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Research Article

FBXL5 Inactivation in Mouse Brain Induces Aberrant Proliferation of Neural Stem Progenitor Cells

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Article: e00470-16 | Received 19 Aug 2016, Accepted 03 Jan 2017, Published online: 17 Mar 2023

REFERENCES

  • Rouault TA, Tong WH. 2005. Iron-sulphur cluster biogenesis and mitochondrial iron homeostasis. Nat Rev Mol Cell Biol 6:345–351. https://doi.org/10.1038/nrm1620.
  • Hentze MW, Muckenthaler MU, Galy B, Camaschella C. 2010. Two to tango: regulation of mammalian iron metabolism. Cell 142:24–38. https://doi.org/10.1016/j.cell.2010.06.028.
  • De Domenico I, McVey Ward D, Kaplan J. 2008. Regulation of iron acquisition and storage: consequences for iron-linked disorders. Nat Rev Mol Cell Biol 9:72–81. https://doi.org/10.1038/nrm2295.
  • Torti SV, Torti FM. 2011. Ironing out cancer. Cancer Res 71:1511–1514. https://doi.org/10.1158/0008-5472.CAN-10-3614.
  • Weinberg ED. 2010. The hazards of iron loading. Metallomics 2:732–740. https://doi.org/10.1039/c0mt00023j.
  • Nakayama KI, Nakayama K. 2006. Ubiquitin ligases: cell-cycle control and cancer. Nat Rev Cancer 6:369–381. https://doi.org/10.1038/nrc1881.
  • Wang Z, Liu P, Inuzuka H, Wei W. 2014. Roles of F-box proteins in cancer. Nat Rev Cancer 14:233–247. https://doi.org/10.1038/nrc3700.
  • Salahudeen AA, Thompson JW, Ruiz JC, Ma HW, Kinch LN, Li Q, Grishin NV, Bruick RK. 2009. An E3 ligase possessing an iron-responsive hemerythrin domain is a regulator of iron homeostasis. Science 326:722–726. https://doi.org/10.1126/science.1176326.
  • Vashisht AA, Zumbrennen KB, Huang X, Powers DN, Durazo A, Sun D, Bhaskaran N, Persson A, Uhlen M, Sangfelt O, Spruck C, Leibold EA, Wohlschlegel JA. 2009. Control of iron homeostasis by an iron-regulated ubiquitin ligase. Science 326:718–721. https://doi.org/10.1126/science.1176333.
  • Moroishi T, Nishiyama M, Takeda Y, Iwai K, Nakayama KI. 2011. The FBXL5-IRP2 axis is integral to control of iron metabolism in vivo. Cell Metab 14:339–351. https://doi.org/10.1016/j.cmet.2011.07.011.
  • Ruiz JC, Bruick RK. 2014. F-box and leucine-rich repeat protein 5 (FBXL5): sensing intracellular iron and oxygen. J Inorg Biochem 133:73–77. https://doi.org/10.1016/j.jinorgbio.2014.01.015.
  • Fietz SA, Huttner WB. 2011. Cortical progenitor expansion, self-renewal and neurogenesis-a polarized perspective. Curr Opin Neurobiol 21:23–35. https://doi.org/10.1016/j.conb.2010.10.002.
  • Kriegstein A, Alvarez-Buylla A. 2009. The glial nature of embryonic and adult neural stem cells. Annu Rev Neurosci 32:149–184. https://doi.org/10.1146/annurev.neuro.051508.135600.
  • Kalani MY, Cheshier SH, Cord BJ, Bababeygy SR, Vogel H, Weissman IL, Palmer TD, Nusse R. 2008. Wnt-mediated self-renewal of neural stem/progenitor cells. Proc Natl Acad Sci U S A 105:16970–16975. https://doi.org/10.1073/pnas.0808616105.
  • Belanger M, Allaman I, Magistretti PJ. 2011. Brain energy metabolism: focus on astrocyte-neuron metabolic cooperation. Cell Metab 14:724–738. https://doi.org/10.1016/j.cmet.2011.08.016.
