Limited Ca2+ and PKA-pathway dependent neurogenic differentiation of human adult mesenchymal stem cells as compared to fetal neuronal stem cells

Experimental Cell Research

Volumn 316, Issue 2, 2010, Pages 216-231

  Lepski, Guilherme ^a   Jannes, Cinthia Elim ^a   Maciaczyk, Jaroslaw ^b   Papazoglou, Anna ^b   Mehlhorn, Alexander T ^c   Kaiser, Stefan ^c   Teixeira, Manoel Jacobsen ^d   Marie, Suely K N ^d   Bischofberger, Josef ^b   Nikkhah, Guido ^b  

^a UNIVERSITY OF TÜBINGEN   (Germany)

^b UNIVERSITY OF FREIBURG   (Germany)

^c UNIVERSITY OF FREIBURG   (Germany)

^d UNIVERSITY OF SÃO PAULO   (Brazil)

Author keywords

Cell therapy; CNS repair; Electrophysiology; Neuronal differentiation; Stem cells

Indexed keywords

CALCIUM CHANNEL BLOCKING AGENT; CALCIUM ION; CYCLIC AMP; CYCLIC AMP DEPENDENT PROTEIN KINASE; CYCLIC AMP DEPENDENT PROTEIN KINASE INHIBITOR; CYCLIC AMP RESPONSIVE ELEMENT BINDING PROTEIN; BRAIN DERIVED NEUROTROPHIC FACTOR; CREB1 PROTEIN, HUMAN; DIFFERENTIATION ANTIGEN; ISOBUTYLMETHYLXANTHINE; PEPTIDE FRAGMENT; PROTEIN KINASE INHIBITOR; PROTEIN KINASE INHIBITOR (6 22) AMIDE; PROTEIN KINASE INHIBITOR (6-22)-AMIDE; SIGNAL PEPTIDE;

ACTION POTENTIAL; ADULT; ADULT STEM CELL; ANIMAL CELL; ARTICLE; CALCIUM CURRENT; CELL CULTURE; CELL FUNCTION; CELL MATURATION; CELL STRUCTURE; CONTROLLED STUDY; CULTURE MEDIUM; ELECTROPHYSIOLOGY; FETAL STEM CELL; FETUS; HUMAN; HUMAN CELL; HUMAN TISSUE; IMMUNOCYTOCHEMISTRY; IMMUNOHISTOCHEMISTRY; MESENCHYMAL STEM CELL; NERVE CELL DIFFERENTIATION; NEURAL STEM CELL; NONHUMAN; NORMAL HUMAN; PHENOTYPE; PLASTICITY; POTASSIUM CURRENT; PRIORITY JOURNAL; SODIUM CURRENT; SYNAPSE; BONE MARROW CELL; CALCIUM SIGNALING; CULTURE TECHNIQUE; CYTOLOGY; DRUG ANTAGONISM; DRUG EFFECT; METABOLISM; NERVE CELL; NERVOUS SYSTEM DEVELOPMENT; PHYSIOLOGY; SIGNAL TRANSDUCTION; TIME;

1-METHYL-3-ISOBUTYLXANTHINE; ACTION POTENTIALS; ADULT; ADULT STEM CELLS; ANTIGENS, DIFFERENTIATION; BONE MARROW CELLS; BRAIN-DERIVED NEUROTROPHIC FACTOR; CALCIUM CHANNEL BLOCKERS; CALCIUM SIGNALING; CELL CULTURE TECHNIQUES; CYCLIC AMP; CYCLIC AMP RESPONSE ELEMENT-BINDING PROTEIN; CYCLIC AMP-DEPENDENT PROTEIN KINASES; ELECTROPHYSIOLOGICAL PHENOMENA; FETAL STEM CELLS; HUMANS; INTERCELLULAR SIGNALING PEPTIDES AND PROTEINS; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; MESENCHYMAL STEM CELLS; NEUROGENESIS; NEURONS; PEPTIDE FRAGMENTS; PROTEIN KINASE INHIBITORS; SIGNAL TRANSDUCTION; TIME FACTORS; YOUNG ADULT;

