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Specialty Areas:

Airway Epithelial Cell Biology and Airway Surface Liquid Homeostasis in CF and COPD

Research Focus:

It has recently been shown that a critical component of airways innate defense is the thin (7 µm) liquid layer lining airway surfaces, the periciliary liquid (PCL), that provides a low viscosity solution for ciliary beating and acts a lubricant layer for mucus transport. Normal airways appear to be able to sense the PCL volume and adjust ion channel activity accordingly by unknown mechanisms. A proposed model for ASL volume regulation is shown in Figure 1.

Apical membrane ion channel activity controls the amount of salt (and water) on airway surfaces and hence, PCL volume and mucus hydration levels. It has recently been proposed that the initiating event in CF lung disease is depletion of the PCL due to abnormal ion channel activity (i.e. a lack of CFTR), which causes dehydrated mucus to adhere to airway surfaces, preventing it from being cleared (Fig. 2), causing increased bacterial infections.

The long term goal of this laboratory is to understand how homeostasis of PCL volume occurs in airway epithelia under normal and pathophysiological conditions. Currently, research in the Tarran lab is focused on three main areas, listed below, and we utilize cell biological and biochemical techniques coupled with in vivo translational approaches to address these questions:

  1. Regulation of epithelial cell function by the extracellular environment: We have hypothesized that nucleotides, proteases and other molecules contained in the ASL (ATP for example) can regulate airway ion transport. Fig. 3 depicts cystic fibrosis airway cells that have lost the ability to regulate ASL volume following infection with GFP-labeled viruses that inhibit intracellular Ca2+ signaling by depleting extracellular ATP.
  2. Gender differences in cystic fibrosis lung disease: Females suffer more severely with cystic fibrosis than their male counterparts, resulting in a significantly shorter lifespan. This gender difference becomes apparent after puberty. Accordingly, we are currently investigating whether estrogens affect Ca2+ signaling and ASL homeostasis. Figure 4 shows an example of simultaneous Fura-2 imaging (as a marker of intracellular Ca2+) and a fusion protein of Estrogen Receptor α (ER α) conjugated to orange fluorescent protein (mOr).
  3. The effects of cigarette smoke on epithelial airway ion transport: Similar to CF, long term tobacco exposure also results in chronic mucus accumulation. We have found that acute tobacco exposure causes a loss of CFTR from the plasma membrane (Fig. 5) and are currently investigating this phenomenon

Techniques Employed:

  • Ca2+ imaging
  • Confocal microscopy
  • Electrophysiology (In vivo nasal potential difference measurements, microelectrodes & Ussing chambers)
  • Fluorescence resonance energy transfer (FRET)
  • Mass Spectrometry
  • Molecular Biology & Real Time (q)PCR
  • Tissue culture
  • Western Blot

Selected Bibliography:

  1. Moore MM, Abraham I, Ballantyne M, Behrsing H, Cao X, Clements J, Gaca M, Gillman G, Hashizume T, Heflich RH, Hurtado S, Jordan KG, Leverette R, McHugh D, Miller-Holt J, Phillips G, Recio L, Roy S, Scian M, Simms L, Smart DJ, Stankowski LF Jr, Tarran R, Thorne D, Weber E, Wieczorek R, Yoshino K, Curren R. Key Challenges and Recommendations for In Vitro Testing of Tobacco Products for Regulatory Applications: Consideration of Test Materials and Exposure Parameters. Altern Lab Anim. 2023 Jan;51(1):55-79. doi: 10.1177/02611929221146536. PMID: 36821083.
  2. Tyrrell J, Ghosh A, Manzo ND, Randell SH, Tarran R. Evaluation of chronic cigarette smoke exposure in human bronchial epithelial cultures. J Appl Toxicol. 2023 Jan 3. doi: 10.1002/jat.4430. Epub ahead of print. PMID: 36594405.
  3. Goriounova AS, Gilmore RC, Wrennall JA, Tarran RSuper resolution microscopy analysis reveals increased Orai1 activity in asthma and cystic fibrosis lungs. J Cyst Fibros. 2023 Jan;22(1):161-171. doi: 10.1016/j.jcf.2022.07.003. PMID: 35961837. PMCID: PMC9982747.
  4. Reidel B, Abdelwahab S, Wrennall JA, Clapp PW, Beers JL, Jackson KD, Tarran R, Kesimer M. Vaping additives cannabinoid oil and vitamin E acetate adhere to and damage the human airway epithelium. J Appl Toxicol. 2022 Nov 13. doi: 10.1002/jat.4415. Epub ahead of print. PMID: 36372912.
