ROS produced by NOX2 controls In Vitro development of cerebellar granule neurons development

ASN Neuro

Volumn 7, Issue 2, 2015, Pages

  Olguín Albuerne, Mauricio ^a   Morán, Julio ^a  

^a INSTITUTO DE FISIOLOGÍA CELULAR   (Mexico)

Author keywords

Axonal morphogenesis; Cerebellar granule neurons; Glutathione; NADPH oxidases; Neuronal development; Reactive oxygen species

Indexed keywords

CALCEIN; GLUTATHIONE; MICROTUBULE ASSOCIATED PROTEIN 2; REACTIVE OXYGEN METABOLITE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE 1; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE 2; TAU PROTEIN; ANTIOXIDANT; CYBB PROTEIN, MOUSE; CYBB PROTEIN, RAT; HYDROGEN PEROXIDE; MEMBRANE PROTEIN; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE;

ANIMAL CELL; ARTICLE; CELL SURVIVAL; CELL VIABILITY; CEREBELLUM GRANULAR LAYER; CONTROLLED STUDY; ENZYME ACTIVITY; FILOPODIUM; GROWTH CONE; IMMUNOCYTOCHEMISTRY; METABOLIC ACTIVITY ASSAY; NERVE CELL DIFFERENTIATION; NERVE FIBER DEGENERATION; NERVE FIBER GROWTH; NONHUMAN; PROTEIN DEPLETION; PROTEIN EXPRESSION; RAT; REAL TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; UPREGULATION; WESTERN BLOTTING; ANIMAL; CELL CULTURE; CELL DEATH; CEREBELLUM; GENETICS; GROWTH, DEVELOPMENT AND AGING; KNOCKOUT MOUSE; METABOLISM; NERVE CELL; PHYSIOLOGY; PSEUDOPODIUM; WISTAR RAT;

ANIMALS; ANTIOXIDANTS; CELL DEATH; CELL SURVIVAL; CELLS, CULTURED; CEREBELLUM; GLUTATHIONE; GROWTH CONES; HYDROGEN PEROXIDE; MEMBRANE GLYCOPROTEINS; MICE, KNOCKOUT; NADPH OXIDASE; NEURONS; PSEUDOPODIA; RATS, WISTAR; REACTIVE OXYGEN SPECIES;

EID: 85003053220     PISSN: None     EISSN: 17590914     Source Type: Journal    
DOI: 10.1177/1759091415578712     Document Type: Article

References (93)

