QUICK SEARCH:   [advanced] Author: Keyword(s): Year:  Vol:  Page:

This Article Abstract Full Text (PDF) Purchase Article View Shopping Cart Alert me when this article is cited Alert me if a correction is posted Services Similar articles in this journal Similar articles in PubMed Alert me to new issues of the journal Download to citation manager Citing Articles Citing Articles via HighWire Citing Articles via Google Scholar Google Scholar Articles by Gal-Garber, O. Articles by Uni, Z. Search for Related Content PubMed PubMed Citation Articles by Gal-Garber, O. Articles by Uni, Z.

---

Article

Partial Sequence and Expression of the Gene for and Activity of the Sodium Glucose Transporter in the Small Intestine of Fed, Starved and Refed Chickens

The Faculty of Agricultural, Food and Environmental Quality Sciences, The Hebrew University of Jerusalem, Rehovot, 76100 Israel

¹To whom correspondence should be addressed.

	ABSTRACT

TOP ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS DISCUSSION REFERENCES

 
A 970 bp cDNA Na⁺/glucose cotransporter (SGLT1) was isolated and sequenced from chicken jejunum by reverse transcriptase polymerase chain reaction (RT-PCR) using primers based on conserved regions. Using the 970 bp PCR product as a specific probe, Northern Blot hybridization indicated a transcript of ca. 4 kb. The isolated chicken intestinal SGLT1 cDNA was used to quantitate mRNA expression. Glucose uptake activity and kinetics were determined in brush border membrane vesicles (BBMV) from jejunum tissue of chickens which were either fed, food-deprived or refed following food deprivation. Net glucose uptake to BBMV was higher (P < 0.02) in the control and refed chicks (149 ± 11.9, 139.6 ± 7.43 pmol · mg protein^-1 · s^-1) than in food-deprived chicks (107 ± 4.23 pmol · mg protein^-1 · s^-1). The k_m (150 µmol/L) and Vmax (1111.1 pmol · mg protein^-1 · s^-1) were higher in the food-deprived chicks compared to control and refed birds (25, 24 µmol/L and 227, 142 pmol · mg protein^-1 · s^-1, respectively). Expression of SGLT1 mRNA was significantly enhanced in the food-deprived and refed birds. In food-deprived chicks the lower affinity and higher activity of the SGLT1 transporter for glucose were accompanied by higher expression of mRNA which might indicate that the transporter was upregulated by low substrate concentration. Quantification of expression of intestinal mRNA of SGLT1 provides important information concerning control of nutrient uptake.

KEY WORDS: • chickens • small intestine • Na⁺ • Glucose cotransporter (SGLT1) • gene sequence.

	INTRODUCTION

TOP ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS DISCUSSION REFERENCES

 
The processes of intestinal absorption of carbohydrates are mediated by transporters localized in the brush border membranes of the enterocytes (Semenza 1986 , Thorens 1996 ). These transporters play a fundamental role in uptake of glucose from the diet, providing glucose as an immediate source of energy for cellular metabolism. Two types of transporters are involved in the brush border membrane hexose transport in the small intestine of higher organisms: i) facilitated glucose transporters (GLUT)² and ii) Na⁺ coupled glucose transporters (SGLT). These transporters are synthesized by two different gene families; SGLT1 and GLUT5 have been mapped to chromosomes 22 and 1 in humans, respectively (Turk et al. 1993 , White et al. 1998 ). In enterocytes of the small intestine, GLUT5 facilitates passive movement of fructose across the plasma membranes down a concentration gradient (Bell et al. 1993 , Marger and Saler 1993 , Rong et al. 1998 , Thorens 1993 ). In contrast, SGLT1 actively transports glucose and galactose together with sodium against concentration gradients (Hirayama et al. 1997 , Wright 1993 ). SGLT1 is the major determinant of small intestinal glucose uptake by animals (Hediger and Rhoads 1994 , Wright 1993 ).

The activity of SGLT1 is regulated by age and by dietary substrate levels in some species. In lambs, both activity and mRNA expression of SGLT1 increased to maximum levels within the first 2 wk after birth and then declined to low constant levels which were maintained over 2–3 y (Freeman et al. 1993 , Shirazi-Beechey et al. 1991). In rats, hexose uptake activity increased with age, with a particularly sharp increase around the time of weaning (Toloza and Diamond 1992 ). Increased levels of nutrients at the lumen of small intestine increased activity and expression of SGLT1 in humans (Dyer et al. 1997 ).

