Density-dependent metabolic heterogeneity in human mesenchymal stem cells

Stem Cells

Volumn 33, Issue 11, 2015, Pages 3368-3381

  Liu, Yijun ^a   Muñoz, Nathalie ^b   Bunnell, Bruce A ^c   Logan, Timothy M ^b   Ma, Teng ^a,b  

^a FAMU FSU COLLEGE OF ENGINEERING   (United States)

^b FLORIDA STATE UNIVERSITY   (United States)

^c TULANE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Cellular proliferation; Cellular therapy; Hypoxia; Mesenchymal stem cells

Indexed keywords

ADENOSINE TRIPHOSPHATE; CD146 ANTIGEN; CELL SURFACE MARKER; GLUCOSE 6 PHOSPHATE DEHYDROGENASE; GLUTAMINE; LACTIC ACID; REACTIVE OXYGEN METABOLITE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE;

ADULT; ANTIGEN EXPRESSION; ARTICLE; CELL AGING; CELL COUNT; CELL CULTURE; CELL DENSITY; CELL EXPANSION; CELL HETEROGENEITY; CELL METABOLISM; CELL PROLIFERATION; CELL SIZE; CELL STRUCTURE; CELLULAR DISTRIBUTION; CITRIC ACID CYCLE; COLONY FORMING UNIT; COMPARATIVE STUDY; ENZYME ACTIVITY; FLOW CYTOMETRY; GENE EXPRESSION; GLYCOLYSIS; HUMAN; HUMAN CELL; IMMUNOCYTOCHEMISTRY; LACTATE BLOOD LEVEL; MASS FRAGMENTOGRAPHY; MESENCHYMAL STEM CELL; MITOCHONDRIAL MEMBRANE POTENTIAL; NORMAL HUMAN; OXIDATION REDUCTION STATE; OXIDATIVE PHOSPHORYLATION; PENTOSE PHOSPHATE CYCLE; PHENOTYPE; REAL TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SECRETION RATE; CELL DIFFERENTIATION; CELL SURVIVAL; GENETIC HETEROGENEITY; MESENCHYMAL STROMA CELL; METABOLISM; MIDDLE AGED; PHYSIOLOGY; PROCEDURES; YOUNG ADULT;

ADULT; CELL COUNT; CELL DIFFERENTIATION; CELL PROLIFERATION; CELL SURVIVAL; CELLS, CULTURED; GENETIC HETEROGENEITY; HUMANS; MESENCHYMAL STROMAL CELLS; MIDDLE AGED; YOUNG ADULT;

EID: 84945456771     PISSN: 10665099     EISSN: 15494918     Source Type: Journal    
DOI: 10.1002/stem.2097     Document Type: Article

References (63)

