Conclusions And Prospects

Grow Taller 4 Idiots

How to Grow Taller

Get Instant Access

During the last two decades, the availability of molecular cloning techniques has helped establish the dual nature of the gonadotropic action also in fish. Yet, due to the variety of reproductive strategies found among fishes, the specific functions of the GtHs in general, and in particular those of the "newly discovered" member, the FSH, are still ambiguous. In salmonids (synchronous spawners), which represent a relatively simple reproductive model, the FSH is predominant during early oogenesis and is thought to promote sex steroid synthesis, follicu-lar differentiation, and gonadal growth. LH at a later phase induces steroido-genic changes that trigger the production of MIS, and consequently direct gamete maturation and spawning. Nevertheless, the role of FSH in multiple spawners is fairly blurred, largely because both GtHs: (i) appear to be present throughout the reproductive cycle; (ii) can stimulate the in vitro production of ovarian T and E2; and (iii) activate FSHR displayed on theca and granulosa cells during oogenesis. This ambiguity is further stressed in multiple spawners like the red sea bream, where LH seems to override FSH action all through the reproductive cycle.

Another puzzle relates to the changeable activity of the GtHs during the follicular development. GtHs support the synthesis of E2 during vitellogenesis, while at the time of maturation they support MIS synthesis. Considering that teleosts do not exhibit the classic follicular model of two-cell types for two-GtHs, it was suggested that binding of different ligands to the same receptor type may stimulate divergence signaling pathways with the result of altered cell functions. In this respect, altered cell functions could also be the outcome of a change in the relative abundance of the FSHR and LHR on the follicular cells. However, to verify these hypotheses further research should be conducted.

It is expected that the ongoing use of fish recombinant GtHs and GtH-Rs for function-structure studies, along with future establishment of transgenic "gain-of function"/ "loss of function" mutants of model fish species such as zebrafish and medaka, will help understanding the nature of GtH-GtHR interactions and their affect on follicular cell functions in fish.


The authors wish to thank Professor Zvi Yaron (Tel-Aviv University, Tel-Aviv, Israel) and Dr. Angelo Colorni (National Center for Mariculture, Eilat, Israel) for reviewing the manuscript.


Benninghoff, A.D., Thomas, P. Involvement of calcium and calmodulin in the regulation of ovarian steroidogenesis in Atlantic croaker (Micropogonias undulatus) and modulation by Aroclor 1254. Gen. Comp. Endocrinol. 144:211-223 (2005). Bobe, J., Maugars, G., Nguyen, T., Rime, H., Jalabert, B. Rainbow trout follicular maturational competence acquisition is associated with an increased expression of follicle stimulating hormone receptor and insulin-like growth factor 2 messenger RNAs. Mol. Reprod. Dev. 66:46-53 (2003). Bobe, J., Nguyen, T., Jalabert, B. Targeted gene expression profiling in the Rainbow trout (Oncorhynchus mykiss) ovary during maturational competence acquisition and oocyte maturation. Biol. Reprod. 71:73-82 (2004). Bogerd, J., Blomenrohr, M., Andersson, E., van der Putten, H.H., Tensen, C.P., Vischer, H.F., Granneman, J.C., Janssen-Dommerholt, C., Goos, H.J., Schulz, R.W. Discrepancy between molecular structure and ligand selectivity of a testicular follicle-stimulating hormone receptor of the African catfish (Clarias gariepinus). Biol. Reprod. 64:1633-1643 (2001). Bogerd, J., Granneman, J.C., Schulz, R.W., Vischer, H.F. Fish FSH receptors bind LH: How to make the human FSH receptor to be more fishy? Gen. Comp. Endocrinol. 142:34-43 (2005). Bogomolnaya, A., Yaron, Z. Stimulation in vitro of estradiol secretion by the ovary of a cichlid fish,

Sarotherodon Aureus. Gen. Comp. Endocrinol. 53:187-196 (1984). Boime, I., Ben-Menahem, D. Glycoprotein hormone structure-function and analog design. Recent

Prog. Horm. Res. 54:271-288 (1999). Bon, E., Breton, B., Govoroun, M., Menn, F. Effects of accelerated photoperiod regimes on the reproductive cycle of the female rainbow trout: II seasonal variations of plasma gonadotropins (GTH I and GTH II) levels correlated with ovarian follicle growth and egg size. Fish Physiol. Biochem. 20:143-154 (1999).

Braun, T., Schofield, P.R., Sprengel, R. Amino-terminal leucine-rich repeats in gonadotropin receptors determine hormone selectivity. EMBO. J. 10:1885-1890 (1991).

Breton, B., Govoroun, M., Mikolajczyk, T. GTH I and GTH II secretion profiles during the reproductive cycle in female rainbow trout: relationship with pituitary responsiveness to GnRH-A stimulation. Gen. Comp. Endocrinol. 111:38-50 (1998).

Campbell, R.K., Dean-Emig, D.M., Moyle, W.R. Conversion of human choriogonadotropin into a follitropin by protein engineering. Proc. Natl. Acad. Sci. USA 88:760-764 (1991).

Chyb, J., Mikolajczyk, T., Breton, B. Post-ovulatory secretion of pituitary gonadotropins GtH I and GtH II in the rainbow trout (Oncorhynchus mykiss): regulation by steroids and possible role of non-steroidal gonadal factors. J. Endocrinol. 163:87-97 (1999).

Cooke, B.A. Signal transduction involving cyclic AMP-dependent and cyclic AMP-independent mechanisms in the control of steroidogenesis. Mol. Cell. Endocrinol. 151:25-35 (1999).

