Hostname: page-component-76fb5796d-vvkck Total loading time: 0 Render date: 2024-04-25T12:55:34.045Z Has data issue: false hasContentIssue false
  • English
  • Français

Effect of lipid fraction of digested milk from different sources in mature 3T3-L1 adipocyte

Published online by Cambridge University Press:  07 February 2019

Antonella Santillo ,
Lucia Figliola ,
Mariangela Caroprese ,
Rosaria Marino ,
Maria dʼApolito ,
Ida Giardino  and
Marzia Albenzio
Antonella Santillo*
Affiliation:
Department of the Sciences of Agriculture, Food and Environment (SAFE), University of Foggia, Via Napoli, 25, 71122 Foggia, Italy
Lucia Figliola
Affiliation:
Department of the Sciences of Agriculture, Food and Environment (SAFE), University of Foggia, Via Napoli, 25, 71122 Foggia, Italy
Mariangela Caroprese
Affiliation:
Department of the Sciences of Agriculture, Food and Environment (SAFE), University of Foggia, Via Napoli, 25, 71122 Foggia, Italy
Rosaria Marino
Affiliation:
Department of the Sciences of Agriculture, Food and Environment (SAFE), University of Foggia, Via Napoli, 25, 71122 Foggia, Italy
Maria dʼApolito
Affiliation:
Department of Medical and Surgical Sciences, University of Foggia, Viale Pinto, 1, 71122 Foggia, Italy
Ida Giardino
Affiliation:
Department of Clinical and Experimental Medicine, University of Foggia, Viale Pinto, 1, 71122 Foggia, Italy
Marzia Albenzio
Affiliation:
Department of the Sciences of Agriculture, Food and Environment (SAFE), University of Foggia, Via Napoli, 25, 71122 Foggia, Italy
*
Author for correspondence: Antonella Santillo, Email: antonella.santillo@unifg.it
Get access Rights & Permissions [Opens in a new window]

Abstract

We evaluated the effect of in vitro digested milk on mature adipocytes 3T3-L1, paying particular attention to its fatty acid composition, and comparing human (HM), donkey (DM), bovine (BM), ovine (OM), caprine (CM) and formula (FM) milk. Cellular viability, apoptosis, oxidative response and gene expression levels of NF-κB p65, HMGB1, SREBP-1c and FAS were evaluated. Digested milk treatments significantly reduced 3T3-L1 mature adipocytes viability and caspase activity compared with control group, but no significant differences were observed among different sources of digested milk. In all digested milk samples, ROS level was higher than the control, however, the digested human and formula milk showed lower levels of ROS than DM, BM, OM and CM samples. Lower capacity of HM and FM to induce oxidative stress in mature adipocytes was ascribed to the peculiar free fatty acids profile of digested milk samples. All milk treatments elicited a significant over-expression of NF-κB p65 in 3T3-L1 adipocytes compared to the control; the lowest gene expression was found in HM, BM, OM and CM, the highest in FM and an intermediate behavior was shown in DM. All digested milk treatments influenced the gene expression of SRBP-1c with FM and HM showing the highest levels. For FAS expression, BM showed the highest level, OM and CM intermediate and FM, HM and DM the lowest levels, however HM and DM had comparable levels to the control.

Keywords

3T3-L1 adipocytedigested milkfatty acidshuman milkmilking species
Type
Research Article
Information
Journal of Dairy Research , Volume 86 , Issue 1 , February 2019 , pp. 129 - 133
Copyright
Copyright © Hannah Dairy Research Foundation 2019 

