Organoids: A historical perspective of thinking in three dimensions
Abstract
In the last ten years, there has been a dramatic surge in the number of publications where single or groups of cells are grown in substrata that have elements of basement membrane leading to the formation of tissue-like structures referred to as organoids. However, this field of research began many decades ago, when the pioneers of cell culture began to ask questions we still ask today: How does organogenesis occur? How do signals integrate to make such vastly different tissues and organs given that the sequence of the genome in our trillions of cells is identical? Here, we summarize how work over the past century generated the conceptual framework that has allowed us to make progress in the understanding of tissue-specific morphogenetic programs. The development of cell culture systems that provide accurate and physiologically relevant models are proving to be key in establishing appropriate platforms for the development of new therapeutic strategies.
- Authors:
- Publication Date:
- Research Org.:
- Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States)
- Sponsoring Org.:
- USDOE Office of Science (SC)
- OSTI Identifier:
- 1340023
- Alternate Identifier(s):
- OSTI ID: 1379625
- Grant/Contract Number:
- AC02-05CH11231
- Resource Type:
- Published Article
- Journal Name:
- Journal of Cell Biology
- Additional Journal Information:
- Journal Name: Journal of Cell Biology Journal Volume: 216 Journal Issue: 1; Journal ID: ISSN 0021-9525
- Publisher:
- Rockefeller University Press
- Country of Publication:
- United States
- Language:
- English
- Subject:
- 59 BASIC BIOLOGICAL SCIENCES
Citation Formats
Simian, Marina, and Bissell, Mina J. Organoids: A historical perspective of thinking in three dimensions. United States: N. p., 2016.
Web. doi:10.1083/jcb.201610056.
Simian, Marina, & Bissell, Mina J. Organoids: A historical perspective of thinking in three dimensions. United States. https://doi.org/10.1083/jcb.201610056
Simian, Marina, and Bissell, Mina J. Wed .
"Organoids: A historical perspective of thinking in three dimensions". United States. https://doi.org/10.1083/jcb.201610056.
@article{osti_1340023,
title = {Organoids: A historical perspective of thinking in three dimensions},
author = {Simian, Marina and Bissell, Mina J.},
abstractNote = {In the last ten years, there has been a dramatic surge in the number of publications where single or groups of cells are grown in substrata that have elements of basement membrane leading to the formation of tissue-like structures referred to as organoids. However, this field of research began many decades ago, when the pioneers of cell culture began to ask questions we still ask today: How does organogenesis occur? How do signals integrate to make such vastly different tissues and organs given that the sequence of the genome in our trillions of cells is identical? Here, we summarize how work over the past century generated the conceptual framework that has allowed us to make progress in the understanding of tissue-specific morphogenetic programs. The development of cell culture systems that provide accurate and physiologically relevant models are proving to be key in establishing appropriate platforms for the development of new therapeutic strategies.},
doi = {10.1083/jcb.201610056},
journal = {Journal of Cell Biology},
number = 1,
volume = 216,
place = {United States},
year = {Wed Dec 28 00:00:00 EST 2016},
month = {Wed Dec 28 00:00:00 EST 2016}
}
https://doi.org/10.1083/jcb.201610056
Web of Science
Works referenced in this record:
Fibroblast surface antigen: A new serum protein
journal, October 1973
- Ruoslahti, Erkki; Vaheri, Antti; Kuusela, Pentti
- Biochimica et Biophysica Acta (BBA) - Protein Structure, Vol. 322, Issue 2
In vitro expansion of single Lgr5+ liver stem cells induced by Wnt-driven regeneration
journal, January 2013
- Huch, Meritxell; Dorrell, Craig; Boj, Sylvia F.
- Nature, Vol. 494, Issue 7436
The interplay of matrix metalloproteinases, morphogens and growth factors is necessary for branching of mammary epithelial cells
journal, August 2001
- Simian, Marina; Hirai, Yohei; Navre, Marc
- Development, Vol. 128, Issue 16
Proliferating Pigment Epithelium: Producing a Simple Organoid Structure in the Subrentinal Space of a Human Eye
journal, May 1967
- Wolter, J. Reimer
- Archives of Ophthalmology, Vol. 77, Issue 5
Tissue Geometry Determines Sites of Mammary Branching Morphogenesis in Organotypic Cultures
journal, October 2006
- Nelson, C. M.; VanDuijn, M. M.; Inman, J. L.
