Bulbospongiosus Muscle Frecuency Activity is Modified by Sucrose Consumption During Pregnancy-lactation and Postweaning Offspring Male Rats

doi:10.21203/rs.3.rs-1995382/v1

Download PDF

Article

Bulbospongiosus Muscle Frecuency Activity is Modified by Sucrose Consumption During Pregnancy-lactation and Postweaning Offspring Male Rats

https://doi.org/10.21203/rs.3.rs-1995382/v1

This work is licensed under a CC BY 4.0 License

Version 1

posted

You are reading this latest preprint version

Disorders of perineal musculature, as the bulbospongiosus muscle (Bsm), could cause male sexual dysfunctions, such as premature ejaculation. We determined the effect of sucrose water consumption during pregnancy-lactation and postweaning on the Bsm frequency during the urethrogenital reflex (UGR), which simulates erection and ejaculation, in adult male rat offspring. Twelve female rats were mated and grouped in control mothers consumed tap-water and sucrose mothers consumed sucrose-water during pregnancy-lactation. Male pups were weaned and assigned into four groups (n = 12 each): those from control mothers who continued drinking tap-water (CM–CO group) or sucrose-water (CM–SO group) until adult life, and those from sucrose mothers who drank tap-water (SM–CO group) or continued drinking sucrose-water (SM–SO group) until adult life. We analyzed Bsm electromyograms during penile stimulation and UGR in male rat offspring (n = 6; each group). We analyzed the frequency of the Bsm through Fourier Transform. Other males rat offspring (n = 6; each group) were killed and was collected the Bsm and processed into histological analysis. Two-way ANOVA followed by posthoc tests, considering P ≤ 0.05 significant difference. The results showed that the consumption of sucrose-water during critical stages increases significantly the frequency of Bsm during the UGR of the CM-SO, SM-CO and SM-SO. Also, the consumption of high-sugar diets changes the morphological arrangement of the Bsm. Our results suggest that a combination of a high-sugar diet during pregnancy, lactation, and post-weaning changes the Bsm morpho-physiology and could cause male sexual dysfunctions.

carbohydrate diet

bulbospongiosus muscle

sexual dysfunction.

Erectile dysfunction is the inability to maintain a penile erection of sufficient quality and to permit a satisfactory sexual intercourse¹ and has been closely associated with metabolic disorders, such as insulin resistance and obesity.^2,3 It related metabolic disorders of the progeny with the type of maternal nutrition during the perinatal period (gestation and lactation).^4–7 A high sucrose diet increased the fat mass and reduced lean mass in the offspring.^8–11 Likewise, the histological arrangement of the testis is hypertrophied¹² and affects the neural and endothelial components of penile erection.¹³ The physiology and morphology of skeletal muscle are compromised in male offspring.^14–17

Skeletal muscle is a metabolic target with a capacity to uptake glucose and store it as glycogen to get energy.¹⁸ The regulation adequately promotes the muscle development and homeostasis in coordination with liver and adipose tissue metabolism.^7,18 Alterations in the growth and the development of the skeletal muscle during the perinatal period could result not only in muscle mass defects, besides metabolic disorders¹⁹ that are related with the erectile dysfunction in males.^15,20 An explanation is severe alterations in the pelvic¹⁵ or perineal²¹ muscles, which play a role in erectile dysfunction with metabolic disorders.

Our research group showed that pubococcygeus and bulbospongiosus muscles (Bsm) take part in the spinal reflex characterized by penile erections and expulsion of urethral fluids, denominated urethrogenital reflex (UGR) in adult male rats.²² The pubococcygeus showed tonic activity during the UGR. Meanwhile, the Bsm was activated at the beginning of the penile extension, with phasic activity during the expulsion²² and is an essential muscle for penile erection.^21,23,24 The consumption of sucrose beverages (5% of sucrose water) during the perinatal period or postweaning were increased the body weight gain and reduced the pubococcygeus reflex and duration of the UGR in male offspring rats.¹⁵ However, in the perinatal period, the high-calorie diet changed the morphology of skeletal muscle in the adult rat offspring.¹⁷ The maternal or postweaning diet could affect the physiology and morphology of important skeletal muscles to sexual reflexes, such as the Bsm.^21–22 We used the experimental design of Corona-Quintanilla et al.¹⁵ to determine if the sucrose-water consumption during pregnancy-lactation or postweaning affects the Bsm activity during UGR and muscle arrangement in adult rat offspring.

