BMC Neuroscience | |
Pheromonal bile acid 3-ketopetromyzonol sulfate primes the neuroendocrine system in sea lamprey | |
Weiming Li2  Nicholas S Johnson1  Hong Wu4  Mara B Bryan5  Michael J Siefkes3  Huiyong Wang2  Yu-Wen Chung-Davidson2  | |
[1] Present address: USGS, Great Lakes Science Center, Hammond Bay Biological Station, 11188 Ray Road, Millersburg, MI, 49759, USA;Department of Fisheries and Wildlife, Michigan State University, 13 Natural Resources Building, 480 Wilson Road, East Lansing, MI, 48824, USA;Present address: Great Lakes Fishery Commission, 2100 Commonwealth Blvd., Suite 100, Ann Arbor, MI, 48105, USA;Present address: Department of Microbiology & Immunology, School of Medicine, Emory University, Rollins Research Center G214, 201 Dowman Drive, Atlanta, Georgia, 30322, USA;Present address: Energy Biosciences Institute, University of California, 130 Calvin Laboratory, MC 5230, Berkeley, CA, 94720, USA | |
关键词: Sexual dimorphism; Steroid; GnRH; HPG axis; Priming; Pheromone; | |
Others : 1140528 DOI : 10.1186/1471-2202-14-11 |
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received in 2012-09-11, accepted in 2013-01-15, 发布年份 2013 | |
【 摘 要 】
Background
Vertebrate pheromones are known to prime the endocrine system, especially the hypothalamic-pituitary-gonadal (HPG) axis. However, no known pheromone molecule has been shown to modulate directly the synthesis or release of gonadotropin releasing hormone (GnRH), the main regulator of the HPG axis. We selected sea lamprey (Petromyzon marinus) as a model system to determine whether a single pheromone component alters the output of GnRH.
Sea lamprey male sex pheromones contain a main component, 7α, 12α, 24-trihydroxy-5α-cholan-3-one 24-sulfate (3 keto-petromyzonol sulfate or 3kPZS), which has been shown to modulate behaviors of mature females. Through a series of experiments, we tested the hypothesis that 3kPZS modulates both synthesis and release of GnRH, and subsequently, HPG output in immature sea lamprey.
Results
The results showed that natural male pheromone mixtures induced differential steroid responses but facilitated sexual maturation in both sexes of immature animals (χ2 = 5.042, dF = 1, p < 0.05). Exposure to 3kPZS increased plasma 15α-hydroxyprogesterone (15α-P) concentrations (one-way ANOVA, p < 0.05) and brain gene expressions (genes examined: three lamprey (l) GnRH-I transcripts, lGnRH-III, Jun and Jun N-terminal kinase (JNK); one-way ANOVA, p < 0.05), but did not alter the number of GnRH neurons in the hypothalamus in immature animals. In addition, 3kPZS treatments increased lGnRH peptide concentrations in the forebrain and modulated their levels in plasma. Overall, 3kPZS modulation of HPG axis is more pronounced in immature males than in females.
Conclusions
We conclude that a single male pheromone component primes the HPG axis in immature sea lamprey in a sexually dimorphic manner.
【 授权许可】
2013 Chung-Davidson et al; licensee BioMed Central Ltd.
【 预 览 】
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【 参考文献 】
- [1]Karlson O, Lüscher M: ‘Pheromones’: a new term for a class of biologically active substances. Nature 1959, 183:55-56.
- [2]Brennan PA, Zufall F: Pheromonal communication in vertebrates. Nature 2006, 444:308-315.
- [3]Rekwot PI, Ogwu D, Oyedipe EO, Sekoni VO: The role of pheromones and biostimulation in animal reproduction. Anim Reprod Sci 2001, 65:157-170.
- [4]Stowers L, Marton TF: What is a pheromone? Mammalian pheromones reconsidered. Neuron 2005, 46:699-702.
- [5]Wyatt T: Pheromones and signature mixtures: defining species-wide signals and variable cues for identity in both invertebrates and vertebrates. J Comp Physiol A 2010, 196:685-700.
