Modulation of Huh7.5 spheroid formation and functionality using modified peg-based hydrogels of different stiffness

PLoS ONE

Volumn 10, Issue 2, 2015, Pages

  Lee, Bae Hoon ^a   Kim, Myung Hee ^a   Lee, Jae Ho ^a   Seliktar, Dror ^b   Lay, Nam Joon Cho ^a   Tan, Poh ^a  

^a NANYANG TECHNOLOGICAL UNIVERSITY   (Singapore)

^b TECHNION ISRAEL INSTITUTE OF TECHNOLOGY   (Israel)

Author keywords

[No Author keywords available]

Indexed keywords

ALBUMIN; CYTOCHROME P450; FIBRONECTIN; POLY(ETHYLENE GLYCOL) DIACRYLATE; POLYMER; UNCLASSIFIED DRUG; HYDROGEL; MACROGOL DERIVATIVE; POLY(ETHYLENE GLYCOL)DIACRYLATE;

ARTICLE; AUTOCRINE EFFECT; CELL ENCAPSULATION; CELL FUNCTION; CELL PROLIFERATION; CELL STIFFNESS; CELL STRUCTURE; CELL SURVIVAL; CELLULAR, SUBCELLULAR AND MOLECULAR BIOLOGICAL PHENOMENA AND FUNCTIONS; COMPLIANCE (PHYSICAL); CONFOCAL MICROSCOPY; CONTROLLED STUDY; ENZYME LINKED IMMUNOSORBENT ASSAY; HUMAN; HUMAN CELL; HYDROGEL; IMMUNOFLUORESCENCE MICROSCOPY; LIVER CIRRHOSIS; MECHANOTRANSDUCTION; PROTEIN EXPRESSION; PROTEIN SECRETION; SCANNING ELECTRON MICROSCOPY; SPHEROID CELL; CHEMISTRY; PHYSIOLOGY; TISSUE ENGINEERING; TUMOR CELL LINE;

CELL LINE, TUMOR; CELL PROLIFERATION; CELL SURVIVAL; HUMANS; HYDROGELS; MECHANOTRANSDUCTION, CELLULAR; POLYETHYLENE GLYCOLS; TISSUE ENGINEERING;

EID: 84923267262     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0118123     Document Type: Article

References (54)

