Some lumbar sympathetic neurons develop a glutamatergic phenotype after peripheral axotomy with a note on VGLUT2-positive perineuronal baskets

Autores
Brumovsky, Pablo Rodolfo; Seroogy, Kim B.; Lundgren, Kerstin H.; Watanabe, Masahiko; Hökfelt, Tomas; Gebhart, G.F.
Año de publicación
2011
Idioma
inglés
Tipo de recurso
artículo
Estado
versión publicada
Descripción
Glutamate is the main excitatory neurotransmitter in the nervous system, including in primary afferent neurons. However, to date a glutamatergic phenotype of autonomic neurons has not been described. Therefore, we explored the expression of vesicular glutamate transporter (VGLUT) types 1, 2 and 3 in lumbar sympathetic chain (LSC) and major pelvic ganglion (MPG) of naïve BALB/C mice, as well as after pelvic nerve axotomy (PNA), using immunohistochemistry and in situ hybridization. Colocalization with activating transcription factor-3 (ATF-3), tyrosine hydroxylase (TH), vesicular acetylcholine transporter (VAChT) and calcitonin gene-related peptide was also examined. Sham-PNA, sciatic nerve axotomy (SNA) or naïve mice were included. In naïve mice, VGLUT2-like immunoreactivity (LI) was only detected in fibers and varicosities in LSC and MPG; no ATF-3-immunoreactive (IR) neurons were visible. In contrast, PNA induced upregulation of VGLUT2 protein and transcript, as well as of ATF-3-LI in subpopulations of LSC neurons. Interestingly, VGLUT2-IR LSC neurons coexpressed ATF-3, and often lacked the noradrenergic marker TH. SNA only increased VGLUT2 protein and transcript in scattered LSC neurons. Neither PNA nor SNA upregulated VGLUT2 in MPG neurons. We also found perineuronal baskets immunoreactive either for VGLUT2 or the acetylcholinergic marker VAChT in non-PNA MPGs, usually around TH-IR neurons. VGLUT1-LI was restricted to some varicosities in MPGs, was absent in LSCs, and remained largely unaffected by PNA or SNA. This was confirmed by the lack of expression of VGLUT1 or VGLUT3 mRNAs in LSCs, even after PNA or SNA. Taken together, axotomy of visceral and non-visceral nerves results in a glutamatergic phenotype of some LSC neurons. In addition, we show previously non-described MPG perineuronal glutamatergic baskets.
Fil: Brumovsky, Pablo Rodolfo. Consejo Nacional de Investigaciones Científicas y Técnicas; Argentina. Universidad Austral; Argentina. Univeristy of Pittsburgh. School of Medicine; Estados Unidos
Fil: Seroogy, Kim B.. University of Cincinnati; Estados Unidos
Fil: Lundgren, Kerstin H.. University of Cincinnati; Estados Unidos
Fil: Watanabe, Masahiko. Hokkaido University School of Medicine; Japón
Fil: Hökfelt, Tomas. Karolinska Huddinge Hospital. Karolinska Institutet; Suecia
Fil: Gebhart, G.F.. Univeristy of Pittsburgh. School of Medicine; Estados Unidos
Materia
AUTONOMIC NEURONS
AXOTOMY
GLUTAMATE
NEUROPEPTIDES
PAIN
PELVIC NERVE
SENSORY NEURONS
VESICULAR GLUTAMATE TRANSPORTER
Nivel de accesibilidad
acceso abierto
Condiciones de uso
https://creativecommons.org/licenses/by-nc-sa/2.5/ar/
Repositorio
CONICET Digital (CONICET)
Institución
Consejo Nacional de Investigaciones Científicas y Técnicas
