Advances in Regenerative Medicine: Role of Nanotechnology, and Engineering Principles pp 115-129 | Cite as
Biomimetic Approaches to Design of Tissue Engineering Bioreactors
- 986 Downloads
Abstract
Tissue engineering is an attractive strategy to address the increasing clinical need for tissue replacement. Engineered tissues can also serve as high-fidelity models for studies of development, disease and therapeutic modalities. Cultivation of three-dimensional tissue equivalents is necessarily based on the use of bioreactors, which are designed to provide controlled steady state cultivation conditions as well as required biochemical and physical regulatory signals. In this chapter, we review the design and operation of tissue engineering bioreactors, with the focus on biomimetic approaches to provide in vivo-like environments for rapid and orderly tissue development by cells cultured on a scaffold. Specifically, we focus on bioreactors for tissue engineering of two distinctly different tissues – articular cartilage and myocardium.
Keywords
Tissue engineering Cartilage Myocardium Bioreactor Oxygen transport Mechanical stimulationNotes
Acknowledgements
The authors would like to acknowledge funding of their research was funded by the Ministry of Science of the Republic of Serbia, grant 142075, Swiss National Science Foundation, grant IB73B0-111016/1 (BO), NIH grants P41 EB002520-01, R01 DE016525 and R01 HL076485-01 (GV), and ARTEC and NSERC Discovery Grant (MR).
References
- Akins RE, Boyce RA, Madonna ML, Schroedl NA, Gonda SR, McLaughlin TA, Hartzell CR (1999) Cardiac organogenesis in vitro: reestablishment of three-dimensional tissue architecture by dissociated neonatal rat ventricular cells. Tissue Eng 5:103–118CrossRefGoogle Scholar
- Ateshian GA, Hung CT (2003) Functional properties of native articular cartilage. In: Guilak F, Butler DL, Goldstein SA, Mooney DJ (eds) Functional tissue engineering. Springer, New York, pp 46–68CrossRefGoogle Scholar
- Brilla CG, Maisch B, Rupp H, Sunck R, Zhou G, Weber KT (1995) Pharmacological modulation of cardiac fibroblast function. Herz 20:127–135Google Scholar
- Buckwalter JA, Mankin HJ (1997) Articular cartilage, part II: degeneration and osteoarthrosis, repair, regeneration, and transplantation. J Bone Joint Surg Am 79A:612–632Google Scholar
- Buckwalter JA, Mankin HJ (1998) Articular cartilage: degeneration and osteoarthritis, repair, regeneration, and transplantation. Instr Course Lect 47:487–504Google Scholar
- Bugarski B, Li Q, Goosen MFA (1994) Electrostatic droplet generation: mechanism of polymer droplet formation. AIChE J 40:1026–1031CrossRefGoogle Scholar
- Bugarski D, Obradovic B, Petakov M, Jovcic G, Stojanovic N, Bugarski B (2005) Alginate microbeads as potential support for cultivation of bone marrow stromal cells. In: Uskokovic DP, Milonjic SK, Rakovic DI (eds) Materials science forum, vol. 494. Progress in advanced materials processes. Trans Tech Publications Ltd, Zurich, pp 525–530Google Scholar
- Bursac N, Papadaki M, Cohen RJ, Schoen FJ, Eisenberg SR, Carrier R, Vunjak-Novakovic G, Freed LE (1999) Cardiac muscle tissue engineering: toward an in vitro model for electrophysiological studies. Am J Physiol Heart Circ Physiol 277:H433–H444Google Scholar
- Carrier RL, Papadaki M, Rupnick M, Schoen FJ, Bursac N, Langer R, Freed LE, Vunjak-Novakovic G (1999) Cardiac tissue engineering: cell seeding, cultivation parameters and tissue construct characterization. Biotechnol Bioeng 64:580–589CrossRefGoogle Scholar
- Carrier RL, Rupnick M, Langer R, Schoen FJ, Freed LE, Vunjak-Novakovic G (2002a) Effects of oxygen on engineered cardiac muscle. Biotechnol Bioeng 78:617–625CrossRefGoogle Scholar
