Note to users. If you're seeing this message, it means that your browser cannot find this page's style/presentation instructions -- or possibly that you are using a browser that does not support current Web standards. Find out more about why this message is appearing, and what you can do to make your experience of our site the best it can be.


Science 18 July 2003:
Vol. 301. no. 5631, pp. 331 - 333
DOI: 10.1126/science.1085753

Review

Organizing Axes in Time and Space; 25 Years of Colinear Tinkering

Marie Kmita and Denis Duboule*

During vertebrate development, clustered genes from the Hox family of transcription factors are activated in a precise temporal and spatial sequence that follows their chromosomal order (the "Hox clock"). Recent advances in the knowledge of the underlying mechanisms reveal that the embryo uses a variety of strategies to implement this colinear process, depending on both the type and the evolutionary history of axial structures. The search for a universal mechanism has likely hampered our understanding of this enigmatic phenomenon, which may be caused by various and unrelated regulatory processes, as long as the final distribution of proteins (the HOX code) is preserved.

Department of Zoology and Animal Biology and National Center of Competence in Research "Frontiers in Genetics," University of Geneva, Sciences III, Quai Ernest Ansermet 30, 1211 Geneva 4, Switzerland.

* To whom correspondence should be addressed. E-mail: denis.duboule{at}zoo.unige.ch

