Restoring soluble guanylyl cyclase expression and function blocks the aggressive course of glioma

Molecular Pharmacology

Volumn 80, Issue 6, 2011, Pages 1076-1084

  Zhu, Haifeng ^b   Li, Jessica Tao ^c   Zheng, Fang ^c   Martin, Emil ^c   Kots, Alexander Y ^a   Krumenacker, Joshua S ^c   Choi, Byung Kwon ^c   McCutcheon, Ian E ^b   Weisbrodt, Norman ^c   Bögler, Oliver ^b   Murad, Ferid ^a   Bian, Ka ^a  

^a GEORGE WASHINGTON UNIVERSITY MEDICAL CENTER   (United States)

^b UNIVERSITY OF TEXAS MD ANDERSON CANCER CENTER   (United States)

^c UNIVERSITY OF TEXAS MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ATRIAL NATRIURETIC FACTOR; BRAIN NATRIURETIC PEPTIDE; CYCLIC GMP; CYCLIC GMP PHOSPHODIESTERASE; GUANYLATE CYCLASE; ISOPROTEIN; MEMBRANE PROTEIN; ZAPRINAST;

ANGIOGENESIS; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CANCER CHEMOTHERAPY; CANCER GROWTH; CANCER RADIOTHERAPY; CANCER SURVIVAL; CELL PROLIFERATION; CELL VIABILITY; COLONY FORMATION; CONTROLLED STUDY; DISEASE COURSE; GENE EXPRESSION PROFILING; GLIOMA; GLIOMA CELL; HISTOPATHOLOGY; HUMAN; HUMAN CELL; HUMAN TISSUE; INHIBITION KINETICS; MOLECULAR DYNAMICS; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN DATABASE; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; REAL TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION; TUMOR XENOGRAFT; WESTERN BLOTTING;

ANIMALS; ANTINEOPLASTIC AGENTS; CELL LINE, TUMOR; GENE EXPRESSION REGULATION, ENZYMOLOGIC; GLIOMA; GUANYLATE CYCLASE; HUMANS; MICE; MICE, NUDE; NEOPLASM INVASIVENESS; RECEPTORS, CYTOPLASMIC AND NUCLEAR; XENOGRAFT MODEL ANTITUMOR ASSAYS;

EID: 81555204242     PISSN: 0026895X     EISSN: 15210111     Source Type: Journal    
DOI: 10.1124/mol.111.073585     Document Type: Article

References (52)

