Increasing 3D Matrix Rigidity Strengthens Proliferation and Spheroid Development of Human Liver Cells in a Constant Growth Factor Environment

Journal of Cellular Biochemistry

Volumn 117, Issue 3, 2016, Pages 708-720

  Bomo, Jérémy ^a   Ezan, Frédéric ^a   Tiaho, François ^a   Bellamri, Medjda ^a   Langouët, Sophie ^a   Theret, Nathalie ^a   Baffet, Georges ^a  

^a UNIVERSITÉ DE RENNES 1   (France)

Author keywords

BIOTRANSFORMATION; LIVER CELLS; M ATRIX STIFFNESS; PROLIFERATION

Indexed keywords

CISPLATIN; COLLAGEN GEL; CYTOCHROME P450 1A2; CYTOKERATIN 8; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; NERVE CELL ADHESION MOLECULE; COLLAGEN; CULTURE MEDIUM; GEL;

ARTICLE; BIOTRANSFORMATION; CELL CULTURE; CELL DEATH; CELL PROLIFERATION; CELL STRESS; CELL SURVIVAL; CONTROLLED STUDY; ENZYME ACTIVITY; EPITHELIUM; EXTRACELLULAR MATRIX; HOMEOSTASIS; HUMAN; HUMAN CELL; LIVER CELL; PHENOTYPE; PRIORITY JOURNAL; PROTEIN EXPRESSION; RIGIDITY; SPHEROID CELL; THREE DIMENSIONAL CELL CULTURE; TWO DIMENSIONAL CELL CULTURE; ANIMAL; CELL CULTURE TECHNIQUE; CELL DIFFERENTIATION; CHEMISTRY; CULTURE MEDIUM; GEL; HARDNESS; LIVER CIRRHOSIS; MULTICELLULAR SPHEROID; PATHOLOGY; PHYSIOLOGY; RAT; SIGNAL TRANSDUCTION; TUMOR CELL LINE;

ANIMALS; CELL CULTURE TECHNIQUES; CELL DIFFERENTIATION; CELL LINE, TUMOR; CELL PROLIFERATION; CELL SURVIVAL; COLLAGEN; CULTURE MEDIA; GELS; HARDNESS; HEPATOCYTES; HUMANS; LIVER CIRRHOSIS; MAP KINASE SIGNALING SYSTEM; RATS; SPHEROIDS, CELLULAR;

EID: 84955352678     PISSN: 07302312     EISSN: 10974644     Source Type: Journal    
DOI: 10.1002/jcb.25356     Document Type: Article

References (45)

