The early development of white adipose tissue. Effects of litter size on the lipoprotein lipase activity of four adipose-tissue depots, serum immunoreactive insulin and tissue cellularity during the first four weeks of life in the rat (original) (raw)

Abstract

1. Newborn rats were reared in litters of either four or sixteen individuals. The animals from the small litters gained body weight more rapidly than those from large litters during the first 29 days of postnatal life studied. 2. The relative weights of the perigenital, perirenal, subcutaneous and intramuscular white-adipose-tissue sites in the animals from small litters indicated their relative obesity compared with controls. 3. The adipose depots from animals reared in small litters had a greater proportion of lipid present, by weight, and had a greater number of larger fat-cells present in them compared with the depots of animals reared in large litters. 4. Compared with both normal-sized litter controls and animals reared in sixteens, during the period of study the animals from small litters were hypertriacylglycerolaemic but normocholesterolaemic. 5. During suckling the blood glucose concentrations of animals reared in fours were increased, as were the concentrations of circulating immunoreactive insulin. 6. During the 29 days of life studied, in general, the lipoprotein lipase activity of adipose depots from animals reared in fours was greater than for animals in large litters when expressed as μmol of nonesterified fatty acid released from the substrate/h per g fresh weight of tissue, per depot, or per million fat-cells, but were similar per cm2 of fat-cell surface area. 7. The previously noted [Cryer & Jones (1978) Biochem. J. 172, 319–325] pattern of mid-suckling elevation, late-suckling decline and post-weaning increase in the lipoprotein lipase activity of the four white-adipose depots studied was not obliterated by the nutritional manipulations employed. 8. The relation of the enzyme-activity changes and their hormonal stimuli to triacylglycerol accumulation in fat-cells of animals from large and small litters is discussed in relation to the possible significance they may have to our understanding of neonatally induced obesity.

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Selected References

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  1. Ashwell M. A., Priest P., Sowter C. Importance of fixed sections in the study of adipose tissue cellularity. Nature. 1975 Aug 28;256(5520):724–725. doi: 10.1038/256724a0. [DOI] [PubMed] [Google Scholar]
  2. Ashwell M., Priest P., Bondoux M., Sowter C., McPherson C. K. Human fat cell sizing--a quick, simple method. J Lipid Res. 1976 Mar;17(2):190–192. [PubMed] [Google Scholar]
  3. Bagdade J. D., Yee E., Albers J., Pykalisto O. J. Glucocorticoids and triglyceride transport: effects on triglyceride secretion rates, lipoprotein lipase, and plasma lipoproteins in the rat. Metabolism. 1976 May;25(5):533–542. doi: 10.1016/0026-0495(76)90007-x. [DOI] [PubMed] [Google Scholar]
  4. Björntorp P. Sjöström L,+SJOSTROM L: Number and size of adipose tissue fat cells in relation to metabolism in human obesity. Metabolism. 1971 Jul;20(7):703–713. doi: 10.1016/0026-0495(71)90084-9. [DOI] [PubMed] [Google Scholar]
  5. Blázquez E., Montoya E., López Quijada C. Relationship between insulin concentrations in plasma and pancreas of oetal and weanling rats. J Endocrinol. 1970 Dec;48(4):553–561. doi: 10.1677/joe.0.0480553. [DOI] [PubMed] [Google Scholar]
  6. Blázquez E., Simon F. A., Blázquez M., Foà P. P. Changes in serum growth hormone levels from fetal to adult age in the rat. Proc Soc Exp Biol Med. 1974 Dec;147(3):780–783. doi: 10.3181/00379727-147-38437. [DOI] [PubMed] [Google Scholar]
