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Short communication
Hormonal regulation of lipogenesis in cultured adipose tissue
from perinatal and month-old goats
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J. Skarda
´ Institute of Animal Physiology and Genetics, Academy of Sciences of the Czech Republic, 104 00 Prague 10-Uhrıneves,
Czech Republic
Received 6 November 1998; received in revised form 23 April 1999; accepted 7 September 1999
Abstract
Perinatal (1–2 days old) and month-old (24–32 days old) male goats were used to investigate the effect of age and chronic culture (24 h) of perirenal and omental adipose tissue explants in the presence of insulin, cortisol and recombinant bovine somatotrophin (bGH), alone or in different combinations, on lipogenic responses in the absence and in the presence of catecholamines in acute incubations (2 h). Addition of insulin alone or bGH alone or insulin plus bGH had no effect on the rate of fatty acid synthesis in tissues of both groups. The presence of cortisol alone decreased (P,0.05) and the combination of insulin plus cortisol increased (P,0.05) lipogenesis in perirenal adipose tissue explants from month-old goats. No such effects of these hormonal combinations were noted in omental adipose tissue from perinatal and month-old goats or in perirenal adipose tissue from perinatal goats. When perirenal adipose tissue explants from month-old goats were cultured in the presence of insulin plus cortisol plus bGH the rates of lipogenesis were lower (P,0.05) than those in cultures with insulin plus cortisol. Isoprenaline (Iso), but not noradrenaline (Ne), inhibited lipogenesis in freshly prepared adipose tissue explants; however, when maintained in tissue culture for 24 h, a response to Ne was induced. In cultured perirenal adipose tissue explants of both perinatal and month-old goats, the mean values of fatty acid synthesis were decreased (P,0.05) by Ne and Iso: Ne and Iso were equally effective. However, in cultured omental adipose tissue explants, Iso was more effective than Ne. 2000 Elsevier Science B.V. All rights reserved.
Keywords: Goat; Ontogenesis; Adipose tissue; Growth hormone; Lipogenesis
1. Introduction direct heat (nonshivering thermogenesis) and release free fatty acids as an energy substrate for shivering At birth, body temperature must be maintained by (Randall, 1992). Thermogenic effects of catechol-mobilization and use of energy reserves. Sympathetic amines are potentiated or inhibited by thyroid hor-stimulation, in response to cold, increases lipolysis mones, glucagon, growth hormone (GH), adreno-and blood flow through the fat depots to provide corticotrophic hormone, insulin and glucocorticoids
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(Jansky, 1995). Co-ordination of the secretion and action of these hormones after birth is therefore required for perinatal survival and thus for decreas-ing the relatively high perinatal mortality in domestic *Tel.: 142-2-6771-1730, fax: 142-2-6771-0803.
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E-mail address: [email protected] (J. Skarda) farm animals. Cold resistance of perinatal animals is
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also increased by hormonally controlled fat deposi- incubation and their interaction) (Skarda, 1998,
tion. 1999).
Whilst the physiological significance of the direct effects of bovine (b) GH on lipolysis remain
uncer-tain, there is evidence that bGH acts in the presence 3. Results of cortisol to modify lipogenesis and the
responsive-ness of adipose tissue of 8-month-old goats to insulin The rate of fatty acid synthesis in freshly-prepared ˇ
and catecholamines (Skarda, 1998). It is not clear, explants in 2-h incubations was established to pro-however, whether bGH acts in a similar manner in vide a measure of the maintenance of lipogenesis in young goats. Therefore, our objectives for these subsequent incubations of explants cultured in the studies were: (1) to define age-related changes in presence of different hormones. Comparison of the hormonal control of lipogenesis; (2) to determine lipogenesis of freshly-prepared explants with ex-whether age-related changes in thermogenic effects plants cultured in the absence of hormones for 24 h of catecholamines in vivo (Noble, 1981) would be showed that the rate of incorporation of acetate into associated with the age-related changes in catechol- fatty acids in both perirenal and omental adipose amine effects in vitro. tissue explants from perinatal animals was lower In the present study, a tissue culture system was (P,0.05) after 24 h of culture (Table 1). In tissues used to investigate the abilities of bovine somatot- from month-old animals, lipogenesis was again rophin (bGH) and cortisol to inhibit lipogenesis and lower (P,0.05) after 24 h of culture in perirenal to antagonize insulin action. In addition, the abilities adipose tissue explants but not in omental adipose of catecholamines to inhibit lipogenesis in adipose tissue explants (Table 2).
