NAD metabolism modulates inflammation and mitochondria function in diabetic kidney disease

Diabetes mellitus is the leading cause of cardiovascular and renal disease in the United -States. Despite the beneficial interventions available for patients with diabetes, there remains a need for additional therapeutic targets and therapies in diabetic kidney disease (DKD). Inflammation and oxidat...

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Published inThe Journal of biological chemistry Vol. 299; no. 8; p. 104975
Main Authors Myakala, Komuraiah, Wang, Xiaoxin X., Shults, Nataliia V., Krawczyk, Ewa, Jones, Bryce A., Yang, Xiaoping, Rosenberg, Avi Z., Ginley, Brandon, Sarder, Pinaki, Brodsky, Leonid, Jang, Yura, Na, Chan Hyun, Qi, Yue, Zhang, Xu, Guha, Udayan, Wu, Ci, Bansal, Shivani, Ma, Junfeng, Cheema, Amrita, Albanese, Chris, Hirschey, Matthew D., Yoshida, Teruhiko, Kopp, Jeffrey B., Panov, Julia, Levi, Moshe
Format Journal Article
LanguageEnglish
Published United States Elsevier Inc 01.08.2023
American Society for Biochemistry and Molecular Biology
Subjects
Animals
Diabetes Mellitus, Experimental - pathology
Diabetes Mellitus, Type 2 - metabolism
Diabetic Nephropathies - metabolism
DNA, Mitochondrial - metabolism
Inflammation - metabolism
Interferons - metabolism
Mice
Mitochondria - metabolism
NAD - metabolism
Nucleotidyltransferases - metabolism
▪
GLP-1
NR
SGLT2
▪
TBARS
KIM-1
NAD
ARB
4-HNE
FAO
ACEI
STING
cGAS-STING
DKD
diabetic kidney disease
mitochondrial DNA damage
mitochondria
sirtuin 3
inflammation, diabetes
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Abstract Diabetes mellitus is the leading cause of cardiovascular and renal disease in the United -States. Despite the beneficial interventions available for patients with diabetes, there remains a need for additional therapeutic targets and therapies in diabetic kidney disease (DKD). Inflammation and oxidative stress are increasingly recognized as important causes of renal diseases. Inflammation is closely associated with mitochondrial damage. The molecular connection between inflammation and mitochondrial metabolism remains to be elucidated. Recently, nicotinamide adenine nucleotide (NAD+) metabolism has been found to regulate immune function and inflammation. In the present studies, we tested the hypothesis that enhancing NAD metabolism could prevent inflammation in and progression of DKD. We found that treatment of db/db mice with type 2 diabetes with nicotinamide riboside (NR) prevented several manifestations of kidney dysfunction (i.e., albuminuria, increased urinary kidney injury marker-1 (KIM1) excretion, and pathologic changes). These effects were associated with decreased inflammation, at least in part via inhibiting the activation of the cyclic GMP-AMP synthase-stimulator of interferon genes (cGAS-STING) signaling pathway. An antagonist of the serum stimulator of interferon genes (STING) and whole-body STING deletion in diabetic mice showed similar renoprotection. Further analysis found that NR increased SIRT3 activity and improved mitochondrial function, which led to decreased mitochondrial DNA damage, a trigger for mitochondrial DNA leakage which activates the cGAS-STING pathway. Overall, these data show that NR supplementation boosted NAD metabolism to augment mitochondrial function, reducing inflammation and thereby preventing the progression of diabetic kidney disease.
