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NEOPLASIA
From the Laboratory of Immunopathology, National
Institute of Allergy and Infectious Diseases, the Hematopathology
Section, Laboratory of Pathology, National Cancer Institute, National
Institutes of Health, Bethesda, MD; the Pathology/Histotechnology
Laboratory, SAIC-Frederick, the Veterinary and Tumor Pathology Section,
Center for Cancer Research, National Cancer Institute at Frederick,
National Institutes of Health, Frederick, MD; the Walter and Eliza Hall
Institute of Medical Research, Melbourne, Victoria, Australia; the
Department of Pathology, Massachusetts General Hospital, Boston, MA;
the Department of Laboratory Medicine, University of California, San
Francisco; Children's Hospital of Los Angeles, CA; and the University
of Birmingham Medical School, Birmingham, United Kingdom.
A consensus system for classification of mouse lymphoid neoplasms
according to their histopathologic and genetic features has been an
elusive target for investigators involved in understanding the
pathogenesis of spontaneous cancers or modeling human hematopoietic diseases in mice. An international panel of scientists with expertise in mouse and human hematopathology joined with the hematopathology subcommittee of the Mouse Models for Human Cancers Consortium to
develop criteria for definition and classification of these diseases
together with a standardized nomenclature. The fundamental elements
contributing to the scheme are clinical features, morphology, immunophenotype, and genetic characteristics. The resulting
classification has numerous parallels to the World Health Organization
classification of human lymphoid tumors while recognizing differences
that may be species specific. The classification should facilitate
communications about mouse models of human lymphoid diseases.
(Blood. 2002;100:246-258) A systematic classification of mouse
hematopoietic neoplasms was first put forward by Dunn in
1954.1 In this assemblage, tumor types were related to
presumed cells of origin, including undifferentiated cells,
lymphocytes, granulocytes, "reticulum cells" Types A and B,
plasmacytes, and tissue mast cells. Similar names for tumor types can
be found in the 1966 Rappaport nomenclature for human hematopoietic
tumors.2 Following the identification of T- and B-cell
lymphocyte subsets in the 1970s, Pattengale and Taylor3
revised the mouse classification scheme to generally parallel the
1974 Lukes-Collins proposal for human hematopoietic neoplasms.4 Within these frameworks, most tumors
previously defined as of reticulum cell origin were recognized to
correspond to B-cell lineage lymphomas. In 1994, Fredrickson et
al5 used the human Kiel classification of 19816
as modified in 19887 as the basis for a nomenclature. Among
other features, it encompassed previously unrecognized subtypes of
mouse B-cell lineage lymphoma, including splenic marginal zone lymphoma
(SMZL).8 Most recently, the consensus nomenclatures for
human hematopoietic tumors established by the 1995 Revised
European-American Lymphoma9 and descendant 2001 World
Health Organization (WHO) schemes10,11 were adopted as a
model by investigators from the National Institutes of Health in an
effort to develop a contemporaneous scheme for classification of mouse
lymphoma and leukemia.12-14
The iterative nature of the lists and definitions of disease entities
in the mouse derives from the increasingly well-supported presumption
that carefully defined and validated model systems can provide
fundamental insights into human disorders with attendant implications
for prevention and intervention. The opportunities to extend this
concept provided by manipulation of the mouse genome were recognized in
the formation of the Mouse Models of Human Cancers Consortium (MMHCC)
by the United States National Cancer Institute
(http://emice.nci.nih.gov). The Hematopathology
Subcommittee of the MMHCC was given the charge of developing a
consensus list of hematopoietic neoplasms with descriptions and
criteria for diagnosis. The goal was to define disease entities that
could be recognized by pathologists and related to human disorders
where possible. To meet this challenge, gatherings of international experts in human and mouse hematopathology were convened. The result of
their deliberations is a proposed classification of hematopoietic
diseases that stratifies disorders according to cell lineage. The
resulting major subgroups are, accordingly, lymphoid and nonlymphoid.
The lymphoid disorders will be discussed here and the nonlymphoid in a
separate article.48
Most of our present knowledge of mouse hematopoietic neoplasms is
based on studies of such diseases in inbred and outbred mice occurring
either spontaneously or following induction with irradiation,
chemicals, or exogenous infection with murine leukemia viruses
(MuLVs).3,5,8,15,16 There is considerable strain dependence of disease types and incidence, with much of the differences being genetically determined. Some of these variations are associated with expression of endogenous MuLV and virus-controlling
genes,17,18 although infectious MuLVs are not required for
induction or progression of many disorders. These considerations are
not obviated for diseases developing in genetically engineered mice
(GEM)19 but are likely of less importance. Although the
range of lymphoid neoplasms seen in conventional mice is broad, it has
been substantially extended through genetic engineering. Some of the
newly recognized disorders in GEM recapitulate those of humans with
greater or lesser levels of fidelity, whereas others appear not to.
