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The BCS classifies drug substances based on their water solubility and intestinal permeability, the main factors that regulate the rate and extent of oral drug absorption .
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Moreover, the BCS is widely used in the pharmaceutical industry during the processes of developing drugs and establishing their registration strategies (e.g., the biowaiver procedure in the registration process of generic drugs).
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The Caco-2 (Cancer coli-2) cell line is commonly used to assess the permeability of compounds in in vitro conditions.
[ { "end": 10, "label": "CellLine", "start": 4, "text": "Caco-2" }, { "end": 25, "label": "CellLine", "start": 12, "text": "Cancer coli-2" } ]
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Caco-2 cells were isolated from colon tissue derived from a 72-year-old in the 1970s .
[ { "end": 6, "label": "CellLine", "start": 0, "text": "Caco-2" } ]
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Differentiated Caco-2 cells exhibit similar structural and functional properties characteristic of small intestine enterocytes .
[ { "end": 21, "label": "CellLine", "start": 15, "text": "Caco-2" } ]
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Towards confluence, they begin to polarize, forming a monolayer with strong, tight junctions, apical brush borders, and microvilli.
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The differentiated Caco-2 cells express the typical digestive enzymes, membrane peptidases, and disaccharidases of the small intestine (lactase, aminopeptidase N, sucrase-isomaltase, and dipeptidylpeptidase IV) .
[ { "end": 25, "label": "CellLine", "start": 19, "text": "Caco-2" } ]
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Therefore, the European Medicines Agency (EMA) and Food and Drug Administration (FDA) have recognized the Caco-2 cell line as a reliable in vitro model for predicting the BA of drugs in the pharmaceutical industry .
[ { "end": 112, "label": "CellLine", "start": 106, "text": "Caco-2" } ]
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The Caco-2 cell line is characterized by high internal (the heterogeneity of cell subpopulations) and external variability (e.g., resulting from intra-laboratory culture methods) .
[ { "end": 10, "label": "CellLine", "start": 4, "text": "Caco-2" } ]
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Therefore, using the Caco-2 cell line in the pharmaceutical industry requires the validation of this biological model to demonstrate its suitability for the intended purposes (e.g., classification of substances into a BCS group).
[ { "end": 27, "label": "CellLine", "start": 21, "text": "Caco-2" } ]
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According to the pharmaceutical requirements, the validation of the Caco-2 cell line is based on demonstrating an appropriate rank order relationship between the experimental permeability values of established model drugs and their absorption in human subjects .
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The FDA and EMA guidelines consider the complexity and variability of biological models, thus enabling the use of individual protocols for preparing cell lines for permeability testing.
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However, to demonstrate the appropriate suitability and functionality of cultivated cell lines, the use of 25 model drugs is required for formal BCS studies.
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The pharmaceutical requirements define only the acceptance criteria for the validation of the Caco-2 cell line and do not specify the protocol for its implementation.
[ { "end": 100, "label": "CellLine", "start": 94, "text": "Caco-2" } ]
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Therefore, the aim of this study is to review the conditions for permeability studies across the Caco-2 monolayer reported in the available literature in relation to the validation guidelines established by regulatory authorities.
[ { "end": 103, "label": "CellLine", "start": 97, "text": "Caco-2" } ]
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In this review, we presented permeability tests in the Caco-2 model used for both scientific (e.g., drug absorption prediction) and regulatory purposes (e.g., formal classification of substances into a BCS group).
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Moreover, we summarized the main aspects affecting the validation process of the Caco-2 cell line, including the culture conditions, cell differentiation process, and monolayer transport conditions.
[ { "end": 87, "label": "CellLine", "start": 81, "text": "Caco-2" } ]
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According to EMA and FDA guidelines, the internal standardization of the Caco-2 cell line includes permeability studies for model compounds representing a range of in vivo human intestinal absorption, with, respectively, low (fa < 50%), moderate (fa = 50–84%), and high permeability (fa ≥ 85%).
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Additionally, permeability studies of zero-permeability markers and efflux substrates should be determined .
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The permeability experimental data for model drugs should be determined using the apparent permeability coefficient (Papp) values.
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The Papp value determines the rate of transport of the substance across the Caco-2 monolayer.
[ { "end": 82, "label": "CellLine", "start": 76, "text": "Caco-2" } ]
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According to the protocols described by Tavelin and Hubatsch , a substance is classified as a high-permeability drug if its Papp is higher than 10 × 10 cm/s.
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In turn, the low-permeability drugs are characterized by a Papp below 1.0 × 10 cm/s.
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Additionally, drugs with Papp values in the range of 1–10 × 10 are classified as moderate .
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The validation of the Caco-2 cell line should demonstrate the correlation between the experimental transport data (Papp) and human intestinal absorption (fa) of selected model drugs.
