Observations on the radiation of lobe-finned fishes, ray-finned fishes, and cartilaginous fishes: Phylogeny of the opioid/orphanin gene family and the 2R hypothesis

General and Comparative Endocrinology

Volumn 170, Issue 2, 2011, Pages 253-264

  Dores, Robert M ^a   Majeed, Qais ^a   Komorowski, Leanne ^a  

^a UNIVERSITY OF DENVER   (United States)

Author keywords

Cartilaginous fish; Lobe finned fish; POMC; Prodynorphin proorphanin; Proenkephalin; Ray finned fish

Indexed keywords

ALPHA INTERMEDIN; ALPHA NEOENDORPHIN; BETA ENDORPHIN; BETA INTERMEDIN; CORTICOTROPIN; DYNORPHIN; DYNORPHIN A; DYNORPHIN B; HORMONE PRECURSOR; NEUROPEPTIDE; OPIATE; ORPHANIN; PRODYNORPHIN; PROENKEPHALIN; PROOPIOMELANOCORTIN; UNCLASSIFIED DRUG;

CHORDATA; DEVONIAN; FIN (ORGAN); FISH; GENE DUPLICATION; GENETIC CONSERVATION; LIMNOLOGY; MARINE ENVIRONMENT; MULTIGENE FAMILY; NONHUMAN; NUCLEOTIDE SEQUENCE; PHYLOGENY; PHYLUM; PRIORITY JOURNAL; REVIEW; SPECIES DIVERSITY; SPECIES DOMINANCE; SPECIES EXTINCTION;

EID: 78650677129     PISSN: 00166480     EISSN: 10956840     Source Type: Journal    
DOI: 10.1016/j.ygcen.2010.09.023     Document Type: Review

References (69)

