help button home button Endocrine Society JCEM
HOME HELP FEEDBACK SUBSCRIPTIONS ARCHIVE SEARCH TABLE OF CONTENTS
Journal of Clinical Endocrinology & Metabolism , doi:10.1210/jc.2008-0526
This Article
Right arrow Abstract Freely available
Right arrow Full Text (PDF)
Right arrow Submit a related Letter to the Editor
Right arrow Alert me when this article is cited
Right arrow Alert me when eLetters are posted
Right arrow Alert me if a correction is posted
Right arrow Citation Map
Services
Right arrow Email this article to a friend
Right arrow Similar articles in this journal
Right arrow Similar articles in PubMed
Right arrow Alert me to new issues of the journal
Right arrow Download to citation manager
Right arrow Request Copyright Permission
Citing Articles
Right arrow Citing Articles via HighWire
Right arrow Citing Articles via Google Scholar
Google Scholar
Right arrow Articles by Ibáñez, L.
Right arrow Articles by de Zegher, F.
Right arrow Search for Related Content
PubMed
Right arrow PubMed Citation
Right arrow Articles by Ibáñez, L.
Right arrow Articles by de Zegher, F.
Related Collections
Right arrow Pediatric Endocrinology
Right arrow Metabolism
The Journal of Clinical Endocrinology & Metabolism Vol. 93, No. 7 2774-2778
Copyright © 2008 by The Endocrine Society

Gender Specificity of Body Adiposity and Circulating Adiponectin, Visfatin, Insulin, and Insulin Growth Factor-I at Term Birth: Relation to Prenatal Growth

Lourdes Ibáñez1, Giorgia Sebastiani1, Abel Lopez-Bermejo, Marta Díaz, Maria Dolores Gómez-Roig and Francis de Zegher

Endocrinology Unit (L.I., G.S., M.D.) and Department of Gynecology (M.D.G.-R.), Hospital Sant Joan de Déu, University of Barcelona, 08950 Esplugues, Barcelona, Spain; Diabetes, Endocrinology, and Nutrition Unit (A.L.-B.), Dr. Trueta Hospital, 17007 Girona, Spain; and Department of Woman and Child (F.d.Z.), University of Leuven, 3000 Leuven, Belgium

Address all correspondence and requests for reprints to: Lourdes Ibáñez, M.D., Ph.D., Endocrinology Unit, Hospital Sant Joan de Déu, University of Barcelona, Passeig de Sant Joan de Déu, 2, 08950 Esplugues, Barcelona, Spain. E-mail: libanez{at}hsjdbcn.org.


   Abstract
Top
 Abstract
Introduction
 Subjects and Methods
 Results
 Discussion
 References
 
Context: Fetal development is thought to be gender specific for adiposity and circulating insulin and IGF-I but not adipokinemia, as judged by serum visfatin and adiponectin at term birth. We studied the potential relationship between these gender specificities and fetal growth.

Setting: The study was conducted at a university hospital.

Study Population: Subjects included 96 strictly matched neonates born appropriate for gestational age (AGA; 24 girls, 24 boys) or small for gestational age (SGA; 24 girls, 24 boys).

Main Outcomes: Outcomes included serum insulin, IGF-I, visfatin, total and high-molecular-weight (HMW) adiponectin, osteocalcin at term birth, and neonatal body composition by absorptiometry.

Results: Cord insulin and IGF-I levels were higher in girls than boys (P ≤ 0.01), in both the AGA and SGA subpopulation. In AGA newborns, fat and lean mass were each gender specific (P < 0.0001), whereas visfatin and total and HMW adiponectin were not. Conversely, in SGA newborns, visfatin and HMW adiponectin were gender specific (higher levels in girls), whereas body adiposity was not. In SGA fetuses, the distribution of adiponectin isoforms was in both genders shifted toward HMW (P < 0.005 vs. AGA). Cord osteocalcin did not differ by either gender or birth weight.

Conclusion: At term birth, the gender specificity of adiposity and circulating visfatin and HMW adiponectin appeared to depend on prenatal growth, whereas the gender specificity of insulin and IGF-I levels did not. The fetal shift in adiponectin isoforms may contribute to explain why SGA newborns tend to be hypersensitive to insulin.


