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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

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Abstract

Purpose

The control of body composition by genetics and dietary nutrients is of the upmost importance for both human and animal physiology. Adult stem cells (aSC) may represent a relevant level of tissue adaptation. The purpose of this study was to determine the impact of macronutrient composition on aSC populations isolated from adipose tissue or muscle in growing pigs.

Methods

Pigs from two lines divergently selected for feed efficiency were fed ad libitum either a high-fat/high-fiber (HF) diet or a low-fat/low-fiber (LF) diet (n = 6 per line and diet) from 74 to 132 days of age. Stroma vascular cells were isolated from adipose tissue and muscle and characterized with cell surface markers.

Results

In both lines, pigs fed the HF diet exhibited a reduced adiposity (P < 0.001) compared with pigs fed the LF diet. In the four groups, CD90 and PDGFRα markers were predominantly expressed in adipose cells, whereas CD90 and CD56 markers were highly expressed in muscle cells. In adipose tissue, the proportions of CD56+/PDGFRα + and of CD90+/PDGFRα + cells were lower (P < 0.05) in HF pigs than in LF pigs. On the opposite, in muscle, these proportions were higher (P < 0.001) in HF pigs.

Conclusion

This study indicates that dietary nutrients affected the relative proportions of CD56+/PDGFRα + cells with opposite effects between muscle and adipose tissue. These cell populations exhibiting adipogenic potential in adipose tissue and myogenic potential in muscle may be a target to modulate body composition.

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References

  1. Hilton TN, Tuttle LJ, Bohnert KL, Mueller MJ, Sinacore DR (2008) Excessive adipose tissue infiltration in skeletal muscle in individuals with obesity, diabetes mellitus, and peripheral neuropathy: association with performance and function. Phys Ther 88:1336–1344. https://doi.org/10.2522/ptj.20080079

    Article  PubMed  PubMed Central  Google Scholar 

  2. Sillence MN (2004) Technologies for the control of fat and lean deposition in livestock. Vet J 167:242–257. https://doi.org/10.1016/j.tvjl.2003.10.020

    Article  CAS  PubMed  Google Scholar 

  3. Minguell JJ, Erices A, Conget P (2001) Mesenchymal stem cells. Exp Biol Med (Maywood) 226:507–520. https://doi.org/10.1177/153537020122600603

    Article  CAS  Google Scholar 

  4. Mihaylova MM, Sabatini DM, Yilmaz OH (2014) Dietary and metabolic control of stem cell function in physiology and cancer. Cell Stem Cell 14(3):292–305. https://doi.org/10.1016/j.stem.2014.02.008

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  5. Onate B, Vilahur G, Ferrer-Lorente R, Ybarra J, Diez-Caballero A, Ballesta-Lopez C, Moscatiello F, Herrero J, Badimon L (2012) The subcutaneous adipose tissue reservoir of functionally active stem cells is reduced in obese patients. FASEB J 26:4327–4336. https://doi.org/10.1096/fj.12-207217

    Article  CAS  Google Scholar 

  6. Perez LM, Bernal A, de Lucas B, San Martin N, Mastrangelo A, Garcia A, Barbas C, Galvez BG (2015) Altered metabolic and stemness capacity of adipose tissue-derived stem cells from obese mouse and human. PLoS ONE 10:e0123397. https://doi.org/10.1371/journal.pone.0123397

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  7. Tachtsis B, Camera D, Lacham-Kaplan O (2018) Potential roles of n – 3 PUFAs during skeletal muscle growth and regeneration. Nutrients 10:309. https://doi.org/10.3390/nu10030309

    Article  CAS  PubMed Central  Google Scholar 

  8. Cerletti M, Jang YC, Finley LW, Haigis MC, Wagers AJ (2012) Short-term calorie restriction enhances skeletal muscle stem cell function. Cell Stem Cell 10:515–519. https://doi.org/10.1016/j.stem.2012.04.002

