Capturing complex 3D tissue physiology in vitro (original) (raw)

• Lysaght, M. J. & Hazlehurst, A. L. Tissue engineering: the end of the beginning. Tissue Eng. 10, 309?320 (2004).
  Article PubMed Google Scholar
• Griffith, L. G. & Naughton, G. Tissue engineering ?current challenges and expanding opportunities. Science 295, 1009?1014 (2002).
  Article CAS PubMed Google Scholar
• Suuronen, E. J., Sheardown, H., Newman, K. D., McLaughlin, C. R. & Griffith, M. Building in vitro models of organs. Int. Rev. Cytol. 244, 137?173 (2005).
  Article CAS PubMed Google Scholar
• Sivaraman, A. et al. A microscale in vitro physiological model of the liver: predictive screens for drug metabolism and enzyme induction. Curr. Drug Metab. 6, 569?592 (2005).
  Article CAS PubMed Google Scholar
• Kuperwasser, C. et al. Reconstruction of functionally normal and malignant human breast tissues in mice. Proc. Natl Acad. Sci. USA 101, 4966?4971 (2004).
  Article CAS PubMed PubMed Central Google Scholar
• Katoh, M. et al. Expression of human phase II enzymes in chimeric mice with humanized liver. Drug Metab. Dispos. 33, 1333?1340 (2005).
  Article CAS PubMed Google Scholar
• Rangarajan, A., Hong, S. J., Gifford, A. & Weinberg, R. A. Species- and cell type-specific requirements for cellular transformation. Cancer Cell 6, 171?183 (2004).
  Article CAS PubMed Google Scholar
• Watt, F. M. Selective migration of terminally differentiating cells from the basal layer of cultured human epidermis. J. Cell Biol. 98, 16?21 (1984).
  Article CAS PubMed Google Scholar
• Louekari, K. Status and prospects of in vitro tests in risk assessment. Altern. Lab. Anim. 32, 431?435 (2004).
  CAS PubMed Google Scholar
• Knight, B. et al. Visualizing muscle cell migration in situ. Curr. Biol. 10, 576?585 (2000).
  Article CAS PubMed Google Scholar
• Roskelley, C. D., Desprez, P. Y. & Bissell, M. J. Extracellular matrix-dependent tissue-specific gene expression in mammary epithelial cells requires both physical and biochemical signal transduction. Proc. Natl Acad. Sci. USA 91, 12378?12382 (1994). Seminal work that links mammary phenotype to 3D-culture conditions.
  Article CAS PubMed PubMed Central Google Scholar
• Bissell, M. J., Rizki, A. & Mian, I. S. Tissue architecture: the ultimate regulator of breast epithelial function. Curr. Opin. Cell Biol. 15, 753?762 (2003).
  Article CAS PubMed PubMed Central Google Scholar
• Debnath, J. & Brugge, J. S. Modelling glandular epithelial cancers in three-dimensional cultures. Nature Rev. Cancer 5, 675?688 (2005).
  Article CAS Google Scholar
• Paszek, M. J. & Weaver, V. M. The tension mounts: mechanics meets morphogenesis and malignancy. J. Mammary Gland Biol. Neoplasia 9, 325?342 (2004).
  Article PubMed Google Scholar
• Wozniak, M. A., Desai, R., Solski, P. A., Der, C. J. & Keely, P. J. ROCK-generated contractility regulates breast epithelial cell differentiation in response to the physical properties of a three-dimensional collagen matrix. J. Cell Biol. 163, 583?595 (2003).
  Article CAS PubMed PubMed Central Google Scholar
• Zegers, M. M., O'Brien, L. E., Yu, W., Datta, A. & Mostov, K. E. Epithelial polarity and tubulogenesis in vitro. Trends Cell Biol. 13, 169?176 (2003).
  Article CAS PubMed Google Scholar
• Grinnell, F., Ho, C. H., Lin, Y.-C. & Skuta, G. Differences in the regulation of fibroblast contraction of floating versus stressed collagen matrices. J. Biol. Chem. 274, 918?923 (1999).
