A prospective case-control study on miRNA circulating levels in subjects born small for gestational age (SGA) evaluated from childhood into young adulthood
Autoři:
Elena Inzaghi aff001; Anna Kistner aff002; Daniela Germani aff004; Annalisa Deodati aff001; Mireille Vanpee aff005; Lena Legnevall aff005; Katarina Berinder aff002; Stefano Cianfarani aff001
Působiště autorů:
Dipartimento Pediatrico Universitario Ospedaliero, “Bambino Gesù” Children’s Hospital – Tor Vergata University, Rome, Italy
aff001; Department of Molecular Medicine and Surgery, Karolinska Institutet, Stockholm, Sweden
aff002; Department of Medical Radiation Physics and Nuclear Medicine, Imaging and Physiology, Karolinska University Hospital, Stockholm, Sweden
aff003; Dipartimento di Medicina dei Sistemi, University of Rome Tor vergata, Rome, Italy
aff004; Department of Women’s and Children’s Health, Karolinska Institutet and University Hospital, Stockholm, Sweden
aff005; Patient Area Endocrinology and Nephrology, Karolinska University Hospital, Stockholm, Sweden
aff006
Vyšlo v časopise:
PLoS ONE 15(1)
Kategorie:
Research Article
doi:
https://doi.org/10.1371/journal.pone.0228075
Souhrn
Objective
microRNAs (miRNAs) associated with metabolic risk have never been extensively investigated in SGA subjects. The aim of the current study was to evaluate miRNAs in SGA and AGA subjects and their relationships with the metabolic status and growth.
Design and methods
A prospective longitudinal case-control study was performed in 23 SGA with postnatal catch-up growth and 27 AGA subjects evaluated at the age of 9 and 21 years. Circulating levels of miR-122-5p, miR-16-5p, miR-126-3p, and miR-486-5p were assessed by qPCR.
Results
SGA subjects were shorter both at 9 and at 21 years. No significant differences in insulin like growth factors and metabolic profile were found with the exception of basal glycemia at 9 years. miRNA levels did not differ between SGA and AGA subjects, at 9 and 21 years. miR-16-5p and miR-126-3p levels were higher at 9 than at 21 years. In SGA subjects, miR-122-5p at 9 years was inversely related to adiponectin levels at 21 years and miR-486-5p at 9 years was inversely related to whole-body insulin sensitivity at 9 years and directly related to Hb1Ac at 21 years. Regression analyses showed no predictive value of miRNAs for growth parameters in neither SGA nor AGA subjects.
Conclusions
SGA with postnatal catch-up growth did not show any difference in metabolic risk markers or miRNA circulating levels compared to AGA controls in childhood and young adulthood. miR-122-5p during childhood could identify SGA subjects at higher risk of developing insulin resistance and, eventually, type 2 diabetes in adulthood but further studies are needed to confirm it.
Klíčová slova:
Adiponectin – Adults – Fats – Childhood obesity – Insulin – Insulin resistance – leptin – MicroRNAs
Zdroje
1. Langley-Evans SC, McMullen S. Developmental origins of adult disease. Med Princ Pract. 2010;19(2):87–98. Epub 2010/02/06. doi: 10.1159/000273066 20134170.
2. Barker DJ, Winter PD, Osmond C, Margetts B, Simmonds SJ. Weight in infancy and death from ischaemic heart disease. Lancet. 1989;2(8663):577–80. Epub 1989/09/09. doi: 10.1016/s0140-6736(89)90710-1 2570282.
3. Barker DJ, Hales CN, Fall CH, Osmond C, Phipps K, Clark PM. Type 2 (non-insulin-dependent) diabetes mellitus, hypertension and hyperlipidaemia (syndrome X): relation to reduced fetal growth. Diabetologia. 1993;36(1):62–7. Epub 1993/01/01. doi: 10.1007/bf00399095 8436255.
4. Ravelli AC, van der Meulen JH, Michels RP, Osmond C, Barker DJ, Hales CN, et al. Glucose tolerance in adults after prenatal exposure to famine. Lancet. 1998;351(9097):173–7. Epub 1998/02/05. doi: 10.1016/s0140-6736(97)07244-9 9449872.
