Supplementary Material
Strategies for improving the physiological relevance of human engineered tissues
Rosalyn D. Abbott, David L. Kaplan
Department of Biomedical Engineering, Tufts University, 4 Colby St,Medford, MA 02115, USA
Corresponding author: Kaplan, D.L. ()
Supplementary Table 1.Long term culture in microfluidic platforms
2D or 3D? / Application / Cell Type / Length of culture / Reference2D / Drug screening for cancer research / T98G human glioblastoma tumor cells / 60h / [S1]
Human T-cell lymphomaHuT 78 cells
Human Burkitt′s lymphoma Ramos cells
Human prostate adenocarcinomaPC-3 cells
Murine endothelial C166-GFP cells / 2d
2d
2d
7d / [S2]
A549 nonsmall lung cancer cells / 11d / [S3]
Human carcinoma HeLa cells / 16d / [S4]
Human carcinoma HeLa cells / 2d / [S5]
Neural network connectivity and/or neuropharmacological studies / Lund human mesencephalic(LUHMES) cells
NeuroblastomaSH-SY5Y cells
Murine cortical cells / 7d
13d
13d / [S6]
Hippocampal neurons / 12d / [S7]
Co-culture of rat primary embryonic cortical cells and thalamic neurons / 35d / [S8]
Neurons from murine embryos / 18d / [S9]
Primary embryonic rat cortical neurons / 35d / [S10]
Co-culture of neurons and glia cells / 21d / [S11]
Primary murine embryonic neuronal cultures / 14d / [S12]
Embryonic rat dorsal root ganglion neurons and cortical neurons / 2d / [S13]
Intestine toxicity and drug screening / Human intestinal Caco-2 cells / 16d / [S14]
Liver toxicity and drug screening / Rat hepatocytes / 9d / [S15]
Human hepatocytes / 32d / [S16]
Dynamic stimulation / Human carcinoma HeLa cells
Hamster ovarian cancer CHO-K1 cells
Murine 3T3 fibroblast / 3d
3d
1d / [S17]
Preadipocyte Differentiation / Murine 3T3-L1 preadipocytes / 14d / [S18]
Cardio-myogenic differentiation / Murine embryoid cell bodies / 4d / [S19]
Human umbilical artery vascular smooth muscle cells / 14d / [S20]
Human induced pluripotent stem cell derived cardiomyocytes / 21d / [S21]
Skeletal muscle differentiation / Murine C2C12 skeletal muscle cells / 14d / [S22]
Murine C2C12 skeletal muscle cells / 14d / [S23]
Vascular hemodynamics / Bovine artery endothelial cells / 6d / [S24]
Artificial skin development / Human neonatal dermal fibroblasts / 21d / [S25]
Single cell monitoring / Human SW480 epithelial cells
Human HT29 colon carcinoma cells
MCF-7 human breast cancer cells
(Co-culture experiments at the single cell level – homotypic and herterotypic) / 5d
5d
5d / [S26]
Human leukemic monocyte lymphoma U937 cells
Human Jurkat T-lymphoblast cells
(non-adherent cells) / 4d
4d / [S27]
T-cell lymphoma EG7 cells
(non-adherent cells) / 12h / [S28]
Platform development / Murine C2C12 skeletal muscle cells
(controlled O2 microenvironment) / 3d / [S29]
Murine C2C12 skeletal muscle cells
(integration of track-etched membranes) / 14d / [S30]
Human embryonic kidney 293 cells
(a stage perfusion incubation system) / 5d / [S31]
HepG2/C3A human hepatoma cells (prevent/remove bubbles) / 3d / [S32]
Amniotic fluid mesenchymal stem cells
(differentiation under continuous flow) / 21d / [S33]
Bovine pulmonary artery endothelial cells
Lungmicrovessel endothelial cells
(portable automated bench-top mammalian cell-based toxicity sensor) / 9d
112d / [S34]
Monkey COS7 kidney cells
(thermomodulated cell culture and harvest without trypsin) / 3d / [S35]
Human malignant melanoma A375 cells (concentration gradients) / 36h / [S36]
Murine MC 3T3 E1 cells
(bubble-free, on-chip culture of cells) / 10d / [S37]
Murine fibroblasts
(portable cell culture device) / 7d / [S38]
Pheochromocytoma PC12 cells of the rat adrenal medulla
(time lapse imaging device that tracks live cells) / 7d / [S39]
Murineembryonic stem cells
Murine C2C12 skeletal muscle cells
Human foreskin fibroblasts
(periodic perfusion for homogenous cell culture) / 6d
6d
50d / [S40]
Monkey CV-1 kidney epithelial cells
(portable cell culture device) / 12d / [S41]
Murine pancreatic islets
(prevent/remove bubbles) / 1d / [S42]
Murine 3T3 fibroblast
Murine connective tissue L929 cells
Human osteosarcoma MG63 cells
(establishment of an air–liquid interface) / 4d
