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J. Anim Sci. 2006. 84:2050-2056. doi:10.2527/jas.2005-638
© 2006 American Society of Animal Science
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ANIMAL GROWTH, PHYSIOLOGY, AND REPRODUCTION

Induction of precocious puberty in heifers III: Hastened reduction of estradiol negative feedback on secretion of luteinizing hormone1

C. L. Gasser2, G. A. Bridges, M. L. Mussard, D. E. Grum, J. E. Kinder and M. L. Day3

Department of Animal Sciences, The Ohio State University, Columbus 43210


   Abstract
Top
 Abstract
INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 IMPLICATIONS
 LITERATURE CITED
 
Precocious puberty (<300 d of age) can be induced in beef heifers by early weaning and feeding a high-concentrate diet. The objective of this experiment was to determine whether precocious puberty occurs as a result of a hastened reduction of estradiol negative feedback on secretion of LH. Thirty crossbred Angus and Simmental heifers were weaned at 83 ± 2 d of age and 114 ± 3 kg of BW, blocked by BW, and randomly assigned to receive a high-concentrate (60% corn; H) or control (30% corn; C) diet and to receive ovariectomy (OVX), OVX plus an estradiol implant (OVXE), or to remain intact (INT). Residual ovarian tissue after OVX necessitated withdrawal of 6 heifers during the course of the experiment, resulting in the following treatment groups: OVX-C, n = 3; OVX-H, n = 5; OVXE-C, n = 4; OVXE-H, n = 2; INT-C, n = 5; INT-H, n = 5. To determine concentrations of progesterone and estradiol, blood samples were collected weekly beginning at a mean age of 160 d. To characterize LH concentrations, serial blood samples were collected at 12-min intervals for 12 h at mean ages of 119, 149, 188, 217, 246, 281, 323, 365, 407, and 449 d. By a mean age of 202 d, heifers fed the H diet were heavier (P < 0.05) than those fed the C diet. Heifers in the INT-H treatment attained puberty earlier (P < 0.05) than in the INT-C treatment (275 ± 30 vs. 385 ± 14 d of age, respectively). Overall mean concentrations of estradiol did not differ between OVXE-H and OVXE-C, between INT-H and INT-C, or between OVXE and INT treatments. The OVX treatments exhibited greater LH pulse frequency than the OVXE and INT treatments by the first serial blood collection (treatment x age, P < 0.05). The frequency of LH pulses was greater (P < 0.05) in the INT-H than the INT-C treatment by a mean age of 246 d and was greater (P < 0.05) in the OVXE-H than the OVXE-C treatment by a mean age of 281 d. In the OVXE-H treatment, LH secretion increased and subsequently "escaped" from estradiol negative feedback (detection of ≥1 LH pulse/h) earlier (P < 0.05) than in the OVXE-C treatment (307 ± 30 and 420 ± 21 d of age, respectively). It is concluded that advancing the reduction of estradiol negative feedback on secretion of LH is the mechanism by which early weaning and feeding a high-concentrate diet results in precocious puberty in heifers.

Key Words: early weaning • estradiol negative feedback • heifer • luteinizing hormone • puberty


   INTRODUCTION
Top
 Abstract
 INTRODUCTION
MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 IMPLICATIONS
 LITERATURE CITED
 
Heifers that attain puberty and experience multiple cycles before the breeding season have the potential for increased first service conception (Buskirk et al., 1995Go), earlier pregnancy (Byerly et al., 1987Go; Bagley, 1993Go), and increased lifetime productivity (Lesmeister et al., 1973Go). Heifer calves with greater weaning BW and/or increased growth rates before weaning reach puberty at a younger age (Wiltbank et al., 1966Go; Arije and Wiltbank, 1971Go; Patterson et al., 1992Go). Likewise, a majority of heifers weaned early (3 to 4 mo of age) and fed a high-concentrate diet exhibit precocious puberty (≤300 d of age; Day and Anderson, 1998Go; Gasser et al., 2006aGo,bGo, companion paper).

