Cloning and characterization of an Mrna encoding an insulin receptor from the horned scarab beetle Onthophagus nigriventris (COLEOPTERA: SCARABAEIDAE)

Archives of Insect Biochemistry and Physiology

Volumn 82, Issue 1, 2013, Pages 43-57

  Lavine, Laura Corley ^a   Hahn, Laura L ^a   Warren, Ian A ^a   Garczynski, Stephen F ^b   Dworkin, Ian ^c   Emlen, Douglas J ^d  

^a WASHINGTON STATE UNIVERSITY   (United States)

^b AGRICULTURAL RESEARCH SERVICE   (United States)

^c MICHIGAN STATE UNIVERSITY   (United States)

^d University of Montana   (United States)

Author keywords

Insulin receptor; Insulin signaling pathway; Onthophagus nigriventris; Polyphenism

Indexed keywords

COMPLEMENTARY DNA; INSULIN RECEPTOR;

ANIMAL; ANTIBODY SPECIFICITY; ARTICLE; BEETLE; DNA SEQUENCE; FEMALE; GENE EXPRESSION REGULATION; GENETICS; GROWTH, DEVELOPMENT AND AGING; LARVA; MALE; METABOLISM; MOLECULAR CLONING; MOLECULAR GENETICS; NUCLEOTIDE SEQUENCE; PHYLOGENY; SEQUENCE ANALYSIS; SEQUENCE HOMOLOGY;

ANIMALS; BEETLES; CLONING, MOLECULAR; DNA, COMPLEMENTARY; FEMALE; GENE EXPRESSION REGULATION; LARVA; MALE; MOLECULAR SEQUENCE DATA; ORGAN SPECIFICITY; PHYLOGENY; RECEPTOR, INSULIN; SEQUENCE ANALYSIS, DNA; SEQUENCE ANALYSIS, PROTEIN; SEQUENCE HOMOLOGY;

ANIMALIA; COLEOPTERA; HEXAPODA; ONTHOPHAGUS NIGRIVENTRIS; SCARABAEIDAE;

EID: 84871715850     PISSN: 07394462     EISSN: 15206327     Source Type: Journal    
DOI: 10.1002/arch.21072     Document Type: Article

References (63)

