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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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References

  1. Cinalli, R. M., Rangan, P. & Lehmann, R. Germ cells are forever. Cell 132, 559–562 (2008).

    Article  CAS  PubMed  Google Scholar 

  2. Seydoux, G. & Braun, R. E. Pathway to totipotency: lessons from germ cells. Cell 127, 891–904 (2006).

    Article  CAS  PubMed  Google Scholar 

  3. Molyneaux, K. A., Stallock, J., Schaible, K. & Wylie, C. Time-lapse analysis of living mouse germ cell migration. Dev. Biol. 240, 488–498 (2001).

    Article  CAS  PubMed  Google Scholar 

  4. Takamura, K., Fujimura, M. & Yamaguchi, Y. Primordial germ cells originate from the endodermal strand cells in the ascidian Ciona intestinalis. Dev. Genes Evol. 212, 11–18 (2002).

    Article  CAS  PubMed  Google Scholar 

  5. Chihara, D. & Nance, J. An E-cadherin-mediated hitchhiking mechanism for C. elegans germ cell internalization during gastrulation. Development 139, 2547–2556 (2012).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  6. DeGennaro, M. et al. Peroxiredoxin stabilization of DE-cadherin promotes primordial germ cell adhesion. Dev. Cell 20, 233–243 (2011).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  7. Sulston, J. E., Schierenberg, E., White, J. G. & Thomson, J. N. The embryonic cell lineage of the nematode Caenorhabditis elegans. Dev. Biol. 100, 64–119 (1983).

    Article  CAS  PubMed  Google Scholar 

  8. Rohrschneider, M. R. & Nance, J. The union of somatic gonad precursors and primordial germ cells during Caenorhabditis elegans embryogenesis. Dev. Biol. 379, 139–151 (2013).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  9. Owraghi, M., Broitman-Maduro, G., Luu, T., Roberson, H. & Maduro, M. F. Roles of the Wnt effector POP-1/TCF in the C. elegans endomesoderm specification gene network. Dev. Biol. 340, 209–221 (2010).

    Article  CAS  PubMed  Google Scholar 

  10. Strome, S. & Wood, W. B. Immunofluorescence visualization of germ-line-specific cytoplasmic granules in embryos, larvae, and adults of Caenorhabditis elegans. Proc. Natl Acad. Sci. USA 79, 1558–1562 (1982).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  11. Head, B. P., Zulaika, M., Ryazantsev, S. & van der Bliek, A. M. A novel mitochondrial outer membrane protein, MOMA-1, that affects cristae morphology in Caenorhabditis elegans. Mol. Biol. Cell 22, 831–841 (2011).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  12. Rolland, S. G., Lu, Y., David, C. N. & Conradt, B. The BCL-2-like protein CED-9 of C. elegans promotes FZO-1/Mfn1,2- and EAT-3/Opa1-dependent mitochondrial fusion. J. Cell Biol. 186, 525–540 (2009).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  13. Yang, W. & Hekimi, S. A mitochondrial superoxide signal triggers increased longevity in Caenorhabditis elegans. PLoS Biol. 8, e1000556 (2010).

    Article  PubMed  PubMed Central  Google Scholar 

  14. Chen, B. C. et al. Lattice light-sheet microscopy: imaging molecules to embryos at high spatiotemporal resolution. Science 346, 1257998 (2014).

    Article  PubMed  PubMed Central  Google Scholar 

  15. Reddien, P. W. & Horvitz, H. R. CED-2/CrkII and CED-10/Rac control phagocytosis and cell migration in Caenorhabditis elegans. Nat. Cell Biol. 2, 131–136 (2000).

    Article  CAS  PubMed  Google Scholar 

  16. Lundquist, E. A., Reddien, P. W., Hartwieg, E., Horvitz, H. R. & Bargmann, C. I. Three C. elegans Rac proteins and several alternative Rac regulators control axon guidance, cell migration and apoptotic cell phagocytosis. Development 128, 4475–4488 (2001).

    CAS  PubMed  Google Scholar 

  17. Kinchen, J. M. et al. Two pathways converge at CED-10 to mediate actin rearrangement and corpse removal in C. elegans. Nature 434, 93–99 (2005).

    Article  CAS  PubMed  Google Scholar 

  18. Wang, X. & Yang, C. Programmed cell death and clearance of cell corpses in Caenorhabditis elegans. Cell Mol. Life Sci. 73, 2221–2236 (2016).

    Article  CAS  PubMed  Google Scholar 

  19. Shin, N. et al. SNX9 regulates tubular invagination of the plasma membrane through interaction with actin cytoskeleton and dynamin 2. J. Cell Sci. 121, 1252–1263 (2008).

