Telocytes and putative stem cells in ageing human heart

Journal of Cellular and Molecular Medicine

Volumn 19, Issue 1, 2015, Pages 31-45

  Popescu, Laurentiu M ^a,b   Curici, Antoanela ^a   Wang, Enshi ^c   Zhang, Hao ^c   Hu, Shengshou ^c   Gherghiceanu, Mihaela ^b  

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

^b VICTOR BABES NATIONAL INSTITUTE OF PATHOLOGY   (Romania)

^c PEKING UNION MEDICAL COLLEGE   (China)

Author keywords

Cardiac stem cells; Cardiomyocytes; Fibroblasts; Human ageing heart; Lipofuscin granules; Macrophages; Schwann cells; Telocytes

Indexed keywords

ADOLESCENT; ADULT; AGING; CHILD; CYTOLOGY; FEMALE; HEART ATRIUM; HEART MUSCLE; HEART MUSCLE CELL; HUMAN; INFANT; INTERSTITIAL CELL OF CAJAL; MALE; MIDDLE AGED; NEWBORN; PHYSIOLOGY; STEM CELL; ULTRASTRUCTURE;

ADOLESCENT; ADULT; AGING; CHILD; FEMALE; HEART ATRIA; HUMANS; INFANT; INFANT, NEWBORN; INTERSTITIAL CELLS OF CAJAL; MALE; MIDDLE AGED; MYOCARDIUM; MYOCYTES, CARDIAC; STEM CELLS;

EID: 84921541190     PISSN: 15821838     EISSN: None     Source Type: Journal    
DOI: 10.1111/jcmm.12509     Document Type: Article

References (114)

