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Article: Degenerative and regenerative peripheral processes are associated with persistent painful chemotherapy-induced neuropathies in males and females.

Naratadam, George T / Mecklenburg, Jennifer / Shein, Sergey A / Zou, Yi / Lai, Zhao / Tumanov, Alexei V / Price, Theodor J / Akopian, Armen N

bioRxiv : the preprint server for biology

2024

Abstract: This study aimed to investigate the time course of gene expression changes during the progression of persistent painful neuropathy caused by paclitaxel (PTX) in male and female mouse hind paws and dorsal root ganglia (DRG). Bulk RNA-seq was used to ... ...

Abstract	This study aimed to investigate the time course of gene expression changes during the progression of persistent painful neuropathy caused by paclitaxel (PTX) in male and female mouse hind paws and dorsal root ganglia (DRG). Bulk RNA-seq was used to investigate the gene expression changes in the paw and DRG collected at 1, 16, and 31 days post-PTX. At these time points, differentially expressed DEGs were predominantly related to reduction or increase in epithelial, skin, bone, and muscle development and to angiogenesis, myelination, axonogenesis, and neurogenesis. These processes were accompanied by regulation of DEGs related to cytoskeleton, extracellular matrix organization and cellular energy production. This gene plasticity during persistent painful neuropathy progression likely represents biological processes linked to tissue regeneration and degeneration. Unlike regeneration/degeneration, gene plasticity related to immune processes was minimal at 1-31 days post-PTX. It was also noted that despite similarities in biological processes and pain chronicity in males and females, specific DEGs showed dramatic sex-dependency. The main conclusions of this study are that gene expression plasticity in paws and DRG during PTX neuropathy progression relates to tissue regeneration and degeneration, minimally affects the immune system processes, and is heavily sex-dependent at the individual gene level.
Language	English
Publishing date	2024-01-26
Publishing country	United States
Document type	Preprint
DOI	10.1101/2024.01.25.577218
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Article ; Online: Trigeminal neurons control immune-bone cell interaction and metabolism in apical periodontitis.

Austah, Obadah N / Lillis, Katherine V / Akopian, Armen N / Harris, Stephen E / Grinceviciute, Ruta / Diogenes, Anibal

Cellular and molecular life sciences : CMLS

2022 Volume 79, Issue 6, Page(s) 330

Abstract: Apical periodontitis (AP) is an inflammatory disease occurring following tooth infection with distinct osteolytic activity. Despite increasing evidence that sensory neurons participate in regulation of non-neuronal cells, their role in the development of ...

Abstract	Apical periodontitis (AP) is an inflammatory disease occurring following tooth infection with distinct osteolytic activity. Despite increasing evidence that sensory neurons participate in regulation of non-neuronal cells, their role in the development of AP is largely unknown. We hypothesized that trigeminal ganglia (TG) Nav1.8
MeSH term(s)	Animals ; Cell Communication ; Mice ; Nociceptors/metabolism ; Osteocytes ; Periapical Periodontitis/metabolism ; Sensory Receptor Cells
Language	English
Publishing date	2022-05-31
Publishing country	Switzerland
Document type	Journal Article
ZDB-ID	1358415-7
ISSN	1420-9071 ; 1420-682X
ISSN (online)	1420-9071
ISSN	1420-682X
DOI	10.1007/s00018-022-04335-w
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Article: Transcriptional Profiles of Non-neuronal and Immune Cells in Mouse Trigeminal Ganglia.

Mecklenburg, Jennifer / Shein, Sergey A / Hovhannisyan, Anahit H / Zou, Yi / Lai, Zhao / Ruparel, Shivani / Tumanov, Alexei V / Akopian, Armen N

bioRxiv : the preprint server for biology

2023

Abstract: Non-neuronal cells constitute 90-95% of sensory ganglia. These cells play critical roles in modulation of nociceptive signal transmissions by sensory neurons. Accordingly, the aim of this review-study was to identify, profile and summarize TG non- ... ...

