Nitric oxide inhibits the proliferation and invasion of pancreatic cancer cells through degradation of insulin receptor substrate-1 protein

Molecular Cancer Research

Volumn 8, Issue 8, 2010, Pages 1152-1163

  Sugita, Hiroki ^a   Kaneki, Masao ^b   Furuhashi, Satoshi ^a   Hirota, Masahiko ^a   Takamori, Hiroshi ^a   Baba, Hideo ^a  

^a KUMAMOTO UNIVERSITY   (Japan)

^b MASSACHUSETTS GENERAL HOSPITAL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

GLYCOGEN SYNTHASE KINASE 3BETA; INSULIN RECEPTOR SUBSTRATE 1; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; N [3 (AMINOMETHYL)BENZYL]ACETAMIDINE; NITRIC OXIDE; PROTEIN KINASE B; SOMATOMEDIN;

ARTICLE; CANCER CELL; CELL INVASION; CELL PROLIFERATION; CELL STIMULATION; CONTROLLED STUDY; DELETION MUTANT; DOWN REGULATION; ENZYME INHIBITION; GENE DELETION; GENETIC TRANSFECTION; HUMAN; MUTANT; PANCREAS CANCER; PHOSPHORYLATION; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION; UBIQUITINATION; UPREGULATION;

BLOTTING, WESTERN; CELL ADHESION; CELL MOVEMENT; CELL PROLIFERATION; FREE RADICAL SCAVENGERS; GLYCOGEN SYNTHASE KINASE 3; HUMANS; IMMUNOPRECIPITATION; INSULIN; INSULIN RECEPTOR SUBSTRATE PROTEINS; INSULIN-LIKE GROWTH FACTOR I; NEOPLASM INVASIVENESS; NITRIC OXIDE; NITRIC OXIDE DONORS; NITRIC OXIDE SYNTHASE TYPE II; NITRITES; PANCREATIC NEOPLASMS; PHOSPHATIDYLINOSITOL 3-KINASE; PHOSPHORYLATION; PROTO-ONCOGENE PROTEINS C-AKT; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, MESSENGER; SIGNAL TRANSDUCTION; TUMOR CELLS, CULTURED; UBIQUITIN; UBIQUITINATION;

EID: 77955740818     PISSN: 15417786     EISSN: 15573125     Source Type: Journal    
DOI: 10.1158/1541-7786.MCR-09-0472     Document Type: Article

References (47)