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

Ajuwon, KM and Spurlock, ME (2005) Palmitate activates the NF-kappaB transcription factor and induces IL-6 and TNFalpha expression in 3T3-L1 adipocytes. The Journal of Nutrition 135, 1841–1846.Google Scholar
Baret, P, Septembre-Malaterre, A, Rigoulet, M, d'Hellencourt, CL, Priault, M, Gonthier, MP and Devin, A (2013) Dietary polyphenols preconditioning protects 3T3-L1 preadipocytes from mitochondrial alterations induced by oxidative stress. The international Journal of Biochemistry & Cell Biology 45, 167–174.Google Scholar
Carrière, A, Carmona, MC, Fernandez, Y, Rigoulet, M, Wenger, RH, Pénicaud, L and Casteilla, L (2004) Mitochondrial reactive oxygen species control the transcription factor CHOP-10/GADD153 and adipocyte differentiation: a mechanism for hypoxia-dependent effect. Journal of Biological Chemistry 279, 40462–40469.Google Scholar
Carrière, A, Fernandez, Y, Rigoulet, M, Pénicaud, L and Casteilla, L (2003) Inhibition of preadipocyte proliferation by mitochondrial reactive oxygen species. FEBS Letters 550, 163–167.Google Scholar
Chang, WT, Wu, CH and Hsu, CL (2015) Diallyl trisulphide inhibits adipogenesis in 3T3-L1 adipocytes through lipogenesis, fatty acid transport, and fatty acid oxidation pathways. Journal of Functional Foods 16, 414–422.Google Scholar
D'Apolito, M, Du, X, Zong, H, Catucci, A, Maiuri, L, Trivisano, T, Pettoello-Mantovani, M, Campanozzi, A, Raia, V, Pessin, JE, Brownlee, M and Giardino, I (2010) Urea-induced ROS generation causes insulin resistance in mice with chronic renal failure. Clinical Investigation 120, 203–213.Google Scholar
D'Apolito, M, Colia, AL, Lasalvia, M, Capozzi, V, Falcone, MP, Pettoello-Mantovani, M, Brownlee, M, Maffione, AB and Giardino, I (2017) Urea-induced ROS accelerate senescence in endothelial progenitor cells. Atherosclerosis 263, 127–136.Google Scholar
Devle, H, Ulleberg, EK, Naess-Andresen, CF, Rukke, EO, Vegarud, GE and Ekeberg, D (2014) Reciprocal interacting effects of proteins and lipids during ex vivo digestion of bovine milk. International Dairy Journal 36, 6–13.Google Scholar
Fernyhough, ME, Okine, E, Hausman, G, Vierck, JL and Dodson, MV (2007) PPAR and GLUT-4 expression as developmental regulators/markers for preadipocyte differentiation into an adipocyte. Domestic Animal Endocrinology 33, 367–378.Google Scholar
Fink, SL and Cookson, BT (2005) Minireview apoptosis, pyroptosis, and necrosis: mechanistic description of dead and dying eukaryotic cells. Infection and Immunity 20, 1907–1916.Google Scholar
Fujisawa, Y, Yamaguchi, R, Nagata, E, Satake, E, Sano, S, Matsushita, R, Kitsuta, K, Nakashima, S, Nakanishi, T, Nakagawa, Y and Ogata, T (2013) The lipid fraction of human milk initiates adipocyte differentiation in 3T3-L1 cells. Early Human Development 89, 713–719.Google Scholar
Furukawa, S, Fujita, T, Shimabukuro, M, Iwaki, M, Yamada, Y, Nakajima, Y, Nakayama, O, Makishima, M, Matsuda, M and Shimomura, I (2017) Increased oxidative stress in obesity and its impact on metabolic syndrome. The Journal of clinical investigation 114, 1752–1761.Google Scholar
Guenther Boden, MD (2011) Obesity, insulin resistance and free fatty acids. Current Opinion in Endocrinology, Diabetes and Obesity 18, 139–143.Google Scholar
Gunasekaran, MK, Viranaicken, W, Girard, AC, Festy, F, Cesari, M, Roche, R and Hoareau, L (2013) Inflammation triggers high mobility group box 1 (HMGB1) secretion in adipose tissue, a potential link to obesity. Cytokine 64, 103–111.Google Scholar
Guo, W, Xie, W and Han, J (2006) Modulation of adipocyte lipogenesis by octanoate: involvement of reactive oxygen species. Nutrition & Metabolism 3, 30.Google Scholar
Han, JC, Lawlor, DA and Kimm, SY (2010) Childhood obesity. Lancet 375, 1737–1748.Google Scholar
Jang, J, Jung, Y, Seo, SJ, Kim, SM, Shim, YJ, Cho, SH, Chung, SI and Yoon, Y (2017) Berberine activates AMPK to suppress proteolytic processing, nuclear translocation and target DNA binding of SREBP-1c in 3T3-L1 adipocytes. Molecular Medicine Reports 15, 4139–4147.Google Scholar
Kennedy, A, Martinez, K, Chuang, CC, LaPoint, K and McIntosh, M (2009) Saturated fatty acid-mediated inflammation and insulin resistance in adipose tissue: mechanisms of action and implications. The Journal of Nutrition 139, 1–4.Google Scholar
