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Article ; Online: Periodontal Pathogens' strategies disarm neutrophils to promote dysregulated inflammation.

Miralda, Irina / Uriarte, Silvia M

2020 Volume 36, Issue 2, Page(s) 103–120

Abstract: Periodontitis is an irreversible, chronic inflammatory disease where inflammophilic pathogenic microbial communities accumulate in the gingival crevice. Neutrophils are a major component of the innate host response against bacterial challenge, and under ... ...

Abstract	Periodontitis is an irreversible, chronic inflammatory disease where inflammophilic pathogenic microbial communities accumulate in the gingival crevice. Neutrophils are a major component of the innate host response against bacterial challenge, and under homeostatic conditions, their microbicidal functions typically protect the host against periodontitis. However, a number of periodontal pathogens developed survival strategies to evade neutrophil microbicidal functions while promoting inflammation, which provides a source of nutrients for bacterial growth. Research on periodontal pathogens has largely focused on a few established species: Tannerella forsythia, Treponema denticola, Fusobacterium nucleatum, Aggregatibacter actinomycetemcomitans, and Porphyromonas gingivalis. However, advances in culture-independent techniques have facilitated the identification of new bacterial species in periodontal lesions, such as the two Gram-positive anaerobes, Filifactor alocis and Peptoanaerobacter stomatis, whose characterization of pathogenic potential has not been fully described. Additionally, there is not a full understanding of the pathogenic mechanisms used against neutrophils by organisms that are abundant in periodontal lesions. This presents a substantial barrier to the development of new approaches to prevent or ameliorate the disease. In this review, we first summarize the neutrophil functions affected by the established periodontal pathogens listed above, denoting unknown areas that still merit a closer look. Then, we review the literature on neutrophil functions and the emerging periodontal pathogens, F. alocis and P. stomatis, comparing the effects of the emerging microbes to that of established pathogens, and speculate on the contribution of these putative pathogens to the progression of periodontal disease.
MeSH term(s)	Aggregatibacter actinomycetemcomitans ; Clostridiales ; Humans ; Inflammation ; Neutrophils ; Porphyromonas gingivalis ; Treponema denticola
Language	English
Publishing date	2020-12-31
Publishing country	Denmark
Document type	Journal Article ; Research Support, N.I.H., Extramural ; Review
ZDB-ID	2537726-7
ISSN	2041-1014 ; 2041-1006
ISSN (online)	2041-1014
ISSN	2041-1006
DOI	10.1111/omi.12321
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Article ; Online: Neutrophilic asthma at an inhibitory checkpoint: A PD-1-targeted approach.

Samanas, Nyssa B / Murphy, Ryan C / Miralda, Irina / Hallstrand, Teal S / Piliponsky, Adrian M

The Journal of allergy and clinical immunology

2022 Volume 151, Issue 2, Page(s) 420–422

MeSH term(s)	Humans ; Programmed Cell Death 1 Receptor ; Asthma/drug therapy ; Lung ; Neutrophils ; Eosinophils ; Inflammation
Chemical Substances	Programmed Cell Death 1 Receptor
Language	English
Publishing date	2022-12-02
Publishing country	United States
Document type	Editorial ; Comment
ZDB-ID	121011-7
ISSN	1097-6825 ; 1085-8725 ; 0091-6749
ISSN (online)	1097-6825 ; 1085-8725
ISSN	0091-6749
DOI	10.1016/j.jaci.2022.11.014
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Article: Human Neutrophil Granule Exocytosis in Response to

Miralda, Irina / Klaes, Christopher K / Graham, James E / Uriarte, Silvia M

Pathogens (Basel, Switzerland)

2020 Volume 9, Issue 2

Abstract: Mycobacterium ... ...

Abstract	Mycobacterium smegmatis
Language	English
Publishing date	2020-02-15
Publishing country	Switzerland
Document type	Journal Article
ZDB-ID	2695572-6
ISSN	2076-0817
ISSN	2076-0817
DOI	10.3390/pathogens9020123
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Article ; Online: The emerging oral pathogen, Filifactor alocis, extends the functional lifespan of human neutrophils.

Miralda, Irina / Vashishta, Aruna / Rogers, Max N / Lamont, Richard J / Uriarte, Silvia M

Molecular microbiology

2022 Volume 117, Issue 6, Page(s) 1340–1351

Abstract: Periodontitis is a chronic inflammatory infectious disease that affects the integrity of tooth-supporting tissues and has adverse systemic consequences. Advances in sequencing technologies have uncovered organisms that are exclusively found in high ... ...

