Generation of tissue-engineered small intestine using embryonic stem cell-derived human intestinal organoids
Open accessAbstract
Short bowel syndrome (SBS) is characterized by poor nutrient absorption due to a deficit of healthy intestine. Current treatment practices rely on providing supportive medical therapy with parenteral nutrition; while life saving, such interventions are not curative and are still associated with significant co-morbidities. As approaches to lengthen remaining intestinal tissue have been met with only limited success and intestinal transplants have poor survival outcomes, new approaches to treating SBS are necessary. Human intestine derived from embryonic stem cells (hESCs) or induced pluripotent stem cells (iPSCs), called human intestinal organoids (HIOs), have the potential to offer a personalized and scalable source of intestine for regenerative therapies. However, given that HIOs are small three-dimensional structures grown in vitro, methods to generate usable HIO-derived constructs are needed. We investigated the ability of hESCs or HIOs to populate acellular porcine intestinal matrices and artificial polyglycolic/poly L lactic acid (PGA/PLLA) scaffolds, and examined the ability of matrix/scaffolds to thrive when transplanted in vivo. Our results demonstrate that the acellular matrix alone is not sufficient to instruct hESC differentiation towards an endodermal or intestinal fate. We observed that while HIOs reseed acellular porcine matrices in vitro, the HIO-reseeded matrices do not thrive when transplanted in vivo. In contrast, HIO-seeded PGA/PLLA scaffolds thrive in vivo and develop into tissue that looks nearly identical to adult human intestinal tissue. Our results suggest that HIO-seeded PGA/PLLA scaffolds are a promising avenue for developing the mucosal component of tissue engineered human small intestine, which need to be explored further to develop them into fully functional tissue.
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Pre-differentiated human intestinal organoids were able to seed onto decellularized porcine intestinal ECM and form correct spatial orientation-mimicking intestine.
“However, pre-differentiated HIOs were able to seed onto decellularized porcine intestinal ECM and form correct spatial orientation-mimicking intestine79.”
From Towards organoid culture without Matrigel (2021) · cites this paper as [79]
Undifferentiated human embryonic stem cells could not directly differentiate into human intestinal organoids in a decellularized porcine intestinal ECM.
“Finkbeiner and colleagues found that undifferentiated human embryonic stem cells (ESCs) could not directly differentiate into HIOs in a decellularized porcine intestinal ECM.”
From Towards organoid culture without Matrigel (2021) · cites this paper as [79]
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3 retracted
GRIM-19 Mediated Translocation of STAT3 to Mitochondria is Necessary for TNF Induced Necroptosis.
Shulga, N., & Pastorino, J. G. (2012) · Journal of Cell Science · doi:10.1242/jcs.103093 · Cited by 101 · see citing works
RetractedMitoneet mediates TNFα induced necroptosis promoted by fructose and ethanol exposure
Shulga, N., & Pastorino, J. G. (2013) · Journal of Cell Science · doi:10.1242/jcs.140764 · Cited by 20 · see citing works
RetractedShulga, N., & Pastorino, J. G. (2014) · Journal of Biological Chemistry · doi:10.1074/jbc.m114.580175 · Cited by 14 · see citing works
RetractedInduction of Pluripotent Stem Cells from Adult Human Fibroblasts by Defined Factors
Takahashi, K., Tanabe, K., Ohnuki, M., Narita, M., Ichisaka, T., Tomoda, K., & Yamanaka, S. (2007) · Cell · doi:10.1016/j.cell.2007.11.019 · Cited by 20,221 · see citing works
Directed differentiation of human pluripotent stem cells into intestinal tissue in vitro
Spence, J. R., Mayhew, C. N., Rankin, S. A., Kuhar, M. F., Vallance, J. E., Tolle, K. A., Hoskins, E. E., Kalinichenko, V. V., Wells, S. I., Zorn, A. M., et al. (2010) · Nature · doi:10.1038/nature09691 · Cited by 1,911 · see citing works
Self-citationMechanisms of Pancreatic β-Cell Death in Type 1 and Type 2 Diabetes
Cnop, M., Welsh, N., Jonas, J.-C., Jörns, A., Lenzen, S., & Eizirik, D. L. (2005) · Diabetes · doi:10.2337/diabetes.54.suppl_2.s97 · Cited by 1,491 · see citing works
NOD/SCID/γcnull mouse: an excellent recipient mouse model for engraftment of human cells
Ito, M., Hiramatsu, H., Kobayashi, K., Suzue, K., Kawahata, M., Hioki, K., Ueyama, Y., Koyanagi, Y., Sugamura, K., Tsuji, K., et al. (2002) · Blood · doi:10.1182/blood-2001-12-0207 · Cited by 1,483 · see citing works
Molecular and metabolic mechanisms of insulin resistance and β-cell failure in type 2 diabetes
Muoio, D. M., & Newgard, C. B. (2008) · Nature Reviews Molecular Cell Biology · doi:10.1038/nrm2327 · Cited by 1,177 · see citing works
In vitro generation of human pluripotent stem cell derived lung organoids
Dye, B. R., Hill, D. R., Ferguson, M. A. H., Tsai, Y.-H., Nagy, M. S., Dyal, R., Wells, J. M., Mayhew, C. N., Nattiv, R., Klein, O. D., et al. (2015) · eLife · doi:10.7554/elife.05098 · Cited by 824 · see citing works
Self-citationBooth, A. J., Hadley, R., Cornett, A. M., Dreffs, A. A., Matthes, S. A., Tsui, J. L., Weiss, K., Horowitz, J. C., Fiore, V. F., Barker, T. H., et al. (2012) · American Journal of Respiratory and Critical Care Medicine · doi:10.1164/rccm.201204-0754oc · Cited by 665 · see citing works
Self-citationAn in vivo model of human small intestine using pluripotent stem cells
Watson, C. L., Mahé, M. M., Múnera, J. O., Howell, J. C., Sundaram, N., Poling, H. M., Schweitzer, J. I., Vallance, J. E., Mayhew, C. N., Sun, Y., et al. (2014) · Nature Medicine · doi:10.1038/nm.3737 · Cited by 561 · see citing works
Self-citationSimcox, J. A., & McClain, D. A. (2013) · Cell Metabolism · doi:10.1016/j.cmet.2013.02.007 · Cited by 545 · see citing works
Regulation of the fructose transporter GLUT5 in health and disease
Douard, V., & Ferraris, R. P. (2008) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.90245.2008 · Cited by 477 · see citing works
Generating human intestinal tissue from pluripotent stem cells in vitro
McCracken, K. W., Howell, J. C., Wells, J. M., & Spence, J. R. (2011) · Nature Protocols · doi:10.1038/nprot.2011.410 · Cited by 433 · see citing works
Self-citationDekker, M. J., Su, Q., Baker, C., Rutledge, A. C., & Adeli, K. (2010) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.00283.2010 · Cited by 419 · see citing works
Jourdan, T., Godlewski, G., Cinar, R., Bertola, A., Szanda, G., Liu, J., Tam, J., Han, T., Mukhopadhyay, B., Skarulis, M. C., et al. (2013) · Nature Medicine · doi:10.1038/nm.3265 · Cited by 388 · see citing works
Inflammation in obesity and diabetes: islet dysfunction and therapeutic opportunity
