A δ-cell subpopulation with pro-β cell identity contributes to efficient age-independent recovery in a zebrafish diabetes model.

Carril Pardo, Claudio Andrès; Massoz, Laura; Dupont, Marie; Bergemann, David; Bourdouxhe, Jordane; Lavergne, Arnaud; Tarifeño Saldivia, Estefania; Helker, Christian Sm; Stainier, Didier Yr True; Peers, Bernard; Voz, Marianne; Manfroid, Isabelle

doi:10.7554/eLife.67576

Article (Scientific journals)

A δ-cell subpopulation with pro-β cell identity contributes to efficient age-independent recovery in a zebrafish diabetes model.

Carril Pardo, Claudio Andrès; Massoz, Laura; Dupont, Marie et al.

2022 • In eLife, 11

Peer Reviewed verified by ORBi

Permalink
https://hdl.handle.net/2268/268196

DOI
10.7554/eLife.67576

PubMed
35060900

Files (1)Send to Details Statistics Bibliography Similar publications

Files

Full Text

Carril_et_al_2022_author.pdf

Author preprint (2.55 MB)

Download

All documents in ORBi are protected by a user license.

Send to

RIS BibTex APA Chicago Permalink X Linkedin

Details

Keywords :

cell biology; zebrafish

Abstract :

[en] Restoring damaged b-cells in diabetic patients by harnessing the plasticity of other pancreatic cells raises the questions of the efficiency of the process and of the functionality of the new Insulin-expressing cells. To overcome the weak regenerative capacity of mammals, we used regeneration-prone zebrafish to study b-cells arising following destruction. We show that most new insulin cells differ from the original b-cells as they coexpress Somatostatin and Insulin. These bihormonal cells are abundant, functional and able to normalize glycemia. Their formation in response to b-cell destruction is fast, efficient and age-independent. Bihormonal cells are transcriptionally close to a subset of d-cells that we identified in control islets and which are characterized by the expression of somatostatin 1.1 (sst1.1) and by genes essential for glucose-induced Insulin secretion in β-cells such as pdx1, slc2a2 and gck. We observed in vivo the conversion of monohormonal sst1.1-expressing cells to sst1.1+ ins+ bihormonal cells following b-cell destruction. Our findings support the conclusion that sst1.1 d-cells possess a pro-b identity enabling them to contribute to the neogenesis of Insulin-producing cells during regeneration. This work unveils that abundant and functional bihormonal cells benefit to diabetes recovery in zebrafish.

Disciplines :

Anatomy (cytology, histology, embryology...) & physiology

Author, co-author :

Carril Pardo, Claudio Andrès ; Université de Liège - ULiège > GIGA

Massoz, Laura ; Université de Liège - ULiège > GIGA Stem Cells - Zebrafish Dev. & Disease Model

Dupont, Marie ; Université de Liège - ULiège > GIGA Stem Cells - Zebrafish Dev. & Disease Model

Bergemann, David

Bourdouxhe, Jordane

Lavergne, Arnaud ; Université de Liège - ULiège > GIGA Platform Genomics

Tarifeño Saldivia, Estefania

Helker, Christian Sm

Stainier, Didier Yr True

Peers, Bernard ; Université de Liège - ULiège > Département des sciences de la vie > GIGA Stem Cells - Zebrafish Dev. & Disease Model

Voz, Marianne ; Université de Liège - ULiège > GIGA Stem Cells - Zebrafish Dev. & Disease Model

Manfroid, Isabelle ; Université de Liège - ULiège > GIGA Stem Cells - Zebrafish Dev. & Disease Model

Language :

English

Title :

A δ-cell subpopulation with pro-β cell identity contributes to efficient age-independent recovery in a zebrafish diabetes model.

Publication date :

2022

Journal title :

eLife

eISSN :

2050-084X

Publisher :

eLife Sciences Publications, United Kingdom

Volume :

Peer reviewed :

Peer Reviewed verified by ORBi

Commentary :

Available on ORBi :

since 11 February 2022

Statistics

Number of views

163 (16 by ULiège)

Number of downloads

102 (5 by ULiège)

