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Erschienen in: Clinical & Experimental Metastasis 5/2012

01.06.2012 | Research Paper

Insidious role of nitric oxide in migration/invasion of colon cancer cells by upregulating MMP-2/9 via activation of cGMP-PKG-ERK signaling pathways

verfasst von: Suboj Babykutty, Priya Suboj, Priya Srinivas, Asha S. Nair, K. Chandramohan, Srinivas Gopala

Erschienen in: Clinical & Experimental Metastasis | Ausgabe 5/2012

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Abstract

Nitric oxide (NO), an uncharged free radical is implicated in various physiological and pathological processes. The present study is an investigation on the effect of NO on proliferation, apoptosis and migration of colon cancer cells. Colon adenocarcinoma cells, WiDr, were used for the in vitro experiments. Tissues from colon adenocarcinoma, adjacent normal and inflammatory tissue and lymph node with metastasis were evaluated for iNOS, MMP-2/9 and Fra-1/Fra-2. NO increases the proliferation of cancer cells and simultaneously prevents apoptosis. Expression of MMP-2/9, RhoB and Rac-1 was enhanced by NO in a time dependent manner. Further, NO increased phosphorylation of ERK1/2 and induced nuclear translocation of Fra-1 and Fra-2. Electrophoretic mobility shift analysis and use of deletion mutant promoter constructs identified role of AP-1 in NO-mediated regulation of MMP-2/9. iNOS, MMP-2/9, Fra-1 and Fra-2 in normal and colon adenocarcinoma tissues were analyzed and it was found that increased expression of these proteins in cancer when compared to normal provides support to our in vitro findings. The study showed that the NO-cGMP-PKG promotes MMP-2/9 expression by activating ERK-1/2 and AP-1. This study reveals the insidious role of NO in imparting tumor aggressiveness.
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Literatur
1.
Zurück zum Zitat Bentz BG, Simmons RL, Haines GK 3rd et al (2000) The yin and yang of nitric oxide: reflections on the physiology and pathophysiology of NO. Head Neck 22(1):71–83PubMedCrossRef Bentz BG, Simmons RL, Haines GK 3rd et al (2000) The yin and yang of nitric oxide: reflections on the physiology and pathophysiology of NO. Head Neck 22(1):71–83PubMedCrossRef
2.
Zurück zum Zitat Moncada S, Higgs A (1993) The l-arginine-nitric oxide pathway. N Engl J Med 329(27):2002–2012PubMedCrossRef Moncada S, Higgs A (1993) The l-arginine-nitric oxide pathway. N Engl J Med 329(27):2002–2012PubMedCrossRef
3.
Zurück zum Zitat Knowles RG, Moncada S (1994) Nitric oxide synthases in mammals. Biochem J 298(Pt 2):249–258PubMed Knowles RG, Moncada S (1994) Nitric oxide synthases in mammals. Biochem J 298(Pt 2):249–258PubMed
4.
Zurück zum Zitat Mocellin S, Bronte V, Nitti D (2007) Nitric oxide, a double edged sword in cancer biology: searching for therapeutic opportunities. Med Res Rev 27(3):317–352PubMedCrossRef Mocellin S, Bronte V, Nitti D (2007) Nitric oxide, a double edged sword in cancer biology: searching for therapeutic opportunities. Med Res Rev 27(3):317–352PubMedCrossRef
5.
Zurück zum Zitat Droge W (2002) Free radicals in the physiological control of cell function. Physiol Rev 82(1):47–95PubMed Droge W (2002) Free radicals in the physiological control of cell function. Physiol Rev 82(1):47–95PubMed
6.
Zurück zum Zitat Hickok JR, Thomas DD (2010) Nitric oxide and cancer therapy: the emperor has NO clothes. Curr Pharm Des 16(4):381–391PubMedCrossRef Hickok JR, Thomas DD (2010) Nitric oxide and cancer therapy: the emperor has NO clothes. Curr Pharm Des 16(4):381–391PubMedCrossRef
7.
Zurück zum Zitat Ridnour LA, Thomas DD, Switzer C et al (2008) Molecular mechanisms for discrete nitric oxide levels in cancer. Nitric Oxide 19(2):73–76PubMedCrossRef Ridnour LA, Thomas DD, Switzer C et al (2008) Molecular mechanisms for discrete nitric oxide levels in cancer. Nitric Oxide 19(2):73–76PubMedCrossRef
8.