The sequence of SGLT1 in the small intestine has been reported for some species: cDNA of SGLT1 was isolated from rabbit (Hediger et al. 1987 , Morrison et al. 1991 ), human (Hediger et al. 1989 ) and sheep (Tarpey et al. 1995 ) small intestine. However, to date, no sequence information on the chicken small intestine SGLT1 has been reported.

Modern meat-type chickens receive about 60% of their diet as carbohydrate, and the efficiency of hexose uptake plays an important role in determining growth. Therefore, the regulation of SGLT1, which plays a central role in glucose uptake, is important.

In this study, a 970-bp cDNA fragment of chick small intestine SGLT1 was isolated, sequenced, and used as a probe to determine its mRNA expression and glucose uptake activity as influenced by nutritional status.

	MATERIALS AND METHODS

TOP ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS DISCUSSION REFERENCES

 
Animals and diets.

Male chicks (Arbor Acres, Glastonbury, CT), were obtained from a commercial hatchery (Yavne Hatcheries, Yavne, Israel) on the day of hatch and maintained under standardized temperature and humidity conditions. The birds were fed corn-soybean based diets formulated to meet or exceed NRC (1994) requirements and had free access to water and food. At the age of 6 wk they were randomly blocked to two dietary treatments (30 chicks/treatment): one treatment had no access to food for 4 d (food-deprived) and the other treatment had free access to food (control). After 4 d, 15 birds from the starved group were allowed access to food for 2 d (Refed). Chicks were killed and the jejunum was removed for mucosal enzyme activity measurement and RNA isolation. All procedures were approved by the Animal Care and Ethics Committee of the Hebrew University of Jerusalem.

Sampling and collection of tissues.

The jejunum was removed from the common bile duct to Meckel’s diverticulum. Segments were flushed with cold 9 g/L NaCl to remove the intestinal digesta, and 2.5-cm sections were dissected for the isolation of total RNA. The rest of the segment was used for further analysis. The epithelial layer was scraped gently with a glass slide for preparation of brush border membrane vesicles (BBMV). Samples were then immediately frozen in liquid nitrogen and then stored at -80°C until further treatment.

Preparation of BBMV.

BBMV were prepared using MgCl₂ precipitation and sequential centrifugation as described by Zhao et al. (1998) . The final protein concentration in BBMV was 9–15 g/L. Aliquots of 50–100 µL of BBMV were frozen in liquid nitrogen and stored at -80°C until use. Enrichment in specific activity of -glutamyl transpeptidase (-GT) in BBMV was 14- to 22-fold compared to homogenates.

Assay of glucose uptake in BBMV.

SGLT1 uptake activity was determined at 37°C as described by Shirazi-Beechey et al. (1981) . Briefly, a suspension of 10 µL of BBMV was added into 190 µL solution containing either 150 mmol/L NaCl or KCl and 30 µmol/L D-Glucose-[6-³H(n)] (Sigma Chemical, St. Louis, MO). The reaction was stopped after 3 s by addition of 2 mL of an ice-cold solution containing 150 mmol/L NaCl and 0.25 mmol/L phlorizin (Lescale-Matys et al. 1993 ). Uptake was measured in duplicate in each individual BBMV for each bird within dietary treatments. The variation in uptake was less then 2% in multiple assays of the same preparation. The SGLT1 kinetics were measured in pooled BBMV from chicks in the same dietary treatments. D-glucose concentrations ranged from 1 to 70 µmol/L in 150 mmol/L NaCl or KCl. Na⁺-dependent uptake activity was calculated as the difference between uptake measured in the presence and absence of Na⁺. Lineweaver-Burke plots were utilized to calculate the kinetic parameters, K_m and V_max.

RNA preparation.

Total RNA was isolated from the jejunal tissues using TRI REAGENT (1 mL/100 mg tissue) according to the manufacturer’s protocol (MRC Molecular research Center, Cincinnati, OH).

Isolation and sequence of fragment from chicken SGLT1 gene.

