Divergent evolution of two corticotropin-releasing hormone (CRH) genes in teleost fishes

Frontiers in Neuroscience

Volumn 9, Issue OCT, 2015, Pages

  Grone, Brian P ^a   Maruska, Karen P ^b  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b LOUISIANA STATE UNIVERSITY   (United States)

Author keywords

Brain; Cichlid; Corticotropin releasing factor (CRF); Genome duplication; Retina; Spotted gar; Subfunctionalization; Zebrafish

Indexed keywords

CORTICOTROPIN RELEASING FACTOR;

ADULT; ANIMAL TISSUE; ARTICLE; ASTATOTILAPIA BURTONI; BRAIN; CLADISTICS; CONTROLLED STUDY; CRH1 GENE; CRHA GENE; CRHB GENE; FEMALE; FLUORESCENCE IN SITU HYBRIDIZATION; GADHUS MORHUA; GASTEROSTEUS ACULEATUS; GENE DUPLICATION; GENE EXPRESSION; GENE FUNCTION; GENE IDENTIFICATION; GENE LOCATION; HYPOTHALAMUS; JUVENILE ANIMAL; LEPISOSTEUS OCULATUS; MALE; MOLECULAR EVOLUTION; NONHUMAN; ORYZIAS LATIPES; OSMERUS MORDAX; PHYLOGENY; RETINA; SALMO SALAR; SEQUENCE ALIGNMENT; STEGASTES PARTITUS; SYNTENY; TAKIFUGU RUBRIPES; TELEOST; ZEBRA FISH;

EID: 84946574355     PISSN: 16624548     EISSN: 1662453X     Source Type: Journal    
DOI: 10.3389/fnins.2015.00365     Document Type: Article

References (79)

