Targeting galectin-1 inhibits pancreatic cancer progression by modulating tumor-stroma crosstalk

Proc Natl Acad Sci U S A 2018 AI 6 Explanations View Original
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Page [1, 2]
The Dense Shield Around Pancreatic Tumors

Pancreatic ductal adenocarcinoma (PDAC) is surrounded by an unusually thick layer of non-cancerous tissue called the tumor stroma. This fibrous, cellular microenvironment -- which can make up more than 80% of the tumor's total volume -- is generated mainly by specialized cells called pancreatic stellate cells (PSCs) that become activated in the presence of the tumor.

The stroma was once considered a passive barrier, but research over the past decade has shown it actively promotes tumor growth and blocks immune attack. It supplies survival signals to cancer cells, fuels the growth of new blood vessels that feed the tumor, excludes cancer-killing T-cells, and physically impedes drug delivery. This makes the stroma not just a bystander but an essential partner in the cancer's growth and resistance to treatment.

This study identified galectin-1 (Gal1), a sugar-binding protein, as one of the key molecules mediating the tumor-promoting effects of the stroma, and investigated whether blocking Gal1 could slow cancer progression.

TL;DR: Pancreatic tumors are encased in a dense, protective stroma that actively helps cancer grow and resist treatment; this study found that a protein called galectin-1 is a key driver of that tumor-stroma partnership.
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What Is Galectin-1 and Why Is It Suspicious?

Galectin-1 (Gal1) is a member of a family of proteins that bind to specific sugar chains (galactosides) found on the surface of many cell types. It plays roles in cell adhesion, immune regulation, and tissue remodeling. While Gal1 is expressed at low levels in many normal tissues, it is significantly overexpressed in several cancers -- including pancreatic cancer -- particularly in the stromal cells surrounding the tumor.

Analysis of human PDAC tissue confirmed that Gal1 is highly expressed in pancreatic stellate cells within the tumor stroma, and that this high expression correlates with poor patient outcomes. This pattern suggested that Gal1 from stromal cells might be sending pro-tumor signals to cancer cells or protecting the tumor from immune attack, rather than simply being a passive marker of disease.

Previous work in other cancer types had linked Gal1 to T-cell suppression -- specifically, to the killing of activated T-cells that would otherwise attack tumors. If Gal1 in pancreatic cancer stroma performs the same function, blocking it could simultaneously reduce tumor-promoting signals and restore immune surveillance.

TL;DR: Galectin-1 is a sugar-binding protein that is highly overexpressed in the cells surrounding pancreatic tumors and correlates with poor survival, suggesting it plays an active role in helping cancer survive.
Pages 4-4
Testing Gal1 Deletion in a Genetically Engineered Mouse Model

To test whether Gal1 is functionally important in PDAC progression, the researchers used a genetically engineered mouse model called Ela-KrasG12V p53-/-, which spontaneously develops pancreatic tumors driven by two mutations common in human PDAC (activated Kras and loss of p53). These mice were crossed with mice lacking the Gal1 gene, producing animals that develop pancreatic cancer without the Gal1 protein.

The experimental design allowed a clean comparison: pancreatic cancer in mice with normal Gal1 versus mice lacking Gal1, in an otherwise identical genetic background. Comparing tumor growth, spread, stromal characteristics, immune infiltration, and overall survival between these groups revealed the specific contribution of Gal1 to disease progression.

Complementary experiments used human pancreatic stellate cells (HPSCs) cultured in the laboratory and treated with Gal1 or with Gal1-blocking antibodies. Measuring how cancer cell behavior changed in response to stellate cell conditioned media -- the signals secreted by those cells -- helped identify the specific cellular mechanisms through which Gal1 exerts its effects.

