ABOUT THE RESEARCHER

OVERVIEW

Neuronal plasticity, its mechanistic basis, how it contributes to the normal and abnormal functions of the nervous system, and how it can be a target for therapy comprise the major focus of Dr. Woolf’s investigations. Specifically, he studies neural plasticity in relation to pain, regeneration, neurodegenerative disorders and developmental neurobiology.

 

Dr. Woolf has spearheaded discoveries on how functional synaptic plasticity, structural reorganization of synaptic architecture, injury-induced transcriptional changes, neuro-immune interactions and activity-dependent loss of interneurons all contribute to the pathogenesis and maintenance of pain. He has linked polymorphisms in human genes with the risk of developing pain and has pioneered new ways of phenotyping pain in patients. His work has led to the identification of novel targets for analgesics, and, with Bruce Bean at HMS, he has discovered a way of producing a long-lasting local analgesia. With Lee Rubin at HU, he has converted human embryonic stem cells into pain neurons for disease modeling and testing analgesics and with Josef Penninger used genome-wide screens in Drosophila to identify novel pain genes.

 

Additionally, Dr. Woolf has explored how axonal injury activates a survival and regeneration program in sensory and motor neurons, and he has identified the transcription factors that act as master regulators of these. This has led to novel genetic approaches to increase regeneration and ameliorate motor neuron disease.

 

Currently devoted to investigating how the functional, chemical and structural plasticity of neurons contributes to adaptive and maladaptive functions of the mammalian nervous system, the Woolf lab’s major efforts are dedicated to the study of pain, the formation of neural circuits during development, and the failure of regeneration in the adult CNS. Most of this work is focused on primary sensory and spinal cord neurons, which are studied using a multidisciplinary approach that spans mouse and human genetics, molecular and cell biology, bioinformatics, synaptic electrophysiology, neuroanatomy, integrative systems biology and behavior. The lab represents a complex mixture of basic and translational neuroscience and works closely with a wide number of academic groups and the pharmaceutical and biotechnology industry to identify and validate molecular targets for novel analgesics and axonal growth determinants. 

Some of the Group’s major current interests include: 

  • Neuro-immune interactions
  • Post-translational processing and transcriptional control of membrane receptors and ion channels mediating pain hypersensitivity
  • Intracellular signal transduction cascade in neurons
  • Role of transcription factors as master regulators of neuronal function
  • Exploiting stem cell technology to model human neurological disease
  • Mechanisms responsible for cell survival in injured sensory and motor neurons
  • Contributions of intrinsic growth determinants in establishing regenerative capacity
  • Central sensitization, its mechanism and contribution to pain
  • Bioinformatic analyses of  the transcriptome in neurons
  • Role of tetrahydrobiopterin in pain
  • Genotype – phenotype associations in pain
  • Targeting drugs selectively into neurons via large pore channels

BACKGROUND

Clifford Woolf, MB, BCh, PhD was appointed Director of the F.M. Kirby Neurobiology Center and the Neurobiology Program at Boston Children's Hospital in February 2010. After training for his MD and PhD at the University of the Witwatersrand in Johannesburg South Africa, Dr. Woolf moved to England in 1978. He worked at University College London for close on 20 years, towards the latter part as a Professor of Neurobiology. In 1997, Dr. Woolf moved to Boston as the first incumbent of the Richard J Kitz Chair of Anesthesia Research at Harvard Medical School and established the Neural Plasticity Research Group, based in the Department of Anesthesia and Critical Care at the Massachusetts General Hospital. Dr Woolf is a faculty member of the Harvard Stem Cell Institute and the Department of Neurobiology at Harvard Medical School.

Honors: 1973   William Cullen Medal, University of the Witwatersrand, Johannesburg, South Africa, for most distinguished B.Sc. graduate in the Faculty of Science; 1977 South African Medical Association Medal for most distinguished Medical graduate; 1987 Distinguished Young Investigator Award, International Association for the Study of Pain; 1991 Bristol-Myers Squibb Pain Research Award; 2001 Spine Society of Europe Medal; 2002 Bonica Medal; 2004 American Society of Anesthesia Award for Excellence in Research; 2009 Wall Medal, Royal College of Anaesthetists. 2010 Bonica Lecture, International Association for the Study of Pain; 2011 Javits Award NINDS; 2012  American Neurological Association F.E. Bennett Memorial Lectureship Award; 2013 Magnes Medal Israel; 2016 Reeve-Irvine Research Medal; 2017 Gill Distinguished Scientist Award; 2020 American Academy of Arts and Sciences.

