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© 2004 The American Society for Nutritional Sciences J. Nutr. 134:2173-2177, September 2004

Biochemical and Molecular Actions of Nutrients

ATB0/ASCT2 Expression in Residual Rabbit Bowel Is Decreased after Massive Enterectomy and Is Restored by Growth Hormone Treatment1,2

Nelly E. Avissar3, Thomas R. Ziegler*, Liana Toia, Liang Gu*, Edward C. Ray, Jorge Berlanga-Acosta{dagger} and Harry C. Sax

Department of Surgery, University of Rochester Medical Center, Rochester, NY; * Department of Medicine, Emory University School of Medicine, Atlanta, GA; and {dagger} Center for Genetic Engineering and Biotechnology (CIGB), Havana, Cuba

3To whom correspondence should be addressed. E-mail: nelly_avissar{at}urmc.rochester.edu.


   ABSTRACT
TOP
 ABSTRACT
MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 LITERATURE CITED
 
Two weeks after 70% enterectomy, glutamine (Gln) transport is downregulated in rabbit residual bowel due to a decrease in system B0 activity. Providing epidermal growth factor (EGF) and growth hormone (GH) restores Gln transport by increasing systems A and B0,+ activities. We hypothesized that changes in Na+-dependent broad-spectrum neutral amino acid transporter (ATB0/ASCT2) protein and mRNA expression correlate with system B0 activity. New Zealand White rabbits underwent 70% jejunoileal resection or no resection. Resected rabbits immediately received parenteral EGF, GH, both, or neither agent for 2 wk. Tissues harvested from jejunum, ileum, and colon were subjected to Western and Northern blot analyses for ATB0/ASCT2 protein and mRNA. In all tissues, ATB0/ASCT2 mRNA was reduced by ~50% in resected rabbits compared with nonresected controls. Similar reductions in protein amount occurred in the ileum and cecum. None of the growth factor treatments restored ATB0/ASCT2 protein, but GH treatment increased ATB0/ASCT2 mRNA abundance 250% in the residual ileum. Because changes in the ATB0/ASCT2 protein amount paralleled those in the system B0 activity in this model, it is likely that this is the protein responsible for this transport system. The increase in mRNA abundance in rabbits treated with GH for 2 wk may be a harbinger of subsequent increases in transporter protein and activity. Unlike reported upregulation of transporters in human colon after small bowel resection, ATB0/ASCT2 protein and mRNA expression in rabbit colon are decreased, suggesting different regulatory pathways.

KEY WORDS: • small bowel resection • ATB0/ASCT2 • rabbits • epidermal growth factor • growth hormone

Short bowel syndrome (SBS)4 is a devastating condition leading to dehydration, malnutrition, and metabolic anomalies. After resection, the residual intestine adapts both morphologically and physiologically, but this does not always adequately compensate for the loss of absorptive capacity (1). This leads to dependence on total parenteral nutrition, a modality with significant morbidity, mortality, and expense. Our laboratory has had a long-term interest in accelerating adaptation and improving nutrient transport.

Because Gln is the main oxidative fuel of the enterocyte and becomes conditionally essential after several kinds of stress (2), we focused our studies on Gln transport in models of SBS. Luminal Gln enters the enterocyte primarily via Na+-dependent neutral amino acid transporters (3). System B0, the major brush border membrane (BBM) Gln transporter, is a broad-spectrum neutral amino acid transporter. A cDNA that confers system B0 activity in oocytes and mammalian cell lines was cloned and designated ATB0/ASCT2. ATB0/ASCT2 belongs to the ASC family of transporters, which also includes narrower-spectrum neutral amino acid transporters such as ASCT1 (3–7). It is unclear whether the ATB0 protein is responsible for system B0 transport because it has not yet been determined whether ATB0/ASCT2 participates in nonobligatory exchange transport, whereas it is known that system B0 can (8). In addition, there may be other transporters that contribute to this activity. For simplicity, we refer to ATB0/ASCT2 as ATB0 protein and message in this manuscript. Other Gln transporters include system B0,+, which transports both neutral and basic amino acids (3,5,9) and the ubiquitous system A, which is present in many tissues, but is localized primarily on the enterocyte basolateral membrane (3,5).

