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Article ; Online: Using tissue clearing and light sheet fluorescence microscopy for the three-dimensional analysis of sensory and sympathetic nerve endings that innervate bone and dental tissue of mice.

Thai, Jenny / Fuller-Jackson, John-Paul / Ivanusic, Jason J

2024 Volume 532, Issue 1, Page(s) e25582

Abstract: Bone and dental tissues are richly innervated by sensory and sympathetic neurons. However, the characterization of the morphology, molecular phenotype, and distribution of nerves that innervate hard tissue has so far mostly been limited to thin ... ...

Abstract	Bone and dental tissues are richly innervated by sensory and sympathetic neurons. However, the characterization of the morphology, molecular phenotype, and distribution of nerves that innervate hard tissue has so far mostly been limited to thin histological sections. This approach does not adequately capture dispersed neuronal projections due to the loss of important structural information during three-dimensional (3D) reconstruction. In this study, we modified the immunolabeling-enabled imaging of solvent-cleared organs (iDISCO/iDISCO+) clearing protocol to image high-resolution neuronal structures in whole femurs and mandibles collected from perfused C57Bl/6 mice. Axons and their nerve terminal endings were immunolabeled with antibodies directed against protein gene product 9.5 (pan-neuronal marker), calcitonin gene-related peptide (peptidergic nociceptor marker), or tyrosine hydroxylase (sympathetic neuron marker). Volume imaging was performed using light sheet fluorescence microscopy. We report high-quality immunolabeling of the axons and nerve terminal endings for both sensory and sympathetic neurons that innervate the mouse femur and mandible. Importantly, we are able to follow their projections through full 3D volumes, highlight how extensive their distribution is, and show regional differences in innervation patterns for different parts of each bone (and surrounding tissues). Mapping the distribution of sensory and sympathetic axons, and their nerve terminal endings, in different bony compartments may be important in further elucidating their roles in health and disease.
MeSH term(s)	Animals ; Mice ; Microscopy, Fluorescence ; Neurons ; Axons ; Mice, Inbred C57BL ; Nerve Endings
Language	English
Publishing date	2024-01-30
Publishing country	United States
Document type	Journal Article ; Research Support, Non-U.S. Gov't
ZDB-ID	3086-7
ISSN	1096-9861 ; 0021-9967 ; 0092-7317
ISSN (online)	1096-9861
ISSN	0021-9967 ; 0092-7317
DOI	10.1002/cne.25582
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Article: Molecular Mechanisms That Contribute to Bone Marrow Pain.

Ivanusic, Jason J

Frontiers in neurology

2017 Volume 8, Page(s) 458

Abstract: Pain associated a bony pathology puts a significant burden on individuals, society, and the health-care systems worldwide. Pathology that involves the bone marrow activates sensory nerve terminal endings of peripheral bone marrow nociceptors, and is the ... ...

Abstract	Pain associated a bony pathology puts a significant burden on individuals, society, and the health-care systems worldwide. Pathology that involves the bone marrow activates sensory nerve terminal endings of peripheral bone marrow nociceptors, and is the likely trigger for pain. This review presents our current understanding of how bone marrow nociceptors are influenced by noxious stimuli presented in pathology associated with bone marrow. A number of ion channels and receptors are emerging as important modulators of the activity of peripheral bone marrow nociceptors. Nerve growth factor (NGF) sequestration has been trialed for the management of inflammatory bone pain (osteoarthritis), and there is significant evidence for interaction of NGF with bone marrow nociceptors. Activation of transient receptor potential cation channel subfamily V member 1 sensitizes bone marrow nociceptors and could contribute to increased sensitivity of patients to noxious stimuli in various bony pathologies. Acid-sensing ion channels sense changes to tissue pH in the bone marrow microenvironment and could be targeted to treat pathology that involves acidosis of the bone marrow. Piezo2 is a mechanically gated ion channel that has recently been reported to be expressed by most myelinated bone marrow nociceptors and might be a target for treatments directed against mechanically induced bone pain. These ion channels and receptors could be useful targets for the development of peripherally acting drugs to treat pain of bony origin.
Language	English
Publishing date	2017-09-11
Publishing country	Switzerland
Document type	Journal Article ; Review
ZDB-ID	2564214-5
ISSN	1664-2295
ISSN	1664-2295
DOI	10.3389/fneur.2017.00458
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Article ; Online: Stomatin-like protein 3 modulates the responses of Aδ, but not C fiber bone afferent neurons to noxious mechanical stimulation in an animal model of acute experimental bone pain.

