FSH: One hormone with multiple forms, or a family of multiple hormones

Reproductive Endocrinology: A Molecular Approach

Volumn , Issue , 2009, Pages 145-160

  Rozell, Tim G ^a   Okrainetz, Rena J ^b  

^a KANSAS STATE UNIVERSITY   (United States)

^b ROYAL UNIVERSITY HOSPITAL   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

EID: 84863414437     PISSN: None     EISSN: None     Source Type: Book    
DOI: 10.1007/978-0-387-88186-7_14     Document Type: Chapter

References (117)

1. Phifer RF, Midgley AR, Spicer SS. Immunohistologic and histologic evidence that follicle-stimulating hormone and luteinizing hormone are present in the same cell type in the human pars distalis. J Clin Endocrinol Metab 1973;36:125-41.
2. Lapthorn AJ, Harris DC, Littlejohn A, et al. Crystal structure of human chorionic gonadotropin. Nature 1994;369:455-61.
3. Fox KM, Dias JA, Van Roey P. Three-dimensional structure of human follicle-stimulating hormone. Mol Endocrinol 2001;15:378-89.
4. Fares F. The role of O-linked and N-linked oligosaccharides on the structure-function of glycoprotein hormones: development of agonists and antagonists. Biochim Biophys Acta 2006;1760:560-7.
5. Villalobos C, Nunez L, Frawley LS, et al. Multi-responsiveness of single anterior pituitary cells to hypothalamic-releasing hormones: a cellular basis for paradoxical secretion. Proc Natl Acad Sci U S A 1997;94:14132-7.
6. Senovilla L, Garcia-Sancho J, Villalobos C. Changes in expression of hypothalamic releasing hormone receptors in individual rat anterior pituitary cells during maturation, puberty and senescence. Endocrinology 2005;146:4627-34.
7. Ferris HA, Shupnik MA. Mechanisms for pulsatile regulation of the gonadotropin subunit genes by GNRH1. Biol Reprod 2006;74:993-8.
8. Burger LL, Dalkin AC, Aylor KW, et al. GnRH pulse frequency modulation of gonadotropin subunit gene transcription in normal gonadotropes-assessment by primary transcript assay provides evidence for roles of GnRH and follistatin. Endocrinology 2002;143:3243-9.
9. Shupnik MA. Effects of gonadotropin-releasing hormone on rat gonadotropin gene transcription in vitro: requirement for pulsatile administration for luteinizing hormone-beta gene stimulation. Mol Endocrinol 1990;4:1444-50.
10. Haisenleder DJ, Dalkin AC, Ortolano GA, et al. A pulsatile gonadotropin-releasing hormone stimulus is required to increase transcription of the gonadotropin subunit genes: evidence for differential regulation of transcription by pulse frequency in vivo. Endocrinology 1991;128:509-17.
11. Clarke IJ, Thomas GB, Yao B, et al. GnRH secretion throughout the ovine estrous cycle. Neuroendocrinology 1987;46:82-8.
12. Jameson JL, Becker CB, Lindell CM, et al. Human folliclestimulating hormone beta-subunit gene encodes multiple messenger ribonucleic acids. Mol Endocrinol 1988;2:806-15.
13. Gharib SD, Roy A, Wierman ME, et al. Isolation and characterization of the gene encoding the beta-subunit of rat folliclestimulating hormone. DNA 1989;8:339-49.
14. Kumar TR, Kelly M, Mortrud M, et al. Cloning of the mouse gonadotropin beta-subunit-encoding genes, I. Structure of the follicle-stimulating hormone beta-subunit-encoding gene. Gene 1995;166:333-4.
15. Kim KE, Gordon DF, Maurer RA. Nucleotide sequence of the bovine gene for follicle-stimulating hormone beta-subunit. DNA 1988;7:227-33.
16. Hirai T, Takikawa H, Kato Y. The gene for the beta subunit of porcine FSH: absence of consensus oestrogen-responsive element and presence of retroposons. J Mol Endocrinol 1990;5:147-58.
17. Guzman K, Miller CD, Phillips CL, et al. The gene encoding ovine follicle-stimulating hormone beta: isolation, characterization, and comparison to a related ovine genomic sequence. DNA Cell Biol 1991;10:593-601.
18. Shen ST, Yu JY. Cloning and gene expression of a cDNA for the chicken follicle-stimulating hormone (FSH)-beta-subunit. Gen Comp Endocrinol 2002;125:375-86.
