Genes & CellsGenes & CellsГены и КлеткиGenes and Cells2313-18292500-2562Human Stem Cells Institute12037110.23868/gc120371ArticlesСтатьиReview ArticleFeatures of multipotent mesenchymal stromal cells derived from various intraoral sourcesОСОБЕННОСТИ МУЛЬТИПОТЕНТНЫХ МЕЗЕНХИМАЛЬНЫХ СТРОМАЛЬНЫХ КЛЕТОК, ПОЛУЧЕННЫХ ИЗ РАЗЛИЧНЫХ ИНТРАОРАЛЬНЫХ ИСТОЧНИКОВBozoI. YБозоИ. ЯZorinV. LЗоринВ. ЛEreminI. IЕреминИ. ИDeevR. VДеевР. ВDrobyshevA. YДробышевА. ЮKorsakovI. NКорсаковИ. НPulinAA. AПулинА. АHuman Stem Cells InstituteИнститут стволовых клеток человекаA.I. Burnasyan Federal Medical Biophysical Center, Moscow, RussiaФедеральный медицинский биофизический центр им. А.И. Бурназяна.A.I. Evdokimov Moscow State University of Medicine and DentistryИнститут стволовых клеток человекаHuman Stem Cells InstituteФедеральный медицинский биофизический центр им. А.И. БурназянаA.I. Burnasyan Federal Medical Biophysical CenterФедеральный медицинский биофизический центр им. А.И. БурназянаA.I. Burnasyan Federal Medical Biophysical CenterИнститут стволовых клеток человекаHuman Stem Cells InstituteКазанский (Приволжский) федеральный университетKazan (Volga region) State UniversityМосковский медико-стоматологический университет им. А.И. ЕвдокимоваA.I. Evdokimov Moscow State University of Medicine and DentistryФедеральный медицинский биофизический центр им. А.И. БурназянаA.I. Burnasyan Federal Medical Biophysical Center1512201494VOL 9, NO4 (2014)ТОМ 9, №4 (2014)344205012023Copyright ©; 2014, Eco-VectorCopyright ©; 2014, Эко-Вектор2014Eco-VectorЭко-Векторhttps://genescells.ru/2313-1829/article/view/120371

Multipotent mesenchymal stromal cells (MMSC) derived from various intraoral sources attracts attention of an increasing number of researchers due to availability and some features making them different from MMSC of bone marrow or adipose tissue. The review describes the main intraoral sources, characterizes their anatomical, topographical and histological peculiarities which may influence on MMSC morphofunctional profile. In comparative aspect we systematized the principal data concerning properties of MMSC derived from gingiva, buccal mucosa; periodontal ligament, dental pulp, apical papilla, jaw periosteum. It is not possible to compare MMSC of various intraoral sources under some parameters because of absence appropriate experimental findings. Some additional difficulties are caused by contradictions in published materials that are discussed in the review as well.

Мультипотентные мезенхимальные стромальные клетки (ММСК) из различных интраоральных источников привлекают внимание все большего числа исследователей в виду доступности получения и некоторых особенностей, отличающих их от ММСК костного мозга и жировой ткани. В обзоре представлены основные интраоральные источники, охарактеризованы их анатомо-топографические и гистологические особенности, способные оказать влияние на морфофункциональный профиль ММСК. В сравнительном аспекте систематизированы основные сведения о свойствах ММСК слизистой десны, щеки; периодонтальной связки, пульпы зуба, апикального сосочка, надкостницы челюстей. По ряду параметров ММСК из различных интраораль-ных источников пока сравнить невозможно в виду отсутствия экспериментальных данных. Некоторые дополнительные сложности для систематизации вносят противоречия в опубликованных материалах исследований, которые обсуждены в обзоре.

