The PNPLA3 I148M variant and chronic liver disease: When a genetic mutation meets nutrients

Food Research International

Volumn 63, Issue , 2014, Pages 239-243

  Maglio, Cristina ^a   Pirazzi, Carlo ^a   Pujia, Arturo ^b   Valenti, Luca ^c   Romeo, Stefano ^a,b  

^a UNIVERSITY OF GOTHENBURG   (Sweden)

^b UNIVERSITY MAGNA GRAECIA OF CATANZARO   (Italy)

^c UNIVERSITY OF MILAN   (Italy)

Author keywords

Adiponutrin; Liver steatosis; Nutrigenetics; Obesity; PNPLA3 rs738409

Indexed keywords

AMINO ACIDS; NUTRITION;

ADIPONUTRIN; LIVER STEATOSIS; NUTRIGENETICS; OBESITY; PNPLA3 RS738409;

NUTRIENTS;

EID: 84905017798     PISSN: 09639969     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.foodres.2014.01.055     Document Type: Article

References (62)

1. Acheson K.J., Flatt J.P., Jéquier E. Glycogen synthesis versus lipogenesis after a 500 gram carbohydrate meal in man. Metabolism 1982, 31(12):1234-1240.
2. Adams L.A., Lymp J.F., St Sauver J., Sanderson S.O., Lindor K.D., Feldstein A., et al. The natural history of nonalcoholic fatty liver disease: A population-based cohort study. Gastroenterology 2005, 129(1):113-121.
3. Amacher D.E. Serum transaminase elevations as indicators of hepatic injury following the administration of drugs. Regulatory Toxicology and Pharmacology 1998, 27(2):119-130.
4. Anstee Q.M., Targher G., Day C.P. Progression of NAFLD to diabetes mellitus, cardiovascular disease or cirrhosis. Nature Reviews Gastroenterology & Hepatology 2013, 10(6):330-344.
5. Basantani M.K., Sitnick M.T., Cai L., Brenner D.S., Gardner N.P., Li J.Z., et al. Pnpla3/Adiponutrin deficiency in mice does not contribute to fatty liver disease or metabolic syndrome. Journal of Lipid Research 2011, 52(2):318-329.
6. Becker U., Deis A., Sorensen T.I.A., Gronbaek M., BorchJohnsen K., Muller C.F., et al. Prediction of risk of liver disease by alcohol intake, sex, and age: A prospective population study. Hepatology 1996, 23(5):1025-1029.
7. Bedogni G., Miglioli L., Masutti F., Tiribelli C., Marchesini G., Bellentani S. Prevalence of and risk factors for nonalcoholic fatty liver disease: The Dionysos nutrition and liver study. Hepatology 2005, 42(1):44-52.
8. Bellentani S., Saccoccio G., Costa G., Tiribelli C., Manenti F., Sodde M., et al. Drinking habits as cofactors of risk for alcohol induced liver damage. The Dionysos Study Group. Gut 1997, 41(6):845-850.
9. Berentzen T.L., Gamborg M., Holst C., Sørensen T.I., Baker J.L. Body mass index in childhood and adult risk of primary liver cancer. Journal of Hepatology 2014, 60(2):325-330.
10. Browning J.D., Szczepaniak L.S., Dobbins R., Nuremberg P., Horton J.D., Cohen J.C., et al. Prevalence of hepatic steatosis in an urban population in the United States: Impact of ethnicity. Hepatology 2004, 40(6):1387-1395.
11. Burza M.A., Molinaro A., Attilia M.L., Rotondo C., Attilia F., Ceccanti M., et al. PNPLA3 I148M (rs738409) genetic variant and age at onset of at-risk alcohol consumption are independent risk factors for alcoholic cirrhosis. Liver International 2013.
12. Burza M.A., Pirazzi C., Maglio C., Sjöholm K., Mancina R.M., Svensson P.A., et al. PNPLA3 I148M (rs738409) genetic variant is associated with hepatocellular carcinoma in obese individuals. Digestive and Liver Disease 2012, 44(12):1037-1041.
13. Chung J., Chen C., Paw B.H. Heme metabolism and erythropoiesis. Current Opinion in Hematology 2012, 19(3):156-162.
14. Corradini S.G., Burza M.A., Molinaro A., Romeo S. Patatin-like phospholipase domain containing 3 sequence variant and hepatocellular carcinoma. Hepatology 2011, 53(5):1776. (author reply 1777).
15. Daly A.K., Ballestri S., Carulli L., Loria P., Day C.P. Genetic determinants of susceptibility and severity in nonalcoholic fatty liver disease. Expert Review of Gastroenterology & Hepatology 2011, 5(2):253-263.
