Genes & Cells

Гены и Клетки

Genes and Cells

2313-18292500-2562

Human Stem Cells Institute

120511

10.23868/gc120511

Articles

Статьи

Research Article

Expression of myogenesis genes by gingiva derived cells

Экспрессия генов миогенеза клетками слизистой оболочки десны

Samchuk

D. P

Самчук

Д. П

Lukyanova

E. N

Лукьянова

Е. Н

Eremin

I. I

Еремин

И. И

Zorin

V. L

Зорин

В. Л

Zorina

A. I

Зорина

А. И

Grinakovskaya

O. S

Гринаковская

О. С

Korsakov

I. N

Корсаков

И. Н

Deev

R. V

Деев

Р. В

Gilmutdinova

I. R

Гильмутдинова

И. Р

Lazareva

N. L

Лазарева

Н. Л

Eremin

P. S

Еремин

П. С

Petrikina

A. P

Петрикина

А. П

Gomzyakov

A. E

Гомзяков

А. Е

Timashkov

D. A

Тимашков

Д. А

Vit’ko

N. K

Витько

Н. К

Kotenko

K. V

Котенко

К. В

Kopnin

P. B

Копнин

П. Б

Pulin

A. A

Пулин

А. А

andreypulin@gmail.com

Central Clinical Hospital with Outpatient Health CenterЦентральная клиническая больница с поликлиникой

Human Stem Cells InstituteИнститут стволовых клеток человека»

Kazan (Volga region) Federal UniversityИнститут стволовых клеток человека»

Казанский (Приволжский) федеральный университетCentral Clinical Hospital with Outpatient Health Center

Центральная клиническая больница с поликлиникойCentral Medical Authority of the Business Administration for the President of the Russian Federation

Главное медицинское управление Управления делами Президента РФN.N. Blokhin Cancer Research Center

Российский онкологический научный центр им. Н.Н. БлохинаCentral Clinical Hospital with Outpatient Health Center

Центральная клиническая больница с поликлиникой

15122015

104

VOL 10, NO4 (2015)

ТОМ 10, №4 (2015)

687705012023

2015

Eco-Vector

Эко-Вектор

https://genescells.ru/2313-1829/article/view/120511

The ability of gingiva derived mesenchymal stromal cells (MSCs) to myogenic differentiation and the possibility of their expansion in vitro revealed in our previous work, open up prospects for their use in regenerative medicine for the correction of muscle pathology. Data on changes in the expression of myogenic regulatory factors in gingiva derived MSCs can serve as confirmation of the possibility of differentiation of these cells into the myogenic direction The study was conducted on cultures of gingiva derived MSCs and skin fibroblasts. When comparing gene expression profiles of gingiva derived MSCs and skin fibroblasts significant changes have been registered for 153 genes. Of these, we selected 19 significant differentially expressed genes, for which main signal pathways were analyzed. Evidences of significant activation / inactivation of signaling pathways and key genes that have been identified for the population of human satellite cells were obtained during analysis of the genome transcriptome profiles of gingiva derived MSCs This applies to such signaling pathways as the p38 MAPK, NOTCH and other groups responsible for the proliferation and differentiation in myogenic direction, the processes of self-renewal or self-maintenance in the population of satellite cells. At the same time full match in the patterns of gene expression between the stable population of gingiva derived MSCs and human satellite cells undergoing myogenic differentiation as well as cells derived from atypical sources and differentiated in the myogenic direction was not observed The data of our experiment suggests that the gingiva derived MSCs are distinct from satellite cells and could be considered as population with plateaued development, possessing the ability to differentiate into myogenic direction due to non-canonical expression pattern of myogenic regulatory factors

