AMPK activation prevents prenatal stress-induced cognitive impairment: Modulation of mitochondrial content and oxidative stress

Free Radical Biology and Medicine

Volumn 75, Issue , 2014, Pages 156-166

  Cao, Ke ^a   Zheng, Adi ^a   Xu, Jie ^a   Li, Hao ^a   Liu, Jing ^a   Peng, Yunhua ^a   Long, Jiangang ^a   Zou, Xuan ^a   Li, Yuan ^a   Chen, Cong ^a   Liu, Jiankang ^a   Feng, Zhihui ^a  

^a XI'AN JIAOTONG UNIVERSITY   (China)

Author keywords

AMPK; Cognitive function; Mitochondrial biogenesis; Oxidative stress; Prenatal stress; Resveratrol

Indexed keywords

COMPOUND C; CYTOCHROME C OXIDASE; GLUTATHIONE; GLUTATHIONE DISULFIDE; HYDROXYMETHYLGLUTARYL COENZYME A REDUCTASE KINASE; HYDROXYMETHYLGLUTARYL COENZYME A REDUCTASE KINASE ACTIVATOR; MESSENGER RNA; MITOCHONDRIAL DNA; NEUROTROPHIC FACTOR; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE DEHYDROGENASE (UBIQUINONE); RESVERATROL; TRANSCRIPTION FACTOR NRF2; UNCLASSIFIED DRUG; ANTIOXIDANT; NFE2L2 PROTEIN, HUMAN; STILBENE DERIVATIVE;

ADULT; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIOXIDANT ACTIVITY; ARTICLE; BIOGENESIS; BRAIN MITOCHONDRION; BRAIN NERVE CELL; COGNITION; COGNITIVE DEFECT; CONCENTRATION RESPONSE; CONTROLLED STUDY; DIET SUPPLEMENTATION; DISEASE MODEL; ENZYME ACTIVATION; ENZYME INDUCTION; FEMALE; HIPPOCAMPUS; HUMAN; HUMAN CELL; IMMOBILIZATION STRESS; MALE; MENTAL PERFORMANCE; MORRIS WATER MAZE TEST; NEUROMODULATION; NEUROPROTECTION; NONHUMAN; OXIDATION; OXIDATIVE STRESS; PRENATAL STRESS; PRIORITY JOURNAL; PROGENY; RAT; SIGNAL TRANSDUCTION; ANIMAL; ANTAGONISTS AND INHIBITORS; CELL LINE; DRUG EFFECTS; ENZYMOLOGY; MENTAL STRESS; METABOLISM; MILD COGNITIVE IMPAIRMENT; MITOCHONDRION; OXIDATION REDUCTION REACTION; PHYSIOLOGY; PREGNANCY; PSYCHOLOGY; SPRAGUE DAWLEY RAT;

AMP-ACTIVATED PROTEIN KINASES; ANIMALS; ANTIOXIDANTS; CELL LINE; COGNITION; ENZYME ACTIVATION; FEMALE; GLUTATHIONE; HIPPOCAMPUS; HUMANS; MALE; MILD COGNITIVE IMPAIRMENT; MITOCHONDRIA; NF-E2-RELATED FACTOR 2; OXIDATION-REDUCTION; OXIDATIVE STRESS; PREGNANCY; RATS; RATS, SPRAGUE-DAWLEY; STILBENES; STRESS, PSYCHOLOGICAL;

EID: 84906668749     PISSN: 08915849     EISSN: 18734596     Source Type: Journal    
DOI: 10.1016/j.freeradbiomed.2014.07.029     Document Type: Article

References (41)