1. Adler CP, Costabel U. Cell number in human heart in atrophy, hypertrophy, and under the influence of cytostatics. Recent Adv Stud Cardiac Struct Metab. 1975; 6: 343-55.
2. Gerdes AM. Cardiomyocyte ultrastructure. In: Hill JA, Olsen EN, editors. Muscle: fundamental biology and mechanisms of disease. San Diego: Academic Press; 2012. pp. 47-55.
3. Zak R. Development and proliferative capacity of cardiac muscle cells. Circ Res. 1974; 32: II-17-26.
4. Nag AC, Zak R. Dissociation of adult mammalian heart into single cell suspension: an ultrastructural study. J Anat. 1979; 129: 541-59.
5. Nag AC. Study of non-muscle cells of the adult mammalian heart: a fine structural analysis and distribution. Cytobios. 1980; 28: 41-61.
6. Vliegen HW, Van der Laarse A, Cornelisse CJ, et al. Myocardial changes in pressure overload-induced left ventricular hypertrophy. A study on tissue composition, polyploidization and multinucleation. Eur Heart J. 1991; 12: 488-94.
7. Camelliti P, Borg TK, Kohl P. Structural and functional characterization of cardiac fibroblasts. Cardiovasc Res. 2005; 65: 40-51.
8. Baudino TA, Carver W, Giles W, et al. Cardiac fibroblasts: friend or foe? Am J Physiol Heart Circ Physiol. 2006; 291: H1015-26.
9. Kohl P, Camelliti P. Fibroblast-myocyte connections in the heart. Heart Rhythm. 2011; 9: 461-4.
10. 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.
11. Gherghiceanu M, Popescu LM. Cardiomyocyte precursors and telocytes in epicardial stem cell niche: electron microscope images. J Cell Mol Med. 2010; 14: 871-7.
12. Gherghiceanu M, Manole CG, Popescu LM. Telocytes in endocardium: electron microscope evidence. J Cell Mol Med. 2010; 14: 2330-4.
13. Kostin S. Myocardial telocytes: a specific new cellular entity. J Cell Mol Med. 2010; 14: 1917-21.
14. Popescu LM, Manole CG, Gherghiceanu M, et al. Telocytes in human epicardium. J Cell Mol Med. 2010; 14: 2085-93.
15. Suciu L, Nicolescu MI, Popescu LM. Cardiac telocytes: serial dynamic images in cell culture. J Cell Mol Med. 2010; 14: 2687-92.
16. Popescu LM. The tandem: telocytes-stem cells. Int J Biol Biomed Eng. 2011; 5: 83-92.
17. Faussone-Pellegrini MS, Popescu LM. Telocytes. BioMol Concepts. 2011; 2: 481-9.
18. Gherghiceanu M, Popescu LM. Cardiac telocytes - their junctions and functional implications. Cell Tissue Res. 2012; 348: 265-79.
19. Rusu MC, Pop F, Hostiuc S, et al. Telocytes form networks in normal cardiac tissues. Histol Histopathol. 2012; 27: 807-16.
20. Zheng Y, Bai C, Wang X. Telocyte morphologies and potential roles in diseases. J Cell Physiol. 2012; 227: 2311-7.
21. Popescu LM, Nicolescu MI. Telocytes and stem cells. In: Goldenberg RCdS, de Campos Carvalho AC, editors. Resident stem cells and regenerative therapy, 1st ed., Chapter 11. Academic Press/Elsevier; 2013. pp. 205-331.
22. Sheng J, Shim W, Lu J, et al. Electrophysiology of human cardiac atrial and ventricular telocytes. J Cell Mol Med. 2014; 18: 355-62.
23. Yang Y, Sun W, Wu SM, et al. Telocytes in human heart valves. J Cell Mol Med. 2014; 18: 759-65.
24. Zhou J, Wang Y, Zhu P, et al. Distribution and characteristics of telocytes as nurse cells in the architectural organization of engineering heart tissues. Sci China Life Sci. 2014; 57: 241-7.
25. 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.
26. Smythies J, Edelstein L. Telocytes, exosomes, gap junctions and cytoskeleton: the makings of a primitive nervous system? Front Cell Neurosci. 2014; 7: 278.
27. Edelstein L, Smythies J. The role of telocytes in morphogenetic bioelectrical signaling: once more unto the breach. Front Cell Neurosci. 2014; 7: 41.
28. Díaz-Flores L, Gutiérrez R, García MP, et al. CD34+ 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.
29. Niculite CM, Regalia TM, Gherghiceanu M, et al. Dynamics of telopodes (telocyte prolongations) in cell culture depends on extracellular matrix protein. MolCell Biochem. 2015; 398: 157-64.
30. Kizilyaprak C, Bittermann AG, Daraspe J, et al. FIB-SEM tomography in biology. Methods Mol Biol. 2014; 1117: 541-58.
