Alanyl-glutamine promotes intestinal epithelial cell homeostasis in vitro and in a murine model of weanling undernutrition.

Alanyl-glutamine (Ala-Gln) has recently been shown to enhance catch-up growth and gut integrity in undernourished children from Northeast Brazil. We hypothesized that the intestinal epithelial effects of Ala-Gln in malnourished weanling mice and mouse small intestinal epithelial (MSIE) cells would include modulation of barrier function, proliferation, and apoptosis. Dams of 10-day-old suckling C57BL/6 pups were randomized to a standard diet or an isocaloric Northeast Brazil "regional basic diet," moderately deficient in protein, fat, and minerals. Upon weaning to their dam's diet on day of life 21, pups were randomized to Ala-Gln solution or water. At 6 wk of age, mice were killed, and jejunal tissue was collected for morphology, immunohistochemistry, and Ussing chamber analysis of transmucosal resistance and permeability. Proliferation of MSIE cells in the presence or absence of Ala-Gln was measured by MTS and bromodeoxyuridine assays. MSIE apoptosis was assessed by annexin and 7-amino-actinomycin D staining. Pups of regional basic diet-fed dams exhibited failure to thrive. Jejunal specimens from undernourished weanlings showed decreased villous height and crypt depth, decreased transmucosal resistance, increased permeability to FITC-dextran, increased claudin-3 expression, and decreased epithelial proliferation and increased epithelial apoptosis (as measured by bromodeoxyuridine and cleaved caspase-3 staining, respectively). Undernourished weanlings supplemented with Ala-Gln showed improvements in weight velocity, villous height, crypt depth, transmucosal resistance, and epithelial proliferation/apoptosis compared with unsupplemented controls. Similarly, Ala-Gln increased proliferation and reduced apoptosis in MSIE cells. In summary, Ala-Gln promotes intestinal epithelial homeostasis in a mouse model of malnutrition-associated enteropathy, mimicking key features of the human disease.

[1]  H. Daniel,et al.  Amino acid absorption and homeostasis in mice lacking the intestinal peptide transporter PEPT1. , 2011, American journal of physiology. Gastrointestinal and liver physiology.

[2]  T. Ahmed,et al.  Intestinal Mucosal Permeability of Severely Underweight and Nonmalnourished Bangladeshi Children and Effects of Nutritional Rehabilitation , 2010, Journal of pediatric gastroenterology and nutrition.

[3]  M. Levine Immunogenicity and efficacy of oral vaccines in developing countries: lessons from a live cholera vaccine , 2010, BMC Biology.

[4]  S. Moore,et al.  Prolonged episodes of acute diarrhea reduce growth and increase risk of persistent diarrhea in children. , 2010, Gastroenterology.

[5]  Kechen Ban,et al.  Glutamine protects against apoptosis via downregulation of Sp3 in intestinal epithelial cells. , 2010, American journal of physiology. Gastrointestinal and liver physiology.

[6]  Hae-Ra Han,et al.  The impact of glutamine dipeptide-supplemented parenteral nutrition on outcomes of surgical patients: a meta-analysis of randomized clinical trials. , 2010, JPEN. Journal of parenteral and enteral nutrition.

[7]  M. Bhan,et al.  Improving the performance of enteric vaccines in the developing world , 2010, Nature Immunology.

[8]  R. Shulman,et al.  Perturbed Zinc Homeostasis in Rural 3–5-y-Old Malawian Children Is Associated With Abnormalities in Intestinal Permeability Attributed to Tropical Enteropathy , 2010, Pediatric Research.

[9]  W. Blaner,et al.  Effects of Vitamin A Supplementation on Intestinal Barrier Function, Growth, Total Parasitic, and Specific Giardia spp Infections in Brazilian Children: A Prospective Randomized, Double-blind, Placebo-controlled Trial , 2010, Journal of pediatric gastroenterology and nutrition.

[10]  F. Finkelman,et al.  Mast cells regulate homeostatic intestinal epithelial migration and barrier function by a chymase/Mcpt4-dependent mechanism , 2009, Proceedings of the National Academy of Sciences.

