Post-Ischemic Neurodegeneration of the Hippocampus Resembling Alzheimer’s Disease Proteinopathy
Abstract
:1. Introduction
2. Neuropathophysiological Changes in Post-Ischemic Hippocampus
3. Neurodegenerative Changes in Post-Ischemic Hippocampus
3.1. Patterns of Neuronal Pathology
3.2. Synaptic Alterations
4. Blood–Brain Barrier Permeability in Post-Ischemic Hippocampus
5. Neuroinflammation in Post-Ischemic Hippocampus
6. Amyloid Accumulation in Post-Ischemic Hippocampus
7. Tau Protein Modification in Post-Ischemic Hippocampus
8. Metals in Post-Ischemic Hippocampus
9. Dementia and Post-Ischemic Hippocampus
10. Conclusions
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Conflicts of Interest
References
- Pluta, R. Brain Ischemia: Alzheimer’s Disease Mechanisms; Nova Science Publishers Inc.: New York, NY, USA, 2019; p. 311. [Google Scholar]
- Ying, Y.; Wang, J.-Z. Illuminating neural circuits in Alzheimer’s disease. Neurosci. Bull. 2021, 37, 1203–1217. [Google Scholar] [CrossRef] [PubMed]
- Kiryk, A.; Pluta, R.; Figiel, I.; Mikosz, M.; Ułamek, M.; Niewiadomska, G.; Jabłoński, M.; Kaczmarek, L. Transient brain ischemia due to cardiac arrest causes irreversible long-lasting cognitive injury. Behav. Brain Res. 2011, 219, 1–7. [Google Scholar] [CrossRef] [PubMed]
- Pluta, R.; Ułamek, M.; Jabłoński, M. Alzheimer’s mechanisms in ischemic brain degeneration. Anat. Rec. 2009, 292, 1863–1881. [Google Scholar] [CrossRef] [PubMed]
- Pluta, R.; Januszewski, S.; Jabłoński, M.; Ułamek, M. Factors in creepy delayed neuronal death in hippocampus following brain ischemia-reperfusion injury with long-term survival. Acta Neurochir. 2010, 106, 37–41. [Google Scholar]
- Radenovic, L.; Nenadic, M.; Ułamek-Kozioł, M.; Januszewski, S.; Czuczwar, S.J.; Andjus, P.R.; Pluta, R. Heterogeneity in brain distribution of activated microglia and astrocytes in a rat ischemic model of Alzheimer’s disease after 2 years of survival. Aging 2020, 12, 12251–12267. [Google Scholar] [CrossRef] [PubMed]
- Sekeljic, V.; Bataveljic, D.; Stamenkovic, S.; Ułamek, M.; Jabłonski, M.; Radenovic, L.; Pluta, R.; Andjus, P.R. Cellular markers of neuroinflammation and neurogenesis after ischemic brain injury in the long-term survival rat model. Brain Struct. Funct. 2012, 217, 411–420. [Google Scholar] [CrossRef]
- Kriska, J.; Hermanova, Z.; Knotek, T.; Tureckova, J.; Anderova, M. On the common journey of neural cells through ischemic brain injury and Alzheimer’s disease. Int. J. Mol. Sci. 2021, 22, 9689. [Google Scholar] [CrossRef]
- Pluta, R.; Salińska, E.; Puka, M.; Stafiej, A.; Łazarewicz, J.W. Early changes in extracellular amino acids and calcium concentrations in rabbit hippocampus following complete 15-min cerebral ischemia. Resuscitation 1988, 16, 193–210. [Google Scholar] [CrossRef]
- Rathmell, J.C.; Thompson, C.B. The central effectors of cell death in the immune system. Annu. Rev. Immunol. 1999, 17, 781–828. [Google Scholar] [CrossRef]
- Dong, Z.; Saikumar, P.; Weinberg, J.M.; Venkatachalam, M.A. Internucleosomal DNA cleavage triggered by plasma membrane damage during necrotic cell death. Involvement of serine but not cysteine proteases. Am. J. Pathol. 1997, 151, 1205–1213. [Google Scholar]
- Nitatori, T.; Sato, N.; Waguri, S.; Karasawa, Y.; Araki, H.; Shibanai, K.; Kominami, E.; Uchiyama, Y. Delayed neuronal death in the CA1 pyramidal cell layer of the gerbil hippocampus following transient ischemia is apoptosis. J. Neurosci. 1995, 15, 1001–1011. [Google Scholar] [CrossRef] [Green Version]
- Fujimura, M.; Morita-Fujimura, Y.; Murakami, K.; Kawase, M.; Chan, P.H. Cytosolic redistribution of cytochrome c after transient focal cerebral ischemia in rats. J. Cereb. Blood Flow Metab. 1998, 18, 1239–1247. [Google Scholar] [CrossRef]
- Sugawara, T.; Fujimura, M.; Morita-Fujimura, Y.; Kawase, M.; Chan, P.H. Mitochondrial release of cytochrome c corresponds to the selective vulnerability of hippocampus CA1 neurons in rats after transient global cerebral ischemia. J. Neurosci. 1999, 19, RC39. [Google Scholar] [CrossRef] [Green Version]
- Sugawara, T.; Fujimura, M.; Noshita, N.; Kim, G.W.; Saito, A.; Hayashi, T.; Narasimhan, P.; Maier, C.M.; Chan, P.H. Neuronal death/survival signaling pathways in cerebral ischemia. NeuroRx 2004, 1, 17–25. [Google Scholar] [CrossRef]
- Ułamek-Kozioł, M.; Kocki, J.; Bogucka-Kocka, A.; Petniak, A.; Gil-Kulik, P.; Januszewski, S.; Bogucki, J.; Jabłoński, M.; Furmaga-Jabłońska, W.; Brzozowska, J.; et al. Dysregulation of autophagy, mitophagy and apoptotic genes in the medial temporal lobe cortex in an ischemic model of Alzheimer’s disease. J. Alzheimers Dis. 2016, 54, 113–121. [Google Scholar] [CrossRef] [Green Version]
