L-plastin is essential for alveolar macrophage production and control of pulmonary pneumococcal infection

Infection and Immunity

Volumn 82, Issue 5, 2014, Pages 1982-1993

  Deady, Lauren E ^a   Todd, Elizabeth M ^a   Davis, Chris G ^a   Zhou, Julie Y ^a   Topcagic, Nermina ^a   Edelson, Brian T ^a   Ferkol, Thomas W ^a   Cooper, Megan A ^a   Muenzer, Jared T ^a,b   Morley, Sharon Celeste ^a  

^a WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF ARIZONA COLLEGE OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CEFTRIAXONE; CXCL1 CHEMOKINE; GRANULOCYTE COLONY STIMULATING FACTOR; INTERLEUKIN 1BETA; INTERLEUKIN 6; LEVO PLASTIN; MACROPHAGE INFLAMMATORY PROTEIN 1BETA; MONOCYTE CHEMOTACTIC PROTEIN 1; PROTEIN; RANTES; TUMOR NECROSIS FACTOR ALPHA; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIBIOTIC THERAPY; ARTICLE; B LYMPHOCYTE; BACTERIAL LOAD; CD4+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; CELL DEATH; CELL MATURATION; CELL TYPE; CONTROLLED STUDY; CYTOKINE PRODUCTION; DENDRITIC CELL; FLOW CYTOMETRY; FLUORESCENCE; INFLAMMATORY INFILTRATE; INNATE IMMUNITY; IRRADIATION; LUNG ALVEOLUS MACROPHAGE; LUNG INFECTION; LUNG LAVAGE; LUNG PARENCHYMA; MALE; MORTALITY; MOUSE; NATURAL KILLER CELL; NEUTROPHIL; NONHUMAN; PATHOGEN CLEARANCE; PERITONEUM MACROPHAGE; PNEUMOCOCCAL INFECTION; PRIORITY JOURNAL; PULMONARY PNEUMOCOCCAL INFECTION; T LYMPHOCYTE;

ANIMALS; BRONCHOALVEOLAR LAVAGE FLUID; CELL PROLIFERATION; FEMALE; GENE EXPRESSION REGULATION; HOMEODOMAIN PROTEINS; MACROPHAGES, ALVEOLAR; MALE; MEMBRANE GLYCOPROTEINS; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MICROFILAMENT PROTEINS; PNEUMONIA, PNEUMOCOCCAL;

EID: 84898893561     PISSN: 00199567     EISSN: 10985522     Source Type: Journal    
DOI: 10.1128/IAI.01199-13     Document Type: Article

References (64)

1. Rudan I, El Arifeen S, Bhutta ZA, Black RE, Brooks A, Chan KY, Chopra M, Duke T, Marsh D, Pio A, Simoes EA, Tamburlini G, Theodoratou E, Weber MW, Whitney CG, Campbell H, Qazi SA. 2011. Setting research priorities to reduce global mortality from childhood pneumonia by 2015. PLoS Med. 8:e1001099. http://dx.doi.org/10.1371 /journal.pmed.1001099.
2. Calbo E, Garau J. 2010. Of mice and men: innate immunity in pneumococcal pneumonia. Int. J. Antimicrob. Agents 35:107-113. http://dx.doi.org/10.1016/j.ijantimicag.2009.10.002.
3. Smith AM, McCullers JA, Adler FR. 2011. Mathematical model of a three-stage innate immune response to a pneumococcal lung infection. J. Theor. Biol. 276:106-116. http://dx.doi.org/10.1016/j.jtbi.2011.01.052.
4. Wang J, Barke RA, Charboneau R, Schwendener R, Roy S. 2008. Morphine induces defects in early response of alveolar macrophages to Streptococcus pneumoniae by modulating TLR9-NF-kappa B signaling. J. Immunol. 180:3594-3600. http://www.jimmunol.org/content/180/5/359 4.long.
5. Xu F, Droemann D, Rupp J, Shen H, Wu X, Goldmann T, Hippenstiel S, Zabel P, Dalhoff K. 2008. Modulation of the inflammatory response to Streptococcus pneumoniae in a model of acute lung tissue infection. Am. J. Respir. Cell Mol. Biol. 39:522-529. http://dx.doi.org/10.1165/rcmb.2007-0328OC.