PUBLICATIONS

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  1. Topoisomerase I inhibition and peripheral nerve injury induce DNA breaks and ATF3-associated axon regeneration in sensory neurons. Cell Rep. 2021 Sep 07; 36(10):109666. View abstract
  2. DeepEthogram, a machine learning pipeline for supervised behavior classification from raw pixels. Elife. 2021 Sep 02; 10. View abstract
  3. Dissecting the precise nature of itch-evoked scratching. Neuron. 2021 Aug 10. View abstract
  4. Promoting Long-Term Cultivation of Motor Neurons for 3D Neuromuscular Junction Formation of 3D In Vitro Using Central-Nervous-Tissue-Derived Bioink. Adv Healthc Mater. 2021 Sep; 10(18):e2100581. View abstract
  5. Isolation of Nuclei from Mouse Dorsal Root Ganglia for Single-nucleus Genomics. Bio Protoc. 2021 Aug 05; 11(15):e4102. View abstract
  6. Inhibition of inflammatory pain and cough by a novel charged sodium channel blocker. Br J Pharmacol. 2021 Oct; 178(19):3905-3923. View abstract
  7. Human amyotrophic lateral sclerosis excitability phenotype screen: Target discovery and validation. Cell Rep. 2021 Jun 08; 35(10):109224. View abstract
  8. Two independent mouse lines carrying the Nav1.7 I228M gain-of-function variant display dorsal root ganglion neuron hyperexcitability but a minimal pain phenotype. Pain. 2021 06 01; 162(6):1758-1770. View abstract
  9. Human cells and networks of pain: Transforming pain target identification and therapeutic development. Neuron. 2021 05 05; 109(9):1426-1429. View abstract
  10. Reduced MC4R signaling alters nociceptive thresholds associated with red hair. Sci Adv. 2021 Apr; 7(14). View abstract
  11. Effect of Ezogabine on Cortical and Spinal Motor Neuron Excitability in Amyotrophic Lateral Sclerosis: A Randomized Clinical Trial. JAMA Neurol. 2021 Feb 01; 78(2):186-196. View abstract
  12. Research design considerations for chronic pain prevention clinical trials: IMMPACT recommendations. Pain Rep. 2021; 6(1):e895. View abstract
  13. FceR1-expressing nociceptors trigger allergic airway inflammation. J Allergy Clin Immunol. 2021 Jun; 147(6):2330-2342. View abstract
  14. Brain Responses to Noxious Stimuli in Patients With Chronic Pain: A Systematic Review and Meta-analysis. JAMA Netw Open. 2021 01 04; 4(1):e2032236. View abstract
  15. Epineural optogenetic activation of nociceptors initiates and amplifies inflammation. Nat Biotechnol. 2021 02; 39(2):179-185. View abstract
  16. Transcriptional Reprogramming of Distinct Peripheral Sensory Neuron Subtypes after Axonal Injury. Neuron. 2020 10 14; 108(1):128-144.e9. View abstract
  17. Nonsurgical mouse model of endometriosis-associated pain that responds to clinically active drugs. Pain. 2020 06; 161(6):1321-1331. View abstract
  18. Vagal sensory neurons drive mucous cell metaplasia. J Allergy Clin Immunol. 2020 06; 145(6):1693-1696.e4. View abstract
  19. Unraveling the Plastic Peripheral Neuroimmune Interactome. J Immunol. 2020 01 15; 204(2):257-263. View abstract
  20. Convergent neural representations of experimentally-induced acute pain in healthy volunteers: A large-scale fMRI meta-analysis. Neurosci Biobehav Rev. 2020 05; 112:300-323. View abstract
  21. Sepiapterin Reductase Inhibition Leading to Selective Reduction of Inflammatory Joint Pain in Mice and Increased Urinary Sepiapterin Levels in Humans and Mice. Arthritis Rheumatol. 2020 01; 72(1):57-66. View abstract
  22. Novel charged sodium and calcium channel inhibitor active against neurogenic inflammation. Elife. 2019 11 25; 8. View abstract
  23. The Role of Iron Regulation in Immunometabolism and Immune-Related Disease. Front Mol Biosci. 2019; 6:116. View abstract
