Comparative analysis of secretory profile of human mesenchymal stromal cells differentiated in myogenic direction

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Abstract

Up to this day there are lots of data accumulated about the role of cytokines in regulation of different tissues homeostasis independently of inflammation framework. Skeletal muscles produce a wide range of biologically active molecules both in a normal condition and after injuries of different etiologies. Moreover, cultures of cells isolated from muscle tissue show same properties. In this regard identification of cytokines profile secreted by cells with myogenic potential is of particular importance as it will help to choose optimal cell types and their sources for clinical application Our research group previously demonstrated the possibility of obtainment of myogenic cells from gingival mucosa derived multipotent mesenchymal stromal cells (MMSC) However, secretory profile of this myogenic cells is not thoroughly investigated to this day The study was conducted on cultures of skin fibroblasts, MMSc derived from the attached and alveolar parts of the gingival mucosa and gingival mucosa MMSc, differentiated in a myogenic direction cells were isolated from skin and gingival mucosa biopsy specimens of 15 healthy volunteers. ELISA assay was performed for evaluation of 48 proinflammatory and anti-inflammatory cytokines, chemokines and growth factors Our data demonstrates tendency of most investigated proteins secretion gradual increase in the following sequence: skin fibroblasts - attached gingival mucosa MMSC - alveolar gingival mucosa MMSC - differentiated myoblasts, including factors directly involved in myogenesis, skeletal muscle homeostasis and regeneration Thus, alveolar gingival mucosa MMSC both before and after induction of myogenic differentiation potentially could facilitate skeletal muscle regeneration Our results indicate that subpopulation of MMSC derived from alveolar gingival mucosa are perspective candidates for clinical usage in patients with skeletal muscle disorders

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About the authors

D. P Samchuk

Central Clinical Hospital with Outpatient Health Center Moscow, Russia

A. A Pulin

Email: andreypulin@gmail.com
Central Clinical Hospital with Outpatient Health Center Moscow, Russia

I. I Eremin

Central Clinical Hospital with Outpatient Health Center Moscow, Russia

I. R Gilmutdinova

Central Clinical Hospital with Outpatient Health Center Moscow, Russia

I. N Korsakov

Central Clinical Hospital with Outpatient Health Center Moscow, Russia

V. L Zorin

Central Clinical Hospital with Outpatient Health Center Human Stem Cells Institute Moscow, Russia

A. I Zorina

Human Stem Cells Institute Moscow, Russia

O. S Grinakovskaya

Central Clinical Hospital with Outpatient Health Center Moscow, Russia

N. L Lazareva

Central Clinical Hospital with Outpatient Health Center Moscow, Russia

P. S Eremin

Central Clinical Hospital with Outpatient Health Center Moscow, Russia

A. P Petrikina

Central Clinical Hospital with Outpatient Health Center Moscow, Russia

A. E Gomzyakov

Central Clinical Hospital with Outpatient Health Center Moscow, Russia

R. V Deev

Human Stem Cells Institute Kazan (Volga region) Federal University Moscow, Russia Kazan, Russia

D. A Timashkov

Central Clinical Hospital with Outpatient Health Center Moscow, Russia

N. K Vit'ko

Central Clinical Hospital with Outpatient Health Center Moscow, Russia

K. V Kotenko

Central Medical Authority of the Business Administration for the President of the Russian Federation Moscow, Russia

