Nanometric self-assembling peptide layers maintain adult hepatocyte phenotype in sandwich cultures

Journal of Nanobiotechnology

Volumn 8, Issue , 2010, Pages

  Wu, Jonathan ^a   Marí Buyé, Núria ^b   Muiños, Teresa F ^b   Borrós, Salvador ^b   Favia, Pietro ^c   Semino, Carlos E ^a,b,d  

^a Massachusetts Institute of Technology Cambridge   (United States)

^b UNIVERSITAT RAMON LLULL   (Spain)

^c UNIVERSITY OF BARI   (Italy)

^d UNIVERSITY OF LEIPZIG   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

BINDING SEQUENCE; CELL MATRIX INTERACTIONS; COLLAGEN SANDWICH; CULTURE MEDIUM; DEPOSITED COATINGS; HEPATOCYTE CULTURE; HEPATOCYTES; INTEGRINS; LAMININ; LAYER THICKNESS; LIVER-SPECIFIC FUNCTIONS; METABOLIC STRESS; MICROENVIRONMENTS; NANOMETRIC RANGES; NANOMETRICS; PEPTIDE MOTIFS; POSITIVE EFFECTS; RECEPTOR BINDING; SCAFFOLD THICKNESS; SELF-ASSEMBLING PEPTIDES; TRANSFER PROBLEMS;

ARTIFICIAL ORGANS; BIOELECTRIC POTENTIALS; COLLAGEN; PEPTIDES; SCAFFOLDS;

CELL CULTURE;

ALANINE; ALBUMIN; ARGININE; ASPARTIC ACID; COLLAGEN; CYTOCHROME P450 3A2; GLYCINE; HEPATOCYTE NUCLEAR FACTOR 4ALPHA; ISOLEUCINE; LAMININ RECEPTOR; PROTEIN RAD1; SERINE; TYROSINE;

AMINO ACID SEQUENCE; ANIMAL CELL; ARTICLE; CELL ADHESION; CELL CULTURE; CONTROLLED STUDY; LIVER CELL; MALE; NONHUMAN; PHENOTYPE; PROTEIN ASSEMBLY; PROTEIN EXPRESSION; PROTEIN MOTIF; RAT; RECEPTOR BINDING; SANDWICH CULTURE;

EID: 78649921806     PISSN: None     EISSN: 14773155     Source Type: Journal    
DOI: 10.1186/1477-3155-8-29     Document Type: Article

References (62)

