Deciphering the Genetic Programme Triggering Timely and Spatially-Regulated Chitin Deposition
In this work we studied the maturation of the extracellular matrix during Drosophila embryogenesis. Drosophila deposit a chitin-rich extracellular matrix with key physiological functions, such as the control of organ size and shape, and cuticle formation. Chitin synthesis depends on chitin synthases, and in Drosophila the gene krotzkopf verkehrt (kkv) encodes the main enzyme of this family. Our observations indicate that Kkv alone is not sufficient to induce chitin formation. We have identified another function (which is exerted by the activity of two genes encoding MH2-domain proteins) that are equally required for chitin deposition. The most striking result of our analysis is that the presence of Kkv and the newly identified function is sufficient to trigger chitin deposition in ectodermally-derived tissues, even if they are normally devoid of this polysaccharide. Importantly, we also demonstrate that unregulated chitin deposition (absent, advanced, or ectopic) leads to severe defects in morphogenesis. We show that the temporal and spatial pattern of kkv and the other two genes perfectly recapitulates the deposition of chitin, thereby unveiling a highly co-ordinated mechanism for the acquisition of mature traits.
Vyšlo v časopise:
Deciphering the Genetic Programme Triggering Timely and Spatially-Regulated Chitin Deposition. PLoS Genet 11(1): e32767. doi:10.1371/journal.pgen.1004939
Kategorie:
Research Article
prolekare.web.journal.doi_sk:
https://doi.org/10.1371/journal.pgen.1004939
Souhrn
In this work we studied the maturation of the extracellular matrix during Drosophila embryogenesis. Drosophila deposit a chitin-rich extracellular matrix with key physiological functions, such as the control of organ size and shape, and cuticle formation. Chitin synthesis depends on chitin synthases, and in Drosophila the gene krotzkopf verkehrt (kkv) encodes the main enzyme of this family. Our observations indicate that Kkv alone is not sufficient to induce chitin formation. We have identified another function (which is exerted by the activity of two genes encoding MH2-domain proteins) that are equally required for chitin deposition. The most striking result of our analysis is that the presence of Kkv and the newly identified function is sufficient to trigger chitin deposition in ectodermally-derived tissues, even if they are normally devoid of this polysaccharide. Importantly, we also demonstrate that unregulated chitin deposition (absent, advanced, or ectopic) leads to severe defects in morphogenesis. We show that the temporal and spatial pattern of kkv and the other two genes perfectly recapitulates the deposition of chitin, thereby unveiling a highly co-ordinated mechanism for the acquisition of mature traits.
Zdroje
1. Daley WP, Yamada KM (2013) ECM-modulated cellular dynamics as a driving force for tissue morphogenesis. Curr Opin Genet Dev 23: 408–414. doi: 10.1016/j.gde.2013.05.005 23849799
2. Rozario T, DeSimone DW The extracellular matrix in development and morphogenesis: a dynamic view. Dev Biol 341: 126–140. doi: 10.1016/j.ydbio.2009.10.026 19854168
3. Moussian B (2010) Recent advances in understanding mechanisms of insect cuticle differentiation. Insect Biochem Mol Biol 40: 363–375. doi: 10.1016/j.ibmb.2010.03.003 20347980
4. Araujo SJ, Aslam H, Tear G, Casanova J (2005) mummy/cystic encodes an enzyme required for chitin and glycan synthesis, involved in trachea, embryonic cuticle and CNS development-Analysis of its role in Drosophila tracheal morphogenesis. Dev Biol 288: 179–193. 16277981
5. Devine WP, Lubarsky B, Shaw K, Luschnig S, Messina L, et al. (2005) Requirement for chitin biosynthesis in epithelial tube morphogenesis. Proc Natl Acad Sci U S A 102: 17014–17019. 16287975
