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SOX1 Is a Backup Gene for Brain Neurons and Glioma Stem Cell Protection and Proliferation

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Abstract

Failed neuroprotection leads to the initiation of several diseases. SOX1 plays many roles in embryogenesis, oncogenesis, and male sex determination, and can promote glioma stem cell proliferation, invasion, and migration due to its high expression in glioblastoma cells. The functional versatility of the SOX1 gene in malignancy, epilepsy, and Parkinson’s disease, as well as its adverse effects on dopaminergic neurons, makes it an interesting research focus. Hence, we collate the most important discoveries relating to the neuroprotective effects of SOX1 in brain cancer and propose hypothesis worthy of SOX1’s role in the survival of senescent neuronal cells, its roles in fibroblast cell proliferation, and cell fat for neuroprotection, and the discharge of electrical impulses for homeostasis. Increase in electrical impulses transmitted by senescent cells affects the synthesis of neurotransmitters, which will modify the brain cell metabolism and microenvironment.

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Abbreviations

CAFs:

Cancer-associated fibroblast

GDNF:

Glial cell line–derived neurotrophic factor

SOX1:

Sex-determining region box1

Na+ :

Sodium

K+ :

Potassium

Cl− :

Chloride

STAT3:

Signal transducer and activator of transcription 3

DNMT:

DNA methyltransferase

Ca2+ :

Calcium ions

References

  1. Hoelzinger DB et al (2005) Gene expression profile of glioblastoma multiforme invasive phenotype points to new therapeutic targets. Neoplasia 7(1):7–16

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  2. Tang J et al (2018) Genome-wide expression profiling of glioblastoma using a large combined cohort. Sci Rep 8(1):15104

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  3. Gimple RC et al (2019) Glioblastoma stem cells: lessons from the tumor hierarchy in a lethal cancer. Genes Dev 33(11-12):591–609

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  4. Garnier D et al (2019) Glioblastoma stem-like cells, metabolic strategy to kill a challenging target. Front Oncol 9:118

    Article  PubMed  PubMed Central  Google Scholar 

  5. Harrison SE et al (2017) Assembly of embryonic and extraembryonic stem cells to mimic embryogenesis in vitro. Science 356(6334)

  6. Miyagi S, Kato H, Okuda A (2009) Role of SoxB1 transcription factors in development. Cell Mol Life Sci 66(23):3675–3684

    Article  CAS  PubMed  Google Scholar 

  7. Archer TC, Jin J, Casey ES (2011) Interaction of Sox1, Sox2, Sox3 and Oct4 during primary neurogenesis. Dev Biol 350(2):429–440

    Article  CAS  PubMed  Google Scholar 

  8. Grimm D et al (2019) The role of SOX family members in solid tumours and metastasis. Semin Cancer Biol

  9. Weina K, Utikal J (2014) SOX2 and cancer: current research and its implications in the clinic. Clin Transl Med 3:19

    Article  PubMed  PubMed Central  Google Scholar 

  10. Garcia I et al (2017) Oncogenic activity of SOX1 in glioblastoma. Sci Rep 7:46575

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  11. Li M et al (2016) Efficient derivation of dopaminergic neurons from SOX1(-) floor plate cells under defined culture conditions. J Biomed Sci 23:34

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  12. Nitta KR et al (2006) Expression of Sox1 during xenopus early embryogenesis. Biochem Biophys Res Commun 351(1):287–293

    Article  CAS  PubMed  Google Scholar 

  13. Parmar M, Li M (2007) Early specification of dopaminergic phenotype during ES cell differentiation. BMC Dev Biol 7:86

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  14. Wood HB, Episkopou V (1999) Comparative expression of the mouse Sox1, Sox2 and Sox3 genes from pre-gastrulation to early somite stages. Mech Dev 86(1-2):197–201

