Tauroursodeoxycholic acid increases neural stem cell pool and neuronal conversion by regulating mitochondria-cell cycle retrograde signaling

References

• Koussevitzky S, Nott A, Mockler TC, Hong F, Sachetto-Martins G, Surpin M, Lim J, Mittler R, Chory J. Signals from chloroplasts converge to regulate nuclear gene expression. Science 2007; 316:715-9; PMID:17395793; http://dx.doi.org/10.1126/science
   PubMed Web of Science ®Google Scholar
• Butow RA, Avadhani NG. Mitochondrial signaling: the retrograde response. Mol Cell 2004; 14:1-15; PMID:15068799; http://dx.doi.org/10.1016/S1097-2765(04)00179-0
   PubMed Web of Science ®Google Scholar
• McBride HM, Neuspiel M, Wasiak S. Mitochondria: more than just a powerhouse. Curr Biol 2006; 16:R551-60; PMID:16860735; http://dx.doi.org/10.1016/j.cub.2006.06.054
   PubMed Web of Science ®Google Scholar
• Nagley P, Higgins GC, Atkin JD, Beart PM. Multifaceted deaths orchestrated by mitochondria in neurones. Biochim Biophys Acta 2010; 1802:167-85; PMID:19751830; http://dx.doi.org/10.1016/j.bbadis.2009.09.004
   PubMed Web of Science ®Google Scholar
• Parker GC, Acsadi G, Brenner CA. Mitochondria: determinants of stem cell fate? Stem Cells Dev 2009; 18:803-6; PMID:19563264; http://dx.doi.org/10.1089/scd.2009.1806.edi
   PubMed Web of Science ®Google Scholar
• Kole AJ, Annis RP, Deshmukh M. Mature neurons: equipped for survival. Cell Death Dis 2013; 4:e689; PMID:23807218; http://dx.doi.org/10.1038/cddis.2013.220
   PubMedGoogle Scholar
• Le Belle JE, Orozco NM, Paucar AA, Saxe JP, Mottahedeh J, Pyle AD, Wu H, Kornblum HI. Proliferative neural stem cells have high endogenous ROS levels that regulate self-renewal and neurogenesis in a PI3K/Akt-dependant manner. Cell Stem Cell 2011; 8:59-71; PMID:21211782; http://dx.doi.org/10.1016/j.stem.2010.11.028
   PubMed Web of Science ®Google Scholar
• Panchision DM. The role of oxygen in regulating neural stem cells in development and disease. J Cell Physiol 2009; 220:562-8; PMID:19441077; http://dx.doi.org/10.1002/jcp.21812
   PubMed Web of Science ®Google Scholar
• Voloboueva LA, Lee SW, Emery JF, Palmer TD, Giffard RG. Mitochondrial protection attenuates inflammation-induced impairment of neurogenesis in vitro and in vivo. J Neurosci 2010; 30:12242-51; PMID:20844120; http://dx.doi.org/10.1523/JNEUROSCI.1752-10.2010
   PubMed Web of Science ®Google Scholar
• Facucho-Oliveira JM, Alderson J, Spikings EC, Egginton S, St John JC. Mitochondrial DNA replication during differentiation of murine embryonic stem cells. J Cell Sci 2007; 120:4025-34; PMID:17971411; http://dx.doi.org/10.1242/jcs.016972
   PubMed Web of Science ®Google Scholar
• Wang W, Osenbroch P, Skinnes R, Esbensen Y, Bjoras M, Eide L. Mitochondrial DNA integrity is essential for mitochondrial maturation during differentiation of neural stem cells. Stem Cells 2010; 28:2195-204; PMID:20954243; http://dx.doi.org/10.1002/stem.542
   PubMed Web of Science ®Google Scholar
• Owusu-Ansah E, Yavari A, Mandal S, Banerjee U. Distinct mitochondrial retrograde signals control the G1-S cell cycle checkpoint. Nat Genet 2008; 40:356-61; PMID:18246068; http://dx.doi.org/10.1038/ng.2007.50
   PubMed Web of Science ®Google Scholar
• Weinberg RA. The retinoblastoma protein and cell cycle control. Cell 1995; 81:323-30; PMID:7736585; http://dx.doi.org/10.1016/0092-8674(95)90385-2
   PubMed Web of Science ®Google Scholar
