#PAGE_PARAMS# #ADS_HEAD_SCRIPTS# #MICRODATA#

Tissue-specific expression of IgG receptors by human macrophages ex vivo


Autoři: Christine W. Bruggeman aff001;  Julia Houtzager aff002;  Barbara Dierdorp aff003;  Jesper Kers aff004;  Steven T. Pals aff004;  René Lutter aff003;  Thomas van Gulik aff002;  Joke M. M. den Haan aff006;  Timo K. van den Berg aff001;  Robin van Bruggen aff001;  Taco W. Kuijpers aff001
Působiště autorů: Department of Blood Cell Research, Sanquin Research and Landsteiner Laboratory, Academic Medical Center (AMC), University of Amsterdam, Amsterdam, The Netherlands aff001;  Department of Experimental Surgery, Academic Medical Center (AMC), University of Amsterdam, Amsterdam, The Netherlands aff002;  Department of Experimental Immunology, Academic Medical Center (AMC), University of Amsterdam, Amsterdam, The Netherlands aff003;  Department of Pathology, Academic Medical Center (AMC), University of Amsterdam, Amsterdam, The Netherlands aff004;  Van 't Hoff Institute for Molecular Sciences, University of Amsterdam, Amsterdam, The Netherlands aff005;  Department of Molecular Cell Biology and Immunology, VU University Medical Center, Amsterdam, The Netherlands aff006;  Emma Children's Hospital, Academic Medical Center (AMC), University of Amsterdam, Amsterdam, The Netherlands aff007
Vyšlo v časopise: PLoS ONE 14(10)
Kategorie: Research Article
doi: https://doi.org/10.1371/journal.pone.0223264

Souhrn

Recently it was discovered that tissue-resident macrophages derive from embryonic precursors, not only from peripheral blood monocytes, and maintain themselves by self-renewal. Most in-vitro studies on macrophage biology make use of in-vitro cultured human monocyte-derived macrophages. Phagocytosis of IgG-opsonized particles by tissue-resident macrophages takes place via interaction with IgG receptors, the Fc-gamma receptors (FcγRs). We investigated the FcγR expression on macrophages both in-vivo and ex-vivo from different human tissues. Upon isolation of primary human macrophages from bone marrow, spleen, liver and lung, we observed that macrophages from all studied tissues expressed high levels of FcγRIII, which was in direct contrast with the low expression on blood monocyte-derived macrophages. Expression levels of FcγRI were highly variable, with bone marrow macrophages showing the lowest and alveolar macrophages the highest expression. Kupffer cells in the liver were the only tissue-resident macrophages that expressed the inhibitory IgG receptor, FcγRIIB. This inhibitory receptor was also found to be expressed by sinusoidal endothelial cells in the liver. In sum, our immunofluorescence data combined with ex-vivo stainings of isolated macrophages indicated that tissue-resident macrophages are remarkably unique and different from monocyte-derived macrophages in their phenotypic expression of IgG receptors. Tissue macrophages show distinct tissue-specific FcγR expression patterns.

Klíčová slova:

Alveolar macrophages – Blood – Flow cytometry – Macrophages – Monocytes – Spleen – Kupffer cells


Zdroje

1. van Furth R., and Cohn Z. A. 1968. The origin and kinetics of mononuclear phagocytes. J Exp Med 128: 415–435. doi: 10.1084/jem.128.3.415 5666958

2. Bruggeman C. W., Dekkers G., Bentlage A. E. H., Treffers L. W., Nagelkerke S. Q., Lissenberg-Thunnissen S., Koeleman C. A. M., Wuhrer M., van den Berg T. K., Rispens T., Vidarsson G., and Kuijpers T. W. 2017. Enhanced Effector Functions Due to Antibody Defucosylation Depend on the Effector Cell Fcgamma Receptor Profile. J Immunol 199: 204–211. doi: 10.4049/jimmunol.1700116 28566370

