Accumulated hippocampal formaldehyde induces age-dependent memory decline

详细信息    查看全文

• 作者：Zhiqian Tong (1)
  Chanshuai Han (1)
  Wenhong Luo (2)
  Xiaohui Wang (4)
  Hui Li (2)
  Hongjun Luo (2)
  Jiangning Zhou (3)
  Jinshun Qi (4)
  Rongqiao He (5) (6)
  
• 关键词：Alzheimer’s disease (AD) ; Aging ; Endogenous formaldehyde ; Long ; term potentiation (LTP) ; Long ; term memory (LTM) ; NMDA receptor
• 刊名：AGE
• 出版年：2013
• 出版时间：June 2013
• 年：2013
• 卷：35
• 期：3
• 页码：583-596
• 全文大小：914KB
• 参考文献：1. Abu-Abeeleh M, Bani Ismail ZA, Alzaben KR, Abu-Halaweh SA, Aloweidi AS, Al-Ammouri IA, Al-Essa MK, Jabaiti SK, Abu-Abeeleh J, Alsmady MM (2010) A preliminary study of the use of human adipose tissue-derived stem cells for the treatment of streptozotocin-induced diabetes mellitus in a rat model. Comp Clin Pathol 19(1):1- CrossRef
  2. Almaguer W, Estupi?án B, Uwe Frey J, Bergado JA (2002) Aging impairs amygdala–hippocampus interactions involved in hippocampal LTP. Neurobiology of aging 23(2):319-24 CrossRef
  3. Amada N, Aihara K, Ravid R, Horie M (2005) Reduction of NR1 and phosphorylated Ca2+/calmodulin-dependent protein kinase II levels in Alzheimer's disease. Neuroreport 16(16):1809 CrossRef
  4. Asaka Y, Jugloff DGM, Zhang L, Eubanks JH, Fitzsimonds RM (2006) Hippocampal synaptic plasticity is impaired in the Mecp2-null mouse model of Rett syndrome. Neurobiol Dis 21(1):217-27 CrossRef
  5. Blevins T, Mirshahi T, Chandler LJ, Woodward JJ (1997) Effects of acute and chronic ethanol exposure on heteromeric / N-methyl-d -aspartate receptors expressed in HEK 293 cells. J Neurochem 69(6):2345-354 CrossRef
  6. Brioni JD, McGaugh JL, Izquierdo I (1989) Amnesia induced by short-term treatment with ethanol: attenuation by pretest oxotremorine. Pharmacol Biochem Behav 33(1):27-9 CrossRef
  7. Burke WJ, McLaughlin JR, Chung HD, Gillespie KN, Grossberg GT, Luque FA, Zimmerman J (1994) Occurrence of cancer in Alzheimer and elderly control patients: an epidemiologic necropsy study. Alzheimer Disease & Associated Disorders 8(1):22 CrossRef
  8. Chapman PF, White GL, Jones MW, Cooper-Blacketer D, Marshall VJ, Irizarry M, Younkin L, Good MA, Bliss T, Hyman BT (1999) Impaired synaptic plasticity and learning in aged amyloid precursor protein transgenic mice. Nat Neurosci 2(3):271-76 CrossRef
  9. Chen K, Maley J, Yu PH (2006) Potential implications of endogenous aldehydes in β-amyloid misfolding, oligomerization and fibrillogenesis. J Neurochem 99(5):1413-424 CrossRef
  10. Chen KL, Wang SSS, Yang YY, Yuan RY, Chen RM, Hu CJ (2009) The epigenetic effects of amyloid-[beta] 1-0 on global DNA and neprilysin genes in murine cerebral endothelial cells. Biochem Biophys Res Commun 378(1):57-1 CrossRef
  11. Cheng L, Yin WJ, Zhang JF, Qi JS (2009) Amyloid beta-protein fragments 25-5 and 31-5 potentiate long-term depression in hippocampal CA1 region of rats in vivo. Synapse 63(3):206-14 CrossRef
  12. Clayton DA, Mesches MH, Alvarez E, Bickford PC, Browning MD (2002) A hippocampal NR2B deficit can mimic age-related changes in long-term potentiation and spatial learning in the Fischer 344 rat. J Neurosci 22(9):3628-637
  13. Connelly CA, Chen LC, Colquhoun SD (2000) Metabolic activity of cultured rat brainstem, hippocampal and spinal cord slices. Journal of neuroscience methods 99(1-):1- CrossRef
  14. Coppedè F (2010) One-carbon metabolism and Alzheimer's disease: focus on epigenetics. Current genomics 11(4):246-60 CrossRef
  15. Cui X (1996) Inhaled formaldehyde on the effects of GSH level and distribution of formaldehyde. China J PrevMed 3:186
  16. Cummings JL (2008) The black book of Alzheimer's disease, part 1. Primary Psychiatry 15(2):66-6
