DNA methylation profiling in the thalamus and hippocampus of postnatal malnourished mice, including effects related to long-term potentiation

详细信息    查看全文

• 作者：Xiaoling Weng (1)
  Daizhan Zhou (2)
  Fatao Liu (3)
  Hong Zhang (1)
  Junyi Ye (1)
  Zhou Zhang (2)
  Di Zhang (2)
  Yinan Wang (2)
  Liming Tao (3)
  Lan Cao (1)
  Mengyuan Kan (3)
  Ting Wang (3)
  Guoyin Feng (2) (3)
  Xiaolan Qin (2)
  Jihui Sun (4)
  Lin He (1) (2) (3) (6)
  Yun Liu (1) (5)
  
• 关键词：Malnutrition ; Thalamus ; Hippocampus ; Mouse model ; Global DNA methylation status ; Whole genome methylation sequencing ; Long ; term potentiation ; Psychiatric disorders
• 刊名：BMC Neuroscience
• 出版年：2014
• 出版时间：December 2014
• 年：2014
• 卷：15
• 期：1
• 全文大小：294 KB
• 参考文献：1. Alamy M, Bengelloun WA: Malnutrition and brain development: an analysis of the effects of inadequate diet during different stages of life in rat. / Neurosci Biobehav Rev 2012,36(6):1463-480. CrossRef
  2. Morgane PJ, Austin-LaFrance R, Bronzino J, Tonkiss J, Diaz-Cintra S, Cintra L, Kemper T, Galler JR: Prenatal malnutrition and development of the brain. / Neurosci Biobehav Rev 1993,17(1):91-28. CrossRef
  3. Black RE, Allen LH, Bhutta ZA, Caulfield LE, de Onis M, Ezzati M, Mathers C, Rivera J: Maternal and child undernutrition: global and regional exposures and health consequences. / Lancet 2008,371(9608):243-60. CrossRef
  4. Bergman Y, Cedar H: DNA methylation dynamics in health and disease. / Nat Struct Mol Biol 2013,20(3):274-81. CrossRef
  5. Weber M, Hellmann I, Stadler MB, Ramos L, Paabo S, Rebhan M, Schubeler D: Distribution, silencing potential and evolutionary impact of promoter DNA methylation in the human genome. / Nat Genet 2007,39(4):457-66. CrossRef
  6. Niwa M, Jaaro-Peled H, Tankou S, Seshadri S, Hikida T, Matsumoto Y, Cascella NG, Kano S, Ozaki N, Nabeshima T, Sawa A: Adolescent stress-induced epigenetic control of dopaminergic neurons via glucocorticoids. / Science 2013,339(6117):335-39. CrossRef
  7. Ball MP, Li JB, Gao Y, Lee JH, LeProust EM, Park IH, Xie B, Daley GQ, Church GM: Targeted and genome-scale strategies reveal gene-body methylation signatures in human cells. / Nat Biotechnol 2009,27(4):361-68. CrossRef
  8. Guo JU, Ma DK, Mo H, Ball MP, Jang MH, Bonaguidi MA, Balazer JA, Eaves HL, Xie B, Ford E, Zhang K, Ming GL, Gao Y, Song H: Neuronal activity modifies the DNA methylation landscape in the adult brain. / Nature neuroscience 2011,14(10):1345-351. CrossRef
  9. Gabory A, Attig L, Junien C: Developmental programming and epigenetics. / Am J Clin Nutr 2011,94(6 Suppl):1943S-1952S. CrossRef
  10. Shen Q, Li X, Qiu Y, Su M, Liu Y, Li H, Wang X, Zou X, Yan C, Yu L, Li S, Wan C, He L, Jia W: Metabonomic and metallomic profiling in the amniotic fluid of malnourished pregnant rats. / Journal of proteome research 2008,7(5):2151-157. CrossRef
  11. da Huang W, Sherman BT, Lempicki RA: Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources. / Nat Protoc 2009,4(1):44-7. CrossRef
  12. Jones PA: Functions of DNA methylation: islands, start sites, gene bodies and beyond. / Nat Rev Genet 2012,13(7):484-92. CrossRef
  13. Bird A: DNA methylation patterns and epigenetic memory. / Genes Dev 2002,16(1):6-1.
  14. Suzuki MM, Bird A: DNA methylation landscapes: provocative insights from epigenomics. / Nat Rev Genet 2008,9(6):465-76. CrossRef
  15. Holliday R: The inheritance of epigenetic defects. / Science 1987,238(4824):163-70. CrossRef
  16. Fox MD, Raichle ME: Spontaneous fluctuations in brain activity observed with functional magnetic resonance imaging. / Nat Rev Neurosci 2007,8(9):700-11. CrossRef
  17. Yasuda H, Barth AL, Stellwagen D, Malenka RC: A developmental switch in the signaling cascades for LTP induction. / Nat Neurosci 2003,6(1):15-6.