OAI Identificador
oai:ri.conicet.gov.ar:11336/192302

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oai_identifier_str oai:ri.conicet.gov.ar:11336/192302
network_acronym_str CONICETDig
repository_id_str 3498
network_name_str CONICET Digital (CONICET)
spelling Some lumbar sympathetic neurons develop a glutamatergic phenotype after peripheral axotomy with a note on VGLUT2-positive perineuronal basketsBrumovsky, Pablo RodolfoSeroogy, Kim B.Lundgren, Kerstin H.Watanabe, MasahikoHökfelt, TomasGebhart, G.F.AUTONOMIC NEURONSAXOTOMYGLUTAMATENEUROPEPTIDESPAINPELVIC NERVESENSORY NEURONSVESICULAR GLUTAMATE TRANSPORTERhttps://purl.org/becyt/ford/1.6https://purl.org/becyt/ford/1Glutamate is the main excitatory neurotransmitter in the nervous system, including in primary afferent neurons. However, to date a glutamatergic phenotype of autonomic neurons has not been described. Therefore, we explored the expression of vesicular glutamate transporter (VGLUT) types 1, 2 and 3 in lumbar sympathetic chain (LSC) and major pelvic ganglion (MPG) of naïve BALB/C mice, as well as after pelvic nerve axotomy (PNA), using immunohistochemistry and in situ hybridization. Colocalization with activating transcription factor-3 (ATF-3), tyrosine hydroxylase (TH), vesicular acetylcholine transporter (VAChT) and calcitonin gene-related peptide was also examined. Sham-PNA, sciatic nerve axotomy (SNA) or naïve mice were included. In naïve mice, VGLUT2-like immunoreactivity (LI) was only detected in fibers and varicosities in LSC and MPG; no ATF-3-immunoreactive (IR) neurons were visible. In contrast, PNA induced upregulation of VGLUT2 protein and transcript, as well as of ATF-3-LI in subpopulations of LSC neurons. Interestingly, VGLUT2-IR LSC neurons coexpressed ATF-3, and often lacked the noradrenergic marker TH. SNA only increased VGLUT2 protein and transcript in scattered LSC neurons. Neither PNA nor SNA upregulated VGLUT2 in MPG neurons. We also found perineuronal baskets immunoreactive either for VGLUT2 or the acetylcholinergic marker VAChT in non-PNA MPGs, usually around TH-IR neurons. VGLUT1-LI was restricted to some varicosities in MPGs, was absent in LSCs, and remained largely unaffected by PNA or SNA. This was confirmed by the lack of expression of VGLUT1 or VGLUT3 mRNAs in LSCs, even after PNA or SNA. Taken together, axotomy of visceral and non-visceral nerves results in a glutamatergic phenotype of some LSC neurons. In addition, we show previously non-described MPG perineuronal glutamatergic baskets.Fil: Brumovsky, Pablo Rodolfo. Consejo Nacional de Investigaciones Científicas y Técnicas; Argentina. Universidad Austral; Argentina. Univeristy of Pittsburgh. School of Medicine; Estados UnidosFil: Seroogy, Kim B.. University of Cincinnati; Estados UnidosFil: Lundgren, Kerstin H.. University of Cincinnati; Estados UnidosFil: Watanabe, Masahiko. Hokkaido University School of Medicine; JapónFil: Hökfelt, Tomas. Karolinska Huddinge Hospital. Karolinska Institutet; SueciaFil: Gebhart, G.F.. Univeristy of Pittsburgh. School of Medicine; Estados UnidosAcademic Press Inc Elsevier