cGMP-dependent protein kinase Iβ regulates breast cancer cell migration and invasion via interaction with the actin/myosin-associated protein caldesmon

Journal of Cell Science

Volumn 126, Issue 7, 2013, Pages 1626-1636

  Schwappacher, Raphaela ^a   Rangaswami, Hema ^a   Su Yuo, Jacqueline ^a   Hassad, Aaron ^a   Spitler, Ryan ^b   Casteel, Darren E ^a  

^a UNIVERSITY OF CALIFORNIA SAN DIEGO   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Caldesmon; Cgmp dependent protein kinase; Human breast cancer cells; Invasion; Migration

Indexed keywords

CALDESMON; CYCLIC GMP DEPENDENT PROTEIN KINASE 1; GLUTAMIC ACID; MYOSIN ADENOSINE TRIPHOSPHATASE; MYOSIN IIA; SERINE; SMALL INTERFERING RNA;

ACTIN MYOSIN INTERACTION; ARTICLE; BREAST CELL; CANCER CELL; CELL INVASION; CELL MIGRATION; CELL MOTILITY; ENZYME ACTIVATION; ENZYME ACTIVITY; HUMAN; HUMAN CELL; MUTATIONAL ANALYSIS; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN DEPLETION; PROTEIN LOCALIZATION; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; PROTEIN PURIFICATION; SIGNAL TRANSDUCTION;

CALDESMON; CGMP-DEPENDENT PROTEIN KINASE; HUMAN BREAST CANCER CELLS; INVASION; MIGRATION;

ACTINS; BREAST NEOPLASMS; CALMODULIN-BINDING PROTEINS; CELL LINE, TUMOR; CELL MOVEMENT; CYCLIC GMP-DEPENDENT PROTEIN KINASE TYPE I; FEMALE; HUMANS; MASS SPECTROMETRY; MYOSINS;

EID: 84877972950     PISSN: 00219533     EISSN: 14779137     Source Type: Journal    
DOI: 10.1242/jcs.118190     Document Type: Article

References (68)