We showed that operative stress transiently increases Gln transport 1 wk after surgery. However, resected rabbits upregulate far less than controls with transection only (61 vs. 130%) (10). By 2 wk, Gln transport after resection is decreased by 50% compared with nonresected rabbits (11). This persists for at least 1 mo, with activity returning to preresection levels by 3 mo (12). The decrease in Gln transport is due mainly to a 50% decrease in system B0 activity (11), which is accompanied by a decrease in ATB0 mRNA (13). Parenteral growth hormone (GH) plus epidermal growth factor (EGF), started 1 wk after resection and given for a week, increased Gln transport in residual jejunum (14) but did not increase ATB0 mRNA (13). The same treatment, given immediately after resection and continued for 2 wk, reversed the decrease in Gln transport in both jejunum and ileum (11). Competitive inhibition studies suggested that this change was due to increased systems B0,+ and A activities (11). In human colon, PEPT1 and ATB0,+ mRNAs and proteins increased after small bowel resection (15,16). We hypothesized that ATB0 protein and mRNA expression is correlated with system B0 activity in small intestine after resection and growth factor (GF) treatment. We also anticipated a compensatory increase in ATB0 in the colon after enterectomy, as seen for PEPT1 and ATB0,+. We produced and characterized specific antibodies to rabbit ATB0 protein (17) and used them to determine ATB0 protein amount in nonresected and in resected and GF-treated rabbits. Message abundance was quantified using a rabbit ATB0 clone (18).


   MATERIALS AND METHODS
TOP
 ABSTRACT
 MATERIALS AND METHODS
RESULTS
 DISCUSSION
 LITERATURE CITED
 
    Reagents, chemicals and diet. EGF was a gift from the Center for Genetic Engineering and Biotechnology (CIGB). GH (Nutropin) was a gift from Genentech. SuperSignal was purchased from Pierce Chemical. Polyclonal goat anti rabbit ATB0 antibodies were custom produced by Quality Controled Biochemicals (BioSource International) and characterized as described before (17). QuikHyb hybridization solution was from Strategene. At present, there are no commercially available antibodies and probes against system B0,+ (ATB0,+) or A (ATA2). Rabbits were fed a commercial diet [PMI Nutrition International LabDiet 5P26 (15.6 kJ/g)]. The diet included 150 g protein, 20 g fat, and 180 g fiber/kg.

    Rabbits and operations. All experimental procedures and protocols were approved by the University of Rochester Institutional Animal Care and Use Committee (IACUC). Eighteen hours before surgical interventions, food was removed, but the rabbits had free access to a 50 g/L glucose solution. Male New Zealand White Rabbits (2 ± 0.2 kg) underwent 70% midgut resection (RC) (12,14) and were randomly assigned to receive immediately EGF, GH, both, or neither. A second nonresected group (nRC) served as additional controls. Four rabbits per group were analyzed. EGF in 30 g/L albumin or 30 g/L albumin alone were delivered at 5µL/h by a subcutaneous Alzet osmotic pump (Durect) providing 1.5 µg/(kg · h) EGF (14). GH or saline was administered once daily by i.m. injection [0.2 mg/(kg · d)].

    Tissue harvest. Two weeks after surgery, whole tissues from the remnant small bowel (divided into jejunal and ileal segments), cecum, and ascending colon were harvested and the rabbits were killed by exsanguination (14). For Western blot analysis, the small bowel, cecal mucosa, and whole colon tissue were immediately frozen in liquid nitrogen. For Northern blot analysis, whole tissues were placed into Tri Reagent and immediately frozen.

