Human B cells have an active phagocytic capability and undergo immune activation upon phagocytosis of Mycobacterium tuberculosis

Immunobiology

Volumn 221, Issue 4, 2016, Pages 558-567

  Zhu, Qi ^a,b   Zhang, Min ^c   Shi, Ming ^a   Liu, Yang ^a,d   Zhao, Qing ^a   Wang, Wenjing ^a   Zhang, Guangyun ^a   Yang, Longxiu ^a,e   Zhi, Jin ^a,f   Zhang, Lin ^a   Hu, Gengyao ^a   Chen, Pin ^a   Yang, Yining ^a   Dai, Wen ^a   Liu, Tingting ^a   He, Ying ^a   Feng, Guodong ^a   Zhao, Gang ^a  

^a FOURTH MILITARY MEDICAL UNIVERSITY   (China)

^b WUHAN GENERAL HOSPITAL OF GUANGZHOU COMMAND   (China)

^c Fuzhou Dongfang Hospital   (China)

^d The 153 Central Hospital of Chinese PLA   (China)

^e FIRST AFFILIATED HOSPITAL OF GUANGXI MEDICAL UNIVERSITY   (China)

^f The First People's Hospital of Xi'an City   (China)

Author keywords

Human B cells; Immune response; Mycobacterium tuberculosis; Phagocytosis; Raji cells

Indexed keywords

B7 ANTIGEN; CD86 ANTIGEN; CYTOCHALASIN B; IMMUNOGLOBULIN G; IMMUNOGLOBULIN M; MICROSPHERE;

ARTICLE; B LYMPHOCYTE; BACTERIAL VIABILITY; CONFOCAL MICROSCOPY; CONTROLLED STUDY; FLOW CYTOMETRY; HUMAN; HUMAN CELL; IMMUNOGLOBULIN PRODUCTION; IMMUNOREGULATION; IMMUNOSTIMULATION; INCUBATION TIME; INNATE IMMUNITY; LYMPHOCYTE FUNCTION; MYCOBACTERIUM TUBERCULOSIS; OPSONIZATION; PHAGOCYTOSIS; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAJI CELL LINE; SCANNING ELECTRON MICROSCOPY; TEMPERATURE SENSITIVITY; TRANSMISSION ELECTRON MICROSCOPY; CHEMISTRY; DRUG EFFECTS; GENE EXPRESSION REGULATION; GENETICS; HOST PATHOGEN INTERACTION; IMMUNOLOGY; LYMPHOCYTE ACTIVATION; SIGNAL TRANSDUCTION; TUMOR CELL LINE; ULTRASTRUCTURE;

ANTIGENS, CD80; ANTIGENS, CD86; B-LYMPHOCYTES; CELL LINE, TUMOR; CYTOCHALASIN B; GENE EXPRESSION REGULATION; HOST-PATHOGEN INTERACTIONS; HUMANS; IMMUNOGLOBULIN M; LYMPHOCYTE ACTIVATION; MICROSPHERES; MYCOBACTERIUM TUBERCULOSIS; PHAGOCYTOSIS; SIGNAL TRANSDUCTION;

EID: 84950275395     PISSN: 01712985     EISSN: 18783279     Source Type: Journal    
DOI: 10.1016/j.imbio.2015.12.003     Document Type: Article

References (50)

