bioRxiv Science⌕ Search

Biology subjects

Boonekamp, K. E.

Publications and source records attributed to Boonekamp, K. E..

7 recordsLinked to original sources

WNT-driven immune evasion promotes malignant transformation of BRAF-mutant colorectal cancer

BRAF-mutant colorectal cancer (CRC) constitutes a molecularly and clinically distinct subtype with poor prognosis and resistance to standard therapies, representing a major unmet clinical need. Arising from the serrated pathway of colorectal carcinogenesis rather than the classical adenoma-carcinoma sequence, this subgroup remains relatively understudied yet displays a more aggressive disease course. To investigate the progression of serrated CRC, we generated multiple genetically engineered mouse models (GEMMs) of BRAF-mutant, microsatellite-stable (MSS) CRC that closely recapitulate human disease. Our findings demonstrate that WNT-pathway activation via APC- or CTNNB1-mutations, but not RNF43-loss, initiates serrated CRC by suppressing immune-mediated tumor surveillance. Mechanistically, WNT-signaling drives distinct alterations in T cell phenotypes within the tumor microenvironment, enabling tumor progression. Together, these data indicate that WNT-signaling mediates immune escape during the malignant transformation of BRAF-mutant CRC.

cancer biology↗

Fully three-dimensional force inference in intestinal organoids reveals ratchet-like bud stabilization

The intestinal epithelium in vertebrates has a characteristic arrangement of protruding villi and receding crypts, which are generated and stabilized by selforganized cell forces. Intestinal organoids recapitulate this development and can be used to shed light on the underlying mechanical processes. Here we combine advanced image processing and the bubbly vertex model for epithelial cell shape to achieve a fully three-dimensional reconstruction of cell shapes, forces and tissue geometries during the development of mouse intestinal organoids. We show that the transition from spherical to budded morphologies is caused by a global increase in tension at the inner side and a decrease in luminal pressure, which however are not maintained after budding, suggesting ratchet-like non-reversibility. Through computer simulations of a vertex model for growing tissue with T1-transitions and comparison with the experimental data, we show that this ratchet is likely of geometrical origin. We further find that the system is mechanically stabilized on the outer side by increases in line tensions and reorganization of the actomyosin network, stabilizing a polygonal organization that also seems to enforce the geometrical ratchet. Our approach demonstrates how one can achieve a complete mechanical analysis of a complex tissue-like system.

biophysics↗

Molecular recording of cellular protein kinase activity with chemical labeling

Protein kinases control most cellular processes and aberrant kinase activity is involved in numerous diseases. To investigate the link between specific kinase activities and cellular phenotypes in heterogeneous cell populations and in vivo, we introduce molecular recorders of kinase activities for later analysis. Based on split-HaloTag and a phosphorylation-dependent molecular switch, our recorders become rapidly labeled in the presence of a specific kinase activity and a fluorescent HaloTag substrate. The kinase activity in a given cell controls the degree of fluorescent labeling whereas the recording window is set by the presence of the fluorescent substrate. We have designed specific recorders for four protein kinases, including protein kinase A. We apply our protein kinase A recorder for the sorting of heterogeneous cell populations and subsequent transcriptome analysis, in genome-wide CRISPR screens to discover regulators of PKA activity and for the tracking of neuromodulation in freely moving mice.

biochemistry↗

An organoid platform reveals MEK-PARP co-targeting to enhance radiation response in rectal cancer

