In vitro and transgenic analysis of a human HOXD4 retinoid-responsive enhancer

Development

Volumn 122, Issue 6, 1996, Pages 1895-1907

  Morrison, Alastair ^a   Moroni, Maria Cristina ^b   Ariza McNaughton, Linda ^a   Krumlauf, Robb ^a   Mavilio, Fulvio ^b  

^a NATIONAL INSTITUTE FOR MEDICAL RESEARCH   (United Kingdom)

^b SAN RAFFAELE HOSPITAL   (Italy)

Author keywords

Developmental regulation; Enhancer; Homeobox; Human; Mouse; Neural tube; Retinoic acid

Indexed keywords

REPETITIVE DNA; RETINOIC ACID RECEPTOR; RETINOID;

ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; EMBRYO; EMBRYO DEVELOPMENT; EMBRYONAL CARCINOMA; GENE EXPRESSION REGULATION; GENE MUTATION; HOMEOBOX; HUMAN; HUMAN CELL; MOUSE; NEUROECTODERM; NONHUMAN; PRIORITY JOURNAL; PROTEIN DNA INTERACTION; REPORTER GENE; TRANSGENE;

ANIMALS; BASE SEQUENCE; CONSERVED SEQUENCE; DNA PRIMERS; ENHANCER ELEMENTS (GENETICS); GENE EXPRESSION REGULATION, DEVELOPMENTAL; HOMEODOMAIN PROTEINS; HUMANS; LAC OPERON; MICE; MICE, TRANSGENIC; MOLECULAR SEQUENCE DATA; TRANSCRIPTION FACTORS; TRETINOIN; TUMOR CELLS, CULTURED;

ANIMALIA; MUS MUSCULUS; VERTEBRATA;

EID: 0030000961     PISSN: 09501991     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Article

References (76)

