Hematopoietically expressed homeobox gene is associated with type 2 diabetes in KK Cg‑Ay/J mice and a Taiwanese Han Chinese population
- Authors:
- Chi‑Cheng Lu
- Yng‑Tay Chen
- Shih‑Yin Chen
- Yuan‑Man Hsu
- Chyi‑Chyang Lin
- Je‑Wei Tsao
- Yu‑Ning Juan
- Jai‑Sing Yang
- Fuu‑Jen Tsai
-
Affiliations: Department of Pharmacy, Buddhist Tzu Chi General Hospital, Hualien 97002, Taiwan, R.O.C., Department of Medical Research, China Medical University Hospital, China Medical University, Taichung 40447, Taiwan, R.O.C., Department of Biological Science and Technology, China Medical University, Taichung 40402, Taiwan, R.O.C., School of Pharmacy, China Medical University, Taichung 40402, Taiwan, R.O.C., Human Genetics Center, Department of Medical Research, China Medical University Hospital, China Medical University, Taichung 40447, Taiwan, R.O.C. - Published online on: May 10, 2018 https://doi.org/10.3892/etm.2018.6152
- Pages: 185-191
-
Copyright: © Lu et al. This is an open access article distributed under the terms of Creative Commons Attribution License.
This article is mentioned in:
Abstract
Hou WH, Li CY, Chen LH, Wang LY, Kuo KN, Shen HN and Chang MF: Prevalence of hand syndromes among patients with diabetes mellitus in Taiwan: A population-based study. J Diabetes. 9:622–627. 2017. View Article : Google Scholar : PubMed/NCBI | |
Chen SY, Hsu YM, Lin YJ, Huang YC, Chen CJ, Lin WD, Liao WL, Chen YT, Lin WY, Liu YH, et al: Current concepts regarding developmental mechanisms in diabetic retinopathy in Taiwan. Biomedicine (Taipei). 6:72016. View Article : Google Scholar : PubMed/NCBI | |
Middleton P, Crowther CA and Simmonds L: Different intensities of glycaemic control for pregnant women with pre-existing diabetes. Cochrane Database Syst Rev: CD008540. 2016. View Article : Google Scholar | |
Adeshara KA, Diwan AG and Tupe RS: Diabetes and complications: Cellular signaling pathways, current understanding and targeted therapies. Curr Drug Targets. 17:1309–1328. 2016. View Article : Google Scholar : PubMed/NCBI | |
Zatalia SR and Sanusi H: The role of antioxidants in the pathophysiology, complications, and management of diabetes mellitus. Acta Med Indones. 45:141–147. 2013.PubMed/NCBI | |
Resl M and Clodi M: Diabetes and cardiovascular complications. Wien Med Wochenschr. 160:3–7. 2010.(In German). View Article : Google Scholar : PubMed/NCBI | |
Hahr AJ and Molitch ME: Diabetes, cardiovascular risk and nephropathy. Cardiol Clin. 28:467–475. 2010. View Article : Google Scholar : PubMed/NCBI | |
World Health Organization, . Global report on diabetes. WHO; Geneva: 2016, http://www.who.int/diabetes/global-report/en/PubMed/NCBI | |
Ministry of Health and Welfare: 2015 statistics of causes of deathMinistry of Health and Welfare. Taiwan, R.O.C.: https://www.mohw.gov.tw/cp-3265-30093-2.htmlLast Updated July 18. 2017 | |
Yang X, Xu Z, Zhang C, Cai Z and Zhang J: Metformin, beyond an insulin sensitizer, targeting heart and pancreatic β cells. Biochim Biophys Acta. 1863:1984–1990. 2017. View Article : Google Scholar : PubMed/NCBI | |
Murillo-Maldonado JM and Riesgo-Escovar JR: Development and diabetes on the fly. Mech Dev. 144:150–155. 2017. View Article : Google Scholar : PubMed/NCBI | |
