Anatomical distribution of histone H3 acetylation in human hippocampus

Bingyue  Cao; Fengling Luo; Wenwen Zhang; Renwei Luo; Lile Cai; Yongchang Wei; Yanqing Wang; Pan Liu

doi:10.37819/hb.1.1900

Anatomical distribution of histone H3 acetylation in human hippocampus

Bingyue Cao

Fengling Luo

Wenwen Zhang

Renwei Luo

Lile Cai

Yongchang Wei

Yanqing Wang

Pan Liu

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Abstract

In recent years, the role of histone acetylation in the brain has been studied from different aspects. However, the anatomical distribution of histone H3 acetylation in the human hippocampus and its potential relevance to triple synaptic circuits are unknown. As one of epigenetic remodeling ways, the modification of histones is involved in multiple aspects of neuronal function and development and is a key process in the onset and development of Alzheimer’s disease (AD). In our study, we compared acetylation levels of histone H3 at different regions of the hippocampus in AD and non-AD patients. We found that histone H3 acetylation can be detected in the dentate gyrus (DG), CA4, CA3, CA2, CA1, and lower Toya regions of the human hippocampus. The highest degree of acetylation in the hippocampus is in DG, and the level of acetylation changes gradually and systematically along the triple synaptic circuit. Besides, there were no significant differences in histone acetylation between AD and non-AD groups.

Keywords: hippocampus histone H3 acetylation anatomical distribution

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References

Knierim JJ. The hippocampus. Curr Biol. 2015 Dec 7;25(23):R1116-1121.
Hainmueller T, Bartos M. Parallel emergence of stable and dynamic memory engrams in the hippocampus. Nature. 2018 Jun;558(7709):292–6.
Moser MB, Moser EI. Functional differentiation in the hippocampus. Hippocampus. 1998;8(6):608–19.
Brewer GJ, Boehler MD, Leondopulos S, Pan L, Alagapan S, DeMarse TB, et al. Toward a self-wired active reconstruction of the hippocampal trisynaptic loop: DG-CA3. Front Neural Circuits. 2013;7:165.
Kitamura T, Ogawa SK, Roy DS, Okuyama T, Morrissey MD, Smith LM, et al. Engrams and circuits crucial for systems consolidation of a memory. Science. 2017 Apr 7;356(6333):73–8.
Sun X, Bernstein MJ, Meng M, Rao S, Sørensen AT, Yao L, et al. Functionally Distinct Neuronal Ensembles within the Memory Engram. Cell. 2020 Apr 16;181(2):410-423.e17.
Scheltens P, De Strooper B, Kivipelto M, Holstege H, Chételat G, Teunissen CE, et al. Alzheimer’s disease. Lancet. 2021 Apr 24;397(10284):1577–90.
Berson A, Nativio R, Berger SL, Bonini NM. Epigenetic Regulation in Neurodegenerative Diseases. Trends Neurosci. 2018 Sep;41(9):587–98.
Verdone L, Agricola E, Caserta M, Di Mauro E. Histone acetylation in gene regulation. Brief Funct Genomic Proteomic. 2006 Sep;5(3):209–21.
Mews P, Donahue G, Drake AM, Luczak V, Abel T, Berger SL. Acetyl-CoA synthetase regulates histone acetylation and hippocampal memory. Nature. 2017 Jun 15;546(7658):381–6.
Pradeepa MM, Grimes GR, Kumar Y, Olley G, Taylor GCA, Schneider R, et al. Histone H3 globular domain acetylation identifies a new class of enhancers. Nat Genet. 2016 Jun;48(6):681–6.
MacDonald VE, Howe LJ. Histone acetylation: where to go and how to get there. Epigenetics. 2009 Apr 1;4(3):139–43.
Pokholok DK, Harbison CT, Levine S, Cole M, Hannett NM, Lee TI, et al. Genome-wide map of nucleosome acetylation and methylation in yeast. Cell. 2005 Aug 26;122(4):517–27.
Rosaleny LE, Ruiz-García AB, García-Martínez J, Pérez-Ortín JE, Tordera V. The Sas3p and Gcn5p histone acetyltransferases are recruited to similar genes. Genome Biol. 2007;8(6):R119.
Wang Z, Zang C, Rosenfeld JA, Schones DE, Barski A, Cuddapah S, et al. Combinatorial patterns of histone acetylations and methylations in the human genome. Nat Genet. 2008 Jul;40(7):897–903.
Oishi T, Hatazawa S, Kujirai T, Kato J, Kobayashi Y, Ogasawara M, et al. Contributions of histone tail clipping and acetylation in nucleosome transcription by RNA polymerase II. Nucleic Acids Res. 2023 Oct 27;51(19):10364–74.
Kim SY, Levenson JM, Korsmeyer S, Sweatt JD, Schumacher A. Developmental regulation of Eed complex composition governs a switch in global histone modification in brain. J Biol Chem. 2007 Mar 30;282(13):9962–72.
Peleg S, Sananbenesi F, Zovoilis A, Burkhardt S, Bahari-Javan S, Agis-Balboa RC, et al. Altered histone acetylation is associated with age-dependent memory impairment in mice. Science. 2010 May 7;328(5979):753–6.
Contestabile A, Sintoni S. Histone acetylation in neurodevelopment. Curr Pharm Des. 2013;19(28):5043–50.
Fan SJ, Sun AB, Liu L. Epigenetic modulation during hippocampal development. Biomed Rep. 2018 Dec;9(6):463–73.
Sakharkar AJ, Vetreno RP, Zhang H, Kokare DM, Crews FT, Pandey SC. A role for histone acetylation mechanisms in adolescent alcohol exposure-induced deficits in hippocampal brain-derived neurotrophic factor expression and neurogenesis markers in adulthood. Brain Struct Funct. 2016 Dec;221(9):4691–703.
Mews P, Egervari G, Nativio R, Sidoli S, Donahue G, Lombroso SI, et al. Alcohol metabolism contributes to brain histone acetylation. Nature. 2019 Oct;574(7780):717–21.
He W, Li Q, Li X. Acetyl-CoA regulates lipid metabolism and histone acetylation modification in cancer. Biochim Biophys Acta Rev Cancer. 2023 Jan;1878(1):188837.
Peleg S, Feller C, Ladurner AG, Imhof A. The Metabolic Impact on Histone Acetylation and Transcription in Ageing. Trends Biochem Sci. 2016 Aug;41(8):700–11.
Nasca C, Zelli D, Bigio B, Piccinin S, Scaccianoce S, Nisticò R, et al. Stress dynamically regulates behavior and glutamatergic gene expression in hippocampus by opening a window of epigenetic plasticity. Proc Natl Acad Sci U S A. 2015 Dec 1;112(48):14960–5.
Schneider JS, Anderson DW, Kidd SK, Sobolewski M, Cory-Slechta DA. Sex-Dependent Effects of Lead and Prenatal Stress on Post-translational Histone Modifications in Frontal Cortex and Hippocampus in the Early Postnatal Brain. Neurotoxicology. 2016 May;54:65–71.
Crisp KM. Multiple spike initiation zones in a neuron implicated in learning in the leech: a computational model. Invert Neurosci. 2009 Mar;9(1):1–10.
Yeckel MF, Berger TW. Feedforward excitation of the hippocampus by afferents from the entorhinal cortex: redefinition of the role of the trisynaptic pathway. Proc Natl Acad Sci U S A. 1990 Aug;87(15):5832–6.

