Digestive tract cancer is one of the most common
types of malignant tumors worldwide and primarily includes
esophageal cancer (EC), gastric cancer (GC), pancreatic cancer
(PC), liver cancer (LC) and colorectal cancer (CRC). According to
the World Health Organization, digestive tract cancer accounts for
more than a quarter (26%) of global cancer incidence, and more than
a third (35%) of all cancer-associated deaths across the world
(1). Therefore, it is urgent to
identify early screening methods for digestive tract cancer, as
well as improved approaches for prognosis of patients with advanced
disease. Improving the prognosis of patients with digestive tract
cancer, particularly those with advanced disease, is an urgent
issue. Accordingly, it is key to identify new targets for the early
diagnosis and treatment of digestive tract cancer to improve
disease survival and overall quality of life.
S100 proteins belong to a polygenic calcium-binding
family composed of small acidic proteins. S100 proteins are widely
expressed with high tissue- and cell-specificity and were firstly
extracted from bovine brain tissues by Moore in 1965 (2). S100 proteins dissolve in saturated
ammonium sulfate solution at neutral pH (3). In human, the S100 protein family
consists of 20 members (4), 16 of
which are located on chromosome 1q21 and known as group A S100
proteins (5) (Table I). The corresponding genes are
highly conserved and encode small proteins with ~100 amino acids in
size. S100 proteins have a highly similar calcium binding protein
sequence, known as the elongation factor (EF hand). When calcium
ion binds the EF hand, S100 proteins bind to the corresponding
receptors and participate in various cellular processes, including
proliferation, differentiation and apoptosis (6). Increasing evidence has demonstrated
that the S100 protein family is associated with pathogenesis of
digestive tract cancer, including LC (7–10).
The aberrant expression of specific S100 isoforms drives LC, such
as S100A4, S100A6, S100A8, S100A9 and S100A11 (7). The present review aimed to summarize
studies on the role of S100 protein family in digestive tract
cancer. Elucidating the effects and underlying mechanisms of S100
proteins may provide insight into the pathogenesis of digestive
tract cancer. In particular, S100 inhibitors for cancer treatment
may have significance, given the pivotal role of S100 signaling in
tumorigenesis and tumor biology (4).
S100 protein family consists of 25 members,
characterized by low molecular weight and a symmetrical dimeric
structure. S100 proteins exhibit notable homology with both
calmodulin and calcium-binding proteins (11). The conformation of S100 protein
changes when bound to Ca2+, exposing hydrophobic amino
acids in the first helix and hinge regions of the C-terminal EF
hand (12). S100 protein members
serve as intracellular Ca2+ sensors during
carcinogenesis via the regulation of
Ca2+/S100A4/myosin-IIA complex and other mechanisms
(13,14).
S100 proteins serve a key role in regulating cell
proliferation, differentiation, and apoptosis by interacting with
enzymes, cytoskeletal subunits, receptors, transcriptional factors
and nucleic acids (15). S100
proteins exert biological effects in either an autocrine or
paracrine manner (16). S100
proteins are implicated in inflammation, tissue repair and
resistance to pathogens by binding to various receptors, including
G protein-coupled receptor, scavenger receptor and receptor for
advanced glycation end products (RAGE), and activating mTOR,
Src/annexin A2 (ANXA2)/AKT and PI3K signaling pathways (17,18).
Besides, S100 family members participate in regulating
neuroinflammation in astrocytes and microglia and may serve as
diagnostic and therapeutic targets (for instance, S100A8/A9)
(19). The expression of S100
protein members is specific in different types of cancer.
Dysregulation of S100 family proteins occurs in most types of
cancers, suggesting their key roles in tumorigenesis. S100P is
upregulated in multiple cancers, such as lung cancer, CRC, and PC
(20). S100A4 is an important
regulator of immunosuppressive T cells in human glioma, affecting
immune microenvironment balance and survival (21). S100A7 is significantly associated
with the prognosis of head and neck squamous carcinoma (22). S100A6 regulates cancer cell
proliferation, apoptosis, migration and invasion, which is also
associated with poor prognosis (4,23).
S100A10, also known as p11, is found to mediate the conversion of
plasminogen to plasmin primarily by binding to ANXA2 (24). This interaction results in
degradation of the extracellular matrix, facilitating the
dissemination of cancer cells through the bloodstream. In breast
cancer, S100A14 enhances the phosphorylation of HER2 and the
activation of AKT/ERK signaling pathway, thereby promoting the
development of breast cancer (25). Taken together, the aforementioned
studies have suggested key roles of S100 family members (including
S100P, S100A4, S100A6, S100A7, S100A10, and S100A14) in the
development and progression of various types of cancers. The
present study summarizes the role of S100 family in digestive tract
cancers to provide insights into cancer pathogenesis and novel
therapeutic strategies.
