skip to content

Department of Pharmacology

 

 

Pre-print

Pattison, L.A., Cloake, A., Chakrabarti, S., Hilton, H., Rickman, R.H., Higham, J.P., Meng, M.Y., Paine, L.W., Qiu, L., Ritoux, A., Bulmer, D.C. and Smith, E.S. Digging deeper into pain – an ethological behavior assay correlating well-being in mice with human pain experience. bioRxiv, doi 10.1101/2023.08.18.553862

Gupta, R.A, Higham, J.P., Urriola-Muñoz, P., Barker, K.H., Paine, L., Ghooraroo, J., Hockley, J.R.F., Rahman, T., Smith, E.S., Brown, A.J.H., Suzuki, R. and Bulmer, D.C. GPR35 inhibits TRPA1-mediated colonic afferent hypersensitivity through suppression of Substance P release. bioRxiv, doi 10.1101/2023.09.12.557415

Sanchez, J.P., Middleton, S.J., Pattison, L.A., Hilton, H., Awadeelkareem, M.A., Zuberi, S.R, Renke, M.B., Hu, H., Yang, X., Clarke, A.J., Smith, E.S. and Bennett, D.L. Inhibition of sensory neuron driven acute, inflammatory and neuropathic pain using a humanised chemogenetic system. bioRxiv, doi

2023

Bohic, M., Pattison, L.A., Jhumka, Z.A., Rossi, H., Thackray, J.K., Ricci, M., Mossazghi, N., Foster, W., Ogundare, S., Twomey, C.R., Hilton, H., Arnold, J., Tischfield, M.A., Yttri, E.A., Smith, E.S., Abdus-Saboor, I. and Abraira, V.E.(2023) Mapping the neuroethological signatures of pain, analgesia, and recovery in mice. Neuron, 111, 2811-2830.

Ai, M., Hotham, W.E., Pattison, L.A., Ma, Q., Henson, F.M.D and Smith, E.S. (2023) Human mesenchymal stem cells and derived extracellular vesicles reduce sensory neuron hyperexcitability and pain-related behaviors in a mouse model of osteoarthritis. ­Arth Rheum, 75, 352-363

Smith, E.S. (2023) A new art to treating osteoarthritis pain? Osteo Cart, 31, 1275-77

Barker, K.H., Higham, J.P., Pattison, L.A., Chessell, I.P., Welsh, F., Smith, E.S., and Bulmer, D.C. (2023) Sensitisation of colonic nociceptors by IL-13 is dependent on JAK and p38 MAPK activity. Am J Physiol Gastrointest Liver Physiol, 324, 250-261

Parey, E., Frost, S., Uribarren, A., Park, T.J., Zoettl, M., Smith, E.S., Berthelot, C. and Villar, D. Phylogenetic modeling of enhancer shifts in African mole-rats reveals regulatory changes associated with tissue-specific traits. Genome Biol in press, doi 10.1101/gr.277715.123

Urriola-Muñoz, P., Pattison, L.A., and Smith, E.S. (2023) Dysregulation of ADAM10 shedding activity as a mechanism of cancer resistance in the naked mole-rat. J Cell Physiol, 238, 761-775

Walters, E.T., Crook, R.J., Neely, G.G., Price, T. J. and Smith, E.S. (2023) Persistent nociceptor hyperactivity as a painful evolutionary adaptation. TiNS, 46, 211-27

2022

Goyens, J., Baeckens, S., Smith, E.S., Pozzi, J., and Mason, M.J. (2022) Parallel evolution of semicircular canal form and sensitivity in subterranean mammals. J Comp Physiol A, 208, 627-40

Fatima, I., Chen, G., Botchkareva, N.V., Sharov, A.A., Thornton, D., Wilkinson, H.N., Hardman, M.J., Grutzkau, A., de Magalhaes, J.P., Seluanov, A., Smith, E.S., Gorbunova, V., Mardaryev, A.N., Faulkes, C.G., and Botchkarev, V.A. (2022) Skin aging in long-lived naked mole-rats is accompanied by increased expression of longevity-associated and tumor suppressor genes. J Inv Derm, 142, 2853-63

