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Proceedings of the Society for Experimental Biology and Medicine 223:270-275 (2000)
© 2000 Society for Experimental Biology and Medicine

Original Article

Peptide YY Stimulates the Expression of Apolipoprotein A-IV Gene in Caco-2 Intestinal Cells

Kei Sonoyama1,, Keiko Suzuki and Takanori Kasai


Laboratory of Food Biochemistry, Department of Bioscience and Chemistry, Faculty of Agriculture, Hokkaido University, Sapporo 060–8589, Japan


   Abstract
Top
 Abstract
Introduction
 Materials and Methods
 Results
 Discussion
 References
 
The effect of peptide YY, a gastrointestinal hormone, on the expression of the apolipoprotein A-IV gene in the intestinal epithelial cell line Caco-2 was examined by semiquantitative RT-PCR followed by Southern hybridization with an inner oligonucleotide probe. Apolipoprotein A-IV mRNA levels were increased in response to peptide YY in a dose- and time-dependent fashion. Western blotting revealed that the exogenous peptide YY increased the intracellular concentration of apolipoprotein A-IV. In contrast, apolipoprotein A-I, B, and C-III mRNA did not respond to peptide YY. Differentiated Caco-2 cells expressed Y1- but not Y2- and Y5-receptor subtype mRNA. The present results suggest that peptide YY modulates apolipoprotein A-IV gene expression, likely via the Y1-receptor subtype in intestinal epithelial cells.


   Introduction
Top
 Abstract
 Introduction
Materials and Methods
 Results
 Discussion
 References
 
Apolipoprotein (apo) A-IV is a component of triglyceride (TG)-rich lipoproteins mainly synthesized by enterocytes in the small intestine (1). Although the precise function of the apo A-IV gene is not known, it has been shown to modulate lipoprotein metabolism (2-6), food intake (7, 8), and gastric functions (9, 10). For this reason, information on the expression of apo A-IV in the small intestine should lead to a better understanding of the regulation of lipoprotein metabolism, feeding behavior, and gastric functions.

We previously reported that massive small bowel resection resulted in a rapid increase in apo A-IV mRNA levels in the remnant ileum of fasted rats (11-13). In addition, plasma apo A-IV concentrations following small bowel resection were transiently decreased initially before recovering to control levels (11). These observations suggest that enterocytes in the residual ileum respond to the loss of proximal intestine by a compensatory increase in apo A-IV gene expression. However, the mechanism for the upregulation of the apo A-IV gene following small bowel resection remains unclear.

Peptide YY (PYY) is a gastrointestinal hormone synthesized in L-cells in the distal bowel (14, 15), and PYY mRNA expression in the residual ileum and plasma PYY concentrations have been reported to be elevated following massive small bowel resection in the rat (16-18). Therefore, we speculated that PYY may be associated with the upregulation of the apo A-IV gene following small bowel resection (11). To test this hypothesis, the present study investigated the effect of exogenous PYY on the expression of apo A-IV mRNA in the human colon adenocarcinoma cell line Caco-2. A number of studies have reported that Caco-2 cells differentiate after reaching confluence to form an epithelium that shares many characteristics with mature small intestinal mucosa in vivo and provides an excellent in vitro model for the investigation of intestinal apolipoprotein synthesis, lipoprotein secretion, and metabolism (19, 20).


   Materials and Methods
Top
 Abstract
 Introduction
 Materials and Methods
Results
 Discussion
 References
 
