Functional Vascular Smooth Muscle-like Cells Derived from Adult Mouse Uterine Mesothelial Cells

PLoS ONE

Volumn 8, Issue 2, 2013, Pages

  Lachaud, Christian Claude ^a   Pezzolla, Daniela ^a   Domínguez Rodríguez, Alejandro ^b   Smani, Tarik ^b   Soria, Bernat ^a,c   Hmadcha, Abdelkrim ^a,c  

^a CABIMER Andalusian Center for Molecular Biology and Regenerative Medicine CSIC University of Seville UPO   (Spain)

^b Instituto de Biomedicina de Sevilla   (Spain)

^c INSTITUTO DE SALUD CARLOS III   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA ACTININ; ALPHA SMOOTH MUSCLE ACTIN; ATRIAL NATRIURETIC FACTOR; BETA CATENIN; BETA1 INTEGRIN; BONE MORPHOGENETIC PROTEIN 2; BONE MORPHOGENETIC PROTEIN 4; CALDESMON; CALPONIN; CYTOKERATIN 18; DESMIN; INTERCELLULAR ADHESION MOLECULE 1; NESTIN; PROTEIN ZO1; SMOOTHELIN; STEM CELL FACTOR RECEPTOR; TRANSCRIPTION FACTOR GATA 4; TRANSCRIPTION FACTOR NANOG; TRANSCRIPTION FACTOR SLUG; TRANSCRIPTION FACTOR SNAIL; TRANSCRIPTION FACTOR SOX2; TRANSCRIPTION FACTOR TWIST; TRANSGELIN; TROPONIN T; UVOMORULIN; BIOLOGICAL MARKER; CADHERIN; CALCIUM; CELL SURFACE RECEPTOR; ENDOTHELIN RECEPTOR; MUSCLE PROTEIN; TRYPSIN;

ANIMAL CELL; ANIMAL CELL CULTURE; ARTICLE; CELL DIFFERENTIATION; CELL FUNCTION; CELL MATURATION; CELL POPULATION; CELL TRANSDIFFERENTIATION; CONTROLLED STUDY; EPITHELIAL MESENCHYMAL TRANSITION; FEMALE; IMMUNOPHENOTYPING; IN VITRO STUDY; MESOTHELIUM CELL; MOUSE; NONHUMAN; PROTEIN EXPRESSION; RAT; VASCULAR SMOOTH MUSCLE; ANIMAL; METABOLISM; MUSCLE CONTRACTION; PHYSIOLOGY; SMOOTH MUSCLE FIBER; UTERUS; WISTAR RAT;

ANIMALS; ANTIGENS, CD29; BETA CATENIN; BIOLOGICAL MARKERS; CADHERINS; CALCIUM; CELL DIFFERENTIATION; EPITHELIAL-MESENCHYMAL TRANSITION; FEMALE; INTERCELLULAR ADHESION MOLECULE-1; MICE; MUSCLE CONTRACTION; MUSCLE PROTEINS; MUSCLE, SMOOTH, VASCULAR; MYOCYTES, SMOOTH MUSCLE; RATS; RATS, WISTAR; RECEPTORS, CELL SURFACE; RECEPTORS, ENDOTHELIN; TRYPSIN; UTERUS; ZONULA OCCLUDENS-1 PROTEIN;

EID: 84873564358     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0055181     Document Type: Article

References (68)

