Skip to main content
SpringerLink
Log in

Impact of preconditioned diabetic stem cells and photobiomodulation on quantity and degranulation of mast cells in a delayed healing wound simulation in type one diabetic rats

  • Original Article
  • Published:
Lasers in Medical Science Aims and scope Submit manuscript

Abstract

Herein, we report the influence of administering different protocols of preconditioned diabetic adipose-derived mesenchymal stem cells (ADSs) with photobiomodulation in vitro, and photobiomodulation in vivo on the number of mast cells (MCs), their degranulation, and wound strength in the maturation step of a Methicillin-resistant Staphylococcus aureus (MRSA)-infectious wound model in rats with type one diabetes. An MRSA-infectious wound model was generated on diabetic animals, and they were arbitrarily assigned into five groups (G). G1 were control rats. In G2, diabetic ADS were engrafted into the wounds. In G3, diabetic ADS were engrafted into the wound, and the wound was exposed to photobiomodulation (890 nm, 890 ± 10 nm, 80 Hz, 0.2 J/cm2) in vivo. In G4, preconditioned diabetic ADS with photobiomodulation (630 and 810 nm; each 3 times with 1.2 J/cm2) in vitro were engrafted into the wound. In G5, preconditioned diabetic ADS with photobiomodulation were engrafted into the wound, and the wound was exposed to photobiomodulation in vivo. The results showed that, the maximum force in all treatment groups was remarkably greater compared to the control group (all, p = 0.000). Maximum force in G4 and G5 were superior than that other treated groups (both p = 0.000). Moreover, G3, G4, and G5 showed remarkable decreases in completely released MC granules and total numbers of MC compared to G1 and G2 (all, p = 0.000). We concluded that diabetic rats in group 5 showed significantly better results in terms of accelerated wound healing and MC count of an ischemic infected delayed healing wound model.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  1. Jneid J, Lavigne J, La Scola B, Cassir N (2017) The diabetic foot microbiota: a review. Hum Microbiome J 5:1–6

    Google Scholar 

  2. Liu C, Ponsero AJ, Armstrong DG, Lipsky BA, Hurwitz BL (2020) The dynamic wound microbiome. BMC Med 18:1–12

    Google Scholar 

  3. Baltzis D, Eleftheriadou I, Veves A (2014) Pathogenesis and treatment of impaired wound healing in diabetes mellitus: new insights. Adv Ther 31:817–836

    CAS  PubMed  Google Scholar 

  4. Komi DEA, Khomtchouk K, Santa Maria PL (2020) A review of the contribution of mast cells in wound healing: involved molecular and cellular mechanisms. Clin Rev Allergy Immunol 58(3):298–312

    CAS  PubMed  Google Scholar 

  5. Johnzon C-F, Rönnberg E, Pejler G (2016) The role of mast cells in bacterial infection. Am J Pathol 186:4–14

    CAS  PubMed  Google Scholar 

  6. Tellechea A, Leal EC, Kafanas A, Auster ME, Kuchibhotla S, Ostrovsky Y, Tecilazich F, Baltzis D, Zheng Y, Carvalho E, Zabolotny JM, Weng Z, Petra A, Patel A, Panagiotidou S, Pradhan-Nabzdyk L, Theoharides TC, Veves A (2016) Mast cells regulate wound healing in diabetes. Diabetes 65:2006–2019

    CAS  PubMed  PubMed Central  Google Scholar 

  7. Dong J, Chen L, Zhang Y, Jayaswal N, Mezghani I, Zhang W, Veves A (2020) Mast cells in diabetes and diabetic wound healing. Adv Ther 37:4519–4537

    PubMed  PubMed Central  Google Scholar 

  8. Kosaric N, Kiwanuka H, Gurtner GC (2019) Stem cell therapies for wound healing. Expert Opin Biol Ther 19:575–585

    CAS  PubMed  Google Scholar 

  9. Patel S, Srivastava S, Singh MR, Singh D (2019) Mechanistic insight into diabetic wounds: Pathogenesis, molecular targets and treatment strategies to pace wound healing, Biomedicine & pharmacotherapy. Biomed Pharmacother 112:108615

    CAS  PubMed  Google Scholar 

  10. Ahmadi H, Amini A, FadaeiFathabady F, Mostafavinia A, Zare F, Ebrahimpour-Malekshah R, Ghalibaf MN, Abrisham M, Rezaei F, Albright R, Ghoreishi SK, Chien S, Bayat M (2020) Transplantation of photobiomodulation-preconditioned diabetic stem cells accelerates ischemic wound healing in diabetic rats. Stem cell Res Ther 11(1):494