1. Brown, C., Pan, X. and Hassid, A. (1999). Nitric oxide and C-type atrial natriuretic peptide stimulate primary aortic smooth muscle cell migration via a cGMP-dependent mechanism: relationship to microfilament dissociation and altered cell morphology. Circ. Res. 84, 655-667.
2. Caenepeel, S., Charydczak, G., Sudarsanam, S., Hunter, T. and Manning, G. (2004). The mouse kinome: discovery and comparative genomics of all mouse protein kinases. Proc. Natl. Acad. Sci. USA 101, 11707-11712.
3. Casteel, D. E., Zhuang, S., Gudi, T., Tang, J., Vuica, M., Desiderio, S. and Pilz, R. B. (2002). cGMP-dependent protein kinase I beta physically and functionally interacts with the transcriptional regulator TFII-I. J. Biol. Chem. 277, 32003-32014.
4. Casteel, D. E., Boss, G. R. and Pilz, R. B. (2005). Identification of the interface between cGMP-dependent protein kinase Ibeta and its interaction partners TFII-I and IRAG reveals a common interaction motif. J. Biol. Chem. 280, 38211-38218.
5. Casteel, D. E., Zhang, T., Zhuang, S. and Pilz, R. B. (2008). cGMP-dependent protein kinase anchoring by IRAG regulates its nuclear translocation and transcriptional activity. Cell. Signal. 20, 1392-1399.
6. Chalovich, J. M., Cornelius, P. and Benson, C. E. (1987). Caldesmon inhibits skeletal actomyosin subfragment-1 ATPase activity and the binding of myosin subfragment-1 to actin. J. Biol. Chem. 262, 5711-5716.
7. Childs, T. J., Watson, M. H., Sanghera, J. S., Campbell, D. L., Pelech, S. L. and Mak, A. S. (1992). Phosphorylation of smooth muscle caldesmon by mitogenactivated protein (MAP) kinase and expression of MAP kinase in differentiated smooth muscle cells. J. Biol. Chem. 267, 22853-22859.
8. Deguchi, A., Thompson, W. J. and Weinstein, I. B. (2004). Activation of protein kinase G is sufficient to induce apoptosis and inhibit cell migration in colon cancer cells. Cancer Res. 64, 3966-3973.
9. Dephoure, N., Zhou, C., Villén, J., Beausoleil, S. A., Bakalarski, C. E., Elledge, S. J. and Gygi, S. P. (2008). A quantitative atlas of mitotic phosphorylation. Proc. Natl. Acad. Sci. USA 105, 10762-10767.
10. Dubey, R. K., Jackson, E. K. and Lüscher, T. F. (1995). Nitric oxide inhibits angiotensin II-induced migration of rat aortic smooth muscle cell. Role of cyclicnucleotides and angiotensin1 receptors. J. Clin. Invest. 96, 141-149.
11. Eckert, M. A., Lwin, T. M., Chang, A. T., Kim, J., Danis, E., Ohno-Machado, L. and Yang, J. (2011). Twist1-induced invadopodia formation promotes tumor metastasis. Cancer Cell 19, 372-386.
12. Elferink, J. G. and De Koster, B. M. (1998). The involvement of protein kinase G in stimulation of neutrophil migration by endothelins. Eur. J. Pharmacol. 350, 285-291.
13. Eppinga, R. D., Li, Y., Lin, J. L., Mak, A. S. and Lin, J. J. (2006). Requirement of reversible caldesmon phosphorylation at P21-activated kinase-responsive sites for lamellipodia extensions during cell migration. Cell Motil. Cytoskeleton 63, 543-562.
14. Francis, S. H., Busch, J. L., Corbin, J. D. and Sibley, D. (2010). cGMP-dependent protein kinases and cGMP phosphodiesterases in nitric oxide and cGMP action. Pharmacol. Rev. 62, 525-563.
15. Hayashi, K., Yano, H., Hashida, T., Takeuchi, R., Takeda, O., Asada, K., Takahashi, E., Kato, I. and Sobue, K. (1992). Genomic structure of the human caldesmon gene. Proc. Natl. Acad. Sci. USA 89, 12122-12126.
16. Haystead, T. A. (2005). ZIP kinase, a key regulator of myosin protein phosphatase 1. Cell. Signal. 17, 1313-1322.
17. Hofmann, F., Bernhard, D., Lukowski, R. and Weinmeister, P. (2009). cGMP regulated protein kinases (cGK). Handb. Exp. Pharmacol. 191, 137-162.
18. Iizaka, M., Han, H. J., Akashi, H., Furukawa, Y., Nakajima, Y., Sugano, S., Ogawa, M. and Nakamura, Y. (2000). Isolation and chromosomal assignment of a novel human gene, CORO1C, homologous to coronin-like actin-binding proteins. Cytogenet. Cell Genet. 88, 221-224.
