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Article: Epigenetic modulators for brain cancer stem cells: Implications for anticancer treatment.

Abballe, Luana / Miele, Evelina

2020 Volume 13, Issue 7, Page(s) 670–684

Abstract: Primary malignant brain tumors are a major cause of morbidity and mortality in both adults and children, with a dismal prognosis despite multimodal therapeutic approaches. In the last years, a specific subpopulation of cells within the tumor bulk, named ... ...

Abstract	Primary malignant brain tumors are a major cause of morbidity and mortality in both adults and children, with a dismal prognosis despite multimodal therapeutic approaches. In the last years, a specific subpopulation of cells within the tumor bulk, named cancer stem cells (CSCs) or tumor-initiating cells, have been identified in brain tumors as responsible for cancer growth and disease progression. Stemness features of tumor cells strongly affect treatment response, leading to the escape from conventional therapeutic approaches and subsequently causing tumor relapse. Recent research efforts have focused at identifying new therapeutic strategies capable of specifically targeting CSCs in cancers by taking into consideration their complex nature. Aberrant epigenetic machinery plays a key role in the genesis and progression of brain tumors as well as inducing CSC reprogramming and preserving CSC characteristics. Thus, reverting the cancer epigenome can be considered a promising therapeutic strategy. Three main epigenetic mechanisms have been described: DNA methylation, histone modifications, and non-coding RNA, particularly microRNAs. Each of these mechanisms has been proven to be targetable by chemical compounds, known as epigenetic-based drugs or epidrugs, that specifically target epigenetic marks. We review here recent advances in the study of epigenetic modulators promoting and sustaining brain tumor stem-like cells. We focus on their potential role in cancer therapy.
Language	English
Publishing date	2020-12-23
Publishing country	United States
Document type	Journal Article ; Review
ZDB-ID	2583482-4
ISSN	1948-0210
ISSN	1948-0210
DOI	10.4252/wjsc.v13.i7.670
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Article: Nanoparticles for Drug and Gene Delivery in Pediatric Brain Tumors' Cancer Stem Cells: Current Knowledge and Future Perspectives.

Abballe, Luana / Spinello, Zaira / Antonacci, Celeste / Coppola, Lucia / Miele, Ermanno / Catanzaro, Giuseppina / Miele, Evelina

Pharmaceutics

2023 Volume 15, Issue 2

Abstract: Primary malignant brain tumors are the most common solid neoplasm in childhood. Despite recent advances, many children affected by aggressive or metastatic brain tumors still present poor prognosis, therefore the development of more effective therapies ... ...

Abstract	Primary malignant brain tumors are the most common solid neoplasm in childhood. Despite recent advances, many children affected by aggressive or metastatic brain tumors still present poor prognosis, therefore the development of more effective therapies is urgent. Cancer stem cells (CSCs) have been discovered and isolated in both pediatric and adult patients with brain tumors (e.g., medulloblastoma, gliomas and ependymoma). CSCs are a small clonal population of cancer cells responsible for brain tumor initiation, maintenance and progression, displaying resistance to conventional anticancer therapies. CSCs are characterized by a specific repertoire of surface markers and intracellular specific pathways. These unique features of CSCs biology offer the opportunity to build therapeutic approaches to specifically target these cells in the complex tumor bulk. Treatment of pediatric brain tumors with classical chemotherapeutic regimen poses challenges both for tumor location and for the presence of the blood-brain barrier (BBB). Lastly, the application of chemotherapy to a developing brain is followed by long-term
Language	English
Publishing date	2023-02-02
Publishing country	Switzerland
Document type	Journal Article ; Review
ZDB-ID	2527217-2
ISSN	1999-4923
ISSN	1999-4923
DOI	10.3390/pharmaceutics15020505
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Article: Modeling Brain Tumors: A Perspective Overview of

Antonica, Francesco / Aiello, Giuseppe / Soldano, Alessia / Abballe, Luana / Miele, Evelina / Tiberi, Luca

Frontiers in molecular neuroscience

2022 Volume 15, Page(s) 818696

Abstract: Brain tumors are a large and heterogeneous group of neoplasms that affect the central nervous system and include some of the deadliest cancers. Almost all the conventional and new treatments fail to hinder tumoral growth of the most malignant brain ... ...

