Programming of Adipose Tissue MiR-483-3p and GDF-3 Expression by Maternal Diet in Type 2 Diabetes

Overview

Journal Cell Death Differ

Specialty Cell Biology

Date 2012 Jan 7

PMID 22223106

Citations 71

Authors

D Ferland-McCollough

D S Fernandez-Twinn

I G Cannell

H David

M Warner

A A Vaag

J Bork-Jensen

C Brons

T W Gant

A E Willis

K Siddle

M Bushell

S E Ozanne

Affiliations

Soon will be listed here.

Abstract

Nutrition during early mammalian development permanently influences health of the adult, including increasing the risk of type 2 diabetes and coronary heart disease. However, the molecular mechanisms underlying such programming are poorly defined. Here we demonstrate that programmed changes in miRNA expression link early-life nutrition to long-term health. Specifically, we show that miR-483-3p is upregulated in adipose tissue from low-birth-weight adult humans and prediabetic adult rats exposed to suboptimal nutrition in early life. We demonstrate that manipulation of miR-483-3p levels in vitro substantially modulates the capacity of adipocytes to differentiate and store lipids. We show that some of these effects are mediated by translational repression of growth/differentiation factor-3, a target of miR-483-3p. We propose that increased miR-483-3p expression in vivo, programmed by early-life nutrition, limits storage of lipids in adipose tissue, causing lipotoxicity and insulin resistance and thus increasing susceptibility to metabolic disease.

Citing Articles

Platelet-enriched microRNAs as novel biomarkers in atherosclerotic and cardiovascular disease patients.

Masoudikabir P, Shirazy M, Taghizadeh F, Gheydari M, Hamidpour M ARYA Atheroscler. 2024; 20(4):47-67.

PMID: 39717424 PMC: 11663285. DOI: 10.48305/arya.2024.41664.2898.

The role of microRNAs in pregnancies complicated by maternal diabetes.

Owen M, Kennedy M, Quilang R, Scott E, Forbes K Clin Sci (Lond). 2024; 138(18):1179-1207.

PMID: 39289953 PMC: 11409017. DOI: 10.1042/CS20230681.

Overexpression of Igf2-derived Mir483 inhibits Igf1 expression and leads to developmental growth restriction and metabolic dysfunction in mice.

Sandovici I, Fernandez-Twinn D, Campbell N, Cooper W, Sekita Y, Zvetkova I Cell Rep. 2024; 43(9):114750.

PMID: 39283743 PMC: 7617298. DOI: 10.1016/j.celrep.2024.114750.

Plasma miRNAs and Treatment Failure in Participants in the Treatment Options for Type 2 Diabetes in Adolescents and Youth (TODAY) Study.

Wander P, Bammler T, MacDonald J, Srinouanprachanh S, Boyko E, Enquobahrie D Diabetes Care. 2023; 47(3):471-475.

PMID: 38153877 PMC: 10909680. DOI: 10.2337/dc23-1540.

Neonatal adiposity is associated with microRNAs in adipocyte-derived extracellular vesicles in maternal and cord blood, a discovery analysis.

Kunte P, Barberio M, Tiwari P, Sukla K, Harmon B, Epstein S Int J Obes (Lond). 2023; 48(3):403-413.

PMID: 38092957 DOI: 10.1038/s41366-023-01432-z.

References

Meas T . Fetal origins of insulin resistance and the metabolic syndrome: a key role for adipose tissue?. Diabetes Metab. 2009; 36(1):11-20. DOI: 10.1016/j.diabet.2009.09.001. View

Carthew R, Sontheimer E . Origins and Mechanisms of miRNAs and siRNAs. Cell. 2009; 136(4):642-55. PMC: 2675692. DOI: 10.1016/j.cell.2009.01.035. View

Gluckman P, Hanson M, Cooper C, Thornburg K . Effect of in utero and early-life conditions on adult health and disease. N Engl J Med. 2008; 359(1):61-73. PMC: 3923653. DOI: 10.1056/NEJMra0708473. View

Jopling C, Yi M, Lancaster A, Lemon S, Sarnow P . Modulation of hepatitis C virus RNA abundance by a liver-specific MicroRNA. Science. 2005; 309(5740):1577-81. DOI: 10.1126/science.1113329. View