Abstract	Periodontitis is a chronic inflammatory infectious disease that affects the integrity of tooth-supporting tissues and has adverse systemic consequences. Advances in sequencing technologies have uncovered organisms that are exclusively found in high numbers in periodontal lesions, such as the gram-positive anaerobic rod, Filifactor alocis. F. alocis can manipulate neutrophil effector functions, which allows the organism to survive within these granulocytes. Several neutrophil functions have been tested in the context of F. alocis challenge, but the effect of the organism on neutrophil apoptosis is still unknown. RNA sequencing of human neutrophils challenged with F. alocis showed that apoptosis pathways were differentially regulated. Compared to media-cultured controls, F. alocis-challenged neutrophils maintain their nuclear morphology, do not stain for Annexin V or 7-AAD, and have decreased DNA fragmentation. Inhibition of apoptosis by F. alocis involved reduced caspase-3, -8, and - 9 activation and upregulation of important anti-apoptotic proteins. Prolonged lifespan was dependent on contact through TLR2/6, and F. alocis-challenged neutrophils retained their functional capacity to induce inflammation for longer timepoints. This is the first in-depth characterization of neutrophil apoptotic programs in response to an oral pathogen and provides key information on how bacteria manipulate immune cell mechanisms to maintain a dysregulated inflammatory response.
MeSH term(s)	Clostridiales ; Humans ; Longevity ; Neutrophils/microbiology ; Periodontitis/microbiology
Language	English
Publishing date	2022-04-29
Publishing country	England
Document type	Journal Article ; Research Support, N.I.H., Extramural ; Research Support, Non-U.S. Gov't
ZDB-ID	619315-8
ISSN	1365-2958 ; 0950-382X
ISSN (online)	1365-2958
ISSN	0950-382X
DOI	10.1111/mmi.14911
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Article: Neutrophil Interaction with Emerging Oral Pathogens: A Novel View of the Disease Paradigm.

Miralda, Irina / Vashishta, Aruna / Uriarte, Silvia M

Advances in experimental medicine and biology

2019 Volume 1197, Page(s) 165–178

Abstract: Periodontitis is a multifactorial chronic inflammatory infectious disease that compromises the integrity of tooth-supporting tissues. The disease progression depends on the disruption of host-microbe homeostasis in the periodontal tissue. This disruption ...

Abstract	Periodontitis is a multifactorial chronic inflammatory infectious disease that compromises the integrity of tooth-supporting tissues. The disease progression depends on the disruption of host-microbe homeostasis in the periodontal tissue. This disruption is marked by a shift in the composition of the polymicrobial oral community from a symbiotic to a dysbiotic, more complex community that is capable of evading killing while promoting inflammation. Neutrophils are the main phagocytic cell in the periodontal pocket, and the outcome of the interaction with the oral microbiota is an important determinant of oral health. Novel culture-independent techniques have facilitated the identification of new bacterial species at periodontal lesions and induced a reappraisal of the microbial etiology of periodontitis. In this chapter, we discuss how neutrophils interact with two emerging oral pathogens, Filifactor alocis and Peptoanaerobacter stomatis, and the different strategies deploy by these organisms to modulate neutrophil effector functions, with the goal to outline a new paradigm in our knowledge about neutrophil responses to putative periodontal pathogens and their contribution to disease progression.
MeSH term(s)	Clostridiales/immunology ; Dysbiosis ; Humans ; Microbiota/immunology ; Neutrophils/immunology ; Neutrophils/microbiology ; Periodontitis/immunology ; Periodontitis/microbiology ; Periodontium/microbiology
Language	English
Publishing date	2019-11-15
Publishing country	United States
Document type	Journal Article ; Review
ISSN	2214-8019 ; 0065-2598
ISSN (online)	2214-8019
ISSN	0065-2598
DOI	10.1007/978-3-030-28524-1_12
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Article: Human Neutrophil Granule Exocytosis in Response to Mycobacterium smegmatis

Miralda, Irina / Klaes, Christopher K / Graham, James E / Uriarte, Silvia M

Pathogens. 2020 Feb. 15, v. 9, no. 2

2020

Abstract: Mycobacterium smegmatis rarely causes disease in the immunocompetent, but reported cases of soft tissue infection describe abscess formation requiring surgical debridement for resolution. Neutrophils are the first innate immune cells to accumulate at ... ...

