Does Small Intestinal Atresia Affect Epithelial Protein Expression in Human Newborns?
Maaike W Schaart
Division of Neonatology, Department of Pediatrics, Erasmus Medical Center–Sophia Children's Hospital, Rotterdam, The Netherlands
Department of Pediatric Surgery, Erasmus Medical Center–Sophia Children's Hospital, Rotterdam, The Netherlands
Search for more papers by this authorTakeshi Yamanouchi
Department of Pediatric Surgery, Erasmus Medical Center–Sophia Children's Hospital, Rotterdam, The Netherlands
Department of Pediatric Surgery, Reproductive and Developmental Medicine, Kyushu University, Fukuoka, Japan
Search for more papers by this authorDanielle JPM van Nispen
Division of Gastroenterology and Nutrition, Department of Pediatrics
Search for more papers by this authorRolien HC Raatgeep
Division of Gastroenterology and Nutrition, Department of Pediatrics
Search for more papers by this authorJohannes B van Goudoever
Division of Neonatology, Department of Pediatrics, Erasmus Medical Center–Sophia Children's Hospital, Rotterdam, The Netherlands
Search for more papers by this authorRonald R de Krijger
Department of Pathology, Josefine Nefkens Institute, Erasmus Medical Center, Rotterdam, The Netherlands
Search for more papers by this authorDick Tibboel
Department of Pediatric Surgery, Erasmus Medical Center–Sophia Children's Hospital, Rotterdam, The Netherlands
Search for more papers by this authorAlexandra WC Einerhand
Division of Gastroenterology and Nutrition, Department of Pediatrics
Search for more papers by this authorCorresponding Author
Ingrid B Renes
Division of Neonatology, Department of Pediatrics, Erasmus Medical Center–Sophia Children's Hospital, Rotterdam, The Netherlands
Address correspondence and reprint requests to Dr Ingrid B. Renes, Laboratory of Pediatrics, Division of Neonatology, Room no. Ee1571A, Erasmus Medical Center–Sophia Children's Hospital, Dr Molewaterplein 50, 3015 GE, Rotterdam, the Netherlands (e-mail: [email protected]).Search for more papers by this authorMaaike W Schaart
Division of Neonatology, Department of Pediatrics, Erasmus Medical Center–Sophia Children's Hospital, Rotterdam, The Netherlands
Department of Pediatric Surgery, Erasmus Medical Center–Sophia Children's Hospital, Rotterdam, The Netherlands
Search for more papers by this authorTakeshi Yamanouchi
Department of Pediatric Surgery, Erasmus Medical Center–Sophia Children's Hospital, Rotterdam, The Netherlands
Department of Pediatric Surgery, Reproductive and Developmental Medicine, Kyushu University, Fukuoka, Japan
Search for more papers by this authorDanielle JPM van Nispen
Division of Gastroenterology and Nutrition, Department of Pediatrics
Search for more papers by this authorRolien HC Raatgeep
Division of Gastroenterology and Nutrition, Department of Pediatrics
Search for more papers by this authorJohannes B van Goudoever
Division of Neonatology, Department of Pediatrics, Erasmus Medical Center–Sophia Children's Hospital, Rotterdam, The Netherlands
Search for more papers by this authorRonald R de Krijger
Department of Pathology, Josefine Nefkens Institute, Erasmus Medical Center, Rotterdam, The Netherlands
Search for more papers by this authorDick Tibboel
Department of Pediatric Surgery, Erasmus Medical Center–Sophia Children's Hospital, Rotterdam, The Netherlands
Search for more papers by this authorAlexandra WC Einerhand
Division of Gastroenterology and Nutrition, Department of Pediatrics
Search for more papers by this authorCorresponding Author
Ingrid B Renes
Division of Neonatology, Department of Pediatrics, Erasmus Medical Center–Sophia Children's Hospital, Rotterdam, The Netherlands
Address correspondence and reprint requests to Dr Ingrid B. Renes, Laboratory of Pediatrics, Division of Neonatology, Room no. Ee1571A, Erasmus Medical Center–Sophia Children's Hospital, Dr Molewaterplein 50, 3015 GE, Rotterdam, the Netherlands (e-mail: [email protected]).Search for more papers by this authorABSTRACT
Objectives:
Bowel segments distal to a congenital intestinal obstruction have been suggested to be immature. In other words, luminal components such as amniotic fluid (before birth) and/or enteral nutrition (after birth) may be required to activate intestinal epithelial protein expression, thereby influencing epithelial differentiation. We investigated cell-type–specific protein expression proximal and distal to jejunal and ileal atresias in human newborns.