AbstractList Diabetes mellitus is the leading cause of cardiovascular and renal disease in the United -States. Despite the beneficial interventions available for patients with diabetes, there remains a need for additional therapeutic targets and therapies in diabetic kidney disease (DKD). Inflammation and oxidative stress are increasingly recognized as important causes of renal diseases. Inflammation is closely associated with mitochondrial damage. The molecular connection between inflammation and mitochondrial metabolism remains to be elucidated. Recently, nicotinamide adenine nucleotide (NAD+) metabolism has been found to regulate immune function and inflammation. In the present studies, we tested the hypothesis that enhancing NAD metabolism could prevent inflammation in and progression of DKD. We found that treatment of db/db mice with type 2 diabetes with nicotinamide riboside (NR) prevented several manifestations of kidney dysfunction (i.e., albuminuria, increased urinary kidney injury marker-1 (KIM1) excretion, and pathologic changes). These effects were associated with decreased inflammation, at least in part via inhibiting the activation of the cyclic GMP-AMP synthase-stimulator of interferon genes (cGAS-STING) signaling pathway. An antagonist of the serum stimulator of interferon genes (STING) and whole-body STING deletion in diabetic mice showed similar renoprotection. Further analysis found that NR increased SIRT3 activity and improved mitochondrial function, which led to decreased mitochondrial DNA damage, a trigger for mitochondrial DNA leakage which activates the cGAS-STING pathway. Overall, these data show that NR supplementation boosted NAD metabolism to augment mitochondrial function, reducing inflammation and thereby preventing the progression of diabetic kidney disease.Diabetes mellitus is the leading cause of cardiovascular and renal disease in the United -States. Despite the beneficial interventions available for patients with diabetes, there remains a need for additional therapeutic targets and therapies in diabetic kidney disease (DKD). Inflammation and oxidative stress are increasingly recognized as important causes of renal diseases. Inflammation is closely associated with mitochondrial damage. The molecular connection between inflammation and mitochondrial metabolism remains to be elucidated. Recently, nicotinamide adenine nucleotide (NAD+) metabolism has been found to regulate immune function and inflammation. In the present studies, we tested the hypothesis that enhancing NAD metabolism could prevent inflammation in and progression of DKD. We found that treatment of db/db mice with type 2 diabetes with nicotinamide riboside (NR) prevented several manifestations of kidney dysfunction (i.e., albuminuria, increased urinary kidney injury marker-1 (KIM1) excretion, and pathologic changes). These effects were associated with decreased inflammation, at least in part via inhibiting the activation of the cyclic GMP-AMP synthase-stimulator of interferon genes (cGAS-STING) signaling pathway. An antagonist of the serum stimulator of interferon genes (STING) and whole-body STING deletion in diabetic mice showed similar renoprotection. Further analysis found that NR increased SIRT3 activity and improved mitochondrial function, which led to decreased mitochondrial DNA damage, a trigger for mitochondrial DNA leakage which activates the cGAS-STING pathway. Overall, these data show that NR supplementation boosted NAD metabolism to augment mitochondrial function, reducing inflammation and thereby preventing the progression of diabetic kidney disease.
Diabetes mellitus is the leading cause of cardiovascular and renal disease in the United -States. Despite the beneficial interventions available for patients with diabetes, there remains a need for additional therapeutic targets and therapies in diabetic kidney disease (DKD). Inflammation and oxidative stress are increasingly recognized as important causes of renal diseases. Inflammation is closely associated with mitochondrial damage. The molecular connection between inflammation and mitochondrial metabolism remains to be elucidated. Recently, nicotinamide adenine nucleotide (NAD+) metabolism has been found to regulate immune function and inflammation. In the present studies, we tested the hypothesis that enhancing NAD metabolism could prevent inflammation in and progression of DKD. We found that treatment of db/db mice with type 2 diabetes with nicotinamide riboside (NR) prevented several manifestations of kidney dysfunction ( i.e. , albuminuria, increased urinary kidney injury marker-1 (KIM1) excretion, and pathologic changes). These effects were associated with decreased inflammation, at least in part via inhibiting the activation of the cyclic GMP-AMP synthase-stimulator of interferon genes (cGAS-STING) signaling pathway. An antagonist of the serum stimulator of interferon genes (STING) and whole-body STING deletion in diabetic mice showed similar renoprotection. Further analysis found that NR increased SIRT3 activity and improved mitochondrial function, which led to decreased mitochondrial DNA damage, a trigger for mitochondrial DNA leakage which activates the cGAS-STING pathway. Overall, these data show that NR supplementation boosted NAD metabolism to augment mitochondrial function, reducing inflammation and thereby preventing the progression of diabetic kidney disease.
