Fol. Biol. 2019, 65, 246-255

https://doi.org/10.14712/fb2019065050246

γ-Aminobutyric Acid (GABA) Induced in Vitro Differentiation of Rat Pancreatic Ductal Stem Cells into Insulin-Secreting Islet-Like Cell Clusters

M. W. Ghani, Z. Yi, W. Jiang, L. Ye, L. Bin, L. G. Cun, M. W. Birmani, Xiao Mei

Department of Animal Breeding, Genetics and Reproduction, Guangdong Ocean University, Zhanjiang, Guangdong, China

Received July 2019
Accepted October 2019

References

1. Ackermann, A. M., Moss, N. G., Kaestner, K. H. (2018) GABA and artesunate do not induce pancreatic α-to-β cell transdifferentiation in vivo. Cell Metab. 28, 787-792.e3. <https://doi.org/10.1016/j.cmet.2018.07.002>
2. Adeghate, E., Ponery, A. S. (2002) GABA in the endocrine pancreas: cellular localization and function in normal and diabetic rats. Tissue Cell 34, 1-6. <https://doi.org/10.1054/tice.2002.0217>
3. Afelik, S., Rovira, M. (2017a). Pancreatic β-cell regeneration: advances in understanding the genes and signaling pathways involved. Genome Med. 9, 1-4.
4. Afelik, S., Rovira, M. (2017b) Pancreatic β-cell regeneration: facultative or dedicated progenitors? Mol. Cell. Endocrinol. 445, 85-4. <https://doi.org/10.1016/j.mce.2016.11.008>
5. Aguayo-Mazzucato, C., Bonner-Weir, S. (2018) Pancreatic β cell regeneration as a possible therapy for diabetes. Cell Metab. 27, 57-67. <https://doi.org/10.1016/j.cmet.2017.08.007>
6. Aikin, R., Rosenberg, L., Maysinger, D. (2000) Phosphatidylinositol 3-kinase signaling to Akt mediates survival in isolated canine islets of Langerhans. Biochem. Biophys. Res. Commun. 277, 455-461. <https://doi.org/10.1006/bbrc.2000.3664>
7. Asghar, F., Zhu, H. (2018) Overview of pancreas transplantation. J. Pancreas 19, 65-69.
8. Bansal, P., Wang, S., Liu, S., Xiang, Y.-Y., Lu, W.-Y., Wang, Q. (2011) GABA coordinates with insulin in regulating secretory function in pancreatic INS-1 β-cells. PLoS One 6, e26225. <https://doi.org/10.1371/journal.pone.0026225>
9. Ben-Othman, N., Vieira, A., Courtney, M., Record, F., Gjernes, E., Avolio, F., Hadzic, B., Druelle, N., Napolitano, T., Navarro- Sanz, S., Silvano, S., Al-Hasani, K., Pfeifer, A., Lacas- Gervais, S., Leuckx, G., Marroquí, L., Thévenet, J., Madsen, O. D., Eizirik, D. L., Heimberg, H., Kerr-Conte, J., Pattou, F., Mansouri, A., Collombat, P. (2017) Longterm GABA administration induces α cell-mediated β-like cell neogenesis. Cell 168, 73-85.e11. <https://doi.org/10.1016/j.cell.2016.11.002>
10. Benthuysen, J. R., Carrano, A. C., Sander, M. (2016) Advances in β cell replacement and regeneration strategies for treating diabetes. J. Clin. Invest. 126, 3651-3660. <https://doi.org/10.1172/JCI87439>
11. Braun, M., Ramracheya, R., Bengtsson, M., Clark, A., Walker, J. N., Johnson, P. R., Rorsman, P. (2010) γ-Aminobutyric acid (GABA) is an autocrine excitatory transmitter in human pancreatic β-cells. Diabetes 59, 1694-1701. <https://doi.org/10.2337/db09-0797>
12. Byrnes, L. E., Wong, D. M., Subramaniam, M., Meyer, N. P., Gilchrist, C. L., Knox, S. M., Tward, A. D., Ye, C. J., Sneddon, J. B. (2018) Lineage dynamics of murine pancreatic development at single-cell resolution. Nat. Commun. 9, 1-17. <https://doi.org/10.1038/s41467-018-06176-3>
13. Cañibano-Hernández, A., Saenz del Burgo, L., Espona- Noguera, A., Orive, G., Hernandez, R. M., Ciriza, J., Pedraz, J. L. (2019) Hyaluronic acid promotes differentiation of mesenchymal stem cells from different sources towards pancreatic progenitors within 3D alginate matrices. Mol. Pharm. 16, 834-845. <https://doi.org/10.1021/acs.molpharmaceut.8b01126>
