Hostname: page-component-cd9895bd7-hc48f Total loading time: 0 Render date: 2024-12-27T13:07:13.542Z Has data issue: false hasContentIssue false
  • English
  • Français

Invited review: Pre- and postnatal adipose tissue development in farm animals: from stem cells to adipocyte physiology

Published online by Cambridge University Press:  06 May 2016

I. Louveau ,
M.-H. Perruchot ,
M. Bonnet  and
F. Gondret
I. Louveau*
Affiliation:
INRA, UMR1348 Pegase, F-35590 Saint-Gilles, France Agrocampus Ouest, UMR1348 Pegase, F-35000 Rennes, France
M.-H. Perruchot
Affiliation:
INRA, UMR1348 Pegase, F-35590 Saint-Gilles, France Agrocampus Ouest, UMR1348 Pegase, F-35000 Rennes, France
M. Bonnet
Affiliation:
INRA, UMR1213 Herbivores, F-63122 Saint-Genès-Champanelle, France Clermont Université, VetAgro Sup, UMR1213 Herbivores, F-63000 Clermont-Ferrand, France
F. Gondret
Affiliation:
INRA, UMR1348 Pegase, F-35590 Saint-Gilles, France Agrocampus Ouest, UMR1348 Pegase, F-35000 Rennes, France
*
†E-mail: isabelle.louveau@rennes.inra.fr
Get access

Abstract

Both white and brown adipose tissues are recognized to be differently involved in energy metabolism and are also able to secrete a variety of factors called adipokines that are involved in a wide range of physiological and metabolic functions. Brown adipose tissue is predominant around birth, except in pigs. Irrespective of species, white adipose tissue has a large capacity to expand postnatally and is able to adapt to a variety of factors. The aim of this review is to update the cellular and molecular mechanisms associated with pre- and postnatal adipose tissue development with a special focus on pigs and ruminants. In contrast to other tissues, the embryonic origin of adipose cells remains the subject of debate. Adipose cells arise from the recruitment of specific multipotent stem cells/progenitors named adipose tissue-derived stromal cells. Recent studies have highlighted the existence of a variety of those cells being able to differentiate into white, brown or brown-like/beige adipocytes. After commitment to the adipocyte lineage, progenitors undergo large changes in the expression of many genes involved in cell cycle arrest, lipid accumulation and secretory functions. Early nutrition can affect these processes during fetal and perinatal periods and can also influence or pre-determinate later growth of adipose tissue. How these changes may be related to adipose tissue functional maturity around birth and can influence newborn survival is discussed. Altogether, a better knowledge of fetal and postnatal adipose tissue development is important for various aspects of animal production, including neonatal survival, postnatal growth efficiency and health.

Keywords

adipose tissueadipocytesadult stem cellsdevelopmentlivestock
Type
Review Article
Information
animal , Volume 10 , Issue 11 , November 2016 , pp. 1839 - 1847
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

