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Evolutionary and Comparative Genomics to Drive Rational Drug Design, with Particular Focus on Neuropeptide Seven-Transmembrane Receptors

  • Received : 2016.09.06
  • Accepted : 2016.11.15
  • Published : 2017.01.01

Abstract

Seven transmembrane receptors (7TMRs), also known as G protein-coupled receptors, are popular targets of drug development, particularly 7TMR systems that are activated by peptide ligands. Although many pharmaceutical drugs have been discovered via conventional bulk analysis techniques the increasing availability of structural and evolutionary data are facilitating change to rational, targeted drug design. This article discusses the appeal of neuropeptide-7TMR systems as drug targets and provides an overview of concepts in the evolution of vertebrate genomes and gene families. Subsequently, methods that use evolutionary concepts and comparative analysis techniques to aid in gene discovery, gene function identification, and novel drug design are provided along with case study examples.

Keywords

References

  1. Abi-Rached, L., Gilles, A., Shiina, T., Pontarotti, P. and Inoko, H. (2002) Evidence of en bloc duplication in vertebrate genomes. Nat. Genet. 31, 100-105 https://doi.org/10.1038/ng855
  2. Ahmad, R., Wojciech, S. and Jockers, R. (2015) Hunting for the function of orphan GPCRs - beyond the search for the endogenous ligand. Br. J. Pharmacol. 172, 3212-3228. https://doi.org/10.1111/bph.12942
  3. Amemiya, C. T., Powers, T. P., Prohaska, S. J., Grimwood, J., Schmutz, J., Dickson, M., Miyake, T., Schoenborn, M. A., Myers, R. M., Ruddle, F. H. and Stadler, P. F. (2010) Complete HOX cluster characterization of the coelacanth provides further evidence for slow evolution of its genome. Proc. Natl. Acad. Sci. U.S.A. 107, 3622-3627. https://doi.org/10.1073/pnas.0914312107
  4. Amores, A., Catchen, J., Ferrara, A., Fontenot, Q. and Postlethwait, J. H. (2011) Genome evolution and meiotic maps by massively parallel DNA sequencing: spotted gar, an outgroup for the teleost genome duplication. Genetics 188, 799-808. https://doi.org/10.1534/genetics.111.127324
  5. Assis, R. and Bachtrog, D. (2013) Neofunctionalization of young duplicate genes in Drosophila. Proc. Natl. Acad. Sci. U.S.A. 110, 17409-17414. https://doi.org/10.1073/pnas.1313759110
  6. Baggio, L. L. and Drucker, D. J. (2007) Biology of incretins: GLP-1 and GIP. Gastroenterology 132, 2131-2157. https://doi.org/10.1053/j.gastro.2007.03.054
  7. Burt, D. W., Bruley, C., Dunn, I. C., Jones, C. T., Ramage, A., Law, A. S., Morrice, D. R., Paton, I. R., Smith, J., Windsor, D., Sazanov, A., Fries, R. and Waddington, D. (1999) The dynamics of chromosome evolution in birds and mammals. Nature 402, 411-413. https://doi.org/10.1038/46555
  8. Caputo Barucchi, V., Giovannotti, M., Nisi Cerioni, P. and Splendiani, A. (2013) Genome duplication in early vertebrates: insights from agnathan cytogenetics. Cytogenet. Genome Res. 141, 80-90. https://doi.org/10.1159/000354098