EID: 70450242640     PISSN: 00144827     EISSN: 10902422     Source Type: Journal    
DOI: 10.1016/j.yexcr.2009.08.006     Document Type: Article

References (48)

1. Lindvall O., and Kokaia Z. Stem cells for the treatment of neurological disorders. Nature 441 (2006) 1094-1096
2. Freed C.R., Greene P.E., Breeze R.E., Tsai W.Y., DuMouchel W., Kao R., Dillon S., Winfield H., Culver S., Trojanowski J.Q., Eidelberg D., and Fahn S. Transplantation of embryonic dopamine neurons for severe Parkinson's disease. N. Engl. J. Med. 344 (2001) 710-719
3. Olanow C.W., Goetz C.G., Kordower J.H., Stoessl A.J., Sossi V., Brin M.F., Shannon K.M., Nauert G.M., Perl D.P., Godbold J., and Freeman T.B. A double-blind controlled trial of bilateral fetal nigral transplantation in Parkinson's disease. Ann. Neurol. 54 (2003) 403-414
4. Mendez I., Sanchez-Pernaute R., Cooper O., Viñuela A., Ferrari D., Björklund L., Dagher A., and Isacson O. Cell type analysis of functional fetal dopamine cell suspension transplants in the striatum and substantia nigra of patients with Parkinson's disease. Brain 128 (2005) 1498-1510
5. Dass B., Olanow C.W., and Kordower J.H. Gene transfer of trophic factors and stem cell grafting as treatments for Parkinson's disease. Neurology 66 (2006) S89-103
6. Reyes M., Lund T., Lenvik T., Aguiar D., Koodie L., and Verfaillie C.M. Purification and ex vivo expansion of postnatal human marrow mesodermal progenitor cells. Blood 98 (2001) 2615-2625
7. Mezey E., Key S., Vogelsang G., Szalayova I., Lange G.D., and Crain B. Transplanted bone marrow generates new neurons in human brains. Proc. Natl. Acad. Sci. USA 100 (2003) 1364-1369
8. Sanchez-Ramos J., Song S., Cardozo-Pelaez F., Hazzi C., Stedeford T., Willing A., Freeman T.B., Saporta S., Janssen W., Patel N., Cooper D.R., and Sanberg P.R. Adult bone marrow stromal cells differentiate into neural cells in vitro. Exp. Neurol. 164 (2000) 247-256
9. Woodbury D., Schwarz E.J., Prockop D.J., and Black I.B. Adult rat and human bone marrow stromal cells differentiate into neurons. J. Neurosci. Res. 61 (2000) 364-370
10. Black I.B., and Woodbury D. Adult rat and human bone marrow stromal stem cells differentiate into neurons. Blood Cells Mol. Dis. 27 (2001) 632-636
11. 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., Du J., Aldrich S., Lisberg A., Low W.C., Largaespada D.A., and Verfaillie C.M. Pluripotency of mesenchymal stem cells derived from adult marrow. Nature 418 (2002) 41-49
12. Kim B.J., Seo J.H., Bubien J.K., and Oh Y.S. Differentiation of adult bone marrow stem cells into neuroprogenitor cells in vitro. Neuroreport 13 (2002) 1185-1188
13. Greco S.J., Zhou C., Ye J.H., and Rameshwar P. An interdisciplinary approach and characterization of neuronal cells transdifferentiated from human mesenchymal stem cells. Stem. Cells Dev. 16 (2007) 811-826
14. Kan I., Ben-Zur T., Barhum Y., Levy Y.S., Burstein A., Charlow T., Bulvik S., Melamed E., and Offen D. Dopaminergic differentiation of human mesenchymal stem cells-utilization of bioassay for tyrosine hydroxylase expression. Neurosci. Lett. 419 (2007) 28-33
15. Khoo M.L., Shen B., Tao H., and Ma D.D.F. Long-term serial passage and neuronal differentiation capability of human bone marrow mesenchymal stem cells. Stem. Cells Dev. 17 (2008) 883-896
