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Article: Maturation of phagosomes containing different erythrophagocytic particles in primary macrophages.

Santarino, Inês B / Vieira, Otília V

2017 Volume 7, Issue 9, Page(s) 1281–1290

Abstract: Erythrophagocytosis is a physiological process that aims to remove damaged red blood cells from the circulation in order to avoid hemolysis and uncontrolled liberation of iron. Many efforts have been made to understand heme trafficking inside macrophages, ...

Abstract	Erythrophagocytosis is a physiological process that aims to remove damaged red blood cells from the circulation in order to avoid hemolysis and uncontrolled liberation of iron. Many efforts have been made to understand heme trafficking inside macrophages, but little is known about the maturation of phagosomes containing different types of erythrophagocytic particles with different signals at their surfaces. Therefore, we performed a comparative study on the maturation of phagosomes containing three different models of red blood cells (RBC): aged/senescent, complement-opsonized, and IgG-opsonized. We also used two types of professional phagocytes: bone marrow-derived and peritoneal macrophages. By comparing markers from different stages of phagosomal maturation, we found that phagosomes carrying aged RBC reach lysosomes with a delay compared to those containing IgG- or complement-opsonized RBC, in both types of macrophages. These findings contribute to understanding the importance of the different signals at the RBC surface in phagolysosome biogenesis, as well as in the dynamics of RBC removal.
Language	English
Publishing date	2017-08-23
Publishing country	England
Document type	Journal Article
ZDB-ID	2651702-4
ISSN	2211-5463
ISSN	2211-5463
DOI	10.1002/2211-5463.12262
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Article: Maturation of phagosomes containing different erythrophagocytic particles in primary macrophages

Santarino, Inês B. / Vieira, Otília V.

FEBS Open Bio. 2017 Sept., v. 7, no. 9

2017

Abstract	Erythrophagocytosis is a physiological process that aims to remove damaged red blood cells from the circulation in order to avoid hemolysis and uncontrolled liberation of iron. Many efforts have been made to understand heme trafficking inside macrophages, but little is known about the maturation of phagosomes containing different types of erythrophagocytic particles with different signals at their surfaces. Therefore, we performed a comparative study on the maturation of phagosomes containing three different models of red blood cells (RBC): aged/senescent, complement‐opsonized, and IgG‐opsonized. We also used two types of professional phagocytes: bone marrow‐derived and peritoneal macrophages. By comparing markers from different stages of phagosomal maturation, we found that phagosomes carrying aged RBC reach lysosomes with a delay compared to those containing IgG‐ or complement‐opsonized RBC, in both types of macrophages. These findings contribute to understanding the importance of the different signals at the RBC surface in phagolysosome biogenesis, as well as in the dynamics of RBC removal.
Keywords	biogenesis ; blood ; comparative study ; heme ; hemolysis ; iron ; lysosomes ; macrophages ; phagosomes
Language	English
Dates of publication	2017-09
Size	p. 1281-1290.
Publishing place	John Wiley & Sons, Ltd
Document type	Article
Note	JOURNAL ARTICLE
ZDB-ID	2651702-4
ISSN	2211-5463
ISSN	2211-5463
DOI	10.1002/2211-5463.12262
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Article ; Online: Maturation of phagosomes containing different erythrophagocytic particles in primary macrophages

Inês B. Santarino / Otília V. Vieira

FEBS Open Bio, Vol 7, Iss 9, Pp 1281-

2017 Volume 1290

Abstract	Erythrophagocytosis is a physiological process that aims to remove damaged red blood cells from the circulation in order to avoid hemolysis and uncontrolled liberation of iron. Many efforts have been made to understand heme trafficking inside macrophages, but little is known about the maturation of phagosomes containing different types of erythrophagocytic particles with different signals at their surfaces. Therefore, we performed a comparative study on the maturation of phagosomes containing three different models of red blood cells (RBC): aged/senescent, complement‐opsonized, and IgG‐opsonized. We also used two types of professional phagocytes: bone marrow‐derived and peritoneal macrophages. By comparing markers from different stages of phagosomal maturation, we found that phagosomes carrying aged RBC reach lysosomes with a delay compared to those containing IgG‐ or complement‐opsonized RBC, in both types of macrophages. These findings contribute to understanding the importance of the different signals at the RBC surface in phagolysosome biogenesis, as well as in the dynamics of RBC removal.
Keywords	complement‐opsonized red blood cells ; aged red blood cells ; erythrophagocytosis ; IgG‐opsonized Red Blood Cells ; phagosomal maturation ; Biology (General) ; QH301-705.5
Subject code	616
Language	English
Publishing date	2017-09-01T00:00:00Z
Publisher	Wiley
Document type	Article ; Online
Database	BASE - Bielefeld Academic Search Engine (life sciences selection)

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Article ; Online: Involvement of the p62/NRF2 signal transduction pathway on erythrophagocytosis.

