YAP signaling in horizontal basal cells promotes the regeneration of olfactory epithelium after injury

Elsevier BV - Tập 17 - Trang 664-677 - 2022
Qian Wu1,2, Xingxing Xu3, Xuemeng Miao1,2, Xiaomei Bao3, Xiuchun Li4, Ludan Xiang2, Wei Wang2, Siyu Du2, Yi Lu2, Xiwu Wang3, Danlu Yang3, Jingjing Zhang3, Xiya Shen3, Fayi Li4, Sheng Lu4, Yiren Fan2, Shujie Xu2, Zihao Chen2, Ying Wang1,5, Honglin Teng4
1School of Pharmacy, Hangzhou Normal University, Hangzhou, Zhejiang 311121, China
2School of Mental Health, Wenzhou Medical University, Wenzhou, Zhejiang 325035, China
3School of Basic Medical Sciences, Wenzhou Medical University, Wenzhou, Zhejiang 325035, China
4Department of Orthopedics (Spine Surgery), The First Affiliated Hospital of Wenzhou Medical University, Wenzhou, Zhejiang 325035, China
5Department of Transfusion Medicine, Zhejiang Provincial People’s Hospital of Hangzhou Medical College, Hangzhou, Zhejiang 310053, China

Tài liệu tham khảo

Akladios, 2017, Epidermal YAP2-5SA-ΔC drives β-catenin activation to promote keratinocyte proliferation in mouse skin in vivo, J. Invest. Dermatol., 137, 716, 10.1016/j.jid.2016.10.029 Andl, 2017, YAP and WWTR1: new targets for skin cancer treatment, Cancer Lett., 396, 30, 10.1016/j.canlet.2017.03.001 Attems, 2015, Olfaction and aging: a mini-review, Gerontology, 61, 485, 10.1159/000381619 Azzolin, 2014, YAP/TAZ incorporation in the β-catenin destruction complex orchestrates the Wnt response, Cell, 158, 157, 10.1016/j.cell.2014.06.013 Bahar-Fuchs, 2010, Olfactory deficits and amyloid-β burden in Alzheimer's disease, mild cognitive impairment, and healthy aging: a PiB PET study, J. Alzheimers Dis., 22, 1081, 10.3233/JAD-2010-100696 Bao, 2020, Sphingosine 1-phosphate promotes the proliferation of olfactory ensheathing cells through YAP signaling and participates in the formation of olfactory nerve layer, Glia, 68, 1757, 10.1002/glia.23803 Carter, 2004, Olfactory horizontal basal cells demonstrate a conserved multipotent progenitor phenotype, J. Neurosci., 24, 5670, 10.1523/JNEUROSCI.0330-04.2004 Chen, 2017, Acute inflammation regulates neuroregeneration through the NF-κB pathway in olfactory epithelium, Proc. Natl. Acad. Sci. U S A, 114, 8089, 10.1073/pnas.1620664114 Chen, 2019, Chronic inflammation directs an olfactory stem cell functional switch from neuroregeneration to immune defense, Cell Stem Cell, 25, 501, 10.1016/j.stem.2019.08.011 Chen, 2014, Wnt-responsive Lgr5⁺ globose basal cells function as multipotent olfactory epithelium progenitor cells, J. Neurosci., 34, 8268, 10.1523/JNEUROSCI.0240-14.2014 Cheng, 2018, S1P stimulates proliferation by upregulating CTGF expression through S1PR2-mediated YAP activation, Mol. Cancer Res., 16, 1543, 10.1158/1541-7786.MCR-17-0681 Choi, 2018, Olfactory epithelium: cells, clinical disorders, and insights from an adult stem cell niche, Laryngoscope Investig. Otolaryngol., 3, 35, 10.1002/lio2.135 Doty, 2018, Age-related deficits in taste and smell, Otolaryngol. Clin. North Am., 51, 815, 10.1016/j.otc.2018.03.014 Ehsanian, 2010, YAP dysregulation by phosphorylation or ΔNp63-mediated gene repression promotes proliferation, survival and migration in head and neck cancer subsets, Oncogene, 29, 6160, 10.1038/onc.2010.339 Elbediwy, 2018, Evolution of mechanotransduction via YAP/TAZ in animal epithelia, Curr. Opin. Cell Biol., 51, 117, 10.1016/j.ceb.2018.02.003 Elbediwy, 2016, Integrin signalling regulates YAP and TAZ to control skin homeostasis, Development, 143, 1674 Fletcher, 2017, Deconstructing olfactory stem cell trajectories at single-cell resolution, Cell Stem Cell, 20, 817, 10.1016/j.stem.2017.04.003 Fletcher, 2011, p63 regulates olfactory stem cell self-renewal and