Cagan, A., Baez-Ortega, A., Brzozowska, N., Abascal, F., Coorens, T.H., Sanders, M.A., Lawson, A.R., Harvey, L.M., Bhosle, S.G., Jones, D., Alcantara, R.E., Butler, T.M., Hooks, Y., Roberts, K., Anderson, E., Flach, E., Spiro, S., Januszczak, I., Wrigglesworth, E., Perkins, M.W., Deaville, R., Druce, M., Bogeska, R., Milsom, M.D., Neumann, B., Gorman, F., Constantino-Casas, F., Peachey, L., Bochynska, D., Smith, E.S., Gerstung, M., Campbell, P.J., Murchison, E.P., Stratton, M.R., and Martincorena, I. (2022) Somatic mutation rates scale with lifespan across mammals. ­Nature, 604, 517-24

Miessner, H., Siedel, J. and Smith, E.S. (2022) In vitro models for investigating itch. Front Mol Neurosci, 15, 084126

Barker, K.H., Higham, J.P., Pattison, L.A., Taylor, T.S., Chessell, I.P., Welsh, F., Smith, E.S., and Bulmer, D.C. Sensitisation of colonic nociceptors by TNF is dependent on TNFR1 expression and p38 MAPK activity. ­J Physiol, 600, 3819-3836

Buffenstein, R., Amoroso, V., Andziak, B., Avdieiev, S., Azpurua, J., Barker, A.J....Smith, E.S.. (2022). The naked truth: a comprehensive clarification and classification of current ‘myths’ in naked mole-rat biology. Biol Rev, 97, 115-140

Gomes, D.M., Loth, A., Hockley, J.R.F. and Smith, E.S. Gut Reaction: The Impact of a Film on Public Understanding of Gastrointestinal Conditions. Front Comms, 7, 769052

Latragna,A., Sabaté, A., Tsimpos, P., Vermeiren, S., Gualdani, R., Chakrabarti, S., Callejo, G., Shomroni, O., Sitte, M., Kricha, S., Luypaert, M., Vanhollebeke, B., Laumet, G., Salinas-Riester, G., Smith, E. S., Ris, L. and Bellefroid, E.J. (2022) Prdm12 modulates pain-related behavior by remodeling gene expression in mature nociceptors. PAIN, in press doi 10.1097/j.pain.0000000000002536

2021

Chakrabarti, S., Ai, M., Wongn, W.Y.K., Newell, K., Henson, F.M.D. and Smith, E.S. (2021) Functional characterization of ovine dorsal root ganglion neurons reveals peripheral sensitization after osteochondral defect. eNeuro, 8, ENEURO.0237-21.2021

Tan, S.L., Barri, M., Atakpa-Adaji, P., Taylor, C.W., Smith, E.S., Murrell-Lagnado, R.D. (2021). P2X4 receptors mediate Ca2+ release from lysosomes in response to stimulation of P2X7 and H1 histamine receptors. Int J Mol Sci, 22, 10492

Smith, E.S., Park, T.J., Holmes, M.M. and Buffenstein, R. (2021). Some Exciting Future Directions for Work on Naked Mole-Rats. Adv Exp Med Biol, 1319, 409-420.   

Hadi, F., Smith, E.S., and Khaled, W.T. (2021). Naked Mole-Rats: Resistant to Developing Cancer or Good at Avoiding It? Adv Exp Med Biol, 1319, 341-352.

Park, T.J., Smith, E.S.., Reznick, J., Bennett, N.C., Applegate, D.T., Larson, J., Lewin, G.R. (2021). African Naked Mole-Rats Demonstrate Extreme Tolerance to Hypoxia and Hypercapnia. Adv Exp Med Biol, 1319, 255-269.

