Neurogenesis, A Potential Target for Intermittent Hypoxia Leading to
Cognitive Decline

Yuxing      Liu; Jin      Tan; Yuyang      Miao; Qiang      Zhang
doi:10.2174/1574888X18666230330083206
Abstract

As a sleep breathing disorder, characterized by intermittent hypoxia (IH) and Obstructive sleep apnea (OSA), is believed to decrease the cognitive function of patients. Many factors are thought to be responsible for cognitive decline in OSA patients. Neurogenesis, a process by which neural stem cells (NSCs) differentiate into new neurons in the brain, is a major determinant affecting cognitive function. However, there is no clear relationship between IH or OSA and neurogenesis. In recent years, increasing numbers of studies on IH and neurogenesis are documented. Therefore, this review summarizes the effects of IH on neurogenesis; then discusses the influencing factors that may cause these effects and the potential signaling pathways that may exist. Finally, based on this impact, we discuss potential methods and future directions for improving cognition.
Keywords: Neurogenesis, intermittent hypoxia, obstructive sleep apnea, hippocampus, disorder, alzheimer's disease.
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[1]
Montagne A, Huuskonen MT, Rajagopal G, et al. Undetectable gadolinium brain retention in individuals with an age-dependent blood-brain barrier breakdown in the hippocampus and mild cognitive impairment. Alzheimers Dement  2019; 15(12): 1568-75.
 [http://dx.doi.org/10.1016/j.jalz.2019.07.012] [PMID: 31862169]

[2]
He B, Chen W, Zeng J, Tong W, Zheng P. MicroRNA‐326 decreases tau phosphorylation and neuron apoptosis through inhibition of the JNK signaling pathway by targeting VAV1 in Alzheimer’s disease. J Cell Physiol  2020; 235(1): 480-93.
 [http://dx.doi.org/10.1002/jcp.28988] [PMID: 31385301]

[3]
Richetin K, Steullet P, Pachoud M, et al. Tau accumulation in astrocytes of the dentate gyrus induces neuronal dysfunction and memory deficits in Alzheimer’s disease. Nat Neurosci  2020; 23(12): 1567-79.
 [http://dx.doi.org/10.1038/s41593-020-00728-x] [PMID: 33169029]

[4]
Cizeron M, Qiu Z, Koniaris B, et al. A brainwide atlas of synapses across the mouse life span. Science  2020; 369(6501): 270-5.
 [http://dx.doi.org/10.1126/science.aba3163] [PMID: 32527927]

[5]
Sahay A, Scobie KN, Hill AS, et al. Increasing adult hippocampal neurogenesis is sufficient to improve pattern separation. Nature  2011; 472(7344): 466-70.
 [http://dx.doi.org/10.1038/nature09817] [PMID: 21460835]

[6]
Choi SH, Bylykbashi E, Chatila ZK, et al. Combined adult neurogenesis and BDNF mimic exercise effects on cognition in an Alzheimer’s mouse model in sentence style. Science  2018; 361.

[7]
Rosenzweig I, Glasser M, Polsek D, Leschziner GD, Williams SCR, Morrell MJ. Sleep apnoea and the brain: A complex relationship. Lancet Respir Med  2015; 3(5): 404-14.
 [http://dx.doi.org/10.1016/S2213-2600(15)00090-9] [PMID: 25887982]

[8]
Nelson R. Obstructive sleep apnoea in children might impair cognition and behaviour. Lancet  2002; 359(9319): 1754.
 [http://dx.doi.org/10.1016/S0140-6736(02)08666-X] [PMID: 12049870]

[9]
Nair D, Zhang SXL, Ramesh V, et al. Sleep fragmentation induces cognitive deficits via nicotinamide adenine dinucleotide phosphate oxidase-dependent pathways in mouse. Am J Respir Crit Care Med  2011; 184(11): 1305-12.
 [http://dx.doi.org/10.1164/rccm.201107-1173OC] [PMID: 21868506]

[10]
Burckhardt IC, Gozal D, Dayyat E, et al. Green tea catechin polyphenols attenuate behavioral and oxidative responses to intermittent hypoxia. Am J Respir Crit Care Med  2008; 177(10): 1135-41.
 [http://dx.doi.org/10.1164/rccm.200701-110OC] [PMID: 18276944]

[11]
Rosenberg GA. Extracellular matrix inflammation in vascular cognitive impairment and dementia. Clin Sci  2017; 131(6): 425-37.
 [http://dx.doi.org/10.1042/CS20160604] [PMID: 28265034]

