Induction of HoxB Transcription by Retinoic Acid Requires Actin Polymerization

Overview

Journal Mol Biol Cell

Specialties Cell Biology
Molecular Biology

Date 2009 May 30

PMID 19477923

Citations 28

Authors

Carmelo Ferrai

Gabriela Naum-Ongania

Elena Longobardi

Martina Palazzolo

Andrea Disanza

Victor M Diaz

Massimo P Crippa

Giorgio Scita

Francesco Blasi

Affiliations

Soon will be listed here.

Abstract

We have analyzed the role of actin polymerization in retinoic acid (RA)-induced HoxB transcription, which is mediated by the HoxB regulator Prep1. RA induction of the HoxB genes can be prevented by the inhibition of actin polymerization. Importantly, inhibition of actin polymerization specifically affects the transcription of inducible Hox genes, but not that of their transcriptional regulators, the RARs, nor of constitutively expressed, nor of actively transcribed Hox genes. RA treatment induces the recruitment to the HoxB2 gene enhancer of a complex composed of "elongating" RNAPII, Prep1, beta-actin, and N-WASP as well as the accessory splicing components p54Nrb and PSF. We show that inhibition of actin polymerization prevents such recruitment. We conclude that inducible Hox genes are selectively sensitive to the inhibition of actin polymerization and that actin polymerization is required for the assembly of a transcription complex on the regulatory region of the Hox genes.

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References

Ferrai C, Munari D, Luraghi P, Pecciarini L, Cangi M, Doglioni C . A transcription-dependent micrococcal nuclease-resistant fragment of the urokinase-type plasminogen activator promoter interacts with the enhancer. J Biol Chem. 2007; 282(17):12537-46. DOI: 10.1074/jbc.M700867200. View

Pantaloni D, Boujemaa R, Didry D, Gounon P, Carlier M . The Arp2/3 complex branches filament barbed ends: functional antagonism with capping proteins. Nat Cell Biol. 2000; 2(7):385-91. DOI: 10.1038/35017011. View

Berthelsen J, Zappavigna V, Ferretti E, Mavilio F, Blasi F . The novel homeoprotein Prep1 modulates Pbx-Hox protein cooperativity. EMBO J. 1998; 17(5):1434-45. PMC: 1170491. DOI: 10.1093/emboj/17.5.1434. View

Simeone A, Acampora D, Arcioni L, Andrews P, Boncinelli E, Mavilio F . Sequential activation of HOX2 homeobox genes by retinoic acid in human embryonal carcinoma cells. Nature. 1990; 346(6286):763-6. DOI: 10.1038/346763a0. View

Diaz V, Mori S, Longobardi E, Menendez G, Ferrai C, Keough R . p160 Myb-binding protein interacts with Prep1 and inhibits its transcriptional activity. Mol Cell Biol. 2007; 27(22):7981-90. PMC: 2169149. DOI: 10.1128/MCB.01290-07. View

Di Rosa P, Villaescusa J, Longobardi E, Iotti G, Ferretti E, Diaz V . The homeodomain transcription factor Prep1 (pKnox1) is required for hematopoietic stem and progenitor cell activity. Dev Biol. 2007; 311(2):324-34. DOI: 10.1016/j.ydbio.2007.08.031. View

Philimonenko V, Zhao J, Iben S, Dingova H, Kysela K, Kahle M . Nuclear actin and myosin I are required for RNA polymerase I transcription. Nat Cell Biol. 2004; 6(12):1165-72. DOI: 10.1038/ncb1190. View

Gould A, Itasaki N, Krumlauf R . Initiation of rhombomeric Hoxb4 expression requires induction by somites and a retinoid pathway. Neuron. 1998; 21(1):39-51. DOI: 10.1016/s0896-6273(00)80513-9. View

Ye J, Zhao J, Hoffmann-Rohrer U, Grummt I . Nuclear myosin I acts in concert with polymeric actin to drive RNA polymerase I transcription. Genes Dev. 2008; 22(3):322-30. PMC: 2216692. DOI: 10.1101/gad.455908. View

10.

Huang D, Chen S, Gudas L . Analysis of two distinct retinoic acid response elements in the homeobox gene Hoxb1 in transgenic mice. Dev Dyn. 2002; 223(3):353-70. DOI: 10.1002/dvdy.10057. View

11.

Percipalle P, Visa N . Molecular functions of nuclear actin in transcription. J Cell Biol. 2006; 172(7):967-71. PMC: 2063754. DOI: 10.1083/jcb.200512083. View

12.

Kukalev A, Nord Y, Palmberg C, Bergman T, Percipalle P . Actin and hnRNP U cooperate for productive transcription by RNA polymerase II. Nat Struct Mol Biol. 2005; 12(3):238-44. DOI: 10.1038/nsmb904. View

13.

Olave I, Reck-Peterson S, Crabtree G . Nuclear actin and actin-related proteins in chromatin remodeling. Annu Rev Biochem. 2002; 71:755-81. DOI: 10.1146/annurev.biochem.71.110601.135507. View

14.

Bettinger B, Gilbert D, Amberg D . Actin up in the nucleus. Nat Rev Mol Cell Biol. 2004; 5(5):410-5. DOI: 10.1038/nrm1370. View

15.

Marshall H, Morrison A, Studer M, Popperl H, Krumlauf R . Retinoids and Hox genes. FASEB J. 1996; 10(9):969-78. View

16.

Ferretti E, Villaescusa J, Di Rosa P, Fernandez-Diaz L, Longobardi E, Mazzieri R . Hypomorphic mutation of the TALE gene Prep1 (pKnox1) causes a major reduction of Pbx and Meis proteins and a pleiotropic embryonic phenotype. Mol Cell Biol. 2006; 26(15):5650-62. PMC: 1592771. DOI: 10.1128/MCB.00313-06. View

17.

Waskiewicz A, Rikhof H, Moens C . Eliminating zebrafish pbx proteins reveals a hindbrain ground state. Dev Cell. 2002; 3(5):723-33. DOI: 10.1016/s1534-5807(02)00319-2. View

18.

Pantaloni D, Le Clainche C, Carlier M . Mechanism of actin-based motility. Science. 2001; 292(5521):1502-6. DOI: 10.1126/science.1059975. View

19.

Egly J, Miyamoto N, Moncollin V, Chambon P . Is actin a transcription initiation factor for RNA polymerase B?. EMBO J. 1984; 3(10):2363-71. PMC: 557695. DOI: 10.1002/j.1460-2075.1984.tb02141.x. View

20.

McDonald D, Carrero G, Andrin C, de Vries G, Hendzel M . Nucleoplasmic beta-actin exists in a dynamic equilibrium between low-mobility polymeric species and rapidly diffusing populations. J Cell Biol. 2006; 172(4):541-52. PMC: 2063674. DOI: 10.1083/jcb.200507101. View