Insights into the pathophysiology of catch-up compared with non-catch-up growth in children born small for gestational age: An integrated analysis of metabolic and transcriptomic data

Pharmacogenomics Journal

Volumn 14, Issue 4, 2014, Pages 376-384

  Stevens, A ^a,b   Bonshek, C ^a,b   Whatmore, A ^a,b   Butcher, I ^a,b   Hanson, D ^a,b   De Leonibus, C ^a,b   Shaikh, G ^c   Brown, M ^b,d   O'Shea, E ^a,b   Victor, S ^e   Powell, P ^f   Settle, P ^g   Padmakumar, B ^h   Tan, A ^h   Odeka, E ^h   Cooper, C ⁱ   Birch, J ^j   Shenoy, A ^k   Westwood, M ^b   Patel, L ^a,b   Dunn, B W ^b,d   Clayton, P ^a,b   more..

^a ROYAL MANCHESTER CHILDREN S HOSPITAL   (United Kingdom)

^b UNIVERSITY OF MANCHESTER   (United Kingdom)

^c ROYAL HOSPITAL FOR SICK CHILDREN   (United Kingdom)

^d MANCHESTER UNIVERSITY NHS FOUNDATION TRUST   (United Kingdom)

^e ST MARY S HOSPITAL   (United Kingdom)

^f ROYAL BOLTON HOSPITAL   (United Kingdom)

^g HOPE HOSPITAL   (United Kingdom)

^h NORTH MANCHESTER GENERAL HOSPITAL   (United Kingdom)

ⁱ STEPPING HILL HOSPITAL   (United Kingdom)

^j TAMESIDE GENERAL HOSPITAL   (United Kingdom)

^k ROYAL ALBERT EDWARD INFIRMARY   (United Kingdom)

more..

Author keywords

catch up growth; metabolomics; network biology; SGA; transcriptomics

Indexed keywords

ADIPONECTIN; CARNITINE; CYCLIC AMP; CYCLIC AMP DEPENDENT PROTEIN KINASE; DECANOIC ACID; EPIDERMAL GROWTH FACTOR; FIBROBLAST GROWTH FACTOR; GLUCOSE; GLUTAMINE; INOSITOL; INSULIN; PLATELET DERIVED GROWTH FACTOR; SOMATOMEDIN C; SPHINGOSINE 1 PHOSPHATE; URIC ACID; VASCULOTROPIN; BIOLOGICAL MARKER; TRANSCRIPTOME;

AMINO ACID BLOOD LEVEL; AMINO ACID URINE LEVEL; ARTICLE; BODY HEIGHT; BODY MASS; BODY WEIGHT; CATCH UP GROWTH; CHILD; CLINICAL ARTICLE; CONTROLLED STUDY; FEMALE; GENE CLUSTER; GENE EXPRESSION; GENE EXPRESSION PROFILING; GLUCOSE BLOOD LEVEL; HUMAN; HUMAN CELL; INSULIN BLOOD LEVEL; INSULIN RESISTANCE; INTRACELLULAR SIGNALING; MALE; METABOLISM; METABOLOMICS; NON CATCH UP GROWTH; PATHOPHYSIOLOGY; PERIPHERAL BLOOD MONONUCLEAR CELL; PRIORITY JOURNAL; PROTEIN BLOOD LEVEL; SMALL FOR DATE INFANT; TRANSCRIPTOMICS; URIC ACID URINE LEVEL; COMPARATIVE STUDY; GROWTH, DEVELOPMENT AND AGING; NEWBORN; PRESCHOOL CHILD;

BIOLOGICAL MARKERS; CHILD; CHILD, PRESCHOOL; FEMALE; HUMANS; INFANT, NEWBORN; INFANT, SMALL FOR GESTATIONAL AGE; MALE; METABOLOMICS; TRANSCRIPTOME;

EID: 84904988471     PISSN: 1470269X     EISSN: 14731150     Source Type: Journal    
DOI: 10.1038/tpj.2014.4     Document Type: Article

References (77)