Morgan, Michael / Thai, Jenny / Nencini, Sara / Xu, James / Ivanusic, Jason J

Molecular pain

2023 Volume 19, Page(s) 17448069231222407

Abstract: STOML3 is a membrane bound scaffolding protein that has been shown to facilitate the opening of mechanically sensitive ion channels and contribute to noxious mechanical sensation, allodynia and hyperalgesia. In this study, we aimed to determine the role ... ...

Abstract	STOML3 is a membrane bound scaffolding protein that has been shown to facilitate the opening of mechanically sensitive ion channels and contribute to noxious mechanical sensation, allodynia and hyperalgesia. In this study, we aimed to determine the role of STOML3 in noxious mechanical sensitivity of bone afferent neurons and carrageenan-induced acute inflammation in the bone. An
MeSH term(s)	Rats ; Animals ; Carrageenan/toxicity ; Carrageenan/metabolism ; Rats, Sprague-Dawley ; Neurons, Afferent/metabolism ; Hyperalgesia/metabolism ; Musculoskeletal Pain/metabolism ; Acute Pain/metabolism ; Models, Animal ; Inflammation/metabolism
Chemical Substances	Carrageenan (9000-07-1)
Language	English
Publishing date	2023-12-08
Publishing country	United States
Document type	Journal Article
ZDB-ID	2174252-2
ISSN	1744-8069 ; 1744-8069
ISSN (online)	1744-8069
ISSN	1744-8069
DOI	10.1177/17448069231222407
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Article: Mini review: The role of sensory innervation to subchondral bone in osteoarthritis pain.

Morgan, Michael / Nazemian, Vida / Harrington, Kate / Ivanusic, Jason J

Frontiers in endocrinology

2022 Volume 13, Page(s) 1047943

Abstract: Osteoarthritis pain is often thought of as a pain driven by nerves that innervate the soft tissues of the joint, but there is emerging evidence for a role for nerves that innervate the underlying bone. In this mini review we cite evidence that ... ...

Abstract	Osteoarthritis pain is often thought of as a pain driven by nerves that innervate the soft tissues of the joint, but there is emerging evidence for a role for nerves that innervate the underlying bone. In this mini review we cite evidence that subchondral bone lesions are associated with pain in osteoarthritis. We explore recent studies that provide evidence that sensory neurons that innervate bone are nociceptors that signal pain and can be sensitized in osteoarthritis. Finally, we describe neuronal remodeling of sensory and sympathetic nerves in bone and discuss how these processes can contribute to osteoarthritis pain.
MeSH term(s)	Humans ; Pain/etiology ; Osteoarthritis/complications ; Osteoarthritis/pathology ; Bone and Bones/pathology ; Sensory Receptor Cells/pathology ; Bone Diseases
Language	English
Publishing date	2022-12-20
Publishing country	Switzerland
Document type	Journal Article ; Review ; Research Support, Non-U.S. Gov't
ZDB-ID	2592084-4
ISSN	1664-2392
ISSN	1664-2392
DOI	10.3389/fendo.2022.1047943
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Article ; Online: Reply to Dr Cornish.

Ivanusic, Jason / Konishi, Yasutaka / Barrington, Michael J

Regional anesthesia and pain medicine

2019 Volume 44, Issue 2, Page(s) 270–271

MeSH term(s)	Analgesics ; Anesthesia, Conduction ; Anesthesia, Local ; Anesthetics, Local ; Humans ; Pain ; United States
Chemical Substances	Analgesics ; Anesthetics, Local
Language	English
Publishing date	2019-04-03
Publishing country	England
Document type	Letter ; Comment
ZDB-ID	1425299-5
ISSN	1532-8651 ; 1098-7339 ; 0146-521X
ISSN (online)	1532-8651
ISSN	1098-7339 ; 0146-521X
DOI	10.1136/rapm-2018-100225
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Article ; Online: Artemin sensitizes nociceptors that innervate the osteoarthritic joint to produce pain.

