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RBL2 represses the transcriptional activity of Multicilin to inhibit multiciliogenesis – Cell Death & Disease

  • Brooks ER, Wallingford JB. Multiciliated cells. Curr Biol 2014;24:R973–82.

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Hoque M, Kim EN, Chen D, Li FQ, Takemaru KI. Essential Roles of Efferent Duct Multicilia in Male Fertility. Cells 2022;11:341.

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Meunier A, Azimzadeh J. Multiciliated Cells in Animals. Cold Spring Harb Perspect Biol 2016;8:a028233.

    Article 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Li Q, Han Z, Singh N, Terre B, Fame RM, Arif U, et al. Disruption of GMNC-MCIDAS multiciliogenesis program is critical in choroid plexus carcinoma development. Cell Death Differ 2022;29:1596–610.

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Roberson EC, Tran NK, Konjikusic MJ, Fitch RD, Gray RS, Wallingford JB. A comparative study of the turnover of multiciliated cells in the mouse trachea, oviduct, and brain. Dev Dyn 2020;249:898–905.

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Wallmeier J, Dallmayer M, Omran H. The role of cilia for hydrocephalus formation. Am J Med Genet C Semin Med Genet 2022;190:47–56.

    Article 
    PubMed 

    Google Scholar
     

  • Cao Y, Chen M, Dong D, Xie S, Liu M. Environmental pollutants damage airway epithelial cell cilia: Implications for the prevention of obstructive lung diseases. Thorac Cancer 2020;11:505–10.

    Article 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Tilley AE, Walters MS, Shaykhiev R, Crystal RG. Cilia dysfunction in lung disease. Annu Rev Physiol 2015;77:379–406.

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Ancel J, Belgacemi R, Diabasana Z, Perotin JM, Bonnomet A, Dewolf M, et al. Impaired Ciliary Beat Frequency and Ciliogenesis Alteration during Airway Epithelial Cell Differentiation in COPD. Diagnost (Basel) 2021;11:1579.

    Article 

    Google Scholar
     

  • Raidt J, Loges NT, Olbrich H, Wallmeier J, Pennekamp P, Omran H. Primary Ciliary Dyskinesia. Presse Med. 2023:104171.

  • Wilson R. Secondary ciliary dysfunction. Clin Sci (Lond) 1988;75:113–20.

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Armengot M, Milara J, Mata M, Carda C, Cortijo J. Cilia motility and structure in primary and secondary ciliary dyskinesia. Am J Rhinol Allergy 2010;24:175–80.

    Article 
    PubMed 

    Google Scholar
     

  • Gerovac BJ, Valencia M, Baumlin N, Salathe M, Conner GE, Fregien NL. Submersion and hypoxia inhibit ciliated cell differentiation in a notch-dependent manner. Am J Respir Cell Mol Biol 2014;51:516–25.

    Article 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Jorissen M, Willems T. The secondary nature of ciliary (dis)orientation in secondary and primary ciliary dyskinesia. Acta Otolaryngol 2004;124:527–31.

    Article 
    PubMed 

    Google Scholar
     

  • Mao S, Shah AS, Moninger TO, Ostedgaard LS, Lu L, Tang XX, et al. Motile cilia of human airway epithelia contain hedgehog signaling components that mediate noncanonical hedgehog signaling. Proc Natl Acad Sci USA 2018;115:1370–5.

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Breslow DK, Holland AJ. Mechanism and Regulation of Centriole and Cilium Biogenesis. Annu Rev Biochem 2019;88:691–724.

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Ma L, Quigley I, Omran H, Kintner C. Multicilin drives centriole biogenesis via E2f proteins. Genes Dev 2014;28:1461–71.

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Al Jord A, Lemaitre AI, Delgehyr N, Faucourt M, Spassky N, Meunier A. Centriole amplification by mother and daughter centrioles differs in multiciliated cells. Nature 2014;516:104–7.

