Age-related changes in the oestrous cycle and reproductive hormones in senescence-accelerated mouse
Ma Yuan A , Zhou Wen-Xia A , Cheng Jun-Ping A and Zhang Yong-Xiang A B
+ Author Affiliations
- Author Affiliations
A Department of Neuro-Immuno Pharmacology of Traditional Chinese Medicine, Beijing Institute of Pharmacology and Toxicology, 27 Taiping Road, Beijing 100850, China.
B Corresponding author. Email: zhangyx@nic.bmi.ac.cn
Reproduction, Fertility and Development 17(5) 507-512 https://doi.org/10.1071/RD04099
Submitted: 17 September 2004 Accepted: 6 March 2005 Published: 2 May 2005
Abstract
To investigate age-related changes in the oestrous cycle and reproductive hormone levels in senescence-accelerated mouse (SAM), we examined these parameters in 3-, 5-, 7-, 9- and 11-month-old female SAM-prone/8 (SAMP8) and SAM-resistant/1 (SAMR1) strains. Levels of β-endorphin (β-EP) and substance P (SP) in the hypothalamus were also measured. The oestrous cycle and dioestrus of 9-month-old SAMP8 mice were significantly prolonged compared with age-matched SAMR1 mice. Furthermore, the concentration of serum oestradiol was lower and the level of pituitary luteinising hormone was higher in SAMP8 mice compared with SAMR1 mice. This characterises the hypothalamus–pituitary–ovary (HPO) axis of the SAMP8 strain as hypergonadotropic–hypogonad. The levels of β-EP and SP in the SAMP8 hypothalamus were lower than in the SAMR1 hypothalamus. These results indicate that the function of the HPO axis in SAMP8 mice declines early and this may be attributed, in part, to the decline in β-EP and SP concentrations in the hypothalamus.
Extra keywords: β-endorphin, luteinising hormone, oestradiol, substance P.
Acknowledgments
This project was supported by the Chinese National Key Project of Basic Research (G1999054401) and the National Natural Science foundation of China (No. 30200367).
References
Adashi, E. Y. (1994). The climacteric ovary as a functional gonadotropin-driven and androgen production gland. Fertil. Steril. 62, 20–26.
| PubMed |
Akhan, S. E. , Gurel, T. , Has, R. , Iyibozkurt, A. C. , and Turfanda, A. (2002). Effects of long-term oral hormone replacement therapy on plasma nitric oxide and beta-endorphin levels in postmenopausal women. Gynecol. Obstet. Invest. 54, 196–200.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Akinbami, M. A. , and Taylor, M. F. (1994). Effect of a peripheral and a central acting opioid antagonist on the testicular response to stress in rats. Neuroendocrinology 59, 343–348.
| PubMed |
Baker, L. D. , Sambamurti, K. , Craft, S. , Cherrier, M. , Raskind, M. A. , Stanczyk, F. Z. , Plymate, S. R. , and Asthana, S. (2003). 17β-Estradiol reduces plasma Aβ40 for HRT-naive postmenopausal women with Alzheimer disease: a preliminary study. Am. J. Geriatr. Psychiatry 11, 239–244.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Billington, C. J. , Shafer, R. B. , and Morley, J. E. (1990). Effects of opioid blockade with nalmefene in older impotent men. Life Sci. 47, 799–805.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Blogowska, A. , Rzepka, G. I. , Krzyzanowska, S. B. , Zoltowski, S. , and Kosmowska, B. (2003). Leptin, neuropeptide Y, beta-endorphin, gonadotropin, and estradiol levels in girls before menarche. Gynecol. Endocrinol. 17, 7–12.
| PubMed |
Bu, S. , Sun, M. , and Zhang, Y. (1998a). Effect of Gengnianjian on up regulated estrogen receptor mRNA to substance P and beta-endorphin in hypothalamus of aging female rats. Zhongguo Zhong Xi Yi Jie He Za Zhi 18, 28–31.
| PubMed |
Bu, S. Z. , Sun, M. , Yu, J. , Zhang, Y. , and Zhang, Y. L. (1998b). Effect of estradiol on estrogen receptor expression and beta-endorphin in hypothalamus of aging female rats. Chin. J. Neurosci. 14, 81–84.