Morgan, Michael / Nazemian, Vida / Ooi, Li Sha / Burger, Sarah / Thai, Jenny / Ivanusic, Jason

Osteoarthritis and cartilage

2023 Volume 31, Issue 10, Page(s) 1342–1352

Abstract: Objective: There have been significant developments in understanding artemin/GFRα3 signaling in recent years, and there is now accumulating evidence that artemin has important roles to play in pain signaling, including that derived from joint and bone, ... ...

Abstract	Objective: There have been significant developments in understanding artemin/GFRα3 signaling in recent years, and there is now accumulating evidence that artemin has important roles to play in pain signaling, including that derived from joint and bone, and that associated with osteorthritis (OA). Methods: A total of 163 Sprague-Dawley rats were used in this study. We used an animal model of mono-iodoacetate (MIA)-induced OA, in combination with electrophysiology, behavioral testing, Western blot analysis, and retrograde tracing and immunohistochemistry, to identify roles for artemin/GFRα3 signaling in the pathogenesis of OA pain. Results: We have found that: 1) GFRα3 is expressed in a substantial proportion of knee joint afferent neurons; 2) exogenous artemin sensitizes knee joint afferent neurons in naïve rats; 3) artemin is expressed in articular tissues of the joint, but not surrounding bone, early in MIA-induced OA; 4) artemin expression increases in bone later in MIA-induced OA when pathology involves subchondral bone; and 5) sequestration of artemin reverses MIA-induced sensitization of both knee joint and bone afferent neurons late in disease when there is inflammation of knee joint tissues and damage to the subchondral bone. Conclusions: Our findings show that artemin/GFRα3 signaling has a role to play in the pathogenesis of OA pain, through effects on both knee joint and bone afferent neurons, and suggest that targeted manipulation of artemin/GFRα3 signaling may provide therapeutic benefit for the management of OA pain. Data availability: Data are available on request of the corresponding author.
MeSH term(s)	Rats ; Animals ; Nociceptors/metabolism ; Rats, Sprague-Dawley ; Pain/etiology ; Pain/metabolism ; Neurons, Afferent ; Inflammation/metabolism ; Disease Models, Animal
Language	English
Publishing date	2023-06-21
Publishing country	England
Document type	Journal Article ; Research Support, Non-U.S. Gov't
ZDB-ID	1167809-4
ISSN	1522-9653 ; 1063-4584
ISSN (online)	1522-9653
ISSN	1063-4584
DOI	10.1016/j.joca.2023.06.003
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Article: Piezo2 Knockdown Inhibits Noxious Mechanical Stimulation and NGF-Induced Sensitization in A-Delta Bone Afferent Neurons.

Nencini, Sara / Morgan, Michael / Thai, Jenny / Jobling, Andrew I / Mazzone, Stuart B / Ivanusic, Jason J

Frontiers in physiology

2021 Volume 12, Page(s) 644929

Abstract: Piezo2 is a mechanically gated ion-channel that has a well-defined role in innocuous mechanical sensitivity, but recently has also been suggested to play a role in mechanically induced pain. Here we have explored a role for Piezo2 in mechanically evoked ... ...

Abstract	Piezo2 is a mechanically gated ion-channel that has a well-defined role in innocuous mechanical sensitivity, but recently has also been suggested to play a role in mechanically induced pain. Here we have explored a role for Piezo2 in mechanically evoked bone nociception in Sprague Dawley rats. We have used an
Language	English
Publishing date	2021-07-15
Publishing country	Switzerland
Document type	Journal Article
ZDB-ID	2564217-0
ISSN	1664-042X
ISSN	1664-042X
DOI	10.3389/fphys.2021.644929
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Article ; Online: Changes to the activity and sensitivity of nerves innervating subchondral bone contribute to pain in late-stage osteoarthritis.

