New trends in the regenerative therapy of vitiligo. Literature review

Abstract

Vitiligo is the most common acquired skin depigmentation disorder characterized by progressive loss of pigmentation caused by the destruction of functional melanocytes in the epidermis. The pathogenesis consists in the interaction of genetic components, metabolic factors associated with cellular oxidative stress, adhesion of melanocytes to the epithelium and autoimmunity, which culminate in aggression against melanocytes. To date, the treatment of vitiligo, according to Russian and European clinical guidelines, consists in the appointment of various drug and non-drug methods: the use of topical and systemic glucocorticosteroids, calcineurin inhibitors, azathioprine, phototherapy, both in the form of monotherapy and their combination.

In recent years, in connection with the development of cellular technologies, alternative methods of therapy based on the transplantation of autologous cultured and non-cultured melanocytes have become widespread in the treatment of vitiligo. The most promising options for vitiligo cell therapy are methods based not only on the transplantation of ready-made cellular structures, but also on the replacement of damaged cells with a transplant of pluropotent progenitor stem cells or their immature committed structures.

This article is of an overview nature. The aim of the review is to update information on promising new treatments for vitiligo. A literature review was conducted using the PubMed, Cochrane Library, CyberLeninka and Internet databases to study clinical and preclinical data on the possibility of using innovative methods of regenerative medicine in patients with vitiligo.

This review is addressed to medical researchers interested in the treatment of vitiligo.

Keywords

vitiligo / treatment of vitiligo / melanocyte / regenerative therapy

References

[1] Gauthier Y, Andre CM, Taïeb A. A critical appraisal of vitiligo etiologic theories. Ismelanocyteloss a melanocytorrhagy? Pigment Cell Res. 2003;16(4):322–332. doi: 10.1034/j.1600-0749.2003.00070.x

[2] Gauthier Y., Andre C.M., Taïeb A. A critical appraisal of vitiligo etiologic theories. Ismelanocyteloss a melanocytorrhagy? // Pigment Cell Res. 2003. Vol. 16, N 4. Р. 322–332. doi: 10.1034/j.1600-0749.2003.00070.x

[3] Bergqvist C, Ezzedine K. Vitiligo: a review. Dermatology. 2020;236(6):571–592. doi: 10.1159/000506103

[4] Bergqvist C., Ezzedine K. Vitiligo: A review // Dermatology. 2020. Vol. 236, N 6. Р. 571–592. doi: 10.1159/000506103

[5] Castro CC, Miot HA. Prevalence of vitiligo in Brazil: A population survey. Pigment Cell Melanoma Res. 2018;31(3):448–450. doi: 10.1111/pcmr.12681

[6] Castro C.C., Miot H.A. Prevalence of vitiligo in Brazil: A population survey // Pigment Cell Melanoma Res. 2018. Vol. 31, N 3. Р. 448–450. doi: 10.1111/pcmr.12681

[7] Castro CC, Nascimento LL, Olandoski M, Mira MT. A pattern of association between clinical form of vitiligo and disease-related variables in a Brazilian population. J Dermatol Sci. 2012;65(1):63–67. doi: 10.1016/j.jdermsci.2011.09.011

[8] Castro C.C., Nascimento L.L., Olandoski M., Mira M.T. A pattern of association between clinical form of vitiligo and disease-related variables in a Brazilian population // J Dermatol Sci. 2012. Vol. 65, N 1. Р. 63–67. doi: 10.1016/j.jdermsci.2011.09.011

[9] Krüger C, Schallreuter KU. A review of the worldwide prevalence of vitiligo in children/adolescents and adults. Int J Dermatol. 2012;51(10):1206–1212. doi: 10.1111/j.1365-4632.2011.05377.x

[10] Krüger C., Schallreuter K.U. A review of the worldwide prevalence of vitiligo in children/adolescents and adults // Int J Dermatol. 2012. Vol. 51, N 10. Р. 1206–1212. doi: 10.1111/j.1365-4632.2011.05377.x

[11] Ezzedine K, Lim HW, Suzuki T, et al.; Vitiligo Global Issue Consensus Conference Panelists. Revised classification/nomenclature of vitiligo and related issues: The Vitiligo Global Issues Consensus Conference. Pigment Cell Melanoma Res. 2012;25(3):E1–13. doi: 10.1111/j.1755-148X.2012.00997.x

