Deletion of Nox4 enhances remyelination following cuprizone-induced demyelination by increasing phagocytic capacity of microglia and macrophages in mice.
Animals
Mice
Microglia
/ metabolism
Cuprizone
/ toxicity
Remyelination
Demyelinating Diseases
/ pathology
Myelin Sheath
/ metabolism
Macrophages
/ metabolism
Corpus Callosum
/ pathology
Myelin Proteins
/ metabolism
Mice, Inbred C57BL
Oligodendroglia
/ metabolism
Disease Models, Animal
NADPH Oxidase 4
/ metabolism
Nox4
cuprizone
macrophage
microglia
remyelination
Journal
Glia
ISSN: 1098-1136
Titre abrégé: Glia
Pays: United States
ID NLM: 8806785
Informations de publication
Date de publication:
Mar 2023
Mar 2023
Historique:
revised:
15
10
2022
received:
03
04
2022
accepted:
18
10
2022
pubmed:
3
11
2022
medline:
25
1
2023
entrez:
2
11
2022
Statut:
ppublish
Résumé
NOX4 is a major reactive oxygen species-producing enzyme that modulates cell stress responses. We here examined the effect of Nox4 deletion on demyelination-remyelination, the most common pathological change in the brain. We used a model of cuprizone (CPZ)-associated demyelination-remyelination in wild-type and Nox4-deficient (Nox4
Substances chimiques
Cuprizone
5N16U7E0AO
Myelin Proteins
0
Nox4 protein, mouse
EC 1.6.3.-
NADPH Oxidase 4
EC 1.6.3.-
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
541-559Subventions
Organisme : Grant-in-Aid for Research Activity Start-up
ID : 21K20693
Organisme : Grants-in-Aid for Scientific Research
ID : 20H03791
Organisme : Grants-in-Aid for Scientific Research
ID : 19K09511
Organisme : Grants-in-Aid for Scientific Research
ID : 19K09530
Organisme : Grants-in-Aid for Scientific Research
ID : 20K09373
Organisme : Mochida Memorial Foundation for Medical and Pharmaceutical Research
Organisme : SENSHIN Medical Research Foundation
Organisme : Smoking Research Foundation
Informations de copyright
© 2022 Wiley Periodicals LLC.
Références
Ago, T., Kuroda, J., Pain, J., Fu, C., Li, H., & Sadoshima, J. (2010). Upregulation of Nox4 by hypertrophic stimuli promotes apoptosis and mitochondrial dysfunction in cardiac myocytes. Circulation Research, 106(7), 1253-1264. https://doi.org/10.1161/CIRCRESAHA.109.213116
Ago, T., Matsushima, S., Kuroda, J., Zablocki, D., Kitazono, T., & Sadoshima, J. (2010). The NADPH oxidase Nox4 and aging in the heart. Aging (Albany NY), 2(12), 1012-1016. https://doi.org/10.18632/aging.100261
Baaklini, C. S., Rawji, K. S., Duncan, G. J., Ho, M. F. S., & Plemel, J. R. (2019). Central nervous system Remyelination: Roles of glia and innate immune cells. Frontiers in Molecular Neuroscience, 12, 225. https://doi.org/10.3389/fnmol.2019.00225
Bas, A., Forsberg, G., Hammarstrom, S., & Hammarstrom, M. L. (2004). Utility of the housekeeping genes 18 S rRNA, beta-Actin and glyceraldehyde-3-phosphate-dehydrogenase for normalization in real-time quantitative reverse transcriptase-polymerase chain reaction analysis of gene expression in human T lymphocytes. Scandinavian Journal of Immunology, 59(6), 566-573. https://doi.org/10.1111/j.0300-9475.2004.01440.x
Bedard, K., & Krause, K. H. (2007). The NOX family of ROS-generating NADPH oxidases: Physiology and pathophysiology. Physiological Reviews, 87(1), 245-313. https://doi.org/10.1152/physrev.00044.2005
Benardais, K., Kotsiari, A., Skuljec, J., Koutsoudaki, P. N., Gudi, V., Singh, V., Vulinovic, F., Skripuletz, T., & Stangel, M. (2013). Cuprizone [bis(cyclohexylidenehydrazide)] is selectively toxic for mature oligodendrocytes. Neurotoxicity Research, 24(2), 244-250. https://doi.org/10.1007/s12640-013-9380-9
