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Topoisomerase I inhibition and peripheral nerve injury induce DNA breaks and ATF3-associated axon regeneration in sensory neurons.

Yung-Chih Cheng, Andrew Snavely, Lee B Barrett, Xuefei Zhang, Crystal Herman, Devlin J Frost, Priscilla Riva, Ivan Tochitsky, Riki Kawaguchi, Bhagat Singh, Jelena Ivanis, Eric A Huebner, Anthony Arvanites, Vatsal Oza, Lance Davidow, Rie Maeda, Miyuki Sakuma, Alyssa Grantham, Qing Wang, Amelia N Chang, Kathleen Pfaff, Michael Costigan, Giovanni Coppola, Lee L Rubin, Bjoern Schwer, Frederick W Alt, Clifford J Woolf,

Although axonal damage induces rapid changes in gene expression in primary sensory neurons, it remains unclear how this process is initiated. The transcription factor ATF3, one of the earliest genes responding to nerve injury, regulates expression of downstream genes that enable axon regeneration. By exploiting ATF3 reporter systems, we identify ... Read more >>

Cell Rep (Cell reports)
[2021, 36(10):109666]

Cited: 0 times

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Cytotoxic Immunity in Peripheral Nerve Injury and Pain.

Alexander J Davies, Simon Rinaldi, Michael Costigan, Seog Bae Oh,

Cytotoxicity and consequent cell death pathways are a critical component of the immune response to infection, disease or injury. While numerous examples of inflammation causing neuronal sensitization and pain have been described, there is a growing appreciation of the role of cytotoxic immunity in response to painful nerve injury. In ... Read more >>

Front Neurosci (Frontiers in neuroscience)
[2020, 14:142]

Cited: 7 times

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Intracolonic Mustard Oil Induces Visceral Pain in Mice by TRPA1-Dependent and -Independent Mechanisms: Role of Tissue Injury and P2X Receptors.

Rafael Gonzalez-Cano, Ángeles Montilla-García, Gloria Perazzoli, Jesús M Torres, Francisco J Cañizares, Eduardo Fernández-Segura, Michael Costigan, José M Baeyens, Enrique J Cobos,

Both TRPA1 and purinergic P2X receptors have been proposed as potential targets for the treatment of visceral pain. We found that the intracolonic administration of a low dose mustard oil (0.5%), a well-known TRPA1 agonist, produced nociceptive responses and abdominal wall referred mechanical hyperalgesia, without inducing apparent tissue damage. Both ... Read more >>

Front Pharmacol (Frontiers in pharmacology)
[2020, 11:613068]

Cited: 0 times

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Human induced pluripotent stem cell-derived GABAergic interneuron transplants attenuate neuropathic pain.

John Manion, Thang Khuong, Dylan Harney, Jamie B Littleboy, Travis Ruan, Lipin Loo, Michael Costigan, Mark Larance, Leslie Caron, G Gregory Neely,

Neuropathic pain causes severe suffering, and most patients are resistant to current therapies. A core element of neuropathic pain is the loss of inhibitory tone in the spinal cord. Previous studies have shown that foetal GABAergic neuron precursors can provide relief from pain. However, the source of these precursor cells ... Read more >>

Pain (Pain)
[2020, 161(2):379-387]

Cited: 4 times

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Sepiapterin Reductase Inhibition Leading to Selective Reduction of Inflammatory Joint Pain in Mice and Increased Urinary Sepiapterin Levels in Humans and Mice.

Masahide Fujita, Débora da Luz Scheffer, Bruna Lenfers Turnes, Shane J F Cronin, Alban Latrémolière, Michael Costigan, Clifford J Woolf, Alexandra Latini, Nick A Andrews,

<h4>Objective</h4>To evaluate the antiinflammatory and analgesic effects of sepiapterin reductase (SPR) inhibition in a mouse model of inflammatory joint disease, and to determine whether urinary sepiapterin levels, as measured in mice and healthy human volunteers, could be useful as a noninvasive, translational biomarker of SPR inhibition/target engagement.<h4>Methods</h4>The collagen antibody-induced arthritis ... Read more >>

Arthritis Rheumatol (Arthritis & rheumatology (Hoboken, N.J.))
[2020, 72(1):57-66]

Cited: 4 times

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The Genetics of Neuropathic Pain from Model Organisms to Clinical Application.

