Published 19 August 2002. doi:10.1084/jem.20011608
© Rockefeller University Press, 0022-1007/2002/8/517/ $5.00
The Journal of Experimental Medicine, Volume 196, Number 4, August 19, 2002 517-527
The CD16+ (Fc
RIII+) Subset of Human Monocytes Preferentially Becomes Migratory Dendritic Cells in a Model Tissue Setting
Gwendalyn J. Randolph1,
Guzman Sanchez-Schmitz1,
Ronald M. Liebman1 and
Knut Schäkel2
1 The Carl C. Icahn Institute for Gene Therapy and Molecular Medicine, Mt. Sinai School of Medicine, New York, NY 10029
2 Institute of Immunology, Department of Dermatology, Medical Faculty, Technical University of Dresden, D-01307 Dresden, Germany
Address correspondence to Gwendalyn J. Randolph, Institute for Gene Therapy and Molecular Medicine, Mt. Sinai School of Medicine, 1425 Madison Ave., Box 1496, New York, NY 10029. Phone: 212-659-8262; Fax: 212-803-6740; E-mail: gwendalyn.randolph{at}mssm.edu
Much remains to be learned about the physiologic events that promote monocytes to become lymph-homing dendritic cells (DCs). In a model of transendothelial trafficking, some monocytes become DCs in response to endogenous signals. These DCs migrate across endothelium in the ablumenal-to-lumenal direction (reverse transmigration), reminiscent of the migration into lymphatic vessels. Here we show that the subpopulation of monocytes that expresses CD16 (Fc
receptor III) is predisposed to become migratory DCs. The vast majority of cells derived from CD16+ monocytes reverse transmigrated, and their presence was associated with migratory cells expressing high levels of CD86 and human histocompatibility leukocyte antigen (HLA)-DR, and robust capacity to induce allogeneic T cell proliferation. A minority of CD16- monocytes reverse transmigrated, and these cells stimulated T cell proliferation less efficiently. CD16 was not functionally required for reverse transmigration, but promoted cell survival when yeast particles (zymosan) were present as a maturation stimulus in the subendothelial matrix. The cell surface phenotype and migratory characteristics of CD16+ monocytes were inducible in CD16- monocytes by preincubation with TGFß1. We propose that CD16+ monocytes may contribute significantly to precursors for DCs that transiently survey tissues and migrate to lymph nodes via afferent lymphatic vessels.
Key Words: antigen presentation cell survival transforming growth factors IgG receptors cell differentiation

CiteULike
Complore
Connotea
Del.icio.us
Digg
Reddit
Technorati What's this?
This article has been cited by other articles:
-
Buonaguro, L., Tornesello, M. L., Gallo, R. C., Marincola, F. M., Lewis, G. K., Buonaguro, F. M.
(2009). Th2 Polarization in Peripheral Blood Mononuclear Cells from Human Immunodeficiency Virus (HIV)-Infected Subjects, as Activated by HIV Virus-Like Particles. J. Virol.
83: 304-313
[Abstract]
[Full Text]
-
Chen, G.-Y., Sakuma, K., Kannagi, R.
(2008). Significance of NF-{kappa}B/GATA Axis in Tumor Necrosis Factor-{alpha}-induced Expression of 6-Sulfated Cell Recognition Glycans in Human T-lymphocytes. J. Biol. Chem.
283: 34563-34570
[Abstract]
[Full Text]
-
Timmerman, K. L., Flynn, M. G., Coen, P. M., Markofski, M. M., Pence, B. D.
(2008). Exercise training-induced lowering of inflammatory (CD14+CD16+) monocytes: a role in the anti-inflammatory influence of exercise?. J. Leukoc. Biol.
84: 1271-1278
[Abstract]
[Full Text]
-
Schaumann, F., Muller, M., Braun, A., Luettig, B., Peden, D. B., Hohlfeld, J. M., Krug, N.
(2008). Endotoxin Augments Myeloid Dendritic Cell Influx into the Airways in Patients with Allergic Asthma. Am. J. Respir. Crit. Care Med.
177: 1307-1313
[Abstract]
[Full Text]
-
Ifergan, I., Kebir, H., Bernard, M., Wosik, K., Dodelet-Devillers, A., Cayrol, R., Arbour, N., Prat, A.
(2008). The blood-brain barrier induces differentiation of migrating monocytes into Th17-polarizing dendritic cells. Brain
131: 785-799
[Abstract]
[Full Text]
-
Glick, A. B., Perez-Lorenzo, R., Mohammed, J.
(2008). Context-dependent regulation of cutaneous immunological responses by TGF{beta}1 and its role in skin carcinogenesis. Carcinogenesis
29: 9-14
[Abstract]
[Full Text]
-
Bradfield, P. F., Scheiermann, C., Nourshargh, S., Ody, C., Luscinskas, F. W., Rainger, G. E., Nash, G. B., Miljkovic-Licina, M., Aurrand-Lions, M., Imhof, B. A.