Bennett, M. L., Bennett, F. C., Liddelow, S. A., Ajami, B., Zamanian, J. L., Fernhoff, N. B., Mulinyawe, S. B., Bohlen, C. J., Adil, A., Tucker, A., Weissman, I. L., Chang, E. F., Li, G., Grant, G. A., Hayden Gephart, M. G., & Barres, B. A. (2016). New tools for studying microglia in the mouse and human CNS. Proceedings of the National Academy of Sciences of the United States of America, 113(12), E1738-E1746. https://doi.org/10.1073/pnas.1525528113
Campana, L., Starkey Lewis, P. J., Pellicoro, A., Aucott, R. L., Man, J., O'Duibhir, E., Mok, S. E., Ferreira-Gonzalez, S., Livingstone, E., Greenhalgh, S. N., Hull, K. L., Kendall, T. J., Vernimmen, D., Henderson, N. C., Boulter, L., Gregory, C. D., Feng, Y., Anderton, S. M., Forbes, S. J., & Iredale, J. P. (2018). The STAT3-IL-10-IL-6 pathway is a novel regulator of macrophage Efferocytosis and phenotypic conversion in sterile liver injury. Journal of Immunology, 200(3), 1169-1187. https://doi.org/10.4049/jimmunol.1701247
Carlton, W. W. (1966). Response of mice to the chelating agents sodium diethyldithiocarbamate, alpha-benzoinoxime, and biscyclohexanone oxaldihydrazone. Toxicology and Applied Pharmacology, 8(3), 512-521. https://doi.org/10.1016/0041-008x(66)90062-7
Cereghetti, G. M., & Scorrano, L. (2011). Phagocytosis: Coupling of mitochondrial uncoupling and engulfment. Current Biology, 21(20), R852-R854. https://doi.org/10.1016/j.cub.2011.09.007
Chang, A., Tourtellotte, W. W., Rudick, R., & Trapp, B. D. (2002). Premyelinating oligodendrocytes in chronic lesions of multiple sclerosis. The New England Journal of Medicine, 346(3), 165-173. https://doi.org/10.1056/NEJMoa010994
Cignarella, F., Filipello, F., Bollman, B., Cantoni, C., Locca, A., Mikesell, R., Manis, M., Ibrahim, A., Deng, L., Benitez, B. A., Cruchaga, C., Licastro, D., Mihindukulasuriya, K., Harari, O., Buckland, M., Holtzman, D. M., Rosenthal, A., Schwabe, T., Tassi, I., & Piccio, L. (2020). TREM2 activation on microglia promotes myelin debris clearance and remyelination in a model of multiple sclerosis. Acta Neuropathologica, 140(4), 513-534. https://doi.org/10.1007/s00401-020-02193-z
Craige, S. M., Chen, K., Pei, Y., Li, C., Huang, X., Chen, C., Shibata, R., Sato, K., Walsh, K., & Keaney, J. F., Jr. (2011). NADPH oxidase 4 promotes endothelial angiogenesis through endothelial nitric oxide synthase activation. Circulation, 124(6), 731-740. https://doi.org/10.1161/CIRCULATIONAHA.111.030775
de la Fuente, A. G., Lange, S., Silva, M. E., Gonzalez, G. A., Tempfer, H., van Wijngaarden, P., Zhao, C., di Canio, L., Trost, A., Bieler, L., Zaunmair, P., Rotheneichner, P., O'Sullivan, A., Couillard-Despres, S., Errea, O., Mae, M. A., Andrae, J., He, L., Keller, A., … Rivera, F. J. (2017). Pericytes stimulate oligodendrocyte progenitor cell differentiation during CNS Remyelination. Cell Reports, 20(8), 1755-1764. https://doi.org/10.1016/j.celrep.2017.08.007
de Maeyer, R. P. H., & Chambers, E. S. (2021). The impact of ageing on monocytes and macrophages. Immunology Letters, 230, 1-10. https://doi.org/10.1016/j.imlet.2020.12.003
Dewar, D., Underhill, S. M., & Goldberg, M. P. (2003). Oligodendrocytes and ischemic brain injury. Journal of Cerebral Blood Flow and Metabolism, 23(3), 263-274. https://doi.org/10.1097/01.WCB.0000053472.41007.F9
Funfschilling, U., Supplie, L. M., Mahad, D., Boretius, S., Saab, A. S., Edgar, J., Brinkmann, B. G., Kassmann, C. M., Tzvetanova, I. D., Mobius, W., Diaz, F., Meijer, D., Suter, U., Hamprecht, B., Sereda, M. W., Moraes, C. T., Frahm, J., Goebbels, S., & Nave, K. A. (2012). Glycolytic oligodendrocytes maintain myelin and long-term axonal integrity. Nature, 485(7399), 517-521. https://doi.org/10.1038/nature11007