Boldison J and Wong FS: Immune and pancreatic β cell interactions in type 1 diabetes. Trends Endocrinol Metab. 27:856–867. 2016. View Article : Google Scholar : PubMed/NCBI | |
Kesavadev J: Insulin pump therapy in pregnancy. J Pak Med Assoc. 66 9 Suppl 1:S39–S44. 2016.PubMed/NCBI | |
Bolinder J, Antuna R, Geelhoed-Duijvestijn P, Kröger J and Weitgasser R: Novel glucose-sensing technology and hypoglycaemia in type 1 diabetes: A multicentre, non-masked, randomised controlled trial. Lancet. 388:2254–2263. 2016. View Article : Google Scholar : PubMed/NCBI | |
Zou D, Ye Y, Zou N and Yu J: Analysis of risk factors and their interactions in type 2 diabetes mellitus: A cross-sectional survey in Guilin, China. J Diabetes Investig. 8:188–194. 2017. View Article : Google Scholar : PubMed/NCBI | |
Hotta-Iwamura C and Tarbell KV: Type 1 diabetes genetic susceptibility and dendritic cell function: Potential targets for treatment. J Leukoc Biol. 100:65–80. 2016. View Article : Google Scholar : PubMed/NCBI | |
Cheng CA, Chien WC, Hsu CY, Lin HC and Chiu HW: Risk analysis of carotid stent from a population-based database in Taiwan. Medicine (Baltimore). 95:e47472016. View Article : Google Scholar : PubMed/NCBI | |
Sakai S, Tanimoto K, Imbe A, Inaba Y, Shishikura K, Tanimoto Y, Ushiroyama T, Terasaki J and Hanafusa T: Decreased β-cell function is associated with reduced skeletal muscle mass in japanese subjects without diabetes. PLoS One. 11:e01626032016. View Article : Google Scholar : PubMed/NCBI | |
Rezai S, LoBue S and Henderson CE: Diabetes prevention: Reproductive age women affected by insulin resistance. Womens Health (Lond). 12:427–432. 2016. View Article : Google Scholar : PubMed/NCBI | |
Arias-Loste MT, Ranchal I, Romero-Gómez M and Crespo J: Irisin, a link among fatty liver disease, physical inactivity and insulin resistance. Int J Mol Sci. 15:23163–23178. 2014. View Article : Google Scholar : PubMed/NCBI | |
Skliros NP, Vlachopoulos C and Tousoulis D: Treatment of diabetes: Crossing to the other side. Hellenic J Cardiol. 57:304–310. 2016. View Article : Google Scholar : PubMed/NCBI | |
Marín-Peñalver JJ, Martín-Timón I, Sevillano-Collantes C and Del Cañizo-Gómez FJ: Update on the treatment of type 2 diabetes mellitus. World J Diabetes. 7:354–395. 2016. View Article : Google Scholar : PubMed/NCBI | |
Nenquin M and Henquin JC: Sulphonylurea receptor-1, sulphonylureas and amplification of insulin secretion by Epac activation in β cells. Diabetes Obes Metab. 18:698–701. 2016. View Article : Google Scholar : PubMed/NCBI | |
Abdelmoneim AS, Welsh RC, Eurich DT and Simpson SH: Sulfonylurea use is associated with larger infarct size in patients with diabetes and ST-elevation myocardial infarction. Int J Cardiol. 202:126–130. 2016. View Article : Google Scholar : PubMed/NCBI | |
Winkler G: Metformin-new data for an ‘old’, but efficient, safe and reliable antidiabetic drug. Orv Hetil. 157:882–891. 2016. View Article : Google Scholar : PubMed/NCBI | |
De Souza A, Khawaja KI, Masud F and Saif MW: Metformin and pancreatic cancer: Is there a role? Cancer Chemother Pharmacol. 77:235–242. 2016. View Article : Google Scholar : PubMed/NCBI | |
