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Chapter 29 - Neuronal Death

from Cellular Responses

Published online by Cambridge University Press:  07 August 2021

Mirna Lechpammer ,
Marc Del Bigio  and
Rebecca Folkerth
By
Marc Del Bigio
Mirna Lechpammer
Affiliation:
New York University School of Medicine
Marc Del Bigio
Affiliation:
University of Manitoba, Canada
Rebecca Folkerth
Affiliation:
New York University School of Medicine
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Summary

The idea that loss of neurons could be associated with disease states and that certain microscopic appearances could be indicative of these arose in the mid to late 1800s. If neurons die, become dysfunctional, or are disconnected following a challenge, functionality of the affected neural circuit is compromised. Depending on the magnitude and localization, this may have relatively mild consequences (such as a learning deficit) or major consequences (such as developmental delay, epilepsy, cerebral palsy, or death). We are interested in selective or regional neuron death because they can help to explain the neurologic dysfunction experienced by an individual or give insight into the pathologic process that preceded death.

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Perinatal Neuropathology , pp. 145 - 154
Publisher: Cambridge University Press
Print publication year: 2021

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References

Lockshin, RA, Williams, CM. Programmed cell death–I. Cytology of degeneration in the intersegmental muscles of the pernyi silkmoth. J Insect Physiol. 1965;11:123–33.Google ScholarPubMed
Kerr, JF, Wyllie, AH, Currie, AR. Apoptosis: a basic biological phenomenon with wide-ranging implications in tissue kinetics. Br J Cancer. 1972;26(4):239–57.CrossRefGoogle ScholarPubMed
Schweichel, JU, Merker, HJ. The morphology of various types of cell death in prenatal tissues. Teratology. 1973;7(3):253–66.Google Scholar
Tsujimoto, Y. Multiple ways to die: non-apoptotic forms of cell death. Acta Oncol. 2012;51(3):293–300.Google Scholar
Denaxa, M, Neves, G, Rabinowitz, A, Kemlo, S, Liodis, P, Burrone, J, et al. Modulation of apoptosis controls inhibitory interneuron number in the cortex. Cell Rep. 2018;22(7):1710–21.Google Scholar
Orrenius, S, McConkey, DJ, Jones, DP, Nicotera, P. Ca2+-activated mechanisms in toxicity and programmed cell death. ISI Atlas Sci: Pharmacol. 1988;2(4):319–24.Google Scholar
Burke, RE, Kholodilov, NG. Programmed cell death: does it play a role in Parkinson’s disease? Ann Neurol. 1998;44(3 Suppl 1):S126–33.CrossRefGoogle ScholarPubMed
Zhang, L, Kokkonen, G, Roth, GS. Identification of neuronal programmed cell death in situ in the striatum of normal adult rat brain and its relationship to neuronal death during aging. Brain Res. 1995;677(1):177–9.Google Scholar
Bursch, W, Kleine, L, Tenniswood, M. The biochemistry of cell death by apoptosis. Biochem Cell Biol. 1990;68(9):1071–4.Google Scholar
Goya, RG. Role of programmed cell death in the aging process: an unexplored possibility. Gerontology. 1986;32(1):37–42.Google Scholar
Krantic, S, Mechawar, N, Reix, S, Quirion, R. Molecular basis of programmed cell death involved in neurodegeneration. Trends Neurosci. 2005;28(12):670–6.CrossRefGoogle ScholarPubMed
Galluzzi, L, Vitale, I, Aaronson, SA, Abrams, JM, Adam, D, Agostinis, P, et al. Molecular mechanisms of cell death: recommendations of the Nomenclature Committee on Cell Death 2018. Cell Death Differ. 2018;25(3):486–541.Google Scholar