1. Andrews, P. W., Damjanov, L, Simon, D., Banting, D. S., Carlin, C., Dracopoli, N. C. and Fogh, J. (1984). Pluripotent embryonal carcinoma clones derived from the human teratocarcinoma cell line Tera-2. Differentiation in vivo and in vitro. Lah. Invest. 50, 147-162.
2. Aparicio, S., Morrison, A., Gould, A., Gilthorpe, J., Chaudhurl, C., Rigby, P., Krumlauf, R. and Brenner, S. (1995). Detecting conserved regulatory elements with the model genome of the Japanese puffer fish, Fugu rubripes. Proc. Nztl. Acad. Sci. USA 92, 1684-1688.
3. Balkan, W., Colbert, M., Bock, C. and Linney, E. (1992). Transgenic indicator mice for studying activated retinoic acid receptors during development. Proc. Natl Acad. Sci. USA 89. 3347-3351.
4. Behringer, R., Crotty, D. A., Tennyson, V. M., Brinster, R., Palmiter, R. and Wolgemuth, D. (1993). Sequences 5′ of the homeobox of the Hox-1.4 gene direct tissue-specific expression of lacZ during mouse development. Development 117, 823-833.
5. Blomhoff, R., Green, M. H., Berg, T. and Norum, K. R. (1990). Transport and storage of vitamin A. Science 250, 399-403.
6. Chen, Y. P., Huang, L., Russo, A. F. and Solursh, M. (1992). Retinoic acid is enriched in Hensen's node and is developmentally regulated in the early chicken embryo. Proc. Nutl. Acad. Sci. USA 89, 10056-10059.
7. Cianetti, L., Di Cristofaro, A., Zappavigna, V., Bottero, L., Boccoli, G., Testa, U., Russo, G., Boncinelli, E. and Peschle, C. (1990). Molecular mechanisms underlying the expression of the human HOX-5.1 gene. Nucl. Acids Res. 18, 4361-4368.
8. Colbert, M. C., Linney, E. and LaMantia, A. S. (1993). Local sources of retinoic acid coincide with retinoid-mediated transgene activity during embryonic development. Proc. Natl. Acad. Sci. USA 90, 6572-6576.
9. Conlon, R. A. and Rossant, J. (1992). Exogenous retinoic acid rapidly induces anterior ectopic expression of murine Hox-2 genes in vivo. Development 116, 357-368.
10. Courtois, G., Baumhueter, S. and Crabtree, G. R. (1988). Purified hepatocyte nuclear factor 1 interacts with a family of hepatocyte-specific promoters. Proc. Natl. Acad. Sci. USA 85. 7937-7941.
11. De Simone, V., De Magistris, L., Lazzaro, D., Gerstner, J., Monaci, P., Nicosia, A. and Cortese, R. (1991). LFB3, a heterodimer-forming homeoprotein of the LFBI family is expressed in specialized epithelia. EMBO J. 10, 1435-1443.
12. de Wet, J. R., Wood, K. V., DeLuca, M., Helsinki, D. R. and Subramani, S. (1987). Firefly luciferase gene: structure and expression in mammalian cells. Mol. Cell. Biol. 7, 725-737.
13. Dignam, J. R., Lebovitz, R. M. and Roeder, R. G. (1983). Accurate transcription initiation by RNA polymerase II in a soluble extract from isolated mammalian nuclei. Nucl. Acids Res. 11, 1475-1489.
14. Duboule, D. (1992). The vertebrate limb: a model system to study the Hox/HOM gene network during development and evolution. BioEssays 14, 375-384.
15. Duboule, D. and Dollé, P. (1989). The structural and functional organization of the murine HOX gene family resembles that of Drosophila homeotic genes. EMBO J. 8, 1497-1505.
16. Eid, R., Koseki, H. and Schughart, K. (1993). Analysis of lacZ reporter genes in transgenic embryos suggests the presence of several cis-acting regulatory elements in the murine Hox-b6 gene. Dev. Dyn. 196, 205-216.
17. Faiella. A., Zappavigna, V., Mavilio, F. and Boncinelli, E. (1994). Inhibition of retinoic acid-induced activation of 3′ human HOXB genes by antisense oligonucleotides affects sequential activation of genes located upstream in the four HOX cluster. Proc. Natl. Acad. Sci. USA 91, 5335-5339.
18. Featherstone, M. S., Baron, A., Gaunt, S. J., Mattel, M. G. and Duboule, D. (1988). Hox-5.1 defines a homeo-box containing gene locus on mouse chromosome 2. Proc: Natl. Acad. Sci. USA 85, 4760-4764.
19. Frasch, M., Chen, X. and Lufkin, T. (1995). Evolutionary-conserved enhancers direct region-specific expression of the murine Haxa-I and Hoxa2 loci in both mice and Drosophila. Development 121, 957-974.
20. Gaunt, S. J., Krumlauf, R. and Duboule, D. (1989). Mouse homeogenes within a subfamily Hox-1.4, -2.6 and -5.1 dispaly similar anteroposterior domains of expression in the embryo, but show stage- and time-dependent differences in their regulation. Development 107, 131-134.
21. Gehring, W. J., Müller, M., Affolter, M., Percival-Smith, A., Billeter, M., Qian, Y. Q., Otting, G. and Wüthrich, K. (1990). The structure of the homeodomain and its functional implications. Trends Genet. 6, 323-329.
22. Gerard, M., Duboule, D. and Zakany, J. (1993). Structure and activity of regulatory elements involved in the activation of the Hoxd-ll gene during late gastrulation. EMBO J. 12, 3539-3550.
23. Graham, A., Papalopulu, N. and Krumlauf, R. (1989). The murine and drosophila homeobox gene complexes have common features of organization and expression. Cell 57, 367-378.