Kusunoki, C, Yang, L, Yoshizaki, T, Nakagawa, F, Ishikado, A, Kondo, M, Morino, K, Sekine, O, Ugi, S, Nishio, Y, Kashiwagi, A and Maegawa, H (2013) Omega-3 polyunsaturated fatty acid has an anti-oxidant effect via Nrf-2/HO-1 pathway in 3T3-L1 adipocytes. Biochemical and Biophysical Research Communication 430, 225–230.Google Scholar
Lin, Y, Berg, AH, Iyengar, P, Lam, TK, Giacca, A, Combs, TP, Rajala, MW, Du, X, Rollman, B, Li, W and Hawkins, M (2005) The hyperglycemia-induced inflammatory response in adipocytes the role of reactive oxygen species. Journal of Biological Chemistry 280, 4617–4626.Google Scholar
Minekus, M, Alminger, M, Alvito, P, Ballance, S, Bohn, T, Bourlieu, C, Carriere, F, Boutrou, R, Corredig, M, Dupont, D, Dufour, C, Egger, L, Golding, M, Karakaya, S, Kirkhus, B, Le Feunteun, S, Lesmes, U, Macierzanka, A, Mackie, A, Marze, S, McClements, DJ, Menard, O, Recio, I, Santos, CN, Singh, RP, Vegarud, GE, Wickham, MSJ, Weitschies, W and Brodkorb, A (2014) A standardised static in vitro digestion method suitable for food-An international consensus. Food & Function 5, 1113–1124.Google Scholar
Mittal, M, Siddiqui, MR, Tran, K, Reddy, SP and Malik, AB (2014) Reactive oxygen species in inflammation and tissue injury. Antioxidants & Redox Signaling 20, 1126–1167.Google Scholar
Navarro-Yepes, J, Burns, M, Anandhan, A, Khalimonchuk, O, del Razo, LM, Quintanilla-Vega, B, Pappa, A, Panayiotidis, MI and Franco, R (2014) Oxidative stress, redox signaling, and autophagy: cell death vs. Survival. Antioxidants & Redox Signaling 21, 66–85.Google Scholar
Rigoulet, M, Yoboue, ED and Devin, A (2011) Mitochondrial ROS generation and its regulation: mechanisms involved in H2O2 signaling. Antioxidants and Redox Signalling 14, 459–468.Google Scholar
Romacho, T, Glosse, P, Richter, I, Elsen, M, Schoemaker, MH, van Tol, EA and Eckel, J (2015) Nutritional ingredients modulate adipokine secretion and inflammation in human primary adipocytes. Nutrients 7, 865–886.Google Scholar
Santillo, A, Figliola, L, Ciliberti, MG, Caroprese, M, Marino, R and Albenzio, M (2018) Focusing on fatty acids profile in milk from different species after in vitro digestion. Journal of Dairy Research 85, 257–262.Google Scholar
SAS Institute (2011) SAS User's Guide: Statistics. Version 9.2 ed. Cary, NC: SAS Inst. Inc.Google Scholar
Sergeev, IN (2009) 1, 25-Dihydroxyvitamin D3 induces Ca2+-mediated apoptosis in adipocytes via activation of calpain and caspase-12. Biochemical and Biophysical Research Communications 384, 18–21.Google Scholar
Shimomura, I, Hammer, RE, Richardson, JA, Ikemoto, S, Bashmakov, Y, Goldstein, JL and Brown, MS (1998) Insulin resistance and diabetes mellitus in transgenic mice expressing nuclear SREBP-1c in adipose tissue: model for congenital generalized lipodystrophy. Genes & Development 12, 3182–3194.Google Scholar
Spalding, KL, Arner, E, Westermark, PO, Bernard, S, Buchholz, BA, Bergmann, O, Blomqvist, L, Hoffstedt, J, Näslund, E, Britton, T, Concha, H, Hassan, M, Rydén, M, Frisén, J and Arner, P (2008) Dynamics of fat cell turnover in humans. Nature 453, 783–787.Google Scholar
Suganami, T, Tanimoto-Koyama, K, Nishida, J, Itoh, M, Yuan, X, Mizuarai, S, Kotani, H, Yamaoka, S, Miyake, K, Aoe, S, Kamei, Y and Ogawa, Y (2007) Role of the toll-like receptor 4/NF-κB pathway in saturated fatty acid–induced inflammatory changes in the interaction between adipocytes and macrophages. Arteriosclerosis, Thrombosis, and Vascular Biology 27, 84–91.Google Scholar
Tang, W, Zeve, D, Suh, JM, Bosnakovski, D, Kyba, M, Hammer, RE, Tallquist, MD and Graff, JM (2008) White fat pro-genitor cells reside in the adipose vasculature. Science 322, 583–586.Google Scholar
Wang, X and Hai, C (2015) Redox modulation of adipocyte differentiation: Hypothesis of “Redox Chain” and novel insights into intervention of adipogenesis and obesity. Free Radical Biology & Medicine 89, 99–125.Google Scholar
Wang, AS, Xu, CW, Xie, HY, Yao, AJ, Shen, YZ, Wan, JJ, Zhang, HQ, Fu, JF, Chen, ZM, Zou, ZQ, Li, D and Zhang, XH (2016) DHA induces mitochondria-mediated 3T3-L1 adipocyte apoptosis by down-regulation of Akt and ERK. Journal of Functional Foods 21, 517–524.Google Scholar
Yang, JP, Hori, M, Takahashi, N, Kawabe, T, Kato, H and Okamoto, T (1999) NF-kappaB subunit p65 binds to 53BP2 and inhibits cell death induced by 53BP2. Oncogene 18, 5177–5186.Google Scholar
Supplementary material: PDF

Santillo et al. supplementary material

Santillo et al. supplementary material 1

Download Santillo et al. supplementary material(PDF)
PDF 369 KB