  5. Wold LE, Tarran R, Crotty Alexander LE, Hamburg NM, Kheradmand F, St Helen G, Wu JC; American Heart Association Council on Basic Cardiovascular Sciences; Council on Arteriosclerosis, Thrombosis and Vascular Biology; Council on Hypertension; and Stroke Council. Cardiopulmonary Consequences of Vaping in Adolescents: A Scientific Statement From the American Heart Association. Circ Res. 2022 Jul 22;131(3):e70-e82. doi: 10.1161/RES.0000000000000544. PMID: 35726609.
  6. Abdelwahab S, Ghosh A, Wrennall J, Tarran R. Vaping /E-liquid Exposure Causes Dysregulation of Neutrophil Extracellular Trap formation. FASEB J. 2022 May;36 Suppl 1. doi: 10.1096/fasebj.2022.36.S1.L7511. PMID: 35556998.
  7. Wu T, Goriounova AS, Worthington EN, Wrennall JA, Ghosh A, Ahmad S, Flori Sassano M, Tarran R. SPLUNC1 is a negative regulator of the Orai1 Ca2+ channel. Physiol Rep. 2022 May;10(10):e15306. doi: 10.14814/phy2.15306. PMID: 35581745; PMCID: PMC9114653.
  8. Smith AJ, Bustamante-Marin XM, Yin W, Sears PR, Herring LE, Dicheva NN, López-Giráldez F, Mane S, Tarran R, Leigh MW, Knowles MR, Zariwala MA, Ostrowski LE. The role of SPAG1 in the assembly of axonemal dyneins in human airway epithelia. J Cell Sci. 2022 Mar 15;135(6):jcs259512. doi: 10.1242/jcs.259512. PMID: 35178554. PMCID: PMC8995097.
  9. Wrennall JA, Ahmad S, Worthington EN, Wu T, Goriounova AS, Voeller AS, Stewart IE, Ghosh A, Krajewski K, Tilley SL, Hickey AJ, Sassano MF, Tarran R. A SPLUNC1 Peptidomimetic Inhibits Orai1 and Reduces Inflammation in a Murine Allergic Asthma Model. Am J Respir Cell Mol Biol. 2022 Mar 15;135(6):jcs259512. doi: 10.1165/rcmb.2020-0452OC. PMID: 34807800. PMCID: PMC8937239.
  10. Davis ES, Ghosh A, Coakley RD, Wrennall JA, Lubamba BA, Rowell TR, Dang H, Pawlak EA, Li Q, Alexis NE, Ribeiro CMP, Tarran RChronic E-Cigarette Exposure Alters Human Alveolar Macrophage Morphology and Gene Expression. Nicotine Tob Res. 2022 Feb 14;24(3):395-399. doi: 10.1093/ntr/ntab186. PMID: 34519792. PMCID: PMC8842413.
  11. Neczypor EW, Mears MJ, Ghosh A, Sassano MF, Gumina RJ, Wold LE, Tarran R. E-Cigarettes and Cardiopulmonary Health: Review for Clinicians. Circulation. 2022 Jan 18;145(3):219-232. doi: 10.1161/CIRCULATIONAHA.121.056777. PMID: 35041473; PMCID: PMC8820458.
  12. Ghosh A, Girish V, Yuan ML, Coakley RD, Wrennall JA, Alexis NE, Sausville EL, Vasudevan A, Chait AR, Sheltzer JM, Tarran RCombustible and Electronic Cigarette Exposures Increase ACE2 Activity and SARS-CoV-2 Spike Binding. Am J Respir Crit Care Med. 2022 Jan 1;205(1):129-133. doi: 10.1164/rccm.202106-1377LE. PMID: 34748720. PMCID: PMC8865588.
  13. Woodall M, Reidel B, Kesimer M, Tarran R, Baines DL. Culture with apically applied healthy or disease sputum alters the airway surface liquid proteome and ion transport across human bronchial epithelial cells. Am J Physiol Cell Physiol. 2021 Dec 1;321(6):C954-C963. doi: 10.1152/ajpcell.00234.2021. PMID: 34613844. PMCID: PMC8714986.
  14. Khanal S, Webster M, Niu N, Zielonka J, Nunez M, Chupp G, Slade MD, Cohn L, Sauler M, Gomez JL, Tarran R, Sharma L, Dela Cruz CS, Egan M, Laguna T, Britto CJ. SPLUNC1: a novel marker of cystic fibrosis exacerbations. Eur Respir J. 2021 Nov 11;58(5):2000507. doi: 10.1183/13993003.00507-2020. PMID: 33958427; PMCID: PMC8571118.
