Generation of highly purified neural stem cells from human adipose-derived mesenchymal stem cells by Sox1 activation

Stem Cells and Development

Volumn 23, Issue 5, 2014, Pages 515-529

  Feng, Nianhua ^a   Han, Qin ^a   Li, Jing ^a   Wang, Shihua ^a   Li, Hongling ^a   Yao, Xinglei ^a   Zhao, Robert Chunhua ^a,b  

^a PEKING UNION MEDICAL COLLEGE   (China)

^b PEKING UNION MEDICAL COLLEGE HOSPITAL   (China)

Author keywords

[No Author keywords available]

Indexed keywords

ADIPOSE TISSUE; CELL DIFFERENTIATION; CELLS, CULTURED; HUMANS; MESENCHYMAL STROMAL CELLS; NEURAL STEM CELLS; NEURODEGENERATIVE DISEASES; NEUROGENESIS; NEURONS; SOXB1 TRANSCRIPTION FACTORS; STEM CELL TRANSPLANTATION; TRANSCRIPTIONAL ACTIVATION;

EID: 84894297427     PISSN: 15473287     EISSN: 15578534     Source Type: Journal    
DOI: 10.1089/scd.2013.0263     Document Type: Article

References (58)

1. Feng Z and F Gao. (2012). Stem cell challenges in the treatment of neurodegenerative disease. CNS Neurosci Ther 18:142-148.
2. Brown RC, AH Lockwood and BR Sonawane. (2005). Neurodegenerative diseases: An overview of environmental risk factors. Environ Health Perspect 113:1250-1256.
3. Honig LS and RN Rosenberg. (2000). Apoptosis and neurologic disease. Am J Med 108:317-330.
4. Mujtaba T, DR Piper, A Kalyani, AK Groves, MT Lucero and MS Rao. (1999). Lineage-restricted neural precursors can be isolated from both the mouse neural tube and cultured ES cells. Dev Biol 214:113-127.
5. Riess P, C Zhang, KE Saatman, HL Laurer, LG Longhi, R Raghupathi, PM Lenzlinger, J Lifshitz, J Boockvar, et al. (2002). Transplanted neural stem cells survive, differentiate, and improve neurological motor function after experimental traumatic brain injury. Neurosurgery 51:1043-1052; discussion 1052-1054.
6. Wong AM, H Hodges and K Horsburgh. (2005). Neural stem cell grafts reduce the extent of neuronal damage in a mouse model of global ischaemia. Brain Res 1063:140-150.
7. Ben-Hur T, RB van Heeswijk, O Einstein, M Aharonowiz, R Xue, EE Frost, S Mori, BE Reubinoff and JW Bulte. (2007). Serial in vivo MR tracking of magnetically labeled neural spheres transplanted in chronic EAE mice. Magn Reson Med 57:164-171.
8. Einstein O, N Fainstein, I Vaknin, R Mizrachi-Kol, E Reihartz, N Grigoriadis, I Lavon, M Baniyash, H Lassmann and T Ben-Hur. (2007). Neural precursors attenuate autoimmune encephalomyelitis by peripheral immunosuppression. Ann Neurol 61:209-218.
9. Einstein O, N Grigoriadis, R Mizrachi-Kol, E Reinhartz, E Polyzoidou, I Lavon, I Milonas, D Karussis, O Abramsky and T Ben-Hur. (2006). Transplanted neural precursor cells reduce brain inflammation to attenuate chronic experimental autoimmune encephalomyelitis. Exp Neurol 198:275-284.
10. Einstein O, D Karussis, N Grigoriadis, R Mizrachi-Kol, E Reinhartz, O Abramsky and T Ben-Hur. (2003). Intraventricular transplantation of neural precursor cell spheres attenuates acute experimental allergic encephalomyelitis. Mol Cell Neurosci 24:1074-1082.
11. Ben-Hur T, O Einstein, R Mizrachi-Kol, O Ben-Menachem, E Reinhartz, D Karussis and O Abramsky. (2003). Transplanted multipotential neural precursor cells migrate into the inflamed white matter in response to experimental autoimmune encephalomyelitis. Glia 41:73-80.
