Suburothelial interstitial cells

Cells Tissues Organs

Volumn 199, Issue 1, 2014, Pages 59-72

  Rusu, Mugurel Constantin ^a,b   Folescu, Roxana ^d   Mənoiu, Vasile Sorin ^c   Didilescu, Andreea Cristiana ^b  

^a MEDCENTER Center of Excellence in Laboratory Medicine and Pathology   (United States)

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

^c NATIONAL INSTITUTE OF RESEARCH AND DEVELOPMENT FOR BIOLOGICAL SCIENCES   (Romania)

^d VICTOR BABES UNIVERSITY OF MEDICINE AND PHARMACY   (Romania)

Author keywords

Actin; Cell cell signaling; Myoid cells; Telocytes; Urinary bladder

Indexed keywords

ALPHA SMOOTH MUSCLE ACTIN; ACTIN;

ADULT; AGED; ANIMAL TISSUE; ARTICLE; AUTOPSY; BLADDER; BLADDER MUCOSA; BLADDER WALL; CELL POPULATION; CELL STRUCTURE; DETRUSOR MUSCLE; ELECTRON MICROSCOPY; FEMALE; FIBROBLAST; HUMAN; HUMAN TISSUE; IMMUNOHISTOCHEMISTRY; INTERSTITIAL CELL OF CAJAL; LEYDIG CELL; MALE; MYOFIBROBLAST; NONHUMAN; RAT; SMOOTH MUSCLE FIBER; TRANSMISSION ELECTRON MICROSCOPY; ANIMAL; CADAVER; CYTOLOGY; METABOLISM; MIDDLE AGED; WISTAR RAT;

MYOIDA;

ACTINS; AGED; ANIMALS; CADAVER; FEMALE; HUMANS; IMMUNOHISTOCHEMISTRY; INTERSTITIAL CELLS OF CAJAL; MALE; MICROSCOPY, ELECTRON, TRANSMISSION; MIDDLE AGED; RATS; RATS, WISTAR; URINARY BLADDER;

EID: 84908656150     PISSN: 14226405     EISSN: 14226421     Source Type: Journal    
DOI: 10.1159/000360816     Document Type: Article

References (78)