5. Barker DJ, Martyn CN, Osmond C, Hales CN, Fall CH. Growth in utero and serum cholesterol concentrations in adult life. Bmj. 1993;307(6918):1524–7. Epub 1993/12/11. doi: 10.1136/bmj.307.6918.1524 8274921.
6. Ramadhani MK, Grobbee DE, Bots ML, Castro Cabezas M, Vos LE, Oren A, et al. Lower birth weight predicts metabolic syndrome in young adults: the Atherosclerosis Risk in Young Adults (ARYA)-study. Atherosclerosis. 2006;184(1):21–7. Epub 2005/12/06. doi: 10.1016/j.atherosclerosis.2005.03.022 16326169.
7. van der Steen M, Hokken-Koelega AC. Growth and Metabolism in Children Born Small for Gestational Age. Endocrinol Metab Clin North Am. 2016;45(2):283–94. Epub 2016/06/01. doi: 10.1016/j.ecl.2016.01.008 27241965.
8. Mericq V, Martinez-Aguayo A, Uauy R, Iñiguez G, Van der Steen M, Hokken-Koelega A. Long-term metabolic risk among children born premature or small for gestational age. Nat Rev Endocrinol. 2017;13(1):50–62. Epub 2016/08/19. doi: 10.1038/nrendo.2016.127 27539244.
9. Cianfarani S, Germani D, Branca F. Low birthweight and adult insulin resistance: the "catch-up growth" hypothesis. Arch Dis Child Fetal Neonatal Ed. 1999;81(1):F71–3. Epub 1999/06/22. doi: 10.1136/fn.81.1.f71 10375369.
10. Leunissen RW, Kerkhof GF, Stijnen T, Hokken-Koelega A. Timing and tempo of first-year rapid growth in relation to cardiovascular and metabolic risk profile in early adulthood. JAMA: the journal of the American Medical Association. 2009;301(21):2234–42. doi: 10.1001/jama.2009.761 19491185
11. Mansego ML, Garcia-Lacarte M, Milagro FI, Marti A, Martinez JA. DNA methylation of miRNA coding sequences putatively associated with childhood obesity. Pediatr Obes. 2017;12(1):19–27. Epub 2016/01/20. doi: 10.1111/ijpo.12101 26780939.
12. Sookoian S, Gianotti TF, Burgueno AL, Pirola CJ. Fetal metabolic programming and epigenetic modifications: a systems biology approach. Pediatr Res. 2013;73(4 Pt 2):531–42. Epub 2013/01/15. doi: 10.1038/pr.2013.2 23314294.
13. Ha M, Kim VN. Regulation of microRNA biogenesis. Nat Rev Mol Cell Biol. 2014;15(8):509–24. Epub 2014/07/17. doi: 10.1038/nrm3838 25027649.
14. Fischer-Posovszky P, Roos J, Kotnik P, Battelino T, Inzaghi E, Nobili V, et al. Functional Significance and Predictive Value of MicroRNAs in Pediatric Obesity: Tiny Molecules with Huge Impact? Horm Res Paediatr. 2016;86(1):3–10. Epub 2016/05/11. doi: 10.1159/000444677 27161162.
15. Seyhan AA. microRNAs with different functions and roles in disease development and as potential biomarkers of diabetes: progress and challenges. Mol Biosyst. 2015;11(5):1217–34. Epub 2015/03/15. doi: 10.1039/c5mb00064e 25765998.
16. Kitsiou-Tzeli S, Tzetis M. Maternal epigenetics and fetal and neonatal growth. Curr Opin Endocrinol Diabetes Obes. 2017;24(1):43–6. Epub 2016/11/30. 27898587.
17. Romaine SP, Tomaszewski M, Condorelli G, Samani NJ. MicroRNAs in cardiovascular disease: an introduction for clinicians. Heart. 2015;101(12):921–8. Epub 2015/03/31. doi: 10.1136/heartjnl-2013-305402 25814653.
