Molecules and Cells

Korean Society for Molecular and Cellular Biology (한국분자세포생물학회)
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Neuroprotective Effects of Protein Tyrosine Phosphatase 1B Inhibition against ER Stress-Induced Toxicity

  • Jeon, Yu-Mi (Department of Neural Development and Disease, Korea Brain Research Institute (KBRI)) ;
  • Lee, Shinrye (Department of Neural Development and Disease, Korea Brain Research Institute (KBRI)) ;
  • Kim, Seyeon (Department of Neural Development and Disease, Korea Brain Research Institute (KBRI)) ;
  • Kwon, Younghwi (Department of Neural Development and Disease, Korea Brain Research Institute (KBRI)) ;
  • Kim, Kiyoung (Department of Medical Biotechnology, Soonchunhyang University) ;
  • Chung, Chang Geon (Department of Brain & Cognitive Sciences, Daegu Gyeongbuk Institute of Science and Technology (DGIST)) ;
  • Lee, Seongsoo (Gwangju Center, Korea Basic Science Institute (KBSI)) ;
  • Lee, Sung Bae (Department of Brain & Cognitive Sciences, Daegu Gyeongbuk Institute of Science and Technology (DGIST)) ;
  • Kim, Hyung-Jun (Department of Neural Development and Disease, Korea Brain Research Institute (KBRI))
  • Received : 2016.12.30
  • Accepted : 2017.03.22
  • Published : 2017.04.30
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Abstract

Several lines of evidence suggest that endoplasmic reticulum (ER) stress plays a critical role in the pathogenesis of many neurodegenerative diseases such as Alzheimer's disease, Parkinson's disease, and amyotrophic lateral sclerosis. Protein tyrosine phosphatase 1B (PTP1B) is known to regulate the ER stress signaling pathway, but its role in neuronal systems in terms of ER stress remains largely unknown. Here, we showed that rotenone-induced toxicity in human neuroblastoma cell lines and mouse primary cortical neurons was ameliorated by PTP1B inhibition. Moreover, the increase in the level of ER stress markers ($eIF2{\alpha}$ phosphorylation and PERK phosphorylation) induced by rotenone treatment was obviously suppressed by concomitant PTP1B inhibition. However, the rotenone-induced production of reactive oxygen species (ROS) was not affected by PTP1B inhibition, suggesting that the neuroprotective effect of the PTP1B inhibitor is not associated with ROS production. Moreover, we found that MG132-induced toxicity involving proteasome inhibition was also ameliorated by PTP1B inhibition in a human neuroblastoma cell line and mouse primary cortical neurons. Consistently, downregulation of the PTP1B homologue gene in Drosophila mitigated rotenone- and MG132-induced toxicity. Taken together, these findings indicate that PTP1B inhibition may represent a novel therapeutic approach for ER stress-mediated neurodegenerative diseases.

Keywords

References

  1. Araki, W., Yuasa, K., Takeda, S., Shirotani, K., Takahashi, K., and Tabira, T. (2000). Overexpression of presenilin-2 enhances apoptotic death of cultured cortical neurons. Ann. N. Y. Acad. Sci. 920, 241-244.