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. doi: 10.1038/ng855
2. Alderman, S. L., and Bernier, N. J. (2007). Localization of corticotropin-releasing factor, urotensin I, and CRF-binding protein gene expression in the brain of the zebrafish, Danio rerio. J. Comp. Neurol. 502, 783-793. doi: 10.1002/cne.21332
3. Alderman, S. L., and Bernier, N. J. (2009). Ontogeny of the corticotropin-releasing factor system in zebrafish. Gen. Comp. Endocrinol. 164, 61-69. doi: 10.1016/j.ygcen.2009.04.007
4. Alsop, D., and Vijayan, M. (2009). The zebrafish stress axis: molecular fallout from the teleost-specific genome duplication event. Gen. Comp. Endocrinol. 161, 62-66. doi: 10.1016/j.ygcen.2008.09.011
5. 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. doi: 10.1534/genetics.111.127324
6. Backström, T., and Winberg, S. (2013). Central corticotropin releasing factor and social stress. Front. Neurosci. 7:117. doi: 10.3389/fnins.2013.00117
7. Batten, T. F., Cambre, M. L., Moons, L., and Vandesande, F. (1990). Comparative distribution of neuropeptide-immunoreactive systems in the brain of the green molly, Poecilia latipinna. J. Comp. Neurol. 302, 893-919. doi: 10.1002/cne.903020416
8. Berthelot, C., Brunet, F., Chalopin, D., Juanchich, A., Bernard, M., Noël, B., et al. (2014). The rainbow trout genome provides novel insights into evolution after whole-genome duplication in vertebrates. Nat. Commun. 5, 3657. doi: 10.1038/ncomms4657
9. Bininda-Emonds, O. R., Cardillo, M., Jones, K. E., MacPhee, R. D., Beck, R. M., Grenyer, R., et al. (2007). The delayed rise of present-day mammals. Nature 446, 507-512. doi: 10.1038/nature05634
10. Braasch, I., Peterson, S. M., Desvignes, T., McCluskey, B. M., Batzel, P., and Postlethwait, J. H. (2015). A new model army: emerging fish models to study the genomics of vertebrate Evo-Devo. J. Exp. Zool. Part B Mol. Dev. Evol. 324, 316-341. doi: 10.1002/jez.b.22589
11. Braasch, I., and Postlethwait, J. (2012). "Polyploidy in fish and the teleost genome duplication," in Polyploidy and Genome Evolution, eds Soltis, P. S., Soltis, D. E. (Berlin; New York, NY: Springer Verlag), 341-383.
12. Brawand, D., Wagner, C. E., Li, Y. I., Malinsky, M., Keller, I., Fan, S., et al. (2014). The genomic substrate for adaptive radiation in African cichlid fish. Nature 513, 375-381. doi: 10.1038/nature13726
13. Broughton, R. E., Betancur, R. R., Li, C., Arratia, G., and Ortí, G. (2013). Multi-locus phylogenetic analysis reveals the pattern and tempo of bony fish evolution. PLoS Curr. 5:ecurrents.tol.2ca8041495ffafd0c92756e75247483e. doi: 10.1371/currents.tol.2ca8041495ffafd0c92756e75247483e
14. Brunet, F. G., Roest Crollius, H., Paris, M., Aury, J. M., Gibert, P., Jaillon, O., et al. (2006). Gene loss and evolutionary rates following whole-genome duplication in teleost fishes. Mol. Biol. Evol. 23, 1808-1816. doi: 10.1093/molbev/msl049
15. Burge, C., and Karlin, S. (1997). Prediction of complete gene structures in human genomic DNA. J. Mol. Biol. 268, 78-94. doi: 10.1006/jmbi.1997.0951
16. Carpenter, R. E., Maruska, K. P., Becker, L., and Fernald, R. D. (2014). Social opportunity rapidly regulates expression of CRF and CRF receptors in the brain during social ascent of a teleost fish, Astatotilapia burtoni. PLoS ONE 9:e96632. doi: 10.1371/journal.pone.0096632
17. Cerdá-Reverter, J. M., Zanuy, S., and Muñoz-Cueto, J. A. (2001). Cytoarchitectonic study of the brain of a perciform species, the sea bass (Dicentrarchus labrax). II. The diencephalon. J. Morphol. 247, 229-251. doi: 10.1002/1097-4687(200103)247:3<229::AID-JMOR1014>3.0.CO;2-K
18. Chandrasekar, G., Lauter, G., and Hauptmann, G. (2007). Distribution of corticotropin-releasing hormone in the developing zebrafish brain. J. Comp. Neurol. 505, 337-351. doi: 10.1002/cne.21496
19. Chen, C. C., and Fernald, R. D. (2008). Sequences, expression patterns and regulation of the corticotropin-releasing factor system in a teleost. Gen. Comp. Endocrinol. 157, 148-155. doi: 10.1016/j.ygcen.2008.04.003
20. Chen, C. C., and Fernald, R. D. (2011). Visual information alone changes behavior and physiology during social interactions in a cichlid fish (Astatotilapia burtoni). PLoS ONE 6:e20313. doi: 10.1371/journal.pone.0020313