Science2011-08info:eu-repo/semantics/articleinfo:eu-repo/semantics/publishedVersionhttp://purl.org/coar/resource_type/c_6501info:ar-repo/semantics/articuloapplication/pdfapplication/pdfapplication/pdfhttp://hdl.handle.net/11336/192302Brumovsky, Pablo Rodolfo; Seroogy, Kim B.; Lundgren, Kerstin H.; Watanabe, Masahiko; Hökfelt, Tomas; et al.; Some lumbar sympathetic neurons develop a glutamatergic phenotype after peripheral axotomy with a note on VGLUT2-positive perineuronal baskets; Academic Press Inc Elsevier Science; Experimental Neurology; 230; 2; 8-2011; 258-2720014-4886CONICET DigitalCONICETenginfo:eu-repo/semantics/altIdentifier/url/https://www.sciencedirect.com/science/article/pii/S0014488611001713info:eu-repo/semantics/altIdentifier/doi/10.1016/j.expneurol.2011.05.004info:eu-repo/semantics/openAccesshttps://creativecommons.org/licenses/by-nc-sa/2.5/ar/reponame:CONICET Digital (CONICET)instname:Consejo Nacional de Investigaciones Científicas y Técnicas2025-09-29T10:15:51Zoai:ri.conicet.gov.ar:11336/192302instacron:CONICETInstitucionalhttp://ri.conicet.gov.ar/Organismo científico-tecnológicoNo correspondehttp://ri.conicet.gov.ar/oai/requestdasensio@conicet.gov.ar; lcarlino@conicet.gov.arArgentinaNo correspondeNo correspondeNo correspondeopendoar:34982025-09-29 10:15:51.404CONICET Digital (CONICET) - Consejo Nacional de Investigaciones Científicas y Técnicasfalse
dc.title.none.fl_str_mv Some lumbar sympathetic neurons develop a glutamatergic phenotype after peripheral axotomy with a note on VGLUT2-positive perineuronal baskets
title Some lumbar sympathetic neurons develop a glutamatergic phenotype after peripheral axotomy with a note on VGLUT2-positive perineuronal baskets
spellingShingle Some lumbar sympathetic neurons develop a glutamatergic phenotype after peripheral axotomy with a note on VGLUT2-positive perineuronal baskets
Brumovsky, Pablo Rodolfo
AUTONOMIC NEURONS
AXOTOMY
GLUTAMATE
NEUROPEPTIDES
PAIN
PELVIC NERVE
SENSORY NEURONS
VESICULAR GLUTAMATE TRANSPORTER
title_short Some lumbar sympathetic neurons develop a glutamatergic phenotype after peripheral axotomy with a note on VGLUT2-positive perineuronal baskets
title_full Some lumbar sympathetic neurons develop a glutamatergic phenotype after peripheral axotomy with a note on VGLUT2-positive perineuronal baskets
title_fullStr Some lumbar sympathetic neurons develop a glutamatergic phenotype after peripheral axotomy with a note on VGLUT2-positive perineuronal baskets
title_full_unstemmed Some lumbar sympathetic neurons develop a glutamatergic phenotype after peripheral axotomy with a note on VGLUT2-positive perineuronal baskets
title_sort Some lumbar sympathetic neurons develop a glutamatergic phenotype after peripheral axotomy with a note on VGLUT2-positive perineuronal baskets
dc.creator.none.fl_str_mv Brumovsky, Pablo Rodolfo
Seroogy, Kim B.
Lundgren, Kerstin H.
Watanabe, Masahiko
Hökfelt, Tomas
Gebhart, G.F.
author Brumovsky, Pablo Rodolfo
author_facet Brumovsky, Pablo Rodolfo
Seroogy, Kim B.
Lundgren, Kerstin H.
Watanabe, Masahiko
Hökfelt, Tomas
Gebhart, G.F.
author_role author
author2 Seroogy, Kim B.
Lundgren, Kerstin H.