  24. Recurrent SMARCB1 Mutations Reveal a Nucleosome Acidic Patch Interaction Site That Potentiates mSWI/SNF Complex Chromatin Remodeling. Cell. 2019 11 27; 179(6):1342-1356.e23. View abstract
  25. Publisher Correction: The metabolite BH4 controls T cell proliferation in autoimmunity and cancer. Nature. 2019 Aug; 572(7769):E18. View abstract
  26. Capturing Novel Non-opioid Pain Targets. Biol Psychiatry. 2020 01 01; 87(1):74-81. View abstract
  27. Composite Pain Biomarker Signatures for Objective Assessment and Effective Treatment. Neuron. 2019 03 06; 101(5):783-800. View abstract
  28. ALS-implicated protein TDP-43 sustains levels of STMN2, a mediator of motor neuron growth and repair. Nat Neurosci. 2019 02; 22(2):167-179. View abstract
  29. Neurite Collapse and Altered ER Ca2+ Control in Human Parkinson Disease Patient iPSC-Derived Neurons with LRRK2 G2019S Mutation. Stem Cell Reports. 2019 01 08; 12(1):29-41. View abstract
  30. The metabolite BH4 controls T cell proliferation in autoimmunity and cancer. Nature. 2018 11; 563(7732):564-568. View abstract
  31. Author Correction: Commensal microflora-induced T cell responses mediate progressive neurodegeneration in glaucoma. Nat Commun. 2018 09 20; 9(1):3914. View abstract
  32. Diltiazem Promotes Regenerative Axon Growth. Mol Neurobiol. 2019 Jun; 56(6):3948-3957. View abstract
  33. Touch and tactile neuropathic pain sensitivity are set by corticospinal projections. Nature. 2018 09; 561(7724):547-550. View abstract
  34. Axonal G3BP1 stress granule protein limits axonal mRNA translation and nerve regeneration. Nat Commun. 2018 08 22; 9(1):3358. View abstract
  35. Neuronal-Specific TUBB3 Is Not Required for Normal Neuronal Function but Is Essential for Timely Axon Regeneration. Cell Rep. 2018 08 14; 24(7):1865-1879.e9. View abstract
  36. Commensal microflora-induced T cell responses mediate progressive neurodegeneration in glaucoma. Nat Commun. 2018 08 10; 9(1):3209. View abstract
  37. Purkinje cells derived from TSC patients display hypoexcitability and synaptic deficits associated with reduced FMRP levels and reversed by rapamycin. Mol Psychiatry. 2018 11; 23(11):2167-2183. View abstract
  38. Optical cuff for optogenetic control of the peripheral nervous system. J Neural Eng. 2018 02; 15(1):015002. View abstract
  39. Mechanistic Differences in Neuropathic Pain Modalities Revealed by Correlating Behavior with Global Expression Profiling. Cell Rep. 2018 01 30; 22(5):1301-1312. View abstract
  40. Staphylococcus aureus produces pain through pore-forming toxins and neuronal TRPV1 that is silenced by QX-314. Nat Commun. 2018 01 02; 9(1):37. View abstract
  41. Sense and Immunity: Context-Dependent Neuro-Immune Interplay. Front Immunol. 2017; 8:1463. View abstract
  42. Mouse embryonic stem cells can differentiate via multiple paths to the same state. Elife. 2017 10 09; 6. View abstract
  43. Breaking barriers to novel analgesic drug development. Nat Rev Drug Discov. 2017 11; 16(11):810. View abstract
  44. Crosstalk between KCNK3-Mediated Ion Current and Adrenergic Signaling Regulates Adipose Thermogenesis and Obesity. Cell. 2017 Nov 02; 171(4):836-848.e13. View abstract
  45. Enhanced Neuronal Regeneration in the CAST/Ei Mouse Strain Is Linked to Expression of Differentiation Markers after Injury. Cell Rep. 2017 08 01; 20(5):1136-1147. View abstract
  46. Time-Resolved Fast Mammalian Behavior Reveals the Complexity of Protective Pain Responses. Cell Rep. 2017 07 05; 20(1):89-98. View abstract
  47. Breaking barriers to novel analgesic drug development. Nat Rev Drug Discov. 2017 Aug; 16(8):545-564. View abstract
  48. Decreased alertness due to sleep loss increases pain sensitivity in mice. Nat Med. 2017 Jun; 23(6):768-774. View abstract
