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Exercise-linked FNDC5/irisin rescues synaptic plasticity and memory defects in Alzheimer’s models

Defective brain hormonal signaling has been associated with Alzheimer's disease (AD), a disorder characterized by synapse and memory failure. Irisin is an exercise-induced myokine released on cleavage of the membrane-bound precursor protein fibronectin type III domain-containing protein 5 (FNDC5), a... Full description

Journal Title: Nature medicine 2019, Vol.25 (1), p.165-175
Main Author: Lourenco, Mychael V
Other Authors: Frozza, Rudimar L , de Freitas, Guilherme B , Zhang, Hong , Kincheski, Grasielle C , Ribeiro, Felipe C , Gonçalves, Rafaella A , Clarke, Julia R , Beckman, Danielle , Staniszewski, Agnieszka , Berman, Hanna , Guerra, Lorena A , Forny-Germano, Letícia , Meier, Shelby , Wilcock, Donna M , de Souza, Jorge M , Alves-Leon, Soniza , Prado, Vania F , Prado, Marco A M , Abisambra, Jose F , Tovar-Moll, Fernanda , Mattos, Paulo , Arancio, Ottavio , Ferreira, Sergio T , De Felice, Fernanda G
Format: Electronic Article Electronic Article
Language: English
Subjects:
Publisher: United States: Nature Publishing Group
ID: ISSN: 1078-8956
Link: https://www.ncbi.nlm.nih.gov/pubmed/30617325
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recordid: cdi_pubmedcentral_primary_oai_pubmedcentral_nih_gov_6327967
title: Exercise-linked FNDC5/irisin rescues synaptic plasticity and memory defects in Alzheimer’s models
format: Article
creator:
  • Lourenco, Mychael V
  • Frozza, Rudimar L
  • de Freitas, Guilherme B
  • Zhang, Hong
  • Kincheski, Grasielle C
  • Ribeiro, Felipe C
  • Gonçalves, Rafaella A
  • Clarke, Julia R
  • Beckman, Danielle
  • Staniszewski, Agnieszka
  • Berman, Hanna
  • Guerra, Lorena A
  • Forny-Germano, Letícia
  • Meier, Shelby
  • Wilcock, Donna M
  • de Souza, Jorge M
  • Alves-Leon, Soniza
  • Prado, Vania F
  • Prado, Marco A M
  • Abisambra, Jose F
  • Tovar-Moll, Fernanda
  • Mattos, Paulo
  • Arancio, Ottavio
  • Ferreira, Sergio T
  • De Felice, Fernanda G
subjects:
  • Adolescent
  • Adult
  • Aged
  • Alzheimer Disease - cerebrospinal fluid
  • Alzheimer Disease - genetics
  • Alzheimer Disease - metabolism
  • Alzheimer Disease - physiopathology
  • Alzheimer's disease
  • Alzheimers disease
  • Analysis
  • Animal models
  • Animals
  • Antibodies
  • Brain
  • Brain - metabolism
  • Brain - pathology
  • Brain research
  • Cerebrospinal fluid
  • Dementia
  • Disease Models, Animal
  • Down-Regulation
  • Exercise
  • Female
  • Fibronectin
  • Fibronectins
  • Fibronectins - cerebrospinal fluid
  • Fibronectins - genetics
  • Fibronectins - metabolism
  • FNDC5
  • Glucagon
  • Hippocampus
  • Humans
  • Immunology
  • Impairment
  • Insulin
  • irisin
  • Long-Term Potentiation
  • Male
  • Mass spectrometry
  • Membrane proteins
  • Memory
  • Memory Disorders - complications
  • Memory Disorders - physiopathology
  • Mice
  • Mice, Inbred C57BL
  • Middle Aged
  • Neuronal Plasticity
  • Neuroprotection
  • Neuroprotective Agents - pharmacology
  • Neuroprotective Agents - therapeutic use
  • Object recognition
  • Pattern recognition
  • Peptides
  • Physical Conditioning, Animal
  • Physical exercise
  • Plasma
  • Plasticity
  • Potentiation
  • Protein binding
  • Proteins
  • Recombinant Proteins - pharmacology
  • Recombinant Proteins - therapeutic use
  • RNA, Messenger - genetics
  • RNA, Messenger - metabolism
  • Scientific imaging
  • Signal Transduction
  • Synaptic plasticity
ispartof: Nature medicine, 2019, Vol.25 (1), p.165-175
