Regulation of insulin resistance and glucose metabolism by interaction of PIM kinases and insulin receptor substrates

References

• Alvarado, Y., Giles, F.J., and Swords, R.T., 2012. The PIM kinases in hematological cancers. Expert review of hematology, 5 (1), 81–96.
   PubMed Web of Science ®Google Scholar
• Asanidze, E., et al., 2018. Correlation of anti-Mullerian hormone with hormonal and ovarian morphological characteristics in patients with polycystic ovary syndrome with and without insulin resistance. Georgian medical news, 2 (275), 34–40.
   Google Scholar
• Aziz, A.U.R., et al., 2018. PIM kinases and their relevance to the PI3K/AKT/mTOR pathway in the regulation of ovarian cancer. Biomolecules, 8 (1). doi:10.3390/biom8010007.
   PubMed Web of Science ®Google Scholar
• Beharry, Z., et al., 2011. The Pim protein kinases regulate energy metabolism and cell growth. Proceedings of the national academy of sciences of the United States of America, 108 (2), 528–533.
   PubMed Web of Science ®Google Scholar
• Blanco-Aparicio, C., et al., 2011. Pim 1 kinase inhibitor ETP-45299 suppresses cellular proliferation and synergizes with PI3K inhibition. Cancer letters, 300 (2), 145–153.
   PubMed Web of Science ®Google Scholar
• Bluher, M., et al., 2002. Adipose tissue selective insulin receptor knockout protects against obesity and obesity-related glucose intolerance. Developmental cell, 3 (1), 25–38.
   PubMed Web of Science ®Google Scholar
• Boucher, J., Kleinridders, A., and Kahn, C.R., 2014. Insulin receptor signaling in normal and insulin-resistant states. Cold Spring Harbour perspectives in biology, 6 (1), a009191.
   PubMed Web of Science ®Google Scholar
• Boura-Halfon, S. and Zick, Y., 2009. Phosphorylation of IRS proteins, insulin action, and insulin resistance. American journal of physiology–endocrinology and metabolism, 296 (4), E581–E591.
   PubMed Web of Science ®Google Scholar
• Brenner, A.K., et al., 2017. CDC25 inhibition in acute myeloid leukemia: A study of patient heterogeneity and the effects of different inhibitors. Molecules, 22 (3), 446.
   Web of Science ®Google Scholar
• Brunen, D., et al., 2016. Intrinsic resistance to PIM kinase inhibition in AML through p38a-mediated feedback activation of mTOR signaling. Oncotarget, 7 (25), 37407–37419.
   PubMedGoogle Scholar
• Cantley, L.C., 2002. The phosphoinositide 3-kinase pathway. Science (New York, NY), 296 (5573), 1655–1657.
   Google Scholar
• Carlson, C.J., White, M.F., and Rondinone, C.M., 2004. Mammalian target of rapamycin regulates IRS-1 serine 307 phosphorylation. Biochemical and biophysical research communications, 316 (2), 533–539.
   PubMed Web of Science ®Google Scholar
• Cen, B., et al., 2014. The Pim-1 protein kinase is an important regulator of MET receptor tyrosine kinase levels and signaling. Molecular cellular biology, 34 (13), 2517–2532.
   PubMed Web of Science ®Google Scholar
• Chen, H., et al., 2017. Effect of "spleen-stomach harmonizing" needling on insulin resistance and expression of insulin receptor substrate-1, -2, and glucose transporter-4 in insulin resistance type 2 diabetes rats. Zhen Ci Yan Jiu, 42, 197–201.
   PubMedGoogle Scholar
• Chen, K., et al., 2016. eIF4B is a convergent target and critical effector of oncogenic Pim and PI3K/Akt/mTOR signaling pathways in Abl transformants. Oncotarget, 7 (9), 10073–10089.
   PubMedGoogle Scholar
• Choudhary, C., et al., 2009. Mislocalized activation of oncogenic RTKs switches downstream signaling outcomes. Molecular cell, 36 (2), 326–339.
   PubMed Web of Science ®Google Scholar
• Copps, K.D. and White, M.F., 2012. Regulation of insulin sensitivity by serine/threonine phosphorylation of insulin receptor substrate proteins IRS1 and IRS2. Diabetologia, 55 (10), 2565–2582.
