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Photoperiodic variations of the polysialylated form of neural cell adhesion molecule within the hypothalamus and related reproductive output in the ewe

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Abstract

Cellular mechanisms induced by melatonin to synchronise seasonal reproduction in several species, including sheep, remain unclear. We sought to evaluate the scale and physiological significance of neural plasticity in order to explain the delay between the change of duration of melatonin secretion and the change of reproductive status following a transition from long days (LD, 16 h light/24 h) to short days (SD, 8 h light/24 h) and from SD to LD. Using Western blots in ovariectomised oestradiol-replaced ewes, we evaluated the content of the polysialylated form of neural cell adhesion molecule (PSA-NCAM), a plasticity marker, in the hypothalamus. From day 15 following a transition to SD, most hypothalamic areas showed a decrease of PSA-NCAM level that was particularly significant in the preoptic area (POA). Following a transition to LD, PSA-NCAM content increased at day 15 in most regions except in the premammillary hypothalamic area (PMH) in which a significant decrease was noted. The functional importance of PSA-NCAM variations for seasonal reproduction was assessed for the PMH and POA. PSA-NCAM was degraded by stereotaxic injections of endoneuraminidase N and luteinising hormone (LH) secretion was recorded in treated and control ewes. Degradation of PSA-NCAM in the PMH in SD-treated ewes failed to produce a significant effect on LH secretion, whereas a similar treatment in the POA before a transition to SD delayed activation of the gonadotroph axis in two-thirds of the ewes. Our results suggest that the photoperiod controls variations of the hypothalamic content of a plasticity marker and that these might be important for the regulation of seasonal reproduction, particularly in the POA.

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References

  • Adams VL, Goodman RL, Salm AK, Coolen LM, Karsch FJ, Lehman MN (2006) Morphological plasticity in the neural circuitry responsible for seasonal breeding in the ewe. Endocrinology 147:4843–4851

    Article  PubMed  CAS  Google Scholar 

  • Anderson GM, Connors JM, Hardy SL, Valent M, Goodman RL (2002) Thyroid hormones mediate steroid-independent seasonal changes in luteinizing hormone pulsatility in the ewe. Biol Reprod 66:701–706

    Article  PubMed  CAS  Google Scholar 

  • Anderson GM, Hardy SL, Valent M, Billings HJ, Connors JM, Goodman RL (2003) Evidence that thyroid hormones act in the ventromedial preoptic area and the premammillary region of the brain to allow the termination of the breeding season in the ewe. Endocrinology 144:2892–2901

    Article  PubMed  CAS  Google Scholar 

  • Barrett P, Ebling FJ, Schuhler S, Wilson D, Ross AW, Warner A, Jethwa P, Boelen A, Visser TJ, Ozanne DM, Archer ZA, Mercer JG, Morgan PJ (2007) Hypothalamic thyroid hormone catabolism acts as a gatekeeper for the seasonal control of body weight and reproduction. Endocrinology 148:3608–3617

    Article  PubMed  CAS  Google Scholar 

  • Billings HJ, Viguie C, Karsch FJ, Goodman RL, Connors JM, Anderson GM (2002) Temporal requirements of thyroid hormones for seasonal changes in LH secretion. Endocrinology 143:2618–2625

    Article  PubMed  CAS  Google Scholar 

  • Bogusz AL, Hardy SL, Lehman MN, Connors JM, Hileman SM, Sliwowska JH, Billings HJ, McManus CJ, Valent M, Singh SR, Nestor CC, Coolen LM, Goodman RL (2008) Evidence that gamma-aminobutyric acid is part of the neural circuit mediating estradiol negative feedback in anestrous ewes. Endocrinology 149:2762–2772

    Article  PubMed  CAS  Google Scholar 

  • Chalivoix S, Bagnolini A, Caraty A, Cognie J, Malpaux B, Dufourny L (2010a) Effects of photoperiod on kisspeptin neuronal populations of the ewe diencephalon in connection with reproductive function. J Neuroendocrinol 22:110–118

    Article  PubMed  CAS  Google Scholar 

  • Chalivoix S, Malpaux B, Dufourny L (2010b) Relationship between polysialylated neural cell adhesion molecule and beta-endorphin- or gonadotropin releasing hormone-containing neurons during activation of the gonadotrope axis in short daylength in the ewe. Neuroscience 169:1326–1336

    Article  PubMed  CAS  Google Scholar 

  • Dardente H, Wyse CA, Birnie MJ, Dupre SM, Loudon AS, Lincoln GA, Hazlerigg DG (2010) A molecular switch for photoperiod responsiveness in mammals. Curr Biol 20:2193–2198