Puberty is stimulated in heifers by increased LH secretion during the peripubertal period (Day et al., 1984Go; 1987Go). The peripubertal increase in LH secretion results from declining negative feedback of estradiol on GnRH/LH secretion (Kinder et al., 1995Go; Day and Anderson, 1998Go). Increased secretion of LH causes increased growth of dominant ovarian follicles (Bergfeld et al., 1994Go) leading to increased systemic estradiol concentrations, which induces the initial preovulatory surge of LH. Precocious puberty is associated with advancement of the peripubertal increase in LH pulse frequency and greater maximum diameter of dominant follicles, duration of follicle waves, and circulating estradiol concentrations (Gasser et al., 2006aGo,bGo, companion paper). These changes are consistent with those that occur in response to the decline in estradiol negative feedback on GnRH secretion in heifers that reach puberty at 12 to 15 mo of age. The age at which estradiol inhibition of LH secretion declines can be influenced by diet (Kurz et al., 1990Go), as it has been postponed through restriction of energy intake.

We hypothesized that precocious attainment of puberty in heifers that are weaned early and fed a high-concentrate diet is facilitated by a reduction in estradiol negative feedback on secretion of LH.


   MATERIALS AND METHODS
Top
 Abstract
 INTRODUCTION
 MATERIALS AND METHODS
RESULTS
 DISCUSSION
 IMPLICATIONS
 LITERATURE CITED
 
Animals and Treatments
All procedures involving animals were in accordance with procedures approved by The Ohio State University Agricultural Animal Care and Use Committee.

Thirty crossbred Angus and Simmental heifers were weaned at 83 ± 2 d of age and 114 ± 3 kg of BW, blocked by BW, and randomly assigned to 1 of 6 treatments. The treatments consisted of feeding either a high-concentrate (H) or a control diet (C) and bilateral ovariectomy (OVX), OVX with addition of an estradiol implant (OVXE), or no further treatment, retaining intact ovaries (INT), to result in the following treatments: INT-H, INT-C, OVX-H, OVX-C, OVXE-H, or OVXE-C.

All heifers were fed a receiving diet after weaning until a mean age of 120 d, at which time the heifers were transitioned over a 10-d period to their respective treatment diets (i.e., H or C). All diets consisted of whole shelled corn, alfalfa pellets, pelleted soybean hulls, and a supplement that contained ground corn, soybean meal, urea, vitamins, minerals, monensin (Rumensin, Elanco, Indianapolis, IN), and fat (Table 1Go). Additionally, 1 kg of grass hay per heifer was added to the experimental diets each day to aid in the prevention of bloat.


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  		Table 1. Ingredients and chemical composition of experimental diets fed to heifers
 
All heifers were fed in groups that consisted of OVX, OVXE, and INT heifers within each diet, with 2 pens per diet. Targeted BW gains were 1.50 and 0.75 kg/d for the H and C diets, respectively, with diets fed at approximately 2.5 to 3.0% of BW (as-fed). Heifers were weighed weekly, and the amount of ration fed was adjusted accordingly to achieve the desired BW gain. All heifers remained on their respective treatment diets for the duration of the experiment.

Ovariectomy occurred at a mean age of 111 d in OVX heifers and 112 d in OVXE heifers and was performed under general anesthesia at The Ohio State University Veterinary Teaching Hospital. The OVXE heifers received implants made with polydimethylsiloxane tubing (3.35-mm i.d. x 4.65-mm o.d.; Dow Corning, Midland, MI) that were filled with 17ß-estradiol (Sigma Chemical, St. Louis, MO) and sealed at each end with medical-grade, adhesive silicone, type A (Dow Corning). A single implant was inserted into each heifer subcutaneously and caudal to the shoulder blade. The constant dose of estradiol delivered via these implants is determined by the surface area, and therefore the length of the implant, and not by the amount of estradiol because diameter and wall thickness of implants are constant (Dziuk and Cook, 1966Go).

The implant scheme was designed to maintain circulating concentrations of estradiol between 2 and 4 pg/mL, as previously shown for ovary-intact heifers of this age (Gasser et al., 2006aGo, companion paper). Based on previous experience with implants of this type in prepubertal heifers (Day et al., 1984Go; Kurz et al., 1990Go), it was estimated that BW-adjusted implants, resulting in 0.075 cm of implant/kg of BW would achieve circulating concentrations within this range. Therefore, the initial implant received by each heifer provided an implant length of 0.075 cm/kg of BW. As the heifers grew and BW increased to the point that the implant dose approached a mean of 0.05 cm/kg of BW for the group, or 0.045 cm/kg of BW in individual heifers, implants were replaced with new implants that restored the dose to 0.075 cm/kg of BW. The first implants were inserted in all OVXE heifers at a mean age of 112 d (the day of OVX), and the implants were replaced twice, at mean ages of 198 and 286 d. Implants were replaced 1 additional time in OVXE-C heifers at a mean age of 387 d.