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Funk MC, Bera AN, Menchen T, Kuales G, Thriene K, Lienkamp SS, et al. Cyclin O (Ccno) functions during deuterosome-mediated centriole amplification of multiciliated cells. EMBO J 2015;34:1078–89.

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Nanjundappa R, Kong D, Shim K, Stearns T, Brody SL, Loncarek J, et al. Regulation of cilia abundance in multiciliated cells. Elife 2019;8:e44039.

    Article 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Rayamajhi D, Roy S. Multiciliated Cells: Rise and Fall of the Deuterosomes. Trends Cell Biol 2020;30:259–62.

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Revinski DR, Zaragosi LE, Boutin C, Ruiz-Garcia S, Deprez M, Thome V, et al. CDC20B is required for deuterosome-mediated centriole production in multiciliated cells. Nat Commun 2018;9:4668.

    Article 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Zhao H, Chen Q, Fang C, Huang Q, Zhou J, Yan X, et al. Parental centrioles are dispensable for deuterosome formation and function during basal body amplification. EMBO Rep. 2019;20:e46735.

    Article 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Kyrousi C, Arbi M, Pilz GA, Pefani DE, Lalioti ME, Ninkovic J, et al. Mcidas and GemC1 are key regulators for the generation of multiciliated ependymal cells in the adult neurogenic niche. Development 2015;142:3661–74.

    CAS 
    PubMed 

    Google Scholar
     

  • Arbi M, Pefani DE, Taraviras S, Lygerou Z. Controlling centriole numbers: Geminin family members as master regulators of centriole amplification and multiciliogenesis. Chromosoma 2018;127:151–74.

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Kyrousi C, Lalioti ME, Skavatsou E, Lygerou Z, Taraviras S. Mcidas and GemC1/Lynkeas specify embryonic radial glial cells. Neurogenesis (Austin) 2016;3:e1172747.

    Article 
    PubMed 

    Google Scholar
     

  • Terre B, Piergiovanni G, Segura-Bayona S, Gil-Gomez G, Youssef SA, Attolini CS, et al. GEMC1 is a critical regulator of multiciliated cell differentiation. EMBO J 2016;35:942–60.

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Lu H, Anujan P, Zhou F, Zhang Y, Chong YL, Bingle CD, et al. Mcidas mutant mice reveal a two-step process for the specification and differentiation of multiciliated cells in mammals. Development 2019;146:dev172643.

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Guiley KZ, Liban TJ, Felthousen JG, Ramanan P, Litovchick L, Rubin SM. Structural mechanisms of DREAM complex assembly and regulation. Genes Dev 2015;29:961–74.

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Balestra FR, Gonczy P. Multiciliogenesis: multicilin directs transcriptional activation of centriole formation. Curr Biol 2014;24:R746–9.

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Boon M, Wallmeier J, Ma L, Loges NT, Jaspers M, Olbrich H, et al. MCIDAS mutations result in a mucociliary clearance disorder with reduced generation of multiple motile cilia. Nat Commun 2014;5:4418.

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Walentek P, Quigley IK, Sun DI, Sajjan UK, Kintner C, Harland RM Ciliary transcription factors and miRNAs precisely regulate Cp110 levels required for ciliary adhesions and ciliogenesis. Elife. 2016;5.

  • Kim S, Ma L, Shokhirev MN, Quigley I, Kintner C. Multicilin and activated E2f4 induce multiciliated cell differentiation in primary fibroblasts. Sci Rep. 2018;8:12369.

    Article 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Hsu J, Sage J. Novel functions for the transcription factor E2F4 in development and disease. Cell Cycle 2016;15:3183–90.

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Henley SA, Dick FA. The retinoblastoma family of proteins and their regulatory functions in the mammalian cell division cycle. Cell Div 2012;7:10.

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Litovchick L, Sadasivam S, Florens L, Zhu X, Swanson SK, Velmurugan S, et al. Evolutionarily conserved multisubunit RBL2/p130 and E2F4 protein complex represses human cell cycle-dependent genes in quiescence. Mol Cell 2007;26:539–51.

