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Cellular and Molecular Neurobiology

, Volume 34, Issue 1, pp 83–94 | Cite as

The Expression Changes of Vacuolar Protein Sorting 4B (VPS4B) Following Middle Cerebral Artery Occlusion (MCAO) in Adult Rats Brain Hippocampus

  • Gang Cui
  • Yunfeng WangEmail author
  • Shanshan Yu
  • Lixiang Yang
  • Bing Li
  • Wei Wang
  • Peng Zhou
  • Jiang Wu
  • Ting Lu
  • Dongjian Chen
Original Research

Abstract

Vacuolar protein sorting 4 (VPS4), is a member of ATPases associated with diverse cellular activities protein family. VPS4 is composed of VPS4A and VPS4B, VPS4B plays an important role in the lysosomal degradation pathway, intracellular protein trafficking, virus budding and abscission of cytokinesis. However, information regarding its distribution and possible function in the central nervous system is limited. Therefore, we performed a middle cerebral artery occlusion (MCAO) in adult rats and detected the dynamic changes of VPS4B in hippocampus CA1 subregion. We found that the VPS4B expression was increased strongly after MCAO and reached the peak after 3 days. VPS4B mainly located in the cytoplasm of neurons, but not astrocytes and microglia. Moreover, there was a concomitant up-regulation of active caspase-3. In vitro studies indicated that the up-regulation of VPS4B may be involved in oxygen-glucose deprivation-induced PC12 cell death. And knock-down of VPS4B in cultured differentiated PC12 cells by siRNA showed that VPS4B promoted the expression of active caspase-3. Collectively, all these results and MTT assay suggested that the up-regulation of VPS4B played an important role in the pathophysiology after MCAO, and further research is needed to have a good understanding of its function and mechanism.

Keywords

Middle cerebral artery occlusion (MCAO) VPS4B Apoptosis Adult rats 

Notes

Conflict of interest

None.

