Skip to main content

Genetic Control of Salivary Gland Tubulogenesis in Drosophila

  • Chapter
  • First Online:
Book cover Organogenetic Gene Networks

Abstract

Organ formation during embryogenesis requires the delicate orchestration of many different events. The specification of an organ primordium is tightly coordinated with the onset and control of morphogenetic events shaping that organ. In many cases, though, only the gene regulatory events that specify organ positioning and identity have been elucidated in much detail, whereas knowledge is scarce about the upstream regulation that controls effectors that directly drive morphogenesis. In this review, we will use the formation of the tubes of the salivary gland in the Drosophila embryo as a model system to illustrate what has been uncovered with regards to different phases of salivary gland morphogenesis: specification and positioning of the primordium, gland invagination, tube extension, organ positioning, as well as gland function. The salivary glands are an excellent model for the analysis of tube formation, as they are amenable to advanced imaging, genetic analysis and perturbance. In addition, upon specification by-and-large no cell death or division occurs, and thus the whole morphogenesis is driven entirely by cell shape changes and cell rearrangements.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 129.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 169.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 169.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

References

  • Abrams, E. W., & Andrew, D. J. (2005). CrebA regulates secretory activity in the Drosophila salivary gland and epidermis. Development, 132, 2743–2758.

    Article  CAS  PubMed  Google Scholar 

  • Abrams, E. W., Mihoulides, W. K., & Andrew, D. J. (2006). Fork head and Sage maintain a uniform and patent salivary gland lumen through regulation of two downstream target genes, PH4alphaSG1 and PH4alphaSG2. Development, 133, 3517–3527.

    Article  CAS  PubMed  Google Scholar 

  • Andrew, D. J., Baig, A., Bhanot, P., Smolik, S. M., & Henderson, K. D. (1997). The Drosophila dCREB-A gene is required for dorsal/ventral patterning of the larval cuticle. Development, 124, 181–193.

    CAS  PubMed  Google Scholar 

  • Andrew, D. J., Horner, M. A., Petitt, M. G., Smolik, S. M., & Scott, M. P. (1994). Setting limits on homeotic gene function: Restraint of Sex combs reduced activity by teashirt and other homeotic genes. The EMBO Journal, 13, 1132–1144.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Booth, A. J. R., Blanchard, G. B., Adams, R. J., & Röper, K. (2014). A dynamic microtubule cytoskeleton directs medial actomyosin function during tube formation. Developmental Cell, 29, 562–576.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bradley, P. L., Myat, M. M., Comeaux, C. A., & Andrew, D. J. (2003). Posterior migration of the salivary gland requires an intact visceral mesoderm and integrin function. Developmental Biology, 257, 249–262.

    Article  CAS  PubMed  Google Scholar 

  • Brönner, G., Chu-LaGraff, Q., Doe, C. Q., Cohen, B., Weigel, D., Taubert, H., et al. (1994). Sp1/egr-like zinc-finger protein required for endoderm specification and germ-layer formation in Drosophila. Nature, 369, 664–668.

    Article  PubMed  Google Scholar 

  • Cao, C., Liu, Y., & Lehmann, M. (2007). Fork head controls the timing and tissue selectivity of steroid-induced developmental cell death. The Journal of Cell Biology, 176, 843–852.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chandrasekaran, V., & Beckendorf, S. K. (2003). senseless is necessary for the survival of embryonic salivary glands in Drosophila. Development, 130, 4719–4728.

    Article  CAS  PubMed  Google Scholar 

  • Chandrasekaran, V., & Beckendorf, S. K. (2005). Tec29 controls actin remodeling and endoreplication during invagination of the Drosophila embryonic salivary glands. Development, 132, 3515–3524.

    Article  CAS  PubMed  Google Scholar 

  • Chung, S., & Andrew, D. J. (2014). Cadherin 99C regulates apical expansion and cell rearrangement during epithelial tube elongation. Development, 141, 1950–1960.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Curtiss, J., & Heilig, J. S. (1995). Establishment of Drosophila imaginal precursor cells is controlled by the Arrowhead gene. Development, 121, 3819–3828.

    CAS  PubMed  Google Scholar 

  • Escudero, L. M., Bischoff, M., & Freeman, M. (2007). Myosin II regulates complex cellular arrangement and epithelial architecture in Drosophila. Developmental Cell, 13, 717–729.