  17. Denk H, Moldeus PW, Schulz RA, Schenkman JB, Keyes SR, Cinti DL (1976) Hepatic organelle interaction. IV. Mechanism of succinate enhancement of formaldehyde accumulation from endoplasmic reticulum N-dealkylations. The Journal of cell biology 69(3):589-98 CrossRef
  18. Dewachter I, Filipkowski R, Priller C, Ris L, Neyton J, Croes S, Terwel D, Gysemans M, Devijver H, Borghgraef P (2009) Deregulation of NMDA-receptor function and down-stream signaling in APP [V717I] transgenic mice. Neurobiology of aging 30(2):241-56 CrossRef
  19. Dildy JE, Leslie SW (1989) Ethanol inhibits NMDA-induced increases in free intracellular Ca2+ in dissociated brain cells. Brain research 499(2):383-87 CrossRef
  20. Drachman DA (2006) Aging of the brain, entropy, and Alzheimer disease. Neurology 67(8):1340-352 CrossRef
  21. Ely J (2001) Mercury induced Alzheimer's disease: accelerating incidence? Bull Environ Contam Toxicol 67(6):800-06
  22. Gaunitz C, Schüttler A, Gillen C, Allgaier C (2002) Formalin-induced changes of NMDA receptor subunit expression in the spinal cord of the rat. Amino Acids 23(1):177-82 CrossRef
  23. Gengler S, Hamilton A, H?lscher C (2010) Synaptic plasticity in the hippocampus of a APP/PS1 mouse model of Alzheimer's disease is impaired in old but not young mice. PLoS One 5(3):e9764 CrossRef
  24. Gr?nvall JLE, Garpenstrand H, Oreland L, Ekblom J (1998) Autoradiographic imaging of formaldehyde adducts in mice: possible relevance for vascular damage in diabetes. Life Sci 63(9):759-68 CrossRef
  25. Gurel A, Coskun O, Armutcu F, Kanter M, Ozen OA (2005) Vitamin E against oxidative damage caused by formaldehyde in frontal cortex and hippocampus: biochemical and histological studies. J Chem Neuroanat 29(3):173-78 CrossRef
  26. Gureviciene I, Ikonen S, Gurevicius K, Sarkaki A, Van Groen T, Pussinen R, Ylinen A, Tanila H (2004) Normal induction but accelerated decay of LTP in APP-?PS1 transgenic mice. Neurobiol Dis 15(2):188-95 CrossRef
  27. He R, Lu J, Miao J (2010) Formaldehyde stress. Science China Life Sciences 53(12):1399-404 CrossRef
  28. Heck HDA, White EL, Casanova-Schmitz M (1982) Determination of formaldehyde in biological tissues by gas chromatography/mass spectrometry. Biological Mass Spectrometry 9(8):347-53 CrossRef
  29. Henniger MSH, Wotjak CT, H?lter SM (2003) Long-term voluntary ethanol drinking increases expression of NMDA receptor 2B subunits in rat frontal cortex. Eur J Pharmacol 470(1-):33-6 CrossRef
  30. Herin GA, Du S, Aizenman E (2001) The neuroprotective agent ebselen modifies NMDA receptor function via the redox modulatory site. J Neurochem 78(6):1307-314 CrossRef
  31. Hynd MR, Scott HL, Dodd PR (2004) Differential expression of / N-methyl-d -aspartate receptor NR2 isoforms in Alzheimer's disease. J Neurochem 90(4):913-19 CrossRef
  32. Kalapos MP (1999) A possible evolutionary role of formaldehyde. Experimental & molecular medicine 31(1):1- CrossRef
  33. Kalász H (2003) Biological role of formaldehyde, and cycles related to methylation, demethylation, and formaldehyde production. Mini reviews in medicinal chemistry 3(3):175-92 CrossRef
  34. Kalluri HSG, Mehta AK, Ticku MK (1998) Up-regulation of NMDA receptor subunits in rat brain following chronic ethanol treatment. Molecular brain research 58(1-):221-24 CrossRef
  35. Kamal A, Biessels GJ, Ramakers GMJ, Hendrik Gispen W (2005) The effect of short duration streptozotocin-induced diabetes mellitus on the late phase and threshold of long-term potentiation induction in the rat. Brain research 1053(1-):126-30 CrossRef
  36. Karuppagounder SS, Pinto JT, Xu H, Chen HL, Beal MF, Gibson GE (2009) Dietary supplementation with resveratrol reduces plaque pathology in a transgenic model of Alzheimer's disease. Neurochem Int 54(2):111-18 CrossRef
  37. Kilburn KH (1994) Neurobehavioral impairment and seizures from formaldehyde. Archives of Environmental Health: An International Journal 49(1):37-4 CrossRef
