Adrenomedullin and nitric oxide: Implications for the etiology and treatment of primary brain tumors

CNS and Neurological Disorders - Drug Targets

Volumn 10, Issue 7, 2011, Pages 820-833

  Fernández, Ana P ^a   Serrano, Julia ^a   Amorim, Miguel A ^a   Pozo Rodrigálvarez, Andrea ^a   Martínez Murillo, Ricardo ^a  

^a INSTITUTO CAJAL   (Spain)

Author keywords

Adrenomedullin; Angiogenesis; Antiangiogenic treatment; Apoptosis; Astrocytoma; Brain tumor; Glioma; Nitric oxide

Indexed keywords

ADRENOMEDULLIN; BASIC FIBROBLAST GROWTH FACTOR RECEPTOR; BEVACIZUMAB; CALCITONIN; CARMUSTINE; CEDIRANIB; FIBROBLAST GROWTH FACTOR 2; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; N(G) NITROARGININE METHYL ESTER; NITRIC OXIDE; NITRIC OXIDE SYNTHASE; PROTEIN BCL 2; TEMOZOLOMIDE; VASCULOTROPIN;

ANGIOGENESIS; APOPTOSIS; ASTROCYTOMA; BRAIN CANCER; GLIOBLASTOMA; HUMAN; METASTASIS; NONHUMAN; PROTEIN EXPRESSION; RECURRENT CANCER; REVIEW; TUMOR GROWTH;

EID: 81155123354     PISSN: 18715273     EISSN: 19963181     Source Type: Journal    
DOI: 10.2174/187152711798072374     Document Type: Review

References (251)

1. DeAngelis, L.M. Brain tumors. N. Engl. J. Med., 2001, 344(2), 114-123.
2. Deorah, S.; Lynch, C.F.; Sibenaller, Z.A.; Ryken, T.C. Trends in brain cancer incidence and survival in the United States: Surveillance, Epidemiology, and End Results Program, 1973 to 2001. Neurosurg. Focus, 2006, 20(4), E1.
3. CBTRUS. Statistical Report: Primary Brain Tumors in the United States, 1998-2002. Published by the Central Brain Tumor Registry of the United States. 2005.
4. Perry, J.R.; Belanger, K.; Mason, W.P.; Fulton, D.; Kavan, P.; Easaw, J.; Shields, C.; Kirby, S.; Macdonald, D.R.; Eisenstat, D.D.; Thiessen, B.; Forsyth, P.; Pouliot, J.F. Phase II trial of continuous dose-intense temozolomide in recurrent malignant glioma: RESCUE study. J. Clin. Oncol., 2010, 28(12), 2051-2057.
5. Hendriksen, E.M.; Span, P.N.; Schuuring, J.; Peters, J.P.; Sweep, F.C.; van der Kogel, A.J.; Bussink, J. Angiogenesis, hypoxia and VEGF expression during tumour growth in a human xenograft tumour model. Microvasc. Res., 2009, 77(2), 96-103.
6. Folkman, J.; Klagsbrun, M. Angiogenic factors. Science, 1987, 235(4787), 442-447.
7. Martinez, A.; Marin, V.G.; Junquera, S.R.; Martinez-Murillo, R.; Freire, M. The contributions of Santiago Ramon y Cajal to cancer research 100 years on. Nat. Rev. Cancer, 2005, 5(11), 904-909.
8. Kogel, D.; Fulda, S.; Mittelbronn, M. Therapeutic exploitation of apoptosis and autophagy for glioblastoma. Anticancer Agents Med. Chem., 2010, 10(6), 438-449.
9. Kargiotis, O.; Geka, A.; Rao, J.S.; Kyritsis, A.P. Effects of irradiation on tumor cell survival, invasion and angiogenesis. J. Neurooncol., 2010, 100(3), 323-338.
10. Campos, B.; Herold-Mende, C.C. Insight into the complex regulation of CD133 in glioma. Int. J. Cancer, 2011, 128(3), 501-510.
11. Singh, S.K.; Hawkins, C.; Clarke, I.D.; Squire, J.A.; Bayani, J.; Hide, T.; Henkelman, R.M.; Cusimano, M.D.; Dirks, P.B. Identification of human brain tumour initiating cells. Nature, 2004, 432(7015), 396-401.
12. Singh, S.K.; Clarke, I.D.; Hide, T.; Dirks, P.B. Cancer stem cells in nervous system tumors. Oncogene, 2004, 23(43), 7267-7273.
13. Stupp, R.; Hegi, M.E. Targeting brain-tumor stem cells. Nat. Biotechnol., 2007, 25(2), 193-194.
14. Wong, J.W. MicroRNA-induced silencing of glioma progression. J. Neurosci., 2010, 30(11), 3868-3869.
15. Wong, M.L.; Prawira, A.; Kaye, A.H.; Hovens, C.M. Tumour angiogenesis: its mechanism and therapeutic implications in malignant gliomas. J. Clin. Neurosci., 2009, 16(9), 1119-1130.
16. Onishi, M.; Ichikawa, T.; Kurozumi, K.; Date, I. Angiogenesis and invasion in glioma. Brain Tumor Pathol., 2011, 28(1), 13-24.
17. Bello, L.; Giussani, C.; Carrabba, G.; Pluderi, M.; Costa, F.; Bikfalvi, A. Angiogenesis and invasion in gliomas. Cancer Treat. Res., 2004, 117, 263-284.
18. Kesari, S.; Schiff, D.; Henson, J.W.; Muzikansky, A.; Gigas, D.C.; Doherty, L.; Batchelor, T.T.; Longtine, J.A.; Ligon, K.L.; Weaver, S.; Laforme, A.; Ramakrishna, N.; Black, P.M.; Drappatz, J.; Ciampa, A.; Folkman, J.; Kieran, M.; Wen, P.Y. Phase II study of temozolomide, thalidomide, and celecoxib for newly diagnosed glioblastoma in adults. NeuroOncology, 2008, 10(3), 300-308.
19. Satchi-Fainaro, R.; Puder, M.; Davies, J.W.; Tran, H.T.; Sampson, D.A.; Greene, A.K.; Corfas, G.; Folkman, J. Targeting angiogenesis with a conjugate of HPMA copolymer and TNP-470. Nat. Med., 2004, 10(3), 255-261.
20. Ouafik, L.; Sauze, S.; Boudouresque, F.; Chinot, O.; Delfino, C.; Fina, F.; Vuaroqueaux, V.; Dussert, C.; Palmari, J.; Dufour, H.; Grisoli, F.; Casellas, P.; Brunner, N.; Martin, P.M. Neutralization of adrenomedullin inhibits the growth of human glioblastoma cell lines in vitro and suppresses tumor xenograft growth in vivo. Am. J. Pathol., 2002, 160(4), 1279-1292.
21. Martinez, A. A new family of angiogenic factors. Cancer Lett., 2006, 236(2), 157-163.
22. Folkman, J. Angiogenesis and apoptosis. Semin. Cancer Biol., 2003, 13(2), 159-167.
23. Neyns, B.; Sadones, J.; Chaskis, C.; Dujardin, M.; Everaert, H.; Lv, S.; Duerinck, J.; Tynninen, O.; Nupponen, N.; Michotte, A.; De, G.J. Phase II study of sunitinib malate in patients with recurrent high-grade glioma. J. Neurooncol., 2010, 103(3), 491-501.
24. Martinez, A.; Julian, M.; Bregonzio, C.; Notari, L.; Moody, T.W.; Cuttitta, F. Identification of vasoactive nonpeptidic positive and negative modulators of adrenomedullin using a neutralizing antibody-based screening strategy. Endocrinology, 2004, 145(8), 3858-3865.
25. Abasolo, I.; Montuenga, L.M.; Calvo, A. Adrenomedullin prevents apoptosis in prostate cancer cells. Regul. Pept., 2006, 133(1-3), 115-122.
26. Zudaire, E.; Martinez, A.; Cuttitta, F. Adrenomedullin and cancer. Regul. Pept., 2003, 112(1-3), 175-183.
27. Zudaire, E.; Martinez, A.; Garayoa, M.; Pio, R.; Kaur, G.; Woolhiser, M.R.; Metcalfe, D.D.; Hook, W.A.; Siraganian, R.P.; Guise, T.A.; Chirgwin, J.M.; Cuttitta, F. Adrenomedullin is a crosstalk molecule that regulates tumor and mast cell function during human carcinogenesis. Am. J. Pathol., 2006, 168(1), 280-291.
28. Fukumura, D.; Kashiwagi, S.; Jain, R.K. The role of nitric oxide in tumour progression. Nat. Rev. Cancer, 2006, 6(7), 521-534.
