Molecular coevolution of neuropeptides gonadotropin-releasing hormone and kisspeptin with their cognate G protein-coupled receptors

Frontiers in Neuroscience

Volumn , Issue JAN, 2012, Pages

  Kim, Dong Kyu ^a   Cho, Eun Bee ^a   Moon, Mi Jin ^a   Park, Sumi ^a   Hwang, Jong Ik ^a   Rego, Jean Luc Do ^b   Vaudry, Hubert ^b   Seong, Jae Young ^a  

^a Korea University College of Medicine   (South Korea)

^b UNIVERSITÉ DE ROUEN   (France)

Author keywords

Comparative genomics; Evolution; G protein coupled receptors; Gonadotropin releasing hormone; Kisspeptin

Indexed keywords

G PROTEIN COUPLED RECEPTOR; G PROTEIN COUPLED RECEPTOR 54; GONADORELIN; GONADORELIN RECEPTOR; KISSPEPTIN; NEUROPEPTIDE;

AMIDATION; AMINO ACID SEQUENCE; BINDING AFFINITY; COEVOLUTION; CONVERGENT EVOLUTION; GENE DUPLICATION; GENETIC VARIABILITY; HUMAN; HYPOTHALAMUS HYPOPHYSIS SYSTEM; LIGAND BINDING; MOLECULAR EVOLUTION; MOLECULAR PHYLOGENY; NONHUMAN; ORTHOLOGY; PROTEIN CONFORMATION; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; REVIEW;

EID: 84861895488     PISSN: 16624548     EISSN: 1662453X     Source Type: Journal    
DOI: 10.3389/fnins.2012.00003     Document Type: Review

References (48)

