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Graph summarizes results from three independent sets of experiments with over organoids counted for each experiment. P value t-test, two tailed : N. We monitored expression of transcription factors that are expressed in a cell type-specific manner within the pancreas Fig. We next analyzed expression of these markers by immunofluorescence. PDX1 protein expression was heterogeneous within each organoid Fig.
Our conditions promoted exocrine lineage specification as determined by a 3. Next we examined if the organoids express markers associated with differentiated acinar, ductal or islet cells. Henceforth, we refer to these structures as progenitor organoids. Transplants were identified in 20 out of 22 glands analyzed. We also tested if the mouse mammary gland fat pad, which is known to support growth of pancreatic islets 16 , would induce differentiation of progenitor organoids into pancreatic exocrine structures.
Organoid transplants lacked NKX6. Differentiated pancreatic ducts or islets, but not acini, are known to have primary cilia Thus, progenitor organoids can generate outgrowths with molecular and morphological characteristics of human fetal exocrine pancreas. KRAS G12V -expressing organoids showed cystic organization with apically positioned nuclei and morphology consistent with early pancreatic tumor lesions Fig. Thus, both in culture and in vivo , progenitor organoids can serve as models for investigating early stages of transformation.
In breast cancer, cytoplasmic SOX9 is a marker of poor prognosis 21 , Insets represent high-resolution images of representative organoids. Graph summarizes results from three independent sets of experiments with over 50 structures counted in each experiment. Samples with different SOX9 status scored for TP53 mutation status and expressed as percentage lower panel.
WT refers to Wild type. As PDAC originates from the exocrine lineage, we reasoned that our culture conditions may be adapted for growing primary pancreatic tumors.
Twenty primary tumor samples obtained from surgical resections under institutionally approved research ethics protocols were used to establish organoid cultures and patient consents were obtained. Time-lapse analysis of UHN6 culture every 45 minutes for 10 days Fig.
We analyzed the histoarchitecture and differentiation status of the tumor organoids after 16 days. Tumor organoids retained similar morphological and cytological features as the primary tumors they were derived from Fig.
None of the tumors or organoids expressed islet NKX6. Results were normalized to vehicle-treated organoids. To determine whether tumor organoids can be serially passaged and form tumors in vivo , we analyzed organoid forming efficiencies and growth rates from three PDAC patients. All samples effectively established serial cultures and maintained similar growth rates during assay periods Supplementary Fig. To test whether the tumor organoids can generate tumors in xenograft models, we subcutaneously injected 50, cells from two independent organoid cultures Supplementary Fig.
All injections resulted in tumor growth within 4—7 weeks. The xenograft tumors maintained the histoarchitectures present in the primary tumors from which the organoids were derived and can be used to re-establish organoid cultures Supplementary Fig. Carcinomas display intratumoral spatial histological heterogeneity 23 , which was maintained in our tumor organoid system.
For example, a primary PDAC showing two distinct populations of invasive glands, composed of larger tall columnar cells with cleared granular cytoplasm or smaller cuboidal cells with deeply eosinophilic cytoplasm, generated organoids recapitulating these morphologically distinct populations Fig.
Thus, we demonstrate that tumor organoids conserve histological organization, differentiation status and morphologic heterogeneity observed in primary PDACs, a property we refer to as histostasis.
Large-scale genomics studies demonstrate patient-specific variations in genetic and epigenetic changes, highlighting the need to use fresh patient tumor material to evaluate or discover new therapies that can be administered on a personalized basis As all patients underwent surgery within the past five months and are currently alive without evidence of disease, we cannot relate organoid response to gemcitabine with patient outcome.
We next tested the five tumor organoid models against drugs targeting epigenetic regulators. Tumor organoids were treated with A and UNC alone or in combination with gemcitabine. While tumor organoids were insensitive to A Supplementary Fig. Recent studies reveal a relationship between oxygenation and H3K27me3 epigenetic mark regulation 25 , Furthermore, cells contributing to PDAC tumor relapse show increased oxidative phosphorylation dependence We measured basal respiration rates to investigate differences in tumor organoid oxygen consumption.
