Vagal afferents are essential for maximal resection-induced intestinal adaptive growth in orally fed rats

David W Nelson; Xiaowen Liu; Jens Juul Holst; Helen E Raybould; Denise M Ney

doi:10.1152/ajpregu.00247.2006

Vagal afferents are essential for maximal resection-induced intestinal adaptive growth in orally fed rats

David W Nelson, Xiaowen Liu, Jens Juul Holst, Helen E Raybould, Denise M Ney

Endocrinology and Metabolism

9 Citationer (Scopus)

Abstract

Small bowel resection stimulates intestinal adaptive growth by a neuroendocrine process thought to involve both sympathetic and parasympathetic innervation and enterotrophic hormones such as glucagon-like peptide-2 (GLP-2). We investigated whether capsaicin-sensitive vagal afferent neurons are essential for maximal resection-induced intestinal growth. Rats received systemic or perivagal capsaicin or ganglionectomy before 70% midjejunoileal resection or transection and were fed orally or by total parenteral nutrition (TPN) for 7 days after surgery. Growth of residual bowel was assessed by changes in mucosal mass, protein, DNA, and histology. Both systemic and perivagal capsaicin significantly attenuated by 48-100% resection-induced increases in ileal mucosal mass, protein, and DNA in rats fed orally. Villus height was significantly reduced in resected rats given capsaicin compared with vehicle. Sucrase specific activity in jejunal mucosa was not significantly different; ileal mucosal sucrase specific activity was significantly increased by resection in capsaicin-treated rats. Capsaicin did not alter the 57% increase in ileal proglucagon mRNA or the 150% increase in plasma concentration of bioactive GLP-2 resulting from resection in orally fed rats. Ablation of spinal/splanchnic innervation by ganglionectomy failed to attenuate resection-induced adaptive growth. In TPN rats, capsaicin did not attenuate resection-induced mucosal growth. We conclude that vagal afferents are not essential for GLP-2 secretion when the ileum has direct contact with luminal nutrients after resection. In summary, vagal afferent neurons are essential for maximal resection-induced intestinal adaptation through a mechanism that appears to involve stimulation by luminal nutrients.

Originalsprog	Engelsk
Tidsskrift	American Journal of Physiology: Regulatory, Integrative and Comparative Physiology
Vol/bind	291
Udgave nummer	5
Sider (fra-til)	R1256-64
ISSN	0363-6119
DOI	https://doi.org/10.1152/ajpregu.00247.2006
Status	Udgivet - nov. 2006

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10.1152/ajpregu.00247.2006

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Vagal afferents are essential for maximal resection-induced intestinal adaptive growth in orally fed rats. / Nelson, David W; Liu, Xiaowen; Holst, Jens Juul et al.

I: American Journal of Physiology: Regulatory, Integrative and Comparative Physiology, Bind 291, Nr. 5, 11.2006, s. R1256-64.

Publikation: Bidrag til tidsskrift › Tidsskriftartikel › Forskning › peer review

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title = "Vagal afferents are essential for maximal resection-induced intestinal adaptive growth in orally fed rats",

abstract = "Small bowel resection stimulates intestinal adaptive growth by a neuroendocrine process thought to involve both sympathetic and parasympathetic innervation and enterotrophic hormones such as glucagon-like peptide-2 (GLP-2). We investigated whether capsaicin-sensitive vagal afferent neurons are essential for maximal resection-induced intestinal growth. Rats received systemic or perivagal capsaicin or ganglionectomy before 70% midjejunoileal resection or transection and were fed orally or by total parenteral nutrition (TPN) for 7 days after surgery. Growth of residual bowel was assessed by changes in mucosal mass, protein, DNA, and histology. Both systemic and perivagal capsaicin significantly attenuated by 48-100% resection-induced increases in ileal mucosal mass, protein, and DNA in rats fed orally. Villus height was significantly reduced in resected rats given capsaicin compared with vehicle. Sucrase specific activity in jejunal mucosa was not significantly different; ileal mucosal sucrase specific activity was significantly increased by resection in capsaicin-treated rats. Capsaicin did not alter the 57% increase in ileal proglucagon mRNA or the 150% increase in plasma concentration of bioactive GLP-2 resulting from resection in orally fed rats. Ablation of spinal/splanchnic innervation by ganglionectomy failed to attenuate resection-induced adaptive growth. In TPN rats, capsaicin did not attenuate resection-induced mucosal growth. We conclude that vagal afferents are not essential for GLP-2 secretion when the ileum has direct contact with luminal nutrients after resection. In summary, vagal afferent neurons are essential for maximal resection-induced intestinal adaptation through a mechanism that appears to involve stimulation by luminal nutrients.",

keywords = "Adaptation, Physiological, Animals, Body Weight, Capsaicin, Enteral Nutrition, Ganglionectomy, Glucagon-Like Peptide 2, Ileum, Intestinal Mucosa, Intestines, Jejunum, Male, Neurons, Afferent, Parenteral Nutrition, Proglucagon, RNA, Messenger, Rats, Rats, Sprague-Dawley, Serine Endopeptidases, Sucrase, Vagus Nerve",

author = "Nelson, {David W} and Xiaowen Liu and Holst, {Jens Juul} and Raybould, {Helen E} and Ney, {Denise M}",

year = "2006",

month = nov,

doi = "10.1152/ajpregu.00247.2006",

language = "English",

volume = "291",

pages = "R1256--64",

journal = "American Journal of Physiology - Regulatory Integrative and Comparative Physiology",

issn = "0363-6119",

publisher = "American Physiological Society",

number = "5",

}

TY - JOUR

T1 - Vagal afferents are essential for maximal resection-induced intestinal adaptive growth in orally fed rats