Zurück zum Zitat Page-McCaw A, Ewald AJ, Werb Z (2007) Matrix metalloproteinases and the regulation of tissue remodelling. Nat Rev Mol Cell Biol 8(3):221–233PubMedCrossRef Page-McCaw A, Ewald AJ, Werb Z (2007) Matrix metalloproteinases and the regulation of tissue remodelling. Nat Rev Mol Cell Biol 8(3):221–233PubMedCrossRef
9.
Zurück zum Zitat Sternlicht MD, Werb Z (2001) How matrix metalloproteinases regulate cell behavior. Annu Rev Cell Dev Biol 17:463–516PubMedCrossRef Sternlicht MD, Werb Z (2001) How matrix metalloproteinases regulate cell behavior. Annu Rev Cell Dev Biol 17:463–516PubMedCrossRef
10.
Zurück zum Zitat Coussens LM, Fingleton B, Matrisian LM (2002) Matrix metalloproteinase inhibitors and cancer: trials and tribulations. Science 295(5564):2387–2392PubMedCrossRef Coussens LM, Fingleton B, Matrisian LM (2002) Matrix metalloproteinase inhibitors and cancer: trials and tribulations. Science 295(5564):2387–2392PubMedCrossRef
11.
Zurück zum Zitat Egeblad M, Werb Z (2002) New functions for the matrix metalloproteinases in cancer progression. Nat Rev Cancer 2(3):161–174PubMedCrossRef Egeblad M, Werb Z (2002) New functions for the matrix metalloproteinases in cancer progression. Nat Rev Cancer 2(3):161–174PubMedCrossRef
12.
Zurück zum Zitat Tamura T, Nakanishi T, Kimura Y et al (1996) Nitric oxide mediates interleukin-1-induced matrix degradation and basic fibroblast growth factor release in cultured rabbit articular chondrocytes: a possible mechanism of pathological neovascularization in arthritis. Endocrinology 137(9):3729–3737PubMedCrossRef Tamura T, Nakanishi T, Kimura Y et al (1996) Nitric oxide mediates interleukin-1-induced matrix degradation and basic fibroblast growth factor release in cultured rabbit articular chondrocytes: a possible mechanism of pathological neovascularization in arthritis. Endocrinology 137(9):3729–3737PubMedCrossRef
13.
Zurück zum Zitat Orucevic A, Bechberger J, Green AM et al (1999) Nitric-oxide production by murine mammary adenocarcinoma cells promotes tumor-cell invasiveness. Int J Cancer 81(6):889–896PubMedCrossRef Orucevic A, Bechberger J, Green AM et al (1999) Nitric-oxide production by murine mammary adenocarcinoma cells promotes tumor-cell invasiveness. Int J Cancer 81(6):889–896PubMedCrossRef
14.
Zurück zum Zitat Burlaka AP, Sidorik EP, Ganusevich II et al (2006) Effects of radical oxygen species and NO: formation of intracellular hypoxia and activation of matrix metalloproteinases in tumor tissues. Exp Oncol 28(1):49–53PubMed Burlaka AP, Sidorik EP, Ganusevich II et al (2006) Effects of radical oxygen species and NO: formation of intracellular hypoxia and activation of matrix metalloproteinases in tumor tissues. Exp Oncol 28(1):49–53PubMed
15.
Zurück zum Zitat Zaragoza C, Balbin M, Lopez-Otin C et al (2002) Nitric oxide regulates matrix metalloprotease-13 expression and activity in endothelium. Kidney Int 61(3):804–808PubMedCrossRef Zaragoza C, Balbin M, Lopez-Otin C et al (2002) Nitric oxide regulates matrix metalloprotease-13 expression and activity in endothelium. Kidney Int 61(3):804–808PubMedCrossRef
16.
Zurück zum Zitat Lopez-Rivera E, Lizarbe TR, Martinez-Moreno M et al (2005) Matrix metalloproteinase 13 mediates nitric oxide activation of endothelial cell migration. Proc Natl Acad Sci USA 102(10):3685–3690PubMedCrossRef Lopez-Rivera E, Lizarbe TR, Martinez-Moreno M et al (2005) Matrix metalloproteinase 13 mediates nitric oxide activation of endothelial cell migration. Proc Natl Acad Sci USA 102(10):3685–3690PubMedCrossRef
17.
Zurück zum Zitat Ridnour LA, Windhausen AN, Isenberg JS et al (2007) Nitric oxide regulates matrix metalloproteinase-9 activity by guanylyl-cyclase-dependent and -independent pathways. Proc Natl Acad Sci U S A 104(43):16898–16903PubMedCrossRef Ridnour LA, Windhausen AN, Isenberg JS et al (2007) Nitric oxide regulates matrix metalloproteinase-9 activity by guanylyl-cyclase-dependent and -independent pathways. Proc Natl Acad Sci U S A 104(43):16898–16903PubMedCrossRef
18.