18. Parrizas M, Novials A. Circulating microRNAs as biomarkers for metabolic disease. Best Pract Res Clin Endocrinol Metab. 2016;30(5):591–601. Epub 2016/12/08. doi: 10.1016/j.beem.2016.08.001 27923453.
19. Carreras-Badosa G, Bonmati A, Ortega FJ, Mercader JM, Guindo-Martinez M, Torrents D, et al. Dysregulation of Placental miRNA in Maternal Obesity Is Associated With Pre- and Postnatal Growth. J Clin Endocrinol Metab. 2017;102(7):2584–94. Epub 2017/04/04. doi: 10.1210/jc.2017-00089 28368446.
20. Cai M, Kolluru GK, Ahmed A. Small Molecule, Big Prospects: MicroRNA in Pregnancy and Its Complications. J Pregnancy. 2017;2017:6972732. Epub 2017/07/18. doi: 10.1155/2017/6972732 28713594.
21. Marzano F, Faienza MF, Caratozzolo MF, Brunetti G, Chiara M, Horner DS, et al. Pilot study on circulating miRNA signature in children with obesity born small for gestational age and appropriate for gestational age. Pediatr Obes. 2018;13(12):803–11. Epub 2018/08/31. doi: 10.1111/ijpo.12439 30160046.
22. Rottiers V, Naar AM. MicroRNAs in metabolism and metabolic disorders. Nat Rev Mol Cell Biol. 2012;13(4):239–50. Epub 2012/03/23. doi: 10.1038/nrm3313 22436747.
23. Cui X, You L, Zhu L, Wang X, Zhou Y, Li Y, et al. Change in circulating microRNA profile of obese children indicates future risk of adult diabetes. Metabolism. 2018;78:95–105. Epub 2017/10/03. doi: 10.1016/j.metabol.2017.09.006 28966078.
24. Prats-Puig A, Ortega FJ, Mercader JM, Moreno-Navarrete JM, Moreno M, Bonet N, et al. Changes in circulating microRNAs are associated with childhood obesity. J Clin Endocrinol Metab. 2013;98(10):E1655–60. Epub 2013/08/10. doi: 10.1210/jc.2013-1496 23928666.
25. Bork-Jensen J, Scheele C, Christophersen DV, Nilsson E, Friedrichsen M, Fernandez-Twinn DS, et al. Glucose tolerance is associated with differential expression of microRNAs in skeletal muscle: results from studies of twins with and without type 2 diabetes. Diabetologia. 2015;58(2):363–73. Epub 2014/11/19. doi: 10.1007/s00125-014-3434-2 25403480.
26. Maccani MA, Padbury JF, Marsit CJ. miR-16 and miR-21 expression in the placenta is associated with fetal growth. PLoS One. 2011;6(6):e21210. Epub 2011/06/24. doi: 10.1371/journal.pone.0021210 21698265.
27. Kistner A, Rakow A, Legnevall L, Marchini G, Brismar K, Hall K, et al. Differences in insulin resistance markers between children born small for gestational age or born preterm appropriate for gestational age. Acta Paediatr. 2012;101(12):1217–24. Epub 2012/08/29. doi: 10.1111/apa.12005 22924816.
28. Wikland KA, Luo ZC, Niklasson A, Karlberg J. Swedish population-based longitudinal reference values from birth to 18 years of age for height, weight and head circumference. Acta Paediatr. 2002;91(7):739–54. Epub 2002/08/31. doi: 10.1080/08035250213216 12200898.
29. Diagnosis and classification of diabetes mellitus. Diabetes Care. 2010;33 Suppl 1:S62–9. Epub 2010/01/29. doi: 10.2337/dc10-S062 20042775.
30. Yeckel CW, Weiss R, Dziura J, Taksali SE, Dufour S, Burgert TS, et al. Validation of insulin sensitivity indices from oral glucose tolerance test parameters in obese children and adolescents. J Clin Endocrinol Metab. 2004;89(3):1096–101. Epub 2004/03/06. doi: 10.1210/jc.2003-031503 15001593.
