Publications (last 3 years)

Books and chapters in edited volumes

Grace, P., Watkina, L.R. & Hutchinson, M.R., The role of the immune system in chronic pain comorbidities, Pain Comorbidities, Giamberardino, M.A. & Jensen, T.S. (Eds). IASP Press, (2011) in press.

Grace, P., Watkins, L.R. & Hutchinson, M.R., Immune to brain communication in pain: historical perspectives, new directions, Psychoneuroimmunology, Wiley-Blackwell, (2011) in press.

Wieseler-Frank, J., Milligan, E.D., Maier, S.F. & Watkins, L.R., Cord glial activation, Encyclopedic Reference of Pain, Schmidt, R. & Willis, W.D. (Ed.) Springer-Verlag, (2011) CD-Rom, invited update in preparation.

Hutchinson, M.R. & Watkins, L.R., Glial dysregulation of opioids, Encyclopedic Reference of Pain, Schmidt, R. & Willis, W.D. (Ed.) Springer-Verlag, (2011) CD-Rom, invited review in preparation.

Wieseler, J., Ellis, A., Maier, S.F. & Watkins, L.R., & Falci, S., Unilateral T13 and L1 Avulsion: methods for a novel model of central neuropathic pain. Pain Research: Methods and Protocols; "Methods of Molecular Medicine", 2nd Edition, D. Luo (Ed.) Humana Press, (2011) invited chapter in press.

Wieseler, J., Maier, S.F. & Watkins, L.R., An awake behaving rat model for the study of dural inflammation-induced facial allodyna: a rat model relevant to migraine. Pain Research: Methods and Protocols; "Methods of Molecular Medicine", 2nd Edition, D. Luo (Ed.) Humana Press, (2011) invited chapter in press.

Milligan, E.D., Maier, S.F., Watkins, L.R., Gene therapy in the central nervous system: chronic pain, Encyclopedia of Pain, 2009.

Maier, S. F., Amat, J., Baratta, M. V., Bland, S. T., Christianson, J. C., Thompson, B., Rozeske, R. R., & Watkins, L. R. The role of the medial prefrontal cortex in mediating resistance and vulnerability to the impact of adverse events. In C. M. Pariente, R. M. Nesse, D. Nutt, & L. Wolpert (Eds.), Understanding depression:a translational approach, Oxford University Press, 2009, 157-171.

Review Articles

Nicotra, L, Loram, L., Watkins, L.R. & Hutchinson, M.R., Toll like receptors in chronic pain, Experimental Neurology Special Issue on Microglia and Chronic Pain, (2011) in press.

Hutchinson, M.R., Shavit, Y., Grace, P.M., Rice, K.C., Maier, S.F. & Watkins, L.R., Exploring the neuroimmunopharmacology of opioids: an integrative review of mechanisms of central immune signaling and their implications for opioid analgesia, Pharmacological Reviews 63 (2011) 722-810.

Frank, M.G., Watkins, L.R. and Maier, S.F. Stress- and glucucorticoid-induced priming of neuroinflammatory responses: potential mechanisms of stress-induced vulnerability to drugs of abuse, Brain, Behavior & Immunity Special Issue, 25 Suppl. 1 (2011) S21-28.

Maier, S.F. & Watkins, L.R., Role of the medial prefrontal cortex in coping and resilience, Brain Research 1355 (2010) 52-60. PMCID: PMC2967290

Barrientos, R.M., Frank, M.G., Watkins, L.R. & Maier, S.F., Memory impairments in healthy aging: role of aging-induced microglial sensitization. Special Issue on Neuroimmunomodulation and Aging, Aging and Disease, (2010) 212-231. PMCID: PMC2995216

Buchanan, M., Hutchinson, M.R., Watkins, L.R. & Yin, H., The role of toll-like receptor 4 in pathologies of the CNS, Journal of Neurochemistry 114 (2010) 13-27.

Watkins, L.R., Hutchinson, M.R., Rice, K., & Maier, S.F., The "toll" of opioid-induced glial activation: improving the clinical efficacy of opioids by targeting glia, Trends in Pharmacological Sciences, 30 (2009) 581-591. PMCID: PMC2783351

Sloane, E., Soderquist, R., Maier, S.F., Mahoney, M., Chavez, R., Watkins, L.R. & Milligan, E.D., Long term control of neuropathic pain in a non-viral gene therapy paradigm, Gene Therapy special issue 16 (2009) 470-5. PMCID: PMC2756299

Milligan, E.D. and Watkins, L.R., Pathological and protective roles of glia in chronic pain, Nature Neuroscience Reviews, 10 (2009) 23-36. PMCID: PMC2752436

Journal Articles

Frank, M.G., Thompson, B.M., Watkins, L.R. & Maier, S.F., Glucocorticoids mediate stress-induced priming of microglial pro-inflammatory responses, Brain, Behavior & Immunity, (2011) in press.

