Animal Science

The impact of housing conditions on porcine mesenchymal stromal/stem cell populations differ between adipose tissue and skeletal muscle

10.24072/pcjournal.109 - Peer Community Journal, Volume 2 (2022), article no. e25.

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Background. In pigs, the ratio between lean mass and fat mass in the carcass determines production efficiency and is strongly influenced by the number and size of cells in tissues. During growth, the increase in the number of cells results from the recruitment of different populations of multipotent mesenchymal stromal/stem cells (MSCs) residing in the tissues. We hypothesized that the impact of hygiene of housing conditions during growth on the proportions of MSCs in adipose tissue and skeletal muscle may differ between pigs with different residual feed intake (RFI), a measure of feed efficiency. Methods. At the age of 12 weeks, Large White pigs from two lines divergently selected for low and high RFI were housed in two contrasting hygiene conditions (good vs poor). After six weeks, pigs were slaughtered (n = 30; 5-9/group). Samples of subcutaneous adipose tissue and longissimus skeletal muscle were collected, and cells from the stromal vascular fraction (SVF), which includes mesenchymal stromal/stem cell populations, were isolated from each tissue. Adipose and muscle cell populations from the SVF were phenotyped by flow cytometry using antibodies that targeted different cell surface markers (CD45 to separate hematopoietic cells from MSCs; CD34, CD38, CD56 and CD140a to identify MSC populations with adipogenic and/or myogenic potential). Results. Adipose tissue and muscle shared some common MSC populations although MSC diversity was higher in muscle than in adipose tissue. In muscle, the CD45-CD56+CD34-CD140a+ and CD45-CD56+CD34+CD140a+ cell populations were abundant. Of these two cell populations, only the proportions of CD45-CD56+CD34+CD140a+ cells increased (P ≤ 0.05) in pigs housed in poor hygiene as compared with pigs in good hygiene conditions. For the CD45-CD56-CD34- cell population, present in low proportion, there was an interaction between hygiene condition and genetic line (P < 0.05) with a decrease in low RFI pigs housed in poor hygiene conditions. In adipose tissue, the two abundant MSC populations were CD45-CD56-CD34- and CD45-CD56+CD34-. The proportion of CD45-CD56-CD34- cells increased (P < 0.05) whereas the proportion of CD45-CD56+CD34- tended to decrease (P < 0.1) in pigs housed in poor conditions. This study shows that the proportions of some MSC populations were affected by hygiene of housing conditions in a tissue-dependent manner in pigs of both RFI lines. It suggests that MSCs may play a significant role in adipose tissue and skeletal muscle homeostasis and may influence later growth and body composition in growing animals.

Published online:
DOI: 10.24072/pcjournal.109
Quéméner, Audrey 1; Dessauge, Frédéric 1; Perruchot, Marie-Hélène 1; Le Floc’h, Nathalie 1; Louveau, Isabelle 1

1 PEGASE, INRAE, Institut Agro, Saint-Gilles, France
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     title = {The impact of housing conditions on porcine mesenchymal stromal/stem cell populations differ between adipose tissue and skeletal muscle},
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Quéméner, Audrey; Dessauge, Frédéric; Perruchot, Marie-Hélène; Le Floc’h, Nathalie; Louveau, Isabelle. The impact of housing conditions on porcine mesenchymal stromal/stem cell populations differ between adipose tissue and skeletal muscle. Peer Community Journal, Volume 2 (2022), article  no. e25. doi : 10.24072/pcjournal.109.

Peer reviewed and recommended by PCI : 10.24072/pci.animsci.100011

[1] Bourin, P.; Bunnell, B. A.; Casteilla, L.; Dominici, M.; Katz, A. J.; March, K. L.; Redl, H.; Rubin, J. P.; Yoshimura, K.; Gimble, J. M. 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, Volume 15 (2013) no. 6, pp. 641-648 | Article

[2] Calle, A.; Barrajón-Masa, C.; Gómez-Fidalgo, E.; Martín-Lluch, M.; Cruz-Vigo, P.; Sánchez-Sánchez, R.; Ramírez, M. Á. Iberian pig mesenchymal stem/stromal cells from dermal skin, abdominal and subcutaneous adipose tissues, and peripheral blood: in vitro characterization and migratory properties in inflammation, Stem Cell Research &amp; Therapy, Volume 9 (2018) no. 1 | Article

[3] Carrière, A.; Jeanson, Y.; Côté, J.-A.; Dromard, C.; Galinier, A.; Menzel, S.; Barreau, C.; Dupuis-Coronas, S.; Arnaud, E.; Girousse, A.; Cuminetti, V.; Paupert, J.; Cousin, B.; Sengenes, C.; Koch-Nolte, F.; Tchernof, A.; Casteilla, L. Identification of the ectoenzyme CD38 as a marker of committed preadipocytes, International Journal of Obesity, Volume 41 (2017) no. 10, pp. 1539-1546 | Article

