1,256
Views
1
CrossRef citations to date
0
Altmetric
Review

Nucleotide stress responses in neural crest cell fate and melanoma

& ORCID Icon
Pages 1455-1467 | Received 22 Feb 2021, Accepted 20 Jun 2021, Published online: 19 Jul 2021

References

  • Erickson CA, Reedy MV. Neural crest development: the interplay between morphogenesis and cell differentiation. Curr Top Dev Biol. 1998;40:177–209.
  • Meredith P, Sarna T. The physical and chemical properties of eumelanin. Pigment Cell Res. 2006;19(6):572–594.
  • Dupin E, Glavieux C, Vaigot P, et al. Endothelin 3 induces the reversion of melanocytes to glia through a neural crest-derived glial-melanocytic progenitor. Proc Nat Acad Sci. 2000;97(14):7882–7887.
  • White RM, Zon LI. Melanocytes in development, regeneration, and cancer. Cell Stem Cell. 2008;3(3):242–252.
  • Yasumoto K, Yokoyama K, Shibata K, et al. Microphthalmia-associated transcription factor as a regulator for melanocyte-specific transcription of the human tyrosinase gene. Mol Cell Biol. 1994;14(12):8058–8070.
  • Aoki H, Moro O. Involvement of microphthalmia-associated transcription factor (MITF) in expression of human melanocortin-1 receptor (MC1R). Life Sci. 2002;71(18):2171–2179.
  • Du J, Fisher DE. Identification of Aim-1 as the underwhite mouse mutant and its transcriptional regulation by MITF. J Biol Chem. 2002;277(1):402–406.
  • Yasumoto K, Yokoyama K, Takahashi K, et al. Functional analysis of microphthalmia-associated transcription factor in pigment cell-specific transcription of the human tyrosinase family genes. J Biol Chem. 1997;272(1):503–509.
  • McGill GG, Horstmann M, Widlund HR, et al. Bcl2 regulation by the melanocyte master regulator Mitf modulates lineage survival and melanoma cell viability. Cell. 2002;109(6):707–718.
  • Steingrímsson E, Moore KJ, Lamoreux ML, et al. Molecular basis of mouse microphthalmia (mi) mutations helps explain their developmental and phenotypic consequences. Nat Genet. 1994;8(3):256–263.
  • Tassabehji M, Newton VE, Read AP. Waardenburg syndrome type 2 caused by mutations in the human microphthalmia (MITF) gene. Nat Genet. 1994;8(3):251–255.
  • Yasumoto K, Takeda K, Saito H, et al. Microphthalmia-associated transcription factor interacts with LEF-1, a mediator of Wnt signaling. EMBO J. 2002;21(11):2703–2714.
  • Potterf SB, Furumura M, Dunn KJ, et al. Transcription factor hierarchy in Waardenburg syndrome: regulation of MITF expression by SOX10 and PAX3. Hum Genet. 2000;107(1):1–6.
  • Bondurand N, Pingault V, Goerich DE, et al. Interaction among SOX10, PAX3 and MITF, three genes altered in Waardenburg syndrome. Hum Mol Genet. 2000;9(13):1907–1917.
  • Shain AH, Bastian BC. From melanocytes to melanomas. Nat Rev Cancer. 2016;16(6):345–358.
  • Shakhova O, Zingg D, Schaefer SM, et al. Sox10 promotes the formation and maintenance of giant congenital naevi and melanoma. Nat Cell Biol. 2012;14(8):882–890.
  • White RM, Cech J, Ratanasirintrawoot S, et al. DHODH modulates transcriptional elongation in the neural crest and melanoma. Nature. 2011;471(7339):518–522.
  • Omholt K, Platz A, Kanter L, et al. NRAS and BRAF mutations arise early during melanoma pathogenesis and are preserved throughout tumor progression. Clin Cancer Res. 2003;9(17):6483–6488.
  • Wellbrock C, Rana S, Paterson H, et al. Oncogenic BRAF regulates melanoma proliferation through the lineage specific factor MITF. PloS One. 2008;3(7):e2734.