1. Verlijsdonk JW, Winkens B, Boers K, Scherjon S, Roumen F. Suspected versus non-suspected small-for-gestational age fetuses at term: perinatal outcomes. J Matern Fetal Neonatal Med 2012; 25: 938-943.
2. Pueyo V, Oros D, Valle S, Tuquet H, Güerri N, Argü elles M et al. Axonal loss and cognitive deficits in term infants with normal umbilical artery Doppler born small-for-gestational age. Ultrasound Obstet Gynecol 2012; 40: 297-303.
3. De Bie HM, Oostrom KJ, Boersma M, Veltman DJ, Barkhof F, Delemarre-van de Waal HA et al. Global and regional differences in brain anatomy of young children born small for gestational age. PLoS ONE 2011; 6: e24116.
4. Puga B, Gil P, de Arriba A, Labarta JI, Romo A, Mayayo E et al. Neurocognitive development of children born small for gestational age (SGA). An update. Pediatr Endocrinol Rev 2012; 9: 716-726.
5. Lee PA, Houk CP. Cognitive and psychosocial development concerns in children born small for gestational age. Pediatr Endocrinol Rev 2012; 10: 209-216.
6. Barker DJ. Fetal nutrition and cardiovascular disease in later life. Br Med Bull 1997; 53: 96-108.
7. Nobili V, Alisi A, Panera N, Agostoni C. Low birth weight and catch-up-growth associated with metabolic syndrome: a ten year systematic review. Pediatr Endocrinol Rev 2008; 6: 241-247.
8. de Arriba A, Dominguez M, Labarta JI, Domínguez M, Puga B, Mayayo E et al. Metabolic syndrome and endothelial dysfunction in a population born small for gestational age relationship to growth and Gh therapy. Pediatr Endocrinol Rev 2013; 10: 297-307.
9. Argente J, Mehls O, Barrios V. Growth and body composition in very young SGA children. Pediatr Nephrol 2010; 25: 679-685.
10. 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: 804-810.
11. Bamberg C, Kalache KD. Prenatal diagnosis of fetal growth restriction. Semin Fetal Neonatal Med 2004; 9: 387-394.
12. Chatelain P, Colle M, Nako JP, Le Luyer B, Wagner K, Berlier P et al. Optimization of growth hormone dosing in children born small for gestational age: an open-label, randomized study of children during the fourth year of therapy. Horm Res Paediatr 2012; 77: 156-163.
13. Vaag A. Low birth weight and early weight gain in the metabolic syndrome: consequences for infant nutrition. Int J Gynaecol Obstet 2009; 104(Suppl 1): S32-S34.
14. Levy-Marchal C, Czernichow P. Small for gestational age and the metabolic syndrome: which mechanism is suggested by epidemiological and clinical studies? Horm Res 2006; 65(Suppl 3): 123-130.
15. Leunissen RW, Kerkhof GF, Stijnen T, Hokken-Koelega AC. Effect of birth size and catch-up growth on adult blood pressure and carotid intima-media thickness. Horm Res Paediatr 2012; 77: 394-401.
16. Ibanez L, Suarez L, Lopez-Bermejo A, Diaz M, Valls C, de Zegher F. Early development of visceral fat excess after spontaneous catch-up growth in children with low birth weight. J Clin Endocrinol Metab 2008; 93: 925-928.
17. Veening MA, Van Weissenbruch MM, Delemarre-van de Waal HA. Glucose tolerance, insulin sensitivity, and insulin secretion in children born small for gesta-tional age. J Clin Endocrinol Metab 2002; 87: 4657-4661.
18. Cianfarani S, Maiorana A, Geremia C, Scire G, Spadoni GL, Germani D. Blood glucose concentrations are reduced in children born small for gestational age (SGA), and thyroid-stimulating hormone levels are increased in SGA with blunted postnatal catch-up growth. J Clin Endocrinol Metab 2003; 88: 2699-2705.
19. Ghirri P, Ladaki C, Bartoli A, Scirè G, Vuerich M, Spadoni GL et al. Low birth weight for gestational age associates with reduced glucose concentrations at birth, infancy and childhood. Horm Res 2007; 67: 123-131.