- Science, Vol. 314, Issue 5797
Organoid-on-a-chip and body-on-a-chip systems for drug screening and disease modeling
journal, September 2016
- Skardal, Aleksander; Shupe, Thomas; Atala, Anthony
- Drug Discovery Today, Vol. 21, Issue 9
Experimental Studies on the Differentiation of Embryonic Tissues Growing in vivo and in vitro.--II. The Development of the Isolated Early Embryonic Eye of the Fowl when Cultivated in vitro
journal, September 1926
- Strangeways, T. S. P.; Fell, H. B.
- Proceedings of the Royal Society B: Biological Sciences, Vol. 100, Issue 703
EXPERIMENTS ON LYMPH NODES COLTURED IN VITRO
journal, March 1955
- Trowell, O. A.
- Annals of the New York Academy of Sciences, Vol. 59, Issue 5
Cerebral organoids model human brain development and microcephaly
journal, August 2013
- Lancaster, Madeline A.; Renner, Magdalena; Martin, Carol-Anne
- Nature, Vol. 501, Issue 7467
Collective Epithelial Migration and Cell Rearrangements Drive Mammary Branching Morphogenesis
journal, April 2008
- Ewald, Andrew J.; Brenot, Audrey; Duong, Myhanh
- Developmental Cell, Vol. 14, Issue 4
Isolation and Characterization of Proteinase and Collagenase from cl. Histolyticum 12
journal, December 1953
- Mandl, Ines; MacLennan, John D.; Howes, Edward L.
- Journal of Clinical Investigation, Vol. 32, Issue 12
Lumen formation by epithelial cell lines in response to collagen overlay: a morphogenetic model in culture.
journal, August 1982
- Hall, H. G.; Farson, D. A.; Bissell, M. J.
- Proceedings of the National Academy of Sciences, Vol. 79, Issue 15
Long-term Expansion of Epithelial Organoids From Human Colon, Adenoma, Adenocarcinoma, and Barrett's Epithelium
journal, November 2011
- Sato, Toshiro; Stange, Daniel E.; Ferrante, Marc
- Gastroenterology, Vol. 141, Issue 5
Epimorphin: A mesenchymal protein essential for epithelial morphogenesis
journal, May 1992
- Hirai, Yohei; Takebe, Kyoko; Takashina, Makoto
- Cell, Vol. 69, Issue 3
Lgr5+ve Stem Cells Drive Self-Renewal in the Stomach and Build Long-Lived Gastric Units In Vitro
journal, January 2010
- Barker, Nick; Huch, Meritxell; Kujala, Pekka
- Cell Stem Cell, Vol. 6, Issue 1
Growth of exocrine acinar cells on a reconstituted basement membrane gel
journal, July 1987
- Oliver, Constance; Waters, Judith F.; Tolbert, Carolyn L.
- In Vitro Cellular & Developmental Biology, Vol. 23, Issue 7
Laminin–a glycoprotein from basement membranes.
journal, October 1979
- Timpl, R.; Rohde, H.; Robey, P. G.
- Journal of Biological Chemistry, Vol. 254, Issue 19
Division of Labor among the α6β4 Integrin, β1 Integrins, and an E3 Laminin Receptor to Signal Morphogenesis and β-Casein Expression in Mammary Epithelial Cells
journal, September 1999
- Muschler, John; Lochter, André; Roskelley, Calvin D.
- Molecular Biology of the Cell, Vol. 10, Issue 9
Altered Growth Behavior of Malignant Cells Associated with Changes in Externally Labeled Glycoprotein and Glycolipid
journal, December 1973
- Gahmberg, C. G.; Hakomori, S. -I.
- Proceedings of the National Academy of Sciences, Vol. 70, Issue 12
Induced Pluripotent Stem Cell Lines Derived from Human Somatic Cells
journal, December 2007
- Yu, J.; Vodyanik, M. A.; Smuga-Otto, K.
