MERTK rs4374383 variant predicts incident nonalcoholic fatty liver disease and diabetes: Role of mononuclear cell activation and adipokine response to dietary fat

Human Molecular Genetics

Volumn 26, Issue 9, 2017, Pages 1747-1758

  Musso, Giovanni ^a   Cassader, Maurizio ^b   Michieli, Franco De ^b   Paschetta, Elena ^a   Pinach, Silvia ^b   Saba, Francesca ^b   Bongiovanni, Daria ^a   Framarin, Luciana ^a   Berrutti, Mara ^a   Leone, Nicola ^a   Corvisieri, Stefania ^c   Parente, Renato ^a   Molinaro, Federica ^a   Sircana, Antonio ^d   Bo, Simona ^b   Gambino, Roberto ^b  

^a Gradenigo Hospital   (Italy)

^b UNIVERSITY OF TURIN   (Italy)

^c UNIVERSITY OF TURIN   (Italy)

^d Department of Internal Medicine   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

ADIPOCYTOKINE; GLUCOSE; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INSULIN; MONOCYTE CHEMOTACTIC PROTEIN 1; MYELOID EPITHELIAL REPRODUCTIVE TYROSINE KINASE; PROTEIN TYROSINE KINASE; UNCLASSIFIED DRUG; FAT INTAKE; LIPOPROTEIN; MERTK PROTEIN, HUMAN; ONCOPROTEIN;

ADULT; ALLELE; ARTICLE; CONTROLLED STUDY; CROSS-SECTIONAL STUDY; DIABETES MELLITUS; DISEASE SEVERITY; FAT INTAKE; FEMALE; FOLLOW UP; GENE; GENETIC POLYMORPHISM; GENETIC VARIABILITY; GLUCOSE HOMEOSTASIS; GLUCOSE METABOLISM; HETEROZYGOTE; HUMAN; HUMAN TISSUE; INCIDENCE; INDIRECT CALORIMETRY; INSULIN SENSITIVITY; LEUKOCYTE ACTIVATION; MAJOR CLINICAL STUDY; MALE; METABOLIC SYNDROME X; MONONUCLEAR CELL; MYELOID EPITHELIAL REPRODUCTIVE TYROSINE KINASE GENE; NONALCOHOLIC FATTY LIVER; ORAL GLUCOSE TOLERANCE TEST; OXIDATION; POPULATION BASED CASE CONTROL STUDY; PREDICTION; PRIORITY JOURNAL; RANDOMIZED CONTROLLED TRIAL; COHORT ANALYSIS; GENETIC PREDISPOSITION; GENETIC VARIATION; GENETICS; INSULIN RESISTANCE; LIPID METABOLISM; LIVER CIRRHOSIS; METABOLISM; MIDDLE AGED; SINGLE NUCLEOTIDE POLYMORPHISM;

ADIPOKINES; COHORT STUDIES; CROSS-SECTIONAL STUDIES; DIABETES MELLITUS; DIETARY FATS; FEMALE; GENETIC PREDISPOSITION TO DISEASE; GENETIC VARIATION; GLUCOSE; HUMANS; INSULIN RESISTANCE; LEUKOCYTES, MONONUCLEAR; LIPID METABOLISM; LIPOPROTEINS; LIVER CIRRHOSIS; MALE; MIDDLE AGED; NON-ALCOHOLIC FATTY LIVER DISEASE; POLYMORPHISM, SINGLE NUCLEOTIDE; PROTO-ONCOGENE PROTEINS; RECEPTOR PROTEIN-TYROSINE KINASES;

EID: 85019169928     PISSN: 09646906     EISSN: 14602083     Source Type: Journal    
DOI: 10.1093/hmg/ddw400     Document Type: Article

References (41)