1. Cheng, S., F.P. Scigalla, P. Speroni di Fenizio, Z.G. Zhang, J.U. Stolzenburg, J. Neuhaus (2011a) ATP enhances spontaneous calcium activity in cultured suburothelial myofibroblasts of the human bladder. PLoS One 6: e25769.
2. Cheng, Y., K.J. Mansfield, S.L. Sandow, P. Sadananda, E. Burcher, K.H. Moore (2011b) Porcine bladder urothelial, myofibroblast, and detrusor muscle cells: characterization and ATP release. Front Pharmacol 2: 27.
3. Cretoiu, D., S.M. Cretoiu, A.A. Simionescu, L.M. Popescu (2012) Telocytes, a distinct type of cell among the stromal cells present in the lamina propria of jejunum. Histol Histopathol 27: 1067-1078.
4. Cunningham, R.M., P. Larkin, K.D. McCloskey (2011) Ultrastructural properties of interstitial cells of Cajal in the Guinea pig bladder. J Urol 185: 1123-1131.
5. Davidson, R.A., K.D. McCloskey (2005) Morphology and localization of interstitial cells in the guinea pig bladder: structural relationships with smooth muscle and neurons. J Urol 173: 1385-1390.
6. Drake, M.J., C.H. Fry, B. Eyden (2006) Structural characterization of myofibroblasts in the bladder. BJU Int 97: 29-32.
7. Duquette, R.A., A. Shmygol, C. Vaillant, A. Mobasheri, M. Pope, T. Burdyga, S. Wray (2005) Vimentin-positive, c-kit-negative interstitial cells in human and rat uterus: A role in pacemaking? Biol Reprod 72: 276-283.
8. Eyden, B. (2009) Are there myofibroblasts in normal bladder? Eur Urol 56: 427-429.
9. Eyden, B., A. Curry, G. Wang (2011) Stromal cells in the human gut show ultrastructural features of fibroblasts and smooth muscle cells but not myofibroblasts. J Cell Mol Med 15: 1483-1491.
10. Eyden, B.P. (1993) Brief review of the fibronexus and its significance for myofibroblastic differentiation and tumor diagnosis. Ultrastruct Pathol 17: 611-622.
11. Faussone-Pellegrini, M.S. (1987) Comparative study of interstitial cells of Cajal. Acta Anat (Basel) 130: 109-126.
12. Faussone-Pellegrini, M.S. (2005) Interstitial cells of Cajal: once negligible players, now blazing protagonists. Ital J Anat Embryol 110: 11-31.
13. Faussone-Pellegrini, M.S., L. Thuneberg (1999) Guide to the identification of interstitial cells of Cajal. Microsc Res Tech 47: 248-266.
14. Fry, C.H., G.P. Sui, A.J. Kanai, C. Wu (2007) The function of suburothelial myofibroblasts in the bladder. Neurourol Urodyn 26(6 suppl): 914-919.
15. Gevaert, T., R. De Vos, F. Van Der Aa, S. Joniau, J. van den Oord, T. Roskams, D. De Ridder (2012) Identification of telocytes in the upper lamina propria of the human urinary tract. J Cell Mol Med 16: 2085-2093.
16. Gherghiceanu, M., C.G. Manole, L.M. Popescu (2010) Telocytes in endocardium: electron microscope evidence. J Cell Mol Med 14: 2330-2334.
17. Gherghiceanu, M., L.M. Popescu (2011) Heterocellular communication in the heart: electron tomography of telocyte-myocyte junctions. J Cell Mol Med 15: 1005-1011.
18. Gherghiceanu, M., L.M. Popescu (2012) Cardiac telocytes - Their junctions and functional implications. Cell Tissue Res 348: 265-279.
19. Gillespie, J.I., M. Markerink-van Ittersum, J. de Vente (2004) cGMP-generating cells in the bladder wall: Identification of distinct networks of interstitial cells. BJU Int 94: 1114- 1124.
20. Grol, S., P.B. Essers, G.A. van Koeveringe, P. Martinez- Martinez, J. de Vente, J.I. Gillespie (2009) M(3) muscarinic receptor expression on suburothelial interstitial cells. BJU Int 104: 398-405.
21. Hashitani, H., Y. Yanai, H. Suzuki (2004) Role of interstitial cells and gap junctions in the transmission of spontaneous Ca2+ signals in detrusor smooth muscles of the guinea-pig urinary bladder. J Physiol 559(Pt 2): 567-581.
