Induction of HoxB transcription by retinoic acid requires actin polymerization

Molecular Biology of the Cell

Volumn 20, Issue 15, 2009, Pages 3543-3551

  Ferrai, Carmelo ^a,c   Naum Onganía, Gabriela ^b,d   Longobardi, Elena ^b   Palazzolo, Martina ^a   Disanza, Andrea ^b   Diaz, Victor M ^a   Crippa, Massimo P ^a   Scita, Giorgio ^b   Blasi, Francesco ^a,b  

^a VITA SALUTE SAN RAFFAELE UNIVERSITY   (Italy)

^b FIRC INSTITUTE OF MOLECULAR ONCOLOGY   (Italy)

^c IMPERIAL COLLEGE SCHOOL OF MEDICINE   (United Kingdom)

^d Ctro Reg de Estud Genomicos   (Argentina)

Author keywords

[No Author keywords available]

Indexed keywords

BETA ACTIN; HOX PROTEIN; HOXB PROTEIN; NEURAL WISKOTT ALDRICH SYNDROME PROTEIN; RETINOIC ACID; RETINOIC ACID RECEPTOR; RNA POLYMERASE II; UNCLASSIFIED DRUG;

ACTIN POLYMERIZATION; ARTICLE; CARBOXY TERMINAL SEQUENCE; CONTROLLED STUDY; ENHANCER REGION; GENE INDUCTION; GENETIC TRANSCRIPTION; HUMAN; HUMAN CELL; PRIORITY JOURNAL; PROTEIN EXPRESSION; RNA SPLICING; TRANSCRIPTION REGULATION;

ACTINS; ANTINEOPLASTIC AGENTS; CELL LINE, TUMOR; CYTOCHALASIN D; DOWN-REGULATION; HOMEODOMAIN PROTEINS; HUMANS; IMMUNOBLOTTING; MUTATION; NUCLEAR MATRIX-ASSOCIATED PROTEINS; NUCLEIC ACID SYNTHESIS INHIBITORS; OCTAMER TRANSCRIPTION FACTORS; POLYMERS; RECEPTORS, RETINOIC ACID; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA INTERFERENCE; RNA POLYMERASE II; RNA, MESSENGER; RNA-BINDING PROTEINS; TRANSCRIPTION FACTORS; TRANSCRIPTION, GENETIC; TRETINOIN; WISKOTT-ALDRICH SYNDROME PROTEIN, NEURONAL;

EID: 68149142653     PISSN: 10591524     EISSN: None     Source Type: Journal    
DOI: 10.1091/mbc.E09-02-0114     Document Type: Article

References (52)

