Degradation meets development: Implications in β-cell development and diabetes.
diabetes
pancreatic β-cells
stem cells
ubiquitin proteasome system
β-cell development
Journal
Cell biology international
ISSN: 1095-8355
Titre abrégé: Cell Biol Int
Pays: England
ID NLM: 9307129
Informations de publication
Date de publication:
18 Mar 2024
18 Mar 2024
Historique:
revised:
22
02
2024
received:
03
11
2023
accepted:
04
03
2024
medline:
19
3
2024
pubmed:
19
3
2024
entrez:
19
3
2024
Statut:
aheadofprint
Résumé
Pancreatic development is orchestrated by timely synthesis and degradation of stage-specific transcription factors (TFs). The transition from one stage to another stage is dependent on the precise expression of the developmentally relevant TFs. Persistent expression of particular TF would impede the exit from the progenitor stage to the matured cell type. Intracellular protein degradation-mediated protein turnover contributes to a major extent to the turnover of these TFs and thereby dictates the development of different tissues. Since even subtle changes in the crucial cellular pathways would dramatically impact pancreatic β-cell performance, it is generally acknowledged that the biological activity of these pathways is tightly regulated by protein synthesis and degradation process. Intracellular protein degradation is executed majorly by the ubiquitin proteasome system (UPS) and Lysosomal degradation pathway. As more than 90% of the TFs are targeted to proteasomal degradation, this review aims to examine the crucial role of UPS in normal pancreatic β-cell development and how dysfunction of these pathways manifests in metabolic syndromes such as diabetes. Such understanding would facilitate designing a faithful approach to obtain a therapeutic quality of β-cells from stem cells.
Types de publication
Journal Article
Review
Langues
eng
Sous-ensembles de citation
IM
Subventions
Organisme : Department of Science and Technology, Ministry of Science and Technology, India
ID : CRG/2021/000960
Informations de copyright
© 2024 The Authors. Cell Biology International published by John Wiley & Sons Ltd on behalf of International Federation of Cell Biology.
Références
Accili, D., & Arden, K. C. (2004). FoxOs at the crossroads of cellular metabolism, differentiation, and transformation. Cell, 117(4), 421-426.
Afelik, S., & Jensen, J. (2013). Notch signaling in the pancreas: patterning and cell fate specification. WIREs Developmental Biology, 2(4), 531-544.
Aghdam, S. Y., Gurel, Z., Ghaffarieh, A., Sorenson, C. M., & Sheibani, N. (2013). High glucose and diabetes modulate cellular proteasome function: implications in the pathogenesis of diabetes complications. Biochemical and Biophysical Research Communications, 432(2), 339-344.
Aguayo-Mazzucato, C., Koh, A., El Khattabi, I., Li, W.-C., Toschi, E., Jermendy, A., Juhl, K., Mao, K., Weir, G. C., Sharma, A., & Bonner-Weir, S. (2011). Mafa expression enhances glucose-responsive insulin secretion in neonatal rat beta cells. Diabetologia, 54, 583-593.
Akhouri, V., Majumder, S., & Gaikwad, A. B. (2023). The emerging insight into E3 ligases as the potential therapeutic target for diabetic kidney disease. Life Sciences, 321, 121643.
Akinci, E., Banga, A., Tungatt, K., Segal, J., Eberhard, D., Dutton, J. R., & Slack, J. M. W. (2013). Reprogramming of various cell types to a beta-like state by Pdx1, Ngn3 and MafA. PLoS ONE, 8(11), e82424.
Altomonte, J., Richter, A., Harbaran, S., Suriawinata, J., Nakae, J., Thung, S. N., Meseck, M., Accili, D., & Dong, H. (2003). Inhibition of Foxo1 function is associated with improved fasting glycemia in diabetic mice. American Journal of Physiology-Endocrinology and Metabolism, 285(4), E718-E728.
Al-Khawaga, S., Memon, B., Butler, A. E., Taheri, S., Abou-Samra, A. B., & Abdelalim, E. M. (2018). Pathways governing development of stem cell-derived pancreatic β cells: lessons from embryogenesis. Biological Reviews, 93(1), 364-389.
Apelqvist, Å., Ahlgren, U., & Edlund, H. (1997). Sonic hedgehog directs specialised mesoderm differentiation in the intestine and pancreas. Current Biology, 7(10), 801-804.
Apelqvist, Å., Li, H., Sommer, L., Beatus, P., Anderson, D. J., Honjo, T., de Angelis, M. H., Lendahl, U., & Edlund, H. (1999). Notch signalling controls pancreatic cell differentiation. Nature, 400(6747), 877-881.
Balasubramanyam, M., Sampathkumar, R., & Mohan, V. (2005). Is insulin signaling molecules misguided in diabetes for ubiquitin-proteasome mediated degradation? Molecular and Cellular Biochemistry, 275, 117-125.
Barbacci, E., Reber, M., Ott, M.-O., Breillat, C., Huetz, F., & Cereghini, S. (1999). Variant hepatocyte nuclear factor 1 is required for visceral endoderm specification. Development, 126(21), 4795-4805.
Barrow, J. R., Howell, W. D., Rule, M., Hayashi, S., Thomas, K. R., Capecchi, M. R., & McMahon, A. P. (2007). Wnt3 signaling in the epiblast is required for proper orientation of the anteroposterior axis. Developmental Biology, 312(1), 312-320.
Bastidas-Ponce, A., Roscioni, S. S., Burtscher, I., Bader, E., Sterr, M., Bakhti, M., & Lickert, H. (2017). Foxa2 and Pdx1 cooperatively regulate postnatal maturation of pancreatic β-cells. Molecular Metabolism, 6(6), 524-534.
Belaguli, N. S., Zhang, M., Brunicardi, F. C., & Berger, D. H. (2012). Forkhead box protein A2 (FOXA2) protein stability and activity are regulated by sumoylation. PLoS ONE, 7(10), e48019.
Bernal-Mizrachi, E., Kulkarni, R. N., Scott, D. K., Mauvais-Jarvis, F., Stewart, A. F., & Garcia-Ocaña, A. (2014). Human β-cell proliferation and intracellular signaling part 2: still driving in the dark without a road map. Diabetes, 63(3), 819-831.
Berndsen, C. E., & Wolberger, C. (2014). New insights into ubiquitin E3 ligase mechanism. Nature Structural & Molecular Biology, 21(4), 301-307.
Bhandari, D., Robia, S. L., & Marchese, A. (2009). The E3 ubiquitin ligase atrophin interacting protein 4 binds directly to the chemokine receptor CXCR4 via a novel WW domain-mediated interaction. Molecular Biology of the Cell, 20(5), 1324-1339.
Bishop, P., Rocca, D., & Henley, J. M. (2016). Ubiquitin C-terminal hydrolase L1 (UCH-L1): structure, distribution and roles in brain function and dysfunction. Biochemical Journal, 473(16), 2453-2462.
del Bosque-Plata, L., Amin, M., & Gragnoli, C. (2022). PSMD9 is linked to T2D age of onset, years of isolated and combined insulin therapy, irregular menses, and hot flashes. European Review for Medical & Pharmacological Sciences, 26(23), 8873-8878.
Brereton, M. F., Rohm, M., & Ashcroft, F. M. (2016). β-Cell dysfunction in diabetes: a crisis of identity? Diabetes, Obesity and Metabolism, 18(S1), 102-109. https://doi.org/10.1111/dom.12732
Cano, D. A., Soria, B., Martín, F., & Rojas, A. (2014). Transcriptional control of mammalian pancreas organogenesis. Cellular and Molecular Life Sciences, 71, 2383-2402.
Çetin, G., Klafack, S., Studencka-Turski, M., Krüger, E., & Ebstein, F. (2021). The ubiquitin-proteasome system in immune cells. Biomolecules, 11(1), 60.
Champeris Tsaniras, S., & Jones, P. M. (2010). Generating pancreatic β-cells from embryonic stem cells by manipulating signaling pathways. Journal of Endocrinology, 206(1), 13-26.
