By Injecting Female Animals With Estrogen, Researchers Can Increase the Animals'

Int J Biol Sci. 2008; iv(3): 126–132.

Sex Hormones' Regulation of Rodent Physical Activity: A Review

Received 2008 Mar 12; Accepted 2008 Apr 24.

Abstract

There is a large body of emerging literature suggesting that physical activeness is regulated to a varying extent by biological factors. Available animal data strongly suggests that there is a differential regulation of physical activity by sex and that the majority of this differential regulation is mediated by estrogen/testosterone pathways with females in many animal species having higher daily activity levels than males. The purpose of this manuscript is to review the mechanisms by which estrogen, progesterone, and testosterone affect the regulation of physical daily activity. This review lays the foundation for future investigations in humans likewise every bit discussions near relative disease risk mediated past differential biological regulation of physical activity past sex.

Keywords: estrogen, testosterone, progesterone, mammals, mice, physiology

I. Introduction

The use of animal models as proctors for homo physiology has a long and meaning history. Subsequently, some researchers have turned to using brute models to increase agreement of the mechanistic underpinnings of practise behaviors. This work is disquisitional given the literature that indicates a general decline in physical activity 50 and an increase in obesity and other hypokinetic diseases in most Western-cultures 27. While physical activeness has ordinarily been considered a 'voluntary activeness', held to complimentary-volition and influenced solely past ecology factors there is a growing body of literature that suggests that physical action is significantly regulated by biological factors. These biological regulating factors may take many forms including a cardinal nervous centre-located "action-stat" 38, an increase or decrease in various physiological substance or structures (due east.grand. GLUT4 ref. 51), and/or genetics 23 , 25 , 46. Biologically, the sex hormones play a large function in regulating diverse physiological parameters in both males and females and thus would be the natural bailiwick of investigations into possible roles they play in regulating physical action. Therefore, the focus of this newspaper is to review the literature investigating the consequence of and the physiological mechanisms through which estrogen, progesterone, and testosterone may regulate concrete action. Given the sparseness of the human being literature in this area, the primary model used in this research has been animal models.

II. Sex activity differences in concrete action

In general, information technology is commonly accepted that human females are less agile than males; this sexual practice differentiation in activity is prevalent in both children and adolescents 31 besides as adults 50. However, confounding factors in human research in this area, including the well-known difficulty of accurately measuring physical activity in large populations 42, the complexity of giving hormone treatments in a physiologically-relevant and upstanding way 52, the full general lack of well-controlled prospective human studies in this area, and the nigh impossibility of controlling ecology variations that can influence activity levels make understanding human sex differences in activity extremely problematic. Given these difficulties and the relative ease of experimental control in creature studies, information technology is appropriate to consider whether in that location is a sex activity difference in activeness present in animal models.

The rodent literature that addresses sex hormone effects on activeness generally shows that female person rodents are more active than male rodents. Figure 1 is a summary of representative literature that has observed sex differences in daily activity in rats or mice. Overall, female rodent activity levels on a daily basis range from 20% to over fifty% higher than males. Bronstein, et al. 6 observed that female Sprague-Dawley rats traversed significantly more distance during open-field testing (ranging from 28-46% more) than male rats, regardless of whether the animals had been handled or not. Craft, et al. 8 while because sexual activity differences in morphine-induced locomotor changes, observed that in the baseline state, female person Sprague-Dawley rats exhibited 46% - 72% more activity (as measured by photobeam breaks in their home cage) than males over a iii-5 hour period, depending upon whether they had been handled or not. Li, et al. 24 showed that there may be strain differences in these sex-related patterns of action by showing that while the full path length that Wistar and WKY rats ran were significantly higher in females, in that location were no observed differences between sexes in the SHR rats. An before strain screen written report in mice 25 showed that while overall female mice ran approximately 20% further per day than male mice, there was large variability in this percentage depending upon which of the 13 strains were tested. The percentage difference between female person and male mice of the aforementioned strain in distance run on a daily basis ranged from -21.nine% (SPRET/EiJ) to 111.2% (C3H/HeJ). Like variation was likewise observed in duration and speed phenotypes. This type of between strain variation in photobeam interruption activity information has likewise been observed by Seburn within the Mouse Phenome database 41. Earlier work by Koteja, et al. 21 monitored bicycle running activity in both control Hsd:ICR mice and mice from generation 10 of an ongoing study to selectively breed mice for bike-running activity. While there were meaning differences between the control and selected lines in daily bike-running activity, there were also significant sex-differences in the amount of altitude run reported in both the control lines (50% higher in females) and the selected lines (58% higher in females). Recent work from our laboratory 26 with a large cohort of F2 animals (due north=310) adult from reciprocally breeding high active C57L/J and low active C3H/HeJ inbred mouse strains have shown that on average (over 21 days), the female animals ran 47% further, 39% longer, and 9% faster than male person animals.