Cell Culture.
Caco-2 cells at passage 18 were obtained from the American Type Culture Collection. Cells were maintained in Falcon 75-cm2 T-flasks (Nippon Becton Dickinson, Tokyo, Japan) in a standard culture medium at 37°C in a humidified atmosphere of 5% CO2 and 95% air. The standard culture medium contained Dulbecco's modified Eagle's medium supplemented with 20% fetal bovine serum, 4 mM L-glutamine, 25 mM glucose, 1X nonessential amino acids (from 100X liquid, GIBCO-BRL, Tokyo, Japan), 100,000 U/l penicillin, 100 mg/l streptomycin, and 50 mg/l gentamycin. Media were replaced every 2 days or every day, depending on harvest times and degree of confluence. For experiments, subconfluent cells were plated onto Falcon 23.4-mm cell-culture inserts (pore size: 0.45 µm, Nippon Becton Dickinson) in six-well plastic plates at initial densities of 0.5 x 106 cells/well in standard medium. To test the effects of different concentrations of PYY on the expression of apolipoprotein genes in Caco-2 cells, the standard medium supplemented with 0, 1, 20, 50, 100, and 500 nM PYY (purified from human colon, purity > 96%, BACHEM AG, Budendorf, Switzerland) was supplied to the basolateral side of the monolayers at 10–14 days postconfluence. The cells were grown under the above conditions for an additional 12 hr and then harvested. To observe the time course of apolipoprotein and PYY receptor mRNA levels and apolipoprotein concentrations after addition of PYY in Caco-2 cells, the standard medium supplemented with 100 nM PYY was supplied to the basolateral side of the monolayers at 10–14 days postconfluence. The cells were cultured for 3, 6, 12, 24, and 72 hr and then harvested. Cells in the control wells were harvested prior to supplementation of PYY (0 time).

Extraction and Analysis of RNA.
After washing with phosphate-buffered saline (PBS), the cell monolayers were added to a 1 ml/well Isogen (Nippon Gene, Tokyo, Japan), a reagent for RNA isolation, gently scraped with a plastic blade, and then transferred to a microcentrifuge tube. Thereafter, total RNA was isolated according to the manufacturer's protocol.

The steady-state levels of mRNA were semiquantitatively determined by reverse transcription polymerase chain reaction (RT-PCR) followed by Southern hybridization with an inner oligonucleotide probe. The total RNA samples were treated with DNase RQ1 (Promega, WI) to remove genomic DNA. Next, 5 µg of total RNA was annealed with 0.5 µg of oligo (dT) primer (GIBCO-BRL) at 70°C for 10 min, and first strand cDNA was then synthesized in a 20-µl solution containing 50 mM Tris-HCl pH 8.3, 75 mM KCl, 3 mM MgCl2, 10 mM dithiothreitol (DTT), 0.5 mM dNTP, 25 U of RNase inhibitor, and 200 U of MMLV RTase (GIBCO-BRL) at 42°C for 50 min, followed by RNA digestion with RNase H (GIBCO-BRL). The first strand cDNA sample (0.5 µl) was added to 50 µl of a PCR reaction mixture containing 0.5 µM gene-specific primers (Table I)Go, 2 mM MgCl2, 0.2 mM dNTP, and 1.25 U of EX-Taq polymerase (Takara, Otsu, Japan). Each cycle of PCR included 1 min of denaturation at 94°C, 1 min of primer annealing at different temperatures for each primer pair, and 2 min of extension at 72°C. The single band was detected by 2% agarose gel electrophoresis of PCR products, and the size of each product was consistent with the predicted size (data not shown). For each combination of primers the kinetics of amplification was studied in preliminary experiments, and PCR was performed within an exponential range. The PCR products separated on 2% agarose gel electrophoresis were transferred to a nylon membrane (Biodyne Plus, Pall, NY), and the blots were hybridized with each inner oligonucleotide probe (Table I)Go labeled with digoxigenin using a DIG oligonucleotide tailing kit (Boehringer Mannheim, Mannheim, Germany). Prehybridization, hybridization, and detection were carried out with a DIG luminescence detection kit (Boehringer Mannheim). The hybridization was performed at 42°C overnight, and posthybridization washing was performed with 0.1 X standard saline citrate (SSC), 0.1% sodium dodecyl sulfate (SDS) at 60°C three times for 15 min each wash. The bands developed on x-ray film were quantitated using NIH Image. The signal intensity of each apolipoprotein relative to that of glyceraldehyde-3-phosphate dehydrogenase (GAPDH), which was used as an internal control of PCR, was expressed as relative intensity. The results shown in Figures 1, 2, and 3GoGoGo are from a representative experiment. The experiment was repeated three times, and similar results were obtained.