- Carrier RL, Rupnick M, Langer R, Schoen FJ, Freed LE, Vunjak-Novakovic G (2002b) Perfusion improves tissue architecture of engineered cardiac muscle. Tissue Eng 8:175–188CrossRefGoogle Scholar
- Chao PhG, Grayson W, Vunjak-Novakovic G (2007) Engineering cartilage and bone using human mesenchymal stem cells. J Orthop Sci 12:398–404CrossRefGoogle Scholar
- Connold AL, Frischknecht R, Dimitrakos M, Vrbova G (1997) The survival of embryonic cardiomyocytes transplanted into damaged host myocardium. J Muscle Res Cell Motil 18:63–70CrossRefGoogle Scholar
- Demarteau O, Jakob M, Schafer D, Heberer M, Martin I (2003a) Development and validation of a bioreactor for physical stimulation of engineered cartilage. Biorheology 40:331–336Google Scholar
- Demarteau O, Wendt D, Braccini A, Jakob M, Schafer D, Heberer M, Martin I (2003b) Dynamic compression of cartilage constructs engineered from expanded human articular chondrocytes. Biochem Biophys Res Commun 310:580–588CrossRefGoogle Scholar
- Einhorn TA (1998) The cell and molecular biology of fracture healing. Clin Orthop 355S:S7–S21CrossRefGoogle Scholar
- Eschenhagen T, Fink C, Remmers U, Scholz H, Wattchow J, Woil J, Zimmermann WD, Schafer H, Bishopric N, Wakatsuki T, Elson E (1997) Three-dimensional reconstitution of embryonic cardiomyocytes in a collagen matrix: a new heart model system. FASEB J 11:683–694Google Scholar
- Fink C, Ergun S, Kralisch D, Remmers U, Weil J, Eschenhagen T (2000) Chronic stretch of engineered heart tissue induces hypertrophy and functional improvement. FASEB J 14:669–679Google Scholar
- Fournier RL (1998) Basic transport phenomena in biomedical engineering. Taylor & Francis, Philadelphia, PAGoogle Scholar
- Freed LE, Vunjak-Novakovic G (2000a) Tissue engineering bioreactors. In: Lanza RP, Langer R, Vacanti J (eds) Principles of tissue engineering. Academic, Boston, MA, pp 143–156CrossRefGoogle Scholar
- Freed LE, Vunjak-Novakovic G (2000b) Tissue engineering of cartilage. In: Bronzino JD (ed) The biomedical engineering handbook. CRC Press, Boca Raton, FL, pp 124-1–124-26Google Scholar
- Freed LE, Marquis JC, Vunjak-Novakovic G, Emmanual J, Langer R (1994a) Composition of cell-polymer cartilage implants. Biotechnol Bioeng 43:605–614CrossRefGoogle Scholar
- Freed LE, Vunjak-Novakovic G, Biron R, Eagles D, Lesnoy D, Barlow S, Langer R (1994b) Biodegradable polymer scaffolds for tissue engineering. Biotechnology 12:689–693CrossRefGoogle Scholar
- Freshney RI, Obradovic B, Grayson W, Cannizzaro C, Vunjak-Novakovic G (2007) Principles of tissue culture and bioreactor design. In: Lanza RP, Langer R, Vacanti J (eds) Principles of tissue engineering. Elsevier, San Deigo, CA, pp 155–183CrossRefGoogle Scholar
- Gray ML, Pizzanelli AM, Lee RC, Grodzinsky AJ, Swann DA (1989) Kinetics of the chondrocyte biosynthetic response to compressive load and release. Biochim Biophys Acta 991:415–425CrossRefGoogle Scholar
- Grodzinsky AJ, Levenston ME, Jin M, Frank EH (2000) Cartilage tissue remodeling in response to mechanical forces. Annu Rev Biomed Eng 2:691–713CrossRefGoogle Scholar
- Grunder T, Gaissmaier C, Fritz S, Stoop R, Hortschansky P, Mollenhauer J, Aicher WK (2004) Bone morphogenetic protein (BMP)-2 enhances the expression of type II collagen and aggrecan in chondrocytes embedded in alginate beads. Osteoarthrytis Cartilage 12:559–567CrossRefGoogle Scholar
- Kiviranta I, Tammi M, Jurvelin J, Saamanen AM, Helminen HJ (1988) Moderate running exercise augments glycosaminoglycans and thickness of articular cartilage in the knee joint of young beagle dogs. J Orthop Res 6:188–195CrossRefGoogle Scholar
