Circulating hsa-miRNAs; Next generation sequencing; Sarcopenia; TaqMan qPCR; MicroRNAs; Male; Humans; Aged; Sarcopenia/genetics; MicroRNAs/genetics; MicroRNAs/metabolism; Aging; Geriatrics and Gerontology
Abstract :
[en] [en] OBJECTIVE: To identify a microRNA signature associated to sarcopenia in community-dwelling older adults form the SarcoPhAge cohort.
METHODS: In a screening phase by next generation sequencing (NGS), we compared the hsa-miRome expression of 18 subjects with sarcopenia (79.6 ± 6.8 years, 9 men) and 19 healthy subjects without sarcopenia (77.1 ± 6 years, 9 men) at baseline. Thereafter, we have selected eight candidate hsa-miRNAs according to the NGS results and after a critical assessment of previous literature. In a validation phase and by real-time qPCR, we then analyzed the expression levels of these 8 hsa-miRNAs at baseline selecting 92 healthy subjects (74.2 ± 10 years) and 92 subjects with sarcopenia (75.3 ± 6.8 years). For both steps, the groups were matched for age and sex.
RESULTS: In the validation phase, serum has-miRNA-133a-3p and has-miRNA-200a-3p were significantly decreased in the group with sarcopenia vs controls [RQ: relative quantification; median (interquartile range)]: -0.16 (-1.26/+0.90) vs +0.34 (-0.73/+1.33) (p < 0.01) and -0.26 (-1.07/+0.68) vs +0.27 (-0.55/+1.10) (p < 0.01) respectively. Has-miRNA-744-5p was decreased and has-miRNA-151a-3p was increased in the group with sarcopenia vs controls, but this barely reached significance: +0.16 (-1.34/+0.79) vs +0.44 (-0.31/+1.00) (p = 0.050) and +0.35 (-0.22/+0.90) vs +0.03 (-0.68/+0.75) (p = 0.054).
CONCLUSION: In subjects with sarcopenia, serum hsa-miRNA-133a-3p and hsa-miRNA-200a-3p expression were downregulated, consistent with their potential targets inhibiting muscle cells proliferation and differentiation.
Disciplines :
Public health, health care sciences & services Laboratory medicine & medical technology
Author, co-author :
Millet, Marjorie; INSERM 1033, Lyon, France ; PMO, Lyon, France
Auroux, Maxime; INSERM 1033, Lyon, France ; Hôpital E. Herriot, Hospices Civils de Lyon, Lyon, France
Beaudart, Charlotte ; Université de Liège - ULiège > Département des sciences de la santé publique > Epidémiologie générale ; Clinical Pharmacology and Toxicology Research Unit (URPC), NARILIS, Department of Biomedical Sciences, Faculty of Medicine, University of Namur, Namur, Belgium
Demonceau, Céline ; Université de Liège - ULiège > Unité de recherche Santé publique, épidémiologie et économie de la santé (URSAPES)
Ladang, Aurélie ; Université de Liège - ULiège > Département de pharmacie > Chimie médicale
Cavalier, Etienne ; Université de Liège - ULiège > Département de pharmacie > Chimie médicale
Reginster, Jean-Yves ; Université de Liège - ULiège > Département des sciences de la santé publique
Bruyère, Olivier ; Université de Liège - ULiège > Département des sciences de la santé publique > Santé publique, Epidémiologie et Economie de la santé
Chapurlat, Roland; INSERM 1033, Lyon, France ; PMO, Lyon, France ; Hôpital E. Herriot, Hospices Civils de Lyon, Lyon, France ; University of Lyon, Lyon, France
Rousseau, Jean-Charles ; INSERM 1033, Lyon, France. jean-charles.rousseau@inserm.fr ; PMO, Lyon, France. jean-charles.rousseau@inserm.fr
Language :
English
Title :
Association of circulating hsa-miRNAs with sarcopenia: the SarcoPhAge study.