   Introduction
Top
 Abstract
 Introduction
Subjects and Methods
 Results
 Discussion
 References
 
At term birth, the average weight of girls is lower than that of boys, but girls are more adipose and have higher circulating levels of leptin, insulin, and IGF-I (1, 2, 3, 4, 5). In contrast, after a normal gestation, girls and boys have similar cord serum levels of visfatin and of total or high-molecular-weight (HMW) adiponectin (6, 7, 8, 9, 10, 11). The current view is thus that fetal development is normally gender specific for adiposity but not for adipokines as visfatin and adiponectin.

In adults, visfatin and adiponectin have been linked to insulin resistance and the development of type 2 diabetes and metabolic syndrome (12, 13). Visfatin is thought to have insulin-mimetic properties and to be a marker of visceral fat in children and adults (14, 15, 16). Circulating adiponectin levels, specifically those of the HMW isoform, correlate positively with insulin sensitivity; HMW adiponectin is the most abundant isoform in cord serum at term birth (9, 17, 18). Osteocalcin, an osteoblast-specific protein, was recently shown to enhance insulin action by increasing the release of adiponectin by adipocytes as well as the secretion of insulin by β-cells; these metabolic functions are mediated by the undercarboxylated form of osteocalcin (19).

We posited that gender-specific fat expansion in the human fetus exerts a gender-specific inhibition on fetal visfatin and adiponectin release, thereby annihilating the intrinsically gender-specific release of both adipokines. According to this concept, a prenatal fat expansion that is reduced and (therefore) less gender specific should be followed by a gender-specific up-regulation of fetal visfatinemia and adiponectinemia. To test this hypothesis, we designed a study in which male and female newborns were matched within narrow ranges of either normal or low birth weight.


   Subjects and Methods
Top
 Abstract
 Introduction
 Subjects and Methods
Results
 Discussion
 References
 
Study population

Inclusion criteria were: 1) maternally uncomplicated pregnancy (no gestational diabetes; no preeclampsia; no use of alcohol, drugs, or illicit substances), with delivery at Hospital Sant Joan de Déu in Barcelona between February and November 2007; 2) birth weight appropriate for gestational age (AGA; between –1 and +1 SD) or small for gestational age (SGA; between 1.8 kg and –2 SD) after a term gestation (37–42 wk) (20, 21); 3) availability of cord serum (logistic restraints, especially at nighttime); 4) body composition assessed by absorptiometry at age ~14 d; 5) possibility of strict matching by gender and birth weight (difference less than 0.1 kg), so that girl-boy and AGA-SGA comparisons had a similar power; and 6) ethnically Catalan background allowing for written consent in Catalan. Exclusion criteria were dysmorphic features and 10-min Apgar score less than 7.

In total, 96 newborns were enrolled (Fig. 1Go): 48 AGA (24 girls, 24 boys) and 48 SGA (24 girls, 24 boys).


Figure 1
View larger version (16K):
[in this window]
[in a new window]

  		FIG. 1. Recruitment of the study population.

 
Gestational age was calculated from the last menses and confirmed by first-trimester ultrasound (~10 wk) (22). Prevalence of birth by cesarean section was 22%. While pregnant, 74 mothers (43 AGA, 31 SGA) did not smoke and 22 (five AGA, 17 SGA) did smoke, on average, five cigarettes per day.

Part of the results from 18 AGA infants were included in an earlier genotype-phenotype report (23); none of the results from SGA infants has so far been reported.

Measurements

Cord blood was collected at birth, before placental separation, for measurement of glucose, insulin, IGF-I, total and HMW adiponectin, visfatin, and undercarboxylated osteocalcin. Blood samples were centrifuged and serum frozen at –80 C until assay.

All infants were measured at birth by the same investigator (G.S.). Length was measured with a standardized length board, the mean of three measurements being used for analysis. Weight was measured to the nearest 10 g with a standard beam balance (Seca, Hamburg, Germany).