4d
4d / [S43]
Metastatic human breast cancer MDA-MB-231 cells
(patterning and differentiation of cells) / 12h / [S44]
Murine MC3T3-E1 osteoblastic cells
Murine C2C12 skeletal muscle cells
(portable cell culture device) / 6d
16d / [S45]
Human umbilical endothelial cells
Rat pheochromocytoma PC12
(electrochemical monitoring of cultured cells) / 14d
10d / [S46]
Human mesenchymal stem cells
(patterning and differentiation of cells) / 21d / [S47]
Murine connective tissueL929 cells
(combined chemical and mechanical gradient) / 44h / [S48]
Human foreskin fibroblasts
Human umbilical vein endothelial cells
Co-culture of human foreskin fibroblasts and human embryonic stem cells
(“flow-stop” perfusion system for shear sensitive cells to withstand medium renewal flow) / 14d
14d
24h / [S49]
Murine endothelial RCL-2583 cells
Human T lymphocyte HuT 78 cells
Human B lymphocyte RPMI 8226 cells
(stable, homogeneous, andlow-shearforce environment) / 4d
4d
4d / [S50]
Human lung adenocarcinoma CL1-5 cells
(integrated heater and a concentration gradient generator) / 122h / [S51]
MCF-7 human breast cancer cells
Human mesenchymal stem cells
(pulsatile pumping system for cell delivery and culturing functions on a single platform) / 7d
7d / [S52]
Human melanoma A2058
Murine Cath.a-differentiated cells
Human bladder epithelial T24 cells
(closed mini chamber system that supports long term time lapse recordings) / 229h
28d
1 d / [S53]
Murine embryonic neural progenitor cells
(on-chip transfection of adherent cells by localized electroporation) / 6d / [S54]
3D / Toxicity and drug screening / MCF-7 human breast cancer cells / 6d / [S55]
Human LS174T colon carcinoma / 4d / [S56]
Non-tumorigenic human breast MCF10A cells
MCF-10A pBabe
Ras-transformed MCF-10AT1
Tumorigenic MCF-10CA1a
Tumorigenic MCF-10CA1d / 21d
21d
21d
21d
21d / [S57]
HT-29 human colon carcinoma cells / 25d / [S58]
Non-tumorigenic human breast MCF10A cells
MCF-7 human breast cancer cells / 12d
12d / [S59]
Human LCC6/Her2 breast tumor cells / 6d / [S60]
Human colon cancer HCT-116 cells / 24h / [S61]
Human LCC6/Her-2 breast tumor cells / 9d / [S62]
Human colon carcinoma HT-29 cells
Human liver carcinoma Hep-G2 cells / 12d
10d / [S63]
MCF-7 human breast cancer cells / 6d / [S64]
Murine Col1a1GFP MC-3T3 E1 osteoblastic cells / 10d / [S65]
Vasculature / Co-culture of human umbilical vein endothelial cells, normal human lung fibroblasts, and either human HL-60 promyelocytic leukemia cells, or human U87MGglioblastomamultiforme cells (microvasculature creation through gels) / 7d / [S66]
Human dermal microvascular endothelial cells (microvasculature creation through tubes) / 32d / [S67]
Mice resistance arteries
(ex vivo artery perfusion and superfusion system) / 24h / [S68]
Primary human umbilical vein endothelial cells
(micropatterning of 3D natural ECM of flexible compositions and gelling mechanisms) / 21d / [S69]
Neural / Co-culture of 2 rat hippocampus slices with a microchannel axonal connection between them / 22d / [S70]
Co-culture of rat or murinehippocampus slices with axonal extensions / 28d / [S71]
Platform development / Primary human periodontal ligament cells
(high-resolution bioimaging) / 28d / [S72]
Cardio-myogenic differentiation / Murine embryoid cell bodies / 4d / [S19]
Liver / Human hepatoma cell line C3A / 4d / [S73]
Rat hepatocytes / 90d / [S74]
Co-culture of primary rat hepatocytes and murine swiss 3T3 cells feeder cells / 90d / [S75]
Rat hepatocytes / 14d / [S76]
Human liver carcinoma HepG2 cells / 14d / [S77]
Co-culture of human liver carcinoma HepG2 cells and murine Balb/c 3T3 fibroblast cells / 5d / [S78]
Skin / Co-culture of human keratinocytes, fibroblasts and endothelial cells / 14d / [S79]
Co-culture of human foreskin keratinocytes and fibroblasts / 3w (21d) / [S80]
Supplementary Table 2.Long term culture in static three dimensional cultures
Application / Cell Type / Length of culture / ReferenceNeural / Co-culture of murine spinal cord motor neurons, murine fibroblasts, and murine schwann cells / 28d / [S81]