    Article  CAS  PubMed  Google Scholar 

  • Fasano, L., Röder, L., Coré, N., Alexandre, E., Vola, C., Jacq, B., et al. (1991). The gene teashirt is required for the development of Drosophila embryonic trunk segments and encodes a protein with widely spaced zinc finger motifs. Cell, 64, 63–79.

    Article  CAS  PubMed  Google Scholar 

  • Fox, R. M., Hanlon, C. D., & Andrew, D. J. (2010). The CrebA/Creb3-like transcription factors are major and direct regulators of secretory capacity. The Journal of Cell Biology, 191, 479–492.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Fox, R. M., Vaishnavi, A., Maruyama, R., & Andrew, D. J. (2013). Organ-specific gene expression: The bHLH protein Sage provides tissue specificity to Drosophila FoxA. Development, 140, 2160–2171.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Haberman, A. S., Isaac, D. D., & Andrew, D. J. (2003). Specification of cell fates within the salivary gland primordium. Developmental Biology, 258, 443–453.

    Article  CAS  PubMed  Google Scholar 

  • Harris, K. E., & Beckendorf, S. K. (2007). Different Wnt signals act through the Frizzled and RYK receptors during Drosophila salivary gland migration. Development, 134, 2017–2025.

    Article  CAS  PubMed  Google Scholar 

  • Harris, K. E., Schnittke, N., & Beckendorf, S. K. (2007). Two ligands signal through the Drosophila PDGF/VEGF receptor to ensure proper salivary gland positioning. Mechanisms of Development, 124, 441–448.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Henderson, K. D., & Andrew, D. J. (2000). Regulation and function of Scr, exd, and hth in the Drosophila salivary gland. Developmental Biology, 217, 362–374.

    Article  CAS  PubMed  Google Scholar 

  • Henderson, K. D., Isaac, D. D., & Andrew, D. J. (1999). Cell fate specification in the Drosophila salivary gland: The integration of homeotic gene function with the DPP signaling cascade. Developmental Biology, 205, 10–21.

    Article  CAS  PubMed  Google Scholar 

  • Hu, N., & Castelli-Gair, J. (1999). Study of the posterior spiracles of Drosophila as a model to understand the genetic and cellular mechanisms controlling morphogenesis. Developmental Biology, 214, 197–210.

    Article  CAS  PubMed  Google Scholar 

  • Irish, V. F., & Gelbart, W. M. (1987). The decapentaplegic gene is required for dorsal-ventral patterning of the Drosophila embryo. Genes & Development, 1, 868–879.

    Article  CAS  Google Scholar 

  • Isaac, D. D., & Andrew, D. J. (1996). Tubulogenesis in Drosophila: A requirement for the trachealess gene product. Genes & Development, 10, 103–117.

    Article  CAS  Google Scholar 

  • Ismat, A., Cheshire, A. M., & Andrew, D. J. (2013). The secreted AdamTS-A metalloprotease is required for collective cell migration. Development, 140, 1981–1993.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jones, N. A., Kuo, Y. M., Sun, Y. H., & Beckendorf, S. K. (1998). The Drosophila Pax gene eye gone is required for embryonic salivary duct development. Development, 125, 4163–4174.

    CAS  PubMed  Google Scholar 

  • Kam, Z., Minden, J. S., Agard, D. A., Sedat, J. W., & Leptin, M. (1991). Drosophila gastrulation: Analysis of cell shape changes in living embryos by three-dimensional fluorescence microscopy. Development, 112, 365–370.

    CAS  PubMed  Google Scholar 

  • Kerman, B. E., Cheshire, A. M., Myat, M. M., & Andrew, D. J. (2008). Ribbon modulates apical membrane during tube elongation through Crumbs and Moesin. Developmental Biology, 320, 278–288.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kidd, S., Baylies, M. K., Gasic, G. P., & Young, M. W. (1989). Structure and distribution of the Notch protein in developing Drosophila. Genes & Development, 3, 1113–1129.

    Article  CAS  Google Scholar 

  • Klämbt, C., Jacobs, J. R., & Goodman, C. S. (1991). The midline of the Drosophila central nervous system: A model for the genetic analysis of cell fate, cell migration, and growth cone guidance. Cell, 64, 801–815.