  9. Cardoso, J. C., Vieira, F. A., Gomes, A. S. and Power, D. M. (2010) The serendipitous origin of chordate secretin peptide family members. BMC Evol. Biol. 10, 135. https://doi.org/10.1186/1471-2148-10-135
  10. Cerda-Reverter, J. M., Martinez-Rodriguez, G., Zanuy, S., Carrillo, M. and Larhammar, D. (2000) Molecular evolution of the neuropeptide Y (NPY) family of peptides: cloning of three NPY-related peptides from the sea bass (Dicentrarchus labrax). Regul. Pept. 95, 25-34. https://doi.org/10.1016/S0167-0115(00)00132-4
  11. Cho, H. J., Acharjee, S., Moon, M. J., Oh, D. Y., Vaudry, H., Kwon, H. B. and Seong, J. Y. (2007) Molecular evolution of neuropeptide receptors with regard to maintaining high affinity to their authentic ligands. Gen. Comp. Endocrinol. 153, 98-107. https://doi.org/10.1016/j.ygcen.2006.12.013
  12. Civelli, O., Saito, Y., Wang, Z., Nothacker, H. P. and Reinscheid, R. K. (2006) Orphan GPCRs and their ligands. Pharmacol. Ther. 110, 525-532. https://doi.org/10.1016/j.pharmthera.2005.10.001
  13. Conroy, J. L., Free, R. B. and Sibley, D. R. (2015) Identification of G protein-biased agonists that fail to recruit ${\beta}$-arrestin or promote internalization of the D1 dopamine receptor. ACS Chem. Neurosci. 6, 681-692. https://doi.org/10.1021/acschemneuro.5b00020
  14. Cornelis, G., Vernochet, C., Malicorne, S., Souquere, S., Tzika, A. C., Goodman, S. M., Catzeflis, F., Robinson, T. J., Milinkovitch, M. C., Pierron, G., Heidmann, O., Dupressoir, A. and Heidmann, T. (2014) Retroviral envelope syncytin capture in an ancestrally diverged mammalian clade for placentation in the primitive Afrotherian tenrecs. Proc. Natl. Acad. Sci. U.S.A. 111, E4332-E4341. https://doi.org/10.1073/pnas.1412268111
  15. Davenport, A. P., Alexander, S. P., Sharman, J. L., Pawson, A. J., Benson, H. E., Monaghan, A. E., Liew, W. C., Mpamhanga, C. P., Bonner, T. I., Neubig, R. R., Pin, J. P., Spedding. M. and Harmar, A. J. (2013) International union of basic and clinical pharmacology. LXXXVIII. G protein-coupled receptor list: recommendations for new pairings with cognate ligands. Pharmacol. Rev. 65, 967-986. https://doi.org/10.1124/pr.112.007179
  16. Dehal, P. and Boore, J. L. (2005) Two rounds of whole genome duplication in the ancestral vertebrate. PLoS Biol. 3, e314. https://doi.org/10.1371/journal.pbio.0030314
  17. Dores, R. M. (2013) Observations on the evolution of the melanocortin receptor gene family: distinctive features of the melanocortin-2 receptor. Front. Neurosci. 7, 28.
  18. Dupressoir, A., Vernochet, C., Bawa, O., Harper, F., Pierron, G., Opolon, P. and Heidmann, T. (2009) Syncytin-A knockout mice demonstrate the critical role in placentation of a fusogenic, endogenous retrovirus-derived, envelope gene. Proc. Natl. Acad. Sci. U.S.A. 106, 12127-12132. https://doi.org/10.1073/pnas.0902925106
  19. Elphick, M. R. and Mirabeau, O. (2014) The evolution and variety of RFamide-type neuropeptides: insights from deuterostomian invertebrates. Front. Endocrinol. (Lausanne) 5, 93.
