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Folliculostellate Cell Network: a Route for Long-Distance Communication In Folliculostellate cell network : A route for long-distance communication in the anterior pituitary Teddy Fauquier, Nathalie Guérineau, R. Mckinney, Karl Bauer, Patrice Mollard To cite this version: Teddy Fauquier, Nathalie Guérineau, R. Mckinney, Karl Bauer, Patrice Mollard. Folliculostellate cell network : A route for long-distance communication in the anterior pituitary. Proceedings of the National Academy of Sciences of the United States of America , National Academy of Sciences, 2001, 98 (15), pp.8891-8896. 10.1073/pnas.151339598. hal-02485565 HAL Id: hal-02485565 https://hal.archives-ouvertes.fr/hal-02485565 Submitted on 25 Feb 2020 HAL is a multi-disciplinary open access L’archive ouverte pluridisciplinaire HAL, est archive for the deposit and dissemination of sci- destinée au dépôt et à la diffusion de documents entific research documents, whether they are pub- scientifiques de niveau recherche, publiés ou non, lished or not. The documents may come from émanant des établissements d’enseignement et de teaching and research institutions in France or recherche français ou étrangers, des laboratoires abroad, or from public or private research centers. publics ou privés. Biological Sciences (Physiology) A new route for long-distance communication in the anterior pituitary Teddy Fauquier*, Nathalie C. Guérineau*, R. Anne McKinney†, Karl Bauer‡ & Patrice Mollard*§ *INSERM Unité 469, CCIPE, 141 rue de la Cardonille, 34094 Montpellier Cedex 5, France † Brain Research Institute, University of Zurich, Winterthurerstrasse 190, CH-8057 Zurich, Switzerland ‡Max-Planck-Institut für experimentelle Endokrinologie, Feodor-Lynen-Straße 7, 30625 Hannover, Germany §To whom reprint requests should be addressed. E-mail: [email protected] Manuscript information: 18 text pages and 6 figures Word and character counts: 164 words in the abstract and 47,740 characters in the paper 2+ Abbreviations: FS cells, folliculostellate cells; [Ca ]i, cytosolic calcium concentration; TTX, tetrodotoxin; TEA, tetraethylammonium; 4-AP, 4-aminopyridine; PPADS, pyridoxal- phosphate-6-azophenyl-2’,4’-disulfonic acid 2 ABSTRACT All higher life forms critically depend on hormones being rhythmically released by the anterior pituitary. The proper functioning of this master gland is dynamically controlled by a complex set of regulatory mechanisms that ultimately determine the fine tuning of the excitable endocrine cells, all of them heterogeneously distributed throughout the gland. Here we provide evidence for a new intrapituitary communication system by which information is transferred via the network of non-endocrine folliculostellate (FS) cells. Local electrical stimulation of FS cells in acute pituitary slices triggered cytosolic calcium waves, which propagated to other FS cells by signaling through gap junctions. Calcium wave initiation was due to the membrane excitability of FS cells, hitherto classified as silent cells. FS cell coupling could relay information between opposite regions of the gland. Since FS cells respond to central and peripheral stimuli and dialogue with endocrine cells, this new form of large-scale intrapituitary communication may provide an efficient mechanism that orchestrates anterior pituitary functioning in response to physiological needs. 3 Classically, the anterior pituitary is considered as a secondary oscillator obeying mainly hypothalamic factors, either increasing or decreasing secretion of pituitary hormones, which are released in an episodic manner at the basis of the medium eminence (1-4). The portal blood vessels form the interorgan communication system driving the hypothalamic inputs to the anterior pituitary gland. They collect the transmitters released by hypothalamic nerve endings at the primary capillary plexus level and slowly distribute them in the endocrine parenchyma via the complex arborescence of pituitary sinusoids between the columnar units of pituitary cells (so-called cell cords) (5, 6). Over the last three decades, many studies carried out in isolated endocrine cells have provided strong evidence that endocrine cells 2+ generate action potential-driven rises in cytosolic calcium concentration ([Ca ]i) that are probably the keystones of dynamic adjustment of numerous cellular functions including exocytosis and gene expression (7-9). Recently, the technique of acute slice preparations 2+ applied to the anterior pituitary revealed that endocrine cells do fire short-term [Ca ]i transients due to their electrical activity in situ (10, 11). Temporal organization of these transients provide a very fine mode of timing information (time-locked rhythmic bursting pattern) when a bolus of secretagogues invades the glandular parenchyma (11). However, the activity of the