31. Matsuda M, DeFronzo RA. Insulin sensitivity indices obtained from oral glucose tolerance testing: comparison with the euglycemic insulin clamp. Diabetes Care. 1999;22(9):1462–70. Epub 1999/09/10. doi: 10.2337/diacare.22.9.1462 10480510.
32. Cianfarani S, Inzaghi E, Alisi A, Germani D, Puglianiello A, Nobili V. Insulin-like growth factor-I and -II levels are associated with the progression of nonalcoholic fatty liver disease in obese children. J Pediatr. 2014;165(1):92–8. Epub 2014/03/13. doi: 10.1016/j.jpeds.2014.01.052 24607243.
33. Vandesompele J, De Preter K, Pattyn F, Poppe B, Van Roy N, De Paepe A, et al. Accurate normalization of real-time quantitative RT-PCR data by geometric averaging of multiple internal control genes. Genome Biol. 2002;3(7):Research0034. Epub 2002/08/20. doi: 10.1186/gb-2002-3-7-research0034 12184808.
34. Mericq V, Martinez-Aguayo A, Uauy R, Iniguez G, Van der Steen M, Hokken-Koelega A. Long-term metabolic risk among children born premature or small for gestational age. Nat Rev Endocrinol. 2017;13(1):50–62. Epub 2016/11/04. doi: 10.1038/nrendo.2016.127 27539244.
35. Wang R, Hong J, Cao Y, Shi J, Gu W, Ning G, et al. Elevated circulating microRNA-122 is associated with obesity and insulin resistance in young adults. Eur J Endocrinol. 2015;172(3):291–300. Epub 2014/12/18. doi: 10.1530/EJE-14-0867 25515554.
36. Miyaaki H, Ichikawa T, Kamo Y, Taura N, Honda T, Shibata H, et al. Significance of serum and hepatic microRNA-122 levels in patients with non-alcoholic fatty liver disease. Liver Int. 2014;34(7):e302–7. Epub 2013/12/10. doi: 10.1111/liv.12429 24313922.
37. Yamada H, Suzuki K, Ichino N, Ando Y, Sawada A, Osakabe K, et al. Associations between circulating microRNAs (miR-21, miR-34a, miR-122 and miR-451) and non-alcoholic fatty liver. Clin Chim Acta. 2013;424:99–103. Epub 2013/06/04. doi: 10.1016/j.cca.2013.05.021 23727030.
38. Brandt S, Roos J, Inzaghi E, Kotnik P, Kovac J, Battelino T, et al. Circulating levels of miR-122 and nonalcoholic fatty liver disease in pre-pubertal obese children. Pediatr Obes. 2018;13(3):175–82. Epub 2017/12/23. doi: 10.1111/ijpo.12261 29271122.
39. Castano C, Kalko S, Novials A, Parrizas M. Obesity-associated exosomal miRNAs modulate glucose and lipid metabolism in mice. Proc Natl Acad Sci U S A. 2018;115(48):12158–63. Epub 2018/11/16. doi: 10.1073/pnas.1808855115 30429322.
40. Lihn AS, Pedersen SB, Richelsen B. Adiponectin: action, regulation and association to insulin sensitivity. Obes Rev. 2005;6(1):13–21. Epub 2005/01/19. doi: 10.1111/j.1467-789X.2005.00159.x 15655035.
41. Flowers E, Aouizerat BE, Abbasi F, Lamendola C, Grove KM, Fukuoka Y, et al. Circulating microRNA-320a and microRNA-486 predict thiazolidinedione response: Moving towards precision health for diabetes prevention. Metabolism. 2015;64(9):1051–9. Epub 2015/06/03. doi: 10.1016/j.metabol.2015.05.013 26031505.
42. Small EM, O’Rourke JR, Moresi V, Sutherland LB, McAnally J, Gerard RD, et al. Regulation of PI3-kinase/Akt signaling by muscle-enriched microRNA-486. Proc Natl Acad Sci U S A. 2010;107(9):4218–23. Epub 2010/02/10. doi: 10.1073/pnas.1000300107 20142475.