  2. Bettaieb, A., Matsuo, K., Matsuo, I., Wang, S., Melhem, R., Koromilas, A.E., and Haj, F.G. (2012). Protein tyrosine phosphatase 1B deficiency potentiates $PERK/eIF2{\alpha}$ signaling in brown adipocytes. PLoS One 7, e32212. https://doi.org/10.1371/journal.pone.0032212
  3. Chen, G., Fan, Z., Wang, X., Ma, C., Bower, K.A., Shi, X., Ke, Z.J., and Luo, J. (2007). Brain-derived neurotrophic factor suppresses tunicamycin-induced upregulation of CHOP in neurons. J. Neurosci. Res. 85, 1674-1684. https://doi.org/10.1002/jnr.21292
  4. Chen, Y.Y., Chen, G., Fan, Z., Luo, J., and Ke, Z.J. (2008). GSK3beta and endoplasmic reticulum stress mediate rotenone-induced death of SK-N-MC neuroblastoma cells. Biochem. Pharmacol. 76, 128-138. https://doi.org/10.1016/j.bcp.2008.04.010
  5. Chung, J., Kim, K.H., Lee, S.C., An, S.H., and Kwon, K. (2015). Ursodeoxycholic acid (UDCA) exerts anti-atherogenic effects by inhibiting endoplasmic reticulum (ER) stress induced by disturbed flow. Mol. Cells 38, 851-858. https://doi.org/10.14348/molcells.2015.0094
  6. Cui, W., Bai, Y., Luo, P., Miao, L., and Cai, L. (2013). Preventive and therapeutic effects of MG132 by activating Nrf2-ARE signaling pathway on oxidative stress-induced cardiovascular and renal injury. Oxid. Med. Cell. Longev. 2013, 306073.
  7. Cui, T., Lai, Y., Janicki, J.S., and Wang, X. (2016). Nuclear factor erythroid-2 related factor 2 (Nrf2)-mediated protein quality control in cardiomyocytes. Front. Biosci. (Landmark Ed.) 21, 192-202. https://doi.org/10.2741/4384
  8. Day, B.J., Patel, M., Calavetta, L., Chang, L.Y., and Stamler, J.S. (1999). A mechanism of paraquat toxicity involving nitric oxide synthase. Proc. Natl. Acad. Sci. USA 96, 12760-12765. https://doi.org/10.1073/pnas.96.22.12760
  9. Foufelle, F., and Fromenty, B. (2016). Role of endoplasmic reticulum stress in drug-induced toxicity. Pharmacol. Res. Perspect. 4, e00211. https://doi.org/10.1002/prp2.211
  10. Goswami, P., Gupta, S., Biswas, J., Joshi, N., Swarnkar, S., Nath, C., and Singh, S. (2016). Endoplasmic reticulum stress plays a key role in rotenone-induced apoptotic death of neurons. Mol. Neurobiol. 53, 285-298. https://doi.org/10.1007/s12035-014-9001-5
  11. Gu, F., Nguyen, D.T., Stuible, M., Dube, N., Tremblay, M.L., and Chevet, E. (2004). Protein-tyrosine phosphatase 1B potentiates IRE1 signaling during endoplasmic reticulum stress. J. Biol. Chem. 279, 49689-49693. https://doi.org/10.1074/jbc.C400261200
  12. Hakim, F., Wang, Y., Carreras, A., Hirotsu, C., Zhang, J., Peris, E., and Gozal, D. (2015). Chronic sleep fragmentation during the sleep period induces hypothalamic endoplasmic reticulum stress and PTP1b-mediated leptin resistance in male mice. Sleep 38, 31-40. https://doi.org/10.5665/sleep.4320
  13. Hardie, R.A., van Dam, E., Cowley, M., Han, T.L., Balaban, S., Pajic, M., Pinese, M., Iconomou, M., Shearer, R.F., McKenna, J., et al. (2017). Mitochondrial mutations and metabolic adaptation in pancreatic cancer. Cancer Metab. 5, 2. https://doi.org/10.1186/s40170-017-0164-1
  14. Hotamisligil, G.S. (2010). Endoplasmic reticulum stress and the inflammatory basis of metabolic disease. Cell 140, 900-917. https://doi.org/10.1016/j.cell.2010.02.034
  15. Kapeta, S., Chondrogianni, N., and Gonos, E.S. (2010). Nuclear erythroid factor 2-mediated proteasome activation delays senescence in human fibroblasts. J. Biol. Chem. 285, 8171-8184. https://doi.org/10.1074/jbc.M109.031575
