Cryopreserved human precision-cut lung slices as a bioassay for live tissue banking a viability study of bronchodilation with bitter-taste receptor agonists

American Journal of Respiratory Cell and Molecular Biology

Volumn 54, Issue 5, 2016, Pages 656-663

  Bai, Yan ^a   Krishnamoorthy, Nandini ^b   Patel, Kruti R ^a   Rosas, Ivan ^b   Sanderson, Michael J ^c   Ai, Xingbin ^a,b  

^a BOSTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b BRIGHAM AND WOMEN S HOSPITAL   (United States)

^c UNIVERSITY OF MASSACHUSETTS MEDICAL SCHOOL   (United States)

Author keywords

Biobank; Bitter taste receptor; Ca21 oscillations; Cryopreservation; Human precision cut lung slices

Indexed keywords

CHLOROQUINE; QUININE; BRONCHODILATING AGENT; G PROTEIN COUPLED RECEPTOR;

AIRWAY SMOOTH MUSCLE CELL; ARTICLE; BIOASSAY; BRONCHODILATATION; CALCIUM CELL LEVEL; CALCIUM TRANSPORT; CD4+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; CELL VIABILITY; CONTROLLED STUDY; CRYOPRESERVATION; FLUORESCENCE MICROSCOPY; HUMAN; HUMAN CELL; HUMAN TISSUE; IMMUNOCOMPETENT CELL; LUNG SLICE; LYMPHOCYTE ACTIVATION; LYMPHOCYTE PROLIFERATION; PHAGOCYTE; PHAGOCYTOSIS; SMOOTH MUSCLE CONTRACTILITY; T LYMPHOCYTE; TISSUE BANK; AGONISTS; CALCIUM SIGNALING; CELL SURVIVAL; CYTOLOGY; DRUG EFFECTS; LUNG; LYMPHOCYTE; METABOLISM; MUSCLE CONTRACTION; MUSCLE RELAXATION; PROCEDURES; SMOOTH MUSCLE CELL; TASTE;

BIOLOGICAL ASSAY; BRONCHODILATOR AGENTS; CALCIUM SIGNALING; CELL SURVIVAL; CRYOPRESERVATION; HUMANS; LUNG; LYMPHOCYTES; MUSCLE CONTRACTION; MUSCLE RELAXATION; MYOCYTES, SMOOTH MUSCLE; PHAGOCYTES; RECEPTORS, G-PROTEIN-COUPLED; TASTE; TISSUE BANKS;

EID: 84988961792     PISSN: 10441549     EISSN: 15354989     Source Type: Journal    
DOI: 10.1165/rcmb.2015-0290MA     Document Type: Article

References (46)

