Semaphorin7A regulates neuroglial plasticity in the adult hypothalamic median eminence

Nature Communications

Volumn 6, Issue , 2015, Pages

  Parkash, Jyoti ^a,b,j   Messina, Andrea ^a,b   Langlet, Fanny ^a,b   Cimino, Irene ^a,b   Loyens, Anne ^a,b   Mazur, Danièle ^a,b   Gallet, Sarah ^a,b   Balland, Eglantine ^a,b   Malone, Samuel A ^a,b   Pralong, François ^c   Cagnoni, Gabriella ^d,e   Schellino, Roberta ^f   De Marchis, Silvia ^f   Mazzone, Massimiliano ^g,h   Pasterkamp, R Jeroen ⁱ   Tamagnone, Luca ^d,e   Prevot, Vincent ^a,b   Giacobini, Paolo ^a,b  

^a JEAN PIERRE AUBERT RESEARCH CENTER   (France)

^b UNIV LILLE   (France)

^c LAUSANNE UNIVERSITY HOSPITAL   (Switzerland)

^d CANDIOLO CANCER INSTITUTE   (Italy)

^e UNIVERSITY OF TURIN   (Italy)

^f UNIVERSITY OF TURIN   (Italy)

^g DEPARTMENT OF PLANT SYSTEMS BIOLOGY   (Belgium)

^h Vesalius Research Center   (Belgium)

ⁱ UNIVERSITY MEDICAL CENTER UTRECHT   (Netherlands)

^j Department of Biotechnology School of Life Sciences DAV University Jalandhar   (India)

more..

Author keywords

[No Author keywords available]

Indexed keywords

COFILIN; ESTROGEN RECEPTOR ALPHA; ESTROGEN RECEPTOR BETA; FOCAL ADHESION KINASE; GONADORELIN; MESSENGER RNA; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; PLEXIN; PLEXIN C1; PROGESTERONE RECEPTOR A; PROGESTERONE RECEPTOR B; PROTEIN KINASE B; SEMAPHORIN; SEMAPHORIN 7A; TRANSFORMING GROWTH FACTOR BETA1; UNCLASSIFIED DRUG; ESTRADIOL; ESTRADIOL 3-BENZOATE; LEUKOCYTE ANTIGEN; PROGESTERONE; SEMAPHORIN 7A PROTEIN, RAT;

CELL ORGANELLE; GENE EXPRESSION; HORMONE; MAMMAL; NEUROLOGY; NUMERICAL MODEL; PLASTICITY;

ADULT; ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; CONTROLLED STUDY; CYTOSKELETON; DIESTRUS; ESTRUS CYCLE; FEMALE; FEMALE FERTILITY; GENE REARRANGEMENT; GLIA CELL; HYPOTHALAMUS; IMMUNOREACTIVITY; MEDIAN EMINENCE; NERVE CELL PLASTICITY; NERVE ENDING; NONHUMAN; OVARY CYCLE; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; RAT; SIGNAL TRANSDUCTION; TANYCYTE; ANALOGS AND DERIVATIVES; ANALYSIS OF VARIANCE; ANIMAL; DRUG EFFECTS; ENZYME LINKED IMMUNOSORBENT ASSAY; FLOW CYTOMETRY; FLUORESCENT ANTIBODY TECHNIQUE; GLIA; IMAGE PROCESSING; IMMUNOHISTOCHEMISTRY; METABOLISM; MOUSE; OVARIECTOMY; PHYSIOLOGY; REAL TIME POLYMERASE CHAIN REACTION; SPRAGUE DAWLEY RAT; WESTERN BLOTTING;

MAMMALIA; MUS; RODENTIA;

ANALYSIS OF VARIANCE; ANIMALS; ANTIGENS, CD; BLOTTING, WESTERN; ENZYME-LINKED IMMUNOSORBENT ASSAY; ESTRADIOL; FEMALE; FLOW CYTOMETRY; FLUORESCENT ANTIBODY TECHNIQUE; IMAGE PROCESSING, COMPUTER-ASSISTED; IMMUNOHISTOCHEMISTRY; MEDIAN EMINENCE; MICE; NEUROGLIA; NEURONAL PLASTICITY; OVARIECTOMY; PROGESTERONE; RATS; RATS, SPRAGUE-DAWLEY; REAL-TIME POLYMERASE CHAIN REACTION; SEMAPHORINS;

EID: 84924023377     PISSN: None     EISSN: 20411723     Source Type: Journal    
DOI: 10.1038/ncomms7385     Document Type: Article

References (63)

