Skip to main content

Advertisement

Log in

The role of autophagy and apoptosis in early brain injury after subarachnoid hemorrhage: an updated review

  • Review
  • Published:
Molecular Biology Reports Aims and scope Submit manuscript

Abstract

Subarachnoid hemorrhage (SAH) is a worldwide devastating type of stroke with high mortality and morbidity. Accumulating evidence show early brain injury (EBI) as the leading cause of mortality after SAH. The pathological processes involved in EBI include decreased cerebral blood flow, increased intracranial pressure, vasospasm, and disruption of the blood–brain barrier. In addition, neuroinflammation, oxidative stress, apoptosis, and autophagy have also been proposed to contribute to EBI. Among the various processes involved in EBI, neuronal apoptosis has been proven to be a key factor contributing to the poor prognosis of SAH patients. Meanwhile, as another important catabolic process maintaining the cellular and tissue homeostasis, autophagy has been shown to be neuroprotective after SAH. Studies have shown that enhancing autophagy reduced apoptosis, whereas inhibiting autophagy aggravate neuronal apoptosis after SAH. The physiological substrates and mechanisms of neuronal autophagy and apoptosis by which defects in neuronal function are largely unknown. In this review, we summarize and discuss the role of autophagy and apoptosis after SAH and contribute to further study for investigation of the means to control the balance between them.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  1. Hemphill JC 3rd, Greenberg SM, Anderson CS, Becker K, Bendok BR, Cushman M, Fung GL, Goldstein JN, Macdonald RL, Mitchell PH, Scott PA, Selim MH, Woo D (2015) Guidelines for the management of spontaneous intracerebral hemorrhage: a guideline for healthcare professionals from the American Heart Association/American Stroke Association. Stroke 46:2032–2060

    Article  PubMed  Google Scholar 

  2. Suzuki H (2022) Letter to irreversible neuronal damage begins just after aneurysm rupture in poor-grade subarachnoid hemorrhage patients. Transl Stroke Res 13:355–356

    Article  PubMed  Google Scholar 

  3. Neulen A, Meyer S, Kramer A, Pantel T, Kosterhon M, Kunzelmann S, Goetz H, Thal SC (2018) Large vessel vasospasm is not associated with cerebral cortical hypoperfusion in a murine model of subarachnoid hemorrhage. Transl Stroke Res 10:319–326

    Article  PubMed Central  Google Scholar 

  4. Chen S, Wu H, Tang J, Zhang J, Zhang JH (2015) Neurovascular events after subarachnoid hemorrhage: focusing on subcellular organelles. Acta Neurochir Suppl 120:39–46

    PubMed  PubMed Central  Google Scholar 

  5. Zheng Y, Zhou Z, Han F, Chen Z (2021) Special issue: neuroinflammatory pathways as treatment targets in brain disorders autophagic regulation of neuroinflammation in ischemic stroke. Neurochem Int 148:105114

    Article  CAS  PubMed  Google Scholar 

  6. Ruan W, Hu J, Zhou H, Li Y, Xu C, Luo Y, Chen T, Xu B, Yan F, Chen G (2020) Intranasal wnt-3a alleviates neuronal apoptosis in early brain injury post subarachnoid hemorrhage via the regulation of wnt target PPAN mediated by the moonlighting role of aldolase C. Neurochem Int 134:104656

    Article  CAS  PubMed  Google Scholar 

  7. Shi L, Liang F, Zheng J, Zhou K, Chen S, Yu J, Zhang J (2018) Melatonin regulates apoptosis and autophagy Via ROS-MST1 pathway in subarachnoid hemorrhage. Front Mol Neurosci 11:93

    Article  PubMed  PubMed Central  Google Scholar 

  8. Guo D, Xie J, Zhao J, Huang T, Guo X, Song J (2018) Resveratrol protects early brain injury after subarachnoid hemorrhage by activating autophagy and inhibiting apoptosis mediated by the Akt/mTOR pathway. NeuroReport 29:368–379

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  9. Jellinger KA, Stadelmann CH (2000) The enigma of cell death in neurodegenerative disorders. J Neural Transm Suppl. https://doi.org/10.1007/978-3-7091-6301-6_2