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Representative literature reporting percentage difference in female activity vs. male activity in rodents.

In summary, the majority of the animal literature over the by 80 years, take largely accepted that concrete activity tin can exist governed by biological factors and thus, activity levels are routinely treated as the dependent variable in many report designs. Additionally, given that most ecology factors can be controlled when using animal models, the animal literature has accordingly focused upon the office that sexual activity hormones play in regulating daily activity, every bit Gorzek, et al. fifteen did in investigating the effect of estrogen on daily activity levels.

Iii. Effects of sex activity hormones on activity in animal models

The investigation of the effect of sex hormones on physical activity in rodent models has a long and varied history. Effigy ii (R. Bowen personal communication) shows the interesting waxing and waning of such research over the past 80 years. While a consummate historical review of this topic is exterior the scope of this newspaper, it is of notation that the consideration of sexual practice hormone furnishings on activeness was initiated in the early on 1920's when it was found that ovariectomies significantly decreased activity in female person rats in conjunction with the observation of a marked decrease in cycle-running action in male person rats subsequently castration eighteen , 35 , 44. These studies also noted that implantation of ovarian tissue into both female rats 35 , 44 and male rats 54 'recovered' the pre-neutering activity patterns whereas implantation of testes into both male and female rats increased activity to a lesser extent than the ovarian implants 36. The testify from these studies, produced earlier estrogen, progesterone, or testosterone were isolated and identified, were so potent that 1 researcher ended that in female rats, "Plain, therefore, the spontaneous activity is dependent on ovarian role". Nonetheless, this aforementioned researcher cautioned that none of the available experiments proved that the "hormone actually produces action" (their emphasis) 35.

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The yearly distribution of studies regarding the issue of sex hormones on physical activity. The x-centrality designates the x-yr period in which the studies were published. (Personal communication from R. Bowen)

Several studies since these early findings have shown that estrogen and testosterone directly impact spontaneous activity in rodent models. For case, recently Gorzek and colleagues xv showed that while ovariectomies reduced daily bike-running activity in female person mice, a dosage of iii µg•d-1 of 17β-estradiol increased activity to a level comparable to activity in sham-operated mice. Roy and Wade 39 demonstrated that administration of varying doses of testosterone propionate (100µg-1mg/day) increased running bicycle activity in castrated male rats. These 2 studies, which are 2 examples of numerous studies, provide prove of a crusade/effect human relationship betwixt reproductive hormones and spontaneous activity in rats and mice.

Estrogen

While several studies take observed a causal relationship betwixt the sex hormones, peculiarly estrogen, and spontaneous activity, the mechanistic underpinnings of this relationship has been somewhat unclear. Cushing, in a series of experiments (summarized past ref. 9), investigated the function of sexual receptivity on the relationship between estrogen and activity using prairie voles. Female prairie voles, dissimilar other female rodents, are unique in that they undergo induced estrus by exposure to male voles and their sexual receptivity does non require progesterone, thus, removing two possible confounding factors that might influence activity. Cushing and Hite 9 found that sexually mature virgin female person voles did not increase seven-day wheel running behavior either with or without estradiol injections (0.05µg or 0.5µg estradiol). It had been earlier shown that the number of estradiol receptors in the encephalon had previously been shown to increase in female person voles when exposed to males 7. Thus, the observation of a the lack of an increase in spontaneous activeness with estradiol administration earlier exposure to males suggested that estradiol's effect on spontaneous activity was linked to the increased number of estradiol receptors in the brain.

