Abstract
Background
Intestinal adaptation occurs in the residual bowel following the loss or resection of a proportion of the small bowel. The purpose of the adaptive response is to return absorptive and digestive properties to near normal levels. This study employed a rat model of massive small bowel resection (MSBR) to study the adaptive response in the residual terminal ileum and the jejunum. The time points were chosen to reflect changes in gene expression early on in the response, because these are the genes that alter to initiate and maximize the response observed during adaptation.
Methods
Sprague Dawley rats underwent an 80% resection. Differential display polymerase chain reaction (DD-PCR) analysis was performed on mRNA extracted from the remnant ileum and jejunum 0, 1, 2, 4, and 7 days post-MSBR.
Results
DD-PCR identified 11 genes that were possibly regulated following MSBR. Genes confirmed to be regulated were 16S ribosomal RNA, lymphocyte antigen 6 (LY6)-like molecule, Krüppel-like factor-3 (KLF-3), G-protein-binding protein (CRFG), system A transporter 2 (SAT2), and an intestine-specific gene (similar to mKIAA0493).
Conclusions
DD-PCR analysis showed regulation of a number of genes not previously known to be involved in adaptation after MSBR or previously characterized in the intestine. These genes may be important in bringing about the complement of changes seen during the adaptive response.
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References
A Tavakkolizadeh EE Whang (2002) ArticleTitleUnderstanding and augmenting human intestinal adaptation: a call for more clinical research JPEN J Parenter Enteral Nutr 26 251–5 Occurrence Handle12090691
RH Dowling (1982) ArticleTitleSmall bowel adaptation and its regulation Scand J Gastroenterol Suppl 74 53–74 Occurrence Handle1:STN:280:DyaL3s%2FmslWntQ%3D%3D Occurrence Handle6815781
CC Booth KT Evans T Menzies DF Street (1959) ArticleTitleIntestinal hypertrophy following partial resection of the small bowel in the rat Br J Surg 46 403–10 Occurrence Handle1:STN:280:DyaG1M%2FmvVWrug%3D%3D Occurrence Handle13638583
JB Bristol RCN Williamson (1988) ArticleTitleMechanisms of intestinal adaptation Pediatr Surg Int 4 233–41
KM Ekelund E Ekblad (1999) ArticleTitleStructural, neuronal, and functional adaptive changes in atrophic rat ileum Gut 45 236–45 Occurrence Handle1:STN:280:DyaK1Mzjt1alsA%3D%3D Occurrence Handle10403736 Occurrence Handle10.1136/gut.45.2.236
RP Thomas M Slogoff FW Smith BM Evers (2003) ArticleTitleEffect of aging on the adaptive and proliferative capacity of the small bowel J Gastrointest Surg 7 88–95 Occurrence Handle10.1016/S1091-255X(02)00128-2 Occurrence Handle12559189
MC Wolvekamp E Heineman RG Taylor PJ Fuller (1996) ArticleTitleTowards understanding the process of intestinal adaptation Dig Dis 14 59–72 Occurrence Handle1:STN:280:DyaK28zlvF2ksw%3D%3D Occurrence Handle8719733
CF Welters CH Dejong NE Deutz E Heineman (2002) ArticleTitleIntestinal adaptation in short bowel syndrome ANZ J Surg 72 229–36 Occurrence Handle10.1046/j.1445-2197.2002.02357.x Occurrence Handle12071459
L Baksheev PJ Fuller (2000) ArticleTitleHumoral factors in intestinal adaptation Trends Endocrinol Metab 11 401–5 Occurrence Handle10.1016/S1043-2760(00)00307-6 Occurrence Handle1:CAS:528:DC%2BD3cXot12ku7o%3D Occurrence Handle11091116
JA Vanderhoof AN Langnas (1997) ArticleTitleShort-bowel syndrome in children and adults Gastroenterology 113 1767–78 Occurrence Handle10.1053/gast.1997.v113.pm9352883 Occurrence Handle1:CAS:528:DyaK2sXnt1ynt7k%3D Occurrence Handle9352883
MA Helmrath WE Vanderkolk G Can CR Erwin BW Warner (1996) ArticleTitleIntestinal adaptation following massive small bowel resection in the mouse J Am Coll Surg 183 441–9 Occurrence Handle1:STN:280:DyaK2s%2FmvFKhuw%3D%3D Occurrence Handle8912612