Animal care and maintenance

The Research Ethics Committee from the Universidad Autónoma de Tlaxcala approved all experimental procedures following the Mexican Guidelines for Animal Care, which are based on recommendations by The International Association for Assessment and Accreditation of Laboratory Animal Care (Norma Oficial Mexicana NOM-062-200-1999, México). Animals were housed in polypropylene cages (65 cm X 25 cm X 15 cm) and maintained under a 12 h light-12 h dark cycle (with the lights off from 08:00 h to 20:00 h) with constant room temperature (20 ± 2°C); standard diet (Purina Laboratory Chow 5001) and tap-water ad libitum.

Dams

Twelve female Wistar-rats (3 months old with 220-250g body weight) were put together with a proven sexually expert adult male to breed (24 h). Upon confirmation of semen plug presence into the vagina, females housed individually and randomly assembled into two different groups: control (CM, control mothers), which consumed tap-water, and treated dams (SM, sucrose mothers), which drank sucrose water during gestation-lactation (n = 6, each group) (5 g sucrose / 100 mL). All litters were adjusted eight to ten pups after birth, to standardize food demand during lactation. Pregnant and lactating mothers were weighed every day until pups were removed (weaning) at postnatal day 22 (P22) to calculate the weight gain and reported in Corona-Quintanilla et al.¹⁵

Offspring

Pups randomly assigned as follows: 1) Those who consumed tap-water postweaning and came from mothers who drank tap-water during gestation-lactation (CM-CO, Control Mother-Control Offspring; n = 12); 2) those who consumed 5% of sucrose-water (5 g sucrose / 100 mL) postweaning and came from mothers that drank tap-water during gestation-lactation (CM-SO, Control Mother-Sucrose Offspring; n = 12); 3) those who drank tap-water postweaning and came from mothers that consumed 5% of sucrose-water during gestation-lactation (SM-CO, Sucrose Mother-Control Offspring; n = 12); and 4) those who consumed 5% of sucrose-water postweaning and came from mothers that consumed 5% of sucrose-water during gestation-lactation (SM-SO, Sucrose Mother-Sucrose Offspring; n = 12) (Fig. 1A).

Urethrogenital reflex and Bsm electromyograms recordings

Other male rats from all groups (n = 6 per group) were anesthetized with urethane (1.5 g / kg, i.p.). The surgical procedure was performed according to Xicohténcatl-Rugerio et al.²² The bladder was exposed, and a small incision was done. A catheter was introduced and placed into the urethra and connected into a P23BC-transducer (Statham-Hato) to record variations in the urethral pressure (UP; Fig. 1B). It also was connected to a 7P1G direct current (Grass-Instruments. Co. Massachusetts, USA) and displayed on a PolyView® Recorder (Grass-Instruments. Co. Massachusetts, USA; Version 2.5) installed on a desktop computer.

The Bsm electromyograms (EMG) were obtained simultaneously during penile stimulation and UGR for animals from all groups. The Bsm were dissected according to Xicohténcatl-Rugerio et al.²¹ Bipolar electrodes (0.01 mm silver-wires) inserted into the proximal Bsm (Fig. 1B). The electrical activity was amplified and filtered by a 7P511-preamplifier connected to a 79E-polygraph (Grass-Instruments. Co. Massachusetts, USA) and plugged into the PolyView® Recorder channels.

Penile stimulation

The penile and UGR stimulation applied three times, leaving a 15-min interval between each. The penile reflex was evaluated through perigenital-skin (including foreskin and scrotum), penile-extension, and occlusion stimulation. A brush was used to perform perigenital-skin stimulation (Fig. 1B).

EMG recordings

The penis was pulled out from the foreskin for penile-extension recording until seeing the dorsal penile vein (1–1.5 cm) at the penis base. The penis occlusion consisted of applying mechanical pressure using forceps to the penis head for 15 sec, while the penis was extended as above-mentioned. During the penis stimulation, the UP and EMG were recorded. Stimulus sequentially applied following the next sequence: perigenital-skin stimulation and penile-occlusion, allowing the UP to return to the baseline before using another series of stimulation.

UGR recording

For the UGR recording, we first stimulated perigenital-skin; after that, the penis was extended and occluded with a clamp until the maximal UP was reached, which continued for 50 ± 10 sec. Meanwhile, saline solution (37°C) was infused at a constant rate of 0.08 ml / s into the urethra (Fig. 1B), which triggered a rapid UP rise and Bsm reflex electrical activity. Each UGR started when the UP and Bsm EMG were at the baseline. This procedure was applied by three times.