(2007). JAM-C regulates unidirectional monocyte transendothelial migration in inflammation. Blood
110: 2545-2555
[Abstract]
[Full Text]
-
Strauss-Ayali, D., Conrad, S. M., Mosser, D. M.
(2007). Monocyte subpopulations and their differentiation patterns during infection. J. Leukoc. Biol.
82: 244-252
[Abstract]
[Full Text]
-
Segain, J.-P., Rolli-Derkinderen, M., Gervois, N., Raingeard de la Bletiere, D., Loirand, G., Pacaud, P.
(2007). Urotensin II is a New Chemotactic Factor for UT Receptor-Expressing Monocytes. J. Immunol.
179: 901-909
[Abstract]
[Full Text]
-
Kwan, W.-H., Boix, C., Gougelet, N., Fridman, W. H., Mueller, C. G. F.
(2007). LPS induces rapid IL-10 release by M-CSF-conditioned tolerogenic dendritic cell precursors. J. Leukoc. Biol.
82: 133-141
[Abstract]
[Full Text]
-
Burdo, T. H., Wood, M. R., Fox, H. S.
(2007). Osteopontin prevents monocyte recirculation and apoptosis. J. Leukoc. Biol.
81: 1504-1511
[Abstract]
[Full Text]
-
Ellery, P. J., Tippett, E., Chiu, Y.-L., Paukovics, G., Cameron, P. U., Solomon, A., Lewin, S. R., Gorry, P. R., Jaworowski, A., Greene, W. C., Sonza, S., Crowe, S. M.
(2007). The CD16+ Monocyte Subset Is More Permissive to Infection and Preferentially Harbors HIV-1 In Vivo. J. Immunol.
178: 6581-6589
[Abstract]
[Full Text]
-
Rydstrom, A., Wick, M. J.
(2007). Monocyte Recruitment, Activation, and Function in the Gut-Associated Lymphoid Tissue during Oral Salmonella Infection. J. Immunol.
178: 5789-5801
[Abstract]
[Full Text]
-
Ziegler-Heitbrock, L.
(2007). The CD14+ CD16+ blood monocytes: their role in infection and inflammation. J. Leukoc. Biol.
81: 584-592
[Abstract]
[Full Text]
-
Matmati, M., Pouwels, W., van Bruggen, R., Jansen, M., Hoek, R. M., Verhoeven, A. J., Hamann, J.
(2007). The human EGF-TM7 receptor EMR3 is a marker for mature granulocytes. J. Leukoc. Biol.
81: 440-448
[Abstract]
[Full Text]
-
Ancuta, P., Wang, J., Gabuzda, D.
(2006). CD16+ monocytes produce IL-6, CCL2, and matrix metalloproteinase-9 upon interaction with CX3CL1-expressing endothelial cells.. J. Leukoc. Biol.
80: 1156-1164
[Abstract]
[Full Text]
-
Cassol, E., Alfano, M., Biswas, P., Poli, G.
(2006). Monocyte-derived macrophages and myeloid cell lines as targets of HIV-1 replication and persistence. J. Leukoc. Biol.
80: 1018-1030
[Abstract]
[Full Text]
-
Kumar, S., Jack, R.
(2006). Invited review: Origin of monocytes and their differentiation to macrophages and dendritic cells. Innate Immunity
12: 278-284
[Abstract]
-
de Gruijl, T. D., Sombroek, C. C., Lougheed, S. M., Oosterhoff, D., Buter, J., van den Eertwegh, A. J. M., Scheper, R. J., Pinedo, H. M.
(2006). A Postmigrational Switch among Skin-Derived Dendritic Cells to a Macrophage-Like Phenotype Is Predetermined by the Intracutaneous Cytokine Balance.. J. Immunol.
176: 7232-7242
[Abstract]
[Full Text]
-
Ancuta, P., Autissier, P., Wurcel, A., Zaman, T., Stone, D., Gabuzda, D.
(2006). CD16+ Monocyte-Derived Macrophages Activate Resting T Cells for HIV Infection by Producing CCR3 and CCR4 Ligands. J. Immunol.
176: 5760-5771
[Abstract]
[Full Text]
-
Di Pucchio, T., Pilla, L., Capone, I., Ferrantini, M., Montefiore, E., Urbani, F., Patuzzo, R., Pennacchioli, E., Santinami, M., Cova, A., Sovena, G., Arienti, F., Lombardo, C., Lombardi, A., Caporaso, P., D'Atri, S., Marchetti, P., Bonmassar, E., Parmiani, G., Belardelli, F., Rivoltini, L.