  20. Fredriksson, R., Lagerstrom, M. C., Lundin, L. G. and Schioth, H. B. (2003) The G-protein-coupled receptors in the human genome form five main families. Phylogenetic analysis, paralogon groups, and fingerprints. Mol. Pharmacol. 63, 1256-1272. https://doi.org/10.1124/mol.63.6.1256
  21. Gibson, T. A. and Goldberg, D. S. (2009) Questioning the ubiquity of neofunctionalization. PLoS Comput. Biol. 5, e1000252. https://doi.org/10.1371/journal.pcbi.1000252
  22. Haitina, T., Takahashi, A., Holmen, L., Enberg, J. and Schioth, H. B. (2007) Further evidence for ancient role of ACTH peptides at melanocortin (MC) receptors; pharmacology of dogfish and lamprey peptides at dogfish MC receptors. Peptides 28, 798-805. https://doi.org/10.1016/j.peptides.2006.12.015
  23. Harris, R. M., Dijkstra, P. D. and Hofmann, H. A. (2014) Complex structural and regulatory evolution of the pro-opiomelanocortin gene family. Gen. Comp. Endocrinol. 195, 107-115. https://doi.org/10.1016/j.ygcen.2013.10.007
  24. Hauser, F., Cazzamali, G., Williamson, M., Blenau, W. and Grimmelikhuijzen, C. J. (2006) A review of neurohormone GPCRs present in the fruitfly Drosophila melanogaster and the honey bee Apis mellifera. Prog. Neurobiol. 80, 1-19. https://doi.org/10.1016/j.pneurobio.2006.07.005
  25. He, X. and Zhang, J. (2005) Rapid subfunctionalization accompanied by prolonged and substantial neofunctionalization in duplicate gene evolution. Genetics 169, 1157-1164. https://doi.org/10.1534/genetics.104.037051
  26. Holland, P. W., Garcia-Fernandez, J., Williams, N. A. and Sidow, A. (1994) Gene duplications and the origins of vertebrate development. Dev. Suppl. 125-133.
  27. Holland, P. W. (2003) More genes in vertebrates? J. Struct. Funct. Genomics 3, 75-84. https://doi.org/10.1023/A:1022656931587
  28. Hwang, J. I., Moon, M. J., Park, S., Kim, D. K., Cho, E. B., Ha, N., Son, G. H., Kim, K., Vaudry, H. and Seong, J. Y. (2013) Expansion of secretin-like G protein-coupled receptors and their peptide ligands via local duplications before and after two rounds of whole-genome duplication. Mol. Biol. Evol. 30, 1119-1130. https://doi.org/10.1093/molbev/mst031
  29. Hwang, J. K., Yun, S., Moon M. J., Park C. R. and Seong, J. Y. (2014) Molecular evolution of GPCRs: GLP1/GLP1 receptors. J. Mol. Endocrinol. 52, T15-T27. https://doi.org/10.1530/JME-13-0137
  30. Jensen, J. D. and Bachtrog, D. (2011) Characterizing the influence of effective population size on the rate of adaptation: Gillespie's Darwin domain. Genome Biol. Evol. 3, 687-701. https://doi.org/10.1093/gbe/evr063
  31. Jiang, H., Lkhagva, A., Daubnerova, I., Chae, H. S., Simo, L., Jung, S. H., Yoon, Y. K., Lee, N. R., Seong, J. Y., Zitnan, D., Park, Y. and Kim, Y. J. (2013) Natalisin, a tachykinin-like signaling system, regulates sexual activity and fecundity in insects. Proc. Natl. Acad. Sci. U.S.A. 110, E3526-E3534. https://doi.org/10.1073/pnas.1310676110
  32. Katritch, V., Cherezov, V. and Stevens, R. C. (2012) Diversity and modularity of G protein-coupled receptor structures. Trends Pharmacol. Sci. 33, 17-27. https://doi.org/10.1016/j.tips.2011.09.003
  33. Kim, D. K., Cho, E. B., Moon, M. J., Park, S., Hwang, J. I., Kah, O., Sower, S. A., Vaudry, H. and Seong, J. Y. (2011) Revisiting the evolution of gonadotropin-releasing hormones and their receptors in vertebrates: secrets hidden in genomes. Gen. Comp. Endocrinol. 170, 68-78. https://doi.org/10.1016/j.ygcen.2010.10.018
  34. Kim, D. K., Cho, E. B., Moon, M. J., Park, S., Hwang, J. I., Do Rego, J. L., Vaudry, H. and Seong, J. Y. (2012) Molecular coevolution of neuropeptides gonadotropin-releasing hormone and kisspeptin with their cognate G protein-coupled receptors. Front. Neurosci. 6, 3.
