1932
0
  1. Home
  2. A-Z Publications
  3. Annual Review of Entomology
  4. Volume 63, 2018
  5. Article

Annual Review of Entomology

Volume 63, 2018

The Evolution and Metamorphosis of Arthropod Proteomics and Genomics

Abstract

This article presents an overview of the development of techniques for analyzing cuticular proteins (CPs), their transcripts, and their genes over the past 50 years based primarily on experience in the laboratory of J.H. Willis. It emphasizes changes in the kind of data that can be gathered and how such data provided insights into the molecular underpinnings of insect metamorphosis and cuticle structure. It describes the techniques that allowed visualization of the location of CPs at both the anatomical and intracuticular levels and measurement of the appearance and deployment of transcripts from CP genes as well as what was learned from genomic and transcriptomic data. Most of the early work was done with the cecropia silkmoth, , and later work was with .

Keyword(s): autobiography, cuticular proteins, Hyalophora cecropia, Anopheles gambiae, insect metamorphosis, juvenile hormone, RNA-Seq
Loading

Article metrics loading...

/content/journals/10.1146/annurev-ento-020117-043447
2018-01-07
2024-05-02
Loading full text...

Full text loading...

/deliver/fulltext/ento/63/1/annurev-ento-020117-043447.html?itemId=/content/journals/10.1146/annurev-ento-020117-043447&mimeType=html&fmt=ahah