Rozeske, R.R., Der-Avakian, A., Watkins, L.R. & Maier, S.F. , Activation of the medial prefrontal cortex by escapable stress is ncesary for protection against subsequent inescapable stress-induced potentiation of morphine conditioned place preference, Eur. J. Neuroscience (2011) in press.

Johnston, I.N., Maier, S.F., Rudy, J.W. and Watkins, L.R., Post-conditioing experience with acute or chronic inflammatory pain reduces contextual fear conditioning in the rat, Behavioral Brain Research, 226 (2011) 361-618.

Rozeske, R.R., Evans, A.K., Frank, M.G., Watkins, L.R., Lowry, C.A. & Maier, S.F., Uncontrollable, but not controllable, stress desensitizes 5-HT1A receptors in the dorsal raphe nucleus, Journal of Neuroscience, 31 (2011) 14107-15.

Hains, L.E., Loram, L.C., Taylor, F., Strand, K., Wieseler, J.L., Barrientos, R., Young, J.C., Frank, M.G., Sobesky, J., Martin, T.J., Eisenach, J.C., Maier, S.F., Johnson, J.D., Fleshner, M.R., & Watkins, L.R., Prior laparotomy or corticosterone potentiates lipopolysaccharide-induced fever and sickness behaviors, Journal of Neuroimmunology, 239 (2011) 53-60.

Barrientos, R., Frank, M., Crysdale, N., Chapman, T., Ahrendsen, J., Day, H., Campeau, S., Watkins, L.R., Patterson, S. and Maier, S.F., Little exercise, big effects: reversing aging and infection-induced memory deficits and underlying processes, Journal of Neuroscience, 31(2011) 11578-11586.

Liu, L., Ghosh, N., Slivka, P.F., Fiorini, Z., Hutchinson, M.R., Watkins, L.R., & Yin, H., An MD2 hot-spot mimicking peptide that suppresses TLR4-mediated inflammatory response in vitro and in vivo, Chemibiochem, 12 (2011) 1827-31.

Wu, Y., Lousberg, E.L., Moldenhauer, L.M., Hayball, J.D., Robertson, S.A., Coller, J.K., Rice, K.C., Watkins, L.R., Somogyi, A.A. & Hutchinson, M.R., Inhibiting the TLR4-MyD88 signalling cascade by genetic or pharmacologic strategies reduces acute alcohol dose-induced sedation and motor impairment in mice, Brit. J. Pharmacol. (2011) in press.

Loram, L.C., Taylor, F.R., Strand, K.A., Frank, M.S. Sholar, P., Harrison, J.A., Maier, S.F. & Watkins, L.R., Prior exposure to glucocorticoids potentiates lipopolysaccharide induced mechanical allodynia and spinal neuroinflammation, Brain, Behavior & Immunity, 25 (2011) 1408-15.

Christianson, J., Jenings, J.H., Ragole, T., Flyer, J., Benison, A., Barth, D. Watkins, L.R. & Maier, S.F., Safety signals mitigate the consequences of uncontrollable stress via a circuit involving the sensory insular cortex and bed nucleus of the stria terminalis, Biological Psychiatry 70 (2011) 458-64.

Liu, L., Coller, J.K., Watkins, L.R., Somogyi, A.A. & Hutchinson, M.R., The association of naloxone-precipitated morphine withdrawal jumping with brain IL-1beta expression: comparison of different mouse strains, Brain, Behavior & Immunity, 25 (2011) 1223-1232.

Barrientos, R.M., Frank, M.G., Crysdale, N.Y., Chapman, T.R., Ahrendsen, J., Day, H.E.W., Campeau, S., Watkins, L.R. & Maier, S.F., Little exercise, big effects: reversing aging and infection-induced memory deficits, and underlying processes, Journal of Neuroscience, 31 (2011) 11578-86.

Rozeske, R.R., Greenwood, B.N., Fleshner, M., Watkins, L.R., Maier, S.F., Voluntary whell running produces resistance to inescapable stress-induced potentiation of morphine conditioned place reference, Behavioral Brain Research, 219 (2011) 378-81.