Chen, C., Gu, L., Matye, D. J., Clayton, Y.-D., Hasan, M. N., Wang, Y., Friedman, J. E., & Li, T. (2022). Cullin neddylation inhibitor attenuates hyperglycemia by enhancing hepatic insulin signaling through insulin receptor substrate stabilization. Proceedings of the National Academy of Sciences, 119(6), e2111737119.
Chen, Z., Chen, X., Bai, Y., Diao, Z., & Liu, W. (2020). Angiotensin-converting enzyme-2 improves diabetic nephropathy by targeting Smad7 for ubiquitin degradation. Molecular Medicine Reports, 22(4), 3008-3016.
Cheng, W., Cai, C., Xu, Y., Xiao, X., Shi, T., Liao, Y., Wang, X., Chen, S., Zhou, M., & Liao, Z. (2023). The TRIM21-FOXD1-BCL-2 axis underlies hyperglycaemic cell death and diabetic tissue damage. Cell Death & Disease, 14(12), 825.
Cheon, S. Y., & Song, J. (2021). The association between hepatic encephalopathy and diabetic encephalopathy: the brain-liver axis. International Journal of Molecular Sciences, 22(1), 463.
Choi, J., & Baek, K.-H. (2018). Cellular functions of stem cell factors mediated by the ubiquitin-proteasome system. Cellular and Molecular Life Sciences, 75, 1947-1957.
Chu, G. C., Dunn, N. R., Anderson, D. C., Oxburgh, L., & Robertson, E. J. (2004). Differential requirements for Smad4 in TGFβ-dependent patterning of the early mouse embryo.
Churchill, A. J., Gutiérrez, G. D., Singer, R. A., Lorberbaum, D. S., Fischer, K. A., & Sussel, L. (2017). Genetic evidence that Nkx2. 2 acts primarily downstream of Neurog3 in pancreatic endocrine lineage development. eLife, 6, e20010.
Ciechanover, A. (2012). Intracellular protein degradation: From a vague idea thru the lysosome and the ubiquitin-proteasome system and onto human diseases and drug targeting. Biochimica et Biophysica Acta (BBA)-Proteins and Proteomics, 1824(1), 3-13.
Ciechanover, A., Heller, H., Elias, S., Haas, A. L., & Hershko, A. (1980). ATP-dependent conjugation of reticulocyte proteins with the polypeptide required for protein degradation. Proceedings of the National Academy of Sciences, 77(3), 1365-1368.
Ciechanover, A., & Iwai, K. (2004). The ubiquitin system: from basic mechanisms to the patient bed. IUBMB Life, 56(4), 193-201.
Ciehanover, A., Hod, Y., & Hershko, A. (1978). A heat-stable polypeptide component of an ATP-dependent proteolytic system from reticulocytes. Biochemical and Biophysical Research Communications, 81(4), 1100-1105.
Claiborn, K. C., Sachdeva, M. M., Cannon, C. E., Groff, D. N., Singer, J. D., & Stoffers, D. A. (2010). Pcif1 modulates Pdx1 protein stability and pancreatic β cell function and survival in mice. Journal of Clinical Investigation, 120(10), 3713-3721. https://doi.org/10.1172/JCI40440
Collombat, P., & Mansouri, A. (2009). [Pax4 transdifferentiates glucagon-secreting alpha cells to insulin-secreting beta endocrine pancreatic cells]. Medecine sciences: M/S, 25(8-9), 763-765.
Conserva, F., Gesualdo, L., & Papale, M. (2016). A systems biology overview on human diabetic nephropathy: From genetic susceptibility to post-transcriptional and post-translational modifications. Journal of Diabetes Research, 2016, 1-23.
Costes, S., Gurlo, T., Rivera, J. F., & Butler, P. C. (2014). UCHL1 deficiency exacerbates human islet amyloid polypeptide toxicity in β-cells: Evidence of interplay between the ubiquitin/proteasome system and autophagy. Autophagy, 10(6), 1004-1014.
Costes, S., Huang, C., Gurlo, T., Daval, M., Matveyenko, A. V., Rizza, R. A., Butler, A. E., & Butler, P. C. (2011). β-cell dysfunctional ERAD/ubiquitin/proteasome system in type 2 diabetes mediated by islet amyloid polypeptide-induced UCH-L1 deficiency. Diabetes, 60(1), 227-238.
Crosas, B., & Puig Sàrries, P. (2015). Different mechanisms that promote protein monoubiquitination. Afinidad, 72(570), 95-100.
Decker, K., Goldman, D. C., Grasch, C. L., & Sussel, L. (2006). Gata6 is an important regulator of mouse pancreas development. Developmental Biology, 298(2), 415-429.
Dong, P. D., Provost, E., Leach, S. D., & Stainier, D. Y. (2008). Graded levels of Ptf1a differentially regulate endocrine and exocrine fates in the developing pancreas. Genes & Development, 22(11), 1445-1450.
Doyle, M. J., & Sussel, L. (2007). Nkx2. 2 regulates β-cell function in the mature islet. Diabetes, 56(8), 1999-2007.
Dupont, S., Zacchigna, L., Cordenonsi, M., Soligo, S., Adorno, M., Rugge, M., & Piccolo, S. (2005). Germ-layer specification and control of cell growth by ectodermin, a Smad4 ubiquitin ligase. Cell, 121(1), 87-99.
De Duve, C., Pressman, B. C., Gianetto, R., Wattiaux, R., & Appelmans, F. (1955). Tissue fractionation studies. 6. Intracellular distribution patterns of enzymes in rat-liver tissue. Biochemical Journal, 60(4), 604-617.
Elsayed, A. K., Younis, I., Ali, G., Hussain, K., & Abdelalim, E. M. (2021). Aberrant development of pancreatic beta cells derived from human iPSCs with FOXA2 deficiency. Cell Death & Disease, 12(1), 103.
Engin, F., Yermalovich, A., Nguyen, T., Hummasti, S., Fu, W., Eizirik, D. L., Mathis, D., & Hotamisligil, G. S. (2013). Restoration of the unfolded protein response in pancreatic β cells protects mice against type 1 diabetes. Science Translational Medicine, 5(211), 211ra156.
Fan, Y., Xu, F., Wang, R., & He, J. (2023). Lysine 222 in PPAR γ1 functions as the key site of MuRF2-mediated ubiquitination modification. Scientific Reports, 13(1), 1999.
Fonseca, S. G., Fukuma, M., Lipson, K. L., Nguyen, L. X., Allen, J. R., Oka, Y., & Urano, F. (2005). WFS1 is a novel component of the unfolded protein response and maintains homeostasis of the endoplasmic reticulum in pancreatic β-cells. Journal of Biological Chemistry, 280(47), 39609-39615.
Francis, M., Ashok, A., Ashwathnarayan, A., Banerjee, S., Prasan-Na, J., & Kumar, A. (2023). Advancement in understanding the concept of epithelial to mesenchymal transition in pancreatic β-Cells: implication in diabetes. Current Diabetes Reviews, 19(6), 190522205030. https://doi.org/10.2174/1573399818666220519143414
Fujimoto, K., Ford, E. L., Tran, H., Wice, B. M., Crosby, S. D., Dorn, G. W., & Polonsky, K. S. (2010). Loss of Nix in Pdx1-deficient mice prevents apoptotic and necrotic β cell death and diabetes. Journal of Clinical Investigation, 120(11), 4031-4039.
Gadue, P., Huber, T. L., Paddison, P. J., & Keller, G. M. (2006). Wnt and TGF-β signaling are required for the induction of an in vitro model of primitive streak formation using embryonic stem cells. Proceedings of the National Academy of Sciences, 103(45), 16806-16811.
Gaertner, B., Carrano, A. C., & Sander, M. (2019). Human stem cell models: lessons for pancreatic development and disease. Genes & Development, 33(21-22), 1475-1490.