description: Defective brain hormonal signaling has been associated with Alzheimer's disease (AD), a disorder characterized by synapse and memory failure. Irisin is an exercise-induced myokine released on cleavage of the membrane-bound precursor protein fibronectin type III domain-containing protein 5 (FNDC5), also expressed in the hippocampus. Here we show that FNDC5/irisin levels are reduced in AD hippocampi and cerebrospinal fluid, and in experimental AD models. Knockdown of brain FNDC5/irisin impairs long-term potentiation and novel object recognition memory in mice. Conversely, boosting brain levels of FNDC5/irisin rescues synaptic plasticity and memory in AD mouse models. Peripheral overexpression of FNDC5/irisin rescues memory impairment, whereas blockade of either peripheral or brain FNDC5/irisin attenuates the neuroprotective actions of physical exercise on synaptic plasticity and memory in AD mice. By showing that FNDC5/irisin is an important mediator of the beneficial effects of exercise in AD models, our findings place FNDC5/irisin as a novel agent capable of opposing synapse failure and memory impairment in AD.
language: eng
source:
identifier: ISSN: 1078-8956
fulltext: no_fulltext
issn:
  • 1078-8956
  • 1546-170X
url: Link


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titleExercise-linked FNDC5/irisin rescues synaptic plasticity and memory defects in Alzheimer’s models
creatorLourenco, Mychael V ; Frozza, Rudimar L ; de Freitas, Guilherme B ; Zhang, Hong ; Kincheski, Grasielle C ; Ribeiro, Felipe C ; Gonçalves, Rafaella A ; Clarke, Julia R ; Beckman, Danielle ; Staniszewski, Agnieszka ; Berman, Hanna ; Guerra, Lorena A ; Forny-Germano, Letícia ; Meier, Shelby ; Wilcock, Donna M ; de Souza, Jorge M ; Alves-Leon, Soniza ; Prado, Vania F ; Prado, Marco A M ; Abisambra, Jose F ; Tovar-Moll, Fernanda ; Mattos, Paulo ; Arancio, Ottavio ; Ferreira, Sergio T ; De Felice, Fernanda G
creatorcontribLourenco, Mychael V ; Frozza, Rudimar L ; de Freitas, Guilherme B ; Zhang, Hong ; Kincheski, Grasielle C ; Ribeiro, Felipe C ; Gonçalves, Rafaella A ; Clarke, Julia R ; Beckman, Danielle ; Staniszewski, Agnieszka ; Berman, Hanna ; Guerra, Lorena A ; Forny-Germano, Letícia ; Meier, Shelby ; Wilcock, Donna M ; de Souza, Jorge M ; Alves-Leon, Soniza ; Prado, Vania F ; Prado, Marco A M ; Abisambra, Jose F ; Tovar-Moll, Fernanda ; Mattos, Paulo ; Arancio, Ottavio ; Ferreira, Sergio T ; De Felice, Fernanda G
descriptionDefective brain hormonal signaling has been associated with Alzheimer's disease (AD), a disorder characterized by synapse and memory failure. Irisin is an exercise-induced myokine released on cleavage of the membrane-bound precursor protein fibronectin type III domain-containing protein 5 (FNDC5), also expressed in the hippocampus. Here we show that FNDC5/irisin levels are reduced in AD hippocampi and cerebrospinal fluid, and in experimental AD models. Knockdown of brain FNDC5/irisin impairs long-term potentiation and novel object recognition memory in mice. Conversely, boosting brain levels of FNDC5/irisin rescues synaptic plasticity and memory in AD mouse models. Peripheral overexpression of FNDC5/irisin rescues memory impairment, whereas blockade of either peripheral or brain FNDC5/irisin attenuates the neuroprotective actions of physical exercise on synaptic plasticity and memory in AD mice. By showing that FNDC5/irisin is an important mediator of the beneficial effects of exercise in AD models, our findings place FNDC5/irisin as a novel agent capable of opposing synapse failure and memory impairment in AD.