- Kraft MP, Riess JG, Weers JG (1998) The design and engineering of oxygen-delivering fluorocarbon emulsions. In: Benita S (ed) Submicron emulsions in drug targeting and delivery. Harwood Academic Publishers, Amsterdam, pp 235–333Google Scholar
- Leor J, Aboulafia-Etzion S, Dar A, Shapiro L, Barbash IM, Battler A, Granot Y, Cohen S (2000) Bioengineered cardiac grafts: a new approach to repair the infarcted myocardium? Circulation 102:III56–III61CrossRefGoogle Scholar
- Li R-K, Jia ZQ, Weisel RD, Mickle DAG, Choi A, Yau TM (1999) Survival and function of bioengineered cardiac grafts. Circulation 100:II63–II69Google Scholar
- Li R-K, Yau TM, Weisel RD, Mickle DAG, Sakai T, Choi A, Jia ZQ (2000) Construction of a bioengineered cardiac graft. J Thorac Cardiovasc Surg 119:368–375CrossRefGoogle Scholar
- MacKenna DA, Omens JH, McCulloch AD, Covell JW (1994) Contribution of collagen matrix to passive left ventricular mechanics in isolated rat heart. Am J Physiol 266:H1007–H1018Google Scholar
- Manojlovic V, Djonlagic J, Obradovic B, Nedovic V, Bugarski B (2006) Investigation of cell immobiliyation in alginate: rheological and electrostatic extrusion studies. J Chem Technol Biotechnol 81:505–510CrossRefGoogle Scholar
- Martin I, Obradovic B, Treppo S, Grodzinsky AJ, Langer R, Freed LE, Vunjak-Novakovic G (2000) Modulation of the mechanical properties of tissue engineered cartilage. Biorheology 37:141–147Google Scholar
- Masuda K, Sah R, Hejna M, Thonar EJ-MA (2003) A novel two–step method for the formation of tissue–engineered cartilage by mature bovine chondrocytes: the alginate–recovered–chondrocyte (ARC) method. J Orthop Res 21:139–148CrossRefGoogle Scholar
- Mauck RL, Soltz MA, Wang CCB, Wong DD, Chao PG, Valhmu WB, Hung CT, Ateshian GA (2000) Functional tissue engineering of articular cartilage through dynamic loading of chondrocyte-seeded agarose gels. J Biomech Eng 122:252–260CrossRefGoogle Scholar
- Mauck RL, Seyhan SL, Ateshian GA, Hung CT (2002) Influence of seeding density and dynamic deformational loading on the developing structure/function relationships of chondrocyte-seeded agarose hydrogels. Ann Biomed Eng 30:1046–1056CrossRefGoogle Scholar
- Mauck RL, Nicoll SB, Seyhan SL, Ateshian GA, Hung CT (2003a) Synergistic action of growth factors and dynamic loading for articular cartilage tissue engineering. Tissue Eng 9:597–611CrossRefGoogle Scholar
- Mauck RL, Wang CC-B, Oswald ES, Ateshian GA, Hung CT (2003b) The role of cell seeding density and nutrient supply for articular cartilage tissue engineering with deformational loading. Osteoarthritis Cartilage 11:879–890CrossRefGoogle Scholar
- Mauck RL, Byers BA, Yuan X, Rackwitz L, Tuan RS (2006) Cartilage tissue engineering with MSC-laden hydrogels: effect of seeding density, exposure to chondrognic medium and loading. 52nd Annual Meeting of the Orthopaedic Research Society, Chicago, Illinois, 19–22 March 2006, Paper No: 0336Google Scholar
- O’Driscoll SW (2001) Preclinical cartilage repair: current status and future perspectives. Clin Orthop 391(Suppl):S397–S401Google Scholar
- O’Hara BP, Urban JPG, Maroudas A (1990) Influence of cyclic loading on the nutrition of articular cartilage. Ann Rheum Dis 49:536–539CrossRefGoogle Scholar
- Obradovic B, Carrier RL, Vunjak-Novakovic G, Freed LE (1999) Gas exchange is essential for bioreactor cultivation of tissue engineered cartilage. Biotechnol Bioeng 63:197–205CrossRefGoogle Scholar
- Obradovic B, Meldon JH, Freed LE, Vunjak-Novakovic G (2000) Glycosaminoglycan deposition in engineered cartilage: experiments and mathematical model. AIChE J 46:1860–1871CrossRefGoogle Scholar
