https://doi.org/10.4081/ejh.2022.3398
Seasonal changes in the expression of PACAP, VPAC1, VPAC2, PAC1 and testicular activity in the testis of the muskrat (Ondatra zibethicus)
Submitted: 18 February 2022
Accepted: 20 April 2022
Published: 2 May 2022
Accepted: 20 April 2022
Abstract Views: 683
PDF: 520
HTML: 61
HTML: 61
Publisher's note
All claims expressed in this article are solely those of the authors and do not necessarily represent those of their affiliated organizations, or those of the publisher, the editors and the reviewers. Any product that may be evaluated in this article or claim that may be made by its manufacturer is not guaranteed or endorsed by the publisher.
All claims expressed in this article are solely those of the authors and do not necessarily represent those of their affiliated organizations, or those of the publisher, the editors and the reviewers. Any product that may be evaluated in this article or claim that may be made by its manufacturer is not guaranteed or endorsed by the publisher.
Authors
Pituitary adenylate cyclase-activating polypeptide (PACAP) plays an important role in the steroidogenesis and spermatogenesis in the testis through its receptors PAC1, VPAC1, and VPAC2. In this study, we investigated the seasonal expressions of PACAP, PAC1, VPAC1, VPAC2, luteinizing hormone receptor (LHR), follicle stimulating hormone receptor (FSHR), steroidogenic acute regulatory protein (StAR), 3β-hydroxysteroid dehydrogenase (3β-HSD), and CYP17A1 in the testis of the male muskrat during the breeding season and the non-breeding season. Histologically, we found the presence of Leydig cells, Sertoli cells and all kinds of germ cells in the testis during the breeding season but only Leydig cells, Sertoli cells, spermatogonia and primary spermatocyte during the non-breeding season. The immunohistochemical localizations of PACAP and VPAC1 were identified in the Leydig cells, spermatogonia and spermatozoa during the breeding season while only in Leydig cells and spermatogonia during the non-breeding season, and PAC1 and VPAC2 were localized in the Leydig cells in both seasons, in which LHR, StAR, 3β-HSD and CYP17A1 were also expressed. Meanwhile, protein and mRNA expression levels of PACAP, PAC1, VPAC1, VPAC2, LHR, FSHR, StAR, 3β-HSD and CYP17A1 in the testis during the breeding season were significantly higher than those during the non-breeding season. These results suggested that PACAP may involve in the regulation of, steroidogenesis and spermatogenesis via an endocrine, autocrine or paracrine manner in the testis of the muskrat.
Miyata A, Arimura A, Dahl RR, Minamino N, Uehara A, Jiang L, et al. Isolation of a novel 38 residue-hypothalamic polypeptide which stimulates adenylate cyclase in pituitary cells. Biochem Biophys Res Commun 1989;164:567-74.
DOI: https://doi.org/10.1016/0006-291X(89)91757-9
Arimura A. Perspectives on pituitary adenylate cyclase activating polypeptide (PACAP) in the neuroendocrine, endocrine, and nervous systems. Jpn J Physiol 1998;48:301-31.
DOI: https://doi.org/10.2170/jjphysiol.48.301
Arimura A, Somogyvári-Vigh A, Miyata A, Mizuno K, Coy DH, Kitada C. Tissue distribution of PACAP as determined by RIA: highly abundant in the rat brain and testes. Endocrinology 1991;129:2787-9.
DOI: https://doi.org/10.1210/endo-129-5-2787
Sherwood NM, Krueckl SL, McRory JE. The origin and function of the pituitary adenylate cyclase-activating polypeptide (PACAP)/glucagon superfamily. Endocr Rev 2000;21:619-70.
DOI: https://doi.org/10.1210/edrv.21.6.0414
Vaudry D, Gonzalez BJ, Basille M, Yon L, Fournier A, Vaudry H. Pituitary adenylate cyclase-activating polypeptide and its receptors: from structure to functions. Pharmacol Rev 2000;52:269-324.
Gottschall PE, Tatsuno I, Miyata A, Arimura A. Characterization and distribution of binding sites for the hypothalamic peptide, pituitary adenylate cyclase-activating polypeptide. Endocrinology 1990;127:272-7.
DOI: https://doi.org/10.1210/endo-127-1-272
Basille M, Vaudry D, Coulouarn Y, Jegou S, Lihrmann I, Fournier A, et al. Comparative distribution of pituitary adenylate cyclase-activating polypeptide (PACAP) binding sites and PACAP receptor mRNAs in the rat brain during development. J Comp Neurol 2000;425:495-509.
DOI: https://doi.org/10.1002/1096-9861(20001002)425:4<495::AID-CNE3>3.0.CO;2-A
Vaudry D, Falluel-Morel A, Bourgault S, Basille M, Burel D, Wurtz O, et al. Pituitary Adenylate cyclase-activating polypeptide and its receptors: 20 years after the discovery. Pharmacol Rev 2009;61:283.
