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YAP is required for prostate development, regeneration, and prostate stem cell function – Cell Death Discovery

  • Siegel RL, Miller KD, Jemal A. Cancer statistics, 2019. CA Cancer J Clin. 2019;69:7–34.

    Article  PubMed  Google Scholar 

  • Attard G, Parker C, Eeles RA, Schroder F, Tomlins SA, Tannock I, et al. Prostate cancer. Lancet. 2016;387:70–82.

    Article  PubMed  Google Scholar 

  • Shen MM, Abate-Shen C. Molecular genetics of prostate cancer: new prospects for old challenges. Genes Dev. 2010;24:1967–2000.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Pierce GB, Speers WC. Tumors as caricatures of the process of tissue renewal: prospects for therapy by directing differentiation. Cancer Res. 1988;48:1996–2004.

    CAS  PubMed  Google Scholar 

  • Pritchard C, Mecham B, Dumpit R, Coleman I, Bhattacharjee M, Chen Q, et al. Conserved gene expression programs integrate mammalian prostate development and tumorigenesis. Cancer Res. 2009;69:1739–47.

    Article  CAS  PubMed  Google Scholar 

  • Schaeffer EM, Marchionni L, Huang Z, Simons B, Blackman A, Yu W, et al. Androgen-induced programs for prostate epithelial growth and invasion arise in embryogenesis and are reactivated in cancer. Oncogene. 2008;27:7180–91.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kasper S. Exploring the origins of the normal prostate and prostate cancer stem cell. Stem Cell Rev. 2008;4:193–201.

    Article  CAS  PubMed  Google Scholar 

  • Matusik RJ, Jin RJ, Sun Q, Wang Y, Yu X, Gupta A, et al. Prostate epithelial cell fate. Differentiation. 2008;76:682–98.

    Article  CAS  PubMed  Google Scholar 

  • Sugimura Y, Cunha GR, Donjacour AA. Morphogenesis of ductal networks in the mouse prostate. Biol Reprod. 1986;34:961–71.

    Article  CAS  PubMed  Google Scholar 

  • Prins GS, Putz O. Molecular signaling pathways that regulate prostate gland development. Differentiation. 2008;76:641–59.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ousset M, Van Keymeulen A, Bouvencourt G, Sharma N, Achouri Y, Simons BD, et al. Multipotent and unipotent progenitors contribute to prostate postnatal development. Nat Cell Biol. 2012;14:1131–8.

    Article  CAS  PubMed  Google Scholar 

  • Choi N, Zhang B, Zhang L, Ittmann M, Xin L. Adult murine prostate basal and luminal cells are self-sustained lineages that can both serve as targets for prostate cancer initiation. Cancer Cell. 2012;21:253–65.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Goldstein AS, Lawson DA, Cheng D, Sun W, Garraway IP, Witte ON. Trop2 identifies a subpopulation of murine and human prostate basal cells with stem cell characteristics. Proc Natl Acad Sci USA. 2008;105:20882–7.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lawson DA, Zong Y, Memarzadeh S, Xin L, Huang J, Witte ON. Basal epithelial stem cells are efficient targets for prostate cancer initiation. Proc Natl Acad Sci USA. 2010;107:2610–5.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Luo W, Rodriguez M, Valdez JM, Zhu X, Tan K, Li D, et al. Lgr4 is a key regulator of prostate development and prostate stem cell differentiation. Stem Cells. 2013;31:2492–505.

    Article  CAS  PubMed  Google Scholar 

  • Mimeault M, Mehta PP, Hauke R, Batra SK. Functions of normal and malignant prostatic stem/progenitor cells in tissue regeneration and cancer progression and novel targeting therapies. Endocr Rev. 2008;29:234–52.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Karthaus WR, Hofree M, Choi D, Linton EL, Turkekul M, Bejnood A, et al. Regenerative potential of prostate luminal cells revealed by single-cell analysis. Science. 2020;368:497–505.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Guo W, Li L, He J, Liu Z, Han M, Li F, et al. Single-cell transcriptomics identifies a distinct luminal progenitor cell type in distal prostate invagination tips. Nat Genet. 2020;52:908–18.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Piccolo S, Dupont S, Cordenonsi M. The biology of YAP/TAZ: hippo signaling and beyond. Physiol Rev. 2014;94:1287–312.

