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Diegel, C. R.

Publications and source records attributed to Diegel, C. R..

6 recordsLinked to original sources

Deletion of the Wnt regulator Znrf3 alters bone geometry without inducing high bone mass

RNF43 and ZNRF3 are transmembrane E3 ubiquitin ligases that negatively regulate Wnt signaling by promoting ubiquitination and degradation of Frizzled receptors. Loss of either gene enhances Wnt/{beta}-catenin signaling and has been linked to tumorigenesis. Wnt signaling is a key regulator of skeletal development and bone homeostasis, and pharmacologic activation of this pathway is an established therapy for osteoporosis. In Xenopus laevis, simultaneous disruption of rnf43 and znrf3 results in supernumerary limb formation; however, their roles in mammalian limb development and skeletal maintenance remain unclear. We demonstrate that mice homozygous for null alleles of both Rnf43 and Znrf3 do not develop supernumerary limbs. Because activation of Wnt/{beta}-catenin signaling in osteoblasts increases bone mass, we hypothesized that osteoblast-specific deletion of Rnf43 and/or Znrf3 would produce a high-bone-mass phenotype. Instead, osteoblast-specific loss of Znrf3 resulted in age-and sex-dependent reductions in trabecular bone mass, characterized by decreased bone mineral density and bone volume fraction, reduced trabecular number, and increased trabecular separation. Cortical bone exhibited increased cross-sectional size with reduced cortical area fraction and altered structural properties, while tissue mineral density was unchanged. In contrast, deletion of Rnf43 had minimal skeletal effects, and combined deletion of both genes did not exacerbate the phenotype observed with loss of Znrf3 alone. These findings identify Znrf3 as the dominant functional paralog regulating bone architecture in mature osteoblasts and underscore the importance of evaluating skeletal geometry when modulating upstream Wnt regulators.

developmental biology↗

Frizzled 6 Drives EMT and Stromal Remodeling Downstream of SP1 in Basal-like Pancreatic Cancer

Pancreatic ductal adenocarcinoma (PDAC) is a highly lethal malignancy, in part due to its rapid progression and early metastasis. To uncover novel drivers of this aggressive behavior, we first analyzed Frizzled receptor expression in human PDAC datasets and identified Frizzled 6 (FZD6) as uniquely predictive of poor clinical outcomes among all ten Frizzled family members. High FZD6 expression correlated with significantly worse overall survival for PDAC patients of any age. Functional studies in human PDAC cell lines showed that FZD6 promotes mesenchymal phenotypes, including enhanced migration and growth in 3D culture, while FZD6 loss induces E-cadherin expression and impairs motility without affecting 2D proliferation. In vivo, conditional epithelial deletion of Fzd6 in KPC mice significantly extended survival, reduced tumor burden and metastasis, and remodeled the tumor microenvironment to suppress stromal activation. Single-cell RNA sequencing analysis of human and mouse PDAC tumors confirms that FZD6 is primarily found within the tumor cells and FZD6-activating, noncanonical Wnt ligands are found to be produced by the cancer-associated fibroblasts surrounding the tumors. Mechanistically, we found that FZD6 is a transcriptional target of specificity protein 1 (SP1), a factor upregulated in mutant p53 contexts and within basal-like PDAC subtypes. SP1 knockdown reduced FZD6 expression and signaling through the PCP pathway. Furthermore, reduced SP1 impaired cell motility. Together this implicates the SP1-Fzd6-Wnt/PCP axis as a key driver of epithelial plasticity and disease progression. These findings suggest that FZD6 is a central effector of mutant p53-driven EMT, and a promising therapeutic target in metastatic PDAC.

cancer biology↗

Structure and Function of the Retina of Low-density Lipoprotein Receptor-related Protein 5 (Lrp5)-deficient Rats

Loss-of-function mutations in the Wnt co-receptor, low-density lipoprotein receptor-related protein 5 (LRP5), result in familial exudative vitreoretinopathy (FEVR), osteoporosis-pseudoglioma syndrome (OPPG), and Norrie disease. CRISPR/Cas9 gene editing was used to produce rat strains deficient in Lrp5. The purpose of this study was to validate this rat model for studies of hypovascular, exudative retinopathies. The retinal vasculature of wildtype and Lrp5 knockout rats was stained with Giffonia simplifolia isolectin B4 and imaged by fluorescence microscopy. Effects on retinal structure were investigated by histology. The integrity of the blood-retina barrier was analyzed by staining for claudin-5 and measurement of permeability to Evans blue dye. Retinas were imaged by fundus photography and SD-OCT, and electroretinograms were recorded. Lrp5 gene deletion led to sparse superficial retinal capillaries and loss of the deep and intermediate plexuses. Autofluorescent exudates were observed, correlated with absence of claudin-5 expression in superficial vessels and increased Evans blue permeability. OCT images show pathology similar to OCT of humans with FEVR, and retinal thickness is reduced by 50% compared to wild-type rats. Histology and OCT reveal that photoreceptor and outer plexiform layers are absent. The retina failed to demonstrate an ERG response. CRISPR/Cas9 gene-editing produced a predictable rat Lrp5 knockout model with extensive defects in the retinal vascular and neural structure and function. This rat model should be useful for studies of exudative retinal vascular diseases involving the Wnt and norrin pathways.

genetics↗

Generation of a New Frizzled 2 Flox Mouse Model to Clarify Its Role in Development

