Cytoophidia safeguard binucleation of Drosophila male accessory gland cells

Although most cells are mononuclear, the nucleus can exist in the form of binucleate or even multinucleate to respond to different physiological processes. The male accessory gland of Drosophila is the organ that produces semen, and its main cells are binucleate. Here we observe that CTP synthase (CTPS) forms filamentous cytoophidia in binuclear main cells, primarily located at the cell boundary. In CTPSH355A, a point mutation that destroys the formation of cytoophidia, we find that the nucleation mode of the main cells changes, including mononucleates and vertical distribution of binucleates. Although the overexpression of CTPSH355A can restore the level of CTPS protein, it will neither form cytoophidia nor eliminate the abnormal nucleation pattern. Therefore, our data indicate that there is an unexpected functional link between the formation of cytoophidia and the maintenance of binucleation in Drosophila main cells.

[1]  Suwen Zhao,et al.  Cytoophidia coupling adipose architecture and metabolism , 2022, Cellular and Molecular Life Sciences.

[2]  T. Stearns,et al.  Postmitotic centriole disengagement and maturation leads to centrosome amplification in polyploid trophoblast giant cells , 2022, bioRxiv.

[3]  Ji-Long Liu,et al.  Drosophila intestinal homeostasis requires CTP synthase. , 2021, Experimental cell research.

[4]  J. Kumari,et al.  Developmental expression patterns of toolkit genes in male accessory gland of Drosophila parallels those of mammalian prostate , 2021, Biology open.

[5]  Peiyao A. Zhao,et al.  Polarised maintenance of cytoophidia in Drosophila follicle epithelia. , 2021, Experimental cell research.

[6]  Ji-Long Liu,et al.  The atlas of cytoophidia in Drosophila larvae. , 2020, Journal of genetics and genomics = Yi chuan xue bao.

[7]  H. Xiang,et al.  CTP synthase forms cytoophidia in archaea. , 2020, Journal of genetics and genomics = Yi chuan xue bao.

[8]  Ji-Long Liu,et al.  Drosophila CTP synthase can form distinct substrate- and product-bound filaments. , 2019, Journal of genetics and genomics = Yi chuan xue bao.

[9]  R. Fischer,et al.  BMP signaling inhibition in Drosophila secondary cells remodels the seminal proteome and self and rival ejaculate functions , 2019, Proceedings of the National Academy of Sciences.

[10]  Ji-Long Liu,et al.  Forming cytoophidia prolongs the half-life of CTP synthase , 2019, Cell Discovery.

[11]  H. Nakagoshi,et al.  Binucleation of Accessory Gland Lobe Contributes to Effective Ejection of Seminal Fluid in Drosophila melanogaster , 2018, Zoological Science.

[12]  Y. Jeng,et al.  CTP synthase forms the cytoophidium in human hepatocellular carcinoma , 2017, Experimental cell research.

[13]  Ji-Long Liu The Cytoophidium and Its Kind: Filamentation and Compartmentation of Metabolic Enzymes. , 2016, Annual review of cell and developmental biology.

[14]  S. Lorenzetti,et al.  The role of the prostate in male fertility, health and disease , 2016, Nature Reviews Urology.

[15]  Ji-Long Liu,et al.  Asymmetric inheritance of cytoophidia in Schizosaccharomyces pombe , 2014, Biology Open.

[16]  Gabriel N. Aughey,et al.  Nucleotide synthesis is regulated by cytoophidium formation during neurodevelopment and adaptive metabolism , 2014, Biology Open.

[17]  H. Nakagoshi,et al.  The Homeodomain Protein Defective Proventriculus Is Essential for Male Accessory Gland Development to Enhance Fecundity in Drosophila , 2012, PloS one.

[18]  Brian K. Sato,et al.  Identification of novel filament-forming proteins in Saccharomyces cerevisiae and Drosophila melanogaster , 2010, The Journal of cell biology.

[19]  S. Celton-Morizur,et al.  The insulin/Akt pathway controls a specific cell division program that leads to generation of binucleated tetraploid liver cells in rodents. , 2009, The Journal of clinical investigation.

[20]  G. Pivert,et al.  Changes to hepatocyte ploidy and binuclearity profiles during human chronic viral hepatitis , 2005, Gut.

[21]  P. Seglen DNA ploidy and autophagic protein degradation as determinants of hepatocellular growth and survival , 1997, Cell Biology and Toxicology.

[22]  D. Pellman,et al.  From polyploidy to aneuploidy, genome instability and cancer , 2004, Nature Reviews Molecular Cell Biology.

[23]  C. Gillott Male accessory gland secretions: modulators of female reproductive physiology and behavior. , 2003, Annual review of entomology.

[24]  L. Partridge,et al.  The sex peptide of Drosophila melanogaster: Female post-mating responses analyzed by using RNA interference , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[25]  H. Malhi,et al.  Polyploidy associated with oxidative injury attenuates proliferative potential of cells. , 2001, Journal of cell science.

[26]  C. Obejero-Paz,et al.  Cks1 Mediates Vascular Smooth Muscle Cell Polyploidization* , 2000, The Journal of Biological Chemistry.

[27]  A. Dominiczak,et al.  Vascular smooth muscle cell polyploidy and cardiomyocyte hypertrophy due to chronic NOS inhibition in vivo. , 1998, American journal of physiology. Heart and circulatory physiology.

[28]  M. Wolfner,et al.  Cell type-specific gene expression in the Drosophila melanogaster male accessory gland , 1992, Mechanisms of Development.

[29]  T. Aigaki,et al.  Ectopic expression of sex peptide alters reproductive behavior of female D. melanogaster , 1991, Neuron.

[30]  M. Bienz,et al.  A male accessory gland peptide that regulates reproductive behavior of female D. melanogaster , 1988, Cell.

[31]  I. V. Uryvaeva,et al.  Cell polyploidy: its relation to tissue growth and function. , 1977, International review of cytology.

[32]  J. James,et al.  Polyploidy in the human myometrium. , 1975, Zeitschrift fur mikroskopisch-anatomische Forschung.

[33]  I. Lieberman Enzymatic amination of uridine triphosphate to cytidine triphosphate. , 1955, The Journal of biological chemistry.