29. Yamaguchi, S.; Bell, H.S.; Shinoda, J.; Holmes, M.C.; Wharton, S.B.; Whittle, I.R. Glioma tumourgenicity is decreased by iNOS knockout: experimental studies using the C6 striatal implantation glioma model. Br. J. Neurosurg., 2002, 16(6), 567-572.
30. Swaroop, G.R.; Kelly, P.A.; Bell, H.S.; Shinoda, J.; Yamaguchi, S.; Whittle, I.R. The effects of chronic nitric oxide synthase suppression on glioma pathophysiology. Br. J. Neurosurg., 2000, 14(6), 543-548.
31. Badn, W.; Siesjo, P. The dual role of nitric oxide in glioma. Curr. Pharm. Des., 2010, 16(4), 428-430.
32. Lala, P.K.; Chakraborty, C. Role of nitric oxide in carcinogenesis and tumour progression. Lancet Oncol., 2001, 2(3), 149-156.
33. Bhadada, S.V.; Goyal, B.R.; Patel, M.M. Angiogenic targets for potential disorders. Fundam. Clin. Pharmacol., 2011, 25(1), 29-47.
34. Boudouresque, F.; Berthois, Y.; Martin, P.M.; Figarella-Branger, D.; Chinot, O.; Ouafik, L. Role of adrenomedullin in glioblastomas growth. Bull. Cancer, 2005, 92(4), 317-326.
35. Lopez, J.; Martinez, A. Cell and molecular biology of the multifunctional peptide, adrenomedullin. Int. Rev. Cytol., 2002, 221, 1-92.
36. Maki, T.; Ihara, M.; Fujita, Y.; Nambu, T.; Miyashita, K.; Yamada, M.; Washida, K.; Nishio, K.; Ito, H.; Harada, H.; Yokoi, H.; Arai, H.; Itoh, H.; Nakao, K.; Takahashi, R.; Tomimoto, H. Angiogenic and Vasoprotective Effects of Adrenomedullin on Prevention of Cognitive Decline After Chronic Cerebral Hypoperfusion in Mice. Stroke, 2011, 42(4), 1122-1128.
37. Ziche, M.; Morbidelli, L. Molecular regulation of tumour angiogenesis by nitric oxide. Eur. Cytokine Netw., 2009, 20(4), 164-170.
38. Moncada, S.; Higgs, E.A. Nitric oxide and the vascular endothelium. Handb. Exp. Pharmacol., 2006, (176 Pt 1), 213-254.
39. Moncada, S.; Higgs, E.A. The discovery of nitric oxide and its role in vascular biology. Br. J. Pharmacol., 2006, 147(Suppl 1), S193-S201.
40. Fukumura, D.; Jain, R.K. Role of nitric oxide in angiogenesis and microcirculation in tumors. Cancer Metastasis Rev., 1998, 17(1), 77-89.
41. Hurtado, O.; Serrano, J.; Sobrado, M.; Fernandez, A.P.; Lizasoain, I.; Martinez-Murillo, R.; Moro, M.A.; Martinez, A. Lack of adrenomedullin, but not complement factor H, results in larger infarct size and more extensive brain damage in a focal ischemia model. Neuroscience, 2010, 171(3), 885-892.
42. Azad, N.; Iyer, A.; Vallyathan, V.; Wang, L.; Castranova, V.; Stehlik, C.; Rojanasakul, Y. Role of oxidative/nitrosative stressmediated Bcl-2 regulation in apoptosis and malignant transformation. Ann. NY Acad. Sci., 2010, 1203, 1-6.
43. Steinert, J.R.; Chernova, T.; Forsythe, I.D. Nitric oxide signaling in brain function, dysfunction, and dementia. Neuroscientist, 2010, 16(4), 435-452.
44. Amitai, Y. Physiologic role for inducible nitric oxide synthase: a new form of astrocytic-neuronal interface. Glia, 2010, 58(15), 1775-1781.
45. Ziche, M.; Morbidelli, L. Nitric oxide and angiogenesis. J. Neurooncol., 2000, 50(1-2), 139-148.
46. Cserep, C.; Szonyi, A.; Veres, J.M.; Nemeth, B.; Szabadits, E.; de, V.J.; Hajos, N.; Freund, T.F.; Nyiri, G. Nitric oxide signaling modulates synaptic transmission during early postnatal development. Cereb. Cortex, 2011, 21(9), 2065-2074.
47. Attwell, D.; Buchan, A.M.; Charpak, S.; Lauritzen, M.; Macvicar, B.A.; Newman, E.A. Glial and neuronal control of brain blood flow. Nature, 2010, 468(7321), 232-243.
48. Huang, P.L.; Lo, E.H. Genetic analysis of NOS isoforms using nNOS and eNOS knockout animals. Prog. Brain Res., 1998, 118, 13-25.
49. Kaur, B.; Khwaja, F.W.; Severson, E.A.; Matheny, S.L.; Brat, D.J.; Van Meir, E.G. Hypoxia and the hypoxia-inducible-factor pathway in glioma growth and angiogenesis. NeuroOncology, 2005, 7(2), 134-153.
50. Dotsch, J.; Harmjanz, A.; Christiansen, H.; Hanze, J.; Lampert, F.; Rascher, W. Gene expression of neuronal nitric oxide synthase and adrenomedullin in human neuroblastoma using real-time PCR. Int. J. Cancer, 2000, 88(2), 172-175.
51. Ito, K.; Yoshii, H.; Asano, T.; Seta, K.; Mizuguchi, Y.; Yamanaka, M.; Tokonabe, S.; Hayakawa, M.; Asano, T. Adrenomedullin increases renal nitric oxide production and ameliorates renal injury in mice with unilateral ureteral obstruction. J. Urol., 2010, 183(4), 1630-1635.
52. Bayram, Z.; Golbasi, I.; Ozdem, S.S. The role of nitric oxide and potassium channels in the effect of adrenomedullin in human internal thoracic arteries. Regul. Pept., 2010, 161(1-3), 92-96.
53. Xu, Y.; Krukoff, T.L. Adrenomedullin stimulates nitric oxide production from primary rat hypothalamic neurons: roles of calcium and phosphatases. Mol. Pharmacol., 2007, 72(1), 112-120.
54. Hamid, S.A.; Totzeck, M.; Drexhage, C.; Thompson, I.; Fowkes, R.C.; Rassaf, T.; Baxter, G.F. Nitric oxide/cGMP signalling mediates the cardioprotective action of adrenomedullin in reperfused myocardium. Basic Res. Cardiol., 2010, 105(2), 257-266.
55. Kaur, B.; Tan, C.; Brat, D.J.; Post, D.E.; Van Meir, E.G. Genetic and hypoxic regulation of angiogenesis in gliomas. J. Neurooncol., 2004, 70(2), 229-243.
56. Jung, C.R.; Hwang, K.S.; Yoo, J.; Cho, W.K.; Kim, J.M.; Kim, W.H.; Im, D.S. E2-EPF UCP targets pVHL for degradation and associates with tumor growth and metastasis. Nat. Med., 2006, 12(7), 809-816.
57. Kalluri, R.; Zeisberg, M. Fibroblasts in cancer. Nat. Rev. Cancer, 2006, 6(5), 392-401.
58. Folkman, J. Tumor angiogenesis: therapeutic implications. N. Engl. J. Med., 1971, 285(21), 1182-1186.
59. Longo, R.; Sarmiento, R.; Fanelli, M.; Capaccetti, B.; Gattuso, D.; Gasparini, G. Anti-angiogenic therapy: rationale, challenges and clinical studies. Angiogenesis, 2002, 5(4), 237-256.
60. Gasparini, G.; Longo, R.; Fanelli, M.; Teicher, B.A. Combination of antiangiogenic therapy with other anticancer therapies: results, challenges, and open questions. J. Clin. Oncol., 2005, 23(6), 1295-1311.
61. Van Meir, E.G.; Polverini, P.J.; Chazin, V.R.; Su Huang, H.J.; de, T.N.; Cavenee, W.K. Release of an inhibitor of angiogenesis upon induction of wild type p53 expression in glioblastoma cells. Nat. Genet., 1994, 8(2), 171-176.
62. Lakka, S.S.; Rao, J.S. Antiangiogenic therapy in brain tumors. Expert Rev. Neurother., 2008, 8(10), 1457-1473.
63. Abdollahi, A.; Lipson, K.E.; Sckell, A.; Zieher, H.; Klenke, F.; Poerschke, D.; Roth, A.; Han, X.; Krix, M.; Bischof, M.; Hahnfeldt, P.; Grone, H.J.; Debus, J.; Hlatky, L.; Huber, P.E. Combined therapy with direct and indirect angiogenesis inhibition results in enhanced antiangiogenic and antitumor effects. Cancer Res., 2003, 63(24), 8890-8898.