    Article  PubMed  Google Scholar 

  10. Boya P, González-Polo RA, Casares N, Perfettini JL, Dessen P, Larochette N, Métivier D, Meley D, Souquere S, Yoshimori T, Pierron G, Codogno P, Kroemer G (2005) Inhibition of macroautophagy triggers apoptosis. Mol Cell Biol 25:1025–1040

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  11. Codogno P, Meijer AJ (2005) Autophagy and signaling: their role in cell survival and cell death. Cell Death Differ 12(Suppl 2):1509–1518

    Article  CAS  PubMed  Google Scholar 

  12. White E (2012) Deconvoluting the context-dependent role for autophagy in cancer. Nature Rev Cancer 12:401–410

    Article  CAS  Google Scholar 

  13. Klionsky DJ, Petroni G, Amaravadi RK, Baehrecke EH, Ballabio A, Boya P, Bravo-San Pedro JM, Cadwell K, Cecconi F, Choi AMK, Choi ME, Chu CT, Codogno P, Colombo MI, Cuervo AM, Deretic V, Dikic I, Elazar Z, Eskelinen EL, Fimia GM, Gewirtz DA, Green DR, Hansen M, Jaattela M, Johansen T, Juhasz G, Karantza V, Kraft C, Kroemer G, Ktistakis NT, Kumar S, Lopez-Otin C, Macleod KF, Madeo F, Martinez J, Melendez A, Mizushima N, Munz C, Penninger JM, Perera RM, Piacentini M, Reggiori F, Rubinsztein DC, Ryan KM, Sadoshima J, Santambrogio L, Scorrano L, Simon HU, Simon AK, Simonsen A, Stolz A, Tavernarakis N, Tooze SA, Yoshimori T, Yuan J, Yue Z, Zhong Q, Galluzzi L, Pietrocola F (2021) Autophagy in major human diseases. EMBO J 40:e108863

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  14. Sonsky I, Vodicka P, Vodickova Kepkova K, Hansikova H (2021) Mitophagy in Huntington’s disease. Neurochem Int 149:105147

    Article  CAS  PubMed  Google Scholar 

  15. Durocher M, Knepp B, Yee A, Jickling G, Rodriguez F, Ng K, Zhan X, Hamade F, Ferino E, Amini H, Carmona-Mora P, Hull H, Ander BP, Sharp FR, Stamova B (2021) Molecular correlates of hemorrhage and edema volumes following human intracerebral hemorrhage implicate inflammation, autophagy, mRNA splicing, and T cell receptor signaling. Transl Stroke Res 12:754–777

    Article  CAS  PubMed  Google Scholar 

  16. Liang Y, Deng Y, Zhao J, Liu L, Wang J, Chen P, Zhang Q, Sun C, Wang Y, Xiang Y, He Z (2022) Ferritinophagy is involved in experimental subarachnoid hemorrhage-induced neuronal ferroptosis. Neurochem Res 47:692–700

    Article  CAS  PubMed  Google Scholar 

  17. Schipper HM, Song W, Tavitian A, Cressatti M (2019) The sinister face of heme oxygenase-1 in brain aging and disease. Prog Neurobiol 172:40–70

    Article  CAS  PubMed  Google Scholar 

  18. Tukaj C (2013) The significance of macroautophagy in health and disease. Folia Morphol 72:87–93

    Article  CAS  Google Scholar 

  19. Nakatogawa H, Suzuki K, Kamada Y, Ohsumi Y (2009) Dynamics and diversity in autophagy mechanisms: lessons from yeast. Nat Rev Mol cell Biol 10:458–467

    Article  CAS  PubMed  Google Scholar 

  20. Levine B, Mizushima N, Virgin HW (2011) Autophagy in immunity and inflammation. Nature 469:323–335

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  21. Mizushima N, Komatsu M (2011) Autophagy: renovation of cells and tissues. Cell 147:728–741

    Article  CAS  PubMed  Google Scholar 

  22. Kim J, Kundu M, Viollet B, Guan KL (2011) AMPK and mTOR regulate autophagy through direct phosphorylation of Ulk1. Nat cell Biol 13:132–141