1. Avshalumov, M. V., Chen, B. T., Koos, T., Tepper, J. M., & Rice, M. E. (2005). Endogenous hydrogen peroxide regulates the excitability of midbrain dopamine neurons via ATP-sensitive potassium channels. The Journal of Neuroscience: The Official Journal of the Society for Neuroscience,, 25 4222-4231.
2. Avshalumov, M. V., Patel, J. C., & Rice, M. E. (2008). AMPA receptor-dependent H2O2 generation in striatal medium spiny neurons but not dopamine axons: One source of a retrograde signal that can inhibit dopamine release. Journal of Neurophysiology,, 100 1590-1601.
3. Baker, K., Marcus, C. B., Huffman, K., Kruk, H., Malfroy, B., & Doctrow, S. R. (1998). Synthetic combined superoxide dismu-tase/catalase mimetics are protective as a delayed treatment in a rat stroke model: A key role for reactive oxygen species in ischemic brain injury. The Journal of Pharmacology and Experimental Therapeutics,, 284 215-221.
4. Barnes, A. P., & Polleux, F. (2009). Establishment of axon-dendrite polarity in developing neurons. Annual Review ofNeuroscience, 32, 347-381.
5. Barnham, K. J., Masters, C. L., & Bush, A. I. (2004). Neurodegenerative diseases and oxidative stress. Nature Reviews. Drug Discovery,, 3 205-214.
6. Bedard, K., & Krause, K. H. (2007). The NOX family of ROS-generating NADPH oxidases: Physiology and pathophysiology. Physiological Reviews,, 87 245-313.
7. Beiswanger, C. M., Diegmann, M. H., Novak, R. F., Philbert, M. A., Graessle, T. L., Reuhl, K. R., …Lowndes, H. E. (1995). Developmental changes in the cellular distribution of glutathi-one and glutathione S-transferases in the murine nervous system. Neurotoxicology,, 16 425-440.
8. Belousov, V. V., Fradkov, A. F., Lukyanov, K. A., Staroverov, D. B., Shakhbazov, K. S., Terskikh, A. V.,… Lukyanov, S. (2006). Genetically encoded fluorescent indicator for intracellular hydrogen peroxide. Nature Methods,, 3 281-286.
9. Borchert, A., Wang, C. C., Ufer, C., Schiebel, H., Savaskan, N. E., & Kuhn, H. (2006). The role of phospholipid hydroper-oxide glutathione peroxidase isoforms in murine embryo-genesis. The Journal of Biological Chemistry,, 281 19655-19664.
10. Brennan, A. M., Suh, S. W., Won, S. J., Narasimhan, P., Kauppinen, T. M., Lee, H.,… Swanson, R. A. (2009). NADPH oxidase is the primary source of superoxide induced by NMDA receptor activation. Nature Neuroscience,, 12 857-863.
11. Caballero-Benitez, A., Alavez, S., Uribe, R. M., & Moran, J. (2004). Regulation of glutamate-synthesizing enzymes by NMDA and potassium in cerebellar granule cells. The European Journal of Neuroscience,, 19 2030-2038.
12. Cassano, S., Agnese, S., D’Amato, V., Papale, M., Garbi, C., Castagnola, P., …Avvedimento, E. V. (2010). Reactive oxygen species, Ki-Ras, and mitochondrial superoxide dismu-tase cooperate in nerve growth factor-induced differentiation of PC12 cells. The Journal of Biological Chemistry,, 285 24141-24153.
13. Caston, J., Vasseur, F., Stelz, T., Chianale, C., Delhaye-Bouchaud, N., & Mariani, J. (1995). Differential roles of cerebellar cortex and deep cerebellar nuclei in the learning of the equilibrium behavior: Studies in intact and cerebellectomized lurcher mutant mice. Brain Research Developmental Brain Research, 86, 311-316.
14. Celotto, A. M., Liu, Z., Vandemark, A. P., & Palladino, M. J. (2012). A novel Drosophila SOD2 mutant demonstrates a role for mitochondrial ROS in neurodevelopment and disease. Brain and Behavior,, 2 424-434.
15. Coleman, M. (2005). Axon degeneration mechanisms: Commonality amid diversity. Nature Reviews Neuroscience,, 6 889-898.
16. Conforti, L., Gilley, J., & Coleman, M. P. (2014). Wallerian degen¬eration: An emerging axon death pathway linking injury and disease. Nature Reviews Neuroscience,, 15 394-409.
17. Coyoy, A., Olguin-Albuerne, M., Martinez-Briseno, P., & Moran, J. (2013). Role of reactive oxygen species and NADPH-oxidase in the development of rat cerebellum. Neurochemistry International,, 62 998-1011.
18. Chen, K., Craige, S. E., & Keaney, J. F. Jr. (2009). Downstream targets and intracellular compartmentalization in Nox signaling. Antioxidants & Redox Signaling,, 11 2467-2480.
