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Folliculostellate Cell Network: a Route for Long- Distance Communication in the Anterior Pituitary

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Folliculostellate Cell Network: a Route for Long- Distance Communication in the Anterior Pituitary Folliculostellate cell network: A route for long- distance communication in the anterior pituitary Teddy Fauquier*, Nathalie C. Gue´ rineau*, R. Anne McKinney†, Karl Bauer‡, and Patrice Mollard*§ *Institut National de la Sante´et de la Recherche Me´dicale (INSERM) Unite´469, Centre National de la Recherche Scientifique–INSERM de Pharmacologie–Endocrinologie, 141 Rue de la Cardonille, 34094 Montpellier Cedex 5, France; †Brain Research Institute, University of Zurich, Winterthurerstrasse 190, CH-8057 Zurich, Switzerland; and ‡Max-Planck-Institut fu¨r Experimentelle Endokrinologie, Feodor-Lynen-Strasse 7, 30625 Hannover, Germany Edited by Michael V. L. Bennett, Albert Einstein College of Medicine, Bronx, NY, and approved May 9, 2001 (received for review July 21, 2000) All higher life forms critically depend on hormones being rhyth- transfer within the gland. FS cells display a star-shaped cyto- mically released by the anterior pituitary. The proper functioning plasmic configuration intermingled between hormone-secreting of this master gland is dynamically controlled by a complex set of cells. The organization of FS cells within the parenchyma forms regulatory mechanisms that ultimately determine the fine tuning a three-dimensional anatomical network, in the meshes of which of the excitable endocrine cells, all of them heterogeneously the endocrine cells reside (15, 16). Very little is known about the distributed throughout the gland. Here, we provide evidence for functioning of this FS cell network, in particular with regard to an intrapituitary communication system by which information is the dynamics of cellular͞intercellular messages. To study the transferred via the network of nonendocrine folliculostellate (FS) behavior of this network, we measured multicellular changes in 2ϩ cells. Local electrical stimulation of FS cells in acute pituitary slices [Ca ]i, a messenger involved in a wide range of cell-to-cell triggered cytosolic calcium waves, which propagated to other FS communication mechanisms (17–23), electrophysiological prop- cells by signaling through gap junctions. Calcium wave initiation erties of FS cells, and intercellular diffusion of dyes in acute was because of the membrane excitability of FS cells, hitherto pituitary slices. We show here that the FS cell network forms a classified as silent cells. FS cell coupling could relay information functional intrapituitary circuitry in which information—Ca2ϩ between opposite regions of the gland. Because FS cells respond to signals and small diffusible molecules—can be transferred over central and peripheral stimuli and dialogue with endocrine cells, long distances (millimeter range) within the intact pituitary the form of large-scale intrapituitary communication described tissue. here may provide an efficient mechanism that orchestrates ante- rior pituitary functioning in response to physiological needs. Methods Cytosolic Ca2؉ Monitoring in Acute Slices. Pituitary slices (200 ␮m lassically, the anterior pituitary is considered as a secondary thick) from 10- to 12-week-old female Wistar rats were prepared oscillator obeying mainly hypothalamic factors, either in- as previously described (11). Ringer’s saline contained (in mM): C ͞ ͞ ͞ ͞ ͞ creasing or decreasing secretion of pituitary hormones, which 125 NaCl 2.5 KCl 2 CaCl2 1 MgCl2 1.25 NaH2PO4 26 ͞ ␮ ␤ NaHCO3 12 glucose. Slices were incubated with 40 M -Ala- are released in an episodic manner at the base of the median ␧ eminence (1–4). The portal blood vessels form the interorgan Lys-N -AMCA, a UV light-excitable fluorescent dipeptide communication system driving the hypothalamic inputs to the (AMCA, 7-amino-4-methylcoumarin-3-acetic acid) taken up by anterior pituitary. They collect the transmitters released by FS cells (24), at 37°C for 1.5 h and then exposed to 15 ␮M Oregon hypothalamic nerve endings at the primary capillary plexus level green 488 1,2-bis(2-aminophenoxy)ethane-N,N,NЈ,NЈ-tetraac- and slowly distribute them in the endocrine parenchyma via the etate (BAPTA)-1 acetoxymethyl ester (Molecular Probes) pe- arborescence of pituitary sinusoids between the columnar units riodically delivered (3 s per 20 s for 15–20 min) onto a cell field of pituitary cells (‘‘cell cords’’) (5, 6). Over the last three decades, via a blunt micropipette (11). Time-lapse optical sequences were many studies carried out in isolated endocrine cells have pro- captured with a real-time confocal microscope (Noran Odyssey vided strong evidence that endocrine cells generate action XL, 488-nm excitation wavelength, 120 images per s with aver- 2ϩ 2ϩ potential-driven rises in cytosolic Ca concentration ([Ca ]i) aging 4 frames), which also delivered a TTL (transistor– that are probably the keystones of dynamic adjustment of transistor logic) signal that synchronized image acquisition with numerous