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Effects of 5α-Androst-16-en-3α-ol on the pulsatile secretion of luteinizing hormone in human females

Authors:
Kazuyuki Shinohara at Nagasaki University
Kazuyuki Shinohara
M Morofushi
M Morofushi
M Morofushi
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Toshiya Funabashi at St. Marianna University School of Medicine
Toshiya Funabashi
Dai Mitsushima at Yamaguchi University
Dai Mitsushima
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Abstract

We examined the effects of 5alpha-androst-16-en-3alpha-ol (3alpha-androstenol) on pulsatile luteinizing hormone (LH) secretion in human females. The frequency of the LH pulse in the follicular phase was decreased by exposing the women to 3alpha-androstenol.
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SHORT REPORT
Effects of 5α-Androst-16-en-3α-ol on the Pulsatile Secretion of Luteinizing
Hormone in Human Females
Kazuyuki Shinohara, Masayo Morofushi, Tosihya Funabashi, Dai Mitsushima and
Fukuko Kimura
Department of Physiology, Yokohama City University School of Medicine, 3–9 Fukuura,
Kanazawa-ku, Yokohama 236-0004, Japan
Correspondence to be sent to: Kazuyuki Shinohara, MD, PhD, Department of Physiology, Yokohama City University School of Medicine,
3–9 Fukuura, Kanazawa-ku, Yokohama 236-0004, Japan. e-mail: Kazuyuki @ med.yokohama-cu.ac.jp
Abstract
We examined the effects of 5α-androst-16-en-3α-ol (3α-androstenol) on pulsatile luteinizing hormone (LH) secretion in
human females. The frequency of the LH pulse in the follicular phase was decreased by exposing the women to
3α-androstenol.
Introduction
Menstrual synchrony, the convergence of the onset date
of the menstrual flow, is observed in women living to-
gether (Weller and Weller, 1993). Menstrual synchrony has
been shown to be mediated by axillary odour (Stern and
McClintock, 1998). Axillary odours from women in the
follicular phase (FP) of the ovulatory cycle shorten both
the time to ovulation and the length of the menstrual cycle
in the recipients whereas axillary odours in the ovulatory
phase (OP) delay ovulation and lengthen the menstrual
cycle. However, the pheromones in the axillary compounds,
which regulate both the time to ovulation and the length of
the menstrual cycle, have not hitherto been identified.
When we examined the relationship between menstrual
synchrony and the ability to smell a putative pheromone,
5α-androst-16-en-3α-ol (3α-androstenol), the women who
showed menstrual synchrony had a high sensitivity to 3α-
androstenol (Morofushi et al., 2000). It is therefore possible
to speculate that human females use 3α-androstenol to syn-
chronize their menstrual cycles. We recently reported that
axillary compounds in the FP increased the frequency of
pulsatile secretion of luteinizing hormone (LH) and axillary
compounds in the OP decreased it, suggesting that axil-
lary compounds change the length of the menstrual cycle
by changing the frequency of the pulsatile LH secretion
(Shinohara et al., 1999). In the present study, we examined
the effect of 3α-androstenol on the pulsatile secretion of LH
to explore the possibility that 3α-androstenol is one of the
active substances in axillary compounds which regulate the
length of the menstrual cycle.
Materials and methods
Eleven female college students, aged 19–25 years and with a
history of regular ovulation, were involved in this study.