Galloway, D. A., Phillips, A. E. M., Owen, D. R. J., & Moore, C. S. (2019). Phagocytosis in the brain: Homeostasis and disease. Frontiers in Immunology, 10, 790. https://doi.org/10.3389/fimmu.2019.00790
Griffiths, I., Klugmann, M., Anderson, T., Yool, D., Thomson, C., Schwab, M. H., Schneider, A., Zimmermann, F., McCulloch, M., Nadon, N., & Nave, K. A. (1998). Axonal swellings and degeneration in mice lacking the major proteolipid of myelin. Science, 280(5369), 1610-1613. https://doi.org/10.1126/science.280.5369.1610
Hass, D. T., & Barnstable, C. J. (2021). Uncoupling proteins in the mitochondrial defense against oxidative stress. Progress in Retinal and Eye Research, 83, 100941. https://doi.org/10.1016/j.preteyeres.2021.100941
Hiremath, M. M., Saito, Y., Knapp, G. W., Ting, J. P. Y., Suzuki, K., & Matsushima, G. K. (1998). Microglial/macrophage accumulation during cuprizone-induced demyelination in C57BL/6 mice. Journal of Neuroimmunology, 92(1-2), 38-49. https://doi.org/10.1016/S0165-5728(98)00168-4
Jackman, K., Kahles, T., Lane, D., Garcia-Bonilla, L., Abe, T., Capone, C., Hochrainer, K., Voss, H., Zhou, P., Ding, A., Anrather, J., & Iadecola, C. (2013). Progranulin deficiency promotes post-ischemic blood-brain barrier disruption. The Journal of Neuroscience, 33(50), 19579-19589. https://doi.org/10.1523/JNEUROSCI.4318-13.2013
Karl, T., Pabst, R., & von Horsten, S. (2003). Behavioral phenotyping of mice in pharmacological and toxicological research. Experimental and Toxicologic Pathology, 55(1), 69-83. https://doi.org/10.1078/0940-2993-00301
Kipp, M., Clarner, T., Dang, J., Copray, S., & Beyer, C. (2009). The cuprizone animal model: New insights into an old story. Acta Neuropathologica, 118(6), 723-736. https://doi.org/10.1007/s00401-009-0591-3
Kleinschnitz, C., Grund, H., Wingler, K., Armitage, M. E., Jones, E., Mittal, M., Barit, D., Schwarz, T., Geis, C., Kraft, P., Barthel, K., Schuhmann, M. K., Herrmann, A. M., Meuth, S. G., Stoll, G., Meurer, S., Schrewe, A., Becker, L., Gailus-Durner, V., … Schmidt, H. H. (2010). Post-stroke inhibition of induced NADPH oxidase type 4 prevents oxidative stress and neurodegeneration. PLoS Biology, 8(9), e1000479. https://doi.org/10.1371/journal.pbio.1000479
Kotter, M. R., Zhao, C., van Rooijen, N., & Franklin, R. J. (2005). Macrophage-depletion induced impairment of experimental CNS remyelination is associated with a reduced oligodendrocyte progenitor cell response and altered growth factor expression. Neurobiology of Disease, 18(1), 166-175. https://doi.org/10.1016/j.nbd.2004.09.019
Kuroda, J., Ago, T., Matsushima, S., Zhai, P., Schneider, M. D., & Sadoshima, J. (2010). NADPH oxidase 4 (Nox4) is a major source of oxidative stress in the failing heart. Proceedings of the National Academy of Sciences of the United States of America, 107(35), 15565-15570. https://doi.org/10.1073/pnas.1002178107
Lappe-Siefke, C., Goebbels, S., Gravel, M., Nicksch, E., Lee, J., Braun, P. E., Griffiths, I. R., & Nave, K. A. (2003). Disruption of Cnp1 uncouples oligodendroglial functions in axonal support and myelination. Nature Genetics, 33(3), 366-374. https://doi.org/10.1038/ng1095
Lee, Y., Morrison, B. M., Li, Y., Lengacher, S., Farah, M. H., Hoffman, P. N., Liu, Y., Tsingalia, A., Jin, L., Zhang, P. W., Pellerin, L., Magistretti, P. J., & Rothstein, J. D. (2012). Oligodendroglia metabolically support axons and contribute to neurodegeneration. Nature, 487(7408), 443-448. https://doi.org/10.1038/nature11314
Levine, J. M., Reynolds, R., & Fawcett, J. W. (2001). The oligodendrocyte precursor cell in health and disease. Trends in Neurosciences, 24(1), 39-47.