MMSCoral mucosagingivaperiodontal ligamentdental pulpapical papillaperiosteumММСКслизистая оболочка полости ртадеснапериодонтальная связкапульпа зубаапикальный сосочекнадкостницаBianco P. «Mesenchymal» stem cells. Annu. Rev. Cell Dev. Biol. 2014; 30: 677-704.Sharma R.R., Pollock K., Hubel A. et al. Mesenchymal stem or stromal cells: a review of clinical applications and manufacturing practices. Transfusion 2014; 54(5): 1418-37.Galderisi U., Giordano A. The gap between the physiological and therapeutic roles of mesenchymal stem cells. Med. Res. Rev. 2014; 34(5): 1100-26.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.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.Dominici M, Le Blanc K, Mueller I. et al. Minimal criteria for defining multipotent mesenchymal stromal cells. The International Society for Cellular Therapy position statement. Cytotherapy 2006; 8(4): 315-7.FACT-JACIE International Standards for Cellular Therapy Product Collection, Processing, and Administration [Foundation for the Accreditation of Cellular Therapy (FACT-Joint Accreditation Committee of International Society of Cellular Therapy (ISCT) and European Group of Blood and Marrow transplantation (EBMT) (JACIE) 5th ed. 2012. www.factwebsite.org.Friedenstein A.J., Deriglasova U.F., Kulagina N.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.Sousa B.R., Parreira R.C., Fonseca E.A. et al. Human adult stem cells from diverse origins: an overview from multiparametric immunophenotyping to clinical applications. Cytometry A. 2014; 85(1): 43-77.Riekstina U., Muceniece R., Cakstina I. et al. Characterization of human skin-derived mesenchymal stem cell proliferation rate in different growth conditions. Cytotechnology 2008; 58(3): 153-62.Hegyi B., Sagi B., Kovacs J. et al. Identical, similar or different? Learning about immunomodulatory function of mesenchymal stem cells isolated from various mouse tissues: bone marrow, spleen, thymus and aorta wall. Int. Immunol. 2010; 22(7): 551-9.Pan Q., Fouraschen S.M., Kaya F.S. et al. Mobilization of hepatic mesenchymal stem cells from human liver grafts. Liver Transpl. 2011; 17(5):596-609.da Silva Meirelles L., Chagastelles P.C., Nardi N.B. Mesenchymal stem cells reside in virtually all post-natal organs and tissues. J. Cell Sci. 2006; 119: 2204-13.Maximow A.A. 1927. Bindegewebe und blutbildende Gewebe. Handb. d. mikr. Anat. herausg. von W. v. Mollendorff. Berlin: Springer. 2: 232-84.Бозо И.Я., Деев Р.В., Пинаев Г.П. «Фибробласт» - специализированная клетка или функциональное состояние клеток мезенхимного происхождения? Цитология 2010. 52 (2): 99-109.Fournier B.P., Larjava H., Hakkinen L. Gingiva as a source of stem cells with therapeutic potential. Stem Cells Dev. 2013; 22(24): 3157-77.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.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.Руководство по гистологии. Р.К. Данилов, редактор. Т2. Санкт-Петербург: «Специальная литература»; 2011.Быков В.Л. Гистология и эмбриология органов полости рта человека. Санкт-Петербург: «Специальная литература»; 1998.Chatterjee K. Essentials of oral histology. Jaypee Brothers Publishers; 2006.Avery J.K. Oral Development and Histology.Thieme; 2011.Nam H., Kim J., Kim J.-W. et al. Establishment of Hertwig's epithelial root sheath/epithelial rests of Malassez cell line from human periodontium. Mol. Cells. 2014; 37(7): 562-7.Singh I. Textbook of human histology: with colour atlas & practical guide. Jaypee Brothers Publishers; 2010.Ирьянов Ю.М., Горбач Е.Н. Строение надкостницы большеберцовой кости взрослой собаки. Гений ортопедии 2008; 1: 81-4.Andreadis D., Bakopoulou A., Leyhausen G. et al. Minor salivary glands of the lips: a novel, easily accessible source of potential stem/ progenitor cells. Clin. Oral Investig. 2014; 18(3): 847-56.Zhang Q., Shi S., Liu Y. et al. 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(12): 7787-98.Stephens P., Genever P. Non-epithelial oral mucosal progenitor cell populations. Oral Dis. 2007; 13(1): 1-10.Зорин В.Л., Зорина А.И., Еремин И.