tissue explants during transition from brown to white Fatty acid synthesis in adipose tissue explants adipose tissue were determined in goats. cultured in the absence of hormones was used as a baseline measure to lipogenic response to different hormones added to the culture medium. Addition of 2. Materials and methods insulin alone or bGH alone or insulin plus bGH had no significant effect on the rate of fatty acid synth-The experiments were carried out with perinatal eses in tissues of both ages of goats. The presence of (age 1–2 days) and month-old (age 24–32 days) cortisol alone decreased (P,0.05) and the combina-male goats of the Czech white breed. All animals tion of insulin plus cortisol increased (P,0.05) were allowed to suckle and remained with their dams lipogenesis in perirenal adipose tissue explants from until they were killed. The great omentum and month-old animals, but no such effects of these perirenal adipose tissues were aseptically removed hormonal combinations were noted in perirenal and and placed immediately into sterile phosphate buf- omental adipose tissue explants from perinatal goats fered saline at about 388C. Explants were prepared, or in omental adipose tissue explants from month-old incubated and cultured as described previously goats. When perirenal adipose tissue explants from
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(Skarda, 1998). To measure the responsiveness to month-old goats were cultured in the presence of catecholamines (inhibition of lipogenesis), explants insulin plus cortisol plus bGH, the rates of were incubated in the presence and absence of either lipogenesis were lower (P,0.05) than those in
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noradrenaline (Ne; 10 mmol l ) or isoprenaline cultures with insulin plus cortisol. No significant 21
(Iso; 10 mmol l ). To study the effect of different effect of this hormonal combination on lipogenesis in hormones during culture on subsequent lipogenic perirenal and omental adipose tissue explants from activity, explants were cultured in the presence of perinatal goats or in omental adipose tissue explants
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insulin (17 nmol l ), cortisol (138 nmol l ) and from month-old goats was observed. 21
Table 1
Effect of chronic culture in the presence of various hormones on the rate of lipogenesis (acetate incorporation into fatty acids in nmol mg 21 21
tissue h ) during acute incubations in the presence or absence of catecholamines in perirenal and omental adipose tissue explants from a
Overall mean after culture 3.76 3.01 2.55
Pooled SEM 0.79 0.67 0.73
Overall mean after culture 17.73 18.17 13.49
Pooled SEM 3.87 5.14 3.59
a
Perirenal adipose tissue explants of six and omental adipose tissue explants of five perinatal animals (killed 1–2 days after birth) were 21
cultured for 24 h in a modified Waymouth’s medium (containing 3.5 mmol l glucose) in the absence of hormones or in the presence of 14
insulin, bGH and cortisol alone or in different combinations. The explants were exposed before and after culture to (1- C)acetate for a 2-h period of incubation in the presence or absence of noradrenaline (Ne) or isoprenaline (Iso) in Krebs–Henseleit buffer supplemented with sodium acetate and glucose. All values are means6pooled SEM (standard error LS mean for paired values). Values within a column which do not have the same upper case superscript (A, B, C, D, E) differ significantly (P,0.05). Values within a row which do not have the same lower case superscript (a, b, c) differ significantly (P,0.05).
adipose tissue explants from month-old animals, plants, Iso was more (P,0.05) effective than Ne lipogenesis was decreased (P,0.05) by both cat- (Tables 1 and 2).
echolamines; however, Iso was more effective (P, 0.05) than Ne.
In cultured perirenal adipose tissue explants of 4. Discussion both perinatal and month-old goats, the mean values
Table 2
Effect of chronic culture in the presence of various hormones on the rate of lipogenesis (acetate incorporation into fatty acids in nmol.mg 21 21
tissue h ) during acute incubations in the presence or absence of catecholamines in perirenal and omental adipose tissue explants from a
Overall mean after culture 41.23 15.17 11.09
Pooled SEM 9.55 10.82 4.00
Overall mean after culture 47.75 19.27 15.22
Pooled SEM 20.71 8.20 5.26
a
Perirenal adipose tissue explants of six and omental adipose tissue explants of three male goats were incubated and cultured as described in the legend to Table 1.
cells, brown adipose tissue-specific mitochondrial rate of lipogenesis in both perirenal and omental uncoupling protein (UCP) and iodothyronine 5- adipose tissue explants in perinatal goats. This deiodinase activity (Thompson and Jenkinson, 1970; refractoriness to hormones disappeared by one month Trayhurn et al., 1993). Although multivacuolar cells in perirenal adipose tissue but was still present in and UCP are present at birth in the adipose tissue of omental adipose tissue explants. The responsiveness newborn ruminants, they disappear over the first of omental adipose tissue to hormones was found in
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days or weeks of postnatal life, indicating that there 8-month-old goats (Skarda, 1998).
Ne on lipogenesis may partly reflect the low to Dr. J. Wolf for statistical analysis. This work was lipogenic activity of the adipocytes of perinatal supported by the Grant Agency of the Academy of goats, so that there is not much to decrease. How- Sciences (No. A7-045608) and by the Grant Agency ever, Iso inhibited lipogenesis in adipose tissue of the Czech Republic (No. 523 / 99 / 0843).
explants of the perinatal goats and was more effec-tive than Ne in month-old goats. The fact that Ne has
thermogenic effects in vivo but no inhibitory effect References on lipogenesis in vitro indicates that either some
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factor must prevent inhibitory effects ofa2-receptors Jansky, L., 1995. Humoral thermogenesis and its role in maintain-ing energy balance. Physiol. Rev. 75, 237–259.
or that the primary target is a cell type other than the
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still present in omental adipose tissue explants. In ˇSkarda, J., 1999. Chronic effects of somatotropin treatment in vivo cultured perirenal adipose tissue explants of both and in vitro on lipogenic activity of goat adipose tissue in a glucose-free buffer during acute incubation. Physiol. Res. 48, perinatal and month-old goats, Ne and Iso were
43–49. equally effective; however, in omental adipose tissue
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the abilities of hormones to affect lipogenesis in Trayhurn, P., Thomas, M.E.A., Duncan, J.S., Nicol, F., Arthur, adipose tissue appear to be linked to developmental J.R., 1993. Presence of the brown fat-specific mitochondrial uncoupling protein and iodothyronine 59deiodinase activity in adaptations in adipose tissue function after birth.
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synthesis in adipose tissues of foetal lambs. Dom. Anim. white adipose tissue. The tissue’s ability to respond
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Acknowledgements