- Pluta, R.; Ułamek-Kozioł, M.; Januszewski, S.; Czuczwar, S.J. Dysregulation of Alzheimer’s disease-related genes and proteins following cardiac arrest. Folia Neuropathol. 2017, 55, 283–288. [Google Scholar] [CrossRef]
- Ułamek-Kozioł, M.; Kocki, J.; Bogucka-Kocka, A.; Januszewski, S.; Bogucki, J.; Czuczwar, S.J.; Pluta, R. Autophagy, mitophagy and apoptotic gene changes in the hippocampal CA1 area in a rat ischemic model of Alzheimer’s disease. Pharmacol. Rep. 2017, 69, 1289–1294. [Google Scholar] [CrossRef]
- Ułamek-Kozioł, M.; Czuczwar, S.J.; Kocki, J.; Januszewski, S.; Bogucki, J.; Bogucka-Kocka, A.; Pluta, R. Dysregulation of autophagy, mitophagy, and apoptosis genes in the CA3 region of the hippocampus in the ischemic model of Alzheimer’s disease in the rat. J. Alzheimers Dis. 2019, 72, 1279–1286. [Google Scholar] [CrossRef] [Green Version]
- Rosenbaum, D.M.; Gupta, G.; D’Amore, J.; Sinhg, M.; Weidenheim, K.; Zhang, H.; Kessler, J.A. Fas(CD95/APO-1) plays a role in the pathophysiology of focal cerebral ischemia. J. Neurosci. Res. 2000, 61, 686–692. [Google Scholar] [CrossRef]
- Degterev, A.; Huang, Z.; Boyce, M.; Li, Y.; Jagtap, P.; Mizushima, N.; Cuny, G.D.; Mitachison, T.J.; Moskowitz, M.A.; Yuan, J. Chemical inhibitor of nonapoptotic cell death with therapeutic potential for ischemic brain injury. Nat. Chem. Biol. 2005, 1, 112–119. [Google Scholar] [CrossRef]
- Unal-Cevik, I.; Kilinc, M.; Can, A.; Gursoy-Ozdemir, Y.; Dalkara, T. Apoptotic and necrotic death mechanisms are concomitantly activated in the same cell after cerebral ischemia. Stroke 2004, 35, 2189–2194. [Google Scholar] [CrossRef] [Green Version]
- Tsujimoto, Y.; Shimizu, S. Another way to die: Autophagic programmed cell death. Cell Death Differ. 2005, 12, 1528–1534. [Google Scholar] [CrossRef] [Green Version]
- Wang, P.; Shao, B.Z.; Deng, Z.; Chen, S.; Yue, Z.; Miao, C.Y. Autophagy in ischemic stroke. Prog Neurobiol 2018, 163–164, 98–117. [Google Scholar] [CrossRef]
- Adhami, F.; Schloemer, A.; Kuan, C.Y. The roles of autophagy in cerebral ischemia. Autophagy 2007, 3, 42–44. [Google Scholar] [CrossRef] [Green Version]
- Kirino, T. Delayed neuronal death in the gerbil hippocampus following ischemia. Brain Res. 1982, 239, 57–69. [Google Scholar] [CrossRef]
- Pulsinelli, W.A.; Brierley, J.B.; Plum, F. Temporal profile of neuronal damage in a model of transient forebrain ischemia. Ann. Neurol. 1982, 11, 491–498. [Google Scholar] [CrossRef]
- Smith, M.L.; Auer, R.N.; Siesjö, B.K. The density and distribution of ischemic brain injury in the rat following 2–10 min of forebrain ischemia. Acta Neuropathol. 1984, 64, 319–332. [Google Scholar] [CrossRef]
- Pluta, R.; Lossinsky, A.S.; Mossakowski, M.J.; Faso, L.; Wisniewski, H.M. Reassessment of new model of complete cerebral ischemia in rats. Method of induction of clinical death, pathophysiology and cerebrovascular pathology. Acta Neuropathol. 1991, 83, 1–11. [Google Scholar] [CrossRef]
- Pluta, R. The role of apolipoprotein E in the deposition of β-amyloid peptide during ischemia–reperfusion brain injury. A model of early Alzheimer’s disease. Ann. N. Y. Acad. Sci. 2000, 903, 324–334. [Google Scholar] [CrossRef]
- Pluta, R. Astroglial expression of the beta-amyloid in ischemia–reperfusion brain injury. Ann. N. Y. Acad. Sci. 2002, 977, 102–108. [Google Scholar] [CrossRef]
- Pluta, R. Glial expression of the beta-amyloid peptide in cardiac arrest. J. Neurol. Sci. 2002, 203–204, 277–280. [Google Scholar] [CrossRef]
- Uchida, H.; Fujita, Y.; Matsueda, M.; Umeda, M.; Matsuda, S.; Kato, H.; Kasahara, J.; Araki, T. Damage to neurons and oligodendrocytes in the hippocampal CA1 sector after transient focal ischemia in rats. Cell Mol. Neurobiol. 2010, 30, 1125–1134. [Google Scholar] [CrossRef] [PubMed]
- Jiao, L.; Zhang, J.; Li, Z.; Liu, H.; Chen, Y.; Xu, S. Edaravone alleviates delayed neuronal death and long-dated cognitive dysfunction of hippocampus after transient focal ischemia in Wistar rat brains. Neuroscience 2011, 182, 177–183. [Google Scholar] [CrossRef] [PubMed]
- Gemmell, E.; Bosomworth, H.; Allan, L.; Hall, R.; Khundakar, A.; Oakley, A.E.; Deramecourt, V.; Polvikoski, T.M.; O’Brien, J.T.; Kalaria, R.N. Hippocampal neuronal atrophy and cognitive function in delayed poststroke and aging-related dementias. Stroke 2012, 43, 808–814. [Google Scholar] [CrossRef] [Green Version]
- Schaapsmeerders, P.; van Uden, I.W.M.; Tuladhar, A.M.; Maaijwee, N.A.M.; van Dijk, E.J.; Rutten-Jacobs, L.C.A.; Arntz, R.M.; Schoonderwaldt, H.C.; Dorresteijn, L.D.A.; de Leeuw, F.E.; et al. Ipsilateral hippocampal atrophy is associated with long-term memory dysfunction after ischemic stroke in young adults. Hum. Brain Mapp. 2015, 36, 2432–2442. [Google Scholar] [CrossRef]
