Cajaninstilbene acid protects corticosterone-induced injury in PC12 cells by inhibiting oxidative and endoplasmic reticulum stress-mediated apoptosis

Neurochemistry International

Volumn 78, Issue , 2014, Pages 43-52

  Liu, Yamin ^a   Shen, Shengnan ^a   Li, Zongyang ^a   Jiang, Yumao ^a   Si, Jianyong ^a   Chang, Qi ^a   Liu, Xinmin ^a   Pan, Ruile ^a  

^a INSTITUTE OF MEDICINAL PLANT DEVELOPMENT   (China)

Author keywords

Cajaninstilbene acid; Corticosterone; Endoplasmic reticulum stress; Neuroprotection; Oxidative stress

Indexed keywords

CAJANINSTILBENE ACID; CATALASE; CCAAT ENHANCER BINDING PROTEIN; CORTICOSTERONE; GLUCOCORTICOID RECEPTOR; GLUCOSE REGULATED PROTEIN 78; HOE 33342; LACTATE DEHYDROGENASE; NEUROPROTECTIVE AGENT; STILBENE; SUPEROXIDE DISMUTASE; UNCLASSIFIED DRUG; 3-HYDROXY-4-PRENYL-5-METHOXYSTILBENE-2-CARBOXYLIC ACID; SALICYLIC ACID DERIVATIVE; STILBENE DERIVATIVE;

ANIMAL CELL; APOPTOSIS; ARTICLE; CALCIUM CELL LEVEL; CELL PROTECTION; CONTROLLED STUDY; CYTOTOXICITY; ENDOPLASMIC RETICULUM STRESS; HIPPOCAMPUS; HOMEOSTASIS; NERVE CELL; NONHUMAN; OXIDATIVE STRESS; RAT; ANIMAL; DOSE RESPONSE; DRUG EFFECTS; PC12 CELL LINE; PHYSIOLOGY;

ANIMALS; APOPTOSIS; CORTICOSTERONE; CYTOPROTECTION; DOSE-RESPONSE RELATIONSHIP, DRUG; ENDOPLASMIC RETICULUM STRESS; OXIDATIVE STRESS; PC12 CELLS; RATS; SALICYLATES; STILBENES;

EID: 84907898362     PISSN: 01970186     EISSN: 18729754     Source Type: Journal    
DOI: 10.1016/j.neuint.2014.08.007     Document Type: Article

References (82)