  49. The G2A receptor (GPR132) contributes to oxaliplatin-induced mechanical pain hypersensitivity. Sci Rep. 2017 03 27; 7(1):446. View abstract
  50. Time for nonaddictive relief of pain. Science. 2017 Mar 10; 355(6329):1026-1027. View abstract
  51. Substance P activates Mas-related G protein-coupled receptors to induce itch. J Allergy Clin Immunol. 2017 Aug; 140(2):447-453.e3. View abstract
  52. Neuronal Circuits Modulate Antigen Flow Through Lymph Nodes. Bioelectron Med. 2016; 3:18-28. View abstract
  53. Targeting CYP2J to reduce paclitaxel-induced peripheral neuropathic pain. Proc Natl Acad Sci U S A. 2016 11 01; 113(44):12544-12549. View abstract
  54. Toward a Mechanism-Based Approach to Pain Diagnosis. J Pain. 2016 09; 17(9 Suppl):T50-69. View abstract
  55. Nucleolin-Mediated RNA Localization Regulates Neuron Growth and Cycling Cell Size. Cell Rep. 2016 08 09; 16(6):1664-1676. View abstract
  56. Pain and infection: pathogen detection by nociceptors. Pain. 2016 06; 157(6):1192-1193. View abstract
  57. Robust Axonal Regeneration Occurs in the Injured CAST/Ei Mouse CNS. Neuron. 2016 May 04; 90(3):662. View abstract
  58. Ensuring transparency and minimization of methodologic bias in preclinical pain research: PPRECISE considerations. Pain. 2016 Apr; 157(4):901-909. View abstract
  59. Inhibition of the kinase WNK1/HSN2 ameliorates neuropathic pain by restoring GABA inhibition. Sci Signal. 2016 Mar 29; 9(421):ra32. View abstract
  60. Association of Joint Inflammation With Pain Sensitization in Knee Osteoarthritis: The Multicenter Osteoarthritis Study. Arthritis Rheumatol. 2016 Mar; 68(3):654-61. View abstract
  61. Neuroimmunity: Physiology and Pathology. Annu Rev Immunol. 2016 05 20; 34:421-47. View abstract
  62. A Systems-Level Analysis of the Peripheral Nerve Intrinsic Axonal Growth Program. Neuron. 2016 Mar 02; 89(5):956-70. View abstract
  63. CD11b+Ly6G- myeloid cells mediate mechanical inflammatory pain hypersensitivity. Proc Natl Acad Sci U S A. 2015 Dec 08; 112(49):E6808-17. View abstract
  64. Doublecortin-Like Kinases Promote Neuronal Survival and Induce Growth Cone Reformation via Distinct Mechanisms. Neuron. 2015 Nov 18; 88(4):704-19. View abstract
  65. Lack of motor recovery after prolonged denervation of the neuromuscular junction is not due to regenerative failure. Eur J Neurosci. 2016 Feb; 43(3):451-62. View abstract
  66. The Stress-Induced Atf3-Gelsolin Cascade Underlies Dendritic Spine Deficits in Neuronal Models of Tuberous Sclerosis Complex. J Neurosci. 2015 Jul 29; 35(30):10762-72. View abstract
  67. From Dish to Bedside: Lessons Learned While Translating Findings from a Stem Cell Model of Disease to a Clinical Trial. Cell Stem Cell. 2015 Jul 02; 17(1):8-10. View abstract
  68. Research design considerations for chronic pain prevention clinical trials: IMMPACT recommendations. Pain. 2015 Jul; 156(7):1184-1197. View abstract
  69. Silencing Nociceptor Neurons Reduces Allergic Airway Inflammation. Neuron. 2015 Jul 15; 87(2):341-54. View abstract
  70. Reduction of Neuropathic and Inflammatory Pain through Inhibition of the Tetrahydrobiopterin Pathway. Neuron. 2015 Jun 17; 86(6):1393-406. View abstract
  71. Robust Axonal Regeneration Occurs in the Injured CAST/Ei Mouse CNS. Neuron. 2015 Jun 03; 86(5):1215-27. View abstract
  72. Injury-induced decline of intrinsic regenerative ability revealed by quantitative proteomics. Neuron. 2015 May 20; 86(4):1000-1014. View abstract
  73. The serine protease inhibitor SerpinA3N attenuates neuropathic pain by inhibiting T cell-derived leukocyte elastase. Nat Med. 2015 May; 21(5):518-23. View abstract
  74. CNS injury: IL-33 sounds the alarm. Immunity. 2015 Mar 17; 42(3):403-5. View abstract
