Stability of neural differentiation in human adipose derived stem cells by two induction protocols

Tissue and Cell

Volumn 44, Issue 2, 2012, Pages 87-94

  Ahmadi, Nafiseh ^a,b   Razavi, Shahnaz ^a   Kazemi, Mohammad ^a   Oryan, Shahrbanoo ^b  

^a ISFAHAN UNIVERSITY OF MEDICAL SCIENCES   (Iran)

^b ISLAMIC AZAD UNIVERSITY   (Iran)

Author keywords

Adipose derived stem cells; Chemical induction; Nerve growth factor; Neurosphere; Stability; Viability

Indexed keywords

3 (4,5 DIMETHYL 2 THIAZOLYL) 2,5 DIPHENYLTETRAZOLIUM BROMIDE; GLIAL FIBRILLARY ACIDIC PROTEIN; MESSENGER RNA; MICROTUBULE ASSOCIATED PROTEIN 2; NESTIN;

ADIPOSE DERIVED STEM CELL; ADULT; ARTICLE; CELL CULTURE; CELL DEATH; CELL LINEAGE; CELL PROLIFERATION; CELL STRUCTURE; CELL VIABILITY; CHEMICAL INDUCTION PROTOCOL; COLORIMETRY; CONTROLLED STUDY; CULTURE MEDIUM; FEMALE; HUMAN; HUMAN CELL; HUMAN TISSUE; IMMUNOCYTOCHEMISTRY; INTERMETHOD COMPARISON; MOLECULAR STABILITY; NERVE CELL; NERVE CELL DIFFERENTIATION; NEUROSPHERE FORMATION PROTOCOL; PROCEDURES CONCERNING CELLS; PROTEIN EXPRESSION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION;

EID: 84857191745     PISSN: 00408166     EISSN: 15323072     Source Type: Journal    
DOI: 10.1016/j.tice.2011.11.006     Document Type: Article

References (65)