From 10:00 to 18:00 on days 5–7 after the menstrual onset,
blood samples were collected through an i.v. heparin-locked
catheter at 10 min intervals. The subjects took 100 kcal
isocaloric snacks and 100 ml water hourly for 8 h. They were
not exposed to anything for the first 4 h. Afterwards,
2.5 mM 3α-androstenol in 70% isopropyl alcohol (IA)
was applied hourly to half of them by wiping above their
upper lip with a pad containing the solution for the next
4 h. IA alone was applied to the others in a similar way to
3α-androstenol. Blood plasma was separated by centri-
fugation at 2000 g for 10 min and stored at –30°C until the
LH assay (SAPC-S LH RIA kit; Daiichi Radioisotope
Laboratory, Tokyo, Japan). The mean of the minimally
detectable amount of LH was ~0.3 mIU/ml. The intra-assay
coefficients of variation (CV) which were calculated on
the basis of duplicated measurement of pooled samples
containing 7.78 and 42.1 mIU/ml were 4.17 and 0.66%,
respectively. An LH pulse was defined as when both the
ascending and descending CVs were >1.7 times the intra-
assay CV. The protocol observed the tenets of the Declaration
of Helsinki and was approved by the Ethics Committee
of Yokohama City University. The subject gave written
© Oxford University Press 2000
Chem. Senses 25: 465–467, 2000
informed consent after the procedures had been fully
explained.
Results
As seen in a representative subject (Figure 1a), the intervals
between consecutive peaks of pulsatile LH secretion were
70, 70 and 70 min before the application of 3α-androstenol,
but after the start of the application the intervals became
longer: 90 and 80 min. On the other hand, IA alone had no
effect on the interpulse intervals: 60, 60 and 50 min before
IA application and 60, 60 and 60 min during the application
(Figure 1b). The mean (± SE) interpulse interval between
LH pulses (n = 6) was significantly (P < 0.05, paired t-test)
increased from 53.9 ± 3.9 to 66.0 ± 1.5 min in response to
3α-androstenol. No change in the mean interpulse interval
between LH pulses was observed in response to IA (P >
0.05, paired t-test). The mean interpulse intervals between
LH pulses (n = 5) before IA application and during the
application were 54.0 ± 4.9 and 53.8 ± 4.7 min, respectively.
The data were expressed as the frequency are shown in
Table 1. 3α-Androstenol decreased the frequency while IA
alone had no effect.
Discussion
The present results demonstrate that the frequency of
pulsatile secretion of LH is decreased by exposing women to
3α-androstenol. This finding indicates that 3α-androstenol
retards the growth and maturation of ovarian follicles and
consequently delays the timing of ovulation. It is therefore
possible that 3α-androstenol is involved in menstrual syn-
chrony by increasing the period of menstrual cycles.
3α-Androstenol is known to be secreted from the axillae
in humans (Gower and Ruparelia, 1993). The steroid has
been demonstrated to act as a pheromone in pigs (Gower
and Ruparelia, 1993). It is secreted in the saliva of the
boar and acts as a pheromone effective in eliciting the
characteristic immobilization response of the estrous sow
to the advance of her mate (Gower and Ruparelia, 1993).
(Z)-7-Dodecen-1-yl acetate is used as a pheromone by the
females of more than 126 species of insects and the elephant
(Rasmussen et al., 1996). 3α-Androstenol has been reported
as affecting women’s mood (Gower and Ruparelia, 1993)
and sexual arousal (Gower and Ruparelia, 1993), so it also
may not be a species-specific pheromone.
Furthermore, women whose menstrual cycles became
synchronized with that of room-mates within 3 months had
higher olfactory acuity for 3α-androstenol than non-
synchronized women, suggesting that the ability to perceive
the odour emitted by 3α-androstenol is related to the men-
strual synchrony (Morofushi et al., 2000). We recently
showed that the frequency of the LH pulse was increased by
axillary compounds in the FP, which shorten the menstrual
cycle, and decreased by axillary compounds in the OP, which
lengthen it (Shinohara et al., 1999). Together with these
findings, the present results suggest that 3α-androstenol may
be a pheromone included in axillary compounds secreted in
the OP, which lengthen the menstrual cycle.
References
Gower, D.B. and Ruparelia, B.A. (1993) Olfaction in humans with special
reference to odorous 16-androstenes: their occurrence, perception and
possible social, psychological and sexual impact. J. Endocrinol., 137,
167–187.
Figure 1 Representative examples of the effect of 3α-androstenol (a) and
isopropyl alcohol (b) on pulatile LH secretion.
