Effect of dietary lipid structure in early postnatal life on mouse adipose tissue development and function in adulthood

British Journal of Nutrition

Volumn 111, Issue 2, 2014, Pages 215-226

  Oosting, Annemarie ^a   Van Vlies, Naomi ^b,e   Kegler, Diane ^a   Schipper, Lidewij ^a   Abrahamse Berkeveld, Marieke ^a   Ringler, Silvia ^a   Verkade, Henkjan J ^c   Van Der Beek, Eline M ^d  

^a DANONE RESEARCH   (Netherlands)

^b UTRECHT UNIVERSITY   (Netherlands)

^c UNIVERSITY OF GRONINGEN   (Netherlands)

^d Danone Research Centre for Specialised Nutrition   (Singapore)

^e UNIVERSITY OF AMSTERDAM   (Netherlands)

Author keywords

Dietary lipids; Infant nutrition; Nutritional programming; Obesity prevention

Indexed keywords

CCAAT ENHANCER BINDING PROTEIN; LIPID; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA; RETINOID X RECEPTOR; RETINOID X RECEPTOR ALPHA; TRANSCRIPTION FACTOR; LEPTIN; STEROL REGULATORY ELEMENT BINDING PROTEIN 1C;

ADIPOSE TISSUE; ADOLESCENT; ADULT; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; ARTIFICIAL MILK; BIOACCUMULATION; BODY COMPOSITION; BREAST MILK; CELL COUNT; CELL DIFFERENTIATION; CELL SIZE; CONTROLLED STUDY; DIETARY INTAKE; DISEASE CONTROL; DUAL ENERGY X RAY ABSORPTIOMETRY; FEMALE; FUNCTIONAL ASSESSMENT; GENE EXPRESSION; GROWTH CURVE; LIPOGENESIS; MALE; MOLECULAR DYNAMICS; MOUSE; NONHUMAN; OBESITY; PERINATAL PERIOD; PROTEIN EXPRESSION; RISK ASSESSMENT; RISK FACTOR; TISSUE GROWTH; ADIPOCYTE; ADIPOGENESIS; ADULTHOOD; CEBP ALPHA GENE; CEBP BETA GENE; CEBP DELTA GENE; DISEASE PREDISPOSITION; FAT INTAKE; GENE; HYPERTROPHY; LEPTIN GENE; LIPID STORAGE; METABOLISM; NEWBORN; PPAR GAMMA GENE; RXR ALPHA GENE; SREBP1C GENE; WHITE ADIPOSE TISSUE; ANIMAL; ANIMAL DISEASE; ANIMAL FOOD; C57BL MOUSE; CHEMISTRY; CYTOLOGY; DIET; DRUG EFFECT; EPIDIDYMIS; GENE EXPRESSION REGULATION; GROWTH, DEVELOPMENT AND AGING; HUMAN; INFANT; RANDOMIZATION;

ADIPOSE TISSUE; ANIMAL FEED; ANIMALS; DIET; DIETARY FATS; EPIDIDYMIS; GENE EXPRESSION REGULATION; HUMANS; INFANT; INFANT FORMULA; LIPOGENESIS; MALE; MICE; MICE, INBRED C57BL; RANDOM ALLOCATION;

EID: 84896626490     PISSN: 00071145     EISSN: 14752662     Source Type: Journal    
DOI: 10.1017/S0007114513002201     Document Type: Article

References (60)

