Annexin II mediates the neutrophil elastase-stimulated exocytosis of mucin 5ac

Xu,Rui; Li,Qi; Zhou,Xiangdong; Perelman,Juliy  M.; Kolosov,Victor  P.

doi:10.3892/mmr.2013.1795

Annexin II mediates the neutrophil elastase-stimulated exocytosis of mucin 5ac

Authors:
- Rui Xu
- Qi Li
- Xiangdong Zhou
- Juliy M. Perelman
- Victor P. Kolosov
View Affiliations

Affiliations: Department of Respiratory Medicine, The Second Affiliated Hospital, Chongqing Medical University, Chongqing 400010, P.R. China, Far Eastern Scientific Center of Physiology and Pathology of Respiration, Russian Academy of Medical Sciences, Blagoveschensk, Amur Oblast 675000, Russia
Published online on: November 14, 2013 https://doi.org/10.3892/mmr.2013.1795
Pages: 299-304

Metrics: Total Views: 0 (Spandidos Publications: | PMC Statistics: )

Metrics: Total PDF Downloads: 0 (Spandidos Publications: | PMC Statistics: )

Cited By (CrossRef): 0 citations Loading Articles...

Abstract

The overexpression and hypersecretion of mucus is a hallmark of several chronic pulmonary inflammatory diseases, including chronic obstructive pulmonary disease (COPD), asthma and cystic fibrosis. Mucin 5ac (MUC5AC) is a major component of airway mucus. Annexin II (ANXII) has been reported to be expressed in various cells and is associated with the fusion of secretory vesicles. Neutrophil elastase (NE) is present at high concentrations in the airway surface fluid in patients with cystic fibrosis and various other severe diseases. However, the role of ANXII in NE-induced secretion of MUC5AC granules remains unclear. It was determined that NE upregulates the transcription and protein synthesis of ANXII in 16HBE human bronchial epithelial cells. Following stimulation with NE, ANXII is recruited to the cell membrane, as visualised by cell immunochemistry and laser confocal microscopy, and the redistribution of ANXII is inhibited by the protein kinase-C (PKC) inhibitor bisindolylmaleimide I. Conversely, depleting endogenous ANXII decreases MUC5AC secretion into the cell culture supernatant and increases the levels of intracellular MUC5AC protein. The data indicated that ANXII is associated with the secretion of MUC5AC granules.