  Article CAS PubMed Google Scholar
• Zaman, M. H., Kamm, R. D., Matsudaira, P. & Lauffenburger, D. A. Computational model for cell migration in three-dimensional matrices. Biophys. J. 89, 1389?1397 (2005).
  Article CAS PubMed PubMed Central Google Scholar
• Lutolf, M. P. et al. Synthetic matrix metalloproteinase-sensitive hydrogels for the conduction of tissue regeneration: engineering cell-invasion characteristics. Proc. Natl Acad. Sci. USA 100, 5413?5418 (2003). Pioneering demonstration of how synthetic extracellular matrices can be tuned to control many facets of cell behaviour in tissue remodelling, using approaches that are accessible to the general cell-biology laboratory.
  Article CAS PubMed PubMed Central Google Scholar
• Lo, C. M., Wang, H. B., Dembo, M. & Wang, Y. L. Cell movement is guided by the rigidity of the substrate. Biophys. J. 79, 144?152 (2000).
  Article CAS PubMed PubMed Central Google Scholar
• Peyton, S. R. & Putnam, A. J. Extracellular matrix rigidity governs smooth muscle cell motility in a biphasic fashion. J. Cell Physiol. 204, 198?209 (2005).
  Article CAS PubMed Google Scholar
• Sieminski, A. L., Hebbel, R. P. & Gooch, K. J. The relative magnitudes of endothelial force generation and matrix stiffness modulate capillary morphogenesis in vitro. Exp. Cell Res. 297, 574?584 (2004).
  Article CAS PubMed Google Scholar
• Muschler, J. et al. A role for dystroglycan in epithelial polarization: loss of function in breast tumor cells. Cancer Res. 62, 7102?7109 (2002).
  CAS PubMed Google Scholar
• Paszek, M. J. et al. Tensional homeostasis and the malignant phenotype. Cancer Cell 8, 241?254 (2005). Elegant demonstration of a link between matrix mechanics and phenotype in normal and malignant mammary tissue, using a comprehensive range of innovative methods to systematically vary matrix properties in vitro to match measured in vivo properties, as well as to quantify cell responses.
  Article CAS PubMed Google Scholar
• Wozniak, M. A. & Keely, P. J. Use of three-dimensional collagen gels to study mechanotransduction in T47D breast epithelial cells. Biol. Proced. Online 7, 144?161 (2005).
  Article CAS PubMed PubMed Central Google Scholar
• Tomasek, J. J., Gabbiani, G., Hinz, B., Chaponnier, C. & Brown, R. A. Myofibroblasts and mechanoregulation of connective tissue remodelling. Nature Rev. Mol. Cell Biol. 3, 349?363 (2002).
  Article CAS Google Scholar
• Shreiber, D. I., Barocas, V. H. & Tranquillo, R. T. Temporal variations in cell migration and traction during fibroblast-mediated gel compaction. Biophys. J. 84, 4102?4114 (2003).
  Article CAS PubMed PubMed Central Google Scholar
• Tsai, K. K., Chuang, E. Y., Little, J. B. & Yuan, Z. M. Cellular mechanisms for low-dose ionizing radiation-induced perturbation of the breast tissue microenvironment. Cancer Res. 65, 6734?6744 (2005).
  Article CAS PubMed Google Scholar
• Paralkar, V. M., Vukicevic, S. & Reddi, A. H. Transforming growth factor β type 1 binds to collagen IV of basement membrane matrix: implications for development. Dev. Biol. 143, 303?308 (1991).
  Article CAS PubMed Google Scholar
• Ruhrberg, C. et al. Spatially restricted patterning cues provided by heparin-binding VEGF-A control blood vessel branching morphogenesis. Genes Dev. 16, 2684?2698 (2002). This paper showed that heparin-binding VEGF isoforms were necessary for endothelial branching, using transgenic mice that expressed only either matrix-interacting or non-interacting VEGF isoforms.
  CAS PubMed PubMed Central Google Scholar
• Tschumperlin, D. et al. Mechanotransduction through growth factor shedding into the extracellular space. Nature 429, 83?86 (2004).
  Article CAS PubMed PubMed Central Google Scholar
• Swartz, M. A. Signaling in morphogenesis: transport cues in morphogenesis. Curr. Opin. Biotech. 14, 547?550 (2003).
