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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 ; 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 ; 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 ; Online: Sequestration of artemin reduces inflammation-induced activation and sensitization of bone marrow nociceptors in a rodent model of carrageenan-induced inflammatory bone pain.

Nencini, Sara / Thai, Jenny / Ivanusic, Jason J

European journal of pain (London, England)

2018 Volume 23, Issue 2, Page(s) 397–409

Abstract: Background: Pathologies that affect the bone marrow have a significant inflammatory component; however, it is not clear how inflammatory mediators affect nociceptive nerve terminals within the marrow cavity.: Methods: In this study, an in vivo bone- ... ...

Abstract	Background: Pathologies that affect the bone marrow have a significant inflammatory component; however, it is not clear how inflammatory mediators affect nociceptive nerve terminals within the marrow cavity. Methods: In this study, an in vivo bone-nerve preparation was used to directly record the physiological response properties of bone marrow nociceptors innervating the tibial marrow cavity of rats, before and after application of the inflammatory agent carrageenan. In addition, endogenous artemin was sequestered by application of an artemin neutralizing antibody to determine if this could prevent the inflammation-induced physiological changes observed. Results: A single injection of carrageenan administered into the tibial marrow cavity produced rapid changes in weight bearing (pain-like behaviour) in conscious animals. Carrageenan, but not saline, activated bone marrow nociceptors in whole-nerve recordings and sensitized a subtype of Aδ-bone marrow nociceptors to mechanical stimulation. The activation and sensitization had a rapid time course that matched that of pain-like behaviours. Sequestration of endogenous artemin significantly reduced carrageenan-induced increases in ongoing activity and completely abolished sensitization of bone marrow nociceptors to mechanical stimulation. Conclusions: These observations indicate that inflammation affects the activity and sensitivity of bone marrow nociceptors; that artemin plays a role in these changes; and that artemin might be a promising target for pharmacological manipulations in the treatment of inflammatory bone pain. Significance: Most pathologies that affect the bone marrow have an inflammatory component. We have used a model of carrageenan-induced inflammation to show that sequestration of artemin reduces inflammation-induced activation and sensitization of bone marrow nociceptors. Our findings suggest that artemin signalling is a target for the treatment of inflammatory bone pain.
MeSH term(s)	Animals ; Bone Marrow ; Carrageenan ; Disease Models, Animal ; Inflammation ; Male ; Musculoskeletal Pain/pathology ; Musculoskeletal Pain/physiopathology ; Musculoskeletal Pain/prevention & control ; Nerve Tissue Proteins/antagonists & inhibitors ; Nociceptors ; Rats ; Rats, Sprague-Dawley
Chemical Substances	Artn protein, rat ; Nerve Tissue Proteins ; Carrageenan (9000-07-1)
Language	English
Publishing date	2018-10-11
Publishing country	England
Document type	Journal Article ; Research Support, Non-U.S. Gov't
ZDB-ID	1390424-3
ISSN	1532-2149 ; 1090-3801
ISSN (online)	1532-2149
ISSN	1090-3801
DOI	10.1002/ejp.1315
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Article ; Online: TRPV1 activation alters the function of Aδ and C fiber sensory neurons that innervate bone.

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

Bone

2019 Volume 123, Page(s) 168–175

Abstract: The Transient receptor potential cation channel subfamily V member 1 (TRPV1) is a non-selective cation channel that is activated by capsaicin, low pH and noxious heat. It has been suggested to have a pro-algesic role in a range of conditions that present ...

