Calponin 3 regulates actin cytoskeleton rearrangement in trophoblastic cell fusion

Molecular Biology of the Cell

Volumn 21, Issue 22, 2010, Pages 3973-3984

  Shibukawa, Yukinao ^a   Yamazaki, Natsuko ^a   Kumasawa, Keiichi ^b   Daimon, Etsuko ^a   Tajiri, Michiko ^a,c   Okada, Yuka ^b   Ikawa, Masahito ^b   Wada, Yoshinao ^a  

^a RESEARCH INSTITUTE FOR MATERNAL AND CHILD HEALTH   (Japan)

^b OSAKA UNIVERSITY   (Japan)

^c JAPAN SCIENCE AND TECHNOLOGY AGENCY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

ASPARTIC ACID; CALPONIN; CALPONIN 3; F ACTIN; FORSKOLIN; MUTANT PROTEIN; SERINE; UNCLASSIFIED DRUG;

ANIMAL TISSUE; ARTICLE; CELL FUSION; CHORIOCARCINOMA; CONTROLLED STUDY; CYTOPLASM; CYTOSKELETON; CYTOTROPHOBLAST; DISSOCIATION; GENE SILENCING; HUMAN; HUMAN CELL; HUMAN TISSUE; MOUSE; NONHUMAN; PLACENTA; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; SYNCYTIUM; TROPHOBLAST; TUMOR CELL;

ACTINS; AMINO ACID SEQUENCE; ANIMALS; BINDING SITES; BLOTTING, WESTERN; CALCIUM-BINDING PROTEINS; CELL FUSION; CELL LINE, TUMOR; CHORIOCARCINOMA; CYTOPLASM; CYTOSKELETON; FEMALE; FORSKOLIN; HEK293 CELLS; HUMANS; LUMINESCENT PROTEINS; MICE; MICROFILAMENT PROTEINS; MICROSCOPY, FLUORESCENCE; MOLECULAR SEQUENCE DATA; MUTATION; PHOSPHORYLATION; PLACENTA; PREGNANCY; PROTEIN BINDING; RNA INTERFERENCE; TROPHOBLASTS;

EID: 78649679434     PISSN: 10591524     EISSN: 19394586     Source Type: Journal    
DOI: 10.1091/mbc.E10-03-0261     Document Type: Article

References (53)

