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Expression and Distribution of the Transient Receptor Potential Cationic Channel Ankyrin 1 (TRPA1) in the Human Vagina

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Expression and Distribution of the Transient Receptor Potential Cationic Channel Ankyrin 1 (TRPA1) in the Human Vagina International Journal of Impotence Research (2014) 27, 16–19 & 2014 Macmillan Publishers Limited All rights reserved 0955-9930/14 www.nature.com/ijir ORIGINAL ARTICLE Expression and distribution of the transient receptor potential cationic channel ankyrin 1 (TRPA1) in the human vagina SU¨ ckert1, JE Sonnenberg2, K Albrecht1, MA Kuczyk1 and P Hedlund3,4 The transient receptor potential cationic channel type A1 (TRPA1), belonging to a superfamily of cationic membrane channels, has been suggested to act as mechano- and pain sensor and, thus, to play a role in neurotransmission in the human body, including the urogenital tract. While the expression of TRPA1 has been investigated in a variety of tissues, up until today, no study has addressed the expression and distribution in the female genital tract. The present study aimed to investigate the expression and distribution of TRPA1 protein in human vaginal tissue. Reverse transcriptase PCR (RT-PCR) was applied in order to identify messenger ribonuleic acid specifically encoding for TRPA/A1. The distribution of TRPA1 in relation to the neuronal nitric oxide synthase (nNOS) and the signaling peptide calcitonin gene-related peptide (CGRP) was examined by means of immunohistochemical methods (double- antibody technique, laser fluorescence microscopy). RT-PCR analysis revealed the expression of mRNA encoding sequences specific for TRPA in the vaginal wall and epithelium. Immunostaining related to TRPA1 was observed in the basal epithelium and in slender varicose nerve fibers transversing the subepithelial and stromal space of the vaginal sections. In addition, these fibers presented immunoreactivity specific for nNOS or CGRP. The smooth musculature of the vaginal wall and small vessels interspersing the tissue did not present signals related to TRPA1. The findings indicate that TRPA1 might be involved in afferent neurotransmission in the vagina and work synergistically together with the nitric oxide/cyclic guanosine monophosphate pathway. International Journal of Impotence Research (2014) 27, 16–19; doi:10.1038/ijir.2014.23; published online 24 July 2014 INTRODUCTION sulfide, enabling the channel to act as mechano- and pain sensor 5 It is assumed that the vagina plays a pivotal role in the perception at the cellular level. To date, there is growing evidence that of coital stimulation, leading to sexual arousal and, finally, orgasm. disturbances in local afferent (sensory) mechanisms might be With visual and sensory stimulation, an increase in genital blood related to the pathogenesis of dysfunctions of the lower urinary flow and the relaxation of the smooth musculature of the vagina tract. Thus, not surprisingly, current research has been devoted to occurs, resulting in an increase in vaginal luminal diameter and the TRPA channel and its potential role in sensory signaling and 9 lubrication, thus allowing penetration of the male penis during neurotransmission in the urogenital tract. The expression and sexual intercourse.1,2 Although our knowledge regarding the distribution of the TRPA1 was investigated by means of molecular physiology of the female sexual response is constantly growing, biology, western blot analysis or immunohistochemistry in the the mediators and mechanisms contributing to this process are prostate, the mucosa and smooth muscle of the human urinary still poorly understood.3,4 This slow progress is due to the bladder, as well as in the urethra. Functional studies using isolated complexity of the factors and their interactions—neuronal path- tissue of the bladder or urethra were also conducted in order to ways, endocrine and local cellular mediators—involved in the evaluate the significance of TRPA1 in the control of the outflow 10–12 biological control of the female sexuality. The transient receptor region. Up until today, no study has addressed TRPA1 in female potential cationic channel ankyrin 1 (TRPA1) is a member of the genital tissues, such as the clitoris, labia or vagina. Therefore, it TRP superfamily of membrane channels, consisting of the six sub- was the aim of the present study to evaluate in the human vagina families TRPA, TRPC, TRPM, TRPP, TRPML and TRPV. TRP channels, by means of molecular biology (reverse transcriptase PCR, RT-PCR permeable to most divalent cations, are known to play a central analysis) and conventional immunohistochemistry the expression role in smooth muscle contraction, the release of neurotransmit- and distribution of TRPA1. ters, cell proliferation and apoptosis.5 Although TRP channels are only poorly selective for Ca2 þ , they contribute mainly to changes 2 þ in cytosolic Ca by acting as