22. Heinrich, M., A. Oberbach, N. Schlichting, J.U. Stolzenburg, J. Neuhaus (2011) Cytokine effects on gap junction communication and connexin expression in human bladder smooth muscle cells and suburothelial myofibroblasts. PLoS One 6: e20792.
23. Hinescu, M.E., M. Gherghiceanu, E. Mandache, S.M. Ciontea, L.M. Popescu (2006) Interstitial Cajal-like cells (ICLC) in atrial myocardium: ultrastructural and immunohistochemical characterization. J Cell Mol Med 10: 243-257.
24. Hinescu, M.E., M. Gherghiceanu, L. Suciu, L.M. Popescu (2011) Telocytes in pleura: Two- And three-dimensional imaging by transmission electron microscopy. Cell Tissue Res 343: 389-397.
25. Hinescu, M.E., L.M. Popescu, M. Gherghiceanu, M.S. Faussone-Pellegrini (2008) Interstitial Cajal-like cells in rat mesentery: An ultrastructural and immunohistochemical approach. J Cell Mol Med 12: 260-270.
26. Huizinga, J.D., M.S. Faussone-Pellegrini (2005) About the presence of interstitial cells of Cajal outside the musculature of the gastrointestinal tract. J Cell Mol Med 9: 468-473.
27. Kim, S.O., B.S. Oh, I.Y. Chang, S.H. Song, K. Ahn, E.C. Hwang, K.J. Oh, D. Kwon, K. Park (2011) Distribution of interstitial cells of Cajal and expression of nitric oxide synthase after experimental bladder outlet obstruction in a rat model of bladder overactivity. Neurourol Urodyn 30: 1639-1645.
28. Komuro, T. (1999) Comparative morphology of interstitial cells of Cajal: ultrastructural characterization. Microsc Res Tech 47: 267-285.
29. Komuro, T., K. Seki, K. Horiguchi (1999) Ultrastructural characterization of the interstitial cells of Cajal. Arch Histol Cytol 62: 295-316.
30. Kostin, S. (2010) Myocardial telocytes: A specific new cellular entity. J Cell Mol Med 14: 1917- 1921.
31. Kubota, Y., H. Hashitani, N. Shirasawa, Y. Kojima, S. Sasaki, Y. Mabuchi, T. Soji, H. Suzuki, K. Kohri (2008) Altered distribution of interstitial cells in the guinea pig bladder following bladder outlet obstruction. Neurourol Urodyn 27: 330-340.
32. Kubota, Y., Y. Kojima, Y. Shibata, M. Imura, S. Sasaki, K. Kohri (2011) Role of KIT-positive interstitial cells of Cajal in the urinary bladder and possible therapeutic target for overactive bladder. Adv Urol 2011: 816342.
33. Kuijpers, K.A., J.P. Heesakkers, C.F. Jansen, J.A. Schalken (2007) Cadherin-11 is expressed in detrusor smooth muscle cells and myofibroblasts of normal human bladder. Eur Urol 52: 1213-1221.
34. Lagou, M., J. De Vente, T.B. Kirkwood, P. Hedlund, K.E. Andersson, J.I. Gillespie, M.J. Drake (2006) Location of interstitial cells and neurotransmitters in the mouse bladder. BJU Int 97: 1332-1337.
35. McCloskey, K.D. (2010) Interstitial cells in the urinary bladder - localization and function. Neurourol Urodyn 29: 82-87.
36. McHale, N.G., M.A. Hollywood, G.P. Sergeant, M. Shafei, K.T. Thornbury, S.M. Ward (2006) Organization and function of ICC in the urinary tract. J Physiol 576(Pt 3): 689-694.
37. Mei, F., J. Han, Y. Huang, Z.Y. Jiang, C.J. Xiong, D.S. Zhou (2009) Plasticity of interstitial cells of Cajal: A study in the small intestine of adult guinea pigs. Anat Rec (Hoboken) 292: 985- 993.
38. Min, K.W., I. Sook Seo (2003) Interstitial cells of Cajal in the human small intestine: Immunochemical and ultrastructural study. Ultrastruct Pathol 27: 67-78.
39. Neuhaus, J., M. Heinrich, N. Schlichting, A. Oberbach, G. Fitzl, T. Schwalenberg, L.C. Horn, J.U. Stolzenburg (2007) Structure and function of suburothelial myofibroblasts in the human urinary bladder under normal and pathological conditions (in German). Urologe A 46: 1197-1202.