A comparison of five different published sequences of the SGLT1 gene from different sources: rat intestine (GeneBank/EMBL Rnu03120), porcine kidney epithelial cell line LLC-PK (GeneEMBL pigsglt1a), rabbit intestine (GeneBank/EMBL ocnaglut), ovine enterocyte (GeneBank/EMBL oasgcotr) and human intestine (GeneBank/EMBL humsglt1) enabled us to identify common regions. The two primers, chosen from conserved regions were: (forward) 5'- TGGCGGGCTTCTACCGCAGCGAG- 3'; (reverse) 5'- CCCGGTAGGTCACCAGTCCCCAG-3'.

Total RNA was amplified using the Promega Access RT-PCR System according to the manufacturer’s (Promega Corporation, Madison, WI). The program used was: 2 min at 94°C, 30 s at 60°C, 2 min at 68°C for 30 cycles followed by 7 min at 68°C.

The RT-PCR products were examined on a 1.5% agarose gel, visualized by staining with ethidium bromide, excised from the gel and purified with a gel extraction column (Wizard PCR Preps DNA purification system; Promega Corporation). The chicken SGLT1 cDNA fragment was subjected to automated sequencing using an Applied Biosystem 373A DNA sequencer (Applied Biosystems, Foster City, CA) Nucleic acid sequences were analyzed using the GCG suite of programs (Devereux et al. 1984 ) on a VAX 4000–300 computer and yielded a segment of 970 bp. The homology between chicken and other SGLT1s sequences was calculated using DNAMAN version 4 (Lynnon Biosoft 1994–1997, Quebec, Canada).

Northern blot.

For Northern blot analysis, 30 µg of total RNA was denatured and separated by electrophoresis on 1.5% agarose/1.1 mol/L formaldehyde gel. After electrophoresis, RNA was transferred overnight by capillary transfer to a nylon filter Hybond-N (Amersham Pharmacia Biotech, Amersham, United Kingdom) and then fixed on the filter by UV at 340 nm for 2 min.

Dot blot.

Total RNA (30 µg) from each jejunal tissue in all dietary treatments were spotted on Hybond-N nylon membrane for dot blot analysis, according to the Amersham procedure (Amersham Pharmacia Biotech) and then fixed on the filter by UV 340 nm for 2 min.

Hybridization.

Two probes were used for hybridization: i The isolated cDNA fragment of chicken SGLT1 and the glyceraldehyde-3-phosphate dehydrogenase (GAPDH) cDNA in order to normalize variations in the total RNA loading. The probes were labeled with ³²P-dCTP by the random prime labeling method (Biological Industries, Kibbutz Beit Haemek, Israel). Prehybridization was done at 42°C for 4 h, hybridization was conducted at 42°C overnight and high-stringency wash [0.1X saline sodium citrate (SSC)/0.1% sodium dodecyl sulfate (SDS) at 60°C] was conducted according to the procedures recommended by Amersham for Hybond N membranes (Amersham Pharmacia Biotech). Blots were exposed for 24 h at -70°C to Kodak XAR 5 film in the presence of an intensifying screen.

Statistics.

Data are expressed as means ± SEM Statistical comparisons were made using ANOVA and t tests between pairs of treatments using the GLM procedures of SAS (SAS 1986 ). Differences were considered significant when P < 0.05.

	RESULTS

TOP ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS DISCUSSION REFERENCES

 
Isolated SGLT1 fragment.

The predicted amino acid sequence of the cDNA fragment isolated from the total RNA of chick jejunum using RT- PCR procedure is shown in Figure 1 . The predicted amino acid sequence of this fragment resulted in a translation product of 322 amino acids. Expression of SGLT1 using this cDNA as a probe in a Northern Blot procedure resulted in a transcript of ca. 4 kb in the jejunum (Fig. 2 ). SGLT1 and GAPDH mRNA levels are presented in Figures 3A and B in chicks under different nutritional status. The SGLT1/GAPDH ratio (Fig. 3C) indicated that expression of SGLT1 mRNA was highest in refed chicks, intermediate in the food-deprived chicks and lowest in the control chicks (P < 0.02).

View larger version (105K): [in this window] [in a new window]   Figure 1. Predicted partial amino acids sequences of chicken sodium glucose transporter (SGLT1). The alignment of predicted amino acid sequences of chicken SGLT1 with sheep, rabbit and human SGLT1. Identical residue species are marked. Predicted membrane-spanning regions are marked by lines numbered from 1 to 6. Consensus sequence for n-linked glycosylation site N-X-N/S are bold.