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  23. Zheng J, Wang Y, Liu Y, Han S, Zhang Y, Luo Y, Yan Y, Li J, Zhao L (2022) cPKCgamma deficiency exacerbates autophagy impairment and hyperphosphorylated tau buildup through the AMPK/mTOR pathway in mice with Type 1 Diabetes Mellitus. Neurosci Bull. https://doi.org/10.1007/s12264-022-00863-4

    Article  PubMed  Google Scholar 

  24. Igney FH, Krammer PH (2002) Death and anti-death: tumour resistance to apoptosis. Nat Rev Cancer 2:277–288

    Article  CAS  PubMed  Google Scholar 

  25. Saelens X, Festjens N, Vande Walle L, van Gurp M, van Loo G, Vandenabeele P (2004) Toxic proteins released from mitochondria in cell death. Oncogene 23:2861–2874

    Article  CAS  PubMed  Google Scholar 

  26. Hegazy AM, Chen N, Lin H, Babu VS, Li F, Yang Y, Qin Z, Shi F, Li J, Lin L (2021) Induction of apoptosis in SSN-1cells by snakehead fish Vesiculovirus (SHVV) via Matrix protein dependent intrinsic pathway. Fish Shellfish Immunol 113:24–34

    Article  CAS  PubMed  Google Scholar 

  27. Wajant H (2002) The Fas signaling pathway: more than a paradigm. Science (New York, NY) 296:1635–1636

    Article  CAS  Google Scholar 

  28. Goelz N, Eekels JJM, Pantic M, Kamber CT, Speer O, Franzoso FD, Schmugge M (2021) Platelets express adaptor proteins of the extrinsic apoptosis pathway and can activate caspase-8. PLoS ONE 16:e0244848

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  29. Yoon JH, Her S, Kim M, Jang IS, Park J (2012) The expression of damage-regulated autophagy modulator 2 (DRAM2) contributes to autophagy induction. Mol Biol Rep 39:1087–1093

    Article  CAS  PubMed  Google Scholar 

  30. Elmore S (2007) Apoptosis: a review of programmed cell death. Toxicol Pathol 35:495–516

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  31. Cory S, Adams JM (2002) The Bcl2 family: regulators of the cellular life-or-death switch. Nat Rev Cancer 2:647–656

    Article  CAS  PubMed  Google Scholar 

  32. Acehan D, Jiang X, Morgan DG, Heuser JE, Wang X, Akey CW (2002) Three-dimensional structure of the apoptosome: implications for assembly, procaspase-9 binding, and activation. Mol Cell 9:423–432

    Article  CAS  PubMed  Google Scholar 

  33. Cain K, Bratton SB, Cohen GM (2002) The Apaf-1 apoptosome: a large caspase-activating complex. Biochimie 84:203–214

    Article  CAS  PubMed  Google Scholar 

  34. Ekert PG, Vaux DL (2005) The mitochondrial death squad: hardened killers or innocent bystanders? Curr Opin Cell Biol 17:626–630

    Article  CAS  PubMed  Google Scholar 

  35. Locksley RM, Killeen N, Lenardo MJ (2001) The TNF and TNF receptor superfamilies: integrating mammalian biology. Cell 104:487–501

    Article  CAS  PubMed  Google Scholar 

  36. Kischkel FC, Hellbardt S, Behrmann I, Germer M, Pawlita M, Krammer PH, Peter ME (1995) Cytotoxicity-dependent APO-1 (Fas/CD95)-associated proteins form a death-inducing signaling complex (DISC) with the receptor. EMBO J 14:5579–5588

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  37. Teringova E, Tousek P (2017) Apoptosis in ischemic heart disease. J Transl Med 15:87

    Article  PubMed  PubMed Central  Google Scholar 

  38. Sorice M (2022) Crosstalk of autophagy and apoptosis. Cells. https://doi.org/10.3390/cells11091479

    Article  PubMed  PubMed Central  Google Scholar 

  39. Thorburn A (2020) Crosstalk between autophagy and apoptosis: mechanisms and therapeutic implications. Prog Mol Biol Transl Sci 172:55–65

    Article  CAS  PubMed  Google Scholar 

  40. Oberstein A, Jeffrey PD, Shi Y (2007) Crystal structure of the Bcl-XL-Beclin 1 peptide complex: Beclin 1 is a novel BH3-only protein. J Biol Chem 282:13123–13132

