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Reported early family environment covaries with menarcheal age as a function of polymorphic variation in estrogen receptor-α

  • Stephen B. Manuck (a1), Anna E. Craig (a1), Janine D. Flory (a2), Indrani Halder (a1) and Robert E. Ferrell (a1)...
Abstract
Abstract

Age at menarche, a sentinel index of pubertal maturation, was examined in relation to early family relationships (conflict, cohesion) and polymorphic variation in the gene encoding estrogen receptor-α (ESR1) in a midlife sample of 455 European American women. Consistent with prior literature, women who reported being raised in families characterized by close interpersonal relationships and little conflict tended to reach menarche at a later age than participants reared in families lacking cohesion and prone to discord. Moreover, this association was moderated by ESR1 variation, such that quality of the family environment covaried positively with menarcheal age among participants homozygous for minor alleles of the two ESR1 polymorphisms studied here (rs9304799, rs2234693), but not among women of other ESR1 genotypes. In addition, (a) family relationship variables were unrelated to ESR1 variation, and (b) genotype-dependent effects of childhood environment on age at menarche could not be accounted for by personality traits elsewhere shown to explain heritable variation in reported family conflict and cohesion. These findings are consistent with theories of differential susceptibility to environmental influence, as well as the more specific hypothesis (by Belsky) that girls differ genetically in their sensitivity to rearing effects on pubertal maturation.

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Address correspondence and reprint requests to: Stephen B. Manuck, Behavioral Physiology Laboratory, University of Pittsburgh, 506 OEH, 4015 O'Hara Street, Pittsburgh, PA 15260; E-mail: manuck@pitt.edu.
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S. E. Anderson , G. E. Dallal , & A. Must (2003). Relative weight and race influence average age at menarche: Results from two nationally representative surveys of US girls studied 25 years apart. Pediatrics, 111, 844850.

D. Apter , & R. Vihko (1983). Early menarche, a risk factor for breast cancer, indicates early onset of ovulatory cycles. Journal of Clinical Endocrinology and Metabolism, 57, 8286.

I. Attie , & J. Brooks-Gunn (1989). Development of eating problems in adolescent girls. Developmental Psychology, 25, 7079.

J. Belsky (1997). Variation in susceptibility to rearing influences: An evolutionary argument. Psychological Inquiry, 8, 182186.

J. Belsky (2000). Conditional and alternative reproductive stragegies: Individual differences in susceptibility to rearing experience. In J. L. Rodgers , D. C. Rowe , & W. B. Miller (Eds.), Genetic influences on human fertility and sexuality: Theoretical and empirical contributions from biological and behavioral sciences (pp. 127146). Boston: Kluwer Academic.

J. Belsky , M. J. Bakermans-Kranenburg , & M. H. van IJzendoorn (2007). For better and for worse: Differential susceptibility to environmental influences. Current Directions in Psychological Science, 16, 300304.

J. Belsky , & M. Pluess (2009). Beyond diathesis stress: Differential susceptibility to environmental influences. Psychological Bulletin, 135, 885908.

J. Belsky , L. Steinberg , & P. Draper (1991). Childhood experience, interpersonal development, and reproductive strategy: An evolutionary theory of socialization. Child Development, 62, 647670.

J. Belsky , L. D. Steinberg , R. M. Houts , S. L. Friedman , G. DeHart , E. Cauffman , (2007). Family rearing antecedents of pubertal timing. Child Development, 78, 13021321.

A. Bergsten-Brucefors (1976). A note on the accuracy of recalled age at menarche. Annals of Human Biology, 3, 7173.

L. Bernstein (2002). Epidemiology of endocrine-related risk factors for breast cancer. Journal of Mammary Gland Biology and Neoplasia, 7, 315.

M. E. Bleil , P. J. Gianaros , J. R. Jennings , J. D. Flory , & S. B. Manuck (2008). Trait negative affect: toward an intergrated model of understanding psychological risk for impairment in cardiac autonomic function. Psychosomatic Medicine, 70, 328337.