1. Ament SA, Corona M, Pollock HS, Robinson GE. 2008. Insulin signaling is involved in the regulation of worker division of labor in honeybee colonies. Proc Natl Acad Sci USA 105:4226-4231.
2. Bendtsen JD, Nielsen H, Von Heijne G, Brunak S. 2004. Improved prediction of signal peptides: SignalP 3.0. J Mol Biol 340:783-795.
3. Brogiolo W, Stocker H, Ikeya T, Rintelen F, Fernandez R, Hafen E. 2001. An evolutionarily conserved function of the Drosophila insulin receptor and insulin-like peptides in growth control. Curr Biol 11:213-221.
4. Chan SJ, Steiner DF. 2000. Insulin through the ages: phylogeny of a growth promoting and metabolic regulatory hormone. Am Zool 40:213-222.
5. Charniaux-Cotton H, Zerbib C, Meusy JJ. 1966. Monographi de la glande androgene des Cursaces superieurs. Crustaceana 10:113-136.
6. Chou CK, Dull TJ, Russell DS, Gherzi R, Lebwohl D, Ullrich A, Rosen OM. 1987. Human insulin receptors mutated at the ATP-binding site lack protein tyrosine kinase activity and fail to mediate postreceptor effects of insulin. J Biol Chem 262:1842-1847.
7. Claeys I, Simonet G, Poels J, Van Loy T, Vercammen L, De Loof A, Vanden Broeck J. 2002. Insulin-related peptides and their conserved signal transduction pathway. Peptides 23:807-816.
8. Colombani J, Raisin S, Pantalacci S, Radimerski T, Montagne J, Leopold P. 2003. A nutrient sensor mechanism controls Drosophila growth. Cell 114:739-749.
9. De Azevedo SV, Hartfelder K. 2008. The insulin signaling pathway in honey bee (Apis mellifera) caste development-differential expression of insulin-like peptides and insulin receptors in queen and worker larvae. J Insect Physiol 54:1064-1071.
10. De Meyts P. 2004. Insulin and its receptor: structure, function, and evolution. Bioessays 26:1351-1362.
11. Edgar BA. 2006. How flies get their size: genetics meets physiology. Nature Rev Gen 7:907-916.
12. Elliot JL, Oldham JM, Ahser GW, Molan PC, Bass JJ. 1996. Effect of testosterone on binding of insulin-like growth factor-I (IGF-1) and IGF-II in growing antlers of fallow deer (Dama dama). Growth Regul 6:214-221.
13. Emlen DJ. 1994. Environmental control of horn length dimorphism in the beetle Onthophagus acuminatus (Coleoptera: Scarabaeidae). Proc R Soc Lond B 256:131-136.
14. Emlen DJ. 1997. Alternative reproductive tacts and male-dimorphism in the horned beetle Onthophagus acuminatus (Coleoptera:Scarabaeidae). Behav Ecol Sociobiol 41:335-341.
15. Emlen DJ, Allen CE. 2004. Genotype to phenotype: physiological control of trait size and scaling in insects. Integr Comp Biol 43:627-634.
16. Emlen DJ, Nijhout HF. 1999. Hormonal control of male horn length dimorphism in the dung beetle Onthophagus taurus (Coleoptera: Scarabaeidae). J Insect Physiol 45:45-53.
17. Emlen DJ, Nijhout HF. 2001. Hormonal control of male horn length dimorphism in the dung beetle Onthophagus taurus (Coleoptera: Scarabaeidae): a second critical period of sensitivity to juvenile hormone. J Insect Physiol 47:1045-1054.
18. Emlen DJ, Marangelo J, Ball B, Cunningham CW. 2005. Diversity in the weapons of sexual selection: horn evolution in the beetle genus Onthophagus (Coleoptera: Scarabaeidae). Evolution 59:1060-1084.
19. Emlen DJ, Szafran Q, Corley LS, Dworkin I. 2006. Insulin signaling and limb-patterning: candidate pathways for the origin and evolutionary diversification of beetle 'horns.' Heredity 97:179-191.
20. Emlen DJ, Corley Lavine L, Ewen-Campen B. 2007. On the origin and evolutionary diversification of beetle horns. Proc Natl Acad Sci USA 104:S8661-S8668.
21. Emlen DJ, Warren I, Johns A, Dworkin I, Corley Lavine L. 2012. A mechanism of extreme growth and reliable signaling in sexually selected ornaments and weapons. Science 337:860-864.