[4] Chatelet, A.; Gondret, F.; Merlot, E.; Gilbert, H.; Friggens, N.; Le Floc’h, N. Impact of hygiene of housing conditions on performance and health of two pig genetic lines divergent for residual feed intake, Animal, Volume 12 (2018) no. 2, pp. 350-358 | Article

[5] Cho, D. S.; Doles, J. D. Skeletal Muscle Progenitor Cell Heterogeneity, Advances in Experimental Medicine and Biology, Springer International Publishing, Cham, 2019, pp. 179-193 | Article

[6] Colditz, I. G.; Hine, B. C. Resilience in farm animals: biology, management, breeding and implications for animal welfare, Animal Production Science, Volume 56 (2016) no. 12 | Article

[7] Cousin, B.; Casteilla, L.; Laharrague, P.; Luche, E.; Lorsignol, A.; Cuminetti, V.; Paupert, J. Immuno-metabolism and adipose tissue: The key role of hematopoietic stem cells, Biochimie, Volume 124 (2016), pp. 21-26 | Article

[8] Crisan, M.; Yap, S.; Casteilla, L.; Chen, C.-W.; Corselli, M.; Park, T. S.; Andriolo, G.; Sun, B.; Zheng, B.; Zhang, L.; Norotte, C.; Teng, P.-N.; Traas, J.; Schugar, R.; Deasy, B. M.; Badylak, S.; Bűhring, H.-J.; Giacobino, J.-P.; Lazzari, L.; Huard, J.; Péault, B. A Perivascular Origin for Mesenchymal Stem Cells in Multiple Human Organs, Cell Stem Cell, Volume 3 (2008) no. 3, pp. 301-313 | Article

[9] De Carvalho, F. G.; Justice, J. N.; Freitas, E. C. d.; Kershaw, E. E.; Sparks, L. M. Adipose Tissue Quality in Aging: How Structural and Functional Aspects of Adipose Tissue Impact Skeletal Muscle Quality, Nutrients, Volume 11 (2019) no. 11 | Article

[10] De clercq, L.; Mourot, J.; Genart, C.; Davidts, V.; Boone, C.; Remacle, C. An anti-adipocyte monoclonal antibody is cytotoxic to porcine preadipocytes in vitro and depresses the development of pig adipose tissue., Journal of Animal Science, Volume 75 (1997) no. 7 | Article

[11] Dodson, M. V.; Allen, R. E.; Du, M.; Bergen, W. G.; Velleman, S. G.; Poulos, S. P.; Fernyhough-Culver, M.; Wheeler, M. B.; Duckett, S. K.; Young, M. R. I.; Voy, B. H.; Jiang, Z.; Hausman, G. J. INVITED REVIEW: Evolution of meat animal growth research during the past 50 years: Adipose and muscle stem cells, Journal of Animal Science, Volume 93 (2015) no. 2, pp. 457-481 | Article

[12] Dominici, M.; Le Blanc, K.; Mueller, I.; Slaper-Cortenbach, I.; Marini, F.; Krause, D.; Deans, R.; Keating, A.; Prockop, D.; Horwitz, E. Minimal criteria for defining multipotent mesenchymal stromal cells. The International Society for Cellular Therapy position statement, Cytotherapy, Volume 8 (2006) no. 4, pp. 315-317 | Article

[13] Gilbert, H.; Bidanel, J.-P.; Gruand, J.; Caritez, J.-C.; Billon, Y.; Guillouet, P.; Lagant, H.; Noblet, J.; Sellier, P. Genetic parameters for residual feed intake in growing pigs, with emphasis on genetic relationships with carcass and meat quality traits, Journal of Animal Science, Volume 85 (2007) no. 12, pp. 3182-3188 | Article

[14] Girousse, A.; Mathieu, M.; Sastourné-Arrey, Q.; Monferran, S.; Casteilla, L.; Sengenès, C. Endogenous Mobilization of Mesenchymal Stromal Cells: A Pathway for Interorgan Communication?, Frontiers in Cell and Developmental Biology, Volume 8 (2021) | Article

[15] Han, T. T. Y.; Walker, J. T.; Grant, A.; Dekaban, G. A.; Flynn, L. E. Preconditioning Human Adipose-Derived Stromal Cells on Decellularized Adipose Tissue Scaffolds Within a Perfusion Bioreactor Modulates Cell Phenotype and Promotes a Pro-regenerative Host Response, Frontiers in Bioengineering and Biotechnology, Volume 9 (2021) | Article

