Cited by 49Neurogenesis and neuroplasticity mechanismsRedox biology and oxidative stressNitric Oxide and Endothelin Effects

Nox4-Generated Superoxide Drives Angiotensin II-Induced Neural Stem Cell Proliferation

Open access
Topchiy, Elena, Panzhinskiy, Evgeniy, Griffin, W. Sue T., Barger, Steven W., Das, Mita, Zawada, W. Michael·2013·Developmental Neuroscience

Abstract

Reactive oxygen species (ROS) have been reported to affect neural stem cell self-renewal and therefore may be important for normal development and may influence neurodegenerative processes when ROS activity is elevated. To determine if increasing production of superoxide, via activation of NADPH oxidase (Nox), increases neural stem cell proliferation, 100 nM angiotensin II (Ang II) - a strong stimulator of Nox - was applied to cultures of a murine neural stem cell line, C17.2. Twelve hours following a single treatment with Ang II, there was a doubling of the number of neural stem cells. This increase in neural stem cell numbers was preceded by a gradual elevation of superoxide levels (detected by dihydroethidium fluorescence) from the steady state at 0, 5, and 30 min and gradually increasing from 1 h to the maximum at 12 h, and returning to baseline at 24 h. Ang II-dependent proliferation was blocked by the antioxidant N-acetyl-L-cysteine. Confocal microscopy revealed the presence of two sources of intracellular ROS in C17.2 cells: (i) mitochondrial and (ii) extramitochondrial; the latter indicative of the involvement of one or more specific isoforms of Nox. Of the Nox family, mRNA expression for one member, Nox4, is abundant in neural stem cell cultures, and Ang II treatment resulted in elevation of the relative levels of Nox4 protein. SiRNA targeting of Nox4 mRNA reduced both the constitutive and Ang II-induced Nox4 protein levels and attenuated Ang II-driven increases in superoxide levels and stem cell proliferation. Our findings are consistent with our hypothesis that Ang II-induced proliferation of neural stem cells occurs via Nox4-generated superoxide, suggesting that an Ang II/Nox4 axis is an important regulator of neural stem cell self-renewal and as such may fine-tune normal, stress- or disease-modifying neurogenesis.

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

A few free checks a day · papers already verified open instantly · results are public

Integrity signals

Registry

Crossref · 10.1159/000350502

Cites

6 of 6 references verified0 citation errors · 0 not checkable

Statistics

Claims the paper makes

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

A few free checks a day · papers already verified open instantly · results are public

Claims other papers make about this one

Each is checked against this paper’s own text: does it say what the citing paper says it does?

  • NOX4 is a major source of superoxide production in human brain and promotes neural stem cell growth.

    “As a member of the NOX family genes that encode subunits of NADPH oxidase, NOX4 is a major source of superoxide production in human brain and a promoter of neural stem cell growth (Kuroda et al., 2014; Topchiy et al., 2013).”

Self-check

Percentages, sums and reported differences re-computed from the paper’s own numbers.

The self-check needs the paper’s full text.

