Environmental and genetic contributors to salivary testosterone levels in infants

Frontiers in Endocrinology

Volumn 5, Issue OCT, 2014, Pages

  Xia, Kai ^a   Yu, Yang ^b   Ahn, Mihye ^c   Zhu, Hongtu ^c   Zou, Fei ^c   Gilmore, John H ^a   Knickmeyer, Rebecca C ^a  

^a UNIVERSITY OF NORTH CAROLINA SCHOOL OF MEDICINE   (United States)

^b The University of North Carolina at Chapel Hill   (United States)

^c University of North Carolina at Chapel Hill   (United States)

Author keywords

APGAR; Hypothalamic pituitary gonadal axis; Infancy; LHCGR; Minipuberty; Neonate; Testosterone; Twins

Indexed keywords

CHOLESTEROL; TESTOSTERONE;

APGAR SCORE; ARTICLE; CONTROLLED STUDY; DEMOGRAPHY; DNA EXTRACTION; ENVIRONMENTAL FACTOR; ENZYME IMMUNOASSAY; FEMALE; GENE; GENETIC ASSOCIATION; GENETIC VARIABILITY; HERITABILITY; HORMONE DETERMINATION; HORMONE TRANSPORT; HUMAN; HUMAN EXPERIMENT; INFANT; LHCGR GENE; MALE; MEDICAL HISTORY; METABOLIC REGULATION; QUANTITATIVE ANALYSIS; RANDOM FOREST; SALIVA ANALYSIS; SIGNAL TRANSDUCTION; SINGLE NUCLEOTIDE POLYMORPHISM; STATISTICAL ANALYSIS; TESTOSTERONE SYNTHESIS;

EID: 84926612307     PISSN: None     EISSN: 16642392     Source Type: Journal    
DOI: 10.3389/fendo.2014.00187     Document Type: Article

References (66)

