REVIEW PAPER
Coronins and their role in immunological phenomena
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Submission date: 2015-09-24
Final revision date: 2016-01-06
Acceptance date: 2016-01-12
Publication date: 2017-01-24
Cent Eur J Immunol 2016;41(4):435-441
KEYWORDS
ABSTRACT
Coronins are a large family of proteins occurring in many eukaryotes. In mammals, seven coronin genes have been identified, evidencing that coronins 1 to 6 present classic coronin structure, while coronin 7 is a tandem coronin particle, without a spiral domain, although the best characterised coronin, in terms of both structure and function, is the mammalian coronin 1. It has been proven that they are related to regulation of actin dynamics, e.g. as a result of interaction with the complex of proteins Arp2/3. These proteins also modulate the activity of immune system cells, including lymphocyte T and B cells, neutrophils and macrophages. They are involved in bacterial infections with Mycobacterium tuberculosis, M. leprae and Helicobacter pylori and participate in the response to viral infections, e.g. infections of lymphocytic choriomeningitis virus (LCMV) and vesicular stomatitis Indiana virus (VSV). Also their involvement in autoimmune diseases such as lupus erythematosus has been recorded.
REFERENCES (93)
1.
Eckert C, Hammesfahr B, Kollmar M (2011): A holistic phylogeny of the coronin gene family reveals an ancient origin of the tandem-coronin, defines a new subfamily, and predicts protein function. BMC Evol Biol 11: 268.
2.
Pieters J, Müller P, Jayachandran R (2013): On guard: coronin proteins in innate and adaptive immunity. Nat Rev Immunol 13: 510-518.
3.
Gatfield J, Albrecht I, Zanolari B, et al. (2005): Association of the leukocyte plasma membrane with the aetin cytoskeleton through coiled coil-mediated trimeric coronin 1 molecules. Mol Biol Cell 16: 2786-2798.
4.
Kammerer RA, Kostrewa D, Progias P, et al. (2005): A conserved trimerization motif controls the topology of short coiled coils. Proc Natl Acad Sci U S A 102: 13891-13896.
5.
Rybakin V, Stumpf M, Schulze A, et al. (2004): Coronin 7, the mammalian POD-l homologue, localizes to the Golgi apparatus. FEBS Lett 573: 161-167.
6.
de Hostos EL (1999): The coronin family of actin-associated proteins. Trends Cell Biol 9: 345-350.
7.
Rybakin V, CIemen CS (2005): Coronin proteins as multifunctional regulators of the cytoskeleton and membrane trafficking. Bioessays 27: 625-632.
8.
Okumura M, Kung C, Wong S, et al. (1998): Definition of family of coronin-related proteins conserved between humans and mice: close genetic linkage between coronin-2 and CD45-associated protein. DNA Cell Biol 17: 779-787.
9.
Nakamura T, Takeuchi K, Muraoka S, et al. (1999): A neurally enriched coranin-like protein, Clipin C, is novel candidate for an actin cytoskeleton-cortical membrane-linking protein. J Biol Chem 274: 13322-13327.
10.
Gatfield J, Pieters J (2000): Essential role for cholesterol in entry of mycobacteria into macrophages. Science 288: 1647-1650.
11.
Huang W, Ghisletti S, Saijo K, et al. (2011): Coranin 2A mediates actin-dependent de-repression of inflammatory response genes. Nature 470: 414-418.
12.
de Hostos EL, Rehfuess C, Bradtke B, et al. (1993): Dictyostelium mutants lacking the cytoskeletal protein coronin are defective in cytokinesis and cell motility. J Cell Biol 120: 163-173.
13.
de Hostos EL, Bradtke B, Lottspeich F, et al. (1991): Coronin, an actin binding protein of Dictyostelium discoideum localized to cell surface projections, has sequence similarities to G protein subunits. EMBO J 1: 4097-4104.
14.
Cal L, Makhov AM, Bear JE (2007): F-actin binding is essential for coronin 1 B function in vivo. J Cell Sci 120: 1779-1790.