1. Alrubaian J., Danielson P., Fitzpatrick M., Schreck C., Dores R.M. Cloning of a second proopiomelanocortin cDNA from the pituitary of the sturgeon, Acipenser transmontanus. Peptides 1999, 20:431-436.
2. Alrubaian J., Danielson P., Walker D., Dores R.M. Cladistic analysis of anuran POMC sequences. Peptides 2002, 23:443-452.
3. Alrubaian J., Sollars C., Danielson P.B., Dores R.M. Evaluating the radiation of the POMC gene in teleost: characterization of American eel POMC. Gen. Comp. Endocrinol. 2003, 132:384-390.
4. Alrubaian J., Lecaude S., Barba J., Szynskie L., Jacobs N., Bauer D., Brown C., Kaminer I., Bagrosky B., Dores R.M. Trends in the evolution of the prodynorphin gene in teleosts: cloning of eel and tilapia prodynorphin cDNAs. Peptides 2006, 27:797-804.
5. Baron A., Veo K., Angleson J., Dores R.M. Modeling the evolution of the MC2R and MC5R genes: studies on the cartilaginous fish, Heterodontus francisci. Gen. Comp. Endocrinol. 2009, 161:13-19.
6. Bentley P.J. Comparative Vertebrate Endocrinology 1998, Cambridge University Press, New York, NY, p. 2. third ed.
7. Bojnik E., Magyar A., Bajusz S., Borsodi A., Benyhe S. Binding studies of novel non-mammalian enkephalins, structures predicted from frog and lungfish brain cDNA sequences. Neuropharmacology 2009, 158:867-874.
8. Carroll R.L. Vertebrate Paleontology and Evolution 1988, W.H. Freeman Press, New York.
9. Carroll R.L. The origin and early radiation of terrestrial vertebrates. J. Paleontol. 2001, 75:1202-1213.
10. Cone R.D. Studies on the physiological studies of the melanocortin system. Endocr. Rev. 2006, 27:736-749.
11. Danielson P.B., Hoversten M.T., Fitzpatrick M., Schreck C., Akil H., Dores R.M. Sturgeon orphanin, a molecular "fossil" that bridges the gap between the opioids and orphanin FQ/nociceptin. J. Biol. Chem. 2001, 276:22114-22119.
12. Danielson P., Walker D., Alrubaian J., Dores R.M. Identification of a fourth opioid core sequence in a prodynorphin cDNA cloned from the brain of the amphibian, Bufo marinus, deciphering the evolution of prodynorphin and proenkephalin. Neuroendocrinology 2002, 76:55-62.
13. Dores R.M., Gorbman A. Detection of Met-enkephalin and Leu-enkephalin in the brain of the hagfish, Eptatretus stouti, and the lamprey, Petromyzon marinus. Gen. Comp. Endocrinol. 1990, 77:489-500.
14. Dores R.M., Lecaude S. Trends in the evolution of the proopiomelanocortin gene. Gen. Comp. Endocrinol. 2005, 142:81-93.
15. Dores R.M., Gieseker K., Steveson T.C. The posttranslational modification of ß-endorphin in the intermediate pituitary of the toad, Bufo marinus, includes processing at a monobasic cleavage site. Peptides 1994, 15:1497-1504.
16. Dores R.M., Smith T.R., Rubin D.A., Danielson P., Marra L., Youson J. Deciphering posttranslational processing events in the pituitary of a neopterygian fish: cloning of a gar POMC cDNA. Gen. Comp. Endocrinol. 1997, 107:401-413.
17. Dores R.M., Sollars C., Danielson P., Lee J., Alrubaian J., Joss J.M.P. Cloning of a POMC cDNA from the pituitary of the australian lungfish, Neoceratodus forsteri: analyzing trends in the organization of the prohormone precursor, proopiomelanocortin. Gen. Comp. Endocrinol. 1999, 116:433-444.
18. Dores R.M., Costantino D., Walnutt J., Danielson P.B., Lecaude S. Analyzing the radiation of the proenkephalin gene in tetrapods: cloning of a Bombina orientalis proenkephalin cDNA. Peptides 2001, 22:2021-2025.
19. Dores R.M., Lecaude S., Bauer D., Danielson P.B. Analyzing the evolution of the opioid/orphanin gene family. Mass Spectrom. Rev. 2002, 21:220-243.
20. Dores R.M., Cameron E., Lecaude S., Danielson P.B. Presence of the δ-MSH sequence in a proopiomelanocortin cDNA cloned from the pituitary of the galeoid shark Heterodontus portusjacksoni. Gen. Comp. Endocrinol. 2003, 133:71-79.
21. Dores R.M., Sollars C., Lecaude S., Lee J., Danielson P., Alrubaian J., Lihrman I., Joss J.M.P., Vaudry H. Reconstructing the evolution of the prodynorphin gene: cloning of prodynorphin cDNAs from the brain of the Australian lungfish and the African lungfish. Neuroendocrinology 2004, 79:185-196.
22. Douglass J., Civelli O., Herbert E. Polyprotein gene expression: generation of diversity of neuroendocrine peptides. Ann. Rev. Biochem. 1984, 53:665-715.
23. Duellman W.E., Trueb L. Biology of the Amphibians 1994, The Johns Hopkins Publishing, Baltimore, USA.
24. Eiden L.E. The enkephalin-containing cell: strategies for polypeptide synthesis and secretion throughout the neuroendocrine system. Cell. Mol. Neurobiol. 1987, 7:339-352.