1. Berthelsen, J., Zappavigna, V., Ferretti, E., Mavilio, F., and Blasi, F. (1998). The novel homeoprotein Prep1 modulates Pbx-Hox protein cooperativity. EMBO J. 17, 1434-1445. (Pubitemid 28105522)
2. Bettinger, B. T., Gilbert, D. M., and Amberg, D. C. (2004). Actin up in the nucleus. Nat. Rev. Mol. Cell. Biol. 5, 410-415.
3. Chuang, C. H., Carpenter, A. E., Fuchsova, B., Johnson, T., de Lanerolle, P., and Belmont, A. S. (2006). Long-range directional movement of an interphase chromosome site. Curr. Biol. 16, 825-831.
4. Core, L. J., and Lis, J. T. (2008). Transcription regulation through promoterproximal pausing of RNA polymerase II. Science 319, 1791-1792.
5. Deflorian, G., Tiso, N., Ferretti, E., Meyer, D., Blasi, F., Bortolussi, M., and Argenton, F. (2004). Prep1.1 has essential genetic functions in hindbrain development and cranial neural crest cell differentiation. Development 131, 613-627. (Pubitemid 38240004)
6. Di Rosa, P., Villaescusa, J. C., Longobardi, E., Iotti, G., Ferretti, E., Diaz, V. M., Miccio, A., Ferrari, G., and Blasi, F. (2007). The homeodomain transcription factor Prep1 (pKnox1) is required for hematopoietic stem and progenitor cell activity. Dev. Biol. 311, 324-334.
7. Diaz, V. M., Bachi, A., and Blasi, F. (2007a). Purification of the Prep1 interactome identifies novel pathways regulated by Prep1. Proteomics 7, 2617-2623. (Pubitemid 47253820)
8. Diaz, V. M., Mori, S., Longobardi, E., Menendez, G., Ferrai, C., Keough, R. A., Bachi, A., and Blasi, F. (2007b). p160 Myb-binding protein interacts with Prep1 and inhibits its transcriptional activity. Mol. Cell. Biol. 27, 7981-7990.
9. Dignam, J. D., Lebovitz, R. M., and Roeder, R. G. (1983). Accurate transcription initiation by RNA polymerase II in a soluble extract from isolated mammalian nuclei. Nucleic Acids Res. 11, 1475-1489.
10. Disanza, A., et al. (2006). Regulation of cell shape by Cdc42 is mediated by the synergic actin-bundling activity of the Eps8-IRSp53 complex. Nat. Cell Biol. 8, 1337-1347.
11. Dundr, M., Ospina, J. K., Sung, M. H., John, S., Upender, M., Ried, T., Hager, G. L., and Matera, A. G. (2007). Actin-dependent intranuclear repositioning of an active gene locus in vivo. J. Cell Biol. 179, 1095-1103. (Pubitemid 350277729)
12. Dupe, V., Ghyselinck, N. B., Wendling, O., Chambon, P., and Mark, M. (1999). Key roles of retinoic acid receptors alpha and beta in the patterning of the caudal hindbrain, pharyngeal arches and otocyst in the mouse. Development 126, 5051-5059. (Pubitemid 30000418)
13. Egly, J. M., Miyamoto, N. G., Moncollin, V., and Chambon, P. (1984). Is actin a transcription initiation factor for RNA polymerase B? EMBO J. 3, 2363-2371.
14. Ferrai, C., Munari, D., Luraghi, P., Pecciarini, L., Cangi, M. G., Doglioni, C., Blasi, F., and Crippa, M. P. (2007). A transcription-dependent micrococcal nuclease-resistant fragment of the urokinase-type plasminogen activator promoter interacts with the enhancer. J. Biol. Chem. 282, 12537-12546.
15. Ferretti, E., Cambronero, F., Tumpel, S., Longobardi, E., Wiedemann, L. M., Blasi, F., and Krumlauf, R. (2005). Hoxb1 enhancer and control of rhombomere 4 expression: complex interplay between PREP1-PBX1-HOXB1 binding sites. Mol. Cell. Biol. 25, 8541-8552.
16. Ferretti, E., Marshall, H., Popperl, H., Maconochie, M., Krumlauf, R., and Blasi, F. (2000). Segmental expression of Hoxb2 in r4 requires two separate sites that integrate cooperative interactions between Prep1, Pbx and Hox proteins. Development 127, 155-166. (Pubitemid 30064397)
