Synteny and phylogenetic analysis of paralogous thyrostimulin beta subunits (GpB5) in vertebrates

English version

Autoři: Krist Hausken ^aff001; Berta Levavi-Sivan ^aff001
Působiště autorů: Department of Animal Sciences, Robert H. Smith Faculty of Agriculture, Food, and Environment, The Hebrew University of Jerusalem, Rehovot, Israel ^aff001
Vyšlo v časopise: PLoS ONE 14(9)
Kategorie: Research Article
doi: https://doi.org/10.1371/journal.pone.0222808

Souhrn

At some point early in the vertebrate lineage, two whole genome duplication events (1R, 2R) took place that allowed for the diversification and sub-/neo-functionalization of the glycoprotein hormones (GpHs). All jawed vertebrates possess the GpHs luteinizing hormone (LH), follicle stimulating hormone (FSH), and thyroid stimulating hormone (TSH), each of which are heterodimers with a common alpha subunit and unique beta subunits. In 2002, a novel glycoprotein hormone named thyrostimulin was described to have unique GpA2 and GpB5 subunits that were homologous to the vertebrate alpha and beta subunits. The presence of GpA2 and GpB5 in representative protostomes and deuterostomes indicates their ancestry in the GpH family. There are several reports of GpH subunit evolution, but none have included GpA2 and GpB5 for species in each major vertebrate class. Thus, we addressed the ancestry of two paralogous GpB5 subunits (GpB5a and GpB5b) that were previously only recognized in two teleost species. Our search for orthologous GpB5a and GpB5b sequences in representative vertebrates and phylogenetic analysis, in addition to the currently published evolutionary scenarios of the GpH family, supports that GpB5a and GpB5b are paralogs that arose from the first vertebrate whole genome duplication event (1R). Syntenic analysis supports lineage specific losses of GpB5a in chondrichthyes, basal actinopterygians, and tetrapods, and retention in coelacanth and teleosts. Additionally, we were unable to identify GpA2 transcripts from tilapia mRNA, suggesting that this species does not produce heterodimeric thyrostimulin. While the conserved or even species-specific functional role of thyrostimulin or its individual subunits are still unknown in vertebrates, the analyses presented here provide context for future studies on the functional divergence of the GpH family.

Klíčová slova:

Biology and life sciences – Organisms – Eukaryota – Animals – Vertebrates – Evolutionary biology – Evolutionary systematics – Phylogenetics – Phylogenetic analysis – Taxonomy – Biochemistry – Hormones – Peptide hormones – Thyroid-stimulating hormone – Research and analysis methods – Computational techniques – Split-decomposition method – Multiple alignment calculation – Database and informatics methods – Bioinformatics – Sequence analysis – Sequence alignment – Sequence motif analysis – Amino acid sequence analysis – Sequence databases – Biological databases – Computer and information sciences – Data management

Zdroje

1. Pierce JG, Parsons TF. Glycoprotein hormones: structure and function. Annual review of biochemistry. 1981;50:465–95. doi: 10.1146/annurev.bi.50.070181.002341 6267989.

2. Ulloa-Aguirre A, Maldonado A, Damian-Matsumura P, Timossi C. Endocrine regulation of gonadotropin glycosylation. Arch Med Res. 2001;32(6):520–32. Epub 2001/12/26. doi: S0188-4409(01)00319-8 [pii]. 11750727.

3. Alvarez E, Cahoreau C, Combarnous Y. Comparative structure analyses of cystine knot-containing molecules with eight aminoacyl ring including glycoprotein hormones (GPH) alpha and beta subunits and GPH-related A2 (GPA2) and B5 (GPB5) molecules. Reproductive biology and endocrinology: RB&E. 2009;7:90. doi: 10.1186/1477-7827-7-90 19715619; PubMed Central PMCID: PMC3224965.

4. Wu H, Lustbader JW, Liu Y, Canfield RE, Hendrickson WA. Structure of human chorionic gonadotropin at 2.6 A resolution from MAD analysis of the selenomethionyl protein. Structure. 1994;2(6):545–58. Epub 1994/06/15. 7922031.

