Functional Specialization Among Members Of Knickkopf Family Of Proteins In Insect Cuticle Organization
We have identified two additional members of the family of Knickkopf (Knk)-like proteins in the genome of the red flour beetle as well as in all insect species with completely sequenced genomes. The previously characterized member of this family, TcKnk, protects chitin in the newly forming cuticle (exoskeleton) from degradation by the chitinase enzyme present in the molting fluid. Knk is also required for the laminar organization of the chitin polymer in the cuticle. The two newly identified members of this family, TcKnk2 and TcKnk3, have distinctly different but related functions. They are essential for adult morphogenesis including specialized “Velcro-like” cuticular denticles found in the lateral body wall, as well as the proper development of the tracheal lining. The TcKnk3 gene gives rise to multiple transcripts as a result of alternative polyadenylation and/or splicing, but only one of these transcripts is essential for adult development.
Vyšlo v časopise:
Functional Specialization Among Members Of Knickkopf Family Of Proteins In Insect Cuticle Organization. PLoS Genet 10(8): e32767. doi:10.1371/journal.pgen.1004537
Kategorie:
Research Article
prolekare.web.journal.doi_sk:
https://doi.org/10.1371/journal.pgen.1004537
Souhrn
We have identified two additional members of the family of Knickkopf (Knk)-like proteins in the genome of the red flour beetle as well as in all insect species with completely sequenced genomes. The previously characterized member of this family, TcKnk, protects chitin in the newly forming cuticle (exoskeleton) from degradation by the chitinase enzyme present in the molting fluid. Knk is also required for the laminar organization of the chitin polymer in the cuticle. The two newly identified members of this family, TcKnk2 and TcKnk3, have distinctly different but related functions. They are essential for adult morphogenesis including specialized “Velcro-like” cuticular denticles found in the lateral body wall, as well as the proper development of the tracheal lining. The TcKnk3 gene gives rise to multiple transcripts as a result of alternative polyadenylation and/or splicing, but only one of these transcripts is essential for adult development.
Zdroje
1. Muthukrishnan S, Merzendorfer H, Arakane Y, Kramer KJ (2012) Chitin metabolism in insects. Insect Bio Mol Bio: San Diego: Gilbert, L. I. Elsevier Inc. pp. 193–235.
2. MerzendorferH (2006) Insect chitin synthases: a review. Journal of Comparative Physiology B-Biochemical Systemic and Environmental Physiology 176: 1–15.
3. MerzendorferH, ZimochL (2003) Chitin metabolism in insects: structure, function and regulation of chitin synthases and chitinases. J Exp Biol 206: 4393–4412.
4. MoussianB (2010) Recent advances in understanding mechanisms of insect cuticle differentiation. Insect Biochem Mol Biol 40: 363–375.
5. MoussianB, SeifarthC, MullerU, BergerJ, SchwarzH (2006) Cuticle differentiation during Drosophila embryogenesis. Arthropod Struct Dev 35: 137–152.
6. ArakaneY, LomakinJ, GehrkeSH, HiromasaY, TomichJM, et al. (2012) Formation of rigid, non-flight forewings (elytra) of a beetle requires two major cuticular proteins. PLoS Genet 8: e1002682.
7. JasrapuriaS, ArakaneY, OsmanG, KramerKJ, BeemanRW, et al. (2010) Genes encoding proteins with peritrophin A-type chitin-binding domains in Tribolium castaneum are grouped into three distinct families based on phylogeny, expression and function. Insect Biochem Mol Biol 40: 214–227.
8. LockeM, HuieP (1979) Apolysis and the turnover of plasma-membrane plaques during cuticle formation in an insect. Tissue & Cell 11: 277–291.
9. Noble-NesbittJ (1963) Cuticle and associated structures of Podura aquatica at moult. Q J Microsc Sci 104: 369–391.
10. Reynolds SE, Samuels RI (1996) Physiology and biochemistry of insect moulting fluid. Advances in Insect Physiology, Vol 26. pp. 157–232.
11. ChaudhariSS, ArakaneY, SpechtCA, MoussianB, BoyleDL, et al. (2011) Knickkopf protein protects and organizes chitin in the newly synthesized insect exoskeleton. Proc Natl Acad Sci U S A 108: 17028–17033.
12. WieschausE, Nusslein-VolhardC, JurgensG (1984) Mutations affecting the pattern of the larval cuticle in Drosophila melanogaster. Roux Arch Dev Biol 193: 196–307.
13. OstrowskiS, DierickHA, BejsovecA (2002) Genetic control of cuticle formation during embryonic development of Drosophila melanogaster. Genetics 161: 171–182.