1. Anghileri E., Marconi S., Pignatelli A., Cifelli P., Galie M., Sbarbati A. Neuronal differentiation potential of human adipose-derived mesenchymal stem cells. Stem Cells Dev. 2008, 17:909-916.
2. Ashjian P.H., Elbarbary A.S., Edmonds B., DeUgarte D., Zhu M., Zuk P.A., Lorenz H.P., Benhaim P., Hedrick M.H. In vitro differentiation of human processed lipoaspirate cells into early neural progenitors. Plast. Reconstr. Surg. 2003, 111:1922-1931.
3. Bertani N., Malatesta P., Volpi G., Sonego P., Perris R. Neurogenic potential of human mesenchymal stem cells revisited: analysis by immunostaining, time-lapes video and microarray. J. Cell Sci. 2005, 118:3925-3936.
4. Blau H.M, Brazelton T.R., Weimann J.M. The evolving concept of a stem cell: entity or function?. Cell 2001, 105:829-841.
5. Caplan A.I. Mesenchymal stem cells. J. Orthop. Res. 1991, 9:641-650.
6. Cardozo A.J., Gómez D.E., Argibay P.F. Transcriptional characterization of wnt and notch signaling pathways in neuronal differentiation of human adipose tissue-derived stem cells. J. Mol. Neurosci. 2011, 44:186-194.
7. Case J., Horvath T.L., Howell J.C., Yoder M.C., March K.L., Srour E.F. Clonal multilineage differentiation of murine common pluripotent stem cells isolated from skeletal muscle and adipose stromal cells. Ann. N. Y. Acad. Sci. 2005, 1044:183-200.
8. Croft A.P., Przyborski S.A. Formation of neurons by nonneural adult stem cells: potential mechanism implicates an artifact of growth in culture. Stem Cells 2006, 24:1841-1851.
9. De Ugarte D.A., Morizono K., Elbarbary A., Alfonso Z., Zuk P.A., Zhu M., Dragoo J.L., Ashjian P., Thomas B., Benhaim P., Chen I., Fraser J., Hedrick M.H. Comparison of multi-lineage cells from human adipose tissue and bone marrow. Cell. Tiss. org. 2003, 174:101-109.
10. Ferrari G., Cusella-De Angelis G., Coletta M., Paolucci E., Stornaiuolo A., Cossu G., Mavilio F. Muscle regeneration by bone marrow-derived myogenic progenitors. Science 1998, 279:1528-1530.
11. Fujimura J., Ogawa R., Mizuno H., Fukunaga Y., Suzuki H. Neural differentiation of adipose-derived stem cells isolated from GFP transgenic mice. Biochem. Biophys. Res. Commun. 2005, 333:116-121.
12. Guilak F., Lott K.E., Awad H.A., Cao Q., Hicok K.C., Fermor B., Gimble J.M. Clonal analysis of the differentiation potential of human adipose-derived adult stem cells. J. Cell Physiol. 2006, 206:229-237.
13. Hermann A., Gastl R., Liebau S., Popa M.O., Fiedler J., Boehm B.O. Efficient generation of neural stem cell-like cells from adult human bone marrow stromal cells. J. Cell Sci. 2004, 117:4411-4422.
14. Hofstetter C.P., Schwarz E.J., Hess D., Widenfalk J., El Manira A., Prockop D.J., Olson L. Marrow stromal cells form guiding strands in the injured spinal cord and promote recovery. Proc. Natl. Acad. Sci. U.S.A. 2002, 99:2199-2204.
15. Huang T., He D., Kleiner G., Kuluz J. Neuron-like differentiation of adipose-derived stem cells from infant piglets in vitro. J. Spinal Cord Med. 2007, 30:S35-S40.
16. Hung S.C., Cheng H., Pan C.Y., Tsai M.J., Kao L.S., Ma H.L. In vitro differentiation of size-sieved stem cells into electrically active neural cells. Stem Cells 2002, 20:522-529.
17. Jang S., Cho H.H., Cho Y.B., Park J.S., Jeong H.S. Functional neural differentiation of human adipose tissue-derived stem cells using bFGF and forskolin. BMC Cell Biol. 2010, 16:11-25.
18. Jiang Y., Jahagirdar B.N., Reinhardt R.L., Schwartz R.E., Keene C.D., Ortiz-Gonzalez X.R., Reyes M., Lenvik T., Lund T., Blackstad M. Pluripotency of mesenchymal stem cells derived from adult marrow. Nature 2002, 418:41-49.
19. Jiang Y., Henderson D., Blackstad M., Chen A., Miller R.F., Verfaillie C.M. Neuroectodermal differentiation from mouse multipotent adult progenitor cells. Proc. Natl. Acad. Sci. U.S.A. 2003, 100:11854-11860.
20. Kalbermatten D.F., Schaakxs D., Kingham P.J., Wiberg M. Neurotrophic activity of human adipose stem cells isolated from deep and superficial layers of abdominal fat. Cell Tissue Res. 2011, 344:251-260.
21. Kang S.K., Lee D.H., Bae Y.C., Kim H.K., Baik S.Y., Jung J.S. Improvement of neurological de3 cits by intracerebral transplant of human adipose-derived stem cells after ischemia in rats. Exp. Neurol. 2003, 183:355-366.