    Article  PubMed  Google Scholar 

  • Kolesnikov, T., & Beckendorf, S. K. (2007). 18 wheeler regulates apical constriction of salivary gland cells via the Rho-GTPase-signaling pathway. Developmental Biology, 307, 53–61.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kuo, Y. M., Jones, N., Zhou, B., Panzer, S., Larson, V., & Beckendorf, S. K. (1996). Salivary duct determination in Drosophila: Roles of the EGF receptor signalling pathway and the transcription factors fork head and trachealess. Development, 122, 1909–1917.

    CAS  PubMed  Google Scholar 

  • Lehmann, M., & Korge, G. (1996). The fork head product directly specifies the tissue-specific hormone responsiveness of the Drosophila Sgs-4 gene. The EMBO Journal, 15, 4825–4834.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Lekven, A. C., Tepass, U., Keshmeshian, M., & Hartenstein, V. (1998). faint sausage encodes a novel extracellular protein of the immunoglobulin superfamily required for cell migration and the establishment of normal axonal pathways in the Drosophila nervous system. Development, 125, 2747–2758.

    CAS  PubMed  Google Scholar 

  • LeMotte, P. K., Kuroiwa, A., Fessler, L. I., & Gehring, W. J. (1989). The homeotic gene Sex Combs Reduced of Drosophila: Gene structure and embryonic expression. The EMBO Journal, 8, 219–227.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Letizia, A., Ricardo, S., Moussian, B., Martin, N., & Llimargas, M. (2013). A functional role of the extracellular domain of Crumbs in cell architecture and apicobasal polarity. Journal of Cell Science, 126, 2157–2163.

    Article  CAS  PubMed  Google Scholar 

  • Letizia, A., Sotillos, S., Campuzano, S., & Llimargas, M. (2011). Regulated Crb accumulation controls apical constriction and invagination in Drosophila tracheal cells. Journal of Cell Science, 124, 240–251.

    Article  CAS  PubMed  Google Scholar 

  • Liu, X., Kiss, I., & Lengyel, J. A. (1999). Identification of genes controlling malpighian tubule and other epithelial morphogenesis in Drosophila melanogaster. Genetics, 151, 685–695.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Liu, Y., & Lehmann, M. (2008). Genes and biological processes controlled by the Drosophila FOXA orthologue Fork head. Insect Molecular Biology, 17, 91–101.

    Article  CAS  PubMed  Google Scholar 

  • Lovegrove, B., Simões, S., Rivas, M. L., Sotillos, S., Johnson, K., Knust, E., et al. (2006). Coordinated control of cell adhesion, polarity, and cytoskeleton underlies Hox-induced organogenesis in Drosophila. Current Biology, 16, 2206–2216.

    Article  CAS  PubMed  Google Scholar 

  • Mach, V., Ohno, K., Kokubo, H., & Suzuki, Y. (1996). The Drosophila fork head factor directly controls larval salivary gland-specific expression of the glue protein gene Sgs3. Nucleic Acids Research, 24, 2387–2394.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Manning, A. J., & Rogers, S. L. (2014). The Fog signaling pathway: Insights into signaling in morphogenesis. Developmental Biology, 394, 6–14.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Martin, A. C. (2010). Pulsation and stabilization: Contractile forces that underlie morphogenesis. Development Biology, 341, 114–125.

    Article  CAS  Google Scholar 

  • Martin, A. C., & Goldstein, B. (2014). Apical constriction: Themes and variations on a cellular mechanism driving morphogenesis. Development, 141, 1987–1998.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Martin, A. C., Kaschube, M., & Wieschaus, E. F. (2009). Pulsed contractions of an actin-myosin network drive apical constriction. Nature, 457, 495–499.

    Article  CAS  PubMed  Google Scholar 

  • Martinez-Arias, A., Ingham, P. W., Scott, M. P., & Akam, M. E. (1987). The spatial and temporal deployment of Dfd and Scr transcripts throughout development of Drosophila. Development, 100, 673–683.

    CAS  PubMed  Google Scholar 

  • Maruyama, R., & Andrew, D. J. (2012). Drosophila as a model for epithelial tube formation. Developmental Dynamics, 241, 119–135.

    Article  CAS  PubMed  Google Scholar 

  • Maruyama, R., Grevengoed, E., Stempniewicz, P., & Andrew, D. J. (2011). Genome-wide analysis reveals a major role in cell fate maintenance and an unexpected role in endoreduplication for the Drosophila FoxA gene Fork head. PLoS ONE, 6, e20901.

