Overfeeding and Substrate Availability, But Not Age or BMI, Alter Human Satellite Cell Function

Overview

Journal Nutrients

Date 2020 Jul 30

PMID 32722351

Citations 2

Authors

Dane W Fausnacht

Ryan P McMillan

Nabil E Boutagy

Ryan A Lupi

Mordecai M Harvey

Brenda M Davy

Kevin P Davy

Robert P Rhoads

Matthew W Hulver

Affiliations

Soon will be listed here.

Abstract

Satellite cells (SC) aid skeletal muscle growth and regeneration. SC-mediated skeletal muscle repair can both be influenced by and exacerbate several diseases linked to a fatty diet, obesity, and aging. The purpose of this study was to evaluate the effects of different lifestyle factors on SC function, including body mass index (BMI), age, and high-fat overfeeding. For this study, SCs were isolated from the vastus lateralis of sedentary young (18-30 years) and sedentary older (60-80 years) men with varying BMIs (18-32 kg/m), as well as young sedentary men before and after four weeks of overfeeding (OVF) (55% fat/ + 1000 kcal, = 4). The isolated SCs were then treated in vitro with a control (5 mM glucose, 10% fetal bovine serum (FBS)) or a high substrate growth media (HSM) (10% FBS, 25 mM glucose, and 400 μM 2:1 oleate-palmitate). Cells were assessed on their ability to proliferate, differentiate, and fuel substrate oxidation after differentiation. The effect of HSM was measured as the percentage difference between SCs exposed to HSM compared to control media. In vitro SC function was not affected by donor age. OVF reduced SC proliferation rates (-19% < 0.05) but did not influence differentiation. Cellular proliferation in response to HSM was correlated to the donor's body mass index (BMI) ( = 0.6121, < 0.01). When exposed to HSM, SCs from normal weight (BMI 18-25 kg/m) participants exhibited reduced proliferation and fusion rates with increased fatty-acid oxidation ( < 0.05), while SCs from participants with higher BMIs (BMI 25-32 kg/m) demonstrated enhanced proliferation in HSM. HSM reduced proliferation and fusion ( < 0.05) in SCs isolated from subjects before OVF, whereas HSM exposure accelerated proliferation and fusion in SCs collected following OVF. These results indicated that diet has a greater influence on SC function than age and BMI. Though age and BMI do not influence in vitro SC function when grown in controlled conditions, both factors influenced the response of SCs to substrate challenges, indicating age and BMI may mediate responses to diet.

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References

Palacios D, Mozzetta C, Consalvi S, Caretti G, Saccone V, Proserpio V . TNF/p38α/polycomb signaling to Pax7 locus in satellite cells links inflammation to the epigenetic control of muscle regeneration. Cell Stem Cell. 2010; 7(4):455-69. PMC: 2951277. DOI: 10.1016/j.stem.2010.08.013. View

Wen Y, Bi P, Liu W, Asakura A, Keller C, Kuang S . Constitutive Notch activation upregulates Pax7 and promotes the self-renewal of skeletal muscle satellite cells. Mol Cell Biol. 2012; 32(12):2300-11. PMC: 3372272. DOI: 10.1128/MCB.06753-11. View

Goodpaster B, Park S, Harris T, Kritchevsky S, Nevitt M, Schwartz A . The loss of skeletal muscle strength, mass, and quality in older adults: the health, aging and body composition study. J Gerontol A Biol Sci Med Sci. 2006; 61(10):1059-64. DOI: 10.1093/gerona/61.10.1059. View

Proto J, Tang Y, Lu A, Chen W, Stahl E, Poddar M . NF-κB inhibition reveals a novel role for HGF during skeletal muscle repair. Cell Death Dis. 2015; 6:e1730. PMC: 4650539. DOI: 10.1038/cddis.2015.66. View

Leturque A, Girard J . Expression and cellular localization of glucose transporters (GLUT1, GLUT3, GLUT4) during differentiation of myogenic cells isolated from rat foetuses. J Cell Sci. 1994; 107 ( Pt 3):487-96. View

Scarda A, Franzin C, Milan G, Sanna M, Dal Pra C, Pagano C . Increased adipogenic conversion of muscle satellite cells in obese Zucker rats. Int J Obes (Lond). 2010; 34(8):1319-27. DOI: 10.1038/ijo.2010.47. View

Alam M, Kauter K, Brown L . Naringin improves diet-induced cardiovascular dysfunction and obesity in high carbohydrate, high fat diet-fed rats. Nutrients. 2013; 5(3):637-50. PMC: 3705310. DOI: 10.3390/nu5030637. View