    Article  CAS  PubMed  Google Scholar 

  41. He Y, Wang W, Xu X, Yang B, Yu X, Wu Y, Wang J (2022) Mettl3 inhibits the apoptosis and autophagy of chondrocytes in inflammation through mediating Bcl2 stability via Ythdf1-mediated m(6)A modification. Bone 154:116182

    Article  CAS  PubMed  Google Scholar 

  42. Maiuri MC, Criollo A, Kroemer G (2010) Crosstalk between apoptosis and autophagy within the Beclin 1 interactome. EMBO J 29:515–516

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  43. Lindqvist LM, Heinlein M, Huang DC, Vaux DL (2014) Prosurvival Bcl-2 family members affect autophagy only indirectly, by inhibiting Bax and Bak. Proc Natl Acad Sci USA 111:8512–8517

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  44. Galonek HL, Hardwick JM (2006) Upgrading the BCL-2 network. Nat Cell Biol 8:1317–1319

    Article  CAS  PubMed  Google Scholar 

  45. Pattingre S, Tassa A, Qu X, Garuti R, Liang XH, Mizushima N, Packer M, Schneider MD, Levine B (2005) Bcl-2 antiapoptotic proteins inhibit Beclin 1-dependent autophagy. Cell 122:927–939

    Article  CAS  PubMed  Google Scholar 

  46. He C, Zhu H, Li H, Zou MH, Xie Z (2013) Dissociation of Bcl-2-Beclin1 complex by activated AMPK enhances cardiac autophagy and protects against cardiomyocyte apoptosis in diabetes. Diabetes 62:1270–1281

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  47. Wei Y, Pattingre S, Sinha S, Bassik M, Levine B (2008) JNK1-mediated phosphorylation of Bcl-2 regulates starvation-induced autophagy. Mol Cell 30:678–688

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  48. Jiang H, Wen X, Zhang X, Zhong X, Li Z, Zhang B (2022) Lens culinaris agglutinin inhibits human hepatoma cell migration via mannose and fucose-mediated ERK1/2 and JNK1/2/3 signalling pathway. Mol Biol Rep. https://doi.org/10.1007/s11033-022-07582-z

    Article  PubMed  Google Scholar 

  49. Chang NC, Nguyen M, Germain M, Shore GC (2010) Antagonism of Beclin 1-dependent autophagy by BCL-2 at the endoplasmic reticulum requires NAF-1. EMBO J 29:606–618

    Article  CAS  PubMed  Google Scholar 

  50. Thomas RL, Gustafsson AB (2013) MCL1 is critical for mitochondrial function and autophagy in the heart. Autophagy 9:1902–1903

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  51. Germain M, Nguyen AP, Le Grand JN, Arbour N, Vanderluit JL, Park DS, Opferman JT, Slack RS (2011) MCL-1 is a stress sensor that regulates autophagy in a developmentally regulated manner. EMBO J 30:395–407

    Article  CAS  PubMed  Google Scholar 

  52. Shende P, Plaisance I, Morandi C, Pellieux C, Berthonneche C, Zorzato F, Krishnan J, Lerch R, Hall MN, Rüegg MA, Pedrazzini T, Brink M (2011) Cardiac raptor ablation impairs adaptive hypertrophy, alters metabolic gene expression, and causes heart failure in mice. Circulation 123:1073–1082

    Article  PubMed  Google Scholar 

  53. Sharma A, Mehan S (2021) Targeting PI3K-AKT/mTOR signaling in the prevention of autism. Neurochem Int 147:105067

    Article  CAS  PubMed  Google Scholar 

  54. Li Y, Wang Y, Kim E, Beemiller P, Wang CY, Swanson J, You M, Guan KL (2007) Bnip3 mediates the hypoxia-induced inhibition on mammalian target of rapamycin by interacting with Rheb. J Biol Chem 282:35803–35813

    Article  CAS  PubMed  Google Scholar 

  55. Movahhed P, Saberiyan M, Safi A, Arshadi Z, Kazerouni F, Teimori H (2022) The impact of DAPK1 and mTORC1 signaling association on autophagy in cancer. Mol Biol Rep. https://doi.org/10.1007/s11033-022-07154-1