1. Michalopoulos GK, DeFrances MC. Liver regeneration. Science 1997, 276:60-66. 10.1126/science.276.5309.60, 9082986.
2. Kmieć Z. Cooperation of liver cells in health and disease. Adv Anat Embryol Cell Biol 2001, 161:III-XIII. 1-151.
3. Ben-Ze'ev A, Robinson GS, Bucher NL, Farmer SR. Cell-cell and cell-matrix interactions differentially regulate the expression of hepatic and cytoskeletal genes in primary cultures of rat hepatocytes. Proc Natl Acad Sci USA 1988, 85:2161-2165. 279949, 3353374.
4. Dunn JC, Yarmush ML, Koebe HG, Tompkins RG. Hepatocyte function and extracellular matrix geometry: long-term culture in a sandwich configuration. FASEB J 1989, 3:174-177.
5. Dunn JC, Tompkins RG, Yarmush ML. Long-term in vitro function of adult hepatocytes in a collagen sandwich configuration. Biotechnol Prog 1991, 7:237-245. 10.1021/bp00009a007, 1367596.
6. Berthiaume F, Moghe PV, Toner M, Yarmush ML. Effect of extracellular matrix topology on cell structure, function, and physiological responsiveness: hepatocytes cultured in a sandwich configuration. FASEB J 1996, 10:1471-1484.
7. Silva JM, Morin PE, Day SH, Kennedy BP, Payette P, Rushmore T, Yergey JA, Nicoll-Griffith DA. Refinement of an in vitro cell model for cytochrome P450 induction. Drug Metab Dispos 1998, 26:490-496.
8. Zeisberg M, Kramer K, Sindhi N, Sarkar P, Upton M, Kalluri R. De-differentiation of primary human hepatocytes depends on the composition of specialized liver basement membrane. Mol Cell Biochem 2006, 283:181-189. 10.1007/s11010-006-2677-8, 16444601.
9. Semler EJ, Moghe PV. Engineering hepatocyte functional fate through growth factor dynamics: the role of cell morphologic priming. Biotechnol Bioeng 2001, 75:510-520. 10.1002/bit.10113, 11745126.
10. Singhvi R, Kumar A, Lopez GP, Stephanopoulos GN, Wang DI, Whitesides GM, Ingber DE. Engineering cell shape and function. Science 1994, 264:696-698. 10.1126/science.8171320, 8171320.
11. Huang S, Chen CS, Ingber DE. Control of cyclin D1, p27(Kip1), and cell cycle progression in human capillary endothelial cells by cell shape and cytoskeletal tension. Mol Biol Cell 1998, 9:3179-3193. 25607, 9802905.
12. Singhvi R, Stephanopoulos G, Wang DI. Effects of substratum morphology on cell physiology. Biotechnol Bioeng 1994, 43:764-771. 10.1002/bit.260430811, 18615800.
13. Hansen LK, Hsiao C, Friend JR, Wu FJ, Bridge GA, Remmel RP, Cerra FB, Hu W. Enhanced morphology and function in hepatocyte spheroids: a model of tissue self-asembly. Tissue Eng 1998, 4:65-74.
14. Torok E, Pollok JM, Ma PX, Kaufmann PM, Dandri M, Petersen J, Burda MR, Kluth D, Perner F, Rogiers X. Optimization of hepatocyte spheroid formation for hepatic tissue engineering on three-dimensional biodegradable polymer within a flow bioreactor prior to implantation. Cells Tissues Organs 2001, 169:34-41. 10.1159/000047858, 11340259.
15. Yuasa C, Tomita Y, Shono M, Ishimura K, Ichihara A. Importance of cell aggregation for expression of liver functions and regeneration demonstrated with primary cultured hepatocytes. J Cell Physiol 1993, 156:522-530. 10.1002/jcp.1041560311, 8360258.
16. Ryan CM, Carter EA, Jenkins RL, Sterling LM, Yarmush ML, Malt RA, Tompkins RG. Isolation and long-term culture of human hepatocytes. Surgery 1993, 113:48-54.
17. Knop E, Bader A, Boker K, Pichlmayr R, Sewing KF. Ultrastructural and functional differentiation of hepatocytes under long-term culture conditions. Anat Rec 1995, 242:337-349. 10.1002/ar.1092420307, 7573981.
