Reproductive responses of male Brandt's voles (Lasiopodomys brandtii) to 6-methoxybenzoxazolinone (6-MBOA) under short photoperiod

详细信息    查看全文

• 作者：Xin Dai ; Lian Yu Jiang ; Mei Han ; Man Hong Ye ; Ai Qin Wang…
• 关键词：Brandt’s vole ; 6 ; MBOA ; Reproductive activity ; KiSS ; 1/GPR54 system
• 刊名：Naturwissenschaften
• 出版年：2016
• 出版时间：April 2016
• 年：2016
• 卷：103
• 期：3-4
• 全文大小：1,756 KB
• 参考文献：Alibhai SK (1986) Reproductive response of Gerbillus harwoodii to 6-MBOA in Kora National Reserve. J Trop Ecol 2:377–379CrossRef
  Anderson KD, Nachman RJ, Turek FW (1988) Effects of melatonin and 6-methoxybenzoxazolinone on photoperiodic control of testis size in adult male golden hamsters. J Pineal Res 5:351–365CrossRef PubMed
  Ansel L, Bolborea M, Bentsen AH, Klosen P, Mikkelsen JD, Simonneaux V (2010) Differential regulation of kiss1 expression by melatonin and gonadal hormones in male and female Syrian hamsters. J Biol Rhythm 25:81–91CrossRef
  Argandoña VH, Niemeyer HM, Corcuera LJ (1981) Effect of content and distribution of hydroxamic acids on infestation in the aphid Schizaphis graminum. Phytochemistry 20:673–676CrossRef
  Ball GF (1993) The neural integration of environmental information by seasonally breeding birds. Am Zool 33:185–199CrossRef
  Berger P, Sanders EH, Gardner PD, Negus NC (1977) Phenolic plant compounds functioning as reproductive inhibitors in Microtus montanus. Science 195:575577CrossRef
  Berger PJ, Negus NC, Sanders EH, Gardner PD (1981) Chemical triggering of reproduction in Microtus montanus. Science 214:69–70CrossRef PubMed
  Berger PJ, Negus NC, Rowsemitt CN (1987) Effect of 6-methoxybenzoxazolinone on sex ratio and breeding performance in Microtus montanus. Biol Reprod 36:255–260CrossRef PubMed
  Butterstein GM, Schadler MH (1988) The plant metabolite 6-methoxybenzoxazolinone interacts with follicle-stimulating hormone to enhance ovarian growth. Biol Reprod 39:465–471CrossRef PubMed
  Butterstein GM, Schadler MH, Lysogorski E, Robin L, Sipperly S (1985) A naturally occurring plant compound, 6-methoxybenzoxazolinone, stimulates reproductive responses in rats. Biol Reprod 32:1018–1023CrossRef PubMed
  Clarkson J, Herbison AE (2006) Postnatal development of kisspeptin neurons in mouse hypothalamus; sexual dimorphism and projections to gonadotropin releasing hormone neurons. Endocrinology 147:5817–5825CrossRef PubMed
  Clarkson J, D’Anglemont de Tassigny X, Colledge WH, Caraty A, Herbison AE (2009) Distribution of Kisspeptin neurones in the adult female mouse brain. J Neuroendocrinol 21:673–682CrossRef PubMed
  Dai X, Zhang YQ, Jiang LY, Yuan F, Wang AQ, Wei WH, Yang SM (2014) Evaluation of the variations in secondary metabolite concentrations of Leymus chinensis seedlings. Israel J Ecol Evol 60:75–84CrossRef
  de Roux N, Genin E, Carel JC, Matsuda F, Chaussain JL, Milgrom E (2003) Hypogonadotropic hypogonadism due to loss of function of the KiSS1-derived peptide receptor GPR54. Proc Natl Acad Sci U S A 100:10972–10976CrossRef PubMed PubMedCentral
  Diedrich V, Scherbarth F, Jähnig S, Kastens S, Steinlechner S (2014) Djungarian hamsters (Phodopus sungorus) are not susceptible to stimulating effects of 6-methoxy-2-benzoxazolinone on reproductive organs. Naturwissenschaften 101:115–121CrossRef PubMed
