Cited by 165Hypothalamic control of reproductive hormonesReproductive Biology and FertilitySexual Differentiation and Disorders

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Genetic Influences on the Timing of Puberty in Mice1

Nelson, James F., Karelus, Katarzyna, Felicio, Lêda S., Johnson, Thomas E.·1990·Biology of Reproduction

DOI 10.1095/biolreprod42.4.649

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Abstract

Genetic influences on the timing of three pubertal events--vaginal opening, first vaginal cornification, and onset of cyclicity--were studied in C57BL/6J, DBA/2J, and C3H/HeJ mice and in two F1 hybrid strains (B6D2F1 and B6C3HF1). Marked genotypic differences were found. Among inbred strains, differences in the onset of vaginal opening and first vaginal cornification (C3H less than DBA less than C57) did not parallel those for the onset of cyclicity (C3H much greater than DBA = C57). Compared to parental strains, F1 hybrid strains were intermediate for times of vaginal opening and first vaginal cornification, consistent with the model in which the genetic effects on the timing of these events are additive. By contrast, onset of cyclicity occurred significantly earlier in the F1 hybrids than in their parent strains, indicating heterosis for one or more genes specifying this event. Body weights also differed among the genotypes from weaning onward, but these differences were only partially correlated with the differences in the timing of the pubertal events. Thus, genetic influences other than those affecting body weight contribute to the differential timing of pubertal events in these mouse strains. These results reveal marked genetic variation in the timing of puberty, and indicate that the set of genes specifying the timing of vaginal opening and first vaginal cornification differs from those specifying the onset of cyclicity.

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Crossref · 10.1095/biolreprod42.4.649