A. M. Boot , I. M. van Der Sluis , S. M. P .F. de Muinck Keizer-Schrama , J. B. J. van Meurs , E. P. Krenning , (2004). Estrogen receptor α gene polymorphisms and bone mineral density in health children and young adults. Calcified Tissue International, 74, 495500.

J. Brooks-Gunn , & M. P. Warren (1988). Mother–daughter differences in menarcheal age in adolescent girls attending national dance company schools and non-dancers. Annals of Human Biology, 15, 3544.

A. Caspi , J. McClay , T. E. Moffitt , J. Mill , & J. Martin , I. W. Craig , (2002). Role of genotype in the cycle of violence in maltreated children. Science, 297, 851854.

A. Caspi , & T. E. Moffitt (1991). Individual differences are accentuated during periods of social change: The sample case of girls at puberty. Journal of Personality and Social Psychology, 61, 157168.

A. Caspi , K. Sugden , T. E. Moffitt , A. Taylor , I. W. Craig , H. Harrington (2003). Influence of life stress on depression: Moderation by a polymorphism in the 5-HTT gene. Science, 301, 386389.

A. Caspi , B. Williams , J. Kim-Cohen , I. W. Craig , B. J. Milne , R. Poulton , (2007). Moderationof breastfeeding effects on IQ by genetic variation in fatty acid metabolism. Proceedings of the National Academy of Science of the United States of America, 104, 1886018865.

A. Castagnoli , I. Maestri , F. Bernardi , & L. Del Senno (1987). PvuII inside the human estrogen receptor gene. Nucleic Acids Research, 15, 866.

D. Cicchetti , F. A. Rogosch , & M. L. Sturge-Apple (2007). Interactions of child maltreatment and serotonin transporter and monoamine oxidase A polymorphisms: Depressive symptomatology among adolescents from low socioeconomic status backgrounds. Development and Psychopathology, 19, 11611180.

J. S. Chisholm , & V. K. Burbank (2001). Evolution and inequality. International Epidemiological Association, 30, 206211.

D. E. Comings , D. Muhleman , J. P. Johnson , & J. P. MacMurray (2002). Parent–daughter transmission of the androgen receptor gene as an explanation of the effect of father absence on age of menarche. Child Development, 73, 10461051.

G. S. Cooper , S. A. Ephross , C. R. Weinberg , D. D. Baird , E. A. Whelan , & D. P. Sandler (1999). Menstrual and reproductive risk factors for ischemic heart disease. Epidemiology, 10, 255259.

J. Deardorff , N. A. Gonzales , F. S. Christopher , M. W. Roosa , & R. E. Millsap (2005). Early puberty and adolescent pregnancy: The influence of alcohol use. Pediatrics, 116, 14511456.

K. Deater-Deckard , D. W. Fulker , & R. Plomin (1999). A genetic study of the family environment in the transition to early adolescence. Journal of Child Psychology and Psychiatry, 40, 769775.

S. A. DiVall , & S. Radovick (2008). Pubertal development and menarche. Annals of the New York Academy of Sciences, 1135, 1928.

S. A. DiVall , & S. Radovick (2009). Endocrinology of female puberty. Current Opinion in Endocrinology, Diabetes and Obesity, 16, 14.

D. Doughty , & J. L. Rodgers (2000). Behavior genetic modeling of menarche in U.S. females. In J. L. Rodgers , D. C. Rowe , & W. B. Miller (Eds.), Genetic influences on human fertility and sexuality (pp. 169182). Boston: Kluwer Academic.

J. Dunbar , J. Sheeder , D. Lezotte , D. Dabelea , & C. Stevens-Siimon (2008). Age at menarche and first pregnancy among psychosically at-risk adolescents. American Journal of Public Health, 98, 18221824.

B. J. Ellis (2004). Timing of pubertal maturation in girls: An integrated life history approach. Psychological Bulletin, 130, 920958.