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languageeng
publisherUnited States: Nature Publishing Group
subjectAdolescent ; Adult ; Aged ; Alzheimer Disease - cerebrospinal fluid ; Alzheimer Disease - genetics ; Alzheimer Disease - metabolism ; Alzheimer Disease - physiopathology ; Alzheimer's disease ; Alzheimers disease ; Analysis ; Animal models ; Animals ; Antibodies ; Brain ; Brain - metabolism ; Brain - pathology ; Brain research ; Cerebrospinal fluid ; Dementia ; Disease Models, Animal ; Down-Regulation ; Exercise ; Female ; Fibronectin ; Fibronectins ; Fibronectins - cerebrospinal fluid ; Fibronectins - genetics ; Fibronectins - metabolism ; FNDC5 ; Glucagon ; Hippocampus ; Humans ; Immunology ; Impairment ; Insulin ; irisin ; Long-Term Potentiation ; Male ; Mass spectrometry ; Membrane proteins ; Memory ; Memory Disorders - complications ; Memory Disorders - physiopathology ; Mice ; Mice, Inbred C57BL ; Middle Aged ; Neuronal Plasticity ; Neuroprotection ; Neuroprotective Agents - pharmacology ; Neuroprotective Agents - therapeutic use ; Object recognition ; Pattern recognition ; Peptides ; Physical Conditioning, Animal ; Physical exercise ; Plasma ; Plasticity ; Potentiation ; Protein binding ; Proteins ; Recombinant Proteins - pharmacology ; Recombinant Proteins - therapeutic use ; RNA, Messenger - genetics ; RNA, Messenger - metabolism ; Scientific imaging ; Signal Transduction ; Synaptic plasticity
ispartofNature medicine, 2019, Vol.25 (1), p.165-175
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1Frozza, Rudimar L
2de Freitas, Guilherme B
3Zhang, Hong
4Kincheski, Grasielle C
5Ribeiro, Felipe C
6Gonçalves, Rafaella A
7Clarke, Julia R
8Beckman, Danielle
9Staniszewski, Agnieszka
10Berman, Hanna
11Guerra, Lorena A
12Forny-Germano, Letícia
13Meier, Shelby
14Wilcock, Donna M
15de Souza, Jorge M
16Alves-Leon, Soniza
17Prado, Vania F
18Prado, Marco A M
19Abisambra, Jose F
20Tovar-Moll, Fernanda
21Mattos, Paulo
22Arancio, Ottavio
23Ferreira, Sergio T
24De Felice, Fernanda G
title
0Exercise-linked FNDC5/irisin rescues synaptic plasticity and memory defects in Alzheimer’s models
1Nature medicine
addtitleNat Med
descriptionDefective brain hormonal signaling has been associated with Alzheimer's disease (AD), a disorder characterized by synapse and memory failure. Irisin is an exercise-induced myokine released on cleavage of the membrane-bound precursor protein fibronectin type III domain-containing protein 5 (FNDC5), also expressed in the hippocampus. Here we show that FNDC5/irisin levels are reduced in AD hippocampi and cerebrospinal fluid, and in experimental AD models. Knockdown of brain FNDC5/irisin impairs long-term potentiation and novel object recognition memory in mice. Conversely, boosting brain levels of FNDC5/irisin rescues synaptic plasticity and memory in AD mouse models. Peripheral overexpression of FNDC5/irisin rescues memory impairment, whereas blockade of either peripheral or brain FNDC5/irisin attenuates the neuroprotective actions of physical exercise on synaptic plasticity and memory in AD mice. By showing that FNDC5/irisin is an important mediator of the beneficial effects of exercise in AD models, our findings place FNDC5/irisin as a novel agent capable of opposing synapse failure and memory impairment in AD.