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MethodInfluential
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BackgroundMethod
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Asynchronous embryonic germ cell development leads to a heterogeneity of postnatal ovarian follicle activation and may influence the timing of puberty onset in mice
Dai, Y., Bo, Y., Wang, P., Xu, X., Singh, M., Jia, L., Zhang, S., Niu, S., Cheng, K., Liang, J., et al. (2022) · BMC Biology · doi:10.1186/s12915-022-01318-y · Cited by 30
“Since each individual in one inbred strain shares stable genetic background [31, 32], which is like the family study in clinics, our result strongly suggests that the profile of embryonic germ cells development could affect the postnatal puberty onset in humans.”
MethodResultInfluential
Effects of maternal nuclear genome on the timing of puberty in mice offspring
Zhou, Y., Zhu, W., Guo, Z., Zhao, Y., Song, Z., & Xiao, J. (2007) · Journal of Endocrinology · doi:10.1677/joe.1.07049 · Cited by 28
“In order to investigate the potential effects of the maternal genomic background on the timing of puberty in the progeny, two inbred strains of mice (C3H/HeJ and C57BL/6J) were used to produce two pedigrees (direct and reciprocal crosses) because the female individuals differ significantly from each other in the timin…”
MethodInfluential
Sex-specific effects of chronic anabolic androgenic steroid treatment on GABAA receptor expression and function in adolescent mice
Penatti, C. A. A., Porter, D. M., Jones, B., & Henderson, L. (2005) · Neuroscience · doi:10.1016/j.neuroscience.2005.06.041 · Cited by 28
Betacellulin Overexpression in the Mouse Ovary Leads to MAPK3/MAPK1 Hyperactivation and Reduces Litter Size by Impairing Fertilization1
Gratão, A. A., Dahlhoff, M., Sinowatz, F., Wolf, E., & Schneider, M. R. (2007) · Biology of Reproduction · doi:10.1095/biolreprod.107.062588 · Cited by 27
“Importantly, starting with the third cycle, the mean cycle length in both groups was shorter than 6 days in duration, the maximal cycle length considered normal for different mouse strains [24].”
Background
Short-Term High-Fat Diet Increases Leptin Activation of CART Neurons and Advances Puberty in Female Mice
Venancio-Brochi, J. C., Margatho, L. O., Rorato, R. C., Costa, R. R., Debarba, L. K., Coletti, R., Antunes‐Rodrigues, J., Elias, C. F., & Elias, L. L. K. (2017) · Endocrinology · doi:10.1210/en.2017-00452 · Cited by 25
A Short-Day Photoperiod Delays the Timing of Puberty in Female Mice via Changes in the Kisspeptin System
Bohlen, T. M., Silveira, M. A., Buonfiglio, D. D. C., Ferreira‐Neto, H. C., Cipolla‐Neto, J., Donato, J., & Frazão, R. (2018) · Frontiers in Endocrinology · doi:10.3389/fendo.2018.00044 · Cited by 25
“Sexual maturation was determined by the age at vaginal opening, assessed through the first occurrence of vaginal cornification in the vaginal lavage (first estrus) and the onset of cyclicity, which is the first occurrence of an estrous cycle of typical duration (4–7 days in mice), as previously described (22, 23).”
Method
A battery of olfactory-based screens for phenotyping the social and sexual behaviors of mice
Ferkin, M. H., & Li, H. (2005) · Physiology & Behavior · doi:10.1016/j.physbeh.2005.05.014 · Cited by 25
“Typically, female mice exhibit 4- to 5-day estrous cycles that can be divided into 4 phases—proestrus, estrus, metestrus, and diestrus [6,44,52].”
Background
Brain Region-Specific Regulation of Urocortin 1 Innervation and Corticotropin-Releasing Factor Receptor Type 2 Binding by Ethanol Exposure
Weitemier, A. Z., & Ryabinin, A. E. (2005) · Alcoholism Clinical and Experimental Research · doi:10.1097/01.alc.0000179363.44542.05 · Cited by 24
“Two-way ANOVA detected differences in basal weight between strains, as was shown previously (Nelson et al., 1990) (F1, 41 " 4.”
Method
The last stage of development: The restructuring and plasticity of the cortex during adolescence especially at puberty
Juraska, J. M. (2024) · Developmental Psychobiology · doi:10.1002/dev.22468 · Cited by 29
Partial normalization of pubertal timing in female mice with DSS colitis treated with anti-TNF-α antibody
DeBoer, M. D., Steinman, J. R., & Li, Y. (2012) · Journal of Gastroenterology · doi:10.1007/s00535-012-0542-y · Cited by 22
“While estradiol measurements in mice at pubertal age are at or below the limit of detection even in untreated controls [16], a validated measure of puberty in female mice is the physical examination feature of vaginal opening [9, 20], which occurred earlier in the DSS ? TNF-a ab group compared to the DSS ? Control ab…”
Background
