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Par6α signaling controls glial-guided neuronal migration

Nature Neuroscience volume 7, pages 1195–1203 (2004)Cite this article

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Abstract

Neuronal migrations along glial fibers provide a primary pathway for the formation of cortical laminae. To examine the mechanisms underlying glial-guided migration, we analyzed the dynamics of cytoskeletal and signaling components in living neurons. Migration involves the coordinated two-stroke movement of a perinuclear tubulin 'cage' and the centrosome, with the centrosome moving forward before nuclear translocation. Overexpression of mPar6α disrupts the perinuclear tubulin cage, retargets PKCζ and γ-tubulin away from the centrosome, and inhibits centrosomal motion and neuronal migration. Thus, we propose that during neuronal migration the centrosome acts to coordinate cytoskeletal dynamics in response to mPar6α-mediated signaling.

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Figure 1: The structure of the microtubule cytoskeleton of purified cerebellar granule cells.
Figure 2: FRAP analysis of Venus–α-tubulin turnover within the cage.
Figure 3: mPar6α and p50 dynactin label the neuronal centrosome.
Figure 4: Movement of the centrosome and nucleus are tightly coordinated in migrating neurons.
Figure 5: Perturbation of mPar6α signaling or dynein activity inhibits granule neuron axon-extension and disrupts the perinuclear microtubule cage.
Figure 6: mPar6α overexpression inhibits centrosomal movement.
Figure 7: shRNA-mediated knockdown of mPar6α perturbs centrosomal organization and positioning.
Figure 8: Overexpression of mPar6α or p50 dynactin inhibits glial-guided migration.

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  • 17 October 2004

    added note to xml beneath the Acknowledgments section; appended AOP version of PDF; print version will be correct

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Acknowledgements

We thank A. Miyawaki (RIKEN Brain Science Institute; Saitama, Japan) for generously sharing Venus, C. Waterman-Storer (Scripps Research Institute, La Jolla, California) for insightful discussions and critical reading of the manuscript, Y. Fang for expert technical assistance, N. Didkovsky for three-dimensional reconstruction of our imaging data sets, K. Zimmerman and J.H. Kim for critical reading of the manuscript, and A. North and the Rockefeller University Bioimaging facility for use of the spinning disk confocal microscope and expert technical advice. Antibodies were generously supplied by J. Fawcett (anti-mPar6α; Mount Sinai Hospital, Toronto, Canada) and R.B. Vallee (anti–dynein intermediate chain; Columbia University, New York). This work was supported by US National Institutes of Health grant R015925-26 to M.E.H. This paper is dedicated to the memory of Rodolfo Rivas, who discovered the perinuclear tubulin cage.

*Note: The version of this article that was published online on October 10, 2004 misstated the supporting National Institutes of Health grant number in the Acknowledgments. The correct grant number is RO1 NS15429-24A1. The online version was corrected on October 17, 2004, and the printed version of the article is correct. This change affects the HTML and PDF versions of the article; print will be corrected before publication.

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Authors and Affiliations

  1. Laboratory of Developmental Neurobiology, The Rockefeller University, New York, 10021, New York, USA

    David J Solecki, Lynn Model & Mary E Hatten

  2. Laboratory of Chemistry and Cell Biology, The Rockefeller University, New York, 10021, New York, USA

    Jedidiah Gaetz & Tarun M Kapoor

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Correspondence to Mary E Hatten.

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Supplementary information

Supplementary Fig. 1

Schematic of retroviral expression vectors and quantification of mPar6α expression. (A) Schematic of retroviral vectors used in these studies. (B) Quantitation of mPar6 protein produced by retroviral and transfection methods. Purified cerebellar granule neurons expressing Venus-mPar6α via retroviral infection or transfected expression vector were fixed and stained with anti-GFP and anti-Par6 antibodies. The fluorescence intensity of the mPar6 immunoreactivity was then measured in control (non-infected or non-transfected cells), retrovirally infected or transfected cells. The intensity of mPar6 immunoreactivity in control cells was normalized to one and the levels yielded by two heterologous expression methods were then plotted relative to that value. Retroviral expression resulted in mPar6 expression levels 2 times of the endogenous level, while transfection yielded 6.7 times the endogenous level. (PDF 63 kb)

