Acute hepatocyte growth factor treatment induces long-term neuroprotection and stroke recovery via mechanisms involving neural precursor cell proliferation and differentiation
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Hepatocyte growth factor (HGF) is an interesting candidate for acute stroke treatment as shown by continuous infusion or gene delivery protocols. However, little is known about HGF-mediated long-term effects. The present study therefore analyzed long-term effects of an acute intrastriatal HGF treatment (5 μg) after a 45-minute stroke, with regard to brain injury and neurologic recovery. Hepatocyte growth factor induced long-term neuroprotection as assessed by infarct volume and neuronal cell death analysis for as long as 4 weeks after stroke, which was associated with sustained neurologic recovery as evidenced by corner-turn and tight-rope tests. Analyzing underlying mechanisms of HGF-induced sustained neuroprotection, enhanced cell proliferation followed by increased neuronal differentiation of neural precursor cells (NPCs) was observed in the ischemic striatum of HGF-treated mice, which persisted for up to 4 weeks. In line with this, HGF promoted neurosphere formation as well as proliferation of NPC and decreased caspase-3-dependent hypoxic injury in vitro. Preservation of blood—brain barrier integrity 24 hours after stroke was furthermore noticed in animals receiving HGF, which was associated with the inhibition of matrix metalloproteases (MMP)-2 and MMP-9 at 4 and 24 hours, respectively. We suggest that sustained recruitment of proliferating cells together with improved neurovascular remodeling provides an explanation for HGF-induced long-term neuroprotection.
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The survival rate of adult neural precursor cells in brain parenchyma is poor, and only a small percentage differentiate into neurons.
“The survival rate of adult neural precursor cells in the brain parenchyma is poor and only a small percentage of the cells differentiate into neurons.35,39–42”
From Promoting brain remodelling and plasticity for stroke recovery: therapeutic promise and potential pitfalls of clinical translation (2012) · cites this paper as [42]
Cites
Mechanisms and Functional Implications of Adult Neurogenesis
Zhao, C., Deng, W., & Gage, F. H. (2008) · Cell · doi:10.1016/j.cell.2008.01.033 · Cited by 3,007 · see citing works
Neuronal replacement from endogenous precursors in the adult brain after stroke
Arvidsson, A., Collin, T., Kirik, D., Kokaia, Z., & Lindvall, O. (2002) · Nature Medicine · doi:10.1038/nm747 · Cited by 2,799 · see citing works
Molecular cloning and expression of human hepatocyte growth factor
Nakamura, T., Nishizawa, T., Hagiya, M., Seki, T., Shimonishi, M., Sugimura, A., Tashiro, K., & Shimizu, S. (1989) · Nature · doi:10.1038/342440a0 · Cited by 2,158 · see citing works
VEGF-induced neuroprotection, neurogenesis, and angiogenesis after focal cerebral ischemia
Sun, Y., Jin, K., Xie, L., Childs, J., Mao, X. O., Logvinova, A., & Greenberg, D. A. (2003) · Journal of Clinical Investigation · doi:10.1172/jci200317977 · Cited by 1,189 · see citing works
VEGF-induced neuroprotection, neurogenesis, and angiogenesis after focal cerebral ischemia