Almost research investigating the mechanisms of estrogenic increases in activity have focused on central neural pathways 12 , 13 , 30. Bilateral implantation of estradiol in the medial preoptic area and the anterior hypothalamus was shown to variably increase wheel running action in ovariectomized female rats 12. Since the preoptic area contains both estrogen receptor isoforms - alpha (ERα) and beta (ERβ) – while the hypothalamic areas contain primarily ERα and trivial if any ERβ 43, Fahrbach, et al. 12 suggested that ERα may control the estrogenergic upshot on activity. This hypothesis was difficult to test since 17β-estradiol has a like affinity for both ERα and ERβ receptor subtypes 22.

Coumesterol is a phytoestrogen with similar affinity as 17β-estradiol for ERβ, simply four-fold less affinity for ERα and seven-fold higher affinity for ERβ than for ERα 22. Garey and colleagues 13 injected coumestrol (x µg), singly and in combination with estradiol implants (2.5µg) in 48 adult, ovariectomized Swiss-Webster mice and measured running wheel activeness for the following x days. Running wheel activity increased with estradiol administration (Fig. 3), but coumestrol administration did not alter running bicycle behavior as compared to a placebo injection. From this data, the authors suggested that the ERβ-pathway did not influence spontaneous activity; rather, the increases in spontaneous activity arising from estrogen administration were mediated primarily through the ERα pathway. Additionally, Garey, et al.'s information as well eased concerns that the phytoestrogens in the standard rodent chows that have been used in many of the published rodent activity papers (e.g. 20 , 21 , 23 , 25 , 47 , 48 , 53) have not confounded the conclusions of these studies as has been noted for other areas of rodent physiology (eastward.thou. 45).

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Bicycle running behavior afterwards five days of phytoestrogen supplementation. *Significantly different from vehicle/placebo handling. Drawn from tabular data presented by Garey, et al. 13.

Garey and colleagues' xiii suggestion that the estrogen-induced increases in spontaneous activity are mediated through the ERα pathway has been supported past further experiments with knock-out animals. Ogawa, et al. 30, using gonadectomized knock-out mice that lacked either ERα or ERβ genes, implanted either a 17β-estradiol sheathing (16 or 160 ng/d) or a placebo capsule and monitored running wheel action for 9 days. Ogawa and colleagues observed that both male and female wild-type mice (i.east. with ERα and ERβ pathways intact) increased running wheel activity significantly with either 16 or 160 ng/d estradiol treatments as compared to placebo mice. Additionally, with estradiol treatments, both sexes of the ERβ knock-out mice also significantly increased their running wheel activity compared to placebo; all the same, even with estradiol administration, the ERα knock-out mice did not increase activity compared to placebo. These results, in conjunction with Garey, et al.'s earlier written report on coumesterol thirteen lend strong evidence to the hypothesis that the estrogenic effects on running wheel behavior in mice are mediated through the ERα-pathway.

While it appears that estrogenic activation of the ERα-pathway is the main mediator of the increase in running wheel behavior, the mechanisms through which the ERα-pathway influences activity are unclear. Morgan, et al. 28 have speculated that the ERα-pathway modulates several neurotransmitters, including dopamine and/or serotonin, which may play a role in the regulation of activity. In a review of the interactions of the sex differences in dopaminergic regulation, Becker 3 proposed that in female rats, estrogen enhanced final release of dopamine relative to male rats, which explains, the authors note, many reproductive-related behaviors such equally increased pacing behavior. Additionally, it has been observed that estrogen tin regulate several different steps in dopaminergic functioning, including dopamine release and metabolism as well as the pre- and post-synaptic receptor and transporter operation (for review come across 10). Interestingly, effects of estrogen on dopamine receptors and transporter mechanisms in the nucleus accumbens have been noted to be as fast as two minutes; faster than would be expected from genomic activation 49 suggesting an influence of estrogen on the dopaminergic systems not arising through activation of either the ERα or ERβ pathways. Supporting this nongenomic activation hypothesis are observations of nongenomic furnishings of estrogens postulated to occur through the activation of a mutual membrane binding site with the same pharmacological profile as the hypothesized γ-adrenergic receptor 29.