Ta b le 1 Effects of 3α-androstenol and isopropyl alcohol on the
frequency (the number of pulses/4 h) of LH pulses
3α-Androstenol Isopropyl alcohol
Before application 4.57 ± 0.81 (6) 4.59 ± 0.88 (5)
During application 3.64 ± 0.21 (6) 4.59 ± 0.83 (5)
Data are the mean ± SE. Numbers in parentheses indicate the number of
subjects.
466 K. Shinohara et al.
Morofushi, M., Shinohara, K., Funabashi, T. and Kimura, F. (2000)
Positive relationship between the menstrual synchrony and ability to
smell 5α-androst-16-en-3α-ol, Chem. Senses, in press.
Rasmussen, L.E.L., Lee, T.D., Roelofs, W.L., Zang, A., and Davis, G.D.
(1996) Insect pheromone in elephants. Nature, 379, 684.
Shinohara K., Morofushi M. and Kimura, F. (1999) Effects of human
pheromones on pulsatile luteinizing hormone secretions. Neurosci. Res.,
Suppl. 23, S233.
Stern, K. and McClintock, M.K. (1998) Regulation of ovulation by human
pheromones. Nature, 392, 177–179.
Weller, A. and Weller, L. (1993) Human menstrual synchrony: a critical
assesment, Neurosci. Biobehav. Rev., 17, 427–439.
Accepted May 17, 2000
Effect of 5αAndrost-16-en-3αol on LH Secretion 467
... This type of chemical signal provides information about gender and reproductive status, mediates social and sexual behaviors, and alters neuroendocrine processes (Spehr et al., 2006). The most commonly used putative pheromone substances are estratetraenol (Estr) (Vermetten and Bremner, 2003;Hare et al., 2017;Oren and Shamay-Tsoory, 2019;Ye et al., 2019) and 5α-androst-16-en-3α-ol (Andr) (Morofushi, 2000;Shinohara, 2000;Jahanfar et al., 2007). Pheromone perception in humans is much debated, and researchers have yet to report positive results to detect a conscious perception of pheromones in humans, especially for physical attraction (Black and Biron, 1982). ...
... In this study the "Hugvie" mediums were stored in the laboratory in three different plastic containers (i.e., Box N-Neuter; Box E-Estr, and Box A-Andr), inside which, for each condition, four vials with different substances were inserted, as described below. All the vials were placed with the cap off but were not in contact with the embodied medium's fabric (Morofushi, 2000;Shinohara, 2000). Before starting the experimental protocol, the Hugvie were stored in the boxes for 2 weeks, at a constant temperature in the laboratory maintained at 21 • centigrade. ...
Perception of Social Odor and Gender-Related Differences Investigated Through the Use of Transfer Entropy and Embodied Medium
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The perception of putative pheromones or social odors (PPSO) in humans is a widely debated topic because the published results seem ambiguous. Our research aimed to evaluate how cross-modal processing of PPSO and gender voice can affect the behavioral and psychophysiological states of the subject during a listening task with a bodily contact medium, and how these effects could be gender related. Before the experimental session, three embodied media, were exposed to volatilized estratetraenol (Estr), 5α-androst-16-en-3 α-ol (Andr), and Vaseline oil. The experimental session consisted in listening to a story that were transmitted, with a male or female voice, by the communicative medium via a Bluetooth system during a listening task, recorded through 64-active channel electroencephalography (EEG). The sense of co-presence and social presence, elicited by the medium, showed how the established relationship with the medium was gender dependent and modulated by the PPSO. In particular, Andr induced greater responses related to co-presence. The gender of the participants was related to the co-presence desire, where women imagined higher medium co-presence than men. EEG findings seemed to be more responsive to the PPSO–gender voice interaction, than behavioral results. The mismatch between female PPSO and male voice elicited the greatest cortical flow of information. In the case of the Andr–male voice condition, the trained model appeared to assign more relevance to the flow of information to the right frontotemporal regions (involved in odor recognition memory and social behavior). The Estr–male voice condition showed activation of the bilateral frontoparietal network, which is linked to cognitive control, cognitive flexibility, and auditory consciousness. The model appears to distinguish the dissonance condition linked to Andr matched with a female voice: it highlights a flow of information to the right occipital lobe and to the frontal pole. The PPSO could influence the co-presence judgements and EEG response. The results seem suggest that could be an implicit pattern linked to PPSO-related gender differences and gender voice.
