Hostname: page-component-76fb5796d-skm99 Total loading time: 0 Render date: 2024-04-26T17:15:20.564Z Has data issue: false hasContentIssue false
  • English
  • Français

Study on PREP localization in mouse seminal vesicles and its possible involvement during regulated exocytosis

Published online by Cambridge University Press:  07 May 2019

Massimo Venditti ,
Francesco Aniello ,
Alessandra Santillo  and
Sergio Minucci Open the ORCID record for Sergio Minucci [Opens in a new window]
Massimo Venditti
Affiliation:
Dipartimento di Medicina Sperimentale, Sez. Fisiologia Umana e Funzioni Biologiche Integrate ‘F. Bottazzi’, Università degli Studi della Campania ‘Luigi Vanvitelli’, via Costantinopoli 16, 80138Napoli, Italy
Francesco Aniello
Affiliation:
Dipartimento di Biologia, Università degli Studi di Napoli ‘Federico II’, via Cinthia 26, 80126Napoli, Italy
Alessandra Santillo
Affiliation:
Dipartimento di Scienze e Tecnologie Ambientali, Biologiche e Farmaceutiche, Università degli Studi della Campania ‘Luigi Vanvitelli’, via Vivaldi 43, 81100Caserta, Italy
Sergio Minucci*
Affiliation:
Dipartimento di Medicina Sperimentale, Sez. Fisiologia Umana e Funzioni Biologiche Integrate ‘F. Bottazzi’, Università degli Studi della Campania ‘Luigi Vanvitelli’, via Costantinopoli 16, 80138Napoli, Italy
*
Address for correspondence: Sergio Minucci, Dipartimento di Medicina Sperimentale, Sez. Fisiologia Umana e Funzioni Biologiche Integrate ‘F. Bottazzi’, Università degli Studi della Campania ‘Luigi Vanvitelli’, via Costantinopoli 16, 80138 Napoli. Tel: +39 081 5665829. Fax: +39 081 5667500. E-mail: sergio.minucci@unicampania.it
Get access Rights & Permissions [Opens in a new window]

Summary

Prolyl endopeptidase (PREP) is a post-proline cleaving enzyme. It is involved in the regulation of multiple inositol polyphosphate phosphatase activity implicated in the pathway of inositol 1,4,5-trisphosphate, resulting in the modulation of cytosolic Ca2+ levels. Besides its peptidase activity, PREP was identified as a binding partner of tubulin, suggesting that it may participate in microtubule-associate processes. In this paper, we evaluated the expression of PREP mRNA and protein by polymerase chain reaction and western blot analyses and its co-localization with tubulin by immunofluorescence in adult mouse seminal vesicles. We showed that both proteins are cytoplasmic: tubulin is localized at the apical half part of the cell, while PREP has a more diffuse localization, showing a prominent distribution at the apical cytoplasm. These findings support our hypothesis of a specific role for PREP in cytoskeletal rearrangement that occurs during the exocytosis of secretory vesicles, and in particular its association with tubulin filaments. Moreover, it may regulate Ca2+ levels, and promote the final step of vesicular exocytosis, namely the fusion of the vesicles with the plasma membrane. These results strongly suggest that there is a pivotal role for PREP in vesicle exocytosis, as well as in the physiology of mouse seminal vesicles.