   PubMed Web of Science ®Google Scholar
• Corbould, A., 2008. Effects of androgens on insulin action in women: Is androgen excess a component of female metabolic syndrome? Diabetes/metabolism research and reviews, 24 (7), 520–532.
   PubMed Web of Science ®Google Scholar
• Costa, M.M., et al., 2012. Reduction of insulin signalling pathway IRS-1/IRS-2/AKT/mTOR and decrease of epithelial cell proliferation in the prostate of glucocorticoid-treated rats. International journal of experimental pathology, 93 (3), 188–195.
   PubMed Web of Science ®Google Scholar
• Cree-Green, M., et al., 2017. Insulin resistance, hyperinsulinemia, and mitochondria dysfunction in nonobese girls with polycystic ovarian syndrome. Journal of the endocrine society, 1 (7), 931–944.
   PubMed Web of Science ®Google Scholar
• Defronzo, R.A. and Tripathy, D., 2009. Skeletal muscle insulin resistance is the primary defect in type 2 diabetes. Diabetes care, 32 (Suppl_2), S157–S163.
   PubMedGoogle Scholar
• Destefano, M.A. and Jacinto, E., 2013. Regulation of insulin receptor substrate-1 by mTORC2 (mammalian target of rapamycin complex 2). Biochemical society transactions, 41 (4), 896–901.
   PubMedGoogle Scholar
• Dong, X.C., et al., 2008. Inactivation of hepatic Foxo1 by insulin signaling is required for adaptive nutrient homeostasis and endocrine growth regulation. Cell metabolism, 8 (1), 65–76.
   PubMed Web of Science ®Google Scholar
• Eckstein, S.S., Weigert, C., and Lehmann, R., 2017. Divergent roles of IRS (insulin receptor substrate) 1 and 2 in liver and skeletal muscle. Current medicinal chemistry, 24, 1827–1852.
   PubMed Web of Science ®Google Scholar
• El Mkadem, S.A., et al., 2001. Role of allelic variants Gly972Arg of IRS-1 and Gly1057Asp of IRS-2 in moderate-to-severe insulin resistance of women with polycystic ovary syndrome. Diabetes, 50 (9), 2164–2168.
   PubMed Web of Science ®Google Scholar
• Farese, R.V., Sajan, M.P., and Standaert, M.L., 2005. Insulin-sensitive protein kinases (atypical protein kinase C and protein kinase B/Akt): Actions and defects in obesity and type II diabetes. Experimental biology and medicine, 230 (9), 593–605.
   Web of Science ®Google Scholar
• Fratantonio, D., et al., 2017. Cyanidin-3-O-glucoside ameliorates palmitate-induced insulin resistance by modulating IRS-1 phosphorylation and release of endothelial derived vasoactive factors. Biochimica et biophysica acta, 1862 (3), 351–357.
   Google Scholar
• Gaglio, D., et al., 2014. Oncogenic K-Ras decouples glucose and glutamine metabolism to support cancer cell growth. Molecular systems biology, 7 (1), 523.
   Google Scholar
• Groeneveld, M.P., et al., 2016. Acute knockdown of the insulin receptor or its substrates Irs1 and 2 in 3T3-L1 adipocytes suppresses adiponectin production. Scientific reports, 6, 21105.
   PubMed Web of Science ®Google Scholar
• Hahn-Windgassen, A., et al., 2005. Akt activates the mammalian target of rapamycin by regulating cellular ATP level and AMPK activity. Journal of biological chemistry, 280 (37), 32081–32089.
   PubMed Web of Science ®Google Scholar
• Hakuno, F., et al., 2015. The novel functions of high-molecular-mass complexes containing insulin receptor substrates in mediation and modulation of insulin-like activities: Emerging concept of diverse functions by IRS-associated proteins. Frontiers in endocrinology, 6, 73.
   PubMed Web of Science ®Google Scholar
• Hammerman, P.S., et al., 2005. Pim and Akt oncogenes are independent regulators of hematopoietic cell growth and survival. Blood, 105 (11), 4477–4483.
