The secretome of myocardial telocytes modulates the activity of cardiac stem cells

Journal of Cellular and Molecular Medicine

Volumn 19, Issue 8, 2015, Pages 1783-1794

  Albulescu, Radu ^a,b   Tanase, Cristiana ^a   Codrici, Elena ^a   Popescu, Daniela I ^a   Cretoiu, Sanda M ^a,c   Popescu, Laurentiu M ^a,c  

^a VICTOR BABES NATIONAL INSTITUTE OF PATHOLOGY   (Romania)

^b NATIONAL INSTITUTE FOR CHEMICAL PHARMACEUTICAL RESEARCH AND DEVELOPMENT   (Romania)

^c CAROL DAVILA UNIVERSITY OF MEDICINE AND PHARMACY   (Romania)

Author keywords

Cardiac stem cells; Chemokines; Cytokines; Fibroblasts; Growth factors; Luminex xMAP; SELDI TOF; Telocytes

Indexed keywords

CXCL1 CHEMOKINE; INTERLEUKIN 10; INTERLEUKIN 13; INTERLEUKIN 2; INTERLEUKIN 6; MACROPHAGE INFLAMMATORY PROTEIN 1ALPHA; MACROPHAGE INFLAMMATORY PROTEIN 2; MONOCYTE CHEMOTACTIC PROTEIN 1; VASCULOTROPIN; PROTEOME; VASCULOTROPIN A;

ADULT; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CARDIAC STEM CELL; CONTROLLED STUDY; MALE; MICROCHIP ELECTROPHORESIS; MOUSE; MYOCARDIAL TELOCYTE; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEOMICS; RAT; SECRETOME; STROMA CELL; SURFACE ENHANCED LASER DESORPTION IONIZATION TIME OF FLIGHT MASS SPECTROMETRY; 3T3 CELL LINE; ANIMAL; C57BL MOUSE; CARDIAC MUSCLE; CARDIAC MYOBLAST; CYTOLOGY; MATRIX-ASSISTED LASER DESORPTION-IONIZATION MASS SPECTROMETRY; METABOLISM; PROTEIN DATABASE; SECRETION (PROCESS); TELOCYTE; WISTAR RAT;

RATTUS;

3T3 CELLS; ANIMALS; DATABASES, PROTEIN; INTERLEUKIN-6; MALE; MICE; MICE, INBRED C57BL; MYOBLASTS, CARDIAC; MYOCARDIUM; PROTEOME; PROTEOMICS; RATS, WISTAR; SPECTROMETRY, MASS, MATRIX-ASSISTED LASER DESORPTION-IONIZATION; TELOCYTES; VASCULAR ENDOTHELIAL GROWTH FACTOR A;

EID: 84938059075     PISSN: 15821838     EISSN: None     Source Type: Journal    
DOI: 10.1111/jcmm.12624     Document Type: Article

References (93)