Supplementary Fig. 2

Venus-mPar6α is a centrosomal component in primary cerebellar astro-glial cells. (A) Localization of Venus-mPar6α in a live astroglial cell. Mixed cerebellar culture was infected with Venus-mPar6α retrovirus, cultured for 48 hours and then examined with a spinning disk confocal microscope. A single punctate organelle was observed in astroglial cells similar to what was observed in cerebellar granule neurons. (B) Purified astroglial cells were infected with Venus-mPar6α retrovirus cultured for 48 hours and then stained with anti-GFP and anti-γ-tubulin antibodies. The immunoreactivity of Venus-mPar6α co-localizes with γ-tubulin, indicating that Venus-mPar6α is a centrosomal component in purified astroglial cells. (C) Purified granule neurons transfected with Venus-mPar6α were stained with anti-GFP, antiβ-tubulin and anti-pericentrin antibodies. Disintegration of the cage and a reduction of pericentrin recruitment to the centrosome are seen in Venus-mPar6α expressing cells, but not in the neighboring non-transfected cell. (PDF 182 kb)

Supplementary Fig. 3

Dynein intermediate chain is localized to the neuronal centrosome. (A) Cerebellar granule neurons were immuno-stained with anti-dynein intermediate chain and anti-a-tubulin antibodies. The predominant dynein intermediate chain labeled structure within the neuronal soma appears at points where the microtubule cytoskeleton is nucleated suggesting that the structure labeled is the centrosome. (B) Cerebellar granule neurons were immunostained with anti-dynein intermediate chain and anti-γ-tubulin antibodies. The predominant dynein intermediate chain labeled structure within the neuronal soma strongly co-localizes with γ-tubulin immunoreactivity. (PDF 166 kb)

Supplementary Fig. 4

Model of a neuron migrating along a glial fiber. Neurons migrate along glial fibers towards their destinations within cortical regions of the developing brain. Within the migrating neuron's soma, tubulin is organized into a perinuclear cage while the centrosome is located just forward of the cage and nucleus. Our studies reveal that as a neuron is migrates along a glial fiber, the cage undergoes complex architectural rearrangements and a highly orchestrated cycle of centrosomal and nuclear movement occurs that is reminiscent of a two-stroke engine. There are two potential mechanisms for nuclear translocation that are consistent with our live imaging data: the centrosome could pull the nucleus forward or molecular motors (i.e. dynein, see Fig. 3) associated with the nucleus could transport the nucleus forward along the microtubules of the perinuclear cage. mPar6α and p50 dynactin are both associated with the centrosome. Our studies show that mPar6α signaling at the centrosome, potentially mediated by PKCz, plays a critical role in organizing the cytoskeleton of migrating neurons. This suggests a broader role for the centrosome in neuronal migration as a signaling center that modulates cytoskeletal dynamics in response to extracellular signaling pathways. (PDF 180 kb)

Supplementary Video 1

The microtubule cytoskeleton of an actively migrating neuron. Purified cerebellar granule neurons were labeled with Ven-α-tubulin and cultured with cerebellar glia. The perinuclear cage of microtubules undergoes complex architectural rearrangements as the soma progressively migrates along the glial fiber. Images from this sequence were used in Fig. 1b. Total elapsed time was 45 min. (MPG 1350 kb)

Supplementary Video 2

The microtubule cytoskeleton of a stationary neuron. Purified cerebellar granule neurons were labeled with Ven-α-tubulin and cultured on a Matrigel-coated culture surface. Although stationary neurons had a perinuclear cage of microtubules the cage remains compact and does not change shape. Microtubule dynamics are evident in the growth cone at the end of the extending axon. Images from this sequence were used in Fig. 1c. Total elapsed time was 8 min. (MPG 590 kb)

Supplementary Video 3

FRAP analysis of the perinuclear cage. Purified cerebellar granule neurons were labeled with Ven-α-tubulin and cultured with cerebellar glia. The perinuclear cage was subjected to 100 iterations of a 541 nm laser line. Images were acquired every 15 s subsequent to the bleach protocol. Nearly full recovery occurred in 208 s. Images from this sequence were used in Fig. 2a. Total elapsed time was 240 s. (MPG 310 kb)