1. M. Weinstock Alterations induced by gestational stress in brain morphology and behaviour of the offspring Prog. Neurobiol. 65 2001 427 451 (Pubitemid 33016408)
2. T.G. O'Connor, J. Heron, J. Golding, and V. Glover Maternal antenatal anxiety and behavioural/emotional problems in children: a test of a programming hypothesis J. Child Psychol. Psychiatry 44 2003 1025 1036 (Pubitemid 37254145)
3. H. Beydoun, and A.F. Saftlas Physical and mental health outcomes of prenatal maternal stress in human and animal studies: a review of recent evidence Paediatr. Perinat. Epidemiol. 22 2008 438 466
4. C. Bustamante, P. Bilbao, W. Contreras, M. Martinez, A. Mendoza, A. Reyes, and R. Pascual Effects of prenatal stress and exercise on dentate granule cells maturation and spatial memory in adolescent mice Int. J. Dev. Neurosci. 28 2010 605 609
5. V. Lemaire, M. Koehl, M. Le Moal, and D.N. Abrous Prenatal stress produces learning deficits associated with an inhibition of neurogenesis in the hippocampus Proc. Natl. Acad. Sci. USA 97 2000 11032 11037
6. A.R. Zuena, J. Mairesse, P. Casolini, C. Cinque, G.S. Alema, S. Morley-Fletcher, V. Chiodi, L.G. Spagnoli, R. Gradini, A. Catalani, F. Nicoletti, and S. Maccari Prenatal restraint stress generates two distinct behavioral and neurochemical profiles in male and female rats PLoS One 3 2008 e2170
7. Z. Zhu, X. Li, W. Chen, Y. Zhao, H. Li, C. Qing, N. Jia, Z. Bai, and J. Liu Prenatal stress causes gender-dependent neuronal loss and oxidative stress in rat hippocampus J. Neurosci. Res. 78 2004 837 844 (Pubitemid 39657571)
8. Z. Feng, X. Zou, H. Jia, X. Li, Z. Zhu, X. Liu, P. Bucheli, O. Ballevre, Y. Hou, W. Zhang, J. Wang, Y. Chen, and J. Liu Maternal docosahexaenoic acid feeding protects against impairment of learning and memory and oxidative stress in prenatally stressed rats: possible role of neuronal mitochondria metabolism Antioxid. Redox Signal. 16 2012 275 289
9. J. Ye, and J.N. Keller Regulation of energy metabolism by inflammation: a feedback response in obesity and calorie restriction Aging (Albany NY) 2 2010 361 368
10. J.H. Kim, J.O. Lee, S.K. Lee, N. Kim, G.Y. You, J.W. Moon, J. Sha, S.J. Kim, S.H. Park, and H.S. Kim Celastrol suppresses breast cancer MCF-7 cell viability via the AMP-activated protein kinase (AMPK)-induced p53-polo like kinase 2 (PLK-2) pathway Cell Signal. 25 2013 805 813
11. Y.Y. Li, L.F. Yu, L.N. Zhang, B.Y. Qiu, M.B. Su, F. Wu, D.K. Chen, T. Pang, M. Gu, W. Zhang, W.P. Ma, H.W. Jiang, J.Y. Li, F.J. Nan, and J. Li Novel small-molecule AMPK activator orally exerts beneficial effects on diabetic db/db mice Toxicol. Appl. Pharmacol. 273 2013 325 334
12. H. Sasaki, H. Asanuma, M. Fujita, H. Takahama, M. Wakeno, S. Ito, A. Ogai, M. Asakura, J. Kim, T. Minamino, S. Takashima, S. Sanada, M. Sugimachi, K. Komamura, N. Mochizuki, and M. Kitakaze Metformin prevents progression of heart failure in dogs: role of AMP-activated protein kinase Circulation 119 2009 2568 2577
13. Y.J. Park, J.W. Ko, Y. Jang, and Y.H. Kwon Activation of AMP-activated protein kinase alleviates homocysteine-mediated neurotoxicity in SH-SY5Y cells Neurochem. Res. 38 2013 1561 1571