  Article CAS PubMed Google Scholar
• Lutolf, M. P. & Hubbell, J. A. Synthetic biomaterials as instructive extracellular microenvironments for morphogenesis in tissue engineering. Nature Biotechnol. 23, 47?55 (2005).
  Article CAS Google Scholar
• Wang, Y. L. & Pelham, R. J. Jr . Preparation of a flexible, porous polyacrylamide substrate for mechanical studies of cultured cells. Methods Enzymol. 298, 489?496 (1998).
  Article CAS PubMed Google Scholar
• Reinhart-King, C. A., Dembo, M. & Hammer, D. A. The dynamics and mechanics of endothelial cell spreading. Biophys. J. 89, 676?689 (2005).
  Article CAS PubMed PubMed Central Google Scholar
• Semler, E. J., Lancin, P. A., Dasgupta, A. & Moghe, P. V. Engineering hepatocellular morphogenesis and function via ligand-presenting hydrogels with graded mechanical compliance. Biotechnol. Bioeng. 89, 296?307 (2005).
  Article CAS PubMed Google Scholar
• Kong, H. J., Polte, T. R., Alsberg, E. & Mooney, D. J. FRET measurements of cell-traction forces and nano-scale clustering of adhesion ligands varied by substrate stiffness. Proc. Natl Acad. Sci. USA 102, 4300?4305 (2005).
  Article CAS PubMed PubMed Central Google Scholar
• Semino, C. E., Merok, J. R., Crane, G. G., Panagiotakos, G. & Zhang, S. Functional differentiation of hepatocyte-like spheroid structures from putative liver progenitor cells in three-dimensional peptide scaffolds. Differentiation 71, 262?270 (2003).
  Article CAS PubMed Google Scholar
• Kisiday, J. et al. Self-assembling peptide hydrogel fosters chondrocyte extracellular matrix production and cell division: implications for cartilage tissue repair. Proc. Natl Acad. Sci. USA 99, 9996?10001 (2002).
  Article CAS PubMed PubMed Central Google Scholar
• Raeber, G. P., Lutolf, M. P. & Hubbell, J. A. Molecularly engineered PEG hydrogels: a novel model system for proteolytically mediated cell migration. Biophys. J. 89, 1374?1388 (2005).
  Article CAS PubMed PubMed Central Google Scholar
• Maheshwari, G., Brown, G., Lauffenburger, D. A., Wells, A. & Griffith, L. G. Cell adhesion and motility depend on nanoscale RGD clustering. J. Cell Sci. 113, 1677?1686 (2000).
  CAS PubMed Google Scholar
• Coussen, F., Choquet, D., Sheetz, M. P. & Erickson, H. P. Trimers of the fibronectin cell adhesion domain localize to actin filament bundles and undergo rearward translocation. J. Cell Sci. 115, 2581?2590 (2002).
  CAS PubMed Google Scholar
• Orend, G. Potential oncogenic action of tenascin-C in tumorigenesis. Int. J. Biochem. Cell Biol. 37, 1066?1083 (2005).
  Article CAS PubMed Google Scholar
• Ehrbar, M. et al. Cell-demanded liberation of VEGF121 from fibrin implants induces local and controlled blood vessel growth. Circ. Res. 94, 1124?1132 (2004). Using protein engineering, this study showed that matrix-binding forms of growth factors led to different signalling patterns, compared with free or unbound growth factors.
  Article CAS PubMed Google Scholar
• Helm, C. E., Fleury, M. E., Zisch, A. H., Boschetti, F. & Swartz, M. A. Synergy between interstitial flow and VEGF directs capillary morphogenesis in vitro through a gradient amplification mechanism. Proc. Natl Acad. Sci. USA 44, 15779?15784 (2005).
  Article CAS Google Scholar
• Gobin, A. S. & West, J. L. Effects of epidermal growth factor on fibroblast migration through biomimetic hydrogels. Biotechnol. Prog. 19, 1781?1785 (2003).
  Article CAS PubMed Google Scholar
• Rosner, B. I., Hang, T. & Tranquillo, R. T. Schwann cell behavior in three-dimensional collagen gels: evidence for differential mechano-transduction and the influence of TGF-β1 in morphological polarization and differentiation. Exp. Neurol. 195, 81?91 (2005).
