#PAGE_PARAMS# #ADS_HEAD_SCRIPTS# #MICRODATA#

RR-1 Cuticular Protein TcCPR4 Is Required for Formation of Pore Canals in Rigid Cuticle


The insect cuticle is a remarkable biomaterial primarily formed from two different types of structural biopolymers, cuticular proteins and chitin. Despite a rather limited composition, insects produce diverse cuticles with the proper combination of mechanical properties such as strength, hardness and flexibility. Adult beetles are covered mostly by a hard cuticle, but they can fly because their cuticle is lightweight. The rigid cuticle is comprised of three major functional layers, namely the outermost envelope, the protein-rich epicuticle and the innermost chitin-protein rich procuticle. In addition, there are a large number of vertically oriented columnar structures denoted as pore canals that contain chitinous fibers (pore canal fibers) that are absent in soft and flexible cuticles. We have identified a cuticular structural protein, TcCPR4, which is predominantly localized in the pore canals of rigid cuticles of the red flour beetle. Loss of function of TcCPR4 by RNA interference causes abnormal and amorphous pore canal fibers resulting in less organized pore canals that do not traverse the procuticle vertically. TcCPR4 plays a major role in determining the morphology of the vertical pore canals and pore canal fibers that contribute to the formation of a lightweight and rigid beetle cuticle.


Vyšlo v časopise: RR-1 Cuticular Protein TcCPR4 Is Required for Formation of Pore Canals in Rigid Cuticle. PLoS Genet 11(2): e32767. doi:10.1371/journal.pgen.1004963
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pgen.1004963

Souhrn

The insect cuticle is a remarkable biomaterial primarily formed from two different types of structural biopolymers, cuticular proteins and chitin. Despite a rather limited composition, insects produce diverse cuticles with the proper combination of mechanical properties such as strength, hardness and flexibility. Adult beetles are covered mostly by a hard cuticle, but they can fly because their cuticle is lightweight. The rigid cuticle is comprised of three major functional layers, namely the outermost envelope, the protein-rich epicuticle and the innermost chitin-protein rich procuticle. In addition, there are a large number of vertically oriented columnar structures denoted as pore canals that contain chitinous fibers (pore canal fibers) that are absent in soft and flexible cuticles. We have identified a cuticular structural protein, TcCPR4, which is predominantly localized in the pore canals of rigid cuticles of the red flour beetle. Loss of function of TcCPR4 by RNA interference causes abnormal and amorphous pore canal fibers resulting in less organized pore canals that do not traverse the procuticle vertically. TcCPR4 plays a major role in determining the morphology of the vertical pore canals and pore canal fibers that contribute to the formation of a lightweight and rigid beetle cuticle.


Zdroje

1. Locke M (2001) The Wigglesworth Lecture: Insects for studying fundamental problems in biology. J Insect Physiol 47: 495–507. 11166314

2. 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

3. Moussian B, Seifarth C, Muller U, Berger J, Schwarz H (2006) Cuticle differentiation during Drosophila embryogenesis. Arthropod Struct Dev 35: 137–152. 18089066

4. Andersen SO (2008) Quantitative determination of catecholic degradation products from insect sclerotized cuticles. Insect Biochem Mol Biol 38: 877–882. doi: 10.1016/j.ibmb.2008.06.003 18675913

5. Hopkins TL, Kramer KJ (1992) Insect cuticle sclerotization. Annu Rev Entomol 37: 273–302.

6. Arakane Y, Muthukrishnan S, Beeman RW, Kanost MR, Kramer KJ (2005) Laccase 2 is the phenoloxidase gene required for beetle cuticle tanning. Proc Natl Acad Sci U S A 102: 11337–11342. 16076951

7. Lomakin J, Huber PA, Eichler C, Arakane Y, Kramer KJ, et al. (2011) Mechanical properties of the beetle elytron, a biological composite material. Biomacromolecules 12: 321–335. doi: 10.1021/bm1009156 21189044

