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Article: Role of complement and other innate immune mechanisms in the removal of apoptotic cells.

Ogden, Carol Anne / Elkon, Keith B

2006 Volume 9, Page(s) 120–142

Abstract: The complement system is regarded as an ancient host defense mechanism that helps to promote phagocytosis and/or killing of foreign microorganisms. Less well known is the facilitatory role that complement and other closely related molecules of the innate ...

Abstract	The complement system is regarded as an ancient host defense mechanism that helps to promote phagocytosis and/or killing of foreign microorganisms. Less well known is the facilitatory role that complement and other closely related molecules of the innate immune system play in the removal of dying cells. In this chapter, we review the complement system and the mechanisms of complement activation that include natural antibodies and acute phase proteins. The effects of spontaneous and genetically engineered mutations on function of these proteins and their relationship to autoimmune diseases such as lupus are discussed. We also review the known function of non-complement receptors and their roles in recognition and removal of dying cells in normal cellular homeostasis and in inflammation.
MeSH term(s)	Acute-Phase Reaction ; Animals ; Antibodies/immunology ; Antigens, CD/physiology ; Apoptosis ; Calreticulin/physiology ; Complement C1q/physiology ; Complement C3/physiology ; Complement System Proteins/physiology ; Humans ; Immunity, Innate ; Lipopolysaccharide Receptors/physiology ; Low Density Lipoprotein Receptor-Related Protein-1 ; Phagocytes/physiology ; Phagocytosis ; Phosphatidylserines/physiology
Chemical Substances	Antibodies ; Antigens, CD ; Calreticulin ; Complement C3 ; LRP1 protein, human ; Lipopolysaccharide Receptors ; Low Density Lipoprotein Receptor-Related Protein-1 ; Phosphatidylserines ; Complement C1q (80295-33-6) ; Complement System Proteins (9007-36-7)
Language	English
Publishing date	2006
Publishing country	Switzerland
Document type	Journal Article ; Research Support, N.I.H., Extramural ; Review
ISSN	1422-2132
ISSN	1422-2132
DOI	10.1159/000090776
Database	MEDical Literature Analysis and Retrieval System OnLINE

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Article: Single-dose therapy for lupus nephritis: C-reactive protein, nature's own dual scavenger and immunosuppressant.

Ogden, Carol Anne / Elkon, Keith B

Arthritis and rheumatism

2005 Volume 52, Issue 2, Page(s) 378–381

MeSH term(s)	Animals ; C-Reactive Protein/administration & dosage ; Immunosuppression/methods ; Interleukin-10/physiology ; Lupus Erythematosus, Systemic/therapy ; Lupus Nephritis/prevention & control ; Mice ; Mice, Inbred NZB ; Serum Amyloid P-Component/administration & dosage
Chemical Substances	Serum Amyloid P-Component ; Interleukin-10 (130068-27-8) ; PTX3 protein (148591-49-5) ; C-Reactive Protein (9007-41-4)
Language	English
Publishing date	2005-02
Publishing country	United States
Document type	Comment ; Editorial
ZDB-ID	127294-9
ISSN	1529-0131 ; 0004-3591 ; 2326-5191
ISSN (online)	1529-0131
ISSN	0004-3591 ; 2326-5191
DOI	10.1002/art.20847
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Article ; Online: Discovering Molecules That Regulate Efferocytosis Using Primary Human Macrophages and High Content Imaging.

Santulli-Marotto, Sandra / Gervais, Alexis / Fisher, Jamie / Strake, Brandy / Ogden, Carol Anne / Riveley, Chelsea / Giles-Komar, Jill

PloS one

2015 Volume 10, Issue 12, Page(s) e0145078

Abstract: Defective clearance of apoptotic cells can result in sustained inflammation and subsequent autoimmunity. Macrophages, the "professional phagocyte" of the body, are responsible for efficient, non-phlogistic, apoptotic cell clearance. Controlling ... ...