    Article  CAS  PubMed  Google Scholar 

  15. Pevny LH et al (1998) A role for SOX1 in neural determination. Development 125(10):1967–1978

    Article  CAS  PubMed  Google Scholar 

  16. Hellmich HL et al (1996) Embryonic expression of glial cell-line derived neurotrophic factor (GDNF) suggests multiple developmental roles in neural differentiation and epithelial-mesenchymal interactions. Mech Dev 54(1):95–105

    Article  CAS  PubMed  Google Scholar 

  17. Messerschmidt D et al (2016) Beta-catenin-mediated adhesion is required for successful preimplantation mouse embryo development. Development 143(11):1993–1999

    Article  CAS  PubMed  Google Scholar 

  18. Clarkson ED, Zawada WM, Freed CR (1997) GDNF improves survival and reduces apoptosis in human embryonic dopaminergic neurons in vitro. Cell Tissue Res 289(2):207–210

    Article  CAS  PubMed  Google Scholar 

  19. Alcock J, Sottile V (2009) Dynamic distribution and stem cell characteristics of Sox1-expressing cells in the cerebellar cortex. Cell Res 19(12):1324–1333

    Article  CAS  PubMed  Google Scholar 

  20. Venere M et al (2012) Sox1 marks an activated neural stem/progenitor cell in the hippocampus. Development 139(21):3938–3949

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  21. Alcock J et al (2009) Expression of Sox1, Sox2 and Sox9 is maintained in adult human cerebellar cortex. Neurosci Lett 450(2):114–116

    Article  CAS  PubMed  Google Scholar 

  22. Golden JP et al (1999) Expression of neurturin, GDNF, and GDNF family-receptor mRNA in the developing and mature mouse. Exp Neurol 158(2):504–528

    Article  CAS  PubMed  Google Scholar 

  23. Bonafina A et al (2018) GDNF/GFRalpha1 Complex abrogates self-renewing activity of cortical neural precursors inducing their differentiation. Stem Cell Rep 10(3):1000–1015

    Article  CAS  Google Scholar 

  24. Lehner CF et al (2001) Regulation of the embryonic cell proliferation by Drosophila cyclin D and cyclin E complexes. Novartis Found Symp 237:43–54 discussion 54-7, 93-9

    CAS  PubMed  Google Scholar 

  25. Choi J, Donehower LA (1999) p53 in embryonic development: maintaining a fine balance. Cell Mol Life Sci 55(1):38–47

    Article  CAS  PubMed  Google Scholar 

  26. Hu DB et al (2017) Effect of potential role of p53 on embryo development arrest induced by H2O2 in mouse. In Vitro Cell Dev Biol Anim 53(4):344–353

    Article  CAS  PubMed  Google Scholar 

  27. Wang Q et al (2017) The p53 family coordinates Wnt and nodal inputs in mesendodermal differentiation of embryonic stem cells. Cell Stem Cell 20(1):70–86

    Article  CAS  PubMed  Google Scholar 

  28. Yan Y et al (2005) Directed differentiation of dopaminergic neuronal subtypes from human embryonic stem cells. Stem Cells 23(6):781–790

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  29. Zeng X et al (2004) Dopaminergic differentiation of human embryonic stem cells. Stem Cells 22(6):925–940

    Article  CAS  PubMed  Google Scholar 

  30. Thomson M et al (2011) Pluripotency factors in embryonic stem cells regulate differentiation into germ layers. Cell 145(6):875–889

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  31. Baylin SB, Ohm JE (2006) Epigenetic gene silencing in cancer - a mechanism for early oncogenic pathway addiction? Nat Rev Cancer 6(2):107–116

    Article  CAS  PubMed  Google Scholar 

  32. DiNapoli L, Capel B (2008) SRY and the standoff in sex determination. Mol Endocrinol 22(1):1–9

    Article  CAS  PubMed  Google Scholar 

  33. Li H et al (2017) 17beta-Oestradiol promotes differentiation of human embryonic stem cells into dopamine neurons via cross-talk between insulin-like growth factors-1 and oestrogen receptor beta. J Cell Mol Med 21(8):1605–1618