19. Ikebe, M. and Reardon, S. (1990). Phosphorylation of smooth muscle caldesmon by calmodulin-dependent protein kinase II. Identification of the phosphorylation sites. J. Biol. Chem. 265, 17607-17612.
20. Jacob, A., Molkentin, J. D., Smolenski, A., Lohmann, S. M. and Begum, N. (2002). Insulin inhibits PDGF-directed VSMC migration via NO/ cGMP increase of MKP-1 and its inactivation of MAPKs. Am. J. Physiol. Cell Physiol. 283, C704-C713.
21. Jadeski, L. C., Hum, K. O., Chakraborty, C. and Lala, P. K. (2000). Nitric oxide promotes murine mammary tumour growth and metastasis by stimulating tumour cell migration, invasiveness and angiogenesis. Int. J. Cancer 86, 30-39.
22. Jadeski, L. C., Chakraborty, C. and Lala, P. K. (2003). Nitric oxide-mediated promotion of mammary tumour cell migration requires sequential activation of nitric oxide synthase, guanylate cyclase and mitogen-activated protein kinase. Int. J. Cancer 106, 496-504.
23. Jalal, S., Arsenault, R., Potter, A. A., Babiuk, L. A., Griebel, P. J. and Napper, S. (2009). Genome to kinome: species-specific peptide arrays for kinome analysis. Sci. Signal. 2, pl1.
24. Kamisato, S., Uemura, Y., Takami, N. and Okamoto, K. (1997). Involvement of intracellular cyclic GMP and cyclic GMP-dependent protein kinase in alpha-elastininduced macrophage chemotaxis. J. Biochem. 121, 862-867.
25. Kawasaki, K., Smith, R. S., Jr, Hsieh, C. M., Sun, J., Chao, J. and Liao, J. K. (2003). Activation of the phosphatidylinositol 3-kinase/protein kinase Akt pathway mediates nitric oxide-induced endothelial cell migration and angiogenesis. Mol. Cell. Biol. 23, 5726-5737.
26. Kim, D. W., Cheriyath, V., Roy, A. L. and Cochran, B. H. (1998). TFII-I enhances activation of the c-fos promoter through interactions with upstream elements. Mol. Cell. Biol. 18, 3310-3320.
27. Kim, Y. M., Chung, H. T., Kim, S. S., Han, J. A., Yoo, Y. M., Kim, K. M., Lee, G. H., Yun, H. Y., Green, A., Li, J. et al. (1999). Nitric oxide protects PC12 cells from serum deprivation-induced apoptosis by cGMP-dependent inhibition of caspase signaling. J. Neurosci. 19, 6740-6747.
28. Koller, A., Schlossmann, J., Ashman, K., Uttenweiler-Joseph, S., Ruth, P. and Hofmann, F. (2003). Association of phospholamban with a cGMP kinase signaling complex. Biochem. Biophys. Res. Commun. 300, 155-160.
29. Leung, E. L., Wong, J. C., Johlfs, M. G., Tsang, B. K. and Fiscus, R. R. (2010). Protein kinase G type Ialpha activity in human ovarian cancer cells significantly contributes to enhanced Src activation and DNA synthesis/cell proliferation. Mol. Cancer Res. 8, 578-591.
30. Li, Y., Zhuang, S., Guo, H., Mabuchi, K., Lu, R. C. and Wang, C. A. (2000). The major myosin-binding site of caldesmon resides near its N-terminal extreme. J. Biol. Chem. 275, 10989-10994.
31. Lin, J. J., Li, Y., Eppinga, R. D., Wang, Q. and Jin, J. P. (2009). Chapter 1: roles of caldesmon in cell motility and actin cytoskeleton remodeling. Int. Rev. Cell Mol. Biol. 274, 1-68.
32. Mayanagi, T. and Sobue, K. (2011). Diversification of caldesmon-linked actin cytoskeleton in cell motility. Cell Adh. Migr. 5, 150-159.
33. Mayanagi, T., Morita, T., Hayashi, K., Fukumoto, K. and Sobue, K. (2008). Glucocorticoid receptor-mediated expression of caldesmon regulates cell migration via the reorganization of the actin cytoskeleton. J. Biol. Chem. 283, 31183-31196.
34. Mirzapoiazova, T., Kolosova, I. A., Romer, L., Garcia, J. G. and Verin, A. D. (2005). The role of caldesmon in the regulation of endothelial cytoskeleton and migration. J. Cell. Physiol. 203, 520-528.
35. Morita, T., Mayanagi, T. and Sobue, K. (2012). Caldesmon regulates axon extension through interaction with myosin II. J. Biol. Chem. 287, 3349-3356.