1. Prockop DJ, Olson SD,. Clinical trials with adult stem/progenitor cells for tissue repair: Let's not overlook some essential precautions. Blood 2007; 109: 3147-3151.
2. Prockop DJ, Kota DJ, Bazhanov N, et al., Evolving paradigms for repair of tissues by adult stem/progenitor cells (MSCs). J Cell Mol Med 2010; 14: 2190-2199.
3. Parekkadan B, Milwid JM,. Mesenchymal stem cells as therapeutics. Annu Rev Biomed Eng 2010; 12: 87-117.
4. Bara JJ, Richards RG, Alini M, et al., Bone marrow-derived mesenchymal stem cells change phenotype following in vitro culture: Implications for basic research and the clinic. Stem Cells 2014; 32: 1713-1723.
5. Russell KC, Phinney DG, Lacey MR, et al., In vitro high-capacity assay to quantify the clonal heterogeneity in trilineage potential of mesenchymal stem cells reveals a complex hierarchy of lineage commitment. Stem Cells 2010; 28: 788-798.
6. Muraglia A, Cancedda R, Quarto R,. Clonal mesenchymal progenitors from human bone marrow differentiate in vitro according to a hierarchical model. J Cell Sci 2000; 113: 1161-1166.
7. Whitfield MJ, Lee WCJ, Van Vliet KJ,. Onset of heterogeneity in culture-expanded bone marrow stromal cells. Stem Cell Res 2013; 11: 1365-1377.
8. Wagner W, Horn P, Castoldi M, et al., Replicative senescence of mesenchymal stem cells: A continuous and organized process. PloS One 2008; 3: e2213.
9. Zhang SH, Ge JB, Sun AJ, et al., Comparison of various kinds of bone marrow stem cells for the repair of infarcted myocardium: Single clonally purified non-hematopoietic mesenchymal stem cells serve as a superior source. J Cell Biochem 2006; 99: 1132-1147.
10. Lee RH, Hsu SC, Munoz J, et al., A subset of human rapidly self-renewing marrow stromal cells preferentially engraft in mice. Blood 2006; 107: 2153-2161.
11. Lee RH, Seo MJ, Pulin AA, et al., The CD34-like protein PODXL and alpha6-integrin (CD49f) identify early progenitor MSCs with increased clonogenicity and migration to infarcted heart in mice. Blood 2009; 113: 816-826.
12. Sepulveda JC, Tome M, Fernandez ME, et al., Cell senescence abrogates the therapeutic potential of human mesenchymal stem cells in the lethal endotoxemia model. Stem Cells 2014; 32: 1865-1877.
13. Folmes CD, Dzeja PP, Nelson TJ, et al., Metabolic plasticity in stem cell homeostasis and differentiation. Cell Stem Cell 2012; 11: 596-606.
14. Shyh-Chang N, Daley GQ, Cantley LC,. Stem cell metabolism in tissue development and aging. Development 2013; 140: 2535-2547.
15. Grayson WL, Zhao F, Izadpanah R, et al., Effects of hypoxia on human mesenchymal stem cell expansion and plasticity in 3D constructs. J Cell Physiol 2006; 207: 331-339.
16. Dos Santos F, Andrade PZ, Boura JS, et al., Ex vivo expansion of human mesenchymal stem cells: A more effective cell proliferation kinetics and metabolism under hypoxia. J Cell Physiol 2010; 223: 27-35.
17. Choudhery MS, Khan M, Mahmood R, et al., Mesenchymal stem cells conditioned with glucose depletion augments their ability to repair infarcted myocardium. J Cell Mol Med 2012; 16: 2518-29.
18. Buravkova LB, Rylova YV, Andreeva ER, et al., Low ATP level is sufficient to maintain the uncommitted state of multipotent mesenchymal stem cells. Biochim Biophys Acta 2013; 1830: 4418-4425.
19. Estrada JC, Albo C, Benguria A, et al., Culture of human mesenchymal stem cells at low oxygen tension improves growth and genetic stability by activating glycolysis. Cell Death Differ 2012; 19: 743-755.
20. Grayson WL, Zhao F, Bunnell B, et al., Hypoxia enhances proliferation and tissue formation of human mesenchymal stem cells. Biochem Biophys Res Commun 2007; 358: 948-953.
21. Mylotte LA, Duffy AM, Murphy M, et al., Metabolic flexibility permits mesenchymal stem cell survival in an ischemic environment. Stem Cells 2008; 26: 1325-1336.
