Gingiva as a source of stromal cells with high differentiating and reparative potential



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Abstract

This review is focused on systematization of data describing several features of multipotent mesenchymal stromal cells. It also presents a detailed review of differentiation and reparation potential of human gingiva-derived stromal cells and opportunities of their therapeutic application in regenerative medicine.

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About the authors

V. L Zorin

Human Stem Cells Institute; Central Clinical Hospital with Outpatient Health Center

A. I Zorina

Human Stem Cells Institute

I. I Eremin

Central Clinical Hospital with Outpatient Health Center

R. V Deev

Human Stem Cells Institute; Central Clinical Hospital with Outpatient Health Center; I.P. Pavlov Ryazan State Medical University

P. B Kopnin

N.N. Blokhin Cancer Research Center

G. A Volozhin

A.I. Evdokimov Moscow State University of Medicine and Dentistry

A. A Pulin

Central Clinical Hospital with Outpatient Health Center

References

  1. Lindvall O., Kokaia Z. Stem cells for the treatment of neurological disorders. Nature 2006; 441: 1094-6.
  2. Segers V., Lee R. Stem-cell therapy for cardiac disease. Nature 2008; 451: 937-42.
  3. El-Sayed K., Dörfer С. Gingival Mesenchymal Stem/Progenitor Cells: A Unique Tissue Engineering Gem. Stem Cells International 2016; 2016: 7154327.
  4. Fournier В., Loison-Robert L., Ferré F. et al. Characterisation of human gingival neural crest-derived stem cells in monolayer and neurosphere cultures. European Cells and Materials 2016; 31: 40-58.
  5. Pevsner-Fischer M., Levin S., Zipori D. The origins of mesenchymal stromal cell heterogeneity. Stem Cell Rev. 2011; 7: 560-8.
  6. Fournier B., Larjava H., Häkkinen L. Gingiva as a source of stem cells with therapeutic potential. Stem Cells Dev. 2013; 22: 3157-77.
  7. Volponi А., Sharpe Р. The tooth - a treasure chest of stem cells. British Dental Journal 2013; 215(7): 353-8.
  8. Jin S., Lee J., Yun J.H. et al. Isolation and characterization of human mesenchymal stem cells from gingival connective tissue. J. Periodont. Res. 2015; 50t4): 461-7.
  9. Caplan A. Mesenchymal stem cells. J. Orthop. Res. 1991; 9: 641-50.
  10. Pittenger M., Mackay A., Beck S. et al. Multilineage potential of adult human mesenchymal stem cells. Science 1999; 284: 143-7.
  11. Horwitz E., Le Blanc K., Dominici M. et al. Clarification of the nomenclature for MSC: The Interrnational Society for Cellular Therapy position statement. Cytotherapy 2005; 7t5): 393-5.
  12. Mao J., Prockop D. Stem cells in the face: tooth regeneration and beyond. Cell Stem Cell 2010; 11: 291-301.
  13. Bianco P., Robey P. Skeletal stem cells. In: Lanza R.P., editor. Handbook of Adult and Fetal Stem Cells. San Diego: Academic Press; 2004. p. 415-24.
  14. Чайлахян Р.К., Лалыкина К.С. Спонтанная и индуцированная дифференцировка костной ткани в популяции фибробластоподобных клеток, полученных из длительных монослойных культур костного мозга и селезенки. ДАН СССР 1969; 187(2): 473-9.
  15. Friedenstein A., Deriglasova U., Kulagina N. et al. Precursors for fibroblasts in different populations of hematopoietic cells as detected by the in vitro colony assay method. Exp. Hematol. 1974; 2: 83-92.
  16. Чайлахян Р.К., Фриденштейн А.Я., Васильев А.В. Клонообразование в монослойных культурах костного мозга и селезенки. Бюлл. эксперим. биол. 1970; 2: 94-8.
  17. Friedenstein A., Chailakhyan R., Lalykina K. The development of fibroblast colonies in monolayer cultures of guinea-pig bone marrow and spleen cells. Cell Tissue Kinet. 1970; 3: 393-403.
  18. Чайлахян Р.К., Герасимов Ю.В., Куралесова А.И. и соавт. Пролиферативные и дифференцировочные потенции индивидуальных клонов стромальных клеток-предшественников костного мозга. Известия АН. Серия биологическая 2001; 6: 682-92.
