Paracellular nutrient absorption is higher in bats than rodents: integrating from intact animals to the molecular level

Autores
Price, Edwin R.; Rott, Katherine H.; Caviedes Vidal, Enrique Juan Raul; Karasov, William H.
Año de publicación
2014
Idioma
inglés
Tipo de recurso
artículo
Estado
versión publicada
Descripción
Flying vertebrates have been hypothesized to rely heavily on paracellular absorption of nutrients to compensate for having smaller intestines than non-flyers. We tested this hypothesis in an insectivorous bat (Myotis lucifugus) and two insect-eating rodents (Onychomys leucogaster and Peromyscus leucopus). In intact animals, the fractional absorption of orally dosed l-arabinose (Mr 150) was 82% in M. lucifugus, which was more than twice that of the rodents. Absorption of creatinine (Mr 113) was greater than 50% for all species and did not differ between M. lucifugus and the rodents. We also conducted intestinal luminal perfusions on anesthetized animals. Absorption of l-arabinose per nominal surface area in M. lucifugus was nearly double that of the rodents, while absorption of creatinine was not different among species. Using an everted sleeve preparation, we demonstrated that high concentrations of l-arabinose and creatinine did not inhibit their own uptake, validating their use as passive, paracellular probes. Histological measurements indicated that M. lucifugus has more cells, and presumably more tight junctions, per nominal surface area than P. leucopus. This seems unlikely to explain entirely the higher absorption of l-arabinose in M. lucifugus during perfusions, because l-arabinose absorption normalized to the number of enterocytes was still double that of P. leucopus. As an alternative, we investigated tight junction gene expression. M. lucifugus had higher expression of claudin-1 and claudin-15, and lower expression of claudin-2 relative to P. leucopus. Expression of claudin-7 and occludin did not differ among species. Taken together, our results support the hypothesis that bats have evolved higher paracellular nutrient absorption than non-flying animals, and that this phenomenon might be driven by both histological characteristics and differences in tight junction gene expression.
Fil: Price, Edwin R.. University Of Wisconsin; Estados Unidos
Fil: Rott, Katherine H.. University Of Wisconsin; Estados Unidos
Fil: Caviedes Vidal, Enrique Juan Raul. Universidad Nacional de San Luis. Facultad de Quimica, Bioquimica y Farmacia. Departamento de Bioquímica y Ciencias Biológicas; Argentina. Consejo Nacional de Investigaciones Científicas y Técnicas. Centro Científico Tecnológico San Luis. Instituto Multidisciplinario de Investigaciones Biológicas de San Luis; Argentina
Fil: Karasov, William H.. University Of Wisconsin; Estados Unidos
Materia
Paracellular absorption
Perfusion
Arabinose
Comparative transcriptomics
Claudin
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:11336/14502

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oai_identifier_str oai:ri.conicet.gov.ar:11336/14502
network_acronym_str CONICETDig
repository_id_str 3498
network_name_str CONICET Digital (CONICET)
spelling Paracellular nutrient absorption is higher in bats than rodents: integrating from intact animals to the molecular levelPrice, Edwin R.Rott, Katherine H.Caviedes Vidal, Enrique Juan RaulKarasov, William H.Paracellular absorptionPerfusionArabinoseComparative transcriptomicsClaudinhttps://purl.org/becyt/ford/1.6https://purl.org/becyt/ford/1Flying vertebrates have been hypothesized to rely heavily on paracellular absorption of nutrients to compensate for having smaller intestines than non-flyers. We tested this hypothesis in an insectivorous bat (Myotis lucifugus) and two insect-eating rodents (Onychomys leucogaster and Peromyscus leucopus). In intact animals, the fractional absorption of orally dosed l-arabinose (Mr 150) was 82% in M. lucifugus, which was more than twice that of the rodents. Absorption of creatinine (Mr 113) was greater than 50% for all species and did not differ between M. lucifugus and the rodents. We also conducted intestinal luminal perfusions on anesthetized animals. Absorption of l-arabinose per nominal surface area in M. lucifugus was nearly double that of the rodents, while absorption of