Human umbilical cord blood stem cells / 73d / [S82]
Adult murine neural stem cells / 5m (150d) / [S83]
Co-culture of murine D3 embryonic stem cells,murine CGR8 embryonic stem cells, and murine MS5 bone marrow-derived stromal feeder cells / 3.5m (105d) / [S84]
Intestine / Small intestine explants of GFP C57BL/6 or wild-type C57BL/6J neonatal mice / 14d / [S85]
Tendon / Human tenocytes / 28d / [S86]
Cancer spheroids / Human epithelial ovarian carcinoma cells / 28d / [S87]
Cardiovascular / Co-culture of primary neonatal rat ventricularcardiomyocytes, murine 3T3-J2 and primary
rat heart microvessel endothelial cells / 28d / [S88]
Murine cardiomyocyte HL1 cell line / 38d / [S89]
Fetal rat cardiocytes / 84d / [S90]
Myocardialtissuefrom newborn mice / 56d / [S91]
Primary neonatal murinecardiomyocytes / 25d / [S92]
Skin / Co-culture of adult human epidermal keratinocytes and human dermal fibroblasts / 95d / [S93]
Co-culture of adult human keratinocytes and human dermal fibroblasts
/ 84d / [S94]Co-culture of murine epidermal keratinocytes and murine dermal fibroblasts / 14d / [S95]
Co-culture of normal human dermal fibroblasts and normal human epidermal keratinocytes
(cultured in human fibroblast-derived matrix) / 140d / [S96]
Human epidermal keratinocytes
(epidermal gene therapy) / 7d / [S97]
Retinal / Murine embryonic stem cells / 24d / [S98]
Adipose / Rat bone marrow stromal cells / 28d / [S99]
Bone and Adipose / Human mesenchymal stem cells / 50d / [S100]
Bone / Rabbit bone marrow stromal cells / 35d / [S101]
Murine periosteummesenchymal stem cells / 365d / [S102]
Co-culture of human umbilical vein endothelial cells and primary human osteoblasts / 42d / [S103]
Human bone marrow derived mesenchymal stem cells / 46d / [S104]
Human cord blood mononuclear cells / 28d / [S105]
Osteochondral / Human mesenchymal stem cells / 45d / [S106]
Cartilage / Human bone marrow derived stem cells / 84d / [S107]
Human bone marrow stromal cells and human neonatal and adult chondrocytes
(dynamic seeding for 24 hours) / 42d / [S108]
Human mesenchymal stem cells
(non-viral gene therapy) / 21d / [S109]
Rat primary chondrocytes
(lentiviral gene therapy) / 56d / [S110]
Porcine femoral condylar chondrocytes / 42d / [S111]
Bovine articular chondrocytes / 52d / [S112]
Porcine articular chondrocytes / 35d / [S113]
Bovine chondrocytes
Bovine mesenchymal stem cells / 70d
70d / [S114]
Bovine articular chondrocytes / 9d / [S115]
Chondrocytes (porcine and equine) / 6m (180d) / [S116]
Bovine juvenile articular chondrocytes / 35d / [S117]
Liver / Co-culture of rat hepatocytes and primary rat hepatic stellate cells / 54d / [S118]
Human fetal hepatocytes / 35d / [S119]
Murine fetal liver cells / 35d / [S120]
Murine fetal liver cells / 245d / [S121]
Human hepatocellular carcinoma-derived FLC-4 / 24d / [S122]
Adult rabbit primary biliary epithelial cells / 3m (90d) / [S123]
Co-culture of rat hepatocytes, rat hepatic stellate cells, and bovine pulmonary microvascular endothelial cells / 40d / [S124]
Human hepatocyte carcinoma (HepG2) / 27d / [S125]
Pancreas / Human islets / 10d / [S126]
Kidney / Co-culture of murine glomerular epithelial and mesangial cells / 1m (30d) / [S127]
Oropharyngeal mucosa / Co-culture of human oropharyngeal keratinocytes and fibroblasts / 10d / [S128]
General 3D encapsulation methods that could be applied to multiple tissues / Murine fibroblasts
(cross-linked collagen gels) / 42d / [S129]
Porcine chondrocytes
Human dermal fibroblasts
(collagen gels) / 7d
7d / [S130]
Murine ATDC5 chondrocytes
(mild cell encapsulation method based on self-assembly and microfluidics technology) / 21d / [S131]
Human trophoblastHTR-8/SVneo cells
Rat aorta vascular smooth muscle cells
Sheep aortic endothelial cells
Human umbilical vein endothelial cells
(modular approach that could be paired with endothelialized, perfusable channels and perfusion in some experiments, see Table 3) / 45d
14d
14d
14d / [S132]
Murine connective tissueL929 cells and normal human dermal fibroblasts
(fibronectin/gelatin multilayered tissues) / 28d / [S133]