  18. Borgesius NZ, van Woerden GM, Buitendijk GH, Keijzer N, Jaarsma D, Hoogenraad CC, Elgersma Y: betaCaMKII plays a nonenzymatic role in hippocampal synaptic plasticity and learning by targeting alphaCaMKII to synapses. / J Neurosci 2011,31(28):10141-0148. CrossRef
  19. Chiocco MJ, Zhu X, Walther D, Pletnikova O, Troncoso JC, Uhl GR, Liu QR: Fine mapping of calcineurin (PPP3CA) gene reveals novel alternative splicing patterns, association of 5′UTR trinucleotide repeat with addiction vulnerability, and differential isoform expression in Alzheimer’s disease. / Subst Use Misuse 2010,45(11):1809-826. CrossRef
  20. Lloret A, Badia MC, Giraldo E, Ermak G, Alonso MD, Pallardo FV, Davies KJ, Vina J: Amyloid-beta toxicity and tau hyperphosphorylation are linked via RCAN1 in Alzheimer’s disease. / J Alzheimers Dis 2011,27(4):701-09.
  21. Vazquez-Higuera JL, Mateo I, Sanchez-Juan P, Rodriguez-Rodriguez E, Pozueta A, Calero M, Dobato JL, Frank-Garcia A, Valdivieso F, Berciano J, Bullido MJ, Combarros O: Genetic variation in the tau kinases pathway may modify the risk and age at onset of Alzheimer's disease. / Journal of Alzheimer's disease : JAD 2011,27(2):291-97.
  22. Girirajan S, Dennis MY, Baker C, Malig M, Coe BP, Campbell CD, Mark K, Vu TH, Alkan C, Cheng Z, Biesecker LG, Bernier R, Eichler EE: Refinement and discovery of new hotspots of copy-number variation associated with autism spectrum disorder. / American journal of human genetics 2013,92(2):221-37. CrossRef
  23. Lo Vasco VR, Cardinale G, Polonia P: Deletion of PLCB1 gene in schizophrenia-affected patients. / J Cell Mol Med 2012,16(4):844-51. CrossRef
  24. Moskvina V, Craddock N, Holmans P, Nikolov I, Pahwa JS, Green E, Owen MJ, O’Donovan MC: Gene-wide analyses of genome-wide association data sets: evidence for multiple common risk alleles for schizophrenia and bipolar disorder and for overlap in genetic risk. / Mol Psychiatry 2009,14(3):252-60. CrossRef
  25. Smoller JW, Craddock N, Kendler K, Lee PH, Neale BM, Nurnberger JI, Ripke S, Santangelo S, Sullivan PF: Identification of risk loci with shared effects on five major psychiatric disorders: a genome-wide analysis. / Lancet 2013,381(9875):1371-379. CrossRef
  26. Schizophrenia Psychiatric Genome-Wide Association Study C: Genome-wide association study identifies five new schizophrenia loci. / Nat Genet 2011,43(10):969-76. CrossRef
  27. Hamshere ML, Walters JT, Smith R, Richards AL, Green E, Grozeva D, Jones I, Forty L, Jones L, Gordon-Smith K, Riley B, O'Neill FA, Kendler KS, Sklar P, Purcell S, Kranz J, Morris D, Gill M, Holmans P, Craddock N, Corvin A, Owen MJ, O'Donovan MC, Schizophrenia Psychiatric Genome-wide Association Study Consortium: Genome-wide significant associations in schizophrenia to ITIH3/4, CACNA1C and SDCCAG8, and extensive replication of associations reported by the Schizophrenia PGC. / Molecular psychiatry 2013,18(6):708-12. CrossRef
  28. Nyegaard M, Demontis D, Foldager L, Hedemand A, Flint TJ, Sorensen KM, Andersen PS, Nordentoft M, Werge T, Pedersen CB, Hougaard DM, Mortensen PB, Mors O, Borglum AD: CACNA1C (rs1006737) is associated with schizophrenia. / Molecular psychiatry 2010,15(2):119-21. CrossRef