Diabetes mellitus is the leading cause of cardiovascular and renal disease in the United -States. Despite the beneficial interventions available for patients with diabetes, there remains a need for additional therapeutic targets and therapies in diabetic kidney disease (DKD). Inflammation and oxidative stress are increasingly recognized as important causes of renal diseases. Inflammation is closely associated with mitochondrial damage. The molecular connection between inflammation and mitochondrial metabolism remains to be elucidated. Recently, nicotinamide adenine nucleotide (NAD+) metabolism has been found to regulate immune function and inflammation. In the present studies, we tested the hypothesis that enhancing NAD metabolism could prevent inflammation in and progression of DKD. We found that treatment of db/db mice with type 2 diabetes with nicotinamide riboside (NR) prevented several manifestations of kidney dysfunction (i.e., albuminuria, increased urinary kidney injury marker-1 (KIM1) excretion, and pathologic changes). These effects were associated with decreased inflammation, at least in part via inhibiting the activation of the cyclic GMP-AMP synthase-stimulator of interferon genes (cGAS-STING) signaling pathway. An antagonist of the serum stimulator of interferon genes (STING) and whole-body STING deletion in diabetic mice showed similar renoprotection. Further analysis found that NR increased SIRT3 activity and improved mitochondrial function, which led to decreased mitochondrial DNA damage, a trigger for mitochondrial DNA leakage which activates the cGAS-STING pathway. Overall, these data show that NR supplementation boosted NAD metabolism to augment mitochondrial function, reducing inflammation and thereby preventing the progression of diabetic kidney disease.
ArticleNumber 104975
Author Wang, Xiaoxin X.
Wu, Ci
Ginley, Brandon
Panov, Julia
Sarder, Pinaki
Guha, Udayan
Bansal, Shivani
Ma, Junfeng
Levi, Moshe
Myakala, Komuraiah
Rosenberg, Avi Z.
Krawczyk, Ewa
Jang, Yura
Na, Chan Hyun
Zhang, Xu
Shults, Nataliia V.
Kopp, Jeffrey B.
Albanese, Chris
Hirschey, Matthew D.
Yang, Xiaoping
Cheema, Amrita
Yoshida, Teruhiko
Brodsky, Leonid
Qi, Yue
Jones, Bryce A.
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  givenname: Xiaoxin X.
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  fullname: Wang, Xiaoxin X.
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  organization: Department of Pathology, Johns Hopkins University, Baltimore, Maryland, USA
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  organization: Departments of Pathology and Anatomical Sciences, SUNY, Buffalo, New York, USA
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  organization: Department of Medicine-Quantitative Health, Department of Electrical and Computer Engineering, University of Florida, Gainesville, Florida, USA
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  organization: Tauber Bioinformatics Research Center, University of Haifa, Haifa, Israel
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  fullname: Jang, Yura
  organization: Department of Neurology, Institute for Cell Engineering, Johns Hopkins University, Baltimore, Maryland, USA
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  givenname: Chan Hyun
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  fullname: Na, Chan Hyun
  organization: Department of Neurology, Institute for Cell Engineering, Johns Hopkins University, Baltimore, Maryland, USA
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  surname: Qi
  fullname: Qi, Yue
  organization: Thoracic and GI Malignancies Branch, National Cancer Institute, National Institutes of Health, Bethesda, Maryland, USA
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  surname: Wu
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  organization: Department of Oncology, Lombardi Comprehensive Cancer Center, Georgetown University, Washington District of Columbia, USA
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  email: Moshe.Levi@georgetown.edu
  organization: Department of Biochemistry and Molecular & Cellular Biology, Georgetown University, Washington, District of Columbia, USA
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Keywords GLP-1
NR
SGLT2
▪
TBARS
KIM-1
NAD
ARB
4-HNE
FAO
ACEI
STING
cGAS-STING
DKD
diabetic kidney disease
mitochondrial DNA damage
mitochondria
sirtuin 3
inflammation, diabetes
Language English
License This is an open access article under the CC BY-NC-ND license.
Copyright © 2023 The Authors. Published by Elsevier Inc. All rights reserved.
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Snippet Diabetes mellitus is the leading cause of cardiovascular and renal disease in the United -States. Despite the beneficial interventions available for patients...
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SubjectTerms Animals
Diabetes Mellitus, Experimental - pathology
Diabetes Mellitus, Type 2 - metabolism
Diabetic Nephropathies - metabolism
DNA, Mitochondrial - metabolism
Inflammation - metabolism
Interferons - metabolism
Mice
Mitochondria - metabolism
NAD - metabolism
Nucleotidyltransferases - metabolism
▪
Title NAD metabolism modulates inflammation and mitochondria function in diabetic kidney disease
URI https://dx.doi.org/10.1016/j.jbc.2023.104975
https://www.ncbi.nlm.nih.gov/pubmed/37429506
https://www.proquest.com/docview/2847746982
https://pubmed.ncbi.nlm.nih.gov/PMC10413283
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