  • Mort RL, Jackson IJ, Patton EE. The melanocyte lineage in development and disease. Development. 2015;142(4):620–632.
  • Zeng Z, Richardson J, Verduzco D, et al. Zebrafish have a competent p53-dependent nucleotide excision repair pathway to resolve ultraviolet B-induced DNA damage in the skin. Zebrafish. 2009;6(4):405–415.
  • Rooijen E, van, Fazio M, Zon LI. From fish bowl to bedside: the power of zebrafish to unravel melanoma pathogenesis and discover new therapeutics. Pigment Cell Melanoma Res. 2017;30(4):402–412.
  • Tsai J, Lee JT, Wang W, et al. Discovery of a selective inhibitor of oncogenic B-Raf kinase with potent antimelanoma activity. Proc Natl Acad Sci U S A. 2008;105(8):3041–3046.
  • Wada T, Takagi T, Yamaguchi Y, et al. DSIF, a novel transcription elongation factor that regulates RNA polymerase II processivity, is composed of human Spt4 and Spt5 homologs. Genes Dev. 1998;12(3):343–356.
  • Valvezan AJ, Turner M, Belaid A, et al. mTORC1 couples nucleotide synthesis to nucleotide demand resulting in a targetable metabolic vulnerability. Cancer Cell. 2017;32(5):624–638.e5.
  • Hubackova S, Davidova E, Boukalova S, et al. Replication and ribosomal stress induced by targeting pyrimidine synthesis and cellular checkpoints suppress p53-deficient tumors. Cell Death Dis. 2020;11(2):110.
  • Fairus AKM, Choudhary B, Hosahalli S, et al. Dihydroorotate dehydrogenase (DHODH) inhibitors affect ATP depletion, endogenous ROS and mediate S-phase arrest in breast cancer cells. Biochimie. 2017;135:154–163.
  • Ladds MJGW, van Leeuwen IMM, Drummond CJ, et al. A DHODH inhibitor increases p53 synthesis and enhances tumor cell killing by p53 degradation blockage. Nat Commun. 2018;9(1):1107.
  • Rainger J, Bengani H, Campbell L, et al. Miller (Genee-Wiedemann) syndrome represents a clinically and biochemically distinct subgroup of postaxial acrofacial dysostosis associated with partial deficiency of DHODH. Hum Mol Genet. 2012;21(18):3969–3983.
  • Ng SB, Buckingham KJ, Lee C, et al. Exome sequencing identifies the cause of a Mendelian disorder. Nat Genet. 2010;42(1):30–35.
  • Guo J, Price DH. RNA polymerase II transcription elongation control. Chem Rev. 2013;113:8583–8603.
  • Gressel S, Schwalb B, Decker TM, et al. CDK9-dependent RNA polymerase II pausing controls transcription initiation. eLife. 2017;6:R106.
  • Adelman K, Lis JT. Promoter-proximal pausing of RNA polymerase II: emerging roles in metazoans. Nat Rev Genet. 2012;13(10):720–731.
  • Sims RJ, Belotserkovskaya R, Reinberg D. Elongation by RNA polymerase II: the short and long of it. Genes Dev. 2004;18(20):2437–2468.
  • Yik JHN, Chen R, Nishimura R, et al. Inhibition of P-TEFb (CDK9/Cyclin T) kinase and RNA polymerase II transcription by the coordinated actions of HEXIM1 and 7SK snRNA. Mol Cell. 2003;12(4):971–982.
  • Tan JL, Fogley R, Flynn R, et al. Stress from nucleotide depletion activates the transcriptional regulator HEXIM1 to suppress melanoma. Mol Cell. 2016;62(1):34–46.
  • Dang CV. c-Myc target genes involved in cell growth, apoptosis, and metabolism. Mol Cell Biol. 1999;19:1–11.
  • Russo A, Russo G. Ribosomal proteins control or bypass p53 during nucleolar stress. Int J Mol Sci. 2017;18(1):140.
  • Zhang Z, Wang H, Li M, et al. Stabilization of E2F1 protein by MDM2 through the E2F1 ubiquitination pathway. Oncogene. 2005;24(48):7238–7247.