31. 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.
32. 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.
33. 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.
34. Cretoiu SM, Cretoiu D, Marin A, et al. Telocytes: ultrastructural, immunohistochemical and electrophysiological characteristics in human myometrium. Reproduction. 2013; 145: 357-70.
35. Cretoiu SM, Radu BM, Banciu A, et al. Isolated human uterine telocytes: immunocytochemistry and electrophysiology of T-type calcium channels. HistochemCell Biol. 2014; Doi:10.1007/s00418-014-1268-0.
36. Cismasiu VB, Radu E, Popescu LM. miR-193 expression differentiates telocytes from other stromal cells. J Cell Mol Med. 2011; 15: 1071-4.
37. 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.
38. 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.
39. Zheng M, Sun X, Zhang M, et al. Variations of chromosome 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.
40. 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.
41. Hinescu ME, Popescu LM. Interstitial Cajal-like cells (ICLC) in human atrial myocardium. J Cell Mol Med. 2005; 9: 972-5.
42. Hinescu ME, Gherghiceanu M, Mandache E, et al. Interstitial Cajal-like cells (ICLC) in atrial myocardium: ultrastructural and immunohistochemical characterization. J Cell Mol Med. 2006; 10: 243-57.
43. Popescu LM, Gherghiceanu M, Hinescu ME, et al. Insights into the interstitium of ventricular myocardium: interstitial Cajal-like cells (ICLC). J Cell Mol Med. 2006; 10: 429-58.
44. Mandache E, Popescu LM, Gherghiceanu M. Myocardial interstitial Cajal-like cells (ICLC) and their nanostructural relationships with intercalated discs: shed vesicles as intermediates. J Cell Mol Med. 2007; 11: 1175-84.
45. Gherghiceanu M, Hinescu ME, Andrei F, et al. Interstitial Cajal-like cells (ICLC) in myocardial sleeves of human pulmonary veins. J Cell Mol Med. 2008; 12: 1777-81.
46. Popescu LM, Gherghiceanu M, Manole CG, et al. Cardiac renewing: interstitial Cajal-like cells nurse cardiomyocyte progenitors in epicardial stem cell niches. J Cell Mol Med. 2009; 13: 866-86.
47. Kostin S, Popescu LM. A distinct type of cell in myocardium: interstitial Cajal-like cells (ICLCs). J Cell Mol Med. 2009; 13: 295-308.
48. Cretoiu SM, Popescu LM. Telocytes revisited. BioMol Concepts. 2014; 5: 353-69.
49. Manole CG, Cismaşiu V, Gherghiceanu M, et al. Experimental acute myocardial infarction: telocytes involvement in neo-angiogenesis. J Cell Mol Med. 2011; 15: 2284-96.
50. 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.
51. Gherghiceanu M, Popescu LM. Heterocellular communication in the heart: electron tomography of telocyte-myocyte junctions. J Cell Mol Med. 2011; 15: 1005-11.
52. Franke WW, Rickelt S, Barth M, et al. The junctions that don't fit the scheme: special symmetrical cell-cell junctions of their own kind. Cell Tissue Res. 2009; 338: 1-17.
53. Hinescu ME, Gherghiceanu M, Suciu L, et al. Telocytes in pleura: two- and three-dimensional imaging by transmission electron microscopy. Cell Tissue Res. 2011; 343: 389-97.
54. Mühlfeld C, Nyengaard JR, Mayhew TM. A review of state-of-the-art stereology for better quantitative 3D morphology in cardiac research. Cardiovasc Pathol. 2010; 19: 65-82.
55. Marone G, Crescenzo G, Adt M, et al. Immunological characterisation and functional importance of human heart mast cells. Immunopharmacology. 1995; 31: 1-18.
56. Fairweather D, Frisancho-Kiss S. Mast cells and inflammatory disease: potential drug targets. Cardiovasc Hematol Disord Drug Targets. 2008; 8: 80-90.
57. Simionescu M, Popov D, Sima A. Endothelial transcytosis in health and disease. Cell Tissue Res. 2009; 335: 27-40.
58. Popescu LM, Gherghiceanu M, Mandache E, et al. Caveolae in smooth muscles: nanocontacts. J Cell Mol Med. 2006; 10: 960-90.
59. Sims DE. The pericyte - a review. Tissue Cell. 1986; 18: 153-74.