1. Acharjee, S., Do-Rego, J. L., Oh, D. Y., Ahn, R. S., Choe, H., Vaudry, H., Kim, K., Seong, J. Y., and Kwon, H. B. (2004). Identification of amino acid residues that direct differential lig-and selectivity of mammalian and nonmammalian V1a type receptors for arginine vasopressin and vaso-tocin. Insights into molecular coevo-lution of V1a type receptors and their ligands. J. Biol. Chem. 279, 54445-54453.
2. 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.
3. Conlon, J. M., and Larhammar, D. (2005). The evolution of neu-roendocrine peptides. Gen. Comp. Endocrinol. 142, 53-59.
4. d'Anglemont de Tassigny, X., Fagg, L. A., Dixon, J. P., Day, K., Leitch, H. G., Hendrick, A. G., Zahn, D., Frances-chini, I., Caraty, A., Carlton, M. B., Aparicio, S. A., and Colledge, W. H. (2007). Hypogonadotropichypogo-nadism in mice lacking a functional Kiss1 gene. Proc. Natl. Acad. Sci. U.S.A. 104, 10714-10719.
5. de Roux, N., Genin, E., Carel, J. C., Mat-suda, F., Chaussain, J. L., and Mil-grom, E. (2003). Hypogonadotropic hypogonadism due to loss of function of the KiSS1-derived peptide receptor GPR54. Proc. Natl. Acad. Sci. U.S.A. 100, 10972-10976.
6. Fernald, R. D., and White, R. B. (1999). Gonadotropin-releasing hormone genes: phylogeny, structure, and functions. Front. Neuro endocrinol. 20,224-240.
7. Flanagan, C. A., Becker, II, Davidson, J. S., Wakefield, I. K., Zhou, W., Sealfon, S. C., and Millar, R. P. (1994). Glutamate 301 of the mouse gonadotropin-releasing hormone receptor confers specificity for arginine 8 of mammalian gonadotropin-releasing hormone. J. Biol. Chem. 269,22636-22641.
8. 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. Phyloge-netic analysis, paralogon groups, and fingerprints. Mol Pharmacol. 63, 1256-1272.
9. Fromme, B. J., Katz, A. A., Roeske, R. W., Millar, R. P., and Flanagan, C. A. (2001). Role of aspartate7.32(302) of the human gonadotropin-releasing hormone receptor in stabilizing a high-affinity ligand conformation. Mol. Pharmacol. 60, 1280-1287.
10. Hoyle, C. H. (1999). Neuropeptide families and their receptors: evolutionary perspectives. Brain Res. 848, 1-25.
11. Hrabovszky, E., Kallo, I., Szlavik, N., Keller, E., Merchenthaler, I., and Liposits, Z. (2007). Gonadotropin-releasing hormone neurons express estrogen receptor-beta. J. Clin. Endocrinol. Metab. 92,2827-2830.
12. Ikemoto, T., and Park, M. K. (2003). Identification and characterization of the reptilian GnRH-II gene in the leopard gecko, Eublepharis macular-ius, and its evolutionary considerations. Gene 316, 157-165.
13. Ikemoto, T., and Park, M. K. (2007). Comparative analysis of the pituitary and ovarian GnRH systems in the leopard gecko: signaling crosstalk between multiple receptor subtypes in ovarian follicles. J. Mol. Endocrinol. 38, 289-304.
14. Kah, O., Lethimonier, C., Somoza, G., Guilgur, L. G., Vaillant, C., and Lareyre, J. J. (2007). GnRH and GnRH receptors in metazoa: a historical, comparative, and evolutive perspective. Gen. Comp. Endocrinol. 153, 346-364.
15. Kavanaugh, S. I., Nozaki, M., and Sower, S. A. (2008). Origins of gonadotropin-releasing hormone (GnRH) in vertebrates: identification of a novel GnRH in a basalvertebrate, the sealamprey. Endocrinology 149, 3860-3869.
16. 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.
17. Kinoshita, M., Tsukamura, H., Adachi, S., Matsui, H., Uenoyama, Y., Iwata, K., Yamada, S., Inoue, K., Ohtaki, T., Matsumoto, H., and Maeda, K. (2005). Involvement of central metastin in the regulation of pre-ovulatoryluteinizinghormone surge and estrous cyclicity in female rats. Endocrinology 146,4431-4436.
18. Kitahashi, T., Ogawa, S., and Parhar, I. S. (2009). Cloning and expression of kiss2 in the zebrafish and medaka. Endocrinology 150, 821-831.