  29. Ferreira MA, O'Donovan MC, Meng YA, Jones IR, Ruderfer DM, Jones L, Fan J, Kirov G, Perlis RH, Green EK, Smoller JW, Grozeva D, Stone J, Nikolov I, Chambert K, Hamshere ML, Nimgaonkar VL, Moskvina V, Thase ME, Caesar S, Sachs GS, Franklin J, Gordon-Smith K, Ardlie KG, Gabriel SB, Fraser C, Blumenstiel B, Defelice M, Breen G, Gill M, / et al.: Collaborative genome-wide association analysis supports a role for ANK3 and CACNA1C in bipolar disorder. / Nature genetics 2008,40(9):1056-058. CrossRef
  30. Sklar P, Smoller JW, Fan J, Ferreira MA, Perlis RH, Chambert K, Nimgaonkar VL, McQueen MB, Faraone SV, Kirby A, de Bakker PI, Ogdie MN, Thase ME, Sachs GS, Todd-Brown K, Gabriel SB, Sougnez C, Gates C, Blumenstiel B, Defelice M, Ardlie KG, Franklin J, Muir WJ, McGhee KA, MacIntyre DJ, McLean A, VanBeck M, McQuillin A, Bass NJ, Robinson M, / et al.: Whole-genome association study of bipolar disorder. / Molecular psychiatry 2008,13(6):558-69. CrossRef
  31. Jogia J, Ruberto G, Lelli-Chiesa G, Vassos E, Maieru M, Tatarelli R, Girardi P, Collier D, Frangou S: The impact of the CACNA1C gene polymorphism on frontolimbic function in bipolar disorder. / Mol Psychiatry 2011,16(11):1070-071. CrossRef
  32. Simons CJ, van Winkel R: Intermediate Phenotype Analysis of Patients, Unaffected Siblings, and Healthy Controls Identifies VMAT2 as a Candidate Gene for Psychotic Disorder and Neurocognition. / Schizophr bulletin 2013,39(4):848-56. CrossRef
  33. Villemagne VL, Okamura N, Pejoska S, Drago J, Mulligan RS, Chetelat G, Ackermann U, O'Keefe G, Jones G, Gong S, Tochon-Danguy H, Kung HF, Masters CL, Skovronsky DM, Rowe CC: In vivo assessment of vesicular monoamine transporter type 2 in dementia with lewy bodies and Alzheimer disease. / Archives of neurology 2011,68(7):905-12. CrossRef
  34. Kotagal V, Albin RL, Muller ML, Koeppe RA, Chervin RD, Frey KA, Bohnen NI: Symptoms of rapid eye movement sleep behavior disorder are associated with cholinergic denervation in Parkinson disease. / Ann Neurol 2012,71(4):560-68. CrossRef
  35. Houlihan LM, Christoforou A, Arbuckle MI, Torrance HS, Anderson SM, Muir WJ, Porteous DJ, Blackwood DH, Evans KL: A case–control association study and family-based expression analysis of the bipolar disorder candidate gene PI4K2B. / J Psychiatr Res 2009,43(16):1272-277. CrossRef
  36. Pun FW, Zhao C, Lo WS, Ng SK, Tsang SY, Nimgaonkar V, Chung WS, Ungvari GS, Xue H: Imprinting in the schizophrenia candidate gene GABRB2 encoding GABA(A) receptor beta(2) subunit. / Mol Psychiatry 2011,16(5):557-68. CrossRef
  37. Zhang W, Wang PJ, Li MH, Gao XL, Gu GJ, Shao ZH: 1H-MRS can monitor metabolites changes of lateral intraventricular BDNF infusion into a mouse model of Alzheimer’s disease in vivo. / Neuroscience 2013, 245C:40-9. CrossRef
  38. Ranjbar E, Shams J, Sabetkasaei M, MS M, Rashidkhani B, Mostafavi A, Bornak E, Nasrollahzadeh J: Effects of zinc supplementation on efficacy of antidepressant therapy, inflammatory cytokines, and brain-derived neurotrophic factor in patients with major depression. / Nutr Neurosci 2014,17(2):65-1. CrossRef
  39. Nakatani N, Hattori E, Ohnishi T, Dean B, Iwayama Y, Matsumoto I, Kato T, Osumi N, Higuchi T, Niwa S, Yoshikawa T: Genome-wide expression analysis detects eight genes with robust alterations specific to bipolar I disorder: relevance to neuronal network perturbation. / Human molecular genetics 2006,15(12):1949-962. CrossRef
  40. Muller U, Winter P, Graeber MB: A presenilin 1 mutation in the first case of Alzheimer’s disease. / Lancet Neurol 2013,12(2):129-30. CrossRef