Davies, B., Bromage, N., Swanson, P. The brain-pituitary-gonadal axis of female rainbow trout Oncorhynchus mykiss: Effects of photoperiod manipulation. Gen. Comp. Endocrinol. 115:155-166 (1999).

Dias, J.A., Zhang, Y., Liu, X. Receptor binding and functional properties of chimeric human follitropin prepared by an exchange between a small hydrophilic intercysteine loop of human follitropin and human lutropin. J. Biol. Chem. 269:25289-25294 (1994).

Dias J.A., Nechamen CA., Atari R. Identifying protein interactors in gonadotropin action. Endocrine. 26:241-247 (2005).

Dufau, M.L. The luteinizing hormone receptor. Annu. Rev. Physiol. 60:461-496 (1998).

Elizur, A., Zmora, N., Meiri, I., Kasuto, H., Rosenfeld, H., Chaouat, S., Kobayashi, M., Zohar, Y., Yaron, Y. Gonadotroins-from genes to recombinant proteins. In: Norberg, B., Kjesbu, O.S., Taranger, G.L., Andersson, E., Stefansson, S.O. (eds.), Proceedings of the 6th International Symposium on Reproductive Physiology of Fish. Fish Symposium 1999. The University of Bergen, Bergen, Norway, pp. 462-465 (2000).

Emanuele, N., Oslapas, R., Connick, E., Kirsteins, L., Lawrence, A.M. Hypothalamic LH may play a role in control of pituitary LH release. Neuroendocrinology 33:12-17 (1981).

Fan, Q.R., Hendrickson, W.A. Structural biology of glycoprotein hormones and their receptors. Endocrine 26:179-188 (2005).

Fontaine, Y.A., Salmon, C., Fontaine-Bertrand, E., Burzawa-Gerard, E., Donaldson, E.M. Comparison of the activities of two purified fish gonadotropins on adenyl cyclase activity in the goldfish ovary. Can. J. Zool. 50:1673-1676 (1972).

Fox, K.M., Dias, J.A., Van Roey, P. Three-dimensional structure of human follicle-stimulating hormone. Mol. Endocrinol. 15:378-389 (2001).

Ge, W. Intrafollicular paracrine communication in the zebrafish ovary: the state of the art of an emerging model for the study of vertebrate folliculogenesis. Mol. Cell. Endocrinol. 237:1-10 (2005).

Gen, K., Okuzawa, K., Senthilkumaran, B., Tanaka, H., Moriyama, S., Kagawa, H. Unique expression of gonadotropin-I and -II subunit genes in male and female red seabream (Pagrus major) during sexual maturation. Biol. Reprod. 63:308-319 (2000).

Gen, K., Yamaguchi, S., Okuzawa, K., Kumakura, N., Tanaka, H., Kagawa, H. Physiological roles of FSH and LH in red seabream, Pagrus major. Fish Physiol. Biochem. 28:77-80 (2003).

Goldsmith, P.C., McGregor, W.G., Raymoure, W.J., Kuhn, R.W., Jaffe, R.B. Cellular localization of chorionic gonadotropin in human fetal kidney and liver. J. Clin. Endocrinol. Metab. 57:654-661 (1983).

Gomez, J.M., Weil, C., Ollitrault, M., Le Bail, P.Y., Breton, B., Le Gac, F. Growth hormone (GH) and gonadotropin subunit gene expression and pituitary and plasma changes during sper-matogenesis and oogenesis in rainbow trout (Oncorhynchus mykiss). Gen. Comp. Endocrinol. 113:413-428 (1999).

Griswold, M.D., Heckert, L., Linder, C. The molecular biology of the FSH receptor. J. Steroid Biochem. Mol. Biol. 53:215-218 (1995).

Grossmann, M., Szkudlinski, M.W., Wong, R., Dias, J.A., Ji, T.H., Weintraub, B.D. Substitution of the seat-belt region of the thyroid-stimulating hormone (TSH) beta-subunit with the corresponding regions of choriogonadotropin or follitropin confers luteotropic but not follitropic activity to chimeric TSH. J. Biol. Chem. 272:15532-15540 (1997).

Gur, G., Melamed, P., Gissis, A., Yaron, Z. Changes along the pituitary-gonadal axis during maturation of the black carp, Mylopharyngodon piceus. J. Exp. Zool. 286:405-413 (2000).

Hai, M.V., De Roux, N., Ghinea, N., Beau, I., Loosfelt, H., Vannier, B., Meduri, G., Misrahi, M., Milgrom, E. Gonadotropin receptors. Ann. Endocrinol. (Paris), 60:89-92 (1999).

Hall, R.A., Lefkowitz, R.J. Regulation of G protein-coupled receptor signaling by scaffold proteins. Circ. Res. 91:672-680 (2002).

Hassin, S., Holland, M.C.H., Zohar, Y. Ontogeny of follicle-stimulating hormone and luteinizing hormone gene expression during pubertal development in the female striped bass, Morone saxatilis (Teleostei). Biol. Reprod. 61:1608-1615 (1999).

Hillier, S.G. Gonadotropic control of ovarian follicular growth and development. Mol. Cell. Endocrinol. 179:39-46 (2001).

Hirai, T., Oba, Y., Yao, Z.X., Cang, X.T., Yoshiura, Y., Kobayashi, T., Nagahama, Y. Putative gonadotropin receptors in tilapia (Oreochromis niloicus) gonads: cDNA cloning and expression during oogenesis. In: Norberg, B., Kjesbu, O.S., Taranger, G.L., Andersson, E., Stefansson, S.O. (eds.), Proceedings of the 6th International Symposium on Reproductive Physiology of Fish. Fish Symposium 1999. The University of Bergen, Bergen, Norway, p. 201 (2000).