For EMG recordings, a muscle was considered activated when the EMG trace increased. The muscle was considered inhibited when the EMG trace remained unchanged from the baseline. Simultaneous to the maximum pressure of UGR was recorded the Bsm activity. The frequency of those bursts was measured with the PolyView program (Grass-Instruments. Co. Massachusetts, USA; Version 2.5). This frequency was determined by the spectral analysis of Fast Fourier Transform (FFT) and filtered using the Hamming windowing tool to avoid FFT distortion plot caused by selected data start and stop discontinuity.

Morphometric measurements and tissue analysis

To morphological study were used male rats from all groups (n = 6 in each group) were anesthetized with urethane (1.5 g/kg, i.p.). The male rats were fixed in a dorsal supine position to make an incision on the perineal skin surgical procedure was performed according to Holmes et al.²³ and Xicohténcatl-Rugerio et al.²² Bsm were identified by using a stereoscopic microscope (SMZ-2T, Nikon, Japan). The width and length were measured with a digital vernier caliper (TRUPER STAINLESS STEEL); after the muscles were photographed using a digital camera (Power Shot S50, Canon, Japan), and subsequently, the Bsm was removed and weight was measured by using the analytical balance.

The Bsm was processed to histological analysis. The Bsm was immersed in Bouin-Duboscq fixative solution for 12 hr., dehydrated in alcohols, and embedded in Paraplast X-TRA® (Sigma-Aldrich, St. Louis, MO, USA) to obtain serial transverse sections (7 µm) using a microtome (Leica RM2135), and then, stained using Hematoxylin-eosin staining protocol. Sections were visualized using a light microscope (Zeiss Axio Imager A1) and photographs were taken. Measurement of muscle fibers was done using a reconstruction of whole fibers transverse sections using Axiovision SE64 Rel. 4.9.1 software (Carl Zeiss Microscopy GmbH). For the histological analysis of the cross-sectional areas (CSA) was selected 100 fibers per section of each animal; subsequently, the fibers were measured in the 12 o'clock direction and three in the clockwise direction.

Statistical Analysis

To determine significant differences in the morphometric measurements, the peripheral myonuclei per fiber and CSA of fibers of the Bsm of all groups, we used the two-way ANOVA tests, followed by the Bonferroni tests. For all cases, a P ≤ 0.05 was accepted as statistically significant. To determine significant differences in the frequency of activation of Bsm during the UGR, it used the Kruskal-Wallis test, and the Dunns' multiple comparison test (P ≤ 0.05). To determine significant differences between the frequencies of activation and the bins of CSA of each group were used the χ2 test followed by Fisher's exact tests. Data are shown as means and standard errors (SEM). All statistical analyses were done in the Graph Pad Prism version 5.0 for Windows (Graph Pad Software, San Diego).

Penile stimulation and Bsm activity frequency

In the CM-CO group, during perigenital skin stimulation triggered Bsm bursts of activity (Fig. 2A). The penile extension and occlusion bursts of activity of Bsm. Specifically, at the start and the end of both stimuli the Bsm showed higher amplitude activity (Fig. 2A). Meanwhile, in the CM-SO, at the start of perigenital skin stimulation, the Bsm was to activate slightly. During the penile extension, the Bsm showed longer lasting activity during penile extension (Fig. 2B). In the SM-CO groups, the Bsm only showed activity during penile extension (Fig. 2C). In the SM–SO group, the electrical activity of the Bsm was found, only, at the start the perigenital skin stimulation, during the penile extension y at the end of occlusion (Fig. 2D).

