Phagocytosis by thrombocytes is a conserved innate immune mechanism in lower vertebrates

Frontiers in Immunology

Volumn 5, Issue SEP, 2014, Pages

  Nagasawa, Takahiro ^a   Nakayasu, Chihaya ^b   Rieger, Aja M ^c   Barreda, Daniel R ^c   Somamoto, Tomonori ^a   Nakao, Miki ^a  

^a KYUSHU UNIVERSITY   (Japan)

^b FISHERIES RESEARCH AGENCY   (Japan)

^c UNIVERSITY OF ALBERTA   (Canada)

Author keywords

Comparative immunology; Fish immunity; Innate immunity; Phagocytosis; Platelet; Thrombocyte

Indexed keywords

CD11 ANTIGEN; CD18 ANTIGEN; CYTOCHALASIN B; HEMOSTATIC AGENT; LATEX; MYELOPEROXIDASE; NITRIC OXIDE SYNTHASE; T LYMPHOCYTE RECEPTOR;

AMPHIBIA; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CARP; CELL ASSAY; CELL ISOLATION; CELL PHAGOCYTOSIS; CONTROLLED STUDY; ESCHERICHIA COLI; FLOW CYTOMETRY; FLUORESCENCE MICROSCOPY; GENE EXPRESSION; IMMUNE RESPONSE; INNATE IMMUNITY; INTRACELLULAR KILLING; NONHUMAN; PHAGOLYSOSOME; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; TELEOST; THROMBOCYTE; TRANSMISSION ELECTRON MICROSCOPY;

EID: 84919355725     PISSN: None     EISSN: 16643224     Source Type: Journal    
DOI: 10.3389/fimmu.2014.00445     Document Type: Article

References (62)