    CAS  PubMed  PubMed Central  Google Scholar 

  11. Ebrahimpour-Malekshah R, Amini A, Zare F, Mostafavinia A, Davoody S, Deravi N, Rahmanian M, Hashemi SM, Habibi M, Ghoreishi SK, Chien S, Shafikhani S, Ahmadi H, Bayat S, Bayat M (2020) Combined therapy of photobiomodulation and adipose-derived stem cells synergistically improve healing in an ischemic, infected and delayed healing wound model in rats with type 1 diabetes mellitus. BMJ Open Diabetes Res Care 8(1):e001033. https://doi.org/10.1136/bmjdrc-2019-001033

  12. Moradi A, Zare F, Mostafavinia A, Safaju S, Shahbazi A, Habibi M, Abdollahifar MA, Hashemi SM, Amini A, Ghoreishi SK, Chien S, Hamblin MR, Kouhkheil R, Bayat M (2020) Photobiomodulation plus adipose-derived stem cells improve healing of ischemic infected wounds in type 2 diabetic rats. Sci Rep 10:1206

    CAS  PubMed  PubMed Central  Google Scholar 

  13. Şener LT, Albeniz I (2015) Challenge of mesenchymal stem cells against diabetic foot ulcer. Curr Stem Cell Res Ther 10:530–534

    PubMed  Google Scholar 

  14. Tsuji W, Rubin JP, Marra KG (2014) Adipose-derived stem cells: implications in tissue regeneration. World J Stem Cells 6:312

    PubMed  PubMed Central  Google Scholar 

  15. Álvaro-Afonso FJ, Sanz-Corbalán I, Lázaro-Martínez JL, Kakagia D, Papanas N (2020) Adipose-derived mesenchymal stem cells in the treatment of diabetic foot ulcers: a review of preclinical and clinical studies. Angiology 71:853–863

    PubMed  Google Scholar 

  16. Chehelcheraghi F, Bayat M, Chien S (2020) Effect of mesenchymal stem cells and chicken embryo extract on flap viability and mast cells in rat skin flaps. J Invest Surgery 33(2):123–133

    Google Scholar 

  17. Chehelcheraghi F, Chien S, Bayat M (2019) Mesenchymal stem cells improve survival in ischemic diabetic random skin flap via increased angiogenesis and VEGF expression. J Cell Biochem 120:17491–17499

    Article  CAS  Google Scholar 

  18. Yadav A, Gupta A (2017) Noninvasive red and near-infrared wavelength-induced photobiomodulation: promoting impaired cutaneous wound healing. Photodermatol Photoimmunol Photomed 33:4–13

    PubMed  Google Scholar 

  19. Pinto H, Goñi Oliver P, Sánchez-VizcaínoMengual E (2021) The effect of photobiomodulation on human mesenchymal cells: a literature review. Aesthetic Plast Surg 45(4):1826–1842

    PubMed  Google Scholar 

  20. Fathabadie FF, Bayat M, Amini A, Bayat M, Rezaie F (2013) Effects of pulsed infra-red low level-laser irradiation on mast cells number and degranulation in open skin wound healing of healthy and streptozotocin-induced diabetic rats. J Cosmet Laser Ther : Off Pub Euro Soc Laser Dermatol 15:294–304

    Google Scholar 

  21. Bagheri M, Amini A, Abdollahifar MA, Ghoreishi SK, Piryaei A, Pouriran R, Chien S, Dadras S, Rezaei F, Bayat M (2018) Effects of photobiomodulation on degranulation and number of mast cells and wound strength in skin wound healing of streptozotocin-induced diabetic rats. Photomed Laser Surg 36:415–423

    CAS  PubMed  Google Scholar 

  22. Kouhkheil R, Fridoni M, Abdollhifar MA, Amini A, Bayat S, Ghoreishi SK, Chien S, Kazemi M, Bayat M (2019) Impact of photobiomodulation and condition medium on mast cell counts, degranulation, and wound strength in infected skin wound healing of diabetic rats. Photobiomodul Photomed Laser Surg 37:706–714

    PubMed  Google Scholar 

  23. Soleimani H, Amini A, Abdollahifar MA, Norouzian M, Kouhkheil R, Mostafavinia A, Ghoreishi SK, Bayat S, Chien S, Bayat M (2021) Combined effects of photobiomodulation and curcumin on mast cells and wound strength in wound healing of streptozotocin-induced diabetes in rats. Lasers Med Sci 36:375–386

    PubMed  Google Scholar 

  24. Amini A, Pouriran R, Abdollahifar M-A, Abbaszadeh HA, Ghoreishi SK, Chien S, Bayat M (2018) Stereological and molecular studies on the combined effects of photobiomodulation and human bone marrow mesenchymal stem cell conditioned medium on wound healing in diabetic rats. J Photochem Photobiol, B 182:42–51