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... Hence, the reported effects that do exist in the literature could be explained by perceptual differences between the experimental and control stimuli. Besides the behavioral effects men-tioned above, androstenol has also been suggested as a potential regulator of the menstrual synchrony phenomena that will be reviewed below (Shinohara, Morofushi, Funabashi, Mitsushima, & Kimura, 2000). ...
... As mentioned above, an androgen has been implicated as the active compound. 5androstenol (androstenol) decreases the luteinizing hormone (LH) pulse 4 , thus serving as a regulatory compound (Shinohara et al., 2000). Women seem to emit pheromone-like compounds that have the capacity to regulate the menstrual cycle of receiving women in a non-conscious way by regulation of the LH pulse (Shinohara, Morofushi, Funabashi, & Kimura, 2001); hence classifying as evidence of human pheromonal communication akin to the priming pheromones in rodents. ...
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... For example, they activate certain regions of the brain, particularly the limbic system (Sobel et al., 1999) and influence social behavior (Cowley and Brooksbank, 1991;Cutler et al., 1998;Grosser et al., 2000). They also regulate ovulation (Stern and McClintock, 1998), as well as physiological parameters such as serum levels of testosterone, luteinizing hormone (LH) and follicle stimulating hormone (FSH) and, in a sex-specific manner, respiration and heart rate (Monti-Bloch et al., 1998;Shinohara et al., 2000). ...
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... One such pheromone-like compound, androstadienone (AND), has been found consistently in male axillary sweat [11,12]. This compound, and estratetraene (EST), a molecule found in female human secretions, have been found to effect neural activity [13][14][15]. This has led investigators to propose AND, EST, and other similar steroid molecules as potential candidates for human pheromones [16,17]. ...
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Preprint
Full-text available
  • Sep 2020
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... There are also abundant sebaceous glands on the back and chest, and their secretory fluids contain steroid compounds [14]. Previous studies involving olfactory experiments in which subjects were exposed to steroid compounds suggested that the steroid compounds were involved in changes in human cognitive function and endocrine response [18][19][20]. Estratetraenol (EST), an estimated pheromone secreted by women, is one of the steroidal compounds [21,22]. EST helps men feel more feminine to women [21,22]. ...
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... Other scientists have also shown that natural compounds from the axillary region of humans can trigger in women neuroendocrine responses such as altered timing of the preovulatory LH surge (McClintock, 2000;Stern and McClintock, 1998) and altered pulse frequency (Preti et al., 2003;Wysocki and Preti, 2004). 3α-androstenol (which together with 5α-androstenone have been shown to act as releasers, that elicit the characteristic immobilisation response of oestrous sows) is proposed to be an axillary pheromonal component that is associated with the altering LH pulsing in women (Morofushi et al., 2000;Shinohara et al., 2000). The effective steroid dose (2.5 mM) tested by Shinohara and co-workers is, however, rather high for a putative pheromone. ...
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Pheromones, Odors, and VasanasThe Neuroendocrinology of Social Chemosignals in Humans and Animals
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  • Dec 2002
Social chemosignals are not simply vestigial. Rather, they are the oldest sensory system for coordinating social and reproductive behavior. Because they are evolutionarily conserved, they are a parsimonious system for integrating social interactions, emotions, and motivation in a variety of physical contexts and endocrine states. Hormones play a role in three ways: they change the meaning of an odorant, often without changing sensitivity or acuity; hormones are regulated by social odors and pheromones; hormones are social chemosignals themselves, functioning as odors, pheromones, and vasanas. Including humans in the comparative psychology and neuroendocrinology of social chemosignals provides animal research with a rich framework for addressing the relationship among perception, psychological responses, and levels of awareness. The animal literature brings precise insights into neuroendocrine mechanisms of production and response. It also brings a heightened appreciation of the diversity of ways that the same social function can be achieved.
