Neuropathy and neural plasticity in the subcutaneous white adipose depot.
The difficulty in obtaining as well as maintaining weight loss, together with the impairment of metabolic control in conditions like diabetes and cardiovascular disease, may represent pathological situations of inadequate neural communication between the brain and peripheral organs and tissues. Inne...
| Main Authors: | , , , , , , , , , , , , |
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| Format: | Article |
| Language: | English |
| Published: |
Public Library of Science (PLoS)
2019-01-01
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| Series: | PLoS ONE |
| Online Access: | https://doi.org/10.1371/journal.pone.0221766 |
| _version_ | 1819042921260777472 |
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| author | Magdalena Blaszkiewicz Jake W Willows Amanda L Dubois Stephen Waible Kristen DiBello Lila L Lyons Cory P Johnson Emma Paradie Nicholas Banks Katherine Motyl Merilla Michael Benjamin Harrison Kristy L Townsend |
| author_facet | Magdalena Blaszkiewicz Jake W Willows Amanda L Dubois Stephen Waible Kristen DiBello Lila L Lyons Cory P Johnson Emma Paradie Nicholas Banks Katherine Motyl Merilla Michael Benjamin Harrison Kristy L Townsend |
| author_sort | Magdalena Blaszkiewicz |
| collection | DOAJ |
| description | The difficulty in obtaining as well as maintaining weight loss, together with the impairment of metabolic control in conditions like diabetes and cardiovascular disease, may represent pathological situations of inadequate neural communication between the brain and peripheral organs and tissues. Innervation of adipose tissues by peripheral nerves provides a means of communication between the master metabolic regulator in the brain (chiefly the hypothalamus), and energy-expending and energy-storing cells in the body (primarily adipocytes). Although chemical and surgical denervation studies have clearly demonstrated how crucial adipose tissue neural innervation is for maintaining proper metabolic health, we have uncovered that adipose tissue becomes neuropathic (ie: reduction in neurites) in various conditions of metabolic dysregulation. Here, utilizing both human and mouse adipose tissues, we present evidence of adipose tissue neuropathy, or loss of proper innervation, under pathophysiological conditions such as obesity, diabetes, and aging, all of which are concomitant with insult to the adipose organ as well as metabolic dysfunction. Neuropathy is indicated by loss of nerve fiber protein expression, reduction in synaptic markers, and lower neurotrophic factor expression in adipose tissue. Aging-related adipose neuropathy particularly results in loss of innervation around the tissue vasculature, which cannot be reversed by exercise. Together with indications of neuropathy in muscle and bone, these findings underscore that peripheral neuropathy is not restricted to classic tissues like the skin of distal extremities, and that loss of innervation to adipose may trigger or exacerbate metabolic diseases. In addition, we have demonstrated stimulation of adipose tissue neural plasticity with cold exposure, which may ameliorate adipose neuropathy and be a potential therapeutic option to re-innervate adipose and restore metabolic health. |
| first_indexed | 2024-12-21T09:48:34Z |
| format | Article |
| id | doaj.art-01ddd7bee3d946ed8cd8819db7a718d5 |
| institution | Directory Open Access Journal |
| issn | 1932-6203 |
| language | English |
| last_indexed | 2024-12-21T09:48:34Z |
| publishDate | 2019-01-01 |
| publisher | Public Library of Science (PLoS) |
| record_format | Article |
| series | PLoS ONE |
| spelling | doaj.art-01ddd7bee3d946ed8cd8819db7a718d52022-12-21T19:08:14ZengPublic Library of Science (PLoS)PLoS ONE1932-62032019-01-01149e022176610.1371/journal.pone.0221766Neuropathy and neural plasticity in the subcutaneous white adipose depot.Magdalena BlaszkiewiczJake W WillowsAmanda L DuboisStephen WaibleKristen DiBelloLila L LyonsCory P JohnsonEmma ParadieNicholas BanksKatherine MotylMerilla MichaelBenjamin HarrisonKristy L TownsendThe difficulty in obtaining as well as maintaining weight loss, together with the impairment of metabolic control in conditions like diabetes and cardiovascular disease, may represent pathological situations of inadequate neural communication between the brain and peripheral organs and tissues. Innervation of adipose tissues by peripheral nerves provides a means of communication between the master metabolic regulator in the brain (chiefly the hypothalamus), and energy-expending and energy-storing cells in the body (primarily adipocytes). Although chemical and surgical denervation studies have clearly demonstrated how crucial adipose tissue neural innervation is for maintaining proper metabolic health, we have uncovered that adipose tissue becomes neuropathic (ie: reduction in neurites) in various conditions of metabolic dysregulation. Here, utilizing both human and mouse adipose tissues, we present evidence of adipose tissue neuropathy, or loss of proper innervation, under pathophysiological conditions such as obesity, diabetes, and aging, all of which are concomitant with insult to the adipose organ as well as metabolic dysfunction. Neuropathy is indicated by loss of nerve fiber protein expression, reduction in synaptic markers, and lower neurotrophic factor expression in adipose tissue. Aging-related adipose neuropathy particularly results in loss of innervation around the tissue vasculature, which cannot be reversed by exercise. Together with indications of neuropathy in muscle and bone, these findings underscore that peripheral neuropathy is not restricted to classic tissues like the skin of distal extremities, and that loss of innervation to adipose may trigger or exacerbate metabolic diseases. In addition, we have demonstrated stimulation of adipose tissue neural plasticity with cold exposure, which may ameliorate adipose neuropathy and be a potential therapeutic option to re-innervate adipose and restore metabolic health.https://doi.org/10.1371/journal.pone.0221766 |
| spellingShingle | Magdalena Blaszkiewicz Jake W Willows Amanda L Dubois Stephen Waible Kristen DiBello Lila L Lyons Cory P Johnson Emma Paradie Nicholas Banks Katherine Motyl Merilla Michael Benjamin Harrison Kristy L Townsend Neuropathy and neural plasticity in the subcutaneous white adipose depot. PLoS ONE |
| title | Neuropathy and neural plasticity in the subcutaneous white adipose depot. |
| title_full | Neuropathy and neural plasticity in the subcutaneous white adipose depot. |
| title_fullStr | Neuropathy and neural plasticity in the subcutaneous white adipose depot. |
| title_full_unstemmed | Neuropathy and neural plasticity in the subcutaneous white adipose depot. |
| title_short | Neuropathy and neural plasticity in the subcutaneous white adipose depot. |
| title_sort | neuropathy and neural plasticity in the subcutaneous white adipose depot |
| url | https://doi.org/10.1371/journal.pone.0221766 |
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