Bsm activity during urethrogenital reflex

In the CM-CO group, the Bsm a phasic activity during the maximum pressure of the UGR. After, the Bsm showed a low intensity activity and small bursts of EMG activity (Fig. 3A). Nevertheless, the CM-SO and SM-SO groups, only, showed lower amplitude activity during the UGR (Fig. 3B, D). Meanwhile, the SM-CO group showed activity from penile stimulation and during the UGR (Fig. 3C). However, in those groups with sucrose-water, in the maternal diet and offspring, the Bsm frequency activity simultaneously with the maximum pressure of UGR showed significant differences (K = 807.9, P < 0.0001) (Fig. 3E). The frequency of burst decreased in the CM–CO compared to CM-SO (P < 0.0001), SM–CO (P < 0.0001) and SM–SO (P < 0.0001) groups. The frequency of burst was minor in the CM–SO vs. SM–CO (P < 0.0001) and SM–SO (P < 0.0001) groups. While, the frequency of Bsm increased in the SM-CO vs. SM-SO (P < 0.0001) groups (Fig. 3E). The maternal diet and offspring sucrose-water promoted significant changes in the different frequencies of Bsm (x² = 113.6; P < 0.0001). The bin of 0 Hz in the CM-CO groups was higher than the SM-CO (P < 0.0001) and SM-SO (P = 0.0006). While, to the CM-SO were the same differences in comparison with the SM-CO (P < 0.0001) and SM-SO (P = 0.0001). Nevertheless, to the SM-CO does not show bin 0 Hz and is significantly different from the SM-SO (P = 0.02). To the bin of 2 Hz, the CM-CO groups was higher than the CM-SO (P = 0.0014), the SM-CO (P < 0.0001) and SM-SO (P = 0.0001). While, to the CM-SO showed higher percentage of 2 Hz than the SM-CO (P = 0.0002). This frequency in SM-CO was lower than in the SM-SO group (P = 0.002). However, to the bin of 6 Hz, the CM-CO groups was lower than the CM-SO (P < 0.0001), the SM-CO (P < 0.0001) and SM-SO (P < 0.0001). While, to the CM-SO, also, showed a lower percentage of 6 Hz than SM-CO (P < 0.0001) and SM-SO (P = 0.03). This frequency in SM-CO was higher than in the SM-SO group (P = 0.003). No significant differences were found for the 4Hz bin (Fig. 3F).

Morphological measurements

The weight of Bsm showed differences between groups (Fig. 4A). This measurement was affected significantly by individual factors maternal diet (F_1,20= 9.21, P = 0.006) and offspring sucrose-water (F_1,20= 40.64, P < 0.0001). Post hoc tests showed that compared to the CM–CO group, CM–SO (P < = 0.001), SM–CO (P < 0.05), and SM-SO (P < 0.001) showed a significant increase in the weight of Bsm (Fig. 4A). But, the length of the muscle does not show significant differences (F_1,20= 0.02, to interaction; F_1,20= 0.62, maternal diet, and F_1,20= 2.13, offspring sucrose-water) (Fig. 4B). Meanwhile, the interaction between maternal diet and offspring sucrose-water promoted significant changes in the width of Bsm (F_1,20= 17.08, P < 0.0005); or individual factors maternal diet (F_1,20= 17.08, P < 0.0001) and offspring sucrose-water (F_1,20= 46.44, P < 0.0001). Likewise, the sucrose intake promoted a significant increase in the width of Bsm at comparing to CM–CO with CM–SO (P = 0.001); SM–CO (P = 0.001), and SM–SO (P < 0.001) (Fig. 4C).

Histological analysis

In the CM-CO group, the Bsm showed the multinucleated muscle fibers with basophilic nuclei, stained blue and located in the periphery of the muscle fibers, were observed. An integral and well-defined membrane was observed. The arrangement of muscle fibers is tight and a conserved ratio in size to cross-sectional area. However, in those groups with sucrose-water, in the maternal diet and offspring show increased connective tissue between muscle fibers and even the presence of immune cells (Fig. 5A). The interaction between maternal diet and offspring sucrose-water promoted significant changes in the number of peripheral myonuclei in the Bsm (F_1,20 = 6.30, P < 0.02). Specifically, significant differences were observed after comparing with CM–CO vs CM–SO; SM–CO and SM–SO (P < 0.05) (Fig. 5B).

The interaction between both factors was significant to the fiber CSA (F_1,20 = 5.47, P < 0.02). The significant differences were at comparing CM–CO vs CM–SO; CM–CO vs SM–CO; CM–SO vs SM–SO; and SM–CO vs SM–SO groups (P < 0.05) (Fig. 5C). Fibers of smaller size observed in the Bsm of the CM-SO and SM-CO groups. To the range < 800 µm² the CM-CO groups was a less than the CM-SO (P < 0.01) and SM-CO (P < 0.0001). While, to the CM-SO and SM-CO showed a higher percentage of fibers of this range than the SM-SO group (P = 0.0007; P = 0.0003). However, the fibers of 1600 µm² were observed in the SM-SO group. Specifically, for this range the significant differences were in the SM-SO group versus CM-SO (P = 0.02) and SM-CO (P = 0.04). However, the CM-CO group the highest percentage of fibers was observed in the range of > 2000 µm2. The CM-CO group showed significant differences versus CM-SO (P = 0.0001) and SM-CO (P = 0.003). In addition, the CM-SO group showed a lower percentage of 2000 µm2 fibers than the SM-SO group (P = 0.015). No significant differences were found for the range of 1200 µm2 (Fig. 5D).

