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Volume 49 Issue 7
Jul.  2022
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Article Navigation >  Journal of Genetics and Genomics  > 2022  >  49(7): 636-644

The sex determination gene doublesex regulates expression and secretion of the basement membrane protein Collagen IV

doi: 10.1016/j.jgg.2021.12.010
  •  

    a The Key Laboratory of Developmental Genes and Human Disease, School of Life Science and Technology, Southeast University, Nanjing, Jiangsu 210096, China;

  •  

    b Co-innovation Center of Neuroregeneration, Nantong University, Nantong, Jiangsu 226019, China

Funds:

We thank the Bloomington Drosophila Stock Center, Tsinghua Fly Center and Dr. José Carlos Pastor-Pareja in Tsinghua University for fly stocks. This work was supported by grants from National Key R&

D Program of China (2019YFA0802400), the National Natural Science Foundation of China (31970943 and 31700905), and the Jiangsu Innovation and Entrepreneurship Team Program.

  • Received Date: 2021-09-06
  • Accepted Date: 2021-12-24
  • Rev Recd Date: 2021-12-19
  • Publish Date: 2022-01-10
    Abstract
  • The highly conserved doublesex (dsx) and doublesex/mab-3 related (Dmrt) genes control sexually dimorphic traits across animals. The dsx gene encodes sex-specific transcription factors, DsxM in males and DsxF in females, which function differentially and often oppositely to establish sexual dimorphism. Here, we report that mutations in dsx, or overexpression of dsx, result in abnormal distribution of the basement membrane (BM) protein Collagen IV in the fat body. We find that Dsx isoforms regulate the expression of Collagen IV in the fat body and its secretion into the BM of other tissues. We identify the procollagen lysyl hydroxylase (dPlod) gene, which is involved in the biosynthesis of Collagen IV, as a direct target of Dsx. We further show that Dsx regulates Collagen IV through dPlod-dependent and independent pathways. These findings reveal how Dsx isoforms function in the secretory fat body to regulate Collagen IV and remotely establish sexual dimorphism.
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    • References(41)
  • Asahina, K., 2018. Sex differences in Drosophila behavior:qualitative and quantitative dimorphism. Curr. Opin. Physiol. 6, 35-45
    Asha, H., Nagy, I., Kovacs, G., Stetson, D., Ando, I.,Dearolf, C.R., 2003. Analysis of ras-induced overproliferation in Drosophila hemocytes. Genetics 163, 203-215
    Baker, B.S.,Belote, J.M., 1983. Sex determination and dosage compensation in Drosophila melanogaster. Annu. Rev. Genet. 17, 345-393
    Belote, J.M., Handler, A.M., Wolfner, M.F., Livak, K.J.,Baker, B.S., 1985. Sex-specific regulation of yolk protein gene expression in Drosophila. Cell 40, 339-348
    Bunt, S., Denholm, B.,Skaer, H., 2011. Characterisation of the Drosophila procollagen lysyl hydroxylase, dplod. Gene Expr. Patterns 11, 72-78
    Burtis, K.C.,Baker, B.S., 1989. Drosophila doublesex gene controls somatic sexual differentiation by producing alternatively spliced mrnas encoding related sex-specific polypeptides. Cell 56, 997-1010
    Christiansen, A.E., Keisman, E.L., Ahmad, S.M.,Baker, B.S., 2002. Sex comes in from the cold:the integration of sex and pattern. Trends Genet. 18, 510-516
    Clough, E., Jimenez, E., Kim, Y.A., Whitworth, C., Neville, M.C., Hempel, L.U., Pavlou, H.J., Chen, Z.X., Sturgill, D., Dale, R.K., et al., 2014. Sex- and tissue-specific functions of Drosophila doublesex transcription factor target genes. Dev. Cell 31, 761-773
    Colombani, J., Raisin, S., Pantalacci, S., Radimerski, T., Montagne, J.,Leopold, P., 2003. A nutrient sensor mechanism controls Drosophila growth. Cell 114, 739-749
    Dauwalder, B., Tsujimoto, S., Moss, J.,Mattox, W., 2002. The Drosophila takeout gene is regulated by the somatic sex-determination pathway and affects male courtship behavior. Genes Dev. 16, 2879-2892
    Demir, E.,Dickson, B.J., 2005. Fruitless splicing specifies male courtship behavior in Drosophila. Cell 121, 785-794
    Fessler, L.I., Nelson, R.E.,Fessler, J.H., 1994. Drosophila extracellular matrix. Methods Enzymol. 245, 271-294
    Fujii, S.,Amrein, H., 2002. Genes expressed in the Drosophila head reveal a role for fat cells in sex-specific physiology. EMBO J. 21, 5353-5363
    Guo, C., Pan, Y.,Gong, Z., 2019. Recent advances in the genetic dissection of neural circuits in Drosophila. Neurosci. Bull 35, 1058-1072
    Isabella, A.J.,Horne-Badovinac, S., 2015. Building from the ground up:basement membranes in Drosophila development. Curr. Top. Membr. 76, 305-336
    Ito, H., Fujitani, K., Usui, K., Shimizu-Nishikawa, K., Tanaka, S.,Yamamoto, D., 1996. Sexual orientation in Drosophila is altered by the satori mutation in the sex-determination gene fruitless that encodes a zinc finger protein with a btb domain. Proc. Natl. Acad. Sci. U. S. A. 93, 9687-9692
    Jayadev, R.,Sherwood, D.R., 2017. Basement membranes. Curr. Biol. 27, R207-R211