36. Olsen, J. V., Vermeulen, M., Santamaria, A., Kumar, C., Miller, M. L., Jensen, L. J., Gnad, F., Cox, J., Jensen, T. S., Nigg, E. A. et al. (2010). Quantitative phosphoproteomics reveals widespread full phosphorylation site occupancy during mitosis. Sci. Signal. 3, ra3.
37. Perkins, D. N., Pappin, D. J., Creasy, D. M. and Cottrell, J. S. (1999). Probabilitybased protein identification by searching sequence databases using mass spectrometry data. Electrophoresis 20, 3551-3567.
38. Punathil, T., Tollefsbol, T. O. and Katiyar, S. K. (2008). EGCG inhibits mammary cancer cell migration through inhibition of nitric oxide synthase and guanylate cyclase. Biochem. Biophys. Res. Commun. 375, 162-167.
39. Rangaswami, H., Schwappacher, R., Marathe, N., Zhuang, S., Casteel, D. E., Haas, B., Chen, Y., Pfeifer, A., Kato, H., Shattil, S. et al. (2010). Cyclic GMP and protein kinase G control a Src-containing mechanosome in osteoblasts. Sci. Signal. 3, ra91.
40. Rolli-Derkinderen, M., Toumaniantz, G., Pacaud, P. and Loirand, G. (2010). RhoA phosphorylation induces Rac1 release from guanine dissociation inhibitor alpha and stimulation of vascular smooth muscle cell migration. Mol. Cell. Biol. 30, 4786-4796.
41. Rothman, A., Kulik, T. J., Taubman, M. B., Berk, B. C., Smith, C. W. and Nadal-Ginard, B. (1992). Development and characterization of a cloned rat pulmonary arterial smooth muscle cell line that maintains differentiated properties through multiple subcultures. Circulation 86, 1977-1986.
42. Roy, A. L. (2012). Biochemistry and biology of the inducible multifunctional transcription factor TFII-I: 10 years later. Gene 492, 32-41.
43. Schlossmann, J., Ammendola, A., Ashman, K., Zong, X., Huber, A., Neubauer, G., Wang, G. X., Allescher,H. D.,Korth, M., Wilm, M. et al. (2000). Regulation of intracellular calcium by a signalling complex of IRAG, IP3 receptor and cGMP kinase Ibeta. Nature 404, 197-201.
44. Smith, C. W., Pritchard, K. and Marston, S. B. (1987). The mechanism of Ca2+ regulation of vascular smooth muscle thin filaments by caldesmon and calmodulin. J. Biol. Chem. 262, 116-122.
45. Smolenski, A., Poller, W., Walter, U. and Lohmann, S. M. (2000). Regulation of human endothelial cell focal adhesion sites and migration by cGMP-dependent protein kinase I. J. Biol. Chem. 275, 25723-25732.
46. Surks, H. K., Mochizuki, N., Kasai, Y., Georgescu, S. P., Tang, K. M., Ito, M., Lincoln, T. M. and Mendelsohn, M. E. (1999). Regulation of myosin phosphatase by a specific interaction with cGMP- dependent protein kinase Ialpha. Science 286, 1583-1587.
47. Tang, K. M., Wang, G. R., Lu, P., Karas, R. H., Aronovitz, M., Heximer, S. P., Kaltenbronn, K. M., Blumer, K. J., Siderovski, D. P., Zhu, Y. et al. (2003). Regulator of G-protein signaling-2 mediates vascular smooth muscle relaxation and blood pressure. Nat. Med. 9, 1506-1512.
48. Tinsley, H. N., Gary, B. D., Keeton, A. B., Lu, W., Li, Y. and Piazza, G. A. (2011). Inhibition of PDE5 by sulindac sulfide selectively induces apoptosis and attenuates oncogenic Wnt/b-catenin-mediated transcription in human breast tumor cells. Cancer Prev. Res. (Phila.) 4, 1275-1284.
49. Uemura, Y. and Okamoto, K. (1997). Elastin-derived peptide induces monocyte chemotaxis by increasing intracellular cyclic GMP level and activating cyclic GMP dependent protein kinase. Biochem. Mol. Biol. Int. 41, 57-64.
50. Uhler, M. D. (1993). Cloning and expression of a novel cyclic GMP-dependent protein kinase from mouse brain. J. Biol. Chem. 268, 13586-13591.
51. Van Eyk, J. E., Arrell, D. K., Foster, D. B., Strauss, J. D., Heinonen, T. Y., Furmaniak-Kazmierczak, E., Côté, G. P. and Mak, A. S. (1998). Different molecular mechanisms for Rho family GTPase-dependent, Ca2+-independent contraction of smooth muscle. J. Biol. Chem. 273, 23433-23439.
52. VanUffelen, B. E., de Koster, B. M., VanSteveninck, J. and Elferink, J. G. (1996). Carbon monoxide enhances human neutrophil migration in a cyclic GMP-dependent way. Biochem. Biophys. Res. Commun. 226, 21-26.
