Gene expression-based enrichment of live cells from adipose tissue produces subpopulations with improved osteogenic potential

Stem Cell Research and Therapy

Volumn 5, Issue 5, 2014, Pages

  Marble, Hetal D ^a   Sutermaster, Bryan A ^a,b   Kanthilal, Manisha ^a,b   Fonseca, Vera C ^a   Darling, Eric M ^a,b  

^a BROWN UNIVERSITY   (United States)

^b Brown University   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

MESSENGER RNA; ALKALINE PHOSPHATASE;

ADIPOGENESIS; ADIPOSE DERIVED STEM CELL; ALPL GENE; ARTICLE; CELL DIFFERENTIATION; CELL ISOLATION; CELL LINEAGE; CELL SUBPOPULATION; CELL VIABILITY; CHONDROGENESIS; CONTROLLED STUDY; FEMALE; FLUORESCENCE ACTIVATED CELL SORTING; GENE; GENE EXPRESSION; HUMAN; HUMAN CELL; METABOLITE; MULTIPOTENT STEM CELL; OSTEOBLAST; PRIORITY JOURNAL; STROMAL VASCULAR FRACTION CELL; ADIPOSE TISSUE; BIOSYNTHESIS; BONE DEVELOPMENT; CELL SEPARATION; CYTOLOGY; ENZYMOLOGY; GENETICS; MESENCHYMAL STROMA CELL; PHYSIOLOGY; PROCEDURES;

ADIPOSE TISSUE; ALKALINE PHOSPHATASE; CELL DIFFERENTIATION; CELL SEPARATION; FEMALE; GENE EXPRESSION; HUMANS; MESENCHYMAL STROMAL CELLS; OSTEOGENESIS;

EID: 84944748301     PISSN: None     EISSN: 17576512     Source Type: Journal    
DOI: 10.1186/scrt502     Document Type: Article

References (51)

