Dietary sodium suppresses digestive efficiency via the renin-angiotensin system

Scientific Reports

Volumn 5, Issue , 2015, Pages

  Weidemann, Benjamin J ^a   Voong, Susan ^a   Morales Santiago, Fabiola I ^a   Kahn, Michael Z ^a   Ni, Jonathan ^a   Littlejohn, Nicole K ^a   Claflin, Kristin E ^a   Burnett, Colin M L ^a   Pearson, Nicole A ^a   Lutter, Michael L ^a,b   Grobe, Justin L ^a,b  

^a UNIVERSITY OF IOWA   (United States)

^b UNIVERSITY OF IOWA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

1 (4 DIMETHYLAMINO 3 METHYLBENZYL) 5 DIPHENYLACETYL 4,5,6,7 TETRAHYDRO 1H IMIDAZO[4,5 C]PYRIDINE 6 CARBOXYLIC ACID; ANGIOTENSIN 2 RECEPTOR; FAT INTAKE; IMIDAZOLE DERIVATIVE; LOSARTAN; PYRIDINE DERIVATIVE; SALT INTAKE;

ANIMAL; DIGESTION; DRUG EFFECTS; FAT INTAKE; GENE DELETION; GENETICS; INTESTINE ABSORPTION; MALE; METABOLISM; MOUSE; PHARMACOLOGY; RENIN ANGIOTENSIN ALDOSTERONE SYSTEM; SALT INTAKE;

ANIMALS; DIETARY FATS; DIGESTION; GENE DELETION; IMIDAZOLES; INTESTINAL ABSORPTION; LOSARTAN; MALE; MICE; PYRIDINES; RECEPTOR, ANGIOTENSIN, TYPE 2; RENIN-ANGIOTENSIN SYSTEM; SODIUM CHLORIDE, DIETARY;

EID: 84931281934     PISSN: None     EISSN: 20452322     Source Type: Journal    
DOI: 10.1038/srep11123     Document Type: Article

References (76)