    Article  CAS  PubMed  Google Scholar 

  • Maugeri-Sacca M, De Maria R. The Hippo pathway in normal development and cancer. Pharm Ther. 2018;186:60–72.

    Article  CAS  Google Scholar 

  • Harvey KF, Pfleger CM, Hariharan IK. The Drosophila Mst ortholog, hippo, restricts growth and cell proliferation and promotes apoptosis. Cell. 2003;114:457–67.

    Article  CAS  PubMed  Google Scholar 

  • Huang J, Wu S, Barrera J, Matthews K, Pan D. The Hippo signaling pathway coordinately regulates cell proliferation and apoptosis by inactivating Yorkie, the Drosophila Homolog of YAP. Cell. 2005;122:421–34.

    Article  CAS  PubMed  Google Scholar 

  • Lai Z-C, Wei X, Shimizu T, Ramos E, Rohrbaugh M, Nikolaidis N, et al. Control of cell proliferation and apoptosis by mob as tumor suppressor, mats. Cell. 2005;120:675–85.

    Article  CAS  PubMed  Google Scholar 

  • Morin-Kensicki EM, Boone BN, Howell M, Stonebraker JR, Teed J, Alb JG, et al. Defects in yolk sac vasculogenesis, chorioallantoic fusion, and embryonic axis elongation in mice with targeted disruption of Yap65. Mol Cell Biol. 2006;26:77–87.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lian I, Kim J, Okazawa H, Zhao J, Zhao B, Yu J, et al. The role of YAP transcription coactivator in regulating stem cell self-renewal and differentiation. Genes Dev. 2010;24:1106–18.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Camargo FD, Gokhale S, Johnnidis JB, Fu D, Bell GW, Jaenisch R, et al. YAP1 increases organ size and expands undifferentiated progenitor cells. Curr Biol. 2007;17:2054–60.

    Article  CAS  PubMed  Google Scholar 

  • Zhu L, Gibson P, Currle DS, Tong Y, Richardson RJ, Bayazitov IT, et al. Prominin 1 marks intestinal stem cells that are susceptible to neoplastic transformation. Nature. 2009;457:603–7.

    Article  CAS  PubMed  Google Scholar 

  • Yin AH, Miraglia S, Zanjani ED, Almeida-Porada G, Ogawa M, Leary AG, et al. AC133, a novel marker for human hematopoietic stem and progenitor cells. Blood. 1997;90:5002–12.

    Article  CAS  PubMed  Google Scholar 

  • Mizrak D, Brittan M, Alison M. CD133: molecule of the moment. J Pathol. 2008;214:3–9.

    Article  CAS  PubMed  Google Scholar 

  • Maitland NJ, Collins AT. Prostate cancer stem cells: a new target for therapy. J Clin Oncol. 2008;26:2862–70.

    Article  PubMed  Google Scholar 

  • Missol‐Kolka E, Karbanová J, Janich P, Haase M, Fargeas CA, Huttner WB, et al. Prominin-1 (CD133) is not restricted to stem cells located in the basal compartment of murine and human prostate. Prostate. 2011;71:254–67.

    Article  PubMed  Google Scholar 

  • Lai KP, Yamashita S, Vitkus S, Shyr CR, Yeh S, Chang C. Suppressed prostate epithelial development with impaired branching morphogenesis in mice lacking stromal fibromuscular androgen receptor. Mol Endocrinol. 2012;26:52–66.

    Article  CAS  PubMed  Google Scholar 

  • Marker PC, Donjacour AA, Dahiya R, Cunha GR. Hormonal, cellular, and molecular control of prostatic development. Dev Biol. 2003;253:165–74.