Cites

Flagged first, then by citations

Research works printed but not linked: 64

  1. [1]Bergstrom T, Forsberg-Nilsson K. Neural stem cells: Brain building blocks and beyond. Ups J Med Sci. 2012;117:132–142. doi: 10.3109/03009734.2012.665096. [DOI] [PMC free article] [PubMed] [Google Scholar] · DOI
  2. [2]Ming GL, Song H. Adult neurogenesis in the mammalian brain: significant answers and significant questions. Neuron. 2011;70:687–702. doi: 10.1016/j.neuron.2011.05.001. [DOI] [PMC free article] [PubMed] [Google Scholar] · DOI · Paper page
  3. [3]Kempermann G. New neurons for ‘survival of the fittest’. Nat Rev Neurosci. 2012;13:727–736. doi: 10.1038/nrn3319. [DOI] [PubMed] [Google Scholar] · DOI
  4. [4]Mohamed A I, Mitra A, Basu A. Epigenetic regulation of self-renewal and fate determination in neural stem cells. J Neurosci Res. 2012;90:529–539. doi: 10.1002/jnr.22804. [DOI] [PubMed] [Google Scholar] · DOI
  5. [5]Drago J, Murphy M, Carroll SM, Harvey RP, Bartlett PF. Fibroblast growth factor-mediated proliferation of central nervous system precursors depends on endogenous production of insulin-like growth factor I. Proc Natl Acad Sci U S A. 1991;88:2199–2203. doi: 10.1073/pnas.88.6.2199. [DOI] [PMC free article] [PubMed] [Google Scholar] · DOI
  6. [6]Reynolds BA, Tetzlaff W, Weiss S. A multipotent EGF-responsive striatal embryonic progenitor cell produces neurons and astrocytes. J Neurosci. 1992;12:4565–4574. doi: 10.1523/JNEUROSCI.12-11-04565.1992. [DOI] [PMC free article] [PubMed] [Google Scholar] · DOI
  7. [7]Aguirre A, Rubio ME, Gallo V. Notch and EGFR pathway interaction regulates neural stem cell number and self-renewal. Nature. 2010;467:323–327. doi: 10.1038/nature09347. [DOI] [PMC free article] [PubMed] [Google Scholar] · DOI
  8. [8]Rodriguez-Pallares J, Quiroz CR, Parga JA, Guerra MJ, Labandeira-Garcia JL. Angiotensin II increases differentiation of dopaminergic neurons from mesencephalic precursors via angiotensin type 2 receptors. Eur J Neurosci. 2004;20:1489–1498. doi: 10.1111/j.1460-9568.2004.03621.x. [DOI] [PubMed] [Google Scholar] · DOI
  9. [9]Sodhi CP, Kanwar YS, Sahai A. Hypoxia and high glucose upregulate AT1 receptor expression and potentiate ANG II-induced proliferation in VSM cells. Am J Physiol Heart Circ Physiol. 2003;284:H846–H852. doi: 10.1152/ajpheart.00625.2002. [DOI] [PubMed] [Google Scholar] · DOI
  10. [10]Yoneyama M, Kawada K, Gotoh Y, Shiba T, Ogita K. Endogenous reactive oxygen species are essential for proliferation of neural stem/progenitor cells. Neurochem Int. 2010;56:740–746. doi: 10.1016/j.neuint.2009.11.018. [DOI] [PubMed] [Google Scholar] · DOI
  11. [11]Katsuyama M. NOX/NADPH oxidase, the superoxide-generating enzyme: its transcriptional regulation and physiological roles. J Pharmacol Sci. 2010;114:134–146. doi: 10.1254/jphs.10r01cr. [DOI] [PubMed] [Google Scholar] · DOI
  12. [12]Pachucki J, Wang D, Christophe D, Miot F. Structural and functional characterization of the two human ThOX/Duox genes and their 5'-flanking regions. Mol Cell Endocrinol. 2004;214:53–62. doi: 10.1016/j.mce.2003.11.026. [DOI] [PubMed] [Google Scholar] · DOI
  13. [13]Kawahara T, Quinn MT, Lambeth JD. Molecular evolution of the reactive oxygen-generating NADPH oxidase (Nox/Duox) family of enzymes. BMC Evol Biol. 2007;7:109. doi: 10.1186/1471-2148-7-109. [DOI] [PMC free article] [PubMed] [Google Scholar] · DOI
  14. [14]Geiszt M, Kopp JB, Varnai P, Leto TL. Identification of renox, an NAD(P)H oxidase in kidney. Proc Natl Acad Sci U S A. 2000;97:8010–8014. doi: 10.1073/pnas.130135897. [DOI] [PMC free article] [PubMed] [Google Scholar] · DOI