19. Cheret, C., Gervais, A., Lelli, A., Colin, C., Amar, L., Ravassard, P., … Mallat, M. (2008). Neurotoxic activation of microglia is promoted by a Nox1-dependent NADPH oxidase. Journal of Neuroscience,, 28 12039-12051.
20. de la Torre-Ubieta, L., Gaudilliere, B., Yang, Y., Ikeuchi, Y., Yamada, T., DiBacco, S.,… Bonni, A. (2010). A FOXO-Pak1 transcriptional pathway controls neuronal polarity. Genes & Development,, 24 799-813.
21. Dehmelt, L., & Halpain, S. (2004). Actin and microtubules in neur-ite initiation: Are MAPs the missing link? Journal of Neurobiology,, 58 18-33.
22. Diatchuk, V., Lotan, O., Koshkin, V., Wikstroem, P., & Pick, E. (1997). Inhibition of NADPH oxidase activation by 4-(2-ami-noethyl)-benzenesulfonyl fluoride and related compounds. The Journal ofBiological Chemistry,, 272 13292-13301.
23. Dickinson, B. C., Peltier, J., Stone, D., Schaffer, D. V., & Chang, C. J. (2011). Nox2 redox signaling maintains essential cell popula¬tions in the brain. Nature chemical biology,, 7 106-112.
24. Dringen, R. (2000). Metabolism and functions of glutathione in brain. Progress in Neurobiology,, 62 649-671.
25. Droge, W. (2002). Free radicals in the physiological control of cell function. Physiological Reviews,, 82 47-95.
26. Dvoriantchikova, G., Grant, J., Santos, A. R. C., Hernandez, E., & Ivanov, D. (2012). Neuronal NAD(P)H oxidases contribute to ROS production and mediate RGC death after ischemia. Investigative Ophthalmology & Visual Science,, 53 2823-2830.
27. Franco, R., & Cidlowski, J. A. (2009). Apoptosis and glutathione: Beyond an antioxidant. Cell Death and Differentiation,, 16 1303-1314.
28. Franco, R., & Cidlowski, J. A. (2012). Glutathione efflux and cell death. Antioxidants & Redox Signaling,, 17 1694-1713.
29. Gallo, V., Kingsbury, A., Balazs, R., & Jorgensen, O. S. (1987). The role of depolarization in the survival and differentiation of cerebellar granule cells in culture. The Journal ofNeuroscience: The Official Journal of the Society for Neuroscience,, 7 2203-2213.
30. Goldsmit, Y., Erlich, S., & Pinkas-Kramarski, R. (2001). Neuregulin induces sustained reactive oxygen species gener¬ation to mediate neuronal differentiation. Cellular and Molecular Neurobiology,, 21 753-769.
31. Gough, D. R., & Cotter, T. G. (2011). Hydrogen peroxide: A Jekyll and Hyde signalling molecule. Cell Death & Disease,, 2 e213.
32. Grek, C. L., Zhang, J., Manevich, Y., Townsend, D. M., & Tew, K. D. (2013). Causes and consequences of cysteine S-glutathiony-lation. The Journal ofBiological Chemistry,, 288 26497-26504.
33. Halliwell, B. (2009). The wanderings of a free radical. Free Radical Biology & Medicine,, 46 531-542.
34. Hernandez-Enriquez, B., Guemez-Gamboa, A., & Moran, J. (2011). Reactive oxygen species are related to ionic fluxes and volume decrease in apoptotic cerebellar granule neurons: Role of NOX enzymes. Journal ofNeurochemistry,, 117 654-664.
35. Ito, S., & Takeichi, M. (2009). Dendrites of cerebellar granule cells correctly recognize their target axons for synaptogenesis in vitro. Proceedings ofthe National Academy ofSciences ofthe United States of America,, 106 12782-12787.
36. Jaquet, V., Scapozza, L., Clark, R. A., Krause, K. H., & Lambeth, J. D. (2009). Small-molecule NOX inhibitors: ROS-generating NADPH oxidases as therapeutic targets. Antioxidants & Redox Signaling,, 11 2535-2552.
37. Jones, D. P. (2006). Redefining oxidative stress. Antioxidants & Redox Signaling,, 8 1865-1879.
38. Kaludercic, N., Deshwal, S., & Di Lisa, F. (2014). Reactive oxygen species and redox compartmentalization. Frontiers in Physiology,, 5 285.
39. Kamata, H., & Hirata, H. (1999). Redox regulation of cellular signalling. Cellular Signalling,, 11 1-14.
40. Kamata, H., Oka, S., Shibukawa, Y., Kakuta, J., & Hirata, H. (2005). Redox regulation of nerve growth factor-induced neur-onal differentiation of PC12 cells through modulation of the nerve growth factor receptor, TrkA. Archives ofBiochemistry and Biophysics,, 434 16-25.