DOI: https://doi.org/10.1124/pr.109.001370
Thomas RL, Crawford NM, Grafer CM, Halvorson LM. Pituitary adenylate cyclase–activating polypeptide (PACAP) in the hypothalamic–pituitary–gonadal axis: A review of the literature. Reprod Sci 2013;20:857-71.
DOI: https://doi.org/10.1177/1933719112466310
Winters SJ, Moore JP. PACAP: A regulator of mammalian reproductive function. Mol Cell Endocrinol 2020;518:110912.
DOI: https://doi.org/10.1016/j.mce.2020.110912
Hannibal J, Fahrenkrug J. Expression of pituitary adenylate cyclase activating polypeptide (PACAP) gene by rat spermatogenic cells. Regul Pept 1995;55:111-5.
DOI: https://doi.org/10.1016/0167-0115(94)00110-J
Li M, Funahashi H, Mbikay M, Shioda S, Arimura A. Pituitary adenylate cyclase activating polypeptide-mediated intracrine signaling in the testicular germ cells. Endocrine 2004;23:59-75.
DOI: https://doi.org/10.1385/ENDO:23:1:59
Daniel PB, Habener JF. Pituitary adenylate cyclase-activating polypeptide gene expression regulated by a testis-specific promoter in germ cells during spermatogenesis. Endocrinology 2000;141:1218-27.
DOI: https://doi.org/10.1210/endo.141.3.7347
Prisco M, Rosati L, Morgillo E, Mollica MP, Agnese M, Andreuccetti P, et al. Pituitary adenylate cyclase-activating peptide (PACAP) and its receptors in Mus musculus testis. Gen Comp Endocrinol 2020;286:113297.
DOI: https://doi.org/10.1016/j.ygcen.2019.113297
Banks WA, Kastin AJ, Komaki G, Arimura A. Pituitary adenylate cyclase activating polypeptide (PACAP) can cross the vascular component of the blood-testis barrier in the mouse. J Andral 1993;14:170-3.
Lacombe A, Lelievre V, Roselli CE, Salameh W, Lue YH, Lawson G, et al. Delayed testicular aging in pituitary adenylate cyclase-activating peptide (PACAP) null mice. Proc Natl Acad Sci USA 2006;103:3793-8.
DOI: https://doi.org/10.1073/pnas.0505827103
Romanelli F, Fillo S, Isidori A, Conte D. Pituitary adenylate cyclase-activating polypeptide regulates rat Leydig cell function in vitro. Neuropeptides 1997;31:311-7.
DOI: https://doi.org/10.1016/S0143-4179(97)90064-0
Halvorson LM. PACAP modulates GnRH signaling in gonadotropes. Mol Cell Endocrinol 2014;385:45-55.
DOI: https://doi.org/10.1016/j.mce.2013.09.029
Purwana IN, Kanasaki H, Oride A, Mijiddorj T, Shintani N, Hashimoto H, et al. GnRH-induced PACAP and PAC1 receptor expression in pituitary gonadotrophs: A possible role in the regulation of gonadotropin subunit gene expression. Peptides 2010;31:1748-55.
DOI: https://doi.org/10.1016/j.peptides.2010.05.012
Radleff-Schlimme A, Leonhardt S, Wuttke W, Jarry H. Evidence for PACAP to be an autocrine factor on gonadotrope cells. Ann N Y Acad Sci 1998;865:486-91.
DOI: https://doi.org/10.1111/j.1749-6632.1998.tb11222.x
Doyle RE, Panneton WM, Vogler GA, Romeo JP, Watson BJ, Higgins B. The muskrat in biomedical research. J Am Assoc Lab Anim Sci 1988;38:667-74.
Xie W, Tang Z, Xu L, Zhong J, Zhang H, Han Y, et al. Seasonal expressions of SF-1, StAR and P450scc in the scent glands of the muskrats (Ondatra zibethicus). J Steroid Biochem Mol Biol 2020;204:105766.
DOI: https://doi.org/10.1016/j.jsbmb.2020.105766
Law AMK, Yin JXM, Castillo L, Young AIJ, Piggin C, Rogers S, et al. Andy's Algorithms: new automated digital image analysis pipelines for FIJI. Sci Rep 2017;7:15717.
DOI: https://doi.org/10.1038/s41598-017-15885-6
Han X, Ran Y, Su M, Liu Y, Tang W, Dong Z, et al. Chronic changes in pituitary adenylate cyclase-activating polypeptide and related receptors in response to repeated chemical dural stimulation in rats. Mol Pain 2017;13:1744806917720361.