Scientific and Regulatory Policy Committee Best Practices: Documentation of Sexual Maturity by Microscopic Evaluation in Nonclinical Safety Studies
Vidal, J. D., Colman, K. A., Bhaskaran, M., et al. (2021) · Toxicologic Pathology · doi:10.1177/0192623321990631 · Cited by 19
“In mice, the time between vaginal opening and first estrus and the onset of regular cyclicity is inconsistent and may vary across strains or with husbandry practices.(64-66) In female rabbits, the features described for other species do not apply.”
Background
A phenotype for the α7 nicotinic acetylcholine receptor null mutant
Morley, B. J., & Rodriguez‐Sierra, J. F. (2004) · Brain Research · doi:10.1016/j.brainres.2004.07.006 · Cited by 19
Expression patterns of estrogen receptors in the central auditory system change in prepubertal and aged mice
Charitidi, K., Frisina, R. D., Vasilyeva, O. N., Zhu, X., & Canlon, B. (2010) · Neuroscience · doi:10.1016/j.neuroscience.2010.08.010 · Cited by 19
“N IH -PA Author M anuscript N IH -PA Author M anuscript N IH -PA Author M anuscript they appear in different strains of mice (Nelson et al., 1990).”
Background
Defective Peripheral Nerve Development Is Linked to Abnormal Architecture and Metabolic Activity of Adipose Tissue in Nscl-2 Mutant Mice
Ruschke, K., Ebelt, H., Klöting, N., Boettger, T., Raum, K., Blüher, M., & Braun, T. W. (2009) · PLoS ONE · doi:10.1371/journal.pone.0005516 · Cited by 19
“5 weeks (cyclicity) [22], body fat increased noticeably (Fig.”
Background
Distinct effects of growth hormone deficiency and disruption of hypothalamic kisspeptin system on reproduction of male mice
de Paula, D. G., Bohlen, T. M., Zampieri, T. T., Mansano, N. D. S., Vieira, H. R., Gusmão, D. O., Wasinski, F., Donato, J., & Frazão, R. (2021) · Life Sciences · doi:10.1016/j.lfs.2021.119970 · Cited by 17
Early Marriage and Female Schooling in Bangladesh
Field, E., & Ambrus, A. (2006) · Journal of Political Economy · Cited by 19
Best practices to quantify the impact of reproductive toxicants on development, function, and diseases of the rodent mammary gland
Matouskova, K., Szabo, G. K., Daum, J., et al. (2022) · Reproductive Toxicology · doi:10.1016/j.reprotox.2022.06.011 · Cited by 18
IMMUNOHISTOCHEMICAL, HISTOLOGICAL AND ULTRASTRUCTURAL EVALUATION OF THE EFFECTS OF LEPTIN ON TESTES IN MICE
Kuş, I., Sarsılmaz, M., Canpolat, S., Yılmaz, B., Keleştimur, H., Akpolat, N., & Özoğul, C. (2005) · Archives of Andrology · doi:10.1080/014850190944375 · Cited by 17
“In addition to this primary role, circulating leptin appears to play an important role in the neuroendocrine axis [2], including regulation of reproductive functions [3, 4, 9, 22, 25].”
Background
Comparison of endpoints relevant to toxicity assessments in 3 generations of CD-1 mice fed irradiated natural and purified ingredient diets with varying soy protein and isoflavone contents
Camacho, L., Lewis, S. M., Vanlandingham, M. M., Juliar, B. E., Olson, G. R., Patton, R. E., da Costa, G. G., Woodling, K. A., Sepehr, E., Bryant, M., et al. (2016) · Food and Chemical Toxicology · doi:10.1016/j.fct.2016.05.014 · Cited by 15
“All smears in the breeding group for 21 days were read regardless of the time that the first estrus smear was detected and evaluated for cycle parameters; however, the majority of mice did not show regular cycles within this time period, consistent with previous reports that regular cycles in mice can take weeks to be…”
Result
The use of mouse chromosome substitution strains to investigate the genetic regulation of pubertal timing
Nathan, B. M., Hodges, C. A., & Palmert, M. R. (2006) · Molecular and Cellular Endocrinology · doi:10.1016/j.mce.2006.04.020 · Cited by 16
Experience-dependent regulation of vesicular zinc in male and female 3xTg-AD mice
Nakashima, A. S., Oddo, S., LaFerla, F. M., & Dyck, R. H. (2008) · Neurobiology of Aging · doi:10.1016/j.neurobiolaging.2008.05.028 · Cited by 16
Social and developmental influences on urinary androgen levels in young male white‐faced marmosets (Callithrix geoffroyi)
Birnie, A. K., Smith, A. S., Nali, C., & French, J. A. (2011) · American Journal of Primatology · doi:10.1002/ajp.20909 · Cited by 15
“Genetic influences have been identified that influence the timing of puberty [e.g., mice: Nelson et al., 1990; humans: Townel et al., 2005], and thus such factors should be considered as well.”
Background
Characterization of the onset of leptin effects on the regulation of energy balance
Teixeira, P. D. S., Ramos-Lobo, A. M., Tavares, M. R., Wasinski, F., Frazão, R., & Donato, J. (2021) · Journal of Endocrinology · doi:10.1530/joe-20-0076 · Cited by 15
Ablation of Arginase II Spares Arginine and Abolishes the Arginine Requirement for Growth in Male Mice