  15. [15]Cross AR, Segal AW. The NADPH oxidase of professional phagocytes--prototype of the NOX electron transport chain systems. Biochim Biophys Acta. 2004;1657:1–22. doi: 10.1016/j.bbabio.2004.03.008. [DOI] [PMC free article] [PubMed] [Google Scholar] · DOI · Paper page
  16. [17]Zawada WM, Banninger GP, Thornton J, Marriott B, Cantu D, Rachubinski AL, Das M, Griffin WS, Jones SM. Generation of reactive oxygen species in 1-methyl-4-phenylpyridinium (MPP+) treated dopaminergic neurons occurs as an NADPH oxidase-dependent two-wave cascade. J Neuroinflammation. 2011;8:129. doi: 10.1186/1742-2094-8-129. [DOI] [PMC free article] [PubMed] [Google Scholar] · DOI
  17. [18]Ryder EF, Snyder EY, Cepko CL. Establishment and characterization of multipotent neural cell lines using retrovirus vector-mediated oncogene transfer. J Neurobiol. 1990;21:356–375. doi: 10.1002/neu.480210209. [DOI] [PubMed] [Google Scholar] · DOI
  18. [19]Rothe G, Valet G. Flow cytometric analysis of respiratory burst activity in phagocytes with hydroethidine and 2',7'-dichlorofluorescin. J Leukoc Biol. 1990;47:440–448. [PubMed] [Google Scholar]
  19. [20]Chabrashvili T, Kitiyakara C, Blau J, Karber A, Aslam S, Welch WJ, Wilcox CS. Effects of ANG II type 1 and 2 receptors on oxidative stress, renal NADPH oxidase, and SOD expression. Am J Physiol Regul Integr Comp Physiol. 2003;285:R117–R124. doi: 10.1152/ajpregu.00476.2002. [DOI] [PubMed] [Google Scholar] · DOI
  20. [21]Rao GN, Berk BC. Active oxygen species stimulate vascular smooth muscle cell growth and proto-oncogene expression. Circ Res. 1992;70:593–599. doi: 10.1161/01.res.70.3.593. [DOI] [PubMed] [Google Scholar] · DOI
  21. [22]Ushio-Fukai M, Zafari AM, Fukui T, Ishizaka N, Griendling KK. p22phox is a critical component of the superoxide-generating NADH/NADPH oxidase system and regulates angiotensin II-induced hypertrophy in vascular smooth muscle cells. J Biol Chem. 1996;271:23317–23321. doi: 10.1074/jbc.271.38.23317. [DOI] [PubMed] [Google Scholar] · DOI
  22. [23]Lee CF, Qiao M, Schroder K, Zhao Q, Asmis R. Nox4 is a novel inducible source of reactive oxygen species in monocytes and macrophages and mediates oxidized low density lipoprotein-induced macrophage death. Circ Res. 2010;106:1489–1497. doi: 10.1161/CIRCRESAHA.109.215392. [DOI] [PMC free article] [PubMed] [Google Scholar] · DOI
  23. [24]Ambasta RK, Kumar P, Griendling KK, Schmidt HH, Busse R, Brandes RP. Direct interaction of the novel Nox proteins with p22phox is required for the formation of a functionally active NADPH oxidase. J Biol Chem. 2004;279:45935–45941. doi: 10.1074/jbc.M406486200. [DOI] [PubMed] [Google Scholar] · DOI · Paper page
  24. [26]Graham KA, Kulawiec M, Owens KM, Li X, Desouki MM, Chandra D, Singh KK. NADPH oxidase 4 is an oncoprotein localized to mitochondria. Cancer Biol Ther. 2010;10:223–231. doi: 10.4161/cbt.10.3.12207. [DOI] [PMC free article] [PubMed] [Google Scholar] · DOI
  25. [27]Lassegue B, Sorescu D, Szocs K, Yin Q, Akers M, Zhang Y, Grant SL, Lambeth JD, Griendling KK. Novel gp91(phox) homologues in vascular smooth muscle cells : nox1 mediates angiotensin II-induced superoxide formation and redox-sensitive signaling pathways. Circ Res. 2001;88:888–894. doi: 10.1161/hh0901.090299. [DOI] [PubMed] [Google Scholar] · DOI · Paper page
  26. [28]Suh YA, Arnold RS, Lassegue B, Shi J, Xu X, Sorescu D, Chung AB, Griendling KK, Lambeth JD. Cell transformation by the superoxide-generating oxidase Mox1. Nature. 1999;401:79–82. doi: 10.1038/43459. [DOI] [PubMed] [Google Scholar] · DOI · Paper page
  27. [29]Limoli CL, Rola R, Giedzinski E, Mantha S, Huang TT, Fike JR. Cell-density-dependent regulation of neural precursor cell function. Proc Natl Acad Sci U S A. 2004;101:16052–16057. doi: 10.1073/pnas.0407065101. [DOI] [PMC free article] [PubMed] [Google Scholar] · DOI