[12] Ezzedine K., Lim H.W., Suzuki T., et al.; Vitiligo Global Issue Consensus Conference Panelists. Revised classification/nomenclature of vitiligo and related issues: The Vitiligo Global Issues Consensus Conference // Pigment Cell Melanoma Res. 2012. Vol. 25, N 3. Р. E1–13. doi: 10.1111/j.1755-148X.2012.00997.x

[13] Boniface K, Seneschal J, Picardo M, Taïeb A. Vitiligo: Focus on clinical aspects, immunopathogenesis, and therapy. Clin Rev Allergy Immunol. 2018;54(1):52–67. doi: 10.1007/s12016-017-8622-7

[14] Boniface K., Seneschal J., Picardo M., Taïeb A. Vitiligo: Focus on clinical aspects, immunopathogenesis, and therapy // Clin Rev Allergy Immunol. 2018. Vol. 54, N 1. Р. 52–67. doi: 10.1007/s12016-017-8622-7

[15] Speeckaert R, van Geel N. Vitiligo: An update on pathophysiology and treatment options. Am J Clin Dermatol. 2017;18(6):733–744. doi: 10.1007/s40257-017-0298-5

[16] Speeckaert R., van Geel N. Vitiligo: An update on pathophysiology and treatment options // Am J Clin Dermatol. 2017. Vol. 18, N 6. Р. 733–744. doi: 10.1007/s40257-017-0298-5

[17] Prignano F, d’Erme AM, Bonciolini V, Lotti T. Mucosal psoriasis: A new insight toward a systemic inflammatory disease. Int J Dermatol. 2011;50(12):1579–1581. doi: 10.1111/j.1365-4632.2010.04864.x

[18] Prignano F., d’Erme A.M., Bonciolini V., Lotti T. Mucosal psoriasis: A new insight toward a systemic inflammatory disease // Int J Dermatol. 2011. Vol. 50, N 12. Р. 1579–1581. doi: 10.1111/j.1365-4632.2010.04864.x

[19] Davletshina AY, Lomonosov KM. Dermatoscopic patterns of vitiligo. Russ J Skin Venereal Dis. 2020;23(6):381–387. (In Russ). doi: 10.17816/dv60488

[20] Давлетшина А.Ю., Ломоносов К.М. Дерматоскопические паттерны витилиго // Российский журнал кожных и венерических болезней. 2020. Т. 23, № 6. C. 381–387. doi: 10.17816/dv60488

[21] Ongenae K, van Geel N, De Schepper S, Naeyaert JM. Effect of vitiligo on self-reported health-related quality of life. Br J Dermatol. 2005;152(6):1165–1172. doi: 10.1111/j.1365-2133.2005.06456.x

[22] Ongenae K., van Geel N., De Schepper S., Naeyaert J.M. Effect of vitiligo on self-reported health-related quality of life // Br J Dermatol. 2005. Vol. 152, N 6. Р. 1165–1172. doi: 10.1111/j.1365-2133.2005.06456.x

[23] Daniel BS, Wittal R. Vitiligo treatment update. Australas J Dermatol. 2015;56(2):85–92. doi: 10.1111/ajd.12256

[24] Daniel B.S., Wittal R. Vitiligo treatment update // Australas J Dermatol. 2015. Vol. 56, N 2. Р. 85–92. doi: 10.1111/ajd.12256

[25] Luger T, Paul C. Potential new indications of topical calcineurin inhibitors. Dermatology. 2007;215(Suppl 1):45–54. doi: 10.1159/000102119

[26] Luger T., Paul C. Potential new indications of topical calcineurin inhibitors // Dermatology. 2007. Vol. 215, Suppl. 1. Р. 45–54. doi: 10.1159/000102119

[27] Kuga K, Nishifuji K, Iwasaki T. Cyclosporine A inhibits transcription of cytokine genes and decreases the frequencies of IL-2 producing cells in feline mononuclear cells. J Vet Med Sci. 2008;70(10):1011–1016. doi: 10.1292/jvms.70.1011

[28] Kuga K., Nishifuji K., Iwasaki T. Cyclosporine A inhibits transcription of cytokine genes and decreases the frequencies of IL-2 producing cells in feline mononuclear cells // J Vet Med Sci. 2008. Vol. 70, N 10. Р. 1011–1016. doi: 10.1292/jvms.70.1011