3. Nagelkerke S. Q., Dekkers G., Kustiawan I., van de Bovenkamp F. S., Geissler J., Plomp R., Wuhrer M., Vidarsson G., Rispens T., van den Berg T. K., and Kuijpers T. W. 2014. Inhibition of FcgammaR-mediated phagocytosis by IVIg is independent of IgG-Fc sialylation and FcgammaRIIb in human macrophages. Blood 124: 3709–3718. doi: 10.1182/blood-2014-05-576835 25352126

4. Ginhoux F., and Jung S. 2014. Monocytes and macrophages: developmental pathways and tissue homeostasis. Nat Rev Immunol 14: 392–404. doi: 10.1038/nri3671 24854589

5. Gentek R., Molawi K., and Sieweke M. H. 2014. Tissue macrophage identity and self-renewal. Immunol Rev 262: 56–73. doi: 10.1111/imr.12224 25319327

6. Hashimoto D., Chow A., Noizat C., Teo P., Beasley M. B., Leboeuf M., Becker C. D., See P., Price J., Lucas D., Greter M., Mortha A., Boyer S. W., Forsberg E. C., Tanaka M., van Rooijen N., Garcia-Sastre A., Stanley E. R., Ginhoux F., Frenette P. S., and Merad M. 2013. Tissue-resident macrophages self-maintain locally throughout adult life with minimal contribution from circulating monocytes. Immunity 38: 792–804. doi: 10.1016/j.immuni.2013.04.004 23601688

7. Ginhoux F., Greter M., Leboeuf M., Nandi S., See P., Gokhan S., Mehler M. F., Conway S. J., Ng L. G., Stanley E. R., Samokhvalov I. M., and Merad M. 2010. Fate mapping analysis reveals that adult microglia derive from primitive macrophages. Science 330: 841–845. doi: 10.1126/science.1194637 20966214

8. Schulz C., Gomez Perdiguero E., Chorro L., Szabo-Rogers H., Cagnard N., Kierdorf K., Prinz M., Wu B., Jacobsen S. E., Pollard J. W., Frampton J., Liu K. J., and Geissmann F. 2012. A lineage of myeloid cells independent of Myb and hematopoietic stem cells. Science 336: 86–90. doi: 10.1126/science.1219179 22442384

9. Gordon S., and Martinez-Pomares L. 2017. Physiological roles of macrophages. Pflugers Archiv: European journal of physiology 469: 365–374. doi: 10.1007/s00424-017-1945-7 28185068

10. Epelman S., Lavine K. J., and Randolph G. J. 2014. Origin and functions of tissue macrophages. Immunity 41: 21–35. doi: 10.1016/j.immuni.2014.06.013 25035951

11. Gordon S., and Taylor P. R. 2005. Monocyte and macrophage heterogeneity. Nat Rev Immunol 5: 953–964. doi: 10.1038/nri1733 16322748

12. Smythies L. E., Sellers M., Clements R. H., Mosteller-Barnum M., Meng G., Benjamin W. H., Orenstein J. M., and Smith P. D. 2005. Human intestinal macrophages display profound inflammatory anergy despite avid phagocytic and bacteriocidal activity. J Clin Invest 115: 66–75. doi: 10.1172/JCI19229 15630445

13. Gonzalez-Dominguez E., Samaniego R., Flores-Sevilla J. L., Campos-Campos S. F., Gomez-Campos G., Salas A., Campos-Pena V., Corbi A. L., Sanchez-Mateos P., and Sanchez-Torres C. 2015. CD163L1 and CLEC5A discriminate subsets of human resident and inflammatory macrophages in vivo. J Leukoc Biol 98: 453–466. doi: 10.1189/jlb.3HI1114-531R 25877931

14. Bruhns P., Iannascoli B., England P., Mancardi D. A., Fernandez N., Jorieux S., and Daeron M. 2009. Specificity and affinity of human Fcgamma receptors and their polymorphic variants for human IgG subclasses. Blood 113: 3716–3725. doi: 10.1182/blood-2008-09-179754 19018092

15. Davies L. C., Jenkins S. J., Allen J. E., and Taylor P. R. 2013. Tissue-resident macrophages. Nat Immunol 14: 986–995. doi: 10.1038/ni.2705 24048120