1. Popescu LM, Faussone-Pellegrini MS. TELOCYTES - a case of serendipity: the winding way from Interstitial Cells of Cajal (ICC), via Interstitial Cajal-Like Cells (ICLC) to TELOCYTES. J Cell Mol Med. 2010; 14: 729-40.
2. Suciu L, Nicolescu MI, Popescu LM. Cardiac telocytes: serial dynamic images in cell culture. J Cell Mol Med. 2010; 14: 2687-92.
3. Gherghiceanu M, Popescu LM. Cardiac telocytes - their junctions and functional implications. Cell Tissue Res. 2012; 348: 265-79.
4. Cretoiu D, Hummel E, Zimmermann H, et al. Human cardiac telocytes: 3D imaging by FIB-SEM tomography. J Cell Mol Med. 2014; 18: 2157-64.
5. Yang Y, Sun W, Wu SM, et al. Telocytes in human heart valves. J Cell Mol Med. 2014; 18: 759-65.
6. Cretoiu SM, Popescu LM. Telocytes revisited. Biomol Concepts. 2014; 5: 353-69.
7. Popescu LM, Curici A, Wang E, et al. Telocytes and putative stem cells in ageing human heart. J Cell Mol Med. 2015; 19: 31-45.
8. Tao L, Wang H, Wang X, et al. Cardiac telocytes. Curr Stem Cell Res Ther. 2015. Doi:10.2174/1574888X10666150113113420.
9. Cismasiu VB, Popescu LM. Telocytes transfer extracellular vesicles loaded with microRNAs to stem cells. J Cell Mol Med. 2015; 19: 351-8.
10. Popescu LM, Gherghiceanu M, Suciu LC, et al. Telocytes and putative stem cells in the lungs: electron microscopy, electron tomography and laser scanning microscopy. Cell Tissue Res. 2011; 345: 391-403.
11. Cretoiu D, Cretoiu SM, Simionescu AA, et al. Telocytes, a distinct type of cell among the stromal cells present in the lamina propria of jejunum. Histol Histopathol. 2012; 27: 1067-78.
12. Vannucchi MG, Traini C, Manetti M, et al. Telocytes express PDGFRalpha in the human gastrointestinal tract. J Cell Mol Med. 2013; 17: 1099-108.
13. Milia AF, Ruffo M, Manetti M, et al. Telocytes in Crohn's disease. J Cell Mol Med. 2013; 17: 1525-36.
14. Manetti M, Rosa I, Messerini L, et al. Telocytes are reduced during fibrotic remodelling of the colonic wall in ulcerative colitis. J Cell Mol Med. 2015; 19: 62-73.
15. Cretoiu SM, Cretoiu D, Popescu LM. Human myometrium - the ultrastructural 3D network of telocytes. J Cell Mol Med. 2012; 16: 2844-9.
16. Cretoiu SM, Cretoiu D, Marin A, et al. Telocytes: ultrastructural, immunohistochemical and electrophysiological characteristics in human myometrium. Reproduction. 2013; 145: 357-70.
17. Campeanu RA, Radu BM, Cretoiu SM, et al. Near-infrared low-level laser stimulation of telocytes from human myometrium. Lasers Med Sci. 2014; 29: 1867-74.
18. Yang J, Chi C, Liu Z, et al. Ultrastructure damage of oviduct telocytes in rat model of acute salpingitis. J Cell Mol Med. 2015; 19: 1720-8.
19. Suciu L, Popescu LM, Gherghiceanu M, et al. Telocytes in human term placenta: morphology and phenotype. Cells Tissues Organs. 2010; 192: 325-39.
20. Bosco C, Diaz E, Gutierrez R, et al. Placental hypoxia developed during preeclampsia induces telocytes apoptosis in chorionic villi affecting the maternal-fetus metabolic exchange. Curr Stem Cell Res Ther. 2015. Doi: 10.2174/1574888X10666150202144855.
21. Bosco C, Diaz E, Gutierrez R, et al. A putative role for telocytes in placental barrier impairment during preeclampsia. Med Hypotheses. 2015; 84: 72-7.
22. Vannucchi MG, Traini C, Guasti D, et al. Telocytes subtypes in human urinary bladder. J Cell Mol Med. 2014; 18: 2000-8.
23. Povysil C, Kana M, Zamecnik L, et al. Podoplanin (D2-40) is a reliable marker of urinary bladder myofibroblasts (telocytes). Folia Biol (Praha). 2014; 60: 286-9.
24. Suciu LC, Popescu BO, Kostin S, et al. Platelet-derived growth factor receptor-beta-positive telocytes in skeletal muscle interstitium. J Cell Mol Med. 2012; 16: 701-7.
25. Diaz-Flores L, Gutierrez R, Saez FJ, et al. Telocytes in neuromuscular spindles. J Cell Mol Med. 2013; 17: 457-65.
26. Xiao J, Wang F, Liu Z, et al. Telocytes in liver: electron microscopic and immunofluorescent evidence. J Cell Mol Med. 2013; 17: 1537-42.
