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Differential characterization of myogenic satellite cells with linolenic and retinoic acid in the presence of thiazolidinediones from prepubertal Korean black goats

  • Subi, S. ;
  • Lee, S.J. ;
  • Shiwani, S. ;
  • Singh, N.K.
  • Received : 2017.04.02
  • Accepted : 2017.08.31
  • Published : 2018.03.01

Abstract

Objective: Myogenic satellite cells were isolated from semitendinosus muscle of prepubertal Korean black goat to observe the differential effect of linolenic and retinoic acid in thepresence of thiazolidinediones (TZD) and also to observe the production insulin sensitive preadipocyte. Methods: Cells were characterized for their stemness with cluster of differentiation 34 (CD34), CD13, CD106, CD44, Vimentin surface markers using flow cytometry. Cells characterized themselves as possessing significant (p<0.05) levels of CD13, CD34, CD106, Vimentin revealing their stemness potential. Goat myogenic satellite cells also exhibited CD44, indicating that they possessed a % of stemness factors of adipose lineage apart from their inherent stemness of paxillin factors 3/7. Results: Cells during proliferation stayed absolutely and firmly within the myogenic fate without any external cues and continued to show a significant (p<0.05) fusion index % to express myogenic differentiation, myosin heavy chain, and smooth muscle actin in 2% horse serum. However, confluent myogenic satellite cells were the ones easily turning into adipogenic lineage. Intriguingly, upregulation in adipose specific genetic markers such as peroxisome proliferation-activated receptor ${\gamma}$, adiponectin, lipoprotein lipase, and CCAAT/enhancer binding protein ${\alpha}$ were observed and confirmed in all given treatments. However, the amount of adipogenesis was found to be statistically significant (p<0.01) with linolenic acid as compared to retinoic acid in combination with TZD's. Conclusion: Retinoic acid was found to produce smaller preadipocytes which have been assumed to have insulin sensitization and hence retinoic acid could be used as a potential agent to sensitize tissues to insulin in combination with TZD's to treat diabetic conditions in humans and animals in future.

Keywords

Goat Muscle Satellite Cells;Thiazolidinedione;Linolenic Acid;Retinoic Acids;Adipogenesis

