Cellular mechanical properties reflect the differentiation potential of adipose-derived mesenchymal stem cells

Proceedings of the National Academy of Sciences of the United States of America

Volumn 109, Issue 24, 2012, Pages

  González Cruz, Rafael D ^a,b   Fonseca, Vera C ^a,b   Darling, Eric M ^a,b,c  

^a BROWN UNIVERSITY   (United States)

^b BROWN UNIVERSITY   (United States)

^c Brown University   (United States)

Author keywords

AFM; Cell mechanics; Mesenchymal stem cell enrichment; Single cell characterization; Viscoelasticity

Indexed keywords

BIOLOGICAL MARKER; CELL SURFACE MARKER;

ADIPOSE DERIVED STEM CELL; ADULT; ARTICLE; ATOMIC FORCE MICROSCOPY; CELL DIFFERENTIATION; CELL SELECTION; CELL TYPE; CLONE; CORRELATION ANALYSIS; ENRICHMENT CULTURE; FEMALE; HUMAN; HUMAN TISSUE; MESENCHYMAL STEM CELL; PREDICTION; PRIORITY JOURNAL; SIMULATION; TISSUE REGENERATION; TISSUE SPECIFICITY; VISCOELASTICITY;

ADIPOSE TISSUE; CELL DIFFERENTIATION; HUMANS; MECHANOTRANSDUCTION, CELLULAR; MESENCHYMAL STEM CELLS; MICROSCOPY, ATOMIC FORCE;

EID: 84862215524     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1120349109     Document Type: Article

References (54)