Blood Sample Collection
Blood samples (10 mL) were collected weekly beginning at a mean age of 160 d and continuing throughout the experiment via jugular venipuncture into evacuated tubes containing anticoagulant (EDTA; Vacutainer, Becton-Dickinson, Franklin Lakes, NJ), centrifuged at 2,785 x g for 20 min immediately after collection, and plasma was harvested and frozen at –20°C until analyzed for progesterone and estradiol concentrations. Age at puberty for heifers in the INT treatments was defined as 7 d before the date of collection of the first blood sample that contained a plasma progesterone concentration >2 ng/mL or 7 d before the collection date of the first of 2 consecutive blood samples with a plasma progesterone concentration >1 ng/mL (Day et al., 1984Go). Heifers that reached puberty before 300 d of age were considered to have experienced precocious puberty.

To characterize LH concentrations, serial blood samples were collected at 12-min intervals for 12 h at a mean ages of 119, 149, 188, 217, 246, 281, 323, and 365 d. Samples were collected via indwelling jugular catheters into polypropylene tubes (Life Science Products Inc., Denver, CO), the blood was allowed to clot for 24 to 48 h at 4°C, the samples were centrifuged at 7,735 x g for 20 min, and serum was harvested and frozen at –20°C until analyzed for LH concentration. Individual INT heifers were removed from serial blood sampling procedures after attainment of puberty was confirmed. Heifers in the OVX and OVXE treatments were removed from serial blood sampling procedures after escape from estradiol negative feedback on LH secretion (detection of ≥1 LH pulse/h) was confirmed. To confirm escape from estradiol negative feedback in the OVXE-C treatment, 2 additional serial blood sample collections were conducted at mean ages of 407 and 449 d.

Hormone Quantification
Concentrations of LH were determined in duplicate for all serial blood serum samples with a double-antibody RIA (Anderson et al., 1996Go). The average intraassay CV was 2.8%, and the average interassay CV for standard sera of 1.09 and 4.07 ng/mL were 18.6 and 17.8%, respectively. The sensitivity of the assay was 0.03 ng/mL. The frequency of LH pulses, LH pulse amplitude, and mean LH concentrations were determined as described by Goodman and Karsch (1980)Go. Heifers were considered to have "escaped" from estradiol negative feedback on LH secretion when the frequency of LH pulses reached ≥1 pulse/h. This definition was developed based on previous research with OVX heifers indicating that after OVX (withdrawal of estradiol negative feedback), LH pulse frequency increases rapidly to ≥1 LH pulse/h (Day et al., 1984Go).

Concentrations of progesterone were determined using a commercially available RIA kit (Coat-a-Count, Diagnostic Products Corporation, Los Angeles, CA) as described previously for our laboratory (Burke et al., 2003Go). The interassay CV were 10.7, 13.1, and 13.0% for standard concentrations of 1.6, 2.6, and 12.1 ng/mL, respectively. The average intraassay CV was 2.2%, and the assay sensitivity was 0.06 ng/mL.

Concentrations of estradiol were determined using a double-extraction, single-antibody RIA as reported by Kojima et al. (1992)Go and previously validated in our laboratory (Anderson et al., 1996Go). The blood samples were all included in a single assay. The average intraassay CV among duplicate samples was 2.5%, and the sensitivity of the assay was 0.6 pg/mL.

Statistical Analyses
The effects of treatment, mean day of age, and the interaction of treatment and mean day of age on BW, estradiol concentration, LH pulse frequency, mean LH pulse amplitude, and mean LH concentration were analyzed by ANOVA using the MIXED procedure of SAS (SAS Inst. Inc., Cary, NC), with repeated measures analysis included in the model. The repeated measures model was


Formula

where Yijk = the observation of the jth heifer in the ith treatment on the kth day, µ = the overall mean, Ti = the ith treatment, hj:i = the random effect of the jth heifer within the ith treatment [hj:i ~ N(0,{sigma}2h)], Dk = the kth day, (TD)ik = the treatment x day interaction, and eijk = the random residual effect [eijk ~ N(0, {Sigma})], where {Sigma} is the variance-covariance structure of the residual errors for repeated measurements within heifers.

The effect of treatment on ADG, age and BW at puberty, and age and BW at escape from estradiol negative feedback on LH secretion were analyzed by ANOVA using the MIXED procedure of SAS (Yij = µ + Ti + eij, with notations as defined previously).


