Neurogenic transdifferentiation of human adipose-derived stem cells? A critical protocol reevaluation with special emphasis on cell proliferation and cell cycle alterations

Histochemistry and Cell Biology

Volumn 134, Issue 5, 2010, Pages 453-468

  Kompisch, Kai Michael ^a   Lange, Claudia ^a   Steinemann, Doris ^b   Skawran, Britta ^b   Schlegelberger, Brigitte ^b   Müller, Reinhard ^a   Schumacher, Udo ^a  

^a UNIVERSITY MEDICAL CENTER HAMBURG EPPENDORF   (Germany)

^b HANNOVER MEDICAL SCHOOL   (Germany)

Author keywords

Adipose derived stem cells; cAMP response element binding protein; Cell cycle arrest; Neurogenic transdifferentiation

Indexed keywords

ACTIVATING TRANSCRIPTION FACTOR; BETA TUBULIN; BRAIN DERIVED NEUROTROPHIC FACTOR; CD59 ANTIGEN; CYCLIC AMP; CYCLIC AMP RESPONSIVE ELEMENT BINDING PROTEIN; ENDOGLIN; GLIAL FIBRILLARY ACIDIC PROTEIN; INDOMETACIN; INSULIN; ISOBUTYLMETHYLXANTHINE; NESTIN; THY 1 ANTIGEN; TRANSCRIPTION FACTOR SOX4; VIMENTIN;

ADIPOSE TISSUE CELL; ARTICLE; CELL CYCLE ARREST; CELL CYCLE G2 PHASE; CELL PROLIFERATION; CELL STRUCTURE; CELL TRANSDIFFERENTIATION; CONTROLLED STUDY; EVALUATION; FEMALE; HUMAN; HUMAN CELL; NERVE CELL; PRIORITY JOURNAL; PROTEIN EXPRESSION; STEM CELL;

1-METHYL-3-ISOBUTYLXANTHINE; ACTIVATING TRANSCRIPTION FACTOR 1; ADIPOCYTES; ADULT; ANTIGENS, CD; BIOLOGICAL MARKERS; CELL CYCLE; CELL PROLIFERATION; CELL SURVIVAL; CELL TRANSDIFFERENTIATION; CYCLIC AMP; CYCLIC AMP RESPONSE ELEMENT-BINDING PROTEIN; FEMALE; GENE EXPRESSION; GENE EXPRESSION PROFILING; HUMANS; INDOMETHACIN; INSULIN; LIPECTOMY; MIDDLE AGED; NEURONS; STEM CELLS; YOUNG ADULT;

EID: 78149465233     PISSN: 09486143     EISSN: None     Source Type: Journal    
DOI: 10.1007/s00418-010-0740-8     Document Type: Article

References (51)

