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Regional Diminution of Von Willebrand Factor Expression on the Endothelial Covering Arachnoid Granulations of Human, Monkey and Dog Brain

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Regional Diminution of Von Willebrand Factor Expression on the Endothelial Covering Arachnoid Granulations of Human, Monkey and Dog Brain Kurume Medical Journal, 49,177-183, 2002 Original Article Regional Diminution of von Willebrand Factor Expression on the Endothelial Covering Arachnoid Granulations of Human, Monkey and Dog Brain KEISUKE OHTA, TETSUO INOKUCHI, YUUHO HAYASHIDA, TETSUYA MIZUKAMI, TOMOHIRO YOSHIDA AND TARO KAWAHARA Department of Anatomy and Histology, Kurume University School of Medicine, Kurume 830-0011, Japan Summary: Arachnoid granulation is a protrusion of the arachnoid membrane into the cranial sinus, and is thought to play an essential role in the cerebrospinal fluid (CSF) absorption. Because the cells covering the apex region of the arachnoid granulation have different morphological features compared to the ordinary endothelial cells lining of the cranial sinus lumen, it has been expected these covering endothelial cells perform some specific function in the CSF absorption mechanism. However, little is known about functional differences between the covering endothelium of the arachnoid granulation and the ordinary sinus endothelium. In the present study, the characteristics of the covering cells located at the apex of arachnoid granulations of human, monkey and dog brain were examined by histochemical and immunohistochemical methods. The endothelial cells lining the cranial sinus lumen generally expressed such proteins as von Willebrand factor (vWF), CD31 and glycoproteins containing GS-1 or LE-1 lectin reacting sugar residue which are endothelial cell markers. However, the endothelial cells specifically located at the apex of arachnoid granulations failed to show vWF immunoreactivity, whereas the other endothelial markers were positive in each species we examined. Double staining of vWF antibody with other markers has clearly demon- strated that the endothelial cells on the apex region of arachnoid granulations exhibit no expression of vWF whereas cells lining the lateral region of arachnoid granulations and the luminal surface of ordinary cranial sinuses showed co-localization of these markers. The structural and histochemical differences between endothelial cells located at the apex region of arachnoid granulations and those of the sinus wall may reflect functional differences. Key words immunohistochemistry, lectin, endothelial marker, arachnoid granulation, von Willebrand factor, endothelial cell, cranial sinus Although the size and the structure of arachnoid INTRODUCTION granulations are considerably differ considerably by The protrusions of arachnoidmembrane into the cra- species or by age of subject, they are generally nial sinus lumen through the dural wall are called thought to play an essential role in CSF transport arachnoid granulations or arachnoid villi. Since from subarachnoid space to the cranial sinus lumen. Weed's classic work [1] describing the role of arach- These granulations are special bulgings of the inner noid villi in the drainage mechanism of cerebrospinal wall of the cranial sinus, and their surfaces are con- fluid (CSF), many physiological and morphological sidered to be covered with a continuous sheet of studies on arachnoid granulation of many laboratory endothelium [7-9]. A number of studies were focused animals [2-4] and humans [5,6] have been reported. on the mechanisms of CSF drainage across the sinus Received for publication August 5, 2002 Corresponding to: Dr. Keisuke Ohta, Department of Anatomy and Histology, Kurume University School of Medicine, 67 Asahi-machi, Kurume 830-0011, Japan. Tel: +81-942-31-7541 Fax: +81-942-31-7555 E-mail: [email protected] 178 OHTA ET AL. endothelial covering. Ultrastructual features of the thiopental anesthesia (25 mg/kg), and the animals cells covering the apical regions of arachnoid granu- were perfused via the aorta with physiological saline, lations are known to be quite different from those of followed by 4% paraformaldehyde/0.1 M cacodylate endothelial cells located at the surface of the ordinary buffered solution. The arachnoid granulations with inner wall of sinuses: The superficial covering cells surrounding dura mater were then dissected out from of the apex of arachnoid granulations have many the superior saggital sinus, and further fixed in the giant intracellular vacuoles which are thought to same fixatives for 3 hrs at 4•Ž. provide a channel for bulk flow of the CSF from the subarachnoid space into the cranial sinus lumen Immunohistochemistry and lectin-histochemistry [10,11 ]. Although many detailed observations of The tissues were rinsed in 0.1 M cacodylate ultrastructural characteristics of the covering cells buffer, and incubated in 15% sucrose solution in have been