Hirai, T., Shibata, Y., Matsuda, M., Yoshikuni, M., Nagahama, Y. Glycoprotein hormone receptor family in medaka (Oryzias latipes). Fish Physiol. Biochem. 28:345-346 (2003).

Hsueh, A.J., McGee, E.A., Hayashi, M., Hsu, S.Y. Hormonal regulation of early follicle development in the rat ovary. Mol. Cell. Endocrinol. 163:95-100 (2000).

Idler, D.R., Hwang, S.J., Bazar, L.S. Fish gonadotropin(s). I. Bioassay of salmon gonadotropin(s) in vitro with immature trout gonads. Endocr. Res. Commun. 2:199-213 (1975).

Iwasawa, A., Hattori, M., Fukuhara, Y., Kawashima, M., Wakabayashi, K., Kamiyoshi, M. Chicken lutropin acts like follitropin in rat ovarian follitropin receptor: an isoelectric focusing study. Comp. Biochem. Physiol. C, Pharmacol. Toxicol. Endocrinol. 120:83-89 (1998).

Jackson, K., Goldberg, D., Ofir, M., Abraham, M., Degani, G. Blue gourami (Trichogaster trichopterus) gonadotropic P subunits (I and II) cDNA sequences and expression during oogenesis. J. Mol. Endocrinol. 23:177-187 (1999).

Jalabert, B. Particularities of reproduction and oogenesis in teleost fish compared to mammals. Reprod. Nutr. Dev. 45:261-279 (2005).

Ji, I., Ji, T.H. Exons 1-10 of the rat LH receptor encode a high affinity hormone binding site and exon 11 encodes G-protein modulation and a potential second hormone binding site. Endocrinology 128:2648-2650 (1991).

Kagawa, H., Tanaka, H., Okuzawa, K., Hirose, K. Development of maturational competence of oocytes of red seabream, Pagrus-Major, after human chorionic-gonadotropin treatment in vitro requires Rna and protein-synthesis. Gen. Comp. Endocrinol. 94:199-206 (1994).

Kagawa, H., Kawazoe, I., Tanaka, H., Okuzawa, K. Immunocytochemical identification of two distinct gonadotropic cells (GTH I and GTH II) in the pituitary of bluefin tuna, Thunnus thynnus. Gen. Comp. Endocrinol. 110:11-18 (1998a).

Kagawa, H., Tanaka, H., Okuzawa, K., Kobayashi, M. GTH II but not GTH I induces final maturation and the development of maturational competence of oocytes of red seabream in vitro. Gen. Comp. Endocrinol. 112:80-88 (1998b).

Kagawa, H., Gen, K., Okuzawa, K., Tanaka, H. Effects of luteinizing hormone and follicle-stimulating hormone and insulin-like growth factor-I on aromatase activity and P450 aromatase gene expression in the ovarian follicles of red seabream, Pagrus major. Biol. Reprod. 68:1562-1568 (2003).

Kajimura, S., Yoshiura, Y., Suzuki, M., Aida, K. cDNA cloning of two gonadotropin beta subunits (GTH-I beta and -II beta) and their expression profiles during gametogenesis in the Japanese flounder (Paralichthys olivaceus). Gen. Comp. Endocrinol. 122:117-129 (2001).

Kanamori, A., Nagahama, Y. Involvement of 3',5'-cyclic adenosine monophosphat in the control of follicular steroidogenesis of the amago salmon. Gen. Comp. Endocrinol. 72:39-53 (1988).

Kawauchi, H., Suzuki, K., Itoh, H., Swanson, P., Naito, N., Nagahama, Y., Nozaki, M., Nakai, Y., Itoh, S. The duality of teleost gonadotropins. Fish Physiol. Biochem. 7:29-38 (1989).

Kim, D.J., Cho, Y.C., Sohn, Y.C. Molecular characterization of rockfish (Sebastes schlegeli) gonadotropin subunits and their mRNA expression profiles during oogenesis. Gen. Comp. Endocrinol. 141:282-290 (2005).

Kraulis, P.J. MOLSCRIPT: a program to produce both detailed and schematic plots of protein structures. J. Appl. Crystallogr. 24:946-950 (1991).

Kubokawa, K., Ishii, S. Receptors for native gonadotropins in amphibian liver. Gen. Comp. Endocrinol. 68:260-270 (1987).

Kumar, R.S., Trant, J.M. Piscine glycoprotein hormone (gonadotropin and thyrotropin) receptors: a review of recent developments. Comp. Biochem. Physiol. B, Biochem. Mol. Biol. 129:347-355 (2001).

Kumar, R.S., Ijiri, S., Kight, K., Swanson, P., Dittman, A., Alok, D., Zohar, Y., Trant, J.M. Cloning and functional expression of a thyrotropin receptor from the gonads of a vertebrate (bony fish): potential thyroid- independent role for thyrotropin in reproduction. Mol. Cell. Endocrinol. 167:1-9 (2000).

Kumar, R.S., Ijiri, S., Trant, J.M. Molecular biology of the channel catfish gonadotropin receptors: 2. Complementary DNA cloning, functional expression, and seasonal gene expression of the follicle-stimulating hormone receptor. Biol. Reprod. 65:710-717 (2001).

Kwok, H.F., So, W.K., Wang, Y., Ge, W. Zebrafish gonadotropins and their receptors: I. Cloning and characterization of zebrafish follicle-stimulating hormone and luteinizing hormone receptors-evidence for their distinct functions in follicle development. Biol. Reprod. 72:1370-1381 (2005).

Laan, M., Richmond, H., He, C.M., Campbell, R.K. Zebrafish as a model for vertebrate reproduction: Characterization of the first functional zebrafish (Danio rerio) gonadotropin receptor. Gen. Comp. Endocrinol. 125:349-364 (2002).