27. Wang F, Song Y, Bei Y, et al. Telocytes in liver regeneration: possible roles. J Cell Mol Med. 2014; 18: 1720-6.
28. Fu S, Wang F, Cao Y, et al. Telocytes in human liver fibrosis. J Cell Mol Med. 2015; 19: 676-83.
29. Nicolescu MI, Popescu LM. Telocytes in the interstitium of human exocrine pancreas: ultrastructural evidence. Pancreas. 2012; 41: 949-56.
30. Nicolescu MI, Bucur A, Dinca O, et al. Telocytes in parotid glands. Anat Rec. 2012; 295: 378-85.
31. Alunno A, Ibba-Manneschi L, Bistoni O, et al. Telocytes in minor salivary glands of primary Sjogren's syndrome: association with the extent of inflammation and ectopic lymphoid neogenesis. J Cell Mol Med. 2015; 19:1689-96.
32. Ceafalan L, Gherghiceanu M, Popescu LM, et al. Telocytes in human skin-are they involved in skin regeneration? J Cell Mol Med. 2012; 16: 1405-20.
33. Manetti M, Guiducci S, Ruffo M, et al. Evidence for progressive reduction and loss of telocytes in the dermal cellular network of systemic sclerosis. J Cell Mol Med. 2013; 17: 482-96.
34. Cretoiu D, Gherghiceanu M, Hummel E, et al. FIB-SEM tomography of human skin telocytes and their extracellular vesicles. J Cell Mol Med. 2015; 19: 714-722. Doi:10.1111/jcmm.12578.
35. Manole CG, Gherghiceanu M, Simionescu O. Telocyte dynamics in psoriasis. J Cell Mol Med. 2015; 19: 1504-19.
36. Popescu BO, Gherghiceanu M, Kostin S, et al. Telocytes in meninges and choroid plexus. Neurosci Lett. 2012; 516: 265-9.
37. Luesma MJ, Gherghiceanu M, Popescu LM. Telocytes and stem cells in limbus and uvea of mouse eye. J Cell Mol Med. 2013; 17: 1016-24.
38. Cantarero I, Luesma MJ, Alvarez-Dotu JM, et al. Transmission electron microscopy as key technique for the characterization of telocytes. Curr Stem Cell Res Ther. 2015. Doi:10.2174/1574888X10666150306155435.
39. Bei Y, Zhou Q, Fu S, et al. Cardiac telocytes and fibroblasts in primary culture: different morphologies and immunophenotypes. PLoS ONE. 2015; 10: e0115991.
40. Niculite CM, Regalia TM, Gherghiceanu M, et al. Dynamics of telopodes (telocyte prolongations) in cell culture depends on extracellular matrix protein. Mol Cell Biochem. 2015; 398: 157-64.
41. Cismasiu VB, Radu E, Popescu LM. miR-193 expression differentiates telocytes from other stromal cells. J Cell Mol Med. 2011; 15: 1071-4.
42. Zheng Y, Zhang M, Qian M, et al. Genetic comparison of mouse lung telocytes with mesenchymal stem cells and fibroblasts. J Cell Mol Med. 2013; 17: 567-77.
43. Zheng Y, Cretoiu D, Yan G, et al. Comparative proteomic analysis of human lung telocytes with fibroblasts. J Cell Mol Med. 2014; 18: 568-89.
44. Zheng Y, Cretoiu D, Yan G, et al. Protein profiling of human lung telocytes and microvascular endothelial cells using iTRAQ quantitative proteomics. J Cell Mol Med. 2014; 18: 1035-59.
45. Sun X, Zheng M, Zhang M, et al. Differences in the expression of chromosome 1 genes between lung telocytes and other cells: mesenchymal stem cells, fibroblasts, alveolar type II cells, airway epithelial cells and lymphocytes. J Cell Mol Med. 2014; 18: 801-10.
46. Zheng M, Sun X, Zhang M, et al. Variations of chromosomes 2 and 3 gene expression profiles among pulmonary telocytes, pneumocytes, airway cells, mesenchymal stem cells and lymphocytes. J Cell Mol Med. 2014; 18: 2044-60.
47. Sheng J, Shim W, Lu J, et al. Electrophysiology of human cardiac atrial and ventricular telocytes. J Cell Mol Med. 2014; 18: 355-62.
48. Cretoiu SM, Radu BM, Banciu A, et al. Isolated human uterine telocytes: immunocytochemistry and electrophysiology of T-type calcium channels. Histochem Cell Biol. 2015; 143: 83-94.
49. + stromal cells/telocytes: endocytic property of telocytes. J Cell Mol Med. 2014; 18: 2478-87.