  • Riggelen J, Van, Yetil A, Felsher DW. MYC as a regulator of ribosome biogenesis and protein synthesis. Nat Rev Cancer. 2010;10(4):301–309.
  • Dimova DK, Dyson NJ. The E2F transcriptional network: old acquaintances with new faces. Oncogene. 2005;24(17):2810–2826.
  • Adelman K, Kennedy MA, Nechaev S, et al. Immediate mediators of the inflammatory response are poised for gene activation through RNA polymerase II stalling. Proc Natl Acad Sci U S A. 2009;106(43):18207–18212.
  • Aida M, Chen Y, Nakajima K, et al. Transcriptional pausing caused by NELF plays a dual role in regulating immediate-Early expression of the junB gene. Mol Cell Biol. 2006;26(16):6094–6104.
  • Rahl PB, Lin CY, Seila AC, et al. c-Myc regulates transcriptional pause release. Cell. 2010;141(3):432–445.
  • Barboric M, Nissen RM, Kanazawa S, et al. NF-kappaB binds P-TEFb to stimulate transcriptional elongation by RNA polymerase II. Mol Cell. 2001;8(2):327–337.
  • Santoriello C, Sporrij A, Yang S, et al. RNA helicase DDX21 mediates nucleotide stress responses in neural crest and melanoma cells. Nat Cell Biol. 2020;22(4):372–379.
  • Schmidt T, Körner K, Karsunky H, et al. The activity of the murine Bax promoter is regulated by Sp1/3 and E-box binding proteins but not by p53. Cell Death Differ. 1999;6(9):873–882.
  • Ben-Sahra I, Manning BD. mTORC1 signaling and the metabolic control of cell growth. Curr Opin Cell Biol. 2017;45:72–82.
  • Hoxhaj G, Hughes-Hallett J, Timson RC, et al. The mTORC1 signaling network senses changes in cellular purine nucleotide levels. Cell Rep. 2017;21(5):1331–1346.
  • Ben-Sahra I, Howell JJ, Asara JM, et al. Stimulation of de Novo pyrimidine synthesis by growth signaling through mTOR and S6K1. Science. 2013;339(6125):1323–1328.
  • Robitaille AM, Christen S, Shimobayashi M, et al. Quantitative phosphoproteomics reveal mTORC1 Activates de Novo pyrimidine synthesis. Science. 2013;339(6125):1320–1323.
  • Henning D, So RB, Jin R, et al. Silencing of RNA helicase II/Gualpha inhibits mammalian ribosomal RNA production. J Biol Chem. 2003;278(52):52307–52314.
  • Yang H, Zhou J, Ochs RL, et al. Down-regulation of RNA helicase II/Gu results in the depletion of 18 and 28 S rRNAs in Xenopus oocyte. J Biol Chem. 2003;278(40):38847–38859.
  • Westermarck J, Weiss C, Saffrich R, et al. The DEXD/H-box RNA helicase RHII/Gu is a co-factor for c-Jun-activated transcription. EMBO J. 2002;21(3):451–460.
  • Calo E, Flynn RA, Martin L, et al. RNA helicase DDX21 coordinates transcription and ribosomal RNA processing. Nature. 2015;518(7538):249–253.
  • Calo E, Gu B, Bowen ME, et al. Tissue-selective effects of nucleolar stress and rDNA damage in developmental disorders. Nature. 2018;554(7690):112–117.
  • Xing Y-H, Yao R-W, Zhang Y, et al. SLERT regulates DDX21 rings associated with Pol I Transcription. Cell. 2017;169(4):664–678.e16.
  • Kültz D. Evolution of the cellular stress proteome: from monophyletic origin to ubiquitous function. J Exp Biol. 2003;206(18):3119–3124.
  • Weake VM, Workman JL. Inducible gene expression: diverse regulatory mechanisms. Nat Rev Genet. 2010;11(6):426–437.
  • Glass CK, Ogawa S. Combinatorial roles of nuclear receptors in inflammation and immunity. Nat Rev Immunol. 2006;6(1):44–55.
