Skip to main content
SpringerLink
Log in

S-Nitrosylation – How Cancer Cells Say NO to Cell Death

  • Chapter
  • First Online:
Book cover Nitric Oxide (NO) and Cancer

Part of the book series: Cancer Drug Discovery and Development ((CDD&D))

  • 1052 Accesses

Abstract

Nitric oxide (NO) is a highly reactive gaseous free radical that regulates various physiological and pathological processes. Of these functions, the role of NO in the transformation, growth, and metastasis of cancers has generated particular interest. However, research describing the role of NO in cancers seems to be conflicting – some studies describe the suppressive role of NO in cancers, while numerous other studies describe the positive role of NO in tumor survival and progression. In this review, we shall examine the various roles of NO with a focus on how NO regulates tumor microenvironment and the various phases of tumor progression from neoplastic evolution, tumor growth, and metastasis. We will also discuss how NO-mediated S-nitrosylation, or covalent attachment of NO to protein cysteine thiols, regulates carcinogenesis by modulating proteins involved in the different phases of cancer development.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Log in via an institution
Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 169.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 219.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 219.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

Abbreviations

NO::

nitric oxide

NOS::

NO synthases

SNO::

S-nitrosothiol

RNOS::

reactive nitrogen–oxygen species

Bcl-2::

B-cell lymphoma-2

c-FLIP::

cellular FLICE-inhibitory protein

DISC::

death-inducing signaling complex

TNF-α::

tumor necrosis factor-α

FasL::

Fas ligand

JNK::

c-Jun N-terminal kinase

MAPK::

mitogen-activated protein kinase

ASK-1::

apoptosis signal-regulating kinase-1

VEGF::

vascular endothelial growth factor

HIF-1α::

hypoxia-inducible factor-1α

VHL::

von Hippel–Lindau

MMPs::

matrix metalloproteinases

References

  • Akhand, A.A., Pu, M., Senga, T., Kato, M., Suzuki, H., Miyata, T., Hamaguchi, M., and Nakashima, I. (1999). Nitric oxide controls src kinase activity through a sulfhydryl group modification-mediated Tyr-527-independent and Tyr-416-linked mechanism. J. Biol. Chem. 274, 25821–25826.

    Article  PubMed  CAS  Google Scholar 

  • Ambs, S., Bennett, W.P., Merriam, W.G., Ogunfusika, M.O., Oser, S.M., Khan, M.A., Jones, R.T., and Harris, C.C. (1998a). Vascular endothelial growth factor and nitric oxide synthase expression in human lung cancer and the relation to p53. Br. J. Cancer 78, 233–239.

    Article  PubMed  CAS  Google Scholar 

  • Ambs, S., Ogunfusika, M.O., Merriam, W.G., Bennett, W.P., Billiar, T.R., and Harris, C.C. (1998b). Up-regulation of inducible nitric oxide synthase expression in cancer-prone p53 knockout mice. Proc. Natl. Acad. Sci. U. S. A 95, 8823–8828.

    Article  PubMed  CAS  Google Scholar 

  • Azad, N., Vallyathan, V., Wang, L., Tantishaiyakul, V., Stehlik, C., Leonard, S.S., and Rojanasakul, Y. (2006). S-nitrosylation of Bcl-2 inhibits its ubiquitin-proteasomal degradation. A novel antiapoptotic mechanism that suppresses apoptosis. J. Biol. Chem. 281, 34124–34134.

    Article  PubMed  CAS  Google Scholar 

  • Beckman, J.S., Ischiropoulos, H., Zhu, L., van der Woerd, M., Smith, C., Chen, J., Harrison, J., Martin, J.C., and Tsai, M. (1992). Kinetics of superoxide dismutase- and iron-catalyzed nitration of phenolics by peroxynitrite. Arch. Biochem. Biophys. 298, 438–445.

    Article  PubMed  CAS  Google Scholar 

  • Beckman, J.S. and Koppenol, W.H. (1996). Nitric oxide, superoxide, and peroxynitrite: the good, the bad, and ugly. Am. J. Physiol 271, C1424–C1437.

    PubMed  CAS  Google Scholar 

  • Ben-Ezra, J.M., Kornstein, M.J., Grimes, M.M., and Krystal, G. (1994). Small cell carcinomas of the lung express the Bcl-2 protein. Am. J. Pathol. 145, 1036–1040.

    PubMed  CAS  Google Scholar 

  • Brennan, P.A., Downie, I.P., Langdon, J.D., and Zaki, G.A. (1999). Emerging role of nitric oxide in cancer. Br. J. Oral Maxillofac. Surg. 37, 370–373.

    Article  PubMed  CAS  Google Scholar 

  • Broillet, M.C. (1999). S-nitrosylation of proteins. Cell Mol. Life Sci. 55, 1036–1042.

    Article  PubMed  CAS  Google Scholar 

  • Callsen, D., Sandau, K.B., and Brune, B. (1999). Nitric oxide and superoxide inhibit platelet-derived growth factor receptor phosphotyrosine phosphatases. Free Radic. Biol. Med. 26, 1544–1553.

