Massive bowel resection upregulates the intestinal mRNA expression levels of cellular retinol-binding protein II and apolipoprotein A-IV and alters the intestinal vitamin A status in rats

Hebiguchi,Taku; Mezaki,Yoshihiro; Morii,Mayako; Watanabe,Ryo; Yoshikawa,Kiwamu; Miura,Mitsutaka; Imai,Katsuyuki; Senoo,Haruki; Yoshino,Hiroaki

doi:10.3892/ijmm.2015.2066

Massive bowel resection upregulates the intestinal mRNA expression levels of cellular retinol-binding protein II and apolipoprotein A-IV and alters the intestinal vitamin A status in rats

Authors:
- Taku Hebiguchi
- Yoshihiro Mezaki
- Mayako Morii
- Ryo Watanabe
- Kiwamu Yoshikawa
- Mitsutaka Miura
- Katsuyuki Imai
- Haruki Senoo
- Hiroaki Yoshino
View Affiliations

Affiliations: Department of Pediatric Surgery, Akita University Graduate School of Medicine, Akita 010-8543, Japan, Department of Cell Biology and Morphology, Akita University Graduate School of Medicine, Akita 010-8543, Japan
Published online on: January 12, 2015 https://doi.org/10.3892/ijmm.2015.2066
Pages: 724-730

Metrics: Total Views: 0 (Spandidos Publications: | PMC Statistics: )

Metrics: Total PDF Downloads: 0 (Spandidos Publications: | PMC Statistics: )

Cited By (CrossRef): 0 citations Loading Articles...

Abstract

Short bowel (SB) syndrome causes the malabsorption of various nutrients. Among these, vitamin A is important for a number of physiological activities. Vitamin A is absorbed by epithelial cells of the small intestine and is discharged into the lymphatic vessels as a component of chylomicrons and is delivered to the liver. In the present study, we used a rat model of SB syndrome in order to assess its effects on the expression of genes associated with the absorption, transport and metabolism of vitamin A. In the rats with SB, the intestinal mRNA expression levels of cellular retinol-binding protein II (CRBP II, gene symbol Rbp2) and apolipoprotein A-IV (gene symbol Apoa4) were higher than those in the sham-operated rats, as shown by RT-qPCR. Immunohistochemical analysis revealed that absorptive epithelial cells stained positive for both CRBP II and lecithin retinol acyltransferase, which are both required for the effective esterification of vitamin A. In the rats with SB, the retinol content in the ileum and the retinyl ester content in the jejunum were lower than those in the sham-operated rats, as shown by quantitative analysis of retinol and retinyl esters by high performance liquid chromatography. These results suggest that the elevated mRNA expression levels of Rbp2 and Apoa4 in the rats with SB contribute to the effective esterification and transport of vitamin A.