5. Okada SL, Ellsworth JL, Durnam DM, Haugen HS, Holloway JL, Kelley ML, et al. A glycoprotein hormone expressed in corticotrophs exhibits unique binding properties on thyroid-stimulating hormone receptor. Molecular endocrinology. 2006;20(2):414–25. doi: 10.1210/me.2005-0270 16210345.

6. Nakabayashi K, Matsumi H, Bhalla A, Bae J, Mosselman S, Hsu SY, et al. Thyrostimulin, a heterodimer of two new human glycoprotein hormone subunits, activates the thyroid-stimulating hormone receptor. The Journal of clinical investigation. 2002;109(11):1445–52. doi: 10.1172/JCI14340 12045258; PubMed Central PMCID: PMC150994.

7. Hsu SY, Nakabayashi K, Bhalla A. Evolution of glycoprotein hormone subunit genes in bilateral metazoa: identification of two novel human glycoprotein hormone subunit family genes, GPA2 and GPB5. Molecular endocrinology. 2002;16(7):1538–51. doi: 10.1210/mend.16.7.0871 12089349.

8. Moroz LL, Edwards JR, Puthanveettil SV, Kohn AB, Ha T, Heyland A, et al. Neuronal transcriptome of Aplysia: neuronal compartments and circuitry. Cell. 2006;127(7):1453–67. doi: 10.1016/j.cell.2006.09.052 17190607; PubMed Central PMCID: PMC4024467.

9. Dos Santos S, Bardet C, Bertrand S, Escriva H, Habert D, Querat B. Distinct expression patterns of glycoprotein hormone-alpha2 and -beta5 in a basal chordate suggest independent developmental functions. Endocrinology. 2009;150(8):3815–22. Epub 2009/03/07. doi: en.2008-1743 [pii] doi: 10.1210/en.2008-1743 19264871.

10. Buechi HB, Bridgham JT. Evolution of specificity in cartilaginous fish glycoprotein hormones and receptors. General and comparative endocrinology. 2017;246:309–20. doi: 10.1016/j.ygcen.2017.01.007 28062301.

11. Sower SA, Decatur WA, Hausken KN, Marquis TJ, Barton SL, Gargan J, et al. Emergence of an Ancestral Glycoprotein Hormone in the Pituitary of the Sea Lamprey, a Basal Vertebrate. Endocrinology. 2015;156(8):3026–37. Epub 2015/06/13. doi: 10.1210/en.2014-1797 26066074.

12. Hausken KN, Tizon B, Shpilman M, Barton S, Decatur W, Plachetzki D, et al. Cloning and characterization of a second lamprey pituitary glycoprotein hormone, thyrostimulin (GpA2/GpB5). General and comparative endocrinology. 2018;264:16–27. doi: 10.1016/j.ygcen.2018.04.010 29678725.

13. Ohno S. Evolution by Gene Duplication: Springer, Berlin, Heidelberg; 1970.

14. Sun SC, Hsu PJ, Wu FJ, Li SH, Lu CH, Luo CW. Thyrostimulin, but not thyroid-stimulating hormone (TSH), acts as a paracrine regulator to activate the TSH receptor in mammalian ovary. The Journal of biological chemistry. 2010;285(6):3758–65. doi: 10.1074/jbc.M109.066266 19955180; PubMed Central PMCID: PMC2823517.

15. van Zeijl CJ, Surovtseva OV, Wiersinga WM, Boelen A, Fliers E. Transient hypothyroxinemia in juvenile glycoprotein hormone subunit B5 knock-out mice. Molecular and cellular endocrinology. 2010;321(2):231–8. doi: 10.1016/j.mce.2010.03.002 20223276.

16. Rocco DA, Paluzzi JP. Functional role of the heterodimeric glycoprotein hormone, GPA2/GPB5, and its receptor, LGR1: An invertebrate perspective. General and comparative endocrinology. 2016;234:20–7. doi: 10.1016/j.ygcen.2015.12.011 26704853.

