Calcium, obesity, and the role of the calcium-sensing receptor

Nutrition Reviews

Volumn 72, Issue 10, 2014, Pages 627-637

  Villarroel, Pia ^a   Villalobos, Elisa ^a   Reyes, Marcela ^a   Cifuentes, Mariana ^a  

^a UNIVERSITY OF CHILE   (Chile)

Author keywords

Adipocyte; Body fat; Body weight; Calcium sensing receptor; CaSR; Dietary calcium; Obesity

Indexed keywords

CALCIUM; CALCIUM SENSING RECEPTOR; FECES LIPID; CALCIUM INTAKE;

ADIPOSE TISSUE; APPETITE; ARTICLE; BODY COMPOSITION; BODY FAT; BODY WEIGHT; CALCIUM INTAKE; ENERGY BALANCE; FAT MASS; HUMAN; INFLAMMATION; NONHUMAN; NUTRITION; OBESITY; OXIDATION; ADMINISTRATION AND DOSAGE; ANIMAL; DIET THERAPY; ENERGY METABOLISM; METABOLISM; PHYSIOLOGY; WEIGHT GAIN;

ADIPOSE TISSUE; ANIMALS; BODY WEIGHT; CALCIUM, DIETARY; ENERGY METABOLISM; HUMANS; INFLAMMATION; OBESITY; RECEPTORS, CALCIUM-SENSING; WEIGHT GAIN;

EID: 84914163548     PISSN: 00296643     EISSN: 17534887     Source Type: Journal    
DOI: 10.1111/nure.12135     Document Type: Article

References (106)

