Metastasis suppressor, NDRG1, mediates its activity through signaling pathways and molecular motors

Carcinogenesis

Volumn 34, Issue 9, 2013, Pages 1943-1954

  Sun, Jing ^a,b,c   Zhang, Daohai ^b   Bae, Dong Hun ^b   Sahni, Sumit ^b   Jansson, Patric ^b   Zheng, Ying ^a   Zhao, Qian ^a   Yue, Fei ^a,c   Zheng, Minhua ^a,c   Kovacevic, Zaklina ^b   Richardson, Des R ^b  

^a SHANGHAI JIAO TONG UNIVERSITY SCHOOL OF MEDICINE   (China)

^b UNIVERSITY OF SYDNEY   (Australia)

^c Shanghai Minimally Invasive Surgery Center   (China)

Author keywords

[No Author keywords available]

Indexed keywords

BETA CATENIN; F ACTIN; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; MAMMALIAN TARGET OF RAPAMYCIN; MITOGEN ACTIVATED PROTEIN KINASE; MOLECULAR MOTOR; PHOSPHATIDYLINOSITOL 3 KINASE; PROTEIN KINASE B; RAF PROTEIN; RAS PROTEIN; TRANSFORMING GROWTH FACTOR BETA;

CELL MIGRATION; CELLULAR DISTRIBUTION; EPITHELIAL MESENCHYMAL TRANSITION; GENE ACTIVITY; GENE INTERACTION; HUMAN; METASTASIS INHIBITION; N MYC DOWNSTREAM REGULATED GENE 1; PRIORITY JOURNAL; PROTEIN LOCALIZATION; PROTEIN PHOSPHORYLATION; PROTEIN POLYMERIZATION; PROTEIN STRUCTURE; REVIEW; SIGNAL TRANSDUCTION; STRESS FIBER; TISSUE DISTRIBUTION; TUMOR SUPPRESSOR GENE; WNT SIGNALING PATHWAY;

ACTINS; CELL CYCLE PROTEINS; EPITHELIAL-MESENCHYMAL TRANSITION; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; NEOPLASM METASTASIS; NEOPLASMS; PHOSPHATIDYLINOSITOL 3-KINASES; PROTO-ONCOGENE PROTEINS C-AKT; SIGNAL TRANSDUCTION;

EID: 84887013316     PISSN: 01433334     EISSN: 14602180     Source Type: Journal    
DOI: 10.1093/carcin/bgt163     Document Type: Review

References (128)