    Article  PubMed  CAS  Google Scholar 

  • Carmeliet, P. and Jain, R.K. (2000). Angiogenesis in cancer and other diseases. Nature 407, 249–257.

    Article  PubMed  CAS  Google Scholar 

  • Carver, D.J., Gaston, B., Deronde, K., and Palmer, L.A. (2007). Akt-mediated activation of HIF-1 in pulmonary vascular endothelial cells by S-nitrosoglutathione. Am. J. Respir. Cell Mol. Biol. 37, 255–263.

    Article  PubMed  CAS  Google Scholar 

  • Caselli, A., Chiarugi, P., Camici, G., Manao, G., and Ramponi, G. (1995). In vivo inactivation of phosphotyrosine protein phosphatases by nitric oxide. FEBS Lett. 374, 249–252.

    Article  PubMed  CAS  Google Scholar 

  • Chanvorachote, P., Nimmannit, U., Stehlik, C., Wang, L., Jiang, B.H., Ongpipatanakul, B., and Rojanasakul, Y. (2006). Nitric oxide regulates cell sensitivity to cisplatin-induced apoptosis through S-nitrosylation and inhibition of Bcl-2 ubiquitination. Cancer Res. 66, 6353–6360.

    Article  PubMed  CAS  Google Scholar 

  • Chanvorachote, P., Nimmannit, U., Wang, L., Stehlik, C., Lu, B., Azad, N., and Rojanasakul, Y. (2005). Nitric oxide negatively regulates Fas CD95-induced apoptosis through inhibition of ubiquitin-proteasome-mediated degradation of FLICE inhibitory protein. J. Biol. Chem. 280, 42044–42050.

    Article  PubMed  CAS  Google Scholar 

  • Chiarugi, V., Magnelli, L., and Gallo, O. (1998). Cox-2, iNOS and p53 as play-makers of tumor angiogenesis (review). Int. J. Mol. Med. 2, 715–719.

    PubMed  CAS  Google Scholar 

  • Cobbs, C.S., Brenman, J.E., Aldape, K.D., Bredt, D.S., and Israel, M.A. (1995). Expression of nitric oxide synthase in human central nervous system tumors. Cancer Res. 55, 727–730.

    PubMed  CAS  Google Scholar 

  • Davel, L., D’Agostino, A., Espanol, A., Jasnis, M.A., Lauria de, C.L., de Lustig, E.S., and Sales, M.E. (2002). Nitric oxide synthase-cyclooxygenase interactions are involved in tumor cell angiogenesis and migration. J. Biol. Regul. Homeost. Agents 16, 181–189.

    PubMed  CAS  Google Scholar 

  • Dehm, S.M. and Bonham, K. (2004). SRC gene expression in human cancer: the role of transcriptional activation. Biochem. Cell Biol. 82, 263–274.

    Article  PubMed  CAS  Google Scholar 

  • Deininger, M.H., Wybranietz, W.A., Graepler, F.T., Lauer, U.M., Meyermann, R., and Schluesener, H.J. (2003). Endothelial endostatin release is induced by general cell stress and modulated by the nitric oxide/cGMP pathway. FASEB J. 17, 1267–1276.

    Article  PubMed  CAS  Google Scholar 

  • delaTorre, A., Schroeder, R.A., Bartlett, S.T., and Kuo, P.C. (1998). Differential effects of nitric oxide-mediated S-nitrosylation on p50 and c-jun DNA binding. Surgery 124, 137–141; discussion 141–132.

    Google Scholar 

  • Dhakshinamoorthy, S. and Porter, A.G. (2004). Nitric oxide-induced transcriptional up-regulation of protective genes by Nrf2 via the antioxidant response element counteracts apoptosis of neuroblastoma cells. J. Biol. Chem. 279, 20096–20107.

    Article  PubMed  CAS  Google Scholar 

  • Doi, K., Akaike, T., Horie, H., Noguchi, Y., Fujii, S., Beppu, T., Ogawa, M., and Maeda, H. (1996). Excessive production of nitric oxide in rat solid tumor and its implication in rapid tumor growth. Cancer 77, 1598–1604.

    PubMed  CAS  Google Scholar 

  • Dong, Z., Staroselsky, A.H., Qi, X., Xie, K., and Fidler, I.J. (1994). Inverse correlation between expression of inducible nitric oxide synthase activity and production of metastasis in K-1735 murine melanoma cells. Cancer Res. 54, 789–793.

    PubMed  CAS  Google Scholar 

  • Ekmekcioglu, S., Ellerhorst, J.A., Prieto, V.G., Johnson, M.M., Broemeling, L.D., and Grimm, E.A. (2006). Tumor iNOS predicts poor survival for stage III melanoma patients. Int. J. Cancer 119, 861–866.

    Article  PubMed  CAS  Google Scholar 

  • Foster, M.W., McMahon, T.J., and Stamler, J.S. (2003). S-nitrosylation in health and disease. Trends Mol. Med. 9, 160–168.

    Article  PubMed  CAS  Google Scholar 

  • Fukumura, D., Kashiwagi, S., and Jain, R.K. (2006). The role of nitric oxide in tumour progression. Nat. Rev. Cancer 6, 521–534.