1. del Pozo CH, Calvo RM, Vesperinas-Garcia G, etal. Expression profile in omental and subcutaneous adipose tissue from lean and obese subjects. Repression of lipolytic and lipogenic genes. Obes Surg. 2011;21:633-643.
2. Aronne LJ. Epidemiology, morbidity, and treatment of overweight and obesity. J Clin Psychiatry. 2001;62(Suppl 23):13-22.
3. McArdle MA, Finucane OM, Connaughton RM, etal. Mechanisms of obesity-induced inflammation and insulin resistance: insights into the emerging role of nutritional strategies. Front Endocrinol (Lausanne). 2013;4:52. doi: 10.3389/fendo.2013.00052.
4. Wilson PW, D'Agostino RB, Parise H, etal. Metabolic syndrome as a precursor of cardiovascular disease and type 2 diabetes mellitus. Circulation. 2005;112:3066-3072.
5. Nicklas TA, O'Neil CE, Fulgoni VL III. The role of dairy in meeting the recommendations for shortfall nutrients in the American diet. J Am Coll Nutr. 2009;28(Suppl 1):73S-81S.
6. Kranz S, Lin PJ, Wagstaff DA. Children's dairy intake in the United States: too little, too fat? J Pediatr. 2007;151:642-646.
7. Gilis-Januszewska A, Topor-Madry R, Pajak A. Education and the quality of diet in women and men at age 45-64, in Cracow [in Polish]. Przegl Lek. 2003;60:675-681.
8. Rodríguez-Rodríguez E, Navia Lombán B, López-Sobaler AM, etal. Review and future perspectives on recommended calcium intake. Nutr Hosp. 2010;25:366-374.
9. Pereira DD, Lima RP, de Lima RT, etal. Association between obesity and calcium:phosphorus ratio in the habitual diets of adults in a city of Northeastern Brazil: an epidemiological study. Nutr J. 2013;12:90. doi: 10.1186/1475-2891-12-90.
10. Peterlik M, Kallay E, Cross HS. Calcium nutrition and extracellular calcium sensing: relevance for the pathogenesis of osteoporosis, cancer and cardiovascular diseases. Nutrients. 2013;5:302-327.
11. Ross AC, Manson JE, Abrams SA, etal. The 2011 report on dietary reference intakes for calcium and vitamin D from the Institute of Medicine: what clinicians need to know. J Clin Endocrinol Metab. 2011;96:53-58.
12. Wang L, Manson JE, Sesso HD. Calcium intake and risk of cardiovascular disease: a review of prospective studies and randomized clinical trials. Am J Cardiovasc Drugs. 2012;12:105-116.
13. Burckhardt P. Calcium in the prevention and treatment of osteoporosis [in German]. Ther Umsch. 1991;48:107-112.
14. Zemel MB. Calcium modulation of hypertension and obesity: mechanisms and implications. J Am Coll Nutr. 2001;20(5 Suppl):428S-435S; discussion 440S-442S.
15. Wu K, Willett WC, Fuchs CS, etal. Calcium intake and risk of colon cancer in women and men. J Natl Cancer Inst. 2002;94:437-446.
16. Zemel MB. Nutritional and endocrine modulation of intracellular calcium: implications in obesity, insulin resistance and hypertension. Mol Cell Biochem. 1998;188:129-136.
17. Beydoun MA, Gary TL, Caballero BH, etal. Ethnic differences in dairy and related nutrient consumption among US adults and their association with obesity, central obesity, and the metabolic syndrome. Am J Clin Nutr. 2008;87:1914-1925.
18. He YH, Song Y, Liao XL, etal. The calcium-sensing receptor affects fat accumulation via effects on antilipolytic pathways in adipose tissue of rats fed low-calcium diets. J Nutr. 2011;141:1938-1946.
19. Zemel MB, Shi H, Greer B, etal. Regulation of adiposity by dietary calcium. FASEB J. 2000;14:1132-1138.
20. Davies KM, Heaney RP, Recker RR, etal. Calcium intake and body weight. J Clin Endocrinol Metab. 2000;85:4635-4638.
21. Heaney RP, Davies KM, Barger-Lux MJ. Calcium and weight: clinical studies. J Am Coll Nutr. 2002;21:152S-155S.
22. Teegarden D. Calcium intake and reduction in weight or fat mass. J Nutr. 2003;133:249S-251S.
23. Parikh SJ, Yanovski JA. Calcium intake and adiposity. Am J Clin Nutr. 2003;77:281-287.
24. de Oliveira Freitas DM, Stampini Duarte Martino H, Machado Rocha Ribeiro S, etal. Calcium ingestion and obesity control. Nutr Hosp. 2012;27:1758-1771.
25. Astrup A, Chaput JP, Gilbert JA, etal. Dairy beverages and energy balance. Physiol Behav. 2010;100:67-75.
26. Soares MJ, She-Ping-Delfos WL. Postprandial energy metabolism in the regulation of body weight: is there a mechanistic role for dietary calcium? Nutrients. 2010;2:586-598.
27. Onakpoya IJ, Perry R, Zhang J, etal. Efficacy of calcium supplementation for management of overweight and obesity: systematic review of randomized clinical trials. Nutr Rev. 2011;69:335-343.