creatinine was not different among species. Using an everted sleeve preparation, we demonstrated that high concentrations of l-arabinose and creatinine did not inhibit their own uptake, validating their use as passive, paracellular probes. Histological measurements indicated that M. lucifugus has more cells, and presumably more tight junctions, per nominal surface area than P. leucopus. This seems unlikely to explain entirely the higher absorption of l-arabinose in M. lucifugus during perfusions, because l-arabinose absorption normalized to the number of enterocytes was still double that of P. leucopus. As an alternative, we investigated tight junction gene expression. M. lucifugus had higher expression of claudin-1 and claudin-15, and lower expression of claudin-2 relative to P. leucopus. Expression of claudin-7 and occludin did not differ among species. Taken together, our results support the hypothesis that bats have evolved higher paracellular nutrient absorption than non-flying animals, and that this phenomenon might be driven by both histological characteristics and differences in tight junction gene expression.Fil: Price, Edwin R.. University Of Wisconsin; Estados UnidosFil: Rott, Katherine H.. University Of Wisconsin; Estados UnidosFil: Caviedes Vidal, Enrique Juan Raul. Universidad Nacional de San Luis. Facultad de Quimica, Bioquimica y Farmacia. Departamento de Bioquímica y Ciencias Biológicas; Argentina. Consejo Nacional de Investigaciones Científicas y Técnicas. Centro Científico Tecnológico San Luis. Instituto Multidisciplinario de Investigaciones Biológicas de San Luis; ArgentinaFil: Karasov, William H.. University Of Wisconsin; Estados UnidosCompany of Biologists2014-06info:eu-repo/semantics/articleinfo:eu-repo/semantics/publishedVersionhttp://purl.org/coar/resource_type/c_6501info:ar-repo/semantics/articuloapplication/pdfapplication/pdfhttp://hdl.handle.net/11336/14502Price, Edwin R.; Rott, Katherine H.; Caviedes Vidal, Enrique Juan Raul; Karasov, William H.; Paracellular nutrient absorption is higher in bats than rodents: integrating from intact animals to the molecular level; Company of Biologists; Journal of Experimental Biology; 217; 19; 6-2014; 3483-34920022-09491477-9145enginfo:eu-repo/semantics/altIdentifier/url/http://jeb.biologists.org/content/217/19/3483info:eu-repo/semantics/altIdentifier/doi/10.1242/jeb.105619info:eu-repo/semantics/openAccesshttps://creativecommons.org/licenses/by-nc-sa/2.5/ar/reponame:CONICET Digital (CONICET)instname:Consejo Nacional de Investigaciones Científicas y Técnicas2025-09-29T09:42:38Zoai:ri.conicet.gov.ar:11336/14502instacron: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 09:42:38.61CONICET Digital (CONICET) - Consejo Nacional de Investigaciones Científicas y Técnicasfalse
dc.title.none.fl_str_mv Paracellular nutrient absorption is higher in bats than rodents: integrating from intact animals to the molecular level
title Paracellular nutrient absorption is higher in bats than rodents: integrating from intact animals to the molecular level
spellingShingle Paracellular nutrient absorption is higher in bats than rodents: integrating from intact animals to the molecular level
Price, Edwin R.
Paracellular absorption
Perfusion
Arabinose
Comparative transcriptomics
Claudin
title_short Paracellular nutrient absorption is higher in bats than rodents: integrating from intact animals to the molecular level
title_full Paracellular nutrient absorption is higher in bats than rodents: integrating from intact animals to the molecular level
title_fullStr Paracellular nutrient absorption is higher in bats than rodents: integrating from intact animals to the molecular level
title_full_unstemmed Paracellular nutrient absorption is higher in bats than rodents: integrating from intact animals to the molecular level
title_sort Paracellular nutrient absorption is higher in bats than rodents: integrating from intact animals to the molecular level
dc.creator.none.fl_str_mv Price, Edwin R.
Rott, Katherine H.
Caviedes Vidal, Enrique Juan Raul
Karasov, William H.
author Price, Edwin R.
author_facet Price, Edwin R.
Rott, Katherine H.
Caviedes Vidal, Enrique Juan Raul
Karasov, William H.
author_role author
author2 Rott, Katherine H.
Caviedes Vidal, Enrique Juan Raul
Karasov, William H.