19. Kotani, M., Detheux, M., Vandenbo-gaerde, A., Communi, D., Van-derwinden, J. M., Le Poul, E., Brezillon, S., Tyldesley, R., Suarez-Huerta, N., Vandeput, F., Blanpain, C., Schiffmann, S. N., Vassart, G., and Parmentier, M. (2001). The metastasis suppressor gene KiSS-Iencodes kisspeptins, the natural ligands of the orphan G protein-coupled receptor GPR54. J. Biol Chem. 276, 34631-34636.
20. Larhammar, D., Lundin, L. G., and Hall-book, F. (2002). The human Hox-bearing chromosome regions did arise by block or chromosome (or even genome) duplications. Genome Res. 12, 1910-1920.
21. Larsson, T. A., Olsson, F., Sundstrom, G., Lundin, L. G., Brenner, S., Venkatesh, B., and Larhammar, D. (2008). Early vertebrate chromosome duplications and the evolution of the neuropeptide Y receptor gene regions. BMCEvol Biol. 8,184. doi:10.1186/1471-2148-8-184
22. 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.
23. Li, J. H., Choe, H., Wang, A. F., Maiti, K., Wang, C., Salam, A., Chun, S. Y., Lee, W. K., Kim, K., Kwon, H. B., and Seong, J. Y. (2005). Extracellular loop 3 (EL3) and EL3-proximal transmembrane helix 7 of the mammalian type I and type II gonadotropin-releasing hormone(GnRH) receptors determine differential ligand selectivity to GnRH-I and GnRH-II. Mol. Pharmacol. 67,1099-1110.
24. Lindemans, M., Janssen, T., Beets, I., Temmerman, L., Meelkop, E., and Schoofs, L. (2011). Gonadotropin-releasing hormone and adipo-kinetic hormone signaling systems share a common evolutionary origin. Front. Endocrinol. 2:16. doi:10.3389/fendo.2011.00016
25. Lundin, L. G. (1993). Evolution of the vertebrate genome as reflected in paralogous chromosomal regions inman and the house mouse. Genomics 16, 1-19.
26. Mayer, C., and Boehm, U. (2011). Female reproductive maturation in the absence of kisspeptin/GPR54 signaling. Nat. Neurosci. 14, 704-710.
27. Messager, S., Chatzidaki, E. E., Ma, D., Hendrick, A. G., Zahn, D., Dixon, J., Thresher, R. R., Malinge, I., Lomet, D., Carlton, M. B., Colledge, W. H., Caraty, A., and Aparicio, S. A. (2005). Kisspeptin directly stimulates gonadotropin-releasing hormone release via G protein-coupled receptor 54. Proc. Natl. Acad. Sci. U.S.A. 102,1761-1766.
28. Millar, R., Lowe, S., Conklin, D., Paw-son, A., Maudsley, S., Troskie, B., Ott, T., Millar, M., Lincoln, G., Sellar, R., Faurholm, B., Scobie, G., Kuest-ner, R., Terasawa, E., and Katz, A. (2001). A novel mammalian receptor for the evolutionarily conserved type II GnRH. Proc. Natl. Acad. Sci. U.S.A. 98, 9636-9641.
29. Millar, R. P., Lu, Z. L., Pawson, A. J., Flanagan, C. A., Morgan, K., and Maudsley, S. R. (2004). Gonadotropin-releasing hormone receptors. Endocr. Rev. 25, 235-275.
30. Moon, M. J., Kim, H. Y., Park, S., Kim, D. K., Cho, E. B., Park, C. R., You, D. Y., Hwang, J.-I., Kim, K., Choe, H., and Seong, J. Y (2012). Evolutionarily conserved residues at the GLP-1 receptor core confer ligand-induced receptor activation. J. Biol. Chem. doi: 10.1074/jbc.mill.276808. [Epub ahead of print].
31. Muir, A. I., Chamberlain, L., Elshourbagy, N. A., Michalovich, D., Moore, D. J., Calamari, A., Szekeres, P. G., Sarau, H. M., Chambers, J. K., Murdock, P., Steplewski, K., Shabon, U., Miller, J. E., Middleton, S. E., Darker, J. G., Larminie, C. G., Wilson, S., Bergsma, D. J., Emson, P., Faull, R., Philpott, K. L., and Harrison, D. C. (2001). AXOR12, a novel human G protein-coupled receptor, activated by the peptide KiSS-1. J. Biol. Chem. 276, 28969-28975.
32. Oakley, A. E., Clifton, D. K., and Steiner, R. A. (2009). Kisspeptin signaling in the brain. Endocr. Rev. 30, 713-743.
33. 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.
34. Ohkura, S., Uenoyama, Y., Yamada, S., Homma, T., Takase, K., Inoue, N., Maeda, K., and Tsukamura, H. (2009). Physiological role of metastin/kisspeptin in regulating gonadotropin-releasing hormone (GnRH) secretion in female rats. Peptides 30, 49-56.
