Sonic Hedgehog Promotes Neurite Outgrowth of Primary Cortical Neurons Through Up-Regulating BDNF Expression

详细信息    查看全文

• 作者：Weiliang He ; Lili Cui ; Cong Zhang ; Xiangjian Zhang ; Junna He…
• 关键词：Sonic hedgehog ; Cortical neuron ; Neurite outgrowth ; Brain ; derived neurotrophic factor
• 刊名：Neurochemical Research
• 出版年：2016
• 出版时间：April 2016
• 年：2016
• 卷：41
• 期：4
• 页码：687-695
• 全文大小：1,056 KB
• 参考文献：1.Bradke F, Dotti CG (2000) Differentiated neurons retain the capacity to generate axons from dendrites. Curr Biol 10:1467–1470CrossRef PubMed
  2.Conde C, Caceres A (2009) Microtubule assembly, organization and dynamics in axons and dendrites. Nat Rev Neurosci 10:319–332CrossRef PubMed
  3.Wilson NH, Stoeckli ET (2012) Sonic Hedgehog regulates Wnt activity during neural circuit formation. Vitam Horm 88:173–209CrossRef PubMed
  4.Hooper JE, Scott MP (2005) Communicating with Hedgehogs. Nat Rev Mol Cell Biol 6:306–317CrossRef PubMed
  5.Charron F, Stein E, Jeong J, McMahon AP, Tessier-Lavigne M (2003) The morphogen sonic hedgehog is an axonal chemoattractant that collaborates with netrin-1 in midline axon guidance. Cell 113:11–23CrossRef PubMed
  6.Lai K, Kaspar BK, Gage FH, Schaffer DV (2003) Sonic hedgehog regulates adult neural progenitor proliferation in vitro and in vivo. Nat Neurosci 6:21–27CrossRef PubMed
  7.Ahn S, Joyner AL (2005) In vivo analysis of quiescent adult neural stem cells responding to Sonic hedgehog. Nature 437:894–897CrossRef PubMed
  8.Palma V, Lim DA, Dahmane N, Sanchez P, Brionne TC, Herzberg CD, Gitton Y, Carleton A, Alvarez-Buylla A, Ruiz i Altaba A (2005) Sonic hedgehog controls stem cell behavior in the postnatal and adult brain. Development 132:335–344CrossRef PubMed PubMedCentral
  9.Sims JR, Lee SW, Topalkara K, Qiu J, Xu J, Zhou Z, Moskowitz MA (2009) Sonic hedgehog regulates ischemia/hypoxia-induced neural progenitor proliferation. Stroke 40:3618–3626CrossRef PubMed PubMedCentral
  10.Ji H, Miao J, Zhang X, Du Y, Liu H, Li S, Li L (2012) Inhibition of sonic hedgehog signaling aggravates brain damage associated with the down-regulation of Gli1, Ptch1 and SOD1 expression in acute ischemic stroke. Neurosci Lett 506:1–6CrossRef PubMed
  11.Trzaska KA, King CC, Li KY, Kuzhikandathil EV, Nowycky MC, Ye JH, Rameshwar P (2009) Brain-derived neurotrophic factor facilitates maturation of mesenchymal stem cell-derived dopamine progenitors to functional neurons. J Neurochem 110:1058–1069CrossRef PubMed
  12.Yoshii A, Constantine-Paton M (2010) Postsynaptic BDNF-TrkB signaling in synapse maturation, plasticity, and disease. Dev Neurobiol 70:304–322PubMed PubMedCentral
  13.Antal A, Chaieb L, Moliadze V, Monte-Silva K, Poreisz C, Thirugnanasambandam N, Nitsche MA, Shoukier M, Ludwig H, Paulus W (2010) Brain-derived neurotrophic factor (BDNF) gene polymorphisms shape cortical plasticity in humans. Brain Stimul 3:230–237CrossRef PubMed
  14.Castillo DV, Escobar ML (2011) A role for MAPK and PI-3K signaling pathways in brain-derived neurotrophic factor modification of conditioned taste aversion retention. Behav Brain Res 217:248–252CrossRef PubMed
  15.Ng BK, Chen L, Mandemakers W, Cosgaya JM, Chan JR (2007) Anterograde transport and secretion of brain-derived neurotrophic factor along sensory axons promote Schwann cell myelination. J Neurosci 27:7597–7603CrossRef PubMed
  16.Dai RL, Zhu SY, Xia YP, Mao L, Mei YW, Yao YF, Xue YM, Hu B (2011) Sonic hedgehog protects cortical neurons against oxidative stress. Neurochem Res 36:67–75CrossRef PubMed
  17.Bond CW, Angeloni N, Harrington D, Stupp S, Podlasek CA (2013) Sonic Hedgehog regulates brain-derived neurotrophic factor in normal and regenerating cavernous nerves. J Sex Med 10:730–737CrossRef PubMed PubMedCentral
  18.Hashimoto M, Ishii K, Nakamura Y, Watabe K, Kohsaka S, Akazawa C (2008) Neuroprotective effect of sonic hedgehog up-regulated in Schwann cells following sciatic nerve injury. J Neurochem 107:918–927CrossRef PubMed
  19.Kolbeck R, Bartke I, Eberle W, Barde YA (1999) Brain-derived neurotrophic factor levels in the nervous system of wild-type and neurotrophin gene mutant mice. J Neurochem 72:1930–1938CrossRef PubMed
  20.Marti E, Bovolenta P (2002) Sonic hedgehog in CNS development: one signal, multiple outputs. Trends Neurosci 25:89–96CrossRef PubMed
  21.Gong Q, Chen H, Farbman AI (2009) Olfactory sensory axon growth and branching is influenced by sonic hedgehog. Dev Dyn 238:1768–1776CrossRef PubMed PubMedCentral
  22.Fantetti KN, Fekete DM (2012) Members of the BMP, Shh, and FGF morphogen families promote chicken statoacoustic ganglion neurite outgrowth and neuron survival in vitro. Dev Neurobiol 72:1213–1228CrossRef PubMed PubMedCentral
  23.Machold R, Hayashi S, Rutlin M, Muzumdar MD, Nery S, Corbin JG, Gritli-Linde A, Dellovade T, Porter JA, Rubin LL, Dudek H, McMahon AP, Fishell G (2003) Sonic hedgehog is required for progenitor cell maintenance in telencephalic stem cell niches. Neuron 39:937–950CrossRef PubMed
  24.Wang L, Zhang ZG, Gregg SR, Zhang RL, Jiao Z, LeTourneau Y, Liu X, Feng Y, Gerwien J, Torup L, Leist M, Noguchi CT, Chen ZY, Chopp M (2007) The Sonic hedgehog pathway mediates carbamylated erythropoietin-enhanced proliferation and differentiation of adult neural progenitor cells. J Biol Chem 282:32462–32470CrossRef PubMed
  25.Radonjić NV, Memi F, Ortega JA, Glidden N, Zhan H, Zecevic N (2014) The role of sonic hedgehog in the specification of human cortical progenitors in vitro. Cereb Cortex. doi:10.​1093/​cercor/​bhu183 PubMed
  26.Zhang L, Chopp M, Meier DH, Winter S, Wang L, Szalad A, Lu M, Wei M, Cui Y, Zhang ZG (2013) Sonic hedgehog signaling pathway mediates cerebrolysin-improved neurological function after stroke. Stroke 44:1965–1972CrossRef PubMed
  27.Murray K, Calaora V, Rottkamp C, Guicherit O, Dubois-Dalcq M (2002) Sonic hedgehog is a potent inducer of rat oligodendrocyte development from cortical precursors in vitro. Mol Cell Neurosci 19:320–332CrossRef PubMed
  28.Hyman C, Hofer M, Barde YA, Juhasz M, Yancopoulos GD, Squinto SP, Lindsay RM (1991) BDNF is a neurotrophic factor for dopaminergic neurons of the substantia nigra. Nature 350:230–232CrossRef PubMed
  29.Binder DK, Scharfman HE (2004) Brain-derived neurotrophic factor. Growth Factors 22:123–131CrossRef PubMed PubMedCentral
  30.Cui X, Chopp M, Zacharek A, Roberts C, Buller B, Ion M, Chen J (2010) Niacin treatment of stroke increases synaptic plasticity and axon growth in rats. Stroke 41:2044–2049CrossRef PubMed PubMedCentral
  31.Su Y, Cui L, Piao C, Li B, Zhao LR (2013) The effects of hematopoietic growth factors on neurite outgrowth. PLoS ONE 8:e75562CrossRef PubMed PubMedCentral
  32.Riobo NA, Manning DR (2007) Pathways of signal transduction employed by vertebrate Hedgehogs. Biochem J 403:369–379CrossRef PubMed
  33.Wu CL, Chen SD, Hwang CS, Yang DI (2009) Sonic hedgehog mediates BDNF-induced neuroprotection against mitochondrial inhibitor 3-nitropropionic acid. Biochem Biophys Res Commun 385:112–117CrossRef PubMed
  34.Wu CL, Chen SD, Yin JH, Hwang CS, Yang DI (2010) Erythropoietin and sonic hedgehog mediate the neuroprotective effects of brain-derived neurotrophic factor against mitochondrial inhibition. Neurobiol Dis 40:146–154CrossRef PubMed
  
