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Article ; Online: Interleukin-6 at the Host-Tumor Interface: STAT3 in Biomolecular Condensates in Cancer Cells.

Sehgal, Pravin B

2022 Volume 11, Issue 7

Abstract: It was recognized over 30 years ago that the polyfunctional cytokine interleukin-6 (IL-6) was an almost invariant presence at the host-tumor interface. The IL-6 in the tumor microenvironment was produced either by the cancer cell or by host stromal cells, ...

Abstract	It was recognized over 30 years ago that the polyfunctional cytokine interleukin-6 (IL-6) was an almost invariant presence at the host-tumor interface. The IL-6 in the tumor microenvironment was produced either by the cancer cell or by host stromal cells, or by tumor-infiltrating immune cells, or all of them. IL-6 effects in this context included local changes in tumor cell-cell and cell-substrate adhesion, enhanced motility, epithelial to mesenchymal transformation (EMT), and changes in cell proliferation rates in both solid tumors as well as hematologic dyscrasias. Locally produced IL-6 enhanced cancer-targeting functions of tumor-infiltrating macrophages and immune cells. Additionally, the sex-biased phenotype of certain cancers [e.g., hepatocellular carcinoma (HCC) which is 3-5-fold more common in men] was related to the inhibition of macrophage-derived IL-6 production by estradiol-17β (E2). In many circumstances, locally produced IL-6 reached the peripheral circulation and elicited systemic effects such as cachexia and paraneoplastic syndrome (including fever, increased erythrocyte sedimentation rate, increased levels of C-reactive protein in serum, hypoalbuminemia). This review highlights the EMT produced by IL-6 in cancer cells, as well as mechanisms underlying sex bias in HCC, enhanced IL-6 expression in cancer cells resulting from mutations in p53, consequent alterations in STAT3 transcriptional signaling, and the newer understanding of STAT3 nuclear bodies in the cancer cell as phase-separated biomolecular condensates and membraneless organelles (MLOs). Moreover, the perplexing issue of discrepant measurements of IL-6 in human circulation using different assays, especially in patients undergoing immunotherapy, is discussed. Additionally, the paradoxical chaperone (enhancing) effect of anti-IL-6 "neutralizing" antibodies on IL-6 in vivo and consequent limitations of immunotherapy using anti-IL-6 mAb is considered.
MeSH term(s)	Biomolecular Condensates ; Carcinoma, Hepatocellular/pathology ; Epithelial-Mesenchymal Transition ; Humans ; Interleukin-6/metabolism ; Liver Neoplasms/pathology ; STAT3 Transcription Factor/metabolism ; Tumor Microenvironment
Chemical Substances	IL6 protein, human ; Interleukin-6 ; STAT3 Transcription Factor ; STAT3 protein, human
Language	English
Publishing date	2022-03-30
Publishing country	Switzerland
Document type	Journal Article ; Review
ZDB-ID	2661518-6
ISSN	2073-4409 ; 2073-4409
ISSN (online)	2073-4409
ISSN	2073-4409
DOI	10.3390/cells11071164
Database	MEDical Literature Analysis and Retrieval System OnLINE

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Article ; Online: Metastable biomolecular condensates of interferon-inducible antiviral Mx-family GTPases: A paradigm shift in the last three years.

Sehgal, Pravin B

Journal of biosciences

2021 Volume 46

Abstract: Membraneless organelles (MLOs) in the cytoplasm and nucleus in the form of phase-separated biomolecular condensates are increasingly viewed as critical in regulating diverse cellular functions. We summarize a paradigm shift over the last 3 years in the ... ...