   RESULTS
Top
 Abstract
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
DISCUSSION
 IMPLICATIONS
 LITERATURE CITED
 
Six heifers were withdrawn from the experiment after detection of residual ovarian tissue due to incomplete OVX during the course of the experiment. The ovarian tissue was detected by observation of follicles via transrectal ultrasonography or circulating progesterone concentrations, or both. Therefore, results are reported based on the following number of animals in each treatment: INT-H, n = 5; INT-C, n = 5; OVX-H, n = 5; OVX-C, n = 3; OVXE-H, n = 2; and OVXE-C, n = 4.

Average daily BW gain from mean age of 120 to 322 d was greater (P < 0.05) in heifers fed the H than C diet (1.1 ± 0.1 and 0.7 ± 0.1 kg/d, respectively). Body weight of heifers fed the H diet was greater (P < 0.05) than in C heifers by a mean age of 202 d, and this difference persisted through the remainder of the experimental period (treatment x age, P < 0.01; Figure 1Go). Within each diet, BW did not differ between heifers in the INT, OVX, and OVXE treatments at any age during the experiment.


Figure 1
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  		Figure 1. Body weight of heifers that were weaned early and fed a high-concentrate (H) or control (C) diet and ovariectomized (OVX), OVX and implanted with estradiol (OVXE), or left intact (INT). Numbers of heifers in each group are shown in parentheses. Body weight of heifers fed the H diet was greater (P < 0.05) than that of heifers fed the C diet by a mean age of 202 d.

 
Precocious puberty (<300 d of age) occurred in 4 of the 5 heifers in the INT-H and none of the heifers in the INT-C treatment. Heifers in the INT-H treatment reached puberty at an earlier age (P < 0.05) than those in the INT-C treatment (275 ± 30 and 385 ± 14 d of age, respectively) but at similar BW (mean = 310 ± 13 kg).

Overall mean concentrations of estradiol during the experiment did not differ between the OVXE-H and OVXE-C treatments or between the INT-H and INT-C treatments. Overall mean concentrations of estradiol were also not different for the OVXE and INT treatments (Figure 2Go) but were greater (P < 0.05) in the OVXE than INT treatments for approximately 1 to 3 wk after each time of insertion of new estradiol implants (treatment x age, P < 0.05).


Figure 2
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  		Figure 2. Circulating concentrations of estradiol in heifers that were weaned early and fed a high-concentrate (H) or control diet (C) and ovariectomized and implanted with estradiol (OVXE) or left intact (INT). Numbers of heifers in each group are shown in parentheses. Estradiol concentrations were not different among the groups.

 
The OVX treatments exhibited greater (P < 0.05) LH pulse frequency than the OVXE and INT treatments by the first serial blood collection at a mean age of 119 d (treatment x age, P < 0.05; Figure 3Go), which was 8 d after OVX was performed. The OVX-H treatment had a greater frequency of LH pulses (P < 0.05) than OVX-C treatment at a single time point (mean age 246 d). The frequency of LH pulses was greater (P < 0.05) in the INT-H than INT-C treatment by a mean age of 246 d. The OVXE-H treatment exhibited greater LH pulse frequency (P < 0.05) than the OVXE-C treatment at mean ages of 281, 323, and 365 d.


Figure 3
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  		Figure 3. Frequency of LH pulses in heifers that were weaned early and fed a high-concentrate (H) or control (C) diet and ovariectomized (OVX), OVX and implanted with estradiol (OVXE), or left intact (INT). The frequency of LH pulses was greater (P < 0.05) in INT-H than INT-C heifers by a mean age of 246 d and was greater (P < 0.05) in OVXE-H than OVXE-C heifers by a mean age of 281 d (treatment x age, P < 0.05). Because of attainment of puberty in one of the INT-H heifers before the 4th collection period, the LH frequency at mean ages of 217 and 246 d includes 4 of the 5 INT-H heifers. All other data points shown include all heifers within each treatment.

 
Mean LH concentrations were greater (P < 0.05) in OVX treatments than other treatments by a mean age of 119 d (treatment x age, P < 0.05), and no differences were detected between OVX-H and OVX-C treatments. Mean LH concentrations were greater (P < 0.05) in OVXE-H than the OVXE-C treatment at mean ages of 246, 281, 323, and 365 d. No differences in mean LH concentrations were detected between INT-H and INT-C treatments. Amplitude of LH pulses fluctuated with age (P < 0.05), though no clear pattern was detected, and there were no differences across treatments.

