress signaling in disease Physiol Rev 86 2006 1133 1149
43. S.C. Cramer, and M. Chopp Recovery recapitulates ontogeny Trends Neurosci 23 2000 265 271
44. R.V. Rao, A. Peel, A. Logvinova, G. del Rio, E. Hermel, and T. Yokota et al. Coupling endoplasmic reticulum stress to the cell death program: role of the ER chaperone GRP78 FEBS Lett 514 2002 122 128
45. Y. Oida, M. Shimazawa, K. Imaizumi, and H. Hara Involvement of endoplasmic reticulum stress in the neuronal death induced by transient forebrain ischemia in gerbil Neuroscience 151 2008 111 119
46. S. Tajiri, S. Oyadomari, S. Yano, M. Morioka, T. Gotoh, and J.I. Hamada et al. Ischemia-induced neuronal cell death is mediated by the endoplasmic reticulum stress pathway involving CHOP Cell Death Differ 11 2004 403 415
47. M. Lindahl, T. Danilova, E. Palm, P. Lindholm, V. Vootele Voikar, and E. Hakonen et al. MANF is indispensable for the proliferation and survival of pancreatic beta cells Cell Rep 7 2 2014 366 375
48. L.Y. Yu, M. Saarma, and U. Arumae Death receptors and caspases but not mitochondria are activated in the GDNF- or BDNF-deprived dopaminergic neurons J Neurosci 28 2008 7467 7475