6. Chen WH, Toapanta FR, Shirey KA, Zhang L, Giannelou A, Page C, Frieman MB, Vogel SN, Cross AS. 2012. Potential role for alternatively activated macrophages in the secondary bacterial infection during recovery from influenza. Immunol. Lett. 141:227-234. http://dx.doi.org/10.1016/j.imlet.2011.10.009.
7. Burnham EL, Phang TL, House R, Vandivier RW, Moss M, Gaydos J. 2011. Alveolar macrophage gene expression is altered in the setting of alcohol use disorders. Alcohol. Clin. Exp. Res. 35:284-294. http://dx.doi.org/10.1111/j.1530-0277.2010.01344.x.
8. Lin CS, Aebersold RH, Kent SB, Varma M, Leavitt J. 1988. Molecular cloning and characterization of plastin, a human leukocyte protein expressed in transformed human fibroblasts. Mol. Cell. Biol. 8:4659-4668.
9. Lin CS, Park T, Chen ZP, Leavitt J. 1993. Human plastin genes. Comparative gene structure, chromosome location, and differential expression in normal and neoplastic cells. J. Biol. Chem. 268:2781-2792.
10. Messier JM, Shaw LM, Chafel M, Matsudaira P, Mercurio AM. 1993. Fimbrin localized to an insoluble cytoskeletal fraction is constitutively phosphorylated on its headpiece domain in adherent macrophages. Cell Motil. Cytoskeleton 25:223-233. http://dx.doi.org/10.1002/cm.970250303.
11. Evans JG, Correia I, Krasavina O, Watson N, Matsudaira P. 2003. Macrophage podosomes assemble at the leading lamella by growth and fragmentation. J. Cell Biol. 161:697-705. http://dx.doi.org/10.1083/jcb.200212037.
12. Chen H, Mocsai A, Zhang H, Ding RX, Morisaki JH, White M, Rothfork JM, Heiser P, Colucci-Guyon E, Lowell CA, Gresham HD, Allen PM, Brown EJ. 2003. Role for plastin in host defense distinguishes integrin signaling from cell adhesion and spreading. Immunity 19:95-104. http://dx.doi.org/10.1016/S1074-7613(03)00172-9.
13. Lin SL, Chien CW, Han CL, Chen ES, Kao SH, Chen YJ, Liao F. 2010. Temporal proteomics profiling of lipid rafts in CCR6-activated T cells reveals the integration of actin cytoskeleton dynamics. J. Proteome Res. 9:283-297. http://dx.doi.org/10.1021/pr9006156.
14. Morley SC, Wang C, Lo WL, Lio CW, Zinselmeyer BH, Miller MJ, Brown EJ, Allen PM. 2010. The actin-bundling protein L-plastin dissociates CCR7 proximal signaling from CCR7-induced motility. J. Immunol. 184:3628-3638. http://dx.doi.org/10.4049/jimmunol.0903851.
15. Wabnitz GH, Lohneis P, Kirchgessner H, Jahraus B, Gottwald S, Konstandin M, Klemke M, Samstag Y. 2010. Sustained LFA-1 cluster formation in the immune synapse requires the combined activities of L-plastin and calmodulin. Eur. J. Immunol. 40:2437-2449. http://dx.doi.org/10.1002/eji.201040345.
16. Wang C, Morley SC, Donermeyer D, Peng I, Lee WP, Devoss J, Danilenko DM, Lin Z, Zhang J, Zhou J, Allen PM, Brown EJ. 2010. Actin-bundling protein L-plastin regulates T cell activation. J. Immunol. 185:7487-7497. http://dx.doi.org/10.4049/jimmunol.1001424.
17. Todd EM, Deady LE, Morley SC. 2011. The actin-bundling protein L-plastin is essential for marginal zone B cell development. J. Immunol. 187:3015-3025. http://dx.doi.org/10.4049/jimmunol.1101033.
