Beta-catenin is selectively required for the expansion and regeneration of mature pancreatic acinar cells
Open accessAbstract
The size of the pancreas is determined by intrinsic factors, such as the number of progenitor cells, and by extrinsic signals that control the fate and proliferation of those progenitors. Both the exocrine and endocrine compartments of the pancreas undergo dramatic expansion after birth and are capable of at least partial regeneration following injury. Whether the expansion of these lineages relies on similar mechanisms is unknown. Although we have shown that the Wnt signaling component β-catenin is selectively required in mouse embryos for the generation of exocrine acinar cells, this protein has been ascribed various functions in the postnatal pancreas, including proliferation and regeneration of islet as well as acinar cells. To address whether β-catenin remains important for the maintenance and expansion of mature acinar cells, we have established a system to follow the behavior and fate of β-catenin-deficient cells during postnatal growth and regeneration in mice. We find that β-catenin is continuously required for the establishment and maintenance of acinar cell mass, extending from embryonic specification through juvenile and adult self-renewal and regeneration. This requirement is not shared with islet cells, which proliferate and function normally in the absence of β-catenin. These results make distinct predictions for the relative role of Wnt-β-catenin signaling in the etiology of human endocrine and exocrine disease. We suggest that loss of Wnt-β-catenin activity is unlikely to drive islet dysfunction, as occurs in type 2 diabetes, but that β-catenin is likely to promote human acinar cell proliferation following injury, and might therefore contribute to the resolution of acute or chronic pancreatitis.
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Augmented Hedgehog, Notch, and Wnt/b-catenin signaling are mandatory for regeneration in mice after experimental induction of pancreatitis.
“Among others, augmented Hedgehog, Notch, and Wnt/b-catenin signaling were delineated as mandatory for regeneration in mice after experimental induction of pancreatitis [21–24].”
From TBX3 is dynamically expressed in pancreatic organogenesis and fine-tunes regeneration (2023) · cites this paper as [24]
The Results section, ‘β-catenin is required for acinar cell proliferation during regeneration’ (page unavailable), reports reduced proliferation of β-catenin-deficient acinar cells after experimentally induced pancreatitis. The Introduction also reports that Notch1 and the Hedgehog component Smo are required for regeneration in this model. But the Discussion says the role of Wnt proteins themselves remains to be determined, and the paper does not establish that augmented signaling in all three pathways is mandatory for regeneration. (LLM, conf=0.87)
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Baumgartner, B. K., Cash, G. M., Hansen, H., Ostler, S., & Murtaugh, L. C. (2014) · Developmental Biology · doi:10.1016/j.ydbio.2014.03.019 · Cited by 38 · see citing works
Self-citationBmi1 Is Required for Regeneration of the Exocrine Pancreas in Mice
Fukuda, A., Morris, J. P., & Hebrok, M. (2012) · Gastroenterology · doi:10.1053/j.gastro.2012.05.009 · Cited by 37 · see citing works
Prevention and Reversion of Pancreatic Tumorigenesis through a Differentiation-Based Mechanism
Krah, N. M., Narayanan, S. M., Yugawa, D. E., Straley, J. A., Wright, C. V. E., MacDonald, R. J., & Murtaugh, L. C. (2019) · Developmental Cell · doi:10.1016/j.devcel.2019.07.012 · Cited by 37 · see citing works
Self-citationEisses, J. F., Criscimanna, A., Dionise, Z. R., Orabi, A. I., Javed, T. A., Sarwar, S., Jin, S., Zhou, L., Singh, S., Poddar, M., et al. (2015) · American Journal Of Pathology · doi:10.1016/j.ajpath.2015.08.006 · Cited by 36 · see citing works
Pathogenesis of Pancreatic Cancer
Murtaugh, L. C. (2013) · Toxicologic Pathology · doi:10.1177/0192623313508250 · Cited by 36 · see citing works
Self-citationWnt Pathway in Pancreatic Development and Pathophysiology