16. Trzaska K.A., Reddy B.Y., Munoz J.L., Li K.Y., Ye J.H., and Rameshwar P. Loss of RE-1 silencing factor in mesenchymal stem cell-derived dopamine progenitors induces functional maturity. Mol. Cell. Neurosci. 39 (2008) 285-290
17. Lu P., Blesch A., and Tuszynski M.H. Induction of bone marrow stromal cells to neurons: differentiation, transdifferentiation, or artifact?. J. Neurosci. Res. 77 (2004) 174-191
18. Neuhuber B., Gallo G., Howard L., Kostura L., Mackay A., and 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. J. Neurosci. Res. 77 (2004) 192-204
19. Jiang Y., Henderson D., Blackstad M., Chen A., Miller R.F., and Verfaillie C.M. Neuroectodermal differentiation from mouse multipotent adult progenitor cells. Proc. Natl. Acad. Sci. USA 100 (2003) 11854-11860
20. Wislet-Gendebien S., Hans G., Leprince P., Rigo J.M., Moonen G., and Rogister B. Plasticity of cultured mesenchymal stem cells: switch from nestin-positive to excitable neuron-like phenotype. Stem Cells (2005) 392-402
21. Wurmser A.E., and Gage F.H. Stem cells: cell fusion causes confusion. Nature 416 (2002) 485-487
22. Choi C.B., Cho Y.K., Prakash K.V.B., Jee B.K., Han C.W., Paik Y.K., Kim H.Y., Lee K.H., Chung N., and Rha H.K. Analysis of neuron-like differentiation of human bone marrow mesenchymal stem cells. Biochem. Biophys. Res. Commun. 350 (2006) 138-146
23. Coppi E., Pugliese A.M., Urbani S., Melani A., Cerbal E., Mazzanti B., Bosi A., Saccardi R., and Pedata F. ATP modulates cell proliferation and elicits two different electrophysiological responses in human mesenchymal stem cells. Stem. Cells 25 (2007) 1840-1849
24. Heubach J.F., Graf E.M., Leutheuser J., Bock M., Balana B., Zahanich I., Christ T., Boxberger S., Wettwer E., and Ravens U. Electrophysiological properties of human mesenchymal stem cells. J. Physiol. 554 (2004) 659-672
25. Li G.R., Deng X.L., Sun H., Chung S.S.M., Tse H.T., and Lau C.P. Ion channels in mesenchymal stem cells from rat bone marrow. Stem. Cells 24 (2006) 1519-1528
26. Wenisch S., Trinkaus K., Hild A., Hose D., Heiss C., Alt V., Klisch C., Meissl H., and Schnettler R. Immunochemical, ultrastructural and electrophysiological investigations of bone-derived stem cells in course of neuronal differentiation. Bone 38 (2006) 911-921
27. Zimmermann S., Voss M., Kaiser S., Kapp U., Waller C.F., and Martens U.M. Lack of telomerase activity in human mesenchymal stem cells. Leukemia 17 (2003) 1146-1149
28. Mehlhorn A.T., Schmal H., Kaiser S., Lepski G., Finkenzeller G., Stark G.B., and Sudkamp N.P. Mesenchymal stem cells maintain TGF-beta-mediated chondrogenic phenotype in alginate bead culture. Tissue. Eng. 12 (2006) 1393-1403
29. Svendsen C.N., Borg M.G., Armstrong R.J., Rosser A.E., Chandran S., Ostenfeld T., and Caldwell M.A. A new method for the rapid and long term growth of human neural precursor cells. J. Neurosci. Methods 85 (1998) 141-152
30. Singec I., Knoth R., Meyer R.P., Maciaczyk J., Volk B., Nikkhah G., Frotscher M., and Snyder E.Y. Defining the actual sensitivity and specificity of the neurosphere assay in stem cell biology. Nat. Methods 3 (2006) 801-806
31. Sala F. Activation kinetics of calcium currents in bull-frog sympathetic neurones. J. Physiol. 437 (1991) 221-238
32. 2+ channel activation in hippocampal mossy fiber boutons. J. Neurosci. 22 (2002) 10593-10602
33. 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., and Marshak D.R. Multilineage potential of adult human mesenchymal stem cells. Science 284 (1999) 143-147