1. Kovacevic, Z. et al. (2006) The metastasis suppressor, Ndrg-1: a new ally in the fight against cancer. Carcinogenesis, 27, 2355-2366.
2. Motwani, M. et al. (2002) Drg1, a novel target for modulating sensitivity to CPT-11 in colon cancer cells. Cancer Res., 62, 3950-3955.
3. Shah, M.A. et al. (2005) Drg1 expression in 131 colorectal liver metastases: correlation with clinical variables and patient outcomes. Clin. Cancer Res., 11, 3296-3302.
4. Park, H. et al. (2000) Hypoxia induces the expression of a 43-kDa protein (PROXY-1) in normal and malignant cells. Biochem. Biophys. Res. Commun., 276, 321-328.
5. Sun, B. et al. (2009) Decreased expression of NDRG1 in glioma is related to tumor progression and survival of patients. J. Neurooncol., 94, 213-219.
6. Kovacevic, Z. et al. (2008) The iron-regulated metastasis suppressor, Ndrg-1: identification of novel molecular targets. Biochim. Biophys. Acta, 1783, 1981-1992.
7. Ellen, T.P. et al. (2008) NDRG1, a growth and cancer related gene: regulation of gene expression and function in normal and disease states. Carcinogenesis, 29, 2-8.
8. Zhao, G. et al. (2011) Identification of NDRG1-regulated genes associated with invasive potential in cervical and ovarian cancer cells. Biochem. Biophys. Res. Commun., 408, 154-159.
9. Bandyopadhyay, S. et al. (2004) Role of the putative tumor metastasis suppressor gene Drg-1 in breast cancer progression. Oncogene, 23, 5675-5681.
10. Cheng, J. et al. (2011) NDRG1 as a biomarker for metastasis, recurrence and of poor prognosis in hepatocellular carcinoma. Cancer Lett., 310, 35-45.
11. Said, H.M. et al. (2009) Oxygen-dependent regulation of NDRG1 in human glioblastoma cells in vitro and in vivo. Oncol. Rep., 21, 237-246.
12. Fotovati, A. et al. (2011) N-myc downstream-regulated gene 1 (NDRG1) a differentiation marker of human breast cancer. Pathol. Oncol. Res., 17, 525-533.
13. Tschan, M.P. et al. (2010) NDRG1/2 expression is inhibited in primary acute myeloid leukemia. Leuk. Res., 34, 393-398.
14. Zhou, R.H. et al. (2001) Characterization of the human NDRG gene family: a newly identified member, NDRG4, is specifically expressed in brain and heart. Genomics, 73, 86-97.
15. Maruyama, Y. et al. (2006) Tumor growth suppression in pancreatic cancer by a putative metastasis suppressor gene Cap43/NDRG1/Drg-1 through modulation of angiogenesis. Cancer Res., 66, 6233-6242.
16. Angst, E. et al. (2006) Cellular differentiation determines the expression of the hypoxia-inducible protein NDRG1 in pancreatic cancer. Br. J. Cancer, 95, 307-313.
17. King, R.H. et al. (2011) Ndrg1 in development and maintenance of the myelin sheath. Neurobiol. Dis., 42, 368-380.
18. Li, Q. et al. (2011) Transcriptional silencing of N-Myc downstream-regulated gene 1 (NDRG1) in metastatic colon cancer cell line SW620. Clin. Exp. Metastasis, 28, 127-135.
19. Li, J. et al. (2003) The growth-inhibitory Ndrg1 gene is a Myc negative target in human neuroblastomas and other cell types with overexpressed N- or c-myc. Mol. Cell. Biochem., 250, 91-105.
20. Masuda, K. et al. (2003) Downregulation of Cap43 gene by von Hippel-Lindau tumor suppressor protein in human renal cancer cells. Int. J. Cancer, 105, 803-810.
21. Toffoli, S. et al. (2009) NDRG1 and CRK-I/II are regulators of endothelial cell migration under Intermittent Hypoxia. Angiogenesis, 12, 339-354.
22. Cangul, H. (2004) Hypoxia upregulates the expression of the NDRG1 gene leading to its overexpression in various human cancers. BMC Genet., 5, 27.