Li, B., Bedard, K., Sorce, S., Hinz, B., Dubois-Dauphin, M., & Krause, K. H. (2009). NOX4 expression in human microglia leads to constitutive generation of reactive oxygen species and to constitutive IL-6 expression. Journal of Innate Immunity, 1(6), 570-581. https://doi.org/10.1159/000235563
Li, Y., Mouche, S., Sajic, T., Veyrat-Durebex, C., Supale, R., Pierroz, D., Ferrari, S., Negro, F., Hasler, U., Feraille, E., Moll, S., Meda, P., Deffert, C., Montet, X., Krause, K. H., & Szanto, I. (2012). Deficiency in the NADPH oxidase 4 predisposes towards diet-induced obesity. International Journal of Obesity, 36(12), 1503-1513. https://doi.org/10.1038/ijo.2011.279
Lian, H., Litvinchuk, A., Chiang, A. C., Aithmitti, N., Jankowsky, J. L., & Zheng, H. (2016). Astrocyte-microglia cross talk through complement activation modulates amyloid pathology in mouse models of Alzheimer's disease. The Journal of Neuroscience, 36(2), 577-589. https://doi.org/10.1523/JNEUROSCI.2117-15.2016
Liedtke, W., Edelmann, W., Bieri, P. L., Chiu, F. C., Cowan, N. J., Kucherlapati, R., & Raine, C. S. (1996). GFAP is necessary for the integrity of CNS white matter architecture and long-term maintenance of myelination. Neuron, 17(4), 607-615. https://doi.org/10.1016/s0896-6273(00)80194-4
Maki, T., Morancho, A., Martinez-San Segundo, P., Hayakawa, K., Takase, H., Liang, A. C., Gabriel-Salazar, M., Medina-Gutierrez, E., Washida, K., Montaner, J., Lok, J., Lo, E. H., Arai, K., & Rosell, A. (2018). Endothelial progenitor cell Secretome and Oligovascular repair in a mouse model of prolonged cerebral Hypoperfusion. Stroke, 49(4), 1003-1010. https://doi.org/10.1161/STROKEAHA.117.019346
Mason, J. L., Jones, J. J., Taniike, M., Morell, P., Suzuki, K., & Matsushima, G. K. (2000). Mature oligodendrocyte apoptosis precedes IGF-1 production and oligodendrocyte progenitor accumulation and differentiation during demyelination/remyelination. Journal of Neuroscience Research, 61(3), 251-262. https://doi.org/10.1002/1097-4547(20000801)61:3<251::AID-JNR3>3.0.CO;2-W
Matsushima, G. K., & Morell, P. (2001). The neurotoxicant, cuprizone, as a model to study demyelination and remyelination in the central nervous system. Brain Pathology, 11(1), 107-116.
Maturana, A., Krause, K. H., & Demaurex, N. (2002). NOX family NADPH oxidases: Do they have built-in proton channels? The Journal of General Physiology, 120(6), 781-786. https://doi.org/10.1085/jgp.20028713
McMahon, E. J., Suzuki, K., & Matsushima, G. K. (2002). Peripheral macrophage recruitment in cuprizone-induced CNS demyelination despite an intact blood-brain barrier. Journal of Neuroimmunology, 130(1-2), 32-45. https://doi.org/10.1016/s0165-5728(02)00205-9
Menichella, D. M., Goodenough, D. A., Sirkowski, E., Scherer, S. S., & Paul, D. L. (2003). Connexins are critical for normal myelination in the CNS. The Journal of Neuroscience, 23(13), 5963-5973.