12. Pluchino S, A Quattrini, E Brambilla, A Gritti, G Salani, G Dina, R Galli, CU Del, S Amadio, et al. (2003). Injection of adult neurospheres induces recovery in a chronic model of multiple sclerosis. Nature 422:688-694.
13. Pluchino S, L Zanotti, B Rossi, E Brambilla, L Ottoboni, G Salani, M Martinello, A Cattalini, A Bergami, et al. (2005). Neurosphere-derived multipotent precursors promote neuroprotection by an immunomodulatory mechanism. Nature 436:266-271.
14. Hallbergson AF, C Gnatenco and DA Peterson. (2003). Neurogenesis and brain injury: Managing a renewable resource for repair. J Clin Invest 112:1128-1133.
15. Taghipour M and A Razmkon. (2012). Isolation and growth of neural stem cells derived from adult human hippocampus. J Inj Violence Res 4.
16. Sun Y, S Pollard, L Conti, M Toselli, G Biella, G Parkin, L Willatt, A Falk, E Cattaneo and A Smith. (2008). Long-Term tripotent differentiation capacity of human neural stem (NS) cells in adherent culture. Mol Cell Neurosci 38:245-258.
17. Koch P, T Opitz, JA Steinbeck, J Ladewig and O Brustle. (2009). A rosette-Type, self-renewing human ES cell-derived neural stem cell with potential for in vitro instruction and synaptic integration. Proc Natl Acad Sci U S A 106:3225-3230.
18. Salewski RP, J Buttigieg, RA Mitchell, D van der Kooy, A Nagy and MG Fehlings. (2013). The generation of definitive neural stem cells from PiggyBac transposon-induced pluripotent stem cells can be enhanced by induction of the NOTCH signaling pathway. Stem Cells Dev 22:383-396.
19. Friedenstein AJ, RK Chailakhyan, NV Latsinik, AF Panasyuk and IV Keiliss-Borok. (1974). Stromal cells responsible for transferring the microenvironment of the hemopoietic tissues. Cloning in vitro and retransplantation in vivo. Transplantation 17:331-340.
20. Aust L, B Devlin, SJ Foster, YD Halvorsen, K Hicok, T du Laney, A Sen, GD Willingmyre and JM Gimble. (2004). Yield of human adipose-derived adult stem cells from liposuction aspirates. Cytotherapy 6:7-14.
21. Takemitsu H, D Zhao, I Yamamoto, Y Harada, M Michishita and T Arai. (2012). Comparison of bone marrow and adipose tissue-derived canine mesenchymal stem cells. BMC Vet Res 8:150.
22. Zhu X, J Du and G Liu. (2012). The comparison of multilineage differentiation of bone marrow and adipose-derived mesenchymal stem cells. Clin Lab 58:897-903.
23. Nakagami H, R Morishita, K Maeda, Y Kikuchi, T Ogihara and Y Kaneda. (2006). Adipose tissue-derived stromal cells as a novel option for regenerative cell therapy. J Atheroscler Thromb 13:77-81.
24. Ikegame Y, K Yamashita, S Hayashi, H Mizuno, M Tawada, F You, K Yamada, Y Tanaka, Y Egashira, et al. (2011). Comparison of mesenchymal stem cells from adipose tissue and bone marrow for ischemic stroke therapy. Cytotherapy 13:675-685.
25. Hsueh YY, YL Chiang, CC Wu and SC Lin. (2012). Spheroid formation and neural induction in human adipose-derived stem cells on a chitosan-coated surface. Cells Tissues Organs 196:117-128.
26. Ahmadi N, S Razavi, M Kazemi and S Oryan. (2012). Stability of neural differentiation in human adipose derived stem cells by two induction protocols. Tissue Cell 44:87-94.