  Ellis LC (1972) Inhibition of rat testicular androgen synthesis in vitro by melatonin and serotonin. Endocrinology 90:17–28CrossRef PubMed
  Freeland WJ, Janzen DH (1974) Strategies in herbivory by mammals: the role of plant secondary compounds. Am Nat 269-289
  Funes S, Hedrick JA, Vassileva G, Markowitz L, Abbondanzo S, Golovko A, Yang S, Monsma FJ, Gustafson EL (2003) The KiSS-1 receptor GPR54 is essential for the development of the murine reproductive system. Biochem Biophys Res Commun 312:1357–1363CrossRef PubMed
  Gehm BD, McAndrews JM, Chien PY, Jameson JL (1997) Resveratrol, a polyphenolic compound found in grapes and wine, is an agonist for the estrogen receptor. Proc Natl Acad Sci U S A 94:14138–14143CrossRef PubMed PubMedCentral
  Ginther OJ, Bergfelt DR, Scraba ST, Pivonka PR, Nuti LC (1985) Effects of 6-MBOA on reproductive function in ponies, mice, rats and mink. Theriogenology 24:587–595CrossRef PubMed
  Gower BA, Berger PJ (1990) Reproductive responses of male Microtus montanus to photoperiod, melatonin, and 6-MBOA. J Pineal Res 8:297–312CrossRef PubMed
  Hegab IM, Shang G, Ye M, Jin Y, Wang A, Yin B, Yang S, Wei W (2014) Defensive responses of Brandt’s voles (Lasiopodomys brandtii) to chronic predatory stress. Physiol Behav 126:1–7CrossRef PubMed
  Hughes CL Jr (1988) Phytochemical mimicry of reproductive hormones and modulation of herbivore fertility by phytoestrogens. Environ Health Perspect 78:171–175CrossRef PubMed PubMedCentral
  Kauffman AS, Gottsch ML, Roa J, Byquist AC, Crown A, Clifton DK, Tena-Sempere M (2007) Sexual differentiation of KiSS1 gene expression in the brain of the rat. Endocrinology 148:1774–1783CrossRef PubMed
  Korn H, Taitt MJ (1987) Initiation of early breeding in a population of Microtus townsendii (Rodentia) with the secondary plant compound 6-MBOA. Oecologia 71:593–596CrossRef
  Król E, Douglas A, Dardente H, Birnie MJ, van der Vinne V, Eijer WG, Gerkema MP, Hazlerigg DG, Hut RA (2012) Strong pituitary and hypothalamic responses to photoperiod but not to 6-methoxy-2-benzoxazolinone in female common voles (Microtus arvalis). Gen Comp Endocrinol 179:289–295CrossRef PubMed
  Larkin MA, Blackshields G, Brown NP, Chenna R, McGettigan PA, McWilliam H, Valentin F, Wallace IM, Wilm A, Lopez R, Thompson JD, Gibson TJ, Higgins DG (2007) Clustal W and Clustal X version 2.0. Bioinformatics 23:2947–2948CrossRef PubMed
  Lefever S, Vandesompele J, Speleman F, Pattyn F (2009) RTPrimerDB: the portal for real-time PCR primers and probes. Nucleic Acids Res 37:942–945CrossRef
  Leopold AS, Erwin M, Oh J, Browning B (1976) Phytoestrogens: adverse effects on reproduction in California quail. Science 191:98–100CrossRef PubMed
  Li XF, Kinsey-Jones JS, Cheng Y, Knox AM, Lin Y, Petrou NA, Roseweir A, Lightman SL, Milligan SR, Millar RP, O’Byrne KT (2009) Kisspeptin signalling in the hypothalamic arcuate nucleus regulates GnRH pulse generator frequency in the rat. PLoS One 4:e8334CrossRef PubMed PubMedCentral
  Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2−ΔΔCT method. Methods 25:402–408CrossRef PubMed