1. D. Acosta-Alvear, Y. Zhou, A. Blais, M. Tsikitis, N.H. Lents, C. Arias, C.J. Lennon, Y. Kluger, and B.D. Dynlacht XBP1 controls diverse cell type- and condition-specific transcriptional regulatory networks Mol. Cell 27 1 2007 53 66
2. M. Aihara, I. Ida, N. Yuuki, A. Oshima, H. Kumano, K. Takahashi, M. Fukuda, N. Oriuchi, K. Endo, and H. Matsuda HPA axis dysfunction in unmedicated major depressive disorder and its normalization by pharmacotherapy correlates with alteration of neural activity in prefrontal cortex and limbic/paralimbic regions Psychiatry Res. 155 3 2007 245 256
3. T. Anelli, and R. Sitia Protein quality control in the early secretory pathway EMBO J. 27 2 2008 315 327
4. S.V. Avery Molecular targets of oxidative stress Biochem. J. 434 2 2011 201 210
5. M. Bilici, H. Efe, M.A. Koroglu, H.A. Uydu, M. Bekaroglu, and O. Deger Antioxidative enzyme activities and lipid peroxidation in major depression: alterations by antidepressant treatments J. Affect. Disord. 64 1 2001 43 51
6. M. Boyce, and J. Yuan Cellular response to endoplasmic reticulum stress: a matter of life or death Cell Death Differ. 13 3 2006 363 373
7. M. Calfon, H. Zeng, F. Urano, J.H. Till, S.R. Hubbard, H.P. Harding, S.G. Clark, and D. Ron IRE1 couples endoplasmic reticulum load to secretory capacity by processing the XBP-1 mRNA Nature 415 6867 2002 92 96
8. J.H. Choi, A.Y. Choi, H. Yoon, W. Choe, K.S. Yoon, J. Ha, E.J. Yeo, and I. Kang Baicalein protects HT22 murine hippocampal neuronal cells against endoplasmic reticulum stress-induced apoptosis through inhibition of reactive oxygen species production and CHOP induction Exp. Mol. Med. 42 12 2010 811 822
9. A.Y. Choi, J.H. Choi, K.Y. Hwang, Y.J. Jeong, W. Choe, K.S. Yoon, J. Ha, S.S. Kim, J.H. Youn, and E.J. Yeo Licochalcone A induces apoptosis through endoplasmic reticulum stress via a phospholipase Cgamma1-, Ca(2+)-, and reactive oxygen species-dependent pathway in HepG2 human hepatocellular carcinoma cells Apoptosis 19 4 2014 682 697
10. Z. Dong, P. Saikumar, J.M. Weinberg, and M.A. Venkatachalam Calcium in cell injury and death Annu. Rev. Pathol. 1 2006 405 434
11. K.M. Doyle, D. Kennedy, A.M. Gorman, S. Gupta, S.J. Healy, and A. Samali Unfolded proteins and endoplasmic reticulum stress in neurodegenerative disorders J. Cell Mol. Med. 15 10 2011 2025 2039
12. B. Eymin, L. Dubrez, M. Allouche, and E. Solary Increased gadd153 messenger RNA level is associated with apoptosis in human leukemic cells treated with etoposide Cancer Res. 57 4 1997 686 695
13. M.R. Farrukh, U.A. Nissar, Q. Afnan, R.A. Rafiq, L. Sharma, S. Amin, P. Kaiser, P.R. Sharma, and S.A. Tasduq Oxidative stress mediated Ca(2+) release manifests endoplasmic reticulum stress leading to unfolded protein response in UV-B irradiated human skin cells J. Dermatol. Sci. 75 1 2014 24 35
14. R.A. Floyd Antioxidants, oxidative stress, and degenerative neurological disorders Proc. Soc. Exp. Biol. Med. 222 3 1999 236 245
15. Fu, Y., 2012. Application of Cajanus cajan stilbene acid for preparing pharmaceutical preparation for preventing and treating bacterial infectious diseases, and the preparation method. In: Northeast Forestry University, Peop. Rep. China. CN102552230A.
16. Fu, Y., Zu, Y., Wu, N., Kong, Y., Liu, W., Hua, X., 2009. Application of longistyline A 2-carboxylic acid and pinostrobin from Cajanus cajan in preparing anti-herpesvirus medicine. In: Northeast Forestry University, Peop. Rep. China. CN101485649A.
