Stromal cell-secreted factors promote the survival of embryonic stem cell-derived early neural stem/progenitor cells via the activation of MAPK and PI3K-Akt pathways

Journal of Neuroscience Research

Volumn 88, Issue 4, 2010, Pages 722-734

  Ishii, Seiji ^a   Okada, Yohei ^a,b   Kadoya, Toshihiko ^c,d   Matsuzaki, Yumi ^a   Shimazaki, Takuya ^a   Okano, Hideyuki ^a  

^a KEIO UNIVERSITY   (Japan)

^b NAGOYA UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

^c KYOWA HAKKO KOGYO CO LTD   (Japan)

^d MAEBASHI INSTITUTE OF TECHNOLOGY   (Japan)

Author keywords

ES cells; Neural stem progenitor cells; Signal transduction; Stromal cells; Survival

Indexed keywords

1,4 DIAMINO 1,4 BIS(2 AMINOPHENYLTHIO) 2,3 DICYANOBUTADIENE; 2 MORPHOLINO 8 PHENYLCHROMONE; MITOGEN ACTIVATED PROTEIN KINASE; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; PHOSPHATIDYLINOSITOL 3 KINASE; RETINOIC ACID;

ANIMAL CELL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; CELL COUNT; CELL DIFFERENTIATION; CELL SURVIVAL; CONTROLLED STUDY; EMBRYONIC STEM CELL; ENZYME ACTIVATION; ENZYME PHOSPHORYLATION; IN VITRO STUDY; MOUSE; NEURAL TUBE; NONHUMAN; PRIORITY JOURNAL; STROMA CELL;

1-PHOSPHATIDYLINOSITOL 3-KINASE; ANIMALS; ANNEXIN A5; APOPTOSIS; CELL PROLIFERATION; CELL SURVIVAL; CELLS, CULTURED; CORPUS STRIATUM; CULTURE MEDIA, CONDITIONED; EMBRYO, MAMMALIAN; EMBRYONIC STEM CELLS; ENZYME INHIBITORS; FLOW CYTOMETRY; GLIAL FIBRILLARY ACIDIC PROTEIN; MICE; MITOGEN-ACTIVATED PROTEIN KINASE KINASES; O ANTIGENS; ONCOGENE PROTEIN V-AKT; SIGNAL TRANSDUCTION; STROMAL CELLS; TRETINOIN; TUBULIN;

EID: 76549088500     PISSN: 03604012     EISSN: 10974547     Source Type: Journal    
DOI: 10.1002/jnr.22250     Document Type: Article

References (49)

