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Protective effect of platelet-rich plasma against cold ischemia-induced apoptosis of canine adipose-derived mesenchymal stem cells

  • Suji Shin (Department of Veterinary Surgery, College of Veterinary Medicine, Kyungpook National University) ;
  • Sung-Eon Kim (Department of Veterinary Surgery, College of Veterinary Medicine, Kyungpook National University) ;
  • Seong-Won An (Department of Veterinary Surgery, College of Veterinary Medicine, Kyungpook National University) ;
  • Seong-Mok Jeong (Department of Veterinary Surgery, College of Veterinary Medicine, Chungnam National University) ;
  • Young-Sam Kwon (Department of Veterinary Surgery, College of Veterinary Medicine, Kyungpook National University)
  • Received : 2023.09.18
  • Accepted : 2024.01.01
  • Published : 2024.03.31

Abstract

This study was performed to assess the antiapoptotic effect of canine platelet-rich plasma (PRP) treated on the canine adipose-derived mesenchymal stem cells (cMSCs) under cold ischemic conditions. The effect of preventing apoptosis of cMSCs was evaluated in the apoptotic condition induced by cold ischemic injury in vitro. To determine the progression of apoptosis, the changes in cell nucleus were observed using 4',6-diamidino-2-phenylindole (DAPI) fluorescence staining. In addition, we examined the mitochondrial membrane potential (MMP) and caspase-3 activity. When the cold hypoxic injury was applied to cMSCs, the apoptotic change was observed by DAPI staining, mitochondrial staining for MMP, and caspase-3 assay. PRP significantly decreased the number of apoptotic cells. Nuclear shrinkage and fragmentation of apoptotic cells in control groups were observed by DAPI staining. The MMP was recovered by the treatment of PRP. In addition, when the luminescence intensity was measured for caspase-3 activity, the value was significantly higher in the PRP treated groups than the control groups. The results of this study showed that the PRP may have a beneficial effect on apoptosis induced by cold ischemic injury.

Keywords

Acknowledgement

This study was supported by the Basic Science Research Program through the National Research Foundation of Korea (NRF), funded by the Ministry of Education, Science and Technology (2021R1F1A1064483).