Donath, M. Y., Dalmas, É., Sauter, N. S., & Böni-Schnetzler, M. (2013) · Cell Metabolism · doi:10.1016/j.cmet.2013.05.001 · Cited by 338 · see citing works
Pediatric Short Bowel Syndrome
Spencer, A. U., Neaga, A., West, B. T., Safran, J., Brown, P., Btaiche, I. F., Kuzma-O’Reilly, B., & Teitelbaum, D. H. (2005) · Annals of Surgery · doi:10.1097/01.sla.0000179647.24046.03 · Cited by 332 · see citing works
Self-citationShort-bowel syndrome in children and adults
Vanderhoof, J., & Langnas, A. N. (1997) · Gastroenterology · doi:10.1053/gast.1997.v113.pm9352883 · Cited by 321 · see citing works
Opposing effects of fructokinase C and A isoforms on fructose-induced metabolic syndrome in mice
Ishimoto, T., Lanaspa, M. A., Le, M. T., García, G., Diggle, C. P., MacLean, P. S., Jackman, M. R., Asipu, A., Roncal-Jiménez, C. A., Kosugi, T., et al. (2012) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1119908109 · Cited by 304 · see citing works
MitoNEET is a uniquely folded 2Fe-2S outer mitochondrial membrane protein stabilized by pioglitazone
Paddock, M. L., Wiley, S. E., Axelrod, H. L., Cohen, A. E., Roy, M., Abresch, E. C., Capraro, D. T., Murphy, A. N., Nechushtai, R., Dixon, J. E., et al. (2007) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0707189104 · Cited by 302 · see citing works
Lanaspa, M. A., Sánchez‐Lozada, L. G., Cicerchi, C., Li, N., Roncal-Jiménez, C. A., Ishimoto, T., Le, M. T., García, G., Thomas, J. B., Rivard, C. J., et al. (2012) · PLoS ONE · doi:10.1371/journal.pone.0047948 · Cited by 283 · see citing works
Wales, P. W., de Silva, N., Kim, J. H., Lecce, L., Sandhu, A., & Moore, A. M. (2005) · Journal of Pediatric Surgery · doi:10.1016/j.jpedsurg.2005.01.037 · Cited by 271 · see citing works
Pastorino, J. G., Simbula, G., Yamamoto, K., Glascott, P. A., Rothman, R. J., & Farber, J. L. (1996) · Journal of Biological Chemistry · doi:10.1074/jbc.271.47.29792 · Cited by 263 · see citing works
Finkbeiner, S. R., Hill, D. R., Altheim, C. H., Dedhia, P. H., Taylor, M. J., Tsai, Y.-H., Chin, A. M., Mahé, M. M., Watson, C. L., Freeman, J. J., et al. (2015) · Stem Cell Reports · doi:10.1016/j.stemcr.2015.04.010 · Cited by 250 · see citing works
Self-citationImproved survival in a multidisciplinary short bowel syndrome program
Modi, B. P., Langer, M., Ching, Y. A., Valim, C., Waterford, S. D., Iglesias, J., Duro, D., Lo, C. W., Jaksic, T., & Duggan, C. (2008) · Journal of Pediatric Surgery · doi:10.1016/j.jpedsurg.2007.09.014 · Cited by 226 · see citing works
High fructose corn syrup and diabetes prevalence: A global perspective
Goran, M., Ulijaszek, S., & Ventura, E. (2013) · Global Public Health · doi:10.1080/17441692.2012.736257 · Cited by 201 · see citing works
Abdelmalek, M. F., Lazo, M., Horska, A., Bonekamp, S., Lipkin, E. W., Balasubramanyam, A., Bantle, J. P., Johnson, R. J., Diehl, A. M., & Clark, J. M. (2012) · Hepatology · doi:10.1002/hep.25741 · Cited by 190 · see citing works
Short bowel syndrome: epidemiology and etiology
Wales, P. W., & Christison-Lagay, E. R. (2009) · Seminars in Pediatric Surgery · doi:10.1053/j.sempedsurg.2009.11.001 · Cited by 187 · see citing works
Dahlén, E., Dawe, K. I., Ohlsson, L., & Hedlund, G. (1998) · PubMed · Cited by 183 · see citing works
Extracellular matrix components in intestinal development
Simon-Assmann, P. M., Kédinger, M., Arcangelis, A. D., Rousseau, V., & Simo, P. (1995) · Cellular and Molecular Life Sciences · doi:10.1007/bf01921739 · Cited by 182 · see citing works
Xue, X., Ramakrishnan, S. K., Anderson, E. R., Taylor, M. J., Zimmermann, E. M., Spence, J. R., Huang, S., Greenson, J. K., & Shah, Y. M. (2013) · Gastroenterology · doi:10.1053/j.gastro.2013.07.010 · Cited by 171 · see citing works
Self-citationLanaspa, M. A., Ishimoto, T., Cicerchi, C., Tamura, Y., Roncal-Jiménez, C. A., Chen, W., Tanabe, K., Andrés-Hernando, A., Orlicky, D. J., Finol, E., et al. (2014) · Journal of the American Society of Nephrology · doi:10.1681/asn.2013080901 · Cited by 168 · see citing works
Koo, H.-Y., Wallig, M. A., Chung, B. H., Nara, T. Y., Cho, B. H. S., & Nakamura, M. T. (2008) · Biochimica et Biophysica Acta (BBA) - Molecular Basis of Disease · doi:10.1016/j.bbadis.2008.02.007 · Cited by 164 · see citing works
Synthetic small intestinal scaffolds for improved studies of intestinal differentiation
Costello, C. M., Jia, H., Shaffiey, S. A., Yu, J., Jain, N. K., Hackam, D. J., & March, J. C. (2014) · Biotechnology and Bioengineering · doi:10.1002/bit.25180 · Cited by 163 · see citing works
Pediatric short-bowel syndrome: the cost of comprehensive care
Spencer, A. U., Kovacevich, D. S., McKinney-Barnett, M., Hair, D., Canham, J., Maksym, C. J., & Teitelbaum, D. H. (2008) · American Journal of Clinical Nutrition · doi:10.3945/ajcn.2008.26007 · Cited by 160 · see citing works
Self-citationCucak, H., Grunnet, L. G., & Rosendahl, A. (2013) · Journal of Leukocyte Biology · doi:10.1189/jlb.0213075 · Cited by 156 · see citing works
Avlasevich, S. L., Bryce, S. M., Cairns, S. E., & Dertinger, S. D. (2005) · Environmental and Molecular Mutagenesis · doi:10.1002/em.20170 · Cited by 152 · see citing works
Hess, R. A., Welch, K. B., Brown, P. I., & Teitelbaum, D. H. (2011) · Journal of Surgical Research · doi:10.1016/j.jss.2011.03.037 · Cited by 133 · see citing works
Self-citationCrystal structure of human mitoNEET reveals distinct groups of iron–sulfur proteins
Lin, J., Zhou, T., Ye, K., & Wang, J. (2007) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0702426104 · Cited by 130 · see citing works
Five-year outcomes after serial transverse enteroplasty in children with short bowel syndrome
Oliveira, C., de Silva, N., & Wales, P. W. (2012) · Journal of Pediatric Surgery · doi:10.1016/j.jpedsurg.2012.01.049 · Cited by 119 · see citing works
Jabaji, Z. B., Brinkley, G. J., Khalil, H. A., Sears, C. M., Lei, N., Lewis, M. S., Stelzner, M. G., Martı́n, M. G., & Dunn, J. (2014) · PLoS ONE · doi:10.1371/journal.pone.0107814 · Cited by 119 · see citing works
Corpe, C. P., Mm, B., Affleck, J. A., Gould, G. W., Jess, T. J., & Kellett, G. L. (1996) · Pflügers Archiv - European Journal of Physiology · doi:10.1007/s004240050124 · Cited by 119 · see citing works
Dekaney, C. M., Fong, J. J., Rigby, R. J., Lund, P. K., Henning, S., & Helmrath, M. A. (2007) · American Journal of Physiology-Gastrointestinal and Liver Physiology · doi:10.1152/ajpgi.00218.2007 · Cited by 112 · see citing works
Mitochondrial dysfunction in pancreatic β-cells in Type 2 Diabetes
Mulder, H., & Ling, C. (2008) · Molecular and Cellular Endocrinology · doi:10.1016/j.mce.2008.05.015 · Cited by 111 · see citing works
Stephens, L. A., Thomas, H. E., Li, M., DARWICHE, M. G. R., Volodin, L., & Kay, T. W. H. (1999) · Endocrinology · doi:10.1210/endo.140.7.6873 · Cited by 107 · see citing works
Enteric glial cells: new players in gastrointestinal motility?
