Stimulation of the hepatoportal nerve plexus with focused ultrasound restores glucose homoeostasis in diabetic mice, rats and swine
Peripheral neurons that sense glucose relay signals of glucose availability to integrative clusters of neurons in the brain. However, the roles of such signalling pathways in the maintenance of glucose homoeostasis and their contribution to disease are unknown. Here we show that the selective activa...
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| Published in: | Nature biomedical engineering Vol. 6; no. 6; pp. 683 - 705 |
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| Main Authors: | , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , |
| Format: | Journal Article |
| Language: | English |
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01-06-2022
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| Abstract | Peripheral neurons that sense glucose relay signals of glucose availability to integrative clusters of neurons in the brain. However, the roles of such signalling pathways in the maintenance of glucose homoeostasis and their contribution to disease are unknown. Here we show that the selective activation of the nerve plexus of the hepatic portal system via peripheral focused ultrasound stimulation (pFUS) improves glucose homoeostasis in mice and rats with insulin-resistant diabetes and in swine subject to hyperinsulinemic-euglycaemic clamps. pFUS modulated the activity of sensory projections to the hypothalamus, altered the concentrations of metabolism-regulating neurotransmitters, and enhanced glucose tolerance and utilization in the three species, whereas physical transection or chemical blocking of the liver–brain nerve pathway abolished the effect of pFUS on glucose tolerance. Longitudinal multi-omic profiling of metabolic tissues from the treated animals confirmed pFUS-induced modifications of key metabolic functions in liver, pancreas, muscle, adipose, kidney and intestinal tissues. Non-invasive ultrasound activation of afferent autonomic nerves may represent a non-pharmacologic therapy for the restoration of glucose homoeostasis in type-2 diabetes and other metabolic diseases.
Selective activation of the hepatoportal nerve plexus via peripheral focused ultrasound stimulation improves glucose homoeostasis and enhances glucose tolerance and utilization in rodent models of diabetes and in swine. |
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| AbstractList | Peripheral neurons that sense glucose relay signals of glucose availability to integrative clusters of neurons in the brain. However, the roles of such signalling pathways in the maintenance of glucose homoeostasis and their contribution to disease are unknown. Here we show that the selective activation of the nerve plexus of the hepatic portal system via peripheral focused ultrasound stimulation (pFUS) improves glucose homoeostasis in mice and rats with insulin-resistant diabetes and in swine subject to hyperinsulinemic-euglycaemic clamps. pFUS modulated the activity of sensory projections to the hypothalamus, altered the concentrations of metabolism-regulating neurotransmitters, and enhanced glucose tolerance and utilization in the three species, whereas physical transection or chemical blocking of the liver–brain nerve pathway abolished the effect of pFUS on glucose tolerance. Longitudinal multi-omic profiling of metabolic tissues from the treated animals confirmed pFUS-induced modifications of key metabolic functions in liver, pancreas, muscle, adipose, kidney and intestinal tissues. Non-invasive ultrasound activation of afferent autonomic nerves may represent a non-pharmacologic therapy for the restoration of glucose homoeostasis in type-2 diabetes and other metabolic diseases. Peripheral neurons that sense glucose relay signals of glucose availability to integrative clusters of neurons in the brain. However, the roles of such signalling pathways in the maintenance of glucose homoeostasis and their contribution to disease are unknown. Here we show that the selective activation of the nerve plexus of the hepatic portal system via peripheral focused ultrasound stimulation (pFUS) improves glucose homoeostasis in mice and rats with