41. Kaplan, D. R., & Miller, F. D. (2000). Neurotrophin signal trans-duction in the nervous system. Current Opinion in Neurobiology,, 10 381-391.
42. Kennedy, K. A., Ostrakhovitch, E. A., Sandiford, S. D., Dayarathna, T., Xie, X., Waese, E. Y., …Li, S. S. (2010). Mammalian numb-interacting protein 1/dual oxidase maturation factor 1 directs neuronal fate in stem cells. The Journal of Biological Chemistry,, 285 17974-17985.
43. Kim, S. H., Won, S. J, Sohn, S., Kwon, H. J., Lee, J. Y., Park, J. H., … Gwag, B. J. (2002). Brain-derived neurotrophic factor can act as a pronecrotic factor through transcriptional and trans-lational activation of NADPH oxidase. The Journal of Cell Biology,, 159 821-831.
44. Kishida, K. T., Hoeffer, C. A., Hu, D., Pao, M., Holland, S. M., & Klann, E. (2006). Synaptic plasticity deficits and mild memory impairments in mouse models of chronic granulomatous dis¬ease. Molecular and Cellular Biology,, 26 5908-5920.
45. Komuro, H., & Yacubova, E. (2003). Recent advances in cerebellar granule cell migration. Cellular and Molecular Life Sciences: CMLS,, 60 1084-1098.
46. Konishi, Y., Stegmuller, J., Matsuda, T., Bonni, S., & Bonni, A. (2004). Cdh1-APC controls axonal growth and patterning in the mammalian brain. Science,, 303 1026-1030.
47. Le Belle, J. E., Orozco, N. M., Paucar, A. A., Saxe, J. P., Mottahedeh, J., Pyle, A. D., …Kornblum, H. I. (2011). Proliferative neural stem cells have high endogenous ROS levels that regulate self-renewal and neurogenesis in a PI3K/ Akt-dependant manner. Cell Stem Cell,, 8 59-71.
48. Lee, B. C., Peterfi, Z., Hoffmann, F. W., Moore, R. E., Kaya, A., Avanesov, A.,… Gladyshev, V. N. (2013). MsrB1 and MICALs regulate actin assembly and macrophage function via reversible stereoselective methionine oxidation. Molecular Cell,, 51 397-404.
49. Lu,Q., Wainwright, M.S., Harris,V.A., Aggarwal, S.,Hou,Y.L.,Rau, T.,… Black, S. M. (2012). Increased NADPH oxidase-derived superoxide is involved in the neuronal cell death induced by hypoxia-ischemia in neonatal hippocampal slice cultures. Free Radical Biology and Medicine,, 53 1139-1151.
50. Lubos, E., Loscalzo, J., & Handy, D. E. (2011). Glutathione per-oxidase-1 in health and disease: From molecular mechanisms to therapeutic opportunities. Antioxidants & Redox Signaling,, 15 1957-1997.
51. Miller, E. W., Tulyathan, O., Isacoff, E. Y., & Chang, C. J. (2007). Molecular imaging of hydrogen peroxide produced for cell sig¬naling. Nature Chemical Biology,, 3 263-267.
52. Mishina, N. M., Tyurin-Kuzmin, P. A., Markvicheva, K. N., Vorotnikov, A. V., Tkachuk, V. A., Laketa, V., … Belousov, V. V. (2011). Does cellular hydrogen peroxide diffuse or act locally? Antioxidants & Redox Signaling,, 14 1-7.
53. Moran, J., & Patel, A. J. (1989). Effect of potassium depolarization on phosphate-activated glutaminase activity in primary cultures of cerebellar granule neurons and astroglial cells during devel¬opment. Brain Research Developmental Brain Research,, 46 97-105.
54. Morinaka, A., Yamada, M., Itofusa, R., Funato, Y., Yoshimura, Y., Nakamura, F.,… Miki, H. (2011). Thioredoxin mediates oxida¬tion-dependent phosphorylation of CRMP2 and growth cone collapse. Science Signaling,, 4 ra26.
55. Munnamalai, V., & Suter, D. M. (2009). Reactive oxygen species regulate F-actin dynamics in neuronal growth cones and neurite outgrowth. Journal ofNeurochemistry,, 108 644-661.
56. Munnamalai, V., Weaver, C. J., Weisheit, C. E., Venkatraman, P., Agim, Z. S., Quinn, M. T.,… Suter, D. M. (2014). Bidirectional interactions between NOX2-type NADPH oxidase and the F-actin cytoskeleton in neuronal growth cones. Journal of Neurochemistry,, 130 526-540.
57. Nanda, D., Tolputt, J., & Collard, K. J. (1996). Changes in brain glutathione levels during postnatal development in the rat. Brain Research Developmental Brain Research,, 94 238-241.
58. Nitti, M., Furfaro, A. L., Cevasco, C., Traverso, N., Marinari, U. M., Pronzato, M. A.,… Domenicotti, C. (2010). PKC delta and NADPH oxidase in retinoic acid-induced neuroblastoma cell differentiation. Cellular Signalling,, 22 828-835.