Literature Cited

  1. Anderson SO, Chase AM, Willis JH. 1.  1973. The amino-acid composition of cuticles from Tenebrio molitor with special reference to the action of juvenile hormone. Insect Biochem 3:171–80 [Google Scholar]
  2. Awolola TS, Oduola OA, Strode C, Koekemoer LL, Brooke B, Ranson H. 2.  2009. Evidence of multiple pyrethroid resistance mechanisms in the malaria vector Anopheles gambiae sensu stricto from Nigeria. Trans. R. Soc. Trop. Med. Hyg. 103:1139–45 [Google Scholar]
  3. Binger LC, Willis JH. 3.  1994. Identification of the cDNA gene and promoter for a major protein from flexible cuticles of the giant silkmoth Hyalophora cecropia. Insect Biochem. Mol. Biol. 24:989–1000 [Google Scholar]
  4. Cassone BJ, Mouline K, Hahn MW, White BJ, Pombi M. 4.  et al. 2008. Differential gene expression in incipient species of Anopheles gambiae. Mol. Ecol. 17:2491–504 [Google Scholar]
  5. Chipman AD, Ferrier DE, Brena C, Qu J, Hughes DS. 5.  et al. 2014. The first myriapod genome sequence reveals conservative arthropod gene content and genome organisation in the centipede Strigamia maritima. PLOS Biol 12:e1002005 [Google Scholar]
  6. Cornman RS, Togawa T, Dunn WA, He N, Emmons AC, Willis JH. 6.  2008. Annotation and analysis of a large cuticular protein family with the R&R Consensus in Anopheles gambiae. BMC Genom 9:22 [Google Scholar]
  7. Cornman RS, Willis JH. 7.  2008. Extensive gene amplification and concerted evolution within the CPR family of cuticular proteins in mosquitoes. Insect Biochem. Mol. Biol. 38:661–76 [Google Scholar]
  8. Cornman RS, Willis JH. 8.  2009. Annotation and analysis of low-complexity protein families of Anopheles gambiae that are associated with cuticle. Insect Mol. Biol. 18:607–22 [Google Scholar]
  9. Cox DL, Willis JH. 9.  1985. The cuticular proteins of Hyalophora cecropia from different anatomical regions and metamorphic stages. Insect Biochem 15:349–62 [Google Scholar]
  10. Dotson EM, Cornel AJ, Willis JH, Collins FH. 10.  1998. A family of pupal-specific cuticular protein genes in the mosquito Anopheles gambiae. Insect Biochem. Mol. Biol. 28:459–72 [Google Scholar]
  11. Fraenkel G, Rudall KM. 11.  1947. The structure of insect cuticles. Proc. R. Soc. Med. 134:111–43 [Google Scholar]
  12. Gu S, Willis JH. 12.  2003. Distribution of cuticular protein mRNAs in silk moth integument and imaginal discs. Insect Biochem. Mol. Biol. 33:1177–88 [Google Scholar]
  13. Hackman RH. 13.  1953. Chemistry of insect cuticle. I. The water-soluble proteins. Biochem. J. 54:362–67 [Google Scholar]
  14. Hamodrakas SJ, Willis JH, Iconomidou VA. 14.  2002. A structural model of the chitin-binding domain of cuticle proteins. Insect Biochem. Mol. Biol. 32:1577–83 [Google Scholar]
  15. He N, Botelho JM, McNall RJ, Belozerov V, Dunn WA. 15.  et al. 2007. Proteomic analysis of cast cuticles from Anopheles gambiae by tandem mass spectrometry. Insect Biochem. Mol. Biol. 37:135–46 [Google Scholar]
  16. Hojrup P, Andersen SO, Roepstorff P. 16.  1986. Primary structure of a structural protein from the cuticle of the migratory locust Locusta migratoria. Biochem. J. 236:713–20 [Google Scholar]
  17. Holt RA, Subramanian GM, Halpern A, Sutton GG, Charlab R. 17.  et al. 2002. The genome sequence of the malaria mosquito Anopheles gambiae. Science 298:129–49 [Google Scholar]
  18. 18. Honeybee Genome Seq. Consort. 2006. Insights into social insects from the genome of the honeybee Apis mellifera. Nature 443:931–49 [Google Scholar]
  19. Iconomidou VA, Chryssikos GD, Gionis V, Willis JH, Hamodrakas SJ. 19.  2001. “Soft”-cuticle protein secondary structure as revealed by FT-Raman, ATR FT-IR and CD spectroscopy. Insect Biochem. Mol. Biol. 31:877–85 [Google Scholar]
  20. Iconomidou VA, Willis JH, Hamodrakas SJ. 20.  1999. Is β-pleated sheet the molecular conformation which dictates formation of helicoidal cuticle?. Insect Biochem. Mol. Biol. 29:285–92 [Google Scholar]
  21. Iconomidou VA, Willis JH, Hamodrakas SJ. 21.  2005. Unique features of the structural model of ‘hard’ cuticle proteins: implications for chitin–protein interactions and cross-linking in cuticle. Insect Biochem. Mol. Biol. 35:553–60 [Google Scholar]
  22. 22. Int. Glossina Genome Initiat. 2014. Genome sequence of the tsetse fly (Glossina morsitans): vector of African trypanosomiasis. Science 344:380–86 [Google Scholar]
  23. Ioannidou ZS, Theodoropoulou MC, Papandreou NC, Willis JH, Hamodrakas SJ. 23.  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 [Google Scholar]
  24. Jasrapuria S, Arakane Y, Osman G, Kramer KJ, Beeman RW, Muthukrishnan S. 24.  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. 40:214–27 [Google Scholar]
  25. Jasrapuria S, Specht CA, Kramer KJ, Beeman RW, Muthukrishnan S. 25.  2012. Gene families of cuticular proteins analogous to peritrophins (CPAPs) in Tribolium castaneum have diverse functions. PLOS ONE 7:e49844 [Google Scholar]
  26. Jindra M, Palli SR, Riddiford LM. 26.  2013. The juvenile hormone signaling pathway in insect development. Annu. Rev. Entomol. 58:181–204 [Google Scholar]
  27. Karouzou MV, Spyropoulos Y, Iconomidou VA, Cornman RS, Hamodrakas SJ, Willis JH. 27.  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. 37:754–60 [Google Scholar]
  28. Konopova B, Jindra M. 28.  2007. Juvenile hormone resistance gene Methoprene-tolerant controls entry into metamorphosis in the beetle Tribolium castaneum. PNAS 104:10488–93 [Google Scholar]
  29. Lampe DJ, Willis JH. 29.  1994. Characterization of a cDNA and gene encoding a cuticular protein from rigid cuticles of the giant silkmoth. Hyalophora cecropia. Insect Biochem. Mol. Biol. 24:419–35 [Google Scholar]
  30. Marinotti O, Calvo E, Nguyen QK, Dissanayake S, Ribeiro JM, James AA. 30.  2006. Genome-wide analysis of gene expression in adult Anopheles gambiae. Insect Mol. Bio. 15:1–12 [Google Scholar]
