© 2014 Nature America, Inc. All rights reserved.
NATURE IMMUNOLOGY ADVANCE ONLINE PUBLICATION 1
RESOURCE
Myeloid cells in mammals are crucial in the formation and execu-
tion of immune responses. They are able to recognize damage- and
pathogen-associated molecular patterns through germline-encoded
receptors and not only initiate but also amplify adaptive immune
response through antigen presentation and cytokine production. In
hematopoiesis, a myeloid cell is any white blood cell that is not a
lymphocyte. By this definition, monocytes and granulocytes are the
most common myeloid cell populations in the blood. But dendritic
cells (DCs) and various populations of macrophages, monocytes and
polymorphonucleated cells can be found in solid tissues
1
. Myeloid
cells can be classified by cell surface–marker expression, ontogeny or
differential dependence on lineage-defining transcription factors and
growth factor signaling, which sharply distinguishes specific popula-
tions
2–5
. However, recent studies have further highlighted the com-
plex ontogeny of macrophages and DCs
5,6
. These advances highlight
the unexpected complexity of the myeloid system and the limited
capacity to identify the numerous cell types of myeloid origin with
highly specialized functions and tissue distribution.
Analysis of myeloid cells relies predominantly on historical nomen-
clature and the use of traditional markers to define cell populations,
but these do not encompass the full complexity of the myeloid sys-
tem. For example, macrophages branded solely by the expression of
the common myeloid marker CD11b and the macrophage marker
F4/80 in adult mice are likely to be contaminated by eosinophils,
monocytes or both
7
. CD11b is not expressed by alveolar macrophages,
and many macrophage subpopulations do not express F4/80 (ref. 8).
Monocyte-derived cells that have phenotypic and functional proper-
ties shared by both DCs and macrophages are difficult to objectively
distinguish
9–12
. Inflammation further complicates the picture when
myeloid cells undergo phenotypic changes or other cell types not
present in the steady state emerge. Such inflammatory DCs have been
termed monocyte-derived DCs (moDCs) or tumor necrosis factor
(TNF)- and iNOS-producing DCs (TIP-DCs)
13
. In addition, a number
of subsets of myeloid-derived suppressor cells have been defined by
association of functional and phenotypic properties in preclinical can-
cer models, but their definitions often overlap with other described
myeloid subsets, which leads to confusing nomenclature
14,15
. A series
of reports identified additional cell surface markers on specific subsets
within the myeloid compartment, which sharpened the distinction
between DCs and macrophages while further increasing the number
and complexity of myeloid subpopulation definitions
16–18
. Multiple
populations of granulocytes, monocytes, monocyte-derived cells, resi-
dent macrophages and DCs coexist in tissues, but their unambiguous
identification is becoming increasingly difficult.
Analysis of cellular lineages relies chiefly on fluorescence flow cytom-
etry and informed biased gating strategies. Such technology, although
far progressed, is bound by the number of independent parameters and
spectral overlap. Fluorescence-based analysis of phagocytic myeloid cells
is further complicated by their (often strong) autofluorescence at wave-
lengths in the range of 500–600 nm, which contributes to potentially
1
Agency for Science, Technology and Research (A*STAR), Singapore Immunology Network (SIgN), Singapore.
2
Institute of Experimental Immunology, University of Zurich,
Zurich, Switzerland.
3
School of Biological Sciences, Nanyang Technological University, Singapore.
4
Present address: Institute of Experimental Immunology, University of
Zurich, Zurich, Switzerland.
5
These authors contributed equally to this work. Correspondence should be addressed to E.W.N. (evan_newell@immunol.a-star.edu.sg) or
B.B. (becher@immunology.uzh.ch).
Received 12 June; accepted 9 September; published online 12 October 2014; doi:10.1038/ni.3006.
High-dimensional analysis of the murine myeloid
cell system
Burkhard Becher
1,4,5
, Andreas Schlitzer
1,5
, Jinmiao Chen
1,5
, Florian Mair
2
, Hermi R Sumatoh
1
,
Karen Wei Weng Teng
1
, Donovan Low
1
, Christiane Ruedl
3
, Paola Riccardi-Castagnoli
1
, Michael Poidinger
1
,
Melanie Greter
2
, Florent Ginhoux
1
& Evan W Newell
1
Advances in cell-fate mapping have revealed the complexity in phenotype, ontogeny and tissue distribution of the mammalian
myeloid system. To capture this phenotypic diversity, we developed a 38-antibody panel for mass cytometry and used
dimensionality reduction with machine learning–aided cluster analysis to build a composite of murine (mouse) myeloid cells
in the steady state across lymphoid and nonlymphoid tissues. In addition to identifying all previously described myeloid
populations, higher-order analysis allowed objective delineation of otherwise ambiguous subsets, including monocyte-macrophage
intermediates and an array of granulocyte variants. Using mice that cannot sense granulocyte macrophage–colony stimulating
factor GM-CSF (Csf2rb
-/-
), which have discrete alterations in myeloid development, we confirmed differences in barrier tissue
dendritic cells, lung macrophages and eosinophils. The methodology further identified variations in the monocyte and innate
lymphoid cell compartment that were unexpected, which confirmed that this approach is a powerful tool for unambiguous and
unbiased characterization of the myeloid system.