- [6]Wysocki CJ, Preti G: Facts, fallacies, fears, and frustrations with human pheromones. Anat Rec Part A 2004, 281A:1201-1211.
- [7]Motofei IG: A dual physiological character for sexual function: libido and sexual pheromones. J Compil BJUI 2009, 104:1702-1708.
- [8]Preti G, Wysocki CJ, Barnhart KT, Sondheimer SJ, Leyden JJ: Male axillary extracts contain pheromones that affect pulsatile secretion of luteinizing hormone and mood in women recipients. Biol Reprod 2003, 68:2107-2113.
- [9]Murata K, Wakabayashi Y, Kitago M, Ohara H, Watanabe H, Tamogami S, Warita Y, Yamagishi K, Ichikawa M, Takeuchi Y, Okamura H, Mori Y: Modulation of gonadotrophin-releasing hormone pulse generator activity by the pheromone in small ruminants. J Neuroendocrinol 2009, 21:346-350.
- [10]Okamura H, Murata K, Sakamoto K, Wakabayashi Y, Ohkura S, Takeuchi Y, Mori Y: Male effect pheromone tickles the gonadotrophin-releasing hormone pulse generator. J Neuroendocrinol 2010, 22:825-832.
- [11]Yu KL, Peng C, Peter RE: Changes in brain levels of gonadotropin-releasing hormone and serum levels of gonadotropin and growth hormone in goldfish during spawning. Can J Zool 1989, 69:182-188.
- [12]Zhang W, Stacey NE: A steroidal pheromone and spawning stimuli act via different neuroendocrine mechanisms to increase gonadotropin and milt volume in male goldfish Carassius auratus. Gen Comp Endocrinol 1997, 105:228-238.
- [13]Sower SA: The endocrinology of reproduction in lampreys and applications for lamprey sterilization. J Great Lakes Res 2003, 29:50-65.
- [14]Li W, Scott AP, Siefkes MJ, Yan HG, Liu Q, Yun SS, Gage DA: Bile acid secreted by mate sea lamprey that acts as a sex pheromone. Science 2002, 296:138-141.
- [15]Li K, Siefkes MJ, Brant CO, Li W: Isolation and identification of petromyzesterosterol, a polyhydroxysteroid from sexually mature male sea lamprey (Petromyzon marinus L.). Steroids 2012, 77:806-810.
- [16]Sorensen PW, Fine JM, Dvornikovs V, Jeffrey CS, Shao F, Wang J, Vrieze LA, Anderson KR, Hoye TR: Mixture of new sulfated steroids functions as a migratory pheromone in the sea lamprey. Nat Chem Biol 2005, 1:324-328.
- [17]Yun SS, Scott AP, Li W: Pheromones of the male sea lamprey, Petromyzon marinus L.: structural studies on a new compound, 3-keto allocholic acid, and 3-keto petromyzonol sulfate. Steroids 2003, 68:297-304.
- [18]Hardisty MW: The significance of lampreys for biological research. Endeavour 1983, 7:110-115.
- [19]Kuratani S, Kuraku S, Murakami Y: Lamprey as an evo-devo model: lessons from comparative embryology and molecular phylogenetics. Genesis 2002, 34:175-183.
- [20]Applegate VC: Natural history of the sea lamprey (Petromyzon marinus) in Michigan. In US Fish and Wildlife Service Special Science Report on Fishery Service 1950, 55:237.
- [21]Hardisty MW, Potter IC: The general biology of adult lampreys. In The biology of lampreys. Volume 1. Edited by Hardisty MW, Potter IC. New York: Academic Press; 1971:127-206.
- [22]Youson JH, Potter IC: A description of the stages in the metamorphosis of the anadromous sea lamprey, Petromyzon marinus L. Can J Zool 1979, 57:1808-1817.
- [23]Potter IC, Gill HS: Adaptive radiation of lampreys. J Great Lakes Res 2003, 29(Suppl 1):95-112.
- [24]Siefkes MJ, Scott AP, Zielinski B, Yun S-S, Li W: Male sea lampreys, Petromyzon marinus L., excrete a sex pheromone from gill epithelia. Biol Reprod 2003, 69:125-132.