differentiation, Neuron, 72, 748, 10.1016/j.neuron.2011.09.009 Gao, 2014, YAP inhibits squamous transdifferentiation of Lkb1-deficient lung adenocarcinoma through ZEB2-dependent DNp63 repression, Nat. Commun., 5, 4629, 10.1038/ncomms5629 Gregorieff, 2015, Yap-dependent reprogramming of Lgr5(+) stem cells drives intestinal regeneration and cancer, Nature, 526, 715, 10.1038/nature15382 Hageman, 2020, Intestinal regeneration: regulation by the microenvironment, Dev. Cell, 54, 435, 10.1016/j.devcel.2020.07.009 Herrick, 2018, Canonical notch signaling directs the fate of differentiating neurocompetent progenitors in the mammalian olfactory epithelium, J. Neurosci., 38, 5022, 10.1523/JNEUROSCI.0484-17.2018 Herrick, 2017, Notch1 maintains dormancy of olfactory horizontal basal cells, a reserve neural stem cell, Proc. Natl. Acad. Sci. U S A, 114, E5589, 10.1073/pnas.1701333114 Ho, 2019, A novel peptide interfering with proBDNF-sortilin interaction alleviates chronic inflammatory pain, Theranostics, 9, 1651, 10.7150/thno.29703 Holbrook, 1995, An immunochemical, ultrastructural, and developmental characterization of the horizontal basal cells of rat olfactory epithelium, J. Comp. Neurol., 363, 129, 10.1002/cne.903630111 Huang, 2016, YAP stabilizes SMAD1 and promotes BMP2-induced neocortical astrocytic differentiation, Development, 143, 2398, 10.1242/dev.130658 Huard, 1995, Cell cycle of globose basal cells in rat olfactory epithelium, Dev. Dyn., 203, 17, 10.1002/aja.1002030103 Inokuchi, 2017, Nrp2 is sufficient to instruct circuit formation of mitral-cells to mediate odour-induced attractive social responses, Nat. Commun., 8, 15977, 10.1038/ncomms15977 Ito-Ishida, 2018, Genome-wide distribution of linker histone H1.0 is independent of MeCP2, Nat. Neurosci., 21, 794, 10.1038/s41593-018-0155-8 Iwai, 2008, Horizontal basal cells are multipotent progenitors in normal and injured adult olfactory epithelium, Stem Cells, 26, 1298, 10.1634/stemcells.2007-0891 Japtok, 2015, Sphingosine 1-phosphate counteracts insulin signaling in pancreatic β-cells via the sphingosine 1-phosphate receptor subtype 2, Faseb J, 29, 3357, 10.1096/fj.14-263194 Joiner, 2015, Primary cilia on horizontal basal cells regulate regeneration of the olfactory epithelium, J. Neurosci., 35, 13761, 10.1523/JNEUROSCI.1708-15.2015 Kikuta, 2015, Sensory deprivation disrupts homeostatic regeneration of newly generated olfactory sensory neurons after injury in adult mice, J. Neurosci., 35, 2657, 10.1523/JNEUROSCI.2484-14.2015 Kovács, 1999, beta-amyloid deposition and neurofibrillary tangle formation in the olfactory bulb in ageing and Alzheimer's disease, Neuropathol. Appl. Neurobiol., 25, 481, 10.1046/j.1365-2990.1999.00208.x Lee, 2014, YAP and TAZ regulate skin wound healing, J. Invest. Dermatol., 134, 518, 10.1038/jid.2013.339 Leung, 2007, Contribution of olfactory neural stem cells to tissue maintenance and regeneration, Nat. Neurosci., 10, 720, 10.1038/nn1882 Lian, 2010, The role of YAP transcription coactivator in regulating stem cell self-renewal and differentiation, Genes Dev., 24, 1106, 10.1101/gad.1903310 Liu, 2018, Sphingosine-1-phosphate induces airway smooth muscle cell proliferation, migration, and contraction by modulating Hippo signaling effector YAP, Am. J. Physiol. Lung Cell Mol. Physiol., 315, L609, 10.1152/ajplung.00554.2017 Mendoza-Reinoso, 2018, Epidermal YAP activity drives canonical WNT16/β-catenin signaling to promote keratinocyte proliferation in vitro and in the murine skin, Stem Cell Res., 29, 15, 10.1016/j.scr.2018.03.005 Moya, 2019, Hippo-YAP/TAZ signalling in organ regeneration and regenerative medicine, Nat. Rev. Mol. Cell Biol., 20, 211, 10.1038/s41580-018-0086-y Ogawa, 2014, Valproic