Zurück zum Zitat Marcet-Palacios M, Graham K, Cass C et al (2003) Nitric oxide and cyclic GMP increase the expression of matrix metalloproteinase-9 in vascular smooth muscle. J Pharmacol Exp Ther 307(1):429–436PubMedCrossRef Marcet-Palacios M, Graham K, Cass C et al (2003) Nitric oxide and cyclic GMP increase the expression of matrix metalloproteinase-9 in vascular smooth muscle. J Pharmacol Exp Ther 307(1):429–436PubMedCrossRef
19.
Zurück zum Zitat Bove PF, Wesley UV, Greul AK et al (2007) Nitric oxide promotes airway epithelial wound repair through enhanced activation of MMP-9. Am J Respir Cell Mol Biol 36(2):138–146PubMedCrossRef Bove PF, Wesley UV, Greul AK et al (2007) Nitric oxide promotes airway epithelial wound repair through enhanced activation of MMP-9. Am J Respir Cell Mol Biol 36(2):138–146PubMedCrossRef
20.
Zurück zum Zitat Kojima H, Nakatsubo N, Kikuchi K et al (1998) Direct evidence of NO production in rat hippocampus and cortex using a new fluorescent indicator: DAF-2 DA. NeuroReport 9(15):3345–3348PubMedCrossRef Kojima H, Nakatsubo N, Kikuchi K et al (1998) Direct evidence of NO production in rat hippocampus and cortex using a new fluorescent indicator: DAF-2 DA. NeuroReport 9(15):3345–3348PubMedCrossRef
21.
Zurück zum Zitat Tsikas D, Fuchs I, Gutzki FM et al (1998) Measurement of nitrite and nitrate in plasma, serum and urine of humans by high-performance liquid chromatography, the Griess assay, chemiluminescence and gas chromatography-mass spectrometry: interferences by biogenic amines and N(G)-nitro-l-arginine analogs. J Chromatogr B Biomed Sci Appl 715(2):441–444 (discussion 5-8)PubMedCrossRef Tsikas D, Fuchs I, Gutzki FM et al (1998) Measurement of nitrite and nitrate in plasma, serum and urine of humans by high-performance liquid chromatography, the Griess assay, chemiluminescence and gas chromatography-mass spectrometry: interferences by biogenic amines and N(G)-nitro-l-arginine analogs. J Chromatogr B Biomed Sci Appl 715(2):441–444 (discussion 5-8)PubMedCrossRef
22.
Zurück zum Zitat Srinivas P, Gopinath G, Banerji A et al (2004) Plumbagin induces reactive oxygen species, which mediate apoptosis in human cervical cancer cells. Mol Carcinog 40(4):201–211PubMedCrossRef Srinivas P, Gopinath G, Banerji A et al (2004) Plumbagin induces reactive oxygen species, which mediate apoptosis in human cervical cancer cells. Mol Carcinog 40(4):201–211PubMedCrossRef
23.
24.
Zurück zum Zitat Du M, Islam MM, Lin L et al (1997) Promotion of proliferation of murine BALB/C3T3 fibroblasts mediated by nitric oxide at lower concentrations. Biochem Mol Biol Int 41(3):625–631PubMed Du M, Islam MM, Lin L et al (1997) Promotion of proliferation of murine BALB/C3T3 fibroblasts mediated by nitric oxide at lower concentrations. Biochem Mol Biol Int 41(3):625–631PubMed
25.
Zurück zum Zitat Luczak K, Balcerczyk A, Soszynski M et al (2004) Low concentration of oxidant and nitric oxide donors stimulate proliferation of human endothelial cells in vitro. Cell Biol Int 28(6):483–486PubMedCrossRef Luczak K, Balcerczyk A, Soszynski M et al (2004) Low concentration of oxidant and nitric oxide donors stimulate proliferation of human endothelial cells in vitro. Cell Biol Int 28(6):483–486PubMedCrossRef
26.
Zurück zum Zitat Mei JM, Borchert GL, Donald SP et al (2002) Matrix metalloproteinase(s) mediate(s) NO-induced dissociation of beta-catenin from membrane bound E-cadherin and formation of nuclear beta-catenin/LEF-1 complex. Carcinogenesis 23(12):2119–2122PubMedCrossRef Mei JM, Borchert GL, Donald SP et al (2002) Matrix metalloproteinase(s) mediate(s) NO-induced dissociation of beta-catenin from membrane bound E-cadherin and formation of nuclear beta-catenin/LEF-1 complex. Carcinogenesis 23(12):2119–2122PubMedCrossRef
27.