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  		Table I.   Oligonucleotide Primers Used for RT-PCR and Inner Oligonucleotide Probes Used for Southern Hybridization of RT-PCR Products
 


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  		Figure 1.   Effect of graded concentrations of PYY on mRNA expression of apolipoproteins in Caco-2 cells. Total RNA was isolated from Caco-2 cells cultured with or without PYY for 12 hr and subjected to semiquantitative RT-PCR followed by Southern hybridization with each inner oligonucleotide probe. The inset illustrates the representative Southern blots of RT-PCR products. GAPDH was used as the internal control for PCR. The signal intensity of each apolipoprotein relative to that of GAPDH is expressed as relative intensity, and the values on each point are expressed relative to values without PYY that are taken as 100. The results shown are from a representative experiment. The experiment was repeated three times, and similar results were obtained.

 


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  		Figure 2.   Time course of changes in mRNA levels of apolipoproteins in Caco-2 cells after supplementation of PYY. Total RNA was isolated from Caco-2 cells cultured with 100 nM of PYY for 0, 3, 6, 12, 24, and 72 hr and analyzed as described in Figure 1Go. The inset illustrates the representative Southern blots of RT-PCR products. The signal intensity of each apolipoprotein relative to that of GAPDH is expressed as relative intensity, and the values on each time point are expressed relative to values of 0 time, which are taken as 100. The results shown are from a representative experiment. The experiment was repeated three times, and similar results were obtained.

 


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  		Figure 3.   Time course of changes in relative concentrations of apolipoproteins in Caco-2 cells after supplementation of PYY. Cells were lyzed at 0, 3, 6, 12, 24, and 72 hr after adding 100 nM of PYY, and the cell lysates were subjected to Western blot analysis. The inset illustrates the representative Western blots. The values on each time point are expressed relative to values of 0 time, which are taken as 100. The results shown are from a representative experiment. The experiment was repeated three times, and similar results were obtained.

 
Western Blot Analysis.
After washing with PBS, the cell monolayers were added to 1 ml/well of cell lysis buffer composed of 10 mM Tris-HCl pH 7.4, 150 mM NaCl, 1 mM EDTA, 10 µg/ml aprotinin, and 0.5% NP40, and incubated for 30 min on ice. The cell lysate was centrifuged (12,000g) for 20 min at 4°C, and a part of the supernatant (20 µg total protein) was subjected to 7.5% SDS-PAGE under reducing conditions. Electrophoresed proteins were electrophoretically transferred to a nitrocellulose membrane (Hybond C extra, Amersham International plc., Buckinghamshire, U.K.) and immunostained with the antihuman apo A-IV monoclonal antibody (Boehringer Mannheim) or the Sheep antihuman apo A-I serum (The Binding Site Ltd., Birmingham, UK) as previously described (11). The relative quantities of apo A-IV and apo A-I were estimated by using NIH Image.


   Results
Top
 Abstract
 Introduction
 Materials and Methods
 Results
Discussion
 References
 
Figure 1Go shows the results of Southern hybridization analysis of semiquantitative RT-PCR products for apolipoproteins in Caco-2 cells cultured for 12 hr with or without exogenous PYY. Apo A-IV mRNA levels progressively increased in response to the graded concentrations of PYY. In contrast, no changes in apo A-I, B, C-III, or GAPDH mRNA levels were observed. The time-course experiment demonstrated that apo A-IV mRNA began to increase at 3 hr following the addition of 100 nM of PYY, reaching a maximum value by 6 hr (Fig. 2)Go. Although apo A-IV mRNA levels decreased somewhat 24 hr following the addition of PYY, they recovered to maximum levels at 72 hr. In contrast, mRNA encoding of other apolipoproteins or of GAPDH showed no change during the culture period following supplementation of PYY. Similarly, cellular concentrations of apo A-IV protein began to increase at 6 hr, whereas apo A-I protein concentrations were relatively constant throughout the culture period (Fig. 3)Go.