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  34. Yang W et al (2019) Sex differences in GBM revealed by analysis of patient imaging, transcriptome, and survival data. Sci Transl Med 11(473)

  35. Tian M et al (2018) Impact of gender on the survival of patients with glioblastoma. Biosci Rep 38(6)

  36. Etchegaray JP, Mostoslavsky R (2016) Interplay between metabolism and epigenetics: a nuclear adaptation to environmental changes. Mol Cell 62(5):695–711

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  37. Spangle JM, Roberts TM, Zhao JJ (2017) The emerging role of PI3K/AKT-mediated epigenetic regulation in cancer. Biochim Biophys Acta Rev Cancer 1868(1):123–131

    Article  CAS  PubMed  Google Scholar 

  38. Fidoamore A et al (2017) Energy metabolism in glioblastoma stem cells: PPARalpha a metabolic adaptor to intratumoral microenvironment. Oncotarget 8(65):108430–108450

    Article  PubMed  PubMed Central  Google Scholar 

  39. Alberts B, Johnson A, Lewis J, et al (2002) New York: Garland science. Programmed cell death (apoptosis), Molecular biology of the cell. 4th

  40. Lang RJ et al (2004) Electrical and neurotransmitter activity of mature neurons derived from mouse embryonic stem cells by Sox-1 lineage selection and directed differentiation. Eur J Neurosci 20(12):3209–3221

    Article  CAS  PubMed  Google Scholar 

  41. Malas S et al (2003) Sox1-deficient mice suffer from epilepsy associated with abnormal ventral forebrain development and olfactory cortex hyperexcitability. Neuroscience 119(2):421–432

    Article  CAS  PubMed  Google Scholar 

  42. Cooper GM (2000) Sunderland (MA). Sinauer Associates. The cell: a molecular approach. 2nd, Structure of the plasma membrane

  43. Lopez-Otin C et al (2013) The hallmarks of aging. Cell 153(6):1194–1217

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  44. Dermol-Cerne J et al (2018) Plasma membrane depolarization and permeabilization due to electric pulses in cell lines of different excitability. Bioelectrochemistry 122:103–114

    Article  CAS  PubMed  Google Scholar 

  45. Frieden BR, Gatenby RA (2019) Signal transmission through elements of the cytoskeleton form an optimized information network in eukaryotic cells. Sci Rep 9(1):6110

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  46. Hunley C, Uribe D, Marucho M (2018) A multi-scale approach to describe electrical impulses propagating along actin filaments in both intracellular and in vitro conditions. RSC Adv 8(22):12017–12028

    Article  CAS  PubMed  Google Scholar 

  47. Mele M, Costa RO, Duarte CB (2019) Alterations in GABAA-receptor trafficking and synaptic dysfunction in brain disorders. Front Cell Neurosci 13:77

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  48. O’Donnell VB, Rossjohn J, Wakelam MJ (2018) Phospholipid signaling in innate immune cells. J Clin Invest 128(7):2670–2679

    Article  PubMed  PubMed Central  Google Scholar 

  49. Enge M et al (2017) Single-cell analysis of human pancreas reveals transcriptional signatures of aging and somatic mutation patterns. Cell 171(2):321–330 e14

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  50. Ayanlaja AA et al (2018) The reversible effects of glial cell line-derived neurotrophic factor (GDNF) in the human brain. Semin Cancer Biol 53:212–222

    Article  CAS  PubMed  Google Scholar 

  51. Zhang BL et al (2016) An epigenetic mechanism of high GDNF transcription in glioma cells revealed by specific sequence methylation. Mol Neurobiol 53(7):4352–4362

    Article  CAS  PubMed  Google Scholar 

  52. Zhang L et al (2019) Mechanism of methylation and acetylation of high GDNF transcription in glioma cells: a review. Heliyon 5(6):e01951

    Article  PubMed  PubMed Central  Google Scholar 

  53. Jin B, Robertson KD (2013) DNA methyltransferases, DNA damage repair, and cancer. Adv Exp Med Biol 754:3–29

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  54. Lyko F (2018) The DNA methyltransferase family: a versatile toolkit for epigenetic regulation. Nat Rev Genet 19(2):81–92