View larger version (80K): [in this window] [in a new window]   Figure 2. Northern blot of chicken jejunum RNA. A radioactively labeled 970 bp jejunum RT-PCR product was used as hybridization probe and the exposure time was 24 h at -70°C. A band at proximal of 4 kb was obtained.

View larger version (45K): [in this window] [in a new window]   Figure 3. Expression of sodium glucose transporter (SGLT1) in control, food-deprived and refed chicks. Expression of SGLT1 was determined by Dot blot analysis using the 970-bp jejunum RT-PCR product as probe (A) in a representative assay. The same blots were rehybridized with radioactive glyceraldehyde 3-phosphate dehydrogenase (GAPDH) as a reference probe (B) Exposure time was 24 h at -70°C. (C) The ratio of SGLT1 and GAPDH. Results are means ± SE, n = 5. Bars without the same letter differ, P < 0.02.

Glucose uptake was greater (P < 0.02) in control and refed chicks than in the starved chicks (149.0, 139.6 and 107.6 pmol · mg protein^-1 · s^-1, SEM = 8.44). The Lineweaver-Burke plots for all treatment groups were significant linear regressions (P < 0.001) with high correlation coefficients (R² = 0.95 to 0.99, Fig. 4A–C ). The calculated V_max (Fig. 4D ) and Michaelis-Menten constants (k_m) (Fig. 4E ) were 4.5- and 5-fold higher in the food-deprived chicks than in either the control or refed chicks.

View larger version (19K): [in this window] [in a new window]   Figure 4. Sodium glucose transporter (SGLT1) kinetics in brush border membrane vesicles (BBMV) from control, food-deprived and refed chicks. SGLT1 kinetics were determined in BBMV (n = 5) from: control (A), food-deprived (B), and refed (C) chicks. Kinetic parameters (Vmax, D and Km, E) were calculated from Lineweaver-Burke plots for the different dietary treatments.

	DISCUSSION

TOP ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS DISCUSSION REFERENCES

The chick SGLT1 amino acid sequence reported here was highly comparable (84–88%) with that of humans (Hediger and Rhoads 1994 ), sheep (Tarpey et al. 1995 ), rabbits (Morrison et al. 1991 ) and rats (Lee et al. 1994 ). A similar degree of homology between chicken aminopeptidase gene was also reported when compared with mammals (Gal-Garber and Uni 2000 ). The SGLT1 protein included the location of the predicted membrane spanning domains including six possible putative membrane-spanning domains (1 to 6), and one consensus sequence for n-linked glycosylation site N-X-N/S (Hediger and Rhoads 1994 ). The size of the chicken SGLT1 gene (4 kb) was similar to human and rat SGLT1 (Dyer et al. 1997 , Hediger and Rhoads 1994 , Rong et al. 1997 ).

The kinetic parameters of glucose uptake revealed high affinity for D-glucose with a k_m ranging from 25 to 150 µmol/L in jejunum of chicks in the different dietary treatment groups. These values are within the range previously reported for cattle (100 µmol/L; Zhao et al. 1998 ), rats, rabbits and humans (13 to 490 µmol/L; Freeman and Quamme 1986 , Panayotova-Heiermann et al. 1996 ).