• Lundberg AS, Weinberg RA. Functional inactivation of the retinoblastoma protein requires sequential modification by at least two distinct cyclin-cdk complexes. Mol Cell Biol 1998; 18:753-61; PMID:9447971
   PubMed Web of Science ®Google Scholar
• Xavier JM, Morgado AL, Sola S, Rodrigues CM. Mitochondrial translocation of p53 modulates neuronal fate by preventing differentiation-induced mitochondrial stress. Antioxid Redox Signal 2014; 21:1009-24; PMID:24329038; http://dx.doi.org/10.1089/ars.2013.5417
   PubMed Web of Science ®Google Scholar
• Wang W, Esbensen Y, Kunke D, Suganthan R, Rachek L, Bjoras M, Eide L. Mitochondrial DNA damage level determines neural stem cell differentiation fate. J Neurosci 2011; 31:9746-51; PMID:21715639; http://dx.doi.org/10.1523/JNEUROSCI.0852-11.2011
   PubMed Web of Science ®Google Scholar
• Rodrigues CM, Stieers CL, Keene CD, Ma X, Kren BT, Low WC, Steer CJ. Tauroursodeoxycholic acid partially prevents apoptosis induced by 3-nitropropionic acid: evidence for a mitochondrial pathway independent of the permeability transition. J Neurochem 2000; 75:2368-79; PMID:11080188; http://dx.doi.org/10.1046/j.1471-4159.2000.0752368.x
   PubMed Web of Science ®Google Scholar
• Sola S, Aranha MM, Rodrigues CM. Driving apoptosis-relevant proteins toward neural differentiation. Mol Neurobiol 2012; 46:316-31; PMID:22752662; http://dx.doi.org/10.1007/s12035-012-8289-2
   PubMed Web of Science ®Google Scholar
• Lazaridis KN, Gores GJ, Lindor KD. Ursodeoxycholic acid 'mechanisms of action and clinical use in hepatobiliary disorders’. J Hepatol 2001; 35:134-46; PMID:11495032; http://dx.doi.org/10.1016/S0168-8278(01)00092-7
   PubMed Web of Science ®Google Scholar
• Paumgartner G, Beuers U. Ursodeoxycholic acid in cholestatic liver disease: mechanisms of action and therapeutic use revisited. Hepatology 2002; 36:525-31; PMID:12198643; http://dx.doi.org/10.1053/jhep.2002.36088
   PubMed Web of Science ®Google Scholar
• Keene CD, Rodrigues CM, Eich T, Chhabra MS, Steer CJ, Low WC. Tauroursodeoxycholic acid, a bile acid, is neuroprotective in a transgenic animal model of Huntington's disease. Proc Natl Acad Sci U S A 2002; 99:10671-6; PMID:12149470; http://dx.doi.org/10.1073/pnas.162362299
   PubMed Web of Science ®Google Scholar
• Duan WM, Rodrigues CM, Zhao LR, Steer CJ, Low WC. Tauroursodeoxycholic acid improves the survival and function of nigral transplants in a rat model of Parkinson's disease. Cell Transplant 2002; 11:195-205; PMID:12075985
   PubMed Web of Science ®Google Scholar
• Rodrigues CM, Sola S, Nan Z, Castro RE, Ribeiro PS, Low WC, Steer CJ. Tauroursodeoxycholic acid reduces apoptosis and protects against neurological injury after acute hemorrhagic stroke in rats. Proc Natl Acad Sci U S A 2003; 100:6087-92; PMID:12721362; http://dx.doi.org/10.1073/pnas.1031632100
   PubMed Web of Science ®Google Scholar
• Sola S, Aranha MM, Steer CJ, Rodrigues CM. Game and players: mitochondrial apoptosis and the therapeutic potential of ursodeoxycholic acid. Curr Issues Mol Biol 2007; 9:123-38; PMID:17489439
   PubMed Web of Science ®Google Scholar
• Oveson BC, Iwase T, Hackett SF, Lee SY, Usui S, Sedlak TW, Snyder SH, Campochiaro PA, Sung JU. Constituents of bile, bilirubin and TUDCA, protect against oxidative stress-induced retinal degeneration. J Neurochem 2011; 116:144-53; PMID:21054389; http://dx.doi.org/10.1111/j.1471-4159.2010.07092.x
   PubMed Web of Science ®Google Scholar