Mi, S., Miller, R. H., Tang, W., Lee, X., Hu, B., Wu, W., Zhang, Y., Shields, C. B., Zhang, Y., Miklasz, S., Shea, D., Mason, J., Franklin, R. J., Ji, B., Shao, Z., Chedotal, A., Bernard, F., Roulois, A., Xu, J., … Pepinsky, B. (2009). Promotion of central nervous system remyelination by induced differentiation of oligodendrocyte precursor cells. Annals of Neurology, 65(3), 304-315. https://doi.org/10.1002/ana.21581
Miao, Y., Dong, Y., Huang, P., Zhao, X., Huang, Z., Yao, J., Li, H., & Xu, Q. (2017). Increasing UCP2 expression and decreasing NOX1/4 expression maintain chondrocyte phenotype by reducing reactive oxygen species production. Oncotarget, 8(38), 63750-63763. https://doi.org/10.18632/oncotarget.18908
Miron, V. E., Boyd, A., Zhao, J. W., Yuen, T. J., Ruckh, J. M., Shadrach, J. L., van Wijngaarden, P., Wagers, A. J., Williams, A., Franklin, R. J. M., & Ffrench-Constant, C. (2013). M2 microglia and macrophages drive oligodendrocyte differentiation during CNS remyelination. Nature Neuroscience, 16(9), 1211-1218. https://doi.org/10.1038/nn.3469
Nayernia, Z., Jaquet, V., & Krause, K. H. (2014). New insights on NOX enzymes in the central nervous system. Antioxidants & Redox Signaling, 20(17), 2815-2837. https://doi.org/10.1089/ars.2013.5703
Neumann, H., Kotter, M. R., & Franklin, R. J. (2009). Debris clearance by microglia: An essential link between degeneration and regeneration. Brain, 132(Pt 2), 288-295. https://doi.org/10.1093/brain/awn109
Nishimura, A., Ago, T., Kuroda, J., Arimura, K., Tachibana, M., Nakamura, K., Wakisaka, Y., Sadoshima, J., Iihara, K., & Kitazono, T. (2016). Detrimental role of pericyte Nox4 in the acute phase of brain ischemia. Journal of Cerebral Blood Flow and Metabolism, 36(6), 1143-1154. https://doi.org/10.1177/0271678X15606456
Ozerdem, U., Grako, K. A., Dahlin-Huppe, K., Monosov, E., & Stallcup, W. B. (2001). NG2 proteoglycan is expressed exclusively by mural cells during vascular morphogenesis. Developmental Dynamics, 222(2), 218-227. https://doi.org/10.1002/dvdy.1200
Pang, Y., Fan, L. W., Tien, L. T., Dai, X., Zheng, B., Cai, Z., Lin, R. C., & Bhatt, A. (2013). Differential roles of astrocyte and microglia in supporting oligodendrocyte development and myelination in vitro. Brain and Behavior: A Cognitive Neuroscience Perspective, 3(5), 503-514. https://doi.org/10.1002/brb3.152
Park, D., Han, C. Z., Elliott, M. R., Kinchen, J. M., Trampont, P. C., Das, S., Collins, S., Lysiak, J. J., Hoehn, K. L., & Ravichandran, K. S. (2011). Continued clearance of apoptotic cells critically depends on the phagocyte Ucp2 protein. Nature, 477(7363), 220-224. https://doi.org/10.1038/nature10340
Philips, T., & Rothstein, J. D. (2017). Oligodendroglia: Metabolic supporters of neurons. The Journal of Clinical Investigation, 127(9), 3271-3280. https://doi.org/10.1172/JCI90610
Praet, J., Guglielmetti, C., Berneman, Z., van der Linden, A., & Ponsaerts, P. (2014). Cellular and molecular neuropathology of the cuprizone mouse model: Clinical relevance for multiple sclerosis. Neuroscience and Biobehavioral Reviews, 47, 485-505. https://doi.org/10.1016/j.neubiorev.2014.10.004
Ransohoff, R. M. (2016). A polarizing question: Do M1 and M2 microglia exist? Nature Neuroscience, 19(8), 987-991. https://doi.org/10.1038/nn.4338
Safaiyan, S., Besson-Girard, S., Kaya, T., Cantuti-Castelvetri, L., Liu, L., Ji, H., Schifferer, M., Gouna, G., Usifo, F., Kannaiyan, N., Fitzner, D., Xiang, X., Rossner, M. J., Brendel, M., Gokce, O., & Simons, M. (2021). White matter aging drives microglial diversity. Neuron, 109(7), 1100-1117 e1110. https://doi.org/10.1016/j.neuron.2021.01.027
Serrander, L., Cartier, L., Bedard, K., Banfi, B., Lardy, B., Plastre, O., Sienkiewicz, A., Forro, L., Schlegel, W., & Krause, K. H. (2007). NOX4 activity is determined by mRNA levels and reveals a unique pattern of ROS generation. The Biochemical Journal, 406(1), 105-114. https://doi.org/10.1042/BJ20061903
