Sex differences in mitochondrial biogenesis determine neuronal death and survival in response to oxygen glucose deprivation and reoxygenation
Open accessAbstract
BACKGROUND: Mitochondrial dysfunction has been linked to neuronal death and a wide array of neurodegenerative diseases. Previously, we have shown sex differences in mitochondria-mediated cell death pathways following hypoxia-ischemia. However, the role of mitochondrial biogenesis in hypoxic-ischemic brain injury between male vs. female has not been studied yet. RESULTS: Primary cerebellar granule neurons (CGNs), isolated from P7 male and female mice (CD-1) segregated based on visual inspection of sex, were exposed to 2 h of oxygen glucose deprivation (OGD) followed by 6-24 h of reoxygenation (Reox). Mitochondrial membrane potential (ΔΨm) and cellular ATP levels were reduced significantly in XX CGNs as compared to XY CGNs. Mitochondrial DNA (mtDNA) content was increased (>2-fold) at 2 h OGD in XY CGNs and remained increased up to 24 h of Reox compared to XX neurons and normoxia controls. The expression of mitochondrial transcription factor A (Tfam), the nuclear respiratory factor-1 (NRF-1) and the peroxisome proliferator-activated receptor γ coactivator-1α (PGC-1α), a master regulator of mitochondrial biogenesis, were up-regulated (2-fold, ***p < 0.001) in XY CGNs but slightly reduced or remained unchanged in XX neurons. Similarly, the TFAM and PGC-1α protein levels and the mitochondrial proteins HSP60 and COXIV were increased in XY neurons only. Supportively, a balanced stimulation of fusion (Mfn 1and Mfn 2) and fission (Fis 1 and Drp 1) genes and enhanced formation of donut-shaped mitochondria were observed in XY CGNs vs. XX neurons (**p < 0.01). CONCLUSIONS: Our results demonstrate that OGD/Reox alters mitochondrial biogenesis and morphological changes in a sex-specific way, influencing neuronal injury/survival differently in both sexes.
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Sex differences in the regulation of genes controlling mitochondrial dynamics have been reported in mice following ischemic injury, a condition that shares pathophysiological features with TBI.
“sex differences in the regulation of genes controlling mitochondrial dynamics have been reported in mice following ischemic injury, a condition that shares pathophysiological features with TBI.”
From Sex Differences in Traumatic Brain Injury: What We Know and What We Should Know (2019) · cites this paper as [136]
Multiple aspects of mitochondrial function appear to be different between males and females under physiological conditions.
“multiple aspects of mitochondrial function appear to be different between males and females under physiological conditions”
From Sex Differences in Traumatic Brain Injury: What We Know and What We Should Know (2019) · cites this paper as [136]
Differences in mitochondrial function between males and females may be exacerbated by stress or injury.
“differences may be exacerbated by stress or injury.”
From Sex Differences in Traumatic Brain Injury: What We Know and What We Should Know (2019) · cites this paper as [136]
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Cites
The Ubiquitin-Proteasome Proteolytic Pathway: Destruction for the Sake of Construction
Glickman, M. H., & Ciechanover, A. J. (2002) · Physiological Reviews · doi:10.1152/physrev.00027.2001 · Cited by 4,216 · see citing works
A Cold-Inducible Coactivator of Nuclear Receptors Linked to Adaptive Thermogenesis