17. Macdonald LE, Wortley KE, Gowen LC, Anderson KD, Murray JD, Poueymirou WT, et al. Resistance to diet-induced obesity in mice globally overexpressing OGH/GPB5. Proceedings of the National Academy of Sciences of the United States of America. 2005;102(7):2496–501. doi: 10.1073/pnas.0409849102 15699348; PubMed Central PMCID: PMC548327.

18. Park JI, Semyonov J, Chang CL, Hsu SY. Conservation of the heterodimeric glycoprotein hormone subunit family proteins and the LGR signaling system from nematodes to humans. Endocrine. 2005;26(3):267–76. doi: 10.1385/ENDO:26:3:267 16034181.

19. Dos Santos S, Mazan S, Venkatesh B, Cohen-Tannoudji J, Querat B. Emergence and evolution of the glycoprotein hormone and neurotrophin gene families in vertebrates. BMC Evol Biol. 2011;11:332. Epub 2011/11/17. doi: 1471-2148-11-332 [pii] doi: 10.1186/1471-2148-11-332 22085792.

20. Camacho C, Coulouris G, Avagyan V, Ma N, Papadopoulos J, Bealer K, et al. BLAST+: architecture and applications. BMC bioinformatics. 2009;10:421. doi: 10.1186/1471-2105-10-421 20003500; PubMed Central PMCID: PMC2803857.

21. Yebra-Pimentel ES, Gebert M, Jansen HJ, Jong-Raadsen SA, Dirks RPH. Deep transcriptome analysis of the heat shock response in an Atlantic sturgeon (Acipenser oxyrinchus) cell line. Fish & shellfish immunology. 2019;88:508–17. doi: 10.1016/j.fsi.2019.03.014 30862517.

22. Petersen TN, Brunak S, von Heijne G, Nielsen H. SignalP 4.0: discriminating signal peptides from transmembrane regions. Nature methods. 2011;8(10):785–6. doi: 10.1038/nmeth.1701 21959131.

23. Campanella JJ, Bitincka L, Smalley J. MatGAT: an application that generates similarity/identity matrices using protein or DNA sequences. BMC bioinformatics. 2003;4:29. doi: 10.1186/1471-2105-4-29 12854978; PubMed Central PMCID: PMC166169.

24. Kumar S, Stecher G, Tamura K. MEGA7: Molecular Evolutionary Genetics Analysis Version 7.0 for Bigger Datasets. Molecular biology and evolution. 2016;33(7):1870–4. doi: 10.1093/molbev/msw054 27004904.

25. Jones DT, Taylor WR, Thornton JM. The rapid generation of mutation data matrices from protein sequences. Computer applications in the biosciences: CABIOS. 1992;8(3):275–82. 1633570.

26. Nguyen NTT, Vincens P, Roest Crollius H, Louis A. Genomicus 2018: karyotype evolutionary trees and on-the-fly synteny computing. Nucleic acids research. 2018;46(D1):D816–D22. doi: 10.1093/nar/gkx1003 29087490; PubMed Central PMCID: PMC5753199.

27. Jansen HJ, Liem M, Jong-Raadsen SA, Dufour S, Weltzien FA, Swinkels W, et al. Rapid de novo assembly of the European eel genome from nanopore sequencing reads. Scientific reports. 2017;7(1):7213. doi: 10.1038/s41598-017-07650-6 28775309; PubMed Central PMCID: PMC5543108.

28. Henkel CV, Burgerhout E, de Wijze DL, Dirks RP, Minegishi Y, Jansen HJ, et al. Primitive duplicate Hox clusters in the European eel's genome. PloS one. 2012;7(2):e32231. doi: 10.1371/journal.pone.0032231 22384188; PubMed Central PMCID: PMC3286462.

29. Okajima Y, Nagasaki H, Suzuki C, Suga H, Ozaki N, Arima H, et al. Biochemical roles of the oligosaccharide chains in thyrostimulin, a heterodimeric hormone of glycoprotein hormone subunits alpha 2 (GPA2) and beta 5 (GPB5). Regulatory peptides. 2008;148(1–3):62–7. doi: 10.1016/j.regpep.2008.03.002 18433898.