22. Fernandez R, Tabarini D, Aspiasu N, Frasch M, Schlessinger J. 1995. The Drosophila insulin receptor homolog: a gene essential for embryonic development encodes two receptor isoforms with different signaling potential. EMBO J 14:3373-3384.
23. Garofalo RS, Rosen OM. 1988. Tissue localization of Drosophila melanogaster insulin receptor transcripts during development. Mol Cell Biol 8:1638-1647.
24. Goberdhan DCI, Wilson C. 2002. Insulin receptor-mediated organ overgrowth in Drosophila is not restricted by body size. Dev Genes Evol 212:196-202.
25. Goberdhan DC, Wilson C. 2003. The functions of insulin signaling: size isn't everything, even in Drosophila. Differentiation 71:375-397.
26. Gotoh H, Cornette R, Koshikawa S, Okada Y, Corley Lavine L, Emlen DJ, Miura T. 2011. Juvenile hormone regulates extreme mandible growth in the male stag beetle Cyclommatus metallifer. PLoS ONE 6:e21139.
27. Graf RS, Neuenschander S, Brown MR, Ackermann U. 1997. Insulin mediated secretion of ecdysteroids from mosquito ovaries and molecular cloning of the insulin receptor homologue from ovaries of blood-fed Aedes aegypti. Insect Mol Biol 6:151-163.
28. Gu LJ, Mo EY, Yang ZH, Zhu XM, Fang ZM, Sun BS, Wang CY, Bao JF, Sung CK. 2007. Expression and localization of insulin-like growth factor-I in four parts of the red deer antler. Growth Factors 25:264-279.
29. Hanks SK, Quinn AM, Hunter T. 1988. The protein tyrosine kinase family: conserved features and deduced phylogeny of the catalytic domains. Science 241:42-52.
30. Hunt JH, Wolschin F, Henshaw MT, Newman TC, Toth AL, Amdam Gro V. 2010. Differential gene expression and protein abundance evince ontogenetic bias toward castes in a primitively eusocial wasp. PLoS One 5:e10674.
31. Iguchi Y. 1998. Horn dimorphism of Allomyrina dichotoma septentrionalis (Coleoptera: Scarabaeidae) affected by larval nutrition. Ann Entom Soc Am 91:845-847.
32. Karino K, Seki N, Chiba M. 2004. Larval nutritional environment determines adult size in Japanese horned beetles Allomyrina dichotoma. Ecol Res 19:663-668.
33. Kijimoto T, Costello J, Tang Z, Moczek AP, Andrews J. 2009. EST and microarray analysis of horn development in Onthophagus beetles. BMC Genom 10:504.
34. Kramer JM, Davidge JT, Lockyer JM, Staveley BE. 2003. Expression of Drosophila FOXO regulates growth and can phenocopy starvation. BMC Dev Biol. 3:5.
35. Larkin MA, Blackshields G, Brown NP, Chenna R, McGettigan PA, McWilliam H, Valentin F, Wallace IM, Wilm A, Lopez R, Thompson JD, Gibson TJ, Higgins DG. 2007. Clustal W and Clustal X version 2.0. Bioinformatics 23:2947-2948.
36. -ΔΔCT method. Methods 25:402-408.
37. Moczek AP, Emlen DJ. 1999. Proximate determination of male horn dimorphism in the beetle Onthophagus taurus (Coleoptera: Scarabaeidae). J Evol Biol 12:27-37.
38. Moczek AP, Nijhout F. 2002. A method for sexing third instar larvae of the genus Onthophagus LATREILLE (Coleoptera: Scarabaeidae). Coleop Bull 56:270-284.
39. Mutti NS, Dolezal AG, Wolschin F, Mutti JS, Gill KS, Amdam GV. 2011. IRS and TOR nutrient-signaling pathways act via juvenile hormone to influence honey bee caste fate. J Exp Biol 214:3977-3984.
40. Nagamine C, Knight AW, Maggenti A, Paxma G. 1980. Masculinization of female Macrobrachium rosenbergii (de Man) (Decapoda, Palaemonidae) by androgenic gland implantation. Gen Comp Endocrinol 41:442-457.
41. Nielsen H, Engelbrecht J, Brunak S, Von Heijne G. 1997. Identification of prokaryotic and eukaryotic signal peptides and prediction of their cleavage sites. Protein Eng 10:1-6.