17. D. Gackowski, R. Rozalski, A. Siomek, T. Dziaman, K. Nicpon, M. Klimarczyk, A. Araszkiewicz, and R. Olinski Oxidative stress and oxidative DNA damage is characteristic for mixed Alzheimer disease/vascular dementia J. Neurol. Sci. 266 1-2 2008 57 62
18. Y. Goodman, A.J. Bruce, B. Cheng, and M.P. Mattson Estrogens attenuate and corticosterone exacerbates excitotoxicity, oxidative injury, and amyloid beta-peptide toxicity in hippocampal neurons J. Neurochem. 66 5 1996 1836 1844
19. A. Habib, A.S. Anisuzzaman, R.I. Khan, and A. Gafur Chemical and pharmacological characterization of hypolipidemic compound from Cajanus cajan Bangladesh J. Pharmacol. 5 1 2010 34 38
20. H.P. Harding, Y. Zhang, A. Bertolotti, H. Zeng, and D. Ron Perk is essential for translational regulation and cell survival during the unfolded protein response Mol. Cell 5 5 2000 897 904
21. W.A. Holtz, J.M. Turetzky, Y.J. Jong, and K.L. O'Malley Oxidative stress-triggered unfolded protein response is upstream of intrinsic cell death evoked by parkinsonian mimetics J. Neurochem. 99 1 2006 54 69
22. X.-y. Ji, Xue S.-t., G.-h. Zheng, Y.-x. Han, Z.-y. Liu, J.-d. Jiang, and Li. Z-r Total synthesis of cajanine and its antiproliferative activity against human hepatoma cells Acta Pharm. Sin. B 1 2 2011 93 99
23. J. Jia, Y. Xiao, W. Wang, L. Qing, Y. Xu, H. Song, X. Zhen, G. Ao, N.J. Alkayed, and J. Cheng Differential mechanisms underlying neuroprotection of hydrogen sulfide donors against oxidative stress Neurochem. Int. 62 8 2013 1072 1078
24. I. Kim, W. Xu, and J.C. Reed Cell death and endoplasmic reticulum stress: disease relevance and therapeutic opportunities Nat. Rev. Drug Discovery 7 12 2008 1013 1030
25. Y. Kong, Y.-J. Fu, Y.-G. Zu, W. Liu, W. Wang, X. Hua, and M. Yang Ethanol modified supercritical fluid extraction and antioxidant activity of cajaninstilbene acid and pinostrobin from pigeonpea [Cajanus cajan (L.) Millsp.] leaves Food Chem. 117 1 2009 152 159
26. M. Kuwabara, T. Asanuma, K. Niwa, and O. Inanami Regulation of cell survival and death signals induced by oxidative stress J. Clin. Biochem. Nutr. 43 2 2008 51 57
27. N. Lassen, W.J. Black, T. Estey, and V. Vasiliou The role of corneal crystallins in the cellular defense mechanisms against oxidative stress Semin. Cell Dev. Biol. 19 2 2008 100 112
28. A.S. Lee The ER chaperone and signaling regulator GRP78/BiP as a monitor of endoplasmic reticulum stress Methods 35 4 2005 373 381
29. A.H. Lee, N.N. Iwakoshi, and L.H. Glimcher XBP-1 regulates a subset of endoplasmic reticulum resident chaperone genes in the unfolded protein response Mol. Cell. Biol. 23 21 2003 7448 7459
30. Y.F. Li, Y.Q. Liu, M. Yang, H.L. Wang, W.C. Huang, Y.M. Zhao, and Z.P. Luo The cytoprotective effect of inulin-type hexasaccharide extracted from Morinda officinalis on PC12 cells against the lesion induced by corticosterone Life Sci. 75 13 2004 1531 1538
31. Z.Y. Li, Z. Guo, Y.M. Liu, X.M. Liu, Q. Chang, Y.H. Liao, and R.L. Pan Neuroprotective effects of total saikosaponins of Bupleurum yinchowense on corticosterone-induced apoptosis in PC12 cells J. Ethnopharmacol. 148 3 2013 794 803
32. B. Li, L. Xiao, Z.Y. Wang, and P.S. Zheng Knockdown of STIM1 inhibits 6-hydroxydopamine-induced oxidative stress through attenuating calcium-dependent ER stress and mitochondrial dysfunction in undifferentiated PC12 cells Free Radical Res. 48 7 2014 758 768