59. Parnham, M. J., & Kindt, S. (1984). A novel biologically active seleno-organic compound-III. Effects of PZ 51 (Ebselen) on glutathione peroxidase and secretory activities of mouse macro-phages. Biochemical Pharmacology,, 33 3247-3250.
60. Patapoutian, A., & Reichardt, L. F. (2001). Trk receptors: Mediators of neurotrophin action. Current Opinion in Neurobiology,, 11 272-280.
61. Pendyala, S., Gorshkova, I. A., Usatyuk, P. V., He, D., Pennathur, A., Lambeth, J. D., … Natarajan, V. (2009). Role of Nox4 and Nox2 in hyperoxia-induced reactive oxygen species generation and migration of human lung endothelial cells. Antioxidants & Redox Signaling,, 11 747-764.
62. Pourova, J., Kottova, M., Voprsalova, M., & Pour, M. (2010). Reactive oxygen and nitrogen species in normal physiological processes. Acta Physiologica (Oxf),, 198 15-35.
63. Powell, S. K., Rivas, R. J., Rodriguez-Boulan, E., & Hatten, M. E. (1997). Development of polarity in cerebellar granule neurons. Journal ofNeurobiology,, 32 223-236.
64. Rahman, I., Kode, A., & Biswas, S. K. (2006). Assay for quanti¬tative determination of glutathione and glutathione disulfide levels using enzymatic recycling method. Nature Protocols,, 1 3159-3165.
65. Ramiro-Cortes, Y., Guemez-Gamboa, A., & Moran, J. (2011). Reactive oxygen species participate in the p38-mediated apop-tosis induced by potassium deprivation and staurosporine in cerebellar granule neurons. The International Journal of Biochemistry & Cell Biology,, 43 1373-1382.
66. Ramiro-Cortes, Y., & Moran, J. (2009). Role of oxidative stress and JNK pathway in apoptotic death induced by potassium depriv¬ation and staurosporine in cerebellar granule neurons. Neurochemistry International,, 55 581-592.
67. Ramos, B., Gaudilliere, B., Bonni, A., & Gill, G. (2007). Transcription factor Sp4 regulates dendritic patterning during cerebellar maturation. Proceedings ofthe National Academy ofSciences ofthe United States ofAmerica,, 104 9882-9887.
68. Rice, M. E., & Russo-Menna, I. (1998). Differential compartmen-talization of brain ascorbate and glutathione between neurons and glia. Neuroscience,, 82 1213-1223.
69. Ryter, S. W., Kim, H. P., Hoetzel, A., Park, J. W., Nakahira, K., Wang, X.,… Choi, A. M. (2007). Mechanisms of cell death in oxidative stress. Antioxidants & Redox Signaling,, 9 49-89.
70. Sakai, J., Li, J., Subramanian, K. K., Mondal, S., Bajrami, B., Hattori, H.,… Luo, H. R. (2012). Reactive oxygen species-induced actin glutathionylation controls actin dynamics in neu-trophils. Immunity,, 37 1037-1049.
71. Savaskan, N. E., Borchert, A., Brauer, A. U., & Kuhn, H. (2007). Role for glutathione peroxidase-4 in brain development and neuronal apoptosis: Specific induction of enzyme expression in reactive astrocytes following brain injury. Free Radical Biology & Medicine,, 43 191-201.
72. Schafer, F. Q., & Buettner, G. R. (2001). Redox environment of the cell as viewed through the redox state of the glutathione disul-fide/glutathione couple. Free Radical Biology & Medicine,, 30 1191-1212.
73. Schulz, J. B., Weller, M., & Klockgether, T. (1996). Potassium deprivation-induced apoptosis of cerebellar granule neurons: A sequential requirement for new mRNA and protein synthesis, ICE-like protease activity, and reactive oxygen species. The Journal ofNeuroscience: The Official Journal ofthe Society for Neuroscience,, 16 4696-4706.
74. Sedeek, M., Callera, G., Montezano, A., Gutsol, A., Heitz, F., Szyndralewiez, C., …Hebert, R. L. (2010). Critical role of Nox4-based NADPH oxidase in glucose-induced oxidative stress in the kidney: Implications in type 2 diabetic nephropathy. American Journal of Physiology Renal Physiology,, 299 F1348-F1358.
75. Shalizi, A., Gaudilliere, B., Yuan, Z., Stegmuller, J., Shirogane, T., Ge, Q., …Bonni, A. (2006). A calcium-regulated MEF2 sumoylation switch controls postsynaptic differentiation. Science,, 311 1012-1017.
