Citation

Tammasse IFU, Tamrin F (2023) Different of Hypothalamic-Pituitary-Gonadal Axis in Male and Female. Reprod Med Int 6:023. doi.org/10.23937/2643-4555/1710023

Review Article | OPEN ACCESS DOI: 10.23937/2643-4555/1710023

Different of Hypothalamic-Pituitary-Gonadal Axis in Male and Female

Iin Fadhilah Utami Tammasse1* and Fachrul Tamrin2

1Medical Doctor, University of Bristol, Bristol, UK

2RSUP Persahabatan, Indonesia

Introduction

Human sexual development starts early in fetal life and is completed in adulthood when the gonads have developed to their full reproductive potential. The HPG axis is a highly complex unit that influences fertility success in men and women [1]. The development, structure, and function of the HPG axis between males and females will be compared and differentiated below (Table 1) [2-8].

Table 1: Comparison of HPG axis of Males and Females. View Table 1

The Hypothalamus-Pituitary-Gonads Axis

In both sexes, the physiological link of the HPG axis initiated when the hypothalamic peptide (GnRH) released into the anterior pituitary, triggers the production of gonadotrophins (LH and FSH), then stimulates spermatogenesis in males or oogenesis in females by binding to the gonad’s receptors which then release estrogen, progesterone, testosterone, and inhibins [1,4]. Complex feedback loops control the HPG axis’s principal hormone production process in males and females are shown in Figure 1 [2,3,9-13].

(Image created with Biorender.com, adapted from Ozawa 2021)
Figure 1: Schematic of the different hormone production pathways of male and female Hypothalamic-pituitary-gonadal (HPG) axis. Kiss 1 neurons in ARC offer tonic stimulatory input to GnRH neurons which are adversely controlled by sex steroids. AVPV sex steroids activate Kiss 1 neurons. Trans-synaptic and glial inputs trigger GnRH release in the hypophysial bloodstream. GnRH modulates LH and FSH, which stimulate ovarian and testicular development. LH activates theca cells in females, which generate estrogen, primarily estradiol. FSH act on granulosa cells that modulate the aromatase. In the ovary, the corpus luteum release progesterone, which, together with estrogen, provides positive and negative feedback to the pituitary and hypothalamus. LH stimulates testosterone production in Leydig cells in males, negatively affecting the hypothalamus and pituitary. Testosterone is metabolized further to dihydrotestosterone and estradiol, negatively affecting the hypothalamus and pituitary. While FSH act on Sertoli cells that stimulate spermatogenesis [2,3,9-13]. View Figure 1

Regarding similarity, male and female hormone productions were initially influenced by the tonic release of kisspeptin by the arcuate and anteroventral periventral kisspeptin neuron, along with neurokinin B and dynorphin [9]. However, we believe there must be a gap of knowledge in terms of Kisspeptin production in males and females since the GnRH surge mechanism only exists in females.

The fundamental difference between both sexes was that males have very few Kisspeptin neurons, while females have many Kisspeptin neurons in the AVPV [2]. It also reflects the morphological differences, such as the amount of cell bodies and fiber density that influence higher input to GnRH neurons in females. In females, the presence of sex hormones stimulates Kiss1 expression as the cellular basis for estrogen’s positive feedback stimulation of the preovulatory GnRH surge [2].We need to better understand the influence of Kisspeptin in the switching mechanism affected by the steroid hormones from negative to positive feedback, which does not exist in males, not only differentiating Kisspeptin morphologically (Table 1).

The Hypothalamic

In males and females, GnRH neurons are directly activated by kisspeptin, produced in the hypothalamus and thought to affect GnRH activity differently. The Kisspeptin 1 gene strongly stimulates GnRH secretion [14]. But the amount of Kisspeptin differs between men and women is unclear. Both sexes have the mechanism of GnRH pulsatility, which is thought to be regulated by ARC and AVPV nuclei [15].

In females, GnRH surge is known to be LH triggered, which will cause the LH surge. In males, the GnRH-LH surge may not occur due to the absence of estrogen and estrogen-sensitive cells [2,16]. Other studies found Kisspeptin cell bodies in the AVPV act as LH surge generator, while KNDy neurons in the ARC as pulse generators [3]. Different neurons and regions of kisspeptin stimulus will affect the GnRH function. Hence, the LH surge activity only happens in females (Table 1).

In females, The AVPV is the focus of positive feedback from estrogen while the ARC is the strong target of estrogen’s negative feedback [17-19]. Estrogen's stimulatory effects on the surge mechanism are assumed to be mediated by Era which expressed by nearly all Kiss1 neurons, and only females have significant amounts of Kiss1 cells [2]. Estrogen can stimulate ovulation and LH secretion in females [2,20].