- Neumann, J.T.; Cohan, C.H.; Dave, K.R.; Wright, C.B.; Perez-Pinzon, M.A. Global cerebral ischemia: Synaptic and cognitive dysfunction. Curr. Drug Targets 2013, 14, 20–35. [Google Scholar] [CrossRef]
- Wang, X.; Xing, A.; Xu, C.; Cai, Q.; Liu, H.; Li, L. Cerebrovascular hypoperfusion induces spatial memory impairment, synaptic changes, and amyloid-beta oligomerization in rats. J. Alzheimers Dis. 2010, 21, 813–822. [Google Scholar] [CrossRef] [Green Version]
- Zhao, Y.; Gu, J.H.; Dai, C.L.; Liu, Q.; Iqbal, K.; Liu, F.; Gong, C.X. Chronic cerebral hypoperfusion causes decrease of O-GlcNAcylation, hyperphosphorylation of tau and behavioral deficits in mice. Front. Aging Neurosci. 2014, 6, 10. [Google Scholar] [CrossRef]
- Ruan, Y.W.; Han, X.J.; Shi, Z.S.; Lei, Z.G.; Xu, Z.C. Remodeling of synapses in the CA1 area of the hippocampus after transient global ischemia. Neuroscience 2012, 218, 268–277. [Google Scholar] [CrossRef]
- Ułamek-Kozioł, M.; Furmaga-Jabłońska, W.; Januszewski, S.; Brzozowska, J.; Sciślewska, M.; Jabłoński, M.; Pluta, R. Neuronal autophagy: Self-eating or self-cannibalism in Alzheimer’s disease. Neurochem. Res. 2013, 38, 1769–1773. [Google Scholar] [CrossRef] [Green Version]
- Hofmeijer, J.; van Putten, M.J. Ischemic cerebral damage: An appraisal of synaptic failure. Stroke 2012, 43, 607–615. [Google Scholar] [CrossRef] [Green Version]
- Curcio, M.; Salazar, I.L.; Mele, M.; Canzoniero, L.M.; Duarte, C.B. Calpains and neuronal damage in the ischemic brain: The swiss knife in synaptic injury. Prog. Neurobiol. 2016, 143, 1–35. [Google Scholar] [CrossRef]
- Yuan, Y.; Shan, X.; Men, W.; Zhai, H.; Qiao, X.; Geng, L.; Li, C. The effect of crocin on memory, hippocampal acetylcholine level, and apoptosis in a rat model of cerebral ischemia. Biomed. Pharmacother. 2020, 30, 110543. [Google Scholar] [CrossRef]
- Scheff, S.W.; Price, D.A.; Schmitt, F.A.; Scheff, M.A.; Mufson, E.J. Synaptic loss in the inferior temporal gyrus in mild cognitive impairment and Alzheimer’s disease. J. Alzheimers Dis. 2011, 24, 547–557. [Google Scholar] [CrossRef]
- Pluta, R. Blood–brain barrier dysfunction and amyloid precursor protein accumulation in microvascular compartment following ischemia–reperfusion brain injury with 1-year survival. Acta Neurochir. 2003, 86, 117–122. [Google Scholar]
- Pluta, R. Pathological opening of the blood–brain barrier to horseradish peroxidase and amyloid precursor protein following ischemia–reperfusion brain injury. Chemotherapy 2005, 51, 223–226. [Google Scholar] [CrossRef]
- Pluta, R.; Ułamek, M.; Januszewski, S. Micro-blood–brain barrier openings and cytotoxic fragments of amyloid precursor protein accumulation in white matter after ischemic brain injury in long-lived rats. Acta Neurochir. 2006, 96, 267–271. [Google Scholar]
- Pluta, R.; Januszewski, S.; Ułamek, M. Ischemic blood-brain barrier and amyloid in white matter as etiological factors in leukoaraiosis. Acta Neurochir. 2008, 102, 353–356. [Google Scholar]
- Pluta, R.; Barcikowska, M.; Januszewski, S.; Misicka, A.; Lipkowski, A.W. Evidence of blood-brain barrier permeability/leakage for circulating human Alzheimer’s β-amyloid-(1-42)-peptide. NeuroReport 1996, 7, 1261–1265. [Google Scholar] [CrossRef]
- Banks, W.A.; Kovac, A.; Majerova, P.; Bullock, K.M.; Shi, M.; Zhang, J. Tau proteins cross the blood-brain barrier. J. Alzheimers Dis. 2017, 55, 411–419. [Google Scholar] [CrossRef]
- Ramos-Cejudo, J.; Wisniewski, T.; Marmar, C.; Zetterberg, H.; Blennow, K.; de Leon, M.J.; Fossati, S. Traumatic brain injury and Alzheimer’s disease: The cerebrovascular link. EBioMedicine 2018, 28, 21–30. [Google Scholar] [CrossRef] [Green Version]
- Petito, C.; Morgello, S.; Felix, J.C.; Lesser, M.L. The two patterns of reactive astrocytosis in postischemic rat brain. J. Cereb. Blood Flow Metab. 1990, 10, 850–859. [Google Scholar] [CrossRef] [Green Version]
- Schmidt-Kastner, R.; Szymas, J.; Hossmann, K.A. Immunohistochemical study of glial reaction and serum-protein extravasation in relation to neuronal damage in rat hippocampus after ischemia. Neuroscience 1990, 38, 527–540. [Google Scholar] [CrossRef]
- Gehrmann, J.; Bonnekoh, P.; Miyazawa, T.; Hossmann, K.A.; Kreutzberg, G. Immunocytochemical study of early microglial activation in ischemia. J. Cereb. Blood Flow Metab. 1992, 12, 257–269. [Google Scholar] [CrossRef]
- Morioka, T.; Kalehua, A.N.; Streit, W.J. Progressive expression of immunomolecules on microglial cells in rat dorsal hippocampus following transient forebrain ischemia. Acta Neuropathol. 1992, 83, 149–157. [Google Scholar] [CrossRef]