P. B Kopnin

N.N. Blokhin Cancer Research Center Moscow, Russia

References

  1. Schiaffino S., Partridge T. Skeletal muscle repair and regeneration. dordrecht: Springer Netherlands; 2008.
  2. Robertson T.A., Maley M.A., Grounds M. D. et al. The role of macrophages in skeletal muscle regeneration with particular reference to chemotaxis. Exp. Cell Res. 1993; 207(2): 321-31.
  3. Novak M.L., Bryer S.C., Cheng M. et al. Macrophage-specific expression of urokinase-type plasminogen activator promotes skeletal muscle regeneration. J. Immunol. 2011; 187t3): 1448-57.
  4. Christopher-Stine L., Plotz P. H. Myositis: an update on pathogenesis. Curr. Opin. Rheumatol. 2004; 16t6): 700-6.
  5. Spencer M. J., Walsh C.M., Dorshkind K.A. et al. Myonuclear apoptosis in dystrophic mdx muscle occurs by perforin-mediated cytotoxicity. J. Clin. Invest. 1997; 99t11): 2745-51.
  6. Pedersen B.K., Febbraio M.A. Muscle as an endocrine organ: focus on muscle-derived interleukin-6. Physiol. Rev. 2008; 88t4): 1379-406.
  7. Зорин В.Л., Зорина А.И., Пулин А.А. и др. Перспективы использования клеток, обладающих миогенным потенциалом, в лечении заболеваний скелетных мышц: обзор исследований. Ч. 1. Сателлитные клетки. Патологическая физиология и экспериментальная терапия 2015; 59(2): 88-98.
  8. Зорин В.Л., Зорина А. И., Пулин А.А. и др. Перспективы использования клеток, обладающих миогенным потенциалом, в лечении заболеваний скелетных мышц: обзор исследований Ч. 2. Популяции стволовых клеток мышечного и немышечного происхождения Патологическая физиология и экспериментальная терапия 2015;59(3): 106-17.
  9. Зорин В.Л., Еремин И.И., Рыбко В.А. и др. Слизистая оболочка полости рта - новый источник для получения миобластов. Гены Клетки 2014; 9(3): 76-84.
  10. Mitrano T.I., Grob M.S., Carrión F. et al. Culture and characterization of mesenchymal stem cells from human gingival tissue. J. Periodontol. 2010; 81(6): 917-25.
  11. 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 Клетки 2014; 9(1): 50-7.
  12. 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.
  13. 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.
  14. 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
  15. Amable P.R., Teixeira M.V.T., Carias R.B.V. et al. Protein synthesis and secretion in human mesenchymal cells derived from bone marrow, adipose tissue and Wharton's jelly. Stem Cell Res Ther. 2014; 5(2): 53.
  16. Podbregar M., Lainscak M., Prelovsek O. et al. Cytokine response of cultured skeletal muscle cells stimulated with proinflammatory factors depends on differentiation stage. Sci. World J. 2013; 2013: 1-8.
  17. Perrini S., Ficarella R., Picardi E. et al. Differences in gene expression and cytokine release profiles highlight the heterogeneity of distinct subsets of adipose tissue-derived stem cells in the subcutaneous and visceral adipose tissue in humans. PLoS One 2013; 8(3): e57892
  18. Naftali-Shani N., Itzhaki-Alfia A., Landa-Rouben N. et al. The origin of human mesenchymal stromal cells dictates their reparative properties J Am Heart Assoc 2013; 2(5): e000253
  19. Hsieh J., Wang H., Chang S. et al. Mesenchymal stem cells from human umbilical cord express preferentially secreted factors related to neuroprotection, neurogenesis, and angiogenesis PLoS One 2013; 8(8): e72604
  20. Rouger K., Larcher T., Dubreil L. et al. Systemic delivery of allogenic muscle stem cells induces long-term muscle repair and clinical efficacy in duchenne muscular dystrophy dogs. Am. J. Pathol. 2011; 179(5): 2501-18.
