A novel 3D high-content assay identifies compounds that prevent fibroblast invasion into tissue surrogates

Experimental Cell Research

Volumn 339, Issue 1, 2015, Pages 35-43

  Wenzel, Carsten ^a   Otto, Saskia ^a   Prechtl, Stefan ^a   Parczyk, Karsten ^a   Steigemann, Patrick ^a  

^a BAYER PHARMA AG   (Germany)

Author keywords

3D co culture; Fibroblast invasion; High content invasion assay; Living tissue surrogate; Prostaglandin; ROCK

Indexed keywords

CYCLIC AMP; MYOSIN II; PROSTAGLANDIN; PROSTAGLANDIN E RECEPTOR; PROTEIN KINASE INHIBITOR; RHO KINASE;

ARTICLE; CELL ASSAY; CELL CULTURE; CELL INVASION; COCULTURE; CONTROLLED STUDY; HUMAN; HUMAN CELL; LUNG FIBROBLAST; PRIORITY JOURNAL; SPHEROID CELL; ANTAGONISTS AND INHIBITORS; BREAST NEOPLASMS; CELL CULTURE TECHNIQUE; DRUG EFFECTS; ENZYME IMMUNOASSAY; FEMALE; FIBROBLAST; HIGH THROUGHPUT SCREENING; IMAGE PROCESSING; METABOLISM; MULTICELLULAR SPHEROID; PATHOLOGY; TUMOR CELL CULTURE;

BREAST NEOPLASMS; CELL CULTURE TECHNIQUES; FEMALE; FIBROBLASTS; HIGH-THROUGHPUT SCREENING ASSAYS; HUMANS; IMAGE PROCESSING, COMPUTER-ASSISTED; IMMUNOENZYME TECHNIQUES; PROSTAGLANDINS; PROTEIN KINASE INHIBITORS; RHO-ASSOCIATED KINASES; SPHEROIDS, CELLULAR; TUMOR CELLS, CULTURED;

EID: 84947067394     PISSN: 00144827     EISSN: 10902422     Source Type: Journal    
DOI: 10.1016/j.yexcr.2015.10.003     Document Type: Article

References (48)