  15. Ahmad S, Sassano MF, Tarran R. Loose ENDs: Electronic Nicotine Delivery Systems and the FDA’s Recent Enforcement Policy. Eur Med J Respir. 2020 Nov;8(1):93-96. PMID: 34336231; PMCID: PMC8323585.
  16. Giorgetti M, Klymiuk N, Bähr A, Hemmerling M, Jinton L, Tarran R, Malmgren A, Åstrand A, Hansson GC, Ermund A. New generation ENaC inhibitors detach cystic fibrosis airway mucus bundles via sodium/hydrogen exchanger inhibition. Eur J Pharmacol. 2021 Aug 5;904:174123. doi: 10.1016/j.ejphar.2021.174123. PMID: 33974881; PMCID: PMC8477379.
  17. Bearham J, Krutrök N, Lindberg B, Woodall M, Astrand A, Taylor JD, Biggart M, Vasiljevs S, Tarran R, Baines DL. A modified fluorescent sensor for reporting glucose concentration in the airway lumen. PLoS One. 2021 Jul 9;16(7):e0254248. doi: 10.1371/journal.pone.0254248. PMID: 34242292; PMCID: PMC8270177.
  18. Lin J, Taggart M, Borthwick L, Fisher A, Brodlie M, Sassano MF, Tarran R, Gray MA. Acute cigarette smoke or extract exposure rapidly activates TRPA1-mediated calcium influx in primary human airway smooth muscle cells. Sci Rep. 2021 May 5;11(1):9643. doi: 10.1038/s41598-021-89051-4. PMID: 33953304; PMCID: PMC8100124.
  19. Ghosh A, Ahmad S, Coakley RD, Sassano MF, Alexis NE, Tarran R. Lipid-Laden Macrophages are not Unique to EVALI Patients. Am J Respir Crit Care Med. 2021 Apr 15;203(8):1030-1033. doi: 10.1164/rccm.202009-3507LE. PMID: 33332247. PMCID: PMC8048758.
  20. Ghosh A, Beyazcicek O, Davis ES, Onyenwoke RU, Tarran R. Cellular effects of nicotine salt-containing e-liquids. J Appl Toxicol. 2021 Mar;41(3):493-505. doi: 10.1002/jat.4060. PMID: 33034066.
  21. Tarran R, Barr RG, Benowitz NL, Bhatnagar A, Chu HW, Dalton P, Doerschuk CM, Drummond MB, Gold DR, Goniewicz ML, Gross ER, Hansel NN, Hopke PK, Kloner RA, Mikheev VB, Neczypor EW, Pinkerton KE, Postow L, Rahman I, Samet JM, Salathe M, Stoney CM, Tsao PS, Widome R, Xia T, Xiao D, Wold LE. E-Cigarettes and Cardiopulmonary Health. Function (Oxf). 2021 Feb 8;2(2):zqab004. doi: 10.1093/function/zqab004. PMID: 33748758; PMCID: PMC7948134.
  22. Zhang R, Jones MM, Dornsife RE, Wu T, Sivaraman V, Tarran R, Onyenwoke RU. JUUL e-liquid exposure elicits cytoplasmic Ca2+ responses and leads to cytotoxicity in cultured airway epithelial cells. Toxicol Lett. 2021 Feb 1;337:46-56. doi: 10.1016/j.toxlet.2020.11.017. PMID: 33253780; PMCID: PMC7772262.
  23. Correia-Álvarez E, Keating JE, Glish G, Tarran R, Sassano MF. Reactive Oxygen Species, Mitochondrial Membrane Potential, and Cellular Membrane Potential Are Predictors of E-Liquid Induced Cellular Toxicity. Nicotine Tob Res. 2020 Dec 15;22(Suppl 1):S4-S13. doi: 10.1093/ntr/ntaa177. PMID: 33320253. PMCID: PMC8493666.
  24. Stanton CA, Tarran R, Mermelstein R. Early Studies of Respiratory Disease Associations with Nicotine and Tobacco Use. Nicotine Tob Res. 2020 Dec 15;22(Suppl 1):S1-S3. doi: 10.1093/ntr/ntaa200. PMID: 33320247; PMCID: PMC7737475.
  25. Abdelwahab SH, Reidel B, Martin JR, Ghosh A, Keating JE, Haridass P, Carpenter J, Glish GL, Tarran R, Doerschuk CM, Kesimer M. Cigarillos Compromise the Mucosal Barrier and Protein Expression in Airway Epithelia. Am J Respir Cell Mol Biol. 2020 Dec;63(6):767-779. doi: 10.1165/rcmb.2019-0085OC. PMID: 32877614. PMCID: PMC7790145.