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“Anatomical Distribution of Histone H3 Acetylation in Human Hippocampus”. Human Brain, vol. 3, no. 1, July 2024, https://doi.org/10.37819/hb.1.1900.

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“Anatomical Distribution of Histone H3 Acetylation in Human Hippocampus”. Human Brain, vol. 3, no. 1, July 2024, https://doi.org/10.37819/hb.1.1900.

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Fengling Luo

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Wenwen Zhang

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Renwei Luo

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Lile Cai

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Yongchang Wei

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Yanqing Wang

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Pan Liu

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[1] Knierim JJ. The hippocampus. Curr Biol. 2015 Dec 7;25(23):R1116-1121.

[2] Hainmueller T, Bartos M. Parallel emergence of stable and dynamic memory engrams in the hippocampus. Nature. 2018 Jun;558(7709):292–6.

[3] Moser MB, Moser EI. Functional differentiation in the hippocampus. Hippocampus. 1998;8(6):608–19.

[4] Brewer GJ, Boehler MD, Leondopulos S, Pan L, Alagapan S, DeMarse TB, et al. Toward a self-wired active reconstruction of the hippocampal trisynaptic loop: DG-CA3. Front Neural Circuits. 2013;7:165.

[5] Kitamura T, Ogawa SK, Roy DS, Okuyama T, Morrissey MD, Smith LM, et al. Engrams and circuits crucial for systems consolidation of a memory. Science. 2017 Apr 7;356(6333):73–8.

[6] Sun X, Bernstein MJ, Meng M, Rao S, Sørensen AT, Yao L, et al. Functionally Distinct Neuronal Ensembles within the Memory Engram. Cell. 2020 Apr 16;181(2):410-423.e17.

[7] Scheltens P, De Strooper B, Kivipelto M, Holstege H, Chételat G, Teunissen CE, et al. Alzheimer’s disease. Lancet. 2021 Apr 24;397(10284):1577–90.

[8] Berson A, Nativio R, Berger SL, Bonini NM. Epigenetic Regulation in Neurodegenerative Diseases. Trends Neurosci. 2018 Sep;41(9):587–98.