Sun, Y., Jin, K., Xie, L., Childs, J., Mao, X. O., Logvinova, A. V., & Greenberg, D. A. (2003) · Journal of Clinical Investigation · doi:10.1172/jci17977 · Cited by 1,181 · see citing works
Rosenberg, G. A., Estrada, E. Y., & Dencoff, J. E. (1998) · Stroke · doi:10.1161/01.str.29.10.2189 · Cited by 861 · see citing works
Wang, L., Zhang, Z., Wang, Y., Zhang, R., & Chopp, M. (2004) · Stroke · doi:10.1161/01.str.0000132196.49028.a4 · Cited by 760 · see citing works
Yamashita, T., Ninomiya, M., Hernandez-Acosta, P., García‐Verdugo, J. M., Sunabori, T., Sakaguchi, M., Adachi, K., Kojima, T., Hirota, Y., Kawase, T., et al. (2006) · Journal of Neuroscience · doi:10.1523/jneurosci.0149-06.2006 · Cited by 720 · see citing works
Molecular targets in cerebral ischemia for developing novel therapeutics
Mehta, S. L., Manhas, N., & Raghubir, R. (2007) · Brain Research Reviews · doi:10.1016/j.brainresrev.2006.11.003 · Cited by 707 · see citing works
Emerging Multipotent Aspects of Hepatocyte Growth Factor
Matsumoto, K., & Nakamura, T. (1996) · The Journal of Biochemistry · doi:10.1093/oxfordjournals.jbchem.a021283 · Cited by 666 · see citing works
Short‐term and long‐term survival of new neurons in the rat dentate gyrus
Dayer, A. G., Ford, A. A., Cleaver, K. M., Yassaee, M., & Cameron, H. A. (2003) · Journal of Comparative Neurology · doi:10.1002/cne.10675 · Cited by 628 · see citing works
Candelario‐Jalil, E., Yang, Y., & Rosenberg, G. A. (2008) · Neuroscience · doi:10.1016/j.neuroscience.2008.06.025 · Cited by 524 · see citing works
Shyu, W., Lin, S., Yang, H.-I., Tzeng, Y.-S., Pang, C., Yen, P.-S., & Li, H. (2004) · Circulation · doi:10.1161/01.cir.0000142616.07367.66 · Cited by 343 · see citing works
Adult neural stem cells in the mammalian central nervous system
Ma, D. K., Bonaguidi, M. A., Ming, G., & Song, H. (2009) · Cell Research · doi:10.1038/cr.2009.56 · Cited by 330 · see citing works
Honda, S., Kagoshima, M., Wanaka, A., Tohyama, M., Matsumoto, K., & Nakamura, T. (1995) · Molecular Brain Research · doi:10.1016/0169-328x(95)00075-4 · Cited by 184 · see citing works
Kampen, J. M. V., Hagg, T., & Robertson, H. A. (2004) · European Journal of Neuroscience · doi:10.1111/j.0953-816x.2004.03342.x · Cited by 168 · see citing works
Yoo, S., Kim, S., Lee, S., Lee, H.-S., Kim, H.-S., Lee, Y., & Suh‐Kim, H. (2008) · Experimental & Molecular Medicine · doi:10.3858/emm.2008.40.4.387 · Cited by 167 · see citing works
Implications of vascular endothelial growth factor for postischemic neurovascular remodeling
Hermann, D. M., & Zechariah, A. (2009) · Journal of Cerebral Blood Flow & Metabolism · doi:10.1038/jcbfm.2009.100 · Cited by 162 · see citing works
Self-citationMiyazawa, T., Matsumoto, K., Ohmichi, H., Katoh, H., Yamashima, T., & Nakamura, T. (1998) · Journal of Cerebral Blood Flow & Metabolism · doi:10.1097/00004647-199804000-00001 · Cited by 136 · see citing works
Novel Therapeutic Strategy to Treat Brain Ischemia
Shimamura, M., Sato, N., Oshima, K., Aoki, M., Kurinami, H., Waguri, S., Uchiyama, Y., Ogihara, T., Kaneda, Y., & Morishita, R. (2004) · Circulation · doi:10.1161/01.cir.0000109496.82683.49 · Cited by 116 · see citing works
Hypoxic Preconditioning-Induced Cerebral Ischemic Tolerance
Wacker, B. K., Park, T. S., & Gidday, J. M. (2009) · Stroke · doi:10.1161/strokeaha.109.560714 · Cited by 115 · see citing works
Neural stem/precursor cells for the treatment of ischemic stroke
