The role of glucokinase and insulin receptor substrate-2 in the proliferation of pancreatic beta cells induced by short-term high-fat diet feeding in mice

Metabolism: Clinical and Experimental

Volumn 85, Issue , 2018, Pages 48-58

  Kitao, Naoyuki ^a   Nakamura, Akinobu ^a   Miyoshi, Hideaki ^a   Nomoto, Hiroshi ^a   Takahashi, Kiyohiko ^a   Omori, Kazuno ^a   Yamamoto, Kohei ^a   Cho, Kyu Yong ^a   Terauchi, Yasuo ^b   Atsumi, Tatsuya ^a  

^a HOKKAIDO UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

^b YOKOHAMA CITY UNIVERSITY   (Japan)

Author keywords

Beta cell proliferation; Glucokinase; High fat diet; Insulin receptor substrate 2

Indexed keywords

BROXURIDINE; FORKHEAD BOX PROTEIN M1; GLUCOKINASE; INSULIN RECEPTOR SUBSTRATE 2; RAPAMYCIN; INSULIN RECEPTOR SUBSTRATE;

AGED; ANIMAL EXPERIMENT; ARTICLE; C57BL 6 MOUSE; CELL PROLIFERATION; CONTROLLED STUDY; FEEDING; GENE EXPRESSION PROFILING; HAPLOINSUFFICIENCY; HISTOPATHOLOGY; IMMUNOHISTOCHEMISTRY; KNOCKOUT MOUSE; LIPID DIET; MALE; MOUSE; NONHUMAN; PANCREAS ISLET BETA CELL; PRIORITY JOURNAL; PROTEIN EXPRESSION LEVEL; UPREGULATION; WESTERN BLOTTING; WILD TYPE MOUSE; ANIMAL; CYTOLOGY; GENETICS; INSULIN RESISTANCE; METABOLISM; PHYSIOLOGY; SIGNAL TRANSDUCTION;

ANIMALS; CELL PROLIFERATION; DIET, HIGH-FAT; GLUCOKINASE; INSULIN RECEPTOR SUBSTRATE PROTEINS; INSULIN RESISTANCE; INSULIN-SECRETING CELLS; MALE; MICE; MICE, KNOCKOUT; SIGNAL TRANSDUCTION;

EID: 85056212107     PISSN: 00260495     EISSN: 15328600     Source Type: Journal    
DOI: 10.1016/j.metabol.2018.03.010     Document Type: Article

References (45)