    Preparation of tissues for Western blot analysis. Crude cleared tissue extracts were prepared by sonication in a modified RIPA buffer with protease and phosphatase inhibitors as described previously (17), but with the addition of Sigma protease inhibitor cocktail (diluted 1:10). Protein concentration was determined using the method of Lowery (19). Despite the presence of excess anti-protease cocktails, jejunal and colon samples from the GF-treated rabbits were found to be degraded and were not further analyzed.

    Western blot analysis. Western blot analysis was performed on 160 µg extract per lane (20) as previously described (17). All samples from a specific tissue of RC and nRC rabbits were analyzed on one gel. The same is true for all samples from untreated resected and resected and GF-treated rabbits. To verify the identity of the transporter band, membranes were incubated with the primary antibody in the presence of 20-fold molar excess of the corresponding rabbit ATB0 peptide (data not shown). All blots were stripped and reprobed with antibody against ß-actin at a ratio of 1:100,000 of both primary and secondary antibodies to control for loading.

    RNA extraction. Full-thickness intestinal segments in Tri-Reagent were homogenized for 20–30 s using a Polytron (Brinkman Instruments). Total RNA was extracted according to the Tri-Reagent protocol (version TB87: 12/89; rev: 8/90). Final RNA concentration was determined by absorption spectrophotometry at 260 nm, and the samples were stored at –70°C.

    Northern blot analysis for rabbit ATB0. Denatured RNA (25 µg) was resolved by electrophoresis in agarose-formaldehyde gels, transferred to nylon filters (Duralon-UV Membranes, Strategene) and fixed by UV light. Samples from a specific tissue from all RC and nRC or from resected and GF-treated rabbits were run on one gel. Hybridization and washings were performed in QuikHyb hybridization solution according to the manufacturer’s manual (Strategene) with the following cDNAs. The rabbit ATB0 cDNA was a 850-bp (nucleotides 1148–1999) PstI fragment of the full-length rabbit ATB0 cDNA subcloned into the Pst1 site of pSPORT (kindly provided by Dr. V. Ganapathy, Medical College of Georgia, Augusta, GA, GenBank access # U75284). Human ß-actin cDNAs were 1.2- and 1.9-kb fragments, purified from commercially purchased plasmids (American Type Culture Collection). Only nonsaturated signals falling within the linear range were used for quantification. To verify equal RNA loading and to determine the specificity of ATB0 mRNA expression, all filters were stripped and sequentially rehybridized with a human ß-actin probe. RNA integrity and equal loading of all samples were also confirmed by analysis of ethidium bromide-stained 28S and 18S ribosomal RNA bands in 10 g/L agarose gels (data not shown).

    Statistical analysis. Results are reported as means ± SEM with significant differences (P < 0.05) determined by one-way ANOVA with Newman-Keuls post-test (resected and resected plus GF-treated rabbits). Student’s t test was used to compare the untreated RC group and the nRC group. The GraphPad Prism statistical software package was used for all analyses.


   RESULTS
TOP
 ABSTRACT
 MATERIALS AND METHODS
 RESULTS
DISCUSSION
 LITERATURE CITED
 
Compared with the actin band, the ATB0 protein band decreased in the residual ileum of RC vs. nRC rabbits (Fig. 1A). Resection induced a 50% decrease in ATB0 protein level in ileum and cecum (P < 0.03) (Fig. 1B).



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  		FIGURE 1 Western blot analysis of ATB0 protein in bowel of rabbits that underwent 70% jejunoileal resection (RC) or no resection (nRC). (A) Representative blots from ileum. (B) Quantification of data. For each tissue, the nRC mean was set at 100%. Values are means ± SEM, n = 4. *Different from nRC, P < 0.03.

 
Similar to the lack of change in system B0 activity in the ileum (11,14), treatment with GF for 2 wk did not alter ATB0 protein in residual ileum or cecum (Fig. 2). It appears that under all conditions studied, ATB0 protein levels parallel system B0 activity.



