Emergence of an Ancestral Glycoprotein Hormone in the Pituitary of the Sea Lamprey, a Basal Vertebrate

Stacia A Sower; Wayne A Decatur; Krist N Hausken; Timothy J Marquis; Shannon L Barton; James Gargan; Mihael Freamat; Michael Wilmot; Lian Hollander; Jeffrey A Hall; Masumi Nozaki; Michal Shpilman; Berta Levavi-Sivan

doi:10.1210/en.2014-1797

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Emergence of an Ancestral Glycoprotein Hormone in the Pituitary of the Sea Lamprey, a Basal Vertebrate

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Emergence of an Ancestral Glycoprotein Hormone in the Pituitary of the Sea Lamprey, a Basal Vertebrate

Stacia A Sower, Wayne A Decatur, Krist N Hausken, Timothy J Marquis, Shannon L Barton, James Gargan, Mihael Freamat, Michael Wilmot, Lian Hollander, Jeffrey A Hall, …

Endocrinology (Philadelphia), Vol.156(8), pp.3026-3037

08/2015

DOI: https://doi.org/10.1210/en.2014-1797

PMID: 26066074

Abstract

Glycoproteins - genetics

Amino Acid Sequence

Pituitary Gland - metabolism

Vertebrates - genetics

Glycoproteins - metabolism

Molecular Sequence Data

Phylogeny

Peptide Hormones - genetics

Lampreys - genetics

Peptide Hormones - metabolism

Sequence Homology

Animals

Vertebrates - classification

Base Sequence

Cloning, Molecular

Pituitary Hormones - genetics

Pituitary Hormones - metabolism

Evolution, Molecular

The gnathostome (jawed vertebrates) classical pituitary glycoprotein hormones, FSH, LH, and TSH, consist of a common α-subunit (GpA1) and unique β-subunits (Gpβ1, -2, and -3), whereas a recently identified pituitary glycoprotein hormone, thyrostimulin, consists of GpA2 and GpB5. This paper reports the identification, expression, and function of an ancestral, nonclassical, pituitary heterodimeric glycoprotein hormone (GpH) consisting of the thyrostimulin A2 subunit with the classical β-subunit in the sea lamprey, Petromyzon marinus, a jawless basal vertebrate. Lamprey (l) GpA2, and lGpHβ were shown to form a heterodimer by coimmunoprecipitation of lGpA2 with FLAG-tagged lGpHβ after the overexpression in transiently transfected COS7 cells using a bipromoter vector. Dual-label fluorescent in situ hybridization and immunohistochemistry showed the coexpression of individual subunits in the proximal pars distalis of the pituitary. GnRH-III (1μΜ) significantly increased the expression of lGpHβ and lGpA2 in in vitro pituitary culture. Recombinant lamprey GpH was constructed by tethering the N terminal of lGpA2 to the C terminal of lGpHβ with a linker region composed of six histidine residues followed by three glycine-serine repeats. This recombinant lamprey GpH activated the lamprey glycoprotein hormone receptor I as measured by increased cAMP/luciferase activity. These data are the first to demonstrate a functional, unique glycoprotein heterodimer that is not found in any other vertebrate. These data suggest an intermediate stage of the structure-function of the gonadotropin/thyroid-stimulating hormone in a basal vertebrate, leading to the emergence of the highly specialized gonadotropin hormones and thyroid stimulating hormones in gnathostomes.