Gannon, M., Tweedie Ables, E., Crawford, L., Lowe, D., Offield, M. F., Magnuson, M. A., & Wright, C. V. E. (2008). pdx-1 function is specifically required in embryonic β cells to generate appropriate numbers of endocrine cell types and maintain glucose homeostasis. Developmental Biology, 314(2), 406-417.
Gao, N., LeLay, J., Vatamaniuk, M. Z., Rieck, S., Friedman, J. R., & Kaestner, K. H. (2008). Dynamic regulation of Pdx1 enhancers by Foxa1 and Foxa2 is essential for pancreas development. Genes & Development, 22(24), 3435-3448.
Gomes, A. V. (2013). Genetics of proteasome diseases. Scientifica, 2013, 1-30.
Gomes, V. M., Wailemann, R. A. M., Arini, G. S., Oliveira, T. C., Almeida, D. R. Q., Dos Santos, A. F., Terra, L. F., Lortz, S., & Labriola, L. (2021). HSPB1 is essential for inducing resistance to proteotoxic stress in beta-cells. Cells, 10(9), 2178.
Gomez, D. L., O'Driscoll, M., Sheets, T. P., Hruban, R. H., Oberholzer, J., McGarrigle, J. J., & Shamblott, M. J. (2015). Neurogenin 3 expressing cells in the human exocrine pancreas have the capacity for endocrine cell fate. PLoS ONE, 10(8), e0133862.
Gorrepati, K., He, W., Lupse, B., Yuan, T., Maedler, K., & Ardestani, A. (2018). An SCFFBXO28 E3 ligase protects pancreatic β-cells from apoptosis. International Journal of Molecular Sciences, 19(4), 975.
Gradwohl, G., Dierich, A., LeMeur, M., & Guillemot, F. (2000). neurogenin3 is required for the development of the four endocrine cell lineages of the pancreas. Proceedings of the National Academy of Sciences, 97(4), 1607-1611.
Group, D. P. P. R. (2003). Effects of withdrawal from metformin on the development of diabetes in the diabetes prevention program. Diabetes Care, 26(4), 977-980.
Gu, C., Stein, G. H., Pan, N., Goebbels, S., Hörnberg, H., Nave, K.-A., Herrera, P., White, P., Kaestner, K. H., Sussel, L., & Lee, J. E. (2010). Pancreatic β cells require NeuroD to achieve and maintain functional maturity. Cell Metabolism, 11(4), 298-310.
Gumienny, T., & Padgett, R. W. (2002). The other side of TGF-beta superfamily signal regulation: thinking outside the cell. Trends in endocrinology and metabolism: TEM, 13(7), 295-299.
Guney, M. A., & Gannon, M. (2009). Pancreas cell fate. Birth Defects Research Part C: Embryo Today: Reviews, 87(3), 232-248.
Guo, S., Burnette, R., Zhao, L., Vanderford, N. L., Poitout, V., Hagman, D. K., Henderson, E., Özcan, S., Wadzinski, B. E., & Stein, R. (2009). The stability and transactivation potential of the mammalian MafA transcription factor are regulated by serine 65 phosphorylation. Journal of Biological Chemistry, 284(2), 759-765.
Guo, S., Vanderford, N. L., & Stein, R. (2010). Phosphorylation within the MafA N terminus regulates C-terminal dimerization and DNA binding. Journal of Biological Chemistry, 285(17), 12655-12661.
Gupta, A., Behl, T., Aleya, L., Rahman, M. H., Yadav, H. N., Pal, G., Kaur, I., & Arora, S. (2021). Role of UPP pathway in amelioration of diabetes-associated complications. Environmental Science and Pollution Research, 28, 19601-19614.
Hammar, E., Parnaud, G., Bosco, D., Perriraz, N., Maedler, K., Donath, M., Rouiller, D. G., & Halban, P. A. (2004). Extracellular matrix protects pancreatic β-Cells against apoptosis. Diabetes, 53(8), 2034-2041.
Hang, Y., & Stein, R. (2011). MafA and MafB activity in pancreatic β. Trends in endocrinology and metabolism: TEM, 22(9), 364-373.
Hanoun, N., Fritsch, S., Gayet, O., Gigoux, V., Cordelier, P., Dusetti, N., Torrisani, J., & Dufresne, M. (2014). The E3 ubiquitin ligase thyroid hormone receptor-interacting protein 12 targets pancreas transcription factor 1a for proteasomal degradation. Journal of Biological Chemistry, 289(51), 35593-35604.
Hansson, M., Olesen, D. R., Peterslund, J. M. L., Engberg, N., Kahn, M., Winzi, M., Klein, T., Maddox-Hyttel, P., & Serup, P. (2009). A late requirement for Wnt and FGF signaling during activin-induced formation of foregut endoderm from mouse embryonic stem cells. Developmental Biology, 330(2), 286-304.
Harmon, E. B., Apelqvist, A. A., Smart, N. G., Gu, X., Osborne, D. H., & Kim, S. K. (2004). GDF11 modulates NGN3+ islet progenitor cell number and promotes β-cell differentiation in pancreas development.
He, J., Zhang, X., Lian, C., Wu, J., Fang, Y., & Ye, X. (2019). KEAP1/NRF2 axis regulates H2O2-induced apoptosis of pancreatic β-cells. Gene, 691, 8-17.
He, Y., Wang, S., Tong, J., Jiang, S., Yang, Y., Zhang, Z., Xu, Y., Zeng, Y., Cao, B., Moran, M. F., & Mao, X. (2020). The deubiquitinase USP7 stabilizes Maf proteins to promote myeloma cell survival. Journal of Biological Chemistry, 295(7), 2084-2096.
Hebrok, M., Kim, S. K., & Melton, D. A. (1998). Notochord repression of endodermal Sonic hedgehog permits pancreas development. Genes & Development, 12(11), 1705-1713. https://doi.org/10.1101/gad.12.11.1705
Hebrok, M., Kim, S. K., St-Jacques, B., McMahon, A. P., & Melton, D. A. (2000). Regulation of pancreas development by hedgehog signaling. Development, 127(22), 4905-4913.
Hershko, A., Ciechanover, A., & Varshavsky, A. (2000). The ubiquitin system. Nature Medicine, 6(10), 1073-1081.
Hicke, L. (2001). Protein regulation by monoubiquitin. Nature Reviews Molecular Cell Biology, 2(3), 195-201.
Holleman, J., & Marchese, A. (2014). The ubiquitin ligase deltex-3l regulates endosomal sorting of the G protein-coupled receptor CXCR4. Molecular Biology of the Cell, 25(12), 1892-1904.
Hu, Y., Gao, Y., Zhang, M., Deng, K.-Y., Singh, R., Tian, Q., Gong, Y., Pan, Z., Liu, Q., Boisclair, Y. R., & Long, Q. (2019). Endoplasmic reticulum-associated degradation (ERAD) has a critical role in supporting glucose-stimulated insulin secretion in pancreatic β-cells. Diabetes, 68(4), 733-746.
Huotari, M. A., Miettinen, P. J., Palgi, J., Koivisto, T., Ustinov, J., Harari, D., Yarden, Y., & Otonkoski, T. (2002). ErbB signaling regulates lineage determination of developing pancreatic islet cells in embryonic organ culture. Endocrinology, 143(11), 4437-4446.
Jacquemin, P., Durviaux, S. M., Jensen, J., Godfraind, C., Gradwohl, G., Guillemot, F., Madsen, O. D., Carmeliet, P., Dewerchin, M., Collen, D., Rousseau, G. G., & Lemaigre, F. P. (2000). Transcription factor hepatocyte nuclear factor 6 regulates pancreatic endocrine cell differentiation and controls expression of the proendocrine gene ngn3. Molecular and Cellular Biology, 20(12), 4445-4454.
Jacquemin, P., Lemaigre, F. P., & Rousseau, G. G. (2003). The Onecut transcription factor HNF-6 (OC-1) is required for timely specification of the pancreas and acts upstream of Pdx-1 in the specification cascade. Developmental Biology, 258(1), 105-116.