Abstract	Brain tumors are a large and heterogeneous group of neoplasms that affect the central nervous system and include some of the deadliest cancers. Almost all the conventional and new treatments fail to hinder tumoral growth of the most malignant brain tumors. This is due to multiple factors, such as intra-tumor heterogeneity, the microenvironmental properties of the human brain, and the lack of reliable models to test new therapies. Therefore, creating faithful models for each tumor and discovering tailored treatments pose great challenges in the fight against brain cancer. Over the years, different types of models have been generated, and, in this review, we investigated the advantages and disadvantages of the models currently used.
Language	English
Publishing date	2022-05-30
Publishing country	Switzerland
Document type	Journal Article ; Review
ZDB-ID	2452967-9
ISSN	1662-5099
ISSN	1662-5099
DOI	10.3389/fnmol.2022.818696
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Article: Evaluating cell culture reliability in pediatric brain tumor primary cells through DNA methylation profiling.

Pedace, Lucia / Pizzi, Simone / Abballe, Luana / Vinci, Maria / Antonacci, Celeste / Patrizi, Sara / Nardini, Claudia / Del Bufalo, Francesca / Rossi, Sabrina / Pericoli, Giulia / Gianno, Francesca / Besharat, Zein Mersini / Tiberi, Luca / Mastronuzzi, Angela / Ferretti, Elisabetta / Tartaglia, Marco / Locatelli, Franco / Ciolfi, Andrea / Miele, Evelina

NPJ precision oncology

2024 Volume 8, Issue 1, Page(s) 92

Abstract: In vitro models of pediatric brain tumors (pBT) are instrumental for better understanding the mechanisms contributing to oncogenesis and testing new therapies; thus, ideally, they should recapitulate the original tumor. We applied DNA methylation (DNAm) ... ...

Abstract	In vitro models of pediatric brain tumors (pBT) are instrumental for better understanding the mechanisms contributing to oncogenesis and testing new therapies; thus, ideally, they should recapitulate the original tumor. We applied DNA methylation (DNAm) and copy number variation (CNV) profiling to characterize 241 pBT samples, including 155 tumors and 86 pBT-derived cell cultures, considering serum vs serum-free conditions, late vs early passages, and dimensionality (2D vs 3D cultures). We performed a t-SNE classification and identified differentially methylated regions in tumors compared to cell models. Early cell cultures recapitulate the original tumor, but serum media and 2D culturing were demonstrated to significantly contribute to the divergence of DNAm profiles from the parental ones. All divergent cells clustered together acquiring a common deregulated epigenetic signature suggesting a shared selective pressure. We identified a set of hypomethylated genes shared among unfaithful cells converging on response to growth factors and migration pathways, such as signaling cascade activation, tissue organization, and cellular migration. In conclusion, DNAm and CNV are informative tools that should be used to assess the recapitulation of pBT-cells from parental tumors.
Language	English
Publishing date	2024-04-18
Publishing country	England
Document type	Journal Article
ISSN	2397-768X
ISSN	2397-768X
DOI	10.1038/s41698-024-00578-x
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Article: β-arrestin1-E2F1-ac axis regulates physiological apoptosis and cell cycle exit in cellular models of early postnatal cerebellum.

Abballe, Luana / Alfano, Vincenzo / Antonacci, Celeste / Cefalo, Maria Giuseppina / Cacchione, Antonella / Del Baldo, Giada / Pezzullo, Marco / Po, Agnese / Moretti, Marta / Mastronuzzi, Angela / De Smaele, Enrico / Ferretti, Elisabetta / Locatelli, Franco / Miele, Evelina

Frontiers in cell and developmental biology

2023 Volume 11, Page(s) 990711

Abstract: Development of the cerebellum is characterized by rapid proliferation of cerebellar granule cell precursors (GCPs) induced by paracrine stimulation of Sonic hedgehog (Shh) signaling from Purkinje cells, in the external granular layer (EGL). Then, granule ...