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  		FIGURE 2 Western blot analysis of ATB0 protein in bowel of rabbits undergoing 70% jejunoileal resection (RC) with 2 wk of GF treatment. For each tissue, the RC mean was set at 100%. Values are means ± SEM, n = 4.

 
Two weeks after resection, ATB0 mRNA in all 3 tissues was significantly decreased in RC compared with nRC rabbits (P < 0.04) (Fig. 3).



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  		FIGURE 3 Northern blot analysis of ATB0 protein in bowel of rabbits that underwent 70% jejunoileal resection (RC) or no resection (nRC). (A) Representative blots from ileum. (B) Quantification of data. For each tissue, the nRC mean was set at 100%. Values are means ± SEM, n = 4. *Different from nRC, P < 0.04.

 
After an immediate 2-wk course of GF treatment, ATB0 mRNA abundance was significantly increased in the ileum of GH-treated rabbits (P < 0.05) (Fig. 4). EGF alone or in combination with GH did not affect any other tissue (Fig. 4).



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  		FIGURE 4 Northern blot analysis of ATB0 protein in bowel of rabbits that underwent 70% jejunoileal resection (RC) with 2 wk of GF treatment. For each tissue, the RC mean was set at 100%. Values are means ± SEM, n = 4. *Different from RC and EGF + GH, P < 0.05.

 

   DISCUSSION
TOP
 ABSTRACT
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
LITERATURE CITED
 
To avoid the devastating sequelae of SBS, the residual bowel must adapt to increase nutrient and fluid uptake, allowing volitional oral support. Counterintuitively, in our rabbit model and in other species, nutrient transport is reduced during mo 1 after resection (11,12,21–23). Administration of GFs, singly or in combination, during the initial period postresection helps overcome this absorptive deficiency of the residual gut (1,2,11,14,24–26). Identifying transporters that are downregulated with resection and differentially upregulated with specific GF treatments enhances our understanding of the mechanisms involved and can lead to novel therapies to reduce morbidity and mortality associated with SBS. We concentrated our studies on Gln transport because it is a major oxidative fuel of the enterocyte and becomes conditionally essential after several kinds of stress (2). In addition, Gln has trophic and cytoprotective effects on the small bowel (27).

The major Gln transporter on the apical membrane is the Na+-dependent, broad-spectrum neutral amino acid transport system B0 (11,28,29). We found previously that a decrease in this system’s activity is responsible for the 50% decrease in Gln transport after massive enterectomy in rabbits. However, it is not the system upregulated by 2 wk of treatment with GFs (11), suggesting differential signaling. The current study shows that changes in ATB0 mRNA and protein parallel changes in system B0 activity. ATB0 has transport properties similar to those of system B0 when expressed in heterologous systems (6,18,30), and its tissue and intracellular distributions parallel those of system B0. It is expressed only on the apical membrane of the enterocyte and the proximal tubular cell of the kidney and is enriched in the BBM vesicles of rabbit intestine. There is a gradient along the rabbit small and large intestine, i.e., ATB0 expression is lowest in the duodenum and highest in the colon (13,17). However, the transport characteristics of ATB0 are not identical to those of classical system B0 because it has not yet been determined whether ATB0 participates in nonobligatory exchange transport (8). The parallel changes in the amount of protein with that of the activity are additional indicators that ATB0 protein might be responsible for system B0 activity. Conclusive evidence could also be generated with antisense or immunodepletion techniques, which to our knowledge, has not been done.