  Article CAS PubMed Google Scholar
• Kellner, K. et al. Determination of oxygen gradients in engineered tissue using a fluorescent sensor. Biotechnol. Bioeng. 80, 73?83 (2002).
  Article CAS PubMed Google Scholar
• Glicklis, R., Merchuk, J. C. & Cohen, S. Modeling mass transfer in hepatocyte spheroids via cell viability, spheroid size, and hepatocellular functions. Biotechnol. Bioeng. 86, 672?680 (2004).
  Article CAS PubMed Google Scholar
• Gebhardt, R. et al. New hepatocyte in vitro systems for drug metabolism: metabolic capacity and recommendations for application in basic research and drug development, standard operation procedures. Drug Metab. Rev. 35, 145?213 (2003).
  Article CAS PubMed Google Scholar
• Martin, Y. & Vermette, P. Bioreactors for tissue mass culture: design, characterization, and recent advances. Biomaterials 26, 7481?7503 (2005).
  Article CAS PubMed Google Scholar
• Guppy, M., Leedman, P., Zu, X. & Russell, V. Contribution by different fuels and metabolic pathways to the total ATP turnover of proliferating MCF-7 breast cancer cells. Biochem. J. 364, 309?315 (2002).
  Article CAS PubMed PubMed Central Google Scholar
• Hermitte, F., Brunet de la Grange, P., Belloc, F., Praloran, V. & Ivanovic, Z. Very low O2 concentration (0.1%) favors G0 return of dividing CD34+ cells. Stem Cells 24, 65?73 (2006).
  Article PubMed Google Scholar
• Ezashi, T., Das, P. & Roberts, R. M. Low O2 tensions and the prevention of differentiation of hES cells. Proc. Natl Acad. Sci. USA 102, 4783?4788 (2005).
  Article CAS PubMed PubMed Central Google Scholar
• Wang, D. W., Fermor, B., Gimble, J. M., Awad, H. A. & Guilak, F. Influence of oxygen on the proliferation and metabolism of adipose derived adult stem cells. J. Cell Physiol. 204, 184?191 (2005).
  Article CAS PubMed Google Scholar
• Zhao, F. et al. Effects of oxygen transport on 3-D human mesenchymal stem cell metabolic activity in perfusion and static cultures: experiments and mathematical model. Biotechnol. Prog. 21, 1269?1280 (2005).
  Article CAS PubMed Google Scholar
• Chow, D. C., Wenning, L. A., Miller, W. M. & Papoutsakis, E. T. Modeling pO2 distributions in the bone marrow hematopoietic compartment. II. Modified Kroghian models. Biophys. J. 81, 685?696 (2001).
  Article CAS PubMed PubMed Central Google Scholar
• Radisky, D. C. et al. Rac1b and reactive oxygen species mediate MMP-3-induced EMT and genomic instability. Nature 436, 123?127 (2005).
  Article CAS PubMed PubMed Central Google Scholar
• Wojciak-Stothard, B., Tsang, L. Y. & Haworth, S. G. Rac and Rho play opposing roles in the regulation of hypoxia/reoxygenation-induced permeability changes in pulmonary artery endothelial cells. Am. J. Physiol. Lung Cell Mol. Physiol. 288, L749?L760 (2005).
  Article CAS PubMed Google Scholar
• Morin, J. P., Preterre, D., Keravec, V. & Thuillez, C. Rotating wall vessel as a new in vitro shear stress generation system: application to rat coronary endothelial cell cultures. Cell Biol. Toxicol. 19, 227?242 (2003).
  Article CAS PubMed Google Scholar
• MacDonald, J. M., Wolfe, S. P., Roy-Chowdhury, I., Kubota, H. & Reid, L. M. Effect of flow configuration and membrane characteristics on membrane fouling in a novel multicoaxial hollow-fiber bioartificial liver. Ann. NY Acad. Sci. 944, 334?343 (2001).
