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Review ArticleReview Article

Homeoprotein Signaling in Development, Health, and Disease: A Shaking of Dogmas Offers Challenges and Promises from Bench to Bed

Julien Spatazza, Elizabeth Di Lullo, Alain Joliot, Edmond Dupont, Kenneth L. Moya and Alain Prochiantz
Glenda E. Gillies, ASSOCIATE EDITOR
Pharmacological Reviews January 2013, 65 (1) 90-104; DOI: https://doi.org/10.1124/pr.112.006577
Julien Spatazza
Development and Neuropharmacology Group (J.S., E.D.L., K.L.M., A.P.), and Cell Biology of Homeoproteins Group (A.J., E.D.), College de France, Centre for Interdisciplinary Research in Biology, CNRS UMR 7241/INSERM U1050, Labex Memolife, PSL Research University, Paris, France
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Elizabeth Di Lullo
Development and Neuropharmacology Group (J.S., E.D.L., K.L.M., A.P.), and Cell Biology of Homeoproteins Group (A.J., E.D.), College de France, Centre for Interdisciplinary Research in Biology, CNRS UMR 7241/INSERM U1050, Labex Memolife, PSL Research University, Paris, France
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Alain Joliot
Development and Neuropharmacology Group (J.S., E.D.L., K.L.M., A.P.), and Cell Biology of Homeoproteins Group (A.J., E.D.), College de France, Centre for Interdisciplinary Research in Biology, CNRS UMR 7241/INSERM U1050, Labex Memolife, PSL Research University, Paris, France
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Edmond Dupont
Development and Neuropharmacology Group (J.S., E.D.L., K.L.M., A.P.), and Cell Biology of Homeoproteins Group (A.J., E.D.), College de France, Centre for Interdisciplinary Research in Biology, CNRS UMR 7241/INSERM U1050, Labex Memolife, PSL Research University, Paris, France
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Kenneth L. Moya
Development and Neuropharmacology Group (J.S., E.D.L., K.L.M., A.P.), and Cell Biology of Homeoproteins Group (A.J., E.D.), College de France, Centre for Interdisciplinary Research in Biology, CNRS UMR 7241/INSERM U1050, Labex Memolife, PSL Research University, Paris, France
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Alain Prochiantz
Development and Neuropharmacology Group (J.S., E.D.L., K.L.M., A.P.), and Cell Biology of Homeoproteins Group (A.J., E.D.), College de France, Centre for Interdisciplinary Research in Biology, CNRS UMR 7241/INSERM U1050, Labex Memolife, PSL Research University, Paris, France
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Glenda E. Gillies
Development and Neuropharmacology Group (J.S., E.D.L., K.L.M., A.P.), and Cell Biology of Homeoproteins Group (A.J., E.D.), College de France, Centre for Interdisciplinary Research in Biology, CNRS UMR 7241/INSERM U1050, Labex Memolife, PSL Research University, Paris, France
Roles: ASSOCIATE EDITOR
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Abstract

Homeoproteins constitute a major class of transcription factors active throughout development and in adulthood. Their membrane transduction properties were discovered over 20 years ago, opening an original field of research in the domain of vector peptides and signal transduction. In early development, homeoprotein transfer participates in tissue patterning, cell/axon guidance, and migration. In the axon guidance model, homeoproteins exert their non–cell autonomous activity through the regulation of translation, in particular, that of nuclear-transcribed mitochondrial mRNAs. An important aspect of these studies on patterning and migration is that homeoproteins sensitize the cells to the action of other growth factors, thus cooperating with established signaling pathways. The role of homeoprotein signaling at later developmental stages is also of interest. In particular, the transfer of homeoprotein Otx2 into parvalbumin-expressing inhibitory neurons (PV-cells) in the visual cortex regulates cortical plasticity. The molecular deciphering of the interaction of Otx2 with binding sites at the surface of PV-cells has allowed the development of a specific Otx2 antagonist that reopens plasticity in the adult cortex and cures mice from experimental amblyopia, a neurodevelopmental disease. Finally, the use of homeoproteins as therapeutic proteins in mouse models of glaucoma and Parkinson disease is reviewed. In the latter case, engrailed homeoproteins protect mesencephalic dopaminergic neurons by increasing the local translation of complex I mitochondrial mRNAs. In conclusion, this review synthesizes 20 years of work on the fundamental and potentially translational aspects of homeoprotein signaling.

Footnotes

  • ↵1Both J.S. and E.D.L. contributed equally as first authors.

  • In addition to institutional support, this study was supported by Agence Nationale pour la Recherche (ANR-10-BLAN-141-01 & ANR-11-BLAN-069467 to A.P. and A.J.) and Global Research Laboratory Program (2009-00424 to A.P. and A.J.) from the Korean Ministry of Education. J.S. and E.D.L. are College de France postdoctoral fellows.

  • dx.doi.org/10.1124/pr.112.006577.

  • Copyright © 2013 by The American Society for Pharmacology and Experimental Therapeutics
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Pharmacological Reviews: 65 (1)
Pharmacological Reviews
Vol. 65, Issue 1
1 Jan 2013
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Review ArticleReview Article

Homeoprotein Signaling in Development, Health, and Disease

Julien Spatazza, Elizabeth Di Lullo, Alain Joliot, Edmond Dupont, Kenneth L. Moya and Alain Prochiantz
Pharmacological Reviews January 1, 2013, 65 (1) 90-104; DOI: https://doi.org/10.1124/pr.112.006577

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Review ArticleReview Article

Homeoprotein Signaling in Development, Health, and Disease

Julien Spatazza, Elizabeth Di Lullo, Alain Joliot, Edmond Dupont, Kenneth L. Moya and Alain Prochiantz
Pharmacological Reviews January 1, 2013, 65 (1) 90-104; DOI: https://doi.org/10.1124/pr.112.006577
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  • Article
    • Abstract
    • I. Introduction: The History of Homeoprotein Transduction
    • II. Penetratin, Homeodomain, and Homeoprotein Internalization
    • III. Homeoprotein Secretion
    • IV. Non–Cell Autonomous Homeoprotein Activity in Pattern Formation
    • V. Non–Cell Autonomous Homeoprotein Activity in Axon Guidance and Cell Migration
    • VI. Non–Cell Autonomous Homeoprotein Activity in the Regulation of Cortex Plasticity
    • VII. Homeoprotein Signal Transduction Pathways
    • VIII. Therapeutic Homeoproteins
    • IX. Conclusion: The Future of Homeoprotein Transduction
    • Acknowledgments
    • Authorship contributions
    • Footnotes
    • Abbreviations
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