24. Hogan, B. L. M., Costantini, F. and Lacy, E. (1986). Manipulating the Mouse Embryo. A Laboratory Manual. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press.
25. Hogan, B. L. M., Thaller, C. and Eichele, G. (1992). Evidence that the Hensen's node is a site of retinoic acid synthesis. Nature 359, 237-241.
26. Horton, G. and Maden, M. (1995). Endogenous distribution of retinoids during normal development and teratogenesis in the mouse embryo. Dev. Dyn. 202, 312-323.
27. Hunt, P., Gulisano, M., Cook, M., Sham, M. H., Faiella, A., Wilkinson, D., Boncinelli, E. and Krumlauf, R. (1991). A distinct Hox code for the branchial region of the vertebrate head. Nature 353, 861-864.
28. Izpisúa-Belmonte, J.-C., Tickle, C., Dollé, P., Wolpert, L. and Duboule, D. (1991). Expression of the homeobox Hox-4 genes and the specification of position in chick wing development. Nature 350, 585-589.
29. Kessel, M. (1992). Respecification of vertebral identities by retinoic acid. Development 115, 487-501.
30. Kessel, M. and Gruss, P. (1991). Homeotic transformations of murine vertebrae and concomitant alteration of Hox codes induced by retinoic acid. Cell 67, 89-104.
31. Kress, C., Vogels, R., De Graaf, W., Bonnerot, C., Meijlink, F., Nicolas, J. F. and Deschamps, J. (1990). HOX 2.3 upstream sequences mediate lacZ expression in intermediate mesoderm derivatives of transgenic mice. Development 109, 775-786.
32. Krumlauf, R. (1993). Hox genes and pattern formation in the branchial region of the vertebrate head. Trends Genet. 9, 106-112.
33. Krumlauf, R. (1994). Hox genes in vertebrate development. Cell 78, 191-201.
34. La Rosa, G. J. and Gudas, L. J. (1988). An early effect of retinoic acid: cloning of an mRNA (ERA-1) exhibiting rapid and protein synthesisindipendent induction during teratorcarcinoma stem cell differentiation. Proc. Natl Acad. Sci. USA 85, 329-333.
35. Langsten, A. W. and Gudas, L. J. (1992). Identification of a retinoic acid responsive enhancer 3′ of the murine homeobox gene Hox-1.6. Mech. Dev. 38, 217-228.
36. Langston, A. W. and Gudas, L. J. (1994). Retinoic acid and homeobox gene regulation. Curr. Opin. Genet. Dev. 4, 550-555.
37. Leid, M., Kastner, P. and Chambon, P. ( 1992). Multiplicity generates diversity in the retinoic acid signalling pathways. Trends Biochem. Sci. 17, 427-433.
38. Marshall, H., Nonchev. S., Sham, M. H., Muchamore, I., Lumsden, A. and Krumlauf, R. ( 1992). Retinoic acid alters hindbrain Hox code and induces transformation of rhombomeres 2/3 into a 4/5 identity. Nature 360, 737-741.
39. Marshall, H., Studer, M., Pöpperl, 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 Hoxh-I. Nature 370, 567-571.
40. Mavilio, F., Simeone, A., Giampaolo, A., Faiella, A., Zappavigna, V., Acampora, D., Poiana, G., Russo, G., Peschle, C. and Boncinelli, E. (1986). Differential and stage-related expression in embryonic tissues of a new human homeobox gene. Nature 324, 664-666.
41. McGinnis, N., Kuziora, M. A. and McGinnis, W. (1990). Human Hox 4.2 and Drosophila Deformed encode similar regulatory specificities in Drosophila embryos and larvae. Cell 63, 969-976.
42. McGinnis, W. and Krumlauf, R. (1992). Homeobox genes and axial patterning. Cell 68, 283-302.
43. Mendelsohn, C., Ruberte, E., LeMeur, M., Morriss-Kay, G. and Chambon, P. (1991). Developmental analysis of the retinoic acid-inducible RAR-beta 2 promoter in transgenic animals. Development 113, 723-734.
44. Moroni, M. C., Vigano, M. A. and Mavilio, F. (1993). Regulation of the human HOXD4 gene by retinoids. Mech. Dev. 44, 139-154.
45. Morrison, A., Chaudhuri, C., Ariza-McNaughton, L., Muchamore, I., Kuroiwa, A. and Krumlauf, R. (1995). Comparative analysis of chicken Hoxb-4 regulation in transgenic mice. Mech. Dev. 63, 47-59.
46. Nohno, T., Noji, S., Koyama, E., Ohyama, K., Myokai, F., Kuroiwa, A., Saito, T. and Taniguchi, S. (1991). Involvement of the Chox-4 chiken homeobox genes in determination of anteroposterior axial polarity during limb development. Cell 64. 1197-1205.
47. Nordeen, S. K. (1988). Luciferase reporter gene vectors for analysis of promoters and enhancers. Biotechniques 6, 454-457.
48. Ogura, T, and Evans, M. R. (1995a). Evidence for two distinct retinoic acid response pathways for HOXBI gene regulation. Proc. Natl. Acad. Sci. USA 92. 392-396.
49. Ogura, T. and Evans, R. M. (1995b). A retinoic acid-triggered cascade of HOXBI gene activation. Proc. Natl. Acad. Sci. USA 92, 387-391.
50. Oliver, G., De Robertis, E. M., Wolpert, L. and Tickle, C. (1990) Expression of a homeobox gene in the chick wing bud following application of retinoic acid and grafts of polarizing region tissue. EMBO J. 9. 3093-3099.