Benison, A.M., Chumachenko, S., Northcutt, A., Harrison, J.A., Falci, S.P., Maier, S.F., Watkins, L.R. & Barth, D.S., Caudal granular insular cortex is sufficient and necessary for the long-term maintenance of allodynic behavior in the rat due to mononeuropathy, Journal of Neuroscience 31 (2011) 6317-28.

Wu, Y., Lousberg, E., Moldenhauer, L.M., Hayball, J.D., Robertson, S.A., Coller, J.K., Watkins, L.R., Somogyi A.A. & Hutchinson, M.R., Attenuating microglial and IL-1 signaling protects mice from acute alcohol-induced sedation and/or motor impairment, Brain, Behavior & Immunity Special Issue, 25 Suppl. 1 (2011) S155-64.

Muscoli, C., Doyle, T., Dagostino, C., Bryant, L., Chen, Z., Watkins, L. Ryerse, J., Bieberich, E., Neuman, W., Salvemini, D., Counter-regulation of opioid analgesia by glial-derived bioactive sphingolipids, Journal of Neuroscience, 30 (2010) 15400-15408. PMCID: PMC3000610

Thompson, B. M., Baratta, M. V., Biedenkapp, J. C., Rudy, J. W., Watkins, L. R., & Maier, S. F. Activation of the infralimbic cortex in a fear context enhances extinction learning, Learning And Memory, 17 (2010) 591-599. PMCID: PMC2981413

Frank, M.G., Miguel, Z.D., Watkins, L.R., & Maier, S.F., Prior exposure to glucocorticoids sensitizes the neuroinflammatory and peripheral inflammatory responses to E. coli lipopolysaccharide, Brain, Behavior & Immunity, 24 (2010) 19-30.

Frank, M.G., Barrientos, R.M., Watkins, L.R. & Maier, S.F., Aging sensitizes rapidly isolated hippocampal microglia to LPS ex vivo, J. Neuroimmunol. 226 (2010) 181-184.

Ramos, K.M., Lewis, M.T., Morgan, K.N., Crysdale, N.Y., Kroll, J.L., Taylor, F.R., Harrison, J.A., Sloane, E.M., Maier, S.F., & Watkins, L.R., Spinal Upregulation of Glutamate Transporter GLT-1 by Ceftriaxone: Therapeutic Efficacy in a Range of Experimental Nervous System Disorders, Neuroscience 169 (2010) 1888-1900. PMCID: PMC2918694

Bevan, D.E., Martinko, A.J., Loram, L.C., Stahl, J.A., Taylor, F.R., Joshee, S., Watkins, L.R., Yin, H., Selection, preparation, and evaluation of small-molecule inhibitors of toll-like receptor 4, ACS Med. Chem. Letters, 1 (2010) 194-198. PMCID: PMC2930797

Bland, S.T., Beckley, J.T., Young, S., Tsang, V., Watkins, L.R., Maier, S.F. & Bilbo, S.D., Enduring consequences of early-life infection on glial and neural genesis within cognitive regions of the brain, Brain, Behavior & Immunity, 24 (2010) 329-338. PMCID: PMC2826544

Bland, S.T., Beckley, J.T., Watkins, L.R., Bilbo, S.D. & Maier, S.F., Neonatal E. coli infection alters glial, cytokine, and neuronal gene expression in response to acute amphetamine in adolescent rats, Neuroscience Letters, 474 (2010) 52-57. PMCID: PMC2865898

Wieseler, J., Ellis, A.L., McFadden, A., Brown, K., Starnes, C., Maier, S.F., Watkins, L.R. & Falci, S., Below level central pain induced by discrete dorsal spinal cord injury, Journal of Neurotrauma 27 (2010) 1697-707.

Amat, J., Aleksejev, R., Watkins, L.R. & Maier, S.F., Behavioral control over shock blocks behavioral and neurochemical effects of later social defeat, Neuroscience, 165 (2010) 1013-1038. PMCID: PMC2847505

Hutchinson, M.R., Lewis, S.S., Coats, B.D., Rezvani, N., Xhang, Y., Wieseler, J.L., Somogyi, A.A., Yin, H., Maier, S.F., Rice, K.C. & Watkin, L.R., Possible involvement of toll-like receptor 4/myeloid differentiation factor-2 activity of opioid inactive isomers causes spinal proinflammation and related behavioral consequences, Neuroscience 167 (2010) 880-93. PMCID: PMC2854318

Hains, L.E., Loram, L.C., Wieseler, J.L., Frank, M.G., Bloss, E.B., Sholar, P., Taylor, F.R., Harrison, J.C., Martin, T.J., Esenach, J.C. Maier, S.F. & Watkins, L.R., Pain intensity and duration can be enhanced by prior challenge: initial evidence suggestive of a role of microglial priming, Journal of Pain, 11 (2010) 1004-1014. PMCID: PMC2916950