Abstract	The Transient receptor potential cation channel subfamily V member 1 (TRPV1) is a non-selective cation channel that is activated by capsaicin, low pH and noxious heat. It has been suggested to have a pro-algesic role in a range of conditions that present with bone pain, but the mechanisms by which this occurs are not yet clear. In this study we aimed to determine if TRPV1 is expressed in Aδ and/or C fiber bone afferent neurons, and to explore its role in the activation and/or sensitization of bone afferent neurons to mechanical stimulation. A combination of retrograde tracing and immunohistochemistry was used to determine expression of TRPV1 in the soma of bone afferent neurons that innervate the rat tibial marrow cavity. A novel, in vivo, electrophysiological bone-nerve preparation, recently developed in our laboratory, was used to make recordings of the activity and sensitivity of bone afferent neurons in response to application of the TRPV1 agonist capsaicin to the marrow cavity. We found that a substantial proportion of bone afferent neurons express TRPV1. These include both small-diameter myelinated (neurofilament rich) and unmyelinated (neurofilament poor) neurons that are likely to be Aδ and C fiber neurons, respectively. Electrophysiological recordings revealed that application of capsaicin to the marrow cavity increased ongoing activity of C fiber, and to a lesser extent Aδ fiber, bone afferent neurons. Capsaicin also sensitized both Aδ and C fiber bone afferent neurons to mechanical stimulation. This evidence supports a role for TRPV1 in the pathogenesis of pain associated with bone pathology or disease.
MeSH term(s)	Animals ; Capsaicin/pharmacology ; Electrophysiology ; Immunohistochemistry ; Male ; Neurons, Afferent/drug effects ; Neurons, Afferent/metabolism ; Rats ; Rats, Sprague-Dawley ; Sensory Receptor Cells/drug effects ; Sensory Receptor Cells/metabolism ; Stress, Mechanical ; TRPV Cation Channels/genetics ; TRPV Cation Channels/metabolism
Chemical Substances	TRPV Cation Channels ; Trpv1 protein, rat ; Capsaicin (S07O44R1ZM)
Language	English
Publishing date	2019-03-29
Publishing country	United States
Document type	Journal Article ; Research Support, Non-U.S. Gov't
ZDB-ID	632515-4
ISSN	1873-2763 ; 8756-3282
ISSN (online)	1873-2763
ISSN	8756-3282
DOI	10.1016/j.bone.2019.03.040
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Article ; Online: ASIC3 inhibition modulates inflammation-induced changes in the activity and sensitivity of Aδ and C fiber sensory neurons that innervate bone.

Morgan, Michael / Thai, Jenny / Trinh, Phu / Habib, Mohamed / Effendi, Kelly N / Ivanusic, Jason J

Molecular pain

2020 Volume 16, Page(s) 1744806920975950

Abstract: The Acid Sensing Ion Channel 3 (ASIC3) is a non-selective cation channel that is activated by acidification, and is known to have a role in regulating inflammatory pain. It has pro-algesic roles in a range of conditions that present with bone pain, but ... ...

Abstract	The Acid Sensing Ion Channel 3 (ASIC3) is a non-selective cation channel that is activated by acidification, and is known to have a role in regulating inflammatory pain. It has pro-algesic roles in a range of conditions that present with bone pain, but the mechanism for this has not yet been demonstrated. We aimed to determine if ASIC3 is expressed in Aδ and/or C fiber bone afferent neurons, and to explore its role in the activation and sensitization of bone afferent neurons after acute inflammation. A combination of retrograde tracing and immunohistochemistry was used to determine expression of ASIC3 in the soma of bone afferent neurons. A novel,
MeSH term(s)	Acid Sensing Ion Channels/metabolism ; Animals ; Bone and Bones/innervation ; Bone and Bones/pathology ; Calcitonin Gene-Related Peptide/metabolism ; Carrageenan ; Ganglia, Spinal/metabolism ; Ganglia, Spinal/pathology ; Inflammation/metabolism ; Inflammation/pathology ; Male ; Myelin Sheath/metabolism ; Nerve Fibers, Unmyelinated/metabolism ; Nerve Fibers, Unmyelinated/pathology ; Neurons, Afferent/metabolism ; Rats, Sprague-Dawley ; Sensory Receptor Cells/metabolism ; Sensory Receptor Cells/pathology ; Stress, Mechanical
Chemical Substances	ASIC3 protein, rat ; Acid Sensing Ion Channels ; Carrageenan (9000-07-1) ; Calcitonin Gene-Related Peptide (JHB2QIZ69Z)
Language	English
Publishing date	2020-11-28
Publishing country	United States
Document type	Journal Article ; Research Support, Non-U.S. Gov't
ZDB-ID	2174252-2
ISSN	1744-8069 ; 1744-8069
ISSN (online)	1744-8069
ISSN	1744-8069
DOI	10.1177/1744806920975950
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Article ; Online: Identifying spinal afferent (sensory) nerve endings that innervate the marrow cavity and periosteum using anterograde tracing.

Thai, Jenny / Kyloh, Melinda / Travis, Lee / Spencer, Nick J / Ivanusic, Jason J

The Journal of comparative neurology

2020 Volume 528, Issue 11, Page(s) 1903–1916

Abstract: While sensory and sympathetic neurons are known to innervate bone, previous studies have found it difficult to unequivocally identify and characterize only those that are of sensory origin. In this study, we have utilized an in vivo anterograde tracing ... ...