Zhang L, Chen Q, Li L, Kwong JS, Jia P, Zhao P, Wang W, Zhou X, Zhang M and Sun X: Alpha-glucosidase inhibitors and hepatotoxicity in type 2 diabetes: A systematic review and meta-analysis. Sci Rep. 6:326492016. View Article : Google Scholar : PubMed/NCBI | |
Smith JD, Mills E and Carlisle SE: Treatment of pediatric type 2 diabetes. Ann Pharmacother. 50:768–777. 2016. View Article : Google Scholar : PubMed/NCBI | |
Ahuja V and Chou CH: Novel therapeutics for diabetes: Uptake, usage trends, and comparative effectiveness. Curr Diab Rep. 16:472016. View Article : Google Scholar : PubMed/NCBI | |
Salazar JJ, Ennis WJ and Koh TJ: Diabetes medications: Impact on inflammation and wound healing. J Diabetes Complications. 30:746–752. 2016. View Article : Google Scholar : PubMed/NCBI | |
Bae EJ: DPP-4 inhibitors in diabetic complications: Role of DPP-4 beyond glucose control. Arch Pharm Res. 39:1114–1128. 2016. View Article : Google Scholar : PubMed/NCBI | |
Bonora E and Cigolini M: DPP-4 inhibitors and cardiovascular disease in type 2 diabetes mellitus. Expectations, observations and perspectives. Nutr Metab Cardiovasc Dis. 26:273–284. 2016. View Article : Google Scholar : PubMed/NCBI | |
King AJ: The use of animal models in diabetes research. Br J Pharmacol. 166:877–894. 2012. View Article : Google Scholar : PubMed/NCBI | |
O'Brien SP, Smith M, Ling H, Phillips L, Weber W, Lydon J, Maloney C, Ledbetter S, Arbeeny C and Wawersik S: Glomerulopathy in the KK. Cg-A(y)/J mouse reflects the pathology of diabetic nephropathy. J Diabetes Res. 2013:4989252013. View Article : Google Scholar : PubMed/NCBI | |
Ikeda H: KK mouse. Diabetes Res Clin Pract. 24 Suppl:S313–S316. 1994. View Article : Google Scholar : PubMed/NCBI | |
Iwatsuka H, Shino A and Suzuoki Z: General survey of diabetic features of yellow KK mice. Endocrinol Jpn. 17:23–35. 1970. View Article : Google Scholar : PubMed/NCBI | |
Wang Y, Qiao W, Zhao X and Tao M: Quantitative assessment of the influence of hematopoietically expressed homeobox variant (rs1111875) on type 2 diabetes risk. Mol Genet Metab. 102:194–199. 2011. View Article : Google Scholar : PubMed/NCBI | |
van Vliet-Ostaptchouk JV, Onland-Moret NC, van Haeften TW, Franke L, Elbers CC, Shiri-Sverdlov R, van der Schouw YT, Hofker MH and Wijmenga C: HHEX gene polymorphisms are associated with type 2 diabetes in the Dutch Breda cohort. Eur J Hum Genet. 16:652–656. 2008. View Article : Google Scholar : PubMed/NCBI | |
Pechlivanis S, Scherag A, Mühleisen TW, Möhlenkamp S, Horsthemke B, Boes T, Bröcker-Preuss M, Mann K, Erbel R, Jöckel KH, et al: Coronary artery calcification and its relationship to validated genetic variants for diabetes mellitus assessed in the Heinz Nixdorf recall cohort. Arterioscler Thromb Vasc Biol. 30:1867–1872. 2010. View Article : Google Scholar : PubMed/NCBI | |
Zhao J, Deliard S, Aziz AR and Grant SF: Expression analyses of the genes harbored by the type 2 diabetes and pediatric BMI associated locus on 10q23. BMC Med Genet. 13:892012. View Article : Google Scholar : PubMed/NCBI | |
Feuk L, McCarthy S, Andersson B, Prince JA and Brookes AJ: Mutation screening of a haplotype block around the insulin degrading enzyme gene and association with Alzheimer's disease. Am J Med Genet B Neuropsychiatr Genet. 136B:69–71. 2005. View Article : Google Scholar : PubMed/NCBI | |