Supplementary Video 4

Centrosomal and nuclear motion in a migrating neuron. Purified cerebellar granule neurons were labeled with Ven-mPar6α and cultured with cerebellar glia. Movement of the centrosome precedes nuclear movement. Images from this sequence were used in Fig. 4a. Total elapsed time was 6 min. (MPG 478 kb)

Supplementary Video 5

Centrosomal and nuclear motion in a stationary neuron. Purified cerebellar granule neurons were labeled with Ven-mPar6α and cultured with cerebellar glia. The neuron depicted in Supplementary Video 4 later stalls and was imaged again to observe centrosomal motion in a stationary neuron. The centrosome and nucleus oscillated non-productively when the cell was stationary, a stark contrast to what was observed when the cells was in motion. Images from this sequence were used in Fig. 4b. Total elapsed time was nearly 6 min. (MPG 519 kb)

Supplementary Video 6

Movement of p50 dynactin labeled centrosome within a migrating neuron. Purified cerebellar granule neurons were labeled with p50 dynactin-Venus and cultured with cerebellar glia. As was seen with Ven-mPar6α labeled centrosomes, the p50 dynactin labeled centrosome initiated forward movement before nuclear movement. Total elapsed time was 5 min. (MPG 590 kb)

Supplementary Video 7

Random centrosomal movements in a stationary neuron. Purified cerebellar granule neurons were labeled with p50 dynactin-Venus and cultured with cerebellar glia. The centrosome randomly moves within in the soma of a stationary neuron. The movements do not correlate to any forward movement of the soma. Elapsed time was 11 min. (MPG 839 kb)

Supplementary Video 8

Three-dimensional reconstruction the perinuclear cage of a cells transfected with Ven-mPar6α. Of the three cells in the field the top one was transfected with Ven-mPar6α, while the two adjacent cells on the bottom of the field were not transfected and had normal perinuclear cages. Rotation of the reconstructed cells reveals the severity of the degradation of the perinuclear cage. (MPG 4579 kb)

Supplementary Video 9

Centrin2-Venus labeled structures do not move in mPar6α over-expressing cells. Purified cerebellar granule neurons were labeled with Centrin2-Venus and electroporated with pRK5-dsRed-mPar6α. Centrin2 labeled structures are diffuse and remain stationary indicating that perturbation of mPar6α signaling inhibits centrosomal positioning events. Images from this sequence were used in Fig. 6b. Total elapsed time was 11 min. (MPG 5232 kb)

Supplementary Video 10

Centrosomal motion in Centrin2 labeled cells. This time-lapse sequence depicts centrosomal motion in two non-electroporated cells from the same field as Movie S9. Although these cells do not undergo directed migration, Centrin2 labeled centrosomes display motility and rapidly change position. Images from this sequence were used in Fig. 6C. Total elapsed time was eleven minutes. (MPG 866 kb)

Supplementary Video 11

Centrosomal motion in cells taking up low amounts of a Par6 shRNA. Purified cerebellar granule neurons were electroporated with pScarlet_Par6 shRNA and pRK5 Centrin2-Venus. This cell displayed weak red fluorescence indicating it took up a low amount of pScarlet_Par6 shRNA during electroporation. The Centrin2 labeled centrosome display motility and rapidly change position. Images from this sequence were used in Fig. 7c. Total elapsed time was 11 min. (MPG 683 kb)

Supplementary Video 12

Centrosomal motion in cells taking up high amounts of a Par6 shRNA. Purified cerebellar granule neurons were electroporated with pScarlet_Par6 shRNA and pRK5 Centrin2-Venus. This cell displayed strong red fluorescence indicating it took up a high amount of pScarlet_Par6 shRNA during electroporation. Individual centrioles could not be distinguished and centrosomes were motionless. Images from this sequence were used in Fig. 7c. Total elapsed time was 11 min. (MPG 683 kb)

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Solecki, D., Model, L., Gaetz, J. et al. Par6α signaling controls glial-guided neuronal migration. Nat Neurosci 7, 1195–1203 (2004). https://doi.org/10.1038/nn1332

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