RG Taylor DJ Beveridge PJ Fuller (1992) ArticleTitleExpression of ileal glucagon and peptide tyrosine-tyrosine genes. Response to inhibition of polyamine synthesis in the presence of massive small-bowel resection Biochem J 286 737–41 Occurrence Handle1:CAS:528:DyaK38Xls1ykt7Y%3D Occurrence Handle1417733
PA Kitchen JR Walters (2001) ArticleTitleMolecular and cellular biology of small-bowel mucosa Curr Opin Gastroenterol 17 104–9 Occurrence Handle10.1097/00001574-200103000-00002 Occurrence Handle1:CAS:528:DC%2BD3MXptlSjsbc%3D Occurrence Handle11224664
RS Macdonald (1999) ArticleTitleThe role of insulin-like growth factors in small intestinal cell growth and development Horm Metab Res 31 103–13 Occurrence Handle1:CAS:528:DyaK1MXitlKlurY%3D Occurrence Handle10226789 Occurrence Handle10.1055/s-2007-978706
PK Lund (1998) ArticleTitleMolecular basis of intestinal adaptation: the role of the insulin-like growth factor system Ann N Y Acad Sci 859 18–36 Occurrence Handle10.1111/j.1749-6632.1998.tb11108.x Occurrence Handle1:CAS:528:DyaK1MXitVCntQ%3D%3D Occurrence Handle9928367
DM Ney (1999) ArticleTitleEffects of insulin-like growth factor-I and growth hormone in models of parenteral nutrition J Parenter Enteral Nutr 23 S184–9 Occurrence Handle1:CAS:528:DC%2BD3cXlvFGmtLo%3D
MZ Schwartz KA Kuenzler (2001) ArticleTitlePharmacotherapy and growth factors in the treatment of short bowel syndrome Semin Pediatr Surg 10 81–90 Occurrence Handle10.1053/spsu.2001.22385 Occurrence Handle1:STN:280:DC%2BD3MzntVyquw%3D%3D Occurrence Handle11329609
HC Lin XT Zhao L Wang H Wong (1996) ArticleTitleFat-induced ileal brake in the dog depends on peptide YY Gastroenterology 110 1491–5 Occurrence Handle10.1053/gast.1996.v110.pm8613054 Occurrence Handle1:CAS:528:DyaK28XjtV2htLY%3D Occurrence Handle8613054
TJ Kalogeris X Qin WY Chey P Tso (1998) ArticleTitlePYY stimulates synthesis and secretion of intestinal apolipoprotein AIV without affecting mRNA expression Am J Physiol 275 G668–74 Occurrence Handle1:CAS:528:DyaK1cXmsl2itLc%3D Occurrence Handle9756495
T Okumura K Fukagawa P Tso IL Taylor TN Pappas (1994) ArticleTitleIntracisternal injection of apolipoprotein A-IV inhibits gastric secretion in pylorus-ligated conscious rats Gastroenterology 107 1861–4 Occurrence Handle1:CAS:528:DyaK2MXivFSlsLg%3D Occurrence Handle7958703
JS Thompson (1999) ArticleTitleEpidermal growth factor and the short bowel syndrome J Parenter Enteral Nutr 23 S113–6 Occurrence Handle1:CAS:528:DC%2BD3cXlvFGnsLw%3D Occurrence Handle10.1177/014860719902300528
MS Chaet G Arya MM Ziegler BW Warner (1994) ArticleTitleEpidermal growth factor enhances intestinal adaptation after massive small bowel resection J Pediatr Surg 29 1035–8 Occurrence Handle10.1016/0022-3468(94)90274-7 Occurrence Handle1:STN:280:DyaK2M%2FlsVymtA%3D%3D Occurrence Handle7965502
GS Howarth CA Shoubridge (2001) ArticleTitleEnhancement of intestinal growth and repair by growth factors Curr Opin Pharmacol 1 568–74 Occurrence Handle10.1016/S1471-4892(01)00098-4 Occurrence Handle1:CAS:528:DC%2BD3MXovVOgtrk%3D Occurrence Handle11757811
CF Welters CH Dejong NE Deutz E Heineman (2001) ArticleTitleIntestinal function and metabolism in the early adaptive phase after massive small bowel resection in the rat J Pediatr Surg 36 1746–51 Occurrence Handle10.1053/jpsu.2001.28813 Occurrence Handle1:STN:280:DC%2BD3MnoslamtQ%3D%3D Occurrence Handle11733898
CR Erwin RA Falcone SuffixJr LE Stern CJ Kemp BW Warner (2000) ArticleTitleAnalysis of intestinal adaptation gene expression by cDNA expression arrays J Parenter Enteral Nutr 24 311–6 Occurrence Handle1:CAS:528:DC%2BD3cXotVOmtbk%3D
LE Stern CR Erwin RA Falcone FS Huang CJ Kemp JL Williams et al. (2001) ArticleTitlecDNA microarray analysis of adapting bowel after intestinal resection J Pediatr Surg 36 190–5 Occurrence Handle10.1053/jpsu.2001.20050 Occurrence Handle1:STN:280:DC%2BD3MzgsVSltA%3D%3D Occurrence Handle11150463