- Orzyłowska, O.; Oderfeld-Nowak, B.; Zaremba, M.; Januszewski, S.; Mossakowski, M.J. Prolonged and concomitant induction of astroglial immunoreactivity of interleukin-1 beta and interleukin-6 in the rat hippocampus after transient global ischemia. Neurosci. Lett. 1999, 263, 72–76. [Google Scholar] [CrossRef]
- Touzani, O.; Boutin, H.; LeFeuvre, R.; Parker, L.; Miller, A.; Luheshi, G.; Rothwell, N. Interleukin-1 influences ischemic brain damage in the mouse independently of the interleukin-1 type I receptor. J. Neurosci. 2002, 22, 38–43. [Google Scholar] [CrossRef] [Green Version]
- Yamasaki, Y.; Matsuura, N.; Shozuhara, H.; Onodera, H.; Itoyama, Y.; Kogure, K. Interleukin-1 as a pathogenetic mediator of ischemic brain damage in rats. Stroke 1995, 26, 676–680. [Google Scholar] [CrossRef]
- Griffin, W.S.; Sheng, J.G.; Royston, M.C.; Gentleman, S.M.; McKenzie, J.E.; Graham, D.I.; Roberts, G.W.; Mrak, R.E. Glial-neuronal interactions in Alzheimer’s disease: The potential role of a “Cytokine Cycle” in disease progression. Brain Pathol. 1998, 8, 65–72. [Google Scholar] [CrossRef]
- Giulian, D.; Haverkamp, L.J.; Li, J.; Karshin, W.L.; Yu, J.; Tom, D.; Li, X.; Kirkpatrick, J.B. Senile plaques stimulate microglia to release a neurotoxin found in Alzheimer brain. Neurochem. Int. 1995, 27, 119–137. [Google Scholar] [CrossRef]
- Pluta, R.; Kida, E.; Lossinsky, A.S.; Golabek, A.A.; Mossakowski, M.J.; Wisniewski, H.M. Complete cerebral ischemia with short-term survival in rats induced by cardiac arrest: I. Extracellular accumulation of Alzheimer’s β-amyloid protein precursor in the brain. Brain Res. 1994, 649, 323–328. [Google Scholar] [CrossRef]
- Hall, E.D.; Oostveen, J.A.; Dunn, E.; Carter, D.B. Increased amyloid protein precursor and apolipoprotein E immunoreactivity in the selectively vulnerable hippocampus following transient forebrain ischemia in gerbils. Exp. Neurol. 1995, 135, 17–27. [Google Scholar] [CrossRef] [PubMed]
- Ishimaru, H.; Ishikawa, K.; Haga, S.; Shoji, M.; Ohe, Y.; Haga, C.; Sasaki, A.; Takashashi, A.; Maruyama, Y. Accumulation of apolipoprotein E and β-amyloid-like protein in a trace of the hippocampal CA1 pyramidal cell layer after ischaemic delayed neuronal death. NeuroReport 1996, 7, 3063–3067. [Google Scholar] [CrossRef] [PubMed]
- Yokota, M.; Saido, T.C.; Tani, E.; Yamaura, I.; Minami, N. Cytotoxic fragment of amyloid precursor protein accumulates in hippocampus after global forebrain ischemia. J. Cereb. Blood Flow Metab. 1996, 16, 1219–1223. [Google Scholar] [CrossRef] [Green Version]
- Pluta, R.; Barcikowska, M.; Dębicki, G.; Ryba, M.; Januszewski, S. Changes in amyloid precursor protein and apolipoprotein E immunoreactivity following ischemic brain injury in rat with long-term survival: Influence of idebenone treatment. Neurosci. Lett. 1997, 232, 95–98. [Google Scholar] [CrossRef]
- Pluta, R.; Barcikowska, M.; Mossakowski, M.J.; Zelman, I. Cerebral accumulation of beta-amyloid following ischemic brain injury with long-term survival. Acta Neurochir. 1998, 71, 206–208. [Google Scholar]
- Pluta, R. No effect of anti-oxidative therapy on cerebral amyloidosis following ischemia–reperfusion brain injury. Folia Neuropathol. 2000, 38, 188–190. [Google Scholar]
- Sinigaglia-Coimbra, R.; Cavalheiro, E.A.; Coimbra, C.G. Postischemic hypertermia induces Alzheimer-like pathology in the rat brain. Acta Neuropathol. 2002, 103, 444–452. [Google Scholar] [CrossRef]
- Banati, R.B.; Gehrmann, J.; Wießner, C.; Hossmann, K.A.; Kreutzberg, G.W. Glial expression of the β-amyloid precursor protein (APP) in global ischemia. J. Cereb. Blood Flow Metab. 1995, 15, 647–654. [Google Scholar] [CrossRef]
- Palacios, G.; Mengod, G.; Tortosa, A.; Ferrer, I.; Palacios, J.M. Increased β-amyloid precursor protein expression in astrocytes in the gerbil hippocampus following ischaemia: Association with proliferation of astrocytes. Eur. J. Neurosci. 1995, 7, 501–510. [Google Scholar] [CrossRef]
- Badan, I.; Dinca, I.; Buchhold, B.; Suofu, Y.; Walker, L.; Gratz, M.; Platt, D.; Kessler, C.H.; Popa-Wagner, A. Accelerated accumulation of N- and C-terminal beta APP fragments and delayed recovery of microtubule-associated protein 1B expression following stroke in aged rats. Eur. J. Neurosci. 2004, 19, 2270–2280. [Google Scholar] [CrossRef]
- Jabłoński, M.; Maciejewski, R.; Januszewski, S.; Ułamek, M.; Pluta, R. One year follow up in ischemic brain injury and the role of Alzheimer factors. Physiol. Res. 2011, 60, S113–S119. [Google Scholar] [CrossRef]
- Takuma, K.; Baba, A.; Matsuda, T. Astrocyte apoptosis: Implications for neuroprotection. Prog. Neurobiol. 2004, 72, 111–127. [Google Scholar] [CrossRef]