Indeed, some of the lymphomas and leukemias seen in GEM have never been
seen previously as spontaneous lymphomas in mice. In this regard, it is
important to remember that only a limited number of strains have been
evaluated in a rigorous manner for the characteristics of spontaneous
lymphomas. The information at hand that forms much of the basis for our
proposals may thus not be representative of the full range of diseases
that develop among unmanipulated mice.
A prominent goal of studying mouse tumors is to develop an
understanding of pathogenesis that would provide opportunities for
preventing or treating similar disorders of humans. It has, therefore,
been important to determine whether diseases in the 2 species are true
homologs and deserve identical names. We have found this case is often
difficult to make. The reasons are multiple. Prominent among these
reasons are fundamental differences between the species in the
characteristics of primary and secondary lymphoid organs. Uniquely in
mice, extramedullary hematopoiesis continues in the red pulp of the
spleen throughout life, and the thymus persists well into adulthood.
The splenic marginal zone of mice has also been shown to differ
significantly from that in humans.20
An additional critical difference is that many modalities used to
classify human lymphomas have been applied much less routinely or
rigorously to studies of mouse tumors. Without these direct comparisons
at hand, guesswork and wishful thinking provide insufficient grounds
for identifying true parallels. Consequently, although the committee
developed a set of recommendations to be used by pathologists and
investigators diagnosing these diseases, these proposals will be
altered and updated as additional information becomes available. The
fundamental elements contributing to classification of lymphomas in the
WHO classification are clinical features, morphology, immunophenotype,
and genetic abnormalities. The committee concluded that the same types
of information should be developed, when possible, in studies of mouse
hematopoietic neoplasms.
Committee recommendations for approaches to diagnosing lymphoid
neoplasms of mice are not presented here because of space constraints
but are provided in supplementary material available on the
Blood website; see the Supplemental Data link at the top of
the online article. These recommendations should be reviewed in
detail by those new to the field of mouse hematopathology studying either spontaneous or induced models of disease. The guidelines may
also provide a helpful review for more established investigators. We
anticipate that more uniform application of these approaches to
diagnosis and classification by the hematopathology community will
facilitate the characterization of lymphomas and leukemias and yield
descriptions that can be more readily understood by all. The
supplementary material provides approaches to necropsies, sample
collection and storage, fixation and staining, as well as flow
cytometric and molecular evaluations of tumor samples. Critical
parameters for distinguishing reactive from malignant processes
complete the online package. The terminology used in the textual
material of the print version is based on the definitions provided in
the supplementary information.
The consensus recommendations of the Hematopathology Subcommittee
of the MMHCC for classification of mouse lymphoid neoplasms follow the
WHO classification in many respects but use distinct terminology when
appropriate. Differences in the schemes have several origins that will
be dealt with in describing each of the diseases.
Just as the classification of human lymphomas is a work in progress
with the WHO scheme being just the most recent version, we view
the proposed classification for mouse lymphoid neoplasms as a statement
of where we are at present. The scheme presented in Figure
1 will be revised as new data on
established
diseases, both human and mouse, become available and as new disorders are described.
Table 1 compares the features of the
lymphoma/leukemia types and their relation to diseases in humans.
Several conventions will be followed in the table. First, the phenotype
of mature B-cell lymphomas will be given as sIg+ B220
[CD45R(B220)]+ CD19+ with the recognition
that other markers may be useful in distinguishing distinct types.
Second, the molecular characteristics of mature B-cell lymphomas,
regardless of type, will be presented in Table 1 as if both heavy chain
and both kappa light chain alleles have undergone rearrangements [IgH
R/R, IgK R/R] with the recognition that only one allele of each may be
rearranged and that lambda light chain may be rearranged and used in a
subset of the neoplasms. In these diagnostic categories, the T-cell
locus will be listed as unrearranged, indicating only the T-cell
receptor locus (TCR
Hypermutation of immunoglobulin variable region sequences
indicates that human lymphomas of this type are of germinal center B-cell origin or have evidence of having passaged the germinal center.