Puigserver, P., Wu, Z., Park, C. W., Graves, R., Wright, M., & Spiegelman, B. M. (1998) · Cell · doi:10.1016/s0092-8674(00)81410-5 · Cited by 3,864 · see citing works
The Pathophysiology of Mitochondrial Cell Death
Green, D. R., & Kroemer, G. (2004) · Science · doi:10.1126/science.1099320 · Cited by 3,416 · see citing works
Chen, H., Detmer, S. A., Ewald, A. J., Griffin, E. E., Fraser, S. E., & Chan, D. C. (2003) · The Journal of Cell Biology · doi:10.1083/jcb.200211046 · Cited by 2,601 · see citing works
Mitochondria: Dynamic Organelles in Disease, Aging, and Development
Chan, D. C. (2006) · Cell · doi:10.1016/j.cell.2006.06.010 · Cited by 1,987 · see citing works
Comparing protein abundance and mRNA expression levels on a genomic scale
Greenbaum, D. (2003) · Genome biology · doi:10.1186/gb-2003-4-9-117 · Cited by 1,692 · see citing works
Transcriptional paradigms in mammalian mitochondrial biogenesis and function
Scarpulla, R. C. (2008) · Physiological Reviews · doi:10.1152/physrev.00025.2007 · Cited by 1,666 · see citing works
Smiley, S. T., Reers, M., Mottola-Hartshorn, C., Lin, M., Chen, A. B., Smith, T. W., Steele, G., & Chen, L. B. (1991) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.88.9.3671 · Cited by 1,629 · see citing works
Mitochondrial transcription factor A is necessary for mtDNA maintance and embryogenesis in mice
Larsson, N.-G., Wang, J., Wilhelmsson, H., Oldfors, A., Rustin, P., Lewandoski, M., Barsh, G. S., & Clayton, D. A. (1998) · Nature Genetics · doi:10.1038/ng0398-231 · Cited by 1,594 · see citing works
Mitochondrial dynamics and apoptosis
Suen, D.-F., Norris, K. L., & Youle, R. J. (2008) · Genes & Development · doi:10.1101/gad.1658508 · Cited by 1,270 · see citing works
Cossarizza, A., Baccarani-Contri, M., Kalashnikova, G., & Franceschi, C. (1993) · Biochemical and Biophysical Research Communications · doi:10.1006/bbrc.1993.2438 · Cited by 1,031 · see citing works
D'Mello, S. R., Galli, C., Ciotti, T., & Calissano, P. (1993) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.90.23.10989 · Cited by 892 · see citing works
Cellular and molecular mechanisms of mitochondrial function
Osellame, L. D., Blacker, T. S., & Duchen, M. R. (2012) · Best Practice & Research Clinical Endocrinology & Metabolism · doi:10.1016/j.beem.2012.05.003 · Cited by 871 · see citing works
The role of mitochondria in apoptosis
Jeong, S., & Seol, D. (2008) · BMB Reports · doi:10.5483/bmbrep.2008.41.1.011 · Cited by 767 · see citing works
TRANSCRIPTION OF THE MAMMALIAN MITOCHONDRIAL GENOME
Clayton, D. A. (1984) · Annual Review of Biochemistry · doi:10.1146/annurev.bi.53.070184.003041 · Cited by 446 · see citing works
Guo, Y.-F., Xiao, P., Lei, S., Deng, F., Xiao, G. G., Liu, Y., Chen, X., Li, L., Wu, S., Chen, Y., et al. (2008) · Acta Biochimica et Biophysica Sinica · doi:10.1111/j.1745-7270.2008.00418.x · Cited by 424 · see citing works
Innate Gender-based Proclivity in Response to Cytotoxicity and Programmed Cell Death Pathway
Du, L., Bayır, H., Lai, Y., Zhang, X., Kochanek, P. M., Watkins, S. C., Graham, S. H., & Clark, R. S. B. (2004) · Journal of Biological Chemistry · doi:10.1074/jbc.m405461200 · Cited by 351 · see citing works
Lagranha, C. J., Deschamps, A. M., Aponte, A. M., Steenbergen, C., & Murphy, E. (2010) · Circulation Research · doi:10.1161/circresaha.109.213645 · Cited by 328 · see citing works
Free radicals, mitochondria, and hypoxia–ischemia in the developing brain
Blomgren, K., & Hagberg, H. (2005) · Free Radical Biology and Medicine · doi:10.1016/j.freeradbiomed.2005.08.040 · Cited by 310 · see citing works
