Original Article
Copyright ©2011 Baishideng Publishing Group Co., Limited. All rights reserved.
World J Gastroenterol. Feb 14, 2011; 17(6): 717-726
Published online Feb 14, 2011. doi: 10.3748/wjg.v17.i6.717
Glutamine depletion induces murine neonatal melena with increased apoptosis of the intestinal epithelium
Takayuki Motoki, Yoshio Naomoto, Junji Hoshiba, Yasuhiro Shirakawa, Tomoki Yamatsuji, Junji Matsuoka, Munenori Takaoka, Yasuko Tomono, Yasuhiro Fujiwara, Hiroshi Tsuchita, Mehmet Gunduz, Hitoshi Nagatsuka, Noriaki Tanaka, Toshiyoshi Fujiwara
Takayuki Motoki, Yoshio Naomoto, Yasuhiro Shirakawa, Tomoki Yamatsuji, Junji Matsuoka, Munenori Takaoka, Yasuhiro Fujiwara, Noriaki Tanaka, Toshiyoshi Fujiwara, Department of Gastroenterological Surgery, Transplant, and Surgical Oncology, Graduate School of Medicine, Dentistry, and Pharmaceutical Sciences, Okayama University, 2-5-1, Shikata-cho, Okayama, 700-8558, Japan
Yoshio Naomoto, Department of General Surgery, Kawasaki Medical School Kawasaki Hospital, 2-1-80, Nakasange, Kita-ku, Okayama, 700-8505, Japan
Junji Hoshiba, Department of Animal Resources, Advanced Science Research Center, Okayama University, 2-5-1, Shikata-cho, Okayama, 700-8558, Japan
Yasuko Tomono, Division of Molecular and Cell Biology, Shigei Medical Research Institute, 2117 Yamada, Okayama, 701-0202, Japan
Hiroshi Tsuchita, Food Technology Research Institute, Meiji Dairies Corporation, 540 Naruda, Odawara, Kanagawa, 250-0862, Japan
Mehmet Gunduz, Hitoshi Nagatsuka, Department of Oral Pathology and Medicine, Graduate School of Medicine, Dentistry, and Pharmaceutical Sciences, Okayama University, 2-5-1, Shikata-cho, Okayama, 700-8558, Japan
Author contributions: Motoki T, Naomoto Y, Matsuoka J, Yamatsuji T, Shirakawa Y, Takaoka M and Tanaka N conceived and designed the study; Motoki T, Naomoto Y, Nagatsuka H and Fujiwara T conducted the study; Hoshiba J produced the feeding bottles; Tsuchita H synthesized the milk; Tomono Y performed the Western blotting; Motoki T and Fujiwara Y statistically analyzed the data; Motoki T, Naomoto Y, Matsuoka J, Yamatsuji T, Shirakawa Y, Takaoka M and Gunduz M wrote the manuscript; all authors were responsible for data interpretation.
Supported by The trust accounts of the Department of Gastroenterological Surgery, Transplant, and Surgical Oncology, Graduate School of Medicine, Dentistry, and Pharmaceutical Sciences, Okayama University
Correspondence to: Yoshio Naomoto, MD, PhD, Professor of Department of General Surgery, Kawasaki Medical School Kawasaki Hospital, 2-1-80, Nakasange, Kita-ku, Okayama, 700-8505, Japan. ynaomoto@med.kawasaki-m.ac.jp
Telephone: +81-86-2252111 Fax: +81-86-2328343
Received: June 20, 2010
Revised: September 17, 2010
Accepted: September 24, 2010
Published online: February 14, 2011
Abstract

AIM: To investigate the possible biological outcome and effect of glutamine depletion in neonatal mice and rodent intestinal epithelial cells.

METHODS: We developed three kinds of artificial milk with different amounts of glutamine; Complete amino acid milk (CAM), which is based on maternal mouse milk, glutamine-depleted milk (GDM), and glutamine-rich milk (GRM). GRM contains three-fold more glutamine than CAM. Eighty-seven newborn mice were divided into three groups and were fed with either of CAM, GDM, or GRM via a recently improved nipple-bottle system for seven days. After the feeding period, the mice were subjected to macroscopic and microscopic observations by immunohistochemistry for 5-bromo-2’-deoxyuridine (BrdU) and Ki-67 as markers of cell proliferation, and for cleaved-caspase-3 as a marker of apoptosis. Moreover, IEC6 rat intestinal epithelial cells were cultured in different concentrations of glutamine and were subject to a 4-[3-(4-iodophenyl)-2-(4-nitrophenyl)-2H-5-tetrazolio]-1,3-benzene disulfonate cell proliferation assay, flow cytometry, and western blotting to examine the biological effect of glutamine on cell growth and apoptosis.

RESULTS: During the feeding period, we found colonic hemorrhage in six of 28 GDM-fed mice (21.4%), but not in the GRM-fed mice, with no differences in body weight gain between each group. Microscopic examination showed destruction of microvilli and the disappearance of glycocalyx of the intestinal wall in the colon epithelial tissues taken from GDM-fed mice. Intake of GDM reduced BrdU incorporation (the average percentage of BrdU-positive staining; GRM: 13.8%, CAM: 10.7%, GDM: 1.14%, GRM vs GDM: P < 0.001, CAM vs GDM: P < 0.001) and Ki-67 labeling index (the average percentage of Ki-67-positive staining; GRM: 24.5%, CAM: 22.4% GDM: 19.4%, GRM vs GDM: P = 0.001, CAM vs GDM: P = 0.049), suggesting that glutamine depletion inhibited cell proliferation of intestinal epithelial cells. Glutamine deprivation further caused the deformation of the nuclear membrane and the plasma membrane, accompanied by chromatin degeneration and an absence of fat droplets from the colonic epithelia, indicating that the cells underwent apoptosis. Moreover, immunohistochemical analysis revealed the appearance of cleaved caspase-3 in colonic epithelial cells of GDM-fed mice. Finally, when IEC6 rat intestinal epithelial cells were cultured without glutamine, cell proliferation was significantly suppressed after 24 h (relative cell growth; 4 mmol/L: 100.0% ± 36.1%, 0 mmol/L: 25.3% ± 25.0%, P < 0.05), with severe cellular damage. The cells underwent apoptosis, accompanied by increased cell population in sub-G0 phase (4 mmol/L: 1.68%, 0.4 mmol/L: 1.35%, 0 mmol/L: 5.21%), where dying cells are supposed to accumulate.

CONCLUSION: Glutamine is an important alimentary component for the maintenance of intestinal mucosa. Glutamine deprivation can cause instability of the intestinal epithelial alignment by increased apoptosis.

Keywords: Glutamine, Newborn mice, Artificial milk, Melena, Intestinal epithelial cells, Apoptosis