Recovery of Human Embryonic Stem Cells-Derived Neural Progenitors Exposed to Hypoxic-Ischemic-Reperfusion Injury by Indirect Exposure to Wharton's Jelly Mesenchymal Stem Cells Through Phosphatidyl-inositol-3-Kinase Pathway.

Glial progenitor population In vitro HIE model Intracellular calcium Migration potential Oxidative stress susceptibility Oxygen glucose deprivation and reperfusion PSA-NCAM Proliferation Umbilical cord-derived MSCs

Journal

Cellular and molecular neurobiology
ISSN: 1573-6830
Titre abrégé: Cell Mol Neurobiol
Pays: United States
ID NLM: 8200709

Informations de publication

Date de publication:
May 2022
Historique:
received: 04 08 2020
accepted: 11 11 2020
pubmed: 19 11 2020
medline: 2 4 2022
entrez: 18 11 2020
Statut: ppublish

Résumé

Increasing evidence suggests that mesenchymal stem cells(MSCs) have beneficial effects in hypoxic ischemic reperfusion injury, but the underlying mechanisms are unclear. Here, we first examined the effect of OGD reperfusion injury on the vulnerability of human NPs derived from human embryonic stem cells (hESCs) with regard to cell survival and oxidative stress. Cellular deregulation was assessed by measuring glutathione levels, basal calcium and intracellular calcium [Ca

Identifiants

pubmed: 33206286
doi: 10.1007/s10571-020-01007-w
pii: 10.1007/s10571-020-01007-w
doi:

Substances chimiques

Inositol 4L6452S749
Phosphatidylinositol 3-Kinase EC 2.7.1.137

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Pagination

1167-1188

Subventions

Organisme : Council for Science and Industrial Research
ID : 37/(1614)/13/EMR-II

Informations de copyright

© 2020. Springer Science+Business Media, LLC, part of Springer Nature.