• Parry GJ, Rodrigues CM, Aranha MM, Hilbert SJ, Davey C, Kelkar P, Low WC, Steer CJ. Safety, tolerability, and cerebrospinal fluid penetration of ursodeoxycholic Acid in patients with amyotrophic lateral sclerosis. Clin Neuropharmacol 2010; 33:17-21; PMID:19935406; http://dx.doi.org/10.1097/WNF.0b013e3181c47569
   PubMed Web of Science ®Google Scholar
• Huxtable RJ. Physiological actions of taurine. Physiol Rev 1992; 72:101-63; PMID:1731369
   PubMed Web of Science ®Google Scholar
• Hernandez-Benitez R, Pasantes-Morales H, Saldana IT, Ramos-Mandujano G. Taurine stimulates proliferation of mice embryonic cultured neural progenitor cells. J Neurosci Res 2010; 88:1673-81; PMID:20029963
   PubMed Web of Science ®Google Scholar
• Shivaraj MC, Marcy G, Low G, Ryu JR, Zhao X, Rosales FJ, Goh EL. Taurine induces proliferation of neural stem cells and synapse development in the developing mouse brain. PLoS One 2012; 7:e42935; PMID:22916184; http://dx.doi.org/10.1371/journal.pone.0042935
   PubMed Web of Science ®Google Scholar
• Antico Arciuch VG, Elguero ME, Poderoso JJ, Carreras MC. Mitochondrial regulation of cell cycle and proliferation. Antioxid Redox Signal 2012; 16:1150-80; PMID:21967640; http://dx.doi.org/10.1089/ars.2011.4085
   PubMed Web of Science ®Google Scholar
• Kato JY, Matsuoka M, Polyak K, Massague J, Sherr CJ. Cyclic AMP-induced G1 phase arrest mediated by an inhibitor (p27Kip1) of cyclin-dependent kinase 4 activation. Cell 1994; 79:487-96; PMID:7954814; http://dx.doi.org/10.1016/0092-8674(94)90257-7
   PubMed Web of Science ®Google Scholar
• Gartel AL, Radhakrishnan SK. Lost in transcription: p21 repression, mechanisms, and consequences. Cancer Res 2005; 65:3980-5; PMID:15899785; http://dx.doi.org/10.1158/0008-5472.CAN-04-3995
   PubMed Web of Science ®Google Scholar
• Finkel T, Hwang PM. The Krebs cycle meets the cell cycle: mitochondria and the G1-S transition. Proc Natl Acad Sci U S A 2009; 106:11825-6; PMID:19617546; http://dx.doi.org/10.1073/pnas.0906430106
   PubMed Web of Science ®Google Scholar
• Alenzi FQ, Alenazi BQ, Ahmad SY, Salem ML, Al-Jabri AA, Wyse RK. The haemopoietic stem cell: between apoptosis and self renewal. Yale J Biol Med 2009; 82:7-18; PMID:19325941
   PubMedGoogle Scholar
• Mandal S, Lindgren AG, Srivastava AS, Clark AT, Banerjee U. Mitochondrial function controls proliferation and early differentiation potential of embryonic stem cells. Stem Cells 2011; 29:486-95; PMID:21425411; http://dx.doi.org/10.1002/stem.590
   PubMed Web of Science ®Google Scholar
• Durand B, Raff M. A cell-intrinsic timer that operates during oligodendrocyte development. Bioessays 2000; 22:64-71; PMID:10649292; http://dx.doi.org/10.1002/(SICI)1521-1878(200001)22:1<64::AID-BIES11>3.0.CO;2-Q
   PubMed Web of Science ®Google Scholar
• Ohnuma S, Harris WA. Neurogenesis and the cell cycle. Neuron 2003; 40:199-208; PMID:14556704; http://dx.doi.org/10.1016/S0896-6273(03)00632-9
   PubMed Web of Science ®Google Scholar
• Salomoni P, Calegari F. Cell cycle control of mammalian neural stem cells: putting a speed limit on G1. Trends Cell Biol 2010; 20:233-43; PMID:20153966; http://dx.doi.org/10.1016/j.tcb.2010.01.006
   PubMed Web of Science ®Google Scholar
• Solter M, Locker M, Boy S, Taelman V, Bellefroid EJ, Perron M, Pieler T. Characterization and function of the bHLH-O protein XHes2: insight into the mechanisms controlling retinal cell fate decision. Development 2006; 133:4097-108; PMID:17008450; http://dx.doi.org/10.1242/dev.02567