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To fully meet the pharmaceutical criteria, permeability assays of a minimum of five model drugs from each presented permeability group (25 model drugs in total) are required.
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The use of 25 model drugs during validation is intended to demonstrate the appropriate suitability and functionality of an in vitro model.
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Finally, a calibration curve should be developed showing the correlation between the obtained Papp values and the fa of selected drugs with low, moderate, and high permeability .
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The Papp values from the selected experimental Caco-2 permeability tests and the selected human absorption of all model drugs determined by the FDA and EMA are listed in Table 1.
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The pharmaceutical industry guidelines specify the model drugs that may be used during the validation of the Caco-2 cell line.
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Eleven model drugs were established for the high-permeability group and ten markers each for the moderate- and low-permeability groups.
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Additionally, five and four were set for the zero-permeability and efflux substrate groups, respectively.
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The selection of five model drugs from each permeability group to validate the Caco-2 model is independent and can be determined individually by the researcher.
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Table 1 presents selected experimental data on the permeability of model drugs with high, moderate, and low permeability.
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The high-permeability group includes model drugs with Papp values in the range of 13.0–76.7 [×10 cm/s].
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The low-permeability group includes substances with a Papp below 0.74 [×10 cm/s].
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Additionally, the moderate-permeability group includes drug models with Papp values from 1.29 to 16.0 [×10 cm/s].
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The Papp values for nine compounds of the moderate group are within the range of 1–10 × 10 cm/s.
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However, the Papp value (16.0 × 10 cm/s) of chlorpheniramine exceeds this range and indicates the high permeability of this substance .
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Although chlorpheniramine is recognized by regulatory authorities as a moderate permeable drug, the permeability data of this model compound require further investigation.
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The cytotoxicity of compounds on the Caco-2 monolayer is one of the crucial limitations of permeability assessments in in vitro conditions.
[ { "end": 43, "label": "CellLine", "start": 37, "text": "Caco-2" } ]
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The cytotoxic effect of the compound may lead to leaks within the Caco-2 monolayer or the reduction in transporter activities resulting, and thus to an underestimation of the efflux effect .
[ { "end": 72, "label": "CellLine", "start": 66, "text": "Caco-2" } ]
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Thus, before permeability studies, it is recommended to determine the effects of all exanimated compounds on the Caco-2 monolayer’s viability.
[ { "end": 119, "label": "CellLine", "start": 113, "text": "Caco-2" } ]
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The MTT test (3-(4,5-dimethyl-2-thiazolyl)-2,5-diphenyl-2H-tetrazolium bromide) is commonly used to determine an appropriate concentration of the analyzed substances in the Caco-2 cell line.
[ { "end": 179, "label": "CellLine", "start": 173, "text": "Caco-2" } ]
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The viability of Caco-2 cells exposed to the tested compound for a period of time equal to or longer than the conditions of the permeability test should be determined.
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The highest concentration of the test compounds with no cytotoxic effect on Caco-2 cells is preferred .
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A literature review showed that the results of cytotoxicity tests of compounds on the Caco-2 cell line are not presented in detail in scientific articles.
[ { "end": 92, "label": "CellLine", "start": 86, "text": "Caco-2" } ]
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The concentrations of the compounds used in permeability tests are usually reported individually for each drug (or collectively) without detailed results of their cytotoxicity on the Caco-2 cell line.
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However, several available data regarding the viability of the Caco-2 cell line exposed to the BCS model drugs are presented in Table 2.
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The concentrations of compounds in permeability tests through the Caco-2 monolayer should be determined by striking a balance between their solubility, cytotoxicity, and analytical response.
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However, in permeability studies across the Caco-2 monolayer, a wide range of concentrations from 10 to 500 µM (or higher) are used.
[ { "end": 50, "label": "CellLine", "start": 44, "text": "Caco-2" } ]
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The non-cytotoxic concentrations of model compounds on the Caco-2 monolayer presented in Table 2 are within this range.
[ { "end": 65, "label": "CellLine", "start": 59, "text": "Caco-2" } ]
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Therefore, the concentrations of the substances in the range of 10–500 µM seem appropriate to assess their cytotoxicity on the Caco-2 line to conduct further in vitro permeability studies.
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To confirm the viability of the Caco-2 monolayer after permeability tests, apoptosis assays can be additionally performed .
[ { "end": 38, "label": "CellLine", "start": 32, "text": "Caco-2" } ]
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It is common knowledge that the Caco-2 cell line is heterogeneous and contains cells with slightly different properties .
[ { "end": 38, "label": "CellLine", "start": 32, "text": "Caco-2" } ]
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Therefore, it is important to standardize the cultivation conditions of the cell line to retain its original properties.