DOI: https://doi.org/10.1177/1744806917720361
Wang J, Wang Y, Zhu M, Zhang F, Sheng X, Zhang H, et al. Seasonal expression of luteinizing hormone receptor and follicle stimulating hormone receptor in testes of the wild ground squirrels (Citellus dauricus Brandt). Acta Histochem 2017;119:727-32.
DOI: https://doi.org/10.1016/j.acthis.2017.09.004
Weng Q, Murase T, Tsubota T. Seasonal changes in spermatogenesis and testicular steroidogenesis in wild male raccoon dogs (Nyctereutes procynoides). J Vet Med Sci 2003;65.
DOI: https://doi.org/10.1292/jvms.65.1087
Shivers BD, Görcs TJ, Gottschall PE, Arimura A. Two high affinity binding sites for pituitary adenylate cyclase-activating polypeptide have different tissue distributions. Endocrinology 1991;128:3055-65.
DOI: https://doi.org/10.1210/endo-128-6-3055
Shioda S, Legradi G, Leung WC, Nakajo S, Nakaya K, Arimura A. Localization of pituitary adenylate cyclase-activating polypeptide and its messenger ribonucleic acid in the rat testis by light and electron microscopic immunocytochemistry and in situ hybridization. Endocrinology 1994;135:818-25.
DOI: https://doi.org/10.1210/endo.135.3.8070375
Matsumoto S, Arakawa Y, Ohishi M, Yanaihara H, Iwanaga T, Kurokawa N. Suppressive action of pituitary adenylate cyclase activating polypeptide (PACAP) on proliferation of immature mouse Leydig cell line TM3 cells. Biomed Res 2008;29:321-30.
DOI: https://doi.org/10.2220/biomedres.29.321
Brubel R, Kiss P, Vincze A, Varga A, Varnagy A, Bodis J, et al. Effects of pituitary adenylate cyclase activating polypeptide on human sperm motility. J Mol Neurosci 2012;48:623-30.
DOI: https://doi.org/10.1007/s12031-012-9806-5
Rosati L, Prisco M, Coraggio F, Valiante S, Scudiero R, Laforgia V, et al. PACAP and PAC1 receptor in the reproductive cycle of male lizard Podarcis sicula. Gen Comp Endocrinol 2014;205:102-8.
DOI: https://doi.org/10.1016/j.ygcen.2014.05.009
Tanii I, Aradate T, Matsuda K, Komiya A, Fuse H. PACAP-mediated sperm-cumulus cell interaction promotes fertilization. Reproduction 2011;141:163-71.
DOI: https://doi.org/10.1530/REP-10-0201
Heindel JJ, Powell CJ, Paschall CS, Arimura A, Culler MD. A Novel hypothalamic peptide, pituitary adenylate cyclase activating peptide, modulates Sertoli cell function in vitro. Biol Reprod 1992;47:800-6.
DOI: https://doi.org/10.1095/biolreprod47.5.800
Lv CM, Cheng DL, Zhao W, Zhu H. Pituitary adenylate cyclase-activating polypeptide mRNA expression in rat testis and epididymis during postnatal development and experimental cryptorchidism. Mol Med Rep 2011;4:793-8.
Moore JP, Jr., Yang RQ, Winters SJ. Targeted pituitary overexpression of pituitary adenylate-cyclase activating polypeptide alters postnatal sexual maturation in male mice. Endocrinology 2012;153:1421-34.
DOI: https://doi.org/10.1210/en.2011-1115
El-Gehani F, Tena-Sempere M, Huhtaniemi I. Evidence that pituitary adenylate cyclase-activating polypeptide is a potent regulator of fetal rat testicular steroidogenesis. Biol Reprod 2000;63:1482-9.
DOI: https://doi.org/10.1095/biolreprod63.5.1482
El-Gehani F, Zhang FP, Pakarinen P, Rannikko A, Huhtaniemi I. Gonadotropin-independent regulation of steroidogenesis in the fetal rat testis. Biol Reprod 1998;58:116-23.
DOI: https://doi.org/10.1095/biolreprod58.1.116
Watts HE. Seasonal regulation of behaviour: what role do hormone receptors play? Proc Royal Soc B 2020;287:20200722.
DOI: https://doi.org/10.1098/rspb.2020.0722
Shuto Y, Somogyvári-Vigh A, Shioda S, Onda H, Arimura A. Effect of hypophysectomy on pituitary adenylate cyclase-activating polypeptide gene expression in the rat testis. Peptides 1995;16:1039-44.
DOI: https://doi.org/10.1016/0196-9781(95)00080-4
Moore JP, Jr, Burger LL, Dalkin AC, Winters SJ. Pituitary adenylate cyclase activating polypeptide messenger RNA in the paraventricular nucleus and anterior pituitary during the rat estrous cycle. Biol Reprod 2005;73:491-9.