1. Mutsaers SE, Wilkosz S, (2007) Structure and function of mesothelial cells. Cancer Treat Res 134: 1-19.
2. Thiery JP, Acloque H, Huang RY, Nieto MA, (2009) Epithelial-mesenchymal transitions in development and disease. Cell 139: 871-890.
3. Dettman RW, Denetclaw W Jr, Ordahl CP, Bristow J, (1998) Common epicardial origin of coronary vascular smooth muscle, perivascular fibroblasts, and intermyocardial fibroblasts in the avian heart. Dev Biol 193: 169-181.
4. Mikawa T, Gourdie RG, (1996) Pericardial mesoderm generates a population of coronary smooth muscle cells migrating into the heart along with ingrowth of the epicardial organ. Dev Biol 174: 221-232.
5. Hungerford JE, Little CD, (1999) Developmental biology of the vascular smooth muscle cell: building a multilayered vessel wall. J Vasc Res 36: 2-27.
6. Zhou B, Ma Q, Rajagopal S, Wu SM, Domian I, et al. (2008) Epicardial progenitors contribute to the cardiomyocyte lineage in the developing heart. Nature 454: 109-113.
7. Cai CL, Martin JC, Sun Y, Cui L, Wang L, et al. (2008) A myocardial lineage derives from Tbx18 epicardial cells. Nature 454: 104-108.
8. Wilm B, Ipenberg A, Hastie ND, Burch JB, Bader DM, (2005) The serosal mesothelium is a major source of smooth muscle cells of the gut vasculature. Development 132: 5317-5328.
9. Que J, Wilm B, Hasegawa H, Wang F, Bader D, et al. (2008) Mesothelium contributes to vascular smooth muscle and mesenchyme during lung development. Proc Natl Acad Sci U S A 105: 16626-16630.
10. Asahina K, Zhou B, Pu WT, Tsukamoto H, (2011) Septum transversum-derived mesothelium gives rise to hepatic stellate cells and perivascular mesenchymal cells in developing mouse liver. Hepatology 53: 983-995.
11. Aroeira LS, Aguilera A, Sanchez-Tomero JA, Bajo MA, del Peso G, et al. (2007) Epithelial to mesenchymal transition and peritoneal membrane failure in peritoneal dialysis patients: pathologic significance and potential therapeutic interventions. J Am Soc Nephrol 18: 2004-2013.
12. Yanez-Mo M, Lara-Pezzi E, Selgas R, Ramirez-Huesca M, Dominguez-Jimenez C, et al. (2003) Peritoneal dialysis and epithelial-to-mesenchymal transition of mesothelial cells. N Engl J Med 348: 403-413.
13. Margetts PJ, Bonniaud P, Liu L, Hoff CM, Holmes CJ, et al. (2005) Transient overexpression of TGF-{beta}1 induces epithelial mesenchymal transition in the rodent peritoneum. J Am Soc Nephrol 16: 425-436.
14. van Tuyn J, Atsma DE, Winter EM, van der Velde-van Dijke I, Pijnappels DA, et al. (2007) Epicardial cells of human adults can undergo an epithelial-to-mesenchymal transition and obtain characteristics of smooth muscle cells in vitro. Stem Cells 25: 271-278.
15. Kawaguchi M, Bader DM, Wilm B, (2007) Serosal mesothelium retains vasculogenic potential. Dev Dyn 236: 2973-2979.
16. Wada AM, Smith TK, Osler ME, Reese DE, Bader DM, (2003) Epicardial/Mesothelial cell line retains vasculogenic potential of embryonic epicardium. Circ Res 92: 525-531.
17. Liu Q, Mao H, Nie J, Chen W, Yang Q, et al. (2008) Transforming growth factor {beta}1 induces epithelial-mesenchymal transition by activating the JNK-Smad3 pathway in rat peritoneal mesothelial cells. Perit Dial Int 28Suppl 3: S88-95.
18. Nasreen N, Mohammed KA, Mubarak KK, Baz MA, Akindipe OA, et al. (2009) Pleural mesothelial cell transformation into myofibroblasts and haptotactic migration in response to TGF-beta1 in vitro. Am J Physiol Lung Cell Mol Physiol 297: L115-124.