Escape from estradiol negative feedback on LH secretion (≥1 LH pulse/h) was achieved at an earlier age (P < 0.01) in OVXE-H than the OVXE-C treatment (307 ± 30 and 420 ± 21 d of age, respectively). Additionally, age at escape in OVXE-H treatment did not differ from age at puberty in INT-H treatment (275 ± 30 d of age). Likewise, age at escape in OVXE-C treatment did not differ from age at puberty in INT-C treatment (385 ± 14 d of age). Body weight at escape was not different between OVXE-H and OVXE-C treatment (mean = 372 ± 16 kg).


   DISCUSSION
Top
 Abstract
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
IMPLICATIONS
 LITERATURE CITED
 
Frequency of LH pulses and mean LH concentrations increased at an earlier age in OVX heifers that were implanted with estradiol and fed a high-concentrate diet as compared with contemporaries fed a control diet, signifying that the decline of estradiol negative feedback on LH secretion that leads to puberty was hastened in these heifers. Intact contemporary heifers that were fed the high-concentrate diet also exhibited an advanced increase in LH pulse frequency and puberty at a younger age than those fed the control diet. Age at puberty corresponded with age at escape from estradiol negative feedback within heifers fed the high-concentrate diet and within heifers fed the control diet. The age at escape from estradiol negative feedback on LH is a primary mechanism that determines age at puberty in heifers (Day et al., 1984Go; Kurz et al., 1990Go). In previous research from our laboratory, an apparent shift of the peripubertal period to an earlier age in heifers that are weaned early and fed a high-concentrate diet was observed, as evidenced by advanced increases in LH secretion and ovarian follicular development (Gasser et al., 2006aGo,bGo, companion paper) leading to precocious attainment of puberty. The present experiment contributes further evidence toward a shift in the timing of the peripubertal period as we have now observed an advanced decline in estradiol negative feedback with the same heifer treatment model.

A rapid increase in mean LH concentrations and frequency of LH pulses was detected in heifers that were OVX at a mean age of 111 d, regardless of dietary treatment. This finding confirms previous reports (Moseley et al., 1984Go; Anderson et al., 1986Go) that ovarian factors are restraining LH secretion in heifers at this age. It appears that the primary factor is estradiol, as estradiol replacement completely prevented this post-OVX increase in LH pulses. The subsequent increase in LH secretion in estradiol-implanted heifers reflects the ensuing decline in estradiol negative feedback.

Some variation in estradiol concentrations was detected in heifers that received estradiol implants. These fluctuations are explained by the nature of the implant strategy for this experiment. As would be expected, estradiol concentrations in implanted heifers were greatest during the short period of time immediately after insertion of new implants. Over time, as heifers increased in BW the circulating concentrations of estradiol gradually decreased until replacement of implants was necessary to maintain the concentrations of estradiol within the appropriate range for heifers of this age. Though the pattern of estradiol concentrations in implanted heifers was not identical to that of the intact heifers, estradiol implants were successful in achieving the intended goal of overall mean concentrations that were not different from those of intact heifers.

The current study confirms previous reports using OVX and estradiol replacement in heifers (Day et al., 1984Go, 1986aGo; Kurz et al., 1990Go) that the peripubertal decline in estradiol negative feedback will occur in the absence of the ovary. Downregulation of estradiol receptors in specific regions within the hypothalamus during the peripubertal period in heifers (Day et al., 1987Go; Day and Anderson, 1998Go) appears to be a critical component of the mechanism responsible for the decline in estradiol negative feedback. The primary signal that initiates the endocrine mechanisms leading to the decline in estradiol negative feedback is yet to be determined, but it was activated in the current study through feeding the high-concentrate diet.

Nutritional status has been linked with hypothalamic regulation in prepubertal heifers in other studies where dietary treatment effects on timing of the decline in estradiol negative feedback have been observed. Restriction of dietary energy intake that leads to delayed puberty in heifers has been shown to delay increases in mean LH concentration and frequency of LH pulses as well as attenuate responsiveness of LH secretion to GnRH (Day et al., 1986bGo). Dietary energy restriction has also been shown to delay follicular development (Bergfeld et al., 1994Go). Similarly, dietary energy restriction delayed the decline in estradiol negative feedback on LH secretion in heifers (Kurz et al., 1990Go). It appears that the decline of estradiol negative feedback on secretion of LH is a common mechanism that is requisite for the process of puberty to progress to completion whether puberty occurs at a typical age or in the case of delayed or precocious puberty.