B. J. Ellis , & M. J. Essex (2007). Family environments, adrenarche, and sexual maturation: A longitudinal test of a life history model. Child Development, 78, 17991817.

B. J. Ellis , & J. Garber (2000). Psychosocial antecedents of variation in girls' pubertal timing: Maternal depression, stepfather presences, and marital and family stress. Child Development, 71, 485501.

B. J. Ellis , J. J. Jackson , & W. T. Boyce (2006). The stress response systems: Universality and adaptive individual differences. Developmental Review, 26, 175212.

B. J. Ellis , S. McFadyen-Ketchum , K. A. Dodge , G. S. Pettit , & J. E. Bates (1999). Quality of early family relationships and individual differences in the timing of pubertal maturation in girls: A longitudinal test of an evolutionary model. Journal of Personality and Social Psychology, 77, 387401.

X. Ge , R. D. Conger , & G. H. Elder (1996). Coming of age too early: Pubertal influences on girls' vulnerability to psychological distress. Child Development, 67, 33863400.

M. S. Golub , G. W. Collman , P. M. D. Foster , C. A. Kimmel , E. Rajpert-De Meyts , E. O. Reiter , (2008). Public health implications of altered puberty timing. Pediatrics, 121, S218S230.

I. Gorai , K. Tanake , M.. Inada , H. Morinaga , Uchiyama, R. Kikuchi , (2003). Estrogen-metabolizing gene polymorphisms, but not estrogen receptor-α gene polymorphisms, are associated with the onset of menarche in health postmenopausal Japanese women. Journal of Clinical Endocrinology and Metabolism, 88, 799803.

J. A. Graber , J. Brooks-Gunn , & M. P. Warren (1995). The antecedents of menarcheal age: Heredity, family environment, and stressful life events. Child Development, 66, 346359.

J. A. Graber , P. M. Lewinsohn , J. R. Seeley , & J. Brooks-Gunn (1997). Is psychopathology associated with the timing of pubertal development? Journal of the American Academy of Child & Adolescent Psychiatry, 36, 17681776.

J. A. Graber , J. R. Seeley , J. Brooks-Gunn , & P. M. Lewinsohn (2004). Is pubertal timing associated with psychopathology in young adulthood? Journal of the American Academy of Child & Adolescent Psychiatry, 43, 718726.

I. Halder , A. L. Marsland , J. Cheong , M. F. Muldoon , R. E. Ferrell , & S. B. Manuck (2010). Polymorphisms in the CRP gene moderate an association between depressive symptoms and circulating levels of C-reactive protein. Brain, Behavior, and Immunity, 24, 160167.

I. Halder , M. F. Muldoon , R. E. Ferrell , & S. B. Manuck (2007). Serotonin receptor 2A (HTR2A) gene polymorphisms are associated with blood pressure, central adiposity, and the metabolic syndrome. Metabolic Syndrome and Related Disorders, 5, 323330.

D. M. Herrington , T. D. Howard , B. Brosnihan , D. P. McDonnell , X. Li , G. A. Hawkins , (2002). Common estrogen receptor polymorphism augments effects of hormone replacement therapy on E-selectin but not C-reactive protein. Circulation, 105, 18791882.

S. Hoier (2003). Father absence and age at menarche. Human Nature, 14, 209233.

C.-C. Hsieh , D. Trichopoulos , K. Katsouyanni , & S. Yuasa (1990). Age at menarche, age at menopause, height and obesity as risk factors for breast cancer: Associations and interactions in an international case–control study. International Journal of Cancer, 46, 796800.

B. K. Jacobsen , K. Oda , S. F. Knutsen , & G. E. Fraser (2009). Age at menarche, total mortality and mortality from ischaemic heart disease and stroke: the Adventist Health Study, 1976–88. International Journal of Epidemiology, 38, 245252.