Cherrier, M. M. , Craft, S. , and Matsumoto, A. H. (2003). Cognitive changes associated with supplementation of testosterone or dihydrotestosterone in mildly hypogonadal men: a preliminary report. J. Androl. 24, 568–576.
| PubMed |
Cholerton, B. , Gleason, C. E. , Baker, L. D. , and Asthana, S. (2002). Estrogen and Alzheimer’s disease: the story so far. Drugs Aging 19, 405–427.
| PubMed |
Coiro, V. , Passeri, M. , and Volpi, R. (1989). Different effects of aging on the opioid mechanisms controlling gonadotropin and cortisol secretion in man. Horm. Res. 32, 119–123.
| PubMed |
Davis, S. R. (2002). The effects of tibolone on mood and libido. Menopause 9, 162–170.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Dawuda, P. M. , Scaife, J. R. , Hutchinson, J. S. , and Sinclair, K. (2002). Mechanisms linking under-nutrition and ovarian function in beef heifers. Anim. Reprod. Sci. 74, 11–26.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Debeljuk, L. , Rao, J. N. , and Bartke, A. (2003). Tachykinins and their possible modulatory role on testicular function: a review. Int. J. Androl. 26, 202–210.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Farr, S. A. , Banks, W. A. , Uezu, K. , Sano, A. , Gaskin, F. S. , and Morley, J. E. (2003a). Antibody to beta-amyloid protein increases acetylcholine in the hippocampus of 12 month SAMP8 male mice. Life Sci. 73, 555–562.
| PubMed |
Farr, S. A. , Poon, H. F. , Dogrukol, A. D. , Drake, J. , Banks, W. A. , Eyerman, E. , Butterfield, D. A. , and Morley, J. E. (2003b). The antioxidants alpha-lipoic acid and N-acetylcysteine reverse memory impairment and brain oxidative stress in aged SAMP8 mice. J. Neurochem. 84, 1173–1183.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Farrag, A. K. , Khedr, E. M. , Abdel, A. H. , and Rageh, T. A. (2002). Effect of surgical menopause on cognitive functions. Dement. Geriatr. Cogn. Disord. 13, 193–198.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Flood, J. , Farr, S. , Kaiser, F. , Regina, M. , and Morley, J. (1995). Age-related decrease of plasma testosterone in SAMP8 mice: replacement improves age-related impairment of learning and memory. Physiol. Behav. 57, 669–673.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Gabor, R. , Nagle, R. , Johnson, D. A. , and Gibbs, R. B. (2003). Estrogen enhances potassium-stimulated acetylcholine release in the rat hippocampus. Brain Res. 962, 244–247.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Gao, H. B. , Tong, M. H. , and Hu, Y. Q. (2002). Glucocorticoid induces apoptosis in rat Leydig cells. Endocrinology 143, 130–138.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Guzeloglu, A. , Ambrose, J. D. , Kassa, T. , and Diaz, T. (2001). Long-term follicular dynamics and biochemical characteristics of dominant follicles in dairy cows subjected to acute heat stress. Anim. Reprod. Sci. 66, 15–34.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Hakola, K. , Boogaart, P. V. D. , Mulders, J. , de Leeuw, R. , Schoonen, W. , Heyst, J. V. , Swolfs, A. , Casteren, J. V. , Huhtaniemi, I. , and Kloosterboer, H. (1997). Recombinant rat luteinizing hormone: production by Chinese hamster ovary cells, purification and functional characterization. Mol. Cell Endocrinol. 128, 47–56.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
He, D. , Sato, I. , Kimura, F. , and Akema, T. (2003). Lipopolysaccharide inhibits luteinizing hormone release through interaction with opioid and excitatory amino acid inputs to gonadotropin-releasing hormone neurones in female rats: possible evidence for a common mechanism involved in infection and immobilization stress. J. Neuroendocrinol. 15, 559–563.
| PubMed |
Hong, X. R. , Zhao, X. L. , Wang, C. H. , and Ling, B. C. (2002). The postburn changes in hypothalamic paraventricular β-endorphin and the roles of the δ-receptor in scalded rats. Chin. J. Burns 18, 45–48.
Howes, M. J. , Houghton, P. J. , Barlow, D. J. , Pocock, V. J. , and Milligan, S. R. (2002). Assessment of estrogenic activity in some common essential oil constituents. J. Pharm. Pharmacol. 54, 1521–1528.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Hung, A. J. , Stanbury, M. G. , Shanabrough, M. , Horvath, T. L. , Garcia, L. M. , and Naftolin, F. (2003). Estrogen, synaptic plasticity and hypothalamic reproductive aging. Exp. Gerontol. 38, 53–59.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Kerdelhue, B. , Williams, R. F. , Lenoir, V. , Fardin, V. , Kolm, P. , Hodgen, G. D. , Jones, G. S. , Scholler, R. , and Jones, H. W. (2000). Variations in plasma levels of substance P and effects of a specific substance P antagonist of the NK (1) receptor on preovulatory LH and FSH surges and progesterone secretion in the cycling cynomolgus monkey. Neuroendocrinology 71, 228–236.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Korszun, A. , Young, E. A. , Engleberg, N. C. , Masterson, L. , Dawson, E. C. , Spindler, K. , McClure, L. A. , Brown, M. B. , and Crofford, L. J. (2000). Follicular phase hypothalamic–pituitary–gonadal axis function in women with fibromyalgia and chronic fatigue syndrome. J. Rheumatol. 27, 1526–1530.
| PubMed |
Kuhl, H. (2002). Influence of the ovarian cycle on the central nervous system. Ther. Umsch. 59, 175–181.
| PubMed |
Liao, B. S. , Ju, G. , Zhang, B. N. , and Zhu, X. Z. (1997). Effects of estradiol valerate on the endogenous opioid peptides gene expression of the hypothalamus in 18 month female rats. Chin. J. Geriatr. 16, 331–333.