18. Chen HL, Wu HL, Fon CC, Chen PJ, Lai MY, Chen DS. Long-term culture of hepatocytes from human adults. J Biomed Sci 1998, 5:435-440. 10.1007/BF02255932, 9845847.
19. Pahernik SA, Thasler WE, Mueller-Hoecker J, Schildberg FW, Koebe HG. Hypothernic storage of pig hepatocytes: influence of different storage solutions and cell density. Cryobiology 1996, 33:552-566. 10.1006/cryo.1996.0059, 8893513.
20. Jensen MD, Wallach DF, Sherwood P. Diffusion in tissue cultures on gas-permeable and impermeable supports. J Theor Biol 1976, 56:443-458. 10.1016/S0022-5193(76)80085-9, 5633.
21. Bader A, Fruhauf N, Tiedge M, Drinkgern M, De BL, Borlak JT, Steinhoff G, Haverich A. Enhanced oxygen delivery reverses anaerobic metabolic states in prolonged sandwich rat hepatocyte culture. Exp Cell Res 1999, 246:221-232. 10.1006/excr.1998.4295, 9882531.
22. McLimans WF, Crouse EJ, Tunnah KV, Moore GE. Kinetics of gas diffusion in mammalian cell culture systems. I. Experimental. Biotechnology and bioengineering 1968, 10:725.
23. Bader A, Knop E, Kern A, Boker K, Fruhauf N, Crome O, Esselmann H, Pape C, Kempka G, Sewing KF. 3-D coculture of hepatic sinusoidal cells with primary hepatocytes-design of an organotypical model. Exp Cell Res 1996, 226:223-233. 10.1006/excr.1996.0222, 8660959.
24. Catapano G, De BL, Lombardi CP, Drioli E. The effect of oxygen transport resistances on the viability and functions of isolated rat hepatocytes. Int J Artif Organs 1996, 19:61-71.
25. Quintana L, Muinos TF, Genove E, Del Mar OM, Borros S, Semino CE. Early tissue patterning recreated by mouse embryonic fibroblasts in a three-dimensional environment. Tissue Eng Part A 2009, 15:45-54. 10.1089/ten.tea.2007.0296, 2809658, 19025338.
26. Garreta E, Genove E, Borros S, Semino CE. Osteogenic differentiation of mouse embryonic stem cells and mouse embryonic fibroblasts in a three-dimensional self-assembling peptide scaffold. Tissue Eng 2006, 12:2215-2227. 10.1089/ten.2006.12.2215, 16968162.
27. Genove E, Shen C, Zhang S, Semino CE. The effect of functionalized self-assembling peptide scaffolds on human aortic endothelial cell function. Biomaterials 2005, 26:3341-3351. 10.1016/j.biomaterials.2004.08.012, 15603830.
28. Semino CE, Kasahara J, Hayashi Y, Zhang S. Entrapment of migrating hippocampal neural cells in three-dimensional peptide nanofiber scaffold. Tissue Eng 2004, 10:643-655. 10.1089/107632704323061997, 15165480.
29. Semino CE. Can We Build Artificial Stem Cell Compartments?. J Biomed Biotechnol 2003, 2003:164-169. 10.1155/S1110724303208019, 400209, 12975532.
30. Kisiday J, Jin M, Kurz B, Hung H, Semino C, Zhang S, Grodzinsky AJ. Self-assembling peptide hydrogel fosters chondrocyte extracellular matrix production and cell division: implications for cartilage tissue repair. Proc Natl Acad Sci USA 2002, 99:9996-10001. 10.1073/pnas.142309999, 126613, 12119393.
31. Genove E, Schmitmeier S, Sala A, Borros S, Bader A, Griffith LG, Semino CE. Functionalized self-assembling peptide hydrogel enhance maintenance of hepatocyte activity in vitro. J Cell Mol Med 2009, 13:3387-3397. 10.1111/j.1582-4934.2009.00970.x, 19912437.
32. Graf J, Ogle RC, Robey FA, Sasaki M, Martin GR, Yamada Y, Kleinman HK. A pentapeptide from the laminin B1 chain mediates cell adhesion and binds the 67,000 laminin receptor. Biochemistry 1987, 26:6896-6900. 10.1021/bi00396a004, 2962631.
33. Nomizu M, Kuratomi Y, Song SY, Ponce ML, Hoffman MP, Powell SK, Miyoshi K, Otaka A, Kleinman HK, Yamada Y. Identification of cell binding sequences in mouse laminin gamma1 chain by systematic peptide screening. J Biol Chem 1997, 272:32198-32205. 10.1074/jbc.272.51.32198, 9405421.