[29] Vovdenko KA, Khafizova AA, Lomonosov KM. Effectiveness of combination of UVB-311 nm and azathioprine in the treatment of non-segmental vitiligo. Russ J Skin Venereal Dis. 2022;25(4):269–278. (In Russ). doi: 10.17816/dv111578

[30] Вовденко К.А., Хафизова А.А., Ломоносов К.М. Эффективность комбинации УФБ-311 нм и азатиоприна в терапии несегментарного витилиго // Российский журнал кожных и венерических болезней. 2022. Т. 25, № 4. C. 269–278. doi: 10.17816/dv111578

[31] Krotkova EA. Treatment of vitiligo: A look into the future (literature review). Russ J Skin Venereal Dis. 2021;24(6):537–542. (In Russ). doi: 10.17816/dv101158

[32] Кроткова Е.А. Лечение витилиго: взгляд в будущее (обзор литературы) // Российский журнал кожных и венерических болезней. 2021. Т. 24, № 6. C. 537–542. doi: 10.17816/dv101158

[33] Lomonosov KM, Gereikhanova LG. Algorithm of vitiligo treatment. Russ J Skin Venereal Dis. 2016;19(3):167–169. (In Russ). doi: 10.18821/1560-9588-2016-19-3-167-169

[34] Ломоносов К.М., Герейханова Л.Г. Алгоритм лечения витилиго // Российский журнал кожных и венерических болезней. 2016. Т. 19, № 3. C. 167–169. doi: 10.18821/1560-9588-2016-19-3-167-169

[35] Qi F, Liu F, Gao L. Janus kinase inhibitors in the treatment of vitiligo: A review. Front Immunol. 2021;(12):790125. doi: 10.3389/fimmu.2021.790125

[36] Qi F., Liu F., Gao L. Janus kinase inhibitors in the treatment of vitiligo: A review // Front Immunol. 2021. N 12. Р. 790125. doi: 10.3389/fimmu.2021.790125

[37] Ramos MG, Ramos DG, Ramos CG. Evaluation of treatment response to autologous transplantation of noncultured melanocyte/keratinocyte cell suspension in patients with stable vitiligo. An Bras Dermatol. 2017;92(3):312–318. doi: 10.1590/abd1806-4841.20175700

[38] Ramos M.G., Ramos D.G., Ramos C.G. Evaluation of treatment response to autologous transplantation of noncultured melanocyte/keratinocyte cell suspension in patients with stable vitiligo // An Bras Dermatol. 2017. Vol. 92, N 3. Р. 312–318. doi: 10.1590/abd1806-4841.20175700

[39] Liebl H, Kloth LC. Skin cell proliferation stimulated by microneedles. J Am Coll Clin Wound Spec. 2012;4(1):2–6. doi: 10.1016/j.jccw.2012.11.001

[40] Liebl H., Kloth L.C. Skin cell proliferation stimulated by microneedles // J Am Coll Clin Wound Spec. 2012. Vol. 4, N 1. Р. 2–6. doi: 10.1016/j.jccw.2012.11.001

[41] Lewin ML, Peck SM. Pigment studies in skin grafts on experimental animals. J Invest Dermat. 1941;(4):483–503.

[42] Lewin M.L., Peck S.M. Pigment studies in skin grafts on experimental animals // J Invest Dermat 1941. N 4. Р. 483–503.

[43] Spencer GA, Tolmach JA. Exchange grafts in vitiligo. J Invest Dermatol. 1952;19(1):1–5. doi: 10.1038/jid.1952.59

[44] Spencer G.A., Tolmach J.A. Exchange grafts in vitiligo // J Invest Dermatol. 1952. Vol. 19, N 1. Р. 1–5. doi: 10.1038/jid.1952.59

[45] Avgirinou G, Antoniu K, Andreas SL. European Guidelines for the treatment of dermatological diseases. Ed. by A.D. Katsambas, T.M. Lotti. Moscow: MEDpress-inform; 2014. 724 p. (In Russ).

[46] Авгериноу Г., Антониу К., Андреасси Л. Европейское руководство по лечению дерматологических болезней / под ред. А.Д. Кацамбас, Т.М. Лотти. Москва: МЕДпресс-информ, 2014. 724 с.