  35. Kim, D. K., Yun, S., Son, G. H., Hwang, J. I., Park, C. R., Kim, J. I., Kim, K., Vaudry, H. and Seong, J. Y. (2014a) Coevolution of the spexin/galanin/kisspeptin family: Spexin activates galanin receptor type II and III. Endocrinology 155, 1864-1873. https://doi.org/10.1210/en.2013-2106
  36. Kim, H. Y., Hwang, J. I., Moon, M. J. and Seong, J. Y. (2014b) A novel long-acting glucagon-like peptide-1 agonist with improved efficacy in insulin secretion and ${\beta}$-cell growth. Endocrinol. Metab. (Seoul) 29, 320-327. https://doi.org/10.3803/EnM.2014.29.3.320
  37. Klingel, S., Morath, I., Strietz, J., Menzel, K., Holstein, T. W. and Gradl, D. (2012) Subfunctionalization and neofunctionalization of vertebrate Lef/Tcf transcription factors. Dev. Biol. 368, 44-53. https://doi.org/10.1016/j.ydbio.2012.05.012
  38. Lagerstrom, M. C., Fredriksson, R., Bjarnadottir, T. K., Fridmanis, D., Holmquist, T., Andersson, J., Yan, Y. L., Raudsepp, T., Zoorob, R., Kukkonen, J. P., Lundin, L. G., Klovins, J., Chowdhary, B. P., Postlethwait, J. H. and Schioth, H. B. (2005) Origin of the prolactin-releasing hormone (PRLH) receptors: evidence of coevolution between PRLH and a redundant neuropeptide Y receptor during vertebrate evolution. Genomics 85, 688-703. https://doi.org/10.1016/j.ygeno.2005.02.007
  39. Lagerstrom, M. C. and Schioth, H. B. (2008) Structural diversity of G protein-coupled receptors and significance for drug discovery. Nat. Rev. Drug Discov. 7, 339-357. https://doi.org/10.1038/nrd2518
  40. Larhammar, D., Lundin, L. G. and Hallbook, F. (2002) The human Hoxbearing chromosome regions did arise by block or chromosome (or even genome) duplications. Genome Res. 12, 1910-1920. https://doi.org/10.1101/gr.445702
  41. Larhammar, D. and Salaneck, E. (2004) Molecular evolution of NPY receptor subtypes. Neuropeptides 38, 141-151. https://doi.org/10.1016/j.npep.2004.06.002
  42. Lee, Y. R., Tsunekawa, K., Moon, M. J., Um, H. N., Hwang, J. I., Osugi, T., Otaki, N., Sunakawa, Y., Kim, K., Vaudry, H., Kwon, H. B., Seong, J. Y. and Tsutsui, K. (2009) Molecular evolution of multiple forms of kisspeptins and GPR54 receptors in vertebrates. Endocrinology 150, 2837-2846. https://doi.org/10.1210/en.2008-1679
  43. Levoye, A., Dam, J., Ayoub, M. A., Guillaume, J. L., Couturier, C., Delagrange, P. and Jockers, R. (2006) The orphan GPR50 receptor specifically inhibits MT1 melatonin receptor function through heterodimerization. EMBO J. 25, 3012-3023. https://doi.org/10.1038/sj.emboj.7601193
  44. Lewis, K. N., Soifer, I., Melamud, E., Roy, M., McIsaac, R. S., Hibbs, M. and Buffenstein, R. (2016) Unraveling the message: insights into comparative genomics of the naked mole-rat. Mamm. Genome 27, 259-278. https://doi.org/10.1007/s00335-016-9648-5
  45. Lindemans, M., Liu, F., Janssen, T., Husson, S. J., Mertens, I., Gade, G. and Schoofs, L. (2009) Adipokinetic hormone signaling through the gonadotropin-releasing hormone receptor modulates egg-laying in Caenorhabditis elegans. Proc. Natl. Acad. Sci. U.S.A. 106, 1642-1647. https://doi.org/10.1073/pnas.0809881106
  46. Lundin, L. G. (1993) Evolution of the vertebrate genome as reflected in paralogous chromosomal regions in man and the house mouse. Genomics 16, 1-19. https://doi.org/10.1006/geno.1993.1133
  47. Lynch, M., O'Hely, M., Walsh, B. and Force, A. (2001) The probability of preservation of a newly arisen gene duplicate. Genetics 159, 1789-1804.