insulin-resistant diabetes and in swine subject to hyperinsulinemic-euglycaemic clamps. pFUS modulated the activity of sensory projections to the hypothalamus, altered the concentrations of metabolism-regulating neurotransmitters, and enhanced glucose tolerance and utilization in the three species, whereas physical transection or chemical blocking of the liver-brain nerve pathway abolished the effect of pFUS on glucose tolerance. Longitudinal multi-omic profiling of metabolic tissues from the treated animals confirmed pFUS-induced modifications of key metabolic functions in liver, pancreas, muscle, adipose, kidney and intestinal tissues. Non-invasive ultrasound activation of afferent autonomic nerves may represent a non-pharmacologic therapy for the restoration of glucose homoeostasis in type-2 diabetes and other metabolic diseases.Peripheral neurons that sense glucose relay signals of glucose availability to integrative clusters of neurons in the brain. However, the roles of such signalling pathways in the maintenance of glucose homoeostasis and their contribution to disease are unknown. Here we show that the selective activation of the nerve plexus of the hepatic portal system via peripheral focused ultrasound stimulation (pFUS) improves glucose homoeostasis in mice and rats with insulin-resistant diabetes and in swine subject to hyperinsulinemic-euglycaemic clamps. pFUS modulated the activity of sensory projections to the hypothalamus, altered the concentrations of metabolism-regulating neurotransmitters, and enhanced glucose tolerance and utilization in the three species, whereas physical transection or chemical blocking of the liver-brain nerve pathway abolished the effect of pFUS on glucose tolerance. Longitudinal multi-omic profiling of metabolic tissues from the treated animals confirmed pFUS-induced modifications of key metabolic functions in liver, pancreas, muscle, adipose, kidney and intestinal tissues. Non-invasive ultrasound activation of afferent autonomic nerves may represent a non-pharmacologic therapy for the restoration of glucose homoeostasis in type-2 diabetes and other metabolic diseases. Peripheral neurons that sense glucose relay signals of glucose availability to integrative clusters of neurons in the brain. However, the roles of such signalling pathways in the maintenance of glucose homoeostasis and their contribution to disease are unknown. Here we show that the selective activation of the nerve plexus of the hepatic portal system via peripheral focused ultrasound stimulation (pFUS) improves glucose homoeostasis in mice and rats with insulin-resistant diabetes and in swine subject to hyperinsulinemic-euglycaemic clamps. pFUS modulated the activity of sensory projections to the hypothalamus, altered the concentrations of metabolism-regulating neurotransmitters, and enhanced glucose tolerance and utilization in the three species, whereas physical transection or chemical blocking of the liver–brain nerve pathway abolished the effect of pFUS on glucose tolerance. Longitudinal multi-omic profiling of metabolic tissues from the treated animals confirmed pFUS-induced modifications of key metabolic functions in liver, pancreas, muscle, adipose, kidney and intestinal tissues. Non-invasive ultrasound activation of afferent autonomic nerves may represent a non-pharmacologic therapy for the restoration of glucose homoeostasis in type-2 diabetes and other metabolic diseases.Selective activation of the hepatoportal nerve plexus via peripheral focused ultrasound stimulation improves glucose homoeostasis and enhances glucose tolerance and utilization in rodent models of diabetes and in swine. Peripheral neurons that sense glucose relay signals of glucose availability to integrative clusters of neurons in the brain. However, the roles of such signalling pathways in the maintenance of glucose homoeostasis and their contribution to disease are unknown. Here we show that the selective activation of the nerve plexus of the hepatic portal system via peripheral focused ultrasound stimulation (pFUS) improves glucose homoeostasis in mice and rats with insulin-resistant diabetes and in swine subject to hyperinsulinemic-euglycaemic clamps. pFUS modulated the activity