Références

AbdelAziz NH, AbdelAzeem HG, Monazea EM, Sherif T (2017) Impact of thrombophilia on the risk of hypoxic-ischemic encephalopathy in term neonates. ClinApplThrombHemost 23(3):266–273
Ahn SY, Chang YS, Sung DK, Sung SI, Park WS (2018) Hypothermia broadens the therapeutic time window of mesenchymal stem cell transplantation for severe neonatal hypoxic ischemic encephalopathy. Sci Rep 8(1):7665
pubmed: 29769612 pmcid: 5955959
Arteaga O, Revuelta M, Urigüen L, Alvarez A, Montalvo H, Hilario E (2015) Pretreatment with resveratrol prevents neuronal injury and cognitive deficits induced by perinatal hypoxia-ischemia in rats. PLoS One 10(11). https://doi.org/10.1371/journal.pone.0142424
Azzopardi D, Strohm B, Marlow N, Brocklehurst P, Deierl A, Eddama O (2014) Effects of hypothermia for perinatal asphyxia on childhood outcomes. N Engl J Med 371(2):140–149. https://doi.org/10.1056/NEJMoa1315788
doi: 10.1056/NEJMoa1315788 pubmed: 25006720
Back SA, Gan X, Li Y, Rosenberg PA, Volpe JJ (1998) Maturation-dependent vulnerability of oligodendrocytes to oxidative stress-induced death caused by glutathione depletion. J Neurosci 18(16):6241–6253
pubmed: 9698317 pmcid: 6793198
Baldoli C, Scola E, Della Rosa PA, Pontesilli S, Longaretti R, Poloniato A (2015) Maturation of preterm newborn brains: a fMRI-DTI study of auditory processing of linguistic stimuli and white matter development. Brain StructFunct 220(6):3733–3751. https://doi.org/10.1007/s00429-014-0887-5
doi: 10.1007/s00429-014-0887-5
Buser JR, Maire J, Riddle A et al (2012) Arrested preoligodendrocyte maturation contributes to myelination failure in premature infants. Ann Neurol 71(1):93–109
pubmed: 22275256 pmcid: 3270934
Cameron SH, Alwakeel AJ, Goddard L, Hobbs CE, Gowing EK, Barnett ER (2015) Delayed post-treatment with bone marrow-derived mesenchymal stem cells is neurorestorative of striatal medium-spiny projection neurons and improves motor function after neonatal rat hypoxia–ischemia. Mol Cell Neurosci 68:56–72
pubmed: 25828540
Cantley LC (2002) The phosphoinositide 3‐kinase pathway. Science 296:1655–1657
Cavalleri F, Lugli L, Pugliese M, D’Amico R, Todeschini A, Della Casa E (2014) Prognostic value of diffusion-weighted imaging summation scores or apparent diffusion coefficient maps in newborns with hypoxic-ischemic encephalopathy. PediatrRadiol 44(9):1141–1154. https://doi.org/10.1007/s00247-014-2945-9
doi: 10.1007/s00247-014-2945-9
Cheng X, Yeung PK, Zhong K, Zilundu PL, Zhou L, Chung SK (2019) Astrocytic endothelin-1 overexpression promotes neural progenitor cells proliferation and differentiation into astrocytes via the Jak2/Stat3 pathway after stroke. J Neuroinflammation 16(1):227
pubmed: 31733648 pmcid: 6858703
Choi N-Y, Kim JY, Hwang M, Lee E-H, Choi H, Lee K-Y (2019) Atorvastatin rejuvenates neural stem cells injured by oxygen-glucose deprivation and induces neuronal differentiation through activating the PI3K/Akt and ERK pathways. MolNeurobiol 56(4):2964–2977
Colleoni S, Galli C, Gaspar JA et al (2012) Characterization of a neural teratogenicity assay based on human ESCs differentiation following exposure to valproic acid. Curr Med Chem 19(35):6065–6071
pubmed: 23061626
Craig A, Ling Luo N, Beardsley DJ et al (2003) Quantitative analysis of perinatal rodent oligodendrocyte lineage progression and its correlation with human. ExpNeurol 181:231–240
Cunningham CJ, Redondo-Castro E, Allan SM (2018) The therapeutic potential of the mesenchymal stem cell secretome in ischaemic stroke. J Cereb Blood Flow Metab 38(8):1276–1292. https://doi.org/10.1177/0271678X18776802
doi: 10.1177/0271678X18776802 pubmed: 29768965 pmcid: 6077926
Datta I, Mishra S, Mohanty L, Pulikkot S, Joshi PG (2011) Neuronal plasticity of human Wharton’s jelly mesenchymal stromal cells to the dopaminergic cell type compared with human bone marrow mesenchymal stromal cells. Cytotherapy 13(8):918–932. https://doi.org/10.3109/14653249.2011.5799[pii]57S1465-3249(11)70573-4
doi: 10.3109/14653249.2011.5799[pii]57S1465-3249(11)70573-4 pubmed: 21696238
Datta I, Ganapathy K, Tattikota SM, Bhonde R (2013) Directed differentiation of human embryonic stem cell-line HUES9 to dopaminergic neurons in a serum-free defined culture niche. Cell BiolInt 37(1):54–64. https://doi.org/10.1002/cbin.10012
doi: 10.1002/cbin.10012
