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Developmentally programmed germ cell remodelling by endodermal cell cannibalism

Nature Cell Biology volume 18, pages 1302–1310 (2016)Cite this article

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Abstract

Primordial germ cells (PGCs) in many species associate intimately with endodermal cells, but the significance of such interactions is largely unexplored. Here, we show that Caenorhabditis elegans PGCs form lobes that are removed and digested by endodermal cells, dramatically altering PGC size and mitochondrial content. We demonstrate that endodermal cells do not scavenge lobes PGCs shed, but rather, actively remove lobes from the cell body. CED-10 (Rac)-induced actin, DYN-1 (dynamin) and LST-4 (SNX9) transiently surround lobe necks and are required within endodermal cells for lobe scission, suggesting that scission occurs through a mechanism resembling vesicle endocytosis. These findings reveal an unexpected role for endoderm in altering the contents of embryonic PGCs, and define a form of developmentally programmed cell remodelling involving intercellular cannibalism. Active roles for engulfing cells have been proposed in several neuronal remodelling events, suggesting that intercellular cannibalism may be a more widespread method used to shape cells than previously thought.

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Figure 1: PGC lobes form autonomously and are digested by endodermal cells.
Figure 2: Lobe loss remodels PGC contents.
Figure 3: Endodermal cells actively remove PGC lobes.
Figure 4: Endodermal cell CED-10 induces actin formation to promote lobe scission.
Figure 5: Endodermal LST-4 and dynamin act to promote lobe scission.
Figure 6: A pathway for lobe scission.

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Acknowledgements

We thank the Caenorhabditis Genetics Center (CGC), National Bioresource Project (NBRP), and Z. Zhou (Baylor College of Medicine, USA) for providing worm strains. Caged rhodamine dextran was a gift from K. Oegema (University of California, San Diego). We thank T. Hurd (NYU School of Medicine, USA) for sharing TMRE dye and mitochondrial discussion; J. H. Choi (NYU School of Medicine, USA) for assistance in developing the technique for cell culture experiments; D. McIntyre (NYU School of Medicine, USA) for designing a nitrogen gas immobilization chamber for embryos; and L. Christiaen (New York University, USA), N. Ringstad (NYU School of Medicine, USA), T. Hurd (NYU School of Medicine, USA) and members of the Nance laboratory for comments on the manuscript. Library preparation and sequencing of genomic DNA samples was performed at the NYULMC Genome Technology Center, which is partially supported by a Cancer Center Support Grant (P30CA016087) at the Laura and Isaac Perlmutter Cancer Center. Funding was provided by the NIH (R35GM118081, R21HD084809 to J.N.), NYSTEM (C029561 to J.N.) and HHMI (J.M.H., T.-L.C). Y.A. is an HHMI International Student Research fellow.

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Authors and Affiliations

  1. Helen L. and Martin S. Kimmel Center for Biology and Medicine at the Skirball Institute of Biomolecular Medicine, NYU School of Medicine, New York, New York 10016, USA

    Yusuff Abdu, Chelsea Maniscalco & Jeremy Nance

  2. Advanced Imaging Center, Janelia Research Campus, Howard Hughes Medical Institute, Ashburn, Virginia 20147, USA

    John M. Heddleston & Teng-Leong Chew

  3. Department of Cell Biology, NYU School of Medicine, New York, New York 10016, USA

    Jeremy Nance

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  1. Yusuff Abdu
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  2. Chelsea Maniscalco
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Contributions

Y.A. and J.N. designed experiments. C.M. performed and analysed cell culture, MOMA-1 imaging, and end-1 end-3 embryo experiments. Y.A. performed and analysed all other experiments, and J.H. and T.-L.C. assisted with experiments on the lattice light-sheet microscope. Y.A. and J.N. wrote the manuscript.

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Correspondence to Jeremy Nance.

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Integrated supplementary information

Supplementary Figure 1 PGC lobe digestion by endoderm.

(a–a’) A newly hatched L1 larva (body outlined). PGC debris (arrowheads) can be seen inside endodermal cells (intestinal rings V and VI). Scale bar, 5 μm.

Supplementary Figure 2 Characterization of mitochondrial dyes.

(a–a’) MitoSOX shows stronger labeling in PGCs (one shown, magenta) compared to most somatic cells in the embryo. Asterisk denotes dye accumulation at hole made in eggshell to introduce dye. (b) MitoTracker Green (b’) and MitoSOX (b”) colocalize in embryonic mitochondria. (c) MitoTracker Green (c’) and TMRE (c”) colocalize to mitochondria in embryonic mitochondria. Scale bar, 5 μm.

Supplementary Figure 3 Rhodamine Dextran diffusion from cell bodies into lobes.

(a–b”) Photoactivation of caged Rhodamine Dextran in wild-type L1 larva. Photoactivation in a single PGC (a’,b’) is followed by diffusion into the adjacent PGC (PGCs are connected by a cytoplasmic bridge) (a”, b”, 9/9 embryos). (c–d”) Photoactivation of caged Rhodamine Dextran in end-1 end-3 L1 larva. Photoactivation in a single PGC (c’,d’) is followed by diffusion into persistent lobes and the adjacent PGC (c”, d”, 8/8 embryos). Some caged Rhodamine Dextran becomes uncaged independently of photoactivation, and is visible as stable bright spots in the pre-photoactivation channel. Scale bar, 5 μm.