40. Neuhaus, J., U. Scholler, K. Freick, T. Schwalenberg, M. Heinrich, L.C. Horn, J.U. Stolzenburg (2008) Myofibroblasts and afferent signalling in the urinary bladder. A concept (in German). Urologe A 47: 1085-1086, 1088- 1090.
41. Nicolescu, M.I., A. Bucur, O. Dinca, M.C. Rusu, L.M. Popescu (2012) Telocytes in parotid glands. Anat Rec (Hoboken) 295: 378-385.
42. Nicolescu, M.I., L.M. Popescu (2012) Telocytes in the interstitium of human exocrine pancreas: ultrastructural evidence. Pancreas 41: 949- 956.
43. Popescu, L.M., S.M. Ciontea, D. Cretoiu (2007) Interstitial Cajal-like cells in human uterus and fallopian tube. Ann NY Acad Sci 1101: 139-165.
44. Popescu, L.M., M.S. Faussone-Pellegrini (2010) 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 14: 729-740.
45. Popescu, L.M., M. Gherghiceanu, M.E. Hinescu, D. Cretoiu, L. Ceafalan, T. Regalia, A.C. Popescu, C. Ardeleanu, E. Mandache (2006) Insights into the interstitium of ventricular myocardium: Interstitial Cajal-like cells (ICLC). J Cell Mol Med 10: 429-458.
46. Popescu, L.M., M. Gherghiceanu, L.C. Suciu, C.G. Manole, M.E. Hinescu (2011) Telocytes and putative stem cells in the lungs: electron microscopy, electron tomography and laser scanning microscopy. Cell Tissue Res 345: 391-403.
47. Popescu, L.M., C.G. Manole, M. Gherghiceanu, A. Ardelean, M.I. Nicolescu, M.E. Hinescu, S. Kostin (2010) Telocytes in human epicardium. J Cell Mol Med 14: 2085-2093.
48. Rasmussen, H., J.J. Rumessen, A. Hansen, F. Smedts, T. Horn (2009) Ultrastructure of Cajal-like interstitial cells in the human detrusor. Cell Tissue Res 335: 517-527.
49. Roosen, A., S.N. Datta, R.A. Chowdhury, P.M. Patel, V. Kalsi, S. Elneil, P. Dasgupta, T.M. Kessler, S. Khan, J. Panicker, C.H. Fry, S. Brandner, C.J. Fowler, A. Apostolidis (2009) Suburothelial myofibroblasts in the human overactive bladder and the effect of botulinum neurotoxin type A treatment. Eur Urol 55: 1440-1448.
50. Rumessen, J.J., H.B. Mikkelsen, K. Qvortrup, L. Thuneberg (1993) Ultrastructure of interstitial cells of Cajal in circular muscle of human small intestine. Gastroenterology 104: 343- 350.
51. Rumessen, J.J., H.B. Mikkelsen, L. Thuneberg (1992) Ultrastructure of interstitial cells of Cajal associated with deep muscular plexus of human small intestine. Gastroenterology 102: 56-68.
52. Rumessen, J.J., L. Thuneberg (1991) Interstitial cells of Cajal in human small intestine. Ultrastructural identification and organization between the main smooth muscle layers. Gastroenterology 100(5 Pt 1): 1417-1431.
53. Rumessen, J.J., L. Thuneberg (1996) Pacemaker cells in the gastrointestinal tract: Interstitial cells of Cajal. Scand J Gastroenterol Suppl 216: 82-94.
54. Rumessen, J.J., J.M. Vanderwinden, A. Hansen, T. Horn (2013) Ultrastructure of interstitial cells in subserosa of human colon. Cells Tissues Organs 197: 322-332.
55. Rumessen, J.J., J.M. Vanderwinden, H. Rasmussen, A. Hansen, T. Horn (2009) Ultrastructure of interstitial cells of Cajal in myenteric plexus of human colon. Cell Tissue Res 337: 197-212.
56. Rusu, M.C., A.M. Jianu, N. Mirancea, A.C. Didilescu, V.S. Manoiu, D. Paduraru (2012a) Tracheal telocytes. J Cell Mol Med 16: 401-405.
57. Rusu, M.C., A.M. Jianu, F. Pop, S. Hostiuc, R. Leonardi, G.C. Curca (2012b) Immunolocalization of 200 kDa neurofilaments in human cardiac endothelial cells. Acta Histochem 114: 842-845.
58. Rusu, M.C., C. Loreto, V.S. Manoiu (2014) Network of telocytes in the temporomandibular joint disc of rats. Acta Histochem, DOI: 10.1016/j.acthis.2013.12.005.