Abstract	Development of the cerebellum is characterized by rapid proliferation of cerebellar granule cell precursors (GCPs) induced by paracrine stimulation of Sonic hedgehog (Shh) signaling from Purkinje cells, in the external granular layer (EGL). Then, granule cell precursors differentiate and migrate into the inner granular layer (IGL) of the cerebellum to form a terminally differentiated cell compartment. Aberrant activation of Sonic hedgehog signaling leads to granule cell precursors hyperproliferation and the onset of Sonic hedgehog medulloblastoma (MB), the most common embryonal brain tumor. β-arrestin1 (ARRB1) protein plays an important role downstream of Smoothened, a component of the Sonic hedgehog pathway. In the medulloblastoma context, β-arrestin1 is involved in a regulatory axis in association with the acetyltransferase P300, leading to the acetylated form of the transcription factor E2F1 (E2F1-ac) and redirecting its activity toward pro-apoptotic gene targets. This axis in the granule cell precursors physiological context has not been investigated yet. In this study, we demonstrate that β-arrestin1 has antiproliferative and pro-apoptotic functions in cerebellar development. β-arrestin1 silencing increases proliferation of Sonic hedgehog treated-cerebellar precursor cells while decreases the transcription of E2F1-ac pro-apoptotic targets genes, thus impairing apoptosis. Indeed, chromatin immunoprecipitation experiments show a direct interaction between β-arrestin1 and the promoter regions of the pro-apoptotic E2F1 target gene and
Language	English
Publishing date	2023-02-27
Publishing country	Switzerland
Document type	Journal Article
ZDB-ID	2737824-X
ISSN	2296-634X
ISSN	2296-634X
DOI	10.3389/fcell.2023.990711
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Article ; Online: The role of FOSL1 in stem-like cell reprogramming processes.

Pecce, Valeria / Verrienti, Antonella / Fiscon, Giulia / Sponziello, Marialuisa / Conte, Federica / Abballe, Luana / Durante, Cosimo / Farina, Lorenzo / Filetti, Sebastiano / Paci, Paola

Scientific reports

2021 Volume 11, Issue 1, Page(s) 14677

Abstract: Cancer stem-like cells (CSCs) have self-renewal abilities responsible for cancer progression, therapy resistance, and metastatic growth. The glioblastoma stem-like cells are the most studied among CSC populations. A recent study identified four ... ...

Abstract	Cancer stem-like cells (CSCs) have self-renewal abilities responsible for cancer progression, therapy resistance, and metastatic growth. The glioblastoma stem-like cells are the most studied among CSC populations. A recent study identified four transcription factors (SOX2, SALL2, OLIG2, and POU3F2) as the minimal core sufficient to reprogram differentiated glioblastoma (GBM) cells into stem-like cells. Transcriptomic data of GBM tissues and cell lines from two different datasets were then analyzed by the SWItch Miner (SWIM), a network-based software, and FOSL1 was identified as a putative regulator of the previously identified minimal core. Herein, we selected NTERA-2 and HEK293T cells to perform an in vitro study to investigate the role of FOSL1 in the reprogramming mechanisms. We transfected the two cell lines with a constitutive FOSL1 cDNA plasmid. We demonstrated that FOSL1 directly regulates the four transcription factors binding their promoter regions, is involved in the deregulation of several stemness markers, and reduces the cells' ability to generate aggregates increasing the extracellular matrix component FN1. Although further experiments are necessary, our data suggest that FOSL1 reprograms the stemness by regulating the core of the four transcription factors.
MeSH term(s)	Brain Neoplasms/genetics ; Brain Neoplasms/pathology ; Cell Differentiation/genetics ; Cell Line, Tumor ; Cellular Reprogramming/genetics ; Gene Expression Regulation, Neoplastic ; Glioblastoma/genetics ; Glioblastoma/pathology ; HEK293 Cells ; HeLa Cells ; Humans ; Neoplastic Stem Cells/pathology ; Neoplastic Stem Cells/physiology ; Proto-Oncogene Proteins c-fos/genetics ; Proto-Oncogene Proteins c-fos/physiology
Chemical Substances	Proto-Oncogene Proteins c-fos ; fos-related antigen 1
Language	English
Publishing date	2021-07-19
Publishing country	England
Document type	Journal Article ; Research Support, Non-U.S. Gov't
ZDB-ID	2615211-3
ISSN	2045-2322 ; 2045-2322
ISSN (online)	2045-2322
ISSN	2045-2322
DOI	10.1038/s41598-021-94072-0
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Article ; Online: Malignant peripheral nerve sheath tumor (MPNST) and MPNST-like entities are defined by a specific DNA methylation profile in pediatric and juvenile population.