The consumption of sucrose-water in the pregnancy-lactation or during postweaning changed the physiology and muscle arrangement of the Bsm, an important skeletal muscle to male sexual reflexes. The maternal diet interaction during pregnancy-lactation and postweaning changed the activity of Bsm during penile stimulation and increased the frequency of the bursts during the UGR. However, each one factor increased the weight of Bsm. The interaction of both factors increased the muscle width and the percentage of fibers less than 800 µm2. Both factors decreased the number of peripheral myonuclei per fiber, the fibre cross-sectional area, and the percentage of fibers larger than 2000 µm2 in Bsm.

We showed that the inadequate consumption of 5% of sucrose-water during the perinatal period or postweaning increased the body weight gain and changed the pubococcygeus activation during penile reflex of the rat offspring.¹⁵ Also, in the male rats, the Bsm is related with the penis and contributes to the penile erection^21–23 and ejaculatory response.^24,25 We in this study determined that the Bsm is another important target for the changes in development during intrauterine life, because of it increased its frequency rate in male rats that came from sucrose mothers and those who received sucrose-water during extrauterine life. In fact, in SM-CO and SM-SO groups, with a consumption of sucrose-water, the Bsm activity decreases during penile stimulation, similar to diabetic rats.²¹ Seppan et al.²¹ suggest that the induced hyperglycemia decreases testosterone levels, as adverse effects on muscle fibers. Thus, the high-carbohydrate diet during pregnancy-lactation and postweaning would produce an alteration of the insulin signaling, which would cause an increase in intramuscular adipocytes and affect the skeletal muscle of the offspring.¹⁶ Therefore, it would be reasonable to believe that it changed if this Bsm activity during penile stimulation because of high sucrose-water then for the animals to suffer from penile dysfunction. This hypothesis is supported because there are significant changes in urethral pressure during UGR in offspring rats with the consumption of sucrose-water.¹⁵ In addition, the decrease in neuromuscular junctions²⁶ and receptors in the urethra,²⁷ could affect the activity of Bsm during the penile stimulation and in the UGR.

While Bsm frequency simultaneously with PMUGR was recorded, it showed a low-intensity reflex activity in the CM-SO group, this possible be related with the changing of Bsm fiber type above mentioned, and also due to all the metabolic changes provoked by the sucrose-water intake, that occur during development such as increased fat mass, intramuscular adipocytes and fibrosis.^14,16,18,28 Besides, the maternal diet in the SM-CO produced an increase in the connective tissue and a decrease in smooth muscle fibers of the corpus cavernosum, as some observe in the male mice with high lipids diet.²⁹ There are some alterations in the striated muscle, as the result of maternal diet, which can be a disruptor in the metabolism of glucose and fatty acids of the offspring.¹⁶ Bsm could also be an important target for this sucrose-water alterations provoked during intrauterine development and during adult life.

The fetal period is a crucial stage for skeletal muscle development, as the length of muscle fibers are formed,^30,31 and in the postnatal stage, muscle growth has only slowed. Other studies reported an increase in fiber size without the new formation of muscle fibers.³² However, the fetal stage is vulnerable to various factors such as maternal nutrition.³¹ We found an increase in the weight and width of the Bsm, without changes in the length, of the groups that consumed water-sucrose during pregnancy-lactation period. This suggests that changes in the maternal diet predispose Bsm to immediate changes to develop in a carbohydrate-rich environment. If it subjected them to a second nutritional challenge during adult life. The skeletal muscle shows alterations that can compromise muscle function and structure. An important physiological index in the muscle's development that is directly related to muscle mass and volume is the cross-sectional area, which has been an important element in the prediction of force production, since the greater the cross-sectional area, the greater the muscle force that develops^33,34 and achieve a higher peak urethral pressure during the UGR in the CM-CO group.²²

Muscle growth is because of an increase in muscle fiber area, resulting in increased muscle mass. During early muscle formation, the cross-sectional area of muscle fibers is approximately the size of the diameter of a single myonucleus,^35,36 and the size increases in proportion to the number of fibers in rats it established this relationship on day 14-28.^21,37