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Insect pheromone in elephants [5]
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  • Mar 1996
(Z)-7-dodecen-1-yl acetate is used by the females of more than 126 species of insects, especially Lepidoptera, as part of their pheromone blends to attract insect males. Female Asian elephants, Elephas maximus, also use a pheromone to signal to males their readiness to mate. This pheromone is released in their urine during oestrus and before ovulation. We have now isolated this compound by bioassay¬ guided fractionation and purification. Remarkably, it is the same compound, (Z)-7-dodecen-1-yl acetate, used by insects including the cabbage looper, tomato looper, silver Y and turnip moths, the dingy cut¬ worm, and the sugarcane stalk borer.
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Positive relationship between menstrual synchrony and ability to smell 5α-androst-16-en-3α-ol
Article
Full-text available
  • Sep 2000
To explore the possibility that compounds which were identified as pheromones in experimental animals mediate human menstrual synchrony, we examined the relationship between menstrual synchrony and the ability to smell putative pheromones, 5alpha-androst-16-en-3alpha-ol (3alpha-androstenol) and 5alpha-androst-16-en-3-one (5alpha-androstenone). When we examined menstrual synchrony among 64 women living together in a college dormitory, we found that 24 (38%) of them became synchronized with room-mates in 3 months. Afterwards, dilution series of 3alpha-androstenol and 5alpha-androstenone and the control odorant (pyridine) were presented to the 64 women and sensitivity to the odors was compared between synchronized and non-synchronized women. No difference was found between the two groups of women in the detection threshold for pyridine, indicating that general olfactory ability did not differ between them. The detection threshold for 3alpha-androstenol of synchronized women was significantly lower than that of non-synchronized women, but no difference in the threshold for 5alpha-androstenone was found between synchronized and non-synchronized women. These results indicate that the women who showed menstrual synchrony had a higher sensitivity to 3alpha-androstenol but not necessarily to 5alpha-androstenone.
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Regulation ovulation by human pheromones
Article
  • Mar 1998
Pheromones are airborne chemical signals that are released by an individual into the environment and which affect the physiology or behaviour of other members of the same species. The idea that humans produce pheromones has excited the imagination of scientists and the public, leading to widespread claims for their existence, which, however, has remained unproven. Here we investigate whether humans produce compounds that regulate a specific neuroendocrine mechanism in other people without being consciously detected as odours (thereby fulfilling the classic definition of a pheromone). We found that odourless compounds from the armpits of women in the late follicular phase of their menstrual cycles accelerated the preovulatory surge of luteinizing hormone of recipient women and shortened their menstrual cycles. Axillary (underarm) compounds from the same donors which were collected later in the menstrual cycle (at ovulation) had the opposite effect: they delayed the luteinizing-hormone surge of the recipients and lengthened their menstrual cycles. By showing in a fully controlled experiment that the timing of ovulation can be manipulated, this study provides definitive evidence of human pheromones.
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Human menstrual synchrony: A critical assessment
Article
  • Feb 1993
  • NEUROSCI BIOBEHAV R
This review on menstrual synchrony in human females has four purposes: (a) to determine whether or not the phenomenon exists, and whether it differs in the various groups studied: roommates in dormitories, roommates in private residences, close friends, work groups, mothers-daughters; (b) to assess the magnitude of its effect, i.e., to what extent does the single factor of living together affect menstrual synchrony?; (c) to examine the effects of menstrual-related factors, social interaction factors, and personality on menstrual synchrony; (d) to assess whether the findings support a pheromonal or common environmental explanation of menstrual synchrony. Several methodological issues are also discussed.
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Effects of human pheromones on pulsatile luteinizing hormone secretions
  • Jan 1999
  • K Shinohara
  • M Morofushi
  • F Kimura
Shinohara K., Morofushi M. and Kimura, F. (1999) Effects of human pheromones on pulsatile luteinizing hormone secretions. Neurosci. Res., Suppl. 23, S233.