16. Varol C., Mildner A., and Jung S. 2015. Macrophages: development and tissue specialization. Annu Rev Immunol 33: 643–675. doi: 10.1146/annurev-immunol-032414-112220 25861979

17. Nagelkerke S. Q., aan de Kerk D. J., Jansen M. H., van den Berg T. K., and Kuijpers T. W. 2014. Failure to detect functional neutrophil B helper cells in the human spleen. PLoS One 9: e88377. doi: 10.1371/journal.pone.0088377 24523887

18. Nagelkerke S. Q., Bruggeman C. W., den Haan J. M. M., Mul E. P. J., van den Berg T. K., van Bruggen R., and Kuijpers T. W. 2018. Red pulp macrophages in the human spleen are a distinct cell population with a unique expression of Fc-gamma receptors. Blood advances 2: 941–953. doi: 10.1182/bloodadvances.2017015008 29692344

19. Werner M., Driftmann S., Kleinehr K., Kaiser G. M., Mathe Z., Treckmann J. W., Paul A., Skibbe K., Timm J., Canbay A., Gerken G., Schlaak J. F., and Broering R. 2015. All-In-One: Advanced preparation of Human Parenchymal and Non-Parenchymal Liver Cells. PLoS One 10: e0138655. doi: 10.1371/journal.pone.0138655 26407160

20. Breunis W. B., van Mirre E., Geissler J., Laddach N., Wolbink G., van der Schoot E., de Haas M., de Boer M., Roos D., and Kuijpers T. W. 2009. Copy number variation at the FCGR locus includes FCGR3A, FCGR2C and FCGR3B but not FCGR2A and FCGR2B. Hum Mutat 30: E640–650. doi: 10.1002/humu.20997 19309690

21. Tsang A. S. M. W., Nagelkerke S. Q., Bultink I. E., Geissler J., Tanck M. W., Tacke C. E., Ellis J. A., Zenz W., Bijl M., Berden J. H., de Leeuw K., Derksen R. H., Kuijpers T. W., and Voskuyl A. E. 2016. Fc-gamma receptor polymorphisms differentially influence susceptibility to systemic lupus erythematosus and lupus nephritis. Rheumatology (Oxford) 55: 939–948.

22. van der Heijden J., Breunis W. B., Geissler J., de Boer M., van den Berg T. K., and Kuijpers T. W. 2012. Phenotypic variation in IgG receptors by nonclassical FCGR2C alleles. J Immunol 188: 1318–1324. doi: 10.4049/jimmunol.1003945 22198951

23. Passlick B., Flieger D., and Ziegler-Heitbrock H. W. 1989. Identification and characterization of a novel monocyte subpopulation in human peripheral blood. Blood 74: 2527–2534. 2478233

24. Ziegler-Heitbrock H. W., Fingerle G., Strobel M., Schraut W., Stelter F., Schutt C., Passlick B., and Pforte A. 1993. The novel subset of CD14+/CD16+ blood monocytes exhibits features of tissue macrophages. Eur J Immunol 23: 2053–2058. doi: 10.1002/eji.1830230902 7690321

25. Ginhoux F., Schultze J. L., Murray P. J., Ochando J., and Biswas S. K. 2016. New insights into the multidimensional concept of macrophage ontogeny, activation and function. Nat Immunol 17: 34–40. doi: 10.1038/ni.3324 26681460

26. Zhang H., Ling X. L., Wu Y. Y., Lu M. H., Guo H., Zhang P. B., Zhao X. Y., and Yang S. M. 2014. CD64 expression is increased in patients with severe acute pancreatitis: clinical significance. Gut Liver 8: 445–451. doi: 10.5009/gnl.2014.8.4.445 25071912

27. Gericke G. H., Ericson S. G., Pan L., Mills L. E., Guyre P. M., and Ely P. 1995. Mature polymorphonuclear leukocytes express high-affinity receptors for IgG (Fc gamma RI) after stimulation with granulocyte colony-stimulating factor (G-CSF). J Leukoc Biol 57: 455–461. doi: 10.1002/jlb.57.3.455 7533820