Lapthorn, A.J., Harris, D.C., Littlejohn, A., Lustbader, J.W., Canfield, R.E., Machin, K.J., Morgan, F.J., Isaacs, N.W. Crystal structure of human chorionic gonadotropin. Nature 369:455-461 (1994).

Li, M.D., Ford, J.J. A comprehensive evolutionary analysis based on nucleotide and amino acid sequences of the a- and P-subunits of glycoprotein hormone gene family. J. Endocrinol. 156:529-542 (1998).

Licht, P., Gallo, A.B., Aggarwal, B.B., Farmer, S.W., Castelino, J.B., Papkoff, H. Biological and binding activities of equine pituitary gonadotrophins and pregnant mare serum gonadotrophin. J. Endocrinol. 83:311-322 (1979).

Lin, Y.W., Petrino, T.R., Wallace, R.A. Fundulus heteroclitus gonadotropins.5: small scale chro-matographic fractionation of pituitary extracts into components with different steroidogenic activities using homologous bioassays. Reprod. Biol. Endocrinol. 2:14 (2004).

Markkula, M., Hamalainen, T., Loune, E., Huhtaniemi, I. The follicle-stimulating hormone (FSH) beta- and common alpha-subunits are expressed in mouse testis, as determined in wild-type mice and those transgenic for the FSH beta-subunit/herpes simplex virus thymidine kinase fusion gene. Endocrinology 136:4769-4775 (1995).

Markkula, M., Kananen, K., Klemi, P., Huhtaniemi, I. Pituitary and ovarian expression of the endogenous follicle-stimulating hormone (FSH) subunit genes and an FSH beta-subunit promoter-driven herpes simplex virus thymidine kinase gene in transgenic mice; specific partial ablation of FSH-producing cells by antiherpes treatment. J. Endocrinol. 150:265-273 (1996).

Mateos, J., Mananos, E., Martinez-Rodriguez, G., Carrillo, M., Querat, B., Zanuy, S. Molecular characterization of sea bass gonadotropin subunits (alpha, FSH beta, and LH beta) and their expression during the reproductive cycle. Gen. Comp. Endocrinol. 133:216-232 (2003).

Matzuk, M.M., Kumar, T.R., Shou, W.N., Coerver, K.A., Lau, A.L., Behringer, R.R., Finegold, M.J. Transgenic models to study the roles of inhibins and activins in reproduction, oncogenesis, and development. Recent Prog. Horm. Res. 51:123-157 (1996).

Matzuk, M.M., Boime, I. The role of the asparagine-linked oligosaccharides of the alpha subunit in the secretion and assembly of human chorionic gonadotrophin. J. Cell. Biol. 106:1049-1059 (1988a).

Matzuk, M.M., Boime, I. Site-specific mutagenesis defines the intracellular role of the asparagine-linked oligosaccharides of chorionic gonadotropin beta subunit. J. Biol. Chem. 263:17106-17111 (1988b).

Matzuk, M.M., Boime, I. Mutagenesis and gene transfer define site-specific roles of the gonadotropin oligosaccharides. Biol. Reprod. 40:48-53 (1989).

Matzuk, M.M., Burns, K.H., Viveiros, M.M., Eppig, J.J. Intercellular communication in the mammalian ovary: oocytes carry the conversation. Science 296:2178-2180 (2002).

Meiri, I., Zmora, N., Elizur, A. Functional expression of recombinant seabream FSH and LH in bac-ulovirus infected insect cells. In: Norberg, B., Kjesbu, O.S., Taranger, G.L., Andersson, E., Stefansson, S.O. (eds.), Proceedings of the 6th International Symposium on Reproductive Physiology of Fish. Fish Symposium 1999. The University of Bergen, Bergen, Norway, p. 488 (2000).

Meiri, I., Knibb, W.R., Zohar, Y., Elizur, A. Temporal profile of P follicle-stimulating hormone, P luteinizing hormone, and growth hormone gene expression in the protandrous hermaphrodite, giltheadseabream, Sparus aurata. Gen. Comp. Endocrinol. 137:288-299 (2004).

Melamed, P., Gur, G., Elizur, A., Rosenfeld, H., Sivan, B., Rentier Delrue, F., Yaron, Z. Differential effects of gonadotropin-releasing hormone, dopamine and somatostatin and their second messengers on the mRNA levels of gonadotropin II beta subunit and growth hormone in the teleost fish, tilapia. Neuroendocrinology 64:320-328 (1996).

Melamed, P., Gur, G., Rosenfeld, H., Elizur, A., Yaron, Z. The mRNA levels of GtH I beta, GtH II beta and GH in relation to testicular development and testosterone treatment in pituitary cells of male tilapia. Fish Physiol. Biochem.17:93-98 (1997).

Melamed, P., Rosenfeld, H., Elizur, A., Yaron, Z. Endocrine regulation of gonadotropin and growth hormone gene transcription in fish. Comp. Biochem. Physiol. C, Pharmacol. Toxicol. Endocrinol. 119:325-338 (1998).

Mercure, F., Van der Kraak, G. Mechanisms of action of free arachidonic acid on ovarian steroid production in the goldfish. Gen. Comp. Endocrinol. 102:130-140 (1996).

Milgrom, E., de Roux, N., Ghinea, N., Beau, I., Loosfelt, H., Vannier, B., Savouret, J.F., Misrahi, M. Gonadotrophin and thyrotrophin receptors. Horm. Res. 48 Suppl. 4:33-37 (1997).

Miwa, S., Yan, L.G., Swanson, P. Localization of two gonadotropin receptors in the salmon gonad by in vitro ligand autoradiography. Biol. Reprod. 50:629-642 (1994).