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1Adult
2Aged
3Alzheimer Disease - cerebrospinal fluid
4Alzheimer Disease - genetics
5Alzheimer Disease - metabolism
6Alzheimer Disease - physiopathology
7Alzheimer's disease
8Alzheimers disease
9Analysis
10Animal models
11Animals
12Antibodies
13Brain
14Brain - metabolism
15Brain - pathology
16Brain research
17Cerebrospinal fluid
18Dementia
19Disease Models, Animal
20Down-Regulation
21Exercise
22Female
23Fibronectin
24Fibronectins
25Fibronectins - cerebrospinal fluid
26Fibronectins - genetics
27Fibronectins - metabolism
28FNDC5
29Glucagon
30Hippocampus
31Humans
32Immunology
33Impairment
34Insulin
35irisin
36Long-Term Potentiation
37Male
38Mass spectrometry
39Membrane proteins
40Memory
41Memory Disorders - complications
42Memory Disorders - physiopathology
43Mice
44Mice, Inbred C57BL
45Middle Aged
46Neuronal Plasticity
47Neuroprotection
48Neuroprotective Agents - pharmacology
49Neuroprotective Agents - therapeutic use
50Object recognition
51Pattern recognition
52Peptides
53Physical Conditioning, Animal
54Physical exercise
55Plasma
56Plasticity
57Potentiation
58Protein binding
59Proteins
60Recombinant Proteins - pharmacology
61Recombinant Proteins - therapeutic use
62RNA, Messenger - genetics
63RNA, Messenger - metabolism
64Scientific imaging
65Signal Transduction
66Synaptic plasticity
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1Frozza, Rudimar L
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4Kincheski, Grasielle C
5Ribeiro, Felipe C
6Gonçalves, Rafaella A
7Clarke, Julia R
8Beckman, Danielle
9Staniszewski, Agnieszka
10Berman, Hanna
11Guerra, Lorena A
12Forny-Germano, Letícia
13Meier, Shelby
14Wilcock, Donna M
15de Souza, Jorge M
16Alves-Leon, Soniza
17Prado, Vania F
18Prado, Marco A M
19Abisambra, Jose F
20Tovar-Moll, Fernanda
21Mattos, Paulo
22Arancio, Ottavio
23Ferreira, Sergio T
24De Felice, Fernanda G
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titleExercise-linked FNDC5/irisin rescues synaptic plasticity and memory defects in Alzheimer’s models
authorLourenco, Mychael V ; Frozza, Rudimar L ; de Freitas, Guilherme B ; Zhang, Hong ; Kincheski, Grasielle C ; Ribeiro, Felipe C ; Gonçalves, Rafaella A ; Clarke, Julia R ; Beckman, Danielle ; Staniszewski, Agnieszka ; Berman, Hanna ; Guerra, Lorena A ; Forny-Germano, Letícia ; Meier, Shelby ; Wilcock, Donna M ; de Souza, Jorge M ; Alves-Leon, Soniza ; Prado, Vania F ; Prado, Marco A M ; Abisambra, Jose F ; Tovar-Moll, Fernanda ; Mattos, Paulo ; Arancio, Ottavio ; Ferreira, Sergio T ; De Felice, Fernanda G
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0Adolescent
1Adult
2Aged
3Alzheimer Disease - cerebrospinal fluid
4Alzheimer Disease - genetics
5Alzheimer Disease - metabolism
6Alzheimer Disease - physiopathology
7Alzheimer's disease
8Alzheimers disease
9Analysis
10Animal models
11Animals
12Antibodies
13Brain
14Brain - metabolism
15Brain - pathology
16Brain research
17Cerebrospinal fluid
18Dementia
19Disease Models, Animal
20Down-Regulation
21Exercise
22Female
23Fibronectin
24Fibronectins
25Fibronectins - cerebrospinal fluid
26Fibronectins - genetics
27Fibronectins - metabolism
28FNDC5
29Glucagon
30Hippocampus
31Humans
32Immunology
33Impairment
34Insulin
35irisin
36Long-Term Potentiation
37Male
38Mass spectrometry
39Membrane proteins
40Memory
41Memory Disorders - complications
42Memory Disorders - physiopathology
43Mice
44Mice, Inbred C57BL
45Middle Aged
46Neuronal Plasticity
47Neuroprotection
48Neuroprotective Agents - pharmacology
49Neuroprotective Agents - therapeutic use
50Object recognition
51Pattern recognition
52Peptides