  38. Kilburn KH, Warshaw R, Thornton JC (1987) Formaldehyde impairs memory, equilibrium, and dexterity in histology technicians: effects which persist for days after exposure. Archives of Environmental Health: An International Journal 42(2):117-20 CrossRef
  39. Kollau A, Hofer A, Russwurm M, Koesling D, Keung WM, Schmidt K, Brunner F, Mayer B (2005) Contribution of aldehyde dehydrogenase to mitochondrial bioactivation of nitroglycerin: evidence for the activation of purified soluble guanylate cyclase through direct formation of nitric oxide. Biochem J 385(Pt 3):769
  40. Lee S, Kim W, Ham BJ, Chen W, Bear MF, Yoon BJ (2008) Activity-dependent NR2B expression is mediated by MeCP2-dependent epigenetic regulation. Biochem Biophys Res Commun 377(3):930-34 CrossRef
  41. Liu L, van Groen T, Kadish I, Tollefsbol TO (2009) DNA methylation impacts on learning and memory in aging. Neurobiology of aging 30(4):549-60 CrossRef
  42. Liu Q, Yang L, Gong C, Tao G, Huang H, Liu J, Zhang H, Wu D, Xia B, Hu G (2011) Effects of long-term low-dose formaldehyde exposure on global genomic hypomethylation in 16HBE cells. Toxicol Lett 205(3):235-40 CrossRef
  43. López-Ramos JC, Jurado-Parras MT, Sanfeliu C, Acu?a-Castroviejo D, Delgado-García JM (2012) Learning capabilities and CA1-prefrontal synaptic plasticity in a mice model of accelerated senescence. Neurobiology of aging 33(3):627, e13-6 CrossRef
  44. Lu J, Miao J, Pan R, He R (2011) Formaldehyde-mediated hyperphosphorylation disturbs the interaction between Tau protein and DNA. Progress in Biochemistry and Biophysics 38(12):1113-120 CrossRef
  45. Luo W, Li H, Zhang Y, Ang CYW (2001) Determination of formaldehyde in blood plasma by high-performance liquid chromatography with fluorescence detection. J Chromatogr B: Biomed Sci Appl 753(2):253-57 CrossRef
  46. Malek FA, M?ritz KU, Fangh?nel J (2003) A study on the effect of inhalative formaldehyde exposure on water labyrinth test performance in rats. Annals of Anatomy-Anatomischer Anzeiger 185(3):277-85 CrossRef
  47. McGahon BM, Martin DSD, Horrobin DF, Lynch MA (1999) Age-related changes in LTP and antioxidant defenses are reversed by an [alpha]-lipoic acid-enriched diet. Neurobiology of aging 20(6):655-64 CrossRef
  48. McKenna JE, Melzack R (2001) Blocking NMDA receptors in the hippocampal dentate gyrus with AP5 produces analgesia in the formalin pain test. Exp Neurol 172(1):92-9 CrossRef
  49. Mesches MH, Gemma C, Veng LM, Allgeier C, Young DA, Browning MD, Bickford PC (2004) Sulindac improves memory and increases NMDA receptor subunits in aged Fischer 344 rats. Neurobiology of aging 25(3):315-24 CrossRef
  50. Metz B, Kersten GFA, Baart GJE, de Jong A, Meiring H, ten Hove J, van Steenbergen MJ, Hennink WE, Crommelin DJA, Jiskoot W (2006) Identification of formaldehyde-induced modifications in proteins: reactions with insulin. Bioconjugate chemistry 17(3):815-22 CrossRef
  51. Mori O, Haseba T, Kameyama K, Shimizu H, Kudoh M, Ohaki Y, Arai Y, Yamazaki M, Asano G (2000) Histological distribution of class III alcohol dehydrogenase in human brain. Brain research 852(1):186-90 CrossRef
  52. Morris R (1984) Developments of a water-maze procedure for studying spatial learning in the rat. Journal of neuroscience methods 11(1):47-0 CrossRef
  53. Nakazawa K, McHugh TJ, Wilson MA, Tonegawa S (2004) NMDA receptors, place cells and hippocampal spatial memory. Nat Rev Neurosci 5(5):361-72 CrossRef
  54. Nie C, Wang X, Liu Y, Perrett S, He R (2007a) Amyloid-like aggregates of neuronal tau induced by formaldehyde promote apoptosis of neuronal cells. BMC Neurosci 8(1):9 CrossRef