Keywords

CytoskeletonExocrine glandProlyl endopeptidaseRegulated exocytosisSeminal vesiclesTubulin
Type
Research Article
Information
Zygote , Volume 27 , Issue 3 , June 2019 , pp. 160 - 165
Copyright
© Cambridge University Press 2019 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Aumüller, G and Seitz, J (1990) Protein secretion and secretory processes in male accessory sex glands. Int Rev Cytol 121, 127–231.Google Scholar
Aoyagi, T, Wada, T, Nagai, M, Kojima, F, Harada, S, Takeuchi, T, Takahashi, H and Tsumita, T (1990) Deficiency of kallikrein-like enzyme activities in cerebral tissue of patients with Alzheimer’s disease. Experientia 6, 94–97.Google Scholar
Bär, JW, Rahfeld, JU, Schulz, I, Gans, K, Ruiz-Carrillo, D, Manhart, S, Rosche, F and Demuth, HU (2006) Prolyl endopeptidase cleaves the apoptosis rescue peptide humanin and exhibits an unknown post-cysteine cleavage specificity. Adv Exp Med Biol 575, 103–108.Google Scholar
Bellemère, G, Morain, P, Vaudry, H and Jégou, S (2003) Effect of S17092, a novel prolyl endopeptidase inhibitor, on substance P and alpha-melanocyte-stimulating hormone breakdown in the rat brain. J Neurochem 84, 919–929.Google Scholar
Burgess, TL and Kelly, RB (1987) Constitutive and regulated secretion of proteins. Annu Rev Cell Biol 3, 243–293.Google Scholar
Chemek, M, Venditti, M, Boughamoura, S, Mimouna, SB, Messaoudi, I and Minucci, S (2018) Involvement of testicular DAAM1 expression in zinc protection against cadmium-induced male rat reproductive toxicity. J Cell Physiol 233, 630–640.Google Scholar
D’Agostino, G, Kim, JD, Liu, ZW, Jeong, JK, Suyama, S, Calignano, A, Gao, XB, Schwartz, M and Diano, S (2013) Prolyl endopeptidase-deficient mice have reduced synaptic spine density in the CA1 region of the hippocampus, impaired LTP, and spatial learning and memory. Cereb Cortex 23, 2007–2014.Google Scholar
Dotolo, R, Kim, JD, Pariante, P, Minucci, S and Diano, S (2016) Prolyl endopeptidase (PREP) is associated with male reproductive functions and gamete physiology in mice. J Cell Physiol 231, 551–557.Google Scholar
Flickinger, CJ (1974) Synthesis, intracellular transport and release of secretory protein in the seminal vesicle of the rat, as studied by electron microscope radioautography. Anat Rec 180, 407–427.Google Scholar
Fülöp, V, Böcskei, Z and Polgár, L (1998) Prolyl oligopeptidase: an unusual beta-propeller domain regulates proteolysis. Cell 94, 161–170.Google Scholar
Hannula, MJ, Myöhänen, TT, Tenorio-Laranga, J, Männistö, PT and Garcia-Horsman, JA (2013) Prolyl oligopeptidase colocalizes with α-synuclein, β-amyloid, tau protein and astroglia in the post-mortem brain samples with Parkinson’s and Alzheimer’s diseases. Neuroscience 242, 140–150.Google Scholar
Irazusta, J, Larrinaga, G, González-Maeso, J, Gil, J, Meana, JJ and Casis, L (2002) Distribution of prolyl endopeptidase activities in rat and human brain. Neurochem Int 40, 337–345.Google Scholar
James, DJ and Martin, TF (2013) CAPS and Munc13: CATCHRs that SNARE vesicles. Front Endocrinol 4, 187.Google Scholar
Kato, T, Nakano, T, Kojima, K, Nagatsu, T and Sakakibara, S (1980) Changes in prolyl endopeptidase during maturation of rat brain and hydrolysis of substance P by the purified enzyme. J Neurochem 35, 527–535.Google Scholar
Kimura, A, Ohnishi, J, Okimura, H, Hamabata, T and Takahashi, T (1998) Localization of prolyl endopeptidase mRNA in small growing follicles of porcine ovary. Mol Reprod Dev 50, 121–127.Google Scholar
Kimura, A, Matsui, H and Takahashi, T (2002) Expression and localization of prolyl oligopeptidase in mouse testis and its possible involvement in sperm motility. Zoo Sci 19, 93–102.Google Scholar