14. F. Liu, S.E. Benashski, R. Persky, Y. Xu, J. Li, and L.D. McCullough Age-related changes in AMP-activated protein kinase after stroke Age (Dordr.) 34 2012 157 168
15. L. Yu, and S.J. Yang AMP-activated protein kinase mediates activity-dependent regulation of peroxisome proliferator-activated receptor gamma coactivator-1alpha and nuclear respiratory factor 1 expression in rat visual cortical neurons Neuroscience 169 2010 23 38
16. E.E. Vomhof-Dekrey, and M.J. Picklo Sr. The Nrf2-antioxidant response element pathway: a target for regulating energy metabolism J. Nutr. Biochem. 23 2012 1201 1206
17. B. Onken, and M. Driscoll Metformin induces a dietary restriction-like state and the oxidative stress response to extend C. elegans health span via AMPK, LKB1, and SKN-1 PLoS One 5 2010 e8758
18. X.M. Liu, K.J. Peyton, A.R. Shebib, H. Wang, R.J. Korthuis, and W. Durante Activation of AMPK stimulates heme oxygenase-1 gene expression and human endothelial cell survival Am. J. Physiol. Heart Circ. Physiol 300 2011 H84 H93
19. C. Mo, L. Wang, J. Zhang, S. Numazawa, H. Tang, X. Tang, X. Han, J. Li, M. Yang, Z. Wang, D. Wei, and H. Xiao The crosstalk between Nrf2 and AMPK signal pathways is important for the anti-inflammatory effect of berberine in LPS-stimulated macrophages and endotoxin-shocked mice Antioxid. Redox Signal. 20 2014 574 588
20. M.Y. Kim, J.H. Lim, H.H. Youn, Y.A. Hong, K.S. Yang, H.S. Park, S. Chung, S.H. Ko, S.J. Shin, B.S. Choi, H.W. Kim, Y.S. Kim, J.H. Lee, Y.S. Chang, and C.W. Park Resveratrol prevents renal lipotoxicity and inhibits mesangial cell glucotoxicity in a manner dependent on the AMPK-SIRT1-PGC1alpha axis in db/db mice Diabetologia 56 2013 204 217
21. D.V. Tillu, O.K. Melemedjian, M.N. Asiedu, N. Qu, M. De Felice, G. Dussor, and T.J. Price Resveratrol engages AMPK to attenuate ERK and mTOR signaling in sensory neurons and inhibits incision-induced acute and chronic pain Mol. Pain 8 2012 5
22. S.S. Sahu, S. Madhyastha, and G.M. Rao Neuroprotective effect of resveratrol against prenatal stress induced cognitive impairment and possible involvement of Na(+), K(+)-ATPase activity Pharmacol. Biochem. Behav. 103 2013 520 525
23. S. Madhyastha, S. Sekhar, and G. Rao Resveratrol improves postnatal hippocampal neurogenesis and brain derived neurotrophic factor in prenatally stressed rats Int. J. Dev. Neurosci. 31 2013 580 585
24. S. Madhyastha, S.S. Sahu, and G. Rao Resveratrol for prenatal-stress- induced oxidative damage in growing brain and its consequences on survival of neurons J. Basic Clin. Physiol. Pharmacol. 2013 1 10
25. R.M. Deacon, and J.N. P. Rawlins T-maze alternation in the rodent Nat. Protoc. 1 2006 7 12
26. F. Fernandez, W. Morishita, E. Zuniga, J. Nguyen, M. Blank, R.C. Malenka, and C.C. Garner Pharmacotherapy for cognitive impairment in a mouse model of Down syndrome Nat. Neurosci. 10 2007 411 413 (Pubitemid 46494581)
27. M. Gué, A. Bravard, J. Meunier, R. Veyrier, S. Gaillet, M. Recasens, and T. Maurice Sex differences in learning deficits induced by prenatal stress in juvenile rats Behav. Brain Res. 150 2004 149 157 (Pubitemid 38368966)