  26. Woodall M, Jacob J, Kalsi K, Davis E, Kenyon B, Khan IH, Garnett JP, Tarran R, Baines DL. E-cigarette constituents propylene glycol and vegetable glycerine decrease glucose uptake and its metabolism in airway epithelial cells in vitro. Am J Physiol Lung Cell Mol Physiol. 2020 Dec 1;319(6):L957-L967. doi: 10.1152/ajplung.00123.2020. PMID: 32996783. PMCID: PMC7792687.
  27. Herman M, Tarran R. E-cigarettes, nicotine, the lung and the brain: multi-level cascading pathophysiology. J Physiol. 2020 Nov;598(22):5063-5071. doi: 10.1113/JP278388. PMID: 32515030. PMCID: PMC7721976.
  28. Crotty Alexander LE, Ware LB, Calfee CS, Callahan SJ, Eissenberg T, Farver C, Goniewicz ML, Jaspers I, Kheradmand F, King TE Jr, Meyer NJ, Mikheev V, Shields PG, Shihadeh A, Strongin R, Tarran R. NIH Workshop Report: E-cigarette or Vaping Product Use Associated Lung Injury (EVALI): Developing a Research Agenda. Am J Respir Crit Care Med. 2020 Sep 15;202(6):795-802. doi: 10.1164/rccm.201912-2332WS. PMID: 32243764. PMCID: PMC7491408.
  29. Lee RE, Miller SM, Mascenik TM, Lewis CA, Dang H, Boggs ZH, Tarran R, Randell SH. Assessing Human Airway Epithelial Progenitor Cells for Cystic Fibrosis Cell Therapy. Am J Respir Cell Mol Biol. 2020 Sep;63(3):374-385. doi: 10.1165/rcmb.2019-0384OC. PMID: 32437238; PMCID: PMC7462339.
  30. Ahmad S, Kim CSK, Tarran R. The SPLUNC1-βENaC complex prevents Burkholderia cenocepacia invasion in normal airway epithelia. Respir Res. 2020 Jul 17;21(1):190. doi: 10.1186/s12931-020-01454-5. PMID: 32680508; PMCID: PMC7368771.
  31. Barros SP, Fahimipour F, Tarran R, Kim S, Scarel-Caminaga RM, Justice A, North K. Epigenetic reprogramming in periodontal disease: Dynamic crosstalk with potential impact in oncogenesis. Periodontol 2000. 2020 Feb;82(1):157-172. doi: 10.1111/prd.12322. PMID: 31850624.
  32. Rowell TR, Keating JE, Zorn BT, Glish GL, Shears SB, Tarran R. Flavored E-liquids Increase Cytoplasmic Ca2+ Levels in Airway Epithelia. Am J Physiol Lung Cell Mol Physiol. 2020 Feb 1;318(2):L226-L241. doi: 10.1152/ajplung.00123.2019. PMID: 31693394. PMCID: PMC7052665.
  33. Ghosh A, Coakley RD, Ghio AJ, Muhlebach MS, Esther CR Jr, Alexis NE, Tarran RChronic E-Cigarette Use Increases Neutrophil Elastase and Matrix Metalloprotease Levels in the Lung. Am J Respir Crit Care Med. 2019 Dec 1;200(11):1392-1401. doi: 10.1164/rccm.201903-0615OC. PMID: 31390877. PMCID: PMC6884043.
  34. Gotts JE, Jordt SE, McConnell R, Tarran R. What are the respiratory effects of e-cigarettes? BMJ. 2019 Sep 30;366:l5275. doi: 10.1136/bmj.l5275. PMID: 31570493. PMCID: PMC7850161.
  35. Marklew AJ, Patel W, Moore PJ, Tan CD, Smith AJ, Sassano MF, Gray MA, Tarran R. Cigarette Smoke Exposure Induces Retrograde Trafficking of CFTR to the Endoplasmic Reticulum. Sci Rep. 2019 Sep 20;9(1):13655. doi: 10.1038/s41598-019-49544-9. PMID: 31541117. PMCID: PMC6754399.
  36. Wetendorf M, Randall LT, Lemma MT, Hurr SH, Pawlak JB, Tarran R, Doerschuk CM, Caron KM. E-Cigarette Exposure Delays Implantation and Causes Reduced Weight Gain in Female Offspring Exposed In Utero. J Endocr Soc. 2019 Sep 5;3(10):1907-1916. doi: 10.1210/js.2019-00216. PMID: 31598571. PMCID: PMC6777403.