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Title: Emergence of an Ancestral Glycoprotein Hormone in the Pituitary of the Sea Lamprey, a Basal Vertebrate
Creators: Stacia A Sower - Center for Molecular and Comparative Endocrinology (C.A.S., W.A.D., K.N.H., T.J.M., S.L.B., J.G., M.F., M.W., J.A.H.), Department of Molecular, Cellular, and Biomedical Sciences, University of New Hampshire, Durham, New Hampshire 03824; Robert H. Smith Faculty of Agriculture, Food, and Environment (L.H., M.S., B.L.-S.), The Hebrew University of Jerusalem, Rehovot, Israel 76100; and Sado Marine Biological Station (M.N.), Niigata University, Tassha, Sado, Niigata 952-2135, Japan
Wayne A Decatur - Center for Molecular and Comparative Endocrinology (C.A.S., W.A.D., K.N.H., T.J.M., S.L.B., J.G., M.F., M.W., J.A.H.), Department of Molecular, Cellular, and Biomedical Sciences, University of New Hampshire, Durham, New Hampshire 03824; Robert H. Smith Faculty of Agriculture, Food, and Environment (L.H., M.S., B.L.-S.), The Hebrew University of Jerusalem, Rehovot, Israel 76100; and Sado Marine Biological Station (M.N.), Niigata University, Tassha, Sado, Niigata 952-2135, Japan
Krist N Hausken - Center for Molecular and Comparative Endocrinology (C.A.S., W.A.D., K.N.H., T.J.M., S.L.B., J.G., M.F., M.W., J.A.H.), Department of Molecular, Cellular, and Biomedical Sciences, University of New Hampshire, Durham, New Hampshire 03824; Robert H. Smith Faculty of Agriculture, Food, and Environment (L.H., M.S., B.L.-S.), The Hebrew University of Jerusalem, Rehovot, Israel 76100; and Sado Marine Biological Station (M.N.), Niigata University, Tassha, Sado, Niigata 952-2135, Japan
Timothy J Marquis - Center for Molecular and Comparative Endocrinology (C.A.S., W.A.D., K.N.H., T.J.M., S.L.B., J.G., M.F., M.W., J.A.H.), Department of Molecular, Cellular, and Biomedical Sciences, University of New Hampshire, Durham, New Hampshire 03824; Robert H. Smith Faculty of Agriculture, Food, and Environment (L.H., M.S., B.L.-S.), The Hebrew University of Jerusalem, Rehovot, Israel 76100; and Sado Marine Biological Station (M.N.), Niigata University, Tassha, Sado, Niigata 952-2135, Japan
Shannon L Barton - Center for Molecular and Comparative Endocrinology (C.A.S., W.A.D., K.N.H., T.J.M., S.L.B., J.G., M.F., M.W., J.A.H.), Department of Molecular, Cellular, and Biomedical Sciences, University of New Hampshire, Durham, New Hampshire 03824; Robert H. Smith Faculty of Agriculture, Food, and Environment (L.H., M.S., B.L.-S.), The Hebrew University of Jerusalem, Rehovot, Israel 76100; and Sado Marine Biological Station (M.N.), Niigata University, Tassha, Sado, Niigata 952-2135, Japan
James Gargan - Center for Molecular and Comparative Endocrinology (C.A.S., W.A.D., K.N.H., T.J.M., S.L.B., J.G., M.F., M.W., J.A.H.), Department of Molecular, Cellular, and Biomedical Sciences, University of New Hampshire, Durham, New Hampshire 03824; Robert H. Smith Faculty of Agriculture, Food, and Environment (L.H., M.S., B.L.-S.), The Hebrew University of Jerusalem, Rehovot, Israel 76100; and Sado Marine Biological Station (M.N.), Niigata University, Tassha, Sado, Niigata 952-2135, Japan
Mihael Freamat - Center for Molecular and Comparative Endocrinology (C.A.S., W.A.D., K.N.H., T.J.M., S.L.B., J.G., M.F., M.W., J.A.H.), Department of Molecular, Cellular, and Biomedical Sciences, University of New Hampshire, Durham, New Hampshire 03824; Robert H. Smith Faculty of Agriculture, Food, and Environment (L.H., M.S., B.L.-S.), The Hebrew University of Jerusalem, Rehovot, Israel 76100; and Sado Marine Biological Station (M.N.), Niigata University, Tassha, Sado, Niigata 952-2135, Japan