  Martin LB, Johnson EM, Hutch CR, Nelson RJ (2008) 6-MBOA affects testis size, but not delayed-type hypersensitivity, in white-footed mice (Peromyscus leucopus). Comp Biochem Physiol A 149:181–187CrossRef
  Meek LR, Lee TM, Gallon JF (1995) Interaction of maternal photoperiod history and food type on growth and reproductive development of laboratory meadow voles (Microtus pennsylvanicus). Physiol Behav 57:905–911CrossRef PubMed
  Mikkelsen JD, Simonneaux V (2009) The neuroanatomy of the Kisspeptin system in the mammalian brain. Peptides 30:26–33CrossRef PubMed
  Mitchell JH, Gardner PT, McPhail DB, Morrice PC, Collins AR, Duthie GG (1998) Antioxidant efficacy of phytoestrogens in chemical and biological model systems. Arch Biochem Biophys 360:142–148CrossRef PubMed
  Moffatt CA, Bennett SA, Nelson RJ (1991) Effects of photoperiod and 6-methoxy-2-benzoxazolinone on male-induced estrus in prairie voles. Physiol Behav 49:27–31CrossRef PubMed
  Negus NC, Berger PJ (1977) Experimental triggering of reproduction in a natural population of Microtus montanus. Science 196:1230–1231CrossRef PubMed
  Negus NC, Berger PJ (1987) Mammalian reproductive physiology: adaptive responses to changing environments. In: Current mammalogy. Springer US, pp 149–173
  Nelson RJ, Shiber JR (1990) Photoperiod affects reproductive responsiveness to 6-methoxy-2-benzoxazolinone in house mice. Biol Reprod 43:586–591CrossRef PubMed
  Niemeyer HM (1988) Hydroxamic acids (4-hydroxy-1,4-benzoxazin-3-ones), defence chemicals in the gramineae. Phytochemistry 27:3349–3358CrossRef
  Oakley AE, Clifton DK, Steiner RA (2009) Kisspeptin signaling in the brain. Endocr Rev 30:713–743CrossRef PubMed PubMedCentral
  Okamura H, Murata K, Sakamoto K, Wakabayashi Y, Ohkura S, Takeuchi Y, Mori Y (2010) Male effect pheromone tickles the gonadotrophin-releasing hormone pulse generator. J Neuroendocrinol 22:825–832CrossRef PubMed
  O’Shaughnessy PJ, Willerton L, Baker PJ (2002) Changes in Leydig cell gene expression during development in the mouse. Biol Reprod 66:966–975CrossRef PubMed
  Paul MJ, Zucker I, Schwartz WJ (2008) Tracking the seasons: the internal calendars of vertebrates. Philos Trans R Soc Lond B Biol Sci 363:341–361CrossRef PubMed PubMedCentral
  Paul MJ, Pyter LM, Freeman DA, Galang J, Prendergast BJ (2009) Photic and nonphotic seasonal cues differentially engage hypothalamic Kisspeptin and RFamide-related peptide mRNA expression in Siberian hamsters. J Neuroendocrinol 21:1007–1014CrossRef PubMed PubMedCentral
  Payne AH, Hales DB (2004) Overview of steroidogenic enzymes in the pathway from cholesterol to active steroid hormones. Endocr Rev 25:947–970CrossRef PubMed
  Peat F, Kinson GA (1971) Testicular steroidogenesis in vitro in the rat in response to blinding, pinealectomy and to the addition of melatonin. Steroids 17:251–284CrossRef PubMed
  Popa SM, Clifton DK, Steiner RA (2008) The role of kisspeptins and GPR54 in the neuroendocrine regulation of reproduction. Annu Rev Physiol 70:213–238CrossRef PubMed
  Reiter RJ (1980) The pineal and its hormones in the control of reproduction in mammals. Endocr Rev 1:109–131CrossRef PubMed
  Reiter RJ, Blask DE, Johnson LY, Rudeen PK, Vaughan MK, Waring PJ (1976) Melatonin inhibition of reproduction in the male hamster: its dependency on time of day of administration and on an intact and sympathetically innervated pineal gland. Neuroendocrinology 22:107–116CrossRef PubMed