Abstract	Defective clearance of apoptotic cells can result in sustained inflammation and subsequent autoimmunity. Macrophages, the "professional phagocyte" of the body, are responsible for efficient, non-phlogistic, apoptotic cell clearance. Controlling phagocytosis of apoptotic cells by macrophages is an attractive therapeutic opportunity to ameliorate inflammation. Using high content imaging, we have developed a system for evaluating the effects of antibody treatment on apoptotic cell uptake in primary human macrophages by comparing the Phagocytic Index (PI) for each antibody. Herein we demonstrate the feasibility of evaluating a panel of antibodies of unknown specificities obtained by immunization of mice with primary human macrophages and show that they can be distinguished based on individual PI measurements. In this study ~50% of antibodies obtained enhance phagocytosis of apoptotic cells while approximately 5% of the antibodies in the panel exhibit some inhibition. Though the specificities of the majority of antibodies are unknown, two of the antibodies that improved apoptotic cell uptake recognize recombinant MerTK; a receptor known to function in this capacity in vivo. The agonistic impact of these antibodies on efferocytosis could be demonstrated without addition of either of the MerTK ligands, Gas6 or ProS. These results validate applying the mechanism of this fundamental biological process as a means for identification of modulators that could potentially serve as therapeutics. This strategy for interrogating macrophages to discover molecules regulating apoptotic cell uptake is not limited by access to purified protein thereby increasing the possibility of finding novel apoptotic cell uptake pathways.
MeSH term(s)	Animals ; Antibodies/classification ; Antibodies/immunology ; Apoptosis ; Cells, Cultured ; Humans ; Macrophages/immunology ; Mice ; Mice, Inbred BALB C ; Phagocytosis ; Proto-Oncogene Proteins/genetics ; Proto-Oncogene Proteins/immunology ; Receptor Protein-Tyrosine Kinases/genetics ; Receptor Protein-Tyrosine Kinases/immunology ; c-Mer Tyrosine Kinase
Chemical Substances	Antibodies ; Proto-Oncogene Proteins ; MERTK protein, human (EC 2.7.10.1) ; Receptor Protein-Tyrosine Kinases (EC 2.7.10.1) ; c-Mer Tyrosine Kinase (EC 2.7.10.1)
Language	English
Publishing date	2015
Publishing country	United States
Document type	Journal Article
ISSN	1932-6203
ISSN (online)	1932-6203
DOI	10.1371/journal.pone.0145078
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Article ; Online: Discovering Molecules That Regulate Efferocytosis Using Primary Human Macrophages and High Content Imaging.

Sandra Santulli-Marotto / Alexis Gervais / Jamie Fisher / Brandy Strake / Carol Anne Ogden / Chelsea Riveley / Jill Giles-Komar

PLoS ONE, Vol 10, Iss 12, p e

2015 Volume 0145078

Abstract	Defective clearance of apoptotic cells can result in sustained inflammation and subsequent autoimmunity. Macrophages, the "professional phagocyte" of the body, are responsible for efficient, non-phlogistic, apoptotic cell clearance. Controlling phagocytosis of apoptotic cells by macrophages is an attractive therapeutic opportunity to ameliorate inflammation. Using high content imaging, we have developed a system for evaluating the effects of antibody treatment on apoptotic cell uptake in primary human macrophages by comparing the Phagocytic Index (PI) for each antibody. Herein we demonstrate the feasibility of evaluating a panel of antibodies of unknown specificities obtained by immunization of mice with primary human macrophages and show that they can be distinguished based on individual PI measurements. In this study ~50% of antibodies obtained enhance phagocytosis of apoptotic cells while approximately 5% of the antibodies in the panel exhibit some inhibition. Though the specificities of the majority of antibodies are unknown, two of the antibodies that improved apoptotic cell uptake recognize recombinant MerTK; a receptor known to function in this capacity in vivo. The agonistic impact of these antibodies on efferocytosis could be demonstrated without addition of either of the MerTK ligands, Gas6 or ProS. These results validate applying the mechanism of this fundamental biological process as a means for identification of modulators that could potentially serve as therapeutics. This strategy for interrogating macrophages to discover molecules regulating apoptotic cell uptake is not limited by access to purified protein thereby increasing the possibility of finding novel apoptotic cell uptake pathways.
Keywords	Medicine ; R ; Science ; Q
Subject code	616
Language	English
Publisher	Public Library of Science (PLoS)
Document type	Article ; Online
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Article ; Online: Interim results of brentuximab vedotin in combination with nivolumab in patients with relapsed or refractory Hodgkin lymphoma.