  21. Shi D., Reinecke H., Murry C.E. et al. Myogenic fusion of human bone marrow stromal cells, but not hematopoietic cells Blood 2004; 104(1): 290-4.
  22. Maxson S., Lopez E.A., Yoo D. et al. Concise review: role of mesenchymal stem cells in wound repair Stem Cells Transl Med 2012; 1(2): 142-9.
  23. Gnecchi M., Zhang Z., Ni A. et al. Paracrine mechanisms in adult stem cell signaling and therapy. Circ. Res. 2008; 103(11): 1204-19.
  24. Kinnaird T., Stabile E., Burnett M. S. et al. Local delivery of marrow-derived stromal cells augments collateral perfusion through paracrine mechanisms. Circulation 2004; 109(12): 1543-9.
  25. Giannoudis P., Jones E., Yang X. et al. Mesenchymal stem cells and skeletal regeneration. 1st ed. Academic Press; 2013.
  26. Yorio T., Clark A., Wax M. B. Ocular therapeutics: eye on new discoveries. 1st ed. Academic Pres; 2008.
  27. Peake J.M., Della Gatta P., Suzuki K. et al. Cytokine expression and secretion by skeletal muscle cells: regulatory mechanisms and exercise effects. Exerc. Immunol. Rev. 2015; 21: 8-25.
  28. Peterson J.M., Pizza F.X. Cytokines derived from cultured skeletal muscle cells after mechanical strain promote neutrophil chemotaxis in vitro. J. Appl. Physiol. 2008; 106(1): 130-7.
  29. Griffin C.A., Apponi L.H., Long K.K. et al. Chemokine expression and control of muscle cell migration during myogenesis J Cell Sci 2010; 123(Pt 18): 3052-60.
  30. Li Y.P., Schwartz R.J. TNF-alpha regulates early differentiation of C2C12 myoblasts in an autocrine fashion. FASEB J. 2001; 15(8): 1413-5
  31. Yahiaoui L., Gvozdic D., Danialou G. et al. CC family chemokines directly regulate myoblast responses to skeletal muscle injury J Physiol. 2008; 586(16): 3991-4004.
  32. Luo G., Hershko D.D., Robb B.W. et al. IL-1beta stimulates IL-6 production in cultured skeletal muscle cells through activation of MAP kinase signaling pathway and NF-kappa B Am J Physiol Regul Integr. Comp. Physiol. 2003; 284(5): R1249-54.
  33. Al-Shanti N., Saini A., Faulkner S.H. et al. Beneficial synergistic interactions of TNF-alpha and IL-6 in C2 skeletal myoblasts--potential cross-talk with IGF system. Growth Factors 2008; 26(2): 61-73.
  34. Alvarez B., Quinn L.S., Busquets S. et al. Tumor necrosis factor-a exerts interleukin-6-dependent and -independent effects on cultured skeletal muscle cells. Biochim. Biophys. Acta - Mol. Cell Res. 2002; 1542(1-3): 66-72.
  35. Frost R.A., Nystrom G.J., Lang C.H. Lipopolysaccharide and proinflammatory cytokines stimulate interleukin-6 expression in C2C12 myoblasts: role of the Jun NH2-terminal kinase. Am. J. Physiol. Regul. Integr. Comp. Physiol. 2003; 285(5): R1153-64.
  36. De Rossi M. Cytokines and chemokines are both expressed by human myoblasts: possible relevance for the immune pathogenesis of muscle inflammation. Int. Immunol. 2000; 12(9): 1329-35.
  37. Mishra D.K., Fridén J., Schmitz M.C. et al. Anti-inflammatory medication after muscle injury A treatment resulting in short-term improvement but subsequent loss of muscle function J Bone Joint Surg. Am. 1995; 77(10): 1510-9.
  38. Baoge L., Van Den Steen E., Rimbaut S. et al. Treatment of skeletal muscle injury: a review. ISRN Orthop. 2012; 2012: 689012.
  39. Rahusen F.T.G., Weinhold P.S., Almekinders L.C. Nonsteroidal anti-inflammatory drugs and acetaminophen in the treatment of an acute muscle injury. Am. J. Sports Med. 2004; 32(8): 1856-9.