25. Endo D., Park M.K. Molecular characterization of the leopard gecko POMC gene and expressional change in the testis by acclimation to low temperature and with a short photoperiod. Gen. Comp. Endocrinol. 2004, 138:70-77.
26. Force A., Lynch M., Pickett F.B., Amores A., Yan Y.L., Postlethwait J. Preservation of duplicate genes by complementary, degenerative mutations. Genetics 1999, 151:1531-1545.
27. Gonzalez-Nunez V., Gonzalez S., Sarmiento R., Rodriguez R.E. Characterization of zebrafish proenkephalin reveals novel opioid sequences. Brain Res. Mol. Brain Res. 2003, 114:31-39.
28. Gonzalez-Nunez V., Gonzalez-Sarmiento R., Rodriguez R.E. Cloning and characterization of a full-length pronociceptin in zebrafish: evidence of the existence of two different nociceptin sequences in the same precursor. Biochim. Biophys. Acta 2003, 1629:114-118.
29. Gonzalez-Nunez V., Fernandez Marron., de Velasco E., Arsequell G., Valencia G., Rodriguez R.E. Identification of dynorphin a from zebrafish: a comparative study with mammalian dynorphin A. Neuroscience 2007, 144:675-684.
30. Henig J.A., Keeley F.W., Robson P., Sower S.A., Youson J.H. The appearance of proopiomelanocortin early in vertebrate evolution: cloning and sequencing of POMC from a lamprey pituitary cDNA library. Gen. Comp. Endocrinol. 1995, 99:137-144.
31. Holland P.W., Garcia-Fernadez J., Williams N.A., Sidow A. Gene duplications and the origins of vertebrate development. Development (Supplement) 1994, 125:133.
32. Hughes J., Smith T.W., Kosterlitz H.W., Fothergill L.A., Morgan B.A., Morris H.R. Identification of two related pentapeptides from the brain with potent opiate agonist activity. Nature 1975, 258:577-579.
33. Kakidani H., Furutani Y., Takahashi H., Noda M., Morimoto Y., Hirose T., Asai M., Inayama S., Nakanishi S., Numa S. Cloning and sequence analysis of cDNA for porcine beta-neo-endorphin/dynorphin precursor. Nature 1982, 298:245-249.
34. Khalap A., Bagrosky B., Lecaude S., Youson J., Danielson P., Dores R.M. Trends in the evolution of the proenkephalin and prodynorphin genes in gnathostomes. Ann. N. Y. Acad. Sci. 2005, 1040:22-37.
35. Kieffer B.L. Recent advances in molecular recognition and signal transduction of active peptides: receptors for opioid peptides. Cell. Mol. Neurobiol. 1995, 15:615-635.
36. Kilpatrick D.L., Howells R.D., Lahm H., Undenfriend S. Evidence for a proenkephalin-like precursor in amphibian brain. Proc. Natl. Acad. Sci. USA 1983, 80:5772-5775.
37. Klovins J., Haitina T., Ringholm A., Lowgren M., Fridmanis D., Slaidina M., Stier S., Schioth H.B. Cloning of two melanocortin (MC) receptors in spiny dogfish. Eur. J. Biochem. 2004, 271:4320-4331.
38. Kozak K., Costantino D., Lecaude S., Sollars C., Danielson P., Dores R.M. Analyzing the radiation of the melanocortins in amphibians: cloning of POMC cDNAs from the pituitary of the urodele amphibians, Amphiuma means and Necturus maculosus. Peptides 2005, 26:1920-1928.
39. Kuraku S., Meyer A., Kuratani S. Timing of genomic duplications relative to the origin of the vertebrates: did cyclostomes diverge before or after. Mol. Boil. Evol. 2009, 26:47-59.
40. Lecaude S., Alrubaian J., Sollars C., Propper C., Danielson P., Dores R.M. Organization of proenkephalin in amphibians: cloning of a proenkephalin cDNA from the brain of the anuran amphibian, Spea multiplicatus. Peptides 2000, 21:339-344.
41. Lee J., Alrubaian J., Dores R.M. Are lungfish living fossils? Observations on the evolution of the opioid/orphanin gene family. Gen. Comp. Endocrinol. 2006, 148:306-314.
42. Lundin L.G. Evolution of the vertebrate genome as reflected in paralogous chromosomal regions in man and the house mouse. Genomics 1993, 16:1-19.
43. Martens G.J., Herbert E. Polymorphism and absence of Leu-enkephalin sequences in proenkephalin genes in Xenopus laevis. Nature 1984, 310:251-254.
44. McClendon J., Lecaude S., Dores A.R., Dores R.M. Evolution of the opioid/ORL-1 receptor gene family. Ann. N. Y. Acad. Sci. 2010, 1200:85-94.
45. Meunier J.C., Mollereau C., Toll L., Suaudeau C., Alvinerie P., Butour J.L., Guillemot J.C., Ferrara P., Monsarrat B., Mazargull H., Vassart G., Parmentier M., Costentin J. Isolation and structure of the endogenous agonist of opioid receptor-like ORL1 receptor. Nature 1995, 377:532-535.
46. Mollereau C., Simons M.J., Soularue P., Liners F., Vassart G., Meunier J.C., Parmentier M. Structure, tissue distribution, and chromosomal localization of the prepronociceptin gene. Proc. Natl. Acad. Sci. USA 1996, 93:8666-8670.