   PubMed Web of Science ®Google Scholar
• Hanke, S. and Mann, M., 2009. The phosphotyrosine interactome of the insulin receptor family and its substrates IRS-1 and IRS-2. Molecular and cellular proteomics, 8 (3), 519–534.
   PubMed Web of Science ®Google Scholar
• Harrington, L.S., et al., 2004. The TSC1-2 tumor suppressor controls insulin-PI3K signaling via regulation of IRS proteins. Journal of cell biology, 166 (2), 213–223.
   PubMed Web of Science ®Google Scholar
• Huang, H., et al., 2018. Circulating bone morphogenetic protein-9 levels are associated with hypertension and insulin resistance in humans. Journal of American society of hypertension, 12 (5), 372–380.
   PubMed Web of Science ®Google Scholar
• Inoue, N., et al., 2008. Cyclin-dependent kinase inhibitor, p21WAF1/CIP1, is involved in adipocyte differentiation and hypertrophy, linking to obesity, and insulin resistance. Journal of biological chemistry, 283 (30), 21220–21229.
   PubMed Web of Science ®Google Scholar
• Ioannidis, A., et al., 2010. Polymorphisms of the insulin receptor and the insulin receptor substrates genes in polycystic ovary syndrome: A Mendelian randomization meta-analysis. Molecular genetics and metabolism, 99 (2), 174–183.
   PubMed Web of Science ®Google Scholar
• Jhorawat, R., et al., 2018. Factors affecting insulin resistance and its relation to vitamin d status and clinical nutritional parameters in dialysis patients: A single-center Indian study. Indian journal of nephrology, 28 (1), 41–45.
   PubMed Web of Science ®Google Scholar
• Karlsson, H.K.R. and Zierath, J.R., 2007. Insulin signaling and glucose transport in insulin resistant human skeletal muscle. Cell biochemistry and biophysics, 48 (2–3), 103–113.
   PubMed Web of Science ®Google Scholar
• Lanzerstorfer, P., et al., 2015. Analysis of insulin receptor substrate signaling dynamics on microstructured surfaces. FEBS journal, 282 (6), 987–1005.
   PubMed Web of Science ®Google Scholar
• Li, F., et al., 2005. Myc stimulates nuclearly encoded mitochondrial genes and mitochondrial biogenesis. Molecular cell biology, 25 (14), 6225–6234.
   PubMed Web of Science ®Google Scholar
• Li, Y., et al., 2004. Protein kinase C theta inhibits insulin signaling by phosphorylating IRS1 at Ser(1101). Journal of biological chemistry, 279 (44), 45304–45307.
   PubMed Web of Science ®Google Scholar
• Lin, M.W., Huang, M.F., and Wu, M.H., 2014. Association of Gly972Arg variant of insulin receptor subtrate-1 and Gly1057Asp variant of insulin receptor subtrate-2 with polycystic ovary syndrome in the Chinese population. Journal of ovarian research, 7 (1), 92.
   PubMedGoogle Scholar
• Linn, D., et al., 2013. Differential regulation of androgen receptor by PIM-1 kinases via phosphorylation-dependent recruitment of distinct ubiquitin E3 ligases. Cancer research, 73 (8 Supplement), 4089.
   Web of Science ®Google Scholar
• Liu, J., et al., 2018. Microcystin-LR disrupts insulin signaling by hyperphosphorylating insulin receptor substrate 1 and glycogen synthase. Environmental toxicology, 33 (1), 16–22.
   PubMed Web of Science ®Google Scholar
• Long, Y.C., et al., 2011. Insulin receptor substrates Irs1 and Irs2 coordinate skeletal muscle growth and metabolism via the Akt and AMPK pathways. Molecular cellular biology, 31 (3), 430–441.
   PubMed Web of Science ®Google Scholar
• Lu, J., et al., 2013. Pim2 is required for maintaining multiple myeloma cell growth through modulating TSC2 phosphorylation. Blood, 122 (9), 1610–1620.
   PubMed Web of Science ®Google Scholar
• Malinen, M., et al., 2013. Proto-oncogene PIM-1 is a novel estrogen receptor target associating with high grade breast tumors. Molecular and cellular endocrinology, 365 (2), 270–276.
   PubMed Web of Science ®Google Scholar
• Manrique, C., et al., 2012. Loss of estrogen receptor alpha signaling leads to insulin resistance and obesity in young and adult female mice. Cardiorenal medicine, 2 (3), 200–210.