cellular functions, including exocytosis and gene a brief voltage pulse (1 ms, 0.5–10 V) applied to a patch-pipette expression (7–9). Recently, the technique of acute slice prepa- filled with Ringer’s saline and positioned on the cell (10). rations applied to the anterior pituitary revealed that endocrine Because the confocal microscope was fitted with an Ar͞Kr laser 2ϩ cells do fire short-term [Ca ]i transients because of their (visible light wavelengths), cells at the slice surface were first electrical activity in situ (10, 11). viewed with a xenon lamp via the epifluorescent port of the ␧ However, the activity of the gland as a whole does not reflect upright microscope. Only cells that showed both ␤-Ala-Lys-N - the average of independent dynamics of cellular messages that AMCA and Oregon green 488 BAPTA-1 were taken for sub- 2ϩ occur in the distinct endocrine cell types scattered throughout sequent [Ca ]i monitoring. In some experiments, electrical field the tissue. In this respect, one puzzling finding is the persistence stimulation was used to locally stimulate a cell field. A current of pulsatile releasing profiles of hormones when the gland is step was shortly applied between the tips (50–100 ␮m apart) of disconnected from the hypothalamic inputs (12, 13). This indi- two pipettes (filled with Ringer’s saline) touching the slice cates that a large-scale communication system exists within the anterior pituitary. Despite the wealth of information on cell-to- cell mechanisms between endocrine cells that comprise the This paper was submitted directly (Track II) to the PNAS office. 2ϩ release of paracrine factors (14) and gap junction signaling (10), Abbreviations: FS, folliculostellate; [Ca ]i, cytosolic calcium concentration; TTX, tetro- Ј spreading of spatial information that crosses the limits of single dotoxin; TEA, tetraethylammonium; BAPTA, 1,2-bis(2-aminophenoxy)ethane-N,N,N , NЈ-tetraacetate; AMCA, 7-amino-4-methylcoumarin-3-acetic acid; IP3, inositol 1,4,5- cell cords could not be explained by these mechanisms. trisphosphate. Because a highly efficient process spreading spatial informa- §To whom reprint requests should be addressed. E-mail: [email protected]. tion to the entire gland and even to pituitary subregions has not The publication costs of this article were defrayed in part by page charge payment. This PHYSIOLOGY been reported yet, we explored here whether nonendocrine article must therefore be hereby marked “advertisement” in accordance with 18 U.S.C. folliculostellate (FS) cells can support long-distance information §1734 solely to indicate this fact. www.pnas.org͞cgi͞doi͞10.1073͞pnas.151339598 PNAS ͉ July 17, 2001 ͉ vol. 98 ͉ no. 15 ͉ 8891–8896 Downloaded by guest on September 28, 2021 2ϩ surface. [Ca ]i changes were imaged with an intensified cooled charge-coupled device camera (PentaMAX Gen IV; Princeton Instruments, Trenton, NJ) and acquired with Metafluor (Uni- versal Imaging, Media, 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 re- corded by using an EPC-9 patch-clamp amplifier (HEKA Elec- tronics, Lambrecht͞Pfalz, Germany). Intrapipette solution con- ͞ ͞ ͞ tained (in mM): 140 potassium gluconate 10 KCl 2 MgCl2 1.1 EGTA͞5 Hepes, pH 7.2 (KOH). Current steps were injected through the pipette tip at the soma level only. When membrane 2ϩ potential measurements were combined with [Ca ]i imaging, fluo-3 potassium salt (100 ␮M) was included, and EGTA was lowered to 0.2 mM. Lucifer yellow (1 mM, Sigma) or Neurobi- otin [N-(2-aminoethyl)biotinamide hydrochloride, 1%, Vector Laboratories] was added to the intrapipette solution when appropriate. When inward currents were recorded in voltage- clamp conditions, CsCl replaced potassium gluconate in equimo- lar amounts, and BAPTA (10 mM) was used as a Ca2ϩ chelator. Only cells with a high input resistance (Ն1G⍀), which provided acceptable space-clamp conditions, were recorded with the 2ϩ Fig. 1. Generation of propagated [Ca ]i waves in FS cells in response to voltage-clamp mode. electrical stimulation. (a) Superimposed differential interference contrast microscopy image of the slice surface with ␤-Ala-Lys-N␧-AMCA fluorescence Immunostaining. Laminin staining was performed with a poly- (pseudocolored in blue) of FS cells (scale bar, 10 ␮m). (b) A confocal image clonal antibody (Sigma) when the FS cell network had been showing 10 FS cells loaded with a fluorescent Ca2ϩ dye (scale bar, 10 ␮m). The traced with Neurobiotin (revealed with FITC-labeled avidin D). color circles highlight the area of each cell used to monitor changes in 2ϩ Samples were examined with a Zeiss LSM 410 confocal micro- fluorescence reflecting [Ca ]i levels. The stimulating micropipette was touch- scope. Neurobiotin was visualized with an argon ion laser at 488 ing the cell circled in green. (c) Changes in fluorescence, normalized to ͞ 2ϩ nm, and a He͞Ne laser, pretuned to 543 nm, was used to image baseline fluorescence (F Fmin), for the 10 regions in b. The spread of a [Ca ]i laminin simultaneously. Optical slices of 0.2-␮m intervals with wave was initiated by a brief electrical stimulation.
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