  40. Authier F.J., Chazaud B., Plonquet A. et al. Differential expression of the IL-1 system components during in vitro myogenesis: Implication of IL-1 β in induction of myogenic cell apoptosis. Cell Death Differ. 1999; 6(10): 1012-21.
  41. Grabiec K., Tokarska J., Milewska M. et al. Interleukin-1beta stimulates early myogenesis of mouse C2C12 myoblasts: the impact on myogenic regulatory factors, extracellular matrix components, IGF binding proteins and protein kinases. Pol. J. Vet. Sci. 2013; 16(2): 255-64.
  42. Broussard S.R., McCusker R.H., Novakofski J.E. et al. IL-1beta impairs insulin-like growth factor i-induced differentiation and downstream activation signals of the insulin-like growth factor i receptor in myoblasts. J Immunol. 2004; 172(12): 7713-20.
  43. Fu X., Xiao J., Wei Y. et al. Combination of inflammation-related cytokines promotes long-term muscle stem cell expansion Cell Res 2015; 25(6): 655-73
  44. Li W., Moylan J.S., Chambers M.A. et al. Interleukin-1 stimulates catabolism in C2C12 myotubes. Am. J. Physiol. Cell Physiol. 2009; 297(3): C706-14.
  45. Bartoccioni E., Michaelis D., Hohlfeld R. Constitutive and cytokine-induced production of interleukin-6 by human myoblasts Immunol. Lett. 1994; 42(3): 135-8.
  46. Hoene M., Runge H., Häring H. U. et al. Interleukin-6 promotes myogenic differentiation of mouse skeletal muscle cells: role of the STAT3 pathway. Am. J. Physiol. Cell Physiol. 2013; 304(2): C128-36.
  47. Serrano A.L., Baeza-Raja B., Perdiguero E. et al. Interleukin-6 is an essential regulator of satellite cell-mediated skeletal muscle hypertrophy. Cell Metab. 2008; 7(1): 33-44.
  48. Pelosi M., De Rossi M., Barberi L. et al. IL-6 impairs myogenic differentiation by downmodulation of p90RSK/eEF2 and mTOR/p70S6K axes, without affecting AKT activity. Biomed. Res. Int. 2014; 2014: 206026
  49. Li P., Li S.-H., Wu J. et al. Interleukin-6 downregulation with mesenchymal stem cell differentiation results in loss of immunoprivilege J. Cell Mol. Med. 2013; 17(9): 1136-45.
  50. Pricola K.L., Kuhn N.Z., Haleem-Smith H. et al. Interleukin-6 maintains bone marrow-derived mesenchymal stem cell stemness by an ERK1/2-dependent mechanism. J. Cell Biochem. 2009; 108(3): 577-88.
  51. Akerstrom T., Steensberg A., Keller P. et al. Exercise induces interleukin-8 expression in human skeletal muscle J Physiol 2005; 563(Pt 2): 507-16.
  52. Frydelund-Larsen L., Penkowa M., Akerstrom T. et al. Exercise induces interleukin-8 receptor (CXCR2) expression in human skeletal muscle. Exp. Physiol. 2007; 92(1): 233-40.
  53. Gillessen S., Carvajal D., Ling P. et al. Mouse interleukin-12 (IL-12) p40 homodimer: a potent IL-12 antagonist. Eur. J. Immunol. 1995; 25(1): 200-6.
  54. D'Andrea A., Rengaraju M., Valiante N.M. et al. Production of natural killer cell stimulatory factor (interleukin 12) by peripheral blood mononuclear cells. J. Exp. Med. 1992; 176(5): 1387-98.
  55. Romanazzo S., Forte G., Morishima K. et al. IL-12 involvement in myogenic differentiation of C2C12 in vitro. Biomater. Sci. 2015; 3(3): 469-79.
  56. Quinn L.S., Anderson B.G., Drivdahl R.H. et al. Overexpression of interleukin-15 induces skeletal muscle hypertrophy in vitro: implications for treatment of muscle wasting disorders. Exp. Cell Res. 2002; 280(1): 55-63.