The nutritive or growth-related signals leading to activation of the reproductive axis in heifers with precocious puberty are unknown. One possible candidate that would provide a logical connection between the high-concentrate diet and precocious maturation of the reproductive axis is IGF-I. A concomitant increase of IGF-I concentration with LH concentration has been detected in heifers fed for increased growth rates that resulted in earlier age at puberty (Yelich et al., 1996Go). In other work by Renaville et al. (2000)Go, a progressive rise in IGF-I concentrations and coincident decrease in IGFBP 2 were detected as puberty approached in a group of control bulls, and the rise in IGF-I was delayed in feed-restricted bulls. Hiney et al. (1996)Go has suggested from research with female rats that IGF-I of peripheral origin contributes to the initiation of female puberty by stimulating GnRH release from the hypothalamus via IGF-I receptors present in the median eminence. There is also evidence to support a role for IGF-I at the pituitary gland. Hashizume et al. (2002)Go has reported from in vitro experiments with bovine anterior pituitary cells that IGF-I enhances GnRH-stimulated LH release without changing the number of GnRH receptors in the pituitary cells and that IGF-I also interacts with estradiol to increase the LH response to GnRH.

Other signals related to nutritional status that may contribute to initiation of mechanisms that facilitate precocious puberty include leptin (Maciel et al., 2004bGo), neuropeptide Y (Morrison et al., 2003Go), and transforming growth factor {alpha} (Ojeda and Ma, 1998Go). Increasing concentrations of leptin have been detected in association with the attainment of puberty in heifers (Garcia et al., 2002Go). However, leptin appears to have more of a permissive role than a stimulatory role in attainment of puberty in heifers (Maciel et al., 2004aGo). Further research is needed to increase our understanding of the role of IGF-I and other potential factors in the process of pubertal development in heifers.

Based on the results of this experiment, we accept the hypothesis and conclude that advanced reduction of estradiol negative feedback on secretion of LH is the mechanism by which early weaning and feeding a high-concentrate diet induces precocious puberty in heifers.


   IMPLICATIONS
Top
 Abstract
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 IMPLICATIONS
LITERATURE CITED
 
Weaning heifer calves early and increasing dietary energy intake through feeding a corn-based diet hastens the pubertal process and results in precocious attainment of puberty in most heifers. As with puberty at a typical age, precocious puberty is preceded by a decline in the inhibition of luteinizing hormone secretion by circulating estradiol. This decline in feedback inhibition facilitates increases in luteinizing hormone secretion and follicular development that are common during the peripubertal period. This treatment model is an effective method for control of puberty that can be utilized to study the processes associated with puberty in heifers. These results also provide evidence that maturation of the reproductive endocrine axis is complete in heifers several months before the typical age of puberty. It is clear that environmental influences such as management and nutrition during early life in heifers exert a profound influence on the timing of reproductive maturation.


   Footnotes
 
1 Salaries and research support provided by USDA NRICGP Award 00-35203-9133 and state and federal funds appropriated to the Ohio Agricultural Research and Development Center, The Ohio State University (Manuscript No. 9-06AS). Back

2 Current address: Southern Utah Univ., 351 W. University Blvd., Cedar City, UT 84720. Back

3 Corresponding author: day.5{at}osu.edu

Received for publication November 3, 2005. Accepted for publication April 5, 2006.


   LITERATURE CITED
Top
 Abstract
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 IMPLICATIONS
 LITERATURE CITED
 


Anderson, W. J., D. W. Forrest, B. A. Goff, A. A. Shaikh, and P. G. Harms. 1986. Ontogeny of ovarian inhibition of pulsatile luteinizing hormone secretion in postnatal Holstein heifers. Domest. Anim. Endocrinol. 3:107–111.

Anderson, L. H., C. M. McDowell, and M. L. Day. 1996. Progestin-induced puberty and secretion of luteinizing hormone in heifers. Biol. Reprod. 54:1025–1031.[Abstract]

Arije, G. F., and J. N. Wiltbank. 1971. Age and weight at puberty in Hereford heifers. J. Anim. Sci. 33:401–406.[Abstract/Free Full Text]

Bagley, C. P. 1993. Nutritional management of replacement beef heifers: a review. J. Anim. Sci. 71:3155–3163.[Abstract]

Bergfeld, E. G. M., F. N. Kojima, A. S. Cupp, M. E. Wehrman, K. E. Peters, M. Garcia-Winder, and J. E. Kinder. 1994. Ovarian follicular development in prepubertal heifers is influenced by level of dietary energy intake. Biol. Reprod. 51:1051–1057.[Abstract]