Zurück zum Zitat Mei JM, Hord NG, Winterstein DF et al (2000) Differential formation of beta-catenin/lymphoid enhancer factor-1 DNA binding complex induced by nitric oxide in mouse colonic epithelial cells differing in adenomatous polyposis coli (Apc) genotype. Cancer Res 60(13):3379–3383PubMed Mei JM, Hord NG, Winterstein DF et al (2000) Differential formation of beta-catenin/lymphoid enhancer factor-1 DNA binding complex induced by nitric oxide in mouse colonic epithelial cells differing in adenomatous polyposis coli (Apc) genotype. Cancer Res 60(13):3379–3383PubMed
28.
Zurück zum Zitat Pervin S, Singh R, Hernandez E et al (2007) Nitric oxide in physiologic concentrations targets the translational machinery to increase the proliferation of human breast cancer cells: involvement of mammalian target of rapamycin/eIF4E pathway. Cancer Res 67(1):289–299PubMedCrossRef Pervin S, Singh R, Hernandez E et al (2007) Nitric oxide in physiologic concentrations targets the translational machinery to increase the proliferation of human breast cancer cells: involvement of mammalian target of rapamycin/eIF4E pathway. Cancer Res 67(1):289–299PubMedCrossRef
29.
Zurück zum Zitat Mannick JB (2007) Regulation of apoptosis by protein S-nitrosylation. Amino Acids 32(4):523–526PubMedCrossRef Mannick JB (2007) Regulation of apoptosis by protein S-nitrosylation. Amino Acids 32(4):523–526PubMedCrossRef
30.
Zurück zum Zitat Kim YM, Talanian RV, Billiar TR (1997) Nitric oxide inhibits apoptosis by preventing increases in caspase-3-like activity via two distinct mechanisms. J Biol Chem 272(49):31138–31148PubMedCrossRef Kim YM, Talanian RV, Billiar TR (1997) Nitric oxide inhibits apoptosis by preventing increases in caspase-3-like activity via two distinct mechanisms. J Biol Chem 272(49):31138–31148PubMedCrossRef
31.
Zurück zum Zitat Potter CL, Hanson PJ (2000) Exogenous nitric oxide inhibits apoptosis in guinea pig gastric mucous cells. Gut 46(2):156–162PubMedCrossRef Potter CL, Hanson PJ (2000) Exogenous nitric oxide inhibits apoptosis in guinea pig gastric mucous cells. Gut 46(2):156–162PubMedCrossRef
32.
Zurück zum Zitat Pullen NA, Fillmore HL (2010) Induction of matrix metalloproteinase-1 and glioma cell motility by nitric oxide. J Neurooncol 96(2):201–209PubMedCrossRef Pullen NA, Fillmore HL (2010) Induction of matrix metalloproteinase-1 and glioma cell motility by nitric oxide. J Neurooncol 96(2):201–209PubMedCrossRef
33.
Zurück zum Zitat Lala PK, Orucevic A (1998) Role of nitric oxide in tumor progression: lessons from experimental tumors. Cancer Metastasis Rev 17(1):91–106PubMedCrossRef Lala PK, Orucevic A (1998) Role of nitric oxide in tumor progression: lessons from experimental tumors. Cancer Metastasis Rev 17(1):91–106PubMedCrossRef
34.
Zurück zum Zitat McCarthy SM, Bove PF, Matthews DE et al (2008) Nitric oxide regulation of MMP-9 activation and its relationship to modifications of the cysteine switch. Biochemistry 47(21):5832–5840PubMedCrossRef McCarthy SM, Bove PF, Matthews DE et al (2008) Nitric oxide regulation of MMP-9 activation and its relationship to modifications of the cysteine switch. Biochemistry 47(21):5832–5840PubMedCrossRef
35.
Zurück zum Zitat Harris LK, McCormick J, Cartwright JE et al (2008) S-nitrosylation of proteins at the leading edge of migrating trophoblasts by inducible nitric oxide synthase promotes trophoblast invasion. Exp Cell Res 314(8):1765–1776PubMedCrossRef Harris LK, McCormick J, Cartwright JE et al (2008) S-nitrosylation of proteins at the leading edge of migrating trophoblasts by inducible nitric oxide synthase promotes trophoblast invasion. Exp Cell Res 314(8):1765–1776PubMedCrossRef
36.