Clinical epigenetics

2024 Volume 16, Issue 1, Page(s) 9

Abstract: Background: Malignant peripheral nerve sheath tumors (MPNSTs) account for 3-10% of pediatric sarcomas, 50% of which occur in neurofibromatosis type 1 (NF1). Sporadic MPNSTs diagnosis may be challenging due to the absence of specific markers, apart from ... ...

Abstract	Background: Malignant peripheral nerve sheath tumors (MPNSTs) account for 3-10% of pediatric sarcomas, 50% of which occur in neurofibromatosis type 1 (NF1). Sporadic MPNSTs diagnosis may be challenging due to the absence of specific markers, apart from immunohistochemical H3K27me3 loss. DNA methylation (DNAm) profiling is a useful tool for brain and mesenchymal neoplasms categorization, and MPNSTs exhibit a specific DNAm signature. An MPNST-like group has recently been recognized, including pediatric tumors with retained H3K27me3 mark and clinical/histological features not yet well explored. This study aims to characterize the DNAm profile of pediatric/juvenile MPNSTs/MPNST-like entities and its diagnostic/prognostic relevance. Results: We studied 42 tumors from two groups. Group 1 included 32 tumors histologically diagnosed as atypical neurofibroma (ANF) (N = 5) or MPNST (N = 27); group 2 comprised 10 tumors classified as MPNST-like according to Heidelberg sarcoma classifier. We performed further immunohistochemical and molecular tests to reach an integrated diagnosis. In group 1, DNAm profiling was inconclusive for ANF; while, it confirmed the original diagnosis in 12/27 MPNSTs, all occurring in NF1 patients. Five/27 MPNSTs were classified as MPNST-like: Integrated diagnosis confirmed MPNST identity for 3 cases; while, the immunophenotype supported the change to high-grade undifferentiated spindle cell sarcoma in 2 samples. The remaining 10/27 MPNSTs variably classified as schwannoma, osteosarcoma, BCOR-altered sarcoma, rhabdomyosarcoma (RMS)-MYOD1 mutant, RMS-like, and embryonal RMS or did not match with any defined entity. Molecular analysis and histologic review confirmed the diagnoses of BCOR, RMS-MYOD1 mutant, DICER1-syndrome and ERMS. Group 2 samples included 5 high-grade undifferentiated sarcomas/MPNSTs and 5 low-grade mesenchymal neoplasms. Two high-grade and 4 low-grade lesions harbored tyrosine kinase (TRK) gene fusions. By HDBSCAN clustering analysis of the whole cohort we identified two clusters mainly distinguished by H3K27me3 epigenetic signature. Exploring the copy number variation, high-grade tumors showed frequent chromosomal aberrations and CDKN2A/B loss significantly impacted on survival in the MPNSTs cohort. Conclusion: DNAm profiling is a useful tool in diagnostic work-up of MPNSTs. Its application in a retrospective series collected during pre-molecular era contributed to classify morphologic mimics. The methylation group MPNST-like is a 'hybrid' category in pediatrics including high-grade and low-grade tumors mainly characterized by TRK alterations.
MeSH term(s)	Humans ; Child ; Neurofibrosarcoma/diagnosis ; Neurofibrosarcoma/genetics ; Neurofibrosarcoma/pathology ; Histones/metabolism ; DNA Methylation ; Retrospective Studies ; DNA Copy Number Variations ; Rhabdomyosarcoma ; Sarcoma/diagnosis ; Sarcoma/genetics ; Sarcoma/pathology ; Protein-Tyrosine Kinases ; Bone Neoplasms ; Ribonuclease III ; DEAD-box RNA Helicases
Chemical Substances	Histones ; Protein-Tyrosine Kinases (EC 2.7.10.1) ; DICER1 protein, human (EC 3.1.26.3) ; Ribonuclease III (EC 3.1.26.3) ; DEAD-box RNA Helicases (EC 3.6.4.13)
Language	English
Publishing date	2024-01-04
Publishing country	Germany
Document type	Journal Article ; Research Support, Non-U.S. Gov't
ZDB-ID	2553921-8
ISSN	1868-7083 ; 1868-7075
ISSN (online)	1868-7083
ISSN	1868-7075
DOI	10.1186/s13148-023-01621-7
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Article ; Online: Low Doses of Methylmercury Induce the Proliferation of Thyroid Cells In Vitro Through Modulation of ERK Pathway.