1. Klatt D, Friedrich C, Korth Y, Vogt R, Braun J, et al. (2010) Viscoelastic properties of liver measured by oscillatory rheometry and multifrequency magnetic resonance elastography. Biorheology 47:133-141. doi: 10.3233/BIR-2010-0565 PMID: 20683156
2. Kamphues C, Klatt D, Bova R, Yahyazadeh A, Bahra M, et al. (2012) Viscoelasticity-based magnetic resonance elastography for the assessment of liver fibrosis in hepatitis C patients after liver transplantation. RoFo: Fortschritte auf dem Gebiete der Rontgenstrahlen und der Nuklearmedizin 184:1013-1019. doi: 10.1055/s-0032-1313126 PMID: 22893489
3. Godoy P, Hewitt NJ, Albrecht U, Andersen ME, Ansari N, et al. (2013) Recent advances in 2D and 3D in vitro systems using primary hepatocytes, alternative hepatocyte sources and non-parenchymal liver cells and their use in investigating mechanisms of hepatotoxicity, cell signaling and ADME. Archives of toxicology 87:1315-1530. doi: 10.1007/s00204-013-1078-5 PMID: 23974980
4. Wells RG (2008) The role of matrix stiffness in regulating cell behavior. Hepatology 47:1394-1400. doi: 10.1002/hep. 22193 PMID: 18307210
5. Dunn JC, Tompkins RG, Yarmush ML (1992) Hepatocytes in collagen sandwich: evidence for transcriptional and translational regulation. The Journal of cell biology 116:1043-1053. PMID: 1734019
6. Dunn JC, Tompkins RG, Yarmush ML (1993) Dynamics of transcriptional and translational processes in hepatocytes cultured in a collagen sandwich. Biotechnology and bioengineering 41:593-598. PMID: 18609591
7. Donato MT, Lahoz A, Montero S, Bonora A, Pareja E, et al. (2008) Functional assessment of the quality of human hepatocyte preparations for cell transplantation. Cell transplantation 17:1211-1219. PMID: 19181215
8. Castell JV, Jover R, Martinez-Jimenez CP, Gomez-Lechon MJ (2006) Hepatocyte cell lines: their use, scope and limitations in drug metabolism studies. Expert opinion on drug metabolism & toxicology 2:183-212. doi: 10.1517/17460441.2015.997205 PMID: 25633410
9. Wang S, Nagrath D, Chen PC, Berthiaume F, Yarmush ML (2008) Three-dimensional primary hepatocyte culture in synthetic self-assembling peptide hydrogel. Tissue engineering Part A 14:227-236. doi: 10.1089/tea.2007.0143 PMID: 18333775
10. Nelson LJ, Walker SW, Hayes PC, Plevris JN (2010) Low-shear modelled microgravity environment maintains morphology and differentiated functionality of primary porcine hepatocyte cultures. Cells, tissues, organs 192:125-140. doi: 10.1159/000308893 PMID: 20395654
11. Friedrich J, Seidel C, Ebner R, Kunz-Schughart LA (2009) Spheroid-based drug screen: considerations and practical approach. Nature protocols 4:309-324. doi: 10.1038/nprot.2008.226 PMID: 19214182
12. Chang TT, Hughes-Fulford M (2009) Monolayer and spheroid culture of human liver hepatocellular carcinoma cell line cells demonstrate distinct global gene expression patterns and functional phenotypes. Tissue engineering Part A 15:559-567. doi: 10.1089/ten. tea.2007.0434 PMID: 18724832
13. Molina-Jimenez F, Benedicto I, Dao Thi VL, Gondar V, Lavillette D, et al. (2012) Matrigel-embedded 3D culture of Huh-7 cells as a hepatocyte-like polarized system to study hepatitis C virus cycle. Virology 425:31-39. doi: 10.1016/j.virol.2011.12.021 PMID: 22280897
14. Ringel M, Von Mach MA, Santos R, Feilen PJ, Brulport M, et al. (2005) Hepatocytes cultured in alginate microspheres: an optimized technique to study enzyme induction. Toxicology 206:153-167. PMID: 15590115
15. Subramanian K, Owens DJ, Raju R, Firpo M, O'Brien TD, et al. (2014) Spheroid culture for enhanced differentiation of human embryonic stem cells to hepatocyte-like cells. Stem cells and development 23:124-131. doi: 10.1089/scd.2013.0097 PMID: 24020366
16. Hou YT, Ijima H, Matsumoto S, Kubo T, Takei T, et al. (2010) Effect of a hepatocyte growth factor/heparinimmobilized collagen system on albumin synthesis and spheroid formation by hepatocytes. Journal of Bioscience and Bioengineering 110:208-216. doi: 10.1016/j.jbiosc.2010.01.016 PMID: 20547342