Kiss 1 cells are more prominent in females than in males [16,21]. Kisspeptin fibers in the AVPV of sexually mature females are 15-fold higher in mice than in rats [22,23] (Figure 2). It was found by the amount and distribution of immunolabelled kisspeptin in the infundibulum, which is higher in women [24].

(Image created with Biorender.com, adapted from Kauffman, 2007)
Figure 2: The schematic comparison of the Kisspeptin pathway in GnRH stimulation of male and female. Kisspeptin from Kiss 1 neurons induce GnRH secretion. The amount of kisspeptin generated differently is higher in female than male along with the sex hormones regulations [2,15]. View Figure 2

Kisspeptin from Kiss 1 neurons induce GnRH secretion. The amount of kisspeptin generated differently is higher in female than male along with the sex hormones regulations.

The Pituitary: LH and FSH

The pituitary or hypophysis gland is crucial in neuroendocrine control, comprised of various cell types that release hormones in blood circulation in both sexes [25]. The pituitary gland is located underneath the hypothalamus and is divided into adenohypophysis and neurohypophysis. Gonadotrophs are pituitary gland cells with GnRH receptors and generate FSH and LH in males and females.

In both sexes, LH and FSH are made up of general α and specific β subunits essential for the heterodimer’s biological activity. The variable size and electron density of gonadotrophic secretory granules distinguish them. The granule population in males rat gonadotroph is unique, while females rat gonadotroph has less diversity in secretory granules [26].

The size of the hypophysis gland is more extensive in females than in males. The hypophysis reaches the maximum size under hormonally active situations such as pregnancy and puberty. Study shows that the median height of the hypophysis gland under a year and the 18-year-old group was 3.81 ± 0.68 and 8.48 ± 1.08 mm for girls and boys was 3.91 ± 0.75 and 6.19 ± 0.88 mm. In terms of size, this might occur due to LH hypersecretion [27-29].

Gametogenesis and Steroidogenesis

The FSH and LH affect both ovaries and testes differently regarding steroid and gametes production. In terms of gametogenesis, FSH plays an essential role in both sexes. In females, FSH promotes follicular maturation and granulosa cell estrogen synthesis. In steroidogenesis, FSH attaches to FSH receptors on granulosa cells causing androgens production in internal theca cells to aromatize estrogens [25]. In contrast with males, after FSH stimulates the synthesis of androgen receptors, inhibin production and calcium signaling on FSH receptors will stimulate spermatogenesis on Sertoli cells [6] (Figure 1).

LH has an essential role in steroidogenesis. In females, LH promotes theca cell androgen production to cause ovulation and maintains corpus luteum progesterone production [26]. On internal theca cells, LH binds in the early follicular phase to LH-receptor surface, increasing androgen synthesis (androstenedione, testosterone) and follicle development [6]. In males, LH binds exclusively to Leydig cells (LH receptors) to stimulate testosterone synthesis, whereas prolactin and inhibin may function simultaneously to boost LH production.

As explained earlier, GnRH/LH surge marks the difference between both sexes. In females, LH pulses change every 90-100 minutes to every 4-8 hours from the early follicular phase to the late luteal phase [6]. While in males, LH pulses occur every 55 minutes in mature males, testosterone is the primary driving factor that governs LH synthesis, either directly or indirectly, via aromatization to estradiol [6] (Figure 3 and Figure 4) [30-32].

(Image created with Biorender.com, adapted from Duraijayanagam, 2015)
Figure 3: The schematic comparison of meiotic phases in Spermatogenesis in males and Oogenesis in females.
In this Oogenesis phase, the periodical process of oocyte production through females life and the meiosis stages of oocytes also the sex steroid produced has been the complete difference to the spermatogenesis process [30,31]. View Figure 3

(Image created with Biorender.com, adapted from Cordeiro, 2015)
Figure 4: The schematic comparison of meiotic phases in Spermatogenesis in males and Oogenesis in females.
In this Spermatogenesis phase, the continuous process of sperm production through the male's life and the meiotic process of the gametes distinguished spermatogenesis from oogenesis [30-32]. View Figure 4

The Gonads: Spermatogenesis and Oogonesis

The meiotic phase between both processes distinguishes oogenesis from spermatogenesis in males and females. In males, the process is continuous without following episodic hormonal phases. In females, in the dictyate stage of meiosis I until LH promotes ultimate oocyte maturation which is periodically according to the hormonal phases [5]. In males, spermatogenesis takes 74 days in the testicular seminiferous tubules to complete SSC differentiation: mitosis, meiosis, and spermiogenesis [7], while In females, it takes 28-35 days for a cycle through different phases, and only one dominant follicle is produced [33,34].