Margarita Calvo, Alexander J Davies, Harry L Hébert, Greg A Weir, Elissa J Chesler, Nanna B Finnerup, Roy C Levitt, Blair H Smith, G Gregory Neely, Michael Costigan, David L Bennett,

Neuropathic pain (NeuP) arises due to injury of the somatosensory nervous system and is both common and disabling, rendering an urgent need for non-addictive, effective new therapies. Given the high evolutionary conservation of pain, investigative approaches from Drosophila mutagenesis to human Mendelian genetics have aided our understanding of the maladaptive ... Read more >>

Neuron (Neuron)
[2019, 104(4):637-653]

Cited: 18 times

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Reading and writing: the evolution of molecular pain genetics.

Daniel Bullock, Aaron Jesuthasan, Rafael González-Cano, Michael Costigan,

Pain (Pain)
[2019, 160(10):2177-2185]

Cited: 0 times

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Publisher Correction: The metabolite BH4 controls T cell proliferation in autoimmunity and cancer.

Shane J F Cronin, Corey Seehus, Adelheid Weidinger, Sebastien Talbot, Sonja Reissig, Markus Seifert, Yann Pierson, Eileen McNeill, Maria Serena Longhi, Bruna Lenfers Turnes, Taras Kreslavsky, Melanie Kogler, David Hoffmann, Melita Ticevic, Débora da Luz Scheffer, Luigi Tortola, Domagoj Cikes, Alexander Jais, Manu Rangachari, Shuan Rao, Magdalena Paolino, Maria Novatchkova, Martin Aichinger, Lee Barrett, Alban Latremoliere, Gerald Wirnsberger, Guenther Lametschwandtner, Meinrad Busslinger, Stephen Zicha, Alexandra Latini, Simon C Robson, Ari Waisman, Nick Andrews, Michael Costigan, Keith M Channon, Guenter Weiss, Andrey V Kozlov, Mark Tebbe, Kai Johnsson, Clifford J Woolf, Josef M Penninger,

An Amendment to this paper has been published and can be accessed via a link at the top of the paper. ... Read more >>

Nature (Nature)
[2019, 572(7769):E18]

Cited: 0 times

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The metabolite BH4 controls T cell proliferation in autoimmunity and cancer.

Shane J F Cronin, Corey Seehus, Adelheid Weidinger, Sebastien Talbot, Sonja Reissig, Markus Seifert, Yann Pierson, Eileen McNeill, Maria Serena Longhi, Bruna Lenfers Turnes, Taras Kreslavsky, Melanie Kogler, David Hoffmann, Melita Ticevic, Débora da Luz Scheffer, Luigi Tortola, Domagoj Cikes, Alexander Jais, Manu Rangachari, Shuan Rao, Magdalena Paolino, Maria Novatchkova, Martin Aichinger, Lee Barrett, Alban Latremoliere, Gerald Wirnsberger, Guenther Lametschwandtner, Meinrad Busslinger, Stephen Zicha, Alexandra Latini, Simon C Robson, Ari Waisman, Nick Andrews, Michael Costigan, Keith M Channon, Guenter Weiss, Andrey V Kozlov, Mark Tebbe, Kai Johnsson, Clifford J Woolf, Josef M Penninger,

Genetic regulators and environmental stimuli modulate T cell activation in autoimmunity and cancer. The enzyme co-factor tetrahydrobiopterin (BH4) is involved in the production of monoamine neurotransmitters, the generation of nitric oxide, and pain<sup>1,2</sup>. Here we uncover a link between these processes, identifying a fundamental role for BH4 in T cell biology. We ... Read more >>

Nature (Nature)
[2018, 563(7732):564-568]

Cited: 45 times

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Diltiazem Promotes Regenerative Axon Growth.

Eric A Huebner, Stéphane Budel, Zhaoxin Jiang, Takao Omura, Tammy Szu-Yu Ho, Lee Barrett, Janie S Merkel, Luis M Pereira, Nick A Andrews, Xingxing Wang, Bhagat Singh, Kush Kapur, Michael Costigan, Stephen M Strittmatter, Clifford J Woolf,

Axotomy results in permanent loss of function after brain and spinal cord injuries due to the minimal regenerative propensity of the adult central nervous system (CNS). To identify pharmacological enhancers of axon regeneration, 960 compounds were screened for cortical neuron axonal regrowth using an in vitro cortical scrape assay. Diltiazem, ... Read more >>

Mol Neurobiol (Molecular neurobiology)
[2019, 56(6):3948-3957]

Cited: 4 times

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Up-Down Reader: An Open Source Program for Efficiently Processing 50% von Frey Thresholds.