30. Liao TH, Pierce JG. The primary structure of bovine thyrotropin. II. The amino acid sequences of the reduced, S-carboxymethyl alpha and beta chains. The Journal of biological chemistry. 1971;246(4):850–65. 5101174.

31. Liu WK, Nahm HS, Sweeney CM, Holcomb GN, Ward DN. The primary structure of ovine luteinizing hormone. II. The amino acid sequence of the reduced, S-carboxymethylated A-subunit (LH-). The Journal of biological chemistry. 1972;247(13):4365–81. 4556309.

32. Papkoff H, Sairam MR, Li CH. Amino acid sequence of the subunits of ovine pituitary interstitial cell-stimulating hormone. Journal of the American Chemical Society. 1971;93(6):1531–2. doi: 10.1021/ja00735a054 5102216.

33. Shome B, Parlow AF. Human follicle stimulating hormone: first proposal for the amino acid sequence of the hormone-specific, beta subunit (hFSHb). The Journal of clinical endocrinology and metabolism. 1974;39(1):203–5. doi: 10.1210/jcem-39-1-203 4835136.

34. Loosfelt H, Misrahi M, Atger M, Salesse R, Vu Hai-Luu Thi MT, Jolivet A, et al. Cloning and sequencing of porcine LH-hCG receptor cDNA: variants lacking transmembrane domain. Science. 1989;245(4917):525–8. doi: 10.1126/science.2502844 2502844.

35. McFarland KC, Sprengel R, Phillips HS, Kohler M, Rosemblit N, Nikolics K, et al. Lutropin-choriogonadotropin receptor: an unusual member of the G protein-coupled receptor family. Science. 1989;245(4917):494–9. doi: 10.1126/science.2502842 2502842.

36. Parmentier M, Libert F, Maenhaut C, Lefort A, Gerard C, Perret J, et al. Molecular cloning of the thyrotropin receptor. Science. 1989;246(4937):1620–2. doi: 10.1126/science.2556796 2556796.

37. Sprengel R, Braun T, Nikolics K, Segaloff DL, Seeburg PH. The testicular receptor for follicle stimulating hormone: structure and functional expression of cloned cDNA. Molecular endocrinology. 1990;4(4):525–30. doi: 10.1210/mend-4-4-525 2126341.

38. Swanson P, Dickey J.T., Campbell B. Biochemistry and physiology of fish gonadotropins. Fish Physiology and Biochemistry. 2003;28:53–9.

39. Wako H, Ishii S. Secondary structure prediction of beta-subunits of the gonadotropin-thyrotropin family from its aligned sequences using environment-dependent amino-acid substitution tables and conformational propensities. Biochimica et biophysica acta. 1995;1247(1):104–12. doi: 10.1016/0167-4838(94)00216-4 7873578.

40. Li MD, Ford JJ. A comprehensive evolutionary analysis based on nucleotide and amino acid sequences of the alpha- and beta-subunits of glycoprotein hormone gene family. The Journal of endocrinology. 1998;156(3):529–42. doi: 10.1677/joe.0.1560529 9582510.

41. Querat B, Sellouk A, Salmon C. Phylogenetic analysis of the vertebrate glycoprotein hormone family including new sequences of sturgeon (Acipenser baeri) beta subunits of the two gonadotropins and the thyroid-stimulating hormone. Biology of reproduction. 2000;63(1):222–8. doi: 10.1095/biolreprod63.1.222 10859263.

42. Sudo S, Kuwabara Y, Park JI, Hsu SY, Hsueh AJ. Heterodimeric fly glycoprotein hormone-alpha2 (GPA2) and glycoprotein hormone-beta5 (GPB5) activate fly leucine-rich repeat-containing G protein-coupled receptor-1 (DLGR1) and stimulation of human thyrotropin receptors by chimeric fly GPA2 and human GPB5. Endocrinology. 2005;146(8):3596–604. doi: 10.1210/en.2005-0317 15890769.

43. Maugars G, Dufour S, Cohen-Tannoudji J, Querat B. Multiple thyrotropin beta-subunit and thyrotropin receptor-related genes arose during vertebrate evolution. PloS one. 2014;9(11):e111361. doi: 10.1371/journal.pone.0111361 25386660; PubMed Central PMCID: PMC4227674.