  16. Kim, H.J., Raphael, A.R., LaDow, E.S., McGurk, L., Weber, R.A., Trojanowski, J.Q., Lee, V.M., Finkbeiner, S., Gitler, A.D., and Bonini, N.M. (2014). Therapeutic modulation of $eIF2{\alpha}$ phosphorylation rescues TDP-43 toxicity in amyotrophic lateral sclerosis disease models. Nat. Genet. 46, 152-160. https://doi.org/10.1038/ng.2853
  17. Kwak, M.K., Wakabayashi, N., Greenlaw, J.L., Yamamoto, M., and Kensler, T.W. (2003a). Antioxidants enhance mammalian proteasome expression through the Keap1-Nrf2 signaling pathway. Mol. Cell. Biol. 23, 8786-8794. https://doi.org/10.1128/MCB.23.23.8786-8794.2003
  18. Kwak, M.K., Wakabayashi, N., Itoh, K., Motohashi, H., Yamamoto, M., and Kensler, T.W. (2003b). Modulation of gene expression by cancer chemopreventive dithiolethiones through the Keap1-Nrf2 pathway. Identification of novel gene clusters for cell survival. J. Biol. Chem. 278, 8135-8145. https://doi.org/10.1074/jbc.M211898200
  19. Mobasher, M.A., Gonzalez-Rodriguez, A., Santamaria, B., Ramos, S., Martin, M.A., Goya, L., and Valverde, A.M. (2013). Protein tyrosine phosphatase 1B modulates GSK3beta/Nrf2 and IGFIR signaling pathways in acetaminophen-induced hepatotoxicity. Cell Death Dis. 4, e626. https://doi.org/10.1038/cddis.2013.150
  20. Moreno, J.A., Halliday, M., Molloy, C., Radford, H., Verity, N., Axten, J.M., Ortori, C.A., Willis, A.E., Fischer, P.M., Barrett, D.A., et al. (2013). Oral treatment targeting the unfolded protein response prevents neurodegeneration and clinical disease in prion-infected mice. Sci. Transl. Med. 5, 206ra138.
  21. Nakajima, S., Kato, H., Takahashi, S., Johno, H., and Kitamura, M. (2011). Inhibition of NF-kappaB by MG132 through ER stressmediated induction of LAP and LIP. FEBS Lett. 585, 2249-2254. https://doi.org/10.1016/j.febslet.2011.05.047
  22. Nandipati, S., and Litvan, I. (2016). Environmental Exposures and Parkinson's Disease. Int. J. Environ. Res. Public Health 13, 881. https://doi.org/10.3390/ijerph13090881
  23. Oslowski, C.M., and Urano, F. (2011). Measuring ER stress and the unfolded protein response using mammalian tissue culture system. Methods Enzymol. 490, 71-92.
  24. Ozcan, L., and Tabas, I. (2012). Role of endoplasmic reticulum stress in metabolic disease and other disorders. Annu. Rev. Med. 63, 317-328. https://doi.org/10.1146/annurev-med-043010-144749
  25. Ozek, C., Kanoski, S.E., Zhang, Z.Y., Grill, H.J., and Bence, K.K. (2014). Protein-tyrosine phosphatase 1B (PTP1B) is a novel regulator of central brain-derived neurotrophic factor and tropomyosin receptor kinase B (TrkB) signaling. J. Biol. Chem. 289, 31682-31692. https://doi.org/10.1074/jbc.M114.603621
  26. Pajares, M., Cuadrado, A., and Rojo, A.I. (2017). Modulation of proteostasis by transcription factor NRF2 and impact in neurodegenerative diseases. Redox Biol. 11, 543-553. https://doi.org/10.1016/j.redox.2017.01.006
  27. Pal, R., Monroe, T.O., Palmieri, M., Sardiello, M., and Rodney, G.G. (2014). Rotenone induces neurotoxicity through Rac1-dependent activation of NADPH oxidase in SHSY-5Y cells. FEBS Lett. 588, 472-481. https://doi.org/10.1016/j.febslet.2013.12.011
  28. Panzhinskiy, E., Ren, J., and Nair, S. (2013a). Protein tyrosine phosphatase 1B and insulin resistance: role of endoplasmic reticulum stress/reactive oxygen species/nuclear factor kappa B axis. PLoS One 8, e77228. https://doi.org/10.1371/journal.pone.0077228
  29. Panzhinskiy, E., Hua, Y., Culver, B., Ren, J., and Nair, S. (2013b). Endoplasmic reticulum stress upregulates protein tyrosine phosphatase 1B and impairs glucose uptake in cultured myotubes. Diabetologia 56, 598-607. https://doi.org/10.1007/s00125-012-2782-z