1. Valarmathi MT, Yost MJ, Goodwin RL, Potts JD: A three-dimensional tubular scaffold that modulates the osteogenic and vasculogenic differentiation of rat bone marrow stromal cells. Tissue Eng A 2008, 14:491-504.
2. Arzi B, Verstraete FJ, Huey DJ, Cissell DD, Athanasiou KA: Regenerating mandibular bone using rhBMP-2: Part 1 - immediate reconstruction of segmental mandibulectomies. Vet Surg 2014. [Epub ahead of print]
3. Diekman BO, Rowland CR, Lennon DP, Caplan AI, Guilak F: Chondrogenesis of adult stem cells from adipose tissue and bone marrow: induction by growth factors and cartilage-derived matrix. Tissue Eng A 2010, 16:523-533.
4. Turgeman G, Pittman DD, Muller R, Kurkalli BG, Zhou S, Pelled G, Peyser A, Zilberman Y, Moutsatsos IK, Gazit D: Engineered human mesenchymal stem cells: a novel platform for skeletal cell mediated gene therapy. J Gene Med 2001, 3:240-251.
5. Bruder SP, Kurth AA, Shea M, Hayes WC, Jaiswal N, Kadiyala S: Bone regeneration by implantation of purified, culture-expanded human mesenchymal stem cells. J Orthop Res 1998, 16:155-162.
6. Parrilla C, Saulnier N, Bernardini C, Patti R, Tartaglione T, Fetoni AR, Pola E, Paludetti G, Michetti F, Lattanzi W: Undifferentiated human adipose tissue-derived stromal cells induce mandibular bone healing in rats. Arch Otolaryngol Head Neck Surg 2011, 137:463-470.
7. Wang CZ, Chen SM, Chen CH, Wang CK, Wang GJ, Chang JK, Ho ML: The effect of the local delivery of alendronate on human adipose-derived stem cell-based bone regeneration. Biomaterials 2010, 31:8674-8683.
8. McIntosh KR, Lopez MJ, Borneman JN, Spencer ND, Anderson PA, Gimble JM: Immunogenicity of allogeneic adipose-derived stem cells in a rat spinal fusion model. Tissue Eng A 2009, 15:2677-2686.
9. McIntosh K, Zvonic S, Garrett S, Mitchell JB, Floyd ZE, Hammill L, Kloster A, Di Halvorsen Y, Ting JP, Storms RW, Goh B, Kilroy G, Wu X, Gimble JM: The immunogenicity of human adipose-derived cells: temporal changes in vitro. Stem Cells 2006, 24:1246-1253.
10. Estes BT, Diekman BO, Guilak F: Monolayer cell expansion conditions affect the chondrogenic potential of adipose-derived stem cells. Biotechnol Bioeng 2008, 99:986-995.
11. Zuk PA, Zhu M, Mizuno H, Huang J, Futrell JW, Katz AJ, Benhaim P, Lorenz HP, Hedrick MH: Multilineage cells from human adipose tissue: implications for cell-based therapies. Tissue Eng 2001, 7:211-228.
12. Tuan RS, Boland G, Tuli R: Adult mesenchymal stem cells and cell-based tissue engineering. Arthritis Res Ther 2003, 5:32-45.
13. Mitchell JB, McIntosh K, Zvonic S, Garretta S, Floyd ZE, Kloster A, Di Halvorsen Y, Storms RW, Goh B, Kilroy G, Wu X, Gimble JM: Immunophenotype of human adipose-derived cells: temporal changes in stromal-associated and stem cell-associated markers. Stem Cells 2006, 24:376-385.
14. Mesimaki K, Lindroos B, Tornwall J, Mauno J, Lindqvist C, Kontio R, Miettinen S, Suuronen R: Novel maxillary reconstruction with ectopic bone formation by GMP adipose stem cells. Int J Oral Maxillofac Surg 2009, 38:201-209.
15. Zimmerlin L, Donnenberg VS, Pfeifer ME, Meyer EM, Peault B, Rubin JP, Donnenberg AD: Stromal vascular progenitors in adult human adipose tissue. Cytometry A 2010, 77:22-30.
16. Lin G, Garcia M, Ning H, Banie L, Guo YL, Lue TF, Lin CS: Defining stem and progenitor cells within adipose tissue. Stem Cells Dev 2008, 17:1053-1063.
17. Bourin P, Bunnell BA, Casteilla L, Dominici M, Katz AJ, March KL, Redl H, Rubin JP, Yoshimura K, Gimble JM: Stromal cells from the adipose tissue-derived stromal vascular fraction and culture expanded adipose tissue-derived stromal/stem cells: a joint statement of the International Federation for Adipose Therapeutics and Science (IFATS) and the International Society for Cellular Therapy (ISCT). Cytotherapy 2013, 15:641-648.
18. Tyagi S, Kramer FR: Molecular beacons: probes that fluoresce upon hybridization. Nat Biotechnol 1996, 14:303-308.
19. King FW, Liszewski W, Ritner C, Bernstein HS: High-throughput tracking of pluripotent human embryonic stem cells with dual fluorescence resonance energy transfer molecular beacons. Stem Cells Dev 2011, 20:475-484.
20. Ban K, Wile B, Kim S, Park HJ, Byun J, Cho KW, Saafir T, Song MK, Yu SP, Wagner M, Bao G, Yoon YS: Purification of cardiomyocytes from differentiating pluripotent stem cells using molecular beacons that target cardiomyocyte-specific mRNA. Circulation 2013, 128:1897-1909.
21. Larsson HM, Lee ST, Roccio M, Velluto D, Lutolf MP, Frey P, Hubbell JA: Sorting live stem cells based on Sox2 mRNA expression. PLoS One 2012, 7:e49874.
22. Desai HV, Voruganti IS, Jayasuriya C, Chen Q, Darling EM: Live-cell, temporal gene expression analysis of osteogenic differentiation in adipose-derived stem cells. Tissue Eng A 2014, 20:899-907.
23. Gonzalez-Cruz RD, Fonseca VC, Darling EM: Cellular mechanical properties reflect the differentiation potential of adipose-derived mesenchymal stem cells. Proc Natl Acad Sci U S A 2012, 109:E1523-E1529.
24. Estes BT, Diekman BO, Gimble JM, Guilak F: Isolation of adipose-derived stem cells and their induction to a chondrogenic phenotype. Nat Protoc 2010, 5:1294-1311.
25. Carpenter AE, Jones TR, Lamprecht MR, Clarke C, Kang IH, Friman O, Guertin DA, Chang JH, Lindquist RA, Moffat J, Golland P, Sabatini DM: Cell Profiler: image analysis software for identifying and quantifying cell phenotypes. Genome Biol 2006, 7:R100.