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  9. Yan H, Potu R, Lu H, Vezzoni de Almeida V, Stewart T, Ragland D, Armstrong A, Adeola O, Nakatsu CH, Ajuwon KM (2013) Dietary fat content and fiber type modulate hind gut microbial community and metabolic markers in the pig. PLoS ONE 8:e59581. https://doi.org/10.1371/journal.pone.0059581

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  10. Brockman DA, Chen X, Gallaher DD (2014) High-viscosity dietary fibers reduce adiposity and decrease hepatic steatosis in rats fed a high-fat diet. J Nutr 144:1415–1422. https://doi.org/10.3945/jn.114.191577

    Article  CAS  PubMed  Google Scholar 

  11. Gilbert H, Bidanel JP, Gruand J, Caritez JC, Billon Y, Guillouet P, Lagant H, Noblet J, Sellier P (2007) Genetic parameters for residual feed intake in growing pigs, with emphasis on genetic relationships with carcass and meat quality traits. J Anim Sci 85:3182–3188. https://doi.org/10.2527/jas.2006-590

    Article  CAS  PubMed  Google Scholar 

  12. Gondret F, Louveau I, Mourot J, Duclos MJ, Lagarrigue S, Gilbert H, van Milgen J (2014) Dietary energy sources affect the partition of body lipids and the hierarchy of energy metabolic pathways in growing pigs differing in feed efficiency. J Anim Sci 92:4865–4877. https://doi.org/10.2527/jas.2014-7995

    Article  CAS  PubMed  Google Scholar 

  13. Gondret F, Vincent A, Houee-Bigot M, Siegel A, Lagarrigue S, Louveau I, Causeur D (2016) Molecular alterations induced by a high-fat high-fiber diet in porcine adipose tissues: variations according to the anatomical fat location. BMC Genomics 17:120. https://doi.org/10.1186/s12864-016-2438-3

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  14. Carninci P (2014) Genomics: mice in the ENCODE spotlight. Nature 515:346–347. https://doi.org/10.1038/515346a

    Article  CAS  PubMed  Google Scholar 

  15. Dodson MV, Hausman GJ, Guan L, Du M, Rasmussen TP, Poulos SP, Mir P, Bergen WG, Fernyhough ME, McFarland DC, Rhoads RP, Soret B, Reecy JM, Velleman SG, Jiang Z (2010) Lipid metabolism, adipocyte depot physiology and utilization of meat animals as experimental models for metabolic research. Int J Biol Sci 6:691–699. https://doi.org/10.7150/ijbs.6.691

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  16. Litten-Brown JC, Corson AM, Clarke L (2010) Porcine models for the metabolic syndrome, digestive and bone disorders: a general overview. Animal 4:899–920. https://doi.org/10.1017/S1751731110000200

    Article  CAS  PubMed  Google Scholar 

  17. Nielsen KL, Hartvigsen ML, Hedemann MS, Laerke HN, Hermansen K, Bach Knudsen KE (2014) Similar metabolic responses in pigs and humans to breads with different contents and compositions of dietary fibers: a metabolomics study. Am J Clin Nutr 99:941–949. https://doi.org/10.3945/ajcn.113.07472

    Article  CAS  PubMed  Google Scholar 

  18. De Clercq L, Mourot J, Genart C, Davidts V, Boone C, Remacle C (1997) An anti-adipocyte monoclonal antibody is cytotoxic to porcine preadipocytes in vitro and depresses the development of pig adipose tissue. J Anim Sci 75:1791–1797. https://doi.org/10.2527/1997.7571791x

    Article  Google Scholar 

  19. Perruchot MH, Ecolan P, Sorensen IL, Oksbjerg N, Lefaucheur L (2012) In vitro characterization of proliferation and differentiation of pig satellite cells. Differentiation 84:322–329. https://doi.org/10.1016/j.diff.2012.08.001

    Article  CAS  PubMed  Google Scholar 

  20. Perruchot MH, Lefaucheur L, Barreau C, Casteilla L, Louveau I (2013) Age-related changes in the features of porcine adult stem cells isolated from adipose tissue and skeletal muscle. Am J Physiol Cell Physiol 305(7):C728–C738. https://doi.org/10.1152/ajpcell.00151.2013