Zurück zum Zitat Ishii Y, Ogura T, Tatemichi M et al (2003) Induction of matrix metalloproteinase gene transcription by nitric oxide and mechanisms of MMP-1 gene induction in human melanoma cell lines. Int J Cancer 103(2):161–168PubMedCrossRef Ishii Y, Ogura T, Tatemichi M et al (2003) Induction of matrix metalloproteinase gene transcription by nitric oxide and mechanisms of MMP-1 gene induction in human melanoma cell lines. Int J Cancer 103(2):161–168PubMedCrossRef
37.
Zurück zum Zitat Lizarbe TR, Garcia-Rama C, Tarin C et al (2008) Nitric oxide elicits functional MMP-13 protein-tyrosine nitration during wound repair. Faseb J 22(9):3207–3215PubMedCrossRef Lizarbe TR, Garcia-Rama C, Tarin C et al (2008) Nitric oxide elicits functional MMP-13 protein-tyrosine nitration during wound repair. Faseb J 22(9):3207–3215PubMedCrossRef
38.
Zurück zum Zitat Maeda H, Okamoto T, Akaike T (1998) Human matrix metalloprotease activation by insults of bacterial infection involving proteases and free radicals. Biol Chem 379(2):193–200PubMedCrossRef Maeda H, Okamoto T, Akaike T (1998) Human matrix metalloprotease activation by insults of bacterial infection involving proteases and free radicals. Biol Chem 379(2):193–200PubMedCrossRef
39.
Zurück zum Zitat Rajagopalan S, Meng XP, Ramasamy S et al (1996) Reactive oxygen species produced by macrophage-derived foam cells regulate the activity of vascular matrix metalloproteinases in vitro. Implications for atherosclerotic plaque stability. J Clin Invest 98(11):2572–2579PubMedCrossRef Rajagopalan S, Meng XP, Ramasamy S et al (1996) Reactive oxygen species produced by macrophage-derived foam cells regulate the activity of vascular matrix metalloproteinases in vitro. Implications for atherosclerotic plaque stability. J Clin Invest 98(11):2572–2579PubMedCrossRef
40.
Zurück zum Zitat Bosca L, Zeini M, Traves PG et al (2005) Nitric oxide and cell viability in inflammatory cells: a role for NO in macrophage function and fate. Toxicology 208(2):249–258PubMedCrossRef Bosca L, Zeini M, Traves PG et al (2005) Nitric oxide and cell viability in inflammatory cells: a role for NO in macrophage function and fate. Toxicology 208(2):249–258PubMedCrossRef
41.
Zurück zum Zitat Shah NS, Billiar TR (1998) Role of nitric oxide in inflammation and tissue injury during endotoxemia and hemorrhagic shock. Environ Health Perspect 106(Suppl 5):1139–1143PubMedCrossRef Shah NS, Billiar TR (1998) Role of nitric oxide in inflammation and tissue injury during endotoxemia and hemorrhagic shock. Environ Health Perspect 106(Suppl 5):1139–1143PubMedCrossRef
42.
Zurück zum Zitat Raulo SM, Sorsa T, Tervahartiala T et al (2001) MMP-9 as a marker of inflammation in tracheal epithelial lining fluid (TELF) and in bronchoalveolar fluid (BALF) of COPD horses. Equine Vet J 33(2):128–136PubMedCrossRef Raulo SM, Sorsa T, Tervahartiala T et al (2001) MMP-9 as a marker of inflammation in tracheal epithelial lining fluid (TELF) and in bronchoalveolar fluid (BALF) of COPD horses. Equine Vet J 33(2):128–136PubMedCrossRef
43.
Zurück zum Zitat Warner RL, Bhagavathula N, Nerusu KC et al (2004) Matrix metalloproteinases in acute inflammation: induction of MMP-3 and MMP-9 in fibroblasts and epithelial cells following exposure to pro-inflammatory mediators in vitro. Exp Mol Pathol 76(3):189–195PubMedCrossRef Warner RL, Bhagavathula N, Nerusu KC et al (2004) Matrix metalloproteinases in acute inflammation: induction of MMP-3 and MMP-9 in fibroblasts and epithelial cells following exposure to pro-inflammatory mediators in vitro. Exp Mol Pathol 76(3):189–195PubMedCrossRef
44.