28. A.S. Paintlia, M.K. Paintlia, S. Mohan, A.K. Singh, and I. Singh AMP-activated protein kinase signaling protects oligodendrocytes that restore central nervous system functions in an experimental autoimmune encephalomyelitis model Am. J. Pathol. 183 2013 526 541
29. C. Frosig, T.E. Jensen, J. Jeppesen, C. Pehmoller, J.T. Treebak, S.J. Maarbjerg, J.M. Kristensen, L. Sylow, T.J. Alsted, P. Schjerling, B. Kiens, J.F. Wojtaszewski, and E.A. Richter AMPK and insulin action - responses to ageing and high fat diet PLoS One 8 2013 e62338
30. N.A. Bishop, T. Lu, and B.A. Yankner Neural mechanisms of ageing and cognitive decline Nature 464 2010 529 535
31. G.E. Gibson, A. Starkov, J.P. Blass, R.R. Ratan, and M.F. Beal Cause and consequence: mitochondrial dysfunction initiates and propagates neuronal dysfunction, neuronal death and behavioral abnormalities in age-associated neurodegenerative diseases Biochim. Biophys. Acta 1802 2010 122 134
32. J. Liu, E. Head, A.M. Gharib, W. Yuan, R.T. Ingersoll, T.M. Hagen, C.W. Cotman, and B.N. Ames Memory loss in old rats is associated with brain mitochondrial decay and RNA/DNA oxidation: partial reversal by feeding acetyl-L-carnitine and/or R-alpha -lipoic acid Proc. Natl. Acad. Sci. USA 99 2002 2356 2361 (Pubitemid 34169065)
33. Z. Feng, H. Jia, X. Li, Z. Bai, Z. Liu, L. Sun, Z. Zhu, P. Bucheli, O. Ballevre, J. Wang, and J. Liu A milk-based wolfberry preparation prevents prenatal stress-induced cognitive impairment of offspring rats, and inhibits oxidative damage and mitochondrial dysfunction in vitro Neurochem. Res. 35 2010 702 711
34. J. Zhu, K.Z. Wang, and C.T. Chu After the banquet: mitochondrial biogenesis, mitophagy, and cell survival Autophagy 9 2013 1663 1676
35. D.W. Kim, Y.M. Kim, S.D. Kang, Y.M. Han, and H.O. Pae Effects of resveratrol and trans-3,5,4′-trimethoxystilbene on glutamate-induced cytotoxicity, heme oxygenase-1, and sirtuin 1 in HT22 neuronal cells Biomol. Ther. (Seoul) 20 2012 306 312
36. Y. Son, S.J. Byun, and H.O. Pae Involvement of heme oxygenase-1 expression in neuroprotection by piceatannol, a natural analog and a metabolite of resveratrol, against glutamate-mediated oxidative injury in HT22 neuronal cells Amino Acids 45 2013 393 401
37. J. Ren, C. Fan, N. Chen, J. Huang, and Q. Yang Resveratrol pretreatment attenuates cerebral ischemic injury by upregulating expression of transcription factor Nrf2 and HO-1 in rats Neurochem. Res. 36 2011 2352 2362
38. C. Sims-Robinson, J. Hur, J.M. Hayes, J.R. Dauch, P.J. Keller, S.V. Brooks, and E.L. Feldman The role of oxidative stress in nervous system aging PLoS One 8 2013 e68011
39. A. Yavari, and G.I. Azizova Effect of oxidative stress on immunological parameters in type 2 diabetes mellitus in the Azerbaijan Republic Diabetes Metab. Syndr 6 2012 195 198
40. S. Suzuki, C.M. Brown, C.D. Dela Cruz, E. Yang, D.A. Bridwell, and P.M. Wise Timing of estrogen therapy after ovariectomy dictates the efficacy of its neuroprotective and antiinflammatory actions Proc. Natl. Acad. Sci. USA 104 2007 6013 6018 (Pubitemid 47175650)
41. M. Gulinello, D. Lebesgue, T. Jover-Mengual, R.S. Zukin, and A.M. Etgen Acute and chronic estradiol treatments reduce memory deficits induced by transient global ischemia in female rats Horm. Behav. 49 2006 246 260 (Pubitemid 43152499)