1. Zuk PA, et al. (2001) Multilineage cells from human adipose tissue: implications for cell-based therapies. Tissue Eng 7:211-228. (Pubitemid 32295155)
2. Zuk PA, et al. (2002) Human adipose tissue is a source of multipotent stem cells. Mol Biol Cell 13:4279-4295. (Pubitemid 35471185)
3. Guilak F, et al. (2006) Clonal analysis of the differentiation potential of human adipose-derived adult stem cells. J Cell Physiol 206:229-237. (Pubitemid 41740736)
4. Katz AJ, Llull R, Hedrick MH, Futrell JW (1999) Emerging approaches to the tissue engineering of fat. Clin Plast Surg 26:587-603. (Pubitemid 29494161)
5. Aust L, et al. (2004) Yield of human adipose-derived adult stem cells from liposuction aspirates. Cytotherapy 6:7-14. (Pubitemid 38325114)
6. Conejero JA, et al. (2006) Repair of palatal bone defects using osteogenically differentiated fat-derived stem cells. Plast Reconstr Surg 117:857-863. (Pubitemid 44324520)
7. Cowan CM, et al. (2004) Adipose-derived adult stromal cells heal critical-size mouse calvarial defects. Nat Biotechnol 22:560-567. (Pubitemid 38585908)
8. Jeon O, et al. (2008) In vivo bone formation following transplantation of human adipose-derived stromal cells that are not differentiated osteogenically. Tissue Eng Pt A 14:1285-1294.
9. Yoshimura K, et al. (2010) Progenitor-enriched adipose tissue transplantation as rescue for breast implant complications. Breast J 16:169-175.
10. Yoshimura K, et al. (2008) Cell-assisted lipotransfer for cosmetic breast augmentation: supportive use of adipose-derived stem/stromal cells. Aesthetic Plast Surg 32:48-55 discussion 56-47.
11. Yoshimura K, et al. (2006) Characterization of freshly isolated and cultured cells derived from the fatty and fluid portions of liposuction aspirates. J Cell Physiol 208:64-76. (Pubitemid 43848990)
12. Rada T, Reis RL, Gomes ME (2011) Distinct stem cells subpopulations isolated from human adipose tissue exhibit different chondrogenic and osteogenic differentiation potential. Stem Cell Rev 7:64-76.
13. Gronthos S, et al. (2001) Surface protein characterization of human adipose tissue-derived stromal cells. J Cell Physiol 189:54-63.
14. Jones EA, et al. (2002) Isolation and characterization of bone marrow multipotential mesenchymal progenitor cells. Arthritis Rheum 46:3349-3360. (Pubitemid 35453547)
15. Zannettino AC, et al. (2008) Multipotential human adipose-derived stromal stem cells exhibit a perivascular phenotype in vitro and in vivo. J Cell Physiol 214:413-421. (Pubitemid 350308998)
16. Alt E, et al. (2011) Fibroblasts share mesenchymal phenotypes with stem cells, but lack their differentiation and colony-forming potential. Biol Cell 103:197-208.
17. Mitchell JB, et al. (2006) Immunophenotype of human adipose-derived cells: temporal changes in stromal-associated and stem cell-associated markers. Stem Cells 24:376-385. (Pubitemid 44464807)
18. Darling EM, Topel M, Zauscher S, Vail TP, Guilak F (2008) Viscoelastic properties of human mesenchymally-derived stem cells and primary osteoblasts, chondrocytes, and adipocytes. J Biomech 41:454-464.
19. Darling EM, et al. (2009) Mechanical properties and gene expression of chondrocytes on micropatterned substrates following dedifferentiation in monolayer. Cellular and Molecular Bioengineering 2:395-404.
20. Darling EM, Zauscher S, Block JA, Guilak F (2007) A thin-layer model for viscoelastic, stress-relaxation testing of cells using atomic force microscopy: do cell properties reflect metastatic potential? Biophys J 92:1784-1791. (Pubitemid 46393489)
21. Darling EM, Zauscher S, Guilak F (2006) Viscoelastic properties of zonal articular chondrocytes measured by atomic force microscopy. Osteoarthritis Cartilage 14:571-579.
22. Suresh S (2007) Biomechanics and biophysics of cancer cells. Acta biomaterialia 3:413-438.
23. Maloney JM, et al. (2010) Mesenchymal stem cell mechanics from the attached to the suspended state. Biophys J 99:2479-2487.
24. Tuan RS, Boland G, Tuli R (2003) Adult mesenchymal stem cells and cell-based tissue engineering. Arthritis Res Ther 5:32-45. (Pubitemid 36849748)
25. Yourek G, Hussain MA, Mao JJ (2007) Cytoskeletal changes of mesenchymal stem cells during differentiation. ASAIO J 53:219-228. (Pubitemid 46597573)
26. Yu H, et al. (2010) Mechanical behavior of human mesenchymal stem cells during adipogenic and osteogenic differentiation. Biochem Biophys Res Commun 393:150-155.
27. Titushkin I, Cho M (2007) Modulation of cellular mechanics during osteogenic differentiation of human mesenchymal stem cells. Biophys J 93:3693-3702. (Pubitemid 350190831)