Body composition was assessed by absorptiometry at the age of 14 ± 0.3 d (mean ± SEM) with a Lunar Prodigy, coupled to Lunar software (version 3.4/3.5; Lunar Corp, Madison, WI), adapted for assessment of infants (23). The instrument underwent daily quality control and weekly calibration against a water phantom. Measurements were performed during the newborn’s spontaneous sleep (and thus without sedation) shortly before a next feeding. The average duration of each measurement was about 10 min; all scans were processed by the same operator. Total body fat, lean mass, and bone mineral content (BMC) were assessed. Irradiation dose was 0.1 m Sievert (~10% of the dose associated with a thorax x-ray). Coefficients of variation (CVs) were less than 3% for fat and lean mass (23).

Assays

Glucose was measured by glucose oxidase method. Insulin and IGF-I were measured by immunochemiluminescence (IMMULITE 2000; Diagnostic Products, Los Angeles, CA). The lower detection limit for insulin was 0.4 µU/ml; values below this limit were considered to be 0.4 µU/ml; the lower limit for IGF-1 was 25 ng/ml; the intra- and interassay CVs for insulin and IGF-1 were less than 10%. Total adiponectin was measured by RIA (Linco Research, St. Charles, MO) with intra- and interassay CVs of 6.2 and 6.9%; HMW adiponectin and visfatin were assessed with ELISA kits from Linco Research and, respectively, Phoenix Pharmaceutical (Belmont, CA); intra- and interassay CVs were less than 6% for visfatin and less than 9% for HMW adiponectin (23, 24). Undercarboxylated osteocalcin was assessed by a solid-phase EIA kit with intra- and interassay CVs of 8.3 and 5.2% (Glu-OC MK-118; Takara Bio Inc., Otsu, Shiga, Japan) based on a sandwich method with two monoclonal antiundercarboxylated osteocalcin antibodies.

Statistics and ethics

Statistical analyses were performed using SPSS 12.0 (SPSS Inc., Chicago, IL). Girls-boys and AGA-SGA differences were tested by unpaired t test. Birth weight and gender effects were tested by analysis of covariance. Skewed data were log transformed before comparison. Non-HMW adiponectin estimates were expressed as medians with interquartile range and compared by Mann-Whitney U test. P < 0.05 was considered significant.

The study was approved by the Institutional Review Board of Barcelona University, Hospital of Sant Joan de Déu; parental consent was an inclusion criterion.


   Results
Top
 Abstract
 Introduction
 Subjects and Methods
 Results
Discussion
 References
 
Cord insulin and IGF-I were confirmed to be gender specific in AGA newborns and were disclosed as being similarly gender specific in SGA newborns (Table 1Go). AGA newborns were gender specific for fat and lean mass but not visfatin or total or HMW adiponectin. In contrast (Table 1Go; Fig. 2Go), SGA girls and boys did not differ in body composition, but they did in visfatin and HMW adiponectin. Non-HMW adiponectin, as judged by the difference between total and HMW adiponectin concentrations, was less abundant in SGA than AGA fetuses, the estimated levels [median (interquartile range)] being, respectively, 4.7 (0.0–11.2) and 10.9 (7.0–16.4) mg/liter (P = 0.004).


View this table:
[in this window]
[in a new window]

  		TABLE 1. Results in girls and boys who were matched within a narrow range of, respectively, normal or low birth weight

 

Figure 2
View larger version (29K):
[in this window]
[in a new window]

  		FIG. 2. Effects of birth weight and gender in newborns (n = 96) who were born either AGA [n = 48, 24 boys and 24 girls (matched for birth weight)] or SGA [n = 48, 24 boys and 24 girls (matched for birth weight)]. Plots represent mean values. *, P ≤ 0.05, **, P ≤ 0.01, and ***, P ≤ 0.001 for SGA; #, P ≤ 0.05 and ##, P ≤ 0.001 for gender effects, by two-way ANOVA. Adipo, Adiponectin.

 
Neither birth weight nor gender effects were detectable for cord osteocalcin (Table 1Go) or glucose (data not shown).