Napolitano, T., Silvano, S., Ayachi, C., Plaisant, M., de Veiga, A. S., Fofo, H., Charles, B., & Collombat, P. (2023) · Cells · doi:10.3390/cells12040565 · Cited by 32 · see citing works
Bhatia, R., Thompson, C. M., Clement, E. J., Ganguly, K., Cox, J. L., Rauth, S., Siddiqui, J. A., Mashiana, S. S., Jain, M., Wyatt, T. A., et al. (2022) · Gastroenterology · doi:10.1053/j.gastro.2022.06.071 · Cited by 28 · see citing works
Epithelial NEMO/IKKγ limits fibrosis and promotes regeneration during pancreatitis
Chan, L. K., Gerstenlauer, M., Konukiewitz, B., Steiger, K., Weichert, W., Wirth, T., & Maier, H. J. (2016) · Gut · doi:10.1136/gutjnl-2015-311028 · Cited by 28 · see citing works
Grabliauskaite, K., Hehl, A. B., Seleznik, G. M., Saponara, E., Schlesinger, K., Zuellig, R. A., Dittmann, A., Bain, M., Reding, T., Sonda, S., et al. (2015) · The Journal of Pathology · doi:10.1002/path.4440 · Cited by 27 · see citing works
Developmental Molecular Biology of the Pancreas
Murtaugh, L. C., Cleaver, O. B., & MacDonald, R. J. (2018) · Springer eBooks · doi:10.1007/978-1-4939-7193-0_4 · Cited by 23 · see citing works
Self-citationRegulation of the Pancreatic Exocrine Differentiation Program and Morphogenesis by Onecut 1/Hnf6
Kropp, P. A., Zhu, X., & GANNON, M. A. (2019) · Cellular and Molecular Gastroenterology and Hepatology · doi:10.1016/j.jcmgh.2019.02.004 · Cited by 22 · see citing works
Effect of Wnt Signaling on the Differentiation of Islet β-Cells from Adipose-Derived Stem Cells
Wang, H., Ren, Y. T., Hu, X., Ma, M., Wang, X., Liang, H., & Liu, D. (2017) · BioMed Research International · doi:10.1155/2017/2501578 · Cited by 21 · see citing works
Self-citationAdult Pancreatic Acinar Progenitor-like Populations in Regeneration and Cancer
Jiang, Z., White, R. A., & Wang, T. C. (2020) · Trends in Molecular Medicine · doi:10.1016/j.molmed.2020.04.003 · Cited by 20 · see citing works
Role of Wnt/β-catenin pathway agonist SKL2001 in Caerulein-induced acute pancreatitis
Huang, H., Tang, G.-D., Liang, Z., Qin, M., Wang, X.-M., Chang, R., & Qin, H. (2018) · Canadian Journal of Physiology and Pharmacology · doi:10.1139/cjpp-2018-0226 · Cited by 20 · see citing works
Pancreatic gene expression during recovery after pancreatitis reveals unique transcriptome profiles
Boggs, K., Wang, T., Orabi, A. I., Mukherjee, A., Eisses, J. F., Sun, T., Wen, L., Javed, T. A., Esni, F., Chen, W., et al. (2018) · Scientific Reports · doi:10.1038/s41598-018-19392-0 · Cited by 19 · see citing works
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Bangs, F. K., Miller, P. F., & O’Neill, E. E. (2020) · Disease Models & Mechanisms · doi:10.1242/dmm.044289 · Cited by 16 · see citing works
Schmitner, N., Kohno, K., & Meyer, D. (2017) · Disease Models & Mechanisms · doi:10.1242/dmm.026633 · Cited by 16 · see citing works
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Clinical Translational Potentials of Stem Cell-Derived Extracellular Vesicles in Type 1 Diabetes
Hu, W., Song, X. H., Yu, H., Sun, J., Wang, H., & Zhao, Y. L. (2022) · Frontiers in Endocrinology · doi:10.3389/fendo.2021.682145 · Cited by 10 · see citing works
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Prete, F. P., Rotelli, M. T., Stella, A., Calculli, G., Sgaramella, L. I., d’Amati, A., Resta, N., Testini, M., & Gurrado, A. (2022) · Clinical and Experimental Medicine · doi:10.1007/s10238-022-00849-6 · Cited by 9 · see citing works
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Hawkins, H. J., Yacob, B. W., Brown, M. E., Goldstein, B. R., Arcaroli, J. J., Bagby, S. M., Hartman, S. J., MacBeth, M. L., Goodspeed, A. E., Danhorn, T., et al. (2024) · PLoS ONE · doi:10.1371/journal.pone.0298808 · Cited by 7 · see citing works
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TBX3 is dynamically expressed in pancreatic organogenesis and fine-tunes regeneration
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“Based on the fact that Tbx3 is involved in the regulation of Wnt signaling in embryonic development [9] and Wnt signaling controls the proliferation of acinar cells during organ regeneration [24], Tbx3 may have a regulatory role on Wnt signaling during acinar cell regeneration.”