- Science, Vol. 318, Issue 5858
Morphology and Function of Cells of Human Embryonic Liver in Monolayer Culture
journal, July 1971
- Bissell, D. M.
- The Journal of Cell Biology, Vol. 50, Issue 1
The MAPKERK-1,2 pathway integrates distinct and antagonistic signals from TGFα and FGF7 in morphogenesis of mouse mammary epithelium
journal, June 2007
- Fata, Jimmie E.; Mori, Hidetoshi; Ewald, Andrew J.
- Developmental Biology, Vol. 306, Issue 1
β4 integrin-dependent formation of polarized three-dimensional architecture confers resistance to apoptosis in normal and malignant mammary epithelium
journal, September 2002
- Weaver, Valerie M.; Lelièvre, Sophie; Lakins, Johnathon N.
- Cancer Cell, Vol. 2, Issue 3
On some phenomena of coalescence and regeneration in sponges
journal, December 1907
- Wilson, H. V.
- Journal of Experimental Zoology, Vol. 5, Issue 2
Modeling Development and Disease with Organoids
journal, June 2016
- Clevers, Hans
- Cell, Vol. 165, Issue 7
Unlimited in vitro expansion of adult bi-potent pancreas progenitors through the Lgr5/R-spondin axis
journal, September 2013
- Huch, Meritxell; Bonfanti, Paola; Boj, Sylvia F.
- The EMBO Journal, Vol. 32, Issue 20
Alteration of Cell-Surface Proteins by Viral Transformation and by Proteolysis
journal, November 1973
- Hynes, R. O.
- Proceedings of the National Academy of Sciences, Vol. 70, Issue 11
Clonal and Population Analyses Demonstrate That an EGF-Responsive Mammalian Embryonic CNS Precursor Is a Stem Cell
journal, April 1996
- Reynolds, Brent A.; Weiss, Samuel
- Developmental Biology, Vol. 175, Issue 1
Organogenesis in a dish: Modeling development and disease using organoid technologies
journal, July 2014
- Lancaster, M. A.; Knoblich, J. A.
- Science, Vol. 345, Issue 6194
Tissue Culture and its Contribution to Biology and Medicine
journal, August 1972
- Fell, H. B.
- Journal of Experimental Biology, Vol. 57, Issue 1
A novel transcriptional enhancer is involved in the prolactin- and extracellular matrix-dependent regulation of beta-casein gene expression.
journal, June 1992
- Schmidhauser, C.; Casperson, G. F.; Myers, C. A.
- Molecular Biology of the Cell, Vol. 3, Issue 6
Induction of Pluripotent Stem Cells from Adult Human Fibroblasts by Defined Factors
journal, November 2007
- Takahashi, Kazutoshi; Tanabe, Koji; Ohnuki, Mari
- Cell, Vol. 131, Issue 5
Influence of collagen gel on the orientation of epithelial cell polarity: follicle formation from isolated thyroid cells and from preformed monolayers
journal, October 1981
- Chambard, M.
- The Journal of Cell Biology, Vol. 91, Issue 1
Cultivation and behavior in vitro of the normal mammary epithelium of the adult mouse
journal, January 1957
- Lasfargues, Etienne Y.
- The Anatomical Record, Vol. 127, Issue 1
How does the extracellular matrix direct gene expression?
journal, November 1982
- Bissell, Mina J.; Hall, H. Glenn; Parry, Gordon
- Journal of Theoretical Biology, Vol. 99, Issue 1
Exogenous basement-membrane-like matrix stimulates adrenergic development in avian neural crest cultures
journal, December 1987
- Maxwell, G. D.; Forbes, M. E.
- Development, Vol. 101, Issue 4
Single Lgr5 stem cells build crypt-villus structures in vitro without a mesenchymal niche
journal, March 2009
- Sato, Toshiro; Vries, Robert G.; Snippert, Hugo J.
- Nature, Vol. 459, Issue 7244
Regulation of gene expression in adult rat hepatocytes cultured on a basement membrane matrix
journal, March 1988
- Schuetz, Erin G.; Li, Donna; Omiecinski, Curtis J.