    Article  CAS  PubMed  Google Scholar 

  • Toivanen R, Shen MM. Prostate organogenesis: tissue induction, hormonal regulation and cell type specification. Development. 2017;144:1382–98.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • English HF, Santen RJ, Isaacs JT. Response of glandular versus basal rat ventral prostatic epithelial cells to androgen withdrawal and replacement. Prostate. 1987;11:229–42.

    Article  CAS  PubMed  Google Scholar 

  • Zanconato F, Cordenonsi M, Piccolo S. YAP/TAZ at the roots of cancer. Cancer Cell. 2016;29:783–803.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Galli GG, Carrara M, Yuan W-C, Valdes-Quezada C, Gurung B, Pepe-Mooney B, et al. YAP drives growth by controlling transcriptional pause release from dynamic enhancers. Mol Cell. 2015;60:328–37.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Dong J, Feldmann G, Huang J, Wu S, Zhang N, Comerford SA, et al. Elucidation of a universal size-control mechanism in Drosophila and mammals. Cell. 2007;130:1120–33.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhang N, Bai H, David KK, Dong J, Zheng Y, Cai J, et al. The Merlin/NF2 tumor suppressor functions through the YAP oncoprotein to regulate tissue homeostasis in mammals. Dev Cell. 2010;19:27–38.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • von Gise A, Lin Z, Schlegelmilch K, Honor LB, Pan GM, Buck JN, et al. YAP1, the nuclear target of Hippo signaling, stimulates heart growth through cardiomyocyte proliferation but not hypertrophy. Proc Natl Acad Sci USA. 2012;109:2394–9.

    Article  Google Scholar 

  • Heallen T, Zhang M, Wang J, Bonilla-Claudio M, Klysik E, Johnson RL, et al. Hippo pathway inhibits Wnt signaling to restrain cardiomyocyte proliferation and heart size. Science. 2011;332:458–61.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Xin M, Kim Y, Sutherland LB, Murakami M, Qi X, McAnally J, et al. Hippo pathway effector Yap promotes cardiac regeneration. Proc Natl Acad Sci USA. 2013;110:13839–44.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cai J, Zhang N, Zheng Y, De Wilde RF, Maitra A, Pan D. The Hippo signaling pathway restricts the oncogenic potential of an intestinal regeneration program. Genes Dev. 2010;24:2383–8.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hayashi S, McMahon AP. Efficient recombination in diverse tissues by a tamoxifen-inducible form of Cre: a tool for temporally regulated gene activation/inactivation in the mouse. Dev Biol. 2002;244:305–18.

    Article  CAS  PubMed  Google Scholar 

  • Metzger D, Clifford J, Chiba H, Chambon P. Conditional site-specific recombination in mammalian cells using a ligand-dependent chimeric Cre recombinase. Proc Natl Acad Sci USA. 1995;92:6991–5.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cunha G, Chung L. Stromal-epithelial interactions—I. Induction of prostatic phenotype in urothelium of testicular feminized (Tfm/y) mice. J Steroid Biochem. 1981;14:1317–24.

    Article  CAS  PubMed  Google Scholar 

  • Prins GS, Chang WY, Wang Y, van Breemen RB. Retinoic acid receptors and retinoids are up-regulated in the developing and adult rat prostate by neonatal estrogen exposure. Endocrinology. 2002;143:3628–40.

    Article  CAS  PubMed  Google Scholar 

  • Prins GS, Birch L. Neonatal estrogen exposure up-regulates estrogen receptor expression in the developing and adult rat prostate lobes. Endocrinology. 1997;138:1801–9.

    Article  CAS  PubMed  Google Scholar 

  • Bhatia-Gaur R, Donjacour AA, Sciavolino PJ, Kim M, Desai N, Young P, et al. Roles for Nkx3. 1 in prostate development and cancer. Genes Dev. 1999;13:966–77.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Economides KD, Capecchi MR. Hoxb13 is required for normal differentiation and secretory function of the ventral prostate. Development. 2003;130:2061–9.