1. Musso, G., Cassader, M., Gambino, R. and Pagano, G.F. (2011) Meta-analysis: Natural history of NAFLD and diagnostic accuracy of non-invasive tests for liver disease severity. Ann. Med, 43, 617-649.
2. Sung, K.C., Kim, B.S. and Cho, Y.K. (2012) Predicting incident fatty liver using simple cardio-metabolic risk factors at baseline. BMC Gastroenterol, 12, 84.
3. Schwab, U., Lauritzen, L. and Tholstrup, T. (2014) Effect of the amount and type of dietary fat on cardiometabolic risk factors and risk of developing type 2 diabetes, cardiovascular diseases, and cancer:a systematic review. Food Nutr. Res., 58.
4. Nseir, W., Hellou, E. and Assy, N. (2014) Role of diet and lifestyle changes in nonalcoholic fatty liver disease. World J. Gastroenterol., 20, 9338-9344.
5. Wood, K.L., Miller, M.H. and Dillon, J.F. (2015) Systematic review of genetic association studies involving histologically confirmed non-alcoholic fatty liver disease. BMJ Open Gastroenterol., 2, e000019-e000017.
6. Patin, E., Kutalik, Z., Guergnon, J., Bibert, S., Nalpas, B. and Jouanguy, E. (2012) Genome-wide association study identifies variants associated with progression of liver fibrosis fromHCV infection. Gastroenterology, 143, 1244-1252.
7. Petta, S., Valenti, L., Marra, F., Grimaudo, S., Tripodo, C., Bugianesi, E., Cammá, C., Cappon, A., Di Marco, V., Di Maira, G., et al. (2016) MERTK rs4374383 polymorphism affects the severity of fibrosis in nonalcoholic fatty liver disease. J. Hepatol., 64, 682-690.
8. van der Meer, J.H., van der Poll, T. and van 't Veer, C. (2014) TAM receptors, Gas6, and protein S: roles in inflammation and hemostasis. Blood, 123, 2460-2469.
9. Fourcot, A., Couchie, D. and Chobert, M.N. (2011) Gas6 deficiency prevents liver inflammation, steatohepatitis, and fibrosis in mice. Am. J. Physiol. Gastrointest. Liver Physiol., 300, G1043-G1053.
10. Maquoi, E., Vörös, G. and Carmeliet, P. (2005) Role of Gas-6 in adipogenesis and nutritionally induced adipose tissue development in mice. Arterioscler. Thromb. Vasc. Biol., 25, 1002-1007.
11. Wu, K.S., Hung, Y.J. and Lee, C.H. (2015) The Involvement of GAS6 Signaling in the Development of Obesity and Associated Inflammation. Int. J. Endocrinol., 2015, 202513.
12. Hsiao, F.C., Lin, Y.F. and Hsieh, P.S. (2013) Circulating growth arrest-specific 6 protein is associated with adiposity, systemic inflammation, and insulin resistance among overweight and obese adolescents. J. Clin. Endocrinol. Metab., 98, E267-E274.
13. Graham, D.K., Dawson, T.L. and Mullaney, D.L. (1994) Cloning and mRNA expression analysis of a novel human protooncogene, c-mer. Cell Growth Differ., 5, 647-657.
14. Dupuis, J., Langenberg, C. and Prokopenko, I. (2010) New genetic loci implicated in fasting glucose homeostasis and their impact on type 2 diabetes risk. Nat. Genet., 42, 105-116.
15. International HapMap Project. http://hapmap.ncbi.nlm.nih. gov/index.html.en; date last accessed August 15, 2016.
16. Gambino, R., Bo, S. and Gentile, L. (2010) Transcription Factor 7-Like 2 (TCF7L2) Polymorphism and Hyperglycemia in an Adult Italian Population-Based Cohort. Diabetes Care, 33, 1233-1235.
17. Chalasani, N., Younossi, Z. and Lavine, J.E. (2012) The diagnosis and management of NAFLD: practice guidelines by the AASLD, ACG and the AGA. Hepatology, 55, 2005-2023.
18. Musso, G., Gambino, R., De Michieli, F., Biroli, G., Premoli, A. and Pagano, G. (2007) Nitrosative stress predicts the presence and severity of nonalcoholic fatty liver at different stages of the development of insulin resistance and metabolic syndrome: possible role of vitamin A intake. Am. J. Clin. Nutr, 86, 661-671.
19. Sacerdote, C., Fiorini, L. and Dalmasso, M. (2000) Alimentazione e rischi di cancro. Indagine su un campione di 10054 volontari residenti nell'area torinese. Torino: AGAT
20. Carnovale, E. and Marletta, P. Food Composition Table. Istituto Nazionale della Nutrizione. Milano: EDRA 1997.
21. Taylor, H.L., Jacobs, D.R., Jr. and Schucker, B. (1978) Questionnaire for the assessment of leisure time physical activities. J. Chronic Dis., 31, 741-755.
22. Abdelmegeed, M.A. and Song, B.J. (2014) Functional roles of protein nitration in acute and chronic liver diseases. Oxid. Medd. Cell. Longev, 2014, 149627.