14. MoussianB, TangE, TonningA, HelmsS, SchwarzH, et al. (2006) Drosophila Knickkopf and Retroactive are needed for epithelial tube growth and cuticle differentiation through their specific requirement for chitin filament organization. Development 133: 163–171.
15. ChaudhariSS, ArakaneY, SpechtCA, MoussianB, KramerKJ, et al. (2013) Retroactive maintains cuticle integrity by promoting the trafficking of Knickkopf into the procuticle of Tribolium castaneum. PLoS Genet 9: e1003268.
16. TamuraK, DudleyJ, NeiM, KumarS (2007) MEGA4: Molecular evolutionary genetics analysis (MEGA) software version 4.0. Mol Biol Evol 24: 1596–1599.
17. AravindL (2001) DOMON: an ancient extracellular domain in dopamine beta-monooxygenase and other proteins. Trends Biochem Sci 26: 524–526.
18. IyerLM, AnantharamanV, AravindL (2007) The DOMON domains are involved in heme and sugar recognition. Bioinformatics 23: 2660–2664.
19. ShaikKS, WangY, AravindL, MoussianB (2014) The Knickkopf DOMON domain is essential for cuticle differentiation in Drosophila melanogaster. Arch Insect Biochem Physiol 86: 100–106.
20. ArakaneY, LiB, MuthukrishnanS, BeemanRW, KramerKJ, et al. (2008) Functional analysis of four neuropeptides, EH, ETH, CCAP and bursicon, and their receptors in adult ecdysis behavior of the red flour beetle, Tribolium castaneum. Mech Dev 125: 984–995.
21. ArakaneY, MuthukrishnanS, KramerKJ, SpechtCA, TomoyasuY, et al. (2005) The Tribolium chitin synthase genes TcCHS1 and TcCHS2 are specialized for synthesis of epidermal cuticle and midgut peritrophic matrix. Insect Mol Biol 14: 453–463.
22. CelnikerSE, DillonLA, GersteinMB, GunsalusKC, HenikoffS, et al. (2009) Unlocking the secrets of the genome. Nature 459: 927–930.
23. WalkerDL, WangD, JinY, RathU, WangY, et al. (2000) Skeletor, a novel chromosomal protein that redistributes during mitosis provides evidence for the formation of a spindle matrix. J Cell Biol 151: 1401–1412.
24. HogenkampDG, ArakaneY, ZimochL, MerzendorferH, KramerKJ, et al. (2005) Chitin synthase genes in Manduca sexta: characterization of a gut-specific transcript and differential tissue expression of alternately spliced mRNAs during development. Insect Biochem Mol Biol 35: 529–540.
25. ZimochL, HogenkampDG, KramerKJ, MuthukrishnanS, MerzendorferH (2005) Regulation of chitin synthesis in the larval midgut of Manduca sexta. Insect Biochem Mol Biol 35: 515–527.
26. BeemanRW, StuartJJ (1990) A gene for lindane + cyclodiene resistance in the red flour beetle (Coleoptera, Tenebrionidae). J Econ Entomol 83: 1745–1751.
27. ArakaneY, MuthukrishnanS, BeemanRW, KanostMR, KramerKJ (2005) Laccase 2 is the phenoloxidase gene required for beetle cuticle tanning. Proc Natl Acad Sci U S A 102: 11337–11342.
28. ArakaneY, SpechtCA, KramerKJ, MuthukrishnanS, BeemanRW (2008) Chitin synthases are required for survival, fecundity and egg hatch in the red flour beetle, Tribolium castaneum. Insect Biochem Mol Biol 38: 959–962.
Štítky
Genetika Reprodukčná medicínaČlánok vyšiel v časopise
PLOS Genetics
2014 Číslo 8
- Je „freeze-all“ pro všechny? Odborníci na fertilitu diskutovali na virtuálním summitu
- Gynekologové a odborníci na reprodukční medicínu se sejdou na prvním virtuálním summitu
Najčítanejšie v tomto čísle
- Meta-Analysis of Genome-Wide Association Studies in African Americans Provides Insights into the Genetic Architecture of Type 2 Diabetes
- KDM6 Demethylase Independent Loss of Histone H3 Lysine 27 Trimethylation during Early Embryonic Development
- The RNA Helicases AtMTR4 and HEN2 Target Specific Subsets of Nuclear Transcripts for Degradation by the Nuclear Exosome in
- EF-P Dependent Pauses Integrate Proximal and Distal Signals during Translation