1. Adachi K, Mirzadeh Z, Sakaguchi M, Yamashita T, Nikolcheva T, Gotoh Y, Peltz G, Gong L, Kawase T, Alvarez-Buylla A, Okano H, Sawamoto K. 2007. Beta-catenin signaling promotes proliferation of progenitor cells in the adult mouse subventricular zone. Stem Cells 25:2827-2836.
2. Androutsellis-Theotokis A, Leker RR, Soldner F, Hoeppner DJ, Ravin R, Poser SW, Rueger MA, Bae SK, Kittappa R, McKay RD. 2006. Notch signalling regulates stem cell numbers in vitro and in vivo. Nature 442:823-826.
3. Arsenijevic Y, Weiss S, Schneider B, Aebischer P. 2001. Insulin-like growth factor-I is necessary for neural stem cell proliferation and demonstrates distinct actions of epidermal growth factor and fibroblast growth factor-2. J Neurosci 21:7194-7202.
4. Barberi T, Klivenyi P, Calingasan NY, Lee H, Kawamata H, Loonam K, Perrier AL, Bruses J, Rubio ME, Topf N, Tabar V, Harrison NL, Beal MF, Moore MA, Studer L. 2003. Neural subtype specification of fertilization and nuclear transfer embryonic stem cells and application in parkinsonian mice. Nat Biotechnol 21:1200-1207.
5. Chang MY, Park CH, Son H, Lee YS, Lee SH. 2004. Developmental stage-dependent self-regulation of embryonic cortical precursor cell survival and differentiation by leukemia inhibitory factor. Cell Death Differ 11:985-996.
6. Dazzi F, Ramasamy R, Glennie S, Jones SP, Roberts I. 2006. The role of mesenchymal stem cells in haemopoiesis. Blood Rev 20:161-171.
7. Dezawa M. 2006. Insights into autotransplantation: the unexpected discovery of specific induction systems in bone marrow stromal cells. Cell Mol Life Sci 63:2764-2772.
8. Friedenstein AJ. 1976. Precursor cells of mechanocytes. Int Rev Cytol 47:327-359.
9. Greenberg DA, Jin K. 2005. From angiogenesis to neuropathology. Nature 438:954-959.
10. Herken R, Gotz W, Wattjes KH. 1989. Initial development of capillaries in the neuroepithelium of the mouse. J Anat 164:85-92.
11. Hirabayashi Y, Itoh Y, Tabata H, Nakajima K, Akiyama T, Masuyama N, Gotoh Y. 2004. The Wnt/beta-catenin pathway directs neuronal differentiation of cortical neural precursor cells. Development 131:2791-2801.
12. Horuk R, Peiper SC. 1996. Chemokines: molecular double agents. Curr Biol 6:1581-1582.
13. Itoh K, Tezuka H, Sakoda H, Konno M, Nagata K, Uchiyama T, Uchino H, Mori KJ. 1989. Reproducible establishment of hemopoietic supportive stromal cell lines from murine bone marrow. Exp Hematol 17:145-153.
14. Jessell TM. 2000. Neuronal specification in the spinal cord: inductive signals and transcriptional codes. Nat Rev Genet 1:20-29.
15. Kawasaki H, Mizuseki K, Nishikawa S, Kaneko S, Kuwana Y, Nakanishi S, Nishikawa SI, Sasai Y. 2000. Induction of midbrain dopaminergic neurons from ES cells by stromal cell-derived inducing activity. Neuron 28:31-40.
16. Kodama HA, Amagai Y, Koyama H, Kasai S. 1982. Hormonal responsiveness of a preadipose cell line derived from newborn mouse calvaria. J Cell Physiol 112:83-88.
17. Lathia JD, Rao MS, Mattson MP, Ffrench-Constant C. 2007. The microenvironment of the embryonic neural stem cell: lessons from adult niches? Dev Dyn 236:3267-3282.
18. Lin HJ, Wang X, Shaffer KM, Sasaki CY, Ma W. 2004. Characterization of H2O2-induced acute apoptosis in cultured neural stem/progenitor cells. FEBS Lett 570:102-106.
19. Martino G, Pluchino S. 2006. The therapeutic potential of neural stem cells. Nat Rev Neurosci 7:395-406.
20. McFarland KN, Wilkes SR, Koss SE, Ravichandran KS, Mandell JW. 2006. Neural-specific inactivation of ShcA results in increased embryonic neural progenitor apoptosis and microencephaly. J Neurosci 26:7885-7897.
21. Miller FD, Gauthier AS. 2007. Timing is everything: making neurons vs. glia in the developing cortex. Neuron 54:357-369.
22. Munoz JR, Stoutenger BR, Robinson AP, Spees JL, Prockop DJ. 2005. Human stem/progenitor cells from bone marrow promote neurogenesis of endogenous neural stem cells in the hippocampus of mice. Proc Natl Acad Sci U S A 102:18171-18176.
23. Muroyama Y, Kondoh H, Takada S. 2004. Wnt proteins promote neuronal differentiation in neural stem cell culture. Biochem Biophys Res Commun 313:915-921.
24. Nagasawa T. 2006. Microenvironmental niches in the bone marrow required for B-cell development. Nat Rev Immunol 6:107-116.
25. Nagasawa T, Kikutani H, Kishimoto T. 1994. Molecular cloning and structure of a pre-B-cell growth-stimulating factor. Proc Natl Acad Sci U S A 91:2305-2309.
26. Naka H, Nakamura S, Shimazaki T, Okano H. 2008. Requirement for COUP-TFI and II in the temporal specification of neural stem cells in CNS development. Nat Neurosci 11:1014-1023.