1. Forest MG, Cathiard AM. Pattern of plasma testosterone and 4-androstenedione in normal newborns: evidence for testicular activity at birth. J Clin Endocrinol Metab (1975) 41:977-80. doi:10.1210/jcem-41-5-977
2. Winter JS, Faiman C, Hobson WC, Prasad AV, Reyes FI. Pituitary-gonadal relations in infancy. I. Patterns of serum gonadotropin concentrations from birth to four years of age in man and chimpanzee. J Clin Endocrinol Metab (1975) 40(4):545-51. doi:10.1210/jcem-40-4-545
3. Forest MG, de Peretti E, Bertrand J. Testicular and adrenal androgens and their binding to plasma proteins in the perinatal period: developmental patterns of plasma testosterone, 4-androstenedione, dehydroepiandrosterone and its sulfate in premature and small for date infants as compared with that of full-term infants. J Steroid Biochem (1980) 12:25-36.
4. Kulle AE, Riepe FG, Melchior D, Hiort O, Holterhus PM. A novel ultrapressure liquid chromatography tandem mass spectrometry method for the simultaneous determination of androstenedione, testosterone, and dihydrotestosterone in pediatric blood samples: age- and sex-specific reference data. J Clin Endocrinol Metab (2010) 95(5):2399-409. doi:10.1210/jc.2009-1670
5. Kuiri-Hanninen T, Seuri R, Tyrvainen E, Turpeinen U, Hamalainen E, Stenman UH, et al. Increased activity of the hypothalamic-pituitary-testicular axis in infancy results in increased androgen action in premature boys. J Clin Endocrinol Metab (2011) 96(1):98-105. doi:10.1210/jc.2010-1359
6. Mann DR, Gould KG, Collins DC. Blockade of neonatal activation of the pituitary-testicular axis: effect on peripubertal luteinizing hormone and testosterone secretion and on testicular development in male monkeys. J Clin Endocrinol Metab (1989) 68:600-7. doi:10.1210/jcem-68-3-600
7. Brown GR, Dixson AF. Investigation of the role of postnatal testosterone in the expression of sex differences in behavior in infnats rhesus macaques (Macaca mulatta). Horm Behav (1999) 35:186-94. doi:10.1006/hbeh.1999.1512
8. Main KM, Schmidt IM, Skakkebaek NE. A possible role for reproductive hormones in newborn boys: progressive hypogonadism without the postnatal testosterone peak. J Clin Endocrinol Metab (2000) 85(12):4905-7. doi:10.1210/jcem.85.12.7058
9. Sharpe RM, Fraser HM, Brougham MF, McKinnell C, Morris KD, Kelnar CJ, et al. Role of the neonatal period of pituitary-testicular activity in germ cell proliferation and differentiation in the primate testis. Hum Reprod (2003) 18(10):2110-7. doi:10.1093/humrep/deg413
10. Zivkovic D, Fratric I. Disturbances of sperm maturation and minipuberty: is there a connection? Biomed Res Int (2014) 2014:912746. doi:10.1155/2014/912746
11. Alexander GM, Wilcox T, Farmer ME. Hormone-behavior associations in early infancy. Horm Behav (2009) 56(5):498-502. doi:10.1016/j.yhbeh.2009.08.003
12. Alexander GM, Saenz J. Postnatal testosterone levels and temperament in early infancy. Arch Sex Behav (2011) 40(6):1287-92. doi:10.1007/s10508-010-9701-5
13. Lamminmaki A, Hines M, Kuiri-Hanninen T, Kilpelainen L, Dunkel L, Sankilampi U. Testosterone measured in infancy predicts subsequent sex-typed behavior in boys and in girls. Horm Behav (2012) 61(4):611-6. doi:10.1016/j.yhbeh.2012.02.013
14. Saenz J, Alexander GM. Digit ratios (2D:4D), postnatal testosterone and eye contact in toddlers. Biol Psychol (2013) 94(1):106-8. doi:10.1016/j.biopsycho.2013.05.010
15. Saenz J, Alexander GM. Postnatal testosterone levels and disorder relevant behavior in the second year of life. Biol Psychol (2013) 94(1):152-9. doi:10.1016/j.biopsycho.2013.05.011