    CAS  Google Scholar 

  25. Babaei S, Bayat M, Nouruzian M, Bayat M (2013) Pentoxifylline improves cutaneous wound healing in streptozotocin-induced diabetic rats. Eur J Pharmacol 700:165–172

    CAS  PubMed  Google Scholar 

  26. Falanga V (2005) Wound healing and its impairment in the diabetic foot. The Lancet 366:1736–1743

    Google Scholar 

  27. Xiao J, Li J, Cai L, Chakrabarti S, Li X (2014) Cytokines and diabetes research. J Diabetes Res 2014:920613. https://doi.org/10.1155/2014/920613. Epub 2014 Jan 16

  28. Rapala K, Laato M, Niinikoski J, Kujari H, Söder O, Mauviel A, Pujol J-P (1991) Tumor necrosis factor alpha inhibits wound healing in the rat. Eur Surg Res 23:261–268

    CAS  PubMed  Google Scholar 

  29. Tellechea A, Bai S, Dangwal S, Theocharidis G, Nagai M, Koerner S, Cheong JE, Bhasin S, Shih TY, Zheng Y, Zhao W, Zhang C, Li X, Kounas K, Panagiotidou S, Theoharides T, Mooney D, Bhasin M, Sun L, Veves A (2020) Topical application of a mast cell stabilizer improves impaired diabetic wound healing. J Invest Dermatol 140(4):901-911 e911

    CAS  PubMed  Google Scholar 

  30. Ding X, Rath P, Angelo R, Stringfellow T, Flanders E, Dinh S, Gomez-Orellana I, Robinson JR (2004) Oral absorption enhancement of cromolyn sodium through noncovalent complexation. Pharm Res 21:2196–2206

    CAS  PubMed  Google Scholar 

  31. Cairns H, Fitzmaurice C, Hunter D, Johnson P, King J, Lee T, Lord G, Minshull R, Cox J (1972) Synthesis and structure-activity relations of disodium cromoglycate and some related compounds. J Med Chem 15:583–589

    CAS  PubMed  Google Scholar 

  32. Edwards AM, Bibawy D, Matthews S, Tongue N, Arshad SH, LødrupCarlsen K, Øymar K, Pollock I, Clifford R, Thomas A (2015) Long-term use of a 4% sodium cromoglicate cutaneous emulsion in the treatment of moderate to severe atopic dermatitis in children. J Dermatolog Treat 26(6):541–547

    PubMed  Google Scholar 

  33. Nazari M, Ni NC, Lüdke A, Li SH, Guo J, Weisel RD, Li RK (2016) Mast cells promote proliferation and migration and inhibit differentiation of mesenchymal stem cells through PDGF. J Mol Cell Cardiol 94:32–42

    CAS  PubMed  Google Scholar 

  34. Yun IS, Jeon YR, Lee WJ, Lee JW, Rah DK, Tark KC, Lew DH et al (2012) Effect of human adipose derived stem cells on scar formation and remodeling in a pig model: a pilot study. Dermatolo Surg 38(10):1678–1688

    CAS  Google Scholar 

  35. Houreld N (2019) Healing effects of photobiomodulation on diabetic wounds. Appl Sci 9:5114

    CAS  Google Scholar 

  36. Gruber BL, Marchese MJ, Kew R (1995) Angiogenic factors stimulate mast-cell migration. Blood 86(7):2488–2493

    CAS  PubMed  Google Scholar 

  37. Hiromatsu Y, Toda S (2003) Mast cells and angiogenesis. Microsc Res Tech 60:64–69

    PubMed  Google Scholar 

  38. Theoharides TC, Alysandratos KD, Angelidou A, Delivanis DA, Sismanopoulos N, Zhang B, Asadi S, Vasiadi M, Weng Z, Miniati A (2012) Mast cells and inflammation. Biochim Biophys Acta 1822(1):21–33

    CAS  PubMed  Google Scholar 

  39. Bayat M, Chien S, Chehelcheraghi F (2021) Co-localization of Flt1 and tryptase of mast cells in skin wound of rats with type I diabetes: Initial studies. Acta Histochem 123(2):151680

    CAS  PubMed  Google Scholar 

  40. do Valle IB, Prazeres PHDM, Mesquita RA, Silva TA, de Castro Oliveira HM, Castro PR, Freitas IDP, Oliveira SR, Gomes NA, de Oliveira RF (2020) Photobiomodulation drives pericyte mobilization towards skin regeneration. Sci Rep 10(1):15

    Google Scholar 

  41. Pereira MCM, de Pinho CB, Medrado ARP, de Araújo Andrade Z, de Almeida Reis SR (2010) Influence of 670 nm low-level laser therapy on mast cells and vascular response of cutaneous injuries. J Photochem Photobiol B 98(3):188–192

