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Portal glucose infusion in the mouse induces hypoglycemia: evidence that the hepatoportal glucose sensor stimulates glucose utilization.
Abstract
To analyze the role of the murine hepatoportal glucose sensor in the control of whole-body glucose metabolism, we infused glucose at a rate corresponding to the endogenous glucose production rate through the portal vein of conscious mice (Po-mice) that were fasted for 6 h. Mice infused with glucose at the same rate through the femoral vein (Fe-mice) and mice infused with a saline solution (Sal-mice) were used as controls. In Po-mice, hypoglycemia progressively developed until glucose levels dropped to a nadir of 2.3 +/- 0.1 mmol/l, whereas in Fe-mice, glycemia rapidly and transiently developed, and glucose levels increased to 7.7 +/- 0.6 mmol/l before progressively returning to fasting glycemic levels. Plasma insulin levels were similar in both Po- and Fe-mice during and at the end of the infusion periods (21.2 +/- 2.2 vs. 25.7 +/- 0.9 microU/ml, respectively, at 180 min of infusion). The whole-body glucose turnover rate was significantly higher in Po-mice than in Fe-mice (45.9 +/- 3.8 vs. 37.7 +/- 2.0 mg x kg(-1) x min)-1), respectively) and in Sal-mice (24.4 +/- 1.8 mg x kg(-1) x min(-1)). Somatostatin co-infusion with glucose in Po-mice prevented hypoglycemia without modifying the plasma insulin profile. Finally, tissue glucose clearance, which was determined after injecting 14C-2-deoxyglucose, increased to a higher level in Po-mice versus Fe-mice in the heart, brown adipose tissue, and the soleus muscle. Our data show that stimulation of the hepatoportal glucose sensor induced hypoglycemia and increased glucose utilization by a combination of insulin-dependent and insulin-independent or -sensitizing mechanisms. Furthermore, activation of the glucose sensor and/or transmission of its signal to target tissues can be blocked by somatostatin.
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“Thus, in the fasting and in the feeding situation, the vagus nerve is responsible for energy storage.”
From Interaction of the endocrine system with inflammation: a function of energy and volume regulation (2014) · cites this paper as [41]
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Self-citationGlucosensing in the gastrointestinal tract: Impact on glucose metabolism
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Self-citationJohnson, K., Edgerton, D. S., Rodewald, T., Scott, M. F., Farmer, B., Neal, D. W., & Cherrington, A. D. (2007) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.00275.2007 · Cited by 46
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“Reprinted with permission from [62] and [63] 487”
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BackgroundInfluentialMoore, M. C., Cardin, S., Edgerton, D. S., Farmer, B., Neal, D. W., Lautz, M., & Cherrington, A. D. (2004) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.00343.2003 · Cited by 28
“Interestingly, the only skeletal muscle that Burcelin et al (7) observed to exhibit a substantial enhancement of glucose uptake following portal glucose infusion was soleus (composed primarily of oxidative fibers), suggesting that 5-HT is involved in the extrahepatic effects of the portal signal.”
BackgroundResultInfluentialThe role of hepatic portal glucose sensing in modulating responses to hypoglycaemia in man
Smith, D., Pernet, A., Reid, H., Bingham, E., Rosenthal, J., Macdonald, I. A., Umpleby, A. M., & Amiel, S. A. (2002) · Diabetologia · doi:10.1007/s00125-002-0909-3 · Cited by 27
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García-Luna, C., Sanchez‐Watts, G., Arnold, M., de Lartigue, G., DeWalt, N., Langhans, W., & Watts, A. G. (2021) · eNeuro · doi:10.1523/eneuro.0419-20.2021 · Cited by 23
“…exocrine (Love et al., 2007) and endocrine function (Buijs et al., 2001; Taborsky and Mundinger, 2012), particularly insulin secretion (Ahrén and Taborsky, 1986; Nagase et al., 1993), a mechanism that may contribute to the hypoglycemic response to HPV hyperglycemia (Burcelin et al., 2000).”
Mithieux, G. (2010) · Diabetes & Metabolism · doi:10.1016/s1262-3636(10)70467-5 · Cited by 20
Johnson, K., Edgerton, D. S., Rodewald, T., Scott, M. F., Farmer, B., Neal, D. W., & Cherrington, A. D. (2007) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.00642.2007 · Cited by 19
Malbert, C.-H., Chauvin, A., Horowitz, M., & Jones, K. L. (2021) · Diabetes · doi:10.2337/db20-0361 · Cited by 18
Brain Processing of Duodenal and Portal Glucose Sensing
Boubaker-Vitre, J., Val‐Laillet, D., Guérin, S., & Malbert, C. (2012) · Journal of Neuroendocrinology · doi:10.1111/j.1365-2826.2012.02326.x · Cited by 18
Gautier‐Stein, A., Zitoun, C., Lalli, E., et al. (2006) · Journal of Biological Chemistry · doi:10.1016/s0021-9258(19)84039-5 · Cited by 18
Comparison of intraduodenal and intravenous glucose metabolism under clamp conditions in humans
Féry, F., Tappy, L., Deviere, J. M. E., et al. (2004) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.00201.2003 · Cited by 18
Distinct Classes of Central GLUT2-Dependent Sensors Control Counterregulation and Feeding
Marty, N., Bady, I., & Thorens, B. (2006) · Diabetes · doi:10.2337/db06-s014 · Cited by 17
“We have provided evidence that this sensor, activated by intraportal glucose infusion in conscious mice, increases the rate of glucose clearance by a subset of peripheral tissues: brown fat, soleus muscle, and the heart (8).”
