Angiotensin-(1-7) prevents radiation-induced inflammation in rat primary astrocytes through regulation of MAP kinase signaling

Free Radical Biology and Medicine

Volumn 65, Issue , 2013, Pages 1060-1068

  Moore, Elizabeth D ^a   Kooshki, Mitra ^a   Metheny Barlow, Linda J ^a   Gallagher, Patricia E ^a   Robbins, Mike E ^a  

^a WAKE FOREST SCHOOL OF MEDICINE   (United States)

Author keywords

Angiotensin (1 7); Inflammation; MAP kinase signaling; Radiation induced; Rat primary astrocytes; Renin angiotensin system

Indexed keywords

1,4 DIAMINO 1,4 BIS(2 AMINOPHENYLTHIO) 2,3 DICYANOBUTADIENE; ANGIOTENSIN[1-7]; CYCLOOXYGENASE 2; GLIAL FIBRILLARY ACIDIC PROTEIN; HEPTAPEPTIDE; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERLEUKIN 1BETA; INTERLEUKIN 6; MITOGEN ACTIVATED PROTEIN KINASE; MITOGEN ACTIVATED PROTEIN KINASE PHOSPHATASE 1; VANADATE SODIUM; ANGIOTENSIN I; ANGIOTENSIN I (1-7); DUSP1 PROTEIN, RAT; PEPTIDE FRAGMENT; RADIOPROTECTIVE AGENT;

ANIMAL CELL; ARTICLE; ASTROCYTE; ASTROCYTE CULTURE; CELL ISOLATION; COGNITIVE DEFECT; CONTROLLED STUDY; CULTURE MEDIUM; ENZYME PHOSPHORYLATION; GENE EXPRESSION; IMMUNOBLOTTING; IMMUNOREACTIVITY; IRRADIATION; NERVE CELL LESION; NERVOUS SYSTEM INFLAMMATION; NONHUMAN; PRIMARY CULTURE; PRIORITY JOURNAL; RAT; REAL TIME POLYMERASE CHAIN REACTION; RENIN ANGIOTENSIN ALDOSTERONE SYSTEM; SIGNAL TRANSDUCTION; WESTERN BLOTTING; ANIMAL; CELL CULTURE; DRUG SCREENING; IMMUNOLOGY; INFLAMMATION; METABOLISM; PRIMARY CELL CULTURE; RADIATION RESPONSE;

RATTUS;

ANGIOTENSIN I; ANIMALS; ASTROCYTES; CELLS, CULTURED; DRUG EVALUATION, PRECLINICAL; DUAL SPECIFICITY PHOSPHATASE 1; INFLAMMATION; MAP KINASE SIGNALING SYSTEM; PEPTIDE FRAGMENTS; PRIMARY CELL CULTURE; RADIATION-PROTECTIVE AGENTS; RATS;

EID: 84884507376     PISSN: 08915849     EISSN: 18734596     Source Type: Journal    
DOI: 10.1016/j.freeradbiomed.2013.08.183     Document Type: Article

References (55)