    Article  PubMed  CAS  Google Scholar 

  • Gansauge, S., Nussler, A.K., Beger, H.G., and Gansauge, F. (1998). Nitric oxide-induced apoptosis in human pancreatic carcinoma cell lines is associated with a G1-arrest and an increase of the cyclin-dependent kinase inhibitor p21WAF1/CIP1. Cell Growth Differ. 9, 611–617.

    PubMed  CAS  Google Scholar 

  • Garban, H.J., Marquez-Garban, D.C., Pietras, R.J., and Ignarro, L.J. (2005). Rapid nitric oxide-mediated S-nitrosylation of estrogen receptor: regulation of estrogen-dependent gene transcription. Proc. Natl. Acad. Sci. USA 102, 2632–2636.

    Google Scholar 

  • Gaston, B.M., Carver, J., Doctor, A., and Palmer, L.A. (2003). S-nitrosylation signaling in cell biology. Mol. Interv. 3, 253–263.

    Article  PubMed  CAS  Google Scholar 

  • Gow, A.J., Chen, Q., Hess, D.T., Day, B.J., Ischiropoulos, H., and Stamler, J.S. (2002). Basal and stimulated protein S-nitrosylation in multiple cell types and tissues. J. Biol. Chem. 277, 9637–9640.

    Article  PubMed  CAS  Google Scholar 

  • Green, D.R. and Reed, J.C. (1998). Mitochondria and apoptosis. Science 281, 1309–1312.

    Article  PubMed  CAS  Google Scholar 

  • Haendeler, J., Weiland, U., Zeiher, A.M., and Dimmeler, S. (1997). Effects of redox-related congeners of NO on apoptosis and caspase-3 activity. Nitric Oxide 1, 282–293.

    Google Scholar 

  • Haendeler, J., Hoffmann, J., Tischler, V., Berk, B.C., Zeiher, A.M., and Dimmeler, S. (2002). Redox regulatory and anti-apoptotic functions of thioredoxin depend on S-nitrosylation at cysteine 69. Nat. Cell Biol. 4, 743–749.

    Article  PubMed  CAS  Google Scholar 

  • Hajri, A., Metzger, E., Vallat, F., Coffy, S., Flatter, E., Evrard, S., Marescaux, J., and Aprahamian, M. (1998). Role of nitric oxide in pancreatic tumour growth: in vivo and in vitro studies. Br. J. Cancer 78, 841–849.

    Article  PubMed  CAS  Google Scholar 

  • Harris, L.K., McCormick, J., Cartwright, J.E., Whitley, G.S., and Dash, P.R. (2008). S-nitrosylation of proteins at the leading edge of migrating trophoblasts by inducible nitric oxide synthase promotes trophoblast invasion. Exp. Cell Res. 314, 1765–1776.

    Article  PubMed  CAS  Google Scholar 

  • Hess, D.T., Matsumoto, A., Kim, S.O., Marshall, H.E., and Stamler, J.S. (2005). Protein S-nitrosylation: purview and parameters. Nat. Rev. Mol. Cell Biol. 6, 150–166.

    Article  PubMed  CAS  Google Scholar 

  • Hirst, D. and Robson, T. (2007). Targeting nitric oxide for cancer therapy. J. Pharm. Pharmacol. 59, 3–13.

    Article  PubMed  CAS  Google Scholar 

  • Hoffmann, J., Haendeler, J., Zeiher, A.M., and Dimmeler, S. (2001). TNFalpha and oxLDL reduce protein S-nitrosylation in endothelial cells. J. Biol. Chem. 276, 41383–41387.

    Google Scholar 

  • Ichijo, H., Nishida, E., Irie, K., Ten, D.P., Saitoh, M., Moriguchi, T., Takagi, M., Matsumoto, K., Miyazono, K., and Gotoh, Y. (1997). Induction of apoptosis by ASK1, a mammalian MAPKKK that activates SAPK/JNK and p38 signaling pathways. Science 275, 90–94.

    Article  PubMed  CAS  Google Scholar 

  • Ignarro, L.J. (1989). Biological actions and properties of endothelium-derived nitric oxide formed and released from artery and vein. Circ. Res. 65, 1–21.

    Article  PubMed  CAS  Google Scholar 

  • Ignarro, L.J., Buga, G.M., Wood, K.S., Byrns, R.E., and Chaudhuri, G. (1987). Endothelium-derived relaxing factor produced and released from artery and vein is nitric oxide. Proc. Natl. Acad. Sci. U. S. A 84, 9265–9269.

    Article  PubMed  CAS  Google Scholar 

  • Ikegaki, N., Katsumata, M., Minna, J., and Tsujimoto, Y. (1994). Expression of bcl-2 in small cell lung carcinoma cells. Cancer Res. 54, 6–8.

    PubMed  CAS  Google Scholar 

  • Irmler, M., Thome, M., Hahne, M., Schneider, P., Hofmann, K., Steiner, V., Bodmer, J.L., Schroter, M., Burns, K., Mattmann, C., Rimoldi, D., French, L.E., and Tschopp, J. (1997). Inhibition of death receptor signals by cellular FLIP. Nature 388, 190–195.