    Ke, H., Feng, Z., Liu, M., Sun, T., Dai, J., Ma, M., Liu, L.P., Ni, J.Q.,Pastor-Pareja, J.C., 2018. Collagen secretion screening in Drosophila supports a common secretory machinery and multiple rab requirements. J. Genet. Genomics 45, 299-313
    Kopp, A., 2012. Dmrt genes in the development and evolution of sexual dimorphism. Trends Genet. 28, 175-184
    Lazareva, A.A., Roman, G., Mattox, W., Hardin, P.E.,Dauwalder, B., 2007. A role for the adult fat body in Drosophila male courtship behavior. PLoS Genet. 3, e16
    Lee, G., Foss, M., Goodwin, S.F., Carlo, T., Taylor, B.J.,Hall, J.C., 2000. Spatial, temporal, and sexually dimorphic expression patterns of the fruitless gene in the Drosophila central nervous system. J. Neurobiol. 43, 404-426
    Lee, G., Hall, J.C.,Park, J.H., 2002. Doublesex gene expression in the central nervous system of Drosophila melanogaster. J. Neurogenet. 16, 229-248
    Li, H., Janssens, J., De Waegeneer, M., Kolluru, S.S., Davie, K., Gardeux, V., Saelens, W., David, F., Brbic, M., Leskovec, J., et al., 2021. Fly cell atlas:a single-cell transcriptomic atlas of the adult fruit fly. bioRxiv 2021.07.04.451050
    Luo, S.D., Shi, G.W.,Baker, B.S., 2011. Direct targets of the d. Melanogaster dsxf protein and the evolution of sexual development. Development 138, 2761-2771
    Manoli, D.S., Foss, M., Villella, A., Taylor, B.J., Hall, J.C.,Baker, B.S., 2005. Male-specific fruitless specifies the neural substrates of Drosophila courtship behaviour. Nature 436, 395-400
    Marin, I.,Baker, B.S., 1998. The evolutionary dynamics of sex determination. Science 281, 1990-1994
    Morin, X., Daneman, R., Zavortink, M.,Chia, W., 2001. A protein trap strategy to detect gfp-tagged proteins expressed from their endogenous loci in Drosophila. Proc. Natl. Acad. Sci. U. S. A. 98, 15050-15055
    Natzle, J.E., Monson, J.M.,McCarthy, B.J., 1982. Cytogenetic location and expression of collagen-like genes in Drosophila. Nature 296, 368-371
    Pan, Y.,Baker, B.S., 2014. Genetic identification and separation of innate and experience-dependent courtship behaviors in Drosophila. Cell 156, 236-248
    Pan, Y., Robinett, C.C.,Baker, B.S., 2011. Turning males on:activation of male courtship behavior in Drosophila melanogaster. PLoS One 6, e21144
    Pastor-Pareja, J.C.,Xu, T., 2011. Shaping cells and organs in Drosophila by opposing roles of fat body-secreted collagen iv and perlecan. Dev. Cell 21, 245-256
    Peng, Q., Chen, J., Su, X., Wang, R., Han, C.,Pan, Y., 2021. The sex determination gene doublesex is required during adulthood to maintain sexual orientation. J Genet. Genomics https://doi.org/10.1016/j.jgg.2021.08.006
    Pfeiffer, B.D., Ngo, T.T., Hibbard, K.L., Murphy, C., Jenett, A., Truman, J.W.,Rubin, G.M., 2010. Refinement of tools for targeted gene expression in Drosophila. Genetics 186, 735-755
    Rideout, E.J., Dornan, A.J., Neville, M.C., Eadie, S.,Goodwin, S.F., 2010. Control of sexual differentiation and behavior by the doublesex gene in Drosophila melanogaster. Nat. Neurosci. 13, 458-466
    Robinett, C.C., Vaughan, A.G., Knapp, J.M.,Baker, B.S., 2010. Sex and the single cell. Ii. There is a time and place for sex. PLoS Biol. 8, e1000365
    Ryner, L.C., Goodwin, S.F., Castrillon, D.H., Anand, A., Villella, A., Baker, B.S., Hall, J.C., Taylor, B.J.,Wasserman, S.A., 1996. Control of male sexual behavior and sexual orientation in Drosophila by the fruitless gene. Cell 87, 1079-1089
    Sanders, L.E.,Arbeitman, M.N., 2008. Doublesex establishes sexual dimorphism in the Drosophila central nervous system in an isoform-dependent manner by directing cell number. Dev. Biol. 320, 378-390
    Sarov-Blat, L., So, W.V., Liu, L.,Rosbash, M., 2000. The Drosophila takeout gene is a novel molecular link between circadian rhythms and feeding behavior. Cell 101, 647-656
    Stockinger, P., Kvitsiani, D., Rotkopf, S., Tirian, L.,Dickson, B.J., 2005. Neural circuitry that governs Drosophila male courtship behavior. Cell 121, 795-807
    Yamamoto, D.,Koganezawa, M., 2013. Genes and circuits of courtship behaviour in Drosophila males. Nat. Rev. Neurosci. 14, 681-692
    Yurchenco, P.D., 2011. Basement membranes:cell scaffoldings and signaling platforms. Cold Spring Harbor Perspect. Biol. 3, a004911
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    1. Berg C., Sieber M., Sun J. Finishing the egg. Genetics, 2024, 226 doi:10.1093/genetics/iyad183
    2. Han C., Peng Q., Su X. et al. A male-specific doublesex isoform reveals an evolutionary pathway of sexual development via distinct alternative splicing mechanisms. Communications Biology, 2022, 5 doi:10.1038/s42003-022-03664-7
    3. Han C., Peng Q., Sun M. et al. The doublesex gene regulates dimorphic sexual and aggressive behaviors in Drosophila. Proceedings of the National Academy of Sciences of the United States of America, 2022, 119 doi:10.1073/pnas.2201513119

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