28. Ofek G, et al. (2009) Mechanical characterization of differentiated human embryonic stem cells. J Biomech Eng 131:061011.
29. Lennon DP, Haynesworth SE, Arm DM, Baber MA, Caplan AI (2000) Dilution of human mesenchymal stem cells with dermal fibroblasts and the effects on in vitro and in vivo osteochondrogenesis. Dev Dyn 219:50-62. (Pubitemid 30667123)
30. Peptan IA, Hong L, Mao JJ (2006) Comparison of osteogenic potentials of visceral and subcutaneous adipose-derived cells of rabbits. Plast Reconstr Surg 117:1462-1470. (Pubitemid 44324447)
31. Estes BT, Wu AW, Storms RW, Guilak F (2006) Extended passaging, but not aldehyde dehydrogenase activity, increases the chondrogenic potential of human adipose-derived adult stem cells. J Cell Physiol 209:987-995. (Pubitemid 44665721)
32. Estes BT, Diekman BO, Guilak F (2008) Monolayer cell expansion conditions affect the chondrogenic potential of adipose-derived stem cells. Biotechnol Bioeng 99:986-995. (Pubitemid 351316640)
33. Sengenes C, Lolmede K, Zakaroff-Girard A, Busse R, Bouloumie A (2005) Preadipocytes in the human subcutaneous adipose tissue display distinct features from the adult mesenchymal and hematopoietic stem cells. J Cell Physiol 205:114-122. (Pubitemid 41262857)
34. Zimmerlin L, et al. (2010) Stromal vascular progenitors in adult human adipose tissue. Cytometry A 77:22-30.
35. Rada T, et al. (2012) Osteogenic differentiation of two distinct subpopulations of human adipose-derived stem cells: an in vitro and in vivo study. J Tissue Eng Regen Med 6:1-11.
36. Trickett A, Kwan YL (2003) T cell stimulation and expansion using anti-CD3/CD28 beads. J Immunol Methods 275:251-255. (Pubitemid 36351559)
37. Kuznetsova TG, Starodubtseva MN, Yegorenkov NI, Chizhik SA, Zhdanov RI (2007) Atomic force microscopy probing of cell elasticity. Micron 38:824-833. (Pubitemid 47554622)
38. Rosenbluth MJ, Lam WA, Fletcher DA (2008) Analyzing cell mechanics in hematologic diseases with microfluidic biophysical flow cytometry. Lab Chip 8:1062-1070. (Pubitemid 351904828)
39. Sraj I, et al. (2010) Cell deformation cytometry using diode-bar optical stretchers. J Biomed Opt 15:047010.
40. Sraj I, Marr DW, Eggleton CD (2010) Linear diode laser bar optical stretchers for cell deformation. Biomedical Optics Express 1:482-488.
41. Gossett DR, et al. (2010) Label-free cell separation and sorting in microfluidic systems. Anal Bioanal Chem 397:3249-3267.
42. Grover WH, et al. (2011) Measuring single-cell density. Proc Natl Acad Sci USA 108:10992-10996.
43. Hur SC, Henderson-MacLennan NK, McCabe ER, Di Carlo D (2011) Deformability-based cell classification and enrichment using inertial microfluidics. Lab Chip 11:912-920.
44. Gabriele S, Benoliel AM, Bongrand P, Theodoly O (2009) Microfluidic investigation reveals distinct roles for actin cytoskeleton and myosin II activity in capillary leukocyte trafficking. Biophys J 96:4308-4318.
45. Carlson RH, et al. (1997) Self-sorting of white blood cells in a lattice. Phys Rev Lett 79:2149-2152. (Pubitemid 127644869)
46. Lincoln B, et al. (2007) Reconfigurable microfluidic integration of a dual-beam laser trap with biomedical applications. Biomed Microdevices 9:703-710. (Pubitemid 47337893)
47. Lincoln B, et al. (2004) Deformability-based flow cytometry. Cytom Part A 59A:203-209. (Pubitemid 38736295)
48. Tan SC, et al. (2008) Viscoelastic behaviour of human mesenchymal stem cells. BMC Cell Biol 9:40.
49. Estes BT, Diekman BO, Gimble JM, Guilak F (2010) Isolation of adipose-derived stem cells and their induction to a chondrogenic phenotype. Nat Protoc 5:1294-1311.
50. Carpenter AE, et al. (2006) CellProfiler: image analysis software for identifying and quantifying cell phenotypes. Genome Biol 7:R100.
51. Gilchrist CL, Darling EM, Chen J, Setton LA (2011) Extracellular matrix ligand and stiffness modulate immature nucleus pulposus cell-cell interactions. PloS one 6:e27170.
52. Takai E, Costa KD, Shaheen A, Hung CT, Guo XE (2005) Osteoblast elastic modulus measured by atomic force microscopy is substrate dependent. Ann Biomed Eng 33:963-971. (Pubitemid 41004864)
53. Dimitriadis EK, Horkay F, Maresca J, Kachar B, Chadwick RS (2002) Determination of elastic moduli of thin layers of soft material using the atomic force microscope. Biophys J 82:2798-2810. (Pubitemid 34441316)
54. Darling EM, Guilak F (2008) A neural network model for cell classification based on single-cell biomechanical properties. Tissue Eng Pt A 14:1507-1515.