Abstract	Membraneless organelles (MLOs) in the cytoplasm and nucleus in the form of phase-separated biomolecular condensates are increasingly viewed as critical in regulating diverse cellular functions. We summarize a paradigm shift over the last 3 years in the field of interferon (IFN)-inducible antiviral Mx-family GTPases. Expression of the 'myxovirus resistance proteins' MxA in human cells and its ortholog Mx1 in murine cells is increased 50- to 100-fold by Type I (IFN-α and -β) and III IFNs (IFN-λ). Human MxA forms
MeSH term(s)	Amino Acid Sequence ; Animals ; Biomolecular Condensates/metabolism ; GTP Phosphohydrolases/biosynthesis ; GTP Phosphohydrolases/metabolism ; Green Fluorescent Proteins/metabolism ; Humans ; Interferons/physiology ; Mice ; Myxovirus Resistance Proteins/biosynthesis ; Myxovirus Resistance Proteins/chemistry ; Myxovirus Resistance Proteins/metabolism ; Subcellular Fractions/metabolism
Chemical Substances	Myxovirus Resistance Proteins ; Green Fluorescent Proteins (147336-22-9) ; Interferons (9008-11-1) ; GTP Phosphohydrolases (EC 3.6.1.-)
Language	English
Publishing date	2021-09-27
Publishing country	India
Document type	Journal Article ; Review
ZDB-ID	756157-x
ISSN	0973-7138 ; 0250-5991
ISSN (online)	0973-7138
ISSN	0250-5991
Database	MEDical Literature Analysis and Retrieval System OnLINE

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Article ; Online: Interleukin-6 at the Host-Tumor Interface

Pravin B. Sehgal

Cells, Vol 11, Iss 1164, p

STAT3 in Biomolecular Condensates in Cancer Cells

2022 Volume 1164

Abstract	It was recognized over 30 years ago that the polyfunctional cytokine interleukin-6 (IL-6) was an almost invariant presence at the host-tumor interface. The IL-6 in the tumor microenvironment was produced either by the cancer cell or by host stromal cells, or by tumor-infiltrating immune cells, or all of them. IL-6 effects in this context included local changes in tumor cell-cell and cell-substrate adhesion, enhanced motility, epithelial to mesenchymal transformation (EMT), and changes in cell proliferation rates in both solid tumors as well as hematologic dyscrasias. Locally produced IL-6 enhanced cancer-targeting functions of tumor-infiltrating macrophages and immune cells. Additionally, the sex-biased phenotype of certain cancers [e.g., hepatocellular carcinoma (HCC) which is 3-5-fold more common in men] was related to the inhibition of macrophage-derived IL-6 production by estradiol-17β (E2). In many circumstances, locally produced IL-6 reached the peripheral circulation and elicited systemic effects such as cachexia and paraneoplastic syndrome (including fever, increased erythrocyte sedimentation rate, increased levels of C-reactive protein in serum, hypoalbuminemia). This review highlights the EMT produced by IL-6 in cancer cells, as well as mechanisms underlying sex bias in HCC, enhanced IL-6 expression in cancer cells resulting from mutations in p53, consequent alterations in STAT3 transcriptional signaling, and the newer understanding of STAT3 nuclear bodies in the cancer cell as phase-separated biomolecular condensates and membraneless organelles (MLOs). Moreover, the perplexing issue of discrepant measurements of IL-6 in human circulation using different assays, especially in patients undergoing immunotherapy, is discussed. Additionally, the paradoxical chaperone (enhancing) effect of anti-IL-6 “neutralizing” antibodies on IL-6 in vivo and consequent limitations of immunotherapy using anti-IL-6 mAb is considered.
Keywords	cytokines ; interleukin-6 (IL-6) ; cancer cells ; stromal cells ; macrophages ; epithelial to mesenchymal transformation (EMT) ; Biology (General) ; QH301-705.5
Language	English
Publishing date	2022-03-01T00:00:00Z
Publisher	MDPI AG
Document type	Article ; Online
Database	BASE - Bielefeld Academic Search Engine (life sciences selection)

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Article: Biomolecular condensates in cancer cell biology: interleukin-6-induced cytoplasmic and nuclear STAT3/PY-STAT3 condensates in hepatoma cells.

