Lis1 and doublecortin function with dynein to mediate coupling of the nucleus to the centrosome in neuronal migration

doi:10.1083/jcb.200309025

Published online 1 June 2004. doi:10.1083/jcb.200309025
The Rockefeller University Press, 0021-9525 $8.00
JCB, Volume 165, Number 5, 709-721

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Article

Lis1 and doublecortin function with dynein to mediate coupling of the nucleus to the centrosome in neuronal migration

Teruyuki Tanaka¹, Finley F. Serneo¹, Christine Higgins¹^,2, Michael J. Gambello³, Anthony Wynshaw-Boris²^,3, and Joseph G. Gleeson¹^,2

¹ Department of Neurosciences, University of California, San Diego, La Jolla, CA 92093
² Graduate Program in Neurosciences, University of California, San Diego, La Jolla, CA 92093
³ Departments of Pediatrics and Medicine, University of California, San Diego, La Jolla, CA 92093

Address correspondence to Joseph G. Gleeson, University of California, San Diego, MTF 312, 9500 Gilman Drive, La Jolla, CA 92093-0624. Tel.: (858) 822-3535. Fax: (858) 534-1437. email: jogleeson{at}ucsd.edu

Humans with mutations in either DCX or LIS1 display nearly identicalneuronal migration defects, known as lissencephaly. To definesubcellular mechanisms, we have combined in vitro neuronal migrationassays with retroviral transduction. Overexpression of wild-typeDcx or Lis1, but not patient-related mutant versions, increasedmigration rates. Dcx overexpression rescued the migration defectin Lis1^+/– neurons. Lis1 localized predominantly to thecentrosome, and after disruption of microtubules, redistributedto the perinuclear region. Dcx outlined microtubules extendingfrom the perinuclear "cage" to the centrosome. Lis1^+/–neurons displayed increased and more variable separation betweenthe nucleus and the preceding centrosome during migration. Dyneininhibition resulted in similar defects in both nucleus–centrosome(N-C) coupling and neuronal migration. These N-C coupling defectswere rescued by Dcx overexpression, and Dcx was found to complexwith dynein. These data indicate Lis1 and Dcx function withdynein to mediate N-C coupling during migration, and suggestdefects in this coupling may contribute to migration defectsin lissencephaly.

Key Words: migration; Lis1; doublecortin; centrosome; nucleus

Abbreviations used in this paper: CETN2, centrin 2; DCX, doublecortin;DHC, dynein heavy chain; DIC, dynein intermediate chain; MT,microtubule; N-C, nucleus–centrosome; SNK, Student-Newman-Kleus;WT, wild type.

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