19. Shen ST, Cheng YS, Shen TY, et al. Molecular cloning of folliclestimulating hormone (FSH)-beta subunit cDNA from duck pituitary. Gen Comp Endocrinol 2006;148:388-94.
20. Chin WW, Kronenberg HM, Dee PC, et al. Nucleotide sequence of the mRNA encoding the pre-alpha-subunit of mouse thyrotropin. Proc Natl Acad Sci U S A 1981;78:5329-33.
21. Chin WW, Habener JF, Kieffer JD, et al. Cell-free translation of the messenger RNA coding for the alpha subunit of thyroidstimulating hormone. J Biol Chem 1978;253:7985-8.
22. Bousfield GR, Perry WM, Ward DN. Gonadotropins. Chemistry and biosynthesis. In: Knobil E, Neill, JD, editors. The Physiology of Reproduction, second edition 1994:1749-92.
23. Godine JE, Chin WW, Habener JF. alpha Subunit of rat pituitary glycoprotein hormones. Primary structure of the precursor determined from the nucleotide sequence of cloned cDNAs. J Biol Chem 1982;257:8368-71.
24. Kaiser UB, Jakubowiak A, Steinberger A, et al. Differential effects of gonadotropin-releasing hormone (GnRH) pulse frequency on gonadotropin subunit and GnRH receptor messenger ribonucleic acid levels in vitro. Endocrinology 1997;138:1224-31.
25. Papavasiliou SS, Zmeili S, Khoury S, et al. Gonadotropinreleasing hormone differentially regulates expression of the genes for luteinizing hormone alpha and beta subunits in male rats. Proc Natl Acad Sci U S A 1986;83:4026-9.
26. Gregg DW, Schwall RH, Nett TM. Regulation of gonadotropin secretion and number of gonadotropin-releasing hormone receptors by inhibin, activin-A, and estradiol. Biol Reprod 1991;44:725-32.
27. Braden TD, Conn PM. Activin-A stimulates the synthesis of gonadotropin-releasing hormone receptors. Endocrinology 1992;130:2101-5.
28. Ruf F, Sealfon SC. Genomics view of gonadotrope signaling circuits. Trends Endocrinol Metab 2004;15:331-8.
29. Salton SR, Blum M, Jonassen JA, et al. Stimulation of pituitary luteinizing hormone secretion by gonadotropin-releasing hormone is not coupled to beta-luteinizing hormone gene transcription. Mol Endocrinol 1988;2:1033-42.
30. Weiss J, Crowley WF, Jr., Jameson JL. Pulsatile gonadotropinreleasing hormone modifies polyadenylation of gonadotropin subunit messenger ribonucleic acids. Endocrinology 1992;130:415-20.
31. Thackray VG, Mellon PL. Synergistic induction of folliclestimulating hormone beta-subunit gene expression by gonadal steroid hormone receptors and Smad proteins. Endocrinology 2008;149:1091-102.
32. Thackray VG, McGillivray SM, Mellon PL. Androgens, progestins, and glucocorticoids induce follicle-stimulating hormone beta-subunit gene expression at the level of the gonadotrope. Mol Endocrinol 2006;20:2062-79.
33. Vale W, Hsueh AJ, Rivier C, et al. The inhibin/activin family of growth factors. In: Sporn MA, Roberts AB, editors. Peptide Growth Factors and Their Receptors, Handbook of Experimental Pharmacology. Heidelberg: Springer-Verlag 1990:211-48.
34. Bilezikjian LM, Blount AL, Donaldson CJ, et al. Pituitary actions of ligands of the TGF-beta family: activins and inhibins. Reproduction 2006;132:207-15.
35. Bilezikjian LM, Blount AL, Leal AM, et al. Autocrine/paracrine regulation of pituitary function by activin, inhibin and follistatin. Mol Cell Endocrinol 2004;225:29-36.
36. Lerch TF, Xu M, Jardetzky TS, et al. The structures that underlie normal reproductive function. Mol Cell Endocrinol 2007;267:1-5.
37. Shimizu A, Kato M, Nakao A, et al. Identification of receptors and Smad proteins involved in activin signalling in a human epidermal keratinocyte cell line. Genes Cells 1998;3:125-34.
38. Farnworth PG, Thean E, Robertson DM, et al. Ovine anterior pituitary production of follistatin in vitro. Endocrinology 1995;136:4397-406.
