publication . Article . Other literature type . 2018

Nanoscale Dynamism of Actin Enables Secretory Function in Cytolytic Cells

Mezida Saeed; Daniel Davis; Alexandre Carisey; Emily Mace;
Open Access English
  • Published: 01 Feb 2018 Journal: Current Biology, volume 28, issue 4, pages 489-502,000,000,000 (issn: 0960-9822, eissn: 1879-0445, Copyright policy)
  • Publisher: Cell Press
  • Country: United Kingdom
Abstract
Summary Natural killer (NK) cells are innate immune effectors that lyse virally infected and tumorigenic cells through the formation of an immunological synapse. Actin remodeling at the lytic immunological synapse is a critical requirement for multiple facets of cytotoxic function. Activating receptor and integrin signaling leads to the regulated turnover and remodeling of actin, which is required for adhesion, sustained receptor signaling, and ultimately exocytosis. NK cells undergo lytic granule exocytosis in hypodense regions of a pervasive actin network. Although these requirements have been well demonstrated, neither the dynamic regulation of synaptic actin...
Subjects
Medical Subject Headings: macromolecular substances
free text keywords: Super Resolution Microscopy, Article, actin cytoskeleton, natural killer cell, immune synapse, cytotoxicity, super-resolution microscopy, degranulation, General Biochemistry, Genetics and Molecular Biology, General Agricultural and Biological Sciences
63 references, page 1 of 5

Mace, E.M., Dongre, P., Hsu, H.T., Sinha, P., James, A.M., Mann, S.S., Forbes, L.R., Watkin, L.B., Orange, J.S.. Cell biological steps and checkpoints in accessing NK cell cytotoxicity. Immunol. Cell Biol.. 2014; 92: 245-255 [OpenAIRE] [PubMed]

Hsu, H.T., Mace, E.M., Carisey, A.F., Viswanath, D.I., Christakou, A.E., Wiklund, M., Önfelt, B., Orange, J.S.. NK cells converge lytic granules to promote cytotoxicity and prevent bystander killing. J. Cell Biol.. 2016; 215: 875-889 [OpenAIRE] [PubMed]

Zhang, M., March, M.E., Lane, W.S., Long, E.O.. A signaling network stimulated by β2 integrin promotes the polarization of lytic granules in cytotoxic cells. Sci. Signal.. 2014; 7

James, A.M., Hsu, H.T., Dongre, P., Uzel, G., Mace, E.M., Banerjee, P.P., Orange, J.S.. Rapid activation receptor- or IL-2-induced lytic granule convergence in human natural killer cells requires Src, but not downstream signaling. Blood. 2013; 121: 2627-2637 [OpenAIRE] [PubMed]

Mentlik, A.N., Sanborn, K.B., Holzbaur, E.L., Orange, J.S.. Rapid lytic granule convergence to the MTOC in natural killer cells is dependent on dynein but not cytolytic commitment. Mol. Biol. Cell. 2010; 21: 2241-2256 [OpenAIRE] [PubMed]

Valitutti, S., Dessing, M., Aktories, K., Gallati, H., Lanzavecchia, A.. Sustained signaling leading to T cell activation results from prolonged T cell receptor occupancy. Role of T cell actin cytoskeleton. J. Exp. Med.. 1995; 181: 577-584 [OpenAIRE] [PubMed]

Varma, R., Campi, G., Yokosuka, T., Saito, T., Dustin, M.L.. T cell receptor-proximal signals are sustained in peripheral microclusters and terminated in the central supramolecular activation cluster. Immunity. 2006; 25: 117-127 [OpenAIRE] [PubMed]

Orange, J.S., Ramesh, N., Remold-O’Donnell, E., Sasahara, Y., Koopman, L., Byrne, M., Bonilla, F.A., Rosen, F.S., Geha, R.S., Strominger, J.L.. Wiskott-Aldrich syndrome protein is required for NK cell cytotoxicity and colocalizes with actin to NK cell-activating immunologic synapses. Proc. Natl. Acad. Sci. USA. 2002; 99: 11351-11356 [OpenAIRE] [PubMed]

Mace, E.M., Wu, W.W., Ho, T., Mann, S.S., Hsu, H.T., Orange, J.S.. NK cell lytic granules are highly motile at the immunological synapse and require F-actin for post-degranulation persistence. J. Immunol.. 2012; 189: 4870-4880 [OpenAIRE] [PubMed]

