Platelets direct monocyte differentiation into epithelioid-like multinucleated giant foam cells with suppressive capacity upon mycobacterial stimulation

Journal of Infectious Diseases

Volumn 210, Issue 11, 2014, Pages 1700-1710

  Feng, Yonghong ^a,b   Dorhoi, Anca ^a   Mollenkopf, Hans Joachim ^a   Yin, Hongyun ^b   Dong, Zhengwei ^b   Mao, Ling ^b   Zhou, Jun ^b   Bi, Aixiao ^b   Weber, Stephan ^a   Maertzdorf, Jeroen ^a   Chen, Gang ^b   Chen, Yang ^c   Kaufmann, Stefan H E ^a  

^a MAX PLANCK INSTITUTE FOR INFECTION BIOLOGY   (Germany)

^b TONGJI UNIVERSITY   (China)

^c TSINGHUA UNIVERSITY   (China)

Author keywords

CXCL5; Macrophage; Multinucleated giant cell; Platelet; Tuberculosis

Indexed keywords

EPITHELIAL DERIVED NEUTROPHIL ACTIVATING FACTOR 78; GLYCOPROTEIN IB ALPHA; INTERLEUKIN 10; TRANSCRIPTOME; BIOLOGICAL MARKER; LIPOPOLYSACCHARIDE;

ADULT; ARTICLE; CELL DIFFERENTIATION; CLINICAL ARTICLE; COCULTURE; CONTROLLED STUDY; CYTOKINE RELEASE; EPITHELIOID CELL; FEMALE; FLOW CYTOMETRY; FOAM CELL; GENETIC TRANSCRIPTION; GIANT CELL; GRANULOMA; HUMAN; HUMAN CELL; IMMUNOASSAY; IMMUNOHISTOCHEMISTRY; MACROPHAGE; MALE; MICROARRAY ANALYSIS; MICROSCOPY; MONOCYTE; MYCOBACTERIUM BOVIS; MYCOBACTERIUM TUBERCULOSIS; PHAGOCYTOSIS; PRIORITY JOURNAL; THROMBOCYTE; THROMBOCYTE AGGREGATION; TUBERCULOSIS; BIOSYNTHESIS; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENE REGULATORY NETWORK; GENETICS; IMMUNOLOGY; IMMUNOMODULATION; METABOLISM; MICROBIOLOGY; MIDDLE AGED; MYCOBACTERIUM; PATHOLOGY; THROMBOCYTE ACTIVATION;

ADULT; BIOLOGICAL MARKERS; BLOOD PLATELETS; COCULTURE TECHNIQUES; FEMALE; FOAM CELLS; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENE REGULATORY NETWORKS; GRANULOMA; HUMANS; IMMUNOMODULATION; INTERLEUKIN-10; LIPOPOLYSACCHARIDES; MALE; MIDDLE AGED; MONOCYTES; MYCOBACTERIUM; PHAGOCYTOSIS; PLATELET ACTIVATION; TUBERCULOSIS;

EID: 84922294254     PISSN: 00221899     EISSN: 15376613     Source Type: Journal    
DOI: 10.1093/infdis/jiu355     Document Type: Article

References (50)