19. Patel P, West-Mays J, Kolb M, Rodrigues JC, Hoff CM, et al. (2010) Platelet derived growth factor B and epithelial mesenchymal transition of peritoneal mesothelial cells. Matrix Biol 29: 97-106.
20. Patel P, Sekiguchi Y, Oh KH, Patterson SE, Kolb MR, et al. (2010) Smad3-dependent and-independent pathways are involved in peritoneal membrane injury. Kidney Int 77: 319-328.
21. Brown DJ, Rzucidlo EM, Merenick BL, Wagner RJ, Martin KA, et al. (2005) Endothelial cell activation of the smooth muscle cell phosphoinositide 3-kinase/Akt pathway promotes differentiation. J Vasc Surg 41: 509-516.
22. Sinha S, Hoofnagle MH, Kingston PA, McCanna ME, Owens GK, (2004) Transforming growth factor-beta1 signaling contributes to development of smooth muscle cells from embryonic stem cells. Am J Physiol Cell Physiol 287: C1560-1568.
23. Yang AH, Chen JY, Lin JK, (2003) Myofibroblastic conversion of mesothelial cells. Kidney Int 63: 1530-1539.
24. Gan Q, Yoshida T, Li J, Owens GK, (2007) Smooth muscle cells and myofibroblasts use distinct transcriptional mechanisms for smooth muscle alpha-actin expression. Circ Res 101: 883-892.
25. Chiavegato A, Roelofs M, Franch R, Castellucci E, Sarinella F, et al. (1999) Differential expression of SM22 isoforms in myofibroblasts and smooth muscle cells from rabbit bladder. J Muscle Res Cell Motil 20: 133-146.
26. Matsubara D, Morikawa T, Goto A, Nakajima J, Fukayama M, et al. (2009) Subepithelial myofibroblast in lung adenocarcinoma: a histological indicator of excellent prognosis. Mod Pathol 22: 776-785.
27. Owens GK, Kumar MS, Wamhoff BR, (2004) Molecular regulation of vascular smooth muscle cell differentiation in development and disease. Physiol Rev 84: 767-801.
28. Chamley-Campbell J, Campbell GR, Ross R, (1979) The smooth muscle cell in culture. Physiol Rev 59: 1-61.
29. Oishi K, Itoh Y, Isshiki Y, Kai C, Takeda Y, et al. (2000) Agonist-induced isometric contraction of smooth muscle cell-populated collagen gel fiber. Am J Physiol Cell Physiol 279: C1432-1442.
30. Boselli C, Govoni S, Vicini D, Lanni C, Racchi M, et al. (2002) Presence and passage dependent loss of biochemical M3 muscarinic receptor function in human detrusor cultured smooth muscle cells. J Urol 168: 2672-2676.
31. Council L, Hameed O, (2009) Differential expression of immunohistochemical markers in bladder smooth muscle and myofibroblasts, and the potential utility of desmin, smoothelin, and vimentin in staging of bladder carcinoma. Mod Pathol 22: 639-650.
32. Qiu X, Montgomery E, Sun B, (2008) Inflammatory myofibroblastic tumor and low-grade myofibroblastic sarcoma: a comparative study of clinicopathologic features and further observations on the immunohistochemical profile of myofibroblasts. Hum Pathol 39: 846-856.
33. Ceballos KM, Nielsen GP, Selig MK, O'Connell JX, (2000) Is anti-h-caldesmon useful for distinguishing smooth muscle and myofibroblastic tumors? An immunohistochemical study. Am J Clin Pathol 114: 746-753.
34. van Eys GJ, Niessen PM, Rensen SS, (2007) Smoothelin in vascular smooth muscle cells. Trends Cardiovasc Med 17: 26-30.
35. Rensen SS, Niessen PM, van Deursen JM, Janssen BJ, Heijman E, et al. (2008) Smoothelin-B deficiency results in reduced arterial contractility, hypertension, and cardiac hypertrophy in mice. Circulation 118: 828-836.