- Journal of Cellular Physiology, Vol. 134, Issue 3
A modified technique for organ culture in vitro
journal, January 1954
- Trowell, O. A.
- Experimental Cell Research, Vol. 6, Issue 1
Functional Culture Models to Study Mechanisms Governing Apoptosis in Normal and Malignant Mammary Epithelial Cells
journal, January 1999
- Weaver, V. M.; Bissell, M. J.
- Journal of Mammary Gland Biology and Neoplasia, Vol. 4, Issue 2, p. 193-201
Niche-to-niche migration of bone-marrow-derived cells
journal, February 2007
- Kaplan, Rosandra N.; Psaila, Bethan; Lyden, David
- Trends in Molecular Medicine, Vol. 13, Issue 2
A murine tumor producing a matrix of basement membrane
journal, January 1977
- Orkin, R. W.
- Journal of Experimental Medicine, Vol. 145, Issue 1
A Study of the Restitution Masses formed by the Dissociated Cells of the Hydroids Antennularia Ramosa and A. Antennina
journal, October 1914
- De Morgan, W.; Drew, late G. Harold
- Journal of the Marine Biological Association of the United Kingdom, Vol. 10, Issue 3
In vitro propagation and transcriptional profiling of human mammary stem/progenitor cells
journal, May 2003
- Dontu, G.
- Genes & Development, Vol. 17, Issue 10
Control of mammary epithelial differentiation: basement membrane induces tissue-specific gene expression in the absence of cell-cell interaction and morphological polarity
journal, December 1991
- Streuli, C. H.
- The Journal of Cell Biology, Vol. 115, Issue 5
The Cultivation of Tissues of the Chick-Embryo Outside the body
journal, December 1910
- Burrows, Montrose T.
- JAMA: The Journal of the American Medical Association, Vol. 55, Issue 24
The growth, development and phosphatase activity of embryonic avian femora and limb-buds cultivated in vitro
journal, January 1929
- Fell, Honor Bridget; Robison, Robert
- Biochemical Journal, Vol. 23, Issue 4
Reversion of the Malignant Phenotype of Human Breast Cells in Three-Dimensional Culture and In Vivo by Integrin Blocking Antibodies
journal, April 1997
- Weaver, V. M.; Petersen, O. W.; Wang, F.
- The Journal of Cell Biology, Vol. 137, Issue 1
Maintenance and induction of morphological differentiation in dissociated mammary epithelium on floating collagen membranes
journal, May 1977
- Emerman, Joanne T.; Pitelka, Dorothy R.
- In Vitro, Vol. 13, Issue 5
Support of cultured hepatocytes by a laminin-rich gel. Evidence for a functionally significant subendothelial matrix in normal rat liver.
journal, March 1987
- Bissell, D. M.; Arenson, D. M.; Maher, J. J.
- Journal of Clinical Investigation, Vol. 79, Issue 3
Interaction with basement membrane serves to rapidly distinguish growth and differentiation pattern of normal and malignant human breast epithelial cells.
journal, October 1992
- Petersen, O. W.; Ronnov-Jessen, L.; Howlett, A. R.
- Proceedings of the National Academy of Sciences, Vol. 89, Issue 19
Reciprocal interactions between 1-integrin and epidermal growth factor receptor in three-dimensional basement membrane breast cultures: A different perspective in epithelial biology
journal, December 1998
- Wang, F.; Weaver, V. M.; Petersen, O. W.
- Proceedings of the National Academy of Sciences, Vol. 95, Issue 25
Interaction of mouse mammary epithelial cells with collagen substrata: regulation of casein gene expression and secretion.
journal, March 1985
- Lee, E. Y.; Lee, W. H.; Kaetzel, C. S.
- Proceedings of the National Academy of Sciences, Vol. 82, Issue 5
Extracellular matrix and hormones transcriptionally regulate bovine beta-casein 5' sequences in stably transfected mouse mammary cells.
journal, December 1990
- Schmidhauser, C.; Bissell, M. J.; Myers, C. A.