  55. Nie C, Wei Y, Chen X, Liu Y, Dui W, Liu Y, Davies MC, Tendler SJB, He R (2007b) Formaldehyde at low concentration induces protein tau into globular amyloid-like aggregates in vitro and in vivo. PLoS One 2(7):e629 CrossRef
  56. Ohsawa I, Nishimaki K, Murakami Y, Suzuki Y, Ishikawa M, Ohta S (2008) Age-dependent neurodegeneration accompanying memory loss in transgenic mice defective in mitochondrial aldehyde dehydrogenase 2 activity. J Neurosci 28(24):6239-249 CrossRef
  57. Patra SK, Patra A, Rizzi F, Ghosh TC, Bettuzzi S (2008) Demethylation of (Cytosine-5-C-methyl) DNA and regulation of transcription in the epigenetic pathways of cancer development. Cancer Metastasis Rev 27(2):315-34 CrossRef
  58. Perna RB, Bordini EJ, Deinzer-Lifrak M (2001) A case of claimed persistent neuropsychological sequelae of chronic formaldehyde exposure: clinical, psychometric, and functional findings. Arch Clin Neuropsychol 16(1):33-4
  59. Reisi P, Alaei H, Babri S, Sharifi MR, Mohaddes G (2009) Effects of treadmill running on spatial learning and memory in streptozotocin-induced diabetic rats. Neurosci Lett 455(2):79-3 CrossRef
  60. Reisi P, Babri S, Alaei H, Sharifi MR, Mohaddes G, Noorbakhsh SM, Lashgari R (2010) Treadmill running improves long-term potentiation (LTP) defects in streptozotocin-induced diabetes at dentate gyrus in rats. Pathophysiology 17(1):33-8 CrossRef
  61. Retfalvi T, Nemeth Z, Sarudi I, Albert L (1998) Alteration of endogenous formaldehyde level following mercury accumulation in different pig tissues. Acta biologica Hungarica 49(2-):375
  62. Rondi-Reig L, Petit GH, Tobin C, Tonegawa S, Mariani J, Berthoz A (2006) Impaired Sequential egocentric and allocentric memories in forebrain-specific-NMDA receptor knock-out mice during a new task dissociating strategies of navigation. J Neurosci 26(15):4071-081 CrossRef
  63. Shcherbakova L, Tel'Pukhov V, Trenin S, Bashilov I, Lapkina T (1986) Permeability of the blood–brain barrier to intra-arterial formaldehyde. Biull Eksp Biol Med 102(11):573-75
  64. Song MS, Baker GB, Dursun SM, Todd KG (2010) The antidepressant phenelzine protects neurons and astrocytes against formaldehyde-induced toxicity. J Neurochem 114(5):1405-413
  65. Sun AY, Wang Q, Simonyi A, Sun GY (2010) Resveratrol as a therapeutic agent for neurodegenerative diseases. Mol Neurobiol 41(2):375-83 CrossRef
  66. Szende B, Tyihák E, Trézl L, Sz?ke E, László I, Kátay G, Király-Véghely Z (1998) Formaldehyde generators and capturers as influencing factors of mitotic and apoptotic processes. Acta biologica Hungarica 49(2-):323
  67. Tang YP, Shimizu E, Dube GR, Rampon C, Kerchner GA, Zhuo M, Liu G, Tsien JZ (1999) Genetic enhancement of learning and memory in mice. Nature 401(6748):63-9 CrossRef
  68. Teng S, Beard K, Pourahmad J, Moridani M, Easson E, Poon R, O'Brien PJ (2001) The formaldehyde metabolic detoxification enzyme systems and molecular cytotoxic mechanism in isolated rat hepatocytes. Chemico-Biological Interactions 130:285-96 CrossRef
  69. Toews J, Rogalski JC, Clark TJ, Kast J (2008) Mass spectrometric identification of formaldehyde-induced peptide modifications under in vivo protein cross-linking conditions. Anal Chim Acta 618(2):168-83 CrossRef
  70. Tokuda K, Zorumski CF, Izumi Y (2007) Modulation of hippocampal long-term potentiation by slow increases in ethanol concentration. Neuroscience 146(1):340-49 CrossRef
  71. Tong Z, Luo W, Wang Y, Yang F, Han Y, Li H, Luo H, Duan B, Xu T, Maoying Q (2010) Tumor tissue-derived formaldehyde and acidic microenvironment synergistically induce bone cancer pain. PLoS One 5(4):e10234 CrossRef
  72. Tong Z, Zhang J, Luo W, Wang W, Li F, Li H, Luo H, Lu J, Zhou J, Wan Y, He R (2011) Urine formaldehyde level is inversely correlated to mini mental state examination scores in senile dementia. Neurobiology of aging 32(1):31-1 CrossRef