References

  1. Yang YB, Pandurangan M, Jeong D, Hwang I. The effect of troglitazone on lipid accumulation and related gene expression in Hanwoo muscle satellite cell. J Physiol Biochem 2013;69:97-109.
  2. Singh NK, Chae HS, Hwang IH, et al. Transdifferentiation of porcine satellite cells to adipoblasts with ciglitizone. J Anim Sci 2007;85:1126-35. https://doi.org/10.2527/jas.2006-524
  3. Chambon P. A decade of molecular biology of retinoic acid receptors. FASEB J 1996;10:940-54. https://doi.org/10.1096/fasebj.10.9.8801176
  4. Schug TT, Berry DC, Shaw NS, Travis SN, Noy N. Opposing effects of retinoic acid on cell growth result from alternate activation of two different nuclear receptors. Cell 2007;129:723-33.
  5. Relaix F, Zammit PS. Satellite cells are essential for skeletal muscle regeneration: the cell on the edge returns centre stage. Development 2012;139:2845-56. https://doi.org/10.1242/dev.069088
  6. Lukjanenko L, Brachat S, Pierrel E, Lach-Trifilieff E, Feige JN. Genomic profiling reveals that transient adipogenic activation is a hallmark of mouse models of skeletal muscle regeneration. PLoS ONE 2013;8:e71084. https://doi.org/10.1371/journal.pone.0071084
  7. Danoviz ME, Reuveni ZY. Skeletal muscle satellite cells: background and methods for isolation and analysis in a primary culture system. Methods Mol Biol 2012;798:21-52.
  8. Folgiero V, Migliano E, Tedesco M, et al. Purification and characterization of adipose-derived stem cells from patients with lipoaspirate transplant. Cell Transplant 2010;19:1225-35.
  9. Vidal M, Kilroy G, Johnson J, et al. Cell growth characteristics and differentiation frequency of adherent equine bone marrowderived mesenchymal stromal cells: adipogenic and osteogenic capacity. Vet Surg 2006;35:601-10. https://doi.org/10.1111/j.1532-950X.2006.00197.x
  10. McNeil M. Adiopocyte staining with oil-red-O. Baton Rouge, LA, USA: Pennington Laboratory. Molecular Endocrinology, Pennington Biomedical Research Centre; 2005.
  11. Ieronimakis N, Balasundaram G, Rainey S, et al. Absence of CD34 on murine skeletal muscle satellite cells marks a reversible state of activation during acute injury. PLoS ONE 2010;5:e10920. https://doi.org/10.1371/journal.pone.0010920
  12. Suzawa K, Kobayashi M, Sakai Y, et al. Preferential induction of peripheral lymph node addressin on high endothelial venulelike vessels in the active phase of ulcerative colitis. Am J Gastroenterol 2007;102:1499-509. https://doi.org/10.1111/j.1572-0241.2007.01189.x
  13. Reza AM, Shiwani S, Singh NK, et al. Keratinocyte growth factor and thiazolidinediones and linolenic acid differentiate characterized mammary fat pad adipose stem cells isolated from prepubertal Korean black goat to epithelial and adipogenic lineage. In Vitro Cell Dev Biol Anim 2014;50:194-206. https://doi.org/10.1007/s11626-013-9690-5
  14. Jankowski RJ, Deasy BM, Huard J. Muscle-derived stem cells. Gene Ther 2002;9:642-7. https://doi.org/10.1038/sj.gt.3301719
  15. Jesse TL, La Chance R, Iademarco MF, Dean DC. Interferon regulatory factor-2 is a transcriptional activator in muscle where it regulates expression of vascular cell adhesion molecule-1. J Cell Biol 1998;140:1265-76. https://doi.org/10.1083/jcb.140.5.1265
  16. Runembert I, Queffeulou G, Federici P, et al. Vimentin affects localization and activity of sodium-glucose cotransporter SGLT1 in membrane rafts. J Cell Sci 2002;115:713-24.
  17. Gallanti A, Prelle A, Moggio M, et al. Desmin and vimentin as markers of regeneration in muscle diseases. Acta Neuropathol 1992;85:88-92. https://doi.org/10.1007/BF00304637
  18. Starkey JD, Yamamoto M, Yamamoto S, Goldhamer DJ. Skeletal muscle satellite cells are committed to myogenesis and do not spontaneously adopt nonmyogenic fates. J Histochem Cytochem 2011;59:33-46. https://doi.org/10.1369/jhc.2010.956995
  19. Ishibashi J, Perry RL, Asakura A, Rudnicki MA. MyoD induces myogenic differentiation through cooperation of its NH2 - and COOH-terminal regions. J Cell Biol 2005;171:471-82. https://doi.org/10.1083/jcb.200502101