39. Kaiser UB, Lee BL, Carroll RS, et al. Follistatin gene expression in the pituitary: localization in gonadotropes and folliculostellate cells in diestrous rats. Endocrinology 1992;130:3048-56.
40. Winters SJ, Moore JP. Paracrine control of gonadotrophs. Semin Reprod Med 2007;25:379-87.
41. Guo Q, Kumar TR, Woodruff T, et al. Overexpression of mouse follistatin causes reproductive defects in transgenic mice. Mol Endocrinol 1998;12:96-106.
42. Dalkin AC, Haisenleder DJ, Yasin M, et al. Pituitary activin receptor subtypes and follistatin gene expression in female rats: differential regulation by activin and follistatin. Endocrinology 1996;137:548-54.
43. Bilezikjian LM, Corrigan AZ, Blount AL, et al. Pituitary follistatin and inhibin subunit messenger ribonucleic acid levels are differentially regulated by local and hormonal factors. Endocrinology 1996;137:4277-84.
44. Winters SJ, Dalkin AC, Tsujii T. Evidence that pituitary adenylate cyclase activating polypeptide suppresses follicle-stimulating hormone-beta messenger ribonucleic acid levels by stimulating follistatin gene transcription. Endocrinology 1997;138:4324-9.
45. Dalkin AC, Haisenleder DJ, Gilrain JT, et al. Regulation of pituitary follistatin and inhibin/activin subunit messenger ribonucleic acids (mRNAs) in male and female rats: evidence for inhibin regulation of follistatin mRNA in females. Endocrinology 1998;139:2818-23.
46. Dalkin AC, Haisenleder DJ, Gilrain JT, et al. Gonadotropinreleasing hormone regulation of gonadotropin subunit gene expression in female rats: actions on follicle-stimulating hormone beta messenger ribonucleic acid (mRNA) involve differential expression of pituitary activin (beta-B) and follistatin mRNAs. Endocrinology 1999;140:903-8.
47. Fujii Y, Okada Y, Moore JP, Jr., et al. Evidence that PACAP and GnRH down-regulate follicle-stimulating hormone-beta mRNA levels by stimulating follistatin gene expression: effects on folliculostellate cells, gonadotrophs and LbetaT2 gonadotroph cells. Mol Cell Endocrinol 2002;192:55-64.
48. Rozell TG, Keisler DH. Effects of oestradiol on LH, FSH and prolactin in ovariectomized ewes. J Reprod Fertil 1990;88:645-53.
49. Karsch FJ, Dahl GE, Evans NP, et al. Seasonal changes in gonadotropin-releasing hormone secretion in the ewe: alteration in response to the negative feedback action of estradiol. Biol Reprod 1993;49:1377-83.
50. Gregg DW, Allen MC, Nett TM. Estradiol-induced increase in number of gonadotropin-releasing hormone receptors in cultured ovine pituitary cells. Biol Reprod 1990;43:1032-6.
51. Gregg DW, Nett TM. Direct effects of estradiol-17 beta on the number of gonadotropin-releasing hormone receptors in the ovine pituitary. Biol Reprod 1989;40:288-93.
52. Baratta M, West LA, Turzillo AM, et al. Activin modulates differential effects of estradiol on synthesis and secretion of folliclestimulating hormone in ovine pituitary cells. Biol Reprod 2001;64:714-9.
53. Paul SJ, Ortolano GA, Haisenleder DJ, et al. Gonadotropin subunit messenger RNA concentrations after blockade of gonadotropin-releasing hormone action: testosterone selectively increases follicle-stimulating hormone beta-subunit messenger RNA by posttranscriptional mechanisms. Mol Endocrinol 1990;4:1943-55.
54. Dalkin AC, Paul SJ, Haisenleder DJ, et al. Gonadal steroids effect similar regulation of gonadotrophin subunit mRNA expression in both male and female rats. J Endocrinol 1992;132:39-45.
55. Burger LL, Haisenleder DJ, Aylor KW, et al. Regulation of luteinizing hormone-beta and follicle-stimulating hormone (FSH)-beta gene transcription by androgens: testosterone directly stimulates FSH-beta transcription independent from its role on follistatin gene expression. Endocrinology 2004;145:71-8.
56. Attardi B, Fitzgerald T. Effects of progesterone on the estradiolinduced follicle-stimulating hormone (FSH) surge and FSH beta messenger ribonucleic acid in the rat. Endocrinology 1990;126:2281-7.