  30. Pickering, A.M., Linder, R.A., Zhang, H., Forman, H.J., and Davies, K.J. (2012). Nrf2-dependent induction of proteasome and $Pa28{\alpha}{\beta}$ regulator are required for adaptation to oxidative stress. J. Biol. Chem. 287, 10021-10031. https://doi.org/10.1074/jbc.M111.277145
  31. Popov, D. (2012). Endoplasmic reticulum stress and the on site function of resident PTP1B. Biochem. Biophys. Res. Commun. 422, 535-538. https://doi.org/10.1016/j.bbrc.2012.05.048
  32. Prada, P.O., Quaresma, P.G., Caricilli, A.M., Santos, A.C., Guadagnini, D., Morari, J., Weissmann, L., Ropelle, E.R., Carvalheira, J.B., Velloso, L.A., et al. (2013). Tub has a key role in insulin and leptin signaling and action in vivo in hypothalamic nuclei. Diabetes 62, 137-148. https://doi.org/10.2337/db11-1388
  33. Qiu, B., Hu, S., Liu, L., Chen, M., Wang, L., Zeng, X., and Zhu, S. (2013). CART attenuates endoplasmic reticulum stress response induced by cerebral ischemia and reperfusion through upregulating BDNF synthesis and secretion. Biochem. Biophys. Res. Commun. 436, 655-659. https://doi.org/10.1016/j.bbrc.2013.05.142
  34. Radford, H., Moreno, J.A., Verity, N., Halliday, M., and Mallucci, G.R. (2015). PERK inhibition prevents tau-mediated neurodegeneration in a mouse model of frontotemporal dementia. Acta Neuropathol. 130, 633-642. https://doi.org/10.1007/s00401-015-1487-z
  35. Seoposengwe, K., van Tonder, J.J., and Steenkamp, V. (2013). In vitro neuroprotective potential of four medicinal plants against rotenone-induced toxicity in SH-SY5Y neuroblastoma cells. BMC Complement. Altern. Med. 13, 353. https://doi.org/10.1186/1472-6882-13-353
  36. Shimoke, K., Utsumi, T., Kishi, S., Nishimura, M., Sasaya, H., Kudo, M., and Ikeuchi, T. (2004). Prevention of endoplasmic reticulum stress-induced cell death by brain-derived neurotrophic factor in cultured cerebral cortical neurons. Brain Res. 1028, 105-111. https://doi.org/10.1016/j.brainres.2004.09.005
  37. Smith, H.L., and Mallucci, G.R. (2016). The unfolded protein response: mechanisms and therapy of neurodegeneration. Brain 139, 2113-2121. https://doi.org/10.1093/brain/aww101
  38. Song, J.X., Choi, M.Y., Wong, K.C., Chung, W.W., Sze, S.C., Ng, T.B., and Zhang, K.Y. (2012) Baicalein antagonizes rotenone-induced apoptosis in dopaminergic SH-SY5Y cells related to Parkinsonism. Chin. Med. 7, 1. https://doi.org/10.1186/1749-8546-7-1
  39. Song, G.J., Jung, M., Kim, J.H., Park, H., Rahman, M.H., Zhang, S., Zhang, Z.Y., Park, D.H., Kook, H., Lee, I.K., et al. (2016). A novel role for protein tyrosine phosphatase 1B as a positive regulator of neuroinflammation. J. Neuroinflammation 13, 86. https://doi.org/10.1186/s12974-016-0545-3
  40. Su, Q., Wang, S., Gao, H.Q., Kazemi, S., Harding, H.P., Ron, D., and Koromilas, A.E. (2008). Modulation of the eukaryotic initiation factor 2 alpha-subunit kinase PERK by tyrosine phosphorylation. J. Biol. Chem. 283, 469-475. https://doi.org/10.1074/jbc.M704612200
  41. Swarnkar, S., Goswami, P., Kamat, P.K., Gupta, S., Patro, I.K., Singh, S., and Nath, C. (2012). Rotenone-induced apoptosis and role of calcium: a study on Neuro-2a cells. Arch. Toxicol. 86, 1387-1397. https://doi.org/10.1007/s00204-012-0853-z
  42. Vieira, M.N., Lyra E Silva, N.M., Ferreira, S.T., and De Felice, F.G. (2017). Protein tyrosine phosphatase 1B (PTP1B): a potential target for Alzheimer's therapy? Front. Aging Neurosci. 9, 7.