    Article  CAS  PubMed  Google Scholar 

  55. Tan Q et al (2016) Epigenetic drift in the aging genome: a ten-year follow-up in an elderly twin cohort. Int J Epidemiol 45(4):1146–1158

    PubMed  Google Scholar 

  56. Cemazar M et al (2009) Control by pulse parameters of DNA electrotransfer into solid tumors in mice. Gene Ther 16(5):635–644

    Article  CAS  PubMed  Google Scholar 

  57. Zhu R et al (2019) Electrical stimulation affects neural stem cell fate and function in vitro. Exp Neurol 319:112963

    Article  PubMed  Google Scholar 

  58. Yamada M et al (2007) Electrical stimulation modulates fate determination of differentiating embryonic stem cells. Stem Cells 25(3):562–570

    Article  CAS  PubMed  Google Scholar 

  59. Duarte Azevedo M, Sander S, Tenenbaum L (2020) GDNF, A neuron-derived factor upregulated in glial cells during disease. J Clin Med 9(2)

  60. Beebe SJ et al (2004) Nanosecond pulsed electric fields modulate cell function through intracellular signal transduction mechanisms. Physiol Meas 25(4):1077–1093

    Article  PubMed  Google Scholar 

  61. Molenaar RJ (2011) Ion channels in glioblastoma. ISRN Neurol 2011:590249

    PubMed  PubMed Central  CAS  Google Scholar 

  62. Beebe SJ et al (2003) Diverse effects of nanosecond pulsed electric fields on cells and tissues. DNA Cell Biol 22(12):785–796

    Article  CAS  PubMed  Google Scholar 

  63. Chopinet L et al (2013) Nanosecond electric pulse effects on gene expression. J Membr Biol 246(11):851–859

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  64. Tasker JG et al (2012) Glial regulation of neuronal function: from synapse to systems physiology. J Neuroendocrinol 24(4):566–576

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  65. Schimanski LA, Barnes CA (2010) Neural protein synthesis during aging: effects on plasticity and memory. Front Aging Neurosci 2

  66. Henstridge CM, Hyman BT, Spires-Jones TL (2019) Beyond the neuron-cellular interactions early in Alzheimer disease pathogenesis. Nat Rev Neurosci 20(2):94–108

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  67. Surmeier DJ, Obeso JA, Halliday GM (2017) Selective neuronal vulnerability in Parkinson disease. Nat Rev Neurosci 18(2):101–113

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  68. Castelli V et al (2019) Neuronal cells rearrangement during aging and neurodegenerative disease: metabolism, oxidative stress and organelles dynamic. Front Mol Neurosci 12:132

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  69. Azpurua J, Eaton BA (2015) Neuronal epigenetics and the aging synapse. Front Cell Neurosci 9:208

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  70. Becchetti A, Munaron L, Arcangeli A (2013) The role of ion channels and transporters in cell proliferation and cancer. Front Physiol 4:312

    Article  PubMed  PubMed Central  Google Scholar 

  71. Zhao YH et al (2015) Hydrostatic pressure promotes the proliferation and osteogenic/chondrogenic differentiation of mesenchymal stem cells: the roles of RhoA and Rac1. Stem Cell Res 14(3):283–296

    Article  CAS  PubMed  Google Scholar 

  72. Schwartz L, da Veiga Moreira J, Jolicoeur M (2018) Physical forces modulate cell differentiation and proliferation processes. J Cell Mol Med 22(2):738–745

    PubMed  Google Scholar 

  73. Jain D et al (2020) Extracellular matrix and biomimetic engineering microenvironment for neuronal differentiation. Neural Regen Res 15(4):573–585

    Article  PubMed  Google Scholar 

  74. Spitzer NC (2015) Neurotransmitter Switching? No Surprise. Neuron 86(5):1131–1144

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  75. Feig C et al (2012) The pancreas cancer microenvironment. Clin Cancer Res 18(16):4266–4276