  48. Mehta, T. K., Ravi, V., Yamasaki, S., Lee, A. P., Lian, M. M., Tay, B. H., Tohari, S., Yanai, S., Tay, A., Brenner, S. and Venkatesh, B. (2013) Evidence for at least six hox clusters in the Japanese lamprey (Lethenteron japonicum). Proc. Natl. Acad. Sci. U.S.A. 110, 16044-16049. https://doi.org/10.1073/pnas.1315760110
  49. Meyer, A. and Van de Peer, Y. (2005) From 2R to 3R: evidence for a fish-specific genome duplication (FSGD). Bioessays 27, 937-945. https://doi.org/10.1002/bies.20293
  50. Mirabeau, O., Perlas, E., Severini, C., Audero, E., Gascuel, O., Possenti, R., Birney, E., Rosenthal, N. and Gross, C. (2007) Identification of novel peptide hormones in the human proteome by hidden Markov model screening. Genome Res. 17, 320-327. https://doi.org/10.1101/gr.5755407
  51. Mirabeau, O. and Joly, J. S. (2013) Molecular evolution of peptidergic signaling systems in bilaterians. Proc. Natl. Acad. Sci. U.S.A. 110, E2028-E2037. https://doi.org/10.1073/pnas.1219956110
  52. Moon, M. J., Kim, H. Y., Kim, S. G., Park, J., Choi, D. S., Hwang, J. I. and Seong, J. Y. (2010) Tyr1 and Ile7 of glucose-dependent insulinotropic polypeptide (GIP) confer differential ligand selectivity toward GIP and glucagon-like peptide-1 receptors. Mol. Cells 30, 149-154. https://doi.org/10.1007/s10059-010-0100-5
  53. Moon, M. J., Lee, Y. N., Park, S., Reyes-Alcaraz, A., Hwang, J. I., Millar, R. P., Choe, H. and Seong, J. Y. (2015) Ligand binding pocket formed by evolutionarily conserved residues in the glucagon-like peptide-1 (GLP-1) receptor core domain. J. Biol. Chem. 290, 5696-5706. https://doi.org/10.1074/jbc.M114.612606
  54. Morais, J. S., Souza, M. M., Campanha, T. M., Muller, C. J., Bittencourt, A. S., Bortoli, V. C., Schenberg, L. C. and Beijamini, V. (2016) Galanin subtype 1 and subtype 2 receptors mediate opposite anxiety-like effects in the rat dorsal raphe nucleus. Behav. Brain Res. 314, 125-133. https://doi.org/10.1016/j.bbr.2016.08.007
  55. M'Kadmi, C., Leyris, J. P., Onfroy, L., Gales, C., Sauliere, A., Gagne, D., Damian, M., Mary, S., Maingot, M., Denoyelle, S., Verdie, P., Fehrentz, J. A., Martinez, J., Baneres, J. L. and Marie, J. (2015) Agonism, antagonism, and inverse agonism bias at the ghrelin receptor signaling. J. Biol. Chem. 290, 27021-27039. https://doi.org/10.1074/jbc.M115.659250
  56. Nakatani, Y., Takeda, H., Kohara, Y. and Morishita, S. (2007) Reconstruction of the vertebrate ancestral genome reveals dynamic genome reorganization in early vertebrates. Genome Res. 17, 1254-1265. https://doi.org/10.1101/gr.6316407
  57. Nishida, C., Ishijima, J., Kosaka, A., Tanabe, H., Habermann, F. A., Griffin, D. K. and Matsuda, Y. (2008) Characterization of chromosome structures of Falconinae (Falconidae, Falconiformes, Aves) by chromosome painting and delineation of chromosome rearrangements during their differentiation. Chromosome Res. 16, 171-181. https://doi.org/10.1007/s10577-007-1210-6
  58. Nordstrom, K. J., Sallman Almen, M., Edstam, M. M., Fredriksson, R. and Schioth, H. B. (2011) Independent HHsearch, Needleman--Wunsch-based, and motif analyses reveal the overall hierarchy for most of the G protein-coupled receptor families. Mol. Biol. Evol. 28, 2471-2480. https://doi.org/10.1093/molbev/msr061
  59. Oh, D. Y., Kim, K., Kwon, H. B. and Seong, J. Y. (2006) Cellular and molecular biology of orphan G protein-coupled receptors. Int. Rev. Cytol. 252, 163-218.