27. Zhang SC. (2006). Neural subtype specification from embryonic stem cells. Brain Pathol 16:132-142.
28. Li XJ, ZW Du, ED Zarnowska, M Pankratz, LO Hansen, RA Pearce and SC Zhang. (2005). Specification of motoneurons from human embryonic stem cells. Nat Biotechnol 23:215-221.
29. Pankratz MT, XJ Li, TM Lavaute, EA Lyons, X Chen and SC Zhang. (2007). Directed neural differentiation of human embryonic stem cells via an obligated primitive anterior stage. Stem Cells 25:1511-1520.
30. Li K, Q Han, X Yan, L Liao and RC Zhao. (2010). Not a process of simple vicariousness, the differentiation of human adipose-derived mesenchymal stem cells to renal tubular epithelial cells plays an important role in acute kidney injury repairing. Stem Cells Dev 19:1267-1275.
31. Hermann A, R Gastl, S Liebau, MO Popa, J Fiedler, BO Boehm, M Maisel, H Lerche, J Schwarz, R Brenner and A Storch. (2004). Efficient generation of neural stem cell-like cells from adult human bone marrow stromal cells. J Cell Sci 117:4411-4422.
32. Jang S, HH Cho, YB Cho, JS Park and HS Jeong. (2010). Functional neural differentiation of human adipose tissuederived stem cells using bFGF and forskolin. BMC Cell Biol 11:25.
33. Chiba S, MS Kurokawa, H Yoshikawa, R Ikeda, M Takeno, M Tadokoro, H Sekino, T Hashimoto and N Suzuki. (2005). Noggin and basic FGF were implicated in forebrain fate and caudal fate, respectively, of the neural tube-like structures emerging in mouse ES cell culture. Exp Brain Res 163:86-99.
34. Liang P, S Zhao, K Kawamoto, L Jin and E Liu. (2003). Neuronal and glial differentiation following culture of the human embryonic cortical stem cells. Hum Cell 16:151-156.
35. Joo KM, BG Kang, JY Yeon, YJ Cho, JY An, HS Song, JH Won, SJ Kim, SC Hong and DH Nam. (2013). Experimental and clinical factors influencing long-Term stable in vitro expansion of multipotent neural cells from human adult temporal lobes. Exp Neurol 240:168-177.
36. Zhao J, W Sun, HM Cho, H Ouyang, W Li, Y Lin, J Do, L Zhang, S Ding, et al. (2013). Integration and long distance axonal regeneration in the central nervous system from transplanted primitive neural stem cells. J Biol Chem 288:164-168.
37. Elkabetz Y, G Panagiotakos, SG Al, ND Socci, V Tabar and L Studer. (2008). Human ES cell-derived neural rosettes reveal a functionally distinct early neural stem cell stage. Genes Dev 22:152-165.
38. Zuk PA, M Zhu, P Ashjian, DA De Ugarte, JI Huang, H Mizuno, ZC Alfonso, JK Fraser, P Benhaim and MH Hedrick. (2002). Human adipose tissue is a source of multipotent stem cells. Mol Biol Cell 13:4279-4295.
39. Ashjian PH, AS Elbarbary, B Edmonds, D DeUgarte, M Zhu, PA Zuk, HP Lorenz, P Benhaim and MH Hedrick. (2003). In vitro differentiation of human processed lipoaspirate cells into early neural progenitors. Plast Reconstr Surg 111:1922-1931.
40. Richter H, R Klee, U Heinemann and C Eder. (1997). Developmental changes of inward rectifier currents in neurons of the rat entorhinal cortex. Neurosci Lett 228:139-141.
41. Furlan F, L Guasti, D Avossa, A Becchetti, E Cilia, L Ballerini and A Arcangeli. (2005). Interneurons transiently express the ERG K+ channels during development of mouse spinal networks in vitro. Neuroscience 135:1179-1192.