15.
Cai L, Marshall TW, Uetrecht AC, et al. (2007): Coronin 1 B coordinates Arp2/3 complex and cofilin activities at the leading edge. Cell 128: 915-929.
16.
Foger N, Rangell L, Danilenko DM, et al. (2006): Requirement for coronin 1 in T lymphocyte trafficking and cellular homeostasis. Science 313: 839-842.
17.
Gaikin VE, Orlova A, Brieher W, et al. (2008): Coronin-l A stabilizes F-actin by bridging adjacent actin protomers and stapling opposite strands of the actin filament. J Mol Biol 376: 607-613.
18.
Haraldsson MK, Louis-Dit-Sully CA, Lawson BR, et al. (2008): The lupus-related Lmb3 locus contains a disease-suppressing Coronin – 1A gene mutation. Immunity 28: 40-51.
19.
Shiow LR, Paris K, Akana MC, et al. (2009): Severe combined immunodeficiency (SCID) and attention deficit hyperactivity disorder (ADHD) associated with a Coronin-lA mutation and a chromosome 16p11.2 deletion. Clin Immunol 131: 24-30.
20.
Moshous D, Martin E, Carpentier W, et al. (2013): Whole-exome sequencing identifies coronin-l A deficiency in three siblings with immunodeficiency and EBV-associated B cell lymphoproliferation. J Allergy Clin Immunol 131: 1594-1603.
21.
Armstrong JA, Hart PD (1975): Phagosome-lysosome interactions in cultured macrophages infected with virulent tubercle bacilli. Reversal of the usual nonfusion pattern and observations on bacterial survival. J Exp Med 142: 1-16.
22.
Russell DG (2001): Mycobacterium tuberculosis: here today, and here tomorrow. Nat Rev Mol Cell Biol 2: 569-577.
23.
Pieters J (2008): Mycobacterium tuberculosis and the macrophage: maintaining a balance. Cell Host Microbe 3: 399-407.
24.
Hasan Z, Schlax C, Kuhn L, et al. (1997): Isolation and characterization of the mycobacterial phagosome: segregation from the endosomal/lysosomal pathway. Mol Microbiol 24: 545-553.
25.
Ferrari G, Langen H, Naito M, et al. (1999): A coat protein on phagosomes involved in the intracellular survival of mycobacteria. Cell 97: 435-447.
26.
Suzuki K, Nishihata J, Arai Y, et al. (1995): Molecular cloning of a novel actin-binding protein, p57, with a WD repeat and a leucine zipper motif. FEBS Lett 364: 283-288.
27.
Mouse Genome Sequencing Consortium, Waterston RH, Lindblad-Toh K, Birney E, et al. (2002): Initial sequencing and comparative analysis of the mouse genome. Nature 420: 520-562.
28.
Lander ES, Linton LM, Birren B, et al. (2001): Initial sequencing and analysis of the human genome. Nature 409: 860-921.
29.
Venter JC, Adams MD, Myers EW, et al. (2001): The sequence of the human genome. Science 291: 1304-1351.
30.
Jayachandran R, Sundaramurthy V, Combaluzier B, et al. (2007): Survival of mycobacteria in macrophages is mediated by coronin l-dependent activation of calcineurin. Cell 130: 37-50.
31.
Jayachandran R, Gatfield J, Massner J, et al. (2008): RNA interference in J774 macrophages reveals a role for coronin 1 in mycobacterial trafficking but not in actin•dependent processes. Mol Biol Cell 19: 1241-1251.
32.
Kumar D, Nath L, Kamal MA, et al. (2010): Genome-wide analysis of the host intracellular network that regulates survival of Mycobacterium tuberculosis. Cell 140: 731-743.
33.
Seto S, Tsujimura K, Koide Y (2012): Coronin-la inhibits autophagosome formation around Mycobacterium tuberculosis-containing phagosomes and assists mycobacterial survival in macrophages. Cell Microbiol 14: 710-727.