Didelija, I. C., Mohammad, M. A., & Marini, J. C. (2017) · Journal of Nutrition · doi:10.3945/jn.117.251249 · Cited by 14
“In C57BL/6 females, this period also coincides with early signs of puberty (vaginal opening; day 28) and onset of vaginal cornification (first day of estrous; day 42) (14).”
Background
The intact immature rodent uterotrophic bioassay: possible effects on assay sensitivity of vomeronasal signals from male rodents and strain differences.
Ashby, J., Owens, W., Odum, J., et al. (2003) · Environmental Health Perspectives · doi:10.1289/ehp.5981 · Cited by 14
“Another factor that may affect the timing of puberty is the strain of animal used (Nelson et al. 1990).”
Background
Onset of sexual maturation in female mice as measured in behavior and fertility: Interactions of exposure to males, phytoestrogen content of diet, and ano-genital distance
Khan, A., Bellefontaine, N., & deCatanzaro, D. (2007) · Physiology & Behavior · doi:10.1016/j.physbeh.2007.10.019 · Cited by 14
Mouse Age Matters: How Age Affects the Murine Plasma Metabolome
Pann, P., de Angelis, M. H., Prehn, C. P., & Adamski, J. (2020) · Metabolites · doi:10.3390/metabo10110472 · Cited by 13
Genetic influences on oestrous cyclicity in mice: evidence that cycle length and frequency are differentially regulated
Nelson, J. F., Karelus, K., Felicio, L. S., & Johnson, T. E. (1992) · Reproduction · doi:10.1530/jrf.0.0940261 · Cited by 13
Self-citation
Three-dimensional quantitative micro-elastography reveals alterations in spatial elasticity patterns in murine ovaries during ageing
Jaeschke, A., Hepburn, M. S., Mowla, A., Kennedy, B. F., & Chan, C. J. (2025) · Communications Biology · doi:10.1038/s42003-025-08835-w · Cited by 13
Postnatal Overnutrition Induces Changes in Synaptic Transmission to Leptin Receptor-Expressing Neurons in the Arcuate Nucleus of Female Mice
Zampieri, T. T., Bohlen, T. M., Silveira, M. A., Lana, L. C., de Paula, D. G., Donato, J., & Frazão, R. (2020) · Nutrients · doi:10.3390/nu12082425 · Cited by 13
“To study pubertal and adult mice, we evaluated sexual maturation, as previously described [25,27,28].”
Method
Med12 regulates ovarian steroidogenesis, uterine development and maternal effects in the mammalian egg†
Wang, X., Mittal, P., Castro, C. A., Rajkovic, G., & Rajkovic, A. (2017) · Biology of Reproduction · doi:10.1093/biolre/iox143 · Cited by 10
“Metestrus stage correlates with decline in estradiol and progesterone levels, and both vaginal cornification and estrous cycle are dependent on circulating estradiol levels [26, 27].”
Background
Prolonged Antibiotic Exposure during Adolescence Dysregulates Liver Metabolism and Promotes Adiposity in Mice
Carson, M. D., Warner, A. J., Geiser, V. L., Hathaway‐Schrader, J. D., Alekseyenko, A. V., Marshall, J. L., Westwater, C., & Novince, C. M. (2023) · American Journal Of Pathology · doi:10.1016/j.ajpath.2023.02.014 · Cited by 10
Addressing Sex as a Biological Variable in Preclinical Models of Lung Disease: An Official American Thoracic Society Research Statement
Lingappan, K., Sundar, I. K., Prakash, Y. S., Redente, E. F., Sin, D. D., Han, M. K., Lahm, T., Krymskaya, V. P., Kotton, D. N., Kulkarni, H. S., et al. (2025) · American Journal of Respiratory and Critical Care Medicine · doi:10.1164/rccm.202506-1361st · Cited by 11
“In rodents, early markers of puberty are vaginal opening, ﬁ rst vaginal corni ﬁ cation, and the onset of cyclicity in females, whereas balanopreputial separation is used as a marker in males (53).”
Maternal pre-conceptional glyphosate exposure impacts the offspring hepatic and ovarian proteome
Novbatova, G., Timme, K. A., Severin, A., Sayadi, M., & Keating, A. (2023) · Toxicological Sciences · doi:10.1093/toxsci/kfad047 · Cited by 8
“In C57Bl6 mice, vaginal opening was demonstrated to occur at approximately 30 days of age with vaginal cornification and cyclicity being demonstrated at 45 and 60 days, respectively (Nelson et al., 1990).”
Background
A Dominant X-Linked QTL Regulating Pubertal Timing in Mice Found by Whole Genome Scanning and Modified Interval-Specific Congenic Strain Analysis
Zhu, W., Fan, Z., Zhang, C., Guo, Z., Zhao, Y., Zhou, Y., Li, K., Xing, Z., Chen, G., Liang, Y., et al. (2008) · PLoS ONE · doi:10.1371/journal.pone.0003021 · Cited by 8
“05) and the discrepancy was ascribed to genetic factors [6].”
Background
A Pair of Mouse KRAB Zinc Finger Proteins Modulates Multiple Indicators of Female Reproduction1
Krebs, C. J., & Robins, D. M. (2009) · Biology of Reproduction · doi:10.1095/biolreprod.109.080846 · Cited by 8
“timing, VO was examined as a marker of puberty onset [30] in”