- Proceedings of the National Academy of Sciences, Vol. 87, Issue 23
Modulation of secreted proteins of mouse mammary epithelial cells by the collagenous substrata
journal, January 1984
- Lee, E. Y.
- The Journal of Cell Biology, Vol. 98, Issue 1
Characterization of BCE-1, a Transcriptional Enhancer Regulated by Prolactin and Extracellular Matrix and Modulated by the State of Histone Acetylation
journal, April 1998
- Myers, Connie A.; Schmidhauser, Christian; Mellentin-Michelotti, Julia
- Molecular and Cellular Biology, Vol. 18, Issue 4
Distribution of a major connective tissue protein, fibronectin, in normal human tissues
journal, April 1978
- Stenman, S.
- Journal of Experimental Medicine, Vol. 147, Issue 4
Why don't we get more cancer? A proposed role of the microenvironment in restraining cancer progression
journal, March 2011
- Bissell, Mina J.; Hines, William C.
- Nature Medicine, Vol. 17, Issue 3
The Dynamic Duo: Niche/Stem Cell Interdependency
journal, June 2015
- Mesa, Kailin R.; Rompolas, Panteleimon; Greco, Valentina
- Stem Cell Reports, Vol. 4, Issue 6
Human Keratoconus Cell Contractility is Mediated by Transforming Growth Factor-Beta Isoforms
journal, June 2015
- Lyon, Desiree'; McKay, Tina; Sarkar-Nag, Akhee
- Journal of Functional Biomaterials, Vol. 6, Issue 2
Extracellular matrix regulates Sertoli cell differentiation, testicular cord formation, and germ cell development in vitro
journal, October 1985
- Hadley, M. A.
- The Journal of Cell Biology, Vol. 101, Issue 4
Nuclear and Cytoplasmic Organoids in the Living cell
journal, November 1954
- Duryee, William R.; Doherty, Josephine K.
- Annals of the New York Academy of Sciences, Vol. 58, Issue 7
Influence of a reconstituted basement membrane and its components on casein gene expression and secretion in mouse mammary epithelial cells.
journal, January 1987
- Li, M. L.; Aggeler, J.; Farson, D. A.
- Proceedings of the National Academy of Sciences, Vol. 84, Issue 1
Tissues from Dissociated Cells
journal, May 1959
- Moscona, A. A.
- Scientific American, Vol. 200, Issue 5
Cultivation of Adult Tissues and Organs Outside of the body
journal, October 1910
- Carrel, Alexis
- JAMA: The Journal of the American Medical Association, Vol. 55, Issue 16
Embryonic Stem Cell Lines Derived from Human Blastocysts
journal, November 1998
- Thomson, J. A.
- Science, Vol. 282, Issue 5391
Laminin mediates tissue-specific gene expression in mammary epithelia
journal, May 1995
- Streuli, C. H.
- The Journal of Cell Biology, Vol. 129, Issue 3
Of Microenvironments and Mammary Stem Cells
journal, August 2007
- LaBarge, Mark A.; Petersen, Ole W.; Bissell, Mina J.
- Stem Cell Reviews, Vol. 3, Issue 2
Functional differentiation and alveolar morphogenesis of primary mammary cultures on reconstituted basement membrane
journal, February 1989
- Barcellos-Hoff, M. H.; Aggeler, J.; Ram, T. G.
- Development, Vol. 105, Issue 2
A four-organ-chip for interconnected long-term co-culture of human intestine, liver, skin and kidney equivalents
journal, January 2015
- Maschmeyer, Ilka; Lorenz, Alexandra K.; Schimek, Katharina
- Lab on a Chip, Vol. 15, Issue 12
Dishing out mini-brains: Current progress and future prospects in brain organoid research
journal, December 2016
- Kelava, Iva; Lancaster, Madeline A.
- Developmental Biology, Vol. 420, Issue 2
Matrigel: Basement membrane matrix with biological activity
journal, October 2005
- Kleinman, Hynda K.; Martin, George R.