1. Sanderson MJ. Exploring lung physiology in health and disease with lung slices. Pulm Pharmacol Ther 2011;24:452-465
2. Morin JP, Baste JM, Gay A, Crochemore C, Corbie re C, Monteil C. Precision cut lung slices as an efficient tool for in vitro lung physiopharmacotoxicology studies. Xenobiotica 2013;43:63-72
3. Jain N, Miu B, Jiang JK, McKinstry KK, Prince A, Swain SL, Greiner DL, Thomas CJ, Sanderson MJ, Berg LJ, et al. CD28 and ITK signals regulate autoreactive T cell trafficking. Nat Med 2013;19: 1632-1637
4. Wohlsen A, Martin C, Vollmer E, Branscheid D, Magnussen H, Becker WM, Lepp U, Uhlig S. The early allergic response in small airways of human precision-cut lung slices. Eur Respir J 2003;21:1024-1032
5. Perez JF, Sanderson MJ. The frequency of calcium oscillations induced by 5-HT, ACH, and KCl determine the contraction of smooth muscle cells of intrapulmonary bronchioles. J Gen Physiol 2005;125:535-553
6. Henjakovic M, Sewald K, Switalla S, Kaiser D, Müller M, Veres TZ, Martin C, Uhlig S, Krug N, Braun A. Ex vivo testing of immune responses in precision-cut lung slices. Toxicol Appl Pharmacol 2008;231:68-76
7. Fahy GM, Guan N, de Graaf IA, Tan Y, Griffin L, Groothuis GM. Cryopreservation of precision-cut tissue slices. Xenobiotica 2013;43: 113-132
8. Kasper HU, Konze E, KutinováCanováN, Dienes HP, Dries V. Cryopreservation of precision cut tissue slices (PCTS): investigation of morphology and reactivity. Exp Toxicol Pathol 2011;63:575-580
9. Rosner SR, Ram-Mohan S, Paez-Cortez JR, Lavoie TL, Dowell ML, Yuan L, Ai X, Fine A, Aird WC, Solway J, et al. Airway contractility in the precision-cut lung slice after cryopreservation. Am J Respir Cell Mol Biol 2014;50:876-881
10. Pegg DE. Principles of cryopreservation. Methods Mol Biol 2015;1257:3-19
11. Gao D, Critser JK. Mechanisms of cryoinjury in living cells. ILAR J 2000; 41:187-196
12. Meryman HT. Cryopreservation of living cells: principles and practice. Transfusion 2007;47:935-945
13. Liggett SB. Bitter taste receptors in the wrong place: novel airway smooth muscle targets for treating asthma. Trans Am Clin Climatol Assoc 2014;125:64-74, discussion 74-75
14. An SS, Wang WC, Koziol-White CJ, Ahn K, Lee DY, Kurten RC, Panettieri RA Jr, Liggett SB. TAS2R activation promotes airway smooth muscle relaxation despite b(2)-adrenergic receptor tachyphylaxis. Am J Physiol Lung Cell Mol Physiol 2012;303:L304-L311
15. Bergner A, Sanderson MJ. Acetylcholine-induced calcium signaling and contraction of airway smooth muscle cells in lung slices. J Gen Physiol 2002;119:187-198
16. Aggarwal NR, King LS, D'Alessio FR. Diverse macrophage populations mediate acute lung inflammation and resolution. Am J Physiol Lung Cell Mol Physiol 2014;306:L709-L725
17. Lavin Y, Winter D, Blecher-Gonen R, David E, Keren-Shaul H, Merad M, Jung S, Amit I. Tissue-resident macrophage enhancer landscapes are shaped by the local microenvironment. Cell 2014;159: 1312-1326
18. Sathaliyawala T, Kubota M, Yudanin N, Turner D, Camp P, Thome JJ, Bickham KL, Lerner H, Goldstein M, Sykes M, et al. Distribution and compartmentalization of human circulating and tissue-resident memory T cell subsets. Immunity 2013;38:187-197
19. Coquet JM, Schuijs MJ, Smyth MJ, Deswarte K, Beyaert R, Braun H, Boon L, Karlsson Hedestam GB, Nutt SL, Hammad H, et al. Interleukin-21-producing CD4(1) T cells promote type 2 immunity to house dust mites. Immunity 2015;43:318-330
20. Kudo M, Melton AC, Chen C, Engler MB, Huang KE, Ren X, Wang Y, Bernstein X, Li JT, Atabai K, et al. IL-17A produced by ab T cells drives airway hyper-responsiveness in mice and enhances mouse and human airway smooth muscle contraction. Nat Med 2012;18: 547-554
21. Yu YA, Hotten DF, Malakhau Y, Volker E, Ghio AJ, Noble PW, Kraft M, Hollingsworth JW, Gunn MD, Tighe RM. Flow cytometric analysis of myeloid cells in human blood, bronchoalveolar lavage, and lung tissues. Am J Respir Cell Mol Biol 2015
22. Cooper PR, Panettieri RA Jr. Steroids completely reverse albuterolinduced beta(2)-adrenergic receptor tolerance in human small airways. J Allergy Clin Immunol 2008;122:734-740
23. Deshpande DA, Walseth TF, Panettieri RA, Kannan MS. CD38/cyclic ADP-ribose-mediated Ca21 signaling contributes to airway smooth muscle hyper-responsiveness. FASEB J 2003;17:452-454
24. Ressmeyer AR, Bai Y, Delmotte P, Uy KF, Thistlethwaite P, Fraire A, Sato O, Ikebe M, Sanderson MJ. Human airway contraction and formoterol-induced relaxation is determined by Ca21 oscillations and Ca21 sensitivity. Am J Respir Cell Mol Biol 2010;43:179-191