Abstract	Non-neuronal cells constitute 90-95% of sensory ganglia. These cells play critical roles in modulation of nociceptive signal transmissions by sensory neurons. Accordingly, the aim of this review-study was to identify, profile and summarize TG non-neuronal cell types in naïve male mice using published and our own data generated by single-cell RNA sequencing (scRNA-seq), flow cytometry (FC) and immunohistochemistry (IHC). TG contains 5 types of non-neuronal cells: glial, fibroblasts, smooth muscle, endothelial and immune cells. There is agreement among publications for glial, fibroblasts, smooth muscle and endothelial cells. Based on gene profiles, glial cells were classified as Schwann cells and satellite glial cells (SGC).
Language	English
Publishing date	2023-08-19
Publishing country	United States
Document type	Preprint
DOI	10.1101/2023.08.18.553897
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Article ; Online: Associations of tissue damage induced inflammatory plasticity in masseter muscle with the resolution of chronic myalgia.

Lindquist, Karen A / Shein, Sergey A / Hovhannisyan, Anahit H / Mecklenburg, Jennifer / Zou, Yi / Lai, Zhao / Tumanov, Alexei V / Akopian, Armen N

Scientific reports

2023 Volume 13, Issue 1, Page(s) 22057

Abstract: Gene plasticity during myogenous temporomandibular disorder (TMDM) development is largely unknown. TMDM could be modeled by intramuscular inflammation or tissue damage. To model inflammation induced TMDM we injected complete Freund's adjuvant (CFA) into ... ...

Abstract	Gene plasticity during myogenous temporomandibular disorder (TMDM) development is largely unknown. TMDM could be modeled by intramuscular inflammation or tissue damage. To model inflammation induced TMDM we injected complete Freund's adjuvant (CFA) into masseter muscle (MM). To model tissue damage induced TMDM we injected extracellular matrix degrading collagenase type 2 (Col). CFA and Col produced distinct myalgia development trajectories. We performed bulk RNA-seq of MM to generate gene plasticity time course. CFA initiated TMDM (1d post-injection) was mainly linked to chemo-tacticity of monocytes and neutrophils. At CFA-induced hypersensitivity post-resolution (5d post-injection), tissue repair processes were pronounced, while inflammation was absent. Col (0.2U) produced acute hypersensitivity linked to tissue repair without inflammatory processes. Col (10U) generated prolonged hypersensitivity with inflammatory processes dominating initiation phase (1d). Pre-resolution phase (6d) was accompanied with acceleration of expressions for tissue repair and pro-inflammatory genes. Flow cytometry showed that immune processes in MM was associated with accumulations of macrophages, natural killer, dendritic and T-cells, further confirming our RNA-seq findings. Altogether, CFA and Col treatments induced different immune processes in MM. Importantly, TMDM resolution was preceded with muscle cell and extracellular matrix repairs, an elevation in immune system gene expressions and distinct immune cell accumulations in MM.
MeSH term(s)	Rats ; Animals ; Humans ; Rats, Sprague-Dawley ; Myalgia ; Masseter Muscle ; Inflammation ; Freund's Adjuvant/adverse effects
Chemical Substances	Freund's Adjuvant (9007-81-2)
Language	English
Publishing date	2023-12-12
Publishing country	England
Document type	Journal Article
ZDB-ID	2615211-3
ISSN	2045-2322 ; 2045-2322
ISSN (online)	2045-2322
ISSN	2045-2322
DOI	10.1038/s41598-023-49280-1
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Article: Association of inflammation and tissue damage induced biological processes in masseter muscle with the resolution of chronic myalgia.

Lindquist, Karen A / Shein, Sergey A / Hovhannisyan, Anahit H / Mecklenburg, Jennifer / Zou, Yi / Lai, Zhao / Tumanov, Alexei V / Akopian, Armen N

bioRxiv : the preprint server for biology

2023

Abstract: Biological processes linked to intramuscular inflammation during myogenous temporomandibular disorder (TMDM) are largely unknown. We mimicked this inflammation by intra-masseteric muscle (MM) injections of complete Freundâ€™s adjuvant (CFA) or ... ...