  7. Borensztajn J., Keig P., Rubenstein A. H. The role of glucagon in the regulation of myocardial lipoprotein lipase activity. Biochem Biophys Res Commun. 1973 Jul 17;53(2):603–608. doi: 10.1016/0006-291x(73)90704-3. [DOI] [PubMed] [Google Scholar]
  8. Borensztajn J., Samols D. R., Rubenstein A. H. Effects of insulin on lipoprotein lipase activity in the rat heart and adipose tissue. Am J Physiol. 1972 Dec;223(6):1271–1275. doi: 10.1152/ajplegacy.1972.223.6.1271. [DOI] [PubMed] [Google Scholar]
  9. Bray G. A. The Zucker-fatty rat: a review. Fed Proc. 1977 Feb;36(2):148–153. [PubMed] [Google Scholar]
  10. Cleary M. P., Greenwood M. R., Brasel J. A. A multifactor analysis of growth in the rat epididymal fat pad. J Nutr. 1977 Nov;107(11):1969–1974. doi: 10.1093/jn/107.11.1969. [DOI] [PubMed] [Google Scholar]
  11. Cryer A., Jones H. M. Changes in the lipoprotein lipase (clearing-factor lipase) activity of white adipose tissue during development of the rat. Biochem J. 1978 May 15;172(2):319–325. doi: 10.1042/bj1720319. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Cryer A., Riley S. E., Williams E. R., Robinson D. S. Effect of nutritional status on rat adipose tissue, muscle and post-heparin plasma clearing factor lipase activities: their relationship to triglyceride fatty acid uptake by fat-cells and to plasma insulin concentrations. Clin Sci Mol Med. 1976 Mar;50(3):213–221. doi: 10.1042/cs0500213. [DOI] [PubMed] [Google Scholar]
  13. Czajka-Narins D. M., Hirsch J. Supplementary feeding during the preweaning period. Effect on carcass composition and adipose tissue cellularity of the rat. Biol Neonate. 1974;25(3-4):176–185. doi: 10.1159/000240690. [DOI] [PubMed] [Google Scholar]
  14. Durham B. C., Miller H. I., Holmes W. L. Comparative rates of free fatty acid esterification in rat epididymal, perirenal and omental adipose tissue. Biochim Biophys Acta. 1971 Mar 16;231(2):257–263. doi: 10.1016/0005-2760(71)90135-4. [DOI] [PubMed] [Google Scholar]
  15. Dussault J. H., Labrie F. Development of the hypothalamic-pituitary-thyroid axis in the neonatal rat. Endocrinology. 1975 Nov;97(5):1321–1324. doi: 10.1210/endo-97-5-1321. [DOI] [PubMed] [Google Scholar]
  16. Enser M. Clearing-factor lipase in obese hyperglycaemic mice (ob-ob). Biochem J. 1972 Sep;129(2):447–453. doi: 10.1042/bj1290447. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Epstein H. T. The effect of litter size on weight gain in mice. J Nutr. 1978 Jan;108(1):120–123. doi: 10.1093/jn/108.1.120. [DOI] [PubMed] [Google Scholar]
  18. Ferre P., Pegorier J. P., Girard J. The effects of inhibition of gluconeogenesis in suckling newborn rats. Biochem J. 1977 Jan 15;162(1):209–212. doi: 10.1042/bj1620209. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Ferré P. R., Pegorier J. P., Girard J. R., Marliss E. B. Evidence that fatty acid oxidation stimulates gluconeogenesis in newborn rats [proceedings]. Biochem Soc Trans. 1977;5(4):982–983. doi: 10.1042/bst0050982. [DOI] [PubMed] [Google Scholar]
  20. Girard J. R., Kervran A., Soufflet E., Assan R. Factors affecting the secretion of insulin and glucagon by the rat fetus. Diabetes. 1974 Apr;23(4):310–317. doi: 10.2337/diab.23.4.310. [DOI] [PubMed] [Google Scholar]
  21. Greenwood M. R., Hirsch J. Postnatal development of adipocyte cellularity in the normal rat. J Lipid Res. 1974 Sep;15(5):474–483. [PubMed] [Google Scholar]
  22. HAHN P., KOLDOVSKY O., MELICHAR V., NOVAK M. Interrelationship between fat and sugar metabolism in infant rats. Nature. 1961 Dec 30;192:1296–1296. doi: 10.1038/1921296a0. [DOI] [PubMed] [Google Scholar]