Sehgal, Pravin B

Contemporary oncology (Poznan, Poland)

2019 Volume 23, Issue 1, Page(s) 16–22

Abstract: We highlight previous incompletely understood cell biology data in the STAT3 signaling field with respect to interleukin-6 (IL-6)-induced activation of this transcription factor in hepatoma cells to generate cytoplasmic and nuclear STAT3 bodies. We ... ...

Abstract	We highlight previous incompletely understood cell biology data in the STAT3 signaling field with respect to interleukin-6 (IL-6)-induced activation of this transcription factor in hepatoma cells to generate cytoplasmic and nuclear STAT3 bodies. We provide a novel re-interpretation of the previous observations. We show that IL-6-induced GFP-STAT3/PY-STAT3 cytoplas-mic and nuclear bodies represent phase-separated biomolecular condensates. These structures represent examples of a cytokine-induced phase transition which occurs within 10-15 min of exposure to the cytokine, and which was Tyr phosphorylation dependent. Evidence that these IL-6-induced cytoplasmic and nuclear GFP-STAT3 bodies in live cells represented phase-separated condensates came from the observation that 1,6-hexanediol caused their disassembly within 30-60 seconds. Moreover, these STAT3 condensates also showed rapid tonicity-driven phase transitions - disassembly under hypotonic conditions and reassembly when cells were returned to isotonic medium. That STAT3 condensates were rapidly disassembled in hypotonic buffer commonly used for cell fractionation points to a limitation of studies of STAT3 biochemistry using hypotonic swelling and mechanical breakage. Overall, the new data help reinterpret IL-6-induced cytoplasmic and nuclear STAT3 bodies as phase-separated biomolecular condensates, and bring the concept of membrane-less organelles to the cytokine-induced STAT transcription factor field and cancer cell biology.
Language	English
Publishing date	2019-02-26
Publishing country	Poland
Document type	Journal Article
ISSN	1428-2526
ISSN	1428-2526
DOI	10.5114/wo.2019.83018
Database	MEDical Literature Analysis and Retrieval System OnLINE

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Article: Metastable biomolecular condensates of interferon-inducible antiviral Mx-family GTPases: A paradigm shift in the last three years

Sehgal, Pravin B

Journal of biosciences. 2021 Sept., v. 46, no. 3

2021

Abstract	Membraneless organelles (MLOs) in the cytoplasm and nucleus in the form of phase-separated biomolecular condensates are increasingly viewed as critical in regulating diverse cellular functions. We summarize a paradigm shift over the last 3 years in the field of interferon (IFN)-inducible antiviral Mx-family GTPases. Expression of the ‘myxovirus resistance proteins’ MxA in human cells and its ortholog Mx1 in murine cells is increased 50- to 100-fold by Type I (IFN-α and -β) and III IFNs (IFN-λ). Human MxA forms cytoplasmic structures, while murine Mx1 forms nuclear bodies. Since 2002, it has been widely thought that human (Hu) MxA is associated with the membraneous smooth endoplasmic reticulum (ER). In a paradigm shift, our recent data showed that HuMxA formed membraneless phase-separated biomolecular condensates in the cytoplasm. Some of the HuMxA condensates adhered to intermediate filaments generating a reticular pattern. Murine (Mu) Mx1, which was predominantly nuclear, was also confirmed to be in phase-separated nuclear biomolecular condensates. A subset of Huh7 cells showed association of GFP-MuMx1 with intermediate filaments in the cytoplasm. While cells with cytoplasmic GFP-HuMxA condensates and cytoplasmic GFP-MuMx1 filaments showed an antiviral phenotype towards vesicular stomatitis virus (VSV), those with only nuclear GFP-MuMx1 bodies did not. The new data bring forward the paradigm that both human MxA and murine Mx1 give rise to phase-separated biomolecular condensates, albeit in different subcellular compartments, and that differences in the subcellular localization of condensates of different Mx proteins determines the spectrum of their antiviral activity.
Keywords	Vesiculovirus ; antiviral properties ; guanosinetriphosphatase ; humans ; mice ; phenotype ; smooth endoplasmic reticulum
Language	English
Dates of publication	2021-09
Size	p. 72.
Publishing place	Springer India
Document type	Article
Note	Review
ZDB-ID	756157-x
ISSN	0973-7138 ; 0250-5991
ISSN (online)	0973-7138
ISSN	0250-5991
DOI	10.1007/s12038-021-00187-x
Database	NAL-Catalogue (AGRICOLA)

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Article ; Online: Oral Antiviral Defense: Saliva- and Beverage-like Hypotonicity Dynamically Regulate Formation of Membraneless Biomolecular Condensates of Antiviral Human MxA in Oral Epithelial Cells.