Abstract	While sensory and sympathetic neurons are known to innervate bone, previous studies have found it difficult to unequivocally identify and characterize only those that are of sensory origin. In this study, we have utilized an in vivo anterograde tracing technique to selectively label spinal afferent (sensory) nerve endings that innervate the periosteum and marrow cavity of murine long bones. Unilateral injections of dextran-biotin (anterograde tracer; 20% in saline, 50-100 nl) were made into L3-L5 dorsal root ganglia. After a 10-day recovery period to allow sufficient time for selective anterograde transport of the tracer to nerve terminal endings in bone, the periosteum (whole-mount) and underlying bone were collected, processed to reveal anterograde labeling, and immuno-labeled with antibodies directed against protein gene product (pan-neuronal marker; PGP9.5), tyrosine hydroxylase (sympathetic neuron marker; TH), calcitonin gene-related protein (peptidergic nociceptor marker; CGRP), and/or neurofilament 200 (myelinated axon marker; NF200). Anterograde-labeled nerve endings were dispersed throughout the periosteum and marrow cavity and could be identified in close apposition to blood vessels and at sites distant from them. The periosteum and the marrow cavity were each innervated by myelinated (NF200+) sensory neurons, and unmyelinated (NF200-) sensory neurons that were either peptidergic (CGRP+) or nonpeptidergic (CGRP-). Spinal afferent nerve endings did not express TH, and lacked the cylindrical morphology around blood vessels characteristic of sympathetic innervation. This approach to selective labeling of sensory nerve terminal endings will help to better identify how different sub-populations of sensory neurons, and their peripheral nerve terminal endings, interact with bone.
MeSH term(s)	Animals ; Bone Marrow/innervation ; Male ; Mice ; Mice, Inbred C57BL ; Periosteum/innervation ; Sensory Receptor Cells/cytology
Language	English
Publishing date	2020-01-29
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.24862
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Article ; Online: A population of nonneuronal GFRα3-expressing cells in the bone marrow resembles nonmyelinating Schwann cells.

Thai, Jenny / Green, Alanna C / Stamp, Lincon A / Spencer, Nick J / Purton, Louise E / Ivanusic, Jason

Cell and tissue research

2019 Volume 378, Issue 3, Page(s) 441–456

Abstract: Artemin is a neurotrophic factor that plays a crucial role in the regulation of neural development and regeneration and has also been implicated in the pathogenesis of inflammatory pain. The receptor for artemin, GFRα3, is expressed by sympathetic and ... ...

Abstract	Artemin is a neurotrophic factor that plays a crucial role in the regulation of neural development and regeneration and has also been implicated in the pathogenesis of inflammatory pain. The receptor for artemin, GFRα3, is expressed by sympathetic and nociceptive sensory neurons, including some that innervate the bone marrow, but it is unclear if it is also expressed in other cell types in the bone marrow. Our goal in the present study was to characterise the expression of GFRα3 in nonneuronal cells in the bone marrow. Immunohistochemical studies revealed that GFRα3-expressing cells in the bone marrow are spatially associated with blood vessels and are in intimate contact with nerve fibres. We used various combinations of markers to distinguish different cell types and found that the GFRα3-expressing cells expressed markers of nonmyelinating Schwann cells (e.g. GFAP, p75NTR, nestin). Analysis of bone marrow sections of Wnt1-reporter mice also demonstrated that they originate from the neural crest. Further characterisation using flow cytometry revealed that GFRα3 is expressed in a population of CD51
MeSH term(s)	Animals ; Bone Marrow/metabolism ; Bone Marrow Cells/cytology ; Bone Marrow Cells/metabolism ; Glial Cell Line-Derived Neurotrophic Factor Receptors/physiology ; Mice ; Mice, Inbred C57BL ; Nerve Tissue Proteins/metabolism ; Schwann Cells/cytology ; Schwann Cells/metabolism
Chemical Substances	Artn protein, mouse ; Gfra3 protein, mouse ; Glial Cell Line-Derived Neurotrophic Factor Receptors ; Nerve Tissue Proteins
Language	English
Publishing date	2019-07-14
Publishing country	Germany
Document type	Journal Article
ZDB-ID	125067-x
ISSN	1432-0878 ; 0302-766X
ISSN (online)	1432-0878
ISSN	0302-766X
DOI	10.1007/s00441-019-03068-w
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