Postnatal development of the gastrin-releasing peptide system in the lumbosacral spinal cord controlling male reproductive function in rats

Katayama, Nao; Oti, Takumi; Takanami, Keiko; Sakamoto, Tatsuya; Sakamoto, Hirotaka

doi:10.2183/pjab.92.69

Cited by 9 publications

(8 citation statements)

References 26 publications

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“…Second, sexual dimorphism in LSt neuron numbers is already present at P4 (Figure and Figure , Tables and ), much before the third postnatal week that was previously suggested for its appearance (Phelan & Newton, ). It is also much before the age examined by Katayama, Oti, Takanami, Sakamoto, and Sakamoto (), who quantified GRP expression and reported sexual dimorphism at P16 in the rat. What could be the cause of sexual dimorphism at P4?…”

Section: Discussionmentioning

confidence: 93%

Lumbar spinal cord neurons putatively involved in ejaculation are sexually dimorphic in early postnatal mice

Federighi

Asteriti

Cangiano

2019

J of Comparative Neurology

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A crucial role in ejaculation is thought to be played by a population of lumbar spino‐thalamic neurons (LSt), which express galanin and other neuropeptides. In rats, these neurons are activated with ejaculation and their lesion selectively abolishes ejaculation but not other mating behaviors. Consistently with their role, in adult rats and humans, LSt neurons are sexually dimorphic, being more numerous in males. Here we examined whether sexual dimorphism arises early in development, using a transgenic mouse line in which the expression of fluorescent protein is driven by the galanin promoter. We focused on postnatal day 4, shortly after a transient perinatal androgen surge in males that could play an organizational role in LSt development. We found a population of brightly fluorescent neurons organized in bilateral columns dorsolateral to the central canal in segments L1–L5, the expected location of the LSt group. Their number was close to that of adult preparations and significantly greater in male than in female siblings (+19%; CI95%: +13% to +27%; p < .01). This was not due to a generalized higher galanin expression in the male since fluorescent L4 DRG neurons, innervating the hindlimbs and lower back, were not significantly dimorphic (−4%; CI95%: −10% to +8%; p = .92). Unexpectedly, we found in cervical segments a population of fluorescent neurons having a location relative to the central canal similar to the LSt. Thus, the LSt group is sexually dimorphic soon after birth. However, it is possible that only a subset of its neurons participate in the control of ejaculation.

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Section: Discussionmentioning

confidence: 93%

Lumbar spinal cord neurons putatively involved in ejaculation are sexually dimorphic in early postnatal mice

Federighi

Asteriti

Cangiano

2019

J of Comparative Neurology

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“…In accordance with the results from rats, the results of double IHC for AR and GRP suggest that the sexually dimorphic spinal GRP system is also androgen‐dependent in suncus and mice. In addition, the androgen surge during perinatal life and after puberty from the testis may contribute to establishing and maintaining the male‐specific GRP system (Katayama et al, ; Oti et al, ). Sexually dimorphic motoneuron pools have also been identified in suncus that are analogous to the spinal nucleus of the bulbocavernosus in rats and mice (Polak & Freeman, ); it is homologous to Onuf's nucleus in humans in that it innervates the striated perineal muscles attached to the base of the penis (Breedlove & Arnold, ; Sengelaub & Forger, ).…”

Section: Discussionmentioning

confidence: 99%

Identification of the sexually dimorphic gastrin‐releasing peptide system in the lumbosacral spinal cord that controls male reproductive function in the mouse and Asian house musk shrew (Suncus murinus)