60. Díaz-Flores L, Gutiérrez R, Madrid JF, et al. Pericytes. Morphofunction, interactions and pathology in a quiescent and activated mesenchymal cell niche. Histol Histopathol. 2009; 24: 909-69.
61. Nees S, Weiss DR, Juchem G. Focus on cardiac pericytes. Eur J Physiol. 2013; 465: 779-87.
62. Porter KE, Turner NA. Cardiac fibroblasts: at the heart of myocardial remodeling. Pharmacol Ther. 2009; 123: 255-78.
63. Kohl P, Camelliti P, Burton FL, et al. Electrical coupling of fibroblasts and myocytes: relevance for cardiac propagation. J Electrocardiol. 2005; 38: 45-50.
64. Davis J, Molkentin JD. Myofibroblasts: trust your heart and let fate decide. J Mol Cell Cardiol. 2014; 70: 9-18.
65. Sun Y, Weber KT. Infarct scar: a dynamic tissue. Cardiovasc Res. 2000; 46: 250-6.
66. Nahrendorf M, Swirski FK. Monocyte and macrophage heterogeneity in the heart. Circ Res. 2013; 112: 1624-33.
67. Lynton PJ, Thoman ML. Immunosenescence in monocytes, macrophages, and dendritic cells: lessons learned from the lung and heart. Immunol Lett. 2014; pii: S0165-2478(14)00196-5.
68. Gherghiceanu M, Barad L, Novak A, et al. Cardiomyocytes derived from human embryonic and induced pluripotent stem cells: comparative ultrastructure. J Cell Mol Med. 2011; 15: 2539-51.
69. Schaper J, Meiser E, Stämmler G. Ultrastructural morphometric analysis of myocardium from dogs, rats, hamsters, mice and from human hearts. Circ Res. 1985; 56: 377-91.
70. Barth E, Stämmler G, Speiser B, et al. Ultrastructural quantification of mitochondria and myofilaments in cardiac muscle from 10 different animal species including man. J Mol Cell Cardiol. 1992; 24: 669-81.
71. Pinali C, Kitmitto A. Serial block face scanning electron microscopy for the study of cardiac muscle ultrastructure at nanoscale resolutions. J Mol Cell Cardiol. 2014; 76: 1-11.
72. Bergmann O, Bhardwaj RD, Bernard S, et al. Evidence for cardiomyocyte renewal in humans. Science. 2009; 324: 98-102.
73. Yang P, Kenchegomda D, Fisher SA. Cardiac myocyte proliferation: not as simple as counting sheep. J Molec Cell Cardiol. 2014; 74: 125-6.
74. Anversa P, Hiler B, Ricci R, et al. Myocyte cell loss and myocyte hypertrophy in the aging rat heart. J Am Coll Cardiol. 1986; 8: 1441-8.
75. Olivetti G, Melissari M, Capasso JM, et al. Cardiomyopathy of the aging human heart. Myocyte loss and reactive cellular hypertrophy. Circ Res. 1991; 68: 1560-8.
76. Rakusan K, Flanagan MF, Geva T, et al. Morphometry of human coronary capillaries during normal growth and the effect of age in left-ventricular pressure-overload hypertrophy. Circulation. 1992; 86: 38-46.
77. Mayhew TM, Pharaon A, Austin A, et al. Stereological estimates of nuclear number in human ventricular cardiomyocytes before and after birth obtained using physical disectors. J Anat. 1997; 191: 107-15.
78. Wulfsohn D, Nyengaard JR, Tang Y. Postnatal growth of cardiomyocytes in the left ventricle of the rat. Anat Rec. 2004; 277A: 236-47.
79. Banerjee I, Fuseler JW, Price RL, et al. Determination of cell types and numbers during cardiac development in the neonatal and adult rat and mouse. Am J Physiol Heart Circ Physiol. 2007; 293: H1883-91.
80. Tang Y, Nyengaard JR, Andersen JB, et al. The application of stereological methods for estimating structural parameters in the human heart. The anatomical record. 2009; 292: 1630-47.
81. Kajstura J, Gurusamy N, Ogórek B, et al. Myocyte turnover in the aging human heart. Circ Res. 2010; 107: 1374-86.
82. Mollova M, Bersell K, Walsh S, et al. Cardiomyocyte proliferation contributes to heart growth in young humans. Proc Natl Acad Sci USA. 2013; 110: 1446-51.
83. Anversa P, Leri A. Innate regeneration of aging heart: healing from within. Mayo Clin Proc. 2013; 88: 871-83.
84. Negro A, Boehm M. Cardiomyocyte maturation: it takes a village to raise a kid. J Molec Cell Cardiol. 2014; 74: 669-81.
85. Porrello ER, Widdop RE, Delbridge LM. Early origins of cardiac hypertrophy: does cardiomyocyte attrition programme for pathological 'catch-up' growth of the heart? Clin Exp Pharmacol Physiol. 2008; 35: 1358-64.