1. R. Siegel, D. Naishadham, and A. Jemal Cancer Statistics, 2012 Cancer J. Clin 62 2012 10 29
2. A. Jemal Global cancer statistics Cancer J. Clin 61 2011 134
3. D. Greene-Schloesser, and M.E. Robbins Radiation-induced cognitive impairment-from bench to bedside Neuro-Oncology 14 2012 37 44
4. R.R. Patel, and M.P. Mehta Targeted therapy for brain metastases: improving the therapeutic ratio Clin. Cancer Res. 13 2007 1675 1683 (Pubitemid 46952932)
5. X.R. Lowe, S. Bhattacharya, F. Marchetti, and A.J. Wyrobek Early brain response to low-dose radiation exposure involves molecular networks and pathways associated with cognitive functions, advanced aging and Alzheimer's disease Radiat. Res 171 2009 53 65
6. C.L. Armstrong, J.V. Hunter, G.E. Ledakis, B. Cohen, E.M. Tallent, B.H. Goldstein, Z. Tochner, R. Lustig, K.D. Judy, A. Pruitt, J.E. Mollman, E.M. Stanczak, M.Y. Jo, T.L. Than, and P. Phillips Late cognitive and radiographic changes related to radiotherapy - initial prospective findings Neurology 59 2002 40 48 (Pubitemid 34742792)
7. E.G. Shaw, R. Rosdhal, R.B. D'Agostino, J. Lovato, M.J. Naughton, M.E. Robbins, and S.R. Rapp Phase II study of donepezil in irradiated brain tumor patients: effect on cognitive function, mood, and quality of life J. Clin. Oncol. 24 2006 1415 1420 (Pubitemid 46622007)
8. K. Jakubs, S. Bonde, R.E. Iosif, C.T. Ekdahl, Z. Kokaia, M. Kokaia, and O. Lindvall Inflammation regulates functional integration of neurons born in adult brain J. Neurosci. 28 2008 12477 12488
9. B. Biscaro, O. Lindvall, G. Tesco, C.T. Ekdahl, and R.M. Nitsch Inhibition of microglial activation protects hippocampal neurogenesis and improves cognitive deficits in a transgenic mouse model for Alzheimer's disease Neurodegener. Dis. 9 2012 187 198
10. C.T. Ekdahl, Z. Kokaia, and O. Lindvall Brain inflammation and adult neurogenesis: the dual role of microglia Neuroscience 158 2009 1021 1029
11. M. Kalm, A. Fukuda, H. Fukuda, A. Ohrfelt, B. Lannering, T. Bjork-Eriksson, K. Blennow, I. Marky, and K. Blomgren Transient inflammation in neurogenic regions after irradiation of the developing brain Radiat. Res. 171 2009 66 76
12. S. Kyrkanides, J.A. Olschowka, J.P. Williams, J.T. Hansen, and M.K. O'Banion TNF alpha and IL-1 beta mediate intercellular adhesion molecule-1 induction via microglia-astrocyte interaction in CNS radiation injury J. Neuroimmunol. 95 1999 95 106 (Pubitemid 29173026)
13. S. Kyrkanides, A.H. Moore, J.A. Olschowka, J.C. Daeschner, J.P. Williams, J.T. Hansen, and M.K. O'Banion Cyclooxygenase-2 modulates brain inflammation-related gene expression in central nervous system radiation injury Mol. Brain Res. 104 2002 159 169
14. M.A. Sama, D.M. Mathis, J.L. Furman, H.M. Abdul, I.A. Artiushin, S.D. Kraner, and C.M. Norris Interleukin-1 beta-dependent signaling between astrocytes and neurons depends critically on astrocytic calcineurin/NFAT activity J. Biol. Chem. 283 2008 21953 21964
15. L. Vallieres, I.L. Campbell, F.H. Gage, and P.E. Sawchenko Reduced hippocampal neurogenesis in adult transgenic mice with chronic astrocytic production of interleukin-6 J. Neurosci. 22 2002 486 492 (Pubitemid 34049087)
16. M. Koto, H. Cho, O. Riesterer, U. Giri, M.D. Story, C.S. Ha, and U. Raju Human lymphoma cells develop resistance to radiation in the presence of astrocytes in vitro Anticancer Res. 31 2011 33 38
17. S.Y. Hwang, J.S. Jung, T.H. Kim, S.J. Lim, E.S. Oh, J.Y. Kim, K.A. Ji, E.H. Joe, K.H. Cho, and I.O. Han Ionizing radiation induces astrocyte gliosis through microglia activation Neurobiol. Dis. 21 2006 457 467
18. Z.Y. Deng, G.C. Sui, P.M. Rosa, and W.L. Zhao Radiation-induced c-Jun activation depends on MEK1-ERK1/2 signaling pathway in microglial cells Plos One 7 2012
19. J.F. Kurland, D.W. Voehringer, and R.E. Meyn The MEK/ERK pathway acts upstream of NF kappa B1 (p50) homodimer activity and Bcl-2 expression in a murine B-cell lymphoma cell line - MEK inhibition restores radiation-induced apoptosis J. Biol. Chem 278 2003 32465 32470 (Pubitemid 37048445)