64. Thompson, E.M.; Frenkel, E.P.; Neuwelt, E.A. The paradoxical effect of bevacizumab in the therapy of malignant gliomas. Neurology, 2011, 76(1), 87-93.
65. Sul, J.; Fine, H.A. Malignant gliomas: new translational therapies. Mt. Sinai J. Med., 2010, 77(6), 655-666.
66. Wong, E.T.; Brem, S. Taming glioblastoma by targeting angiogenesis: 3 years later. J. Clin. Oncol., 2011, 29(2), 124-126.
67. Wesseling, P.; van der Laak, J.A.; Link, M.; Teepen, H.L.; Ruiter, D.J. Quantitative analysis of microvascular changes in diffuse astrocytic neoplasms with increasing grade of malignancy. Hum. Pathol., 1998, 29(4), 352-358.
68. Van Meir, E.G.; Hadjipanayis, C.G.; Norden, A.D.; Shu, H.K.; Wen, P.Y.; Olson, J.J. Exciting new advances in neuro-oncology: the avenue to a cure for malignant glioma. CA Cancer J. Clin., 2010, 60(3), 166-193.
69. Norden, A.D.; Drappatz, J.; Wen, P.Y. Antiangiogenic therapies for high-grade glioma. Nat. Rev. Neurol., 2009, 5(11), 610-620.
70. Yang, J.C.; Haworth, L.; Sherry, R.M.; Hwu, P.; Schwartzentruber, D.J.; Topalian, S.L.; Steinberg, S.M.; Chen, H.X.; Rosenberg, S.A. A randomized trial of bevacizumab, an anti-vascular endothelial growth factor antibody, for metastatic renal cancer. N. Engl. J. Med., 2003, 349(5), 427-434.
71. Gasparini, G.; Longo, R.; Toi, M.; Ferrara, N. Angiogenic inhibitors: a new therapeutic strategy in oncology. Nat. Clin. Pract. Oncol., 2005, 2(11), 562-577.
72. Brown, J.M.; Wilson, W.R. Exploiting tumour hypoxia in cancer treatment. Nat. Rev. Cancer, 2004, 4(6), 437-447.
73. Folkman, J. The role of angiogenesis in tumor growth. Semin. Cancer Biol., 1992, 3(2), 65-71.
74. Hanahan, D.; Folkman, J. Patterns and emerging mechanisms of the angiogenic switch during tumorigenesis. Cell, 1996, 86(3), 353-364.
75. Dvorak, H.F.; Nagy, J.A.; Feng, D.; Brown, L.F.; Dvorak, A.M. Vascular permeability factor/vascular endothelial growth factor and the significance of microvascular hyperpermeability in angiogenesis. Curr. Top. Microbiol. Immunol., 1999, 237, 97-132.
76. Konno, T.; Ohtsuka, N.; Yamasaki, K.; Mizutani, J.; Miyauchi, Y.; Maeda, H.; Matsumura, Y. Targeting of anticancer chemotherapy utilizing the characteristic nature of the neovasculature of solid tumors. Gan To Kagaku Ryoho, 1986, 13(4 Pt 2), 1448-1455.
77. Holmgren, L.; O'Reilly, M.S.; Folkman, J. Dormancy of micrometastases: balanced proliferation and apoptosis in the presence of angiogenesis suppression. Nat. Med., 1995, 1(2), 149-153.
78. Patel, N.S.; Li, J.L.; Generali, D.; Poulsom, R.; Cranston, D.W.; Harris, A.L. Up-regulation of delta-like 4 ligand in human tumor vasculature and the role of basal expression in endothelial cell function. Cancer Res., 2005, 65(19), 8690-8697.
79. Lopes, M.B. Angiogenesis in brain tumors. Microsc. Res. Tech., 2003, 60(2), 225-230.
80. Lebelt, A.; Dzieciol, J.; Guzinska-Ustymowicz, K.; Lemancewicz, D.; Zimnoch, L.; Czykier, E. Angiogenesis in gliomas. Folia Histochem. Cytobiol., 2008, 46(1), 69-72.
81. Goldbrunner, R.H.; Wagner, S.; Roosen, K.; Tonn, J.C. Models for assessment of angiogenesis in gliomas. J. Neurooncol., 2000, 50(1-2), 53-62.
82. Goldbrunner, R.H.; Bendszus, M.; Tonn, J.C. Models for angiogenesis in gliomas. Cancer Treat. Res., 2004, 117, 115-135.
83. Hu, X.; Holland, E.C. Applications of mouse glioma models in preclinical trials. Mutat. Res., 2005, 576(1-2), 54-65.
84. Reilly, K.M.; Jacks, T. Genetically engineered mouse models of astrocytoma: GEMs in the rough? Semin. Cancer Biol., 2001, 11(3), 177-191.
85. Serrano, J.; Fernandez, A.P.; Martinez-Murillo, R.; Martinez, A. High sensitivity to carcinogens in the brain of a mouse model of Alzheimer's disease. Oncogene, 2010, 29(15), 2165-2171.
86. Martinez-Murillo, R.; Martinez, A. Standardization of an orthotopic mouse brain tumor model following transplantation of CT-2A astrocytoma cells. Histol. Histopathol., 2007, 22(12), 1309-1326.
87. Lasker, S.E.; Iatropoulos, M.J.; Hecht, S.S.; Misra, B.; Amin, S.; Zang, E.; Williams, G.M. N-ethyl-N-nitrosourea induced brain tumors in rats monitored by nuclear magnetic resonance imaging, plasma proton nuclear magnetic resonance spectroscopy and microscopy. Cancer Lett., 1992, 67(2-3), 125-131.
88. Hambardzumyan, D.; Parada, L.F.; Holland, E.C.; Charest, A. Genetic modeling of gliomas in mice: new tools to tackle old problems. Glia, 2011, 59(8), 1155-1168.
89. Kolibaba, K.S.; Druker, B.J. Protein tyrosine kinases and cancer. Biochim. Biophys. Acta, 1997, 1333(3), F217-F248.
90. Auguste, P.; Gursel, D.B.; Lemiere, S.; Reimers, D.; Cuevas, P.; Carceller, F.; Di Santo, J.P.; Bikfalvi, A. Inhibition of fibroblast growth factor/fibroblast growth factor receptor activity in glioma cells impedes tumor growth by both angiogenesis-dependent and independent mechanisms. Cancer Res., 2001, 61(4), 1717-1726.
91. Cuevas, P.; Carceller, F.; Angulo, J.; Gonzalez-Corrochano, R.; Cuevas-Bourdier, A.; Gimenez-Gallego, G. Antiglioma effects of a new, low molecular mass, inhibitor of fibroblast growth factor. Neurosci. Lett., 2011, 491(1), 1-7.
92. Tao, J.; Xiang, J.J.; Li, D.; Deng, N.; Wang, H.; Gong, Y.P. Selection and characterization of a human neutralizing antibody to human fibroblast growth factor-2. Biochem. Biophys. Res. Commun., 2010, 394(3), 767-773.
93. Argyriou, A.A.; Giannopoulou, E.; Kalofonos, H.P. Angiogenesis and anti-angiogenic molecularly targeted therapies in malignant gliomas. Oncology, 2009, 77(1), 1-11.
94. Norden, A.D.; Drappatz, J.; Wen, P.Y. Novel anti-angiogenic therapies for malignant gliomas. Lancet Neurol., 2008, 7(12), 1152-1160.
95. Kim, K.J.; Li, B.; Winer, J.; Armanini, M.; Gillett, N.; Phillips, H.S.; Ferrara, N. Inhibition of vascular endothelial growth factorinduced angiogenesis suppresses tumour growth in vivo. Nature, 1993, 362(6423), 841-844.
96. di, T.E.; Snuderl, M.; Kamoun, W.S.; Duda, D.G.; Auluck, P.K.; Fazlollahi, L.; Andronesi, O.C.; Frosch, M.P.; Wen, P.Y.; Plotkin, S.R.; Hedley-Whyte, E.T.; Sorensen, A.G.; Batchelor, T.T.; Jain, R.K. Glioblastoma recurrence after cediranib therapy in patients: lack of rebound revascularization as mode of escape. Cancer Res., 2011, 71(1), 19-28.
97. Batchelor, T.T.; Duda, D.G.; di, T.E.; Ancukiewicz, M.; Plotkin, S.R.; Gerstner, E.; Eichler, A.F.; Drappatz, J.; Hochberg, F.H.; Benner, T.; Louis, D.N.; Cohen, K.S.; Chea, H.; Exarhopoulos, A.; Loeffler, J.S.; Moses, M.A.; Ivy, P.; Sorensen, A.G.; Wen, P.Y.; Jain, R.K. Phase II study of cediranib, an oral pan-vascular endothelial growth factor receptor tyrosine kinase inhibitor, in patients with recurrent glioblastoma. J. Clin. Oncol., 2010, 28(17), 2817-2823.