  • Knobloch M, Braun SM, Zurkirchen L, von Schoultz C, Zamboni N, Arauzo-Bravo MJ, Kovacs WJ, Karalay O, Suter U, Machado RA, Roccio M, Lutolf MP, Semenkovich CF, Jessberger S. 2013. Metabolic control of adult neural stem cell activity by Fasn-dependent lipogenesis. Nature 493:226–230. https://doi.org/10.1038/nature11689.
  • De Felice C, Della Ragione F, Signorini C, Leoncini S, Pecorelli A, Ciccoli L, Scalabri F, Marracino F, Madonna M, Belmonte G, Ricceri L, De Filippis B, Laviola G, Valacchi G, Durand T, Galano JM, Oger C, Guy A, Bultel-Ponce V, Guy J, Filosa S, Hayek J, D'Esposito M. 2014. Oxidative brain damage in Mecp2-mutant murine models of Rett syndrome. Neurobiol Dis 68:66–77. https://doi.org/10.1016/j.nbd.2014.04.006.
  • Rouault TA. 2013. Iron metabolism in the CNS: implications for neurodegenerative diseases. Nat Rev Neurosci 14:551–564. https://doi.org/10.1038/nrn3453.
  • Weinreb O, Mandel S, Youdim MB, Amit T. 2013. Targeting dysregulation of brain iron homeostasis in Parkinson's disease by iron chelators. Free Radic Biol Med 62:52–64. https://doi.org/10.1016/j.freeradbiomed.2013.01.017.
  • Lei P, Ayton S, Finkelstein DI, Spoerri L, Ciccotosto GD, Wright DK, Wong BX, Adlard PA, Cherny RA, Lam LQ, Roberts BR, Volitakis I, Egan GF, McLean CA, Cappai R, Duce JA, Bush AI. 2012. Tau deficiency induces parkinsonism with dementia by impairing APP-mediated iron export. Nat Med 18:291–295. https://doi.org/10.1038/nm.2613.
  • Raven EP, Lu PH, Tishler TA, Heydari P, Bartzokis G. 2013. Increased iron levels and decreased tissue integrity in hippocampus of Alzheimer's disease detected in vivo with magnetic resonance imaging. J Alzheimers Dis 37:127–136. https://doi.org/10.3233/JAD-130209.
  • Xiong P, Chen X, Guo C, Zhang N, Ma B. 2012. Baicalin and deferoxamine alleviate iron accumulation in different brain regions of Parkinson's disease rats. Neural Regen Res 7:2092–2098. https://doi.org/10.3969/j.issn.1673-5374.2012.27.002.
  • Regensburger M, Prots I, Winner B. 2014. Adult hippocampal neurogenesis in Parkinson's disease: impact on neuronal survival and plasticity. Neural Plast 2014:454696. https://doi.org/10.1155/2014/454696.
  • van den Berge SA, van Strien ME, Hol EM. 2013. Resident adult neural stem cells in Parkinson's disease—the brain's own repair system? Eur J Pharmacol 719:117–127. https://doi.org/10.1016/j.ejphar.2013.04.058.
  • Turgeon B, Meloche S. 2009. Interpreting neonatal lethal phenotypes in mouse mutants: insights into gene function and human diseases. Physiol Rev 89:1–26. https://doi.org/10.1152/physrev.00040.2007.
  • Dehay C, Kennedy H. 2007. Cell-cycle control and cortical development. Nat Rev Neurosci 8:438–450. https://doi.org/10.1038/nrn2097.
  • Arnold SJ, Huang GJ, Cheung AF, Era T, Nishikawa S, Bikoff EK, Molnar Z, Robertson EJ, Groszer M. 2008. The T-box transcription factor Eomes/Tbr2 regulates neurogenesis in the cortical subventricular zone. Genes Dev 22:2479–2484. https://doi.org/10.1101/gad.475408.
  • Sessa A, Mao CA, Hadjantonakis AK, Klein WH, Broccoli V. 2008. Tbr2 directs conversion of radial glia into basal precursors and guides neuronal amplification by indirect neurogenesis in the developing neocortex. Neuron 60:56–69. https://doi.org/10.1016/j.neuron.2008.09.028.