Montserrat, N., Gonzalez, A., Mendez, E., Piferrer, F., Planas, J.V. Effects of follicle stimulating hormone on estradiol-17 beta production and P-450 aromatase (CYP19) activity and mRNA expression in brown trout vitellogenic ovarian follicles in vitro. Gen. Comp. Endocrinol. 137:123-131 (2004).

Moyle, W.R., Campbell, R.K., Myers, R.V., Bernard, M.P., Han, Y., Wang, X. Co-evolution of ligand-receptor pairs. Nature 368:251-255 (1994).

Moyle, W.R., Xing, Y., Lin, W., Cao, D., Myers, R.V., Kerrigan, J.E., Bernard, M.P. Model of glycoprotein hormone receptor ligand binding and signaling. J. Biol. Chem. 279:44442-44459 (2004).

Moyle, W.R., Lin, W., Myers, R.V., Cao, D., Kerrigan, J.E., Bernard, M.P. Models of glycoprotein hormone receptor interaction. Endocrine 26:189-205 (2005).

Nagahama, Y. Endocrine Regulation of Gametogenesis in Fish. Int. J. Dev. Biol. 38:217-229 (1994).

Nagahama,Y., Kagawa, H., Adachi, S., Young, G. Stimulation of 17a,203-dihydroxy-4-pregnen-3-one production in the granulosa cells of amago salmon, Oncorhynchus rhodurus, by cyclic nucleotides. J. Exp. Zool. 236:371-375 (1984).

Nagahama, Y., Matsuhisa, A., Iwamatsu, T., Sakai, N., Fukada, S. A Mechanism for the Action of Pregnant Mare Serum Gonadotropin on Aromatase-Activity in the Ovarian Follicle of the Medaka, Oryzias-Latipes. J. Exp. Zool. 259:53-58 (1991).

Nagahama, Y., Yoshikuni, M., Yamashita, M., Tanaka, M. Regulation of oocyte maturation in fish. In: Sherwood, N.M., Hew, C.L. (eds.), Molecular Endocrinology of Fish, Fish Physiology, Vol. XIII. Academic Press, New York, pp. 393-439 (1994).

Naito, N., Hyodo, S., Okumoto, N., Urano, A., Nakai, Y. Differential production and regulation of gonadotropins (GtH-I and GtH-II) in the pituitary-gland of Rainbow-trout, Oncorhynchus Mykiss, during ovarian development. Cell Tissue Res. 266:457-467 (1991).

Nozaki, M., Naito, N., Swanson, P., Miyata, K., Nakai, Y., Oota, Y., Suzuki, K., Kawauchi, H. Salmonid pituitary gonadotrophs.1. distinct cellular-distributions of two gonadotropins, GtH-I and GtH-II. Gen. Comp. Endocrinol. 77:348-357 (1990).

Oba, Y., Hirai, T., Yoshiura, Y., Yoshikuni, M., Kawauchi, H., Nagahama, Y. Cloning, functional characterization, and expression of a gonadotropin receptor cDNA in the ovary and testis of amago salmon (Oncorhynchus rhodurus). Biochem. Biophys. Res. Commun. 263:584-590 (1999a).

Oba, Y., Hirai, T., Yoshiura, Y., Yoshikuni, M., Kawauchi, H., Nagahama, Y. The duality of fish gonadotropin receptors: cloning and functional characterization of a second gonadotropin receptor cDNA expressed in the ovary and testis of amago salmon (Oncorhynchus rhodurus). Biochem. Biophys. Res. Commun. 265:366-371 (1999b).

Oba, Y., Hirai, T., Yoshiura, Y., Kobayashi, T., Nagahama, Y. Fish gonadotropin and thyrotropin receptors: the evolution of glycoprotein hormone receptors in vertebrates. Comp. Biochem. Physiol. B, Biochem. Mol. Biol. 129:441-448 (2001).

Okada, T., Kawazoe, I., Kimura, S., Sasamoto, Y., Aida, K., Kawauchi, H. Purification and characterization of gonadotropin-I and gonadotropin-II from pituitary-glands of Tuna (Thunnus Obesus). Int. Pept. Prot. Res. 43:69-80 (1994).

Pabon, J.E., Bird, J.S., Li, X., Huang, Z.H., Lei, Z.M., Sanfilippo, J.S., Yussman, M.A., Rao, C.V Human skin contains luteinizing hormone/chorionic gonadotropin receptors. J. Clin. Endocrinol. Metab. 81:2738-2741 (1996).

Pang, Y., Ge, W. Activin stimulation of Zebrafish oocyte maturation in vitro and its potential role in mediating gonadotropin-induced oocyte maturation. Biol. Reprod. 61:987-992 (1999).

Pang, Y.F., Ge, W. Gonadotropin and activin enhance maturational competence of oocytes in the zebrafish (Danio rerio). Biol. Reprod. 66:259-265 (2002).

Parhar, I.S., Ogawa, S., Hamada, T., Sakuma, Y. Single-cell real-time quantitative polymerase chain reaction of immunofluorescently identified neurons of gonadotropin-releasing hormone subtypes in cichlid fish. Endocrinology 144:3297-3300 (2003a).

Parhar, I.S., Soga, T., Ogawa, S., Sakuma, Y. FSH and LH-beta subunits in the preoptic nucleus: ontogenic expression in teleost. Gen. Comp. Endocrinol. 132:369-378 (2003b).

Park, J.I., Semyonov, J., Chang, C.L., Hsu, S.Y. Conservation of the heterodimeric glycoprotein hormone subunit family proteins and the LGR signaling system from nematodes to humans. Endocrine 26:267-276 (2005).