- Obradovic B, Martin I, Freed LE, Vunjak-Novakovic G (2001) Bioreactor studies of natural and tissue engineered cartilage. Ortop Traumatol Rehabil 3:181–189Google Scholar
- Obradovic B, Bugarski D, Petakov M, Jovcic G, Stojanovic N, Bugarski B, Vunjak-Novakovic G (2004) Cell support studies aimed for cartilage tissue engineering in perfused bioreactors. In: Uskokovic DP, Milonjic SK, Rakovic DI (eds) Materials science forum, vol. 453–454. Progress in advanced materials processes. Trans Tech Publications Ltd, Zurich, pp 549–555Google Scholar
- Obradovic B, Radisic M, Vunjak-Novakovic G (2005) Tissue engineering of cartilage and myocardium. In: Nedovic V, Willaert RG (eds) Focus on biotechnology, vol. 8b. Applications of cell immobilisation biotechnology. Springer, Dordrecht/Berlin/Heidelberg/New York, pp 99–133Google Scholar
- Obradovic B, Osmokrovic A, Bugarski B, Bugarski D, Vunjak-Novakovic G (2007) Alginate microbeads as cell support for cartilage tissue engineering: bioreactor studies. In: Uskokovic DP, Milonjic SK, Rakovic DI (eds) Materials science forum, vol. 555. Progress in advanced materials processes. Trans Tech Publications Ltd, Zurich, pp 417–422Google Scholar
- Osmokrovic A, Obradovic B, Bugarski D, Bugarski B, Vunjak-Novakovic G (2006) Development of a packed bed bioreactor for cartilage tissue engineering. FME Trans 34:65–70Google Scholar
- Palmoski M, Perricone E, Brandt KD (1979) Development and reversal of a proteoglycan aggregation defect in normal canine knee cartilage after immobilization. Arthritis Rheum 22:508–517CrossRefGoogle Scholar
- Papadaki M, Bursac N, Langer R, Merok J, Vunjak-Novakovic G, Freed LE (2001) Tissue engineering of functional cardiac muscle: molecular, structural and electrophysiological studies. Am J Physiol Heart Circ Physiol 280:H168–H178Google Scholar
- Parkkinen JJ, Ikonen J, Lammi MJ, Laakkonen J, Tammi M, Helminen HJ (1993) Effects of cyclic hydrostatic pressure on proteoglycan synthesis in cultured chondrocytes and articular cartilage explants. Arch Biochem Biophys 300:458–465CrossRefGoogle Scholar
- Pei M, Solchaga LA, Seidel J, Zeng L, Vunjak-Novakovic G, Caplan AI, Freed LE (2002) Bioreactors mediate the effectiveness of tissue engineering scaffolds. FASEB J 16:1691–1694Google Scholar
- Petrovic M, Mitrakovic D, Bugarski B, Vonwil D, Martin I, Obradovic B (2009) A novel bioreactor with mechanical stimulation for skeletal tissue engineering. CI&CEQ 15:41–44CrossRefGoogle Scholar
- Poncelet D, Babak VG, Neufeld RJ, Goosen M, Bugarski B (1999) Theory of electrostatic dispersion of polymer solutions in the production of microgel beads containing biocatalyst. Adv Colloid Interface Sci 79:213–228CrossRefGoogle Scholar
- Radisic M, Euloth M, Yang L, Langer R, Freed LE, Vunjak-Novakovic G (2003) High density seeding of myocyte cells for tissue engineering. Biotechnol Bioeng 82:403–414CrossRefGoogle Scholar
- Radisic M, Yang L, Boublik J, Cohen RJ, Langer R, Freed LE, Vunjak-Novakovic G (2004) Medium perfusion enables engineering of compact and contractile cardiac tissue. Am J Physiol Heart Circ Physiol 286:H507–H516CrossRefGoogle Scholar
- Radisic M, Obradovic B, Vunjak-Novakovic G (2005) Functional tissue engineering of cartilage and myocardium: bioreactor aspects. In: Ma PX, Elisseeff J (eds) Scaffolding in tissue engineering. Marcel Dekker, New York, pp 491–520Google Scholar
- Radisic M, Malda J, Epping E, Geng W, Langer R, Vunjak-Novakovic G (2006a) Oxygen gradients correlate with cell density and cell viability in engineered cardiac tissue. Biotechnol Bioeng 93:332–343CrossRefGoogle Scholar