In spermatogenesis, spermatogonia are undifferentiated, capable of self-renewal and differentiation into A-paired (Ap) spermatogonia. A-aligned (Aal) spermatogonia develop through sequential mitosis. Sertoli cell-derived, FSH-induced growth factors [7]. While in female oogenesis, the mitotic process occur before birth and undergoes an arrest in prophase I. In contrast to males, which mitotic divisions change into A2, A3, A4, and B spermatogonia [33].

Spermiogenesis takes 26 days, as secondary spermatocytes go through meiosis II when sister chromatids split to form haploid round spermatids. While in females, after puberty, oocyte meiotic maturation begins As a result of the LH surge, the oocyte progresses to metaphase II, culminating in the ejection of the first polar body [34]. Meiosis restarts after the LH surge when cumulus cells expand, mediated by the formation of hyaluronic acid by the cumulus cells. Upon an LH trigger, Nppc mRNA levels (encoding CNP) decline, resulting in reduced synthesis and diffusion [34]. Finally, developed spermatozoa are highly specialized cells that need active mobility to enter the female genital canal and reach the oocyte [8]. In females, the oocyte will complete meiosis if it is fertilized.

Conclusions

Overall, the similarity and differences between both sexes are essential in reproduction. In males and females, the similarity was reflected in the hypothalamic-pituitary structure, hormonal feedback, and GnRH pulsatility. The differences between both sexes were reflected in kisspeptin, gonads (ovary and testes), sex steroids (estrogen and testosterone), number of gametes produced (oocyte and sperms), and duration (periodical and continuous process) see (Table 1).