  23. HALES C. N., RANDLE P. J. Immunoassay of insulin with insulin-antibody precipitate. Biochem J. 1963 Jul;88:137–146. doi: 10.1042/bj0880137. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Hahn P., Girard J., Assan R., Frohlich J., Kervran A. Control of blood cholesterol levels in suckling and weanling rats. J Nutr. 1977 Nov;107(11):2062–2066. doi: 10.1093/jn/107.11.2062. [DOI] [PubMed] [Google Scholar]
  25. Hemon P., Ricquier D., Mory G. The lipoprotein lipase activity of brown adipose tissue during early post-natal development of the normal and hypothyroid rat. Horm Metab Res. 1975 Nov;7(6):481–484. doi: 10.1055/s-0028-1093708. [DOI] [PubMed] [Google Scholar]
  26. Hietanen E., Greenwood M. R. A comparison of lipoprotein lipase activity and adipocyte differentiation in growing male rats. J Lipid Res. 1977 Jul;18(4):480–490. [PubMed] [Google Scholar]
  27. Hirsch J., Gallian E. Methods for the determination of adipose cell size in man and animals. J Lipid Res. 1968 Jan;9(1):110–119. [PubMed] [Google Scholar]
  28. Hirsch J., Han P. W. Cellularity of rat adipose tissue: effects of growth, starvation, and obesity. J Lipid Res. 1969 Jan;10(1):77–82. [PubMed] [Google Scholar]
  29. Holm G., Jacobsson B., Björntorp P., Smith U. Effects of age and cell size on rat adipose tissue metabolism. J Lipid Res. 1975 Nov;16(6):461–464. [PubMed] [Google Scholar]
  30. Hunt C. E., Lindsey J. R., Walkley S. U. Animal models of diabetes and obesity, including the PBB/Ld mouse. Fed Proc. 1976 Apr;35(5):1206–1217. [PubMed] [Google Scholar]
  31. Johnson P. R., Hirsch J. Cellularity of adipose depots in six strains of genetically obese mice. J Lipid Res. 1972 Jan;13(1):2–11. [PubMed] [Google Scholar]
  32. Johnson P. R., Stern J. S., Greenwood M. R., Zucker L. M., Hirsch J. Effect of early nutrition on adipose cellularity and pancreatic insulin release in the Zucker rat. J Nutr. 1973 May;103(5):738–743. doi: 10.1093/jn/103.5.738. [DOI] [PubMed] [Google Scholar]
  33. Johnson P. R., Zucker L. M., Cruce J. A., Hirsch J. Cellularity of adipose depots in the genetically obese Zucker rat. J Lipid Res. 1971 Nov;12(6):706–714. [PubMed] [Google Scholar]
  34. Kazdová L., Fábry P., Vrána A. Effect of small doses of insulin in vivo on the proliferation and cellularity of adipose tissue. Diabetologia. 1974 Feb;10(1):77–83. doi: 10.1007/BF00421417. [DOI] [PubMed] [Google Scholar]
  35. Kirtland J., Gurr M. I., Saville G., Widdowson E. M. Occurrence of "pockets" of very small cells in adipose tissue of the guinea pig. Nature. 1975 Aug 28;256(5520):723–724. doi: 10.1038/256723a0. [DOI] [PubMed] [Google Scholar]
  36. Kirtland J., Gurr M. I., Widdowson E. M. Body lipids of guinea pigs exposed to different dietary fats from mid-gestation to 3 months of age. Nutr Metab. 1976;20(5):338–350. doi: 10.1159/000175719. [DOI] [PubMed] [Google Scholar]
  37. Knittle J. L., Hirsch J. Effect of early nutrition on the development of rat epididymal fat pads: cellularity and metabolism. J Clin Invest. 1968 Sep;47(9):2091–2098. doi: 10.1172/JCI105894. [DOI] [PMC free article] [PubMed] [Google Scholar]
  38. MCCANCE R. A. Food, growth, and time. Lancet. 1962 Sep 29;2(7257):621–626. doi: 10.1016/s0140-6736(62)92539-4. [DOI] [PubMed] [Google Scholar]
  39. Martin P. J. A quick inexpensive method for serum triglycerides. Clin Chim Acta. 1975 Jul 9;62(1):79–88. doi: 10.1016/0009-8981(75)90282-x. [DOI] [PubMed] [Google Scholar]
  40. Nestel P. J., Austin W. Relationship between adipose lipoprotein lipase activity and compounds which affect intracellular lipolysis. Life Sci. 1969 Feb 15;8(4):157–164. doi: 10.1016/0024-3205(69)90075-7. [DOI] [PubMed] [Google Scholar]