34.
Suzuki K, Takeshita F, Nakata N, et al. (2006): Localization of CORO1A in the macrophages containing Mycobacterium leprae. Acta Histochem Cytochem 39: 107-112.
35.
Sibley LD, Franzblau SG, Krahenbuhl JL (1987): Intracellular fate of Mycobacterium leprae in normal and activated mouse macrophages. Infect Immun 55: 680-685.
36.
Montoya D, Modlin RL (2010): Learning from leprosy: insight into the human innate immune response. Adv Immunol 105: 1-24.
37.
Allen LA, Schlesinger LS, Kang B (2000): Virulent strains oh Helicobacter pylori demonstrate delayed phagocytosis and stimulate homotypic phagosome fusion in macrophages. J Exp Med 191: 115-128.
38.
Falkow S (2006): Is persistent bacterial infection good for your health? Cell 124: 699-702.
39.
Janeway CA Jr. (1989): Approaching the asymptote? Evolution and revolution in immunology. Cold Spring Harb Symp Ouant Biol 54: 1-13.
40.
Dory D, Echchannaoui H, Letiembre M, et al. (2003): Generation and functional characterization of a clonal murine periportal Kupffer cell line from H-2Kb-tsA58 mice. J Leukoc Biol 74: 49-59.
41.
Wardle EN (1987): Kupffer cells and their function. Liver 7: 63-75.
42.
Brandborg LL, Goldman IS (1990): Hepatology: A Textbook of Liver Disease. Saunders, Philadelphia; 1086-1098.
43.
North RJ (1974): T cell dependence of macrophage activation and mobilization during infection with Mycobacterium tuberculosis. Infect Immun 10: 66-71.
44.
Mendez-Samperio P, Palma-Barrios J, Vazquez-Hernandez A, et al. (2004): Secretion of interleukin-8 by human-derived cell lines infected with Mycobacterium bovis. Mediators Inflamm 13: 45-49.
45.
Mendez-Samperio P, Alba L, Trejo A (2007): Mycobacterium bovis-mediated induction of human beta-defensin-2 in epithelial cells is controlled by intracellular calcium and p38MAPK. J Infect 54: 469-474.
46.
Mendez-Samperio P, Trejo A, Miranda E (2006): Activation of ERK1/2 and TNF- production are mediated by calcium/calmodulin, and PKA signaling pathways during Mycobacterium bovis infection. J Infect 52: 147-153.
47.
Rojas M, Garcia LE, Nigou J, et al. (2000): Mannosylated lipoarabinomannan antagonizes Mycobocterium tuberculosis-induced macrophage apoptosis by altering Cah+2-dependent cell signaling. J Infect Dis 182: 240-251.
48.
Carrithers LM, Hulseberg P, Sandor M, et al. (2011): The human macrophage sodium channel NaV1.5 regulates mycobacteria processing through organelle polarization and localized calcium oscillations. FEMS Immunol Med Microbiol 63: 319-327.
49.
Winslow MM, Neilson JR, Crabtree GR (2003): Calcium signalling in lymphocytes. Curr Opin Immunol 15: 299-307.
50.
Klee CB, Crouch TH, Krinks MH (1979): Calcineurin: a calcium-and calmodulin-binding protein of the nervous system. Proc Natl Acad Sci U S A 76: 6270-6273.
51.
Stewart AA, Ingebritsen TS, Manalan A, et al. (1982): Discovery of a Ca2+-and calmodulin-dependent protein phosphatase: probable identity with calcineurin’ [CaM-BP80). FEBS Lett 137: 80-84.
52.
Tchanga VS, Mekker A, Siegmund K, et al. (2013): Diverging role for coronin 1 in antiviral CD4+ and CD8+ T cell responses. Mol Immunol 56: 683-692.
53.
Fung-Leung WP, Kundig TM, Zinkernagel RM, et al. (1991): Immuneresponse against lymphocytic choriomeningitis virus infection in mice without CD8 expression. J Exp Med 174: 1425-1429.