  • Meguro R, Asano Y, Iwatsuki H, Shoumura K. 2003. Perfusion-Perls and -Turnbull methods supplemented by DAB intensification for nonheme iron histochemistry: demonstration of the superior sensitivity of the methods in the liver, spleen, and stomach of the rat. Histochem Cell Biol 120:73–82. https://doi.org/10.1007/s00418-003-0539-y.
  • Schieber M, Chandel NS. 2014. ROS function in redox signaling and oxidative stress. Curr Biol 24:R453–R462. https://doi.org/10.1016/j.cub.2014.03.034.
  • Kwon J, Lee SR, Yang KS, Ahn Y, Kim YJ, Stadtman ER, Rhee SG. 2004. Reversible oxidation and inactivation of the tumor suppressor PTEN in cells stimulated with peptide growth factors. Proc Natl Acad Sci U S A 101:16419–16424. https://doi.org/10.1073/pnas.0407396101.
  • Leslie NR. 2006. The redox regulation of PI 3-kinase-dependent signaling. Antioxid Redox Signal 8:1765–1774. https://doi.org/10.1089/ars.2006.8.1765.
  • Le Belle JE, Orozco NM, Paucar AA, Saxe JP, Mottahedeh J, Pyle AD, Wu H, Kornblum HI. 2011. Proliferative neural stem cells have high endogenous ROS levels that regulate self-renewal and neurogenesis in a PI3K/Akt-dependent manner. Cell Stem Cell 8:59–71. https://doi.org/10.1016/j.stem.2010.11.028.
  • Magri L, Cambiaghi M, Cominelli M, Alfaro-Cervello C, Cursi M, Pala M, Bulfone A, Garcia-Verdugo JM, Leocani L, Minicucci F, Poliani PL, Galli R. 2011. Sustained activation of mTOR pathway in embryonic neural stem cells leads to development of tuberous sclerosis complex-associated lesions. Cell Stem Cell 9:447–462. https://doi.org/10.1016/j.stem.2011.09.008.
  • Kennedy KA, Sandiford SD, Skerjanc IS, Li SS. 2012. Reactive oxygen species and the neuronal fate. Cell Mol Life Sci 69:215–221. https://doi.org/10.1007/s00018-011-0807-2.
  • Paik JH, Ding Z, Narurkar R, Ramkissoon S, Muller F, Kamoun WS, Chae SS, Zheng H, Ying H, Mahoney J, Hiller D, Jiang S, Protopopov A, Wong WH, Chin L, Ligon KL, DePinho RA. 2009. FoxOs cooperatively regulate diverse pathways governing neural stem cell homeostasis. Cell Stem Cell 5:540–553. https://doi.org/10.1016/j.stem.2009.09.013.
  • Chuikov S, Levi BP, Smith ML, Morrison SJ. 2010. Prdm16 promotes stem cell maintenance in multiple tissues, partly by regulating oxidative stress. Nat Cell Biol 12:999–1006. https://doi.org/10.1038/ncb2101.
  • Wang CR, Liang CC, Bian ZC, Zhu Y, Guan JL. 2013. FIP200 is required for maintenance and differentiation of postnatal neural stem cells. Nat Neurosci 16:532–542. https://doi.org/10.1038/nn.3365.
  • Guan P, Wang N. 2014. Mammalian target of rapamycin coordinates iron metabolism with iron-sulfur cluster assembly enzyme and tristetraprolin. Nutrition 30:968–974. https://doi.org/10.1016/j.nut.2013.12.016.
  • Ndong M, Kazami M, Suzuki T, Uehara M, Katsumata S, Inoue H, Kobayashi K, Tadokoro T, Suzuki K, Yamamoto Y. 2009. Iron deficiency down-regulates the Akt/TSC1-TSC2/mammalian target of rapamycin signaling pathway in rats and in COS-1 cells. Nutr Res 29:640–647. https://doi.org/10.1016/j.nutres.2009.09.007.
  • Ohyashiki JH, Kobayashi C, Hamamura R, Okabe S, Tauchi T, Ohyashiki K. 2009. The oral iron chelator deferasirox represses signaling through the mTOR in myeloid leukemia cells by enhancing expression of REDD1. Cancer Sci 100:970–977. https://doi.org/10.1111/j.1349-7006.2009.01131.x.