Datta I, Ganapathy K, Razdan R, Bhonde R (2018) Location and number of astrocytes determine dopaminergic neuron survival and function under 6-ohda stress mediated through differential BDNF release. MolNeurobiol 55(7):5505–5525. https://doi.org/10.1007/s12035-017-0767-0
doi: 10.1007/s12035-017-0767-0
Datta I, Jagtap S, Potdar C, Yadav R, Pal P (2020) Generation of induced pluripotent stem cells (NIMHi001-A) from a Parkinson's disease patient of East Indian ethnicity carrying LRRK2 I1371V variant. Stem Cell Res. https://doi.org/10.1016/j.scr.2020.101768
Davidson JO, Wassink G, van den Heuij LG, Bennet L, Gunn AJ (2015) Therapeutic hypothermia for neonatal hypoxic–ischemic encephalopathy–where to from here? Front Neurol 6:198
pubmed: 26441818 pmcid: 4568393
Donega V, van Velthoven CT, Nijboer CH, van Bel F, Kas MJ, Kavelaars A (2013) Intranasal mesenchymal stem cell treatment for neonatal brain damage: long-term cognitive and sensorimotor improvement. PLoS ONE 8(1):e51253
pubmed: 23300948 pmcid: 3536775
Donega V, Nijboer CH, van Tilborg G, Dijkhuizen RM, Kavelaars A, Heijnen CJ (2014) Intranasally administered mesenchymal stem cells promote a regenerative niche for repair of neonatal ischemic brain injury. ExpNeurol 261:53–64
Duprat F, Lesage F, Fink M et al (1997) TASK, a human background K+ channel to sense external pH variations near physiological pH. EMBO J 16(17):5464–5471. https://doi.org/10.1093/emboj/16.17.5464
Ebner S, Dunbar M, McKinnon RD (2000) Distinct roles for PI3K in proliferation and survival of oligodendrocyte progenitor cells. J Neurosci Res 62(3):336–345
pubmed: 11054802
Fang C-z, Yang Y-j, Wang Q-h, Yao Y, Zhang X-y, He X-h (2013) Intraventricular injection of human dental pulp stem cells improves hypoxic-ischemic brain damage in neonatal rats. PLoS One, 8(6). https://doi.org/10.1371/journal.pone.0066748
Ganapathy K, Datta I, Sowmithra S, Joshi P, Bhonde R (2016) Influence of 6-Hydroxydopamine Toxicity on alpha-Synuclein phosphorylation, resting vesicle expression, and vesicular dopamine release. J Cell Biochem 117(12):2719–2736. https://doi.org/10.1002/jcb.25570
doi: 10.1002/jcb.25570 pubmed: 27064513
Gerner GJ, Newman EI, Burton VJ, Roman B, Cristofalo EA, Leppert M (2019) Correlation between white matter injury identified by neonatal diffusion tensor imaging and neurodevelopmental outcomes following term neonatal asphyxia and therapeutic hypothermia: an exploratory pilot study. J Child Neurol 34(10):556–566. https://doi.org/10.1177/0883073819841717
doi: 10.1177/0883073819841717 pubmed: 31070085 pmcid: 7318916
Goldstein SA, Bockenhauer D, O’Kelly I, Zilberberg N (2001) Potassium leak channels and the KCNK family of two-P-domain subunits. Nat Rev Neurosci 2(3):175–184
pubmed: 11256078
Gonzalez-Perez O, Romero-Rodriguez R, Soriano-Navarro M, Garcia-Verdugo JM, Alvarez-Buylla A (2009) Epidermal growth factor induces the progeny of subventricular zone type B cells to migrate and differentiate into oligodendrocytes. Stem Cells 27(8):2032–2043
pubmed: 19544429 pmcid: 3346259
Gorlach A, Bertram K, Hudecova S, Krizanova O (2015) Calcium and ROS: A mutual interplay. Redox Biol 6:260–271
pubmed: 26296072 pmcid: 4556774
Grynkiewicz G, Poenie M, Tsien RY (1985) A new generation of Ca2+ indicators with greatly improved fluorescence properties. J BiolChem 260(6):3440–3450
Guan F, Wang X, He F (2015) Promotion of cell migration by neural cell adhesion molecule (NCAM) is enhanced by PSA in a polysialyltransferase-specific manner. PLoS One 10(4). https://doi.org/10.1371/journal.pone.0124237
Hofer HR, Tuan RS (2016) Secreted trophic factors of mesenchymal stem cells support neurovascular and musculoskeletal therapies. Stem Cell Res Ther 7(1):131. https://doi.org/10.1186/s13287-016-0394-0
Hsieh JY, Wang HW, Chang SJ, Liao KH, Lee IH, Lin WS (2013) Mesenchymal stem cells from human umbilical cord express preferentially secreted factors related to neuroprotection, neurogenesis, and angiogenesis. PLoS ONE 8(8):e72604
pubmed: 23991127 pmcid: 3749979
Huang EJ, Reichardt LF (2003) Trk receptors: roles in neuronal signal transduction. Annu Rev Biochem 72(1):609–642
pubmed: 12676795
Hughes S, Foster RG, Peirson SN, Hankins MW (2017) Expression and localisation of two-pore domain (K2P) background leak potassium ion channels in the mouse retina. Sci Rep 7:46085
pubmed: 28443635 pmcid: 5405414
