Original Article
Copyright ©2012 Baishideng Publishing Group Co., Limited. All rights reserved.
World J Gastroenterol. Sep 28, 2012; 18(36): 5034-5041
Published online Sep 28, 2012. doi: 10.3748/wjg.v18.i36.5034
Interplay of neuropilin-1 and semaphorin 3A after partial hepatectomy in rats
Ling Fu, Tsuneo Kitamura, Kazuhisa Iwabuchi, Syozo Ichinose, Mitsuaki Yanagida, Hideoki Ogawa, Sumio Watanabe, Toshihide Maruyama, Masafumi Suyama, Kenji Takamori
Ling Fu, Tsuneo Kitamura, Kazuhisa Iwabuchi, Syozo Ichinose, Mitsuaki Yanagida, Hideoki Ogawa, Kenji Takamori, Institute for Environmental and Gender Specific Medicine, Juntendo University Graduate School of Medicine, Urayasu 279-0021, Japan
Tsuneo Kitamura, Toshihide Maruyama, Masafumi Suyama, Department of Gastroenterology, Juntendo University Urayasu Hospital, Urayasu 279-0021, Japan
Tsuneo Kitamura, Sumio Watanabe, Toshihide Maruyama, Masafumi Suyama, Department of Gastroenterology, Juntendo University School of Medicine, Tokyo 113-8421, Japan
Author contributions: Fu L and Kitamura T designed the research and wrote the paper; Iwabuchi K and Yanagida M revised the article; Fu L and Ichinose S performed the experiments; Ogawa H, Watanabe S, Maruyama T, Suyama M and Takamori K supervised and approved the final publication.
Supported by A Grant-in-aid for Young Scientists from Japan Society for the Promotion of Science, No. 22790671
Correspondence to: Tsuneo Kitamura, MD, PhD, Department of Gastroenterology, Juntendo University Urayasu Hospital, 2-1-1 Tomioka, Urayasu 279-0021, Japan. kitamura@juntendo.ac.jp
Telephone: +81-47-3533111 Fax: +81-47-3815079
Received: March 29, 2012
Revised: July 3, 2012
Accepted: July 9, 2012
Published online: September 28, 2012
Abstract

AIM: To elucidate the role of neuropilin-1 (Nrp-1) and semaphorin 3A (Sema3A) in sinusoidal remodeling during liver regeneration in rats.

METHODS: Male Wistar/ST rats at 7 wk of age, weighing about 200 g, were used for all animal experiments. In vivo, at 24, 48, 72, 96, 144 and 192 h after two-thirds partial hepatectomy (PHx), the remnant livers were removed. Liver tissues were immunohistochemically stained for Nrp-1, Sema3A and SE-1, a liver sinusoidal endothelial cell (SEC) marker. Total RNA of the liver tissue was extracted and reversely transcribed into cDNA. The mRNA expression of Sema3A was analyzed by quantitative real-time polymerase chain reaction and normalized to that of ribosomal protein S18. In vitro, SECs were isolated from rat liver and cultured in endothelial growth medium containing 20 ng/mL vascular endothelial cell growth factor. Migration of SECs in primary culture was assessed by cell transwell assay with or without recombinant Sema3A. Apoptotic cells were determined by a terminal deoxynucleotidyl transferase-mediated deoxyuridine triphosphate nick end labeling method.

RESULTS: In vitro, immunohistochemistry study revealed that Sema3A and Nrp-1 were constitutively expressed in hepatocytes and SECs, respectively, in normal rat liver tissues. Nrp-1 expression in SECs was quantified by the percentage of immunostained area with anti-Nrp-1 antibody in relation to the area stained with SE-1. Between 24 h and 96 h following resection of liver, Nrp-1 expression in SECs was transiently increased. Compared with the baseline (5.2% ± 0.1%), Nrp-1 expression in SECs significantly increased at 24 h (17.3% ± 0.7%, P < 0.05), 48 h (39.1% ± 0.6%, P < 0.01), 72 h (46.9% ± 4.5%, P < 0.01) and 96 h (29.9% ± 3.8%, P < 0.01) after PHx, then returned to the basal level at termination of liver regeneration. Interestingly, the expression of Sema3A was inversely associated with that of Nrp-1 in liver after PHx. Sema3A mRNA expression was significantly reduced by about 75% over the period 24-144 h after PHx (P < 0.05), and returned to basal levels at 192 h after PHx. In vitro, SECs isolated from rats after PHx (PHx-SECs) were observed to migrate to the lower chamber of the cell transwell system after incubation for 24 h, but not cells from normal rats (CONT-SECs), indicating that mobility of PHx-SECs increases as compared with that of CONT-SECs. Moreover, recombinant Sema3A significantly attenuated migration in PHx-SECs in primary culture (vehicle-treated 100% ± 7.9% vs Sema3A-treated 42.6% ± 5.4%, P < 0.01), but not in CONT-SECs. Compared with CONT-SECs, the apoptotic rate of PHx-SECs decreased by 78.3% (P < 0.05). There was no difference in apoptosis between CONT-SECs that were treated with vehicle and Sema3A. However, in PHx-SECs, apoptosis was induced by the presence of 5 nmol Sema3A for 24 h (vehicle-treated 21.7% ± 7.6% vs Sema3A-treated 104.3% ± 8.9%, P < 0.05). In addition, immunohistochemistry confirmed the increased expression of Nrp-1 in PHx-SECs, while it was noted to a lesser extent in CONT-SECs.

CONCLUSION: The interplay of Nrp-1 and Sema3A shown in our results may lead to a better understanding of interaction between sinusoidal remodeling and SECs during liver regeneration.

Keywords: Neuropilin-1; Semaphorin 3A; Sinusoidal remodeling; Liver regeneration; Two-thirds partial hepatectomy; Angiogenesis; Liver sinusoidal endothelial cells