[47] Kubanova AA, Volnukhin VA, Proshutinskaya DV, et al. Possibilities of regenerative medicine in the treatment of patients with vitiligo. Bulletin Dermatol Venereol. 2014;90(3):43–52. (In Russ). doi: 10.25208/0042-4609-2014-90-3-43-52

[48] Кубанова А.А., Волнухин В.А., Прошутинская Д.В., и др. Возможности регенеративной медицины в лечении больных витилиго // Вестник дерматологии и венерологии. 2014. Т. 90, № 3. C. 43–52. doi: 10.25208/0042-4609-2014-90-3-43-52

[49] Fronchek A, Kasprovich-Furmanschik M, Plastik V, Ovcharchik-Sanek A. Surgical treatment of vitiligo. Field Environmental Protection Public Health. 2022;19(8):4812. (In Russ). doi: 10.3390/ijerph19084812

[50] Фрончек А., Каспрович-Фурманчик М., Пласек В., Овчарчик-Сацонек А. Хирургическое лечение витилиго // В области охраны окружающей среды и общественного здравоохранения. 2022. Т. 19, № 8. C. 4812. doi: 10.3390/ijerph19084812

[51] Yannas IV. Similarities and differences between induced organ regeneration in adults and early foetal regeneration. J R Soc Interface. 2005;2(5):403–417. doi: 10.1098/rsif.2005.0062

[52] Yannas I.V. Similarities and differences between induced organ regeneration in adults and early foetal regeneration // J R Soc Interface. 2005. Vol. 2, N 5. Р. 403–417. doi: 10.1098/rsif.2005.0062

[53] Liau LL, Ruszymah BH, Ng MH, Law JX. Characteristics and clinical applications of Wharton’s jelly-derived mesenchymal stromal cells. Curr Res Transl Med. 2020;68(1):5–16. doi: 10.1016/j.retram.2019.09.001

[54] Liau L.L., Ruszymah B.H., Ng M.H., Law J.X. Characteristics and clinical applications of Wharton’s jelly-derived mesenchymal stromal cells // Curr Res Transl Med. 2020. Vol. 68, N 1. Р. 5–16. doi: 10.1016/j.retram.2019.09.001

[55] Mizukami A, Swiech K. Mesenchymal stromal cells: From discovery to manufacturing and commercialization. Stem Cells Int. 2018;2018:4083921. doi: 10.1155/2018/4083921

[56] Mizukami A., Swiech K. Mesenchymal stromal cells: From discovery to manufacturing and commercialization // Stem Cells Int. 2018. Vol. 2018. Р. 4083921. doi: 10.1155/2018/4083921

[57] Zhang M, Xia T, Lin F, et al. Vitiligo: An immune disease and its emerging mesenchymal stem cell therapy paradigm. Transpl Immunol. 2023;(76):101766. doi: 10.1016/j.trim.2022.101766

[58] Zhang M., Xia T., Lin F., et al. Vitiligo: An immune disease and its emerging mesenchymal stem cell therapy paradigm // Transpl Immunol. 2023. N 76. Р. 101766. doi: 10.1016/j.trim.2022.101766

[59] Hyvärinen K, Holopainen M, Skirdenko V, et al. Mesenchymal stromal cells and their extracellular vesicles enhance the anti-inflammatory phenotype of regulatory macrophages by downregulating the production of interleukin (IL)-23 and IL-22. Front Immunol. 2018;(9):771. doi: 10.3389/fimmu.2018.00771

[60] Hyvärinen K., Holopainen M., Skirdenko V., et al. Mesenchymal stromal cells and their extracellular vesicles enhance the anti-inflammatory phenotype of regulatory macrophages by downregulating the production of interleukin (IL)-23 and IL-22 // Front Immunol. 2018. N 9. Р. 771. doi: 10.3389/fimmu.2018.00771

[61] Jiang W, Xu J. Immune modulation by mesenchymal stem cells. Cell Prolif. 2020;53(1):e12712. doi: 10.1111/cpr.12712

[62] Jiang W., Xu J. Immune modulation by mesenchymal stem cells // Cell Prolif. 2020. Vol. 53, N 1. Р. e12712. doi: 10.1111/cpr.12712