Whether a differential activation of the dopaminergic systems by the ERα pathway or some other nongenomic pathway leads to the sex-related difference in action levels is currently unknown. Still, the involvement of dopamine in regulating daily activity is supported past indirect prove. Garland's group 33 , 34 have suggested that an alteration in dopaminergic functioning is ane of the primary characteristics of mice experimentally evolved for high activity. Specifically, Rhodes and Garland accept observed that an inhibition of dopamine transporter (DAT) will reduce the wheel-running of mice that are high agile 34. Additionally, they have shown that female high agile mice have a reduced functioning of the D1 and D5 dopamine receptors 33. Whereas Rhodes and Garland merely studied female mice in each of their studies, it is yet to be determined if these alterations in dopaminergic functioning are different in male high active mice. Thus, while tenuous evidence suggests that the estrogen activation of the ERα-pathway and a possible nongenomic pathway may lead to an enhanced release of dopamine in female person rodents which coupled with alterations in dopamine ship and/or receptors, may pb to increased activeness, it is unclear whether this results in differential levels of activeness between sexes.

Progesterone

While there take been numerous investigations of estrogen's function in determining physical activity levels in animal models, there take been virtually no studies considering whether progesterone influences activity. Progesterone is known to impact several physiological mechanisms and given that estrogen and progesterone normally cycle together during at to the lowest degree one portion of the female reproductive cycle 16, progesterone could too affect activity behavior. In a larger study concentrating on the differential effect of estradiol and estrone on activity, Young and Fish 55 noted that progesterone injected in conjunction with estradiol did non influence activity in rats in any manner. This event was expanded upon in a three-phase study conducted by Rodier 37 which is the only other currently bachelor study in this area. Sherman albino rats received varying dosages of progesterone (4, 8, or twoscore mg/kg/24-hour interval) or placebo injections. Rodier noted that injections of 8 or 40 mg/kg/day in gonadally-intact rats decreased normal wheel-running activeness, just neither an injection of iv mg/kg/solar day progesterone or placebo solvents changed normal action levels. Rodier and then ovariectomized seven of the rats, injected them with 40 mg/kg/day progesterone for six days and then injected them with solvent for another 6 days. After ovariectomy, activity decreased to a level similar to that seen with progesterone injection in intact animals and was not farther depressed with subsequent progesterone injection suggesting that progesterone was interfering with endogenous estrogens' furnishings on physical activity. To make up one's mind if exogenous estrogen interacted with the progesterone inhibition of cycle-running activity, Rodier then injected 17β-estradiol (100 µg/kg) into the ovarectomized and control animals, with each injection separated by v days. 8 days afterwards the final estradiol injection, he injected either progesterone (40 mg/kg/day) or a placebo. While the estrogen injections increased the animals' running wheel behavior for at to the lowest degree 21 days after the beginning injection, the animals receiving the progesterone injections sharply decreased their activity, which and then increased again after the cessation of the progesterone injections. Thus, given that either intrinsic or extrinsic estrogen had to exist present for the inhibitory effects of progesterone to be observed, Rodier suggested that the progesterone decrease in physical action was mediated through a direct interference with estrogen. A negative interference of progesterone on estrogenergic effects on neurotransmitters has been observed in both rats 17 and primates fourteen; conversely, there is too literature available suggesting that progesterone augments 4 or has no effect 2 on estrogenic effects on neurotransmitters. However, an interference of progesterone on estrogen's physical activeness furnishings is bonny to hypothesize considering such an interference would explain the common sinusoidal activity blueprint observed in female person rats 35; information technology could be suggested that height activeness was occurring during the follicular phase due to the primacy of the estrogen height with the subsequent decrease in physical activity occurring during the luteal stage when progesterone is the dominant hormone and is interfering with estrogen's activeness increasing effects. The famine of investigations in this expanse leaves this and other hypotheses related to progesterone and estrogen's interactions on activity, such as the role of physiological doses of progesterone in activity regulation and the specific site(southward) and machinery(southward) of the estrogen/progesterone interference open for further investigation.

Testosterone

In rodents, several studies using orchidectomized males accept indicated a potential role for sex hormones in the regulation of activeness 5 , 36 , 39. For instance, Broida and Svare 5 showed that locomotor activeness – measured past photobeam breaks - could be rescued in castrated animals by implanting silastic capsules containing testosterone. Additionally, Broida and Svare suggested that in that location may be a genotype dependency in these responses, since they observed a larger decrement in physical action after castration in inbred C57BL/6J mice as compared to inbred DBA/2J and random-bred Rockland-Swiss mice 5.