[11]  Jean H Humphrey,et al.  Child undernutrition, tropical enteropathy, toilets, and handwashing , 2009, The Lancet.

[12]  R. Shulman,et al.  A Randomized, Double-Blind, Placebo-Controlled Trial of Rifaximin, a Nonabsorbable Antibiotic, in the Treatment of Tropical Enteropathy , 2009, The American Journal of Gastroenterology.

[13]  Ricardo Luzardo,et al.  Chronic undernutrition alters renal active Na+ transport in young rats: potential hidden basis for pathophysiological alterations in adulthood? , 2009, European journal of nutrition.

[14]  E. Chang,et al.  Glutamine increases autophagy under Basal and stressed conditions in intestinal epithelial cells. , 2009, Gastroenterology.

[15]  Guoyao Wu,et al.  Glutamine, arginine, and leucine signaling in the intestine , 2009, Amino Acids.

[16]  D. Herndon,et al.  Starvation-induced proximal gut mucosal atrophy diminished with aging. , 2009, JPEN. Journal of parenteral and enteral nutrition.

[17]  R. Guerrant,et al.  Cryptosporidium Infection Causes Undernutrition and, Conversely, Weanling Undernutrition Intensifies Infection , 2008, The Journal of parasitology.

[18]  S. Moore,et al.  Malnutrition as an enteric infectious disease with long-term effects on child development. , 2008, Nutrition reviews.

[19]  F. Finkelman,et al.  IL-9– and mast cell–mediated intestinal permeability predisposes to oral antigen hypersensitivity , 2008, The Journal of experimental medicine.

[20]  C. Mathers,et al.  Maternal and child undernutrition: global and regional exposures and health consequences , 2008, The Lancet.

[21]  D. Chung,et al.  Molecular mechanisms contributing to glutamine-mediated intestinal cell survival. , 2007, American journal of physiology. Gastrointestinal and liver physiology.

[22]  H. Vaudry,et al.  Glutamine Regulates the Human Epithelial Intestinal HCT-8 Cell Proteome under Apoptotic Conditions*S , 2007, Molecular & Cellular Proteomics.

[23]  M. Elia,et al.  A double-blind, placebo-controlled, glutamine-supplementation trial in growth-faltering Gambian infants. , 2007, The American journal of clinical nutrition.

[24]  A. Coran,et al.  Dietary Glutamine Supplementation Prevents Mucosal Injury and Modulates Intestinal Epithelial Restitution Following Ischemia-Reperfusion Injury in the Rat , 2007, Digestive Diseases and Sciences.

[25]  R. Guerrant,et al.  Wasting and Intestinal Barrier Function in Children Taking Alanyl-Glutamine–Supplemented Enteral Formula , 2007, Journal of pediatric gastroenterology and nutrition.

[26]  J. Clark,et al.  Intestinal barrier failure during experimental necrotizing enterocolitis: protective effect of EGF treatment. , 2006, American journal of physiology. Gastrointestinal and liver physiology.

[27]  L. Cerchietti,et al.  Double-blinded, placebo-controlled trial on intravenous L-alanyl-L-glutamine in the incidence of oral mucositis following chemoradiotherapy in patients with head-and-neck cancer. , 2006, International journal of radiation oncology, biology, physics.

[28]  D. Polk,et al.  Regulation of apoptosis during homeostasis and disease in the intestinal epithelium. , 2006, Inflammatory bowel diseases.

[29]  F. Canon,et al.  A regional model (Northeastern Brazil) of induced mal-nutrition delays ontogeny of reflexes and locomotor activity in rats , 2006, Nutritional neuroscience.

[30]  R. Guerrant,et al.  Caspase and Bid Involvement in Clostridium difficile Toxin A-Induced Apoptosis and Modulation of Toxin A Effects by Glutamine and Alanyl-Glutamine In Vivo and In Vitro , 2006, Infection and Immunity.

[31]  R. Shulman,et al.  Effect of Lactobacillus GG on intestinal integrity in Malawian children at risk of tropical enteropathy. , 2005, The American journal of clinical nutrition.