Read the Full Text



THIS ARTICLE HAS BEEN CITED BY OTHER ARTICLES:
Elephant shark (Callorhinchus milii) provides insights into the evolution of Hox gene clusters in gnathostomes.
V. Ravi, K. Lam, B.-H. Tay, A. Tay, S. Brenner, and B. Venkatesh (2009)
PNAS 106, 16327-16332
   Abstract »    Full Text »    PDF »
Fork Stalling and Template Switching As a Mechanism for Polyalanine Tract Expansion Affecting the DYC Mutant of HOXD13, a New Murine Model of Synpolydactyly.
O. Cocquempot, V. Brault, C. Babinet, and Y. Herault (2009)
Genetics 183, 23-30
   Abstract »    Full Text »    PDF »
Conservation of enhancer location in divergent insects.
J. Cande, Y. Goltsev, and M. S. Levine (2009)
PNAS 106, 14414-14419
   Abstract »    Full Text »    PDF »
HoxB5 induces endothelial sprouting in vitro and modifies intussusceptive angiogenesis in vivo involving angiopoietin-2.
S. Winnik, M. Klinkert, H. Kurz, C. Zoeller, J. Heinke, Y. Wu, C. Bode, C. Patterson, and M. Moser (2009)
Cardiovasc Res 83, 558-565
   Abstract »    Full Text »    PDF »
Epigenetic Temporal Control of Mouse Hox Genes in Vivo.
N. Soshnikova and D. Duboule (2009)
Science 324, 1320-1323
   Abstract »    Full Text »    PDF »
Atypical relaxation of structural constraints in Hox gene clusters of the green anole lizard.
N. Di-Poi, J. I. Montoya-Burgos, and D. Duboule (2009)
Genome Res. 19, 602-610
   Abstract »    Full Text »    PDF »
Long noncoding RNAs in mouse embryonic stem cell pluripotency and differentiation.
M. E. Dinger, P. P. Amaral, T. R. Mercer, K. C. Pang, S. J. Bruce, B. B. Gardiner, M. E. Askarian-Amiri, K. Ru, G. Solda, C. Simons, et al. (2008)
Genome Res. 18, 1433-1445
   Abstract »    Full Text »    PDF »
Increased Cdx protein dose effects upon axial patterning in transgenic lines of mice.
S. J. Gaunt, D. Drage, and R. C. Trubshaw (2008)
Development 135, 2511-2520
   Abstract »    Full Text »    PDF »
Differential Evolution of the 13 Atlantic Salmon Hox Clusters.
S. Mungpakdee, H.-C. Seo, A. R. Angotzi, X. Dong, A. Akalin, and D. Chourrout (2008)
Mol. Biol. Evol. 25, 1333-1343
   Abstract »    Full Text »    PDF »
CTCF physically links cohesin to chromatin.
E. D. Rubio, D. J. Reiss, P. L. Welcsh, C. M. Disteche, G. N. Filippova, N. S. Baliga, R. Aebersold, J. A. Ranish, and A. Krumm (2008)
PNAS 105, 8309-8314
   Abstract »    Full Text »    PDF »
An ultraconserved Hox-Pbx responsive element resides in the coding sequence of Hoxa2 and is active in rhombomere 4.
X. Lampe, O. A. Samad, A. Guiguen, C. Matis, S. Remacle, J. J. Picard, F. M. Rijli, and R. Rezsohazy (2008)
Nucleic Acids Res. 36, 3214-3225
   Abstract »    Full Text »    PDF »
Ectopic nuclear reorganisation driven by a Hoxb1 transgene transposed into Hoxd.
C. Morey, N. R. Da Silva, M. Kmita, D. Duboule, and W. A. Bickmore (2008)
J. Cell Sci. 121, 571-577
   Abstract »    Full Text »    PDF »
Modeling Hox gene regulation in digits: reverse collinearity and the molecular origin of thumbness.
T. Montavon, J.-F. Le Garrec, M. Kerszberg, and D. Duboule (2008)
Genes & Dev. 22, 346-359
   Abstract »    Full Text »    PDF »
Implications of cnidarian gene expression patterns for the origins of bilaterality is the glass half full or half empty?.
E. E. Ball, D. M. de Jong, B. Schierwater, C. Shinzato, D. C. Hayward, and D. J. Miller (2007)
Integr. Comp. Biol. 47, 701-711
   Abstract »    Full Text »    PDF »
Hox patterning of the vertebrate rib cage.
D. C. McIntyre, S. Rakshit, A. R. Yallowitz, L. Loken, L. Jeannotte, M. R. Capecchi, and D. M. Wellik (2007)
Development 134, 2981-2989
   Abstract »    Full Text »    PDF »
The rise and fall of Hox gene clusters.
D. Duboule (2007)
Development 134, 2549-2560
   Abstract »    Full Text »    PDF »
Wnt signaling is a key mediator of Cdx1 expression in vivo.
N. Pilon, K. Oh, J.-R. Sylvestre, J. G. A. Savory, and D. Lohnes (2007)
Development 134, 2315-2323
   Abstract »    Full Text »    PDF »
Nuclear reorganisation and chromatin decondensation are conserved, but distinct, mechanisms linked to Hox gene activation.
C. Morey, N. R. Da Silva, P. Perry, and W. A. Bickmore (2007)
Development 134, 909-919
   Abstract »    Full Text »    PDF »
Conserved distances between vertebrate highly conserved elements.
H. Sun, G. Skogerbo, and R. Chen (2006)
Hum. Mol. Genet. 15, 2911-2922
   Abstract »    Full Text »    PDF »
Genomic evolution of Hox gene clusters..
D. Lemons and W. McGinnis (2006)
Science 313, 1918-1922
   Abstract »    Full Text »    PDF »
Interplay between Chromatin and Trans-acting Factors Regulating the Hoxd4 Promoter during Neural Differentiation.
L. Kobrossy, M. Rastegar, and M. Featherstone (2006)
J. Biol. Chem. 281, 25926-25939
   Abstract »    Full Text »    PDF »
Differential regulation of gene expression in the digit forming area of the mouse limb bud by SHH and gremlin 1/FGF-mediated epithelial-mesenchymal signalling.
L. Panman, A. Galli, N. Lagarde, O. Michos, G. Soete, A. Zuniga, and R. Zeller (2006)
Development 133, 3419-3428
   Abstract »    Full Text »    PDF »
Proteolysis of MLL family proteins is essential for Taspase1-orchestrated cell cycle progression.
