Metformin Enhances Autophagy and Normalizes Mitochondrial Function to Alleviate Aging-Associated Inflammation
Age is a non-modifiable risk factor for the inflammation that underlies age-associated diseases; thus, anti-inflammaging drugs hold promise for increasing health span. Cytokine profiling and bioinformatic analyses showed that Th17 cytokine production differentiates CD4+ T cells from lean, normoglyce...
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| Published in | Cell metabolism Vol. 32; no. 1; pp. 44 - 55.e6 |
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| Main Authors | , , , , , , , , , , , , , , , , , , , , |
| Format | Journal Article |
| Language | English |
| Published |
United States
Elsevier Inc
07.07.2020
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| Subjects | |
| Online Access | Get full text |
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| Abstract | Age is a non-modifiable risk factor for the inflammation that underlies age-associated diseases; thus, anti-inflammaging drugs hold promise for increasing health span. Cytokine profiling and bioinformatic analyses showed that Th17 cytokine production differentiates CD4+ T cells from lean, normoglycemic older and younger subjects, and mimics a diabetes-associated Th17 profile. T cells from older compared to younger subjects also had defects in autophagy and mitochondrial bioenergetics that associate with redox imbalance. Metformin ameliorated the Th17 inflammaging profile by increasing autophagy and improving mitochondrial bioenergetics. By contrast, autophagy-targeting siRNA disrupted redox balance in T cells from young subjects and activated the Th17 profile by activating the Th17 master regulator, STAT3, which in turn bound IL-17A and F promoters. Mitophagy-targeting siRNA failed to activate the Th17 profile. We conclude that metformin improves autophagy and mitochondrial function largely in parallel to ameliorate a newly defined inflammaging profile that echoes inflammation in diabetes.
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•CD4+ T cells from healthy older people preferentially produce a Th17 profile•Autophagy, but not mitophagy, knockdown activates a Th17 profile in “young” cells•Mitochondrial ROS is needed, but not sufficient, for a Th17 profile in “young” cells•Metformin improves autophagy and mitochondria in parallel to decrease inflammaging
We uncovered a dominant Th17 inflammaging profile made by CD4+ T cells. Knockdown of autophagy in T cells from young subjects activates this profile. In vitro metformin improves autophagy and mitochondrial function in parallel to ameliorate Th17 inflammaging. Oral metformin intervention improves T cell autophagy in people, indicating potential use for age-associated inflammation. |
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| AbstractList | Age is a non-modifiable risk factor for the inflammation that underlies age-associated diseases; thus, anti-inflammaging drugs hold promise for increasing health span. Cytokine profiling and bioinformatic analyses showed that Th17 cytokine production differentiates CD4+ T cells from lean, normoglycemic older and younger subjects, and mimics a diabetes-associated Th17 profile. T cells from older compared to younger subjects also had defects in autophagy and mitochondrial bioenergetics that associate with redox imbalance. Metformin ameliorated the Th17 inflammaging profile by increasing autophagy and improving mitochondrial bioenergetics. By contrast, autophagy-targeting siRNA disrupted redox balance in T cells from young subjects and activated the Th17 profile by activating the Th17 master regulator, STAT3, which in turn bound IL-17A and F promoters. Mitophagy-targeting siRNA failed to activate the Th17 profile. We conclude that metformin improves autophagy and mitochondrial function largely in parallel to ameliorate a newly defined inflammaging profile that echoes inflammation in diabetes.