[32]  Dean P. Jones,et al.  Glutamine inhibits cytokine-induced apoptosis in human colonic epithelial cells via the pyrimidine pathway. , 2005, American journal of physiology. Gastrointestinal and liver physiology.

[33]  R. Guerrant,et al.  Intestinal Barrier Function and Weight Gain in Malnourished Children Taking Glutamine Supplemented Enteral Formula , 2005, Journal of pediatric gastroenterology and nutrition.

[34]  N. Tanaka,et al.  Glutamine is a key regulator for amino acid-controlled cell growth through the mTOR signaling pathway in rat intestinal epithelial cells. , 2004, Biochemical and biophysical research communications.

[35]  R. Guerrant,et al.  Alanyl-glutamine hastens morphologic recovery from 5-fluorouracil-induced mucositis in mice. , 2004, Nutrition.

[36]  P. Sheth,et al.  L-Glutamine ameliorates acetaldehyde-induced increase in paracellular permeability in Caco-2 cell monolayer. , 2004, American journal of physiology. Gastrointestinal and liver physiology.

[37]  L. Caulfield,et al.  Undernutrition as an underlying cause of child deaths associated with diarrhea, pneumonia, malaria, and measles. , 2004, The American journal of clinical nutrition.

[38]  J. Neu,et al.  Effects of Protein Deprivation on Growth and Small Intestine Morphology Are Not Improved By Glutamine or Glutamate in Gastrostomy-Fed Rat Pups , 2004, Journal of pediatric gastroenterology and nutrition.

[39]  S. Piscitelli,et al.  Diarrhea and reduced levels of antiretroviral drugs: improvement with glutamine or alanyl-glutamine in a randomized controlled trial in northeast Brazil. , 2004, Clinical infectious diseases : an official publication of the Infectious Diseases Society of America.

[40]  E. Elliott,et al.  Intestinal Infections and Environmental Enteropathy: Working Group Report of the Second World Congress of Pediatric Gastroenterology, Hepatology, and Nutrition , 2004, Journal of pediatric gastroenterology and nutrition.

[41]  E. Chang,et al.  Bacterial Superantigen-Treated Intestinal Epithelial Cells Upregulate Heat Shock Proteins 25 and 72 and Are Resistant to Oxidant Cytotoxicity , 2004, Infection and Immunity.

[42]  J. Mwansa,et al.  Responses of small intestinal architecture and function over time to environmental factors in a tropical population. , 2004, The American journal of tropical medicine and hygiene.

[43]  Dean P. Jones,et al.  Trophic and cytoprotective nutrition for intestinal adaptation, mucosal repair, and barrier function. , 2003, Annual review of nutrition.

[44]  Dean P. Jones,et al.  Glutamine prevents cytokine-induced apoptosis in human colonic epithelial cells. , 2003, The Journal of nutrition.

[45]  R. Guerrant,et al.  Effects of an alanyl-glutamine-based oral rehydration and nutrition therapy solution on electrolyte and water absorption in a rat model of secretory diarrhea induced by cholera toxin. , 2002, Nutrition.

[46]  D. C. Gomes,et al.  Morphological aspects of Schistosoma mansoni adult worms isolated from nourished and undernourished mice: a comparative analysis by confocal laser scanning microscopy. , 2001, Memorias do Instituto Oswaldo Cruz.

[47]  I. Zulu,et al.  Tropical enteropathy: a T-cell-mediated crypt hyperplastic enteropathy , 2001, European journal of gastroenterology & hepatology.

[48]  R. Guerrant,et al.  Glutamine transporter in crypts compensates for loss of villus absorption in bovine cryptosporidiosis. , 2001, American journal of physiology. Gastrointestinal and liver physiology.

[49]  R. Martindale,et al.  Glutamine and the gastrointestinal tract , 2000, Current opinion in clinical nutrition and metabolic care.

[50]  J. Schulzke,et al.  Leaks in the epithelial barrier caused by spontaneous and TNF‐α‐induced single‐cell apoptosis , 2000 .

[51]  D. Chung,et al.  Prevention of mucosal atrophy: Role of glutamine and caspases in apoptosis in intestinal epithelial cells , 2000, Journal of Gastrointestinal Surgery.

