Display options
Cite
Veenstra JA. Ambulacrarian insulin-related peptides and their putative receptors suggest how insulin and similar peptides may have evolved from insulin-like growth factor. PeerJ. 2021;9:e11799doi: 10.7717/peerj.11799.
Veenstra, J. A. (2021). Ambulacrarian insulin-related peptides and their putative receptors suggest how insulin and similar peptides may have evolved from insulin-like growth factor. PeerJ, 9e11799. https://doi.org/10.7717/peerj.11799
Veenstra, Jan A. "Ambulacrarian insulin-related peptides and their putative receptors suggest how insulin and similar peptides may have evolved from insulin-like growth factor." PeerJ vol. 9 (2021): e11799. doi: https://doi.org/10.7717/peerj.11799
Veenstra JA. Ambulacrarian insulin-related peptides and their putative receptors suggest how insulin and similar peptides may have evolved from insulin-like growth factor. PeerJ. 2021 Jul 14;9:e11799. doi: 10.7717/peerj.11799. eCollection 2021. PMID: 34316411; PMCID: PMC8286064.
Copy Download .nbib Format: NLM
Share it on

PeerJ. 2021 Jul 14;9:e11799. doi: 10.7717/peerj.11799. eCollection 2021.

Ambulacrarian insulin-related peptides and their putative receptors suggest how insulin and similar peptides may have evolved from insulin-like growth factor.

PeerJ

Jan A Veenstra

Affiliations

  1. INCIA UMR 5287 CNRS, Université de Bordeaux, Pessac, Gironde, France.

PMID: 34316411 PMCID: PMC8286064 DOI: 10.7717/peerj.11799

Abstract

BACKGROUND: Some insulin/IGF-related peptides (irps) stimulate a receptor tyrosine kinase (RTK) that transfers the extracellular hormonal signal into an intracellular response. Other irps, such as relaxin, do not use an RTK, but a G-protein coupled receptor (GPCR). This is unusual since evolutionarily related hormones typically either use the same or paralogous receptors. In arthropods three different irps, i.e. arthropod IGF, gonadulin and

METHODOLOGY: Genes encoding irps as well as their putative receptors were identified in genomes and transcriptomes from echinoderms and hemichordates.

RESULTS: A similar triplet of genes coding for irps also occurs in some ambulacrarians. Two of these are orthologs of arthropod IGF and dilp7 and the third is likely a gonadulin ortholog. In echinoderms, two novel irps emerged, gonad stimulating substance (GSS) and multinsulin, likely from gene duplications of the IGF and dilp7-like genes respectively. The structures of GSS diverged considerably from IGF, which would suggest they use different receptors from IGF, but no novel irp receptors evolved. If IGF and GSS use different receptors, and the evolution of GSS from a gene duplication of IGF is not associated with the appearance of a novel receptor, while irps are known to use two different types of receptors, the ancestor of GSS and IGF might have acted on both types of receptors while one or both of its descendants act on only one. There are three ambulacrarian GPCRs that have amino acid sequences suggestive of being irp GPCRs, two of these are orthologs of the gonadulin and dilp7 receptors. This suggests that the third might be an IGF receptor, and that by deduction, GSS only acts on the RTK. The evolution of GSS from IGF may represent a pattern, where IGF gene duplications lead to novel genes coding for shorter peptides that activate an RTK. It is likely this is how insulin and the insect neuroendocrine irps evolved independently from IGF.

CONCLUSION: The local gene triplication described from arthropods that yielded three genes encoding irps was already present in the last common ancestor of protostomes and deuterostomes. It seems plausible that irps, such as those produced by neuroendocrine cells in the brain of insects and echinoderm GSS evolved independently from IGF and, thus, are not true orthologs, but the result of convergent evolution.

©2021 Veenstra.

Keywords: Dilp7; Evolution; GPCR; Gonadulin; IGF; Insulin; Multinsulin; Octinsulin; Receptor tyrosine kinase; Relaxin

Conflict of interest statement

The author declares that he has no competing interests.