[12]
Cai XH, Li XC, Jin SW, et al. Endoplasmic reticulum stress plays critical role in brain damage after chronic intermittent hypoxia in growing rats. Exp Neurol  2014; 257: 148-56.
 [http://dx.doi.org/10.1016/j.expneurol.2014.04.029] [PMID: 24810321]

[13]
Khuu MA, Nallamothu T, Castro-Rivera CI, Arias-Cavieres A, Szujewski CC, Garcia AJ III. Stage-dependent effects of intermittent hypoxia influence the outcome of hippocampal adult neurogenesis. Sci Rep  2021; 11(1): 6005.
 [http://dx.doi.org/10.1038/s41598-021-85357-5] [PMID: 33727588]

[14]
Martin N, Bossenmeyer-Pourié C, Koziel V, et al. Non-injurious neonatal hypoxia confers resistance to brain senescence in aged male rats. PLoS One  2012; 7(11): e48828.
 [http://dx.doi.org/10.1371/journal.pone.0048828] [PMID: 23173039]

[15]
Tsai YW, Yang YR, Sun SH, Liang KC, Wang RY. Post ischemia intermittent hypoxia induces hippocampal neurogenesis and synaptic alterations and alleviates long-term memory impairment. J Cereb Blood Flow Metab  2013; 33(5): 764-73.
 [http://dx.doi.org/10.1038/jcbfm.2013.15] [PMID: 23443175]

[16]
Zhu XH, Yan HC, Zhang J, et al. Intermittent hypoxia promotes hippocampal neurogenesis and produces antidepressant-like effects in adult rats. J Neurosci  2010; 30(38): 12653-63.
 [http://dx.doi.org/10.1523/JNEUROSCI.6414-09.2010] [PMID: 20861371]

[17]
Meng SX, Wang B, Li WT. Intermittent hypoxia improves cognition and reduces anxiety‐related behavior in APP/PS1 mice. Brain Behav  2020; 10(2): e01513.
 [http://dx.doi.org/10.1002/brb3.1513] [PMID: 31877583]

[18]
Khuu MA, Pagan CM, Nallamothu T, et al. Intermittent hypoxia disrupts adult neurogenesis and synaptic plasticity in the dentate gyrus. J Neurosci  2019; 39(7): 1320-31.
 [http://dx.doi.org/10.1523/JNEUROSCI.1359-18.2018] [PMID: 30587544]

[19]
Wu X, Lu H, Hu L, et al. Chronic intermittent hypoxia affects endogenous serotonergic inputs and expression of synaptic proteins in rat hypoglossal nucleus. Am J Transl Res  2017; 9(2): 546-57.
 [PMID: 28337282]

[20]
Gozal D, Row BW, Gozal E, et al. Temporal aspects of spatial task performance during intermittent hypoxia in the rat: Evidence for neurogenesis. Eur J Neurosci  2003; 18(8): 2335-42.
 [http://dx.doi.org/10.1046/j.1460-9568.2003.02947.x] [PMID: 14622195]

[21]
Cha J, Zea-Hernandez JA, Sin S, et al. The effects of obstructive sleep apnea syndrome on the dentate gyrus and learning and memory in children. J Neurosci  2017; 37(16): 4280-8.
 [http://dx.doi.org/10.1523/JNEUROSCI.3583-16.2017] [PMID: 28320844]

[22]
Canessa N, Castronovo V, Cappa SF, et al. Obstructive sleep apnea: Brain structural changes and neurocognitive function before and after treatment. Am J Respir Crit Care Med  2011; 183(10): 1419-26.
 [http://dx.doi.org/10.1164/rccm.201005-0693OC] [PMID: 21037021]

[23]
Bi XY, Wang TS, Zhang M, Liu QQ, Li WB, Zhang Y. The up-regulation of p-p38 MAPK during the induction of brain ischemic tolerance induced by intermittent hypobaric hypoxia preconditioning in rats. Chung Kuo Ying Yung Sheng Li Hsueh Tsa Chih  2014; 30(2): 97-100.
 [PMID: 25016855]

[24]
Zhu L, Zhao T, Li H, et al. Neurogenesis in the adult rat brain after intermittent hypoxia. Brain Res  2005; 1055(1-2): 1-6.
 [http://dx.doi.org/10.1016/j.brainres.2005.04.075] [PMID: 16098951]