14. Chen, X. C., Liu, H., Li, H., Cheng, Y., Yang, L., Liu, Y. F. (2016) In vitro expansion and differentiation of rat pancreatic duct-derived stem cells into insulin secreting cells using a dynamic three-dimensional cell culture system. Genet. Mol. Res. 15, 1-12.
15. Corritore, E., Lee, Y., Sokal, E. M., Lysy, P. A. (2016) β-Cell replacement sources for type 1 diabetes: a focus on pancreatic ductal cells. Ther. Adv. Endocrinol. Metab. Rev. 7, 182-199. <https://doi.org/10.1177/2042018816652059>
16. Criscimanna, A., Speicher, J. A., Houshmand, G., Shiota, C., Prasadan, K., Ji, B., Logsdon, C. D., Gittes, G. K., Esni, F. (2011) Duct cells contribute to regeneration of endocrine and acinar cells following pancreatic damage in adult mice. Gastroenterology 141, 1451-1462. <https://doi.org/10.1053/j.gastro.2011.07.003>
17. Eizirik, D. L., Gurzov, E. N. (2018) Can GABA turn pancreatic α-cells into β-cells? Nat. Rev. Endocrinol. 14, 629-630. <https://doi.org/10.1038/s41574-018-0101-6>
18. El-Gohary, Y., Wiersch, J., Tulachan, S., Xiao, X., Guo, P., Rymer, C., Fischbach, S., Prasadan, K., Shiota, C., Gaffar, I., Song, Z., Galambos, C., Esni, F., Gittes, G. K. (2016) Intraislet pancreatic ducts can give rise to insulin-positive cells. Endocrinology 157, 166-175. <https://doi.org/10.1210/en.2015-1175>
19. Franklin, I. K., Wollheim, C. B. (2004) GABA in the endocrine pancreas: its putative role as an islet cell paracrinesignalling molecule. J. Gen. Physiol. 123, 185-190. <https://doi.org/10.1085/jgp.200409016>
20. Ghani, M. W., Ye, L., Yi, Z., Ghani, H., Birmani, M. W., Nawab, A., Cun, L. G., Bin, L., Mei, X. (2019) Pancreatic β-cell replacement: advances in protocols used for differentiation of pancreatic progenitors to β-like cells. Folia Histochem. Cytobiol. 53, 1-36.
21. Huch, M., Bonfanti, P., Boj, S. F., Sato, T., Loomans, C. J. M., Van De Wetering, M., Sojoodi, M., Li, V. S. W., Schuijers, J., Gracanin, A., Ringnalda, F., Begthel, H., Hamer, K., Mulder, J., Van Es, J. H., De Koning, E., Vries, R. G. J., Heimberg, H., Clevers, H. (2013) Unlimited in vitro expansion of adult bi-potent pancreas progenitors through the Lgr5/R-spondin axis. EMBO J. 32, 2708-2721. <https://doi.org/10.1038/emboj.2013.204>
22. Inada, A., Nienaber, C., Katsuta, H., Fujitani, Y., Levine, J., Morita, R., Sharma, A., Bonner-Weir, S. (2008) Carbonic anhydrase II-positive pancreatic cells are progenitors for both endocrine and exocrine pancreas after birth. Proc. Natl. Acad. Sci. USA 105, 19915-19919. <https://doi.org/10.1073/pnas.0805803105>
23. Jacobson, E. F., Tzanakakis, E. S. (2017) Human pluripotent stem cell differentiation to functional pancreatic cells for diabetes therapies: innovations, challenges and future directions. J. Biol. Eng. 11, 1-13. <https://doi.org/10.1186/s13036-017-0066-3>
24. Kuise, T., Noguchi, H. (2011) Recent progress in pancreatic islet transplantation. World J. Transplant. 1, 13-18. <https://doi.org/10.5500/wjt.v1.i1.13>
25. Larqué, C., Velasco, M., Barajas-Olmos, F., García-Delgado, N., Chávez-Maldonado, J. P., García-Morales, J., Orozco, L., Hiriart, M. (2016) Transcriptome landmarks of the functional maturity of rat β-cells, from lactation to adulthood. J. Mol. Endocrinol. 57, 45-59. <https://doi.org/10.1530/JME-16-0052>
26. Li, L., Lili, R., Hui, Q., Min, W., Xue, W., Xin, S., Jing, L., Yan, L., Yeqiang, L., Fenrong, H., Furong, L., Guanxin, S. (2008) Combination of GLP-1 and sodium butyrate promote differentiation of pancreatic progenitor cells into insulin- producing cells. Tissue Cell 40, 437-445. <https://doi.org/10.1016/j.tice.2008.04.006>