Lewin, G.R., Smith, E.S., Reznick, J., Debus, K., Barker, A.J. and Park, T.J. (2021). The Somatosensory World of the African Naked Mole-Rat. Adv Exp Med Biol, 1319, 197-220.

Vice, E.N., Lagestee, S., Browe, B.M., Deb, D., Smith, E.S. and Park, T.J. (2021). Sensory Systems of the African Naked Mole-Rat. Adv Exp Med Biol, 1319, 137-156.

Pattison, L.A., Krock, E., Svensson, C.I. and Smith, E.S. (2021). Cell-cell interactions in joint pain: rheumatoid arthritis and osteoarthritis. Pain15, 714-717.

Dulai, J.S., Smith, E.S. and Rahman, T.R. (2021). Acid-sensing ion channel 3: Analgesic target. Channels15, 94-127.

2020

Lee, M., Nahorski, M., Hockley, J.R.F., Lu, V., Ison, G., Pattison, L.A., Callejo, G., Stouffer, K., Fletcher, E., Brown, C., Drissi, I., Wheeler, D., Ernfors, P.,  Menon, D., Reimann, F., Smith, E.S., Woods, C.G. Human labour pain is influenced by the voltage-gated potassium channel KV6.4 subunit. Cell Reports, 32, 107941

Hadi, F., Kulaberoglu, Y., Lazarus, K., Bach, K., Ugur, R., Beattie, P., Smith, E.S. and Khaled, W.T. (2020). Transformation of naked mole-rat cells. Nature, 583, E1-E13  

Chakrabarti, S., Pattison, L.A., Doleschall, B., Rickman, R.H., Blake, H., Callejo, G., Heppenstall, P.A. & Smith, E.S. Intra-articular AAV-PHP.S mediated chemogenetic targeting of knee-innervating dorsal root ganglion neurons alleviates inflammatory pain in mice. Arth Rheum, 72, 1749-58

Chakrabarti, S., Hore, Z., Pattison, L.A., Lalnunhlimi, S., Bhebhe, C.N., Callejo, G., Bulmer, D.C., Taams, L.S., Denk, F. & Smith, E.S. Sensitization of knee-innervating sensory neurons by tumor necrosis factor-α activated fibroblast-like synoviocytes: an in vitro, co-culture model of inflammatory pain. Pain, 161, 2129-2141

Browe, B.M., Olsen, A.R., Ramirez, C., Rickman, R.H., Smith, E.S. and Park, T.J. The naked mole-rat has a functional purinergic pain pathway despite having a non-functional peptidergic pain pathway. Neurobiol Pain, 8, 100051

Du, Z., Chakrabarti, S., Kulaberoglu, Y., Smith, E.S., Dobson, C.M., Itzhaki, L. and Kumita, J. (2020). Probing the unfolded protein response in long-lived naked mole-rats. Biochem Biophys Res Comm, 529, 1151-1157

Hacker, L., Brunker, J., Smith, E.S., Gozales, I.Q. and Bohndiek, S.E. (2020). Photoacoustics resolves species-specific differences in haemoglobin concentration and oxygenation. J Biomed Opt,

Smith, E.S. and Park, T.J. (2020). Neurobiology: Crowdsourcing CO2 to conserve brain energy. Curr Biol30, R649-651

Smith, E.S., Park, T.J. and Lewin, G.R. (2020) Independent evolution of pain insensitivity in African mole-rats: origins and mechanisms. J Comp Physiol A, 206, 313-325

Callejo, G., Pattison, L.A., Greenhalgh, J.C., Chakrabarti, S., Andreopoulou, E., Hockley, J.R.F., Smith, E.S. and Rahman, T. (2020) In silico screening of GMQ-like compounds reveals guanabenz and sephin1 as new allosteric modulators of acid-sensing ion channel 3. Biochem Pharmacol, 174, 113834