  28. [30]Le Belle JE, Orozco NM, Paucar AA, Saxe JP, Mottahedeh J, Pyle AD, Wu H, Kornblum HI. Proliferative neural stem cells have high endogenous ROS levels that regulate self-renewal and neurogenesis in a PI3K/Akt-dependant manner. Cell Stem Cell. 2011;8:59–71. doi: 10.1016/j.stem.2010.11.028. [DOI] [PMC free article] [PubMed] [Google Scholar] · DOI · Paper page
  29. [31]Sturrock A, Huecksteadt TP, Norman K, Sanders K, Murphy TM, Chitano P, Wilson K, Hoidal JR, Kennedy TP. Nox4 mediates TGF-beta1-induced retinoblastoma protein phosphorylation, proliferation, and hypertrophy in human airway smooth muscle cells. Am J Physiol Lung Cell Mol Physiol. 2007;292:L1543–L1555. doi: 10.1152/ajplung.00430.2006. [DOI] [PubMed] [Google Scholar] · DOI
  30. [33]Madhavan L, Ourednik V, Ourednik J. Increased “vigilance” of antioxidant mechanisms in neural stem cells potentiates their capability to resist oxidative stress. Stem Cells. 2006;24:2110–2119. doi: 10.1634/stemcells.2006-0018. [DOI] [PubMed] [Google Scholar] · DOI
  31. [34]Valente AJ, Yoshida T, Murthy SN, Sakamuri SS, Katsuyama M, Clark RA, Delafontaine P, Chandrasekar B. Angiotensin II enhances AT1-Nox1 binding and stimulates arterial smooth muscle cell migration and proliferation through AT1, Nox1, and interleukin-18. Am J Physiol Heart Circ Physiol. 2012;303:H282–H296. doi: 10.1152/ajpheart.00231.2012. [DOI] [PMC free article] [PubMed] [Google Scholar] · DOI
  32. [35]Fang L, Chen MF, Xiao ZL, Yu GL, Chen XB, Xie XM. The effect of endothelial progenitor cells on angiotensin II-induced proliferation of cultured rat vascular smooth muscle cells. J Cardiovasc Pharmacol. 2011;58:617–625. doi: 10.1097/FJC.0b013e318230bb5f. [DOI] [PubMed] [Google Scholar] · DOI
  33. [36]Schroder K, Zhang M, Benkhoff S, Mieth A, Pliquett R, Kosowski J, Kruse C, Ludike P, Michaelis UR, Weissmann N, Dimmeler S, Shah AM, Brandes RP. Nox4 Is a Protective Reactive Oxygen Species Generating Vascular NADPH Oxidase. Circ Res. 2012;110:1217–1225. doi: 10.1161/CIRCRESAHA.112.267054. [DOI] [PubMed] [Google Scholar] · DOI · Paper page
  34. [37]Zhang M, Brewer AC, Schroder K, Santos CX, Grieve DJ, Wang M, Anilkumar N, Yu B, Dong X, Walker SJ, Brandes RP, Shah AM. NADPH oxidase-4 mediates protection against chronic load-induced stress in mouse hearts by enhancing angiogenesis. Proc Natl Acad Sci U S A. 2010;107:18121–18126. doi: 10.1073/pnas.1009700107. [DOI] [PMC free article] [PubMed] [Google Scholar] · DOI
  35. [38]Niethammer P, Grabher C, Look AT, Mitchison TJ. A tissue-scale gradient of hydrogen peroxide mediates rapid wound detection in zebrafish. Nature. 2009;459:996–999. doi: 10.1038/nature08119. [DOI] [PMC free article] [PubMed] [Google Scholar] · DOI · Paper page
  36. [39]Kim JH, Song SY, Park SG, Song SU, Xia Y, Sung JH. Primary involvement of NADPH oxidase 4 in hypoxia-induced generation of reactive oxygen species in adipose-derived stem cells. Stem Cells Dev. 2012;21:2212–2221. doi: 10.1089/scd.2011.0561. [DOI] [PMC free article] [PubMed] [Google Scholar] · DOI
  37. [40]Ishizuka T, Goshima H, Ozawa A, Watanabe Y. Effect of angiotensin II on proliferation and differentiation of mouse induced pluripotent stem cells into mesodermal progenitor cells. Biochem Biophys Res Commun. 2012;420:148–155. doi: 10.1016/j.bbrc.2012.02.132. [DOI] [PubMed] [Google Scholar] · DOI
  38. [41]Buggisch M, Ateghang B, Ruhe C, Strobel C, Lange S, Wartenberg M, Sauer H. Stimulation of ES-cell-derived cardiomyogenesis and neonatal cardiac cell proliferation by reactive oxygen species and NADPH oxidase. J Cell Sci. 2007;120:885–894. doi: 10.1242/jcs.03386. [DOI] [PubMed] [Google Scholar] · DOI