Abstract	Mycobacterium smegmatis rarely causes disease in the immunocompetent, but reported cases of soft tissue infection describe abscess formation requiring surgical debridement for resolution. Neutrophils are the first innate immune cells to accumulate at sites of bacterial infection, where reactive oxygen species and proteolytic enzymes are used to kill microbial invaders. As these phagocytic cells play central roles in protection from most bacteria, we assessed human neutrophil phagocytosis and granule exocytosis in response to serum opsonized or non-opsonized M. smegmatis mc². Although phagocytosis was enhanced by serum opsonization, M. smegmatis did not induce exocytosis of secretory vesicles or azurophilic granules at any time point tested, with or without serum opsonization. At early time points, opsonized M. smegmatis induced significant gelatinase granule exocytosis compared to non-opsonized bacteria. Differences in granule release between opsonized and non-opsonized M. smegmatis decreased in magnitude over the time course examined, with bacteria also evoking specific granule exocytosis by six hours after addition to cultured primary single-donor human neutrophils. Supernatants from neutrophils challenged with opsonized M. smegmatis were able to digest gelatin, suggesting that complement and gelatinase granule exocytosis can contribute to neutrophil-mediated tissue damage seen in these rare soft tissue infections.
Keywords	Mycobacterium smegmatis ; abscess ; bacteria ; bacterial infections ; blood serum ; complement ; cytoplasmic granules ; debridement ; exocytosis ; gelatin ; humans ; infection ; neutrophils ; pathogens ; phagocytosis ; proteinases ; reactive oxygen species ; secretory granules ; tissues
Language	English
Dates of publication	2020-0215
Publishing place	Multidisciplinary Digital Publishing Institute
Document type	Article
Note	NAL-light
ZDB-ID	2695572-6
ISSN	2076-0817
ISSN	2076-0817
DOI	10.3390/pathogens9020123
Database	NAL-Catalogue (AGRICOLA)

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Article ; Online: Siglec-9 is an inhibitory receptor on human mast cells in vitro.

Miralda, Irina / Samanas, Nyssa B / Seo, Albert J / Foronda, Jake S / Sachen, Josie / Hui, Yvonne / Morrison, Shane D / Oskeritzian, Carole A / Piliponsky, Adrian M

The Journal of allergy and clinical immunology

2023 Volume 152, Issue 3, Page(s) 711–724.e14

Abstract: Background: Mast cell activation is critical for the development of allergic diseases. Ligation of sialic acid-binding immunoglobin-like lectins (Siglecs), such as Siglec-6, -7, and -8 as well as CD33, have been shown to inhibit mast cell activation. ... ...

Abstract	Background: Mast cell activation is critical for the development of allergic diseases. Ligation of sialic acid-binding immunoglobin-like lectins (Siglecs), such as Siglec-6, -7, and -8 as well as CD33, have been shown to inhibit mast cell activation. Recent studies showed that human mast cells express Siglec-9, an inhibitory receptor also expressed by neutrophils, monocytes, macrophages, and dendritic cells. Objective: We aimed to characterize Siglec-9 expression and function in human mast cells in vitro. Methods: We assessed the expression of Siglec-9 and Siglec-9 ligands on human mast cell lines and human primary mast cells by real-time quantitative PCR, flow cytometry, and confocal microscopy. We used a clustered regularly interspaced short palindromic repeats (CRISPR)/CRISPR-associated protein 9 (Cas9) gene editing approach to disrupt the SIGLEC9 gene. We evaluated Siglec-9 inhibitory activity on mast cell function by using native Siglec-9 ligands, glycophorin A (GlycA), and high-molecular-weight hyaluronic acid, a monoclonal antibody against Siglec-9, and coengagement of Siglec-9 with the high-affinity receptor for IgE (FcεRI). Results: Human mast cells express Siglec-9 and Siglec-9 ligands. SIGLEC9 gene disruption resulted in increased expression of activation markers at baseline and increased responsiveness to IgE-dependent and IgE-independent stimulation. Pretreatment with GlycA or high-molecular-weight hyaluronic acid followed by IgE-dependent or -independent stimulation had an inhibitory effect on mast cell degranulation. Coengagement of Siglec-9 with FcεRI in human mast cells resulted in reduced degranulation, arachidonic acid production, and chemokine release. Conclusions: Siglec-9 and its ligands play an important role in limiting human mast cell activation in vitro.
MeSH term(s)	Humans ; Mast Cells ; Ligands ; Hyaluronic Acid/metabolism ; Sialic Acid Binding Immunoglobulin-like Lectins/genetics ; Immunoglobulin E/metabolism
Chemical Substances	Ligands ; Hyaluronic Acid (9004-61-9) ; Sialic Acid Binding Immunoglobulin-like Lectins ; Immunoglobulin E (37341-29-0)
Language	English
Publishing date	2023-04-24
Publishing country	United States
Document type	Journal Article ; Research Support, Non-U.S. Gov't ; Research Support, N.I.H., Extramural
ZDB-ID	121011-7
ISSN	1097-6825 ; 1085-8725 ; 0091-6749
ISSN (online)	1097-6825 ; 1085-8725
ISSN	0091-6749
DOI	10.1016/j.jaci.2023.04.007
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Article ; Online: Carrageenan films as promising mucoadhesive ocular drug delivery systems.