98. Ishiwata, T.; Matsuda, Y.; Naito, Z. Nestin in gastrointestinal and other cancers: Effects on cells and tumor angiogenesis. World J. Gastroenterol., 2011, 17(4), 409-418.
99. Krupkova, O., Jr.; Loja, T.; Zambo, I.; Veselska, R. Nestin expression in human tumors and tumor cell lines. Neoplasma, 2010, 57(4), 291-298.
100. Mokry, J.; Ehrmann, J.; Karbanova, J.; Cizkova, D.; Soukup, T.; Suchanek, J.; Filip, S.; Kolar, Z. Expression of intermediate filament nestin in blood vessels of neural and non-neural tissues. Acta Medica. Hradec. Kralove, 2008, 51(3), 173-179.
101. Mokry, J.; Cizkova, D.; Filip, S.; Ehrmann, J.; Osterreicher, J.; Kolar, Z.; English, D. Nestin expression by newly formed human blood vessels. Stem Cells Dev., 2004, 13(6), 658-664.
102. Sugawara, K.; Kurihara, H.; Negishi, M.; Saito, N.; Nakazato, Y.; Sasaki, T.; Takeuchi, T. Nestin as a marker for proliferative endothelium in gliomas. Lab. Invest., 2002, 82(3), 345-351.
103. Christensen, K.; Schroder, H.D.; Kristensen, B.W. CD133 identifies perivascular niches in grade II-IV astrocytomas. J. Neurooncol., 2008, 90(2), 157-170.
104. Dell'Albani, P. Stem cell markers in gliomas. Neurochem. Res., 2008, 33(12), 2407-2415.
105. Aguado, T.; Carracedo, A.; Julien, B.; Velasco, G.; Milman, G.; Mechoulam, R.; Alvarez, L.; Guzman, M.; Galve-Roperh, I. Cannabinoids induce glioma stem-like cell differentiation and inhibit gliomagenesis. J. Biol. Chem., 2007, 282(9), 6854-6862.
106. Blazquez, C.; Gonzalez-Feria, L.; Alvarez, L.; Haro, A.; Casanova, M.L.; Guzman, M. Cannabinoids inhibit the vascular endothelial growth factor pathway in gliomas. Cancer Res., 2004, 64(16), 5617-5623.
107. Salazar, M.; Carracedo, A.; Salanueva, I.J.; Hernandez-Tiedra, S.; Lorente, M.; Egia, A.; Vazquez, P.; Blazquez, C.; Torres, S.; Garcia, S.; Nowak, J.; Fimia, G.M.; Piacentini, M.; Cecconi, F.; Pandolfi, P.P.; Gonzalez-Feria, L.; Iovanna, J.L.; Guzman, M.; Boya, P.; Velasco, G. Cannabinoid action induces autophagymediated cell death through stimulation of ER stress in human glioma cells. J. Clin. Invest., 2009, 119(5), 1359-1372.
108. Hay, D.L.; Walker, C.S.; Poyner, D.R. Adrenomedullin and calcitonin gene-related peptide receptors in endocrine-related cancers: opportunities and challenges. Endocr. Relat. Cancer, 2011, 18(1), C1-14.
109. Nikitenko, L.L.; Fox, S.B.; Kehoe, S.; Rees, M.C.; Bicknell, R. Adrenomedullin and tumour angiogenesis. Br. J. Cancer, 2006, 94(1), 1-7.
110. Takahashi, K.; Satoh, F.; Hara, E.; Sone, M.; Murakami, O.; Kayama, T.; Yoshimoto, T.; Shibahara, S. Production and secretion of adrenomedullin from glial cell tumors and its effects on cAMP production. Peptides, 1997, 18(8), 1117-1124.
111. Deville, J.L.; Bartoli, C.; Berenguer, C.; Fernandez-Sauze, S.; Kaafarani, I.; Delfino, C.; Fina, F.; Salas, S.; Muracciole, X.; Mancini, J.; Lechevallier, E.; Martin, P.M.; Figarella-Branger, D.; Ouafik, L.; Daniel, L. Expression and role of adrenomedullin in renal tumors and value of its mRNA levels as prognostic factor in clear-cell renal carcinoma. Int. J. Cancer, 2009, 125(10), 2307-2315.
112. Jones, R.J.; Jourd'heuil, D.; Salerno, J.C.; Smith, S.M.; Singer, H.A. iNOS regulation by calcium/calmodulin-dependent protein kinase II in vascular smooth muscle. Am. J. Physiol. Heart Circ. Physiol., 2007, 292(6), H2634-H2642.
113. Kroncke, K.D.; Suschek, C.V.; Kolb-Bachofen, V. Implications of inducible nitric oxide synthase expression and enzyme activity. Antioxid. Redox Signal. 2000, 2(3), 585-605.
114. Yang, D.I.; Yin, J.H.; Mishra, S.; Mishra, R.; Hsu, C.Y. NO-mediated chemoresistance in C6 glioma cells. Ann. NY Acad. Sci., 2002, 962, 8-17.
115. Wink, D.A.; Vodovotz, Y.; Laval, J.; Laval, F.; Dewhirst, M.W.; Mitchell, J.B. The multifaceted roles of nitric oxide in cancer. Carcinogenesis, 1998, 19(5), 711-721.
116. Bulnes, S.; Argandona, E.G.; Bengoetxea, H.; Leis, O.; Ortuzar, N.; Lafuente, J.V. The role of eNOS in vascular permeability in ENUinduced gliomas. Acta Neurochir. Suppl., 2010, 106, 277-282.
117. Erdamar, S.; Bagci, P.; Oz, B.; Dirican, A. Correlation of endothelial nitric oxide synthase and vascular endothelial growth factor expression with malignancy in patients with astrocytic tumors. J. BUON, 2006, 11(2), 213-216.
118. Broholm, H.; Rubin, I.; Kruse, A.; Braendstrup, O.; Schmidt, K.; Skriver, E.B.; Lauritzen, M. Nitric oxide synthase expression and enzymatic activity in human brain tumors. Clin. Neuropathol., 2003, 22(6), 273-281.
119. Chen, J.; Zacharek, A.; Zhang, C.; Jiang, H.; Li, Y.; Roberts, C.; Lu, M.; Kapke, A.; Chopp, M. Endothelial nitric oxide synthase regulates brain-derived neurotrophic factor expression and neurogenesis after stroke in mice. J. Neurosci., 2005, 25(9), 2366-2375.
120. Rubenstein, J.L.; Kim, J.; Ozawa, T.; Zhang, M.; Westphal, M.; Deen, D.F.; Shuman, M.A. Anti-VEGF antibody treatment of glioblastoma prolongs survival but results in increased vascular cooption. Neoplasia, 2000, 2(4), 306-314.
121. Martinez, A.; Zudaire, E.; Portal-Nunez, S.; Guedez, L.; Libutti, S.K.; Stetler-Stevenson, W.G.; Cuttitta, F. Proadrenomedullin NH2-terminal 20 peptide is a potent angiogenic factor, and its inhibition results in reduction of tumor growth. Cancer Res., 2004, 64(18), 6489-6494.
122. Bree, R.T.; Stenson-Cox, C.; Grealy, M.; Byrnes, L.; Gorman, A.M.; Samali, A. Cellular longevity: role of apoptosis and replicative senescence. Biogerontology, 2002, 3(4), 195-206.
123. Fulda, S.; Debatin, K.M. Apoptosis signaling in tumor therapy. Ann. NY Acad. Sci., 2004, 1028, 150-156.
124. Quintieri, L.; Fantin, M.; Vizler, C. Identification of molecular determinants of tumor sensitivity and resistance to anticancer drugs. Adv. Exp. Med. Biol., 2007, 593, 95-104.
125. Longley, D.B.; Johnston, P.G. Molecular mechanisms of drug resistance. J. Pathol., 2005, 205(2), 275-292.
126. Plati, J.; Bucur, O.; Khosravi-Far, R. Apoptotic cell signaling in cancer progression and therapy. Integr. Biol. (Camb.), 2011, 3(4), 279-296.
127. Umansky, V.; Rocha, M.; Breitkreutz, R.; Hehner, S.; Bucur, M.; Erbe, N.; Droge, W.; Ushmorov, A. Glutathione is a factor of resistance of Jurkat leukemia cells to nitric oxide-mediated apoptosis. J. Cell Biochem., 2000, 78(4), 578-587.
128. Mori, S.; Ito, G.; Usami, N.; Yoshioka, H.; Ueda, Y.; Kodama, Y.; Takahashi, M.; Fong, K.M.; Shimokata, K.; Sekido, Y. p53 apoptotic pathway molecules are frequently and simultaneously altered in nonsmall cell lung carcinoma. Cancer, 2004, 100(8), 1673-1682.