Our muscle fiber cross-sectional area results showed a decrease in cross-sectional areas from the CM-SO and SM-CO postnatally reversed diet groups. However, the SM-SO group was like CM-CO group in the cross-sectional area, suggesting that the maternal diet is a key predisposing factor in muscle development during pregnancy. However, strength to cross-sectional area varies according to several factors, and adaptations in cross-sectional area are based on activity levels of a muscle, as well as changes in interstitial volume, mitochondrial density, amount of glycogen and even intravascular changes.³⁸ Muscle adaptations to various stimuli include changes in fiber content, in the distribution of capillaries and intracellular components such as connective tissue, which leads to changes that generate hypertrophy or atrophy of muscle fibers.³⁹ In our histology results, we observed a structural disorder in terms of an interstitial increase in muscle fibers, as well as connective tissue, in the CM-SO, SM-CO and SM-SO groups. The consumption of high sugar diets both prenatally and postnatally changes the structural organization of muscle. In the skeletal muscle, there is a balance between processes of protein synthesis and degradation whose major function is to keep muscle proteins renewed to preserve the size of muscle fibers through the mTOR complex, which can sense amino acids through nutrition.⁴¹ The mTOR is probably the pathway altered by nutrition during critical windows of development and to promote anabolic cellular processes including protein synthesis, pyrimidines, lipid biosynthesis, and inhibits cellular processes.⁴² Other of the results got were the number of myonuclei per fiber, which was decreased in the CM-SO, SM-CO, SM-SO groups. The modulation of the distribution of the nuclei at along the muscle fiber is associated with adaptive processes associated with hypertrophy or atrophy of a skeletal muscle,^43,44 that depend on different factors present at various stages of development, that could predispose to poor positioning of the nuclei, favoring the appearance of various severe muscle disorders,⁴⁵ implicated in the development of male sexual dysfunctions.

Our results suggest that a combination of a high-sugar diet during pregnancy, lactation, and post-weaning changes the frequency of Bsm during penile and ejaculatory reflexes, such as the UGR. In addition, the structural organization of the Bsm was changed by the consumption of high-sugar diets, generating a decrease in the cross-sectional area and the number of peripheral nuclei of the muscle fibers, which could cause alterations related to the force of muscle contraction. This change in Bsm could cause male sexual dysfunctions, such as premature ejaculation.

Funding: Conacyt 857159SDS, 295860VVO.

Acknowledgements: Authors thank the excellent technical assistance of Laura García (Universidad Autónoma de México, Instituto de Investigación Biomédicas, Departamento de Biología Celular y Fisiología). The assistance of Diego Zacapa in preparing drawings is also acknowledged.

Financial Support: Conacyt 857159SDS, 295860VVO.

Conflicts of Interest: No conflicts of interest, financial or otherwise, are declared by the authors.