6. Herscovics A, Orlean P (1993) Glycoprotein biosynthesis in yeast. FASEB J 7: 540–550.
7. Merzendorfer H, Zimoch L (2003) Chitin metabolism in insects: structure, function and regulation of chitin synthases and chitinases. J Exp Biol 206: 4393–4412. 14610026
8. Staneloni RJ, Leloir LF (1982) The biosynthetic pathway of the asparagine-linked oligosaccharides of glycoproteins. CRC Crit Rev Biochem 12: 289–326. 6806012
9. Tonning A, Helms S, Schwarz H, Uv AE, Moussian B (2006) Hormonal regulation of mummy is needed for apical extracellular matrix formation and epithelial morphogenesis in Drosophila. Development 133: 331–341. 16368930
10. Moussian B (2013) The apical plasma membrane of chitin-synthesizing epithelia. Insect Sci 20: 139–146. doi: 10.1111/j.1744-7917.2012.01549.x 23955854
11. Dong B, Hannezo E, Hayashi S (2014) Balance between apical membrane growth and luminal matrix resistance determines epithelial tubule shape. Cell Rep 7: 941–950. doi: 10.1016/j.celrep.2014.03.066 24794438
12. Luschnig S, Batz T, Armbruster K, Krasnow MA (2006) serpentine and vermiform encode matrix proteins with chitin binding and deacetylation domains that limit tracheal tube length in Drosophila. Curr Biol 16: 186–194. 16431371
13. Luschnig S, Uv A (2014) Luminal matrices: an inside view on organ morphogenesis. Exp Cell Res 321: 64–70. doi: 10.1016/j.yexcr.2013.09.010 24075963
14. Swanson LE, Beitel GJ (2006) Tubulogenesis: an inside job. Curr Biol 16: R51–53. 16431358
15. Tonning A, Hemphala J, Tang E, Nannmark U, Samakovlis C, et al. (2005) A transient luminal chitinous matrix is required to model epithelial tube diameter in the Drosophila trachea. Dev Cell 9: 423–430. 16139230
16. Wang S, Jayaram SA, Hemphala J, Senti KA, Tsarouhas V, et al. (2006) Septate-junction-dependent luminal deposition of chitin deacetylases restricts tube elongation in the Drosophila trachea. Curr Biol 16: 180–185. 16431370
17. Merzendorfer H (2006) Insect chitin synthases: a review. J Comp Physiol B 176: 1–15. 16075270
18. Merzendorfer H (2011) The cellular basis of chitin synthesis in fungi and insects: common principles and differences. Eur J Cell Biol 90: 759–769. doi: 10.1016/j.ejcb.2011.04.014 21700357
19. Iordanou E, Chandran RR, Yang Y, Essak M, Blackstone N, et al. (2014) The novel Smad protein expansion Regulates receptor tyrosine kinase pathway to control drosophila tracheal tube size. Dev Biol.
20. Rotstein B, Molnar D, Adryan B, Llimargas M (2011) Tramtrack is genetically upstream of genes controlling tracheal tube size in Drosophila. PLoS One 6: e28985. doi: 10.1371/journal.pone.0028985 22216153
21. Kuhnlein RP, Schuh R (1996) Dual function of the region-specific homeotic gene spalt during Drosophila tracheal system development. Development 122: 2215–2223. 8681802