Patino, R., Yoshizaki, G., Bolamba, D., Thomas, P. Role of arachidonic acid and protein kinase c during maturation-inducing hormone-dependent meiotic resumption and ovulation in ovarian follicles of Atlantic croaker. Biol. Reprod. 68:516-523 (2003).

Planas, J.V., Swanson, P. Maturation-associated changes in the response of the salmon testis to the steroidogenic actions of gonadotropins (GTH I and GTH II) in vitro. Biol. Reprod. 52:697-704 (1995).

Planas, J.V., Swanson, P., Dickhoff, W.W. Regulation of testicular steroid production in vitro by gonadotropins (GTH I and GTH II) and cyclic AMP in coho salmon (Oncorhynchus kisutch). Gen. Comp. Endocrinol. 91:8-24 (1993).

Planas, J.V., Goetz, F.W., Swanson, P. Stimulation of brook trout ovarian steroidogenesis by gonadotropins I and II is mediated by the cyclic adenosine 3',5'-monophosphate/protein kinase A pathway. Biol. Reprod. 57:647-654 (1997).

Planas, J.V., Athos, J., Goetz, F.W., Swanson, P. Regulation of ovarian steroidogenesis in vitro by follicle-stimulating hormone and luteinizing hormone during sexual maturation in salmonid fish. Biol. Reprod. 62:1262-1269 (2000).

Prat, F., Sumpter, J.P., Tyler, C.R. Validation of radioimmunoassays for two salmon gonadotropins (GTH I and GTH II) and their plasma concentrations throughout the reproductive cycle in male and female rainbow trout (Oncorhynchus mykiss). Biol. Reprod. 54:1375-1382 (1996).

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. Biol. Reprod. 63:222-228 (2000).

Querat, B., Tonnerre-Doncarli, C., Genies, F., Salmon, C. Duality of gonadotropins in gnathostomes. Gen. Comp. Endocrinol. 124:308-314 (2001).

Querat, B., Arai, Y., Henry, A., Akama, Y., Longhurst, T.J., Joss, J.M.P. Pituitary glycoprotein hormone ß subunits in the Australian lungfish and estimation of the relative evolution rate of these subunits within vertebrates. Biol. Reprod. 70:356-363 (2004).

Rao Ch, V., Zhou, X.L., Lei, Z.M. Functional luteinizing hormone/chorionic gonadotropin receptors in human adrenal cortical H295R cells. Biol. Reprod. 71:579-587 (2004).

Rastogi, S., Liberles, D.A. Subfunctionalization of duplicated genes as a transition state to neofunctionalization. BMC Evol. Biol. 5:28 (2005).

Remy, J.J., Couture, L., Pantel, J., Haertle, T., Rabesona, H., Bozon, V., Pajot-Augy, E., Robert, P., Troalen, F., Salesse, R., Bidart, J.M. Mapping of HCG-receptor complexes. Mol. Cell. Endocrinol. 125:79-91 (1996).

Rocha, A., Gómez, M., Carrillo, M. Cloning of a gonadal luteinizing hormone receptor cDNA from the European sea bass, Dicentrarchus labrax. In: Proceeding of the 5th International Symposium on Fish Endocrinology. Castellón, Spain, September 5-9. No. P69 (2004).

Salmon, C., Marchelidon, J., Fontaine-Bertrand, E., Fontaine, Y.A. Human chorionic gonadotrophin and immature fish ovary: characterization and mechanism of the in vitro stimulation of cyclic adenosine monophosphate accumulation. Gen. Comp. Endocrinol. 58:101-108 (1985).

Santos, E.M., Rand-Weaver, M., Tyler, C.R. Follicle-stimulating hormone and its alpha and beta subunits in rainbow trout (Oncorhynchus mykiss): purification, characterization, development of specific radioimmunoassays, and their seasonal plasma and pituitary concentrations in females. Biol. Reprod. 65:288-294 (2001).

Schulz, R.W., Zandbergen, M.A., Peute, J., Bogerd, J., vanDijk, W., Goos, H.J.T. Pituitary gonadotrophs are strongly activated at the beginning of spermatogenesis in African catfish, Clarias gariepinus. Biol. Reprod. 57:139-147 (1997).

Selman, K., Petrino, T.R., Wallace, R. Experimental conditions for oocyte maturation in the zebrafish, Brachydanio rerio. J. Exp. Zool. 269:538-550 (1994).

Simoni, M., Gromoll, J., Nieschlag, E. The follicle-stimulating hormone receptor: biochemistry, molecular biology, physiology, and pathophysiology. Endocr. Rev. 18:739-773 (1997).

So, W.K., Kwok, H.F., Ge, W. Zebrafish gonadotropins and their receptors: II. Cloning and characterization of zebrafish follicle-stimulating hormone and luteinizing hormone subunits-their spatial-temporal expression patterns and receptor specificity. Biol. Reprod. 72:1382-1396 (2005).

Sohn, Y.C., Yoshiura, Y., Suetake, H., Kobayashi, M., Aida, K. Nucleotide sequence of gonadotropin II beta subunit gene in goldfish. Fish. Sci. 65:800-801 (1999).

Sorbera, L.A., Asturiano, J.F., Carrillo, M., Zanuy, S. Effects of polyunsaturated fatty acids and prostaglandins on oocyte maturation in a marine teleost, the European sea bass (Dicentrarchus labrax). Biol. Reprod. 64:382-389 (2001).

Srivastava, R.K., Van der Kraak, G. Effects of activators of different intracellular signaling pathways on steroid production by goldfish vitellogenic ovarian follicles. Gen. Comp. Endocrinol. 93:181-191 (1994).