DOI: https://doi.org/10.1095/biolreprod.105.041624
Ethics Approval
All animals were treated according to the Policy on the Care and Use of Animals by the Ethical Committee and Animal Welfare Committee and all procedures were approved by Beijing Forestry University, China (EAWC_BJFU_2022003)How to Cite
Tang, Z., Yuan, X., Bai, Y., Guo, Y., Zhang, H., Han, Y., … Weng, Q. (2022). Seasonal changes in the expression of PACAP, VPAC1, VPAC2, PAC1 and testicular activity in the testis of the muskrat (<em>Ondatra zibethicus</em>). European Journal of Histochemistry, 66(2). https://doi.org/10.4081/ejh.2022.3398
Copyright (c) 2022 The Author(s)
This work is licensed under a Creative Commons Attribution-NonCommercial 4.0 International License.
PAGEPress has chosen to apply the Creative Commons Attribution NonCommercial 4.0 International License (CC BY-NC 4.0) to all manuscripts to be published.
Similar Articles
- Claudia Lombardo, Grazia Maugeri, Agata Grazia D'Amico, Giuseppe Broggi, Rosario Caltabiano, Veronica Filetti, Serena Matera, Velia D'Agata, Carla Loreto, Pleural mesothelioma from fluoro-edenite exposure: PACAP and PAC1 receptor. A preliminary report , European Journal of Histochemistry: Vol. 68 No. 2 (2024)
- M. Acosta, V. Filippa, F. Mohamed, Folliculostellate cells in pituitary pars distalis of male viscacha: immunohistochemical, morphometric and ultrastructural study , European Journal of Histochemistry: Vol. 54 No. 1 (2010)
- C. Fede, G. Albertin, L. Petrelli, M.M. Sfriso, C. Biz, R. De Caro, C. Stecco, Expression of the endocannabinoid receptors in human fascial tissue , European Journal of Histochemistry: Vol. 60 No. 2 (2016)
- H. Zhang, Y. Wang, J. Zhang, L. Wang, Q. Li, X. Sheng, Y. Han, Z. Yuan, Q. Weng, Testicular expression of NGF, TrkA and p75 during seasonal spermatogenesis of the wild ground squirrel (Citellus dauricus Brandt) , European Journal of Histochemistry: Vol. 59 No. 3 (2015)
- M. A. Sandhu, Z. U. Rahman, A. Riaz, S. U. Rahman, I. Javed, N. Ullah, Somatotrophs and lactotrophs: an immunohistochemical study of Gallus domesticus pituitary gland at different stages of induced moult , European Journal of Histochemistry: Vol. 54 No. 2 (2010)
- Mariailaria Verderame, Ermelinda Limatola, Rosaria Scudiero, Metallothionein expression and synthesis in the testis of the lizard Podarcis sicula under natural conditions and following estrogenic exposure , European Journal of Histochemistry: Vol. 61 No. 2 (2017)
- Viktória Dénes, Kármen Kovacs, Ákos Lukáts, Adrienn Mester, Gergely Berta, Arnold Szabó, Robert Gabriel, Secreted key regulators (Fgf1, Bmp4, Gdf3) are expressed by PAC1-immunopositive retinal ganglion cells in the postnatal rat retina , European Journal of Histochemistry: Vol. 66 No. 2 (2022)
- M. A. Sandhu, A. A. Saeed, M. S. Khilji, R. H. Pasha, N. Mukhtar, M. S. Anjum, Ontogenic development of corticotrophs in fetal buffalo (Bubalus bubalis) pituitary gland , European Journal of Histochemistry: Vol. 58 No. 1 (2014)
- Q. Li, F. Zhang, S. Zhang, X. Sheng, X. Han, Q. Weng, Z. Yuan, Seasonal expression of androgen receptor, aromatase, and estrogen receptor alpha and beta in the testis of the wild ground squirrel (Citellus dauricus Brandt) , European Journal of Histochemistry: Vol. 59 No. 1 (2015)
- L. Bao, Q. Li, Y. Liu, B. Li, X. Sheng, Y. Han, Q. Weng, Immunolocalization of NGF and its receptors in ovarian surface epithelium of the wild ground squirrel during the breeding and nonbreeding seasons , European Journal of Histochemistry: Vol. 58 No. 2 (2014)
You may also start an advanced similarity search for this article.
Publication Facts
Metric
This article
Other articles
Peer reviewers
2
2.4
Reviewer profiles N/A
Author statements
Author statements
This article
Other articles
Data availability
N/A
16%
External funding
N/A
32%
Competing interests
N/A
11%
Metric
This journal
Other journals
Articles accepted
57%
33%
Days to publication
72
145
- Editor & editorial board
- profiles
- Academic society
- N/A
- Publisher
- PAGEPress Publications, Pavia, Italy
To learn about these publication facts, click 
PF is maintained by the Public Knowledge Project