  37. Ahmad S, Gilmore RC, Alexis NE, Tarran R. SPLUNC1 Loses its Antimicrobial Activity in Acidic Cystic Fibrosis Airway Secretions. Am J Respir Crit Care Med. 2019 Sep 1;200(5):633-636. doi: 10.1164/rccm.201812-2303LE. PMID: 31013116. PMCID: PMC6727152.
  38. Couroux P, Farias P, Rizvi L, Griffin K, Hudson C, Crowder T, Tarran R, Tullis E. First clinical trials of novel ENaC targeting therapy, SPX-101, in healthy volunteers and adults with cystic fibrosis. Pulm Pharmacol Ther. 2019 Jul 11;58:101819. doi: 10.1016/j.pupt.2019.101819. PMID: 31302339.
  39. Moore PJ, Sesma J, Alexis NE, Tarran R. Tobacco exposure inhibits SPLUNC1-dependent antimicrobial activity. Respir Res. 2019 May 21;20(1):94. doi: 10.1186/s12931-019-1066-2. PMID: 31113421. PMCID: PMC6530064.
  40. Patel W, Moore PJ, Sassano MF, Lopes-Pacheco M, Aleksandrov AA, Amaral MD, Tarran R, Gray MA. Increases in cytosolic Ca2+ induce dynamin- and calcineurin-dependent internalisation of CFTR. Cell Mol Life Sci. 2019 Mar;76(5):977-994. doi: 10.1007/s00018-018-2989-3. PMID: 30547226. PMCID: PMC6394554.
  41. Hill DB, Long RF, Kissner WJ, Atieh E, Garbarine IC, Markovetz MR, Fontana NC, Christy M, Habibpour M, Tarran R, Forest MG, Boucher RC, Button B. Pathological mucus and impaired mucus clearance in cystic fibrosis patients result from increased concentration, not altered pH. Eur Respir J. 2018 Dec 6;52(6). doi: 10.1183/13993003.01297-2018. PMID: 30361244. PMCID: PMC6446239.
  42. Webster MJ, Tarran RSlippery when wet: airway surface liquid homeostasis and mucus hydration. Curr Top Membr. 2018;81:293-335. doi: 10.1016/bs.ctm.2018.08.004. PMID: 30243435.
  43. Webster MJ, Reidel B, Tan CD, Ghosh A, Alexis NE, Donaldson SH, Kesimer M, Ribeiro CMP, Tarran RSPLUNC1 degradation by the cystic fibrosis mucosal environment drives airway surface liquid dehydration. Eur Respir J. 2018 Oct 4;52(4). doi: 10.1183/13993003.00668-2018. PMID: 30190268. PMCID: PMC6547379.
  44. Moore PJ, Tarran RThe epithelial sodium channel (ENaC) as a therapeutic target for cystic fibrosis lung disease. Expert Opin Ther Targets. 2018 Aug;22(8):687-701. doi: 10.1080/14728222.2018.1501361. PMID: 30028216.
  45. Ghosh A, Coakley RC, Mascenik T, Rowell TR, Davis ES, Rogers K, Webster MJ, Dang H, Herring LE, Sassano MF, Livraghi-Butrico A, Van Buren SK, Graves LM, Herman MA, Randell SH, Alexis NE, Tarran R. Chronic e-cigarette exposure alters the human bronchial epithelial proteome. Am J Respir Crit Care Med. 2018 Jul 1;198(1):67-76. doi: 10.1164/rccm.201710-2033OC. PMID: 29481290. PMCID: PMC6034122.
  46. Moore PJ, Reidel B, Ghosh A, Sesma J, Kesimer M, Tarran R. Cigarette smoke modifies and inactivates SPLUNC1, leading to airway dehydration. FASEB J. 2018 Jun 11:fj201800345R. doi: 10.1096/fj.201800345R. PMID: 29890087. PMCID: PMC6219833.
  47. Kim CS, Ahmad S, Wu T, Walton WG, Redinbo MR, Tarran R. SPLUNC1 is an allosteric modulator of the epithelial sodium channel. FASEB J. 2018 May;32(5):2478-2491. doi: 10.1096/fj.201701126R. PMID: 29295861. PMCID: PMC5901381.