[63] Weiss AR, Dahlke MH. Immunomodulation by Mesenchymal Stem Cells (MSCs): Mechanisms of action of living, apoptotic, and dead MSCs. Front Immunol. 2019;(10):1191. doi: 10.3389/fimmu.2019.01191

[64] Weiss A.R., Dahlke M.H. Immunomodulation by Mesenchymal Stem Cells (MSCs): Mechanisms of action of living, apoptotic, and dead MSCs // Front Immunol. 2019. N 10. Р. 1191. doi: 10.3389/fimmu.2019.01191

[65] Bernardi L, Dos Santos CH, Pinheiro VA, et al. Transplantation of adipose-derived mesenchymal stem cells in refractory Crohn’s disease: Systematic review. Arq Bras Cir Dig (São Paulo). 2019;32(4):e1465. doi: 10.1590/0102-672020190001e1465

[66] Bernardi L., Dos Santos C.H., Pinheiro V.A., et al. Transplantation of adipose-derived mesenchymal stem cells in refractory Crohn’s disease: Systematic review // Arq Bras Cir Dig (São Paulo). 2019. Vol. 32, N 4. Р. e1465. doi: 10.1590/0102-672020190001e1465

[67] Ra JC, Kang SK, Shin IS, et al. Stem cell treatment for patients with autoimmune disease by systemic infusion of culture-expanded autologous adipose tissue derived mesenchymal stem cells. J Transl Med. 2011;(9):181. doi: 10.1186/1479-5876-9-181

[68] Ra J.C., Kang S.K., Shin I.S., et al. Stem cell treatment for patients with autoimmune disease by systemic infusion of culture-expanded autologous adipose tissue derived mesenchymal stem cells // J Transl Med. 2011. N 9. Р. 181. doi: 10.1186/1479-5876-9-181

[69] Bellei B, Migliano E, Tedesco M, et al. Maximizing non-enzymatic methods for harvesting adipose-derived stem from lipoaspirate: Technical considerations and clinical implications for regenerative surgery. Sci Reports. 2017;7(1):10015. doi: 10.1038/s41598-017-10710-6

[70] Bellei B., Migliano E., Tedesco M., et al. Maximizing non-enzymatic methods for harvesting adipose-derived stem from lipoaspirate: Technical considerations and clinical implications for regenerative surgery // Sci Reports. 2017. Vol. 7, N 1. Р. 10015. doi: 10.1038/s41598-017-10710-6

[71] Zavala G, Sandoval C, Meza D, et al. Differentiation of adipose-derived stem cells to functional CD105neg CD73low melanocyte precursors guided by defined culture condition. Stem Cell Res Ther. 2019;10(1):249. doi: 10.1186/s13287-019-1364-0

[72] Zavala G., Sandoval C., Meza D., et al. Differentiation of adipose-derived stem cells to functional CD105neg CD73low melanocyte precursors guided by defined culture condition // Stem Cell Res Ther. 2019. Vol. 10, N 1. Р. 249. doi: 10.1186/s13287-019-1364-0

[73] Kim JY, Park CD, Lee A, et al. Co-culture of melanocytes with adipose-derived stem cells as a potential substitute for co-culture with keratinocytes. Acta Derm Venereol. 2012;92(1):16–23. doi: 10.2340/00015555-1174

[74] Kim J.Y., Park C.D., Lee A., et al. Co-culture of melanocytes with adipose-derived stem cells as a potential substitute for co-culture with keratinocytes // Acta Derm Venereol. 2012. Vol. 92, N 1. Р. 16–23. doi: 10.2340/00015555-1174

[75] Lim WS, Kim CH, Kim JY, et al. Adipose-Derived stem cells improve efficacy of melanocyte transplantation in animal skin. Biomol Ther. 2014;22(4):328–333. doi: 10.4062/biomolther.2014.065

[76] Lim W.S., Kim C.H., Kim J.Y., et al. Adipose-Derived stem cells improve efficacy of melanocyte transplantation in animal skin // Biomol Ther. 2014. Vol. 22, N 4. Р. 328–333. doi: 10.4062/biomolther.2014.065

[77] Kuroda Y, Kitada M, Wakao S, et al. Unique multipotent cells in adult human mesenchymal cell populations. Proc Natl Acad Sci U.S.A. 2010;107(19):8639–8643. doi: 10.1073/pnas.0911647107