Patients and Methods:
We immunohistochemically studied intestinal tissue specimens of 16 newborns who had undergone surgery for jejunal or ileal atresia. Sections were taken from both the proximal and distal sides of the atresias.
Results:
For all patients, the enterocyte-specific markers lactase, sucrase-isomaltase, sodium glucose cotransporter 1, glucose transporters 2 and 5, intestinal fatty acid–binding protein and alkaline phosphatase were expressed at a mean 3 ± 1 days after birth, both proximal and distal to jejunal and ileal atresias. Expression of goblet cell–specific markers mucin 2 and trefoil factor 3 and that of the Paneth cell marker lysozyme was maintained at either side of the atretic segment.
Conclusions:
With respect to the markers used, the human small intestinal epithelium is already differentiated shortly after birth. The absence of intestinal continuity in case of a jejunal or ileal atresia does not affect epithelial protein expression. This would seem to indicate that the developing small intestinal epithelium matures independently of luminal components.
REFERENCES
- 1Miller AJW, Rode H, Cywes S. Intestinal atresia and stenosis. In: KW Ashcraft, GW Holcomb, JP Murphy, eds. Pediatric Surgery. Philadelphia, PA: Elsevier Saunders, 2005: 416–34.
- 2Van Beers EH, Buller HA, Grand RJ, et al. Intestinal brush border glycohydrolases: structure, function, and development. Crit Rev Biochem Mol Biol 1995; 30: 197–262.
- 3Cohn SM, Simon TC, Roth KA, et al. Use of transgenic mice to map cis-acting elements in the intestinal fatty acid binding protein gene (Fabpi) that control its cell lineage-specific and regional patterns of expression along the duodenal-colonic and crypt-villus axes of the gut epithelium. J Cell Biol 1992; 119: 27–44.
- 4Poelstra K, Bakker WW, Klok PA, et al. Dephosphorylation of endotoxin by alkaline phosphatase in vivo. Am J Pathol 1997; 151: 1163–1169.
- 5Van Klinken BJ, Dekker J, Buller HA, et al. Mucin gene structure and expression: protection vs. adhesion. Am J Physiol 1995; 269: G613–G627.
- 6Lin J, Nadroo AM, Chen W, et al. Ontogeny and prenatal expression of trefoil factor 3/ITF in the human intestine. Early Hum Dev 2003; 71: 103–109.
- 7Hancock RE. Peptide antibiotics. Lancet 1997; 349: 418–422.
- 8Mahida YR, Rose F, Chan WC. Antimicrobial peptides in the gastrointestinal tract. Gut 1997; 40: 161–163.
- 9Tovar JA, Sunol M, Lopez de Torre B, et al. Mucosal morphology in experimental intestinal atresia: studies in the chick embryo. J Pediatr Surg 1991; 26: 184–189.
- 10Touloukian RJ. Antenatal intestinal adaptation with experimental jejunoileal atresia. J Pediatr Surg 1978; 13: 468–474.
- 11Trahair JF, Harding R. Ultrastructural anomalies in the fetal small intestine indicate that fetal swallowing is important for normal development: an experimental study. Virchows Arch A Pathol Anat Histopathol 1992; 420: 305–312.
- 12Touloukian RJ, Wright HK. Intrauterine villus hypertrophy with jejunoileal atresia. J Pediatr Surg 1973; 8: 779–784.
- 13Verburg M, Renes IB, Meijer HP, et al. Selective sparing of goblet cells and paneth cells in the intestine of methotrexate-treated rats. Am J Physiol Gastrointest Liver Physiol 2000; 279: G1037–G1047.
- 14Yeh KY, Yeh M, Holt PR. Thyroxine and cortisone cooperate to modulate postnatal intestinal enzyme differentiation in the rat. Am J Physiol 1991; 260: G371–G378.
- 15Hirayama BA, Lostao MP, Panayotova-Heiermann M, et al. Kinetic and specificity differences between rat, human, and rabbit Na+-glucose cotransporters (SGLT-1). Am J Physiol 1996; 270: G919–G926.
- 16Kanda T, Fujii H, Fujita M, et al. Intestinal fatty acid binding protein is available for diagnosis of intestinal ischaemia: immunochemical analysis of two patients with ischaemic intestinal diseases. Gut 1995; 36: 788–791.