36. Jain M, He Q, Lee WS, Kashiki S, Foster LC, et al. (1996) Role of CD44 in the reaction of vascular smooth muscle cells to arterial wall injury. J Clin Invest 98: 877.
37. Comin CE, Saieva C, Messerini L, (2007) h-caldesmon, calretinin, estrogen receptor, and Ber-EP4: a useful combination of immunohistochemical markers for differentiating epithelioid peritoneal mesothelioma from serous papillary carcinoma of the ovary. Am J Surg Pathol 31: 1139-1148.
38. Deruiter MC, Rensen SS, Coolen GP, Hierck BP, Bergwerff M, et al. (2001) Smoothelin expression during chicken embryogenesis: detection of an embryonic isoform. Dev Dyn 221: 460-463.
39. Pikkarainen S, Tokola H, Kerkela R, Ruskoaho H, (2004) GATA transcription factors in the developing and adult heart. Cardiovasc Res 63: 196-207.
40. Cai CL, Liang X, Shi Y, Chu PH, Pfaff SL, et al. (2003) Isl1 identifies a cardiac progenitor population that proliferates prior to differentiation and contributes a majority of cells to the heart. Dev Cell 5: 877-889.
41. Moretti A, Caron L, Nakano A, Lam JT, Bernshausen A, et al. (2006) Multipotent embryonic isl1+ progenitor cells lead to cardiac, smooth muscle, and endothelial cell diversification. Cell 127: 1151-1165.
42. Sun Y, Liang X, Najafi N, Cass M, Lin L, et al. (2007) Islet 1 is expressed in distinct cardiovascular lineages, including pacemaker and coronary vascular cells. Dev Biol 304: 286-296.
43. Laugwitz KL, Moretti A, Lam J, Gruber P, Chen Y, et al. (2005) Postnatal isl1+ cardioblasts enter fully differentiated cardiomyocyte lineages. Nature 433: 647-653.
44. Schlueter J, Manner J, Brand T, (2006) BMP is an important regulator of proepicardial identity in the chick embryo. Dev Biol 295: 546-558.
45. Liu J, Stainier DY, (2010) Tbx5 and Bmp signaling are essential for proepicardium specification in zebrafish. Circ Res 106: 1818-1828.
46. Wang J, Greene SB, Bonilla-Claudio M, Tao Y, Zhang J, et al. (2010) Bmp signaling regulates myocardial differentiation from cardiac progenitors through a MicroRNA-mediated mechanism. Dev Cell 19: 903-912.
47. Hegde SS, Choppin A, Bonhaus D, Briaud S, Loeb M, et al. (1997) Functional role of M2 and M3 muscarinic receptors in the urinary bladder of rats in vitro and in vivo. Br J Pharmacol 120: 1409-1418.
48. Kim MR, Jeon ES, Kim YM, Lee JS, Kim JH, (2009) Thromboxane a(2) induces differentiation of human mesenchymal stem cells to smooth muscle-like cells. Stem Cells 27: 191-199.
49. Masaki T, (2004) Historical review: Endothelin. Trends Pharmacol Sci 25: 219-224.
50. Ahmed N, Maines-Bandiera S, Quinn MA, Unger WG, Dedhar S, et al. (2006) Molecular pathways regulating EGF-induced epithelio-mesenchymal transition in human ovarian surface epithelium. Am J Physiol Cell Physiol 290: C1532-1542.
51. Katsara O, Mahaira LG, Iliopoulou EG, Moustaki A, Antsaklis A, et al. (2011) Effects of donor age, gender, and in vitro cellular aging on the phenotypic, functional, and molecular characteristics of mouse bone marrow-derived mesenchymal stem cells. Stem Cells Dev 20: 1549-1561.
52. Pacini S, Carnicelli V, Trombi L, Montali M, Fazzi R, et al. (2010) Constitutive expression of pluripotency-associated genes in mesodermal progenitor cells (MPCs). PLoS One 5: e9861.