18. Wabnitz GH, Michalke F, Stober C, Kirchgessner H, Jahraus B, van den Boomen DJ, Samstag Y. 2011. L-plastin phosphorylation: a novel target for the immunosuppressive drug dexamethasone in primary human T cells. Eur. J. Immunol. 41:3157-3169. http://dx.doi.org/10.1002/eji.201041366.
19. Freeley M, O'Dowd F, Paul T, Kashanin D, Davies A, Kelleher D, Long A. 2012. L-plastin regulates polarization and migration in chemokinestimulated human T lymphocytes. J. Immunol. 188:6357-6370. http://dx.doi.org/10.4049/jimmunol.1103242.
20. Schreiber T, Swanson PE, Chang KC, Davis CC, Dunne WM, Karl IE, Reinhart K, Hotchkiss RS. 2006. Both gram-negative and gram-positive experimental pneumonia induce profound lymphocyte but not respiratory epithelial cell apoptosis. Shock 26:271-276. http://dx.doi.org/10.1097 /01.shk0000225856.32260.0d.
21. Muenzer JT, Davis CG, Chang K, Schmidt RE, Dunne WM, Coopersmith CM, Hotchkiss RS. 2010. Characterization and modulation of the immunosuppressive phase of sepsis. Infect. Immun. 78:1582-1592. http: //dx.doi.org/10.1128/IAI.01213-09.
22. McConnell KW, Fox AC, Clark AT, Chang NY, Dominguez JA, Farris AB, Buchman TG, Hunt CR, Coopersmith CM. 2011. The role of heat shock protein 70 in mediating age-dependent mortality in sepsis. J. Immunol. 186:3718-3725. http://dx.doi.org/10.4049/jimmunol.1003652.
23. Edelson BT, KC W, Juang R, Kohyama M, Benoit LA, Klekotka PA, Moon C, Albring JC, Ise W, Michael DG, Bhattacharya D, Stappenbeck TS, Holtzman MJ, Sung SS, Murphy TL, Hildner K, Murphy KM. 2010. Peripheral CD103+ dendritic cells form a unified subset developmentally related to CD8alpha+ conventional dendritic cells. J. Exp. Med. 207:823-836. http://dx.doi.org/10.1084/jem.20091627.
24. Keppel MP, Yang L, Cooper MA. 2013. Murine NK cell intrinsic cytokine-induced memory-like responses are maintained following homeostatic proliferation. J. Immunol. 190:4754-4762. http://dx.doi.org/10.4049/jimmunol.1201742.
25. Todd EM, Deady LE, Morley SC. 2013. Intrinsic T-and B-cell defects impair T-cell-dependent antibody responses in mice lacking the actinbundling protein L-plastin. Eur. J. Immunol. 43:1735-1744. http://dx.doi.org/10.1002/eji.201242780.
26. 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 Res. 45:5643-5647.
27. de Arruda MV, Watson S, Lin CS, Leavitt J, Matsudaira P. 1990. Fimbrin is a homologue of the cytoplasmic phosphoprotein plastin and has domains homologous with calmodulin and actin gelation proteins. J. Cell Biol. 111:1069-1079. http://dx.doi.org/10.1083/jcb.111.3.1069.
28. Pacaud M, Derancourt J. 1993. Purification and further characterization of macrophage 70-kDa protein, a calcium-regulated, actin-binding protein identical to L-plastin. Biochemistry 32:3448-3455. http://dx.doi.org /10.1021/bi00064a031.
29. Wu C, Orozco C, Boyer J, Leglise M, Goodale J, Batalov S, Hodge CL, Haase J, Janes J, Huss JW, III, Su AI. 2009. BioGPS: an extensible and customizable portal for querying and organizing gene annotation resources. Genome Biol. 10:R130. http://dx.doi.org/10.1186/gb-2009-10-11 -r130.
30. Hotchkiss RS, Karl IE. 2003. The pathophysiology and treatment of sepsis. N. Engl. J. Med. 348:138-150. http://dx.doi.org/10.1056 /NEJMra021333.