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Marshall CB, Mays DJ, Beeler JS, Rosenbluth JM, Boyd KL, Santos Guasch GL, et al. p73 Is Required for Multiciliogenesis and Regulates the Foxj1-Associated Gene Network. Cell Rep. 2016;14:2289–300.

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Treutlein B, Brownfield DG, Wu AR, Neff NF, Mantalas GL, Espinoza FH, et al. Reconstructing lineage hierarchies of the distal lung epithelium using single-cell RNA-seq. Nature 2014;509:371–5.

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Sun A, Bagella L, Tutton S, Romano G, Giordano A. From G0 to S phase: a view of the roles played by the retinoblastoma (Rb) family members in the Rb-E2F pathway. J Cell Biochem 2007;102:1400–4.

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Roufayel R, Mezher R, Storey KB. The Role of Retinoblastoma Protein in Cell Cycle Regulation: An Updated Review. Curr Mol Med 2021;21:620–9.

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Hansen K, Farkas T, Lukas J, Holm K, Ronnstrand L, Bartek J. Phosphorylation-dependent and -independent functions of p130 cooperate to evoke a sustained G1 block. EMBO J 2001;20:422–32.

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Lizcano JM, Deak M, Morrice N, Kieloch A, Hastie CJ, Dong L, et al. Molecular basis for the substrate specificity of NIMA-related kinase-6 (NEK6). Evidence that NEK6 does not phosphorylate the hydrophobic motif of ribosomal S6 protein kinase and serum- and glucocorticoid-induced protein kinase in vivo. J Biol Chem 2002;277:27839–49.

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Litovchick L, Florens LA, Swanson SK, Washburn MP, DeCaprio JA. DYRK1A protein kinase promotes quiescence and senescence through DREAM complex assembly. Genes Dev 2011;25:801–13.

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Tedesco D, Lukas J, Reed SI. The pRb-related protein p130 is regulated by phosphorylation-dependent proteolysis via the protein-ubiquitin ligase SCF(Skp2). Genes Dev 2002;16:2946–57.

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Bhattacharya S, Garriga J, Calbo J, Yong T, Haines DS, Grana X. SKP2 associates with p130 and accelerates p130 ubiquitylation and degradation in human cells. Oncogene 2003;22:2443–51.

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Caillat C, Fish A, Pefani DE, Taraviras S, Lygerou Z, Perrakis A. The structure of the GemC1 coiled coil and its interaction with the Geminin family of coiled-coil proteins. Acta Crystallogr D Biol Crystallogr 2015;71:2278–86.

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Arbi M, Pefani DE, Kyrousi C, Lalioti ME, Kalogeropoulou A, Papanastasiou AD, et al. GemC1 controls multiciliogenesis in the airway epithelium. EMBO Rep. 2016;17:400–13.

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Collins C, Ventrella R, Mitchell BJ. Building a ciliated epithelium: Transcriptional regulation and radial intercalation of multiciliated cells. Curr Top Dev Biol 2021;145:3–39.

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Lewis M, Terre B, Knobel PA, Cheng T, Lu H, Attolini CS, et al. GEMC1 and MCIDAS interactions with SWI/SNF complexes regulate the multiciliated cell-specific transcriptional program. Cell Death Dis 2023;14:201.

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Arvanitis DA, Spandidos DA. Deregulation of the G1/S phase transition in cancer and squamous intraepithelial lesions of the uterine cervix: a case control study. Oncol Rep. 2008;20:751–60.

    CAS 
    PubMed 

    Google Scholar
     

  • Cao L, Peng B, Yao L, Zhang X, Sun K, Yang X, et al. The ancient function of RB-E2F pathway: insights from its evolutionary history. Biol Direct 2010;5:55.

    Article 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Gaubatz S, Lindeman GJ, Ishida S, Jakoi L, Nevins JR, Livingston DM, et al. E2F4 and E2F5 play an essential role in pocket protein-mediated G1 control. Mol Cell 2000;6:729–35.

