Identification of a plasma membrane Ca<sup>2+</sup>‐ATPase in epithelial cells and aposomes of the rat coagulating gland

Post, Heidi; Wiche, Regina; Sen, Parimal C.; Hoffbauer, Gudrun; Albrecht, Martín; Seitz, Jürgen; Aumüller, Gerhard; Wilhelm, Beate

doi:10.1002/pros.10109

Cited by 14 publications

(5 citation statements)

References 42 publications

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“…5A). The expression of murine PMCA4a in the apical plasma membranes of the epididymis strongly suggests that it is secreted into the lumen: PMCA concentrated in glandular epithelial cells in a variety of tissues is known to be secreted (e.g., into milk from the apical membrane of lactating mammary gland epithelia) [34][35][36][37]. Indeed, Western blots revealed that the ELF from each epididymal region contained the ;128-kDa PMCA4a variant (Fig.…”

Section: Pmca4 Splice Variants Are Differentially Expressed In Testismentioning

confidence: 93%

Plasma Membrane Ca2+-ATPase 4 in Murine Epididymis: Secretion of Splice Variants in the Luminal Fluid and a Role in Sperm Maturation1

Patel

Al‐Dossary

Stabley

et al. 2013

Biology of Reproduction

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Plasma membrane Ca(2+)-ATPase isoform 4 (PMCA4) is the primary Ca(2+) efflux pump in murine sperm, where it regulates motility. In Pmca4 null sperm, motility loss results in infertility. We have shown that murine sperm PMCA4b interacts with Ca(2+)/CaM-dependent serine kinase (CASK) in regulating Ca(2+) homeostasis and motility. However, recent work indicated that the bovine PMCA4a splice variant (missing in testis) is epididymally expressed, along with 4b, and may be transferred to sperm. Here we show, via conventional and in situ RT-PCR, that both the splice variants of Pmca4 mRNA are expressed in murine testis and throughout the epididymis. Immunofluorescence localized PMCA4a to the apical membrane of the epididymal epithelium, and Western analysis not only confirmed its presence but showed for the first time that PMCA4a and PMCA4b are secreted in the epididymal luminal fluid (ELF), from which epididymosomes containing PMCA4a were isolated. Flow cytometry indicated the presence of PMCA4a on mature caudal sperm where it was increased ~5-fold compared to caput sperm (detected by Western blotting) and ~2-fold after incubation in ELF, revealing in vitro uptake and implicating PMCA4a in epididymal sperm maturation. Coimmunoprecipitation using pan-PMCA4 antibodies, revealed that both variants associate with CASK, suggesting their presence in a complex. Because they have different kinetic properties for Ca(2+) transport and different abilities to bind to CASK, our study suggests a mechanism for combining the functional attributes of both PMCA4 variants, leading to heightened efficiency of the pump in the maintenance of Ca(2+) homeostasis, which is crucial for normal motility and male fertility.

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Section: Pmca4 Splice Variants Are Differentially Expressed In Testismentioning

confidence: 93%

Plasma Membrane Ca2+-ATPase 4 in Murine Epididymis: Secretion of Splice Variants in the Luminal Fluid and a Role in Sperm Maturation1

Patel

Al‐Dossary

Stabley

et al. 2013

Biology of Reproduction

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“…The exact function of the cells with a "knobbled" apical surface, also referred to as blebs or cells with pitted surfaces (Motta and Andrews, 1976;Post et al, 2002), is unknown, although they may also be associated with apocrine secretions (Girling, 2002). Aposomes, which are the apical protrusions of the plasma membrane prior to apocrine secretion, are initially derived from apical microvilli (Post et al, 2002).…”

Section: Morphological Attributes Suggesting Histotrophic Nutrient Trmentioning

confidence: 99%

“…Aposomes, which are the apical protrusions of the plasma membrane prior to apocrine secretion, are initially derived from apical microvilli (Post et al, 2002). After an apical portion of the cell pinches off from the plasma membrane, the remaining part of the cell repairs itself and repeats the secretory process (Tortora and Grabowski, 1996).…”

Section: Morphological Attributes Suggesting Histotrophic Nutrient Trmentioning

confidence: 99%

Cyto‐epitheliochorial placenta of the viviparous lizard Pseudemoia entrecasteauxii: A new placental morphotype