28. Barr SI. Increased dairy product or calcium intake: is body weight or composition affected in humans? J Nutr. 2003;133:245S-248S.
29. Barba G, Russo P. Dairy foods, dietary calcium and obesity: a short review of the evidence. Nutr Metab Cardiovasc Dis. 2006;16:445-451.
30. Winzenberg T, Shaw K, Fryer J, etal. Calcium supplements in healthy children do not affect weight gain, height, or body composition. Obesity (Silver Spring). 2007;15:1789-1798.
31. Lanou AJ, Barnard ND. Dairy and weight loss hypothesis: an evaluation of the clinical trials. Nutr Rev. 2008;66:272-279.
32. Chen M, Pan A, Malik VS, etal. Effects of dairy intake on body weight and fat: a meta-analysis of randomized controlled trials. Am J Clin Nutr. 2012;96:735-747.
33. Tremblay A. Dairy and weight loss hypothesis. Nutr Rev. 2008;66:544-545. author reply 546-547.
34. Zemel MB. Dairy and weight loss hypothesis. Nutr Rev. 2008;66:542-543. author reply 546-547.
35. Tremblay A. Dairy food and body fat: when the epidemiologist meets the physiologist. Am J Clin Nutr. 2013;97:447-448.
36. Chen M, Malik VS, Hu FB. Reply to A Tremblay. Am J Clin Nutr. 2013;97:448. doi: 10.3945/ajcn.112.053678.
37. Heaney RP. Guidelines for optimizing design and analysis of clinical studies of nutrient effects. Nutr Rev. 2014;72:48-54.
38. Soares MJ, Chan She Ping-Delfos W, Ghanbari MH. Calcium and vitamin D for obesity: a review of randomized controlled trials. Eur J Clin Nutr. 2011;65:994-1004.
39. Chaput JP, Leblanc C, Perusse L, etal. Risk factors for adult overweight and obesity in the Quebec Family Study: have we been barking up the wrong tree? Obesity (Silver Spring). 2009;17:1964-1970.
40. Heaney RP, Rafferty K. Preponderance of the evidence: an example from the issue of calcium intake and body composition. Nutr Rev. 2009;67:32-39.
41. McCarron DA, Morris CD, Henry HJ, etal. Blood pressure and nutrient intake in the United States. Science. 1984;224:1392-1398.
42. Shi H, Dirienzo D, Zemel MB. Effects of dietary calcium on adipocyte lipid metabolism and body weight regulation in energy-restricted aP2-agouti transgenic mice. FASEB J. 2001;15:291-293.
43. Pereira MA, Jacobs DR, Jr, Van Horn L, etal. Dairy consumption, obesity, and the insulin resistance syndrome in young adults: the CARDIA Study. JAMA. 2002;287:2081-2089.
44. Lovejoy JC, Champagne CM, Smith SR, etal. Ethnic differences in dietary intakes, physical activity, and energy expenditure in middle-aged, premenopausal women: the Healthy Transitions Study. Am J Clin Nutr. 2001;74:90-95.
45. Abreu S, Santos R, Moreira C, etal. Milk intake is inversely related to body mass index and body fat in girls. Eur J Pediatr. 2012;171:1467-1474.
46. dos Santos LC, Martini LA, Cintra Ide P, etal. Relationship between calcium intake and body mass index in adolescents. Arch Latinoam Nutr. 2005;55:345-349.
47. Palacios C, Benedetti P, Fonseca S. Impact of calcium intake on body mass index in Venezuelan adolescents. P R Health Sci J. 2007;26:199-204.
48. Carruth BR, Skinner JD. The role of dietary calcium and other nutrients in moderating body fat in preschool children. Int J Obes Relat Metab Disord. 2001;25:559-566.
49. Kabrnova-Hlavata K, Hainer V, Gojova M, etal. Calcium intake and the outcome of short-term weight management. Physiol Res. 2008;57:237-245.
50. Jones KW, Eller LK, Parnell JA, etal. Effect of a dairy- and calcium-rich diet on weight loss and appetite during energy restriction in overweight and obese adults: a randomized trial. Eur J Clin Nutr. 2013;67:371-376.
51. Yanovski JA, Parikh SJ, Yanoff LB, etal. Effects of calcium supplementation on body weight and adiposity in overweight and obese adults: a randomized trial. Ann Intern Med. 2009;150:821-829.
52. Rajpathak SN, Rimm EB, Rosner B, etal. Calcium and dairy intakes in relation to long-term weight gain in US men. Am J Clin Nutr. 2006;83:559-566.
53. Vergnaud AC, Peneau S, Chat-Yung S, etal. Dairy consumption and 6-y changes in body weight and waist circumference in middle-aged French adults. Am J Clin Nutr. 2008;88:1248-1255.
54. Trowman R, Dumville JC, Hahn S, etal. A systematic review of the effects of calcium supplementation on body weight. Br J Nutr. 2006;95:1033-1038.
55. Berkey CS, Rockett HR, Willett WC, etal. Milk, dairy fat, dietary calcium, and weight gain: a longitudinal study of adolescents. Arch Pediatr Adolesc Med. 2005;159:543-550.