1. PH Ashjian AS Elbarbary B Edmonds D DeUgarte M Zhu PA Zuk, et al. 2003 In vitro differentiation of human processed lipoaspirate cells into early neural progenitors Plast Reconstr Surg 111 1922 1931 10.1097/01.PRS.0000055043.62589.05 12711954 (Pubitemid 36532347)
2. M Baptist JE Dumont PP Roger 1993 Demonstration of cell cycle kinetics in thyroid primary culture by immunostaining of proliferating cell nuclear antigen: differences in cyclic AMP- dependent and -independent mitogenic stimulations J Cell Sci 105 69 80 1:CAS:528:DyaK3sXlsFOjs74%3D 8103056
3. M Bergsland M Werme M Malewicz T Perlmann J Muhr 2006 The establishment of neuronal properties is controlled by Sox4 and Sox11 Genes Dev 20 24 3475 3486 1:CAS:528:DC%2BD2sXhs1ejtA%3D%3D 10.1101/gad.403406 17182872 (Pubitemid 44969164)
4. N Bertani P Malatesta G Volpi P Sonego R Perris 2005 Neurogenic potential of human mesenchymal stem cells revisited: analysis by immunostaining, time-lapse video and microarray J Cell Sci 118 3925 3936 1:CAS:528: DC%2BD2MXhtVOqtr%2FN 10.1242/jcs.02511 16091422 (Pubitemid 41410276)
5. AC Boquest A Shahdadfar K Frønsdal O Sigurjonsson SH Tunheim P Collas, et al. 2005 Isolation and transcription profiling of purified uncultured human stromal stem cells: alteration of gene expression after in vitro cell culture Mol Biol Cell 16 1131 1141 1:CAS:528:DC%2BD2MXit1Srtr4%3D 10.1091/mbc.E04-10-0949 15635089 (Pubitemid 40349551)
6. YM Cho YS Jang YM Jang SM Chung HS Kim JH Lee, et al. 2009 Induction of unfolded protein response during neuronal induction of rat bone marrow stromal cells and mouse embryonic stem cells Exp Mol Med 41 6 440 452 1:CAS:528:DC%2BD1MXotlaitrc%3D 10.3858/emm.2009.41.6.049 19322020
7. LP Cramer TJ Mitchison 1997 Investigation of the mechanism of retraction of the cell margin and rearward flow of nodules during mitotic cell rounding Mol Biol Cell 8 109 119 1:CAS:528:DyaK2sXptVKitw%3D%3D 9017599
8. L da Silva Meirelles PC Chagastelles NB Nardi 2006 Mesenchymal stem cells reside in virtually all post-natal organs and tissues J Cell Sci 119 2204 2213 10.1242/jcs.02932 16684817 (Pubitemid 43960310)
9. R de la Fuente JL Abad J Garcia-Castro G Fernandez-Miguel J Petriz D Rubio, et al. 2004 Dedifferentiated adult articular chondrocytes: a population of human multipotent primitive cells Exp Cell Res 297 313 328 10.1016/j.yexcr.2004.02.026 15212937 (Pubitemid 38798396)
10. H Dvory-Sobol E Cohen-Noyman D Kazanov A Figer S Birkenfeld L Madar-Shapiro, et al. 2006 Celecoxib leads to G2/M arrest by induction of p21 and downregulation of cyclin B1 expression in a p53-independent manner Eur J Cancer 42 422 426 1:CAS:528:DC%2BD28XosFKqsw%3D%3D 10.1016/j.ejca.2005.11.009 16426843 (Pubitemid 43132900)
11. J Fujimura R Ogawa H Mizuno Y Fukunaga H Suzuki 2005 Neural differentiation of adipose-derived stem cells isolated from GFP transgenic mice Biochem Biophys Res Commun 333 116 121 1:CAS:528:DC%2BD2MXlt1Sks7w%3D 10.1016/j.bbrc.2005.05.096 15939405 (Pubitemid 40813454)
12. F Guilak KE Lott HA Awad Q Cao KC Hicok B Fermor, et al. 2006 Clonal analysis of the differentiation potential of human adipose-derived adult stem cells J Cell Physiol 206 229 237 1:CAS:528:DC%2BD2MXht12gsLvJ 10.1002/jcp.20463 16021633 (Pubitemid 41740736)