[25]
Bartlett D, Rae C, Thompson C, et al. Hippocampal area metabolites relate to severity and cognitive function in obstructive sleep apnea. Sleep Med  2004; 5(6): 593-6.
 [http://dx.doi.org/10.1016/j.sleep.2004.08.004] [PMID: 15511707]

[26]
Wall AM, Corcoran AE, O’Halloran KD, O’Connor JJ. Effects of prolyl-hydroxylase inhibition and chronic intermittent hypoxia on synaptic transmission and plasticity in the rat CA1 and dentate gyrus. Neurobiol Dis  2014; 62: 8-17.
 [http://dx.doi.org/10.1016/j.nbd.2013.08.016] [PMID: 24055213]

[27]
Reeves SR, Guo SZ, Brittian KR, Row BW, Gozal D. Anatomical changes in selected cardio-respiratory brainstem nuclei following early post-natal chronic intermittent hypoxia. Neurosci Lett  2006; 402(3): 233-7.
 [http://dx.doi.org/10.1016/j.neulet.2006.04.013] [PMID: 16697524]

[28]
Kjell J, Fischer-Sternjak J, Thompson AJ, et al. Defining the adult neural stem cell niche proteome identifies key regulators of adult neurogenesis. Cell Stem Cell  2020; 26(2): 277-93.
 [http://dx.doi.org/10.1016/j.stem.2020.01.002] [PMID: 32032526]

[29]
Ernst A, Alkass K, Bernard S, et al. Neurogenesis in the striatum of the adult human brain. Cell  2014; 156(5): 1072-83.
 [http://dx.doi.org/10.1016/j.cell.2014.01.044] [PMID: 24561062]

[30]
Prabhakar NR, Semenza GL. Adaptive and maladaptive cardiorespiratory responses to continuous and intermittent hypoxia mediated by hypoxia-inducible factors 1 and 2. Physiol Rev  2012; 92(3): 967-1003.
 [http://dx.doi.org/10.1152/physrev.00030.2011] [PMID: 22811423]

[31]
Wu X, Gong L, Xie L, et al. NLRP3 deficiency protects against intermittent hypoxia-induced neuroinflammation and mitochondrial ROS by promoting the PINK1-parkin pathway of mitophagy in a murine model of sleep apnea. Front Immunol  2021; 12: 628168.
 [http://dx.doi.org/10.3389/fimmu.2021.628168] [PMID: 33717152]

[32]
Jung ME, Simpkins JW, Wilson AM, et al. Intermittent hypoxia conditioning prevents behavioral deficit and brain oxidative stress in ethanol-withdrawn rats in sentence style. J Appl Physiol  1985; 2008(105): 510-7.

[33]
Kang JJ, Guo B, Liang WH, et al. Daily acute intermittent hypoxia induced dynamic changes in dendritic mitochondrial ultrastructure and cytochrome oxidase activity in the pre-Bötzinger complex of rats. Exp Neurol  2019; 313: 124-34.
 [http://dx.doi.org/10.1016/j.expneurol.2018.12.008] [PMID: 30586594]

[34]
Kang JJ, Fung ML, Zhang K, et al. Chronic intermittent hypoxia alters the dendritic mitochondrial structure and activity in the pre‐Bötzinger complex of rats. FASEB J  2020; 34(11): 14588-601.
 [http://dx.doi.org/10.1096/fj.201902141R] [PMID: 32910512]

[35]
Sapin E, Peyron C, Roche F, et al. Chronic intermittent hypoxia induces chronic low-grade neuroinflammation in the dorsal hippocampus of mice. Sleep  2015; 38(10): 1537-46.
 [http://dx.doi.org/10.5665/sleep.5042] [PMID: 26085297]

[36]
Willis EF, MacDonald KPA, Nguyen QH, et al. Repopulating microglia promote brain repair in an IL-6-dependent manner. Cell  2020; 180(5): 833-846.e16.
 [http://dx.doi.org/10.1016/j.cell.2020.02.013] [PMID: 32142677]

[37]
Lam CS, Tipoe GL, So KF, Fung ML. Neuroprotective mechanism of Lycium barbarum polysaccharides against hippocampal-dependent spatial memory deficits in a rat model of obstructive sleep apnea. PLoS One  2015; 10(2): e0117990.
 [http://dx.doi.org/10.1371/journal.pone.0117990] [PMID: 25714473]