16. Alexander GM. Postnatal testosterone concentrations and male social development. Front Endocrinol (2014) 5:15. doi:10.3389/fendo.2014.00015
17. Harris JA, Vernon PA, Boomsma DI. The heritability of testosterone: a study of Dutch adolescent twins and their parents. Behav Genet (1998) 28:165-71. doi:10.1023/A:1021466929053
18. Sluyter F, Keijser JM, Boomsma DI, van Doornen LJ, van den Oord EJCG, Snieder H. Genetics of testosterone and the aggression-hostility-anger (AHA) syndrome: a study of middle aged twins. Twin Res (2000) 3:266-76. doi:10.1375/twin.3.4.266
19. Ring HZ, Lessov CN, Reed T, Marcus R, Holloway L, Swan GE, et al. Heritability of plasma sex hormones and hormone binding globulin in adult male twins. J Clin Endocrinol Metab (2005) 90(6):3653-8. doi:10.1210/jc.2004-1025
20. Hoekstra RA, Bartels M, Boomsma DI. Heritability of testosterone levels in 12-year-old twins and its relation to pubertal development. Twin Res Hum Genet (2006) 9(4):558-65. doi:10.1375/twin.9.4.558
21. Kuijper EA, Lambalk CB, Boomsma DI, van der Sluis S, Blankenstein MA, de Geus EJ, et al. Heritability of reproductive hormones in adult male twins. Hum Reprod (2007) 22(8):2153-9. doi:10.1093/humrep/dem145
22. Koenis MM, Brouwer RM, van Baal GC, van Soelen IL, Peper JS, van Leeuwen M, et al. Longitudinal study of hormonal and physical development in young twins. J Clin Endocrinol Metab (2013) 98(3):E518-27. doi:10.1210/jc.2012-3361
23. Harden KP, Kretsch N, Tackett JL, Tucker-Drob EM. Genetic and environmental influences on testosterone in adolescents: evidence for sex differences. Dev Psychobiol (2014) 56(6):1278-89. doi:10.1002/dev.21207
24. Ohlsson C, Wallaschofski H, Lunetta KL, Stolk L, Perry JR, Koster A, et al. Genetic determinants of serum testosterone concentrations in men. PLoS Genet (2011) 7(10):e1002313. doi:10.1371/journal.pgen.1002313
25. Jin G, Sun J, Kim ST, Feng J, Wang Z, Tao S, et al. Genome-wide association study identifies a new locus JMJD1C at 10q21 that may influence serum androgen levels in men. Hum Mol Genet (2012) 21(23):5222-8. doi:10.1093/hmg/dds361
26. Chen Z, Tao S, Gao Y, Zhang J, Hu Y, Mo L, et al. Genome-wide association study of sex hormones, gonadotropins and sex hormone-binding protein in Chinese men. J Med Genet (2013) 50(12):794-801. doi:10.1136/jmedgenet-2013-101705
27. Prescott J, Thompson DJ, Kraft P, Chanock SJ, Audley T, Brown J, et al. Genome-wide association study of circulating estradiol, testosterone, and sex hormone-binding globulin in postmenopausal women. PLoS One (2012) 7(6):e37815. doi:10.1371/journal.pone.0037815
28. Caramaschi D, Booij L, Petitclerc A, Boivin M, Tremblay RE. Genetic and environmental contributions to saliva testosterone levels in male and female infant twins. Psychoneuroendocrinology (2012) 37(12):1954-9. doi:10.1016/j.psyneuen.2012.04.008
29. Forest MG, Sizonenko PC, Cathiard AM, Bertrand J. Hypophyso-gonadal function in humans during the first year of life: I. Evidence for testicular activity in early infancy. J Clin Invest (1974) 53:819-28. doi:10.1172/JCI107621
30. Konforte D, Shea JL, Kyriakopoulou L, Colantonio D, Cohen AH, Shaw J, et al. Complex biological pattern of fertility hormones in children and adolescents: a study of healthy children from the CALIPER cohort and establishment of pediatric reference intervals. Clin Chem (2013) 59(8):1215-27. doi:10.1373/clinchem.2013.204123
31. Bidlingmaier F, Dorr HG, Eisenmenger W, Kuhnle U, Knorr D. Contribution of the adrenal gland to the production of androstenedione and testosterone during the first two years of life. J Clin Endocrinol Metab (1986) 62(2):331-5. doi:10.1210/jcem-62-2-331
