Differentiated markers in undifferentiated cells: Expression of smooth muscle contractile proteins in multipotent bone marrow mesenchymal stem cells

Development Growth and Differentiation

Volumn 55, Issue 5, 2013, Pages 591-605

  Liu, Yingxi ^a   Deng, Bingqing ^a   Zhao, Yong ^a   Xie, Shuanglun ^a   Nie, Ruqiong ^a  

^a SUN YAT SEN UNIVERSITY   (China)

Author keywords

Calponin; Differentiation; Mesenchymal stem cell; Smooth muscle cells; Smooth muscle contractile proteins

Indexed keywords

ACTIN; ALPHA SMOOTH MUSCLE ACTIN; CALPONIN; DESMIN; H1 CALPONIN; ISOPROTEIN; PROTEIN; SMOOTH MUSCLE MYOSIN HEAVY CHAIN; UNCLASSIFIED DRUG;

ACTIN FILAMENT; ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; CELL DIFFERENTIATION; CELL FUNCTION; CELL LINE; CELL STRUCTURE; CONTROLLED STUDY; HEMATOPOIETIC STEM CELL; MESENCHYMAL STEM CELL; NONHUMAN; NUCLEOTIDE SEQUENCE; PHENOTYPE; PROTEIN EXPRESSION; RAT; SIGNAL TRANSDUCTION; SMOOTH MUSCLE FIBER; UPREGULATION;

ACTINS; ADIPOCYTES; ANIMALS; BIOLOGICAL MARKERS; BLOTTING, WESTERN; BONE MARROW CELLS; CALCIUM-BINDING PROTEINS; CELL DIFFERENTIATION; CELLS, CULTURED; CHONDROCYTES; DESMIN; GENE EXPRESSION; MESENCHYMAL STROMAL CELLS; MICROFILAMENT PROTEINS; MULTIPOTENT STEM CELLS; MUSCLE PROTEINS; MYOCYTES, SMOOTH MUSCLE; MYOSIN HEAVY CHAINS; OSTEOBLASTS; RATS; RATS, SPRAGUE-DAWLEY; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION;

EID: 84879284174     PISSN: 00121592     EISSN: 1440169X     Source Type: Journal    
DOI: 10.1111/dgd.12052     Document Type: Article

References (49)