Выявленная в наших предыдущих работах способность мезенхимальных стромальных клеток (МСК) слизистой оболочки полости рта (десны) к миогенной дифференцировке, а также возможность их экспансии in vitro, открывают перспективы для применения этих клеток в регенеративной медицине с целью коррекции мышечной патологии Подтверждением возможности дифференцировки МСК десны в миогенном направлении могут служить данные об изменениях экспрессии регуляторных факторов миогенеза в этих клетках Исследование проведено на культурах фибробластов кожи и МСК десны При сравнении профилей экспрессии генов МСК десны и фибробластов кожи значимые изменения зарегистрированы для 153 генов. Из них нами отобраны 19 значимых дифференциально экспрессированных генов, для которых были проанализированы основные сигнальные пути При анализе транскриптомных профилей генома МСК десны выявлены данные, свидетельствующие о значимой активации/инактивации сигнальных путей и основных генов, которые были идентифицированы для популяции сателлитных клеток человека. Это относится к таким сигнальным путям как p38 MAPK, NOTCH и др., отвечающим за пролиферацию и дифференцировку в миогенном направлении, процессы самообновления или самоподдержания в популяции сателлитных клеток В то же время полного совпадения в паттернах экспрессии генов между стабильной популяцией МСК десны и сателлитных клеток человека, проходящих миогенную дифференцировку, а также дифференцированных в миогенном направлении клеток, полученных из нетипичных источников, отмечено не было. Данные настоящего эксперимента позволяют говорить о МСК десны как об отличной от миосателлитных клеток популяции, обладающей способностью дифференцироваться в миогенном направлении на фоне неканонического паттерна экспрессии миогенных регуляторных факторов

CustomArray 12Kgingivaregenerative medicinegingiva derived mesenchymal stromal cellsmyogenic differentiationmicroarrayCustomArray 12Kgenes expression profile

деснарегенеративная медицинамезенхимальные стромальные клетки деснымиогенная дифференцировкамикрочипыпрофиль экспрессии генов

Meadows E., Cho J.-H., Flynn J.M., Klein W.H. Myogenin regulates a distinct genetic program in adult muscle stem cells. Dev. Biol. 2008; 322(2): 406-14.

Olson E.N., Brennan T.J., Chakraborty T. et al. Molecular control of myogenesis: antagonism between growth and differentiation. Mol. Cell Biochem. 1991; 104(1-2): 7-13.

Mohun T. Muscle differentiation. Curr. Opin. Cell Biol. 1992; 4(6): 923-8

Andrés V., Walsh K. Myogenin expression, cell cycle withdrawal, and phenotypic differentiation are temporally separable events that precede cell fusion upon myogenesis. J. Cell Biol. 1996; 132(4): 657-66

Moran J. L., Li Y., Hill A.A. et al. Gene expression changes during mouse skeletal myoblast differentiation revealed by transcriptional profiling. Physiol. Genomics 2002; 10(2): 103-11.

Janot M., Audfray A., Loriol C. et al. Glycogenome expression dynamics during mouse C2C12 myoblast differentiation suggests a sequential reorganization of membrane glycoconjugates. BMC Genomics 2009;10: 483. doi: 10. 1186/1471-2164-10-483.

Rajan S., Chu Pham Dang H., Djambazian H. et al. Analysis of early C2C12 myogenesis identifies stably and differentially expressed transcriptional regulators whose knock-down inhibits myoblast differentiation. Physiol. Genomics 2012; 44(2): 183-97.

Studitsky A.N. Free auto- and homografts of muscle tissue in experiments on animals. Ann. N.-Y. Acad. Sci. 1964; 120: 789-801.

Mauro A. Satellite cell of skeletal muscle fibers J Biophys Biochem. Cytol. 1961; 9: 493-5.

10.

Ehrhardt J., Morgan J. Regenerative capacity of skeletal muscle. Curr. Opin. Neurol. 2005; 18t5): 548-53.

11.

Sambasivan R., Yao R., Kissenpfennig A. et al. Pax7-expressing satellite cells are indispensable for adult skeletal muscle regeneration Dev. 2011; 138(17): 3647-56.

12.

Lepper C., Partridge T.A., Fan C.-M. An absolute requirement for Pax7-positive satellite cells in acute injury-induced skeletal muscle regeneration. Dev. 2011; 138(17): 3639-46.

13.

Hawke T.J., Garry D.J. Myogenic satellite cells: physiology to molecular biology. J. Appl. Physiol. 2001; 91(2): 534-51.

14.

Charville G.W., Cheung T.H., Yoo B. et al. Ex Vivo Expansion and In Vivo Self-Renewal of Human Muscle Stem Cells. Stem cell reports 2015; 5(4): 621-32.