gland as a whole does not reflect the average of independent dynamics of cellular messages that occur in the distinct endocrine cell types scattered throughout the tissue. In this respect, one puzzling finding is the persistence of pulsatile releasing profiles of hormones when the gland is disconnected from the hypothalamic inputs (12, 13). This indicates that a large-scale communication system exists within the anterior pituitary. In spite of the wealth of information on cell-to-cell mechanisms between endocrine cells that comprise the release of paracrine factors (14) and gap junction signaling (10), spreading of spatial information that crosses the limits of single pituitary cell cords could not be explained by these mechanisms. Since a highly efficient process spreading spatial information to the entire gland and even to pituitary sub-regions has not been reported yet, we explored here whether non- endocrine folliculostellate (FS) cells can support long-distance information transfer within the gland. FS cells display a star-shaped cytoplasmic configuration intermingled between hormone-secreting cells. The organization of FS cells within the parenchyma forms a three- dimensional anatomical network, in the meshes of which the endocrine cells reside (15, 16). Very little is known about the functioning of this FS cell network, in particular with regard to the dynamics of cellular/intercellular messages. To study the behavior of this network, we 2+ measured multicellular changes in [Ca ]i, a messenger involved in a wide range of cell-to- cell communication mechanisms (17-23), electrophysiological properties of FS cells and intercellular diffusion of dyes in acute pituitary slices. We showed here that the FS cell 4 network forms a functional intrapituitary circuitry in which information¾ Ca2+ signals and small diffusible molecules¾ can be transferred over long distances (mm range) within the intact pituitary tissue. 5 METHODS Cytosolic calcium monitoring in acute slices 200-mm-thick pituitary slices from 10-12-week-old female Wistar rats were prepared as previously described (11). Ringer’s saline contained (in mM): NaCl, 125; KCl, 2.5; CaCl2, 2; MgCl2, 1; NaH2PO4, 1.25; NaHCO3, 26; Glucose, 12. Slices were incubated with 40 mM b-Ala-Lys-Ne-AMCA, a UV light-excitable fluorescent dipeptide taken up by FS cells (24), at 37°C for 1.5 hours and then exposed to 15 mM Oregon Green 488 BAPTA-1/AM (Molecular Probes) periodically delivered (3 s per 20 s for 15-20 min) onto a cell field via a blunt micropipette (11). Time-lapse optical sequences were captured with a real-time confocal microscope (Noran Odyssey XL, 488 nm-excitation wavelength, 120 images/s with averaging 4 frames), which also delivered a TTL signal that synchronized image acquisition with a brief voltage pulse (1 ms, 0.5-10 V) applied to a patch-pipette filled with Ringer’s saline and positioned on the cell (10). Since the confocal microscope was fitted with an Argon/Krypton laser (visible light wavelengths), cells at the slice surface were first viewed with a Xenon lamp via the epifluorescent port of the upright microscope. Only cells that showed both b-Ala-Lys-Ne-AMCA and Oregon Green 488 BAPTA-1 were taken for 2+ subsequent [Ca ]i monitoring. In some experiments, electrical field stimulation was used to locally stimulate a cell field. A current step was shortly applied between the tips (50-100 µm 2+ apart) of two pipettes (filled with Ringer’s saline) touching the slice surface. [Ca ]i changes were imaged with an intensified cooled CCD camera (PentaMAX Gen IV; Princeton Inst., Trenton, NJ) and acquired with Metafluor (Universal Imaging Corp., West Chester, PA). Image analysis was carried out with InterVision 1.5.1, NIH Image 68k 1.58, Igor Pro 3.14, and Adobe Photoshop 5.0. Pharmacological agents were either superfused or locally applied with a puff pipette. Patch-clamp measurements Whole-cell electrical events were recorded using an EPC-9 patch-clamp amplifier (HEKA Electronik, Lambrecht-Pfalz, Germany). Intra-pipette solution contained (in mM): Kgluconate, 140; KCl, 10; MgCl2, 2; EGTA, 1.1; HEPES, 5; pH, 7.2 (KOH). Current steps were injected through the pipette tip at the soma level only. When membrane potential 2+ measurements were combined with [Ca ]i imaging, fluo-3 Ksalt (100 mM) was included and EGTA was lowered to 0.2 mM. Lucifer yellow (1 mM, Sigma) or NeurobiotinTM (N-(2- aminoethyl)-biotinamide hydrochloride, 1%, Vector) was added to the intrapipette solution when appropriate. When inward currents were recorded in voltage-clamp conditions, CsCl replaced Kgluconate in equimolar amounts and BAPTA (10 mM) was used as a Ca2+ 6 chelator. Only cells with a high input resistance (³ 1 GW), which provided acceptable space- clamp conditions, were recorded with the voltage-clamp mode.
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