  19. Фриденштейн А.Я., Лурия Е.А. Изменение численности клоногенных стромальных клеток в кроветворных органах. В: Клеточные основы кроветворного микроокружения. Москва: Медицина; 1980. с. 122-5.
  20. Владимирская Е.В., Кошель И.В. Стромальные фибробласты нормального костного мозга у детей. Гематология и трансфузиология 1990; 1: 3-5.
  21. Астахова В.С. Активность КОЕф костного мозга - показатель регенераторного потенциала кости у человека. В: Туник Л.В., редактор. Остеогенные клетки-предшественники костного мозга человека. Киев: Феникс; 2000. с. 87-132.
  22. Kuznetsov S., Mankani М., Bianco Р. et al. Enumeration of the colony-forming units-fibroblast from mouse and human bone marrow in normal and pathological conditions. Stem Cell Research 2009; 2: 83-94.
  23. Morrison S., Kimble J. Asymmetric and symmetric stem cell divisions in development and cancer. Nature 2006; 441(7097): 1068-74.
  24. Фриденштейн А.Я., Чайлахян Р.К., Герасимов Ю.В. Пролиферативные и дифференцировочные потенции скелетогенных костномозговых колониеобразующих клеток. Цитология 1986; XXVIII(3): 341-9.
  25. Friedenstein A., Chailakhyan R., Gerasimov U. Bone marrow osteogenic stem cells: in vitro cultivation and transplantation in diffusion chambers. Cell Tissue Kinet. 1987; 20: 263-72.
  26. Augello A., Kurth T., Bari C. Mesenchymal stem cells: a perspective from in vitro cultures to in vivo migration and niches. Eur. Cell. Mater. 2010; 20: 121-33.
  27. Al-Nbaheen M., Vishnubalaji R., Ali D. et al. Human stromal (mesenchymal) stem cells from bone marrow, adipose tissue and skin exhibit differences in molecular phenotype and differentiation potential. Stem Cell Rev. 2013; 9(1): 32-43.
  28. Keating A. Mesenchymal stromal cells: new directions. Cell Stem Cell 2012; 14: 709-16.
  29. Bianco P., Cao X., Frenette P. et al. The meaning, the sense and the significance: translating the science of mesenchymal stem cells into medicine. Nat. Med. 2013; 19: 35-42.
  30. Nombela-Arrieta C., Ritz J., Silberstein L. The elusive nature and function of mesenchymal stem cells. Nat. Rev. Mol. Cell Biol. 2011; 12(2): 126-31.
  31. Oswald J., Boxberger S., Jurgensen B. et al. Mesenchymal stem cells can be differentiated into endothelial cells in vitro. Stem Cells 2004; 22(3): 377-84.
  32. Meligy F., Shigemura K., Behnsawy H. et al. The efficiency of in vitro isolation and myogenic differentiation of MSCs derived from adipose connective tissue, bone marrow, and skeletal muscle tissue. In Vitro Cell. Dev. Biol. Anim. 2012; 48(4): 203-15.
  33. Tropel P., Platet N., Platel J. et al. Functional neuronal differentiation of bone marrow-derived mesenchymal stem cells. Stem Cells 2006; 24(12): 2868-76.
  34. Sasaki M., Abe R., Fujita Y. et al. Mesenchymal stem cells are recruited into wounded skin and contribute to wound repair by transdifferentiation into multiple skin cell type. J. Immunol. 2008; 180(4): 2581-7.
  35. Wu Y., Chen L., Scott P. et al. Mesenchymal stem cells enhance wound healing through differentiation and angiogenesis. Stem Cells 2007; 25: 2648-59.
  36. Wu Y., Zhao R.C., Tredget E.E. Concise review. Bone marrow derived stem/progenitor cells in cutaneous repair and regeneration. Stem Cells 2010; 28: 905-15.
  37. Harris R.G., Herzog E.L., Bruscia E.M. et al. Lack of a fusion requirement for development of bone marrow-derived epithelia. Science 2004; 305: 90-3.
  38. Galderisi U., Giordano A. The gap between the physiological and therapeutic roles of mesenchymal stem cells. Med. Res. Rev. 2014; 34(5): 1100-26.
  39. Boink M., van den Broek L., Roffel S. et al. Different wound healing properties of dermis, adipose, and gingiva mesenchymal stromal cells. Wound Repair Regen. 2016; 24(1): 100-9.
  40. Shakoori P., Zhang Q., Le A.D. Applications of Mesenchymal Stem Cells in Oral and Craniofacial Regeneration. Oral Maxillofac. Surg. Clin. North. Am. 2017; 29(1): 19-25.