1. Desjardins M, Houde M, Gagnon E. Phagocytosis: the convoluted way from nutrition to adaptive immunity. Immunol Rev (2005) 207:158-65. doi: 10.1111/j.0105-2896.2005.00319.x
2. Neumann NF, Stafford JL, Barreda D, Ainsworth AJ, Belosevic M. Antimicrobial mechanisms of fish phagocytes and their role in host defense. Dev Comp Immunol (2001) 25(8-9):807-25. doi:10.1016/S0145-305X(01)00037-4
3. Jutras I, Desjardins M. Phagocytosis: at the crossroads of innate and adaptive immunity. Annu Rev Cell Dev Biol (2005) 21:511-27. doi:10.1146/annurev.cellbio.20.010403.102755
4. Li J, Barreda DR, Zhang YA, Boshra H, Gelman AE, Lapatra S, et al. B lymphocytes from early vertebrates have potent phagocytic and microbicidal abilities. Nat Immunol (2006) 7(10):1116-24. doi:10.1038/ni1389
5. Zimmerman LM, Vogel LA, Edwards KA, Bowden RM. Phagocytic B cells in a reptile. Biol Lett (2010) 6(2):270-3. doi:10.1098/rsbl.2009.0692
6. Parra D, Rieger AM, Li J, Zhang YA, Randall LM, Hunter CA, et al. Pivotal advance: peritoneal cavity B-1 B cells have phagocytic and microbicidal capacities and present phagocytosed antigen to CD4+ T cells. J Leukoc Biol (2012) 91(4):525-36. doi:10.1189/jlb.0711372
7. Nakashima M, Kinoshita M, Nakashima H, Habu Y, Miyazaki H, Shono S, et al. Pivotal advance: characterization of mouse liver phagocytic B cells in innate immunity. J Leukoc Biol (2012) 91(4):537-46. doi:10.1189/jlb.0411214
8. Gao J, Ma X, Gu W, Fu M, An J, Xing Y, et al. Novel functions of murine B1 cells: active phagocytic and microbicidal abilities. Eur J Immunol (2012) 42(4):982-92. doi:10.1002/eji.201141519
9. Wu Y, Wu W, Wong WM, Ward E, Thrasher AJ, Goldblatt D, et al. Human gamma delta T cells: a lymphoid lineage cell capable of professional phagocytosis. J Immunol (2009) 183(9):5622-9. doi:10.4049/jimmunol.0901772
10. Kim S, Radhakrishnan UP, Rajpurohit SK, Kulkarni V, Jagadeeswaran P. Vivo-Morpholino knockdown of alphaIIb: a novel approach to inhibit thrombocyte function in adult zebrafish. Blood Cells Mol Dis (2010) 44(3):169-74. doi:10.1016/j.bcmd.2009.12.004
11. Belamarich FA, Fusari MH, Shepro D, Kien M. In vitro studies of aggregation of non-mammalian thrombocytes. Nature (1966) 212(5070):1579-80. doi:10.1038/2121579a0
12. Elzey BD, Sprague DL, Ratliff TL. The emerging role of platelets in adaptive immunity. Cell Immunol (2005) 238(1):1-9. doi:10.1016/j.cellimm.2005.12.005
13. Awadhiya RP, Vegad JL, Kolte GN. Demonstration of the phagocytic activity of chicken thrombocytes using colloidal carbon. Res Vet Sci (1980) 29(1):120-2.
14. Grecchi R, Saliba AM, Mariano M. Morphological changes, surface receptors and phagocytic potential of fowl mono-nuclear phagocytes and thrombocytes in vivo and in vitro. J Pathol (1980) 130(1):23-31. doi:10.1002/path.1711300104
15. Hill DJ, Hallett MB, Rowley AF. Effect of prostanoids and their precursors on the aggregation of rainbow trout thrombocytes. Am J Physiol (1999) 276(3 Pt 2):R659-64.
16. Stosik M, Deptula W, Travnicek M, Baldy-Chudzik K. Phagocytic and bactericidal activity of blood thrombocytes in carps (Cyprinus carpio). Vet. Med. - Czech (2002) 47:21-5.
17. Wigley P, Hulme SD, Barrow PA. Phagocytic and oxidative burst activity of chicken thrombocytes to Salmonella, Escherichia coli and other bacteria. Avian Pathol (1999) 28:567-72. doi:10.1080/03079459994353
18. DaMatta RA, Seabra SH, de Souza W. Further studies on the phagocytic capacity of chicken thrombocytes. J Submicrosc Cytol Pathol (1998) 30(2):271-7.
19. Meseguer J, Esteban MA, Rodriguez A. Are thrombocytes and platelets true phagocytes? Microsc Res Tech (2002) 57(6):491-7. doi:10.1002/jemt.10102
20. Passantino L, Cianciotta A, Patruno R, Ribaud MR, Jirillo E, Passantino GF. Do fish thrombocytes play an immunological role? Their cytoenzymatic profiles and function during an accidental piscine candidiasis in aquarium. Immunopharmacol Immunotoxicol (2005) 27(2):345-56. doi:10.1081/IPH-200067959
21. Daimon T, Uchida K. Cytochemical demonstration of amine-storing vacuoles and lysosomes in the chicken thrombocytes. Histochemistry (1982) 75(3):309-17. doi:10.1007/BF00496734