    Article  PubMed  Google Scholar 

  56. Bialik S, Kimchi A (2006) The death-associated protein kinases: structure, function, and beyond. Ann Rev Biochem 75:189–210

    Article  CAS  PubMed  Google Scholar 

  57. Nasiri-Ansari N, Nikolopoulou C, Papoutsi K, Kyrou I, Mantzoros CS, Kyriakopoulos G, Chatzigeorgiou A, Kalotychou V, Randeva MS, Chatha K, Kontzoglou K, Kaltsas G, Papavassiliou AG, Randeva HS, Kassi E (2021) Empagliflozin attenuates non-alcoholic fatty liver disease (NAFLD) in high fat diet fed ApoE((-/-)) mice by activating autophagy and reducing ER stress and apoptosis. Int J Mol Sci 22:818

    Article  CAS  PubMed Central  Google Scholar 

  58. Gozuacik D, Bialik S, Raveh T, Mitou G, Shohat G, Sabanay H, Mizushima N, Yoshimori T, Kimchi A (2008) DAP-kinase is a mediator of endoplasmic reticulum stress-induced caspase activation and autophagic cell death. Cell Death Differ 15:1875–1886

    Article  CAS  PubMed  Google Scholar 

  59. Mills KR, Reginato M, Debnath J, Queenan B, Brugge JS (2004) Tumor necrosis factor-related apoptosis-inducing ligand (TRAIL) is required for induction of autophagy during lumen formation in vitro. Proc Natl Acad Sci USA 101:3438–3443

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  60. Thorburn J, Moore F, Rao A, Barclay WW, Thomas LR, Grant KW, Cramer SD, Thorburn A (2005) Selective inactivation of a Fas-associated death domain protein (FADD)-dependent apoptosis and autophagy pathway in immortal epithelial cells. Mol Biol Cell 16:1189–1199

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  61. Kim SA, Jang JH, Kim W, Lee PR, Kim YH, Vang H, Lee K, Oh SB (2022) Mitochondrial reactive oxygen species elicit acute and chronic itch via transient receptor potential canonical 3 activation in mice. Neurosci Bull 38:373–385

    Article  CAS  PubMed  Google Scholar 

  62. Gao L, Loveless J, Shay C, Teng Y (2020) Targeting ROS-mediated crosstalk between autophagy and apoptosis in cancer. Adv Exp Med Biol 1260:1–12

    Article  CAS  PubMed  Google Scholar 

  63. Kirkland RA, Adibhatla RM, Hatcher JF, Franklin JL (2002) Loss of cardiolipin and mitochondria during programmed neuronal death: evidence of a role for lipid peroxidation and autophagy. Neuroscience 115:587–602

    Article  CAS  PubMed  Google Scholar 

  64. Kirkland RA, Saavedra GM, Franklin JL (2007) Rapid activation of antioxidant defenses by nerve growth factor suppresses reactive oxygen species during neuronal apoptosis: evidence for a role in cytochrome c redistribution. J Neurosci Off J Soc Neurosci 27:11315–11326

    Article  CAS  Google Scholar 

  65. Luo Z, Xu X, Sho T, Zhang J, Xu W, Yao J, Xu J (2019) ROS-induced autophagy regulates porcine trophectoderm cell apoptosis, proliferation, and differentiation. Am J Physiol Cell Physiol 316:C198–C209

    Article  CAS  PubMed  Google Scholar 

  66. Li B, Zhou P, Xu K, Chen T, Jiao J, Wei H, Yang X, Xu W, Wan W, Xiao J (2020) Metformin induces cell cycle arrest, apoptosis and autophagy through ROS/JNK signaling pathway in human osteosarcoma. Int J Biol Sci 16:74–84

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  67. Maheswari U, Ghosh K, Sadras SR (2018) Licarin A induces cell death by activation of autophagy and apoptosis in non-small cell lung cancer cells. Apoptosis Int J Progr Cell Death 23:210–225

    Article  CAS  Google Scholar 

  68. Park S, Yamaguchi M, Zhou C, Calvert JW, Tang J, Zhang JH (2004) Neurovascular protection reduces early brain injury after subarachnoid hemorrhage. Stroke 35:2412–2417