59. Rusu, M.C., N. Mirancea, V.S. Manoiu, M. Valcu, M.I. Nicolescu, D. Paduraru (2012c) Skin telocytes. Ann Anat 194: 359-367.
60. Rusu, M.C., M.I. Nicolescu, A.M. Jianu, R. Lighezan, V.S. Manoiu, D. Paduraru (2012d) Esophageal telocytes and hybrid morphologies. Cell Biol Int 36: 1079-1088.
61. Rusu, M.C., F. Pop, S. Hostiuc, G.C. Curca, A.M. Jianu, D. Paduraru (2012e) Telocytes form networks in normal cardiac tissues. Histol Histopathol 27: 807-816.
62. Sadananda, P., R. Chess-Williams, E. Burcher (2008) Contractile properties of the pig bladder mucosa in response to neurokinin A: A role for myofibroblasts? Br J Pharmacol 153: 1465-1473.
63. Sanders, K.M. (2006) Interstitial cells of Cajal at the clinical and scientific interface. J Physiol 576(Pt 3): 683-687.
64. Smet, P.J., J. Jonavicius, V.R. Marshall, J. de Vente (1996) Distribution of nitric oxide synthase- immunoreactive nerves and identification of the cellular targets of nitric oxide in guinea-pig and human urinary bladder by cGMP immunohistochemistry. Neuroscience 71: 337-348.
65. Smeulders, N., A.S. Woolf, D.T. Wilcox (2002) Smooth muscle differentiation and cell turnover in mouse detrusor development. J Urol 167: 385-390.
66. Suciu, L., L.M. Popescu, M. Gherghiceanu, T. Regalia, M.I. Nicolescu, M.E. Hinescu, M.S. Faussone-Pellegrini (2010) Telocytes in human term placenta: morphology and phenotype. Cells Tissues Organs 192: 325-339.
67. Sui, G.P., S. Rothery, E. Dupont, C.H. Fry, N.J. Severs (2002) Gap junctions and connexin expression in human suburothelial interstitial cells. BJU Int 90: 118-129.
68. Sui, G.P., C. Wu, C.H. Fry (2006) Characterization of the purinergic receptor subtype on guinea-pig suburothelial myofibroblasts. BJU Int 97: 1327-1331.
69. Sui, G.P., C. Wu, A. Roosen, Y. Ikeda, A.J. Kanai, C.H. Fry (2008) Modulation of bladder myofibroblast activity: Implications for bladder function. Am J Physiol Renal Physiol 295: F688-F697.
70. Timmermans, J.P. (2001) Interstitial cells of Cajal: Is their role in gastrointestinal function in view of therapeutic perspectives underestimated or exaggerated? Folia Morphol (Warsz) 60: 1-9.
71. Vanderwinden, J.M., J.J. Rumessen, F. Bernex, S.N. Schiffmann, J.J. Panthier (2000) Distribution and ultrastructure of interstitial cells of Cajal in the mouse colon, using antibodies to Kit and Kit(W-lacZ) mice. Cell Tissue Res 302: 155-170.
72. Wiseman, O.J., C.J. Fowler, D.N. Landon (2003) The role of the human bladder lamina propria myofibroblast. BJU Int 91: 89-93.
73. Wu, C., G.P. Sui, C.H. Fry (2004) Purinergic regulation of guinea pig suburothelial myofibroblasts. J Physiol 559(Pt 1): 231-243.
74. Xue, L., Y. Li, X. Han, L. Yao, J. Yuan, W. Qin, F. Liu, H. Wang (2012) Investigation of hyperpolarization- Activated cyclic nucleotide-gated channels in interstitial cells of Cajal of human bladder. Urology 80: 224.e13-224.e18.
75. Zhang, J., M.W. Hess, M. Thurnher, A. Hobisch, C. Radmayr, M.V. Cronauer, A. Hittmair, Z. Culig, G. Bartsch, H. Klocker (1997) Human prostatic smooth muscle cells in culture: estradiol enhances expression of smooth muscle cell-specific markers. Prostate 30: 117- 129.
76. Zheng, Y., C. Bai, X. Wang (2012a) Telocyte morphologies and potential roles in diseases. J Cell Physiol 227: 2311-2317.
77. Zheng, Y., H. Li, C.G. Manole, A. Sun, J. Ge, X. Wang (2011) Telocytes in trachea and lungs. J Cell Mol Med 15: 2262-2268.
78. Zheng, Y., T. Zhu, M. Lin, D. Wu, X. Wang (2012b) Telocytes in the urinary system. J Transl Med 10: 188.