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Cited by 38Genomics and Chromatin DynamicsLipid metabolism and biosynthesisNuclear Structure and Function

Sequestration to lipid droplets promotes histone availability by preventing turnover of excess histones

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Stephenson, Roxan A., Thomalla, Jonathon M., Chen, Lili, Kolkhof, Petra, White, Roger P., Beller, Mathias, Welte, Michael A.·2021·Development
DOI 10.1242/dev.199381PMC PMC8380457

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Abstract

Because both dearth and overabundance of histones result in cellular defects, histone synthesis and demand are typically tightly coupled. In Drosophila embryos, histones H2B, H2A and H2Av accumulate on lipid droplets (LDs), which are cytoplasmic fat storage organelles. Without LD binding, maternally provided H2B, H2A and H2Av are absent; however, how LDs ensure histone storage is unclear. Using quantitative imaging, we uncover when during oogenesis these histones accumulate, and which step of accumulation is LD dependent. LDs originate in nurse cells (NCs) and are transported to the oocyte. Although H2Av accumulates on LDs in NCs, the majority of the final H2Av pool is synthesized in oocytes. LDs promote intercellular transport of the histone anchor Jabba and thus its presence in the ooplasm. Ooplasmic Jabba then prevents H2Av degradation, safeguarding the H2Av stockpile. Our findings provide insight into the mechanism for establishing histone stores during Drosophila oogenesis and shed light on the function of LDs as protein-sequestration sites.

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  1. Ables, E. T. (2015, Jan). Drosophila oocytes as a model for understanding meiosis: an educational primer to accompany "corolla is a novel protein that contributes to the architecture of the synaptonemal complex of Drosophila". Genetics, 199(1), 17-23. https://doi.org/10.1534/genetics.114.167940 · DOI
  2. Ambrosio, L., & Schedl, P. (1985). Two discrete modes of histone gene expression during oogenesis in Drosophila melanogaster. Developmental biology, 111(1), 220-231.
  3. Aramburu, J., Drews-Elger, K., Estrada-Gelonch, A., Minguillon, J., Morancho, B., Santiago, V., & Lopez-Rodriguez, C. (2006, Nov 30). Regulation of the hypertonic stress response and other cellular functions by the Rel-like transcription factor NFAT5. Biochem Pharmacol, 72(11), 1597-1604. https://doi.org/10.1016/j.bcp.2006.07.002 · DOI
  4. Bannister, A. J., & Kouzarides, T. (2011, Mar). Regulation of chromatin by histone modifications. Cell Res, 21(3), 381-395. https://doi.org/10.1038/cr.2011. · DOI
  5. Beller, M., Riedel, D., Jansch, L., Dieterich, G., Wehland, J., Jackle, H., & Kuhnlein, R. P. (2006, Jun). Characterization of the Drosophila lipid droplet subproteome. Mol Cell Proteomics, 5(6), 1082-1094. https://doi.org/10.1074/mcp.M600011-MCP200 · DOI
  6. Bersuker, K., Peterson, C. W. H., To, M., Sahl, S. J., Savikhin, V., Grossman, E. A., Nomura, D. K., & Olzmann, J. A. (2018, Jan 8). A Proximity Labeling Strategy Provides Insights into the Composition and Dynamics of Lipid Droplet Proteomes. Dev Cell, 44(1), 97-112 e117. https://doi.org/10.1016/j.devcel.2017.11.020 · DOI · Paper page
  7. Bozza, P. T., Magalhaes, K. G., & Weller, P. F. (2009, Jun). Leukocyte lipid bodies -Biogenesis and functions in inflammation. Biochim Biophys Acta, 1791(6), 540-551. https://doi.org/10.1016/j.bbalip.2009.01.005 · DOI