20. Tenhola S, Todorova B, Jaaskelainen J, Janne OA, Raivio T, Voutilainen R. Serum glucocorticoids and adiponectin associate with insulin resistance in children born small for gestational age. Eur J Endocrinol 2010; 162: 551-557.
21. Dunn WB, Broadhurst DI, Atherton HJ, Goodacre R, Griffin JL. Systems level studies of mammalian metabolomes: the roles of mass spectrometry and nuclear magnetic resonance spectroscopy. Chem Soc Rev 2011; 40: 387-426.
22. Dessi A, Atzori L, Noto A, Visser GH, Gazzolo D, Zanardo V et al. Metabolomics in newborns with intrauterine growth retardation (IUGR): urine reveals markers of metabolic syndrome. J Matern Fetal Neonatal Med 2011; 24(Suppl 2): 35-39.
23. Horgan RP, Broadhurst DI, Dunn WB, Brown M, Heazell AE, Kell DB et al. Changes in the metabolic footprint of placental explant-conditioned medium cultured in different oxygen tensions from placentas of small for gestational age and normal pregnancies. Placenta 2010; 31: 893-901.
24. Horgan RP, Broadhurst DI, Walsh SK, Brown M, Heazell AE, Kell DB et al. Metabolic profiling uncovers a phenotypic signature of small for gestational age in early pregnancy. J Proteome Res 2011; 10: 3660-3673.
25. Nascimento NR, Lessa LM, Kerntopf MR, Sousa CM, Alves RS, Queiroz MG et al. Inositols prevent and reverse endothelial dysfunction in diabetic rat and rabbit vasculature metabolically and by scavenging superoxide. Proc Natl Acad Sci USA 2006; 103: 218-223.
26. Jones DR, Varela-Nieto I. The role of glycosyl-phosphatidylinositol in signal transduction. Int J Biochem Cell Biol 1998; 30: 313-326.
27. Larner J. D-chiro-inositol-its functional role in insulin action and its deficit in insulin resistance. Int J Exp Diabetes Res 2002; 3: 47-60.
28. Mannik J, Vaas P, Rull K, Teesalu P, Rebane T, Laan M. Differential expression profile of growth hormone/chorionic somatomammotropin genes in placenta of small-and large-for-gestational-age newborns. J Clin Endocrinol Metab 2010; 95: 2433-2442.
29. Guo L, Choufani S, Ferreira J, Smith A, Chitayat D, Shuman C et al. Altered gene expression and methylation of the human chromosome 11 imprinted region in small for gestational age (SGA) placentae. Dev Biol 2008; 320: 79-91.
30. Toft JH, Lian IA, Tarca AL, Erez O, Espinoza J, Eide IP et al. Whole-genome microarray and targeted analysis of angiogenesis-regulating gene expression (ENG, FLT1, VEGF, PlGF) in placentas from pre-eclamptic and small-for-gestational-age pregnancies. J Matern Fetal Neonatal Med 2008; 21: 267-273.
31. Adkins RM, Tylavsky FA, Krushkal J. Newborn umbilical cord blood DNA methy-lation and gene expression levels exhibit limited association with birth weight. Chem Biodivers 2012; 9: 888-899.
32. Stark C, Breitkreutz BJ, Chatr-Aryamontri A, Boucher L, Oughtred R, Livstone MS et al. The BioGRID Interaction Database: 2011 update. Nucleic Acids Res 2011; 39(Database issue): D698-D704.
33. Choi H, Pavelka N. When one and one gives more than two: challenges and opportunities of integrative omics. Front Genet 2011; 2: 105.
34. Ideker T, Dutkowski J, Hood L. Boosting signal-to-noise in complex biology: prior knowledge is power. Cell 2011; 144: 860-863.
35. Aloy P, Russell RB. Taking the mystery out of biological networks. EMBO Rep 2004; 5: 349-350.
36. Arrell DK, Terzic A. Interpreting networks in systems biology. Clin Pharmacol Ther 2013; 93: 389-392.
37. Barabasi AL. Scale-free networks: a decade and beyond. Science 2009; 325: 412-413.
38. Albert R, Jeong H, Barabasi AL. Error and attack tolerance of complex networks. Nature 2000; 406: 378-382.
39. Barabasi AL, Albert R. Emergence of scaling in random networks. Science 1999; 286: 509-512.
40. Karnovsky A, Weymouth T, Hull T, Tarcea VG, Scardoni G, Laudanna C et al. Metscape 2 bioinformatics tool for the analysis and visualization of metabolomics and gene expression data. Bioinformatics 2012; 28: 373-380.