Ives HE, Daniel TO (1987) Interrelationship between growth factor-induced pH changes and intracellular Ca2+. ProcNatlAcadSci 84(7):1950–1954
Jacobs SE, Berg M, Hunt R, Tarnow-Mordi WO, Inder TE, Davis PG (2013) Cooling for newborns with hypoxic ischaemic encephalopathy. Cochrane Database Syst Rev (1). doi: https://doi.org/10.1002/14651858.CD003311.pub3
Janelidze S, Hu BR, Siesjo P, Siesjo BK (2001) Alterations of akt1 (pkbalpha) and p70 (s6k) in transient focal ischemia. Neurobiol Dis 8:147–154
Kamal MM, Kassem DH (2020) Therapeutic potential of Wharton’s jelly mesenchymal stem cells for diabetes: achievements and challenges. Front Cell Dev Biol 8. https://doi.org/10.3389/fcell.2020.00016
Kaneko Y, Tajiri N, Su TP, Wang Y, Borlongan CV (2012) Combination treatment of hypothermia and mesenchymal stromal cells amplifies neuroprotection in primary rat neurons exposed to hypoxic-ischemic-like injury in vitro: role of the opioid system. PLoS ONE 7(10):e47583
pubmed: 23077646 pmcid: 3471862
Kang D, Kim D (2004) Single-channel properties and pH sensitivity of two-pore domain K+ channels of the TALK family. BiochemBiophys Res Commun 315(4):836–844
Kang SM, Cho MS, Seo H, Yoon CJ, Oh SK, Choi YM (2007) Efficient induction of oligodendrocytes from human embryonic stem cells. Stem Cells 25(2):419–424
pubmed: 17053214
Katakowski M, Zhang ZG, Chen J, Zhang R, Wang Y, Jiang H (2003) Phosphoinositide 3-kinase promotes adult subventricularneuroblast migration after stroke. J Neurosci Res 74(4):494–501
pubmed: 14598293
Katso R, Okkenhaug K, Ahmadi K, White S, Timms J, Waterfield MD (2001) Cellular function of phosphoinositide 3-kinases: implications for development, homeostasis, and cancer. Annu Rev Cell Dev Biol 17:615–675
pubmed: 11687500
Kemp P, Peers C, Lewis A, Miller P (2004) Regulation of recombinant human brain tandem P domain K+ channels by hypoxia: a role for O
pubmed: 15090259 pmcid: 6740131
Kido J, Matsumoto T (2016) Neural stem and progenitor cells with high proliferation potential in injured areas in a model of neonatal hypoxic-ischemic encephalopathy. J NeurolNeurophysiol 7(1):1–8
Koh S-H, Lo EH (2015) The role of the PI3K pathway in the regeneration of the damaged brain by neural stem cells after cerebral infarction. J ClinNeurol 11(4):297–304
Kurozumi K, Nakamura K, Tamiya T, Kawano Y, Ishii K, Kobune M (2005) Mesenchymal stem cells that produce neurotrophic factors reduce ischemic damage in the rat middle cerebral artery occlusion model. MolTher 11(1):96–104
Lee KY, Koh SH, Noh MY, Kim SH, Lee YJ (2008) Phosphatidylinositol‐3‐kinase activation blocks amyloid beta‐induced neurotoxicity. Toxicology 243:43–50
Li J, Dai G, Cheng YB, Qi X, Geng MY (2011) Polysialylation promotes neural cell adhesion molecule-mediated cell migration in a fibroblast growth factor receptor-dependent manner, but independent of adhesion capability. Glycobiology 21(8):1010–1018
pubmed: 21367877
Li R, Li X, Wu H, Yang Z, Fei L, Zhu J (2019) Theaflavin attenuates cerebral ischemia/reperfusion injury by abolishing miRNA-128-3p-mediated Nrf2 inhibition and reducing oxidative stress. Mol Med Rep 20(6):4893–4904
pubmed: 31638230 pmcid: 6854549
Lin S, Fan L-W, Pang Y, Rhodes PG, Mitchell HJ, Cai Z (2005) IGF-1 protects oligodendrocyte progenitor cells and improves neurological functions following cerebral hypoxia–ischemia in the neonatal rat. Brain Res 1063(1):15–26
pubmed: 16259966
Lorek A, Takei Y, Cady E, Wyatt J, Penrice J, Edwards A (1994) Delayed (“secondary”) cerebral energy failure after acute hypoxia-ischemia in the newborn piglet: continuous 48-hour studies by phosphorus magnetic resonance spectroscopy. Pediatr Res 36(6):699–706
pubmed: 7898977
Lukovic D, DiezLloret A, Stojkovic P, Rodríguez-Martínez D, Perez Arago MA, Rodriguez-Jimenez FJ (2017) Highly efficient neural conversion of human pluripotent stem cells in adherent and animal-free conditions. Stem Cells Transl Med 6(4):1217–1226
pubmed: 28213969 pmcid: 5442830
Majumdar D, Bhonde R, Datta I (2013) Influence of ischemic microenvironment on human Wharton’s Jelly mesenchymal stromal cells. Placenta 34(8):642–649
pubmed: 23702186
Mattiesen WR, Tauber SC, Gerber J et al (2009) Increased neurogenesis after hypoxic-ischemic encephalopathy in humans is age related. ActaNeuropathol 117(5):525–534