  8. Campos, E. I., Fillingham, J., Li, G., Zheng, H., Voigt, P., Kuo, W. H., Seepany, H., Gao, Z., Day, L. A., Greenblatt, J. F., & Reinberg, D. (2010, Nov). The program for processing newly synthesized histones H3.1 and H4. Nat Struct Mol Biol, 17(11), 1343-1351. https://doi.org/10.1038/nsmb.1911 · DOI
  9. Camus, G., Herker, E., Modi, A. A., Haas, J. T., Ramage, H. R., Farese, R. V., Jr., & Ott, M. (2013, Apr 5). Diacylglycerol acyltransferase-1 localizes hepatitis C virus NS5A protein to lipid droplets and enhances NS5A interaction with the viral capsid core. J Biol Chem, 288(14), 9915-9923. https://doi.org/10.1074/jbc.M112.434910 · DOI
  10. Celona, B., Weiner, A., Di Felice, F., Mancuso, F. M., Cesarini, E., Rossi, R. L., Gregory, L., Baban, D., Rossetti, G., Grianti, P., Pagani, M., Bonaldi, T., Ragoussis, J., Friedman, N., Camilloni, G., Bianchi, M. E., & Agresti, A. (2011, Jun). Substantial histone reduction modulates genomewide nucleosomal occupancy and global transcriptional output. PLoS Biol, 9(6), e1001086. https://doi.org/10.1371/journal.pbio.1001086 · DOI
  11. Cermelli, S., Guo, Y., Gross, S. P., & Welte, M. A. (2006, Sep 19). The lipid- droplet proteome reveals that droplets are a protein-storage depot. Curr Biol, 16(18), 1783-1795. https://doi.org/10.1016/j.cub.2006.07.062 · DOI
  12. Connolly, K., Rife, J. P., & Culver, G. (2008, Dec). Mechanistic insight into the ribosome biogenesis functions of the ancient protein KsgA. Mol Microbiol, 70(5), 1062-1075. https://doi.org/10.1111/j.1365-2958.2008.06485.x · DOI
  13. Eichhorn, S. W., Subtelny, A. O., Kronja, I., Kwasnieski, J. C., Orr-Weaver, T. L., & Bartel, D. P. (2016, Jul 30). mRNA poly(A)-tail changes specified by deadenylation broadly reshape translation in Drosophila oocytes and early embryos. Elife, 5. https://doi.org/10.7554/eLife.16955 · DOI
  14. Fadiga, J., & Nystul, T. G. (2019, Dec 18). The follicle epithelium in the Drosophila ovary is maintained by a small number of stem cells. Elife, 8. https://doi.org/10.7554/eLife.49050 · DOI
  15. Filipe, A., & McLauchlan, J. (2015, Jan). Hepatitis C virus and lipid droplets: finding a niche. Trends Mol Med, 21(1), 34-42. https://doi.org/10.1016/j.molmed.2014.11.003 · DOI
  16. Finn, R. M., Ellard, K., Eirin-Lopez, J. M., & Ausio, J. (2012, Dec). Vertebrate nucleoplasmin and NASP: egg histone storage proteins with multiple chaperone activities. FASEB J, 26(12), 4788-4804. https://doi.org/10.1096/fj.12-216663 · DOI
  17. Gallardo-Montejano, V. I., Saxena, G., Kusminski, C. M., Yang, C., McAfee, J. L., Hahner, L., Hoch, K., Dubinsky, W., Narkar, V. A., & Bickel, P. E. (2016, Aug 24). Nuclear Perilipin 5 integrates lipid droplet lipolysis with PGC- 1alpha/SIRT1-dependent transcriptional regulation of mitochondrial function. Nat Commun, 7, 12723. https://doi.org/10.1038/ncomms12723 · DOI
  18. Gaspar, I., & Szabad, J. (2009, Feb). In vivo analysis of MT-based vesicle transport by confocal reflection microscopy. Cell Motil Cytoskeleton, 66(2), 68-79. https://doi.org/10.1002/cm.20334 · DOI
  19. Gunjan, A., Paik, J., & Verreault, A. (2006, Apr). The emergence of regulated histone proteolysis. Curr Opin Genet Dev, 16(2), 112-118. https://doi.org/10.1016/j.gde.2006.02.010 · DOI
  20. Gunjan, A., & Verreault, A. (2003, Nov 26). A Rad53 kinase-dependent surveillance mechanism that regulates histone protein levels in S. cerevisiae. Cell, 115(5), 537-549. https://doi.org/10.1016/s0092- 8674(03)00896-1 · DOI
  21. Guruharsha, K., Obar, R. A., Mintseris, J., Aishwarya, K., Krishnan, R., Vijayraghavan, K., & Artavanis-Tsakonas, S. (2012). Drosophila Protein interaction Map (DPiM) A paradigm for metazoan protein complex interactions. Fly, 6(4), 246-253.