Abstract	Biological processes linked to intramuscular inflammation during myogenous temporomandibular disorder (TMDM) are largely unknown. We mimicked this inflammation by intra-masseteric muscle (MM) injections of complete Freundâ€™s adjuvant (CFA) or collagenase type 2 (Col), which emulates tissue damage. CFA triggered mechanical hypersensitivity at 1d post-injection was mainly linked to processes controlling chemotactic activity of monocytes and neutrophils. At 5d post-CFA, when hypersensitivity was resolved, there was minimal inflammation whereas tissue repair processes were pronounced. Low dose Col (0.2U) also produced acute orofacial hypersensitivity that was linked to tissue repair, but not inflammatory processes. High dose Col (10U) triggered prolonged orofacial hypersensitivity with inflammatory processes dominating at 1d post-injection. At pre-resolution time point (6d), tissue repair processes were underway and a significant increase in pro-inflammatory gene expressions compared to 1d post-injection were detected. RNA-seq and flow cytometry showed that immune processes in MM were linked to accumulation of macrophages, natural killer and natural killer T cells, dendritic cells and T-cells. Altogether, CFA and Col treatments induced different immune processes in MM. Importantly, orofacial hypersensitivity resolution was preceded with repairs of muscle cell and extracellular matrix, an elevation in immune system gene expression and accumulation of distinct immune cells in MM.
Language	English
Publishing date	2023-04-22
Publishing country	United States
Document type	Preprint
DOI	10.1101/2023.04.21.537828
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Article ; Online: Approaches to cloning of pain-related ion channel genes.

Akopian, Armen N

Methods in molecular biology (Clifton, N.J.)

2013 Volume 998, Page(s) 3–19

Abstract: Molecular pain research is a relatively new and rapidly expanding field that represents advancement in conventional pain research. One of the fundamentals of molecular pain involves the cloning of genes and especially the ion channels specifically ... ...

Abstract	Molecular pain research is a relatively new and rapidly expanding field that represents advancement in conventional pain research. One of the fundamentals of molecular pain involves the cloning of genes and especially the ion channels specifically involved in nociceptive processing at the periphery and centrally. A variety of approaches were used to isolate these critically important genes. Cloning of these genes involved innovative strategies based on existing molecular approaches. This review will discuss well-utilized cloning approaches and their exploitation in molecular pain research.
MeSH term(s)	Animals ; Chromosome Mapping ; Cloning, Molecular/methods ; Humans ; Ion Channels/genetics ; Ion Channels/metabolism ; Mutation ; Pain/genetics ; Pain/metabolism ; Sequence Homology, Nucleic Acid
Chemical Substances	Ion Channels
Language	English
Publishing date	2013
Publishing country	United States
Document type	Journal Article ; Research Support, N.I.H., Extramural ; Review
ISSN	1940-6029
ISSN (online)	1940-6029
DOI	10.1007/978-1-62703-351-0_1
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Article ; Online: Characterization of Fragile X Mental Retardation Protein expression in human nociceptors and their axonal projections to the spinal dorsal horn.

Mitchell, Molly E / Cook, Lauren C / Shiers, Stephanie / Tavares-Ferreira, Diana / Akopian, Armen N / Dussor, Gregory / Price, Theodore J

The Journal of comparative neurology

2023 Volume 531, Issue 7, Page(s) 814–835

Abstract: Fragile X Mental Retardation Protein (FMRP) regulates activity-dependent RNA localization and local translation to modulate synaptic plasticity throughout the central nervous system. Mutations in the FMR1 gene that hinder or ablate FMRP function cause ... ...