15.

Tedesco F.S., Dellavalle A., Diaz-Manera J. et al. Repairing skeletal muscle: regenerative potential of skeletal muscle stem cells. J. Clin. Invest. 2010; 120(1): 11-9.

16.

Di Rocco G., Iachininoto M.G., Tritarelli A. et al. Myogenic potential of adipose-tissue-derived cells. J. Cell Sci. 2006; 119(14): 2945-52

17.

Liu G., Sun X., Bian J. et al. Correction of diabetic erectile dysfunction with adipose derived stem cells modified with the vascular endothelial growth factor gene in a rodent diabetic model PLoS One 2013; 8(8): e72790.

18.

Xynos A., Corbella P., Belmonte N. et al. Bone marrow-derived hematopoietic cells undergo myogenic differentiation following a Pax-7 independent pathway. Stem Cells 2010; 28(5): 965-73.

19.

Catacchio I., Berardi S., Reale A. et al. Evidence for Bone Marrow Adult Stem Cell Plasticity: Properties, Molecular Mechanisms, Negative Aspects, and Clinical Applications of Hematopoietic and Mesenchymal Stem Cells Transdifferentiation. Stem Cells Int. 2013; 2013: 1-11. doi: 10. 1155/2013/589139.

20.

Ferrari G., Cusella-De Angelis G., Coletta M. et al. Muscle regeneration by bone marrow-derived myogenic progenitors Science 1998; 279(5356): 1528-30.

21.

Dezawa M., Ishikawa H., Itokazu Y. et al. Bone marrow stromal cells generate muscle cells and repair muscle degeneration Science 2005; 309(5732): 314-7.

22.

Зорин В.Л., Зорина А.И., Пулин А.А. и др. Перспективы использования клеток, обладающих миогенным потенциалом, в лечении заболеваний скелетных мышц: обзор исследований. Популяции стволовых клеток мышечного и немышечного происхождения. Патологическая физиология и экспериментальная терапия 2015; 59(3): 106-17.

23.

Зорин В.Л., Зорина А.И., Пулин А.А. и др. Перспективы использования клеток, обладающих миогенным потенциалом, в лечении заболеваний скелетных мышц: обзор исследований. Сателлитные клетки Патологическая физиология и экспериментальная терапия. 2015; 59(2): 88-98.

24.

Grogan B.F., Hsu J.R. Volumetric muscle loss J Am Acad Orthop. Surg. 2011; 19 Suppl 1: S35-7.

25.

Rizzi R., Bearzi C., Mauretti A. et al. Tissue engineering for skeletal muscle regeneration. Muscle, Ligaments, Tendons J. 2012; 2(3): 230-4.

26.

Luz M.A.M., Marques M.J., Santo Neto H. Impaired regeneration of dystrophin-deficient muscle fibers is caused by exhaustion of myogenic cells. Brazilian J. Med. Biol. Res. 2002; 35(6): 691-5.

27.

Зорин В.Л., Еремин И.И., Рыбко В.А. и др. Слизистая оболочка полости рта - новый источник для получения миобластов Гены и Клетки 2014; 9(3): 76-84.

28.

Gilbert S.F. Developmental Biology. 10th ed. Sunderland, MA: Sinauer Associates, Inc.; 2013.

29.

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; 9(1): 50-7.

30.

Robinson M.D., McCarthy D.J., Smyth G.K. edge R: a Bioconductor package for differential expression analysis of digital gene expression data. Bioinformatics 2010; 26(1): 139-40.

31.

Gene Ontology Consortium. Gene Ontology Consortium: going forward. Nucleic Acids Res. 2015; 43 (Database issue): D1049-56

32.

UniProt Consortium. UniProt: a hub for protein information. Nucleic Acids Res. 2015; 43 (Database issue): D204-12.

33.

Kamburov A., Stelzl U., Lehrach H., Herwig R. The ConsensusPathDB interaction database: 2013 update. Nucleic Acids Res. 2013; 41 (Database issue): D793-800.

34.

Blais A. Myogenesis in the genomics era J Mol Biol 2015; 427(11): 2023-38.

35.

