Paternal Spatial Training Enhances Offspring's Cognitive Performance and Synaptic Plasticity in Wild-type but Not Improve Memory Deficit in Alzheimer's Mice

Overview

Journal Sci Rep

Specialty Science

Date 2017 May 10

PMID 28484240

Citations 4

Authors

Shujuan Zhang

Xiaoguang Li

Zhouyi Wang

Yanchao Liu

Yuan Gao

Lu Tan

Enjie Liu

Qiuzhi Zhou

Cheng Xu

Xin Wang

Gongping Liu

Haote Chen

Jian-Zhi Wang

Affiliations

Soon will be listed here.

Abstract

Recent studies suggest that spatial training can maintain associative memory capacity in Tg2576 mice, but it is not known whether the beneficial effects can be inherited from the trained fathers to their offspring. Here, we exposed male wild-type and male 3XTg Alzheimer disease (AD) mice (3-m old) respectively to spatial training for one week and assessed the transgenerational effects in the F1 offspring when they were grown to 7-m old. We found that the paternal spatial training significantly enhanced progeny's spatial cognitive performance and synaptic transmission in wild-type mice. Among several synapse- or memory-associated proteins, we observed that the expression level of synaptotagmin 1 (SYT1) was significantly increased in the hippocampus of the paternally trained-offspring. Paternal training increased histone acetylation at the promoter of SYT1 in both fathers' and the offspring's hippocampus, and as well as in the fathers' sperm. Finally, paternal spatial training for one week did not improve memory and synaptic plasticity in 3XTg AD F1 offspring. Our findings suggest paternal spatial training for one week benefits the offspring's cognitive performance in wild-type mice with the mechanisms involving an enhanced transgenerational histone acetylation at SYT1 promoter.

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References

Kawarabayashi T, Younkin L, Saido T, Shoji M, Ashe K, Younkin S . Age-dependent changes in brain, CSF, and plasma amyloid (beta) protein in the Tg2576 transgenic mouse model of Alzheimer's disease. J Neurosci. 2001; 21(2):372-81. PMC: 6763819. View

Liu Y, Chen H, Wu C, Kuo Y, Yu L, Huang A . Differential effects of treadmill running and wheel running on spatial or aversive learning and memory: roles of amygdalar brain-derived neurotrophic factor and synaptotagmin I. J Physiol. 2009; 587(Pt 13):3221-31. PMC: 2727033. DOI: 10.1113/jphysiol.2009.173088. View

Geppert M, Goda Y, Hammer R, Li C, Rosahl T, Stevens C . Synaptotagmin I: a major Ca2+ sensor for transmitter release at a central synapse. Cell. 1994; 79(4):717-27. DOI: 10.1016/0092-8674(94)90556-8. View

Zhao Z, Fan L, Frick K . Epigenetic alterations regulate estradiol-induced enhancement of memory consolidation. Proc Natl Acad Sci U S A. 2010; 107(12):5605-10. PMC: 2851775. DOI: 10.1073/pnas.0910578107. View

Zheng Y, Fan W, Zhang X, Dong E . Gestational stress induces depressive-like and anxiety-like phenotypes through epigenetic regulation of BDNF expression in offspring hippocampus. Epigenetics. 2016; 11(2):150-62. PMC: 4846107. DOI: 10.1080/15592294.2016.1146850. View

Cotman C, Berchtold N . Exercise: a behavioral intervention to enhance brain health and plasticity. Trends Neurosci. 2002; 25(6):295-301. DOI: 10.1016/s0166-2236(02)02143-4. View

van Praag H, Christie B, Sejnowski T, Gage F . Running enhances neurogenesis, learning, and long-term potentiation in mice. Proc Natl Acad Sci U S A. 1999; 96(23):13427-31. PMC: 23964. DOI: 10.1073/pnas.96.23.13427. View

Ihara M, Meyer-Ficca M, Leu N, Rao S, Li F, Gregory B . Paternal poly (ADP-ribose) metabolism modulates retention of inheritable sperm histones and early embryonic gene expression. PLoS Genet. 2014; 10(5):e1004317. PMC: 4014456. DOI: 10.1371/journal.pgen.1004317. View

Zheng S, Rollet M, Pan Y . Maternal protein restriction during pregnancy induces CCAAT/enhancer-binding protein (C/EBPβ) expression through the regulation of histone modification at its promoter region in female offspring rat skeletal muscle. Epigenetics. 2010; 6(2):161-70. DOI: 10.4161/epi.6.2.13472. View

10.

Kawasaki H, Schiltz L, Chiu R, Itakura K, Taira K, Nakatani Y . ATF-2 has intrinsic histone acetyltransferase activity which is modulated by phosphorylation. Nature. 2000; 405(6783):195-200. DOI: 10.1038/35012097. View

11.

Boulle F, Pawluski J, Homberg J, Machiels B, Kroeze Y, Kumar N . Developmental fluoxetine exposure increases behavioral despair and alters epigenetic regulation of the hippocampal BDNF gene in adult female offspring. Horm Behav. 2016; 80:47-57. DOI: 10.1016/j.yhbeh.2016.01.017. View

12.

Sweatt J . Neuroscience. Epigenetics and cognitive aging. Science. 2010; 328(5979):701-2. DOI: 10.1126/science.1189968. View

13.

Alonso A, Grundke-Iqbal I, Iqbal K . Alzheimer's disease hyperphosphorylated tau sequesters normal tau into tangles of filaments and disassembles microtubules. Nat Med. 1996; 2(7):783-7. DOI: 10.1038/nm0796-783. View

14.

Rodgers A, Morgan C, Leu N, Bale T . Transgenerational epigenetic programming via sperm microRNA recapitulates effects of paternal stress. Proc Natl Acad Sci U S A. 2015; 112(44):13699-704. PMC: 4640733. DOI: 10.1073/pnas.1508347112. View

15.

Benoit J, Rakic P, Frick K . Prenatal stress induces spatial memory deficits and epigenetic changes in the hippocampus indicative of heterochromatin formation and reduced gene expression. Behav Brain Res. 2014; 281:1-8. PMC: 4305490. DOI: 10.1016/j.bbr.2014.12.001. View

16.

Mattson M . Methylation and acetylation in nervous system development and neurodegenerative disorders. Ageing Res Rev. 2003; 2(3):329-42. DOI: 10.1016/s1568-1637(03)00013-8. View

17.

Babenko O, Kovalchuk I, Metz G . Stress-induced perinatal and transgenerational epigenetic programming of brain development and mental health. Neurosci Biobehav Rev. 2014; 48:70-91. DOI: 10.1016/j.neubiorev.2014.11.013. View

18.

Lithfous S, Dufour A, Despres O . Spatial navigation in normal aging and the prodromal stage of Alzheimer's disease: insights from imaging and behavioral studies. Ageing Res Rev. 2012; 12(1):201-13. DOI: 10.1016/j.arr.2012.04.007. View

19.

Quarini C, Pearson R, Stein A, Ramchandani P, Lewis G, Evans J . Are female children more vulnerable to the long-term effects of maternal depression during pregnancy?. J Affect Disord. 2015; 189:329-35. PMC: 4650986. DOI: 10.1016/j.jad.2015.09.039. View

20.

Gapp K, Soldado-Magraner S, Alvarez-Sanchez M, Bohacek J, Vernaz G, Shu H . Early life stress in fathers improves behavioural flexibility in their offspring. Nat Commun. 2014; 5:5466. DOI: 10.1038/ncomms6466. View