   PubMed Web of Science ®Google Scholar
• Miki, H., et al., 2001. Essential role of insulin receptor substrate 1 (IRS-1) and IRS-2 in adipocyte differentiation. Molecular and cellular biology, 21 (7), 2521–2532.
   PubMed Web of Science ®Google Scholar
• Muraski, J.A., et al., 2007. Pim-1 regulates cardiomyocyte survival downstream of Akt. Nature medicine, 13 (12), 1467–1475.
   PubMed Web of Science ®Google Scholar
• Nogueira-De-Almeida, C.A., and De Mello, E.D., 2018. Different criteria for the definition of insulin resistance and its relation with dyslipidemia in overweight and obese children and adolescents. Pediatric gastroenterology, hepatology and nutrition, 21 (1), 59–67.
   PubMed Web of Science ®Google Scholar
• Obata, T., et al., 2000. Peptide and protein library screening defines optimal substrate motifs for AKT/PKB. Journal of biological chemistry, 275 (46), 36108–36115.
   PubMed Web of Science ®Google Scholar
• Pearce, L.R., Komander, D., and Alessi, D.R., 2010. The nuts and bolts of AGC protein kinases. Nature reviews. Molecular cell biology, 11 (1), 9–22.
   PubMed Web of Science ®Google Scholar
• Peng, C., et al., 2007. Pim kinase substrate identification and specificity. Journal of biochemistry, 141 (3), 353–362.
   PubMed Web of Science ®Google Scholar
• Pfeiffer, S. and Prehn, J.H., 2015. The esoteric roles of Bcl-2 family proteins in glucose homeostasis and cell survival. Cell death and diseases, 6, e1968.
   PubMed Web of Science ®Google Scholar
• Prahallad, A., et al., 2012. Unresponsiveness of colon cancer to BRAF(V600E) inhibition through feedback activation of EGFR. Nature, 483 (7388), 100–103.
   PubMedGoogle Scholar
• Priyanka, A., et al., 2017. Bilobalide abates inflammation, insulin resistance and secretion of angiogenic factors induced by hypoxia in 3T3-L1 adipocytes by controlling NF-kappaB and JNK activation. International immunopharmacology, 42, 209–217.
   PubMed Web of Science ®Google Scholar
• Qu, W., et al., 2018. Anti-TNF-alpha antibody alleviates insulin resistance in rats with sepsis-induced stress hyperglycemia. Journal of endocrinological investigation, 41 (4), 455–463.
   PubMed Web of Science ®Google Scholar
• Rabiee, A., et al., 2018. Distinct signalling properties of insulin receptor substrate (IRS)-1 and IRS-2 in mediating insulin/IGF-1 action. Cell signalling, 47, 1–15.
   PubMed Web of Science ®Google Scholar
• Ramos-Lopez, O., et al., 2018. Endoplasmic reticulum stress epigenetics is related to adiposity, dyslipidemia, and insulin resistance. Adipocyte, 1–6. doi:10.1080/21623945.2018.1447731
   Web of Science ®Google Scholar
• Ramos-Romero, S., et al., 2018. Mechanistically different effects of fat and sugar on insulin resistance, hypertension and gut microbiota in rats. American journal of physiology, endocrinology, and metabolism, 314 (6), 552–563.
   PubMed Web of Science ®Google Scholar
• Ruan, Y., Ma, J.H., and Xie, X.J., 2012. Association of IRS-1 and IRS-2 genes polymorphisms with polycystic ovary syndrome: A meta-analysis. Endocrine journal, 59 (7), 601–609.
   PubMed Web of Science ®Google Scholar
• Salaroli, L.B., et al., 2017. Insulin resistance and associated factors: A cross-sectional study of bank employees. Clinics (Sao Paulo), 72 (4), 224–230.
   PubMed Web of Science ®Google Scholar
• Schatz, J.H., et al., 2011. Targeting cap-dependent translation blocks converging survival signals by AKT and PIM kinases in lymphoma. Journal of experimental medicine, 208 (9), 1799–1807.