RG Taylor PJ Fuller (1994) ArticleTitleHumoral regulation of intestinal adaptation Baillieres Clin Endocrinol Metab 8 165–83 Occurrence Handle10.1016/S0950-351X(05)80230-7 Occurrence Handle1:STN:280:DyaK2c7otlWitQ%3D%3D Occurrence Handle8135702
RG Taylor K Verity PJ Fuller (1990) ArticleTitleIleal glucagon gene expression: ontogeny and response to massive small bowel resection Gastroenterology 99 724–9 Occurrence Handle1:CAS:528:DyaK3MXkt1OjsLk%3D Occurrence Handle2379778
J Sambrook DW Russell (2001) Molecular cloning: a laboratory manual Cold Spring Harbour Laboratory Press NY, USA
P Liang AB Pardee (1998) ArticleTitleDifferential display. A general protocol Mol Biotechnol 10 261–7 Occurrence Handle1:CAS:528:DyaK1MXht1Gmt7Y%3D Occurrence Handle9951706
PJ Fuller DJ Beveridge RG Taylor (1993) ArticleTitleIleal proglucagon gene expression in the rat: characterization in intestinal adaptation using in situ hybridization Gastroenterology 104 459–66 Occurrence Handle1:CAS:528:DyaK3sXpsVOmuw%3D%3D Occurrence Handle8425688
DB Rountree MH Ulshen S Selub CR Fuller SR Bloom MA Ghatei et al. (1992) ArticleTitleNutrient-independent increases in proglucagon and ornithine decarboxylase messenger RNAs after jejunoileal resection Gastroenterology 103 462–8 Occurrence Handle1:CAS:528:DyaK3sXhvV2isro%3D Occurrence Handle1634064
P Liang AB Pardee (1992) ArticleTitleDifferential display of eukaryotic messenger RNA by means of the polymerase chain reaction Science 257 967–71 Occurrence Handle10.1126/science.1354393 Occurrence Handle1:CAS:528:DyaK38Xls1Cqt70%3D Occurrence Handle1354393
P Liang D Bauer L Averboukh P Warthoe M Rohrwild H Muller et al. (1995) ArticleTitleAnalysis of altered gene expression by differential display Methods Enzymol 254 304–21 Occurrence Handle1:CAS:528:DyaK2MXps1Cktr8%3D Occurrence Handle8531695 Occurrence Handle10.1016/0076-6879(95)54022-9
TP Mayall I Bjarnason UY Khoo TJ Peters AJ Macpherson (1995) ArticleTitleMitochondrial gene expression in small intestinal epithelial cells Biochem J 308 665–71 Occurrence Handle1:CAS:528:DyaK2MXmtFersb0%3D Occurrence Handle7539612
M Mallya RD Campbell B Aguado (2002) ArticleTitleTranscriptional analysis of a novel cluster of LY-6 family members in the human and mouse major histocompatibility complex: five genes with many splice forms Genomics 80 113–23 Occurrence Handle10.1006/geno.2002.6794 Occurrence Handle1:CAS:528:DC%2BD38XkslSjsbY%3D Occurrence Handle12079290
TJ Fleming C O'huigin TR Malek (1993) ArticleTitleCharacterization of two novel Ly-6 genes. Protein sequence and potential structural similarity to alpha-bungarotoxin and other neurotoxins J Immunol 150 5379–90 Occurrence Handle1:CAS:528:DyaK3sXmt1eltro%3D Occurrence Handle8515066
H Takatsu K Yoshino K Nakayama (2000) ArticleTitleAdaptor gamma ear homology domain conserved in gamma-adaptin and GGA proteins that interact with gamma-synergin Biochem Biophys Res Commun 271 719–25 Occurrence Handle10.1006/bbrc.2000.2700 Occurrence Handle1:CAS:528:DC%2BD3cXjt1Sjtr4%3D Occurrence Handle10814529
EC Dell'angelica R Puertollano C Mullins RC Aguilar JD Vargas LM Hartnell et al. (2000) ArticleTitleGGAs: a family of ADP ribosylation factor-binding proteins related to adaptors and associated with the Golgi complex J Cell Biol 149 81–94 Occurrence Handle10.1083/jcb.149.1.81 Occurrence Handle10747089
T Shiba M Kawasaki H Takatsu T Nogi N Matsugaki N Igarashi et al. (2003) ArticleTitleMolecular mechanism of membrane recruitment of GGA by ARF in lysosomal protein transport Nat Struct Biol 10 386–93 Occurrence Handle10.1038/nsb920 Occurrence Handle1:CAS:528:DC%2BD3sXjtFKnsrc%3D Occurrence Handle12679809