- Radisic M, Park H, Chen F, Salazar-Lazzaro JE, Wang Y, Dennis RG, Langer R, Freed LE, Vunjak-Novakovic G (2006b) Biomimetic approach to cardiac tissue engineering: oxygen carriers and channeled scaffolds. Tissue Eng 12:1–15CrossRefGoogle Scholar
- Radisic M, Cannizzaro C, Vunjak-Novakovic G (2006c) Scaffolds and fluid flow in cardiac tissue engineering. FDMP: Fluid Dynamics Mater Process 2:1–15Google Scholar
- Radisic M, Park H, Gerecht-Nir S, Cannizzaro C, Langer R, Vunjak-Novakovic G (2007) Biomimetic approach to cardiac tissue engineering. Phil Trans R Soc B 362:1357–1368CrossRefGoogle Scholar
- Radisic M, Park H, Salazar-Lazaro JE, Wang Y, Langer R, Freed LE, Vunjak-Novakovic G (2008) Pretreatment of synthetic elastomeric scaffolds by cardiac fibroblasts improves engineered heart tissue. J Biomed Mater Res A 86:713–724Google Scholar
- Saamanen AM, Tammi M, Kiviranta I, Jurvelin J, Helminen HJ (1987) Maturation of proteoglycan matrix in articular cartilage under increased and decreased joint loading. A study in young rabbits. Connect Tissue Res 16:163–175CrossRefGoogle Scholar
- Sah RLY, Kim YJ, Doong JYH, Grodzinsky AJ, Plaas AHK, Sandy JD (1989) Biosynthetic response of cartilage explants to dynamic compression. J Orthop Res 7:619–636CrossRefGoogle Scholar
- Scorsin M, Marotte F, Sabri A, Le Dref O, Demirag M, Samuel J-L, Rappaport L, Measche P (1996) Can grafted cardiomyocytes colonize peri-infarct myocardial areas? Circulation 94:II337–II340Google Scholar
- Sharma B, Elisseeff J (2004) Engineering structurally organized cartilage and bone tissues. Annals Biomed Eng 32:148–159CrossRefGoogle Scholar
- Soonpaa MH, Koh GY, Klug MG, Field LJ (1994) Formation of nascent intercalated disks between grafted fetal cardiomyocytes and host myocardium. Science 264:98–101CrossRefGoogle Scholar
- Steinmeyer J, Knue S (1997) The proteoglycan metabolism of mature bovine articular cartilage explants superimposed to continuously applied cyclic mechanical loading. Biochem Biophys Res Co 240:216–221CrossRefGoogle Scholar
- Vanwanseele B, Lucchinetti E, Stussi E (2002) The effects of immobilization on the characteristics of articular cartilage: current concepts and future directions. Osteoarthritis Cartilage 10:408–419CrossRefGoogle Scholar
- Vunjak-Novakovic G, Martin I, Obradovic B, Treppo S, Grodzinsky AJ, Langer R, Freed LE (1999) Bioreactor cultivation conditions modulate the composition and mechanical properties of tissue engineered cartilage. J Orthop Res 17:130–138CrossRefGoogle Scholar
- Vunjak-Novakovic G, Obradovic B, Martin I, Freed LE (2002) Bioreactor studies of native and tissue engineered cartilage. Biorheology 39:259–268Google Scholar
- Wang Y, Ameer GA, Sheppard BJ, Langer R (2002) A tough biodegradable elastomer. Nat Biotechnol 20:602–606CrossRefGoogle Scholar
- Weber M, Steinert A, Jork A, Dimmler A, Thurmer F, Schutze N, Hendrich C, Zimmermann U (2002) Formation of cartilage matrix proteins by BMP-transfected murine mesenchymal stem cells encapsulated in a novel class of alginates. Biomaterials 23:2003–2013CrossRefGoogle Scholar
- Wong M, Siegrist M, Cao X (1999) Cyclic compression of articular cartilage explants is associated with progressive consolidation and altered expression pattern of extracellular matrix proteins. Matrix Biol 18:391–399CrossRefGoogle Scholar
- Zimmermann WH, Fink C, Kralish D, Remmers U, Weil J, Eschenhagen T (2000) Three-dimensional engineered heart tissue from neonatal rat cardiac myocytes. Biotechnol Bioeng 68:106–114CrossRefGoogle Scholar
- Zimmermann WH, Schneiderbanger K, Schubert P, Didie M, Munzel F, Heubach JF, Kostin S, Nehuber WL, Eschenhagen T (2002) Tissue engineering of a differentiated cardiac muscle construct. Circ Res 90:223–230CrossRefGoogle Scholar