Expression of SGLT1 mRNA was affected by nutritional status. The lowest levels of mRNA were found in control chicks, whereas both starved and refed birds had higher expressions of SGLT1. Net glucose uptake in BBMV was higher in the control and refed chicks than in the food-deprived birds. Thus, lower affinity and activity of the SGLT1 transporter for glucose were accompanied by higher expression of the gene in the starved chickens. In previous studies in other species, a greater number of glucose carriers (higher V_max) was observed in the small intestine of malnourished infant rabbits (Buntzner et al. 1990 ). In contrast, at high dietary supply of glucose, facilitated glucose uptake was enhanced and transporters tended to be down-regulated by their substrates (Ferraris et al. 1989 , Sharp et al. 1996 ). Thus, at high levels of substrate, as in the case of the fed and refed animals, fewer transporters with higher affinity suffice for transport of the dietary substrate to supply nutritional requirements. In the food-deprived chicks, the higher expression and lower affinity of the transporter may be also related to higher turnover and degradation rate at the microvillus membrane as has been shown in other experimental models (Fedorak et al. 1989 , Ferraris and Diamond 1986). However, in this study, we examined SGLT1 mRNA expression only at one point after refeeding. In starved chicks the rates of proliferation and maturation of enterocytes may also be influenced, thus changing mRNA expression. The higher expression of mRNA following starvation in chicks is similar to results observed in determining lactase gene expression in rats (Hodin et al. 1994 and 1995 ). However, high expression of SGLT1 was also observed in the refed chicks, although the K_m and V_max did not differ from the control group. A parallel high expression of lactase mRNA was observed in starved and then refed rats. However, after 48 h of refeeding, expression decreased to that in the normal fed state (Hodin et al. 1994 and 1995 ). In White Leghorn hens, higher mitotic activity was observed after refeeding than during food-deprivation (Yamauchi et al. 1996 ). Thus, the higher mRNA expression observed here in jejunal tissue of the refed chicks might be a result of increased enterocyte proliferation and differentiation. Since we did not directly determine SGLT1 concentrations, but rather its activity, it is possible that some form of regulation of translation occurs, as indicated by the lower V_max in refed chicks. It thus appears that starvation and refeeding alter both expression and translation of the SGLT1 in different ways in the chicken jejunum.

This study demonstrates that quantification of expression of intestinal mRNA of SGLT1 provides important information concerning the control of nutrient uptake.

	ACKNOWLEDGMENTS

 
The authors thank Guy Dafna for technical assistance.

	FOOTNOTES

 
² Abbreviations used: BBMV, brush border membrane vesicles; -GT, -glutamyl transpeptidase; GAPDH, glyceraldehyde-3-phosphate dehydrogenase; GLUT, glucose transporters; RT-PCR, reverse transcriptase polymerase chain reaction; SGLT1, Na+/glucose cotransporter.

Manuscript received February 17, 2000. Initial review completed March 29, 2000. Revision accepted May 15, 2000.

	REFERENCES

TOP ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS DISCUSSION REFERENCES

 

1. Bell G. I., Burant C. F., Takeda J., Gould G. W. Molecular biology of glucose transporters. J. Biol. Chem. 1993;268:19161-19164[Free Full Text]

2. Buntzner J. D., Brockway P. D., Meddings J. B. Effects of malnutrition on microvillus membrane glucose transport and physical properties. Am. J. Physiol. 1990;259:G940-G946[Abstract/Free Full Text]

3. Devereux J., Haeberli P., Smithies O. A comprehensive set of sequence analysis programs for the VAX. Nucleic-Acids-Res 1984;12:387-395

4. Dyer J., Hosie K. B., Shirazi-Beechey S. P. Nutrient regulation of human intestinal sugar transporter (SGLT1) expression. Gut 1997;41:56-59[Abstract/Free Full Text]

5. Fedorak R. N., Gershon M. D., Field M. Induction of intestinal glucose carriers in streptozocin-treated chronically diabetic rates. Gastroenterol 1989;96:37-44[Medline]

6. Ferraris R. P., Diamond J. M. Specific regulation of intestinal nutrient transporters by their dietary substrates. Ann. Rev. Physiol. 1989;51:125-141[Medline]

7. Freeman H. J., Quamme G. A. Age-related changes sodium-dependent glucose transporter in rat small intestine. Am. J. Physiol. 1986;251:G208-G217[Medline]

8. Freeman T. C., Wood I. S., Sirinathsinghji D.J.S., Brian Beechey R., Dyer J., Shirazi-Beechey S. P. The expression of the Na⁺/glucose cotransporter (SGLT1) gene in lamb small intestine during postnatal development. Biochem. Biophys. Acta 1993;1146:203-212[Medline]

9. Gal-Garber O., Uni Z. Chicken intestinal aminopeptidase: partial sequence of the gene, expression and activity. Poult. Sci. 2000;79:41-45[Abstract/Free Full Text]

10. Hediger M. A., Coady M. J., Ikeda T. S., Wright E. M. Expression, cloning and cDNA sequence of Na⁺/glucose cotransporter. Nature 1987;330:379-381[Medline]

11. Hediger M. A., Rhoads D. B. Molecular physiology of sodium-glucose cotransporters. Physiol. Rev. 1994;74:993-1026[Free Full Text]