  41. Deng X, Takaki H, Wang L, Kuroki T, Nakahara T, Hashimoto K, Ninomiya H, Arinami T, Inada T, Ujike H, Itokawa M, Tochigi M, Watanabe Y, Someya T, Kunugi H, Iwata N, Ozaki N, Shibata H, Fukumaki Y: Positive association of phencyclidine-responsive genes, PDE4A and PLAT, with schizophrenia. / Am J Med Genet B Neuropsychiatr Genet 2011,156B(7):850-58. CrossRef
  42. Fatemi SH, Reutiman TJ, Folsom TD, Lee S: Phosphodiesterase-4A expression is reduced in cerebella of patients with bipolar disorder. / Psychiatr Genet 2008,18(6):282-88. CrossRef
  43. Mikhail FM, Lose EJ, Robin NH, Descartes MD, Rutledge KD, Rutledge SL, Korf BR, Carroll AJ: Clinically relevant single gene or intragenic deletions encompassing critical neurodevelopmental genes in patients with developmental delay, mental retardation, and/or autism spectrum disorders. / Am J Med Genet A 2011,155A(10):2386-396. CrossRef
  44. Bangash MA, Park JM, Melnikova T, Wang D, Jeon SK, Lee D, Syeda S, Kim J, Kouser M, Schwartz J, Cui Y, Zhao X, Speed HE, Kee SE, Tu JC, Hu J, Petralia RS, Linden DJ, Powell CM, Savonenko A, Xiao B, Worley PF: Retraction notice to: Enhancedpolyubiquitination of Shank3 and NMDA receptor in a mouse model of autism. / Cell 2013,152(1-):367. CrossRef
  45. Herbert MR: SHANK3, the synapse, and autism. / N Engl J Med 2011,365(2):173-75. CrossRef
  46. Denayer A, Van Esch H, de Ravel T, Frijns JP, Van Buggenhout G, Vogels A, Devriendt K, Geutjens J, Thiry P, Swillen A: Neuropsychopathology in 7 Patients with the 22q13 Deletion Syndrome: Presence of Bipolar Disorder and Progressive Loss of Skills. / Molecular syndromology 2012,3(1):14-0.
  47. Tan L, Yu JT, Zhang W, Wu ZC, Zhang Q, Liu QY, Wang W, Wang HF, Ma XY, Cui WZ: Association of GWAS-linked loci with late-onset Alzheimer’s disease in a northern Han Chinese population. / Alzheimers Dement 2013,9(5):546-53. CrossRef
  48. Yu JT, Ma XY, Wang YL, Sun L, Tan L, Hu N, Tan L: Genetic variation in Clusterin gene and Alzheimer’s disease risk in Han Chinese. / Neurobiol Aging 2013,34(7):1921. e1917-923
  49. Dieset I, Djurovic S, Tesli M, Hope S, Mattingsdal M, Michelsen A, Joa I, Larsen TK, Agartz I, Melle I, Rossberg JI, Aukrust P, Andreassen OA, Ueland T: Up-regulation of NOTCH4 gene expression in bipolar disorder. / Am J Psychiatry 2012,169(12):1292-300. CrossRef
  50. Shayevitz C, Cohen OS, Faraone SV, Glatt SJ: A re-review of the association between the NOTCH4 locus and schizophrenia. / Am J Med Genet B Neuropsychiatr Genet 2012,159B(5):477-83. CrossRef
  51. Meltzer HY, Brennan MD, Woodward ND, Jayathilake K: Association of Sult4A1 SNPs with psychopathology and cognition in patients with schizophrenia or schizoaffective disorder. / Schizophr Res 2008,106(2-):258-64. CrossRef
  52. Anderson LR, Betarbet R, Gearing M, Gulcher J, Hicks AA, Stefansson K, Lah JJ, Levey AI: PARK10 candidate RNF11 is expressed by vulnerable neurons and localizes to Lewy bodies in Parkinson disease brain. / J Neuropathol Exp Neurol 2007,66(10):955-64. CrossRef
  53. Sullivan PF, de Geus EJ, Willemsen G, James MR, Smit JH, Zandbelt T, Arolt V, Baune BT, Blackwood D, Cichon S, Coventry WL, Domschke K, Farmer A, Fava M, Gordon SD, He Q, Heath AC, Heutink P, Holsboer F, Hoogendijk WJ, Hottenga JJ, Hu Y, Kohli M, Lin D, Lucae S, Macintyre DJ, Maier W, McGhee KA, McGuffin P, Montgomery GW, / et al.: Genome-wide association for major depressive disorder: a possible role for the presynaptic protein piccolo. / Molecular psychiatry 2009,14(4):359-75. CrossRef