Rafael Gonzalez-Cano, Bruno Boivin, Daniel Bullock, Laura Cornelissen, Nick Andrews, Michael Costigan,

Most pathological pain conditions in patients and rodent pain models result in marked alterations in mechanosensation and the gold standard way to measure this is by use of von Frey fibers. These graded monofilaments are used to gauge the level of stimulus-evoked sensitivity present in the affected dermal region. One ... Read more >>

Front Pharmacol (Frontiers in pharmacology)
[2018, 9:433]

Cited: 5 times

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Neuropathic pain drives anxiety behavior in mice, results consistent with anxiety levels in diabetic neuropathy patients.

Christine B Sieberg, Caitlin Taras, Aya Gomaa, Chelsea Nickerson, Cindy Wong, Catherine Ward, Georgios Baskozos, David L H Bennett, Juan D Ramirez, Andreas C Themistocleous, Andrew S C Rice, Pallai R Shillo, Solomon Tesfaye, Robert R Edwards, Nick A Andrews, Charles Berde, Michael Costigan,

<h4>Background</h4>Epidemiological studies in patients with neuropathic pain demonstrate a strong association with psychiatric conditions such as anxiety; however, the precipitating pathology between these symptoms remains unclear. To investigate this, we studied the effects of lifelong stress on levels of neuropathic pain-like behavior and conversely, the effects of chronic neuropathic injury ... Read more >>

Pain Rep (Pain reports)
[2018, 3(3):e651]

Cited: 11 times

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Mechanistic Differences in Neuropathic Pain Modalities Revealed by Correlating Behavior with Global Expression Profiling.

Enrique J Cobos, Chelsea A Nickerson, Fuying Gao, Vijayendran Chandran, Inmaculada Bravo-Caparrós, Rafael González-Cano, Priscilla Riva, Nick A Andrews, Alban Latremoliere, Corey R Seehus, Gloria Perazzoli, Francisco R Nieto, Nicole Joller, Michio W Painter, Chi Him Eddie Ma, Takao Omura, Elissa J Chesler, Daniel H Geschwind, Giovanni Coppola, Manu Rangachari, Clifford J Woolf, Michael Costigan,

Chronic neuropathic pain is a major morbidity of neural injury, yet its mechanisms are incompletely understood. Hypersensitivity to previously non-noxious stimuli (allodynia) is a common symptom. Here, we demonstrate that the onset of cold hypersensitivity precedes tactile allodynia in a model of partial nerve injury, and this temporal divergence was ... Read more >>

Cell Rep (Cell reports)
[2018, 22(5):1301-1312]

Cited: 42 times

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Enhanced Neuronal Regeneration in the CAST/Ei Mouse Strain Is Linked to Expression of Differentiation Markers after Injury.

Véronique Lisi, Bhagat Singh, Michel Giroux, Elmer Guzman, Michio W Painter, Yung-Chih Cheng, Eric Huebner, Giovanni Coppola, Michael Costigan, Clifford J Woolf, Kenneth S Kosik,

Peripheral nerve regeneration after injury requires a broad program of transcriptional changes. We investigated the basis for the enhanced nerve regenerative capacity of the CAST/Ei mouse strain relative to C57BL/6 mice. RNA sequencing of dorsal root ganglia (DRG) showed a CAST/Ei-specific upregulation of Ascl1 after injury. Ascl1 overexpression in DRG neurons of ... Read more >>

Cell Rep (Cell reports)
[2017, 20(5):1136-1147]

Cited: 9 times

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Combining Human and Rodent Genetics to Identify New Analgesics.