Herrera, Alex F / Moskowitz, Alison J / Bartlett, Nancy L / Vose, Julie M / Ramchandren, Radhakrishnan / Feldman, Tatyana A / LaCasce, Ann S / Ansell, Stephen M / Moskowitz, Craig H / Fenton, Keenan / Ogden, Carol Anne / Taft, David / Zhang, Qu / Kato, Kazunobu / Campbell, Mary / Advani, Ranjana H

Blood

2017 Volume 131, Issue 11, Page(s) 1183–1194

Abstract: In this phase 1/2 study, brentuximab vedotin (BV) and nivolumab (Nivo) administered in combination were evaluated as initial salvage therapy in patients with relapsed or refractory (R/R) classical Hodgkin lymphoma (HL). Patients received up to 4 cycles ... ...

Abstract	In this phase 1/2 study, brentuximab vedotin (BV) and nivolumab (Nivo) administered in combination were evaluated as initial salvage therapy in patients with relapsed or refractory (R/R) classical Hodgkin lymphoma (HL). Patients received up to 4 cycles of combination treatment, with BV administered on day 1 and Nivo on day 8 of the first cycle. For cycles 2 to 4, BV and Nivo were both administered on day 1. After study treatment, responses were evaluated by investigators per the 2014 Lugano classification, and patients could proceed to autologous stem cell transplantation (ASCT). Sixty-two patients were enrolled; the complete response rate among all treated patients (n = 61) was 61%, with an objective response rate of 82%. Before ASCT, adverse events (AEs) occurred in 98% of patients, mostly grades 1 and 2. Infusion-related reactions (IRRs) occurred in 44% of patients overall, with 41% of patients experiencing an IRR during at least 1 infusion of BV. Five patients (8%) were treated with systemic steroids for immune-related AEs. A reduction of peripheral T-cell subsets including regulatory T cells was observed after the first dose of BV, and reduced serum levels of thymus- and activation-regulated chemokine concurrent with an increase in proinflammatory cytokines and chemokines were seen after the first BV plus Nivo infusions. The combination of BV plus Nivo was an active and well-tolerated first salvage regimen, potentially providing patients with R/R HL an alternative to traditional chemotherapy. This trial was registered at www.clinicaltrials.gov as #NCT02572167.
MeSH term(s)	Adolescent ; Adult ; Aged ; Antineoplastic Combined Chemotherapy Protocols/administration & dosage ; Antineoplastic Combined Chemotherapy Protocols/adverse effects ; Brentuximab Vedotin ; Chemokines/blood ; Female ; Hodgkin Disease/blood ; Hodgkin Disease/drug therapy ; Hodgkin Disease/pathology ; Humans ; Immunoconjugates/administration & dosage ; Immunoconjugates/adverse effects ; Male ; Middle Aged ; Nivolumab/administration & dosage ; Nivolumab/adverse effects ; Recurrence ; T-Lymphocytes, Regulatory/metabolism ; T-Lymphocytes, Regulatory/pathology
Chemical Substances	Chemokines ; Immunoconjugates ; Nivolumab (31YO63LBSN) ; Brentuximab Vedotin (7XL5ISS668)
Language	English
Publishing date	2017-12-11
Publishing country	United States
Document type	Clinical Trial, Phase I ; Clinical Trial, Phase II ; Journal Article ; Multicenter Study ; Research Support, N.I.H., Extramural ; Research Support, Non-U.S. Gov't
ZDB-ID	80069-7
ISSN	1528-0020 ; 0006-4971
ISSN (online)	1528-0020
ISSN	0006-4971
DOI	10.1182/blood-2017-10-811224
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Article: Innate and adaptive immune response to apoptotic cells.