Burke, C. R., M. L. Mussard, C. L. Gasser, D. E. Grum, and M. L. Day. 2003. Estradiol benzoate delays new follicular wave emergence in a dose-dependent manner after ablation of the dominant ovarian follicle in cattle. Theriogenology 60:647–658.[CrossRef][Medline]

Buskirk, D. D., D. B. Faulkner, and F. A. Ireland. 1995. Increased postweaning gain of beef heifers enhances fertility and milk production. J. Anim. Sci. 73:937–946.[Abstract]

Byerly, D. J., R. B. Staigmiller, J. G. Berardinelli, and R. E. Short. 1987. Pregnancy rates of beef heifers bred either on puberal or third estrus. J. Anim. Sci. 65:645–650.[Abstract/Free Full Text]

Day, M. L., and L. H. Anderson. 1998. Current concepts on the control of puberty in cattle. J. Anim. Sci. 76(Suppl. 3):1–15.[Abstract/Free Full Text]

Day, M. L., K. Imakawa, M. Garcia-Winder, R. J. Kittok, B. D. Schanbacher, and J. E. Kinder. 1986a. Influence of prepubertal ovariectomy and estradiol replacement therapy on secretion of luteinizing hormone before and after pubertal age in heifers. Domest. Anim. Endocrinol. 3:17–25.

Day, M. L., K. Imakawa, M. Garcia-Winder, D. D. Zalesky, B. D. Schanbacher, R. J. Kittok, and J. E. Kinder. 1984. Endocrine mechanisms of puberty in heifers: Estradiol negative feedback regulation of luteinizing hormone secretion. Biol. Reprod. 31:332–341.[Abstract]

Day, M. L., K. Imakawa, P. L. Wolfe, R. J. Kittok, and J. E. Kinder. 1987. Endocrine mechanisms of puberty in heifers. Role of hypothalamo-pituitary estradiol receptors in the negative feedback of estradiol on luteinizing hormone secretion. Biol. Reprod. 37:1054–1065.[Abstract]

Day, M. L., K. Imakawa, D. D. Zalesky, R. J. Kittok, and J. E. Kinder. 1986b. Effects of restriction of dietary energy intake during the prepubertal period on secretion of luteinizing hormone and responsiveness of the pituitary to luteinizing hormone-releasing hormone in heifers. J. Anim. Sci. 62:1641–1648.[Abstract/Free Full Text]

Dziuk, P. J., and B. Cook. 1966. Passage of steroids through silicone rubber. Endocrinology 78:208–211.[Medline]

Garcia, M. R., M. Amstalden, S. W. Williams, R. L. Stanko, C. D. Morrison, D. H. Keisler, S. E. Nizielski, and G. L. Williams. 2002. Serum leptin and its adipose gene expression during pubertal development, the estrous cycle, and different seasons in cattle. J. Anim. Sci. 80:2158–2167.[Abstract/Free Full Text]

Gasser, C. L., C. R. Burke, M. L. Mussard, E. J. Behlke, D. E. Grum, J. E. Kinder, and M. L. Day. 2006a. Induction of precocious puberty in heifers II: Advanced ovarian follicular development. J. Anim. Sci. 84:2042–2049.[Abstract/Free Full Text]

Gasser, C. L., D. E. Grum, M. L. Mussard, F. L. Fluharty, J. E. Kinder, and M. L. Day. 2006b. Induction of precocious puberty in heifers I: Enhanced secretion of luteinizing hormone. J. Anim. Sci. 84:2035–2041.[Abstract/Free Full Text]

Goodman, R. L., and F. J. Karsch. 1980. Pulsatile secretion of luteinizing hormone: Differential suppression by ovarian steroids. Endocrinology 107:1286–1290.[Abstract]

Hashizume, T., A. Kumahara, M. Fujino, and K. Okada. 2002. Insulin-like growth factor I enhances gonadotropin-releasing hormone-stimulated luteinizing hormone release from bovine anterior pituitary cells. Anim. Reprod. Sci. 70:13–21.[CrossRef][Medline]

Hiney, J. K., V. Srivastava, C. L. Nyberg, S. R. Ojeda, and W. L. Dees. 1996. Insulin-like growth factor I of peripheral origin acts centrally to accelerate the initiation of female puberty. Endocrinology 137:3717–3728.[Abstract]