Bassotti, G., Villanacci, V., Antonelli, E., Morelli, A., & Salerni, B. (2007) · Laboratory Investigation · doi:10.1038/labinvest.3700564 · Cited by 107 · see citing works
Short bowel syndrome: A review of management options
Rodrigues, G. S., & Seetharam, P. (2011) · Saudi Journal of Gastroenterology · doi:10.4103/1319-3767.82573 · Cited by 100 · see citing works
Dietary fructose induces endotoxemia and hepatic injury in calorically controlled primates
Kavanagh, K., Wylie, A. T., Tucker, K. L., Hamp, T. J., Gharaibeh, R. Z., Fodor, A. A., & Cullen, J. M. (2013) · American Journal of Clinical Nutrition · doi:10.3945/ajcn.112.057331 · Cited by 99 · see citing works
Serial Transverse Enteroplasty Enhances Intestinal Function in a Model of Short Bowel Syndrome
Chang, R. W., Javid, P. J., Oh, J.-T., Andreoli, S. M., Kim, H. B., Fauza, D. O., & Jaksic, T. (2006) · Annals of Surgery · doi:10.1097/01.sla.0000197704.76166.07 · Cited by 98 · see citing works
Human and mouse tissue-engineered small intestine both demonstrate digestive and absorptive function
Grant, C. N., Mojica, S. G., Sala, F. G., Hill, J. R., Levin, D. E., Speer, A. L., Barthel, E. R., Shimada, H., Zachos, N. C., & Grikscheit, T. C. (2015) · American Journal of Physiology-Gastrointestinal and Liver Physiology · doi:10.1152/ajpgi.00111.2014 · Cited by 98 · see citing works
Self-citationThe surface molecular functionality of decellularized extracellular matrices
Barnes, C. A., Brison, J., Michel, R., Brown, B. N., Castner, D. G., Badylak, S. F., & Ratner, B. D. (2010) · Biomaterials · doi:10.1016/j.biomaterials.2010.09.007 · Cited by 97 · see citing works
Intestinal Rehabilitation and Bowel Reconstructive Surgery
Khalil, B. A., Ba’Ath, M. E., Aziz, A., Forsythe, L., Gozzini, S., Murphy, F., Carlson, G., Bianchi, A., & Morabito, A. (2011) · Journal of Pediatric Gastroenterology and Nutrition · doi:10.1097/mpg.0b013e318230c27e · Cited by 96 · see citing works
Low-fructose diet lowers blood pressure and inflammation in patients with chronic kidney disease
Brymora, A., Flisiński, M., Johnson, R. J., Goszka, G., Stefańska, A., & Manitius, J. (2011) · Nephrology Dialysis Transplantation · doi:10.1093/ndt/gfr223 · Cited by 94 · see citing works
Redox Characterization of the FeS Protein MitoNEET and Impact of Thiazolidinedione Drug Binding
Bak, D. W., Zuris, J. A., Paddock, M. L., Jennings, P. A., & Elliott, S. J. (2009) · Biochemistry · doi:10.1021/bi9016445 · Cited by 92 · see citing works
Sala, F. G., Matthews, J. A., Speer, A. L., Torashima, Y., Barthel, E. R., & Grikscheit, T. C. (2011) · Tissue Engineering Part A · doi:10.1089/ten.tea.2010.0564 · Cited by 92 · see citing works
Self-citationMacrophages, cytokines and β-cell death in Type 2 diabetes
Ehses, J. A., Böni‐Schnetzler, M., Faulenbach, M. V., & Donath, M. Y. (2008) · Biochemical Society Transactions · doi:10.1042/bst0360340 · Cited by 92 · see citing works
Jabaji, Z. B., Sears, C. M., Brinkley, G. J., Lei, N., Joshi, V. S., Wang, J., Lewis, M. S., Stelzner, M. G., Martı́n, M. G., & Dunn, J. (2013) · Tissue Engineering Part C Methods · doi:10.1089/ten.tec.2012.0710 · Cited by 82 · see citing works
Intestinal adaptation after small bowel resection in human infants
McDuffie, L. A., Bucher, B. T., Erwin, C. R., Wakeman, D. S., White, F., & Warner, B. W. (2011) · Journal of Pediatric Surgery · doi:10.1016/j.jpedsurg.2011.03.027 · Cited by 81 · see citing works
Pancreatic β-Cell Death in Response to Pro-Inflammatory Cytokines Is Distinct from Genuine Apoptosis
Collier, J. J., Burke, S. J., Eisenhauer, M. E., Lu, D., Sapp, R. C., Frydman, C. J., & Campagna, S. R. (2011) · PLoS ONE · doi:10.1371/journal.pone.0022485 · Cited by 80 · see citing works
Sugar sensing by enterocytes combines polarity, membrane bound detectors and sugar metabolism
Gall, M. L., Tobin, V., Stolarczyk, É., Dalet‐Fumeron, V., Leturque, A., & Brot‐Laroche, E. (2007) · Journal of Cellular Physiology · doi:10.1002/jcp.21245 · Cited by 80 · see citing works
Lablanche, S., Cottet‐Rousselle, C., Lamarche, F., Benhamou, P., Halimi, S., Leverve, X. M., & Fontaine, E. M. (2011) · Cell Death and Disease · doi:10.1038/cddis.2011.15 · Cited by 79 · see citing works
Human tissue-engineered small intestine forms from postnatal progenitor cells
Levin, D. E., Barthel, E. R., Speer, A. L., Sala, F. G., Hou, X., Torashima, Y., & Grikscheit, T. C. (2013) · Journal of Pediatric Surgery · doi:10.1016/j.jpedsurg.2012.10.029 · Cited by 76 · see citing works
Self-citationSuccessful Implantation of Bioengineered, Intrinsically Innervated, Human Internal Anal Sphincter
Raghavan, S. A., Gilmont, R. R., Miyasaka, E. A., Somara, S., Srinivasan, S., Teitelbaum, D. H., & Bitar, K. N. (2011) · Gastroenterology · doi:10.1053/j.gastro.2011.03.056 · Cited by 76 · see citing works
Self-citationDirect Spectrophotometric Determination of Serum Fructose in Pancreatic Cancer Patients
Hui, H., Huang, D., McArthur, D. L., Nissen, N., Boros, L. G., & Heaney, A. P. (2009) · Pancreas · doi:10.1097/mpa.0b013e3181a7c6e5 · Cited by 72 · see citing works
Garrison, A. P., Dekaney, C. M., von Allmen, D. C., Lund, P. K., Henning, S., & Helmrath, M. A. (2009) · American Journal of Physiology-Gastrointestinal and Liver Physiology · doi:10.1152/ajpgi.90588.2008 · Cited by 65 · see citing works
Metabolic Complications of Total Parenteral Nutrition: Effects of a Nutrition Support Service