57. Ringstrom SJ, Szabo M, Kilen SM, et al. The antiprogestins RU486 and ZK98299 affect follicle-stimulating hormone secretion differentially on estrus, but not on proestrus. Endocrinology 1997;138:2286-90.
58. Webster JC, Pedersen NR, Edwards DP, et al. The 5'-flanking region of the ovine follicle-stimulating hormone-beta gene contains six progesterone response elements: three proximal elements are sufficient to increase transcription in the presence of progesterone. Endocrinology 1995;136:1049-58.
59. O'Conner JL, Wade MF, Prendergast P, et al. A 361 base pair region of the rat FSH-beta promoter contains multiple progesterone receptor-binding sequences and confers progesterone responsiveness. Mol Cell Endocrinol 1997;136:67-78.
60. Tom L, Bhasin S, Salameh W, et al. Induction of azoospermia in normal men with combined Nal-Glu gonadotropin-releasing hormone antagonist and testosterone enanthate. J Clin Endocrinol Metab 1992;75:476-83.
61. Kawakami S, Fujii Y, Okada Y, et al. Paracrine regulation of FSH by follistatin in folliculostellate cell-enriched primate pituitary cell cultures. Endocrinology 2002;143:2250-8.
62. Kilen SM, Szabo M, Strasser GA, et al. Corticosterone selectively increases follicle-stimulating hormone beta-subunit messenger ribonucleic acid in primary anterior pituitary cell culture without affecting its half-life. Endocrinology 1996;137:3802-7.
63. Fares FA, Suganuma N, Nishimori K, et al. Design of a longacting follitropin agonist by fusing the C-terminal sequence of the chorionic gonadotropin beta subunit to the follitropin beta subunit. Proc Natl Acad Sci USA 1992;89:4304-8.
64. La Polt PS, Nishimori K, Fares FA, et al. Enhanced stimulation of follicle maturation and ovulatory potential by long acting folliclestimulating hormone agonists with extended carboxyl-terminal peptides. Endocrinology 1992;131:2514-20.
65. Klein J, Lobel L, Pollak S, et al. Development and characterization of a long-acting recombinant hFSH agonist. Hum Reprod 2003;18:50-6.
66. Ulloa-Aguirre A, Timossi C, Barrios-de-Tomasi J, et al. Impact of carbohydrate heterogeneity in function of follicle-stimulating hormone: Studies derived from in vitro and in vivo models. Biol Reprod 2003;69:379-89.
67. Rathnam P, Saxena BB. Primary amino acid sequence of folliclestimulating hormone from human pituitary glands. I. alpha subunit. J Biol Chem 1975;250:6735-46.
68. Bishop LA, Robertson DM, Cahir N, et al. Specific roles for the asparagine-linked carbohydrate residues of recombinant human follicle stimulating hormone in receptor binding and signal transduction. Mol Endocrinol 1994;8:722-31.
69. Baenziger JU, Green ED. Pituitary glycoprotein hormone oligosaccharides: structure, synthesis and function of the asparagine-linked oligosaccharides on lutropin, follitropin and thyrotropin. Biochim Biophys Acta 1988;947:287-306.
70. Creus S, Chaia Z, Pellizzari EH, et al. Human FSH isoforms: carbohydrate complexity as determinant of in-vitro bioactivity. Mol Cell Endocrinol 2001;174:41-9.
71. Ulloa-Aguirre A, Midgley AR, Jr., Beitins IZ, et al. Folliclestimulating isohormones: characterization and physiological relevance. Endocr Rev 1995;16:765-87.
72. Timossi CM, Barrios De Tomasi J, Zambrano E, et al. A naturally occurring basically charged human follicle-stimulating hormone (FSH) variant inhibits FSH-induced androgen aromatization and tissue-type plasminogen activator enzyme activity in vitro. Neuroendocrinology 1998;67:153-63.
73. Phillips DJ, Albertsson-Wikland K, Eriksson K, et al. Changes in the isoforms of luteinizing hormone and follicle-stimulating hormone during puberty in normal children. J Clin Endocrinol Metab 1997;82:3103-6.
74. Padmanabhan V, Mieher CD, Borondy M, et al. Circulating bioactive follicle-stimulating hormone and less acidic folliclestimulating hormone isoforms increase during experimental induction of puberty in the female lamb. Endocrinology 1992;131:213-20.
75. Smith PL, Baenziger JU. Molecular basis of recognition by the glycoprotein hormone-specific N-acetylgalactosaminetransferase. Proc Natl Acad Sci U S A 1992;89:329-33.