    Article  CAS  PubMed  Google Scholar 

  21. Joe AW, Yi L, Natarajan A, Le Grand F, So L, Wang J, Rudnicki MA, Rossi FM (2010) Muscle injury activates resident fibro/adipogenic progenitors that facilitate myogenesis. Nat Cell Biol 12:153–163. https://doi.org/10.1038/ncb2015

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  22. Uezumi A, Fukada S, Yamamoto N, Takeda S, Tsuchida K (2010) Mesenchymal progenitors distinct from satellite cells contribute to ectopic fat cell formation in skeletal muscle. Nat Cell Biol 12:143–152. https://doi.org/10.1038/ncb2014

    Article  CAS  PubMed  Google Scholar 

  23. Uezumi A, Fukada S, Yamamoto N, Ikemoto-Uezumi M, Nakatani M, Morita M, Yamaguchi A, Yamada H, Nishino I, Hamada Y, Tsuchida K (2014) Identification and characterization of PDGFRalpha+ mesenchymal progenitors in human skeletal muscle. Cell Death Dis 5:e1186. https://doi.org/10.1038/cddis.2014.161

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  24. Lee YH, Granneman JG (2012) Seeking the source of adipocytes in adult white adipose tissues. Adipocyte 1:230–236. https://doi.org/10.4161/adip.20804

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  25. Lee YH, Petkova AP, Mottillo EP, Granneman JG (2012) In vivo identification of bipotential adipocyte progenitors recruited by beta3-adrenoceptor activation and high-fat feeding. Cell Metab 15:480–491. https://doi.org/10.1016/j.cmet.2012.03.009

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  26. Arrighi N, Moratal C, Clement N, Giorgetti-Peraldi S, Peraldi P, Loubat A, Kurzenne JY, Dani C, Chopard A, Dechesne CA (2015) Characterization of adipocytes derived from fibro/adipogenic progenitors resident in human skeletal muscle. Cell Death Dis 6:e1733. https://doi.org/10.1038/cddis.2015.79

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  27. Zimmerlin L, Donnenberg VS, Pfeifer ME, Meyer EM, Peault B, Rubin JP, Donnenberg AD (2010) Stromal vascular progenitors in adult human adipose tissue. Cytometry A 77:22–30. https://doi.org/10.1002/cyto.a.20813

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  28. Pisani DF, Clement N, Loubat A, Plaisant M, Sacconi S, Kurzenne JY, Desnuelle C, Dani C, Dechesne CA (2010) Hierarchization of myogenic and adipogenic progenitors within human skeletal muscle. Stem Cells 28:2182–2194. https://doi.org/10.1002/stem.537

    Article  PubMed  Google Scholar 

  29. Iwayama T, Steele C, Yao L, Dozmorov MG, Karamichos D, Wren JD, Olson LE (2015) PDGFRalpha signaling drives adipose tissue fibrosis by targeting progenitor cell plasticity. Genes Dev 29:1106–1119. https://doi.org/10.1101/gad.260554.115

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  30. Capkovic KL, Stevenson S, Johnson MC, Thelen JJ, Cornelison DD (2008) Neural cell adhesion molecule (NCAM) marks adult myogenic cells committed to differentiation. Exp Cell Res 314:1553–1565. https://doi.org/10.1016/j.yexcr.2008.01.021

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  31. Meln I, Wolff G, Gajek T, Koddebusch J, Lerch S, Harbrecht L, Hong W, Bayindir-Buchhalter I, Krunic D, Augustin HG, Vegiopoulos A (2019) Dietary calories and lipids synergistically shape adipose tissue cellularity during postnatal growth. Mol Metab 24:139–148. https://doi.org/10.1016/j.molmet.2019.03.012

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  32. Silva KR, Baptista LS (2019) Adipose-derived stromal/stem cells from different adipose depots in obesity development. World J Stem Cells 11:147–166. https://doi.org/10.4252/wjsc.v11.i3.147

