Expansion of the dentate mossy fiber–CA3 projection in the brain-derived neurotrophic factor-enriched mouse hippocampus

Highlights • BDNF expression is chronically increased in the hippocampus of TgBDNF mice. • Mossy fiber volume in CA3 is enlarged by 2–3 months of age in TgBDNF mice. • At seizure-prone ages (6–7 months) mossy fiber volume increases further. • By 8 months, granule cell number is also significantly in...

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Published in	Neuroscience Vol. 288; pp. 10 - 23
Main Authors	Isgor, C, Pare, C, McDole, B, Coombs, P, Guthrie, K
Format	Journal Article
Language	English
Published	United States Elsevier Ltd 12.03.2015
Subjects	Animals brain-derived neurotrophic factor Brain-Derived Neurotrophic Factor - genetics Brain-Derived Neurotrophic Factor - metabolism CA3 Region, Hippocampal - cytology CA3 Region, Hippocampal - growth & development CA3 Region, Hippocampal - metabolism Cell Count dentate granule cells Dentate Gyrus - growth & development Dentate Gyrus - metabolism epilepsy Female hippocampus Male Mice, Inbred C57BL Mice, Transgenic Neurology Neurons - cytology Neurons - metabolism Pilocarpine Rats RNA, Messenger - metabolism seizure Seizures - metabolism TrkB epilepsy tropomyosin-related kinase B receptor DG seizure intra/infrapyramidal inner molecular layer molecular layer phosphate buffer Tris-buffered saline transgenic CAMKIIa-BDNF mouse strain MF proBDNF brain-derived neurotrophic factor mossy fiber SP suprapyramidal WT dentate granule cells ML TBS hippocampus BDNF granule cell layer IML TgBDNF GCL IIP dentate gyrus PB TrkB mature BDNF prepro-brain-derived neurotrophic factor mBDNF wild-type
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Abstract	Highlights • BDNF expression is chronically increased in the hippocampus of TgBDNF mice. • Mossy fiber volume in CA3 is enlarged by 2–3 months of age in TgBDNF mice. • At seizure-prone ages (6–7 months) mossy fiber volume increases further. • By 8 months, granule cell number is also significantly increased in TgBDNF mice.
AbstractList	Structural changes that alter hippocampal functional circuitry are implicated in learning impairments, mood disorders and epilepsy. Reorganization of mossy fiber (MF) axons from dentate granule cells is one such form of plasticity. Increased neurotrophin signaling is proposed to underlie MF plasticity, and there is evidence to support a mechanistic role for brain-derived neurotrophic factor (BDNF) in this process. Transgenic mice overexpressing BDNF in the forebrain under the alpha -calcium/calmodulin-dependent protein kinase II promoter (TgBDNF mice) exhibit spatial learning deficits at 2-3months of age, followed by the emergence of spontaneous seizures at 6months. These behavioral changes suggest that chronic increases in BDNF progressively disrupt hippocampal functional organization. To determine if the dentate MF pathway is structurally altered in this strain, the present study employed Timm staining and design-based stereology to compare MF distribution and projection volumes in transgenic and wild-type mice at 2-3months, and at 6-7months. Mice in the latter age group were assessed for seizure vulnerability with a low dose of pilocarpine given 2h before euthanasia. At 2-3months, TgBDNF mice showed moderate expansion of CA3-projecting MFs (20%), with increased volumes measured in the suprapyramidal (SP-MF) and intra/infrapyramidal (IIP-MF) compartments. At 6-7months, a subset of transgenic mice exhibited increased seizure susceptibility, along with an increase in IIP-MF volume (30%). No evidence of MF sprouting was seen in the inner molecular layer. Additional stereological analyses demonstrated significant increases in molecular layer (ML) volume in TgBDNF mice at both ages, as well as an increase in granule cell number by 8months of age. Collectively, these results indicate that sustained increases in endogenous BDNF modify dentate structural organization over time, and may thereby contribute to the development of pro-epileptic circuitry. Structural changes that alter hippocampal functional circuitry are implicated in learning impairments, mood disorders and epilepsy. Reorganization of mossy fiber (MF) axons from dentate granule cells is one such form of plasticity. Increased neurotrophin signaling is proposed to underlie MF plasticity, and there is evidence to support a mechanistic role for brain-derived neurotrophic factor (BDNF) in this process. Transgenic mice overexpressing BDNF in the forebrain under the α-calcium/calmodulin-dependent protein kinase II promoter (TgBDNF mice) exhibit spatial learning deficits at 2-3months of age, followed by the emergence of spontaneous seizures at ∼6months. These behavioral changes suggest that chronic increases in BDNF progressively disrupt hippocampal functional organization. To determine if the dentate MF pathway is structurally altered in this strain, the present study employed Timm staining and design-based stereology to compare MF distribution and projection volumes in transgenic and wild-type mice at 2-3months, and at 6-7months. Mice in the latter age group were assessed for seizure vulnerability with a low dose of pilocarpine given 2h before euthanasia. At 2-3months, TgBDNF mice showed moderate expansion of CA3-projecting MFs (∼20%), with increased volumes measured in the suprapyramidal (SP-MF) and intra/infrapyramidal (IIP-MF) compartments. At 6-7months, a subset of transgenic mice exhibited increased seizure susceptibility, along with an increase in IIP-MF volume (∼30%). No evidence of MF sprouting was seen in the inner molecular layer. Additional stereological analyses demonstrated significant increases in molecular layer (ML) volume in TgBDNF mice at both ages, as well as an increase in granule cell number by 8months of age. Collectively, these results indicate that sustained increases in endogenous BDNF modify dentate structural organization over time, and may thereby contribute to the development of pro-epileptic circuitry. •BDNF expression is chronically increased in the hippocampus of TgBDNF mice.