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Tyagi A, Agarwal C, Agarwal R. The cancer preventive flavonoid silibinin causes hypophosphorylation of Rb/p107 and Rb2/p130 via modulation of cell cycle regulators in human prostate carcinoma DU145 cells. Cell Cycle 2002;1:137–42.

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Lalioti M-E, Arbi M, Loukas I, Kaplani K, Kalogeropoulou A, Lokka G, et al. GemC1 governs multiciliogenesis through direct interaction with and transcriptional regulation of p73. J Cell Sci 2019;132:jcs228684.

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Schwarze F, Meraner J, Lechner M, Loidl A, Stasyk T, Laich A, et al. Cell cycle-dependent acetylation of Rb2/p130 in NIH3T3 cells. Oncogene 2010;29:5755–60.

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Zini N, Trimarchi C, Claudio PP, Stiegler P, Marinelli F, Maltarello MC, et al. pRb2/p130 and p107 control cell growth by multiple strategies and in association with different compartments within the nucleus. J Cell Physiol 2001;189:34–44.

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Fulcher ML, Gabriel S, Burns KA, Yankaskas JR, Randell SH. Well-differentiated human airway epithelial cell cultures. Methods Mol Med 2005;107:183–206.

    CAS 
    PubMed 

    Google Scholar
     

  • Neuberger T, Burton B, Clark H, Van Goor F. Use of primary cultures of human bronchial epithelial cells isolated from cystic fibrosis patients for the pre-clinical testing of CFTR modulators. Methods Mol Biol 2011;741:39–54.

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Chen C, Okayama H. High-efficiency transformation of mammalian cells by plasmid DNA. Mol Cell Biol 1987;7:2745–52.

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Dull T, Zufferey R, Kelly M, Mandel RJ, Nguyen M, Trono D, et al. A Third-Generation Lentivirus Vector with a Conditional Packaging System. J Virol 1998;72:8463–71.

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Salomonis N, Schlieve CR, Pereira L, Wahlquist C, Colas A, Zambon AC, et al. Alternative splicing regulates mouse embryonic stem cell pluripotency and differentiation. Proc Natl Acad Sci 2010;107:10514–9.

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • He L, Diedrich J, Chu YY, Yates JR 3rd. Extracting Accurate Precursor Information for Tandem Mass Spectra by RawConverter. Anal Chem 2015;87:11361–7.

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Xu T, Park SK, Venable JD, Wohlschlegel JA, Diedrich JK, Cociorva D, et al. ProLuCID: An improved SEQUEST-like algorithm with enhanced sensitivity and specificity. J Proteom 2015;129:16–24.

    Article 
    CAS 

    Google Scholar
     

  • Tabb DL, McDonald WH, Yates JR 3rd. DTASelect and Contrast: tools for assembling and comparing protein identifications from shotgun proteomics. J Proteome Res 2002;1:21–6.

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Peng J, Elias JE, Thoreen CC, Licklider LJ, Gygi SP. Evaluation of multidimensional chromatography coupled with tandem mass spectrometry (LC/LC-MS/MS) for large-scale protein analysis: the yeast proteome. J Proteome Res 2003;2:43–50.

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Schindelin J, Arganda-Carreras I, Frise E, Kaynig V, Longair M, Pietzsch T, et al. Fiji: an open-source platform for biological-image analysis. Nat Methods 2012;9:676–82.

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Chen S, Zhou Y, Chen Y, Gu J. fastp: an ultra-fast all-in-one FASTQ preprocessor. Bioinformatics 2018;34:i884–i90.

    Article 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Dobin A, Davis CA, Schlesinger F, Drenkow J, Zaleski C, Jha S, et al. STAR: ultrafast universal RNA-seq aligner. Bioinformatics 2013;29:15–21.

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Liao Y, Smyth GK, Shi W. featureCounts: an efficient general purpose program for assigning sequence reads to genomic features. Bioinformatics 2014;30:923–30.

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Love MI, Huber W, Anders S. Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2. Genome Biol 2014;15:550.

    Article 
    PubMed 
    PubMed Central 

    Google Scholar