- [25]Siefkes MJ, Li W: Electrophysiological evidence for detection and discrimination of pheromonal bile acids by the olfactory epithelium of female sea lampreys (Petromyzon marinus). J Comp Physiol A 2004, 190:193-199.
- [26]Johnson NS, Yun S-S, Thompson HT, Brant CO, Li W: A synthesized pheromone induces upstream movement in female sea lamprey and summons them into traps. PNAS 2009, 106:1021-1026.
- [27]Li W, Scott AP, Siefkes MJ, Yun SS, Zielinski BS: A male pheromone in the sea lamprey (Petromyzon marinus): an overview. Fish Physiol Biochem 2003, 28:259-262.
- [28]Siefkes MJ, Winterstein SR, Li W: Evidence that 3-keto petromyzonol sulphate specifically attracts ovulating female sea lamprey, Petromyzon marinus. Anim Behav 2005, 70:1037-1045.
- [29]Reed KL, MacIntyre JK, Tobet SA, Trudeau VL, MacEachern L, Rubin BS, Sower SA: The spatial relationship of γ-aminobutyric acid (GABA) neurons and gonadotropin-releasing hormone (GnRH) Neurons in larval and adult sea lamprey, Petromyzon marinus. Brain Behav Evol 2002, 60:1-12.
- [30]Nozaki M, Ominato K, Gorbman A, Sower SA: The distribution of lamprey GnRH-III in brains of adult sea lampreys (Petromyzon marinus). Gen Comp Endocrinol 2000, 118:57-67.
- [31]Sørensen PW, Scott AP: The evolution of hormonal sex pheromones in teleost fish: poor correlation between the pattern of steroid release by goldfish and olfactory sensitivity suggests that these cues evolved as a result of chemical spying rather than signal specialization. Acta Physiol Scand 1994, 152:191-205.
- [32]Koyama S: Primer: effects by conspecific odors in house mice: a new perspective in the study of primer effects on reproductive activities. Horm Behav 2004, 46:303-310.
- [33]Misgeld U, Zeilhofer HU, Swandulla D: Synaptic modulation of oscillatory activity of hypothalamic neuronal networks in vitro. Cell Mol Neurobiol 1998, 18:29-43.
- [34]Caraty A, Evans NP, Fabre-Nys CJ, Karsch FJ: The preovulatory gonadotropin-releasing hormone surge: a neuroendocrine signal for ovulation. J Reprod Fertil Suppl 1995, 49:245-255.
- [35]Christian CA, Moenter SM: Critical roles for fast synaptic transmission in mediating estradiol negative and positive feedback in the neural control of ovulation. Endocrinol 2008, 149:5500-5508.
- [36]Ping L, Mahesh VB, Bhat GK, Brann DW: Regulation of gonadotropin-releasing hormone and luteinizing hormone secretion by AMPA receptors. Evidence for a physiological role of AMPA receptors in the steroid-induced luteinizing hormone surge. Neuroendocrinol 1997, 66:246-253.
- [37]Lee WS, Smith MS, Hoffman GE: Luteinizing hormone-releasing hormone neurons express Fos protein during proestrous surge of luteinizing hormone. PNAS 1990, 87:5163-5167.
- [38]Lee WS, Abbud R, Smith MS, Hoffman GE: LHRH neurons express c-Jun protein during proestrous surge of luteinizing hormone. Endocrinol 1992, 130:3101-3103.
- [39]Park OK, Gugneja S, Mayo KE: Gonadotropin-releasing hormone gene expression during the rat estrous cycle: effect of pentobarbital and ovarian steroids. Endocrinol 1990, 127:365-372.
- [40]Zoeller RT, Young WS: Changes in cellular levels of messenger ribonucleic acid encoding gonadotropin-releasing hormone in the anterior hypothalamus of female rats during the estrous cycle. Endocrinol 1988, 123:1688-1689.
- [41]Gore AC, Roberts JL: Regulation of gonadotropin-releasing hormone gene expression in the rat during the luteinizing hormone surge. Endocrinol 1995, 136:889-896.