  22. Han, M., Chang, M., Kim, U. J., & Grunstein, M. (1987, Feb 27). Histone H2B repression causes cell-cycle-specific arrest in yeast: effects on chromosomal segregation, replication, and transcription. Cell, 48(4), 589- 597. https://doi.org/10.1016/0092-8674(87)90237-6 · DOI
  23. Herrero, A. B., & Moreno, S. (2011, May 18). Lsm1 promotes genomic stability by controlling histone mRNA decay. EMBO J, 30(10), 2008-2018. https://doi.org/10.1038/emboj.2011.117 · DOI
  24. Huang, L., Haratake, K., Miyahara, H., & Chiba, T. (2016). Proteasome activators, PA28γ and PA200, play indispensable roles in male fertility. Scientific reports, 6(1), 1-9.
  25. Hudson, A. M., & Cooley, L. (2010, Jan 11). Drosophila Kelch functions with Cullin-3 to organize the ring canal actin cytoskeleton. J Cell Biol, 188(1), 29-37. https://doi.org/10.1083/jcb.200909017 · DOI
  26. Hudson, A. M., & Cooley, L. (2014, Jun 15). Methods for studying oogenesis. Methods, 68(1), 207-217. https://doi.org/10.1016/j.ymeth.2014.01.005 · DOI
  27. Imschenetzky, M., Diaz, F., Montecino, M., Sierra, F., & Puchi, M. (1997, Dec 1). Identification of a cysteine protease responsible for degradation of sperm histones during male pronucleus remodeling in sea urchins. J Cell Biochem, 67(3), 304-315.
  28. Jia, D., Xu, Q., Xie, Q., Mio, W., & Deng, W. M. (2016, Jan 6). Automatic stage identification of Drosophila egg chamber based on DAPI images. Sci Rep, 6, 18850. https://doi.org/10.1038/srep18850 · DOI
  29. Johnson, M. R., Stephenson, R. A., Ghaemmaghami, S., & Welte, M. A. (2018, Jul 25). Developmentally regulated H2Av buffering via dynamic sequestration to lipid droplets in Drosophila embryos. Elife, 7. https://doi.org/10.7554/eLife.36021 · DOI
  30. Kan, R., Jin, M., Subramanian, V., Causey, C. P., Thompson, P. R., & Coonrod, S. A. (2012, Jun 19). Potential role for PADI-mediated histone citrullination in preimplantation development. BMC Dev Biol, 12, 19. https://doi.org/10.1186/1471-213X-12-19 · DOI
  31. Kaygun, H., & Marzluff, W. F. (2005, Sep). Regulated degradation of replication- dependent histone mRNAs requires both ATR and Upf1. Nat Struct Mol Biol, 12(9), 794-800. https://doi.org/10.1038/nsmb972 · DOI
  32. Keembiyehetty, C. N., Krzeslak, A., Love, D. C., & Hanover, J. A. (2011, Aug 15). A lipid-droplet-targeted O-GlcNAcase isoform is a key regulator of the proteasome. J Cell Sci, 124(Pt 16), 2851-2860. https://doi.org/10.1242/jcs.083287 · DOI
  33. Khor, B., Bredemeyer, A. L., Huang, C.-Y., Turnbull, I. R., Evans, R., Maggi, L. B., White, J. M., Walker, L. M., Carnes, K., & Hess, R. A. (2006). Proteasome activator PA200 is required for normal spermatogenesis. Molecular and cellular biology, 26(8), 2999-3007.
  34. King, R., & Koch, E. A. (1963). Studies on the ovarian follicle cells of Drosophila. Journal of Cell Science, 3(67), 297-320.