View Figures

View References

1	Ordonez CL, Khashayar R, Wong HH, et al: Mild and moderate asthma is associated with airway goblet cell hyperplasia and abnormalities in mucin gene expression. Am J Respir Crit Care Med. 163:517–523. 2001. View Article : Google Scholar : PubMed/NCBI
2	Turner J and Jones CE: Regulation of mucin expression in respiratory diseases. Biochem Soc Trans. 37:877–881. 2009. View Article : Google Scholar
3	Voynow JA, Fischer BM, Malarkey DE, et al: Neutrophil elastase induces mucus cell metaplasia in mouse lung. Am J Physiol Lung Cell Mol Physiol. 287:L1293–1302. 2004. View Article : Google Scholar : PubMed/NCBI
4	Kohri K, Ueki IF and Nadel JA: Neutrophil elastase induces mucin production by ligand-dependent epidermal growth factor receptor activation. Am J Physiol Lung Cell Mol Physiol. 283:L531–L540. 2002.PubMed/NCBI
5	Jiang DP, Li Q, Yang J, Perelman JM, Kolosov VP and Zhou XD: Scutellarin attenuates human-neutrophil-elastase-induced mucus production by inhibiting the PKC-ERK signaling pathway in vitro and in vivo. Am J Chin Med. 39:1193–1206. 2011. View Article : Google Scholar : PubMed/NCBI
6	Roghanian A, Drost EM, MacNee W, Howie SE and Sallenave JM: Inflammatory lung secretions inhibit dendritic cell maturation and function via neutrophil elastase. Am J Respir Crit Care Med. 174:1189–1198. 2006. View Article : Google Scholar : PubMed/NCBI
7	Benz J and Hofmann A: Annexins: from structure to function. Biol Chem. 378:177–183. 1997.PubMed/NCBI
8	Paumet F, Rahimian V and Rothman JE: The specificity of SNARE-dependent fusion is encoded in the SNARE motif. Proc Natl Acad Sci USA. 101:3376–3380. 2004. View Article : Google Scholar : PubMed/NCBI
9	Chattopadhyay S, Sun P, Wang P, Abonyo B, Cross NL and Liu L: Fusion of lamellar body with plasma membrane is driven by the dual action of annexin II tetramer and arachidonic acid. J Biol Chem. 278:39675–39683. 2003. View Article : Google Scholar : PubMed/NCBI
10	Umbrecht-Jenck E, Demais V, Calco V, Bailly Y, Bader MF and Chasserot-Golaz S: S100A10-mediated translocation of annexin-A2 to SNARE proteins in adrenergic chromaffin cells undergoing exocytosis. Traffic. 11:958–971. 2010. View Article : Google Scholar
11	Chasserot-Golaz S, Vitale N, Sagot I, Delouche B, Dirrig S, Pradel LA, Henry JP, Aunis D and Bader MF: Annexin II in exocytosis: catecholamine secretion requires the translocation of p36 to the subplasmalemmal region in chromaffin cells. J Cell Biol. 133:1217–1236. 1996. View Article : Google Scholar
12	Chasserot-Golaz S, Vitale N, Umbrecht-Jenck E, Knight D, Gerke V and Bader MF: Annexin 2 promotes the formation of lipid microdomains required for calcium-regulated exocytosis of dense-core vesicles. Mol Biol Cell. 16:1108–1119. 2005. View Article : Google Scholar : PubMed/NCBI
13	Sarkar P and Hayes BE: Proteomic profiling of rat lung epithelial cells induced by acrolein. Life Sci. 85:188–195. 2009. View Article : Google Scholar : PubMed/NCBI
14	Oudinet JP, Russo-Marie F, Cavadore JC and Rothhut B: Protein kinase C-dependent phosphorylation of annexins I and II in mesangial cells. Biochem J. 292:63–68. 1993.PubMed/NCBI
15	Vestbo J: Epidemiological studies in mucus hypersecretion. Novartis Found Symp. 248:3–19. 277–282. 2002. View Article : Google Scholar : PubMed/NCBI
16	Rogers DF: Physiology of airway mucus secretion and pathophysiology of hypersecretion. Respir Care. 52:1134–1149. 2007.PubMed/NCBI
17	Foster WM, Adler KB, Crews AL, Potts EN, Fischer BM and Voynow JA: MARCKS-related peptide modulates in vivo the secretion of airway Muc5ac. Am J Physiol Lung Cell Mol Physiol. 299:L345–352. 2010. View Article : Google Scholar : PubMed/NCBI
18	Park JA, Crews AL, Lampe WR, Fang S, Park J and Adler KB: Protein kinase C delta regulates airway mucin secretion via phosphorylation of MARCKS protein. Am J Pathol. 171:1822–1830. 2007. View Article : Google Scholar : PubMed/NCBI
19	Senda T, Okabe T, Matsuda M and Fujita H: Quick-freeze, deep-etch visualization of exocytosis in anterior pituitary secretory cells: localization and possible roles of actin and annexin II. Cell Tissue Res. 277:51–60. 1994. View Article : Google Scholar : PubMed/NCBI
20	Deora AB, Kreitzer G, Jacovina AT and Hajjar KA: An annexin 2 phosphorylation switch mediates p11-dependent translocation of annexin 2 to the cell surface. J Biol Chem. 279:43411–43418. 2004. View Article : Google Scholar : PubMed/NCBI
21	Behrendorff N, Dolai S, Hong W, Gaisano HY and Thorn P: Vesicle-associated membrane protein 8 (VAMP8) is a SNARE (soluble N-ethylmaleimide-sensitive factor attachment protein receptor) selectively required for sequential granule-to-granule fusion. J Biol Chem. 286:29627–29634. 2011. View Article : Google Scholar
22	Jones LC, Moussa L, Fulcher ML, et al: VAMP8 is a vesicle SNARE that regulates mucin secretion in airway goblet cells. J Physiol. 590:545–562. 2012. View Article : Google Scholar : PubMed/NCBI
23	Wang P, Chintagari NR, Gou D, Su L and Liu L: Physical and functional interactions of SNAP-23 with annexin A2. Am J Respir Cell Mol Biol. 37:467–476. 2007. View Article : Google Scholar : PubMed/NCBI
24	Madureira PA, Hill R, Miller VA, Giacomantonio C, Lee PW and Waisman DM: Annexin A2 is a novel cellular redox regulatory protein involved in tumorigenesis. Oncotarget. 2:1075–1093. 2011.
25	Genetos DC, Wong A, Watari S and Yellowley CE: Hypoxia increases Annexin A2 expression in osteoblastic cells via VEGF and ERK. Bone. 47:1013–1019. 2010. View Article : Google Scholar : PubMed/NCBI
26	Chasserot-Golaz S, Vitale N, Sagot I, et al: Annexin II in exocytosis: catecholamine secretion requires the translocation of p36 to the subplasmalemmal region in chromaffin cells. J Cell Biol. 133:1217–1236. 1996. View Article : Google Scholar : PubMed/NCBI
27	Voynow JA, Young LR, Wang Y, Horger T, Rose MC and Fischer BM: Neutrophil elastase increases MUC5AC mRNA and protein expression in respiratory epithelial cells. Am J Physiol. 276:L835–843. 1999.PubMed/NCBI
28	Zhou J, Perelman JM, Kolosov VP and Zhou X: Neutrophil elastase induces MUC5AC secretion via protease-activated receptor 2. Mol Cell Biochem. 377:75–85. 2013. View Article : Google Scholar : PubMed/NCBI