35. Ohno, S. (1970). Evolution by Gene Duplication. New York: Allen & Unwin Springer-Verlag.
36. Ohtaki, T., Shintani, Y., Honda, S., Mat-sumoto, H., Hori, A., Kanehashi, K., Terao, Y., Kumano, S., Takatsu, Y., Masuda, Y., Ishibashi, Y., Watanabe, T., Asada, M., Yamada, T., Suenaga, M., Kitada, C., Usuki, S., Kurokawa, T., Onda, H., Nishimura, O., and Fujino, M. (2001). Metastasis suppressor gene KiSS-1 encodes pep-tide ligand of a G-protein-coupled receptor. Nature 411, 613-617.
37. Okubo, K., and Nagahama, Y (2008). Structural and functional evolution of gonadotropin-releasing hormone in vertebrates. Acta Physiol (Oxf) 193,3-15.
38. Powell, J. F., Zohar, Y., Elizur, A., Park, M., Fischer, W. H., Craig, A. G., Riv-ier, J. E., Lovejoy, D. A., and Sherwood, N. M. (1994). Three forms of gonadotropin-releasing hormone characterized from brains of one species. Proc. Natl. Acad. Sci. U.S.A. 91,12081-12085.
39. Schally, A. V., Arimura, A., Kastin, A. J., Matsuo, H., Baba, Y., Redding, T.W., Nair, R. M., Debeljuk, L., and White, W. E (1971). Gonadotropin-releasing hormone: one polypeptide regulates secretion of luteinizing and follicle-stimulating hormones. Science 173,1036-1038.
40. Seminara, S. B., Messager, S., Chatzi-daki, E. E., Thresher, R. R., Acierno, J. S. Jr., Shagoury, J. K., Bo-Abbas, Y., Kuohung, W., Schwinof, K. M., Hendrick, A. G., Zahn, D., Dixon, J., Kaiser, U. B., Slaugenhaupt, S. A., Gusella, J. F., O'Rahilly, S., Carlton, M. B., Crowley, W. F. Jr., Aparicio, S. A., and Colledge, W. H. (2003). The GPR54 gene as a regulator of puberty. N. Engl. J. Med. 349, 1614-1627.
41. Servili, A., Le Page, Y., Leprince, J., Caraty, A., Escobar, S., Parhar, I. S., Seong, J. Y., Vaudry, H., and Kah, O. (2011). Organization of two independent kisspeptin systems derived from evolutionary-ancient kiss genes in the brain of zebrafish. Endocrinology 152, 1527-1540.
42. Silver, M. R., Kawauchi, H., Nozaki, M., and Sower, S. A. (2004). Cloning and analysis of the lamprey GnRH-III cDNA from eight species of lamprey representing the three families of Petromyzontif-ormes. Gen. Comp. Endocrinol. 139, 85-94.
43. Tello, J. A., and Sherwood, N. M. (2009). Amphioxus: beginning of vertebrate and end of invertebrate type GnRH receptor lineage. Endocrinology 150, 2847-2856.
44. Tello, J. A., Wu, S., Rivier, J. E., and Sherwood, N. M. (2008). Four functional GnRH receptors in zebrafish: analysis of structure, signaling, synteny and phylogeny. Integr. Comp. Biol. 48, 570-587.
45. Um, H. N., Han, J. M., Hwang, J. I., Hong, S. I., Vaudry, H., and Seong, J. Y. (2010). Molecular coevolution of kisspeptins and their receptors from fish to mammals. Ann. N. Y Acad. Sci. 1200, 67-74.
46. Wang, C., Yun, O., Maiti, K., Oh, D. Y., Kim, K. K., Chae, C. H., Lee, C. J., Seong, J. Y., and Kwon, H. B. (2004). Position of Pro and Ser near Glu7.32 in the extracellular loop 3 of mammalian and non-mammalian gonadotropin-releasing hormone (GnRH) receptors is a critical determinant for differential ligand selectivity for mammalian GnRH and chicken GnRH-II. Mol. Endocrinol. 18, 105-116.
47. Wang, L., Bogerd, J., Choi, H. S., Seong, J. Y., Soh, J. M., Chun, S. Y., Blomen-rohr, M., Troskie, B. E., Millar, R. P., Yu, W H., McCann, S. M., and Kwon, H. B. (2001). Three distinct types of GnRH receptor characterized in the bullfrog. Proc. Natl. Acad. Sci. U.S.A. 98,361-366.
48. Yoo, M. S., Kang, H. M., Choi, H. S., Kim, J. W., Troskie, B. E., Millar, R. P., and Kwon, H. B. (2000).Molecular cloning, distribution and pharmacological characterization of a novel gonadotropin-releasing hormone ([Trp8] GnRH) in frog brain. Mol. Cell Endocrinol. 164, 197-204.