(2006). Immunization of Stage IV Melanoma Patients with Melan-A/MART-1 and gp100 Peptides plus IFN-{alpha} Results in the Activation of Specific CD8+ T Cells and Monocyte/Dendritic Cell Precursors.. Cancer Res.
66: 4943-4951
[Abstract]
[Full Text]
-
Yrlid, U., Jenkins, C. D., MacPherson, G. G.
(2006). Relationships between Distinct Blood Monocyte Subsets and Migrating Intestinal Lymph Dendritic Cells In Vivo under Steady-State Conditions. J. Immunol.
176: 4155-4162
[Abstract]
[Full Text]
-
Tacke, F., Ginhoux, F., Jakubzick, C., van Rooijen, N., Merad, M., Randolph, G. J.
(2006). Immature monocytes acquire antigens from other cells in the bone marrow and present them to T cells after maturing in the periphery. JEM
203: 583-597
[Abstract]
[Full Text]
-
Slukvin, I. I., Vodyanik, M. A., Thomson, J. A., Gumenyuk, M. E., Choi, K.-D.
(2006). Directed Differentiation of Human Embryonic Stem Cells into Functional Dendritic Cells through the Myeloid Pathway.. J. Immunol.
176: 2924-2932
[Abstract]
[Full Text]
-
Webster, N. L., Kedzierska, K., Azzam, R., Paukovics, G., Wilson, J., Crowe, S. M., Jaworowski, A.
(2006). Phagocytosis stimulates mobilization and shedding of intracellular CD16A in human monocytes and macrophages: inhibition by HIV-1 infection. J. Leukoc. Biol.
79: 294-302
[Abstract]
[Full Text]
-
Soares, G., Barral, A., Costa, J. M., Barral-Netto, M., Van Weyenbergh, J.
(2006). CD16+ monocytes in human cutaneous leishmaniasis: increased ex vivo levels and correlation with clinical data. J. Leukoc. Biol.
79: 36-39
[Abstract]
[Full Text]
-
Rossi, M., Young, J. W.
(2005). Human Dendritic Cells: Potent Antigen-Presenting Cells at the Crossroads of Innate and Adaptive Immunity. J. Immunol.
175: 1373-1381
[Abstract]
[Full Text]
-
Schmitz, M., Zhao, S., Deuse, Y., Schakel, K., Wehner, R., Wohner, H., Holig, K., Wienforth, F., Kiessling, A., Bornhauser, M., Temme, A., Rieger, M. A., Weigle, B., Bachmann, M., Rieber, E. P.
(2005). Tumoricidal Potential of Native Blood Dendritic Cells: Direct Tumor Cell Killing and Activation of NK Cell-Mediated Cytotoxicity. J. Immunol.
174: 4127-4134
[Abstract]
[Full Text]
-
Demedts, I. K., Brusselle, G. G., Vermaelen, K. Y., Pauwels, R. A.
(2005). Identification and Characterization of Human Pulmonary Dendritic Cells. Am. J. Respir. Cell Mol. Bio.
32: 177-184
[Abstract]
[Full Text]
-
Kwakkenbos, M. J., Pouwels, W., Matmati, M., Stacey, M., Lin, H.-H., Gordon, S., van Lier, R. A. W., Hamann, J.
(2005). Expression of the largest CD97 and EMR2 isoforms on leukocytes facilitates a specific interaction with chondroitin sulfate on B cells. J. Leukoc. Biol.
77: 112-119
[Abstract]
[Full Text]
-
Munz, C., Dao, T., Ferlazzo, G., de Cos, M. A., Goodman, K., Young, J. W.
(2005). Mature myeloid dendritic cell subsets have distinct roles for activation and viability of circulating human natural killer cells. Blood
105: 266-273
[Abstract]
[Full Text]
-
Rivollier, A., Mazzorana, M., Tebib, J., Piperno, M., Aitsiselmi, T., Rabourdin-Combe, C., Jurdic, P., Servet-Delprat, C.
(2004). Immature dendritic cell transdifferentiation into osteoclasts: a novel pathway sustained by the rheumatoid arthritis microenvironment. Blood
104: 4029-4037
[Abstract]
[Full Text]
-
Qu, C., Edwards, E. W., Tacke, F., Angeli, V., Llodra, J., Sanchez-Schmitz, G., Garin, A., Haque, N. S., Peters, W., van Rooijen, N., Sanchez-Torres, C., Bromberg, J., Charo, I. F., Jung, S., Lira, S. A., Randolph, G. J.
(2004). Role of CCR8 and Other Chemokine Pathways in the Migration of Monocyte-derived Dendritic Cells to Lymph Nodes. JEM
200: 1231-1241
[Abstract]
[Full Text]
-
De Rosa, S. C., Lu, F. X., Yu, J., Perfetto, S. P., Falloon, J., Moser, S., Evans, T. G., Koup, R., Miller, C. J., Roederer, M.