  54. Choi KH, Higgs BW, Wendland JR, Song J, McMahon FJ, Webster MJ: Gene expression and genetic variation data implicate PCLO in bipolar disorder. / Biol Psychiatry 2011,69(4):353-59. CrossRef
  55. Zheng Y, Wang Q, Xiao B, Lu Q, Wang Y, Wang X: Involvement of receptor tyrosine kinase Tyro3 in amyloidogenic APP processing and beta-amyloid deposition in Alzheimer’s disease models. / PLoS One 2012,7(6):e39035. CrossRef
  56. Kang HJ, Voleti B, Hajszan T, Rajkowska G, Stockmeier CA, Licznerski P, Lepack A, Majik MS, Jeong LS, Banasr M, Son H, Duman RS: Decreased expression of synapse-related genes and loss of synapses in major depressive disorder. / Nature medicine 2012,18(9):1413-417. CrossRef
  
• 作者单位：Xiaoling Weng (1)
  Daizhan Zhou (2)
  Fatao Liu (3)
  Hong Zhang (1)
  Junyi Ye (1)
  Zhou Zhang (2)
  Di Zhang (2)
  Yinan Wang (2)
  Liming Tao (3)
  Lan Cao (1)
  Mengyuan Kan (3)
  Ting Wang (3)
  Guoyin Feng (2) (3)
  Xiaolan Qin (2)
  Jihui Sun (4)
  Lin He (1) (2) (3) (6)
  Yun Liu (1) (5)
  
  1. Institutes of Biomedical Sciences, Fudan University, Shanghai, 200032, PR China
  2. Bio-X Center, Key Laboratory for the Genetics of Developmental and Neuropsychiatric Disorders, Ministry of Education, Shanghai Jiao Tong University, Shanghai, 200030, PR China
  3. Institute for Nutritional Sciences, Shanghai Institutes for Biological Sciences, Chinese Academy of Sciences, Shanghai, 200031, PR China
  4. Luwan Branch of Ruijin Hospital, Shanghai Jiaotong University School of Medicine, Shanghai, 200030, PR China
  6. Bio-X Institute, Shanghai Jiao Tong University, Small White House, 1954 Hua Shan Road, Shanghai, 200030, PR China
  5. Key Laboratory of Molecular Medicine, The Ministry of Education, Department of Biochemistry and Molecular Biology, Fudan University Shanghai Medical College, 303 Ming Dao Building, 138 Yi Xue Yuan Road, Shanghai, 200032, PR China
  
• ISSN：1471-2202

文摘

Background DNA methylation has been viewed as the most highly characterized epigenetic mark for genome regulation and development. Postnatal brains appear to exhibit stimulus-induced methylation changes because of factors such as environment, lifestyle, and diet (nutrition). The purpose of this study was to examine how extensively the brain DNA methylome is regulated by nutrition in early life. Results By quantifying the total amount of 5-methylcytosine (5mC) in the thalamus and the hippocampus of postnatal malnourished mice and normal mice, we found the two regions showed differences in global DNA methylation status. The methylation level in the thalamus was much higher than that in the hippocampus. Then, we used a next-generation sequencing (NGS)-based method (MSCC) to detect the whole genome methylation of the two regions in malnourished mice and normal mice. Notably, we found that in the thalamus, 500 discriminable variations existed and that approximately 60% were related to neuronal development or psychiatric diseases. Pathway analyses of the corresponding genes highlighted changes for 9 genes related to long-term potentiation (5.3-fold enrichment, P--.033). Conclusions Our findings may help to indicate the genome-wide DNA methylation status of different brain regions and the effects of malnutrition on brain DNA methylation. The results also indicate that postnatal malnutrition may increase the risk of psychiatric disorders.