  57. Pistilli E. E., Quinn L.S. From anabolic to oxidative: reconsidering the roles of IL-15 and IL-15Ra in skeletal muscle. Exerc. Sport. Sci. Rev. 2013; 41(2): 100-6.
  58. Li F., Li Y., Tang Y. et al. Protective effect of myokine IL-15 against H2O2-mediated oxidative stress in skeletal muscle cells. Mol. Biol. Rep. 2014; 41(11): 7715-22.
  59. Plomgaard P., Penkowa M., Pedersen B.K. Fiber type specific expression of TNF-alpha, IL-6 and IL-18 in human skeletal muscles. Exerc. Immunol. Rev. 2005; 11: 53-63.
  60. Chandrasekar B., Mummidi S., Claycomb W.C., et al. Interleukin-18 is a pro-hypertrophic cytokine that acts through a phosphatidylinositol 3-kinase-phosphoinositide-dependent kinase-1-Akt-GATA4 signaling pathway in cardiomyocytes. J. Biol. Chem. 2005; 280(6): 4553-67
  61. Kalovidouris A. E., Plotkin Z., Graesser D. Interferon-gamma inhibits proliferation, differentiation, and creatine kinase activity of cultured human muscle cells. II. A possible role in myositis. J. Rheumatol. 1993; 20(10): 1718-23.
  62. Cheng M., Nguyen M., Fantuzzi G. et al. Endogenous interferongamma is required for efficient skeletal muscle regeneration. Am. J. Physiol. Cell Physiol. 2008; 294(5): C1183-91.
  63. Saghizadeh M., Ong J.M., Garvey W.T. et al. The expression of TNF alpha by human muscle. Relationship to insulin resistance. J. Clin. Invest. 1996; 97(4): 1111-6.
  64. Chen S., Jin B., Li Y. TNF-alpha regulates myogenesis and muscle regeneration by activating p38 MAPK. Am. J. Physiol. Cell Physiol. 2007; 292(5): C1660-71.
  65. Torrente Y., El Fahime E., Caron N. J. et al. Tumor necrosis factor-alpha (TNF-alpha) stimulates chemotactic response in mouse myogenic cells. Cell Transplant. 2003; 12(1): 91-100.
  66. Keeling S., Deashinta N., Howard K. M. et al. Macrophage colony stimulating factor-induced macrophage differentiation influences myotube elongation. Biol. Res. Nurs. 2013; 15(1): 62-70.
  67. Dumont N.A., Frenette J. Macrophage colony-stimulating factor-induced macrophage differentiation promotes regrowth in atrophied skeletal muscles and C2C12 myotubes. Am. J. Pathol. 2013; 182(2): 505-15.
  68. Rissanen T.T., Vajanto I., Hiltunen M.O. et al. Expression of vascular endothelial growth factor and vascular endothelial growth factor receptor-2 (KDR/Flk-1) in ischemic skeletal muscle and its regeneration. Am. J. Pathol. 2002; 160(4): 1393-403.
  69. Couffinhal T., Silver M., Zheng L.P. et al. Mouse model of angiogenesis. Am. J. Pathol. 1998; 152(6): 1667-79.
  70. Arsic N., Zacchigna S., Zentilin L. et al. Vascular endothelial growth factor stimulates skeletal muscle regeneration in Vivo. Mol. Ther. 2004; 10(5): 844-54.
  71. Швальб П.Г., Гавриленко А.В., Калинин Р.Е. и др. Эффективность и безопасность применения препарата «Неоваскулген» в комплексной терапии пациентов с хронической ишемией нижних конечностей (IIb-III фаза клинических испытаний). Клеточная трансплантология и тканевая инженерия 2011; 6(3): 83.
  72. Germani A., Di Carlo A., Mangoni A. et al. Vascular endothelial growth factor modulates skeletal myoblast function. Am. J. Pathol. 2003; 163(4): 1417-28.
  73. Bryan B.A., Walshe T.E., Mitchell D.C. et al. Coordinated vascular endothelial growth factor expression and signaling during skeletal myogenic differentiation. Mol. Biol. Cell. 2008; 19(3): 994-1006.
  74. Benigni F., Atsumi T., Calandra T. et al. The proinflammatory mediator macrophage migration inhibitory factor induces glucose catabolism in muscle. J. Clin. Invest. 2000; 106(10): 1291-300.