  41. Wang Y., Chen X., Cao W. et al. Plasticity of mesenchymal stem cells in immunomodulation: pathological and therapeutic implications. Nat. Immunol. 2014; 15(11): 1009-16.
  42. Nauta A., Fibbe W. Immunomodulatory properties of mesenchymal stromal cells. Blood 2007; 110: 3499-506.
  43. Chen L., Tredget E., Wu P. et al. Paracrine factors of mesenchymal stem cells recruit macrophages and endothelial lineage cells and enhance wound healing. PLoS ONE 2008; 3(4): 1886.
  44. Maxson S., Lopez E., Yoo D. Concise review: role of mesenchymal stem cells in wound repair. Stem Cells Transl. Med. 2012; 1: 142-9.
  45. Dominici М., Le Blanc K., Mueller I. et al. Minimal criteria for defining ultipotent mesenchymal stromal cells. The International Society for Cellular Therapy position statement. Cytotherapy 2006; 8(4): 315-7.
  46. Sorrell J., Caplan A. Fibroblast heterogeneity: more than skin deep. J. Cell Sci. 2004; 117: 667-75.
  47. Haniffa M., Collin M., Buckley C. et al. Mesenchymal stem cells: the fibroblasts' new clothes? Haematologica 2009; 94: 258-63.
  48. Wong T., McGrath J., Navsaria H. The role of fibroblasts in tissue engineering and regeneration. Br. J. Dermatol. 2007; 156: 1149-55.
  49. Пулин А.А., Сабурина И.Н., Репин B.C. Поверхностные маркеры, характеризующие мультипотентные мезенхимальные стромальные клетки (ММСК) костного мозга человека. Гены и Клетки 2008; 3(3): 25-30.
  50. Robey P.G., Kuznetsov S.A., Riminucci M. et al. Bone marrow stromal cell assays: in vitro and in vivo. Methods Mol. Biol. 2014; 1130: 279-93.
  51. Davies L., Locke M., Webb R. et al. A multipotent neural crest-derived progenitor cell population is resident within the oral mucosa lamina propria. Stem Cells Dev. 2010; 19: 819-30.
  52. Лебединская О., Горская Ю., Куралесова А. Mорфологическая характеристика колоний стромальных клеток-предшественников в культурах гетеротопных трансплантатов костного мозга и селезенки мышей разного возраста. Морфология: научно-теоретический мед. журнал 2004; 126(6): 46-9.
  53. Häkkinen L., Larjava H., Fournier B. Distinct phenotype and therapeutic potential of gingival fibroblasts. Cytotherapy 2014; 16: 1171-86.
  54. Djouad F., Bouffi C., Ghannam S. et al. Mesenchymal stem cells: innovative therapeutic tools for rheumatic diseases. Nat. Rev. Rheumatol. 2009; 5(7): 392-9.
  55. Hocking A., Gibran N. Mesenchymal stem cells: paracrine signaling and differentiation during cutaneous wound repair. Exp. Cell Res. 2010; 316: 2213-9.
  56. Linard С., Tissedre F., Busson E. et al. Therapeutic Potential of Gingival Fibroblasts for Cutaneous Radiation Syndrome: Comparison to Bone Marrow-Mesenchymal Stem Cell Grafts. Stem Oells and Development 2015; 24(10): 1182-93.
  57. Bourin P., Bunnell B.A., Casteilla L. et al. Stromal cells from the adipose tissue-derived stromal vascular fraction and culture expanded adipose tissue-derived stromal/stem cells: a joint statement of the International Federation for Adipose Therapeutics and Science (IFATS) and the International Society for Cellular Therapy (ISCT). Cytotherapy 2013; 15(6): 641-8.
  58. Бозо И., Зорин В., Еремин И. и соавт. Особенности мультипотентных мезенхимальных стромальных клеток, полученных из различных интраоральных источников. Гены и Клетки 2014; 9(4): 34-42.
  59. Sousa B., Parreira R., Fonseca E. et al. Human adult stem cells from diverse origins: an overview from multiparametric immunophenotyping to clinical applications. Cytometry A 2014; 85(1): 43-77.
  60. Chen L., He D., Zhang Y. The differentiation of human placenta-derived mesenchymal stem cells into dopaminergic cells in vitro. Cell. Mol. Biol. Lett. 2009; 14: 528-36.
  61. da Silva Meirelles L., Chagastelles P., Nardi N. Mesenchymal stem cells reside in virtually all post-natal organs and tissues. J. Cell Sci. 2006; 119: 2204-13.
  62. Бозо И.Я., Деев Р.В., Пинаев Г.П. «Фибробласт» - специализированная клетка или функциональное состояние клеток мезенхимного происхождения? Цитология 2010; 52(2): 99-109.