- Van Groen, T.; Puurunen, K.; Maki, H.M.; Sivenius, J.; Jolkkonen, J. Transformation of diffuse beta-amyloid precursor protein and beta-amyloid deposits to plaques in the thalamus after transient occlusion of the middle cerebral artery in rats. Stroke 2005, 36, 1551–1556. [Google Scholar] [CrossRef] [Green Version]
- Pluta, R.; Kocki, J.; Maciejewski, R.; Ułamek-Kozioł, M.; Jabłoński, M.; Bogucka-Kocka, A.; Czuczwar, S.J. Ischemia signaling to Alzheimer-related genes. Folia Neuropathol. 2012, 50, 322–329. [Google Scholar] [CrossRef] [Green Version]
- Pluta, R.; Jabłoński, M.; Czuczwar, S.J. Postischemic dementia with Alzheimer phenotype: Selectively vulnerable versus resistant areas of the brain and neurodegeneration versus β-amyloid peptide. Folia Neuropathol. 2012, 50, 101–109. [Google Scholar]
- Jendroska, K.; Poewe, W.; Daniel, S.E.; Pluess, J.; Iwerssen-Schmidt, H.; Paulsen, J.; Barthel, S.; Schelosky, L.; Cervos-Navarro, J.; DeArmond, S.J. Ischemic stress induces deposition of amyloid beta immunoreactivity in human brain. Acta Neuropathol. 1995, 90, 461–466. [Google Scholar] [CrossRef]
- Wiśniewski, H.M.; Maślińska, D. Beta-protein immunoreactivity in the human brain after cardiac arrest. Folia Neuropathol. 1996, 34, 65–71. [Google Scholar]
- Jendroska, K.; Hoffmann, O.M.; Patt, S. Amyloid β peptide and precursor protein (APP) in mild and severe brain ischemia. Ann. N. Y. Acad. Sci. 1997, 826, 401–405. [Google Scholar] [CrossRef]
- Qi, J.; Wu, H.; Yang, Y.; Wand, D.; Chen, Y.; Gu, Y.; Liu, T. Cerebral ischemia and Alzheimer’s disease: The expression of amyloid-β and apolipoprotein E in human hippocampus. J. Alzheimers Dis. 2007, 12, 335–341. [Google Scholar] [CrossRef]
- Akinyemi, R.O.; Allan, L.M.; Oakley, A.; Kalaria, R.N. Hippocampal neurodegenerative pathology in post-stroke dementia compared to other dementias and aging controls. Front. Neurosci. 2017, 11, 717. [Google Scholar] [CrossRef] [Green Version]
- Lee, P.H.; Bang, O.Y.; Hwang, E.M.; Lee, J.S.; Joo, U.S.; Mook-Jung, I.; Huh, K. Circulating beta amyloid protein is elevated in patients with acute ischemic stroke. J Neural Transm. 2005, 112, 1371–1379. [Google Scholar] [CrossRef]
- Zetterberg, H.; Mörtberg, E.; Song, L.; Chang, L.; Provuncher, G.K.; Patel, P.P.; Ferrell, E.; Fournier, D.R.; Kan, C.W.; Campbell, T.G.; et al. Hypoxia due to cardiac arrest induces a time-dependent increase in serum amyloid β levels in humans. PLoS ONE 2011, 6, e28263. [Google Scholar] [CrossRef] [Green Version]
- Liu, Y.H.; Cao, H.Y.; Wang, Y.R.; Jiao, S.S.; Bu, X.L.; Zeng, F.; Wang, Q.H.; Li, J.; Deng, J.; Zhou, H.D.; et al. Serum Aβ is predictive for short-term neurological deficits after acute ischemic stroke. Neurotox. Res. 2015, 27, 292–299. [Google Scholar] [CrossRef]
- Kocki, J.; Ułamek-Kozioł, M.; Bogucka-Kocka, A.; Januszewski, S.; Jabłoński, M.; Gil-Kulik, P.; Brzozowska, J.; Petniak, A.; Furmaga-Jabłońska, W.; Bogucki, J.; et al. Dysregulation of amyloid precursor protein, β-secretase, presenilin 1 and 2 genes in the rat selectively vulnerable CA1 subfield of hippocampus following transient global brain ischemia. J. Alzheimers Dis. 2015, 47, 1047–1056. [Google Scholar] [CrossRef] [Green Version]
- Pluta, R.; Ułamek-Kozioł, M.; Kocki, J.; Bogucki, J.; Januszewski, S.; Bogucka-Kocka, A.; Czuczwar, S.J. Expression of the tau protein and amyloid protein precursor processing genes in the CA3 area of the hippocampus in the ischemic model of Alzheimer’s disease in the rat. Mol. Neurobiol. 2020, 57, 1281–1290. [Google Scholar] [CrossRef] [Green Version]
- Geddes, J.W.; Schwab, C.; Craddock, S.; Wilson, J.L.; Pettigrew, L.C. Alterations in tau immunostaining in the rat hippocampus following transient cerebral ischemia. J. Cereb. Blood Flow Metab. 1994, 14, 554–564. [Google Scholar] [CrossRef] [Green Version]
- Majd, S.; Power, J.H.; Koblar, S.A.; Grantham, H.J. Early glycogen synthase kinase-3 and protein phosphatase 2A independent tau dephosphorylation during global brain ischaemia and reperfusion following cardiac arrest and the role of the adenosine monophosphate kinase pathway. Eur. J. Neurosci. 2016, 44, 1987–1997. [Google Scholar] [CrossRef] [Green Version]
- Fujii, H.; Takahashi, T.; Mukai, T.; Tanaka, S.; Hosomi, N.; Maruyama, H.; Sakai, N.; Matsumoto, M. Modifications of tau protein after cerebral ischemia and reperfusion in rats are similar to those occurring in Alzheimer’s disease—Hyperphosphorylation and cleavage of 4- and 3-repeat tau. J. Cereb. Blood Flow Metab. 2017, 37, 2441–2457. [Google Scholar] [CrossRef] [Green Version]