S. Takeda, D. Y. Chen, T. D. Westergard, J. K. Fisher, J. A. Rubens, S. Sasagawa, J. T. Kan, S. J. Korsmeyer, E. H.-Y. Cheng, and J. J.-D. Hsieh (2006)
Genes & Dev. 20, 2397-2409
   Abstract »    Full Text »    PDF »
Highly conserved syntenic blocks at the vertebrate Hox loci and conserved regulatory elements within and outside Hox gene clusters.
A. P. Lee, E. G. L. Koh, A. Tay, S. Brenner, and B. Venkatesh (2006)
PNAS 103, 6994-6999
   Abstract »    Full Text »    PDF »
Steroid-dependent modification of Hox function drives myocyte reprogramming in the Drosophila heart.
B. Monier, M. Astier, M. Semeriva, and L. Perrin (2005)
Development 132, 5283-5293
   Abstract »    Full Text »    PDF »
HoxD cluster scanning deletions identify multiple defects leading to paralysis in the mouse mutant Ironside.
B. Tarchini, T. H. N. Huynh, G. A. Cox, and D. Duboule (2005)
Genes & Dev. 19, 2862-2876
   Abstract »    Full Text »    PDF »
Developmental regulation of the Hox genes during axial morphogenesis in the mouse.
J. Deschamps and J. van Nes (2005)
Development 132, 2931-2942
   Abstract »    Full Text »    PDF »
Development of the Mammalian Female Reproductive Tract.
Y. Yin and L. Ma (2005)
J. Biochem. 137, 677-683
   Abstract »    Full Text »    PDF »
Conservation of regulatory sequences and gene expression patterns in the disintegrating Drosophila Hox gene complex.
B. Negre, S. Casillas, M. Suzanne, E. Sanchez-Herrero, M. Akam, M. Nefedov, A. Barbadilla, P. de Jong, and A. Ruiz (2005)
Genome Res. 15, 692-700
   Abstract »    Full Text »    PDF »
Nuclear re-organisation of the Hoxb complex during mouse embryonic development.
S. Chambeyron, N. R. Da Silva, K. A. Lawson, and W. A. Bickmore (2005)
Development 132, 2215-2223
   Abstract »    Full Text »    PDF »
Cdx Protein Interaction with Hoxa5 Regulatory Sequences Contributes to Hoxa5 Regional Expression along the Axial Skeleton.
S. Tabaries, J. Lapointe, T. Besch, M. Carter, J. Woollard, C. K. Tuggle, and L. Jeannotte (2005)
Mol. Cell. Biol. 25, 1389-1401
   Abstract »    Full Text »    PDF »
Direct crossregulation between retinoic acid receptor {beta} and Hox genes during hindbrain segmentation.
P. Serpente, S. Tumpel, N. B. Ghyselinck, K. Niederreither, L. M. Wiedemann, P. Dolle, P. Chambon, R. Krumlauf, and A. P. Gould (2005)
Development 132, 503-513
   Abstract »    Full Text »    PDF »
Inhibition of neurogenesis at the zebrafish midbrain-hindbrain boundary by the combined and dose-dependent activity of a new hairy/E(spl) gene pair.
J. Ninkovic, A. Tallafuss, C. Leucht, J. Topczewski, B. Tannhauser, L. Solnica-Krezel, and L. Bally-Cuif (2005)
Development 132, 75-88
   Abstract »    Full Text »    PDF »
Loss of Function but No Gain of Function Caused by Amino Acid Substitutions in the Hexapeptide of Hoxa1 In Vivo.
S. Remacle, L. Abbas, O. De Backer, N. Pacico, A. Gavalas, F. Gofflot, J. J. Picard, and R. Rezsohazy (2004)
Mol. Cell. Biol. 24, 8567-8575
   Abstract »    Full Text »    PDF »
The Homeoprotein Alx3 Contains Discrete Functional Domains and Exhibits Cell-specific and Selective Monomeric Binding and Transactivation.
B. Perez-Villamil, M. Mirasierra, and M. Vallejo (2004)
J. Biol. Chem. 279, 38062-38071
   Abstract »    Full Text »    PDF »
Segmentation in vertebrates: clock and gradient finally joined.
A. Aulehla and B. G. Herrmann (2004)
Genes & Dev. 18, 2060-2067
   Abstract »    Full Text »    PDF »
Retinoic acid influences anteroposterior positioning of epidermal sensory neurons and their gene expression in a developing chordate (amphioxus).
M. Schubert, N. D. Holland, H. Escriva, L. Z. Holland, and V. Laudet (2004)
PNAS 101, 10320-10325
   Abstract »    Full Text »    PDF »
Chromatin decondensation and nuclear reorganization of the HoxB locus upon induction of transcription.
S. Chambeyron and W. A. Bickmore (2004)
Genes & Dev. 18, 1119-1130
   Abstract »    Full Text »    PDF »
Protein Kinase C-Mediated Phosphorylation of the Leukemia-Associated HOXA9 Protein Impairs Its DNA Binding Ability and Induces Myeloid Differentiation.
U. Vijapurkar, N. Fischbach, W. Shen, C. Brandts, D. Stokoe, H. J. Lawrence, and C. Largman (2004)
Mol. Cell. Biol. 24, 3827-3837
   Abstract »    Full Text »    PDF »
MicroRNA-Directed Cleavage of HOXB8 mRNA.
S. Yekta, I-h. Shih, and D. P. Bartel (2004)
Science 304, 594-596
   Abstract »    Full Text »    PDF »
Hoxa9 influences the phenotype but not the incidence of Mll-AF9 fusion gene leukemia.
A. R. Kumar, W. A. Hudson, W. Chen, R. Nishiuchi, Q. Yao, and J. H. Kersey (2004)
Blood 103, 1823-1828
   Abstract »    Full Text »    PDF »
Do Higher-Order Chromatin Structure and Nuclear Reorganization Play a Role in Regulating Hox Gene Expression during Development?.
W.A. BICKMORE, N.L. MAHY, and S. CHAMBEYRON (2004)
Cold Spring Harb Symp Quant Biol 69, 251-258
   Abstract »    PDF »
Mechanism of Polycomb Group Gene Silencing.
Y. ZHANG, R. CAO, L. WANG, and R.S. JONES (2004)
Cold Spring Harb Symp Quant Biol 69, 309-318
   Abstract »    PDF »
The Segmentation Clock: Converting Embryonic Time into Spatial Pattern.
O. Pourquie (2003)
Science 301, 328-330
   Abstract »    Full Text »    PDF »



To Advertise     Find Products


Science. ISSN 0036-8075 (print), 1095-9203 (online)