References

  1. Johnson EO, Kamilaris TC, Chrousos GP, Gold PW. Mechanisms of stress: a dynamic overview of hormonal and behavioral homeostasis. Neurosci Biobehav Rev 1992;16:115-130. 
  2. Sahin E, Gumuslu S. Cold-stress-induced modulation of antioxidant defence: role of stressed conditions in tissue injury followed by protein oxidation and lipid peroxidation. Int J Biometeorol 2004;48:165-171. 
  3. Venditti P, De Rosa R, Di Meo S. Effect of cold-induced hyperthyroidism on H2O2 production and susceptibility to stress conditions of rat liver mitochondria. Free Radic Biol Med 2004;36:348-358. 
  4. Nakayama K, Kataoka N. Regulation of gene expression under hypoxic conditions. Int J Mol Sci 2019;20:3278. 
  5. Pugh CW, Ratcliffe PJ. New horizons in hypoxia signaling pathways. Exp Cell Res 2017;356:116-121. 
  6. Kim JY, Park JH. ROS-dependent caspase-9 activation in hypoxic cell death. FEBS Lett 2003;549:94-98. 
  7. Galan A, Garcia-Bermejo L, Troyano A, Vilaboa NE, Fernandez C, de Blas E, Aller P. The role of intracellular oxidation in death induction (apoptosis and necrosis) in human promonocytic cells treated with stress inducers (cadmium, heat, X-rays). Eur J Cell Biol 2001;80:312-320. 
  8. Ren L, Song ZJ, Cai QW, Chen RX, Zou Y, Fu Q, Ma YY. Adipose mesenchymal stem cell-derived exosomes ameliorate hypoxia/serum deprivation-induced osteocyte apoptosis and osteocyte-mediated osteoclastogenesis in vitro. Biochem Biophys Res Commun 2019;508:138-144. 
  9. Blagojevic DP. Antioxidant systems in supporting environmental and programmed adaptations to low temperatures. Cryo Letters 2007;28:137-150. 
  10. Finkel T, Holbrook NJ. Oxidants, oxidative stress and the biology of ageing. Nature 2000;408:239-247. 
  11. Deng S, Yang Y, Han Y, Li X, Wang X, Li X, Zhang Z, Wang Y. UCP2 inhibits ROS-mediated apoptosis in A549 under hypoxic conditions. PLoS One 2012;7:e30714. 
  12. Solaini G, Baracca A, Lenaz G, Sgarbi G. Hypoxia and mitochondrial oxidative metabolism. Biochim Biophys Acta 2010;1797:1171-1177. 
  13. Li SC, Acevedo J, Wang L, Jiang H, Luo J, Pestell RG, Loudon WG, Chang AC. Mechanisms for progenitor cell-mediated repair for ischemic heart injury. Curr Stem Cell Res Ther 2012;7:2-14. 
  14. Mates JM, Segura JA, Alonso FJ, Marquez J. Oxidative stress in apoptosis and cancer: an update. Arch Toxicol 2012;86:1649-1665. 
  15. Elmore S. Apoptosis: a review of programmed cell death. Toxicol Pathol 2007;35:495-516. 
  16. Norbury CJ, Hickson ID. Cellular responses to DNA damage. Annu Rev Pharmacol Toxicol 2001;41:367-401. 
  17. Mates JM, Segura JA, Alonso FJ, Marquez J. Intracellular redox status and oxidative stress: implications for cell proliferation, apoptosis, and carcinogenesis. Arch Toxicol 2008;82:273-299. 
  18. Sinha K, Das J, Pal PB, Sil PC. Oxidative stress: the mitochondria-dependent and mitochondria-independent pathways of apoptosis. Arch Toxicol 2013;87:1157-1180. 
  19. Kaufmann SH, Earnshaw WC. Induction of apoptosis by cancer chemotherapy. Exp Cell Res 2000;256:42-49. 
  20. Kerr JF, Wyllie AH, Currie AR. Apoptosis: a basic biological phenomenon with wide-ranging implications in tissue kinetics. Br J Cancer 1972;26:239-257. 
  21. Cao W, Guo XW, Chen K, Xu RX, Zheng HZ, Wang J. Inhibition of hypoxia and serum deprivation-induced apoptosis by salvianolic acid in rat mesenchymal stem cells. J Tradit Chin Med 2012;32:222-228. 
  22. Yuan T, Guo SC, Han P, Zhang CQ, Zeng BF. Applications of leukocyte- and platelet-rich plasma (L-PRP) in trauma surgery. Curr Pharm Biotechnol 2012;13:1173-1184. 
  23. Yun S, Ku SK, Kwon YS. Adipose-derived mesenchymal stem cells and platelet-rich plasma synergistically ameliorate the surgical-induced osteoarthritis in Beagle dogs. J Orthop Surg Res 2016;11:9. 
  24. Metcalf KB, Mandelbaum BR, McIlwraith CW. Application of platelet-rich plasma to disorders of the knee joint. Cartilage 2013;4:295-312. 
  25. Uraloglu M, Ural A, Efe G, Yulug E, Livaoglu M, Karacal N. The effect of platelet-rich plasma on the zone of stasis and apoptosis in an experimental burn model. Plast Surg (Oakv) 2019;27:173-181. 
  26. Peerbooms JC, Sluimer J, Bruijn DJ, Gosens T. Positive effect of an autologous platelet concentrate in lateral epicondylitis in a double-blind randomized controlled trial: platelet-rich plasma versus corticosteroid injection with a 1-year follow-up. Am J Sports Med 2010;38:255-262. 
  27. Asjid R, Faisal T, Qamar K, Khan SA, Khalil A, Zia MS. Platelet-rich plasma-induced inhibition of chondrocyte apoptosis directly affects cartilage thickness in osteoarthritis. Cureus 2019;11:e6050. 
  28. Tsai WC, Yu TY, Chang GJ, Lin LP, Lin MS, Pang JS. Platelet-rich plasma releasate promotes regeneration and decreases inflammation and apoptosis of injured skeletal muscle. Am J Sports Med 2018;46:1980-1986. 
  29. Zhu Y, Yuan M, Meng HY, Wang AY, Guo QY, Wang Y, Peng J. Basic science and clinical application of platelet-rich plasma for cartilage defects and osteoarthritis: a review. Osteoarthritis Cartilage 2013;21:1627-1637. 
  30. Park YG, Han SB, Song SJ, Kim TJ, Ha CW. Platelet-rich plasma therapy for knee joint problems: review of the literature, current practice and legal perspectives in Korea. Knee Surg Relat Res 2012;24:70-78. 
  31. Intini G. The use of platelet-rich plasma in bone reconstruction therapy. Biomaterials 2009;30:4956-4966. 
  32. Freitag J, Wickham J, Shah K, Tenen A. Effect of autologous adipose-derived mesenchymal stem cell therapy in the treatment of an osteochondral lesion of the ankle. BMJ Case Rep 2020;13:e234595. 
  33. Mifune Y, Matsumoto T, Takayama K, Ota S, Li H, Meszaros LB, Usas A, Nagamune K, Gharaibeh B, Fu FH, Huard J. The effect of platelet-rich plasma on the regenerative therapy of muscle derived stem cells for articular cartilage repair. Osteoarthritis Cartilage 2013;21:175-185. 
  34. Kim SA, Ryu HW, Lee KS, Cho JW. Application of platelet-rich plasma accelerates the wound healing process in acute and chronic ulcers through rapid migration and upregulation of cyclin A and CDK4 in HaCaT cells. Mol Med Rep 2013;7:476-480. 
  35. Kanemaru H, Kajihara I, Yamanaka K, Igata T, Makino T, Masuguchi S, Fukushima S, Jinnin M, Ihn H. Platelet-rich plasma therapy is effective for the treatment of refractory skin ulcers in patients with systemic sclerosis. Mod Rheumatol 2015;25:660-661. 
  36. Kawakami T, Takeuchi S, Okano T, Inoue H, Soma Y. Therapeutic effect of autologous platelet-rich plasma (PRP) on recalcitrant cutaneous ulcers in livedoid vasculopathy. JAAD Case Rep 2015;1:310-311. 
  37. Chen NF, Sung CS, Wen ZH, Chen CH, Feng CW, Hung HC, Yang SN, Tsui KH, Chen WF. Therapeutic effect of platelet-rich plasma in rat spinal cord injuries. Front Neurosci 2018;12:252. 
  38. Kotsovilis S, Markou N, Pepelassi E, Nikolidakis D. The adjunctive use of platelet-rich plasma in the therapy of periodontal intraosseous defects: a systematic review. J Periodontal Res 2010;45:428-443. 
  39. Khan H, Mafi P, Mafi R, Khan W. The effects of ageing on differentiation and characterisation of human mesenchymal stem cells. Curr Stem Cell Res Ther 2018;13:378-383. 
  40. D'Esposito V, Passaretti F, Perruolo G, Ambrosio MR, Valentino R, Oriente F, Raciti GA, Nigro C, Miele C, Sammartino G, Beguinot F, Formisano P. Platelet-rich plasma increases growth and motility of adipose tissue-derived mesenchymal stem cells and controls adipocyte secretory function. J Cell Biochem 2015;116:2408-2418.