17. Ananthanarayanan A, Nugraha B, Triyatni M, Hart S, Sankuratri S, et al. (2014) Scalable spheroid model of human hepatocytes for hepatitis C infection and replication. Molecular pharmaceutics 11:2106-2114. doi: 10.1021/mp500063y PMID: 24761996
18. Mahou R, Tran NM, Dufresne M, Legallais C, Wandrey C (2012) Encapsulation of Huh-7 cells within alginatepoly (ethylene glycol) hybrid microspheres. Journal of materials science Materials in medicine 23:171-179. doi: 10.1007/s10856-011-4512-3 PMID: 22160783
19. Tran NM, Dufresne M, Duverlie G, Castelain S, Defarge C, et al. (2013) An appropriate selection of a 3D alginate culture model for hepatic Huh-7 cell line encapsulation intended for viral studies. Tissue engineering Part A 19:103-113. doi: 10.1089/ten. TEA.2012.0139 PMID: 22889091
20. Fey SJ, Wrzesinski K (2012) Determination of drug toxicity using 3D spheroids constructed from an immortal human hepatocyte cell line. Toxicological sciences: an official journal of the Society of Toxicology 127:403-411. doi: 10.1093/toxsci/kfs122 PMID: 22454432
21. Georges PC, Janmey PA (2005) Cell type-specific response to growth on soft materials. Journal of applied physiology 98:1547-1553. PMID: 15772065
22. Semler EJ, Moghe PV (2001) Engineering hepatocyte functional fate through growth factor dynamics: the role of cell morphologic priming. Biotechnology and bioengineering 75:510-520. PMID: 11745126
23. Dikovsky D, Bianco-Peled H, Seliktar D (2006) The effect of structural alterations of PEG-fibrinogen hydrogel scaffolds on 3-D cellular morphology and cellular migration. Biomaterials 27:1496-1506. PMID: 16243393
24. Nguyen KT, West JL (2002) Photopolymerizable hydrogels for tissue engineering applications. Biomaterials 23:4307-4314. PMID: 12219820
25. Weber LM, He J, Bradley B, Haskins K, Anseth KS (2006) PEG-based hydrogels as an in vitro encapsulation platform for testing controlled beta-cell microenvironments. Acta Biomaterialia 2:1-8. PMID: 16701853
26. Phelps EA, Enemchukwu NO, Fiore VF, Sy JC, Murthy N, et al. (2012) Maleimide cross-linked bioactive PEG hydrogel exhibits improved reaction kinetics and cross-linking for cell encapsulation and in situ delivery. Advanced Materials 24:64-70, 62. doi: 10.1002/adma.201103574 PMID: 22174081
27. Li CY, Stevens KR, Schwartz RE, Alejandro BS, Huang JH, et al. (2014) Micropatterned Cell-Cell Interactions Enable Functional Encapsulation of Primary Hepatocytes in Hydrogel Microtissues. Tissue engineering Part A.
28. Underhill GH, Chen AA, Albrecht DR, Bhatia SN (2007) Assessment of hepatocellular function within PEG hydrogels. Biomaterials 28:256-270. PMID: 16979755
29. Williams CM, Mehta G, Peyton SR, Zeiger AS, Van Vliet KJ, et al. (2011) Autocrine-controlled formation and function of tissue-like aggregates by primary hepatocytes in micropatterned hydrogel arrays. Tissue engineering Part A 17:1055-1068. doi: 10.1089/ten. TEA.2010.0398 PMID: 21121876
30. Cho NJ, Elazar M, Xiong A, Lee W, Chiao E, et al. (2009) Viral infection of human progenitor and liverderived cells encapsulated in three-dimensional PEG-based hydrogel. Biomedical materials 4:011001. doi: 10.1088/1748-6041/25/1/011001 PMID: 18981544
31. Lee W, Cho NJ, Xiong A, Glenn JS, Frank CW (2010) Hydrophobic nanoparticles improve permeability of cell-encapsulating poly (ethylene glycol) hydrogels while maintaining patternability. Proceedings of the National Academy of Sciences of the United States of America 107:20709-20714. doi: 10.1073/pnas.1005211107 PMID: 21071674
32. Lin TY, Ki CS, Lin CC (2014) Manipulating hepatocellular carcinoma cell fate in orthogonally crosslinked hydrogels. Biomaterials 35:6898-6906. doi: 10.1016/j.biomaterials.2014.04.118 PMID: 24857292
33. Underhill GH, Chen AA, Albrecht DR, Bhatia SN (2007) Assessment of hepatocellular function within PEG hydrogels. Biomaterials 28:256-270. PMID: 16979755
34. Tay CY, Pal M, Yu H, Leong WS, Tan NS, et al. (2011) Bio-inspired micropatterned platform to steer stem cell differentiation. Small 7:1416-1421. doi: 10.1002/smll.201002298 PMID: 21495185
35. Chen CS, Mrksich M, Huang S, Whitesides GM, Ingber DE (1997) Geometric control of cell life and death. Science 276:1425-1428. PMID: 9162012