1. Appel, S., Allen, P. G., Vetterkind, S., Jin, J. P. & Morgan, K. G. 2010. h3/Acidic calponin: an actin-binding protein that controls extracellular signal-regulated kinase 1/2 activity in nonmuscle cells. Mol. Biol. Cell 21, 1409-22.
2. Ball, S. G., Shuttleworth, A. C. & Kielty, C. M. 2004. Direct cell contact influences bone marrow mesenchymal stem cell fate. Int. J. Biochem. Cell Biol. 36, 714-27.
3. Barja, F., Coughlin, C., Belin, D. & Gabbiani, G. 1986. Actin isoform synthesis and mRNA levels in quiescent and proliferating rat aortic smooth muscle cells in vivo and in vitro. Lab. Invest. 55, 226-33.
4. Burkhard, K., Smith, S., Deshmukh, R., MacKerell, A. D. Jr. & Shapiro, P. 2009. Development of extracellular signal-regulated kinase inhibitors. Curr. Top. Med. Chem. 9, 678-89.
5. Capetanaki, Y., Milner, D. J. & Weitzer, G. 1997. Desmin in muscle formation and maintenance: knockouts and consequences. Cell Struct. Funct. 22, 103-16.
6. Caplice, N. M., Bunch, T. J., Stalboerger, P. G., Wang, S., Simper, D., Miller, D. V., Russell, S. J., Litzow, M. R. & Edwards, W. D. 2003. Smooth muscle cells in human coronary atherosclerosis can originate from cells administered at marrow transplantation. Proc. Natl. Acad. Sci. USA 100, 4754-9.
7. Chamley-Campbell, J., Campbell, G. R. & Ross, R. 1979. The smooth muscle cell in culture. Physiol. Rev. 59, 1-61.
8. Frid, M. G., Shekhonin, B. V., Koteliansky, V. E. & Glukhova, M. A. 1992. Phenotypic changes of human smooth muscle cells during development: late expression of heavy caldesmon and calponin. Dev. Biol. 153, 185-93.
9. Gojo, S., Gojo, N., Takeda, Y., Mori, T., Abe, H., Kyo, S., Hata, J. & Umezawa, A. 2003. In vivo cardiovasculogenesis by direct injection of isolated adult mesenchymal stem cells. Exp. Cell Res. 288, 51-9.
10. Hegner, B., Weber, M., Dragun, D. & Schulze-Lohoff, E. 2005. Differential regulation of smooth muscle markers in human bone marrow-derived mesenchymal stem cells. J. Hypertens. 23, 1191-202.
11. Hillebrands, J. L., Klatter, F. A., van den Hurk, B. M., Popa, E. R., Nieuwenhuis, P. & Rozing, J. 2001. Origin of neointimal endothelium and alpha-actin-positive smooth muscle cells in transplant arteriosclerosis. J. Clin. Invest. 107, 1411-22.
12. Hossain, M. M., Hwang, D. Y., Huang, Q. Q., Sasaki, Y. & Jin, J. P. 2003. Developmentally regulated expression of calponin isoforms and the effect of h2-calponin on cell proliferation. Am. J. Physiol. Cell Physiol. 284, C156-67.
13. Hossain, M. M., Smith, P. G., Wu, K. & Jin, J. P. 2006. Cytoskeletal tension regulates both expression and degradation of h2-calponin in lung alveolar cells. Biochemistry 45, 15670-83.
14. Jimenez, M., Daret, D., Choussat, A. & Bonnet, J. 1999. Immunohistological and ultrastructural analysis of the intimal thickening in coarctation of human aorta. Cardiovasc. Res. 41, 737-45.
15. Kanematsu, A., Yamamoto, S., Iwai-Kanai, E., Kanatani, I., Imamura, M., Adam, R. M., Tabata, Y. & Ogawa, O. 2005. Induction of smooth muscle cell-like phenotype in marrow-derived cells among regenerating urinary bladder smooth muscle cells. Am. J. Pathol. 166, 565-73.
16. Kasper, G., Mao, L., Geissler, S., Draycheva, A., Trippens, J., Kuhnisch, J., Tschirschmann, M., Kaspar, K., Perka, C., Duda, G. N. & Klose, J. 2009. Insights into mesenchymal stem cell aging: involvement of antioxidant defense and actin cytoskeleton. Stem Cells 27, 1288-97.
17. Kim, M. R., Jeon, E. S., Kim, Y. M., Lee, J. S. & Kim, J. H. 2009. Thromboxane a(2) induces differentiation of human mesenchymal stem cells to smooth muscle-like cells. Stem Cells 27, 191-9.