- [42]King JC, Sower SA, Anthony EL: Neuronal systems immunoreactive with antiserum to lamprey gonadotropin-releasing hormone in the brain of Petromyzon marinus. Cell Tissue Res 1988, 253:1-8.
- [43]Zohar Y, Muñoz-Cueto JA, Elizur A, Kah O: Neuroendocrinology of reproduction in teleost fish. Gen Comp Endocrinol 2010, 165:438-455.
- [44]Sower SA, Moriyama S, Kasaraha M, Takahashi A, Nozaki M, Uchida K, Dahlstrom JM, Kawauchi H: Identification of sea lamprey GTHβ-like cDNA and its evolutionary implications. Gen Comp Endocrinol 2006, 148:22-32.
- [45]Sower SA: Gonadotropin-releasing hormone in primitive fishes. Prog Clin Biol Res 1990, 342:73-78.
- [46]Sower SA: Neuroendocrine control of reproduction in lampreys. Fish Physiol Biochem 1990, 8:365-374.
- [47]Deragon KL, Sower SA: Effects of lamprey gonadotropin-releasing hormone-III on steroidogenesis and spermiation in male sea lampreys. Gen Comp Endocrinol 1994, 95:363-367.
- [48]Gazourian L, Derragon KL, Chase CF, Pati D, Habibi HR, Sower SA: Characteristics of GnRH binding in the gonads and effects of lamprey GnRH-I and -III on reproduction in the adult sea lamprey. Gen Comp Endocrinol 1997, 108:327-339.
- [49]Sower SA, Chiang YC, Lovas S, Conlon JM: Primary structure and biological activity of a third gonadotropin-releasing hormone from lamprey brain. Endocrinol 1993, 132:1125-1131.
- [50]Tobet SA, Nozaki M, Youson JH, Sower SA: Distribution of lamprey gonadotropin releasing hormone-III (GnRH-III) in brains in larval lampreys (Petromyzon marinus). Cell Tissue Res 1995, 279:261-267.
- [51]Wright GM, McBurney KM, Youson JH, Sower SA: Distribution of lamprey gonadotropin-releasing hormone in the brain and pituitary of larval, metamorphic and adult sea lamprey, Petromyzon marinus. Can J Zool 1994, 72:48-53.
- [52]Sower SA, Kawauchi H: Update: brain and pituitary hormones of lampreys. Comp Biochem Physiol 2001, 129:291-302.
- [53]Chung-Davidson Y-W, Bryan MB, Teeter J, Bedore CN, Li W: Neuroendocrine and behavioral responses to weak electric fields in adult sea lampreys (Petromyzon marinus). Horm Behav 2008, 54:34-40.
- [54]Dellovade T, Schwanzel-Fukuda M, Gordan J, Pfaff D: Aspects of GnRH neurobiology conserved across vertebrate forms. Gen Comp Endocrinol 1998, 112:276-282.
- [55]Stern K, McClintock MK: Regulation of ovulation by human pheromones. Nature 1998, 392:177-179.
- [56]Burger LL, Haisenleder DJ, Dalkin AC, Marshall JC: Regulation of gonadotropin subunit gene transcription. J Mol Endocrinol 2004, 33:559-584.
- [57]Bonfil D, Chuderland D, Kraus S, Shahbazian D, Friedberg I, Seger R, Naor Z: Extracellular signal-regulated kinase, Jun N-terminal kinase, p38, and c-Src are involved in gonadotropin-releasing hormone-stimulated activity of the glycoprotein hormone follicle-stimulating hormone β-subunit promoter. Endocrinol 2004, 145:2228-2244.
- [58]Burger LL, Haisenleder DJ, Aylor KW, Marshall JC: Regulation of Lhb and Egr1 gene expression by GnRH pulses in rat pituitaries is both c-Jun N-terminal kinase (JNK)- and extracellular signal-regulated kinase (ERK)-dependent. Biol Reprod 2009, 81:1206-1215.
- [59]Haisenleder DJ, Burger LL, Walsh HE, Stevens J, Aylor KW, Shupnik MA, Marshall JC: Pulsatile gonadotropin-releasing hormone stimulation of gonadotropin subunit transcription in rat pituitaries: evidence for the involvement of Jun N-terminal kinase but not p38. Endocrinol 2008, 149:139-145.