  Revel FG, Saboureau M, Masson-Pevet M, Pevet P, Mikkelsen JD, Simonneaux V (2006) Kisspeptin mediates the photoperiodic control of reproduction in hamsters. Curr Biol 16:1730–5CrossRef PubMed
  Rose TM (2005) CODEHOP-mediated PCR—a powerful technique for the identification and characterization of viral genomes. Virol J 2:3763–6CrossRef
  Rowsemitt CN, O’Connor AJ (1989) Reproductive function in Dipodomys ordii stimulated by 6-methoxybenzoxazolinone. J Mammal 70:805–809CrossRef
  Sanders EH, Gardner PD, Berger PJ, Negus NC (1981) 6-methoxybenzoxazolinone: a plant derivative that stimulates reproduction in Microtus montanus. Science 214:67–69CrossRef PubMed
  Schadler MH, Butterstein GM, Faulkner BJ, Rice SC, Weisinger LA (1988) The plant metabolite, 6-methoxybenzoxazolinone, stimulates an increase in secretion of follicle-stimulating hormone and size of reproductive organs in Microtus pinetorum. Biol Reprod 38:817–820CrossRef PubMed
  Shi DZ, Hai SZ, Lu D, Liu XL (1999) The structure and order in colony of Brandt’s vole. Acta Theriol Sin 19:48–55
  Smith JT, Cunningham MJ, Rissman EF, Clifton DK, Steiner RA (2005a) Regulation of Kiss1 gene expression in the brain of the female mouse. Endocrinology 146:3686–3692CrossRef PubMed
  Smith JT, Dungan HM, Stoll EA, Gottsch ML, Braun RE, Eacker SM, Clifton DK, Steiner RA (2005b) Differential regulation of KiSS-1 mRNA expression by sex steroids in the brain of the male mouse. Endocrinology 146:2976–2984CrossRef PubMed
  Smith JT, Clifton DK, Steiner RA (2006) Regulation of the neuroendocrine reproductive axis by kisspeptin-GPR54 signaling. Reproduction 131:623–630CrossRef PubMed
  Stocco DM (2001) StAR protein and the regulation of steroid hormone biosynthesis. Annu Rev Physiol 63:193–213CrossRef PubMed
  Sweat FW, Berger PJ (1988) Uterotropic 6-methoxybenzoxazolinone is an adrenergic agonist and a melatonin analog. Mol Cell Endocrinol 57:131–138CrossRef PubMed
  Vaughan MK, Little JC, Vaughant GM, Reiter RJ (1988) Hormonal consequences of subcutaneous 6-methoxy-2-benzoxazolinone pellets or injections in prepubertal male and female rats. J Reprod Fertil 83:859–866CrossRef PubMed
  Wakabayashi Y, Nakada T, Murata K, Ohkura S, Mogi K, Navarro VM, Clifton DK, Mori Y, Tsukamura H, Maeda K, Steiner RA, Okamura H (2010) Neurokinin B and dynorphin A in kisspeptin neurons of the arcuate nucleus participate in generation of periodic oscillation of neural activity driving pulsatile gonadotropin-releasing hormone secretion in the goat. J Neurosci Nurs 30:3124–3132CrossRef
  Wan XR, Wang MJ, Wang GH, Liu W, Zhong WQ (2002) The reproductive parameters in the marked populations of Brandt’s vole. Acta Theriol Sin 22:116–122
  Wang GM, Zhou QQ, Zhong WQ, Wang GH (1992) Food habits of Brandt’s vole (Microtus brandti). Acta Theriol Sin 12:57–64
  Willard ST, Dickerson T, Dodson R, Weis A, Godfrey RW (2006) Administration of 6-methoxybenzoxazolinone (MBOA) does not augment ovulatory responses in St. Croix White ewes superovulated with PMSG. Anim Reprod Sci 93:280–291CrossRef PubMed