18. Kurpinski, K., Chu, J., Hashi, C. & Li, S. 2006. Anisotropic mechanosensing by mesenchymal stem cells. Proc. Natl Acad. Sci. USA 103, 16095-100.
19. Kurpinski, K., Lam, H., Chu, J., Wang, A., Kim, A., Tsay, E., Agrawal, S., Schaffer, D. V. & Li, S. 2010. Transforming growth factor-beta and notch signaling mediate stem cell differentiation into smooth muscle cells. Stem Cells 28, 734-42.
20. Leinweber, B., Parissenti, A. M., Gallant, C., Gangopadhyay, S. S., Kirwan-Rhude, A., Leavis, P. C. & Morgan, K. G. 2000. Regulation of protein kinase C by the cytoskeletal protein calponin. J. Biol. Chem. 275, 40329-36.
21. Leinweber, B. D., Leavis, P. C., Grabarek, Z., Wang, C. L. & Morgan, K. G. 1999. Extracellular regulated kinase (ERK) interaction with actin and the calponin homology (CH) domain of actin-binding proteins. Biochem. J. 344(Pt 1), 117-23.
22. Madsen, C. S., Regan, C. P., Hungerford, J. E., White, S. L., Manabe, I. & Owens, G. K. 1998. Smooth muscle-specific expression of the smooth muscle myosin heavy chain gene in transgenic mice requires 5′-flanking and first intronic DNA sequence. Circ. Res. 82, 908-17.
23. Matsumura, G., Miyagawa-Tomita, S., Shin'oka, T., Ikada, Y. & Kurosawa, H. 2003. First evidence that bone marrow cells contribute to the construction of tissue-engineered vascular autografts in vivo. Circulation 108, 1729-34.
24. Menice, C. B., Hulvershorn, J., Adam, L. P., Wang, C. A. & Morgan, K. G. 1997. Calponin and mitogen-activated protein kinase signaling in differentiated vascular smooth muscle. J. Biol. Chem. 272, 25157-61.
25. Miano, J. M., Cserjesi, P., Ligon, K. L., Periasamy, M. & Olson, E. N. 1994. Smooth muscle myosin heavy chain exclusively marks the smooth muscle lineage during mouse embryogenesis. Circ. Res. 75, 803-12.
26. Morioka, T., Koyama, H., Yamamura, H., Tanaka, S., Fukumoto, S., Emoto, M., Mizuguchi, H., Hayakawa, T., Kojima, I., Takahashi, K. & Nishizawa, Y. 2003. Role of H1-calponin in pancreatic AR42J cell differentiation into insulin-producing cells. Diabetes 52, 760-6.
27. Owens, G. K. 1995. Regulation of differentiation of vascular smooth muscle cells. Physiol. Rev. 75, 487-517.
28. Owens, G. K., Kumar, M. S. & Wamhoff, B. R. 2004. Molecular regulation of vascular smooth muscle cell differentiation in development and disease. Physiol. Rev. 84, 767-801.
29. Pittenger, M. F., Mackay, A. M., Beck, S. C., Jaiswal, R. K., Douglas, R., Mosca, J. D., Moorman, M. A., Simonetti, D. W., Craig, S. & Marshak, D. R. 1999. Multilineage potential of adult human mesenchymal stem cells. Science 284, 143-7.
30. Plantier, M., Fattoum, A., Menn, B., Ben-Ari, Y., der Terrossian, E. & Represa, A. 1999. Acidic calponin immunoreactivity in postnatal rat brain and cultures: subcellular localization in growth cones, under the plasma membrane and along actin and glial filaments. Eur. J. Neurosci. 11, 2801-12.
31. Rami, G., Caillard, O., Medina, I., Pellegrino, C., Fattoum, A., Ben-Ari, Y. & Ferhat, L. 2006. Change in the shape and density of dendritic spines caused by overexpression of acidic calponin in cultured hippocampal neurons. Hippocampus 16, 183-97.
32. Regan, C. P., Manabe, I. & Owens, G. K. 2000. Development of a smooth muscle-targeted cre recombinase mouse reveals novel insights regarding smooth muscle myosin heavy chain promoter regulation. Circ. Res. 87, 363-9.
33. Rozenblum, G. T. & Gimona, M. 2008. Calponins: adaptable modular regulators of the actin cytoskeleton. Int. J. Biochem. Cell Biol. 40, 1990-5.
34. Saiura, A., Sata, M., Hirata, Y., Nagai, R. & Makuuchi, M. 2001. Circulating smooth muscle progenitor cells contribute to atherosclerosis. Nat. Med. 7, 382-3.