    Article  CAS  PubMed  Google Scholar 

  20. Lundmark, R. & Carlsson, S. R. Sorting nexin 9 participates in clathrin-mediated endocytosis through interactions with the core components. J. Biol. Chem. 278, 46772–46781 (2003).

    Article  CAS  PubMed  Google Scholar 

  21. McMahon, H. T. & Boucrot, E. Molecular mechanism and physiological functions of clathrin-mediated endocytosis. Nat. Rev. Mol. Cell Biol. 12, 517–533 (2011).

    Article  CAS  PubMed  Google Scholar 

  22. Almendinger, J. et al. A conserved role for SNX9-family members in the regulation of phagosome maturation during engulfment of apoptotic cells. PLoS ONE 6, e18325 (2011).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  23. Chen, D. et al. Clathrin and AP2 are required for phagocytic receptor-mediated apoptotic cell clearance in Caenorhabditis elegans. PLoS Genet. 9, e1003517 (2013).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  24. Cheng, S. et al. PtdIns(4,5)P(2) and PtdIns3P coordinate to regulate phagosomal sealing for apoptotic cell clearance. J. Cell Biol. 210, 485–502 (2015).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  25. Lu, N., Shen, Q., Mahoney, T. R., Liu, X. & Zhou, Z. Three sorting nexins drive the degradation of apoptotic cells in response to PtdIns(3)P signaling. Mol. Biol. Cell 22, 354–374 (2011).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  26. Yu, X., Odera, S., Chuang, C. H., Lu, N. & Zhou, Z. C. elegans dynamin mediates the signaling of phagocytic receptor CED-1 for the engulfment and degradation of apoptotic cells. Dev. Cell 10, 743–757 (2006).

    Article  CAS  PubMed  Google Scholar 

  27. Lundmark, R. & Carlsson, S. R. Regulated membrane recruitment of dynamin-2 mediated by sorting nexin 9. J. Biol. Chem. 279, 42694–42702 (2004).

    Article  CAS  PubMed  Google Scholar 

  28. Soulet, F., Yarar, D., Leonard, M. & Schmid, S. L. SNX9 regulates dynamin assembly and is required for efficient clathrin-mediated endocytosis. Mol. Biol. Cell 16, 2058–2067 (2005).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  29. Yarar, D., Waterman-Storer, C. M. & Schmid, S. L. SNX9 couples actin assembly to phosphoinositide signals and is required for membrane remodeling during endocytosis. Dev. Cell 13, 43–56 (2007).

    Article  CAS  PubMed  Google Scholar 

  30. Badour, K. et al. Interaction of the Wiskott-Aldrich syndrome protein with sorting nexin 9 is required for CD28 endocytosis and cosignaling in T cells. Proc. Natl Acad. Sci. USA 104, 1593–1598 (2007).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  31. Taylor, M. J., Perrais, D. & Merrifield, C. J. A high precision survey of the molecular dynamics of mammalian clathrin-mediated endocytosis. PLoS Biol. 9, e1000604 (2011).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  32. Baugh, L. R. To grow or not to grow: nutritional control of development during Caenorhabditis elegans L1 arrest. Genetics 194, 539–555 (2013).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  33. Fukuyama, M. et al. C. elegans AMPKs promote survival and arrest germline development during nutrient stress. Biol. Open. 1, 929–936 (2012).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  34. Wolf, T., Qi, W., Schindler, V., Runkel, E. D. & Baumeister, R. Doxycyclin ameliorates a starvation-induced germline tumor in C. elegans daf-18/PTEN mutant background. Exp. Gerontol. 56, 114–122 (2014).

    Article  CAS  PubMed  Google Scholar 

  35. Wolke, U., Jezuit, E. A. & Priess, J. R. Actin-dependent cytoplasmic streaming in C. elegans oogenesis. Development 134, 2227–2236 (2007).

    Article  CAS  PubMed  Google Scholar 

  36. Lei, L. & Spradling, A. C. Mouse oocytes differentiate through organelle enrichment from sister cyst germ cells. Science 352, 95–99 (2016).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  37. Cox, R. T. & Spradling, A. C. A Balbiani body and the fusome mediate mitochondrial inheritance during Drosophila oogenesis. Development 130, 1579–1590 (2003).

    Article  CAS  PubMed  Google Scholar 

  38. Chu, D. S. & Shakes, D. C. Spermatogenesis. Adv. Exp. Med. Biol. 757, 171–203 (2013).

    Article  CAS  PubMed  Google Scholar 

  39. Kevany, B. M. & Palczewski, K. Phagocytosis of retinal rod and cone photoreceptors. Physiology (Bethesda) 25, 8–15 (2010).