Watanabe, Masahiko
Hökfelt, Tomas
Gebhart, G.F.
author2_role author
author
author
author
author
dc.subject.none.fl_str_mv AUTONOMIC NEURONS
AXOTOMY
GLUTAMATE
NEUROPEPTIDES
PAIN
PELVIC NERVE
SENSORY NEURONS
VESICULAR GLUTAMATE TRANSPORTER
topic AUTONOMIC NEURONS
AXOTOMY
GLUTAMATE
NEUROPEPTIDES
PAIN
PELVIC NERVE
SENSORY NEURONS
VESICULAR GLUTAMATE TRANSPORTER
purl_subject.fl_str_mv https://purl.org/becyt/ford/1.6
https://purl.org/becyt/ford/1
dc.description.none.fl_txt_mv Glutamate is the main excitatory neurotransmitter in the nervous system, including in primary afferent neurons. However, to date a glutamatergic phenotype of autonomic neurons has not been described. Therefore, we explored the expression of vesicular glutamate transporter (VGLUT) types 1, 2 and 3 in lumbar sympathetic chain (LSC) and major pelvic ganglion (MPG) of naïve BALB/C mice, as well as after pelvic nerve axotomy (PNA), using immunohistochemistry and in situ hybridization. Colocalization with activating transcription factor-3 (ATF-3), tyrosine hydroxylase (TH), vesicular acetylcholine transporter (VAChT) and calcitonin gene-related peptide was also examined. Sham-PNA, sciatic nerve axotomy (SNA) or naïve mice were included. In naïve mice, VGLUT2-like immunoreactivity (LI) was only detected in fibers and varicosities in LSC and MPG; no ATF-3-immunoreactive (IR) neurons were visible. In contrast, PNA induced upregulation of VGLUT2 protein and transcript, as well as of ATF-3-LI in subpopulations of LSC neurons. Interestingly, VGLUT2-IR LSC neurons coexpressed ATF-3, and often lacked the noradrenergic marker TH. SNA only increased VGLUT2 protein and transcript in scattered LSC neurons. Neither PNA nor SNA upregulated VGLUT2 in MPG neurons. We also found perineuronal baskets immunoreactive either for VGLUT2 or the acetylcholinergic marker VAChT in non-PNA MPGs, usually around TH-IR neurons. VGLUT1-LI was restricted to some varicosities in MPGs, was absent in LSCs, and remained largely unaffected by PNA or SNA. This was confirmed by the lack of expression of VGLUT1 or VGLUT3 mRNAs in LSCs, even after PNA or SNA. Taken together, axotomy of visceral and non-visceral nerves results in a glutamatergic phenotype of some LSC neurons. In addition, we show previously non-described MPG perineuronal glutamatergic baskets.
Fil: Brumovsky, Pablo Rodolfo. Consejo Nacional de Investigaciones Científicas y Técnicas; Argentina. Universidad Austral; Argentina. Univeristy of Pittsburgh. School of Medicine; Estados Unidos
Fil: Seroogy, Kim B.. University of Cincinnati; Estados Unidos
Fil: Lundgren, Kerstin H.. University of Cincinnati; Estados Unidos
Fil: Watanabe, Masahiko. Hokkaido University School of Medicine; Japón
Fil: Hökfelt, Tomas. Karolinska Huddinge Hospital. Karolinska Institutet; Suecia
Fil: Gebhart, G.F.. Univeristy of Pittsburgh. School of Medicine; Estados Unidos
description Glutamate is the main excitatory neurotransmitter in the nervous system, including in primary afferent neurons. However, to date a glutamatergic phenotype of autonomic neurons has not been described. Therefore, we explored the expression of vesicular glutamate transporter (VGLUT) types 1, 2 and 3 in lumbar sympathetic chain (LSC) and major pelvic ganglion (MPG) of naïve BALB/C mice, as well as after pelvic nerve axotomy (PNA), using immunohistochemistry and in situ hybridization. Colocalization with activating transcription factor-3 (ATF-3), tyrosine hydroxylase (TH), vesicular acetylcholine transporter (VAChT) and calcitonin gene-related peptide was also examined. Sham-PNA, sciatic nerve axotomy (SNA) or naïve mice were included. In naïve mice, VGLUT2-like immunoreactivity (LI) was only detected in fibers and varicosities in LSC and MPG; no ATF-3-immunoreactive (IR) neurons were visible. In contrast, PNA induced upregulation of VGLUT2 protein and transcript, as well as of ATF-3-LI in subpopulations of LSC neurons. Interestingly, VGLUT2-IR LSC neurons coexpressed ATF-3, and often lacked the noradrenergic marker TH. SNA only increased VGLUT2 protein and transcript in scattered LSC neurons. Neither PNA nor SNA upregulated VGLUT2 in MPG neurons. We also found perineuronal baskets immunoreactive either for VGLUT2 or the acetylcholinergic marker VAChT in non-PNA MPGs, usually around TH-IR neurons. VGLUT1-LI was restricted to some varicosities in MPGs, was absent in LSCs, and remained largely unaffected by PNA or SNA. This was confirmed by the lack of expression of VGLUT1 or VGLUT3 mRNAs in LSCs, even after PNA or SNA. Taken together, axotomy of visceral and non-visceral nerves results in a glutamatergic phenotype of some LSC neurons. In addition, we show previously non-described MPG perineuronal glutamatergic baskets.