31. McConnell KW, McDunn JE, Clark AT, Dunne WM, Dixon DJ, Turnbull IR, Dipasco PJ, Osberghaus WF, Sherman B, Martin JR, Walter MJ, Cobb JP, Buchman TG, Hotchkiss RS, Coopersmith CM. 2010. Streptococcus pneumoniae and Pseudomonas aeruginosa pneumonia induce distinct host responses. Crit. Care Med. 38:223-241. http://dx.doi.org/10.1097/CCM.0b013e3181b4a76b.
32. Rubins JB, Pomeroy C. 1997. Role of gamma interferon in the pathogenesis of bacteremic pneumococcal pneumonia. Infect. Immun. 65:2975-2977.
33. Sun K, Salmon SL, Lotz SA, Metzger DW. 2007. Interleukin-12 promotes gamma interferon-dependent neutrophil recruitment in the lung and improves protection against respiratory Streptococcus pneumoniae infection. Infect. Immun. 75:1196-1202. http://dx.doi.org/10.1128/IAI.01403-06.
34. Ivanov S, Fontaine J, Paget C, Macho Fernandez E, Van Maele L, Renneson J, Maillet I, Wolf NM, Rial A, Leger H, Ryffel B, Frisch B, Chabalgoity JA, Sirard JC, Benecke A, Faveeuw C, Trottein F. 2012. Key role for respiratory CD103(+) dendritic cells, IFN-gamma, and IL-17 in protection against Streptococcus pneumoniae infection in response to alpha-galactosylceramide. J. Infect. Dis. 206:723-734. http://dx.doi.org /10.1093/infdis/jis413.
35. Marques JM, Rial A, Munoz N, Pellay FX, Van Maele L, Leger H, Camou T, Sirard JC, Benecke A, Chabalgoity JA. 2012. Protection against Streptococcus pneumoniae serotype 1 acute infection shows a signature of Th17-and IFN-gamma-mediated immunity. Immunobiology 217:420-429. http://dx.doi.org/10.1016/j.imbio.2011.10.012.
36. Lauw FN, Branger J, Florquin S, Speelman P, van Deventer SJ, Akira S, van der Poll T. 2002. IL-18 improves the early antimicrobial host response to pneumococcal pneumonia. J. Immunol. 168:372-378. http: //www.jimmunol.org/content/168/1/372.long.
37. Ferreira DM, Moreno AT, Cianciarullo AM, Ho PL, Oliveira ML, Miyaji EN. 2009. Comparison of the pulmonary response against lethal and non-lethal intranasal challenges with two different pneumococcal strains. Microb. Pathog. 47:157-163. http://dx.doi.org/10.1016/j.micpath.2009.05.005.
38. Wang J, Li F, Zheng M, Sun R, Wei H, Tian Z. 2012. Lung natural killer cells in mice: phenotype and response to respiratory infection. Immunology 137:37-47. http://dx.doi.org/10.1111/j.1365-2567.2012.03607.x.
39. Cooper MA, Fehniger TA, Ponnappan A, Mehta V, Wewers MD, Caligiuri MA. 2001. Interleukin-1beta costimulates interferon-gamma production by human natural killer cells. Eur. J. Immunol. 31:792-801. http://dx.doi.org/10.1002/1521-4141(200103)31:3 <792::AID-IMMU792>3.0.CO;2-U.
40. Matute-Bello G, Lee JS, Frevert CW, Liles WC, Sutlief S, Ballman K, Wong V, Selk A, Martin TR. 2004. Optimal timing to repopulation of resident alveolar macrophages with donor cells following total body irradiation and bone marrow transplantation in mice. J. Immunol. Methods 292:25-34. http://dx.doi.org/10.1016/j.jim.2004.05.010.
41. Hahn I, Klaus A, Maus R, Christman JW, Welte T, Maus UA. 2011. Dendritic cell depletion and repopulation in the lung after irradiation and bone marrow transplantation in mice. Am. J. Respir. Cell Mol. Biol. 45: 534-541. http://dx.doi.org/10.1165/rcmb.2010-0279OC.