76. Phillips DJ, Wide L. Serum gonadotropin isoforms become more basic after an exogenous challenge of gonadotropin-releasing hormone in children undergoing pubertal development. J Clin Endocrinol Metab 1994;79:814-9.
77. Creus S, Pellizzari E, Cigorraga SB, et al. FSH isoforms: bio and immuno-activities in post-menopausal and normal menstruating women. Clin Endocrinol (Oxf) 1996;44:181-9.
78. Wide L, Bakos O. More basic forms of both human folliclestimulating hormone and luteinizing hormone in serum at midcycle compared with the follicular or luteal phase. J Clin Endocrinol Metab 1993;76:885-9.
79. Cooke DJ, Crowe MA, Roche JF. Circulating FSH isoform patterns during recurrent increases in FSH throughout the oestrous cycle of heifers. J Reprod Fertil 1997;110:339-45.
80. Dharmesh SM, Baenziger JU. Estrogen modulates expression of the glycosyltransferases that synthesize sulfated oligosaccharides on lutropin. Proc Natl Acad Sci U S A 1993;90:11127-31.
81. Damian-Matsumura P, Zaga V, Maldonado A, et al. Oestrogens regulate pituitary alpha2, 3-sialyltransferase messenger ribonucleic acid levels in the female rat. J Mol Endocrinol 1999;23:153-65.
82. Ulloa-Aguirre A, Damian-Matsumura P, Espinoza R, et al. Effects of neonatal androgenization on the chromatofocusing pattern of anterior pituitary FSH in the female rat. J Endocrinol 1990;126:323-32.
83. Ulloa-Aguirre A, Schwall R, Cravioto A, et al. Effects of gonadotrophin-releasing hormone, recombinant human activin-A and sex steroid hormones upon the follicle-stimulating isohormones secreted by rat anterior pituitary cells in culture. J Endocrinol 1992;134:97-106.
84. Padmanabhan V, Christman GM, Randolph JF, et al. Dynamics of bioactive follicle-stimulating hormone secretion in women with polycystic ovary syndrome: effects of estradiol and progesterone. Fertil Steril 2001;75:881-8.
85. Rulli SB, Creus S, Pellizzari E, et al. Immunological and biological activities of pituitary FSH isoforms in prepubertal male rats: effect of antiandrogens. Neuroendocrinology 1996;63:514-21.
86. Prestoz LL, Couto AS, Shin YS, et al. Altered follicle stimulating hormone isoforms in female galactosemia patients. Eur J Pediatr 1997;156:116-20.
87. Flack MR, Bennet AP, Froehlich J, et al. Increased biological activity due to basic isoforms in recombinant human folliclestimulating hormone produced in a human cell line. J Clin Endocrinol Metab 1994;79:756-60.
88. Cerpa-Poljak A, Bishop LA, Hort YJ, et al. Isoelectric charge of recombinant human follicle-stimulating hormone isoforms determines receptor affinity and in vitro bioactivity. Endocrinology 1993;132:351-6.
89. Barrios-De-Tomasi J, Timossi C, Merchant H, et al. Assessment of the in vitro and in vivo biological activities of the human follicle-stimulating isohormones. Mol Cell Endocrinol 2002;186:189-98.
90. Vitt UA, Kloosterboer HJ, Rose UM, et al. Isoforms of human recombinant follicle-stimulating hormone: comparison of effects on murine follicle development in vitro. Biol Reprod 1998;59:854-61.
91. West CR, Carlson NE, Lee JS, et al. Acidic mix of FSH isoforms are better facilitators of ovarian follicular maturation and E2 production than the less acidic. Endocrinology 2002;143:107-16.
92. Vitt UA, Nayudu PL, Rose UM, et al. Embryonic development after follicle culture is influenced by follicle-stimulating hormone isoelectric point range. Biol Reprod 2001;65:1542-7.
93. Zambrano E, Zarinan T, Olivares A, et al. Receptor binding activity and in vitro biological activity of the human FSH charge isoforms as disclosed by heterologous and homologous assay systems - implications for the structure-function relationship of the FSH variants. Endocrine 1999;10:113-21.
94. Arey BJ, Stevis PE, Deecher DC, et al. Induction of promiscuous G protein coupling of the follicle-stimulating hormone (FSH) receptor: A novel mechanism for transducing pleiotropic actions of FSH isoforms. Mol Endocrinol 1997;11:517-26.
