Intracellular localisation of SNARE proteins in rat parotid acinar cells: SNARE complexes on the apical plasma membrane

Imai, Akane; Nashida, Tomoko; Souma, Yoshie; Shimomura, Hiromi

doi:10.1016/s0003-9969(03)00116-x

Cited by 40 publications

(41 citation statements)

References 35 publications

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“…Several studies revealed that the SNARE components are also present in the rat parotid and human submandibular glands, as part of the secretory machinery (22,51,53), in support of our hypothesis that PAP also regulates endo-/exocytosis in the mouse SMG. In addition, it has been reported that a PAP-like acid phosphatase activity is present in human endometrial glands during the secretory, but not the proliferative, phase (40).…”

Section: Discussionsupporting

confidence: 89%

Prostatic acid phosphatase is the main acid phosphatase with 5′-ectonucleotidase activity in the male mouse saliva and regulates salivation

Araujo

Quintero

Kipar

et al. 2014

American Journal of Physiology-Cell Physiology

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Araujo CL, Quintero IB, Kipar A, Herrala AM, Pulkka AE, Saarinen L, Hautaniemi S, Vihko P. Prostatic acid phosphatase is the main acid phosphatase with 5=-ectonucleotidase activity in the male mouse saliva and regulates salivation. Am J Physiol Cell Physiol 306: C1017-C1027, 2014. First published April 9, 2014; doi:10.1152/ajpcell.00062.2014.-We have previously shown that in addition to the well-known secreted isoform of prostatic acid phosphatase (sPAP), a transmembrane isoform exists (TMPAP) that interacts with snapin (a SNARE-associated protein) and regulates the endo-/exocytic pathways. We have also shown that PAP has 5=-ectonucleotidase and thiamine monophosphatase activity and elicits antinociceptive effects in mouse models of chronic inflammatory and neuropathic pain. Therefore, to determine the physiological role of PAP in a typical exocrine organ, we studied the submandibular salivary gland (SMG) of PAP Ϫ/Ϫ and wild-type C57BL/6J mice by microarray analyses, microRNA sequencing, activity tests, immunohistochemistry, and biochemical and physiological analyses of saliva. We show that PAP is the main acid phosphatase in the wild-type male mouse saliva, accounting for 50% of the total acid phosphatase activity, and that it is expressed only in the granular convoluted tubules of the SMGs, where it is the only 5=-ectonucleotidase. The lack of PAP in male PAP Ϫ/Ϫ mice was associated with a significant increase in the salivation volume under secretagogue stimulation, overexpression of genes related to cell proliferation (Mki67, Aurkb, Birc5) and immune response (Irf7, Cxcl9, Ccl3, Fpr2), and upregulation of miR-146a in SMGs. An increased and sustained acinar cell proliferation was detected without signs of glandular hyperplasia. Our results indicate that in PAP Ϫ/Ϫ mice, SMG homeostasis is maintained by an innate immune response. Additionally, we suggest that in male mice, PAP via its 5=-ectonucleotidase activity and production of adenosine can elicit analgesic effects when animals lick their wounds. acid phosphatase; transmembrane prostatic acid phosphatase; 5=-ectonucleotidase activity; TMPase activity; submandibular salivary gland PROSTATIC ACID PHOSPHATASE (PAP, E.C. 3.1.3.2) is a tartratesensitive histidine acid phosphatase enzyme with two known isoforms, the secreted (sPAP) and the type-I transmembrane (TMPAP) isoform, originating from alternative splicing of the same gene (Acpp) (45). Both isoforms are widely expressed in human and mouse tissues. In humans, PAP is predominately expressed in the prostate gland. TMPAP contains an extracellular NH 2 -terminal catalytic domain and a cytosolic COOHterminal domain, carrying a tyrosine-based endosomal/lysosomal targeting motif (Yxx) (45). In addition, TMPAP is an integral membrane protein of cells and is located in the plasma and vesicular membranes, from where it cycles through the endocytic/exocytic pathway via endosomes, multivesicular endosomes, lysosomes, and exosomes (46). Unlike the activity of other acid phosphatases, such as those derived from erythroc...

