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Human Adipose-Derived Stem Cells Delay Muscular Atrophy after Peripheral Nerve Injury in Rats

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Abstract

Introduction

Given that denervation atrophy often occurs in muscle after peripheral nerve injury, the effects of injections of human adipose-derived stem cells (hADSCs) and platelet-rich plasma (PRP) into muscle after peripheral nerve injury were examined.

Methods

hADSCs were isolated from human subcutaneous fat tissue, and PRP was prepared from rat whole blood before injection into a rat sciatic nerve injury model. Muscle atrophy was evaluated by quantitating the gross musculature and muscle fiber area and walking footprint analysis.

Results

At 4 weeks post-surgery, there were significant differences in the sciatic functional index between experimental (injected with hADSCs, PRP, or combined hADSCs + PRP) and non-operated groups (p < 0.0001), but no significant differences were observed between the different treatment groups (p > 0.05). Post hoc Bonferroni tests also showed significant differences in the wet muscle weight ratios of hADSC, PRP, and combined groups compared to PBS group. The gastrocnemius muscle fiber area was larger in hADSC group and the combined group compared to PBS group at 4 weeks post-surgery.

Conclusion

The injection of hADSCs delays muscular atrophy after sciatic nerve injury in rats; thus, hADSCs are a promising alternative for regenerating atrophied muscle.

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Data Availability

All data generated or analyzed during this study are included in this published article and its supplementary information files.

References

  1. Yoshioka, N. (2020). Hypoglossal-facial side-to-end neurorrhaphy with concomitant masseteric-zygomatic nerve branch coaptation and muscle transfer for facial reanimation: technique and case report. Operative Neurosurgery (Hagerstown), 19(3), E230–E235.

    Article  Google Scholar 

  2. Tabata, S., Aizawa, M., Kinoshita, M., Ito, Y., Kawamura, Y., Takebe, M., Pan, W., & Sakuma, K. (2019). The influence of isoflavone for denervation-induced muscle atrophy. European Journal Nutrition, 58(1), 291–300.

    Article  CAS  Google Scholar 

  3. Choi, W. H., Jang, Y. J., Son, H. J., Ahn, J., Jung, C. H., & Ha, T. Y. (2018). Apigenin inhibits sciatic nerve denervation-induced muscle atrophy. Muscle & Nerve, 58(2), 314–318.

    Article  CAS  Google Scholar 

  4. Bueno, C. R. S., Pereira, M., Favaretto, I. A. J., Bortoluci, C. H. F., Santos, T., Dias, D. V., Dare, L. R., & Rosa, G. M. J. (2017). Electrical stimulation attenuates morphological alterations and prevents atrophy of the denervated cranial tibial muscle. Einstein (Sao Paulo), 15(1), 71–76.

    Article  Google Scholar 

  5. Su, Z., Hu, L., Cheng, J., Klein, J. D., Hassounah, F., Cai, H., Li, M., Wang, H. & Wang, X. H. (2016). Acupuncture plus low-frequency electrical stimulation (Acu-LFES) attenuates denervation-induced muscle atrophy. Journal of Applied Physiology, 120(4), 426–436.

    Article  CAS  Google Scholar 

  6. Sowa, Y., Imura, T., Numajiri, T., Nishino, K., & Fushiki, S. (2012). Adipose-derived stem cells produce factors enhancing peripheral nerve regeneration: influence of age and anatomic site of origin. Stem Cells and Development, 21(11), 1852–1862.

    Article  CAS  Google Scholar 

  7. Fairbairn, N. G., Meppelink, A. M., Ng-Glazier, J., Randolph, M. A., & Winograd, J. M. (2015). Augmenting peripheral nerve regeneration using stem cells: A review of current opinion. World Journal of Stem Cells, 7(1), 11–26.

    Article  Google Scholar 

  8. Gimble, J. M., Bunnell, B. A., Chiu, E. S., & Guilak, F. (2011). Concise review: adipose-derived stromal vascular fraction cells and stem cells: let’s not get lost in translation. Stem Cells, 29(5), 749–754.

