Follow that cell: Leukocyte migration in L-plastin mutant zebrafish.


Journal

Cytoskeleton (Hoboken, N.J.)
ISSN: 1949-3592
Titre abrégé: Cytoskeleton (Hoboken)
Pays: United States
ID NLM: 101523844

Informations de publication

Date de publication:
04 2022
Historique:
revised: 21 06 2022
received: 22 02 2022
accepted: 07 07 2022
pubmed: 12 7 2022
medline: 7 10 2022
entrez: 11 7 2022
Statut: ppublish

Résumé

Actin assemblies are important in motile cells such as leukocytes, which form dynamic plasma membrane extensions or podia. L-plastin (LCP1) is a leukocyte-specific calcium-dependent actin-bundling protein that, in mammals, is known to affect immune cell migration. Previously, we generated CRISPR/Cas9 engineered zebrafish lacking L-plastin (lcp1-/-) and reported that they had reduced survival to adulthood, suggesting that lack of this actin-bundler might negatively affect the immune system. To test this hypothesis, we examined the distribution and migration of neutrophils and macrophages in the transparent tail of early zebrafish larvae using cell-specific markers and an established wound-migration assay. Knockout larvae were similar to their heterozygous siblings in having equal body sizes and comparable numbers of neutrophils in caudal hematopoietic tissue at 2 days postfertilization, indicating no gross defect in neutrophil production or developmental migration. When stimulated by a tail wound, all genotypes of neutrophils were equally migratory in a two-hour window. However, for macrophages we observed both migration defects and morphological differences. L-plastin knockout macrophages (lcp1 -/-) still homed to wounds but were slower, less directional and had a star-like morphology with many leading and trailing projections. In contrast, heterozygous macrophages lcp1 (+/-) were faster, more directional, and had a streamlined, slug-like morphology. Overall, these findings show that in larval zebrafish L-plastin knockout primarily affects the macrophage response with possible consequences for organismal immunity. Consistent with our observations, we propose a model in which cytoplasmic L-plastin negatively regulates macrophage integrin adhesion by holding these transmembrane heterodimers in a "clasped," inactive form and is a necessary part of establishing macrophage polarity during chemokine-induced motility.

Identifiants

pubmed: 35811499
doi: 10.1002/cm.21717
doi:

Substances chimiques

Actins 0
Chemokines 0
Integrins 0
Membrane Glycoproteins 0
Microfilament Proteins 0
plastin 0
Calcium SY7Q814VUP

Types de publication

Journal Article Research Support, N.I.H., Extramural

Langues

eng

Sous-ensembles de citation

IM

Pagination

26-37

Subventions

Organisme : NIGMS NIH HHS
ID : P41 GM103545
Pays : United States
Organisme : NIGMS NIH HHS
ID : R01 GM098151
Pays : United States
Organisme : NIGMS NIH HHS
ID : R15 GM120664
Pays : United States

Informations de copyright

© 2022 Wiley Periodicals LLC.