34. Caldwell M.A., He X., Wilkie N., Pollack S., Marshall G., Wafford K.A., and Svendsen C.N. Growth factors regulate the survival and fate of cells derived from human neurospheres. Nat. Biotechnol. 19 (2001) 475-479
35. Scheffler B., Walton N.M., Lin D.D., Goetz A.K., Enikolopov G., Roper S.N., and Steindler D.A. Phenotypic and functional characterization of adult brain neuropoiesis. Proc. Natl. Acad. Sci. U.S.A. 102 (2005) 9353-9358
36. Giachino C., De Marchis S., Giampietro C., Parlato R., Perroteau I., Schütz G., Fasolo A., and Peretto P. cAMP response element-binding protein regulates differentiation and survival of newborn neurons in the olfactory bulb. J. Neurosci. 25 (2005) 10105-10118
37. Kabos P., Ehtesham M., Kabosova A., Black K.L., and Yu J.S. Generation of neural progenitor cells from whole adult bone marrow. Exp. Neurol. 178 (2002) 288-293
38. Schmidt-Hieber C., Jonas P., and Bischofberger J. Enhanced synaptic plasticity in newly generated granule cells of the adult hippocampus. Nature 429 (2004) 184-187
39. 2+ signalling in young and mature hippocampal granule cells. J. Physiol. 586 (2008) 3795-3811
40. Woodbury D., Reynolds K., and Black I.B. Adult bone marrow stromal stem cells express germline, ectodermal, endodermal, and mesodermal genes prior to neurogenesis. J. Neurosci. Res. 69 (2002) 908-917
41. Lee J., Elkahloun A.G., Messina S.A., Ferrari N., Xi D., Smith C.L., Cooper Jr. R., Albert P.S., and Fine H.A. Cellular and genetic characterization of human adult bone marrow-derived neural stem-like cells: a potential antiglioma cellular vector. Cancer Res. 63 (2003) 8877-8889
42. Hermann A., Liebau S., Gastl R., Fickert S., Habisch H.J., Fiedler J., Schwarz J., Brenner R., and Storch A. Comparative analysis of neuroectodermal differentiation capacity of human bone marrow stromal cells using various conversion protocols. J. Neurosci. Res. 83 (2006) 1502-1514
43. Krampera M., Marconi S., Pasini A., Galiè M., Rigotti G., Mosna F., Tinelli M., Lovato L., Anghileri E., Andreini A., Pizzolo G., Sbarbati A., and Bonetti B. Induction of neural-like differentiation in human mesenchymal stem cells derived from bone marrow, fat, spleen and thymus. Bone 40 (2007) 382-390
44. Mareschi K., Novara M., Rustichelli D., Ferrero I., Guido D., Carbone E., Medico E., Madon E., Vercelli A., and Fagioli F. Neural differentiation of human mesenchymal stem cells: Evidence for expression of neural markers and eag K+ channel types. Exp. Hematol. 34 (2006) 1563-1572
45. Sauerzweig S., Munsch T., Lessmann V., Reymann K.G., and Braun H. A population of serum deprivation-induced bone marrow stem cells (SD-BMSC) expresses marker typical for embryonic and neural stem cells. Exp. Cell. Res. 315 (2009) 50-66
46. Tatard V.M., D'Ippolito G., Diabira S., Valeyev A., Hackman J., McCarthy M., Bouckenooghe T., Menei P., Montero-Menei C., and Schiller P.C. Neurotrophin-directed differentiation of human adult marrow stromal cells to dopaminergic-like neurons. Bone 40 (2007) 360-373
47. Bae J.S., Han H.S., Youn D.H., Carter J.E., Modo M., Schuchman H., and Jin H.K. Networks with functional synaptic transmission after transplantation into mice with neurodegeneration. Stem. Cells 25 (2007) 1307-1316
48. Bai L., Caplan A., Lennon D., and Miller R.H. Human mesenchymal stem cells signals regulate neural stem cell fate. Neurochem. Res. 32 (2007) 353-362