GC is one of the most common types of malignant
tumors across the world. The majority of patients with GC are
diagnosed at advanced stage with poor prognosis. Therefore, it is
necessary to explore more effective strategies for the early
diagnosis of GC. A previous study demonstrated that S100A4 promotes
proliferation and migration of GC cells by regulating a downstream
effector family with sequence similarity 107 member B via the PI3K
signaling (Fig. 1) (26). Another study found that S100A4
increases the stemness of cancer cells via upregulating NANOG and
SOX2, thereby promoting gastric carcinogenesis (27). Bian et al (28) reported that silencing S100A4 using
small interfering RNA inhibited the proliferation and migration of
GC cells. Furthermore, this effect is enhanced by microRNA (miRNA
or miR)-3189-3p mimics, which targeting cofilin-2 and further
inhibiting GC cell proliferation and migration (28). Accordingly, S100A4 may serve as a
promising biomarker and treatment target for GC due to its key
effects in regulating the biological behavior of cancer cells
(Table II).
Another well-established S100 family member is
S100A9, the expression and function of which exhibit variability
across types of cancer (29–31).
Enhanced expression of S100A9 has been observed in GC and promotes
the proliferation and migration of cancer cells (30). S100A9 plays dual roles, acting both
as a pro- and anti-tumor factor independently and forming
heterodimers with S100A8 (S100A8/A9) during gastric carcinogenesis
(31). It is involved in
inflammation in GC. At low concentrations, S100A8/A9 promotes
cancer cell proliferation and migration by activating NF-κB-, RAGE-
and MAP kinase-dependent signaling pathways (32). Conversely, at high concentrations,
S100A8/A9 exhibits cytotoxic (33)
and pro-apoptosis effects on GC cells by regulating Bax/Bcl-2
expression and activation of ERK (34). Positive association between S100A9
expression and the overall survival of patients with GC has been
demonstrated (35), suggesting the
protective role of S100A9 at high concentration against GC. It has
also been well documented that endogenous S100A8/A9 inhibits
migration and invasion of GC cells, whereas exogenous S100A8/A9
functions as a heterodimer to activate NF-κB signaling, thereby
promoting the development of GC (32,36).
This discrepancy may be attributed to differences in cancer
microenvironment (37). Given the
complicated effects of S100A9 under varying concentrations and
cellular locations, it is key to elucidate the precise molecular
mechanisms of S100A9 in regulating GC.
S100A10, a key member of the S100 family, is
upregulated in some malignant tumors, including lung cancer
(38) and LC (39). Similarly, increased expression of
S100A10 has been found in GC (40). S100A10 can promote gastric
carcinogenesis by enhancing GC cell proliferation and the
consumption of glucose via the Src/ANXA2/AKT/mTOR signaling pathway
(40). Besides, enhanced
succinylation of S100A10 promotes GC invasion and metastasis
depending on the activity of carnitine palmitoyltransferase 1A
(41). Taken together, S100A10
emerges as a promising therapeutic target due to its key role in
regulating the growth, invasion and metastasis of GC.
Liver is one of the most important digestive organs
responsible for the metabolisms of lipid, fatty acid and other
substances by regulating various active factors, such as growth
factors and cytokines (46,47).
Effective therapeutic strategies for HCC include surgery,
chemotherapy, targeted therapy and liver transplantation. However,
the prognosis of HCC remains poor (48). Therefore, it is necessary to
explore more effective strategies to achieve early intervention and
treatment of HCC. Increasing studies have demonstrated that S100
proteins play important roles in HCC and may serve as useful
diagnostic and prognostic markers (49–52).
Increased expression of S100A1 is observed in HCC tissue and is
positively related to tumor and tumor grade and survival rate
(53). Moreover, S100A1
contributes to HCC by inhibiting phosphorylation of LATS1 and
yes-associated protein via the Hippo pathway (53). S100A4 is a risk factor for GC
(26). Zhai et al (50) reported that S100A4 is involved in
HCC pathogenesis by promoting EMT and upregulating MMP-9 via the
NF-κB pathway (51,52). In HCC, Hepatitis B virus X (HBx)
protein can enhance the expression of S100A4, thus promoting the
proliferation of HCC cells (54).
