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Plasma Soluble A-Klotho Protein Levels in Premature and Term Neonates

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Plasma Soluble A-Klotho Protein Levels in Premature and Term Neonates European Journal of Endocrinology (2012) 167 433–440 ISSN 0804-4643 CLINICAL STUDY Plasma soluble a-klotho protein levels in premature and term neonates: correlations with growth and metabolic parameters Tania Siahanidou1,*, Maria Garatzioti1,*, Christina Lazaropoulou2, Georgia Kourlaba1, Ioannis Papassotiriou2, Tomoshige Kino3, Akihiro Imura4, Yo-ichi Nabeshima4 and George Chrousos1 1First Department of Pediatrics, Athens University Medical School and 2Department of Clinical Biochemistry, ‘AghiaSophia’ Children’s Hospital, 115 27 Athens, Greece, 3Unit on Molecular Hormone Action, Program in Reproductive and Adult Endocrinology, Eunice Kennedy Shriver National Institute of Child Health and Human Development, National Institutes of Health, Bethesda, Maryland, USA and 4Laboratory of Molecular Life Science, Institute of Biomedical Research and Innovation, Foundation for Biochemical Research and Innovation, Kyoto, Japan (Correspondence should be addressed to T Siahanidou; Email: [email protected]) *(T Siahanidou and M Garatzioti contributed equally to this work) Abstract Objective: a-Klotho (a-KL), a protein with antiaging properties, regulates phosphate, calcium, and bone metabolism, induces resistance to oxidative stress, and may participate in insulin signaling. The role of a-KL in neonates, known to be prone to metabolic disturbances and oxidative stress, is not known. The aim of this study was to evaluate circulating soluble a-KL concentrations in preterm and full-term neonates and unravel possible correlations with growth, metabolism, and indices of oxidative stress. Design: Prospective study. Methods: Plasma-soluble a-KL levels were determined by specific ELISA in 50 healthy neonates (25 preterm, mean (S.D.) gestational age (GA) 33.7 (1.1) weeks, and 25 full-term infants) at days 14 and 28 of life. Associations of a-KL with anthropometric, metabolic parameters, and indices of oxidative stress were examined. Results: a-KL levels were significantly higher in full-term than in preterm infants at both days 14 (1099 (480) pg/ml vs 884 (239) pg/ml respectively; P!0.05) and 28 (1277 (444) pg/ml vs 983 (264) pg/ml respectively; P!0.01). In both preterm and full-term infants, a-KL levels increased significantly from day 14 to 28 of life (P!0.001). Circulating a-KL concentrations correlated with GA (bZ0.32, PZ0.001), body weight (bZ0.34, PZ0.001), body length (bZ0.33, PZ0.001), 1,25-dihydroxy-vitamin D level (bZ0.24, P!0.05), and malondialdehyde level (bZ0.20, P!0.05) but not with glucose, insulin, or homeostasis model assessment index of insulin resistance values. Conclusions: Soluble a-KL levels rise as GA and postnatal age advance in neonates and may have an impact on vitamin D metabolism and oxidative stress. Whether a-KL may have a role in the regulation of infants’ growth should be further studied. European Journal of Endocrinology 167 433–440 Introduction tissue, and the placenta (1, 3, 4). The extracellular domain of a-KL protein is shed and secreted into the In Greek mythology, Klotho – the daughter of Zeus and blood (soluble a-KL protein), exerting hormonal actions Themis – was combing and spinning the thread of life. (2, 5, 6). This fragment is also detectable in the In science, the name Klotho was given to a gene cerebrospinal fluid and urine (6, 7). a-KL protein (a-klotho (a-kl) gene), first identified in 1997, whose participates in the regulation of parathyroid hormone disruption resulted in premature aging-related pheno- (PTH) secretion and vitamin D biosynthesis, in the types in a mouse model (1, 2). The a-kl mutant mice transepithelial transport of calcium ions (Ca2C) in the exhibited early progressive arteriosclerosis, neural choroid plexus and kidney, and also in phosphate degeneration, skin and gonadal atrophy, infertility, reabsorption by the kidney (8, 9, 10). calcification of soft tissues, pulmonary emphysema, Although its molecular mechanisms of action have and a short life span. not been fully elucidated, a-KL protein acts as a cofactor The a-kl gene encodes a 130 kDa (1014 amino acids) of fibroblast growth factor 23 (FGF23), a hormone type I membrane protein (a-KL protein) expressed produced by osteoblasts, that enhances renal phosphate mainly in the kidneys, parathyroid glands, and choroid excretion and suppresses circulating 1,25-dihydroxy- plexus of the brain but also at lower levels in other vitamin D (1,25(OH)2D) levels (9, 11, 12). In addition, organs, including the liver, skeletal muscles, adipose a-KL protein plays a critical role in transepithelial Ca2C q 2012 European Society of Endocrinology DOI: 10.1530/EJE-12-0476 Online version via www.eje-online.org Downloaded from Bioscientifica.com at 09/24/2021 01:08:03AM via free access 434 T Siahanidou, M Garatzioti and others EUROPEAN JOURNAL OF ENDOCRINOLOGY (2012) 167 transport by regulating the abundance of transient weight 1726 (268) g, and male:female ratio 12:13 and receptor