22. Kang S.K., Putnam L.A., Ylostalo J., Popescu I.R., Dufour J., Belousov A. Neurogenesis of Rhesus adipose stromal cells. J. Cell Sci. 2004, 117:4289-4299.
23. Kang S.K., Shin M.J., Jung J.S., Kim Y.G., Kim C.H. Autologous adipose tissue-derived stromal cells for treatment of spinal cord injury. Stem Cells Dev. 2006, 15:583-594.
24. Katz A.J., Tholpady A., Tholpady S.S., Shang H., Ogle R.C. Cell surface and transcriptional characterization of human adipose-derived adherent stromal cells. Stem Cells 2005, 23:412-418.
25. Kern S., Eichler H., Stoeve J., Kluter H., Bieback K. Comparative analysis of mesenchymal stem cells from bone marrow, umbelical cord blood or adipose tissue. Stem Cells 2006, 24:1294-1301.
26. Kohyama J., Abe H., Shimazaki T., Koizumi A., Nakashima K., Gojo S., Taga T., Okano H., Hata J., Umezawa A. Brain from bone: efficient 'meta-differentiation' of marrow stroma-derived mature osteoblasts to neurons with Noggin or a demethylating agent. Differentiation 2001, 68:235-244.
27. Krause D.S., Theise N.D., Collector M.I., Henegariu O., Hwang S., Gardner R., Neutzel S., Sharkis S.J. Multi-organ, multilineage engraftment by a single bone marrow-derived stem cell. Cell 2001, 105:369-377.
28. Kuznetsov S.A., Friedenstein A.J., Robey P.G. Factors required for bone marrow stromal fibroblast colony formation in vitro. Br. J. Haemotol. 1997, 97:561-570.
29. Lemiscka I. Searching for stem cell regulatory molecules. Some general thoughts and possible approaches. Ann. N. Y. Acad. Sci. 1999, 872:274-288.
30. Lu P., Blesch A., Tuszynski M.H. Induction of bone marrow stromal cells to neurons: differentiation, transdifferentiation, or artifact?. J. Neurosci. Res. 2004, 77:174-191.
31. Lu P., Tuszynski M.H. Can bone marrow-derived stem cells differentiate into functional neurons?. Exp. Neurol. 2005, 193:273-278.
32. Majumdar M.K., Thiede M.A., Mosca J.D., Moorman M., Gerson S.L. Phenotypic and functional comparison of cultures of marrow-derived mesenchymal stem cells (MSCs) and stromal cells. J. Cell Physiol. 1998, 176:57-66.
33. McKay R.D. Brain stem cells change their identity. Nat. Med. 1999, 5:261-262.
34. Miller R.H., Bai L., Lennon D.P., Caplan A.I. The potential of mesenchymal stem cells for neural repair. Discov. Med. 2010, 9:236-242.
35. Neuhuber B., Gallo G., Howard L., Kostura L., Mackay A., Fischer I. Reevaluation of in vitro differentiation protocols for bone marrow stromal cells: disruption of actin cytoskeleton induces rapid morphological changes and mimics neuronal phenotype. Neurosci. Res. 2004, 77:192-204.
36. Ning H., Lin G., Lue T.F., Lin C.S. Neuron-like differentiation of adipose tissue-derived stromal cells and vascular smooth muscle cells. Differentiation 2006, 74:510-518.
37. Ono K., Yoshihara K., Suzuki H., Tanaka K.F., Takii T., Onozaki K. Preservation of hematopoietic properties in transplanted bone marrow cells in the brain. J. Neurosci. Res. 2003, 72:503-507.
38. Owens M.E., Friedenstein A.J. Cell and molecular biology of vertebrate hard tissues. Ciba Found. Symp. 1988, 136:42-60.
39. Padovan C.S., Jahn K., Birnbaum T., Reich P., Sostak P., Strupp M., Straube A. Expression of neuronal markers in differentiated marrow stromal cells and CD133+ stem-like cells. Cell Transplant. 2003, 12:839-848.
40. Pereira .R.F., Halford K.W., O'Hara M.D., Leeper D.B., Sokolov B.P., Pollard M.D., Bagasra O., Pittenger M.F., Mackay A.M., Beck S.C., Jaiswal R.K., Douglas R., Mosca J.D., Moorman M.A., Simonetti D.W., Craig S., Marshak D.R. Multilineage potential of adult human mesenchymal stem cells. Science 1999, 284:143-147.
41. Prockop D.J. Marrow stromal cells as stem cells for nonhematopoietic tissues. Science 1997, 276:71-74.
42. Prockop D.J. Further proof of the plasticity of adult stem cells and their role in tissue repair. J. Cell Biol. 2003, 160:807-809.
43. Rafii S., Lyden D. Therapeutic stem and progenitor cell transplantation for organ vascularization and regeneration. Nat. Med. 2003, 9:702-712.
44. Reynolds B.A., Weiss S. Generation of neurons and astrocytes from isolated cells of the adult mammalian central nervous system. Science 1992, 255:1707-1710.
45. Richards L.J., Kilpatrick T.J., Bartlett P.F. De novo generation of neuronal cells from the adult mouse brain. Proc. Natl. Acad. Sci. U.S.A. 1992, 89:8591-8595.