56. Lappe JM. Why blame milk? Arch Pediatr Adolesc Med. 2005;159:1187-1188; author reply 1188.
57. Wennersberg MH, Smedman A, Turpeinen AM, etal. Dairy products and metabolic effects in overweight men and women: results from a 6-mo intervention study. Am J Clin Nutr. 2009;90:960-968.
58. Major GC, Alarie FP, Dore J, etal. Calcium plus vitamin D supplementation and fat mass loss in female very low-calcium consumers: potential link with a calcium-specific appetite control. Br J Nutr. 2009;101:659-663.
59. Torres MR, Sanjuliani AF. Effects of weight loss from a high-calcium energy-reduced diet on biomarkers of inflammatory stress, fibrinolysis, and endothelial function in obese subjects. Nutrition. 2013;29:143-151.
60. Zemel MB, Thompson W, Milstead A, etal. Calcium and dairy acceleration of weight and fat loss during energy restriction in obese adults. Obes Res. 2004;12:582-590.
61. Zemel MB, Richards J, Mathis S, etal. Dairy augmentation of total and central fat loss in obese subjects. Int J Obes (Lond). 2005;29:391-397.
62. Zemel MB, Richards J, Milstead A, etal. Effects of calcium and dairy on body composition and weight loss in African-American adults. Obes Res. 2005;13:1218-1225.
63. Thompson WG, Rostad Holdman N, Janzow DJ, etal. Effect of energy-reduced diets high in dairy products and fiber on weight loss in obese adults. Obes Res. 2005;13:1344-1353.
64. Shapses SA, Heshka S, Heymsfield SB. Effect of calcium supplementation on weight and fat loss in women. J Clin Endocrinol Metab. 2004;89:632-637.
65. Heaney RP. Calcium and obesity: effect size and clinical relevance. Nutr Rev. 2011;69:333-334.
66. Bhattacharyya AK, Thera C, Anderson JT, etal. Dietary calcium and fat. Effect on serum lipids and fecal excretion of cholesterol and its degradation products in man. Am J Clin Nutr. 1969;22:1161-1174.
67. Denke MA, Fox MM, Schulte MC. Short-term dietary calcium fortification increases fecal saturated fat content and reduces serum lipids in men. J Nutr. 1993;123:1047-1053.
68. Boon N, Hul GB, Stegen JH, etal. An intervention study of the effects of calcium intake on faecal fat excretion, energy metabolism and adipose tissue mRNA expression of lipid-metabolism related proteins. Int J Obes (Lond). 2007;31:1704-1712.
69. Jacobsen R, Lorenzen JK, Toubro S, etal. Effect of short-term high dietary calcium intake on 24-h energy expenditure, fat oxidation, and fecal fat excretion. Int J Obes (Lond). 2005;29:292-301.
70. Bendsen NT, Hother AL, Jensen SK, etal. Effect of dairy calcium on fecal fat excretion: a randomized crossover trial. Int J Obes (Lond). 2008;32:1816-1824.
71. Christensen R, Lorenzen JK, Svith CR, etal. Effect of calcium from dairy and dietary supplements on faecal fat excretion: a meta-analysis of randomized controlled trials. Obes Rev. 2009;10:475-486.
72. Hill JO, Wyatt HR, Reed GW, etal. Obesity and the environment: where do we go from here? Science. 2003;299:853-855.
73. Yuangklang C, Wensing T, Lankhorst A, etal. Cholate and deoxycholate counteract the calcium-induced lowering of fat digestion in rats. J Anim Physiol Anim Nutr (Berl). 2005;89:337-341.
74. Gilbert JA, Joanisse DR, Chaput JP, etal. Milk supplementation facilitates appetite control in obese women during weight loss: a randomised, single-blind, placebo-controlled trial. Br J Nutr. 2011;105:133-143.
75. Ping-Delfos WC, Soares M. Diet induced thermogenesis, fat oxidation and food intake following sequential meals: influence of calcium and vitamin D. Clin Nutr. 2011;30:376-383.
76. Lorenzen JK, Nielsen S, Holst JJ, etal. Effect of dairy calcium or supplementary calcium intake on postprandial fat metabolism, appetite, and subsequent energy intake. Am J Clin Nutr. 2007;85:678-687.
77. Tordoff MG. Calcium: taste, intake, and appetite. Physiol Rev. 2001;81:1567-1597.
78. Hall WL, Millward DJ, Long SJ, etal. Casein and whey exert different effects on plasma amino acid profiles, gastrointestinal hormone secretion and appetite. Br J Nutr. 2003;89:239-248.
79. Xue B, Greenberg AG, Kraemer FB, etal. Mechanism of intracellular calcium ([Ca2+]i) inhibition of lipolysis in human adipocytes. FASEB J. 2001;15:2527-2529.
80. Melanson EL, Sharp TA, Schneider J, etal. Relation between calcium intake and fat oxidation in adult humans. Int J Obes Relat Metab Disord. 2003;27:196-203.