  39. [42]Wang N, Xie K, Huo S, Zhao J, Zhang S, Miao J. Suppressing phosphatidylcholine-specific phospholipase C and elevating ROS level, NADPH oxidase activity and Rb level induced neuronal differentiation in mesenchymal stem cells. J Cell Biochem. 2007;100:1548–1557. doi: 10.1002/jcb.21139. [DOI] [PubMed] [Google Scholar] · DOI
  40. [44]Xiao Q, Luo Z, Pepe AE, Margariti A, Zeng L, Xu Q. Embryonic stem cell differentiation into smooth muscle cells is mediated by Nox4-produced H2O2. Am J Physiol Cell Physiol. 2009;296:C711–C723. doi: 10.1152/ajpcell.00442.2008. [DOI] [PubMed] [Google Scholar] · DOI
  41. [45]Le CV, Maridonneau-Parini I. Complete and reversible inhibition of NADPH oxidase in human neutrophils by phenylarsine oxide at a step distal to membrane translocation of the enzyme subunits. J Biol Chem. 1995;270:2067–2073. doi: 10.1074/jbc.270.5.2067. [DOI] [PubMed] [Google Scholar] · DOI
  42. [46]Stefanska J, Pawliczak R. Apocynin: molecular aptitudes. Mediators Inflamm. 2008;2008:106507. doi: 10.1155/2008/106507. [DOI] [PMC free article] [PubMed] [Google Scholar] · DOI
  43. [47]Lull ME, Levesque S, Surace MJ, Block ML. Chronic apocynin treatment attenuates beta amyloid plaque size and microglial number in hAPP(751)(SL) mice. PLoS One. 2011;6:e20153. doi: 10.1371/journal.pone.0020153. [DOI] [PMC free article] [PubMed] [Google Scholar] · DOI
  44. [48]Krause KH. Tissue distribution and putative physiological function of NOX family NADPH oxidases. Jpn J Infect Dis. 2004;57:S28–S29. [PubMed] [Google Scholar]
  45. [49]Sorce S, Krause KH. NOX enzymes in the central nervous system: from signaling to disease. Antioxid Redox Signal. 2009;11:2481–2504. doi: 10.1089/ars.2009.2578. [DOI] [PubMed] [Google Scholar] · DOI
  46. [50]Katsuyama M, Matsuno K, Yabe-Nishimura C. Physiological roles of NOX/NADPH oxidase, the superoxide-generating enzyme. J Clin Biochem Nutr. 2012;50:9–22. doi: 10.3164/jcbn.11-06SR. [DOI] [PMC free article] [PubMed] [Google Scholar] · DOI
  47. [51]Mittal M, Roth M, Konig P, Hofmann S, Dony E, Goyal P, Selbitz AC, Schermuly RT, Ghofrani HA, Kwapiszewska G, Kummer W, Klepetko W, Hoda MA, Fink L, Hanze J, Seeger W, Grimminger F, Schmidt HH, Weissmann N. Hypoxia-dependent regulation of nonphagocytic NADPH oxidase subunit NOX4 in the pulmonary vasculature. Circ Res. 2007;101:258–267. doi: 10.1161/CIRCRESAHA.107.148015. [DOI] [PubMed] [Google Scholar] · DOI
  48. [52]Diebold I, Petry A, Hess J, Gorlach A. The NADPH oxidase subunit NOX4 is a new target gene of the hypoxia-inducible factor-1. Mol Biol Cell. 2010;21:2087–2096. doi: 10.1091/mbc.E09-12-1003. [DOI] [PMC free article] [PubMed] [Google Scholar] · DOI
  49. [54]Carmona-Cuenca I, Roncero C, Sancho P, Caja L, Fausto N, Fernandez M, Fabregat I. Upregulation of the NADPH oxidase NOX4 by TGF-beta in hepatocytes is required for its pro-apoptotic activity. J Hepatol. 2008;49:965–976. doi: 10.1016/j.jhep.2008.07.021. [DOI] [PubMed] [Google Scholar] · DOI
  50. [55]McKallip RJ, Jia W, Schlomer J, Warren JW, Nagarkatti PS, Nagarkatti M. Cannabidiol-induced apoptosis in human leukemia cells: A novel role of cannabidiol in the regulation of p22phox and Nox4 expression. Mol Pharmacol. 2006;70:897–908. doi: 10.1124/mol.106.023937. [DOI] [PubMed] [Google Scholar] · DOI
  51. [56]Lundqvist J, Andaloussi-Lilja JE, Svensson C, Dorfh HG, Forsby A. Optimisation of culture conditions for differentiation of C17.2 neural stem cells to be used for in vitro toxicity tests. Toxicol In Vitro. 2012 doi: 10.1016/j.tiv.2012.04.020. E-pub ahead of print. [DOI] [PubMed] [Google Scholar] · DOI
  52. [57]Kim SJ, Son TG, Kim K, Park HR, Mattson MP, Lee J. Interferon-gamma promotes differentiation of neural progenitor cells via the JNK pathway. Neurochem Res. 2007;32:1399–1406. doi: 10.1007/s11064-007-9323-z. [DOI] [PubMed] [Google Scholar] · DOI