The list of older references (before 2010) is given in Supplementary Material S1.Google Scholar
Arnhold, S and Wenisch, S 2015. Adipose tissue derived mesenchymal stem cells for musculoskeletal repair in veterinary medicine. American Journal of Stem Cells 4, 1–12.Google ScholarPubMed
Asano, H, Yamada, T, Hashimoto, O, Umemoto, T, Sato, R, Ohwatari, S, Kanamori, Y, Terachi, T, Funaba, M and Matsui, T 2013. Diet-induced changes in Ucp1 expression in bovine adipose tissues. General and Comparative Endocrinology 184, 87–92.Google Scholar
Basse, AL, Dixen, K, Yadav, R, Tygesen, MP, Qvortrup, K, Kristiansen, K, Quistorff, B, Gupta, R, Wang, J and Hansen, JB 2015. Global gene expression profiling of brown to white adipose tissue transformation in sheep reveals novel transcriptional components linked to adipose remodeling. BMC Genomics 16, 215.CrossRefGoogle Scholar
Beaulieu, AD, Aalhus, JL, Williams, NH and Patience, JF 2010. Impact of piglet birth weight, birth order, and litter size on subsequent growth performance, carcass quality, muscle composition, and eating quality of pork. Journal of Animal Science 88, 2767–2778.CrossRefGoogle ScholarPubMed
Bonnet, M, Cassar-Malek, I, Chilliard, Y and Picard, B 2010. Ontogenesis of muscle and adipose tissues and their interactions in ruminants and other species. Animal 4, 1093–1109.Google Scholar
Bourin, P, Bunnell, BA, Casteilla, L, Dominici, M, Katz, AJ, March, KL, Redl, H, Rubin, JP, Yoshimura, K and Gimble, JM 2013. Stromal cells from the adipose tissue-derived stromal vascular fraction and culture expanded adipose tissue-derived stromal/stem cells: a joint statement of the International Federation for Adipose Therapeutics and Science (IFATS) and the International Society for Cellular Therapy (ISCT). Cytotherapy 15, 641–648.Google Scholar
Carberry, AE, Colditz, PB and Lingwood, BE 2010. Body composition from birth to 4.5 months in infants born to non-obese women. Pediatric Research 68, 84–88.Google Scholar
Casteilla, L, Planat-Benard, V, Laharrague, P and Cousin, B 2011. Adipose-derived stromal cells: their identity and uses in clinical trials, an update. World Journal of Stem Cells 3, 25–33.CrossRefGoogle ScholarPubMed
Cawthorn, WP, Scheller, EL and Macdougald, OA 2012. Adipose tissue stem cells meet preadipocyte commitment: going back to the future. Journal of Lipid Research 53, 227–246.Google Scholar
Chau, YY, Bandiera, R, Serrels, A, Martinez-Estrada, OM, Qing, W, Lee, M, Slight, J, Thornburn, A, Berry, R, McHaffie, S, Stimson, RH, Walker, BR, Chapuli, RM, Schedl, A and Hastie, N 2014. Visceral and subcutaneous fat have different origins and evidence supports a mesothelial source. Nature Cell Biology 16, 367–375.Google Scholar
Dodson, MV, Allen, RE, Du, M, Bergen, WG, Velleman, SG, Poulos, SP, Fernyhough-Culver, M, Wheeler, MB, Duckett, SK, Young, MR, Voy, BH, Jiang, Z and Hausman, GJ 2015. Invited Review: evolution of meat animal growth research during the past 50 years: adipose and muscle stem cells. Journal of Animal Science 93, 457–481.Google Scholar
Du, M, Wang, B, Fu, X, Yang, Q and Zhu, MJ 2015. Fetal programming in meat production. Meat Science 109, 40–47.CrossRefGoogle ScholarPubMed
Frondas-Chauty, A, Louveau, I, Le Huërou-Luron, I, Rozé, JC and Darmaun, D 2012. Air-displacement plethysmography for determining body composition in neonates: validation using live piglets. Pediatric Research 72, 26–31.Google Scholar
Giralt, M and Villarroya, F 2013. White, brown, beige/brite: different adipose cells for different functions? Endocrinology 154, 2992–3000.Google Scholar
Gondret, F, Père, MC, Tacher, S, Daré, S, Tréfeu, C, Le Huërou-Luron, I and Louveau, I 2013. Spontaneous intra-uterine growth restriction modulates the endocrine status and the developmental expression of genes in porcine fetal and neonatal adipose tissue. General and Comparative Endocrinology 194, 208–216.Google Scholar
Hausman, GJ, Basu, U, Wei, S, Hausman, DB and Dodson, MV 2014. Preadipocyte and adipose tissue differentiation in meat animals: influence of species and anatomical location. Annual Review of Animal Biosciences 2, 323–351.CrossRefGoogle ScholarPubMed