Références

Afonso, A., Lousada, S., Silva, J., Ellis, A. E., & Silva, M. T. (1998). Neutrophil and macrophage responses to inflammation in the peritoneal cavity of rainbow trout Oncorhynchus mykiss. A light and electron microscopic cytochemical study. Diseases of Aquatic Organisms, 34, 27-37.
Amos, L. A., & Amos, W. B. (1991). Molecules of the cytoskeleton. New York: Guilford Press.
Arpin, M., Friederich, E., Algrain, M., Vernel, F., & Louvard, D. (1994). Functional differences between L-plastin and T-plastin isoforms. Journal of Cell Biology, 127, 1995-2008.
Askari, J. A., Buckley, P. A., Mould, A. P., & Humphries, M. J. (2009). Linking integrin conformation to function. Journal of Cell Science, 122, 165-170.
Bachmann, M., Kukkurainen, S., Hytönen, V. P., & Wehrle-Haller, B. (2019). Cell adhesion by integrins. Physiological Reviews, 99, 1655-1699.
Beltman, J. B., Marée, A. F., & de Boer, R. J. (2009). Analysing immune cell migration. Nature Reviews. Immunology, 9, 789-798.
Bennett, C. M., Kanki, J. P., Rhodes, J., Liu, T. X., Paw, B. H., Kieran, M. W., … Look, A. T. (2001). Myelopoiesis in the zebrafish, Danio rerio. Blood, 98, 643-651.
Bertrand, J. Y., Kim, A. D., Violette, E. P., Stachura, D. L., Cisson, J. L., & Traver, D. (2007). Definitive hematopoiesis initiates through a committed erythromyeloid progenitor in the zebrafish embryo. Development, 134, 4147-4156.
Best, J., Adatto, I., Cockington, J., James, A., & Lawrence, C. (2010). A novel method for rearing first-feeding larval zebrafish: Polyculture with type L saltwater rotifers (Brachionus plicatilis). Zebrafish, 7, 289-295.
Bhatlekar, S., Manne, B. K., Basak, I., Edelstein, L. C., Tugolukova, E., Stoller, M. L., … Weyrich, A. S. (2020). Mir-125a-5p regulates megakaryocyte proplatelet formation via the actin-bundling protein L-plastin. Blood, 136, 1760-1772.
Buccione, R., Orth, J. D., & McNiven, M. A. (2004). Foot and mouth: Podosomes, invadopodia and circular dorsal ruffles. Nature Reviews Molecular Cell Biology, 5, 647-657.
Caswell, P. T., & Zech, T. (2018). Actin-based cell protrusion in a 3D matrix. Trends in Cell Biology, 28, 823-834.
Chellaiah, M. A., Majumdar, S., & Aljohani, H. (2018). Peptidomimetic inhibitors of L-plastin reduce the resorptive activity of osteoclast but not the bone forming activity of osteoblasts in vitro. PLoS One, 13, e0204209.
Chen, H., Mocsai, A., Zhang, H., Ding, R. X., Morisaki, J. H., White, M., … Brown, E. J. (2003). Role for plastin in host defense distinguishes integrin signaling from cell adhesion and spreading. Immunity, 19, 95-104.
Chigaev, A., & Sklar, L. A. (2012). Overview: assays for studying integrin-dependent cell adhesion. Methods in Molecular Biology, 757, 3-14.
Clatworthy, A. E., Lee, J. S., Leibman, M., Kostun, Z., Davidson, A. J., & Hung, D. T. (2009). Pseudomonas aeruginosa infection of zebrafish involves both host and pathogen determinants. Infection and Immunity, 77, 1293-1303.
Codling, E. A., Plank, M. J., & Benhamou, S. (2008). Random walk models in biology. Journal of the Royal Society Interface, 5, 813-834.
Crowhurst, M. O., Layton, J. E., & Lieschke, G. J. (2002). Developmental biology of zebrafish myeloid cells. The International Journal of Developmental Biology, 46, 483-492.
Davidson, A. J., & Zon, L. I. (2004). The 'definitive' (and 'primitive') guide to zebrafish hematopoiesis. Oncogene, 23, 7233-7246.
Deady, L. E., Todd, E. M., Davis, C. G., Zhou, J. Y., Topcagic, N., Edelson, B. T., … Morley, S. C. (2014). L-plastin is essential for alveolar macrophage production and control of pulmonary pneumococcal infection. Infection and Immunity, 82, 1982-1993.
Dubey, M., Singh, A. K., Awasthi, D., Nagarkoti, S., Kumar, S., Ali, W., … Dikshit, M. (2015). L-plastin S-glutathionylation promotes reduced binding to beta-actin and affects neutrophil functions. Free Radical Biology & Medicine, 86, 1-15.