51. Papalopulu, N., Lovell-Badge, R. and Krumlauf, R. (1991). The expression of murine Hox-2 genes is dependent on the differentiation pathway and displays a colinear sensitivity to retinoic acid in F9 cells and Xenopus embryos. Nucl. Acids Res. 19, 5497-5506.
52. Pöpperl, H., Bienz, M., Studer, M., Chang, S.-K., Aparicio, S., Brenner, S., Mann, R. and Krumlauf, R. (1995). Segmental expression of Hoxh-l is controlled by a highly conserved autoregulatory loop dependent upon exd/Pbx.Cell 81, 1031-1042.
53. Pöpperl, H. and Featherstone, M. S. (1992). An autoregulatory element of the murine Hox-4.2 gene. EMBO J. 11. 3673-3680.
54. Pöpperl, H. and Featherstone, M. S. (1993). Identification of a retinoic acid response element upstream of the murine Hax-4.2 gene. Mol. Cell. Biol. 13, 257-265.
55. Püschel, A. W., Balling, R. and Gruss, P. ( 1990). Position-specific activity of the Hoxl. I promoter in transgenic mice. Development 108, 435-442.
56. Püschel, A. W., Balling, R. and Gruss, P. (1991). Separate elements cause lineage restriction and specific boundaries of Hox 1.1 expression. Development 112, 279-287.
57. Reynolds, K., Mezey, E. and Zimmer, A. (1991 ). Activity of the beta-retinoic acid receptor promoter in transgenic mice. Mech. Dev. 36, 15-29.
58. Rossant, J., Zirngibl, R., Cado, D., Shago, M. and Gigiiere, V. (1991). Expression of retinoic acid response element-hsp lacZ transgene defines specific domains of transcriptional activity during mouse embryogenesis. Genes Dev.5, 1333-1344.
59. Sambrook, J., Fritsch, E. F. and Maniatis, T. (1989). Molecular Cloning: A Laboratory Manual. 2nd ed., pp. Cold Spring Harbor. NY: Cold Spring Harbor Laboratory Press.
60. Saurat, J. H. (1990). Retinoids: 10 years on. Basel :
61. S. Karger. Sham, M. H., Hunt, P., Nonchev, S., Papalopulu, N., Graham, A., Boncinelli, E. and Krumlauf, R. (1992). Analysis of the murine Hox-2.7 gene: conserved alternative transcripts with differential distributions in the nervous system and the potential for shared regulatory regions. EMBO J. 11, 1825-1836.
62. Sham, M. H., Vesque, C., Nonchev, S., Marshall, H., Frain, M., Das Gupta, R., Whiting, J., Wilkinson, D., Charnay, P. and Krumlauf, R. (1993). The zinc finger gene Krox-20 regulates Hox-b2 (Hox-2.8) during hindbrain segmentation. Cell 72, 183-197.
63. Simeone, A., Acampora, D., Arcioni, L., Andrews, P. W., Boncinelli, E. and Mavilio, F. (1990). Sequential activation of HOX 2 homeobox genes by retinoic acid in human embryonal carcinoma cells. Nature 346, 763-766.
64. Simeone, A., Acampora, D., Nigro, V., Faiella, A., D'Esposito, M., Stornaiuolo, A., Mavilio, F. and Boncinelli, E. (1991). Differential regulation by retinoic acid of the homeobox genes of the four Hox loci in human embryonal carcinoma cells. Mech. Dev 33, 215-228.
65. Simeone, A., Avantaggiato, V., Moroni, M. C., Mavilio, F., Arra, C., Cotelli, F., Nigro, V. and Acampora, C. (1995). Retinoic acid induces stage-specific anteroposterior transformation of rostral central nervous system. Mech. Dev. 51, 83-98.
66. Studer, M., Popperl, H., Marshall, H., Kuroiwa, A. and Krumlauf, R. (1994). Role of a conserved retinoic acid response element in rhombomere restriction oiHoxb-l. Science 256, 1728-1732.
67. Summerbell, D. and Maden, M. (1990). Retinoic acid, a developmental signalling molecule. Trends Neurosci. 13, 142-147.
68. Tabin, C. J. (1991). Retinoids, Homeoboxes and Growth Factors: toward molecular models for limb development. Cell 66. 199-217.
69. Thaller, C. and Eichele, G. (1987). Identification and spatial distribution of retinoids in the developing chick limb bud. Nature 397, 625-628.
70. Thaller, C. and Eichele, G. (1990). Isolation of 3.4-didehydroretinoic acid, a novel morphogenetic signal in the chick wing bud. Nature 345, 815-819.
71. Tuggle, C. K., Zàkàny, J., Cianetti, L., Peschle, C. and Nguyen-Huu, C. M. (1990). Region-specific enhancers near two mammalian homeobox genes define adjacent rostrocaudal domains in the central nervous system. Genes Dev. 4, 180-189.
72. Vogels, R., Charite, J., de Graaff, W. and Deschamps, J. (1993). Proximal cis-acting elements cooperate to set Hox-b7(Hox-2.3) expression boundaries in transgenic mice. Development 117, 71-82.
73. Wagner, M., Han, B. and Jessel, T. M. (1992). Regional differences in retinoid release from embryonic neural tissue detected by an in vitro reporter assay. Development 116, 55-66.
74. Wagner, M., Thaller, C., Jessel, T. and Eichele, G. (1990). Polarizing activity and retinoid synthesis in the floor plate of the neural tube. Nature 345, 819-822.
75. Whiting, J., Marshall, H., Cook, M., Krumlauf, R., Rigby, P., Stott, D. and Allemann, R. (1991). Multiple spatially-specific enhancers are required to reconstruct the pattern of Hox-2.6 gene expression. Genes Dev. 5, 20482059.
76. Wilkinson, D. G. (1992). Whole Mount in Situ Hybridisation of Vertebrate Embryos, pp. 75-83. Oxford. UK: Oxford University Press.