Michael Wilmot - Center for Molecular and Comparative Endocrinology (C.A.S., W.A.D., K.N.H., T.J.M., S.L.B., J.G., M.F., M.W., J.A.H.), Department of Molecular, Cellular, and Biomedical Sciences, University of New Hampshire, Durham, New Hampshire 03824; Robert H. Smith Faculty of Agriculture, Food, and Environment (L.H., M.S., B.L.-S.), The Hebrew University of Jerusalem, Rehovot, Israel 76100; and Sado Marine Biological Station (M.N.), Niigata University, Tassha, Sado, Niigata 952-2135, Japan
Lian Hollander - Center for Molecular and Comparative Endocrinology (C.A.S., W.A.D., K.N.H., T.J.M., S.L.B., J.G., M.F., M.W., J.A.H.), Department of Molecular, Cellular, and Biomedical Sciences, University of New Hampshire, Durham, New Hampshire 03824; Robert H. Smith Faculty of Agriculture, Food, and Environment (L.H., M.S., B.L.-S.), The Hebrew University of Jerusalem, Rehovot, Israel 76100; and Sado Marine Biological Station (M.N.), Niigata University, Tassha, Sado, Niigata 952-2135, Japan
Jeffrey A Hall - Center for Molecular and Comparative Endocrinology (C.A.S., W.A.D., K.N.H., T.J.M., S.L.B., J.G., M.F., M.W., J.A.H.), Department of Molecular, Cellular, and Biomedical Sciences, University of New Hampshire, Durham, New Hampshire 03824; Robert H. Smith Faculty of Agriculture, Food, and Environment (L.H., M.S., B.L.-S.), The Hebrew University of Jerusalem, Rehovot, Israel 76100; and Sado Marine Biological Station (M.N.), Niigata University, Tassha, Sado, Niigata 952-2135, Japan
Masumi Nozaki - Center for Molecular and Comparative Endocrinology (C.A.S., W.A.D., K.N.H., T.J.M., S.L.B., J.G., M.F., M.W., J.A.H.), Department of Molecular, Cellular, and Biomedical Sciences, University of New Hampshire, Durham, New Hampshire 03824; Robert H. Smith Faculty of Agriculture, Food, and Environment (L.H., M.S., B.L.-S.), The Hebrew University of Jerusalem, Rehovot, Israel 76100; and Sado Marine Biological Station (M.N.), Niigata University, Tassha, Sado, Niigata 952-2135, Japan
Michal Shpilman - Center for Molecular and Comparative Endocrinology (C.A.S., W.A.D., K.N.H., T.J.M., S.L.B., J.G., M.F., M.W., J.A.H.), Department of Molecular, Cellular, and Biomedical Sciences, University of New Hampshire, Durham, New Hampshire 03824; Robert H. Smith Faculty of Agriculture, Food, and Environment (L.H., M.S., B.L.-S.), The Hebrew University of Jerusalem, Rehovot, Israel 76100; and Sado Marine Biological Station (M.N.), Niigata University, Tassha, Sado, Niigata 952-2135, Japan
Berta Levavi-Sivan - Center for Molecular and Comparative Endocrinology (C.A.S., W.A.D., K.N.H., T.J.M., S.L.B., J.G., M.F., M.W., J.A.H.), Department of Molecular, Cellular, and Biomedical Sciences, University of New Hampshire, Durham, New Hampshire 03824; Robert H. Smith Faculty of Agriculture, Food, and Environment (L.H., M.S., B.L.-S.), The Hebrew University of Jerusalem, Rehovot, Israel 76100; and Sado Marine Biological Station (M.N.), Niigata University, Tassha, Sado, Niigata 952-2135, Japan
Publication Details: Endocrinology (Philadelphia), Vol.156(8), pp.3026-3037
Publisher: United States
Identifiers: 9923982375101921
Academic Unit: Department of Biology
Language: English
Resource Type: Journal article

Emergence of an Ancestral Glycoprotein Hormone in the Pituitary of the Sea Lamprey, a Basal Vertebrate

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