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To minimize laboratory variability, it is recommended to use the original Caco-2 cell lines obtained from commercial banks for drug permeability testing.
[ { "end": 80, "label": "CellLine", "start": 74, "text": "Caco-2" } ]
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A summary of the commercially available Caco-2 cell lines is presented in Table 3.
[ { "end": 46, "label": "CellLine", "start": 40, "text": "Caco-2" } ]
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Caco-2 cells used in the pharmaceutical industry should be appropriately identified and confirmed as original Caco-2 cells.
[ { "end": 6, "label": "CellLine", "start": 0, "text": "Caco-2" }, { "end": 116, "label": "CellLine", "start": 110, "text": "Caco-2" } ]
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Pharmaceutical regulatory authorities may require documentation of the origin of cells and their genetic properties .
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However, the documents proving the authenticity of the Caco-2 cell line are not strictly specified and are subject to the requirements of the relevant regulatory authority.
[ { "end": 61, "label": "CellLine", "start": 55, "text": "Caco-2" } ]
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However, it is common practice to provide documents not older than three years for all continuous human cell lines.
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For the Caco-2 cell line obtained from a commercial source such as the ATCC or ECACC, relevant purchase orders or invoices may be presented for authentication.
[ { "end": 14, "label": "CellLine", "start": 8, "text": "Caco-2" } ]
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Moreover, the authenticity of the internal Caco-2 cell line can be confirmed using STR profiling (ang.
[ { "end": 49, "label": "CellLine", "start": 43, "text": "Caco-2" } ]
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short tandem repeats) .
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pharmaceutics-15-02523-t003_Table 3Table 3List of commonly used Caco-2 cell lines in permeability studies.
[ { "end": 70, "label": "CellLine", "start": 64, "text": "Caco-2" } ]
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Organization NameCaco-2 Cell Line Catalog NumberGrowth Medium [Original Protocol]Incubation ConditionsSubject of Scientific ResearchAmerican Type Culture Collection (ATCC)HTB-37™Eagle’s Minimum Essential Medium with fetal bovine serum (20% final concentration)95% Air, 5% CO2; 37 °CClassification of drug into BCS group Drug absorption prediction nutrient absorption studies Toxicity screening European Collection of Authenticated Cell Cultures (ECACC)86010202EMEM (EBSS) with 2 mM glutamine, 1% non-essential amino acids (NEAAs), and 10% fetal bovine serum (FBS)95% Air, 5% CO2; 37 °CClassification of drug into BCS group Drug absorption prediction Toxicity screening Deutsche Sammlung von Mikroorganismen und Zellkulturen (DSMZ)ACC 16980% MEM (with Earle’s salts) with 20% heat-inactivated FBS and 1× NEAA95% Air, 5% CO2; 37 °CPermeability study Nutrient absorption studies Toxicity screening List of commonly used Caco-2 cell lines in permeability studies.
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Classification of drug into BCS group Drug absorption prediction nutrient absorption studies Toxicity screening Classification of drug into BCS group Drug absorption prediction Toxicity screening Permeability study Nutrient absorption studies Toxicity screening Each of the presented Caco-2 cell lines is widely used in research related to the absorption and transport of substances through the epithelium of the small intestine.
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Therefore, the selection of the Caco-2 cell line for permeability studies depends on the researcher’s preference.
[ { "end": 38, "label": "CellLine", "start": 32, "text": "Caco-2" } ]
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However, the Caco-2 cell lines delivered from the ATTC are most frequently used in formal studies to classify substances into BCS groups.
[ { "end": 19, "label": "CellLine", "start": 13, "text": "Caco-2" } ]
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A review of the literature revealed that there are no available comparisons of the Caco-2 cell lines obtained from different cell banks in the context of the validation of this in vitro model for pharmaceutical industrial purposes.
[ { "end": 89, "label": "CellLine", "start": 83, "text": "Caco-2" } ]
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However, Yasuda et al. showed slightly different α-defensin 5 secretion levels in differentiated Caco-2 cells obtained from the ATCC and the DSMZ.
[ { "end": 103, "label": "CellLine", "start": 97, "text": "Caco-2" } ]
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However, both Caco-2 cell lines were considered models for screening healthy food components and drugs that affect α-defensin 5 secretion .
[ { "end": 20, "label": "CellLine", "start": 14, "text": "Caco-2" } ]
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A literature review showed that the composition of the culture medium for the Caco-2 cell line varies depending on the supplier, the internal culture protocol, and the purpose of the experiment.
[ { "end": 84, "label": "CellLine", "start": 78, "text": "Caco-2" } ]
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However, in general, the composition of the culture medium for the Caco-2 cell line contains the basic components necessary for the growth and maintenance of the cells in culture.
