Cell metabolism sets the differences between subpopulations of satellite cells (SCs)

BMC Cell Biology

Michelangelo Campanella³  Paolo De Coppi¹  Luca Urbani¹  Simon Eaton¹  Ramona Lupi³  Andrea Repele² 

[1] Institute of Child Health & Great Ormond Street Hospital, London, UK;Department of Comparative Biomedical Sciences, the Royal Veterinary College, University College London; University of London, Royal College Street, London NW1 0TU, UK;EuropeanBrain Research Institute, Rita Levi-Montalcini Foundation, 00140, Rome, Italy

关键词: Apoptosis;    CO₂ production;    Metabolism;    Clones;    Satellite cells;   

Others  :  855331
DOI  :  10.1186/1471-2121-14-24

 received in 2012-07-05, accepted in 2013-01-23,  发布年份 2013

【 摘 要 】

Background

We have recently characterized two distinct populations of Satellite Cells (SCs) that differ in proliferation, regenerative potential, and mitochondrial coupling efficiency and classified these in Low Proliferative Clones (LPC) and High Proliferative Clones (HPC). Herewith, we have investigated their cell metabolism and individuated features that remark an intrinsic difference in basal physiology but that are retrievable also at the initial phases of their cloning.

Results

Indeed, LPC and HPC can be distinguished for mitochondrial membrane potential (ΔΨ_m) just after isolation from the fiber. This is matched by mitochondrial redox state measured via NAD⁺/NADH analysis and alternative respiratory CO₂ production in cloned cells. All these parameters are accountable for metabolic differences reflected indeed by alternative expression of the glycolytic enzyme 6-phosphofructo-2-kinase/fructose-2,6-biphosphatase 3 (Pfkfb3). Also Ca²⁺ handling by mitochondria is different together with the sensitivity to apoptosis triggered via this pathway. Finally, according to the above, we were able to determine which one among the clones represents the suitable stem cell.

Conclusions

These experimental observations report novel physiological features in the cell biology of SCs and refer to an intrinsic heterogeneity within which their stemness may reside.