42. Chamoto K, Gibney BC, Ackermann M, Lee GS, Lin M, Konerding MA, Tsuda A, Mentzer SJ. 2012. Alveolar macrophage dynamics in murine lung regeneration. J. Cell. Physiol. 227:3208-3215. http://dx.doi.org/10.1002/jcp.24009.
43. Guilliams M, De Kleer I, Henri S, Post S, Vanhoutte L, De Prijck S, Deswarte K, Malissen B, Hammad H, Lambrecht BN. 2013. Alveolar macrophages develop from fetal monocytes that differentiate into longlived cells in the first week of life via GM-CSF. J. Exp. Med. 210:1977-1992. http://dx.doi.org/10.1084/jem.20131199.
44. Trottier MD, Irwin R, Li Y, McCabe LR, Fraker PJ. 2012. Enhanced production of early lineages of monocytic and granulocytic cells in mice with colitis. Proc. Natl. Acad. Sci. U. S. A. 109:16594-16599. http://dx.doi.org/10.1073/pnas.1213854109.
45. Schabbauer G, Matt U, Gunzl P, Warszawska J, Furtner T, Hainzl E, Elbau I, Mesteri I, Doninger B, Binder BR, Knapp S. 2010. Myeloid PTEN promotes inflammation but impairs bactericidal activities during murine pneumococcal pneumonia. J. Immunol. 185:468-476. http://dx.doi.org/10.4049/jimmunol.0902221.
46. Hahn I, Klaus A, Janze AK, Steinwede K, Ding N, Bohling J, Brumshagen C, Serrano H, Gauthier F, Paton JC, Welte T, Maus UA. 2011. Cathepsin G and neutrophil elastase play critical and nonredundant roles in lung-protective immunity against Streptococcus pneumoniae in mice. Infect. Immun. 79:4893-4901. http://dx.doi.org/10.1128/IAI.05593-11.
47. Pittet LA, Quinton LJ, Yamamoto K, Robson BE, Ferrari JD, Algul H, Schmid RM, Mizgerd JP. 2011. Earliest innate immune responses require macrophage RelA during pneumococcal pneumonia. Am. J. Respir. Cell Mol. Biol. 45:573-581. http://dx.doi.org/10.1165/rcmb.2010-0210OC.
48. van der Windt GJ, Hoogendijk AJ, de Vos AF, Kerver ME, Florquin S, van der Poll T. 2011. The role of CD44 in the acute and resolution phase of the host response during pneumococcal pneumonia. Lab. Invest. 91: 588-597. http://dx.doi.org/10.1038/labinvest.2010.206.
49. Skerrett SJ, Liggitt HD, Hajjar AM, Ernst RK, Miller SI, Wilson CB.2004. Respiratory epithelial cells regulate lung inflammation in response to inhaled endotoxin. Am. J. Physiol. Lung Cell. Mol. Physiol. 287:L143-L152. http://dx.doi.org/10.1152/ajplung.00030.2004.
50. Koppe U, Hogner K, Doehn JM, Muller HC, Witzenrath M, Gutbier B, Bauer S, Pribyl T, Hammerschmidt S, Lohmeyer J, Suttorp N, Herold S, Opitz B. 2012. Streptococcus pneumoniae stimulates a STING-and IFN regulatory factor 3-dependent type I IFN production in macrophages, which regulates RANTES production in macrophages, cocultured alveolar epithelial cells, and mouse lungs. J. Immunol. 188:811-817. http://dx.doi.org/10.4049/jimmunol.1004143.
51. Yamamoto K, Ferrari JD, Cao Y, Ramirez MI, Jones MR, Quinton LJ, Mizgerd JP. 2012. Type I alveolar epithelial cells mount innate immune responses during pneumococcal pneumonia. J. Immunol. 189:2450-2459. http://dx.doi.org/10.4049/jimmunol.1200634.
52. Landsman L, Jung S. 2007. Lung macrophages serve as obligatory intermediate between blood monocytes and alveolar macrophages. J. Immunol. 179: 3488-3494. http://www.jimmunol.org/content/179/6/3488.long.