[ { "end": 73, "label": "CellLine", "start": 67, "text": "Caco-2" } ]
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Typically, Dulbecco’s Modified Eagle’s Medium (DMEM) culture medium supplemented with 10–20% fetal bovine serum (FBS) is used.
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Some culture media for the Caco-2 line may contain amino acids (1% nonessential amino acid mixture) that are essential for cell growth .
[ { "end": 33, "label": "CellLine", "start": 27, "text": "Caco-2" } ]
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To prevent infections, antibiotics are added to the media, mainly with amino acids (e.g., 2 mM L-glutamine, 100 U/mL penicillin, and 0.1 mg/mL streptomycin solution) .
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The literature’s data indicate that glutamine is an essential factor in differentiating Caco-2 cells and maintaining the intestinal barrier function.
[ { "end": 94, "label": "CellLine", "start": 88, "text": "Caco-2" } ]
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As demonstrated, glutamine maintains the transepithelial resistance of the Caco-2 monolayer and reduces its permeability .
[ { "end": 81, "label": "CellLine", "start": 75, "text": "Caco-2" } ]
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The complete culture medium is stored at 4 °C, while the medium additives are stored in small aliquots at −20 °C (to reduce freeze–thaw cycles).
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The Caco-2 cells are cultured at 37 °C in a humidified atmosphere containing 5% CO2 and 95% air .
[ { "end": 10, "label": "CellLine", "start": 4, "text": "Caco-2" } ]
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It is common laboratory practice to replace the growth medium every other day.
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Caco-2 cells are passaged when they reach approximately 80–90% confluence.
[ { "end": 6, "label": "CellLine", "start": 0, "text": "Caco-2" } ]
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Passaging the Caco-2 cells in the indicated confluence helps to keep the cells in the exponential growth phase, which is beneficial for maintaining their properties .
[ { "end": 20, "label": "CellLine", "start": 14, "text": "Caco-2" } ]
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According to the pharmaceutical requirements, internal procedures for the cultivation and maintenance of the Caco-2 cell line should be developed .
[ { "end": 115, "label": "CellLine", "start": 109, "text": "Caco-2" } ]
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Additionally, all reagents used to cultivate the Caco-2 cell line should be monitored and reported on an ongoing basis.
[ { "end": 55, "label": "CellLine", "start": 49, "text": "Caco-2" } ]
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Data should include the name of the reagent, batch/lot number, source/origin, concentration (if applicable), retest date or expiry date, and storage conditions .
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The influence of factors such as culture conditions and the number of passages on the morphology and biochemistry of the Caco-2 cell line has been reported .
[ { "end": 127, "label": "CellLine", "start": 121, "text": "Caco-2" } ]
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The Caco-2 cell line is characterized by a heterogeneous population demonstrating, e.g., different transport velocity and differentiation parameters, including shaping the brush border.
[ { "end": 10, "label": "CellLine", "start": 4, "text": "Caco-2" } ]
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Long-term maintenance of the Caco-2 cell culture, and thus increasing the number of passages, leads to the selection of faster-growing subpopulations of cells expressing different subsets of characteristics .
[ { "end": 35, "label": "CellLine", "start": 29, "text": "Caco-2" } ]
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The literature review showed that the number of passages has a strong effect on the differentiation process and the integrity of the Caco-2 monolayer (assessed using the TEER value) .
[ { "end": 139, "label": "CellLine", "start": 133, "text": "Caco-2" } ]
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Selected permeability studies taking into account the number of passages of the Caco-2 cell line are presented in Table 4.
[ { "end": 86, "label": "CellLine", "start": 80, "text": "Caco-2" } ]
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The presented data show that the Caco-2 cell line is used for permeability studies with a passage number of approximately 20–50 .
[ { "end": 39, "label": "CellLine", "start": 33, "text": "Caco-2" } ]
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Moreover, validation of the Caco-2 cell line used for pharmaceutical purposes is performed for a single passage number .
[ { "end": 34, "label": "CellLine", "start": 28, "text": "Caco-2" } ]
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A review of the literature data showed that active Caco-2 cell cultures should be maintained for a period not longer than three months.
[ { "end": 57, "label": "CellLine", "start": 51, "text": "Caco-2" } ]
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The expended culture time and associated cell population drift may affect comparisons with historical permeability data.
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In addition, every time a new batch of Caco-2 cells is thawed, a new permeability calibration curve must be generated (using model drugs for each group’s permeability ).
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For the transport monolayer preparation, the Caco-2 cells are cultured on membrane inserts made from polycarbonate, polyester, or polyethylene terephthalate.
[ { "end": 51, "label": "CellLine", "start": 45, "text": "Caco-2" } ]
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Transparent filters are recommended for monitoring the differentiation process in an inverted or confocal microscope .
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