Bacigaluppi, M., Pluchino, S., Martino, G., Kilic, E., & Hermann, D. M. (2008) · Journal of the Neurological Sciences · doi:10.1016/j.jns.2007.06.012 · Cited by 111 · see citing works
Self-citationSood, R., Taheri, S., Candelario‐Jalil, E., Estrada, E. Y., & Rosenberg, G. A. (2007) · Journal of Cerebral Blood Flow & Metabolism · doi:10.1038/sj.jcbfm.9600534 · Cited by 108 · see citing works
Expression of HGF and cMet in the developing and adult brain
Achim, C. L., Katyal, S. L., Wiley, C. A., Shiratori, M., Wang, G., Oshika, E., Petersen, B. E., Li, J., & Michalopoulos, G. K. (1997) · Developmental Brain Research · doi:10.1016/s0165-3806(97)00108-9 · Cited by 92 · see citing works
Wada, K., Sugimori, H., Bhide, P. G., Moskowitz, M. A., & Finklestein, S. P. (2003) · Stroke · doi:10.1161/01.str.0000094421.61917.71 · Cited by 78 · see citing works
Nicoleau, C., Benzakour, O., Agasse, F., Thiriet, N., Petit, J., Prestoz, L., Roger, M., Jaber, M., & Coronas, V. (2008) · Stem Cells · doi:10.1634/stemcells.2008-0226 · Cited by 75 · see citing works
Niimura, M., Takagi, N., Takagi, K., Mizutani, R., Ishihara, N., Matsumoto, K., Funakoshi, H., Nakamura, T., & Takeo, S. (2006) · Journal of Cerebral Blood Flow & Metabolism · doi:10.1038/sj.jcbfm.9600287 · Cited by 69 · see citing works
Hepatocyte growth factor attenuates cerebral ischemia-induced learning dysfunction
Date, I., Takagi, N., Takagi, K., Kago, T., Matsumoto, K., Nakamura, T., & Takeo, S. (2004) · Biochemical and Biophysical Research Communications · doi:10.1016/j.bbrc.2004.05.100 · Cited by 68 · see citing works
Wang, Y., Galván, V., Gorostiza, O. F., Ataie, M., Jin, K., & Greenberg, D. A. (2006) · Brain Research · doi:10.1016/j.brainres.2006.07.060 · Cited by 65 · see citing works
Shang, J., Deguchi, K., Yamashita, T., Ohta, Y., Zhang, H., Morimoto, N., Liu, N., Zhang, X., Tian, F., Matsuura, T., et al. (2010) · Journal of Neuroscience Research · doi:10.1002/jnr.22373 · Cited by 61 · see citing works
Date, I., Takagi, N., Takagi, K., Tanonaka, K., Funakoshi, H., Matsumoto, K., Nakamura, T., & Takeo, S. (2006) · Neuroscience Letters · doi:10.1016/j.neulet.2006.08.050 · Cited by 58 · see citing works
Transient focal cerebral ischemia induces sensorimotor deficits in mice
Gerlai, R. T. (2000) · Behavioural Brain Research · doi:10.1016/s0166-4328(99)00130-8 · Cited by 56 · see citing works
Kokuzawa, J., Yoshimura, S., Kitajima, H., Shinoda, J., Kaku, Y., Iwama, T., Morishita, R., Shimazaki, T., Okano, H., Kunisada, T., et al. (2003) · Molecular and Cellular Neuroscience · doi:10.1016/s1044-7431(03)00160-x · Cited by 50 · see citing works
D3 dopamine receptors do not regulate neurogenesis in the subventricular zone of adult mice
Baker, S. A., Baker, K. A., & Hagg, T. (2005) · Neurobiology of Disease · doi:10.1016/j.nbd.2005.01.004 · Cited by 50 · see citing works
Doeppner, T. R., Aanbouri, M. E., Dietz, G. P. H., Weise, J., Schwarting, S., & Bähr, M. (2010) · Neurobiology of Disease · doi:10.1016/j.nbd.2010.05.033 · Cited by 39 · see citing works
Self-citationDoeppner, T. R., Dietz, G. P. H., Aanbouri, M. E., Gerber, J., Witte, O. W., Bähr, M., & Weise, J. (2009) · Neurobiology of Disease · doi:10.1016/j.nbd.2008.12.013 · Cited by 36 · see citing works
Self-citationAnti-VEGF receptor antagonist (VGA1155) reduces infarction in rat permanent focal brain ischemia.