1. Christian, C. A. & Moenter, S. M. The neurobiology of preovulatory and estradiol-induced gonadotropin-releasing hormone surges. Endocr. Rev. 31, 544-577 (2010).
2. Gonzalez-Martinez, D., Hu, Y. & Bouloux, P. M. Ontogeny of GnRH and olfactory neuronal systems in man: novel insights from the investigation of inherited forms of Kallmann's syndrome. Front. Neuroendocrinol. 25, 108-130 (2004).
3. Prevot, V. et al. Gonadotrophin-releasing hormone nerve terminals, tanycytes and neurohaemal junction remodelling in the adult median eminence: functional consequences for reproduction and dynamic role of vascular endothelial cells. J. Neuroendocrinol. 22, 639-649 (2010).
4. Herbison, A. E. Multimodal influence of estrogen upon gonadotropin-releasing hormone neurons. Endocr. Rev. 19, 302-330 (1998).
5. Moenter, S. M., Chu, Z. & Christian, C. A. Neurobiological mechanisms underlying oestradiol negative and positive feedback regulation of gonadotrophin-releasing hormone neurones. J. Neuroendocrinol. 21, 327-333 (2009).
6. Ronnekleiv, O. K. & Kelly, M. J. Diversity of ovarian steroid signaling in the hypothalamus. Front. Neuroendocrinol. 26, 65-84 (2005).
7. Piet, R., Boehm, U. & Herbison, A. E. Estrous cycle plasticity in the hyperpolarization-activated current Ih is mediated by circulating 17betaestradiol in preoptic area kisspeptin neurons. J. Neurosci. 33, 10828-10839 (2013).
8. Prevot, V. et al. Function-related structural plasticity of the GnRH system: a role for neuronal-glial-endothelial interactions. Front. Neuroendocrinol. 31, 241-258 (2010).
9. Garcia-Segura, L. M., Lorenz, B. & DonCarlos, L. L. The role of glia in the hypothalamus: implications for gonadal steroid feedback and reproductive neuroendocrine output. Reproduction 135, 419-429 (2008).
10. Barres, B. A. A role for glia in LHRH release. Curr. Biol. 2, 645-647 (1992).
11. Ojeda, S. R., Lomniczi, A. & Sandau, U. Contribution of glial-neuronal interactions to the neuroendocrine control of female puberty. Eur. J. Neurosci. 32, 2003-2010 (2010).
12. Sharif, A., Baroncini, M. & Prevot, V. Role of glia in the regulation of gonadotropin-releasing hormone neuronal activity and secretion. Neuroendocrinology 98, 1-15 (2013).
13. Zhou, Y., Gunput, R. A. & Pasterkamp, R. J. Semaphorin signaling: progress made and promises ahead. Trends Biochem. Sci. 33, 161-170 (2008).
14. Pasterkamp, R. J. Getting neural circuits into shape with semaphorins. Nat. Rev. Neurosci. 13, 605-618 (2012).
15. Messina, A. et al. Dysregulation of Semaphorin7A/beta1-integrin signaling leads to defective GnRH-1 cell migration, abnormal gonadal development and altered fertility. Hum. Mol. Genet. 20, 4759-4774 (2011).
16. Parkash, J. et al. Suppression of beta1-integrin in gonadotropin-releasing hormone cells disrupts migration and axonal extension resulting in severe reproductive alterations. J. Neurosci. 32, 16992-17002 (2012).
17. Vo, T. et al. The chemorepulsive axon guidance protein semaphorin 3A is a constituent of perineuronal nets in the adult rodent brain. Mol. Cell. Neurosci. 56, 186-200 (2013).
18. Pasterkamp, R. J., Kolk, S. M., Hellemons, A. J. & Kolodkin, A. L. Expression patterns of semaphorin7A and plexinC1 during rat neural development suggest roles in axon guidance and neuronal migration. BMC Dev. Biol. 7, 98 (2007).
19. Prevot, V. et al. Definitive evidence for the existence of morphological plasticity in the external zone of the median eminence during the rat estrous cycle: implication of neuro-glio-endothelial interactions in gonadotropin-releasing hormone release. Neuroscience 94, 809-819 (1999).
20. King, J. C. & Letourneau, R. J. Luteinizing hormone-releasing hormone terminals in the median eminence of rats undergo dramatic changes after gonadectomy, as revealed by electron microscopic image analysis. Endocrinology 134, 1340-1351 (1994).
21. Page, R. in: Physiology of Reproduction. (eds Knobil, E. & Neill, J. D. 1527-1620 (Raven Press, 1994).