  35. King, R. C. (1970). Ovarian development in Drosophila melanogaster. Academic Press.
  36. Kolkhof, P., Werthebach, M., van de Venn, A., Poschmann, G., Chen, L., Welte, M., Stuhler, K., & Beller, M. (2017, Mar). A Luciferase-fragment Complementation Assay to Detect Lipid Droplet-associated Protein- Protein Interactions. Mol Cell Proteomics, 16(3), 329-345. https://doi.org/10.1074/mcp.M116.061499 · DOI
  37. Li, Z., Johnson, M. R., Ke, Z., Chen, L., & Welte, M. A. (2014, Jul 7). Drosophila lipid droplets buffer the H2Av supply to protect early embryonic development. Curr Biol, 24(13), 1485-1491. https://doi.org/10.1016/j.cub.2014.05.022 · DOI
  38. Li, Z., Thiel, K., Thul, P. J., Beller, M., Kuhnlein, R. P., & Welte, M. A. (2012, Nov 20). Lipid droplets control the maternal histone supply of Drosophila embryos. Curr Biol, 22(22), 2104-2113. https://doi.org/10.1016/j.cub.2012.09.018 · DOI
  39. Lin, R., Cook, R. G., & Allis, C. D. (1991, Sep). Proteolytic removal of core histone amino termini and dephosphorylation of histone H1 correlate with the formation of condensed chromatin and transcriptional silencing during Tetrahymena macronuclear development. Genes Dev, 5(9), 1601-1610. https://doi.org/10.1101/gad.5.9.1601 · DOI
  40. Maki, J. A., Schnobrich, D. J., & Culver, G. M. (2002, Jul). The DnaK chaperone system facilitates 30S ribosomal subunit assembly. Mol Cell, 10(1), 129- 138. https://doi.org/10.1016/s1097-2765(02)00562-2 · DOI
  41. Marzluff, W. F., Wagner, E. J., & Duronio, R. J. (2008, Nov). Metabolism and regulation of canonical histone mRNAs: life without a poly(A) tail. Nat Rev Genet, 9(11), 843-854. https://doi.org/10.1038/nrg2438 · DOI
  42. Masuda, Y., Itabe, H., Odaki, M., Hama, K., Fujimoto, Y., Mori, M., Sasabe, N., Aoki, J., Arai, H., & Takano, T. (2006). ADRP/adipophilin is degraded through the proteasome-dependent pathway during regression of lipid- storing cells. Journal of lipid research, 47(1), 87-98.
  43. McLauchlan, J., Lemberg, M. K., Hope, G., & Martoglio, B. (2002, Aug 1). Intramembrane proteolysis promotes trafficking of hepatitis C virus core protein to lipid droplets. EMBO J, 21(15), 3980-3988. https://doi.org/10.1093/emboj/cdf414 · DOI
  44. Meekswagner, D., & Hartwell, L. H. (1986, Jan). Normal Stoichiometry of Histone Dimer Sets Is Necessary for High Fidelity of Mitotic Chromosome Transmission. Cell, 44(1), 43-52. https://doi.org/Doi 10.1016/0092- 8674(86)90483-6 · DOI
  45. Mejhert, N., Kuruvilla, L., Gabriel, K. R., Elliott, S. D., Guie, M. A., Wang, H., Lai, Z. W., Lane, E. A., Christiano, R., Danial, N. N., Farese, R. V., Jr., & Walther, T. C. (2020, Jan 28). Partitioning of MLX-Family Transcription Factors to Lipid Droplets Regulates Metabolic Gene Expression. Mol Cell. https://doi.org/10.1016/j.molcel.2020.01.014 · DOI · Paper page
  46. Mir, M., Stadler, M. R., Ortiz, S. A., Hannon, C. E., Harrison, M. M., Darzacq, X., & Eisen, M. B. (2018, Dec 27). Dynamic multifactor hubs interact transiently with sites of active transcription in Drosophila embryos. Elife, 7. https://doi.org/10.7554/eLife.40497 · DOI · Paper page
  47. Morin, V., Sanchez-Rubio, A., Aze, A., Iribarren, C., Fayet, C., Desdevises, Y., Garcia-Huidobro, J., Imschenetzky, M., Puchi, M., & Geneviere, A. M. (2012). The protease degrading sperm histones post-fertilization in sea urchin eggs is a nuclear cathepsin L that is further required for embryo development. PLoS One, 7(11), e46850. https://doi.org/10.1371/journal.pone.0046850 · DOI
  48. Mulligan, P., & Rasch, E. (1985). Determination of DNA content in the nurse and follicle cells from wild type and mutant Drosophila melanogaster by DNA- Feulgen cytophotometry. Histochemistry, 82(3), 233-247.