1. Hoffmann, I. S. , Cubeddu, L. X. Salt and the metabolic syndrome. Nutrition, metabolism, and cardiovascular diseases : NMCD 19, 123-128, doi:10.1016/j.numecd.2008.02.011 (2009).
2. Donovan, D. S., Solomon, C. G., Seely, E. W., Williams, G. H. , Simonson, D. C. Effect of sodium intake on insulin sensitivity. The American journal of physiology 264, E730-E734 (1993).
3. Graudal, N., Jurgens, G., Baslund, B. , Alderman, M. H. Compared With Usual Sodium Intake, Low-and Excessive-Sodium Diets Are Associated With Increased Mortality: A Meta-Analysis. American journal of hypertension, doi:10.1093/ajh/hpu028 (2014).
4. Bray, G. A. , Popkin, B. M. Dietary fat intake does affect obesity! The American journal of clinical nutrition 68, 1157-1173 (1998).
5. Rosini, T. C., Silva, A. S. , Moraes, C. Diet-induced obesity: rodent model for the study of obesity-related disorders. Revista da Associacao Medica Brasileira (1992) 58, 383-387 (2012).
6. Marantz, P. R., Bird, E. D. , Alderman, M. H. A call for higher standards of evidence for dietary guidelines. American journal of preventive medicine 34, 234-240, doi:10.1016/j.amepre.2007.11.017 (2008).
7. Garber, A. K. , Lustig, R. H. Is fast food addictive? Current drug abuse reviews 4, 146-162 (2011).
8. Mejean, C. et al. Association between intake of nutrients and food groups and liking for fat (The Nutrinet-Sante Study). Appetite 78, 147-155, doi:10.1016/j.appet.2014.03.017 (2014).
9. Grobe, J. L., Rahmouni, K., Liu, X. , Sigmund, C. D. Metabolic rate regulation by the renin-angiotensin system: brain vs. body. Pflugers Archiv : European journal of physiology 465, 167-175, doi:10.1007/s00424-012-1096-9 (2013).
10. Mathai, M. L., Chen, N., Cornall, L. , Weisinger, R. S. The role of angiotensin in obesity and metabolic disease. Endocrine, metabolic & immune disorders drug targets 11, 198-205 (2011).
11. Faloia, E. et al. Comparison of circulating and local adipose tissue renin-angiotensin system in normotensive and hypertensive obese subjects. Journal of endocrinological investigation 25, 309-314 (2002).
12. Giacchetti, G. et al. Overexpression of the renin-angiotensin system in human visceral adipose tissue in normal and overweight subjects. American journal of hypertension 15, 381-388 (2002).
13. Massiera, F. et al. Adipose angiotensinogen is involved in adipose tissue growth and blood pressure regulation. FASEB journal : official publication of the Federation of American Societies for Experimental Biology 15, 2727-2729, doi:10.1096/fj.01-0457fje (2001).
14. Bloem, L. J., Manatunga, A. K., Tewksbury, D. A. , Pratt, J. H. The serum angiotensinogen concentration and variants of the angiotensinogen gene in white and black children. The Journal of clinical investigation 95, 948-953, doi:10.1172/JCI117803 (1995).
15. Cooper, R. et al. ACE, angiotensinogen and obesity: a potential pathway leading to hypertension. Journal of human hypertension 11, 107-111 (1997).
16. Engeli, S. et al. Weight loss and the renin-angiotensin-aldosterone system. Hypertension 45, 356-362, doi:10.1161/01. HYP.0000154361.47683.d3 (2005).
17. Messerli, F. H., Nunez, B. D., Ventura, H. O. , Snyder, D. W. Overweight and sudden death. Increased ventricular ectopy in cardiopathy of obesity. Archives of internal medicine 147, 1725-1728 (1987).
18. Alligier, M. et al. Subcutaneous adipose tissue remodeling during the initial phase of weight gain induced by overfeeding in humans. The Journal of clinical endocrinology and metabolism 97, E183-E192, doi:10.1210/jc.2011-2314 (2012).
19. Wang, P. et al. Circulating ACE is a predictor of weight loss maintenance not only in overweight and obese women, but also in men. International journal of obesity (2005) 36, 1545-1551, doi:10.1038/ijo.2011.278 (2012).
20. Takahashi, N. et al. Increased energy expenditure, dietary fat wasting, and resistance to diet-induced obesity in mice lacking renin. Cell metabolism 6, 506-512, doi:10.1016/j.cmet.2007.10.011 (2007).