[38]
Hirota Y, Sawada M, Huang S, et al. Roles of wnt signaling in the neurogenic niche of the adult mouse ventricular–subventricular zone. Neurochem Res  2016; 41(1-2): 222-30.
 [http://dx.doi.org/10.1007/s11064-015-1766-z] [PMID: 26572545]

[39]
Ortiz-Matamoros A, Salcedo-Tello P, Avila-Muñoz E, Zepeda A, Arias C. Role of wnt signaling in the control of adult hippocampal functioning in health and disease: Therapeutic implications. Curr Neuropharmacol  2013; 11(5): 465-76.
 [http://dx.doi.org/10.2174/1570159X11311050001] [PMID: 24403870]

[40]
L’Episcopo F, Tirolo C, Testa N, et al. 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/β-catenin signaling pathways: Functional consequences for neuroprotection and repair. J Neurosci  2012; 32(6): 2062-85.
 [http://dx.doi.org/10.1523/JNEUROSCI.5259-11.2012] [PMID: 22323720]

[41]
L’Episcopo F, Tirolo C, Testa N, et al. Wnt/β-catenin signaling is required to rescue midbrain dopaminergic progenitors and promote neurorepair in ageing mouse model of Parkinson’s disease. Stem Cells  2014; 32(8): 2147-63.
 [http://dx.doi.org/10.1002/stem.1708] [PMID: 24648001]

[42]
Sun C, Fu J, Qu Z, et al. Chronic intermittent hypobaric hypoxia restores hippocampus function and rescues cognitive impairments in chronic epileptic rats via Wnt/β-catenin signaling. Front Mol Neurosci  2021; 13: 617143.
 [http://dx.doi.org/10.3389/fnmol.2020.617143] [PMID: 33584201]

[43]
Pan YY, Deng Y, Xie S, et al. Altered wnt signaling pathway in cognitive impairment caused by chronic intermittent hypoxia. Chin Med J  2016; 129(7): 838-45.
 [http://dx.doi.org/10.4103/0366-6999.178969] [PMID: 26996481]

[44]
Erickson KI, Voss MW, Prakash RS, et al. Exercise training increases size of hippocampus and improves memory. Proc Natl Acad Sci  2011; 108(7): 3017-22.
 [http://dx.doi.org/10.1073/pnas.1015950108] [PMID: 21282661]

[45]
Bhattarai P, Cosacak MI, Mashkaryan V, et al. Neuron-glia interaction through Serotonin-BDNF-NGFR axis enables regenerative neurogenesis in Alzheimer’s model of adult zebrafish brain. PLoS Biol  2020; 18(1): e3000585.
 [http://dx.doi.org/10.1371/journal.pbio.3000585] [PMID: 31905199]

[46]
Kushwah N, Jain V, Deep S, Prasad D, Singh SB, Khan N. Neuroprotective role of intermittent hypobaric hypoxia in unpredictable chronic mild stress induced depression in rats. PLoS One  2016; 11(2): e0149309.
 [http://dx.doi.org/10.1371/journal.pone.0149309] [PMID: 26901349]

[47]
Zhang K, Zhao T, Huang X, et al. Notch1 mediates postnatal neurogenesis in hippocampus enhanced by intermittent hypoxia. Neurobiol Dis  2014; 64: 66-78.
 [http://dx.doi.org/10.1016/j.nbd.2013.12.010] [PMID: 24368168]

[48]
Ross HH, Sandhu MS, Cheung TF, et al. In Vivo intermittent hypoxia elicits enhanced expansion and neuronal differentiation in cultured neural progenitors. Exp Neurol  2012; 235(1): 238-45.
 [http://dx.doi.org/10.1016/j.expneurol.2012.01.027] [PMID: 22366327]

[49]
Schoenfeld TJ, McCausland HC, Morris HD, Padmanaban V, Cameron HA. Stress and loss of adult neurogenesis differentially reduce hippocampal volume. Biol Psychiatry  2017; 82(12): 914-23.
 [http://dx.doi.org/10.1016/j.biopsych.2017.05.013] [PMID: 28629541]

[50]
Musso MF, Lindsey HM, Wilde EA, et al. Volumetric brain magnetic resonance imaging analysis in children with obstructive sleep apnea. Int J Pediatr Otorhinolaryngol  2020; 138: 110369.
 [http://dx.doi.org/10.1016/j.ijporl.2020.110369] [PMID: 32927352]