42. Oldham S, Stocker H, Laffargue M, Wittwer F, Wymann M, Hafen E. 2002. The Drosophila insulin;IGF receptor controls growth and size by modulating PrdInsP3 levels. Development 129:4103-4109.
43. Potter CJ, Huang H, Xu T. 2001. Drosophila Tsc1 functions with Tsc2 to antagonize insulin signaling in regulating cell growth, cell proliferation, and organ size. Cell 105:357-368.
44. Puig O, Tjian T. 2005. Transcriptional feedback control of insulin receptor by dFOXO1/FOXO1. Genes Dev 15:2435-2446.
45. Puig O, Marr MT, Ruhf ML, Tjian R. 2003. Control of cell number by Drosophila FOXO: downstream and feedback regulation of the insulin receptor pathway. Genes Dev 17:2006-2020.
46. Rendell M. 2008. Insulin: moments in history. Drug Dev Res 69:95-100.
47. Roovers E, Vincent ME, Van Kesteren E, Geraerts WPM, Planta RJ, Vreugdenhil E, Van Heerikhuizen H. 1995. Characterization of a putative molluscan insulin-related peptide receptor. Gene 162:181-188.
48. Rozen S, Skaletsky HJ. 2000. Primer3 on the WWW for general users and for biologist programmers. In: Krawetz S, Misener S, editors. Bioinformatics methods and protocols: methods in molecular biology. Totowa, NJ: Humana Press. p 365-386.
49. Ruan Y, Chen C, Cao Y, Garofalo RS. 1995. The Drosophila insulin receptor contains a novel carboxyl-terminal extension likely to play an important role in signal transduction. J Biol Chem 270:4236-4243.
50. Shingleton AW, Das J, Vinicius L, Stern DL. 2005. The temporal requirements for insulin signaling during development in Drosophila. PLoS Biology 3:1607.
51. Shingleton AW, Mirth CK, Bates PW. 2008. Developmental model of static allometry in holometabolous insects. Proc R Soc Lond B 275:1878-1885.
52. Snell-Rood EC, Moczek AP. 2012. Insulin signaling as a mechanism underlying developmental plasticity: the role of FOXO in a nutritional polyphenism. PLoS One 7:e34857.
53. Snell-Rood EC, Cash A, Han MV, Kijimoto T, Andrews A, Moczek AP. 2011. Developmental decoupling of alternative phenotypes: insights from the transcriptomes of horn-polyphenic beetles. Evolution 65:231-245.
54. Suttie JM, Gluckman PD, Butler JH, Fennessy PF, Corson ID, Laas FJ. 1985. Insulin-like growth factor 1 (IGF-1) antler-stimulating hormone? Endocrinology 116:846-848.
55. Suttie JM, Corson ID, Gluckman PD, Fennessy PF. 1991. Insulin-like growth factor 1, growth and body composition of red deer stags. Anim Prod 53:237-242.
56. Tamura K, Dudley J, Nei M, Kumar S. 2007. MEGA4: molecular Evolutionary Genetics Analysis (MEGA) software version 4.0. Mole Biol Evol 24:1596-1599.
57. Tang HY, Smith-Caldas MSB, Driscoll MV, Salhadar S, Shingleton AW. 2011. FOXO regulates organ-specific phenotypic plasticity in Drosophila. PLoS Genet 7:e1002373.
58. Wang Y, Mutti NS, Ihle KE, Siegel A, Dolezal AG, Kaftanoglu O, Amdam GV. 2010. Down-regulation of honey bee IRS gene biases behavior toward food rich in protein. PLoS Genet. 6, e1000896.
59. West-Eberhard MJ. 2003. Developmental plasticity and evolution. Oxford, United Kingdom: Oxford University Press, Inc.
60. Wheeler DE, Buck N, Evans JD. 2006. Expression of the insulin pathway genes during the period of caste determination in the honey bee, Apis mellifera. Insect Mol Biol 15:597-602.
61. Wolschin F, Mutti NS, Amdam Gro V. 2011. Insulin receptor substrate influences female caste development in honeybees. Biol Lett 7:112-115.
62. Wu Q, Brown MR. 2006. Signaling and function of insulin-like peptides in insects. Ann Rev Entom 51:1-24.
63. Zhulidov AV, Bogdanova EA, Shcheglov AS, Vagner LL, Khaspekov GL, Kozhemyako VB, Matz MV, Meleshkevitch E, Moroz LL, Lukyanov SA, Shagin DA. 2004. Simple cDNA normalization using Kamchatka crab duplex-specific nuclease. Nucleic Acids Res 32:e37.