Maggisano, Valentina / Bulotta, Stefania / Celano, Marilena / Maiuolo, Jessica / Lepore, Saverio Massimo / Abballe, Luana / Iannone, Michelangelo / Russo, Diego

International journal of molecular sciences

2020 Volume 21, Issue 5

Abstract: Exposure to environmental endocrine disruptors has been associated with an increased frequency of thyroid pathology. In this study, we evaluated the effects of various concentrations of methylmercury (MeHg) on immortalized, non-tumorigenic thyroid cells ( ...

Abstract	Exposure to environmental endocrine disruptors has been associated with an increased frequency of thyroid pathology. In this study, we evaluated the effects of various concentrations of methylmercury (MeHg) on immortalized, non-tumorigenic thyroid cells (Nthy-ori-3-1). Exposure to MeHg at 2.5 and 5 µM for 24 h caused a reduction in cell viability with a decrease of the cell population in sub-G0 phase, as detected by MTT and flow cytometry. Conversely, MeHg at the lower concentration of 0.1 µM increased the cell viability with a rise of G2/M phase. An immunoblot analysis showed higher expression levels of phospho-ERK and not of phospho-Akt. Further enhancement of the cell growth rate was observed after a prolonged exposure of the cells up to 18 days to MeHg 0.1 µM. The present findings demonstrate the toxicity of high concentrations of MeHg on thyroid cells, while showing that treatment with lower doses of Hg, as may occur after prolonged exposure to this environmental contaminant, exerts a promoting effect on thyroid cell proliferation, by acting on the ERK-mediated pro-oncogenic signal transduction pathway.
MeSH term(s)	Cell Line ; Cell Proliferation ; Endocrine Disruptors/pharmacology ; Humans ; MAP Kinase Signaling System ; Methylmercury Compounds/pharmacology ; Thyroid Epithelial Cells/drug effects ; Thyroid Epithelial Cells/metabolism ; Thyroid Epithelial Cells/physiology
Chemical Substances	Endocrine Disruptors ; Methylmercury Compounds
Language	English
Publishing date	2020-02-25
Publishing country	Switzerland
Document type	Journal Article
ZDB-ID	2019364-6
ISSN	1422-0067 ; 1422-0067 ; 1661-6596
ISSN (online)	1422-0067
ISSN	1422-0067 ; 1661-6596
DOI	10.3390/ijms21051556
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Article ; Online: Patient- and xenograft-derived organoids recapitulate pediatric brain tumor features and patient treatments.

EMBO molecular medicine

2023 Volume 15, Issue 12, Page(s) e18199

Abstract: Brain tumors are the leading cause of cancer-related death in children. Experimental in vitro models that faithfully capture the hallmarks and tumor heterogeneity of pediatric brain cancers are limited and hard to establish. We present a protocol that ... ...