17. Ferretti, E., et al. (2006). 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. 26, 5650-5662.
18. Fomproix, N., and Percipalle, P. (2004). An actin-myosin complex on actively transcribing genes. Exp. Cell Res. 294, 140-148.
19. Gould, A., Itasaki, N., and Krumlauf, R. (1998). Initiation of rhombomeric Hoxb4 expression requires induction by somites and a retinoid pathway. Neuron 21, 39-51. (Pubitemid 28355690)
20. Grummt, I. (2006). Actin and myosin as transcription factors. Curr. Opin. Genet. Dev. 16, 191-196.
21. Hu, P., Wu, S., and Hernandez, N. (2004). A role for beta-actin in RNA polymerase III transcription. Genes Dev. 18, 3010-3015. (Pubitemid 39658170)
22. Huang, D., Chen, S. W., and Gudas, L. J. (2002). Analysis of two distinct retinoic acid response elements in the homeobox gene Hoxb1 in transgenic mice. Dev. Dyn. 223, 353-370.
23. Jacobs, Y., Schnabel, C. A., and Cleary, M. L. (1999). Trimeric association of Hox and TALE homeodomain proteins mediates Hoxb2 hindbrain enhancer activity. Mol. Cell. Biol. 19, 5134-5142.
24. Jockusch, B. M., Schoenenberger, C. A., Stetefeld, J., and Aebi, U. (2006). Tracking down the different forms of nuclear actin. Trends Cell Biol. 16, 391-396. (Pubitemid 44118783)
25. Krumlauf, R. (1994). Hox genes in vertebrate development. Cell 78, 191-201.
26. Kukalev, A., Nord, Y., Palmberg, C., Bergman, T., and Percipalle, P. (2005). Actin and hnRNP U cooperate for productive transcription by RNA polymerase II. Nat. Struct. Mol. Biol. 12, 238-244.
27. Maconochie, M. K., Nonchev, S., Studer, M., Chan, S. K., Popperl, H., Sham, M. H., Mann, R. S., and Krumlauf, R. (1997). Cross-regulation in the mouse HoxB complex: the expression of Hoxb2 in rhombomere 4 is regulated by Hoxb1. Genes Dev. 11, 1885-1895. (Pubitemid 27315217)
28. Marshall, H., Morrison, A., Studer, M., Popperl, H., and Krumlauf, R. (1996). Retinoids and Hox genes. FASEB J. 10, 969-978.
29. Marshall, H., Studer, M., Popperl, H., Aparicio, S., Kuroiwa, A., Brenner, S., and Krumlauf, R. (1994). A conserved retinoic acid response element required for early expression of the homeobox gene Hoxb-1. Nature 370, 567-571. (Pubitemid 24264924)
30. McDonald, D., Carrero, G., Andrin, C., de Vries, G., and Hendzel, M. J. (2006). Nucleoplasmic beta-actin exists in a dynamic equilibrium between low-mobility polymeric species and rapidly diffusing populations. J. Cell Biol. 172, 541-552. (Pubitemid 43243875)
31. Obrdlik, A., Kukalev, A., and Percipalle, P. (2007). The function of actin in gene transcription. Histol. Histopathol. 22, 1051-1055.
32. Olave, I. A., Reck-Peterson, S. L., and Crabtree, G. R. (2002). Nuclear actin and actin-related proteins in chromatin remodeling. Annu. Rev. Biochem. 71, 755-781.
33. Pantaloni, D., Boujemaa, R., Didry, D., Gounon, P., and Carlier, M. F. (2000). The Arp2/3 complex branches filament barbed ends: functional antagonism with capping proteins. Nat. Cell Biol. 2, 385-391.
34. Pantaloni, D., Le Clainche, C., and Carlier, M. F. (2001). Mechanism of actin-based motility. Science 292, 1502-1506.
35. Pederson, T., and Aebi, U. (2002). Actin in the nucleus: what form and what for? J. Struct. Biol. 140, 3-9.
36. Penkov, D., Di Rosa, P., Fernandez Diaz, L., Basso, V., Ferretti, E., Grassi, F., Mondino, A., and Blasi, F. (2005). Involvement of Prep1 in the alphabeta T-cell receptor T-lymphocytic potential of hematopoietic precursors. Mol. Cell. Biol. 25, 10768-10781.