  Wynne-Edwards KE (2001) Evolutionary biology of plant defenses against herbivory and their predictive implications for endocrine disruptor susceptibility in vertebrates. Environ Health Perspect 109:443–448CrossRef PubMed PubMedCentral
  Xi W, Lee CKF, Yeung WSB, Giesy JP, Wong MH, Zhang X, Hecker M, Wong CK (2011) Effect of perinatal and postnatal bisphenol A exposure to the regulatory circuits at the hypothalamus–pituitary–gonadal axis of CD-1 mice. Reprod Toxicol 31:409–417CrossRef PubMed
  Xie XM, Sun RY, Fang JM (1994) The mating system and reproduction of Brandt’s voles (Microtus brandtii). Acta Zool Sin 40:262–265
  Yuwiler A, Winters WD (1985) Effects of 6-methoxy-2-benzoxazolinone on the pined melatonin generating system. J Pharmacol Exp Ther 233:45–50PubMed
  Zhang Z, Pech R, Davis S, Shi D, Wan X, Zhong W (2003) Extrinsic and intrinsic factors determine the eruptive dynamics of Brandt’s voles Microtus brandtii in Inner Mongolia China. Oikos 100:299–310CrossRef
  Zhang Q, Lin Y, Zhang XY, Wang DH (2014) Cold exposure inhibits hypothalamic Kiss-1 gene expression, serum leptin concentration, and delays reproductive development in male Brandt’s vole (Lasiopodomys brandtii). Int J Biometeorol 59:679–691CrossRef PubMed
  
• 作者单位：Xin Dai (1) (2)
  Lian Yu Jiang (1)
  Mei Han (1)
  Man Hong Ye (1)
  Ai Qin Wang (1)
  Wan Hong Wei (1) (2)
  Sheng Mei Yang (1) (2)
  
  1. College of Bioscience and Biotechnology, Yangzhou University, 48 East Wenhui Road, Yangzhou, 225009, People’s Republic of China
  2. Jiangsu Co-innovation Center for Prevention and Control of Important Animal Infectious Diseases and Zoonoses, Yangzhou University, Yangzhou, 225009, People’s Republic of China
  
• 刊物类别：Biomedical and Life Sciences
• 刊物主题：Life Sciences
  Life Sciences
  Environment
  
• 出版者：Springer Berlin / Heidelberg
• ISSN：1432-1904

文摘

The plant secondary metabolite 6-methoxybenzoxazolinone (6-MBOA) can stimulate and enhance animal reproduction. This compound has been successfully detected in Leymus chinensis, which is the main diet of Brandt’s voles. The aim of this study was to investigate the effect of different 6-MBOA doses on the reproductive physiology of male Brandt’s voles under a short photoperiod. The results showed that 6-MBOA administration increased relative testis weight, regardless of the dose, but it had little effect on the body mass. Low and middle doses of 6-MBOA increased the concentrations of luteinizing hormone and testosterone in the serum and the mRNA levels of StAR and CYP11a1 in the testes. However, 6-MBOA did not cause any significant increase in the mRNA levels of KiSS-1, GPR54, and GnRH compared to those in the control group. The mRNA level of KiSS-1 in the arcuate nucleus (ARC) was higher than that in the anteroventral periventricular nucleus (AVPV). Collectively, our results demonstrated that the number of KiSS-1-expressing neurons located in the ARC was the highest, and that 6-MBOA, which might modulate the reproductive activity along the hypothalamic-pituitary-gonadal axis, had a dose-dependent stimulatory effect on the reproductive activity of Brandt’s voles under a short photoperiod. Our study provided insights into the mechanism of 6-MBOA action and the factors influencing the onset of reproduction in Brandt’s voles.