129. Boumela, I.; Assou, S.; Aouacheria, A.; Haouzi, D.; Dechaud, H.; De, V.J.; Handyside, A.; Hamamah, S. Involvement of Bcl-2 family members in the regulation of human oocyte and early embryo survival and death: gene expression and beyond. Reproduction, 2011, 141(5), 549-61.
130. Kabore, A.F.; Johnston, J.B.; Gibson, S.B. Changes in the apoptotic and survival signaling in cancer cells and their potential therapeutic implications. Curr. Cancer Drug Targets, 2004, 4(2), 147-163.
131. Dutta, J.; Fan, Y.; Gupta, N.; Fan, G.; Gelinas, C. Current insights into the regulation of programmed cell death by NF-kappaB. Oncogene, 2006, 25(51), 6800-6816.
132. Xia, C.F.; Yin, H.; Borlongan, C.V.; Chao, J.; Chao, L. Postischemic infusion of adrenomedullin protects against ischemic stroke by inhibiting apoptosis and promoting angiogenesis. Exp. Neurol., 2006, 197(2), 521-530.
133. Xia, C.F.; Yin, H.; Borlongan, C.V.; Chao, J.; Chao, L. Adrenomedullin gene delivery protects against cerebral ischemic injury by promoting astrocyte migration and survival. Hum. Gene Ther., 2004, 15(12), 1243-1254.
134. Ola, M.S.; Nawaz, M.; Ahsan, H. Role of Bcl-2 family proteins and caspases in the regulation of apoptosis. Mol. Cell Biochem., 2011, 351(1-2), 41-58.
135. Lam-Himlin, D.; Espey, M.G.; Perry, G.; Smith, M.A.; Castellani, R.J. Malignant glioma progression and nitric oxide. Neurochem. Int., 2006, 49(8), 764-768.
136. Weyerbrock, A.; Baumer, B.; Papazoglou, A. Growth inhibition and chemosensitization of exogenous nitric oxide released from NONOates in glioma cells in vitro. J. Neurosurg., 2009, 110(1), 128-136.
137. Yang, J.J.; Yin, J.H.; Yang, D.I. Nitric oxide donors attenuate clongenic potential in rat C6 glioma cells treated with alkylating chemotherapeutic agents. Neurosci. Lett., 2007, 418(1), 106-110.
138. Kim, J.H.; Zheng, L.T.; Lee, W.H.; Suk, K. Pro-apoptotic role of integrin beta3 in glioma cells. J. Neurochem., 2011, 117(3), 494-503.
139. Shinoda, J.; Whittle, I.R. Nitric oxide and glioma: a target for novel therapy? Br. J. Neurosurg., 2001, 15(3), 213-220.
140. Takahashi, K. Multifunctional peptide, adrenomedullin. Seikagaku, 2001, 73(2), 99-104.
141. Deville, J.L.; Salas, S.; Figarella-Branger, D.; Ouafik, L.; Daniel, L. Adrenomedullin as a therapeutic target in angiogenesis. Expert Opin. Ther. Targets, 2010, 14(10), 1059-1072.
142. Ribatti, D.; Conconi, M.T.; Nussdorfer, G.G. Nonclassic endogenous novel[corrected] regulators of angiogenesis. Pharmacol. Rev., 2007, 59(2), 185-205.
143. Ishikawa, T.; Chen, J.; Wang, J.; Okada, F.; Sugiyama, T.; Kobayashi, T.; Shindo, M.; Higashino, F.; Katoh, H.; Asaka, M.; Kondo, T.; Hosokawa, M.; Kobayashi, M. Adrenomedullin antagonist suppresses in vivo growth of human pancreatic cancer cells in SCID mice by suppressing angiogenesis. Oncogene, 2003, 22(8), 1238-1242.
144. Hinson, J.P.; Kapas, S.; Smith, D.M. Adrenomedullin, a multifunctional regulatory peptide. Endocr. Rev., 2000, 21(2), 138-167.
145. Serrano, J.; Uttenthal, L.O.; Martinez, A.; Fernandez, A.P.; Martinez, d. V; Alonso D.; Bentura M.L.; Santacana M.; Gallardo J.R.; Martinez-Murillo, R.; Cuttitta F.; Rodrigo J. Distribution of adrenomedullin-like immunoreactivity in the rat central nervous system by light and electron microscopy. Brain Res., 2000, 853(2), 245-268.
146. Serrano, J.; Alonso, D.; Fernandez, A.P.; Encinas, J.M.; Lopez, J.C.; Castro-Blanco, S.; Fernandez-Vizarra, P.; Richart, A.; Santacana, M.; Uttenthal, L.O.; Bentura, M.L.; Martinez-Murillo, R.; Martinez, A.; Cuttitta, F.; Rodrigo, J. Adrenomedullin in the central nervous system. Microsc. Res. Tech., 2002, 57(2), 76-90.
147. Kitamura, K.; Sakata, J.; Kangawa, K.; Kojima, M.; Matsuo, H.; Eto, T. Cloning and characterization of cDNA encoding a precursor for human adrenomedullin. Biochem. Biophys. Res. Commun., 1993, 194(2), 720-725.
148. Kitamura, K.; Kangawa, K.; Kawamoto, M.; Ichiki, Y.; Nakamura, S.; Matsuo, H.; Eto, T. Adrenomedullin: a novel hypotensive peptide isolated from human pheochromocytoma. Biochem. Biophys. Res. Commun., 1993, 192(2), 553-560.
149. Kis, B.; Abraham, C.S.; Deli, M.A.; Kobayashi, H.; Niwa, M.; Yamashita, H.; Busija, D.W.; Ueta, Y. Adrenomedullin, an autocrine mediator of blood-brain barrier function. Hypertens. Res., 2003, 26(Suppl), S61-S70.
150. Encinas, J.M.; Serrano, J.; Alonso, D.; Fernandez, A.P.; Rodrigo, J. Adrenomedullin over-expression in the caudate-putamen of the adult rat brain after ischaemia-reperfusion injury. Neurosci. Lett., 2002, 329(2), 197-200.
151. Serrano, J.; Alonso, D.; Encinas, J.M.; Lopez, J.C.; Fernandez, A.P.; Castro-Blanco, S.; Fernandez-Vizarra, P.; Richart, A.; Bentura, M.L.; Santacana, M.; Uttenthal, L.O.; Cuttitta, F.; Rodrigo, J.; Martinez, A. Adrenomedullin expression is upregulated by ischemia-reperfusion in the cerebral cortex of the adult rat. Neuroscience, 2002, 109(4), 717-731.
152. Fernandez, A.P.; Serrano, J.; Tessarollo, L.; Cuttitta, F.; Martinez, A. Lack of adrenomedullin in the mouse brain results in behavioral changes, anxiety, and lower survival under stress conditions. Proc. Natl. Acad. Sci. USA, 2008, 105(34), 12581-12586.
153. Vergano-Vera, E.; Fernandez, A.P.; Hurtado-Chong, A.; Vicario-Abejon, C.; Martinez, A. Lack of adrenomedullin affects growth and differentiation of adult neural stem/progenitor cells. Cell Tissue Res., 2010, 340(1), 1-11.
154. Serrano, J.; Encinas, J.M.; Fernandez, A.P.; Castro-Blanco, S.; Alonso, D.; Fernandez-Vizarra, P.; Richart, A.; Bentura, M.L.; Santacana, M.; Cuttitta, F.; Martinez, A.; Rodrigo, J. Distribution of immunoreactivity for the adrenomedullin binding protein, complement factor H, in the rat brain. Neuroscience, 2003, 116(4), 947-962.
155. Lucyk, S.; Taha, H.; Yamamoto, H.; Miskolzie, M.; Kotovych, G. NMR conformational analysis of proadrenomedullin N-terminal 20 peptide, a proangiogenic factor involved in tumor growth. Biopolymers, 2006, 81(4), 295-308.
156. Martinez, A.; Bengoechea, J.A.; Cuttitta, F. Molecular evolution of proadrenomedullin N-terminal 20 peptide(PAMP): evidence for gene co-option. Endocrinology, 2006, 147(7), 3457-3461.
157. Kapas, S.; Clark, A.J. Identification of an orphan receptor gene as a type 1 calcitonin gene-related peptide receptor. Biochem. Biophys. Res. Commun., 1995, 217(3), 832-838.
158. Kapas, S.; Catt, K.J.; Clark, A.J. Cloning and expression of cDNA encoding a rat adrenomedullin receptor. J. Biol. Chem., 1995, 270(43), 25344-25347.
159. Fraser, N.J.; Wise, A.; Brown, J.; McLatchie, L.M.; Main, M.J.; Foord, S.M. The amino terminus of receptor activity modifying proteins is a critical determinant of glycosylation state and ligand binding of calcitonin receptor-like receptor. Mol. Pharmacol., 1999, 55(6), 1054-1059.