    Article  PubMed  CAS  Google Scholar 

  • Ishii, Y., Ogura, T., Tatemichi, M., Fujisawa, H., Otsuka, F., and Esumi, H. (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, 161–168.

    Article  PubMed  CAS  Google Scholar 

  • Ishima, Y., Akaike, T., Kragh-Hansen, U., Hiroyama, S., Sawa, T., Suenaga, A., Maruyama, T., Kai, T., and Otagiri, M. (2008). S-Nitrosylated human serum albumin-mediated cytoprotective activity is enhanced by fatty acid binding. J. Biol. Chem. 283, 34966–34975.

    Google Scholar 

  • Iyer, A.K., Azad, N., Wang, L., and Rojanasakul, Y. (2008). Role of S-nitrosylation in apoptosis resistance and carcinogenesis. Nitric. Oxide. 19, 146–151.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • Jenkins, D.C., Charles, I.G., Thomsen, L.L., Moss, D.W., Holmes, L.S., Baylis, S.A., Rhodes, P., Westmore, K., Emson, P.C., and Moncada, S. (1995). Roles of nitric oxide in tumor growth. Proc. Natl. Acad. Sci. USA 92, 4392–4396.

    Article  PubMed  CAS  Google Scholar 

  • Jiang, S.X., Sato, Y., Kuwao, S., and Kameya, T. (1995). Expression of bcl-2 oncogene protein is prevalent in small cell lung carcinomas. J. Pathol. 177, 135–138.

    Article  PubMed  CAS  Google Scholar 

  • Kang-Decker, N., Cao, S., Chatterjee, S., Yao, J., Egan, L.J., Semela, D., Mukhopadhyay, D., and Shah, V. (2007). Nitric oxide promotes endothelial cell survival signaling through S-nitrosylation and activation of dynamin-2. J. Cell Sci. 120, 492–501.

    Google Scholar 

  • Kashiwagi, S., Izumi, Y., Gohongi, T., Demou, Z.N., Xu, L., Huang, P.L., Buerk, D.G., Munn, L.L., Jain, R.K., and Fukumura, D. (2005). NO mediates mural cell recruitment and vessel morphogenesis in murine melanomas and tissue-engineered blood vessels. J. Clin. Invest 115, 1816–1827.

    Article  PubMed  CAS  Google Scholar 

  • Kelleher, Z.T., Matsumoto, A., Stamler, J.S., and Marshall, H.E. (2007). NOS2 regulation of NF-kappaB by S-nitrosylation of p65. J. Biol. Chem. 282, 30667–30672.

    Google Scholar 

  • Kim, J.E. and Tannenbaum, S.R. (2004). S-Nitrosation regulates the activation of endogenous procaspase-9 in HT-29 human colon carcinoma cells. J. Biol. Chem. 279, 9758–9764.

    Article  PubMed  CAS  Google Scholar 

  • Kim, Y.M., Kim, T.H., Chung, H.T., Talanian, R.V., Yin, X.M., and Billiar, T.R. (2000). Nitric oxide prevents tumor necrosis factor alpha-induced rat hepatocyte apoptosis by the interruption of mitochondrial apoptotic signaling through S-nitrosylation of caspase-8. Hepatology 32, 770–778.

    Google Scholar 

  • Kimura, H., Weisz, A., Kurashima, Y., Hashimoto, K., Ogura, T., D, Acquisto, F., Addeo, R., Makuuchi, M., and Esumi, H. (2000). Hypoxia response element of the human vascular endothelial growth factor gene mediates transcriptional regulation by nitric oxide: control of hypoxia-inducible factor-1 activity by nitric oxide. Blood 95, 189–197.

    PubMed  CAS  Google Scholar 

  • Kimura, H., Weisz, A., Ogura, T., Hitomi, Y., Kurashima, Y., Hashimoto, K., D,Acquisto, F., Makuuchi, M., and Esumi, H. (2001). Identification of hypoxia-inducible factor 1 ancillary sequence and its function in vascular endothelial growth factor gene induction by hypoxia and nitric oxide. J. Biol. Chem. 276, 2292–2298.

    PubMed  CAS  Google Scholar 

  • Klas, C., Debatin, K.M., Jonker, R.R., and Krammer, P.H. (1993). Activation interferes with the APO-1 pathway in mature human T cells. Int. Immunol. 5, 625–630.

    Article  PubMed  CAS  Google Scholar 

  • Klotz, T., Bloch, W., Volberg, C., Engelmann, U., and Addicks, K. (1998). Selective expression of inducible nitric oxide synthase in human prostate carcinoma. Cancer 82, 1897–1903.

    Article  PubMed  CAS  Google Scholar 

  • Knowles, R.G. (1996). Nitric oxide synthases. Biochem. Soc. Trans. 24, 875–878.

    PubMed  CAS  Google Scholar 

  • Knowles, R.G. and Moncada, S. (1994). Nitric oxide synthases in mammals. Biochem. J. 298 (Pt 2), 249–258.