  75. Correction: Transcriptional profiling at whole population and single cell levels reveals somatosensory neuron molecular diversity. Elife. 2015 Feb 06; 4:e06720. View abstract
  76. Early psychological reactions in parents of children with a life threatening illness within a pediatric hospital setting. Eur Psychiatry. 2015 Jul; 30(5):555-61. View abstract
  77. Transcriptional profiling at whole population and single cell levels reveals somatosensory neuron molecular diversity. Elife. 2014 Dec 19; 3. View abstract
  78. Modeling pain in vitro using nociceptor neurons reprogrammed from fibroblasts. Nat Neurosci. 2015 Jan; 18(1):17-24. View abstract
  79. A three-dimensional human neural cell culture model of Alzheimer's disease. Nature. 2014 Nov 13; 515(7526):274-8. View abstract
  80. Ronald R. Tasker Young Investigator Award 165 Promoting Endogenous GABAergic Analgesia via Kinase Modulation of Neuronal Ion Plasticity. Neurosurgery. 2014 Aug; 61 Suppl 1:214. View abstract
  81. What to call the amplification of nociceptive signals in the central nervous system that contribute to widespread pain? Pain. 2014 Oct; 155(10):1911-1912. View abstract
  82. Diminished Schwann cell repair responses underlie age-associated impaired axonal regeneration. Neuron. 2014 Jul 16; 83(2):331-343. View abstract
  83. Skin ß-endorphin mediates addiction to UV light. Cell. 2014 Jun 19; 157(7):1527-34. View abstract
  84. Therapeutic restoration of spinal inhibition via druggable enhancement of potassium-chloride cotransporter KCC2-mediated chloride extrusion in peripheral neuropathic pain. JAMA Neurol. 2014 May; 71(5):640-5. View abstract
  85. Intrinsic membrane hyperexcitability of amyotrophic lateral sclerosis patient-derived motor neurons. Cell Rep. 2014 Apr 10; 7(1):1-11. View abstract
  86. Pathways disrupted in human ALS motor neurons identified through genetic correction of mutant SOD1. Cell Stem Cell. 2014 Jun 05; 14(6):781-95. View abstract
  87. Casting light on pain. Nat Biotechnol. 2014 Mar; 32(3):240-1. View abstract
  88. ATF3 expression improves motor function in the ALS mouse model by promoting motor neuron survival and retaining muscle innervation. Proc Natl Acad Sci U S A. 2014 Jan 28; 111(4):1622-7. View abstract
  89. Bupivacaine-induced cellular entry of QX-314 and its contribution to differential nerve block. Br J Pharmacol. 2014 Jan; 171(2):438-51. View abstract
  90. Sensitivity and sensitisation in relation to pain severity in knee osteoarthritis: trait or state? Ann Rheum Dis. 2015 Apr; 74(4):682-8. View abstract
  91. Bacteria activate sensory neurons that modulate pain and inflammation. Nature. 2013 Sep 05; 501(7465):52-7. View abstract
  92. Activity-dependent silencing reveals functionally distinct itch-generating sensory neurons. Nat Neurosci. 2013 Jul; 16(7):910-8. View abstract
  93. A small molecule screen in stem-cell-derived motor neurons identifies a kinase inhibitor as a candidate therapeutic for ALS. Cell Stem Cell. 2013 Jun 06; 12(6):713-26. View abstract
  94. CLP1 links tRNA metabolism to progressive motor-neuron loss. Nature. 2013 Mar 28; 495(7442):474-80. View abstract
  95. Photochemical activation of TRPA1 channels in neurons and animals. Nat Chem Biol. 2013 Apr; 9(4):257-63. View abstract
  96. Personalized medicine and opioid analgesic prescribing for chronic pain: opportunities and challenges. J Pain. 2013 Feb; 14(2):103-13. View abstract
  97. Permeation and block of TRPV1 channels by the cationic lidocaine derivative QX-314. J Neurophysiol. 2013 Apr; 109(7):1704-12. View abstract
  98. Phenotyping the function of TRPV1-expressing sensory neurons by targeted axonal silencing. J Neurosci. 2013 Jan 02; 33(1):315-26. View abstract