32. Prince FP. The triphasic nature of Leydig cell development in humans, and comments on nomenclature. J Endocrinol (2001) 168(2):213-6. doi:10.1677/joe.0.1680213
33. Knickmeyer RC, Woolson S, Hamer RM, Konneker T, Gilmore JH. 2D:4D ratios in the first 2 years of life: stability and relation to testosterone exposure and sensitivity. Horm Behav (2011) 60(3):256-63. doi:10.1016/j.yhbeh.2011.05.009
34. Patterson N, Price AL, Reich D. Population structure and eigenanalysis. PLoS Genet (2006) 2(12):e190. doi:10.1371/journal.pgen.0020190
35. Price AL, Patterson NJ, Plenge RM, Weinblatt ME, Shadick NA, Reich D. Principal components analysis corrects for stratification in genome-wide association studies. Nat Genet (2006) 38(8):904-9. doi:10.1038/ng1847
36. Purcell S, Neale B, Todd-Brown K, Thomas L, Ferreira MA, Bender D, et al. PLINK: a tool set for whole-genome association and population-based linkage analyses. Am J Hum Genet (2007) 81(3):559-75. doi:10.1086/519795
37. Ahn M, Zhang HH, Lu W. Moment-based method for random effects selection in linear mixed models. Stat Sin (2012) 22(4):1539-62. doi:10.5705/ss.2011.054
38. Liaw A, Wiener M. Classification and regression by randomforest. R News (2002) 2(3):18-22. Available from: http://cran.r-project.org/doc/Rnews/Rnews_2002-3.pdf
39. Garagorri JM, Rodriguez G, Lario-Elboj AJ, Olivares JL, Lario-Munoz A, Orden I. Reference levels for 17-hydroxyprogesterone, 11-desoxycortisol, cortisol, testosterone, dehydroepiandrosterone sulfate and androstenedione in infants from birth to six months of age. Eur J Pediatr (2007) 167(6):647-53. doi:10.1007/s00431-007-0565-1
40. Ji C, Huang XW, Yang RW, Wang X, Zhao ZY. Gonadotropins and sex hormones in healthy Chinese infants. Indian Pediatr (2008) 45(6):489-92. Available from: http://indianpediatrics.net/june2008/june-489-492.htm
41. Granger DA, Cicchetti D, Rogosch FA, Hibel LC, Teisl M, Flores E. Blood contamination in children's saliva: prevalence, stability, and impact on the measurement of salivary cortisol, testosterone, and dehydroepiandrosterone. Psychoneuroendocrinology (2007) 32(6):724-33. doi:10.1016/j.psyneuen.2007.05.003
42. Apgar V. A proposal for a new method of evaluation of the newborn infant. Curr Res Anesth Analg (1953) 32(4):260-7. doi:10.1213/00000539-195301000-00041
43. AAP ACOG. The Apgar score. Pediatrics (2006) 117(4):1444-7. doi:10.1542/peds.2006-0325
44. Li J, Cnattingus S, Gissler M, Vestergaard M, Obel C, Ahrensberg J, et al. The 5-minute Apgar score as a predictor of childhood cancer: a population-based cohort study in five million children. BMJ Open (2012) 2(4):e001095. doi:10.1136/bmjopen-2012-001095
45. Velazquez-Moctezuma J, Dominguez Salazar E, Cruz Rueda ML. The effect of prenatal stress on adult sexual behavior in rats depends on the nature of the stressor. Physiol Behav (1993) 53(3):443-8. doi:10.1016/0031-9384(93)90137-5
46. Wang CT, Huang RL, Tai MY, Tsai YF, Peng MT. Dopamine release in the nucleus accumbens during sexual behavior in prenatally stressed adult male rats. Neurosci Lett (1995) 200(1):29-32. doi:10.1016/0304-3940(95)12071-B
47. Rhees RW, Al-Saleh HN, Kinghorn EW, Fleming DE, Lephart ED. Relationship between sexual behavior and sexually dimorphic structures in the anterior hypothalamus in control and prenatally stressed male rats. Brain Res Bull (1999) 50(3):193-9. doi:10.1016/S0361-9230(99)00191-4
48. Ward IL, Ward OB, Hayden T, Weisz J, Orth JM. Naltrexone normalizes the suppression but not the surge of delta 5-3 beta-hydroxysteroid dehydrogenase activity in Leydig cells of stressed rat fetuses. Endocrinology (1990) 127(1):88-92. doi:10.1210/endo-127-1-88