[51]
Macey PM, Henderson LA, Macey KE, et al. Brain morphology associated with obstructive sleep apnea. Am J Respir Crit Care Med  2002; 166(10): 1382-7.
 [http://dx.doi.org/10.1164/rccm.200201-050OC] [PMID: 12421746]

[52]
Huang X, Tang S, Lyu X, Yang C, Chen X. Structural and functional brain alterations in obstructive sleep apnea: A multimodal meta-analysis. Sleep Med  2019; 54: 195-204.
 [http://dx.doi.org/10.1016/j.sleep.2018.09.025] [PMID: 30580194]

[53]
Torelli F, Moscufo N, Garreffa G, et al. Cognitive profile and brain morphological changes in obstructive sleep apnea. Neuroimage  2011; 54(2): 787-93.
 [http://dx.doi.org/10.1016/j.neuroimage.2010.09.065] [PMID: 20888921]

[54]
Owen JE, Benediktsdottir B, Cook E, Olafsson I, Gislason T, Robinson SR. Alzheimer’s disease neuropathology in the hippocampus and brainstem of people with obstructive sleep apnea. Sleep  2021; 44(3): zsaa195.
 [http://dx.doi.org/10.1093/sleep/zsaa195]

[55]
Cross NE, Memarian N, Duffy SL, et al. Structural brain correlates of obstructive sleep apnoea in older adults at risk for dementia in sentence style. Eur Respir J  2018; 52.

[56]
Yang L, Zhao J, Qu Y, et al. Metoprolol prevents neuronal dendrite remodeling in a canine model of chronic obstructive sleep apnea. Acta Pharmacol Sin  2020; 41(5): 620-8.
 [http://dx.doi.org/10.1038/s41401-019-0323-8] [PMID: 31863057]

[57]
An JR, Zhao YS, Luo LF, Guan P, Tan M. Ji ES. Huperzine A, reduces brain iron overload and alleviates cognitive deficit in mice exposed to chronic intermittent hypoxia. Life Sci  2020; 250: 117573.
 [http://dx.doi.org/10.1016/j.lfs.2020.117573] [PMID: 32209423]

[58]
Yin X, Zhang X, Lv C, et al. Protocatechuic acid ameliorates neurocognitive functions impairment induced by chronic intermittent hypoxia. Sci Rep  2015; 5(1): 14507.
 [http://dx.doi.org/10.1038/srep14507] [PMID: 26419512]

[59]
Xie H, Leung KL, Chen L, et al. Brain-derived neurotrophic factor rescues and prevents chronic intermittent hypoxia-induced impairment of hippocampal long-term synaptic plasticity. Neurobiol Dis  2010; 40(1): 155-62.
 [http://dx.doi.org/10.1016/j.nbd.2010.05.020] [PMID: 20553872]

[60]
Zigova T, Pencea V, Wiegand SJ, Luskin MB. Intraventricular administration of BDNF increases the number of newly generated neurons in the adult olfactory bulb. Mol Cell Neurosci  1998; 11(4): 234-45.
 [http://dx.doi.org/10.1006/mcne.1998.0684] [PMID: 9675054]

[61]
Takeshima Y, Nakamura M, Miyake H, et al. Neuroprotection with intraventricular brain-derived neurotrophic factor in rat venous occlusion model. Neurosurgery  2011; 68(5): 1334-41.
 [http://dx.doi.org/10.1227/NEU.0b013e31820c048e] [PMID: 21307800]

[62]
Maresky HS, Shpirer I, Klar MM, Levitt M, Sasson E, Tal S. Continuous positive airway pressure alters brain microstructure and perfusion patterns in patients with obstructive sleep apnea. Sleep Med  2019; 57: 61-9.
 [http://dx.doi.org/10.1016/j.sleep.2018.12.027] [PMID: 30897457]

[63]
Orrù G, Storari M, Scano A, Piras V, Taibi R, Viscuso D. Obstructive sleep apnea, oxidative stress, inflammation and endothelial dysfunction-An overview of predictive laboratory biomarkers. Eur Rev Med Pharmacol Sci  2020; 24(12): 6939-48.
 [PMID: 32633387]

[64]
Sharma D, Maslov LN, Singh N, Jaggi AS. Remote ischemic preconditioning-induced neuroprotection in cerebral ischemia-reperfusion injury: Preclinical evidence and mechanisms. Eur J Pharmacol  2020; 883: 173380.
 [http://dx.doi.org/10.1016/j.ejphar.2020.173380] [PMID: 32693098]