References

  1. Kaprara A, Huhtaniemi IT (2018) The hypothalamus-pituitary-gonad axis: Tales of mice and men. Metabolism 86: 3-17.
  2. Kauffman AS, Clifton DK, Steiner RA (2007) Emerging ideas about kisspeptin- GPR54 signaling in the neuroendocrine regulation of reproduction. Trends Neurosci 30: 504-511.
  3. Ozawa H (2022) Kisspeptin neurons as an integration center of reproductive regulation: Observation of reproductive function based on a new concept of reproductive regulatory nervous system. Reprod Med Biol 21: e12419.
  4. Vadakkadath Meethal S, Atwood CS (2005) The role of hypothalamic-pituitary-gonadal hormones in the normal structure and functioning of the brain. Cell Mol Life Sci 62: 257-270.
  5. Sanchez F, Smitz J (2012) Molecular control of oogenesis. Biochim Biophys Acta 1822: 1896-1912.
  6. Ulloa-Aguirre A, Lira-Albarran S (2016) Clinical applications of gonadotropins in the male. Prog Mol Biol Transl Sci 143: 121-174.
  7. Chen SR, Liu YX (2015) Regulation of spermatogonial stem cell self-renewal and spermatocyte meiosis by Sertoli cell signaling. Reproduction 149: R159-R167.
  8. Cannarella R, Condorelli RA, Mongioi LM, La Vignera S, Calogero AE (2020) Molecular biology of spermatogenesis: novel targets of apparently idiopathic male infertility. Int J Mol Sci 21: 1728.
  9. Navarro VM (2020) Metabolic regulation of kisspeptin - the link between energy balance and reproduction. Nat Rev Endocrinol 16: 407-420.
  10. Creasy DM, Chapin RE (2013) Male reproductive system. Haschek and Rousseaux's Handbook of Toxicologic Pathology 3: 2493-2598.
  11. Matsuda F, Ohkura S, Magata F, Munetomo A, Chen J, et al. (2019) Role of kisspeptin neurons as a GnRH surge generator: Comparative aspects in rodents and non-rodent mammals. J Obstet Gynaecol Res 45: 2318-2329.
  12. Skorupskaite K, George JT, Anderson RA (2014) The kisspeptin-GnRH pathway in human reproductive health and disease. Hum Reprod Update 20: 485-500.
  13. Pinilla L, Aguilar E, Dieguez C, Millar RP, Tena-Sempere M (2012) Kisspeptins and reproduction: Physiological roles and regulatory mechanisms. Physiol Rev 92: 1235-1316.
  14. Acevedo-Rodriguez A, Kauffman AS, Cherrington BD, Borges CS, Roepke TA, et al. (2018) Emerging insights into hypothalamic-pituitary-gonadal axis regulation and interaction with stress signalling. J Neuroendocrinol 30: e12590.
  15. Bianco SD (2012) A potential mechanism for the sexual dimorphism in the onset of puberty and incidence of idiopathic central precocious puberty in children: Sex-specific kisspeptin as an integrator of puberty signals. Front Endocrinol (Lausanne) 3: 149.
  16. Ottem EN, Godwin JG, Krishnan S, Petersen SL (2004) Dual-Phenotype GABA/Glutamate neurons in adult preoptic area: sexual dimorphism and function. The Journal of Neuroscience 24: 8097-8105.
  17. Mayer C, Acosta-Martinez M, Dubois SL, Wolfe A, Radovick S, et al. (2010) Timing and completion of puberty in female mice depend on estrogen receptor alpha-signaling in kisspeptin neurons. Proceedings of the National Academy of Sciences 107: 22693-22698.
  18. Oakley AE, Clifton DK, Steiner RA (2009) Kisspeptin signaling in the brain. Endocr Rev 30: 713-743.
  19. Kauffman AS (2010) Coming of age in the kisspeptin era: sex differences, development, and puberty. Mol Cell Endocrinol 324: 51-63.
  20. Clarkson J, Herbison AE (2006) Postnatal development of kisspeptin neurons in mouse hypothalamus; sexual dimorphism and projections to gonadotropin-releasing hormone neurons. Endocrinology 147: 5817-5825.
  21. Smith KB, Murray E, Chandrasegaram R, Liang J, Mallet JF, et al. (2021) Pubertal immune challenge suppresses the hypothalamic-pituitary-gonadal axis in male and female mice. Brain Res Bull 170: 90-97.
  22. Bakker J, Pierman S, González-Martínez D (2010) Effects of aromatase mutation (ArKO) on the sexual differentiation of kisspeptin neuronal numbers and their activation by same versus opposite sex urinary pheromones. Horm Behav 57: 390-395.
  23. Pita J, Barrios V, Gavela-Pérez T, Martos-Moreno GÁ, Muñoz-Calvo MT, et al. (2011) Circulating kisspeptin levels exhibit sexual dimorphism in adults, are increased in obese prepubertal girls and do not suffer modifications in girls with idiopathic central precocious puberty. Peptides 32: 1781-1786.
  24. Hrabovszky E, Ciofi P, Vida B, Horvath MC, Keller E, et al. (2010) The kisspeptin system of the human hypothalamus: sexual dimorphism and relationship with gonadotropin-releasing hormone and neurokinin B neurons. Eur J Neurosci 31: 1984-1998.
  25. Dagklis T, Ravanos K, Makedou K, Kourtis A, Rousso D (2015) Common features and differences of the hypothalamic-pituitary-gonadal axis in male and female. Gynecol Endocrinol 31: 14-17.
  26. Abel MH, Widen A, Wang X, Huhtaniemi I, Pakarinen P, et al. (2014) Pituitary gonadotrophic hormone synthesis, secretion, subunit gene expression and cell structure in normal and follicle-stimulating hormone beta knockout, follicle-stimulating hormone receptor knockout, luteinising hormone receptor knockout, hypogonadal and ovariectomised female mice. J Neuroendocrinol 26: 785-795.
  27. Kato K, Saeki N, Yamaura A (2002) Morphological changes on MR imaging of the normal pituitary gland related to age and sex: Main emphasis on pubescent females. J Clin Neurosci 9: 53-56.
  28. Avinash Kumar K (2017) MRI measurement of normal pituitary size using volumetric imaging in scottish patients. Current Trends in Clinical & Medical Imaging 1.
  29. Tsunoda A, Okuda O, Sato K (1997) MR height of the pituitary gland as a function of age and sex: Especially physiological hypertrophy in adolescence and in climacterium. AJNR Am J Neuroradiol 18: 551-554.
  30. Cordeiro MH, Kim S-Y, Woodruff TK (2015) Chapter 1 - Ovarian follicle biology and the basis for gonadotoxicity. in: anderson ra, spears n, editors. cancer treatment and the ovary. Boston, Academic Press 3-20.
  31. Xiao X, Mruk DD, Wong CKC, Cheng CY (2014) Germ cell transport across the seminiferous epithelium during spermatogenesis. Physiology 29: 286-298.
  32. Durairajanayagam D, Rengan AK, Sharma RK, Agarwal A (2015) Sperm biology from production to ejaculation. Unexplained Infertility 29-42.
  33. Wu S, Yan M, Ge R, Cheng CY (2020) Crosstalk between sertoli and germ cells in male fertility. Trends Mol Med 26: 215-231.
  34. Richard FJ, Tsafriri A, Conti M (2001) Role of phosphodiesterase type 3A in rat oocyte maturation. Biol Reprod 65: 1444-1451.

Citation

Tammasse IFU, Tamrin F (2023) Different of Hypothalamic-Pituitary-Gonadal Axis in Male and Female. Reprod Med Int 6:023. doi.org/10.23937/2643-4555/1710023