Loram, L.C., Harrison, J.A., Chao, L., Taylor, F.R., Reddy, A., Travis, C., Giffard, R., Al-Abed, Y., Tracey, K., Maier, S.F. & Watkins, L.R., Intrathecal injection of an alpha 7 nicotinic acetylcholine receptor agonist attenuates gp120-induced mechanical allodynia and spinal pro-inflammatory cytokine release in rats, Brain Behavior & Immunity 24 (2010) 959-967. PMCID: PMC2902784

Christianson, J.P., Ragole, T., Amat, J., Greenwood, B.N., Strong, P.V., Paul, E.D., Fleshner, M., Watkins, L.R. & Maier, S.F., 5-hydroxytrapamine 2C receptors in the basolateral amgycala are involved in the expression of anxiety after uncontrollable traumatic stress, Biological Psychiatry, 67 (2010) 339-345.

Soderquist, R.G., Sloane, E.M., Loram, L.C., Harrison, J.A., Dengler, E.C., Johnson, S.M., Amer, L.D., Young, C.S., Lewis, M.T., Poole, S., Watkins, L.R., Milligan, E.D., and Mahoney, M.J., Release of plasmid DNA encoding IL-10 from PLGA microparticles facilitates long-term reversal of neuropathic pain following a single intrathecal administration, Pharm. Research 27 (2010) 841-54.

Hutchinson, M.R., Loram, L.C., Zhang, Y., Shridhar, M., Rezvani, N., Berkelhammer, D., Phipps, S., Foster, P.S., Landgraf, K., Falke, J.J., Rice, K.C., Maier, S.F., Yin, H., Watkins, L.R., Evidence that tricyclic small molecules possess toll-like receptor-4 (TLR4)/MD-2 activity, Neuroscience, 168 (2010) 551-563. PMC2872682

Frank, M., Barrientos, R., Hein, A., Biedenkapp, J., Watkins, L.R. & Maier, S.F., IL-1RA blocks E. coli-induced suppression of Arc and long-term memory in aged F344xBN rats, Brain, Behavior & Immunity, 24 (2010) 254-62. PMCID: PMC2818379

Bilbo, S., Wieseler, J., Barrientos, R., Tsang, V., Watkins, L.R. & Maier, S.F., Neonatal bacterial infection alters fever to live and simulated infections in adulthood, Psychoneuroendocrinology 474 (2010) 52-57. PMCID in progress

Joce, C., Stahl, J.A., Shridhar, M., Hutchinson, M.R. Watkins, L.R., Fedichev, P.O. & Yin, H., Application of a novel in silico high-throughput screen to identify selective inhibitors for protein-protein interactions, Bioorganic & Medicinal Chemistry Letters, 20 (2010) 5411-5413. PMCID: PMC2930491

Wieseler, J., Ellis, A., Sprunger, D., Brown, K., McFadden, A., Mahoney, J., Rezvani, N., Maier, S.F., & Watkins, L.R., A novel method for modeling facial allodynia associated with migraine in awake and freely moving rats, Journal of Neuroscience Methods, 185 (2010) 236-245. PMCID: PMC281493

Loram, L., Harrison, J., Sloane, E., Hutchinson, M., Sholar, P., Taylor, R., Berkelhammer, D., Coats, B., Poole, S., Milligan, E., Maier, S., Rieger, J., & Watkins, L.R., Enduring reversal of neuropathic pain by a single intrathecal injection of adenosine 2A receptor agonists: a novel therapy for neuropathic pain, Journal of Neuroscience, 29 (2009) 14015-25. PMCID: PMC2799253

Sloane, E., Langer, S., Jekich, B., Mahoney, J., Hughes, T., Seibert, W., Huberty, G., Coats, B., Harrison, J., Klinman, D., Poole, S., Maier, S., Johnson, K.W., Chavez, R., Watkins, L.R., Leinwand, L., Milligan, E.D., Immunological priming potentiates non-viral anti-inflammatory gene therapy treatment of neuropathic pain, Gene Therapy, 16 (2009) 1210-22. PMCID: PMC2762489

Barrientos, R.M., Watkins, L.R., Rudy, J.W. & Maier, S.F., Characterization of the sickness response in young and aging rats following E. coli infection, Brain, Behavior & Immunity, 23 (2009) 3450-4. PMCID: PMC2783183