  41. Persico P. A., Cerchio M., Jeffay H. Glycerokinase in mammalian adipose tissue: stimulation by lipogenic substances. Am J Physiol. 1975 Jun;228(6):1868–1874. doi: 10.1152/ajplegacy.1975.228.6.1868. [DOI] [PubMed] [Google Scholar]
  42. Pégorier J. P., Ferré P., Girard J. The effects of inhibition of fatty acid oxidation in suckling newborn rats. Biochem J. 1977 Sep 15;166(3):631–634. doi: 10.1042/bj1660631. [DOI] [PMC free article] [PubMed] [Google Scholar]
  43. Péquignot-Planche E., De Gasquet P., Boulangé A., Tonnu N. T. Lipoprotein lipase activity at onset of development of white adipose tissue in newborn rats. Biochem J. 1977 Feb 15;162(2):461–463. doi: 10.1042/bj1620461. [DOI] [PMC free article] [PubMed] [Google Scholar]
  44. Richmond W. Preparation and properties of a cholesterol oxidase from Nocardia sp. and its application to the enzymatic assay of total cholesterol in serum. Clin Chem. 1973 Dec;19(12):1350–1356. [PubMed] [Google Scholar]
  45. Salaman M. R., Robinson D. S. Clearing-factor lipase in adipose tissue. A medium in which the enzyme activity of tissue from starved rats increases in vitro. Biochem J. 1966 Jun;99(3):640–647. doi: 10.1042/bj0990640. [DOI] [PMC free article] [PubMed] [Google Scholar]
  46. Schonfeld G., Felski C., Howald M. A. Characterization of the plasma lipoproteins of the genetically obese hyperlipoproteinemic Zucker fatty rat. J Lipid Res. 1974 Sep;15(5):457–464. [PubMed] [Google Scholar]
  47. Snell K., Walker D. G. Gluconeogenesis in the newborn rat: the substrates and their quantitative significance. Enzyme. 1973;15(1):40–81. [PubMed] [Google Scholar]
  48. Stern J. S., Greenwood M. R. A review of development of adipose cellularity in man and animals. Fed Proc. 1974 Aug;33(8):1952–1955. [PubMed] [Google Scholar]
  49. Takeuchi T., Ogawa M., Furihata C., Kawachi T., Sugimura T. Perinatal changes in amylase and serum corticosterone levels in rats. Biochim Biophys Acta. 1977 May 26;497(3):657–662. doi: 10.1016/0304-4165(77)90286-0. [DOI] [PubMed] [Google Scholar]
  50. Uete T., Hori T., Fukutani C. Ultra-micromethods for the biochemical analysis of cutaneous capillary blood. IV. Selection of the glucose oxidase-2,2'-Azino-di-(3-ethyl-benzthiazolin-sulphonic acid-6)diammonium method for measuring blood sugar of neonates. Clin Chim Acta. 1976 Jul 15;70(2):329–332. doi: 10.1016/0009-8981(76)90435-6. [DOI] [PubMed] [Google Scholar]
  51. WIDDOWSON E. M., McCANCE R. A. Some effects of accelerating growth. I. General somatic development. Proc R Soc Lond B Biol Sci. 1960 May 17;152:188–206. doi: 10.1098/rspb.1960.0032. [DOI] [PubMed] [Google Scholar]
  52. Whatson T. S., Moore W. J., Smart J. L., Dobbing J. Early undernutrition: subsequent growth of male and female rats. Life Sci. 1978 Jan;22(2):179–185. doi: 10.1016/0024-3205(78)90535-0. [DOI] [PubMed] [Google Scholar]
  53. Wurtman J. J., Miller S. A. Effect of litter size on weight gain in rats. J Nutr. 1976 May;106(5):697–701. doi: 10.1093/jn/106.5.697. [DOI] [PubMed] [Google Scholar]
  54. de Gasquet P., Péquignot E., Lemonnier D., Alexiu A. Adipose-tissue lipoprotein lipase activity and cellularity in the genetically obese Zucker rat (fa-fa). Biochem J. 1973 Mar;132(3):633–635. doi: 10.1042/bj1320633. [DOI] [PMC free article] [PubMed] [Google Scholar]
  55. de Gasquet P., Péquignot E. Lipoprotein lipase activities in adipose tissues, heart and diaphragm of the genetically obese mouse(ob-ob). Biochem J. 1972 Apr;127(2):445–447. doi: 10.1042/bj1270445. [DOI] [PMC free article] [PubMed] [Google Scholar]