- [60]Harris D, Bonfil D, Chuderland D, Kraus S, Seger R, Naor Z: Activation of MAPK cascades by GnRH: ERK and Jun N-terminal kinase are involved in basal and GnRH-stimulated activity of the glycoprotein hormone LHβ-subunit promoter. Endocrinol 2002, 143:1018-1025.
- [61]Yokoi T, Ohmichi M, Tasaka K, Kimura A, Kanda Y, Hayakawa J, Tahara M, Hisamoto K, Kurachi H, Murata Y: Activation of the luteinizing hormone β promoter by gonadotropin-releasing hormone requires c-Jun NH2-terminal protein kinase. J Biol Chem 2000, 275:21639-21647.
- [62]Fahien CM, Sower SA: Relationship between brain gonadotropin-releasing hormone and final reproductive period of the adult male sea lamprey, Petromyzon marinus. Gen Comp Endocrinol 1990, 80:427-437.
- [63]Millar RP, King JA: Structure and functional evolution of gonadotropin-releasing hormone. Int Rev Cytol 1987, 106:149-182.
- [64]Nozaki M, Gorbman A, Sower SA: Diffusion between the neurophysis and the adenohypophysis of lampreys, Petromyzon marinus. Gen Comp Endocrinol 1994, 96:385-391.
- [65]Sower SA, Balz E, Aquilina-Beck A, Kavanaugh SI: Seasonal changes of brain GnRH-I, -II, and -III during the final reproductive period in adult male and female sea lamprey. Gen Comp Endocrinol 2011, 170:276-282.
- [66]Gazourian L, Evans EL, Hanson L, Chase CF, Sower SA: The effects of lamprey GnRH-I, -III and analogs on steroidogenesis in the sea lamprey (Petromyzon marinus). Aquaculture 2000, 188:147-165.
- [67]Bolduc TG, Sower SA: Changes in brain gonadotropin-releasing hormone, plasma estradiol 17-beta, and progesterone during the final reproductive cycle of the female sea lamprey, Petromyzon marinus. J Exp Zool 1992, 264:55-63.
- [68]Kavanaugh SI, Nozaki M, Sower SA: Origins of gonadotropin-releasing hormone (GnRH) in vertebrates: identification of a novel GnRH in a basal vertebrate, the sea lamprey. Endocriol 2008, 149:3860-3869.
- [69]Zhang L, Tello JA, Zhang W, Tsai P-S: Molecular cloning, expression pattern, and immunocytochemical localization of a gonadotropin-releasing hormone-like molecule in the gastropod mollusk, Aplysia californica. Gen Comp Endocrinol 2008, 126:201-209.
- [70]Gorbman A, Whiteley A, Kavanaugh S: Pheromonal stimulation of spawning release of gametes by gonadotropin releasing hormone in the chiton, Mopalia sp. Gen Comp Endocrinol 2003, 131:62-65.
- [71]Bryan MB, Scott AP, Cerny I, Young BA, Li W: 15 Alpha-hydroxyprogesterone in male sea lampreys, Petromyzon marinus L. Steroids 2004, 69:473-481.
- [72]Bryan MB, Young BA, Close DA, Semeyn J, Robinson TC, Bayer J, Li W: Comparison of synthesis of 15 alpha-hydroxylated steroids in males of four North American lamprey species. Gen Comp Endocrinol 2006, 146:149-156.
- [73]Hanson LH, Manion PJ: Sterility method of pest-control and its potential role in an integrated sea lamprey (Petromyzon marinus) control program. Can J Fish Aquat Sci 1980, 37:2108-2117.
- [74]Suzuki K, Gamble RL, Sower SA: Multiple transcripts encoding lamprey gonadotropin-releasing hormone-I precursors. J Mol Endocrinol 2000, 24:365-376.
- [75]Nieuwenhuys R, Nicholson C: Lampreys, Petromyzontoidea. In The Central Nervous System of Vertebrates. Volume 1. Edited by Nieuwenhuys R, ten Donkelaar HJ, Nicholson C. Heidelberg: Springer-Verlag; 1998:397-495.