[52]  T. Ko,et al.  Glutamine deprivation induces apoptosis in intestinal epithelial cells. , 1998, Surgery.

[53]  D. Brenner,et al.  L-glutamine stimulates intestinal cell proliferation and activates mitogen-activated protein kinases. , 1997, The American journal of physiology.

[54]  R. Guedes,et al.  Spreading depression is facilitated in adult rats previously submitted to short episodes of malnutrition during the lactation period. , 1997, Brazilian journal of medical and biological research = Revista brasileira de pesquisas medicas e biologicas.

[55]  R. Thisted,et al.  Glutamine protects intestinal epithelial cells: role of inducible HSP70. , 1997, The American journal of physiology.

[56]  E. O'Loughlin,et al.  Intestinal permeability in kwashiorkor , 1997, Archives of disease in childhood.

[57]  N. Darmon,et al.  Intestinal paracellular permeability during malnutrition in guinea pigs: effect of high dietary zinc. , 1996, Gut.

[58]  B. Evers,et al.  Glutamine-mediated regulation of heat shock protein expression in intestinal cells. , 1995, Surgery.

[59]  K. Magnusson,et al.  Enteral glutamine increases growth and absorptive capacity of intestinal mucosa in the malnourished rat. , 1995, Scandinavian journal of gastroenterology.

[60]  M. R. Toledo,et al.  Asymptomatic environmental enteropathy among slum-dwelling infants. , 1994, Journal of the American College of Nutrition.

[61]  E. Coutinho,et al.  Intestinal protein absorption in malnourished mice with acute schistosomiasis mansoni. , 1993, Memorias do Instituto Oswaldo Cruz.

[62]  S. Romani,et al.  A regional basic diet from northeast Brazil as a dietary model of experimental malnutrition. , 1990, Archivos latinoamericanos de nutricion.

[63]  R. Levin,et al.  Diarrhoea of famine and malnutrition--investigations using a rat model. 2--Ileal hypersecretion induced by starvation. , 1990, Gut.

[64]  E. Savilahti,et al.  Morphometric Study of the Jejunal Mucosa in Various Childhood Enteropathies with Special Reference to Intraepithelial Lymphocytes , 1982, Journal of pediatric gastroenterology and nutrition.

[65]  G. Slavin,et al.  Jejunal mucosal morphometry in children with and without gut symptoms and in normal adults. , 1981, Journal of clinical pathology.

[66]  H. Lotero,et al.  Enteropathy in adult protein malnutrition: light microscopic findings. , 1975, The American journal of clinical nutrition.

[67]  D. Brenner,et al.  Glutamine metabolism stimulates intestinal cell MAPKs by a cAMP-inhibitable, Raf-independent mechanism. , 2000, Gastroenterology.

[68]  P. Wolf,et al.  Tropical sprue and subclinical enteropathy: a vision for the nineties. , 1997, Critical reviews in clinical laboratory sciences.

[69]  E. Coutinho,et al.  Nutrition and acute schistosomiasis. , 1992, Memorias do Instituto Oswaldo Cruz.

[70]  E. Coutinho,et al.  The influence of the regional basic diet from northeast Brazil on health and nutritional conditions of mice infected with Schistosoma mansoni. , 1992, Revista da Sociedade Brasileira de Medicina Tropical.

[71]  R. Guedes,et al.  Enhanced rate of cortical spreading depression due to malnutrition: prevention by dietary protein supplementation. , 1990, Brazilian journal of medical and biological research = Revista brasileira de pesquisas medicas e biologicas.

[72]  R. Guedes,et al.  Sciatic nerve conduction velocity of malnourished rats fed the human "basic regional diet" of the northeast of Brazil. , 1987, Brazilian journal of medical and biological research = Revista brasileira de pesquisas medicas e biologicas.

[73]  R. Guedes,et al.  Propagation of cortical spreading depression in malnourished rats: facilitatory effect of dietary protein deficiency. , 1987, Brazilian journal of medical and biological research = Revista brasileira de pesquisas medicas e biologicas.