  63. Sacchetti В., Funari А., Remoli С. et al. No Identical ''Mesenchymal Stem Cells'' at Different Times and Sites: Human Committed Progenitors of Distinct Origin and Differentiation Potential Are Incorporated as Adventitial Cells in Microvessels. Stem Cell Reports 2016; 6: 897-913.
  64. Schatteman G., Ma N. Old bone marrow cells inhibit skin wound vascularisation. Stem Cells 2006; 24: 717-21.
  65. Chen J., Wong V., Gurtner G. Therapeutic potential of bone marrow-derived mesenchymal stem cells for cutaneous wound healing. Front. Immunol. 2012; 3: 192-212.
  66. Fournier B., Ferre F., Couty L. et al. Multipotent progenitor cells in gingival connective tissue. Tissue Eng. Part A 2010; 16: 2891-9.
  67. El-Sayed K., Paris S., Graetz С. et al. Isolation and characterization of human gingival margin-derived STRO-1/MACS( + ) and MACS(-) cell populations. International Journal of Oral Science 2014; 7(2): 80-8.
  68. Zhang Q., Shi S., Liu Y. Mesenchymal stem cells derived from human gingiva are capable of immunomodulatory functions and ameliorate inflammation-related tissue destruction in experimental colitis. J. Immunol. 2009; 183: 7787-98.
  69. Mak K., Manji A., Gallant-Behm C. et al. Scarless healing of oral mucosa is characterized by faster resolution of inflammation and control of myofibroblast action compared to skin wounds in the red Duroc pig model. J. Dermatol. Sci. 2009; 56: 168-80.
  70. Wong J., Gallant-Behm C., Wiebe C. et al. Wound healing in oral mucosa results in reduced scar formation as compared with skin: evidence from the red Duroc pig model and humans. Wound Repair Regen. 2009; 17: 717-29.
  71. Glim J., van Egmond M., Niessen F. et al. Detrimental dermal wound healing: what can we learn from the oral mucosa? Wound Repair Regen. 2013; 21: 648-60.
  72. Larjava H., Wiebe C., Gallant-Behm С. et al. Exploring scarless healing of oral soft tissues. Journal of the Canadian Dental Association 2011; 77: 18-28.
  73. Hakkinen L., Uitto V.J., Larjava H. Cell biology of gingival wound healing. Periodontol. 2000; 24: 127-52.
  74. Chesney J., Bucala R. Peripheral blood fibrocytes: novel fibroblast-like cells that present antigen and mediate tissue repair. Biochem. Soc. Trans. 1997; 25: 520.
  75. Ivarsson M., Sundberg C., Farrokhnia N. et al. Recruitment of type I collagen producing cells from the microvasculature in vitro. Exp. Cell Res. 1996; 229(2): 336-49.
  76. Mah W., Jiang G., Olver D. et al. Human gingival fibroblasts display a non-fibrotic phenotype distinct from skin fibroblasts in threedimensional cultures. PloS oNe 2014; 9: 907-15.
  77. Chai Y., Jiang X., Ito Y. et al. Fate of the mammalian cranial neural crest during tooth and mandibular morphogenesis. Development 2000; 127: 1671-9.
  78. Chai Y., Maxson R. Recent advances in craniofacial morphogenesis. Dev. Dyn. 2006; 235: 2353-75.
  79. Le Douarin N., Calloni G., Dupin E. The stem cells of the neural crest. Cell Cycle 2008; 7: 1013-9.
  80. Yoshida T., Vivatbutsiri P., Morriss-Kay G. et al. Cell lineage in mammalian craniofacial mesenchyme. Mech. Dev. 2008; 125: 797-808.
  81. Xu X., Chen C., Akiyama K. et al. Gingivae Contain Neuralcrest- and Mesoderm-derived Mesenchymal Stem Cells. J. Dent. Res. 2013; 92(9): 825-32.
  82. Tang L., Li N., Xie H. et al. Characterization of mesenchymal stem cells from human normal and hyperplastic gingiva. J. Cell. Physiol. 2011; 226: 832-42.
  83. Mitrano T., Grob M., Carrion F. et al. Culture and characterization of mesenchymal stem cells from human gingival tissue. J. Periodontol. 2010; 81: 917-25.
  84. Зорин В., Зорина А., Еремин И. и соавт. Сравнительный анализ остеогенного потенциала мультипотентных мезенхимальных стромальных клеток слизистой оболочки полости рта и костного мозга. Гены и Клетки 2014; 9(1): 50-7.