1. Polonsky, K.S., Sturis, J., Bell, G.I., Non-insulin-dependent diabetes mellitus—a genetically programmed failure of the beta cell to compensate for insulin resistance. N Engl J Med 334 (2002), 777–783.
2. Prentki, M., Nolan, C.J., Islet beta cell failure in type 2 diabetes. J Clin Invest 116 (2006), 1802–1812.
3. Rhodes, C.J., Type 2 diabetes-a matter of beta-cell life and death?. Science 307 (2005), 380–384.
4. Sakuraba, H., Mizukami, H., Yagihashi, N., Wada, R., Hanyu, C., Yagihashi, S., Reduced beta-cell mass and expression of oxidative stress-related DNA damage in the islets of Japanese Type II diabetic patients. Diabetologia 45 (2002), 85–96.
5. Butler, A.E., Janson, J., Bonner-Weir, S., Ritzel, R., Rizza, R.A., Butler, P.C., Beta-cell deficit and increased beta-cell apoptosis in humans with type 2 diabetes. Diabetes 52 (2003), 102–110.
6. Yoon, K.H., Ko, S.H., Cho, J.H., Lee, J.M., Ahn, Y.B., Song, K.H., et al. Selective beta-cell loss and alpha-cell expansion in patients with type 2 diabetes mellitus in Korea. J Clin Endocrinol Metab 88 (2003), 2300–2308.
7. Wang, P., Fiaschi-Taesch, N.M., Vasavada, R.C., Scott, D.K., García-Ocaña, A., Stewart, A.F., Diabetes mellitus—advances and challenges in human beta-cell proliferation. Nat Rev Endocrinol 11 (2015), 201–212.
8. Vetere, A., Choudhary, A., Burns, S.M., Wagner, B.K., Targeting the pancreatic beta-cell to treat diabetes. Nat Rev Drug Discov 13 (2014), 278–289.
9. Teta, M., Rankin, M.M., Long, S.Y., Stein, G.M., Kushner, J.A., Growth and regeneration of adult beta cells does not involve specialized progenitors. Dev Cell 12 (2007), 817–826.
10. Meier, J.J., Butler, A.E., Saisho, Y., Monchamp, T., Galasso, R., Bhushan, A., et al. Beta-cell replication is the primary mechanism subserving the postnatal expansion of beta-cell mass in humans. Diabetes 57 (2008), 1584–1594.
11. Hull, R.L., Kodama, K., Utzschneider, K.M., Carr, D.B., Prigeon, R.L., Kahn, S.E., Dietary-fat-induced obesity in mice results in beta cell hyperplasia but not increased insulin release: evidence for specificity of impaired beta cell adaptation. Diabetologia 48 (2005), 1350–1358.
12. Peshavaria, M., Larmie, B.L., Lausier, J., Satish, B., Habibovic, A., Roskens, V., et al. Regulation of pancreatic beta-cell regeneration in the normoglycemic 60% partial-pancreatectomy mouse. Diabetes 55 (2006), 3289–3298.
13. Togashi, Y., Shirakawa, J., Orime, K., Kaji, M., Sakamoto, E., Tajima, K., et al. Beta-cell proliferation after a partial pancreatectomy is independent of IRS-2 in mice. Endocrinology 155 (2014), 1643–1652.
14. Karnik, S.K., Chen, H., McLean, G.W., Heit, J.J., Gu, X., Zhang, A.Y., et al. Menin controls growth of pancreatic beta-cells in pregnant mice and promotes gestational diabetes mellitus. Science 318 (2007), 806–809.
15. Kim, H., Toyofuku, Y., Lynn, F.C., Chak, E., Uchida, T., Mizukami, H., et al. Serotonin regulates pancreatic beta cell mass during pregnancy. Nat Med 16 (2010), 804–808.
16. Golson, M.L., Misfeldt, A.A., Kopsombut, U.G., Petersen, C.P., Gannon, M., High fat diet regulation of beta-cell proliferation and beta-cell mass. Open Endocrinol J, 4, 2010.
17. Terauchi, Y., Takamoto, I., Kubota, N., Matsui, J., Suzuki, R., Komeda, K., et al. Glucokinase and IRS-2 are required for compensatory beta cell hyperplasia in response to high-fat diet-induced insulin resistance. J Clin Invest 117 (2007), 246–257.
18. Weir, G.C., Bonner-Weir, S., A dominant role for glucose in beta cell compensation of insulin resistance. J Clin Invest 117 (2007), 81–83.
19. Stamateris, R.E., Sharma, R.B., Hollern, D.A., Alonso, L.C., Adaptive beta-cell proliferation increases early in high-fat feeding in mice, concurrent with metabolic changes, with induction of islet cyclin D2 expression. Am J Physiol Endocrinol Metab 305 (2013), E149–59.
20. Mosser, R.E., Maulis, M.F., Moullé V.S., Dunn, J.C., Carboneau, B.A., Arasi, K., et al. High-fat diet-induced beta-cell proliferation occurs prior to insulin resistance in C57Bl/6J male mice. Am J Physiol Endocrinol Metab 308 (2015), E573–82.
21. Woodland, D.C., Liu, W., Leong, J., Sears, M.L., Luo, P., Chen, X., Short-term high-fat feeding induces islet macrophage infiltration and beta-cell replication independently of insulin resistance in mice. Am J Physiol Endocrinol Metab 311 (2016), E763–71.
22. Nakamura, A., Terauchi, Y., Ohyama, S., Kubota, J., Shimazaki, H., Nambu, T., et al. Impact of small-molecule glucokinase activator on glucose metabolism and beta-cell mass. Endocrinology 150 (2009), 1147–1154.
23. Nakamura, A., Togashi, Y., Orime, K., Sato, K., Shirakawa, J., Ohsugi, M., et al. Control of beta cell function and proliferation in mice stimulated by small-molecule glucokinase activator under various conditions. Diabetologia 55 (2012), 1745–1754.