Adams

Biazik

Thompson

et al. 2005

Journal of Morphology

114

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The structural features of the uterine epithelium of the chorioallantoic placenta and omphalloplacenta in the viviparous Australian skink, Pseudemoia entrecasteauxii, were investigated using SEM and TEM techniques. In particular, the structural characteristics that would allow interpretation of function were analyzed, particularly those of gas exchange in the chorioallantoic placenta and histotrophy in the omphaloplacenta. Pseudemoia entrecasteauxii has a complex placenta consisting of a placentome, paraplacentome, and omphaloplacenta. The paraplacentome has a well-vascularized lamina propria in which projecting uterine capillaries displace the overlying uterine epithelial cells, reducing them to attenuated cytoplasmic extensions. Associated cell nuclei and organelles are lost from this region, to provide a capillary lumen to uterine lumen barrier of 0.5-1.0 microm. Hence, the paraplacentome is likely a prominent site for gaseous exchange via simple diffusion. The omphaloplacenta has a similar cytology to that of the placentome, but the uterine epithelial cells are hypertrophied and the apical plasma membrane actively secretes vesicles into the uterine lumen. The omphaloplacenta shows features that are associated with histotrophic transport of nutrients via vesicle secretion, very similar to that of lipid apocrine secretion. The placentome consists of cuboidal cells in the uterine epithelium, with large centrally located nuclei overlying the well-vascularized lamina propria. Although the placentome has a similar cytological structure to that of the omphaloplacenta, granules or active vesicle secretion were not observed. Thus, the placentome may be associated with histotrophy, but not via apocrine secretion. Squamate placentation is epitheliochorial; however, we propose a new term be used to describe the type of placentation in P. entrecasteauxii: "cyto-epitheliochorial," because of the extreme attenuation of uterine epithelial cells of the paraplacentome.

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“…in the intestines and distal tubules of the kidney (Friedman and Gesek 1995;Hoenderop et al 2002;Larsson and Nemere 2002). In secretory epithelial cells such as pancreatic acinar cells, salivary gland cells and in epithelial cells of the rat-coagulating gland, PMCA is largely concentrated in the apical plasma membrane (Belan et al 1996; Lee et al 1997;Post et al 2002). The principal cells of the epididymis combine both resorptive and secretory functions (Cooper 1999), therefore, the localization of PMCA in the plasma membrane in the caput epididymidis is conclusive; it indicates that PMCA4 contributes substantially to vectorial, transcellular Ca 2+ transport from the apical to the basolateral compartment.…”

Section: Distribution Of Pmca4 In Rat Epididymismentioning

confidence: 99%

Expression and localization of PMCA4 in rat testis and epididymis

Wilhelm

Brandenburger

Post

et al. 2007

Histochem Cell Biol

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It has recently been shown in mice that the plasma membrane Ca(2+)-ATPase isoform 4 (PMCA4) is essential for sperm fertilization capacity. We analyzed whether sperm PMCA4 is formed in the rat during spermatogenesis or is synthesized in the epididymis and transferred onto sperm during sperm maturation. We could show that PMCA4 is conserved in sperm from testis to epididymis. In testis, PMCA4 mRNA was restricted to spermatogonia and early spermatocytes, while the PMCA4 protein was detected in spermatogonia, late spermatocytes, spermatids and in epididymal sperm. In epididymis PMCA4 mRNA was localized in basolateral plasma membranes of epithelial cells of the caput, corpus and cauda epididymidis. In contrast, the protein was only detectable in the epithelial cells of the caput, indicating that PMCA4 mRNA is only translated into protein in caput epithelium. In the epididymal corpus and cauda, PMCA4 mRNA and protein, respectively, was localized and in peritubular cells. Furthermore, we detected an identical distribution of PMCA4a and b splice variants in rat testis, epididymal corpus and cauda. In the caput epididymidis, where PMCA4 is located in the epithelium splice variant 4b was more prominent. Further experiments have to clarify the functional importance of the differences in the PMCA4 distribution.

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Identification of a plasma membrane Ca²⁺‐ATPase in epithelial cells and aposomes of the rat coagulating gland

Abstract: We show for the first time that Ca(2+)-ATPase as an important, functionally active membrane protein of the apical plasma membrane is incorporated into the aposomal membranes and is released from the cells during apocrine secretion process.

Cited by 14 publications

References 42 publications

Plasma Membrane Ca2+-ATPase 4 in Murine Epididymis: Secretion of Splice Variants in the Luminal Fluid and a Role in Sperm Maturation1

Plasma Membrane Ca2+-ATPase 4 in Murine Epididymis: Secretion of Splice Variants in the Luminal Fluid and a Role in Sperm Maturation1

Cyto‐epitheliochorial placenta of the viviparous lizard Pseudemoia entrecasteauxii: A new placental morphotype

Expression and localization of PMCA4 in rat testis and epididymis

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Identification of a plasma membrane Ca2+‐ATPase in epithelial cells and aposomes of the rat coagulating gland

Abstract: We show for the first time that Ca(2+)-ATPase as an important, functionally active membrane protein of the apical plasma membrane is incorporated into the aposomal membranes and is released from the cells during apocrine secretion process.

Cited by 14 publications

References 42 publications

Plasma Membrane Ca2+-ATPase 4 in Murine Epididymis: Secretion of Splice Variants in the Luminal Fluid and a Role in Sperm Maturation1

Plasma Membrane Ca2+-ATPase 4 in Murine Epididymis: Secretion of Splice Variants in the Luminal Fluid and a Role in Sperm Maturation1

Cyto‐epitheliochorial placenta of the viviparous lizard Pseudemoia entrecasteauxii: A new placental morphotype

Expression and localization of PMCA4 in rat testis and epididymis

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Identification of a plasma membrane Ca²⁺‐ATPase in epithelial cells and aposomes of the rat coagulating gland