  49. Nagai, A., Sato, T., Akimoto, N., Ito, A., & Sumida, M. (2005, Jun). Isolation and identification of histone H3 protein enriched in microvesicles secreted from cultured sebocytes. Endocrinology, 146(6), 2593-2601. https://doi.org/10.1210/en.2004-1478 · DOI
  50. Navarro-Costa, P., McCarthy, A., Prudencio, P., Greer, C., Guilgur, L. G., Becker, J. D., Secombe, J., Rangan, P., & Martinho, R. G. (2016, Aug 10). Early programming of the oocyte epigenome temporally controls late prophase I transcription and chromatin remodelling. Nat Commun, 7, 12331. https://doi.org/10.1038/ncomms12331 · DOI
  51. O'Farrell, P. H., Stumpff, J., & Su, T. T. (2004, Jan 6). Embryonic cleavage cycles: how is a mouse like a fly? Curr Biol, 14(1), R35-45. https://doi.org/10.1016/j.cub.2003.12.022 · DOI
  52. Ohsaki, Y., Cheng, J., Fujita, A., Tokumoto, T., & Fujimoto, T. (2006, Jun). Cytoplasmic lipid droplets are sites of convergence of proteasomal and autophagic degradation of apolipoprotein B. Mol Biol Cell, 17(6), 2674- 2683. https://doi.org/10.1091/mbc.e05-07-0659 · DOI
  53. Ohsaki, Y., Cheng, J., Suzuki, M., Fujita, A., & Fujimoto, T. (2008, Jul 15). Lipid droplets are arrested in the ER membrane by tight binding of lipidated apolipoprotein B-100. J Cell Sci, 121(Pt 14), 2415-2422. https://doi.org/10.1242/jcs.025452 · DOI
  54. Onikubo, T., Nicklay, J. J., Xing, L., Warren, C., Anson, B., Wang, W. L., Burgos, E. S., Ruff, S. E., Shabanowitz, J., Cheng, R. H., Hunt, D. F., & Shechter, D. (2015, Mar 17). Developmentally Regulated Post-translational Modification of Nucleoplasmin Controls Histone Sequestration and Deposition. Cell Rep, 10(10), 1735-1748. https://doi.org/10.1016/j.celrep.2015.02.038 · DOI
  55. Palanker, L., Tennessen, J. M., Lam, G., & Thummel, C. S. (2009, Mar). Drosophila HNF4 regulates lipid mobilization and beta-oxidation. Cell Metab, 9(3), 228-239. https://doi.org/10.1016/j.cmet.2009.01.009 · DOI
  56. Pennetta, G., & Welte, M. A. (2018, May 21). Emerging Links between Lipid Droplets and Motor Neuron Diseases. Dev Cell, 45(4), 427-432. https://doi.org/10.1016/j.devcel.2018.05.002 · DOI
  57. Romanauska, A., & Kohler, A. (2018, Jul 26). The Inner Nuclear Membrane Is a Metabolically Active Territory that Generates Nuclear Lipid Droplets. Cell, 174(3), 700-715 e718. https://doi.org/10.1016/j.cell.2018.05.047 · DOI
  58. Rowe, E. R., Mimmack, M. L., Barbosa, A. D., Haider, A., Isaac, I., Ouberai, M. M., Thiam, A. R., Patel, S., Saudek, V., & Siniossoglou, S. (2016). Conserved amphipathic helices mediate lipid droplet targeting of perilipins 1-3. Journal of Biological Chemistry, 291(13), 6664-6678.
  59. Ruddell, A., & Jacobs-Lorena, M. (1985, May). Biphasic pattern of histone gene expression during Drosophila oogenesis. Proc Natl Acad Sci U S A, 82(10), 3316-3319. https://doi.org/10.1073/pnas.82.10.3316 · DOI
  60. Schejter, E. D., & Wieschaus, E. (1993). Functional elements of the cytoskeleton in the early Drosophila embryo. Annu Rev Cell Biol, 9, 67-99. https://doi.org/10.1146/annurev.cb.09.110193.000435 · DOI
  61. Shindo, Y., & Amodeo, A. A. (2019, Jan 21). Dynamics of Free and Chromatin- Bound Histone H3 during Early Embryogenesis. Curr Biol, 29(2), 359-366 e354. https://doi.org/10.1016/j.cub.2018.12.020 · DOI
  62. Singh, R. K., Kabbaj, M. H., Paik, J., & Gunjan, A. (2009, Aug). Histone levels are regulated by phosphorylation and ubiquitylation-dependent proteolysis. Nat Cell Biol, 11(8), 925-933. https://doi.org/10.1038/ncb1903 · DOI
  63. Singh, R. K., Liang, D., Gajjalaiahvari, U. R., Kabbaj, M. H., Paik, J., & Gunjan, A. (2010, Oct 15). Excess histone levels mediate cytotoxicity via multiple mechanisms. Cell Cycle, 9(20), 4236-4244. https://doi.org/10.4161/cc.9.20.13636 · DOI
  64. Spracklen, A. J., & Tootle, T. L. (2013, Dec 2). The utility of stage-specific mid-to- late Drosophila follicle isolation. J Vis Exp(82), 50493. https://doi.org/10.3791/50493 · DOI
  65. Takahashi, Y., Shinoda, A., Kamada, H., Shimizu, M., Inoue, J., & Sato, R. (2016). Perilipin2 plays a positive role in adipocytes during lipolysis by escaping proteasomal degradation. Scientific reports, 6(1), 1-14.