Volod'ko, Aleksandra V / Son, Elvira Yu / Glazunov, Valery P / Davydova, Viktoriya N / Alexander-Sinkler, Elga I / Aleksandrova, Svetlana A / Blinova, Miralda I / Yermak, Irina M

Colloids and surfaces. B, Biointerfaces

2024 Volume 237, Page(s) 113854

Abstract: Polymer mucoadhesive films being developed for use in ophthalmology represent a new tool for drug delivery and are considered an alternative to traditional dosage forms. Due to their mucoadhesive properties, carrageenans (CRGs) are widely used in various ...

Abstract	Polymer mucoadhesive films being developed for use in ophthalmology represent a new tool for drug delivery and are considered an alternative to traditional dosage forms. Due to their mucoadhesive properties, carrageenans (CRGs) are widely used in various forms for drug delivery. In this study, films based on CRGs of various structural types (κ/β, κ, x, and λ) for use in ophthalmology were studied. The films were loaded with the active substance echinochrome (ECH), a sea urchin pigment used in ophthalmology. Spectral data showed that ECH remained stable after its incorporation into the CRG films and did not oxidize for at least six months. Hydrophilic CRG films with a thickness of 10-12 µm were characterized in terms of their swelling and mucoadhesive properties. The rheological properties of solutions formed after film dissolution in artificial tears were also assessed. κ- and κ/β-CRG films with ECH exhibited pseudoplastic behavior after rehydrating films with an artificial tear solution. The CRG-loaded films had different swelling characteristics depending on the structure of the CRG used. The films based on highly sulfated CRGs dissolved in artificial tears, while the films of low-sulfated κ/β-CRG exhibited limited swelling. All studied ECH-loaded films exhibited mucoadhesive properties, which were evaluated by a texture analyzer using mucous tissue of the small intestine of the pig as a model. There was a slight prolongation of ECH release from CRG films in artificial tears. The effect of CRG/ECH on the epithelial cell lines of the outer shell of the human eye was investigated. At low concentrations, ECH in the composition of the CRG/ECH complex had no cytotoxic effect on corneal epithelial and conjunctival human cells. The use of ECH-containing films can prevent the drug from being immediately washed away by tears and help to retain it by increasing viscosity and having mucoadhesive properties.
MeSH term(s)	Humans ; Animals ; Swine ; Carrageenan/chemistry ; Lubricant Eye Drops/metabolism ; Lubricant Eye Drops/pharmacology ; Drug Delivery Systems ; Eye ; Intestine, Small
Chemical Substances	Carrageenan (9000-07-1) ; Lubricant Eye Drops
Language	English
Publishing date	2024-03-16
Publishing country	Netherlands
Document type	Journal Article
ZDB-ID	1500523-9
ISSN	1873-4367 ; 0927-7765
ISSN (online)	1873-4367
ISSN	0927-7765
DOI	10.1016/j.colsurfb.2024.113854
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Article ; Online: Multiple Phenotypic Changes Define Neutrophil Priming.

Miralda, Irina / Uriarte, Silvia M / McLeish, Kenneth R

Frontiers in cellular and infection microbiology

2017 Volume 7, Page(s) 217

Abstract: Exposure to pro-inflammatory cytokines, chemokines, mitochondrial contents, and bacterial and viral products induces neutrophils to transition from a basal state into a primed one, which is currently defined as an enhanced response to activating stimuli. ...