Exosome-derived S100A4 can induce the metastasis of HCC by
regulating cell adhesion and remodeling of extracellular matrix
(55,56). Furthermore, S100A4 is highly
expressed in hypermetastatic HCC cells, which can promote invasion
and metastasis by upregulating miR-155 and activating STAT3
(57,58). In addition, high expression of
S100A4 predicts poor prognosis of HCC (49). Accordingly, S100A4 is a key
regulator in HCC. Exosomal S100A4 may serve as a promising marker
for HCC progression and prognosis. Other S100 proteins are involved
in the pathogenesis of HCC, such as S100A6 (59), S100A9 (60), S100A10 (61), S100A11 (62) and S10013 (63). Among them, increased expression of
S100A6 leads to HCC cell proliferation and invasion by enhancing
degradation of p53 (64). In
addition to cancer cell proliferation and invasion, high expression
of S100A9 is associated with poor differentiation and increased
malignancy of HCC (65). S100A9
secreted by tumor-associated macrophages functions as a cancer
promoter by recruiting more macrophages and other inflammatory
cells via chemokine ligand 2, thereby establishing a positive
feedback loop that leads to increased production of S100A9 within
the tumor microenvironment (66).
Similar to S100A4, HBx protein can elevate the expression of S100A9
via the NF-κB pathway, which thus promotes hepatitis B
virus-associated HCC occurrence and metastasis (67). In addition, increased expression of
S100A11 occurs in HCC, contributing to the invasion and migration
of HCC cells (68). It also
enhances inflammation and fibrosis via epidermal growth factor
receptor variant III/STAT3 signaling (68), ultimately leading to poor prognosis
of HCC (62). A recent study
confirmed that S100A11 is superior to alpha fetoprotein antibody in
predicting haematogenous metastasis in patients with HCC (69). Certain S100 proteins and the key
signaling molecules can serve as promising targets for the
treatment of HCC in future, although more high-quality studies are
warranted to determine the precise molecular mechanisms.
There are increasing studies supporting the key role
of S100 protein members in PC (9,71,72).
Bachet et al (71)
demonstrated that S100A2 predicts longer disease-free and overall
survival in patients with pancreatic adenocarcinoma, suggesting a
predictive benefit of S100A2 in the adjuvant therapy of pancreatic
adenocarcinoma. By contrast, another study (9) has implicated that elevated expression
of S100A2 is related to progression and poor prognosis of patients
with PC. Moreover, a recent study has shown that S100A2 serves as a
predictive biomarker of CD8+ T and activated natural
killer (NK) cell infiltration in PC, suggesting a prognostic factor
for predicting the response to immunotherapy response in patients
with PC (72). The expression of
S100A2 is positively associated with PD-L1 and infiltration of M0
macrophages in the immune microenvironment (72). Accordingly, more studies are
warranted to elucidate the effect and mechanism of S100A2 in
regulating PC. Che et al (73) demonstrated that the expression of
S100A4 is positively associated with the differentiation grade and
metastasis of PC (71) and
promoted the PC cell proliferation, angiogenesis, invasion, and
progression. High expression of S100A4 leads to poor
differentiation of PC by inducing hypomethylation of the
corresponding intron (74). In
addition, expression of S100A4 is positively associated with the
serum levels of CA19.9, an important prognostic factor for PC
(75). Accordingly, S100A4 is a
tumor promoter in PC but its precise molecular mechanism remains
unclear. It has been well documented that the expression of S100A11
is increased in multiple types of cancers, including lung (76) and thyroid cancer (77). A previous study demonstrated
elevated expression of S100A11 in PC, which also predicts poor
cancer prognosis (78). Similar
findings have also been demonstrated in subsequent studies
(79–81). S100A11 promotes pancreatic
carcinogenesis by enhancing expression, phosphorylation and
activation of AKT, upregulating P21 and facilitating the transition
of G0/G1 cell cycle through the PI3K/AKT signaling pathway in
cancer cells (80). Moreover,
S100A11 can also function as a PC promoter by facilitating the
spread of fibroblast population and promoting cancer progression
via the RAGE/MyD88/mTOR/p70 signaling pathway (81). As a result, S100A11 may serve as a
promising therapeutic target due to the key modifying effects in
regulating PC. Increasing evidence has demonstrated the altered
expression of S100A14 in multiple malignant tumors, such as LC,
breast cancer and CRC (82–85).