  • Jacobsen BM, Horwitz KB. Progesterone receptors, their isoforms and progesterone regulated transcription. Mol Cell Endocrinol. 2012;357(1–2):18–29.
  • Bertucci PY, Nacht AS, Alló M, et al. Progesterone receptor induces bcl-x expression through intragenic binding sites favoring RNA polymerase II elongation. Nucleic Acids Res. 2013;41(12):6072–6086.
  • Kininis M, Isaacs GD, Core LJ, et al. Postrecruitment regulation of RNA polymerase II directs rapid signaling responses at the promoters of estrogen target genes. Mol Cell Biol. 2009;29(5):1123–1133.
  • Clarke CL, Graham JD. Non-overlapping progesterone receptor cistromes contribute to cell-specific transcriptional outcomes. PloS One. 2012;7(4):e35859.
  • Mohammed H, Russell IA, Stark R, et al. Progesterone receptor modulates ERα action in breast cancer. Nature. 2015;523(7560):313–317.
  • Bamberger AM, Bamberger CM, Gellersen B, et al. Modulation of AP-1 activity by the human progesterone receptor in endometrial adenocarcinoma cells. Proc Nat Acad Sci. 1996;93(12):6169–6174.
  • Bayaa M, Booth RA, Sheng Y, et al. The classical progesterone receptor mediates Xenopus oocyte maturation through a nongenomic mechanism. Proc Nat Acad Sci. 2000;97(23):12607–12612.
  • Migliaccio A, Piccolo D, Castoria G, et al. Activation of the Src/p21ras/Erk pathway by progesterone receptor via cross-talk with estrogen receptor. EMBO J. 1998;17(7):2008–2018.
  • Holmström TH, Mialon A, Kallio M, et al. c-Jun supports ribosomal RNA processing and nucleolar localization of RNA helicase DDX21. J Biol Chem. 2008;283(11):7046–7053.
  • Mialon A, Thastrup J, Kallunki T, et al. Identification of nucleolar effects in JNK-deficient cells. FEBS Lett. 2008;582(20):3145–3151.
  • Bora P, Gahurova L, View ORCID ProfileHauserova A, et al. DDX21 is a p38-MAPK sensitive nucleolar protein necessary for mouse preimplantation embryo development and cell-fate specification. bioRxiv. 2021;4:13.439318, 2021
  • Song C, Hotz-Wagenblatt A, Voit R, et al. SIRT7 and the DEAD-box helicase DDX21 cooperate to resolve genomic R loops and safeguard genome stability. Genes Dev. 2017;31(13):1370–1381.
  • Choudhary C, Kumar C, Gnad F, et al. Lysine acetylation targets protein complexes and co-regulates major cellular functions. Science. 2009;325(5942):834–840.
  • Schölz C, Weinert BT, Wagner SA, et al. Acetylation site specificities of lysine deacetylase inhibitors in human cells. Nat Biotechnol. 2015;33(4):415–423.
  • Kim D-S, Camacho CV, Nagari A, et al. Activation of PARP-1 by snoRNAs controls ribosome biogenesis and cell growth via the RNA helicase DDX21. Mol Cell. 2019;75(6):1270–1285.e14.
  • Johansson JA, Marie KL, Lu Y, et al. PRL3-DDX21 transcriptional control of endolysosomal genes restricts melanocyte stem cell differentiation. Dev Cell. 2020;54(3):317–332.e9.
  • Hanson K, Robinson SD, Al-Yousuf K, et al. The anti-rheumatic drug, leflunomide, synergizes with MEK inhibition to suppress melanoma growth. Oncotarget. 2018;9(3):3815–3829.
  • Cortés H, Reyes-Hernández OD, Alcalá-Alcalá S, et al. Repurposing of drug candidates for treatment of skin cancer. Front Oncol. 2020;10:605714.
  • Christian S, Merz C, Evans L, et al. The novel dihydroorotate dehydrogenase (DHODH) inhibitor BAY 2402234 triggers differentiation and is effective in the treatment of myeloid malignancies. Leukemia. 2019;33(10):2403–2415.

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.