Zurück zum Zitat Chen JH, Lin HH, Chiang TA et al (2008) Gaseous nitrogen oxide promotes human lung cancer cell line A549 migration, invasion, and metastasis via iNOS-mediated MMP-2 production. Toxicol Sci 106(2):364–375PubMedCrossRef Chen JH, Lin HH, Chiang TA et al (2008) Gaseous nitrogen oxide promotes human lung cancer cell line A549 migration, invasion, and metastasis via iNOS-mediated MMP-2 production. Toxicol Sci 106(2):364–375PubMedCrossRef
45.
Zurück zum Zitat Malik MT, Kakar SS (2006) Regulation of angiogenesis and invasion by human Pituitary tumor transforming gene (PTTG) through increased expression and secretion of matrix metalloproteinase-2 (MMP-2). Mol Cancer 5:61PubMedCrossRef Malik MT, Kakar SS (2006) Regulation of angiogenesis and invasion by human Pituitary tumor transforming gene (PTTG) through increased expression and secretion of matrix metalloproteinase-2 (MMP-2). Mol Cancer 5:61PubMedCrossRef
46.
Zurück zum Zitat Jespersen C, Doller A, el Akool S et al (2009) Molecular mechanisms of nitric oxide-dependent inhibition of TPA-induced matrix metalloproteinase-9 (MMP-9) in MCF-7 cells. J Cell Physiol 219(2):276–287PubMedCrossRef Jespersen C, Doller A, el Akool S et al (2009) Molecular mechanisms of nitric oxide-dependent inhibition of TPA-induced matrix metalloproteinase-9 (MMP-9) in MCF-7 cells. J Cell Physiol 219(2):276–287PubMedCrossRef
47.
Zurück zum Zitat Zaragoza C, Soria E, Lopez E et al (2002) Activation of the mitogen activated protein kinase extracellular signal-regulated kinase 1 and 2 by the nitric oxide-cGMP-cGMP-dependent protein kinase axis regulates the expression of matrix metalloproteinase 13 in vascular endothelial cells. Mol Pharmacol 62(4):927–935PubMedCrossRef Zaragoza C, Soria E, Lopez E et al (2002) Activation of the mitogen activated protein kinase extracellular signal-regulated kinase 1 and 2 by the nitric oxide-cGMP-cGMP-dependent protein kinase axis regulates the expression of matrix metalloproteinase 13 in vascular endothelial cells. Mol Pharmacol 62(4):927–935PubMedCrossRef
48.
Zurück zum Zitat Hovsepian E, Mirkin GA, Penas F et al (2011) Modulation of inflammatory response and parasitism by 15-Deoxy-Delta(12,14) prostaglandin J(2) in Trypanosoma cruzi-infected cardiomyocytes. Int J Parasitol 41(5):553–562PubMedCrossRef Hovsepian E, Mirkin GA, Penas F et al (2011) Modulation of inflammatory response and parasitism by 15-Deoxy-Delta(12,14) prostaglandin J(2) in Trypanosoma cruzi-infected cardiomyocytes. Int J Parasitol 41(5):553–562PubMedCrossRef
49.
Zurück zum Zitat Komalavilas P, Shah PK, Jo H et al (1999) Activation of mitogen-activated protein kinase pathways by cyclic GMP and cyclic GMP-dependent protein kinase in contractile vascular smooth muscle cells. J Biol Chem 274(48):34301–34309PubMedCrossRef Komalavilas P, Shah PK, Jo H et al (1999) Activation of mitogen-activated protein kinase pathways by cyclic GMP and cyclic GMP-dependent protein kinase in contractile vascular smooth muscle cells. J Biol Chem 274(48):34301–34309PubMedCrossRef
50.
Zurück zum Zitat Parri M, Chiarugi P (2010) Rac and Rho GTPases in cancer cell motility control. Cell Commun Signal 8:23PubMedCrossRef Parri M, Chiarugi P (2010) Rac and Rho GTPases in cancer cell motility control. Cell Commun Signal 8:23PubMedCrossRef
51.
Zurück zum Zitat Ridley AJ (2006) Rho GTPases and actin dynamics in membrane protrusions and vesicle trafficking. Trends Cell Biol 16(10):522–529PubMedCrossRef Ridley AJ (2006) Rho GTPases and actin dynamics in membrane protrusions and vesicle trafficking. Trends Cell Biol 16(10):522–529PubMedCrossRef
52.
Zurück zum Zitat Loirand G, Guilluy C, Pacaud P (2006) Regulation of Rho proteins by phosphorylation in the cardiovascular system. Trends Cardiovasc Med 16(6):199–204PubMedCrossRef Loirand G, Guilluy C, Pacaud P (2006) Regulation of Rho proteins by phosphorylation in the cardiovascular system. Trends Cardiovasc Med 16(6):199–204PubMedCrossRef
53.