The major apolipoproteins reported to have been expressed in the enterocytes of the small intestine include apo A-I, A-IV, and B48 (21-24). In the present study, semiquantitative RT-PCR followed by Southern hybridization demonstrated that Caco-2 cells expressed mRNA that encoded the above apolipoproteins, suggesting that the cells showed an enterocyte-like phenotype when under experimental conditions like those used in the present study. In addition, apo A-I, C-III, and A-IV are reportedly encoded in a gene cluster localized in human chromosome 11 (11q23-qter) (25), and the present study detected apo C-III mRNA in Caco-2 cells. Among the apolipoproteins mentioned previously, apo A-IV was clearly shown to be the only one whose mRNA levels increased as a result of exogenous PYY in a dose- and time-dependent fashion, suggesting the specific upregulation of the apo A-IV gene by the gastrointestinal hormone PYY. Additionally, the increase in cellular concentrations of apo A-IV protein after adding the PYY suggests that exogenous PYY stimulates apo A-IV synthesis at pretranslational levels in Caco-2 cells. As the PYY release from enteroendocrine cells in the distal bowel has been shown to be stimulated by dietary fat (26-28), the PYY modulation of apo A-IV gene expression may, at least in part, explain the stimulation of intestinal apo A-IV gene expression by dietary fat (29).


   Discussion
Top
 Abstract
 Introduction
 Materials and Methods
 Results
 Discussion
References
 
We previously demonstrated that massive small bowel resection led to a rapid increase in apo A-IV mRNA levels in the remnant ileum of the rat (11-13). Given that PYY mRNA levels in the residual ileum and the plasma PYY concentrations were reported to be elevated following massive small bowel resection (16-18), we suspected the involvement of PYY in the postresectional increase in apo A-IV gene expression in the residual ileum. The present results suggest that increased concentrations of plasma PYY following small bowel resection may, at least in part, contribute to the upregulation of the apo A-IV gene in the residual ileum.

Halldén and Aponte (30) demonstrated that the expression of the intestinal fatty acid binding protein (I-FABP) gene was stimulated by 100 nM of PYY in the small intestinal somatic cell hybrids (hBRIE 380i cells). Additionally, I-FABP was shown to be a cytosolic protein abundantly expressed in enterocytes (31), which are involved in the intracellular trafficking and/or metabolism of free fatty acids (FFAs) in the enterocytes (32). The synthesis of I-FABP in enterocytes has been shown to be stimulated by a high-fat diet (33). Furthermore, Rubin et al. (34) reported that, as with apo A-IV mRNA, I-FABP mRNA was increased in the residual ileum following massive small bowel resection in the rat. Given the above findings, it was believed that under conditions of increased availability of intestinal fatty acids derived from diet and bile (e.g., a high-fat diet and small bowel resection), the increased concentrations of PYY would induce both I-FABP and apo A-IV, and thus facilitate intracellular trafficking and/or metabolism of FFAs followed by assembly and/or secretion of TG-rich lipoproteins in the enterocytes.

A few potential limitations of the present study should be noted at this point. First, although Savage et al. (16) previously reported that the plasma concentrations of PYY were 28 and 85 pM in sham-operated and small bowel–resected rats, respectively, the increase in apo A-IV mRNA in Caco-2 cells was observed when PYY was added at concentrations of over 1 nM. Thus, Caco-2 cells likely require supraphysiological concentrations of PYY for the upregulation of the apo A-IV gene. One possible explanation for this problem is that there may be certain defects in the signal transduction pathway of PYY in Caco-2 cells. The present study investigated the gene expression of recently cloned Y1, Y2 and Y5 receptor subtypes that have similar affinity for PYY and neuropeptide Y (35). Southern hybridization of RT-PCR products indicated that mRNA for the Y1 receptor was detected in Caco-2 cells and transiently increased by 100 nM PYY (Fig. 4)Go. However, in the case of Y2 and Y5 receptor mRNA, no signal was detected even when the number of PCR cycles was increased to 40 (data not shown). These findings suggest that modulation of apo A-IV gene expression by PYY is likely through the Y1-receptor subtype in Caco-2 cells and that the Y1-receptor gene is upregulated by its putative ligand, PYY. However, it remains unclear whether the abundance, structure, and function of the receptor in Caco-2 cells are similar to those in the enterocyte in vivo. In addition, there is no information on the integrity of intracellular machinery for signal transduction of PYY in Caco-2 cells. Nevertheless, given the dose- and time-dependent increase in apo A-IV mRNA levels in the present study, it is likely that the upregulation of the apo A-IV gene in Caco-2 cells is a physiological response to PYY. Thus, further studies are necessary to clarify not only the molecular mechanisms underlying the regulation of the apo A-IV gene by PYY but also the integrity of signal transduction of PYY in Caco-2 cells.