    Article  PubMed  CAS  Google Scholar 

  • Dufourny L, Migaud M, Thiery JC, Malpaux B (2008) Development of an in vivo adeno-associated virus-mediated siRNA approach to knockdown tyrosine hydroxylase in the lateral retrochiasmatic area of the ovine brain. J Neurosci Methods 170:56–66

    Article  PubMed  CAS  Google Scholar 

  • Evans NP, Dahl GE, Glover BH, Karsch FJ (1994) Central regulation of pulsatile gonadotropin-releasing hormone (GnRH) secretion by estradiol during the period leading up to the preovulatory GnRH surge in the ewe. Endocrinology 134:1806–1811

    Article  PubMed  CAS  Google Scholar 

  • Faure MO, Nicol L, Fabre S, Fontaine J, Mohoric N, McNeilly A, Taragnat C (2005) BMP-4 inhibits follicle-stimulating hormone secretion in ewe pituitary. J Endocrinol 186:109–121

    Article  PubMed  CAS  Google Scholar 

  • Glass JD, Shen H, Fedorkova L, Chen L, Tomasiewicz H, Watanabe M (2000) Polysialylated neural cell adhesion molecule modulates photic signaling in the mouse suprachiasmatic nucleus. Neurosci Lett 280:207–210

    Article  PubMed  CAS  Google Scholar 

  • Glass JD, Watanabe M, Fedorkova L, Shen H, Ungers G, Rutishauser U (2003) Dynamic regulation of polysialylated neural cell adhesion molecule in the suprachiasmatic nucleus. Neuroscience 117:203–211

    Article  PubMed  CAS  Google Scholar 

  • Hanon EA, Lincoln GA, Fustin JM, Dardente H, Masson-Pevet M, Morgan PJ, Hazlerigg DG (2008) Ancestral TSH mechanism signals summer in a photoperiodic mammal. Curr Biol 18:1147–1152

    Article  PubMed  CAS  Google Scholar 

  • Jansen HT, Cutter C, Hardy S, Lehman MN, Goodman RL (2003) Seasonal plasticity within the gonadotropin-releasing hormone (GnRH) system of the ewe: changes in identified GnRH inputs and glial association. Endocrinology 144:3663–3676

    Article  PubMed  CAS  Google Scholar 

  • Kaur G, Heera PK, Srivastava LK (2002) Neuroendocrine plasticity in GnRH release during rat estrous cycle: correlation with molecular markers of synaptic remodeling. Brain Res 954:21–31

    Article  PubMed  CAS  Google Scholar 

  • Kennaway DJ, Rowe SA (1995) Melatonin binding sites and their role in seasonal reproduction. J Reprod Fertil Suppl 49:423–435

    PubMed  CAS  Google Scholar 

  • Kiss JZ, Wang C, Olive S, Rougon G, Lang J, Baetens D, Harry D, Pralong WF (1994) Activity-dependent mobilization of the adhesion molecule polysialic NCAM to the cell surface of neurons and endocrine cells. EMBO J 13:5284–5292

    PubMed  CAS  Google Scholar 

  • Kojima N, Yoshida Y, Kurosawa N, Lee YC, Tsuji S (1995) Enzymatic activity of a developmentally regulated member of the sialyltransferase family (STX): evidence for alpha 2,8-sialyltransferase activity toward N-linked oligosaccharides. FEBS Lett 360:1–4

    Article  PubMed  CAS  Google Scholar 

  • Legan SJ, Karsch FJ (1980) Photoperiodic control of seasonal breeding in ewes: modulation of the negative feedback action of estradiol. Biol Reprod 23:1061–1068

    Article  PubMed  CAS  Google Scholar 

  • Legan SJ, Karsch FJ, Foster DL (1977) The endocrine control of seasonal reproductive function in the ewe: a marked change in response to the negative feedback action of estradiol on luteinizing hormone secretion. Endocrinology 101:818–824

    Article  PubMed  CAS  Google Scholar 

  • Lincoln GA, Short RV (1980) Seasonal breeding: nature’s contraceptive. Recent Prog Horm Res 36:1–52

    PubMed  CAS  Google Scholar 

  • Malpaux B, Daveau A, Maurice-Mandon F, Duarte G, Chemineau P (1998) Evidence that melatonin acts in the premammillary hypothalamic area to control reproduction in the ewe: presence of binding sites and stimulation of luteinizing hormone secretion by in situ microimplant delivery. Endocrinology 139:1508–1516