35. Sata, M., Saiura, A., Kunisato, A., Tojo, A., Okada, S., Tokuhisa, T., Hirai, H., Makuuchi, M., Hirata, Y. & Nagai, R. 2002. Hematopoietic stem cells differentiate into vascular cells that participate in the pathogenesis of atherosclerosis. Nat. Med. 8, 403-9.
36. Shibukawa, Y., Yamazaki, N., Kumasawa, K., Daimon, E., Tajiri, M., Okada, Y., Ikawa, M. & Wada, Y. 2010. Calponin 3 regulates actin cytoskeleton rearrangement in trophoblastic cell fusion. Mol. Biol. Cell 21, 3973-84.
37. Shimizu, K., Sugiyama, S., Aikawa, M., Fukumoto, Y., Rabkin, E., Libby, P. & Mitchell, R. N. 2001. Host bone-marrow cells are a source of donor intimal smooth- muscle-like cells in murine aortic transplant arteriopathy. Nat. Med. 7, 738-41.
38. Soleimani, M. & Nadri, S. 2009. A protocol for isolation and culture of mesenchymal stem cells from mouse bone marrow. Nat. Protoc. 4, 102-6.
39. Takahashi, K., Abe, M., Hiwada, K. & Kokubu, T. 1988. A novel troponin T-like protein (calponin) in vascular smooth muscle: interaction with tropomyosin paracrystals. J. Hypertens. Suppl. 6, S40-3.
40. Tamama, K., Sen, C. K. & Wells, A. 2008. Differentiation of bone marrow mesenchymal stem cells into the smooth muscle lineage by blocking ERK/MAPK signaling pathway. Stem Cells Dev. 17, 897-908.
41. Tang, J., Hu, G., Hanai, J., Yadlapalli, G., Lin, Y., Zhang, B., Galloway, J., Bahary, N., Sinha, S., Thisse, B., Thisse, C., Jin, J. P., Zon, L. I. & Sukhatme, V. P. 2006. A critical role for calponin 2 in vascular development. J. Biol. Chem. 281, 6664-72.
42. Tian, H., Bharadwaj, S., Liu, Y., Ma, P. X., Atala, A. & Zhang, Y. 2010. Differentiation of human bone marrow mesenchymal stem cells into bladder cells: potential for urological tissue engineering. Tissue Eng. Part A 16, 1769-79.
43. Treguer, K., Naye, F., Thiebaud, P., Fedou, S., Soulet, F., Theze, N. & Faucheux, C. 2009. Smooth muscle cell differentiation from human bone marrow: variations in cell type specific markers and Id gene expression in a new model of cell culture. Cell Biol. Int. 33, 621-31.
44. Tremain, N., Korkko, J., Ibberson, D., Kopen, G. C., Digirolamo, C. & Phinney, D. G. 2001. MicroSAGE analysis of 2, 353 expressed genes in a single cell-derived colony of undifferentiated human mesenchymal stem cells reveals mRNAs of multiple cell lineages. Stem Cells 19, 408-18.
45. Wagers, A. J., Sherwood, R. I., Christensen, J. L. & Weissman, I. L. 2002. Little evidence for developmental plasticity of adult hematopoietic stem cells. Science 297, 2256-9.
46. Wang, C. H., Cherng, W. J., Yang, N. I., Kuo, L. T., Hsu, C. M., Yeh, H. I., Lan, Y. J., Yeh, C. H. & Stanford, W. L. 2008. Late-outgrowth endothelial cells attenuate intimal hyperplasia contributed by mesenchymal stem cells after vascular injury. Arterioscler. Thromb. Vasc. Biol. 28, 54-60.
47. Winder, S. J. & Walsh, M. P. 1990. Smooth muscle calponin. Inhibition of actomyosin MgATPase and regulation by phosphorylation. J. Biol. Chem. 265, 10148-55.
48. Yamada, T., Shiraishi, R., Taki, K., Nakano, S., Tokunaga, O. & Itoh, T. 1997. Immunohistochemical and ultrastructural examination of smooth muscle cells in aortocoronary saphenous vein grafts. Angiology 48, 381-90.
49. Yoshikawa, H., Taniguchi, S. I., Yamamura, H., Mori, S., Sugimoto, M., Miyado, K., Nakamura, K., Nakao, K., Katsuki, M., Shibata, N. & Takahashi, K. 1998. Mice lacking smooth muscle calponin display increased bone formation that is associated with enhancement of bone morphogenetic protein responses. Genes Cells 3, 685-95.