Suzuki, K., Nagahama, Y., Kawauchi, H. Steroidogenic activities of two distinct salmon gonadotropins. Gen. Comp. Endocrinol. 71:452-458 (1988).

Swanson, P., Dittman, A. Pituitary gonadotropins and their receptors in fish. In: Kawashima, S., Kikuyama, S. (eds.), Advances in Comparative Endocrinology. Monduzzi Editore, Bologna, Italy, pp. 841-846 (1997).

Swanson, P., Bernard, M., Suzuki, K., Kawauchi, H., Dickhoff, W.W. Gonadotropins I and II in juvenile coho salmon. Fish Physiol. Biochem. 7:169-176 (1989).

Swanson, P., Suzuki, K., Kawauchi, H., Dickhoff, W.W. Isolation and Characterization of 2 Coho Salmon Gonadotropins, Gth-I and Gth-II. Biol. Reprod. 44:29-38 (1991).

Swanson, P., Dickey, J.T., Campbell, B. Biochemistry and physiology of fish gonadotropins. Fish Physiol. Biochem. 28:53-59 (2003).

Tan, J.D., Adachi, S., Nagahama, Y. The in vitro effects of cyclic nucleotides, cyanoketone, and cycloheximide on the production of estradiol-17 beta by vitellogenic ovarian follicles of goldfish (Carassius auratus). Gen. Comp. Endocrinol. 63:110-116 (1986).

Tanaka, H., Kagawa, H., Hirose, K. Steroidogenic activities of two distinct gonadotropins in red seabream, Pagrus major. In: Goetz, F.W., Thomas, P., (eds.), Proceedings of the 5th International Symposium on the Reproductive Physiology of Fish. University of Texas, Austin, TX, pp 10-12 (1995).

Tena-Sempere, M., Zhang, F.P., Huhtaniemi, I. Persistent expression of a truncated form of the luteinizing hormone receptor messenger ribonucleic acid in the rat testis after selective Leydig cell destruction by ethylene dimethane sulfonate. Endocrinology 135:1018-1024 (1994).

Thomas, P., Pinter, J., Das, S. Upregulation of the maturation-inducing steroid membrane receptor in spotted seatrout ovaries by gonadotropin during oocyte maturation and its physiological significance. Biol. Reprod. 64:21-29 (2001).

Tilly, J.L., LaPolt, P.S., Hsueh, A.J. Hormonal regulation of follicle-stimulating hormone receptor messenger ribonucleic acid levels in cultured rat granulosa cells. Endocrinology 130:1296-1302 (1992).

Tyler, C.R., Sumpter, J.P., Kawauchi, H., Swanson, P. Involvement of gonadotropin in the uptake of vitellogenin into vitellogenic oocytes of the rainbow trout, Oncorhynchus mykiss. Gen. Comp. Endocrinol. 84:291-299 (1991).

Tyler, C.R., Pottinger, T.C., Coward, K., Prat, F., Beresford, N., Maddix, S. Salmonid follicle-stimulating hormone (GtH I) mediates vitellogenic development of oocytes in the rainbow trout, Oncorhynchus mykiss. Biol. Reprod. 57:1238-1244 (1997).

Ulloa-Aguirre, A., Maldonado, A., Damian-Matsumura, P., Timossi, C. Endocrine regulation of gonadotropin glycosylation. Arch. Med. Res. 32:520-532 (2001).

Van der Kraak, G. Role of calcium in the control of steroidogenesis in preovulatory ovarian follicles of the goldfish. Gen. Comp. Endocrinol. 81:268-275 (1991).

Van der Kraak, G. Mechanisms by which calcium ionophore and phorbol ester modulate steroid production by goldfish preovulatory ovarian follicles. J. Exp. Zool. 262:271-278 (1992).

Van der Kraak, G., Chang, J.P. Arachidonic acid stimulates steroidogenesis in goldfish preovulatory ovarian follicles. Gen. Comp. Endocrinol. 77:221-228 (1990).

Van der Kraak, G., Jacobson, P.M. Regulation of steroid production by goldfish ovarian follicles: interaction of GtH I and GtH II with calcium ionophore and phorbol ester. In: Scott, A.P., Sumpter, J.P., Kime, D.E., Rolfe, M.S (eds.), Reproductive Physiology of Fish: Fish Symposium 91. Sheffield, UK, pp. 215-217 (1991).

Van der Kraak, G., Wade, M.G. A comparison of signal transduction pathways mediating gonadotropin actions in vertebrates. In: Davey, K.G., Peter, R.E., Tobe, S.S. (eds.), Perspectives in Comparative Endocrinology. National Research Council of Canada, Toronto, Canada, pp. 59-63 (1994).

Van der Kraak, G., Suzuki, K., Peter, R.E., Itoh, H., Kawauchi, H. Properties of common carp gonadotropin I and gonadotropin II. Gen. Comp. Endocrinol. 85:217-229 (1992).

Vischer, H.F., Bogerd, J. Cloning and functional characterization of a gonadal luteinizing hormone receptor complementary DNA from the African catfish (Clarias gariepinus). Biol. Reprod. 68:262-271 (2003).

Vischer, H.F., Teves, A.C.C., Ackermans, J.C.M., van Dijk, W., Schulz, R.W., Bogerd, J. Cloning and spatiotemporal expression of the follicle-stimulating hormone beta subunit complementary DNA in the African catfish (Clarias gariepinus). Biol. Reprod. 68:1324-1332 (2003a).

Vischer, H.F., Granneman, J.C.M., Linskens, M.H.K., Schulz, R.W., Bogerd, J. Both recombinant African catfish LH and FSH are able to activate the African catfish FSH receptor. J. Mol. Endocrinol. 31:133-140 (2003b).