  60. Osugi, T., Ubuka, T. and Tsutsui, K. (2014) Review: evolution of GnIH and related peptides structure and function in the chordates. Front. Neurosci. 8, 255.
  61. Park, C. R., Moon, M. J., Park, S., Kim, D. K., Cho, E. B., Millar, R. P., Hwang, J. I. and Seong, J. Y. (2013) A novel glucagon-related peptide (GCRP) and its receptor GCRPR account for coevolution of their family members in vertebrates. PLoS ONE 8, e65420. https://doi.org/10.1371/journal.pone.0065420
  62. Putnam, N. H., Butts, T., Ferrier, D. E., Furlong, R. F., Hellsten, U., Kawashima, T., Robinson-Rechavi, M., Shoguchi, E., Terry, A., Yu, J. K., Benito-Gutierrez, E. L., Dubchak, I., Garcia-Fernandez, J., Gibson-Brown, J. J., Grigoriev, I. V., Horton, A. C., de Jong, P. J., Jurka, J., Kapitonov, V. V., Kohara, Y., Kuroki, Y., Lindquist, E., Lucas, S., Osoegawa, K., Pennacchio, L. A., Salamov, A. A., Satou, Y., Sauka-Spengler, T., Schmutz, J., Shin-I, T., Toyoda, A., Bronner-Fraser, M., Fujiyama, A., Holland, L. Z., Holland, P. W., Satoh, N. and Rokhsar, D. S. (2008) The amphioxus genome and the evolution of the chordate karyotype. Nature 453, 1064-1071. https://doi.org/10.1038/nature06967
  63. Rask-Andersen, M., Almen, M. S. and Schioth, H. B. (2011) Trends in the exploitation of novel drug targets. Nat. Rev. Drug Discov. 10, 579-590. https://doi.org/10.1038/nrd3478
  64. Rastogi, S. and Liberles, D. A. (2005) Subfunctionalization of duplicated genes as a transition state to neofunctionalization. BMC Evol. Biol. 5, 28. https://doi.org/10.1186/1471-2148-5-28
  65. Redelsperger, F., Cornelis, G., Vernochet, C., Tennant, B. C., Catzeflis, F., Mulot, B., Heidmann, O., Heidmann, T. and Dupressoir, A. (2014) Capture of syncytin-Mar1, a fusogenic endogenous retroviral envelope gene involved in placentation in the Rodentia squirrelrelated clade. J. Virol. 88, 7915-7928. https://doi.org/10.1128/JVI.00141-14
  66. Reyes-Alcaraz, A., Lee, Y. N., Son, G. H., Kim, N. H., Kim, D. K., Yun, S., Kim, D. H., Hwang, J. I. and Seong, J. Y. (2016) Development of spexin-based human galanin receptor type II-specific agonists with increased stability in serum and anxiolytic effect in mice. Sci. Rep. 6, 21453. https://doi.org/10.1038/srep21453
  67. Santini, S., Boore, J. L. and Meyer, A. (2003) Evolutionary conservation of regulatory elements in vertebrate Hox gene clusters. Genome Res. 13, 1111-1122. https://doi.org/10.1101/gr.700503
  68. Sefideh, F. A., Moon, M. J., Yun, S., Hong, S. I., Hwang, J. I. and Seong, J. Y. (2014) Local duplication of gonadotropin-releasing hormone (GnRH) receptor before two rounds of whole genome duplication and origin of the mammalian GnRH receptor. PLoS ONE 9, e87901. https://doi.org/10.1371/journal.pone.0087901
  69. Shiba, K., Kageyama, H., Takenoya, F. and Shioda, S. (2010) Galaninlike peptide and the regulation of feeding behavior and energy metabolism. FEBS J. 277, 5006-5013. https://doi.org/10.1111/j.1742-4658.2010.07933.x
