Existence of long-lasting experience-dependent plasticity in endocrine cell networks

Nature Communications

Volumn 3, Issue , 2012, Pages

  Hodson, David J ^a,b   Schaeffer, Marie ^a,b,c   Romanò, Nicola ^a,b   Fontanaud, Pierre ^a,b   Lafont, Chrystel ^a,b   Birkenstock, Jerome ^a,b   Molino, François ^a,b   Christian, Helen ^d   Lockey, Joe ^d   Carmignac, Danielle ^e   Fernandez Fuente, Marta ^e   Le Tissier, Paul ^e   Mollard, Patrice ^a,b  

^a INSTITUT DE GÉNOMIQUE FONCTIONNELLE   (France)

^b UNIV MONTPELLIER   (France)

^c ROYAL COLLEGE OF SURGEONS IN IRELAND   (Ireland)

^d UNIVERSITY OF OXFORD   (United Kingdom)

^e NATIONAL INSTITUTE FOR MEDICAL RESEARCH   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

CALCIUM ION; PROLACTIN; CALCIUM;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CALCIUM SIGNALING; CELL ACTIVATION; CELL COMMUNICATION; CELL FUNCTION; CELL INTERACTION; CELL PLASTICITY; CELL STIMULATION; CELL STRUCTURE; CONTROLLED STUDY; ENDOCRINE CELL; ENDOCRINE CELL NETWORK; FEMALE; HYPOPHYSIS CELL; INTRACELLULAR SIGNALING; LACTATION; MALE; MOUSE; NEWBORN; NONHUMAN; PROLACTIN BLOOD LEVEL; PROLACTIN RELEASE; PROLACTIN SECRETING CELL; STIMULUS RESPONSE; TISSUE STRUCTURE; ADAPTATION; ANIMAL; BIOLOGICAL MODEL; C57BL MOUSE; CHEMISTRY; ENDOCRINE SYSTEM; HOMEOSTASIS; HYPOPHYSIS; METABOLISM; PHOTON; PHYSIOLOGY; THEORETICAL MODEL; TRANSGENIC MOUSE;

MAMMALIA;

ADAPTATION, PHYSIOLOGICAL; ANIMALS; CALCIUM; CELL COMMUNICATION; ENDOCRINE SYSTEM; FEMALE; HOMEOSTASIS; LACTATION; MALE; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; MODELS, BIOLOGICAL; MODELS, THEORETICAL; PHOTONS; PITUITARY GLAND;

EID: 84856719886     PISSN: None     EISSN: 20411723     Source Type: Journal    
DOI: 10.1038/ncomms1612     Document Type: Article

References (59)