Alban Latremoliere, Michael Costigan,

Most attempts at rational development of new analgesics have failed, in part because chronic pain involves multiple processes that remain poorly understood. To improve translational success, one strategy is to select novel targets for which there is proof of clinical relevance, either genetically through heritable traits, or pharmacologically. Such an ... Read more >>

Neurosci Bull (Neuroscience bulletin)
[2018, 34(1):143-155]

Cited: 1 time

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Arachidonic acid containing phosphatidylcholine increases due to microglial activation in ipsilateral spinal dorsal horn following spared sciatic nerve injury.

Tomohiro Banno, Takao Omura, Noritaka Masaki, Hideyuki Arima, Dongmin Xu, Ayako Okamoto, Michael Costigan, Alban Latremoliere, Yukihiro Matsuyama, Mitsutoshi Setou,

Peripheral nerve injury induces substantial molecular changes in the somatosensory system that leads to maladaptive plasticity and cause neuropathic pain. Understanding the molecular pathways responsible for the development of neuropathic pain is essential to the development of novel rationally designed therapeutics. Although lipids make up to half of the dry ... Read more >>

PLoS One (PloS one)
[2017, 12(5):e0177595]

Cited: 4 times

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Time-Resolved Fast Mammalian Behavior Reveals the Complexity of Protective Pain Responses.

Liam E Browne, Alban Latremoliere, Brendan P Lehnert, Alyssa Grantham, Catherine Ward, Chloe Alexandre, Michael Costigan, Frédéric Michoud, David P Roberson, David D Ginty, Clifford J Woolf,

Potentially harmful stimuli are detected at the skin by nociceptor sensory neurons that drive rapid protective withdrawal reflexes and pain. We set out to define, at a millisecond timescale, the relationship between the activity of these sensory neurons and the resultant behavioral output. Brief optogenetic activation of cutaneous nociceptors was ... Read more >>

Cell Rep (Cell reports)
[2017, 20(1):89-98]

Cited: 10 times

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Enhanced neuronal regeneration in the CAST/Ei mouse strain is linked to expression of differentiation markers after injury

Véronique Lisi, Bhagat Singh, Michel Giroux, Elmer Guzman, Michio Painter, Yung-Chih Cheng, Eric Huebner, Giovanni Coppola, Michael Costigan, Clifford Woolf, Kenneth Kosik,

<h4>Summary</h4> Peripheral nerve regeneration after injury requires a broad program of transcriptional changes. We investigated the basis for the enhanced nerve regenerative capacity of the CAST/Ei mouse strain relative to C57BL/6 mice. RNA sequencing of dorsal root ganglia (DRG) showed a CAST/Ei specific upregulation of Ascl1 after injury. Ascl1 overexpression ... Read more >>

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Robust Axonal Regeneration Occurs in the Injured CAST/Ei Mouse CNS.

Takao Omura, Kumiko Omura, Andrea Tedeschi, Priscilla Riva, Michio W Painter, Leticia Rojas, Joshua Martin, Véronique Lisi, Eric A Huebner, Alban Latremoliere, Yuqin Yin, Lee B Barrett, Bhagat Singh, Stella Lee, Tom Crisman, Fuying Gao, Songlin Li, Kush Kapur, Daniel H Geschwind, Kenneth S Kosik, Giovanni Coppola, Zhigang He, S Thomas Carmichael, Larry I Benowitz, Michael Costigan, Clifford J Woolf,

Neuron (Neuron)
[2016, 90(3):662]

Cited: 4 times

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Transcriptomic Approaches to Neural Repair.

Jennifer N Dulin, Ana Antunes-Martins, Vijayendran Chandran, Michael Costigan, Jessica K Lerch, Dianna E Willis, Mark H Tuszynski,

<h4>Unlabelled</h4>Understanding why adult CNS neurons fail to regenerate their axons following injury remains a central challenge of neuroscience research. A more complete appreciation of the biological mechanisms shaping the injured nervous system is a crucial prerequisite for the development of robust therapies to promote neural repair. Historically, the identification of ... Read more >>

J Neurosci (The Journal of neuroscience : the official journal of the Society for Neuroscience)
[2015, 35(41):13860-13867]

Cited: 15 times

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Reduction of Neuropathic and Inflammatory Pain through Inhibition of the Tetrahydrobiopterin Pathway.