1. Burger PC, Wagner DD. Platelet P-selection facilitates atherosclerotic lesion development. Blood 2003; 101:2661-6.
2. Gay LJ, Felding-Habermann B. Contribution of platelets to tumour metastasis. Nat Rev Cancer 2011; 11:123-34.
3. Boilard E, Nigrovic PA, Larabee K, et al. Platelets amplify inflammation in arthritis via collagen-dependent microparticle production. Science 2010; 327:580-3.
4. Semple JW, Italiano JE Jr, Freedman J. Platelets and the immune continuum. Nat Rev Immunol 2011; 11:264-74.
5. Yeaman MR. Platelets in defense against bacterial pathogens. Cell Mol Life Sci 2010; 67:525-44.
6. Clark SR, Ma AC, Tavener SA, et al. Platelet TLR4 activates neutrophil extracellular traps to ensnare bacteria in septic blood. Nat Med 2007; 13:463-9.
7. Kornerup KN, Salmon GP, Pitchford SC, Liu WL, Page CP. Circulating platelet-neutrophil complexes are important for subsequent neutrophil activation and migration. J Appl Physiol 2010; 109:758-67.
8. Li Z, Yang F, Dunn S, Gross KA, Smyth SS. Platelets as immune mediators: their role in host defense responses and sepsis. Thromb Res 2011; 127:184-8.
9. Daub K, Langer H, Seizer P, et al. Platelets induce differentiation of human CD34+ progenitor cells into foam cells and endothelial cells. FASEB J 2006; 20:2559-61.
10. Ishihara T, Akizuki S, Yokota T, et al. Foamy cells associated with platelet phagocytosis. Am J Pathol 1984; 114:104-11.
11. De Meyer GR, De Cleen DM, Cooper S, et al. Platelet phagocytosis and processing of beta-amyloid precursor protein as a mechanism of macrophage activation in atherosclerosis. Circ Res 2002; 90:1197-204.
12. Churchill GA. Fundamentals of experimental design for cDNA micro-arrays. Nat Genet 2002; 32(suppl): 490-5.
13. Eden E, Navon R, Steinfeld I, Lipson D, Yakhini Z. GOrilla: a tool for discovery and visualization of enriched GO terms in ranked gene lists. BMC Bioinformatics 2009; 10:48.
14. Huang da W, Sherman BT, Lempicki RA. Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources. Nat Protocol 2009; 4:44-57.
15. Puissegur MP, Lay G, Gilleron M, et al. Mycobacterial lipomannan induces granuloma macrophage fusion via a TLR2-dependent, ADAM9- and beta1 integrin-mediated pathway. J Immunol 2007; 178: 3161-9.
16. Helming L, Gordon S. Molecular mediators of macrophage fusion. Trends Cell Biol 2009; 19:514-22.
17. Martinez FO, Sica A, Mantovani A, Locati M. Macrophage activation and polarization. Front Biosci 2008; 13:453-61.
18. McRedmond JP, Park SD, Reilly DF, et al. Integration of proteomics and genomics in platelets: a profile of platelet proteins and platelet-specific genes. Mol Cell Proteomics 2004; 3:133-44.
19. Feng Y, Yin H, Mai G, et al. Elevated serum levels of CCL17 correlate with increased peripheral blood platelet count in patients with active tuberculosis in China. Clin Vaccine Immunol 2011; 18:629-32.
20. Tarhan G, Gümüşlü F, Yilmaz N, et al. Serum adenosine deaminase enzyme and plasma platelet factor 4 activities in active pulmonary tuberculosis, HIV-seropositive subjects and cancer patients. J Infect 2006; 52:264-8.
21. Tabuchi A, Kuebler WM. Endothelium-platelet interactions in inflammatory lung disease. Vasc Pharmacol 2008; 49:141-50.
22. Torrado E, Adusumilli S, Fraga AG, et al. Mycolactone-mediated inhibition of tumor necrosis factor production by macrophages infected with Mycobacterium ulcerans has implications for the control of infection. Infect Immun 2007; 75:3979-88.
23. Cognasse F, Hamzeh-Cognasse H, Lafarge S, et al. Donor platelets stored for at least 3 days can elicit activation marker expression by the recipient's blood mononuclear cells: an in vitro study. Transfusion 2009; 49: 91-8.
24. Ammon C, Kreutz M, Rehli M, Krause SW, Andreesen R. Platelets induce monocyte differentiation in serum-free coculture. J Leuko Biol 1998; 63:469-76.
25. Stephen J, Emerson B, Fox KA, Dransfield I. The uncoupling of mono-cyte-platelet interactions from the induction of proinflammatory signaling in monocytes. J Immunol 2013; 191:5677-83.