Thus tumor organoids retain patient-specific traits including repressive epigenetic marks, oxygen consumption and EZH2 dependence, highlighting the utility of this system for drug screening.
We report conditions for inducing human PSC differentiation to pancreatic exocrine lineage organoids and use these organoids to obtain clinically relevant insights to PDAC. We also adapt the approach for establishing and propagating primary PDAC tumors as organoids that maintain tumor-specific traits and show differential responses to novel therapeutic drugs.
Previous reports have used mouse pancreas tissue progenitors to develop organoid cultures of ductal cells, which can be manipulated and transplanted in-vivo 4 — 6 , We report conditions for differentiation of human PSCs towards exocrine lineage in culture and in vivo.
Further studies using this model will facilitate a better understanding of human pancreatic exocrine differentiation, which has implications for regenerative medicine. Progenitor organoids can identify genotype-phenotype relationships in PDAC. Although the mechanistic relationship between TP53 and SOX9 localization remains unknown, it highlights the utility of progenitor organoids.
Although this model can provide insights into early lesions, our KRAS G12V -induced lesions do not contain luminal space, precluding an evaluation of changes in nuclei position associated with PanINs. A recent study reported a method to establish tumor organoids that have histological features consistent with low-grade PanINs, despite being derived from adenocarcinoma In contrast, our conditions promote histostasis where the organoids conserve inter-patient variation in tumor histoarchitecture, and maintain the differentiation status observed in the matched primary tumor.
PDAC organoids have been used for Omics approaches to compare mouse and human tumors to gain insights We demonstrate the use of clonally-derived organoids to identify patient-specific sensitivities to novel therapeutic agents.
Organoids from different patients showed differential sensitivity to EZH2 inhibition, which correlated with H3K27me3 in both tumor organoids and matched patient tumor. The relatively short time required to establish organoid cultures from the time of surgery 21—45 days minimizes culture-induced genetic drift and is hence likely to better represent the primary tumor than established cell-lines.
This suggests organoids may be used to predict clinical response and for personalized cancer treatment. Human embryonic stem cell hESC -derived pancreatic progenitors were generated in a monolayer format using a modification of our previously described staged differentiation protocol 30 , Stem cells were regularly tested to be mycoplasma free using MycoAlert Lonza. Stanley and A. The cells were plated on a bed of Matrigel as described before Tumor cells were then seeded in 3D culture chambers as described above.
Culture media were replaced every 4 days. For serial passaging of organoids, day 16 organoids were treated with collagenase for 2 hours then further dissociated with trypsin for 10—30 minutes. Cells were collected and re-seeded in 3D culture following protocols as described above.
Lentiviruses were packaged using a third generation packaging system and pseudotyped with RabbiesG Addgene, in T cells. Concentrated virus was used to infect pluripotent progenitors grown on a thin layer of Matrigel in PTOM and subsequently replated in 3D, as outlined above.
Progenitor cells and primary tumor cells were seeded in 3D as described above and epigenetic inhibitors or DMSO were added to 3D culture at day 1. At day 8, cell growth was analyzed using CellTiter 96 non-radioactive cell proliferation assay Promega, G In brief, cells were seeded to each matrigel coated well of an XF e 96 cell culture plate. At day 8, basal oxygen consumption rates were measured and values normalized to fluorescence intensity readings, obtained from CyQUANT Thermo-Scientific cell proliferation assays conducted on the XF e 96 cell culture plate.
Tumor organoids and patient primary tumors were compared by two clinical pathologists blindly. Patient tissue microarrays were analyzed by two clinical pathology groups.
Patients who underwent curative surgical resection of histologically confirmed pancreatic adenocarcinoma who provided consent to tissue and molecular research were included in the study.
Patients were excluded if they had been lost to follow-up or died within 90 days of their surgical resection. Staging, clinical, surgical pathologic and treatment data were retrospectively extracted from a prospectively maintained database. Univariate and multivariate comparisons of disease-free and overall survival were assessed using the Kaplan-Meier method by Log-rank and Cox-proportional Hazards models, respectively. Alexa fluorophore labeled secondary antibodies for corresponding primary antibodies were purchased from Life Technologies and used at Confocal images were acquired with the Olympus FluoView system.