- Stamer, K.; Vogel, R.; Thies, E.; Mandelkow, E.; Mandelkow, E.M. Tau blocks traffic of organelles, neurofilaments, and APP vesicles in neurons and enhances oxidative stress. J. Cell. Biol. 2002, 156, 1051–1063. [Google Scholar] [CrossRef]
- Wen, Y.; Yang, S.; Liu, R.; Simpkins, J.W. Transient cerebral ischemia induces site-specific hyperphosphorylation of tau protein. Brain Res. 2004, 1022, 30–38. [Google Scholar] [CrossRef] [PubMed]
- Wen, Y.; Yang, S.; Liu, R.; Brun-Zinkernagel, A.M.; Koulen, P.; Simpkins, J.W. Transient cerebral ischemia induces aberrant neuronal cell cycle re-entry and Alzheimer’s disease-like tauopathy in female rats. J. Biol. Chem. 2004, 279, 22684–22692. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Wen, Y.; Yang, S.H.; Liu, R.; Perez, E.J.; Brun-Ziukemagel, A.M.; Koulen, P.; Simpkins, J.W. Cdk5 is involved in NFT-like tauopathy induced by transient cerebral ischemia in female rats. Biochim. Biophys. Acta 2007, 1772, 473–483. [Google Scholar] [CrossRef] [PubMed]
- Khan, S.; Yuldasheva, N.Y.; Batten, T.F.C.; Pickles, A.R.; Kellett, K.A.B.; Saha, S. Tau pathology and neurochemical changes associated with memory dysfunction in an optimized murine model of global cerebral ischaemia—A potential model for vascular dementia? Neurochem. Int. 2018, 118, 134–144. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Kato, T.; Hirano, A.; Katagiri, T.; Sasaki, H.; Yamada, S. Neurofibrillary tangle formation in the nucleus basalis of Meynert ipsilateral to a massive cerebral infarct. Ann. Neurol. 1988, 23, 620–623. [Google Scholar] [CrossRef] [PubMed]
- Hatsuta, H.; Takao, M.; Nogami, A.; Uchino, A.; Sumikura, H.; Takata, T.; Morimoto, S.; Kanemaru, K.; Adachi, T.; Arai, T.; et al. Tau and TDP-43 accumulation of the basal nucleus of Meynert in individuals with cerebral lobar infarcts or hemorrhage. Acta Neuropathol. Commun. 2019, 7, 49. [Google Scholar] [CrossRef]
- Bi, M.; Gladbach, A.; van Eersel, J.; Ittner, A.; Przybyla, M.; van Hummel, A.; Chua, S.W.; van der Hoven, J.; Lee, W.S.; Muller, J.; et al. Tau exacerbates excitotoxic brain damage in an animal model of stroke. Nat. Commun. 2017, 8, 473. [Google Scholar] [CrossRef] [Green Version]
- Tuo, Q.Z.; Lei, P.; Jackman, K.A.; Li, X.L.; Xiong, H.; Li, X.L.; Liuyang, Z.Y.; Roisman, L.; Zhang, S.T.; Ayton, S.; et al. Tau-mediated iron export prevents ferroptotic damage after ischemic stroke. Mol. Psychiatry 2017, 22, 1520–1530. [Google Scholar] [CrossRef]
- Basurto-Islas, G.; Gu, J.H.; Tung, Y.C.; Liu, F.; Iqbal, K. Mechanism of tau hyperphosphorylation involving lysosomal enzyme asparagine endopeptidase in a mouse model of brain ischemia. J. Alzheimers Dis. 2018, 63, 821–833. [Google Scholar] [CrossRef]
- Bitsch, A.; Horn, C.; Kemmling, Y.; Seipelt, M.; Hellenbrand, U.; Stiefel, M.; Ciesielczyk, B.; Cepek, L.; Bahn, E.; Ratzka, P.; et al. Serum tau protein level as a marker of axonal damage in acute ischemic stroke. Eur. Neurol. 2002, 47, 45–51. [Google Scholar] [CrossRef]
- Kurzepa, J.; Bielewicz, J.; Grabarska, A.; Stelmasiak, Z.; Stryjecka-Zimmer, M.; Bartosik-Psujek, H. Matrix metalloproteinase-9 contributes to the increase of tau protein in serum during acute ischemic stroke. J Clin. Neurosci. 2010, 17, 997–999. [Google Scholar] [CrossRef]
- Bielewicz, J.; Kurzepa, J.; Czekajska-Chehab, E.; Stelmasiak, Z.; Bartosik-Psujek, H. Does serum tau protein predict the outcome of patients with ischemic stroke? J. Mol. Neurosci. 2011, 43, 241–245. [Google Scholar] [CrossRef]
- Mörtberg, E.; Zetterberg, H.; Nordmark, J.; Blennow, K.; Catry, C.; Decraemer, H.; Vanmechelen, E.; Rubertsson, S. Plasma tau protein in comatose patients after cardiac arrest treated with therapeutic hypothermia. Acta Anaesthesiol. Scand. 2011, 55, 1132–1138. [Google Scholar] [CrossRef]
- Randall, J.; Mörtberg, E.; Provuncher, G.K.; Fournier, D.R.; Duffy, D.C.; Rubertsson, S.; Blennow, K.; Zetterberg, H.; Wilson, D.H. Tau proteins in serum predict neurological outcome after hypoxic brain injury from cardiac arrest: Results of a pilot study. Resuscitation 2013, 84, 351–356. [Google Scholar] [CrossRef]
- Lasek-Bal, A.; Jedrzejowska-Szypulka, H.; Rozycka, J.; Bal, W.; Kowalczyk, A.; Holecki, M.; Dulawa, J.; Lewin-Kowalik, J. The presence of tau protein in blood as a potential prognostic factor in stroke patients. J. Physiol. Pharmacol. 2016, 67, 691–696. [Google Scholar]
- De Vos, A.; Bjerke, M.; Brouns, R.; De Roeck, N.; Jacobs, D.; Van den Abbeele, L.; Guldolf, K.; Zetterberg, H.; Blennow, K.; Engelborghs, S.; et al. Neurogranin and tau in cerebrospinal fluid and plasma of patients with acute ischemic stroke. BMC Neurol. 2017, 17, 170. [Google Scholar] [CrossRef] [Green Version]