76. Shi, Z. Z., Osei-Frimpong, J., Kala, G., Kala, S. V., Barrios, R. J., Habib, G. M.,… Lieberman, M. W. (2000). Glutathione synthe¬sis is essential for mouse development but not for cell growth in culture. Proceedings ofthe National Academy ofSciences ofthe United States ofAmerica,, 97 5101-5106.
77. Sidlo, Z., Reggio, P. H., & Rice, M. E. (2008). Inhibition of striatal dopamine release by CB1 receptor activation requires nonsy-naptic communication involving GABA, H2O2, and KATP channels. Neurochemistry International,, 52 80-88.
78. Solecki, D. J., Govek, E. E., Tomoda, T., & Hatten, M. E. (2006). Neuronal polarity in CNS development. Genes & Development, 20, 2639-2647.
79. Sorce, S., & Krause, K. H. (2009). NOX enzymes in the central nervous system: From signaling to disease. Antioxidants & Redox Signaling,, 11 2481-2504.
80. Suzukawa, K., Miura, K., Mitsushita, J., Resau, J., Hirose, K., Crystal, R., …Kamata, T. (2000). Nerve growth factor-induced neuronal differentiation requires generation of Rac1-regulated reactive oxygen species. The Journal ofBiological Chemistry, 275, 13175-13178.
81. Taglialatela, G., Perez-Polo, J. R., & Rassin, D. K. (1998). Induction of apoptosis in the CNS during development by the combination of hyperoxia and inhibition of glutathione synthe¬sis. Free Radical Biology & Medicine,, 25 936-942.
82. Thiels, E., Urban, N. N., Gonzalez-Burgos, G. R., Kanterewicz, B. I., Barrionuevo, G., Chu, C. T., …Klann, E. (2000). Impairment of long-term potentiation and associative memory in mice that overexpress extracellular superoxide dismutase. The Journal of Neuroscience: The Official Journal of the Society for Neuroscience,, 20 7631-7639.
83. Tietze, F. (1969). Enzymic method for quantitative determination of nanogram amounts of total and oxidized glutathione: Applications to mammalian blood and other tissues. Analytical Biochemistry,, 27 502-522.
84. Tsatmali, M., Walcott, E. C., & Crossin, K. L. (2005). Newborn neurons acquire high levels of reactive oxygen species and increased mitochondrial proteins upon differentiation from pro¬genitors. Brain Research,, 1040 137-150.
85. Tsatmali, M., Walcott, E. C., Makarenkova, H., & Crossin, K. L. (2006). Reactive oxygen species modulate the differentiation of neurons in clonal cortical cultures. Molecular and Cellular Neurosciences,, 33 345-357.
86. Ushio-Fukai, M. (2009). Compartmentalization of redox signaling through NADPH oxidase-derived ROS. Antioxidants & Redox Signaling,, 11 1289-1299.
87. Valencia, A., & Moran, J. (2004). Reactive oxygen species induce different cell death mechanisms in cultured neurons. Free Radical Biology & Medicine,, 36 1112-1125.
88. Valko, M., Leibfritz, D., Moncol, J., Cronin, M. T., Mazur, M., & Telser, J. (2007). Free radicals and antioxidants in normal physiological functions and human disease. The International Journal ofBiochemistry & Cell Biology,, 39 44-84.
89. Wang, N., Xie, K., Huo, S., Zhao, J., Zhang, S., & Miao, J. (2007). Suppressing phosphatidylcholine-specific phospholipase C and elevating ROS level, NADPH oxidase activity and Rb level induced neuronal differentiation in mesenchymal stem cells. Journal ofCellular Biochemistry,, 100 1548-1557.
90. Wechsler-Reya, R. J., & Scott, M. P. (1999). Control of neuronal precursor proliferation in the cerebellum by Sonic Hedgehog. Neuron,, 22 103-114.
91. Wallace, P. K., Tario, J. D. Jr., Fisher, J. L., Wallace, S. S., Ernstoff, M. S., & Muirhead, K. A. (2008). Tracking antigen-driven responses by flow cytometry: monitoring proliferation by dye dilution. Cytometry Part A: the journal ofthe International Society for Analytical Cytology,, 73 1019-1034.
92. Yant, L. J., Ran, Q., Rao, L., Van Remmen, H., Shibatani, T., Belter, J. G., …Prolla, T. A. (2003). The selenoprotein GPX4 is essential for mouse development and protects from radiation and oxidative damage insults. Free Radical Biology & Medicine,, 34 496-502.
93. Yoneyama, M., Kawada, K., Gotoh, Y., Shiba, T., & Ogita, K. (2010). Endogenous reactive oxygen species are essential for proliferation of neural stem/progenitor cells. Neurochemistry International,, 56 740-746.