49. Ward IL, Ward OB, Affuso JD, Long WD III, French JA, Hendricks SE. Fetal testosterone surge: specific modulations induced in male rats by maternal stress and/or alcohol consumption. Horm Behav (2003) 43(5):531-9. doi:10.1016/S0018-506X(03)00061-8
50. Pallares ME, Adrover E, Baier CJ, Bourguignon NS, Monteleone MC, Brocco MA, et al. Prenatal maternal restraint stress exposure alters the reproductive hormone profile and testis development of the rat male offspring. Stress (2013) 16(4):429-40. doi:10.3109/10253890.2012.761195
51. Shirtcliff EA, Granger DA, Likos A. Gender differences in the validity of testosterone measured in saliva by immunoassay. Horm Behav (2002) 42(1):62-9. doi:10.1006/hbeh.2002.1798
52. Visscher PM, Hill WG, Wray NR. Heritability in the genomics era-concepts and misconceptions. Nat Rev Genet (2008) 9(4):255-66. doi:10.1038/nrg2322
53. Johnson W, Penke L, Spinath FM. Heritability in the era of molecular genetics: some thoughts for understanding genetic influences on behavioral traits. Eur J Pers (2011) 25(4):254-66. doi:10.1002/per.834
54. Miller WL, Auchus RJ. The molecular biology, biochemistry, and physiology of human steroidogenesis and its disorders. Endocr Rev (2011) 32(1):81-151. doi:10.1210/er.2010-0013
55. Yang JA, Benyamin B, McEvoy BP, Gordon S, Henders AK, Nyholt DR, et al. Common SNPs explain a large proportion of the heritability for human height. Nat Genet (2010) 42(7):565-U131. doi:10.1038/ng.608
56. Visscher PM, Goddard ME, Derks EM, Wray NR. Evidence-based psychiatric genetics, AKA the false dichotomy between common and rare variant hypotheses. Mol Psychiatry (2012) 17(5):474-85. doi:10.1038/mp.2011.65
57. Safran M, Chalifa-Caspi V, Shmueli O, Olender T, Lapidot M, Rosen N, et al. Human gene-centric databases at the weizmann institute of science: genecards, UDB, CroW 21 and HORDE. Nucleic Acids Res (2003) 31(1):142-6. doi:10.1093/nar/gkg050
58. Sherry ST, Ward MH, Kholodov M, Baker J, Phan L, Smigielski EM, et al. dbSNP: the NCBI database of genetic variation. Nucleic Acids Res (2001) 29(1):308-11. doi:10.1093/nar/29.1.308
59. Karolchik DM, Barber GP, Clawson H, Cline MS, Diekhans M, Dreszer TR, et al. The UCSC Genome Browser database: 2014 update. Nucelic Acids Res (2014) 42:D764-70. doi:10.1093/nar/gkt1168
60. Goodarzi MO, Antoine HJ, Azziz R. Genes for enzymes regulating dehydroepiandrosterone sulfonation are associated with levels of dehydroepiandrosterone sulfate in polycystic ovary syndrome. J Clin Endocrinol Metab (2007) 92(7):2659-64. doi:10.1210/jc.2006-2600
61. Groschl M. Current status of salivary hormone analysis. Clin Chem (2008) 54(11):1759-69. doi:10.1373/clinchem.2008.108910
62. Baxendale PM, Reed MJ, James VHT. Testosterone in saliva of normal men and its relationship with unbound and total testosterone levels in plasma. J Endocrinol (1980) 4:46-7.
63. Vittek J, L'Hommedieu DG, Gordon GG, Rappaport SC, Southren AL. Direct radioimmunoassay (RIA) of salivary testosterone: correlation with free and total serum testosterone. Life Sci (1985) 37(8):711-6. doi:10.1016/0024-3205(85)90540-5
64. Navarro MA, Juan L, Bonnin MR, Villabona C. Salivary testosterone: relationship to total and free testosterone in serum. Clin Chem (1986) 32(1 Pt 1):231-2.
65. Magrini G, Chiodoni G, Rey F, Felber JP. Further evidence for the usefulness of the salivary testosterone radioimmunoassay in the assessment of androgenicity in man in basal and stimulated conditions. Horm Res (1986) 23(2):65-73. doi:10.1159/000180291
66. Schwartz EB, Granger DA. Transferrin enzyme immunoassay for quantitative monitoring of blood contamination in saliva. Clin Chem (2004) 50(3):654-6. doi:10.1373/clinchem.2003.028266