Sex chromosome genes directly affect brain sexual differentiation
Carruth, L. L., Reisert, I., & Arnold, A. P. (2002) · Nature Neuroscience · doi:10.1038/nn922 · Cited by 298 · see citing works
Abnormal mitochondrial dynamics and neurodegenerative diseases
Su, B., Wang, X., Zheng, L., Perry, G. L., Smith, M. A., & Zhu, X. (2009) · Biochimica et Biophysica Acta (BBA) - Molecular Basis of Disease · doi:10.1016/j.bbadis.2009.09.013 · Cited by 289 · see citing works
Liu, X., & Hajnóczky, G. (2011) · Cell Death and Differentiation · doi:10.1038/cdd.2011.13 · Cited by 285 · see citing works
Soltys, B. J., & Gupta, R. S. (1996) · Experimental Cell Research · doi:10.1006/excr.1996.0003 · Cited by 271 · see citing works
Rapidly Increased Neuronal Mitochondrial Biogenesis After Hypoxic-Ischemic Brain Injury
Yin, W., Signore, A. P., Iwai, M., Cao, G., Gao, Y., & Chen, J. (2008) · Stroke · doi:10.1161/strokeaha.108.520114 · Cited by 229 · see citing works
Gutsaeva, D. R., Carraway, M. S., Suliman, H. B., It, D., Shitara, H., Yonekawa, H., & Piantadosi, C. A. (2008) · Journal of Neuroscience · doi:10.1523/jneurosci.5654-07.2008 · Cited by 200 · see citing works
Mandemakers, W. J., Morais, V. A., & Strooper, B. D. (2007) · Journal of Cell Science · doi:10.1242/jcs.03443 · Cited by 176 · see citing works
Xu, S., Zhou, Z., Zhang, L., Yu, Z., Zhang, W., Wang, Y., Wang, X., Li, M., Chen, Y., Chen, C., et al. (2009) · Brain Research · doi:10.1016/j.brainres.2009.10.062 · Cited by 149 · see citing works
The Many Shapes of Mitochondrial Membranes
Griparić, L., & van der Bliek, A. M. (2001) · Traffic · doi:10.1034/j.1600-0854.2001.1r008.x · Cited by 145 · see citing works
Robertson, C., Scafidi, S., McKenna, M. C., & Fiskum, G. M. (2009) · Experimental Neurology · doi:10.1016/j.expneurol.2009.04.030 · Cited by 143 · see citing works
Assessing mitochondria biogenesis
Medeiros, D. M. (2008) · Methods · doi:10.1016/j.ymeth.2008.09.026 · Cited by 135 · see citing works
Puka‐Sundvall, M., Gajkowska, B., Cholewiński, M., Blomgren, K., Łazarewicz, J. W., & Hagberg, H. (2000) · Developmental Brain Research · doi:10.1016/s0165-3806(00)00110-3 · Cited by 127 · see citing works
Mitochondrial Targets for Stroke
Vosler, P. S., Graham, S. H., Wechsler, L. R., & Chen, J. (2009) · Stroke · doi:10.1161/strokeaha.108.543769 · Cited by 120 · see citing works
Penaloza, C. G., Estevez, B., Orlanski, S., Sikorska, M., Walker, R., Smith, C. C., Smith, B., Lockshin, R. A., & Zakeri, Z. F. (2009) · The FASEB Journal · doi:10.1096/fj.08-119388 · Cited by 111 · see citing works
Gender-Related Differences in Apoptotic Pathways After Neonatal Cerebral Ischemia
Renolleau, S., Fau, S., & Charriaut‐Marlangue, C. (2007) · The Neuroscientist · doi:10.1177/1073858407308889 · Cited by 106 · see citing works
Robertson, C. (2004) · Journal of Bioenergetics and Biomembranes · doi:10.1023/b:jobb.0000041769.06954.e4 · Cited by 105 · see citing works
Kaufman, B. A., Kolesar, J. E., Perlman, P. S., & Butow, R. A. (2003) · The Journal of Cell Biology · doi:10.1083/jcb.200306132 · Cited by 101 · see citing works
Cerebral Palsy After Perinatal Arterial Ischemic Stroke
Golomb, M. R., Garg, B. P., Saha, C., Azzouz, F., & Williams, L. S. (2008) · Journal of Child Neurology · doi:10.1177/0883073807309246 · Cited by 96 · see citing works
Liu, F., Lang, J. T., Li, J., Benashski, S. E., Siegel, M., Xu, Y., & McCullough, L. D. (2011) · Stroke · doi:10.1161/strokeaha.110.594861 · Cited by 79 · see citing works
Reduction and Restoration of Mitochondrial DNA Content After Focal Cerebral Ischemia/Reperfusion