Chiba, Y., Sasayama, T., Miyake, S., Koyama, J., Kondoh, T., Hosoda, K., & Kohmura, E. (2008) · PubMed · doi:10.24546/81000770 · Cited by 33 · see citing works
Greenberg, D. A., & Jin, K. (2006) · NeuroRx · doi:10.1016/j.nurx.2006.08.003 · Cited by 33 · see citing works
Kato, M., Yoshimura, S., Kokuzawa, J., Kitajima, H., Kaku, Y., Iwama, T., Shinoda, J., Kunisada, T., & Sakai, N. (2003) · Neuroreport · doi:10.1097/00001756-200401190-00002 · Cited by 24 · see citing works
Niimura, M., Takagi, N., Takagi, K., Funakoshi, H., Nakamura, T., & Takeo, S. (2006) · European Journal of Pharmacology · doi:10.1016/j.ejphar.2006.01.037 · Cited by 24 · see citing works
Niimura, M., Takagi, N., Takagi, K., Mizutani, R., Tanonaka, K., Funakoshi, H., Matsumoto, K., Nakamura, T., & Takeo, S. (2006) · Neuroscience Letters · doi:10.1016/j.neulet.2006.08.060 · Cited by 18 · see citing works
Shimamura, M. (2006) · Frontiers in bioscience · doi:10.2741/1833 · Cited by 15 · see citing works
商, 敬. (2011) · Institutional Repositories DataBase (IRDB) · Cited by 10 · see citing works
Ozaki, S., Beppu, H., Sonoda, S., Okazaki, H., Mizutani, K., Itani, Y., Hayashi, N., Okamotos, S., & Matsui, T. (2007) · PubMed · Cited by 3 · see citing works
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Zhang, M., Liu, Q., Meng, H., Duan, H., Liu, X., Wu, J., Gao, F., Wang, S., Tan, R., & Yuan, J. (2024) · Signal Transduction and Targeted Therapy · doi:10.1038/s41392-023-01688-x · Cited by 773 · see citing works
Hermann, D. M., & Chopp, M. (2012) · The Lancet Neurology · doi:10.1016/s1474-4422(12)70039-x · Cited by 333 · see citing works
Self-citationZhang, L., Wei, W., Ai, X., Kılıç, E., Hermann, D. M., Venkataramani, V., Bähr, M., & Doeppner, T. R. (2021) · Cell Death and Disease · doi:10.1038/s41419-021-04363-7 · Cited by 192 · see citing works
Self-citationDoeppner, T. R., Doehring, M., Bretschneider, E., Zechariah, A., Kaltwasser, B., Müller, B., Koch, J. C., Bähr, M., Hermann, D. M., & Michel, U. (2013) · Acta Neuropathologica · doi:10.1007/s00401-013-1142-5 · Cited by 155 · see citing works
Self-citationHGF and MET: From Brain Development to Neurological Disorders
Desole, C., Gallo, S., Vitacolonna, A., Montarolo, F., Bertolotto, A., Vivien, D., Comoglio, P., & Crepaldi, T. (2021) · Frontiers in Cell and Developmental Biology · doi:10.3389/fcell.2021.683609 · Cited by 114 · see citing works
Zhang, G., Zhang, T., Li, N., Wu, L., Gu, J., Li, C., Zhao, C., Liu, W., Shan, L., Yu, P., et al. (2017) · British Journal of Pharmacology · doi:10.1111/bph.14102 · Cited by 90 · see citing works
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Chen, J., Shehadah, A., Pal, A., Zacharek, A., Cui, X., Cui, Y., Roberts, C., Lu, M., Zeitlin, A., Hariri, R., et al. (2013) · Cell Transplantation · doi:10.3727/096368911x637380 · Cited by 70 · see citing works
Doeppner, T. R., Młynarczuk-Biały, I., Kuckelkorn, U., Kaltwasser, B., Herz, J., Hasan, M. R., Hermann, D. M., & Bähr, M. (2012) · Brain · doi:10.1093/brain/aws269 · Cited by 64 · see citing works
Self-citationThe pericyte secretome: Potential impact on regeneration
Gaceb, A., Barbariga, M., Özen, Í., & Paul, G. (2018) · Biochimie · doi:10.1016/j.biochi.2018.04.015 · Cited by 63 · see citing works
Nakaguchi, K., Jinnou, H., Kaneko, N., Sawada, M., Hikita, T., Saitoh, S., Tabata, Y., & Sawamoto, K. (2012) · Stem Cells International · doi:10.1155/2012/915160 · Cited by 58 · see citing works