Peng, Yufeng / Martin, David A / Kenkel, Justin / Zhang, Kang / Ogden, Carol Anne / Elkon, Keith B

Journal of autoimmunity

2007 Volume 29, Issue 4, Page(s) 303–309

Abstract: The immune system is constantly exposed to dying cells, most of which arise during central tolerance and from effete circulating immune cells. Under homeostatic conditions, phagocytes (predominantly macrophages and dendritic cells) belonging to the ... ...

Abstract	The immune system is constantly exposed to dying cells, most of which arise during central tolerance and from effete circulating immune cells. Under homeostatic conditions, phagocytes (predominantly macrophages and dendritic cells) belonging to the innate immune system, rapidly ingest cells and their debris. Apoptotic cell removal requires recognition of altered self on the apoptotic membrane, a process which is facilitated by natural antibodies and serum opsonins. Recognition, may be site and context specific. Uptake and ingestion of apoptotic cells promotes an immunosuppressive environment that avoids inflammatory responses to self-antigens. However, it does not preclude a T cell response and it is likely that constant exposure to self-antigen, particularly by immature dendritic cells, leads to T cell tolerance. Tolerance occurs by several different mechanisms including anergy and deletion (for CD8+T cells) and induction of T regulatory cells (for CD4+T cells). Failed apoptotic cell clearance promotes immune responses to self-antigens, especially when the cellular contents are leaked from the cell (necrosis). Inflammatory responses may be induced by nucleic acid stimulation of Toll like receptors and other immune sensors, specific intracellular proteins and non-protein (uric acid) stimulation of inflammasomes.
MeSH term(s)	Animals ; Apoptosis/immunology ; Autoantigens/immunology ; Humans ; Immune Tolerance ; Immunity, Innate ; Models, Immunological
Chemical Substances	Autoantigens
Language	English
Publishing date	2007-12
Publishing country	England
Document type	Journal Article ; Research Support, N.I.H., Extramural ; Research Support, Non-U.S. Gov't ; Review
ZDB-ID	639452-8
ISSN	0896-8411
ISSN	0896-8411
DOI	10.1016/j.jaut.2007.07.017
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Article ; Online: Transient Receptor Potential Melastatin 2 (TRPM2) ion channel is required for innate immunity against Listeria monocytogenes.

Knowles, Heather / Heizer, Justin W / Li, Yuan / Chapman, Kathryn / Ogden, Carol Anne / Andreasen, Karl / Shapland, Ellen / Kucera, Gary / Mogan, Jennifer / Humann, Jessica / Lenz, Laurel L / Morrison, Alastair D / Perraud, Anne-Laure

Proceedings of the National Academy of Sciences of the United States of America

2011 Volume 108, Issue 28, Page(s) 11578–11583

Abstract: The generation of reactive oxygen species (ROS) is inherent to immune responses. ROS are crucially involved in host defense against pathogens by promoting bacterial killing, but also as signaling agents coordinating the production of cytokines. Transient ...