8. Arakane Y, Lomakin J, Gehrke SH, Hiromasa Y, Tomich JM, et al. (2012) Formation of rigid, non-flight forewings (elytra) of a beetle requires two major cuticular proteins. PLoS Genet 8: e1002682. doi: 10.1371/journal.pgen.1002682 22570623

9. Karouzou MV, Spyropoulos Y, Iconomidou VA, Cornman RS, Hamodrakas SJ, et al. (2007) Drosophila cuticular proteins with the R&R Consensus: annotation and classification with a new tool for discriminating RR-1 and RR-2 sequences. Insect Biochem Mol Biol 37: 754–760. 17628275

10. Honeybee Genome Sequencing Consortium. (2006) Insights into social insects from the genome of the honeybee Apis mellifera. Nature 443: 931–949. 17073008

11. Cornman RS, Togawa T, Dunn WA, He N, Emmons AC, et al. (2008) Annotation and analysis of a large cuticular protein family with the R&R Consensus in Anopheles gambiae. BMC Genomics 9: 22. doi: 10.1186/1471-2164-9-22 18205929

12. Futahashi R, Okamoto S, Kawasaki H, Zhong YS, Iwanaga M, et al. (2008) Genome-wide identification of cuticular protein genes in the silkworm, Bombyx mori. Insect Biochem Mol Biol 38: 1138–1146. 19280704

13. Richards S, Gibbs RA, Weinstock GM, Brown SJ, Denell R, et al. (2008) The genome of the model beetle and pest Tribolium castaneum. Nature 452: 949–955. doi: 10.1038/nature06784 18362917

14. Dittmer NT, Hiromasa Y, Tomich JM, Lu N, Beeman RW, et al. (2012) Proteomic and transcriptomic analyses of rigid and membranous cuticles and epidermis from the elytra and hindwings of the red flour beetle, Tribolium castaneum. J Proteome Res 11: 269–278. doi: 10.1021/pr2009803 22087475

15. Willis JH (2010) Structural cuticular proteins from arthropods: annotation, nomenclature, and sequence characteristics in the genomics era. Insect Biochem Mol Biol 40: 189–204. doi: 10.1016/j.ibmb.2010.02.001 20171281

16. Ioannidou ZS, Theodoropoulou MC, Papandreou NC, Willis JH, Hamodrakas SJ (2014) CutProtFam-Pred: detection and classification of putative structural cuticular proteins from sequence alone, based on profile hidden Markov models. Insect Biochem Mol Biol 52: 51–59. doi: 10.1016/j.ibmb.2014.06.004 24978609

17. Rebers JE, Riddiford LM (1988) Structure and expression of a Manduca sexta larval cuticle gene homologous to Drosophila cuticle genes. Journal of molecular biology 203: 411–423. 2462055

18. Andersen SO (1998) Amino acid sequence studies on endocuticular proteins from the desert locust, Schistocerca gregaria. Insect Biochem Mol Biol 28: 421–434. 9692242

19. Andersen SO (2000) Studies on proteins in post-ecdysial nymphal cuticle of locust, Locusta migratoria, and cockroach, Blaberus craniifer. Insect Biochem Mol Biol 30: 569–577. 10844249

20. Willis JH, Inconomidou VA, Smith RF, Hamodrakas SJ (2005) Cuticular proteins. In: Gilbert L.I., Iatrou K., Gill S.S. (Eds). Comprehensive Molecular Insect Science, vol 4 Elsevier, Oxford Vol. 4: 79–110.

21. Noh MY, Kramer KJ, Muthukrishnan S, Kanost MR, Beeman RW, et al. (2014) Two major cuticular proteins are required for assembly of horizontal laminae and vertical pore canals in rigid cuticle of Tribolium castaneum. Insect Biochem Mol Biol 53C: 22–29.