Chakrabarti, S., Jadon, D.R., Bulmer D.C. and Smith, E.S. (2020) Human osteoarthritic synovial fluid increases excitability of mouse dorsal root ganglion sensory neurons: an in-vitro translational model to study arthritic pain. Rheumatology, 59, 662-667

Hockley, J.R.F., Taylor, T.S., Callejo, G., Husson, Z.M. and Smith, E.S. (2020) Acid and inflammatory sensitisation of naked mole-rat colonic afferent nerves. Mol Pain, 16, 1-11

Taylor, T.S., Konda, P, John, S.S., Bulmer, D.C., Hockley, J.R.F & Smith, E.S. (2020) Galanin suppresses visceral afferent responses to noxious mechanical and inflammatory stimuli. Phys Rep, 8, e14326

2019

Pattison, L.A., Callejo, G. and Smith, E.S. (2019). Evolution of acid nociception: ion channels and receptors for detecting acid. Phil Trans R Soc B, 374, 20190291

Kulaberoglu, Y., Bhushan, B., Hadi, F., Chakrabarti, S., Khaled, W.T., Rankin, K., Smith, E.S. and Frankel, D. (2019) The material properties of naked mole-rat hyaluronan. Sci Reports, 9, 6632 ( co-corresponding authors)

Hockley, J.R.F., Taylor, T.S., Callejo, G., Wilbrey, A.L., Gutterridge, A., Bach, K., Winchester, W.J., Bulmer, D.C., McMurray, G. and Smith, E.S. (2019) Single-cell RNAseq reveals seven classes of colonic sensory neuron. Gut, 68, 633-644

2018

Bautzova, T., Hockley, J.R., Perez-Berezo, T., Pujo, J., Tranter, M.M., Desormeaux, C., Barbaro, M.R., Basso, L. Le Faouder, P-. Rolland, C., Malapert, P., Moqrich, A., Eutamene, H., Denadi-Souza, A., Vergnolle, N., Smith, E.S., Hughes, D.I., Barabara, G., Dietrich, G., Bulmer, D.C. and Cenac, N. (2018) 5-oxoETE triggers nociception in constipation predominant irritable bowel syndrome through MAS-related G protein coupled receptor D. Sci Sig, 11, eaal2171

Chakrabarti, S., Pattison, L.A., Singhal, K., Hockley, J.R.F., Callejo, G.and Smith, E.S. (2018) Acute inflammation sensitizes knee-innervating sensory neurons and decreases mouse digging behavior in a TRPV1-dependent manner. Neuropharm143, 49-62

Hockley, J.R.F., Smith, E.S. and Bulmer, D.C. (2018) Human visceral nociception: findings from translational studies in human tissue. Am J Physiol Gastro Liv Physiol, 315, G464-G472

Husson, Z. and Smith, E. S. (2018) Naked mole-rat cortical neurons are resistant to acid-induced cell death. Mol Brain, 11, 26

Wright, A. J., Husson, Z. M. A., Hu, D. E., Callejo, G., Brindle, K. M. and Smith, E. S. (2018) Increased hyperpolarized [1-13C]lactate production in a model of joint inflammation is not accompanied by tissue acidosis as assessed using hyperpolarized 13C-labeled bicarbonate. NMR Biomed e3892

Schuhmacher, L. N., Callejo, G., Srivats, S. and Smith, E. S. (2018) Naked mole-rat acid-sensing ion channel 3 forms nonfunctional homomers, but functional heteromers.  J Biol Chem, 293, 1756-1766.     

Smith, E.S. (2018). Advances in understanding nociception and neuropathic pain. J Neurol, 265, 231-238.

 

2017

Prato, V., Taberner, F.J., Hockley, J.R.F., Callejo, G., Arcourt, A., Tazir, B., Hammer, L., Schad, P., Heppenstall, P.A., Smith, E.S. and Lechner, S.G. (2017). Functional and molecular characterization of mechanoinsensitive "silent" nociceptors. Cell Reports, 21, 3012.