  99. Pain: morphine, metabolites, mambas, and mutations. Lancet Neurol. 2013 Jan; 12(1):18-20. View abstract
  100. Construction of a global pain systems network highlights phospholipid signaling as a regulator of heat nociception. PLoS Genet. 2012; 8(12):e1003071. View abstract
  101. Neurogenic inflammation and the peripheral nervous system in host defense and immunopathology. Nat Neurosci. 2012 Jul 26; 15(8):1063-7. View abstract
  102. Overexpression of human HSP27 protects sensory neurons from diabetes. Neurobiol Dis. 2012 Sep; 47(3):436-43. View abstract
  103. 5,6-EET is released upon neuronal activity and induces mechanical pain hypersensitivity via TRPA1 on central afferent terminals. J Neurosci. 2012 May 02; 32(18):6364-72. View abstract
  104. Understanding chronic inflammatory and neuropathic pain. Ann N Y Acad Sci. 2012 May; 1255:30-44. View abstract
  105. Genetically determined P2X7 receptor pore formation regulates variability in chronic pain sensitivity. Nat Med. 2012 Mar 25; 18(4):595-9. View abstract
  106. Deconstructing the neuropathic pain phenotype to reveal neural mechanisms. Neuron. 2012 Feb 23; 73(4):638-52. View abstract
  107. Inflammation-induced decrease in voluntary wheel running in mice: a nonreflexive test for evaluating inflammatory pain and analgesia. Pain. 2012 Apr; 153(4):876-884. View abstract
  108. Analgesia by inhibiting tetrahydrobiopterin synthesis. Curr Opin Pharmacol. 2012 Feb; 12(1):92-9. View abstract
  109. The BMP coreceptor RGMb promotes while the endogenous BMP antagonist noggin reduces neurite outgrowth and peripheral nerve regeneration by modulating BMP signaling. J Neurosci. 2011 Dec 14; 31(50):18391-400. View abstract
  110. Soluble epoxide hydrolase limits mechanical hyperalgesia during inflammation. Mol Pain. 2011 Oct 04; 7:78. View abstract
  111. Accelerating axonal growth promotes motor recovery after peripheral nerve injury in mice. J Clin Invest. 2011 Nov; 121(11):4332-47. View abstract
  112. Conversion of mouse and human fibroblasts into functional spinal motor neurons. Cell Stem Cell. 2011 Sep 02; 9(3):205-18. View abstract
  113. Targeting of sodium channel blockers into nociceptors to produce long-duration analgesia: a systematic study and review. Br J Pharmacol. 2011 Sep; 164(1):48-58. View abstract
  114. TrpA1 regulates thermal nociception in Drosophila. PLoS One. 2011; 6(8):e24343. View abstract
  115. Considerations for extrapolating evidence of acute and chronic pain analgesic efficacy. Pain. 2011 Aug; 152(8):1705-1708. View abstract
  116. A functionally characterized test set of human induced pluripotent stem cells. Nat Biotechnol. 2011 Mar; 29(3):279-86. View abstract
  117. A genome-wide Drosophila screen for heat nociception identifies a2d3 as an evolutionarily conserved pain gene. Cell. 2010 Nov 12; 143(4):628-38. View abstract
  118. TRPA1 contributes to cold hypersensitivity. J Neurosci. 2010 Nov 10; 30(45):15165-74. View abstract
  119. What is this thing called pain? J Clin Invest. 2010 Nov; 120(11):3742-4. View abstract
  120. Central sensitization: implications for the diagnosis and treatment of pain. Pain. 2011 Mar; 152(3 Suppl):S2-S15. View abstract
  121. Overcoming obstacles to developing new analgesics. Nat Med. 2010 Nov; 16(11):1241-7. View abstract
  122. Multiple chronic pain states are associated with a common amino acid-changing allele in KCNS1. Brain. 2010 Sep; 133(9):2519-27. View abstract
  123. Synaptic plasticity and central sensitization: author reply. J Pain. 2010 Aug; 11(8):801-3. View abstract
  124. Loss of inhibitory interneurons in the dorsal spinal cord and elevated itch in Bhlhb5 mutant mice. Neuron. 2010 Mar 25; 65(6):886-98. View abstract
  125. Selectively targeting pain in the trigeminal system. Pain. 2010 Jul; 150(1):29-40. View abstract