While a possible role for testosterone in the regulation of daily activity has been proposed five , 36 , 39, few studies accept attempted to determine mechanistic causes of this effect. Roy and Wade 39 in a widely quoted study, injected either testosterone (100 µg/day), estradiol (x µg/twenty-four hours), dihydrotestosterone propionate (DHTP - 100 µg/day), or sesame oil (placebo) into 20 castrated adult male person Sprague-Dawley rats and then monitored running wheel activeness for 16 days. They noted that testosterone injections significantly increased the running wheel activity of the rats (p<0.05) but not every bit much as estradiol injections (p<0.02). Neither the DHTP or placebo injections increased running action above baseline. Given that testosterone is aromatizable to estrogen whereas DHTP is not, the authors concluded that the primary mechanism regulating running wheel activity with testosterone assistants was the aromatization of the testosterone into estrogen. In the 2d part of this experiment 39, these authors found that administration of an estrogen antagonist (MER-25) attenuated the increased running cycle activity resulting from either estradiol or testosterone injection. These results further supported the hypothesis that the increased activeness from testosterone injection was mediated by the estrogen pathways.

While it appears that testosterone injections/implants can rescue action levels after orchidectomy, supplementation of testosterone in intact animals does not increase concrete action levels. Eleftheriou and colleagues observed that testosterone level was not significantly correlated to a unmarried 24 60 minutes observation of wheel-running activeness 11 in gonadally intact male C57BL/6By and Balb/cBy mice, in seven recombinent inbred strains (CXBD, CXBE, CXBG, CXBH, CXBI, CXBJ, and CXBK) or in two Fane hybrid strains (B6CF1 and CB6F1). Salvador, et al. 40 showed that suprapharmacological doses (three.75, seven.5, 15, or 30 mg/kg) of artificial anabolic-androgenic steroids (testosterone propionate and nandrolone decanoate), injected into gonadally intact male OF1 male mice, did not affect running wheel activeness measured 24 hours after the injection. Furthermore, mice injected with suprapharmacological doses for x weeks, did not show alterations in action levels compared to baseline during 24 hour monitoring periods in the eight, ninth, or tenth week. These results support work in rats by Li and Huang 24 that showed that testosterone injections in both male and female gonadally-intact animals did non generally effect in an increment in total path length. Thus, while work in gonadally-scarce animals has shown that testosterone, afterward aromatization to estrogen, will increment physical activeness levels in rodents, supplementation to a higher place baseline levels will not further increase activity.

V. Summary

A broad-variety of prove suggests that in rodents, females are generally more agile than males, with a large proportion of this differential activeness explained by sex hormone furnishings. The mechanism of this regulation (Fig. 4) appears to be mediated through the estrogen-α receptor pathway with the requirement of aromatization of testosterone to estrogen in males. Little literature exists to explicate the machinery leading from estrogen-α receptor activation to an increment in action; withal, recent literature has suggested that alterations in dopaminergic systems as well as possible non-genomic deportment of estrogen may be involved. The few bachelor human studies in this area i , 19 , 32 have contained multiple confounders that make deriving any useful conclusions from these studies hard at best. Thus, extensions of the existing mechanistic studies on ERα-pathway regulation of physical activity in rodents also as more advisedly controlled human studies are needed to determine if sexual activity hormones provide any physiological regulation of activity in humans and if so, possible pathways through which this consequence may be mediated. The increasing rate of inactivity which has led to the increased cardiovascular and other hypokinetic diseases in most populations 27 make understanding the mechanisms of concrete activity regulation critical in the context of the health-related goals of our social club.

An external file that holds a picture, illustration, etc.  Object name is ijbsv04p0126g04.jpg

Hypothesized schematic of the regulation of physical activity by sex hormones in rodents. "?" = pathway currently supported by speculation and/or tentative information. DAT = dopamine transporter; D2/D4, D1/D5 signify different dopamine receptor populations.

Acknowledgments

The author would similar to thank the editing and proof-reading comments of the Kinesiology Writing Accountability Klatch: Drs. Thousand. Turner, T. Hubbard, S. Tsivitse, and Yard. Cordova as well as suggestions for studies and verbiage to include in this review past R. Bowen and A. Knab. This review supported by funding from NIH NIAMS RO1AR050085.

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Source: https://www.ncbi.nlm.nih.gov/pmc/articles/PMC2359866/

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