Santarino, Inês B / Viegas, Michelle S / Domingues, Neuza S / Ribeiro, Ana M / Soares, Miguel P / Vieira, Otília V

Scientific reports

2017 Volume 7, Issue 1, Page(s) 5812

Abstract: Erythrophagocytosis, the phagocytic removal of damaged red blood cells (RBC), and subsequent phagolysosome biogenesis are important processes in iron/heme metabolism and homeostasis. Phagolysosome biogenesis implies the interaction of nascent phagosomes ... ...

Abstract	Erythrophagocytosis, the phagocytic removal of damaged red blood cells (RBC), and subsequent phagolysosome biogenesis are important processes in iron/heme metabolism and homeostasis. Phagolysosome biogenesis implies the interaction of nascent phagosomes with endocytic compartments and also autophagy effectors. Here, we report that besides recruitment of microtubule-associated protein-1-light chain 3 (LC3), additional autophagy machinery such as sequestosome 1 (p62) is also acquired by single-membrane phagosomes at very early stages of the phagocytic process and that its acquisition is very important to the outcome of the process. In bone marrow-derived macrophages (BMDM) silenced for p62, RBC degradation is inhibited. P62, is also required for nuclear translocation and activation of the transcription factor Nuclear factor E2-related Factor 2 (NRF2) during erythrophagocytosis. Deletion of the Nrf2 allele reduces p62 expression and compromises RBC degradation. In conclusion, we reveal that erythrophagocytosis relies on an interplay between p62 and NRF2, potentially acting as protective mechanism to maintain reactive oxygen species at basal levels and preserve macrophage homeostasis.
MeSH term(s)	Animals ; Autophagy ; Cell Line ; Erythrocytes/cytology ; Erythrocytes/metabolism ; Gene Expression Regulation ; Humans ; Intracellular Space/metabolism ; Mice, Inbred C57BL ; Mice, Knockout ; Microtubule-Associated Proteins ; NF-E2-Related Factor 2/metabolism ; Phagocytosis ; Phagosomes/metabolism ; Phosphorylation ; Rabbits ; Sequestosome-1 Protein/metabolism ; Signal Transduction ; Ubiquitin/metabolism
Chemical Substances	Map1lc3b protein, mouse ; Microtubule-Associated Proteins ; NF-E2-Related Factor 2 ; Sequestosome-1 Protein ; Sqstm1 protein, mouse ; Ubiquitin
Language	English
Publishing date	2017-07-19
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/s41598-017-05687-1
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Article ; Online: Involvement of the p62/NRF2 signal transduction pathway on erythrophagocytosis

Inês B. Santarino / Michelle S. Viegas / Neuza S. Domingues / Ana M. Ribeiro / Miguel P. Soares / Otília V. Vieira

Scientific Reports, Vol 7, Iss 1, Pp 1-

2017 Volume 16

Abstract: Abstract Erythrophagocytosis, the phagocytic removal of damaged red blood cells (RBC), and subsequent phagolysosome biogenesis are important processes in iron/heme metabolism and homeostasis. Phagolysosome biogenesis implies the interaction of nascent ... ...

Abstract	Abstract Erythrophagocytosis, the phagocytic removal of damaged red blood cells (RBC), and subsequent phagolysosome biogenesis are important processes in iron/heme metabolism and homeostasis. Phagolysosome biogenesis implies the interaction of nascent phagosomes with endocytic compartments and also autophagy effectors. Here, we report that besides recruitment of microtubule-associated protein-1-light chain 3 (LC3), additional autophagy machinery such as sequestosome 1 (p62) is also acquired by single-membrane phagosomes at very early stages of the phagocytic process and that its acquisition is very important to the outcome of the process. In bone marrow-derived macrophages (BMDM) silenced for p62, RBC degradation is inhibited. P62, is also required for nuclear translocation and activation of the transcription factor Nuclear factor E2-related Factor 2 (NRF2) during erythrophagocytosis. Deletion of the Nrf2 allele reduces p62 expression and compromises RBC degradation. In conclusion, we reveal that erythrophagocytosis relies on an interplay between p62 and NRF2, potentially acting as protective mechanism to maintain reactive oxygen species at basal levels and preserve macrophage homeostasis.
Keywords	Medicine ; R ; Science ; Q
Language	English
Publishing date	2017-07-01T00:00:00Z
Publisher	Nature Portfolio
Document type	Article ; Online
Database	BASE - Bielefeld Academic Search Engine (life sciences selection)

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Article ; Online: Human colon adenocarcinoma HT-29 cell: electrochemistry and nicotine stimulation.