At 2 wk after resection, Gln transport was increased in the residual intestine with a delayed 1-wk or an immediate 2-wk combination of EGF plus GH (11,14). This increase was due to augmentation in systems B0,+ and A (11). There is a nutritional advantage to an immediate increase in these 2 systems. System A is a highly regulated system and system B0,+ is a broader-spectrum transporter, including neutral, basic, and D-amino acids; it has a higher concentrative capacity than system B0. However, adaptation to achieve more normal gut function implies that the total amount and distribution of transporters in the residual bowel should be similar to those before surgery. We showed previously that a delayed 1-wk treatment with GH did not change the abundance of ATB0 mRNA in the residual gut (13). However, an immediate and a longer 2-wk course of GH increased it 250% in the ileum (Fig. 4). This suggests that protein and B0 activity will be increased later in response to increased ATB0 message. This is consistent with human studies in which a 21-d infusion of GH was used (31–34). We have not yet conducted longer-term infusion studies. The inhibition of the GH-induced increase in ATB0 mRNA by EGF in the ileum (Fig. 4) is in contrast to the enhanced system A and B0,+ activities that occurred with the combination of these 2 GFs. This might indicate that each transporter is differentially regulated by various GFs. Because jejunum and colon do not respond in the same way as the ileum, there may be segment-specific responses to the GFs.

The regulation of ATB0 message with resection and treatment with GFs is not a generalized process for the regulation of transporters. ATB0 mRNA was reduced with resection in both the small and large intestine (Fig 3), whereas PEPT1 mRNA is reduced with resection in the small intestine and increased in the large intestine in humans (13,15). In addition, ATB0,+ mRNA and protein are increased in the human colon after small bowel resection (16). In rabbits, the large intestine does not compensate for the resection-induced deficiency of ATB0 in the small intestine as it does in humans for PEPT1 and ATB0,+. Part of this may be explained by diet because rabbits are herbivores with significant colonic fermentation and humans are omnivores. Treatment of resected rabbits with the GFs also does not increase ATB0 protein or mRNA in the large intestine.

In summary, massive enterectomy decreased ATB0 protein and mRNA steady-state amounts by at least 50% in the residual small bowel and colon of rabbits. EGF and/or GH therapy did not significantly change ATB0 protein level in ileum or cecum, but GH increased ATB0 mRNA abundance in the ileum, suggesting a subsequent possible future increase in the protein. Changes in ATB0 protein paralleled alternations previously demonstrated in small bowel BBM system B0 activity. Therefore, ATB0 may be responsible for in vivo system B0 activity.

In contrast to the increase in colonic PEPT1 and ATB0,+ message in humans, ATB0 protein and message expression in rabbit large intestine are decreased after massive enterectomy. Identifying the transporters altered by resection and by GF treatment will enhance our understanding of the mechanisms of adaptation and provide guidelines for the development of novel therapeutic interventions in SBS.


   FOOTNOTES
 
1 Presented in part at the 104th Annual Meeting of the American Gastroenterological Association, May 17–23, 2003, Orlando, FL [Avissar, N. E., Toia, L., Ray, E. C., Vukcevic, D., Berlanga-Acosta, J. & Sax, H. C. (2003) ATB0/ASCT2 protein expression. Gastroenterology 124 (suppl.): A798 (abs.)], and at the 105th Annual Meeting of the American Gastroenterological Association, May 15–20, 2004, New Orleans, LA [Avissar, N. E., Ziegler, T. R., Gu, L. H., Toia, L., Ray, E. C., Berlanga-Acosta, J. & Sax, H. C. (2004) ATB0/ASCT2 mRNA in residual bowel is decreased by massive enterectomy and increased by trophic factor (TF) treatment. Gastroenterology 126 (suppl.): A784 (abs.)]. Back

2 Supported by National Institutes of Health grants R01-DK47989–08 (to H.C.S.) and RO1-DK55850 (to T.R.Z.). Back

4 Abbreviations used: ATB0/ASCT2, Na+-dependent broad-spectrum neutral amino acid transporter; BBM, brush border membrane; EGF, epidermal growth factor; GF, growth factor; GH, growth hormone; nRC, nonresected controls; PEPT1, oligopeptide transporter 1; RC, resected controls; SBS, short bowel syndrome. Back

Manuscript received 9 April 2004. Initial review completed 11 May 2004. Revision accepted 15 June 2004.


   LITERATURE CITED
TOP
 ABSTRACT
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 LITERATURE CITED
 

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Right arrow Articles by Avissar, N. E.
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