Zhang, L., Graf, I., Kuang, Y., Zheng, X., Haupt, M., Majid, A., Kılıç, E., Hermann, D. M., Psychogios, M., Weber, M. S., et al. (2020) · Arteriosclerosis Thrombosis and Vascular Biology · doi:10.1161/atvbaha.120.315031 · Cited by 56 · see citing works
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Zhu, T., Wang, L., Xie, W., Meng, X., Feng, Y., Sun, G., & Sun, X. (2021) · Frontiers in Pharmacology · doi:10.3389/fphar.2021.615998 · Cited by 55 · see citing works
Wright, J. W., Kawas, L. H., & Harding, J. W. (2014) · Progress in Neurobiology · doi:10.1016/j.pneurobio.2014.11.004 · Cited by 51 · see citing works
Detante, O., Jaillard, A. S., Moisan, A., Barbieux, M., Favre, I., Garambois, K., Hommel, M., & Rémy, C. (2014) · Revue Neurologique · doi:10.1016/j.neurol.2014.10.005 · Cited by 49 · see citing works
Haupt, M., Zechmeister, B., Bosche, B., Lieschke, S., Zheng, X., Zhang, L., Venkataramani, V., Jin, F., Hein, K., Weber, M. S., et al. (2020) · Neuropharmacology · doi:10.1016/j.neuropharm.2020.108357 · Cited by 48 · see citing works
Self-citationLiu, Y., Yang, J., Che, X., Huang, J., Zhang, X., Fu, X., Cai, J., Yao, Y., Zhang, H., Cai, R., et al. (2021) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.2109600118 · Cited by 44 · see citing works
Mungunsukh, O., & Day, R. M. (2013) · Molecular Biology of the Cell · doi:10.1091/mbc.e13-01-0017 · Cited by 41 · see citing works
Doeppner, T. R., Doehring, M., Kaltwasser, B., Majid, A., Lin, F., Bähr, M., Kılıç, E., & Hermann, D. M. (2016) · Molecular Neurobiology · doi:10.1007/s12035-016-0137-3 · Cited by 40 · see citing works
Self-citationCichoń, N., Bijak, M., Czarny, P. L., Miller, E. D., Synowiec, E., Śliwiński, T., & Saluk, J. (2018) · Frontiers in Aging Neuroscience · doi:10.3389/fnagi.2018.00294 · Cited by 39 · see citing works
Doeppner, T. R., Kaltwasser, B., Fengyan, J., Hermann, D. M., & Bähr, M. (2013) · Journal of Cerebral Blood Flow & Metabolism · doi:10.1038/jcbfm.2013.126 · Cited by 37 · see citing works
Self-citationBoldyreva, M. A., Bondar, I. V., Stafeev, I., Макаревич, П. И., Beloglazova, I. B., Zubkova, E., Шевченко, Е. К., Molokotina, Y. D., Karagyaur, M. N., Ratner, E. I., et al. (2018) · Biomedicine & Pharmacotherapy · doi:10.1016/j.biopha.2018.02.138 · Cited by 35 · see citing works
Benoist, C. C., Kawas, L. H., Zhu, M., Tyson, K. A., Stillmaker, L., Appleyard, S. M., Wright, J. W., Wayman, G. A., & Harding, J. W. (2014) · Journal of Pharmacology and Experimental Therapeutics · doi:10.1124/jpet.114.218735 · Cited by 35 · see citing works
RetractedDoeppner, T. R., Kaltwasser, B., Kuckelkorn, U., Henkelein, P., Bretschneider, E., Kılıç, E., & Hermann, D. M. (2015) · Molecular Neurobiology · doi:10.1007/s12035-015-9533-3 · Cited by 28 · see citing works
Self-citationNishioka, R., Sugimoto, K., Aono, H., Mise, A., Choudhury, M. E., Miyanishi, K., Islam, A., Fujita, T., Takeda, H., Takahashi, H., et al. (2015) · Experimental Neurology · doi:10.1016/j.expneurol.2015.12.016 · Cited by 27 · see citing works
Chaparro, R. E., Izutsu, M., Sasaki, T., Sheng, H., Zheng, Y. Z., Sadeghian, H., Qin, T., von Bornstaedt, D., Hérisson, F., Duan, B., et al. (2015) · Journal of Cerebral Blood Flow & Metabolism · doi:10.1038/jcbfm.2015.23 · Cited by 26 · see citing works