  126. Future directions in neuropathic pain therapy: closing the translational loop. Oncologist. 2010; 15 Suppl 2:24-9. View abstract
  127. T-cell infiltration and signaling in the adult dorsal spinal cord is a major contributor to neuropathic pain-like hypersensitivity. J Neurosci. 2009 Nov 18; 29(46):14415-22. View abstract
  128. Overexpression of the wild-type SPT1 subunit lowers desoxysphingolipid levels and rescues the phenotype of HSAN1. J Neurosci. 2009 Nov 18; 29(46):14646-51. View abstract
  129. Central sensitization: a generator of pain hypersensitivity by central neural plasticity. J Pain. 2009 Sep; 10(9):895-926. View abstract
  130. Coapplication of lidocaine and the permanently charged sodium channel blocker QX-314 produces a long-lasting nociceptive blockade in rodents. Anesthesiology. 2009 Jul; 111(1):127-37. View abstract
  131. Mu and delta opioid receptors diverge. Cell. 2009 Jun 12; 137(6):987-8. View abstract
  132. A novel tool for the assessment of pain: validation in low back pain. PLoS Med. 2009 Apr 07; 6(4):e1000047. View abstract
  133. Periganglionic inflammation elicits a distally radiating pain hypersensitivity by promoting COX-2 induction in the dorsal root ganglion. Pain. 2009 Mar; 142(1-2):59-67. View abstract
  134. COX2 in CNS neural cells mediates mechanical inflammatory pain hypersensitivity in mice. J Clin Invest. 2009 Feb; 119(2):287-94. View abstract
  135. Transient receptor potential channels: targeting pain at the source. Nat Rev Drug Discov. 2009 Jan; 8(1):55-68. View abstract
  136. Neuropathic pain: a maladaptive response of the nervous system to damage. Annu Rev Neurosci. 2009; 32:1-32. View abstract
  137. Nociceptors are interleukin-1beta sensors. J Neurosci. 2008 Dec 24; 28(52):14062-73. View abstract
  138. Capsaicin combined with local anesthetics preferentially prolongs sensory/nociceptive block in rat sciatic nerve. Anesthesiology. 2008 Nov; 109(5):872-8. View abstract
  139. GCH1 haplotype determines vascular and plasma biopterin availability in coronary artery disease effects on vascular superoxide production and endothelial function. J Am Coll Cardiol. 2008 Jul 08; 52(2):158-65. View abstract
  140. Novel analgesic development: from target to patient or patient to target? Curr Opin Investig Drugs. 2008 Jul; 9(7):694-5. View abstract
  141. Bradykinin enhances AMPA and NMDA receptor activity in spinal cord dorsal horn neurons by activating multiple kinases to produce pain hypersensitivity. J Neurosci. 2008 Apr 23; 28(17):4533-40. View abstract
  142. Reduced hyperalgesia in homozygous carriers of a GTP cyclohydrolase 1 haplotype. Eur J Pain. 2008 Nov; 12(8):1069-77. View abstract
  143. Ro5-4864 promotes neonatal motor neuron survival and nerve regeneration in adult rats. Eur J Neurosci. 2008 Feb; 27(4):937-46. View abstract
  144. Low-dose methotrexate reduces peripheral nerve injury-evoked spinal microglial activation and neuropathic pain behavior in rats. Pain. 2008 Aug 15; 138(1):130-142. View abstract
  145. The neuropathic pain triad: neurons, immune cells and glia. Nat Neurosci. 2007 Nov; 10(11):1361-8. View abstract
  146. Inhibition of nociceptors by TRPV1-mediated entry of impermeant sodium channel blockers. Nature. 2007 Oct 04; 449(7162):607-10. View abstract
  147. Complement induction in spinal cord microglia results in anaphylatoxin C5a-mediated pain hypersensitivity. J Neurosci. 2007 Aug 08; 27(32):8699-708. View abstract
  148. Nociceptors--noxious stimulus detectors. Neuron. 2007 Aug 02; 55(3):353-64. View abstract
  149. Delayed sympathetic dependence in the spared nerve injury (SNI) model of neuropathic pain. Mol Pain. 2007 Jul 31; 3:21. View abstract