    Article  CAS  PubMed Central  Google Scholar 

  • Mason, F. M., Tworoger, M., & Martin, A. C. (2013). Apical domain polarization localizes actin–myosin activity to drive ratchet-like apical constriction. Nature Cell Biology, 15, 1–15 (Nature Publishing Group).

    Google Scholar 

  • Moore, A. W., Barbel, S., Jan, L. Y., & Jan, Y. N. (2000). A genomewide survey of basic helix-loop-helix factors in Drosophila. Proceedings of the National Academy of Sciences, 97, 10436–10441.

    Article  CAS  Google Scholar 

  • Myat, M. M., & Andrew, D. J. (2000a). Fork head prevents apoptosis and promotes cell shape change during formation of the Drosophila salivary glands. Development, 127, 4217–4226.

    CAS  PubMed  Google Scholar 

  • Myat, M. M., & Andrew, D. J. (2000b). Organ shape in the Drosophila salivary gland is controlled by regulated, sequential internalization of the primordia. Development, 127, 679–691.

    CAS  PubMed  Google Scholar 

  • Myat, M. M., & Andrew, D. J. (2002). Epithelial tube morphology is determined by the polarized growth and delivery of apical membrane. Cell, 111, 879–891.

    Article  CAS  PubMed  Google Scholar 

  • Myat, M. M., Isaac, D. D., & Andrew, D. J. (2000). Early genes required for salivary gland fate determination and morphogenesis in Drosophila melanogaster. Advances in Dental Research, 14, 89–98.

    Article  CAS  PubMed  Google Scholar 

  • Nikolaidou, K. K., & Barrett, K. (2004). A rho GTPase signaling pathway is used reiteratively in epithelial folding and potentially selects the outcome of rho activation. Current Biology, 14, 1822–1826.

    Article  CAS  PubMed  Google Scholar 

  • Nishimura, M., Inoue, Y., & Hayashi, S. (2007). A wave of EGFR signaling determines cell alignment and intercalation in the Drosophila tracheal placode. Development, 134, 4273–4282.

    Article  CAS  PubMed  Google Scholar 

  • Padgett, R. W., St Johnston, R. D., & Gelbart, W. M. (1987). A transcript from a Drosophila pattern gene predicts a protein homologous to the transforming growth factor-beta family. Nature, 325, 81–84.

    Article  CAS  PubMed  Google Scholar 

  • Panzer, S., Weigel, D., & Beckendorf, S. K. (1992). Organogenesis in Drosophila melanogaster: Embryonic salivary gland determination is controlled by homeotic and dorsoventral patterning genes. Development, 114, 49–57.

    CAS  PubMed  Google Scholar 

  • Pederson, J. D., Kiehart, D. P., & Mahaffey, J. W. (1996). The role of HOM-C genes in segmental transformations: Reexamination of the Drosophila Sex combs reduced embryonic phenotype. Development Biology, 180, 131–142.

    Article  CAS  Google Scholar 

  • Pirraglia, C., Walters, J., Ahn, N., & Myat, M. M. (2013). Rac1 GTPase acts downstream of αPS1βPS integrin to control collective migration and lumen size in the Drosophila salivary gland. Developmental Biology, 377, 21–32.

    Article  CAS  PubMed  Google Scholar 

  • Pirraglia, C., Walters, J., & Myat, M. M. (2010). Pak1 control of E-cadherin endocytosis regulates salivary gland lumen size and shape. Development, 137, 4177–4189.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ray, R. P., Arora, K., Nüsslein-Volhard, C., & Gelbart, W. M. (1991). The control of cell fate along the dorsal-ventral axis of the Drosophila embryo. Development, 113, 35–54.

    CAS  PubMed  Google Scholar 

  • Renault, N., King-Jones, K., & Lehmann, M. (2001). Downregulation of the tissue-specific transcription factor Fork head by Broad-Complex mediates a stage-specific hormone response. Development, 128, 3729–3737.

    CAS  PubMed  Google Scholar 

  • Riley, P. D., Carroll, S. B., & Scott, M. P. (1987). The expression and regulation of Sex combs reduced protein in Drosophila embryos. Genes & Development, 1, 716–730.

    Article  CAS  Google Scholar 

  • Röper, K. (2012). Anisotropy of Crumbs and aPKC drives myosin cable assembly during tube formation. Developmental Cell, 23, 939–953.