Elevated expression of S100A14 has also been reported in several
publications (83–85). Zhuang et al (84) demonstrated that the overexpression
of S100A14 promotes the proliferation, migration and invasion of PC
cells by adhering to Ras and inhibiting CD8+ T cell
infiltration and cytolytic activity. S100A14 is found to inhibit
the activation of CD8+T cells by enhancing the
expression of PD-L1, which affects the immunotherapy response of
patients with PC (85).
Accordingly, S100A14 is also a PC promoter and prognostic
predictor. Fang et al (86)
demonstrated that S100A16 promotes PC progression by enhancing the
expression of FGF19 via the AKT/ERK1/2 signaling pathway. Besides,
S100A16 plays a critical role in regulating cancer immunity in PC,
affecting the function of CD8+ T, dendritic and NK cells
by inhibiting the activation of JAK/STAT signaling (87). S100A16 induces EMT by enhancing
TWIST expression and activating the STAT3 signaling pathway
(87). Moreover, the anti-tumor
effect of gemcitabine is augmented following inhibition of S100A16
(88). Therefore, elevated
expression of S100A16 predicts poor overall survival of patients
with PC (89,90). Taken together, S100 family members
are potential biomarkers for PC diagnosis, treatment and prognosis,
particularly S100A4, S100A11, S100A14 and S100A16. Nonetheless, the
underlying mechanisms of S100 family in PC warrant more studies
with high quality.
CRC is one of the most common types of
gastrointestinal cancer and has unclear etiology and pathogenesis
(91). It is the fourth most
common cause of cancer-related death worldwide after lung cancer,
LC and GC (92). It is urgent to
identify novel strategies for the early diagnosis and treatment of
CRC.
Taken together, S100 family members are involved in
the pathogenesis of CRC, particularly S100A2, S100A4, S100A8,
S100A14 and S100A16. They may serve as useful therapeutic targets
for CRC but the underlying mechanisms need to be elucidated in
future.
S100A7 is an ideal diagnostic marker for oral
potentially malignant disorders (OPMDs) and oral squamous cell
carcinoma (OSCC) (114). The
disease-free survival of patients with esophageal squamous cell
carcinoma (ESCC) with higher expression of S100A8/A9 is shorter
(115). Besides, S100A8/A9
promotes migration and invasion of ESCC cells via Akt/p38 signaling
(115), suggesting a pivotal role
of S100A8/A9 in ESCC progression and prognosis. Moreover,
extracellular S100A14 enhances the proliferation and survival of
ESCC cells via interacting with RAGE and activating MAP and NF-κB
pathways (25). Accordingly, S100
family members S100A7, S100A8/A9 and S100A14 may serve as useful
markers for the diagnosis and treatment of oral cancer and EC.
To date, there is no effective strategy for the
early diagnosis of most types of cancer. It is urgent to identify
novel makers for early screening and effective treatment of
digestive tract cancers due to the rising incidence and
cancer-associated mortality. Tumor-targeted therapy, which
selectively kills cancer cells while sparing healthy cells, has
garnered significant attention in recent years (103,116). Molecular targeted therapy, also
known as a ‘biological missile’, has emerged as a key focus in
cancer research. The S100 protein has been identified as a highly
promising biological target in recent studies (88,117). S100 protein family has been
demonstrated to participate in regulating inflammation, immunity,
tissue repair and tumorigenesis. Most importantly, certain S100
family members (such as S100A4, S100A8/9, S100A11, S100A14, and
S100A16) have shown potential for the molecular diagnosis,
progression monitoring and prognostic prediction of digestive tract
cancer. These proteins are involved in regulating tumor
proliferation, metastasis, angiogenesis and immune evasion,
although the precise mechanisms are elusive (118–121). Thus, elucidating the effects and
potential mechanisms of S100 proteins in digestive tract cancer may
facilitate the identification of novel targets for targeted
therapy. Future studies should focus on validation of
cancer-specific S100 proteins as biomarkers for early detection,
anti-tumor targets and prognostic prediction. S100 family members
hold promise as potential targets for the diagnosis and targeted
therapy of digestive tract cancer.
Not applicable.
The present study was supported by National Natural Science
Foundation (grant nos. 82003042 and 82171790) and Natural Science
Foundation of Shandong Province, China (grant no. ZR2020KC001).
Not applicable.
ML, DX and SY wrote and revised the manuscript. SJ,
BC, PC, WD, HZ, SY, DX and YS collected the data and constructed
tables and figures. ML and SY confirm the authenticity of all the
raw data. All authors have read and approved the final
manuscript.
Not applicable.
Not applicable.
The authors declare that they have no competing
interests.
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