  Article CAS PubMed Google Scholar
• Zeilinger, K. et al. Time course of primary liver cell reorganization in three-dimensional high-density bioreactors for extracorporeal liver support: an immunohistochemical and ultrastructural study. Tissue Eng. 10, 1113?1124 (2004).
  Article CAS PubMed Google Scholar
• Reddy, C. C., Niyogi, S. K., Wells, A., Wiley, H. S. & Lauffenburger, D. A. Engineering EGF for enhanced mitogenic potency. Nature Biotechnol. 14, 1696?1699 (1996).
  Article CAS Google Scholar
• Janowska-Wieczorek, A., Majka, M., Ratajczak, J. & Ratajczak, M. Z. Autocrine/paracrine mechanisms in human hematopoiesis. Stem Cells 19, 99?107 (2001).
  Article CAS PubMed Google Scholar
• Prabhu, S. D. Cytokine-induced modulation of cardiac function. Circ. Res. 95, 1140?1153 (2004).
  Article CAS PubMed Google Scholar
• Singh, A. B. & Harris, R. C. Autocrine, paracrine and juxtacrine signaling by EGFR ligands. Cell. Signal. 17, 1183?1193 (2005).
  Article CAS PubMed Google Scholar
• Janes, K. A. et al. A systems model of signaling identifies a molecular basis set for cytokine-induced apoptosis. Science 310, 1646?1653 (2005).
  Article CAS PubMed Google Scholar
• DeWitt, A. et al. Affinity regulates spatial range of EGF receptor autocrine ligand binding. Dev. Biol. 250, 305?316 (2002). Determined quantitative properties that govern tissue distribution of secreted growth factors.
  Article CAS PubMed Google Scholar
• Wiley, H. S., Shvartsman, S. Y. & Lauffenburger, D. A. Computational modeling of the EGF-receptor system: a paradigm for systems biology. Trends Cell Biol. 13, 43?50 (2003).
  Article CAS PubMed Google Scholar
• Cartmell, S. H., Porter, B. D., Garcia, A. J. & Guldberg, R. E. Effects of medium perfusion rate on cell-seeded three-dimensional bone constructs in vitro. Tissue Eng. 9, 1197?1203 (2003).
  Article CAS PubMed Google Scholar
• Chary, S. R. & Jain, R. K. Direct measurement of interstitial convection and diffusion of albumin in normal and neoplastic tissues by fluorescence photobleaching. Proc. Natl Acad. Sci. USA 86, 5385?5389 (1989).
  Article CAS PubMed PubMed Central Google Scholar
• Dafni, H., Israely, T., Bhujwalla, Z. M., Benjamin, L. E. & Neeman, M. Overexpression of vascular endothelial growth factor 165 drives peritumor interstitial convection and induces lymphatic drain: magnetic resonance imaging, confocal microscopy, and histological tracking of triple-labeled albumin. Cancer Res. 62, 6731?6739 (2002).
  CAS PubMed Google Scholar
• Gurdon, J. B. & Bourillot, P. Y. Morphogen gradient interpretation. Nature 413, 797?803 (2001).
  Article CAS PubMed Google Scholar
• Quinn, T. M., Grodzinsky, A. J., Buschmann, M. D., Kim, Y. J. & Hunziker, E. B. Mechanical compression alters proteoglycan deposition and matrix deformation around individual cells in cartilage explants. J. Cell Sci. 111, 573?583 (1998).
  CAS PubMed Google Scholar
• Garcia, A. M., Lark, M. W., Trippel, S. B. & Grodzinsky, A. J. Transport of tissue inhibitor of metalloproteinases-1 through cartilage: Contributions of fluid flow and electrical migration. J. Orthop. Res. 16, 734?742 (1998).
  Article CAS PubMed Google Scholar
• Semino, C. E., Kamm, R. D. & Lauffenburger, D. A. Autocrine EGF receptor activation mediates endothelial cell migration and vascular morphogenesis induced by VEGF under interstitial flow. Exp. Cell Res. 312, 289?298 (2006).
  CAS PubMed Google Scholar
• Swartz, M. A., Tschumperlin, D. J., Kamm, R. D. & Drazen, J. M. Mechanical stress is communicated between cell types to elicit matrix remodeling. Proc. Natl Acad. Sci. USA 98, 6180?6185 (2001).