Kulaberoglu, Y., Lin, K., Holder, M., Gai, Z., Gomez, M., Assefa Shifa, B., Mavis, M., Hoa, L., Sharif, A.A.D., Lujan, C., Smith, E.S., Bjedov, I., Tapon, N., Wu, G. and Hergovich, A. (2017). Stable MOB1 interaction with Hippo/MST is not essential for development and tissue growth control. Nature Com., 8, 695.

Park, T. J., Reznick, J., Peterson, B. L., Blass, G., Omerbasic, D., Bennett, N.C. Kuich, P.H.J.L, Zasada, C., Browe, B.M., Hamann, W., Applegate, D.T., Radke, M.H., Kosten, T., Lutermann, H., Gavaghan, V., Eigenbrod, O., Bégay, V., Amoroso, V.G., Govind, V., Minshall, R.D., Smith, E.S., Larson, J., Gotthardt, M., Kempa, S. and Lewin, G.R. (2017) Fructose-driven glycolysis supports anoxia resistance in the naked mole-ratScience356, 307-311.

Wetzel, C., Pifferi, S., Picci, P., Gök, C., Hoffmann, D., Bali, K.K., Lampe, A., Lapatsina, L., Fleischer, R., Smith, E. S., Bégy, V., Moroni, M., Estebanez, L., Kühnemund, J., Walcher, J., Specker, E., Neuenschwander, M., von Kreis, J.P., Haucke, V., Kuner, R., Poulet, J.F.A., Schmoranzer, J., Poole, K. and Lewin, G.R. (2017). Small molecule inhibition of STOML3 oligomerization reverses pathological mechanical hypersensitivity. Nature Neurosci, 20, 209-218

Peiris, M., Hockley, J. R., Reed, D. E., Smith, E. S., Bulmer, D. C., Blackshaw, L. A. (2017). Peripheral KV7 channels regulate visceral sensory function in mouse and human colon. Mol Pain 13, 1744806917709371

2016

Schuhmacher, L. N. and Smith, E. S. (2016). Expression of acid-sensing ion channels and selection of reference genes in mouse and naked mole rat. Mol Brain997.

Mason, M. J., Cornwall, H. L. and Smith, E. S. (2016). Ear Structures of the Naked Mole-Rat, Heterocephalus glaber, and Its Relatives (Rodentia: Bathyergidae). PLoS One, 11, e0167079.

da Silva Serra, I., Husson, Z., Bartlett, J. D. and Smith E. S. (2016). Characterization of cutaneous and articular sensory neurons. Mol Pain, 12, 1-14
 
Omerbasic, D., Smith, E. S., Moroni, M, Eigenbrod, O., Homfeld, J., Reznick, J., Bennett, N. C. Faulkes, C., Selbach, M, and Lewin, G. R. (2016).  Hypofunctional TrkA accounts for the absence of pain sensitization in the African naked mole-ratCell Reports17, 748-758.

 

2015

Schuhmacher, L. N., Husson, Z. and Smith, E. S. (2015). The naked mole-rat as an animal model in biomedical research: current perspectives. Open Acc Animal Phys, 7, 137-148

 

Jeggle, P., Smith, E. S., Stewart, A. P., Haerteis, S., Korbmacher ,C., Edwardson, J. M. (2015). Atomic force microscopy imaging reveals the formation of ASIC/ENaC cross-clade ion channels. Biochem Biophys Res Comm, 464, 38
 
Omerbašić, D., Schuhmacher, L. N., Bernal Sierra, Y. A., Smith, E. S. and Lewin, G. R (2015). ASICs and mammalian mechanoreceptor function. Neuropharm, 94, 80-86
 

Schuhmacher, L. N., Srivats, S. and Smith, E. St. J (2015). Structural domains underlying the activation of acid-sensing ion channel 2a. Mol Pharmacol, 87, 561-71

 

2014

Rahman, T. and Smith, E. St. J. (2014)In silico assessment of interaction of sea anemone toxin APETx2 and acid sensing channel 3. Biochem. Biophys. Res. Commun., 450, 384-9

Lewin, G. R., Lechner, S. G. and Smith, E. St. J. (2014). Nerve growth factor and nociception: from experimental embryology to new analgesic therapy. Handb Exp Pharmacol, 220, 251-82.