    CAS  PubMed  Google Scholar 

  42. Silveira L, Prates R, Novelli M, Marigo H, Garrocho A, Amorim J, Sousa G, Pinotti M, Ribeiro M (2008) Investigation of mast cells in human gingiva following low-intensity laser irradiation. Photomed Laser Surg 26:315–321

    CAS  PubMed  Google Scholar 

  43. Sawasaki I, Geraldo-Martins VR, Ribeiro MS, Marques MM (2009) Effect of low-intensity laser therapy on mast cell degranulation in human oral mucosa. Lasers Med Sci 24:113–116

    PubMed  Google Scholar 

  44. Khoshvaghti A, Zibamanzarmofrad M, Bayat M (2011) Effect of low-level treatment with an 80-Hz pulsed infrared diode laser on mast-cell numbers and degranulation in a rat model of third-degree burn. Photomed Laser Surg 29:597–604

    PubMed  Google Scholar 

Download references

Funding

The present study was financially supported by the Research Department of the School of Medicine at Shahid Beheshti University of Medical Sciences, Tehran, Iran (Grant no. 20266). This article was extracted from the thesis written by Mr. Houssein Ahmadi (Registration No.: IR. SBMU. MSP.REC.1399.105).

Author information

Author notes

  1. Mohammad Bayat

    Present address: Price Institute of Surgical Research, University of Louisville, and Noveratech LLC, Louisville, KY, USA

Authors and Affiliations

  1. Department of Biology and Anatomical Sciences, Shahid Beheshti University of Medical Sciences, Tehran, Iran

    Houssein Ahmadi, Mohammad Bayat, Abdollah Amini & Roohollah Ebrahimpour-Malekshah

  2. Department of Anatomy, Faculty of Medicine, Tehran Medical Sciences, Islamic Azad University, Tehran, Iran

    Atarodalsadat Mostafavinia

  3. Department of Anatomy, School of Medicine, Guilan University of Medical Sciences, Rasht, Iran

    Rouhallah Gazor

  4. Paramedical School, Tehran University of Medical Sciences, Tehran, Iran

    Robabeh Asadi

  5. Infectious Diseases Department, Loghman Hakim Hospital, Kamali St., South Karegar St., Tehran, Iran

    Latif Gachkar

  6. College of Pharmacy, University of Kentucky, 789 South Limestone, Lexington, KY, 40536, USA

    Fatemehalsadat Rezaei

  7. Department of Medicine, Division of Hematology/Oncology/Cell Therapy, Department of Microbial Pathogens and Immunity, Cancer Center, Rush University Medical Center, Chicago, IL, USA

    Sasha H. Shafikhani

  8. Department of Statistics, Qom University, Qom, Iran

    Seyed Kamran Ghoreishi

  9. Price Institute of Surgical Research, University of Louisville, and Noveratech LLC, Louisville, KY, USA

    Sufan Chien

Authors
  1. Houssein Ahmadi
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Mohammad Bayat
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Abdollah Amini
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Atarodalsadat Mostafavinia
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Roohollah Ebrahimpour-Malekshah
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Rouhallah Gazor
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Robabeh Asadi
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Latif Gachkar
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Fatemehalsadat Rezaei
    View author publications

    You can also search for this author in PubMed Google Scholar

  10. Sasha H. Shafikhani
    View author publications

    You can also search for this author in PubMed Google Scholar

  11. Seyed Kamran Ghoreishi
    View author publications

    You can also search for this author in PubMed Google Scholar

  12. Sufan Chien
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

Mohammad Bayat and Abdollah Amini researched the data and wrote the manuscript. Houssein Ahmadi, Robabeh Asadi, and Roohollah Ebrahimpour-Malekshah performed the methods; Rouhallah Gazor, Sasha H. Shafikhani, Fatemehalsadat Rezaei, Latif Gachkar, and Sufan Chien presented their comments; Atarodalsadat Mostafavinia and Seyed Kamran Ghoreishi performed statistical tests.

Corresponding authors

Correspondence to Mohammad Bayat or Abdollah Amini.

Ethics declarations

Competing interests

The authors declare no competing interests.

Additional information

Publisher's note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary Information

Below is the link to the electronic supplementary material.

Supplementary file1 (DOCX 208 KB)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Ahmadi, H., Bayat, M., Amini, A. et al. Impact of preconditioned diabetic stem cells and photobiomodulation on quantity and degranulation of mast cells in a delayed healing wound simulation in type one diabetic rats. Lasers Med Sci 37, 1593–1604 (2022). https://doi.org/10.1007/s10103-021-03408-9

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10103-021-03408-9

Keywords

Search

Navigation