  73. Trézl L, Csiba A, Juhasz S, Szentgy?rgyi M, Lombai G, Hullán L, Juhász A (1997) Endogenous formaldehyde level of foods and its biological significance. Zeitschrift für Lebensmitteluntersuchung und -Forschung A 205(4):300-04 CrossRef
  74. Tyihák E, Albert L, Németh ZI, Kátay G, Király-Véghely Z, Szende B (1998) Formaldehyde cycle and the natural formaldehyde generators and capturers. Acta biologica Hungarica 49(2-):225-38
  75. Wang RS, Nakajima T, Kawamoto T, Honma T (2002) Effects of aldehyde dehydrogenase-2 genetic polymorphisms on metabolism of structurally different aldehydes in human liver. Drug metabolism and disposition 30(1):69-3 CrossRef
  76. Wang B, Wang J, Zhou S, Tan S, He X, Yang Z, Xie YC, Li S, Zheng C, Ma X (2008) The association of mitochondrial aldehyde dehydrogenase gene (ALDH2) polymorphism with susceptibility to late-onset Alzheimer's disease in Chinese. J Neurol Sci 268(1-):172-75 CrossRef
  77. Wirkner K, Poelchen W, K?les L, Mühlberg K, Scheibler P, Allgaier C, Illes P (1999) Ethanol-induced inhibition of NMDA receptor channels. Neurochem Int 35(2):153-62 CrossRef
  78. Wu SC, Zhang Y (2010) Active DNA demethylation: many roads lead to Rome. Nat Rev Mol Cell Biol 11(9):607-20 CrossRef
  79. Zhang JF, Qi JS, Qiao JT (2009) Protein kinase C mediates amyloid [beta]-protein fragment 31-35-induced suppression of hippocampal late-phase long-term potentiation in vivo. Neurobiol Learn Mem 91(3):226-34 CrossRef
  80. Zhu Y, Carvey PM, Ling Z (2006) Age-related changes in glutathione and glutathione-related enzymes in rat brain. Brain research 1090(1):35-4 CrossRef
  
• 作者单位：Zhiqian Tong (1)
  Chanshuai Han (1)
  Wenhong Luo (2)
  Xiaohui Wang (4)
  Hui Li (2)
  Hongjun Luo (2)
  Jiangning Zhou (3)
  Jinshun Qi (4)
  Rongqiao He (5) (6)
  
  1. State Key Laboratory of Brain and Cognitive Sciences, Institute of Biophysics, Chinese Academy of Sciences, Graduate University of the Chinese Academy of Sciences, Beijing, 100101, China
  2. Central Laboratory, Shantou University Medical College, Guangdong, 515041, China
  4. Department of Neurobiology and National Key Discipline of Physiology, Shanxi Medical University, Taiyuan, 030001, China
  3. University of Science and Technology of China, Anhui, 230026, China
  5. State Key Laboratory of Brain and Cognitive Sciences, Institute of Biophysics, Chinese Academy of Sciences, Beijing, 100101, China
  6. Key Lab of Mental Health, Institute of Psychology, Chinese Academy of Sciences, Beijing, 100101, China
  
• ISSN：1574-4647

文摘

Aging is an important factor in memory decline in aged animals and humans and in Alzheimer’s disease and is associated with the impairment of hippocampal long-term potentiation (LTP) and down-regulation of NR1/NR2B expression. Gaseous formaldehyde exposure is known to induce animal memory loss and human cognitive decline; however, it is unclear whether the concentrations of endogenous formaldehyde are elevated in the hippocampus and how excess formaldehyde affects LTP and memory formation during the aging process. In the present study, we report that hippocampal formaldehyde accumulated in memory-deteriorating diseases such as age-related dementia. Spatial memory performance was gradually impaired in normal Sprague–Dawley rats by persistent intraperitoneal injection with formaldehyde. Furthermore, excess formaldehyde treatment suppressed the hippocampal LTP formation by blocking N-methyl-d-aspartate (NMDA) receptor. Chronic excess formaldehyde treatment over a period of 30?days markedly decreased the viability of the hippocampus and down-regulated the expression of the NR1 and NR2B subunits of the NMDA receptor. Our results indicate that excess endogenous formaldehyde is a critical factor in memory loss in age-related memory-deteriorating diseases.