Jastroch, M and Andersson, L 2015. When pigs fly, UCP1 makes heat. Molecular Metabolism 4, 359–362.Google Scholar
Komolka, K, Albrecht, E, Wimmers, K, Michal, JJ and Maak, S 2014. Molecular heterogeneities of adipose depots – potential effects on adipose-muscle cross-talk in humans, mice and farm animals. Journal of Genomics 2, 31–44.CrossRefGoogle ScholarPubMed
Koppen, A and Kalkhoven, E 2010. Brown vs white adipocytes: the PPARgamma coregulator story. FEBS Letters 584, 3250–3259.Google Scholar
Lafontan, M 2012. Historical perspectives in fat cell biology: the fat cell as a model for the investigation of hormonal and metabolic pathways. American Journal of Physiology – Cell Physiology 302, C327–C359.Google Scholar
Lee, P, Swarbrick, MM and Ho, KK 2013. Brown adipose tissue in adult humans: a metabolic renaissance. Endocrine Reviews 34, 413–438.CrossRefGoogle ScholarPubMed
Lee, YH and Granneman, JG 2012. Seeking the source of adipocytes in adult white adipose tissues. Adipocyte 1, 230–236.Google Scholar
Ma, X, Hou, YQ, Dahanayaka, S, Satterfield, MC, Burghardt, RC, Bazer, FW and Wu, G 2015. Technical note: isolation and characterization of ovine brown adipocyte precursor cells. Journal of Animal Science 93, 2094–2099.CrossRefGoogle ScholarPubMed
Madsen, JG and Bee, G 2015. Compensatory growth feeding strategy does not overcome negative effects on growth and carcass composition of low birth weight pigs. Animal 9, 427–436.CrossRefGoogle Scholar
Mihaylova, MM, Sabatini, DM and Yilmaz, ÖH 2014. Dietary and metabolic control of stem cell function in physiology and cancer. Cell Stem Cell 14, 292–305.Google Scholar
Monaco, E, Bionaz, M, Rodriguez-Zas, S, Hurley, WL and Wheeler, MB 2012. Transcriptomics comparison between porcine adipose and bone marrow mesenchymal stem cells during in vitro osteogenic and adipogenic differentiation. PLoS One 7, e32481.Google Scholar
Obregon, MJ 2014. Adipose tissues and thyroid hormones. Frontiers in Physiology 5, 479.Google Scholar
Oñate, B, Vilahur, G, Camino-López, S, Díez-Caballero, A, Ballesta-López, C, Ybarra, J, Moscatiello, F, Herrero, J and Badimon, L 2013. Stem cells isolated from adipose tissue of obese patients show changes in their transcriptomic profile that indicate loss in stemcellness and increased commitment to an adipocyte-like phenotype. BMC Genomics 14, 625.CrossRefGoogle Scholar
Oñate, B, Vilahur, G, Ferrer-Lorente, R, Ybarra, J, Díez-Caballero, A, Ballesta-López, C, Moscatiello, F, Herrero, J and Badimon, L 2012. The subcutaneous adipose tissue reservoir of functionally active stem cells is reduced in obese patients. FASEB Journal 26, 4327–4336.Google Scholar
Perruchot, MH, Lefaucheur, L, Barreau, C, Casteilla, L and Louveau, I 2013. Age-related changes in the features of porcine adult stem cells isolated from adipose tissue and skeletal muscle. American Journal of Physiology – Cell Physiology 305, C728–C738.Google Scholar
Pisani, DF, Clement, N, Loubat, A, Plaisant, M, Sacconi, S, Kurzenne, JY, Desnuelle, C, Dani, C and Dechesne, CA 2010. Hierarchization of myogenic and adipogenic progenitors within human skeletal muscle. Stem Cells 28, 2182–2194.Google Scholar
Pope, M, Budge, H and Symonds, ME 2014. The developmental transition of ovine adipose tissue through early life. Acta Physiologica (Oxf) 210, 20–30.Google Scholar
Ranera, B, Lyahyai, J, Romero, A, Vázquez, FJ, Remacha, AR, Bernal, ML, Zaragoza, P, Rodellar, C and Martín-Burriel, I 2011. Immunophenotype and gene expression profiles of cell surface markers of mesenchymal stem cells derived from equine bone marrow and adipose tissue. Veterinary Immunology and Immunopathology 144, 147–154.Google Scholar
Rehfeldt, C, Lefaucheur, L, Block, J, Stabenow, B, Pfuhl, R, Otten, W, Metges, CC and Kalbe, C 2012a. Limited and excess protein intake of pregnant gilts differently affects body composition and cellularity of skeletal muscle and subcutaneous adipose tissue of newborn and weanling piglets. European Journal of Nutrition 51, 151–165.Google Scholar