Abstract	Fragile X Mental Retardation Protein (FMRP) regulates activity-dependent RNA localization and local translation to modulate synaptic plasticity throughout the central nervous system. Mutations in the FMR1 gene that hinder or ablate FMRP function cause Fragile X Syndrome (FXS), a disorder associated with sensory processing dysfunction. FXS premutations are associated with increased FMRP expression and neurological impairments including sex dimorphic presentations of chronic pain. In mice, FMRP ablation causes dysregulated dorsal root ganglion (DRG) neuron excitability and synaptic vesicle exocytosis, spinal circuit activity, and decreased translation-dependent nociceptive sensitization. Activity-dependent, local translation is a key mechanism for enhancing primary nociceptor excitability that promotes pain in animals and humans. These works indicate that FMRP likely regulates nociception and pain at the level of the primary nociceptor or spinal cord. Therefore, we sought to better understand FMRP expression in the human DRG and spinal cord using immunostaining in organ donor tissues. We find that FMRP is highly expressed in DRG and spinal neuron subsets with substantia gelatinosa exhibiting the most abundant immunoreactivity in spinal synaptic fields. Here, it is expressed in nociceptor axons. FMRP puncta colocalized with Nav1.7 and TRPV1 receptor signals suggesting a pool of axoplasmic FMRP localizes to plasma membrane-associated loci in these branches. Interestingly, FMRP puncta exhibited notable colocalization with calcitonin gene-related peptide (CGRP) immunoreactivity selectively in female spinal cord. Our results support a regulatory role for FMRP in human nociceptor axons of the dorsal horn and implicate it in the sex dimorphic actions of CGRP signaling in nociceptive sensitization and chronic pain.
MeSH term(s)	Humans ; Animals ; Mice ; Female ; Fragile X Mental Retardation Protein/genetics ; Fragile X Mental Retardation Protein/metabolism ; Nociceptors/metabolism ; Chronic Pain ; Calcitonin Gene-Related Peptide/metabolism ; Axons/metabolism ; Fragile X Syndrome/genetics ; Spinal Cord Dorsal Horn/metabolism
Chemical Substances	Fragile X Mental Retardation Protein (139135-51-6) ; Calcitonin Gene-Related Peptide (JHB2QIZ69Z) ; FMR1 protein, human ; Fmr1 protein, mouse
Language	English
Publishing date	2023-02-20
Publishing country	United States
Document type	Journal Article ; Research Support, N.I.H., Extramural
ZDB-ID	3086-7
ISSN	1096-9861 ; 0021-9967 ; 0092-7317
ISSN (online)	1096-9861
ISSN	0021-9967 ; 0092-7317
DOI	10.1002/cne.25463
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Article ; Online: Identification of Trigeminal Sensory Neuronal Types Innervating Masseter Muscle.

Lindquist, Karen A / Belugin, Sergei / Hovhannisyan, Anahit H / Corey, Tatiana M / Salmon, Adam / Akopian, Armen N

eNeuro

2021 Volume 8, Issue 5

Abstract: Understanding masseter muscle (MM) innervation is critical for the study of cell-specific mechanisms of pain induced by temporomandibular disorder (TMDs) or after facial surgery. Here, we identified trigeminal (TG) sensory neuronal subtypes (MM TG ... ...

Abstract	Understanding masseter muscle (MM) innervation is critical for the study of cell-specific mechanisms of pain induced by temporomandibular disorder (TMDs) or after facial surgery. Here, we identified trigeminal (TG) sensory neuronal subtypes (MM TG neurons) innervating MM fibers, masseteric fascia, tendons, and adjusted tissues. A combination of patch clamp electrophysiology and immunohistochemistry (IHC) on TG neurons back-traced from reporter mouse MM found nine distinct subtypes of MM TG neurons. Of these neurons, 24% belonged to non-peptidergic IB-4
MeSH term(s)	Animals ; Face ; Immunohistochemistry ; Masseter Muscle ; Mice ; Sensory Receptor Cells ; TRPV Cation Channels
Chemical Substances	TRPV Cation Channels
Language	English
Publishing date	2021-10-12
Publishing country	United States
Document type	Journal Article ; Research Support, N.I.H., Extramural
ZDB-ID	2800598-3
ISSN	2373-2822 ; 2373-2822
ISSN (online)	2373-2822
ISSN	2373-2822
DOI	10.1523/ENEURO.0176-21.2021
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Article ; Online: Oscillating from Neurosecretion to Multitasking Dopamine Neurons.