Sehgal, Pravin B / Yuan, Huijuan / Centone, Anthony / DiSenso-Browne, Susan V

Cells

2024 Volume 13, Issue 7

Abstract: The oral mucosa represents a defensive barrier between the external environment and the rest of the body. Oral mucosal cells are constantly bathed in hypotonic saliva (normally one-third tonicity compared to plasma) and are repeatedly exposed to ... ...

Abstract	The oral mucosa represents a defensive barrier between the external environment and the rest of the body. Oral mucosal cells are constantly bathed in hypotonic saliva (normally one-third tonicity compared to plasma) and are repeatedly exposed to environmental stresses of tonicity, temperature, and pH by the drinks we imbibe (e.g., hypotonic: water, tea, and coffee; hypertonic: assorted fruit juices, and red wines). In the mouth, the broad-spectrum antiviral mediator MxA (a dynamin-family large GTPase) is constitutively expressed in healthy periodontal tissues and induced by Type III interferons (e.g., IFN-λ1/IL-29). Endogenously induced human MxA and exogenously expressed human GFP-MxA formed membraneless biomolecular condensates in the cytoplasm of oral carcinoma cells (OECM1 cell line). These condensates likely represent storage granules in equilibrium with antivirally active dispersed MxA. Remarkably, cytoplasmic MxA condensates were exquisitely sensitive sensors of hypotonicity-the condensates in oral epithelium disassembled within 1-2 min of exposure of cells to saliva-like one-third hypotonicity, and spontaneously reassembled in the next 4-7 min. Water, tea, and coffee enhanced this disassembly. Fluorescence changes in OECM1 cells preloaded with calcein-AM (a reporter of cytosolic "macromolecular crowding") confirmed that this process involved macromolecular uncrowding and subsequent recrowding secondary to changes in cell volume. However, hypertonicity had little effect on MxA condensates. The spontaneous reassembly of GFP-MxA condensates in oral epithelial cells, even under continuous saliva-like hypotonicity, was slowed by the protein-phosphatase-inhibitor cyclosporin A (CsA) and by the K-channel-blocker tetraethylammonium chloride (TEA); this is suggestive of the involvement of the volume-sensitive WNK kinase-protein phosphatase (PTP)-K-Cl cotransporter (KCC) pathway in the regulated volume decrease (RVD) during condensate reassembly in oral cells. The present study identifies a novel subcellular consequence of hypotonic stress in oral epithelial cells, in terms of the rapid and dynamic changes in the structure of one class of phase-separated biomolecular condensates in the cytoplasm-the antiviral MxA condensates. More generally, the data raise the possibility that hypotonicity-driven stresses likely affect other intracellular functions involving liquid-liquid phase separation (LLPS) in cells of the oral mucosa.
MeSH term(s)	Humans ; Biomolecular Condensates ; Coffee ; Epithelial Cells ; Saliva/metabolism ; Tea ; Water ; Myxovirus Resistance Proteins/metabolism
Chemical Substances	Coffee ; Tea ; Water (059QF0KO0R) ; MX1 protein, human ; Myxovirus Resistance Proteins
Language	English
Publishing date	2024-03-28
Publishing country	Switzerland
Document type	Journal Article
ZDB-ID	2661518-6
ISSN	2073-4409 ; 2073-4409
ISSN (online)	2073-4409
ISSN	2073-4409
DOI	10.3390/cells13070590
Database	MEDical Literature Analysis and Retrieval System OnLINE

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Article ; Online: Rapid Reversible Osmoregulation of Cytoplasmic Biomolecular Condensates of Human Interferon-α-Induced Antiviral MxA GTPase.