  Article CAS PubMed PubMed Central Google Scholar
• Choe, M. M., Sporn, P. H. S. & Swartz, M. A. An in vitro airway wall model of remodeling. Am. J. Physiol. Lung Cell Physiol. 285, L427?L433 (2003).
  Article CAS Google Scholar
• Popel, A. S. & Johnson, P. C. Microcirculation and microrheology. Ann. Rev. Fluid Mech. 37, 43?69 (2005).
  Article Google Scholar
• Schmid-Schonbein, G. W. Biomechanics of microcirculatory blood perfusion. Annu. Rev. Biomed. Eng. 1, 73?102 (1999).
  Article CAS PubMed Google Scholar
• Boardman, K. C. & Swartz, M. A. Interstitial flow as a guide for lymphangiogenesis. Circ. Res. 92, 801?808 (2003).
  Article CAS PubMed Google Scholar
• Ng, C. P., Helm, C. L. & Swartz, M. A. Interstitial flow differentially stimulates blood and lymphatic endothelial cell morphogenesis in vitro. Microvasc. Res. 68, 258?264 (2004).
  Article PubMed Google Scholar
• LeCouter, J. et al. Angiogenesis-independent endothelial protection of liver: role of VEGFR-1. Science 299, 890?893 (2003).
  Article CAS PubMed Google Scholar
• Shin, V., Zebboudj, A. F. & Bostrom, K. Endothelial cells modulate osteogenesis in calcifying vascular cells. J. Vasc. Res. 41, 193?201 (2004).
  Article PubMed Google Scholar
• Matsumoto, K., Yoshitomi, H., Roussant, J. & Zaret, K. Liver organogenesis promoted by endothelial cells prior to vascular function. Science 294, 559?563 (2001).
  Article CAS PubMed Google Scholar
• Cao, Y. Emerging mechanisms of tumour lymphangiogenesis and lymphatic metastasis. Nature Rev. Cancer 5, 735?743 (2005).
  Article CAS Google Scholar
• Swartz, M. A. & Skobe, M. Lymphatic function, lymphangiogenesis, and cancer metastasis. Microsc. Res. Tech. 55, 92?99 (2001).
  Article CAS PubMed Google Scholar
• Saharinen, P., Tammela, T., Karkkainen, M. J. & Alitalo, K. Lymphatic vasculature: development, molecular regulation and role in tumor metastasis and inflammation. Trends Immunol. 25, 387?395 (2004).
  Article CAS PubMed Google Scholar
• Van Trappen, P. O. & Pepper, M. S. Lymphatic dissemination of tumour cells and the formation of micrometastases. Lancet Oncol. 3, 44?52 (2002).
  Article CAS PubMed Google Scholar
• Balkwill, F. Cancer and the chemokine network. Nature Rev. Cancer 4, 540?550 (2004).
  Article CAS Google Scholar
• Mougel, L. et al. Three-dimensional culture and multidrug resistance: effects on immune reactivity of MCF-7 cells by monocytes. Anticancer Res. 24, 935?941 (2004).
  CAS PubMed Google Scholar
• Elgert, K. D., Alleva, D. G. & Mullins, D. W. Tumor-induced immune dysfunction: The macrophage connection. J. Leukoc. Biol. 64, 275?290 (1998).
  Article CAS PubMed Google Scholar
• Wiley, H. E., Gonzalez, E. B., Maki, W., Wu, M. T. & Hwang, S. T. Expression of CC chemokine receptor-7 and regional lymph node metastasis of B16 murine melanoma. J. Natl Cancer Inst. 93, 1638?1643 (2001).
  Article CAS PubMed Google Scholar
• Patel, D. D. et al. Chemokines have diverse abilities to form solid phase gradients. Clin. Immunol. 99, 43?52 (2001).
  Article CAS PubMed Google Scholar
• Goswami, S. et al. Macrophages promote the invasion of breast carcinoma cells via a colony-stimulating factor-1/epidermal growth factor paracrine loop. Cancer Res. 65, 5278?5283 (2005). Compelling evidence of a cell-generated chemotactic gradient that operates in 3D on a heterotypic cell type.