   PubMed Web of Science ®Google Scholar
• Seko, Y., et al., 2018. Insulin resistance increases the risk of incident type 2 diabetes mellitus in patients with non-alcoholic fatty liver disease. Hepatology research, 48 (3), E42–E51.
   PubMed Web of Science ®Google Scholar
• Sengupta, S., Peterson, T.R., and Sabatini, D.M., 2010. Regulation of the mTOR complex 1 pathway by nutrients, growth factors, and stress. Molecular cell, 40 (2), 310–322.
   PubMed Web of Science ®Google Scholar
• Shah, O.J. and Hunter, T., 2006. Turnover of the active fraction of IRS1 involves raptor-mTOR- and S6K1-dependent serine phosphorylation in cell culture models of tuberous sclerosis. Molecular and cellular biology, 26 (17), 6425–6434.
   PubMed Web of Science ®Google Scholar
• Shuai, K. and Liu, B., 2003. Regulation of JAK-STAT signalling in the immune system. Nature reviews immunology, 3 (11), 900–911.
   PubMed Web of Science ®Google Scholar
• Sir-Petermann, T., et al., 2004. Insulin secretion in women who have polycystic ovary syndrome and carry the Gly972Arg variant of insulin receptor substrate-1 in response to a high-glycemic or low-glycemic carbohydrate load. Nutrition, 20 (10), 905–910.
   PubMed Web of Science ®Google Scholar
• Son, J., et al., 2013. Glutamine supports pancreatic cancer growth through a KRAS-regulated metabolic pathway. Nature, 496 (7443), 101–105.
   PubMed Web of Science ®Google Scholar
• Song, J.H., et al., 2015. Deletion of Pim kinases elevates the cellular levels of reactive oxygen species and sensitizes to K-Ras-induced cell killing. Oncogene, 34 (28), 3728–3736.
   PubMed Web of Science ®Google Scholar
• Song, J.H., et al., 2016. Insulin receptor substrate 1 is a substrate of the Pim protein kinases. Oncotarget, 7 (15), 20152–20165.
   PubMedGoogle Scholar
• Soucek, L., et al., 2013. Inhibition of Myc family proteins eradicates KRas-driven lung cancer in mice. Genes and development, 27 (5), 504–513.
   PubMed Web of Science ®Google Scholar
• Srivastava, A., et al., 2018. Chronic hyperinsulinemia induced miR-27b is linked to adipocyte insulin resistance by targeting insulin receptor. Journal of molecular medicine, 96 (3–4), 315–331.
   PubMed Web of Science ®Google Scholar
• Sun, X.J. and Liu, F., 2009. Phosphorylation of IRS proteins Yin–Yang regulation of insulin signaling. Vitamins and hormones, 80, 351–387.
   PubMed Web of Science ®Google Scholar
• Tanti, J.F. and Jager, J., 2009. Cellular mechanisms of insulin resistance: Role of stress-regulated serine kinases and insulin receptor substrates (IRS) serine phosphorylation. Current opinion in pharmacology, 9 (6), 753–762.
   PubMed Web of Science ®Google Scholar
• Tremblay, F., et al., 2007. Identification of IRS-1 Ser-1101 as a target of S6K1 in nutrient- and obesity-induced insulin resistance. Proceedings of the national academy of sciences of the United States of America, 104 (35), 14056–14061.
   PubMed Web of Science ®Google Scholar
• Turaihi, A.H., et al., 2018. Insulin receptor substrate 2 controls insulin-mediated vasoreactivity and perivascular adipose tissue function in muscle. Frontiers in physiology, 9, 245.
   PubMed Web of Science ®Google Scholar
• Tursynbay, Y., et al. 2016. Pim-1 kinase as cancer drug target: An update. Biomedical reports, 4 (2), 140–146.
   PubMed Web of Science ®Google Scholar
• Ueki, K., Kondo, T., and Kahn, C.R., 2004. Suppressor of cytokine signaling 1 (SOCS-1) and SOCS-3 cause insulin resistance through inhibition of tyrosine phosphorylation of insulin receptor substrate proteins by discrete mechanisms. Molecular and cellular biology, 24 (12), 5434–5446.
   PubMed Web of Science ®Google Scholar
• Um, S.H., et al., 2004. Absence of S6K1 protects against age- and diet-induced obesity while enhancing insulin sensitivity. Nature, 431 (7005), 200–205.