1. Bergmann U, Funatomi H, Yokoyama M, Beger HG, Korc M. Insulin-like growth factor I overexpression in human pancreatic cancer: evidence for autocrine and paracrine roles. Cancer Res 1995;55:2007-11.
2. Furukawa M, Raffeld M, Mateo C, et al. Increased expression of insulin-like growth factor I and/or its receptor in gastrinomas is associated with low curability, increased growth, and development of metastases. Clin Cancer Res 2005;11:3233-42. (Pubitemid 40627870)
3. Kim HJ, Litzenburger BC, Cui X, et al. Constitutively active type I insulin-like growth factor receptor causes transformation and xenograft growth of immortalized mammary epithelial cells and is accompanied by an epithelial-to-mesenchymal transition mediated by NF-κB and snail. Mol Cell Biol 2007;27:3165-75. (Pubitemid 46581327)
4. Tanaka S, Wands JR. A carboxy-terminal truncated insulin receptor substrate-1 dominant negative protein reverses the human hepatocellular carcinoma malignant phenotype. J Clin Invest 1996;98:2100-8. (Pubitemid 26376299)
5. Ito T, Sasaki Y, Wands JR. Overexpression of human insulin receptor substrate 1 induces cellular transformation with activation of mitogen-activated protein kinases. Mol Cell Biol 1996;16:943-51. (Pubitemid 26061665)
6. Chang Q, Li Y, White MF, Fletcher JA, Xiao S. Constitutive activation of insulin receptor substrate 1 is a frequent event in human tumors: therapeutic implications. Cancer Res 2002;62:6035-8. (Pubitemid 35244449)
7. Asano T, Yao Y, Shin S, McCubrey J, Abbruzzese JL, Reddy SA. Insulin receptor substrate is a mediator of phosphoinositide 3-kinase activation in quiescent pancreatic cancer cells. Cancer Res 2005;65:9164-8. (Pubitemid 41507979)
8. Dearth RK, Cui X, Kim HJ, et al. Mammary tumorigenesis and metastasis caused by overexpression of insulin receptor substrate 1 (IRS-1) or IRS-2. Mol Cell Biol 2006;26:9302-14. (Pubitemid 44904425)
9. Park HS, Huh SH, Kim MS, Lee SH, Choi EJ. 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 2000;97:14382-7.
10. Reynaert NL, Ckless K, Korn SH, et al. Nitric oxide represses inhibitory κB kinase through S-nitrosylation. Proc Natl Acad Sci U S A 2004;101:8945-50. (Pubitemid 38781591)
11. Mannick JB, Hausladen A, Liu L, et al. Fas-induced caspase denitrosylation. Science 1999;284:651-4.
12. Yasukawa T, Tokunaga E, Ota H, Sugita H, Martyn JA, Kaneki M. S-nitrosylation-dependent inactivation of Akt/protein kinase B in insulin resistance. J Biol Chem 2005;280:7511-8. (Pubitemid 40349643)
13. Ignarro LJ, Buga GM, Wood KS, Byrns RE, Chaudhuri G. Endothelium-derived relaxing factor produced and released from artery and vein is nitric oxide. Proc Natl Acad Sci U S A 1987;84:9265-9.
14. Palmer RM, Ferrige AG, Moncada S. Nitric oxide release accounts for the biological activity of endothelium-derived relaxing factor. Nature 1987;327:524-6. (Pubitemid 17085822)
15. Kuo PC, Schroeder RA. The emerging multifaceted roles of nitric oxide. Ann Surg 1995;221:220-35.
16. Wink DA, Miranda KM, Espey MG. Effects of oxidative and nitrosative stress in cytotoxicity. Semin Perinatol 2000;24:20-3.
17. Perreault M, Marette A. Targeted disruption of inducible nitric oxide synthase protects against obesity-linked insulin resistance in muscle. Nat Med 2001;7:1138-43. (Pubitemid 33010023)
18. Xie K, Fidler IJ. Therapy of cancer metastasis by activation of the inducible nitric oxide synthase. Cancer Metastasis Rev 1998;17:55-75. (Pubitemid 28194646)
19. Sugita H, Fujimoto M, Yasukawa T, et al. Inducible nitric-oxide synthase and NO donor induce insulin receptor substrate-1 degradation in skeletal muscle cells. J Biol Chem 2005;280:14203-11. (Pubitemid 40517322)
20. Ambs S, Merriam WG, Ogunfusika MO, et al. p53 and vascular endothelial growth factor regulate tumor growth of NOS2-expressing human carcinoma cells. Nat Med 1998;4:1371-6. (Pubitemid 28553458)
21. Camp ER, Yang A, Liu W, et al. Roles of nitric oxide synthase inhibition and vascular endothelial growth factor receptor-2 inhibition on vascular morphology and function in an in vivo model of pancreatic cancer. Clin Cancer Res 2006;12:2628-33.
22. Kalivendi SV, Kotamraju S, Zhao H, Joseph J, Kalyanaraman B. Doxorubicin-induced apoptosis is associated with increased transcription of endothelial nitric-oxide synthase. Effect of antiapoptotic antioxidants and calcium. J Biol Chem 2001;276:47266-76. (Pubitemid 37373106)
23. Wang B, Wei D, Crum VE, et al. A novel model system for studying the double-edged roles of nitric oxide production in pancreatic cancer growth and metastasis. Oncogene 2003;22:1771-82. (Pubitemid 36513137)
24. Peshes-Yaloz N, Rosen D, Sondel PM, Krammer PH, Berke G. Up-regulation of Fas (CD95) expression in tumour cells in vivo. Immunology 2007;120:502-11. (Pubitemid 46365008)