21. Stucchi, P., Cano, V., Ruiz-Gayo, M. , Fernandez-Alfonso, M. S. Aliskiren reduces body-weight gain, adiposity and plasma leptin during diet-induced obesity. British journal of pharmacology 158, 771-778, doi:10.1111/j.1476-5381.2009.00355.x (2009).
22. Chou, C. L., Lai, Y. H., Lin, T. Y., Lee, T. J. , Fang, T. C. Aliskiren prevents and ameliorates metabolic syndrome in fructose-fed rats. Archives of medical science : AMS 7, 882-888, doi:10.5114/aoms.2011.25566 (2011).
23. Massiera, F. et al. Angiotensinogen-deficient mice exhibit impairment of diet-induced weight gain with alteration in adipose tissue development and increased locomotor activity. Endocrinology 142, 5220-5225, doi:10.1210/endo.142.12.8556 (2001).
24. Jayasooriya, A. P. et al. Mice lacking angiotensin-converting enzyme have increased energy expenditure, with reduced fat mass and improved glucose clearance. Proceedings of the National Academy of Sciences of the United States of America 105, 6531-6536, doi:10.1073/pnas.0802690105 (2008).
25. Mathai, M. L., Naik, S., Sinclair, A. J., Weisinger, H. S. , Weisinger, R. S. Selective reduction in body fat mass and plasma leptin induced by angiotensin-converting enzyme inhibition in rats. International journal of obesity (2005) 32, 1576-1584, doi:10.1038/ijo.2008.126 (2008).
26. Weisinger, R. S. et al. Angiotensin converting enzyme inhibition lowers body weight and improves glucose tolerance in C57BL/6J mice maintained on a high fat diet. Physiology & behavior 98, 192-197, doi:10.1016/j.physbeh.2009.05.009 (2009).
27. Santos, E. L. et al. Effect of angiotensin converting enzyme inhibitor enalapril on body weight and composition in young rats. International immunopharmacology 8, 247-253, doi:10.1016/j.intimp.2007.07.021 (2008).
28. Carter, C. S. et al. Angiotensin-converting enzyme inhibition, body composition, and physical performance in aged rats. The journals of gerontology. Series A, Biological sciences and medical sciences 59, 416-423 (2004).
29. de Kloet, A. D. et al. Obesity induces neuroinflammation mediated by altered expression of the renin-angiotensin system in mouse forebrain nuclei. Physiology & behavior, doi:10.1016/j.physbeh.2014.01.016 (2014).
30. de Kloet, A. D. et al. Angiotensin type 1a receptors in the paraventricular nucleus of the hypothalamus protect against dietinduced obesity. The Journal of neuroscience : the official journal of the Society for Neuroscience 33, 4825-4833, doi:10.1523/jneurosci.3806-12.2013 (2013).
31. Burnett, C. M. , Grobe, J. L. Direct calorimetry identifies deficiencies in respirometry for the determination of resting metabolic rate in C57Bl/6 and FVB mice. American journal of physiology. Endocrinology and metabolism 305, E916-E924, doi:10.1152/ajpendo.00387.2013 (2013).
32. Hilzendeger, A. M. et al. A brain leptin-renin angiotensin system interaction in the regulation of sympathetic nerve activity. American journal of physiology. Heart and circulatory physiology 303, H197-H206, doi:10.1152/ajpheart.00974.2011 (2012).
33. Grobe, J. L. et al. Angiotensinergic signaling in the brain mediates metabolic effects of deoxycorticosterone (DOCA)-salt in C57 mice. Hypertension 57, 600-607, doi:10.1161/hypertensionaha.110.165829 (2011).
34. Grobe, J. L. et al. The brain Renin-angiotensin system controls divergent efferent mechanisms to regulate fluid and energy balance. Cell metabolism 12, 431-442, doi:10.1016/j.cmet.2010.09.011 (2010).
35. Alderman, M. H. et al. Association of the renin-sodium profile with the risk of myocardial infarction in patients with hypertension. The New England journal of medicine 324, 1098-1104, doi:10.1056/nejm199104183241605 (1991).
36. Dahl, L. K. Possible role of salt intake in the development of essential hypertension. 1960. International journal of epidemiology 34, 967-972; discussion 972-964, 975-968, doi:10.1093/ije/dyh317 (2005).
37. Bingham, S., McNeil, N. I. , Cummings, J. H. The diet of individuals: a study of a randomly-chosen cross section of British adults in a Cambridgeshire village. The British journal of nutrition 45, 23-35 (1981).