1. Andrieux L, Langouët S, Fautrel A, Ezan F, Krauser JA, Savouret JF, Guengerich FP, Baffet G, Guillouzo A,. 2004. Aryl hydrocarbon receptor activation and cytochrome P450 1A induction by the mitogen-activated protein kinase inhibitor U0126 in hepatocytes. Mol Pharmacol 65: 934-943.
2. Baffet G, Loyer P, Glaise D, Corlu A, Etienne PL, Guguen-Guillouzo C,. 1991. Distinct effects of cell-cell communication and corticosteroids on the synthesis and distribution of cytokeratins in cultured rat hepatocytes. J Cell Sci 99 (Pt 3): 609-615.
3. Bessard A, Frémin C, Ezan F, Coutant A, Baffet G,. 2007. MEK/ERK-dependent uPAR expression is required for motility via phosphorylation of P70S6K in human hepatocarcinoma cells. J Cell Physiol 212: 526-536.
4. Bessard A, Frémin C, Ezan F, Fautrel A, Gailhouste L, Baffet G,. 2008. RNAi-mediated ERK2 knockdown inhibits growth of tumor cells in vitro and in vivo. Oncogene 27: 5315-5325.
5. Bourbonnais E, Raymond V-A, Ethier C, Nguyen BN, El-Leil MS, Meloche S, Bilodeau M,. 2012. Liver fibrosis protects mice from acute hepatocellular injury. Gastroenterology 142: 130-139.
6. Burke MD, Mayer RT,. 1983. Differential effects of phenobarbitone and 3-methylcholanthrene induction on the hepatic microsomal metabolism and cytochrome P-450-binding of phenoxazone and a homologous series of its n-alkyl ethers (alkoxyresorufins). Chem Biol Interact 45: 243-258.
7. Campagnola PJ, Millard AC, Terasaki M, Hoppe PE, Malone CJ, Mohler WA,. 2002. Three-dimensional high-resolution second-harmonic generation imaging of endogenous structural proteins in biological tissues. Biophys J 82: 493-508.
8. Chen X, Nadiarynkh O, Plotnikov S, Campagnola PJ,. 2012. Second harmonic generation microscopy for quantitative analysis of collagen fibrillar structure. Nat Protoc 7: 654-669.
9. Darnell M, Ulvestad M, Ellis E, Weidolf L, Andersson TB,. 2012. In vitro evaluation of major in vivo drug metabolic pathways using primary human hepatocytes and HepaRG cells in suspension and a dynamic three-dimensional bioreactor system. J Pharmacol Exp Ther 343: 134-144.
10. Fassett J, Tobolt D, Hansen LK,. 2006. Type I collagen structure regulates cell morphology and EGF signaling in primary rat hepatocytes through cAMP-dependent protein kinase A. Mol Biol Cell 17: 345-356.
11. Frémin C, Bessard A, Ezan F, Gailhouste L, Régeard M, Le Seyec J, Gilot D, Pagès G, Pouysségur J, Langouët S, Baffet G,. 2009. Multiple division cycles and long-term survival of hepatocytes are distinctly regulated by extracellular signal-regulated kinases ERK1 and ERK2. Hepatology 49: 930-939.
12. Frémin C, Ezan F, Boisselier P, Bessard A, Pagès G, Pouysségur J, Baffet G,. 2007. ERK2 but not ERK1 plays a key role in hepatocyte replication: An RNAi-mediated ERK2 knockdown approach in wild-type and ERK1 null hepatocytes. Hepatology 45: 1035-1045.
13. Frémin C, Ezan F, Guegan J-P, Gailhouste L, Trotard M, Le Seyec J, Rageul J, Theret N, Langouët S, Baffet G,. 2012. The complexity of ERK1 and ERK2 MAPKs in multiple hepatocyte fate responses. J Cell Physiol 227: 59-69.
14. Gailhouste L, Ezan F, Bessard A, Frémin C, Rageul J, Langouët S, Baffet G,. 2010. RNAi-mediated MEK1 knock-down prevents ERK1/2 activation and abolishes human hepatocarcinoma growth in vitro and in vivo. Int J Cancer 126: 1367-1377.
15. Gauderon R, Lukins PB, Sheppard CJ,. 2001a. Optimization of second-harmonic generation microscopy. Micron 32: 691-700.
16. Gauderon R, Lukins PB, Sheppard CJ,. 2001b. Simultaneous multichannel nonlinear imaging: Combined two-photon excited fluorescence and second-harmonic generation microscopy. Micron 32: 685-689.
17. Georges PC, Hui J-J, Gombos Z, McCormick ME, Wang AY, Uemura M, Mick R, Janmey PA, Furth EE, Wells RG,. 2007. Increased stiffness of the rat liver precedes matrix deposition: Implications for fibrosis. Am J Physiol Gastrointest Liver Physiol 293: G1147-G1154.
18. Godoy P, Hengstler JG, Ilkavets I, Meyer C, Bachmann A, Müller A, Tuschl G, Mueller SO, Dooley S,. 2009. Extracellular matrix modulates sensitivity of hepatocytes to fibroblastoid dedifferentiation and transforming growth factor beta-induced apoptosis. Hepatol Baltim Md 49: 2031-2043.
19. Gómez-Lechón MJ, Jover R, Donato T, Ponsoda X, Rodriguez C, Stenzel KG, Klocke R, Paul D, Guillén I, Bort R, Castell JV,. 1998. Long-term expression of differentiated functions in hepatocytes cultured in three-dimensional collagen matrix. J Cell Physiol 177: 553-562.
20. Grinnell F, Petroll WM,. 2010. Cell motility and mechanics in three-dimensional collagen matrices. Annu Rev Cell Dev Biol 26: 335-361.
21. Guégan J-P, Ezan F, Théret N, Langouët S, Baffet G,. 2013. MAPK signaling in cisplatin-induced death: Predominant role of ERK1 over ERK2 in human hepatocellular carcinoma cells. Carcinogenesis 34: 38-47.