K. C. Jacobson , & D. C. Rowe (1999). Genetic and environmental influences on the relationships between family connectedness, school connectedness, and adolescent depressed mood: Sex differences. Developmental Psychology, 35, 926939.

K. L. Jang , P. A. Vernon , W. J. Liveley , M. B. Stein , & H. Wolf (2001). Intra- and extra-familial influences on alcohol and drug misuse: A twin study of gene–environment correlation. Addiction, 96, 13071318.

A. F. Jorm , Rodgers Christensen , B., P. A. Jacomb , & S. Easteal (2004). Association of adverse childhood experiences, age of menarche, and adult reproductive behavior: Does the androgen receptor gene play a role? American Journal of Medical Genetics, 125B, 105111.

R. Kaltiala-Heino , E. Kosunen , & M. Rimpela (2003). Pubertal timing, sexual behavior and self-reported depression in middle adolescence. Journal of Adolescence, 26, 531545.

R. Kaltiala-Heino , M. Marttunen , P. Rantanen , & M. Rimpela (2003). Early puberty is associated with mental health problems in middle adolescence. Social Science and Medicine, 57, 10551064.

R. Kaltiala-Heino , M. Rimpel , A. Rissanen , & P. Rentanen (2001). Early puberty and early sexual activity are associated with bulimic-type eating pathology in middle adolescence. Journal of Adolescent Health, 28, 346352.

K. Kim , & P. K. Smith (1998). Retrospective survey of parental marital relations and child reproductive development. International Journal of Behavioral Development, 22, 729751.

K. Kim , P. K. Smith , & A.-L. Palermiti (1997). Conflict I childhood and reproductive development. Evolution and Human Behavior, 18, 109142.

K. M. Kirk , S. P. Blomberg , D. L. Duffy , A. C. Health , I. P. F. Owens , & N. G. Martin (2001). Natural selection and quantitative genetics of life-history traits in western women: A twin study. Evolution, 55, 423435.

C. Koprowski , R. J. Coates , & L. Bernstein (2001). Ability of young women to recall past body size and age at menarche. Obesity Research, 9, 478485.

K. L. Kramer (2008). Early sexual maturity among Pume foragers of Venezuela: Fitness implications of teen motherhood. American Journal of Physical Anthropology, 136, 338350.

R. F. Krueger , K. E. Markon , & T. J. Bouchard (2003). The extended genotype: The heritability of personality accounts for the heritability of recalled family environments in twins reared apart. Journal of Personality, 71, 809833.

T. A. Kunnas , P. Laipala , A. Pentilla , T. Lehtmaki , & P. J. Karhunen (2000). Association of polymorphism of human α oestrogen receptor gene with coronary artery disease in men: A necropsy study. British Medical Journal, 321, 273274.

R. Lakshman , N. G. Forouhi , S. J. Sharp , R. Luben , S. A. Bingham , K.-T. Khaw , (2009). Early age at menarche associated with cardiovascular disease and mortality. Journal of Clinical Endocrinology and Metabolism, 94, 49535960.

T. H. Lam , H. J. Shi , L. M. Ho , S. M. Stewart , & S. Fan (2002). Timing of pubertal maturation and heterosexual behavior among Hong Kong Chinese adolescents. Archives of Sexual Behavior, 31, 359366.

W. D. Lassek , & S. J. Gaulin (2007). Menarche Is related to fat distribution. American Journal of Physical Anthropology, 133, 11471151.

T. Lehtimaki , T. W. Kunnas , K. M. Mattila , M. Perola , A. Penttila , T. Koivula , (2002). Coronary artery wall atherosclerosis in relation to the estrogen receptor 1 gene polymorphism: An autopsy study. Journal of Molecular Medicine, 80, 176180.

J.-R. Long , H. Xu , L.-J. Zhao , P.-Y. Liu , H. Shen , Y.-J. Liu , (2005). The oestrogen receptor α gene is linked and/or associated with age at menarche in different ethnic groups. Journal of Medical Genetics, 42, 796800.