38. Elliott, P. et al. The INTERSALT study: main results, conclusions and some implications. Clinical and experimental hypertension. Part A, Theory and practice 11, 1025-1034 (1989).
39. Elliott, P. , Brown, I. Sodium Intakes Around the World. (World Health Organization, 2007).
40. O'Donnell, M. et al. Urinary sodium and potassium excretion, mortality, and cardiovascular events. The New England journal of medicine 371, 612-623, doi:10.1056/NEJMoa1311889 (2014).
41. McDonald's USA. Nutrition Information, accessed 12/01/2014, (2014).
42. Hussain, Y., Guzelhan, C., Odink, J., van der Beek, E. J. , Hartmann, D. Comparison of the inhibition of dietary fat absorption by full versus divided doses of orlistat. Journal of clinical pharmacology 34, 1121-1125 (1994).
43. Zhi, J. et al. Retrospective population-based analysis of the dose-response (fecal fat excretion) relationship of orlistat in normal and obese volunteers. Clinical pharmacology and therapeutics 56, 82-85 (1994).
44. Garg, M. et al. Review article: the pathophysiological roles of the renin-angiotensin system in the gastrointestinal tract. Alimentary pharmacology & therapeutics 35, 414-428, doi:10.1111/j.1365-2036.2011.04971.x (2012).
45. Seo, M. S., Fukamizu, A., Saito, T. , Murakami, K. Identification of a previously unrecognized production site of human renin. Biochimica et biophysica acta 1129, 87-89 (1991).
46. Hirasawa, K., Sato, Y., Hosoda, Y., Yamamoto, T. , Hanai, H. Immunohistochemical localization of angiotensin II receptor and local renin-angiotensin system in human colonic mucosa. The journal of histochemistry and cytochemistry : official journal of the Histochemistry Society 50, 275-282 (2002).
47. Bruneval, P. et al. Angiotensin I converting enzyme in human intestine and kidney. Ultrastructural immunohistochemical localization. Histochemistry 85, 73-80 (1986).
48. Hamming, I. et al. Tissue distribution of ACE2 protein, the functional receptor for SARS coronavirus. A first step in understanding SARS pathogenesis. The Journal of pathology 203, 631-637, doi:10.1002/path.1570 (2004).
49. Harmer, D., Gilbert, M., Borman, R. , Clark, K. L. Quantitative mRNA expression profiling of ACE 2, a novel homologue of angiotensin converting enzyme. FEBS letters 532, 107-110 (2002).
50. Tipnis, S. R. et al. A human homolog of angiotensin-converting enzyme. Cloning and functional expression as a captoprilinsensitive carboxypeptidase. The Journal of biological chemistry 275, 33238-33243, doi:10.1074/jbc.M002615200 (2000).
51. Kubota, E. et al. Differential tissue and enzyme inhibitory effects of the vasopeptidase inhibitor omapatrilat in the rat. Clinical science (London, England : 1979) 105, 339-345, doi:10.1042/cs20030097 (2003).
52. Shorning, B. Y. et al. Intestinal renin-angiotensin system is stimulated after deletion of Lkb1. Gut 61, 202-213, doi:10.1136/gutjnl-2011-300046 (2012).
53. Ewert, S. et al. Angiotensin II induced contraction of rat and human small intestinal wall musculature in vitro. Acta physiologica (Oxford, England) 188, 33-40, doi:10.1111/j.1748-1716.2006.01600.x (2006).
54. Spak, E., Casselbrant, A., Olbers, T., Lonroth, H. , Fandriks, L. Angiotensin II-induced contractions in human jejunal wall musculature in vitro. Acta physiologica (Oxford, England) 193, 181-190, doi:10.1111/j.1748-1716.2007.01826.x (2008).
55. Hallersund, P., Elfvin, A., Helander, H. F. , Fandriks, L. The expression of renin-angiotensin system components in the human gastric mucosa. Journal of the renin-angiotensin-aldosterone system : JRAAS 12, 54-64, doi:10.1177/1470320310379066 (2011).
56. Casselbrant, A. et al. Angiotensin II receptors are expressed and functional in human esophageal mucosa. American journal of physiology. Gastrointestinal and liver physiology 297, G1019-G1027, doi:10.1152/ajpgi.00255.2009 (2009).
57. Casselbrant, A. et al. Actions by angiotensin II on esophageal contractility in humans. Gastroenterology 132, 249-260, doi:10.1053/j.gastro.2006.11.010 (2007).