33. L. Liang, M. Luo, Y. Fu, Y. Zu, W. Wang, C. Gu, C. Zhao, C. Li, and T. Efferth Cajaninstilbene acid (CSA) exerts cytoprotective effects against oxidative stress through the Nrf2-dependent antioxidant pathway Toxicol. Lett. 219 3 2013 254 261
34. B. Liu, H. Zhang, C. Xu, G. Yang, J. Tao, J. Huang, J. Wu, X. Duan, Y. Cao, and J. Dong Neuroprotective effects of icariin on corticosterone-induced apoptosis in primary cultured rat hippocampal neurons Brain Res. 1375 2011 59 67
35. Z.W. Liu, H.T. Zhu, K.L. Chen, X. Dong, J. Wei, C. Qiu, and J.H. Xue Protein kinase RNA-like endoplasmic reticulum kinase (PERK) signaling pathway plays a major role in reactive oxygen species (ROS)-mediated endoplasmic reticulum stress-induced apoptosis in diabetic cardiomyopathy Cardiovas. Diabetol. 12 1 2013 158
36. Y.M.J.B. Liu, S.N. Shen, Z. Guo, Z.Y. Li, J.Y. Si, and R.L. Pan Chemical constituents from leaves of Cajanus cajan Chin. Tradit. Herbal Drugs 45 4 2014 466 470
37. Q.-F. Luo, L. Sun, J.-Y. Si, and D.-H. Chen Hypocholesterolemic effect of stilbenes containing extract-fraction from Cajanus cajan L. on diet-induced hypercholesterolemia in mice Phytomedicine 15 11 2008 932 939
38. Y. Ma, and L.M. Hendershot ER chaperone functions during normal and stress conditions J. Chem. Neuroanat. 28 1-2 2004 51 65
39. J.D. Malhotra, and R.J. Kaufman The endoplasmic reticulum and the unfolded protein response Semin. Cell Dev. Biol. 18 6 2007 716 731
40. J.D. Malhotra, and R.J. Kaufman Endoplasmic reticulum stress and oxidative stress: a vicious cycle or a double-edged sword? Antioxid. Redox Signal. 9 12 2007 2277 2293
41. Q.Q. Mao, S.P. Ip, K.M. Ko, S.H. Tsai, M. Zhao, and C.T. Che Peony glycosides protect against corticosterone-induced neurotoxicity in PC12 cells Cell. Mol. Neurobiol. 29 5 2009 643 647
42. S.J. Marciniak, C.Y. Yun, S. Oyadomari, I. Novoa, Y. Zhang, R. Jungreis, K. Nagata, H.P. Harding, and D. Ron CHOP induces death by promoting protein synthesis and oxidation in the stressed endoplasmic reticulum Genes Dev. 18 24 2004 3066 3077
43. A.A. McCracken, and J.L. Brodsky Evolving questions and paradigm shifts in endoplasmic-reticulum-associated degradation (ERAD) Bioessays 25 9 2003 868 877
44. K.D. McCullough, J.L. Martindale, L.O. Klotz, T.Y. Aw, and N.J. Holbrook Gadd153 sensitizes cells to endoplasmic reticulum stress by down-regulating Bcl2 and perturbing the cellular redox state Mol. Cell. Biol. 21 4 2001 1249 1259
45. L.J. McIntosh, and R.M. Sapolsky Glucocorticoids increase the accumulation of reactive oxygen species and enhance adriamycin-induced toxicity in neuronal culture Exp. Neurol. 141 2 1996 201 206
46. L.J.C.K. McIntosh, and R.M. Sapolsky Glucocorticoids may alter antioxidant enzyme capacity in the brain: kainic acid studies Brain Res. 791 1-2 1998 215 222
47. N. Morishima, K. Nakanishi, H. Takenouchi, T. Shibata, and Y. Yasuhiko An endoplasmic reticulum stress-specific caspase cascade in apoptosis. Cytochrome c-independent activation of caspase-9 by caspase-12 J. Biol. Chem. 277 37 2002 34287 34294
48. A.G.P. Munck, and N.J. Holbrook Physiological functions of glucocorticoids in stress and their relation to pharmacological actions Endocr. Rev. 5 1 1984 25 44
49. F. Murray, D.W. Smith, and P.H. Hutson Chronic low dose corticosterone exposure decreased hippocampal cell proliferation, volume and induced anxiety and depression like behaviours in mice Eur. J. Pharmacol. 583 1 2008 115 127