Kirby M.The Circle of Lifestyle and Erectile Dysfunction. Sex Med Rev. 2015;3(3):169–182.
eh SU, Yoon S, Choi JH, Do J, Seo DH, Lee SW, et al. Metabolic syndrome is an independent risk factor for acquired premature ejaculation. World J Mens Health. 2019;37:226.
Dursun M, Besiroglu H, Cakir SS, Otunctemur A, Ozbek E. Increased visceral adiposity index associated with sexual dysfunction in men. Aging Male. 2017;21:187–92.
Silveira P, Portella A, Goldani M, Barbieri M. Developmental origins of health and disease (DOHaD). J Pediatr (Rio J). 2007;83 (6): 494–504.
Sharples A, Stewart C, Seaborne R. Does skeletal muscle have an “epi”-memory? The role of epigenetics in nutritional programming, metabolic disease, aging and exercise. Aging cell. 2016;15: 603–616.
Malik VS, et al. Sugar-sweetened beverages and risk of metabolic syndrome and type 2 diabetes: a meta-analysis. Diabetes Care. 2010. PMID: 20693348 Free PMC article. Review.
Nicolás-Toledo L, Cervantes-Rodríguez M, Cuevas-Romero E, et al. Hitting a triple in the non-alcoholic fatty liver disease field: sucrose intake in adulthood increases fat content in the female but not in the male rat offspring of dams fed a gestational low-protein diet. J Dev Orig Health Dis. 2018;9 (2): 151–159.
Kjaergaard M, Nilsson C, Rosendal A, Nielsen MO, Raun K. Maternal chocolate and sucrose soft drink intake induces hepatic steatosis in rat offspring associated with altered lipid gene expression profile. Acta Physiol. 2014;210(1):142–53.
Ding GL, Wang FF, Shu J, et al. Transgenerational glucose intolerance with Igf2/H19 epigenetic alterations in mouse islet induced by intrauterine hyperglycemia. Diabetes. 2012;61(5):1133–42.
Du M, Yan X, Tong JF, Zhao J, Zhu MJ. Maternal obesity, inflammation, and fetal skeletal muscle development. Biol Reprod. 2010;82:4–12.
Navya H, Yajurvedi HN. Obesity causes weight increases in prepubertal and pubertal male offspring and is related to changes in spermatogenesis and sperm production in rats. Reprod Fertil Dev. 2017 29(4):815–823.
Córdoba-Sosa G, Nicolás-Toledo L, Cervantes-Rodríguez M, Xelhuantzi-Arreguín N, Arteaga-Castañeda ML, Zambrano E, Cuevas-Romero E, Rodríguez-Antolín J. Maternal and Offspring Sugar Consumption Increases Perigonadal Adipose Tissue Hypertrophy and Negatively Affects the Testis Histological Organization in Adult Rats Front Cell Dev Biol. 2022 Jun 17;10:893099. doi: 10.3389/fcell.2022.893099. eCollection 2022.
Burnett AL. Novel nitric oxide signaling mechanisms regulate the erectile response. Int J Impot Res. 2004;16:15–19.
Huber K, Miles JL, Norman AM, Thompson NM, Davison M, Breier B. Prenatally induced changes in muscle structure and metabolic function facilitate exercise-induced obesity prevention. Endocrinology. 2009;150:4135–44.
Corona-Quintanilla DL, Velázquez-Orozco V, Xicohténcatl-Rugerio I, Lara-García O, Cuevas E, Martínez-Gómez M, et al. Sucrose Exposure during Gestation Lactation and Postweaning Periods Increases the Pubococcygeus Muscle Reflex Activity in Adult Male Rats. Int. J. Impot. Res.2022; Online ahead of print. 10.1038/s41443-021-00450-7 – DOI
Yan X, Huang Y, Zhao JX, Long NM, Uthlaut AB, Zhu MJ, et al. Maternal obesity-impaired insulin signaling in sheep and induced lipid accumulation and fibrosis in skeletal muscle of offspring. Biol Reprod. 2011;85:172–8.
Oliveira PTR, Manhães-de-Castro R, Silva MJ, Burbano CVE, Cavalcanti LCC, Benjamim CAR, et al. Differential effects of maternal high-fat/high-caloric or isocaloric diet on offspring’s skeletal muscle phenotype. Life Sci. 2018;215:136–44.
Salto R, Manzano M, Giron MD, Cano A, Castro A, Vilchez JD, Cabrera, E, Lopez-Pedrosa JM. A Slow-Digesting Carbohydrate Diet during Rat Pregnancy Protects Offspring from Non-Alcoholic Fatty Liver Disease Risk through the Modulation of the Carbohydrate-Response Element and Sterol Regulatory Element Binding Proteins. Nutrients. 2019;11:844.
Bayol SA, Bruce CR, Wadley GD. Growing healthy muscles to optimise metabolic health into adult life. J Dev Orig Health Dis. 2014;5:420–34
Goodpaster BH, Sparks LM. Metabolic Flexibility in Health and Disease. Cell Metab. 2017;25:1027–1036.
Seppan P, Muhammed I, Mohammad ZIK, Sathyanathan SB. Pathobiology of ischiocavernosus and bulbospongiosus muscles in long-term diabetic male rats and its implication on erectile dysfunction. Aging Male. 2019;1:1–12.
Xicohténcatl RI, Corona-Quintanilla DL, Nicolás L, Martínez- Gómez M, Cuevas E, Castelán F, et al. The role of the pubococcygeous muscle in the urethrogenital reflex of male rats. Neurourol Urodyn. 2017;36:80–85.
Holmes GM, Chapple WD, Leipheimer RE, Sachs BD. Electromyographic analysis of male rat perineal muscles during copulation and reflexive erections. Physiol Behav. 1991;49(6):1235–46.