  66. Thurmond, J., Goodman, J. L., Strelets, V. B., Attrill, H., Gramates, L. S., Marygold, S. J., Matthews, B. B., Millburn, G., Antonazzo, G., Trovisco, V., Kaufman, T. C., Calvi, B. R., & FlyBase, C. (2019, Jan 8). FlyBase 2.0: the next generation. Nucleic Acids Res, 47(D1), D759-D765. https://doi.org/10.1093/nar/gky1003 · DOI
  67. Tran, S. L., & Welte, M. A. (2010, Jun 23). In-vivo centrifugation of Drosophila embryos. J Vis Exp(40). https://doi.org/10.3791/2005 · DOI
  68. Velentzas, P. D., Velentzas, A. D., Mpakou, V. E., Papassideri, I. S., Stravopodis, D. J., & Margaritis, L. H. (2011, Jan). Proteasome inhibition induces developmentally deregulated programs of apoptotic and autophagic cell death during Drosophila melanogaster oogenesis. Cell Biol Int, 35(1), 15- 27. https://doi.org/10.1042/CBI20100191 · DOI
  69. Vevea, J. D., Garcia, E. J., Chan, R. B., Zhou, B., Schultz, M., Di Paolo, G., McCaffery, J. M., & Pon, L. A. (2015, Dec 7). Role for Lipid Droplet Biogenesis and Microlipophagy in Adaptation to Lipid Imbalance in Yeast. Dev Cell, 35(5), 584-599. https://doi.org/10.1016/j.devcel.2015.11.010 · DOI
  70. Von Stetina, J. R., & Orr-Weaver, T. L. (2011, Oct 1). Developmental control of oocyte maturation and egg activation in metazoan models. Cold Spring Harb Perspect Biol, 3(10), a005553. https://doi.org/10.1101/cshperspect.a005553 · DOI
  71. Walther, T. C., & Farese, R. V., Jr. (2012). Lipid droplets and cellular lipid metabolism. Annu Rev Biochem, 81, 687-714. https://doi.org/10.1146/annurev-biochem-061009-102430 · DOI
  72. Wan, H. C., Melo, R. C., Jin, Z., Dvorak, A. M., & Weller, P. F. (2007, Jan). Roles and origins of leukocyte lipid bodies: proteomic and ultrastructural studies. FASEB J, 21(1), 167-178. https://doi.org/10.1096/fj.06-6711com Wat, L. W., Chao, C., Bartlett, R., Buchanan, J. L., Millington, J. W., Chih, H. J., Chowdhury, Z. S., Biswas, P., Huang, V., Shin, L. J., Wang, L. C., Gauthier, M. L., Barone, M. C., Montooth, K. L., Welte, M. A., & Rideout, E. J. (2020, Jan). A role for triglyceride lipase brummer in the regulation of sex differences in Drosophila fat storage and breakdown. PLoS Biol, 18(1), e3000595. https://doi.org/10.1371/journal.pbio.3000595 · DOI
  73. Welte, M. A. (2007, Aug). Proteins under new management: lipid droplets deliver. Trends Cell Biol, 17(8), 363-369. https://doi.org/10.1016/j.tcb.2007.06.004 · DOI
  74. Welte, M. A. (2015, Sep). As the fat flies: The dynamic lipid droplets of Drosophila embryos. Biochim Biophys Acta, 1851(9), 1156-1185. https://doi.org/10.1016/j.bbalip.2015.04.002 · DOI
  75. Welte, M. A., Cermelli, S., Griner, J., Viera, A., Guo, Y., Kim, D. H., Gindhart, J. G., & Gross, S. P. (2005, Jul 26). Regulation of lipid-droplet transport by the perilipin homolog LSD2. Curr Biol, 15(14), 1266-1275. https://doi.org/10.1016/j.cub.2005.06.062 · DOI
  76. Welte, M. A., & Gould, A. P. (2017, Oct). Lipid droplet functions beyond energy storage. Biochim Biophys Acta Mol Cell Biol Lipids, 1862(10 Pt B), 1260- 1272. https://doi.org/10.1016/j.bbalip.2017.07.006 · DOI