22. Moustakas A, Heldin CH (2009) The regulation of TGFbeta signal transduction. Development 136: 3699–3714.
23. Shi Y (2001) Structural insights on Smad function in TGFbeta signaling. Bioessays 23: 223–232. 11223879
24. Tiklova K, Tsarouhas V, Samakovlis C (2013) Control of airway tube diameter and integrity by secreted chitin-binding proteins in Drosophila. PLoS One 8: e67415. doi: 10.1371/journal.pone.0067415 23826295
25. Moussian B, Schwarz H, Bartoszewski S, Nusslein-Volhard C (2005) Involvement of chitin in exoskeleton morphogenesis in Drosophila melanogaster. J Morphol 264: 117–130. 15747378
26. Moussian B, Seifarth C, Muller U, Berger J, Schwarz H (2006) Cuticle differentiation during Drosophila embryogenesis. Arthropod Struct Dev 35: 137–152. 18089066
27. Ribeiro C, Neumann M, Affolter M (2004) Genetic Control of Cell Intercalation during Tracheal Morphogenesis in Drosophila. Curr Biol 14: 2197–2207. 15620646
28. Tsarouhas V, Senti KA, Jayaram SA, Tiklova K, Hemphala J, et al. (2007) Sequential pulses of apical epithelial secretion and endocytosis drive airway maturation in Drosophila. Dev Cell 13: 214–225. 17681133
29. Wright CS (1984) Structural comparison of the two distinct sugar binding sites in wheat germ agglutinin isolectin II. J Mol Biol 178: 91–104. 6548265
30. Cohen E (2001) Chitin synthesis and inhibition: a revisit. Pest Manag Sci 57: 946–950. 11695188
31. Zhang Y, Foster JM, Nelson LS, Ma D, Carlow CK (2005) The chitin synthase genes chs-1 and chs-2 are essential for C. elegans development and responsible for chitin deposition in the eggshell and pharynx, respectively. Dev Biol 285: 330–339. 16098962
32. Hegedus D, Erlandson M, Gillott C, Toprak U (2009) New insights into peritrophic matrix synthesis, architecture, and function. Annu Rev Entomol 54: 285–302. doi: 10.1146/annurev.ento.54.110807.090559 19067633
33. Bowman SM, Free SJ (2006) The structure and synthesis of the fungal cell wall. Bioessays 28: 799–808. 16927300
34. Latge JP (2010) Tasting the fungal cell wall. Cell Microbiol 12: 863–872.
35. Xie X, Lipke PN (2010) On the evolution of fungal and yeast cell walls. Yeast 27: 479–488. 20641026
36. Merzendorfer H (2013) Chitin synthesis inhibitors: old molecules and new developments. Insect Sci 20: 121–138. doi: 10.1111/j.1744-7917.2012.01535.x 23955853
37. Chung S, Chavez C, Andrew DJ (2011) Trachealess (Trh) regulates all tracheal genes during Drosophila embryogenesis. Dev Biol 360: 160–172. 21963537
38. Broehan G, Zimoch L, Wessels A, Ertas B, Merzendorfer H (2007) A chymotrypsin-like serine protease interacts with the chitin synthase from the midgut of the tobacco hornworm. J Exp Biol 210: 3636–3643. 17921165
39. Broehan G, Kemper M, Driemeier D, Vogelpohl I, Merzendorfer H (2008) Cloning and expression analysis of midgut chymotrypsin-like proteinases in the tobacco hornworm. J Insect Physiol 54: 1243–1252. doi: 10.1016/j.jinsphys.2008.06.007 18634789
40. Maue L, Meissner D, Merzendorfer H (2009) Purification of an active, oligomeric chitin synthase complex from the midgut of the tobacco hornworm. Insect Biochem Mol Biol 39: 654–659. doi: 10.1016/j.ibmb.2009.06.005 19576988
41. Hartenstein K, Sinha P, Mishra A, Schenkel H, Torok I, et al. (1997) The congested-like tracheae gene of Drosophila melanogaster encodes a member of the mitochondrial carrier family required for gas-filling of the tracheal system and expansion of the wings after eclosion. Genetics 147: 1755–1768. 9409834
42. Campos-Ortega AJ, Hartenstein V (1985) The Embryonic Development of Drosophila Melanogaster. Springer-Verlag New York: 10–84.
43. Wiegmann BM, Trautwein MD, Kim JW, Cassel BK, Bertone MA, et al. (2009) Single-copy nuclear genes resolve the phylogeny of the holometabolous insects. BMC Biol 7: 34. doi: 10.1186/1741-7007-7-34 19552814
Štítky
Genetika Reprodukčná medicínaČlánok vyšiel v časopise
PLOS Genetics
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