  53. [58]Grammatopoulos TN, Jones SM, Ahmadi FA, Hoover BR, Snell LD, Skoch J, Jhaveri VV, Poczobutt AM, Weyhenmeyer JA, Zawada WM. Angiotensin type 1 receptor antagonist losartan, reduces MPTP-induced degeneration of dopaminergic neurons in substantia nigra. Mol Neurodegener. 2007;2:1. doi: 10.1186/1750-1326-2-1. [DOI] [PMC free article] [PubMed] [Google Scholar] · DOI
  54. [59]L'Episcopo F, Tirolo C, Testa N, Caniglia S, Morale MC, Deleidi M, Serapide MF, Pluchino S, Marchetti B. Plasticity of subventricular zone neuroprogenitors in MPTP (1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine) mouse model of Parkinson's disease involves cross talk between inflammatory and Wnt/beta-catenin signaling pathways: functional consequences for neuroprotection and repair. J Neurosci. 2012;32:2062–2085. doi: 10.1523/JNEUROSCI.5259-11.2012. [DOI] [PMC free article] [PubMed] [Google Scholar] · DOI
  55. [60]Monje ML, Toda H, Palmer TD. Inflammatory blockade restores adult hippocampal neurogenesis. Science. 2003;302:1760–1765. doi: 10.1126/science.1088417. [DOI] [PubMed] [Google Scholar] · DOI · Paper page
  56. [61]Jenrow KA, Brown SL, Liu J, Kolozsvary A, Lapanowski K, Kim JH. Ramipril mitigates radiation-induced impairment of neurogenesis in the rat dentate gyrus. Radiat Oncol. 2010;5:6. doi: 10.1186/1748-717X-5-6. [DOI] [PMC free article] [PubMed] [Google Scholar] · DOI
  57. [62]Paton JF, Raizada MK. Neurogenic hypertension. Exp Physiol. 2010;95:569–571. doi: 10.1113/expphysiol.2009.047282. [DOI] [PubMed] [Google Scholar] · DOI
  58. [63]Zubcevic J, Waki H, Raizada MK, Paton JF. Autonomic-immune-vascular interaction: an emerging concept for neurogenic hypertension. Hypertension. 2011;57:1026–1033. doi: 10.1161/HYPERTENSIONAHA.111.169748. [DOI] [PMC free article] [PubMed] [Google Scholar] · DOI
  59. [64]Jun JY, Zubcevic J, Qi Y, Afzal A, Carvajal JM, Thinschmidt JS, Grant MB, Mocco J, Raizada MK. Brain-Mediated Dysregulation of the Bone Marrow Activity in Angiotensin II-Induced Hypertension. Hypertension. 2012;60:1316–1323. doi: 10.1161/HYPERTENSIONAHA.112.199547. [DOI] [PMC free article] [PubMed] [Google Scholar] · DOI
  60. [65]Miners S, Ashby E, Baig S, Harrison R, Tayler H, Speedy E, Prince JA, Love S, Kehoe PG. Angiotensin-converting enzyme levels and activity in Alzheimer's disease: differences in brain and CSF ACE and association with ACE1 genotypes. Am J Transl Res. 2009;1:163–177. [PMC free article] [PubMed] [Google Scholar]
  61. [66]Konings CH, Kuiper MA, Bergmans PL, Grijpma AM, van Kamp GJ, Wolters EC. Increased angiotensin-converting enzyme activity in cerebrospinal fluid of treated patients with Parkinson's disease. Clin Chim Acta. 1994;231:101–106. doi: 10.1016/0009-8981(94)90259-3. [DOI] [PubMed] [Google Scholar] · DOI
  62. [67]Constantinescu CS, Goodman DB, Grossman RI, Mannon LJ, Cohen JA. Serum angiotensin-converting enzyme in multiple sclerosis. Arch Neurol. 1997;54:1012–1015. doi: 10.1001/archneur.1997.00550200068012. [DOI] [PubMed] [Google Scholar] · DOI
  63. [68]Anilkumar N, Weber R, Zhang M, Brewer A, Shah AM. Nox4 and nox2 NADPH oxidases mediate distinct cellular redox signaling responses to agonist stimulation. Arterioscler Thromb Vasc Biol. 2008;28:1347–1354. doi: 10.1161/ATVBAHA.108.164277. [DOI] [PubMed] [Google Scholar] · DOI
  64. [69]Chabrashvili T, Kitiyakara C, Blau J, Karber A, Aslam S, Welch WJ, Wilcox CS. Effects of ANG II type 1 and 2 receptors on oxidative stress, renal NADPH oxidase, and SOD expression. Am J Physiol Regul Integr Comp Physiol. 2003;285:R117–R124. doi: 10.1152/ajpregu.00476.2002. [DOI] [PubMed] [Google Scholar] · DOI