1. Basson MD and Hong F (1996) Regulation of human Caco-2 intestinal epithelial brush border enzyme activity by cyclic nucleotides. Cancer Lett 99:155-160. (Pubitemid 26034629)
2. Bhuiyan MB, Murad F, and Fant ME (2006) The placental cholinergic system: localization to the cytotrophoblast and modulation of nitric oxide. Cell Commun Signal 4:4.
3. Bian K, Doursout MF, and Murad F (2008) Vascular system: role of nitric oxide in cardiovascular diseases. J Clin Hypertens (Greenwich) 10:304-310.
4. Bian K, Gao Z, Weisbrodt N, and Murad F (2003) The nature of heme/iron-induced protein tyrosine nitration. Proc Natl Acad Sci USA 100:5712-5717. (Pubitemid 36576873)
5. Bian K, Harari Y, Zhong M, Lai M, Castro G, Weisbrodt N, and Murad F (2001) Down-regulation of inducible nitric-oxide synthase (NOS-2) during parasite-induced gut inflammation: a path to identify a selective NOS-2 inhibitor. Mol Pharmacol 59:939-947. (Pubitemid 32274023)
6. Bian K and Murad F (2003) Nitric oxide (NO)-biogeneration, regulation, and relevance to human diseases. Front Biosci 8:d264-278. (Pubitemid 39069977)
7. Bonkale WL, Winblad B, Ravid R, and Cowburn RF (1995) Reduced nitric oxide responsive soluble guanylyl cyclase activity in the superior temporal cortex of patients with Alzheimer's disease. Neurosci Lett 187:5-8.
8. Corbalán R, Chatauret N, Behrends S, Butterworth RF, and Felipo V (2002) Region selective alterations of soluble guanylate cyclase content and modulation in brain of cirrhotic patients. Hepatology 36:1155-1162. (Pubitemid 35253431)
9. Criss WE and Murad F (1976) Urinary excretion of cyclic guanosine 3′:5′- monophosphate and cyclic adenosine 3′:5′- monophosphate in rats bearing transplantable liver and kidney tumors. Cancer Res 36:1714-1716.
10. Cuny E, Loiseau H, Penchet G, Ellie E, Arsaut J, Vital A, Vincendeau P, and Demotes-Mainard J (2002) Association of elevated glial expression of interleukin-1beta with improved survival in patients with glioblastomas multiforme. J Neurosurg 96:294-301. (Pubitemid 34230244)
11. Deguchi A, Thompson WJ, and Weinstein IB (2004) Activation of protein kinase G is sufficient to induce apoptosis and inhibit cell migration in colon cancer cells. Cancer Res 64:3966-3973. (Pubitemid 38697311)
12. DeRubertis FR, Chayoth R, and Field JB (1976) The content and metabolism of cyclic adenosine 3′,5′-monophosphate and cyclic guanosine 3′,5′-monophosphate in adenocarcinoma of the human colon. J Clin Invest 57:641-649.
13. Ertel A, Verghese A, Byers SW, Ochs M, and Tozeren A (2006) Pathway-specific differences between tumor cell lines and normal and tumor tissue cells. Mol Cancer 5:55.
14. Farias CB, Lima RC, Lima LO, Flores DG, Meurer L, Brunetto AL, Schwartsmann G, and Roesler R (2008) Stimulation of proliferation of U138-MG glioblastoma cells by gastrin-releasing peptide in combination with agents that enhance cAMP signaling. Oncology 75:27-31.
15. Fischbach C, Chen R, Matsumoto T, Schmelzle T, Brugge JS, Polverini PJ, and Mooney DJ (2007) Engineering tumors with 3D scaffolds. Nat Methods 4:855-860. (Pubitemid 350055585)
16. Frattola L, Carenzi A, Cerri C, Kumakura K, and Trabucchi M (1976) Regulation of the cyclic guanosine 3′-5′ monophosphate system in human brain tumors. Acta Neurol Scand 54:382-390. (Pubitemid 8017746)
17. Garg UC, Devi L, Turndorf H, Goldfrank LR, and Bansinath M (1992) Effect of nitric oxide on mitogenesis and proliferation of cerebellar glial cells. Brain research 592:208-212.
18. Garg UC and Hassid A (1989) Nitric oxide-generating vasodilators and 8-bromocyclic guanosine monophosphate inhibit mitogenesis and proliferation of cultured rat vascular smooth muscle cells. J Clin Invest 83:1774-1777. (Pubitemid 19124139)