  48. Sassano MF, Davis ES, Keating JE, Zorn BT, Kochar TK, Wolfgang MC, Glish GL, Tarran R. Evaluation of e-liquid toxicity using an open-source high-throughput screening assay. PLoS Biol. 2018 Mar 27;16(3):e2003904. doi: 10.1371/journal.pbio.2003904. PMID: 29584716. PMCID: PMC5870948.
  49. Abdullah LH, Coakley R, Webster MJ, Zhu Y, Tarran R, Radicioni G, Kesimer M, Boucher RC, Davis CW, Ribeiro CMP. Mucin production and hydration responses to mucopurulent materials in normal vs. CF airway epithelia. Am J Respir Crit Care Med. 2018 Feb 15;197(4):481-491. doi: 10.1164/rccm.201706-1139OC. PMID: 29099608. PMCID: PMC5821906.
  50. Terryah ST, Fellner RC, Ahmad S, Moore PJ, Reidel B, Sesma JI, Kim CS, Garland AL, Scott DW, Sabater JR, Carpenter J, Randell SH, Kesimer M, Abraham WM, Arendshorst WJ, Tarran R. Evaluation of a SPLUNC1-derived peptide for the treatment of cystic fibrosis lung disease. Am J Physiol Lung Cell Mol Physiol. 2018 Jan 1;314(1):L192-L205. doi: 10.1152/ajplung.00546.2016. PMID: 28982737. PMCID: PMC5866433.
  51. Scott DW, Walker MP, Sesma J, Wu B, Stuhlmiller TJ, Sabater JR, Abraham WM, Crowder TM, Christensen DJ, Tarran R. SPX-101 is a novel epithelial sodium channel-targeted therapeutic for cystic fibrosis that restores mucus transport. Am J Respir Crit Care Med. 2017 Sep 15;196(6):734-744. doi: 10.1164/rccm.201612-2445OC. PMID: 28481660.
  52. Matson BC, Pierce SL, Espenschied ST, Holle E, Sweatt IH, Davis ES, Tarran R, Young SL, Kohout TA, van Duin M, Caron KM. Adrenomedullin improves fertility and promotes pinopodes and cell junctions in the peri-implantation endometrium. Biol Reprod. 2017 Sep 1;97(3):466-477. doi: 10.1093/biolre/iox101. PMID: 29025060. PMCID: PMC6248476.
  53. Schick SF, Blount BC, Jacob P Rd, Saliba NA, Bernert JT, El Hellani A, Jatlow P, Pappas RS, Wang L, Foulds J, Ghosh A, Hecht SS, Gomez JC, Martin JR, Mesaros C, Srivastava S, St Helen G, Tarran R, Lorkiewicz PK, Blair IA, Kimmel HL, Doerschuk CM, Benowitz NL, Bhatnagar A. Biomarkers of exposure to new and emerging tobacco delivery products. Am J Physiol Lung Cell Mol Physiol. 2017 Sep 1;313(3):L425-L452. doi: 10.1152/ajplung.00343.2016. PMID: 28522563. PMCID: PMC5626373.
  54. Davis ES, Sassano MF, Goodell H, Tarran R. E-liquid autofluorescence can be used as a marker of vaping deposition and third-hand vape exposure. Sci Rep. 2017 Aug 7;7(1):7459. doi: 10.1038/s41598-017-07862-w. PMID: 28785072. PMCID: PMC5547159.
  55. Rowell TR, Reeber SL, Lee SL, Harris RA, Nethery RC, Herring AH, Glish GL, Tarran R. Flavored e-cigarette liquids reduce proliferation and viability in the CALU3 airway epithelial cell line. Am J Physiol Lung Cell Mol Physiol. 2017 Jul 1;313(1):L52-L66. doi: 10.1152/ajplung.00392.2016. PMID: 28428175. PMCID: PMC5538872.
  56. Sassano MF, Ghosh A, Tarran R. Tobacco smoke constituents trigger cytoplasmic calcium release. Appl In Vitro Toxicol. 2017 Jun 1;3(2):193-198. doi: 10.1089/aivt.2016.0039. PMID: 28620626. PMCID: PMC5469188.
  57. Ghosh A, Abdelwahab SH, Reeber SL, Reidel B, Marklew AJ, Garrison AJ, Lee S, Dang H, Herring AH, Glish GL, Kesimer M, Tarran R. Little cigars are more toxic than cigarettes and uniquely change the airway gene and protein expression. Sci Rep. 2017 Apr 27;7:46239. doi: 10.1038/srep46239. PMID: 28447619. PMCID: PMC5406835.