   Discussion
Top
 Abstract
 Introduction
 Subjects and Methods
 Results
 Discussion
References
 
It is only recently that gender has been unmasked as a key determinant of body adiposity and endocrine homeostasis in the human fetus. Circulating insulin and IGF-I are among the fetal growth factors that are gender specific in AGA fetuses, and they were here both identified as also being gender specific in SGA fetuses (2, 3, 4, 5). Conversely, visfatin and HMW adiponectin are among the most gender-specific adipokines of prepubertal childhood (25), but their circulating levels do not appear to be gender specific in the healthy fetus at term birth (6, 7, 8, 9, 10, 11). Together, these findings indicate that one gender difference (i.e. in adiposity) may mask another (i.e. in circulating adipokines). Here this concept is corroborated by the results of visfatin and adiponectin in SGA girls and boys, who had a body composition that was no longer detectably gender specific. BMC and undercarboxylated osteocalcin were comparable in girls and boys, whether born AGA or SGA, suggesting that bone mineralization and osteoblast activity are in the fetus among those processes that are less gender specific.

An unanticipated observation in both genders was that SGA fetuses had lower levels of non-HMW adiponectin, as judged by the difference between total and HMW adiponectin. In adults, a relative or absolute shift toward HMW adiponectin is known to occur in states of low insulin activity, i.e. secondary to anorexia nervosa or to inactivating insulin receptor antibodies (26, 27). Such a shift is thought to reflect a change in the adipocytes’ secretory pattern rather than a postrelease interconversion among circulating adiponectin isoforms (28). In the SGA fetus, the shift away from non-HMW adiponectin could thus reflect a relatively depleted state of the adipocytes and/or a catabolic mode of the body. Conceivably, such a shift has a net insulin-sensitizing effect, and it may thus contribute to the hitherto poorly understood phenomenon that SGA newborns are hypersensitive to insulin during the very first days after birth (29).

Visfatin was initially thought to have insulin-mimetic properties and to be a marker of visceral fat; these thoughts, however, are currently under reappraisal (13, 14). Hypervisfatinemia may in fetal SGA girls also be a marker of adipocyte underfilling (30), and it may further amplify any insulin-sensitizing effects of the adiponectin shift toward the HMW isoform. Alternatively, given that visfatin can up-regulate insulin secretion (31), the hypervisfatinemia of fetal SGA girls may be one more endocrine way of anticipating neonatal catch-up growth.

Our findings should be interpreted with caution. By study design, the conclusions are limited to infants with a birth weight below –2 SD and those with a birth weight between –1 SD and +1 SD; the study hypothesis remains to be corroborated across a broader birth weight range. Another study limitation is that the newborns were matched independently of maternal characteristics and that some of the detected fetal-neonatal differences (especially between AGA and SGA infants) may thus partly be a reflection of maternal differences. Finally, the study population was limited to 96 infants; our main findings did reach levels of significance between P < 0.0001 and P = 0.01; minor effects, however, may have escaped detection due to lack of study power.

In conclusion, the present results indicate that prenatal weight gain is normally gender specific, yielding more fat expansion in girls than boys and, conversely, that prenatal growth restraint leads in girls to a relative fat deficit that is more marked than in boys. Cord insulin and IGF-I concentrations were gender specific, girls having higher levels than boys in the AGA and SGA subpopulation. Cord visfatin and HMW adiponectin were not gender specific in AGA fetuses (who have a gender specific adiposity) but were unmasked as gender specific in SGA fetuses (who have a less gender specific adiposity). Finally, SGA fetuses shifted their adiponectin pattern toward the HMW isoform; such a shift may be one of the survival strategies whereby SGA fetuses sensitize their body to insulin and thus prepare for neonatal catch-up growth.


   Footnotes
 
This work was supported by the Social Security Research Fund, Instituto de Salud Carlos III, Madrid, Spain (PI05/2405).