Sehgal, Pravin B / Yuan, Huijuan / Jin, Ye

International journal of molecular sciences

2022 Volume 23, Issue 21

Abstract: We previously discovered that exogenously expressed GFP-tagged cytoplasmic human myxovirus resistance protein (MxA), a major antiviral effector of Type I and III interferons (IFNs) against several RNA- and DNA-containing viruses, existed in the cytoplasm ...

Abstract	We previously discovered that exogenously expressed GFP-tagged cytoplasmic human myxovirus resistance protein (MxA), a major antiviral effector of Type I and III interferons (IFNs) against several RNA- and DNA-containing viruses, existed in the cytoplasm in phase-separated membraneless biomolecular condensates of varying sizes and shapes with osmotically regulated disassembly and reassembly. In this study we investigated whether cytoplasmic IFN-α-induced
MeSH term(s)	Humans ; Antiviral Agents/pharmacology ; Antiviral Agents/metabolism ; GTP Phosphohydrolases/metabolism ; Myxovirus Resistance Proteins/genetics ; Myxovirus Resistance Proteins/metabolism ; Osmoregulation ; Biomolecular Condensates ; Interferon-alpha/pharmacology ; Interferon-alpha/metabolism ; Cytoplasm/metabolism ; Proteins/metabolism
Chemical Substances	Antiviral Agents ; GTP Phosphohydrolases (EC 3.6.1.-) ; Myxovirus Resistance Proteins ; Interferon-alpha ; Proteins
Language	English
Publishing date	2022-10-22
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/ijms232112739
Database	MEDical Literature Analysis and Retrieval System OnLINE

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Article ; Online: Biomolecular condensates in cancer cell biology

Pravin B. Sehgal

Contemporary Oncology, Vol 23, Iss 1, Pp 16-

interleukin-6-induced cytoplasmic and nuclear STAT3/PY-STAT3 condensates in hepatoma cells

2019 Volume 22

Abstract	We highlight previous incompletely understood cell biology data in the STAT3 signaling field with respect to interleukin-6 (IL-6)-induced activation of this transcription factor in hepatoma cells to generate cytoplasmic and nuclear STAT3 bodies. We provide a novel re-interpretation of the previous observations. We show that IL-6-induced GFP-STAT3/PY-STAT3 cytoplas-mic and nuclear bodies represent phase-separated biomolecular condensates. These structures represent examples of a cytokine-induced phase transition which occurs within 10–15 min of exposure to the cytokine, and which was Tyr phosphorylation dependent. Evidence that these IL-6-induced cytoplasmic and nuclear GFP-STAT3 bodies in live cells represented phase-separated condensates came from the observation that 1,6-hexanediol caused their disassembly within 30–60 seconds. Moreover, these STAT3 condensates also showed rapid tonicity-driven phase transitions – disassembly under hypotonic conditions and reassembly when cells were returned to isotonic medium. That STAT3 condensates were rapidly disassembled in hypotonic buffer commonly used for cell fractionation points to a limitation of studies of STAT3 biochemistry using hypotonic swelling and mechanical breakage. Overall, the new data help reinterpret IL-6-induced cytoplasmic and nuclear STAT3 bodies as phase-separated biomolecular condensates, and bring the concept of membrane-less organelles to the cytokine-induced STAT transcription factor field and cancer cell biology.
Keywords	interleukin-6 ; cytokine-inducible biomolecular condensates ; cytoplasmic STAT3 sequestering condensates ; nuclear STAT3 bodies ; 1 ; 6-hexanediol ; liquid-like condensates ; Tyr phosphorylation-driven phase transitions ; tonicity-driven phase transitions ; cytokine signaling ; Medicine ; R
Subject code	571
Language	English
Publishing date	2019-02-01T00:00:00Z
Publisher	Termedia Publishing House
Document type	Article ; Online
Database	BASE - Bielefeld Academic Search Engine (life sciences selection)