NJ Laping BA Olson Y Zhu (2001) ArticleTitleIdentification of a novel nuclear guanosine triphosphate-binding protein differentially expressed in renal disease J Am Soc Nephrol 12 883–90 Occurrence Handle1:CAS:528:DC%2BD3MXjvVCgt7g%3D Occurrence Handle11316846
J Turner M Crossley (1998) ArticleTitleCloning and characterization of mCtBP2, a co-repressor that associates with basic Kruppel-like factor and other mammalian transcriptional regulators EMBO J 17 5129–40 Occurrence Handle10.1093/emboj/17.17.5129 Occurrence Handle1:CAS:528:DyaK1cXmt1Clsbo%3D Occurrence Handle9724649
J Turner H Nicholas D Bishop JM Matthews M Crossley (2003) ArticleTitleThe LIM protein FHL3 binds basic Kruppel-like factor/Kruppel-like factor 3 and its co-repressor C-terminal-binding protein 2 J Biol Chem 278 12786–95 Occurrence Handle10.1074/jbc.M300587200 Occurrence Handle1:CAS:528:DC%2BD3sXislGrsb4%3D Occurrence Handle12556451
AB Thomson M Keelan (1986) ArticleTitleThe development of the small intestine Can J Physiol Pharmacol 64 13–29 Occurrence Handle1:CAS:528:DyaL28Xht1Ojt7c%3D Occurrence Handle3513924
AB Thomson M Keelan A Thiesen MT Clandinin M Ropeleski GE Wild (2001) ArticleTitleSmall bowel review: normal physiology part 1 Dig Dis Sci 46 2567–87 Occurrence Handle10.1023/A:1012794505897 Occurrence Handle1:CAS:528:DC%2BD38XltVKmsA%3D%3D Occurrence Handle11768247
A Stahl DJ Hirsch RE Gimeno S Punreddy P Ge N Watson et al. (1999) ArticleTitleIdentification of the major intestinal fatty acid transport protein Mol Cell 4 299–308 Occurrence Handle10.1016/S1097-2765(00)80332-9 Occurrence Handle1:CAS:528:DyaK1MXmsVChs78%3D Occurrence Handle10518211
D Yao B Mackenzie H Ming H Varoqui H Zhu MA Hediger et al. (2000) ArticleTitleA novel system A isoform mediating Na+/neutral amino acid cotransport J Biol Chem 275 22790–7 Occurrence Handle10.1074/jbc.M002965200 Occurrence Handle1:CAS:528:DC%2BD3cXltlGru7w%3D Occurrence Handle10811809
R Hyde K Peyrollier HS Hundal (2002) ArticleTitleInsulin promotes the cell surface recruitment of the SAT2/ATA2 system A amino acid transporter from an endosomal compartment in skeletal muscle cells J Biol Chem 277 13628–34 Occurrence Handle10.1074/jbc.M108609200 Occurrence Handle1:CAS:528:DC%2BD38XjsFWnsr8%3D Occurrence Handle11834730
AU Dignass A Sturm (2001) ArticleTitlePeptide growth factors in the intestine Eur J Gastroenterol Hepatol 13 763–70 Occurrence Handle10.1097/00042737-200107000-00002 Occurrence Handle1:CAS:528:DC%2BD3MXlvFais7w%3D Occurrence Handle11474304
GC Hansson D Baeckstrom I Carlstedt K Klinga-Levan (1994) ArticleTitleMolecular cloning of a cDNA coding for a region of an apoprotein from the “insoluble” mucin complex of rat small intestine Biochem Biophys Res Commun 198 181–90 Occurrence Handle10.1006/bbrc.1994.1026 Occurrence Handle1:CAS:528:DyaK2cXhsFGgsLk%3D Occurrence Handle8292021
I Carlstedt A Herrmann H Karlsson J Sheehan LA Fransson GC Hansson (1993) ArticleTitleCharacterization of two different glycosylated domains from the insoluble mucin complex of rat small intestine J Biol Chem 268 18771–81 Occurrence Handle1:CAS:528:DyaK3sXlvFyjsb8%3D Occurrence Handle8360170
A Ozaki T Nagase A Watanabe D Nakajima K Shimada M Nagano et al. (2005) ArticleTitleUtilization of mammalian cells for efficient and reliable evaluation of specificity of antibodies to unravel the cellular function of mKIAA proteins Gene 360 35–44 Occurrence Handle10.1016/j.gene.2005.06.033 Occurrence Handle1:CAS:528:DC%2BD2MXhtFSit73K Occurrence Handle16169687
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Baksheev, L., Fuller, P. Gene expression in the adapting small bowel after massive small bowel resection. J Gastroenterol 41, 1041–1052 (2006). https://doi.org/10.1007/s00535-006-1896-9
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DOI: https://doi.org/10.1007/s00535-006-1896-9