  77. Werthebach, M., Stewart, F. A., Gahlen, A., Mettler-Altmann, T., Akhtar, I., Maas- Enriquez, K., Droste, A., Eichmann, T. O., Poschmann, G., Stuhler, K., & Beller, M. (2019, Mar 26). Control of Drosophila Growth and Survival by the Lipid Droplet-Associated Protein CG9186/Sturkopf. Cell Rep, 26(13), 3726-3740 e3727. https://doi.org/10.1016/j.celrep.2019.02.110 · DOI
  78. Xu, G., Sztalryd, C., & Londos, C. (2006). Degradation of perilipin is mediated through ubiquitination-proteasome pathway. Biochimica et Biophysica Acta (BBA)-Molecular and Cell Biology of Lipids, 1761(1), 83-90.
  79. Yu, J., & Li, P. (2017, Jan). The size matters: regulation of lipid storage by lipid droplet dynamics. Sci China Life Sci, 60(1), 46-56. https://doi.org/10.1007/s11427-016-0322-x · DOI
  80. Zechner, R., Zimmermann, R., Eichmann, T. O., Kohlwein, S. D., Haemmerle, G., Lass, A., & Madeo, F. (2012, Mar 7). FAT SIGNALS--lipases and lipolysis in lipid metabolism and signaling. Cell Metab, 15(3), 279-291. https://doi.org/10.1016/j.cmet.2011.12.018 · DOI
  81. Zhang, C., Yang, L., Ding, Y., Wang, Y., Lan, L., Ma, Q., Chi, X., Wei, P., Zhao, Y., Steinbuchel, A., Zhang, H., & Liu, P. (2017, Jul 6). Bacterial lipid droplets bind to DNA via an intermediary protein that enhances survival under stress. Nat Commun, 8, 15979. https://doi.org/10.1038/ncomms15979 · DOI

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Authors
Stephenson, R. A., Thomalla, J. M., Chen, L., Kolkhof, P., White, R. P., Beller, M., & Welte, M. A.
Affiliations
  • University of Rochester (US)
  • Heinrich Heine University Düsseldorf (DE)
ORCID
Venue
Development
Publisher
The Company of Biologists
Published
2021-08-01
Volume
148
Issue
15
ISSN
  • 0950-1991 (ISSN-L)
  • 1477-9129
DOI
10.1242/dev.199381
PMC
PMC8380457
OpenAlex
W3187060569
Cited by
38
References
1
Citations by year
2026: 8 · 2025: 9 · 2024: 5 · 2023: 11 · 2022: 2 · 2021: 3
FWCI
1.65
Type
journal article
Language
en
Open access
Licence
www.biologists.com/user-licence-1-1/ (vor)
Locations
  • Development (publishedVersion)
  • bioRxiv (Cold Spring Harbor Laboratory) (acceptedVersion)
  • PubMed Central (publishedVersion)
  • PubMed (publishedVersion)
Funders
  • National Institutes of Health (RO1 GM102155)
  • Deutsche Forschungsgemeinschaft (INST 208/760-1FUGG)
Topics
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Genomics and Chromatin Dynamics
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Biochemistry › Lipid metabolism and biosynthesis
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Nuclear Structure and Function
Keywords
lipid droplets, histone turnover, histone H2B, histone H2A, oogenesis, nurse cells, oocytes, Drosophila embryo, protein sequestration, histone degradation, intercellular transport
MeSH terms
Animals, Carrier Proteins, Drosophila, Female, Histones, Oocytes, Oogenesis, Drosophila Proteins, Lipid Droplets

About these checks

Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.

Statistics and arithmetic are recomputed, not judged.

Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.

What counts as a claim ›How we measure confidence ›How we check this ›

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