53. Wang, Z. and Yang, Z. Q. (2000). Casein kinase II phosphorylation of caldesmon downregulates myosin-caldesmon interactions. Biochemistry 39, 11114-11120.
54. Wang, Z., Jiang, H., Yang, Z. Q. and Chacko, S. (1997). Both N-terminal myosinbinding and C-terminal actin-binding sites on smooth muscle caldesmon are required for caldesmon-mediated inhibition of actin filament velocity. Proc. Natl. Acad. Sci. USA 94, 11899-11904.
55. Wang, Y., El-Zaru, M. R., Surks, H. K. and Mendelsohn, M. E. (2004). Formin homology domain protein (FHOD1) is a cyclic GMP-dependent protein kinase Ibindingprotein and substrate in vascular smooth muscle cells. J. Biol. Chem. 279, 24420-24426.
56. Wei, Q. and Adelstein, R. S. (2000). Conditional expression of a truncated fragment of nonmuscle myosin II-A alters cell shape but not cytokinesis in HeLa cells. Mol. Biol. Cell 11, 3617-3627.
57. Weitzel, D. H., Chambers, J. and Haystead, T. A. (2011). Phosphorylation-dependent control of ZIPK nuclear import is species specific. Cell. Signal. 23, 297-303.
58. Whitt, J. D., Li, N., Tinsley, H. N., Chen, X., Zhang, W., Li, Y., Gary, B. D., Keeton, A. B., Xi, Y., Abadi, A. H. et al. (2012). A novel sulindac derivative that potently suppresses colon tumor cell growth by inhibiting cGMP phosphodiesterase and bcatenin transcriptional activity. Cancer Prev. Res. (Phila.) 5, 822-833.
59. Wong, J. C., Bathina, M. and Fiscus, R. R. (2012). Cyclic GMP/protein kinase G type-Ia (PKG-Ia) signaling pathway promotes CREB phosphorylation and maintains higher c-IAP1, livin, survivin, and Mcl-1 expression and the inhibition of PKG-Ia kinase activity synergizes with cisplatin in non-small cell lung cancer cells. J. Cell. Biochem. 113, 3587-3598.
60. Yamashiro, S., Yamakita, Y., Hosoya, H. and Matsumura, F. (1991). Phosphorylation of non-muscle caldesmon by p34cdc2 kinase during mitosis. Nature 349, 169-172.
61. Yin, H. L., Zaner, K. S. and Stossel, T. P. (1980). Ca2+ control of actin gelation. Interaction of gelsolin with actin filaments and regulation of actin gelation. J. Biol. Chem. 255, 9494-9500.
62. Yokouchi, K., Numaguchi, Y., Kubota, R., Ishii, M., Imai, H., Murakami, R., Ogawa, Y., Kondo, T., Okumura, K., Ingber, D. E. et al. (2006). l-Caldesmon regulates proliferation and migration of vascular smooth muscle cells and inhibits neointimal formation after angioplasty. Arterioscler. Thromb. Vasc. Biol. 26, 2231-2237.
63. Yoshio, T., Morita, T., Kimura, Y., Tsujii, M., Hayashi, N. and Sobue, K. (2007). Caldesmon suppresses cancer cell invasion by regulating podosome/invadopodium formation. FEBS Lett. 581, 3777-3782.
64. Yuasa, K., Omori, K. and Yanaka, N. (2000). Binding and phosphorylation of a novel male germ cell-specific cGMP-dependent protein kinase-anchoring protein by cGMPdependent protein kinase Ialpha. J. Biol. Chem. 275, 4897-4905.
65. Zhang, S., Yang, Y., Kone, B. C., Allen, J. C. and Kahn, A. M. (2003). Insulinstimulated cyclic guanosine monophosphate inhibits vascular smooth muscle cell migration by inhibiting Ca/calmodulin-dependent protein kinase II. Circulation 107, 1539-1544.
66. Zhang, T., Zhuang, S., Casteel, D. E., Looney, D. J., Boss, J. R. and Pilz, R. B. (2007). A cysteine-rich LIM-only protein mediates regulation of smooth musclespecific gene expression by cGMP-dependent protein kinase. J. Biol. Chem. 282, 33367-33380.
67. Zheng, P. P., van der Weiden, M. and Kros, J. M. (2005). Differential expression of Hela-type caldesmon in tumour neovascularization: a new marker of angiogenic endothelial cells. J. Pathol. 205, 408-414.
68. Zheng, P. P., van der Weiden, M. and Kros, J. M. (2007). Hela l-CaD is implicated in the migration of endothelial cells/endothelial progenitor cells in human neoplasms. Cell Adh. Migr. 1, 84-91.