reported, the histochemical features of buffer overnight at 4•Ž. They were then embedded these cells has remained largely unknown. Therefore, in OCT-compound (Tissue-Tec; Miles Laboratories in the present study, we investigated the histochemi- Inc., Elkhart, Ind., USA) and were frozen in chilled cal differences between the covering cells of arach- ethanol by dry ice. noid granulations and those of the ordinary sinus The antibodies against vWF and CD31, and the walls. Immunohistochemical and lectin-histochemi- lectins of Lycopersicon esculentum (LE) and cal studies using four commonly-used endothelial Griffonia simplicifolia I (GS-1), were used as the markers (von Willebrand factor (vWF), CD31 anti- endothelial cell markers. Seven micrometer frozen bodies, GS-1 and LE-1 lectins) revealed that the sections on slide-glasses were applied to hema- arachnoid granulations are distinctly covered with toxylin-eosin (HE) staining and also to the histo- endothelial cell lining, and that cells in the apical chemistry. Several sections of the arachnoid granula- region of arachnoid granulations show no or only tions were treated with 1% bovine serum albumin weak expression of vWF. A similar mode of vWF (BSA) and 2.5% normal goat serum in 0.01 M phos- expression was reported in human arachnoid granula- phate buffered saline (PBS) and subsequently incu- tions by Kida et al. who interpreted their finding as a bated in diluted primary antibody or biotinylated proof of a lack of endothelial lining [6]. We used lectin. The best staining contrast was obtained at a dual immunohistochemical staining methods with the dilution of 1:1600 for rabbit anti-human vWF anti- antibodies against vWF and other endothelial marker body (DAKO, Denmark), 1:50 for mouse anti-human proteins or sugar residues in several animals and also CD31 antibody (DAKO, Denmark), 1:1600 for in human beings. We have clarified that the defect of biotinylated-LE (Sigma Chemical Co., St. Louis, vWF expression in the apex region of arachnoid USA) and 1:1600 for biotinylated-GS-1 (Vector, granulations indicates some region-specific charac- Burlingame, Ca., USA). The specimens for immuno- teristic of the endothelium but not a lack of endothe- histochemical studies were subsequently reacted with lial covering itself. the secondary antibodies, biotinylated anti-rabbit or anti-mouse IgG. The biotin-marked antigens or sugar residues were visualized by immuno-peroxidase MATERIALS AND METHODS methods (Vectastain ABC Kit; Vector, Burlingame, Human arachnoid granulations were obtained Ca., USA) or by immuno-fluorescence methods from ten cadavers during regular educational dissec- (Amersham, Great Britain). tions for medical students at Kurume University For double fluorescence histochemistry of vWF School of Medicine. Arachnoid granulations which and other markers, the sections were incubated were dissected out from cadavers were re-fixed overnight with anti-vWF antibody and the other by 4% paraformaldehyde/0.1 M cacodylate buffer endothelial marker antibody or lectin at the concen- (pH 7.3) for 4 hrs at 4•Ž. trations described above. Following incubation with Arachnoid granulations of laboratory animals primary antibodies or lectins, the sections were were obtained from three adult Japanese monkeys reacted with biotinylated anti-mouse IgG (Vector, (Macacus fuscatus) and two canines. The mainte- Burlingame, Ca., USA), if necessary, followed by nance of the animals and all experimental procedures fluorescein linked anti-rabbit IgG (Amersham, Great were carried out in accordance with the Guide for Britain) and Texas Red-labeled streptoavidin. The Animal Experimentation, Kurume University School double-stained sections were observed by confocal of Medicine. All surgeries were performed under laser scanning microscope (Carl Zeiss, LSM-310). Kurume Medical Journal Vol. 49, No. 4, 2002 VWF FXPRESSION IN ARACHNOID GRANULATION 179 The specificitics of primary antibodies were checked is surrounded by fibrous capsule. The surface of the in sections reacted without the antibodies or Iectins. fibrous capsule of the arachnoid granulations in the Those studies revealed the absence of cross-fractions present study was seen to be covered with endothe- with other primary or secondary antibodies. lial sheets, although these were hard to identify in the light microscopic sections stained with hematoxylin Scinning electron mcroseope and eosin (Fig. la). Canine arachnoid granulations were observed On the other hand, the "fibrous capsule". which under the scanning elect on microscope (SEM). The was commonly observed in human arachnoid gran- specimens dissected out as above were fixed by 2% ulations, was not observed in any arachnoid granula- paraformaldehyde + 2.5% glutaraldchyde solution in tions of monkeys and dogs. The apex of the granula- 0.1 M cacodylate buffer (pH 7.3) for 2 hrs at room tions was frequently lobulated with rugged surfaces temperature. Specimens
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