Maternal protein restriction during pregnancy affects gene expression and immunolocalization of intestinal nutrient transporters in rats

Clinical Science

Volumn 125, Issue 6, 2013, Pages 281-289

  Pinheiro, Daniela F ^a   Pinheiro, Patricia F F ^a   Buratini, José ^a   Castilho, Anthony C S ^a   Lima, Paula F ^a   Trinca, Luiza A ^a   Vicentini Paulino, Maria de Lourdes M ^a  

^a SÃO PAULO STATE UNIVERSITY UNESP   (Brazil)

Author keywords

Fetal programming; Intestinal transporter; Peptide transporter 1 (PEPT1); Sodium glucose co transporter 1 (SGLT1)

Indexed keywords

GLUCOSE TRANSPORTER 2; MESSENGER RNA; PEPTIDE TRANSPORTER 1; SODIUM GLUCOSE COTRANSPORTER 2;

ADULT ANIMAL; ANIMAL TISSUE; ARTICLE; CELL PROLIFERATION; CONTROLLED STUDY; DUODENUM; FEMALE; GENE EXPRESSION; IMMUNOLOCALIZATION; IMMUNOREACTIVITY; INTESTINE CELL; MALE; MATERNAL NUTRITION; NONHUMAN; PRIORITY JOURNAL; PROGENY; PROTEIN RESTRICTION; RAT; REAL TIME POLYMERASE CHAIN REACTION; SMALL INTESTINE;

ADAPTATION, PHYSIOLOGICAL; ADIPOSITY; ANIMAL NUTRITIONAL PHYSIOLOGICAL PHENOMENA; ANIMALS; BODY WEIGHT; CELL PROLIFERATION; DIET, PROTEIN-RESTRICTED; DISEASE MODELS, ANIMAL; FEMALE; GENE EXPRESSION REGULATION; GLUCOSE TRANSPORTER TYPE 2; IMMUNOHISTOCHEMISTRY; INTESTINE, SMALL; MALNUTRITION; MATERNAL NUTRITIONAL PHYSIOLOGICAL PHENOMENA; MEMBRANE TRANSPORT PROTEINS; PREGNANCY; RATS; RATS, WISTAR; REAL-TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, MESSENGER; SODIUM-GLUCOSE TRANSPORTER 1; SYMPORTERS;

EID: 84878657380     PISSN: 01435221     EISSN: None     Source Type: Journal    
DOI: 10.1042/CS20120400     Document Type: Article

References (48)

