Hostname: page-component-cd9895bd7-jn8rn Total loading time: 0 Render date: 2024-12-18T16:42:21.598Z Has data issue: false hasContentIssue false

Anterior pituitary influence on adipokine expression and secretion by porcine adipocytes

Published online by Cambridge University Press:  06 January 2016

R. Saleri*
Affiliation:
Dipartimento di Scienze Medico-Veterinarie, Università di Parma, Via del Taglio 10, 43126 Parma, Italy
V. Cavalli
Affiliation:
Dipartimento di Scienze Medico-Veterinarie, Università di Parma, Via del Taglio 10, 43126 Parma, Italy
P. Martelli
Affiliation:
Dipartimento di Scienze Medico-Veterinarie, Università di Parma, Via del Taglio 10, 43126 Parma, Italy
P. Borghetti
Affiliation:
Dipartimento di Scienze Medico-Veterinarie, Università di Parma, Via del Taglio 10, 43126 Parma, Italy
*
Get access

Abstract

Nutritional stressors may cause negative effects on animal health and growth and lead to significant economic impact. Adipose tissue is an endocrine organ producing, mediators and hormones, called adipokines. They play a dynamic role in body homeostasis and in the regulation of energy expenditure, interacting with feeding behavior, hormones and growth factors. This in vitro study aimed to investigate how nutritional conditions and growth hormone (GH) can influence nitric oxide (NO) production and the expression and secretion of three important adipokines, that is leptin, interleukin-6 (IL-6) and tumor necrosis factor-α (TNF-α), by swine adipocytes. In our experimental model, mesenchymal stem cells from omental adipose tissue were induced to adipogenic differentiation. After differentiation, adipocytes were incubated for 24 h (T0) with DMEM/Ham’s F12 (group A) or DMEM/Ham’s F12 salts (group B), a DMEM/Ham’s F12 formulation deprived of nutritional components. Primary adipocyte cells were also co-cultured for 4 h (T+4) or 12 h (T+12) with or without anterior pituitary slices. To stimulate GH secretion by pituitary cells, growth hormone releasing hormone at 10−8 M was added at the start of the incubation times (4 or 12 h). At T0, T+4 and T+12, NO production, leptin, IL-6 and TNF-α expression and secretion were measured. NO increased (P<0.05) up to twofold in restricted culture conditions. Deprived medium and coincubation with anterior pituitary positively influenced leptin secretion and expression. TNF-α was expressed and secreted only in deprived culture condition groups (B, B1 and B2). Nutrients availability and pituitary co-culture did not affect IL-6 expression and secretion. Our study shows an endocrine function for porcine adipocytes. In our model, adipocytes readily responded to nutritional inputs by secretion of molecules affecting energy balance. This secretion capacity was modulated by GH. Improving our knowledge of the role of adipocyte in the endocrine system, may lead to a more complete understanding of regulating energy balance in swine.