Chrisanderson, D., Heimburger, D. C., Morgan, S. L., Geels, W. J., Henry, K. L., Conner, W., Hensrud, D. D., Thompson, G., & Weinsier, R. L. (1996) · Journal of Parenteral and Enteral Nutrition · doi:10.1177/0148607196020003206 · Cited by 53 · see citing works
A Gutsy Task: Generating Intestinal Tissue from Human Pluripotent Stem Cells
Finkbeiner, S. R., & Spence, J. R. (2013) · Digestive Diseases and Sciences · doi:10.1007/s10620-013-2620-2 · Cited by 48 · see citing works
Self-citationManagement of short bowel syndrome
Sulkowski, J. P., & Minneci, P. C. (2013) · Pathophysiology · doi:10.1016/j.pathophys.2013.11.013 · Cited by 42 · see citing works
Leibowitz, A., Rehman, A., Paradis, P., & Schiffrin, E. L. (2013) · Hypertension · doi:10.1161/hypertensionaha.111.203521 · Cited by 39 · see citing works
Imaging β-Cell Death With a Near-Infrared Probe
Medarova, Z. O., Bonner‐Weir, S., Lipes, M. A., & Moore, A. V. (2005) · Diabetes · doi:10.2337/diabetes.54.6.1780 · Cited by 33 · see citing works
Tissue Engineering of the Intestine in a Murine Model
Barthel, E. R., Speer, A. L., Levin, D. E., Sala, F. G., Hou, X., Torashima, Y., Wigfall, C. M., & Grikscheit, T. C. (2012) · Journal of Visualized Experiments · doi:10.3791/4279 · Cited by 31 · see citing works
Self-citationPresence of fructokinase in pancreatic islets
Malaisse, W. J., MALAISSE-LAGAE, F., Davies, D. R., & SCHAFTINGEN, E. V. (1989) · FEBS Letters · doi:10.1016/0014-5793(89)81085-3 · Cited by 28 · see citing works
Repeated Mechanical Lengthening of Intestinal Segments in a Novel Model
Scott, A., Sullins, V. F., Steinberger, D., Rouch, J. D., Wagner, J. P., Chiang, E. K., Lee, S. L., Wu, B. M., & Dunn, J. (2015) · Journal of Pediatric Surgery · doi:10.1016/j.jpedsurg.2015.03.020 · Cited by 27 · see citing works
Short Bowel Syndrome: How Short is Too Short?
Goday, P. S. (2009) · Clinics in Perinatology · doi:10.1016/j.clp.2008.09.006 · Cited by 27 · see citing works
High-fructose corn syrup and the obesity epidemic
Jacobson, M. F. (2004) · American Journal of Clinical Nutrition · doi:10.1093/ajcn/80.4.1081 · Cited by 25 · see citing works
Kawasaki, T., Igarashi, K., Ogata, N., Oka, Y., Ichiyanagi, K., & Yamanouchi, T. (2010) · Acta Diabetologica · doi:10.1007/s00592-010-0179-3 · Cited by 20 · see citing works
Advances in short bowel syndrome: an updated review
Sukhotnik, I., Coran, A. G., Kramer, A., Shiloni, E., & Mogilner, J. G. (2005) · Pediatric Surgery International · doi:10.1007/s00383-005-1500-z · Cited by 17 · see citing works
Countries that use large amounts of high fructose corn syrup have higher rates of type 2 diabetes
Kmietowicz, Z. (2012) · BMJ · doi:10.1136/bmj.e7994 · Cited by 15 · see citing works
Wulkersdorfer, B., Kao, K. K., Agopian, V. G., Dunn, J., Wu, B. M., & Stelzner, M. G. (2009) · Journal of Surgical Research · doi:10.1016/j.jss.2009.11.719 · Cited by 14 · see citing works
Tagzirt, M., Corseaux, D., Pasquesoone, L., Mouquet, F., Lavisse, C., Ung, A., Lorenzi, R., Jude, B., Elkalioubie, A., BELLE, E. V., et al. (2014) · American Journal of Hypertension · doi:10.1093/ajh/hpu021 · Cited by 11 · see citing works
Fructose misuse, the obesity epidemic, the special problems of the child, and a call to action
Krilanovich, N. J. (2004) · American Journal of Clinical Nutrition · doi:10.1093/ajcn/80.5.1446a · Cited by 5 · see citing works
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Cruz-Acuña, R., Quirós, M., Farkas, A. E., Dedhia, P. H., Huang, S., Siuda, D., García-Hernández, V., Miller, A. J., Spence, J. R., Nusrat, A., et al. (2017) · Nature Cell Biology · doi:10.1038/ncb3632 · Cited by 558 · see citing works
Self-citationCorrò, C., Novellasdemunt, L., & Li, V. S. W. (2020) · American Journal of Physiology-Cell Physiology · doi:10.1152/ajpcell.00120.2020 · Cited by 561 · see citing works
Engineered materials for organoid systems
Kratochvil, M. J., Seymour, A. J., Li, T. L., Pașca, S. P., Kuo, C. J., & Heilshorn, S. C. (2019) · Nature Reviews Materials · doi:10.1038/s41578-019-0129-9 · Cited by 413 · see citing works
Towards organoid culture without Matrigel
Kozlowski, M. T., Crook, C. J., & Ku, H. T. (2021) · Communications Biology · doi:10.1038/s42003-021-02910-8 · Cited by 409 · see citing works
Microbial Metabolite Signaling Is Required for Systemic Iron Homeostasis
Das, N. K., Schwartz, A. J., Barthel, G., Inohara, N., Liu, Q., Sankar, A., Hill, D. R., Ma, X., Lamberg, O., Schnizlein, M. K., et al. (2020) · Cell Metabolism · doi:10.1016/j.cmet.2019.10.005 · Cited by 331 · see citing works
Self-citationOrganoid Models of Human Gastrointestinal Development and Disease
Dedhia, P. H., Bertaux‐Skeirik, N., Zavros, Y. L., & Spence, J. R. (2016) · Gastroenterology · doi:10.1053/j.gastro.2015.12.042 · Cited by 246 · see citing works
Self-citationEngineering Multi‐Cellular Spheroids for Tissue Engineering and Regenerative Medicine
Kim, S., Kim, E. M., Yamamoto, M., Park, H., & Shin, H. (2020) · Advanced Healthcare Materials · doi:10.1002/adhm.202000608 · Cited by 233 · see citing works
Nonadhesive Alginate Hydrogels Support Growth of Pluripotent Stem Cell-Derived Intestinal Organoids
Capeling, M. M., Czerwinski, M., Huang, S., Tsai, Y.-H., Wu, A., Nagy, M. S., Juliar, B., Sundaram, N., Song, Y., Han, W. M., et al. (2019) · Stem Cell Reports · doi:10.1016/j.stemcr.2018.12.001 · Cited by 226 · see citing works
Self-citationDye, B. R., Dedhia, P. H., Miller, A. J., Nagy, M. S., White, E. S., Shea, L. D., & Spence, J. R. (2016) · eLife · doi:10.7554/elife.19732 · Cited by 191 · see citing works
Self-citationIn Vitro Models to Study Human Lung Development, Disease and Homeostasis.