Orange, J.S., Harris, K.E., Andzelm, M.M., Valter, M.M., Geha, R.S., Strominger, J.L.. The mature activating natural killer cell immunologic synapse is formed in distinct stages. Proc. Natl. Acad. Sci. USA. 2003; 100: 14151-14156 [OpenAIRE] [PubMed]

Bouma, G., Mendoza-Naranjo, A., Blundell, M.P., de Falco, E., Parsley, K.L., Burns, S.O., Thrasher, A.J.. Cytoskeletal remodeling mediated by WASp in dendritic cells is necessary for normal immune synapse formation and T-cell priming. Blood. 2011; 118: 2492-2501 [OpenAIRE] [PubMed]

Orange, J.S., Roy-Ghanta, S., Mace, E.M., Maru, S., Rak, G.D., Sanborn, K.B., Fasth, A., Saltzman, R., Paisley, A., Monaco-Shawver, L.. IL-2 induces a WAVE2-dependent pathway for actin reorganization that enables WASp-independent human NK cell function. J. Clin. Invest.. 2011; 121: 1535-1548 [OpenAIRE] [PubMed]

Snapper, S.B., Rosen, F.S., Mizoguchi, E., Cohen, P., Khan, W., Liu, C.H., Hagemann, T.L., Kwan, S.P., Ferrini, R., Davidson, L.. Wiskott-Aldrich syndrome protein-deficient mice reveal a role for WASP in T but not B cell activation. Immunity. 1998; 9: 81-91 [OpenAIRE] [PubMed]

Brown, A.C., Dobbie, I.M., Alakoskela, J.M., Davis, I., Davis, D.M.. Super-resolution imaging of remodeled synaptic actin reveals different synergies between NK cell receptors and integrins. Blood. 2012; 120: 3729-3740 [OpenAIRE] [PubMed]

Brown, A.C., Oddos, S., Dobbie, I.M., Alakoskela, J.M., Parton, R.M., Eissmann, P., Neil, M.A., Dunsby, C., French, P.M., Davis, I., Davis, D.M.. Remodelling of cortical actin where lytic granules dock at natural killer cell immune synapses revealed by super-resolution microscopy. PLoS Biol.. 2011; 9: e1001152 [OpenAIRE] [PubMed]

63 references, page 1 of 5
Abstract
Summary Natural killer (NK) cells are innate immune effectors that lyse virally infected and tumorigenic cells through the formation of an immunological synapse. Actin remodeling at the lytic immunological synapse is a critical requirement for multiple facets of cytotoxic function. Activating receptor and integrin signaling leads to the regulated turnover and remodeling of actin, which is required for adhesion, sustained receptor signaling, and ultimately exocytosis. NK cells undergo lytic granule exocytosis in hypodense regions of a pervasive actin network. Although these requirements have been well demonstrated, neither the dynamic regulation of synaptic actin...
Subjects
Medical Subject Headings: macromolecular substances
free text keywords: Super Resolution Microscopy, Article, actin cytoskeleton, natural killer cell, immune synapse, cytotoxicity, super-resolution microscopy, degranulation, General Biochemistry, Genetics and Molecular Biology, General Agricultural and Biological Sciences
63 references, page 1 of 5

Mace, E.M., Dongre, P., Hsu, H.T., Sinha, P., James, A.M., Mann, S.S., Forbes, L.R., Watkin, L.B., Orange, J.S.. Cell biological steps and checkpoints in accessing NK cell cytotoxicity. Immunol. Cell Biol.. 2014; 92: 245-255 [OpenAIRE] [PubMed]

Hsu, H.T., Mace, E.M., Carisey, A.F., Viswanath, D.I., Christakou, A.E., Wiklund, M., Önfelt, B., Orange, J.S.. NK cells converge lytic granules to promote cytotoxicity and prevent bystander killing. J. Cell Biol.. 2016; 215: 875-889 [OpenAIRE] [PubMed]

Zhang, M., March, M.E., Lane, W.S., Long, E.O.. A signaling network stimulated by β2 integrin promotes the polarization of lytic granules in cytotoxic cells. Sci. Signal.. 2014; 7