1. Budge H, Sebert S, Sharkey D, et al. (2009) Session on 'obesity'. Adipose tissue development, nutrition in early life and its impact on later obesity. Proc Nutr Soc 68, 321-326.
2. Knittle JL, Timmers K, Ginsberg-Fellner F, et al. (1979) The growth of adipose tissue in children and adolescents. Cross-sectional and longitudinal studies of adipose cell number and size. J Clin Invest 63, 239-246.
3. Spalding KL, Arner E, Westermark PO, et al. (2008) Dynamics of fat cell turnover in humans. Nature 453, 783-787.
4. Gruen R, Kava R & Greenwood MR (1980) Development of basal lipolysis and fat cell size in the epididymal fat pad of normal rats. Metabolism 29, 246-253.
5. Hubbard RW & Matthew WT (1971) Growth and lipolysis of rat adipose tissue: effect of age, body weight, and food intake. J Lipid Res 12, 286-293.
6. Greenwood MR & Hirsch J (1974) Postnatal development of adipocyte cellularity in the normal rat. J Lipid Res 15, 474-483.
7. Hemmeryckx B, Loeckx D, Dresselaers T, et al. (2010) Age-associated adaptations in murine adipose tissues. Endocr J 57, 925-930.
8. Obst BE, Schemmel RA, Czajka-Narins D, et al. (1981) Adipocyte size and number in dietary obesity resistant and susceptible rats. Am J Physiol 240, E47-E53.
9. Bourgeois F, Alexiu A & Lemonnier D (1983) Dietary-induced obesity: effect of dietary fats on adipose tissue cellularity in mice. Br J Nutr 49, 17-26.
10. DiGirolamo M, Fine JB, Tagra K, et al. (1998) Qualitative regional differences in adipose tissue growth and cellularity in male Wistar rats fed ad libitum. Am J Physiol 274, R1460-R1467.
11. Darlington GJ, Ross SE & MacDougald OA (1998) The role of C/EBP genes in adipocyte differentiation. J Biol Chem 273, 30057-30060.
12. Berger J & Moller DE (2002) The mechanisms of action of PPARs. Annu Rev Med 53, 409-435.
13. Rosen ED, Sarraf P, Troy AE, et al. (1999) PPAR gamma is required for the differentiation of adipose tissue in vivo and in vitro. Mol Cell 4, 611-617.
14. Tamori Y, Masugi J, Nishino N, et al. (2002) Role of peroxi-some proliferator-activated receptor-gamma in maintenance of the characteristics of mature 3T3-L1 adipocytes. Diabetes 51, 2045-2055.
15. Waku T, Shiraki T, Oyama T, et al. (2009) Structural insight into PPAR gamma activation through covalent modification with endogenous fatty acids. J Mol Biol 385, 188-199.
16. Desai M, Guang H, Ferelli M, et al. (2008) Programmed upregulation of adipogenic transcription factors in intrauter-ine growth-restricted offspring. Reprod Sci 15, 785-796.
17. Desai M & Ross MG (2011) Fetal programming of adipose tissue: effects of intrauterine growth restriction and maternal obesity/high-fat diet. Semin Reprod Med 29, 237-245.
18. Verier C, Meirhaeghe A, Bokor S, et al. (2010) Breast-feeding modulates the influence of the peroxisome proliferator-activated receptor-gamma (PPARG2) Pro12Ala polymorphism on adiposity in adolescents: The Healthy Lifestyle in Europe by Nutrition in Adolescence (HELENA) cross-sectional study. Diabetes Care 33, 190-196.
19. Agostoni C (2005) Ghrelin, leptin and the neurometabolic axis of breastfed and formula-fed infants. Acta Paediatr 94, 523-525.
20. Michalski MC (2007) On the supposed influence of milk homogenization on the risk of CVD, diabetes and allergy. Br J Nutr 97, 598-610.
21. Oosting A, Kegler D, Wopereis HJ, et al. (2012) Size and phospholipid coating of lipid droplets in the diet of young mice modify body fat accumulation in adulthood. Pediatr Res 72, 362-369.
22. van Baalen A, van der Beek E, Beermann C, et al. (2010) Nutritional Compositions with Lipid Globules with a Core Comprising Vegetable Lipids and a Coating Comprising Phospholipids or Polar Lipids [NV NUTRICIA, editor]. WO patent: NUTRICIA, N.V.
23. Reeves PG, Nielsen FH & Fahey GC (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.
24. Golde WT, Gollobin P & Rodriguez LL (2005) A rapid, simple, and humane method for submandibular bleeding of mice using a lancet. Lab Anim (NY) 34, 39-43.
25. Di Girolamo M & Fine JB (2001) Cellularity measurements. Methods Mol Biol 155, 65-75.
26. Folch J, Lees M & Sloane Stanley GH (1957) A simple method for the isolation and purification of total lipides from animal tissues. J Biol Chem 226, 497-509.
27. de Jonge HJ, Fehrmann RS, de Bont ES, et al. (2007) Evidence based selection of housekeeping genes. PLoS One 2, e898.
28. Knittle JL & Hirsch J (1968) Effect of early nutrition on the development of rat epididymal fat pads: cellularity and metabolism. J Clin Invest 47, 2091-2098.
29. Wahlen K, Sjolin E & Lofgren P (2011) Role of fat cell size for plasma leptin in a large population based sample. Exp Clin Endocrinol Diabetes 119, 291-294.
30. Eberle D, Hegarty B, Bossard P, et al. (2004) SREBP transcription factors: master regulators of lipid homeostasis. Biochimie 86, 839-848.
31. Palou M, Priego T, Sanchez J, et al. (2008) Sequential changes in the expression of genes involved in lipid metabolism in adipose tissue and liver in response to fasting. Pflugers Arch 456, 825-836.
32. Morgan K, Uyuni A, Nandgiri G, et al. (2008) Altered expression of transcription factors and genes regulating lipogenesis in liver and adipose tissue of mice with high fat diet-induced obesity and nonalcoholic fatty liver disease. Eur J Gastroenterol Hepatol 20, 843-854.