More statistics

Scopus citations^®

Scopus citations^®
without self-citations

OpenCitations

OpenAlex citations

Bibliography

Ahlgren, U., Jonsson, J., Jonsson, L., Simu, K., & Edlund, H. (1998). beta-cell-specific inactivation of the mouse Ipf1/Pdx1 gene results in loss of the beta-cell phenotype and maturity onset diabetes. Genes & Development, 12(12), 1763-1768. https://doi.org/10.1101/gad.12.12.1763
Bergemann, D., Massoz, L., Bourdouxhe, J., Carril Pardo, C. A., Voz, M. L., Peers, B., & Manfroid, I. (2018). Nifurpirinol: A more potent and reliable substrate compared to metronidazole for nitroreductase-mediated cell ablations. Wound Repair and Regeneration : Official Publication of the Wound Healing Society [and] the European Tissue Repair Society. https://doi.org/10.1111/wrr.12633
Binot, A-C, Manfroid, I., Flasse, L., Winandy, M., Motte, P., Martial, J. A., Voz, M. L. (2010). Nkx6.1 and nkx6.2 regulate alpha-and beta-cell formation in zebrafish by acting on pancreatic endocrine progenitor cells. Developmental Biology, 340(2), 397-407. https://doi.org/10.1016/j.ydbio.2010.01.025
Binot, A.-C., Manfroid, I., Flasse, L., Winandy, M., Motte, P., Martial, J. A., Voz, M. L. (2010). Nkx6.1 and nkx6.2 regulate α-and β-cell formation in zebrafish by acting on pancreatic endocrine progenitor cells. Developmental Biology, 340(2). https://doi.org/10.1016/j.ydbio.2010.01.025
Blum, B., Hrvatin, S., Schuetz, C., Bonal, C., Rezania, A., & Melton, D. A. (2012). Functional beta-cell maturation is marked by an increased glucose threshold and by expression of urocortin 3. Nature Biotechnology, 30(3), 261-264. https://doi.org/10.1038/nbt.2141
Chera, S., Baronnier, D., Ghila, L., Cigliola, V., Jensen, J. N., Gu, G., Herrera, P. L. (2014). Diabetes recovery by age-dependent conversion of pancreatic delta-cells into insulin producers. Nature, 514(7523), 503-507. https://doi.org/10.1038/nature13633
Cigliola, V., Ghila, L., Thorel, F., van Gurp, L., Baronnier, D., Oropeza, D., Herrera, P. L. (2018). Pancreatic islet-autonomous insulin and smoothened-mediated signaling modulate identity changes of glucagon(+) α-cells. Nature Cell Biology, 20(11), 1267-1277. https://doi.org/10.1038/s41556-018-0216-y
Curado, S., Anderson, R. M., Jungblut, B., Mumm, J., Schroeter, E., & Stainier, D. Y. R. (2007). Conditional targeted cell ablation in zebrafish: A new tool for regeneration studies. Developmental Dynamics : An Official Publication of the American Association of Anatomists, 236(4), 1025-1035. https://doi.org/10.1002/dvdy.21100
Dalgin, G., Ward, A. B., Hao, L. T., Beattie, C. E., Nechiporuk, A., & Prince, V. E. (2011). Zebrafish mnx1 controls cell fate choice in the developing endocrine pancreas. Development (Cambridge, England), 138(21), 4597-4608. https://doi.org/10.1242/dev.067736
Delaspre, F., Beer, R. L., Rovira, M., Huang, W., Wang, G., Gee, S., Parsons, M. J. (2015). Centroacinar Cells Are Progenitors That Contribute to Endocrine Pancreas Regeneration. Diabetes, 64(10), 3499-3509. https://doi.org/10.2337/db15-0153
Devos, N., Deflorian, G., Biemar, F., Bortolussi, M., Martial, J. A., Peers, B., & Argenton, F. (2002). Differential expression of two somatostatin genes during zebrafish embryonic development. Mechanisms of Development, 115(1-2), 133-137. https://doi.org/10.1016/s0925-4773(02)00082-5
Dobin, A., Davis, C. A., Schlesinger, F., Drenkow, J., Zaleski, C., Jha, S., Gingeras, T. R. (2013). STAR: Ultrafast universal RNA-seq aligner. Bioinformatics (Oxford, England), 29(1), 15-21. https://doi.org/10.1093/bioinformatics/bts635
Eames, S. C., Philipson, L. H., Prince, V. E., & Kinkel, M. D. (2010). Blood sugar measurement in zebrafish reveals dynamics of glucose homeostasis. Zebrafish, 7(2), 205-213. https://doi.org/10.1089/zeb.2009.0640
Feil, R., Wagner, J., Metzger, D., & Chambon, P. (1997). Regulation of Cre recombinase activity by mutated estrogen receptor ligand-binding domains. Biochemical and Biophysical Research Communications, 237(3), 752-757. https://doi.org/10.1006/bbrc.1997.7124