21. Christoffels, A., Koh, E. G., Chia, J. M., Brenner, S., Aparicio, S., and Venkatesh, B. (2004). Fugu genome analysis provides evidence for a whole-genome duplication early during the evolution of ray-finned fishes. Mol. Biol. Evol. 21, 1146-1151. doi: 10.1093/molbev/msh114
22. David, L., Blum, S., Feldman, M. W., Lavi, U., and Hillel, J. (2003). Recent duplication of the common carp (Cyprinus carpio L.) genome as revealed by analyses of microsatellite loci. Mol. Biol. Evol. 20, 1425-1434. doi: 10.1093/molbev/msg173
23. Dehal, P., and Boore, J. L. (2005). Two rounds of whole genome duplication in the ancestral vertebrate. PLoS Biol. 3:e314. doi: 10.1371/journal.pbio.0030314
24. de Souza, F. S., Bumaschny, V. F., Low, M. J., and Rubinstein, M. (2005). Subfunctionalization of expression and peptide domains following the ancient duplication of the proopiomelanocortin gene in teleost fishes. Mol. Biol. Evol. 22, 2417-2427. doi: 10.1093/molbev/msi236
25. Fernald, R. D. (1977). Quantitative behavioural observations of Haplochromis burtoni under semi-natural conditions. Anim. Behav. 25, 643-653. doi: 10.1016/0003-3472(77)90115-4
26. Fernald, R. D., and Hirata, N. R. (1979). The ontogeny of social behavior and body coloration in the African cichlid fish Haplochromis burtoni. Zeitschrift für Tierpsychologie 50, 180-187.
27. Flik, G., Klaren, P. H., Van Den Burg, E. H., Metz, J. R., and Huising, M. O. (2006). CRF and stress in fish. Gen. Comp. Endocrinol. 146, 36-44. doi: 10.1016/j.ygcen.2005.11.005
28. Force, A., Lynch, M., Pickett, F. B., Amores, A., Yan, Y. L., and Postlethwait, J. (1999). Preservation of duplicate genes by complementary, degenerative mutations. Genetics 151, 1531-1545.
29. Fryer, J. N., and Peter, R. E. (1977). Hypothalamic control ACTH secretion in goldfish: II. Hypothalamic lesioning studies. Gen. Comp. Endocrinol. 33, 202-214. doi: 10.1016/0016-6480(77)90245-3
30. Garcia De La Serrana, D., Mareco, E. A., and Johnston, I. A. (2014). Systematic variation in the pattern of gene paralog retention between the teleost superorders Ostariophysi and Acanthopterygii. Genome Biol. Evol. 6, 981-987. doi: 10.1093/gbe/evu074
31. Gehrke, A. R., Schneider, I., de la Calle-Mustienes, E., Tena, J. J., Gomez-Marin, C., Chandran, M., et al. (2015). Deep conservation of wrist and digit enhancers in fish. Proc. Natl. Acad. Sci. U.S.A. 112, 803-808. doi: 10.1073/pnas.1420208112
32. Glasauer, S. M., and Neuhauss, S. C. (2014). Whole-genome duplication in teleost fishes and its evolutionary consequences. Mol. Gen. Genom. 289, 1045-1060. doi: 10.1007/s00438-014-0889-2
33. Grone, B. P., and Maruska, K. P. (2015). A second corticotropin-releasing hormone gene (CRH2) is conserved across vertebrate classes and expressed in the hindbrain of a basal neopterygian fish, the spotted gar (Lepisosteus oculatus). J. Comp. Neurol. 523, 1125-1143. doi: 10.1002/cne.23729
34. Guindon, S., and Gascuel, O. (2003). A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Syst. Biol. 52, 696-704. doi: 10.1080/10635150390235520
35. Hauger, R. L., Grigoriadis, D. E., Dallman, M. F., Plotsky, P. M., Vale, W. W., and Dautzenberg, F. M. (2003). International union of pharmacology. XXXVI. Current status of the nomenclature for receptors for corticotropin-releasing factor and their ligands. Pharmacol. Rev. 55, 21-26. doi: 10.1124/pr.55.1.3
36. He, X., and Zhang, J. (2005). Rapid subfunctionalization accompanied by prolonged and substantial neofunctionalization in duplicate gene evolution. Genetics 169, 1157-1164. doi: 10.1534/genetics.104.037051
37. Hoegg, S., Brinkmann, H., Taylor, J. S., and Meyer, A. (2004). Phylogenetic timing of the fish-specific genome duplication correlates with the diversification of teleost fish. J. Mol. Evol. 59, 190-203. doi: 10.1007/s00239-004-2613-z
38. Hosono, K., Kikuchi, Y., Miyanishi, H., Hiraki-Kajiyama, T., Takeuchi, A., Nakasone, K., et al. (2015). Teleocortin: a novel member of the corticotropin-releasing hormone family in teleost fish. Endocrinology 156, 2949-2957. doi: 10.1210/en.2015-1042
39. Howe, K., Clark, M. D., Torroja, C. F., Torrance, J., Berthelot, C., Muffato, M., et al. (2013). The zebrafish reference genome sequence and its relationship to the human genome. Nature 496, 498-503. doi: 10.1038/nature12111