Locally advanced rectal cancer is usually treated by neoadjuvant chemoradiotherapy. However, tumor response rates to this treatment vary greatly. Thus, most patients do not reach a complete remission and have to undergo tumor resection. In the present study, we introduce a patient-derived rectal cancer organoid platform that reflects clinical radiosensitivity and use this to screen 1596 drug-radiation combinations. We identify inhibitors of RAS-MAPK signaling, especially MEK inhibitors, strongly synergizing with radiation response. Mechanistically, MEK inhibitors suppressed radiation-induced activation of RAS-MAPK signaling, and selectively downregulated the homologous recombination DNA repair pathway component RAD51, thereby achieving radio-enhancement. Through testing drug-drug-radiation combinations in organoids and cell lines, we identified synergism between PARP and MEK inhibitors to further enhance the effect of radiation. Our data support clinical testing of combined MEK and PARP inhibition with radiotherapy in locally advanced rectal cancers. Graphical Abstract O_FIG O_LINKSMALLFIG WIDTH=200 HEIGHT=82 SRC="FIGDIR/small/597640v1_ufig1.gif" ALT="Figure 1"> View larger version (34K): org.highwire.dtl.DTLVardef@1d77d62org.highwire.dtl.DTLVardef@68b928org.highwire.dtl.DTLVardef@154142eorg.highwire.dtl.DTLVardef@f8f462_HPS_FORMAT_FIGEXP M_FIG C_FIG

cancer biology↗

Restraining Wnt activation and intestinal tumorigenesis by a Rab35 dependent GTPase relay

Maintenance of homeostatic processes ensure curtailment of intestinal tumorigenesis. Inactivating mutations to Adenomatous Polyposis Coli (Apc) result in aberrantly activated Wnt signalling and initiates colorectal cancer (CRC) in approx. 80% of cases, yet our understanding of the subcellular mechanisms that modulate dysregulated pathway activity is limited. Here, using a conditional in vivo genetic screen, we identify Rab35 GTPase as a novel tumour suppressor that modulates regional Wnt activity after loss of Apc in progenitor cells. Single cell analysis revealed that progenitor cells respond to Apc depletion by increasing the expression of a GTPase activating protein, which we named blackbelt, and triggering Rab35 disassociation from the plasma membrane. Mechanistically, we demonstrate that Rab35 controls the localisation and activation of the Rho GTPase, Cdc42, which functions as a relay to regulate JNK signalling. This in turn tunes the Wnt pathway upstream of {beta}-catenin to direct proliferation and differentiation of progenitor cells. Importantly, we show that maintaining active JNK signalling is important for the propagation of Apc mutant mouse colon organoids. Our findings highlight a novel GTPase cascade that sustains aberrant Wnt activity in specific segments of the intestine and provides impetus to therapeutically exploit this pathway to target CRC.

cancer biology↗

RNF43 truncating mutations mediate a tumour suppressor-to-oncogene switch to drive niche-independent self-renewal in cancer

Wnt/{beta}-catenin signalling is a primary pathway for stem cell maintenance during tissue renewal and a frequent target for mutations in cancer. Impaired Wnt receptor endocytosis due to loss of the ubiquitin ligase RNF43 gives rise to Wnt-hypersensitive tumours that are susceptible to anti-Wnt-based therapy. Contrary to this paradigm, we identify a class of RNF43 truncating cancer mutations that strongly induce {beta}-catenin-mediated transcription, despite exhibiting retained Wnt receptor downregulating activity. Mechanistically, these RNF43 mutants trap Casein Kinase (CK)1 at the plasma membrane, which prevents {beta}-catenin turnover and propels ligand-independent Wnt target gene transcription. When introduced in human colon stem cells, these oncogenic RNF43 mutants cooperate with p53 loss to drive a niche-independent program for self-renewal and proliferation. Importantly, onco-RNF43 mutations, unlike conventional LOF RNF43 mutations, confer resistance to anti-Wnt-based therapy. Our data demonstrate the relevance of studying patient-derived mutations for understanding disease mechanisms and improved applications of precision medicine.

cancer biology↗

Modelling cancer immunomodulation using epithelial organoid cultures

Here we utilize organoid technology to study immune-cancer interactions and assess immunomodulation by colorectal cancer (CRC). Transcriptional profiling and flow cytometry revealed that organoids maintain differential expression of immunomodulatory molecules present in primary tumours. Finally, we established a method to model antigen-specific epithelial cell killing and cancer immunomodulation in vitro using CRC organoids co-cultured with cytotoxic T cells (CTLs).

cancer biology↗