  75. Reimann J., Schnell S., Schwartz S. et al. Macrophage migration inhibitory factor in normal human skeletal muscle and inflammatory myopathies. J Neuropathol. Exp. Neurol. 2010; 69(6): 654-62
  76. O'Flaherty J., Mei Y., Freer M. et al. Signaling through the TRAIL receptor DR5/FADD pathway plays a role in the apoptosis associated with skeletal myoblast differentiation. Apoptosis 2006; 11(12): 2103-13.
  77. Mampuru L.J., Chen S.J., Kalenik J.L. et al. Analysis of events associated with serum deprivation-induced apoptosis in C3H/Sol8 muscle satellite cells. Exp. Cell Res. 1996; 226(2): 372-80.
  78. Sandri M., Carraro U. Apoptosis of skeletal muscles during development and disease. Int. J. Biochem. Cell Biol. 1999; 31(12): 1373-90.
  79. Broholm C., Laye M.J., Brandt C. et al. LIF is a contraction-induced myokine stimulating human myocyte proliferation. J. Appl. Physiol. 2011; 111(1): 251-9.
  80. Kurek J.B., Bower J.J., Romanella M. et al. The role of leukemia inhibitory factor in skeletal muscle regeneration. Muscle Nerve 1997; 20(7): 815-22.
  81. White J.D., Davies M., Grounds M.D. Leukaemia inhibitory factor increases myoblast replication and survival and affects extracellular matrix production: combined in vivo and in vitro studies in post-natal skeletal muscle. Cell Tissue Res. 2001; 306(1): 129-41.
  82. Hunt L.C., Tudor E.M., White J. D. Leukemia inhibitory factor-dependent increase in myoblast cell number is associated with phosphotidylinositol 3-kinase-mediated inhibition of apoptosis and not mitosis. Exp. Cell Res. 2010; 316(6): 1002-9.
  83. Forte G., Minieri M., Cossa P. et al. Hepatocyte growth factor effects on mesenchymal stem cells: proliferation, migration, and differentiation. Stem Cells 2006; 24(1): 23-33.
  84. Neuss S., Becher E., Wöltje M. et al. Functional expression of HGF and HGF receptor/c-met in adult human mesenchymal stem cells suggests a role in cell mobilization, tissue repair, and wound healing. Stem Cells 2004; 22(3): 405-14.
  85. Miller K.J., Thaloor D., Matteson S. et al. Hepatocyte growth factor affects satellite cell activation and differentiation in regenerating skeletal muscle. Am. J. Physiol. Cell Physiol. 2000; 278(1): C174-81.
  86. Anastasi S., Giordano S., Sthandier O. et al. A natural hepatocyte growth factor/scatter factor autocrine loop in myoblast cells and the effect of the constitutive Met kinase activation on myogenic differentiation. J. Cell Biol. 1997; 137(5): 1057-68.
  87. Tatsumi R., Allen R.E. Active hepatocyte growth factor is present in skeletal muscle extracellular matrix. Muscle Nerve 2004; 30(5): 654-8.
  88. Miyatake S., Bilan P. J., Pillon N. J. et al. Contracting C2C12 myotubes release CCL2 in an NF-KB-dependent manner to induce monocyte chemoattraction. Am. J. Physiol. Endocrinol. Metab. 2015 Nov 10. [Epub ahead of print].
  89. Henningsen J., Pedersen B.K., Kratchmarova I. Quantitative analysis of the secretion of the MCP family of chemokines by muscle cells. Mol. Biosyst. 2011; 7(2): 311-21.
  90. Shireman P.K., Contreras-Shannon V., Ochoa O. et al. MCP-1 deficiency causes altered inflammation with impaired skeletal muscle regeneration. J. Leukoc. Biol. 2007; 81(3): 775-85.
  91. Iwasaki S., Miyake M., Hayashi S. et al. Effect of myostatin on chemokine expression in regenerating skeletal muscle cells. Cells Tissues Organs. 2013; 198(1): 66-74.

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