Role of apolipoprotein E and estrogen in mossy fiber sprouting in hippocampal slice cultures

Teter, Bruce; Harris-White, Marni E.; Frautschy, Sally A.; Cole, Greg M.

doi:10.1016/s0306-4522(98)00630-7

Cited by 69 publications

(45 citation statements)

References 77 publications

(82 reference statements)

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“…This concentration of E 2 also induces maximal apoE induction in mixed glia [195]. E 2 -dependent sprouting can be blocked by P 4 or tamoxifen [192]. P 4 appears to differ from MPA in its ability to regulate synaptic plasticity.…”

Section: Progesterone Regulation Of Glial Cell Function and Responsementioning

confidence: 85%

“…During pregnancy, two-fold increases in uterine apoE levels are associated with increased import of maternal lipids [190]. Also, estrogen-dependent sprouting of perforant path fibers to the hippocampus is absent in apoE-knockout mice [191] [189] [192]. Complex heterotypic cellular interactions that occur in response to ovarian steroids extend beyond astrocytic-neuronal interactions.…”

Section: Progesterone Regulation Of Glial Cell Function and Responsementioning

confidence: 99%

“…As discussed above, E 2 drives increases in CA1 spine density (growth phase), while P 4 promotes the regression of dendritic spines (during the proestrus to estrus transition). In mouse hippocampal slice cultures, mossy fiber sprouting into the molecular layer of the dentate gyrus is induced by deafferentation of the entorhinal cortex [192]. In this system, E 2 (100 pM) increases sprouting by 75%.…”

Section: Progesterone Regulation Of Glial Cell Function and Responsementioning

confidence: 99%

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Progesterone receptors: Form and function in brain

Brinton

Thompson

Foy

et al. 2008

Frontiers in Neuroendocrinology

569

443

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Emerging data indicate that progesterone has multiple non-reproductive functions in the central nervous system to regulate cognition, mood, inflammation, mitochondrial function, neurogenesis and regeneration, myelination and recovery from traumatic brain injury. Progesterone-regulated neural responses are mediated by an array of progesterone receptors (PR) that include the classic nuclear PRA and PRB receptors and splice variants of each, the seven transmembrane domain 7TMPRβ and the membrane-associated 25-Dx PR (PGRMC1). These PRs induce classic regulation of gene expression while also transducing signaling cascades that originate at the cell membrane and ultimately activate transcription factors. Remarkably, PRs are broadly expressed throughout the brain and can be detected in every neural cell type. The distribution of PRs beyond hypothalamic borders, suggests a much broader role of progesterone in regulating neural function. Despite the large body of evidence regarding progesterone regulation of reproductive behaviors and estrogen-inducible responses as well as effects of progesterone metabolite neurosteroids, much remains to be discovered regarding the functional outcomes resulting from activation of the complex array of PRs in brain by gonadally and / or glial derived progesterone. Moreover, the impact of clinically used progestogens and developing selective PR modulators for targeted outcomes in brain is a critical avenue of investigation as the non-reproductive functions of PRs have far-reaching implications for hormone therapy to maintain neurological health and function throughout menopausal aging.

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Section: Progesterone Regulation Of Glial Cell Function and Responsementioning

confidence: 85%

Section: Progesterone Regulation Of Glial Cell Function and Responsementioning

confidence: 99%

Section: Progesterone Regulation Of Glial Cell Function and Responsementioning

confidence: 99%

See 1 more Smart Citation

Progesterone receptors: Form and function in brain

Brinton

Thompson

Foy

et al. 2008

Frontiers in Neuroendocrinology

569

443

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“…In the absence of ApoE, estrogen did not show any effect on neurite sprouting (42,43). Nathan et al (16) found that E 2 -induced neurite sprouting depended on the ApoE genotype.…”

Section: E2-regulated Apoe Expression Is Mediated By Er and Is Er Isomentioning

confidence: 98%

Activation of estrogen receptor α increases and estrogen receptor β decreases apolipoprotein E expression in hippocampus in vitro and in vivo

Wang

Irwin

Brinton

2006

Proc. Natl. Acad. Sci. U.S.A.

