Calmodulin Promotes N-BAR Domain-Mediated Membrane Constriction and Endocytosis

Overview

Journal Dev Cell

Publisher Cell Press

Specialties Cell Biology
Reproductive Medicine

Date 2016 Apr 20

PMID 27093085

Citations 12

Authors

Margaret D Myers

Sergey Ryazantsev

Linda Hicke

Gregory S Payne

Affiliations

Soon will be listed here.

Abstract

Membrane remodeling by BAR (Bin, Amphiphysin, RVS) domain-containing proteins, such as endophilins and amphiphysins, is integral to the process of endocytosis. However, little is known about the regulation of endocytic BAR domain activity. We have identified an interaction between the yeast Rvs167 N-BAR domain and calmodulin. Calmodulin-binding mutants of Rvs167 exhibited defects in endocytic vesicle release. In vitro, calmodulin enhanced membrane tubulation and constriction by wild-type Rvs167 but not calmodulin-binding-defective mutants. A subset of mammalian N-BAR domains bound calmodulin, and co-expression of calmodulin with endophilin A2 potentiated tubulation in vivo. These studies reveal a conserved role for calmodulin in regulating the intrinsic membrane-sculpting activity of endocytic N-BAR domains.

Citing Articles

Amphiphysin AoRvs167-Mediated Membrane Curvature Facilitates Trap Formation, Endocytosis, and Stress Resistance in .

Cui P, Tian M, Huang J, Zheng X, Guo Y, Li G Pathogens. 2022; 11(9).

PMID: 36145429 PMC: 9501185. DOI: 10.3390/pathogens11090997.

Ca Regulates Dimerization of the BAR Domain Protein PICK1 and Consequent Membrane Curvature.

Stan G, Shoemark D, Alibhai D, Hanley J Front Mol Neurosci. 2022; 15:893739.

PMID: 35721319 PMC: 9201945. DOI: 10.3389/fnmol.2022.893739.

Endophilin A1 drives acute structural plasticity of dendritic spines in response to Ca2+/calmodulin.

Yang Y, Chen J, Chen X, Li D, He J, Wang S J Cell Biol. 2021; 220(6).

PMID: 33988695 PMC: 8129810. DOI: 10.1083/jcb.202007172.

Yeast as a Model to Understand Actin-Mediated Cellular Functions in Mammals-Illustrated with Four Actin Cytoskeleton Proteins.

Akram Z, Ahmed I, Mack H, Kaur R, Silva R, Castilho B Cells. 2020; 9(3).

PMID: 32164332 PMC: 7140605. DOI: 10.3390/cells9030672.

Yeast-model-based study identified myosin- and calcium-dependent calmodulin signalling as a potential target for drug intervention in chorea-acanthocytosis.

Soczewka P, Kolakowski D, Smaczynska-de Rooij I, Rzepnikowska W, Ayscough K, Kaminska J Dis Model Mech. 2019; 12(1).

PMID: 30635263 PMC: 6361151. DOI: 10.1242/dmm.036830.

References

Wu X, McNeil B, Xu J, Fan J, Xue L, Melicoff E . Ca(2+) and calmodulin initiate all forms of endocytosis during depolarization at a nerve terminal. Nat Neurosci. 2009; 12(8):1003-1010. PMC: 4887276. DOI: 10.1038/nn.2355. View

Kishimoto T, Sun Y, Buser C, Liu J, Michelot A, Drubin D . Determinants of endocytic membrane geometry, stability, and scission. Proc Natl Acad Sci U S A. 2011; 108(44):E979-88. PMC: 3207701. DOI: 10.1073/pnas.1113413108. View

Rao Y, Ma Q, Vahedi-Faridi A, Sundborger A, Pechstein A, Puchkov D . Molecular basis for SH3 domain regulation of F-BAR-mediated membrane deformation. Proc Natl Acad Sci U S A. 2010; 107(18):8213-8. PMC: 2889545. DOI: 10.1073/pnas.1003478107. View

Yamashita T, Eguchi K, Saitoh N, von Gersdorff H, Takahashi T . Developmental shift to a mechanism of synaptic vesicle endocytosis requiring nanodomain Ca2+. Nat Neurosci. 2010; 13(7):838-44. PMC: 3677945. DOI: 10.1038/nn.2576. View