    PubMed  CAS  Google Scholar 

  • Kwak, J.Y., Han, M.K., Choi, K.S., Park, I.H., Park, S.Y., Sohn, M.H., Kim, U.H., McGregor, J.R., Samlowski, W.E., and Yim, C.Y. (2000). Cytokines secreted by lymphokine-activated killer cells induce endogenous nitric oxide synthesis and apoptosis in DLD-1 colon cancer cells. Cell Immunol. 203, 84–94.

    Article  PubMed  CAS  Google Scholar 

  • Lala, P.K. and Chakraborty, C. (2001). Role of nitric oxide in carcinogenesis and tumour progression. Lancet Oncol. 2, 149–156.

    Article  PubMed  CAS  Google Scholar 

  • Lala, P.K. and Orucevic, A. (1998). Role of nitric oxide in tumor progression: lessons from experimental tumors. Cancer Metastasis Rev. 17, 91–106.

    Article  PubMed  CAS  Google Scholar 

  • Lancaster, J.R., Jr. and Xie, K. (2006). Tumors face NO problems? Cancer Res. 66, 6459–6462.

    Article  PubMed  CAS  Google Scholar 

  • Lander, H.M., Ogiste, J.S., Pearce, S.F., Levi, R., and Novogrodsky, A. (1995). Nitric oxide-stimulated guanine nucleotide exchange on p21ras. J. Biol. Chem. 270, 7017–7020.

    Article  PubMed  CAS  Google Scholar 

  • Lane, P., Hao, G., and Gross, S.S. (2001). S-nitrosylation is emerging as a specific and fundamental posttranslational protein modification: head-to-head comparison with O-phosphorylation. Sci. STKE. 2001, RE1.

    Article  PubMed  CAS  Google Scholar 

  • Lechner, M., Lirk, P., and Rieder, J. (2005). Inducible nitric oxide synthase (iNOS) in tumor biology: the two sides of the same coin. Semin. Cancer Biol. 15, 277–289.

    Article  PubMed  CAS  Google Scholar 

  • Li, C.Q., Robles, A.I., Hanigan, C.L., Hofseth, L.J., Trudel, L.J., Harris, C.C., and Wogan, G.N. (2004). Apoptotic signaling pathways induced by nitric oxide in human lymphoblastoid cells expressing wild-type or mutant p53. Cancer Res. 64, 3022–3029.

    Article  PubMed  CAS  Google Scholar 

  • Li, F., Sonveaux, P., Rabbani, Z.N., Liu, S., Yan, B., Huang, Q., Vujaskovic, Z., Dewhirst, M.W., and Li, C.Y. (2007). Regulation of HIF-1alpha stability through S-nitrosylation. Mol. Cell 26, 63–74.

    Article  PubMed  CAS  Google Scholar 

  • Li, S. and Whorton, A.R. (2003). Regulation of protein tyrosine phosphatase 1B in intact cells by S-nitrosothiols. Arch. Biochem. Biophys. 410, 269–279.

    Article  PubMed  CAS  Google Scholar 

  • Lirk, P., Hoffmann, G., and Rieder, J. (2002). Inducible nitric oxide synthase – time for reappraisal. Curr. Drug Targets. Inflamm. Allergy 1, 89–108.

    Article  PubMed  CAS  Google Scholar 

  • Mannick, J.B., Schonhoff, C., Papeta, N., Ghafourifar, P., Szibor, M., Fang, K., and Gaston, B. (2001). S-Nitrosylation of mitochondrial caspases. J. Cell Biol. 154, 1111–1116.

    Article  PubMed  CAS  Google Scholar 

  • Mannick, J.B., Hausladen, A., Liu, L., Hess, D.T., Zeng, M., Miao, Q.X., Kane, L.S., Gow, A.J., and Stamler, J.S. (1999). Fas-induced caspase denitrosylation. Science 284, 651–654.

    Google Scholar 

  • Matsumoto, A., Comatas, K.E., Liu, L., and Stamler, J.S. (2003). Screening for nitric oxide-dependent protein-protein interactions. Science 301, 657–661.

    Article  PubMed  CAS  Google Scholar 

  • Metzen, E., Zhou, J., Jelkmann, W., Fandrey, J., and Brune, B. (2003). Nitric oxide impairs normoxic degradation of HIF-1alpha by inhibition of prolyl hydroxylases. Mol. Biol. Cell 14, 3470–3481.

    Article  PubMed  CAS  Google Scholar 

  • Mikkelsen, R.B. and Wardman, P. (2003). Biological chemistry of reactive oxygen and nitrogen and radiation-induced signal transduction mechanisms. Oncogene 22, 5734–5754.

    Article  PubMed  CAS  Google Scholar 

  • Mocellin, S., Bronte, V., and Nitti, D. (2007). Nitric oxide, a double edged sword in cancer biology: searching for therapeutic opportunities. Med. Res. Rev. 27, 317–352.

    Article  PubMed  CAS  Google Scholar 

  • Moncada, S. (1993). The L-arginine: nitric oxide pathway, cellular transduction and immunological roles. Adv. Second Messenger Phosphoprotein Res. 28, 97–99.