Chen, H., Hu, C., He, Y. Y., Yang, D., Xu, J., & Hsu, C. Y. (2001) · Stroke · doi:10.1161/hs1001.097099 · Cited by 68 · see citing works
Arnold, S., de Araújo, G. W., & Beyer, C. (2008) · Journal of Molecular Endocrinology · doi:10.1677/jme-08-0085 · Cited by 65 · cited 7× · see citing works
“The sequence of primers for mitochondrial fusion and fission used are; Mfn15’- CAGAGAAGAGGGTTTATTCA-3’ (sense) and 5’- ACTCATCAACCAAAACAGAT-3’ (antisense), Mfn 2 5’- TGAATGTTGTGTTCTTTCTG-3’ (sense) and 5’- AA GTGCTCTCTGCTAAATGT-3’ (antisense), Drp1 5’- TTT GCTCGTGTGAAGACTGG-3’ (sense) and 5’- TCCTGG AGCTTCCTTTCTGA-3’…”
BackgroundMethodInfluentialHossain, M. A., Russell, J. C., Gomes, R., & Laterra, J. (2002) · Journal of Neurochemistry · doi:10.1046/j.1471-4159.2002.00837.x · Cited by 65 · see citing works
Self-citationMitochondrial Biogenesis and the Role of the Protein Import Pathway
Hood, D. A., Adhihetty, P. J., Colavecchia, M., Gordon, J. W., Irrcher, I., JOSEPH, A.-M., LOWE, S. T., & Rungi, A. A. (2003) · Medicine & Science in Sports & Exercise · doi:10.1097/00005768-200301000-00015 · Cited by 54 · see citing works
Neuronal Pentraxin 1: A Novel Mediator of Hypoxic-Ischemic Injury in Neonatal Brain
Hossain, M. A., Russell, J. C., O’Brien, R., & Laterra, J. (2004) · Journal of Neuroscience · doi:10.1523/jneurosci.0347-04.2004 · Cited by 47 · see citing works
Self-citationSharma, J., Nelluru, G., Wilson, M. A., Johnston, M. V., & Hossain, M. A. (2011) · ASN NEURO · doi:10.1042/an20100032 · Cited by 41 · see citing works
Self-citationReactive Structural Dynamics of Synaptic Mitochondria in Ischemic Delayed Neuronal Death
Bertoni–Freddari, C., Fattoretti, P., Casoli, T., Stefano, G. D., Solazzi, M., PERNA, E., & de Angelis, C. (2006) · Annals of the New York Academy of Sciences · doi:10.1196/annals.1378.003 · Cited by 16 · see citing works
Alterations in mitochondria and mtTFA in response to LPS-induced differentiation of B-cells
Kain, K. H., Popov, V. L., & Herzog, N. K. (2000) · Biochimica et Biophysica Acta (BBA) - Gene Structure and Expression · doi:10.1016/s0167-4781(00)00223-2 · Cited by 15 · see citing works
Flagged first, then by citations
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Sorted by citations
Mitochondrial Dysfunction and Biogenesis in Neurodegenerative diseases: Pathogenesis and Treatment
Golpich, M., Amini, E., Mohamed, Z., Raymond, A. A., Ibrahim, N. M., & Ahmadiani, A. (2016) · CNS Neuroscience & Therapeutics · doi:10.1111/cns.12655 · Cited by 540 · see citing works
Sex Differences in Traumatic Brain Injury: What We Know and What We Should Know
Gupte, R. P., Brooks, W. M., Vukas, R. R., Pierce, J. D., & Harris, J. L. (2019) · Journal of Neurotrauma · doi:10.1089/neu.2018.6171 · Cited by 533 · see citing works
Marosi, K., Kim, S. W., Moehl, K., Scheibye‐Knudsen, M., Cheng, A., Cutler, R., Camandola, S., & Mattson, M. P. (2016) · Journal of Neurochemistry · doi:10.1111/jnc.13868 · Cited by 242 · see citing works
Miyazono, Y., Hirashima, S., Ishihara, N., Kusukawa, J., Nakamura, K., & Ohta, K. (2018) · Scientific Reports · doi:10.1038/s41598-017-18582-6 · Cited by 221 · see citing works
Muscle metabolism and atrophy: let’s talk about sex
Rosa-Caldwell, M. E., & Greene, N. P. (2019) · Biology of Sex Differences · doi:10.1186/s13293-019-0257-3 · Cited by 202 · see citing works
Sex differences in mitochondrial (dys)function: Implications for neuroprotection
Demarest, T. G., & McCarthy, M. M. (2015) · Journal of Bioenergetics and Biomembranes · doi:10.1007/s10863-014-9583-7 · Cited by 192 · see citing works