46. Safford K.M., Hicok K.C., Safford S.D., Halvorsen Y.D., Wilkison W.O., Gimble J.M., Rice H.E. Neurogenic differentiation of murine and human adiposederived stromal cells. Biochem. Biophys. Res. Commun. 2002, 294:371-379.
47. Safford K.M., Safford S.D., Gimble J.M., Shetty A.K., Rice H.E. Characterization of neuronal/glial differentiation of murine adipose-derived adult stromal cells. Exp. Neurol. 2004, 187:319-328.
48. Sanchez-Ramos J., Song S., Cardozo-Pelaez F., Hazzi C., Stedeford T., Willing A., Freeman T.B., Saporta S., Janssen W., Patel N. Adult bone marrow stromal cells differentiate into neural cells in vitro. Exp. Neurol. 2000, 164:247-256.
49. Schwartz R.E., Reyes M., Koodie L., Jiang Y., Blackstad M., Lund T., Lenvik T., Johnson S., Hu W.S., Verfaillie C.M. Multipotent adult progenitor cells from bone marrow differentiate into functional hepatocyte-like cells. J. Clin. Invest. 2002, 109:1291-1302.
50. Sterodimas A., de-Faria J., Nicaretta B., Pitanguy I. Tissue engineering with adipose-derived stem cells (ADSCs): current and future applications. J. Plast. Reconstr. Aesthet. Surg. 2010, 63:1886-1892.
51. Suon S., Jin H., Donaldson A.E., Caterson E.J., Tuan R.S., Deschennes G., Marshall C., Iacovitti L. Transient differentiation of adult human bone marrow cells into neuron-like cells in culture: development of morphological and biochemical traits is mediated by different molecular mechanisms. Stem Cells Dev. 2004, 13:625-635.
52. Taha M.F., Hedayati V. Isolation, identification and multipotential differentiation of mouse adipose tissue-derived stem cells. Tissue Cell 2010, 42:211-216.
53. Terenghi G., Wiberg M., Kingham P.J. Chapter 21: use of stem cells for improving nerve regeneration. Int. Rev. Neurobiol. 2009, 87:393-403.
54. Tholpady S.S., Aojanepong C., Llull R., Jeong J.H., Mason A.C., Futrell J.W., Ogle R.C., Katz A.J. The cellular plasticity of human adipocytes. Ann. Plast. Surg. 2005, 54:651-656.
55. Urdzakova L., Jendelova P., Glogarova K., Burian M., Hajek M., Sykova E. Transplantation of bone marrow stem cells as well as mobilization by granulocyte-colony stimulating factor promotes recovery after spinal cord injury in rats. J. Neurotrauma 2006, 23:1379-1391.
56. Verfaillie C.M. Adult stem cells: assessing the case for pluripotency. Trends Cell Biol. 2002, 12:502-508.
57. Wagers A.J., Christensen J.L., Weissman I.L. Cell fate determination from stem cells. Gene Ther. 2002, 9:606-612.
58. Wang P.P., Wang J.H., Yan Z.P., Hu M.Y., Lau G.K., Fan S.T., Luk J.M. Expression of hepatocyte-like phenotypes in bone marrow stromal cells after HGF induction. Biochem. Biophys. Res. Commun. 2004, 320:712-716.
59. Woodbury D., Schwarz E.J., Prockop D.J., Black I.B. Adult rat and human bone marrow stromal cells differentiate into neurons. J. Neurosci. Res. 2000, 61:364-370.
60. Woodbury D., Reynolds K., Black I.B. Adult bone marrow stromal stem cells express germline, ectodermal, endodermal, and mesodermal genes prior to neurogenesis. J. Neurosci. Res. 2002, 69:908-917.
61. Yaghoobi M.M., Mowla S.J., Tiraihi T. Nucleostemin, a coordinator of selfrenewal, is expressed in rat marrow stromal cells and turns off after induction of neural differentiation. Neurosci. Lett. 2005, 390:81-86.
62. Zappia E., Casazza S., Pedemonte E., Benvenuto F., Bonanni I., Gerdoni E., Giunti D., Ceravolo A., Cazzanti F., Frassoni F., Mancardi G., Uccelli A. Mesenchymal stem cells ameliorate experimental autoimmune encephalomyelitis inducing T-cell anergy. Blood 2005, 106:1755-1761.
63. Zhao L.R., Duan W.M., Reyes M., Keene C.D., Verfaillie C.M., Low W.C. Human bone marrow stem cells exhibit neural phenotypes and ameliorate neurological de3 cits after grafting into the ischemic brain of rats. Exp. Neurol. 2002, 174:1120.
64. Zuk P.A., Zhu M., Mizuno H., Huang J., Futrell J.W., Katz A.J., Benhaim P., Lorenz H.P., Hedrick M.H. Multilineage cells from human adipose tissue: implications for cell-based therapies. Tissue Eng. 2001, 7:211-228.
65. Zuk P.A., Zhu M., Ashjian P., De Ugarte D.A., Huang J.I., Mizuno H., Alfonso Z.C., Fraser J.K., Benhaim P., Hedrick M.H. Human adipose tissue is a source of multipotent stem cells. Mol. Biol. Cell 2002, 13:4279-4295.