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Alzheimer's disease ͉ estrogen therapy ͉ risk factor regulation ͉ Alzheimer's disease prevention A polipoprotein E (ApoE) is a 34-kDa lipid binding protein that functions in the transport of triglycerides and cholesterol in multiple tissues, including brain, by interacting with lipoprotein receptors on target cells (1-4). Three ApoE isoforms exist in humans: ApoE2, ApoE3, and ApoE4, which differ from one another by single amino acid substitutions at positions 112 and 158, ApoE2 (Cys-112, Cys-158), ApoE3 (Cys-112, Arg-158), and ApoE4 (Arg-112, Arg-158) (5). Substitution of cysteine at position 158 in ApoE2 results in hypocholesterolemia caused by low levels of low-density lipoprotein (LDL), cholesterol (6). In contrast, substitution of cysteine with arginine at position 112 in ApoE4 results in elevation of plasma cholesterol and LDL levels and predisposes the carrier to cardiovascular disease and neurodegenerative disorders, including Alzheimer's disease (AD) (7,8).Statistically, individuals with one copy of the ApoE4 allele show a 4-fold increase in the risk of AD, whereas those with two copies of the ApoE4 allele exhibit a 15-fold increase in risk coupled with a significantly lower age of onset compared with AD patients carrying ApoE2͞3 alleles (9). The ApoE4 allele itself appears to account for as much as 50% of the populationattributable AD risk in the United States (for reviews see refs. 10 and 11). Thus, ApoE4 is considered a risk factor for late-onset AD, whereas ApoE2 and ApoE3 are associated with decreased risk of AD (10,12,13).Previous in vitro and in vivo analyses indicate that 17␤-estradiol (E 2 ) increased ApoE expression in astrocytes and microglia and in neurons (14, 15). Further, ApoE synthesis was required for E 2 -induced neuroprotection and neurotrophism, including neurite outgrowth (16,17).Recently, we discovered that in HT-22 cells ectopically transfected with full-length estrogen receptor (ER) (ER␣ or ER␤), E 2 -induced an opposite effect on ApoE expression depending on the transfected ER subtype. Based on our own data and others (17-19), we hypothesized that ApoE expression is differentially regulated by ER subtypes. To test this hypothesis, we investigated the impact of ER␣ versus ER␤ on ApoE gene expression by using real-time RT-PCR with confirmation of protein levels by Western blot in primary cultured rat hippocampal neurons. To determine the in vivo significance of our in vitro findings, we conducted in vivo analyses in ovariectomized (OVX) female rats treated with either the ER␣-selective ligand, propylpyrazole triol (PPT) or the ER␤-selective ligand, diarylpropionitrile (DPN). Results of these analyses demonstrated that the expression of ApoE is differentially regulated by ER␣ and ER␤. Activation of ER␣ increased, whereas activation of ER␤ decreased ApoE mRNA and protein expression in vitro and in vivo in rat hippocampus. Results Differential ApoE Expression in HT-22 Cells Transfected with ER␣ orER␤. To determine the ER subtype mediating E 2 regulation of ApoE, mouse hybrid HT-22 cel...

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“…In previous work, 50 the authors found that axonal sprouting was stimulated by estrogen through upregulation of apolipoprotein E expression, but progesterone inhibited this effect. In contrast, other steroids, such as prednisolone, inhibit aberrant sprouting in the injured rat spinal cord.…”

Section: Discussionmentioning

confidence: 91%

Aberrant gastrocnemius muscle innervation by tibial nerve afferents after implantation of chitosan tubes impregnated with progesterone favored locomotion recovery in rats with transected sciatic nerve

Sarabia-Estrada

Bañuelos-Pineda

Osuna-Carrasco³

et al. 2015

JNS

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obJect Transection of peripheral nerves produces loss of sensory and/or motor function. After complete nerve cutting, the distal and proximal segment ends retract, but if both ends are bridged with unaltered chitosan, progesteroneimpregnated chitosan, or silicone tubes, an axonal repair process begins. Progesterone promotes nerve repair and has neuroprotective effects thwarting regulation of neuron survival, inflammation, and edema. It also modulates aberrant axonal sprouting and demyelination. The authors compared the efficacy of nerve recovery after implantation of progesterone-loaded chitosan, unaltered chitosan, or silicone tubes after sciatic nerve transection in rats. methods After surgical removal of a 5-mm segment of the proximal sciatic nerve, rats were implanted with progesterone-loaded chitosan, unaltered chitosan, or silicone tubes in the transected nerve for evaluating progesterone and chitosan effects on sciatic nerve repair and ipsilateral hindlimb kinematic function, as well as on gastrocnemius electromyographic responses. In some experiments, tube implantation was performed 90 minutes after nerve transection. results At 90 days after sciatic nerve transection and tube implantation, rats with progesterone-loaded chitosan tubes showed knee angular displacement recovery and better outcomes for step length, velocity of locomotion, and normal hindlimb raising above the ground. In contrast, rats with chitosan-only tubes showed reduced normal raising and pendulum-like hindlimb movements. Aberrant fibers coming from the tibial nerve innervated the gastrocnemius muscle, producing electromyographic responses. Electrical responses in the gastrocnemius muscle produced by sciatic nerve stimulation occurred only when the distal nerve segment was stimulated; they were absent when the proximal or intratubular segment was stimulated. A clear sciatic nerve morphology with some myelinated fiber fascicles appeared in the tube section in rats with progesterone-impregnated chitosan tubes. Some gastrocnemius efferent fibers were partially repaired 90 days after nerve resection. The better outcome in knee angle displacement may be partially attributable to the aberrant neuromuscular synaptic effects, since nerve conduction in the gastrocnemius muscle could be blocked in the progesterone-impregnated chitosan tubes. In addition, in the region of the gap produced by the nerve resection, the number of axons and amount of myelination were reduced in the sciatic nerve implanted with chitosan, progesteroneloaded chitosan, and silicone tubes. At 180 days after sciatic nerve sectioning, the knee kinematic function recovered to a level observed in control rats of a similar age. In rats with progesterone-loaded chitosan tubes, stimulation of the proximal and intratubular sciatic nerve segments produced an electromyographic response. The axon morphology of the proximal and intratubular segments of the sciatic nerve resembled that of the contralateral nontransected nerve. coNclusioNs Progesterone-impregnated chitosan tubes produced...

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Role of apolipoprotein E and estrogen in mossy fiber sprouting in hippocampal slice cultures

Cited by 69 publications

References 77 publications

Progesterone receptors: Form and function in brain

Progesterone receptors: Form and function in brain

Activation of estrogen receptor α increases and estrogen receptor β decreases apolipoprotein E expression in hippocampus in vitro and in vivo

Aberrant gastrocnemius muscle innervation by tibial nerve afferents after implantation of chitosan tubes impregnated with progesterone favored locomotion recovery in rats with transected sciatic nerve

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