Abstract	Brain tumors are the leading cause of cancer-related death in children. Experimental in vitro models that faithfully capture the hallmarks and tumor heterogeneity of pediatric brain cancers are limited and hard to establish. We present a protocol that enables efficient generation, expansion, and biobanking of pediatric brain cancer organoids. Utilizing our protocol, we have established patient-derived organoids (PDOs) from ependymomas, medulloblastomas, low-grade glial tumors, and patient-derived xenograft organoids (PDXOs) from medulloblastoma xenografts. PDOs and PDXOs recapitulate histological features, DNA methylation profiles, and intratumor heterogeneity of the tumors from which they were derived. We also showed that PDOs can be xenografted. Most interestingly, when subjected to the same routinely applied therapeutic regimens, PDOs respond similarly to the patients. Taken together, our study highlights the potential of PDOs and PDXOs for research and translational applications for personalized medicine.
MeSH term(s)	Humans ; Child ; Heterografts ; Biological Specimen Banks ; Brain Neoplasms/therapy ; Brain Neoplasms/pathology ; Organoids/pathology
Language	English
Publishing date	2023-11-30
Publishing country	England
Document type	Journal Article
ZDB-ID	2467145-9
ISSN	1757-4684 ; 1757-4676
ISSN (online)	1757-4684
ISSN	1757-4676
DOI	10.15252/emmm.202318199
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Article ; Online: Clinicopathological and molecular landscape of 5-year IDH-wild-type glioblastoma survivors: A multicentric retrospective study.

Miele, Evelina / Anghileri, Elena / Calatozzolo, Chiara / Lazzarini, Elisabetta / Patrizi, Sara / Ciolfi, Andrea / Pedace, Lucia / Patanè, Monica / Abballe, Luana / Paterra, Rosina / Maddaloni, Luisa / Barresi, Sabina / Mastronuzzi, Angela / Petruzzi, Alessandra / Tramacere, Irene / Farinotti, Mariangela / Gurrieri, Lorena / Pirola, Elena / Scarpelli, Mauro /

Lombardi, Giuseppe / Villani, Veronica / Simonelli, Matteo / Merli, Rossella / Salmaggi, Andrea / Tartaglia, Marco / Silvani, Antonio / DiMeco, Francesco / Calistri, Daniele / Lamperti, Elena / Locatelli, Franco / Indraccolo, Stefano / Pollo, Bianca

Cancer letters

2024 Volume 588, Page(s) 216711

Abstract: Five-year glioblastoma (GBM) survivors (LTS) are the minority of the isocitrate dehydrogenase (IDH)-wild-type GBM patients, and their molecular fingerprint is still largely unexplored. This multicenter retrospective study analyzed a large LTS-GBM cohort ... ...

Abstract	Five-year glioblastoma (GBM) survivors (LTS) are the minority of the isocitrate dehydrogenase (IDH)-wild-type GBM patients, and their molecular fingerprint is still largely unexplored. This multicenter retrospective study analyzed a large LTS-GBM cohort from nine Italian institutions and molecularly characterized a subgroup of patients by mutation, DNA methylation (DNAm) and copy number variation (CNV) profiling, comparing it to standard survival GBM. Mutation scan allowed the identification of pathogenic variants in most cases, showing a similar mutational spectrum in both groups, and highlighted TP53 as the most commonly mutated gene in the LTS group. We confirmed DNAm as a valuable tool for GBM classification with a diagnostic refinement by using brain tumor classifier v12.5. LTS were more heterogeneous with more cases classified as diffuse pediatric high-grade glioma subtypes and having peculiar CNVs. We observed a global higher methylation in CpG islands and in gene promoters of LTS with methylation levels of distinct gene promoters correlating with prognosis.
MeSH term(s)	Humans ; Child ; Glioblastoma/pathology ; Retrospective Studies ; Isocitrate Dehydrogenase/genetics ; DNA Copy Number Variations ; Brain Neoplasms/pathology ; Mutation ; Prognosis ; DNA Methylation ; Survivors
Chemical Substances	Isocitrate Dehydrogenase (EC 1.1.1.41)
Language	English
Publishing date	2024-02-27
Publishing country	Ireland
Document type	Multicenter Study ; Journal Article
ZDB-ID	195674-7
ISSN	1872-7980 ; 0304-3835
ISSN (online)	1872-7980
ISSN	0304-3835
DOI	10.1016/j.canlet.2024.216711
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