• 作者单位：Weiliang He (1) (2) (3) (4)
  Lili Cui (1) (2) (3) (4)
  Cong Zhang (1) (2) (3) (4)
  Xiangjian Zhang (1) (2) (3) (4)
  Junna He (1) (2) (3) (4)
  Yanzhao Xie (1) (2) (3) (4)
  
  1. Department of Neurology, Second Hospital of Hebei Medical University, Shijiazhuang, 050000, Hebei, People’s Republic of China
  2. Hebei Key Laboratory for Neurology, Shijiazhuang, 050000, Hebei, People’s Republic of China
  3. Hebei Collaborative Innovation Center for Cardio-cerebrovascular Disease, Shijiazhuang, 050000, Hebei, People’s Republic of China
  4. Hebei Key Laboratory of Vascular Homeostasis, Shijiazhuang, 050000, Hebei, People’s Republic of China
  
• 刊物类别：Biomedical and Life Sciences
• 刊物主题：Biomedicine
  Neurosciences
  Biochemistry
  Neurology
  
• 出版者：Springer Netherlands
• ISSN：1573-6903

文摘

Sonic hedgehog (Shh), a secreted glycoprotein factor, can activate the Shh pathway, which has been implicated in neuronal polarization involving neurite outgrowth. However, little evidence is available about the effect of Shh on neurite outgrowth in primary cortical neurons and its potential mechanism. Here, we revealed that Shh increased neurite outgrowth in primary cortical neurons, while the Shh pathway inhibitor (cyclopamine, CPM) partially suppressed Shh-induced neurite outgrowth. Similar results were found for the expressions of Shh and Patched genes in Shh-induced primary cortical neurons. Moreover, Shh increased the levels of brain-derived neurotrophic factor (BDNF) not only in lysates and in culture medium but also in the longest neurites of primary cortical neurons, which was partially blocked by CPM. In addition, blocking of BDNF action suppressed Shh-mediated neurite elongation in primary cortical neurons. In conclusion, these findings suggest that Shh promotes neurite outgrowth in primary cortical neurons at least partially through modulating BDNF expression.