[65]
Mieszkowski J, Stankiewicz B, Kochanowicz A, et al. Remote ischemic preconditioning reduces marathon-induced oxidative stress and decreases liver and heart injury markers in the serum. Front Physiol  2021; 12: 731889.
 [http://dx.doi.org/10.3389/fphys.2021.731889] [PMID: 34552508]

[66]
Bouslama M, Adla-Biassette H, Ramanantsoa N, et al. Protective effects of intermittent hypoxia on brain and memory in a mouse model of apnea of prematurity. Front Physiol  2015; 6: 313.
 [http://dx.doi.org/10.3389/fphys.2015.00313] [PMID: 26582992]

[67]
Tsai YW, Yang YR, Wang PS, Wang RY. Intermittent hypoxia after transient focal ischemia induces hippocampal neurogenesis and c-Fos expression and reverses spatial memory deficits in rats. PLoS One  2011; 6(8): e24001.
 [http://dx.doi.org/10.1371/journal.pone.0024001] [PMID: 21887361]

[68]
Ross HH, Sandhu MS, Sharififar S, Fuller DD. Delivery of in vivo Acute Intermittent Hypoxia in Neonatal Rodents to Prime Subventricular Zone-derived Neural Progenitor Cell Cultures. J Vis Exp  2015; (105): e52527.
 [PMID: 26556530]

[69]
Ding FS, Cheng X, Zhao T, et al. Intermittent hypoxic preconditioning relieves fear and anxiety behavior in post-traumatic stress model mice. Sheng Li Xue Bao  2019; 71(4): 537-46.
 [PMID: 31440750]

[70]
Baker-Herman TL, Fuller DD, Bavis RW, et al. BDNF is necessary and sufficient for spinal respiratory plasticity following intermittent hypoxia. Nat Neurosci  2004; 7(1): 48-55.
 [http://dx.doi.org/10.1038/nn1166] [PMID: 14699417]

[71]
Huang YJ, Yuan YJ, Liu YX, et al. Nitric oxide participates in the brain ischemic tolerance induced by intermittent hypobaric hypoxia in the hippocampal CA1 subfield in rats. Neurochem Res  2018; 43(9): 1779-90.
 [http://dx.doi.org/10.1007/s11064-018-2593-9] [PMID: 29995175]

[72]
Rybnikova E, Sitnik N, Gluschenko T, Tjulkova E, Samoilov MO. The preconditioning modified neuronal expression of apoptosis-related proteins of Bcl-2 superfamily following severe hypobaric hypoxia in rats. Brain Res  2006; 1089(1): 195-202.
 [http://dx.doi.org/10.1016/j.brainres.2006.03.053] [PMID: 16638610]

[73]
Yue W, Cunlin G, Lu H, Yuanqing Z, Yanjun T, Qiong W. Neuroprotective effect of intermittent hypobaric hypoxia preconditioning on cerebral ischemia/reperfusion in rats. Int J Clin Exp Pathol  2020; 13(11): 2860-9.
 [PMID: 33284899]

[74]
Zhen J, Wang W, Zhou J, et al. Chronic intermittent hypoxic preconditioning suppresses pilocarpine-induced seizures and associated hippocampal neurodegeneration. Brain Res  2014; 1563: 122-30.
 [http://dx.doi.org/10.1016/j.brainres.2014.03.032] [PMID: 24680745]

[75]
Das T, Soren K, Yerasi M, Kamle A, Kumar A, Chakravarty S. Molecular basis of sex difference in neuroprotection induced by hypoxia preconditioning in Zebrafish. Mol Neurobiol  2020; 57(12): 5177-92.
 [http://dx.doi.org/10.1007/s12035-020-02091-1] [PMID: 32862360]

[76]
Wu Q, Yu KX, Ma QS, Liu YN. Effects of intermittent hypobaric hypoxia preconditioning on the expression of neuroglobin and Bcl-2 in the rat hippocampal CA1 area following ischemia-reperfusion. Genet Mol Res  2015; 14(3): 10799-807.
 [http://dx.doi.org/10.4238/2015.September.9.18] [PMID: 26400308]
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DOI https://dx.doi.org/10.2174/1574888X18666230330083206	Print ISSN 1574-888X
Publisher Name Bentham Science Publisher	Online ISSN 2212-3946
Current Stem Cell Research & Therapy

Neurogenesis, A Potential Target for Intermittent Hypoxia Leading to Cognitive Decline

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