33. Palou M, Sanchez J, Priego T, et al. (2010) Regional differences in the expression of genes involved in lipid metabolism in adipose tissue in response to short-and medium-term fasting and refeeding. J Nutr Biochem 21, 23-33.
34. Kersten S (2001) Mechanisms of nutritional and hormonal regulation of lipogenesis. EMBO Rep 2, 282-286.
35. de Heredia FP, Larque E, Del Puy Portillo M, et al. (2008) Age-related changes in fatty acids from different adipose depots in rat and their association with adiposity and insulin. Nutrition 24, 1013-1022.
36. Guo KY, Halo P, Leibel RL, et al. (2004) Effects of obesity on the relationship of leptin mRNA expression and adipocyte size in anatomically distinct fat depots in mice. Am J Physiol Regul Integr Comp Physiol 287, R112-R119.
37. Drolet R, Richard C, Sniderman AD, et al. (2008) Hypertrophy and hyperplasia of abdominal adipose tissues in women. Int J Obes (Lond) 32, 283-291.
38. Muhlhausler BS, Cook-Johnson R, James M, et al. (2010) Opposing effects of omega-3 and omega-6 long chain polyunsaturated fatty acids on the expression of lipogenic genes in omental and retroperitoneal adipose depots in the rat. J Nutr Metab (epublication 5 August 2010).
39. van Harmelen V, Dicker A, Ryden M, et al. (2002) Increased lipolysis and decreased leptin production by human omental as compared with subcutaneous preadipocytes. Diabetes 51, 2029-2036.
40. Di Girolamo M, Mendlinger S & Fertig JW (1971) A simple method to determine fat cell size and number in four mammalian species. Am J Physiol 221, 850-858.
41. Hishikawa D, Hong YH, Roh SG, et al. (2005) Identification of genes expressed differentially in subcutaneous and visceral fat of cattle, pig, and mouse. Physiol Genomics 21, 343-350.
42. Tchernof A, Belanger C, Morisset AS, et al. (2006) Regional differences in adipose tissue metabolism in women: minor effect of obesity and body fat distribution. Diabetes 55, 1353-1360.
43. Ray H, Pinteur C, Frering V, et al. (2009) Depot-specific differences in perilipin and hormone-sensitive lipase expression in lean and obese. Lipids Health Dis 8, 58.
44. Kloting N, Berthold S, Kovacs P, et al. (2009) MicroRNA expression in human omental and subcutaneous adipose tissue. PLoS One 4, e4699.
45. Durmus B, Mook-Kanamori DO, Holzhauer S, et al. (2010) Growth in foetal life and infancy is associated with abdominal adiposity at the age of 2 years: the generation R study. Clin Endocrinol (Oxf) 72, 633-640.
46. Ibanez L, Lopez-Bermejo A, Diaz M, et al. (2011) Catch-up growth in girls born small for gestational age precedes childhood progression to high adiposity. Fertil Steril 96, 220-223.
47. Wells JC, Haroun D, Levene D, et al. (2011) Prenatal and postnatal programming of body composition in obese children and adolescents: evidence from anthropometry, DXA and the 4-component model. Int J Obes (Lond) 35, 534-540.
48. Demerath EW, Reed D, Choh AC, et al. (2009) Rapid postnatal weight gain and visceral adiposity in adulthood: the Fels Longitudinal Study. Obesity (Silver Spring) 17, 2060-2066.
49. Holzhauer S, Zwijsen RM, Jaddoe VW, et al. (2009) Sonographic assessment of abdominal fat distribution in infancy. Eur J Epidemiol 24, 521-529.
50. Cryer A & Jones HM (1980) The development of white adipose tissue. Effect of litter size on the lipoprotein lipase activity of four adipose-tissue depots, serum immunoreactive insulin and tissue cellularity during the first year of life in male and female rats. Biochem J 186, 805-815.
51. Garcia AP, Palou M, Sanchez J, et al. (2011) Moderate caloric restriction during gestation in rats alters adipose tissue sympathetic innervation and later adiposity in offspring. PLoS One 6, e17313.
52. Vallee M, Mayo W, Maccari S, et al. (1996) Long-term effects of prenatal stress and handling on metabolic parameters: relationship to corticosterone secretion response. Brain Res 712, 287-292.
53. Young JB (2000) Effects of neonatal handling on sympathoa-drenal activity and body composition in adult male rats. Am J Physiol Regul Integr Comp Physiol 279, R1745-R1752.
54. Faust IM, Johnson PR & Hirsch J (1980) Long-term effects of early nutritional experience on the development of obesity in the rat. J Nutr 110, 2027-2034.
55. Bays HE, Gonzalez-Campoy JM, Bray GA, et al. (2008) Pathogenic potential of adipose tissue and metabolic consequences of adipocyte hypertrophy and increased visceral adiposity. Expert Rev Cardiovasc Ther 6, 343-368.
56. Chumlea WC, Siervogel RM, Roche AF, et al. (1982) Changes in adipocyte cellularity in children ten to 18 years of age. Int J Obes 6, 383-389.
57. Spiegelman BM & Flier JS (1996) Adipogenesis and obesity: rounding out the big picture. Cell 87, 377-389.
58. Armand M, Hamosh M, Mehta NR, et al. (1996) Effect of human milk or formula on gastric function and fat digestion in the premature infant. Pediatr Res 40, 429-437.
59. Michalski MC, Briard V, Desage M, et al. (2005) The dispersion state of milk fat influences triglyceride metabolism in the rat-a 13CO2 breath test study. Eur J Nutr 44, 436-444.
60. Michalski MC, Soares AF, Lopez C, et al. (2006) The supramolecular structure of milk fat influences plasma tria-cylglycerols and fatty acid profile in the rat. Eur J Nutr 45, 215-224.