27. Niwa H, Masui S, Chambers I, Smith AG, Miyazaki J. 2002. Phenotypic complementation establishes requirements for specific POU domain and generic transactivation function of Oct-3/4 in embryonic stem cells. Mol Cell Biol 22:1526-1536.
28. Okada Y, Shimazaki T, Sobue G, Okano H. 2004. Retinoic-acid- concentration-dependent acquisition of neural cell identity during in vitro differentiation of mouse embryonic stem cells. Dev Biol 275:124-142.
29. Okada Y, Matsumoto A, Shimazaki T, Enoki R, Koizumi A, Ishii S, Itoyama Y, Sobue G, Okano H. 2008. Spatiotemporal recapitulation of central nervous system development by murine embryonic stem cellderived neural stem/progenitor cells. Stem Cells 26:3086-3098.
30. Okano H. 2002. Stem cell biology of the central nervous system. J Neurosci Res 69:698-707.
31. Pluchino S, Zanotti L, Rossi B, Brambilla E, Ottoboni L, Salani G, Martinello M, Cattalini A, Bergami A, Furlan R, Comi G, Constantin G, Martino G. 2005. Neurosphere-derived multipotent precursors promote neuroprotection by an immunomodulatory mechanism. Nature 436:266-271.
32. Prockop DJ. 1997. Marrow stromal cells as stem cells for nonhematopoietic tissues. Science 276:71-74.
33. Rak J, Filmus J, Kerbel RS. 1996. Reciprocal paracrine interactions between tumour cells and endothelial cells: the "angiogenesis progression" hypothesis. Eur J Cancer 32:2438-2450.
34. Ramirez-Castillejo C, Sanchez-Sanchez F, Andreu-Agullo C, Ferron SR, Aroca-Aguilar JD, Sanchez P, Mira H, Escribano J, Farinas I. 2006. Pigment epithelium-derived factor is a niche signal for neural stem cell renewal. Nat Neurosci 9:331-339.
35. Reyes M, Dudek A, Jahagirdar B, Koodie L, Marker PH, Verfaillie CM. 2002. Origin of endothelial progenitors in human postnatal bone marrow. J Clin Invest 109:337-346.
36. Reynolds BA, Weiss S. 1992. Generation of neurons and astrocytes from isolated cells of the adult mammalian central nervous system. Science 255:1707-1710.
37. Sakaguchi M, Shingo T, Shimazaki T, Okano HJ, Shiwa M, Ishibashi S, Oguro H, Ninomiya M, Kadoya T, Horie H, Shibuya A, Mizusawa H, Poirier F, Nakauchi H, Sawamoto K, Okano H. 2006. A carbohydrate-binding protein, galectin-1, promotes proliferation of adult neural stem cells. Proc Natl Acad Sci U S A 103:7112-7117.
38. Sakaguchi M, Imaizumi Y, Okano H. 2007. Expression and function of galectin-1 in adult neural stem cells. Cell Mol Life Sci 64:1254-1258.
39. Shen Q, Goderie SK, Jin L, Karanth N, Sun Y, Abramova N, Vincent P, Pumiglia K, Temple S. 2004. Endothelial cells stimulate self-renewal and expand neurogenesis of neural stem cells. Science 304:1338-1340.
40. Shimazaki T, Shingo T, Weiss S. 2001. The ciliary neurotrophic factor/leukemia inhibitory factor/gp130 receptor complex operates in the maintenance of mammalian forebrain neural stem cells. J Neurosci 21:7642-7653.
41. Sinor AD, Lillien L. 2004. Akt-1 expression level regulates CNS precursors. J Neurosci 24:8531-8541.
42. Takagi Y, Takahashi J, Saiki H, Morizane A, Hayashi T, Kishi Y, Fukuda H, Okamoto Y, Koyanagi M, Ideguchi M, Hayashi H, Imazato T, Kawasaki H, Suemori H, Omachi S, Iida H, Itoh N, Nakatsuji N, Sasai Y, Hashimoto N. 2005. Dopaminergic neurons generated from monkey embryonic stem cells function in a Parkinson primate model. J Clin Invest 115:102-109.
43. Takahashi K, Tanabe K, Ohnuki M, Narita M, Ichisaka T, Tomoda K, Yamanaka S. 2007. Induction of pluripotent stem cells from adult human fibroblasts by defined factors. Cell 131:861-872.
44. Temple S. 2001. The development of neural stem cells. Nature 414:112-117.
45. van Engeland M, Nieland LJ, Ramaekers FC, Schutte B, Reutelingsperger CP. 1998. Annexin V-affinity assay: a review on an apoptosis detection system based on phosphatidylserine exposure. Cytometry 31:1-9.
46. Wada T, Haigh JJ, Ema M, Hitoshi S, Chaddah R, Rossant J, Nagy A, van der Kooy D. 2006. Vascular endothelial growth factor directly inhibits primitive neural stem cell survival but promotes definitive neural stem cell survival. J Neurosci 26:6803-6812.
47. Wieczorek G, Steinhoff C, Schulz R, Scheller M, Vingron M, Ropers HH, Nuber UA. 2003. Gene expression profile of mouse bone marrow stromal cells determined by cDNA microarray analysis. Cell Tissue Res 311:227-237.
48. Yuan J, Yankner BA. 2000. Apoptosis in the nervous system. Nature 407:802-809.
49. Zhang SC. 2003. Embryonic stem cells for neural replacement therapy: prospects and challenges. J Hematother Stem Cell Res 12:625-634.