For all experiments, three independent experiments were conducts with over 50 structures evaluated in each experiment to ensure well representation as we regularly performed in our lab. Time-series images were processed to concatenate and align time-series stacks using ImageJ. Edges of organoids in images were further enhanced by Sobel method and dark holes were suppressed.
Ki67 staining analysis was done using CellProfiler. Then the total cell nuclei area and Ki67 staining area were calculated for each organoid and exported to a spreadsheet. Equals 1 for a perfectly circular object. Adult pancreas RNAs were purchased from Clontech Fetal tissue RNAs were purchased from Biochain www. RNAs of 3D cultured organoids or cells lines were obtained using Trizol extraction following a previously published method Array hybridization was done following a standard Illumina expression array protocol starting with high quality total RNA from each of the samples.
RNA was quantified using Agilent Bioanalyzer before processing to prepare for array hybridization. In brief, hybridization protocol features first and second-strand reverse transcription steps, followed by in vitro transcription amplification that incorporates biotin-labelled nucleotides, array hybridization, washing, blocking, streptavidin-Cy3 staining and scanning using iScan. All the probes with a detection P value less than 0.
If a gene was represented by more than one probe, mean expression values of all those probes were used to represent the expression level of that gene. Hierarchical clustering of expression levels of all genes based on Euclidean distance. Three technical replicates of three biological replicates were used as empirically done. The primers for PCR are listed as following:.
Standard animal care was provided during and after surgery, following the animal user protocol approved by the Animal Care Committee at UHN. Growth of transplants was monitored every week from four weeks after injection. No randomization was used but analyses were conducted in a blinded manner by three separate investigators. For monitoring in vivo tumorigenesis of progenitor organoid expressing oncogenes, progenitors were lentivirally-transduced and cultured in 3D for 16 days as described above.
Then progenitor organoids were injected into mouse mammary gland and monitored as outlined above. Passage 3 tumor organoids were cultured in 3D for 16 days then isolated and dissociated by enzymatic digestion. Both flanks of mice were injected and standard animal cares were provided during and after surgery.
Growth of transplants was monitored every week from two weeks after injection. Xenograft tumors were isolated 4—7 weeks after injection and reseeded in 3D following the protocol described above.
Organoid size and shape measurements were analyzed using t-test with Graphpad Prism program. Patient survival data were analyzed using a univariate Cox proportional hazards model with R program. We thank members of the Muthuswamy laboratory for helpful suggestions and discussions.
Dalia Barsyte-Lovejoy for helping with epigenetic drug screening experiments and members of the PanCuRx team including Dr. David Hedley for their support and assistance. Read article at publisher’s site DOI : Nat Commun , 13 1 , 19 Apr Nat Commun , 13 1 , 21 Apr Mutagenesis , 37 2 , 01 May Nat Methods , 19 4 , 08 Apr Cited by: 0 articles PMID: Nat Cell Biol , 24 3 , 15 Mar This data has been text mined from the article, or deposited into data resources.
To arrive at the top five similar articles we use a word-weighted algorithm to compare words from the Title and Abstract of each citation. Nat Med , 21 11 , 01 Nov Cohen Aquaculture Evidentiary Documents.
Miller-Saunders to S. Riddell to A. Exhibit — Krkosek et al, Dynamics of outbreak and control of salmon lice on two salmon farms in the Broughton Archipelago, BC — CAN September 1, — for a full listing of exhibits, click September 1st at this link on the Cohen Commission website. Hargreaves etal, Re: Urgent-science budget impacts, Jun 16 — CAN August 31, — for a full listing of exhibits, click August 31st at this link on the Cohen Commission website. Fowler to S. Ford to A. Sugiyama, M.
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An experimental design to detect differences of by-catch rates in surface and subsurface driftnets in North Pacific squid driftnet fisheries L. Kato, and K. II—Oceanographic data H.