【 授权许可】

   
2013 Repele et al.; licensee BioMed Central Ltd.

【 图 表 】

【 参考文献 】

• [1]Biressi S, Rando TA: Heterogeneity in the muscle satellite cell population. Semin Cell Dev Biol 2010, 21(8):845-854.
• [2]Shi X, Garry DJ: Muscle stem cells in development, regeneration, and disease. Genes Dev 2006, 20:1692-1708.
• [3]Gayraud-Morel B, Chretien F, Tajbakhsh S: Skeletal muscle as a paradigm for regenerative biology and medicine. Regenerative Med 2009, 4:293-319.
• [4]Sambasivan R, Tajbakhsh S: Skeletal muscle stem cell birth and properties. Semin Cell Dev Biol 2007, 18:870-882.
• [5]Bischoff R: The satellite cell and muscle regeneration. In Myology. Edited by Engle AG, Franzini-Armstrong C. New York: McGraw-Hill; 1994:97-118.
• [6]Tedesco FS, Dellavalle A, Diaz-Manera J, Messina G, Cossu G: Repairing skeletal muscle: regenerative potential of skeletal muscle stem cells. J Clin Invest 2010, 120(1):11-19.
• [7]Charge SB, Rudnicki MA: Cellular and molecular regulation of muscle regeneration. Physiol Rev 2004, 84:209-238.
• [8]Kuang S, Gillespie MA, Rudnicki MA: Niche regulation of muscle satellite cell self-renewal and differentiation. Cell Stem Cell 2008, 2(1):22-31.
• [9]Appell HJ, Forsberg S, Hollmann W: Satellite cell activation in human skeletal muscle after training: evidence for muscle fiber neoformation. Int J Sports Med 1988, 9:297-299.
• [10]Rosenblatt JD, Yong D, Parry DJ: Satellite cell activity is required for hypertrophy of overloaded adult rat muscle. Muscle Nerve 1994, 17:608-613.
• [11]Schultz E: Satellite cell in normal, regenerating and dystrophic muscle. Adv Exp Med Biol 1985, 182:73-84.
• [12]Huang S, Wang Z: Influence of platelet-rich plasma on proliferation and osteogenic differentiation of skeletal muscle satellite cells: an in vitro study. Oral Surg Oral Med Oral Pathol Oral Radiol Endod 2010, 110(4):453-462.
• [13]Rossi CA, Pozzobon M, Ditadi A, Archacka K, Gastaldello A, Sanna M, Franzin C, Malerba A, Milan G, Cananzi M, Schiaffino S, Campanella M, Vettor R, De Coppi P: Clonal characterization of rat muscle satellite cells: proliferation, metabolism and differentiation define an intrinsic heterogeneity. PLoS One 2010, 5(1):e8523.
• [14]Szabadkai G, Duchen MR: Mitochondria: the hub of cellular Ca2+ signalling. Physiology (Bethesda) 2008, 23:84-94.
• [15]Gastaldello A, Callaghan H, Gami P, Campanella M: Ca (2+) -dependent autophagy is enhanced by the pharmacological agent PK11195. Autophagy 2010, 6(5):607-613.
• [16]Campanella M, Seraphim A, Abeti R, Casswell E, Echave P, Duchen MR: IF1, the endogenous regulator of the F1F0-ATP synthase, defines mitochondrial volume fraction in HeLa cells by regulating autophagy. Biochim Biophys Acta 2009, 1787:393-401.
• [17]Mayevsky A, Rogatsky GG: Mitochondrial function in vivo evaluated by NADH fluorescence: from animal models to human studies. Am J Physiol Cell Physiol 2007, 292(2):C615-C640.
• [18]Abramov AY, Fraley C, Diao CT, Winkfein R, Colicos MA, Duchen MR, French RJ, Pavlov E: Targeted polyphosphatase expression alters mitochondrial metabolism and inhibits calcium-dependent cell death. Proc Natl Acad Sci 2007, 104(46):18091-18096.
• [19]Herrero-Mendez A, Almeida A, Fernández E, Maestre C, Moncada S, Bolaños JP: The bioenergetic and antioxidant status of neurons is controlled by continuous degradation of a key glycolytic enzyme by APC/C-Cdh1. Nat Cell Biol 2009, 11(6):747-752.
• [20]Yalcin A, Clem BF, Simmons A, Lane A, Nelson K, Clem AL, Brock E, Siow D, Wattenberg B, Telang S, Chesney J: Nuclear targeting of 6-phosphofructo-2-kinase (PFKFB3) increases proliferation via cyclin-dependent kinases. J Biol Chem 2009, 284(36):24223-24232.
• [21]McNamara CJ, Perry TD, Bearce K, Hernandez-Duque G, Mitchell R: Measurement of limestone biodeterioration using the Ca2+ binding fluorochrome Rhod-5N. J Microbiol Methods 2005, 61:245-250.
• [22]Soibinet M, Souchon V, Leray I, Valeur B: Rhod-5N as a fluorescent molecular sensor of cadmium (II) ion. J Fluoresc 2008, 18(6):1077-1082.
• [23]Lin X, Várnai P, Csordás G, Balla A, Nagai T, Miyawaki A, Balla T, Hajnóczky G: Control of calcium signal propagation to the mitochondria by inositol 1,4,5-trisphosphate-binding proteins. J Biol Chem 2005, 280(13):12820-12832.
• [24]Campanella M, Pinton P, Rizzuto R: Mitochondrial Ca2+ homeostasis in health and disease. Biol Res 2004, 37(4):653-660.
• [25]Delafosse B, Viale JP, Tissot S, Normand S, Pachiaudi C, Goudable J, Bouffard Y, Annat G, Bertrand O: Effects of glucose-to-lipid ratio and type of lipid on substrate oxidation rate in patients. Am J Physiol 1994, 267(5 Pt 1):E775-E780.