Bort R, Signore M, Tremblay K, Barbera Martinez JP and Zaret KS: Hex homeobox gene controls the transition of the endoderm to a pseudostratified, cell emergent epithelium for liver bud development. Dev Biol. 290:44–56. 2006. View Article : Google Scholar : PubMed/NCBI | |
Hindy G, Mollet IG, Rukh G, Ericson U and Orho-Melander M: Several type 2 diabetes-associated variants in genes annotated to WNT signaling interact with dietary fiber in relation to incidence of type 2 diabetes. Genes Nutr. 11:62016. View Article : Google Scholar : PubMed/NCBI | |
Kommoju UJ, Samy SK, Maruda J, Irgam K, Kotla JP, Velaga L and Reddy BM: Association of CDKAL1, CDKN2A/B & HHEX gene polymorphisms with type 2 diabetes mellitus in the population of Hyderabad, India. Indian J Med Res. 143:455–463. 2016. View Article : Google Scholar : PubMed/NCBI | |
Qian Y, Lu F, Dong M, Lin Y, Li H, Chen J, Shen C, Jin G, Hu Z and Shen H: Genetic variants of IDE-KIF11-HHEX at 10q23.33 associated with type 2 diabetes risk: A fine-mapping study in Chinese population. PLoS One. 7:e350602012. View Article : Google Scholar : PubMed/NCBI | |
Chen YT, Liao JW, Tsai YC and Tsai FJ: Inhibition of DNA methyltransferase 1 increases nuclear receptor subfamily 4 group A member 1 expression and decreases blood glucose in type 2 diabetes. Oncotarget. 7:39162–39170. 2016.PubMed/NCBI | |
Steneberg P, Bernardo L, Edfalk S, Lundberg L, Backlund F, Ostenson CG and Edlund H: The type 2 diabetes-associated gene ide is required for insulin secretion and suppression of α-synuclein levels in β-cells. Diabetes. 62:2004–2014. 2013. View Article : Google Scholar : PubMed/NCBI | |
Asrafuzzaman M, Cao Y, Afroz R, Kamato D, Gray S and Little PJ: Animal models for assessing the impact of natural products on the aetiology and metabolic pathophysiology of Type 2 diabetes. Biomed Pharmacother. 89:1242–1251. 2017. View Article : Google Scholar : PubMed/NCBI | |
Kaul N and Ali S: Genes, genetics, and environment in Type 2 diabetes: Implication in personalized medicine. DNA Cell Biol. 35:1–12. 2016. View Article : Google Scholar : PubMed/NCBI | |
Cornelis MC, Zaitlen N, Hu FB, Kraft P and Price AL: Genetic and environmental components of family history in type 2 diabetes. Hum Genet. 134:259–267. 2015. View Article : Google Scholar : PubMed/NCBI | |
Flannick J and Florez JC: Type 2 diabetes: Genetic data sharing to advance complex disease research. Nat Rev Genet. 17:535–549. 2016. View Article : Google Scholar : PubMed/NCBI | |
Fuchsberger C, Flannick J, Teslovich TM, Mahajan A, Agarwala V, Gaulton KJ, Ma C, Fontanillas P, Moutsianas L, McCarthy DJ, et al: The genetic architecture of type 2 diabetes. Nature. 536:41–47. 2016. View Article : Google Scholar : PubMed/NCBI | |
Kong X, Zhang X, Xing X, Zhang B, Hong J and Yang W: The association of Type 2 diabetes loci identified in genome-wide association studies with metabolic syndrome and its components in a chinese population with Type 2 diabetes. PLoS One. 10:e01436072015. View Article : Google Scholar : PubMed/NCBI | |