Miller, A. J., & Spence, J. (2017) · Physiology · doi:10.1152/physiol.00041.2016 · Cited by 166 · see citing works
Self-citationHill, D. R., Huang, S., Nagy, M. S., Yadagiri, V. K., Fields, C., Thornhill, D., Bons, B., Dedhia, P. H., Chin, A. M., Tsai, Y.-H., et al. (2017) · eLife · doi:10.7554/elife.29132 · Cited by 173 · see citing works
Self-citationBarrila, J., Crabbé, A., Yang, J., Franco, K., Nydam, S. D., Forsyth, R. J., Davis, R. R., Gangaraju, S., Ott, C. M., Coyne, C. B., et al. (2018) · Infection and Immunity · doi:10.1128/iai.00282-18 · Cited by 159 · see citing works
Charting human development using a multi-endodermal organ atlas and organoid models
Yu, Q., Kilik, U., Holloway, E. M., Tsai, Y.-H., Harmel, C., Wu, A., Wu, J. H., Czerwinski, M. J., Childs, C. J., He, Z., et al. (2021) · Cell · doi:10.1016/j.cell.2021.04.028 · Cited by 145 · see citing works
Self-citationGut organoids: mini-tissues in culture to study intestinal physiology and disease
Almeqdadi, M., Mana, M., Roper, J., & Yilmaz, Ö. H. (2019) · American Journal of Physiology-Cell Physiology · doi:10.1152/ajpcell.00300.2017 · Cited by 151 · see citing works
Meran, L., Massie, I., Campinoti, S., Weston, A. E., Gaifulina, R., Tullie, L., Faull, P., Orford, M., Kucharska, A., Baulies, A., et al. (2020) · Nature Medicine · doi:10.1038/s41591-020-1024-z · Cited by 143 · see citing works
Laurent, J., Blin, G., Chatelain, F., Vanneaux, V., Fuchs, A., Larghero, J., & Théry, M. (2017) · Nature Biomedical Engineering · doi:10.1038/s41551-017-0166-x · Cited by 117 · see citing works
Differentiation of Human Intestinal Organoids with Endogenous Vascular Endothelial Cells
Holloway, E. M., Wu, J. H., Czerwinski, M. J., Sweet, C. W., Wu, A., Tsai, Y.-H., Huang, S., Stoddard, A. E., Capeling, M. M., Glass, I. A., et al. (2020) · Developmental Cell · doi:10.1016/j.devcel.2020.07.023 · Cited by 125 · see citing works
Self-citationProgress in biomaterials inspired by the extracellular matrix
Chen, Z., Du, C., Liu, S., Liu, J., Yang, Y., Dong, L., Zhao, W., Huang, W., & Lei, Y. (2024) · Giant · doi:10.1016/j.giant.2024.100323 · Cited by 132 · see citing works
Advancing Intestinal Organoid Technology Toward Regenerative Medicine
Nakamura, T., & Sato, T. (2017) · Cellular and Molecular Gastroenterology and Hepatology · doi:10.1016/j.jcmgh.2017.10.006 · Cited by 118 · see citing works
Schlieve, C. R., Fowler, K. L., Thornton, M. E., Huang, S., Hajjali, I., Hou, X., Grubbs, B. H., Spence, J. R., & Grikscheit, T. C. (2017) · Stem Cell Reports · doi:10.1016/j.stemcr.2017.07.017 · Cited by 115 · see citing works
Self-citationInduced organoids derived from patients with ulcerative colitis recapitulate colitic reactivity
Sarvestani, S. K., Signs, S. A., Hu, B., Yeu, Y., Feng, H., Ni, Y., Hill, D. R., Fisher, R. C., Ferrandon, S., DeHaan, R. K., et al. (2021) · Nature Communications · doi:10.1038/s41467-020-20351-5 · Cited by 113 · see citing works
Self-citationBacterial cellulose as a potential biopolymer in biomedical applications: a state-of-the-art review
Shrivastav, P., Pramanik, S., Vaidya, G., Abdelgawad, M. A., Ghoneim, M. M., SINGH, A. K., Abualsoud, B. M., Amaral, L. S., & Abourehab, M. A. S. (2022) · Journal of Materials Chemistry B · doi:10.1039/d1tb02709c · Cited by 116 · see citing works
Bioengineering of functional human induced pluripotent stem cell-derived intestinal grafts
Kitano, K., Schwartz, D. M., Zhou, H., Gilpin, S. E., Wojtkiewicz, G. R., Ren, X., Sommer, C., Capilla, A., Mathisen, D. J., Goldstein, A. M., et al. (2017) · Nature Communications · doi:10.1038/s41467-017-00779-y · Cited by 112 · see citing works
Innervation: the missing link for biofabricated tissues and organs
Das, S., Gordián‐Vélez, W. J., Ledebur, H. C., Mourkioti, F., Rompolas, P., Chen, H.-C. I., Serruya, M. D., & Cullen, D. K. (2020) · npj Regenerative Medicine · doi:10.1038/s41536-020-0096-1 · Cited by 107 · see citing works
Intestinal organoids: A new paradigm for engineering intestinal epithelium in vitro
Rahmani, S., Breyner, N. M., Su, H.-M., Verdu, E. F., & Didar, T. F. (2019) · Biomaterials · doi:10.1016/j.biomaterials.2018.12.006 · Cited by 98 · see citing works
Onozato, D., Yamashita, M., Nakanishi, A., Akagawa, T., Kida, Y., Ogawa, I., Hashita, T., Iwao, T., & Matsunaga, T. (2018) · Drug Metabolism and Disposition · doi:10.1124/dmd.118.080374 · Cited by 99 · see citing works
Biologically inspired approaches to enhance human organoid complexity
Holloway, E. M., Capeling, M. M., & Spence, J. R. (2019) · Development · doi:10.1242/dev.166173 · Cited by 96 · see citing works
Self-citationOrgan-on-Chip Approaches for Intestinal 3D In Vitro Modeling
Pimenta, J. M., Ribeiro, R. D. C., Almeida, R., Costa, P. F., da Silva, M. A., & Pereira, B. (2021) · Cellular and Molecular Gastroenterology and Hepatology · doi:10.1016/j.jcmgh.2021.08.015 · Cited by 92 · see citing works
Gastrointestinal Organoids: Understanding the Molecular Basis of the Host–Microbe Interface
Hill, D. R., & Spence, J. R. (2016) · Cellular and Molecular Gastroenterology and Hepatology · doi:10.1016/j.jcmgh.2016.11.007 · Cited by 87 · see citing works
Self-citationTsai, Y.-H., Nattiv, R., Dedhia, P. H., Nagy, M. S., Chin, A. M., Thomson, M., Klein, O. D., & Spence, J. R. (2016) · Development · doi:10.1242/dev.138453 · Cited by 87 · see citing works
Self-citationHuman Microphysiological Models of Intestinal Tissue and Gut Microbiome
Steinway, S. N., Saleh, J., Koo, B., Delacour, D., & Kim, D. (2020) · Frontiers in Bioengineering and Biotechnology · doi:10.3389/fbioe.2020.00725 · Cited by 79 · see citing works
Human Pluripotent Stem Cell-Derived Endoderm for Modeling Development and Clinical Applications