1. Wynn T.A., Ramalingam T.R. Mechanisms of fibrosis: therapeutic translation for fibrotic disease. Nat. Med. 2012, 18:1028-1040.
2. Karagiannis G.S., Poutahidis T., Erdman S.E., Kirsch R., Riddell R.H., Diamandis E.P. Cancer-associated fibroblasts drive the progression of metastasis through both paracrine and mechanical pressure on cancer tissue. Mol. Cancer Res. 2012, 10:1403-1418.
3. Franco O.E., Shaw A.K., Strand D.W., Hayward S.W. Cancer associated fibroblasts in cancer pathogenesis. Semin. Cell Dev. Biol. 2010, 21:33-39.
4. Kalluri R., Zeisberg M. Fibroblasts in cancer. Nat. Rev. Cancer 2006, 6:392-401.
5. Ishii G., Ochiai A., Neri S. Phenotypic and functional heterogeneity of cancer-associated fibroblast within the tumor microenvironment. Adv. Drug Deliv. Rev. 2015.
6. Neri S., Ishii G., Hashimoto H., Kuwata T., Nagai K., Date H., Ochiai A. Podoplanin-expressing cancer-associated fibroblasts lead and enhance the local invasion of cancer cells in lung adenocarcinoma. Int. J. Cancer 2015, 137:784-796.
7. Noble P.W., Barkauskas C.E., Jiang D. Pulmonary fibrosis: patterns and perpetrators. J. Clin. Investig. 2012, 122:2756-2762.
8. Scotton C.J., Chambers R.C. Molecular targets in pulmonary fibrosis: the myofibroblast in focus. Chest 2007, 132:1311-1321.
9. Li Y., Jiang D., Liang J., Meltzer E.B., Gray A., Miura R., Wogensen L., Yamaguchi Y., Noble P.W. Severe lung fibrosis requires an invasive fibroblast phenotype regulated by hyaluronan and CD44. J. Exp. Med. 2011, 208:1459-1471.
10. Lovgren A.K., Kovacs J.J., Xie T., Potts E.N., Li Y., Foster W.M., Liang J., Meltzer E.B., Jiang D., Lefkowitz R.J., Noble P.W. beta-arrestin deficiency protects against pulmonary fibrosis in mice and prevents fibroblast invasion of extracellular matrix. Sci. Transl. Med. 2011, 3:74ra23.
11. Phillips R.J., Burdick M.D., Hong K., Lutz M.A., Murray L.A., Xue Y.Y., Belperio J.A., Keane M.P., Strieter R.M. Circulating fibrocytes traffic to the lungs in response to CXCL12 and mediate fibrosis. J. Clin. Investig. 2004, 114:438-446.
12. Moffat J.G., Rudolph J., Bailey D. Phenotypic screening in cancer drug discovery-past, present and future. Nat. Rev. Drug Discov. 2014, 13:588-602.
13. Svee K., White J., Vaillant P., Jessurun J., Roongta U., Krumwiede M., Johnson D., Henke C. Acute lung injury fibroblast migration and invasion of a fibrin matrix is mediated by CD44. J. Clin. Investig. 1996, 98:1713-1727.
14. White E.S., Thannickal V.J., Carskadon S.L., Dickie E.G., Livant D.L., Markwart S., Toews G.B., Arenberg D.A. Integrin alpha4beta1 regulates migration across basement membranes by lung fibroblasts: a role for phosphatase and tensin homologue deleted on chromosome 10. Am. J. Respir. Crit. Care Med. 2003, 168:436-442.
15. Burgstaller G., Oehrle B., Koch I., Lindner M., Eickelberg O. Multiplex profiling of cellular invasion in 3D cell culture models. PloS One 2013, 8:e63121.
16. Friedrich J., Seidel C., Ebner R., Kunz-Schughart L.A. Spheroid-based drug screen: considerations and practical approach. Nat. Protoc. 2009, 4:309-324.
17. Vinci M., Gowan S., Boxall F., Patterson L., Zimmermann M., Court W., Lomas C., Mendiola M., Hardisson D., Eccles S.A. Advances in establishment and analysis of three-dimensional tumor spheroid-based functional assays for target validation and drug evaluation. BMC Biol. 2012, 10:29.
18. Wenzel C., Riefke B., Grundemann S., Krebs A., Christian S., Prinz F., Osterland M., Golfier S., Rase S., Ansari N., Esner M., Bickle M., Pampaloni F., Mattheyer C., Stelzer E.H., Parczyk K., Prechtl S., Steigemann P. 3D high-content screening for the identification of compounds that target cells in dormant tumor spheroid regions. Exp. Cell Res. 2014, 323:131-143.