   PubMed Web of Science ®Google Scholar
• Rodrigues CM, Sola S, Silva R, Brites D. Bilirubin and amyloid-beta peptide induce cytochrome c release through mitochondrial membrane permeabilization. Mol Med 2000; 6:936-46; PMID:11147571
   PubMed Web of Science ®Google Scholar
• Sola S, Castro RE, Laires PA, Steer CJ, Rodrigues CM. Tauroursodeoxycholic acid prevents amyloid-beta peptide-induced neuronal death via a phosphatidylinositol 3-kinase-dependent signaling pathway. Mol Med 2003; 9:226-34; PMID:15208744; http://dx.doi.org/10.2119/2003-00042.Rodrigues
   PubMed Web of Science ®Google Scholar
• Rugarli EI, Langer T. Mitochondrial quality control: a matter of life and death for neurons. EMBO J 2012; 31:1336-49; PMID:22354038; http://dx.doi.org/10.1038/emboj.2012.38
   PubMed Web of Science ®Google Scholar
• Cheng A, Hou Y, Mattson MP. Mitochondria and neuroplasticity. ASN Neuro 2010; 2:e00045; PMID:20957078; http://dx.doi.org/10.1042/AN20100019
   PubMed Web of Science ®Google Scholar
• Facucho-Oliveira JM, St John JC. The relationship between pluripotency and mitochondrial DNA proliferation during early embryo development and embryonic stem cell differentiation. Stem Cell Rev 2009; 5:140-58; PMID:19521804; http://dx.doi.org/10.1007/s12015-009-9058-0
   PubMed Web of Science ®Google Scholar
• Tolkovsky AM. Mitophagy. Biochim Biophys Acta 2009; 1793:1508-15; PMID:19289147; http://dx.doi.org/10.1016/j.bbamcr.2009.03.002
   PubMed Web of Science ®Google Scholar
• O'Farrell PH, Stumpff J, Su TT. Embryonic cleavage cycles: how is a mouse like a fly? Curr Biol 2004; 14:R35-45; PMID:14711435; http://dx.doi.org/10.1016/j.cub.2003.12.022
   PubMed Web of Science ®Google Scholar
• Pauklin S, Vallier L. The cell-cycle state of stem cells determines cell fate propensity. Cell 2013; 155:135-47; PMID:24074866; http://dx.doi.org/10.1016/j.cell.2013.08.031
   PubMed Web of Science ®Google Scholar
• Tsunekawa Y, Osumi N. How to keep proliferative neural stem/progenitor cells: a critical role of asymmetric inheritance of cyclin D2. Cell Cycle 2012; 11:3550-4; PMID:22895110; http://dx.doi.org/10.4161/cc.21500
   PubMed Web of Science ®Google Scholar
• Molofsky AV, Slutsky SG, Joseph NM, He S, Pardal R, Krishnamurthy J, Sharpless NE, Morrison SJ. Increasing p16INK4a expression decreases forebrain progenitors and neurogenesis during ageing. Nature 2006; 443:448-52; PMID:16957738; http://dx.doi.org/10.1038/nature05091
   PubMed Web of Science ®Google Scholar
• Behrens A, van Deursen JM, Rudolph KL, Schumacher B. Impact of genomic damage and ageing on stem cell function. Nat Cell Biol 2014; 16:201-7; PMID:24576896; http://dx.doi.org/10.1038/ncb2928
   PubMed Web of Science ®Google Scholar
• Piccin D, Morshead CM. Potential and pitfalls of stem cell therapy in old age. Dis Model Mech 2010; 3:421-5; PMID:20504968; http://dx.doi.org/10.1242/dmm.003137
   PubMed Web of Science ®Google Scholar
• Artegiani B, Calegari F. Age-related cognitive decline: can neural stem cells help us? Aging (Albany NY) 2012; 4:176-86; PMID:22466406
   PubMedGoogle Scholar
• Sauer H, Wartenberg M, Hescheler J. Reactive oxygen species as intracellular messengers during cell growth and differentiation. Cell Physiol Biochem 2001; 11:173-86; PMID:11509825; http://dx.doi.org/10.1159/000047804
   PubMed Web of Science ®Google Scholar
• Deng X, Gao F, May WS Jr. Bcl2 retards G1/S cell cycle transition by regulating intracellular ROS. Blood 2003; 102:3179-85; PMID:12855558; http://dx.doi.org/10.1182/blood-2003-04-1027