40. Hughes, A. L. (1994). The evolution of functionally novel proteins after gene duplication. Proc. Biol. Sci. 256, 119-124. doi: 10.1098/rspb.1994.0058
41. Jaillon, O., Aury, J. M., Brunet, F., Petit, J. L., Stange-Thomann, N., Mauceli, E., et al. (2004). Genome duplication in the teleost fish Tetraodon nigroviridis reveals the early vertebrate proto-karyotype. Nature 431, 946-957. doi: 10.1038/nature03025
42. Jones, D. T., Taylor, W. R., and Thornton, J. M. (1992). The rapid generation of mutation data matrices from protein sequences. Comp. Appl. Biosci. 8, 275-282. doi: 10.1093/bioinformatics/8.3.275
43. Jones, F. C., Grabherr, M. G., Chan, Y. F., Russell, P., Mauceli, E., Johnson, J., et al. (2012). The genomic basis of adaptive evolution in threespine sticklebacks. Nature 484, 55-61. doi: 10.1038/nature10944
44. Kasahara, M., Naruse, K., Sasaki, S., Nakatani, Y., Qu, W., Ahsan, B., et al. (2007). The medaka draft genome and insights into vertebrate genome evolution. Nature 447, 714-719. doi: 10.1038/nature05846
45. Kassahn, K. S., Dang, V. T., Wilkins, S. J., Perkins, A. C., and Ragan, M. A. (2009). Evolution of gene function and regulatory control after whole-genome duplication: comparative analyses in vertebrates. Genome Res. 19, 1404-1418. doi: 10.1101/gr.086827.108
46. Katoh, K., and Standley, D. M. (2013). MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Mol. Biol. Evol. 30, 772-780. doi: 10.1093/molbev/mst010
47. Kearse, M., Moir, R., Wilson, A., Stones-Havas, S., Cheung, M., Sturrock, S., et al. (2012). Geneious Basic: an integrated and extendable desktop software platform for the organization and analysis of sequence data. Bioinformatics 28, 1647-1649. doi: 10.1093/bioinformatics/bts199
48. Kiyama, H., Shiosaka, S., Kuwayama, Y., Shibasaki, T., Ling, N., and Tohyama, M. (1984). Corticotropin-releasing factor in the amacrine cells of the chicken retina. Brain Res. 298, 197-200. doi: 10.1016/0006-8993(84)91170-3
49. Korosi, A., and Baram, T. Z. (2008). The central corticotropin releasing factor system during development and adulthood. Eur. J. Pharmacol. 583, 204-214. doi: 10.1016/j.ejphar.2007.11.066
50. Kovács, K. J. (2013). CRH: the link between hormonal-, metabolic-and behavioral responses to stress. J. Chem. Neuroanat. 54, 25-33. doi: 10.1016/j.jchemneu.2013.05.003
51. Kurrasch, D. M., Nevin, L. M., Wong, J. S., Baier, H., and Ingraham, H. A. (2009). Neuroendocrine transcriptional programs adapt dynamically to the supply and demand for neuropeptides as revealed in NSF mutant zebrafish. Neural Dev. 4:22. doi: 10.1186/1749-8104-4-22
52. Lister, J. A., Close, J., and Raible, D. W. (2001). Duplicate mitf genes in zebrafish: complementary expression and conservation of melanogenic potential. Dev. Biol. 237, 333-344. doi: 10.1006/dbio.2001.0379
53. Louis, A., Muffato, M., and Roest Crollius, H. (2013). Genomicus: five genome browsers for comparative genomics in eukaryota. Nucleic Acids Res. 41, D700-D705. doi: 10.1093/nar/gks1156
54. Lovejoy, D. A., Chang, B. S., Lovejoy, N. R., and del Castillo, J. (2014). Molecular evolution of GPCRs: CRH/CRH receptors. J. Mol. Endocrinol. 52, T43-T60. doi: 10.1530/JME-13-0238
55. Lovejoy, D. A., and de Lannoy, L. (2013). Evolution and phylogeny of the corticotropin-releasing factor (CRF) family of peptides: expansion and specialization in the vertebrates. J. Chem. Neuroanat. 54, 50-56. doi: 10.1016/j.jchemneu.2013.09.006
56. Lynch, M., and Force, A. (2000). The probability of duplicate gene preservation by subfunctionalization. Genetics 154, 459-473.
57. Maruska, K. P., and Fernald, R. D. (2012). Contextual chemosensory urine signaling in an African cichlid fish. J. Exp. Biol. 215, 68-74. doi: 10.1242/jeb.062794
58. Maruska, K. P., Ung, U. S., and Fernald, R. D. (2012). The African cichlid fish Astatotilapia burtoni uses acoustic communication for reproduction: sound production, hearing, and behavioral significance. PLoS ONE 7:e37612. doi: 10.1371/journal.pone.0037612
59. Matsuda, K. (2013). Regulation of feeding behavior and psychomotor activity by corticotropin-releasing hormone (CRH) in fish. Front. Neurosci. 7:91. doi: 10.3389/fnins.2013.00091
60. Mungpakdee, S., Seo, H. C., Angotzi, A. R., Dong, X., Akalin, A., and Chourrout, D. (2008). Differential evolution of the 13 Atlantic salmon Hox clusters. Mol. Biol. Evol. 25, 1333-1343. doi: 10.1093/molbev/msn097