27. Ligon, B., Yang, J., Morin, S. B., Ruberti, M. F., Steer, M. L. (2007) Regulation of pancreatic islet cell survival and replication by γ-aminobutyric acid. Diabetologia 50, 764-773. <https://doi.org/10.1007/s00125-007-0601-8>
28. Ma, D., Tang, S., Song, J., Wu, Q., Zhang, F., Xing, Y., Pan, Y., Zhang, Y., Jiang, J., Zhang, Y., Jiang, J., Zhang, Y., Jin, L. (2017) Culturing and transcriptome profiling of progenitor- like colonies derived from adult mouse pancreas. Stem Cell Res. Ther. 8, 1-16.
29. Meulen van der, T., Lee, S., Noordeloos, E., Donaldson, C. J., Adams, M. W., Noguchi, G. M., Mawla, A. M., Huising, M. O. (2018) Artemether does not turn α cells into β cells. Cell Metab. 27, 218-225.e4. <https://doi.org/10.1016/j.cmet.2017.10.002>
30. Noguchi, H., Naziruddin, B., Shimoda, M., Fujita, Y., Chujo, D., Takita, M., Peng, H., Sugimoto, K., Itoh, T., Tamura, Y., Olsen, G. S., Kobayashi, N., Onaca, N., Hayashi, S., Levy, M. F., Matsumoto, S. (2010) Induction of insulin-producing cells from human pancreatic progenitor cells. Transplant. Proc. 42, 2081-2083. <https://doi.org/10.1016/j.transproceed.2010.05.097>
31. Pagliuca, F. W., Millman, J. R., Gürtler, M., Segel, M., Van Dervort, A., Ryu, J. H., Peterson, Q. P., Greiner, D., Melton, D. A. (2014) Generation of functional human pancreatic β cells in vitro. Cell 159, 428-439. <https://doi.org/10.1016/j.cell.2014.09.040>
32. Peng, B.-Y., Dubey, N. K., Mishra, V. K., Tsai, F.-C., Dubey, R., Deng, W.-P., Wei, H.-J. (2018) Addressing stem cell therapeutic approaches in pathobiology of diabetes and its complications. J. Diabetes Res. 2018, 1-16. <https://doi.org/10.1155/2018/7806435>
33. Piero, M. N. (2015) Diabetes mellitus – a devastating metabolic disorder. Asian J. Biomed. Pharm. Sci. 4, 1-7. <https://doi.org/10.15272/ajbps.v4i40.645>
34. Qadir, M. M. F., Álvarez-Cubela, S., Klein, D., Lanzoni, G., García-Santana, C., Montalvo, A., Pláceres-Uray, F., Mazza, E. M. C., Ricordi, C., Inverardi, L. A., Pastori, R. L., Domínguez-Bendala, J. (2018) P2RY1/ALK3-expressing cells within the adult human exocrine pancreas are BMP-7 expandable and exhibit progenitor-like characteristics. Cell Rep. 22, 245-2468. <https://doi.org/10.1016/j.celrep.2018.02.006>
35. Ravindranath Aathira, V. J. (2014) Advances in management of type 1 diabetes mellitus. World J. Diabetes 5, 689-696.
36. Reetz, A., Solimena, M., Matteoli, M., Folli, F., Takei, K., De Camilli, P. (1991) GABA and pancreatic β-cells: colocalization of glutamic acid decarboxylase (GAD) and GABA with synaptic-like microvesicles suggests their role in GABA storage and secretion. EMBO J. 10, 1275-1284. <https://doi.org/10.1002/j.1460-2075.1991.tb08069.x>
37. Rezania, A., Bruin, J. E., Arora, P., Rubin, A., Batushansky, I., Asadi, A., O’Dwyer, S., Quiskamp, N., Mojibian, M., Albrecht, T., Yang, Y. H. C., Johnson, J. D., Kieffer, T. J. (2014) Reversal of diabetes with insulin-producing cells derived in vitro from human pluripotent stem cells. Nat. Biotechnol. 32, 1121-1133. <https://doi.org/10.1038/nbt.3033>
38. Rogers, K. K. (2019) Diabetes and disclosure. N. Engl. J. Med. 380, 1495-1497. <https://doi.org/10.1056/NEJMp1814423>
39. Rutter, G. A. (2017) GABA signaling: a route to new pancreatic β cells. Cell Res. 27, 309-310. <https://doi.org/10.1038/cr.2017.20>
40. Scavuzzo, M. A., Hill, M. C., Chmielowiec, J., Yang, D., Teaw, J., Sheng, K., Kong, Y., Bettini, M., Zong, C., Martin, J. F., Borowiak, M. (2018) Endocrine lineage biases arise in temporally distinct endocrine progenitors during pancreatic morphogenesis. Nat. Commun. 9, 1-21. <https://doi.org/10.1038/s41467-018-05740-1>