34. Tsilibary EC, Reger LA, Vogel AM, Koliakos GG, Anderson SS, Charonis AS, Alegre JN, Furcht LT. Identification of a multifunctional, cell-binding peptide sequence from the a1(NC1) of type IV collagen. J Cell Biol 1990, 111:1583-1591. 10.1083/jcb.111.4.1583, 2116235, 2211826.
35. Carlisle ES, Mariappan MR, Nelson KD, Thomes BE, Timmons RB, Constantinescu A, Eberhart RC, Bankey PE. Enhancing hepatocyte adhesion by pulsed plasma deposition and polyethylene glycol coupling. Tissue Eng 2000, 6:45-52. 10.1089/107632700320883, 10941200.
36. Bhadriraju K, Hansen LK. Hepatocyte adhesion, growth and differentiated function on RGD-containing proteins. Biomaterials 2000, 21:267-272. 10.1016/S0142-9612(99)00175-1, 10646943.
37. Wang S, Nagrath D, Chen PC, Berthiaume F, Yarmush ML. Three-dimensional primary hepatocyte culture in synthetic self-assembling peptide hydrogel. Tissue Eng Part A 2008, 14:227-236. 10.1089/tea.2007.0143, 18333775.
38. d'Agostino R, Favia P, Oehr C, Wertheimer MR. Low Temperature Plasma Processing of Materials: Past, Present and Future. Plasma Processes and Polymers 2005, 2:7.
39. Palumbo F, Favia P, Vulpio M, d'Agostino R. Plasma Deposition of PEO-like films: diagnostics and process control. Plasmas and Polymers 2001, 6:163.
40. Sardella E, Gristina R, Senesi GS, d'Agostino R, Favia P. Homogeneous and micro-patterned plasma-deposited PEO-like coatings for biomedical surfaces. Plasma Processes and Polymers 2004, 1:63.
41. Gristina R, D'Aloia E, Senesi GS, Milella A, Nardulli M, Sardella E, Favia P, d'Agostino R. Increasing cell adhesion on plasma deposited fluorocarbon coatings by changing the surface topography. J Biomed Mater Res B Appl Biomater 2009, 88:139-149.
42. Sardella E, Detomaso L, Gristina R, Senesi GS, Agheli H, Sutherland DS, d'Agostino R, Favia P. Nano-structured cell-adhesive and cell-repulsive plasma-deposited coatings: chemical and topographical effects on keratinocyte adhesion. Plasma Proc. Polym 2008, 5:540.
43. Senesi GS, D'Aloia E, Gristina R, Favia P, d'Agostino R. Surface characterization of plasma deposited nano-structured fluorocarbon coatings for promoting in-vitro cell growth. Surface Sicence 2007, 601:1019.
44. Salerno S, Piscioneri A, Laera S, Morelli S, Favia P, Bader A, Drioli E, De Bartolo L. Improved functions of human hepatocytes on NH3 plasma-grafted PEEK-WC-PU membranes. Biomaterials 2009, 30:4348-4356. 10.1016/j.biomaterials.2009.04.052, 19500831.
45. De Bartolo L, Morelli S, Piscioneri A, Lopez LC, Favia P, d'Agostino R, Drioli E. Novel membranes and surface modification able to activate specific cellular responses. Biomol Eng 2007, 24:23-26. 10.1016/j.bioeng.2006.07.001, 16914370.
46. Lopez LC, Gristina R, Ceccone G, Rossi F, Favia P, d'Agostino R. Immobilization of RGD peptide on stable plasma-deposited acrylic acid coatings for biomedical devices. Surface and Coatings Technology 2005, 200:1000.
47. De Bartolo L, Morelli S, Rende M, Salerno S, Giorno L, Lopez LC, Favia P, d'Agostino R, Drioli E. Galactose derivative immobilized glow discharge processed polyethersulfone membranes maintain the liver cell metabolic activity. J Nanosci Nanotechnol 2006, 6:2344-2353. 10.1166/jnn.2006.514, 17037840.
48. Memoli B, De Bartolo L, Favia P, Morelli S, Lopez LC, Procino A, Barbieri G, Curcio E, Giorno L, Esposito P, Cozzolino M, Brancaccio D, Andreucci VE, d'Agostino R, Drioli E. Fetuin-A gene expression, synthesis and release in primary human hepatocytes cultured in a galactosylated membrane bioreactor. Biomaterials 2007, 28:4836-4844. 10.1016/j.biomaterials.2007.05.043, 17706279.