41. Wit JM, Clayton PE, Rogol AD, Savage MO, Saenger PH, Cohen P. Idiopathic short stature: definition, epidemiology, and diagnostic evaluation. Growth Horm IGF Res 2008; 18: 89-110.
42. Elmlinger MW, Kuhnel W, Weber MM, Ranke MB. Reference ranges for two automated chemiluminescent assays for serum insulin-like growth factor I (IGF-I) and IGF-binding protein 3 (IGFBP-3). Clin Chem Lab Med 2004; 42: 654-664.
43. Heinze E, Holl RW. Tests of Beta Cell Function in Childhood and Adolescence. In: Ranke M (ed). Diagnostics of Endocrine Function in Children and Adolescents. Karger: Basel, AG, 2003, pp 318-338.
44. Dunn WB, Broadhurst D, Begley P, Zelena E, Francis-McIntyre S, Anderson N et al. Procedures for large-scale metabolic profiling of serum and plasma using gas chromatography and liquid chromatography coupled to mass spectrometry. Nat Protoc 2011; 6: 1060-1083.
45. Whatmore AJ, Patel L, Clayton PE. A pilot study to evaluate gene expression profiles in peripheral blood mononuclear cells (PBMCs) from children with GH deficiency and Turner syndrome in response to GH treatment. Clin Endocrinol (Oxf) 2009; 70: 429-434.
46. Stevens A, Hanson D, Whatmore A, Destenaves B, Chatelain P, Clayton P. Human growth is associated with distinct patterns of gene expression in evolutionarily conserved networks. BMC Genomics 2013; 14: 547.
47. Stevens A, Clayton P, Tato L, Yoo HW, Rodriguez-Arnao MD, Skorodok J et al. Pharmacogenomics of insulin-like growth factor-I generation during GH treatment in children with GH deficiency or Turner syndrome. Pharmacogenomics J 2013; 14: 54-62.
48. Sartor MA, Leikauf GD, Medvedovic M. LRpath: a logistic regression approach for identifying enriched biological groups in gene expression data. Bioinformatics 2009; 25: 211-217.
49. Benjamini Y, Hochberg Y. Controlling the False Discovery Rate: A Practical and Powerful Approach to Multiple Testing. J R Statist Soc B 1995; 57: 289-300.
50. Calvano SE, Xiao W, Richards DR, Felciano RM, Baker HV, Cho RJ et al. A network-based analysis of systemic inflammation in humans. Nature 2005; 437: 1032-1037.
51. Smoot ME, Ono K, Ruscheinski J, Wang PL, Ideker T. Cytoscape 2.8: new features for data integration and network visualization. Bioinformatics 2011; 27: 431-432.
52. Deng HZ, Deng H, Su Z, Li YH, Ma HM, Chen HS et al. Insulin resistance and adiponectin levels are associated with height catch-up growth in pre-pubertal Chinese individuals born small for gestational age. Nutr Metab (Lond) 2012; 9: 107-109.
53. Cianfarani S, Martinez C, Maiorana A, Scire G, Spadoni GL, Boemi S. Adiponectin levels are reduced in children born small for gestational age and are inversely related to postnatal catch-up growth. J Clin Endocrinol Metab 2004; 89: 1346-1351.
54. Stefan N, Bunt JC, Salbe AD, Funahashi T, Matsuzawa Y, Tataranni PA. Plasma adiponectin concentrations in children: relationships with obesity and insuline-mia. J Clin Endocrinol Metab 2002; 87: 4652-4656.
55. Lindsay RS, Funahashi T, Hanson RL, Matsuzawa Y, Tanaka S, Tataranni PA et al. Adiponectin and development of type 2 diabetes in the Pima Indian population. Lancet 2002; 360: 57-58.
56. Yamauchi T, Kamon J, Waki H, Terauchi Y, Kubota N, Hara K et al. The fat-derived hormone adiponectin reverses insulin resistance associated with both lipoatrophy and obesity. Nat Med 2001; 7: 941-946.
57. Berg AH, Combs TP, Du X, Brownlee M, Scherer PE. The adipocyte-secreted protein Acrp30 enhances hepatic insulin action. Nat Med 2001; 7: 947-953.
58. Ibanez L, Lopez-Bermejo A, Diaz M, de Zegher F. Catch-up growth in girls born small for gestational age precedes childhood progression to high adiposity. Fertil Steril 2011; 96: 220-223.