(2004). Vaccination in Humans Generates Broad T Cell Cytokine Responses. J. Immunol.
173: 5372-5380
[Abstract]
[Full Text]
-
Rivas-Carvalho, A., Meraz-Rios, M. A., Santos-Argumedo, L., Bajana, S., Soldevila, G., Moreno-Garcia, M. E., Sanchez-Torres, C.
(2004). CD16+ human monocyte-derived dendritic cells matured with different and unrelated stimuli promote similar allogeneic Th2 responses: regulation by pro- and anti-inflammatory cytokines. Int Immunol
16: 1251-1263
[Abstract]
[Full Text]
-
Birdsall, H. H., Porter, W. J., Green, D. M., Rubio, J., Trial, J., Rossen, R. D.
(2004). Impact of Fibronectin Fragments on the Transendothelial Migration of HIV-Infected Leukocytes and the Development of Subendothelial Foci of Infectious Leukocytes. J. Immunol.
173: 2746-2754
[Abstract]
[Full Text]
-
Gregerson, D. S., Kawashima, H.
(2004). APC derived from donor splenocytes support retinal autoimmune disease in allogeneic recipients. J. Leukoc. Biol.
76: 383-387
[Abstract]
[Full Text]
-
Fagnoni, F. F., Oliviero, B., Giorgiani, G., De Stefano, P., Deho, A., Zibera, C., Gibelli, N., Maccario, R., Da Prada, G., Zecca, M., Locatelli, F.
(2004). Reconstitution dynamics of plasmacytoid and myeloid dendritic cell precursors after allogeneic myeloablative hematopoietic stem cell transplantation. Blood
104: 281-289
[Abstract]
[Full Text]
-
Gregerson, D. S., Sam, T. N., McPherson, S. W.
(2004). The Antigen-Presenting Activity of Fresh, Adult Parenchymal Microglia and Perivascular Cells from Retina. J. Immunol.
172: 6587-6597
[Abstract]
[Full Text]
-
Han, K. H., Hong, K.-H., Park, J.-H., Ko, J., Kang, D.-H., Choi, K.-J., Hong, M.-K., Park, S.-W., Park, S.-J.
(2004). C-Reactive Protein Promotes Monocyte Chemoattractant Protein-1--Mediated Chemotaxis Through Upregulating CC Chemokine Receptor 2 Expression in Human Monocytes. Circulation
109: 2566-2571
[Abstract]
[Full Text]
-
Giordano, D., Magaletti, D. M., Clark, E. A., Beavo, J. A.
(2003). Cyclic Nucleotides Promote Monocyte Differentiation Toward a DC-SIGN+ (CD209) Intermediate Cell and Impair Differentiation into Dendritic Cells. J. Immunol.
171: 6421-6430
[Abstract]
[Full Text]
-
Turville, S., Wilkinson, J., Cameron, P., Dable, J., Cunningham, A. L.
(2003). The role of dendritic cell C-type lectin receptors in HIV pathogenesis. J. Leukoc. Biol.
74: 710-718
[Abstract]
[Full Text]
-
Crowe, S., Zhu, T., Muller, W. A.
(2003). The contribution of monocyte infection and trafficking to viral persistence, and maintenance of the viral reservoir in HIV infection. J. Leukoc. Biol.
74: 635-641
[Abstract]
[Full Text]
-
Farges, J.-C., Romeas, A., Melin, M., Pin, J.-J., Lebecque, S., Lucchini, M., Bleicher, F., Magloire, H.
(2003). TGF-{beta}1 Induces Accumulation of Dendritic Cells in the Odontoblast Layer. JDR
82: 652-656
[Abstract]
[Full Text]
-
Li, G., Kim, Y.-J., Mantel, C., Broxmeyer, H. E.
(2003). P-Selectin Enhances Generation of CD14+CD16+ Dendritic-Like Cells and Inhibits Macrophage Maturation from Human Peripheral Blood Monocytes. J. Immunol.
171: 669-677
[Abstract]
[Full Text]
-
Schnurr, M., Toy, T., Stoitzner, P., Cameron, P., Shin, A., Beecroft, T., Davis, I. D., Cebon, J., Maraskovsky, E.
(2003). ATP gradients inhibit the migratory capacity of specific human dendritic cell types: implications for P2Y11 receptor signaling. Blood
102: 613-620
[Abstract]
[Full Text]
-
Ancuta, P., Rao, R., Moses, A., Mehle, A., Shaw, S. K., Luscinskas, F. W., Gabuzda, D.
(2003). Fractalkine Preferentially Mediates Arrest and Migration of CD16+ Monocytes. JEM
197: 1701-1707
[Abstract]
[Full Text]
-
Hamilton, J. A.
(2003). Nondisposable materials, chronic inflammation, and adjuvant action. J. Leukoc. Biol.
73: 702-712
[Abstract]
[Full Text]