Murine 3T3 fibroblasts
(dense fibrillar collagen scaffold) / 7d / [S134]
Normal human dermal fibroblasts
(Silica nanoparticle–collagen bionanocomposites) / 21d / [S135]
Co-culture of bovine fibroblasts and bovine mesenchymal stem cells
(photo-patterned hydrogels) / 14d / [S136]
Rat primary bladder smooth muscle cells
(multilayered printing of 3D cell-laden collagen hydrogel structures) / 14d / [S137]
Murine embryonic stem D3 cells
(polyethylene terephthalate fibrousmatrices) / 28d / [S138]
Supplementary Table 3.Long term culture in large scale 3D bioreactors
Type of Bioreactor / Cell Type (application) / Length of culture / ReferenceDirect Perfusion / Human primary tonsil cells
(packed bed bioreactor studying peripheral lymphoid structure and function) / 42d / [S139]
Rat primary hepatocytes
(packed bed bioreactor for creating a liver tissue model) / 14d / [S132]
Human mesenchymal stem cells
(packed bed of alginate beads for determining the effects of shear stresses on differentiating hMSCs) / 28d / [S140]
Murine C2C12 skeletal muscle cells
(cell cycle analysis to study relevant population markers) / 10d / [S141]
Murine C2C12 skeletal muscle cells
Skeletal-muscleprecursorcells
(platform development for a cellularized artificial graft with high density of viable cells and uniform cell distribution) / 7d
7d / [S142]
Sheep mesenchymal stem cell
(platform development for the maintenance of critically sized scaffolds) / 28d / [S143]
Human mesenchymal stem cells
(stem cell tissue engineering) / 40d / [S144]
Primary rat osteoblasts
Rat bone marrow stromal cells
(bone model for improved viability) / 42d
42d / [S145]
Human chondrocytes
(generation of artificial connectivetissue) / 40d / [S146]
Human adipose derived mesenchymal stem cells
(differentialpressure laminar flow reactor for osteogenic differentiation towards a tissue-engineered bone substitute) / 60d / [S147]
Perfusion + mechanical stimulation / Bovine calf articular chondrocytes
(cartilage cultivation for functional tissue engineering) / 67d / [S148]
Mechanical Simulation / Rat bone marrow stromal cells
(four point bending of natural or engineered tissues in vitro) / 16d / [S149]
Porcine annulus fibrosus cells
(cyclic compressive platform for enhanced matrix production) / 14d / [S150]
Human bone marrow derived and adipose derived stem cells
(cyclic hydrostatic cultures for cartilage tissue engineering) / 21d / [S151]
Indirect Perfusion / Human liver carcinoma HepG2 cells
(radial flow high cell density liver model for drug testing/regenerative medicine) / 17d / [S152]
Co-culture of primary porcine hepatocytes and nonparenchymal cells
(hollow fiber bioreactor for liver regeneration andtissueformation) / 30d / [S153]
Primary osteoblasts isolated from embryonic chick calvaria
(hollow fiber bioreactor for studying bone formation) / 63d / [S154]
Primary human hepatocytes
(hollow fiber bioreactor for liver metabolism and toxicity studies) / 21d / [S155]
Rotating wall vessel / Rat neural stem cells and neural progenitors
(neuralmodel for cell replacement therapy) / 63d / [S156]
Human liver carcinoma HepG2 cells
(liver tissue model) / 70d / [S157]
Bovine articular chondrocytes
(pseudo-weightlessness in prolonged immobilization, hydrotherapy, and intrauterine development) / 210d / [S158]
Dura mater stem cells from a rat fetus
(bone mineralization model) / 28d / [S159]
Spinner flask / Co-culture of human endothelial cells and human adipose derived stem cells
(adipose silk scaffold model for long term sustainable function) / 180d / [S160]
Murine embryonic stem D3 cells (ATCC CRL-1934)
(fibrous bed for long term expansion of embryoid bodies) / 15d / [S161]
Orbital shaker / Bovine mesenchymal stem cells
Bovine chondrocytes
(cartilage model comparing chondrocytes to MSCs for functional repair) / 112d
112d / [S162]
Rat marrow stromal cells
(bone model to investigate dose patterns under dynamic stimulation) / 32d / [S163]
Primary rat hepatocytes
(hollow fiber liver organoid tissue model) / 176d / [S164]
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