Publication date :
14 March 2024
Journal title :
Aging Clinical and Experimental Research
ISSN :
1594-0667
eISSN :
1720-8319
Publisher :
Springer Science and Business Media Deutschland GmbH, Germany
A.J. Cruz-Jentoft G. Bahat J. Bauer Y. Boirie O. Bruyere T. Cederholm et al. Sarcopenia: revised European consensus on definition and diagnosis Age Ageing 2019 48 601 31081853 6593317
Z. Javanmardifard S. Shahrbanian S.J. Mowla MicroRNAs associated with signaling pathways and exercise adaptation in sarcopenia Life Sci 2021 285 1:CAS:528:DC%2BB3MXitVKmsrfL 34480932
F. Petermann-Rocha V. Balntzi S.R. Gray J. Lara F.K. Ho J.P. Pell et al. Global prevalence of sarcopenia and severe sarcopenia: a systematic review and meta-analysis J Cachexia Sarcopenia Muscle 2022 13 86 99 34816624
O. Yilmaz G. Bahat Muscle mass adjustment method affects association of sarcopenia and sarcopenic obesity with metabolic syndrome Geriatr Gerontol Int 2019 19 272 30821065
O. Ethgen C. Beaudart F. Buckinx O. Bruyere J.Y. Reginster The future prevalence of sarcopenia in Europe: a claim for public health action Calcif Tissue Int 2017 100 229 234 1:CAS:528:DC%2BC28XitFCls7fN 28012107
A. Ladang C. Beaudart J.Y. Reginster N. Al-Daghri O. Bruyere N. Burlet et al. Biochemical markers of musculoskeletal health and aging to be assessed in clinical trials of drugs aiming at the treatment of sarcopenia: consensus paper from an expert group meeting organized by the European Society for Clinical and Economic Aspects of Osteoporosis, Osteoarthritis and Musculoskeletal Diseases (ESCEO) and the Centre Academique de Recherche et d'Experimentation en Sante (CARES SPRL), Under the auspices of the World Health Organization Collaborating Center for the epidemiology of musculoskeletal conditions and aging Calcif Tissue Int 2023 112 197 217 1:CAS:528:DC%2BB3sXhtV2mtbs%3D 36633611 9859913
L.M. Margolis D.A. Rivas Potential role of microRNA in the anabolic capacity of skeletal muscle with aging Exerc Sport Sci Rev 2018 46 86 91 29346160 5856619
C. Beaudart J.Y. Reginster J. Petermans S. Gillain A. Quabron M. Locquet et al. Quality of life and physical components linked to sarcopenia: the SarcoPhAge study Exp Gerontol 2015 69 103 110 1:STN:280:DC%2BC2Mfktl2ltg%3D%3D 25979160
A.J. Cruz-Jentoft J.P. Baeyens J.M. Bauer Y. Boirie T. Cederholm F. Landi et al. Sarcopenia: European consensus on definition and diagnosis: report of the European working group on sarcopenia in older people Age Ageing 2010 39 412 423 20392703 2886201
R.N. Baumgartner K.M. Koehler D. Gallagher L. Romero S.B. Heymsfield R.R. Ross et al. Epidemiology of sarcopenia among the elderly in New Mexico Am J Epidemiol 1998 147 755 763 1:STN:280:DyaK1c3htlSkuw%3D%3D 9554417
H.C. Roberts H.J. Denison H.J. Martin H.P. Patel H. Syddall C. Cooper et al. A review of the measurement of grip strength in clinical and epidemiological studies: towards a standardised approach Age Ageing 2011 40 423 429 21624928
J.M. Guralnik L. Ferrucci C.F. Pieper S.G. Leveille K.S. Markides G.V. Ostir et al. Lower extremity function and subsequent disability: consistency across studies, predictive models, and value of gait speed alone compared with the short physical performance battery J Gerontol A Biol Sci Med Sci 2000 55 M221 M231 1:STN:280:DC%2BD3c3mvFaruw%3D%3D 10811152