37. Percipalle, P., and Visa, N. (2006). Molecular functions of nuclear actin in transcription. J. Cell Biol. 172, 967-971.
38. Philimonenko, V. V., Zhao, J., Iben, S., Dingova, H., Kysela, K., Kahle, M., Zentgraf, H., Hofmann, W. A., de Lanerolle, P., Hozak, P., and Grummt, I. (2004). Nuclear actin and myosin I are required for RNA polymerase I transcription. Nat. Cell Biol. 6, 1165-1172.
39. Rohatgi, R., Ma, L., Miki, H., Lopez, M., Kirchhausen, T., Takenawa, T., and Kirschner, M. W. (1999). The interaction between N-WASP and the Arp2/3 complex links Cdc42-dependent signals to actin assembly. Cell 97, 221-231. (Pubitemid 129746811)
40. Ryoo, H. D., Marty, T., Casares, F., Affolter, M., and Mann, R. S. (1999). Regulation of Hox target genes by a DNA bound Homothorax/Hox/ Extradenticle complex. Development 126, 5137-5148. (Pubitemid 30000426)
41. Scheer, U., Hinssen, H., Franke, W. W., and Jockusch, B. M. (1984). Microinjection of actin-binding proteins and actin antibodies demonstrates involvement of nuclear actin in transcription of lampbrush chromosomes. Cell 39, 111-122. (Pubitemid 15218230)
42. Selleri, L., Depew, M. J., Jacobs, Y., Chanda, S. K., Tsang, K. Y., Cheah, K. S., Rubenstein, J. L., O'Gorman, S., and Cleary, M. L. (2001). Requirement for Pbx1 in skeletal patterning and programming chondrocyte proliferation and differentiation. Development 128, 3543-3557. (Pubitemid 32962722)
43. Shav-Tal, Y., and Zipori, D. (2002). PSF and p54(nrb)/NonO-multi- functional nuclear proteins. FEBS Lett. 531, 109-114.
44. Simeone, A., Acampora, D., Arcioni, L., Andrews, P. W., Boncinelli, E., and Mavilio, F. (1990). Sequential activation of HOX2 homeobox genes by retinoic acid in human embryonal carcinoma cells. Nature 346, 763-766. (Pubitemid 20251093)
45. Stock, J. K., Giadrossi, S., Casanova, M., Brookes, E., Vidal, M., Koseki, H., Brockdorff, N., Fisher, A. G., and Pombo, A. (2007). Ring1-mediated ubiquitination of H2A restrains poised RNA polymerase II at bivalent genes in mouse ES cells. Nat. Cell Biol. 9, 1428-1435.
46. Vartiainen, M. K., Guettler, S., Larijani, B., and Treisman, R. (2007). Nuclear actin regulates dynamic subcellular localization and activity of the SRF cofactor MAL. Science 316, 1749-1752. (Pubitemid 46988550)
47. Visa, N. (2005). Actin in transcription. Actin is required for transcription by all three RNA polymerases in the eukaryotic cell nucleus. EMBO Rep. 6, 218-219.
48. Waskiewicz, A. J., Rikhof, H. A., and Moens, C. B. (2002). Eliminating zebrafish pbx proteins reveals a hindbrain ground state. Dev. Cell 3, 723-733.
49. Wu, X., Suetsugu, S., Cooper, L. A., Takenawa, T., and Guan, J. L. (2004). Focal adhesion kinase regulation of N-WASP subcellular localization and function. J. Biol. Chem. 279, 9565-9576.
50. Wu, X., Yoo, Y., Okuhama, N. N., Tucker, P. W., Liu, G., and Guan, J. L. (2006). Regulation of RNA-polymerase-II-dependent transcription by N-WASP and its nuclear-binding partners. Nat. Cell Biol. 8, 756-763.
51. Ye, J., Zhao, J., Hoffmann-Rohrer, U., and Grummt, I. (2008). Nuclear myosin I acts in concert with polymeric actin to drive RNA polymerase I transcription. Genes Dev. 22, 322-330. (Pubitemid 351214274)
52. Yoo, Y., Wu, X., and Guan, J. L. (2007). A novel role of the actin-nucleating Arp2/3 complex in the regulation of RNA polymerase II-dependent transcription. J. Biol. Chem. 282, 7616-7623.