23. Hickok, J.R. et al. (2011) Nitric oxide suppresses tumor cell migration through N-Myc downstream-regulated gene-1 (NDRG1) expression: role of chelatable iron. J. Biol. Chem., 286, 41413-41424.
24. Zheng, Y. et al. (2009) NDRG1 is down-regulated in the early apoptotic event induced by camptothecin analogs: the potential role in proteolytic activation of PKC delta and apoptosis. Proteomics, 9, 2064-2075.
25. Stein, S. et al. (2004) NDRG1 is necessary for p53-dependent apoptosis. J. Biol. Chem., 279, 48930-48940.
26. Zhang, A.H. et al. (2007) p53-dependent NDRG1 expression induces inhibition of intestinal epithelial cell proliferation but not apoptosis after polyamine depletion. Am. J. Physiol. Cell Physiol., 293, C379-C389.
27. Bandyopadhyay, S. et al. (2006) The tumor metastasis suppressor gene Drg-1 down-regulates the expression of activating transcription factor 3 in prostate cancer. Cancer Res., 66, 11983-11990.
28. Matsugaki, T. et al. (2010) N-myc downstream-regulated gene 1/Cap43 expression promotes cell differentiation of human osteosarcoma cells. Oncol. Rep., 24, 721-725.
29. Chua, H.L. et al. (2007) NF-kappaB represses E-cadherin expression and enhances epithelial to mesenchymal transition of mammary epithelial cells: potential involvement of ZEB-1 and ZEB-2. Oncogene, 26, 711-724.
30. McCaig, C. et al. (2011) Phosphorylation of NDRG1 is temporally and spatially controlled during the cell cycle. Biochem. Biophys. Res. Commun., 411, 227-234.
31. Lachat, P. et al. (2002) Expression of NDRG1, a differentiation-related gene, in human tissues. Histochem. Cell Biol., 118, 399-408.
32. Chen, S. et al. (2009) NDRG1 contributes to retinoic acid-induced differentiation of leukemic cells. Leuk. Res., 33, 1108-1113.
33. Nagai, M.A. et al. (2011) Prognostic value of NDRG1 and SPARC protein expression in breast cancer patients. Breast Cancer Res. Treat., 126, 1-14.
34. Nishio, S. et al. (2008) Cap43/NDRG1/Drg-1 is a molecular target for angiogenesis and a prognostic indicator in cervical adenocarcinoma. Cancer Lett., 264, 36-43.
35. Sugiki, T. et al. (2004) N-myc downregulated gene 1 is a phosphorylated protein in mast cells. Biol. Pharm. Bull., 27, 624-627.
36. Liang, S.X. et al. (2003) The effect of potent iron chelators on the regulation of p53: examination of the expression, localization and DNA-binding activity of p53 and the transactivation of WAF1. Carcinogenesis, 24, 1601-1614.
37. Le, N.T. et al. (2003) Potent iron chelators increase the mRNA levels of the universal cyclin-dependent kinase inhibitor p21(CIP1/WAF1), but paradoxically inhibit its translation: a potential mechanism of cell cycle dysregulation. Carcinogenesis, 24, 1045-1058.
38. Kurdistani, S.K. et al. (1998) Inhibition of tumor cell growth by RTP/rit42 and its responsiveness to p53 and DNA damage. Cancer Res., 58, 4439-4444.
39. Chen, Z. et al. (2012) The iron chelators Dp44mT and DFO inhibit TGF-β-induced epithelial-mesenchymal transition via up-regulation of N-Myc downstream-regulated gene 1 (NDRG1). J. Biol. Chem., 287, 17016-17028.
40. Liu, W. et al. (2012) N-myc downstream regulated gene 1 modulates Wnt-β-catenin signalling and pleiotropically suppresses metastasis. EMBO Mol. Med., 4, 93-108.
41. Yan, X. et al. (2008) N-Myc down-regulated gene 1 mediates proliferation, invasion, and apoptosis of hepatocellular carcinoma cells. Cancer Lett., 262, 133-142.
42. Liu, W. et al. (2011) KAI1 gene is engaged in NDRG1 gene-mediated metastasis suppression through the ATF3-NFkappaB complex in human prostate cancer. J. Biol. Chem., 286, 18949-18959.