Ma RC, So WY, Tam CH, Luk AO, Ho JS, Wang Y, Lam VK, Lee HM, Kong AP, Tong PC, et al: Genetic variants for type 2 diabetes and new-onset cancer in Chinese with type 2 diabetes. Diabetes Res Clin Pract. 103:328–337. 2014. View Article : Google Scholar : PubMed/NCBI | |
Klimentidis YC, Lemas DJ, Wiener HH, O'Brien DM, Havel PJ, Stanhope KL, Hopkins SE, Tiwari HK and Boyer BB: CDKAL1 and HHEX are associated with type 2 diabetes-related traits among Yup'ik people. J Diabetes. 6:251–259. 2014. View Article : Google Scholar : PubMed/NCBI | |
Sanghera DK, Ortega L, Han S, Singh J, Ralhan SK, Wander GS, Mehra NK, Mulvihill JJ, Ferrell RE, Nath SK and Kamboh MI: Impact of nine common type 2 diabetes risk polymorphisms in Asian Indian Sikhs: PPARG2 (Pro12Ala), IGF2BP2, TCF7L2 and FTO variants confer a significant risk. BMC Med Genet. 9:592008. View Article : Google Scholar : PubMed/NCBI | |
Scott LJ, Mohlke KL, Bonnycastle LL, Willer CJ, Li Y, Duren WL, Erdos MR, Stringham HM, Chines PS, Jackson AU, et al: A genome-wide association study of type 2 diabetes in Finns detects multiple susceptibility variants. Science. 316:1341–1345. 2007. View Article : Google Scholar : PubMed/NCBI | |
Diabetes Genetics Initiative of Broad Institute of Harvard and MIT, Lund University, and Novartis Institutes of BioMedical Research, . Saxena R, Voight BF, Lyssenko V, Burtt NP, de Bakker PI, Chen H, Roix JJ, Kathiresan S, Hirschhorn JN, et al: Genome-wide association analysis identifies loci for type 2 diabetes and triglyceride levels. Science. 316:1331–1336. 2007. View Article : Google Scholar : PubMed/NCBI | |
Malhotra A, Coon H, Feitosa MF, Li WD, North KE, Price RA, Bouchard C, Hunt SC and Wolford JK: American Diabetes Association GENNID Study Group: Meta-analysis of genome-wide linkage studies for quantitative lipid traits in African Americans. Hum Mol Genet. 14:3955–3962. 2005. View Article : Google Scholar : PubMed/NCBI | |
Kong X, Xing X, Hong J, Zhang X and Yang W: Genetic variants associated with lean and obese type 2 diabetes in a Han Chinese population: A case-control study. Medicine (Baltimore). 95:e38412016. View Article : Google Scholar : PubMed/NCBI | |
Kong X, Xing X, Hong J, Zhang X and Yang W: Association of a type 2 diabetes genetic risk score with insulin secretion modulated by insulin sensitivity among Chinese Hans. Clin Genet. 91:832–842. 2017. View Article : Google Scholar : PubMed/NCBI | |
Sladek R, Rocheleau G, Rung J, Dina C, Shen L, Serre D, Boutin P, Vincent D, Belisle A, Hadjadj S, et al: A genome-wide association study identifies novel risk loci for type 2 diabetes. Nature. 445:881–885. 2007. View Article : Google Scholar : PubMed/NCBI | |
Arterbery AS and Bogue CW: Hhex is necessary for the hepatic differentiation of mouse ES cells and Acts via Vegf signaling. PLoS One. 11:e01468062016. View Article : Google Scholar : PubMed/NCBI | |
Watanabe H, Takayama K, Inamura M, Tachibana M, Mimura N, Katayama K, Tashiro K, Nagamoto Y, Sakurai F, Kawabata K, et al: HHEX promotes hepatic-lineage specification through the negative regulation of eomesodermin. PLoS One. 9:e907912014. View Article : Google Scholar : PubMed/NCBI | |