[16] Johnson, S. E. GROWTH AND DEVELOPMENT SYMPOSIUM: Participation of adult tissue-restricted stem cells to livestock growth and development1, Journal of Animal Science, Volume 91 (2013) no. 1, pp. 57-58 | Article

[17] Knap, P. W.; Doeschl-Wilson, A. Why breed disease-resilient livestock, and how?, Genetics Selection Evolution, Volume 52 (2020) no. 1 | Article

[18] Laurens, C.; Louche, K.; Sengenes, C.; Coué, M.; Langin, D.; Moro, C.; Bourlier, V. Adipogenic progenitors from obese human skeletal muscle give rise to functional white adipocytes that contribute to insulin resistance, International Journal of Obesity, Volume 40 (2016) no. 3, pp. 497-506 | Article

[19] Lecourt, S.; Marolleau, J.-P.; Fromigué, O.; Vauchez, K.; Andriamanalijaona, R.; Ternaux, B.; Lacassagne, M.-N.; Robert, I.; Boumédiene, K.; Chéreau, F.; Marie, P.; Larghéro, J.; Fiszman, M.; Vilquin, J.-T. Characterization of distinct mesenchymal-like cell populations from human skeletal muscle in situ and in vitro, Experimental Cell Research, Volume 316 (2010) no. 15, pp. 2513-2526 | Article

[20] Lee, Y.-H.; Granneman, J. G. Seeking the source of adipocytes in adult white adipose tissues, Adipocyte, Volume 1 (2012) no. 4, pp. 230-236 | Article

[21] Lefaucheur, L. A second look into fibre typing – Relation to meat quality, Meat Science, Volume 84 (2010) no. 2, pp. 257-270 | Article

[22] Lewis, F. C.; Henning, B. J.; Marazzi, G.; Sassoon, D.; Ellison, G. M.; Nadal-Ginard, B. Porcine Skeletal Muscle-Derived Multipotent PW1pos/Pax7neg Interstitial Cells: Isolation, Characterization, and Long-Term Culture, Stem Cells Translational Medicine, Volume 3 (2014) no. 6, pp. 702-712 | Article

[23] Louveau, I.; Perruchot, M.-H.; Bonnet, M.; Gondret, F. Invited review: Pre- and postnatal adipose tissue development in farm animals: from stem cells to adipocyte physiology, Animal, Volume 10 (2016) no. 11, pp. 1839-1847 | Article

[24] Mackey, A. L.; Magnan, M.; Chazaud, B.; Kjaer, M. Human skeletal muscle fibroblasts stimulate <i>in vitro</i> myogenesis and <i>in vivo</i> muscle regeneration, The Journal of Physiology, Volume 595 (2017) no. 15, pp. 5115-5127 | Article

[25] Mihaylova, M. M.; Sabatini, D. M.; Yilmaz, Ö. H. Dietary and Metabolic Control of Stem Cell Function in Physiology and Cancer, Cell Stem Cell, Volume 14 (2014) no. 3, pp. 292-305 | Article

[26] Patience, J. F.; Rossoni-Serão, M. C.; Gutiérrez, N. A. A review of feed efficiency in swine: biology and application, Journal of Animal Science and Biotechnology, Volume 6 (2015) no. 1 | Article

[27] Perruchot, M.-H.; Dessauge, F.; Gondret, F.; Louveau, I. Response of adult stem cell populations to a high-fat/high-fiber diet in skeletal muscle and adipose tissue of growing pigs divergently selected for feed efficiency, European Journal of Nutrition, Volume 60 (2020) no. 5, pp. 2397-2408 | Article

[28] Perruchot, M.-H.; Lefaucheur, L.; Barreau, C.; Casteilla, L.; Louveau, I. Age-related changes in the features of porcine adult stem cells isolated from adipose tissue and skeletal muscle, American Journal of Physiology-Cell Physiology, Volume 305 (2013) no. 7 | Article

[29] Pisani, D. F.; Clement, N.; Loubat, A.; Plaisant, M.; Sacconi, S.; Kurzenne, J.-Y.; Desnuelle, C.; Dani, C.; Dechesne, C. A. Hierarchization of Myogenic and Adipogenic Progenitors Within Human Skeletal Muscle, Stem Cells, Volume 28 (2010) no. 12, pp. 2182-2194 | Article

[30] Pisani, D. F.; Dechesne, C. A.; Sacconi, S.; Delplace, S.; Belmonte, N.; Cochet, O.; Clement, N.; Wdziekonski, B.; Villageois, A. P.; Butori, C.; Bagnis, C.; Di Santo, J. P.; Kurzenne, J.-Y.; Desnuelle, C.; Dani, C. Isolation of a Highly Myogenic CD34-Negative Subset of Human Skeletal Muscle Cells Free of Adipogenic Potential, Stem Cells, Volume 28 (2010) no. 4, pp. 753-764 | Article

