Literature DB >> 31120438

Platelet bioenergetics correlate with muscle energetics and are altered in older adults.

Andrea Braganza1, Catherine G Corey1, Adam J Santanasto2, Giovanna Distefano3, Paul M Coen3, Nancy W Glynn2, Seyed-Mehdi Nouraie1,4, Bret H Goodpaster3, Anne B Newman2, Sruti Shiva1,5,6.   

Abstract

BACKGROUND: Physical function decreases with age, and though bioenergetic alterations contribute to this decline, the mechanisms by which mitochondrial function changes with age remains unclear. This is partially because human mitochondrial studies require highly invasive procedures, such as muscle biopsies, to obtain live tissue with functional mitochondria. However, recent studies demonstrate that circulating blood cells are potentially informative in identifying systemic bioenergetic changes. Here, we hypothesize that human platelet bioenergetics reflect bioenergetics measured in muscle biopsies. METHODS &
RESULTS: We demonstrate that maximal and ATP-linked respiratory rate measured in isolated platelets from older adults (86-93 years) correlates significantly with maximal respiration (r = 0.595; P = 0.003) measured by muscle biopsy respirometry and maximal ATP production (r = 0.643; P = 0.004) measured by 31P-MRS respectively, in the same individuals. Comparison of platelet bioenergetics in this aged cohort to platelets from younger adults (18-35 years) shows aged adults demonstrate lower basal and ATP-linked respiration. Platelets from older adults also show enhanced proton leak, which is likely due to increased protein levels of uncoupling protein 2, and correlates with increased gate speed in this cohort (r = 0.58; P = 0.0019). While no significant difference in glycolysis was observed in older adults compared to younger adults, platelet glycolytic rate correlated with fatigability (r = 0.44; P = 0.016).
CONCLUSIONS: These data advance the mechanistic understanding of age-related changes in mitochondrial function. Further, they suggest that measuring platelet bioenergetics provides a potential supplement or surrogate for muscle biopsy measurement and may be a valuable tool to study mitochondrial involvement in age-related decline of physical function.

Entities:  

Keywords:  Bioenergetics; Muscle Biology; Platelets; Skeletal muscle; Vascular Biology

Mesh:

Substances:

Year:  2019        PMID: 31120438      PMCID: PMC6629251          DOI: 10.1172/jci.insight.128248

Source DB:  PubMed          Journal:  JCI Insight        ISSN: 2379-3708


  42 in total

1.  Oxidative capacity and ageing in human muscle.

Authors:  K E Conley; S A Jubrias; P C Esselman
Journal:  J Physiol       Date:  2000-07-01       Impact factor: 5.182

2.  Adipose tissue thickness affects in vivo quantitative near-IR spectroscopy in human skeletal muscle.

Authors:  M C van Beekvelt; M S Borghuis; B G van Engelen; R A Wevers; W N Colier
Journal:  Clin Sci (Lond)       Date:  2001-07       Impact factor: 6.124

3.  Attenuation of skeletal muscle and strength in the elderly: The Health ABC Study.

Authors:  B H Goodpaster; C L Carlson; M Visser; D E Kelley; A Scherzinger; T B Harris; E Stamm; A B Newman
Journal:  J Appl Physiol (1985)       Date:  2001-06

4.  Analyses of mitochondrial respiratory chain function and mitochondrial DNA deletion in human skeletal muscle: effect of ageing.

Authors:  J M Cooper; V M Mann; A H Schapira
Journal:  J Neurol Sci       Date:  1992-11       Impact factor: 3.181

5.  Superoxide activates mitochondrial uncoupling proteins.

Authors:  Karim S Echtay; Damien Roussel; Julie St-Pierre; Mika B Jekabsons; Susana Cadenas; Jeff A Stuart; James A Harper; Stephen J Roebuck; Alastair Morrison; Susan Pickering; John C Clapham; Martin D Brand
Journal:  Nature       Date:  2002-01-03       Impact factor: 49.962

6.  Regulation of skeletal muscle mitochondrial content during aging.

Authors:  Carrie N Lyons; Odile Mathieu-Costello; Christopher D Moyes
Journal:  J Gerontol A Biol Sci Med Sci       Date:  2006-01       Impact factor: 6.053

7.  Strength and muscle quality in a well-functioning cohort of older adults: the Health, Aging and Body Composition Study.