References

  1. Barone FC, Irving EA, Ray AM, Lee JC, Kassis S, Kumar S, Badger AM, Legos JJ, Erhardt JA, Ohlstein EH, Hunter AJ, Harrison DC, Philpott K, Smith BR, Adams JL, Parsons AA (2001) Inhibition of p38 mitogen-activated protein kinase provides neuroprotection in cerebral focal ischemia. Med Res Rev 21(2):129–145PubMedCrossRefGoogle Scholar
  2. Bederson JB, Pitts LH, Tsuji M, Nishimura MC, Davis RL, Bartkowski H (1986) Rat middle cerebral artery occlusion: evaluation of the model and development of a neurologic examination. Stroke 17(3):472–476PubMedCrossRefGoogle Scholar
  3. Beyer A, Scheuring S, Muller S, Mincheva A, Lichter P, Kohrer K (2003) Comparative sequence and expression analyses of four mammalian VPS4 genes. Gene 305(1):47–59PubMedCrossRefGoogle Scholar
  4. Bishop N, Woodman P (2000) ATPase-defective mammalian VPS4 localizes to aberrant endosomes and impairs cholesterol trafficking. Mol Biol Cell 11(1):227–239PubMedCentralPubMedCrossRefGoogle Scholar
  5. Boulton TG, Nye SH, Robbins DJ, Ip NY, Radziejewska E, Morgenbesser SD, DePinho RA, Panayotatos N, Cobb MH, Yancopoulos GD (1991) ERKs: a family of protein-serine/threonine kinases that are activated and tyrosine phosphorylated in response to insulin and NGF. Cell 65(4):663–675PubMedCrossRefGoogle Scholar
  6. Casanova E, Garate C, Ovalle S, Calvo P, Chinchetru MA (1996) Identification of four splice variants of the mouse stress-activated protein kinase JNK/SAPK alpha-isoform. NeuroReport 7(7):1320–1324PubMedCrossRefGoogle Scholar
  7. Choi DW (1996) Ischemia-induced neuronal apoptosis. Curr Opin Neurobiol 6(5):667–672PubMedCrossRefGoogle Scholar
  8. Culmsee C, Zhu C, Landshamer S, Becattini B, Wagner E, Pellecchia M, Blomgren K, Plesnila N (2005) Apoptosis-inducing factor triggered by poly(ADP-ribose) polymerase and Bid mediates neuronal cell death after oxygen-glucose deprivation and focal cerebral ischemia. J Neurosci 25(44):10262–10272PubMedCrossRefGoogle Scholar
  9. Davies BA, Azmi IF, Katzmann DJ (2009) Regulation of Vps4 ATPase activity by ESCRT-III. Biochem Soc Trans 37(Pt 1):143–145PubMedCentralPubMedCrossRefGoogle Scholar
  10. Dirnagl U, Iadecola C, Moskowitz MA (1999) Pathobiology of ischaemic stroke: an integrated view. Trends Neurosci 22(9):391–397PubMedCrossRefGoogle Scholar
  11. Elmore S (2007) Apoptosis: a review of programmed cell death. Toxicol Pathol 35(4):495–516PubMedCentralPubMedCrossRefGoogle Scholar
  12. Erhardt L (1996) Biochemical markers in acute myocardial infarction–the beginning of a new era. Eur Heart J 17(12):1781–1782PubMedCrossRefGoogle Scholar
  13. Fujita H, Yamanaka M, Imamura K, Tanaka Y, Nara A, Yoshimori T, Yokota S, Himeno M (2003) A dominant negative form of the AAA ATPase SKD1/VPS4 impairs membrane trafficking out of endosomal/lysosomal compartments: class E vps phenotype in mammalian cells. J Cell Sci 116(Pt 2):401–414PubMedCrossRefGoogle Scholar
  14. Furuichi T, Liu W, Shi H, Miyake M, Liu KJ (2005) Generation of hydrogen peroxide during brief oxygen-glucose deprivation induces preconditioning neuronal protection in primary cultured neurons. J Neurosci Res 79(6):816–824PubMedCrossRefGoogle Scholar
  15. Genetos DC, Toupadakis CA, Raheja LF, Wong A, Papanicolaou SE, Fyhrie DP, Loots GG, Yellowley CE (2010) Hypoxia decreases sclerostin expression and increases Wnt signaling in osteoblasts. J Cell Biochem 110(2):457–467PubMedCentralPubMedGoogle Scholar
  16. Gupta S, Barrett T, Whitmarsh AJ, Cavanagh J, Sluss HK, Derijard B, Davis RJ (1996) Selective interaction of JNK protein kinase isoforms with transcription factors. EMBO J 15(11):2760–2770PubMedGoogle Scholar
  17. Hasegawa T, Konno M, Baba T, Sugeno N, Kikuchi A, Kobayashi M, Miura E, Tanaka N, Tamai K, Furukawa K, Arai H, Mori F, Wakabayashi K, Aoki M, Itoyama Y, Takeda A (2011) The AAA-ATPase VPS4 regulates extracellular secretion and lysosomal targeting of alpha-synuclein. PLoS ONE 6(12):e29460PubMedCentralPubMedCrossRefGoogle Scholar
  18. Hossmann KA (1996) Periinfarct depolarizations. Cerebrovasc Brain Metab Rev 8(3):195–208PubMedGoogle Scholar
  19. Katsura K, Kristian T, Siesjo BK (1994) Energy metabolism, ion homeostasis, and cell damage in the brain. Biochem Soc Trans 22(4):991–996PubMedGoogle Scholar
  20. Kirino T (1982) Delayed neuronal death in the gerbil hippocampus following ischemia. Brain Res 239(1):57–69PubMedCrossRefGoogle Scholar
  21. Kunau WH, Beyer A, Franken T, Gotte K, Marzioch M, Saidowsky J, Skaletz-Rorowski A, Wiebel FF (1993) Two complementary approaches to study peroxisome biogenesis in Saccharomyces cerevisiae: forward and reversed genetics. Biochimie 75(3–4):209–224PubMedCrossRefGoogle Scholar
  22. Leist M, Nicotera P (1998) Apoptosis, excitotoxicity, and neuropathology. Exp Cell Res 239(2):183–201PubMedCrossRefGoogle Scholar
  23. Lindsberg PJ, Hallenbeck JM, Feuerstein G (1991) Platelet-activating factor in stroke and brain injury. Ann Neurol 30(2):117–129PubMedCrossRefGoogle Scholar