[Display omitted]
•CD4+ T cells from healthy older people preferentially produce a Th17 profile•Autophagy, but not mitophagy, knockdown activates a Th17 profile in “young” cells•Mitochondrial ROS is needed, but not sufficient, for a Th17 profile in “young” cells•Metformin improves autophagy and mitochondria in parallel to decrease inflammaging
We uncovered a dominant Th17 inflammaging profile made by CD4+ T cells. Knockdown of autophagy in T cells from young subjects activates this profile. In vitro metformin improves autophagy and mitochondrial function in parallel to ameliorate Th17 inflammaging. Oral metformin intervention improves T cell autophagy in people, indicating potential use for age-associated inflammation. Age is a non-modifiable risk factor for the inflammation that underlies age-associated diseases; thus, anti-inflammaging drugs hold promise for increasing health span. Cytokine profiling and bioinformatic analyses showed that Th17 cytokine production differentiates CD4+ T cells from lean, normoglycemic older and younger subjects, and mimics a diabetes-associated Th17 profile. T cells from older compared to younger subjects also had defects in autophagy and mitochondrial bioenergetics that associate with redox imbalance. Metformin ameliorated the Th17 inflammaging profile by increasing autophagy and improving mitochondrial bioenergetics. By contrast, autophagy-targeting siRNA disrupted redox balance in T cells from young subjects and activated the Th17 profile by activating the Th17 master regulator, STAT3, which in turn bound IL-17A and F promoters. Mitophagy-targeting siRNA failed to activate the Th17 profile. We conclude that metformin improves autophagy and mitochondrial function largely in parallel to ameliorate a newly defined inflammaging profile that echoes inflammation in diabetes.Age is a non-modifiable risk factor for the inflammation that underlies age-associated diseases; thus, anti-inflammaging drugs hold promise for increasing health span. Cytokine profiling and bioinformatic analyses showed that Th17 cytokine production differentiates CD4+ T cells from lean, normoglycemic older and younger subjects, and mimics a diabetes-associated Th17 profile. T cells from older compared to younger subjects also had defects in autophagy and mitochondrial bioenergetics that associate with redox imbalance. Metformin ameliorated the Th17 inflammaging profile by increasing autophagy and improving mitochondrial bioenergetics. By contrast, autophagy-targeting siRNA disrupted redox balance in T cells from young subjects and activated the Th17 profile by activating the Th17 master regulator, STAT3, which in turn bound IL-17A and F promoters. Mitophagy-targeting siRNA failed to activate the Th17 profile. We conclude that metformin improves autophagy and mitochondrial function largely in parallel to ameliorate a newly defined inflammaging profile that echoes inflammation in diabetes. Age is a non-modifiable risk factor for the inflammation that underlies age-associated diseases; thus, anti-inflammaging drugs hold promise for increasing health span. Cytokine profiling and bioinformatic analyses showed that Th17 cytokine production differentiates CD4 + T cells from lean, normoglycemic older and younger subjects, and mimics a diabetes-associated Th17 profile. T cells from older compared to younger subjects also had defects in autophagy and mitochondrial bioenergetics that associate with redox imbalance. Metformin ameliorated the Th17 inflammaging profile by increasing autophagy and improving mitochondrial bioenergetics. By contrast, autophagy-targeting siRNA disrupted redox balance in T cells from young subjects and activated the Th17 profile by activating the Th17 master regulator, STAT3, which in turn bound IL-17A and F promoters. Mitophagy-targeting siRNA failed to activate the Th17 profile. We conclude that metformin improves autophagy and mitochondrial function largely in parallel to ameliorate a newly defined inflammaging profile that echoes inflammation in diabetes. • CD4 + T cells from healthy older people preferentially produce a Th17 profile • Autophagy, but not mitophagy, knockdown activates a Th17 profile in “young” cells • Mitochondrial ROS is needed, but not sufficient, for a Th17 profile in “young” cells • Metformin improves autophagy and mitochondria in parallel to decrease inflammaging We uncovered a dominant Th17 inflammaging profile made by CD4 + T cells. Knockdown of autophagy in T cells from young subjects activates this profile. In vitro metformin improves autophagy and mitochondrial function in parallel to ameliorate Th17 inflammaging. Oral metformin intervention improves T cell autophagy in people, indicating potential use for age-associated inflammation. Age is a non-modifiable risk factor for the inflammation that underlies age-associated diseases; thus, anti-inflammaging drugs hold promise for increasing health span. Cytokine profiling and bioinformatic analyses showed that Th17 cytokine production differentiates CD4 T cells from lean, normoglycemic older and younger subjects, and mimics a diabetes-associated Th17 profile. T cells from older compared to younger subjects also had defects in autophagy and mitochondrial bioenergetics that associate with redox imbalance. Metformin ameliorated the Th17 inflammaging profile by increasing autophagy and improving mitochondrial bioenergetics. By contrast, autophagy-targeting siRNA disrupted redox balance in T cells from young subjects and activated the Th17 profile by activating the Th17 master regulator, STAT3, which in turn bound IL-17A and F promoters. Mitophagy-targeting siRNA failed to activate the Th17 profile. We conclude that metformin improves autophagy and mitochondrial function largely in parallel to ameliorate a newly defined inflammaging profile that echoes inflammation in diabetes. |