Abstract	Exposure to pro-inflammatory cytokines, chemokines, mitochondrial contents, and bacterial and viral products induces neutrophils to transition from a basal state into a primed one, which is currently defined as an enhanced response to activating stimuli. Although, typically associated with enhanced generation of reactive oxygen species (ROS) by the NADPH oxidase, primed neutrophils show enhanced responsiveness of exocytosis, NET formation, and chemotaxis. Phenotypic changes associated with priming also include activation of a subset of functions, including adhesion, transcription, metabolism, and rate of apoptosis. This review summarizes the breadth of phenotypic changes associated with priming and reviews current knowledge of the molecular mechanisms behind those changes. We conclude that the current definition of priming is too restrictive. Priming represents a combination of enhanced responsiveness and activated functions that regulate both adaptive and innate immune responses.
MeSH term(s)	Apoptosis/immunology ; Apoptosis/physiology ; Cell Adhesion/immunology ; Chemokines/metabolism ; Chemotaxis/immunology ; Cytokines/immunology ; Cytokines/metabolism ; Exocytosis/immunology ; Extracellular Traps/immunology ; Extracellular Vesicles ; Humans ; Immunity, Innate/immunology ; Lipid Metabolism ; NADPH Oxidases/metabolism ; Neutrophils/immunology ; Neutrophils/metabolism ; Phagocytosis/immunology ; Phenotype ; Reactive Oxygen Species/metabolism ; Respiratory Burst/immunology
Chemical Substances	Chemokines ; Cytokines ; Reactive Oxygen Species ; NADPH Oxidases (EC 1.6.3.-)
Language	English
Publishing date	2017-05-29
Publishing country	Switzerland
Document type	Journal Article ; Review
ZDB-ID	2619676-1
ISSN	2235-2988 ; 2235-2988
ISSN (online)	2235-2988
ISSN	2235-2988
DOI	10.3389/fcimb.2017.00217
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Article ; Online: The roles of NADPH oxidase in modulating neutrophil effector responses.

Zeng, Melody Y / Miralda, Irina / Armstrong, Cortney L / Uriarte, Silvia M / Bagaitkar, Juhi

Molecular oral microbiology

2019 Volume 34, Issue 2, Page(s) 27–38

Abstract: Neutrophils are phagocytic innate immune cells essential for killing bacteria via activation of a wide variety of effector responses and generation of large amounts of reactive oxygen species (ROS). Majority of the ROS in neutrophils is generated by ... ...

Abstract	Neutrophils are phagocytic innate immune cells essential for killing bacteria via activation of a wide variety of effector responses and generation of large amounts of reactive oxygen species (ROS). Majority of the ROS in neutrophils is generated by activation of the superoxide-generating enzyme nicotinamide adenine dinucleotide phosphate (NADPH) oxidase. Independent of their anti-microbial function, NADPH oxidase-derived ROS have emerged as key regulators of host immune responses and neutrophilic inflammation. Data from patients with inherited defects in the NADPH oxidase subunit alleles that ablate its enzyme function as well as mouse models demonstrate profound dysregulation of host inflammatory responses, neutrophil hyper-activation and tissue damage in response to microbial ligands or tissue trauma. A large body of literature now demonstrates how oxidants function as essential signaling molecules that are essential for the regulation of neutrophil responses during priming, degranulation, neutrophil extracellular trap formation, and apoptosis, independent of their role in microbial killing. In this review we summarize how NADPH oxidase-derived oxidants modulate neutrophil function in a cell intrinsic manner and regulate host inflammatory responses. In addition, we summarize studies that have elucidated possible roles of oxidants in neutrophilic responses within the oral mucosa and periodontal disease.
MeSH term(s)	Animals ; Anti-Infective Agents/metabolism ; Anti-Infective Agents/pharmacology ; Apoptosis ; Bacteria/immunology ; Bacteria/pathogenicity ; Extracellular Traps ; Granulomatous Disease, Chronic/immunology ; Humans ; Immunity, Innate ; Inflammation/immunology ; Mice ; Mouth Mucosa/immunology ; NADPH Oxidase 2 ; NADPH Oxidases/immunology ; NADPH Oxidases/metabolism ; Neutrophils/enzymology ; Neutrophils/immunology ; Neutrophils/metabolism ; Oxidative Stress ; Periodontal Diseases/immunology ; Reactive Oxygen Species/metabolism ; Reactive Oxygen Species/pharmacology ; Respiratory Burst/immunology
Chemical Substances	Anti-Infective Agents ; Reactive Oxygen Species ; CYBB protein, human (EC 1.6.3.-) ; NADPH Oxidase 2 (EC 1.6.3.-) ; NADPH Oxidases (EC 1.6.3.-)
Language	English
Publishing date	2019-02-07
Publishing country	Denmark
Document type	Journal Article ; Research Support, N.I.H., Extramural ; Review
ZDB-ID	2537726-7
ISSN	2041-1014 ; 2041-1006
ISSN (online)	2041-1014
ISSN	2041-1006
DOI	10.1111/omi.12252
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