49. Palumbo F, Favia P, Rinaldi A, Vulpio M, d'Agostino RP. PE-CVD of organic thin films with controlled surface concentration of carboxylic groups. Plasmas and Polymers 1999, 4:133.
50. Detomaso L, Gristina R, d'Agostino R, Senesi GS, Favia P. Plasma deposited acrylic acid coatings: surface characterization and the attachment of 3T3 murine fibroblasts cell lines. Surf. Coat. Tech 2005, 200:1022.
51. Detomaso L, Gristina R, Senesi GS, d'Agostino R, Favia P. Stable plasma-deposited acrylic acid surfaces for cell culture applications. Biomaterials 2005, 26:3831-3841. 10.1016/j.biomaterials.2004.10.011, 15626431.
52. Mattioli-Belmonte M, Lucarini G, Virgili L, Biagini G, Detomaso L, Favia P, d'Agostino R, Gristina R, Gigante A, Bevilacqua C. Mesenchymal stem cells on plasma-deposited acrylic acid coatings: an in vitro investigation to improve biomaterial performance in bone reconstruction. J Bioact Comp Plym 2005, 20:343.
53. Francesch L, Borros S, Knoll W, Forch R. Surface reactivity of pulsed-plasma polymerized pentafluorophenyl methacrylate (PFM) toward amines and proteins in solution. Langmuir 2007, 23:3927-3931. 10.1021/la062422d, 17338554.
54. Marí-Buyé N, O'Shaughnessy S, Colominas C, Semino CE, Gleason KK, Borrós S. Functionalized, Swellable Hydrogel Layers as a Platform for Cell Studies. Advanced Functional Materials 2009, 19:1276-1286.
55. Morin O, Normand C. Long-term maintenance of hepatocyte functional activity in co-culture: requirements for sinusoidal endothelial cells and dexamethasone. J Cell Physiol 1986, 129:103-110. 10.1002/jcp.1041290115, 3531216.
56. Baffet G, Clement B, Glaise D, Guillouzo A, Guguen-Guillouzo C. Hydrocortisone modulates the production of extracellular material and albumin in long-term cocultures of adult rat hepatocytes with other liver epithelial cells. Biochem Biophys Res Commun 1982, 109:507-512. 10.1016/0006-291X(82)91750-8, 7181931.
57. Johansson S, Hook M. Substrate adhesion of rat hepatocytes: on the mechanism of attachment to fibronectin. J Cell Biol 1984, 98:810-817. 10.1083/jcb.98.3.810, 2113136, 6321520.
58. Reid LM, Gaitmaitan Z, Arias I, Ponce P, Rojkind M. Long-term cultures of normal rat hepatocytes on liver biomatrix. Ann N Y Acad Sci 1980, 349:70-76. 10.1111/j.1749-6632.1980.tb29516.x, 6939374.
59. Li ML, Aggeler J, Farson DA, Hatier C, Hassell J, Bissell MJ. Influence of a reconstituted basement membrane and its components on casein gene expression and secretion in mouse mammary epithelial cells. Proc Natl Acad Sci USA 1987, 84:136-140. 10.1073/pnas.84.1.136, 304157, 3467345.
60. De Bartolo L, Morelli S, Lopez LC, Giorno L, Campana C, Salerno S, Rende M, Favia P, Detomaso L, Gristina R, d'Agostino R, Drioli E. Biotransformation and liver-specific functions of human hepatocytes in culture on RGD-immobilized plasma-processed membranes. Biomaterials 2005, 26:4432-4441. 10.1016/j.biomaterials.2004.11.009, 15701372.
61. Powers MJ, Janigian DM, Wack KE, Baker CS, Beer SD, Griffith LG. Functional behavior of primary rat liver cells in a three-dimensional perfused microarray bioreactor. Tissue Eng 2002, 8:499-513. 10.1089/107632702760184745, 12167234.
62. Zhang S, Holmes T, Lockshin C, Rich A. Spontaneous assembly of a self-complementary oligopeptide to form a stable macroscopic membrane. Proc Natl Acad Sci USA 1993, 90:3334-3338. 10.1073/pnas.90.8.3334, 46294, 7682699.