of sensory projections to the hypothalamus, altered the concentrations of metabolism-regulating neurotransmitters, and enhanced glucose tolerance and utilization in the three species, whereas physical transection or chemical blocking of the liver–brain nerve pathway abolished the effect of pFUS on glucose tolerance. Longitudinal multi-omic profiling of metabolic tissues from the treated animals confirmed pFUS-induced modifications of key metabolic functions in liver, pancreas, muscle, adipose, kidney and intestinal tissues. Non-invasive ultrasound activation of afferent autonomic nerves may represent a non-pharmacologic therapy for the restoration of glucose homoeostasis in type-2 diabetes and other metabolic diseases. Selective activation of the hepatoportal nerve plexus via peripheral focused ultrasound stimulation improves glucose homoeostasis and enhances glucose tolerance and utilization in rodent models of diabetes and in swine. |
| Author | Song, Weiguo Loghin, Evelina Zanos, Stavros Hirschstein, Zall Tomaio, Jacquelyn N. Miwa, Hiromi Tai, Ningwen Ashe, Jeffrey Di Carlo, Dino Devarajan, Alex Kao, Tzu-Jen Maietta, Teresa Cotero, Victoria Barenboim, Linda Morton, Christine Shin, Damian Wallace, Kirk Akhtar, Kainat Puleo, Chris Fan, Ying Coleman, Thomas R. Jimenez-Cowell, Kevin Tracey, Kevin J. Graf, John Ding, Yuyan Herzog, Raimund I. Madhavan, Radhika Qanud, Khaled Huerta, Tomás S. Tsaava, Tea Chavan, Sangeeta S. Damaraju, Meghana |
| AuthorAffiliation | 4 Feinstein Institutes for Medical Research, Manhasset, NY, USA 2 University of California, Los Angeles, Los Angeles, CA, USA 1 General Electric (GE) Research, 1 Research Circle, Niskayuna, NY, USA 5 Yale School of Medicine, New Haven, CT, USA 6 German Cancer Research Center (DKFZ), Heidelberg, Germany 3 Albany Medical College, Albany, NY, USA |
| AuthorAffiliation_xml | – name: 1 General Electric (GE) Research, 1 Research Circle, Niskayuna, NY, USA – name: 6 German Cancer Research Center (DKFZ), Heidelberg, Germany – name: 2 University of California, Los Angeles, Los Angeles, CA, USA – name: 3 Albany Medical College, Albany, NY, USA – name: 4 Feinstein Institutes for Medical Research, Manhasset, NY, USA – name: 5 Yale School of Medicine, New Haven, CT, USA |
| Author_xml | – sequence: 1 givenname: Victoria surname: Cotero fullname: Cotero, Victoria organization: General Electric (GE) Research, 1 Research Circle – sequence: 2 givenname: John orcidid: 0000-0002-0396-9867 surname: Graf fullname: Graf, John organization: General Electric (GE) Research, 1 Research Circle – sequence: 3 givenname: Hiromi surname: Miwa fullname: Miwa, Hiromi organization: University of California, Los Angeles – sequence: 4 givenname: Zall surname: Hirschstein fullname: Hirschstein, Zall organization: Albany Medical College – sequence: 5 givenname: Khaled surname: Qanud fullname: Qanud, Khaled organization: Feinstein Institutes for Medical Research – sequence: 6 givenname: Tomás S. surname: Huerta fullname: Huerta, Tomás S. organization: Feinstein Institutes for Medical Research – sequence: 7 givenname: Ningwen surname: Tai fullname: Tai, Ningwen organization: Yale School of Medicine – sequence: 8 givenname: Yuyan surname: Ding fullname: Ding, Yuyan organization: Yale School of Medicine – sequence: 9 givenname: Kevin surname: Jimenez-Cowell fullname: Jimenez-Cowell, Kevin organization: Yale School of Medicine, German Cancer Research Center (DKFZ) – sequence: 10 givenname: Jacquelyn N. surname: Tomaio fullname: Tomaio, Jacquelyn N. organization: Feinstein Institutes for Medical Research – sequence: 11 givenname: Weiguo surname: Song fullname: Song, Weiguo organization: Feinstein Institutes for Medical Research – sequence: 12 givenname: Alex surname: Devarajan fullname: Devarajan, Alex organization: Feinstein Institutes for Medical Research – sequence: 13 givenname: Tea surname: Tsaava fullname: Tsaava, Tea organization: Feinstein Institutes for Medical Research – sequence: 14 givenname: Radhika surname: Madhavan fullname: Madhavan, Radhika organization: General Electric (GE) Research, 1 Research Circle – sequence: 15 givenname: Kirk surname: Wallace fullname: Wallace, Kirk organization: General Electric (GE) Research, 1 Research