43. Hosoi, F. et al. (2009) N-myc downstream regulated gene 1/Cap43 suppresses tumor growth and angiogenesis of pancreatic cancer through attenuation of inhibitor of kappaB kinase beta expression. Cancer Res., 69, 4983-4991.
44. Bandyopadhyay, S. et al. (2004) PTEN up-regulates the tumor metastasis suppressor gene Drg-1 in prostate and breast cancer. Cancer Res., 64, 7655-7660.
45. He, J. et al. (2010) The p85beta regulatory subunit of PI3K serves as a substrate for PTEN protein phosphatase activity during insulin mediated signaling. Biochem. Biophys. Res. Commun., 397, 513-519.
46. Pearce, L.R. et al. (2011) Protor-1 is required for efficient mTORC2-mediated activation of SGK1 in the kidney. Biochem. J., 436, 169-179.
47. Kovacevic, Z. et al. (2013) The iron-regulated metastasis suppressor NDRG1 targets NEDD4L, PTEN, and SMAD4 and inhibits the PI3K and Ras signaling pathways. Antioxid. Redox Signal., 18, 874-887.
48. Brasier, A.R. (2006) The NF-kappaB regulatory network. Cardiovasc. Toxicol., 6, 111-130.
49. Ghosh, S. et al. (2002) Missing pieces in the NF-kappaB puzzle. Cell, 109, S81-S96.
50. Wilczynski, J. et al. (2011) Targeting NF-κB and HIF-1 pathways for the treatment of cancer: part II. Arch. Immunol. Ther. Exp. (Warsz)., 59, 301-307.
51. Wilken, R. et al. (2011) Curcumin: a review of anti-cancer properties and therapeutic activity in head and neck squamous cell carcinoma. Mol. Cancer, 10, 12.
52. Tong, Y. et al. (2012) Enhanced TLR-induced NF-κB signaling and type I interferon responses in NLRC5 deficient mice. Cell Res., 22, 822-835.
53. Wu, Y. et al. (2010) TNF-alpha/NF-kappaB/Snail pathway in cancer cell migration and invasion. Br. J. Cancer, 102, 639-644.
54. Pham, C.G. et al. (2007) Upregulation of Twist-1 by NF-kappaB blocks cytotoxicity induced by chemotherapeutic drugs. Mol. Cell. Biol., 27, 3920-3935.
55. Moreau, M. et al. (2011) β-Catenin and NF-κB cooperate to regulate the uPA/uPAR system in cancer cells. Int. J. Cancer, 128, 1280-1292.
56. Farina, A.R. et al. (2011) Thioredoxin stimulates MMP-9 expression, deregulates the MMP-9/TIMP-1 equilibrium and promotes MMP-9 dependent invasion in human MDA-MB-231 breast cancer cells. FEBS Lett., 585, 3328-3336.
57. Lu, Y. et al. (2012) Apelin-APJ induces ICAM-1, VCAM-1 and MCP-1 expression via NF-κB/JNK signal pathway in human umbilical vein endothelial cells. Amino Acids, 43, 2125-2136.
58. Stanisavljevic, J. et al. (2011) The p65 subunit of NF-κB and PARP1 assist Snail1 in activating fibronectin transcription. J. Cell Sci., 124(Pt 24), 4161-4171.
59. Hada, N. et al. (2012) Receptor activator of NF-κB ligand-dependent expression of caveolin-1 in osteoclast precursors, and high dependency of osteoclastogenesis on exogenous lipoprotein. Bone, 50, 226-236.
60. Wu, X. et al. (2009) TNF induces caspase-dependent inflammation in renal endothelial cells through a Rho- and myosin light chain kinasedependent mechanism. Am. J. Physiol. Renal Physiol., 297, F316-F326.
61. Jeon, H.G. et al. (2011) Induction of caspase mediated apoptosis and down-regulation of nuclear factor-κB and Akt signaling are involved in the synergistic antitumor effect of gemcitabine and the histone deacetylase inhibitor trichostatin A in human bladder cancer cells. J. Urol., 186, 2084-2093.
62. Chi, F. et al. (2012) Vimentin and PSF act in concert to regulate IbeA+ E. coli K1 induced activation and nuclear translocation of NF-κB in human brain endothelial cells. PLoS One, 7, e35862.