entry gates into the plasma. TRPA1 MATERIALS AND METHODS is abundantly expressed in vertebrate dorsal root and trigeminal Tissue source and handling ganglia, as well as in hair cells of the inner ear.6–8 The channel protein can be activated by physical stimuli, such as noxious cold, In accordance with the regulations of the local ethical committee of the Hannover Medical School, specimens of the human vagina were obtained or chemical activators, including arachidonic acid, isothiocyanates, from five female cadavers (age at the time of death: 16–42 years) as well as cinnamonaldehyde, allicin, diallyl disulfide (stinging compounds in from five women (aged 48–63 years, three menopausal, two postmeno- mustard, wasabi, horseradish, cinnamon or garlic, respectively), pausal; mean age: 53 years) who had undergone pelvic surgery for acrolein (irritant in exhaust fumes and tear gas) or dihydrogen gynecological malignancies. None of the female donors had a known 1Division of Surgery, Department of Urology and Urological Oncology, Hannover Medical School, Hannover, Germany; 2Sexual Function Research Unit, Institute for Biochemical Research and Analysis, Hannover, Germany; 3Faculty of Medicine, Department of Clinical Pharmacology, Linko¨ping University, Linko¨ping, Sweden and 4Department of Urology, Urological Research Institute (URI), University Vita Salute San Raffaele, Milan, Italy. Correspondence: Professor S U¨ ckert, Division of Surgery, Department of Urology and Urological Oncology, Hannover Medical School, 30625 Hannover, Germany. E-mail: [email protected] Received 10 October 2013; revised 9 January 2014; accepted 30 May 2014; published online 24 July 2014 TRPA1 in the human vagina SU¨ ckert et al 17 history of endocrinological or neurological diseases or sexual dysfunction. RT-PCRs were of the expected size of 656 base pairs (bp). Different Full wall preparations were taken from the lower mid portion of the vagina magnitudes of mRNA expression were observed in the vaginal and immediately placed in an ice-cold solution of CUSTODIOL (Dr Franz tissues: the relative degree of mRNA expression appeared to be Ko¨hler Chemie GmbH, Alsbach, Germany). more abundant in the vaginal wall than in the epithelial layer. A characteristic pattern of RT-PCR products from the experiments RT-PCR analysis using human vaginal wall and vaginal epithelium is displayed in For RT-PCR experiments, the vaginal epithelium was carefully separated Figure 1. from the smooth musculature and both tissue portions were frozen in liquid nitrogen. The expression of mRNA specifically encoding for TRPA1 Immunohistochemistry was analyzed by means of the RT-PCR. Reaction mixtures were prepared in test tubes (volume: 0.2 ml) using up to 5 mg total RNA extracted from Examination of numerous sections (three to five) at different levels specimens of the vaginal wall or epithelium, 1 ml 10 mM dNTP and 1 ml revealed that the TRPA1 protein is present in the human vagina. oligo (dT)12–18 (0.5 mg ml À 1) and made-up to 10 ml with sterile water. The The findings appeared consistent in all tissue sections examined. mixtures were incubated for 5 min at 65 1C, then placed on ice for at least Immunosignals related to TRPA1 were observed in the epithelial 1 min. Nine (9) ml of a mixture comprising 2 ml10Â RT buffer, 4 ml25mM layer (basal epithelial cells and cells lining the vaginal lumen) and MgCl2,2ml 0.1 M dithiothreitol and 1 ml RaceOUT recombinant ribonuclease À 1 in slender varicose nerve fibers transversing the subepithelial space inhibitor (40 units ml ) was added followed by incubation for 2 min at and smooth muscle layer of the vaginal sections. In the epithelial 1 42 C. Fifty units of SuperScript II reverse transcriptase (Invitrogen GmbH, cells, staining was seen throughout the cytoplasm without any Karlsruhe, Germany) were added to each test tube (except for the negative RT control) followed by incubation for 50 min at 42 1C. The reaction was particular relation to subcellular structures (Figure 2a). A majority, terminated by heating for 15 min to 70 1C and then cooling the samples to but not all, TRPA1-immunoreactive (IR) subepithlial nerves pre- 0 1C. Two units of RNase H were added to each tube followed by sented immunoreactivity for CGRP (Figure 2b–d). In nerve fibers incubation for 20 min at 37 1C. PCR amplification was performed using extending through the muscle layer, TRPA1 was also co-localized 1–2 ml cDNA template (200 ng ml À 1), 1–2 ml specific primers (10 pmol ml À 1) with CGRP (Figure 2e–g). In addition, these fibers were character- and 25 ml Taq PCR Master Mix (Qiagen AG, Hilden, Germany). A negative ized by the expression of nNOS. All TRPA1-IR nerves also exhibited control (omitting the template cDNA) was included in each experiment. strong fluorescence signals specific for nNOS and vice versa PCRs were performed in a Model 9600 thermocycler (PE Biosystems GmbH, (Figure 2h–l). The smooth musculature
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