26. Passacquale G, Vamadevan P, Pereira L, et al. Monocyte-platelet interaction induces a pro-inflammatory phenotype in circulating monocytes. PLoS One 2011; 6:e25595.
27. Gudbrandsdottir S, Hasselbalch HC, Nielsen CH. Activated platelets enhance IL-10 secretion and reduce TNF-α secretion by monocytes. J Immunol 2013; 191:4059-67.
28. Peterson HJ, Smith AM. The role of the innate immune system in granulomatous disorders. Front Immunol 2013; 4:120.
29. Philips JA, Rubin EJ, Perrimon N. Drosophila RNAi screen reveals CD36 family member required for mycobacterial infection. Science 2005; 309:1251-3.
30. Lay G, Poquet Y, Salek-Peyron P, et al. Langhans giant cells from M. tuberculosis-induced human granulomas cannot mediate mycobacterial uptake. J Pathol 2007; 211:76-85.
31. Astarita JL, Acton SE, Turley SJ. Podoplanin: emerging functions in development, the immune system, and cancer. Front Immunol 2012; 3:283.
32. Mei J, Liu Y, Dai N, et al. Cxcr2 and Cxcl5 regulate the IL-17/G-CSF axis and neutrophil homeostasis in mice. J. Clin Invest 2012; 122: 974-86.
33. Wiedermann FJ, Mayr AJ, Kaneider NC, et al. Alveolar granulocyte colony-stimulating factor and alpha-chemokines in relation to serum levels, pulmonary neutrophilia, and severity of lung injury in ARDS. Chest 2004; 125:212-9.
34. Chen L, Yang Z, Lu B, et al. Serum CXC ligand 5 is a new marker of subclinical atherosclerosis in type 2 diabetes. Clin Endocrinol (Oxf) 2011; 75:766-70.
35. Saintigny P, Massarelli E, Lin S, et al. CXCR2 expression in tumor cells is a poor prognostic factor and promotes invasion and metastasis in lung adenocarcinoma. Cancer Res 2013; 73:571-82.
36. Schenk BI, Petersen F, Flad HD, Brandt E. Platelet-derived chemokines CXC chemokine ligand (CXCL)7, connective tissue-activating peptide III, and CXCL4 differentially affect and cross-regulate neutrophil adhesion and transendothelial migration. J Immunol 2002; 169:2602-10.
37. Power CA, Furness RB, Brawand C, Wells TN. Cloning of a full-length cDNA encoding the neutrophil-activating peptide ENA-78 from human platelets. Gene 1994; 151:333-4.
38. Nouailles G, Dorhoi A, Koch M, et al. CXCL5-secreting pulmonary epithelial cells drive destructive neutrophilic inflammation in tuberculosis. J Clin Invest 2014; 124:1268-82.
39. Lowe DM, Redford PS, Wilkinson RJ, O'Garra A, Martineau AR. Neutrophils in tuberculosis: friend or foe? Trends Immunol 2012; 33:14-25.
40. Russel DG. Who puts the tubercle in tuberculosis? Nat Rev Microbiol 2007; 5:39-47.
41. Siegel-Axel D, Daub K, Seizer P, Lindemann S, Gawaz M. Platelet lipoprotein interplay: trigger of foam cell formation and driver of atherosclerosis. Cardiovasc Res 2008; 78:8-17.
42. Greenlee-Wacker MC, Galvan MD, Bohlson SS. CD93: recent advances and implications in disease. Curr Drug Targets 2012; 13:411-20.
43. Sierro F, Biben C, Martínez-Muñoz L, et al. Disrupted cardiac development but normal hematopoisis in mice deficient in the second CXCL12/ SDF-1 receptor, CXCR7. Proc Natl Acad Sci U S A 2007; 104:14759-64.
44. Checa M, Ruiz V, Montaño M, et al. MMP-1 polymorphisms and the risk of idiopathic pulmonary fibrosis. Hum Genet 2008; 124:465-72.
45. Scambler PJ, Wainwright BJ, Farrall M, et al. Linkage of COL1A2 collagen gene to cystic fibrosis, and its clinical implications. Lancet 1985; 2:1241-2.
46. Peyron P, Vaubourgeix J, Poquet Y, et al. Foamy macrophages from tuberculous patients' granulomas constitute nutrient-rich reservoir for M. tuberculosis persistence. PLoS Pathog 2008; 4:e1000204.
47. Chandler AB, Hand RA. Phagocytized platelets: a source of lipids in human thrombi and atherosclerotic plaques. Science 1961; 134:946-7.
48. Denis MM, Tolley ND, Bunting M, et al. Escaping the nuclear confines: signal-dependent pre-mRNA splicing in anucleate platelets. Cell 2005; 122:379-91.
49. Edelstein LC, Bray PF. MicroRNAs in platelet production and activation. Blood 2011; 117:5289-96.
50. Elkington P, Shiomi T, Breen R, et al. MMP-1 drives immunopathology in human tuberculosis and transgenic mice. J Clin Invest 2011; 121: 1827-33.