Abstract	The generation of reactive oxygen species (ROS) is inherent to immune responses. ROS are crucially involved in host defense against pathogens by promoting bacterial killing, but also as signaling agents coordinating the production of cytokines. Transient Receptor Potential Melastatin 2 (TRPM2) is a Ca(2+)-permeable channel gated via binding of ADP-ribose, a metabolite formed under conditions of cellular exposure to ROS. Here, we show that TRPM2-deficient mice are extremely susceptible to infection with Listeria monocytogenes (Lm), exhibiting an inefficient innate immune response. In a comparison with IFNγR-deficient mice, TRPM2(-/-) mice shared similar features of uncontrolled bacterial replication and reduced levels of inducible (i)NOS-expressing monocytes, but had intact IFNγ responsiveness. In contrast, we found that levels of cytokines IL-12 and IFNγ were diminished in TRPM2(-/-) mice following Lm infection, which correlated with their reduced innate activation. Moreover, TRPM2(-/-) mice displayed a higher degree of susceptibility than IL-12-unresponsive mice, and supplementation with recombinant IFNγ was sufficient to reverse the unrestrained bacterial growth and ultimately the lethal phenotype of Lm-infected TRPM2(-/-) mice. The severity of listeriosis we observed in TRPM2(-/-) mice has not been reported for any other ion channel. These findings establish an unsuspected role for ADP-ribose and ROS-mediated cation flux for innate immunity, opening up unique possibilities for immunomodulatory intervention through TRPM2.
MeSH term(s)	Adjuvants, Immunologic/pharmacology ; Animals ; Cytokines/biosynthesis ; Female ; Immunity, Innate/drug effects ; Immunity, Innate/genetics ; Immunity, Innate/physiology ; Interferon-gamma/pharmacology ; Interleukin-12/deficiency ; Interleukin-12/genetics ; Interleukin-12/immunology ; Interleukin-12 Receptor beta 2 Subunit/deficiency ; Interleukin-12 Receptor beta 2 Subunit/genetics ; Interleukin-12 Receptor beta 2 Subunit/immunology ; Listeria monocytogenes/immunology ; Listeria monocytogenes/pathogenicity ; Listeriosis/immunology ; Listeriosis/prevention & control ; Macrophages/immunology ; Male ; Mice ; Mice, Inbred C57BL ; Mice, Knockout ; Neutrophils/immunology ; Receptors, Interferon/deficiency ; Receptors, Interferon/genetics ; Receptors, Interferon/immunology ; Recombinant Proteins ; TRPM Cation Channels/deficiency ; TRPM Cation Channels/genetics ; TRPM Cation Channels/immunology ; Interferon gamma Receptor
Chemical Substances	Adjuvants, Immunologic ; Cytokines ; Interleukin-12 Receptor beta 2 Subunit ; Receptors, Interferon ; Recombinant Proteins ; TRPM Cation Channels ; TRPM2 protein, mouse ; Interleukin-12 (187348-17-0) ; Interferon-gamma (82115-62-6)
Language	English
Publishing date	2011-06-27
Publishing country	United States
Document type	Journal Article ; Research Support, N.I.H., Extramural ; Research Support, Non-U.S. Gov't
ZDB-ID	209104-5
ISSN	1091-6490 ; 0027-8424
ISSN (online)	1091-6490
ISSN	0027-8424
DOI	10.1073/pnas.1010678108
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Article: IGM is required for efficient complement mediated phagocytosis of apoptotic cells in vivo.

Ogden, Carol Anne / Kowalewski, Robert / Peng, Yufeng / Montenegro, Vivianne / Elkon, Keith B

Autoimmunity

2005 Volume 38, Issue 4, Page(s) 259–264

Abstract: A variety of complement components have been detected on apoptotic cells and proposed to facilitate recognition and/or ingestion by phagocytes. The triggers for complement activation remain uncertain. To determine the role of IgM in classical pathway ... ...