  • Knight ZA, Schmidt SF, Birsoy K, Tan K, Friedman JM. 2014. A critical role for mTORC1 in erythropoiesis and anemia. eLife 3:e01913. https://doi.org/10.7554/eLife.01913.
  • Fretham SJ, Carlson ES, Georgieff MK. 2013. Neuronal-specific iron deficiency dysregulates mammalian target of rapamycin signaling during hippocampal development in nonanemic genetic mouse models. J Nutr 143:260–266. https://doi.org/10.3945/jn.112.168617.
  • Gregorian C, Nakashima J, Le Belle J, Ohab J, Kim R, Liu A, Smith KB, Groszer M, Garcia AD, Sofroniew MV, Carmichael ST, Kornblum HI, Liu X, Wu H. 2009. Pten deletion in adult neural stem/progenitor cells enhances constitutive neurogenesis. J Neurosci 29:1874–1886. https://doi.org/10.1523/JNEUROSCI.3095-08.2009.
  • Zeng LH, Rensing NR, Zhang B, Gutmann DH, Gambello MJ, Wong M. 2011. Tsc2 gene inactivation causes a more severe epilepsy phenotype than Tsc1 inactivation in a mouse model of tuberous sclerosis complex. Hum Mol Genet 20:445–454. https://doi.org/10.1093/hmg/ddq491.
  • Amiri A, Cho W, Zhou J, Birnbaum SG, Sinton CM, McKay RM, Parada LF. 2012. Pten deletion in adult hippocampal neural stem/progenitor cells causes cellular abnormalities and alters neurogenesis. J Neurosci 32:5880–5890. https://doi.org/10.1523/JNEUROSCI.5462-11.2012.
  • Yokogami K, Wakisaka S, Avruch J, Reeves SA. 2000. Serine phosphorylation and maximal activation of STAT3 during CNTF signaling is mediated by the rapamycin target mTOR. Curr Biol 10:47–50. https://doi.org/10.1016/S0960-9822(99)00268-7.
  • Costa-Mattioli M, Monteggia LM. 2013. mTOR complexes in neurodevelopmental and neuropsychiatric disorders. Nat Neurosci 16:1537–1543. https://doi.org/10.1038/nn.3546.
  • Pecorelli A, Leoncini S, De Felice C, Signorini C, Cerrone C, Valacchi G, Ciccoli L, Hayek J. 2013. Non-protein-bound iron and 4-hydroxynonenal protein adducts in classic autism. Brain Dev 35:146–154. https://doi.org/10.1016/j.braindev.2012.03.011.
  • Matsumoto A, Onoyama I, Sunabori T, Kageyama R, Okano H, Nakayama KI. 2011. Fbxw7-dependent degradation of Notch is required for control of “stemness” and neuronal-glial differentiation in neural stem cells. J Biol Chem 286:13754–13764. https://doi.org/10.1074/jbc.M110.194936.
  • Patel BN, Dunn RJ, Jeong SY, Zhu QZ, Julien JP, David S. 2002. Ceruloplasmin regulates iron levels in the CNS and prevents free radical injury. J Neurosci 22:6578–6586.
  • Moroishi T, Yamauchi T, Nishiyama M, Nakayama KI. 2014. HERC2 targets the iron regulator FBXL5 for degradation and modulates iron metabolism. J Biol Chem 289:16430–16441. https://doi.org/10.1074/jbc.M113.541490.
  • Yamauchi T, Nishiyama M, Moroishi T, Yumimoto K, Nakayama KI. 2014. MDM2 mediates nonproteolytic polyubiquitylation of the DEAD-box RNA helicase DDX24. Mol Cell Biol 34:3321–3340. https://doi.org/10.1128/MCB.00320-14.
  • Lee SR, Yang KS, Kwon J, Lee C, Jeong W, Rhee SG. 2002. Reversible inactivation of the tumor suppressor PTEN by H2O2. J Biol Chem 277:20336–20342. https://doi.org/10.1074/jbc.M111899200.

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