  58. Ghosh A, Nethery RC, Herring AH, Tarran R. Flavored little cigar smoke induces cytotoxicity and apoptosis in airway epithelia. Cell Death Discov. 2017 Apr 24;3:17019. doi: 10.1038/cddiscovery.2017.19. PMID: 28496992. PMCID: PMC5402522.
  59. Wu T, Huang J, Moore PJ, Little MS, Walton WG, Fellner RC, Alexis NE, Peter Di Y, Redinbo MR, Tilley SL, Tarran R. Identification of BPIFA1/SPLUNC1 as an epithelium-derived smooth muscle relaxing factor. Nat Commun. 2017 Feb 6;8:14118. doi: 10.1038/ncomms14118. PMID: 28165446; PMCID: PMC5303822.
  60. Fellner RC, Terryah ST, Tarran R. Inhaled protein/peptide-based therapies for respiratory disease. Mol Cell Pediatr. 2016 Dec;3(1):16. doi: 10.1186/s40348-016-0044-8. PMID: 27098663. PMCID: PMC4839019.
  61. Garnett JP, Kalsi KK, Sobotta M, Bearham J, Carr G, Powell J, Brodlie M, Ward C, Tarran R, Baines DL. Hyperglycaemia and Pseudomonas aeruginosa acidify cystic fibrosis airway surface liquid by elevating epithelial monocarboxylate transporter 2 dependent lactate-H+ secretion. Sci Rep. 2016 Nov 29;6:37955. doi: 10.1038/srep37955. PMID: 27897253. PMCID: PMC5126573.
  62. Ahmad S, Tyrrell J, Walton WG, Tripathy A, Redinbo MR, Tarran R. Short palate, lung, and nasal epithelial clone 1 has antimicrobial and antibiofilm activities against the Burkholderia cepacia complex. Antimicrob Agents Chemother. 2016 Sep 23;60(10):6003-12. doi: 10.1128/AAC.00975-16. PMID: 27458217. PMCID: PMC5038247.
  63. Sun Y, Hu W, Yu X, Liu Z, Tarran R, Ravid K, Huang P. Actinin-1 binds to the C-terminus of A2B adenosine receptor (A2BAR) and enhances A2BAR cell-surface expression. Biochem J. 2016 Jul 15;473(14):2179-86. doi: 10.1042/BCJ20160272. PMID: 27208173.
  64. Watson MJ, Lee SL, Marklew AJ, Gilmore RC, Gentzsch M, Sassano MF, Gray MA, Tarran R. The cystic fibrosis transmembrane conductance regulator (CFTR) uses its C-terminus to regulate the A2B adenosine receptor. Sci Rep. 2016 Jun 9;6:27390. doi: 10.1038/srep27390. PMID: 27278076. PMCID: PMC4899698.
  65. Walton WG, Ahmad S, Little MS, Kim CS, Tyrrell J, Lin Q, Di YP, Tarran R, Redinbo MR. Structural features essential to the antimicrobial functions of human SPLUNC1. Biochemistry. 2016 May 31;55(21):2979-91. doi: 10.1021/acs.biochem.6b00271. PMID: 27145151. PMCID: PMC4887393.
  66. Turner MJ, Saint-Criq V, Patel W, Ibrahim SH, Verdon B, Ward C, Garnett JP, Tarran R, Cann MJ, Gray MA. Hypercapnia modulates cAMP signalling and cystic fibrosis transmembrane conductance regulator-dependent anion and fluid secretion in airway epithelia. J Physiol. 2016 Mar 15;594(6):1643-61. doi: 10.1113/JP271309. PMID: 26574187. PMCID: PMC4799982.
  67. Behrsing H, Raabe H, Manuppello J, Bombick B, Curren R, Sullivan K, Sethi S, Phipps R, Tesfaigzi Y, Yan S, D’Ruiz C, Tarran R, Constant S, Phillips G, Gaça M, Hayden P, Cao X, Mathis C, Hoeng J, Braun A, Hill E. Assessment of in vitro COPD models for tobacco regulatory science: Workshop proceedings, conclusions and paths forward for in vitro model use. Altern Lab Anim. 2016 May;44(2):129-66. PMID: 27256455.
  68. Rowell TR, Tarran R. Will chronic e-cigarette use cause lung disease? Am J Physiol Lung Cell Mol Physiol. 2015 Dec 15;309(12):L1398-409. doi: 10.1152/ajplung.00272.2015. PMID: 26408554. PMCID: PMC4683316.