1. Sprent J.&Surh C.D.T cell memory.Annu.Rev.Immunol.20 551-579 ( 2002 ). (Pubitemid 34293434)
2. Sun J.C.Beilke J.N.&Lanier L.L.Adaptive immune features of natural killer cells.Nature 4 57 557-561 ( 2009 ).
3. Bliss T.V.&Collingridge G.L.A synaptic model of memory: Long-Term potentiation in the hippocampus.Nature 3 61 31-39 ( 1993 ). (Pubitemid 23020772)
4. Chklovskii D.B.Mel B.W.&Svoboda K.Cortical rewiring and information storage.Nature 4 31 782-788 ( 2004 ). (Pubitemid 39434067)
5. Redondo R.L.&Morris R.G.Making memories last: The synaptic tagging and capture hypothesis.Nat.Rev.Neurosci.12 17 -30 ( 2011 ).
6. McHugh T.J.Blum K.I.Tsien J.Z.Tonegawa S.&Wilson M.A.Impaired hippocampal representation of space in CA1-specific NMDAR1 knockout mice.Cell 8 7 1339-1349 ( 1996 ). (Pubitemid 27010116)
7. Tang Y.P.et al.Genetic enhancement of learning and memory in mice.Nature 401 63-69 ( 1999 ).
8. Bonnefont X.et al.Revealing the large-scale network organization of growth hormone-secreting cells.Proc.Natl Acad.Sci.USA 102 16880-16885 ( 2005 ). (Pubitemid 41688871)
9. Sanchez-Cardenas C.et al.Pituitary growth hormone network responses are sexually dimorphic and regulated by gonadal steroids in adulthood.Proc.Natl Acad.Sci.USA 107 21878 -21883 ( 2010 ).
10. Budry L.et al.Related pituitary cell lineages develop into interdigitated 3D cell networks.Proc.Natl Acad.Sci.USA 108 12515 -12520 ( 2011 ).
11. Schaeffer M.et al.Infl uence of estrogens on GH-cell network dynamics in females: A live in Situ imaging approach.Endocrinology 152 4789 -4799 ( 2011 ).
12. Ludwig M.et al.Intracellular calcium stores regulate activity-dependent neuropeptide release from dendrites.Nature 418 85-89 ( 2002 ). (Pubitemid 34742575)
13. Kashtan N.&Alon U.Spontaneous evolution of modularity and network motifs.Proc.Natl Acad.Sci.USA 102 13773-13778 ( 2005 ). (Pubitemid 41377654)
14. Frankland P.W.&Bontempi B.The organization of recent and remote memories.Nat.Rev.Neurosci.6 119-130 ( 2005 ). (Pubitemid 40188946)
15. Freeman M.E.Kanyicska S.Lerant A.&Nagy G.Prolactin: Structurefunctionand regulation of secretion.Physiol.Rev.80 1523-1631 ( 2000 ).
16. Shingo T.et al.Pregnancy-stimulated neurogenesis in the adult female forebrain mediated by prolactin.Science 2 99117-120 ( 2003 ). (Pubitemid 36042416)
17. Larsen C.M.&Grattan D.R.Prolactin-induced mitogenesis in the subventricular zone of the maternal brain during early pregnancy is essential for normal postpartum behavioral responses in the mother.Endocrinology 151 3805 -3814 ( 2010 ).
18. Bridges R.S.DiBiase R.Loundes D.D.&Doherty P.C.Prolactin stimulation of maternal behavior in female rats.Science 227 782-784 ( 1985 ). (Pubitemid 15168273)
19. Schwartz T.H.et al.Networks of coactive neurons in developing layer 1.Neuron 2 0 541-552 ( 1998 ). (Pubitemid 28153083)
20. Peterlin Z.A.Kozloski J.Mao B.Q.Tsiola A.&Yuste R.Optical probing of neuronal circuits with calcium indicators.Proc.Natl Acad.Sci.USA 97 3619-3624 ( 2000 ). (Pubitemid 30183352)
21. Schlegel W.et al.Oscillations of cytosolic Ca2+ in pituitary cells due to action potentials.Nature 329 719-721 ( 1987 ). (Pubitemid 17151627)
22. He Z.et al.Continuous on-line monitoring of secretion from rodent pituitary endocrine cells using fluorescent protein surrogate markers.J.Neuroendocrinol.23197 -207 ( 2011 ).
23. Barabasi A.L.Scale-free networks: A decade and beyond.Science 3 25 412-413 ( 2009 ).