24. Nakamura, A., Tajima, K., Zolzaya, K., Sato, K., Inoue, R., Yoneda, M., et al. Protection from non-alcoholic steatohepatitis and liver tumourigenesis in high fat-fed insulin receptor substrate-1-knockout mice despite insulin resistance. Diabetologia 55 (2012), 3382–3391.
25. Sato, K., Nakamura, A., Shirakawa, J., Muraoka, T., Togashi, Y., Shinoda, K., et al. Impact of the dipeptidyl peptidase-4 inhibitor vildagliptin on glucose tolerance and beta-cell function and mass in insulin receptor substrate-2-knockout mice fed a high-fat diet. Endocrinology 153 (2012), 1093–1102.
26. Matschinsky, F.M., Magnuson, M.A., Zelent, D., Jetton, T.L., Doliba, N., Han, Y., et al. The network of glucokinase-expressing cells in glucose homeostasis and the potential of glucokinase activators for diabetes therapy. Diabetes 55 (2006), 1–12.
27. Nakamura, A., Terauchi, Y., Present status of clinical deployment of glucokinase activators. J Diabetes Investig 6 (2015), 124–132.
28. Terauchi, Y., Sakura, H., Yasuda, K., Iwamoto, K., Takahashi, N., Ito, K., et al. Pancreatic beta-cell-specific targeted disruption of glucokinase gene. Diabetes mellitus due to defective insulin secretion to glucose. J Biol Chem 270 (1995), 30253–30256.
29. Porat, S., Weinberg-Corem, N., Tornovsky-Babaey, S., Schyr-Ben-Haroush, R., Hija, A., Stolovich-Rain, M., et al. Control of pancreatic beta cell regeneration by glucose metabolism. Cell Metab 13 (2011), 440–449.
30. Dadon, D., Tornovsky-Babaey, S., Furth-Lavi, J., Ben-Zvi, D., Ziv, O., Schyr-Ben-Haroush, R., et al. Glucose metabolism: key endogenous regulator of beta-cell replication and survival. Diabetes Obes Metab 14:Suppl. 3 (2012), 101–108.
31. Bernal-Mizrachi, E., Kulkarni, R.N., Scott, D.K., Mauvais-Jarvis, F., Stewart, A.F., Garcia-Ocaña, A., Human beta-cell proliferation and intracellular signaling part 2: still driving in the dark without a road map. Diabetes 63 (2014), 819–831.
32. Stamateris, R.E., Sharma, R.B., Kong, Y., Ebrahimpour, P., Panday, D., Ranganath, P., et al. Glucose induces mouse beta cell proliferation via IRS2, MTOR, and cyclin D2 but not the insulin receptor. Diabetes 65 (2016), 981–995.
33. Withers, D.J., Gutierrez, J.S., Towery, H., Burks, D.J., Ren, J.M., Previs, S., et al. Disruption of IRS-2 causes type 2 diabetes in mice. Nature 391 (1998), 900–904.
34. Kubota, N., Tobe, K., Terauchi, Y., Eto, K., Yamauchi, T., Suzuki, R., et al. Disruption of insulin receptor substrate-2 causes type 2 diabetes due to liver insulin resistance and lack of compensatory beta-cell hyperplasia. Diabetes 49 (2000), 1880–1889.
35. Kubota, N., Terauchi, Y., Tobe, K., Yano, W., Suzuki, R., Ueki, K., et al. Insulin receptor substrate 2 plays a crucial role in beta cells and the hypothalamus. J Clin Invest 114 (2004), 917–927.
36. Wierstra, I., The transcription factor FOXM1 (Forkhead box M1): proliferation-specific expression, transcription factor function, target genes, mouse models, and normal biological roles. Adv Cancer Res 118 (2013), 97–398.
37. Ackermann Misfeldt, A., Costa, R.H., Gannon, M., Beta-cell proliferation, but not neogenesis, following 60% partial pancreatectomy is impaired in the absence of FoxM1. Diabetes 57 (2008), 3069–3077.
38. Zhang, H., Zhang, J., Pope, C.F., Crawford, L.A., Vasavada, R.C., Jagasia, S.M., et al. Gestational diabetes mellitus resulting from impaired beta-cell compensation in the absence of FoxM1, a novel downstream effector of placental lactogen. Diabetes 59 (2010), 143–152.
39. Davis, D.B., Lavine, J.A., Suhonen, J.I., Krautkramer, K.A., Rabaglia, M.E., Sperger, J.M., et al. FoxM1 is up-regulated by obesity and stimulates beta-cell proliferation. Mol Endocrinol 24 (2010), 1822–1834.
40. Shirakawa, J., Fernandez, M., Takatani, T., El Ouaamari, A., Jungtrakoon, P., Okawa, E.R., et al. Insulin signaling regulates the FoxM1/PLK1/CENP—a pathway to promote adaptive pancreatic beta cell proliferation. Cell Metab 25 (2017), 868–882.
41. Zarrouki, B., Benterki, I., Fontés, G., Peyot, M.L., Seda, O., Prentki, M., et al. Epidermal growth factor receptor signaling promotes pancreatic beta-cell proliferation in response to nutrient excess in rats through mTOR and FOXM1. Diabetes 63 (2014), 982–993.
42. Blandino-Rosano, M., Chen, A.Y., Scheys, J.O., Alejandro, E.U., Gould, A.P., Taranukha, T., et al. mTORC1 signaling and regulation of pancreatic beta-cell mass. Cell Cycle 11 (2012), 1892–1902.
43. Teta, M., Long, S.Y., Wartschow, L.M., Rankin, M.M., Kushner, J.A., Very slow turnover of beta-cells in aged adult mice. Diabetes 54 (2005), 2557–2567.
44. Rankin, M.M., Kushner, J.A., Adaptive beta-cell proliferation is severely restricted with advanced age. Diabetes 58 (2009), 1365–1372.
45. Golson, M.L., Dunn, J.C., Maulis, M.F., Dadi, P.K., Osipovich, A.B., Magnuson, M.A., et al. Activation of FoxM1 revitalizes the replicative potential of aged beta-cells in male mice and enhances insulin secretion. Diabetes 64 (2015), 3829–3838.