Jean-Charles, P.-Y., Snyder, J. C., & Shenoy, S. K. (2016). Chapter one-ubiquitination and deubiquitination of G protein-coupled receptors. Progress in Molecular Biology and Translational Science, 141, 1-55.
Jennings, R. E., Berry, A. A., Strutt, J. P., Gerrard, D. T., & Hanley, N. A. (2015). Human pancreas development. Development, 142(18), 3126-3137.
Jensen, J., Heller, R. S., Funder-Nielsen, T., Pedersen, E. E., Lindsell, C., Weinmaster, G., Madsen, O. D., & Serup, P. (2000). Independent development of pancreatic alpha- and beta-cells from neurogenin3-expressing precursors: a role for the notch pathway in repression of premature differentiation. Diabetes, 49(2), 163-176. https://doi.org/10.2337/diabetes.49.2.163
Jensen, J., Serup, P., Karlsen, C., Nielsen, T. F., & Madsen, O. D. (1996). mRNA profiling of rat islet tumors reveals Nkx 6.1 as a β-cell-specific homeodomain transcription factor. Journal of Biological Chemistry, 271(31), 18749-18758.
Jiang, F.-X., & Harrison, L. C. (2002). Extracellular signals and pancreatic β-cell development: A brief review. Molecular Medicine, 8(12), 763-770.
Jiang, H., Zheng, S., Qian, Y., Zhou, Y., Dai, H., Liang, Y., He, Y., Gao, R., Lv, H., & Zhang, J. (2023). Restored UBE2C expression in islets promotes β-cell regeneration in mice by ubiquitinating PER1.
Jonatan, D., Spence, J. R., Method, A. M., Kofron, M., Sinagoga, K., Haataja, L., Arvan, P., Deutsch, G. H., & Wells, J. M. (2014). Sox17 regulates insulin secretion in the normal and pathologic mouse β cell. PLoS ONE, 9(8), e104675.
Jørgensen, M. C., Ahnfelt-Rønne, J., Hald, J., Madsen, O. D., Serup, P., & Hecksher-Sørensen, J. (2007). An illustrated review of early pancreas development in the mouse. Endocrine Reviews, 28(6), 685-705.
Kahn, S. E., Andrikopoulos, S., & Verchere, C. B. (1999). Islet amyloid: A long-recognized but underappreciated pathological feature of type 2 diabetes. Diabetes, 48(2), 241-253.
Kanai, K., Aramata, S., Katakami, S., Yasuda, K., & Kataoka, K. (2011). Proteasome activator PA28 stimulates degradation of GSK3-phosphorylated insulin transcription activator MAFA. Journal of Molecular Endocrinology, 47(1), 119-127.
Kanai, Y., Kanai-Azuma, M., Noce, T., Saido, T. C., Shiroishi, T., Hayashi, Y., & Yazaki, K. (1996). Identification of two Sox17 messenger RNA isoforms, with and without the high mobility group box region, and their differential expression in mouse spermatogenesis. The Journal of Cell Biology, 133(3), 667-681.
Kaneto, H., Miyagawa, J., Kajimoto, Y., Yamamoto, K., Watada, H., Umayahara, Y., Hanafusa, T., Matsuzawa, Y., Yamasaki, Y., Higashiyama, S., & Taniguchi, N. (1997). Expression of heparin-binding epidermal growth factor-like growth factor during pancreas development. Journal of Biological Chemistry, 272(46), 29137-29143.
Katsumoto, K., Fukuda, K., Kimura, W., Shimamura, K., Yasugi, S., & Kume, S. (2009). Origin of pancreatic precursors in the chick embryo and the mechanism of endoderm regionalization. Mechanisms of Development, 126(7), 539-551.
Katsumoto, K., & Kume, S. (2011). Endoderm and mesoderm reciprocal signaling mediated by CXCL12 and CXCR4 regulates the migration of angioblasts and establishes the pancreatic fate. Development, 138(10), 1947-1955.
Katsumoto, K., & Kume, S. (2013). The role of CXCL12-CXCR4 signaling pathway in pancreatic development. Theranostics, 3(1), 11-17.
Kaur, K., Park, H., Pandey, N., Azuma, Y., & De Guzman, R. N. (2017). Identification of a new small ubiquitin-like modifier (SUMO)-interacting motif in the E3 ligase PIASy. Journal of Biological Chemistry, 292(24), 10230-10238.
Kawaguchi, Y., Cooper, B., Gannon, M., Ray, M., MacDonald, R. J., & Wright, C. V. E. (2002). The role of the transcriptional regulator Ptf1a in converting intestinal to pancreatic progenitors. Nature Genetics, 32(1), 128-134.
Kayali, A. G., Lopez, A. D., Hao, E., Hinton, A., Hayek, A., & King, C. C. (2012). The SDF-1α/CXCR4 axis is required for proliferation and maturation of human fetal pancreatic endocrine progenitor cells. PLoS ONE, 7(6), e38721.
Ketola, I., Otonkoski, T., Pulkkinen, M. A., Niemi, H., Palgi, J., Jacobsen, C. M., Wilson, D. B., & Heikinheimo, M. (2004). Transcription factor GATA-6 is expressed in the endocrine and GATA-4 in the exocrine pancreas. Molecular and Cellular Endocrinology, 226(1-2), 51-57.
Kim, M.-H., Kim, E.-H., Jung, H. S., Yang, D., Park, E.-Y., & Jun, H.-S. (2017). EX4 stabilizes and activates Nrf2 via PKCδ, contributing to the prevention of oxidative stress-induced pancreatic beta cell damage. Toxicology and Applied Pharmacology, 315, 60-69.
Kim, S. K., & Melton, D. A. (1998). Pancreas development is promoted by cyclopamine, a hedgehog signaling inhibitor. Proceedings of the National Academy of Sciences, 95(22), 13036-13041.
Kim, Y. Y., Jang, H., Lee, G., Jeon, Y. G., Sohn, J. H., Han, J. S., Lee, W. T., Park, J., Huh, J. Y., Nahmgoong, H., Han, S. M., Kim, J., Pak, M., Kim, S., Kim, J. S., & Kim, J. B. (2022). Hepatic GSK3β-dependent CRY1 degradation contributes to diabetic hyperglycemia. Diabetes, 71(7), 1373-1387.
Kitamura, T. (2013). The role of FOXO1 in β-cell failure and type 2 diabetes mellitus. Nature Reviews Endocrinology, 9(10), 615-623.
Kitamura, Y. I., Kitamura, T., Kruse, J.-P., Raum, J. C., Stein, R., Gu, W., & Accili, D. (2005). FoxO1 protects against pancreatic β cell failure through NeuroD and MafA induction. Cell Metabolism, 2(3), 153-163. https://doi.org/10.1016/j.cmet.2005.08.004
Klein, S., Meng, R., Montenarh, M., & Götz, C. (2016). The phosphorylation of PDX-1 by protein kinase CK2 is crucial for its stability. Pharmaceuticals, 10(1), 2.
Kobayashi, M., Kikuchi, O., Sasaki, T., Kim, H.-J., Yokota-Hashimoto, H., Lee, Y.-S., Amano, K., Kitazumi, T., Susanti, V. Y., Kitamura, Y. I., & Kitamura, T. (2012). FoxO1 as a double-edged sword in the pancreas: analysis of pancreas-and β-cell-specific FoxO1 knockout mice. American Journal of Physiology-Endocrinology and Metabolism, 302(5), E603-E613.
Komander, D., & Rape, M. (2012). The ubiquitin code. Annual Review of Biochemistry, 81, 203-229.
Kong, C., Guo, Z., Liu, F., Tang, N., Wang, M., Yang, D., Li, C., Yang, Z., Ma, Y., Wang, P., & Tang, Q. (2023). Triad3A-Mediated K48-Linked ubiquitination and degradation of TLR9 impairs mitochondrial bioenergetics and exacerbates diabetic cardiomyopathy. Journal of Advanced Research, 1232(23). https://doi.org/10.1016/j.jare.2023.08.015
Koutsourakis, M., Langeveld, A., Patient, R., Beddington, R., & Grosveld, F. (1999). The transcription factor GATA6 is essential for early extraembryonic development. Development, 126(9), 723-732.