23. Musso, G., Cassader, M. and De Michieli, F. (2012) Nonalcoholic steatohepatitis versus steatosis: adipose tissue insulin resistance and dysfunctional response to fat ingestion predict liver injury and altered glucose and lipoprotein metabolism. Hepatology, 56, 933-942.
24. Nunez, C., Gallagher, D. and Visser, M. (1997) Bioimpedance analysis: evaluation of leg-to-leg system based on pressare contact footpad electrodes. Med. Sci. Sports Exerc., 29, 524-531.
25. Frayn, K.N. (1983) Calculation of substrate oxidation rates in vivo from gaseous exchange. J. Appl. Physiol., 55, 628-634.
26. Cobelli, C., Toffolo, G.M. and Dalla Man, C. (2007) Assessment of beta-cell function in humans, simultaneously with insulin sensitivity and hepatic extraction, from intravenous and oral glucose tests. Am. J. Physiol. Endocrinol. Metab., 293, E1-E15.
27. Pirillo, A., Norata, G.D. and Catapano, A.L. (2014) Postprandial lipemia as a cardiometabolic risk factor. Curr. Med. Res. Opin., 30, 1489-1503.
28. Musso, G., Cassader, M. and Gambino, R. (2016) Non-alcoholic steatohepatitis: emerging molecular targets and therapeutic strategies. Nat. Rev. Drug Discov., 15, 249-274.
29. Benjamini, Y. and Hochberg, Y. (1995) Controlling the False Discovery Rate: a practical and powerful approach to multiple testing. J. Royal Stat. Soc. Ser. B, 57, 289-300.
30. Negre-Salvayre, A., Vieira, O. and Escargueil-Blanc, I. (2003) Oxidized LDL and 4-hydroxynonenal modulate tyrosine kinase receptor activity. Mol. Aps. Med., 24, 251-261.
31. Georgescu, M.M., Kirsch, K.H. and Shishido, T. (1999) Biological effects of c-Mer receptor tyrosine kinase in hematopoietic cells depend on the Grb2 binding site in the receptor and activation of NF-kappaB. Mol. Cell. Biol., 19, 1171-1181.
32. Ghanim, H., Abuaysheh, S. and Sia, C.L. (2009) Increase in plasma endotoxin concentrations and the expression of Toll-like receptors and suppressor of cytokine signaling-3 in mononuclear cells following a high-fat high-carbohydrate meal: implications for insulin resistance. Diabetes Care, 32, 2281-2287.
33. Arsov, T., Carter, C.Z. and Nolan, C.J. (2006) Adaptive failure to high-fat diet characterizes steatohepatitis in Alms1 mutant mice. Biochem. Biophys. Res. Comm., 342, 1152-1159.
34. Dordevic, A.L., Pendergast, F.J. and Morgan, H. (2015) Postprandial Responses to Lipid and Carbohydrate Ingestion in Repeated Subcutaneous Adipose Tissue Biopsies in Healthy Adults. Nutrients, 7, 5347-5361.
35. Liang, W., Lindeman, J.H., Menke, A.L., Koonen, D.P., Morrison, M., Havekes, L.M., van den Hoek, A.M. and Kleemann, R. (2014) Metabolically induced liver inflammation leads to NASH and differs from LPS-or IL-1b-induced chronic inflammation. Lab. Invest., 94, 491-502.
36. Musso G., Cassader M., Paschetta E., and Gambino R. (2017) Thiazolidinediones and Advanced Liver Fibrosis in Nonalcoholic Steatohepatitis: A Meta-analysis. JAMA Intern. Med., doi: 10.1001/jamainternmed.2016.9607.
37. Lee-Sherick, A.B., Zhang, W., Menachof, K.K., Hill, A.A., Rinella, S., Kirkpatrick, G., Page, L.S., Stashko, M.A., Jordan, C.T., Wei, Q., et al. (2015) Efficacy of a Mer and Flt3 tyrosine kinase small molecule inhibitor, UNC1666, in acute myeloid leukemia. Oncotarget, 6, 6722-6736.
38. Musso, G., Cassader, M., Cohney, S., De Michieli, F., Pinach, S., Saba, F. and Gambino, R. (2016) Fatty Liver and Chronic Kidney Disease: Novel Mechanistic Insights and Therapeutic Opportunities. Diabetes Care, 39, 1830-1845.
39. Nobili, V., Cutrera, R., Liccardo, D., Pavone, M., Devito, R., Giorgio, V., Verrillo, E., Baviera, G. and Musso, G. (2014) Obstructive sleep apnea syndrome affects liver histology and inflammatory cell activation in pediatric nonalcoholic fatty liver disease, regardless of obesity/insulin resistance. Am. J. Respir. Crit. Care Med., 189, 66-76.
40. Nobili, V., Alisi, A., Cutrera, R., Carpino, G., De Stefanis, C., D'Oria, V., De Vito, R., Cucchiara, S., Gaudio, E. and Musso, G. (2015) Altered gut-liver axis and hepatic adiponectin expression in OSAS: novel mediators of liver injury in paediatric non-alcoholic fatty liver. Thorax, 70, 769-781.
41. Musso, G., Olivetti, C., Cassader, M. and Gambino, R. (2012) Obstructive sleep apnea-hypopnea syndrome and nonalcoholic fatty liver disease: emerging evidence and mechanisms. Semin. Liver Dis., 32, 49-64.