63. Wilson, C. et al. (2008) Chemotherapy-induced CXC-chemokine/CXCchemokine receptor signaling in metastatic prostate cancer cells confers resistance to oxaliplatin through potentiation of nuclear factor-kappaB transcription and evasion of apoptosis. J. Pharmacol. Exp. Ther., 327, 746-759.
64. Murakami, Y. et al. (2010) Identification of sites subjected to serine/threonine phosphorylation by SGK1 affecting N-myc downstream-regulated gene 1 (NDRG1)/Cap43-dependent suppression of angiogenic CXC chemokine expression in human pancreatic cancer cells. Biochem. Biophys. Res. Commun., 396, 376-381.
65. Carnero, A. et al. (2008) The PTEN/PI3K/AKT signalling pathway in cancer, therapeutic implications. Curr. Cancer Drug Targets, 8, 187-198.
66. Engelman, J.A. (2009) Targeting PI3K signalling in cancer: opportunities, challenges and limitations. Nat. Rev. Cancer, 9, 550-562.
67. Katso, R. et al. (2001) Cellular function of phosphoinositide 3-kinases: implications for development, homeostasis, and cancer. Annu. Rev. Cell Dev. Biol., 17, 615-675.
68. Cantley, L.C. (2002) The phosphoinositide 3-kinase pathway. Science, 296, 1655-1657.
69. McDonald, P.C. et al. (2008) Rictor and integrin-linked kinase interact and regulate Akt phosphorylation and cancer cell survival. Cancer Res., 68, 1618-1624.
70. Yoshida, S. et al. (2011) Redox regulates mammalian target of rapamycin complex 1 (mTORC1) activity by modulating the TSC1/TSC2-Rheb GTPase pathway. J. Biol. Chem., 286, 32651-32660.
71. Dixon, K.M. et al. (2013) Dp44mT targets the AKT, TGF-β and ERK pathways via the metastasis suppressor NDRG1 in normal prostate epithelial cells and prostate cancer cells. Br. J. Cancer, 108, 409-419.
72. Steelman, L.S. et al. (2011) Roles of the Ras/Raf/MEK/ERK pathway in leukemia therapy. Leukemia, 25, 1080-1094.
73. Bao, X.H. et al. (2012) Esophageal cancer exhibits resistance to a novel IGF-1R inhibitor NVP-AEW541 with maintained RAS-MAPK activity. Anticancer Res., 32, 2827-2834.
74. Fucini, R.V. et al. (1999) Insulin-induced desensitization of extracellular signal-regulated kinase activation results from an inhibition of Raf activity independent of Ras activation and dissociation of the Grb2-SOS complex. J. Biol. Chem., 274, 18651-18658.
75. Hurley, J.B. et al. (1984) Homologies between signal transducing G proteins and ras gene products. Science, 226, 860-862.
76. Marais, R. et al. (1995) Ras recruits Raf-1 to the plasma membrane for activation by tyrosine phosphorylation. EMBO J., 14, 3136-3145.
77. McCubrey, J.A. et al. (2008) Targeting survival cascades induced by activation of Ras/Raf/MEK/ERK, PI3K/PTEN/Akt/mTOR and Jak/STAT pathways for effective leukemia therapy. Leukemia, 22, 708-722.
78. Tyner, J.W. et al. (2009) High-throughput sequencing screen reveals novel, transforming RAS mutations in myeloid leukemia patients. Blood, 113, 1749-1755.
79. Iglesias, M. et al. (2000) Blockade of Smad4 in transformed keratinocytes containing a Ras oncogene leads to hyperactivation of the Ras-dependent Erk signalling pathway associated with progression to undifferentiated carcinomas. Oncogene, 19, 4134-4145.
80. Mendoza, M.C. et al. (2011) The Ras-ERK and PI3K-mTOR pathways: cross-talk and compensation. Trends Biochem. Sci., 36, 320-328.
81. Arnaud, M. et al. (2004) Phosphorylation of Grb2-associated binder 2 on serine 623 by ERK MAPK regulates its association with the phosphatase SHP-2 and decreases STAT5 activation. J. Immunol., 173, 3962-3971.
82. Carr, B.I. et al. (2011) c-Met-Akt pathway-mediated enhancement of inhibitory c-Raf phosphorylation is involved in vitamin K1 and sorafenib synergy on HCC growth inhibition. Cancer Biol. Ther., 12, 531-538.