28. Matt P., Lindqvist U., and Kleinau S. 2015. Up-regulation of CD64-expressing monocytes with impaired FcgammaR function reflects disease activity in polyarticular psoriatic arthritis. Scand J Rheumatol 44: 464–473. doi: 10.3109/03009742.2015.1020864 26084203

29. van der Poel C. E., Spaapen R. M., van de Winkel J. G., and Leusen J. H. 2011. Functional characteristics of the high affinity IgG receptor, FcgammaRI. J Immunol 186: 2699–2704. doi: 10.4049/jimmunol.1003526 21325219

30. Peebles R. S. Jr., Liu M. C., Lichtenstein L. M., and Hamilton R. G. 1995. IgA, IgG and IgM quantification in bronchoalveolar lavage fluids from allergic rhinitics, allergic asthmatics, and normal subjects by monoclonal antibody-based immunoenzymetric assays. Journal of immunological methods 179: 77–86. doi: 10.1016/0022-1759(94)00275-2 7868927

31. Van Vyve T., Chanez P., Bernard A., Bousquet J., Godard P., Lauwerijs R., and Sibille Y. 1995. Protein content in bronchoalveolar lavage fluid of patients with asthma and control subjects. The Journal of allergy and clinical immunology 95: 60–68. doi: 10.1016/s0091-6749(95)70153-2 7822665

32. Gillis C. M., Zenatti P. P., Mancardi D. A., Beutier H., Fiette L., Macdonald L. E., Murphy A. J., Celli S., Bousso P., Jonsson F., and Bruhns P. 2017. In vivo effector functions of high-affinity mouse IgG receptor FcgammaRI in disease and therapy models. Journal of autoimmunity 80: 95–102. doi: 10.1016/j.jaut.2016.09.009 27745779

33. Mancardi D. A., Albanesi M., Jonsson F., Iannascoli B., Van Rooijen N., Kang X., England P., Daeron M., and Bruhns P. 2013. The high-affinity human IgG receptor FcgammaRI (CD64) promotes IgG-mediated inflammation, anaphylaxis, and antitumor immunotherapy. Blood 121: 1563–1573. doi: 10.1182/blood-2012-07-442541 23293080

34. van der Poel C. E., Karssemeijer R. A., Boross P., van der Linden J. A., Blokland M., van de Winkel J. G., and Leusen J. H. 2010. Cytokine-induced immune complex binding to the high-affinity IgG receptor, FcgammaRI, in the presence of monomeric IgG. Blood 116: 5327–5333. doi: 10.1182/blood-2010-04-280214 20805361

35. Ganesan L. P., Kim J., Wu Y., Mohanty S., Phillips G. S., Birmingham D. J., Robinson J. M., and Anderson C. L. 2012. FcgammaRIIb on liver sinusoidal endothelium clears small immune complexes. J Immunol 189: 4981–4988. doi: 10.4049/jimmunol.1202017 23053513

36. March S., Hui E. E., Underhill G. H., Khetani S., and Bhatia S. N. 2009. Microenvironmental regulation of the sinusoidal endothelial cell phenotype in vitro. Hepatology 50: 920–928. doi: 10.1002/hep.23085 19585615

37. Mousavi S. A., Sporstol M., Fladeby C., Kjeken R., Barois N., and Berg T. 2007. Receptor-mediated endocytosis of immune complexes in rat liver sinusoidal endothelial cells is mediated by FcgammaRIIb2. Hepatology 46: 871–884. doi: 10.1002/hep.21748 17680646

38. Ganesan L. P., Mohanty S., Kim J., Clark K. R., Robinson J. M., and Anderson C. L. 2011. Rapid and efficient clearance of blood-borne virus by liver sinusoidal endothelium. PLoS pathogens 7: e1002281. doi: 10.1371/journal.ppat.1002281 21980295