Authors: Nelson, J. F., Karelus, K., Felicio, L. S., & Johnson, T. E.
Affiliations: McGill University (CA)
The University of Texas at San Antonio (US)
University of Colorado Boulder (US)
Corresponding author: Nelson, James F.
ORCID: Nelson, James F.
Johnson, Thomas E.
Venue: Biology of Reproduction
Publisher: Oxford University Press (OUP)
Published: 1990-04-01
Volume: 42
Issue: 4
Pages: 649-655
ISSN: 0006-3363 (ISSN-L)
1529-7268
DOI: 10.1095/biolreprod42.4.649
OpenAlex: W2026104991
Cited by: 165
References: 0
Citations by year: 2026: 6 · 2025: 11 · 2024: 9 · 2023: 9 · 2022: 12 · 2021: 7 · 2020: 5 · 2019: 8 · 2018: 2 · 2017: 12 · 2016: 9 · 2015: 3 · 2014: 5 · 2013: 3 · 2012: 5
FWCI: 0.90
Type: journal article
Language: en
Open access: closed
Locations: Biology of Reproduction (publishedVersion)
PubMed (publishedVersion)
Funders: Medical Research Council Canada
U.S. Public Health Service
Medical Research Council
National Institute on Aging (AG 08322, AG00369)
Topics: Health Sciences › Medicine › Reproductive Medicine › Hypothalamic control of reproductive hormones
Health Sciences › Medicine › Reproductive Medicine › Reproductive Biology and Fertility
Health Sciences › Medicine › Endocrinology, Diabetes and Metabolism › Sexual Differentiation and Disorders
Keywords: pubertal timing, vaginal opening, vaginal cornification, genetic variation, inbred mouse strains, F1 hybrids, heterosis, additive genetic effects, body weight, C57BL/6J mice, DBA/2J, C3H/HeJ
MeSH terms: Age Factors, Animals, Body Weight, Estrus, Female, Genotype, Mice, Inbred Strains, Sexual Maturation, Vagina, Mice

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Genetic Influences on the Timing of Puberty in Mice1

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