Disclosure Statement: L.I., G.S., A.L.-B., M.D., M.D.G.-R., and F.d.Z. have nothing to declare. G.S. is a predoctoral investigator of FIS, Instituto de Salud Carlos III, Madrid, Spain (FI06/00425). L.I. and M.D. are clinical investigators of Centro de Investigación Biomédica en Red sobre Diabetes y Enfermedades Metabólicas Asociadas (CIBERDEM) CB07/08/0044 (FIS, Instituto de Salud Carlos III, Madrid, Spain). A.L.-B. is an investigator of the Fund for Scientific Research "Ramon y Cajal" (Ministry of Education and Science, Spain). F.d.Z. is a clinical investigator of the Fund for Scientific Research (Flanders, Belgium).

First Published Online May 6, 2008

1 L.I. and G.S. were equal contributors to this manuscript and thus joint first authors. Back

Abbreviations: AGA, Appropriate for gestational age; BMC, bone mineral content; CV, coefficient of variation; HMW, high molecular weight; SGA, small for gestational age.

Received March 5, 2008.

Accepted April 25, 2008.


   References
Top
 Abstract
 Introduction
 Subjects and Methods
 Results
 Discussion
 References
 

  1. Hammami M, Koo WW, Hockman EM 2003 Body composition of neonates from fan beam dual energy X-ray absorptiometry measurement. J Parenter Enteral Nutr 27:423–426[Abstract/Free Full Text]
  2. Vatten LJ, Nilsen ST, Odegård RA, Romundstad PR, Austgulen R 2002 Insulin-like growth factor I and leptin in umbilical cord plasma and infant birth size at term. Pediatrics 109:1131–1135[Abstract/Free Full Text]
  3. Verkauskiene R, Beltrand J, Claris O, Chevenne D, Deghmoun S, Dorgeret S, Alison M, Gaucherand P, Sibony O, Lévy-Marchal C 2007 Impact of fetal growth restriction on body composition and hormonal status at birth in infants of small and appropriate weight for gestational age. Eur J Endocrinol 157:605–612[Abstract/Free Full Text]
  4. Shields BM, Knight B, Hopper H, Hill A, Powell RJ, Hattersley AT, Clark PM 2007 Measurement of cord insulin and insulin-related peptides suggests that girls are more insulin resistant than boys at birth. Diabetes Care 30:2661–2666[Abstract/Free Full Text]
  5. Geary MP, Pringle PJ, Rodeck CH, Kingdom JC, Hindmarsh PC 2003 Sexual dimorphism in the growth hormone and insulin-like growth factor axis at birth. J Clin Endocrinol Metab 88:3708–3714[Abstract/Free Full Text]
  6. Lindsay RS, Walker JD, Havel PJ, Hamilton BA, Calder AA, Johnstone FD; Scottish Multicentre Study of Diabetes Pregnancy 2003 Adiponectin is present in cord blood but is unrelated to birth weight. Diabetes Care 26:2244–2249[Abstract/Free Full Text]
  7. Sivan E, Mazaki-Tovi S, Pariente C, Efraty Y, Schiff E, Hemi R, Kanety H 2003 Adiponectin in human cord blood: relation to fetal birth weight and gender. J Clin Endocrinol Metab 88:5656–5660[Abstract/Free Full Text]
  8. Kajantie E, Hytinantti T, Hovi P, Andersson S 2004 Cord plasma adiponectin: a 20-fold rise between 24 weeks gestation and term. J Clin Endocrinol Metab 89:4031–4036[Abstract/Free Full Text]
  9. Odden N, Mørkrid L 2007 High molecular weight adiponectin dominates in cord blood of newborns but is unaffected by pre-eclamptic pregnancies. Clin Endocrinol (Oxf) 67:891–896[CrossRef][Medline]
  10. López-Bermejo A, de Zegher F, Díaz-Silva M, Vicente MP, Valls C, Ibáñez L 2008 Cord serum visfatin at term birth: maternal smoking unmasks the relation to foetal growth. Clin Endocrinol (Oxf) 68:77–81[Medline]
  11. Malamitsi-Puchner A, Briana DD, Gourgiotis D, Boutsikou M, Baka S, Hassiakos D 2007 Blood visfatin concentrations in normal full-term pregnancies. Acta Paediatr 96:526–529[Medline]
  12. Lara-Castro C, Fu Y, Chung BH, Garvey WT 2007 Adiponectin and the metabolic syndrome: mechanisms mediating risk for metabolic and cardiovascular disease. Curr Opin Lipidol 18:263–270[Medline]
  13. Arner P 2006 Visfatin—a true or false trail to type 2 diabetes mellitus. J Clin Endocrinol Metab 91:28–30[Free Full Text]
  14. Stephens JM, Vidal-Puig AJ 2006 An update on visfatin/pre-B cell colony-enhancing factor, an ubiquitously expressed, illusive cytokine that is regulated in obesity. Curr Opin Lipidol 17:128–131[Medline]