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  76. Landskron G et al (2014) Chronic inflammation and cytokines in the tumor microenvironment. J Immunol Res 2014:149185

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  77. West AJ et al (2018) The role of interleukin-6-STAT3 signalling in glioblastoma. Oncol Lett 16(4):4095–4104

    PubMed  PubMed Central  Google Scholar 

  78. Tao L et al (2017) Cancer associated fibroblasts: an essential role in the tumor microenvironment. Oncol Lett 14(3):2611–2620

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  79. Liu T et al (2019) Cancer-associated fibroblasts build and secure the tumor microenvironment. Front Cell Dev Biol 7:60

    Article  PubMed  PubMed Central  Google Scholar 

  80. Riegler J et al (2018) Tumor elastography and its association with collagen and the tumor microenvironment. Clin Cancer Res 24(18):4455–4467

    Article  CAS  PubMed  Google Scholar 

  81. Ishiwata T et al (2011) Neuroepithelial stem cell marker nestin regulates the migration, invasion and growth of human gliomas. Oncol Rep 26(1):91–99

    CAS  PubMed  Google Scholar 

  82. Niciu MJ, Kelmendi B, Sanacora G (2012) Overview of glutamatergic neurotransmission in the nervous system. Pharmacol Biochem Behav 100(4):656–664

    Article  CAS  PubMed  Google Scholar 

  83. Natarajan SK, Venneti S (2019) Glutamine metabolism in brain tumors. Cancers (Basel) 11(11)

  84. Chen TJ, Kukley M (2020) Glutamate receptors and glutamatergic signalling in the peripheral nerves. Neural Regen Res 15(3):438–447

    Article  PubMed  Google Scholar 

  85. Zhu L et al (2017) Metabolic imaging of glutamine in cancer. J Nucl Med 58(4):533–537

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  86. Buettner R, Mora LB, Jove R (2002) Activated STAT signaling in human tumors provides novel molecular targets for therapeutic intervention. Clin Cancer Res 8(4):945–954

    CAS  PubMed  Google Scholar 

  87. Marquez J et al (2017) Glutamine addiction in gliomas. Neurochem Res 42(6):1735–1746

    Article  CAS  PubMed  Google Scholar 

  88. Strong AD et al (2018) GL261 glioma tumor cells respond to ATP with an intracellular calcium rise and glutamate release. Mol Cell Biochem 446(1-2):53–62

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  89. San Martin A et al (2013) A genetically encoded FRET lactate sensor and its use to detect the Warburg effect in single cancer cells. PLoS One 8(2):e57712

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  90. Duan K et al (2018) Lactic acid induces lactate transport and glycolysis/OXPHOS interconversion in glioblastoma. Biochem Biophys Res Commun 503(2):888–894

    Article  CAS  PubMed  Google Scholar 

  91. Goldszmid RS, Dzutsev A, Trinchieri G (2014) Host immune response to infection and cancer: unexpected commonalities. Cell Host Microbe 15(3):295–305

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  92. Jacqueline C et al (2017) Infections and cancer: the “fifty shades of immunity” hypothesis. BMC Cancer 17(1):257

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  93. Sun Y, Nelson PS (2012) Molecular pathways: involving microenvironment damage responses in cancer therapy resistance. Clin Cancer Res 18(15):4019–4025

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  94. Weyerhauser P, Kantelhardt SR, Kim EL (2018) Re-purposing chloroquine for glioblastoma: potential merits and confounding variables. Front Oncol 8:335

    Article  PubMed  PubMed Central  Google Scholar 

  95. Ishibashi T et al (2006) Astrocytes promote myelination in response to electrical impulses. Neuron 49(6):823–832

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  96. Ardito F et al (2017) The crucial role of protein phosphorylation in cell signaling and its use as targeted therapy (Review). Int J Mol Med 40(2):271–280

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  97. Takai Y et al (1984) Membrane phospholipid metabolism and signal transduction for protein phosphorylation. Adv Cyclic Nucleotide Protein Phosphorylation Res 18:119–158