Abstract	A variety of complement components have been detected on apoptotic cells and proposed to facilitate recognition and/or ingestion by phagocytes. The triggers for complement activation remain uncertain. To determine the role of IgM in classical pathway activation and clearance of apoptotic cells in vitro and in vivo, we quantified these parameters in mice deficient in serum IgM (sIgM). Phagocytosis by bone marrow-derived macrophages of apoptotic cells incubated with serum deficient in sIgM was markedly reduced, similar to apoptotic cells incubated with C1q deficient serum in vitro. Similarly, intraperitoneal clearance of apoptotic cells and cellular C3 deposition were significantly reduced in mice deficient in sIgM compared to wild-type mice. Clearance and C3 deposition were reconstituted by addback of IgM. In mice deficient in both sIgM and Clq, addback of both serum factors was required for restoration of clearance. These findings indicate that, on a quantitative basis, sIgM is a potent factor required for intraperitoneal phagocytosis of apoptotic cells, and further demonstrate that IgM and C1q work in concert to activate complement, resulting in C3 deposition on the apoptotic cell surface and ultimately, efficient clearance of the apoptotic cell by macrophages.
MeSH term(s)	Animals ; Apoptosis/immunology ; Complement C1q/immunology ; Complement C3/immunology ; Complement Pathway, Classical/immunology ; Female ; Flow Cytometry ; Humans ; Immunoglobulin M/immunology ; Jurkat Cells ; Macrophages, Peritoneal/immunology ; Male ; Mice ; Mice, Inbred C57BL ; Mice, Knockout ; Phagocytosis/immunology ; T-Lymphocytes/immunology
Chemical Substances	Complement C3 ; Immunoglobulin M ; Complement C1q (80295-33-6)
Language	English
Publishing date	2005-07-26
Publishing country	England
Document type	Journal Article ; Research Support, N.I.H., Extramural ; Research Support, Non-U.S. Gov't ; Research Support, U.S. Gov't, P.H.S.
ZDB-ID	1025450-x
ISSN	0891-6934
ISSN	0891-6934
DOI	10.1080/08916930500124452
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Article: Macrophage chemotaxis to apoptotic Burkitt's lymphoma cells in vitro: role of CD14 and CD36.

Truman, Lucy A / Ogden, Carol Anne / Howie, Sarah E M / Gregory, Christopher D

Immunobiology

2004 Volume 209, Issue 1-2, Page(s) 21–30

Abstract: In Burkitt's lymphoma (BL), apoptosis occurs at high frequency alongside uncontrolled proliferation. Macrophages infiltrate these tumours in large numbers and engage in the phagocytic clearance of apoptotic cells in situ. Here we tested the hypothesis ... ...

Abstract	In Burkitt's lymphoma (BL), apoptosis occurs at high frequency alongside uncontrolled proliferation. Macrophages infiltrate these tumours in large numbers and engage in the phagocytic clearance of apoptotic cells in situ. Here we tested the hypothesis that apoptosis of BL cells may provide a mechanism for recruitment of macrophages to these tumours. We show that monocytes and macrophages, but not neutrophils, preferentially migrated to apoptotic BL cells in vitro. Transfection of BL cells with the anti-apoptotic gene bcl-2 both prevented apoptosis and abolished macrophage chemotaxis. Macrophage migration to BL populations correlated well with the number of apoptotic BL cells present (the Pearson correlation r = 0.81, p<0.0001). Chemoattraction of murine macrophages to apoptotic human BL cells demonstrated that the mechanism was conserved across these species. In an attempt to identify the macrophage receptors involved in this process, we investigated whether CD14 and CD36, two receptors important in the phagocytic clearance of apoptotic cells, were also involved in the chemotactic macrophage response. We found that bone marrow-derived macrophages from CD14-/- and CD36-/- mice moved as well as wild-type macrophages in chemotaxis assays towards apoptotic BL cells. Migrating macrophages were found to be up-regulated in their expression of CD14, however, suggesting that, although this receptor does not appear to be required for 'sensing' apoptotic cells, it may be up-regulated on the surface of the migrating macrophage in readiness for apoptotic corpse clearance.
MeSH term(s)	Animals ; Apoptosis ; Burkitt Lymphoma/immunology ; CD36 Antigens/physiology ; Cells, Cultured ; Chemotaxis ; Flow Cytometry ; Humans ; Lipopolysaccharide Receptors/physiology ; Macrophages/physiology ; Mice ; Mice, Inbred BALB C ; Mice, Inbred C57BL ; Tumor Cells, Cultured ; Up-Regulation
Chemical Substances	CD36 Antigens ; Lipopolysaccharide Receptors
Language	English
Publishing date	2004
Publishing country	Netherlands
Document type	Journal Article ; Research Support, Non-U.S. Gov't
ZDB-ID	563292-4
ISSN	1878-3279 ; 0171-2985
ISSN (online)	1878-3279
ISSN	0171-2985
DOI	10.1016/j.imbio.2004.02.001
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Article ; Online: Oncogenic properties of apoptotic tumor cells in aggressive B cell lymphoma.