44. Sacerdot C, Louis A, Bon C, Berthelot C, Roest Crollius H. Chromosome evolution at the origin of the ancestral vertebrate genome. Genome biology. 2018;19(1):166. doi: 10.1186/s13059-018-1559-1 30333059; PubMed Central PMCID: PMC6193309.

45. Smith JJ, Keinath MC. The sea lamprey meiotic map improves resolution of ancient vertebrate genome duplications. Genome research. 2015;25(8):1081–90. doi: 10.1101/gr.184135.114 26048246; PubMed Central PMCID: PMC4509993.

46. Smith JJ, Kuraku S, Holt C, Sauka-Spengler T, Jiang N, Campbell MS, et al. Sequencing of the sea lamprey (Petromyzon marinus) genome provides insights into vertebrate evolution. Nat Genet. 2013;45(4):415–21. Epub 2013/02/26. doi: ng.2568 [pii] doi: 10.1038/ng.2568 23435085.

47. Sower SA, Moriyama S, Kasahara M, Takahashi A, Nozaki M, Uchida K, et al. Identification of sea lamprey GTHbeta-like cDNA and its evolutionary implications. General and comparative endocrinology. 2006;148(1):22–32. Epub 2006/01/24. doi: 10.1016/j.ygcen.2005.11.009 16427051.

48. Uchida K, Moriyama S, Chiba H, Shimotani T, Honda K, Miki M, et al. Evolutionary origin of a functional gonadotropin in the pituitary of the most primitive vertebrate, hagfish. Proceedings of the National Academy of Sciences of the United States of America. 2010;107(36):15832–7. doi: 10.1073/pnas.1002208107 20733079; PubMed Central PMCID: PMC2936635.

49. Marquis TJ, Nozaki M, Fagerberg W, Sower SA. Comprehensive histological and immunological studies reveal a novel glycoprotein hormone and thyrostimulin expressing proto-glycotrope in the sea lamprey pituitary. Cell and tissue research. 2017;367(2):311–38. doi: 10.1007/s00441-016-2502-y 27771775.

50. Benton MJ. Vertebrate Palaeontology. 3rd ed. Oxford, UK: Blackwell Publishing; 2005. 455 p.

51. Wallis M. The molecular evolution of pituitary hormones. Biological reviews of the Cambridge Philosophical Society. 1975;50(1):35–98. 169922.

52. Vassart G, Pardo L, Costagliola S. A molecular dissection of the glycoprotein hormone receptors. Trends Biochem Sci. 2004;29(3):119–26. Epub 2004/03/09. doi: 10.1016/j.tibs.2004.01.006 S0968-0004(04)00023-4 [pii]. 15003269.

53. Roch GJ, Sherwood NM. Glycoprotein hormones and their receptors emerged at the origin of metazoans. Genome biology and evolution. 2014;6(6):1466–79. doi: 10.1093/gbe/evu118 24904013; PubMed Central PMCID: PMC4079206.

54. Wang P, Liu S, Yang Q, Liu Z, Zhang S. Functional Characterization of Thyrostimulin in Amphioxus Suggests an Ancestral Origin of the TH Signaling Pathway. Endocrinology. 2018;159(10):3536–48. doi: 10.1210/en.2018-00550 30192937.

55. Van Hiel MB, Vandersmissen HP, Van Loy T, Vanden Broeck J. An evolutionary comparison of leucine-rich repeat containing G protein-coupled receptors reveals a novel LGR subtype. Peptides. 2012;34(1):193–200. doi: 10.1016/j.peptides.2011.11.004 22100731.

56. Chauvigne F, Tingaud-Sequeira A, Agulleiro MJ, Calusinska M, Gomez A, Finn RN, et al. Functional and evolutionary analysis of flatfish gonadotropin receptors reveals cladal- and lineage-level divergence of the teleost glycoprotein receptor family. Biology of reproduction. 2010;82(6):1088–102. doi: 10.1095/biolreprod.109.082289 20200210.