Gao, T., McKenna, B., Li, C., Reichert, M., Nguyen, J., Singh, T., Stanger, B. Z. (2014). Pdx1 maintains β cell identity and function by repressing an α cell program. Cell Metabolism, 19(2), 259-271. https://doi.org/10.1016/j.cmet.2013.12.002
Ghaye, A. P., Bergemann, D., Tarifeño-Saldivia, E., Flasse, L. C., Von Berg, V., Peers, B., Manfroid, I. (2015). Progenitor potential of nkx6.1-expressing cells throughout zebrafish life and during beta cell regeneration. BMC Biology, 13(1). https://doi.org/10.1186/s12915-015-0179-4
Hans, S., Kaslin, J., Freudenreich, D., & Brand, M. (2009). Temporally-controlled site-specific recombination in zebrafish. PloS One, 4(2), e4640. https://doi.org/10.1371/journal.pone.0004640
Kawakami, K. (2007). Tol2: A versatile gene transfer vector in vertebrates. Genome Biology, 8 Suppl 1, S7. https://doi.org/10.1186/gb-2007-8-s1-s7
Kwan, K. M., Fujimoto, E., Grabher, C., Mangum, B. D., Hardy, M. E., Campbell, D. S., Chien, C.-B. (2007). The Tol2kit: A multisite gateway-based construction kit for Tol2 transposon transgenesis constructs. Developmental Dynamics : An Official Publication of the American Association of Anatomists, 236(11), 3088-3099. https://doi.org/10.1002/dvdy.21343
Leonard, J., Peers, B., Johnson, T., Ferreri, K., Lee, S., & Montminy, M. R. (1993). Characterization of somatostatin transactivating factor-1, a novel homeobox factor that stimulates somatostatin expression in pancreatic islet cells. Molecular Endocrinology (Baltimore, Md.), 7(10), 1275-1283. https://doi.org/10.1210/mend.7.10.7505393
Liao, Y., Wang, J., Jaehnig, E. J., Shi, Z., & Zhang, B. (2019). WebGestalt 2019: Gene set analysis toolkit with revamped UIs and APIs. Nucleic Acids Research, 47(W1), W199-W205. https://doi.org/10.1093/nar/gkz401
Love, M. I., Huber, W., & Anders, S. (2014). Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2. Genome Biology, 15(12), 550. https://doi.org/10.1186/s13059-014-0550-8
Milewski, W. M., Duguay, S. J., Chan, S. J., & Steiner, D. F. (1998). Conservation of PDX-1 structure, function, and expression in zebrafish. Endocrinology, 139(3), 1440-1449. https://doi.org/10.1210/endo.139.3.5768
Moin, A. S. M., & Butler, A. E. (2019). Alterations in Beta Cell Identity in Type 1 and Type 2 Diabetes. Current Diabetes Reports, 19(9), 83. https://doi.org/10.1007/s11892-019-1194-6
Mosimann, C., Kaufman, C. K., Li, P., Pugach, E. K., Tamplin, O. J., & Zon, L. I. (2011). Ubiquitous transgene expression and Cre-based recombination driven by the ubiquitin promoter in zebrafish. Development (Cambridge, England), 138(1), 169-177. https://doi.org/10.1242/dev.059345
Moss, J. B., Koustubhan, P., Greenman, M., Parsons, M. J., Walter, I., & Moss, L. G. (2009). Regeneration of the pancreas in adult zebrafish. Diabetes, 58(8), 1844-1851. https://doi.org/10.2337/db08-0628
Ninov, N., Hesselson, D., Gut, P., Zhou, A., Fidelin, K., & Stainier, D. Y. R. (2013). Metabolic regulation of cellular plasticity in the pancreas. Current Biology : CB, 23(13), 1242-1250. https://doi.org/10.1016/j.cub.2013.05.037
Pan, F. C., Brissova, M., Powers, A. C., Pfaff, S., & Wright, C. V. E. (2015). Inactivating the permanent neonatal diabetes gene Mnx1 switches insulin-producing β-cells to a δ-like fate and reveals a facultative proliferative capacity in aged β-cells. Development (Cambridge, England), 142(21), 3637-3648. https://doi.org/10.1242/dev.126011
Parsons, M. J., Pisharath, H., Yusuff, S., Moore, J. C., Siekmann, A. F., Lawson, N., & Leach, S. D. (2009). Notch-responsive cells initiate the secondary transition in larval zebrafish pancreas. Mechanisms of Development, 126(10), 898-912. https://doi.org/10.1016/j.mod.2009.07.002