It is currently accepted that Wnt receptors, Frizzleds (Fzd), have high functional redundancy, making individual receptors challenging to target therapeutically. Specifically, Fzd2 is believed to be functionally redundant with Fzd1 and Fzd7, findings which were based largely on previously published global knockout mouse studies. Conversely, a Fzd2 global knockout mouse model developed by the International Mouse Phenotype Consortium (IMPC) is early embryonic lethal, suggesting Fzd2 is critical for early embryonic development. If global deletion of Fzd2 leads to early lethality, floxed models are necessary to identify tissue-specific phenotypes. We found that a previously published Fzd2 flox model does not fully delete Fzd2 function. To reconcile the contradictory findings in Fzd2 mouse models and allow for tissue-specific studies of Fzd2, we have generated a new flox model using a modified two-cell homologous recombination CRISPR approach. We demonstrated successful simultaneous insertion of two loxP sites fully surrounding the Fzd2 gene and confirmed cre-mediated recombination deletes the sequence between the loxP sites leading to a Fzd2 null allele. Preliminary studies suggest global knockouts are early embryonic lethal and full characterization of the tissue-specific effects of Fzd2 deletion is currently underway. This work suggests Fzd2 uniquely regulates development and emphasizes the importance of thorough validation of newly generated mouse models.

cell biology↗

Low-density Lipoprotein Receptor-related Protein 5 (LRP5)-deficient Rats Have Reduced Bone Mass and Abnormal Development of the Retinal Vasculature

Humans carrying homozygous loss-of-function mutations in the Wnt co-receptor LRP5 (low-density lipoprotein receptor-related protein 5) develop osteoporosis and a defective retinal vasculature known as familial exudative vitreoretinopathy (FEVR) due to disruption of the Wnt signaling pathway. The purpose of this study was to use CRISPR/Cas9-mediated gene editing to create strains of Lrp5-deficient rats and to determine whether knockout of Lrp5 resulted in phenotypes that model the bone and retina pathology in LRP5-deficient humans. Knockout of Lrp5 in rats produced low bone mass, decreased bone mineral density, and decreased bone size. The superficial retinal vasculature of Lrp5-deficient rats was sparse and disorganized, with extensive exudates and decreases in vascularized area, vessel length, and branch point density. This study showed that Lrp5 could be predictably knocked out in rats using CRISPR/Cas9, causing the expression of bone and retinal phenotypes that will be useful for studying the role of Wnt signaling in bone and retina development and for research on the treatment of osteoporosis and FEVR.

developmental biology↗

An Osteocalcin-deficient mouse strain without endocrine abnormalities

Osteocalcin (OCN), the most abundant non-collagenous protein in the bone matrix, is reported to be a bone-derived endocrine hormone with wide-ranging effects on many aspects of physiology, including glucose metabolism and male fertility. Many of these observations were made using an OCN-deficient mouse allele (Osc-) in which the 2 OCN-encoding genes in mice, Bglap and Bglap2, were deleted in ES cells by homologous recombination. Here we describe mice with a new Bglap and Bglap2 double knockout (dko) allele (Bglap/2p.Pro25fs17Ter) that was generated by CRISPR/Cas9-mediated gene editing. Mice homozygous for this new allele do not express full length Bglap or Bglap2 mRNA and have no immunodetectable OCN in their plasma. FTIR imaging of cortical and trabecular bone in these homozygous knockout animals finds alterations in the crystal size and maturity of the bone mineral, hydroxyapatite, compared to wild-type littermates; however, CT and 3-point bending tests do not find differences from wild-type littermates with respect to bone mass and strength. In contrast to the previously reported OCN-deficient mice with the Osc- allele, blood glucose levels and male fertility in the OCN-deficient mice with Bglap/2pPro25fs17Ter allele did not have significant differences from wild-type littermates. We cannot explain the absence of endocrine effects in mice with this new knockout allele. Potential explanations include effects of each mutated allele on the transcription of neighboring genes, and differences in genetic background and environment. So that our findings can be confirmed and extended by other interested investigators, we are donating this new Bglap and Bglap2 double knockout strain to The Jackson Laboratory for academic distribution.\n\nAuthor SummaryCells that make and maintain bone express proteins that function locally or systemically. The former proteins, such as type 1 collagen, affect the material properties of the skeleton while the latter proteins, such as fibroblast growth factor 23, enable the skeleton to communicate with other organ systems. Mutations that affect the functions of most bone cell expressed proteins cause diseases that have similar features in humans and other mammals, such as mice; for example, brittle bone diseases for type 1 collagen mutations and hypophosphatemic rickets for fibroblast growth factor 23 mutations.\n\nOur study focuses on another bone cell expressed protein, osteocalcin, which has been suggested to function locally to affect bone strength and systemically as hormone. Studies using osteocalcin knockout mice led other investigators to suggest endocrine roles for osteocalcin in regulating blood glucose levels, male fertility, muscle mass, brain development, behavior and cognition. We therefore decided to generate a new strain of osteocalcin knockout mice that could also be used to investigate these non-skeletal effects.\n\nTo our surprise the osteocalcin knockout mice we created do not significantly differ from wild-type mice for the 3 phenotypes we examined: bone strength, blood glucose levels, and male fertility. Our data are consistent with findings from osteocalcin knockout rats, but inconsistent with data from the original osteocalcin knockout mice. Because we do not know why our new strain of osteocalcin knockout mice fails to recapitulate phenotypes previously reported for another knockout mouse stain, we have donated our mice to a public repository so that they can be easily obtained and studied in other academic laboratories.

genetics↗