View Figures

View References

1	Duro D, Kamin D and Duggan C: Overview of pediatric short bowel syndrome. J Pediatr Gastroenterol Nutr. 47(Suppl 1): S33–S36. 2008. View Article : Google Scholar : PubMed/NCBI
2	Wall EA: An overview of short bowel syndrome management: adherence, adaptation, and practical recommendations. J Acad Nutr Diet. 113:1200–1208. 2013. View Article : Google Scholar : PubMed/NCBI
3	Shaw D, Gohil K and Basson MD: Intestinal mucosal atrophy and adaptation. World J Gastroenterol. 18:6357–6375. 2012. View Article : Google Scholar : PubMed/NCBI
4	Wang L, Tang Y, Rubin DC and Levin MS: Chronically administered retinoic acid has trophic effects in the rat small intestine and promotes adaptation in a resection model of short bowel syndrome. Am J Physiol Gastrointest Liver Physiol. 292:G1559–G1569. 2007. View Article : Google Scholar : PubMed/NCBI
5	Harrison EH: Mechanisms of digestion and absorption of dietary vitamin A. Annu Rev Nutr. 25:87–103. 2005. View Article : Google Scholar : PubMed/NCBI
6	Blomhoff R and Blomhoff HK: Overview of retinoid metabolism and function. J Neurobiol. 66:606–630. 2006. View Article : Google Scholar : PubMed/NCBI
7	Wake K: ‘Sternzellen’ in the liver: perisinusoidal cells with special reference to storage of vitamin A. Am J Anat. 132:429–462. 1971. View Article : Google Scholar : PubMed/NCBI
8	Senoo H: Structure and function of hepatic stellate cells. Med Electron Microsc. 37:3–15. 2004. View Article : Google Scholar : PubMed/NCBI
9	Newcomer ME: Retinoid-binding proteins: structural determinants important for function. FASEB J. 9:229–239. 1995.PubMed/NCBI
10	Flower DR, North AC and Sansom CE: The lipocalin protein family: structural and sequence overview. Biochim Biophys Acta. 1482:9–24. 2000. View Article : Google Scholar : PubMed/NCBI
11	Sherman DR, Lloyd RS and Chytil F: Rat cellular retinol-binding protein: cDNA sequence and rapid retinol-dependent accumulation of mRNA. Proc Natl Acad Sci USA. 84:3209–3213. 1987. View Article : Google Scholar : PubMed/NCBI
12	Colantuoni V, Cortese R, Nilsson M, Lundvall J, Bavik CO, Eriksson U, Peterson PA and Sundelin J: Cloning and sequencing of a full length cDNA corresponding to human cellular retinol-binding protein. Biochem Biophys Res Commun. 130:431–439. 1985. View Article : Google Scholar : PubMed/NCBI
13	Li E, Demmer LA, Sweetser DA, Ong DE and Gordon JI: Rat cellular retinol-binding protein II: use of a cloned cDNA to define its primary structure, tissue-specific expression, and developmental regulation. Proc Natl Acad Sci USA. 83:5779–5783. 1986. View Article : Google Scholar : PubMed/NCBI
14	E X, Zhang L, Lu J, Tso P, Blaner WS, Levin MS and Li E: Increased neonatal mortality in mice lacking cellular retinol-binding protein II. J Biol Chem. 277:36617–36623. 2002. View Article : Google Scholar : PubMed/NCBI
15	Takase S, Goda T and Shinohara H: Adaptive changes of intestinal cellular retinol-binding protein, type II following jejunum-bypass operation in the rat. Biochim Biophys Acta. 1156:223–231. 1993. View Article : Google Scholar : PubMed/NCBI
16	Dodson BD, Wang JL, Swietlicki EA, Rubin DC and Levin MS: Analysis of cloned cDNAs differentially expressed in adapting remnant small intestine after partial resection. Am J Physiol. 271:G347–G356. 1996.PubMed/NCBI
17	Wang JL, Swartz-Basile DA, Rubin DC and Levin MS: Retinoic acid stimulates early cellular proliferation in the adapting remnant rat small intestine after partial resection. J Nutr. 127:1297–1303. 1997.PubMed/NCBI
18	Ong DE, Kakkad B and MacDonald PN: Acyl-CoA-independent esterification of retinol bound to cellular retinol-binding protein (type II) by microsomes from rat small intestine. J Biol Chem. 262:2729–2736. 1987.PubMed/NCBI
19	Yost RW, Harrison EH and Ross AC: Esterification by rat liver microsomes of retinol bound to cellular retinol-binding protein. J Biol Chem. 263:18693–18701. 1988.PubMed/NCBI
20	Rubin DC, Swietlicki EA, Wang JL, Dodson BD and Levin MS: Enterocytic gene expression in intestinal adaptation: evidence for a specific cellular response. Am J Physiol. 270:G143–G152. 1996.PubMed/NCBI
21	Green PH, Glickman RM, Riley JW and Quinet E: Human apolipoprotein A-IV Intestinal origin and distribution in plasma. J Clin Invest. 65:911–919. 1980. View Article : Google Scholar : PubMed/NCBI
22	Goodman DW, Huang HS and Shiratori T: Tissue distribution and metabolism of newly absorbed vitamin A in the rat. J Lipid Res. 6:390–396. 1965.PubMed/NCBI
23	Ruiz A, Winston A, Lim YH, Gilbert BA, Rando RR and Bok D: Molecular and biochemical characterization of lecithin retinol acyltransferase. J Biol Chem. 274:3834–3841. 1999. View Article : Google Scholar : PubMed/NCBI
24	Ong DE and Chytil F: Cellular retinol-binding protein from rat liver Purification and characterization. J Biol Chem. 253:828–832. 1978.PubMed/NCBI
25	Napoli JL: Interactions of retinoid binding proteins and enzymes in retinoid metabolism. Biochim Biophys Acta. 1440:139–162. 1999. View Article : Google Scholar : PubMed/NCBI
26	Bok D, Ruiz A, Yaron O, Jahng WJ, Ray A, Xue L and Rando RR: Purification and characterization of a transmembrane domain-deleted form of lecithin retinol acyltransferase. Biochemistry. 42:6090–6098. 2003. View Article : Google Scholar : PubMed/NCBI
27	Moise AR, Golczak M, Imanishi Y and Palczewski K: Topology and membrane association of lecithin:retinol acyltransferase. J Biol Chem. 282:2081–2090. 2007. View Article : Google Scholar
28	Senoo H, Mezaki Y, Morii M, Hebiguchi T, Miura M and Imai K: Uptake and storage of vitamin A as lipid droplets in the cytoplasm of cells in the lamina propria mucosae of the rat intestine. Cell Biol Int. 37:1171–1180. 2013.PubMed/NCBI
29	Wakabayashi Y, Yamada E, Yoshida T and Takahashi H: Arginine becomes an essential amino acid after massive resection of rat small intestine. J Biol Chem. 269:32667–32671. 1994.PubMed/NCBI
30	Hebiguchi T, Kato T, Yoshino H, Mizuno M, Wakui H, Komatsuda A and Imai H: Extremely short small bowel induces focal tubulointerstitial fibrosis. J Pediatr Gastroenterol Nutr. 32:586–592. 2001. View Article : Google Scholar : PubMed/NCBI
31	Taguchi S, Masumoto K, Yamanouchi T and Suita S: Decrease in hepatic circulation induces hepatic fibrosis in a neonatal piglet model with short bowel syndrome. J Pediatr Surg. 40:1592–1597. 2005. View Article : Google Scholar : PubMed/NCBI
32	Senoo H and Wake K: Suppression of experimental hepatic fibrosis by administration of vitamin A. Lab Invest. 52:182–194. 1985.PubMed/NCBI