Zurück zum Zitat Sauzeau V, Rolli-Derkinderen M, Marionneau C et al (2003) RhoA expression is controlled by nitric oxide through cGMP-dependent protein kinase activation. J Biol Chem 278(11):9472–9480PubMedCrossRef Sauzeau V, Rolli-Derkinderen M, Marionneau C et al (2003) RhoA expression is controlled by nitric oxide through cGMP-dependent protein kinase activation. J Biol Chem 278(11):9472–9480PubMedCrossRef
54.
Zurück zum Zitat Chen SC, Liu YC, Shyu KG et al (2008) Acute hypoxia to endothelial cells induces activating transcription factor 3 (ATF3) expression that is mediated via nitric oxide. Atherosclerosis 201(2):281–288PubMedCrossRef Chen SC, Liu YC, Shyu KG et al (2008) Acute hypoxia to endothelial cells induces activating transcription factor 3 (ATF3) expression that is mediated via nitric oxide. Atherosclerosis 201(2):281–288PubMedCrossRef
55.
Zurück zum Zitat Sandau KB, Fandrey J, Brune B (2001) Accumulation of HIF-1alpha under the influence of nitric oxide. Blood 97(4):1009–1015PubMedCrossRef Sandau KB, Fandrey J, Brune B (2001) Accumulation of HIF-1alpha under the influence of nitric oxide. Blood 97(4):1009–1015PubMedCrossRef
56.
Zurück zum Zitat Brune B, Zhou J (2003) The role of nitric oxide (NO) in stability regulation of hypoxia inducible factor-1alpha (HIF-1alpha). Curr Med Chem 10(10):845–855PubMedCrossRef Brune B, Zhou J (2003) The role of nitric oxide (NO) in stability regulation of hypoxia inducible factor-1alpha (HIF-1alpha). Curr Med Chem 10(10):845–855PubMedCrossRef
57.
Zurück zum Zitat Kim JW, Gao P, Liu YC et al (2007) Hypoxia-inducible factor 1 and dysregulated c-Myc cooperatively induce vascular endothelial growth factor and metabolic switches hexokinase 2 and pyruvate dehydrogenase kinase 1. Mol Cell Biol 27(21):7381–7393PubMedCrossRef Kim JW, Gao P, Liu YC et al (2007) Hypoxia-inducible factor 1 and dysregulated c-Myc cooperatively induce vascular endothelial growth factor and metabolic switches hexokinase 2 and pyruvate dehydrogenase kinase 1. Mol Cell Biol 27(21):7381–7393PubMedCrossRef
58.
Zurück zum Zitat Dulak J, Jozkowicz A (2002) Nitric oxide and angiogenic activity of endothelial cells: direct or VEGF-dependent effect? Cardiovasc Res 56(3):487–488 (author reply 9-91)PubMedCrossRef Dulak J, Jozkowicz A (2002) Nitric oxide and angiogenic activity of endothelial cells: direct or VEGF-dependent effect? Cardiovasc Res 56(3):487–488 (author reply 9-91)PubMedCrossRef
59.
Zurück zum Zitat Hebert C, Siavash H, Norris K et al (2005) Endostatin inhibits nitric oxide and diminishes VEGF and collagen XVIII in squamous carcinoma cells. Int J Cancer 114(2):195–201PubMedCrossRef Hebert C, Siavash H, Norris K et al (2005) Endostatin inhibits nitric oxide and diminishes VEGF and collagen XVIII in squamous carcinoma cells. Int J Cancer 114(2):195–201PubMedCrossRef
60.
Zurück zum Zitat Tian X, Cong M, Zhou W et al (2008) Relationship between protein expression of VEGF-C, MMP-2 and lymph node metastasis in papillary thyroid cancer. J Int Med Res 36(4):699–703PubMed Tian X, Cong M, Zhou W et al (2008) Relationship between protein expression of VEGF-C, MMP-2 and lymph node metastasis in papillary thyroid cancer. J Int Med Res 36(4):699–703PubMed
61.
Zurück zum Zitat Imler JL, Wasylyk B (1989) AP1, a composite transcription factor implicated in abnormal growth control. Prog Growth Factor Res 1(2):69–77PubMedCrossRef Imler JL, Wasylyk B (1989) AP1, a composite transcription factor implicated in abnormal growth control. Prog Growth Factor Res 1(2):69–77PubMedCrossRef
62.