- Pluta, R.; Bogucka-Kocka, A.; Ułamek-Kozioł, M.; Bogucki, J.; Kocki, J.; Czuczwar, S.J. Ischemic tau protein gene induction as an additional key factor driving development of Alzheimer’s phenotype changes in CA1 area of hippocampus in an ischemic model of Alzheimer’s disease. Pharmacol. Rep. 2018, 70, 881–884. [Google Scholar] [CrossRef]
- Choi, S.; Hong, D.K.; Choi, B.Y.; Suh, S.W. Zinc in the brain: Friend or foe? Int. J. Mol. Sci. 2020, 21, 8941. [Google Scholar] [CrossRef]
- Higashi, Y.; Aratake, T.; Shimizu, T.; Shimizu, S.; Saito, M. Protective role of glutathione in the hippocampus after brain ischemia. Int. J. Mol. Sci. 2021, 22, 7765. [Google Scholar] [CrossRef]
- Yan, N.; Xu, Z.; Qu, C.; Zhang, J. Dimethyl fumarate improves cognitive deficits in chronic cerebral hypoperfusion rats by alleviating inflammation, oxidative stress, and ferroptosis via NRF2/ARE/NF-κB signal pathway. Int. Immunopharmacol. 2021, 98, 107844. [Google Scholar] [CrossRef]
- Takeda, A. Zinc homeostasis and functions of zinc in the brain. Biometals 2001, 14, 343–351. [Google Scholar] [CrossRef]
- Koh, J.Y.; Suh, S.W.; Gwag, B.J.; He, Y.Y.; Hsu, C.Y.; Choi, D.W. The role of zinc in selective neuronal death after transient global cerebral ischemia. Science 1996, 272, 1013–1016. [Google Scholar] [CrossRef]
- Ji, S.G.; Medvedeva, Y.V.; Wang, H.L.; Yin, H.Z.; Weiss, J.H. Mitochondrial Zn2+ accumulation: A potential trigger of hippocampal ischemic injury. Neuroscientist 2019, 25, 126–138. [Google Scholar] [CrossRef]
- Won, S.J.; Yoo, B.H.; Brennan, A.M.; Shin, B.S.; Kauppinen, T.M.; Berman, A.E.; Swanson, R.A.; Suh, S.W. EAAC1 gene deletion alters zinc homeostasis and exacerbates neuronal injury after transient cerebral ischemia. J. Neurosci. 2010, 30, 15409–15418. [Google Scholar] [CrossRef]
- Aratake, T.; Higashi, Y.; Hamada, T.; Ueba, Y.; Shimizu, T.; Shimizu, S.; Yawata, T.; Ueba, T.; Saito, M. The role of diurnal fluctuations in excitatory amino acid carrier 1 levels in post-ischemic hippocampal Zn2+ accumulation. Exp. Neurol. 2021, 336, 113538. [Google Scholar] [CrossRef]
- Bush, A.I.; Pettingell, W.H.; Multhaup, G.; d Paradis, M.; Vonsattel, J.P.; Gusella, J.F.; Beyreuther, K.; Masters, C.L.; Tanzi, R.E. Rapid induction of Alzheimer A beta amyloid formation by zinc. Science 1994, 265, 1464–1467. [Google Scholar] [CrossRef]
- Takeda, A.; Tamano, H.; Tempaku, M.; Sasaki, M.; Uematsu, C.; Sato, S.; Kanazawa, H.; Datki, Z.L.; Adlard, P.A.; Bush, A.I. Extracellular Zn2+ is essential for Amyloid beta1-42-induced cognitive decline in the normal brain and its rescue. J. Neurosci. 2017, 37, 7253–7262. [Google Scholar] [CrossRef] [Green Version]
- De Benedictis, C.A.; Vilella, A.; Grabrucker, A.M. The role of trace metals in Alzheimer’s disease. In Alzheimer’s Disease; Wisniewski, T., Ed.; Codon Publications: Brisbane, Australia, 2019; pp. 85–106. [Google Scholar]
- Berg, D.; Youdim, M.B. Role of iron in neurodegenerative disorders. Top. Magn. Reson. Imaging 2006, 17, 5–17. [Google Scholar] [CrossRef]
- Li, Y.; He, Y.; Guan, Q.; Liu, W.; Han, H.; Nie, Z. Disrupted iron metabolism and ensuing oxidative stress may mediate cognitive dysfunction induced by chronic cerebral hypoperfusion. Biol. Trace Element Res. 2012, 150, 242–248. [Google Scholar] [CrossRef]
- Zhu, K.; Zhu, X.; Sun, S.; Yang, W.; Liu, S.; Tang, Z.; Zhang, R.; Li, J.; Shen, T.; Hei, M. Inhibition of TLR4 prevents hippocampal hypoxic-ischemic injury by regulating ferroptosis in neonatal rats. Exp. Neurol. 2021, 345, 113828. [Google Scholar] [CrossRef]
- Li, J.; Wang, Y.J.; Zhang, M.; Fang, C.Q.; Zhou, H.D. Cerebral ischemia aggravates cognitive impairment in a rat model of Alzheimer’s disease. Life Sci. 2011, 89, 86–92. [Google Scholar] [CrossRef] [PubMed]
- Pluta, R.; Jolkkonen, J.; Cuzzocrea, S.; Pedata, F.; Cechetto, D.; PopaWagner, A. Cognitive impairment with vascular impairment and degeneration. Curr. Neurovasc. Res. 2011, 8, 342–350. [Google Scholar] [CrossRef] [PubMed]
- Cohan, C.H.; Neumann, J.T.; Dave, K.R.; Alekseyenko, A.; Binkert, M.; Stransky, K.; Lin, H.W.; Barnes, C.A.; Wright, C.B.; Perez-Pinzon, M.A. Effect of cardiac arrest on cognitive impairment and hippocampal plasticity in middle-aged rats. PLoS ONE 2015, 10, e0124918. [Google Scholar] [CrossRef] [PubMed]
- Kuroiwa, T.; Bonnekoh, P.; Hossmann, K.A. Locomotor hyperactivity and hippocampal CA1 injury after transient forebrain ischemia in gerbils. Neurosci. Lett. 1991, 122, 141–144. [Google Scholar] [CrossRef]
- Karasawa, Y.; Araki, H.; Otomo, S. Changes in locomotor activity and passive avoidance task performance induced by cerebral ischemia in mongolian gerbils. Stroke 1994, 25, 645–650. [Google Scholar] [CrossRef] [Green Version]