  15. Araki S, Dobashi K, Kubo K, Kawagoe R, Yamamoto Y, Kawada Y, Asayama K, Shirahata A 2008 Plasma visfatin concentration as a surrogate marker for visceral fat accumulation in obese children. Obesity (Silver Spring) 16:384–388[CrossRef][Medline]
  16. Sandeep S, Velmurugan K, Deepa R, Mohan V 2007 Serum visfatin in relation to visceral fat, obesity, and type 2 diabetes mellitus in Asian Indians. Metabolism 56:565–570[CrossRef][Medline]
  17. Scherer PE 2006 Adipose tissue: from lipid storage compartment to endocrine organ. Diabetes 55:1537–1545[Abstract/Free Full Text]
  18. Araki S, Dobashi K, Kubo K, Asayama K, Shirahata A 2006 High molecular weight, rather than total, adiponectin levels better reflect metabolic abnormalities associated with childhood obesity. J Clin Endocrinol Metab 91:5113–5116[Abstract/Free Full Text]
  19. Lee NK, Sowa H, Hinoi E, Ferron M, Ahn JD, Confavreux C, Dacquin R, Mee PJ, McKee MD, Jung DY, Zhang Z, Kim JK, Mauvais-Jarvis F, Ducy P, Karsenty G 2007 Endocrine regulation of energy metabolism by the skeleton. Cell 130:456–469[CrossRef][Medline]
  20. Ferrández-Longás A, Mayayo E, Labarta JI, Bagué L, Puga B, Rueda C, Ruiz-Echarri M, Labena C 2004 Estudio longitudinal de crecimiento y desarrollo. Centro Andrea Prader. Zaragoza 1980–2002. In: Garcia-Dihinx J, Romo A, Ferrández A, eds Patrones de crecimiento y desarrollo en España. Atlas de gráficas y tablas. Madrid: ERGON; 61–115
  21. Lapillonne A, Braillon P, Claris O, Chatelain PG, Delmas PD, Salle BL 1997 Body composition in appropriate and in small for gestational age infants. Acta Paediatr 86:196–200[Medline]
  22. Robinson HP, Fleming JE 1975 A critical evaluation of sonar "crown-rump length" measurements. Br J Obstet Gynaecol 82:702–710[Medline]
  23. López-Bermejo A, Petry CJ, Díaz M, Sebastiani G, de Zegher F, Dunger DB, Ibáñez L 2008 The association between the FTO gene and fat mass in humans develops within two weeks after birth. J Clin Endocrinol Metab 93:1501–1505[Abstract/Free Full Text]
  24. Ibáñez L, López-Bermejo A, Diaz M, Enríquez G, Valls C, de Zegher F 2008 Pioglitazone (7.5 mg/d) added to flutamide-metformin in women with androgen excess: additional increments of visfatin and high-molecular-weight adi-ponectin. Clin Endocrinol (Oxf) 68:317–320[Medline]
  25. Ibáñez L, López-Bermejo A, Suárez L, Marcos MV, Diaz M, de Zegher F 2008 Visceral adiposity without overweight in children born small-for-gestational-age. J Clin Endocrinol Metab 93:2079–2083[Abstract/Free Full Text]
  26. Modan-Moses D, Stein D, Pariente C, Yaroslavsky A, Ram A, Faigin M, Loewenthal R, Yissachar E, Hemi R, Kanety H 2007 Modulation of adiponectin and leptin during refeeding of female anorexia nervosa patients. J Clin Endocrinol Metab 92:1843–1847[Abstract/Free Full Text]
  27. Semple RK, Halberg NH, Burling K, Soos MA, Schraw T, Luan J, Cochran EK, Dunger DB, Wareham NJ, Scherer PE, Gorden P, O'Rahilly S 2007 Paradoxical elevation of high-molecular weight adiponectin in acquired extreme insulin resistance due to insulin receptor antibodies. Diabetes 56:1712–1717[CrossRef][Medline]
  28. Peake PW, Kriketos AD, Campbell LV, Shen Y, Charlesworth JA 2005 The metabolism of isoforms of human adiponectin: studies in human subjects and in experimental animals. Eur J Endocrinol 153:409–417[Abstract/Free Full Text]
  29. Bazaes RA, Salazar TE, Pittaluga E, Peña V, Alegría A, Iñiguez G, Ong KK, Dunger DB, Mericq MV 2003 Glucose and lipid metabolism in small for gestational age infants at 48 hours of age. Pediatrics 111:804–809[Abstract/Free Full Text]
  30. MacLaren R, Cui W, Cianflone K 2007 Visfatin expression is hormonally regulated by metabolic and sex hormones in 3T3–L1 pre-adipocytes and adipocytes. Diabetes Obes Metab 9:490–497[CrossRef][Medline]
  31. Revollo JR, Körner A, Mills KF, Satoh A, Wang T, Garten A, Dasgupta B, Sasaki Y, Wolberger C, Townsend RR, Milbrandt J, Kiess W, Imai S 2007 Nampt/PBEF/visfatin regulates insulin secretion in β cells as a systemic NAD biosynthetic enzyme. Cell Metab 6:363–375[CrossRef][Medline]