12. Hediger M. A., Turk E., Wright E. M. Homology of the human intestinal Na⁺/glucose and Escherichia coli Na⁺/proline cotransporters. Proc. Natl. Acad. Sci. U.S.A. 1989;86(15):5748-5752[Abstract/Free Full Text]

13. Hirayama B. A., Loo D.D.F., Wright E. M. Cation effects on protein conformation and transport in the Na⁺/glucose cotransporter. J. Biol. Chem. 1997;272:2110-2115[Abstract/Free Full Text]

14. Hodin R. A., Chamberlain M. S., Mang S. Pattern of rat intestinal brush-border enzyme gene expression changes with epithelial growth state. Am. J. Physiol. 1995;269:C385-C391[Abstract/Free Full Text]

15. Hodin R. A., Graham J. R., Meng S., Upton M. P. Temporal pattern of rat small intestinal gene expression with refeeding. Am. J. Physiol. 1994;266:G83-G89[Abstract/Free Full Text]

16. Lee W. S., Kanai Y., Wells R. G., Hediger M. A. The high affinity Na⁺/glucose cotransporter: re-evaluation of function and distribution of expression. J. Biol. Chem. 1994;369:12032-12039

17. Lescale-Matys L., Dyer J., Scot D., Freeman T. C., Wright E. M., Shirazi-Beechey S. P Regulation of the ovine intestinal/Na⁺ glucose co-transporter (SGLT1) is dissociated from mRNA abundance. Biochem. J. 1993;291:435-440

18. Marger M. D., Saler M. H. A major superfamily of transmembrane facilitators that catalyze uniport, symport and antiport. Trends Biochem. Sci. 1993;18:13-20[Medline]

19. Morrison A. I., Panayotova-Heiermann M., Feigl G., Scholermann B., Kinne R.K.H. Sequence comparison of the sodium-d-glucose cotransporter systems in rabbit renal and intestinal epithelia. Biochem. Biophys. Acta 1991;1089:121-123[Medline]

20. National Research Council Nutritional Requirements for Poultry 9th Ed. 1994 National Academy Press Washington, D.C.

21. Panayotova-Heiermann M, Loo D.D.F., Kong C. T., Lever J., Wright E. M. Sugar binding to Na⁺/glucose contransporters is determined by the carboxy-terminal half of the protein. J. Biol. Chem. 1996;271:10029-10043[Abstract/Free Full Text]

22. Rong S., Elmer S. D., Ferraris R. P. Luminal fructose modulates fructose transport and GLUT-5 expression in small intestine of weaning rats. Am. J. Physiol. 1998;274:G232-G239[Abstract/Free Full Text]

23. Rong D., Srai S. K., Debnam E., Smith M. Transcriptional and translational control over sodium-glucose-linked transporter (SGLT!) gene expression in adult small intestine. FEBS Letters 1997;406:79-82[Medline]

24. SAS Institute SAS Users Guide, version 6 1986 SAS Institute Cary, NC.

25. Semenza G. Anchoring and biosynthesis of stalked brush border membrane protein: glycosidases and peptidases of enterocytes and of renal tubuli. Ann. Rev. Cell Biol. 1986;2:255-313

26. Sharp P. A., Debnam E. S., Srai S.K.S. Rapid enhancement of brush border glucose uptake after exposure of rat jejunal mucosa to glucose. Gut 1996;39:545-550[Abstract/Free Full Text]

27. Shirazi S. P., Beechy R. B., Butterworth P. J. The use of potent inhibitors of alkaline phosphatase to investigate the role of inorganic phosphate. Biochem. J. 1981;194:803-809[Medline]

28. Shirazi-Beechey S. P., Hirayama B. A., Wang Y., Scott D., Smith M. W., Wright E. M. Ontogenic development of lamb intestinal sodium-glucose co-transporter is regulated by diet. J. Physiol. 1981;437:699-708[Abstract/Free Full Text]

29. Tarpey P. S., Wood I. S., Shirazi-Beechey S. P., Beechey R. B. Amino acid sequence and the cellular location of the Na⁺ dependent D-glucose symporters (SGLT1) in the ovine enterocyte and the parotid acinar cell. Biochem. J. 1995;312(Pt1):293-300

30. Thorens B. Facilitated glucose transporters in epithelial cells. Ann. Rev. Physiol. 1993;55:591-608[Medline]

31. Thorens B. Glucose transporters in the regulation of intestinal, renal and liver glucose fluxes. Am. J. Physiol. 1996;270:G541-G553[Abstract/Free Full Text]