- 17Tytgat KM, Bovelander FJ, Opdam FJ, et al. Biosynthesis of rat MUC2 in colon and its analogy with human MUC2. Biochem J 1995; 309: 221–229.
- 18Podolsky DK, Lynch-Devaney K, Stow JL, et al. Identification of human intestinal trefoil factor. Goblet cell-specific expression of a peptide targeted for apical secretion. J Biol Chem 1993; 268: 6694–6702.
- 19Alpers DH. Digestion and absorption of carbohydrates and proteins. In: LR Johnson, ed. Physiology of the Gastrointestinal Tract. New York, NY: Raven Press, 1994: 1723–49.
- 20Wright EM, Hirayama BA, Loo DD, et al. Intestinal sugar transport. In: LR Johnson, ed. Physiology of the Gastrointestinal Tract. New York, NY: Raven Press, 1994.
- 21Alpers DH, Bass NM, Engle MJ, et al. Intestinal fatty acid binding protein may favor differential apical fatty acid binding in the intestine. Biochim Biophys Acta 2000; 1483: 352–362.
- 22Tilson MD. Compensatory hypertrophy of the gut in an infant with intestinal atresia. Am J Surg 1972; 123: 733–734.
- 23Davidson NO, Hausman AM, Ifkovits CA, et al. Human intestinal glucose transporter expression and localization of GLUT5. Am J Physiol 1992; 262: C795–C800.
- 24Montgomery RK, Mulberg AE, Grand RJ. Development of the human gastrointestinal tract: twenty years of progress. Gastroenterology 1999; 116: 702–731.
- 25Dahlqvist A, Lindberg T. Development of the intestinal disaccharidase and alkaline phosphatase activities in the human foetus. Clin Sci (Lond) 1966; 30: 517–528.
- 26Pelsers MM, Namiot Z, Kisielewski W, et al. Intestinal-type and liver-type fatty acid-binding protein in the intestine. Tissue distribution and clinical utility. Clin Biochem 2003; 36: 529–535.
- 27Buisine MP, Devisme L, Savidge TC, et al. Mucin gene expression in human embryonic and fetal intestine. Gut 1998; 43: 519–524.
- 28Klockars M, Reitamo S, Adinolfi M. Ontogeny of human lysozyme. Distribution in fetal tissues. Biol Neonate 1977; 32: 243–249.
- 29Surana R, Puri P. Small intestinal atresia: effect on fetal nutrition. J Pediatr Surg 1994; 29: 1250–1252.
- 30Trahair JF. Is fetal enteral nutrition important for normal gastrointestinal growth? a discussion. JPEN J Parenter Enteral Nutr 1993; 17: 82–85.
- 31Trahair JF, Rodgers HF, Cool JC, et al. Altered intestinal development after jejunal ligation in fetal sheep. Virchows Arch A Pathol Anat Histopathol 1993; 423: 45–50.
- 32Rubin DC, Swietlicki E, Roth KA, et al. Use of fetal intestinal isografts from normal and transgenic mice to study the programming of positional information along the duodenal-to-colonic axis. J Biol Chem 1992; 267: 15122–15133.
- 33Blache P, van de Wetering M, Duluc I, et al. SOX9 is an intestine crypt transcription factor, is regulated by the Wnt pathway, and represses the CDX2 and MUC2 genes. J Cell Biol 2004; 166: 37–47.
- 34Pinto D, Clevers H. Wnt control of stem cells and differentiation in the intestinal epithelium. Exp Cell Res 2005; 306: 357–363.
- 35van Es JH, Jay P, Gregorieff A, et al. Wnt signalling induces maturation of Paneth cells in intestinal crypts. Nat Cell Biol 2005; 7: 381–386.
- 36Trahair JF, Sangild PT. Systemic and luminal influences on the perinatal development of the gut. Equine Vet J Suppl 1997; 24: 40–50.
10.1111/j.2042-3306.1997.tb05077.x Google Scholar
- 37Serrano J, Zetterstrom R. Disaccharidase activities and intestinal absorption in infants with congenital intestinal obstruction. J Pediatr Gastroenterol Nutr 1987; 6: 238–243.
- 38Goulet O, Baglin-Gobet S, Talbotec C, et al. Outcome and long-term growth after extensive small bowel resection in the neonatal period: a survey of 87 children. Eur J Pediatr Surg 2005; 15: 95–101.
- 39Cohen IT, Greecher CP. Nutritional status following surgical correction of congenital gastrointestinal anomalies. J Pediatr Surg 1979; 14: 289–386.
Citing Literature