- Seminars in Cancer Biology, Vol. 15, Issue 5
Generation of human-induced pluripotent stem cells
journal, June 2008
- Park, In-Hyun; Lerou, Paul H.; Zhao, Rui
- Nature Protocols, Vol. 3, Issue 7
Hepatocyte growth factor stimulates extensive development of branching duct-like structures by cloned mammary gland epithelial cells
journal, February 1995
- Soriano, J. V.; Pepper, M. S.; Nakamura, T.
- Journal of Cell Science, Vol. 108, Issue 2
HIGH-YIELD PREPARATION OF ISOLATED RAT LIVER PARENCHYMAL CELLS: A Biochemical and Fine Structural Study
journal, December 1969
- Berry, M. N.
- The Journal of Cell Biology, Vol. 43, Issue 3
Self-Organized Formation of Polarized Cortical Tissues from ESCs and Its Active Manipulation by Extrinsic Signals
journal, November 2008
- Eiraku, Mototsugu; Watanabe, Kiichi; Matsuo-Takasaki, Mami
- Cell Stem Cell, Vol. 3, Issue 5
Organoids as an in vitro model of human development and disease
journal, February 2016
- Fatehullah, Aliya; Tan, Si Hui; Barker, Nick
- Nature Cell Biology, Vol. 18, Issue 3
Observations on the living developing nerve fiber
journal, August 1906
- Harrison, R. G.
- Experimental Biology and Medicine, Vol. 4, Issue 1
Reconstituted basement membrane promotes morphological and functional differentiation of primary human prostatic epithelial cells
journal, January 1991
- Fong, Chau-Jye; Sherwood, Edward R.; Sutkowski, Debra M.
- The Prostate, Vol. 19, Issue 3
Primary culture of parenchymal liver cells on collagen membranes
journal, August 1975
- Michalopoulos, G.; Pitot, H. C.
- Experimental Cell Research, Vol. 94, Issue 1
Establishment in culture of pluripotential cells from mouse embryos
journal, July 1981
- Evans, M. J.; Kaufman, M. H.
- Nature, Vol. 292, Issue 5819
Mammary epithelial tubes elongate through MAPK-dependent coordination of cell migration
journal, February 2016
- Huebner, Robert J.; Neumann, Neil M.; Ewald, Andrew J.
- Development, Vol. 143, Issue 6
TGF-β1Induces Morphogenesis of Branching Cords by Cloned Mammary Epithelial Cells at Subpicomolar Concentrations
journal, March 1996
- Soriano, J. V.; Orci, L.; Montesano, R.
- Biochemical and Biophysical Research Communications, Vol. 220, Issue 3
Expression of extracellular matrix components is regulated by substratum
journal, April 1990
- Steuli, C. H.
- The Journal of Cell Biology, Vol. 110, Issue 4
Chip-based human liver–intestine and liver–skin co-cultures – A first step toward systemic repeated dose substance testing in vitro
journal, September 2015
- Maschmeyer, Ilka; Hasenberg, Tobias; Jaenicke, Annika
- European Journal of Pharmaceutics and Biopharmaceutics, Vol. 95
Some unusual observations of organoid tissues and blood elements in monolayer cultures
journal, May 1963
- Schneider, H.; Muirhead, E. E.; Zydeck, F. A.
- Experimental Cell Research, Vol. 30, Issue 3
Self-organizing optic-cup morphogenesis in three-dimensional culture
journal, April 2011
- Eiraku, Mototsugu; Takata, Nozomu; Ishibashi, Hiroki
- Nature, Vol. 472, Issue 7341
Quantitative cine Analysis of cell Organoid Activity
journal, November 1954
- Pomerat, C. M.; Lefeber, C. G.; Smith, McD.
- Annals of the New York Academy of Sciences, Vol. 58, Issue 7
Three-dimensional organotypic culture: experimental models of mammalian biology and disease
journal, September 2014
- Shamir, Eliah R.; Ewald, Andrew J.
- Nature Reviews Molecular Cell Biology, Vol. 15, Issue 10
Self-Formation of Optic Cups and Storable Stratified Neural Retina from Human ESCs
journal, June 2012
- Nakano, Tokushige; Ando, Satoshi; Takata, Nozomu
- Cell Stem Cell, Vol. 10, Issue 6