Liu, J. X. , Liu, M. R. , and Song, T. (2001). Clinical and experimental study on the ovulation promoting effect of Yangjing decoction. Zhongguo Zhong Xi Yi Jie He Za Zhi 21, 94–98.
| PubMed |
Marinelli, P. W. , Quirion, R. , and Gianoulakis, C. (2003). Estradiol valerate and alcohol intake: a comparison between Wistar and Lewis rats and the putative role of endorphins. Behav. Brain Res. 139, 59–67.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Markowska, A. L. , and Savonenko, A. V. (2002). Effectiveness of estrogen replacement in restoration of cognitive function after long-term estrogen withdrawal in aging rats. J. Neurosci. 22, 10 985–10 995.
| PubMed |
Morley, J. E. , Farr, S. A. , Kumar, V. B. , and Banks, W. A. (2002). Alzheimer’s disease through the eye of a mouse. Acceptance lecture for the 2001 Gayle A. Olson and Richard D. Olson prize. Peptides 23, 589–599.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Nonaka, N. , Banks, W. A. , Mizushima, H. , Shioda, S. , and Morley, J. E. (2002). Regional differences in PACAP transport across the blood–brain barrier in mice: a possible influence of strain, amyloid beta protein, and age. Peptides 23, 2197–2202.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Pan, H. A. , Wang, S. T. , Pai, M. C. , Chen, C. H. , Wu, M. H. , and Huang, K. E. (2003). Cognitive function variations in postmenopausal women treated with continuous, combined HRT or tibolone. A comparison. J. Reprod. Med. 48, 375–380.
| PubMed |
Shughrue, P. J. , and Merchenthaler, I. (2003). Estrogen prevents the loss of CA1 hippocampal neurons in gerbils after ischemic injury. Neuroscience 116, 851–861.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Stemmelin, J. , Lazarus, C. , Cassel, S. , and Kelche, C. (2000). Immunohistochemical and neurochemical correlates of learning deficits in aged rats. Neuroscience 96, 275–289.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Stomati, M. , Bernardi, F. , Luisi, S. , Puccetti, S. , and Casarosa, E. , et al. (2002). Conjugated equine estrogens, estrone sulphate and estradiol valerate oral administration in ovariectomized rats: effects on central and peripheral allopregnanolone and β-endorphin. Maturitas 43, 195–206.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Takeda, T. (1999). Senescence accelerated mouse (SAM): a biogerontological resource in aging research. Neurobiol. Aging 20, 105–110.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Twist, S. J. , Tayleor, G. A. , and Weddell, A. (2000). Brain estradiol and testosterone levels in Alzheimer’s disease. Neurosci. Lett. 286, 1–4.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Vermeulen, A. , Deslypere, J. P. , and Kaufman, J. M. (1989). Influence of antiopioids on luteinizing hormone pulsatility in aging men. J. Clin. Endocrinol. Metab. 68, 68–72.
| PubMed |
Walczewska, A. , Dziedzic, B. , Jakubowska, B. , and Traczyk, W. Z. (1996). Gonadotropin-releasing hormone (GnRH) content in the medial basal hypothalamus after substance P injection into the 3rd cerebral ventricle in female rats. Endocr. Regul. 30, 99–107.
| PubMed |
Warren, M. P. , and Perlroth, N. E. (2001). The effects of intense exercise on the female reproductive system. J. Endocrinol. 170, 3–11.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Wei, X. L. (2000). Studies on learning and memory function-related genes in the hippocampus and the relationship between the cognitive enhancing effect of Liuwei Dihuang decoction (LW) and gene expression. Sheng Li Ke Xue Jin Zhan 31, 227–230.[In Chinese]
| PubMed |
Wei, X. L. , Zhang, Y. X. , and Zhou, J. H. (1999). Alzheimer’s disease-related gene expression in the brain of senescence accelerated mouse (SAM). Neurosci. Lett. 268, 139–142.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Wolf, O. T. (2003). Cognitive functions and sex steroids. Ann. Endocrinol. (Paris) 64, 158–161.
| PubMed |
Zhao, Y. F. , Jiang, X. Z. , Liu, Y. , Miao, L. , Hu, S. H. , Ye, T. J. , Zhao, Y. , and Song, C. Y. (2002). Clinical investigation of neuropeptides in patients with trigeminal neuralgia. J. Pract. Stomatol. 18, 71–74.