19. Dolznig H., Rupp C., Puri C., Haslinger C., Schweifer N., Wieser E., Kerjaschki D., Garin-Chesa P. Modeling colon adenocarcinomas in vitro a 3D co-culture system induces cancer-relevant pathways upon tumor cell and stromal fibroblast interaction. Am. J. Pathol. 2011, 179:487-501.
20. Fang X., Sittadjody S., Gyabaah K., Opara E.C., Balaji K.C. Novel 3D co-culture model for epithelial-stromal cells interaction in prostate cancer. PloS One 2013, 8:e75187.
21. Hsiao A.Y., Torisawa Y.S., Tung Y.C., Sud S., Taichman R.S., Pienta K.J., Takayama S. Microfluidic system for formation of PC-3 prostate cancer co-culture spheroids. Biomaterials 2009, 30:3020-3027.
22. Jaganathan H., Gage J., Leonard F., Srinivasan S., Souza G.R., Dave B., Godin B. Three-dimensional in vitro co-culture model of breast tumor using magnetic levitation. Sci. Rep. 2014, 4:6468.
23. Kim J.B. Three-dimensional tissue culture models in cancer biology. Semin. Cancer Biol. 2005, 15:365-377.
24. Wang R., Xu J., Juliette L., Castilleja A., Love J., Sung S.Y., Zhau H.E., Goodwin T.J., Chung L.W. Three-dimensional co-culture models to study prostate cancer growth, progression, and metastasis to bone. Semin. Cancer Biol. 2005, 15:353-364.
25. Bozyk P.D., Moore B.B. Prostaglandin E2 and the pathogenesis of pulmonary fibrosis. Am. J. Respir. Cell Mol. Biol. 2011, 45:445-452.
26. Zhou Y., Huang X., Hecker L., Kurundkar D., Kurundkar A., Liu H., Jin T.H., Desai L., Bernard K., Thannickal V.J. Inhibition of mechanosensitive signaling in myofibroblasts ameliorates experimental pulmonary fibrosis. J. Clin. Investig. 2013, 123:1096-1108.
27. Jiang C., Huang H., Liu J., Wang Y., Lu Z., Xu Z. Fasudil, a rho-kinase inhibitor, attenuates bleomycin-induced pulmonary fibrosis in mice. Int. J. Mol. Sci. 2012, 13:8293-8307.
28. Bei Y., Hua-Huy T., Duong-Quy S., Nguyen V.H., Chen W., Nicco C., Batteux F., Dinh-Xuan A.T. Long-term treatment with fasudil improves bleomycin-induced pulmonary fibrosis and pulmonary hypertension via inhibition of Smad2/3 phosphorylation. Pulm. Pharmacol. Ther. 2013, 26:635-643.
29. Boj S.F., Hwang C.I., Baker L.A., Chio, Engle D.D., Corbo V., Jager M., Ponz-Sarvise M., Tiriac H., Spector M.S., Gracanin A., Oni T., Yu K.H., van Boxtel R., Huch M., Rivera K.D., Wilson J.P., Feigin M.E., Ohlund D., Handly-Santana A., Ardito-Abraham C.M., Ludwig M., Elyada E., Alagesan B., Biffi G., Yordanov G.N., Delcuze B., Creighton B., Wright K., Park Y., Morsink F.H., Molenaar I.Q., Borel Rinkes I.H., Cuppen E., Hao Y., Jin Y., Nijman I.J., Iacobuzio-Donahue C., Leach S.D., Pappin D.J., Hammell M., Klimstra D.S., Basturk O., Hruban R.H., Offerhaus G.J., Vries R.G., Clevers H., Tuveson D.A. Organoid models of human and mouse ductal pancreatic cancer. Cell 2015, 160:324-338.
30. Sugimoto Y., Narumiya S. Prostaglandin E receptors. J. Biol. Chem. 2007, 282:11613-11617.
31. Narumiya S., Sugimoto Y., Ushikubi F. Prostanoid receptors: structures, properties, and functions. Physiol. Rev. 1999, 79:1193-1226.
32. Regan J.W., Bailey T.J., Pepperl D.J., Pierce K.L., Bogardus A.M., Donello J.E., Fairbairn C.E., Kedzie K.M., Woodward D.F., Gil D.W. Cloning of a novel human prostaglandin receptor with characteristics of the pharmacologically defined EP2 subtype. Mol. Pharmacol. 1994, 46:213-220.
33. Griffin B.W., Magnino P.E., Pang I.H., Sharif N.A. Pharmacological characterization of an FP prostaglandin receptor on rat vascular smooth muscle cells (A7r5) coupled to phosphoinositide turnover and intracellular calcium mobilization. J. Pharmacol. Exp. Ther. 1998, 286:411-418.