22. Mullier, A., Bouret, S. G., Prevot, V. & Dehouck, B. Differential distribution of tight junction proteins suggests a role for tanycytes in blood-hypothalamus barrier regulation in the adult mouse brain. J. Comp. Neurol. 518, 943-962 (2010).
23. Peitz, M., Pfannkuche, K., Rajewsky, K. & Edenhofer, F. Ability of the hydrophobic FGF and basic TAT peptides to promote cellular uptake of recombinant Cre recombinase: a tool for efficient genetic engineering of mammalian genomes. Proc. Natl Acad. Sci. USA 99, 4489-4494 (2002).
24. Langlet, F. et al. Tanycytic VEGF-A boosts blood-hypothalamus barrier plasticity and access of metabolic signals to the arcuate nucleus in response to fasting. Cell Metab. 17, 607-617 (2013).
25. Hokfelt, T. et al. DARPP-32 as a marker for D-1 dopaminoceptive cells in the rat brain: prenatal development and presence in glial elements (tanycytes) in the basal hypothalamus. Adv. Exp. Med. Biol. 235, 65-82 (1988).
26. Kang, H. R., Lee, C. G., Homer, R. J. & Elias, J. A. Semaphorin 7A plays a critical role in TGF-beta1-induced pulmonary fibrosis. J. Exp. Med. 204, 1083-1093 (2007).
27. Bouret, S., De Seranno, S., Beauvillain, J. C. & Prevot, V. Transforming growth factor beta1 may directly influence gonadotropin-releasing hormone gene expression in the rat hypothalamus. Endocrinology 145, 1794-1801 (2004).
28. Galbiati, M., Magnaghi, V., Martini, L. & Melcangi, R. C. Hypothalamic transforming growth factor beta1 and basic fibroblast growth factor mRNA expression is modified during the rat oestrous cycle. J. Neuroendocrinol. 13, 483-489 (2001).
29. Balland, E. et al. Hypothalamic tanycytes are an ERK-gated conduit for leptin into the brain. Cell Metab. 19, 293-301 (2014).
30. De Seranno, S. et al. Vascular endothelial cells promote acute plasticity in ependymoglial cells of the neuroendocrine brain. J. Neurosci. 24, 10353-10363 (2004).
31. Prevot, V., Dutoit, S., Croix, D., Tramu, G. & Beauvillain, J. C. Semiquantitative ultrastructural analysis of the localization and neuropeptide content of gonadotropin releasing hormone nerve terminals in the median eminence throughout the estrous cycle of the rat. Neuroscience 84, 177-191 (1998).
32. Prevot, V. et al. Estradiol coupling to endothelial nitric oxide stimulates gonadotropin-releasing hormone release from rat median eminence via a membrane receptor. Endocrinology 140, 652-659 (1999).
33. de Seranno, S. et al. Role of estradiol in the dynamic control of tanycyte plasticity mediated by vascular endothelial cells in the median eminence. Endocrinology 151, 1760-1772 (2010).
34. Salvi, R. et al. Gonadotropin-releasing hormone-expressing neurons immortalized conditionally are activated by insulin: implication of the mitogen-activated protein kinase pathway. Endocrinology 147, 816-826 (2006).
35. Igaz, P. et al. Effects of cytokines on gonadotropin-releasing hormone (GnRH) gene expression in primary hypothalamic neurons and in GnRH neurons immortalized conditionally. Endocrinology 147, 1037-1043 (2006).
36. Agnew, B. J., Minamide, L. S. & Bamburg, J. R. Reactivation of phosphorylated actin depolymerizing factor and identification of the regulatory site. J. Biol. Chem. 270, 17582-17587 (1995).
37. Bamburg, J. R., McGough, A. & Ono, S. Putting a new twist on actin: ADF/cofilins modulate actin dynamics. Trends Cell Biol. 9, 364-370 (1999).
38. Walzer, T., Galibert, L., Comeau, M. R. & De Smedt, T. Plexin C1 engagement on mouse dendritic cells by viral semaphorin A39R induces actin cytoskeleton rearrangement and inhibits integrin-mediated adhesion and chemokineinduced migration. J. Immunol. 174, 51-59 (2005).
39. Scott, G. A., McClelland, L. A., Fricke, A. F. & Fender, A. Plexin C1, a receptor for semaphorin 7a, inactivates cofilin and is a potential tumor suppressor for melanoma progression. J. Invest. Dermatol. 129, 954-963 (2009).
40. Puschel, A. W. GTPases in semaphorin signaling. Adv. Exp. Med. Biol. 600, 12-23 (2007).
41. Wang, Y. et al. Plexins are GTPase-activating proteins for Rap and are activated by induced dimerization. Sci. Signal. 5, ra6 (2012).