95. Sairam MR. Role of carbohydrates in glycoprotein hormone signal transduction. FASEB J 1989;3:1915-26.
96. Sairam MR, Bhargavi GN. A role for glycosylation of the alpha subunit in transduction of biological signal in glycoprotein hormones. Science 1985;229:65-7.
97. Padmanabhan V, Sairam MR, Hassing JM, et al. Folliclestimulating hormone signal transduction: role of carbohydrate in aromatase induction in immature rat Sertoli cells. Mol Cell Endocrinol 1991;79:119-28.
98. Keene JL, Nishimori K, Galway AB, et al. Recombinant deglycosylated human FSH is an antagonist of human FSH action in cultured rat granulosa cells. Endocr J 1994;2:175-8.
99. D'Antonio M, Borrelli F, Datola A, et al. Biological characterization of recombinant human follicle stimulating hormone isoforms. Hum Reprod 1999;14:1160-7.
100. Fan QR, Hendrickson WA. Structure of human folliclestimulating hormone in complex with its receptor. Nature 2005;433:269-77.
101. Sato A, Perlas E, Ben-Menahem D, et al. Cystine knot of the gonadotropin alpha subunit is critical for intracellular behavior but not for in vitro biological activity. J Biol Chem 1997;272:18098-103.
102. Xing Y, Myers RV, Cao D, et al. Glycoprotein hormone assembly in the endoplasmic reticulum: III. The seatbelt and its latch site determine the assembly pathway. J Biol Chem 2004;279:35449-57.
103. Fan QR, Hendrickson WA. Assembly and structural characterization of an authentic complex between human follicle stimulating hormone and a hormone-binding ectodomain of its receptor. Mol Cell Endocrinol 2007;260-262:73-82.
104. Vassart G, Pardo L, Costagliola S. A molecular dissection of the glycoprotein hormone receptors. Trends Biochem Sci 2004;29:119-26.
105. Vasseur C, Rodien P, Beau I, et al. A chorionic gonadotropinsensitive mutation in the follicle-stimulating hormone receptor as a cause of familial gestational spontaneous ovarian hyperstimulation syndrome. N Engl J Med 2003;349:753-9.
106. Cariboni A, Maggi R. Kallmann's syndrome, a neuronal migration defect. Cell Mol Life Sci 2006;63:2512-26.
107. Stouffer RL, Zelinski-Wooten MB. Overriding follicle selection in controlled ovarian stimulation protocols: quality vs quantity. Reprod Biol Endocrinol 2004;2:32.
108. Gleicher N, Vietzke M, Vidali A. Bye-bye urinary gonadotrophins? Recombinant FSH: a real progress in ovulation induction and IVF? Hum Reprod 2003;18:476-82..
109. Nishimura R, Shin J, Ji I, et al. A single amino acid substitution in an ectopic alpha subunit of a human carcinoma choriogonadotropin. J Biol Chem 1986;261:10475-7.
110. Meduri G, Bachelot A, Cocca MP, et al. Molecular pathology of the FSH receptor: new insights into FSH physiology. Mol Cell Endocrinol 2008;282:130-42.
111. Themmen A P N, Huhtaniemi IT. Mutations of gonadotropins and gonadotropin receptors: elucidating the physiology and pathophysiology of pituitary-gonadal function. Endocr Rev 2000;21:551-83.
112. Latronico AC, Costa EM, Domenice S, et al. Clinical and molecular analysis of human reproductive disorders in Brazilian patients. Braz J Med Biol Res 2004;37:137-44.
113. Matthews CH, Borgato S, Beck-Peccoz P, et al. Primary amenorrhoea and infertility due to a mutation in the beta-subunit of follicle-stimulating hormone. Nat Genet 1993;5:83-6.
114. Layman LC, Lee EJ, Peak DB, et al. Delayed puberty and hypogonadism caused by mutations in the follicle-stimulating hormone beta-subunit gene. N Engl J Med 1997;337:607-11.
115. Layman LC, Porto AL, Xie J, et al. FSH beta gene mutations in a female with partial breast development and a male sibling with normal puberty and azoospermia. J Clin Endocrinol Metab 2002;87:3702-7.
116. Phillip M, Arbelle JE, Segev Y, et al. Male hypogonadism due to a mutation in the gene for the beta-subunit of follicle-stimulating hormone. N Engl J Med 1998;338:1729-32.
117. Zhang M, Tao YX, Ryan GL, et al. Intrinsic differences in the response of the human lutropin receptor versus the human follitropin receptor to activating mutations. J Biol Chem 2007;282:25527-39.