Khalifa, A. R. M., Abdel‐Rahman, E. A., Mahmoud, A. M., Ali, M. H., Noureldin, M., Saber, S. H., Mohsen, M., & Ali, S. S. (2017) · Physiological Reports · doi:10.14814/phy2.13125 · Cited by 154 · see citing works
Zhao, Q., Tian, Z., Zhou, G., Niu, Q., Chen, J., Li, P., Dong, L., Xia, T., Zhang, S., & Wang, A. (2020) · Theranostics · doi:10.7150/thno.42387 · Cited by 127 · see citing works
Ullah, M. F., Ahmad, A., Bhat, S. H., Abuduhier, F. M., Barreto, G. E., & Ashraf, G. M. (2019) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2019.04.003 · Cited by 113 · see citing works
Brunst, K. J., Sanchez-Guerra, M., Chiu, Y.-H. M., Wilson, A., Coull, B. A., Kloog, I., Schwartz, J., Brennan, K. J., Bosquet Enlow, M., Wright, R. O., et al. (2018) · Environment International · doi:10.1016/j.envint.2017.12.020 · Cited by 81 · see citing works
Quercetin-mediated SIRT1 activation attenuates collagen-induced mice arthritis
Shen, P., Lin, W., Ba, X., Huang, Y., Chen, Z., Han, L., Qin, K., Huang, Y., & Tu, S. (2021) · Journal of Ethnopharmacology · doi:10.1016/j.jep.2021.114213 · Cited by 80 · see citing works
The problem of genotype and sex differences in life expectancy in transgenic AD mice
Rae, E. A., & Brown, R. E. (2015) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2015.09.002 · Cited by 75 · see citing works
Mitochondria and sensory processing in inflammatory and neuropathic pain
Ribeiro, P. S. S., Willemen, H. L. D. M., & Eijkelkamp, N. (2022) · Frontiers in Pain Research · doi:10.3389/fpain.2022.1013577 · Cited by 86 · see citing works
Pataj, Z., Liebisch, G., Schmitz, G., & Matysik, S. (2015) · Journal of Chromatography A · doi:10.1016/j.chroma.2015.11.015 · Cited by 69 · see citing works
Yasuda, K., Maki, T., Kinoshita, H., Kaji, S., Toyokawa, M., Nishigori, R., Kinoshita, Y., Ono, Y., Kinoshita, A., & Takahashi, R. (2020) · Stem Cell Research · doi:10.1016/j.scr.2020.101866 · Cited by 65 · see citing works
Pastukh, V. M., Gorodnya, O. M., Gillespie, M. N., & Ruchko, M. V. (2016) · Free Radical Biology and Medicine · doi:10.1016/j.freeradbiomed.2016.04.011 · Cited by 54 · see citing works
NLRP3 inflammasomes: A potential target to improve mitochondrial biogenesis in Parkinson's disease
Khot, M., Sood, A., Tryphena, K. P., Khan, S. S., Srivastava, S., Singh, S. B., & Khatri, D. K. (2022) · European Journal of Pharmacology · doi:10.1016/j.ejphar.2022.175300 · Cited by 55 · see citing works
Mitochondrial dynamics, mitophagy and biogenesis in neonatal hypoxic‐ischaemic brain injury
Thornton, C., Jones, A., Nair, S., Aabdien, A., Mallard, C. E., & Hagberg, H. (2017) · FEBS Letters · doi:10.1002/1873-3468.12943 · Cited by 55 · see citing works
Hou, D., Liao, H., Hao, S., Liu, R., Huang, H., & Duan, C. (2024) · Heliyon · doi:10.1016/j.heliyon.2024.e28501 · Cited by 51 · see citing works
Jia, L., Wang, J., Cao, H., Zhang, X., Rong, W., & Xu, Z. (2020) · Neuroscience · doi:10.1016/j.neuroscience.2020.02.035 · Cited by 49 · see citing works
Rodríguez‐Fanjul, J., Fernández-Feijóo, C. D., López‐Abad, M., López-Ramos, M. G., Balada, R., Alcántara, S., & Camprubí-Camprubí, M. (2017) · PLoS ONE · doi:10.1371/journal.pone.0184643 · Cited by 45 · see citing works
Li, J., Zhu, X., Yang, S., Xu, H., Guo, M., Yao, Y., Huang, Z., & Lin, D. (2019) · Neurochemical Research · doi:10.1007/s11064-019-02799-0 · Cited by 44 · see citing works
The role of mitochondrial disturbances in Alzheimer, Parkinson and Huntington diseases