54.
Thomsen AR, Johansen J, Marker O, et al. (1996): Exhaustion of CTL memory and recrudescence of viremia in lymphocytic choriomeningitis virus-infected MHC class II-deficient mice and B cell-deficient mice. J Immunol 157: 3074-3080.
55.
Moriceau S, Kantari C, Mocek J, et al. (2009): Coronin-1 is associated with neutrophil survival and is cleaved during apoptosis: potential implication in neutrophils from cystic fibrosis patients. J Immunol 182: 7254-7263.
56.
Yan M, Di Ciano-Oliveira C, Grinstein S, et al. (2007): Coronin function is required for chemotaxis and phagocytosis in human neutrophils. J Immunol 178: 5769-5778.
57.
Westritschnig K, Bosedasgupta S, Tchang V, et al. (2013): Antigen processing and presentation by dendritic cells is independent of coronin 1. Mol Immunol 53: 379-386.
58.
Muller U, Steinhoff U, Reis LF, et al. (1994): Functional role of type I and type II interferons in antiviral defense. Science 264: 1918-1921.
59.
Thomsen A, Nansen A, Andersen C, et al. (1997): Cooperation of B cells and T cells is required for survival of mice infected with vesicular stomatitis virus. Int Immunol 9: 1757-1766.
60.
Mace EM, Orange JS (2014): Lytic immune synapse function requires filamentous actin deconstruction by coronin 1a. Proc Natl Acad Sci U S A 6: 6708-6713.
61.
Föger N, Jenckel A, Orinska Z, et al. (2011): Differential regulation of mast cell degranulation versus cytokine secretion by the actin regulatory proteins coronin1a and coronin1b. J Exp Med 208: 1777-1787.
62.
Arandjelovic S, McKenney KR, Leming SS, et al. (2010): Mast cell function is not altered by coronin-1A deficiency. J Leukoc Biol 88: 737-745.
63.
Mueller P, Massner J, Jayachandran R, et al. (2008): Regulation of T cell survival through coronin-1-mediated generation of inositol-1,4,5-trisphosphate and calcium mobilization after.
64.
T cell receptor triggering. Nat Immunol 9: 424-431.
65.
Shiow LR, Roadcap DW, Paris K, et al. (2008): The actin regulator coronin 1A is mutant in a thymic egress-deficient mouse strain and in a patient with severe combined immunodeficiency. Nat Immunol 9: 1307-1315.
66.
Combaluzier B, Pieters J (2009): Chemotaxis and phagocytosis in neutrophils is independent of coronin 1. J Immunol 182: 2745-2752.
67.
Mueller P, Liu X, Pieters J (2011): Migration and homeostasis of naive T cells depends on coronin 1-mediated prosurvival signals and not on coronin 1-dependent filamentous actin modulation. J Immunol 186: 4039-4050.
68.
Gallo EM, Cante-Barrett K, Crabtree GR (2006): Lymphocyte calcium signaling from membrane to nucleus. Nat Immunol 7: 25-32.
69.
Combaluzier B, Mueller P, Massner J, et al. (2009): Coronin 1 is essential for IgM-mediated Ca2+ mobilization in B cells but dispensable for the generation of immune responses in vivo. J Immunol 182: 1954-1961.
70.
Kerstan A, Armbruster N, Leverkus M, et al. (2006): Cyclosporin A abolishes CD28-mediated resistance to CD95-induced apoptosis via superinduction of caspase-3. J Immunol 177: 7689-7697.
71.
Mugnier B, Nal B, Verthuy C, et al. (2008): Coronin-1A links cytoskeleton dynamics to TCR-induced cell signaling. PLoS One 3: e3467.
72.
Ma A, Pena JC, Chang B, et al. (1995): Bclx regulates the survival of double-positive thymocytes. Proc Natl Acad Sci U S A 92: 4763-4767.
73.
Motoyama N, Wang F, Roth KA, et al. (1995): Massive cell death of immature hematopoietic cells and neurons in Bcl-x-deficient mice. Science 267: 1506-1510.