M.A. Legrand M. Millet B. Merle J.C. Rousseau A. Hemmendinger E. Gineyts et al. A signature of circulating miRNAs associated with fibrous dysplasia of bone: the mirDys study J Bone Miner Res 2020 35 1881 1892 1:CAS:528:DC%2BB3cXitFehtrvN 32526052
J.C. Rousseau M. Millet M. Croset E. Sornay-Rendu O. Borel R. Chapurlat Association of circulating microRNAs with prevalent and incident knee osteoarthritis in women: the OFELY study Arthritis Res Ther 2020 22 2 1:CAS:528:DC%2BB3cXmtVyhsg%3D%3D 31898522 6941326
A. Mercier-Guery M. Millet B. Merle C. Collet F. Bagouet O. Borel et al. Dysregulation of microRNAs in adult osteogenesis imperfecta: the miROI study J Bone Miner Res 2023 38 1665 1678 1:CAS:528:DC%2BB3sXitVCkurrM 37715362
L. Zhang M. Yang P. Marks L.M. White M. Hurtig Q.S. Mi et al. Serum non-coding RNAs as biomarkers for osteoarthritis progression after ACL injury Osteoar Cartil 2012 20 1631 1637 1:STN:280:DC%2BC38bjslSrsg%3D%3D
V.M. Borgonio Cuadra N.C. Gonzalez-Huerta S. Romero-Cordoba A. Hidalgo-Miranda A. Miranda-Duarte Altered expression of circulating microRNA in plasma of patients with primary osteoarthritis and in silico analysis of their pathways PLoS ONE 2014 9 2014PLoSO..997690B 24901787 4046959
C. Beyer A. Zampetaki N.Y. Lin A. Kleyer C. Perricone A. Iagnocco et al. Signature of circulating microRNAs in osteoarthritis Ann Rheum Dis 2015 74 24515954
Y.H. Li G. Tavallaee T. Tokar A. Nakamura K. Sundararajan A. Weston et al. Identification of synovial fluid microRNA signature in knee osteoarthritis: differentiating early- and late-stage knee osteoarthritis Osteoarth Cartil 2016 24 1577 1586 1:CAS:528:DC%2BC28XitFCqt7vO
R. Kong J. Gao Y. Si D. Zhao Combination of circulating miR-19b-3p, miR-122-5p and miR-486-5p expressions correlates with risk and disease severity of knee osteoarthritis Am J Transl Res 2017 9 2852 2864 1:CAS:528:DC%2BC1cXisVChurnJ 28670374 5489886
E. Ntoumou M. Tzetis M. Braoudaki G. Lambrou M. Poulou K. Malizos et al. Serum microRNA array analysis identifies miR-140-3p, miR-33b-3p and miR-671-3p as potential osteoarthritis biomarkers involved in metabolic processes Clin Epigenetics 2017 9 127 1:STN:280:DC%2BC1MzivFKhsA%3D%3D 29255496 5728069
H.C. Liu D.S. Han C.C. Hsu J.S. Wang Circulating microRNA-486 and microRNA-146a serve as potential biomarkers of sarcopenia in the older adults BMC Geriatr 2021 21 86 2021Mate..15..86L 1:CAS:528:DC%2BB3MXkslSgtr4%3D 33516190 7847166
S. Peng C. Song H. Li X. Cao Y. Ma X. Wang et al. Circular RNA SNX29 sponges miR-744 to regulate proliferation and differentiation of myoblasts by activating the Wnt5a/Ca(2+) signaling pathway Mol Ther Nucleic Acids 2019 16 481 493 1:CAS:528:DC%2BC1MXhtFerurjP 31051333 6495097
D.M. Brown K. Goljanek-Whysall microRNAs: modulators of the underlying pathophysiology of sarcopenia? Ageing Res Rev 2015 24 263 273 1:CAS:528:DC%2BC2MXhsVyitbbO 26342566
R. Qaisar A. Karim T. Muhammad I. Shah J. Khan Circulating microRNAs as biomarkers of accelerated sarcopenia in chronic heart failure Glob Heart 2021 16 56 34692380 8415175
