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5 Endocrine Control of Testicular Development and Initiation of Spermatogenesis in Bulls
Leonardo F.C. Brito
STgenetics, Middleton, WI, USA
Introduction
The process of testicular development that leads to initiation of spermatogenesis in bulls involves complex maturation mechanisms of the hypothalamus–pituitary–testes axis. Sexual development can be divided into three periods according to changes in gonadotropin and testosterone concentrations, namely the infantile, prepubertal, and pubertal periods. These changes are accompanied by changes in testicular cell proliferation and differentiation (Figure 5.1).
Figure 5.1 Mean serum luteinizing hormone (LH), follicle‐stimulating hormone (FSH), and testosterone concentrations in bulls during the infantile (a), prepubertal (b), and pubertal/postpubertal (c) periods. Data from 2 to 6 weeks are adapted from Hereford × Charolais bulls [1]. Data from 10 to 70 weeks are from Angus and Angus × Charolais bulls receiving adequate nutrition [2–5]. Infancy is the period that extends from birth until approximately eight weeks of age. During this period gonadotropin and testosterone concentrations are low, the testicular parenchyma is occupied mostly by interstitial tissue, seminiferous cords are lined by undifferentiated Sertoli cells, and centrally located gonocytes with large nuclei can be observed. The prepubertal period is characterized by a dramatic increase in gonadotropin concentrations (the early gonadotropin rise) and by slowly increasing testosterone secretion. The prepubertal period extends from approximately 10 to 26 weeks of age and during this period a cord lumen begins to develop and gonocytes migrate toward the basement membrane, differentiating into spermatogonia. Gonadotropin concentrations decrease concomitantly with a rapid increase in testosterone concentration during the pubertal period, which also coincides with the start of a phase of rapid testicular growth. Formation of the tubular lumen is evidence of Sertoli cell differentiation and development of a functional blood–testis barrier that precedes the appearance of primary spermatocytes and spermatids around 32 weeks of age. With continuous increase in diameter, seminiferous tubules occupy most of the testicular parenchyma and start to produce mature sperm at approximately 40 weeks of age.
Sources: Data from [2,4–6].
Infantile Period
The infantile period is characterized by low gonadotropin and testosterone secretion and relatively few changes in testicular cellular composition. This period extends from birth until approximately two months of age in Bos taurus bulls.
Gonadotropin secretion during the infantile period is low due to reduced gonadotropin‐releasing hormone (GnRH) secretion; maturation changes within the hypothalamus result in increased GnRH pulse secretion and drive the transition from the infantile period. Increased GnRH secretion is dependent on either the development of central stimulatory inputs or removal of inhibitory inputs. Hypothalamus weight and GnRH content do not increase during the infantile period, but hypothalamic concentrations of estradiol receptors decrease after one month of age [7]. However, the hypothesis that GnRH secretion is low during infancy due to elevated sensitivity of the hypothalamus to the negative feedback of sex steroids (gonadostat hypothesis) has been questioned in bulls, since castration does not alter luteinizing hormone (LH) pulse frequency or mean concentrations before two months of age [8]. Nonetheless, since GnRH secretion into hypophyseal portal blood is not necessarily accompanied by LH secretion during the infantile period, experiments that use LH concentrations to infer GnRH secretion patterns during this period need to be interpreted with caution [9]. Another possibility is that removal of opioidergic inhibition and/or increased dopaminergic activity may be involved in triggering the increase in GnRH secretion during the infantile period. Opioidergic inhibition of LH pulse frequency during the infantile period has been demonstrated by increased LH secretion between one and four months of age in bulls treated with naloxone, an opioid competitive receptor antagonist [10], whereas concentrations of norepinephrine, dopamine, and dopamine metabolites increased twofold to threefold in the anterior hypothalamic–preoptic area in bulls aged 0.5–2.5 months [11].
Direct evaluation of blood samples from the hypophyseal portal system has demonstrated that GnRH pulsatile secretion increases linearly from age two weeks (3.5 pulses per 10 hours) to 12 weeks (8.9 pulses per 10 hours) in bulls. Although GnRH secretion into hypophyseal portal blood was detected at two weeks, pulsatile LH secretion was not detected in jugular blood samples before eight weeks of age. In addition, GnRH pulses are not necessarily accompanied by LH secretion until 8–12 weeks of age, when all GnRH pulses result in LH pulses. The increase in pulsatile GnRH release from two to eight weeks of age without a concomitant increase in LH secretion may represent a reduced ability of the pituitary gland to respond to GnRH stimulus [9]. The period in which GnRH pulses do not stimulate LH secretion correspond to a period during which there is an increase in pituitary weight, GnRH receptor concentration, and LH content [7]. Moreover, frequent GnRH treatments during the infantile period in calves increases pituitary LH‐β mRNA, LH content, and GnRH receptors, with resulting increases in LH pulse frequency and mean concentrations [12], indicating that increased GnRH pulse frequency results in increased pituitary sensitivity to GnRH. With time, the increased GnRH secretion results in the increased LH pulse frequency observed during the prepubertal period.
From birth until approximately two months of age, mesenchymal‐like cells comprise the majority of the cells in the testicular interstitial tissue. Typical Leydig cells constitute about 6% of all intertubular cells at one month of age and a number of these cells are found in an advanced degenerative state, probably as remnants of the fetal Leydig cell population. Degenerating fetal and newly formed Leydig cells coexist until two months of age, but only Leydig cells formed postnatally are observed thereafter [13, 14]. The diameter of the seminiferous tubules is approximately 50 μm during the infantile period; tubule is actually a misnomer, since these are in fact solid cords with no lumen at this stage of development. Undifferentiated Sertoli cells (or undifferentiated supporting cells) are the predominant intratubular cells