D. Maestripieri , J. R. Roney , N. DeBias , K. M. Durante , & G. M. Spaepen (2004). Father absence, menarche and interest in infants among adolescent girls. Developmental Science, 7, 560566.

S. B. Manuck (1994). Cardiovascular reactivity in cardiovascular disease. International Journal of Behavioral Medicine, 1, 431.

S. B. Manuck (2010). The reaction norm in Gene × Environment interaction. Molecular Psychiatry, 15, 881882.

S. B. Manuck , A. L. Marsland , J. R. Kaplan , & J. K. Williams (1995). The pathogenicity of behavior and its neuroendocrine mediation: An example from coronary artery disease. Psychosomatic Medicine, 57, 275283.

S. B. Manuck , J. E. Phillips , P. J. Gianaros , J. D. Flory , & M. F. Muldoon (2010). Subjective socioeconomic status and presence of the in midlife community volunteers. Psychosomatic Medicine, 72, 3545.

L. M. Marshall , D. Spiegelman , M. B. Goldman , J. E. Manson , G. A. Colditz , R. L. Barbieri , (1998). A prospective study of reproductive factors and oral contraceptive use in relation to risk of uterine leiomyomata. Fertility and Sterility, 70, 432439.

N. Mendoza , F. J. Moron , F. Quereda , F. Vazquez , M. C. Rivero , T. Martinez-Astorquiza , (2008). A digenic combination of polymorphisms within ESR1 and ESR2 genes are associated with age at menarche in the Spanish population. Reproductive Sciences, 15, 305311.

A. C. Mezzich , R. E. Tarter , P. R. Giancola , S. Lu , L. Kirisci , & S. Parks (1997). Substance use and risky sexual behavior in female adolescents. Drug and Alcohol Dependence, 44, 157166.

B.C. Miller , M. C. Norton , T. Curtis , E. J. Hill , P. Schvaneveldt , & M. H. Young (1997). The timing of sexual intercourse among adolescents: Family, peer, and other antecedents. Youth and Society, 29, 5466.

F. Modugno , J. M. Zmuda , D. Potter , C. Cai , E. Ziv , S. R. Cummings , (2005). Association of estrogen receptor α polymorphisms with breast cancer risk in older Caucasian women. International Journal of Cancer, 116, 984991.

T. E. Moffitt , A. Caspi , J. Belsky , & P. A. Silva (1992). Childhood experience and the onset of menarche: A test of a sociobiological model. Child Development, 63, 4758.

A. Must , S. M. Phillips , E. N. Naumova , M. Blum , S. Harris , B. Dawson-Hughes , (2002). Recall of early menstrual history and menarcheal body size: After 30 years, how well do women remember? American Journal of Epidemiology, 155, 672679.

N. C. Onland-Moret , C. H. van Gils , M. Roest , D. E. Grobbee , & P. H. M. Peeters (2005). The estrogen receptor α gene and breast cancer risk (The Netherlands). Cancer Causes and Control, 16, 11951202.

C. J. Patrick , J. J. Curtin , & A. Tellegen (2002). Development and validation of a brief form of the Multidimensional Personality Questionnaire. Psychological Assessment, 14, 150163.

R. Plomin , G. E. McClearn , N. L. Pedersen , J. R. Nesselroade , & C. S. Bergeman (1988). Genetic influence on childhood family environment perceived retrospectively from the last half of the life span. Developmental Psychology, 24, 738745.

R. Plomin , G. E. McClearn , N. Pedersen , J. R. Nesselroade , & C. S. Bergeman (1989). Genetic influence on adult's ratings of their current family environment. Journal of Marriage and the Family, 51, 791803.

R. J. Quinlan (2003). Father absence, parental care, and female reproductive development. Evolution and Human Behavior, 24, 376390.