81. Melanson EL, Donahoo WT, Dong F, etal. Effect of low- and high-calcium dairy-based diets on macronutrient oxidation in humans. Obes Res. 2005;13:2102-2112.
82. Gonzalez JT, Rumbold PL, Stevenson EJ. Effect of calcium intake on fat oxidation in adults: a meta-analysis of randomized, controlled trials. Obes Rev. 2012;13:848-857.
83. Fruhbeck G, Gomez-Ambrosi J, Muruzabal FJ, etal. The adipocyte: a model for integration of endocrine and metabolic signaling in energy metabolism regulation. Am J Physiol Endocrinol Metab. 2001;280:E827-E847.
84. Schaffler A, Scholmerich J. Innate immunity and adipose tissue biology. Trends Immunol. 2010;31:228-235.
85. Ouchi N, Parker JL, Lugus JJ, etal. Adipokines in inflammation and metabolic disease. Nat Rev Immunol. 2011;11:85-97.
86. Kloting N, Fasshauer M, Dietrich A, etal. Insulin-sensitive obesity. Am J Physiol Endocrinol Metab. 2010;299:E506-E515.
87. Lind L, Carlstedt F, Rastad J, etal. Hypocalcemia and parathyroid hormone secretion in critically ill patients. Crit Care Med. 2000;28:93-99.
88. Panagiotakos DB, Pitsavos CH, Zampelas AD, etal. Dairy products consumption is associated with decreased levels of inflammatory markers related to cardiovascular disease in apparently healthy adults: the ATTICA study. J Am Coll Nutr. 2011;29:357-364.
89. Sun X, Zemel MB. Calcium and 1, 25-dihydroxyvitamin D3 regulation of adipokine expression. Obesity (Silver Spring). 2007;15:340-348.
90. Zemel MB, Sun X, Sobhani T, etal. Effects of dairy compared with soy on oxidative and inflammatory stress in overweight and obese subjects. Am J Clin Nutr. 2010;91:16-22.
91. Brown EM, Gamba G, Riccardi D, etal. Cloning and characterization of an extracellular Ca(2+)-sensing receptor from bovine parathyroid. Nature. 1993;366:575-580.
92. Armato U. The calcium-sensing receptor: pathophysiology and pharmacological modulation. Curr Pharm Biotechnol. 2009;10:268-269.
93. Cifuentes M, Albala C, Rojas C. Calcium-sensing receptor expression in human adipocytes. Endocrinology. 2005;146:2176-2179.
94. Breitwieser GE. Minireview: the intimate link between calcium sensing receptor trafficking and signaling: implications for disorders of calcium homeostasis. Mol Endocrinol. 2012;26:1482-1495.
95. Canaff L, Hendy GN. Calcium-sensing receptor gene transcription is up-regulated by the proinflammatory cytokine, interleukin-1β. Role of the NF-κB pathway and κB elements. J Biol Chem. 2005;280:14177-14188.
96. Cifuentes M, Fuentes C, Mattar P, etal. Obesity-associated proinflammatory cytokines increase calcium sensing receptor (CaSR) protein expression in primary human adipocytes and LS14 human adipose cell line. Arch Biochem Biophys. 2010;500:151-156.
97. Cifuentes M, Fuentes C, Tobar N, etal. Calcium sensing receptor activation elevates proinflammatory factor expression in human adipose cells and adipose tissue. Mol Cell Endocrinol. 2012;361:24-30.
98. Hultin H, Edfeldt K, Sundbom M, etal. Left-shifted relation between calcium and parathyroid hormone in obesity. J Clin Endocrinol Metab. 2010;95:3973-3981.
99. He Y, Perry B, Bi M, etal. Allosteric regulation of the calcium-sensing receptor in obese individuals. Int J Mol Med. 2013;32:511-518.
100. Nemeth EF, Shoback D. Calcimimetic and calcilytic drugs for treating bone and mineral-related disorders. Best Pract Res Clin Endocrinol Metab. 2013;27:373-384.
101. Nakagawa K, Perez EC, Oh J, etal. Cinacalcet does not affect longitudinal growth but increases body weight gain in experimental uraemia. Nephrol Dial Transplant. 2008;23:2761-2767.
102. Cifuentes M, Albala C, Rojas CV. Differences in lipogenesis and lipolysis in obese and non-obese adult human adipocytes. Biol Res. 2008;41:197-204.
103. He Y, Zhang H, Teng J, etal. Involvement of calcium-sensing receptor in inhibition of lipolysis through intracellular cAMP and calcium pathways in human adipocytes. Biochem Biophys Res Commun. 2011;404:393-399.
104. He YH, He Y, Liao XL, etal. The calcium-sensing receptor promotes adipocyte differentiation and adipogenesis through PPARγ pathway. Mol Cell Biochem. 2012;361:321-328.
105. Brown AJ, Zhong M, Finch J, etal. Rat calcium-sensing receptor is regulated by vitamin D but not by calcium. Am J Physiol. 1996;270(3 Pt 2):F454-F460.
106. Canaff L, Hendy GN. Human calcium-sensing receptor gene. Vitamin D response elements in promoters P1 and P2 confer transcriptional responsiveness to 1, 25-dihydroxyvitamin D. J Biol Chem. 2002;277:30337-30350.