Hunter MP, Wilson CM, Jiang X, Cong R, Vasavada H, Kaestner KH and Bogue CW: The homeobox gene Hhex is essential for proper hepatoblast differentiation and bile duct morphogenesis. Dev Biol. 308:355–367. 2007. View Article : Google Scholar : PubMed/NCBI | |
Deng XP, Zhao LX, Wang BB, Wang J, Cheng LF, Cheng Z, Suo PS, Li H and Ma X: The HHEX gene is not related to congenital heart disease in 296 Chinese patients. World J Pediatr. 9:278–280. 2013. View Article : Google Scholar : PubMed/NCBI | |
Foley AC and Mercola M: Heart induction by Wnt antagonists depends on the homeodomain transcription factor Hex. Genes Dev. 19:387–396. 2005. View Article : Google Scholar : PubMed/NCBI | |
Liu S, Chai J, Zheng G, Li H, Lu D and Ge Y: Screening of HHEX mutations in chinese children with thyroid dysgenesis. J Clin Res Pediatr Endocrinol. 8:21–25. 2016. View Article : Google Scholar : PubMed/NCBI | |
McLin VA, Rankin SA and Zorn AM: Repression of Wnt/beta-catenin signaling in the anterior endoderm is essential for liver and pancreas development. Development. 134:2207–2217. 2007. View Article : Google Scholar : PubMed/NCBI | |
Zhang J, McKenna LB, Bogue CW and Kaestner KH: The diabetes gene Hhex maintains δ-cell differentiation and islet function. Genes Dev. 28:829–834. 2014. View Article : Google Scholar : PubMed/NCBI | |
Rong R, Hanson RL, Ortiz D, Wiedrich C, Kobes S, Knowler WC, Bogardus C and Baier LJ: Association analysis of variation in/near FTO, CDKAL1, SLC30A8, HHEX, EXT2, IGF2BP2, LOC387761, and CDKN2B with type 2 diabetes and related quantitative traits in Pima Indians. Diabetes. 58:478–488. 2009. View Article : Google Scholar : PubMed/NCBI | |
Moore AF, Jablonski KA, McAteer JB, Saxena R, Pollin TI, Franks PW, Hanson RL, Shuldiner AR, Knowler WC, Altshuler D, et al: Extension of type 2 diabetes genome-wide association scan results in the diabetes prevention program. Diabetes. 57:2503–2510. 2008. View Article : Google Scholar : PubMed/NCBI | |
Chiasson JL: Early insulin use in type 2 diabetes: What are the cons? Diabetes Care. 32 Suppl 2:S270–S274. 2009. View Article : Google Scholar : PubMed/NCBI | |
Fonseca VA: Defining and characterizing the progression of type 2 diabetes. Diabetes Care. 32 Suppl 2:S151–S156. 2009. View Article : Google Scholar : PubMed/NCBI | |
Vigneri R, Goldfine ID and Frittitta L: Insulin, insulin receptors, and cancer. J Endocrinol Invest. 39:1365–1376. 2016. View Article : Google Scholar : PubMed/NCBI | |
de Miguel-Díez J, Muñoz-Rivas N, Jiménez-García R, Hernández-Barrera V, Carrasco-Garrido P, Monreal M, Jiménez D, Guijarro R and de Andrés López A: Type 2 diabetes is associated with a higher incidence of hospitalization for pulmonary embolism in Spain: Analysis of hospital discharge data during 2004–2013. Respirology. 21:1277–1284. 2016. View Article : Google Scholar : PubMed/NCBI | |
Yu F, Guo Y, Wang H, Feng J, Jin Z, Chen Q, Liu Y and He J: Type 2 diabetes mellitus and risk of colorectal adenoma: A meta-analysis of observational studies. BMC Cancer. 16:6422016. View Article : Google Scholar : PubMed/NCBI | |
Sun R, Liu JP, Gao C, Xiong YY, Li M, Wang YP, Su YW, Lin M, Jiang AL, Xiong LF, et al: Two variants on T2DM susceptible gene HHEX are associated with CRC risk in a Chinese population. Oncotarget. 7:29770–29779. 2016.PubMed/NCBI |