25. Prakash YS, Pabelick CM, Kannan MS, Sieck GC. Spatial and temporal aspects of ACh-induced [Ca21]i oscillations in porcine tracheal smooth muscle. Cell Calcium 2000;27:153-162
26. Berridge MJ. Smooth muscle cell calcium activation mechanisms. J Physiol 2008;586:5047-5061
27. Baatz JE, Newton DA, Riemer EC, Denlinger CE, Jones EE, Drake RR, Spyropoulos DD. Cryopreservation of viable human lung tissue for versatile post-thaw analyses and culture. In Vivo 2014;28:411-423
28. Bakhach J. The cryopreservation of composite tissues: principles and recent advancement on cryopreservation of different type of tissues. Organogenesis 2009;5:119-126
29. MacRae JW, Tholpady SS, Ogle RC, Morgan RF. Ex vivo fat graft preservation: effects and implications of cryopreservation. Ann Plast Surg 2004;52:281-282, discussion 283
30. Maas WJ, Leeman WR, Groten JP, van Sandt JJ. Cryopreservation of precision-cut rat liver slices using a computer-controlled freezer. Toxicol In Vitro 2000;14:523-530
31. Mukherjee S, Trice J, Shinde P, Willis RE, Pressley TA, Perez-Zoghbi JF. Ca21 oscillations, Ca21 sensitization, and contraction activated by protein kinase C in small airway smooth muscle. J Gen Physiol 2013;141:165-178
32. Perez-Zoghbi JF, Sanderson MJ. Endothelin-induced contraction of bronchiole and pulmonary arteriole smooth muscle cells is regulated by intracellular Ca21 oscillations and Ca21 sensitization. Am J Physiol Lung Cell Mol Physiol 2007;293:L1000-L1011
33. Chiba Y, Nakazawa S, Todoroki M, Shinozaki K, Sakai H, Misawa M. Interleukin-13 augments bronchial smoothmuscle contractility with an upregulation of RhoA protein. Am J Respir Cell Mol Biol 2009;40:159-167
34. Lan B, Deng L, Donovan GM, Chin LY, Syyong HT, Wang L, Zhang J, Pascoe CD, Norris BA, Liu JC, et al. Force maintenance and myosin filament assembly regulated by Rho-kinase in airway smooth muscle. Am J Physiol Lung Cell Mol Physiol 2015;308:L1-L10
35. Artamonov MV, Momotani K, Stevenson A, Trentham DR, Derewenda U, Derewenda ZS, Read PW, Gutkind JS, Somlyo AV. Agonist-induced Ca21 sensitization in smooth muscle: redundancy of Rho guanine nucleotide exchange factors (RhoGEFs) and response kinetics, a caged compound study. J Biol Chem 2013;288:34030-34040
36. Bai Y, Sanderson MJ. Modulation of the Ca21 sensitivity of airway smooth muscle cells in murine lung slices. Am J Physiol Lung Cell Mol Physiol 2006b;291:L208-L221
37. Somlyo AP, Somlyo AV. Ca21 sensitivity of smooth muscle and nonmuscle myosin II: modulated by G proteins, kinases, and myosin phosphatase. Physiol Rev 2003;83:1325-1358
38. Gosens R, Stelmack GL, Dueck G, Mutawe MM, Hinton M, McNeill KD, Paulson A, Dakshinamurti S, Gerthoffer WT, Thliveris JA, et al. Caveolae facilitate muscarinic receptor-mediated intracellular Ca21 mobilization and contraction in airway smooth muscle. Am J Physiol Lung Cell Mol Physiol 2007;293:L1406-L1418
39. Delmotte P, Sanderson MJ. Effects of formoterol on contraction and Ca21 signaling of mouse airway smooth muscle cells. Am J Respir Cell Mol Biol 2010;42:373-381
40. Bai Y, Sanderson MJ. Airway smooth muscle relaxation results from a reduction in the frequency of Ca21 oscillations induced by a cAMP-mediated inhibition of the IP3 receptor. Respir Res 2006;7:34
41. Morgan SJ, Deshpande DA, Tiegs BC, Misior AM, Yan H, Hershfeld AV, Rich TC, Panettieri RA, An SS, Penn RB. b-agonist-mediated relaxation of airway smooth muscle is protein kinase A-dependent. J Biol Chem 2014;289:23065-23074
42. McGraw DW, Elwing JM, Fogel KM, Wang WC, Glinka CB, Mihlbachler KA, Rothenberg ME, Liggett SB. Crosstalk between Gi and Gq/Gs pathways in airway smooth muscle regulates bronchial contractility and relaxation. J Clin Invest 2007;117: 1391-1398
43. Delmotte P, Ressmeyer AR, Bai Y, Sanderson MJ. Mechanisms of airway smooth muscle relaxation induced by beta2-adrenergic agonists. Front Biosci (Landmark Ed) 2010;15:750-764
44. Robinett KS, Koziol-White CJ, Akoluk A, An SS, Panettieri RA Jr, Liggett SB. Bitter taste receptor function in asthmatic and nonasthmatic human airway smooth muscle cells. Am J Respir Cell Mol Biol 2014;50:678-683
45. Deshpande DA, Wang WC, McIlmoyle EL, Robinett KS, Schillinger RM, An SS, Sham JS, Liggett SB. Bitter taste receptors on airway smooth muscle bronchodilate by localized calcium signaling and reverse obstruction. Nat Med 2010;16:1299-1304
46. Tan X, Sanderson MJ. Bitter tasting compounds dilate airways by inhibiting airway smooth muscle calcium oscillations and calcium sensitivity. Br J Pharmacol 2014;171:646-662