    Article  PubMed  CAS  Google Scholar 

  • Metropolis N, Ulam S (1949) The Monte Carlo method. J Am Stat Assoc 44:335–341

    Article  PubMed  CAS  Google Scholar 

  • Nakao N, Ono H, Yamamura T, Anraku T, Takagi T, Higashi K, Yasuo S, Katou Y, Kageyama S, Uno Y, Kasukawa T, Iigo M, Sharp PJ, Iwasawa A, Suzuki Y, Sugano S, Niimi T, Mizutani M, Namikawa T, Ebihara S, Ueda HR, Yoshimura T (2008) Thyrotrophin in the pars tuberalis triggers photoperiodic response. Nature 452:317–322

    Article  PubMed  CAS  Google Scholar 

  • Ono H, Hoshino Y, Yasuo S, Watanabe M, Nakane Y, Murai A, Ebihara S, Korf HW, Yoshimura T (2008) Involvement of thyrotropin in photoperiodic signal transduction in mice. Proc Natl Acad Sci USA 105:18238–18242

    Article  PubMed  CAS  Google Scholar 

  • Parkash J, Kaur G (2007) Transcriptional regulation of PSA-NCAM mediated neuron-glial plasticity in the adult hypothalamus. Neuron Glia Biol 3:299–307

    Article  PubMed  Google Scholar 

  • Phillips GR, Krushel LA, Crossin KL (1997) Developmental expression of two rat sialyltransferases that modify the neural cell adhesion molecule, N-CAM. Brain Res Dev Brain Res 102:143–155

    Article  PubMed  CAS  Google Scholar 

  • Pompolo S, Pereira A, Kaneko T, Clarke IJ (2003) Seasonal changes in the inputs to gonadotropin-releasing hormone neurones in the ewe brain: an assessment by conventional fluorescence and confocal microscopy. J Neuroendocrinol 15:538–545

    Article  PubMed  CAS  Google Scholar 

  • Rougon G, Dubois C, Buckley N, Magnani JL, Zollinger W (1986) A monoclonal antibody against meningococcus group B polysaccharides distinguishes embryonic from adult N-CAM. J Cell Biol 103:2429–2437

    Article  PubMed  CAS  Google Scholar 

  • Rutishauser U, Watanabe M, Silver J, Troy FA, Vimr ER (1985) Specific alteration of NCAM-mediated cell adhesion by an endoneuraminidase. J Cell Biol 101:1842–1849

    Article  PubMed  CAS  Google Scholar 

  • Sergeeva A, Jansen HT (2009) Neuroanatomical plasticity in the gonadotropin-releasing hormone system of the ewe: seasonal variation in glutamatergic and gamma-aminobutyric acidergic afferents. J Comp Neurol 515:615–628

    Article  PubMed  CAS  Google Scholar 

  • Smith JT, Coolen LM, Kriegsfeld LJ, Sari IP, Jaafarzadehshirazi MR, Maltby M, Bateman K, Goodman RL, Tilbrook AJ, Ubuka T, Bentley GE, Clarke IJ, Lehman MN (2008) Variation in kisspeptin and RFamide-related peptide (RFRP) expression and terminal connections to gonadotropin-releasing hormone neurons in the brain: a novel medium for seasonal breeding in the sheep. Endocrinology 149:5770–5782

    Article  PubMed  CAS  Google Scholar 

  • Tan O, Fadiel A, Chang A, Demir N, Jeffrey R, Horvath T, Garcia-Segura LM, Naftolin F (2009) Estrogens regulate posttranslational modification of neural cell adhesion molecule during the estrogen-induced gonadotropin surge. Endocrinology 150:2783–2790

    Article  PubMed  CAS  Google Scholar 

  • Thiery JC, Martin GB, Tillet Y, Caldani M, Quentin M, Jamain C, Ravault JP (1989) Role of hypothalamic catecholamines in the regulation of luteinizing hormone and prolactin secretion in the ewe during seasonal anestrus. Neuroendocrinology 49:80–87

    Article  PubMed  CAS  Google Scholar 

  • Viguie C, Jansen HT, Glass JD, Watanabe M, Billings HJ, Coolen L, Lehman MN, Karsch FJ (2001) Potential for polysialylated form of neural cell adhesion molecule-mediated neuroplasticity within the gonadotropin-releasing hormone neurosecretory system of the ewe. Endocrinology 142:1317–1324

    Article  PubMed  CAS  Google Scholar 

  • Vimr ER, McCoy RD, Vollger HF, Wilkison NC, Troy FA (1984) Use of prokaryotic-derived probes to identify poly(sialic acid) in neonatal neuronal membranes. Proc Natl Acad Sci USA 81:1971–1975

    Article  PubMed  CAS  Google Scholar 

  • Wagner AP, Reck G, Platt D (1992) Dynamics of gene expression for microtubule-associated protein MAP1B, embryonic alpha-tubulin and late neural beta-tubulin mRNAs in the hippocampus of aged rats. Biochem Biophys Res Commun 184:292–299