acid promotes neural regeneration of olfactory epithelium in adult mice after methimazole-induced damage, Am. J. Rhinol. Allergy, 28, e95, 10.2500/ajra.2014.28.4027 Packard, 2011, DeltaNp63 regulates stem cell dynamics in the mammalian olfactory epithelium, J. Neurosci., 31, 8748, 10.1523/JNEUROSCI.0681-11.2011 Peterson, 2019, Activating a reserve neural stem cell population in vitro enables engraftment and multipotency after transplantation, Stem Cell Rep., 12, 680, 10.1016/j.stemcr.2019.02.014 Rognoni, 2019, The roles of YAP/TAZ and the Hippo pathway in healthy and diseased skin, Cells, 8, 411, 10.3390/cells8050411 Roviezzo, 2015, S1P-induced airway smooth muscle hyperresponsiveness and lung inflammation in vivo: molecular and cellular mechanisms, Br. J. Pharmacol., 172, 1882, 10.1111/bph.13033 Saladi, 2017, ACTL6A is co-amplified with p63 in squamous cell carcinoma to drive YAP activation, regenerative proliferation, and poor prognosis, Cancer Cell, 31, 35, 10.1016/j.ccell.2016.12.001 Schlegelmilch, 2011, Yap1 acts downstream of α-catenin to control epidermal proliferation, Cell, 144, 782, 10.1016/j.cell.2011.02.031 Schnittke, 2015, Transcription factor p63 controls the reserve status but not the stemness of horizontal basal cells in the olfactory epithelium, Proc. Natl. Acad. Sci. U S A, 112, E5068, 10.1073/pnas.1512272112 Schwob, 2017, Stem and progenitor cells of the mammalian olfactory epithelium: taking poietic license, J. Comp. Neurol., 525, 1034, 10.1002/cne.24105 Schwob, 1995, Reconstitution of the rat olfactory epithelium after methyl bromide-induced lesion, J. Comp. Neurol., 359, 15, 10.1002/cne.903590103 Taniguchi, 2015, A gp130-Src-YAP module links inflammation to epithelial regeneration, Nature, 519, 57, 10.1038/nature14228 Tukijan, 2018, The signalling roles of sphingosine-1-phosphate derived from red blood cells and platelets, Br. J. Pharmacol., 175, 3741, 10.1111/bph.14451 Wu, 2013, Amyloid-β deposition and olfactory dysfunction in an Alzheimer's disease model, J. Alzheimers Dis., 37, 699, 10.3233/JAD-122443 Xie, 2020, Astrocytic YAP promotes the formation of glia scars and neural regeneration after spinal cord injury, J. Neurosci., 40, 2644, 10.1523/JNEUROSCI.2229-19.2020 Yan, 2015, NF-κB-induced microRNA-31 promotes epidermal hyperplasia by repressing protein phosphatase 6 in psoriasis, Nat. Commun., 6, 7652, 10.1038/ncomms8652 Yao, 2014, BMP2-SMAD signaling represses the proliferation of embryonic neural stem cells through YAP, J. Neurosci., 34, 12039, 10.1523/JNEUROSCI.0486-14.2014 Yoo, 2017, Differential spatial expression of peripheral olfactory neuron-derived BACE1 induces olfactory impairment by region-specific accumulation of β-amyloid oligomer, Cell Death Dis., 8, e2977, 10.1038/cddis.2017.349 Yu, 2012, Regulation of the Hippo-YAP pathway by G-protein-coupled receptor signaling, Cell, 150, 780, 10.1016/j.cell.2012.06.037 Yu, 2016, Myocardin-related transcription factor A and yes-associated protein exert dual control in G protein-coupled receptor- and RhoA-mediated transcriptional regulation and cell proliferation, Mol. Cell Biol., 36, 39, 10.1128/MCB.00772-15 Zhang, 2021, Severe acute respiratory syndrome coronavirus 2 infects and damages the mature and immature olfactory sensory neurons of hamsters, Clin. Infect. Dis., 73, e503, 10.1093/cid/ciaa995 Zhang, 2014, Downstream of mutant KRAS, the transcription regulator YAP is essential for neoplastic progression to pancreatic ductal adenocarcinoma, Sci. Signal, 7, ra42, 10.1126/scisignal.2005049 Zhao, 2014, Yap tunes airway epithelial size and architecture by regulating the identity, maintenance, and self-renewal of stem cells, Dev. Cell, 30, 151, 10.1016/j.devcel.2014.06.004