[78] Kuroda Y., Kitada M., Wakao S., et al. Unique multipotent cells in adult human mesenchymal cell populations // Proc Natl Acad Sci U.S.A. 2010. Vol. 107, N 19. Р. 8639–8643. doi: 10.1073/pnas.0911647107

[79] Dezawa M. Muse cells provide the pluripotency of mesenchymal stem cells: Direct contribution of muse cells to tissue regeneration. Cell Transplant. 2016;25(5):849–861. doi: 10.3727/096368916X690881

[80] Dezawa M. Muse cells provide the pluripotency of mesenchymal stem cells: Direct contribution of muse cells to tissue regeneration // Cell Transplant. 2016. Vol. 25, N 5. Р. 849–861. doi: 10.3727/096368916X690881

[81] Yamauchi T, Yamasaki K, Tsuchiyama K, et al. The potential of muse cells for regenerative medicine of skin: Procedures to reconstitute skin with muse cell-derived keratinocytes, fibroblasts, and melanocytes. J Invest Dermatol. 2017;137(12):2639–2642. doi: 10.1016/j.jid.2017.06.021

[82] Yamauchi T., Yamasaki K., Tsuchiyama K., et al. The potential of muse cells for regenerative medicine of skin: Procedures to reconstitute skin with muse cell-derived keratinocytes, fibroblasts, and melanocytes // J Invest Dermatol. 2017. Vol. 137, N 12. Р. 2639–2642. doi: 10.1016/j.jid.2017.06.021

[83] Fisch SC, Gimeno ML, Phan JD, et al. Pluripotent nontumorigenic multilineage differentiating stress enduring cells (Muse cells): A seven-year retrospective. Stem Cell Res Ther. 2017;8(1):227. doi: 10.1186/s13287-017-0674-3

[84] Fisch S.C., Gimeno M.L., Phan J.D., et al. Pluripotent nontumorigenic multilineage differentiating stress enduring cells (Muse cells): A seven-year retrospective // Stem Cell Res Ther. 2017. Vol. 8, N 1. Р. 227. doi: 10.1186/s13287-017-0674-3

[85] Tian T, Zhang RZ, Yang YH, et al. Muse cells derived from dermal tissues can differentiate into melanocytes. Cell Reprogram. 2017;19(2):116–122. doi: 10.1089/cell.2016.0032

[86] Tian T., Zhang R.Z., Yang Y.H., et al. Muse cells derived from dermal tissues can differentiate into melanocytes // Cell Reprogram. 2017. Vol. 19, N 2. Р. 116–122. doi: 10.1089/cell.2016.0032

[87] Tsuchiyama K, Wakao S, Kuroda Y, et al. Functional melanocytes are readily reprogrammable from multilineage: Differentiating stress-enduring (muse) cells, distinct stem cells in human fibroblasts. J Invest Dermatol. 2013;133(10):2425–2435. doi: 10.1038/jid.2013.172

[88] Tsuchiyama K., Wakao S., Kuroda Y., et al. Functional melanocytes are readily reprogrammable from multilineage: Differentiating stress-enduring (muse) cells, distinct stem cells in human fibroblasts // J Invest Dermatol. 2013. Vol. 133, N 10. Р. 2425–2435. doi: 10.1038/jid.2013.172

[89] Ikeda Y, Wada A, Hasegawa T, et al. Melanocyte progenitor cells reside in human subcutaneous adipose tissue. PLoS One. 2021;16(8):e0256622. doi: 10.1371/journal.pone.0256622

[90] Ikeda Y., Wada A., Hasegawa T., et al. Melanocyte progenitor cells reside in human subcutaneous adipose tissue // PLoS One. 2021. Vol. 16, N 8. Р. e0256622. doi: 10.1371/journal.pone.0256622

[91] Sun DZ, Abelson B, Babbar P, Damaser MS. Harnessing the mesenchymal stem cell secretome for regenerative urology. Nat Rev Urol. 2019;16(6):363–375. doi: 10.1038/s41585-019-0169-3

[92] Sun D.Z., Abelson B., Babbar P., Damaser M.S. Harnessing the mesenchymal stem cell secretome for regenerative urology // Nat Rev Urol. 2019. Vol. 16, N 6. Р. 363–375. doi: 10.1038/s41585-019-0169-3