22. Daimon T, Gotoh Y, Kawai K, Uchida K. Ultrastructural distribution of peroxidase in thrombocytes of mammals and submammals. Histochemistry (1985) 82(4):345-50. doi:10.1007/BF00494063
23. Taffarel M, Oliveira MP. Cytochemical analysis of the content of chicken thrombocytes vacuoles. Cell Biol Int (1993) 17(11):993-9. doi:10.1006/cbir.1993.1028
24. Nakayasu C, Yoshitomi T, Oyamatsu T, Okamoto N, Ikeda Y. Separation of carp (Cyprinus carpio L.) thrombocytes by using a monoclonal antibody, and their aggregation by collagen. Vet Immunol Immunopathol (1997) 57(3-4):337-46. doi:10.1016/S0165-2427(97)00005-6
25. White JG. Uptake of latex particles by blood platelets: phagocytosis or sequestration? Am J Pathol (1972) 69(3):439-58.
26. White JG. Platelets are covercytes, not phagocytes: uptake of bacteria involves channels of the open canalicular system. Platelets (2005) 16(2):121-31. doi:10.1080/09537100400007390
27. Shiraki R, Inoue N, Kawasaki S, Takei A, Kadotani M, Ohnishi Y, et al. Expression of Toll-like receptors on human platelets. Thromb Res (2004) 113(6):379-85. doi:10.1016/j.thromres.2004.03.023
28. Cognasse F, Hamzeh H, Chavarin P, Acquart S, Genin C, Garraud O. Evidence of Toll-like receptor molecules on human platelets. Immunol Cell Biol (2005) 83(2):196-8. doi:10.1111/j.1440-1711.2005.01314.x
29. Andonegui G, Kerfoot SM, McNagny K, Ebbert KV, Patel KD, Kubes P. Platelets express functional Toll-like receptor-4. Blood (2005) 106(7):2417-23. doi:10.1182/blood-2005-03-0916
30. Rosenfeld SI, Looney RJ, Leddy JP, Phipps DC, Abraham GN, Anderson CL. Human platelet Fc receptor for immunoglobulin G. Identification as a 40,000-molecular-weight membrane protein shared by monocytes. J Clin Invest (1985) 76(6):2317-22. doi:10.1172/JCI112242
31. King M, McDermott P, Schreiber AD. Characterization of the Fc gamma receptor on human platelets. Cell Immunol (1990) 128(2):462-79. doi:10.1016/0008-8749(90)90041-O
32. Qian K, Xie F, Gibson AW, Edberg JC, Kimberly RP, Wu J. Functional expression of IgA receptor FcalphaRI on human platelets. J Leukoc Biol (2008) 84(6):1492-500. doi:10.1189/jlb.0508327
33. Lindemann S, Tolley ND, Dixon DA, McIntyre TM, Prescott SM, Zimmerman GA, et al. Activated platelets mediate inflammatory signaling by regulated interleukin 1beta synthesis. J Cell Biol (2001) 154(3):485-90. doi:10.1083/jcb.200105058
34. Henn V, Slupsky JR, Grafe M, Anagnostopoulos I, Forster R, Muller-Berghaus G, et al. CD40 ligand on activated platelets triggers an inflammatory reaction of endothelial cells. Nature (1998) 391(6667):591-4. doi:10.1038/35393
35. Elzey BD, Tian J, Jensen RJ, Swanson AK, Lees JR, Lentz SR, et al. Platelet-mediated modulation of adaptive immunity. A communication link between innate and adaptive immune compartments. Immunity (2003) 19(1):9-19. doi:10.1016/S1074-7613(03)00177-8
36. Movat HZ, Weiser WJ, Glynn MF, Mustard JF. Platelet phagocytosis and aggregation. J Cell Biol (1965) 27(3):531-43. doi:10.1083/jcb.27.3.531
37. Clawson CC, White JG. Platelet interaction with bacteria. II. Fate of the bacteria. Am J Pathol (1971) 65(2):381-97.
38. Youssefian T, Drouin A, Masse JM, Guichard J, Cramer EM. Host defense role of platelets: engulfment of HIV and Staphylococcus aureus occurs in a specific subcellular compartment and is enhanced by platelet activation. Blood (2002) 99(11):4021-9. doi:10.1182/blood-2001-12-0191
39. White JG. Why human platelets fail to kill bacteria. Platelets (2006) 17(3):191-200. doi:10.1080/09537100500441234
40. Kollner B, Fischer U, Rombout JH, Taverne-Thiele JJ, Hansen JD. Potential involvement of rainbow trout thrombocytes in immune functions: a study using a panel of monoclonal antibodies and RT-PCR. Dev Comp Immunol (2004) 28(10):1049-62. doi:10.1016/j.dci.2004.03.005
41. St Paul M, Paolucci S, Barjesteh N, Wood RD, Schat KA, Sharif S. Characterization of chicken thrombocyte responses to toll-like receptor ligands. PLoS One (2012) 7(8):e43381. doi:10.1371/journal.pone.0043381
42. Toda H, Saito Y, Koike T, Takizawa F, Araki K, Yabu T, et al. Conservation of characteristics and functions of CD4 positive lymphocytes in a teleost fish. Dev Comp Immunol (2011) 35(6):650-60. doi:10.1016/j.dci.2011.01.013