Kinder, J. E., E. G. M. Bergfeld, M. E. Wehrman, K. E. Peters, and F. N. Kojima. 1995. Endocrine basis for puberty in heifers and ewes. J. Reprod. Fertil. Suppl. 49:393–407.[Medline]

Kojima, N., T. T. Stumpf, A. S. Cupp, L. A. Werth, M. S. Roberson, M. W. Wolfe, R. J. Kittok, and J. E. Kinder. 1992. Exogenous progesterone and progestins as used in estrous synchrony regimens do not mimic the corpus luteum in regulation of luteinizing hormone and 17ß-estradiol in circulation of cows. Biol. Reprod. 47:1009–1017.[Abstract]

Kurz, S. G., R. M. Dyer, Y. Hu, M. D. Wright, and M. L. Day. 1990. Regulation of luteinizing hormone secretion in prepubertal heifers fed an energy-deficient diet. Biol. Reprod. 43:450–456.[Abstract]

Lesmeister, J. L., P. J. Burfening, and R. L. Blackwell. 1973. Date of first calving in beef cows and subsequent calf production. J. Anim. Sci. 36:1–6.[Abstract/Free Full Text]

Maciel, M. N., D. A. Zieba, M. Amstalden, D. H. Keisler, J. P. Neves, and G. L. Williams. 2004a. Chronic administration of recombinant ovine leptin in growing beef heifers: Effects on secretion of LH, metabolic hormones, and timing of puberty. J. Anim. Sci. 82:2930–2936.[Abstract/Free Full Text]

Maciel, M. N., D. A. Zieba, M. Amstalden, D. H. Keisler, J. P. Neves, and G. L. Williams. 2004b. Leptin prevents fasting-mediated reductions in pulsatile secretion of luteinizing hormone and enhances its gonadotropin-releasing hormone-mediated release in heifers. Biol. Reprod. 70:229–235.[Abstract/Free Full Text]

Morrison, C. D., J. A. Daniel, J. H. Hampton, P. R. Buff, T. M. McShane, M. G. Thomas, and D. H. Keisler. 2003. Luteinizing hormone and growth hormone secretion in ewes infused intrace-rebroventricularly with neuropeptide Y. Domest. Anim. Endocrinol. 24:69–80.[CrossRef][Medline]

Moseley, W. M., T. G. Dunn, C. C. Kaltenbach, R. E. Short, and R. B. Staigmiller. 1984. Negative feedback control of luteinizing hormone secretion in prepubertal beef heifers at 60 and 200 days of age. J. Anim. Sci. 58:145–150.[Abstract/Free Full Text]

Ojeda, S. R., and Y. J. Ma. 1998. Epidermal growth factor tyrosine kinase receptors and the neuroendocrine control of mammalian puberty. Mol. Cell. Endocrinol. 140:101–106.[CrossRef][Medline]

Patterson, D. J., L. R. Corah, J. R. Brethour, J. J. Higgins, G. H. Kiracofe, and J. S. Stevenson. 1992. Evaluation of reproductive traits in Bos taurus and Bos indicus crossbred heifers: Relationship of age at puberty to length of the postpartum interval to estrus. J. Anim. Sci. 70:1994–1999.[Abstract]

Renaville, R., C. Van Eenaeme, B. H. Breier, L. Vleurick, C. Bertozzi, N. Gengler, J.-L. Hornick, I. Parmentier, L. Istasse, V. Haezebroeck, S. Massart, and D. Portetelle. 2000. Feed restriction in young bulls alters the onset of puberty in relationship with plasma insulin-like growth factor-I (IGF-I) and IGF-binding proteins. Domest. Anim. Endocrinol. 18:165–176.[CrossRef][Medline]

Wiltbank, J. N., K. E. Gregory, L. A. Swiger, J. E. Ingalls, J. A. Rothlisberger, and R. M. Koch. 1966. Effects of heterosis on age and weight at puberty in beef heifers. J. Anim. Sci. 25:744–751.[Abstract/Free Full Text]

Yelich, J. V., R. P. Wetteman, T. T. Marston, and L. J. Spicer. 1996. Luteinizing hormone, growth hormone, insulin-like growth factor-I, insulin and metabolites before puberty in heifers fed to gain at two rates. Domest. Anim. Endocrinol. 13:325–338.[CrossRef][Medline]


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C. L. Gasser, E. J. Behlke, D. E. Grum, and M. L. Day
Effect of timing of feeding a high-concentrate diet on growth and attainment of puberty in early-weaned heifers
J Anim Sci, November 1, 2006; 84(11): 3118 - 3122.
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