Yiangou, L., Ross, A., Goh, K. J., & Vallier, L. (2018) · Cell stem cell · doi:10.1016/j.stem.2018.03.016 · Cited by 76 · see citing works
Wallach, T. E., & Bayrer, J. R. (2016) · Journal of Pediatric Gastroenterology and Nutrition · doi:10.1097/mpg.0000000000001411 · Cited by 72 · see citing works
hPSC-derived lung and intestinal organoids as models of human fetal tissue
Aurora, M., & Spence, J. R. (2016) · Developmental Biology · doi:10.1016/j.ydbio.2016.06.006 · Cited by 69 · see citing works
Self-citationMing, Y., Hao, S., Wang, F., Lewis‐Israeli, Y. R., Volmert, B. D., Xu, Z., Goestenkors, A. P., Aguirre, A., & Zhou, C. (2022) · Biosensors and Bioelectronics · doi:10.1016/j.bios.2022.114136 · Cited by 68 · see citing works
Standardization and consensus in the development and application of bone organoids
Jian, W., Chen, X., Li, R., Wang, S., Geng, Z., Shi, Z., Jing, Y., Xu, K., Wei, Y., Wang, G., et al. (2024) · Theranostics · doi:10.7150/thno.105840 · Cited by 72 · see citing works
Repair and regeneration of small intestine: A review of current engineering approaches
Qi, D., Shi, W., Black, A. R., Kuss, M. A., Pang, X., He, Y., Liu, B., & Duan, B. (2020) · Biomaterials · doi:10.1016/j.biomaterials.2020.119832 · Cited by 59 · see citing works
Li, X., Chen, M., Zhao, S., & Wang, X. (2021) · Stem Cell Reviews and Reports · doi:10.1007/s12015-021-10205-y · Cited by 61 · see citing works
Norovirus replication, host interactions and vaccine advances
Prasad, B. V. V., Atmar, R. L., Ramani, S., Palzkill, T. G., Song, Y., Crawford, S. E., & Estes, M. K. (2025) · Nature Reviews Microbiology · doi:10.1038/s41579-024-01144-9 · Cited by 62 · see citing works
Advances in modelling the human microbiome–gut–brain axis in vitro
Moysidou, C., & Owens, R. M. (2021) · Biochemical Society Transactions · doi:10.1042/bst20200338 · Cited by 60 · see citing works
Lamboni, L., Xu, C., Clasohm, J., Yang, J., Saumer, M., Schäfer, K., & Yang, G. (2019) · Materials Science and Engineering C · doi:10.1016/j.msec.2019.04.043 · Cited by 57 · see citing works
Engineered organoids for biomedical applications
de Barros, N. R., Wang, C., Maity, S., Peirsman, A., Nasiri, R., Herland, A., Ermis, M., Kawakita, S., de Carvalho, B. G., Kouchehbaghi, N. H., et al. (2023) · Advanced Drug Delivery Reviews · doi:10.1016/j.addr.2023.115142 · Cited by 56 · see citing works
Self-citationBioinks for jet-based bioprinting
Zhou, D., Chen, J., Liu, B., Zhang, X., Li, X., & Xu, T. (2019) · Bioprinting · doi:10.1016/j.bprint.2019.e00060 · Cited by 54 · see citing works
Advancing Organoid Engineering for Tissue Regeneration and Biofunctional Reconstruction
Jin, H., Xue, Z., Liu, J., Ma, B., Yang, J., & Lei, L. (2024) · Biomaterials Research · doi:10.34133/bmr.0016 · Cited by 53 · see citing works
Tissue-Engineering the Intestine: The Trials before the Trials
Clevers, H. C., Conder, R. K., Li, V. S. W., Lütolf, M. P., Vallier, L., Chan, S., Grikscheit, T. C., Jensen, K. B., & Coppi, P. D. (2019) · Cell stem cell · doi:10.1016/j.stem.2019.04.018 · Cited by 53 · see citing works
Self-citationDickman, C. T., Russo, V., Thain, K. R., Pan, S., Beyer, S., Walus, K., Getsios, S., Mohamed, T., & Wadsworth, S. J. (2019) · The FASEB Journal · doi:10.1096/fj.201901063rr · Cited by 53 · see citing works
Understanding the cellular origin and progression of esophageal cancer using esophageal organoids
Sachdeva, U. M., Shimonosono, M., Flashner, S. P., Cruz‐Acuña, R., Gabre, J. T., & Nakagawa, H. (2021) · Cancer Letters · doi:10.1016/j.canlet.2021.03.031 · Cited by 47 · see citing works
Das, N. K., Jain, C., Sankar, A. D., Schwartz, A. J., Santana-Codina, N., Solanki, S. A., Zhang, Z., Ma, X., Parimi, S., Rui, L., et al. (2022) · Blood · doi:10.1182/blood.2021013452 · Cited by 47 · see citing works
Liu, Y., Nelson, T., Chakroff, J., Cromeens, B. P., Johnson, J. K., Lannutti, J. J., & Besner, G. E. (2018) · Journal of Biomedical Materials Research Part B Applied Biomaterials · doi:10.1002/jbm.b.34169 · Cited by 47 · see citing works
Yadak, R., Breur, M., & Bugiani, M. (2019) · Orphanet Journal of Rare Diseases · doi:10.1186/s13023-019-1016-6 · Cited by 45 · see citing works
Meran, L., Tullie, L., Eaton, S. D., Coppi, P. D., & Li, V. S. W. (2022) · Nature Protocols · doi:10.1038/s41596-022-00751-1 · Cited by 44 · see citing works
Tissue Engineering Laboratory Models of the Small Intestine
Dosh, R. H., Jordan, N., Sammon, C., & Maitre, C. L. L. (2017) · Tissue Engineering Part B Reviews · doi:10.1089/ten.teb.2017.0276 · Cited by 42 · see citing works
Engineering anisotropic 3D tubular tissues with flexible thermoresponsive nanofabricated substrates
Williams, N. P., Rhodehamel, M., Yan, C., Smith, A. S. T., Jiao, A., Murry, C. E., Scatena, M., & Kim, D. (2020) · Biomaterials · doi:10.1016/j.biomaterials.2020.119856 · Cited by 41 · see citing works
Tissue engineering for the treatment of short bowel syndrome in children
Martin, L. Y., Ladd, M. R., Werts, A. D., Sodhi, C. P., March, J. C., & Hackam, D. J. (2017) · Pediatric Research · doi:10.1038/pr.2017.234 · Cited by 39 · see citing works
Examining the gut-liver axis in liver cancer using organoid models
Shek, D., Chen, D., Read, S. A., & Ahlenstiel, G. (2021) · Cancer Letters · doi:10.1016/j.canlet.2021.04.008 · Cited by 39 · see citing works
Engineered Synthetic Matrices for Human Intestinal Organoid Culture and Therapeutic Delivery
Mulero‐Russe, A., & Garcı́a, A. J. (2023) · Advanced Materials · doi:10.1002/adma.202307678 · Cited by 40 · see citing works
Recent progress in organoid culture to model intestinal epithelial barrier functions
Nakamura, T. (2018) · International Immunology · doi:10.1093/intimm/dxy065 · Cited by 38 · see citing works
Onozato, D., Akagawa, T., Kida, Y., Ogawa, I., Hashita, T., Iwao, T., & Matsunaga, T. (2020) · Biological and Pharmaceutical Bulletin · doi:10.1248/bpb.b20-00088 · Cited by 38 · see citing works