Rehfeldt, C, Stabenow, B, Pfuhl, R, Block, J, Nürnberg, G, Otten, W, Metges, CC and Kalbe, C 2012b. Effects of limited and excess protein intakes of pregnant gilts on carcass quality and cellular properties of skeletal muscle and subcutaneous adipose tissue in fattening pigs. Journal of Animal Science 90, 184–196.CrossRefGoogle ScholarPubMed
Ren, Y, Wu, H, Zhou, X, Wen, J, Jin, M, Cang, M, Guo, X, Wang, Q, Liu, D and Ma, Y 2012. Isolation, expansion, and differentiation of goat adipose-derived stem cells. Research in Veterinary Science 93, 404–411.Google Scholar
Restelli, L, Codrea, MC, Savoini, G, Ceciliani, F and Bendixen, E 2014. LC-MS/MS analysis of visceral and subcutaneous adipose tissue proteomes in young goats with focus on innate immunity and inflammation related proteins. Journal of Proteomics 108, 295–305.CrossRefGoogle ScholarPubMed
Romacho, T, Elsen, M, Röhrborn, D and Eckel, J 2014. Adipose tissue and its role in organ crosstalk. Acta Physiologica (Oxf) 210, 733–753.Google Scholar
Rozemuller, H, Prins, HJ, Naaijkens, B, Staal, J, Bühring, HJ and Martens, AC 2010. Prospective isolation of mesenchymal stem cells from multiple mammalian species using cross-reacting anti-human monoclonal antibodies. Stem Cells Development 19, 1911–1921.Google Scholar
Sampaio, RV, Chiaratti, MR, Santos, DC, Bressan, FF, Sangalli, JR, Sá, AL, Silva, TV, Costa, NN, Cordeiro, MS, Santos, SS, Ambrosio, CE, Adona, PR, Meirelles, FV, Miranda, MS and Ohashi, OM 2015. Generation of bovine (Bos indicus) and buffalo (Bubalus bubalis) adipose tissue derived stem cells: isolation, characterization, and multipotentiality. Genetics and Molecular Research 14, 53–62.CrossRefGoogle ScholarPubMed
Sanchez-Gurmaches, J and Guertin, DA 2014. Adipocyte lineages: tracing back the origins of fat. Biochimica and Biophysica Acta 1842, 340–351.Google Scholar
Sarr, O, Gondret, F, Jamin, A, Le Huërou-Luron, I and Louveau, I 2011. A high-protein neonatal formula induces a temporary reduction of adiposity and changes later adipocyte physiology. American Journal Physiology – Regulatory Integrative and Comparative Physiology 300, R387–R397.Google Scholar
Sarr, O, Louveau, I, Le Huërou-Luron, I and Gondret, F 2012. Adipose tissue proteomes of intrauterine growth-restricted piglets artificially reared on a high-protein neonatal formula. Journal of Nutrition and Biochemistry 23, 1417–1424.Google Scholar
Symonds, ME, Pope, M and Budge, H 2015. The ontogeny of brown adipose tissue. Annual Review of Nutrition 35, 295–320.Google Scholar
Taga, H, Chilliard, Y, Meunier, B, Chambon, C, Picard, B, Zingaretti, C, Cinti, S and Bonnet, M 2012a. Cellular and molecular-large scale features of fetal adipose tissue: is bovine perirenal adipose tissue brown? Journal of Cellular Physiology 227, 1688–1700.Google Scholar
Taga, H, Chilliard, Y, Picard, B, Zingaretti, MC and Bonnet, M 2012b. Foetal bovine intermuscular adipose tissue exhibits histological and metabolic features of brown and white adipocytes during the last third of pregnancy. Animal 6, 641–649.Google Scholar
Uezumi, A, Fukada, S, Yamamoto, N, Takeda, S and Tsuchida, K 2010. Mesenchymal progenitors distinct from satellite cells contribute to ectopic fat cell formation in skeletal muscle. Nature Cell Biology 12, 143–152.Google Scholar
Villarroya, J, Cereijo, R and Villarroya, F 2013. An endocrine role for brown adipose tissue? American Journal of Physiology – Endocrinology and Metabolism 305, E567–E572.Google Scholar
Wu, J, Boström, P, Sparks, LM, Ye, L, Choi, JH, Giang, AH, Khandekar, M, Virtanen, KA, Nuutila, P, Schaart, G, Huang, K, Tu, H, van Marken Lichtenbelt, WD, Hoeks, J, Enerbäck, S, Schrauwen, P and Spiegelman, BM 2012. Beige adipocytes are a distinct type of thermogenic fat cell in mouse and human. Cell 150, 366–376.Google Scholar
Zhang, J, Suh, Y, Choi, YM, Ahn, J, Davis, ME and Lee, K 2014. Differential expression of cyclin G2, cyclin-dependent kinase inhibitor 2C and peripheral myelin protein 22 genes during adipogenesis. Animal 8, 800–809.Google Scholar
Supplementary material: File

Louveau supplementary material

Louveau supplementary material 1

Download Louveau supplementary material(File)
File 43.6 KB