13. H Hauner G Entenmann M Wabitsch D Gaillard G Ailhaud R Negrel, et al. 1989 Promoting effect of glucocorticoids on the differentiation of human adipocyte precursor cells cultured in a chemically defined medium J Clin Invest 84 1663 1670 1:CAS:528:DyaK3cXoslM%3D 10.1172/JCI114345 2681273
14. A Hermann R Gastl S Liebau MO Popa J Fiedler BO Boehm, et al. 2004 Efficient generation of neural stem cell-like cells from adult human bone marrow stromal cells J Cell Sci 117 4411 4422 1:CAS:528:DC%2BD2cXovVehtr4%3D 10.1242/jcs.01307 15304527 (Pubitemid 39360068)
15. EL Herzog L Chai DS Krause 2003 Plasticity of marrow-derived stem cells Blood 102 3483 3493 1:CAS:528:DC%2BD3sXptVymsbg%3D 10.1182/blood-2003-05-1664 12893756 (Pubitemid 37409363)
16. J Hirsch B Batchelor 1976 Adipose tissue cellularity in human obesity Clin Endocrinol Metab 5 299 311 1:STN:280:DyaE283ls1SltQ%3D%3D 10.1016/S0300-595X(76)80023-0 1085232
17. MR Hogan GP Cockram R Lu 2006 Cooperative interaction of Zhangfei and ATF4 in transactivation of the cyclic AMP response element FEBS Lett 580 58 62 1:CAS:528:DC%2BD28XkvVSl 10.1016/j.febslet.2005.11.046 16343488 (Pubitemid 43005312)
18. MD Houslay G Milligan 1997 Tailoring cAMP-signalling responses through isoform multiplicity Trends Biochem Sci 22 217 224 1:CAS:528:DyaK2sXktFait7Y%3D 10.1016/S0968-0004(97)01050-5 9204709 (Pubitemid 27246638)
19. Y Jiang BN Jahagirdar RL Reinhardt RE Schwartz CD Keene XR Ortiz-Gonzales, et al. 2002 Pluripotency of mesenchymal stem cells derived from adult marrow Nature 418 41 49 1:CAS:528:DC%2BD38XltVantrs%3D 10.1038/nature00870 12077603 (Pubitemid 34742565)
20. K Kamiya K Sakakibara EJ Ryer RP Hom EB Leof KC Kent, et al. 2007 Phosphorylation of the cyclic AMP response element binding protein mediates transforming growth factor beta-induced downregulation of cyclin A in vascular smooth muscle cells Mol Cell Biol 27 3489 3498 1:CAS:528:DC%2BD2sXltFCksbo%3D 10.1128/MCB.00665-06 17325033 (Pubitemid 46685223)
21. Y Kaneko S Sakakibara T Imai A Suzuki Y Nakamura K Sawamoto, et al. 2000 Musashi1: an evolutionally conserved marker for CNS progenitor cells including neural stem cells Dev Neurosci 22 139 153 1:CAS:528:DC%2BD3cXhvVaksr8%3D 10.1159/000017435 10657706
22. SK Kang DH Lee YC Bae HK Kim SY Baik JS Jung 2003 Improvement of neurological deficits by intracerebral transplantation of human adipose tissue-derived stromal cells after cerebral ischemia in rats Exp Neurol 183 355 366 1:CAS:528:DC%2BD3sXnvVykt7g%3D 10.1016/S0014-4886(03)00089-X 14552877 (Pubitemid 37205078)
23. SK Kang LA Putnam J Ylostalo IR Popescu J Dufour A Belousov, et al. 2004 Neurogenesis of rhesus adipose stromal cells J Cell Sci 117 4289 4299 1:CAS:528:DC%2BD2cXotlGrtL0%3D 10.1242/jcs.01264 15292397 (Pubitemid 39328315)
24. SK Kang MJ Shin JS Jung YG Kim CH Kim 2006 Autologous adipose tissue-derived stromal cells for treatment of spinal cord injury Stem Cells 15 583 594 1:CAS:528:DC%2BD28XpsFOku7k%3D 10.1089/scd.2006.15.583 (Pubitemid 44701177)
25. T Kayahara M Sawada S Takaishi H Fukui H Seno H Fukuzawa, et al. 2003 Candidate markers for stem and early progenitor cells, Musashi-1 and Hes1, are expressed in crypt base columnar cells of mouse small intestine FEBS Lett 535 131 135 1:CAS:528:DC%2BD3sXmsFSgtQ%3D%3D 10.1016/S0014-5793(02)03896-6 12560091 (Pubitemid 36126368)