This article has been cited by other articles:


Home page
 J. Clin. Endocrinol. Metab.Home page
F. de Zegher and L. Ibanez
Early Origins of Polycystic Ovary Syndrome: Hypotheses May Change without Notice
J. Clin. Endocrinol. Metab., October 1, 2009; 94(10): 3682 - 3685.
[Full Text] [PDF]

Home page
 J. Clin. Endocrinol. Metab.Home page
S. Mazaki-Tovi, H. Kanety, C. Pariente, R. Hemi, Y. Yinon, A. Wiser, E. Schiff, and E. Sivan
Adiponectin and Leptin Concentrations in Dichorionic Twins with Discordant and Concordant Growth
J. Clin. Endocrinol. Metab., March 1, 2009; 94(3): 892 - 898.
[Abstract] [Full Text] [PDF]

Home page
 Eur J EndocrinolHome page
D. D Briana and A. Malamitsi-Puchner
Intrauterine growth restriction and adult disease: the role of adipocytokines
Eur. J. Endocrinol., March 1, 2009; 160(3): 337 - 347.
[Abstract] [Full Text] [PDF]

This Article
Right arrow Abstract Freely available
Right arrow Full Text (PDF)
Right arrow Submit a related Letter to the Editor
Right arrow Alert me when this article is cited
Right arrow Alert me when eLetters are posted
Right arrow Alert me if a correction is posted
Right arrow Citation Map
Services
Right arrow Email this article to a friend
Right arrow Similar articles in this journal
Right arrow Similar articles in PubMed
Right arrow Alert me to new issues of the journal
Right arrow Download to citation manager
Right arrow Request Copyright Permission
Citing Articles
Right arrow Citing Articles via HighWire
Right arrow Citing Articles via Google Scholar
Google Scholar
Right arrow Articles by Ibáñez, L.
Right arrow Articles by de Zegher, F.
Right arrow Search for Related Content
PubMed
Right arrow PubMed Citation
Right arrow Articles by Ibáñez, L.
Right arrow Articles by de Zegher, F.
Related Collections
Right arrow Pediatric Endocrinology
Right arrow Metabolism

HOME HELP FEEDBACK SUBSCRIPTIONS ARCHIVE SEARCH TABLE OF CONTENTS
Endocrinology Endocrine Reviews J. Clin. End. & Metab.
Molecular Endocrinology Recent Prog. Horm. Res. All Endocrine Journals