Cited by

Sorted by citations

Authors
Topchiy, E., Panzhinskiy, E., Griffin, W. S. T., Barger, S. W., Das, M., & Zawada, W. M.
Affiliations
  • Oregon Health & Science University (US)
  • Central Arkansas Veterans Healthcare System (US)
Venue
Developmental Neuroscience
Publisher
S. Karger AG
Published
2013
Volume
35
Issue
4
Pages
293-305
ISSN
  • 0378-5866 (ISSN-L)
  • 1421-9859
OpenAlex
W2004244982
Cited by
49
References
6
Citations by year
2025: 3 · 2024: 1 · 2023: 1 · 2022: 3 · 2021: 4 · 2020: 7 · 2019: 10 · 2018: 2 · 2017: 4 · 2016: 6 · 2015: 4 · 2014: 2 · 2013: 2
FWCI
1.73
Type
journal article
Language
en
Open access
Locations
  • Developmental Neuroscience (publishedVersion)
  • PubMed (publishedVersion)
  • Europe PMC (PubMed Central) (acceptedVersion)
  • PubMed Central (acceptedVersion)
Funders
  • University of Colorado Denver
  • National Institute on Alcohol Abuse and Alcoholism (U01AA016654)
  • National Institute on Aging (P01AG012411)
  • National Heart, Lung, and Blood Institute (R01HL064917)
  • National Institute on Drug Abuse (T32DA007262)
Topics
  • Life Sciences › Neuroscience › Developmental Neuroscience › Neurogenesis and neuroplasticity mechanisms
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Redox biology and oxidative stress
  • Health Sciences › Medicine › Physiology › Nitric Oxide and Endothelin Effects
Keywords
NOX4, NADPH oxidase, superoxide, angiotensin II, neural stem cell proliferation, reactive oxygen species, C17.2 cells, mitochondrial reactive oxygen species, N-acetylcysteine, neurogenesis, stem cell self-renewal
MeSH terms
NADPH Oxidase 4, Angiotensin II, Animals, Cell Count, Cells, Cultured, Data Interpretation, Statistical, Superoxides, Blotting, Western, Reactive Oxygen Species, Microscopy, Confocal, NADPH Oxidases, RNA Interference, Cell Proliferation, Mice, Neural Stem Cells, Real-Time Polymerase Chain Reaction

About these checks

Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.

Statistics and arithmetic are recomputed, not judged.

Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.

What counts as a claim ›How we measure confidence ›How we check this ›

Are you an author, or do you see a problem with this page? Request a review