Shen X., Collier J.M., Hlaing M. et al. Genome-wide examination of myoblast cell cycle withdrawal during differentiation Dev. Dyn. 2003; 226(1): 128-38.

36.

Dilworth F.J., Blais A Epigenetic regulation of satellite cell activation during muscle regeneration. Stem Cell Res. Ther. 2011; 2(2): 18.

37.

Berkes C.A., Tapscott S.J. MyoD and the transcriptional control of myogenesis. Semin Cell Dev. Biol. 2005; 16(4-5): 585-95

38.

Liu Y., Chu A., Chakroun I. et al. Cooperation between myogenic regulatory factors and SIX family transcription factors is important for myoblast differentiation. Nucleic Acids Res. 2010; 38(20): 6857-71.

39.

Edmondson D.G., Cheng T.C., Cserjesi P. et al. Analysis of the myogenin promoter reveals an indirect pathway for positive autoregulation mediated by the muscle-specific enhancer factor MEF-2. Mol. Cell Biol. 1992; 12(9): 3665-77.

40.

Armand A.-S., Bourajjaj M., Martinez-Martfnez S., et al. Cooperative synergy between NFAT and MyoD regulates myogenin expression and myogenesis. J. Biol. Chem. 2008; 283(43): 29004-10.

41.

Yang Z.J.P., Broz D.K., Noderer W.L. et al. p53 suppresses muscle differentiation at the myogenin step in response to genotoxic stress. Cell Death Differ. 2015;22(4): 560-73.

42.

Liu L., Cheung T.H., Charville G.W. et al. Chromatin modifications as determinants of muscle stem cell quiescence and chronological aging. Cell Rep. 2013; 4(1): 189-204.

43.

Bharathy N., Ling B.M.T., Taneja R. Epigenetic regulation of skeletal muscle development and differentiation Subcell Biochem 2013; 61: 139-50.

44.

Brand-Saberi B. Genetic and epigenetic control of skeletal muscle development. Ann. Anat. 2005; 187(3): 199-207.

45.

Shenoy A., Blelloch R.H. Regulation of microRNA function in somatic stem cell proliferation and differentiation. Nat. Rev. Mol. Cell Biol. 2014; 15(9): 565-76.

46.

Buckingham M., Rigby P.W.J. Gene regulatory networks and transcriptional mechanisms that control myogenesis. Dev. Cell 2014; 28(3): 225-38.

47.

Bentzinger C.F., Wang Y.X., Rudnicki M.A. Building muscle: molecular regulation of myogenesis Cold Spring Harb Perspect Biol 2012; 4(2). doi: 10. 1101/cshperspect. a008342.

48.

Cao Y., Kumar R.M., Penn B.H. et al. Global and gene-specific analyses show distinct roles for Myod and Myog at a common set of promoters. EMBO J. 2006; 25(3): 502-11.

49.

Kirillova I., Gussoni E., Goldhamer D.J., Yablonka-Reuveni Z. Myogenic reprogramming of retina-derived cells following their spontaneous fusion with myotubes. Dev. Biol. 2007; 311(2): 449-63

50.

Asakura A. Myogenic specification of side population cells in skeletal muscle. J. Cell. Biol. 2002; 159(1): 123-34.

51.

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.

52.

Gang E.J., Darabi R., Bosnakovski D. et a.l Engraftment of mesenchymal stem cells into dystrophin-deficient mice is not accompanied by functional recovery. Exp. Cell. Res. 2009; 315(15): 2624-36.

53.

Braun T., Gautel M. Transcriptional mechanisms regulating skeletal muscle differentiation, growth and homeostasis Nat Rev Mol. Cell. Biol. 2011; 12(6): 349-61.

54.

Johanson M., Meents H., Ragge K. et al. Transcriptional activation of the myogenin gene by MEF2-mediated recruitment of myf5 is inhibited by adenovirus E1A protein. Biochem. Biophys. Res. Commun. 1999; 265(1): 222-32.

55.

Valdez M.R., Richardson J.A., Klein W.H., Olson E.N. Failure of Myf5 to support myogenic differentiation without myogenin, MyoD, and MRF4. Dev. Biol. 2000; 219(2): 287-98.

56.