Authors:  Anne B Newman; Catherine L Haggerty; Bret Goodpaster; Tamara Harris; Steve Kritchevsky; Michael Nevitt; Toni P Miles; Marjolein Visser
Journal:  J Am Geriatr Soc       Date:  2003-03       Impact factor: 5.562

8.  Measuring fitness in healthy older adults: the Health ABC Long Distance Corridor Walk.

Authors:  E M Simonsick; P S Montgomery; A B Newman; D C Bauer; T Harris
Journal:  J Am Geriatr Soc       Date:  2001-11       Impact factor: 5.562

9.  Glucose sensing by POMC neurons regulates glucose homeostasis and is impaired in obesity.

Authors:  Laura E Parton; Chian Ping Ye; Roberto Coppari; Pablo J Enriori; Brian Choi; Chen-Yu Zhang; Chun Xu; Claudia R Vianna; Nina Balthasar; Charlotte E Lee; Joel K Elmquist; Michael A Cowley; Bradford B Lowell
Journal:  Nature       Date:  2007-08-29       Impact factor: 49.962

10.  Improvement in usual gait speed predicts better survival in older adults.

Authors:  Susan E Hardy; Subashan Perera; Yazan F Roumani; Julie M Chandler; Stephanie A Studenski
Journal:  J Am Geriatr Soc       Date:  2007-10-03       Impact factor: 5.562

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  17 in total

1.  Impaired skeletal muscle mitochondrial bioenergetics and physical performance in chronic kidney disease.

Authors:  Bryan Kestenbaum; Jorge Gamboa; Sophia Liu; Amir S Ali; Eric Shankland; Thomas Jue; Cecilia Giulivi; Lucas R Smith; Jonathan Himmelfarb; Ian H de Boer; Kevin Conley; Baback Roshanravan
Journal:  JCI Insight       Date:  2020-03-12

2.  Arginine for mitochondrial oxidative enzymopathy.

Authors:  Daniel B Kim-Shapiro; Mark T Gladwin
Journal:  Blood       Date:  2020-09-17       Impact factor: 22.113

3.  Mitochondrial respiration of human platelets in young adult and advanced age - Seahorse or O2k?

Authors:  J Jedlička; R Kunc; J Kuncová
Journal:  Physiol Res       Date:  2021-12-31       Impact factor: 1.881

4.  Self-reported sleep efficiency and duration are associated with bioenergetic function in peripheral blood mononuclear cells (PBMCs) of adults.

Authors:  H Matthew Lehrer; Lauren E Chu; Martica H Hall; Kyle W Murdock
Journal:  Mitochondrion       Date:  2021-11-14       Impact factor: 4.160

5.  Microvesicles transfer mitochondria and increase mitochondrial function in brain endothelial cells.

Authors:  Anisha D'Souza; Amelia Burch; Kandarp M Dave; Aravind Sreeram; Michael J Reynolds; Duncan X Dobbins; Yashika S Kamte; Wanzhu Zhao; Courtney Sabatelle; Gina M Joy; Vishal Soman; Uma R Chandran; Sruti S Shiva; Nidia Quillinan; Paco S Herson; Devika S Manickam
Journal:  J Control Release       Date:  2021-08-24       Impact factor: 11.467

6.  Inhibition of mitochondrial complex I leading to NAD+/NADH imbalance in type 2 diabetic patients who developed late stent thrombosis: Evidence from an integrative analysis of platelet bioenergetics and metabolomics.

Authors:  Mi-Jie Gao; Ning-Hua Cui; Xia'nan Liu; Xue-Bin Wang
Journal:  Redox Biol       Date:  2022-10-11       Impact factor: 10.787

7.  Ex vivo use of cell-permeable succinate prodrug attenuates mitochondrial dysfunction in blood cells obtained from carbon monoxide-poisoned individuals.

Authors:  Shawn Owiredu; Abhay Ranganathan; David M Eckmann; Frances S Shofer; Kevin Hardy; David S Lambert; Matthew Kelly; David H Jang
Journal:  Am J Physiol Cell Physiol       Date:  2020-05-06       Impact factor: 4.249

Review 8.  Blood-based bioenergetics: An emerging translational and clinical tool.

Authors:  Andrea Braganza; Gowtham K Annarapu; Sruti Shiva
Journal:  Mol Aspects Med       Date:  2019-12-18

Review 9.  Platelet Proteomes, Pathways, and Phenotypes as Informants of Vascular Wellness and Disease.

Authors:  Joseph E Aslan
Journal:  Arterioscler Thromb Vasc Biol       Date:  2021-01-14       Impact factor: 8.311

10.  Metabolic Flexibility and Mechanical Efficiency in Women Over-60.

Authors:  Cristina Blasco-Lafarga; Jordi Monferrer-Marín; Ainoa Roldán; Pablo Monteagudo; Ivan Chulvi-Medrano
Journal:  Front Physiol       Date:  2022-04-06       Impact factor: 4.755

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