43. Matsuyama T, Nakayasu C, Sano M. Immunocytochemical studies of the ontogeny of peripheral blood leucocyte subpopulations in Japanese flounder (Paralichthys olivaceus). Fish Shellfish Immunol (2010) 29(2):362-5. doi:10.1016/j.fsi.2010.03.005
44. Hagemeyer CE, Peter K. Targeting the platelet integrin GPIIb/IIIa. Curr Pharm Des (2010) 16(37):4119-33. doi:10.2174/138161210794519255
45. Lin HF, Traver D, Zhu H, Dooley K, Paw BH, Zon LI, et al. Analysis of thrombocyte development in CD41-GFP transgenic zebrafish. Blood (2005) 106(12):3803-10. doi:10.1182/blood-2005-01-0179
46. Forstermann U, Sessa WC. Nitric oxide synthases: regulation and function. Eur Heart J (2012) 33(7):829-37. doi:10.1093/eurheartj/ehr304 837a-837d
47. Ross GD, Vetvicka V. CR3 (CD11b, CD18): a phagocyte and NK cell membrane receptor with multiple ligand specificities and functions. Clin Exp Immunol (1993) 92(2):181-4. doi:10.1111/j.1365-2249.1993.tb03377.x
48. Imagawa T, Hashimoto Y, Kitagawa H, Kon Y, Kudo N, Sugimura M. Morphology of blood cells in carp (Cyprinus carpio L.). Nihon Juigaku Zasshi (1989) 51(6):1163-72. doi:10.1292/jvms1939.51.1163
49. Worth RG, Kim MK, Kindzelskii AL, Petty HR, Schreiber AD. Signal sequence within Fc gamma RIIA controls calcium wave propagation patterns: apparent role in phagolysosome fusion. Proc Natl Acad Sci U S A (2003) 100(8):4533-8. doi:10.1073/pnas.0836650100
50. Rieger AM, Hall BE, Barreda DR. Macrophage activation differentially modulates particle binding, phagocytosis and downstream antimicrobial mechanisms. Dev Comp Immunol (2010) 34(11):1144-59. doi:10.1016/j.dci.2010.06.006
51. Ibrahim-Granet O, Philippe B, Boleti H, Boisvieux-Ulrich E, Grenet D, Stern M, et al. Phagocytosis and intracellular fate of Aspergillus fumigatus conidia in alveolar macrophages. Infect Immun (2003) 71(2):891-903. doi:10.1128/IAI.71.2.891-903.2003
52. Vosbeck K, James PR, Zimmermann W. Antibiotic action on phagocytosed bacteria measured by a new method for determining viable bacteria. Antimicrob Agents Chemother (1984) 25(6):735-41. doi:10.1128/AAC.25.6.735
53. Meng A, Tang H, Ong BA, Farrell MJ, Lin S. Promoter analysis in living zebrafish embryos identifies a cis-acting motif required for neuronal expression of GATA-2. Proc Natl Acad Sci U S A (1997) 94(12):6267-72. doi:10.1073/pnas.94.12.6267
54. Carradice D, Lieschke GJ. Zebrafish in hematology: sushi or science? Blood (2008) 111(7):3331-42. doi:10.1182/blood-2007-10-052761
55. Tavares-Dias M, de Moraes FR. Leukocyte and thrombocyte reference values for channel catfish (Ictalurus punctatus Raf), with an assessment of morphologic, cytochemical, and ultrastructural features. Vet Clin Pathol (2007) 36(1):49-54. doi:10.1111/j.1939-165X.2007.tb00181.x
56. Petrie-Hanson L, Hohn C, Hanson L. Characterization of rag1 mutant zebrafish leukocytes. BMC Immunol (2009) 10:8. doi:10.1186/1471-2172-10-8
57. Feng Y, Dorhoi A, Mollenkopf HJ, Yin H, Dong Z, Mao L, et al. Platelets direct monocyte differentiation into epithelioid-like multinucleated giant foam cells with suppressive capacity upon mycobacterial stimulation. J Infect Dis (2014). doi:10.1093/infdis/jiu355
58. Deuel TF, Senior RM, Chang D, Griffin GL, Heinrikson RL, Kaiser ET. Platelet factor 4 is chemotactic for neutrophils and monocytes. Proc Natl Acad Sci U S A (1981) 78(7):4584-7. doi:10.1073/pnas.78.7.4584
59. Boehlen F, Clemetson KJ. Platelet chemokines and their receptors: what is their relevance to platelet storage and transfusion practice? Transfus Med (2001) 11(6):403-17. doi:10.1046/j.1365-3148.2001.00340.x
60. Akashi K, Traver D, Miyamoto T, Weissman IL. A clonogenic common myeloid progenitor that gives rise to all myeloid lineages. Nature (2000) 404(6774):193-7. doi:10.1038/35004599
61. Lu M, Kawamoto H, Katsube Y, Ikawa T, Katsura Y. The common myelolymphoid progenitor: a key intermediate stage in hemopoiesis generating T and B cells. J Immunol (2002) 169(7):3519-25. doi:10.4049/jimmunol.169.7.3519
62. Kawamoto H, Katsura Y. A new paradigm for hematopoietic cell lineages: revision of the classical concept of the myeloid-lymphoid dichotomy. Trends Immunol (2009) 30(5):193-200. doi:10.1016/j.it.2009.03.001