Myer A., Wagner D.S., Vivian J.L. et al. Wild-type myoblasts rescue the ability of myogenin-null myoblasts to fuse in vivo. Dev. Biol. 1997; 185(2): 127-38.

57.

Ohkawa Y., Marfella C.G.A., Imbalzano A.N. Skeletal muscle specification by myogenin and Mef2D via the SWI/SNF ATPase Brg1. EMBO J. 2006; 25(3): 490-501.

58.

Salminen A., Braun T., Buchberger A. et al. Transcription of the muscle regulatory gene Myf4 is regulated by serum components, peptide growth factors and signaling pathways involving G proteins J Cell. Biol. 1991; 115(4): 905-17.

59.

Tajbakhsh S., Vivarelli E., Cusella-De Angelis G. et al. A population of myogenic cells derived from the mouse neural tube Neuron 1994; 13(4): 813-21.

60.

Satyaraj E., Storb U. Mef2 proteins, required for muscle differentiation, bind an essential site in the Ig lambda enhancer. J. Immunol. 1998; 161(9): 4795-802.

61.

Bitto F.F., Klumpp D., Lange C. et al. Myogenic differentiation of mesenchymal stem cells in a newly developed neurotised AV-loop model. Biomed. Res. Int. 2013; 2013: 935046.

62.

Morisaki T., Sermsuvitayawong K., Byun S.H. et al. Mouse Mef2b gene: unique member of MEF2 gene family. J. Biochem. 1997; 122(5): 939-46.

63.

Konig S., Hinard V., Arnaudeau S. et al. Membrane hyperpolarization triggers myogenin and myocyte enhancer factor-2 expression during human myoblast differentiation J Biol Chem 2004; 279(27): 28187-96.

64.

Molkentin J.D., Firulli A.B., Black B.L. et al. MEF2B is a potent transactivator expressed in early myogenic lineages Mol Cell Biol 1996; 16(7): 3814-24.

65.

Han A., He J., Wu Y. et al. Mechanism of recruitment of class II histone deacetylases by myocyte enhancer factor-2. J. Mol Biol. 2005; 345(1): 91-102.

66.

Wu M.Y., Ramel M.-C., Howell M., Hill C.S. SNW1 is a critical regulator of spatial BMP activity, neural plate border formation, and neural crest specification in vertebrate embryos. PLoS Biol. 2011; 9(2): e1000593.

67.

Ngo M.A., Müller A., Li Y. et al. Human mesenchymal stem cells express a myofibroblastic phenotype in vitro: comparison to human cardiac myofibroblasts. Mol. Cell. Biochem. 2014; 392(1-2): 187-204.

68.

Swailes N.T., Colegrave M., Knight P.J., Peckham M. Nonmuscle myosins 2A and 2B drive changes in cell morphology that occur as myoblasts align and fuse. J. Cell. Sci. 2006; 119(17): 3561-70.

69.

Lo C.-M., Buxton D.B., Chua G.C.H. et al. Nonmuscle myosin IIb is involved in the guidance of fibroblast migration. Mol. Biol. Cell. 2004; 15(3): 982-9.

70.

Duan R., Gallagher P.J. Dependence of myoblast fusion on a cortical actin wall and nonmuscle myosin IIA. Dev. Biol. 2009; 325(2): 374-85

71.

De Arcangelis V., Coletti D., Conti M. et al. IGF-I-induced differentiation of L6 myogenic cells requires the activity of cAMP-phosphodiesterase. Mol. Biol. Cell. 2003; 14(4): 1392-404.

72.

Philippou A., Maridaki M., Halapas A., Koutsilieris M. The role of the insulin-like growth factor 1 (IGF-1) in skeletal muscle physiology. In Vivo 2007; 21(1): 45-54.

73.

Lu J., McKinsey T.A., Zhang C.-L., Olson E.N. Regulation of Skeletal Myogenesis by Association of the MEF2 Transcription Factor with Class II Histone Deacetylases. Mol. Cell. 2000; 6(2): 233-44.

74.

Huang Y., Qiu R., Mai W. et al. Effects of insulin-like growth factor-1 on the properties of mesenchymal stem cells in vitro. J. Zhejiang Univ. Sci. B. 2012; 13(1): 20-8.