16. Davis J.N., Lê K.A., Walker R.W., Vikman S., Spruijt-Metz D., Weigensberg M.J., et al. Increased hepatic fat in overweight Hispanic youth influenced by interaction between genetic variation in PNPLA3 and high dietary carbohydrate and sugar consumption. American Journal of Clinical Nutrition 2010, 92(6):1522-1527.
17. Freedman D.S., Khan L.K., Serdula M.K., Dietz W.H., Srinivasan S.R., Berenson G.S. Inter-relationships among childhood BMI, childhood height, and adult obesity: the Bogalusa Heart Study. International Journal of Obesity and Related Metabolic Disorders 2004, 28(1):10-16.
18. Freedman D.S., Khan L.K., Serdula M.K., Dietz W.H., Srinivasan S.R., Berenson G.S. The relation of childhood BMI to adult adiposity: The Bogalusa Heart Study. Pediatrics 2005, 115(1):22-27.
19. Graff M., North K.E., Franceschini N., Reiner A.P., Feitosa M., Carr J.J., et al. PNPLA3 gene-by-visceral adipose tissue volume interaction and the pathogenesis of fatty liver disease: The NHLBI family heart study. International Journal of Obesity 2013, 37(3):432-438.
20. Guyot E., Sutton A., Rufat P., Laguillier C., Mansouri A., Moreau R., et al. PNPLA3 rs738409, hepatocellular carcinoma occurrence and risk model prediction in patients with cirrhosis. Journal of Hepatology 2013, 58(2):312-318.
21. Huang Y., Cohen J.C., Hobbs H.H. Expression and characterization of a PNPLA3 isoform (I148M) associated with nonalcoholic fatty liver disease. Journal of Biological Chemistry 2011, 286(43):37085-37093.
22. Hyysalo J., Gopalacharyulu P., Bian H., Hyötyläinen T., Leivonen M., Jaser N. Circulating triacylglycerol signatures in nonalcoholic fatty liver disease (NAFLD) associated with the I148M variant in PNPLA3 ('PNPLA3 NAFLD') and with obesity ('obese NAFLD'). Diabetes 2014, 63(1):312-322.
23. Kalish B.T., Fallon E.M., Puder M. A tutorial on fatty acid biology. Journal of Parenteral and Enteral Nutrition 2012, 36(4):380-388.
24. Krarup N.T., Grarup N., Banasik K., Friedrichsen M., Færch K., Sandholt C.H., et al. The PNPLA3 rs738409 G-allele associates with reduced fasting serum triglyceride and serum cholesterol in Danes with impaired glucose regulation. PLoS One 2012, 7(7):e40376.
25. Krawczyk M., Gruenhage F., Mahler M., Tirziu S., Acalovschi M., Lammert F. The common adiponutrin variant p.I148M does not confer gallstone risk but affects fasting glucose and triglyceride levels. Journal of Physiology and Pharmacology 2011, 62(3):369-375.
26. Kumari M., Schoiswohl G., Chitraju C., Paar M., Cornaciu I., Rangrez A.Y., et al. Adiponutrin functions as a nutritionally regulated lysophosphatidic acid acyltransferase. Cell Metabolism 2012, 15(5):691-702.
27. Kumashiro N., Yoshimura T., Cantley J.L., Majumdar S.K., Guebre-Egziabher F., Kursawe R., et al. Role of patatin-like phospholipase domain-containing 3 on lipid-induced hepatic steatosis and insulin resistance in rats. Hepatology 2013, 57(5):1763-1772.
28. Li J.Z., Huang Y., Karaman R., Ivanova P.T., Brown H.A., Roddy T. Chronic overexpression of PNPLA3I148M in mouse liver causes hepatic steatosis. Journal of Clinical Investigation 2012, 122(11):4130-4144.
29. Li Y., Xing C., Tian Z., Ku H.C. Genetic variant I148M in PNPLA3 is associated with the ultrasonography-determined steatosis degree in a Chinese population. BMC Medical Genomics 2012, 13:113.
30. Lin Y.C., Chang P.F., Hu F.C., Yang W.S., Chang M.H., Ni Y.H. A common variant in the PNPLA3 gene is a risk factor for non-alcoholic fatty liver disease in obese Taiwanese children. The Journal of pediatrics 2011, 158(5):740-744.