Eckfeldt, C. E., Mendenhall, E. M., Flynn, C. M., Wang, T. F., Pickart, M. A., Grindle, S. M., … Verfaillie, C. M. (2005). Functional analysis of human hematopoietic stem cell gene expression using zebrafish. PLoS Biology, 3, e254.
Ellett, F., Pase, L., Hayman, J. W., Andrianopoulos, A., & Lieschke, G. J. (2011). mpeg1 promoter transgenes direct macrophage-lineage expression in zebrafish. Blood, 117, e49-e56.
Faull, R. J., & Ginsberg, M. H. (1996). Inside-out signaling through integrins. Journal of the American Society of Nephrology, 7, 1091-1097.
Feng, Y., Santoriello, C., Mione, M., Hurlstone, A., & Martin, P. (2010). Live imaging of innate immune cell sensing of transformed cells in zebrafish larvae: parallels between tumor initiation and wound inflammation. PLoS Biology, 8, e1000562.
Ferrero, G., Gomez, E., Lyer, S., Rovira, M., Miserocchi, M., Langenau, D. M., … Wittamer, V. (2020). The macrophage-expressed gene (mpeg) 1 identifies a subpopulation of B cells in the adult zebrafish. Journal of Leukocyte Biology, 107, 431-443.
Gardel, M. L., Schneider, I. C., Aratyn-Schaus, Y., & Waterman, C. M. (2010). Mechanical integration of actin and adhesion dynamics in cell migration. Annual Review of Cell and Developmental Biology, 26, 315-333.
Goldstein, D., Djeu, J., Latter, G., Burbeck, S., & Leavitt, J. (1985). Abundant synthesis of the transformation-induced protein of neoplastic human fibroblasts, plastin, in normal lymphocytes. Cancer Research, 45, 5643-5647.
Henry, K. M., Loynes, C. A., Whyte, M. K., & Renshaw, S. A. (2013). Zebrafish as a model for the study of neutrophil biology. Journal of Leukocyte Biology, 94, 633-642.
Hughes, P. E., Diaz-Gonzalez, F., Leong, L., Wu, C., McDonald, J. A., Shattil, S. J., & Ginsberg, M. H. (1996). Breaking the integrin hinge. A defined structural constraint regulates integrin signaling. The Journal of Biological Chemistry, 271, 6571-6574.
Ishida, H., Jensen, K. V., Woodman, A. G., Hyndman, M. E., & Vogel, H. J. (2017). The calcium-dependent switch helix of L-plastin regulates actin bundling. Scientific Reports, 7, 40662.
Jones, S. L., Wang, J., Turck, C. W., & Brown, E. J. (1998). A role for the actin-bundling protein L-plastin in the regulation of leukocyte integrin function. Proceedings of the National Academy of Sciences of the United States of America, 95, 9331-9336.
Kell, M. J., Riccio, R. E., Baumgartner, E. A., Compton, Z. J., Pecorin, P. J., Mitchell, T. A., … LeClair, E. E. (2018). Targeted deletion of the zebrafish actin-bundling protein L-plastin (lcp1). PLoS One, 13, e0190353.
Kolanus, W., & Zeitlmann, L. (1998). Regulation of integrin function by inside-out signaling mechanisms. In: B. Holzmann & H. Wagner (Eds.). Leukocyte Integrins in the Immune System and Malignant Disease. Current Topics in Microbiology and Immunology, Vol. 231. Springer: Berlin, Heidelberg.
Krummel, M. F., Bartumeus, F., & Gérard, A. (2016). T cell migration, search strategies and mechanisms. Nature Reviews Immunology, 16, 193-201.
Le Goff, E., Vallentin, A., Harmand, P. O., Aldrian-Herrada, G., Rebière, B., Roy, C., … Lebart, M. C. (2010). Characterization of L-plastin interaction with beta integrin and its regulation by micro-calpain. Cytoskeleton (Hoboken), 67, 286-296.
Le Guyader, D., Redd, M. J., Colucci-Guyon, E., Murayama, E., Kissa, K., Briolat, V., … Herbomel, P. (2008). Origins and unconventional behavior of neutrophils in developing zebrafish. Blood, 111, 132-141.
Leithner, A., Eichner, A., Müller, J., Reversat, A., Brown, M., Schwarz, J., Merrin, J., … Sixt, M. (2016). Diversified actin protrusions promote environmental exploration but are dispensable for locomotion of leukocytes. Nature Cell Biology, 18, 1253-1259.