    Article  Google Scholar 

  9. Minteer, D., Marra, K. G., & Rubin, J. P. (2013). Adipose-derived mesenchymal stem cells: biology and potential applications. Advances in Biochemical Engineering/Biotechnology, 129, 59–71.

    Article  CAS  Google Scholar 

  10. Abdul Halim, N. S. S., Yahaya, B. H., & Lian, J. (2022). Therapeutic potential of adipose-derived stem cells in the treatment of pulmonary diseases. Current Stem Cell Research & Therapy, 17(2), 103–112.

    Article  Google Scholar 

  11. Schilling, B. K., Schusterman, 2nd, M. A., Kim, D. Y., Repko, A. J., Klett, K. C., Christ, G. J., & Marra, K. G. (2019). Adipose-derived stem cells delay muscle atrophy after peripheral nerve injury in the rodent model. Muscle & Nerve, 59(5), 603–610.

    Article  CAS  Google Scholar 

  12. Edalatmanesh, M. A., Bahrami, A. R., Hosseini, E., Hosseini, M., & Khatamsaz, S. (2011). Neuroprotective effects of mesenchymal stem cell transplantation in animal model of cerebellar degeneration. Neurological Research, 33(9), 913–920.

    Article  Google Scholar 

  13. Haddad-Mashadrizeh, A., Bahrami, A. R., Matin, M. M., Edalatmanesh, M. A., Zomorodipour, A., Fallah, A., Gardaneh, M., Ahmadian Kia, N., & Sanjarmoosavi, N. (2013). Evidence for crossing the blood barrier of adult rat brain by human adipose-derived mesenchymal stromal cells during a 6-month period of post-transplantation. Cytotherapy, 15(8), 951–960.

    Article  CAS  Google Scholar 

  14. Mohamed-Ahmed, S., Fristad, I., Lie, S. A., Suliman, S., Mustafa, K., Vindenes, H., & Idris, S. B. (2018). Adipose-derived and bone marrow mesenchymal stem cells: a donor-matched comparison. Stem Cell Research & Therapy, 9(1), 168.

    Article  CAS  Google Scholar 

  15. Dominici, M., Le Blanc, K., Mueller, I., Slaper-Cortenbach, I., Marini, F., Krause, D., Deans, R., Keating, A., Prockop, D., & Horwitz, E. (2006). Minimal criteria for defining multipotent mesenchymal stromal cells. The International Society for Cellular Therapy position statement. Cytotherapy, 8(4), 315–317.

    Article  CAS  Google Scholar 

  16. Inserra, M. M., Bloch, D. A., & Terris, D. J. (1998). Functional indices for sciatic, peroneal, and posterior tibial nerve lesions in the mouse. Microsurgery, 18(2), 119–124.

    Article  CAS  Google Scholar 

  17. Wu, R., Wang, L., Chen, F., Huang, Y., Shi, J., Zhu, X., Ding, Y., & Zhang, X. (2016). Evaluation of artificial nerve conduit and autografts in peripheral nerve repair in the rat model of sciatic nerve injury. Neurological Research, 38(5), 461–466.

    Article  CAS  Google Scholar 

  18. Asami, Y., Aizawa, M., Kinoshita, M., Ishikawa, J. & Sakuma, K. (2018). Resveratrol attenuates denervation-induced muscle atrophy due to the blockade of atrogin-1 and p62 accumulation. International Journal of Medical Sciences, 15(6), 628–637.

    Article  CAS  Google Scholar 

  19. Lala-Tabbert, N., Lejmi-Mrad, R., Timusk, K., Fukano, M., Holbrook, J., St-Jean, M., LaCasse, E. C., & Korneluk, R. G. (2019). Targeted ablation of the cellular inhibitor of apoptosis 1 (cIAP1) attenuates denervation-induced skeletal muscle atrophy. Skeletal Muscle, 9(1), 13.

    Article  Google Scholar 

  20. Park, J. U., & Kwon, S. T. (2017). Potential of autologous adipose-derived stem cells to regenerate atrophied muscle in a rat model. Wound Repair and Regeneration, 25(6), 944–955.