Lillycrop K, Phillips E, Torrens C, Hanson M, Jackson A, Burdge G . Feeding pregnant rats a protein-restricted diet persistently alters the methylation of specific cytosines in the hepatic PPAR alpha promoter of the offspring. Br J Nutr. 2008; 100(2):278-82. PMC: 2564112. DOI: 10.1017/S0007114507894438. View

Ozanne S, Constancia M . Mechanisms of disease: the developmental origins of disease and the role of the epigenotype. Nat Clin Pract Endocrinol Metab. 2007; 3(7):539-46. DOI: 10.1038/ncpendmet0531. View

Fernandez-Twinn D, Ozanne S . Mechanisms by which poor early growth programs type-2 diabetes, obesity and the metabolic syndrome. Physiol Behav. 2006; 88(3):234-43. DOI: 10.1016/j.physbeh.2006.05.039. View

Ozanne S, Jensen C, Tingey K, Storgaard H, Madsbad S, Vaag A . Low birthweight is associated with specific changes in muscle insulin-signalling protein expression. Diabetologia. 2005; 48(3):547-52. DOI: 10.1007/s00125-005-1669-7. View

Bartel D . MicroRNAs: genomics, biogenesis, mechanism, and function. Cell. 2004; 116(2):281-97. DOI: 10.1016/s0092-8674(04)00045-5. View

10.

Virtue S, Vidal-Puig A . Adipose tissue expandability, lipotoxicity and the Metabolic Syndrome--an allostatic perspective. Biochim Biophys Acta. 2010; 1801(3):338-49. DOI: 10.1016/j.bbalip.2009.12.006. View

11.

Erhuma A, Salter A, Sculley D, Langley-Evans S, Bennett A . Prenatal exposure to a low-protein diet programs disordered regulation of lipid metabolism in the aging rat. Am J Physiol Endocrinol Metab. 2007; 292(6):E1702-14. PMC: 1890310. DOI: 10.1152/ajpendo.00605.2006. View

12.

Zhang J, Zhang F, Didelot X, Bruce K, Cagampang F, Vatish M . Maternal high fat diet during pregnancy and lactation alters hepatic expression of insulin like growth factor-2 and key microRNAs in the adult offspring. BMC Genomics. 2009; 10:478. PMC: 2770530. DOI: 10.1186/1471-2164-10-478. View

13.

Shen J, Huang L, Li L, Jorgez C, Matzuk M, Brown C . Deficiency of growth differentiation factor 3 protects against diet-induced obesity by selectively acting on white adipose. Mol Endocrinol. 2008; 23(1):113-23. PMC: 2646597. DOI: 10.1210/me.2007-0322. View

14.

Le Quesne J, Spriggs K, Bushell M, Willis A . Dysregulation of protein synthesis and disease. J Pathol. 2009; 220(2):140-51. DOI: 10.1002/path.2627. View

15.

Nielsen F . The molecular and cellular biology of insulin-like growth factor II. Prog Growth Factor Res. 1992; 4(3):257-90. DOI: 10.1016/0955-2235(92)90023-b. View

16.

Herrera B, Lockstone H, Taylor J, Ria M, Barrett A, Collins S . Global microRNA expression profiles in insulin target tissues in a spontaneous rat model of type 2 diabetes. Diabetologia. 2010; 53(6):1099-109. PMC: 2860560. DOI: 10.1007/s00125-010-1667-2. View

17.

Grimson A, Farh K, Johnston W, Garrett-Engele P, Lim L, Bartel D . MicroRNA targeting specificity in mammals: determinants beyond seed pairing. Mol Cell. 2007; 27(1):91-105. PMC: 3800283. DOI: 10.1016/j.molcel.2007.06.017. View

18.

Andersson O, Korach-Andre M, Reissmann E, Ibanez C, Bertolino P . Growth/differentiation factor 3 signals through ALK7 and regulates accumulation of adipose tissue and diet-induced obesity. Proc Natl Acad Sci U S A. 2008; 105(20):7252-6. PMC: 2438236. DOI: 10.1073/pnas.0800272105. View

19.

Vaag A, Jensen C, Poulsen P, Brons C, Pilgaard K, Grunnet L . Metabolic aspects of insulin resistance in individuals born small for gestational age. Horm Res. 2006; 65 Suppl 3:137-43. DOI: 10.1159/000091519. View

20.

Murrell A, Heeson S, Reik W . Interaction between differentially methylated regions partitions the imprinted genes Igf2 and H19 into parent-specific chromatin loops. Nat Genet. 2004; 36(8):889-93. DOI: 10.1038/ng1402. View