43. Hromadnikova I, Kotlabova K, Hympanova L, Krofta L. Cardiovascular and Cerebrovascular Disease Associated microRNAs Are Dysregulated in Placental Tissues Affected with Gestational Hypertension, Preeclampsia and Intrauterine Growth Restriction. PLoS One. 2015;10(9):e0138383. Epub 2015/09/24. doi: 10.1371/journal.pone.0138383 26394310.
44. Wang X, Lian Y, Wen X, Guo J, Wang Z, Jiang S, et al. Expression of miR-126 and its potential function in coronary artery disease. Afr Health Sci. 2017;17(2):474–80. Epub 2017/10/25. doi: 10.4314/ahs.v17i2.22 29062343.
45. Huan T, Chen G, Liu C, Bhattacharya A, Rong J, Chen BH, et al. Age-associated microRNA expression in human peripheral blood is associated with all-cause mortality and age-related traits. Aging Cell. 2018;17(1). Epub 2017/10/19. doi: 10.1111/acel.12687 29044988.
46. Clayton PE, Cianfarani S, Czernichow P, Johannsson G, Rapaport R, Rogol A. Management of the child born small for gestational age through to adulthood: a consensus statement of the International Societies of Pediatric Endocrinology and the Growth Hormone Research Society. J Clin Endocrinol Metab. 2007;92(3):804–10. Epub 2007/01/04. doi: 10.1210/jc.2006-2017 17200164.
47. Finken MJJ, van der Steen M, Smeets CCJ, Walenkamp MJE, de Bruin C, Hokken-Koelega ACS, et al. Children Born Small for Gestational Age: Differential Diagnosis, Molecular Genetic Evaluation, and Implications. Endocr Rev. 2018;39(6):851–94. Epub 2018/07/10. doi: 10.1210/er.2018-00083 29982551.
48. Meas T, Deghmoun S, Armoogum P, Alberti C, Levy-Marchal C. Consequences of being born small for gestational age on body composition: an 8-year follow-up study. J Clin Endocrinol Metab. 2008;93(10):3804–9. Epub 2008/07/17. doi: 10.1210/jc.2008-0488 18628518.
49. Leunissen RW, Stijnen T, Hokken-Koelega AC. Influence of birth size on body composition in early adulthood: the programming factors for growth and metabolism (PROGRAM)-study. Clin Endocrinol (Oxf). 2009;70(2):245–51. Epub 2008/07/12. doi: 10.1111/j.1365-2265.2008.03320.x 18616715.
50. Inzaghi E, Baldini Ferroli B, Fintini D, Grossi A, Nobili V, Cianfarani S. Insulin-Like Growth Factors and Metabolic Syndrome in Obese Children. Horm Res Paediatr. 2017;87(6):400–4. Epub 2017/06/02. doi: 10.1159/000477241 28571015.
51. Cianfarani S. Insulin-like growth factor-II: new roles for an old actor. Front Endocrinol (Lausanne). 2012;3:118. Epub 2012/10/13. doi: 10.3389/fendo.2012.00118 23060858.
Článek vyšel v časopise
PLOS One
2020 Číslo 1
- S diagnostikou Parkinsonovy nemoci může nově pomoci AI nástroj pro hodnocení mrkacího reflexu
- Proč při poslechu některé muziky prostě musíme tančit?
- Je libo čepici místo mozkového implantátu?
- Chůze do schodů pomáhá prodloužit život a vyhnout se srdečním chorobám
- Pomůže v budoucnu s triáží na pohotovostech umělá inteligence?
Nejčtenější v tomto čísle
- Severity of misophonia symptoms is associated with worse cognitive control when exposed to misophonia trigger sounds
- Chemical analysis of snus products from the United States and northern Europe
- Calcium dobesilate reduces VEGF signaling by interfering with heparan sulfate binding site and protects from vascular complications in diabetic mice
- Effect of Lactobacillus acidophilus D2/CSL (CECT 4529) supplementation in drinking water on chicken crop and caeca microbiome
Zvyšte si kvalifikaci online z pohodlí domova
Všechny kurzy