19. Goldberg ND, Haddox MK, Nicol SE, Glass DB, Sanford CH, Kuehl FA Jr, and Estensen R (1975) Biologic regulation through opposing influences of cyclic GMP and cyclic AMP: the Yin Yang hypothesis. Adv Cyclic Nucleotide Res 5:307-330.
20. Hadden JW, Hadden EM, Haddox MK, and Goldberg ND (1972) Guanosine 3′:5′- cyclic monophosphate: a possible intracellular mediator of mitogenic influences in lymphocytes. Proc Natl Acad Sci USA 69:3024-3027.
21. Jemal A, Siegel R, Ward E, Hao Y, Xu J, Murray T, and Thun MJ (2008) Cancer statistics, 2008. CA Cancer J Clin 58:71-96. (Pubitemid 351521864)
22. Kamisaki Y, Saheki S, Nakane M, Palmieri JA, Kuno T, Chang BY, Waldman SA, and Murad F (1986) Soluble guanylate cyclase from rat lung exists as a heterodimer. J Biol Chem 261:7236-7241. (Pubitemid 17224718)
23. Kimura H and Murad F (1975) Increased particulate and decreased soluble guanylate cyclase activity in regenerating liver, fetal liver, and hepatoma. Proc Natl Acad Sci USA 72:1965-1969.
24. Kots AY, Choi BK, Estrella-Jimenez ME, Warren CA, Gilbertson SR, Guerrant RL, and Murad F (2008) Pyridopyrimidine derivatives as inhibitors of cyclic nucleotide synthesis: application for treatment of diarrhea. Proc Natl Acad Sci USA 105: 8440-8445. (Pubitemid 351904775)
25. Krumenacker JS, Katsuki S, Kots A, and Murad F (2006) Differential expression of genes involved in cGMP-dependent nitric oxide signaling in murine embryonic stem (ES) cells and ES cell-derived cardiomyocytes. Nitric Oxide 14:1-11. (Pubitemid 43063502)
26. Leung EL, Wong JC, Johlfs MG, Tsang BK, and Fiscus RR (2010) Protein kinase G type Ialpha activity in human ovarian cancer cells significantly contributes to enhanced Src activation and DNA synthesis/cell proliferation. Mol Cancer Res 8:578-591.
27. Martin E, Sharina I, Kots A, and Murad F (2003) A constitutively activated mutant of human soluble guanylyl cyclase (sGC): implication for the mechanism of sGC activation. Proc Natl Acad Sci USA 100:9208-9213. (Pubitemid 37033908)
28. Mathieu V, De Nève N, Le Mercier M, Dewelle J, Gaussin JF, Dehoux M, Kiss R, and Lefranc F (2008) Combining bevacizumab with temozolomide increases the antitumor efficacy of temozolomide in a human glioblastoma orthotopic xenograft model. Neoplasia 10:1383-1392.
29. McCutcheon IE, Friend KE, Gerdes TM, Zhang BM, Wildrick DM, and Fuller GN (2000) Intracranial injection of human meningioma cells in athymic mice: an orthotopic model for meningioma growth. J Neurosurg 92:306-314. (Pubitemid 30071051)
30. McLendon R, Friedman A, Bigner D, Van Meir EG, Brat DJ, Mastrogianakis M, Olson JJ, Mikkelsen T, Lehman N, et al., for Cancer Genome Atlas Research Network (2008) Comprehensive genomic characterization defines human glioblastoma genes and core pathways. Nature 455:1061-1068.
31. Mujoo K, Krumenacker JS, Wada Y, and Murad F (2006) Differential expression of nitric oxide signaling components in undifferentiated and differentiated human embryonic stem cells. Stem Cells Dev 15:779-787. (Pubitemid 46147850)
32. Mujoo K, Sharin VG, Martin E, Choi BK, Sloan C, Nikonoff LE, Kots AY, and Murad F (2010) Role of soluble guanylyl cyclase-cyclic GMP signaling in tumor cell proliferation. Nitric Oxide 22:43-50.
33. Murad F, Kimura H, Hopkins HA, Looney WB, and Kovacs CJ (1975) Increased urinary excretion of cyclic guanosine monophosphate in rats bearing Morris hepatoma 3924A. Science 190:58-60.