74.
Surh CD, Sprent J (2008): Homeostasis of naive and memory T cells. Immunity 29: 848-862.
75.
Manicassamy S, Gupta S, Huang Z, et al. (2008): Requirement of calcineurin- for the survival of naive T cells. J Immunol 180: 106-112.
76.
Bueno OF, Brandt EB, Rothenberg ME, et al. (2002): Defective T cell development and function in calcineurin-A-deficient mice. Proc Natl Acad Sci U S A 99: 9398-9403.
77.
Yagi H, Matsumoto M, Nakamura M, et al. (1996): Defect of thymocyte emigration in a T cell deficiency strain (CTS) of the mouse. J Immunol 157: 3412-3419.
78.
Polic B, Kunkel D, Scheffold A, et al. (2001): How T cells deal with induced TCR ablation. Proc Natl Acad Sci U S A 98: 8744-8749.
79.
Labrecque N, Whitfield LS, Obst R, et al. (2001): How much TCR does a T cell need? Immunity 15: 71-82.
80.
Takeda S, Rodewald HR, Arakawa H, et al. (1996): MHC class II molecules are not required for survival of newly generated CD4+ T cells, but affect their long-term life span. Immunity 5: 217-228.
81.
Kirberg J, Berns A, von Boehmer H (1997): Peripheral T cell survival requires continual ligation of the T cell receptor to major histocompatibility complex-encoded molecules. J Exp Med 186: 1269-1275.
82.
Tanchot C, Lemonnier FA, Perarnau B, et al. (1997): Differential requirements for survival and proliferation of CD8 naive or memory T cells. Science 276: 2057-2062.
83.
Swain SL (2000): CD4 T-cell memory can persist in the absence of class II. Philos Trans R Soc Lond B Biol Sci 355: 407-411.
84.
Murali-Krishna K, Lau LL, Sambhara S, et al. (1999): Persistence of memory CD8 T cells in MHC class I-deficient mice. Science 286: 1377-1381.
85.
Zheng PY, Jones NL (2003): Helicobacter pylori strains expressing the vacuolating cytotoxin interrupt phagosome maturation in macrophages by recruiting and retaining TACO (coronin l) protein. Cell Microbiol 5: 25-40.
86.
Battegay M, Bachmann MF, Burhkart C, et al. (1996): Antiviral immune responses of mice lacking MHC class II or its associated invariant chain. Cell Immunol 167: 115-121.
87.
Siegmund K, Zeis T, Kunz G, et al. (2011): Coronin 1-mediated naive T cell survival is essential for the development of autoimmune encephalomyelitis. J Immunol 186: 3452-3461.
88.
Pareek TK, Lam E, Zheng X, et al. (2010): Cyclin-dependent kinase 5 activity is required for T cell activation and induction of experimental autoimmune encephalomyelitis. J Exp Med 207: 2507-2519.
89.
Kaminski S, Hermann-Kleiter N, Meisel M, et al. (2011): Coronin 1A is an essential regulator of the TGF receptor/SMAD3 signaling pathway in Th17 CD4+ T cells. J Autoimmun 37: 198-208.
90.
Bettelli E, Oukka M, Kuchroo VK (2007): TH17 cells in the circle of immunity and autoimmunity. Nat Immunol 8: 345-350.
91.
Weaver CT, Hatton RD, Mangan PR, et al. (2007): IL-17 family cytokines and the expanding diversity of effector T cell lineages. Annu Rev Immunol 25: 821-852.
92.
Hogquist KA (2008): Immunodeficiency: when T cells are stuck at home. Nat Immunol 9: 1207-1208.
93.
Santiago-Raber ML, Haraldsson MK, Theofilopoulos AN, et al. (2007): Characterization of reciprocal Lmb1-4 interval MRL-Faslpr and C57BL/6-Faslpr congenic mice reveals significant effects from Lmb3. J Immunol 178: 8195-8202.