57. Maugars G, Dufour S. Demonstration of the Coexistence of Duplicated LH Receptors in Teleosts, and Their Origin in Ancestral Actinopterygians. PloS one. 2015;10(8):e0135184. doi: 10.1371/journal.pone.0135184 26271038; PubMed Central PMCID: PMC4536197.

58. Caltabiano G, Campillo M, De Leener A, Smits G, Vassart G, Costagliola S, et al. The specificity of binding of glycoprotein hormones to their receptors. Cell Mol Life Sci. 2008;65(16):2484–92. Epub 2008/04/29. doi: 10.1007/s00018-008-8002-9 18438608.

59. Moyle WR, Campbell RK, Myers RV, Bernard MP, Han Y, Wang X. Co-evolution of ligand-receptor pairs. Nature. 1994;368(6468):251–5. doi: 10.1038/368251a0 8145825.

60. Karponis D, Ananth S. The role of thyrostimulin and its potential clinical significance. Endocrine regulations. 2017;51(2):117–28. doi: 10.1515/enr-2017-0012 28609287.

61. Szkudlinski MW, Fremont V, Ronin C, Weintraub BD. Thyroid-stimulating hormone and thyroid-stimulating hormone receptor structure-function relationships. Physiological reviews. 2002;82(2):473–502. doi: 10.1152/physrev.00031.2001 11917095.

62. Bruser A, Schulz A, Rothemund S, Ricken A, Calebiro D, Kleinau G, et al. The Activation Mechanism of Glycoprotein Hormone Receptors with Implications in the Cause and Therapy of Endocrine Diseases. The Journal of biological chemistry. 2016;291(2):508–20. doi: 10.1074/jbc.M115.701102 26582202; PubMed Central PMCID: PMC4705372.

63. Krause G, Kreuchwig A, Kleinau G. Extended and structurally supported insights into extracellular hormone binding, signal transduction and organization of the thyrotropin receptor. PloS one. 2012;7(12):e52920. doi: 10.1371/journal.pone.0052920 23300822; PubMed Central PMCID: PMC3531376.

64. Urizar E, Montanelli L, Loy T, Bonomi M, Swillens S, Gales C, et al. Glycoprotein hormone receptors: link between receptor homodimerization and negative cooperativity. The EMBO journal. 2005;24(11):1954–64. doi: 10.1038/sj.emboj.7600686 15889138; PubMed Central PMCID: PMC1142614.

65. Allen MD, Neumann S, Gershengorn MC. Occupancy of both sites on the thyrotropin (TSH) receptor dimer is necessary for phosphoinositide signaling. FASEB journal: official publication of the Federation of American Societies for Experimental Biology. 2011;25(10):3687–94. doi: 10.1096/fj.11-188961 21705666; PubMed Central PMCID: PMC3177577.

66. Tando Y, Kubokawa K. Expression of the gene for ancestral glycoprotein hormone beta subunit in the nerve cord of amphioxus. General and comparative endocrinology. 2009;162(3):329–39. doi: 10.1016/j.ygcen.2009.04.015 19393658.

67. Tando Y, Kubokawa K. A homolog of the vertebrate thyrostimulin glycoprotein hormone alpha subunit (GPA2) is expressed in Amphioxus neurons. Zoolog Sci. 2009;26(6):409–14. doi: 10.2108/zsj.26.409 19583500.

68. Cahoreau C, Klett D, Combarnous Y. Structure-function relationships of glycoprotein hormones and their subunits' ancestors. Frontiers in endocrinology. 2015;6:26. doi: 10.3389/fendo.2015.00026 25767463; PubMed Central PMCID: PMC4341566.

69. Nagasaki H, Wang Z, Jackson VR, Lin S, Nothacker HP, Civelli O. Differential expression of the thyrostimulin subunits, glycoprotein alpha2 and beta5 in the rat pituitary. Journal of molecular endocrinology. 2006;37(1):39–50. doi: 10.1677/jme.1.01932 16901922.

Synteny and phylogenetic analysis of paralogous thyrostimulin beta subunits (GpB5) in vertebrates

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