Carvalho, C., Correia, S. C., Cardoso, S., Plácido, A. I., Candeias, E., Duarte, A. I., & Moreira, P. I. (2015) · Expert Review of Neurotherapeutics · doi:10.1586/14737175.2015.1058160 · Cited by 43 · see citing works
Jaber, S. M., Bordt, E. A., Bhatt, N. M., Lewis, D. M., Gerecht, S., Fiskum, G., & Polster, B. M. (2018) · Neurochemistry International · doi:10.1016/j.neuint.2017.09.003 · Cited by 40 · see citing works
Zawada, I., Masternak, M. M., List, E. O., Stout, M. B., Berryman, D. E., Lewiñski, A., Kopchick, J. J., Bartke, A., Karbownik‐Lewińska, M., & Gesing, A. (2015) · Aging · doi:10.18632/aging.100733 · Cited by 39 · see citing works
Wang, L., Zhang, X., Chan, J. Y., Shan, L., Cui, G., Cui, Q., Wang, Y., Li, J., Chen, H., Zhang, Q., et al. (2015) · Journal of Cellular Biochemistry · doi:10.1002/jcb.25253 · Cited by 38 · see citing works
Semple, B. D. (2014) · Experimental Neurology · doi:10.1016/j.expneurol.2014.07.013 · Cited by 31 · see citing works
Demarest, T. G., Schuh, R. A., Waite, E. L., Waddell, J., McKenna, M. C., & Fiskum, G. M. (2016) · Journal of Bioenergetics and Biomembranes · doi:10.1007/s10863-016-9678-4 · Cited by 28 · see citing works
Chen, J., Shen, N., Duan, X., & Guo, Y. (2017) · Experimental and Therapeutic Medicine · doi:10.3892/etm.2017.5589 · Cited by 26 · see citing works
Li, L., Voloboueva, L. A., Griffiths, B. B., Xu, L., Giffard, R. G., & Stary, C. M. (2021) · Mitochondrion · doi:10.1016/j.mito.2021.04.013 · Cited by 23 · see citing works
Elucidating Critical Proteinopathic Mechanisms and Potential Drug Targets in Neurodegeneration
Dar, K. B., Bhat, A. H., Amin, S., Reshi, B. A., Zargar, M. A., Masood, A., & Ganie, S. A. (2019) · Cellular and Molecular Neurobiology · doi:10.1007/s10571-019-00741-0 · Cited by 23 · see citing works
Thatipamula, S., Rahim, M. A., Zhang, J., & Hossain, M. A. (2014) · Neurobiology of Disease · doi:10.1016/j.nbd.2014.12.016 · Cited by 20 · see citing works
Self-citationJu, X., Ryu, M. J., Cui, J., Lee, Y., Park, S., Hong, B., Yoo, S., Lee, W. H., Shin, Y. S., Yoon, S.-H., et al. (2020) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2020.00004 · Cited by 19 · see citing works
Lee, C., Wu, C., Chou, W., Lee, M., Chou, M., Lee, S.-Y., & Wang, L. (2019) · Mitochondrion · doi:10.1016/j.mito.2019.07.007 · Cited by 18 · see citing works
Circulating Cell-Free Mitochondrial DNA in Pregnancy
Bradshaw, J. L., Cushen, S. C., Phillips, N., & Goulopoulou, S. (2022) · Physiology · doi:10.1152/physiol.00037.2021 · Cited by 16 · see citing works
Zhu, M., Zhang, D., Zhou, C. Y., & Chai, Z. (2019) · ACS Chemical Neuroscience · doi:10.1021/acschemneuro.8b00737 · Cited by 18 · see citing works
Sex may influence motor phenotype in a novel rodent model of cerebral palsy
Aravamuthan, B. R., Gandham, S., Young, A. B., & Rutkove, S. B. (2019) · Neurobiology of Disease · doi:10.1016/j.nbd.2019.104711 · Cited by 18 · see citing works
Shaw, R. L., Norton, C. E., & Segal, S. S. (2021) · American Journal of Physiology-Heart and Circulatory Physiology · doi:10.1152/ajpheart.00956.2020 · Cited by 18 · see citing works
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Ziaaldini, M. M., Hosseini, S. R. A., & Fathi, M. (2017) · Physiological Research · doi:10.33549/physiolres.933329 · Cited by 16 · see citing works
Santa‐Marina, L., Lertxundi, N., Andiarena, A., Irizar, A., Sunyer, J., Molinuevo, A., Llop, S., Júlvez, J., Beneíto, A., Ibarluzea, J. M., et al. (2020) · International Journal of Environmental Research and Public Health · doi:10.3390/ijerph17217704 · Cited by 14 · see citing works