Krapp, A., Knöfler, M., Ledermann, B., Bürki, K., Berney, C., Zoerkler, N., Hagenbüchle, O., & Wellauer, P. K. (1998). The bHLH protein PTF1-p48 is essential for the formation of the exocrine and the correct spatial organization of the endocrine pancreas. Genes & Development, 12(23), 3752-3763.
Kraus, M. R., & Grapin-Botton, A. (2012). Patterning and shaping the endoderm in vivo and in culture. Current Opinion in Genetics & Development, 22(4), 347-353.
Kumar, M., Jordan, N., Melton, D., & Grapin-Botton, A. (2003). Signals from lateral plate mesoderm instruct endoderm toward a pancreatic fate. Developmental Biology, 259(1), 109-122.
Lazaridou, A., Gioulvanidou, S., Mascalidis, C., & Tsitouridis, I. (2022). Embryological development and congenital anomalies of the pancreas: A pictorial review. Hellenic Journal Οf Radiology, 7(3), 32-51.
Lee, C. S., Sund, N. J., Behr, R., Herrera, P. L., & Kaestner, K. H. (2005). Foxa2 is required for the differentiation of pancreatic α-cells. Developmental Biology, 278(2), 484-495.
Lee, H. S., Suh, J. Y., Kang, B.-C., & Lee, E. (2021). Lipotoxicity dysregulates the immunoproteasome in podocytes and kidneys in type 2 diabetes. American Journal of Physiology-Renal Physiology, 320(4), F548-F558.
Lee, J.-H., Lee, J.-H., & Rane, S. G. (2021). TGF-β signaling in pancreatic islet β cell development and function. Endocrinology, 162(3), 1-10. https://doi.org/10.1210/endocr/bqaa233
Leone, P., Shin, E.-C., Perosa, F., Vacca, A., Dammacco, F., & Racanelli, V. (2013). MHC class I antigen processing and presenting machinery: Organization, function, and defects in tumor cells. JNCI Journal of the National Cancer Institute, 105(16), 1172-1187.
LeRoith, D. (2002). β-cell dysfunction and insulin resistance in type 2 diabetes: role of metabolic and genetic abnormalities. The American Journal of Medicine, 113(6), 3-11.
Li, H., Arber, S., Jessell, T. M., & Edlund, H. (1999). Selective agenesis of the dorsal pancreas in mice lacking homeobox gene Hlxb9. Nature Genetics, 23(1), 67-70.
Li, L. C., Qiu, W. L., Zhang, Y. W., Xu, Z. R., Xiao, Y. N., Hou, C., Lamaoqiezhong, C., Yu, P., Cheng, X., & Xu, C. R. (2018). Single-cell transcriptomic analyses reveal distinct dorsal/ventral pancreatic programs. EMBO Reports, 19(10), e46148.
Li, S., Yu, G., Huang, W., Wang, R., Pu, P., & Chen, M. (2019). RING finger protein 10 is a potential drug target for diabetic vascular complications. Molecular Medicine Reports, 20(2), 931-938.
Li, X., Elmira, E., Rohondia, S., Wang, J., Liu, J., & Dou, Q. P. (2018). A patent review of the ubiquitin ligase system: 2015-2018. Expert Opinion on Therapeutic Patents, 28(12), 919-937.
Li, X.-Y., Zhai, W.-J., & Teng, C.-B. (2015). Notch signaling in pancreatic development. International Journal of Molecular Sciences, 17(1), 48.
Liang, J., Chirikjian, M., Pajvani, U. B., & Bartolomé, A. (2022). MafA regulation in β-cells: From transcriptional to post-translational mechanisms. Biomolecules, 12(4), 535.
Liang, L., Li, S., Liu, H., Mao, Y., Liu, L., Zhang, X., Peng, W., Xiao, Y., Zhang, F., Shi, M., Wang, Y., & Guo, B. (2021). Blood glucose control contributes to protein stability of Ski-related novel protein N in a rat model of diabetes. Experimental and Therapeutic Medicine, 22(5), 1341.
Lin, K. H., Ali, A., Kuo, C. H., Yang, P. C., Kumar, V. B., Padma, V. V., Lo, J. F., Huang, C. Y., & Kuo, W. W. (2022). Carboxyl terminus of HSP70-interacting protein attenuates advanced glycation end products-induced cardiac injuries by promoting NFκB proteasomal degradation. Journal of Cellular Physiology, 237(3), 1888-1901.
Lingbeck, J. M., Trausch-Azar, J. S., Ciechanover, A., & Schwartz, A. L. (2003). Determinants of nuclear and cytoplasmic ubiquitin-mediated degradation of MyoD. Journal of Biological Chemistry, 278(3), 1817-1823. https://doi.org/10.1074/jbc.M208815200
Litwak, S. A., Wali, J. A., Pappas, E. G., Saadi, H., Stanley, W. J., Varanasi, L. C., Kay, T. W. H., Thomas, H. E., & Gurzov, E. N. (2015). Lipotoxic stress induces pancreatic β-cell apoptosis through modulation of Bcl-2 proteins by the ubiquitin-proteasome system. Journal of Diabetes Research, 2015, 1-16.
Liu, L., Huang, S., Xu, M., Gong, Y., Li, D., Wan, C., Wu, H., & Tang, Q. (2021). Isoquercitrin protects HUVECs against high glucose-induced apoptosis through regulating p53 proteasomal degradation. International Journal of Molecular Medicine, 48(1), 122.
Liu, P., Wakamiya, M., Shea, M. J., Albrecht, U., Behringer, R. R., & Bradley, A. (1999). Requirement for Wnt3 in vertebrate axis formation. Nature Genetics, 22(4), 361-365.
Malenczyk, K., Szodorai, E., Schnell, R., Lubec, G., Szabó, G., Hökfelt, T., & Harkany, T. (2018). Secretagogin protects Pdx1 from proteasomal degradation to control a transcriptional program required for β cell specification. Molecular Metabolism, 14, 108-120. https://doi.org/10.1016/j.molmet.2018.05.019
Mamin, A., & Philippe, J. (2007). Activin A decreases glucagon and arx gene expression in α-cell lines. Molecular Endocrinology, 21(1), 259-273.
Marchese, A., & Benovic, J. L. (2001). Agonist-promoted ubiquitination of the G protein-coupled receptor CXCR4 mediates lysosomal sorting. Journal of Biological Chemistry, 276(49), 45509-45512.
Marfella, R., D'Amico, M., Di Filippo, C., Siniscalchi, M., Sasso, F., Ferraraccio, F., Rossi, F., & Paolisso, G. (2007). The possible role of the ubiquitin proteasome system in the development of atherosclerosis in diabetes. Cardiovascular Diabetology, 6(1), 35.
Masui, T., Swift, G. H., Deering, T., Shen, C., Coats, W. S., Long, Q., Elsässer, H. P., Magnuson, M. A., & MacDonald, R. J. (2010). Replacement of Rbpj with Rbpjl in the PTF1 complex controls the final maturation of pancreatic acinar cells. Gastroenterology, 139(1), 270-280.
Matveyenko, A. V., & Butler, P. C. (2008). Relationship between β-cell mass and diabetes onset. Diabetes, Obesity and Metabolism, 10, 23-31.
McDermott, A., Jacks, J., Kessler, M., Emanuel, P. D., & Gao, L. (2015). Proteasome-associated autoinflammatory syndromes: advances in pathogeneses, clinical presentations, diagnosis, and management. International Journal of Dermatology, 54(2), 121-129.
Mfopou, J. K., Chen, B., Mateizel, I., Sermon, K., & Bouwens, L. (2010). Noggin, retinoids, and fibroblast growth factor regulate hepatic or pancreatic fate of human embryonic stem cells. Gastroenterology, 138(7), 2233-2245.e14.