34. Coleman R.A., Humphrey P.P., Kennedy I., Levy G.P., Lumley P. Comparison of the actions of U-46619, a prostaglandin H2-analogue, with those of prostaglandin H2 and thromboxane A2 on some isolated smooth muscle preparations. Br. J. Pharmacol. 1981, 73:773-778.
35. af Forselles K.J., Root J., Clarke T., Davey D., Aughton K., Dack K., Pullen N. In vitro and in vivo characterization of PF-04418948, a novel, potent and selective prostaglandin EP(2) receptor antagonist. Br. J. Pharmacol. 2011, 164:1847-1856.
36. Durocher Y., Perret S., Thibaudeau E., Gaumond M.H., Kamen A., Stocco R., Abramovitz M. A reporter gene assay for high-throughput screening of G-protein-coupled receptors stably or transiently expressed in HEK293 EBNA cells grown in suspension culture. Anal. Biochem. 2000, 284:316-326.
37. Juteau H., Gareau Y., Labelle M., Sturino C.F., Sawyer N., Tremblay N., Lamontagne S., Carriere M.C., Denis D., Metters K.M. Structure-activity relationship of cinnamic acylsulfonamide analogues on the human EP3 prostanoid receptor. Bioorg. Med. Chem. 2001, 9:1977-1984.
38. Kast R., Schirok H., Figueroa-Perez S., Mittendorf J., Gnoth M.J., Apeler H., Lenz J., Franz J.K., Knorr A., Hutter J., Lobell M., Zimmermann K., Munter K., Augstein K.H., Ehmke H., Stasch J.P. Cardiovascular effects of a novel potent and highly selective azaindole-based inhibitor of Rho-kinase. Br. J. Pharmacol. 2007, 152:1070-1080.
39. Shewan A.M., Maddugoda M., Kraemer A., Stehbens S.J., Verma S., Kovacs E.M., Yap A.S. Myosin 2 is a key Rho kinase target necessary for the local concentration of E-cadherin at cell-cell contacts. Mol. Biol. Cell 2005, 16:4531-4542.
40. Totsukawa G., Yamakita Y., Yamashiro S., Hartshorne D.J., Sasaki Y., Matsumura F. Distinct roles of ROCK (Rho-kinase) and MLCK in spatial regulation of MLC phosphorylation for assembly of stress fibers and focal adhesions in 3T3 fibroblasts. J. Cell Biol. 2000, 150:797-806.
41. Zhang X.D. A pair of new statistical parameters for quality control in RNA interference high-throughput screening assays. Genomics 2007, 89:552-561.
42. Zhang X.D. Novel analytic criteria and effective plate designs for quality control in genome-scale RNAi screens. J. Biomol. Screen. 2008, 13:363-377.
43. Kolodsick J.E., Peters-Golden M., Larios J., Toews G.B., Thannickal V.J., Moore B.B. Prostaglandin E2 inhibits fibroblast to myofibroblast transition via E. prostanoid receptor 2 signaling and cyclic adenosine monophosphate elevation. Am. J. Respir. Cell Mol. Biol. 2003, 29:537-544.
44. Molina-Molina M., Serrano-Mollar A., Bulbena O., Fernandez-Zabalegui L., Closa D., Marin-Arguedas A., Torrego A., Mullol J., Picado C., Xaubet A. Losartan attenuates bleomycin induced lung fibrosis by increasing prostaglandin E2 synthesis. Thorax 2006, 61:604-610.
45. Penke L.R., Huang S.K., White E.S., Peters-Golden M. Prostaglandin E2 inhibits alpha-smooth muscle actin transcription during myofibroblast differentiation via distinct mechanisms of modulation of serum response factor and myocardin-related transcription factor-A. J. Biol. Chem. 2014, 289:17151-17162.
46. Wilborn J., Crofford L.J., Burdick M.D., Kunkel S.L., Strieter R.M., Peters-Golden M. Cultured lung fibroblasts isolated from patients with idiopathic pulmonary fibrosis have a diminished capacity to synthesize prostaglandin E2 and to express cyclooxygenase-2. J. Clin. Investig. 1995, 95:1861-1868.
47. Ivanova V., Garbuzenko O.B., Reuhl K.R., Reimer D.C., Pozharov V.P., Minko T. Inhalation treatment of pulmonary fibrosis by liposomal prostaglandin E2. Eur. J. Pharm. Biopharm. Off. J. Arb. Pharm. Verfahr. 2013, 84:335-344.
48. Hinz B., Gabbiani G. Mechanisms of force generation and transmission by myofibroblasts. Curr. Opin. Biotechnol. 2003, 14:538-546.