    Article  PubMed  PubMed Central  Google Scholar 

  33. Kulenkampff E, Wolfrum C (2018) Proliferation of nutrition sensing preadipocytes upon short term HFD feeding. Adipocyte:1–10. Adipocyte 8:16–25. https://doi.org/10.1080/21623945.2018.1521229

    Article  PubMed  PubMed Central  Google Scholar 

  34. Pincu Y, Huntsman HD, Zou K, De Lisio M, Mahmassani ZS, Munroe MR, Garg K, Jensen T, Boppart MD (2016) Diet-induced obesity regulates adipose-resident stromal cell quantity and extracellular matrix gene expression. Stem Cell Res 17:181–190. https://doi.org/10.1016/j.scr.2016.07.002

    Article  CAS  PubMed  Google Scholar 

  35. Fiorotto ML, Davis TA (2018) Critical windows for the programming effects of early-life nutrition on skeletal muscle mass. Nestle Nutr Inst Workshop Ser. 89:25–35. https://doi.org/10.1159/000486490

    Article  PubMed  PubMed Central  Google Scholar 

  36. Mostyn A, Symonds ME (2009) Early programming of adipose tissue function: a large-animal perspective. Proc Nutr Soc 68:393–400. https://doi.org/10.1017/S002966510999022X

    Article  PubMed  Google Scholar 

  37. Choe SS, Huh JY, Hwang IJ, Kim JI, Kim JB (2016) Adipose tissue remodeling: its role in energy metabolism and metabolic disorders. Front Endocrinol (Lausanne) 7:30. https://doi.org/10.3389/fendo.2016.00030

    Article  Google Scholar 

  38. Jang H, Kim M, Lee S, Kim J, Woo DC, Kim KW, Song K, Lee I (2016) Adipose tissue hyperplasia with enhanced adipocyte-derived stem cell activity in Tc1(C8orf4)-deleted mice. Sci Rep 6:35884. https://doi.org/10.1038/srep35884

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  39. Girousse A, Gil-Ortega M, Bourlier V, Bergeaud C, Sastourne-Arrey Q, Moro C, Barreau C, Guissard C, Vion J, Arnaud E, Pradere JP, Juin N, Casteilla L, Sengenes C (2019) The release of adipose stromal cells from subcutaneous adipose tissue regulates ectopic intramuscular adipocyte deposition. Cell Rep 27:323–333. https://doi.org/10.1016/j.celrep.2019.03.038(e325)

    Article  CAS  PubMed  Google Scholar 

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Acknowledgmeents

The authors’ responsibilities were as follows—MHP, FG and IL designed the research and had primary responsibility for the final content; MHP conducted the research; MHP and FD analyzed the data; MHP, FD, FG, and IL wrote the paper; and all authors read and approved the final manuscript. The authors thank H. Gilbert (GenPhySE, INRAE, 31326 Castanet-Tolosan, France), and Y. Billon and A. Priet (GenESI, INRAE, 17700 Surgères, France) for line selection. They are also grateful to P. Roger and J. Delamarre for animal care, G. Guillemois for diet preparation, J. Liger and J.F. Rouault for animal slaughter procedures, and F. Mayeur and C. Tréfeu for their help in sample collection and/or laboratory analyzes (PEGASE, INRAE). Animal design was granted by the French National Research Agency (Agence Nationale de la Recherche, ANR-11-SVSE7004 FatInteger).

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Authors and Affiliations

  1. PEGASE, INRAE, Institut Agro, 35590, Saint Gilles, France

    Marie-Hélène Perruchot, Frédéric Dessauge, Florence Gondret & Isabelle Louveau

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  1. Marie-Hélène Perruchot
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  2. Frédéric Dessauge
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Correspondence to Marie-Hélène Perruchot.

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Perruchot, MH., Dessauge, F., Gondret, F. et al. 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. Eur J Nutr 60, 2397–2408 (2021). https://doi.org/10.1007/s00394-020-02418-7

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  • DOI: https://doi.org/10.1007/s00394-020-02418-7

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