42. Venere M, YG Han, R Bell, JS Song, A Alvarez-Buylla and R Blelloch. (2012). Sox1 marks an activated neural stem/ progenitor cell in the hippocampus. Development 139:3938-3949.
43. Guth SI and M Wegner. (2008). Having it both ways: Sox protein function between conservation and innovation. Cell Mol Life Sci 65:3000-3018.
44. Nitta KR, S Takahashi, Y Haramoto, M Fukuda, Y Onuma and M Asashima. (2006). Expression of Sox1 during Xenopus early embryogenesis. Biochem Biophys Res Commun 351:287-293.
45. Pevny LH, S Sockanathan, M Placzek and R Lovell-Badge. (1998). A role for SOX1 in neural determination. Development 125:1967-1978.
46. Malas S, M Postlethwaite, A Ekonomou, B Whalley, S Nishiguchi, H Wood, B Meldrum, A Constanti and V Episkopou. (2003). Sox1-deficient mice suffer from epilepsy associated with abnormal ventral forebrain development and olfactory cortex hyperexcitability. Neuroscience 119:421-432.
47. Tanaka S, Y Kamachi, A Tanouchi, H Hamada, N Jing and H Kondoh. (2004). Interplay of SOX and POU factors in regulation of the Nestin gene in neural primordial cells. Mol Cell Biol 24:8834-8846.
48. Ou Y, XD Yuan, YN Cai and YH Lu. (2011). Ultrastructure and electrophysiology of astrocytes differentiated from adult adipose-derived stromal cells. ChinMed J (Engl) 124:2656-2660.
49. Liao D, P Gong, X Li, Z Tan and Q Yuan. (2010). Co-culture with Schwann cells is an effective way for adipose-derived stem cells neural transdifferentiation. Arch Med Sci 6:145-151.
50. Wang B, J Han, Y Gao, Z Xiao, B Chen, X Wang, W Zhao and J Dai. (2007). The differentiation of rat adipose-derived stem cells into OEC-like cells on collagen scaffolds by coculturing with OECs. Neurosci Lett 421:191-196.
51. Chen J, YX Tang, YM Liu, J Chen, XQ Hu, N Liu, SX Wang, Y Zhang, WG Zeng, et al. (2012). Transplantation of adiposederived stem cells is associated with neural differentiation and functional improvement in a rat model of intracerebral hemorrhage. CNS Neurosci Ther 18:847-854.
52. Zavan B, L Michelotto, L Lancerotto, PA Della, D D'Avella, G Abatangelo, V Vindigni and R Cortivo. (2010). Neural potential of a stem cell population in the adipose and cutaneous tissues. Neurol Res 32:47-54.
53. Qian DX, HT Zhang, X Ma, XD Jiang and RX Xu. (2010). Comparison of the efficiencies of three neural induction protocols in human adipose stromal cells. Neurochem Res 35:572-579.
54. Kirkeby A, S Grealish, DA Wolf, J Nelander, J Wood, M Lundblad, O Lindvall and M Parmar. (2012). Generation of regionally specified neural progenitors and functional neurons from human embryonic stem cells under defined conditions. Cell Rep 1:703-714.
55. Chenn A and CA Walsh. (2002). Regulation of cerebral cortical size by control of cell cycle exit in neural precursors. Science 297:365-369.
56. Oelgeschlager M, H Kuroda, B Reversade and EM De Robertis. (2003). Chordin is required for the Spemann organizer transplantation phenomenon in Xenopus embryos. Dev Cell 4:219-230.
57. Gerrard L, L Rodgers and W Cui. (2005). Differentiation of human embryonic stem cells to neural lineages in adherent culture by blocking bone morphogenetic protein signaling. Stem Cells 23:1234-1241.
58. Pevny L and M Placzek. (2005). SOX genes and neural progenitor identity. Curr Opin Neurobiol 15:7-13.