    Article  CAS  PubMed  Google Scholar 

  69. Bederson JB, Levy AL, Ding WH, Kahn R, DiPerna CA, Jenkins AL 3rd, Vallabhajosyula P (1998) Acute vasoconstriction after subarachnoid hemorrhage. Neurosurgery 42:352–360 (discussion 360-352)

    Article  CAS  PubMed  Google Scholar 

  70. Matz PG, Copin JC, Chan PH (2000) Cell death after exposure to subarachnoid hemolysate correlates inversely with expression of CuZn-superoxide dismutase. Stroke 31:2450–2459

    Article  CAS  PubMed  Google Scholar 

  71. Prunell GF, Mathiesen T, Diemer NH, Svendgaard NA (2003) Experimental subarachnoid hemorrhage: subarachnoid blood volume, mortality rate, neuronal death, cerebral blood flow, and perfusion pressure in three different rat models. Neurosurgery 52:165–175

    PubMed  Google Scholar 

  72. Endo H, Nito C, Kamada H, Yu F, Chan PH (2006) Akt/GSK3beta survival signaling is involved in acute brain injury after subarachnoid hemorrhage in rats. Stroke 37:2140–2146

    Article  CAS  PubMed  Google Scholar 

  73. Chung CL, Wu CH, Huang YH, Wu SC, Chai CY, Tsai HP, Kwan AL (2022) Blocking hepatoma-derived growth factor attenuates vasospasm and neuron cell apoptosis in rats subjected to subarachnoid hemorrhage. Transl Stroke Res 13:300–310

    Article  CAS  PubMed  Google Scholar 

  74. Shioda N, Ishigami T, Han F, Moriguchi S, Shibuya M, Iwabuchi Y, Fukunaga K (2007) Activation of phosphatidylinositol 3-kinase/protein kinase B pathway by a vanadyl compound mediates its neuroprotective effect in mouse brain ischemia. Neuroscience 148:221–229

    Article  CAS  PubMed  Google Scholar 

  75. Xu MX, Zhao GL, Hu X, Zhou H, Li SY, Li F, Miao Y, Lei B, Wang Z (2022) P2X7/P2X4 receptors mediate proliferation and migration of retinal microglia in experimental glaucoma in mice. Neurosci Bull. https://doi.org/10.1007/s12264-022-00833-w

    Article  PubMed  PubMed Central  Google Scholar 

  76. Satturu V, Vattikuti JLJDS, Kumar A, Singh RKMSP, Zaw H, Jubay ML, Satish L, Rathore A, Mulinti S, Lakshmi H, Chakraborty A, Thirunavukkarasu N (2020) Multiple genome wide association mapping models identify quantitative trait nucleotides for BROWN Planthopper (Nilaparvata lugens) resistance in MAGIC indica population of rice. Vaccines (Basel) 8:608

    Article  CAS  Google Scholar 

  77. Cahill J, Calvert JW, Solaroglu I, Zhang JH (2006) Vasospasm and p53-induced apoptosis in an experimental model of subarachnoid hemorrhage. Stroke 37:1868–1874

    Article  PubMed  Google Scholar 

  78. Cahill J, Calvert JW, Zhang JH (2006) Mechanisms of early brain injury after subarachnoid hemorrhage. J Cereb Blood Flow Metab 26:1341–1353

    Article  CAS  PubMed  Google Scholar 

  79. Cahill J, Zhang JH (2009) Subarachnoid hemorrhage: is it time for a new direction? Stroke 40:S86-87

    Article  PubMed  Google Scholar 

  80. Li T, Sun KJ, Wang HD, Zhou ML, Ding K, Lu XY, Wei WT, Wang CX, Zhou XM (2015) Tert-butylhydroquinone ameliorates early brain injury after experimental subarachnoid hemorrhage in mice by enhancing Nrf2-independent autophagy. Neurochem Res 40:1829–1838

    Article  CAS  PubMed  Google Scholar 

  81. Galluzzi L, Bravo-San Pedro JM, Blomgren K, Kroemer G (2016) Autophagy in acute brain injury. Nat Rev Neurosci 17:467–484