Kamli M, Kim J, Pokharel S, Jan A, Lee E, Choi I . Expressional studies of the aldehyde oxidase (AOX1) gene during myogenic differentiation in C2C12 cells. Biochem Biophys Res Commun. 2014; 450(4):1291-6. DOI: 10.1016/j.bbrc.2014.06.126. View

Javaheri B, Sunters A, Zaman G, Suswillo R, Saxon L, Lanyon L . Lrp5 is not required for the proliferative response of osteoblasts to strain but regulates proliferation and apoptosis in a cell autonomous manner. PLoS One. 2012; 7(5):e35726. PMC: 3342322. DOI: 10.1371/journal.pone.0035726. View

10.

Nicholson T, Church C, Baker D, Jones S . The role of adipokines in skeletal muscle inflammation and insulin sensitivity. J Inflamm (Lond). 2018; 15:9. PMC: 5944154. DOI: 10.1186/s12950-018-0185-8. View

11.

Abrigo J, Rivera J, Aravena J, Cabrera D, Simon F, Ezquer F . High Fat Diet-Induced Skeletal Muscle Wasting Is Decreased by Mesenchymal Stem Cells Administration: Implications on Oxidative Stress, Ubiquitin Proteasome Pathway Activation, and Myonuclear Apoptosis. Oxid Med Cell Longev. 2016; 2016:9047821. PMC: 4992759. DOI: 10.1155/2016/9047821. View

12.

Nyman L, Tian L, Hamm D, Schoeb T, Gower B, Nagy T . Long term effects of high fat or high carbohydrate diets on glucose tolerance in mice with heterozygous carnitine palmitoyltransferase-1a (CPT-1a) deficiency: Diet influences on CPT1a deficient mice. Nutr Diabetes. 2012; 1:e14. PMC: 3251273. DOI: 10.1038/nutd.2011.11. View

13.

Kondoh H, LLeonart M, Nakashima Y, Yokode M, Tanaka M, Bernard D . A high glycolytic flux supports the proliferative potential of murine embryonic stem cells. Antioxid Redox Signal. 2006; 9(3):293-9. DOI: 10.1089/ars.2006.1467. View

14.

Izumiya Y, Hopkins T, Morris C, Sato K, Zeng L, Viereck J . Fast/Glycolytic muscle fiber growth reduces fat mass and improves metabolic parameters in obese mice. Cell Metab. 2008; 7(2):159-72. PMC: 2828690. DOI: 10.1016/j.cmet.2007.11.003. View

15.

Frisard M, Wu Y, McMillan R, Voelker K, Wahlberg K, Anderson A . Low levels of lipopolysaccharide modulate mitochondrial oxygen consumption in skeletal muscle. Metabolism. 2014; 64(3):416-27. PMC: 4501015. DOI: 10.1016/j.metabol.2014.11.007. View

16.

Sacco A, Mourkioti F, Tran R, Choi J, Llewellyn M, Kraft P . Short telomeres and stem cell exhaustion model Duchenne muscular dystrophy in mdx/mTR mice. Cell. 2010; 143(7):1059-71. PMC: 3025608. DOI: 10.1016/j.cell.2010.11.039. View

17.

Shefer G, Rauner G, Yablonka-Reuveni Z, Benayahu D . Reduced satellite cell numbers and myogenic capacity in aging can be alleviated by endurance exercise. PLoS One. 2010; 5(10):e13307. PMC: 2953499. DOI: 10.1371/journal.pone.0013307. View

18.

Zhao Q, Yang S, Wang J, Zhou J, Xing S, Shen C . TNF alpha inhibits myogenic differentiation of C2C12 cells through NF-κB activation and impairment of IGF-1 signaling pathway. Biochem Biophys Res Commun. 2015; 458(4):790-5. DOI: 10.1016/j.bbrc.2015.02.026. View

19.

Xie L, Yin A, Nichenko A, Beedle A, Call J, Yin H . Transient HIF2A inhibition promotes satellite cell proliferation and muscle regeneration. J Clin Invest. 2018; 128(6):2339-2355. PMC: 5983316. DOI: 10.1172/JCI96208. View

20.

Urbani L, Piccoli M, Franzin C, Pozzobon M, De Coppi P . Hypoxia increases mouse satellite cell clone proliferation maintaining both in vitro and in vivo heterogeneity and myogenic potential. PLoS One. 2012; 7(11):e49860. PMC: 3500318. DOI: 10.1371/journal.pone.0049860. View