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J Cell Sci. 2016 Sep 1;129(17):3282-94. doi: 10.1242/jcs.187294. Epub 2016 Jul 15.

Drosophila Ringmaker regulates microtubule stabilization and axonal extension during embryonic development.

Author information

1
Department of Physiology, University of Texas School of Medicine, Health Science Center, San Antonio, TX 78229, USA.
2
Department of Biology, University of North Carolina, Chapel Hill, NC 27599, USA.
3
Department of Pharmacology, University of Texas School of Medicine, Health Science Center, San Antonio, TX 78229, USA.
4
Department of Pharmacology, University of Texas School of Medicine, Health Science Center, San Antonio, TX 78229, USA Department of Medicine, University of California, San Diego, CA 92093, USA.
5
Department of Physiology, University of Texas School of Medicine, Health Science Center, San Antonio, TX 78229, USA bhatm@uthscsa.edu.

Abstract

Axonal growth and targeting are fundamental to the organization of the nervous system, and require active engagement of the cytoskeleton. Polymerization and stabilization of axonal microtubules is central to axonal growth and maturation of neuronal connectivity. Studies have suggested that members of the tubulin polymerization promoting protein (TPPP, also known as P25α) family are involved in cellular process extension. However, no in vivo knockout data exists regarding its role in axonal growth during development. Here, we report the characterization of Ringmaker (Ringer; CG45057), the only Drosophila homolog of long p25α proteins. Immunohistochemical analyses indicate that Ringer expression is dynamically regulated in the embryonic central nervous system (CNS). ringer-null mutants show cell misplacement, and errors in axonal extension and targeting. Ultrastructural examination of ringer mutants revealed defective microtubule morphology and organization. Primary neuronal cultures of ringer mutants exhibit defective axonal extension, and Ringer expression in cells induced microtubule stabilization and bundling into rings. In vitro assays showed that Ringer directly affects tubulin, and promotes microtubule bundling and polymerization. Together, our studies uncover an essential function of Ringer in axonal extension and targeting through proper microtubule organization.

KEYWORDS:

Axon growth; Cytoskeleton; Microtubules; Nervous system; TPPP; Tubulin polymerization; Tubulin stabilization

PMID:
27422099
PMCID:
PMC5047701
DOI:
10.1242/jcs.187294
[Indexed for MEDLINE]
Free PMC Article

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