47. Nakanishi S., Inoue A., Kita T., Nakamura M., Chung A.C.Y., Cohen S.N., Numa S. Nucleotide sequence of cloned cDNA for bovine corticotropin-beta-lipotropin precursor. Nature 1979, 278:423-427.
48. Naude R., Oelofson W., Takahashi A., Masafumi A., Kawauchi H. Molecular cloning and characterization of preproopiomelanocortin cDNA from the ostrich. Gen. Comp. Endocrinol. 2006, 146:310-317.
49. Nelson J.S. Fishes of the World 1994, John Wiley and Sons Press, New York, NY. third ed.
50. Noda M., Furutani Y., Takahashi H., Toyosato M., Notake S., Nakanishi S., Numa S. Cloning and sequence analysis of cDNA for bovine adrenal preproenkephalin. Nature 1982, 295:202-206.
51. Northcutt R.G., Gans C. The genesis of neural crest and epidermal placodes: a reinterpretation of vertebrate origins. Q. Rev. Biol. 1983, 58:1-28.
52. Ohno S., Wolf U., Atkins N.B. Evolution from fish to mammals by gene duplication. Hereditas 1968, 59:169-187.
53. Pattee P., Ilie A.E., Benyhe S., Toth G., Borsodi A., Nagalla S.R. Cloning and characterization of Xen-dorphin prohormone from Xenopus laevis: a new opioid-like prohormone distinct from proenkephalin and prodynorphin. J. Biol. Chem. 2003, 278:53098-53104.
54. Reinscheid R.K., Nothacker H.P., Bourson A., Ardati A., Hennigsen R.A., Bunzow J.R., Grandy D.K., Langen H., Monsma F.J., Civelli O. Orphanin FQ: a neuropeptide that activates an opioidlike G protein-coupled receptor. Science 1995, 270:792-794.
55. Ringholm A., Klovins J., Fredriksson R., Poliakova N., Larson E.T., Kukkonen J.P., Larhammar D., Schioth H.B. Presence of melanocortin (MC4) receptor in spiny dogfish suggests an ancient vertebrate origin of central melanocortin system. Eur. J. Biochem. 2003, 270:213-221.
56. Roberts E., Shoureshi P., Kozak K., Szynskie L., Baron A., Lecaude S., Dores R.M. Tracking the evolution of the proenkephalin gene in tetrapods. Gen. Comp. Endocrinol. 2007, 153:189-197.
57. Sallan L.C., Coates M.I. End-Devonian extinction and a bottleneck in the early evolution of modern jawed vertebrates. Proc. Natl. Acad. Sci. USA 2010, 99:8139-8144.
58. Schaeffer B., Thompson K.S. Reflections on the agnathan/gnathostome relationships. Aspects of Vertebrate History; Essays in Honor of Edwin Harris Colbert 1980, 19-33. Museum of Northern Arizona Press, Flagstaff. L.L. Jacob (Ed.).
59. Schwyzer R. ACTH: a short introductory review. Ann. N. Y. Acad. Sci. 1977, 297:3-26.
60. Shen S.-T., Lu L.-M., Chen J.-R., Chien J.-T., Yu J.Y.-L. Molecular cloning of proopiomelanocortin (POMC) cDNA from mud turtle, Pelodiscus sinensis. Gen. Comp. Endocrinol. 2003, 131:192-201.
61. Shoureshi P., Baron A., Szynskie L., Dores R.M. Analyzing the evolution of β-endorphin posttranslational processing events: studies on reptiles. Gen. Comp. Endocrinol. 2007, 153:145-158.
62. Sollars C., Danielson P., Joss J.M.P., Dores R.M. Deciphering the origin of Met-enkephalin and Leu-enkephalin in lobe-finned fish: cloning of Australian lungfish proenkephalin. Brain Res. 2000, 874:131-136.
63. Sundstrom, G., Dreborg, S., Larhammar, D., 2010. Concomitant duplication of the opioid peptide and receptor genes before the origin of jawed vertebrates. Plos one 5(5), e10512. doi:10.1371/journal.pone,001052.
64. Takahashi A., Kawauchi H. Evolution of melanocortin systems in fish. Gen. Comp. Endocrinol. 2006, 148:85-94.
65. Takahashi A., Amemiya Y., Sarashi M., Sower S.A., Kawauchi H. Melanotropin and corticotropin are encoded on two distinct genes in the lamprey, the earliest evolved extant vertebrate. Biochem. Biophys. Res. Commun. 1995, 213:490-496.
66. Takahashi A., Amemiya Y., Nozaki M., Sower S.A., Kawauchi H. Evolutionary significance of proopiomelanocortin in agnathan and chondrorichthyes. Comp. Biochem. Physiol. B Biochem. Mol. Biol. 2001, 129:283-289.
67. van Strien F.J.C., Jenks B.G., Heerma W., Versluis C., Awauchi H., Roubos E.W. C,N-acetyl β-endorphin(1-8) is the terminal product of processing of endorphins in the melanotrope cell of Xenopus laevis, as demonstrated by FAB tandem mass spectrometry. Biochem. Biophys. Res. Commun. 1993, 191:262-268.
68. Walthers E.A., Moore F.L. Cloning proenkephalin from the brain of a urodele amphibian (Taricha granulosa) using a DOR-specific primer in a 3'RACE reaction. Gen. Comp. Endocrinol. 2005, 142:364-370.
69. Wraith A., Tornsten A., Chardon P., Harbitz I., Chowdhary B.P., Andersson Lief., Lundin L.-G., Larhammar D. Evolution of the neuropeptide Y receptor family: gene and chromosome duplications deduced from the cloning and mapping of five receptor subtype genes in pig. Genome Res. 2000, 10:302-310.