Mines, M. A., Goodwin, J. S., Limbird, L. E., Cui, F.-F., & Fan, G.-H. (2009). Deubiquitination of CXCR4 by USP14 is critical for both CXCL12-induced CXCR4 degradation and chemotaxis but not ERK activation. Journal of Biological Chemistry, 284(9), 5742-5752.
Ming, Z., Vining, B., Bagheri-Fam, S., & Harley, V. (2022). SOX9 in organogenesis: Shared and unique transcriptional functions. Cellular and Molecular Life Sciences, 79(10), 522.
Moon, J., Parry, G., & Estelle, M. (2004). The ubiquitin-proteasome pathway and plant development. The Plant Cell, 16(12), 3181-3195.
Morrisey, E. E., Tang, Z., Sigrist, K., Lu, M. M., Jiang, F., Ip, H. S., & Parmacek, M. S. (1998). GATA6 regulates HNF4 and is required for differentiation of visceral endoderm in the mouse embryo. Genes and Development, 12(22), 3579-3590.
Murtaugh, L. C. (2007). Pancreas and beta-cell development: from the actual to the possible.
Murtaugh, L. C., & Melton, D. A. (2003). Genes, signals, and lineages in pancreas development. Annual Review of Cell and Developmental Biology, 19(1), 71-89.
Nagao, Y., Amo-Shiinoki, K., Nakabayashi, H., Hatanaka, M., Kondo, M., Matsunaga, K., Emoto, M., Okuya, S., Tanizawa, Y., & Tanabe, K. (2022). Gsk-3-mediated proteasomal degradation of ATF4 is a proapoptotic mechanism in mouse pancreatic β-cells. International Journal of Molecular Sciences, 23(21), 13586.
Nandi, D., Tahiliani, P., Kumar, A., & Chandu, D. (2006). The ubiquitin-proteasome system. Journal of Biosciences, 31(1), 137-155. https://doi.org/10.1007/BF02705243
Napolitano, T., Avolio, F., Courtney, M., Vieira, A., Druelle, N., Ben-Othman, N., Hadzic, B., Navarro, S., & Collombat, P. (2015). Pax4 acts as a key player in pancreas development and plasticity. Seminars in Cell & Developmental Biology, 44, 107-114.
Naujokat, C., & Šarić, T. (2007). Concise review: role and function of the ubiquitin-proteasome system in mammalian stem and progenitor cells. Stem Cells, 25(10), 2408-2418.
Nishida, T., & Yasuda, H. (2002). PIAS1 and PIASx alpha function as SUMO-E3 ligases toward androgen receptor and repress androgen receptor-dependent transcription. Journal of Biological Chemistry, 277(44), 41311-41317.
Nishimura, W., Takahashi, S., & Yasuda, K. (2015). MafA is critical for maintenance of the mature beta cell phenotype in mice. Diabetologia, 58, 566-574.
Offield, M. F., Jetton, T. L., Labosky, P. A., Ray, M., Stein, R. W., Magnuson, M. A., Hogan, B. L. M., & Wright, C. V. E. (1996). PDX-1 is required for pancreatic outgrowth and differentiation of the rostral duodenum. Development, 122(3), 983-995.
Oliver-Krasinski, J. M., Kasner, M. T., Yang, J., Crutchlow, M. F., Rustgi, A. K., Kaestner, K. H., & Stoffers, D. A. (2009). The diabetes gene Pdx1 regulates the transcriptional network of pancreatic endocrine progenitor cells in mice. Journal of Clinical Investigation, 119(7), 1888-1898.
Ostertag, M. S., Messias, A. C., Sattler, M., & Popowicz, G. M. (2019). The structure of the SPOP-Pdx1 interface reveals insights into the phosphorylation-dependent binding regulation. Structure, 27(2), 327-334.e3.
Pagliuca, F. W., & Melton, D. A. (2013). How to make a functional β-cell. Development, 140(12), 2472-2483.
Pan, F. C., & Wright, C. (2011). Pancreas organogenesis: from bud to plexus to gland. Developmental Dynamics, 240(3), 530-565.
Passmore, L. A., & Barford, D. (2004). Getting into position: the catalytic mechanisms of protein ubiquitylation. Biochemical Journal, 379(3), 513-525.
Pecoits-Filho, R., Abensur, H., Betônico, C. C., Machado, A. D., Parente, E. B., Queiroz, M., Salles, J. E., Titan, S., & Vencio, S. (2016). Interactions between kidney disease and diabetes: Dangerous liaisons. Diabetology & Metabolic Syndrome, 8(1), 50.
Peng, W., Zhou, X., Xu, T., Mao, Y., Zhang, X., Liu, H., Liang, L., Liu, L., Liu, L., Xiao, Y., Zhang, F., Li, S., Shi, M., Zhou, Y., Tang, L., Wang, Y., & Guo, B. (2022). BMP-7 ameliorates partial epithelial-mesenchymal transition by restoring SnoN protein level via Smad1/5 pathway in diabetic kidney disease. Cell Death & Disease, 13(3), 254.
Petroski, M. D., & Deshaies, R. J. (2005). Function and regulation of cullin-RING ubiquitin ligases. Nature Reviews Molecular Cell Biology, 6(1), 9-20.
Pickart, C. M. (2001). Mechanisms underlying ubiquitination. Annual Review of Biochemistry, 70(1), 503-533.
Pinney, S. E., Oliver-Krasinski, J., Ernst, L., Hughes, N., Patel, P., Stoffers, D. A., Russo, P., & De León, D. D. (2011). Neonatal diabetes and congenital malabsorptive diarrhea attributable to a novel mutation in the human neurogenin-3 gene coding sequence. The Journal of Clinical Endocrinology and Metabolism, 96(7), 1960-1965.
Pontrelli, P., Conserva, F., Papale, M., Oranger, A., Barozzino, M., Vocino, G., Rocchetti, M. T., Gigante, M., Castellano, G., Rossini, M., Simone, S., Laviola, L., Giorgino, F., Grandaliano, G., Paolo, S., & Gesualdo, L. (2017). Lysine 63 ubiquitination is involved in the progression of tubular damage in diabetic nephropathy. The FASEB Journal, 31(1), 308-319.
Prado, C. L., Pugh-Bernard, A. E., Elghazi, L., Sosa-Pineda, B., & Sussel, L. (2004). Ghrelin cells replace insulin-producing β cells in two mouse models of pancreas development. Proceedings of the National Academy of Sciences, 101(9), 2924-2929.
Qu, J., Zou, T., & Lin, Z. (2021). The roles of the ubiquitin-proteasome system in the endoplasmic reticulum stress pathway. International Journal of Molecular Sciences, 22(4), 1526.
Queisser, M. A., Yao, D., Geisler, S., Hammes, H.-P., Lochnit, G., Schleicher, E. D., Brownlee, M., & Preissner, K. T. (2010). Hyperglycemia impairs proteasome function by methylglyoxal. Diabetes, 59(3), 670-678.
Rao, H., Uhlmann, F., Nasmyth, K., & Varshavsky, A. (2001). Degradation of a cohesin subunit by the N-end rule pathway is essential for chromosome stability. Nature, 410(6831), 955-959.
Reddy, S. S., Shruthi, K., Prabhakar, Y. K., Sailaja, G., & Reddy, G. B. (2018). Implication of altered ubiquitin-proteasome system and ER stress in the muscle atrophy of diabetic rats. Archives of Biochemistry and Biophysics, 639, 16-25.
Reers, C., Erbel, S., Esposito, I., Schmied, B., Büchler, M. W., Nawroth, P. P., & Ritzel, R. A. (2009). Impaired islet turnover in human donor pancreata with aging. European Journal of Endocrinology, 160(2), 185-191.
Roark, R., Itzhaki, L., & Philpott, A. (2012). Complex regulation controls Neurogenin3 proteolysis. Biology Open, 1(12), 1264-1272.