160. McLatchie, L.M.; Fraser, N.J.; Main, M.J.; Wise, A.; Brown, J.; Thompson, N.; Solari, R.; Lee, M.G.; Foord, S.M. RAMPs regulate the transport and ligand specificity of the calcitonin-receptor-like receptor. Nature, 1998, 393(6683), 333-339.
161. Serrano, J.; Fernandez, A.P.; Sanchez, J.; Rodrigo, J.; Martinez, A. Adrenomedullin expression is up-regulated by acute hypobaric hypoxia in the cerebral cortex of the adult rat. Brain Pathol., 2008, 18(3), 434-442.
162. Keleg, S.; Kayed, H.; Jiang, X.; Penzel, R.; Giese, T.; Buchler, M.W.; Friess, H.; Kleeff, J. Adrenomedullin is induced by hypoxia and enhances pancreatic cancer cell invasion. Int. J. Cancer, 2007, 121(1), 21-32.
163. Kato, H.; Shichiri, M.; Marumo, F.; Hirata, Y. Adrenomedullin as an autocrine/paracrine apoptosis survival factor for rat endothelial cells. Endocrinology, 1997, 138(6), 2615-2620.
164. Shichiri, M.; Kato, H.; Doi, M.; Marumo, F.; Hirata, Y. Induction of max by adrenomedullin and calcitonin gene-related peptide antagonizes endothelial apoptosis. Mol. Endocrinol., 1999, 13(8), 1353-1363.
165. Kim, W.; Moon, S.O.; Sung, M.J.; Kim, S.H.; Lee, S.; Kim, H.J.; Koh, G.Y.; Park, S.K. Protective effect of adrenomedullin in mannitol-induced apoptosis. Apoptosis, 2002, 7(6), 527-536.
166. Ramachandran, V.; Arumugam, T.; Hwang, R.F.; Greenson, J.K.; Simeone, D.M.; Logsdon, C.D. Adrenomedullin is expressed in pancreatic cancer and stimulates cell proliferation and invasion in an autocrine manner via the adrenomedullin receptor, ADMR. Cancer Res., 2007, 67(6), 2666-2675.
167. Nakamura, M.; Han, B.; Nunobiki, O.; Kakudo, K. Adrenomedullin: a tumor progression factor via angiogenic control. Curr. Cancer Drug Targets, 2006, 6(7), 635-643.
168. Takahashi, K.; Udono-Fujimori, R.; Totsune, K.; Murakami, O.; Shibahara, S. Suppression of cytokine-induced expression of adrenomedullin and endothelin-1 by dexamethasone in T98G human glioblastoma cells. Peptides, 2003, 24(7), 1053-1062.
169. Cormier-Regard, S.; Nguyen, S.V.; Claycomb, W.C. Adrenomedullin gene expression is developmentally regulated and induced by hypoxia in rat ventricular cardiac myocytes. J. Biol. Chem., 1998, 273(28), 17787-17792.
170. Garayoa, M.; Martinez, A.; Lee, S.; Pio, R.; An, W.G.; Neckers, L.; Trepel, J.; Montuenga, L.M.; Ryan, H.; Johnson, R.; Gassmann, M.; Cuttitta, F. Hypoxia-inducible factor-1(HIF-1) up-regulates adrenomedullin expression in human tumor cell lines during oxygen deprivation: a possible promotion mechanism of carcinogenesis. Mol. Endocrinol., 2000, 14(6), 848-862.
171. Spinella, F.; Rosano, L.; Di, C., V; Natali, P.G.; Bagnato, A. Endothelin-1 induces vascular endothelial growth factor by increasing hypoxia-inducible factor-1alpha in ovarian carcinoma cells. J. Biol. Chem., 2002, 277(31), 27850-27855.
172. Yamaguchi, T.; Dayton, C.; Shigematsu, T.; Carter, P.; Yoshikawa, T.; Gute, D.C.; Korthuis, R.J. Preconditioning with ethanol prevents postischemic leukocyte-endothelial cell adhesive interactions. Am. J. Physiol. Heart Circ. Physiol., 2002, 283(3), H1019-H1030.
173. Miller, M.J.; Martinez, A.; Unsworth, E.J.; Thiele, C.J.; Moody, T.W.; Elsasser, T.; Cuttitta, F. Adrenomedullin expression in human tumor cell lines.Its potential role as an autocrine growth factor. J. Biol. Chem., 1996, 271(38), 23345-23351.
174. Garcia, M.A.; Martin-Santamaria, S.; de Pascual-Teresa, B.; Ramos, A.; Julian, M.; Martinez, A. Adrenomedullin: a new and promising target for drug discovery. Expert Opin. Ther. Targets, 2006, 10(2), 303-317.
175. Julian, M.; Cacho, M.; Garcia, M.A.; Martin-Santamaria, S.; de Pascual-Teresa, B.; Ramos, A.; Martinez, A.; Cuttitta, F. Adrenomedullin: a new target for the design of small molecule modulators with promising pharmacological activities. Eur. J. Med. Chem., 2005, 40(8), 737-750.
176. Sugo, S.; Minamino, N.; Kangawa, K.; Miyamoto, K.; Kitamura, K.; Sakata, J.; Eto, T.; Matsuo, H. Endothelial cells actively synthesize and secrete adrenomedullin. Biochem. Biophys. Res. Commun., 1994, 201(3), 1160-1166.
177. Hinson, J.P.; Kapas, S. The role of endothelial cell products in the regulation of adrenocortical function: actions of endothelin, nitric oxide, adrenomedullin and PAMP. Horm. Metab. Res., 1998, 30(6-7), 334-340.
178. Ishizaka, Y.; Ishizaka, Y.; Tanaka, M.; Kitamura, K.; Kangawa, K.; Minamino, N.; Matsuo, H.; Eto, T. Adrenomedullin stimulates cyclic AMP formation in rat vascular smooth muscle cells. Biochem. Biophys. Res. Commun., 1994, 200(1), 642-646.
179. Moody, T.W.; Miller, M.J.; Martinez, A.; Unsworth, E.; Cuttitta, F. Adrenomedullin binds with high affinity, elevates cyclic AMP, and stimulates c-fos mRNA in C6 glioma cells. Peptides, 1997, 18(8), 1111-1115.
180. Kohno, M.; Yasunari, K.; Yokokawa, K.; Horio, T.; Ikeda, M.; Kano, H.; Minami, M.; Hanehira, T.; Yoskikawa, J. Interaction of adrenomedullin and platelet-derived growth factor on rat mesangial cell production of endothelin. Hypertension, 1996, 27(3 Pt 2), 663-667.
181. Terata, K.; Miura, H.; Liu, Y.; Loberiza, F.; Gutterman, D.D. Human coronary arteriolar dilation to adrenomedullin: role of nitric oxide and K(+) channels. Am. J. Physiol. Heart Circ. Physiol., 2000, 279(6), H2620-H2626.
182. Uezono, Y.; Shibuya, I.; Ueda, Y.; Tanaka, K.; Oishi, Y.; Yanagihara, N.; Ueno, S.; Toyohira, Y.; Nakamura, T.; Yamashita, H.; Izumi, F. Adrenomedullin increases intracellular Ca2+ and inositol 1,4,5-trisphosphate in human oligodendroglial cell line KG-1C. Brain Res., 1998, 786(1-2), 230-234.
183. Hayakawa, H.; Hirata, Y.; Kakoki, M.; Suzuki, Y.; Nishimatsu, H.; Nagata, D.; Suzuki, E.; Kikuchi, K.; Nagano, T.; Kangawa, K.; Matsuo, H.; Sugimoto, T.; Omata, M. Role of nitric oxide-cGMP pathway in adrenomedullin-induced vasodilation in the rat. Hypertension, 1999, 33(2), 689-693.
184. Dasari, V.R.; Kaur, K.; Velpula, K.K.; Gujrati, M.; Fassett, D.; Klopfenstein, J.D.; Dinh, D.H.; Rao, J.S. Upregulation of PTEN in glioma cells by cord blood mesenchymal stem cells inhibits migration via downregulation of the PI3K/Akt pathway. PLoS One, 2010, 5(4), e10350.
185. Knobbe, C.B.; Merlo, A.; Reifenberger, G. Pten signaling in gliomas. NeuroOncology, 2002, 4(3), 196-211.
186. Abe, T.; Terada, K.; Wakimoto, H.; Inoue, R.; Tyminski, E.; Bookstein, R.; Basilion, J.P.; Chiocca, E.A. PTEN decreases in vivo vascularization of experimental gliomas in spite of proangiogenic stimuli. Cancer Res., 2003, 63(9), 2300-2305.