75.

Haider H.K., Jiang S., Idris N.M., Ashraf M. IGF-1-overexpressing mesenchymal stem cells accelerate bone marrow stem cell mobilization via paracrine activation of SDF-1alpha/CXCR4 signaling to promote myocardial repair. Circ. Res. 2008; 103(11): 1300-8.

76.

Самчук Д.П., Пулин А.А., Еремин И.И. и др. Сравнительный анализ секреторного профиля мезенхимальных стромальных клеток десны человека, дифференцированных в миогенном направлении. Гены и Клетки 2015; 10(3): 94-105.

77.

Sacco A., Doyonnas R., LaBarge M.A., et al. IGF-I increases bone marrow contribution to adult skeletal muscle and enhances the fusion of myelomonocytic precursors. J. Cell. Biol. 2005; 171(3): 483-92

78.

Evron T., Philipp M., Lu J. et al. Growth Arrest Specific 8 (Gas8) and G protein-coupled receptor kinase 2 (GRK2) cooperate in the control of Smoothened signaling. J. Biol. Chem. 2011; 286(31): 27676-86

79.

Zhang S.-T., Zhao R., Ma W.-X. et al. Nrf1 is time-dependently expressed and distributed in the distinct cell types after trauma to skeletal muscles in rats. Histol. Histopathol. 2013; 28(6): 725-35.

80.

Furuya N., Ikeda S.-I., Sato S. et al. PARK2/Parkin-mediated mitochondrial clearance contributes to proteasome activation during slow-twitch muscle atrophy via NFE2L1 nuclear translocation. Autophagy 2014; 10(4): 631-41.

81.

Latouche C., Jowett J.B.M., Carey A.L. et al. Effects of breaking up prolonged sitting on skeletal muscle gene expression. J. Appl. Physiol. 2013; 114(4): 453-60.

82.

Behan W.M.H., Longman C., Petty R.K.H. et al. Muscle fibrillin deficiency in Marfan's syndrome myopathy. J. Neurol. Neurosurg. Psychiatry. 2003; 74(5): 633-8.

83.

De Lisio M., Jensen T., Sukiennik R.A. et al. Substrate and strain alter the muscle-derived mesenchymal stem cell secretome to promote myogenesis. Stem Cell Res. Ther. 2014; 5(3): 74.

84.

Kopan R., Nye J. S., Weintraub H. The intracellular domain of mouse Notch: a constitutively activated repressor of myogenesis directed at the basic helix-loop-helix region of MyoD. Dev. 1994; 120(9): 2385-96

85.

Hirsinger E., Malapert P., Dubrulle J. et al. Notch signalling acts in postmitotic avian myogenic cells to control MyoD activation Dev. 2001; 128(1): 107-16.

86.

Wen F., Wong H.K., Tay C.Y. et al. Induction of myogenic differentiation of human mesenchymal stem cells cultured on Notch agonist (Jagged-1) modified biodegradable scaffold surface. ACS Appl. Mater. Interfaces 2014 ;6(3): 1652-61.

87.

Wen Y., Bi P., Liu W. et al. Constitutive Notch activation upregulates Pax7 and promotes the self-renewal of skeletal muscle satellite cells. Mol. Cell. Biol. 2012; 32(12): 2300-11.

88.

Lu J., McKinsey T.A., Nicol R.L., Olson E.N. Signal-dependent activation of the MEF2 transcription factor by dissociation from histone deacetylases. PNAS USA 2000; 97(8): 4070-5.

89.

Suzuki E., Guo K., Kolman M. et al. Serum induction of MEF2/ RSRF expression in vascular myocytes is mediated at the level of translation. Mol. Cell. Biol. 1995; 15(6): 3415-23.

90.

Cossu G. Unorthodox myogenesis: possible developmental significance and implications for tissue histogenesis and regeneration Histol. Histopathol. 1997; 12(3): 755-60.

91.

Jejurikar S.S., Marcelo C.L., Kuzon W.M. Skeletal muscle denervation increases satellite cell susceptibility to apoptosis. Plast. Reconstr. Surg. 2002; 110(1):160-8.