И. и др. Сравнительный анализ остеогенного потенциала мультипотентных мезенхимальных стромальных клеток слизистой оболочки полости рта и костного мозга. Гены и клетки 2014; IX(1): 50-7.Fournier B.P., Ferre F.C., Couty L. et al. Multipotent progenitor cells in gingival connective tissue. Tissue Eng. Part A. 2010; 16(9): 2891-9.Wang F., Yu M., Yan X. et al. Gingiva-derived mesenchymal stem cell-mediated therapeutic approach for bone tissue regeneration. Stem Cells Dev. 2011; 20(12): 2093-102.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.Gao Y., Zhao G., Li D. et al. Isolation and multiple differentiation potential assessment of human gingival mesenchymal stem cells. Int. J. Mol. Sci. 2014; 15(11): 20982-96.Mitrano T.I., Grob M.S., Carrion F. et al. Culture and characterization of mesenchymal stem cells from human gingival tissue. J. Periodontol. 2010; 81(6): 917-25.Marynka-Kalmani K., Treves S., Yafee M. et al. The lamina propria of adult human oral mucosa harbors a novel stem cell population. Stem Cell. 2010; 28(5): 984-95.Ganz J., Arie I., Ben-Zur T. et al. Astrocyte-like cells derived from human oral mucosa stem cells provide neuroprotection in vitro and in vivo. Stem Cells Transl. Med. 2014; 3(3): 375-86.Bedada F.B., Technau A., Ebelt H. et al. Activation of myogenic differentiation pathways in adult bone marrow-derived stem cells. Mol. Cell. Biol. 2005; 25(21):9509-19.Gang E.J., Bosnakovski D., Simsek T. et al. Pax3 activation promotes the differentiation of mesenchymal stem cells toward the myogenic lineage. Exp.Cell Res.2008; 314(8):1721-33.Beier J.P., Bitto F.F., Lange C. et al. Myogenic differentiation of mesenchymal stem cells co-cultured with primary myoblasts. Cell Biol. Int. 2011; 35(4): 397-406.Dave S. Mesenchymal stem cells derived in vitro transdifferentiated insulin-producing cells: A new approach to treat type 1 diabetes. Adv. Biomed. Res. 2014; 3: 266.Зорин В.Л., Еремин И.И., Рыбко В.А. и др. Слизистая оболочка полости рта - новый источник получения миобластов. Гены и клетки 2014; IX(3A): 76-84.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.Mankani M.H., Kuznetsov S.A., Fowler B. et al. In vivo bone formation by human bone marrow stromal cells: effect of carrier particle size and shape. Biotechnol. Bioeng. 2001; 72(1):96-107.Xu X., Chen C., Akiyama K. et al. Gingivae Contain Neural-crest- and Mesoderm-derived Mesenchymal Stem Cells. J. Dent. Res. 2013; 92(9): 825-32.Zhang Q.Z., Su W.R., Shi S.H. et al. Human gingiva-derived mesenchymal stem cells elicit polarization of m2 macrophages and enhance cutaneous wound healing. Stem Cells 2010; 28(10): 1856-68.Zhang Q.Z., Nguyen A.L., Yu W.H. et al. Human oral mucosa and gingiva: a unique reservoir for mesenchymal stem cells. J. Dent. Res. 2012; 91(11): 1011-8.Davies L.C., Locke M., Webb R.D. 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.Marynka-Kalmani K., Treves S., Yafee M. et al. The lamina propria of adult human oral mucosa harbors a novel stem cell population. Stem Cells 2010; 28(5): 984-95.Treves-Manusevitz S., Hoz L., Rachima H. et al. Stem cells of the lamina propria of human oral mucosa and gingiva develop into mineralized tissues in vivo. J. Clin. Periodontol. 2013; 40(1): 73-81.Davies L.C., Lonnies H., Locke M. et al. Oral mucosal progenitor cells are potently immunosuppressive in a dose-independent manner. Stem Cells Dev. 2012; 21(9):1478-87.Gould T.R. Ultrastructural characteristics of progenitor cell populations in the periodontal ligament. J. Dent. Res. 1983; 62: 873-6.McCulloch C.A. Progenitor cell populations in the periodontal ligament of mice. Anat. Rec. 1985; 211: 258-62.Song M., Kim H., Choi Y. et al. Skeletal myogenic differentiation of human periodontal ligament stromal cells isolated from orthodontically extracted premolars. Korean J. Orthod. 2012; 42(5): 249-54.Huang C.Y., Pelaez D., Dominguez-Bendala J. et al. Plasticity of stem cells derived from adult periodontal ligament. Regen. Med. 2009; 4(6): 809-21.Covas D.T., Panepucci R.A., Fontes A.M. et al. Multipotent mesenchymal stromal cells obtained from diverse human tissues share functional properties and gene-expression profile with CD146 + perivascular cells and fibroblasts. Exp. Hematol. 