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  		Figure 4.   Time-course of changes in mRNA levels of the PYY/Y1 receptor in Caco-2 cells after supplementation of 100 nM PYY. The same samples used in Figure 2Go were analyzed for Y1 receptor mRNA. The inset illustrates the representative Southern blots of RT-PCR products. The signal intensity of each apolipoprotein relative to that of GAPDH is expressed as relative intensity, and the values on each time point are expressed relative to values of 0 time, which are taken as 100. The results shown are from a representative experiment. The experiment was repeated three times, and similar results were obtained.

 
Secondly, although we demonstrated that exogenous PYY increased both mRNA and protein levels of apo A-IV in Caco-2 cells in the present study, Kalogeris et al. (36) recently reported that intravenous infusion of physiological doses of PYY resulted in a significant increase in the synthesis and lymphatic output of apo A-IV protein, with no corresponding changes in mRNA levels in the jejunum of rats. Similarly, we confirmed that intravenous infusion of PYY (1–100 pmole/kg hr for 8 hr) did not stimulate the apo A-IV gene in either the jejunum or ileum of rats (unpublished data). Although one may consider that lower concentrations of PYY can stimulate apo A-IV synthesis without increasing mRNA levels, our preliminary experiment showed that physiological concentrations of PYY (1–100 pM) could stimulate neither protein contents (analyzed by Western blotting) nor mRNA levels of apo A-IV in Caco-2 cells (unpublished data). Despite the lack of any experimental evidence to date to explain the above inconsistent observations, it is possible that there may be species-dependent differences in the PYY modulation of intestinal apo A-IV expression. Another possibility is that PYY stimulation of apo A-IV synthesis in vivo would be mediated by indirect mechanisms that may not be accompanied by the induction of mRNA expression. Thus, since inhibition of proximal gut function as part of the "ileal brake" by systemic PYY has been shown to be mediated by the vagus nerve (37), and since apo A-IV has been reported to share the "ileal brake" with PYY (9, 10), it is theoretically possible that PYY may stimulate apo A-IV synthesis via the vagus nerve. Therefore, it is of interest to investigate whether PYY stimulation of apo A-IV synthesis is diminished by blockade of the vagus nerve.

The present study findings taken as a whole demonstrated that the gastrointestinal hormone PYY specifically stimulated the expression of the apo A-IV gene in the human intestinal cell line Caco-2. The results suggest that PYY may play an important role in the regulation of apo A-IV gene expression, likely via the PYY/Y1 receptor in the enterocytes. This may, at least in part, explain the upregulation of apo A-IV expression in the residual ileum following massive small bowel resection.


   Acknowledgments
 
We are grateful to Dr. Gregory W. Aponte for helpful suggestions.


   Footnotes
 
This work was partly supported by Grant-in-Aid for Encouragement of Young Scientists from The Ministry of Education, Science, Sports and Culture of Japan, by the Nutritional Science Institute of Meiji Milk Products Co., and by Yamanouchi Pharmaceutical Co.

1 To whom requests for reprints should be addressed at Laboratory of Food Biochemistry, Faculty of Agriculture, Hokkaido University, Kita-9, Nishi-9, Sapporo 060–8589, Japan. E-mail: ksnym{at}chem.agr.hokudai.ac.jp Back


   References
Top
 Abstract
 Introduction
 Materials and Methods
 Results
 Discussion
 References
 