50. + stromal cells/fibroblasts/fibrocytes/telocytes as a tissue reserve and a principal source of mesenchymal cells. Location, morphology, function and role in pathology. Histol Histopathol. 2014; 29: 831-70.
51. + stromal cells/telocytes have progenitor capacity and are a source of alphasma+ cells during repair. Histol Histopathol. 2015; 30: 615-27.
52. Bani D, Nistri S. New insights into the morphogenic role of stromal cells and their relevance for regenerative medicine. Lessons from the heart. J Cell Mol Med. 2014; 18: 363-70.
53. Bani D, Formigli L, Gherghiceanu M, et al. Telocytes as supporting cells for myocardial tissue organization in developing and adult heart. J Cell Mol Med. 2010; 14: 2531-8.
54. Gherghiceanu M, Popescu LM. Cardiomyocyte precursors and telocytes in epicardial stem cell niche: electron microscope images. J Cell Mol Med. 2010; 14: 871-7.
55. Bojin FM, Gavriliuc OI, Cristea MI, et al. Telocytes within human skeletal muscle stem cell niche. J Cell Mol Med. 2011; 15: 2269-72.
56. Fertig ET, Gherghiceanu M, Popescu LM. Extracellular vesicles release by cardiac telocytes: electron microscopy and electron tomography. J Cell Mol Med. 2014; 18: 1938-43.
57. Barile L, Lionetti V, Cervio E, et al. Extracellular vesicles from human cardiac progenitor cells inhibit cardiomyocyte apoptosis and improve cardiac function after myocardial infarction. Cardiovasc Res. 2014; 103: 530-41.
58. Manole CG, Cismasiu V, Gherghiceanu M, et al. Experimental acute myocardial infarction: telocytes involvement in neo-angiogenesis. J Cell Mol Med. 2011; 15: 2284-96.
59. Zhao B, Chen S, Liu J, et al. Cardiac telocytes were decreased during myocardial infarction and their therapeutic effects for ischaemic heart in rat. J Cell Mol Med. 2013; 17: 123-33.
60. Zhao B, Liao Z, Chen S, et al. Intramyocardial transplantation of cardiac telocytes decreases myocardial infarction and improves post-infarcted cardiac function in rats. J Cell Mol Med. 2014; 18: 780-9.
61. Urbanek K, Rota M, Cascapera S, et al. Cardiac stem cells possess growth factor-receptor systems that after activation regenerate the infarcted myocardium, improving ventricular function and long-term survival. Circ Res. 2005; 97: 663-73.
62. Nagoshi T, Matsui T, Aoyama T, et al. PI3K rescues the detrimental effects of chronic Akt activation in the heart during ischemia/reperfusion injury. J Clin Invest. 2005; 115: 2128-38.
63. Urbanek K, Torella D, Sheikh F, et al. Myocardial regeneration by activation of multipotent cardiac stem cells in ischemic heart failure. Proc Natl Acad Sci USA. 2005; 102: 8692-7.
64. http://www.chem.agilent.com/library/usermanuals/Public/G2938-90310_AgilentHighSensitivityProtein250KitGuide.pdf. 2014.
65. http://www.merckmillipore.com/GB/en/product/MILLIPLEX-MAP-Rat-CytokineChemokine-Magnetic-Bead-Panel-Premixed-27-Plex-Immunology-Multiplex-Assay, MM_NF-RECYMAG65K27PMX. 2014.
66. http://www.merckmillipore.com/GB/en/product/MILLIPLEX-MAP-Mouse-Cytokine-Chemokine-Magnetic-Bead-Panel-Premixed-25-Plex-Immunology-Multiplex-Assay, MM_NF-MCYTOMAG-70K-PMX. 2014.
67. www.uniprot.org.
68. Ailawadi S, Wang X, Gu H, et al. Pathologic function and therapeutic potential of exosomes in cardiovascular disease. Biochim Biophys Acta. 2015; 1852: 1-11.
69. Harrison RH, St-Pierre JP, Stevens MM. Tissue engineering and regenerative medicine: a year in review. Tissue Eng Part B Rev. 2014; 20: 1-16.
70. Barile L, Gherghiceanu M, Popescu LM, et al. Ultrastructural evidence of exosome secretion by progenitor cells in adult mouse myocardium and adult human cardiospheres. J Biomed Biotechnol. 2012; 2012: 354605.
71. Mohri T, Fujio Y, Obana M, et al. Signals through glycoprotein 130 regulate the endothelial differentiation of cardiac stem cells. Arterioscler Thromb Vasc Biol. 2009; 29: 754-60.
72. Pereira MJ, Carvalho IF, Karp JM, et al. Sensing the cardiac environment: exploiting cues for regeneration. J Cardiovasc Transl Res. 2011; 4: 616-30.