Vischer, H.F., Granneman, J.C., Bogerd, J. Opposite contribution of two ligand-selective determinants in the N-terminal hormone-binding exodomain of human gonadotropin receptors. Mol. Endocrinol. 17:1972-1981 (2003c).

Vischer, H.F., Granneman, J.C., Noordam, M.J., Mosselman, S., Bogerd, J. Ligand selectivity of gonadotropin receptors. Role of the beta-strands of extracellular leucine-rich repeats 3 and 6 of the human luteinizing hormone receptor. J. Biol. Chem. 278:15505-15513 (2003d).

Vischer, H.F., Marques, R.B., Granneman, J.C., Linskens, M.H., Schulz, R.W., Bogerd, J. Receptor-selective determinants in catfish gonadotropin seat-belt loops. Mol. Cell. Endocrinol. 224:55-63 (2004).

Wallis, M. The molecular evolution of vertebrate growth hormones: a pattern of near-stasis interrupted by sustained bursts of rapid change. J. Mol. Evol. 43:93-100 (1996).

Wallis, M. Episodic evolution of protein hormones: molecular evolution of pituitary prolactin. J. Mol. Evol. 50:465-473 (2000).

Wallis, M. Episodic evolution of protein hormones in mammals. J. Mol. Evol. 53:10-18 (2001).

Wang, Y., Ge, W. Gonadotropin regulation of follistatin expression in the cultured ovarian follicle cells of zebrafish, Danio rerio. Gen. Comp. Endocrinol. 134:308-315 (2003a).

Wang, Y., Ge, W. Involvement of cyclic adenosine 3',5'-monophosphate in the differential regulation of activin betaA and betaB expression by gonadotropin in the zebrafish ovarian follicle cells. Endocrinology 144:491-499 (2003b).

Wang, Y., Ge, W. Spatial expression patterns of activin and its signaling system in the zebrafish ovarian follicle: evidence for paracrine action of activin on the oocytes. Biol. Reprod. 69:1998-2006 (2003c).

Wang, Y., Ge, W. Cloning of epidermal growth factor (EGF) and EGF receptor from the zebrafish ovary: evidence for EGF as a potential paracrine factor from the oocyte to regulate activin/follis-tatin system in the follicle cells. Biol. Reprod. 71:749-760 (2004).

Weber, G.M., Sullivan, C.V. In vitro hormone induction of final oocyte maturation in striped bass (Morone saxatilis) follicles is inhibited by blockers of phosphatidylinositol 3-kinase activity. Comp. Biochem. Physiol. B, Biochem. Mol. Biol. 129:467-473 (2001).

Weltzien, F.A., Norberg, B., Swanson, P. Isolation and characterization of FSH and LH from pituitary glands of Atlantic halibut (Hippoglossus hippoglossus L.). Gen. Comp. Endocrinol. 131:97-105 (2003a).

Weltzien, F.A., Norberg, B., Helvik, J.V., Andersen, O., Swanson, P., Andersson, E. Identification and localization of eight distinct hormone- producing cell types in the pituitary of male Atlantic halibut (Hippoglossus hippoglossus L.). Comp. Biochem. Physiol. Part A Mol. Integr. Physiol. 134:315-327 (2003b).

Wong, T., Zohar, Y. Novel expression of gonadotropin subunit genes in oocytes of the gilthead seabream (Sparus aurata). Endocrinology 145:5210-5220 (2004).

Wu, H., Lustbader, J.W., Liu, Y., Canfield, R.E., Hendrickson, W.A. Structure of human chorionic gonadotropin at 2.6 A resolution from MAD analysis of the selenomethionyl protein. Structure 2:545-558 (1994).

Xing, Y., Myers, R.V., Cao, D., Lin, W., Jiang, M., Bernard, M.P., Moyle, W.R. Glycoprotein hormone assembly in the endoplasmic reticulum: III The seatbelt and its latch site determine the assembly pathway. J. Biol. Chem. 279:35449-35457 (2004).

Yan, L., Swanson, P., Dickhoff, W.W. A two-receptor model for salmon gonadotropins (GTH I and GTH II). Biol. Reprod. 47:418-427 (1992).

Yaron, Z., Sivan, B. Reproduction. In: Evans, D.H., Claiborne, J.B. (eds.), The Physiology of Fishes. CRC Press, Boca Raton, FL, pp. 343-386 (2006).

Yaron, Z., Gur, G., Melamed, P., Rosenfeld, H., Levavi-Sivan, B., Elizur, A. Regulation of gonadotropin subunit genes in tilapia. Comp. Biochem. Physiol. B, Biochem. Mol. Biol. 129:489-502 (2001).

Yaron, Z., Gur, G., Melamed, P., Rosenfeld, H., Elizur, A., Levavi-Sivan, B. Regulation of fish gonadotropins. Int. Rev. Cytol. - Surv. Cell Biol. 225:131-185 (2003).

Zhang, F.P., Rannikko, A., Huhtaniemi, I. Isolation and characterization of testis-specific cDNAs for luteinizing hormone beta-subunit in the rat. Biochem. Biophys. Res. Commun. 210:858-865 (1995).

Zmora, N., Kumar, S., Kazeto, Y., Trant, J.M. Production of channel catfish (Ictaluruspunctatus) recombinant gonadotropins using the S2 Drosophila cell line system. Fish Physiol. Biochem. 28:475-477 (2003).

Was this article helpful?

0 0
Delicious Diabetic Recipes

Delicious Diabetic Recipes

This brilliant guide will teach you how to cook all those delicious recipes for people who have diabetes.

Get My Free Ebook

Post a comment