   PubMed Web of Science ®Google Scholar
• Mandal S, Guptan P, Owusu-Ansah E, Banerjee U. Mitochondrial regulation of cell cycle progression during development as revealed by the tenured mutation in Drosophila. Dev Cell 2005; 9:843-54; PMID: 16326395; http://dx.doi.org/10.1016/j.devcel.2005.11.006
   PubMed Web of Science ®Google Scholar
• Lange C, Huttner WB, Calegari F. Cdk4/cyclinD1 overexpression in neural stem cells shortens G1, delays neurogenesis, and promotes the generation and expansion of basal progenitors. Cell Stem Cell 2009; 5:320-31; PMID:19733543; http://dx.doi.org/10.1016/j.stem.2009.05.026
   PubMed Web of Science ®Google Scholar
• Qian X, Shen Q, Goderie SK, He W, Capela A, Davis AA, Temple S. Timing of CNS cell generation: a programmed sequence of neuron and glial cell production from isolated murine cortical stem cells. Neuron 2000; 28:69-80; PMID:11086984; http://dx.doi.org/10.1016/S0896-6273(00)00086-6
   PubMed Web of Science ®Google Scholar
• Sola S, Morgado AL, Rodrigues CM. Death receptors and mitochondria: Two prime triggers of neural apoptosis and differentiation. Biochim Biophys Acta 2013; 1830:2160-6; PMID:23041071; http://dx.doi.org/10.1016/j.bbagen.2012.09.021
   PubMed Web of Science ®Google Scholar
• Castro RE, Sola S, Ramalho RM, Steer CJ, Rodrigues CM. The bile acid tauroursodeoxycholic acid modulates phosphorylation and translocation of bad via phosphatidylinositol 3-kinase in glutamate-induced apoptosis of rat cortical neurons. J Pharmacol Exp Ther 2004; 311:845-52; PMID:15190125; http://dx.doi.org/10.1124/jpet.104.070532
   PubMed Web of Science ®Google Scholar
• Qureshi IA, Gokhan S, Mehler MF. REST and CoREST are transcriptional and epigenetic regulators of seminal neural fate decisions. Cell Cycle 2010; 9:4477-86; PMID:21088488; http://dx.doi.org/10.4161/cc.9.22.13973
   PubMed Web of Science ®Google Scholar
• Silva J, Chambers I, Pollard S, Smith A. Nanog promotes transfer of pluripotency after cell fusion. Nature 2006; 441:997-1001; PMID:16791199; http://dx.doi.org/10.1038/nature04914
   PubMed Web of Science ®Google Scholar
• Conti L, Pollard SM, Gorba T, Reitano E, Toselli M, Biella G, Sun Y, Sanzone S, Ying QL, Cattaneo E, et al. Niche-independent symmetrical self-renewal of a mammalian tissue stem cell. PLoS Biol 2005; 3:e283; PMID:16086633; http://dx.doi.org/10.1371/journal.pbio.0030283
   PubMed Web of Science ®Google Scholar
• Pollard SM, Conti L, Sun Y, Goffredo D, Smith A. Adherent neural stem (NS) cells from fetal and adult forebrain. Cereb Cortex 2006; 16 Suppl 1:i112-20; PMID:16766697; http://dx.doi.org/10.1093/cercor/bhj167
   PubMed Web of Science ®Google Scholar
• Glaser T, Pollard SM, Smith A, Brustle O. Tripotential differentiation of adherently expandable neural stem (NS) cells. PLoS One 2007; 2:e298; PMID:17356704; http://dx.doi.org/10.1371/journal.pone.0000298
   PubMed Web of Science ®Google Scholar
• Santos DM, Xavier JM, Morgado AL, Sola S, Rodrigues CM. Distinct regulatory functions of calpain 1 and 2 during neural stem cell self-renewal and differentiation. PLoS One 2012; 7:e33468; PMID:22432027; http://dx.doi.org/10.1371/journal.pone.0033468
   PubMedGoogle Scholar
• MacMillan-Crow LA, Crow JP, Thompson JA. Peroxynitrite-mediated inactivation of manganese superoxide dismutase involves nitration and oxidation of critical tyrosine residues. Biochemistry 1998; 37:1613-22; PMID:9484232; http://dx.doi.org/10.1021/bi971894b