[93] Vizoso FJ, Eiro N, Cid S, et al. Mesenchymal stem cell secretome: Toward cell-free therapeutic strategies in regenerative medicine. Int J Mol Sci. 2017;18(9):1852. doi: 10.3390/ijms18091852

[94] Vizoso F.J., Eiro N., Cid S., et al. Mesenchymal stem cell secretome: Toward cell-free therapeutic strategies in regenerative medicine // Int J Mol Sci. 2017. Vol. 18, N 9. Р. 1852. doi: 10.3390/ijms18091852

[95] Bellei B, Migliano E, Tedesco M, et al. Adipose tissue-derived extracellular fraction characterization: Biological and clinical considerations in regenerative medicine. Stem Cell Res Ther. 2018;9(1):207. doi: 10.1186/s13287-018-0956-4

[96] Bellei B., Migliano E., Tedesco M., et al. Adipose tissue-derived extracellular fraction characterization: Biological and clinical considerations in regenerative medicine // Stem Cell Res Ther. 2018. Vol. 9, N 1. Р. 207. doi: 10.1186/s13287-018-0956-4

[97] Bellei B, Papaccio F, Filoni A, et al. Extracellular fraction of adipose tissue as an innovative regenerative approach for vitiligo treatment. Exp Dermatol. 2019;28(6):695–703. doi: 10.1111/exd.13954

[98] Bellei B., Papaccio F., Filoni A., et al. Extracellular fraction of adipose tissue as an innovative regenerative approach for vitiligo treatment // Exp Dermatol. 2019. Vol. 28, N 6. Р. 695–703. doi: 10.1111/exd.13954

[99] Goldstein NB, Koster MI, Jones KL, et al. Repigmentation of human vitiligo skin by NBUVB is controlled by transcription of GLI1 and activation of the β-catenin pathway in the hair follicle bulge stem cells. J Invest Dermatol. 2018;138(3):657–668. doi: 10.1016/j.jid.2017.09.040

[100] Goldstein N.B., Koster M.I., Jones K.L., et al. Repigmentation of human vitiligo skin by NBUVB is controlled by transcription of GLI1 and activation of the β-catenin pathway in the hair follicle bulge stem cells // J Invest Dermatol. 2018. Vol. 138, N 3. Р. 657–668. doi: 10.1016/j.jid.2017.09.040

[101] Regazzetti C, Joly F, Marty C, et al. Transcriptional analysis of vitiligo skin reveals the alteration of Wnt pathway: A promising target for repigmenting vitiligo patients. J Invest Dermatol. 2015;135(12):3105–3114. doi: 10.1038/jid.2015.335

[102] Regazzetti C., Joly F., Marty C., et al. Transcriptional analysis of vitiligo skin reveals the alteration of Wnt pathway: A promising target for repigmenting vitiligo patients // J Invest Dermatol. 2015. Vol. 135, N 12. Р. 3105–3114. doi: 10.1038/jid.2015.335

[103] Braunersreuther V, Jaquet V. Reactive oxygen species in myocardial reperfusion injury: From physiopathology to therapeutic approaches. Curr Pharm Biotechnol. 2011;13(1):97–114. doi: 10.2174/138920112798868782

[104] Braunersreuther V., Jaquet V. Reactive oxygen species in myocardial reperfusion injury: From physiopathology to therapeutic approaches // Curr Pharm Biotechnol. 2011. Vol. 13, N 1. Р. 97–114. doi: 10.2174/138920112798868782

[105] Xuan Y, Yang Y, Xiang L, Zhang C. The role of oxidative stress in the pathogenesis of vitiligo: A culprit for melanocyte death. Oxid Med Cell Longev. 2022;2022:8498472. doi: 10.1155/2022/8498472

[106] Xuan Y., Yang Y., Xiang L., Zhang C. The role of oxidative stress in the pathogenesis of vitiligo: A culprit for melanocyte death // Oxid Med Cell Longev. 2022. Vol. 2022. Р. 8498472. doi: 10.1155/2022/8498472

RIGHTS & PERMISSIONS

Olisova O.Y., Timashev P.S., Pishulina E.V., Semiklet J.M., Berdnikova E.A., Koteneva P.I., Lomonosov K.M.