31. Miraglia Del Giudice E., Grandone A., Cirillo G., Santoro N., Amato A., Brienza C., et al. The association of PNPLA3 variants with liver enzymes in childhood obesity is driven by the interaction with abdominal fat. PLoS One 2011, 6(11):e27933.
32. Müller T., Buch S., Berg T., Hampe J., Stickel F. Distinct, alcohol-modulated effects of PNPLA3 genotype on progression of chronic hepatitis C. Journal of Hepatology 2011, 55(3):732-733.
33. Nischalke H.D., Berger C., Luda C., Berg T., Müller T., Grünhage F., et al. The PNPLA3 rs738409 148M/M genotype is a risk factor for liver cancer in alcoholic cirrhosis but shows no or weak association in hepatitis C cirrhosis. PLoS One 2011, 6(11):e27087.
34. Nobili V., Bedogni G., Donati B., Alisi A., Valenti L. The I148M variant of PNPLA3 reduces the response to docosahexaenoic acid in children with non-alcoholic fatty liver disease. Journal of Medicinal Food 2013, 16(10):957-960.
35. Ouyang X., Cirillo P., Sautin Y., McCall S., Bruchette J.L., Diehl A.M., et al. Fructose consumption as a risk factor for non-alcoholic fatty liver disease. Journal of Hepatology 2008, 48(6):993-999.
36. Palmer C.N., Maglio C., Pirazzi C., Burza M.A., Adiels M., Burch L., et al. Paradoxical lower serum triglyceride levels and higher type 2 diabetes mellitus susceptibility in obese individuals with the PNPLA3 148M variant. PLoS One 2012, 7(6):e39362.
37. Petit J.M., Guiu B., Masson D., Duvillard L., Jooste V., Buffier P., et al. Specifically PNPLA3-mediated accumulation of liver fat in obese patients with type 2 diabetes. The Journal of Clinical Endocrinology and Metabolism 2010, 95(12):E430-E436.
38. Pietrangelo A. Hereditary hemochromatosis: Pathogenesis, diagnosis, and treatment. Gastroenterology 2010, 139(2):393-408. (408.e391-392).
39. Pingitore P., Pirazzi C., Mancina R.M., Motta B.M., Indiveri C., Pujia A., et al. Recombinant PNPLA3 protein shows triglyceride hydrolase activity and its I148M mutation results in loss of function. Biochimica et Biophysica Acta 2014, in press.
40. Pirazzi C., Adiels M., Burza M.A., Mancina R.M., Levin M., Ståhlman M., et al. Patatin-like phospholipase domain-containing 3 (PNPLA3) I148M (rs738409) affects hepatic VLDL secretion in humans and in vitro. Journal of Hepatology 2012, 57(6):1276-1282.
41. Romeo S., Kozlitina J., Xing C., Pertsemlidis A., Cox D., Pennacchio L.A., et al. Genetic variation in PNPLA3 confers susceptibility to nonalcoholic fatty liver disease. Nature Genetics 2008, 40(12):1461-1465.
42. Romeo S., Sentinelli F., Cambuli V.M., Incani M., Congiu T., Matta V., et al. The 148M allele of the PNPLA3 gene is associated with indices of liver damage early in life. Journal of Hepatology 2010, 53(2):335-338.
43. Romeo S., Sentinelli F., Dash S., Yeo G.S., Savage D.B., Leonetti F., et al. Morbid obesity exposes the association between PNPLA3 I148M (rs738409) and indices of hepatic injury in individuals of European descent. International Journal of Obesity 2010, 34(1):190-194.
44. Santoro N., Caprio S., Giannini C., Kim G., Kursawe R., Pierpont B., et al. Oxidized fatty acids: A potential pathogenic link between fatty liver and type 2 diabetes in obese adolescents?. Antioxidants Redox Signaling 2014, 20(2):383-389.
45. Santoro N., Kursawe R., D'Adamo E., Dykas D.J., Zhang C.K., Bale A.E., et al. A common variant in the patatin-like phospholipase 3 gene (PNPLA3) is associated with fatty liver disease in obese children and adolescents. Hepatology 2010, 52(4):1281-1290.
46. Santoro N., Savoye M., Kim G., Marotto K., Shaw M.M., Pierpont B., et al. Hepatic fat accumulation is modulated by the interaction between the rs738409 variant in the PNPLA3 gene and the dietary omega6/omega3 PUFA intake. PLoS One 2012, 7(5):e37827.