36. Yu H, Tay CY, Pal M, Leong WS, Li H, et al. (2013) A bio-inspired platform to modulate myogenic differentiation of human mesenchymal stem cells through focal adhesion regulation. Advanced healthcare materials 2:442-449. doi: 10.1002/adhm.201200142 PMID: 23184715
37. Leong WS, Tay CY, Yu H, Li A, Wu SC, et al. (2010) Thickness sensing of hMSCs on collagen gel directs stem cell fate. Biochemical and Biophysical Research Communications 401:287-292. doi: 10. 1016/j.bbrc.2010.09.052 PMID: 20851103
38. Engler AJ, Sen S, Sweeney HL, Discher DE (2006) Matrix elasticity directs stem cell lineage specification. Cell 126:677-689. PMID: 16923388
39. Lam CR, Wong HK, Nai S, Chua CK, Tan NS, et al. (2014) A 3D Biomimetic Model of Tissue Stiffness Interface for Cancer Drug Testing. Molecular pharmaceutics 11:2016-2021. doi: 10.1021/mp500059q PMID: 24754837
40. Mueller S, Sandrin L (2010) Liver stiffness: a novel parameter for the diagnosis of liver disease. Hepatic medicine: evidence and research 2:49-67.
41. Lee BH, Tin SP, Chaw SY, Cao Y, Xia Y, et al. (2014) Influence of soluble PEG-OH incorporation in a 3D cell-laden PEG-fibrinogen (PF) hydrogel on smooth muscle cell morphology and growth. Journal of biomaterials science Polymer edition 25:394-409. doi: 10.1080/09205063.2013.862401 PMID: 24304216
42. Freudenberg U, Hermann A, Welzel PB, Stirl K, Schwarz SC, et al. (2009) A star-PEG-heparin hydrogel platform to aid cell replacement therapies for neurodegenerative diseases. Biomaterials 30:5049-5060. doi: 10.1016/j.biomaterials.2009.06.002 PMID: 19560816
43. Liang Y, Jeong J, De Volder RJ, Cha C, Wang F, et al. (2011) A cell-instructive hydrogel to regulate malignancy of 3D tumor spheroids with matrix rigidity. Biomaterials 32:9308-9315. doi: 10.1016/j. biomaterials.2011.08.045 PMID: 21911252
44. Semler EJ, Lancin PA, Dasgupta A, Moghe PV (2005) Engineering hepatocellular morphogenesis and function via ligand-presenting hydrogels with graded mechanical compliance. Biotechnology and bioengineering 89:296-307. PMID: 15744840
45. Lin RZ, Chang HY (2008) Recent advances in three-dimensional multicellular spheroid culture for biomedical research. Biotechnology journal 3:1172-1184. doi: 10.1002/biot.200700228 PMID: 18566957
46. Napolitano AP, Chai P, Dean DM, Morgan JR (2007) Dynamics of the self-assembly of complex cellular aggregates on micromolded nonadhesive hydrogels. Tissue Engineering 13:2087-2094. PMID: 17518713
47. Robinson EE, Foty RA, Corbett SA (2004) Fibronectin matrix assembly regulates alpha5beta1-mediated cell cohesion. Molecular biology of the cell 15:973-981. PMID: 14718567
48. Ivascu A, Kubbies M (2007) Diversity of cell-mediated adhesions in breast cancer spheroids. International journal of oncology 31:1403-1413. PMID: 17982667
49. Lin RZ, Chou LF, Chien CC, Chang HY (2006) Dynamic analysis of hepatoma spheroid formation: roles of E-cadherin and beta1-integrin. Cell and tissue research 324:411-422. PMID: 16489443
50. Makogonenko E, Tsurupa G, Ingham K, Medved L (2002) Interaction of fibrin (ogen) with fibronectin: further characterization and localization of the fibronectin-binding site. Biochemistry 41:7907-7913. PMID: 12069579
51. Stamatoglou SC, Hughes RC, Lindahl U (1987) Rat hepatocytes in serum-free primary culture elaborate an extensive extracellular matrix containing fibrin and fibronectin. The Journal of cell biology 105:2417-2425. PMID: 3316251
52. Peshwa MV, Wu FJ, Sharp HL, Cerra FB, Hu WS (1996) Mechanistics of formation and ultrastructural evaluation of hepatocyte spheroids. In vitro cellular & developmental biology Animal 32:197-203. doi: 10.1016/j.vaccine.2015.01.041 PMID: 25637904
53. Nakazawa K, Ijima H, Fukuda J, Sakiyama R, Yamashita Y, et al. (2002) Development of a hybrid artificial liver using polyurethane foam/hepatocyte spheroid culture in a preclinical pig experiment. The International journal of artificial organs 25:51-60. PMID: 11853072
54. Khaitan D, Dwarakanath BS (2006) Multicellular spheroids as an in vitro model in experimental oncology: applications in translational medicine. Expert opinion on drug discovery 1:663-675. doi: 10.1517/17460441.1.7.663 PMID: 23495992