26. DT Leong WM Khor FT Chew TC Lim DW Hutmacher 2006 Characterization of osteogenically induced adipose tissue-derived precursor cells in 2-dimensional and 3-dimensional environments Cells Tissues Organs 182 1 11 1:CAS:528:DC%2BD28XjvF2rsL8%3D 10.1159/000091713 16651824
27. L Liu Y Xie L Lou 2005 Cyclic AMP inhibition of proliferation of hepatocellular carcinoma cells is mediated by Akt Cancer Biol Ther 4 1240 1247 1:CAS:528:DC%2BD28XkvFGhtb4%3D 16177565
28. G López-Lluch DJ Fernández-Ayala FJ Alcaín MI Burón JM Quesada P Navas 2005 Inhibition of COX activity by NSAIDs or ascorbate increases cAMP levels and enhances differentiation in 1α, 25-dihydroxyvitamin D3-induced HL-60 cells Arch Biochem Biophys 436 32 39 10.1016/j.abb.2004.12.031 15752706 (Pubitemid 40332422)
29. P Lu A Blesch MH Tuszynski 2004 Induction of bone marrow stromal cells to neurons: differentiation, transdifferentiation, or artefact? J Neurosci Res 77 174 191 1:CAS:528:DC%2BD2cXlslemsL8%3D 10.1002/jnr.20148 15211585 (Pubitemid 38859403)
30. P Malatesta E Hartfuss M Götz 2000 Isolation of radial glial cells by fluorescent-activated cell sorting reveals neuronal lineage Development 127 5253 5263 1:CAS:528:DC%2BD3MXltFWmtw%3D%3D 11076748
31. Z Mo AR Moore R Filipovic Y Ogawa I Kazuhiro SD Antic, et al. 2007 Human cortical neurons originate from radial glia and neuron-restricted progenitors J Neurosci 15 4132 4145 10.1523/JNEUROSCI.0111-07.2007 (Pubitemid 46597153)
32. Montzka K, Lassonczyk N, Tschöke B, Neuss S, Führmann T, Franzen R et al (2009) Neural differentiation potential of human bone marrow-derived mesenchymal stromal cells: misleading marker gene expression. BMC Neurosci 10:16
33. M Moreels F Vandenabeele L Deryck I Lambrichts 2005 Radial glial cells derived from the neonatal rat spinal cord: morphological and immunocytochemical characterization Arch Histol Cytol 68 361 369 10.1679/aohc.68.361 16505582
34. T Nagase D Matsumoto M Nagase K Yoshimura T Shigeura M Inouge, et al. 2007 Neurospheres from human adipose tissue transplanted into cultured mouse embryos can contribute to craniofacial morphogenesis: a preliminary report J Craniofac Surg 18 49 53 10.1097/01.scs.0000249357.66720.d2 17251835 (Pubitemid 46168312)
35. N Nègre A Ghysen AM Martinez 2003 Mitotic G2-arrest is required for neural cell fate determination in Drosophila Mech Dev 120 253 265 10.1016/S0925-4773(02)00419-7 12559497 (Pubitemid 36143742)
36. B Neuhuber G Gallo L Howard L Kostura A Mackay I Fischer 2004 Reevaluation of in vitro differentiation protocols for bone marrow stromal cells: disruption of actin cytoskeleton induces rapid morphological changes and mimics neuronal phenotype J Neurosci Res 77 192 204 1:CAS:528: DC%2BD2cXlslemsLw%3D 10.1002/jnr.20147 15211586 (Pubitemid 38859404)
37. kip1 independently promotes neuronal differentiation and migration in the cerebral cortex Genes Dev 20 1511 1524 1:CAS:528:DC%2BD28XlsF2ktb8%3D 10.1101/gad.377106 16705040 (Pubitemid 43830657)
38. I receptor with neuronal and glial markers BMC Neurosci 5 41 10.1186/1471-2202-5-41 15511288