    Article  PubMed  PubMed Central  Google Scholar 

  • Roth, G. E., Wattler, S., Bornschein, H., Lehmann, M., & Korge, G. (1999). Structure and regulation of the salivary gland secretion protein gene Sgs-1 of Drosophila melanogaster. Genetics, 153, 753–762.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Sawyer, J. M., Harrell, J. R., Shemer, G., Sullivan-Brown, J., Roh-Johnson, M., & Goldstein, B. (2010). Apical constriction: A cell shape change that can drive morphogenesis. Developmental Biology, 341. 5–19 (Elsevier Inc).

    Google Scholar 

  • Simoes, S., Denholm, B., Azevedo, D., Sotillos, S., Martin, P., Skaer, H., et al. (2006). Compartmentalisation of Rho regulators directs cell invagination during tissue morphogenesis. Development, 133, 4257–4267.

    Article  CAS  PubMed  Google Scholar 

  • Smith, A. V., & Orr-Weaver, T. L. (1991). The regulation of the cell cycle during Drosophila embryogenesis: The transition to polyteny. Development, 112, 997–1008.

    CAS  PubMed  Google Scholar 

  • Taghli-Lamallem, O., Gallet, A., Leroy, F., Malapert, P., Vola, C., Kerridge, S., et al. (2007). Direct interaction between Teashirt and Sex combs reduced proteins, via Tsh’s acidic domain, is essential for specifying the identity of the prothorax in Drosophila. Developmental Biology, 307, 142–151.

    Article  CAS  PubMed  Google Scholar 

  • Tepass, U., Theres, C., & Knust, E. (1990). crumbs encodes an EGF-like protein expressed on apical membranes of Drosophila epithelial cells and required for organization of epithelia. Cell, 61, 787–799.

    Article  CAS  PubMed  Google Scholar 

  • Urban, S., Lee, J. R., & Freeman, M. (2001). Drosophila rhomboid-1 defines a family of putative intramembrane serine proteases. Cell, 107, 173–182.

    Article  CAS  PubMed  Google Scholar 

  • Vining, M. S., Bradley, P. L., Comeaux, C. A., & Andrew, D. J. (2005). Organ positioning in Drosophila requires complex tissue-tissue interactions. Developmental Biology, 287, 19–34.

    Article  CAS  PubMed  Google Scholar 

  • Weigel, D., Jürgens, G., Küttner, F., Seifert, E., & Jäckle, H. (1989). The homeotic gene fork head encodes a nuclear protein and is expressed in the terminal regions of the Drosophila embryo. Cell, 57, 645–658.

    Article  CAS  PubMed  Google Scholar 

  • Widmann, T. J., & Dahmann, C. (2009). Dpp signaling promotes the cuboidal-to-columnar shape transition of Drosophila wing disc epithelia by regulating Rho1. Journal of Cell Science, 122, 1362–1373.

    Article  CAS  PubMed  Google Scholar 

  • Xu, N., Bagumian, G., Galiano, M., & Myat, M. M. (2011). Rho GTPase controls Drosophila salivary gland lumen size through regulation of the actin cytoskeleton and Moesin. Development, 138, 5415–5427.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Xu, N., Keung, B., & Myat, M. M. (2008). Rho GTPase controls invagination and cohesive migration of the Drosophila salivary gland through Crumbs and Rho-kinase. Developmental Biology, 321, 88–100.

    Article  CAS  PubMed  Google Scholar 

  • Zhou, B., Bagri, A., & Beckendorf, S. K. (2001). Salivary gland determination in Drosophila: A salivary-specific, fork head enhancer integrates spatial pattern and allows fork head autoregulation. Developmental Biology, 237, 54–67.

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

The authors would like to apologize to colleagues whose work could not be cited or discussed in sufficient depth owing to space limitations, and would like to thank Gemma Girdler and the reviewer for critical reading of the manuscript and valuable suggestions.

Work in the lab is supported by the Medical Research Council (MRC file reference number MC_UP_1201/11).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Katja Röper .

Editor information

Editors and Affiliations

Rights and permissions

Reprints and permissions

Copyright information

© 2016 Springer International Publishing Switzerland

About this chapter

Cite this chapter

Sidor, C., Röper, K. (2016). Genetic Control of Salivary Gland Tubulogenesis in Drosophila . In: Castelli-Gair Hombría, J., Bovolenta, P. (eds) Organogenetic Gene Networks. Springer, Cham. https://doi.org/10.1007/978-3-319-42767-6_5

Download citation

Publish with us

Policies and ethics