  85. Tomar G., Srivastava R., Gupta N. et al. Human gingivaderived mesenchymal stem cells are superior to bone marrow-derived mesenchymal stem cells for cell therapy in regenerative medicine. Biochem. Biophys. Res. Commun. 2010; 393: 377-83.
  86. Zhang Q., Nguyen A., Yu W. et al. Human oral mucosa and gingiva: a unique reservoir for mesenchymal stem cells. Journal of Dental Research 2012; 91(11): 1011-8.
  87. Robey P.G., Kuznetsov S.A., Riminucci M. et al. Bone marrow stromal cell assays: in vitro and in vivo. Methods Mol. Biol. 2014; 1130: 279-93.
  88. Ge S., Mrozik K., Menicanin D. et al. Isolation and characterization of mesenchymal stem cell-like cells from healthy and inflamed gingival tissue: potential use for clinical therapy. Regen. Med. 2012; 7(6): 819-32.
  89. Petrof G., Lwin S.M., Martinez-Queipo M. et al. Potential of Systemic Allogeneic Mesenchymal Stromal Cell Therapy for Children with Recessive Dystrophic Epidermolysis Bullosa. Journal of Investigative Dermatology 2015; 135: 2319-21.
  90. El-Darouti M., Fawzy M., Amin I. et al. Treatment dystrophic epidermolysis bullosa with bone marrow non-hematopoietic stem cells: a randomized controlled trial. Dermalogic Therapy 2016; 29: 96-100.
  91. Yang H., Gao L., An Y. et al. Comparison of mesenchymal stem cells derived from gingival tissue and periodontal ligament in different incubation conditions. Biomaterials 2013; 34(29): 7033-47.
  92. Zorin V.L., Komlev V.S., Zorina A.I. et al. Octacalcium phosphate ceramics combined with gingiva-derived stromal cells for engineered functional bone grafts. Biomed. Mater. 2014; 9(5): 055005.
  93. Wang F., Yu N., Yan X. et al. Gingiva-derived mesenchymal stem cell-mediated therapeutic approach for bone tissue regeneration. Stem Cells Dev. 2011; 20: 2093-102.
  94. El-Sayed K., Paris S., Becker S. et al. Periodontal regeneration employing gingival margin-derived stem/progenitor cells: an animal study. J. Clin. Periodontol. 2012; 39: 861-70.
  95. Li N., Liu N., Zhou J. et al. Inflammatory environment induces gingival tissue-specific mesenchymal stem cells to differentiate towards a pro-fibrotic phenotype. Biol. Cell 2013; 105(6): 261-75.
  96. Zhang W., Walboomers X., Kuppevelt T. et al. In vivo evaluation of human dental pulp stem cells differentiated towards multiple lineages. J. Tissue Eng. Regen. Med. 2008; 2: 117-25
  97. Xu X., Chen C., Akiyama K. et al. Gingivae Contain Neuralcrestand Mesoderm-derived Mesenchymal Stem Cells. J. Dent. Res. 2013; 92(9): 825-32.
  98. Fernandes K., Toma J., Miller F. Multipotent skin-derived precursors: adult neural crest-related precursors with therapeutic potential. Philos. Trans. R. Soc. Lond. B: Biol. Sci. 2008; 363: 185-98.
  99. Зорин В., Еремин И., Рыбко В. и соавт. Слизистая оболочка полости рта - новый источник получения миобластов. Гены и Клетки 2014; IXC3J: 5-13.
  100. Ansari S., Chen C., Xu X. et al. Muscle Tissue Engineering Using Gingival Mesenchymal Stem Cells Encapsulated in Alginate Hydrogels Containing Multiple Growth Factors. Annals of Biomedical Engineering 2016; 44t6): 1908-20.
  101. Durand E., Fournier B., Couty L. et al. Endoluminal gingival fibroblast transfer reduces the size of rabbit carotid aneurisms via elastin repair. Arterioscler. Thromb. Vasc. Biol. 2010; 32: 1892-901.
  102. Zhang Q., Su W., Shi S. et al. Human gingiva-derived mesenchymal stem cells elicit polarization of M2 macrophages and enhance cutaneous wound healing. Stem Cells 2010; 28: 1856-68.
  103. Liu J., Yu F., Sun Y. et al. Concise Reviews: Characteristics and Potential Applications of Human Dental Tissue-Derived Mesenchymal Stem Cells. Stem Cells 2015; 33: 627-38.
  104. Nemeth K., Leelahavanichkul A., Yuen P. et al. Bone marrow stromal cells attenuate sepsis via prostaglandin E(2)-dependent reprogramming of host macrophages to increase their interleukin-10 production. Nat. Med. 2009; 15: 42-9.