1. Abouzaglou, J., Benistant, C., Gimona, M., Roustan, C., Kassab, R., and Fattoum, A. (2004). Tyrosine phosphorylation of calponins: inhibition of the interaction with F-actin. Eur. J. Biochem. 271, 2615-2623.
2. Applegate, D., Feng, W., Green, R. S., and Taubman, M. B. (1994). Cloning and expression of a novel acidic calponin isoform from rat aortic vascular smooth muscle. J. Biol. Chem. 269, 10683-10690.
3. Burgstaller, G., Kranewitter, W. J., and Gimona, M. (2002). The molecular basis for the autoregulation of calponin by isoform-specific C-terminal tail sequences. J. Cell Sci. 115, 2021-2029.
4. Chaney, L. K., and Jacobson, B. S. (1983). Coating cells with colloidal silica for high yield isolation of plasma membrane sheets and identification of transmembrane proteins. J. Biol. Chem. 258, 10062-10072.
5. Chen, E. H., and Olson, E. N. (2005). Unveiling the mechanisms of cell-cell fusion. Science. 308, 369-373.
6. Danninger, C., and Gimona, M. (2000). Live dynamics of GFP-calponin: isoform-specific modulation of the actin cytoskeleton and autoregulation by C-terminal sequences. J. Cell Sci. 113, 3725-3736.
7. Dupressoir, A., Marceau, G., Vernochet, C., Benit, L., Kanellopoulos, C., Sapin, V., and Heidmann, T. (2005). Syncytin-A and syncytin-B, two fusogenic placenta-specific murine envelope genes of retroviral origin conserved in Muridae. Proc. Natl. Acad. Sci. USA 102, 725-730.
8. Dupressoir, A., Vernochet, C., Bawa, O., Harper, F., Pierron, G., Opolon, P., and Heidmann, T. (2009). Syncytin-A knockout mice demonstrate the critical role in placentation of a fusogenic, endogenous retrovirus-derived, envelope gene. Proc. Natl. Acad. Sci. USA 106, 12127-12132.
9. el-Mezgueldi, M., Strasser, P., Fattoum, A., and Gimona, M. (1996). Expressing functional domains of mouse calponin: involvement of the region around alanine 145 in the actomyosin ATPase inhibitory activity of calponin. Biochemistry 35, 3654-3661.
10. Fraser, E. D., and Walsh, M. P. (1995). Dephosphorylation of calponin by type 2B protein phosphatase. Biochemistry 34, 9151-9158.
11. Frendo, J. L., Olivier, D., Cheynet, V., Blond, J. L., Bouton, O., Vidaud, M., Rabreau, M., Evain-Brion, D., and Mallet, F. (2003). Direct involvement of HERV-W Env glycoprotein in human trophoblast cell fusion and differentiation. Mol. Cell. Biol. 23, 3566-3574.
12. Fukui, Y., Masuda, H., Takagi, M., Takahashi, K., and Kiyokane, K. (1997). The presence of h2-calponin in human keratinocyte. J. Dermatol. Sci. 14, 29-36.
13. Ghitescu, L. D., Crine, P., and Jacobson, B. S. (1997). Antibodies specific to the plasma membrane of rat lung microvascular endothelium. Exp. Cell. Res. 232, 47-55.
14. Ghitescu, L. D., Gugliucci, A., and Dumas, F. (2001). Actin and annexins I and II are among the main endothelial plasmalemma-associated proteins forming early glucose adducts in experimental diabetes. Diabetes 50, 1666-1674.
15. Hatano, N., Mori, Y., Oh-hora, M., Kosugi, A., Fujikawa, T., Nakai, N., Niwa, H., Miyazaki, J., Hamaoka, T., and Ogata, M. (2003). Essential role for ERK2 mitogen-activated protein kinase in placental development. Genes Cells. 8, 847-856. (Pubitemid 37428014)
16. Hossain, M. M., Smith, P. G., Wu, K., and Jin, J. P. (2006). Cytoskeletal tension regulates both expression and degradation of h2-calponin in lung alveolar cells. Biochemistry 45, 15670-15683. (Pubitemid 46032488)
17. Huang, Q. Q., Hossain, M. M., Wu, K., Parai, K., Pope, R. M., and Jin, J. P. (2008). Role of H2-calponin in regulating macrophage motility and phagocytosis. J. Biol. Chem. 283, 25887-25899.