32. Toloza E. M., Diamond J. M. Ontogenetic development of nutrient transporters in rat intestine. Am. J. Physiol. 1992;263:G593-G604[Abstract/Free Full Text]

33. Turk E., Klisak I., Bacallao R., Sparkes R. S., Wright E. M. Assignment of the human Na⁺/glucose cotransporter gene SGLT1 to chromosome 22q13.1. Genomics 1993;17:752-754[Medline]

34. White P. S., Jensen S. J., Rajalingam V., Stairs D., Sulman E. P., Maris J. M., Biegel J. A., Wooster R., Brodeur G. M. Physical mapping of the CA6, ENO1 and SLC2A5 (GLUT5) genes and reassignment of SLC2A5 to 1p36.2. Cytogenet Cell Genet 1998;81:60-64[Medline]

35. Wright E. M. The intestinal Na⁺/glucose cotransporter. Ann. Rev. Physiol. 1993;55:575-589[Medline]

36. Yamauchi K., Kamisoyama H., Isshiki Y. Effect of fasting and refeeding on structures of the intestinal villi and epithelial cells in White Leghorn hens. Br. Poult. Sci. 1996;37:909-921[Medline]

37. Zhao F. Q., Okine E. K., Cheeseman C.I., Shirazi-Beechey S. P., Kennelly J. J. Glucose transporter gene expression in lactating bovine gastrointestinal tract. J. Anim. Sci. 1998;76:2921-2929[Abstract/Free Full Text]

This article has been cited by other articles:

				E. R. Gilbert, H. Li, D. A. Emmerson, K. E. Webb Jr, and E. A. Wong Dietary Protein Quality and Feed Restriction Influence Abundance of Nutrient Transporter mRNA in the Small Intestine of Broiler Chicks J. Nutr., February 1, 2008; 138(2): 262 - 271. [Abstract] [Full Text] [PDF]

				E. R. Gilbert, H. Li, D. A. Emmerson, K. E. Webb Jr., and E. A. Wong Developmental Regulation of Nutrient Transporter and Enzyme mRNA Abundance in the Small Intestine of Broilers Poult. Sci., August 1, 2007; 86(8): 1739 - 1753. [Abstract] [Full Text] [PDF]

				A. Smirnov, R. Perez, E. Amit-Romach, D. Sklan, and Z. Uni Mucin Dynamics and Microbial Populations in Chicken Small Intestine Are Changed by Dietary Probiotic and Antibiotic Growth Promoter Supplementation J. Nutr., February 1, 2005; 135(2): 187 - 192. [Abstract] [Full Text] [PDF]

				A. Smirnov, D. Sklan, and Z. Uni Mucin Dynamics in the Chick Small Intestine Are Altered by Starvation J. Nutr., April 1, 2004; 134(4): 736 - 742. [Abstract] [Full Text] [PDF]

				G. Gabel and J. R. Aschenbach Influence of food deprivation on the transport of 3-O-methyl-{alpha}-D-glucose across the isolated ruminal epithelium of sheep J Anim Sci, October 1, 2002; 80(10): 2740 - 2746. [Abstract] [Full Text] [PDF]

				A. Barfull, C. Garriga, A. Tauler, and J. M. Planas Regulation of SGLT1 expression in response to Na+ intake Am J Physiol Regulatory Integrative Comp Physiol, March 1, 2002; 282(3): R738 - R743. [Abstract] [Full Text] [PDF]

				A. Barfull, C. Garriga, M. Mitjans, and J. M. Planas Ontogenetic expression and regulation of Na+-D-glucose cotransporter in jejunum of domestic chicken Am J Physiol Gastrointest Liver Physiol, March 1, 2002; 282(3): G559 - G564. [Abstract] [Full Text] [PDF]

This Article Abstract Full Text (PDF) Purchase Article View Shopping Cart Alert me when this article is cited Alert me if a correction is posted Services Similar articles in this journal Similar articles in PubMed Alert me to new issues of the journal Download to citation manager Citing Articles Citing Articles via HighWire Citing Articles via Google Scholar Google Scholar Articles by Gal-Garber, O. Articles by Uni, Z. Search for Related Content PubMed PubMed Citation Articles by Gal-Garber, O. Articles by Uni, Z.