2008; 36 (5): 642-54.Menicanin D., Mrozik K.M., Wada N. et al. Periodontal-ligament-derived stem cells exhibit the capacity for long-term survival, self-renewal, and regeneration of multiple tissue types in vivo. Stem Cells Dev. 2014; 23(9): 1001-11.Song D.S., Park J.C., Jung I.H. et al. Enhanced adipogenic differentiation and reduced collagen synthesis induced by human periodontal ligament stem cells might underlie the negative effect of recombinant human bone morphogenetic protein-2 on periodontal regeneration. J. Periodontal. Res. 2011; 46(2): 193-203.Wang L., Shen H., Zheng W. et al. Characterization of stem cells from alveolar periodontal ligament. Tissue Eng. Part A. 2011; 17(7-8): 1015-26.Silverio K.G., Rodrigues T.L., Coletta R.D. et al. Mesenchymal stem cell properties of periodontal ligament cells from deciduous and permanent teeth. J. Periodontol. 2010; 81(8): 1207-15.Song J.S., Kim S.O., Kim S.H. et al. In vitro and in vivo characteristics of stem cells derived from the periodontal ligament of human deciduous and permanent teeth. Tissue Eng. Part A. 2012; 18(19-20): 2040-51.Gronthos S., Mankani M., Brahim J. et al. Postnatal human dental pulp stem cells tDPSCs) in vitro and in vivo. PNAS USA 2000; 97: 13625-30.Akpinar G., Kasap M., Aksoy A. et al. Phenotypic and proteomic characteristics of human dental pulp derived mesenchymal stem cells from a natal, an exfoliated deciduous, and an impacted third molar tooth. Stem Cells Int. 2014; 2014: 457059.Lee J.H., Um S., Song I.S. et al. Neurogenic differentiation of human dental stem cells in vitro. J. Korean Assoc. Oral Maxillofac. Surg. 2014; 40(4):173-80.Zhang W., Walboomers X.F., Shi S. et al. Multilineage differentiation potential of stem cells derived from human dental pulp after cryopreservation. Tissue Eng. 2006; 12t10):2813-23.Pisciotta A., Riccio M., Carnevale G. et al. Human serum promotes osteogenic differentiation of human dental pulp stem cells in vitro and in vivo. PLoS One 2012; 7(11): e50542.Zhang W., Walboomers X.F., Van Kuppevelt T.H. et al. In vivo evaluation of human dental pulp stem cells differentiated towards multiple lineages. J. Tissue Eng. Regen. Med. 2008; 2(2-3): 117-25.Dimitrova-Nakov S., Baudry A., Harichane Y. et al. Pulp stem cells: implication in reparative dentin formation. J. Endod. 2014; 40(4 Suppl): S13-8.Sonoyama W., Liu Y., Fang D. et al. Mesenchymal stem cell-mediated functional tooth regeneration in swine. PLoS One 2006; 1: e79.Ding G., Wang W., Liu Y. et al. Effect of cryopreservation on biological and immunological properties of stem cells from apical papilla. J. Cell Physiol. 2010; 223(2): 415-22.Volponi A.A., Sharpe P.T. The tooth - a treasure chest of stem cells.Br. Dent. J. 2013; 215(7): 353-8.Huang G.T., Gronthos S., Shi S. Mesenchymal stem cells derived from dental tissues vs. those from other sources: their biology and role in regenerative medicine. J. Dent. Res. 2009; 88(9): 792-806.Sonoyama W., Liu Y., Yamaza T. et al. Characterization of the apical papilla and its residing stem cells from human immature permanent teeth: a pilot study. J. Endod. 2008; 34(2): 166-71.Фриденштейн А.Я., Лалыкина К.С. Индукция костной ткани и остеогенные клетки предшественники. М.: Медицина, 1973.Alexander D., Schafer F., Olbrich M. et al. MSCA-1/TNAP Selection of human jaw periosteal cells improves their mineralization capacity. Cell Physiol. Biochem. 2010; 26: 1073-80.Caballero M., Pappa A.K., Roden K.S. et al. Osteoinduction of umbilical cord and palate periosteum-derived mesenchymal stem cells on poly(lactic-co-glycolic) acid nanomicrofibers. Ann. Plast. Surg. 2014; 72(6): S176-83.Грудянов А.И., Зорин В.Л., Переверзев Р.В. и др. Эффективность использования аутофибробластов при хирургическом лечении пародонтита. Клеточная трансплантология и тканевая инженерия 2013; VIII (3): 72-7.Eremin I., Zorin V., Deev R. et al. Autologous gingival multipotent mesenchymal stromal cells and adipose-derived regenerative cells for maxillofacial reconstruction: pilot study. J. Tissue Eng. Regen. Med. 2014; 8 (Suppl. 1): 439.Tomar G.B., Srivastava R.K., Gupta N. et al. Human gingiva-derived mesenchymal stem cells are superior to bone marrow-derived mesenchymal stem cells for cell therapy in regenerative medicine. Biochem. Biophys. Res. Commun. 2010; 393(3): 377-83.