53. Kong D, Banerjee S, Ahmad A, Li Y, Wang Z, et al. (2010) Epithelial to mesenchymal transition is mechanistically linked with stem cell signatures in prostate cancer cells. PLoS One 5: e12445.
54. Pirozzi G, Tirino V, Camerlingo R, Franco R, La Rocca A, et al. (2011) Epithelial to mesenchymal transition by TGFbeta-1 induction increases stemness characteristics in primary non small cell lung cancer cell line. PLoS One 6: e21548.
55. Ijpenberg A, Perez-Pomares JM, Guadix JA, Carmona R, Portillo-Sanchez V, et al. (2007) Wt1 and retinoic acid signaling are essential for stellate cell development and liver morphogenesis. Dev Biol 312: 157-170.
56. Martinez-Estrada OM, Lettice LA, Essafi A, Guadix JA, Slight J, et al. (2010) Wt1 is required for cardiovascular progenitor cell formation through transcriptional control of Snail and E-cadherin. Nat Genet 42: 89-93.
57. Oikawa H, Hayashi K, Maesawa C, Masuda T, Sobue K, (2010) Expression profiles of nestin in vascular smooth muscle cells in vivo and in vitro. Exp Cell Res 316: 940-950.
58. Mutsaers SE, McAnulty RJ, Laurent GJ, Versnel MA, Whitaker D, et al. (1997) Cytokine regulation of mesothelial cell proliferation in vitro and in vivo. Eur J Cell Biol 72: 24-29.
59. Kim J, Wu Q, Zhang Y, Wiens KM, Huang Y, et al. (2010) PDGF signaling is required for epicardial function and blood vessel formation in regenerating zebrafish hearts. Proc Natl Acad Sci U S A 107: 17206-17210.
60. Mellgren AM, Smith CL, Olsen GS, Eskiocak B, Zhou B, et al. (2008) Platelet-derived growth factor receptor beta signaling is required for efficient epicardial cell migration and development of two distinct coronary vascular smooth muscle cell populations. Circ Res 103: 1393-1401.
61. Smith CL, Baek ST, Sung CY, Tallquist MD, (2011) Epicardial-derived cell epithelial-to-mesenchymal transition and fate specification require PDGF receptor signaling. Circ Res 108: e15-26.
62. Wang Z, Wang DZ, Pipes GC, Olson EN, (2003) Myocardin is a master regulator of smooth muscle gene expression. Proc Natl Acad Sci U S A 100: 7129-7134.
63. Chen YL, Shepherd C, Spinelli W, Lai FM, (1999) Oxytocin and vasopressin constrict rat isolated uterine resistance arteries by activating vasopressin V1A receptors. Eur J Pharmacol 376: 45-51.
64. Vedernikov YP, Betancourt A, Wentz MJ, Saade GR, Garfield RE, (2006) Adaptation to pregnancy leads to attenuated rat uterine artery smooth muscle sensitivity to oxytocin. Am J Obstet Gynecol 194: 252-260.
65. Jankowski M, Wang D, Hajjar F, Mukaddam-Daher S, McCann SM, et al. (2000) Oxytocin and its receptors are synthesized in the rat vasculature. Proc Natl Acad Sci U S A 97: 6207-6211.
66. Fukuroda T, Ozaki S, Ihara M, Ishikawa K, Yano M, et al. (1994) Synergistic inhibition by BQ-123 and BQ-788 of endothelin-1-induced contractions of the rabbit pulmonary artery. Br J Pharmacol 113: 336-338.
67. Smani T, Zakharov SI, Csutora P, Leno E, Trepakova ES, et al. (2004) A novel mechanism for the store-operated calcium influx pathway. Nat Cell Biol 6: 113-120.
68. Smani T, Dominguez-Rodriguez A, Hmadcha A, Calderon-Sanchez E, Horrillo-Ledesma A, et al. (2007) Role of Ca2+-independent phospholipase A2 and store-operated pathway in urocortin-induced vasodilatation of rat coronary artery. Circ Res 101: 1194-1203.