Tamura

Kobayashi

Hirooka

et al. 2017

J of Comparative Neurology

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Several regions of the brain and spinal cord control male reproductive function. We previously demonstrated that the gastrin-releasing peptide (GRP) system, located in the lumbosacral spinal cord of rats, controls spinal centers to promote penile reflexes during male copulatory behavior. However, little information exists on the male-specific spinal GRP system in animals other than rats. The objective of this study was to examine the functional generality of the spinal GRP system in mammals using the Asian house musk shrew (Suncus murinus; suncus named as the laboratory strain), a specialized placental mammal model. Mice are also used for a representative model of small laboratory animals. We first isolated complementary DNA encoding GRP in suncus. Phylogenetic analysis revealed that suncus preproGRP was clustered to an independent branch. Reverse transcription-PCR showed that GRP and its receptor mRNAs were both expressed in the lumbar spinal cord of suncus and mice. Immunohistochemistry for GRP demonstrated that the sexually dimorphic GRP system and male-specific expression/distribution patterns of GRP in the lumbosacral spinal cord in suncus are similar to those of mice. In suncus, we further found that most GRP-expressing neurons in males also express androgen receptors, suggesting that this male-dominant system in suncus is also androgen-dependent. Taken together, these results indicate that the sexually dimorphic spinal GRP system exists not only in mice but also in suncus, suggesting that this system is a conserved property in mammals. J. Comp. Neurol. 525:1586-1598, 2017. © 2016 Wiley Periodicals, Inc.

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“…The specificity of the anti-GRP serum in the spinal cord was performed as demonstrated elsewhere [ 31 ]. Immunoreactive products were detected with the Streptavidin-biotin Kit (Nichirei, Tokyo, Japan), followed by diaminobenzidine (Dojindo, Kumamoto, Japan) development according to our method detailed previously [ 7 , 11 , 14 , 30 , 31 , 32 ]. To determine the density of GRP + fibers in the lumbosacral spinal cord (L5–S1 level), at least ten sections per animal were analyzed using ImageJ software (ImageJ 1.44p, RRID_ SCR_003070) with a set threshold level.…”

Section: Methodsmentioning

confidence: 99%

“…We determined the proportion of pERK + , GRP + , and YFP + neurons in the lumbosacral spinal cord. Immunofluorescence analysis of pERK, GRP, and YFP expression in the neurons of the anterior lumbar spinal cord (L3–L4 level) was performed as described earlier using horizontal sections (approximately 18–22 30 µm-thick sections per animal) [ 29 , 30 , 32 ]. Briefly, we counted the number of pERK + , GRP + , and YFP + cell bodies at ×200 magnification in all sections and analyzed a 600 µm 2 area localized to the midline at the center.…”

Section: Methodsmentioning

confidence: 99%

Sexual Experience Induces the Expression of Gastrin-Releasing Peptide and Oxytocin Receptors in the Spinal Ejaculation Generator in Rats

Oti

Ueda

Kumagai

et al. 2021

IJMS

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Male sexual function in mammals is controlled by the brain neural circuits and the spinal cord centers located in the lamina X of the lumbar spinal cord (L3–L4). Recently, we reported that hypothalamic oxytocin neurons project to the lumbar spinal cord to activate the neurons located in the dorsal lamina X of the lumbar spinal cord (dXL) via oxytocin receptors, thereby facilitating male sexual activity. Sexual experiences can influence male sexual activity in rats. However, how this experience affects the brain–spinal cord neural circuits underlying male sexual activity remains unknown. Focusing on dXL neurons that are innervated by hypothalamic oxytocinergic neurons controlling male sexual function, we examined whether sexual experience affects such neural circuits. We found that >50% of dXL neurons were activated in the first ejaculation group and ~30% in the control and intromission groups in sexually naïve males. In contrast, in sexually experienced males, ~50% of dXL neurons were activated in both the intromission and ejaculation groups, compared to ~30% in the control group. Furthermore, sexual experience induced expressions of gastrin-releasing peptide and oxytocin receptors in the lumbar spinal cord. This is the first demonstration of the effects of sexual experience on molecular expressions in the neural circuits controlling male sexual activity in the spinal cord.

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Postnatal development of the gastrin-releasing peptide system in the lumbosacral spinal cord controlling male reproductive function in rats

Cited by 9 publications

References 26 publications

Lumbar spinal cord neurons putatively involved in ejaculation are sexually dimorphic in early postnatal mice

Lumbar spinal cord neurons putatively involved in ejaculation are sexually dimorphic in early postnatal mice

Identification of the sexually dimorphic gastrin‐releasing peptide system in the lumbosacral spinal cord that controls male reproductive function in the mouse and Asian house musk shrew (Suncus murinus)

Sexual Experience Induces the Expression of Gastrin-Releasing Peptide and Oxytocin Receptors in the Spinal Ejaculation Generator in Rats

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