    Article  Google Scholar 

  21. Chen, H. S., Su, Y. T., Chan, T. M., Su, Y. J., Syu, W. S., Harn, H. J., Lin, S. Z., & Chiu, S. C. (2015). Human adipose-derived stem cells accelerate the restoration of tensile strength of tendon and alleviate the progression of rotator cuff injury in a rat model. Cell Transplantation, 24(3), 509–520.

    Article  Google Scholar 

  22. Siregar, S., Sasongko Noegroho, B., Adriansjah, R., Mustafa, A. & Wijayanti, Z. (2021). Intratesticular human adipose-derived stem cell (hADSC) transplantation decreased oxidative stress in testicular torsion model of wistar rat. Research and Reports in Urology, 13, 1–8.

    Article  Google Scholar 

  23. Zhang, M., Park, G., Zhou, B. & Luo, D. (2018). Applications and efficacy of platelet-rich plasma in dermatology: A clinical review. Journal of Cosmetic Dermatology, 17(5), 660–665.

    Article  Google Scholar 

  24. Garbin, L. C., & Olver, C. S. (2020). Platelet-rich products and their application to osteoarthritis. Journal of Equine Veterinary Science, 86, 102820. https://doi.org/10.1016/j.jevs.2019.102820.

    Article  PubMed  Google Scholar 

  25. Chou, T. M., Chang, H. P. & Wang, J. C. (2020). Autologous platelet concentrates in maxillofacial regenerative therapy. The Kaohsiung Journal of Medical Sciences, 36(5), 305–310.

    Article  CAS  Google Scholar 

  26. Andia, I., & Abate, M. (2013). Platelet-rich plasma: underlying biology and clinical correlates. Regenerative Medicine, 8(5), 645–658.

    Article  CAS  Google Scholar 

  27. Mussano, F., Genova, T., Munaron, L., Petrillo, S., Erovigni, F., & Carossa, S. (2016). Cytokine, chemokine, and growth factor profile of platelet-rich plasma. Platelets, 27(5), 467–471.

    Article  CAS  Google Scholar 

  28. Giusti, I., D’Ascenzo, S., Macchiarelli, G., & Dolo, V. (2020). In vitro evidence supporting applications of platelet derivatives in regenerative medicine. Blood Transfusion, 18(2), 117–129.

    PubMed  PubMed Central  Google Scholar 

  29. Emer, J. (2019). Platelet-rich plasma (PRP): current applications in dermatology. Skin Therapy Letter, 24(5), 1–6.

    PubMed  Google Scholar 

  30. Wu, C. C., Chen, W. H., Zao, B., Lai, P. L., Lin, T. C., Lo, H. Y., Shieh, Y. H., Wu, C. H., & Deng, W. P. (2011). Regenerative potentials of platelet-rich plasma enhanced by collagen in retrieving pro-inflammatory cytokine-inhibited chondrogenesis. Biomaterials, 32(25), 5847–5854.

    Article  CAS  Google Scholar 

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Funding

This study was supported by the Discipline Construction Project of Peking Union Medical College (201920200401) and CAMS Innovation Fund for Medical Sciences (2021-I2M-1-068).

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Authors and Affiliations

Authors

Contributions

Q.S. performed the experiments, analyzed the data, and wrote the manuscript. M.N., W.W., C.S., W.Q., and L.Y. designed the research, analyzed the data, and contributed to the writing of the manuscript. Y.Z. supervised the study.

Corresponding author

Correspondence to Zhe Yang.

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Conflict of Interest

The authors declare no competing interests.

Ethical approval and consent to participate

All experiments conducted in this study were reviewed and approved by the Local Animal Ethics Committee (No. 202003003). Using human adipose tissue was approved by the Ethics Committee of Plastic Surgery Hospital (No. 2150019022). All methods in this study were conducted following relevant guidelines and regulations. All methods are reported in this study following ARRIVE guidelines for the reporting of animal experiments.

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Qu, S., Ma, N., Wang, W. et al. Human Adipose-Derived Stem Cells Delay Muscular Atrophy after Peripheral Nerve Injury in Rats. Cell Biochem Biophys 80, 555–562 (2022). https://doi.org/10.1007/s12013-022-01082-4

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  • DOI: https://doi.org/10.1007/s12013-022-01082-4

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