    CAS  Google Scholar 

  40. Corty, M. M. & Freeman, M. R. Cell biology in neuroscience: architects in neural circuit design: glia control neuron numbers and connectivity. J. Cell Biol. 203, 395–405 (2013).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  41. Schafer, D. P. et al. Microglia sculpt postnatal neural circuits in an activity and complement-dependent manner. Neuron 74, 691–705 (2012).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  42. Han, C. et al. Epidermal cells are the primary phagocytes in the fragmentation and clearance of degenerating dendrites in Drosophila. Neuron 81, 544–560 (2014).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  43. Wehman, A. M., Poggioli, C., Schweinsberg, P., Grant, B. D. & Nance, J. The P4-ATPase TAT-5 inhibits the budding of extracellular vesicles in C. elegans embryos. Curr. Biol. 21, 1951–1959 (2011).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  44. Treusch, S. et al. Caenorhabditis elegans functional orthologue of human protein h-mucolipin-1 is required for lysosome biogenesis. Proc. Natl Acad. Sci. USA 101, 4483–4488 (2004).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  45. Shirayama, M. et al. piRNAs initiate an epigenetic memory of nonself RNA in the C. elegans germline. Cell 150, 65–77 (2012).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  46. Chen, C. C. RAB-10 is required for endocytic recycling in the Caenorhabditis elegans intestine. Mol. Biol. Cell 17, 1286–1297 (2006).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  47. Kamath, R. S., Martinez-Campos, M., Zipperlen, P., Fraser, A. G. & Ahringer, J. Effectiveness of specific RNA-mediated interference through ingested double-stranded RNA in Caenorhabditis elegans. Genome Biol. 2, RESEARCH0002 (2001).

    CAS  PubMed  Google Scholar 

  48. Brenner, S. The genetics of Caenorhabditis elegans. Genetics 77, 71–94 (1974).

    CAS  PubMed  PubMed Central  Google Scholar 

  49. Minevich, G., Park, D. S., Blankenberg, D., Poole, R. J. & Hobert, O. CloudMap: a cloud-based pipeline for analysis of mutant genome sequences. Genetics 192, 1249–1269 (2012).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  50. Robinson, J. T. et al. Integrative genomics viewer. Nat. Biotechnol. 29, 24–26 (2011).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  51. Thorvaldsdottir, H., Robinson, J. T. & Mesirov, J. P. Integrative Genomics Viewer (IGV): high-performance genomics data visualization and exploration. Brief Bioinform. 14, 178–192 (2013).

    Article  CAS  PubMed  Google Scholar 

  52. Gibson, D. G. et al. Enzymatic assembly of DNA molecules up to several hundred kilobases. Nat. Methods 6, 343–345 (2009).

    Article  CAS  PubMed  Google Scholar 

  53. Nance, J., Munro, E. M. & Priess, J. R. C. elegans PAR-3 and PAR-6 are required for apicobasal asymmetries associated with cell adhesion and gastrulation. Development 130, 5339–5350 (2003).

    Article  CAS  PubMed  Google Scholar 

  54. Frokjaer-Jensen, C. et al. Single-copy insertion of transgenes in Caenorhabditis elegans. Nat. Genet. 40, 1375–1383 (2008).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  55. Armenti, S. T., Chan, E. & Nance, J. Polarized exocyst-mediated vesicle fusion directs intracellular lumenogenesis within the C. elegans excretory cell. Dev. Biol. 394, 110–121 (2014).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  56. Mello, C. C., Kramer, J. M., Stinchcomb, D. & Ambros, V. Efficient gene transfer in C. elegans extrachromosomal maintenance and integration of transforming sequences. EMBO J. 10, 3959–3970 (1991).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  57. Strange, K., Christensen, M. & Morrison, R. Primary culture of Caenorhabditis elegans developing embryo cells for electrophysiological, cell biological and molecular studies. Nat. Protoc. 2, 1003–1012 (2007).

    Article  CAS  PubMed  Google Scholar 

  58. Lynch, A. M. et al. A genome-wide functional screen shows MAGI-1 is an L1CAM-dependent stabilizer of apical junctions in C. elegans. Curr. Biol. 22, 1891–1899 (2012).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  59. Green, R. A. et al. The midbody ring scaffolds the abscission machinery in the absence of midbody microtubules. J. Cell Biol. 203, 505–520 (2013).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  60. Fukushige, T., Goszczynski, B., Yan, J. & McGhee, J. D. Transcriptional control and patterning of the pho-1 gene, an essential acid phosphatase expressed in the C. elegans intestine. Dev. Biol. 279, 446–461 (2005).

    Article  CAS  PubMed  Google Scholar 

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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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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

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Supplementary Table 1

Supplementary Information (XLSX 30 kb)

Supplementary Table 2

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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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