Oliveira, S C B / Santarino, I B / Enache, T A / Nunes, C / Laranjinha, J / Barbosa, R M / Oliveira-Brett, A M

Bioelectrochemistry (Amsterdam, Netherlands)

2013 Volume 94, Page(s) 30–38

Abstract: Recently, it was demonstrated that colorectal cancer HT-29 cells can secrete epinephrine (adrenaline) in an autocrine manner to auto-stimulate cellular growth by adrenoreceptors activation, and that this secretion is enhanced by nicotine, showing an ... ...

Abstract	Recently, it was demonstrated that colorectal cancer HT-29 cells can secrete epinephrine (adrenaline) in an autocrine manner to auto-stimulate cellular growth by adrenoreceptors activation, and that this secretion is enhanced by nicotine, showing an indirect relation between colorectal cancer and tobacco. The electrochemical behaviour of human colon adenocarcinoma HT-29 cells from a colorectal adenocarcinoma cell line, the hormone and neurotransmitter epinephrine, and nicotine, were investigated by cyclic voltammetry, using indium tin oxide (ITO), glassy carbon (GC) and screen printed carbon (SPC) electrodes. The oxidation of the HT-29 cells, previously grown onto ITO or SPC surfaces, followed an irreversible oxidation process that involved the formation of a main oxidation product that undergoes irreversible reduction, as in the epinephrine oxidation mechanism. The effect of nicotine stimulation of the HT-29 cells was also investigated. Nicotine, at different concentration levels 1, 2 and 15 mM, was introduced in the culture medium and an increase with incubation time, 0 to 3h and 30 min, of the HT-29 cells oxidation and reduction peaks was observed. The interaction of nicotine with the HT-29 cells stimulated the epinephrine secretion causing an increase in epinephrine release concentration, and enabling the conclusion that epinephrine and nicotine play an important role in the colorectal tumour growth.
MeSH term(s)	Adenocarcinoma/chemistry ; Adenocarcinoma/pathology ; Carbon/chemistry ; Cell Proliferation/drug effects ; Colonic Neoplasms/chemistry ; Colonic Neoplasms/pathology ; Electrochemistry ; Electrodes ; Epinephrine/pharmacology ; HT29 Cells ; Humans ; Nicotine/pharmacology ; Oxidation-Reduction/drug effects ; Tin Compounds/chemistry ; Tin Compounds/therapeutic use
Chemical Substances	Tin Compounds ; Nicotine (6M3C89ZY6R) ; indium tin oxide (71243-84-0) ; Carbon (7440-44-0) ; Epinephrine (YKH834O4BH)
Language	English
Publishing date	2013-12
Publishing country	Netherlands
Document type	Journal Article ; Research Support, Non-U.S. Gov't
ZDB-ID	2010650-6
ISSN	1878-562X ; 0302-4598 ; 1567-5394
ISSN (online)	1878-562X
ISSN	0302-4598 ; 1567-5394
DOI	10.1016/j.bioelechem.2013.05.004
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Article ; Online: A Rab3a-dependent complex essential for lysosome positioning and plasma membrane repair.

Encarnação, Marisa / Espada, Lília / Escrevente, Cristina / Mateus, Denisa / Ramalho, José / Michelet, Xavier / Santarino, Inês / Hsu, Victor W / Brenner, Michael B / Barral, Duarte C / Vieira, Otília V

The Journal of cell biology

2016 Volume 213, Issue 6, Page(s) 631–640

Abstract: Lysosome exocytosis plays a major role in resealing plasma membrane (PM) disruptions. This process involves two sequential steps. First, lysosomes are recruited to the periphery of the cell and then fuse with the damaged PM. However, the trafficking ... ...