publishDate 2011
dc.date.none.fl_str_mv 2011-08
dc.type.none.fl_str_mv info:eu-repo/semantics/article
info:eu-repo/semantics/publishedVersion
http://purl.org/coar/resource_type/c_6501
info:ar-repo/semantics/articulo
format article
status_str publishedVersion
dc.identifier.none.fl_str_mv http://hdl.handle.net/11336/192302
Brumovsky, Pablo Rodolfo; Seroogy, Kim B.; Lundgren, Kerstin H.; Watanabe, Masahiko; Hökfelt, Tomas; et al.; Some lumbar sympathetic neurons develop a glutamatergic phenotype after peripheral axotomy with a note on VGLUT2-positive perineuronal baskets; Academic Press Inc Elsevier Science; Experimental Neurology; 230; 2; 8-2011; 258-272
0014-4886
CONICET Digital
CONICET
url http://hdl.handle.net/11336/192302
identifier_str_mv Brumovsky, Pablo Rodolfo; Seroogy, Kim B.; Lundgren, Kerstin H.; Watanabe, Masahiko; Hökfelt, Tomas; et al.; Some lumbar sympathetic neurons develop a glutamatergic phenotype after peripheral axotomy with a note on VGLUT2-positive perineuronal baskets; Academic Press Inc Elsevier Science; Experimental Neurology; 230; 2; 8-2011; 258-272
0014-4886
CONICET Digital
CONICET
dc.language.none.fl_str_mv eng
language eng
dc.relation.none.fl_str_mv info:eu-repo/semantics/altIdentifier/url/https://www.sciencedirect.com/science/article/pii/S0014488611001713
info:eu-repo/semantics/altIdentifier/doi/10.1016/j.expneurol.2011.05.004
dc.rights.none.fl_str_mv info:eu-repo/semantics/openAccess
https://creativecommons.org/licenses/by-nc-sa/2.5/ar/
eu_rights_str_mv openAccess
rights_invalid_str_mv https://creativecommons.org/licenses/by-nc-sa/2.5/ar/
dc.format.none.fl_str_mv application/pdf
application/pdf
application/pdf
dc.publisher.none.fl_str_mv Academic Press Inc Elsevier Science
publisher.none.fl_str_mv Academic Press Inc Elsevier Science
dc.source.none.fl_str_mv reponame:CONICET Digital (CONICET)
instname:Consejo Nacional de Investigaciones Científicas y Técnicas
reponame_str CONICET Digital (CONICET)
collection CONICET Digital (CONICET)
instname_str Consejo Nacional de Investigaciones Científicas y Técnicas
repository.name.fl_str_mv CONICET Digital (CONICET) - Consejo Nacional de Investigaciones Científicas y Técnicas
repository.mail.fl_str_mv dasensio@conicet.gov.ar; lcarlino@conicet.gov.ar
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