Grattan, David R / Akopian, Armen N

Cell reports

2016 Volume 15, Issue 4, Page(s) 681–682

Abstract: In this issue of Cell Reports, Stagkourakis et al. (2016) report that oscillating hypothalamic TIDA neurons, previously thought to be simple neurosecretory neurons controlling pituitary prolactin secretion, control dopamine output via autoregulatory ... ...

Abstract	In this issue of Cell Reports, Stagkourakis et al. (2016) report that oscillating hypothalamic TIDA neurons, previously thought to be simple neurosecretory neurons controlling pituitary prolactin secretion, control dopamine output via autoregulatory mechanisms and thus could potentially regulate other physiologically important hypothalamic neuronal circuits.
MeSH term(s)	Animals ; Dopaminergic Neurons/metabolism ; Hypothalamus/metabolism ; Models, Biological ; Nerve Net/metabolism ; Neurons/metabolism ; Neurosecretion
Language	English
Publishing date	2016-04-27
Publishing country	United States
Document type	Journal Article ; Comment
ZDB-ID	2649101-1
ISSN	2211-1247 ; 2211-1247
ISSN (online)	2211-1247
ISSN	2211-1247
DOI	10.1016/j.celrep.2016.04.013
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Article ; Online: Prolactin signaling modulates stress-induced behavioral responses in a preclinical mouse model of migraine.

Mason, Bianca N / Kallianpur, Rohini / Price, Theodore J / Akopian, Armen N / Dussor, Gregory O

Headache

2021 Volume 62, Issue 1, Page(s) 11–25

Abstract: ... Plasma prolactin levels were assessed in naïve and stressed CD-1 mice (n = 3-5/group) and transgenic mice ... with conditional deletion of the Prlr in Nav1.8-positive sensory neurons (Prlr conditional knock-out [CKO]; n = 3 ... CD-1 mice were treated with the prolactin release inhibitor bromocriptine (2 mg/kg; n = 7-12/group ...