22. Chen CT, Shih YRV, Kuo TK, et al., Coordinated changes of mitochondrial biogenesis and antioxidant enzymes during osteogenic differentiation of human mesenchymal stem cells. Stem Cells 2008; 26: 960-968.
23. Pattappa G, Heywood HK, De Bruijn JD, et al., The metabolism of human mesenchymal stem cells during proliferation and differentiation. J Cell Physiol 2011; 226: 2562-2570.
24. Yoon DS, Kim YH, Jung HS, et al., Importance of Sox2 in maintenance of cell proliferation and multipotency of mesenchymal stem cells in low-density culture. Cell Prolif 2011; 44: 428-440.
25. Zhao F, Ma T,. Perfusion bioreactor system for human mesenchymal stem cell tissue engineering: Dynamic cell seeding and construct development. Biotechnol Bioeng 2005; 91: 482-493.
26. Grayson WL, Ma T, Bunnell B,. Human mesenchymal stem cells tissue development in 3D PET matrices. Biotechnol Prog 2004; 20: 905-912.
27. Munoz N, Kim J, Liu Y, et al., Gas chromatography-mass spectrometry analysis of human mesenchymal stem cell metabolism during proliferation and osteogenic differentiation under different oxygen tensions. J Biotechnol 2014; 169: 95-102.
28. Kim J, Ma T,. Bioreactor strategy in bone tissue engineering: Pre-culture and osteogenic differentiation under two flow configurations. Tissue Eng Part A 2012; 18: 2354-2364.
29. Lv FJ, Tuan RS, Cheung KM, et al., The surface markers and identity of human mesenchymal stem cells. Stem Cells 2014; 32: 1408-1419.
30. Rafalski VA, Mancini E, Brunet A,. Energy metabolism and energy-sensing pathways in mammalian embryonic and adult stem cell fate. J Cell Sci 2012; 125: 5597-5608.
31. Metallo CM, Vander Heiden MG,. Understanding metabolic regulation and its influence on cell physiology. Mol Cell 2013; 49: 388-398.
32. Xu XL, Duan SL, Yi F, et al., Mitochondrial regulation in pluripotent stem cells. Cell Metab 2013; 18: 325-332.
33. Hamanaka RB, Chandel NS,. Mitochondrial reactive oxygen species regulate cellular signaling and dictate biological outcomes. Trends Biochem Sci 2010; 35: 505-513.
34. Tian WN, Braunstein LD, Pang JD, et al., Importance of glucose-6-phosphate dehydrogenase activity for cell growth. J Biol Chem 1998; 273: 10609-10617.
35. Stroncek DF, Sabatino M, Ren J, et al., Establishing a bone marrow stromal cell transplant program at the National Institutes of Health Clinical Center. Tissue Eng Part B Rev 2014; 20: 200-205.
36. Colter DC, Class R, DiGirolamo CM, et al., Rapid expansion of recycling stem cells in cultures of plastic-adherent cells from human bone marrow. Proc Natl Acad Sci USA 2000; 97: 3213-3218.
37. DiGirolamo CM, Stokes D, Colter D, et al., Propagation and senescence of human marrow stromal cells in culture: A simple colony-forming assay identifies samples with the greatest potential to propagate and differentiate. Br J Haematol 1999; 107: 275-281.
38. Jingting Li, Brendan Jones, Ying Zhang, et al., Low-density expansion protects human synovium-derived stem cells from replicative senescence: A preliminary study. Drug Deliv Transl Res 2012; 2: 363-374.
39. Bianco P, Robey PG, Simmons PJ,. Mesenchymal stem cells: Revisiting history, concepts, and assays. Cell Stem Cell 2008; 2: 313-319.
40. Kuznetsov SA, Mankani MH, Bianco P, et al., Enumeration of the colony-forming units-fibroblast from mouse and human bone marrow in normal and pathological conditions. Stem Cell Res 2009; 2: 83-94.
41. Sorrentino A, Ferracin M, Castelli G, et al., Isolation and characterization of CD146(+) multipotent mesenchymal stromal cells. Exp Hematol 2008; 36: 1035-1046.
42. Sacchetti B, Funari A, Michienzi S, et al., Self-renewing osteoprogenitors in bone marrow sinusoids can organize a hematopoietic microenvironment. Cell 2007; 131: 324-336.