34. Murad F, Leitman DC, Bennett BM, Molina C, and Waldman SA (1987) Regulation of guanylate cyclase by atrial natriuretic factor and the role of cyclic GMP in vasodilation. Am J Med Sci 294:139-143. (Pubitemid 18021326)
35. Murillo-Carretero M, Ruano MJ, Matarredona ER, Villalobo A, and Estrada C (2002) Antiproliferative effect of nitric oxide on epidermal growth factor-responsive human neuroblastoma cells. J Neurochem 83:119-131.
36. Parsons DW, Jones S, Zhang X, Lin JC, Leary RJ, Angenendt P, Mankoo P, Carter H, Siu IM, Gallia GL, et al. (2008) An integrated genomic analysis of human glioblastoma multiforme. Science 321:1807-1812.
37. Rao CV (2004) Nitric oxide signaling in colon cancer chemoprevention. Mutat Res 555:107-119.
38. Ruiz-Stewart I, Tiyyagura SR, Lin JE, Kazerounian S, Pitari GM, Schulz S, Martin E, Murad F, and Waldman SA (2004) Guanylyl cyclase is an ATP sensor coupling nitric oxide signaling to cell metabolism. Proc Natl Acad Sci USA 101:37-42. (Pubitemid 38084199)
39. Ryan WL and Heidrick ML (1968) Inhibition of cell growth in vitro by adenosine 3′,5′-monophosphate. Science 162:1484-1485.
40. Shailubhai K, Yu HH, Karunanandaa K, Wang JY, Eber SL, Wang Y, Joo NS, Kim HD, Miedema BW, Abbas SZ, et al. (2000) Uroguanylin treatment suppresses polyp formation in the Apc(Min/+) mouse and induces apoptosis in human colon adenocarcinoma cells via cyclic GMP. Cancer Res 60:5151-5157.
41. Sharina IG, Jelen F, Bogatenkova EP, Thomas A, Martin E, and Murad F (2008) Alpha1 soluble guanylyl cyclase (sGC) splice forms as potential regulators of human sGC activity. J Biol Chem 283:15104-15113.
42. Singh SK, Hawkins C, Clarke ID, Squire JA, Bayani J, Hide T, Henkelman RM, Cusimano MD, and Dirks PB (2004) Identification of human brain tumour initiating cells. Nature 432:396-401. (Pubitemid 39551674)
43. Swartling FJ, Ferletta M, Kastemar M, Weiss WA, and Westermark B (2009) Cyclic GMP-dependent protein kinase II inhibits cell proliferation, Sox9 expression and Akt phosphorylation in human glioma cell lines. Oncogene 28:3121-3131.
44. Takemoto DJ, Dunford C, Vaughn D, Kramer KJ, Smith A, and Powell RG (1982) Guanylate cyclase activity in human leukemic and normal lymphocytes. Enzyme inhibition and cytotoxicity of plant extracts. Enzyme 27:179-188. (Pubitemid 12103000)
45. 1 in human hepatocellular carcinoma cells. J Pharmacol Exp Ther 312:917-925.
46. Wilcox JN, Augustine A, Goeddel DV, and Lowe DG (1991) Differential regional expression of three natriuretic peptide receptor genes within primate tissues. Mol Cell Biol 11:3454-3462. (Pubitemid 21895732)
47. Yamanaka H, Oue T, Uehara S, and Fukuzawa M (2010) Forskolin, a Hedgehog signal inhibitor, inhibits cell proliferation and induces apoptosis in pediatric tumor cell lines. Mol Med Report 3:133-139.
48. Yamanaka H, Oue T, Uehara S, and Fukuzawa M (2011) Hedgehog signal inhibitor forskolin suppresses cell proliferation and tumor growth of human rhabdomyosarcoma xenograft. J Pediatr Surg 46:320-325.
49. Yang W, Ando J, Korenaga R, Toyo-oka T, and Kamiya A (1994) Exogenous nitric oxide inhibits proliferation of cultured vascular endothelial cells. Biochem Biophys Res Commun 203:1160-1167. (Pubitemid 24304951)
50. Yuan X, Curtin J, Xiong Y, Liu G, Waschsmann-Hogiu S, Farkas DL, Black KL, and Yu JS (2004) Isolation of cancer stem cells from adult glioblastoma multiforme. Oncogene 23:9392-9400. (Pubitemid 40069671)
51. Zabel U, Weeger M, La M, and Schmidt HH (1998) Human soluble guanylate cyclase: functional expression and revised isoenzyme family. Biochem J 335:51-57. (Pubitemid 28477049)
52. Zhu H, Wei X, Bian K, and Murad F (2008) Effects of nitric oxide on skin burn wound healing. J Burn Care Res 29:804-814.