   PubMed Web of Science ®Google Scholar
• Villuendas, G., et al., 2005. Polymorphisms in the insulin receptor substrate-1 (IRS-1) gene and the insulin receptor substrate-2 (IRS-2) gene influence glucose homeostasis and body mass index in women with polycystic ovary syndrome and non-hyperandrogenic controls. Human reproduction, 20 (11), 3184–3191.
   PubMed Web of Science ®Google Scholar
• Wang, X.J., et al., 2013. Discovery of novel pyrazolo[1,5-a]pyrimidines as potent pan-Pim inhibitors by structure- and property-based drug design. Bioorganic and medicinal chemistry letters, 23 (11), 3149–3153.
   PubMed Web of Science ®Google Scholar
• Ward, C.W. and Lawrence, M.C., 2009. Ligand-induced activation of the insulin receptor: a multi-step process involving structural changes in both the ligand and the receptor. Bioessays, 31 (4), 422–434.
   PubMed Web of Science ®Google Scholar
• Warfel, N.A. and Kraft, A.S., 2015. PIM kinase (and Akt) biology and signaling in tumors. Pharmacology and therapeutics, 151, 41–49.
   PubMed Web of Science ®Google Scholar
• White, M.F., 2003. Insulin signaling in health and disease. Science (New York, NY), 302 (5651), 1710–1711.
   Google Scholar
• Wu, X., et al., 2000. Expression of insulin-receptor substrate-1 and -2 in ovaries from women with insulin resistance and from controls. Fertility and sterility, 74 (3), 564–572.
   PubMed Web of Science ®Google Scholar
• Xin, Y., et al., 2017. C1qTNF-related protein 1 improve insulin resistance by reducing phosphorylation of serine 1101 in insulin receptor substrate 1. Endocrine journal, 64 (8), 787–796.
   PubMed Web of Science ®Google Scholar
• Yin, Y., et al., 2016. mTORC2 promotes type I insulin-like growth factor receptor and insulin receptor activation through the tyrosine kinase activity of mTOR. Cell research, 26 (1), 46–65.
   PubMed Web of Science ®Google Scholar
• Ying, H.Q., et al., 2012. Oncogenic Kras maintains pancreatic tumors through regulation of anabolic glucose metabolism. Cell, 149 (3), 656–670.
   PubMed Web of Science ®Google Scholar
• Yoneyama, Y., et al., 2018a. IRS-1 acts as an endocytic regulator of IGF-I receptor to facilitate sustained IGF signaling. eLife, 7. doi:10.7554/eLife.32893.
   PubMed Web of Science ®Google Scholar
• Yoneyama, Y., et al., 2018b. Serine phosphorylation by mTORC1 promotes IRS-1 degradation through SCFβ-TRCP E3 ubiquitin ligase. iScience, 5, 1–18.
   PubMed Web of Science ®Google Scholar
• Yoneyama, Y., et al., 2013. The AP-1 complex regulates intracellular localization of insulin receptor substrate 1, which is required for insulin-like growth factor I-dependent cell proliferation. Molecular cell biology, 33 (10), 1991–2003.
   PubMed Web of Science ®Google Scholar
• Yoon, M.S., 2017. The role of mammalian target of rapamycin (mTor) in insulin signaling. Nutrients, 9, (11), doi:10.3390/nu9111176.
   Web of Science ®Google Scholar
• Zhang, F., et al., 2009. PIM1 protein kinase regulates PRAS40 phosphorylation and mTOR activity in FDCP1 cells. Cancer biology and therapy, 8 (9), 846–853.
   PubMed Web of Science ®Google Scholar
• Zhang, Z., Wang, J., and Wang, H., 2018. Correlation of blood glucose, serum chemerin and insulin resistance with NAFLD in patients with type 2 diabetes mellitus. Experimental and therapeutic medicine, 15, 2936–2940.
   Google Scholar
• Zhou, X., et al., 2018. The antipsychotics sulpiride induces fatty liver in rats via phosphorylation of insulin receptor substrate-1 at Serine 307-mediated adipose tissue insulin resistance. Toxicology and applied pharmacology, 345, 66–74.
   Google Scholar