41. Shih, H. P., Wang, A., Sander, M. (2013) Pancreas organogenesis: from lineage determination to morphogenesis. Annu. Rev. Cell Dev. Biol. 29, 81-105. <https://doi.org/10.1146/annurev-cellbio-101512-122405>
42. Shin, J., Kim, J., Min, B. (2019) Absence of spontaneous regeneration of endogenous pancreatic β-cells after chemical- induced diabetes and no effect of GABA on α-to-β cell transdifferentiation in rhesus monkeys. Biochem. Biophys. Res. Commun. 508, <https://doi.org/10.1016/j.bbrc.2018.12.062>
43. Shiroi, A., Ueda, S., Ouji, Y., Saito, K., Moriya, K., Sugie, Y., Fukui, H., Ishizaka, S., Yoshikawa, M. (2005) Differentiation of embryonic stem cells into insulin-producing cells promoted by Nkx2.2 gene transfer. World J. Gastroenterol. 11, 4161-4166. <https://doi.org/10.3748/wjg.v11.i27.4161>
44. Soltania, N., Qiua, H., Aleksicb, M., Glinkac, Y., Zhaoa, F., Liua, R., Lid, Y., Zhanga, N., Chakrabartid, R., Nga, T., Jinb, T., Zhang, H., Lu, W. Y., Feng, Z. P., Prud’homme, G. J., Wang, Q. (2011) GABA exerts protective and regenerative effects on islet β cells and reverses diabetes. Proc. Natl. Acad. Sci. USA 108, 11692-11697. <https://doi.org/10.1073/pnas.1102715108>
45. Tan, J., Liu, L., Li, B., Xie, Q., Sun, J., Pu, H., Zhang, L. (2019) Pancreatic stem cells differentiate into insulin-secreting cells on fibroblast-modified PLGA membranes. Mater. Sci. Eng. C 97, 593-601. <https://doi.org/10.1016/j.msec.2018.12.062>
46. Tillakaratne, N. J. K., Medina-Kauwe, L., Gibson, K. M. (1995) γ-Aminobutyric acid (GABA) metabolism in mammalian neural and nonneural tissues. Comp. Biochem. Physiol. 2, 247-263. <https://doi.org/10.1016/0300-9629(95)00099-2>
47. Trümper, K., Trümper, A., Trusheim, H., Arnold, R., Göke, B., Hörsch, D. (2000) Integrative mitogenic role of protein kinase B/Akt in β-cells. Ann. N. Y. Acad. Sci. 921, 242-250. <https://doi.org/10.1111/j.1749-6632.2000.tb06972.x>
48. Vieira, A., Ben-Othman, N., Collombat, P. (2017) GABA triggers pancreatic β-like cell neogenesis. Cell Cycle 16, 727-728. <https://doi.org/10.1080/15384101.2017.1302212>
49. Wang, C.-Y., Gou, S.-M., Liu, T., Wu, H.-S., Xiong, J.-X., Zhou, F., Tao, J. (2008) Differentiation of CD24- pancreatic ductal cell-derived cells into insulin-secreting cells. Dev. Growth Differ. 50, 633-643. <https://doi.org/10.1111/j.1440-169X.2008.01061.x>
50. Wang, S., Luo, Y., Feng, A., Li, T., Yang, X., Nofech-Mozes, R., Yu, M., Wang, C., Li, Z., Yi, F., Liu, C., Lu, W. Y., Luo, Y., Feng, A., Li, T., Yang, X., Nofech-Mozes, R., Yu, M., Wang, C., Li, Z., Yi, F., Liu, C., Lu, W. Y. (2014) Ethanol induced impairment of glucose metabolism involves alterations of GABAergic signaling in pancreatic β-cells. Toxicology 326, 44-52. <https://doi.org/10.1016/j.tox.2014.10.005>
51. Weir, G. C., Bonner-Weir, S. (2017) GABA signaling stimulates β cell regeneration in diabetic mice. Cell 168, 7-9. <https://doi.org/10.1016/j.cell.2016.12.006>
52. Yu, X.-X., Qiu, W.-L., Yang, L., Zhang, Y., He, M.-Y., Li, L.- C., Xu, C.-R. (2019) Defining multistep cell fate decision pathways during pancreatic development at single‐cell resolution. EMBO J. 38, 1-20.
53. Zhou, Q., Melton, D. A. (2018) Pancreas regeneration. Nature 557, 351-358. <https://doi.org/10.1038/s41586-018-0088-0>
54. Zimmet, P., Alberti, K. G., Magliano, D. J., Bennett, P. H. (2016) Diabetes mellitus statistics on prevalence and mortality: facts and fallacies. Nat. Rev. Endocrinol. 12, 616-622. <https://doi.org/10.1038/nrendo.2016.105>
front cover

ISSN 0015-5500 (Print) ISSN 2533-7602 (Online)

Open access journal

Archive