73. Shabbir A, Zisa D, Lin H, et al. Activation of host tissue trophic factors through JAK-STAT3 signaling: a mechanism of mesenchymal stem cell-mediated cardiac repair. Am J Physiol Heart Circ Physiol. 2010; 299: H1428-38.
74. Irving SG, Zipfel PF, Balke J, et al. Two inflammatory mediator cytokine genes are closely linked and variably amplified on chromosome 17q. Nucleic Acids Res. 1990; 18: 3261-70.
75. Tang JM, Wang JN, Zhang L, et al. VEGF/SDF-1 promotes cardiac stem cell mobilization and myocardial repair in the infarcted heart. Cardiovasc Res. 2011; 91: 402-11.
76. Bei Y, Wang F, Yang C, Xiao J. Telocytes in regenerative medicine. J Cell Mol Med. 2015. Doi:10.1111/jcmm.12594.
77. Song YH, Gehmert S, Sadat S, et al. VEGF is critical for spontaneous differentiation of stem cells into cardiomyocytes. Biochem Biophys Res Commun. 2007; 354: 999-1003.
78. Mangi AA, Noiseux N, Kong D, et al. Mesenchymal stem cells modified with Akt prevent remodeling and restore performance of infarcted hearts. Nat Med. 2003; 9: 1195-201.
79. Markel TA, Wang Y, Herrmann JL, et al. VEGF is critical for stem cell-mediated cardioprotection and a crucial paracrine factor for defining the age threshold in adult and neonatal stem cell function. Am J Physiol Heart Circ Physiol. 2008; 295: H2308-14.
80. Uemura R, Xu M, Ahmad N, et al. Bone marrow stem cells prevent left ventricular remodeling of ischemic heart through paracrine signaling. Circ Res. 2006; 98: 1414-21.
81. Ye L, Haider H, Tan R, et al. Transplantation of nanoparticle transfected skeletal myoblasts overexpressing vascular endothelial growth factor-165 for cardiac repair. Circulation. 2007; 116: I113-20.
82. Melchiorri AJ, Nguyen BN, Fisher JP. Mesenchymal stem cells: roles and relationships in vascularization. Tissue Eng Part B Rev. 2014; 20: 218-28.
83. Wang M, Tan J, Wang Y, et al. IL-18 binding protein-expressing mesenchymal stem cells improve myocardial protection after ischemia or infarction. Proc Natl Acad Sci USA. 2009; 106: 17499-504.
84. Huang J, Lin X, Shi Y, et al. Tissue engineering and regenerative medicine in basic research: a year in review of 2014. Tissue Eng Part B Rev. 2015; 21: 167-76.
85. Al-Alwan LA, Chang Y, Mogas A, et al. Differential roles of CXCL2 and CXCL3 and their receptors in regulating normal and asthmatic airway smooth muscle cell migration. J Immunol. 2013; 191: 2731-41.
86. Chang Y, Al-Alwan L, Risse PA, et al. Th17-associated cytokines promote human airway smooth muscle cell proliferation. FASEB J. 2012; 26: 5152-60.
87. Zhang J, Xiao Z, Qu C, et al. CD8 T cells are involved in skeletal muscle regeneration through facilitating MCP-1 secretion and Gr1(high) macrophage infiltration. J Immunol. 2014; 193: 5149-60.
88. Pinto AR, Godwin JW, Rosenthal NA. Macrophages in cardiac homeostasis, injury responses and progenitor cell mobilisation. Stem Cell Res. 2014; 13: 705-14.
89. Ben-Mordechai T, Holbova R, Landa-Rouben N, et al. Macrophage subpopulations are essential for infarct repair with and without stem cell therapy. J Am Coll Cardiol. 2013; 62: 1890-901.
90. Nakajima H, Uchida K, Guerrero AR, et al. Transplantation of mesenchymal stem cells promotes an alternative pathway of macrophage activation and functional recovery after spinal cord injury. J Neurotrauma. 2012; 29: 1614-25.
91. Stoffels JM, Zhao C, Baron W. Fibronectin in tissue regeneration: timely disassembly of the scaffold is necessary to complete the build. Cell Mol Life Sci. 2013; 70: 4243-53.
92. Wang J, Karra R, Dickson AL, et al. Fibronectin is deposited by injury-activated epicardial cells and is necessary for zebrafish heart regeneration. Dev Biol. 2013; 382: 427-35.
93. Hunt GC, Singh P, Schwarzbauer JE. Endogenous production of fibronectin is required for self-renewal of cultured mouse embryonic stem cells. Exp Cell Res. 2012; 318: 1820-31.