APOL1 and kidney cell function
Kumar, V., & Singhal, P. C. (2019) · American Journal of Physiology-Renal Physiology · doi:10.1152/ajprenal.00233.2019 · Cited by 34 · see citing works
Regenerative medicine: postnatal approaches
Tam, P. K. H., Wong, K. K. Y., Atala, A., Giobbe, G. G., Booth, C., Gruber, P. J., Mononen, M., Rafii, S., Rando, T. A., Vacanti, J. P., et al. (2022) · The Lancet Child & Adolescent Health · doi:10.1016/s2352-4642(22)00193-6 · Cited by 32 · see citing works
Self-citationLiver organoid culture methods
Hu, Y., Hu, X., Luo, J. C., Huang, J., Sun, Y., Li, H., Qiao, Y., Wu, H., Li, J., Zhou, L., et al. (2023) · Cell & Bioscience · doi:10.1186/s13578-023-01136-x · Cited by 33 · see citing works
Generation of Budding-Like Intestinal Organoids from Human Induced Pluripotent Stem Cells
Onozato, D., Ogawa, I., Kida, Y., Mizuno, S., Hashita, T., Iwao, T., & Matsunaga, T. (2021) · Journal of Pharmaceutical Sciences · doi:10.1016/j.xphs.2021.03.014 · Cited by 31 · see citing works
Engineered biomaterials in stem cell-based regenerative medicine
Zhu, F., Nie, G., & Liu, C. (2023) · Life Medicine · doi:10.1093/lifemedi/lnad027 · Cited by 32 · see citing works
Spheres of Influence: Insights into Salmonella Pathogenesis from Intestinal Organoids
Verma, S., Senger, S., Cherayil, B. J., & Faherty, C. S. (2020) · Microorganisms · doi:10.3390/microorganisms8040504 · Cited by 30 · see citing works
Priester, C., MacDonald, A., Dhar, M. S., & Bow, A. J. (2020) · Pharmaceuticals · doi:10.3390/ph13110344 · Cited by 32 · see citing works
Bioengineering for intestinal organoid cultures
Kim, G.-A., Spence, J. R., & Takayama, S. (2017) · Current Opinion in Biotechnology · doi:10.1016/j.copbio.2017.05.006 · Cited by 30 · see citing works
Self-citationBuilding gut from scratch — progress and update of intestinal tissue engineering
Tullie, L., Jones, B. C., De Coppi, P., & Li, V. S. W. (2022) · Nature Reviews Gastroenterology & Hepatology · doi:10.1038/s41575-022-00586-x · Cited by 27 · see citing works
Inflammatory Bowel Disease: Pathophysiology, Treatment, and Disease Modeling
Jang, J., & Jeong, S. (2023) · BioChip Journal · doi:10.1007/s13206-023-00118-y · Cited by 29 · see citing works
Intestinal organoids in infants and children
Chusilp, S., Li, B., Lee, D., Lee, C., Vejchapipat, P., & Pierro, A. (2019) · Pediatric Surgery International · doi:10.1007/s00383-019-04581-3 · Cited by 28 · see citing works
Zhu, Z., Cheng, Y., Liu, X., Ding, W., Liu, J., Ling, Z., & Wu, L. (2025) · Cell Transplantation · doi:10.1177/09636897241303271 · Cited by 27 · see citing works
Seeger, B. (2020) · Alternatives to Laboratory Animals · doi:10.1177/0261192920974026 · Cited by 27 · see citing works
Engineering mechanobiology through organoids‐on‐chip: A strategy to boost therapeutics
Charelli, L. E., Ferreira, J. P. D., Naveira‐Cotta, C. P., & Balbino, T. A. (2021) · Journal of Tissue Engineering and Regenerative Medicine · doi:10.1002/term.3234 · Cited by 27 · see citing works
Tissue engineering of the gastrointestinal tract: the historic path to translation
Collier, C. A., Mendiondo, C., & Raghavan, S. A. (2022) · Journal of Biological Engineering · doi:10.1186/s13036-022-00289-6 · Cited by 27 · see citing works
LGR4 and LGR5 Function Redundantly During Human Endoderm Differentiation
Tsai, Y.-H., Hill, D. R., Kumar, N., Huang, S., Chin, A. M., Dye, B. R., Nagy, M. S., Verzi, M. P., & Spence, J. R. (2016) · Cellular and Molecular Gastroenterology and Hepatology · doi:10.1016/j.jcmgh.2016.06.002 · Cited by 27 · see citing works
Self-citationGrandi, F., Stocco, E., Barbon, S., Rambaldo, A., Contran, M., Leon, F. F., Gamba, P., Parnigotto, P. P., Macchi, V., De, R., et al. (2018) · BioMed Research International · doi:10.1155/2018/7824757 · Cited by 26 · see citing works
Taming the Wild West of Organoids, Enteroids, and Mini-Guts
Spence, J. R. (2018) · Cellular and Molecular Gastroenterology and Hepatology · doi:10.1016/j.jcmgh.2017.11.003 · Cited by 24 · see citing works
Self-citationTowards better models and mechanistic biomarkers for drug-induced gastrointestinal injury
Carr, D. F., Ayehunie, S., Davies, A., Duckworth, C. A., French, S., Hall, N., Hussain, S. A., Mellor, H. R., Norris, A. M., Park, B. K., et al. (2017) · Pharmacology & Therapeutics · doi:10.1016/j.pharmthera.2017.01.002 · Cited by 25 · see citing works
Wilmes, P., Calatayud, M., & Tom, V. D. W. (2018) · Current Opinion in Microbiology · doi:10.1016/j.mib.2018.07.001 · Cited by 23 · see citing works
Pednekar, D. D., Liguori, M., Marques, C. N. H., Zhang, T., Zhang, N., Zhou, Z., Amoako, K. A., & Gu, H. (2022) · ACS Biomaterials Science & Engineering · doi:10.1021/acsbiomaterials.2c00182 · Cited by 22 · see citing works
Pan, T., Chen, Y., Zhuang, Y., Yang, F., Xu, Y., Tao, J., You, K., Wang, N., Wu, Y., Lin, X.-H., et al. (2019) · Stem Cell Research & Therapy · doi:10.1186/s13287-019-1463-y · Cited by 21 · see citing works
Regenerative medicine technologies applied to transplant medicine. An update
Petrosyan, A., Montali, F., Peloso, A., Citro, A., Byers, L. N., Pointe, C. L., Suleiman, M., Marchetti, A., McNeill, E. P., Speer, A. L., et al. (2022) · Frontiers in Bioengineering and Biotechnology · doi:10.3389/fbioe.2022.1015628 · Cited by 22 · see citing works
Schwartz, D. M., Kara, M. O. P., Goldstein, A. M., Ott, H. C., & Ekenseair, A. K. (2017) · Tissue Engineering Part C Methods · doi:10.1089/ten.tec.2017.0269 · Cited by 21 · see citing works
A Comparison of Sterilization Techniques for Production of Decellularized Intestine in Mice
Gosztyla, C. E., Ladd, M. R., Werts, A. D., Fulton, W. B., Johnson, B. A., Sodhi, C. P., & Hackam, D. J. (2019) · Tissue Engineering Part C Methods · doi:10.1089/ten.tec.2019.0219 · Cited by 21 · see citing works