BackgroundHøj, K., Baldan, J., Seymour, P. A., Rift, C. V., Hasselby, J. P., Sandelin, A., & Arnes, L. (2024) · Gastro Hep Advances · doi:10.1016/j.gastha.2024.07.002 · Cited by 5 · see citing works
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Functioning of whole bone marrow cell population in a model of L-arginine-induced pancreatitis
Stojanović, N. M., Mitić, K. V., Stojnev, S., Sokolovic, D. T., Vukelić-Nikolić, M. Đ., Tričković-Vukić, D., Randjelović, P. J., Krstić, M., & Radulović, N. S. (2023) · European Journal of Inflammation · doi:10.1177/1721727x231177816 · Cited by 3 · see citing works
Amino Acid Transporters of Epithelia
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Developmental Molecular Biology of the Pancreas
Murtaugh, L. C., Cleaver, O. B., & MacDonald, R. J. (2016) · Springer eBooks · doi:10.1007/978-1-4939-6631-8_4-2 · Cited by 2 · see citing works
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Heterozygous missense variant in GLI2 impairs human endocrine pancreas developmentPreprint
Mueller, L. M., Isaacson, A., WILSON, H. M., Salowka, A., Gong, M., Raile, K., & Spagnoli, F. M. (2023) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2023.11.05.565673
Heterozygous missense variant in GLI2 impairs human endocrine pancreas development
Mueller, L. M., Isaacson, A., WILSON, H. M., Salowka, A., Tay, I., Gong, M., Elbarbary, N. S., Raile, K., & Spagnoli, F. M. (2024) · Nature Communications · doi:10.1038/s41467-024-46740-8
- Authors
- Keefe, M., Wang, H., De La O, J.-P., Khan, A., Firpo, M. A., & Murtaugh, L. C.
- Affiliations
- University of Utah (US)
- Department of Human Genetics, University of Utah School of Medicine, Salt Lake City, Utah, USA;
- Corresponding author
- Murtaugh, L. Charles
- Venue
- Disease Models & Mechanisms
- Publisher
- The Company of Biologists
- Published
- 2012-01-01
- Volume
- 5
- Issue
- 4
- Pages
- 503-14
- ISSN
- 1754-8403 (ISSN-L)
- 1754-8411
- PMC
- PMC3380713
- OpenAlex
- W2096547892
- Cited by
- 54
- References
- 67
- Citations by year
- 2026: 1 · 2024: 4 · 2023: 5 · 2022: 4 · 2021: 3 · 2020: 4 · 2019: 3 · 2018: 5 · 2017: 4 · 2016: 5 · 2015: 4 · 2014: 4 · 2013: 6 · 2012: 2
- FWCI
- 5.22
- Type
- journal article
- Language
- en
- Open access
- gold
- doi.org
- Licence
- Locations
- Disease Models & Mechanisms (publishedVersion, cc-by-nc-sa)
- PubMed Central (publishedVersion, cc-by-nc-sa)
- PubMed (publishedVersion)
- DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
- HighWire Press Open Archive (submittedVersion)
- Funders
- National Institute of General Medical Sciences (T32GM007464)
- National Institute of Diabetes and Digestive and Kidney Diseases (R01DK075072)
- Eunice Kennedy Shriver National Institute of Child Health and Human Development (T32HD07491, T32HD007491)
- Topics
- Health Sciences › Medicine › Surgery › Pancreatic function and diabetes
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Wnt/β-catenin signaling in development and cancer
- Health Sciences › Medicine › Oncology › Pancreatic and Hepatic Oncology Research
- Keywords
- β-catenin, Wnt signaling, pancreatic acinar cells, pancreatic development, pancreatic regeneration, pancreatic endocrine cells, self-renewal, acinar cell proliferation, pancreatitis, type 2 diabetes
- MeSH terms
- Aging, Animals, Animals, Newborn, Ceruletide, Cell Differentiation, Homeostasis, Humans, Pancreatitis, Regeneration, Gene Deletion, Mice, Knockout, Cell Lineage, Pancreas, Exocrine, Cell Proliferation, beta Catenin, Mice, Acinar Cells
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