Lin, C. S., Aebersold, R. H., Kent, S. B., Varma, M., & Leavitt, J. (1988). Molecular cloning and characterization of plastin, a human leukocyte protein expressed in transformed human fibroblasts. Molecular and Cellular Biology, 8, 4659-4668.
Lin, C. S., Park, T., Chen, Z. P., & Leavitt, J. (1993). Human plastin genes. Comparative gene structure, chromosome location, and differential expression in normal and neoplastic cells. The Journal of Biological Chemistry, 268, 2781-2792.
Luo, B.-H., Carman, C. V., & Springer, T. A. (2007). Structural basis of integrin regulation and signaling. Annual Review of Immunology, 25, 619-647.
Ma, N., Huang, Z., Chen, X., He, F., Wang, K., Liu, W., … Zhang, W. (2011). Characterization of a weak allele of zebrafish cloche mutant. PLoS One, 6, e27540.
Ma, T., Sadashivaiah, K., Madayiputhiya, N., & Chellaiah, M. A. (2010). Regulation of sealing ring formation by L-plastin and cortactin in osteoclasts. The Journal of Biological Chemistry, 285, 29911-29924.
Mathias, J. R., Walters, K. B., & Huttenlocher, A. (2009). Neutrophil motility in vivo using zebrafish. Methods in Molecular Biology, 571, 151-166.
Morley, S. (2012). The actin-bundling protein L-plastin: A critical regulator of immune cell function. International Journal of Cell Biology, 2012, 935173.
Morley, S. C. (2013). The actin-bundling protein L-plastin supports T-cell motility and activation. Immunological Reviews, 256, 48-62.
Ning, Y., Gerger, A., Zhang, W., Hanna, D. L., Yang, D., Winder, T., … Volz, N. (2014). Plastin polymorphisms predict gender-and stage-specific colon cancer recurrence after adjuvant chemotherapy. Molecular Cancer Therapeutics, 13, 528-539.
Nolte, M. A., & Margadant, C. (2020). Activation and suppression of hematopoietic integrins in hemostasis and immunity. Blood, 135, 7-16.
Novoa, B., & Figueras, A. (2012). Zebrafish: model for the study of inflammation and the innate immune response to infectious diseases. Advances in Experimental Medicine and Biology, 946, 253-275.
Pacaud, M., & Derancourt, J. (1993). Purification and further characterization of macrophage-70kDA protein, a calcium-regulated, actin-binding protein identical to L-plastin. Biochemistry, 32, 3448-3455.
Petrie, T. A., Strand, N. S., Yang, C. T., Tsung-Yang, C., Rabinowitz, J. S., & Moon, R. T. (2014). Macrophages modulate adult zebrafish tail fin regeneration. Development, 141, 2581-2591.
Renshaw, S. A., & Trede, N. S. (2012). A model 450 million years in the making: Zebrafish and vertebrate immunity. Disease Models & Mechanisms, 5, 38-47.
Roehl, H. H. (2018). Linking wound response and inflammation to regeneration in the zebrafish larval fin. The International Journal of Developmental Biology, 62, 473-477.
Samstag, Y., & Klemke, M. (2007). Ectopic expression of L-plastin in human tumor cells: Diagnostic and therapeutic implications. Advances in Enzyme Regulation, 47, 118-126.
Schaffner-Reckinger, E., & Machado, R. A. C. (2020). The actin-bundling protein L-plastin-a double-edged sword: beneficial for the immune response, maleficent in cancer. International Review of Cell and Molecular Biology, 355, 109-154.
Schwebach, C. L., Agrawal, R., Lindert, S., Kudryashova, E., & Kudryashov, D. S. (2017). The roles of actin-binding domains 1 and 2 in the calcium-dependent regulation of actin filament bundling by human plastins. Journal of Molecular Biology, 429, 2490-2508.
Sheehan, H. L., & Storey, G. W. (1947). An improved method of staining leucocyte granules with Sudan Black B. The Journal of Pathology and Bacteriology, 59, 336-337.
Shinomiya, H. (2012). Plastin family of actin-bundling proteins: Its functions in leukocytes, neurons, intestines, and cancer. International Journal of Cell Biology, 2012, 1-8.
Spilsbury, K., O'Mara, M. A., Wu, W. M., Rowe, P. B., Symonds, G., & Takayama, Y. (1995). Isolation of a novel macrophage-specific gene by differential cDNA analysis. Blood, 85, 1620-1629.