  150. ATF3 increases the intrinsic growth state of DRG neurons to enhance peripheral nerve regeneration. J Neurosci. 2007 Jul 25; 27(30):7911-20. View abstract
  151. GDNF selectively promotes regeneration of injury-primed sensory neurons in the lesioned spinal cord. Mol Cell Neurosci. 2007 Oct; 36(2):185-94. View abstract
  152. BACE1 regulates voltage-gated sodium channels and neuronal activity. Nat Cell Biol. 2007 Jul; 9(7):755-64. View abstract
  153. Cannabinoids mediate analgesia largely via peripheral type 1 cannabinoid receptors in nociceptors. Nat Neurosci. 2007 Jul; 10(7):870-9. View abstract
  154. Central sensitization: uncovering the relation between pain and plasticity. Anesthesiology. 2007 Apr; 106(4):864-7. View abstract
  155. Reliable screening for a pain-protective haplotype in the GTP cyclohydrolase 1 gene (GCH1) through the use of 3 or fewer single nucleotide polymorphisms. Clin Chem. 2007 Jun; 53(6):1010-5. View abstract
  156. The voltage-gated sodium channel Na(v)1.9 is an effector of peripheral inflammatory pain hypersensitivity. J Neurosci. 2006 Dec 13; 26(50):12852-60. View abstract
  157. GTP cyclohydrolase and tetrahydrobiopterin regulate pain sensitivity and persistence. Nat Med. 2006 Nov; 12(11):1269-77. View abstract
  158. Prostaglandin E2 receptor EP4 contributes to inflammatory pain hypersensitivity. J Pharmacol Exp Ther. 2006 Dec; 319(3):1096-103. View abstract
  159. The transcription factor ATF-3 promotes neurite outgrowth. Mol Cell Neurosci. 2006 May-Jun; 32(1-2):143-54. View abstract
  160. Persistent postsurgical pain: risk factors and prevention. Lancet. 2006 May 13; 367(9522):1618-25. View abstract
  161. TRPA1 contributes to cold, mechanical, and chemical nociception but is not essential for hair-cell transduction. Neuron. 2006 Apr 20; 50(2):277-89. View abstract
  162. Bone morphogenetic protein signaling by hemojuvelin regulates hepcidin expression. Nat Genet. 2006 May; 38(5):531-9. View abstract
  163. Perceptual wind-up in the human oesophagus is enhanced by central sensitisation. Gut. 2006 Jul; 55(7):920-5. View abstract
  164. Runx1 determines nociceptive sensory neuron phenotype and is required for thermal and neuropathic pain. Neuron. 2006 Feb 02; 49(3):365-77. View abstract
  165. Bradykinin and peripheral sensitization. Biol Chem. 2006 Jan; 387(1):11-4. View abstract
  166. Detection of cold pain, cold allodynia and cold hyperalgesia in freely behaving rats. Mol Pain. 2005 Dec 14; 1:36. View abstract
  167. RNAi blocks DYT1 mutant torsinA inclusions in neurons. Neurosci Lett. 2006 Mar 13; 395(3):201-5. View abstract
  168. Upregulation of the voltage-gated sodium channel beta2 subunit in neuropathic pain models: characterization of expression in injured and non-injured primary sensory neurons. J Neurosci. 2005 Nov 23; 25(47):10970-80. View abstract
  169. Mutant SPTLC1 dominantly inhibits serine palmitoyltransferase activity in vivo and confers an age-dependent neuropathy. Hum Mol Genet. 2005 Nov 15; 14(22):3507-21. View abstract
  170. Role of the peripheral benzodiazepine receptor in sensory neuron regeneration. Mol Cell Neurosci. 2005 Oct; 30(2):228-37. View abstract
  171. Peripheral axonal injury results in reduced mu opioid receptor pre- and post-synaptic action in the spinal cord. Pain. 2005 Sep; 117(1-2):77-87. View abstract
  172. Bradykinin produces pain hypersensitivity by potentiating spinal cord glutamatergic synaptic transmission. J Neurosci. 2005 Aug 31; 25(35):7986-92. View abstract
  173. Constitutive cyclo-oxygenase-2 does not contribute to the development of human visceral pain hypersensitivity. Eur J Pain. 2006 Aug; 10(6):487-94. View abstract
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