Wang Huizhen, Butnev Vladimir, Bousfield George R, Kumar T Rajendra
Department of Molecular and Integrative Physiology.
Department of Biological Sciences, Wichita State University, Wichita, KS 67260, USA.
Mol Cell Endocrinol. 2016 May 5;426:113-24. doi: 10.1016/j.mce.2016.02.015. Epub 2016 Feb 19.
Follicle-stimulating hormone (FSH) is a gonadotrope-derived heterodimeric glycoprotein. Both the common α- and hormone-specific β subunits contain Asn-linked N-glycan chains. Recently, macroheterogeneous FSH glycoforms consisting of β-subunits that differ in N-glycan number were identified in pituitaries of several species and subsequently the recombinant human FSH glycoforms biochemically characterized. Although chemical modification and in vitro site-directed mutagenesis studies defined the roles of N-glycans on gonadotropin subunits, in vivo functional analyses in a whole-animal setting are lacking. Here, we have generated transgenic mice with gonadotrope-specific expression of either an HFSHB(WT) transgene that encodes human FSHβ WT subunit or an HFSHB(dgc) transgene that encodes a human FSHβ(Asn7Δ 24Δ) double N-glycosylation site mutant subunit, and separately introduced these transgenes onto Fshb null background using a genetic rescue strategy. We demonstrate that the human FSHβ(Asn7Δ 24Δ) double N-glycosylation site mutant subunit, unlike human FSHβ WT subunit, inefficiently combines with the mouse α-subunit in pituitaries of Fshb null mice. FSH dimer containing this mutant FSHβ subunit is inefficiently secreted with very low levels detectable in serum. Fshb null male mice expressing HFSHB(dgc) transgene are fertile and exhibit testis tubule size and sperm number similar to those of Fshb null mice. Fshb null female mice expressing the mutant, but not WT human FSHβ subunit-containing FSH dimer are infertile, demonstrate no evidence of estrus cycles, and many of the FSH-responsive genes remain suppressed in their ovaries. Thus, HFSHB(dgc) unlike HFSHB(WT) transgene does not rescue Fshb null mice. Our genetic approach provides direct in vivo evidence that N-linked glycans on FSHβ subunit are essential for its efficient assembly with the α-subunit to form FSH heterodimer in pituitary. Our studies also reveal that N-glycans on FSHβ subunit are essential for FSH secretion and FSH in vivo bioactivity to regulate gonadal growth and physiology.
促卵泡激素(FSH)是一种由促性腺激素细胞产生的异源二聚体糖蛋白。常见的α亚基和激素特异性β亚基均含有天冬酰胺连接的N-聚糖链。最近,在几种物种的垂体中鉴定出了由N-聚糖数量不同的β亚基组成的大异质性FSH糖型,随后对重组人FSH糖型进行了生化特性分析。尽管化学修饰和体外定点诱变研究确定了N-聚糖在促性腺激素亚基上的作用,但缺乏在全动物环境中的体内功能分析。在这里,我们生成了转基因小鼠,其促性腺激素细胞特异性表达编码人FSHβ野生型亚基的HFSHB(WT)转基因或编码人FSHβ(Asn7Δ 24Δ)双N-糖基化位点突变亚基的HFSHB(dgc)转基因,并使用基因拯救策略将这些转基因分别导入Fshb基因敲除背景中。我们证明,与人类FSHβ野生型亚基不同,人类FSHβ(Asn7Δ 24Δ)双N-糖基化位点突变亚基在Fshb基因敲除小鼠的垂体中与小鼠α亚基的结合效率低下。含有这种突变FSHβ亚基的FSH二聚体分泌效率低下,血清中可检测到的水平非常低。表达HFSHB(dgc)转基因的Fshb基因敲除雄性小鼠可育,其睾丸小管大小和精子数量与Fshb基因敲除小鼠相似。表达含突变而非野生型人FSHβ亚基的FSH二聚体的Fshb基因敲除雌性小鼠不育,没有发情周期的迹象,并且它们卵巢中的许多FSH反应基因仍然受到抑制。因此,与HFSHB(WT)转基因不同,HFSHB(dgc)不能拯救Fshb基因敲除小鼠。我们的遗传学方法提供了直接的体内证据,表明FSHβ亚基上的N-连接聚糖对于其与α亚基有效组装以在垂体中形成FSH异源二聚体至关重要。我们的研究还表明,FSHβ亚基上的N-聚糖对于FSH分泌和FSH在体内调节性腺生长和生理的生物活性至关重要。