Supplementary Figure 4 ced-10 in lobe scission.

(a–a’) ced-10(n1993) mutant L1 larva with mosaic rescue by ced-10(+)END. The rescuing ced-10(+)END extrachromosomal array, which also expresses nuclear SUR-5-GFP, was lost in the Ea endodermal lineage [inset; lost in cells of intestinal ring V (white arrow), and retained in cells of intestinal ring VI (green arrow)]. (b) Schematic of endodermal cell lineage with placements of cells in intestinal rings shown below and reflecting the mosaic pattern seen in a; adapted from60. Green cells indicate cells with rescue array while grey cells represent loss of array. Two mosaics were found with this loss pattern, and both mosaics showed persistent lobes in intestinal ring V (white arrowhead in inset) and lobe debris in intestinal ring VI. 11/11 intestinal mosaic L1 larvae had persistent lobes. (c) Quantification of PGC volume (cell body + lobes) in wild type, ced-10 mutants and ced-10 mutants with ced-10(+)END (WT, n = 14 embryos/L1 larvae; ced-10 mutants, n = 14 embryos/ L1 larvae; ced-10(+)END,n = 14 embryos/L1 larvae. ∗∗∗P < 0.001, Student’s t-test, mean ± s.d.). Data shown is from a single independent experiment. Source data for repeat experiments is provided in Supplementary Table 3. (d) ced-10(tm597) null mutant L1 larva with mosaic rescue ced-10ALL. Rescue is lost in the intestinal ring V, where a PGC lobe persists (arrowhead). 32/32 intestinal mosaic L1 larvae had persistent lobes. Scale bar, 5 μm.

Supplementary Figure 5 lst-4 in lobe scission.

(a) lst-4( +) rescue of persistent lobes in lst-4(xn45)mutants; arrowheads point to lobe debris (4/4 extrachromosomal arrays completely rescued persistent lobes, n = 13–28 L1 larvae examined per array). (b) Quantification of PGC volume (cell body + lobes) in L1 larvae of lst-4(xn45)mutants (n = 10 L1 larvae) and lst-4(xn45) mutants with lst-4( +)(n = 10 L1 larvae), ∗∗∗P < 0.001, Student’s t-test, mean ± s.d. Data shown is from a single independent experiment. Source data for repeat experiments is provided in Supplementary Table 3. (c) Percent recovered lobes in FRAP experiment on persistent lobes in lst-4(xn45) (n = 18 L1 larvae) and lst-4 (RNAi) (n = 18 L1 larvae) L1 larvae. (d) lst-4 gene structure (isoform c, Wormbase WS252). Gray rectangles are coding exons, white rectangle is the 3′ UTR, and chevrons are introns. Regions of the gene encoding the SH3, PX and BAR domains are indicated. The xn45 lesion mutates a splice donor base within an intron in the region encoding the BAR domain. Scale bar, 5 μm.

Supplementary information

Supplementary Information

Supplementary Information (PDF 949 kb)

Supplementary Table 1

Supplementary Information (XLSX 30 kb)

Supplementary Table 2

Supplementary Information (XLSX 34 kb)

Supplementary Table 3

Supplementary Information (XLSX 40 kb)

PGC lobe formation.

Embryo is oriented posterior to the left, and turns from a ventral view to a lateral view (dorsal up) as the movie progresses. PGC and endodermal cell membranes are labeled. PGC lobes (‘L’) begin forming ∼50 min into the movie and embed into endodermal cells. (AVI 2026 kb)

Rendering of PGC lobes embedded into endodermal cells.

Rendered data from a 2-fold embryo expressing endoderm and PGC surface markers. PGCs (magenta) extend lobes into adjacent endodermal cells (green). (AVI 4401 kb)

Lobe formation in a cultured PGC.

PGC membranes and nucleus are labeled. The nucleus moves to one side of the cell and lobe (‘L’) extends from the opposite side beginning at ∼150 min into the movie. (AVI 119 kb)

P granule movement into PGC lobes.

Embryo is oriented posterior to the left. Before lobe formation, all P granules (PGL-1-RFP) are found at the nuclear periphery. A P granule can be seen detaching from the nuclear periphery and moving into the lobe (‘L’) beginning at 42 min into the movie. (AVI 4342 kb)

Mitochondria in PGC lobes.

Embryo is oriented posterior to the left. All cell membranes are labeled with GFP (PGC membranes are brighter), and mitochondria within PGCs are labeled with mCh-MOMA-1 (green and red channels were switched). Both PGCs are initially visible, then one moves out of the focal plane. Lobe formation begins 16 min into the movie, and mitochondria can be seen localizing preferentially to the lobe (‘L’). (AVI 673 kb)

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Abdu, Y., Maniscalco, C., Heddleston, J. et al. Developmentally programmed germ cell remodelling by endodermal cell cannibalism. Nat Cell Biol 18, 1302–1310 (2016). https://doi.org/10.1038/ncb3439

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