    PubMed  CAS  Google Scholar 

  • Montrucchio, G., Lupia, E., de, M.A., Battaglia, E., Arese, M., Tizzani, A., Bussolino, F., and Camussi, G. (1997). Nitric oxide mediates angiogenesis induced in vivo by platelet-activating factor and tumor necrosis factor-alpha. Am. J. Pathol. 151, 557–563.

    PubMed  CAS  Google Scholar 

  • Morita, E.H., Ohkubo, T., Kuraoka, I., Shirakawa, M., Tanaka, K., and Morikawa, K. (1996). Implications of the zinc-finger motif found in the DNA-binding domain of the human XPA protein. Genes Cells 1, 437–442.

    Article  PubMed  CAS  Google Scholar 

  • Mortensen, K., Skouv, J., Hougaard, D.M., and Larsson, L.I. (1999). Endogenous endothelial cell nitric-oxide synthase modulates apoptosis in cultured breast cancer cells and is transcriptionally regulated by p53. J. Biol. Chem. 274, 37679–37684.

    Article  PubMed  CAS  Google Scholar 

  • Nagata, S. (1997). Apoptosis by death factor. Cell 88, 355–365.

    Article  PubMed  CAS  Google Scholar 

  • Nakano, S., Matsukado, K., and Black, K.L. (1996). Increased brain tumor microvessel permeability after intracarotid bradykinin infusion is mediated by nitric oxide. Cancer Res. 56, 4027–4031.

    PubMed  CAS  Google Scholar 

  • Nathan, C. and Xie, Q.W. (1994). Nitric oxide synthases: roles, tolls, and controls. Cell 78, 915–918.

    Article  PubMed  CAS  Google Scholar 

  • Nathan, C.F. and Hibbs, J.B., Jr. (1991). Role of nitric oxide synthesis in macrophage antimicrobial activity. Curr. Opin. Immunol. 3, 65–70.

    Article  PubMed  CAS  Google Scholar 

  • Nikitovic, D., Holmgren, A., and Spyrou, G. (1998). Inhibition of AP-1 DNA binding by nitric oxide involving conserved cysteine residues in Jun and Fos. Biochem. Biophys. Res. Commun. 242, 109–112.

    Google Scholar 

  • Oltvai, Z.N., Milliman, C.L., and Korsmeyer, S.J. (1993). Bcl-2 heterodimerizes in vivo with a conserved homolog, Bax, that accelerates programmed cell death. Cell 74, 609–619.

    Article  PubMed  CAS  Google Scholar 

  • Padmaja, S. and Huie, R.E. (1993). The reaction of nitric oxide with organic peroxyl radicals. Biochem. Biophys. Res. Commun. 195, 539–544.

    Article  PubMed  CAS  Google Scholar 

  • Palmer, R.M., Ferrige, A.G., and Moncada, S. (1987). Nitric oxide release accounts for the biological activity of endothelium-derived relaxing factor. Nature 327, 524–526.

    Article  PubMed  CAS  Google Scholar 

  • Park, H.S., Huh, S.H., Kim, M.S., Lee, S.H., and Choi, E.J. (2000). Nitric oxide negatively regulates c-Jun N-terminal kinase/stress-activated protein kinase by means of S-nitrosylation. Proc. Natl. Acad. Sci. U. S. A 97, 14382–14387.

    Article  PubMed  CAS  Google Scholar 

  • Park, H.S., Yu, J.W., Cho, J.H., Kim, M.S., Huh, S.H., Ryoo, K., and Choi, E.J. (2004). Inhibition of apoptosis signal-regulating kinase 1 by nitric oxide through a thiol redox mechanism. J. Biol. Chem. 279, 7584–7590.

    Article  PubMed  CAS  Google Scholar 

  • Park, S.W., Lee, S.G., Song, S.H., Heo, D.S., Park, B.J., Lee, D.W., Kim, K.H., and Sung, M.W. (2003). The effect of nitric oxide on cyclooxygenase-2 (COX-2) overexpression in head and neck cancer cell lines. Int. J. Cancer 107, 729–738.

    Article  PubMed  CAS  Google Scholar 

  • Pugh, C.W. and Ratcliffe, P.J. (2003). Regulation of angiogenesis by hypoxia: role of the HIF system. Nat. Med. 9, 677–684.

    Article  PubMed  CAS  Google Scholar 

  • Radomski, M.W., Jenkins, D.C., Holmes, L., and Moncada, S. (1991). Human colorectal adenocarcinoma cells: differential nitric oxide synthesis determines their ability to aggregate platelets. Cancer Res. 51, 6073–6078.

    PubMed  CAS  Google Scholar 

  • Raspollini, M.R., Amunni, G., Villanucci, A., Boddi, V., Baroni, G., Taddei, A., and Taddei, G.L. (2004). Expression of inducible nitric oxide synthase and cyclooxygenase-2 in ovarian cancer: correlation with clinical outcome. Gynecol. Oncol. 92, 806–812.