18. Hubbard, A. L., and Ma, A. (1983). Isolation of rat hepatocyte plasma membranes. II. Identification of membrane-associated cytoskeletal proteins. J. Cell. Biol. 96, 230-239.
19. Ichikawa, K., Ito, M., Okubo, S., Konishi, T., Nakano, T., Mino, T., Nakamura, F., Naka, M., and Tanaka, T. (1993). Calponin phosphatase from smooth muscle: a possible role of type 1 protein phosphatase in smooth muscle relaxation. Biochem. Biophys. Res. Commun. 193, 827-833.
20. Kaneko, T., Amano, M., Maeda, A., Goto, H., Takahashi, K., Ito, M., and Kaibuchi, K. (2000). Identification of calponin as a novel substrate of Rhokinase. Biochem. Biophys. Res. Commun. 273, 110-116.
21. Keryer, G., Alsat, E., Tasken, K., and Evain-Brion, D. (1998). Cyclic AMP-dependent protein kinases and human trophoblast cell differentiation in vitro. J. Cell. Sci. 111, 995-1004.
22. Kontani, K., Moskowitz, I. P., and Rothman, J. H. (2005). Repression of cell-cell fusion by components of the C. elegans vacuolar ATPase complex. Dev. Cell. 8, 787-794.
23. Lyden, T. W., Ng, A. K., and Rote, N. S. (1993). Modulation of phosphatidylserine epitope expression by BeWo cells during forskolin treatment. Placenta 14, 177-186.
24. Mi, S., Lee, X., Li, X., Veldman, G. M., Finnerty, H., Racie, L., LaVallie, E., Tang, X. Y., Edouard, P., Howes, S., Keith, J. C., Jr., and McCoy, J. M. (2000). Syncytin is a captive retroviral envelope protein involved in human placental morphogenesis. Nature 403, 785-789.
25. Miyoshi, H. (2004). Gene delivery to hematopoietic stem cells using lentiviral vectors. Methods Mol Biol. 246, 429-438.
26. Mohler, W. A., Shemer, G., del Campo, J. J., Valansi, C., Opoku-Serebuoh, E., Scranton, V., Assaf, N., White, J. G., and Podbilewicz, B. (2002). The type I membrane protein EFF-1 is essential for developmental cell fusion. Dev. Cell. 2, 355-362.
27. Morgan, K. G., and Gangopadhyay, S. S. (2001). Invited review: cross-bridge regulation by thin filament-associated proteins. J. Appl. Physiol. 91, 953-962.
28. Nakamura, F., Mino, T., Yamamoto, J., Naka, M., and Tanaka, T. (1993). Identification of the regulatory site in smooth muscle calponin that is phosphorylated by protein kinase C. J. Biol. Chem. 268, 6194-6201.
29. Pajcini, K. V., Pomerantz, J. H., Alkan, O., Doyonnas, R., and Blau, H. M. (2008). Myoblasts and macrophages share molecular components that contribute to cell-cell fusion. J. Cell. Biol. 180, 1005-1019.
30. Rahbar, A. M., and Fenselau, C. (2004). Integration of Jacobson's pellicle method into proteomic strategies for plasma membrane proteins. J. Proteome Res. 3, 1267-1277.
31. Rossant, J., and Cross, J. C. (2001). Placental development: lessons from mouse mutants. Nat. Rev. Genet. 2, 538-548.
32. Rozenblum, G. T., and Gimona, M. (2007). Calponins: adaptable modular regulators of the actin cytoskeleton. Int. J. Biochem. Cell. Biol. 31, 31.
33. Ruiz-Gomez, M., Coutts, N., Price, A., Taylor, M. V., and Bate, M. (2000). Drosophila dumbfounded: a myoblast attractant essential for fusion. Cell. 102, 189-198.
34. Schreiber, J., Riethmacher-Sonnenberg, E., Riethmacher, D., Tuerk, E. E., Enderich, J., Bosl, M. R., and Wegner, M. (2000). Placental failure in mice lacking the mammalian homolog of glial cells missing, GCMa. Mol. Cell. Biol. 20, 2466-2474.
35. Sohn, R. L., Huang, P., Kawahara, G., Mitchell, M., Guyon, J., Kalluri, R., Kunkel, L. M., and Gussoni, E. (2009). A role for nephrin, a renal protein, in vertebrate skeletal muscle cell fusion. Proc. Natl. Acad. Sci. USA 106, 9274-9279.