Rao, J., Li, H., Zhang, H., Xiang, X., Ding, X., Li, L., Geng, F., & Qi, H. (2023) · Journal of Ethnopharmacology · doi:10.1016/j.jep.2023.117400 · Cited by 26 · see citing works
Method parameters’ impact on mortality and variability in mouse stroke experiments: a meta-analysis
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Xie, H., Yu, K., Zhou, N., Shen, X., Tian, S., Zhang, B., Wang, Y., Wu, J., Liu, G., Jiang, C., et al. (2018) · Translational Stroke Research · doi:10.1007/s12975-018-0629-8 · Cited by 24 · see citing works
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Lin, S., Chang, Y., Lee, W., Chiang, C., Liu, S., Lee, H., Jeng, L., & Shyu, W. (2024) · Advanced Science · doi:10.1002/advs.202404882 · Cited by 22 · see citing works
Liu, Y., Qu, M., Wang, N., & Wang, L. (2021) · Restorative Neurology and Neuroscience · doi:10.3233/rnn-201080 · Cited by 20 · see citing works
Freese, C., Hanada, S., Fallier‐Becker, P., Kirkpatrick, C. J., & Unger, R. E. (2016) · Microvascular Research · doi:10.1016/j.mvr.2016.12.001 · Cited by 18 · see citing works
Johnston, J. L., Reda, S. M., Setti, S. E., Taylor, R. W., Berthiaume, A.-A., Walker, W. E., Wu, W., Moebius, H. J., & Church, K. J. (2023) · Neurotherapeutics · doi:10.1007/s13311-022-01325-5 · Cited by 18 · see citing works
Sun, X. H., Pan, Y., Luo, Y., Guo, H., Zhang, Z., Wang, D., Li, C., & Sun, X. (2023) · Journal of Ethnopharmacology · doi:10.1016/j.jep.2023.117672 · Cited by 18 · see citing works
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Li, F., Ma, Q., Li, L., Zhang, L., Yang, Z., Huang, Y., Han, Z., Wang, R., Tao, Z., Zheng, Y., et al. (2022) · Journal of Clinical Neuroscience · doi:10.1016/j.jocn.2022.02.034 · Cited by 17 · see citing works
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Issa, S. S., Fayoud, H. J., Shaimardanova, A. A., Sufianov, A. A., Суфианова, Г. З., Solovyeva, V. V., & Rizvanov, A. A. (2024) · Biomedicines · doi:10.3390/biomedicines12081906 · Cited by 16 · see citing works
Wei, J., Ma, X., Nehme, A., Cui, Y., Zhang, L., & Qiu, S. (2022) · Frontiers in Aging Neuroscience · doi:10.3389/fnagi.2022.954266 · Cited by 13 · see citing works
Jang, Y. H., You, D. H., & Nam, M. J. (2015) · Growth Factors · doi:10.3109/08977194.2015.1080695 · Cited by 12 · see citing works
Wu, L., Cao, J., Li, N., Chen, H., Liu, W. D., Zhang, G., Liu, Y., Wang, Y., Sun, Y., & Zhang, Z. (2019) · Neuroreport · doi:10.1097/wnr.0000000000001256 · Cited by 11 · see citing works
Moebius, H. J., & Church, K. J. (2023) · Journal of Alzheimer s Disease · doi:10.3233/jad-220871 · Cited by 9 · see citing works
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Chade, A., & Stewart, N. J. (2013) · Journal of the American Society of Hypertension · doi:10.1016/j.jash.2013.01.004 · Cited by 9 · see citing works
Janssen, L., Ai, X., Zheng, X., Wei, W., Çağlayan, A. B., Kılıç, E., Wang, Y., Hermann, D. M., Venkataramani, V., Bähr, M., et al. (2021) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2021.733973 · Cited by 9 · see citing works
Self-citationBernstock, J. D., Verheyen, J., Huang, B. Y., Hallenbeck, J. M., & Pluchino, S. (2014) · InTech eBooks · doi:10.5772/58599 · Cited by 8 · see citing works
Fang, J., & Lee, S.-L. (2014) · Biochimica et Biophysica Acta (BBA) - Molecular Cell Research · doi:10.1016/j.bbamcr.2014.03.020 · Cited by 8 · see citing works