Maruyama, Y, Matsubara, S and Kimura, AP (2017) Mouse prolyl oligopeptidase plays a role in trophoblast stem cell differentiation into trophoblast giant cell and spongiotrophoblast. Placenta 53, 8–15.Google Scholar
Matsubara, Y, Ono, T, Tsubuki, S, Irie, S and Kawashima, S (1998) Transient up-regulation of a prolyl endopeptidase activity in the microsomal fraction of rat liver during postnatal development. Eur J Biochem 252, 178–183.Google Scholar
Matsuda, T, Sakaguchi, M, Tanaka, S, Yoshimoto, T and Takaoka, M (2013) Prolyl oligopeptidase is a glyceraldehyde-3-phosphate dehydrogenase-binding protein that regulates genotoxic stress-induced cell death. Int J Biochem Cell Biol 45, 850–857.Google Scholar
Mentlein, R (1988) Proline residues in the maturation and degradation of peptide hormones and neuropeptides. FEBS Lett 234, 251–256.Google Scholar
Messenger, SW, Falkowski, MA and Groblewski, GE (2014) Ca2+-regulated secretory granule exocytosis in pancreatic and parotid acinar cells. Cell Calcium 55, 369–375.Google Scholar
Mikoshiba, K (1993) Inositol 1,4,5-triphosphate receptor. Trends Pharmacol Sci 14, 86–89.Google Scholar
Morawski, M, Schulz, I, Zeitschel, U, Blosa, M, Seeger, G and Rossner, S (2011) Role of prolyl endopeptidase in intracellular transport and protein secretion. CNS Neurol Disord Drug Targets 10, 327–332.Google Scholar
Myöhänen, TT, Venäläinen, JI, Garcia-Horsman, JA and Männistö, PT (2008) Spatial association of prolyl oligopeptidase, inositol 1,4,5-triphosphate type 1 receptor, substance P and its neurokinin-1 receptor in the rat brain: an immunohistochemical colocalization study. Neuroscience 153, 1177–1189.Google Scholar
Myöhänen, TT, Pyykkö, E, Männistö, PT and Carpen, O (2012) Distribution of prolyl oligopeptidase in human peripheral tissues and in ovarian and colorectal tumors. J Histochem Cytochem 60, 706–715.Google Scholar
Müsch, A (2004) Microtubule organization and function in epithelial cells. Traffic 5, 1–9.Google Scholar
Noordstra, I and Akhmanova, A (2017) Linking cortical microtubule attachment and exocytosis. F1000Res 6, 469.Google Scholar
Ohtsuki, S, Homma, K, Kurata, S, Komano, H and Natori, S (1994) A prolyl endopeptidase of Sarcophaga peregrina (flesh fly): its purification and suggestion for its participation in the differentiation of the imaginal discs. J Biochem 115, 449–453.Google Scholar
Pariante, P, Dotolo, R, Venditti, M, Ferrara, D, Donizetti, A, Aniello, F and Minucci, S (2016) First evidence of DAAM1 localization during the post-natal development of rat testis and in mammalian sperm. J Cell Physiol 231, 2172–2184.Google Scholar
Park, JJ and Loh, YP (2008) How peptide hormone vesicles are transported to the secretion site for exocytosis. Mol Endocrinol 22, 2583–2595.Google Scholar
Petersen, OH (2014) Calcium signalling and secretory epithelia. Cell Calcium 55, 282–289.Google Scholar
Petersen, OH and Tepikin, AV (2008) Polarized calcium signaling in exocrine gland cells. Annu Rev Physiol 70, 273–299.Google Scholar
Raveh, A, Valitsky, M, Shani, L, Coorssen, JR, Blank, PS, Zimmerberg, J and Rahamimoff, R (2012) Observations of calcium dynamics in cortical secretory vesicles. Cell Calcium 52, 217–225.Google Scholar
Rossner, S, Schulz, I, Zeitschel, U, Schliebs, R, Bigl, V and Demuth, HU (2005) Brain prolyl endopeptidase expression in aging, APP transgenic mice and Alzheimer’s disease. Neurochem Res 30, 695–702.Google Scholar
Schulz, I, Gerhartz, B, Neubauer, A, Holloschi, A, Heiser, U, Hafner, M and Demuth, HU (2002) Modulation of inositol 1,4,5-triphosphate concentration by prolyl endopeptidase inhibition. Eur J Biochem 269, 5813–5820.Google Scholar
Schulz, I, Zeitschel, U, Rudolph, T, Ruiz-Carrillo, D, Rahfeld, JU, Gerhartz, B, Bigl, D, Demuth, HU and Rossner, S (2005) Subcellular localization suggests novel functions for prolyl endopeptidase in protein secretion. J Neurochem 94, 970–979.Google Scholar