22. Lorenzen MD, Brown SJ, Denell RE, Beeman RW (2002) Cloning and characterization of the Tribolium castaneum eye-color genes encoding tryptophan oxygenase and kynurenine 3-monooxygenase. Genetics 160: 225–234. 11805058

23. Tomoyasu Y, Arakane Y, Kramer KJ, Denell RE (2009) Repeated co-options of exoskeleton formation during wing-to-elytron evolution in beetles. Current biology: CB 19: 2057–2065. doi: 10.1016/j.cub.2009.11.014 20005109

24. Locke M (1961) Pore canals and related structures in insect cuticle. The Journal of biophysical and biochemical cytology 10: 589–618. 13762980

25. Delachambre J (1971) La formtion des canauxcutoiculaiores chezL'adulte de Tenebrio molitor L.: Etude ultrastructureale et remarques histochimiques. Tissue & cell 3: 499–520. doi: 10.1371/journal.pone.0114963 25608302

26. Wigglesworth VB (1985) The transfer of lipid in insects from the epidermal cells to the cuticle. Tissue & cell 17: 249–265.

27. Cheng L, Wang LY, Karlsson AM (2008) Image analyses of two crustacean exoskeletons and implications of the exoskeletal microstructure on the mechanical behavior. J Mater Res 23: 2854–2872.

28. Seidl B, Huemer K, Neues F, Hild S, Epple M, et al. (2011) Ultrastructure and mineral distribution in the tergite cuticle of the beach isopod Tylos europaeus Arcangeli, 1938. J Struct Biol 174: 512–526. doi: 10.1016/j.jsb.2011.03.005 21414408

29. Raabe D, Romano P, Sachs C, Fabritius H, Al-Sawalmih A, et al. (2006) Microstructure and crystallographic texture of the chitin-protein network in the biological composite material of the exoskeleton of the lobster Homarus americanus. Mat Sci Eng a-Struct 421: 143–153.

30. Arakane Y, Muthukrishnan S, Kramer KJ, Specht CA, Tomoyasu Y, et al. (2005) The Tribolium chitin synthase genes TcCHS1 and TcCHS2 are specialized for synthesis of epidermal cuticle and midgut peritrophic matrix. Insect molecular biology 14: 453–463. 16164601

31. Qiao L, Xiong G, Wang RX, He SZ, Chen J, et al. (2014) Mutation of a cuticular protein, BmorCPR2, alters larval body shape and adaptability in silkworm, Bombyx mori. Genetics 196: 1103–1115. doi: 10.1534/genetics.113.158766 24514903

32. Beeman RW, Stuart JJ (1990) A gene for lindane + cyclodiene resistance in the red flour beetle (Coleoptera: Tenebrionidae). J Econ Entomol 83: 1745–1751.

33. Tomoyasu Y, Denell RE (2004) Larval RNAi in Tribolium (Coleoptera) for analyzing adult development. Development genes and evolution 214: 575–578. 15365833

34. Arakane Y, Lomakin J, Beeman RW, Muthukrishnan S, Gehrke SH, et al. (2009) Molecular and functional analyses of amino acid decarboxylases involved in cuticle tanning in Tribolium castaneum. J Biol Chem 284: 16584–16594. doi: 10.1074/jbc.M901629200 19366687

35. Arakane Y, Dixit R, Begum K, Park Y, Specht CA, et al. (2009) Analysis of functions of the chitin deacetylase gene family in Tribolium castaneum. Insect Biochem Mol Biol 39: 355–365. doi: 10.1016/j.ibmb.2009.02.002 19268706

Štítky
Genetika Reprodukčná medicína

Článok vyšiel v časopise

PLOS Genetics


2015 Číslo 2
Najčítanejšie tento týždeň
Najčítanejšie v tomto čísle
Kurzy

Zvýšte si kvalifikáciu online z pohodlia domova

Aktuální možnosti diagnostiky a léčby litiáz
nový kurz
Autori: MUDr. Tomáš Ürge, PhD.

Všetky kurzy
Prihlásenie
Zabudnuté heslo

Zadajte e-mailovú adresu, s ktorou ste vytvárali účet. Budú Vám na ňu zasielané informácie k nastaveniu nového hesla.

Prihlásenie

Nemáte účet?  Registrujte sa

#ADS_BOTTOM_SCRIPTS#