  69. Manzanares D, Krick S, Baumlin N, Dennis JS, Tyrrell J, Tarran R, Salathe M. Airway surface dehydration by transforming growth factor β (TGF-β) in cystic fibrosis is due to decreased function of a voltage-dependent potassium channel and can be rescued by the drug pirfenidone. J Biol Chem. 2015 Oct 16;290(42):25710-6. doi: 10.1074/jbc.M115.670885. PMID: 26338706. PMCID: PMC4646213.
  70. Choi HC, Kim CS, Tarran R. Automated acquisition and analysis of airway surface liquid height by confocal microscopy. Am J Physiol Lung Cell Mol Physiol. 2015 Jul 15;309(2):L109-18. doi: 10.1152/ajplung.00027.2015. PMID: 26001773. PMCID: PMC4504972.
  71. Xu X, Balsiger R, Tyrrell J, Boyaka PN, Tarran R, Cormet-Boyaka E. Cigarette smoke exposure reveals a novel role for the MEK/ERK1/2 MAPK pathway in regulation of CFTR. Biochim Biophys Acta. 2015 Jun;1850(6):1224-32. doi: 10.1016/j.bbagen.2015.02.004. PMID: 25697727. PMCID: PMC4398641.
  72. Tyrrell J, Qian X, Freire J, Tarran R. Roflumilast combined with adenosine increases mucosal hydration in human airway epithelial cultures after cigarette smoke exposure. Am J Physiol Lung Cell Mol Physiol. 2015 May 15;308(10):L1068-77. doi: 10.1152/ajplung.00395.2014. PMID: 25795727. PMCID: PMC4437008.
  73. Åstrand AB, Hemmerling M, Root J, Wingren C, Pesic J, Johansson E, Garland AL, Ghosh A, Tarran R. Linking increased airway hydration, ciliary beating, and mucociliary clearance through ENaC inhibition. Am J Physiol Lung Cell Mol Physiol. 2015 Jan 1;308(1):L22-32. doi: 10.1152/ajplung.00163.2014. PMID: 25361567. PMCID: PMC4281700.
  74. Ghosh A, Boucher RC, Tarran R. Airway hydration and COPD. Cell Mol Life Sci. 2015;72(19):3637-52. PMID: 26068443. PMCID: PMC4567929.
  75. Rasmussen JE, Sheridan JT, Polk W, Davies CM, Tarran R. Cigarette smoke-induced Ca2+ release leads to cystic fibrosis transmembrane conductance regulator (CFTR) dysfunction. J Biol Chem. 2014 Mar 14;289(11):7671-81. doi: 10.1074/jbc.M113.545137. PMID: 24448802; PMCID: PMC3953278.
  76. Garland AL, Walton WG, Coakley RD, Tan CD, Gilmore RC, Hobbs CA, Tripathy A, Clunes LA, Bencharit S, Stutts MJ, Betts L, Redinbo MR, Tarran R. Molecular basis for pH-dependent mucosal dehydration in cystic fibrosis airways. Proc Natl Acad Sci U S A. 2013 Oct 1;110(40):15973-8. doi: 10.1073/pnas.1311999110. PMID: 24043776; PMCID: PMC3791714.
  77. Clunes LA, Davies CM, Coakley RD, Aleksandrov AA, Henderson AG, Zeman KL, Worthington EN, Gentzsch M, Kreda SM, Cholon D, Bennett WD, Riordan JR, Boucher RC, Tarran R. Cigarette smoke exposure induces CFTR internalization and insolubility, leading to airway surface liquid dehydration. FASEB J. 2012 Feb;26(2):533-45. doi: 10.1096/fj.11-192377. PMID: 21990373; PMCID: PMC3290447.
  78. Garcia-Caballero A, Rasmussen JE, Gaillard E, Watson MJ, Olsen JC, Donaldson SH, Stutts MJ, Tarran R. SPLUNC1 regulates airway surface liquid volume by protecting ENaC from proteolytic cleavage. Proc Natl Acad Sci U S A. 2009 Jul 7;106(27):11412-7. doi: 10.1073/pnas.0903609106. PMID: 19541605; PMCID: PMC2708735. Erratum in: Proc Natl Acad Sci U S A. 2009 Sep 1;106(35):15091.
  79. Coakley RD, Sun H, Clunes LA, Rasmussen JE, Stackhouse JR, Okada SF, Fricks I, Young SL, Tarran R. 17beta-Estradiol inhibits Ca2+-dependent homeostasis of airway surface liquid volume in human cystic fibrosis airway epithelia. J Clin Invest. 2008 Dec;118(12):4025-35. doi: 10.1172/JCI33893. PMID: 19033671; PMCID: PMC2582929.

Dr. Tarran has several open post-doctoral positions. Please contact him at

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