    Article  CAS  PubMed  Google Scholar 

  82. Wang Z, Shi XY, Yin J, Zuo G, Zhang J, Chen G (2012) Role of autophagy in early brain injury after experimental subarachnoid hemorrhage. J Mol Neurosci 46:192–202

    Article  CAS  PubMed  Google Scholar 

  83. Zheng B, Zhou X, Pang L, Che Y, Qi X (2021) Baicalin suppresses autophagy-dependent ferroptosis in early brain injury after subarachnoid hemorrhage. Bioengineered 12:7794–7804

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  84. Lee JY, He Y, Sagher O, Keep R, Hua Y, Xi G (2009) Activated autophagy pathway in experimental subarachnoid hemorrhage. Brain Res 1287:126–135

    Article  CAS  PubMed  Google Scholar 

  85. Shao A, Wang Z, Wu H, Dong X, Li Y, Tu S, Tang J, Zhao M, Zhang J, Hong Y (2016) Enhancement of autophagy by histone deacetylase inhibitor Trichostatin A ameliorates neuronal apoptosis after subarachnoid hemorrhage in rats. Mol Neurobiol 53:18–27

    Article  CAS  PubMed  Google Scholar 

  86. Wang J, Wang Y, Zuo Y, Duan J, Pan A, Li JM, Yan XX, Liu F (2021) MFGE8 mitigates brain injury in a rat model of SAH by maintaining vascular endothelial integrity via TIGbeta5/PI3K/CXCL12 signaling. Exp Brain Res 239:2193–2205

    Article  CAS  PubMed  Google Scholar 

  87. Jing CH, Wang L, Liu PP, Wu C, Ruan D, Chen G (2012) Autophagy activation is associated with neuroprotection against apoptosis via a mitochondrial pathway in a rat model of subarachnoid hemorrhage. Neuroscience 213:144–153

    Article  CAS  PubMed  Google Scholar 

  88. Huang W, Li N, Zhang Y, Wang X, Yin M, Lei QY (2022) AHCYL1 senses SAH to inhibit autophagy through interaction with PIK3C3 in an MTORC1-independent manner. Autophagy 18:309–319

    Article  CAS  PubMed  Google Scholar 

  89. Sun L, Ma Y, Zhang Z, Li X, Chen Y, Liu G, Fu A (2018) ROCK2 regulates autophagy in the hippocampus of rats after subarachnoid hemorrhage. NeuroReport 29:1571–1577

    Article  CAS  PubMed  Google Scholar 

  90. Cai Z, Zhang H, Song H, Piao Y, Zhang X (2020) Edaravone combined with cinepazide maleate on neurocyte autophagy and neurological function in rats with subarachnoid hemorrhage. Exp Ther Med 19:646–650

    CAS  PubMed  Google Scholar 

  91. Sun CM, Enkhjargal B, Reis C, Zhou KR, Xie ZY, Wu LY, Zhang TY, Zhu QQ, Tang JP, Jiang XD, Zhang JH (2019) Osteopontin attenuates early brain injury through regulating autophagy-apoptosis interaction after subarachnoid hemorrhage in rats. CNS Neurosci Ther 25:1162–1172

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  92. Asada R, Suzuki H (2022) Osteopontin in post-subarachnoid hemorrhage pathologies. J Integr Neurosci 21:62

    Article  PubMed  Google Scholar 

Download references

Acknowledgements

SC and QW were the principal investigators. YZ and YL wrote the paper. YL made the original figures. YZ and YL revised the figures. CL handled the language and made some comments.

Funding

This research was supported by the National Natural Science Foundation of China (81971107).

Author information

Authors and Affiliations

Authors

Corresponding authors

Correspondence to Qun Wu or Sheng Chen.

Ethics declarations

Conflict of interest

The authors declare no conflict of interest, financial or otherwise.

Consent for publication

Not applicable.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Zhao, Y., Luo, Y., Liu, Y. et al. The role of autophagy and apoptosis in early brain injury after subarachnoid hemorrhage: an updated review. Mol Biol Rep 49, 10775–10782 (2022). https://doi.org/10.1007/s11033-022-07756-9

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11033-022-07756-9

Keywords

Navigation