58. Wong, T. P., Debnam, E. S. , Leung, P. S. Involvement of an enterocyte renin-angiotensin system in the local control of SGLT1-dependent glucose uptake across the rat small intestinal brush border membrane. The Journal of physiology 584, 613-623, doi:10.1113/jphysiol.2007.138578 (2007).
59. Campbell, D. J. , Habener, J. F. Angiotensinogen gene is expressed and differentially regulated in multiple tissues of the rat. The Journal of clinical investigation 78, 31-39, doi:10.1172/jci112566 (1986).
60. Nagata, S., Kato, J., Kuwasako, K. , Kitamura, K. Plasma and tissue levels of proangiotensin-12 and components of the renin-angiotensin system (RAS) following low-or high-salt feeding in rats. Peptides 31, 889-892, doi:10.1016/j.peptides.2010.02.008 (2010).
61. Sun, L. et al. Angiotensin II induces apoptosis in intestinal epithelial cells through the AT2 receptor, GATA-6 and the Bax pathway. Biochemical and biophysical research communications 424, 663-668, doi:10.1016/j.bbrc.2012.07.003 (2012).
62. Ewert, S. et al. The angiotensin II receptor type 2 agonist CGP 42112A stimulates NO production in the porcine jejunal mucosa. BMC pharmacology 3, 2 (2003).
63. Jin, X. H., Wang, Z. Q., Siragy, H. M., Guerrant, R. L. , Carey, R. M. Regulation of jejunal sodium and water absorption by angiotensin subtype receptors. The American journal of physiology 275, R515-R523 (1998).
64. Tsang, S. W., Cheng, C. H. , Leung, P. S. The role of the pancreatic renin-angiotensin system in acinar digestive enzyme secretion and in acute pancreatitis. Regulatory peptides 119, 213-219, doi:10.1016/j.regpep.2004.02.003 (2004).
65. Itaya, Y., Suzuki, H., Matsukawa, S., Kondo, K. , Saruta, T. Central renin-angiotensin system and the pathogenesis of DOCA-salt hypertension in rats. The American journal of physiology 251, H261-H268 (1986).
66. Kubo, T., Yamaguchi, H., Tsujimura, M., Hagiwara, Y. , Fukumori, R. Blockade of angiotensin receptors in the anterior hypothalamic preoptic area lowers blood pressure in DOCA-salt hypertensive rats. Hypertension research : official journal of the Japanese Society of Hypertension 23, 109-118 (2000).
67. Park, C. G. , Leenen, F. H. Effects of centrally administered losartan on deoxycorticosterone-salt hypertension rats. Journal of Korean medical science 16, 553-557 (2001).
68. Kaiyala, K. J. , Ramsay, D. S. Direct animal calorimetry, the underused gold standard for quantifying the fire of life. Comparative biochemistry and physiology. Part A, Molecular & integrative physiology 158, 252-264, doi:10.1016/j.cbpa.2010.04.013 (2011).
69. Walsberg, G. E. , Hoffman, T. C. Direct calorimetry reveals large errors in respirometric estimates of energy expenditure. The Journal of experimental biology 208, 1035-1043, doi:10.1242/jeb.01477 (2005).
70. Burnett, C. M. , Grobe, J. L. Dietary effects on resting metabolic rate in C57BL/6 mice are differentially detected by indirect (O2/CO2 respirometry) and direct calorimetry. Molecular metabolism 3, 460-464, doi:10.1016/j.molmet.2014.03.003 (2014).
71. National Research Council. Guide for the Care and Use of Laboratory Animals. 8th edn, (National Acadamies Press, 2011).
72. Lusk, G. The elements of the science of nutrition. 4th edition edn, (W.B. Saunders Company, 1928).
73. Littlejohn, N. K. et al. Hypertension in mice with transgenic activation of the brain renin-angiotensin system is vasopressin dependent. American journal of physiology. Regulatory, integrative and comparative physiology 304, R818-R828, doi:10.1152/ajpregu.00082.2013 (2013).
74. Li, H. et al. Renal proximal tubule angiotensin AT1A receptors regulate blood pressure. American journal of physiology. Regulatory, integrative and comparative physiology 301, R1067-R1077, doi:10.1152/ajpregu.00124.2011 (2011).
75. Grobe, J. L., Xu, D. , Sigmund, C. D. An intracellular renin-angiotensin system in neurons: fact, hypothesis, or fantasy. Physiology (Bethesda, Md.) 23, 187-193, doi:10.1152/physiol.00002.2008 (2008).
76. Livak, K. J. , Schmittgen, T. D. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. Methods (San Diego, Calif.) 25, 402-408, doi:10.1006/meth.2001.1262 (2001).