K. E. Remsberg , E. W. Demerath , C. M. Schubert , W. C. Chumlea , S. S. Sun , & R. M. Siervogel (2005). Early menarche and the development of cardiovascular risk factors in adolescent girls: The Fels Longitudinal Study. Journal of Clinical Endocrinology and Metabolism, 90, 27182724.

D. C. Rowe (2000). Environmental and genetic influences on pubertal development: Evolutionary life history traits. In J. L. Rodgers , D. C. Rowe , & W. B. Miller (Eds.), Genetic influences on human fertility and sexuality (pp. 147168). Boston: Kluwer Academic.

K. J. Saudino (2005). Behavioral genetics and child temperatment. Developmental and Behavioral Pediatrics, 26, 214223.

S. C. E. Schuit , H.-H. S. Oei , J. C. M. Witteman , C. H. G. van Kessel , J. B. J. van Meurs , R. L. Nijhuis , (2004). Estrogen receptor α gene polymorphisms and risk of myocardial infarction. Journal of the American Medical Association, 291, 29692977.

A. M. Shearman , L. A. Cupples , S. Demissie , I. Peter , C. H. Schmid , R. H. Karas , (2003). Association between estrogen receptor alpha gene variation and cardiovascular disease. Journal of the American Medical Association, 290, 22632270.

A. Shin , D. Kang , H. Nishio , J. L. Lee , S. K. Park , S.-U. Kim , (2003). Estrogen receptor alpha gene polymorphisms and breast cancer risk. Breast Cancer Research and Treatment, 80, 127131.

R. K. Silbereisen , A. C. Petersen , H. T. Albrecht , & B. Kracke (1989). Maturational timing and the development of problem behavior. Journal of Early Adolescence, 9, 247268.

D. M. Sloboda , R. Hart , D. A. Doherty , C. E. Pennell , & M. Hickey (2007). Age at menarche: Influences of prenatal and postnatal growth. Journal of Clinical Endocrinology and Metabolism, 92, 4650.

J. T. Smith , D. K. Clifton , & R. A. Steiner (2006). Regulation of the neuroendocrine reproductive axis by kisspeptin-GPR54 signaling. Reproduction, 131, 623630.

H. Snieder , A. J. MacGregor , & T. D. Spector (1998). Genes control the cessation of a woman's reproductive life: A twin study of hysterectorm and age at menopause. Journal of Clinical Endocrinology and Metabolism, 83, 18751880.

I. Stavrou , C. Zois , J. P. A. Ioannidis , & A. Tsatsoulis (2002). Association of polymorphisms of the estrogen receptor α gene with age of menarche. Human Reproduction, 17, 11011105.

L. Steinberg (1988). Reciprocal relation between parent–child distance and pubertal maturation. Developmental Psychology, 24, 122128.

E. Stice , K. Presnell , & S. K. Bearman (2001). Relation of early menarche to depression, eating disorders, substance abuse, and comorbid psychopathology among adolescent girls. Developmental Psychology, 37, 608619.

B. Towne , S. A. Czerwinski , E. W. Demerath , J. Blangero , A. F. Roche , & R. M. Siervogel (2004). Heritability of age at menarche in girls from the Fels Longitudinal Study. American Journal of Physical Anthropology, 128, 210219.

S. Wedren , L. Lovmar , K. Humphreys , C. Magnusson , H. Melhus , A.-C. Syvanen , (2004). Oestrogen receptor α gene haplotype and postmenopausal breast cancer risk: A case control study. Breast Cancer Research, 6, R437R449.

A. E. A. M. Weel , A. G. Uitterlinden , I. C. D. Westendorp , H. Burger , S. C. E. Schuit , A. Hofman , (1999). Estrogen receptor polymorphism predicts the onset of natural and surgical menopause. Journal of Clinical Endocrinology and Metabolism, 84, 31463150.

H. Xu , J.-R. Long , M.-X. Li , & H.-W. Deng (2005). Interaction effects between estrogen receptor α and vitamin D receptor genes on age at menarche Chinese women. Acta Pharmacologica Sinica, 26, 860864.

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