Azarafrouz, F., Farhangian, M., Chavoshinezhad, S., Dargahi, S., Nassiri‐Asl, M., & Dargahi, L. (2022) · Neuropeptides · doi:10.1016/j.npep.2022.102262 · Cited by 13 · see citing works
Protective Roles of N-acetyl Cysteine and/or Taurine against Sumatriptan-Induced Hepatotoxicity
Fard, J. K., Hamzeiy, H., Sattari, M., & Eghbal, M. A. (2016) · Advanced Pharmaceutical Bulletin · doi:10.15171/apb.2016.077 · Cited by 13 · see citing works
Critical role of extracellularly secreted neuronal pentraxin 1 in ischemic neuronal death
Thatipamula, S., & Hossain, M. A. (2014) · BMC Neuroscience · doi:10.1186/s12868-014-0133-3 · Cited by 12 · see citing works
Self-citationToniazzo, A. P., Arcego, D. M., Lazzaretti, C., Mota, C. D. S., Schnorr, C. E., Pettenuzzo, L. F., Krolow, R., Moreira, J. C. F., & Dalmaz, C. (2019) · Neurochemistry International · doi:10.1016/j.neuint.2019.01.008 · Cited by 12 · see citing works
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Guan, D., Liang, C., Zheng, D., Liu, S., Luo, J., Cai, Z., Zhang, H., & Chen, J. (2025) · Neurochemistry International · doi:10.1016/j.neuint.2024.105927 · Cited by 11 · see citing works
Jiang, J., Giri, T. K., Raghuraman, N., Cahill, A. G., & Palanisamy, A. (2021) · Scientific Reports · doi:10.1038/s41598-021-89299-w · Cited by 10 · see citing works
Revisiting the Mitochondrial Function and Communication in Neurodegenerative Diseases
Wankhede, N. L., Kale, M. B., Umare, M. D., Lokhande, S., Upaganlawar, A. B., Wal, P., Taksande, B. G., Umekar, M. J., Khandige, P. S., Singh, B., et al. (2024) · Current Pharmaceutical Design · doi:10.2174/0113816128286655240304070740 · Cited by 9 · see citing works
Sexual Dimorphism in Migraine. Focus on Mitochondria
Fila, M., Przysło, Ł., Derwich, M., Pawłowska, E., & Błasiak, J. (2025) · Current Pain and Headache Reports · doi:10.1007/s11916-024-01317-4 · Cited by 8 · see citing works
Lin, D., Zhu, X., Li, J., Yao, Y., Guo, M., & Xu, H. (2020) · Human & Experimental Toxicology · doi:10.1177/0960327120926242 · Cited by 8 · see citing works
Polyphenols and Exercise in Mitochondrial Biogenesis: Focus on Age-Related CNS Disorders
Tu, J. (2025) · Molecular Neurobiology · doi:10.1007/s12035-025-05121-y · Cited by 10 · see citing works
Cell-type-specific transposon demethylation and TAD remodeling in aging mouse brain
Zeng, Q., Wang, W., Tian, W., Klein, A., Bartlett, A., Liu, H., Nery, J. R., Castanon, R., Osteen, J. K., Johnson, N. D., et al. (2026) · Cell · doi:10.1016/j.cell.2026.02.015 · Cited by 12 · see citing works
Bahire, K., Maļuhins, R., Bello, F. M., Valero-Freitag, S., Jelisejevs, I., Gile, R., Upīte, J., Plesnila, N., & Jansone, B. (2023) · Mitochondrion · doi:10.1016/j.mito.2023.02.005 · Cited by 7 · see citing works
Margulies, C. M., Chaim, I. A., Mazumder, A., Criscione, J., & Samson, L. D. (2017) · PLoS ONE · doi:10.1371/journal.pone.0184619 · Cited by 7 · see citing works
Rescue from Sexually Dimorphic Neuronal Cell Death by Estradiol and PI3 Kinase Activity
Cheng, H.-Y., Hung, S.-H., & Chu, P. (2015) · Cellular and Molecular Neurobiology · doi:10.1007/s10571-015-0259-6 · Cited by 6 · see citing works
Rahim, M. A., Thatipamula, S., Pasinetti, G. M., & Hossain, M. A. (2021) · ASN NEURO · doi:10.1177/17590914211012888 · Cited by 6 · see citing works
Self-citationHypoxia-ischemia and sexual dimorphism: modeling mitochondrial dysfunction using brain organoids
Gaston-Breton, R., Disdier, C., Hagberg, H., & Mabondzo, A. M. (2025) · Cell & Bioscience · doi:10.1186/s13578-025-01402-0 · Cited by 6 · see citing works