potential vanilloid 5 (TRPV5) channels and by 25 full-term infants (GA 39.1 (1.3) weeks and birth recruiting NaC/KC-ATPase to the cell surface mem- weight 3033 (460) g) who had similar gender brane (7, 10, 12, 13). A decrease in a-KL protein in distribution to that of preterm infants. Ten out of 50 mice and humans results in severe hyperphosphatemia neonates (five preterm and five full-term babies) were and increased 1,25(OH)2D concentrations followed by small for GA (SGA; birth weight below the 10th increased PTH levels, hypercalcemia, and elevated percentile after adjusting for GA and gender). GA was FGF23 serum concentrations in compensation for the estimated from the last menstrual period and confirmed impaired FGF23 signaling (10). On the other hand, by fetal ultrasound measurements and clinical exami- an increase in circulating a-KL protein concentrations nation of the neonate according to the new Ballard led to elevation of FGF23 signaling, phosphaturia, score (24). severe hypophosphatemia, and decreased 1,25(OH)2D Criteria for eligibility in the study included: i) absence circulating levels (hypophosphatemic rickets) associated of congenital malformations or major neonatal morbid- with increased PTH circulating levels and marked ities (respiratory distress requiring assisted ventilation parathyroid hyperplasia (10, 14). or oxygen supplementation after day 3 of life in preterm Although the majority of studies have focused on the and full-term infants respectively, hypotension with role of a-KL protein in calcium and phosphorus need for inotropes, intraventricular hemorrhageO homeostasis, there is also evidence that a-KL induces grade I (criteria Volpe), sepsis, and necrotizing enter- resistance against oxidative stress (15) while it possibly ocolitis); and ii) tolerance of full enteric feeding suppresses insulin signaling and participates in the (R150 ml/kg per day) up to day 3 of life for full-term pathogenesis of insulin resistance (IR) (2, 16). More- infants and day 10 of life for preterm infants. All the over, it has been reported that a-KL promotes adipocyte infants were fed with breast milk and formula during differentiation (17) while, interestingly, leptin, the the experiment. In order to avoid differences in nutrient ob gene product secreted by adipocytes, is involved in intake that might have had an impact on a-KL levels or the control of calcium, phosphate, and 1,25(OH)2D other blood measurements, the same commercial homeostasis via stimulation of FGF23 synthesis (18). formula (S26Gold; Wyeth Nutritionals, Askeaton, Neonates, especially preterm ones, are prone to Ireland) was used. In all the infants, anthropometric metabolic disturbances of calcium, phosphate, glucose, parameters were obtained periodically by the same and vitamin D and are also susceptible to oxidative investigator. Body weight was obtained daily in preterm stress due to immature antioxidant defense mechanisms infants and weekly in full-term infants using a standard (19, 20). Moreover, preterm infants are at risk for the electronic scale. Recumbent length was measured using later development of IR (21). Indeed, prepubertal children a standardized length board. aged between 4 and 10 years old, who had been born Blood samples were drawn from a forearm vein in all prematurely, had a reduction in insulin sensitivity the infants before feeding on the morning of days 14 and compared with children born at term (22). Interestingly, 28 of life for routine blood tests as well as for a previous study showed that IR may be present even at determining plasma levels of soluble a-KL protein; birth in preterm infants (23).Toourknowledge,a-KL serum concentrations of calcium, phosphate, FGF23, protein has been little studied in neonates; its circulating 1,25(OH)2D, PTH, glucose, and insulin; and oxidative levels were determined only in a study of full-term babies stress indices; MDA level in serum as marker of oxidative at birth and/or at day 4 of life (4). stress damage and SOD activity in washed red blood The aim of this study was to evaluate the circulating cells as a free radical scavenging system were concentrations of a-KL protein during the first month of determined. In addition, HOMA-IR index was calculated age in preterm and full-term infants and to unravel as fasting glucose (in mmol/l)!fasting insulin (in mIU/l) possible associations with anthropometric (body weight divided by 22.5 (25). Plasma and serum samples were and length) and metabolic parameters (serum calcium, stored at K80 8C until assayed. The ‘Aghia Sophia’ phosphate, FGF23, 1,25(OH)2D, PTH, glucose, insulin, Children’s Hospital Ethics Committee approved the study homeostasis model assessment index of IR (HOMA-IR)), and informed parental consent was also obtained. and indices of oxidative stress (malondialdehyde (MDA) concentration and superoxide dismutase (SOD) activity). Assays Plasma soluble a-KL protein levels were determined using a sandwich ELISA established by Yamazaki et al. Materials and methods (26); the ELISA kit was provided from Kyowa Hakko- Subjects and study protocol Kirin (Tokyo, Japan).
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