Matsuoka H, Inoue M (2015) Src mediates endocytosis of TWIK-related acid-sensitive K+ 1 channels in PC12 cells in response to nerve growth factor. Am J Physiol-Cell Physiol 309(4):C251–C263
pubmed: 26084307
Minich T, Riemer J, Schulz JB, Wielinga P, Wijnholds J, Dringen R (2006) The multidrug resistance protein 1 (Mrp1), but not Mrp5, mediates export of glutathione and glutathione disulfide from brain astrocytes. J Neurochem 97(2):373–384
pubmed: 16539673
Mukai T, Tojo A, Nagamura-Inoue T (2018) Umbilical cord-derived mesenchymal stromal cells contribute to neuroprotection in neonatal cortical neurons damaged by oxygen-glucose deprivation. Front Neurol 9:466. https://doi.org/10.3389/fneur.2018.00466
doi: 10.3389/fneur.2018.00466 pubmed: 29963009 pmcid: 6013549
Nakatomi H, Kuriu T, Okabe S et al (2002) Regeneration of hippocampal pyramidal neurons after ischemic brain injury by recruitment of endogenous neural progenitors. Cell 110(4):429–441
pubmed: 12202033
Nguyen N, Lee SB, Lee YS, Lee KH, Ahn JY (2009) Neuroprotection by NGF and BDNF against neurotoxin-exerted apoptotic death in neural stem cells are mediated through Trk receptors, activating PI3-kinase and MAPK pathways. Neurochem Res 34:942–951
Noshita N, Lewen A, Sugawara T, Chan PH (2001) Evidence of phosphorylation of akt and neuronal survival after transient focal cerebral ischemia in mice. J Cereb Blood Flow Metab 21:1442–1450
Nunes MC, Roy NS, Keyoung HM, Goodman RR, McKhann G, Jiang L (2003) Identification and isolation of multipotential neural progenitor cells from the subcortical white matter of the adult human brain. Nat Med 9(4):439–447
pubmed: 12627226
O’Kelly I (2015) Endocytosis as a mode to regulate functional expression of two-pore domain potassium (K 2P) channels. PflügersArchiv-Eur J Physiol 467(5):1133–1142
Ong J, Plane JM, Parent JM et al (2005) Hypoxic-ischemic injury stimulates subventricular zone proliferation and neurogenesis in the neonatal rat. Pediatr Res 58:600–606
pubmed: 16148080
Pap M, Cooper GM (1998) Role of glycogen synthase kinase-3 in the phosphatidylinositol 3-kinase/Akt cell survival pathway. J Biol Chem 273:19929–19932
Park H-A, Kubicki N, Gnyawali S, Chan YC, Roy S, Khanna S (2011) Natural vitamin E α-tocotrienol protects against ischemic stroke by induction of multidrug resistance-associated protein 1. Stroke 42(8):2308–2314
pubmed: 21719775 pmcid: 3362046
Park WS, Sung SI, Ahn SY, Yoo HS, Sung DK, Im GH (2015) Hypothermia augments neuroprotective activity of mesenchymal stem cells for neonatal hypoxic-ischemic encephalopathy. PLoS ONE 10(3):e0120893
pubmed: 25816095 pmcid: 4376738
Peltier J, O'Neill A, Schaffer DV (2007) PI3K/Akt and CREB regulate adult neural hippocampal progenitor proliferation and differentiation. Dev Neurobiol 67:1348–1361
Plane JM, Liu R, Wang TW et al (2004) Neonatal hypoxic–ischemic injury increases forebrain subventricular zone neurogenesis in the mouse. Neurobiol Dis 16:585–595
pubmed: 15262271
Pruszak J, Sonntag KC, Aung MH, Sanchez-Pernaute R, Isacson O (2007) Markers and methods for cell sorting of human embryonic stem cell-derived neural cell populations. Stem Cells 25(9):2257–2268
pubmed: 17588935 pmcid: 2238728
Rajan S, Wischmeyer E, Liu GX, Preisig-Müller R, Daut J, Karschin A (2000) TASK-3, a novel tandem pore domain acid-sensitive K+ channel an extracellular histidine as pH sensor. J BiolChem 275(22):16650–16657
Robertson NJ, Cox IJ, Cowan FM, Counsell SJ, Azzopardi D, Edwards AD (1999) Cerebral intracellular lactic alkalosis persisting months after neonatal encephalopathy measured by magnetic resonance spectroscopy. Pediatr Res 46(3):287–296
pubmed: 10473043
Robertson NJ, Cowan FM, Cox IJ, Edwards AD (2002) Brain alkaline intracellular pH after neonatal encephalopathy. Ann Neurol 52(6):732–742
pubmed: 12447926
Rothstein RP, Levison SW (2005) Gray matter oligodendrocyte progenitors and neurons die caspase-3 mediated deaths subsequent to mild perinatal hypoxic/ischemic insults. Dev Neurosci 27(2–4):149–159
pubmed: 16046849
Scafidi J, Hammond TR, Scafidi S, Ritter J, Jablonska B, Roncal M (2014) Intranasal epidermal growth factor treatment rescues neonatal brain injury. Nature 506(7487):230–234
pubmed: 24390343
Semple BD, Blomgren K, Gimlin K et al (2013) Brain development in rodents and humans: Identifying benchmarks of maturation and vulnerability to injury across species. ProgNeurobiol 106–107:1–16