BackgroundSelf-citationHepatic interoception in health and disease
Berthoud, H., Münzberg, H., Morrison, C. D., & Neuhuber, W. (2024) · Autonomic Neuroscience · doi:10.1016/j.autneu.2024.103174 · Cited by 17
“…insulin, is critical for regulation of postprandial hepatic glucose uptake and the overall allocation of glucose to other organs (Adkins-Marshall et al., 1992; Burcelin et al., 2000; Cherrington et al., 1987; Galassetti et al., 1998; Stumpel and Jungermann, 1997), reviewed by (Moore et al., 2012).”
InfluentialImpact of PPAR-α induction on glucose homoeostasis in alcohol-fed mice
Lebrun, V., Molendi‐Coste, O., Lanthier, N., Sempoux, C. L., Cani, P. D., van Rooijen, N., Stärkel, P., Horsmans, Y., & Leclercq, I. A. (2013) · Clinical Science · doi:10.1042/cs20130064 · Cited by 15
Effect of Portal Glucose Sensing on Systemic Glucose Levels in SD and ZDF Rats
Pal, A., Rhoads, D. B., & Tavakkoli, A. (2016) · PLoS ONE · doi:10.1371/journal.pone.0165592 · Cited by 14
Charpentier, J., Waget, A., Klopp, P., Magnan, C., Cruciani‐Guglielmacci, C., Lee, S. J., Burcelin, R., & Grasset, E. (2018) · American Journal of Physiology-Gastrointestinal and Liver Physiology · doi:10.1152/ajpgi.00348.2017 · Cited by 15
“lixisenatide has been described as des-38-proline-exendin-4(1-39)-peptidylpenta-L-lysyl-L-lysinamide, which is derived from the first 39 amino acids of exendin 4 omitting proline at position 38 and adding six lysine residues (11).”
BackgroundSelf-citationGrasset, E., Puel, A., Charpentier, J., Klopp, P., Christensen, J. E., Lelouvier, B., Servant, F., Blasco‐Baqué, V., Tercé, F., & Burcelin, R. (2021) · Acta Diabetologica · doi:10.1007/s00592-021-01790-y · Cited by 15
Self-citationMithieux, G. (2012) · Current Diabetes Reports · doi:10.1007/s11892-012-0257-8 · Cited by 13
Ertl, A. C., Mann, S. L., Richardson, A., Briscoe, V. J., Blair, H. B., Tate, D. B., & Davis, S. N. (2008) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.90470.2008 · Cited by 11
Impact of portal glucose delivery on glucose metabolism in conscious, unrestrained mice
Chueh, F., Malabanan, C. M., & McGuinness, O. P. (2006) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.00608.2005 · Cited by 11
Zangeneh, F., Basu, R., Shah, P., Arora, P. S., Camilleri, M., & Rizza, R. A. (2003) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.00055.2003 · Cited by 11
The Hepatoportal Glucose Sensor
Thorens, B. (2004) · KARGER eBooks · doi:10.1159/000079027 · Cited by 10
Self-citationThe contribution of afferent signals from the liver to metabolic regulation during exercise
Lavoie, J.-M. (2002) · Canadian Journal of Physiology and Pharmacology · doi:10.1139/y02-137 · Cited by 10
Zheng, D., Ionut, V., Mooradian, V., Stefanovski, D., & Bergman, R. N. (2009) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.00280.2009 · Cited by 9
Characterization of the portal signal in a nonsteady hyperglycemic state in conscious dogs
Ogihara, N., Ebihara, S., Kawamura, W., et al. (2003) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.00079.2002 · Cited by 9
Metadata
- Authors
- Burcelin, R., Dolci, W., & Thorens, B.
- Affiliations
- University of Lausanne (CH)
- Venue
- Diabetes
- Publisher
- American Diabetes Association
- Published
- 2000-10-01
- Volume
- 49
- Issue
- 10
- Pages
- 1635-1642
- ISSN
- 0012-1797 (ISSN-L)
- 1939-327X
- OpenAlex
- W2137028096
- Cited by
- 137
- References
- 0
- Citations by year
- 2026: 1 · 2024: 2 · 2023: 2 · 2022: 2 · 2021: 6 · 2020: 3 · 2019: 2 · 2018: 2 · 2017: 2 · 2016: 5 · 2015: 6 · 2014: 6 · 2013: 11 · 2012: 6
- FWCI
- 7.02
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Diabetes (publishedVersion)
- PubMed (publishedVersion)
- IRIS (submittedVersion)
- SERVAL (Université de Lausanne) (submittedVersion)
- Funders
- Schweizerischer Nationalfonds zur Förderung der Wissenschaftlichen Forschung
- Topics
- Health Sciences › Medicine › Endocrinology, Diabetes and Metabolism › Pancreatic function and diabetes
- Health Sciences › Medicine › Endocrinology, Diabetes and Metabolism › Diabetes Management and Research
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Metabolism, Diabetes, and Cancer
- Keywords
- hypoglycemia, glucose infusion, portal vein, somatostatin, insulin, insulin-independent glucose uptake, heart, brown adipose tissue, soleus muscle, glucose clearance, 2-deoxyglucose, glucose metabolism
- MeSH terms
- Animals, Blood Glucose, Glucose, Homeostasis, Hypoglycemia, Hypothalamus, Infusions, Intravenous, Insulin, Liver, Metabolic Clearance Rate, Mice, Inbred C57BL, Muscle Denervation, Portal Vein, Somatostatin, Vagus Nerve, Muscle, Skeletal, Mice
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