24. Bonifazi P.et al.GABAergic hub neurons orchestrate synchrony in developing hippocampal networks.Science 3 26 1419-1424 ( 2009 ).
25. Selmanoff M.&Wise P.M.Decreased dopamine turnover in the median eminence in response to suckling in the lactating rat.Brain Res.2 12 101-115 ( 1981 ). (Pubitemid 11100788)
26. Demarest K.T.McKay D.W.Riegle G.D.&Moore K.E.Biochemical indices of tuberoinfundibular dopaminergic neuronal activity during lactation: A lack of response to prolactin.Neuroendocrinology 3 6 130-137 ( 1983 ). (Pubitemid 13174283)
27. Anderson G.M.Grattan D.R.van den Ancker W.&Bridges R.S.Reproductive experience increases prolactin responsiveness in the medial preoptic area and arcuate nucleus of female rats.Endocrinology 1 47 4688-4694 ( 2006 ). (Pubitemid 44402176)
28. Castrique E.Fernandez-Fuente M.Le Tissier P.Herman A.&Levy A.Use of a prolactin-Cre/ROSA-YFP transgenic mouse provides no evidence for lactotroph transdiff erentiation after weaningor increase in lactotroph/ somatotroph proportion in lactation.J.Endocrinol.205 49 -60 ( 2010 ).
29. Guerineau N.C.Bonnefont X.Stoeckel L.&Mollard P.Synchronized spontaneous Ca2+ transients in acute anterior pituitary slices.J.Biol.Chem. 27310389-10395 ( 1998 ). (Pubitemid 28227647)
30. Fauquier T.Guerineau N.C.McKinney R.A.Bauer K.&Mollard P.Folliculostellate cell network: A route for long-distance communication in the anterior pituitary.Proc.Natl Acad.Sci.USA 98 8891-8896 ( 2001 ). (Pubitemid 32678123)
31. Lafont C.et al.Cellular in vivo imaging reveals coordinated regulation of pituitary microcirculation and GH cell network function.Proc.Natl Acad.Sci.USA 107 4465 -4470 ( 2010 ).
32. Stojilkovic S.S.Tabak J.&Bertram R.Ion channels and signaling in the pituitary gland.Endocr.Rev.31 845 -915 ( 2010 ).
33. Martin A.O.Mathieu M.N.Chevillard C.&Guerineau N.C.Gap junctions mediate electrical signaling and ensuing cytosolic Ca2+ increases between chromaffi n cells in adrenal slices: A role in catecholamine release.J.Neurosci.21 5397-5405 ( 2001 ). (Pubitemid 32692138)
34. Eriksson M.&Uvnas-Moberg K.Plasma levels of vasoactive intestinal polypeptide and oxytocin in response to sucklingelectrical stimulation of the mammary nerve and oxytocin infusion in rats.Neuroendocrinology 51 237-240 ( 1990 ). (Pubitemid 20066587)
35. Wanke I.E.&Rorstad O.P.Receptors for vasoactive intestinal peptide in rat anterior pituitary glands: Localization of binding to lactotropes. Endocrinology 126 1981-1988 ( 1990 ). (Pubitemid 20139743)
36. Kennett J.E.Poletini M.O.Fitch C.A.&Freeman M.E.Antagonism of oxytocin prevents suckling- and estradiol-inducedbut not progesteroneinducedsecretion of prolactin.Endocrinology 1 50 2292-2299 ( 2009 ).
37. Booth F.W.Effect of limb immobilization on skeletal muscle.J.Appl. Physiol.52 1113-1118 ( 1982 ). (Pubitemid 12055057)
38. Booth F.W.&Seider M.J.Recovery of skeletal muscle after 3 mo of hindlimb immobilization in rats.J.Appl.Physiol.4 7 435-439 ( 1979 ). (Pubitemid 10109507)
39. Grattan D.R.The actions of prolactin in the brain during pregnancy and lactation.Prog.Brain Res.133153-171 ( 2001 ).
40. Grattan D.R.&Kokay I.C.Prolactin: A pleiotropic neuroendocrine hormone.J.Neuroendocrinol.2 0 752-763 ( 2008 ). (Pubitemid 351858727)
41. Kinsley C.H.et al.Motherhood improves learning and memory.Nature 402 137-138 ( 1999 ).