1. Ross, M. G. and Desai, M. (2005) Gestational programming: population survival effects of drought and famine during pregnancy. Am. J. Physiol. Regul. Comp. Physiol. 288, R25-R33
2. Fowden, A. L., Giussani, D. A. and Forhead, A. J. (2006) Intrauterine programming of physiological systems: causes and consequences. Physiology 21, 29-37
3. Desai, M., Gayle, D., Babu, J. and Ross, M. G. (2005) Permanent reduction in heart and kidney organ growth in offspring of undernourished rat dams. Am. J. Obst. Gynecol. 193, 1224-1232
4. Weaver, L. T., Desai, M. and Hales, C. N. (1998) Effects of protein restriction in early life on growth and function of the gastrointestinal tract of the rat. J. Pediatr. Gastroenterol. Nutr. 27, 53-59
5. Pinheiro, D. F., Pacheco, P. D. G., Alvarenga, P. V., Buratini, Jr, J., Castilho, A. C. S., Lima, P. F., Sartori, D. R. S. and Vicentini- Paulino, M. L. M. (2013) Maternal protein restriction affects gene expression and enzyme activity of intestinal disaccharides in adult rat offspring. Braz. J. Med. Biol. Res. 46, 287-292.
6. Timofeeva, N. M., Gordova, L. A., Egorova, V. V. and Nikitina, A. A. (2003) Protein-deficient diet in pregnant females impairs functional activity of enzyme systems in digestive and non-digestive organs in the offspring. Bull. Exp. Biol. Med. 135, 117-119
7. Levin, R. J. (1994) Digestion and absorption of carbohydrates - from molecules and membranes to humans. Am. J. Clin. Nutr. 59, 690S-698S
8. Wit, N. J. W., Bosch-Vermeulen, H., Groot, P. J., Hooiveld, G. J. E. J., Bromhaar, M. M. G., Jansen, J., Müller, M. and Van der Meer, R. (2008) The role of the small intestine in the development of dietary fat-induced obesity and insulin resistance in C57BL/6J mice. BMC Med. Gen. 1, 14-30
9. Mozes, Š., Šefciková, Z., Lenhardt, L'. and Racek, L'. (2004) Obesity and changes of alkaline phosphatase activity in the small intestine of 40- and 80-day-old rats subjected to early postnatal overfeeding or monosodium glutamate. Physiol. Res. 53, 177-186
10. Osswald, C., Baumgarten, K., Stumpel, F., Gorboulev, V., Akimjanova, M., Knobeloch, K-P., Horak, I., Kluge, R., Joost, H-J. and Koepsell, H. (2005) Mice without the regulator gene Rsc1A1 exhibit increased Na-D-Glucose cotransport in small intestine and develop obesity. Mol. Cell. Biol. 25, 78-87
11. Stearns, A. T., Balakrishnan, A. and Tavakkolizadeh, A. (2009) Impact of Roux-en-Ygastric bypass surgery on rat intestinal glucose transport. Am. J. Physiol. Gastrointest. Liver Physiol. 297, G950-G957
12. Drozdowski, L. A., Clandinin, T. and Thomson, A. B. R. (2009) Morphological, kinetic membrane biochemical and genetic aspects of intestinal enteroplasticity. World J. Gastroenterol. 15, 774-787
13. Kellett, G. L. and Helliwell, P. A. (2000) The diffusive component of intestinal glucose absorption is mediated by the glucose-induced recruitment of GLUT2 to the brush-border membrane. Biochem. J. 350, 155-162
14. Kellett, G. L. and Brot-Laroche, E. (2005) Perspectives in diabetes apical GLUT2 a major pathway of intestinal sugar absorption. Diabetes 54, 3056-3062
15. Leibach, F. H. and Ganapathy, V. (1996) Peptide transporters in the intestine and kidney. Annu. Rev. Nutr. 16, 99-119
16. Chen, H., Pan, Y. X., Wong, E. A., Bloomquist, J. R. and Webb, Jr, K. E. (2002) Molecular cloning and functional expression of a chicken intestinal peptide transporter (cPepT1) in Xenopus oocytes and Chinese hamster ovary cells. J. Nutr. 132, 387-393
17. Chen, H., Pan, Y. X., Wong, E. A. and Webb, Jr, K. E. (2005) Dietary protein level and stage of development affect expression of an intestinal peptide transporter (cPepT1) in chickens. J. Nutr. 135, 193-198
18. Freeman, T. C., Bentsen, B. S., Thwaites, D. T. and Simmons, N. L. (1995) H+ /di-tripeptide transporter (PepT1) expression in the rabbit intestine. Eur. J. Physiol. 430, 394-400
19. Reeves, P. G., Nielsen, F. H. and Fahey, Jr, G. C. (1993) AIN-93 purified diets for laboratory rodents: final report of the American Institute of Nutrition ad hoc writing committee on the reformulation of the AIN-76A rodent diet. J. Nutr. 123, 1939-1951
20. Fernandez, C. D. B., Bellentani, F. F., Fernandes, G. S. A., Perobelli, J. E., Favareto, A. P. A., Nascimento, A. F., Cicogna, A. C. and Kempinas, W. D. G. (2011) Diet-induced obesity in rats leads to a decrease in sperm motility. Reprod. Biol. Endocrinol. 9, 32-42
21. Fernandez-Twinn, D. S. and Ozanne, S. E. (2010) Early life nutrition and metabolic programming. Ann. N.Y. Acad. Sci. 1212, 78-96
22. Barker, D. J. P. (2004) The developmental origins of adult disease. J. Am. Coll. Nutr. 23, 588S-595S
23. Gluckman, P. D., Hanson, M. A. and Beedle, A. S. (2007) Early life events and their consequences for later disease: a life history and evolutionary perspective. Am. J. Hum. Biol. 19, 1-19
24. Warner, M. J. and Ozanne, S. E. (2010) Mechanisms involved in the developmental programming of adulthood disease. Biochem. J. 427, 333-347
25. Taylor, P. D. and Poston, L. (2007) Developmental programming of obesity in mammals. Exp. Physiol. 92, 287-298
26. Alwasel, S. H., Barker, D. J. and Ashton, N. (2012) Prenatal programming of renal salt wasting resets postnatal salt appetite, which drives food intake in the rat. Clin. Sci. 122, 281-288