References

  1. Nat Biotechnol. 2011 May 15;29(7):644-52 - PubMed
  2. Proc Natl Acad Sci U S A. 2013 May 28;110(22):E2028-37 - PubMed
  3. Insect Biochem Mol Biol. 1996 Sep-Oct;26(8-9):755-65 - PubMed
  4. FASEB J. 2020 Jul;34(7):8824-8832 - PubMed
  5. Science. 2012 May 4;336(6081):579-82 - PubMed
  6. PLoS Biol. 2008 Mar 11;6(3):e58 - PubMed
  7. Nat Commun. 2019 Jul 22;10(1):3257 - PubMed
  8. Arch Insect Biochem Physiol. 2000 Feb;43(2):49-63 - PubMed
  9. Genome Biol Evol. 2021 Apr 5;13(4): - PubMed
  10. Nature. 2015 Nov 26;527(7579):459-65 - PubMed
  11. Front Endocrinol (Lausanne). 2020 Jul 17;11:461 - PubMed
  12. J Endocrinol. 2020 Oct 1;247(1):R1-R12 - PubMed
  13. Mol Syst Biol. 2011 Oct 11;7:539 - PubMed
  14. Proteins. 2004 Jun 1;55(4):874-84 - PubMed
  15. J Comp Neurol. 2017 May 1;525(7):1599-1617 - PubMed
  16. Nature. 2017 Apr 5;544(7649):231-234 - PubMed
  17. Science. 2006 Nov 10;314(5801):941-52 - PubMed
  18. Eur J Biochem. 1990 Jul 5;190(3):445-62 - PubMed
  19. Open Biol. 2016 Feb;6(2):150224 - PubMed
  20. Structure. 2010 Mar 10;18(3):320-31 - PubMed
  21. Mol Cell. 2006 Apr 21;22(2):277-83 - PubMed
  22. Gigascience. 2017 Jan 1;6(1):1-6 - PubMed
  23. PLoS One. 2020 Nov 23;15(11):e0242877 - PubMed
  24. Gen Comp Endocrinol. 2019 Sep 15;281:41-48 - PubMed
  25. Mol Ecol. 2020 Mar;29(6):1087-1102 - PubMed
  26. Gen Comp Endocrinol. 2014 Sep 1;205:68-79 - PubMed
  27. Nat Struct Mol Biol. 2016 Oct;23(10):916-920 - PubMed
  28. Gen Comp Endocrinol. 2020 Sep 15;296:113528 - PubMed
  29. Curr Biol. 2015 Oct 19;25(20):2723-9 - PubMed
  30. Insect Biochem Mol Biol. 2012 Apr;42(4):277-95 - PubMed
  31. iScience. 2019 Jan 25;11:93-113 - PubMed
  32. Eur J Biochem. 1995 Feb 1;227(3):707-14 - PubMed
  33. Nat Biotechnol. 2019 Apr;37(4):420-423 - PubMed
  34. Proc Natl Acad Sci U S A. 1994 May 24;91(11):4816-20 - PubMed
  35. Development. 2013 Sep;140(18):3915-26 - PubMed
  36. PLoS Biol. 2017 Oct 12;15(10):e2003790 - PubMed
  37. J Biol Chem. 2013 Feb 8;288(6):4424-35 - PubMed
  38. Nat Commun. 2015 Oct 29;6:8732 - PubMed
  39. FEBS Lett. 1991 Mar 25;280(2):189-94 - PubMed
  40. Front Genet. 2019 Feb 19;10:77 - PubMed
  41. PeerJ. 2020 Jul 10;8:e9534 - PubMed
  42. Front Endocrinol (Lausanne). 2021 Jun 04;12:693068 - PubMed
  43. PLoS One. 2010 Mar 10;5(3):e9490 - PubMed
  44. Genome Biol Evol. 2020 Jul 1;12(7):1080-1086 - PubMed
  45. Science. 2008 Mar 21;319(5870):1679-83 - PubMed
  46. Cells. 2020 Feb 19;9(2): - PubMed
  47. Science. 2015 Nov 13;350(6262):aac6767 - PubMed
  48. Gen Comp Endocrinol. 2020 Dec 1;299:113583 - PubMed
  49. Proc Natl Acad Sci U S A. 2009 Jun 9;106(23):9507-12 - PubMed
  50. Bioinformatics. 2000 Oct;16(10):944-5 - PubMed
  51. Proc Natl Acad Sci U S A. 1995 Jul 3;92(14):6334-8 - PubMed
  52. Cell. 2014 Jan 16;156(1-2):69-83 - PubMed

Publication Types