  Article CAS PubMed Google Scholar
• Muschler, G. F., Nakamoto, C. & Griffith, L. G. Engineering principles of clinical cell-based tissue engineering. J. Bone Joint Surg. Am. 86-A, 1541?1558 (2004).
  Article Google Scholar
• Stern, R., McPherson, M. & Longaker, M. T. Histologic study of artificial skin used in the treatment of full-thickness thermal injury. J. Burn Care Rehabil. 11, 7?13 (1990).
  Article CAS PubMed Google Scholar
• Mansbridge, J., Liu, K., Patch, R., Symons, K. & Pinney, E. Three-dimensional fibroblast culture implant for the treatment of diabetic foot ulcers: metabolic activity and therapeutic range. Tissue Eng. 4, 403?414 (1998).
  Article CAS PubMed Google Scholar
• Yannas, I. V. Synthesis of tissues and organs. ChemBioChem 5, 26?39 (2004).
  Article CAS PubMed Google Scholar
• Stock, U. A. & Vacanti, J. P. Tissue engineering: current state and prospects. Annu. Rev. Med. 52, 443?451 (2001).
  Article CAS PubMed Google Scholar
• Yannas, I. V., Lee, E., Orgill, D. P., Skrabut, E. M. & Murphy, G. F. Synthesis and characterization of a model extracellular matrix that induces partial regeneration of adult mammalian skin. Proc. Natl Acad. Sci. USA 86, 933?937 (1989). Pioneering demonstration of design principles that are applied to the development of synthetic scaffolds for tissue regeneration.
  Article CAS PubMed PubMed Central Google Scholar
• Jakab, K., Neagu, A., Mironov, V., Markwald, R. R. & Forgacs, G. Engineering biological structures of prescribed shape using self-assembling multicellular systems. Proc. Natl Acad. Sci. USA 101, 2864?2869 (2004).
  Article CAS PubMed PubMed Central Google Scholar
• Tremblay, P. L., Hudon, V., Berthod, F., Germain, L. & Auger, F. A. Inosculation of tissue-engineered capillaries with the host's vasculature in a reconstructed skin transplanted on mice. Am. J. Transplant. 5, 1002?1010 (2005).
  Article PubMed Google Scholar
• Levenberg, S. et al. Engineering vascularized skeletal muscle tissue. Nature Biotechnol. 23, 879?884 (2005).
  Article CAS Google Scholar
• Tlsty, T. D. & Hein, P. W. Know thy neighbor: stromal cells can contribute oncogenic signals. Curr. Opin. Genet. Dev. 11, 54?59 (2001).
  Article CAS PubMed Google Scholar
• Jasmund, I. & Bader, A. Bioreactor developments for tissue engineering applications by the example of the bioartificial liver. Adv. Biochem. Eng. Biotechnol. 74, 99?109 (2002).
  CAS PubMed Google Scholar
• Poznansky, M. C. et al. Efficient generation of human T cells from a tissue-engineered thymic organoid. Nature Biotechnol. 18, 729?734 (2000).
  Article CAS Google Scholar
• Stachowiak, A. N., Bershteyn, A. & Irvine, D. J. Bioactive hydrogels with an ordered cellular structure combine interconnected macroporosity and robust mechanical properties. Adv. Mater. 17, 399?403 (2005). Demonstration of an innovative approach in creating synthetic scaffolds for the recreation of complex tissue behaviours in vitro.
  Article CAS Google Scholar
• Whitesides, G. M., Ostuni, E., Takayama, S., Jiang, X. & Ingber, D. E. Soft lithography in biology and biochemistry. Annu. Rev. Biomed. Eng. 3, 335?373 (2001).
  Article CAS PubMed Google Scholar
• Klebe, R. J. Cytoscribing: a method for micropositioning cells and the construction of two- and three-dimensional synthetic tissues. Exp. Cell Res. 179, 362?373 (1988).
  Article CAS PubMed Google Scholar
• Tsuda, Y. et al. The use of patterned dual thermoresponsive surfaces for the collective recovery as co-cultured cell sheets. Biomaterials 26, 1885?1893 (2005).