27. Ferraris, R. P. (2001) Dietary and developmental regulation of intestinal sugar transport. Biochem. J. 360, 265-276
28. Boudry, G., David, E. S., Douard, V., Monteiro, I. M., Le Huërou-Luron, I. and Ferraris, R. P. (2010) Role of intestinal transporters in neonatal nutrition: carbohydrates, proteins, lipids, minerals, and vitamins. J. Pediatr. Gastroenterol. Nutr. 51, 380-401
29. Naruhashi, K., Sai, Y., Tamai, I., Suzuki, N. and Tsuji, A. (2002) PepT1 mRNA expression is induced by starvation and its level correlates with absorptive transport of cefadroxil longitudinally in the rat intestine. Pharm. Res. 19, 1417-1423
30. Daniel, H. (2006) Molecular and integrative physiology of intestinal peptide transport. Annu. Rev. Physiol. 66, 361-384
31. Ihara, T., Tsujikawa, T., Fujiyama, Y. and Bamba, T. (2000) Regulation of Pept1 peptide transporter expression in the rat small intestine under malnourished conditions. Digestion 61, 59-67
32. Armitage, J. A., Khan, I. Y., Taylor, P. D., Nathanielsz, P. W., Peter, W. and Poston, L. (2004) Developmental programming of the metabolic syndrome by maternal nutritional imbalance: how strong is the evidence from experimental models in mammals? J. Physiol. 561, 355-377
33. Pácha, J. (2000) Development of intestinal transport function in mammals. Physiol. Rev. 80, 1633-1667
34. Ferraris, R. P., Cao, Q. X. and Prabhakaram, S. (2001) Chronic but not acute energy restriction increases intestinal nutrient transport in mice. J. Nutr. 131, 770-786
35. Thiesen Jr, A., Drozdowski, L., Iordache, C., Neo, C. C. T., Keelan, M., Clandinin, M. T., Thomson, A. B. R. and Wild, G. (2003) Adaptation following intestinal resection: mechanisms and signals. Best Pract. Res. Clin. Gastroenterol., 17, 981-995
36. Gouyon, F., Caillaud, L., Carriere, V., Klein, C., Dalet, V., Citadelle, D., Kellett, G. L., Thorens, B., Leturque, A. and Brot-Laroche, E. (2003) Simple-sugar meals target GLUT2 at enterocyte apical membranes to improve sugar absorption: a study in GLUT2-null mice. J. Physiol. 552, 823-832
37. Ait-Omar, A., Monteiro-Sepulveda, M., Poitou, C., Le Gall, M., Cotillard, A., Gilet, J., Garbin, K., Houllier, A., Château, D., Lacombe, A. et al. (2011) GLUT2 accumulation in enterocyte apical and intracellular membranes: a study in morbidly obese human subjects and ob/ob and high fat-fed mice. Diabetes 60, 2598-2607
38. Kellett, G. L. and Helliwell, P. A. (2000) The diffusive component of intestinal glucose absorption is mediated by the glucose-induced recruitment of GLUT2 to the brush-border membrane. Biochem. J. 350, 155-162
39. Gouyon, F., Caillaud, L., Carriere, V., Klein, C., Dalet, V., Citadelle, D., Kellett, G. L., Thorens, B., Leturque, A. and Brot-Laroche, E. (2003) Simple-sugar meals target GLUT2 at enterocyte apical membranes to improve sugar absorption: a study in GLUT2-null mice. J. Physiol. 552, 823-832
40. Tobin, V., Le Gall, M., Fioramonti, X., Stolarczyk, E., Blazquez, A. G., Klein, C., Prigent, M., Serradas, P., Cuif, M. H., Magnan, C., Leturque, A. and Brot-Laroche, E. (2008) Insulin internalizes GLUT2 in the enterocytes of healthy but not insulin-resistant mice. Diabetes 57, 555-562
41. Wright, E. M., Loo, D. D. F. and Hirayama, B. A. (2011) Biology of human sodium glucose transporters. Physiol. Rev. 91, 733-794
42. Lang, F. (2004) Surfing the lipid bilayer: how basolateral insulin receptors regulate Na+ channels in the apical cell membrane. Focus on 'real-time three-dimensional imaging of lipid signal transduction: apical membrane insertion of epithelial Na+ channels'. Am. J. Physiol. Cell Physiol. 287, C1539-C1540
43. Lopes, K. L., Furukawa, L. N. S., Oliveira, I. B., Dolnikoff, M. S. and Heimann, J. C. (2008) Perinatal salt restriction: a new pathway to programming adiposity indices in adult female Wistar rats. Life Sci. 82, 728-732
44. Gilbert, E. R., Li, H., Emmerson, D. A., Webb, Jr, K. E. and Wong, E. A. (2007) Developmental regulation of nutrient transporter and enzyme mRNA abundance in the small intestine of broilers. Poult. Sci. 86, 1739-1753
45. Duarte, C. R. A., Vicentini-Paulino, M. L. M., Buratini, Jr, J., Castilho, A. C. S. and Pinheiro, D. F. (2011) Messenger ribonucleic acid abundance of intestinal enzymes and transporters in feed-restricted and refed chickens at different ages. Poult. Sci. 90, 863-868
46. Gal-Garber, O., Mabjeesh, S. J. and Sklan, D. (2000) Partial sequence and expression of the gene for and activity of the glucose transporter in the small intestine of fed, starved and refed chickens. J. Nutr. 130, 2174-2179
47. Hussain, I., Kellett, G. L., Affleck, J., Shepherd, E. J. and Boyd, C. A. R. (2002) Expression and cellular distribution during development of the peptide transporter (PepT1) in the small intestinal epithelium of the rat. Cell Tissue Res. 307, 139-142
48. Rubino, F., Forgione, A., Cummings, D. E., Vix, M., Gnuli, D., Mingrone, G., Castagneto, M. and Marescaux, J. (2006) The mechanism of diabetes control after gastrointestinal bypass surgery reveals a role of the proximal small intestine in the pathophysiology of type 2 diabetes. Ann. Surg. 244, 741-749