[31] Rauw, W.; Kanis, E.; Noordhuizen-Stassen, E.; Grommers, F. Undesirable side effects of selection for high production efficiency in farm animals: a review, Livestock Production Science, Volume 56 (1998) no. 1, pp. 15-33 | Article

[32] Relaix, F.; Bencze, M.; Borok, M. J.; Der Vartanian, A.; Gattazzo, F.; Mademtzoglou, D.; Perez-Diaz, S.; Prola, A.; Reyes-Fernandez, P. C.; Rotini, A.; Taglietti, Perspectives on skeletal muscle stem cells, Nature Communications, Volume 12 (2021) no. 1 | Article

[33] Shenoy P., S.; Bose, B. Hepatic perivascular mesenchymal stem cells with myogenic properties, Journal of Tissue Engineering and Regenerative Medicine, Volume 12 (2017) no. 3 | Article

[34] Sierżant, K.; Perruchot, M.-H.; Merlot, E.; Le Floc’h, N.; Gondret, F. Tissue-specific responses of antioxidant pathways to poor hygiene conditions in growing pigs divergently selected for feed efficiency, BMC Veterinary Research, Volume 15 (2019) no. 1 | Article

[35] Sillence, M. Technologies for the control of fat and lean deposition in livestock, The Veterinary Journal, Volume 167 (2004) no. 3, pp. 242-257 | Article

[36] Silva, K. R.; Baptista, L. S. Adipose-derived stromal/stem cells from different adipose depots in obesity development, World Journal of Stem Cells, Volume 11 (2019) no. 3, pp. 147-166 | Article

[37] Stavrakakis, S.; Loisel, F.; Sakkas, P.; Le Floc’h, N.; Kyriazakis, I.; Stewart, G.; Montagne, L. A systematic literature mapping and meta-analysis of animal-based traits as indicators of production diseases in pigs, Animal, Volume 13 (2019) no. 7, pp. 1508-1518 | Article

[38] Uezumi, A.; Fukada, S.; Yamamoto, N.; Ikemoto-Uezumi, M.; Nakatani, M.; Morita, M.; Yamaguchi, A.; Yamada, H.; Nishino, I.; Hamada, Y.; Tsuchida, K. Identification and characterization of PDGFRα+ mesenchymal progenitors in human skeletal muscle, Cell Death &amp; Disease, Volume 5 (2014) no. 4 | Article

[39] Uezumi, A.; Fukada, S.-i.; Yamamoto, N.; Takeda, S.; Tsuchida, K. Mesenchymal progenitors distinct from satellite cells contribute to ectopic fat cell formation in skeletal muscle, Nature Cell Biology, Volume 12 (2010) no. 2, pp. 143-152 | Article

[40] Uezumi, A.; Ikemoto-Uezumi, M.; Tsuchida, K. Roles of nonmyogenic mesenchymal progenitors in pathogenesis and regeneration of skeletal muscle, Frontiers in Physiology, Volume 5 (2014) | Article

[41] Vauchez, K.; Marolleau, J.-P.; Schmid, M.; Khattar, P.; Chapel, A.; Catelain, C.; Lecourt, S.; Larghéro, J.; Fiszman, M.; Vilquin, J.-T. Aldehyde Dehydrogenase Activity Identifies a Population of Human Skeletal Muscle Cells With High Myogenic Capacities, Molecular Therapy, Volume 17 (2009) no. 11, pp. 1948-1958 | Article

[42] Wilschut, K. J.; Jaksani, S.; Van Den Dolder, J.; Haagsman, H. P.; Roelen, B. A. Isolation and characterization of porcine adult muscle-derived progenitor cells, Journal of Cellular Biochemistry, Volume 105 (2008) no. 5, pp. 1228-1239 | Article

[43] Wilschut, K. J.; van Tol, H. T.; Arkesteijn, G. J.; Haagsman, H. P.; Roelen, B. A. Alpha 6 integrin is important for myogenic stem cell differentiation, Stem Cell Research, Volume 7 (2011) no. 2, pp. 112-123 | Article

[44] Wosczyna, M. N.; Konishi, C. T.; Perez Carbajal, E. E.; Wang, T. T.; Walsh, R. A.; Gan, Q.; Wagner, M. W.; Rando, T. A. Mesenchymal Stromal Cells Are Required for Regeneration and Homeostatic Maintenance of Skeletal Muscle, Cell Reports, Volume 27 (2019) no. 7 | Article

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