Spring-Mills, E, and Hafez, ESE (1979) Functional anatomy and histology. In E.S.E. Hafez and E. Spring-Mills (eds). Accessory Glands of Male Reproductive Tract. Ann Arbor Sci Ann Arbor MI, USA, pp. 29–57.Google Scholar
Suzuki, K, Sakaguchi, M, Tanaka, S, Yoshimoto, T and Takaoka, M (2014) Prolyl oligopeptidase inhibition-induced growth arrest of human gastric cancer cells. Biochem Biophys Res Commun 443, 91–96.Google Scholar
Szeltner, Z and Polgár, L (2008) Structure, function and biological relevance of prolyl oligopeptidase. Curr Protein Pept Sci 9, 96–107.Google Scholar
Taylor, WL, Andrews, PC, Henrikson, CK and Dixon, JE (1980) New fluorogenic substrates for a rat brain proline endopeptidase. Anal Biochem 105, 58–64.Google Scholar
Toide, K, Okamiya, K, Iwamoto, Y and Kato, T (1995) Effect of a novel prolyl endopeptidase inhibitor, JTP-4819, on prolyl endopeptidase activity and substance P- and arginine-vasopressin-like immunoreactivity in the brains of aged rats. J Neurochem 65, 234–240.Google Scholar
Valdivia, A, Irazusta, J, Fernández, D, Múgica, J, Ochoa, C and Casis, L (2004) Pyroglutamyl peptidase I and prolyl endopeptidase in human semen: increased activity in necrozoospermia. Regul Pept 122, 79–84.Google Scholar
Venäläinen, JI, Juvonen, RO and Männistö, PT (2004) Evolutionary relationships of the prolyl oligopeptidase family enzymes. Eur J Biochem 271, 2705–2715.Google Scholar
Venditti, M and Minucci, S (2018) Subcellular localization of prolyl endopeptidase (PREP) during the first wave of rat spermatogenesis and in rat and human sperm. J Histochem Cytochem 67, 229–243.Google Scholar
Venditti, M, Fasano, C, Santillo, A, Aniello, F and Minucci, S (2018) First evidence of DAAM1 localization in mouse seminal vesicles and its possible involvement during regulated exocytosis. CR Biol 341, 228–234.Google Scholar
Verhage, M and Sorensen, JB (2008) Vesicle docking in regulated exocytosis. Traffic 9, 1414–1424.Google Scholar
Walter, R, Shlank, H, Glass, JD, Schwartz, IL and Kerenyi, TD (1971) Leucylglycinamide released from oxytocin by human uterine enzyme. Science 173, 827–829.Google Scholar
Walter, R (1976) Partial purification and characterization of post-proline cleaving enzyme: enzymatic inactivation of neurohypophyseal hormones by kidney preparations of various species. Biochim Biophys Acta 422, 138–158.Google Scholar
Wilk, S (1983) Prolyl endopeptidase. Life Sci 33, 2149–2157.Google Scholar
Williams, RS, Eames, M, Ryves, WJ, Viggars, J and Harwood, AJ (1999) Loss of a prolyl oligopeptidase confers resistance to lithium by elevation of inositol(1,4,5)-trisphosphate. EMBO J 18, 2734–2745.Google Scholar
Wu, LG, Hamid, E, Shin, W and Chiang, HC (2014) Exocytosis and endocytosis: modes, functions, and coupling mechanisms. Annu Rev Physiol 76, 301–331.Google Scholar
Yokosawa, H, Miyata, M, Sawada, H and Ishii, S (1983) Isolation and characterization of a postproline cleaving enzyme and its inhibitor from sperm of the ascidian, Halocynthia roretzi . J Biochem 94, 1067–1076.Google Scholar
Yoo, SH (2011) Role of secretory granules in inositol 1,4,5-trisphosphate-dependent Ca2+ signaling: from phytoplankton to mammals. Cell Calcium 50, 175–183.Google Scholar
Yoshida, K, Inaba, K, Ohtake, H and Morisawa, M (1999) Purification and characterization of prolyl endopeptidase from the Pacific herring, Clupea pallasi, and its role in the activation of sperm motility. Dev Growth Differ 41, 217–225.Google Scholar
Yoshimoto, T, Ogita, K, Walter, R, Koida, M and Tsuru, D (1979) Post-proline cleaving enzyme. Synthesis of a new fluorogenic substrate and distribution of the endopeptidase in rat tissues and body fluids of man. Biochim Biophys Acta 569, 184–192.Google Scholar