Rocha, M., Apostolova, N., Diaz-Rua, R., Muntane, J., & Victor, V. M. (2020). Mitochondria and T2D: Role of autophagy, ER stress, and inflammasome. Trends in Endocrinology and Metabolism: TEM, 31(10), 725-741.
Ron, D., & Walter, P. (2007). Signal integration in the endoplasmic reticulum unfolded protein response. Nature Reviews Molecular Cell Biology, 8(7), 519-529.
Rulifson, I. C., Karnik, S. K., Heiser, P. W., ten Berge, D., Chen, H., Gu, X., Taketo, M. M., Nusse, R., Hebrok, M., & Kim, S. K. (2007). Wnt signaling regulates pancreatic β cell proliferation. Proceedings of the National Academy of Sciences, 104(15), 6247-6252. https://doi.org/10.1073/pnas.0701509104
Sabaratnam, R., Skov, V., Paulsen, S. K., Juhl, S., Kruse, R., Hansen, T., Halkier, C., Kristensen, J. M., Vind, B. F., Richelsen, B., Knudsen, S., Dahlgaard, J., Beck-Nielsen, H., Kruse, T. A., & Højlund, K. (2022). A signature of exaggerated adipose tissue dysfunction in type 2 diabetes is linked to low plasma adiponectin and increased transcriptional activation of proteasomal degradation in muscle. Cells, 11(13), 2005.
Saez, I., Koyuncu, S., Gutierrez-Garcia, R., Dieterich, C., & Vilchez, D. (2018). Insights into the ubiquitin-proteasome system of human embryonic stem cells. Scientific Reports, 8(1), 4092.
Sancho, R., Gruber, R., Gu, G., & Behrens, A. (2014). Loss of Fbw7 reprograms adult pancreatic ductal cells into α, δ, and β cells. Cell Stem Cell, 15(2), 139-153. https://doi.org/10.1016/j.stem.2014.06.019
Sander, M., Sussel, L., Conners, J., Scheel, D., Kalamaras, J., Cruz, F. D., Schwitzgebel, V., Hayes-Jordan, A., & German, M. (2000). Homeobox gene Nkx6. 1 lies downstream of Nkx2. 2 in the major pathway of β-cell formation in the pancreas. Development, 127(24), 5533-5540.
Scaglione, K. M., Basrur, V., Ashraf, N. S., Konen, J. R., Elenitoba-Johnson, K. S. J., Todi, S. V., & Paulson, H. L. (2013). The ubiquitin-conjugating enzyme (E2) Ube2w ubiquitinates the N terminus of substrates. Journal of Biological Chemistry, 288(26), 18784-18788.
Schlesinger, D. H., Goldstein, G., & Niall, H. D. (1975). Complete amino acid sequence of ubiquitin, an adenylate cyclase stimulating polypeptide probably universal in living cells. Biochemistry, 14(10), 2214-2218.
Seifert, B. A., & Xiong, Y. (2014). Out of the F-box: reawakening the pancreas. Cell Stem Cell, 15(2), 111-112.
Selenina, V., Tsimokha, S., & Tomilin, N. (2017). Proteasomes in protein homeostasis of pluripotent stem cells. Acta Naturae, 9(3), 39-47.
Seymour, P. A., Freude, K. K., Tran, M. N., Mayes, E. E., Jensen, J., Kist, R., Scherer, G., & Sander, M. (2007). SOX9 is required for maintenance of the pancreatic progenitor cell pool. Proceedings of the National Academy of Sciences, 104(6), 1865-1870.
Sherwood, R. I., Chen, T. Y. A., & Melton, D. A. (2009). Transcriptional dynamics of endodermal organ formation. Developmental Dynamics, 238(1), 29-42.
Sherwood, R. I., Jitianu, C., Cleaver, O., Shaywitz, D. A., Lamenzo, J. O., Chen, A. E., Golub, T. R., & Melton, D. A. (2007). Prospective isolation and global gene expression analysis of definitive and visceral endoderm. Developmental Biology, 304(2), 541-555.
Shih, H. P., Kopp, J. L., Sandhu, M., Dubois, C. L., Seymour, P. A., Grapin-Botton, A., & Sander, M. (2012). A notch-dependent molecular circuitry initiates pancreatic endocrine and ductal cell differentiation. Development, 139(14), 2488-2499.
Smalle, J., & Vierstra, R. D. (2004). The ubiquitin 26S proteasome proteolytic pathway. Annual review of plant biology, 55, 555-590.
Soumya, D., & Srilatha, B. (2011). Late stage complications of diabetes and insulin resistance. J Diabetes Metab, 2(9), 1000167.
Spence, J. R., Lange, A. W., Lin, S.-C. J., Kaestner, K. H., Lowy, A. M., Kim, I., Whitsett, J. A., & Wells, J. M. (2009). Sox17 regulates organ lineage segregation of ventral foregut progenitor cells. Developmental Cell, 17(1), 62-74.
Spooner, B. S., Walther, B. T., & Rutter, W. J. (1970). The development of the dorsal and ventral mammalian pancreas in vivo and in vitro. The Journal of Cell Biology, 47(1), 235-246.
Sussel, L., Kalamaras, J., Hartigan-O'Connor, D. J., Meneses, J. J., Pedersen, R. A., Rubenstein, J. L. R., & German, M. S. (1998). Mice lacking the homeodomain transcription factor Nkx2. 2 have diabetes due to arrested differentiation of pancreatic β cells. Development, 125(12), 2213-2221.
Svikle, Z., Peterfelde, B., Sjakste, N., Baumane, K., Verkauskiene, R., Jeng, C.-J., & Sokolovska, J. (2022). Ubiquitin-proteasome system in diabetic retinopathy. PeerJ, 10, e13715.
Talchai, C., Xuan, S., Lin, H. V., Sussel, L., & Accili, D. (2012). Pancreatic β cell dedifferentiation as a mechanism of diabetic β cell failure. Cell, 150(6), 1223-1234.
Thowfeequ, S., Ralphs, K. L., Yu, W.-Y., Slack, J. M. W., & Tosh, D. (2007). Betacellulin inhibits amylase and glucagon production and promotes beta cell differentiation in mouse embryonic pancreas. Diabetologia, 50, 1688-1697.
Tomasi, M. L., & Ramani, K. (2018). SUMOylation and phosphorylation cross-talk in hepatocellular carcinoma. Translational Gastroenterology and Hepatology, 3, 20.
Tschen, S.-I., Georgia, S., Dhawan, S., & Bhushan, A. (2011). Skp2 is required for incretin hormone-mediated β-cell proliferation. Molecular Endocrinology, 25(12), 2134-2143.
Uruno, A., Yagishita, Y., & Yamamoto, M. (2015). The Keap1-Nrf2 system and diabetes mellitus. Archives of Biochemistry and Biophysics, 566, 76-84.
Varshavsky, A. (1997). The ubiquitin system. Trends in Biochemical Sciences, 22(10), 383-387.
Varshavsky, A. (2006). The early history of the ubiquitin field. Protein Science, 15(3), 647-654. https://doi.org/10.1110/ps.052012306
Vidaković, M., Grdović, N., Dinić, S., Mihailović, M., Uskoković, A., & Arambašić Jovanović, J. (2015). The importance of the CXCL12/CXCR4 axis in therapeutic approaches to diabetes mellitus attenuation. Frontiers in Immunology, 6, 403.
Vig, S., Lambooij, J. M., Zaldumbide, A., & Guigas, B. (2021). Endoplasmic reticulum-mitochondria crosstalk and beta-cell destruction in type 1 diabetes. Frontiers in Immunology, 12, 669492.
Volchuk, A., & Ron, D. (2010). The endoplasmic reticulum stress response in the pancreatic β-cell. Diabetes, Obesity and Metabolism, 12, 48-57.
Vosper, J. M. D., McDowell, G. S., Hindley, C. J., Fiore-Heriche, C. S., Kucerova, R., Horan, I., & Philpott, A. (2009). Ubiquitylation on canonical and non-canonical sites targets the transcription factor neurogenin for ubiquitin-mediated proteolysis. Journal of Biological Chemistry, 284(23), 15458-15468.