Shanmugasundaram, K., Nayak, B. K., Friedrichs, W. E., Kaushik, D., Rodriguez, R., & Block, K. (2017). NOX4 functions as a mitochondrial energetic sensor coupling cancer metabolic reprogramming to drug resistance. Nature Communications, 8(1), 997. https://doi.org/10.1038/s41467-017-01106-1
Shi, H., Hu, X., Leak, R. K., Shi, Y., An, C., Suenaga, J., Chen, J., & Gao, Y. (2015). Demyelination as a rational therapeutic target for ischemic or traumatic brain injury. Experimental Neurology, 272, 17-25. https://doi.org/10.1016/j.expneurol.2015.03.017
Shibahara, T., Ago, T., Nakamura, K., Tachibana, M., Yoshikawa, Y., Komori, M., Yamanaka, K., Wakisaka, Y., & Kitazono, T. (2020). Pericyte-mediated tissue repair through PDGFRβ promotes Peri-infarct Astrogliosis, Oligodendrogenesis, and functional recovery after acute ischemic stroke. eNeuro, 7(2), ENEURO.0474-19.2020. https://doi.org/10.1523/ENEURO.0474-19.2020
Shibahara, T., Ago, T., Tachibana, M., Nakamura, K., Yamanaka, K., Kuroda, J., Wakisaka, Y., & Kitazono, T. (2020). Reciprocal interaction between Pericytes and macrophage in Poststroke tissue repair and functional recovery. Stroke, 51(10), 3095-3106. https://doi.org/10.1161/STROKEAHA.120.029827
Skripuletz, T., Hackstette, D., Bauer, K., Gudi, V., Pul, R., Voss, E., Berger, K., Kipp, M., Baumgartner, W., & Stangel, M. (2013). Astrocytes regulate myelin clearance through recruitment of microglia during cuprizone-induced demyelination. Brain, 136(Pt 1), 147-167. https://doi.org/10.1093/brain/aws262
Skripuletz, T., Miller, E., Moharregh-Khiabani, D., Blank, A., Pul, R., Gudi, V., Trebst, C., & Stangel, M. (2010). Beneficial effects of minocycline on cuprizone induced cortical demyelination. Neurochemical Research, 35(9), 1422-1433. https://doi.org/10.1007/s11064-010-0202-7
Smith, K. J., Kapoor, R., & Felts, P. A. (1999). Demyelination: The role of reactive oxygen and nitrogen species. Brain Pathology, 9(1), 69-92. https://doi.org/10.1111/j.1750-3639.1999.tb00212.x
Tachibana, M., Ago, T., Wakisaka, Y., Kuroda, J., Shijo, M., Yoshikawa, Y., Komori, M., Nishimura, A., Makihara, N., Nakamura, K., & Kitazono, T. (2017). Early reperfusion after brain ischemia has beneficial effects beyond rescuing neurons. Stroke, 48(8), 2222-2230. https://doi.org/10.1161/STROKEAHA.117.016689
Taylor, L. C., Gilmore, W., Ting, J. P., & Matsushima, G. K. (2010). Cuprizone induces similar demyelination in male and female C57BL/6 mice and results in disruption of the estrous cycle. Journal of Neuroscience Research, 88(2), 391-402. https://doi.org/10.1002/jnr.22215
Tong, X., Khandelwal, A. R., Wu, X., Xu, Z., Yu, W., Chen, C., Zhao, W., Yang, J., Qin, Z., Weisbrod, R. M., Seta, F., Ago, T., Lee, K. S., Hammock, B. D., Sadoshima, J., Cohen, R. A., & Zeng, C. (2016). Pro-atherogenic role of smooth muscle Nox4-based NADPH oxidase. Journal of Molecular and Cellular Cardiology, 92, 30-40. https://doi.org/10.1016/j.yjmcc.2016.01.020
Vankriekelsvenne, E., Chrzanowski, U., Manzhula, K., Greiner, T., Wree, A., Hawlitschka, A., Llovera, G., Zhan, J., Joost, S., Schmitz, C., Ponsaerts, P., Amor, S., Nutma, E., Kipp, M., & Kaddatz, H. (2022). Transmembrane protein 119 is neither a specific nor a reliable marker for microglia. Glia, 70(6), 1170-1190. https://doi.org/10.1002/glia.24164
Yoshikawa, Y., Ago, T., Kuroda, J., Wakisaka, Y., Tachibana, M., Komori, M., Shibahara, T., Nakashima, H., Nakashima, K., & Kitazono, T. (2019). Nox4 promotes neural stem/precursor cell proliferation and neurogenesis in the hippocampus and restores memory function following Trimethyltin-induced injury. Neuroscience, 398, 193-205. https://doi.org/10.1016/j.neuroscience.2018.11.046