39. H Ning G Lin TF Lue C Lin 2006 Neuron-like differentiation of adipose tissue-derived stromal cells and vascular smooth muscle cells Differentiation 74 510 518 1:CAS:528:DC%2BD2sXmsl0%3D 10.1111/j.1432-0436.2006.00081.x 17177848 (Pubitemid 44922496)
40. H Okano H Kawahara M Toriya K Nakao S Shibata T Imai 2005 Function of RNA-binding protein Musashi-1 in stem cells Exp Cell Res 306 349 356 1:CAS:528:DC%2BD2MXltVKgsLs%3D 10.1016/j.yexcr.2005.02.021 15925591 (Pubitemid 40732760)
41. J Oswald S Boxberger B Jorgensen S Feldmann G Ehninger M Bornhauser, et al. 2004 Mesenchymal stem cells can be differentiated into endothelial cells in vitro Stem Cells 22 377 384 10.1634/stemcells.22-3-377 15153614 (Pubitemid 38736621)
42. KM Safford KC Hicok SD Safford YD Halvorsen WO Wilkison JM Gimble, et al. 2002 Neurogenic differentiation of murine and human adipose-derived stromal cells Biochem Biophys Res Commun 294 371 379 1:CAS:528:DC%2BD38XktlGrs7s%3D 10.1016/S0006-291X(02)00469-2 12051722 (Pubitemid 34694105)
43. KM Safford SD Safford JM Ginmble AK Shetty HE Rice 2004 Characterization of neural/glial differentiation of murine adipose-derived adult stromal cells Exp Neurol 187 319 328 1:CAS:528:DC%2BD2cXktV2ls78%3D 10.1016/j.expneurol.2004. 01.027 15144858 (Pubitemid 38610278)
44. F Scintu C Reali R Pillai M Badiali MA Sanna F Argiolu, et al. 2006 Differentiation of human bone marrow stem cells into cells with a neural phenotype: diverse effects of two specific treatments BMC Neurosci 7 14 10.1186/1471-2202-7-14 16483379 (Pubitemid 43379295)
45. B Skawran D Steinemann A Weigmann P Flemming T Becker J Flik, et al. 2008 Gene expression profiling in hepatocellular carcinoma: upregulation of genes in amplified chromosome regions Mod Pathol 21 5 505 516 1:CAS:528: DC%2BD1cXltVGksr8%3D 10.1038/modpathol.3800998 18277965 (Pubitemid 351589646)
46. SS Tholpady AJ Katz RC Ogle 2003 Mesenchymal stem cells from rat visceral fat exhibit multipotential differentiation in vitro Anat Rec A Discov Mol Cell Evol Biol 272 398 402 1:STN:280:DC%2BD3s7osFaktA%3D%3D 10.1002/ar.a.10039 12704697
47. AB Tonchev T Yamashima K Sawamoto H Okano 2005 Enhanced proliferation of progenitor cells in the subventricular zone and limited neuronal production in the striatum and neocortex of adult macaque monkeys after global cerebral ischemia J Neurosci Res 81 776 788 1:CAS:528:DC%2BD2MXpvFKksbY%3D 10.1002/jnr.20604 16047371 (Pubitemid 41532143)
48. Vandesompele J, De Preter K, Pattyn F, Poppe B, Van Roy N, De Paepe A, Speleman F (2002) Accurate normalization of real-time quantitative RT-PCR data by geometric averaging of multiple internal control genes. Genome Biol. 3(7):RESEARCH0034. [Epub 2002 Jun 18]
49. Zuk PA (2004) International Fat Applied Technology Society. Pittsburgh, PA, USA. Consensus Statement
50. PA Zuk M Zhu H Mizuno J Huang JW Futrell AJ Katz, et al. 2001 Multilineage cells from human adipose tissue: implications for cell-based therapies Tissue Eng 7 211 228 1:CAS:528:DC%2BD3MXjsFShtro%3D 10.1089/107632701300062859 11304456 (Pubitemid 32295155)
51. PA Zuk M Zhu P Ashjian DA De Ugarte JI Huang H Mizuno ZC Alfonso, et al. 2002 Human adipose tissue is a source of multipotent stem cells Mol Biol Cell 13 4279 4295 1:CAS:528:DC%2BD38XpsFOqsrw%3D 10.1091/mbc.E02-02-0105 12475952 (Pubitemid 35471185)