Sukhorukov, V. S., Baranich, T. I., Egorova, A. V., Fedorova, E. N., Андреевна, С. К., Алексеевич, Х. Д., & Krapivkin, A. I. (2024) · Rossiyskiy Vestnik Perinatologii i Pediatrii (Russian Bulletin of Perinatology and Pediatrics) · doi:10.21508/1027-4065-2024-69-1-25-33 · Cited by 4 · see citing works
Genotype and Sex Differences in Longevity in Transgenic Mouse Models of Alzheimer’s Disease
Brown, R. E., Shin, S., Woodland, N., & Rae, E. A. (2018) · Elsevier eBooks · doi:10.1016/b978-0-12-811353-0.00042-7 · Cited by 2 · see citing works
Xie, W., Wu, F., He, J., Chen, S., Chen, L., Zhang, X., Sun, J., Liu, X., & Tao, J. (2020) · Journal of Human Hypertension · doi:10.1038/s41371-020-0364-y · Cited by 2 · see citing works
Sex-specific differences in cerebral blood flow for athletes with a history of concussion
Hamer, J. (2018) · TSpace (University of Toronto)
Park, S.-H., & Yoon, J.-H. (2021) · Exercise Science · doi:10.15857/ksep.2021.30.2.249
Liu, R., Hao, S., Hou, D., Tian, H., Hong, W., Huang, H., & Duan, C. (2023) · Research Square · doi:10.21203/rs.3.rs-3210579/v1
Mitochondrial Dysfunction and Its Impact on Cellular Metabolism in Degenerative Diseases
Safi, S. Z. (2024) · Premier Journal of Neuroscience · doi:10.70389/pjn.100002
Systems biology approach in the detection of neuronal disorders
Rao, D., Yadav, S., Chandra, N., Muthamma, T., Sivamani, Y., Pokkuluri, K. S., & Elayaperumal, S. (2025) · Elsevier eBooks · doi:10.1016/b978-0-443-33351-4.00016-7
Nardast, S., Asadirad, A., Bavarsad, K., Sarkaki, A., Shojaei, A., & Ghafouri, S. (2026) · European Journal of Pharmacology · doi:10.1016/j.ejphar.2026.178551
Ghani, S. A., & Singh, L. (2026) · Molecular Biology Reports · doi:10.1007/s11033-026-12263-2
- Authors
- Sharma, J., Johnston, M. V., & Hossain, M. A.
- Affiliations
- Kennedy Krieger Institute (US)
- Corresponding author
- Hossain, Mir Ahamed
- ORCID
- Johnston, Michael V
- Venue
- BMC Neuroscience
- Published
- 2014-01-10
- Volume
- 15
- Issue
- 1
- Pages
- 9-9
- ISSN
- 1471-2202 (ISSN-L)
- PMC
- PMC3898007
- OpenAlex
- W2042796333
- Cited by
- 67
- References
- 46
- Citations by year
- 2026: 3 · 2025: 5 · 2024: 4 · 2023: 2 · 2022: 4 · 2021: 6 · 2020: 7 · 2019: 9 · 2018: 3 · 2017: 8 · 2016: 5 · 2015: 7 · 2014: 4
- FWCI
- 3.28
- Type
- journal article
- Language
- en
- Open access
- gold
- doi.org
- Licence
- cc-by
- Locations
- BMC Neuroscience (publishedVersion, cc-by)
- Europe PMC (PubMed Central) (publishedVersion, cc-by)
- PubMed Central (publishedVersion, cc-by)
- PubMed (publishedVersion)
- Funders
- National Institutes of Health
- National Institute of Neurological Disorders and Stroke (R01NS046030, R01NS028208)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Mitochondrial Function and Pathology
- Health Sciences › Medicine › Pediatrics, Perinatology and Child Health › Neonatal and fetal brain pathology
- Health Sciences › Medicine › Epidemiology › Autophagy in Disease and Therapy
- Keywords
- sex differences, mitochondrial biogenesis, oxygen-glucose deprivation, reoxygenation, neuronal cell death, cerebellar granule cells, mitochondrial DNA, TFAM, PGC-1α, mitochondrial fission and fusion, mitochondrial membrane potential, ATP depletion, hypoxic-ischemic brain injury, mitochondrial dysfunction
- MeSH terms
- Animals, Brain, Cell Survival, Female, Glucose, Male, Mitochondria, Neurons, Oxygen, Sex Factors, Apoptosis, Hypoxia-Ischemia, Brain, Mice, Mitochondrial Turnover
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