Sen I, Joshi DC, Joshi PG, Joshi NB (2008) NMDA and non-NMDA receptor-mediated differential Ca2+ load and greater vulnerability of motor neurons in spinal cord cultures. NeurochemInt 52(1–2):247–255
Segovia KN, McClure M, Moravec M et al (2008) Arrested oligodendrocyte lineage maturation in chronic perinatal white matter injury. Ann Neurol 63(4):520–530
pubmed: 18393269 pmcid: 3140464
Shibata M, Yamawaki T, Sasaki T, Hattori H, Hamada J, Fukuuchi Y, Okano H, Miura M (2002) Upregulation of akt phosphorylation at the early stage of middle cerebral artery occlusion in mice. Brain Res 942:1–10
Shiota Y, Nagai A, Sheikh AM, Mitaki S, Mishima S, Yano S (2018) Transplantation of a bone marrow mesenchymal stem cell line increases neuronal progenitor cell migration in a cerebral ischemia animal model. Sci Rep 8(1):1–12
Sowmithra S, Jain NK, Datta I (2020) Evaluating in vitro neonatal hypoxic-ischemic injury using neural progenitors derived from human embryonic stem cells. Stem Cells Dev. https://doi.org/10.1089/scd.2020.0018
doi: 10.1089/scd.2020.0018 pubmed: 32326841
Stokoe D, Stephens LR, Copeland T, Gaffney PR, Reese CB et al (1997) Dual role of phosphatidylinositol-3,4,5-trisphosphate in the activation of protein kinase B. Science 277:567–570
pubmed: 9228007
Stummann TC, Hareng L, Bremer S (2009) Hazard assessment of methylmercury toxicity to neuronal induction in embryogenesis using human embryonic stem cells. Toxicology 257(3):117–126
pubmed: 19150642
Thomas D, Plant LD, Wilkens CM, McCrossan ZA, Goldstein SA (2008) Alternative translation initiation in rat brain yields K2P2. 1 potassium channels permeable to sodium. Neuron 58(6):859–870
Uylings HB, van Eden CG (1990) Qualitative and quantitative comparison of the prefrontal cortex in rat and in primates, including humans. Prog Brain Res 85:31–62
pubmed: 2094901
Vanhaesebroeck B, Leevers SJ, Ahmadi K, Timms J, Katso R, Driscoll PC, Woscholski R, Parker PJ, Waterfield MD (2001) Synthesis and function of 3-phosphorylated inositol lipids. Annu Rev Biochem 70:535–602
pubmed: 11395417
Vanhaesebroeck B, Stephens L, Hawkins P (2012) PI3K signalling: the path to discovery and understanding. Nat Rev Mol Cell Biol 13:195–203
pubmed: 22358332
van Velthoven CT, Kavelaars A, van Bel F, Heijnen CJ (2010a) Mesenchymal stem cell treatment after neonatal hypoxic-ischemic brain injury improves behavioral outcome and induces neuronal and oligodendrocyte regeneration. Brain Behav Immun 24(3):387-393.
van Velthoven CT, Kavelaars A, van Bel F, Heijnen CJ (2010b) Repeated mesenchymal stem cell treatment after neonatal hypoxia-ischemia has distinct effects on formation and maturation of new neurons and oligodendrocytes leading to restoration of damage, corticospinal motor tract activity, and sensorimotor function. J Neurosci 30(28):9603-9611
Wang C, Nguyen HN, Maguire JL, Perry DC (2002) Role of intracellular calcium stores in cell death from oxygen–glucose deprivation in a neuronal cell line. J Cereb Blood Flow Metab 22(2):206–214
pubmed: 11823718
Waterston RH, Lindblad-Toh K, Birney E, Rogers J, Abril JF, Agarwal P, Agarwala R, Ainscough R, Mouse Genome Sequencing Consortium et al (2002) Initial sequencing and comparative analysis of the mouse genome. Nature 420:520
Yang Z, Levison SW (2006) Hypoxia/ischemia expands the regenerative capacity of progenitors in the perinatal subventricular zone. Neuroscience 139:555–564
pubmed: 16500031
Zhang H-W, Hu J-J, Fu R-Q, Liu X, Zhang Y-H, Li J (2018) Flavonoids inhibit cell proliferation and induce apoptosis and autophagy through downregulation of PI3Kγ mediated PI3K/AKT/mTOR/p70S6K/ULK signaling pathway in human breast cancer cells. Sci Rep 8(1):1–13
Zhang K, Yang Y, Ge H, Wang J, Chen X, Lei X (2020) Artesunate promotes the proliferation of neural stem/progenitor cells and alleviates Ischemia-reperfusion Injury through PI3K/Akt/FOXO-3a/p27kip1 signaling pathway. Aging 12:8029–8048
Zhong J, Zhao L, Du Y, Wei G, Yao W-G, Lee W-H (2009) Delayed IGF-1 treatment reduced long-term hypoxia–ischemia-induced brain damage and improved behavior recovery of immature rats. Neurol Res 31(5):483–489
pubmed: 19500451
Zimmer B, Lee G, Stiegler NV et al (2012) Evaluation of developmental toxicants and signaling pathways in a functional test based on the migration of human neural crest cells. Environ Health Perspect 120(8):1116–1122
pubmed: 22571897 pmcid: 3440079