Springer, T. A., & Dustin, M. L. (2012). Integrin inside-out signaling and the immunological synapse. Current Opinion in Cell Biology, 24, 107-115.
Tiedemann, K., Sadvakassova, G., Mikolajewicz, N., Juhas, M., Sabirova, Z., Tabariès, S., … Komarova, S. V. (2019). Exosomal release of L-plastin by breast cancer cells facilitates metastatic bone osteolysis. Translational Oncology, 12, 462-474.
Tinevez, J. Y., Perry, N., Schindelin, J., Hoopes, G. M., Reynolds, G. D., Laplantine, E., … Eliceiri, K. W. (2017). TrackMate: An open and extensible platform for single-particle tracking. Methods, 115, 80-90.
Todd, E. M., Deady, L. E., & Morley, S. C. (2011). The actin-bundling protein L-plastin is essential for marginal zone B cell development. Journal of Immunology, 187, 3015-3025.
Todd, E. M., Deady, L. E., & Morley, S. C. (2013). Intrinsic T- and B-cell defects impair T-cell-dependent antibody responses in mice lacking the actin-bundling protein L-plastin. European Journal of Immunology, 43, 1735-1744.
Todd, E. M., Zhou, J. Y., Szasz, T. P., Deady, L. E., D'Angelo, J. A., Cheung, M. D., … Morley, S. C. (2016). Alveolar macrophage development in mice requires L-plastin for cellular localization in alveoli. Blood, 128, 2785-2796.
Traver, D., Herbomel, P., Patton, E. E., Murphey, R. D., Yoder, J. A., Litman, G. W., … Trede, N. S. (2003). The zebrafish as a model organism to study development of the immune system. Advances in Immunology, 81, 253-330.
Trede, N. S., Langenau, D. M., Traver, D., Look, A. T., & Zon, L. I. (2004). The use of zebrafish to understand immunity. Immunity, 20, 367-379.
Tseng, H. Y., Samarelli, A. V., Kammerer, P., Scholze, S., Ziegler, T., Immler, R., Zent, R., … Bottcher, R.T. (2018). LCP1 preferentially binds clasped αMβ2 integrin and attenuates leukocyte adhesion under flow. Journal of Cell Science, 131, 22: jcs218214.
van Audenhove, I., Denert, M., Boucherie, C., Pieters, L., Cornelissen, M., & Gettemans, J. (2016). Fascin rigidity and L-plastin flexibility cooperate in cancer cell Invadopodia and Filopodia. The Journal of Biological Chemistry, 291, 9148-9160.
van den Dries, K., Linder, S., Maridonneau-Parini, I., & Poincloux, R. (2019). Probing the mechanical landscape-new insights into podosome architecture and mechanics. Journal of Cell Science, 132, jcs236828.
Wang, C., Morley, S. C., Donermeyer, D., Peng, I., Lee, W. P., Devoss, J., … Brown, E. J. (2010). Actin-bundling protein L-plastin regulates T cell activation. Journal of Immunology, 185, 7487-7497.
Wang, J., Chen, H., & Brown, E. J. (2001). L-plastin peptide activation of alpha(v)beta(3)-mediated adhesion requires integrin conformational change and actin filament disassembly. The Journal of Biological Chemistry, 276, 14474-14481.
Westerfield, M. (2000). The zebrafish book: A guide for the laboratory use of zebrafish (Danio rerio). Eugene, OR: University of Oregon Press.
Xu, X., Wang, X., Todd, E. M., Jaeger, E. R., Vella, J. L., Mooren, O. L., … Huang, Y. H. (2016). Mst1 Kinase regulates the actin-bundling protein L-plastin to promote T cell migration. Journal of Immunology, 197, 1683-1691.
Zhou, J. Y., Szasz, T. P., Stewart-Hutchinson, P. J., Sivapalan, J., Todd, E. M., Deady, L. E., … Morley, S. C. (2016). L-plastin promotes podosome longevity and supports macrophage motility. Molecular Immunology, 78, 79-88.

Auteurs

John B Linehan (JB)

Department of Biological Sciences, DePaul University, Chicago, USA.

Jose Lucas Zepeda (J)

Department of Biological Sciences, DePaul University, Chicago, USA.

Taylor A Mitchell (TA)

Department of Biological Sciences, DePaul University, Chicago, USA.

Elizabeth E LeClair (EE)

Department of Biological Sciences, DePaul University, Chicago, USA.

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