AU - Nelson, David W

AU - Liu, Xiaowen

AU - Holst, Jens Juul

AU - Raybould, Helen E

AU - Ney, Denise M

PY - 2006/11

Y1 - 2006/11

N2 - Small bowel resection stimulates intestinal adaptive growth by a neuroendocrine process thought to involve both sympathetic and parasympathetic innervation and enterotrophic hormones such as glucagon-like peptide-2 (GLP-2). We investigated whether capsaicin-sensitive vagal afferent neurons are essential for maximal resection-induced intestinal growth. Rats received systemic or perivagal capsaicin or ganglionectomy before 70% midjejunoileal resection or transection and were fed orally or by total parenteral nutrition (TPN) for 7 days after surgery. Growth of residual bowel was assessed by changes in mucosal mass, protein, DNA, and histology. Both systemic and perivagal capsaicin significantly attenuated by 48-100% resection-induced increases in ileal mucosal mass, protein, and DNA in rats fed orally. Villus height was significantly reduced in resected rats given capsaicin compared with vehicle. Sucrase specific activity in jejunal mucosa was not significantly different; ileal mucosal sucrase specific activity was significantly increased by resection in capsaicin-treated rats. Capsaicin did not alter the 57% increase in ileal proglucagon mRNA or the 150% increase in plasma concentration of bioactive GLP-2 resulting from resection in orally fed rats. Ablation of spinal/splanchnic innervation by ganglionectomy failed to attenuate resection-induced adaptive growth. In TPN rats, capsaicin did not attenuate resection-induced mucosal growth. We conclude that vagal afferents are not essential for GLP-2 secretion when the ileum has direct contact with luminal nutrients after resection. In summary, vagal afferent neurons are essential for maximal resection-induced intestinal adaptation through a mechanism that appears to involve stimulation by luminal nutrients.

AB - Small bowel resection stimulates intestinal adaptive growth by a neuroendocrine process thought to involve both sympathetic and parasympathetic innervation and enterotrophic hormones such as glucagon-like peptide-2 (GLP-2). We investigated whether capsaicin-sensitive vagal afferent neurons are essential for maximal resection-induced intestinal growth. Rats received systemic or perivagal capsaicin or ganglionectomy before 70% midjejunoileal resection or transection and were fed orally or by total parenteral nutrition (TPN) for 7 days after surgery. Growth of residual bowel was assessed by changes in mucosal mass, protein, DNA, and histology. Both systemic and perivagal capsaicin significantly attenuated by 48-100% resection-induced increases in ileal mucosal mass, protein, and DNA in rats fed orally. Villus height was significantly reduced in resected rats given capsaicin compared with vehicle. Sucrase specific activity in jejunal mucosa was not significantly different; ileal mucosal sucrase specific activity was significantly increased by resection in capsaicin-treated rats. Capsaicin did not alter the 57% increase in ileal proglucagon mRNA or the 150% increase in plasma concentration of bioactive GLP-2 resulting from resection in orally fed rats. Ablation of spinal/splanchnic innervation by ganglionectomy failed to attenuate resection-induced adaptive growth. In TPN rats, capsaicin did not attenuate resection-induced mucosal growth. We conclude that vagal afferents are not essential for GLP-2 secretion when the ileum has direct contact with luminal nutrients after resection. In summary, vagal afferent neurons are essential for maximal resection-induced intestinal adaptation through a mechanism that appears to involve stimulation by luminal nutrients.

KW - Adaptation, Physiological

KW - Animals

KW - Body Weight

KW - Capsaicin

KW - Enteral Nutrition

KW - Ganglionectomy

KW - Glucagon-Like Peptide 2

KW - Ileum

KW - Intestinal Mucosa

KW - Intestines

KW - Jejunum

KW - Male

KW - Neurons, Afferent

KW - Parenteral Nutrition

KW - Proglucagon

KW - RNA, Messenger

KW - Rats

KW - Rats, Sprague-Dawley

KW - Serine Endopeptidases

KW - Sucrase

KW - Vagus Nerve

U2 - 10.1152/ajpregu.00247.2006

DO - 10.1152/ajpregu.00247.2006

M3 - Journal article

C2 - 17028287

SN - 0363-6119

VL - 291

SP - R1256-64

JO - American Journal of Physiology - Regulatory Integrative and Comparative Physiology

JF - American Journal of Physiology - Regulatory Integrative and Comparative Physiology

IS - 5

ER -

Vagal afferents are essential for maximal resection-induced intestinal adaptive growth in orally fed rats

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