  105. Galler K., Cavender A., Koeklue U. et al. Bioengineering of dental stem cells in a PEGylated fibrin gel. Regen. Med. 2011; 6: 191-200.
  106. Maggini J., Mirkin G., Bognanni I. et al. Mouse bone marrow-derived mesenchymal stromal cells turn activated macrophages into a regulatory-like profile. PLoS ONE 2010; 5t2): 9252.
  107. Yamaza T., Kentaro A., Chen C. et al. Immunomodulatory properties of stem cells from human exfoliated deciduous teeth. Stem Cell Res. Ther. 2010; 1(1): 5.
  108. Le Blanc K., Frassoni F., Ball L. et al. Treatment of severe acute graft versus host disease with third party haploidentical mesenchymal stem cells. Lancet 2004; 363: 1439-41.
  109. Hunt D., Jahoda C., Chandran S. Multipotent skin-derived precursors: from biology to clinical translation. Curr. Opin. Biotechnol. 2009; 20: 522-30.
  110. Svendsen C., Bhattacharyya A., Tai Y. Neurons from stem cells: preventing an identity crisis. Nat. Rev. Neurosci. 2001; 2: 831-4.
  111. Abe S., Hamada K., Miura M. et al. Neural crest stem cell property of apical pulp cells derived from human developing tooth. Cell Biol. Int. 2012; 36: 927-36.
  112. Taneyhill L. To adhere or not to adhere: the role of Cadherins in neural crest development. Cell Adh. Migr. 2008; 2: 223-30.
  113. Taneyhill L., Schiffmacher A. Cadherin dynamics during neural crest cell ontogeny. Prog. Mol. Biol. Transl. Sci. 2013; 116: 291-315.
  114. Yagita Y., Sakurai T., Tanaka H. et al. N-cadherin mediates interaction between precursor cells in the subventricular zone and regulates further differentiation. J. Neurosci. Res. 2009; 87: 3331-42.
  115. Зорина A., Бозо И., Зорин В. и соавт. Фибробласты дермы: особенности цитогенеза, цитофизиологии и возможности их клинического применения. Гены и Клетки 2011; 6(2): 15-26.
  116. Chang H., Chi J., Dudoit S. et al. Diversity, topographic differentiation, and positional memory in human fibroblasts. PNAs USA 2009; 99: 12877-82.
  117. Gogly B., Naveau A., Fournier B. et al. Preservation of rabbit aorta elastin from degradation by gingival fibroblasts in an ex vivo model. Arterioscler. Thromb. Vasc. Biol. 2007; 27: 1984-90
  118. Häkkinen L., Larjava H., Koivisto L. Granulation tissue formation and remodeling. Endodontic Topics 2012; 24: 94-129.
  119. Dufour A., Overall C. Missing the target: matrix metalloproteinase antitargets in inflammation and cancer. Trends Pharmacol. Sci. 2013; 34: 233-42.
  120. Guo F., Carter D., Mukhopadhyay A. et al. Gingival fibroblasts display reduced adhesion and spreading on extracellular matrix: a possible basis for scarless tissue repair? PLoS ONE 2011; 6: 270-97.
  121. Cappellesso-Fleury S., Puissant-Lubrano B., Apoil P. et al. Human fibroblasts share immunosuppressive properties with bone marrow mesenchymal stem cells. J. Clin. Immunol. 2010; 30: 607-19.
  122. Seguier S., Tartour E., Guerin C. et al. Inhibition of the differentiation of monocyte-derived dendritic cells by human gingival fibroblasts. PLoS ONE 2013; 8: 709-37.
  123. Hosokawa Y., Hosokawa I., Ozaki K. et al. Cytokines differentially regulate ICAM-1 and VCAM-1 expression on human gingival fibroblasts. Clin. Exp. Immunol. 2006; 144: 494-502.
  124. Okada Y., Meguro M., Ohyama H. et al. Human leukocyte histocompatibility antigen class II-induced cytokines from human gingival fibroblasts promote proliferation of human umbilical vein endothelial cells: potential association with enhanced angiogenesis in chronic periodontal inflammation. J. Periodont. Res. 2009; 44: 103-9.
  125. McKeown S., Hyland P., Locke M. et al. Keratinocyte growth factor and scatter factor expression by regionally defined oral fibroblasts. Eur. J. Oral Sci. 2003; 111: 42-50.
  126. Chinnathambi S., Bickenbach J. Human skin and gingival keratinocytes show differential regulation of matrix metalloproteinases when combined with fibroblasts in 3-dimensional cultures. J. Periodontol. 2005; 76: 1072-83.