  1. Elshourbagy NA, Boguski MS, Liao WSL, Jefferson LS, Gordon JI, Taylor JM. Expression of rat apolipoprotein A-IV and A-I genes: mRNA induction during development and in response to glucocorticoids and insulin. Proc Natl Acad Sci U S A 82:8242–8246, 1985.[Abstract/Free Full Text]
  2. Chen CH, Albers JJ. Activation of lecithin: Cholesterol acyltransferase by apolipoproteins E-2, E-3, and A-IV isolated from human plasma. Biochim Biophys Acta 836:279–285, 1985.[Medline]
  3. Dvorin E, Gorder NL, Benson DM, Gotto Am Jr. Apolipoprotein A-IV: A determinant for binding and uptake of high density lipoproteins by rat hepatocytes. J Biol Chem 261:15714–15728, 1986.[Abstract/Free Full Text]
  4. Stein O, Stein Y, Lefevre M, Roheim PS. The role of apolipoprotein A-IV in reverse cholesterol transport studied with cultured cells and liposomes derived from an ether analog of phosphatidylcholine. Biochim Biophys Acta 878:7–13, 1986.[Medline]
  5. Steinmetz A, Utermann G. Activation of lecithin: Cholesterol acyltransferase by human apolipoprotein A-IV. J Biol Chem 260:2258–2264, 1985.[Abstract/Free Full Text]
  6. Steinmetz A, Barbaras R, Ghalim N, Clavey V, Fruchart JC, Ailhaud G. Human apolipoprotein A-IV binds to apolipoprotein A-I/A-II receptor sites and promotes cholesterol efflux from adipose cells. J Biol Chem 265:7859–7863, 1990.[Abstract/Free Full Text]
  7. Fujimoto K, Cardelli JA, Tso P. Increased apolipoprotein A-IV in rat mesenteric lymph after lipid meal acts as a physiological signal for satiation. Am J Physiol 262:G1002–G1006, 1992.[Abstract/Free Full Text]
  8. Fujimoto K, Fukagawa K, Sakata T, Tso P. Suppression of food intake by apolipoprotein A-IV is mediated through the central nervous system in rats. J Clin Invest 91:1830–1833, 1993.
  9. Okumura T, Fukagawa K, Tso P, Taylor IL, Pappas TN. Intracisternal injection of apolipoprotein A-IV inhibits gastric secretion in pylorus-ligated conscious rats. Gastroenterology 107:1861–1864, 1994.[Medline]
  10. Okumura T, Fukagawa K, Tso P, Taylor IL, Pappas TN, Uehara A, Kohgo Y. Delayed gastric emptying by central apolipoprotein A-IV in rats. Gastroenterology 108:A996, 1995.
  11. Sonoyama K, Kiriyama S, Niki R. Adaptive response of apolipoprotein A-I and A-IV mRNA in residual ileum after massive small bowel resection in rats. J Nutr Sci Vitaminol 41:253–264, 1995.
  12. Sonoyama K, Nakamura Y, Kiriyama S, Niki R. Upregulation of apolipoprotein A-IV gene expression in residual ileum after massive small bowel resection requires the biliary secretion in rats. Proc Soc Exp Biol Med 211:273–280, 1996.[Abstract]
  13. Sonoyama K, Aoyama Y. Different responses of apolipoprotein A-I, A-IV, and B gene expression during intestinal adaptation to a massive small bowel resection in rats. Biosci Biotechnol Biochem 61:1810–1813, 1997.[Medline]
  14. Ali-Rachedi A, Varndell IM, Adrian TE, Gapp DA, Van Noorden S, Bloom SR, Polak JM. Peptide YY (PYY) immunoreactivity is co-stored with glucagon-related immunoreactants in endocrine cells of the gut and pancreas. Histochemistry 80:487–491, 1984.[Medline]
  15. Bottcher G, Sjolund K, Ekblad E, Hakanson R, Schwartz TW, Sundler F. Coexistence of peptide YY and glicentin immunoreactivity in endocrine cells of the gut. Regul Pept 8:261–266, 1984.[Medline]
  16. Savage AP, Gornacz GE, Adrian TE, Ghatei MA, Goodlad RA, Wright NA, Bloom SR. Is raised plasma peptide YY after intestinal resection in the rat responsible for the trophic response? Gut 26:1353–1358, 1985.[Abstract/Free Full Text]
  17. Taylor RG, Beveridge DJ, Fuller PJ. Expression of ileal glucagon and peptide tyrosine-tyrosine genes: Response to inhibition of polyamine synthesis in the presence of massive small-bowel resection. Biochem J 286:737–741, 1992.
