Actin Depolymerisation and Crosslinking Join Forces with Myosin II to Contract Actin Coats on Fused Secretory Vesicles

Overview

Journal J Cell Sci

Specialty Cell Biology

Date 2015 Feb 1

PMID 25637593

Citations 27

Authors

Pika Miklavc

Konstantin Ehinger

Ayesha Sultan

Tatiana Felder

Patrick Paul

Kay-Eberhard Gottschalk

Manfred Frick

Affiliations

Soon will be listed here.

Abstract

In many secretory cells actin and myosin are specifically recruited to the surface of secretory granules following their fusion with the plasma membrane. Actomyosin-dependent compression of fused granules is essential to promote active extrusion of cargo. However, little is known about molecular mechanisms regulating actin coat formation and contraction. Here, we provide a detailed kinetic analysis of the molecules regulating actin coat contraction on fused lamellar bodies in primary alveolar type II cells. We demonstrate that ROCK1 and myosin light chain kinase 1 (MLCK1, also known as MYLK) translocate to fused lamellar bodies and activate myosin II on actin coats. However, myosin II activity is not sufficient for efficient actin coat contraction. In addition, cofilin-1 and α-actinin translocate to actin coats. ROCK1-dependent regulated actin depolymerisation by cofilin-1 in cooperation with actin crosslinking by α-actinin is essential for complete coat contraction. In summary, our data suggest a complementary role for regulated actin depolymerisation and crosslinking, and myosin II activity, to contract actin coats and drive secretion.

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References

Riento K, Ridley A . Rocks: multifunctional kinases in cell behaviour. Nat Rev Mol Cell Biol. 2003; 4(6):446-56. DOI: 10.1038/nrm1128. View

Sokac A, Co C, Taunton J, Bement W . Cdc42-dependent actin polymerization during compensatory endocytosis in Xenopus eggs. Nat Cell Biol. 2003; 5(8):727-32. DOI: 10.1038/ncb1025. View

Gasman S, Chasserot-Golaz S, Malacombe M, Way M, Bader M . Regulated exocytosis in neuroendocrine cells: a role for subplasmalemmal Cdc42/N-WASP-induced actin filaments. Mol Biol Cell. 2003; 15(2):520-31. PMC: 329227. DOI: 10.1091/mbc.e03-06-0402. View

Dulyaninova N, Patskovsky Y, Bresnick A . The N-terminus of the long MLCK induces a disruption in normal spindle morphology and metaphase arrest. J Cell Sci. 2004; 117(Pt 8):1481-93. DOI: 10.1242/jcs.00993. View

Sudhof T . The synaptic vesicle cycle. Annu Rev Neurosci. 2004; 27:509-47. DOI: 10.1146/annurev.neuro.26.041002.131412. View

Nemoto T, Kojima T, Oshima A, Bito H, Kasai H . Stabilization of exocytosis by dynamic F-actin coating of zymogen granules in pancreatic acini. J Biol Chem. 2004; 279(36):37544-50. DOI: 10.1074/jbc.M403976200. View

Orci L, GABBAY K, Malaisse W . Pancreatic beta-cell web: its possible role in insulin secretion. Science. 1972; 175(4026):1128-30. DOI: 10.1126/science.175.4026.1128. View

Jockusch B, Burger M, DAPRADA M, Richards J, Chaponnier C, Gabbiani G . alpha-Actinin attached to membranes of secretory vesicles. Nature. 1977; 270(5638):628-9. DOI: 10.1038/270628a0. View

Tsilibary E, Williams M . Actin and secretion of surfactant. J Histochem Cytochem. 1983; 31(11):1298-304. DOI: 10.1177/31.11.6688627. View

10.

Dobbs L, Gonzalez R, Williams M . An improved method for isolating type II cells in high yield and purity. Am Rev Respir Dis. 1986; 134(1):141-5. DOI: 10.1164/arrd.1986.134.1.141. View

11.

Segawa A, Yamashina S . Roles of microfilaments in exocytosis: a new hypothesis. Cell Struct Funct. 1989; 14(5):531-44. DOI: 10.1247/csf.14.531. View

12.

Gotow T, Miyaguchi K, HASHIMOTO P . Cytoplasmic architecture of the axon terminal: filamentous strands specifically associated with synaptic vesicles. Neuroscience. 1991; 40(2):587-98. DOI: 10.1016/0306-4522(91)90143-c. View

13.

Lindau M, Gomperts B . Techniques and concepts in exocytosis: focus on mast cells. Biochim Biophys Acta. 1991; 1071(4):429-71. DOI: 10.1016/0304-4157(91)90006-i. View

14.

Galkin V, Orlova A, Kudryashov D, Solodukhin A, Reisler E, Schroder G . Remodeling of actin filaments by ADF/cofilin proteins. Proc Natl Acad Sci U S A. 2011; 108(51):20568-72. PMC: 3251117. DOI: 10.1073/pnas.1110109108. View

15.

Mseka T, Cramer L . Actin depolymerization-based force retracts the cell rear in polarizing and migrating cells. Curr Biol. 2011; 21(24):2085-91. DOI: 10.1016/j.cub.2011.11.006. View

16.

Stoeckelhuber M, Scherer E, Janssen K, Slotta-Huspenina J, Loeffelbein D, Rohleder N . The human submandibular gland: immunohistochemical analysis of SNAREs and cytoskeletal proteins. J Histochem Cytochem. 2011; 60(2):110-20. PMC: 3351120. DOI: 10.1369/0022155411432785. View

17.

Reymann A, Boujemaa-Paterski R, Martiel J, Guerin C, Cao W, Chin H . Actin network architecture can determine myosin motor activity. Science. 2012; 336(6086):1310-4. PMC: 3649007. DOI: 10.1126/science.1221708. View

18.

Mendes Pinto I, Rubinstein B, Li R . Force to divide: structural and mechanical requirements for actomyosin ring contraction. Biophys J. 2013; 105(3):547-54. PMC: 3736747. DOI: 10.1016/j.bpj.2013.06.033. View

19.

Uenishi E, Shibasaki T, Takahashi H, Seki C, Hamaguchi H, Yasuda T . Actin dynamics regulated by the balance of neuronal Wiskott-Aldrich syndrome protein (N-WASP) and cofilin activities determines the biphasic response of glucose-induced insulin secretion. J Biol Chem. 2013; 288(36):25851-25864. PMC: 3764791. DOI: 10.1074/jbc.M113.464420. View

20.

Miklavc P, Ehinger K, Thompson K, Hobi N, Shimshek D, Frick M . Surfactant secretion in LRRK2 knock-out rats: changes in lamellar body morphology and rate of exocytosis. PLoS One. 2014; 9(1):e84926. PMC: 3897396. DOI: 10.1371/journal.pone.0084926. View