187. Betchen, S.A.; Musatov, S.; Roberts, J.; Pena, J.; Kaplitt, M.G. PTEN inhibits adrenomedullin expression and function in brain tumor cells. J. Neurooncol., 2006, 79(2), 117-123.
188. Thomsen, L.L.; Miles, D.W. Role of nitric oxide in tumour progression: lessons from human tumours. Cancer Metastasis Rev., 1998, 17(1), 107-118.
189. Lala, P.K.; Orucevic, A. Role of nitric oxide in tumor progression: lessons from experimental tumors. Cancer Metastasis Rev., 1998, 17(1), 91-106.
190. Lancaster, J.R., Jr.; Xie, K. Tumors face NO problems? Cancer Res., 2006, 66(13), 6459-6462.
191. Thomsen, L.L.; Lawton, F.G.; Knowles, R.G.; Beesley, J.E.; Riveros-Moreno, V.; Moncada, S. Nitric oxide synthase activity in human gynecological cancer. Cancer Res., 1994, 54(5), 1352-1354.
192. Thomsen, L.L.; Miles, D.W.; Happerfield, L.; Bobrow, L.G.; Knowles, R.G.; Moncada, S. Nitric oxide synthase activity in human breast cancer. Br. J. Cancer, 1995, 72(1), 41-44.
193. Duenas-Gonzalez, A.; Isales, C.M.; del, M.A.-H.; Gonzalez-Sarmiento, R.; Sangueza, O.; Rodriguez-Commes, J. Expression of inducible nitric oxide synthase in breast cancer correlates with metastatic disease. Mod. Pathol., 1997, 10(7), 645-649.
194. Cobbs, C.S.; Brenman, J.E.; Aldape, K.D.; Bredt, D.S.; Israel, M.A. Expression of nitric oxide synthase in human central nervous system tumors. Cancer Res., 1995, 55(4), 727-730.
195. Liu, R.H.; Hotchkiss, J.H. Potential genotoxicity of chronically elevated nitric oxide: a review. Mutat. Res., 1995, 339(2), 73-89.
196. Kolb, J.P. Mechanisms involved in the proand anti-apoptotic role of NO in human leukemia. Leukemia, 2000, 14(9), 1685-1694.
197. Lejeune, P.; Lagadec, P.; Onier, N.; Pinard, D.; Ohshima, H.; Jeannin, J.F. Nitric oxide involvement in tumor-induced immunosuppression. J. Immunol., 1994, 152(10), 5077-5083.
198. Xie, K.; Huang, S.; Dong, Z.; Juang, S.H.; Gutman, M.; Xie, Q.W.; Nathan, C.; Fidler, I.J. Transfection with the inducible nitric oxide synthase gene suppresses tumorigenicity and abrogates metastasis by K-1735 murine melanoma cells. J. Exp. Med., 1995, 181(4), 1333-1343.
199. Pipili-Synetos E.;Sakkoula E.; Haralabopoulos G.; Andriopoulou P.; Peristeris P.; Maragoudakis M.E. Evidence that nitric oxide is an endogenous antiangiogenic mediator. Br. J. Pharmacol., 1994, 111(3), 894-902.
200. Radomski, M.W.; Jenkins, D.C.; Holmes, L.; Moncada, S. Human colorectal adenocarcinoma cells: differential nitric oxide synthesis determines their ability to aggregate platelets. Cancer Res., 1991, 51(22), 6073-6078.
201. Cohen, R.A. The role of nitric oxide and other endothelium-derived vasoactive substances in vascular disease. Prog. Cardiovasc. Dis., 1995, 38(2), 105-128.
202. Magrinat, G.; Mason, S.N.; Shami, P.J.; Weinberg, J.B. Nitric oxide modulation of human leukemia cell differentiation and gene expression. Blood, 1992, 80(8), 1880-1884.
203. Albina, J.E.; Reichner, J.S. Role of nitric oxide in mediation of macrophage cytotoxicity and apoptosis. Cancer Metastasis Rev., 1998, 17(1), 39-53.
204. Hofseth, L.J.; Ying, L. Identifying and defusing weapons of mass inflammation in carcinogenesis. Biochim. Biophys. Acta, 2006, 1765(1), 74-84.
205. Bouvard, V.; Baan, R.; Straif, K.; Grosse, Y.; Secretan, B.; El, G.F.; brahim-Tallaa, L.; Guha, N.; Freeman, C.; Galichet, L.; Cogliano, V. A review of human carcinogens--Part B: biological agents. Lancet Oncol., 2009, 10(4), 321-322.
206. Hussain, S.P.; Hofseth, L.J.; Harris, C.C. Radical causes of cancer. Nat. Rev. Cancer, 2003, 3(4), 276-285.
207. Hussain, S.P.; Harris, C.C. p53 biological network: at the crossroads of the cellular-stress response pathway and molecular carcinogenesis. J. Nippon Med. Sch., 2006, 73(2), 54-64.
208. Orucevic, A.; Bechberger, J.; Green, A.M.; Shapiro, R.A.; Billiar, T.R.; Lala, P.K. Nitric-oxide production by murine mammary adenocarcinoma cells promotes tumor-cell invasiveness. Int. J. Cancer, 1999, 81(6), 889-896.
209. Jadeski, L.C.; Hum, K.O.; Chakraborty, C.; Lala, P.K. Nitric oxide promotes murine mammary tumour growth and metastasis by stimulating tumour cell migration, invasiveness and angiogenesis. Int. J. Cancer, 2000, 86(1), 30-39.
210. Jadeski, L.C.; Lala, P.K. Nitric oxide synthase inhibition by N(G)-nitro-L-arginine methyl ester inhibits tumor-induced angiogenesis in mammary tumors. Am. J. Pathol., 1999, 155(4), 1381-1390.
211. Chhatwal, V.J.; Ngoi, S.S.; Chan, S.T.; Chia, Y.W.; Moochhala, S.M. Aberrant expression of nitric oxide synthase in human polyps, neoplastic colonic mucosa and surrounding peritumoral normal mucosa. Carcinogenesis, 1994, 15(10), 2081-2085.
212. Lala, P.K. Significance of nitric oxide in carcinogenesis, tumor progression and cancer therapy. Cancer Metastasis Rev., 1998, 17(1), 1-6.
213. Juang, S.H.; Xie, K.; Xu, L.; Shi, Q.; Wang, Y.; Yoneda, J.; Fidler, I.J. Suppression of tumorigenicity and metastasis of human renal carcinoma cells by infection with retroviral vectors harboring the murine inducible nitric oxide synthase gene. Hum. Gene Ther., 1998, 9(6), 845-854.
214. 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.; Moncada, S. Roles of nitric oxide in tumor growth. Proc. Natl. Acad. Sci. USA, 1995, 92(10), 4392-4396.
215. Lee, P.C.; Salyapongse, A.N.; Bragdon, G.A.; Shears, L.L.; Watkins, S.C.; Edington, H.D.; Billiar, T.R. Impaired wound healing and angiogenesis in eNOS-deficient mice. Am. J. Physiol 1999, 277(4 Pt 2), H1600-H1608.
216. Veikkola, T.; Karkkainen, M.; Claesson-Welsh, L.; Alitalo, K. Regulation of angiogenesis via vascular endothelial growth factor receptors. Cancer Res., 2000, 60(2), 203-212.
217. Louis, D.N.; Pomeroy, S.L.; Cairncross, J.G. Focus on central nervous system neoplasia. Cancer Cell, 2002, 1(2), 125-128.
218. Davis, F.G.; Freels, S.; Grutsch, J.; Barlas, S.; Brem, S. Survival rates in patients with primary malignant brain tumors stratified by patient age and tumor histological type: an analysis based on Surveillance, Epidemiology, and End Results(SEER) data, 1973-1991. J. Neurosurg., 1998, 88(1), 1-10.
219. Rajkumar, S.V.; Buckner, J.C.; Schomberg, P.J.; Pitot, H.C.; Ingle, J.N.; Cascino, T.L. Phase I evaluation of preirradiation chemotherapy with carmustine and cisplatin and accelerated radiation therapy in patients with high-grade gliomas. Neurosurgery, 1999, 44(1), 67-73.
220. Kostourou, V.; Cartwright, J.E.; Johnstone, A.P.; Boult, J.K.; Cullis, E.R.; Whitley, G.; Robinson, S.P. The role of tumourderived iNOS in tumour progression and angiogenesis. Br. J. Cancer, 2011, 104(1), 83-90.
221. Esteban, F.J.; Horcajadas, A.; El-Rubaidi, O.; Luque-Barona, R.; Ibanez, G.; Garcia-Carriazo, A.; Segovia, M.; del Moral-Leal, M.L. Nitric oxide in malignant astrocytes. Rev. Neurol., 2005, 40(7), 437-440.