20. R.F. Regan, Y.Z. Wang, X. Ma, A. Chong, and Y.P. Guo Activation of extracellular signal-regulated kinases potentiates hemin toxicity in astrocyte cultures J. Neurochem. 79 2001 545 555 (Pubitemid 33029928)
21. T.C. Lee, D. Greene-Schloesser, V. Payne, D.I. Diz, F.C. Hsu, M. Kooshki, R. Mustafa, D.R. Riddle, W.L. Zhao, M.D. Chan, and M.E. Robbins Chronic administration of the angiotensin-converting enzyme inhibitor, ramipril, prevents fractionated whole-brain irradiation-induced perirhinal cortex-dependent cognitive impairment Radiat. Res. 178 2012 46 56
22. M.E. Robbins, W. Zhao, M.A. Garcia-Espinosa, and D.I. Diz Renin-angiotensin system blockers and modulation of radiation-induced brain injury Curr. Drug Targets 11 2010 1413 1422
23. M.E. Robbins, and D.I. Diz Pathogenic role of the renin-angiotensin system in modulating radiation-induced late effects Int. J. Radiat. Oncol. Biol. Phys. 64 2006 6 12 (Pubitemid 41831202)
24. W.L. Zhao, and M.E.C. Robbins Inflammation and chronic oxidative stress in radiation-induced late normal tissue injury: therapeutic implications Curr. Med. Chem. 16 2009 130 143
25. K.R. Conner, V.S. Payne, M.E. Forbes, M.E. Robbins, and D.R. Riddle Effects of the AT(1) receptor antagonist L-158,809 on microglia and neurogenesis after fractionated whole-brain irradiation Radiat. Res. 173 2010 49 61
26. M.E. Robbins, V. Payne, E. Tommasi, D.I. Diz, F.C. Hsu, W.R. Brown, K.T. Wheeler, J. Olson, and W.L. Zhao The AT(1) receptor antagonist, L-158,809, prevents or ameliorates fractionated whole-brain irradiation-induced cognitive impairment Int. J. Radiat. Oncol. Biol. Phys. 73 2009 499 505
27. E.S.A. Simoes, K. Silveira, A. Ferreira, and M. Teixeira ACE2, angiotensin-(1-7) and Mas receptor axis in inflammation and fibrosis Br. J. Pharmacol. 169 2013 477 492
28. T. Jiang, L. Gao, J. Guo, J. Lu, Y. Wang, and Y. Zhang Suppressing inflammation by inhibiting the NF-kappaB pathway contributes to the neuroprotective effect of angiotensin-(1-7) in rats with permanent cerebral ischaemia Br. J. Pharmacol 167 2012 1520 1532
29. L.L. Souza, and C.M. Costa-Neto Angiotensin-(1-7) decreases LPS-induced inflammatory response in macrophages J. Cell. Physiol. 227 2012 2117 2122
30. L.J. Wang, X.S. Hu, W.W. Zhang, and F. Tian Angiotensin (1-7) ameliorates angiotensin II-induced inflammation by inhibiting LOX-1 expression Inflamm. Res. 62 2013 219 228
31. K.D. da Silveira, F.M. Coelho, A.T. Vieira, D. Sachs, L.C. Barroso, V.V. Costa, T.L.B. Bretas, M. Bader, L.P. de Sousa, T.A. da Silva, R.A.S. dos Santos, A. Silva, and M.M. Teixeira Anti-inflammatory effects of the activation of the angiotensin-(1-7) receptor, mas, in experimental models of arthritis J. Immunol. 185 2010 5569 5576
32. J. Menon, D.R. Soto-Pantoja, M.F. Callahan, J.M. Cline, C.M. Ferrario, E.A. Tallant, and P.E. Gallagher Angiotensin-(1-7) inhibits growth of human lung adenocarcinoma xenografts in nude mice through a reduction in cyclooxygenase-2 Cancer Res. 67 2007 2809 2815 (Pubitemid 46548970)
33. L.T. McCollum, P.E. Gallagher, and E.A. Tallant Angiotensin-(1-7) abrogates mitogen-stimulated proliferation of cardiac fibroblasts Peptides 34 2012 380 388
34. K.L. Cook, L.J. Metheny-Barlow, E.A. Tallant, and P.E. Gallagher Angiotensin-(1-7) reduces fibrosis in orthotopic breast tumors Cancer Res. 70 2010 8319 8328
35. P.E. Gallagher, C.M. Ferrario, and E.A. Tallant MAP kinase/phosphatase pathway mediates the regulation of ACE2 by angiotensin peptides Am. J. Physiol.-Cell Physiol 295 2008 C1169 C1174
36. P.E. Gallagher, and E.A. Tallant Angiotensin-(1-7) reduces MAP kinase activity by upregulation of the dual-specificity phosphatase DUSP1 Hypertension 54 2009 (E35-E35)
37. L.T. McCollum, P.E. Gallagher, and E.A. Tallant Angiotensin-(1-7) attenuates angiotensin II-induced cardiac remodeling associated with upregulation of dual-specificity phosphatase 1 Am. J. Physiol.-Heart Circ. Physiol 302 2012 H801 H810