  Article CAS PubMed Google Scholar
• Andersson, H. & van den Berg, A. Microfabrication and microfluidics for tissue engineering: state of the art and future opportunities. Lab Chip 4, 98?103 (2004).
  Article CAS PubMed Google Scholar
• Tan, W. & Desai, T. A. Microscale multilayer cocultures for biomimetic blood vessels. J. Biomed. Mater. Res. A 72, 146?160 (2005).
  Article CAS PubMed Google Scholar
• Shin, M. et al. Endothelialized networks with a vascular geometry in microfabricated poly(dimethyl siloxane). Biomed. Microdevices 6, 269?278 (2004).
  Article CAS PubMed Google Scholar
• Weibel, D. B., Garstecki, P. & Whitesides, G. M. Combining microscience and neurobiology. Curr. Opin. Neurobiol. 15, 560?567 (2005).
  Article CAS PubMed Google Scholar
• Hansen, C. & Quake, S. R. Microfluidics in structural biology: smaller, faster em leader better. Curr. Opin. Struct. Biol. 13, 538?544 (2003).
  Article CAS PubMed Google Scholar
• Lin, F. et al. Neutrophil migration in opposing chemoattractant gradients using microfluidic chemotaxis devices. Ann. Biomed. Eng. 33, 475?482 (2005).
  Article PubMed Google Scholar
• Lu, H. et al. Microfluidic shear devices for quantitative analysis of cell adhesion. Anal. Chem. 76, 5257?5264 (2004).
  Article CAS PubMed Google Scholar
• Song, J. W. et al. Computer-controlled microcirculatory support system for endothelial cell culture and shearing. Anal. Chem. 77, 3993?3999 (2005).
  Article CAS PubMed Google Scholar
• Sin, A. et al. The design and fabrication of three-chamber microscale cell culture analog devices with integrated dissolved oxygen sensors. Biotechnol. Prog. 20, 338?345 (2004). Shows the principles of multi-compartment tissue models 'on a chip', incorporating many principles of microfabrication and microfluidics.
  Article CAS PubMed Google Scholar
• Yaakov, N., Schwartz, R. E., Hu, W.-S., Verfaillie, C. & Odde, D. J. Endothelium-mediated hepatocyte recruitment in the establishment of liver-like tissue in vitro. Tissue Eng. (in the press).
• DeLeve, L. D., Wang, X., Hu, L., McCuskey, M. K. & McCuskey, R. S. Rat liver sinusoidal endothelial cell phenotype is maintained by paracrine and autocrine regulation. Am. J. Physiol. Gastrointest. Liver Physiol. 287, G757?G763 (2004).
  Article CAS PubMed Google Scholar
• Powers, M. J. et al. Functional behavior of primary rat liver cells in a three-dimensional perfused microarray bioreactor. Tissue Eng. 8, 499?513 (2002).
  Article PubMed Google Scholar
• Powers, M. J. et al. A microfabricated array bioreactor for perfused 3D liver culture. Biotechnol. Bioeng. 78, 257?269 (2002).
  Article CAS PubMed Google Scholar
• Lin, C. Y., Kikuchi, N. & Hollister, S. J. A novel method for biomaterial scaffold internal architecture design to match bone elastic properties with desired porosity. J. Biomech. 37, 623?636 (2004).
  Article PubMed Google Scholar
• Yeong, W. Y., Chua, C. K., Leong, K. F. & Chandrasekaran, M. Rapid prototyping in tissue engineering: challenges and potential. Trends Biotechnol. 22, 643?652 (2004).
  Article CAS PubMed Google Scholar
• Sherwood, J. K. et al. A three-dimensional osteochondral composite scaffold for articular cartilage repair. Biomaterials 23, 4739?4751 (2002).
  Article CAS PubMed Google Scholar
• Bornstein, P. & Sage, E. H. Matricellular proteins: extracellular modulators of cell function. Curr. Opin. Cell Biol. 14, 608?616 (2002).
  Article CAS PubMed Google Scholar
• Sigal, S. H., Brill, S., Fiorino, A. S. & Reid, L. M. The liver as a stem cell and lineage system. Am. J. Physiol. 263, G139?G148 (1992).
  CAS PubMed Google Scholar