Abstract	Objective: The aim of this study was to determine if prolactin signaling modulates stress-induced behavioral responses in a preclinical migraine model. Background: Migraine is one of the most complex and prevalent disorders. The involvement of sex-selective hormones in migraine pathology is highly likely as migraine is more common in women and its frequency correlates with reproductive stages. Prolactin has been shown to be a worsening factor for migraine. Normally prolactin levels are low; however levels can surge during stress. Dopamine receptor agonists, which suppress pituitary prolactin release, are an effective migraine treatment in a subset of patients. Previously, we showed that administration of prolactin onto the dura mater induces female-specific behavioral responses, suggesting that prolactin may play a sex-specific role in migraine. Methods: The effects of prolactin signaling were assessed using a preclinical migraine model we published recently in which behavioral sensitization is induced by repeated stress. Plasma prolactin levels were assessed in naïve and stressed CD-1 mice (n = 3-5/group) and transgenic mice with conditional deletion of the Prlr in Nav1.8-positive sensory neurons (Prlr conditional knock-out [CKO]; n = 3/group). To assess the contribution of prolactin release during stress, naïve or stressed male and female CD-1 mice were treated with the prolactin release inhibitor bromocriptine (2 mg/kg; n = 7-12/group) or vehicle for 5 days (8-12/group) and tested for facial hypersensitivity following stress. Additionally, the contribution of ovarian hormones in regulating the prolactin-induced responses was assessed in ovariectomized female CD-1 mice (n = 6-10/group). Furthermore, the contribution of Prlr activation on Nav1.8-positive sensory neurons was assessed. Naïve or stressed male and female Prlr CKO mice and their control littermates were tested for facial hypersensitivity (n = 8-9/group). Immunohistochemistry was used to confirm loss of Prlr in Nav1.8-positive neurons in Prlr CKO mice. The total sample size is n = 245; the full analysis sample size is n = 221. Results: Stress significantly increased prolactin levels in vehicle-treated female mice (39.70 ± 2.77; p < 0.0001). Bromocriptine significantly reduced serum prolactin levels in stressed female mice compared to vehicle-treated mice (-44.85 ± 3.1; p < 0.0001). Additionally, no difference was detected between female stressed mice that received bromocriptine compared to naïve mice treated with bromocriptine (-0.70 ± 2.9; p = 0.995). Stress also significantly increased serum prolactin levels in male mice, although to a much smaller extent than in females (0.61 ± 0.08; p < 0.001). Bromocriptine significantly reduced serum prolactin levels in stressed males compared to those treated with vehicle (-0.49 ± 0.08; p = 0.002). Furthermore, bromocriptine attenuated stress-induced behavioral responses in female mice compared to those treated with vehicle (maximum effect observed on day 4 post stress [0.21 ± 0.08; p = 0.03]). Bromocriptine did not attenuate stress-induced behavior in males at any timepoint compared to those treated with vehicle. Moreover, loss of ovarian hormones did not affect the ability of bromocriptine to attenuate stress responses compared to vehicle-treated ovariectomy mice that were stressed (maximum effect observed on day 4 post stress [0.29 ± 0.078; p = 0.013]). Similar to CD-1 mice, stress increased serum prolactin levels in both Prlr CKO female mice (27.74 ± 9.96; p = 0.047) and control littermates (28.68 ± 9.9; p = 0.041) compared to their naïve counterparts. There was no significant increase in serum prolactin levels detected in male Prlr CKO mice or control littermates. Finally, conditional deletion of Prlr from Nav1.8-positive sensory neurons led to a female-specific attenuation of stress-induced behavioral responses (maximum effect observed on day 7 post stress [0.32 ± 0.08; p = 0.007]) compared to control littermates. Conclusion: These data demonstrate that prolactin plays a female-specific role in stress-induced behavioral responses in this preclinical migraine model through activation of Prlr on sensory neurons. They also support a role for prolactin in migraine mechanisms in females and suggest that modulation of prolactin signaling may be an effective therapeutic strategy in some cases.
MeSH term(s)	Animals ; Behavior, Animal/drug effects ; Behavior, Animal/physiology ; Bromocriptine/administration & dosage ; Bromocriptine/pharmacology ; Disease Models, Animal ; Facial Pain/chemically induced ; Facial Pain/metabolism ; Facial Pain/physiopathology ; Female ; Hormone Antagonists/administration & dosage ; Hormone Antagonists/pharmacology ; Hyperalgesia/chemically induced ; Hyperalgesia/metabolism ; Hyperalgesia/physiopathology ; Male ; Mice ; Mice, Knockout ; Migraine Disorders/metabolism ; Migraine Disorders/physiopathology ; Ovariectomy ; Prolactin/antagonists & inhibitors ; Prolactin/drug effects ; Prolactin/metabolism ; Receptors, Prolactin/genetics ; Sex Characteristics ; Signal Transduction/drug effects ; Signal Transduction/physiology ; Stress, Psychological/metabolism ; Stress, Psychological/physiopathology
Chemical Substances	Hormone Antagonists ; Receptors, Prolactin ; Bromocriptine (3A64E3G5ZO) ; Prolactin (9002-62-4)
Language	English
Publishing date	2021-12-29
Publishing country	United States
Document type	Journal Article
ZDB-ID	410130-3
ISSN	1526-4610 ; 0017-8748
ISSN (online)	1526-4610
ISSN	0017-8748
DOI	10.1111/head.14248
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