1. Abebe F., Bjune G. The protective role of antibody responses during Mycobacterium tuberculosis infection. Clin. Exp. Immunol. 2009, 157:235-243.
2. Aderem A. How to eat something bigger than your head. Cell 2002, 110:5-8.
3. Barral P., Eckl-Dorna J., Harwood N.E., De Santo C., Salio M., Illarionov P., Besra G.S., Cerundolo V., Batista F.D. B cell receptor-mediated uptake of CD1d-restricted antigen augments antibody responses by recruiting invariant NKT cell help in vivo. Proc. Natl. Acad. Sci. U. S. A. 2008, 105:8345-8350.
4. Bohnsack J.F., O'Shea J.J., Takahashi T., Brown E.J. Fibronectin-enhanced phagocytosis of an alternative pathway activator by human culture-derived macrophages is mediated by the C4b/C3b complement receptor (CR1). J. Immunol. 1985, 135:2680-2686.
5. Botelho R.J., Grinstein S. Phagocytosis. Curr. Biol. 2011, 21:R533-R538.
6. Brekke O.L., Christiansen D., Fure H., Fung M., Mollnes T.E. The role of complement C3 opsonization, C5a receptor, and CD14 in E. coli-induced up-regulation of granulocyte and monocyte CD11b/CD18 (CR3), phagocytosis, and oxidative burst in human whole blood. J. Leukoc. Biol. 2007, 81:1404-1413.
7. Brodsky F.M. Living with clathrin: its role in intracellular membrane traffic. Science 1988, 242:1396-1402.
8. Cardelli J. Phagocytosis and macropinocytosis in Dictyostelium: phosphoinositide-based processes, biochemically distinct. Traffic 2001, 2:311-320.
9. Castellano F., Chavrier P., Caron E. Actin dynamics during phagocytosis. Semin. Immunol. 2001, 13:347-355.
10. Chen P., Shi M., Feng G.D., Liu J.Y., Wang B.J., Shi X.D., Ma L., Liu X.D., Yang Y.N., Dai W., Liu T.T., He Y., Li J.G., Hao X.K., Zhao G. A highly efficient Ziehl-Neelsen stain: identifying de novo intracellular Mycobacterium tuberculosis and improving detection of extracellular M. tuberculosis in cerebrospinal fluid. J. Clin. Microbiol. 2012, 50:1166-1170.
11. Cossart P., Sansonetti P.J. Bacterial invasion: the paradigms of enteroinvasive pathogens. Science 2004, 304:242-248.
12. Desjardins M., Griffiths G. Phagocytosis: latex leads the way. Curr. Opin. Cell Biol. 2003, 15:498-503.
13. Ezekowitz R.A., Sim R.B., Hill M., Gordon S. Local opsonization by secreted macrophage complement components. Role of receptors for complement in uptake of zymosan. J. Exp. Med. 1984, 159:244-260.
14. Feger J., Gil-Falgon S., Lamaze C. Cell receptors: definition: mechanisms and regulation of receptor-mediated endocytosis. Cell. Mol. Biol. 1994, 40:1039-1061.
15. Gao J., Ma X., Gu W., Fu M., An J., Xing Y., Gao T., Li W., Liu Y. Novel functions of murine B1 cells: active phagocytic and microbicidal abilities. Eur. J. Immunol. 2012, 42:982-992.
16. Garcia-Perez B.E., Mondragon-Flores R., Luna-Herrera J. Internalization of Mycobacterium tuberculosis by macropinocytosis in non-phagocytic cells. Microb. Pathog. 2003, 35:49-55.
17. Garcia-Perez B.E., De la Cruz-Lopez J.J., Castaneda-Sanchez J.I., Munoz-Duarte A.R., Hernandez-Perez A.D., Villegas-Castrejon H., Garcia-Latorre E., Caamal-Ley A., Luna-Herrera J. Macropinocytosis is responsible for the uptake of pathogenic and non-pathogenic mycobacteria by B lymphocytes (Raji cells). BMC Microbiol. 2012, 12:246.
18. Greenberg S., Grinstein S. Phagocytosis and innate immunity. Curr. Opin. Immunol. 2002, 14:136-145.
19. Harnack U., Kellermann U., Pecher G. Yeast-derived beta-(1-3), (1-6)-d-glucan induces up-regulation of CD86 on dectin-1-positive human B-lymphoma cell lines. Anticancer Res. 2011, 31:4195-4199.
20. Kremlitzka M., Polgar A., Fulop L., Kiss E., Poor G., Erdei A. Complement receptor type 1 (CR1, CD35) is a potent inhibitor of B-cell functions in rheumatoid arthritis patients. Int. Immunol. 2013, 25:25-33.
21. Krocova Z., Hartlova A., Souckova D., Zivna L., Kroca M., Rudolf E., Macela A., Stulik J. Interaction of B cells with intracellular pathogen Francisella tularensis. Microb. Pathog. 2008, 45:79-85.
22. Lehmann A.K., Sornes S., Halstensen A. Phagocytosis: measurement by flow cytometry. J. Immunol. Methods 2000, 243:229-242.
23. Lenschow D.J., Walunas T.L., Bluestone J.A. CD28/B7 system of T cell costimulation. Annu. Rev. Immunol. 1996, 14:233-258.
24. Li J., Barreda D.R., Zhang Y.A., Boshra H., Gelman A.E., Lapatra S., Tort L., Sunyer J.O. B lymphocytes from early vertebrates have potent phagocytic and microbicidal abilities. Nat. Immunol. 2006, 7:1116-1124.
25. Liu D., Niu Z.X. The structure, genetic polymorphisms, expression and biological functions of complement receptor type 1 (CR1/CD35). Immunopharmacol. Immunotoxicol. 2009, 31:524-535.