  43. Werner, E.D., Brodsky, J.L., and McCracken, A.A. (1996). Proteasome-dependent endoplasmic reticulum-associated protein degradation: an unconventional route to a familiar fate. Proc. Natl. Acad. Sci. USA 93, 13797-13801. https://doi.org/10.1073/pnas.93.24.13797
  44. Wei, H.J., Xu, J.H., Li, M.H., Tang, J.P., Zou, W., Zhang, P., Wang, L., Wang, C.Y., and Tang, X.Q. (2014). Hydrogen sulfide inhibits homocysteine-induced endoplasmic reticulum stress and neuronal apoptosis in rat hippocampus via upregulation of the BDNF-TrkB pathway. Acta Pharmacol. Sin. 35, 707-715. https://doi.org/10.1038/aps.2013.197
  45. Wiesmann, C., Barr, K.J., Kung, J., Zhu, J., Erlanson, D.A., Shen, W., Fahr, B.J., Zhong, M., Taylor, L., Randal, M., et al. (2004). Allosteric inhibition of protein tyrosine phosphatase 1B. Nat. Struct. Mol. Biol. 11, 730-737. https://doi.org/10.1038/nsmb803
  46. Xiang, C., Wang, Y., Zhang, H., and Han, F. (2017). The role of endoplasmic reticulum stress in neurodegenerative disease. Apoptosis 22, 1-26. https://doi.org/10.1007/s10495-016-1296-4
  47. Xu, C., Bailly-Maitre, B., and Reed, J.C. (2005). Endoplasmic reticulum stress: cell life and death decisions. J. Clin. Invest. 115, 2656-2664. https://doi.org/10.1172/JCI26373
  48. Xu, Y., Liu, X., Guo, F., Ning, Y., Zhi, X., Wang, X., Chen, S., Yin, L., and Li, X. (2012). Effect of estrogen sulfation by SULT1E1 and PAPSS on the development of estrogen-dependent cancers. Cancer Sci. 103, 1000-1009. https://doi.org/10.1111/j.1349-7006.2012.02258.x
  49. Zhang, K. (2010). Integration of ER stress, oxidative stress and the inflammatory response in health and disease. Int. J. Clin. Exp. Med. 3, 33-40.
  50. Zhu, W., Bijur, G.N., Styles, N.A., and Li, X. (2004). Regulation of FOXO3a by brain-derived neurotrophic factor in differentiated human SH-SY5Y neuroblastoma cells. Brain Res. Mol. Brain Res. 126, 45-56. https://doi.org/10.1016/j.molbrainres.2004.03.019
  51. Zhu, X., Zhou, Y., Tao, R., Zhao, J., Chen, J., Liu, C., Xu, Z., Bao, G., Zhang, J., Chen, M., et al. (2015). Upregulation of PTP1B after rat spinal cord injury. Inflammation 38, 1891-1902. https://doi.org/10.1007/s10753-015-0169-2

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