   PubMed Web of Science ®Google Scholar
• Redondo-Horcajo M, Romero N, Martinez-Acedo P, Martinez-Ruiz A, Quijano C, Lourenco CF, Movilla N, Enriquez JA, Rodriguez-Pascual F, Rial E, et al. Cyclosporine A-induced nitration of tyrosine 34 MnSOD in endothelial cells: role of mitochondrial superoxide. Cardiovasc Res 2010; 87:356-65; PMID:20106845; http://dx.doi.org/10.1093/cvr/cvq028
   PubMed Web of Science ®Google Scholar
• Holley AK, Dhar SK, St Clair DK. Manganese superoxide dismutase vs. p53: regulation of mitochondrial ROS. Mitochondrion 2010; 10:649-61; PMID:20601193; http://dx.doi.org/10.1016/j.mito.2010.06.003
   PubMed Web of Science ®Google Scholar
• Bakthavatchalu V, Dey S, Xu Y, Noel T, Jungsuwadee P, Holley AK, Dhar SK, Batinic-Haberle I, St Clair DK. Manganese superoxide dismutase is a mitochondrial fidelity protein that protects Polgamma against UV-induced inactivation. Oncogene 2012; 31:2129-39; PMID:21909133; http://dx.doi.org/10.1038/onc.2011.407
   PubMed Web of Science ®Google Scholar
• Devenish RJ, Prescott M, Boyle GM, Nagley P. The oligomycin axis of mitochondrial ATP synthase: OSCP and the proton channel. J Bioenerg Biomembr 2000; 32:507-15; PMID:15254386; http://dx.doi.org/10.1023/A:1005621125812
   PubMed Web of Science ®Google Scholar
• Symersky J, Osowski D, Walters DE, Mueller DM. Oligomycin frames a common drug-binding site in the ATP synthase. Proc Natl Acad Sci U S A 2012; 109:13961-5; PMID:22869738; http://dx.doi.org/10.1073/pnas.1207912109
   PubMed Web of Science ®Google Scholar
• Pagliarani A, Nesci S, Ventrella V. Modifiers of the oligomycin sensitivity of the mitochondrial F1F0-ATPase. Mitochondrion 2013; 13:312-9; PMID:23597783; http://dx.doi.org/10.1016/j.mito.2013.04.005
   PubMed Web of Science ®Google Scholar
• Eaton JS, Lin ZP, Sartorelli AC, Bonawitz ND, Shadel GS. Ataxia-telangiectasia mutated kinase regulates ribonucleotide reductase and mitochondrial homeostasis. J Clin Invest 2007; 117:2723-34; PMID:17786248; http://dx.doi.org/10.1172/JCI31604
   PubMed Web of Science ®Google Scholar
• Nowakowski RS, Lewin SB, Miller MW. Bromodeoxyuridine immunohistochemical determination of the lengths of the cell cycle and the DNA-synthetic phase for an anatomically defined population. J Neurocytol 1989; 18:311-8; PMID:2746304; http://dx.doi.org/10.1007/BF01190834
   PubMedGoogle Scholar
• Graham V, Khudyakov J, Ellis P, Pevny L. SOX2 functions to maintain neural progenitor identity. Neuron 2003; 39:749-65; PMID:12948443; http://dx.doi.org/10.1016/S0896-6273(03)00497-5
   PubMed Web of Science ®Google Scholar
• Thiel G. How Sox2 maintains neural stem cell identity. Biochem J 2013; 450:e1-2; PMID:23445224; http://dx.doi.org/10.1042/BJ20130176
   PubMedGoogle Scholar
• Xapelli S, Agasse F, Sarda-Arroyo L, Bernardino L, Santos T, Ribeiro FF, Valero J, Braganca J, Schitine C, de Melo Reis RA, et al. Activation of type 1 cannabinoid receptor (CB1R) promotes neurogenesis in murine subventricular zone cell cultures. PLoS One 2013; 8:e63529; PMID:23704915; http://dx.doi.org/10.1371/journal.pone.0063529
   PubMedGoogle Scholar
• Shen Q, Zhong W, Jan YN, Temple S. Asymmetric Numb distribution is critical for asymmetric cell division of mouse cerebral cortical stem cells and neuroblasts. Development 2002; 129:4843-53; PMID:12361975
   PubMed Web of Science ®Google Scholar