    CAS  PubMed  Google Scholar 

  98. Kikkawa U et al (1986) The role of protein kinase C in cell surface signal transduction and tumor promotion. Gan To Kagaku Ryoho 13(3 Pt 2):861–869

    CAS  PubMed  Google Scholar 

  99. Missler M, Sudhof TC, Biederer T (2012) Synaptic cell adhesion. Cold Spring Harb Perspect Biol 4(4):a005694

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  100. Kooij V, Stienen GJM, van der Velden J (2011) The role of protein kinase C-mediated phosphorylation of sarcomeric proteins in the heart-detrimental or beneficial? Biophys Rev 3(3):107

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  101. Herget T et al (1995) The myristoylated alanine-rich C-kinase substrate (MARCKS) is sequentially phosphorylated by conventional, novel and atypical isotypes of protein kinase C. Eur J Biochem 233(2):448–457

    Article  CAS  PubMed  Google Scholar 

  102. Ott LE et al (2011) Two myristoylated alanine-rich C-kinase substrate (MARCKS) paralogs are required for normal development in zebrafish. Anat Rec (Hoboken) 294(9):1511–1524

    Article  CAS  Google Scholar 

  103. Sigal CT, Resh MD (1993) The ADP/ATP carrier is the 32-kilodalton receptor for an NH2-terminally myristoylated Src peptide but not for pp60src polypeptide. Mol Cell Biol 13(5):3084–3092

    CAS  PubMed  PubMed Central  Google Scholar 

  104. Procaccini C et al (2014) Neuro-endocrine networks controlling immune system in health and disease. Front Immunol 5:143

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  105. Rolim AL et al (2010) Ion channelopathies in endocrinology: recent genetic findings and pathophysiological insights. Arq Bras Endocrinol Metabol 54(8):673–681

    Article  PubMed  Google Scholar 

  106. Schwarz N et al (2016) Mutations in the sodium channel gene SCN2A cause neonatal epilepsy with late-onset episodic ataxia. J Neurol 263(2):334–343

    Article  CAS  PubMed  Google Scholar 

  107. Gajewski TF, Schreiber H, Fu YX (2013) Innate and adaptive immune cells in the tumor microenvironment. Nat Immunol 14(10):1014–1022

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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Funding

Researches in our laboratories are funded by the National Natural Science Foundation of China (Grant Numbers: 81772688 and 81372698), China and Jiangsu Postgraduate Science Foundation–funded project (2013 M540466 and 1301068C), Qing Lan Project, and the project Priority Academic Program Development of Jiangsu Higher Education Institutions (PAPD).

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Authors and Affiliations

  1. Public Experimental Research Center, Department of Neurobiology and Anatomy, Xuzhou Medical University, Xuzhou, 221004, Jiangsu, China

    Kouminin Kanwore, Xiao-xiao Guo, Ayanlaja Abiola Abdulrahman, Piniel Alphayo Kambey, Iqra Nadeem & Dianshuai Gao

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  1. Kouminin Kanwore
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  2. Xiao-xiao Guo
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  3. Ayanlaja Abiola Abdulrahman
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  4. Piniel Alphayo Kambey
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  5. Iqra Nadeem
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  6. Dianshuai Gao
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Contributions

Kanwore Kouminin is the mastermind behind the ideas, write up, and image production. Guo Xiao-xiao helped in data gathering. Ayanlaja Abiola Abdulrahman is responsible for reorganization and editing. Piniel Alphayo Kambey and Nadeem Iqra are responsible for further data gathering. Gao Dianshuai read and approved the manuscript for publication.

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Correspondence to Dianshuai Gao.

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Kanwore, K., Guo, Xx., Abdulrahman, A.A. et al. SOX1 Is a Backup Gene for Brain Neurons and Glioma Stem Cell Protection and Proliferation. Mol Neurobiol 58, 2634–2642 (2021). https://doi.org/10.1007/s12035-020-02240-6

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