F. Iannone A. Montesanto E. Cione P. Crocco M.C. Caroleo S. Dato et al. Expression patterns of muscle-specific miR-133b and miR-206 correlate with nutritional status and sarcopenia Nutrients 2020 12 297 1:CAS:528:DC%2BB3cXhslGks73N 31979011 7071413
H. Wei Z. Li X. Wang J. Wang W. Pang G. Yang et al. MicroRNA-151-3p regulates slow muscle gene expression by targeting ATP2a2 in skeletal muscle cells J Cell Physiol 2015 230 1003 1012 1:CAS:528:DC%2BC2MXhslamtLc%3D 25200835
J.F. Chen E.M. Mandel J.M. Thomson Q. Wu T.E. Callis S.M. Hammond et al. The role of microRNA-1 and microRNA-133 in skeletal muscle proliferation and differentiation Nat Genet 2006 38 228 233 1:CAS:528:DC%2BD28XotlGktg%3D%3D 16380711
P. Gonzalez-Lopez C. Ares-Carral A.R. Lopez-Pastor J. Infante-Menendez T. Gonzalez llaness M. Vega de Ceniga et al. Implication of miR-155-5p and miR-143-3p in the vascular insulin resistance and instability of human and experimental atherosclerotic plaque Int J Mol Sci 2022 23 10253 1:CAS:528:DC%2BB38XisFagtLnP 36142173 9499612
Y. Bian W. Cai H. Lu S. Tang K. Yang Y. Tan miR-150-5p affects AS plaque with ASMC proliferation and migration by STAT1 Open Med (Wars) 2021 16 1642 1652 34761115
Z. Shi Q. Zhu J. Fan lncRNA TUG1 promotes atherosclerosis progression by targeting miR-382-5p Int J Clin Exp Pathol 2021 14 972 979 1:CAS:528:DC%2BB38XjtlynsLY%3D 34646415 8493262
P. Huang Y. Zhang F. Wang M. Qin L. Ren MiRNA-205-5p regulates the ERBB4/AKT signaling pathway to inhibit the proliferation and migration of HAVSMCs induced by ox-LDL Pathol Res Pract 2022 233 1:CAS:528:DC%2BB38Xhtlajs7nK 35364459
P. Huang F. Wang Y. Zhang Y. Zhang M. Qin J. Ji et al. Icariin alleviates atherosclerosis by regulating the miR-205-5p/ERBB4/AKT signaling pathway Int Immunopharmacol 2023 114 1:CAS:528:DC%2BB38XjtFGqtLrL 36700779
Y. Zhang H. Wang Y. Xia The expression of miR-211-5p in atherosclerosis and its influence on diagnosis and prognosis BMC Cardiovasc Disord 2021 21 371 34340677 8330028
J. Yang X. Zhou J. Lu M. Li miR-146-5p restrains calcification of vascular smooth muscle cells by suppressing TRAF6 Open Med (Wars) 2022 17 1515 1527 1:CAS:528:DC%2BB3sXltFOjtLY%3D 36237831
X. Wei Y. Su Q. Li Z. Zheng P. Hou Analysis of crucial genes, pathways and construction of the molecular regulatory networks in vascular smooth muscle cell calcification Exp Ther Med 2021 21 589 1:CAS:528:DC%2BB3MXptFais7Y%3D 33850561 8027762
D. Pan G. Liu B. Li J. Jiang W. Chen W. Li et al. MicroRNA-1246 regulates proliferation, invasion, and differentiation in human vascular smooth muscle cells by targeting cystic fibrosis transmembrane conductance regulator (CFTR) Pflugers Arch 2021 473 231 240 1:CAS:528:DC%2BB3MXpsVelsg%3D%3D 33420548
S. Bi Q. Peng W. Liu C. Zhang Z. Liu MicroRNA-342-5p activates the Akt signaling pathway by downregulating PIK3R1 to modify the proliferation and differentiation of vascular smooth muscle cells Exp Ther Med 2020 20 239 1:CAS:528:DC%2BB3cXit1ymurvF 33193844 7646700
N. Park H. Kang BMP-induced microRNA-101 expression regulates vascular smooth muscle cell migration Int J Mol Sci 2020 21 4764 1:CAS:528:DC%2BB3cXhvF2gsLzF 32635504 7369869
L. Fang X. Wang M. Zhang P. Khan M. Tamm M. Roth MicroRNA-101-3p Suppresses mTOR and causes mitochondrial fragmentation and cell degeneration in COPD Can Respir J 2022 2022 5933324 36518817 9744603