39. Mates J. M., Yao Z., Cheplowitz A. M., Suer O., Phillips G. S., Kwiek J. J., Rajaram M. V., Kim J., Robinson J. M., Ganesan L. P., and Anderson C. L. 2017. Mouse Liver Sinusoidal Endothelium Eliminates HIV-Like Particles from Blood at a Rate of 100 Million per Minute by a Second-Order Kinetic Process. Frontiers in immunology 8: 35. doi: 10.3389/fimmu.2017.00035 28167948

40. Laskin D. L., Weinberger B., and Laskin J. D. 2001. Functional heterogeneity in liver and lung macrophages. J Leukoc Biol 70: 163–170. 11493607

41. Krenkel O., and Tacke F. 2017. Liver macrophages in tissue homeostasis and disease. Nat Rev Immunol 17: 306–321. doi: 10.1038/nri.2017.11 28317925

42. Beutier H., Hechler B., Godon O., Wang Y., Gillis C. M., de Chaisemartin L., Gouel-Cheron A., Magnenat S., Macdonald L. E., Murphy A. J., Chollet-Martin S., Longrois D., Gachet C., Bruhns P., and Jonsson F. 2018. Platelets expressing IgG receptor FcgammaRIIA/CD32A determine the severity of experimental anaphylaxis. Science immunology 3.

43. Gillis C. M., Jonsson F., Mancardi D. A., Tu N., Beutier H., Van Rooijen N., Macdonald L. E., Murphy A. J., and Bruhns P. 2017. Mechanisms of anaphylaxis in human low-affinity IgG receptor locus knock-in mice. The Journal of allergy and clinical immunology 139: 1253–1265.e1214. doi: 10.1016/j.jaci.2016.06.058 27568081

44. Arce Vargas F., Furness A. J. S., Litchfield K., Joshi K., Rosenthal R., Ghorani E., Solomon I., Lesko M. H., Ruef N., Roddie C., Henry J. Y., Spain L., Ben Aissa A., Georgiou A., Wong Y. N. S., Smith M., Strauss D., Hayes A., Nicol D., O'Brien T., Martensson L., Ljungars A., Teige I., Frendeus B., Pule M., Marafioti T., Gore M., Larkin J., Turajlic S., Swanton C., Peggs K. S., and Quezada S. A. 2018. Fc Effector Function Contributes to the Activity of Human Anti-CTLA-4 Antibodies. Cancer cell 33: 649–663.e644. doi: 10.1016/j.ccell.2018.02.010 29576375

45. Gautier E. L., and Yvan-Charvet L. 2014. Understanding macrophage diversity at the ontogenic and transcriptomic levels. Immunol Rev 262: 85–95. doi: 10.1111/imr.12231 25319329

46. Lavin Y., Winter D., Blecher-Gonen R., David E., Keren-Shaul H., Merad M., Jung S., and Amit I. 2014. Tissue-resident macrophage enhancer landscapes are shaped by the local microenvironment. Cell 159: 1312–1326. doi: 10.1016/j.cell.2014.11.018 25480296


Článek vyšel v časopise

PLOS One


2019 Číslo 10
Nejčtenější tento týden
Nejčtenější v tomto čísle
Kurzy

Zvyšte si kvalifikaci online z pohodlí domova

KOST
Koncepce osteologické péče pro gynekology a praktické lékaře
nový kurz
Autoři: MUDr. František Šenk

Sekvenční léčba schizofrenie
Autoři: MUDr. Jana Hořínková

Hypertenze a hypercholesterolémie – synergický efekt léčby
Autoři: prof. MUDr. Hana Rosolová, DrSc.

Svět praktické medicíny 5/2023 (znalostní test z časopisu)

Imunopatologie? … a co my s tím???
Autoři: doc. MUDr. Helena Lahoda Brodská, Ph.D.

Všechny kurzy
Kurzy Podcasty Doporučená témata Časopisy
Přihlášení
Zapomenuté heslo

Zadejte e-mailovou adresu, se kterou jste vytvářel(a) účet, budou Vám na ni zaslány informace k nastavení nového hesla.

Přihlášení

Nemáte účet?  Registrujte se

#ADS_BOTTOM_SCRIPTS#