61. Near, T. J., Eytan, R. I., Dornburg, A., Kuhn, K. L., Moore, J. A., Davis, M. P., et al. (2012). Resolution of ray-finned fish phylogeny and timing of diversification. Proc. Natl. Acad. Sci. U.S.A. 109, 13698-13703. doi: 10.1073/pnas.1206625109
62. Nock, T. G., Chand, D., and Lovejoy, D. A. (2011). Identification of members of the gonadotropin-releasing hormone (GnRH), corticotropin-releasing factor (CRF) families in the genome of the holocephalan, Callorhinchus milii (elephant shark). Gen. Comp. Endocrinol. 171, 237-244. doi: 10.1016/j.ygcen.2011.02.001
63. Nornes, S., Clarkson, M., Mikkola, I., Pedersen, M., Bardsley, A., Martinez, J. P., et al. (1998). Zebrafish contains two pax6 genes involved in eye development. Mech. Dev. 77, 185-196. doi: 10.1016/S0925-4773(98)00156-7
64. Ohno, S. (1970). Evolution by Gene Duplication. Berlin; New York, NY: Springer-Verlag.
65. Ohno, S., Wolf, U., and Atkin, N. B. (1968). Evolution from fish to mammals by gene duplication. Hereditas 59, 169-187. doi: 10.1111/j.1601-5223.1968.tb02169.x
66. Olianas, M. C., and Onali, P. (1995). G protein-coupled corticotropin-releasing hormone receptors in rat retina. Regul. Pept. 56, 61-70. doi: 10.1016/0167-0115(95)00007-X
67. Pepels, P. P., Meek, J., Wendelaar Bonga, S. E., and Balm, P. H. (2002). Distribution and quantification of corticotropin-releasing hormone (CRH) in the brain of the teleost fish Oreochromis mossambicus (tilapia). J. Comp. Neurol. 453, 247-268. doi: 10.1002/cne.10377
68. Skofitsch, G., and Jacobowitz, D. M. (1984). Corticotropin releasing factor-like immunoreactive neurons in the rat retina. Brain Res. Bull. 12, 539-542. doi: 10.1016/0361-9230(84)90169-2
69. Song, Y., Golling, G., Thacker, T. L., and Cone, R. D. (2003). Agouti-related protein (AGRP) is conserved and regulated by metabolic state in the zebrafish, Danio rerio. Endocrine 22, 257-265. doi: 10.1385/ENDO:22:3:257
70. Star, B., Nederbragt, A. J., Jentoft, S., Grimholt, U., Malmstrøm, M., Gregers, T. F., et al. (2011). The genome sequence of Atlantic cod reveals a unique immune system. Nature 477, 207-210. doi: 10.1038/nature10342
71. Swanson, L. W., Sawchenko, P. E., Rivier, J., and Vale, W. W. (1983). Organization of ovine corticotropin-releasing factor immunoreactive cells and fibers in the rat brain: an immunohistochemical study. Neuroendocrinology 36, 165-186. doi: 10.1159/000123454
72. Tamura, K., Peterson, D., Peterson, N., Stecher, G., Nei, M., and Kumar, S. (2011). MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol. Biol. Evol. 28, 2731-2739. doi: 10.1093/molbev/msr121
73. Toloza-Villalobos, J., Arroyo, J. I., and Opazo, J. C. (2015). The circadian clock of teleost fish: a comparative analysis reveals distinct fates for duplicated genes. J. Mol. Evol. 80, 57-64. doi: 10.1007/s00239-014-9660-x
74. Vale, W., Spiess, J., Rivier, C., and Rivier, J. (1981). Characterization of a 41-residue ovine hypothalamic peptide that stimulates secretion of corticotropin and beta-endorphin. Science 213, 1394-1397. doi: 10.1126/science.6267699
75. Williamson, D. E., and Eldred, W. D. (1989). Amacrine and ganglion cells with corticotropin-releasing-factor-like immunoreactivity in the turtle retina. J. Comp. Neurol. 280, 424-435. doi: 10.1002/cne.902800308
76. Wullimann, M. F., Rupp, B., and Reichert, H. (1996). Neuroanatomy of the Zebrafish Brain: A Topological Atlas. Basel; Boston, MA: Birkhäuser Verlag.
77. Zhang, C., Forlano, P. M., and Cone, R. D. (2012). AgRP and POMC neurons are hypophysiotropic and coordinately regulate multiple endocrine axes in a larval teleost. Cell Metab. 15, 256-264. doi: 10.1016/j.cmet.2011.12.014
78. Zmora, N., Stubblefield, J., Golan, M., Servili, A., Levavi-Sivan, B., and Zohar, Y. (2014). The medio-basal hypothalamus as a dynamic and plastic reproduction-related kisspeptin-gnrh-pituitary center in fish. Endocrinology 155, 1874-1886. doi: 10.1210/en.2013-1894
79. Zupanc, G. K., Horschke, I., and Lovejoy, D. A. (1999). Corticotropin releasing factor in the brain of the gymnotiform fish, Apteronotus leptorhynchus: immunohistochemical studies combined with neuronal tract tracing. Gen. Comp. Endocrinol. 114, 349-364. doi: 10.1006/gcen.1999.7273