Abstract	Lysosome exocytosis plays a major role in resealing plasma membrane (PM) disruptions. This process involves two sequential steps. First, lysosomes are recruited to the periphery of the cell and then fuse with the damaged PM. However, the trafficking molecular machinery involved in lysosome exocytosis and PM repair (PMR) is poorly understood. We performed a systematic screen of the human Rab family to identify Rabs required for lysosome exocytosis and PMR. Rab3a, which partially localizes to peripheral lysosomes, was one of the most robust hits. Silencing of Rab3a or its effector, synaptotagmin-like protein 4a (Slp4-a), leads to the collapse of lysosomes to the perinuclear region and inhibition of PMR. Importantly, we have also identified a new Rab3 effector, nonmuscle myosin heavy chain IIA, as part of the complex formed by Rab3a and Slp4-a that is responsible for lysosome positioning at the cell periphery and lysosome exocytosis.
MeSH term(s)	Cell Line ; Cell Line, Tumor ; Cell Membrane/metabolism ; Cell Membrane/physiology ; Exocytosis/physiology ; HEK293 Cells ; HeLa Cells ; Humans ; Leukocytes, Mononuclear ; Lysosomes/metabolism ; Lysosomes/physiology ; Myosin Heavy Chains/metabolism ; Vesicular Transport Proteins/metabolism ; rab3A GTP-Binding Protein/metabolism
Chemical Substances	SYTL4 protein, human ; Vesicular Transport Proteins ; Myosin Heavy Chains (EC 3.6.4.1) ; rab3A GTP-Binding Protein (EC 3.6.5.2)
Language	English
Publishing date	2016--20
Publishing country	United States
Document type	Journal Article
ZDB-ID	218154-x
ISSN	1540-8140 ; 0021-9525
ISSN (online)	1540-8140
ISSN	0021-9525
DOI	10.1083/jcb.201511093
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Article: Cholesteryl hemiesters alter lysosome structure and function and induce proinflammatory cytokine production in macrophages.

Domingues, Neuza / Estronca, Luís M B B / Silva, João / Encarnação, Marisa R / Mateus, Rita / Silva, Diogo / Santarino, Inês B / Saraiva, Margarida / Soares, Maria I L / Pinho E Melo, Teresa M V D / Jacinto, António / Vaz, Winchil L C / Vieira, Otília V

Biochimica et biophysica acta. Molecular and cell biology of lipids

2016 Volume 1862, Issue 2, Page(s) 210–220

Abstract: Rationale: Cholesteryl hemiesters are oxidation products of polyunsaturated fatty acid esters of cholesterol. Their oxo-ester precursors have been identified as important components of the "core aldehydes" of human atheromata and in oxidized ... ...

Abstract	Rationale: Cholesteryl hemiesters are oxidation products of polyunsaturated fatty acid esters of cholesterol. Their oxo-ester precursors have been identified as important components of the "core aldehydes" of human atheromata and in oxidized lipoproteins (Ox-LDL). We had previously shown, for the first time, that a single compound of this family, cholesteryl hemisuccinate (ChS), is sufficient to cause irreversible lysosomal lipid accumulation (lipidosis), and is toxic to macrophages. These features, coupled to others such as inflammation, are typically seen in atherosclerosis. Objective: To obtain insights into the mechanism of cholesteryl hemiester-induced pathological changes in lysosome function and induction of inflammation in vitro and assess their impact in vivo. Methods and results: We have examined the effects of ChS on macrophages (murine cell lines and primary cultures) in detail. Specifically, lysosomal morphology, pH, and proteolytic capacity were examined. Exposure of macrophages to sub-toxic ChS concentrations caused enlargement of the lysosomes, changes in their luminal pH, and accumulation of cargo in them. In primary mouse bone marrow-derived macrophages (BMDM), ChS-exposure increased the secretion of IL-1β, TNF-α and IL-6. In zebrafish larvae (wild-type AB and PU.1:EGFP), fed with a ChS-enriched diet, we observed lipid accumulation, myeloid cell-infiltration in their vasculature and decrease in larval survival. Under the same conditions the effects of ChS were more profound than the effects of free cholesterol (FC). Conclusions: Our data strongly suggest that cholesteryl hemiesters are pro-atherogenic lipids able to mimic features of Ox-LDL both in vitro and in vivo.
MeSH term(s)	Animals ; Atherosclerosis/metabolism ; Cell Line ; Cholesterol/metabolism ; Cholesterol Esters/metabolism ; Esters/metabolism ; Humans ; Hydrogen-Ion Concentration ; Inflammation/metabolism ; Interleukin-1beta/metabolism ; Interleukin-6/metabolism ; Larva/metabolism ; Lipidoses/metabolism ; Lysosomes/metabolism ; Macrophages/metabolism ; Mice ; RAW 264.7 Cells ; Tumor Necrosis Factor-alpha/metabolism ; Zebrafish
Chemical Substances	Cholesterol Esters ; Esters ; Interleukin-1beta ; Interleukin-6 ; Tumor Necrosis Factor-alpha ; Cholesterol (97C5T2UQ7J) ; cholesteryl succinate (T3J4KS4201)
Language	English
Publishing date	2016-10-26
Publishing country	Netherlands
Document type	Journal Article ; Research Support, Non-U.S. Gov't
ZDB-ID	60-7
ISSN	1879-2596 ; 1879-260X ; 1872-8006 ; 1879-2642 ; 1879-2618 ; 1879-2650 ; 1879-2618 ; 0006-3002 ; 0005-2728 ; 0005-2736 ; 0304-4165 ; 0167-4838 ; 1388-1981 ; 0167-4889 ; 0167-4781 ; 0304-419X ; 1570-9639 ; 0925-4439 ; 1874-9399
ISSN (online)	1879-2596 ; 1879-260X ; 1872-8006 ; 1879-2642 ; 1879-2618 ; 1879-2650
ISSN	1879-2618 ; 0006-3002 ; 0005-2728 ; 0005-2736 ; 0304-4165 ; 0167-4838 ; 1388-1981 ; 0167-4889 ; 0167-4781 ; 0304-419X ; 1570-9639 ; 0925-4439 ; 1874-9399
DOI	10.1016/j.bbalip.2016.10.009
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Article: Cholesteryl hemiesters alter lysosome structure and function and induce proinflammatory cytokine production in macrophages

