The metastasis of tumour cells is a leading cause of mor-
tality in cancer patients and occurs through lymphatic
vessels and blood vessels. The presence of tumour cells
in regional or sentinel lymph nodes (SLNs) is a key pre-
dictor of poor outcome in human cancer
1
, which illus-
trates the relevance of lymphatics to cancer biology. It
was previously thought that the lymphatic vasculature
had a passive role in cancer metastasis; however, experi-
mental and clinicopathological studies indicate that
lymphatic vessels undergo dynamic changes that facili-
tate metastasis. These changes include lymphangiogenesis
and lymphatic enlargement (which can occur through
lymphatic hyperplasia), and they involve initial lymphatics
around the primary tumour. These events are thought to
favour entry of tumour cells into the lymphatic vascula-
ture
2–5
. The enlargement of collecting lymphatics that are
proximal or distal to SLNs, which is a process that can
involve proliferation of lymphatic endothelial cells
(LECs), other non-proliferative mechanisms and altera-
tions to lymphatic-associated vascular smooth muscle
cells (LVSMCs), has also been reported and is thought to
facilitate the dissemination of tumour cells
6,7
. Moreover,
lymphangiogenesis in tumour-draining lymph nodes
might increase the spread of tumour cells to distant sites
in the body
8
.
The recognition that lymphangiogenesis and lymph-
atic remodelling are functionally important in cancer
has led to the idea that blocking them, by targeting
lymphangiogenic signalling pathways, might be a use-
ful therapeutic strategy to restrict metastatic spread
9
.
Furthermore, the remodelling of tumour-associated
lymphatics and of lymphatics in tumour-draining
lymph nodes might provide prognostic opportuni-
ties
10
. In this Review we discuss lymphangiogenesis and
lymphatic remodelling in cancer, and we focus on recent
progress in defining the molecular and cellular mecha-
nisms that control these processes. The implications of
these findings for the development of new diagnostics
and therapeutics, and for future cancer research, are
also discussed.
Structure of the lymphatic system
Although the structure and physiology of the lymphatic
system have been studied since the Renaissance
11
,
advances in identifying molecular markers of lymph-
atics (BOX 1), which have predominantly occurred over
the past 20 years, have focused on the unique cellular
and functional features of this system and its role in
pathology. The lymphatic vasculature is essential for
immune function, tissue fluid homeostasis and for the
absorption of dietary fat. Starting as small blind-ended
vessels that absorb fluid and cells in tissues
12,13
, the ini-
tial lymphatics are characterized by short anchoring
filaments, which connect the abluminal membrane of
LECs to the surrounding elastic fibres in the tissue
12
(FIG. 1). These lymphatics have an intermittent basement
membrane and no pericytes or VSMCs. The tethering
of LECs to elastic fibres, as well as unique discontinu-
ous ‘button-like’ cell–cell junctions between LECs allow
flaps of the vessel to open and fluid to enter but not to
leave. The anchoring filaments are particularly impor-
tant when the interstitial fluid pressure is increased
1
Tumour Angiogenesis
Program, Peter MacCallum
Cancer Centre, East
Melbourne, Victoria 3002,
Australia.
2
Sir Peter MacCallum
Department of Oncology,
University of Melbourne,
Victoria 3010, Australia.
3
Department of Surgery,
Royal Melbourne Hospital,
University of Melbourne,
Parkville, Victoria 3050,
Australia.
4
Department of Surgery,
St. Vincent’s Hospital,
University of Melbourne,
Fitzroy, Victoria 3065,
Australia.
5
O’Brien Institute, Australian
Catholic University, Fitzroy,
Victoria 3065, Australia.
6
Department of Pathology,
Peter MacCallum Cancer
Centre, East Melbourne,
Victoria 3002, Australia.
Correspondence to
S.A.S. and M.G.A.
e‑mails: Steven.stacker@
petermac.org;
Marc.achen@petermac.org
doi:10.1038/nrc3677
Published online
13 February 2014
Lymphangiogenesis and lymphatic
vessel remodelling in cancer
Steven A. Stacker
1–3
, Steven P. Williams
1
, Tara Karnezis
1,2
, Ramin Shayan
1,3–5
,
Stephen B. Fox
2,6
and Marc G. Achen
1–3
Abstract | The generation of new lymphatic vessels through lymphangiogenesis and the
remodelling of existing lymphatics are thought to be important steps in cancer metastasis.
The past decade has been exciting in terms of research into the molecular and cellular
biology of lymphatic vessels in cancer, and it has been shown that the molecular control of
tumour lymphangiogenesis has similarities to that of tumour angiogenesis. Nevertheless,
there are significant mechanistic differences between these biological processes. We are
now developing a greater understanding of the specific roles of distinct lymphatic vessel
subtypes in cancer, and this provides opportunities to improve diagnostic and therapeutic
approaches that aim to restrict the progression of cancer.
REVIEWS
NATURE REVIEWS | CANCER VOLUME 14 | MARCH 2014 | 159
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