TL;DR: Mice engineered to develop pancreatic cancer without the Gal1 gene were compared to mice with normal Gal1, revealing exactly what Gal1 contributes to tumor growth and immune evasion.
Pages 6-6
Deleting Gal1 Extended Survival and Reduced Tumor Progression

Mice lacking Gal1 showed a 22.3% increase in median survival compared to Gal1-intact controls -- a substantial and statistically significant improvement for an aggressive cancer model. This survival benefit was accompanied by smaller tumor volumes, reduced stromal density, and lower rates of metastasis to the liver and lungs, indicating that Gal1 deletion impairs multiple aspects of pancreatic cancer progression simultaneously.

Tumors in Gal1-deficient mice had fewer activated pancreatic stellate cells and less deposition of collagen and fibronectin, the extracellular matrix proteins that form the physical scaffold of the stroma. A less dense stroma is both a sign of reduced tumor-stromal crosstalk and a functionally significant change because it may improve drug delivery by reducing the physical barriers to therapeutic penetration.

Angiogenesis -- the formation of new blood vessels to feed the tumor -- was also reduced in Gal1-deficient tumors. Fewer and smaller blood vessels were present, and expression of vascular endothelial growth factor (VEGF), the primary driver of tumor angiogenesis, was lower. This suggests Gal1 in the stroma promotes tumor vascularization, providing the cancer with oxygen and nutrients needed for rapid growth.

TL;DR: Removing Gal1 extended mouse survival by 22%, reduced stroma formation, lowered angiogenesis, and decreased metastasis -- confirming that Gal1 drives multiple aspects of pancreatic cancer progression.
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Gal1 Suppresses Anti-Tumor Immunity

One of the most striking findings was that Gal1 deletion dramatically changed the immune landscape within pancreatic tumors. Tumors from Gal1-deficient mice showed a significant increase in tumor-infiltrating T-cells, including both CD4+ helper T-cells and CD8+ cytotoxic T-cells that can directly kill cancer cells. The immunosuppressive, T-cell-excluding environment characteristic of PDAC was substantially reversed.

Mechanistically, Gal1 secreted by stellate cells was shown to kill activated T-cells directly by binding to sugar chains on their surface and triggering programmed cell death (apoptosis). This provides a molecular explanation for how the stroma shields pancreatic tumors from immune attack: Gal1 acts as an invisible barrier that destroys T-cells before they can reach and kill cancer cells.

Importantly, Gal1 blockade also reduced the number of immunosuppressive regulatory T-cells (Tregs) within the tumor, which normally dampen immune responses and help tumors evade immune surveillance. The combined effect of more cytotoxic T-cells and fewer regulatory T-cells represents a shift toward an immune-permissive environment that could make tumors more susceptible to immunotherapy.

TL;DR: Gal1 from stromal cells actively kills anti-tumor T-cells and promotes immunosuppressive cells in the tumor, explaining why pancreatic tumors are so resistant to immune attack.
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Gal1 as a Therapeutic Target: Potential for Combination with Immunotherapy

Pancreatic cancer has been notoriously resistant to immune checkpoint inhibitors -- drugs like pembrolizumab and nivolumab that have transformed treatment in melanoma and lung cancer. The prevailing explanation is that PDAC's dense stroma prevents T-cells from entering the tumor in the first place, making checkpoint blockade ineffective. Gal1 inhibition could address this by remodeling the stroma and allowing T-cells to accumulate within tumors.

The findings suggest that combining a Gal1 inhibitor with a checkpoint inhibitor could be synergistic: the Gal1 inhibitor opens up immune access to the tumor while the checkpoint inhibitor prevents T-cells from being subsequently deactivated by other suppressive signals. This combination strategy is the basis for planned clinical investigations.

Several Gal1-targeting agents have been developed, including monoclonal antibodies and small molecule inhibitors. The data from this study provide a strong biological rationale for advancing these agents into clinical trials for pancreatic cancer, particularly in combination with immunotherapy. The 22.3% survival improvement in mice with Gal1 deletion alone suggests that even monotherapy could provide meaningful benefit.

TL;DR: Blocking Gal1 could overcome pancreatic cancer's resistance to immunotherapy by remodeling the stroma and allowing T-cells to enter tumors, making Gal1 inhibitors a promising target for clinical development.
Citation: Open Access, 2018. Available at: PMC5910865.