Domingues, Neuza / António Jacinto / Diogo Silva / Inês B. Santarino / João Silva / Luís M.B.B. Estronca / Margarida Saraiva / Maria I.L. Soares / Marisa R. Encarnação / Otília V. Vieira / Rita Mateus / Teresa M.V.D. Pinho e Melo / Winchil L.C. Vaz

Biochimica et biophysica acta. 2017 Feb., v. 1862, no. 2

2017

Abstract: Cholesteryl hemiesters are oxidation products of polyunsaturated fatty acid esters of cholesterol. Their oxo-ester precursors have been identified as important components of the “core aldehydes” of human atheromata and in oxidized lipoproteins (Ox-LDL). ... ...

Abstract	Cholesteryl hemiesters are oxidation products of polyunsaturated fatty acid esters of cholesterol. Their oxo-ester precursors have been identified as important components of the “core aldehydes” of human atheromata and in oxidized lipoproteins (Ox-LDL). We had previously shown, for the first time, that a single compound of this family, cholesteryl hemisuccinate (ChS), is sufficient to cause irreversible lysosomal lipid accumulation (lipidosis), and is toxic to macrophages. These features, coupled to others such as inflammation, are typically seen in atherosclerosis.To obtain insights into the mechanism of cholesteryl hemiester-induced pathological changes in lysosome function and induction of inflammation in vitro and assess their impact in vivo.We have examined the effects of ChS on macrophages (murine cell lines and primary cultures) in detail. Specifically, lysosomal morphology, pH, and proteolytic capacity were examined. Exposure of macrophages to sub-toxic ChS concentrations caused enlargement of the lysosomes, changes in their luminal pH, and accumulation of cargo in them. In primary mouse bone marrow-derived macrophages (BMDM), ChS-exposure increased the secretion of IL-1β, TNF-α and IL-6. In zebrafish larvae (wild-type AB and PU.1:EGFP), fed with a ChS-enriched diet, we observed lipid accumulation, myeloid cell-infiltration in their vasculature and decrease in larval survival. Under the same conditions the effects of ChS were more profound than the effects of free cholesterol (FC).Our data strongly suggest that cholesteryl hemiesters are pro-atherogenic lipids able to mimic features of Ox-LDL both in vitro and in vivo.
Keywords	aldehydes ; cholesterol ; cholesteryl esters ; Danio rerio ; diet ; fatty acid esters ; humans ; inflammation ; interleukin-1beta ; interleukin-6 ; larvae ; lipoproteins ; lysosomes ; macrophages ; mice ; oxidation ; pH ; polyunsaturated fatty acids ; proteolysis ; secretion ; toxicity ; tumor necrosis factor-alpha
Language	English
Dates of publication	2017-02
Size	p. 210-220.
Publishing place	Elsevier B.V.
Document type	Article
ISSN	1388-1981
DOI	10.1016/j.bbalip.2016.10.009
Database	NAL-Catalogue (AGRICOLA)

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