47. Seth D., Daly A.K., Haber P.S., Day C.P. Patatin-like phospholipase domain containing 3: A case in point linking genetic susceptibility for alcoholic and nonalcoholic liver disease. Hepatology 2010, 51(4):1463-1465.
48. Sevastianova K., Kotronen A., Gastaldelli A., Perttilä J., Hakkarainen A., Lundbom J., et al. Genetic variation in PNPLA3 (adiponutrin) confers sensitivity to weight loss-induced decrease in liver fat in humans. American Journal of Clinical Nutrition 2011, 94(1):104-111.
49. Sevastianova K., Santos A., Kotronen A., Hakkarainen A., Makkonen J., Silander K., et al. Effect of short-term carbohydrate overfeeding and long-term weight loss on liver fat in overweight humans. American Journal of Clinical Nutrition 2012, 96(4):727-734.
50. Sookoian S., Castaño G.O., Burgueño A.L., Gianotti T.F., Rosselli M.S., Pirola C.J. A nonsynonymous gene variant in the adiponutrin gene is associated with nonalcoholic fatty liver disease severity. Journal of Lipid Research 2009, 50(10):2111-2116.
51. Sookoian S., Pirola C.J. Meta-analysis of the influence of I148M variant of patatin-like phospholipase domain containing 3 gene (PNPLA3) on the susceptibility and histological severity of nonalcoholic fatty liver disease. Hepatology 2011, 53(6):1883-1894.
52. Stickel F., Buch S., Lau K., Zu Schwabedissen H.M., Berg T., Ridinger M., et al. Genetic variation in the PNPLA3 gene is associated with alcoholic liver injury in caucasians. Hepatology 2011, 53(1):86-95.
53. Stickel F., Hampe J. Genetic determinants of alcoholic liver disease. Gut 2012, 61(1):150-159.
54. Tian C., Stokowski R.P., Kershenobich D., Ballinger D.G., Hinds D.A. Variant in PNPLA3 is associated with alcoholic liver disease. Nature Genetics 2010, 42(1):21-23.
55. Trépo E., Gustot T., Degré D., Lemmers A., Verset L., Demetter P., et al. Common polymorphism in the PNPLA3/adiponutrin gene confers higher risk of cirrhosis and liver damage in alcoholic liver disease. Journal of Hepatology 2011, 55(4):906-912.
56. Trépo E., Nahon P., Bontempi G., Valenti L., Falleti E., Nischalke H.D., et al. Association Between the PNPLA3 (rs738409 C>G) Variant and Hepatocellular Carcinoma: Evidence from a Meta-Analysis of Individual Participant Data 2014, (accepted for publication). 10.1002/hep.26767.
57. Valenti L., Alisi A., Galmozzi E., Bartuli A., Del Menico B., Alterio A., et al. I148M patatin-like phospholipase domain-containing 3 gene variant and severity of pediatric nonalcoholic fatty liver disease. Hepatology 2010, 52(4):1274-1280.
58. Valenti L., Al-Serri A., Daly A.K., Galmozzi E., Rametta R., Dongiovanni P., et al. Homozygosity for the patatin-like phospholipase-3/adiponutrin I148M polymorphism influences liver fibrosis in patients with nonalcoholic fatty liver disease. Hepatology 2010, 51(4):1209-1217.
59. Valenti L., Colombo M., Fargion S. Modulation of the effect of PNPLA3 I148M mutation on steatosis and liver damage by alcohol intake in patients with chronic hepatitis C. Journal of Hepatology 2011, 55(6):1470-1471. (author reply 1471-1472).
60. Valenti L., Dongiovanni P., Ginanni Corradini S., Burza M.A., Romeo S. PNPLA3 I148M variant and hepatocellular carcinoma: A common genetic variant for a rare disease. Digestive and Liver Disease 2013, 45(8):619-624.
61. Valenti L., Maggioni P., Piperno A., Rametta R., Pelucchi S., Mariani R., et al. Patatin-like phospholipase domain containing-3 gene I148M polymorphism, steatosis, and liver damage in hereditary hemochromatosis. World Journal of Gastroenterology 2012, 18(22):2813-2820.
62. Zampino R., Coppola N., Cirillo G., Boemio A., Pisaturo M., Marrone A., et al. Abdominal fat interacts with PNPLA3 I148M, but not with the APOC3 variant in the pathogenesis of liver steatosis in chronic hepatitis C. Journal of Viral Hepatitis 2013, 20(8):517-523.