Zurück zum Zitat Leaner VD, Chick JF, Donninger H et al (2009) Inhibition of AP-1 transcriptional activity blocks the migration, invasion, and experimental metastasis of murine osteosarcoma. Am J Pathol 174(1):265–275PubMedCrossRef Leaner VD, Chick JF, Donninger H et al (2009) Inhibition of AP-1 transcriptional activity blocks the migration, invasion, and experimental metastasis of murine osteosarcoma. Am J Pathol 174(1):265–275PubMedCrossRef
63.
Zurück zum Zitat Knipp BS, Ailawadi G, Ford JW et al (2004) Increased MMP-9 expression and activity by aortic smooth muscle cells after nitric oxide synthase inhibition is associated with increased nuclear factor-kappaB and activator protein-1 activity. J Surg Res 116(1):70–80PubMedCrossRef Knipp BS, Ailawadi G, Ford JW et al (2004) Increased MMP-9 expression and activity by aortic smooth muscle cells after nitric oxide synthase inhibition is associated with increased nuclear factor-kappaB and activator protein-1 activity. J Surg Res 116(1):70–80PubMedCrossRef
64.
Zurück zum Zitat Tkach V, Tulchinsky E, Lukanidin E et al (2003) Role of the Fos family members, c-Fos, Fra-1 and Fra-2, in the regulation of cell motility. Oncogene 22(32):5045–5054PubMedCrossRef Tkach V, Tulchinsky E, Lukanidin E et al (2003) Role of the Fos family members, c-Fos, Fra-1 and Fra-2, in the regulation of cell motility. Oncogene 22(32):5045–5054PubMedCrossRef
65.
Zurück zum Zitat Zhang Q, Kleeberger SR, Reddy SP (2004) DEP-induced fra-1 expression correlates with a distinct activation of AP-1-dependent gene transcription in the lung. Am J Physiol Lung Cell Mol Physiol 286(2):L427–L436PubMedCrossRef Zhang Q, Kleeberger SR, Reddy SP (2004) DEP-induced fra-1 expression correlates with a distinct activation of AP-1-dependent gene transcription in the lung. Am J Physiol Lung Cell Mol Physiol 286(2):L427–L436PubMedCrossRef
66.
Zurück zum Zitat Singh NK, Quyen DV, Kundumani-Sridharan V et al (2010) AP-1 (Fra-1/c-Jun)-mediated induction of expression of matrix metalloproteinase-2 is required for 15S-hydroxyeicosatetraenoic acid-induced angiogenesis. J Biol Chem 285(22):16830–16843PubMedCrossRef Singh NK, Quyen DV, Kundumani-Sridharan V et al (2010) AP-1 (Fra-1/c-Jun)-mediated induction of expression of matrix metalloproteinase-2 is required for 15S-hydroxyeicosatetraenoic acid-induced angiogenesis. J Biol Chem 285(22):16830–16843PubMedCrossRef
67.
Zurück zum Zitat Franchi A, Santucci M, Masini E et al (2002) Expression of matrix metalloproteinase 1, matrix metalloproteinase 2, and matrix metalloproteinase 9 in carcinoma of the head and neck. Cancer 95(9):1902–1910PubMedCrossRef Franchi A, Santucci M, Masini E et al (2002) Expression of matrix metalloproteinase 1, matrix metalloproteinase 2, and matrix metalloproteinase 9 in carcinoma of the head and neck. Cancer 95(9):1902–1910PubMedCrossRef
68.
Zurück zum Zitat Sun MH, Han XC, Jia MK et al (2005) Expressions of inducible nitric oxide synthase and matrix metalloproteinase-9 and their effects on angiogenesis and progression of hepatocellular carcinoma. World J Gastroenterol 11(38):5931–5937PubMed Sun MH, Han XC, Jia MK et al (2005) Expressions of inducible nitric oxide synthase and matrix metalloproteinase-9 and their effects on angiogenesis and progression of hepatocellular carcinoma. World J Gastroenterol 11(38):5931–5937PubMed
Metadaten
Titel
Insidious role of nitric oxide in migration/invasion of colon cancer cells by upregulating MMP-2/9 via activation of cGMP-PKG-ERK signaling pathways
verfasst von
Suboj Babykutty
Priya Suboj
Priya Srinivas
Asha S. Nair
K. Chandramohan
Srinivas Gopala
Publikationsdatum
01.06.2012
Verlag
Springer Netherlands
Erschienen in
Clinical & Experimental Metastasis / Ausgabe 5/2012
Print ISSN: 0262-0898
Elektronische ISSN: 1573-7276
DOI
https://doi.org/10.1007/s10585-012-9464-6

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