25. Kotamraju S, Williams CL, Kalyanaraman B. Statin-induced breast cancer cell death: role of inducible nitric oxide and arginase-dependent pathways. Cancer Res 2007;67:7386-94. (Pubitemid 47206569)
26. Notas G, Nifli AP,Kampa M, Vercauteren J, Kouroumalis E, Castanas E. Resveratrol exerts its antiproliferative effect on HepG2 hepatocellular carcinoma cells, by inducing cell cycle arrest, and NOS activation. Biochim Biophys Acta 2006;1760:1657-66. (Pubitemid 44667277)
27. Jarry A, Charrier L, Bou-Hanna C, et al. Position in cell cycle controls the sensitivity of colon cancer cells to nitric oxide-dependent programmed cell death. Cancer Res 2004;64:4227-34. (Pubitemid 38802427)
28. Chawla-Sarkar M, Bauer JA, Lupica JA, et al. Suppression of NF-κB survival signaling by nitrosylcobalamin sensitizes neoplasms to the anti-tumor effects of Apo2L/TRAIL. J Biol Chem 2003;278:39461-9. (Pubitemid 37248502)
29. Misko TP, Schilling RJ, Salvemini D, Moore WM, Currie MG. A fluorometric assay for the measurement of nitrite in biological samples. Anal Biochem 1993;214:11-6. (Pubitemid 23300346)
30. Ceyhan GO, Giese NA, Erkan M, et al. The neurotrophic factor artemin promotes pancreatic cancer invasion. Ann Surg 2006;244:274-81. (Pubitemid 44305543)
31. Shi B, Sepp-Lorenzino L, Prisco M, Linsley P, deAngelis T, Baserga R. Micro RNA 145 targets the insulin receptor substrate-1 and inhibits the growth of colon cancer cells. J Biol Chem 2007;282:32582-90. (Pubitemid 350159311)
32. Scamuffa N, Siegfried G, Bontemps Y, et al. Selective inhibition of proprotein convertases represses the metastatic potential of human colorectal tumor cells. J Clin Invest 2008;118:352-63.
33. Jiang P, Enomoto A, Jijiwa M, et al. An actin-binding protein Girdin regulates the motility of breast cancer cells. Cancer Res 2008;68:1310-8. (Pubitemid 351346837)
34. Yu Y, Hao Y, Feig LA. The R-Ras GTPase mediates cross talk between estrogen and insulin signaling in breast cancer cells. Mol Cell Biol 2006;26:6372-80. (Pubitemid 44277878)
35. Lander HM, Hajjar DP, Hempstead BL, et al. A molecular redox switch on p21(ras). Structural basis for the nitric oxide-p21(ras) interaction. J Biol Chem 1997;272:4323-6.
36. Lim KH, Ancrile BB, Kashatus DF, Counter CM. Tumour maintenance is mediated by eNOS. Nature 2008;452:646-9.
37. Ibiza S, Perez-Rodriguez A, Ortega A, et al. Endothelial nitric oxide synthase regulates N-Ras activation on the Golgi complex of antigen-stimulated T cells. Proc Natl Acad Sci U S A 2008;105:10507-12.
38. Ellerhorst JA, Ekmekcioglu S, Johnson MK, Cooke CP, Johnson MM, Grimm EA. Regulation of iNOS by the p44/42 mitogen-activated protein kinase pathway in human melanoma. Oncogene 2006;25:3956-62. (Pubitemid 43990751)
39. Donnini S, Finetti F, Solito R, et al. EP2 prostanoid receptor promotes squamous cell carcinoma growth through epidermal growth factor receptor transactivation and iNOS and ERK1/2 pathways. FASEB J 2007;21:2418-30. (Pubitemid 47230672)
40. Hofseth LJ, Saito S, Hussain SP, et al. Nitric oxide-induced cellular stress and p53 activation in chronic inflammation. Proc Natl Acad Sci U S A 2003;100:143-8. (Pubitemid 36078042)
41. Heller R, Polack T, Grabner R, Till U. Nitric oxide inhibits proliferation of human endothelial cells via a mechanism independent of cGMP. Atherosclerosis 1999;144:49-57. (Pubitemid 29259965)
42. Mancuso C, Bonsignore A, Di Stasio E, Mordente A, Motterlini R. Bilirubin and S-nitrosothiols interaction: evidence for a possible role of bilirubin as a scavenger of nitric oxide. Biochem Pharmacol 2003;66:2355-63. (Pubitemid 37456743)
43. Janssens MY, Verovski VN, Van den Berge DL, Monsaert C, Storme GA. Radiosensitization of hypoxic tumour cells by S-nitroso-N-acetylpenicillamine implicates a bioreductive mechanism of nitric oxide generation. Br J Cancer 1999;79:1085-9. (Pubitemid 29087879)
44. Adams C, McCarthy HO, Coulter JA, et al. Nitric oxide synthase gene therapy enhances the toxicity of cisplatin in cancer cells. J Gene Med 2009;11:160-8.
45. Kiziltepe T, Hideshima T, Ishitsuka K, et al. JS-K, a GST-activated nitric oxide generator, induces DNA double-strand breaks, activates DNA damage response pathways, and induces apoptosis in vitro and in vivo in human multiple myeloma cells. Blood 2007;110:709-18. (Pubitemid 47105410)
46. Wang Z, Cook T, Alber S, et al. Adenoviral gene transfer of the human inducible nitric oxide synthase gene enhances the radiation response of human colorectal cancer associated with alterations in tumor vascularity. Cancer Res 2004;64:1386-95. (Pubitemid 38235607)
47. Ma Q, Wang Y, Gao X, Ma Z, Song Z. L-Arginine reduces cell proliferation and ornithine decarboxylase activity in patients with colorectal adenoma and adenocarcinoma. Clin Cancer Res 2007;13:7407-12.