Mizuno N, Jao C, Langen R, Steven A . Multiple modes of endophilin-mediated conversion of lipid vesicles into coated tubes: implications for synaptic endocytosis. J Biol Chem. 2010; 285(30):23351-8. PMC: 2906327. DOI: 10.1074/jbc.M110.143776. View

Rao Y, Haucke V . Membrane shaping by the Bin/amphiphysin/Rvs (BAR) domain protein superfamily. Cell Mol Life Sci. 2011; 68(24):3983-93. PMC: 11114942. DOI: 10.1007/s00018-011-0768-5. View

Yao L, Sakaba T . Activity-dependent modulation of endocytosis by calmodulin at a large central synapse. Proc Natl Acad Sci U S A. 2011; 109(1):291-6. PMC: 3252931. DOI: 10.1073/pnas.1100608109. View

Mim C, Cui H, Gawronski-Salerno J, Frost A, Lyman E, Voth G . Structural basis of membrane bending by the N-BAR protein endophilin. Cell. 2012; 149(1):137-45. PMC: 3319357. DOI: 10.1016/j.cell.2012.01.048. View

Mim C, Unger V . Membrane curvature and its generation by BAR proteins. Trends Biochem Sci. 2012; 37(12):526-33. PMC: 3508348. DOI: 10.1016/j.tibs.2012.09.001. View

10.

Liu Y, Zheng X, Mueller G, Sobhany M, DeRose E, Zhang Y . Crystal structure of calmodulin binding domain of orai1 in complex with Ca2+ calmodulin displays a unique binding mode. J Biol Chem. 2012; 287(51):43030-41. PMC: 3522297. DOI: 10.1074/jbc.M112.380964. View

11.

Vazquez F, Unger V, Voth G . Autoinhibition of endophilin in solution via interdomain interactions. Biophys J. 2013; 104(2):396-403. PMC: 3552259. DOI: 10.1016/j.bpj.2012.12.009. View

12.

Daumke O, Roux A, Haucke V . BAR domain scaffolds in dynamin-mediated membrane fission. Cell. 2014; 156(5):882-92. DOI: 10.1016/j.cell.2014.02.017. View

13.

Wu T, Shi Z, Baumgart T . Mutations in BIN1 associated with centronuclear myopathy disrupt membrane remodeling by affecting protein density and oligomerization. PLoS One. 2014; 9(4):e93060. PMC: 3995651. DOI: 10.1371/journal.pone.0093060. View

14.

Wu X, Zhang Z, Zhao W, Wang D, Luo F, Wu L . Calcineurin is universally involved in vesicle endocytosis at neuronal and nonneuronal secretory cells. Cell Rep. 2014; 7(4):982-8. PMC: 4070379. DOI: 10.1016/j.celrep.2014.04.020. View

15.

Miller S, Mathiasen S, Bright N, Pierre F, Kelly B, Kladt N . CALM regulates clathrin-coated vesicle size and maturation by directly sensing and driving membrane curvature. Dev Cell. 2015; 33(2):163-75. PMC: 4406947. DOI: 10.1016/j.devcel.2015.03.002. View

16.

Okano H, Cyert M, Ohya Y . Importance of phenylalanine residues of yeast calmodulin for target binding and activation. J Biol Chem. 1998; 273(41):26375-82. DOI: 10.1074/jbc.273.41.26375. View

17.

Colwill K, Field D, Moore L, Friesen J, Andrews B . In vivo analysis of the domains of yeast Rvs167p suggests Rvs167p function is mediated through multiple protein interactions. Genetics. 1999; 152(3):881-93. PMC: 1460664. DOI: 10.1093/genetics/152.3.881. View

18.

Kaksonen M, Toret C, Drubin D . A modular design for the clathrin- and actin-mediated endocytosis machinery. Cell. 2005; 123(2):305-20. DOI: 10.1016/j.cell.2005.09.024. View

19.

Friesen H, Humphries C, Ho Y, Schub O, Colwill K, Andrews B . Characterization of the yeast amphiphysins Rvs161p and Rvs167p reveals roles for the Rvs heterodimer in vivo. Mol Biol Cell. 2006; 17(3):1306-21. PMC: 1382319. DOI: 10.1091/mbc.e05-06-0476. View

20.

Ren G, Vajjhala P, Lee J, Winsor B, Munn A . The BAR domain proteins: molding membranes in fission, fusion, and phagy. Microbiol Mol Biol Rev. 2006; 70(1):37-120. PMC: 1393252. DOI: 10.1128/MMBR.70.1.37-120.2006. View