  31. Neafsey DE, Waterhouse RM, Abai MR, Aganezov SS, Alekseyev MA. 31.  et al. 2015. Mosquito genomics. Highly evolvable malaria vectors: the genomes of 16 Anopheles mosquitoes. Science 347:1258522 [Google Scholar]
  32. Papandreou NC, Iconomidou VA, Willis JH, Hamodrakas SJ. 32.  2010. A possible structural model of members of the CPF family of cuticular proteins implicating binding to components other than chitin. J. Insect Physiol. 56:1420–26 [Google Scholar]
  33. Rebers JE, Riddiford LM. 33.  1988. Structure and expression of a Manduca sexta larval cuticle gene homologous to Drosophila cuticle genes. J. Mol. Biol. 203:411–23 [Google Scholar]
  34. Rebers JE, Willis JH. 34.  2001. A conserved domain in arthropod cuticular proteins binds chitin. Insect Biochem. Mol. Biol. 31:1083–93 [Google Scholar]
  35. Roberts PE, Willis JH. 35.  1980. Effects of juvenile hormone, ecdysterone, actinomycin D, and mitomycin C on the cuticular proteins of Tenebrio molitor. J. Embryol. Exp. Morphol. 56:107–23 [Google Scholar]
  36. Roberts PE, Willis JH. 36.  1980. The cuticular proteins of Tenebrio molitor. I. Electrophoretic banding patterns during postembryonic development. Dev. Biol. 75:59–69 [Google Scholar]
  37. Ruh MF, Willis JH. 37.  1974. Synthesis of blood and cuticular proteins in late pharate adults of the cecropia silkmoth. J. Insect Physiol. 20:1277–85 [Google Scholar]
  38. Savakis C, Ashburner M, Willis JH. 38.  1986. The expression of the gene coding for alcohol dehydrogenase during the development of Drosophila melanogaster. Dev. Biol. 114:194–207 [Google Scholar]
  39. Schneiderman HA, Horwitz J. 39.  1958. The induction and termination of facultative diapause in the chalcid wasps Mormoniella vitripennis (Walker) and Tritneptis klugii (Ratzeburg). J. Exp. Biol. 35:520–51 [Google Scholar]
  40. Tetreau G, Dittmer NT, Cao X, Agrawal S, Chen Y-R. 40.  et al. 2015. Analysis of chitin-binding proteins from Manduca sexta provides new insights into evolution of peritrophin A-type chitin-binding domains in insects. Insect Biochem. Mol. Biol. 62:127–41 [Google Scholar]
  41. Togawa T, Dunn WA, Emmons AC, Nagao J, Willis JH. 41.  2008. Developmental expression patterns of cuticular protein genes with the R&R Consensus from Anopheles gambiae. Insect Biochem. Mol. Biol. 38:508–19 [Google Scholar]
  42. Togawa T, Dunn WA, Emmons AC, Willis JH. 42.  2007. CPF and CPFL, two related gene families encoding cuticular proteins of Anopheles gambiae and other insects. Insect Biochem. Mol. Biol. 37:675–88 [Google Scholar]
  43. Togawa T, Nakato H, Izumi S. 43.  2004. Analysis of the chitin recognition mechanism of cuticle proteins from the soft cuticle of the silkworm Bombyx mori. Insect Biochem. Mol. Biol. 34:1059–67 [Google Scholar]
  44. Vannini L, Dunn WA, Reed TW, Willis JH. 44.  2014. Changes in transcript abundance for cuticular proteins and other genes three hours after a blood meal in Anopheles gambiae. Insect Biochem. Mol. Biol. 44:33–43 [Google Scholar]
  45. Vannini L, Reed TW, Willis JH. 45.  2014. Temporal and spatial expression of cuticular proteins of Anopheles gambiae implicated in insecticide resistance or differentiation of M/S incipient species. Parasites Vectors 7:24 [Google Scholar]
  46. Vontas J, David JP, Nikou D, Hemingway J, Christophides GK. 46.  et al. 2007. Transcriptional analysis of insecticide resistance in Anopheles stephensi using cross-species microarray hybridization. Insect Mol. Biol. 16:315–24 [Google Scholar]
  47. Watson JD, Crick FH. 47.  1953. Genetical implications of the structure of deoxyribonucleic acid. Nature 171:964–67 [Google Scholar]
  48. Werren JH, Richards S, Desjardins CA, Niehuis O. 48.  et al. 2010. Functional and evolutionary insights from the genomes of three parasitoid Nasonia species. Science 327:343–48 [Google Scholar]
  49. Wigglesworth VB. 49.  1959. Metamorphosis, polymorphism, differentiation. Sci. Am. 200:2100–6 [Google Scholar]
  50. Williams CM. 50.  1951. Morphogenesis and the metamorphosis of insects. Harvey Lect 47:126–55 [Google Scholar]
  51. Williams CM. 51.  1959. The juvenile hormone I. Endocrine activity of the corpora allata of the adult Cecropia silkworm. Biol. Bull. 116:323–38 [Google Scholar]
  52. Willis JH. 52.  1969. The programming of differentiation and its control by juvenile hormone in saturniids. J. Embryol. Exp. Morphol. 22:27–44 [Google Scholar]
  53. Willis JH. 53.  1986. The paradigm of stage-specific gene sets in insect metamorphosis: time for revision. Arch. Insect Biochem. Physiol. 3:Suppl. 147–58 [Google Scholar]
  54. Willis JH. 54.  1989. Partial amino acid sequences of cuticular proteins from Hyalophora cecropia. Insect Biochem 19:41–46 [Google Scholar]
  55. Willis JH, Cox DL. 55.  1984. Defining the anti-metamorphic action of juvenile hormone. Biosynthesis, Metabolism and Mode of Action of Invertebrate Hormones, JA Hoffmann, M Porchet 466–74 Berlin: Springer-Verlag [Google Scholar]
  56. Willis JH, Papandreou NC, Iconomidou VA, Hamodrakas SJ. 56.  2012. Cuticular proteins. Insect Molecular Biology and Biochemistry LI Gilbert 134–66 London: Academic [Google Scholar]
  57. Willis JH, Regier JC, Debrunner BA. 57.  1981. The metamorphosis of arthropodin. Current Topics in Insect Endocrinology and Nutrition G Bhaskaran, S Friedman, JG Rodriguez 27–46 New York: Plenum Press [Google Scholar]
/content/journals/10.1146/annurev-ento-020117-043447
Loading
The Evolution and Metamorphosis of Arthropod Proteomics and Genomics
Annual Review of Entomology 63, 1 (2018); https://doi.org/10.1146/annurev-ento-020117-043447
/content/journals/10.1146/annurev-ento-020117-043447
/content/journals/10.1146/annurev-ento-020117-043447
Loading

Data & Media loading...

  • Article Type: Review Article

Most Cited Most Cited RSS feed

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error