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Article ; Online: Rapid Reversible Osmoregulation of Cytoplasmic Biomolecular Condensates of Human Interferon-α-Induced Antiviral MxA GTPase

Pravin B. Sehgal / Huijuan Yuan / Ye Jin

International Journal of Molecular Sciences, Vol 23, Iss 12739, p

2022 Volume 12739

Abstract	We previously discovered that exogenously expressed GFP-tagged cytoplasmic human myxovirus resistance protein (MxA), a major antiviral effector of Type I and III interferons (IFNs) against several RNA- and DNA-containing viruses, existed in the cytoplasm in phase-separated membraneless biomolecular condensates of varying sizes and shapes with osmotically regulated disassembly and reassembly. In this study we investigated whether cytoplasmic IFN-α-induced endogenous human MxA structures were also biomolecular condensates, displayed hypotonic osmoregulation and the mechanisms involved. Both IFN-α-induced endogenous MxA and exogenously expressed GFP-MxA formed cytoplasmic condensates in A549 lung and Huh7 hepatoma cells which rapidly disassembled within 1–2 min when cells were exposed to 1,6-hexanediol or to hypotonic buffer (~40–50 mOsm). Both reassembled into new structures within 1–2 min of shifting cells to isotonic culture medium (~330 mOsm). Strikingly, MxA condensates in cells continuously exposed to culture medium of moderate hypotonicity (in the range one-fourth, one-third or one-half isotonicity; range 90–175 mOsm) first rapidly disassembled within 1–3 min, and then, in most cells, spontaneously reassembled 7–15 min later into new structures. This spontaneous reassembly was inhibited by 2-deoxyglucose (thus, was ATP-dependent) and by dynasore (thus, required membrane internalization). Indeed, condensate reassembly was preceded by crowding of the cytosolic space by large vacuole-like dilations (VLDs) derived from internalized plasma membrane. Remarkably, the antiviral activity of GFP-MxA against vesicular stomatitis virus survived hypoosmolar disassembly and subsequent reassembly. The data highlight the exquisite osmosensitivity of MxA condensates, and the preservation of antiviral activity in the face of hypotonic stress.
Keywords	liquid-liquid phase separation (LLPS) ; biomolecular condensates ; membraneless organelles (MLOs) ; endogenous interferon-α-induced human myxovirus resistance protein (MxA) ; osmoregulation ; hypotonic stress ; Biology (General) ; QH301-705.5 ; Chemistry ; QD1-999
Subject code	571
Language	English
Publishing date	2022-10-01T00:00:00Z
Publisher	MDPI AG
Document type	Article ; Online
Database	BASE - Bielefeld Academic Search Engine (life sciences selection)

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Article: Smooth Muscle-Specific

Yang, Yang-Ming / Sehgal, Pravin B

International journal of endocrinology

2018 Volume 2018, Page(s) 3473105

Abstract: ... of the transcription factors STAT5a/b and BCL6 as downstream mediators of this patterned GH-driven sex bias. As a test ...

Abstract	The "estrogen paradox" in pulmonary arterial hypertension (PAH) refers to observations that while there is a higher incidence of idiopathic PAH in women, rodent models of PAH show male dominance and estrogens are protective. To explain these differences, we previously proposed the neuroendocrine-STAT5-BCL6 hypothesis anchored in the sex-biased and species-specific patterns of growth hormone (GH) secretion by the pituitary, the targeting of the hypothalamus by estrogens to feminize GH secretion patterns, and the role of the transcription factors STAT5a/b and BCL6 as downstream mediators of this patterned GH-driven sex bias. As a test of this hypothesis, we previously reported that vascular smooth muscle cell- (SMC-) specific deletion of the
Language	English
Publishing date	2018-07-24
Publishing country	Egypt
Document type	Journal Article
ZDB-ID	2502951-4
ISSN	1687-8345 ; 1687-8337
ISSN (online)	1687-8345
ISSN	1687-8337
DOI	10.1155/2018/3473105
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