222. mberger-Murphy, V. Hypoxia helps glioma to fight therapy. Curr. Cancer Drug Targets, 2009, 9(3), 381-390.
223. Ban, H.S.; Uno, M.; Nakamura, H. Suppression of hypoxia-induced HIF-1alpha accumulation by VEGFR inhibitors: Different profiles of AAL993 versus SU5416 and KRN633. Cancer Lett., 2010, 296(1), 17-26.
224. Sogawa, K.; Numayama-Tsuruta, K.; Ema, M.; Abe, M.; Abe, H.; Fujii-Kuriyama, Y. Inhibition of hypoxia-inducible factor 1 activity by nitric oxide donors in hypoxia. Proc. Natl. Acad. Sci. USA, 1998, 95(13), 7368-7373.
225. Kimura, H.; Weisz, A.; Kurashima, Y.; Hashimoto, K.; Ogura, T.; D'Acquisto, F.; Addeo, R.; Makuuchi, M.; Esumi, H. 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, 2000, 95(1), 189-197.
226. Feinstein, D.L.; Galea, E.; Roberts, S.; Berquist, H.; Wang, H.; Reis, D.J. Induction of nitric oxide synthase in rat C6 glioma cells. J. Neurochem., 1994, 62(1), 315-321.
227. Fujisawa, H.; Ogura, T.; Hokari, A.; Weisz, A.; Yamashita, J.; Esumi, H. Inducible nitric oxide synthase in a human glioblastoma cell line. J. Neurochem., 1995, 64(1), 85-91.
228. Towner, R.A.; Smith, N.; Doblas, S.; Garteiser, P.; Watanabe, Y.; He, T.; Saunders, D.; Herlea, O.; Silasi-Mansat, R.; Lupu, F. In vivo detection of inducible nitric oxide synthase in rodent gliomas. Free Radic. Biol. Med., 2010, 48(5), 691-703.
229. Isakovic, A.; Harhaji, L.; Dacevic, M.; Trajkovic, V. Adenosine rescues glioma cells from cytokine-induced death by interfering with the signaling network involved in nitric oxide production. Eur. J. Pharmacol., 2008, 591(1-3), 106-113.
230. Pan, J.W.; Zhan, R.Y.; Tong, Y.; Zhou, Y.Q.; Zhang, M. Expression of endothelial nitric oxide synthase and vascular endothelial growth factor in association with neovascularization in human primary astrocytoma. J. Zhejiang Univ. Sci. B., 2005, 6(7), 693-698.
231. Tanriover, N.; Ulu, M.O.; Isler, C.; Durak, H.; Oz, B.; Uzan, M.; Akar, Z. Neuronal nitric oxide synthase expression in glial tumors: correlation with malignancy and tumor proliferation. Neurol. Res., 2008, 30(9), 940-944.
232. Cobbs, C.S.; Whisenhunt, T.R.; Wesemann, D.R.; Harkins, L.E.; Van Meir, E.G.; Samanta, M. Inactivation of wild-type p53 protein function by reactive oxygen and nitrogen species in malignant glioma cells. Cancer Res., 2003, 63(24), 8670-8673.
233. Contestabile, A. Regulation of transcription factors by nitric oxide in neurons and in neural-derived tumor cells. Prog. Neurobiol., 2008, 84(4), 317-328.
234. Brandes, A.A.; Fiorentino, M.V. The role of chemotherapy in recurrent malignant gliomas: an overview. Cancer Invest., 1996, 14(6), 551-559.
235. Miller, D.S.; Bauer, B.; Hartz, A.M. Modulation of P-glycoprotein at the blood-brain barrier: opportunities to improve central nervous system pharmacotherapy. Pharmacol. Rev., 2008, 60(2), 196-209.
236. Hau, P.; Fabel, K.; Baumgart, U.; Rummele, P.; Grauer, O.; Bock, A.; Dietmaier, C.; Dietmaier, W.; Dietrich, J.; Dudel, C.; Hubner, F.; Jauch, T.; Drechsel, E.; Kleiter, I.; Wismeth, C.; Zellner, A.; Brawanski, A.; Steinbrecher, A.; Marienhagen, J.; Bogdahn, U. Pegylated liposomal doxorubicin-efficacy in patients with recurrent high-grade glioma. Cancer, 2004, 100(6), 1199-1207.
237. Black, K.L.; Ningaraj, N.S. Modulation of brain tumor capillaries for enhanced drug delivery selectively to brain tumor. Cancer Control, 2004, 11(3), 165-173.
238. Moncada, S.; Higgs, A. The L-arginine-nitric oxide pathway. N. Engl. J. Med., 1993, 329(27), 2002-2012.
239. Janigro, D.; West, G.A.; Nguyen, T.S.; Winn, H.R. Regulation of blood-brain barrier endothelial cells by nitric oxide. Circ. Res., 1994, 75(3), 528-538.
240. Nakano, S.; Matsukado, K.; Black, K.L. Increased brain tumor microvessel permeability after intracarotid bradykinin infusion is mediated by nitric oxide. Cancer Res., 1996, 56(17), 4027-4031.
241. Cote, J.; Savard, M.; Bovenzi, V.; Dubuc, C.; Tremblay, L.; Tsanaclis, A.M.; Fortin, D.; Lepage, M.; Gobeil, F., Jr. Selective tumor blood-brain barrier opening with the kinin B2 receptor agonist [Phe(8)psi(CH(2)NH)Arg(9)] -BK in a F98 glioma rat model: an MRI study. Neuropeptides, 2010, 44(2), 177-185.
242. Weyerbrock, A.; Walbridge, S.; Pluta, R.M.; Saavedra, J.E.; Keefer, L.K.; Oldfield, E.H. Selective opening of the blood-tumor barrier by a nitric oxide donor and long-term survival in rats with C6 gliomas. J. Neurosurg., 2003, 99(4), 728-737.
243. Yin, D.; Wang, X.; Konda, B.M.; Ong, J.M.; Hu, J.; Sacapano, M.R.; Ko, M.K.; Espinoza, A.J.; Irvin, D.K.; Shu, Y.; Black, K.L. Increase in brain tumor permeability in glioma-bearing rats with nitric oxide donors. Clin. Cancer Res., 2008, 14(12), 4002-4009.
244. Ruiz-Hurtado, G.; Fernandez-Velasco, M.; Mourelle, M.; Delgado, C. LA419, a novel nitric oxide donor, prevents pathological cardiac remodeling in pressure-overloaded rats via endothelial nitric oxide synthase pathway regulation. Hypertension, 2007, 50(6), 1049-1056.
245. Pullen, N.A.; Fillmore, H.L. Induction of matrix metalloproteinase-1 and glioma cell motility by nitric oxide. J. NeuroOncol., 2010, 96(2), 201-209.
246. Lin, Y.M.; Jan, H.J.; Lee, C.C.; Tao, H.Y.; Shih, Y.L.; Wei, H.W.; Lee, H.M. Dexamethasone reduced invasiveness of human malignant glioblastoma cells through a MAPK phosphatase1(MKP-1) dependent mechanism. Eur. J. Pharmacol., 2008, 593(1-3), 1-9.
247. Djinovic, V.; Momcilovic, M.; Grguric-Sipka, S.; Trajkovic, V.; Mostarica, S.M.; Miljkovic, D.; Sabo, T. Novel ruthenium complex K2[Ru(dmgly)Cl4]. 2H2O is toxic to C6 astrocytoma cell line, but not to primary rat astrocytes. J. Inorg. Biochem., 2004, 98(12), 2168-2173.
248. Perez-Ortiz, J.M.; Tranque, P.; Burgos, M.; Vaquero, C.F.; Llopis, J. Glitazones induce astroglioma cell death by releasing reactive oxygen species from mitochondria: modulation of cytotoxicity by nitric oxide. Mol. Pharmacol., 2007, 72(2), 407-417.
249. Yang, D.I.; Yin, J.H.; Ju, T.C.; Chen, L.S.; Hsu, C.Y. Nitric oxide and BCNU chemoresistance in C6 glioma cells: role of Snitrosoglutathione. Free Radic. Biol. Med., 2004, 36(10), 1317-1328.
250. Yang, D.I.; Chen, S.D.; Yin, J.H.; Hsu, C.Y. S-nitrosoglutathione and hypoxia-inducible factor-1 confer chemoresistance against carbamoylating cytotoxicity of BCNU in rat C6 glioma cells. Ann. NY Acad. Sci., 2005, 1042, 229-234.
251. Yin, J.H.; Yang, D.I.; Chou, H.; Thompson, E.M.; Xu, J.; Hsu, C.Y. Inducible nitric oxide synthase neutralizes carbamoylating potential of 1,3-bis(2-chloroethyl)-1-nitrosourea in c6 glioma cells. J. Pharmacol. Exp. Ther., 2001, 297(1), 308-315.