Browse > Article
http://dx.doi.org/10.14348/molcells.2014.0244

Nox4-Mediated Cell Signaling Regulates Differentiation and Survival of Neural Crest Stem Cells  

Lee, Ji-Eun (Department of Life Science and GT5 Program, Ewha Womans University)
Cho, Kyu Eun (Department of Life Science and GT5 Program, Ewha Womans University)
Lee, Kyung Eun (Department of Life Science and GT5 Program, Ewha Womans University)
Kim, Jaesang (Department of Life Science and GT5 Program, Ewha Womans University)
Bae, Yun Soo (Department of Life Science and GT5 Program, Ewha Womans University)
Publication Information
Molecules and Cells / v.37, no.12, 2014 , pp. 907-911 More about this Journal
Abstract
The function of reactive oxygen species (ROS) as second messengers in cell differentiation has been demonstrated only for a limited number of cell types. Here, we used a well-established protocol for BMP2-induced neuronal differentiation of neural crest stem cells (NCSCs) to examine the function of BMP2-induced ROS during the process. We first show that BMP2 indeed induces ROS generation in NCSCs and that blocking ROS generation by pretreatment of cells with diphenyleneiodonium (DPI) as NADPH oxidase (Nox) inhibitor inhibits neuronal differentiation. Among the ROS-generating Nox isozymes, only Nox4 was expressed at a detectable level in NCSCs. Nox4 appears to be critical for survival of NCSCs at least in vitro as down-regulation by RNA interference led to apoptotic response from NCSCs. Interestingly, development of neural crest-derived peripheral neural structures in Nox4-/- mouse appears to be grossly normal, although Nox4-/- embryos were born at a sub-Mendelian ratio and showed delayed over-all development. Specifically, cranial and dorsal root ganglia, derived from NCSCs, were clearly present in Nox4-/- embryo at embryonic days (E) 9.5 and 10.5. These results suggest that Nox4-mediated ROS generation likely plays important role in fate determination and differentiation of NCSCs, but other Nox isozymes play redundant function during embryogenesis.
Keywords
bone morphogenetic protein; neural crest stem cell; neuronal differentiation; Nox4; reactive oxygen species;
Citations & Related Records
Times Cited By KSCI : 1  (Citation Analysis)
연도 인용수 순위
1 Rosc-Schluter, B.I., Hauselmann, S.P., Lorenz, V., Mochizuki, M., Facciotti, F., Pfister, O., and Kuster, G.M. (2012). NOX2-derived reactive oxygen species are crucial for CD29-induced prosurvival signalling in cardiomyocytes. Cardiovasc. Res. 93, 454-462.   DOI
2 Shah, N.M., Groves, A.K., and Anderson, D.J. (1996). Alternative neural crest cell fates are instructively promoted by TGFbeta superfamily members. Cell 85, 331-343.   DOI   ScienceOn
3 Simone, S., Cosola, C., Loverre, A., Cariello, M., Sallustio, F., Rascio, F., Gesualdo, L., Schena, F.P., Grandaliano, G., and Pertosa, G. (2012). BMP-2 induces a profibrotic phenotype in adult renal progenitor cells through Nox4 activation. Am. J. Physiol. Renal. Physiol. 303, F23-34.   DOI   ScienceOn
4 Stemple, D.L., and Anderson, D.J. (1992). Isolation of a stem cell for neurons and glia from the mammalian neural crest. Cell 71, 973-985.   DOI   ScienceOn
5 Ma, Q., Chen, Z., del Barco Barrantes, I., de la Pompa, J.L., and Anderson, D.J. (1998). neurogenin1 is essential for the determination of neuronal precursors for proximal cranial sensory ganglia. Neuron 20, 469-482.   DOI   ScienceOn
6 Madenspacher, J.H., Azzam, K.M., Gowdy, K.M., Malcolm, K.C., Nick, J.A., Dixon, D., Aloor, J.J., Draper, D.W., Guardiola, J.J., Shatz, M., et al. (2013). p53 Integrates host defense and cell fate during bacterial pneumonia. J. Exp. Med. 210, 891-904.   DOI   ScienceOn
7 Morrison, S.J., White, P.M., Zock, C., and Anderson, D.J. (1999). Prospective identification, isolation by flow cytometry, and in vivo self-renewal of multipotent mammalian neural crest stem cells. Cell 96, 737-749.   DOI   ScienceOn
8 Nadworny, A.S., Guruju, M.R., Poor, D., Doran, R.M., Sharma, R.V., Kotlikoff, M.I., and Davisson, R.L. (2013). Nox2 and Nox4 influence neonatal c-kit(+) cardiac precursor cell status and differentiation. Am. J. Physiol. Heart Circ. Physiol. 305, H829-842.   DOI   ScienceOn