  70. Steiner, D. F. (1998) The proprotein convertases. Curr. Opin. Chem. Biol. 2, 31-39. https://doi.org/10.1016/S1367-5931(98)80033-1
  71. Swanson, C. J., Blackburn, T. P., Zhang, X., Zheng, K., Xu, Z. Q., Hokfelt, T., Wolinsky, T. D., Konkel, M. J., Chen, H., Zhong, H., Walker, M. W., Craig, D. A., Gerald, C. P. and Branchek, T. A. (2005) Anxiolytic-and antidepressant-like profiles of the galanin-3 receptor (Gal3) antagonists SNAP 37889 and SNAP 398299. Proc. Natl. Acad. Sci. U.S.A. 102, 17489-17494. https://doi.org/10.1073/pnas.0508970102
  72. Taylor, A., Madison, F. N. and Fraley, G. S. (2009) Galanin-like peptide stimulates feeding and sexual behavior via dopaminergic fibers within the medial preoptic area of adult male rats. J. Chem. Neuroanat. 37, 105-111. https://doi.org/10.1016/j.jchemneu.2008.12.003
  73. Ufuk, E. (2014) G-protein coupled receptor (GPCR) targeting: technologies and global markets. BCC Res. BIO136A.
  74. Vaudry, H. and Seong, J. Y. (2014) Neuropeptide GPCRs in Neuroendocrinology. Front. Endocrinol. (Lausanne) 5, 41.
  75. Venkatesh, B., Lee, A. P., Ravi, V., Maurya, A. K., Lian, M. M., Swann, J. B., Ohta, Y., Flajnik, M. F., Sutoh, Y., Kasahara, M., Hoon, S., Gangu, V., Roy, S. W., Irimia, M., Korzh, V., Kondrychyn, I., Lim, Z. W., Tay, B. H., Tohari, S., Kong, K. W., Ho, S., Lorente-Galdos, B., Quilez, J., Marques-Bonet, T., Raney, B. J., Ingham, P. W., Tay, A., Hillier, L. W., Minx, P., Boehm, T., Wilson, R. K., Brenner, S. and Warren, W. C. (2014) Elephant shark genome provides unique insights into gnathostome evolution. Nature 505, 174-179. https://doi.org/10.1038/nature12826
  76. Vienne, A., Rasmussen, J., Abi-Rached, L., Pontarotti, P. and Gilles, A. (2003) Systematic phylogenomic evidence of en bloc duplication of the ancestral 8p11.21-8p21.3-like region. Mol. Biol. Evol. 20, 1290-1298. https://doi.org/10.1093/molbev/msg127
  77. Wong, M. K., Sze, K. H., Chen, T., Cho, C. K., Law, H. C., Chu, I. K. and Wong, A. O. (2013) Goldfish spexin: solution structure and novel function as a satiety factor in feeding control. Am. J. Physiol. Endocrinol. Metab. 305, E348-E366. https://doi.org/10.1152/ajpendo.00141.2013
  78. Yegorov, S. and Good, S. (2012) Using paleogenomics to study the evolution of gene families: origin and duplication history of the relaxin family hormones and their receptors. PLoS ONE 7, e32923. https://doi.org/10.1371/journal.pone.0032923
  79. Yue, J. X., Yu, J. K., Putnam, N. H. and Holland, L. Z. (2014) The transcriptome of an amphioxus, Asymmetron lucayanum, from the Bahamas: a window into chordate evolution. Genome Biol. Evol. 6, 2681-2696. https://doi.org/10.1093/gbe/evu212
  80. Yun, S., Furlong, M., Sim, M., Cho, M., Park, S., Cho, E. B., Reyes-Alcaraz, A., Hwang, J. I., Kim, J. and Seong, J. Y. (2015) Prevertebrate local gene duplication facilitated expansion of the neuropeptide GPCR superfamily. Mol. Biol. Evol. 32, 2803-2817. https://doi.org/10.1093/molbev/msv179

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