Zeng, W., Wang, Y., Xi, Y., Wei, G., & Ju, R. (2021) · Translational Neuroscience · doi:10.1515/tnsci-2020-0204 · Cited by 7 · see citing works
Bauer, A., Boehme, C., Mayer‐Suess, L., Rudzki, D., Knoflach, M., Kiechl, S., & Reindl, M. (2024) · Scientific Reports · doi:10.1038/s41598-024-62557-3 · Cited by 7 · see citing works
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Borlongan, C., Suárez-Meade, P., Carvajal, H. G., Yasuhara, T., Tajiri, N., & Date, I. (2015) · Brain Circulation · doi:10.4103/2394-8108.172884 · Cited by 7 · see citing works
Vertebrate Neural Stem Cells: Development, Plasticity, and Regeneration
Shimazaki, T. (2016) · The Keio Journal of Medicine · doi:10.2302/kjm.2015-0005-ir · Cited by 7 · see citing works
Chopp, M., & Li, Y. (2011) · European Neurological Review · doi:10.17925/enr.2011.06.02.97 · Cited by 6 · see citing works
Mungunsukh, O., Lee, Y. H., Bottaro, D. P., & Day, R. M. (2016) · Cellular Signalling · doi:10.1016/j.cellsig.2016.05.012 · Cited by 6 · see citing works
Hepatocyte growth factor protects PC12 cells against OGD/R-induced injury by reducing iron
Li, S., Qian, Z., Xu, G.-J., Zheng, J., & Wu, Y. (2020) · Bioscience Reports · doi:10.1042/bsr20200287 · Cited by 6 · see citing works
Bhasin, A. (2014) · Journal of Transplantation Technologies & Research · doi:10.4172/2161-0991.1000136 · Cited by 4 · see citing works
Prototyping Minimal Extracellular Vesicle Mimetics Using Cell-Free Synthesis
Henson, T., Arizzi, A., Meyer, C. C., Wang, D., Lowe, N. M., Wang, Y., Ananda, K., Carney, R. P., Wang, A., & Tan, C. (2026) · ACS Nano · doi:10.1021/acsnano.5c05047 · Cited by 3 · see citing works
Nakka, S. S., Johansson, J., Shahzad, F., Hanning, A., & Nayeri, F. (2013) · Open Journal of Gastroenterology · doi:10.4236/ojgas.2013.31007 · Cited by 3 · see citing works
Mucke, H. A. (2013) · Pharmaceutical Patent Analyst · doi:10.4155/ppa.13.46 · Cited by 3 · see citing works
Wells, R. G., Azzam, A. F., Hiller, A., & Sardinia, M. F. (2024) · Journal of Huntington s Disease · doi:10.3233/jhd-231507 · Cited by 2 · see citing works
Lönn, J., Nakka, S. S., Olsson, H., Bengtsson, T., Almer, S. H., & Nayeri, F. (2013) · Advances in Bioscience and Biotechnology · doi:10.4236/abb.2013.48a2006 · Cited by 2 · see citing works
Pharmacological Agents in Post Stroke Recovery
Moonis, M. (2014) · Journal of Neurology & Stroke · doi:10.15406/jnsk.2014.01.00040 · Cited by 1 · see citing works
Paradoxical role of hepatocyte growth factor in ischemic stroke: stroke risk/stroke recovery
Al-Ahmar, I., Mohamed, N., & Elshony, H. (2021) · The Egyptian Journal of Neurology Psychiatry and Neurosurgery · doi:10.1186/s41983-021-00364-7 · Cited by 1 · see citing works
Cui, Y., Ma, X., Wei, J., Chen, C., Shakir, N., Guirram, H., Dai, Z., Anderson, T. R., Ferguson, D., & Qiu, S. (2024) · Neural Regeneration Research · doi:10.4103/nrr.nrr-d-23-01471 · Cited by 1 · see citing works
Unraveling the impact of human cerebrospinal fluid on human neural stem cell fate
Radoszkiewicz, K., Bzinkowska, A., Sypecka, M., Sulejczak, D., Ferrari, D., Gelati, M., Vescovi, A. L., & Sarnowska, A. (2025) · Frontiers in Cell and Developmental Biology · doi:10.3389/fcell.2025.1527557 · Cited by 1 · see citing works
Lee, S., Lee, M. H., Wu, K., Chiang, C., Chang, Y.-X., Fang, J., Tung, H., Kuo, L., & Wang, Y. (2022) · The FASEB Journal · doi:10.1096/fj.202200414r · Cited by 1 · see citing works