  127. Koivisto L., Larjava H., Häkkinen L. Reepithelialization of wounds. Endodontic Topics 2012; 24: 59-93.
  128. Karring T., Ostergaard E., Loe H. Conservation of tissue specificity after heterotopic transplantation of gingiva and alveolar mucosa. J. Periodont. Res. 1971; 6: 282-93.
  129. Kobayashi K., Suzuki T., Nomoto Y. et al. Potential of heterotopic fibroblasts as autologous transplanted cells for tracheal epithelial regeneration. Tissue Eng. 2007; 13: 2175-84.
  130. Kobayashi K., Suzuki T., Nomoto Y. et al. A tissue-engineered trachea derived from a framed collagen scaffold, gingival fibroblasts and adipose-derived stem cells. Biomaterials 2010; 31: 4855-63.
  131. Locke M., Hyland P., Irwin C. et al. Modulation of gingival epithelial phenotypes by interactions with regionally defined populations of fibroblasts. J. Periodont. Res. 2008; 43: 279-89.
  132. Karring T., Lang N., Loe H. The role of gingival connective tissue in determining epithelial differentiation. J. Periodont. Res. 1975; 10: 1-11.
  133. Lorimier S., Hornebeck W., Godeau G. et al. Morphometric studies of collagen and fibrin lattices contracted by human gingival fibroblasts; comparison with dermal fibroblasts. J. Dent. Res. 1998; 77: 1717-29.
  134. Parsonage G., Filer A., Haworth O. et al. A stromal address code defined by fibroblasts. Trends Immunol. 2005; 26: 150-6.
  135. Palaiologou A., Yukna R., Moses R. et al. Gingival, dermal, and periodontal ligament fibroblasts express different extracellular matrix receptors. J. Periodontol. 2001; 72: 798-807.
  136. Ebisawa K., Kato R., Okada M. et al. Gingival and dermal fibroblasts: their similarities and differences revealed from gene expression. J. Biosci. Bioeng. 2011; 111: 255-8.
  137. Brizzi M., Tarone G., Defilippi P. Extracellular matrix, integrins, and growth factors as tailors of the stem cell niche. Curr. Opin. Cell Biol. 2012; 24: 645-51.
  138. Mahanonda R., Sa-Ard-Iam N., Montreekachon P. et al. IL-8 and IDO expression by human gingival fibroblasts via TLRs. J. Immunol. 2007; 178: 1151-7.
  139. Su W., Zhang Q., Shi S. et al. Human gingiva derived mesenchymal stromal cells attenuate contact hypersensitivity via prostaglandin E(2)-dependent mechanisms. Stem Cells 2011; 29: 1849-60.
  140. Грудянов А.И., Степанова И.И., Зорин В.Л. и соавт. Применение аутогенных фибробластов слизистой оболочки полости рта человека для устранения рецессий десны. Стоматология 2013; 1: 21-5.
  141. Неробеев А.И., Голубева С.Н., Добродеев А.С. и соавт. Нейрофиброматоз - возможности хирургической реабилитации. Анналы пластической реконструктивной и эстетической хирургии 2014; 4: 10-20.
  142. Görski B. Gingiva as a new and the most accessible source of mesenchymal stem cells from the oral cavity to be used in regenerative therapies. Postepy Hig. Med. Dosw. (Online) 2016; 70(0): 858-71.
  143. Lucas T., Waisman A., Ranjan R. et al. Differential roles of macrophages in diverse phases of skin repair. J. Immunol. 2010; 184: 3964-77.
  144. Yano K., Brown L., Detmar M. Control of hair growth and follicle size by VEGF-mediated angiogenesis. J. Clin. Invest. 2001; 107: 409-17.
  145. Felder J., Goyal S., Attinger C. A systematic review of skin substitutes for foot ulcers. Plast. Reconstr. Surg. 2012; 130: 145-64.
  146. Moshaverinia А., Chen С., Xu Х. et al. Bone regeneration potential of stem cells derived from periodontal ligament or gingival tissue sources encapsulated in RGD-modified alginate scaffold. Tissue Engineering Part A 2014; 20(3-4): 611-21.
  147. Xu Q.C., Wang Z.G., Ji Q.X. et al. Systemically transplanted human gingiva-derived mesenchymal stem cells contributing to bone tissue regeneration. International Journal of Clinical and Experimental Pathology 2014; 7(8): 4922-9.
  148. Корсаков И., Самчук Д., Пулин А. и соавт. Влияние аутологичных клеток альвеолярной десны, обладающих миогенным потенциалом, на регенерацию скелетной мышечной ткани. Гены и Клетки. В печати 2017.