    Article  PubMed  CAS  Google Scholar 

  • Ravi, K., Brennan, L.A., Levic, S., Ross, P.A., and Black, S.M. (2004). S-nitrosylation of endothelial nitric oxide synthase is associated with monomerization and decreased enzyme activity. Proc. Natl. Acad. Sci. USA 101, 2619–2624.

    Google Scholar 

  • Reed, J.C. (1997). Cytochrome c: can,t live with it – can,t live without it. Cell 91, 559–562.

    Article  PubMed  CAS  Google Scholar 

  • Ridnour, L.A., Thomas, D.D., Donzelli, S., Espey, M.G., Roberts, D.D., Wink, D.A., and Isenberg, J.S. (2006). The biphasic nature of nitric oxide responses in tumor biology. Antioxid. Redox. Signal. 8, 1329–1337.

    Article  PubMed  CAS  Google Scholar 

  • Rizzo, M.A., and Piston, D.W. (2003). Regulation of beta cell glucokinase by S-nitrosylation and association with nitric oxide synthase. J. Cell Biol. 161, 243–248.

    Google Scholar 

  • Rosbe, K.W., Prazma, J., Petrusz, P., Mims, W., Ball, S.S., and Weissler, M.C. (1995). Immunohistochemical characterization of nitric oxide synthase activity in squamous cell carcinoma of the head and neck. Otolaryngol. Head Neck Surg. 113, 541–549.

    PubMed  CAS  Google Scholar 

  • Salvesen, G.S. and Dixit, V.M. (1997). Caspases: intracellular signaling by proteolysis. Cell 91, 443–446.

    Article  PubMed  CAS  Google Scholar 

  • Sidorkina, O., Espey, M.G., Miranda, K.M., Wink, D.A., and Laval, J. (2003). Inhibition of poly(ADP-RIBOSE) polymerase (PARP) by nitric oxide and reactive nitrogen oxide species. Free Radic. Biol. Med. 35, 1431–1438.

    Article  PubMed  CAS  Google Scholar 

  • Siegert, A., Rosenberg, C., Schmitt, W.D., Denkert, C., and Hauptmann, S. (2002). Nitric oxide of human colorectal adenocarcinoma cell lines promotes tumour cell invasion. Br. J. Cancer 86, 1310–1315.

    Article  PubMed  CAS  Google Scholar 

  • Snyder, S.H. and Bredt, D.S. (1992). Biological roles of nitric oxide. Sci. Am. 266, 68–7.

    Article  Google Scholar 

  • Stamler, J.S. (1994). Redox signaling: nitrosylation and related target interactions of nitric oxide. Cell 78, 931–936.

    Article  PubMed  CAS  Google Scholar 

  • Stamler, J.S., Lamas, S., and Fang, F.C. (2001). Nitrosylation. the prototypic redox-based signaling mechanism. Cell 106, 675–683.

    CAS  Google Scholar 

  • Stamler, J.S., Simon, D.I., Osborne, J.A., Mullins, M.E., Jaraki, O., Michel, T., Singel, D.J., and Loscalzo, J. (1992). S-nitrosylation of proteins with nitric oxide: synthesis and characterization of biologically active compounds. Proc. Natl. Acad. Sci. U. S. A 89, 444–448.

    Article  PubMed  CAS  Google Scholar 

  • Stamler, J.S., Toone, E.J., Lipton, S.A., and Sucher, N.J. (1997). (S)NO signals: translocation, regulation, and a consensus motif. Neuron 18, 691–696.

    Article  PubMed  CAS  Google Scholar 

  • Sumbayev, V.V., Budde, A., Zhou, J., and Brune, B. (2003). HIF-1 alpha protein as a target for S-nitrosation. FEBS Lett. 535, 106–112.

    Article  PubMed  CAS  Google Scholar 

  • Thomsen, L.L., Lawton, F.G., Knowles, R.G., Beesley, J.E., Riveros-Moreno, V., and Moncada, S. (1994). Nitric oxide synthase activity in human gynecological cancer. Cancer Res. 54, 1352–1354.

    PubMed  CAS  Google Scholar 

  • Thomsen, L.L., Miles, D.W., Happerfield, L., Bobrow, L.G., Knowles, R.G., and Moncada, S. (1995). Nitric oxide synthase activity in human breast cancer. Br. J. Cancer 72, 41–44.

    Article  PubMed  CAS  Google Scholar 

  • Torok, N.J., Higuchi, H., Bronk, S., and Gores, G.J. (2002). Nitric oxide inhibits apoptosis downstream of cytochrome C release by nitrosylating caspase 9. Cancer Res. 62, 1648–1653.

    PubMed  CAS  Google Scholar 

  • Wallach, D., Varfolomeev, E.E., Malinin, N.L., Goltsev, Y.V., Kovalenko, A.V., and Boldin, M.P. (1999). Tumor necrosis factor receptor and Fas signaling mechanisms. Annu. Rev. Immunol. 17, 331–367.

    Article  PubMed  CAS  Google Scholar 

  • Wang, G.Y., Ji, B., Wang, X., and Gu, J.H. (2005). Anti-cancer effect of iNOS inhibitor and its correlation with angiogenesis in gastric cancer. World J. Gastroenterol. 11, 3830–3833.