50. S.H. Mustafa Rizvi, A. Parveen, A.K. Verma, I. Ahmad, M. Arshad, and A.A. Mahdi Aluminium induced endoplasmic reticulum stress mediated cell death in SH-SY5Y neuroblastoma cell line is independent of p53 PLoS ONE 9 5 2014 e98409
51. I. Niebroj-Dobosz, D. Dziewulska, and H. Kwiecinski Oxidative damage to proteins in the spinal cord in amyotrophic lateral sclerosis (ALS) Folia Neuropathol. 42 3 2004 151 156
52. A. Nunomura, G. Perry, G. Aliev, K. Hirai, A. Takeda, E.K. Balraj, P.K. Jones, H. Ghanbari, T. Wataya, and S. Shimohama Oxidative damage is the earliest event in Alzheimer disease J. Neuropathol. Exp. Neurol. 60 8 2001 759 767
53. S. Orrenius, B. Zhivotovsky, and P. Nicotera Regulation of cell death: the calcium-apoptosis link Nat. Rev. Mol. Cell Biol. 4 7 2003 552 565
54. R. Ozgur, I. Turkan, B. Uzilday, and A.H. Sekmen Endoplasmic reticulum stress triggers ROS signalling, changes the redox state, and regulates the antioxidant defence of Arabidopsis thaliana J. Exp. Bot. 65 5 2014 1377 1390
55. M.C. Paes, M.B. Oliveira, and P.L. Oliveira Hydrogen peroxide detoxification in the midgut of the blood-sucking insect, Rhodnius prolixus Arch. Insect Biochem. Physiol. 48 2 2001 63 71
56. J.M. Reul, F.R. van den Bosch, and E.R. de Kloet Relative occupation of type-I and type-II corticosteroid receptors in rat brain following stress and dexamethasone treatment: functional implications J. Endocrinol. 115 3 1987 459 467
57. 2+ liaison Sci. STKE 20 215 2004 re1
58. D. Ron, and P. Walter Signal integration in the endoplasmic reticulum unfolded protein response Nat. Rev. Mol. Cell Biol. 8 7 2007 519 529
59. C.J. Ruan, J.Y. Si, L. Zhang, D.H. Chen, G.H. Du, and L. Su Protective effect of stilbenes containing extract-fraction from Cajanus cajan L. on Abeta (25-35)-induced cognitive deficits in mice Neurosci. Lett. 467 2 2009 159 163
60. R. Sano, and J.C. Reed ER stress-induced cell death mechanisms Biochim. Biophys. Acta 1833 12 2013 3460 3470
61. C.X. Santos, L.Y. Tanaka, J. Wosniak, and F.R. Laurindo Mechanisms and implications of reactive oxygen species generation during the unfolded protein response: roles of endoplasmic reticulum oxidoreductases, mitochondrial electron transport, and NADPH oxidase Antioxid. Redox Signal. 11 10 2009 2409 2427
62. R.M. Sapolsky Glucocorticoids and hippocampal atrophy in neuropsychiatric disorders Arch. Gen. Psychiatry 57 10 2000 925 935
63. R.M. Sapolsky, D.R. Packan, and W.W. Vale Glucocorticoid toxicity in the hippocampus: in vitro demonstration Brain Res. 453 1-2 1988 367 371
64. F. Saravia, M. Wallgren, A. Johannisson, J.J. Calvete, L. Sanz, F.J. Pena, J. Roca, and H. Rodriguez-Martinez Exposure to the seminal plasma of different portions of the boar ejaculate modulates the survival of spermatozoa cryopreserved in MiniFlatPacks Theriogenology 71 4 2009 662 675
65. S. Shen, Y. Zhang, R. Zhang, X. Tu, and X. Gong Ursolic acid induces autophagy in U87MG cells via ROS-dependent endoplasmic reticulum stress Chem. Biol. Interact. 218 2014 28 41
66. C. Sidrauski, and P. Walter The transmembrane kinase Ire1p is a site-specific endonuclease that initiates mRNA splicing in the unfolded protein response Cell 90 6 1997 1031 1039
67. N. Wu, Y. Kong, Y. Fu, Y. Zu, Z. Yang, M. Yang, X. Peng, and T. Efferth In vitro antioxidant properties, DNA damage protective activity, and xanthine oxidase inhibitory effect of cajaninstilbene acid, a stilbene compound derived from pigeon pea [Cajanus cajan (L.) Millsp.] leaves J. Agric. Food Chem. 59 1 2011 437 443