9 Mandal, C.C., Ganapathy, S., Gorin, Y., Mahadev, K., Block, K., Abboud, H.E., Harris, S.E., Ghosh-Choudhury, G., and Ghosh-Choudhury, N. (2011). Reactive oxygen species derived from Nox4 mediate BMP2 gene transcription and osteoblast differentiation. Biochem. J. 433, 393-402.   DOI   ScienceOn
10 Milosevic, N., Bekhite, M.M., Sharifpanah, F., Ruhe, C., Wartenberg, M., and Sauer, H. (2010). Redox stimulation of cardiomyogenesis versus inhibition of vasculogenesis upon treatment of mouse embryonic stem cells with thalidomide. Antioxid. Redox. Signal. 13, 1813-1827.   DOI   ScienceOn
11 Paoli, P., Giannoni, E., and Chiarugi, P. (2013). Anoikis molecular pathways and its role in cancer progression. Biochim. Biophys. Acta 1833, 3481-3498.   DOI   ScienceOn
12 Perris, R., and Perissinotto, D. (2000). Role of the extracellular matrix during neural crest cell migration. Mech. Dev. 95, 3-21.   DOI   ScienceOn
13 Gao, X.P., Standiford, T.J., Rahman, A., Newstead, M., Holland, S.M., Dinauer, M.C., Liu, Q.H., and Malik, A.B. (2002). Role of NADPH oxidase in the mechanism of lung neutrophil sequestration and microvessel injury induced by Gram-negative sepsis: studies in p47phox-/- and gp91phox-/- mice. J. Immunol. 168, 3974-3982.   DOI
14 Groeger, G., Quiney, C., and Cotter, T.G. (2009). Hydrogen peroxide as a cell-survival signaling molecule. Antioxid. Redox Signal. 11, 2655-2671.   DOI
15 Kim, J., Lo, L., Dormand, E., and Anderson, D.J. (2003). SOX10 maintains multipotency and inhibits neuronal differentiation of neural crest stem cells. Neuron 38, 17-31.   DOI   ScienceOn
16 Lee, K.E., Nam, S., Cho, E.A., Seong, I., Limb, J.K., Lee, S., and Kim, J. (2008). Identification of direct regulatory targets of the transcription factor Sox10 based on function and conservation. BMC Genomics 9, 408.   DOI   ScienceOn
17 Kim, K.S., Choi, H.W., Yoon, H.E., and Kim, I.Y. (2010). Reactive oxygen species generated by NADPH oxidase 2 and 4 are required for chondrogenic differentiation. J. Biol. Chem. 285, 40294-40302.   DOI   ScienceOn
18 Le Douarin, N.M. (1980). The ontogeny of the neural crest in avian embryo chimaeras. Nature 286, 663-669.   DOI   ScienceOn
19 Lee, J.E., Hollenberg, S.M., Snider, L., Turner, D.L., Lipnick, N., and Weintraub, H. (1995). Conversion of Xenopus ectoderm into neurons by NeuroD, a basic helix-loop-helix protein. Science 268, 836-844.   DOI
20 Lee, J.H., Joo, J.H., Kim, J., Lim, H.J., Kim, S., Curtiss, L., Seong, J.K., Cui, W., Yabe-Nishimura, C., and Bae, Y.S. (2013). Interaction of NADPH oxidase 1 with Toll-like receptor 2 induces migration of smooth muscle cells. Cardiovasc. Res. 99, 483-493.   DOI   ScienceOn
21 Lo, L., Dormand, E., Greenwood, A., and Anderson, D.J. (2002). Comparison of the generic neuronal differentiation and neuron subtype specification functions of mammalian achaete-scute and atonal homologs in cultured neural progenitor cells. Development 129, 1553-1567.
22 Birren, S.J., Lo, L., and Anderson, D.J. (1993). Sympathetic neuroblasts undergo a developmental switch in trophic dependence. Development 119, 597-610.
23 Buggisch, M., Ateghang, B., Ruhe, C., Strobel, C., Lange, S., Wartenberg, M., and Sauer, H. (2007). Stimulation of ES-cell-derived cardiomyogenesis and neonatal cardiac cell proliferation by reactive oxygen species and NADPH oxidase. J. Cell Sci. 120, 885-894.   DOI   ScienceOn
24 Anderson, D.J. (1997). Cellular and molecular biology of neural crest cell lineage determination. Trends Genet. 13, 276-280.   DOI   ScienceOn
25 Bae, Y.S., Oh, H., Rhee, S.G., and Yoo, Y.D. (2011). Regulation of reactive oxygen species generation in cell signaling. Mol. Cells 32, 491-509.   DOI   ScienceOn
26 Chiarugi, P., and Giannoni, E. (2008). Anoikis: a necessary death program for anchorage-dependent cells. Biochem. Pharmacol. 76, 1352-1364.   DOI   ScienceOn
27 Matsuno, K., Yamada, H., Iwata, K., Jin, D., Katsuyama, M., Matsuki, M., Takai, S., Yamanishi, K., Miyazaki, M., Matsubara, H., et al. (2005). Nox1 is involved in angiotensin II-mediated hypertension: a study in Nox1-deficient mice. Circulation 112, 2677-2685.   DOI   ScienceOn