  24. Liu Y, Lv L, Xue Q, Wan C, Ni T, Chen B, Zhou Y, Ni R, Mao G (2013) Vacuolar protein sorting 4B, an ATPase protein positively regulates the progression of NSCLC via promoting cell division. Mol Cell Biochem 381(1–2):163–171PubMedCrossRefGoogle Scholar
  25. Longa EZ, Weinstein PR, Carlson S, Cummins R (1989) Reversible middle cerebral artery occlusion without craniectomy in rats. Stroke 20(1):84–91PubMedCrossRefGoogle Scholar
  26. Magistretti PJ, Pellerin L (1997) Metabolic coupling during activation. A cellular view. Adv Exp Med Biol 413:161–166PubMedCrossRefGoogle Scholar
  27. Magistretti PJ, Pellerin L, Rothman DL, Shulman RG (1999) Energy on demand. Science 283(5401):496–497PubMedCrossRefGoogle Scholar
  28. Martin RL, Lloyd HG, Cowan AI (1994) The early events of oxygen and glucose deprivation: setting the scene for neuronal death? Trends Neurosci 17(6):251–257PubMedCrossRefGoogle Scholar
  29. Mun-Bryce S, Rosenberg GA (1998) Matrix metalloproteinases in cerebrovascular disease. J Cereb Blood Flow Metab 18(11):1163–1172PubMedCrossRefGoogle Scholar
  30. Murray CJ, Lopez AD (1997) Global mortality, disability, and the contribution of risk factors: global Burden of Disease Study. Lancet 349(9063):1436–1442PubMedCrossRefGoogle Scholar
  31. Pirttila TR, Kauppinen RA (1992) Recovery of intracellular pH in cortical brain slices following anoxia studied by nuclear magnetic resonance spectroscopy: role of lactate removal, extracellular sodium and sodium/hydrogen exchange. Neuroscience 47(1):155–164PubMedCrossRefGoogle Scholar
  32. Qin AP, Liu CF, Qin YY, Hong LZ, Xu M, Yang L, Liu J, Qin ZH, Zhang HL (2010) Autophagy was activated in injured astrocytes and mildly decreased cell survival following glucose and oxygen deprivation and focal cerebral ischemia. Autophagy 6(6):738–753PubMedCrossRefGoogle Scholar
  33. Rakic P (1985) Limits of neurogenesis in primates. Science 227(4690):1054–1056PubMedCrossRefGoogle Scholar
  34. Rothwell NJ, Hopkins SJ (1995) Cytokines and the nervous system II: actions and mechanisms of action. Trends Neurosci 18(3):130–136PubMedCrossRefGoogle Scholar
  35. Scheuring S, Rohricht RA, Schoning-Burkhardt B, Beyer A, Muller S, Abts HF, Kohrer K (2001) Mammalian cells express two VPS4 proteins both of which are involved in intracellular protein trafficking. J Mol Biol 312(3):469–480PubMedCrossRefGoogle Scholar
  36. Sugawara T, Fujimura M, Noshita N, Kim GW, Saito A, Hayashi T, Narasimhan P, Maier CM, Chan PH (2004) Neuronal death/survival signaling pathways in cerebral ischemia. NeuroRx 1(1):17–25PubMedCentralPubMedCrossRefGoogle Scholar
  37. Teis D, Saksena S, Emr SD (2008) Ordered assembly of the ESCRT-III complex on endosomes is required to sequester cargo during MVB formation. Dev Cell 15(4):578–589PubMedCrossRefGoogle Scholar
  38. Thornberry NA, Lazebnik Y (1998) Caspases: enemies within. Science 281(5381):1312–1316PubMedCrossRefGoogle Scholar
  39. Tu C, Ortega-Cava CF, Winograd P, Stanton MJ, Reddi AL, Dodge I, Arya R, Dimri M, Clubb RJ, Naramura M, Wagner KU, Band V, Band H (2010) Endosomal-sorting complexes required for transport (ESCRT) pathway-dependent endosomal traffic regulates the localization of active Src at focal adhesions. Proc Natl Acad Sci U S A 107(37):16107–16112PubMedCentralPubMedCrossRefGoogle Scholar
  40. Webster KA, Graham RM, Thompson JW, Spiga MG, Frazier DP, Wilson A, Bishopric NH (2006) Redox stress and the contributions of BH3-only proteins to infarction. Antioxid Redox Signal 8(9–10):1667–1676PubMedCrossRefGoogle Scholar
  41. Yang YP, Liang ZQ, Gao B, Jia YL, Qin ZH (2008) Dynamic effects of autophagy on arsenic trioxide-induced death of human leukemia cell line HL60 cells. Acta Pharmacol Sin 29(1):123–134PubMedCrossRefGoogle Scholar
  42. Yoshimori T, Yamagata F, Yamamoto A, Mizushima N, Kabeya Y, Nara A, Miwako I, Ohashi M, Ohsumi M, Ohsumi Y (2000) The mouse SKD1, a homologue of yeast Vps4p, is required for normal endosomal trafficking and morphology in mammalian cells. Mol Biol Cell 11(2):747–763PubMedCentralPubMedCrossRefGoogle Scholar
  43. Ziemka-Nalecz M, Stanaszek L, Zalewska T (2013) Oxygen-glucose deprivation promotes gliogenesis and microglia activation in organotypic hippocampal slice culture: involvement of metalloproteinases. Acta Neurobiol Exp (Wars) 73(1):130–142Google Scholar

Copyright information

© Springer Science+Business Media New York 2013

Authors and Affiliations

  • Gang Cui
    • 1
  • Yunfeng Wang
    • 1
    Email author
  • Shanshan Yu
    • 2
  • Lixiang Yang
    • 1
  • Bing Li
    • 1
  • Wei Wang
    • 1
  • Peng Zhou
    • 1
  • Jiang Wu
    • 1
  • Ting Lu
    • 1
  • Dongjian Chen
    • 1
  1. 1.Department of NeurosurgeryThe First Affiliated Hospital of Soochow UniversitySuzhouPeople’s Republic of China
  2. 2.Department of DermatologyThe First Affiliated Hospital of Soochow UniversitySuzhouPeople’s Republic of China

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