Kozlenkov, A., Lapatsina, L., Lewin, G. R. and Smith, E. St. J. (2014). Subunit-specific inhibition of acid sensing ion channels by stomatin-like protein 1. J Physiol, 592, 557-69.

2013

Smith, E. St. J., Martinez-Valazquez, L. and Ringstad, N. (2013). A chemoreceptor that detects molecular carbon dioxide. J Biol Chem, 288, 37071-81.

2012

Brand, J., Smith, E. St. J., Schwefel, D., Lapatsina, L., Poole, K., Omerbasic, D., Kozlenkov, A., Behlke, J., Lewin, G. R. and Daumke, O. (2012). A stomatin dimer modulates the activity of acid-sensing ion channels. EMBO J., 31, 3635 – 3646.

Lapatsina, L., Jira, J., Smith, E. St. J., Poole, K., Kozlenkov, A., Bilbao, D., Lewin, G. R. and Heppenstall, P. A. (2012). A complex of Stomatin and STOML3 defines a highly mobile vesicle pool in sensory neurons. Open Biology, 2, 120096.

Smith, E. St. J., Purfürst, E., Grigoryan, T., Park, T. J., Bennett, N. C. and Lewin, G. R. (2012). A specific paucity of unmyelinated C-fibers in cutaneous peripheral nerves of the African naked-mole rat: A comparative analysis using six species of Bathyergidae. J. Comp. Neurol., 520, 2785 – 2803.

2011

Smith, E. St. J., Omerbasic, D., Lechner, S. G., Anirudhan, G., Lapatsina, L. and Lewin, G. R. (2011). The physiological basis of acid insensitivity in the African naked mole rat. Science, 334, 1557 – 1560.

2010

Smith, E. St. J., Blass, G. R. C., Lewin, G.R. and Park, T.J. (2010). Lack of histamine-induced itch in the African naked mole-rat and “rescue” by substance P administration. Mol. Pain, 6, 29.

2009

Smith, E. St. J. and Lewin, G. R. (2009). Nociceptors: a phylogenetic view. J. Comp. Physiol. A 195, 1089 – 1106.

2008

Park, T. J., Lu, Y.*, Juttner, R.*, Smith, E. St. J., Hu, J., Brand, A., Wetzel, C., Milenkovic, N., Erdmann, B., Heppenstall, P. A., Laurito, C. E., Wilson, S. P. and Lewin, G. R. (2008). Selective inflammatory pain insensitivity in the African naked mole-rat (Heterocephalus glaber). PLoS Biol. 6, e13. (* equal contribution)

2007

Cadiou, H., Studer, M., Jones, N. G., Smith, E. S., Ballard, A., McMahon, S.B. and McNaughton, P.A. (2007) Modulation of acid-sensing ion channel activity by nitric oxide. J. Neurosci., 27, 13251-13260.

Smith, E. S., Zhang, X., Cadiou, H. and McNaughton, P. A. (2007) Proton binding sites involved in the activation of acid sensing ion channel ASIC2a. Neurosci.Lett., 426, 12-17.

Smith, E. S., Cadiou, H. and McNaughton, P. A. (2007) Arachidonic acid potentiates acid-sensing ion channels in rat sensory neurons by a direct action. Neuroscience, 145, 686-698.

For a full list of publications go to Google Scholar.