Type
Research Article
Copyright
© The Animal Consortium 2016 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Andersson, K, Gaudiot, N, Ribiere, C, Elizalde, M, Giudicelli, Y and Arner, P 1999. A nitric oxide-mediated mechanism regulates lipolysis in human adipose tissue in vivo. British Journal of Pharmacology 126, 16391645.Google Scholar
Baratta, M, Saleri, R, Mainardi, GL, Valle, D, Giustina, A and Tamanini, C 2002. Leptin regulates GH gene expression and secretion and nitric oxide production in pig pituitary cells. Endocrinology 143, 551557.Google Scholar
Barb, CR, Hausman, GJ and Houseknecht, KL 2001. Biology of leptin in the pig. Domestic Animal Endocrinology 21, 297317.Google Scholar
Berg, M, Fraker, DL and Alexander, HR 1994. Characterization of differentiation factor/leukaemia inhibitory factor effect on lipoprotein lipase activity and mRNA in 3T3-L1 adipocytes. Cytokines 6, 425432.Google Scholar
Bernotiene, E, Palmer, G and Gabay, C 2006. The role of leptin in innate and adaptive immune responses. Arthritis Research & Therapy 8, 217227.Google Scholar
Borghetti, P, De Angelis, E, Saleri, R, Cavalli, V, Cacchioli, A, Corradi, A, Mocchegiani, E and Martelli, P 2006. Peripheral T lymphocyte changes in neonatal piglets: Relationship with growth hormone (GH), prolactin (PRL) and cortisol changes. Veterinary Immunology and Immunopathology 110, 1725.Google Scholar
Borghetti, P, Saleri, R, Mocchegiani, E, Corradi, A and Martelli, P 2009. Infection, immunity and the neuroendocrine response. Veterinary Immunology and Immunopathology 130, 141162.Google Scholar
Chen, X, Xun, K, Chen, L and Wang, Y 2009. TNF-α, a potent lipid metabolism. Cell Biochemistry and Function 27, 407416.Google Scholar
Elsasser, TH, Caperna, TJ, Li, CJ, Kahl, S and Sartin, JL 2004. Critical control points in the impact of the proinflammatory immune response on growth and metabolism. Journal of Animal Science 86 (14 suppl.), E105E125.Google Scholar
Friedman, JM and Halaas, JL 1998. Leptin and the regulation of body weight in mammals. Nature 395, 763770.Google Scholar
Frost, RA and Lang, CH 2004. Alteration of somatotropic function by proinflammatory cytokines. Journal of Animal Science 82, E100E109.Google Scholar
Galic, S, Oakhill, JS and Steinberg, GR 2010. Adipose tissue as an endocrine organ. Molecular and Cellular Endocrinology 316, 129139.CrossRefGoogle ScholarPubMed
Green, A, Rumberger, JM, Stuart, CA and Ruhoff, MS 2004. Stimulation of lipolysis by tumor necrosis factor-alpha in 3T3-L1 adipocytes is glucose dependent: implications for longterm regulation of lipolysis. Diabetes 53, 7481.CrossRefGoogle ScholarPubMed
Hausman, GJ, Barb, CR and Dean, RG 2008. Patterns of gene expression in pig adipose tissue: insulin-like growth factor system proteins, neuropeptide Y (NPY), NPY receptors, neurotrophic factors and other secreted factors. Domestic Animal Endocrinology 35, 2434.Google Scholar
Hevener, W, Routh, PA and Almond, GW 1999. Effects of immune challenge on concentrations of serum insulin-like growth factor-I and growth performance in pigs. Canadian Veterinary Journal 40, 782786.Google Scholar
Hochdorfer, T, Kuhny, M, Zorn, CN, Hendriks, RW, Vanhaesebroeck, B, Bohnacker, T, Krystal, G and Huber, M 2011. Activation of the PI3K pathway increases TLR-induced TNF-alpha and IL-6 but reduces IL-1beta production in mast cells. Cellular Signalling 23, 866875.Google Scholar
Jensen, MD 2003. Cytokine regulation of lipolysis in humans? Journal of Clinical Endocrinology & Metabolism 88, 30033004.Google Scholar
Joffin, N, Niang, F, Forest, C and Jaubert, AM 2012. Is there NO help for leptin? Biochimie 94, 21042110.Google Scholar