  20. Yablonka-Reuveni Z, Rivera AJ. Temporal expression of regulatory and structural muscle proteins during myogenesis of satellite cells on isolated adult rat fibers. Dev Biol 1994;164:588-603.
  21. Springer ML, Ozawa CR, Blau HM. Transient production of ${\alpha}$-smooth muscle actin by skeletal myoblasts during differentiation in culture and following intramuscular implantation. Cell Motil Cytoskeleton 2002;51:177-86. https://doi.org/10.1002/cm.10022
  22. Talmadge RJ, Roy RR. Electrophoretic separation of rat skeletal muscle myosin heavy-chain isoforms. J Appl Physiol 1993;75:2337-40. https://doi.org/10.1152/jappl.1993.75.5.2337
  23. Koch U, Lehal R, Radtke F. Stem cells living with a Notch. Development 2013;140:689-704. https://doi.org/10.1242/dev.080614
  24. Narkar VA, Downes M, Yu RT, et al. AMPK and PPARdelta agonists are exercise mimetics. Cell 2008;134:405-15. https://doi.org/10.1016/j.cell.2008.06.051
  25. Gervois PI, Torra P, Fruchart JC, Staels B. Regulation of lipid and lipoprotein metabolism by PPAR activators. Clin Chem Lab Med 2000;38:3-11.
  26. Hallakou S, Doare L, Foufelle F, et al. Pioglitazone induces in vivo adipocyte differentiation in the obese Zuckerfa/fa rat. Diabetes 1997;46:1393-9. https://doi.org/10.2337/diab.46.9.1393
  27. Rebrin K, Steil GM, Mittelman SD, Bergman RN. Causal linkage between insulin suppression of lipolysis and suppression of liver glucose output in dogs. J Clin Invest 1996;98:741-9. https://doi.org/10.1172/JCI118846
  28. Foellmi-Adams LA, Wyse BM, Herron D, Nedergaard J, Kletzien RF. Induction of uncoupling protein in brown adipose tissue: synergy between norepinephrine and pioglitazone, an insulinsensitizing agent. Biochem Pharmacol 1996;52:693-701. https://doi.org/10.1016/0006-2952(96)00345-0
  29. Mukherjee R, Davies PJ, Crombi DL, et al. Sensitization of diabetic and obese mice to insulin by retinoid X receptor agonists. Nature 1997;386:407-10.
  30. Kubota N, Terauchi Y, Miki H, et al. $PPAR{\gamma}$ mediates highfat diet-induced adipocyte hypertrophy and insulin resistance. Mol Cell 1999;4:597-609.
  31. Jarrar MH, Baranova A. $PPAR{\gamma}$ activation by thiazolidinediones (TZDs) may modulate breast carcinoma outcome: the importance of interplay with $TGF{\beta}$ signaling. J Cell Mol Med 2007; 11:71-87. https://doi.org/10.1111/j.1582-4934.2007.00003.x
  32. Dai LH, Xiong YZ, Deng CY, et al. Association of the A-G polymorphism in porcine adiponectin gene with fat deposition and carcass traits. Asian-Australas J Anim Sci 2006;19:779-83. https://doi.org/10.5713/ajas.2006.779
  33. Fu Y, Luo N, Klein RL, Garvey WT. Adiponectin promotes adipocyte differentiation, insulin sensitivity, and lipid accumulation. J Lipid Res 2005;46:1369-79. https://doi.org/10.1194/jlr.M400373-JLR200
  34. Kolehmainen M, Vidal H, Ohisalo JJ, et al. Hormone sensitive lipase expression and adipose tissue metabolism show gender difference in obese subjects after weight loss. Int J Obes Relat Metab Disord 2002;26:6-16. https://doi.org/10.1038/sj.ijo.0801858
  35. Gregoire FM, Smas CM, Sul HS. Understanding adipocyte differentiation. Physiol Rev 1998;78:783-809.
  36. Darlington GJ, Ross SE, MacDougald OA. The role of C/EBP genes in adipocyte differentiation. J Biol Chem 1998;273:30057-60. https://doi.org/10.1074/jbc.273.46.30057
  37. Rosen ED. The transcriptional basis of adipocyte development. Prostaglandins Leukot Essent Fatty Acids 2005;73:31-4. https://doi.org/10.1016/j.plefa.2005.04.004
  38. Ohyama M, Matsuda K, Torii S, et al. The interaction between vitamin A and thiazolidinedione on bovine adipocyte differentiation in primary culture. J Anim Sci 1998;76:61-5. https://doi.org/10.2527/1998.76161x
  39. Zizola CF, Frey SK, Jitngarmkusol S, et al. Cellular retinolbinding protein type I (CRBP-I) regulates adipogenesis. Mol Cell Biol 2010;30:3412-20.

Acknowledgement

Supported by : National Research Foundation of Korea