59. Bottner A, Kratzsch J, Muller G, Kapellen TM, Blü her S, Keller E et al. Gender differences of adiponectin levels develop during the progression of puberty and are related to serum androgen levels. J Clin Endocrinol Metab 2004; 89: 4053-4061.
60. Wishart DS, Jewison T, Guo AC, Wilson M, Knox C, Liu Y et al. HMDB 3.0-The Human Metabolome Database in 2013. Nucleic Acids Res 2013; 41(Database issue): D801-D807.
61. Nissen PM, Nebel C, Oksbjerg N, Bertram HC. Metabolomics reveals relationship between plasma inositols and birth weight: possible markers for fetal programming of type 2 diabetes. J Biomed Biotechnol 2011; 2011: 1147-1155.
62. Muller G, Wied S, Crecelius A, Kessler A, Eckel J. Phosphoinositolglycan- peptides from yeast potently induce metabolic insulin actions in isolated rat adipocytes, cardiomyocytes, and diaphragms. Endocrinology 1997; 138: 3459-3475.
63. Corrado F, D'Anna R, Di VG, Giordano D, Pintaudi B, Santamaria A et al. The effect of myoinositol supplementation on insulin resistance in patients with gestational diabetes. Diabet Med 2011; 28: 972-975.
64. Falasca M, Hughes WE, Dominguez V, Sala G, Fostira F, Fang MQ et al. The role of phosphoinositide 3-kinase C2alpha in insulin signaling. J Biol Chem 2007; 282: 28226-28236.
65. Islam MS, Rorsman P, Berggren PO. Ca(2 +)-induced Ca2 + release in insulin-secreting cells. FEBS Lett 1992; 296: 287-291.
66. MacDonald MJ, Smith III AD, Hasan NM, Sabat G, Fahien LA. Feasibility of pathways for transfer of acyl groups from mitochondria to the cytosol to form short chain acyl-CoAs in the pancreatic beta cell. J Biol Chem 2007; 282: 30596-30606.
67. Kobayashi T, Kouzaki H, Kita H. Human eosinophils recognize endogenous danger signal crystalline uric acid and produce proinflammatory cytokines mediated by autocrine ATP. J Immunol 2010; 184: 6350-6358.
68. Yuneva M, Zamboni N, Oefner P, Sachidanandam R, Lazebnik Y. Deficiency in glutamine but not glucose induces MYC-dependent apoptosis in human cells. J Cell Biol 2007; 178: 93-105.
69. Li T, Francl JM, Boehme S, Ochoa A, Zhang Y, Klaassen CD et al. Glucose and insulin induction of bile acid synthesis: mechanisms and implication in diabetes and obesity. J Biol Chem 2012; 287: 1861-1873.
70. McLean BN, Allen J, Ferdinandusse S, Wanders RJ. A new defect of peroxisomal function involving pristanic acid: a case report. J Neurol Neurosurg Psychiatry 2002; 72: 396-399.
71. Mitchell CJ, Nelson AE, Cowley MJ, Kaplan W, Stone G, Sutton SK et al. Detection of growth hormone doping by gene expression profiling of peripheral blood. J Clin Endocrinol Metab 2009; 94: 4703-4709.
72. Powell JE, Henders AK, McRae AF, Wright MJ, Martin NG, Dermitzakis ET et al. Genetic control of gene expression in whole blood and lymphoblastoid cell lines is largely independent. Genome Res 2012; 22: 456-466.
73. Horowitz MC, Lorenzo JA. Immunologic regulation of bone development. Adv Exp Med Biol. 2007; 602: 47-56.
74. Romanyukha AA, Yashin AI. Age related changes in population of peripheral T cells: towards a model of immunosenescence. Mech Ageing Dev 2003; 124: 433-443.
75. Weksler ME, Szabo P. The effect of age on the B-cell repertoire. J Clin Immunol 2000; 20: 240-249.
76. Karlberg JP, Albertsson-Wikland K, Kwan EY, Lam BC, Low LC. The timing of early postnatal catch-up growth in normal, full-term infants born short for gestational age. Horm Res 1997; 48(Suppl 1): 17-24.
77. Lee PA, Chernausek SD, Hokken-Koelega AC, Czernichow P. International Small for Gestational Age Advisory Board consensus development conference statement: management of short children born small for gestational age, April 24-October 1, 2001. Pediatrics 2003; 111(6 Pt 1): 1253-1261.