Waldrip, W. R., Bikoff, E. K., Hoodless, P. A., Wrana, J. L., & Robertson, E. J. (1998). Smad2 signaling in extraembryonic tissues determines anterior-posterior polarity of the early mouse embryo. Cell, 92(6), 797-808.
Wang, Q., Elghazi, L., Martin, S., Martins, I., Srinivasan, R. S., Geng, X., Sleeman, M., Collombat, P., Houghton, J., & Sosa-Pineda, B. (2008). Ghrelin is a novel target of Pax4 in endocrine progenitors of the pancreas and duodenum. Developmental Dynamics, 237(1), 51-61.
Wang, W.-H., Chen, S.-K., Huang, H.-C., & Juan, H.-F. (2021). Proteomic analysis reveals that metformin suppresses PSMD2, STIP1, and CAP1 for preventing gastric cancer AGS cell proliferation and migration. ACS Omega, 6(22), 14208-14219.
Weisberg, S., Leibel, R., & Tortoriello, D. V. (2016). Proteasome inhibitors, including curcumin, improve pancreatic β-cell function and insulin sensitivity in diabetic mice. Nutrition & Diabetes, 6(4), 205.
Weissman, A. M. (2001). Themes and variations on ubiquitylation. Nature Reviews Molecular Cell Biology, 2(3), 169-178.
Wessells, N. K., & Cohen, J. H. (1967). Early pancreas organogenesis: morphogenesis, tissue interactions, and mass effects. Developmental Biology, 15(3), 237-270.
Westermark, P., Andersson, A., & Westermark, G. T. (2011). Islet amyloid polypeptide, islet amyloid, and diabetes mellitus. Physiological Reviews, 91(3), 795-826. https://doi.org/10.1152/physrev.00042.2009
Wilson, P. C., Wu, H., Kirita, Y., Uchimura, K., Ledru, N., Rennke, H. G., Welling, P. A., Waikar, S. S., & Humphreys, B. D. (2019). The single-cell transcriptomic landscape of early human diabetic nephropathy. Proceedings of the National Academy of Sciences, 116(39), 19619-19625.
Wu, D., Wang, Y., Zhou, Y., Gao, H., & Zhao, B. (2023). Inhibition of the proteasome regulator PA28 aggravates oxidized protein overload in the diabetic rat brain. Cellular and Molecular Neurobiology, 43, 2857-2869.
Wu, T., Zhang, S., Xu, J., Zhang, Y., Sun, T., Shao, Y., Wang, J., Tang, W., Chen, F., & Han, X. (2020). HRD1, an important player in pancreatic β-cell failure and therapeutic target for type 2 diabetic mice. Diabetes, 69(5), 940-953.
Xie, Y., Gao, R., Gao, Y., Dong, Z., Moses, R. E., Li, X., & Ge, J. (2022). The proteasome activator REGγ promotes diabetic endothelial impairment by inhibiting HMGA2-GLUT1 pathway. Translational Research, 246, 33-48.
Xu, J., Wu, Y., Song, P., Zhang, M., Wang, S., & Zou, M.-H. (2007). Proteasome-dependent degradation of guanosine 5′-triphosphate cyclohydrolase I causes tetrahydrobiopterin deficiency in diabetes mellitus. Circulation, 116(8), 944-953.
Xu, X., Arunagiri, A., Haataja, L., Alam, M., Ji, S., Qi, L., Tsai, B., Liu, M., & Arvan, P. (2022). Proteasomal degradation of WT proinsulin in pancreatic beta cells. Journal of Biological Chemistry, 298(10), 102406.
Yan, C., Yu, C., Zhang, D., Cui, Y., Zhou, J., & Cui, S. (2016). Protein inhibitor of activated STAT Y (PIASy) regulates insulin secretion by interacting with LIM homeodomain transcription factor Isl1. Scientific Reports, 6(1), 39308.
Yang, Y., Chang, B. H.-J., Samson, S. L., Li, M. V., & Chan, L. (2009). The krüppel-like zinc finger protein Glis3 directly and indirectly activates insulin gene transcription. Nucleic Acids Research, 37(8), 2529-2538.
Yang, Y., Xiao, H., Lin, Z., Chen, R., Li, S., Li, C., Sun, X., Hei, Z., Gong, W., & Huang, H. (2022). The ubiquitination of CKIP-1 mediated by Src aggravates diabetic renal fibrosis. Biochemical Pharmacology, 206, 115339.
You, S., Xu, J., Yin, Z., Wu, B., Wang, P., Hao, M., Cheng, C., Liu, M., Zhao, Y., Jia, P., Jiang, H., Li, D., Cao, L., Zhang, X., Zhang, Y., Sun, Y., & Zhang, N. (2023). Down-regulation of WWP2 aggravates Type 2 diabetes mellitus-induced vascular endothelial injury through modulating ubiquitination and degradation of DDX3X. Cardiovascular Diabetology, 22(1), 107.
ZeRuth, G. T., Takeda, Y., & Jetten, A. M. (2013). The Krüppel-like protein Gli-similar 3 (Glis3) functions as a key regulator of insulin transcription. Molecular Endocrinology, 27(10), 1692-1705.
ZeRuth, G. T., Williams, J. G., Cole, Y. C., & Jetten, A. M. (2015). HECT E3 ubiquitin ligase itch functions as a novel negative regulator of Gli-Similar 3 (Glis3) transcriptional activity. PLoS ONE, 10(7), e0131303.
Zhang, C., Moriguchi, T., Kajihara, M., Esaki, R., Harada, A., Shimohata, H., Oishi, H., Hamada, M., Morito, N., Hasegawa, K., Kudo, T., Engel, J. D., Yamamoto, M., & Takahashi, S. (2005). MafA is a key regulator of glucose-stimulated insulin secretion. Molecular and Cellular Biology, 25(12), 4969-4976.
Zhang, H., Ables, E. T., Pope, C. F., Washington, M. K., Hipkens, S., Means, A. L., Path, G., Seufert, J., Costa, R. H., Leiter, A. B., Magnuson, M. A., & Gannon, M. (2009). Multiple, temporal-specific roles for HNF6 in pancreatic endocrine and ductal differentiation. Mechanisms of Development, 126(11-12), 958-973.
Zhang, T., Kim, D. H., Xiao, X., Lee, S., Gong, Z., Muzumdar, R., Calabuig-Navarro, V., Yamauchi, J., Harashima, H., Wang, R., Bottino, R., Alvarez-Perez, J. C., Garcia-Ocaña, A., Gittes, G., & Dong, H. H. (2016). FoxO1 plays an important role in regulating β-cell compensation for insulin resistance in male mice. Endocrinology, 157(3), 1055-1070.
Zhang, X., Hu, C., Yuan, X.-P., Yuan, Y.-P., Song, P., Kong, C.-Y., Teng, T., Hu, M., Xu, S.-C., Ma, Z.-G., & Tang, Q. Z. (2021). Osteocrin, a novel myokine, prevents diabetic cardiomyopathy via restoring proteasomal activity. Cell Death & Disease, 12(7), 624.
Zhang, Y., Guo, Q., Jiang, G., & Zhang, C. (2021). Dysfunction of Cullin 3 RING E3 ubiquitin ligase causes vasoconstriction and increased sodium reabsorption in diabetes. Archives of Biochemistry and Biophysics, 710, 109000.
Zhong, X., Wang, T., Xie, Y., Wang, M., Zhang, W., Dai, L., Lai, J., Nie, X., He, X., Madhusudhan, T., Zeng, H., & Wang, H. (2021). Activated protein C ameliorates diabetic cardiomyopathy via modulating OTUB1/YB-1/MEF2B axis. Frontiers in Cardiovascular Medicine, 8, 758158.
Zhou, Q., Brown, J., Kanarek, A., Rajagopal, J., & Melton, D. A. (2008). In vivo reprogramming of adult pancreatic exocrine cells to β-cells. Nature, 455(7213), 627-632.