InVERT Molding for Scalable Control of Tissue Microarchitecture

Overview

Journal Nat Commun

Specialty Biology

Date 2013 May 16

PMID 23673632

Citations 64

Authors

K R Stevens

M D Ungrin

R E Schwartz

S Ng

B Carvalho

K S Christine

R R Chaturvedi

C Y Li

P W Zandstra

C S Chen

S N Bhatia

Affiliations

Soon will be listed here.

Abstract

Complex tissues contain multiple cell types that are hierarchically organized within morphologically and functionally distinct compartments. Construction of engineered tissues with optimized tissue architecture has been limited by tissue fabrication techniques, which do not enable versatile microscale organization of multiple cell types in tissues of size adequate for physiological studies and tissue therapies. Here we present an 'Intaglio-Void/Embed-Relief Topographic molding' method for microscale organization of many cell types, including induced pluripotent stem cell-derived progeny, within a variety of synthetic and natural extracellular matrices and across tissues of sizes appropriate for in vitro, pre-clinical, and clinical studies. We demonstrate that compartmental placement of non-parenchymal cells relative to primary or induced pluripotent stem cell-derived hepatocytes, compartment microstructure, and cellular composition modulate hepatic functions. Configurations found to sustain physiological function in vitro also result in survival and function in mice for at least 4 weeks, demonstrating the importance of architectural optimization before implantation.

Citing Articles

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References

Matsumoto K, Yoshitomi H, Rossant J, Zaret K . Liver organogenesis promoted by endothelial cells prior to vascular function. Science. 2001; 294(5542):559-63. DOI: 10.1126/science.1063889. View

Hui E, Bhatia S . Micromechanical control of cell-cell interactions. Proc Natl Acad Sci U S A. 2007; 104(14):5722-6. PMC: 1851558. DOI: 10.1073/pnas.0608660104. View

Si-Tayeb K, Noto F, Nagaoka M, Li J, Battle M, Duris C . Highly efficient generation of human hepatocyte-like cells from induced pluripotent stem cells. Hepatology. 2009; 51(1):297-305. PMC: 2946078. DOI: 10.1002/hep.23354. View

Tsang V, Chen A, Cho L, Jadin K, Sah R, DeLong S . Fabrication of 3D hepatic tissues by additive photopatterning of cellular hydrogels. FASEB J. 2007; 21(3):790-801. DOI: 10.1096/fj.06-7117com. View

Nelson C, VanDuijn M, Inman J, Fletcher D, Bissell M . Tissue geometry determines sites of mammary branching morphogenesis in organotypic cultures. Science. 2006; 314(5797):298-300. PMC: 2933179. DOI: 10.1126/science.1131000. View

Mikos A, Herring S, Ochareon P, Elisseeff J, Lu H, Kandel R . Engineering complex tissues. Tissue Eng. 2007; 12(12):3307-39. PMC: 2821210. DOI: 10.1089/ten.2006.12.3307. View

Mironov V, Visconti R, Kasyanov V, Forgacs G, Drake C, Markwald R . Organ printing: tissue spheroids as building blocks. Biomaterials. 2009; 30(12):2164-74. PMC: 3773699. DOI: 10.1016/j.biomaterials.2008.12.084. View

Miller J, Stevens K, Yang M, Baker B, Nguyen D, Cohen D . Rapid casting of patterned vascular networks for perfusable engineered three-dimensional tissues. Nat Mater. 2012; 11(9):768-74. PMC: 3586565. DOI: 10.1038/nmat3357. View

Levenberg S, Rouwkema J, Macdonald M, Garfein E, Kohane D, Darland D . Engineering vascularized skeletal muscle tissue. Nat Biotechnol. 2005; 23(7):879-84. DOI: 10.1038/nbt1109. View

10.

Gaebel R, Ma N, Liu J, Guan J, Koch L, Klopsch C . Patterning human stem cells and endothelial cells with laser printing for cardiac regeneration. Biomaterials. 2011; 32(35):9218-30. DOI: 10.1016/j.biomaterials.2011.08.071. View

11.

Kloxin A, Kasko A, Salinas C, Anseth K . Photodegradable hydrogels for dynamic tuning of physical and chemical properties. Science. 2009; 324(5923):59-63. PMC: 2756032. DOI: 10.1126/science.1169494. View

12.

Ding B, Nolan D, Guo P, Babazadeh A, Cao Z, Rosenwaks Z . Endothelial-derived angiocrine signals induce and sustain regenerative lung alveolarization. Cell. 2011; 147(3):539-53. PMC: 3228268. DOI: 10.1016/j.cell.2011.10.003. View

13.

Brophy C, Luebke-Wheeler J, Amiot B, Khan H, Remmel R, Rinaldo P . Rat hepatocyte spheroids formed by rocked technique maintain differentiated hepatocyte gene expression and function. Hepatology. 2008; 49(2):578-86. PMC: 2680349. DOI: 10.1002/hep.22674. View

14.

MacNeil S . Progress and opportunities for tissue-engineered skin. Nature. 2007; 445(7130):874-80. DOI: 10.1038/nature05664. View

15.

DeForest C, Anseth K . Cytocompatible click-based hydrogels with dynamically tunable properties through orthogonal photoconjugation and photocleavage reactions. Nat Chem. 2011; 3(12):925-31. PMC: 3229165. DOI: 10.1038/nchem.1174. View

16.

Williams C, Mehta G, Peyton S, Zeiger A, Van Vliet K, Griffith L . Autocrine-controlled formation and function of tissue-like aggregates by primary hepatocytes in micropatterned hydrogel arrays. Tissue Eng Part A. 2010; 17(7-8):1055-68. PMC: 3063704. DOI: 10.1089/ten.TEA.2010.0398. View

17.

Wong S, No D, Choi Y, Kim D, Chung B, Lee S . Concave microwell based size-controllable hepatosphere as a three-dimensional liver tissue model. Biomaterials. 2011; 32(32):8087-96. DOI: 10.1016/j.biomaterials.2011.07.028. View

18.

Khetani S, Bhatia S . Microscale culture of human liver cells for drug development. Nat Biotechnol. 2007; 26(1):120-6. DOI: 10.1038/nbt1361. View

19.

Abu-Absi S, Friend J, Hansen L, Hu W . Structural polarity and functional bile canaliculi in rat hepatocyte spheroids. Exp Cell Res. 2002; 274(1):56-67. DOI: 10.1006/excr.2001.5467. View

20.

Schwartz R, Trehan K, Andrus L, Sheahan T, Ploss A, Duncan S . Modeling hepatitis C virus infection using human induced pluripotent stem cells. Proc Natl Acad Sci U S A. 2012; 109(7):2544-8. PMC: 3289320. DOI: 10.1073/pnas.1121400109. View