Auteurs

Sowmithra Sowmithra (S)

Department of Biophysics, National Institute of Mental Health and Neurosciences, Institute of National Importance, Hosur Road, P.B. No. 2900, Bengaluru, 560029, Karnataka, India.

Nishtha Kusum Jain (NK)

Department of Biophysics, National Institute of Mental Health and Neurosciences, Institute of National Importance, Hosur Road, P.B. No. 2900, Bengaluru, 560029, Karnataka, India.

Ramesh Bhonde (R)

Dr D.Y. Patil University (DPU), Pune, 411018, India.

Indrani Datta (I)

Department of Biophysics, National Institute of Mental Health and Neurosciences, Institute of National Importance, Hosur Road, P.B. No. 2900, Bengaluru, 560029, Karnataka, India. indranidatta.nimhans@gmail.com.

Articles similaires

[Redispensing of expensive oral anticancer medicines: a practical application].

Lisanne N van Merendonk, Kübra Akgöl, Bastiaan Nuijen
1.00
Humans Antineoplastic Agents Administration, Oral Drug Costs Counterfeit Drugs

Smoking Cessation and Incident Cardiovascular Disease.

Jun Hwan Cho, Seung Yong Shin, Hoseob Kim et al.
1.00
Humans Male Smoking Cessation Cardiovascular Diseases Female
Humans United States Aged Cross-Sectional Studies Medicare Part C
1.00
Humans Yoga Low Back Pain Female Male

Classifications MeSH