  149. Zorin V., Pulin А., Eremin I. et.al. Myogenic potential of human alveolar mucosa derived cells. Cell Cycle 2017; 16(6): 545-55.
  150. Chhetri D., Berke G. Injection of cultured autologous fibroblasts for human vocal fold scars. Laryngoscope 2011; 121: 785-92.
  151. Zhang Q., Nguyen P., Xu Q. et al. Neural progenitor-like cells induced from human gingiva-derived mesenchymal stem cells regulate myelination of schwann cells in rat sciatic nerve regeneration. Stem Cells Translational Medicine 2016; 5: 1-13.
  152. Zhang Q., Nguyen A., Shi S. et al. Threedimensional spheroid culture of human gingiva-derived mesenchymal stem cells enhances mitigation of chemotherapyinduced oral mucositis. Stem Cells Dev. 2011; 21: 937-47.
  153. Chen M., Su W., Lin X. et al. Adoptive transfer of human gingiva- derived mesenchymal stem cells ameliorates collagen-induced arthritis VIA suppressing Th1 and Th17 and enhancing regulatory T cell differentiation. Arthritis Rheum. 2013; 65: 1181-93.
  154. Takahashi K., Yamanaka S. Induction of pluripotent stem cells from mouse embryonic and adult fibroblast cultures by defined factors. Cell 2006; 126: 663-76.
  155. Hynes K., Menicanin D., Mrozik K. et al. Generation of functional mesenchymal stem cells from different induced pluripotent stem cell lines. Stem Cells and Development 2014; 23t10): 1084-96.
  156. Umezaki Y., Hashimoto Y., Nishishita Т. et al. Human Gingival Integration-Free iPSCs; a Source for MSC-Like Cells. Int. J. Mol. Sci. 2015; 16: 13633-48.
  157. Okita K., Matsumura Y., Sato Y. et al. A more efficient method to generate integration-free human iPS cells. Nat. Methods 2011; 8: 409-12.
  158. Chun Y., Byun K., Lee В. Induced pluripotent stem cells and personalized medicine: current progress and future perspectives. Anat. Cell Biol. 2011; 44: 245-55.
  159. Streckfuss-Bömeke K., Wolf F., Azizian A. et al. Comparative study of human-induced pluripotent stem cells derived from bone marrow cells, hair keratinocytes, and skin fibroblasts. Eur. Heart J. 2013; 34(33): 2618-29.
  160. Egusa H., Okita K., Kayashima H. et al. Gingival fibroblasts as a promising source of induced pluripotent stem cells. PLoS ONE 2010; 5(9): 127-43.
  161. Wada N., Wang В., Lin N.H. et al. Induced pluripotent stem cell lines derived from human gingival fibroblasts and periodontal ligament fibroblasts. Journal of Periodontal Research 2011; 46(4): 438-47.
  162. Yamanaka S. Induced pluripotent stem cells: past, present, and future. Cell Stem Cell 2012; 10(6): 678-84.
  163. Hussein S., Nagy K., Nagy A. Human induced pluripotent stem cells: the past, present, and future. Clinical Pharmacology &Therapeutics 2011; 89(5): 741-5.
  164. Yin X., Li Y., Li J. et al. Generation and periodontal differentiation of human gingival fibroblasts-derived integration-free induced pluripotent stem cells. Biochemical and Biophysical Research Communications 2016; 473(3): 726-32.
  165. Ji J., Tong X., Huang X. et al. Sphere-shaped nanoydroxyapatite/chitosan/gelatin 3D porous scaffolds increase proliferation and osteogenic differentiation of human induced pluripotent stem cells from gingival fibroblasts. Biomed. Mater. 2015; 10(4): 045005.
  166. Zou L., Luo Y., Chen M. et al. A simple method for deriving functional MSCs and applied for osteogenesis in 3d scaffolds. Sci. Rep. 2013; 3: 2243.
  167. Okita K., Matsumura Y., Sato Y. et al. A more efficient method to generate integration-free human iPS cells. Nat. Methods 2011; 8: 409-12.
  168. Lian Q., Zhang Y., Zhang J. et al. Functional mesenchymal stem cells derived from human induced pluripotent stem cells attenuate limb ischemia in mice. Circulation 2010; 121: 1113-23.
  169. Srijaya T., Pradeep P., Zain R. et al. The promise of human induced pluripotent stem cells in dental research. Stem Cells Int. 2012; 2012: 1-10.

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