38. E.A. Tallant, and J.T. Higson Angiotensin II activates distinct signal transduction pathways in astrocytes isolated from neonatal rat brain Glia 19 1997 333 342 (Pubitemid 27165240)
39. S. Ramanan, M. Kooshki, W.L. Zhao, F.C. Hsu, and M.E. Robbins PPAR alpha ligands inhibit radiation-induced microglial inflammatory responses by negatively regulating NF-kappa B and AP-1 pathways Free Radic. Biol. Med. 45 2008 1695 1704
40. C.I. Schnegg, M. Kooshki, F.C. Hsu, G.C. Sui, and M.E. Robbins PPAR delta prevents radiation-induced proinflammatory responses in microglia via transrepression of NF-kappa B and inhibition of the PK alpha/MEK1/2/ERK1/2/AP-1 pathway Free Radic. Biol. Med 52 2012 1734 1743
41. A. Larionov, A. Krause, and W. Miller A standard curve based method for relative real time PCR data processing BMC Bioinformatics 6 2005
42. E.A. Tallant, L.T. McCollum, and P.E. Gallagher Angiotensin-(1-7) reduces Ang II-induced cardiac hypertrophy with an associated increase in the dual-specificity phosphatase 1 (DUSP1) Hypertension 54 2009 (E122-E122)
43. A.V. Molofsky, R. Krenick, E. Ullian, H.H. Tsai, B. Deneen, W.D. Richardson, B.A. Barres, and D.H. Rowitch Astrocytes and disease: a neurodevelopmental perspective Genes Dev. 26 2012 891 907
44. H.H. Tsai, H.L. Li, L.C. Fuentealba, A.V. Molofsky, R. Taveira-Marques, H.L. Zhuang, A. Tenney, A.T. Murnen, S.P.J. Fancy, F. Merkle, N. Kessaris, A. Alvarez-Buylla, W.D. Richardson, and D.H. Rowitch Regional astrocyte allocation regulates CNS synaptogenesis and repair Science 337 2012 358 362
45. E.A. Tallant, C.M. Ferrario, and P.E. Gallagher Angiotensin-(1-7) inhibits growth of cardiac myocytes through activation of the mas receptor Am. J. Physiol.-Heart Circ. Physiol 289 2005 H1560 H1566
46. M.L. Monje, H. Toda, and T.D. Palmer Inflammatory blockade restores adult hippocampal neurogenesis Science 302 2003 1760 1765 (Pubitemid 37505739)
47. M.C. Chappell, K.B. Brosnihan, D.I. Diz, and C.M. Ferrario Identification of angiotensin-(1-7) in rat-brain - evidence for differential processing of angiotensin peptides J. Biol. Chem. 264 1989 16518 16523 (Pubitemid 19243542)
48. C.I. Schnegg, D. Greene-Schloesser, M. Kooshki, V.S. Payne, F.C. Hsu, and M.E. Robbins The PPARdelta agonist GW0742 inhibits neuroinflammation, but does not restore neurogenesis or prevent early delayed hippocampal-dependent cognitive impairment after whole-brain irradiation Free Radic. Biol. Med. 61C 2013 1 9
49. S. Ramanan, M. Kooshki, W.L. Zhao, F.C. Hsu, D.R. Riddle, and M.E. Robbins The PPAR alpha agonist fenofibrate preserves hippocampal neurogenesis and inhibits microglial activation after whole-brain irradiatioN Int. J. Radiat. Oncol. Biol. Phys. 75 2009 870 877
50. K.A. Jenrow, S.L. Brown, J.G. Liu, A. Kolozsvary, K. Lapanowski, and J.H. Kim Ramipril mitigates radiation-induced impairment of neurogenesis in the rat dentate gyrus Radiat. Oncol 5 2010
51. K.A. Jenrow, J.G. Liu, S.L. Brown, A. Kolozsvary, K. Lapanowski, and J.H. Kim Combined atorvastatin and ramipril mitigate radiation-induced impairment of dentate gyrus neurogenesis J. Neuro-Oncol. 101 2011 449 456
52. M.A. Lopez Verrilli, M. Rodriguez Fermepin, N. Longo Carbajosa, S. Landa, B.D. Cerrato, S. Garcia, B.E. Fernandez, and M.M. Gironacci Angiotensin-(1-7) through Mas receptor up-regulates neuronal norepinephrine transporter via Akt and Erk1/2-dependent pathways J. Neurochem. 120 2012 46 55
53. B. Krishnan, T.L. Smith, P. Dubey, M.E. Zapadka, F.M. Torti, M.C. Willingham, E.A. Tallant, and P.E. Gallagher Angiotensin-(1-7) attenuates metastatic prostate cancer and reduces osteoclastogenesis Prostate 73 2013 71 82
54. P.E. Gallagher, K. Cook, D. Soto-Pantoja, J. Menon, and E.A. Tallant Angiotensin peptides and lung cancer Curr. Cancer Drug Targets 11 2011 394 404
55. W.J. Petty, A.A. Miller, T.P. McCoy, P.E. Gallagher, E.A. Tallant, and F.M. Torti Phase I and pharmacokinetic study of angiotensin-(1-7), an endogenous antiangiogenic hormone Clin. Cancer Res. 15 2009 7398 7404