43. Jones EA, Kinsey SE, English A, et al., Isolation and characterization of bone marrow multipotential mesenchymal progenitor cells. Arthritis Rheuma 2002; 46: 3349-3360.
44. Boiani M, Scholer HR,. Regulatory networks in embryo-derived pluripotent stem cells. Nat Rev Mol Cell Bio 2005; 6: 872-884.
45. Kleijn RJ, van Winden WA, van Gulik WM, et al., Revisiting the C-13-label distribution of the non-oxidative branch of the pentose phosphate pathway based upon kinetic and genetic evidence. FEBS J 2005; 272: 4970-4982.
46. Brekke EMF, Walls AB, Schousboe A, et al., Quantitative importance of the pentose phosphate pathway determined by incorporation of C-13 from [2-C-13]- and [3-C-13]glucose into TCA cycle intermediates and neurotransmitter amino acids in functionally intact neurons. J Cereb Blood Flow Metab 2012; 32: 1788-1799.
47. Dusick JR, Glenn TC, Lee WP, et al., Increased pentose phosphate pathway flux after clinical traumatic brain injury: A [1,2-C-13(2)]glucose labeling study in humans. J Cereb Blood Flow Metab 2007; 27: 1593-1602.
48. Brandl A, Meyer M, Bechmann V, et al., Oxidative stress induces senescence in human mesenchymal stem cells. Exp Cell Res 2011; 317: 1541-1547.
49. Van Blerkom J,. Mitochondria in early mammalian development. Semin Cell Dev Biol 2009; 20: 354-364.
50. Schieke SM, Ma MC, Cao L, et al., Mitochondrial metabolism modulates differentiation and teratoma formation capacity in mouse embryonic stem cells. J Biol Chem 2008; 283: 28506-28512.
51. Simsek T, Kocabas F, Zheng JK, et al., The distinct metabolic profile of hematopoietic stem cells reflects their location in a hypoxic niche. Cell Stem Cell 2010; 7: 380-390.
52. Arranz L, Urbano-Ispizua A, Mendez-Ferrer S,. Mitochondria underlie different metabolism of hematopoietic stem and progenitor cells. Haematologica 2013; 98: 993-995.
53. Romero-Moya D, Bueno C, Montes R, et al., Cord blood-derived CD34(+) hematopoietic cells with low mitochondrial mass are enriched in hematopoietic repopulating stem cell function. Haematologica 2013; 98: 1022-1029.
54. Lonergan T, Brenner C, Bavister B,. Differentiation-related changes in mitochondrial properties as indicators of stem cell competence. J Cell Physiol 2006; 208: 149-153.
55. Chen CT, Hsu SH, Wei YH,. Upregulation of mitochondrial function and antioxidant defense in the differentiation of stem cells. Biochim Biophys Acta 2010; 1800: 257-263.
56. Ma T, Grayson WL, Frohlich M, et al., Hypoxia and stem cell-based engineering of mesenchymal tissues. Biotechnol Prog 2009; 25: 32-42.
57. Palomaki S, Pietila M, Laitinen S, et al., HIF-1 alpha is upregulated in human mesenchymal stem cells. Stem cells 2013; 31: 1902-1909.
58. Fink BD, Hong YS, Mathahs MM, et al., UCP2-dependent proton leak in isolated mammalian mitochondria. J Biol Chem 2002; 277: 3918-3925.
59. Krauss S, Zhang CY, Lowell BB,. A significant portion of mitochondrial proton leak in intact thymocytes depends on expression of UCP2. Proc Natl Acad Sci USA 2002; 99: 118-122.
60. Zhang J, Khvorostov I, Hong JS, et al., UCP2 regulates energy metabolism and differentiation potential of human pluripotent stem cells. EMBO J 2011; 30: 4860-4873.
61. Rombouts WJC, Ploemacher RE,. Primary murine MSC show highly efficient homing to the bone marrow but lose homing ability following culture. Leukemia 2003; 17: 160-170.
62. Li WY, Choi YJ, Lee PH, et al., Mesenchymal stem cells for ischemic stroke: Changes in effects after ex vivo culturing. Cell Transplant 2008; 17: 1045-1059.
63. McMurray RJ, Gadegaard N, Tsimbouri PM, et al., Nanoscale surfaces for the long-term maintenance of mesenchymal stem cell phenotype and multipotency. Nat Mater 2011; 10: 637-644.