Careful studies among medical hematopathologists led to the
conclusion that it is difficult to reproducibly distinguish morphologic
variants designated centroblastic, immunoblastic, T-cell/histiocyte
rich, and other subsets of this disorder defined in pre-WHO
nomenclatures.9 The prospect that morphologic variants may
in time be associated with specific genetic features defined by using
complementary DNA microarray or other technologies led to the
suggestion that use of the terminology for the variants remains
optional.10 The mouse lymphomas may provide a
stronger case for continuing with subset designations in view of highly distinctive morphologic and histologic features of several proposed types (Figure 3A-D). Until such time as these designations can be
buttressed by criteria other than histologic appearance, it would seem
prudent to keep the use of these morphologic subgroups optional.
There are aspects to distinguishing diffuse large B-cell lymphomas
(DLBCLs) from other entities in both humans and mice that deserve
comment. First, human follicular lymphomas are defined by a combination
of what, for purposes of discussion, can be termed cytologic and
architectural features within lymph nodes. The cytologic range of these
neoplasms comprises primarily centrocytes and centroblasts. The
representation of centroblasts is variable, ranging from less than 5 per high-power field to solid sheets of blasts. The architectural hallmark of this disease is poorly defined follicular structures. The
proportion of lymph nodes with follicular structures can vary from less
than 25% to complete, the remaining areas being diffusely involved.
Retention of follicular architecture may thus be said to be the
signature distinction between human DLBCL of centroblastic type and
follicular lymphomas comprising exclusively centroblasts.
In mice, the cytologic and architectural features that
distinguish follicular from DLBCLs are distinct. First, mouse
follicular tumors composed almost uniformly of centrocytes are
extremely rare, and more evenly balanced populations of centrocytes and centroblasts tend to be the distinguishing feature (Figure 2E). Second,
follicular lymphomas in mice usually arise in spleen rather than lymph
nodes, meaning that the architectural-distinguishing features of the
diseases are fundamentally different for the 2 species. The appearance
of involved spleen is nodular at both the gross and microscopic levels
with progressive expansion of multiple or all follicles in the white
pulp leading to compression of the red pulp as well as the T-cell
periarteriolar lymphocytic sheath. Progression may lead to lymphomas
with an almost pure population of centroblasts that remain restricted
to the white pulp or spread into the red pulp but with the follicular
origin still evident. These are centroblastic lymphomas of follicular origin. For historical reasons, it is worth noting that Pattengale and
Taylor3 defined follicular center cell lymphomas as small cell, large cell, and mixed. The large cell type corresponds to what we
are here calling DLBCL.
Two other subtypes of centroblastic lymphoma have been observed. The
first represents a progression of SMZL to a higher grade with clear
anatomic evidence of its origins.8 The other type comprises centroblastic tumors for which an origin from the follicle or
marginal zone cannot be inferred.
Recent studies have described clonal B-cell lymphomas with high
proportions of nonclonal T cells.21 It has been suggested that these mouse tumors may be the equivalent of human T-cell-rich DLBCL, but the frequencies of T cells have not been determined by flow
cytometry and may not reach the levels seen in the human disease.
Second, there are mouse lymphomas that are histologically
indistinguishable from precursor B-cell and precursor T-cell lymphomas but comprise mature sIg+ B cells.22,23 In the
veterinary literature, these lymphomas have been classified together
with precursor neoplasms as lymphoblastic lymphoma. The fact that some
lymphomas of this type derived from 2 different populations of mice
exhibited structural alterations in BCL-6, the most common genetic
abnormality of human DLBCL,24 originally was used to argue
for their classification as DLBCL, despite their lymphoblastic
appearance and the lack of human tumors with this combination of
histologic and immunophenotypic features.22,23 With the
more recent opportunity to study large numbers of cases of mouse
Burkitt lymphoma (Figure 3E),25 it became apparent that a
proportion of the sIg+ lymphoblastic tumors resembled mouse
Burkitt lymphoma histologically while sharing a proliferative fraction
approaching 100%. This finding suggests atypical Burkitt or
Burkittlike as perhaps more appropriate terminology for these lymphomas
(Figure 3F). In the WHO classification, however, this term is reserved
for cases with nonclassical cytology despite proven or likely
translocations activating MYC.10 MYC is not rearranged in
a significant proportion of the mouse lymphomas of this type, weakening
an argument for a change in classification terminology from DLBCL.
Nevertheless, the common morphologic and behavioral features of mouse
Burkitt lymphoma and mouse sIg+ "lymphoblastic" tumors
suggest that they may share analogous pathogenesis. Therefore, we
recommend that the term Burkittlike be applied to mature B-cell
neoplasms with proliferative fractions approaching 100% even in the
absence of MYC translocation. The term Burkitt lymphoma will be
reserved for tumors with compatible morphology, phenotype, and MYC
dysregulation because of translocation or genetic manipulation. This
area is clearly one in which it can be anticipated that molecular
profiling will be of great use in sorting out histologically similar
mature B-cell lymphomas.