Current biology : CB

2015 Volume 25, Issue 5, Page(s) 577–588

Abstract: Background: Cells undergoing apoptosis are known to modulate their tissue microenvironments. By acting on phagocytes, notably macrophages, apoptotic cells inhibit immunological and inflammatory responses and promote trophic signaling pathways. ... ...

Abstract	Background: Cells undergoing apoptosis are known to modulate their tissue microenvironments. By acting on phagocytes, notably macrophages, apoptotic cells inhibit immunological and inflammatory responses and promote trophic signaling pathways. Paradoxically, because of their potential to cause death of tumor cells and thereby militate against malignant disease progression, both apoptosis and tumor-associated macrophages (TAMs) are often associated with poor prognosis in cancer. We hypothesized that, in progression of malignant disease, constitutive loss of a fraction of the tumor cell population through apoptosis could yield tumor-promoting effects. Results: Here, we demonstrate that apoptotic tumor cells promote coordinated tumor growth, angiogenesis, and accumulation of TAMs in aggressive B cell lymphomas. Through unbiased "in situ transcriptomics" analysis-gene expression profiling of laser-captured TAMs to establish their activation signature in situ-we show that these cells are activated to signal via multiple tumor-promoting reparatory, trophic, angiogenic, tissue remodeling, and anti-inflammatory pathways. Our results also suggest that apoptotic lymphoma cells help drive this signature. Furthermore, we demonstrate that, upon induction of apoptosis, lymphoma cells not only activate expression of the tumor-promoting matrix metalloproteinases MMP2 and MMP12 in macrophages but also express and process these MMPs directly. Finally, using a model of malignant melanoma, we show that the oncogenic potential of apoptotic tumor cells extends beyond lymphoma. Conclusions: In addition to its profound tumor-suppressive role, apoptosis can potentiate cancer progression. These results have important implications for understanding the fundamental biology of cell death, its roles in malignant disease, and the broader consequences of apoptosis-inducing anti-cancer therapy.
MeSH term(s)	Analysis of Variance ; Apoptosis/physiology ; Cell Proliferation/physiology ; Fluorescence ; Gene Expression Profiling ; Gene Expression Regulation, Neoplastic/physiology ; Histological Techniques ; Humans ; Kaplan-Meier Estimate ; Lymphoma, B-Cell/physiopathology ; Macrophages/physiology ; Matrix Metalloproteinases/metabolism ; Melanoma, Experimental/physiopathology ; Neovascularization, Pathologic/physiopathology ; Phagocytes/physiology ; Signal Transduction/physiology ; Tumor Microenvironment/physiology
Chemical Substances	Matrix Metalloproteinases (EC 3.4.24.-)
Language	English
Publishing date	2015-02-19
Publishing country	England
Document type	Journal Article ; Research Support, Non-U.S. Gov't
ZDB-ID	1071731-6
ISSN	1879-0445 ; 0960-9822
ISSN (online)	1879-0445
ISSN	0960-9822
DOI	10.1016/j.cub.2014.12.059
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