Perez-Frances, M., van Gurp, L., Abate, M. V., Cigliola, V., Furuyama, K., Bru-Tari, E., Herrera, P. L. (2021). Pancreatic Ppy-expressing γ-cells display mixed phenotypic traits and the adaptive plasticity to engage insulin production. Nature Communications, 12(1), 4458. https://doi.org/10.1038/s41467-021-24788-0
Picelli, S., Faridani, O. R., Björklund, A. K., Winberg, G., Sagasser, S., & Sandberg, R. (2014). Full-length RNA-seq from single cells using Smart-seq2. Nature Protocols, 9(1), 171-181. https://doi.org/10.1038/nprot.2014.006
Piran, R., Lee, S.-H., Li, C.-R., Charbono, A., Bradley, L. M., & Levine, F. (2014). Pharmacological induction of pancreatic islet cell transdifferentiation: Relevance to type I diabetes. Cell Death & Disease, 5(7), e1357. https://doi.org/10.1038/cddis.2014.311
Pisharath, H., & Parsons, M. J. (2009). Nitroreductase-mediated cell ablation in transgenic zebrafish embryos. Methods in Molecular Biology (Clifton, N.J.), 546, 133-143. https://doi.org/10.1007/978-1-60327-977-2_9
Schaffer, A. E., Taylor, B. L., Benthuysen, J. R., Liu, J., Thorel, F., Yuan, W., Sander, M. (2013). Nkx6.1 controls a gene regulatory network required for establishing and maintaining pancreatic Beta cell identity. PLoS Genetics, 9(1), e1003274. https://doi.org/10.1371/journal.pgen.1003274
Segerstolpe, A., Palasantza, A., Eliasson, P., Andersson, E.-M., Andreasson, A.-C., Sun, X., Sandberg, R. (2016). Single-Cell Transcriptome Profiling of Human Pancreatic Islets in Health and Type 2 Diabetes. Cell Metabolism, 24(4), 593-607. https://doi.org/10.1016/j.cmet.2016.08.020
Singh, S. P., Chawla, P., Hnatiuk, A., Kamel, M., Silva, L. D., Spanjard, B., Ninov, N. (2021). A single-cell atlas of de novo β-cell regeneration reveals the contribution of hybrid β/δ cells to diabetes recovery in zebrafish. BioRxiv, 2021.06.24.449704. https://doi.org/10.1101/2021.06.24.449704
Singh, S. P., Janjuha, S., Hartmann, T., Kayisoglu, O., Konantz, J., Birke, S., Ninov, N. (2017). Different developmental histories of beta-cells generate functional and proliferative heterogeneity during islet growth. Nature Communications, 8(1), 664. https://doi.org/10.1038/s41467-017-00461-3
Spanjaard, B., Hu, B., Mitic, N., Olivares-Chauvet, P., Janjuha, S., Ninov, N., & Junker, J. P. (2018). Simultaneous lineage tracing and cell-type identification using CRISPR-Cas9-induced genetic scars. Nature Biotechnology, 36(5), 469-473. https://doi.org/10.1038/nbt.4124
Tarifeño-Saldivia, E., Lavergne, A., Bernard, A., Padamata, K., Bergemann, D., Voz, M. L., Peers, B. (2017). Transcriptome analysis of pancreatic cells across distant species highlights novel important regulator genes. BMC Biology, 15(1). https://doi.org/10.1186/s12915-017-0362-x
Thorel, F., Nepote, V., Avril, I., Kohno, K., Desgraz, R., Chera, S., & Herrera, P. L. (2010). Conversion of adult pancreatic alpha-cells to beta-cells after extreme beta-cell loss. Nature, 464(7292), 1149-1154. https://doi.org/10.1038/nature08894
Waeber, G., Thompson, N., Nicod, P., & Bonny, C. (1996). Transcriptional activation of the GLUT2 gene by the IPF-1/STF-1/IDX-1 homeobox factor. Molecular Endocrinology (Baltimore, Md.), 10(11), 1327-1334. https://doi.org/10.1210/mend.10.11.8923459
Wang, Y., Rovira, M., Yusuff, S., & Parsons, M. J. (2011). Genetic inducible fate mapping in larval zebrafish reveals origins of adult insulin-producing beta-cells. Development (Cambridge, England), 138(4), 609-617. https://doi.org/10.1242/dev.059097
Watada, H., Kajimoto, Y., Miyagawa, J., Hanafusa, T., Hamaguchi, K., Matsuoka, T., Yamasaki, Y. (1996). PDX-1 induces insulin and glucokinase gene expressions in alphaTC1 clone 6 cells in the presence of betacellulin. Diabetes, 45(12), 1826-1831. https://doi.org/10.2337/diab.45.12.1826
Ye, L., Robertson, M. A., Hesselson, D., Stainier, D. Y. R., & Anderson, R. M. (2015). Glucagon is essential for alpha cell transdifferentiation and beta cell neogenesis. Development (Cambridge, England), 142(8), 1407-1417. https://doi.org/10.1242/dev.117911