Hutchinson, M.R., Ramos, K., Loram, L., Wieseler, J., Lewis, M., Crysdale, N., Sholar, P.W., Kearney, J.J., Zhang, Y., Harrison, J., Maier, S.F., Rice, K.C. & Watkins, L.R., Evidence for a role of heat shock protein-90 (HSP90) in TLR4 mediated pain enhancement, Neuroscience. 164 (2009) 1821-1832. PMCID: PMC2783248

Baratta, M.V., Zarza, C.M., Gomez, D.M., Campeau, S., Watkins, L.R. & Maier, S.F., Selective activation of dorsal raphe nucleus-projecting neurons in the ventral medial prefrontal cortex by controllable stress, European Journal of Neuroscience 30 (2009) 1111-6. PMCID: PMC2757732

Hutchinson, M.R., Zhang, Y., Shridhar, M., Evans, J., Slivka, P.F., Buchanan, M.M., Zhao, T.X., Rezvani, N., Wieseler, J., Hughes, T.S., Falke, J.J., Leinwand, L.A., Maier, S.F., Yin, H., Rice, K.C. & Watkins, L.R., Evidence that opioids may have toll like receptor 4 and MD-2 effects, Brain, Behavior & Immunity 24 (2009) 83-95. PMCID: PMC2788078

Rodgers, K.M., Hutchinson, M.R., Northcutt, A., Maier, S.F., Watkins, L.R. & Barth, D.S., The innate immune response of cortical glial cells increases neuronal excitability leading to seizures, Brain, 132 (2009) 2478-86. PMCID: PMC2732268

Soderquist, R.G., Milligan, E.D., Sloane, E.M., Harrison, J.A., Douvas, K.K., Potter, J.M., Hughes, T.S., Watkins, L.R. & Mahoney, M.J., PEGylation of brain-derived neurotrophic factor for preserved biological activity and enhanced intrathecal delivery, Journal of Biomedical Materials Research, 91 (2009) 719-29. PMCID in progress

Soderquist, R.G., Miligan, E.D., Harrison, J.A., Chavez, R.A., Johnson, K.W., Watkins, L.R. & Mahoney, M.J. PEGylation of interleukin-10 for the mitigation of enhanced pain states, Journal of Biomedical Materials Research, 93 (2010) 1169-79.

Lewis, S.S., Hutchinson, M.R., Rezvani, N., Zhang, Y., Maier, S.F., Rice, K.C., Watkins, L.R., Morphine-3-glucuronide cuases enhance pain through pro-inflammatory glial mechanisms, Neuroscience 165(2010) 569-583 PMCID: PMC2795035

Rozeske, R.R., Der-Avakian, A., Bland, S.T., Beckley, J.T., Watkins, L.R. & Maier, S.F., The medial prefrontal cortex regulates the differential expression of morphine conditioned place preference following a single exposure to controllable or uncontrollable stress Neuropsychopharmacology 34 (2009) 834-43

Slivka, P.F., Shridhar, M., Lee, Gui-in, Sammond, D.W., Hutchinson, M.R., Martinko, A.J., Buchanan, M.M., Sholar, P.W., Kearney, J.J., Harrison, J.A., Watkins, L.R. & Ying, H., A peptide antagonist of the TLR4/MD2 interaction, ChemBioChem, 10 (2009) 645-649. PMCID: PMC2982775

Bland, S.T., Hutchinson, M.R., Maier, S.F., Watkins, L.R. & Johnson, K.W., The glial activation inhibitor AV411 reduces morphine-induced nucleus accumbens dopamine release, Brain, Behavior & Immunity 23 (2009) 492-497. PMCID: PMC2783267

Hughes, T.S., Langer, S.J., Virtanen, S., Chavez, R.A., Watkins, L.R., Milligan, E.D. & Leinwand, L.A., Immunogenicity of intrathecal plasmid gene delivery: cytokine release and effects on transgene expression, Journal of Gene Medicine, 11 (2009) 782-790. PMCID in progress

Hughes, T.S., Langer, S.J., Johnson, K.W., Chavez, R., Milligan, E.D., Watkins, L.R.,& Leinwand, L.A., Intrathecal injection of naked plasmid DNA provides long-term expression of secreted proteins, Molecular Therapy 17 (2009) 88-94. PMCID: PMC2834984

Christianson, J. P., Thompson, B., Watkins, L. R., & Maier, S. F., Medial prefrontal cortical activation modulates the impact of controllable and uncontrollable stressor exposure on a social exploration test of anxiety, Stress, 12 (2009) 445-450. PMCID: PMC2787917