    Article  CAS  PubMed  Google Scholar 

  • Gao N, Ishii K, Mirosevich J, Kuwajima S, Oppenheimer SR, Roberts RL, et al. Forkhead box A1 regulates prostate ductal morphogenesis and promotes epithelial cell maturation. Development. 2005;132:3431–43.

    Article  CAS  PubMed  Google Scholar 

  • Kwon OJ, Valdez JM, Zhang L, Zhang B, Wei X, Su Q, et al. Increased Notch signalling inhibits anoikis and stimulates proliferation of prostate luminal epithelial cells. Nat Commun. 2014;5:4416.

    Article  CAS  PubMed  Google Scholar 

  • Valdez JM, Zhang L, Su Q, Dakhova O, Zhang Y, Shahi P, et al. Notch and TGFβ form a reciprocal positive regulatory loop that suppresses murine prostate basal stem/progenitor cell activity. Cell Stem Cell. 2012;11:676–88.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wang X-D, Leow CC, Zha J, Tang Z, Modrusan Z, Radtke F, et al. Notch signaling is required for normal prostatic epithelial cell proliferation and differentiation. Dec Biol. 2006;290:66–80.

    Article  CAS  Google Scholar 

  • Dalrymple S, Antony L, Xu Y, Uzgare AR, Arnold JT, Savaugeot J, et al. Role of notch-1 and E-cadherin in the differential response to calcium in culturing normal versus malignant prostate cells. Cancer Res. 2005;65:9269–79.

    Article  CAS  PubMed  Google Scholar 

  • Shahi P, Seethammagari MR, Valdez JM, Xin L, Spencer DM. Wnt and Notch pathways have interrelated opposing roles on prostate progenitor cell proliferation and differentiation. Stem Cells. 2011;29:678–88.

    Article  CAS  PubMed  Google Scholar 

  • Li Q, Alsaidan OA, Rai S, Wu M, Shen H, Beharry Z, et al. Stromal Gli signaling regulates the activity and differentiation of prostate stem and progenitor cells. J Biol Chem. 2018;293:10547–60.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Olson AW, Le V, Wang J, Hiroto A, Kim WK, Lee DH, et al. Stromal androgen and hedgehog signaling regulates stem cell niches in pubertal prostate development. Development. 2021;148:dev199738.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jiang N, Hjorth-Jensen K, Hekmat O, Iglesias-Gato D, Kruse T, Wang C, et al. In vivo quantitative phosphoproteomic profiling identifies novel regulators of castration-resistant prostate cancer growth. Oncogene. 2015;34:2764–76.

    Article  CAS  PubMed  Google Scholar 

  • Nguyen LT, Tretiakova MS, Silvis MR, Lucas J, Klezovitch O, Coleman I, et al. ERG activates the YAP1 transcriptional program and induces the development of age-related prostate tumors. Cancer Cell. 2015;27:797–808.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kuser-Abali G, Alptekin A, Lewis M, Garraway IP, Cinar B. YAP1 and AR interactions contribute to the switch from androgen-dependent to castration-resistant growth in prostate cancer. Nat Commun. 2015;6:8126.

    Article  PubMed  Google Scholar 

  • Lee HC, Ou CH, Huang YC, Hou PC, Creighton CJ, Lin YS, et al. YAP1 overexpression contributes to the development of enzalutamide resistance by induction of cancer stemness and lipid metabolism in prostate cancer. Oncogene. 2021;40:2407–21.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Xin L, Ide H, Kim Y, Dubey P, Witte ON. In vivo regeneration of murine prostate from dissociated cell populations of postnatal epithelia and urogenital sinus mesenchyme. Proc Natl Acad Sci USA. 2003;100:11896–903.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lukacs RU, Goldstein AS, Lawson DA, Cheng D, Witte ON. Isolation, cultivation and characterization of adult murine prostate stem cells. Nat Protoc. 2010;5:702–13.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Xin L, Lukacs RU, Lawson DA, Cheng D, Witte ON. Self-renewal and multilineage differentiation in vitro from murine prostate stem cells. Stem Cells. 2007;25:2760–9.

    Article  CAS  PubMed  Google Scholar