83. Zoncu, R. et al. (2011) mTOR: from growth signal integration to cancer, diabetes and ageing. Nat. Rev. Mol. Cell Biol., 12, 21-35.
84. Reddy, V.S. et al. (2008) Interleukin-18 stimulates fibronectin expression in primary human cardiac fibroblasts via PI3K-Akt-dependent NF-kappaB activation. J. Cell. Physiol., 215, 697-707.
85. Nisticò, P. et al. (2012) Epithelial-mesenchymal transition: general principles and pathological relevance with special emphasis on the role of matrix metalloproteinases. Cold Spring Harb. Perspect. Biol., 4, a011908.
86. Zhang, K. et al. (2009) Cortactin is involved in transforming growth factor-beta1-induced epithelial-mesenchymal transition in AML-12 cells. Acta Biochim. Biophys. Sin. (Shanghai)., 41, 839-845.
87. Tojkander, S. et al. (2012) Actin stress fibers-assembly, dynamics and biological roles. J. Cell Sci., 125(Pt 8), 1855-1864.
88. Kalluri, R. et al. (2009) The basics of epithelial-mesenchymal transition. J. Clin. Invest., 119, 1420-1428.
89. Voulgari, A. et al. (2009) Epithelial-mesenchymal transition in cancer metastasis: mechanisms, markers and strategies to overcome drug resistance in the clinic. Biochim. Biophys. Acta, 1796, 75-90.
90. Parvani, J.G. et al. (2011) Noncanonical TGF-β signaling during mammary tumorigenesis. J. Mammary Gland Biol. Neoplasia, 16, 127-146.
91. Koli, K. et al. (2001) Latency, activation, and binding proteins of TGFbeta. Microsc. Res. Tech., 52, 354-362.
92. Huang, T. et al. (2011) TGF-β signalling is mediated by two autonomously functioning TβRI:TβRII pairs. EMBO J., 30, 1263-1276.
93. Samanta, D. et al. (2012) Alterations in the Smad pathway in human cancers. Front. Biosci., 17, 1281-1293.
94. Matsuzaki, K. et al. (2009) Smad2 and Smad3 phosphorylated at both linker and COOH-terminal regions transmit malignant TGF-beta signal in later stages of human colorectal cancer. Cancer Res., 69, 5321-5330.
95. Moustakas, A. et al. (2007) Signaling networks guiding epithelial-mesenchymal transitions during embryogenesis and cancer progression. Cancer Sci., 98, 1512-1520.
96. Xu, J. et al. (2009) TGF-beta-induced epithelial to mesenchymal transition. Cell Res., 19, 156-172.
97. Ye, P. (2012) Modulation of epithelial tight junctions by TGF-beta 3 in cultured oral epithelial cells. Aust. Dent. J., 57, 11-17.
98. Zhang, Y.E. (2009) Non-Smad pathways in TGF-beta signaling. Cell Res., 19, 128-139.
99. Franch-Marro, X. et al. (2008) In vivo role of lipid adducts on Wingless. J. Cell Sci., 121(Pt 10), 1587-1592.
100. Kolligs, F.T. et al. (2002) Wnt/beta-catenin/tcf signaling: a critical pathway in gastrointestinal tumorigenesis. Digestion, 66, 131-144.
101. Angers, S. et al. (2009) Proximal events in Wnt signal transduction. Nat. Rev. Mol. Cell Biol., 10, 468-477.
102. Clevers, H. et al. (2012) Wnt/β-catenin signaling and disease. Cell, 149, 1192-1205.
103. Mitra, A. et al. (2012) DNAJB6 chaperones PP2A mediated dephosphorylation of GSK3β to downregulate β-catenin transcription target, osteopontin. Oncogene, 31, 4472-4483.
104. Hsu, Y.M. et al. (2007) KCl cotransporter-3 down-regulates E-cadherin/beta-catenin complex to promote epithelial-mesenchymal transition. Cancer Res., 67, 11064-11073.
105. Zhai, B. et al. (2008) Reduced expression of E-cadherin/catenin complex in hepatocellular carcinomas. World J. Gastroenterol., 14, 5665-5673.
106. Murray, J.T. et al. (2004) Exploitation of KESTREL to identify NDRG family members as physiological substrates for SGK1 and GSK3. Biochem. J., 384, 477-488.