author2_role author
author
author
dc.subject.none.fl_str_mv Paracellular absorption
Perfusion
Arabinose
Comparative transcriptomics
Claudin
topic Paracellular absorption
Perfusion
Arabinose
Comparative transcriptomics
Claudin
purl_subject.fl_str_mv https://purl.org/becyt/ford/1.6
https://purl.org/becyt/ford/1
dc.description.none.fl_txt_mv Flying vertebrates have been hypothesized to rely heavily on paracellular absorption of nutrients to compensate for having smaller intestines than non-flyers. We tested this hypothesis in an insectivorous bat (Myotis lucifugus) and two insect-eating rodents (Onychomys leucogaster and Peromyscus leucopus). In intact animals, the fractional absorption of orally dosed l-arabinose (Mr 150) was 82% in M. lucifugus, which was more than twice that of the rodents. Absorption of creatinine (Mr 113) was greater than 50% for all species and did not differ between M. lucifugus and the rodents. We also conducted intestinal luminal perfusions on anesthetized animals. Absorption of l-arabinose per nominal surface area in M. lucifugus was nearly double that of the rodents, while absorption of creatinine was not different among species. Using an everted sleeve preparation, we demonstrated that high concentrations of l-arabinose and creatinine did not inhibit their own uptake, validating their use as passive, paracellular probes. Histological measurements indicated that M. lucifugus has more cells, and presumably more tight junctions, per nominal surface area than P. leucopus. This seems unlikely to explain entirely the higher absorption of l-arabinose in M. lucifugus during perfusions, because l-arabinose absorption normalized to the number of enterocytes was still double that of P. leucopus. As an alternative, we investigated tight junction gene expression. M. lucifugus had higher expression of claudin-1 and claudin-15, and lower expression of claudin-2 relative to P. leucopus. Expression of claudin-7 and occludin did not differ among species. Taken together, our results support the hypothesis that bats have evolved higher paracellular nutrient absorption than non-flying animals, and that this phenomenon might be driven by both histological characteristics and differences in tight junction gene expression.
Fil: Price, Edwin R.. University Of Wisconsin; Estados Unidos
Fil: Rott, Katherine H.. University Of Wisconsin; Estados Unidos
Fil: Caviedes Vidal, Enrique Juan Raul. Universidad Nacional de San Luis. Facultad de Quimica, Bioquimica y Farmacia. Departamento de Bioquímica y Ciencias Biológicas; Argentina. Consejo Nacional de Investigaciones Científicas y Técnicas. Centro Científico Tecnológico San Luis. Instituto Multidisciplinario de Investigaciones Biológicas de San Luis; Argentina
Fil: Karasov, William H.. University Of Wisconsin; Estados Unidos
description Flying vertebrates have been hypothesized to rely heavily on paracellular absorption of nutrients to compensate for having smaller intestines than non-flyers. We tested this hypothesis in an insectivorous bat (Myotis lucifugus) and two insect-eating rodents (Onychomys leucogaster and Peromyscus leucopus). In intact animals, the fractional absorption of orally dosed l-arabinose (Mr 150) was 82% in M. lucifugus, which was more than twice that of the rodents. Absorption of creatinine (Mr 113) was greater than 50% for all species and did not differ between M. lucifugus and the rodents. We also conducted intestinal luminal perfusions on anesthetized animals. Absorption of l-arabinose per nominal surface area in M. lucifugus was nearly double that of the rodents, while absorption of creatinine was not different among species. Using an everted sleeve preparation, we demonstrated that high concentrations of l-arabinose and creatinine did not inhibit their own uptake, validating their use as passive, paracellular probes. Histological measurements indicated that M. lucifugus has more cells, and presumably more tight junctions, per nominal surface area than P. leucopus. This seems unlikely to explain entirely the higher absorption of l-arabinose in M. lucifugus during perfusions, because l-arabinose absorption normalized to the number of enterocytes was still double that of P. leucopus. As an alternative, we investigated tight junction gene expression. M. lucifugus had higher expression of claudin-1 and claudin-15, and lower expression of claudin-2 relative to P. leucopus. Expression of claudin-7 and occludin did not differ among species. Taken together, our results support the hypothesis that bats have evolved higher paracellular nutrient absorption than non-flying animals, and that this phenomenon might be driven by both histological characteristics and differences in tight junction gene expression.
publishDate 2014
dc.date.none.fl_str_mv 2014-06
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/11336/14502
Price, Edwin R.; Rott, Katherine H.; Caviedes Vidal, Enrique Juan Raul; Karasov, William H.; Paracellular nutrient absorption is higher in bats than rodents: integrating from intact animals to the molecular level; Company of Biologists; Journal of Experimental Biology; 217; 19; 6-2014; 3483-3492
0022-0949
1477-9145
url http://hdl.handle.net/11336/14502
identifier_str_mv Price, Edwin R.; Rott, Katherine H.; Caviedes Vidal, Enrique Juan Raul; Karasov, William H.; Paracellular nutrient absorption is higher in bats than rodents: integrating from intact animals to the molecular level; Company of Biologists; Journal of Experimental Biology; 217; 19; 6-2014; 3483-3492
0022-0949
1477-9145
dc.language.none.fl_str_mv eng
language eng
dc.relation.none.fl_str_mv info:eu-repo/semantics/altIdentifier/url/http://jeb.biologists.org/content/217/19/3483
info:eu-repo/semantics/altIdentifier/doi/10.1242/jeb.105619
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
dc.publisher.none.fl_str_mv Company of Biologists
publisher.none.fl_str_mv Company of Biologists
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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