Morgan, Michael / Thai, Jenny / Nazemian, Vida / Song, Richard / Ivanusic, Jason J

Pain

2021 Volume 163, Issue 2, Page(s) 390–402

Abstract: Abstract: Although it is clear that osteoarthritis (OA) pain involves activation and/or sensitization of nociceptors that innervate knee joint articular tissues, much less is known about the role of the innervation of surrounding bone. In this study, we ...

Abstract	Abstract: Although it is clear that osteoarthritis (OA) pain involves activation and/or sensitization of nociceptors that innervate knee joint articular tissues, much less is known about the role of the innervation of surrounding bone. In this study, we used monoiodoacetate (MIA)-induced OA in male rats to test the idea that pain in OA is driven by differential contributions from nerves that innervate knee joint articular tissues vs the surrounding bone. The time-course of pain behavior was assayed using the advanced dynamic weight-bearing device, and histopathology was examined using haematoxylin and eosin histology. Extracellular electrophysiological recordings of knee joint and bone afferent neurons were made early (day 3) and late (day 28) in the pathogenesis of MIA-induced OA. We observed significant changes in the function of knee joint afferent neurons, but not bone afferent neurons, at day 3 when there was histological evidence of inflammation in the joint capsule, but no damage to the articular cartilage or subchondral bone. Changes in the function of bone afferent neurons were only observed at day 28, when there was histological evidence of damage to the articular cartilage and subchondral bone. Our findings suggest that pain early in MIA-induced OA involves activation and sensitization of nerves that innervate the joint capsule but not the underlying subchondral bone, and that pain in late MIA-induced OA involves the additional recruitment of nerves that innervate the subchondral bone. Thus, nerves that innervate bone should be considered important targets for development of mechanism-based therapies to treat pain in late OA.
MeSH term(s)	Animals ; Arthritis, Experimental/chemically induced ; Cartilage, Articular/pathology ; Disease Models, Animal ; Knee Joint/pathology ; Male ; Osteoarthritis/chemically induced ; Osteoarthritis/complications ; Pain/etiology ; Pain/pathology ; Rats
Language	English
Publishing date	2021-06-08
Publishing country	United States
Document type	Journal Article ; Research Support, Non-U.S. Gov't
ZDB-ID	193153-2
ISSN	1872-6623 ; 0304-3959
ISSN (online)	1872-6623
ISSN	0304-3959
DOI	10.1097/j.pain.0000000000002355
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Article: The Physiology of Bone Pain. How Much Do We Really Know?

Nencini, Sara / Ivanusic, Jason J

Frontiers in physiology

2016 Volume 7, Page(s) 157

Abstract: Pain is associated with most bony pathologies. Clinical and experimental observations suggest that bone pain can be derived from noxious stimulation of the periosteum or bone marrow. Sensory neurons are known to innervate the periosteum and marrow cavity, ...