Tanahashi M, Karicheti V, Thor KB, Marson L. Characterization of bulbospongiosus muscle reflexes activated by urethral disten- sion in male rats. Am J Physiol Regul Integr Comp Physiol. 2012;303:737–47.
Carro-Juárez M, Rodríguez-Manzo M, Rodrıíguez-Peña ML, Franco MA. Rhythmic motor patterns accompanying ejaculation in spinal cord-transected male rats. Int J Impot Res. 2014;26:191–5.
Confortim DH, Jerônimo CL, Centenaro AL, Pinheiro FFP, Matheus MMS, Torrejais MM. Maternal protein restriction during pregnancy and lactation affects the development of muscle fibers and neuromuscular junctions in rats. Muscle Nerve. 2017; 55:109–15.
Chess WR. The use of α-adrenoceptor antagonists in lower urinary tract disease. Expert Opin Pharmacother. 2002;3:167–72.
Huang Y, Zhao JX, Yan X, Zhu MJ, Long NM, McCormick RJ, et al. Maternal obesity enhances collagen accumulation and cross- linking in skeletal muscle of ovine offspring. PLoS ONE. 2012;7: e31691 https://doi.org/10.1371/journal.pone.0031691.
Alves-Pereira JL, Frantz CDE, Pires SAL, Babinski AM, Ramos FDC. Effects of a high energy density diet in the “corpus cavernosum” of mice. Int J Impot Res. 2019;31:126–31.
Stickland NC. A quantitative study of muscle development in the bovine foetus (Bos indicus). Anat. Histol. Embryol. 1978;7: 193–205.
Zhu MJ, Ford SP, Nathanielsz PW, and Du M. Effect of maternal nutrient restriction in sheep on the development of fetal skeletal muscle. Biol. Reprod. 2004;71: 1968–1973.
Karunaratne JF, Ashton CJ, and Stickland NC. Fetal programming of fat and collagen in porcine skeletal muscles. J. Anat. 2005;207: 763–768.
Fukunaga M, Miyatani M, Tachi M, et al. Muscle volume is a major determinant of joint torque in humans. Acta Phys Scand 2001; 172: 249–55.
Moss BM, Refsnes PE, Abildgaard A, et al. Effects of maximal effort strength training with different loads on dynamic strength, cross-sectional area, load-power and load-velocity relationships. Eur J Appl Phys 1997; 75: 193–9.
OhiraY, Jiang B, Roy RR, Oganov V, Ilyina-Kakueva E, Marini JF, et al. Rat soleus muscle fiber responses to 14 days of spaceflight and hindlimb suspension. J Appl Physiol 1992;73: 51S _7S. 27.
Kawano F, Takeno Y, Nakai N, Higo Y, Terada M, Ohira T, et al. Essential role of satellite cells in the growth of rat soleus muscle fibers. Am J Physiol Cell Physiol 2008;295:C45867.
Mantilla CB, Sill RV, Aravamudan B, Zhan WZ, Sieck GC. Developmental effects on myonuclear domain size of rat diaphragm fibers. J Appl Physiol 2008;104: 78794.
Jones EJ, Bishop PA, Woods AK and Green JM. Cross-Sectional Area and Muscular Strength A Brief Review. Sports Med 2008; 38 (12): 987–994.
Stein TP, Bolster DR. Insights into muscle atrophy and recovery pathway based on genetic models. Curr Opin Clin Nutr Metab Care 2006;9(4):395–402. https://doi.org/10.1097/01.mco.0000232899.51544.69.
Léger B, Cartoni R, Praz M, Lamon S, Dériaz O, Crettenand A et al. Akt signalling through GSK-3beta, mTOR and Foxo1 is involved in human skeletal muscle hypertrophy and atrophy. J Physiol 2006;576(Pt 3):923–933. https://doi.org/10.1113/jphysiol.2006.116715.
Daniel John Owens J. Xiao (ed.), Muscle Atrophy, Advances in Experimental Medicine and Biology 1088 Owens, D.J. (2018). Nutritional Support to Counteract Muscle Atrophy. In: Xiao, J. (eds) Muscle Atrophy. Advances in Experimental Medicine and Biology, vol 1088. Springer, Singapore. https://doi.org/10.1007/978-981-13-1435-3_22.
Teixeira CE, Duarte JA. Myonuclear domain in skeletal muscle fibers. Acritical review. Arch ExercHealthDis 2011;2:92–101.
Kim JA, Roy RR, and Edgerton VR. Chapter 55 - Neuromechanical Interactions that Control Muscle Function and Adaptation. Fundamental Biology and Mechanisms of Disease Volume 2, 2012, Pages 789–800.
Perillo M and Folker ES. Specialized Positioning of Myonuclei Near Cell-Cell Junctions. Frontiers in Physiology November 2018 | Volume 9 | Article 1531.

There is NO conflict of interest to disclose.

Download PDF

Version 1

posted

You are reading this latest preprint version

Bulbospongiosus Muscle Frecuency Activity is Modified by Sucrose Consumption During Pregnancy-lactation and Postweaning Offspring Male Rats

Status:

Version 1

Abstract

Figures

Introduction

Material And Methods

Animal care and maintenance

Dams

Offspring

Urethrogenital reflex and Bsm electromyograms recordings

Penile stimulation

EMG recordings

UGR recording

Morphometric measurements and tissue analysis

Statistical Analysis

Results

Penile stimulation and Bsm activity frequency

Bsm activity during urethrogenital reflex

Morphological measurements

Histological analysis

Discussion

Conclusion

Declarations

References

Additional Declarations

Status:

Version 1