53Physical Conditioning, Animal
54Physical exercise
55Plasma
56Plasticity
57Potentiation
58Protein binding
59Proteins
60Recombinant Proteins - pharmacology
61Recombinant Proteins - therapeutic use
62RNA, Messenger - genetics
63RNA, Messenger - metabolism
64Scientific imaging
65Signal Transduction
66Synaptic plasticity
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1Frozza, Rudimar L
2de Freitas, Guilherme B
3Zhang, Hong
4Kincheski, Grasielle C
5Ribeiro, Felipe C
6Gonçalves, Rafaella A
7Clarke, Julia R
8Beckman, Danielle
9Staniszewski, Agnieszka
10Berman, Hanna
11Guerra, Lorena A
12Forny-Germano, Letícia
13Meier, Shelby
14Wilcock, Donna M
15de Souza, Jorge M
16Alves-Leon, Soniza
17Prado, Vania F
18Prado, Marco A M
19Abisambra, Jose F
20Tovar-Moll, Fernanda
21Mattos, Paulo
22Arancio, Ottavio
23Ferreira, Sergio T
24De Felice, Fernanda G
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0Lourenco, Mychael V
1Frozza, Rudimar L
2de Freitas, Guilherme B
3Zhang, Hong
4Kincheski, Grasielle C
5Ribeiro, Felipe C
6Gonçalves, Rafaella A
7Clarke, Julia R
8Beckman, Danielle
9Staniszewski, Agnieszka
10Berman, Hanna
11Guerra, Lorena A
12Forny-Germano, Letícia
13Meier, Shelby
14Wilcock, Donna M
15de Souza, Jorge M
16Alves-Leon, Soniza
17Prado, Vania F
18Prado, Marco A M
19Abisambra, Jose F
20Tovar-Moll, Fernanda
21Mattos, Paulo
22Arancio, Ottavio
23Ferreira, Sergio T
24De Felice, Fernanda G
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pages165-175
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eissn1546-170X
notes
0M.V.L., R.L.F., O.A., S.T.F., and F.G.d.F. designed the study. M.V.L., R.L.F., G.B.d.F., H.Z., G.C.K, F.C.R., R.A.G., J.R.C., D.B., A.S., H.B., L.A.G., L.F.-G., S.M., and J.F.A. performed research. M.V.L., R.L.F., G.B.d.F., H.Z., D.B., A.S., S.M., J.F.A., O.A., S.T.F., and F.G.d.F. analyzed data. J.F.A., D.M.W., J.M.d.S., S.A.-L., V.F.P., M.A.M.P., F.T.-M., P.M., and O.A. contributed reagents, materials, and analysis tools. M.V.L., R.L.F., G.B.d.F., A.S, J.F.A., F.T-M., P.M., O.A., S.T.F., and F.G.d.F. analyzed and discussed results. M.V.L., R.L.F., S.T.F., and F.G.d.F. wrote the manuscript.
1Author Contributions
abstractDefective brain hormonal signaling has been associated with Alzheimer's disease (AD), a disorder characterized by synapse and memory failure. Irisin is an exercise-induced myokine released on cleavage of the membrane-bound precursor protein fibronectin type III domain-containing protein 5 (FNDC5), also expressed in the hippocampus. Here we show that FNDC5/irisin levels are reduced in AD hippocampi and cerebrospinal fluid, and in experimental AD models. Knockdown of brain FNDC5/irisin impairs long-term potentiation and novel object recognition memory in mice. Conversely, boosting brain levels of FNDC5/irisin rescues synaptic plasticity and memory in AD mouse models. Peripheral overexpression of FNDC5/irisin rescues memory impairment, whereas blockade of either peripheral or brain FNDC5/irisin attenuates the neuroprotective actions of physical exercise on synaptic plasticity and memory in AD mice. By showing that FNDC5/irisin is an important mediator of the beneficial effects of exercise in AD models, our findings place FNDC5/irisin as a novel agent capable of opposing synapse failure and memory impairment in AD.
copUnited States
pubNature Publishing Group
pmid30617325
doi10.1038/s41591-018-0275-4
tpages1
orcidid
0https://orcid.org/0000-0001-7160-9866
1https://orcid.org/0000-0001-6335-164X
2https://orcid.org/0000-0002-3028-5778
3https://orcid.org/0000-0001-6341-679X
4https://orcid.org/0000-0001-8358-0589
oafree_for_read