J. Meng Y. Zou L. Hou L. He Y. Liu M. Cao et al. MiR-140-3p ameliorates the inflammatory response of airway smooth muscle cells by targeting HMGB1 to regulate the JAK2/STAT3 signaling pathway Cell J 2022 24 673 680 36377217 9663964
G. Wang X. Tao L. Peng miR-155-5p regulates hypoxia-induced pulmonary artery smooth muscle cell function by targeting PYGL Bioengineered 2022 13 12985 12997 1:CAS:528:DC%2BB38XhsVSnsL7J 35611851 9275946
Z. Zhuang Y. Zhou J. Xu L. Pan Anti-asthmatic miR-224-5p inhibits the FHL1/MAPK pathway to repress airway smooth muscle cell proliferation in a murine model of asthma-like airway inflammation Allergy Asthma Clin Immunol 2022 18 88 1:CAS:528:DC%2BB38Xis1CjsL3M 36184652 9526920
J. Wang R. Jiang Y. Tan K. Cheng Human pulmonary artery smooth muscle cell dysfunction is regulated by miR-509-5p in hypoxic environment Cell Cycle 2022 21 1212 1221 1:CAS:528:DC%2BB38XmtFyitb0%3D 35244512 9103279
Z. Hou X. Qin Y. Hu X. Zhang G. Li J. Wu et al. Longterm exercise-derived exosomal miR-342-5p: a novel exerkine for cardioprotection Circ Res 2019 124 1386 1400 1:CAS:528:DC%2BC1MXotlWmsLY%3D 30879399
D.Z. Wei C. Lin Y.Q. Huang L.P. Wu M.Y. Huang Ellagic acid promotes ventricular remodeling after acute myocardial infarction by up-regulating miR-140-3p Biomed Pharmacother 2017 95 983 989 1:CAS:528:DC%2BC2sXhsFSmtr%2FI 28922712
Z. Wang M. Fu Y. Li miR-142-5p and miR-212-5p cooperatively inhibit the proliferation and collagen formation of cardiac fibroblasts by regulating c-Myc/TP53INP1 Can J Physiol Pharmacol 2020 98 314 323 1:CAS:528:DC%2BB3cXosVWrtbY%3D 32268073
J. Zhou L. Li H. Hu J. Wu H. Chen K. Feng et al. Circ-HIPK2 accelerates cell apoptosis and autophagy in myocardial oxidative injury by sponging miR-485-5p and targeting ATG101 J Cardiovasc Pharmacol 2020 76 427 436 1:CAS:528:DC%2BB3cXitVSjtLvO 33027196
S. Xiao Y. Zhou Q. Liu T. Zhang D. Pan Identification of pivotal microRNAs and target genes associated with persistent atrial fibrillation based on bioinformatics analysis Comput Math Methods Med 2021 2021 6680211 33747117 7960048
H. Li J. Fan Z. Yin F. Wang C. Chen D.W. Wang Identification of cardiac-related circulating microRNA profile in human chronic heart failure Oncotarget 2016 7 33 45 26683101
B. Krist P. Podkalicka O. Mucha M. Mendel A. Sepiol O.M. Rusiecka et al. miR-378a influences vascularization in skeletal muscles Cardiovasc Res 2020 116 1386 1397 1:CAS:528:DC%2BB3cXht1OhsrjO 31504257
S. Muroya M. Taniguchi M. Shibata M. Oe K. Ojima I. Nakajima et al. Profiling of differentially expressed microRNA and the bioinformatic target gene analyses in bovine fast- and slow-type muscles by massively parallel sequencing J Anim Sci 2013 91 90 103 1:CAS:528:DC%2BC3sXjsFKitrY%3D 23100578
C. Lu J. Wu S. Xiong X. Zhang J. Zhang J. Mei MicroRNA-203a regulates fast muscle differentiation by targeting dmrt2a in zebrafish embryos Gene 2017 625 49 54 1:CAS:528:DC%2BC2sXnsFSju74%3D 28483596
X. Shen C. Cui S. Tang S. Han Y. Zhang L. Xia et al. MyoG-enhanced circGPD2 regulates chicken skeletal muscle development by targeting miR-203a Int J Biol Macromol 2022 222 2212 2224 1:CAS:528:DC%2BB38XisF2gtb7J 36208808