| Author | Bharath, Leena P. Nicholas, Dequina A. Liu, Jing Kern, Philip A. Guo, Zhenheng Hasturk, Hatice Fleeman, Rebecca M. Proctor, Elizabeth A. Jiang, Kai Deeney, Jude Snyder-Cappione, Jennifer Hawk, Gregory S. Liu, Rui Nikolajczyk, Barbara S. Pihl, Riley M.F. Cui, Licong Agrawal, Madhur Apovian, Caroline M. Belkina, Anna C. McCambridge, Grace Thompson, Katherine |
| Author_xml | – sequence: 1 givenname: Leena P. surname: Bharath fullname: Bharath, Leena P. organization: Department of Nutrition and Public Health, Merrimack College, North Andover, MA, USA – sequence: 2 givenname: Madhur surname: Agrawal fullname: Agrawal, Madhur organization: Department of Pharmacology and Nutritional Sciences, University of Kentucky, Lexington, KY, USA – sequence: 3 givenname: Grace surname: McCambridge fullname: McCambridge, Grace organization: Department of Nutrition and Public Health, Merrimack College, North Andover, MA, USA – sequence: 4 givenname: Dequina A. surname: Nicholas fullname: Nicholas, Dequina A. organization: Department of Obstetrics, Gynecology, and Reproductive Sciences, School of Medicine, University of California, San Diego, San Diego, CA, USA – sequence: 5 givenname: Hatice surname: Hasturk fullname: Hasturk, Hatice organization: Forsyth Institute, Cambridge, MA, USA – sequence: 6 givenname: Jing surname: Liu fullname: Liu, Jing organization: Department of Computer Science, University of Kentucky, Lexington, KY, USA – sequence: 7 givenname: Kai surname: Jiang fullname: Jiang, Kai organization: Department of Physiology, University of Kentucky, Lexington, KY, USA – sequence: 8 givenname: Rui surname: Liu fullname: Liu, Rui organization: Department of Pharmaceutical Sciences, University of Kentucky, Lexington, KY, USA – sequence: 9 givenname: Zhenheng surname: Guo fullname: Guo, Zhenheng organization: Department of Pharmacology and Nutritional Sciences, University of Kentucky, Lexington, KY, USA – sequence: 10 givenname: Jude surname: Deeney fullname: Deeney, Jude organization: Department of Medicine, Endocrinology, Diabetes & Nutrition, Boston University School of Medicine, Boston, MA, USA – sequence: 11 givenname: Caroline M. surname: Apovian fullname: Apovian, Caroline M. organization: Department of Medicine, Endocrinology, Diabetes & Nutrition, Boston University School of Medicine, Boston, MA, USA – sequence: 12 givenname: Jennifer surname: Snyder-Cappione fullname: Snyder-Cappione, Jennifer organization: Department of Microbiology, Boston University School of Medicine, Boston, MA, USA – sequence: 13 givenname: Gregory S. surname: Hawk fullname: Hawk, Gregory S. organization: Department of Statistics, University of Kentucky, Lexington, KY, USA – sequence: 14 givenname: Rebecca M. surname: Fleeman fullname: Fleeman, Rebecca M. organization: Departments of Neurosurgery and Pharmacology, Pennsylvania State University College of Medicine, Hershey, PA, USA – sequence: 15 givenname: Riley M.F. surname: Pihl fullname: Pihl, Riley M.F. organization: Flow Cytometry Core Facility, Boston University School of Medicine, Boston, MA, USA – sequence: 16 givenname: Katherine surname: Thompson fullname: Thompson, Katherine organization: Department of Statistics, University of Kentucky, Lexington, KY, USA – sequence: 17 givenname: Anna C. surname: Belkina fullname: Belkina, Anna C. organization: Flow Cytometry Core Facility, Boston University School of Medicine, Boston, MA, USA – sequence: 18 givenname: Licong surname: Cui fullname: Cui, Licong organization: Department of Computer Science, University of Kentucky, Lexington, KY, USA – sequence: 19 givenname: Elizabeth A. surname: Proctor fullname: Proctor, Elizabeth A. organization: Departments of Neurosurgery and Pharmacology, Pennsylvania State University College of Medicine, Hershey, PA, USA – sequence: 20 givenname: Philip A. surname: Kern fullname: Kern, Philip A. organization: Barnstable Brown Diabetes and Obesity Center, University of Kentucky, Lexington, KY, USA – sequence: 21 givenname: Barbara S. surname: Nikolajczyk fullname: Nikolajczyk, Barbara S. email: barb.nik@uky.edu organization: Department of Pharmacology and Nutritional Sciences, University of Kentucky, Lexington, KY, USA |
| BackLink | https://www.ncbi.nlm.nih.gov/pubmed/32402267$$D View this record in MEDLINE/PubMed |
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| Title | Metformin Enhances Autophagy and Normalizes Mitochondrial Function to Alleviate Aging-Associated Inflammation |
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