Circle – sequence: 16 givenname: Evelina surname: Loghin fullname: Loghin, Evelina organization: General Electric (GE) Research, 1 Research Circle – sequence: 17 givenname: Christine surname: Morton fullname: Morton, Christine organization: General Electric (GE) Research, 1 Research Circle – sequence: 18 givenname: Ying surname: Fan fullname: Fan, Ying organization: General Electric (GE) Research, 1 Research Circle – sequence: 19 givenname: Tzu-Jen surname: Kao fullname: Kao, Tzu-Jen organization: General Electric (GE) Research, 1 Research Circle – sequence: 20 givenname: Kainat surname: Akhtar fullname: Akhtar, Kainat organization: Albany Medical College – sequence: 21 givenname: Meghana surname: Damaraju fullname: Damaraju, Meghana organization: Albany Medical College – sequence: 22 givenname: Linda surname: Barenboim fullname: Barenboim, Linda organization: Albany Medical College – sequence: 23 givenname: Teresa surname: Maietta fullname: Maietta, Teresa organization: Albany Medical College – sequence: 24 givenname: Jeffrey surname: Ashe fullname: Ashe, Jeffrey organization: General Electric (GE) Research, 1 Research Circle – sequence: 25 givenname: Kevin J. orcidid: 0000-0003-1884-6314 surname: Tracey fullname: Tracey, Kevin J. organization: Feinstein Institutes for Medical Research – sequence: 26 givenname: Thomas R. surname: Coleman fullname: Coleman, Thomas R. organization: Feinstein Institutes for Medical Research – sequence: 27 givenname: Dino orcidid: 0000-0003-3942-4284 surname: Di Carlo fullname: Di Carlo, Dino organization: University of California, Los Angeles – sequence: 28 givenname: Damian surname: Shin fullname: Shin, Damian organization: Albany Medical College – sequence: 29 givenname: Stavros surname: Zanos fullname: Zanos, Stavros organization: Feinstein Institutes for Medical Research – sequence: 30 givenname: Sangeeta S. orcidid: 0000-0002-4822-3356 surname: Chavan fullname: Chavan, Sangeeta S. organization: Feinstein Institutes for Medical Research – sequence: 31 givenname: Raimund I. surname: Herzog fullname: Herzog, Raimund I. organization: Yale School of Medicine – sequence: 32 givenname: Chris orcidid: 0000-0002-2988-1820 surname: Puleo fullname: Puleo, Chris email: puleo@ge.com organization: General Electric (GE) Research, 1 Research Circle |
| BackLink | https://www.ncbi.nlm.nih.gov/pubmed/35361935$$D View this record in MEDLINE/PubMed |
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| Notes | ObjectType-Article-1 SourceType-Scholarly Journals-1 ObjectType-Feature-2 content type line 23 V.C. performed chronic stimulation experiments in ZDF and DIO models, data analysis and short-term stimulation experiments involving chemical lesioning and in vivo blocking; H.M. performed the in vitro stimulation experiments and data analysis; Z.H., K.A., M.D., L.B. and T.M. performed in vivo electrical recording experiments and contributed to data analysis; K.Q., J.N.T. and W.S. performed swine model experiments and data analysis; T.S.H., A.D. and T.T. performed western diet model experiments; N.T., Y.D. and K.J.-C. performed rodent H/E clamp experiments; J.G. performed transcriptomic and metabolomic analyses, data presentation and statistical analysis across manuscript data; R.M. performed analysis of electrical nerve recording data; K.W., T.-J.K. and Y.F. installed, set-up and calibrated ultrasound equipment and contributed experimental results from the mechanical piston stimulation data; E.L. and C.M. assisted in sample collection, storage and analysis of DIO and ZDF biological samples; J.A., K.J.T., T.R.C., D.D.C., D.S., S.Z., S.S.C., R.I.H. and C.P. designed the research and experiments, performed data analysis, edited and co-wrote sections of the manuscript; C.P. wrote the manuscript, including the assembly of sections from the collaborating institutions. Author contributions |
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| Publisher | Nature Publishing Group UK Nature Publishing Group |
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| Title | Stimulation of the hepatoportal nerve plexus with focused ultrasound restores glucose homoeostasis in diabetic mice, rats and swine |
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