  18. Fuller PJ, Beveridge DJ, Taylor RG. Ileal proglucagon gene expression in the rat: Characterization in intestinal adaptation using in situ hybridization. Gastroenterology 104:459–466, 1993.[Medline]
  19. Gordon JI. Intestinal epithelial differentiation: New insights from chimeric and transgenic mice. J Cell Biol 108:1187–1194, 1989.[Free Full Text]
  20. Levy E, Mehran M, Seidman E. Caco-2 cells as a model for intestinal lipoprotein synthesis and secretion. FASEB J 9:626–635, 1995.[Abstract]
  21. Davidson NO, Magun AM, Brasitus TA, Glickman RM. Intestinal apolipoprotein A-I and B-48 metabolism: Effects of sustained alterations in dietary triglyceride and mucosal cholesterol flux. J Lipid Res 28:388–402, 1987.[Abstract]
  22. Fidge NH. The redistribution and metabolism of iodinated apolipoprotein A-IV in rats. Biochim Biophys Acta 619:129–141, 1980.[Medline]
  23. Hayashi H, Fujimoto K, Cardelli JA, Nutting DF, Bergstedt S, Tso P. Fat feeding increases size, but not number, of chylomicrons produced by small intestine. Am J Physiol 259:G709–G719, 1990.[Abstract/Free Full Text]
  24. Weinberg RB, Dantzker C, Patton CS. Sensitivity of serum apolipoprotein A-IV levels to changes in dietary fat content. Gastroenterology 98:17–24, 1990.[Medline]
  25. Karathanasis SK. Apolipoprotein multigene family: Tandem organization of human apolipoprotein AI, CIII, and AIV genes. Proc Natl Acad Sci U S A 82:6374–6378, 1985.[Abstract/Free Full Text]
  26. Pappas TN, Debas HT, Goto Y, Taylor IL. Peptide YY inhibits meal-stimulated pancreatic and gastric secretion. Am J Physiol 248:G118–G123, 1985.[Abstract/Free Full Text]
  27. Aponte GW, Fink AS, Meyer JH, Tatemoto K, Taylor IL. Regional distribution and release of peptide YY with fatty acids of different chain length. Am J Physiol 249:G745–G750, 1985.[Abstract/Free Full Text]
  28. Aponte GW, Park K, Hess R, Garcia R, Taylor IL. Meal-induced peptide tyrosine tyrosine inhibition of pancreatic secretion in the rat. FASEB J 3:1949–1955, 1989.[Abstract]
  29. Gordon JI, Smith DP, Alpers DH, Strauss AW. Cloning of a complementary deoxyribonucleic acid encoding a portion of rat intestinal preapolipoprotein AIV messenger ribonucleic acid. Biochemistry 21:5424–5431, 1982.[Medline]
  30. Halldén G, Aponte GW. Evidence for a role of the gut hormone PYY in the regulation of intestinal fatty acid-binding protein transcripts in differentiated subpopulations of intestinal epithelial cell hybrids. J Biol Chem 272:12591– 12600, 1997.[Abstract/Free Full Text]
  31. Gordon JI, Elshourbagy N, Lowe JB, Liao WS, Alpers DH, Taylor JM. Tissue-specific expression and developmental regulation of two genes coding for rat fatty acid binding proteins. J Biol Chem 260:1995–1998, 1985.[Abstract/Free Full Text]
  32. Hsu KT, Storch J. Fatty acid transfer from liver and intestinal fatty acid-binding proteins to membranes occurs by different mechanisms. J Biol Chem 271:13317– 13323, 1996.[Abstract/Free Full Text]
  33. Bass NM. The cellular fatty acid binding proteins: Aspects of structure, regulation, and function. Int Rev Cytol 111:143–184, 1988.[Medline]
  34. Rubin DC, Swietlicki EA, Wang JL, Dodson BD, Levin MS. Enterocytic gene expression in intestinal adaptation: Evidence for a specific cellular response. Am J Physiol 270:G143–G152, 1996.[Abstract/Free Full Text]
  35. Blomqvist AG, Herzog H. Y-receptor subtypes: How many more? Trends Neurosci 20:294–298, 1997.[Medline]
  36. Kalogeris TJ, Qin X, Chey WY, Tso P. PYY stimulates synthesis and secretion of intestinal apolipoprotein A-IV without affecting mRNA expression. Am J Physiol 275:G668–G674, 1998.[Abstract/Free Full Text]
  37. Chen CH, Rogers RC. Central inhibitory action of peptide YY on gastric motility in rats. Am J Physiol 269:R787–R792, 1995.[Abstract/Free Full Text]
Received for publication April 19, 1999. Accepted for publication September 29, 1999.




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