Abstract	Pain is associated with most bony pathologies. Clinical and experimental observations suggest that bone pain can be derived from noxious stimulation of the periosteum or bone marrow. Sensory neurons are known to innervate the periosteum and marrow cavity, and most of these have a morphology and molecular phenotype consistent with a role in nociception. However, little is known about the physiology of these neurons, and therefore information about mechanisms that generate and maintain bone pain is lacking. The periosteum has received greater attention relative to the bone marrow, reflecting the easier access of the periosteum for experimental assessment. With the electrophysiological preparations used, investigators have been able to record from single periosteal units in isolation, and there is a lot of information available about how they respond to different stimuli, including those that are noxious. In contrast, preparations used to study sensory neurons that innervate the bone marrow have been limited to recording multi-unit activity in whole nerves, and whilst they clearly report responses to noxious stimulation, it is not possible to define responses for single sensory neurons that innervate the bone marrow. There is only limited evidence that peripheral sensory neurons that innervate bone can be sensitized or that they can be activated by multiple stimulus types, and at present this only exists in part for periosteal units. In the central nervous system, it is clear that spinal dorsal horn neurons can be activated by noxious stimuli applied to bone. Some can be sensitized under pathological conditions and may contribute in part to secondary or referred pain associated with bony pathology. Activity related to stimulation of sensory nerves that innervate bone has also been reported in neurons of the spinoparabrachial pathway and the somatosensory cortices, both known for roles in coding information about pain. Whilst these provide some clues as to the way information about bone pain is centrally coded, they need to be expanded to further our understanding of other central territories involved. There is a lot more to learn about the physiology of peripheral sensory neurons that innervate bone and their central projections.
Language	English
Publishing date	2016-04-26
Publishing country	Switzerland
Document type	Journal Article ; Review
ZDB-ID	2564217-0
ISSN	1664-042X
ISSN	1664-042X
DOI	10.3389/fphys.2016.00157
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Article ; Online: Distribution of Corneal TRPV1 and Its Association With Immune Cells During Homeostasis and Injury.

Jiao, Haihan / Ivanusic, Jason J / McMenamin, Paul G / Chinnery, Holly R

Investigative ophthalmology & visual science

2021 Volume 62, Issue 9, Page(s) 6

Abstract: Purpose: Given the role of corneal sensory nerves during epithelial wound repair, we sought to examine the relationship between immune cells and polymodal nociceptors following corneal injury.: Methods: Young C57BL/6J mice received a 2 mm corneal ... ...

Abstract	Purpose: Given the role of corneal sensory nerves during epithelial wound repair, we sought to examine the relationship between immune cells and polymodal nociceptors following corneal injury. Methods: Young C57BL/6J mice received a 2 mm corneal epithelial injury. One week later, corneal wholemounts were immunostained using β-tubulin-488, TRPV1 (transient receptor potential ion channel subfamily V member-1, a nonselective cation channel) and immune cell (MHC-II, CD45 and CD68) antibodies. The sum length of TRPV1+ and TRPV1- nerve fibers, and their spatial association with immune cells, was quantified in intact and injured corneas. Results: TRPV1+ nerves account for ∼40% of the nerve fiber length in the intact corneal epithelium and ∼80% in the stroma. In the superficial epithelial layers, TRPV1+ nerve terminal length was similar in injured and intact corneas. In intact corneas, the density (sum length) of basal epithelial TRPV1+ and TRPV1- nerve fibers was similar, however, in injured corneas, TRPV1+ nerve density was higher compared to TRPV1- nerves. The degree of physical association between TRPV1+ nerves and intraepithelial CD45+ MHC-II+ CD11c+ cells was similar in intact and injured corneas. Stromal leukocytes co-expressed TRPV1, which was partially localized to CD68+ lysosomes, and this expression pattern was lower in injured corneas. Conclusions: TRPV1+ nerves accounted for a higher proportion of corneal nerves after injury, which may provide insights into the pathophysiology of neuropathic pain following corneal trauma. The close interactions of TRPV1+ nerves with intraepithelial immune cells and expression of TRPV1 by stromal macrophages provide evidence of neuroimmune interactions in the cornea.
MeSH term(s)	Animals ; Cell Count ; Cornea/immunology ; Cornea/metabolism ; Cornea/pathology ; Corneal Injuries/immunology ; Corneal Injuries/metabolism ; Disease Models, Animal ; Female ; Homeostasis/physiology ; Immunity, Cellular ; Male ; Mice ; Mice, Inbred C57BL ; Microscopy, Confocal ; Nerve Fibers/pathology ; TRPV Cation Channels/metabolism
Chemical Substances	TRPV Cation Channels ; TRPV1 protein, mouse
Language	English
Publishing date	2021-07-07
Publishing country	United States
Document type	Journal Article ; Research Support, Non-U.S. Gov't
ZDB-ID	391794-0
ISSN	1552-5783 ; 0146-0404
ISSN (online)	1552-5783
ISSN	0146-0404
DOI	10.1167/iovs.62.9.6
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