26. Lombardi G., del Gallo F., Vismara D., Piccolella E., de Martino C., Garzelli C., Puglisi C., Colizzi V. Epstein-Barr virus-transformed B cells process and present Mycobacterium tuberculosis particulate antigens to T-cell clones. Cell. Immunol. 1987, 107:281-292.
27. Maglione P.J., Chan J. How B cells shape the immune response against Mycobacterium tuberculosis. Eur. J. Immunol. 2009, 39:676-686.
28. Menon A., Shroyer M.L., Wampler J.L., Chawan C.B., Bhunia A.K. In vitro study of Listeria monocytogenes infection to murine primary and human transformed B cells. Comp. Immunol. Microbiol. Infect. Dis. 2003, 26:157-174.
29. Mikami N., Sakaguchi S. CD28 signals the differential control of regulatory T cells and effector T cells. Eur. J. Immunol. 2014, 44:955-957.
30. Moore T., Ekworomadu C.O., Eko F.O., MacMillan L., Ramey K., Ananaba G.A., Patrickson J.W., Nagappan P.R., Lyn D., Black C.M., Igietseme J.U. Fc receptor-mediated antibody regulation of T cell immunity against intracellular pathogens. J. Infect. Dis. 2003, 188:617-624.
31. Nakashima M., Kinoshita M., Nakashima H., Habu Y., Miyazaki H., Shono S., Hiroi S., Shinomiya N., Nakanishi K., Seki S. Pivotal advance: characterization of mouse liver phagocytic B cells in innate immunity. J. Leukoc. Biol. 2012, 91:537-546.
32. Nguyen L., Pieters J. The Trojan horse: survival tactics of pathogenic mycobacteria in macrophages. Trends Cell Biol. 2005, 15:269-276.
33. Ochando J.C., Homma C., Yang Y., Hidalgo A., Garin A., Tacke F., Angeli V., Li Y., Boros P., Ding Y., Jessberger R., Trinchieri G., Lira S.A., Randolph G.J., Bromberg J.S. Alloantigen-presenting plasmacytoid dendritic cells mediate tolerance to vascularized grafts. Nat. Immunol. 2006, 7:652-662.
34. Overland H.S., Pettersen E.F., Ronneseth A., Wergeland H.I. Phagocytosis by B-cells and neutrophils in Atlantic salmon (Salmo salar L.) and Atlantic cod (Gadus morhua L.). Fish Shellfish Immunol. 2010, 28:193-204.
35. Parra D., Rieger A.M., Li J., Zhang Y.A., Randall L.M., Hunter C.A., Barreda D.R., Sunyer J.O. 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, 91:525-536.
36. Pieters J. Mycobacterium tuberculosis and the macrophage: maintaining a balance. Cell Host Microbe 2008, 3:399-407.
37. Rabinovitch M. Professional and non-professional phagocytes: an introduction. Trends Cell Biol. 1995, 5:85-87.
38. Redelman-Sidi G., Iyer G., Solit D.B., Glickman M.S. Oncogenic activation of Pak1-dependent pathway of macropinocytosis determines BCG entry into bladder cancer cells. Cancer Res. 2013, 73:1156-1167.
39. Rosales-Reyes R., Perez-Lopez A., Sanchez-Gomez C., Hernandez-Mote R.R., Castro-Eguiluz D., Ortiz-Navarrete V., Alpuche-Aranda C.M. Salmonella infects B cells by macropinocytosis and formation of spacious phagosomes but does not induce pyroptosis in favor of its survival. Microb. Pathog. 2012, 52:367-374.
40. Sandor N., Kristof K., Parej K., Pap D., Erdei A., Bajtay Z. CR3 is the dominant phagocytotic complement receptor on human dendritic cells. Immunobiology 2013, 218:652-663.
41. Stuart L.M., Ezekowitz R.A. Phagocytosis: elegant complexity. Immunity 2005, 22:539-550.
42. Sundaramurthy V., Pieters J. Interactions of pathogenic mycobacteria with host macrophages. Microbes Infect. 2007, 9:1671-1679.
43. Swanson J.A. Shaping cups into phagosomes and macropinosomes. Nat. Rev. Mol. Cell Biol. 2008, 9:639-649.
44. Swanson J.A., Baer S.C. Phagocytosis by zippers and triggers. Trends Cell Biol. 1995, 5:89-93.
45. Underhill D.M., Ozinsky A. Phagocytosis of microbes: complexity in action. Annu. Rev. Immunol. 2002, 20:825-852.
46. van Lookeren Campagne M., Wiesmann C., Brown E.J. Macrophage complement receptors and pathogen clearance. Cell. Microbiol. 2007, 9:2095-2102.
47. Verjans G.M., Ringrose J.H., van Alphen L., Feltkamp T.E., Kusters J.G. Entrance and survival of Salmonella typhimurium and Yersinia enterocolitica within human B- and T-cell lines. Infect. Immunol. 1994, 62:2229-2235.
48. Vidard L., Kovacsovics-Bankowski M., Kraeft S.K., Chen L.B., Benacerraf B., Rock K.L. Analysis of MHC class II presentation of particulate antigens of B lymphocytes. J. Immunol. 1996, 156:2809-2818.
49. Yuste J., Sen A., Truedsson L., Jonsson G., Tay L.S., Hyams C., Baxendale H.E., Goldblatt F., Botto M., Brown J.S. Impaired opsonization with C3b and phagocytosis of Streptococcus pneumoniae in sera from subjects with defects in the classical complement pathway. Infect. Immunol. 2008, 76:3761-3770.
50. Zimmerman L.M., Vogel L.A., Edwards K.A., Bowden R.M. Phagocytic B cells in a reptile. Biol. Lett. 2010, 6:270-273.