86. Mescher AL. Junqueira basic histology: text and atlas. 13th ed. Shanghai: McGraw-Hill Medical; 2013. pp. 205.
87. Severs NJ. The cardiac muscle cell. BioEssays. 2000; 22: 188-99.
88. Lajiness JD, Conway SJ. Origin, development, and differentiation of cardiac fibroblasts. J Mol Cell Cardiol. 2014; 70: 2-8.
89. Snider P, Standley KN, Wang J, et al. Origin of cardiac fibroblasts and the role of periostin. Circ Res. 2009; 105: 934-47.
90. Souders CA, Bowers SL, Baudino TA. Cardiac fibroblast: the renaissance cell. Circ Res. 2009; 105: 1164-76.
91. Jugdutt BI. Ventricular remodeling after infarction and the extracellular collagen matrix: when is enough enough? Circulation. 2003; 108: 1395-403.
92. Kendall RT, Feghali-Bostwick CA. Fibroblasts in fibrosis: novel roles and mediators. Front Pharmacol. 2014; 5: 1-13.
93. Aurora AB, Porrello ER, Tan W, et al. Macrophages are required for neonatal heart regeneration. J Clin Invest. 2014; 124: 1382-92.
94. Epelman S, Lavine KJ, Beaudin AE, et al. Embryonic and adult-derived resident cardiac macrophages are maintained through distinct mechanisms at steady state and during inflammation. Immunity. 2014; 40: 91-104.
95. 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.
96. Mandache E, Gherghiceanu M, Macarie C, et al. Telocytes in human isolated atrial amyloidosis: ultrastructural remodelling. J Cell Mol Med. 2010; 14: 2739-47.
97. Manetti M, Rosa I, Messerini L, et al. A loss of telocytes accompanies fibrosis of multiple organs in systemic sclerosis. J Cell Mol Med. 2014; 18: 253-62.
98. Beltrami AP, Barlucchi L, Torella D, et al. Adult cardiac stem cells are multipotent and support myocardial regeneration. Cell. 2003; 1114: 763-76.
99. Chien KR. Stem cells: lost in translation. Nature. 2004; 428: 607-8.
100. Boyle AJ, Schulman SP, Hare JM, et al. Is stem cell therapy ready for patients? Stem cell therapy for cardiac repair. Ready for the next step. Circulation. 2006; 114: 339-52.
101. Boudoulas KD, Hatzopoulos AK. Cardiac repair and regeneration: the Rubik's cube of cell therapy for heart disease. Dis Model Mech. 2009; 2: 344-58.
102. du Pré BC, Doevendans PA, van Laake LW. Stem cells for cardiac repair: an introduction. J Geriatr Cardiol. 2013; 10: 186-97.
103. Sanganalmath SK, Bolli R. Cell therapy for heart failure: a comprehensive overview of experimental and clinical studies, current challenges, and future directions. Circ Res. 2013; 113: 810-34.
104. de Jong R, van Hout GP, Houtgraaf JH, et al. Intracoronary infusion of encapsulated glucagon-like Peptide-1-eluting mesenchymal stem cells preserves left ventricular function in a porcine model of acute myocardial infarction. Circ Cardiovasc Interv. 2014; 7: 673-83.
105. Behfar A, Crespo-Diaz R, Terzic A, et al. Cell therapy for cardiac repair-lessons from clinical trials. Nat Rev Cardiol. 2014; 11: 232-4.
106. Popescu LM, Gherghiceanu M, Kostin S, et al. Telocytes and heart renewing. In: Wang P, Kuo CH, Takeda N, Singal PK, editors. Adaptation biology and medicine, vol 6. Cell adaptations and challenges. New Delhi: Narosa; 2011. pp. 17-39.
107. 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.
108. Popescu LM, Manole E, Serboiu CS, et al. Identification of telocytes in skeletal muscle interstitium: implication for muscle regeneration. J Cell Mol Med. 2011; 15: 1379-92.
109. 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.
110. Popescu BO, Gherghiceanu M, Kostin S, et al. Telocytes in meninges and choroid plexus. Neurosci Lett. 2012; 516: 265-9.
111. 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.
112. Xiao J, Wang F, Liu Z, et al. Telocytes in liver: electron microscopic and immunofluorescent evidence. J Cell Mol Med. 2013; 17: 1537-42.
113. Wang F, Song Y, Bei Y, et al. Telocytes in liver regeneration: possible roles. J Cell Mol Med. 2014; 18: 1720-6.
114. Haines DD, Juhasz B, Tosaki A. Management of multicellular senescence and oxidative stress. J Cell Mol Med. 2013; 17: 936-57.