W. Wu Y. Shang S. Dai C. Yu J. Wang Downregulation of miR-142-5p inhibits human aortic smooth muscle cell proliferation and migration by targeting MKL2 Mol Med Rep 2020 22 277 285 32626937 7248461
E.M. Small J.R. O'Rourke V. Moresi L.B. Sutherland J. McAnally R.D. Gerard et al. Regulation of PI3-kinase/Akt signaling by muscle-enriched microRNA-486 Proc Natl Acad Sci U S A 2010 107 4218 4223 2010PNAS.107.4218S 1:CAS:528:DC%2BC3cXjtlKmsrc%3D 20142475 2840099
M. Xu X. Chen D. Chen B. Yu Z. Huang FoxO1: a novel insight into its molecular mechanisms in the regulation of skeletal muscle differentiation and fiber type specification Oncotarget 2017 8 10662 10674 27793012
H. Park X. Huang C. Lu M.S. Cairo X. Zhou MicroRNA-146a and microRNA-146b regulate human dendritic cell apoptosis and cytokine production by targeting TRAF6 and IRAK1 proteins J Biol Chem 2015 290 2831 2841 1:CAS:528:DC%2BC2MXhvVersrg%3D 25505246
M. Jiang Y. Xiang D. Wang J. Gao D. Liu Y. Liu et al. Dysregulated expression of miR-146a contributes to age-related dysfunction of macrophages Aging Cell 2012 11 29 40 1:CAS:528:DC%2BC38XitVensLc%3D 21981419
Z. Chen M.G. Bemben D.A. Bemben Bone and muscle specific circulating microRNAs in postmenopausal women based on osteoporosis and sarcopenia status Bone 2019 120 271 278 1:CAS:528:DC%2BC1cXit1CgsrfL 30408612
N. He Y.L. Zhang Y. Zhang B. Feng Z. Zheng D. Wang et al. Circulating microRNAs in plasma decrease in response to sarcopenia in the elderly Front Genet 2020 11 167 1:CAS:528:DC%2BB3cXhvVarsbjP 32194634 7066121
N. He Y. Zhang Y. Zhang B. Feng Z. Zheng D. Wang et al. Increasing fracture risk associates with plasma circulating microRNAs in aging people's sarcopenia Front Physiol 2021 12 34163374 8215392
A. Luo H. Yan J. Liang C. Du X. Zhao L. Sun et al. MicroRNA-21 regulates hepatic glucose metabolism by targeting FOXO1 Gene 2017 627 194 201 1:CAS:528:DC%2BC2sXhtVGmsbbM 28627440
M.Y. Zhao L.M. Wang J. Liu X. Huang J. Liu Y.F. Zhang MiR-21 Suppresses anoikis through targeting PDCD4 and PTEN in human esophageal adenocarcinoma Curr Med Sci 2018 38 245 251 1:CAS:528:DC%2BC1cXptV2ks74%3D 30074182
N. Bakkar J. Wang K.J. Ladner H. Wang J.M. Dahlman M. Carathers et al. IKK/NF-kappaB regulates skeletal myogenesis via a signaling switch to inhibit differentiation and promote mitochondrial biogenesis J Cell Biol 2008 180 787 802 1:CAS:528:DC%2BD1cXis12iurg%3D 18299349 2265568
P. Bella A. Farini S. Banfi D. Parolini N. Tonna M. Meregalli et al. Blockade of IGF2R improves muscle regeneration and ameliorates Duchenne muscular dystrophy EMBO Mol Med 2020 12 1:CAS:528:DC%2BC1MXit1OhtL7M 31793167
H. Yin H. He X. Shen S. Tang J. Zhao X. Cao et al. MicroRNA profiling reveals an abundant miR-200a-3p promotes skeletal muscle satellite cell development by targeting TGF-beta2 and regulating the TGF-beta2/SMAD signaling pathway Int J Mol Sci 2020 21 3274 1:CAS:528:DC%2BB3cXhvVOjsL3M 32380777 7247338
S. Valaskova A. Gazova P. Vrbova T. Koller B. Salingova A. Adamickova et al. The severity of muscle performance deterioration in sarcopenia correlates with circulating muscle tissue-specific miRNAs Physiol Res 2021 70 S91 S98 1:CAS:528:DC%2BB38Xjtlyrt70%3D 35503054 8884374