James, A.M., Hsu, H.T., Dongre, P., Uzel, G., Mace, E.M., Banerjee, P.P., Orange, J.S.. Rapid activation receptor- or IL-2-induced lytic granule convergence in human natural killer cells requires Src, but not downstream signaling. Blood. 2013; 121: 2627-2637 [OpenAIRE] [PubMed]

Mentlik, A.N., Sanborn, K.B., Holzbaur, E.L., Orange, J.S.. Rapid lytic granule convergence to the MTOC in natural killer cells is dependent on dynein but not cytolytic commitment. Mol. Biol. Cell. 2010; 21: 2241-2256 [OpenAIRE] [PubMed]

Valitutti, S., Dessing, M., Aktories, K., Gallati, H., Lanzavecchia, A.. Sustained signaling leading to T cell activation results from prolonged T cell receptor occupancy. Role of T cell actin cytoskeleton. J. Exp. Med.. 1995; 181: 577-584 [OpenAIRE] [PubMed]

Varma, R., Campi, G., Yokosuka, T., Saito, T., Dustin, M.L.. T cell receptor-proximal signals are sustained in peripheral microclusters and terminated in the central supramolecular activation cluster. Immunity. 2006; 25: 117-127 [OpenAIRE] [PubMed]

Orange, J.S., Ramesh, N., Remold-O’Donnell, E., Sasahara, Y., Koopman, L., Byrne, M., Bonilla, F.A., Rosen, F.S., Geha, R.S., Strominger, J.L.. Wiskott-Aldrich syndrome protein is required for NK cell cytotoxicity and colocalizes with actin to NK cell-activating immunologic synapses. Proc. Natl. Acad. Sci. USA. 2002; 99: 11351-11356 [OpenAIRE] [PubMed]

Mace, E.M., Wu, W.W., Ho, T., Mann, S.S., Hsu, H.T., Orange, J.S.. NK cell lytic granules are highly motile at the immunological synapse and require F-actin for post-degranulation persistence. J. Immunol.. 2012; 189: 4870-4880 [OpenAIRE] [PubMed]

Orange, J.S., Harris, K.E., Andzelm, M.M., Valter, M.M., Geha, R.S., Strominger, J.L.. The mature activating natural killer cell immunologic synapse is formed in distinct stages. Proc. Natl. Acad. Sci. USA. 2003; 100: 14151-14156 [OpenAIRE] [PubMed]

Bouma, G., Mendoza-Naranjo, A., Blundell, M.P., de Falco, E., Parsley, K.L., Burns, S.O., Thrasher, A.J.. Cytoskeletal remodeling mediated by WASp in dendritic cells is necessary for normal immune synapse formation and T-cell priming. Blood. 2011; 118: 2492-2501 [OpenAIRE] [PubMed]

Orange, J.S., Roy-Ghanta, S., Mace, E.M., Maru, S., Rak, G.D., Sanborn, K.B., Fasth, A., Saltzman, R., Paisley, A., Monaco-Shawver, L.. IL-2 induces a WAVE2-dependent pathway for actin reorganization that enables WASp-independent human NK cell function. J. Clin. Invest.. 2011; 121: 1535-1548 [OpenAIRE] [PubMed]

Snapper, S.B., Rosen, F.S., Mizoguchi, E., Cohen, P., Khan, W., Liu, C.H., Hagemann, T.L., Kwan, S.P., Ferrini, R., Davidson, L.. Wiskott-Aldrich syndrome protein-deficient mice reveal a role for WASP in T but not B cell activation. Immunity. 1998; 9: 81-91 [OpenAIRE] [PubMed]

Brown, A.C., Dobbie, I.M., Alakoskela, J.M., Davis, I., Davis, D.M.. Super-resolution imaging of remodeled synaptic actin reveals different synergies between NK cell receptors and integrins. Blood. 2012; 120: 3729-3740 [OpenAIRE] [PubMed]

Brown, A.C., Oddos, S., Dobbie, I.M., Alakoskela, J.M., Parton, R.M., Eissmann, P., Neil, M.A., Dunsby, C., French, P.M., Davis, I., Davis, D.M.. Remodelling of cortical actin where lytic granules dock at natural killer cell immune synapses revealed by super-resolution microscopy. PLoS Biol.. 2011; 9: e1001152 [OpenAIRE] [PubMed]

63 references, page 1 of 5
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