42. Polakis, P. & McCormick, F. Interactions between p21ras proteins and their GTPase activating proteins. Cancer Surv. 12, 25-42 (1992).
43. Sullivan, S. D. & Moenter, S. M. Prenatal androgens alter GABAergic drive to gonadotropin-releasing hormone neurons: implications for a common fertility disorder. Proc. Natl Acad. Sci. USA 101, 7129-7134 (2004).
44. Giacobini, P. & Prevot, V. Semaphorins in the development, homeostasis and disease of hormone systems. Semin. Cell Dev. Biol. 24, 190-198 (2013).
45. Giacobini, P. et al. Brain Endothelial Cells Control Fertility through Ovarian-Steroid-Dependent Release of Semaphorin 3A. PLoS Biol. 12, e1001808 (2014).
46. Smith, M. S., Freeman, M. E. & Neill, J. D. The control of progesterone secretion during the estrous cycle and early pseudopregnancy in the rat: prolactin, gonadotropin and steroid levels associated with rescue of the corpus luteum of pseudopregnancy. Endocrinology 96, 219-226 (1975).
47. Dafopoulos, K. et al. Evidence that termination of the estradiol-induced luteinizing hormone surge in women is regulated by ovarian factors. J. Clin. Endocrinol. Metab. 91, 641-645 (2006).
48. Kasa-Vubu, J. Z. et al. Progesterone blocks the estradiol-induced gonadotropin discharge in the ewe by inhibiting the surge of gonadotropin-releasing hormone. Endocrinology 131, 208-212 (1992).
49. Zhao, H., Tian, Z., Hao, J. & Chen, B. Extragonadal aromatization increases with time after ovariectomy in rats. Reprod. Biol. Endocrinol. 3, 6 (2005).
50. Boon, W. C., Chow, J. D. & Simpson, E. R. The multiple roles of estrogens and the enzyme aromatase. Prog. Brain Res. 181, 209-232 (2010).
51. Bouret, S., Prevot, V., Takumi, T., Beauvillain, J. C. & Mitchell, V. Regulation by gonadal steroids of the mRNA encoding for a type I receptor for TGF-beta in the female rat hypothalamus. Neuroendocrinology 76, 1-7 (2002).
52. Campbell, C. S., Schwartz, N. B. & Firlit, M. G. The role of adrenal and ovarian steroids in the control of serum LH and FSH. Endocrinology 101, 162-172 (1977).
53. Stouffer, R. L. & Hennebold, J. D. in: Knobil and Neill's Physiology of Reproduction 4th edn (eds. Plant, T. M. & Zeleznik, J.) 1023-1076 (Elsevier, 2015).
54. Prevot, V. et al. Evidence that members of the TGFbeta superfamily play a role in regulation of the GnRH neuroendocrine axis: expression of a type I serine-threonine kinase receptor for TGRbeta and activin in GnRH neurones and hypothalamic areas of the female rat. J. Neuroendocrinol. 12, 665-670 (2000).
55. Tamagnone, L. et al. Plexins are a large family of receptors for transmembrane, secreted, and GPI-anchored semaphorins in vertebrates. Cell 99, 71-80 (1999).
56. Campbell, D. S. & Holt, C. E. Apoptotic pathway and MAPKs differentially regulate chemotropic responses of retinal growth cones. Neuron 37, 939-952 (2003).
57. Bechara, A. et al. FAK-MAPK-dependent adhesion disassembly downstream of L1 contributes to semaphorin3A-induced collapse. EMBO J. 27, 1549-1562 (2008).
58. Rohm, B., Rahim, B., Kleiber, B., Hovatta, I. & Puschel, A. W. The semaphorin 3A receptor may directly regulate the activity of small GTPases. FEBS Lett. 486, 68-72 (2000).
59. Hu, H., Marton, T. F. & Goodman, C. S. Plexin B mediates axon guidance in Drosophila by simultaneously inhibiting active Rac and enhancing RhoA signaling. Neuron 32, 39-51 (2001).
60. Freeman, S. A. et al. Cofilin-mediated F-actin severing is regulated by the Rap GTPase and controls the cytoskeletal dynamics that drive lymphocyte spreading and BCR microcluster formation. J. Immunol. 187, 5887-5900 (2011).
61. Baroncini, M. et al. Sex steroid hormones-related structural plasticity in the human hypothalamus. NeuroImage 50, 428-433 (2010).
62. Kansakoski, J. et al. Mutation screening of SEMA3A and SEMA7A in patients with congenital hypogonadotropic hypogonadism. Pediatr. Res. 75, 641-644 (2014).
63. Pasterkamp, R. J., Peschon, J. J., Spriggs, M. K. & Kolodkin, A. L. Semaphorin 7A promotes axon outgrowth through integrins and MAPKs. Nature 424, 398-405 (2003).