68. X.Q. Xiao, N.T. Lee, P.R. Carlier, Y. Pang, and Y.F. Han Bis(7)-tacrine, a promising anti-Alzheimer's agent, reduces hydrogen peroxide-induced injury in rat pheochromocytoma cells: comparison with tacrine Neurosci. Lett. 290 3 2000 197 200
69. Y.P. Yen, K.S. Tsai, Y.W. Chen, C.F. Huang, R.S. Yang, and S.H. Liu Arsenic induces apoptosis in myoblasts through a reactive oxygen species-induced endoplasmic reticulum stress and mitochondrial dysfunction pathway Arch. Toxicol. 86 6 2012 923 933
70. H. Yoshida, T. Okada, K. Haze, H. Yanagi, T. Yura, M. Negishi, and K. Mori ATF6 activated by proteolysis binds in the presence of NF-Y (CBF) directly to the cis-acting element responsible for the mammalian unfolded protein response Mol. Cell. Biol. 20 18 2000 6755 6767
71. H. Yoshida, T. Matsui, A. Yamamoto, T. Okada, and K. Mori XBP1 mRNA is induced by ATF6 and spliced by IRE1 in response to ER stress to produce a highly active transcription factor Cell 107 7 2001 881 891
72. A. Zafir, and N. Banu Induction of oxidative stress by restraint stress and corticosterone treatments in rats Indian J. Biochem. Biophys. 46 1 2009 53 58
73. Z.K. Zeng, Q.Y. Li, X.S. Piao, J.D. Liu, P.F. Zhao, X. Xu, S. Zhang, and S. Niu Forsythia suspensa extract attenuates corticosterone-induced growth inhibition, oxidative injury, and immune depression in broilers Poult. Sci. 2014
74. J.-c. Zhang, L.-w. Wang, J. Sun, S.-x. Wang, S.-g. Shen, H. Chen, and P. Wang Effects of water extract of Cajanus cajan leaves on formation and bone-resorbing activity of osteoclast-like cells Hebei Daxue Xuebao, Ziran Kexueban 29 1 2009 45 50
75. H. Zhang, B. Liu, J. Wu, C. Xu, J. Tao, X. Duan, Y. Cao, and J. Dong Icariin inhibits corticosterone-induced apoptosis in hypothalamic neurons via the PI3-K/Akt signaling pathway Mol. Med. Rep. 6 5 2012 967 972
76. Y. Zhang, L. Zhao, X. Li, Y. Wang, J. Yao, H. Wang, F. Li, Z. Li, and Q. Guo V8, a newly synthetic flavonoid, induces apoptosis through ROS-mediated ER stress pathway in hepatocellular carcinoma Arch. Toxicol. 88 1 2014 97 107
77. J. Zhao, Y. Fu, M. Luo, Y. Zu, W. Wang, C. Zhao, and C. Gu Endophytic fungi from pigeon pea [Cajanus cajan (L.) Millsp.] produce antioxidant cajaninstilbene acid J. Agric. Food Chem. 60 17 2012 4314 4319
78. Y.Y. Zheng, J. Yang, D.H. Chen, and L. Sun Effects of the extracts of Cajanus cajan L. on cell functions in human osteoblast-like TE85 cells and the derivation of osteoclast-like cells Yao Xue Xue Bao 42 4 2007 386 391
79. M. Zheng, C. Liu, F. Pan, D. Shi, F. Ma, Y. Zhang, and Y. Zhang Protective effects of flavonoid extract from Apocynum venetum leaves against corticosterone-induced neurotoxicity in PC12 cells Cell. Mol. Neurobiol. 31 3 2011 421 428
80. H. Zhou, X. Li, and M. Gao Curcumin protects PC12 cells from corticosterone-induced cytotoxicity: possible involvement of the ERK1/2 pathway Basic Clin. Pharmacol. Toxicol. 104 3 2009 236 240
81. Y. Zhou, F. Shu, X. Liang, H. Chang, L. Shi, X. Peng, J. Zhu, and M. Mi Ampelopsin induces cell growth inhibition and apoptosis in breast cancer cells through ROS generation and endoplasmic reticulum stress pathway PLoS ONE 9 2 2014 e89021
82. M.Y. Zhu, W.P. Wang, and G. Bissette Neuroprotective effects of agmatine against cell damage caused by glucocorticoids in cultured rat hippocampal neurons Neuroscience 141 4 2006 2019 2027