- Langdon, K.D.; Granter-Button, S.; Corbett, D. Persistent behavioral impairments and neuroinflammation following global ischemia in the rat. Eur. J. Neurosci. 2008, 28, 2310–2318. [Google Scholar] [CrossRef]
- Colbourne, F.; Corbett, D. Delayed postischemic hypothermia: A six month survival study using behavioral and histological assessments of neuroprotection. J. Neurosci. 1995, 15, 7250–7260. [Google Scholar] [CrossRef] [Green Version]
- Karhunen, H.; Pitkanen, A.; Virtanen, T.; Gureviciene, I.; Pussinen, R.; Ylinen, A.; Sivenius, J.; Nissinen, J.; Jolkkonen, J. Long-term functional consequences of transient occlusion of the middle cerebral artery in rats: A 1-year follow-up of the development of epileptogenesis and memory impairment in relation to sensorimotor deficits. Epilepsy Res. 2003, 54, 1–10. [Google Scholar] [CrossRef]
- Ishibashi, S.; Kuroiwa, T.; Liyuan, S.; Katsumata, N.; Li, S.; Endo, S.; Mizusawa, H. Long-term cognitive and neuropsychological symptoms after global cerebral ischemia in Mongolian gerbils. Acta Neurochir. 2006, 96, 299–302. [Google Scholar]
- Hossmann, K.A.; Schmidt-Kastner, R.; Ophoff, B.G. Recovery of integrative central nervous function after one hour global cerebro-circulatory arrest in normothermic cat. J. Neurol. Sci. 1987, 77, 305–320. [Google Scholar] [CrossRef]
- Brainin, M.; Tuomilehto, J.; Heiss, W.D.; Bornstein, N.M.; Bath, P.M.; Teuschl, Y.; Richard, E.; Guekht, A.; Quinn, T. Post Stroke Cognition Study Group. Post-stroke cognitive decline: An update and perspectives for clinical research. Eur. J. Neurol. 2015, 22, 229–238. [Google Scholar] [CrossRef]
- Mok, V.C.T.; Lam, B.Y.K.; Wang, Z.; Liu, W.; Au, L.; Leung, E.Y.L.; Chen, S.; Yang, J.; Chu, W.C.W.; Lau, A.Y.L.; et al. Delayed-onset dementia after stroke or transient ischemic attack. Alzheimers Dement. 2016, 12, 1167–1176. [Google Scholar] [CrossRef]
- Portegies, M.L.; Wolters, F.J.; Hofman, A.; Ikram, M.K.; Koudstaal, P.J.; Ikram, M.A. Prestroke vascular pathology and the risk of recurrent stroke and poststroke dementia. Stroke 2016, 47, 2119–2122. [Google Scholar] [CrossRef] [Green Version]
- Kim, J.H.; Lee, Y. Dementia and death after stroke in older adults during a 10-year follow-up: Results from a competing risk model. J. Nutr. Health Aging 2018, 22, 297–301. [Google Scholar] [CrossRef]
- Surawan, J.; Areemit, S.; Tiamkao, S.; Sirithanawuthichai, T.; Saensak, S. Risk factors associated with post-stroke dementia: A systematic review and meta-analysis. Neurol. Int. 2017, 9, 7216. [Google Scholar] [CrossRef]
- Altieri, M.; Di Piero, V.; Pasquini, M.; Gasparini, M.; Vanacore, N.; Vicenzini, E.; Lenzi, G.L. Delayed poststroke dementia: A 4-year follow-up study. Neurology 2004, 62, 2193–2197. [Google Scholar] [CrossRef]
- Pluta, R.; Januszewski, S.; Czuczwar, S.J. Brain ischemia as a prelude to Alzheimer’s disease. Front. Aging Neurosci. 2021, 13, 636653. [Google Scholar] [CrossRef]
- Pluta, R. Brain ischemia as a bridge to Alzheimer’s disease. Neural Regen. Res. 2022, 17, 791–792. [Google Scholar] [CrossRef]
Genes | APP | BACE1 | PSEN1 | PSEN2 | MAPT | |
---|---|---|---|---|---|---|
Survival | ||||||
CA1 sector | ||||||
2 days | ↓ | ↑↑ | ↑ | ↑↑ | ↑↑ | |
7 days | ↑ | ↑ | ↑ | ↑ | ↑ | |
30 days | ↑ | ↓ | ↓ | ↓ | ↓ | |
CA3 sector | ||||||
2 days | ↓ | ↑ | ||||
7 days | ↑ | ↓ | ↑ | ↓ | ↑ | |
30 days | ↑ | ↑ | ↑ |
Publisher’s Note: MDPI stays neutral with regard to jurisdictional claims in published maps and institutional affiliations. |
© 2021 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https://creativecommons.org/licenses/by/4.0/).
Share and Cite
Pluta, R.; Januszewski, S.; Czuczwar, S.J. Post-Ischemic Neurodegeneration of the Hippocampus Resembling Alzheimer’s Disease Proteinopathy. Int. J. Mol. Sci. 2022, 23, 306. https://doi.org/10.3390/ijms23010306
Pluta R, Januszewski S, Czuczwar SJ. Post-Ischemic Neurodegeneration of the Hippocampus Resembling Alzheimer’s Disease Proteinopathy. International Journal of Molecular Sciences. 2022; 23(1):306. https://doi.org/10.3390/ijms23010306
Chicago/Turabian StylePluta, Ryszard, Sławomir Januszewski, and Stanisław J. Czuczwar. 2022. "Post-Ischemic Neurodegeneration of the Hippocampus Resembling Alzheimer’s Disease Proteinopathy" International Journal of Molecular Sciences 23, no. 1: 306. https://doi.org/10.3390/ijms23010306
APA StylePluta, R., Januszewski, S., & Czuczwar, S. J. (2022). Post-Ischemic Neurodegeneration of the Hippocampus Resembling Alzheimer’s Disease Proteinopathy. International Journal of Molecular Sciences, 23(1), 306. https://doi.org/10.3390/ijms23010306