Alban Latremoliere, Alexandra Latini, Nick Andrews, Shane J Cronin, Masahide Fujita, Katarzyna Gorska, Ruud Hovius, Carla Romero, Surawee Chuaiphichai, Michio Painter, Giulia Miracca, Olusegun Babaniyi, Aline Pertile Remor, Kelly Duong, Priscilla Riva, Lee B Barrett, Nerea Ferreirós, Alasdair Naylor, Josef M Penninger, Irmgard Tegeder, Jian Zhong, Julian Blagg, Keith M Channon, Kai Johnsson, Michael Costigan, Clifford J Woolf,

Human genetic studies have revealed an association between GTP cyclohydrolase 1 polymorphisms, which decrease tetrahydrobiopterin (BH4) levels, and reduced pain in patients. We now show that excessive BH4 is produced in mice by both axotomized sensory neurons and macrophages infiltrating damaged nerves and inflamed tissue. Constitutive BH4 overproduction in sensory ... Read more >>

Neuron (Neuron)
[2015, 86(6):1393-1406]

Cited: 39 times

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The serine protease inhibitor SerpinA3N attenuates neuropathic pain by inhibiting T cell-derived leukocyte elastase.

Lucas Vicuña, David E Strochlic, Alban Latremoliere, Kiran Kumar Bali, Manuela Simonetti, Dewi Husainie, Sandra Prokosch, Priscilla Riva, Robert S Griffin, Christian Njoo, Stefanie Gehrig, Marcus A Mall, Bernd Arnold, Marshall Devor, Clifford J Woolf, Stephen D Liberles, Michael Costigan, Rohini Kuner,

Neuropathic pain is a major, intractable clinical problem and its pathophysiology is not well understood. Although recent gene expression profiling studies have enabled the identification of novel targets for pain therapy, classical study designs provide unclear results owing to the differential expression of hundreds of genes across sham and nerve-injured ... Read more >>

Nat Med (Nature medicine)
[2015, 21(5):518-523]

Cited: 76 times

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Robust Axonal Regeneration Occurs in the Injured CAST/Ei Mouse CNS.

Takao Omura, Kumiko Omura, Andrea Tedeschi, Priscilla Riva, Michio W Painter, Leticia Rojas, Joshua Martin, Véronique Lisi, Eric A Huebner, Alban Latremoliere, Yuqin Yin, Lee B Barrett, Bhagat Singh, Stella Lee, Tom Crisman, Fuying Gao, Songlin Li, Kush Kapur, Daniel H Geschwind, Kenneth S Kosik, Giovanni Coppola, Zhigang He, S Thomas Carmichael, Larry I Benowitz, Michael Costigan, Clifford J Woolf,

Axon regeneration in the CNS requires reactivating injured neurons' intrinsic growth state and enabling growth in an inhibitory environment. Using an inbred mouse neuronal phenotypic screen, we find that CAST/Ei mouse adult dorsal root ganglion neurons extend axons more on CNS myelin than the other eight strains tested, especially when ... Read more >>

Neuron (Neuron)
[2015, 86(5):1215-1227]

Cited: 43 times

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Post-stroke pain hypersensitivity induced by experimental thalamic hemorrhage in rats is region-specific and demonstrates limited efficacy of gabapentin.

Fei Yang, Han Fu, Yun-Fei Lu, Xiao-Liang Wang, Yan Yang, Fan Yang, Yao-Qing Yu, Wei Sun, Jia-Shuang Wang, Michael Costigan, Jun Chen,

Intractable central post-stroke pain (CPSP) is one of the most common sequelae of stroke, but has been inadequately studied to date. In this study, we first determined the relationship between the lesion site and changes in mechanical or thermal pain sensitivity in a rat CPSP model with experimental thalamic hemorrhage ... Read more >>

Neurosci Bull (Neuroscience bulletin)
[2014, 30(6):887-902]

Cited: 13 times

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Heritability of nociception IV: neuropathic pain assays are genetically distinct across methods of peripheral nerve injury.

Erin E Young, Michael Costigan, Teri A Herbert, William R Lariviere,

Prior genetic correlation analysis of 22 heritable behavioral measures of nociception and hypersensitivity in the mouse identified 5 genetically distinct pain types. In the present study, we reanalyzed that dataset and included the results of an additional 9 assays of nociception and hypersensitivity, with the following goals: to replicate the ... Read more >>

Pain (Pain)
[2014, 155(5):868-880]

Cited: 9 times

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