22. Guégan J-P, Frémin C, Baffet G,. 2012. The MAPK MEK1/2-ERK1/2 pathway and its implication in hepatocyte cell cycle control. Int J Hepatol 328372. doi: 10.1155/2012/328372
23. Guguen-Guillouzo C. 2002. Isolation and culture of animal and human hepatocytes, in: Freshney, R.I., Freshney, ry G. (Eds.), Culture of epithelial cells. John Wiley & Sons, Inc., pp. 337-379.
24. Gunness P, Mueller D, Shevchenko V, Heinzle E, Ingelman-Sundberg M, Noor F,. 2013. 3D organotypic cultures of human HepaRG cells: A tool for in vitro toxicity studies. Toxicol Sci Off J Soc Toxicol 133: 67-78.
25. Kholodenko BN, Hancock JF, Kolch W,. 2010. Signalling ballet in space and time. Nat Rev Mol Cell Biol 11: 414-426.
26. König K,. 2000. Multiphoton microscopy in life sciences. J Microsc 200: 83-104.
27. Kornek M, Raskopf E, Tolba R, Becker U, Klöckner M, Sauerbruch T, Schmitz V,. 2008. Accelerated orthotopic hepatocellular carcinomas growth is linked to increased expression of pro-angiogenic and prometastatic factors in murine liver fibrosis. Liver Int Off J Int Assoc Study Liver 28: 509-518.
28. Kostadinova R, Boess F, Applegate D, Suter L, Weiser T, Singer T, Naughton B, Roth A,. 2013. A long-term three dimensional liver co-culture system for improved prediction of clinically relevant drug-induced hepatotoxicity. Toxicol Appl Pharmacol 268: 1-16.
29. Lee UE, Friedman SL,. 2011. Mechanisms of hepatic fibrogenesis. Best Pract Res Clin Gastroenterol 25: 195-206.
30. Lefloch R, Pouysségur J, Lenormand P,. 2008. Single and combined silencing of ERK1 and ERK2 reveals their positive contribution to growth signaling depending on their expression levels. Mol Cell Biol 28: 511-527.
31. Leite SB, Wilk-Zasadna I, Zaldivar JM, Airola E, Reis-Fernandes MA, Mennecozzi M, Guguen-Guillouzo C, Chesne C, Guillou C, Alves PM, Coecke S,. 2012. Three-dimensional HepaRG model as an attractive tool for toxicity testing. Toxicol Sci Off J Soc Toxicol 130: 106-116.
32. Lupsor Platon M, Stefanescu H, Feier D, Maniu A, Badea R,. 2013. Performance of unidimensional transient elastography in staging chronic hepatitis C. Results from a cohort of 1,202 biopsied patients from one single center. J Gastrointest Liver Dis JGLD 22: 157-166.
33. Lutolf MP, Hubbell JA,. 2005. Synthetic biomaterials as instructive extracellular microenvironments for morphogenesis in tissue engineering. Nat Biotechnol 23: 47-55.
34. Masuzaki R, Tateishi R, Yoshida H, Goto E, Sato T, Ohki T, Imamura J, Goto T, Kanai F, Kato N, Ikeda H, Shiina S, Kawabe T, Omata M,. 2009. Prospective risk assessment for hepatocellular carcinoma development in patients with chronic hepatitis C by transient elastography. Hepatology 49: 1954-1961.
35. Meli L, Jordan ET, Clark DS, Linhardt RJ, Dordick JS,. 2012. Influence of a three-dimensional, microarray environment on human cell culture in drug screening systems. Biomaterials 33: 9087-9096.
36. Moll R, Franke WW, Schiller DL, Geiger B, Krepler R,. 1982. The catalog of human cytokeratins: Patterns of expression in normal epithelia, tumors and cultured cells. Cell 31: 11-24.
37. Morel-Chany E, Guillouzo C, Trincal G, Szajnert MF,. 1978. "Spontaneous" neoplastic transformation in vitro of epithelial cell strains of rat liver: Cytology, growth and enzymatic activities. Eur J Cancer 14: 1341-1352.
38. Paszek MJ, Weaver VM,. 2004. The tension mounts: Mechanics meets morphogenesis and malignancy. J Mammary Gland Biol Neoplasia 9: 325-342.
39. Paszek MJ, Zahir N, Johnson KR, Lakins JN, Rozenberg GI, Gefen A, Reinhart-King CA, Margulies SS, Dembo M, Boettiger D, Hammer DA, Weaver VM,. 2005. Tensional homeostasis and the malignant phenotype. Cancer Cell 8: 241-254.
40. Provenzano PP, Inman DR, Eliceiri KW, Knittel JG, Yan L, Rueden CT, White JG, Keely PJ,. 2008. Collagen density promotes mammary tumor initiation and progression. BMC Med 6: 11.
41. Schrader J, Gordon-Walker TT, Aucott RL, van Deemter M, Quaas A, Walsh S, Benten D, Forbes SJ, Wells RG, Iredale JP,. 2011. Matrix stiffness modulates proliferation, chemotherapeutic response, and dormancy in hepatocellular carcinoma cells. Hepatology 53: 1192-1205.
42. Wallace K, Burt AD, Wright MC,. 2008. Liver fibrosis. Biochem J 411: 1-18.
43. Wang HB, Dembo M, Wang YL,. 2000. Substrate flexibility regulates growth and apoptosis of normal but not transformed cells. Am J Physiol Cell Physiol 279: C1345-C1350.
44. Yang M-C, Chang C-P, Lei H-Y,. 2010. Induction of liver fibrosis in a murine hepatoma model by thioacetamide is associated with enhanced tumor growth and suppressed antitumor immunity. Lab Investig J Tech Methods Pathol 90: 1782-1793.
45. Zipfel WR, Williams RM, Webb WW,. 2003. Nonlinear magic: multiphoton microscopy in the biosciences. Nat Biotechnol 21: 1369-1377.