Stem Cell-Derived Models of Viral Infections in the Gastrointestinal Tract
Lanik, W. E., Mara, M., Mihi, B., Coyne, C. B., & Good, M. L. (2018) · Viruses · doi:10.3390/v10030124 · Cited by 18 · see citing works
Chan, W. S., Mo, X.-T., Ip, P. P. C., & Tse, K. Y. (2023) · Cancer Medicine · doi:10.1002/cam4.6521 · Cited by 18 · see citing works
Intestinal organoids: roadmap to the clinic
Kasendra, M. J., Troutt, M. L., Broda, T. R., Bacon, W. C., Wang, T. C., Niland, J. C., & Helmrath, M. A. (2021) · American Journal of Physiology-Gastrointestinal and Liver Physiology · doi:10.1152/ajpgi.00425.2020 · Cited by 18 · see citing works
Saito‐Diaz, K., & Zeltner, N. (2019) · Clinical Autonomic Research · doi:10.1007/s10286-018-00587-4 · Cited by 18 · see citing works
Hung, Y.-H., Huang, S., Dame, M. K., Yu, Q., Yu, Q. C., Zeng, Y. A., Camp, J. G., Spence, J. R., & Sethupathy, P. (2020) · Nucleic Acids Research · doi:10.1093/nar/gkaa1204 · Cited by 18 · see citing works
Self-citationMaterials and Microenvironments for Engineering the Intestinal Epithelium
Snyder, J. R., Wang, C.-M., Zhang, A. Q., Li, Y., Luchan, J., Hosic, S., Koppes, R. A., Carrier, R. L., & Koppes, A. N. (2020) · Annals of Biomedical Engineering · doi:10.1007/s10439-020-02470-8 · Cited by 18 · see citing works
Chang, D. F., Zuber, S. M., Gilliam, E. A., Nucho, L.-M. A., Levin, G., Wang, F., Squillaro, A. I., Huang, S., Spence, J. R., & Grikscheit, T. C. (2020) · Journal of Tissue Engineering · doi:10.1177/2041731420905701 · Cited by 15 · see citing works
Self-citationJurj, A. M., Paşca, S., Braicu, C., Rusu, I., Korban, S. S., & Berindan‐Neagoe, I. (2021) · Seminars in Cancer Biology · doi:10.1016/j.semcancer.2021.12.002 · Cited by 15 · see citing works
Bioengineering toolkits for potentiating organoid therapeutics
Park, S., & Cho, S. (2024) · Advanced Drug Delivery Reviews · doi:10.1016/j.addr.2024.115238 · Cited by 15 · see citing works
Kumar, D., Gupta, S., Gupta, V., Tanwar, R., & Chandel, A. (2025) · Stem Cell Reviews and Reports · doi:10.1007/s12015-025-10893-w · Cited by 17 · see citing works
Tissue Engineering for Gastrointestinal and Genitourinary Tracts
Elia, E., Brownell, D., Chabaud, S., & Bolduc, S. (2022) · International Journal of Molecular Sciences · doi:10.3390/ijms24010009 · Cited by 13 · see citing works
Levin, G., Zuber, S. M., Squillaro, A. I., Sogayar, M. C., Grikscheit, T. C., & Carreira, A. C. O. (2020) · Frontiers in Bioengineering and Biotechnology · doi:10.3389/fbioe.2020.00476 · Cited by 14 · see citing works
Self-citationCombating COVID-19 with tissue engineering: a review
Aydin, A., Çebi, G., Demirtas, Z. E., Erkus, H., Kucukay, A., Ok, M., Sakalli, L., Alpdağtaş, S., Gündüz, O., & Üstündağ, C. B. (2020) · Emergent Materials · doi:10.1007/s42247-020-00138-6 · Cited by 13 · see citing works
Plumbing our organs: Lessons from vascular development to instruct lab generated tissues
Ryan, A. R., & Cleaver, O. B. (2022) · Current topics in developmental biology/Current Topics in Developmental Biology · doi:10.1016/bs.ctdb.2022.02.013 · Cited by 12 · see citing works
Bao, L., Cui, X., Bai, R., & Chen, C. (2022) · Nano Research · doi:10.1007/s12274-022-5150-4 · Cited by 12 · see citing works
Using 3D Organoid Cultures to Model Intestinal Physiology and Colorectal Cancer
Short, S. P., Costacurta, P. W., & Williams, C. S. (2017) · Current Colorectal Cancer Reports · doi:10.1007/s11888-017-0363-8 · Cited by 13 · see citing works
Hou, X., Chang, D. F., Trecartin, A., Barthel, E. R., Schlieve, C. R., Frey, M. R., Fowler, K. L., & Grikscheit, T. C. (2018) · Experimental Physiology · doi:10.1113/ep086990 · Cited by 13 · see citing works
Self-citation
- Authors
- Finkbeiner, S. R., Freeman, J. J., Wieck, M. M., El-Nachef, W., Altheim, C. H., Tsai, Y.-H., Huang, S., Dyal, R., White, E. S., Grikscheit, T. C., Teitelbaum, D. H., & Spence, J. R.
- Affiliations
- University of Michigan (US)
- Children's Hospital Los Angeles (US)
- Corresponding author
- Spence, Jason R.
- ORCID
- Venue
- Biology Open
- Publisher
- The Company of Biologists
- Published
- 2015-10-12
- Volume
- 4
- Issue
- 11
- Pages
- 1462-1472
- ISSN
- 2046-6390 (ISSN-L)
- PMC
- PMC4728347
- OpenAlex
- W2261291226
- Cited by
- 174
- References
- 82
- Citations by year
- 2026: 4 · 2025: 11 · 2024: 7 · 2023: 12 · 2022: 17 · 2021: 24 · 2020: 31 · 2019: 20 · 2018: 18 · 2017: 20 · 2016: 10
- FWCI
- 16.13
- Type
- journal article
- Language
- en
- Open access
- gold
- doi.org
- Locations
- Biology Open (publishedVersion, cc-by)
- PubMed Central (publishedVersion, cc-by)
- PubMed (publishedVersion)
- DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
- eScholarship (California Digital Library) (submittedVersion, cc-by)
- Funders
- California Institute for Regenerative Medicine (RN3-06425)
- Hartwell Foundation
- National Institutes of Health (UL1TR000433, DK034933)
- Harvard Stem Cell Institute
- National Institute of Diabetes and Digestive and Kidney Diseases (U24DK085532, P30DK034933, DK 034933, K01DK091415, U01DK085532, U01DK103141, T32DK094775)
- National Center for Advancing Translational Sciences
- Eunice Kennedy Shriver National Institute of Child Health and Human Development (T32HD007505)
- Topics
- Health Sciences › Medicine › Surgery › Tissue Engineering and Regenerative Medicine
- Physical Sciences › Engineering › Biomedical Engineering › 3D Printing in Biomedical Research
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Pluripotent Stem Cells Research
- Keywords
- human intestinal organoids, embryonic stem cells, short bowel syndrome, intestinal regeneration, in vivo transplantation
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