•Mossy fiber volume in CA3 is enlarged by 2–3months of age in TgBDNF mice.•At seizure-prone ages (6–7months) mossy fiber volume increases further.•By 8months, granule cell number is also significantly increased in TgBDNF mice. Structural changes that alter hippocampal functional circuitry are implicated in learning impairments, mood disorders and epilepsy. Reorganization of mossy fiber (MF) axons from dentate granule cells is one such form of plasticity. Increased neurotrophin signaling is proposed to underlie MF plasticity, and there is evidence to support a mechanistic role for brain-derived neurotrophic factor (BDNF) in this process. Transgenic mice overexpressing BDNF in the forebrain under the α-calcium/calmodulin-dependent protein kinase II promoter (TgBDNF mice) exhibit spatial learning deficits at 2–3months of age, followed by the emergence of spontaneous seizures at ∼6months. These behavioral changes suggest that chronic increases in BDNF progressively disrupt hippocampal functional organization. To determine if the dentate MF pathway is structurally altered in this strain, the present study employed Timm staining and design-based stereology to compare MF distribution and projection volumes in transgenic and wild-type mice at 2–3months, and at 6–7months. Mice in the latter age group were assessed for seizure vulnerability with a low dose of pilocarpine given 2h before euthanasia. At 2–3months, TgBDNF mice showed moderate expansion of CA3-projecting MFs (∼20%), with increased volumes measured in the suprapyramidal (SP-MF) and intra/infrapyramidal (IIP-MF) compartments. At 6–7months, a subset of transgenic mice exhibited increased seizure susceptibility, along with an increase in IIP-MF volume (∼30%). No evidence of MF sprouting was seen in the inner molecular layer. Additional stereological analyses demonstrated significant increases in molecular layer (ML) volume in TgBDNF mice at both ages, as well as an increase in granule cell number by 8months of age. Collectively, these results indicate that sustained increases in endogenous BDNF modify dentate structural organization over time, and may thereby contribute to the development of pro-epileptic circuitry. Highlights • BDNF expression is chronically increased in the hippocampus of TgBDNF mice. • Mossy fiber volume in CA3 is enlarged by 2–3 months of age in TgBDNF mice. • At seizure-prone ages (6–7 months) mossy fiber volume increases further. • By 8 months, granule cell number is also significantly increased in TgBDNF mice.
Author	Coombs, P Isgor, C Pare, C McDole, B Guthrie, K
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BackLink	https://www.ncbi.nlm.nih.gov/pubmed/25555929$$D View this record in MEDLINE/PubMed
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Keywords	epilepsy tropomyosin-related kinase B receptor DG seizure intra/infrapyramidal inner molecular layer molecular layer phosphate buffer Tris-buffered saline transgenic CAMKIIa-BDNF mouse strain MF proBDNF brain-derived neurotrophic factor mossy fiber SP suprapyramidal WT dentate granule cells ML TBS hippocampus BDNF granule cell layer IML TgBDNF GCL IIP dentate gyrus PB TrkB mature BDNF prepro-brain-derived neurotrophic factor mBDNF wild-type
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Snippet	Highlights • BDNF expression is chronically increased in the hippocampus of TgBDNF mice. • Mossy fiber volume in CA3 is enlarged by 2–3 months of age in TgBDNF... •BDNF expression is chronically increased in the hippocampus of TgBDNF mice.•Mossy fiber volume in CA3 is enlarged by 2–3months of age in TgBDNF mice.•At... Structural changes that alter hippocampal functional circuitry are implicated in learning impairments, mood disorders and epilepsy. Reorganization of mossy...
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SubjectTerms	Animals brain-derived neurotrophic factor Brain-Derived Neurotrophic Factor - genetics Brain-Derived Neurotrophic Factor - metabolism CA3 Region, Hippocampal - cytology CA3 Region, Hippocampal - growth & development CA3 Region, Hippocampal - metabolism Cell Count dentate granule cells Dentate Gyrus - growth & development Dentate Gyrus - metabolism epilepsy Female hippocampus Male Mice, Inbred C57BL Mice, Transgenic Neurology Neurons - cytology Neurons - metabolism Pilocarpine Rats RNA, Messenger - metabolism seizure Seizures - metabolism TrkB
Title	Expansion of the dentate mossy fiber–CA3 projection in the brain-derived neurotrophic factor-enriched mouse hippocampus
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