26. Guilak F, Lott KE, Awad HA, Cao Q, Hicok KC, Fermor B, Gimble JM: Clonal analysis of the differentiation potential of human adipose-derived adult stem cells. J Cell Physiol 2006, 206:229-237.
27. Awad HA, Halvorsen YD, Gimble JM, Guilak F: Effects of transforming growth factor beta1 and dexamethasone on the growth and chondrogenic differentiation of adipose-derived stromal cells. Tissue Eng 2003, 9:1301-1312.
28. Enobakhare BO, Bader DL, Lee DA: Quantification of sulfated glycosaminoglycans in chondrocyte/alginate cultures, by use of 1,9-dimethylmethylene blue. Anal Biochem 1996, 243:189-191.
29. Kim EK, Lim S, Park JM, Seo JK, Kim JH, Kim KT, Ryu SH, Suh PG: Human mesenchymal stem cell differentiation to the osteogenic or adipogenic lineage is regulated by AMP-activated protein kinase. J Cell Physiol 2012, 227:1680-1687.
30. Oedayrajsingh-Varma MJ, van Ham SM, Knippenberg M, Helder MN, Klein-Nulend J, Schouten TE, Ritt MJ, van Milligen FJ: Adipose tissue-derived mesenchymal stem cell yield and growth characteristics are affected by the tissue-harvesting procedure. Cytotherapy 2006, 8:166-177.
31. Kanthilal M, Darling EM: Characterization of mechanical and regenerative properties of human, adipose stromal cells. Cell Mol Bioeng 2014. doi:10.1007/s12195-014-0350-y
32. Engler AJ, Sen S, Sweeney HL, Discher DE: Matrix elasticity directs stem cell lineage specification. Cell 2006, 126:677-689.
33. Ishikawa M, Iwamoto T, Nakamura T, Doyle A, Fukumoto S, Yamada Y: Pannexin 3 functions as an ER Ca(2+) channel, hemichannel, and gap junction to promote osteoblast differentiation. J Cell Biol 2011, 193:1257-1274.
34. Nakahama K: Cellular communications in bone homeostasis and repair. Cell Mol Life Sci 2010, 67:4001-4009.
35. Chang JC, Fujita S, Tonami H, Kato K, Iwata H, Hsu SH: Cell orientation and regulation of cell-cell communication in human mesenchymal stem cells on different patterns of electrospun fibers. Biomed Mater 2013, 8:055002.
36. Bodle JC, Teeter SD, Hluck BH, Hardin JW, Bernacki SH, Loboa EG: Age-related effects on the potency of human adipose-derived stem cells: creation and evaluation of superlots and implications for musculoskeletal tissue engineering applications. Tissue Eng Part C 2014. doi:10.1089/ten.tec.2013.0683
37. Baer PC, Kuci S, Krause M, Kuci Z, Zielen S, Geiger H, Bader P, Schubert R: Comprehensive phenotypic characterization of human adipose-derived stromal/stem cells and their subsets by a high throughput technology. Stem Cells Dev 2013, 22:330-339.
38. Varma MJ, Breuls RG, Schouten TE, Jurgens WJ, Bontkes HJ, Schuurhuis GJ, van Ham SM, van Milligen FJ: Phenotypical and functional characterization of freshly isolated adipose tissue-derived stem cells. Stem Cells Dev 2007, 16:91-104.
39. Li H, Zimmerlin L, Marra KG, Donnenberg VS, Donnenberg AD, Rubin JP: Adipogenic potential of adipose stem cell subpopulations. Plast Reconstr Surg 2011, 128:663-672.
40. Zannettino AC, Paton S, Arthur A, Khor F, Itescu S, Gimble JM, Gronthos S: Multipotential human adipose-derived stromal stem cells exhibit a perivascular phenotype in vitro and in vivo. J Cell Physiol 2008, 214:413-421.
41. Gronthos S, Zannettino AC: A method to isolate and purify human bone marrow stromal stem cells. Methods Mol Biol 2008, 449:45-57.
42. Stains JP, Civitelli R: Cell-cell interactions in regulating osteogenesis and osteoblast function. Birth Defects Res C Embryo Today 2005, 75:72-80.
43. Forriol F, Shapiro F: Bone development: interaction of molecular components and biophysical forces. Clin Orthop Relat Res 2005, 432:14-33.
44. Wang IE, Shan J, Choi R, Oh S, Kepler CK, Chen FH, Lu HH: Role of osteoblast-fibroblast interactions in the formation of the ligament-to-bone interface. J Orthop Res 2007, 25:1609-1620.
45. Qureshi AT, Chen C, Shah F, Thomas-Porch C, Gimble JM, Hayes DJ: Human adipose-derived stromal/stem cell isolation, culture, and osteogenic differentiation. Methods Enzymol 2014, 538:67-88.
46. Schellenberg A, Lin Q, Schuler H, Koch CM, Joussen S, Denecke B, Walenda G, Pallua N, Suschek CV, Zenke M, Wagner W: Replicative senescence of mesenchymal stem cells causes DNA-methylation changes which correlate with repressive histone marks. Aging 2011, 3:873-888.
47. Dao LT, Park EY, Hwang OK, Cha JY, Jun HS: Differentiation potential and profile of nuclear receptor expression during expanded culture of human adipose tissue-derived stem cells reveals PPARγ as an important regulator of Oct4 expression. Stem Cells Dev 2014, 23:24-33.
48. Ochiai-Shino H, Kato H, Sawada T, Onodera S, Saito A, Takato T, Shibahara T, Muramatsu T, Azuma T: A novel strategy for enrichment and isolation of osteoprogenitor cells from induced pluripotent stem cells based on surface marker combination. PLoS One 2014, 9:e99534.
49. Tsourkas A, Behlke MA, Bao G: Hybridization of 2′-O-methyl and 2′-deoxy molecular beacons to RNA and DNA targets. Nucleic Acids Res 2003, 31:5168-5174.
50. Santangelo PJ, Nix B, Tsourkas A, Bao G: Dual FRET molecular beacons for mRNA detection in living cells. Nucleic Acids Res 2004, 32:e57.
51. Bratu DP, Catrina IE, Marras SA: Tiny molecular beacons for in vivo mRNA detection. Methods Mol Biol 2011, 714:141-157.