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Section: Discussionsupporting

confidence: 89%

Prostatic acid phosphatase is the main acid phosphatase with 5′-ectonucleotidase activity in the male mouse saliva and regulates salivation

Araujo

Quintero

Kipar

et al. 2014

American Journal of Physiology-Cell Physiology

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“…Furthermore, TI-VAMP is not involved in apical sorting of proteins that use a transcytotic pathway. Instead, the apical transcytotic pathway is regulated by VAMP8, another tetanus-neurotoxin-insensitive v-SNARE, which can pair with both apical and basolateral t-SNAREs (Imai et al, 2003;Pombo et al, 2003;Wang et al, 2007). Thus, we demonstrate that at least two different VAMPs are involved in the regulation of the two alternative routes to the apical plasma membrane.…”

Section: Introductionmentioning

confidence: 74%

“…Furthermore, it has also been proposed that VAMP8, Stx4 and SNAP23 act together (Wang et al, 2007). Finally VAMP8, Stx3 and Stx4 were coimmunoprecipitated in parotid acinar cells (Imai et al, 2003). In addition, it was recently shown that, although the major localization of VAMP8 is endosomal in fixed MDCK cells, in live conditions it appears to be present in fine, long tubular structures emanating from endosomes and to be present at the apical surface of the cell (Wakabayashi et al, 2007).…”

Section: Discussionmentioning

confidence: 96%

Distinct v-SNAREs regulate direct and indirect apical delivery in polarized epithelial cells

Pocard

Bivic

Galli

et al. 2007

Journal of Cell Science

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SNARE [soluble N-ethylmaleimide-sensitive factor (NSF) attachment protein (SNAP) receptor] proteins control the membrane-fusion events of eukaryotic membrane-trafficking pathways. Specific vesicular and target SNAREs operate in specific trafficking routes, but the degree of specificity of SNARE functions is still elusive. Apical fusion requires the polarized distribution at the apical surface of the t-SNARE syntaxin 3, and several v-SNAREs including TI-VAMP and VAMP8 operate at the apical plasma membrane in polarized epithelial cells. It is not known, however, whether specific v-SNAREs are involved in direct and indirect routes to the apical surface. Here, we used RNAi to assess the role of two tetanus-neurotoxin-insensitive v-SNAREs, TI-VAMP/VAMP7 and VAMP8, in the sorting of raft- and non-raft-associated apical markers that follow either a direct or a transcytotic delivery, respectively, in FRT or Caco2 cells. We show that TI-VAMP mediates the direct apical delivery of both raft- and non-raft-associated proteins. By contrast, sorting by means of the transcytotic pathway is not affected by TI-VAMP knockdown but does appear to be regulated by VAMP8. Together with the specific role of VAMP3 in basolateral transport, our results demonstrate a high degree of specificity in v-SNARE function in polarized cells.

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“…Moreover, syntaxin-3 was detected on the granule membrane fraction of rat parotid acinar cells by Western blotting but was not detectable by immunocytochemistry. Imai et al (2003) speculated that the reason for that phenomenon is similar to that described by Fujita-Yoshigaki et al (1999).…”

Section: Actin and Actin-binding Proteins In The Process Of Exocytosismentioning

confidence: 54%

The Human Submandibular Gland

Stoeckelhuber

Scherer

Janssen

et al. 2011

J Histochem Cytochem.

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SummarySubmandibular acinar glands secrete numerous proteins such as digestive enzymes and defense proteins on the basis of the exocrine secretion mode. Exocytosis is a complex process, including a soluble NSF attachment protein receptor (SNARE)-mediated membrane fusion of vesicles and target membrane and the additional activation of cytoskeletal proteins. Relevant data are available predominantly for animal salivary glands, especially of the rat parotid acinar cells. The authors investigated the secretory molecular machinery of acinar (serous) cells in the human submandibular gland by immunohistochemistry and immunofluorescence and found diverse proteins associated with exocytosis for the first time. SNAP-23, syntaxin-2, syntaxin-4, and VAMP-2 were localized at the luminal plasma membrane; syntaxin-2 and septin-2 were expressed in vesicles in the cytoplasm. Double staining of syntaxin-2 and septin-2 revealed a colocalization on the same vesicles. Lactoferrin and α-amylase served as a marker for secretory vesicles and were labeled positively together with syntaxin-2 and septin-2 in double-staining procedures. Cytoskeletal components such as actin, myosin II, cofilin, and profilin are concentrated at the apical plasma membrane of acinar submandibular glands. These observations complement the understanding of the complex exocytosis mechanisms. (J Histochem Cytochem 60:110-120, 2012)

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Intracellular localisation of SNARE proteins in rat parotid acinar cells: SNARE complexes on the apical plasma membrane

Cited by 40 publications

References 35 publications

Prostatic acid phosphatase is the main acid phosphatase with 5′-ectonucleotidase activity in the male mouse saliva and regulates salivation

Prostatic acid phosphatase is the main acid phosphatase with 5′-ectonucleotidase activity in the male mouse saliva and regulates salivation

Distinct v-SNAREs regulate direct and indirect apical delivery in polarized epithelial cells

The Human Submandibular Gland

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