    Article  PubMed  CAS  Google Scholar 

  • Watanabe M, Yasuo S, Watanabe T, Yamamura T, Nakao N, Ebihara S, Yoshimura T (2004) Photoperiodic regulation of type 2 deiodinase gene in Djungarian hamster: possible homologies between avian and mammalian photoperiodic regulation of reproduction. Endocrinology 145:1546–1549

    Article  PubMed  CAS  Google Scholar 

  • Xiong JJ, Karsch FJ, Lehman MN (1997) Evidence for seasonal plasticity in the gonadotropin-releasing hormone (GnRH) system of the ewe: changes in synaptic inputs onto GnRH neurons. Endocrinology 138:1240–1250

    Article  PubMed  CAS  Google Scholar 

  • Yasuo S, Nakao N, Ohkura S, Iigo M, Hagiwara S, Goto A, Ando H, Yamamura T, Watanabe M, Watanabe T, Oda S, Maeda K, Lincoln GA, Okamura H, Ebihara S, Yoshimura T (2006) Long-day suppressed expression of type 2 deiodinase gene in the mediobasal hypothalamus of the Saanen goat, a short-day breeder: implication for seasonal window of thyroid hormone action on reproductive neuroendocrine axis. Endocrinology 147:432–440

    Article  PubMed  CAS  Google Scholar 

  • Yoshimura T, Yasuo S, Watanabe M, Iigo M, Yamamura T, Hirunagi K, Ebihara S (2003) Light-induced hormone conversion of T4 to T3 regulates photoperiodic response of gonads in birds. Nature 426:178–181

    Article  PubMed  CAS  Google Scholar 

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Acknowledgments

The authors thank the staff of the assay platform laboratory and of the experimental unit of INRA Centre de Tours (UEPAO) and the staff of the Experimental Hospital (PRC) for their technical help. They also thank S. Formosa and A. Collet for their technical help and Drs. J.-L. Gatti, J.-L. Dacheux, I. Franceschini and S. Fabre for their useful technical comments. They are grateful to Drs. H. Dardente and M. Beltramo for helpful scientific comments regarding the manuscript and to Dr. P. Kohnke for English revision.

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Authors and Affiliations

  1. INRA, UMR85 Physiologie de la Reproduction et des Comportements, 37380, Nouzilly, France

    S. Chalivoix, D. Guillaume, J. Cognié, J. C. Thiéry, B. Malpaux & L. Dufourny

  2. CNRS, UMR 7247, 37380, Nouzilly, France

    S. Chalivoix, D. Guillaume, J. Cognié, J. C. Thiéry, B. Malpaux & L. Dufourny

  3. Université de Tours, 37041, Tours, France

    S. Chalivoix, D. Guillaume, J. Cognié, J. C. Thiéry, B. Malpaux & L. Dufourny

  4. Institut Français du Cheval et de l’Equitation, 37380, Nouzilly, France

    S. Chalivoix, D. Guillaume, J. Cognié, J. C. Thiéry, B. Malpaux & L. Dufourny

  5. Centre INRA de Tours, 37380, Nouzilly, France

    L. Dufourny

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  1. S. Chalivoix
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  2. D. Guillaume
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  3. J. Cognié
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  4. J. C. Thiéry
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  5. B. Malpaux
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  6. L. Dufourny
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Corresponding author

Correspondence to L. Dufourny.

Additional information

S. Chalivoix was the recipient of a Region Centre Ph.D. thesis fellowship.

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ESM 1

Representative Western blots of PSA-NCAM and tubulin showing their respective signals at 200–250 KDa and 50 KDa. Lanes A-J Preoptic area samples from day 0 (A, B), day 15 (C, D), day 30 (E, F), day 45 (G, H) and day 80 (I, J) ewes following a transition to short days. Lane R Control sample from rat hypothalamus. (JPEG 25 kb)

High resolution image (TIFF 3308 kb)

ESM 2

Photomicrographs of representative brain coronal sections at the level of the preoptic area after immunocytochemical detection of PSA-NCAM (stained brown after the DAB reaction) in ewes injected either with 5 μl saline (a) or with 5 μl endoN at 1 week (b) or 3 weeks (c) before being killed (oc optic chiasm, star third ventricle). Bar 470 μm. (JPEG 46 kb)

High resolution image (TIFF 13395 kb)

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Chalivoix, S., Guillaume, D., Cognié, J. et al. Photoperiodic variations of the polysialylated form of neural cell adhesion molecule within the hypothalamus and related reproductive output in the ewe. Cell Tissue Res 352, 387–399 (2013). https://doi.org/10.1007/s00441-012-1544-z

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