Kern, PA, Ranganathan, S, Li, C, Wood, L and Ranganathan, G 2004. Adipose tissue tumor necrosis factor and interleukin-6 expression in human obesity and insulin resistance. American Journal of Physiology – Endocrinology and Metabolism 280, E745E751.CrossRefGoogle Scholar
Louveau, I and Gondret, F 2004. Regulation of development and metabolism of adipose tissue by growth hormone and the insulin-like growth factor system. Domestic Animal Endocrinology 27, 241255.Google Scholar
Mehebik, N, Jaubert, AM, Sabourault, D, Giudicelli, Y and Ribière, C 2005. Leptin-induced nitric oxide production in white adipocytes is mediated through PKA and MAP kinase activation. American Journal of Physiology. Cell Physiology 289, C379C387.Google Scholar
Pagani, S, Meazza, C, Travaglino, P, De Benedetti, F, Tinelli, C and Bozzola, M 2005. Serum cytokine levels in GH-deficient children during substitutive GH therapy. European Journal of Endocrinology 152, 207210.Google Scholar
Petersen, EW, Carey, AL, Sacchetti, M, Steinberg, GR, Macaulay, SL, Febbraio, MA and Pedersen, BK 2005. Acute IL-6 treatment increases fatty acid turnover in elderly humans in vivo and in tissue culture in vitro. American Journal of Physiology Endocrinology and Metabolism 288, E155E162.Google Scholar
Pou, KM, Massaro, JM, Hoffmann, U, Vasan, RS, Maurovich-Horvat, P, Larson, MG, Keaney, JF Jr, Meigs, JB, Lipinska, I, Kathiresan, S, Murabito, JM, O’Donnell, CJ, Benjamin, EJ and Fox, CS 2007. Visceral and subcutaneous adipose tissue volumes are cross-sectionally related to markers of inflammation and oxidative stress: the Framingham Heart Study. Circulation 11, 12341241.Google Scholar
Qu, C, Zhang, G, Zhang, L and Gong, Y 2007. Osteogenic and adipogenic potential of porcine adipose. In Vitro Cellular & Developmental Biology. Animal 43, 95100.Google Scholar
Saleri, R, Grasselli, F and Tamanini, C 2005. Effects of different culture conditions and leptin on GH mRNA expression and GH secretion by pig pituitary cells. Hormone and Metabolic Research 37, 214219.Google Scholar
Shan, T, Wu, T, Reng, Y and Wang, Y 2009. Breed difference and regulation of the porcine adipose triglyceride lipase and hormone sensitive lipase by TNFalpha. Animal Genetics 40, 863870.Google Scholar
Simons, PJ, van den Pangaart, PS, van Roomen, CP and Aerts, L 2005. Cytokine-mediated modulation of leptin and adiponectin secretion during in vitro adipogenesis: evidence that tumor necrosis factor-alpha- and interleukin-1beta-treated human preadipocytes are potent leptin producers. Cytokine 32, 94103.Google Scholar
Sørensen, MT, Chaudhuri, S, Louveau, I, Coleman, ME and Etherton, TD 1992. Growth hormone binding proteins in pig adipose tissue: number, size and effects of pGH treatment on pGH and bGH binding. Domestic Animal Endocrinology 9, 1324.Google Scholar
Tilg, H and Moschen, AR 2006. Adipocytokines: mediators linking adipose tissue, inflammation and immunity. Nature Reviews Immunology 6, 772783.Google Scholar
Trayhurn, P and Wood, IS 2004. Adipokines: inflammation and the pleiotropic role of white adipose tissue. British Journal of Nutrition 92, 347355.Google Scholar
Uronen-Hansson, H, Allen, ML, Lichtarowicz-Krynska, E, Aynsley-Green, A, Cole, TJ, Hoiden-Guthenberg, I, Fryklund, L and Klein, N 2003. Growth hormone enhances proinflammatory cytokine production by monocytes in whole blood. Growth Hormone & IGF Research 13, 282286.Google Scholar
Wallenius, K, Wallenius, V, Sunter, D, Dickson, SL and Jansson, JO 2002. Intracerebroventricular interleukin-6 treatment decreases body fat in rats. Biochemical and Biophysical Research Communications 293, 560565.Google Scholar
Zhang, Y, Proenca, R, Maffei, M, Barone, M, Leopold, L and Friedman, JM 1994. Positional cloning of the mouse obese gene and its human homologue. Nature 372, 425432.Google Scholar