36. Stolz, D. B., Ross, M. A., Salem, H. M., Mars, W. M., Michalopoulos, G. K., and Enomoto, K. (1999). Cationic colloidal silica membrane perturbation as a means of examining changes at the sinusoidal surface during liver regeneration. Am. J. Pathol. 155, 1487-1498.
37. Strasser, P., Gimona, M., Moessler, H., Herzog, M., and Small, J. V. (1993). Mammalian calponin. Identification and expression of genetic variants. FEBS Lett. 330, 13-18.
38. Strunkelnberg, M., Bonengel, B., Moda, L. M., Hertenstein, A., de Couet, H. G., Ramos, R. G., and Fischbach, K. F. (2001). rst and its paralogue kirre act redundantly during embryonic muscle development in Drosophila. Development. 128, 4229-4239.
39. Sugiyama, N., Masuda, T., Shinoda, K., Nakamura, A., Tomita, M., and Ishihama, Y. (2007). Phosphopeptide enrichment by aliphatic hydroxy acid-modified metal oxide chromatography for nano-LC-MS/MS in proteomics applications. Mol. Cell. Proteomics. 6, 1103-1109.
40. Takahashi, K., Hiwada, K., and Kokubu, T. (1988). Vascular smooth muscle calponin: a novel troponin T-like protein. Hypertension 11, 620-626.
41. Takahashi, K., and Nadal-Ginard, B. (1991). Molecular cloning and sequence analysis of smooth muscle calponin. J. Biol. Chem. 266, 13284-13288.
42. Tang, D. C., Kang, H. M., Jin, J. P., Fraser, E. D., and Walsh, M. P. (1996). Structure-function relations of smooth muscle calponin. The critical role of serine 175. J. Biol. Chem. 271, 8605-8611.
43. 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., and Sukhatme, V. P. (2006). A critical role for calponin 2 in vascular development. J. Biol. Chem. 281, 6664-6672.
44. Thumkeo, D., Keel, J., Ishizaki, T., Hirose, M., Nonomura, K., Oshima, H., Oshima, M., Taketo, M. M., and Narumiya, S. (2003). Targeted disruption of the mouse rho-associated kinase 2 gene results in intrauterine growth retardation and fetal death. Mol. Cell. Biol. 23, 5043-5055.
45. Tsunekawa, S., Takahashi, K., Abe, M., Hiwada, K., Ozawa, K., and Murachi, T. (1989). Calpain proteolysis of free and bound forms of calponin, a troponin T-like protein in smooth muscle. FEBS Lett. 250, 493-496.
46. Vargas, A., Moreau, J., Landry, S., LeBellego, F., Toufaily, C., Rassart, E., Lafond, J., and Barbeau, B. (2009). Syncytin-2 plays an important role in the fusion of human trophoblast cells. J. Mol. Biol. 392, 301-318.
47. Vargas, A., Moreau, J., Le Bellego, F., Lafond, J., and Barbeau, B. (2008). Induction of trophoblast cell fusion by a protein tyrosine phosphatase inhibitor. Placenta 29, 170-174.
48. Wice, B., Menton, D., Geuze, H., and Schwartz, A. L. (1990). Modulators of cyclic AMP metabolism induce syncytiotrophoblast formation in vitro. Exp. Cell. Res. 186, 306-316.
49. Winder, S. J., and Walsh, M. P. (1990). Smooth muscle calponin. Inhibition of actomyosin MgATPase and regulation by phosphorylation. J. Biol. Chem. 265, 10148-10155.
50. Yoshikawa, H., Taniguchi, S. I., Yamamura, H., Mori, S., Sugimoto, M., Miyado, K., Nakamura, K., Nakao, K., Katsuki, M., Shibata, N., and 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, 685-695. (Pubitemid 28557209)
51. Yoshimoto, R., Hori, M., Ozaki, H., and Karaki, H. (2000). Proteolysis of acidic calponin by mu-calpain. J. Biochem. 128, 1045-1049.
52. Yu, C., Shen, K., Lin, M., Chen, P., Lin, C., Chang, G. D., and Chen, H. (2002). GCMa regulates the syncytin-mediated trophoblastic fusion. J. Biol. Chem. 277, 50062-50068.
53. Zufferey, R., Nagy, D., Mandel, R. J., Naldini, L., and Trono, D. (1997). Multiply attenuated lentiviral vector achieves efficient gene delivery in vivo. Nat. Biotechnol. 15, 871-875.