    PubMed  CAS  Google Scholar 

  • Whalen, E.J., Foster, M.W., Matsumoto, A., Ozawa, K., Violin, J.D., Que, L.G., Nelson, C.D., Benhar, M., Keys, J.R., Rockman, H.A., Koch, W.J., Daaka, Y., Lefkowitz, R.J., and Stamler, J.S. (2007). Regulation of beta-adrenergic receptor signaling by S-nitrosylation of G-protein-coupled receptor kinase 2. Cell 129, 511–522.

    Google Scholar 

  • Williams, E.L. and Djamgoz, M.B. (2005). Nitric oxide and metastatic cell behaviour. Bioessays 27, 1228–1238.

    Article  PubMed  CAS  Google Scholar 

  • Williams, J.G., Pappu, K., and Campbell, S.L. (2003). Structural and biochemical studies of p21Ras S-nitrosylation and nitric oxide-mediated guanine nucleotide exchange. Proc. Natl. Acad. Sci. U. S. A 100, 6376–6381.

    Article  PubMed  CAS  Google Scholar 

  • Wink, D.A., Vodovotz, Y., Laval, J., Laval, F., Dewhirst, M.W., and Mitchell, J.B. (1998). The multifaceted roles of nitric oxide in cancer. Carcinogenesis 19, 711–721.

    Article  PubMed  CAS  Google Scholar 

  • Wyllie, A.H., Kerr, J.F., and Currie, A.R. (1980). Cell death: the significance of apoptosis. Int. Rev. Cytol. 68, 251–306.

    Article  PubMed  CAS  Google Scholar 

  • Xie, K., Huang, S., Dong, Z., Gutman, M., and Fidler, I.J. (1995a). Direct correlation between expression of endogenous inducible nitric oxide synthase and regression of M5076 reticulum cell sarcoma hepatic metastases in mice treated with liposomes containing lipopeptide CGP 31362. Cancer Res. 55, 3123–3131.

    PubMed  CAS  Google Scholar 

  • Xie, K., Huang, S., Dong, Z., Juang, S.H., Gutman, M., Xie, Q.W., Nathan, C., and Fidler, I.J. (1995b). Transfection with the inducible nitric oxide synthase gene suppresses tumorigenicity and abrogates metastasis by K-1735 murine melanoma cells. J. Exp. Med. 181, 1333–1343.

    Article  PubMed  CAS  Google Scholar 

  • Yang, J., Liu, X., Bhalla, K., Kim, C.N., Ibrado, A.M., Cai, J., Peng, T.I., Jones, D.P., and Wang, X. (1997). Prevention of apoptosis by Bcl-2: release of cytochrome c from mitochondria blocked. Science 275, 1129–1132.

    Article  PubMed  CAS  Google Scholar 

  • Yasinska, I.M. and Sumbayev, V.V. (2003). S-nitrosation of Cys-800 of HIF-1alpha protein activates its interaction with p300 and stimulates its transcriptional activity. FEBS Lett. 549, 105–109.

    Article  PubMed  CAS  Google Scholar 

  • Yuan, J. (1997). Transducing signals of life and death. Curr. Opin. Cell Biol. 9, 247–251.

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgment

This work was supported by the National Institutes of Health Grant R01-HL076340.

Author information

Authors and Affiliations

  1. Department of Pharmaceutical Sciences, Hampton University, Hampton, VA, 23668, USA

    Anand Krishnan V. Iyer & Neelam Azad

  2. Pathology and Physiology Research Branch, National Institute for Occupational Safety and Health, Morgantown, WV, 26505, USA

    Liying Wang

  3. Department of Pharmaceutical and Pharmacological Sciences, West Virginia University, Morgantown, WV, 26506, USA

    Yon Rojanasakul

Authors
  1. Anand Krishnan V. Iyer
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Neelam Azad
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Liying Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Yon Rojanasakul
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Yon Rojanasakul .

Editor information

Editors and Affiliations

  1. Dept. Microbiology, Immunology &, Molecular Genetics, University of California, Los Angeles, Charles E. Young Dr. E. 609, Los Angeles, 90095, California, USA

    Benjamin Bonavida

Rights and permissions

Reprints and permissions

Copyright information

© 2010 Springer Science + Business Media, LLC

About this chapter

Cite this chapter

Iyer, A.K.V., Azad, N., Wang, L., Rojanasakul, Y. (2010). S-Nitrosylation – How Cancer Cells Say NO to Cell Death. In: Bonavida, B. (eds) Nitric Oxide (NO) and Cancer. Cancer Drug Discovery and Development. Springer, New York, NY. https://doi.org/10.1007/978-1-4419-1432-3_5

Download citation

  • DOI: https://doi.org/10.1007/978-1-4419-1432-3_5

  • Published:

  • Publisher Name: Springer, New York, NY

  • Print ISBN: 978-1-4419-1431-6

  • Online ISBN: 978-1-4419-1432-3

  • eBook Packages: MedicineMedicine (R0)

Publish with us

Policies and ethics

Search

Navigation