107. Vicente-Manzanares, M. et al. (2011) Cell migration: an overview. Methods Mol. Biol., 769, 1-24.
108. Dominguez, R. et al. (2011) Actin structure and function. Annu. Rev. Biophys., 40, 169-186.
109. Blanchoin, L. et al. (2012) Actin cytoskeleton: a team effort during actin assembly. Curr. Biol., 22, R643-R645.
110. Frank, D.J. et al. (2006) Capping protein and the Arp2/3 complex regulate nonbundle actin filament assembly to indirectly control actin bundle positioning during Drosophila melanogaster bristle development. Mol. Biol. Cell, 17, 3930-3939.
111. Vlahou, G. et al. (2006) Rho GTPase signaling in Dictyostelium discoideum: insights from the genome. Eur. J. Cell Biol., 85, 947-959.
112. Webb, R.L. et al. (2009) A novel role for an APC2-Diaphanous complex in regulating actin organization in Drosophila. Development, 136, 1283-1293.
113. Takenawa, T. et al. (2007) The WASP-WAVE protein network: connecting the membrane to the cytoskeleton. Nat. Rev. Mol. Cell Biol., 8, 37-48.
114. Schafer, D.A. et al. (1996) Dynamics of capping protein and actin assembly in vitro: uncapping barbed ends by polyphosphoinositides. J. Cell Biol., 135, 169-179.
115. Weeds, A.G. et al. (1986) Preparation and characterization of pig plasma and platelet gelsolins. Eur. J. Biochem., 161, 69-76.
116. Gervasi, M. et al. (2012) JunB contributes to Id2 repression and the epithelial-mesenchymal transition in response to transforming growth factor-β. J. Cell Biol., 196, 589-603.
117. Shutova, M. et al. (2012) Functions of nonmuscle myosin II in assembly of the cellular contractile system. PLoS One, 7, e40814.
118. Katoh, K. et al. (2011) Rho-associated kinase-dependent contraction of stress fibres and the organization of focal adhesions. J. R. Soc. Interface, 8, 305-311.
119. Xue, Y. et al. (2011) Phosphatidylinositol 3'-kinase signaling pathway is essential for Rac1-induced hypoxia-inducible factor-1(alpha) and vascular endothelial growth factor expression. Am. J. Physiol. Heart Circ. Physiol., 300, H2169-H2176.
120. Lu, Q. et al. (2009) Signaling through Rho GTPase pathway as viable drug target. Curr. Med. Chem., 16, 1355-1365.
121. Gregory, S.L. et al. (2010) Signalling through the RhoGEF Pebble in Drosophila. IUBMB Life, 62, 290-295.
122. Rathinam, R. et al. (2011) Role of Rho GTPases and their regulators in cancer progression. Front. Biosci., 16, 2561-2571.
123. Boureux, A. et al. (2007) Evolution of the Rho family of ras-like GTPases in eukaryotes. Mol. Biol. Evol., 24, 203-216.
124. Amano, M. et al. (1996) Phosphorylation and activation of myosin by Rho-associated kinase (Rho-kinase). J. Biol. Chem., 271, 20246-20249.
125. Vidal, C. et al. (2002) Cdc42/Rac1-dependent activation of the p21-activated kinase (PAK) regulates human platelet lamellipodia spreading: implication of the cortical-actin binding protein cortactin. Blood, 100, 4462-4469.
126. Wirth, A. et al. (2003) Inhibition of contraction and myosin light chain phosphorylation in guinea-pig smooth muscle by p21-activated kinase 1. J. Physiol., 549, 489-500.
127. Ifere, G.O. et al. (2010) Cholesterol and phytosterols differentially regulate the expression of caveolin 1 and a downstream prostate cell growthsuppressor gene. Cancer Epidemiol., 34, 461-471.
128. Sun, J. et al. (2013) Targeting the metastasis suppressor, NDRG1, using novel iron chelators: regulation of stress fiber-mediated tumor cell migration via modulation of the ROCK1/pMLC2 signaling pathway. Mol. Pharmacol., 83, 454-469.