53. Schulz C, Gomez Perdiguero E, Chorro L, Szabo-Rogers H, Cagnard N, Kierdorf K, Prinz M, Wu B, Jacobsen SE, Pollard JW, Frampton J, Liu KJ, Geissmann F. 2012. A lineage of myeloid cells independent of Myb and hematopoietic stem cells. Science 336:86-90. http://dx.doi.org/10.1126/science.1219179.
54. Taut K, Winter C, Briles DE, Paton JC, Christman JW, Maus R, Baumann R, Welte T, Maus UA. 2008. Macrophage turnover kinetics in the lungs of mice infected with Streptococcus pneumoniae. Am. J. Respir. Cell Mol. Biol. 38:105-113. http://dx.doi.org/10.1165/rcmb.2007-0132OC.
55. Ohsawa K, Imai Y, Sasaki Y, Kohsaka S. 2004. Microglia/macrophagespecific protein Iba1 binds to fimbrin and enhances its actin-bundling activity. J. Neurochem. 88:844-856. http://dx.doi.org/10.1046/j.1471 -4159.2003.02213.x.
56. Standish AJ, Weiser JN. 2009. Human neutrophils kill Streptococcus pneumoniae via serine proteases. J. Immunol. 183:2602-2609. http://dx.doi.org/10.4049/jimmunol.0900688.
57. Walker J, Lee R, Mathy N, Doughty S, Conlon J. 1996. Restricted B-cell responses to microbial challenge of the respiratory tract. Vet. Immunol. Immunopathol. 54:197-204. http://dx.doi.org/10.1016 /S0165-2427(96)05709-1.
58. GeurtsvanKessel CH, Willart MA, van Rijt LS, Muskens F, Kool M, Baas C, Thielemans K, Bennett C, Clausen BE, Hoogsteden HC, Osterhaus AD, Rimmelzwaan GF, Lambrecht BN. 2008. Clearance of influenza virus from the lung depends on migratory langerin CD11b+but-not plasmacytoid dendritic cells. J. Exp. Med. 205:1621-1634. http://dx.doi.org/10.1084/jem.20071365.
59. LeMessurier K, Hacker H, Tuomanen E, Redecke V. 2010. Inhibition of T cells provides protection against early invasive pneumococcal disease. Infect. Immun. 78:5287-5294. http://dx.doi.org/10.1128/IAI.00431-10.
60. Teijaro JR, Verhoeven D, Page CA, Turner D, Farber DL. 2010. Memory CD4 T cells direct protective responses to influenza virus in the lungs through helper-independent mechanisms. J. Virol. 84:9217-9226. http: //dx.doi.org/10.1128/JVI.01069-10.
61. Elhaik-Goldman S, Kafka D, Yossef R, Hadad U, Elkabets M, Vallon-Eberhard A, Hulihel L, Jung S, Ghadially H, Braiman A, Apte RN, Mandelboim O, Dagan R, Mizrachi-Nebenzahl Y, Porgador A. 2011. The natural cytotoxicity receptor 1 contribution to early clearance of Streptococcus pneumoniae and to natural killer-macrophage cross talk. PLoS One 6:e23472. http://dx.doi.org/10.1371/journal.pone.0023472.
62. Weber SE, Tian H, Pirofski LA. 2011. CD8+ cells enhance resistance to pulmonary serotype 3 Streptococcus pneumoniae infection in mice. J. Immunol. 186:432-442. http://dx.doi.org/10.4049/jimmunol.1001963.
63. Winter C, Taut K, Langer F, Mack M, Briles DE, Paton JC, Maus R, Srivastava M, Welte T, Maus UA. 2007. FMS-like tyrosine kinase 3 ligand aggravates the lung inflammatory response to Streptococcus pneumoniae infection in mice: role of dendritic cells. J. Immunol. 179:3099-3108. http: //www.jimmunol.org/content/179/5/3099.long.
64. Rosendahl A, Bergmann S, Hammerschmidt S, Goldmann O, Medina E. 2013. Lung dendritic cells facilitate extrapulmonary bacterial dissemination during pneumococcal pneumonia. Front. Cell. Infect. Microbiol. 3:21. http://dx.doi.org/10.3389/fcimb.2013.00021.