Cazzella, T., Fortaner‐Uyà, L., Paolini, M., Percaccioli, C., Colombo, F., Venturelli, E., Colombo, C., Zanardi, R., Spadini, S., Lorenzi, C., et al. (2026) · Psychiatry and Clinical Neurosciences · doi:10.1111/pcn.70144
VEGF-induced angiogenesis in the ischemic brain: effect of hyperlipidemia
Zechariah, A. (2012) · DuEPublico (University of Duisburg-Essen)
Self-citationNeuroprotective Agents: An Overview on the General Modes of Action
Volsko, C. M., & Dutta, R. (2017) · doi:10.1002/9783527803781.ch2
Neuronal Regeneration by Using Endogenous Stem Cells and DDS Technology
Tsuboi, Y., Sawada, M., Otsuka, T., & Sawamoto, K. (2017) · Drug Delivery System · doi:10.2745/dds.32.46
Targeting Adult Neurogenesis for Brain Recovery After Stroke: The Next Frontier in Stroke Medicine
Ong, L. K., Ilicic, M., Hood, R. J., Warren, K. E., & Coupland, K. (2022) · Springer eBooks · doi:10.1007/978-981-16-8562-0_1
Sun, X. H., Pan, Y., Luo, Y., Guo, H., Zhang, Z.-X., Wang, D., Li, C., & Sun, X. (2023) · SSRN Electronic Journal · doi:10.2139/ssrn.4618293
Lenhard, T., Herkel, M.-T., Falk, C. S., Balzer, V., Fricker, G., Schranz, C., & Meyding‐Lamadé, U. (2025) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2025.03.27.645675
Martino, K. A., Nakhre, A., Demarest, R. M., & Devilbiss, D. M. (2025) · Neurotrauma Reports · doi:10.1177/2689288x251392851
Hepatokines and stellakines in liver and neurological diseases: The liver-brain axis
Park, J., Guo, F., Lee, J. E., & Cheon, S. Y. (2026) · Experimental Neurology · doi:10.1016/j.expneurol.2026.115899
- Authors
- Doeppner, T. R., Kaltwasser, B., ElAli, A., Zechariah, A., Hermann, D. M., & Bähr, M.
- Affiliations
- Universitätsmedizin Göttingen (DE)
- University of Duisburg-Essen (DE)
- Corresponding author
- Doeppner, Thorsten R
- Venue
- Journal of Cerebral Blood Flow & Metabolism
- Publisher
- SAGE Publications
- Published
- 2010-12-01
- Volume
- 31
- Issue
- 5
- Pages
- 1251-1262
- ISSN
- 0271-678X (ISSN-L)
- 1559-7016
- PMC
- PMC3099629
- OpenAlex
- W2007483459
- Cited by
- 76
- References
- 43
- Citations by year
- 2026: 3 · 2025: 3 · 2024: 6 · 2023: 4 · 2022: 8 · 2021: 8 · 2020: 3 · 2019: 1 · 2018: 4 · 2017: 3 · 2016: 5 · 2015: 5 · 2014: 7 · 2013: 10 · 2012: 5
- FWCI
- 1.62
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Locations
- Journal of Cerebral Blood Flow & Metabolism (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Universitätsbibliographie, Universität Duisburg-Essen (submittedVersion)
- GRO (submittedVersion)
- Topics
- Life Sciences › Neuroscience › Developmental Neuroscience › Neurogenesis and neuroplasticity mechanisms
- Life Sciences › Neuroscience › Neurology › Neurological Disorders and Treatments
- Health Sciences › Medicine › Epidemiology › Acute Ischemic Stroke Management
- Keywords
- hepatocyte growth factor, acute stroke, neuroprotection, stroke recovery, neural progenitor cells, cell proliferation, neuronal differentiation, neurosphere formation, infarct size, neuronal cell death, blood-brain barrier integrity, matrix metalloproteinases, MMP-2, MMP-9, caspase-3, neurovascular remodeling
- MeSH terms
- Animals, Cell Differentiation, Immunohistochemistry, Male, Mice, Inbred C57BL, Time, Hepatocyte Growth Factor, Neuroprotective Agents, Recovery of Function, In Situ Nick-End Labeling, Stroke, Cell Proliferation, Mice, Neural Stem Cells
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