Finally, although the term plasmablastic lymphoma is used for a variant
of human DLBCL, it is subsumed under plasma cell neoplasms in mice
(Figure 4). The major reason for this decision is that most mouse
plasmacytic lymphomas cover a range of cytologic features, ranging from
mature monoclonal plasma cells to plasmablasts in varying
proportions. The plasmablastic variant represents one extreme. Human
plasmablastic lymphoma, by comparison, typically lacks mature plasma
cells and can have a morphologic spectrum that ranges from
immunoblastic to Burkitt lymphoma.
Several diseases are recognized as occurring in unusual
circumstances. One is found in association with 2 different mutations in a common signaling pathway, and a second is found in response to
infection with a unique mixture of MuLVs. These are the diseases of
mice homozygous for mutations of Fas or Fasl and
mice with the retrovirus-induced immunodeficiency syndrome, MAIDS.
These diseases are characterized in their early stages by greatly
expanded polyclonal proliferations of lymphocytes that are ultimately
replaced by monoclonal populations of B cells. Cells in the early
stages of these chronic proliferative disorders do not transplant to immunocompetent or immunodeficient hosts, whereas those cells from
late-stage animals can be transferred most readily to mice with
impaired immunity. The cells that proliferate in the adoptive hosts are
clearly lymphomas, but their presence in the original animal is not
often apparent, as the expanded populations of nontransformed cells
obscure their presence. The committee was hesitant to classify these
lymphomas with those readily diagnosed in the primary host because
there was no way to determine the stage of the tumor in the primary
host or to know how passage in vivo may have influenced histologic
appearance and phenotype. The difficulties associated with defining the
MAIDS tumors as true lymphoma have been discussed.26 These
disorders and their associations with lymphoma are important areas for
further study.
Mice with mutations of Fas or Fasl develop
massive lymphadenopathy and splenomegaly due to the polyclonal
accumulation of TCR Mice infected with the LP-BM5 mixture of MuLV develop a
degree of splenomegaly and lymphadenopathy rivaled only by mice with mutations in Fas and Fasl.31,32
Initially, germinal centers are very prominent with large numbers of
plasma cells intermixed with centroblasts and increasing numbers of
immunoblasts. The disease is initially polyclonal for both B and T
cells,33,34 followed by the appearance of oligoclonal
populations of B cells more often than of T cells around 8 weeks after
infection.33 By 12 weeks, all mice have monoclonal
populations of T or B cells that can be transplanted to immunodeficient
hosts.35,36 In occasional mice, lymphomas can result in
paralysis and death from invasion of the central nervous
system.33 Under the proposed nomenclature, the transplants
can be described as DLBCL. B-cell lineage lymphomas occur at high
frequencies in patients with genetically determined, iatrogenic, or
acquired immunodeficiencies such as AIDS,37 providing
possible human parallels.
The content of this publication does not necessarily reflect the
views or policies of the Department of Health and Human Services, nor
does the mention of trade names, commercial products, or organizations imply endorsement by the United States government.
Submitted October 25, 2001; accepted February 25, 2002.
Supported in part with funds from the Mouse Models of Human Cancers
Consortium, National Cancer Institute, National Institutes of Health,
and by contract N01-CO56000 from the National Cancer Institute.
H.C.M.III and J.M.W. assisted in the organization of the pathology
meeting and prepared the manuscript with assistance from the other
authors listed alphabetically. The publication represents the consensus
of the committee that included the authors, Robert D. Cardiff, Cory
Brayton, James Downing, Hiroshi Hiai, Pier Paolo Pandolfi, Jules J. Berman, Mark S. Tuttle, and Archibald S. Perkins.
The online version of the article contains a data supplement.
The publication costs of this
article were defrayed in part by
page charge payment. Therefore,
and solely to indicate this fact,
this article is hereby marked
"advertisement"
in accordance with 18 U.S.C.
section 1734.
Reprints: Herbert C. Morse III, 7 Center Dr, Rm 7/304, MSC
0760, Bethesda, MD 20892-0760; e-mail: hmorse{at}niaid.nih.gov.
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|
Top
Abstract
Introduction
G/G), with the recognition that the locus is
rearranged in some B-lineage tumors. An expanded description of the
occurrence of lymphomas of each diagnostic category is given in Table 5 of the supplementary material, and a more complete listing will be
given at the MMHCC Web site
(
/
CD8
do fibroblasts guide lymphocyte immigration?
Am J Pathol.
2001;159:501-512