[9] Verdone L, Agricola E, Caserta M, Di Mauro E. Histone acetylation in gene regulation. Brief Funct Genomic Proteomic. 2006 Sep;5(3):209–21.

[10] Mews P, Donahue G, Drake AM, Luczak V, Abel T, Berger SL. Acetyl-CoA synthetase regulates histone acetylation and hippocampal memory. Nature. 2017 Jun 15;546(7658):381–6.

[11] Pradeepa MM, Grimes GR, Kumar Y, Olley G, Taylor GCA, Schneider R, et al. Histone H3 globular domain acetylation identifies a new class of enhancers. Nat Genet. 2016 Jun;48(6):681–6.

[12] MacDonald VE, Howe LJ. Histone acetylation: where to go and how to get there. Epigenetics. 2009 Apr 1;4(3):139–43.

[13] Pokholok DK, Harbison CT, Levine S, Cole M, Hannett NM, Lee TI, et al. Genome-wide map of nucleosome acetylation and methylation in yeast. Cell. 2005 Aug 26;122(4):517–27.

[14] Rosaleny LE, Ruiz-García AB, García-Martínez J, Pérez-Ortín JE, Tordera V. The Sas3p and Gcn5p histone acetyltransferases are recruited to similar genes. Genome Biol. 2007;8(6):R119.

[15] Wang Z, Zang C, Rosenfeld JA, Schones DE, Barski A, Cuddapah S, et al. Combinatorial patterns of histone acetylations and methylations in the human genome. Nat Genet. 2008 Jul;40(7):897–903.

[16] Oishi T, Hatazawa S, Kujirai T, Kato J, Kobayashi Y, Ogasawara M, et al. Contributions of histone tail clipping and acetylation in nucleosome transcription by RNA polymerase II. Nucleic Acids Res. 2023 Oct 27;51(19):10364–74.

[17] Kim SY, Levenson JM, Korsmeyer S, Sweatt JD, Schumacher A. Developmental regulation of Eed complex composition governs a switch in global histone modification in brain. J Biol Chem. 2007 Mar 30;282(13):9962–72.

[18] Peleg S, Sananbenesi F, Zovoilis A, Burkhardt S, Bahari-Javan S, Agis-Balboa RC, et al. Altered histone acetylation is associated with age-dependent memory impairment in mice. Science. 2010 May 7;328(5979):753–6.

[19] Contestabile A, Sintoni S. Histone acetylation in neurodevelopment. Curr Pharm Des. 2013;19(28):5043–50.

[20] Fan SJ, Sun AB, Liu L. Epigenetic modulation during hippocampal development. Biomed Rep. 2018 Dec;9(6):463–73.

[21] Sakharkar AJ, Vetreno RP, Zhang H, Kokare DM, Crews FT, Pandey SC. A role for histone acetylation mechanisms in adolescent alcohol exposure-induced deficits in hippocampal brain-derived neurotrophic factor expression and neurogenesis markers in adulthood. Brain Struct Funct. 2016 Dec;221(9):4691–703.

[22] Mews P, Egervari G, Nativio R, Sidoli S, Donahue G, Lombroso SI, et al. Alcohol metabolism contributes to brain histone acetylation. Nature. 2019 Oct;574(7780):717–21.

[23] He W, Li Q, Li X. Acetyl-CoA regulates lipid metabolism and histone acetylation modification in cancer. Biochim Biophys Acta Rev Cancer. 2023 Jan;1878(1):188837.

[24] Peleg S, Feller C, Ladurner AG, Imhof A. The Metabolic Impact on Histone Acetylation and Transcription in Ageing. Trends Biochem Sci. 2016 Aug;41(8):700–11.

[25] Nasca C, Zelli D, Bigio B, Piccinin S, Scaccianoce S, Nisticò R, et al. Stress dynamically regulates behavior and glutamatergic gene expression in hippocampus by opening a window of epigenetic plasticity. Proc Natl Acad Sci U S A. 2015 Dec 1;112(48):14960–5.

[26] Schneider JS, Anderson DW, Kidd SK, Sobolewski M, Cory-Slechta DA. Sex-Dependent Effects of Lead and Prenatal Stress on Post-translational Histone Modifications in Frontal Cortex and Hippocampus in the Early Postnatal Brain. Neurotoxicology. 2016 May;54:65–71.

[27] Crisp KM. Multiple spike initiation zones in a neuron implicated in learning in the leech: a computational model. Invert Neurosci. 2009 Mar;9(1):1–10.

[28] Yeckel MF, Berger TW. Feedforward excitation of the hippocampus by afferents from the entorhinal cortex: redefinition of the role of the trisynaptic pathway. Proc Natl Acad Sci U S A. 1990 Aug;87(15):5832–6.

Anatomical distribution of histone H3 acetylation in human hippocampus

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