42. Tomizawa K.et al.Oxytocin improves long-lasting spatial memory during motherhood through MAP kinase cascade.Nat.Neurosci.6 384-390 ( 2003 ). (Pubitemid 36373984)
43. Townsend J.et al.Effects of prolactin on hypothalamic supraoptic neurones: Evidence for modulation of STAT5 expression and electrical activity.Neuro.Endocrinol.Lett.2 6 125-130 ( 2005 ). (Pubitemid 40674214)
44. Kokay I.C.Bull P.M.Davis R.L.Ludwig M.&Grattan D.R.Expression of the long form of the prolactin receptor in magnocellular oxytocin neurons is associated with specific prolactin regulation of oxytocin neurons.Am.J.Physiol. Regul.Integr.Comp.Physiol.2 90 R1216 -R 1225 ( 2006 ).
45. Konstantinova I.et al.EphA-Ephrin-A-mediated beta cell communication regulates insulin secretion from pancreatic islets.Cell 129 359-370 ( 2007 ). (Pubitemid 46574973)
46. Ravier M.A.et al.Loss of connexin36 channels alters beta-cell couplingislet synchronization of glucose-induced Ca2+ and insulin oscillationsand basal insulin release.Diabetes 5 4 1798-1807 ( 2005 ). (Pubitemid 40770770)
47. Santos R.M.et al.Widespread synchronous [Ca2+]i oscillations due to bursting electrical activity in single pancreatic islets.Pflugers Arch.4 18 417-422 ( 1991 ).
48. Van Assche F.A.Aerts L.&De Prins F.A morphological study of the endocrine pancreas in human pregnancy.Br.J.Obstet.Gynaecol.8 5 818-820 ( 1978 ). (Pubitemid 9009998)
49. Karnik S.K.et al.Menin controls growth of pancreatic beta-cells in pregnant mice and promotes gestational diabetes mellitus.Science 318 806-809 ( 2007 ). (Pubitemid 351411773)
50. Orskov C.et al.Glucagon-like peptides GLP-1 and GLP-2predicted products of the glucagon geneare secreted separately from pig small intestine but not pancreas.Endocrinology 1191467-1475 ( 1986 ). (Pubitemid 17170509)
51. Kojima M.et al.Ghrelin is a growth-hormone-releasing acylated peptide from stomach.Nature 402 656-660 ( 1999 ). (Pubitemid 129516334)
52. Feyrter F.Ü ber diff use endokrine epitheliale Organe.Zentralblatt Innere Medizin 5 9 546-556 ( 1938 ).
53. Magoulas C.et al.A secreted fluorescent reporter targeted to pituitary growth hormone cells in transgenic mice.Endocrinology 141 4681-4689 ( 2000 ). (Pubitemid 32055148)
54. Sanchez-Cardenas C.&Hernandez-Cruz A.GnRH-Induced [Ca2+]isignalling patterns in mouse gonadotrophs recorded from acute pituitary slices in vitro.Neuroendocrinology 91 239 -255 ( 2010 ).
55. Niesner R.Andresen V.Neumann J.Spiecker H.&Gunzer M.The power of single and multibeam two-photon microscopy for high-resolution and high-speed deep tissue and intravital imaging.Biophys.J.9 3 2519-2529 ( 2007 ). (Pubitemid 47511151)
56. McGuinness L.et al.Autosomal dominant growth hormone deficiency disrupts secretory vesicles in vitro and in vivo in transgenic mice.Endocrinology 144 720-731 ( 2003 ). (Pubitemid 36205246)
57. Munari-Silem Y.Lebrethon M.C.Morand I.Rousset B.&Saez J.M.Gap junction-mediated cell-To-cell communication in bovine and human adrenal cells.A process whereby cells increase their responsiveness to physiological corticotropin concentrations.J.Clin.Invest.95 1429-1439 ( 1995 ).
58. Lledo P.M.Legendre P.Israel J.M.&Vincent J.D.Dopamine inhibits two characterized voltage-dependent calcium currents in identifi ed rat lactotroph cells.Endocrinology 127 990-1001 ( 1990 ). (Pubitemid 20277574)
59. Hodson D.J.Molino F.Fontanaud P.Bonnefont X.&Mollard P.Investigating and Modelling Pituitary Endocrine Network Function.J.Neuroendocrinol.22 1217 -1225 ( 2010 ).