Napoletano, F, Baron, O, Vandenabeele, P, Mollereau, B, Fanto, M. Intersections between regulated cell death and autophagy. Trends Cell Biol. 2019;29(4):323–38.CrossRefGoogle ScholarPubMed
Virchow, R. Die Cellularpathologie in ihrer Begründung auf physiologische und pathologische Gewebelehre. 1st ed. Berlin: August Hirschwald; 1858.Google Scholar
King, LS. Studies on eastern equine encephalomyelitis. I. Histopathology of the nervous system in the guinea pig. J Exp Med. 1938;68(5):677–92.CrossRefGoogle ScholarPubMed
Weller, SD, Norman, RM. Epilepsy due to birth injury in one of identical twins. Arch Dis Child. 1955;30(153):453–6.CrossRefGoogle ScholarPubMed
Meriwether, LS, Hager, H, Scholz, W. Kernicterus; hypoxemia, significant pathogenic factor. AMA Arch Neurol Psychiatry. 1955;73(3):293–301.CrossRefGoogle ScholarPubMed
Levine, S. Anoxic-ischemic encephalopathy in rats. Am J Pathol. 1960;36:1–17.Google ScholarPubMed
Claireaux, A. Haemolytic disease of the newborn: Part I. A clinical-pathological study of 157 cases. Arch Dis Child. 1950;25(121):61–80.Google Scholar
Lossi, L, Castagna, C, Merighi, A. Neuronal cell death: an overview of its different forms in central and peripheral neurons. Methods Mol Biol. 2015;1254:1–18.CrossRefGoogle ScholarPubMed
Fricker, M, Tolkovsky, AM, Borutaite, V, Coleman, M, Brown, GC. Neuronal cell death. Physiol Rev. 2018;98(2):813–80.CrossRefGoogle ScholarPubMed
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(9):2189–94.Google Scholar
Elmore, SA, Dixon, D, Hailey, JR, Harada, T, Herbert, RA, Maronpot, RR, et al. Recommendations from the INHAND Apoptosis/Necrosis Working Group. Toxicol Pathol. 2016;44(2):173–88.CrossRefGoogle ScholarPubMed
Kroemer, G, Galluzzi, L, Vandenabeele, P, Abrams, J, Alnemri, ES, Baehrecke, EH, et al. Classification of cell death: recommendations of the Nomenclature Committee on Cell Death 2009. Cell Death Differ. 2009;16(1):3–11.Google Scholar
Galluzzi, L, Bravo-San Pedro, JM, Vitale, I, Aaronson, SA, Abrams, JM, Adam, D, et al. Essential versus accessory aspects of cell death: recommendations of the NCCD 2015. Cell Death Differ. 2015;22(1):58–73.CrossRefGoogle ScholarPubMed
Galluzzi, L, Vitale, I, Abrams, JM, Alnemri, ES, Baehrecke, EH, Blagosklonny, MV, et al. Molecular definitions of cell death subroutines: recommendations of the Nomenclature Committee on Cell Death 2012. Cell Death Differ. 2012;19(1):107–20.Google Scholar
Martin, LJ, Chang, Q. DNA damage response and repair, DNA methylation, and cell death in human neurons and experimental animal neurons are different. J Neuropathol Exp Neurol. 2018;77(7):636–55.CrossRefGoogle ScholarPubMed
Tagaya, M, Liu, KF, Copeland, B, Seiffert, D, Engler, R, Garcia, JH, et al. DNA scission after focal brain ischemia. Temporal differences in two species. Stroke. 1997;28(6):1245–54.CrossRefGoogle ScholarPubMed
Elmore, S. Apoptosis: a review of programmed cell death. Toxicol Pathol. 2007;35(4):495–516.Google Scholar
Mnatsakanyan, N, Beutner, G, Porter, GA, Alavian, KN, Jonas, EA. Physiological roles of the mitochondrial permeability transition pore. J Bioenerg Biomembr. 2017;49(1):13–25.Google Scholar
Lossi, L, Castagna, C, Merighi, A. Caspase-3 mediated cell death in the normal development of the mammalian cerebellum. Int J Mol Sci. 2018;19(12):ii:E3999.Google Scholar
Srinivasan, A, Roth, KA, Sayers, RO, Shindler, KS, Wong, AM, Fritz, LC, et al. In situ immunodetection of activated caspase-3 in apoptotic neurons in the developing nervous system. Cell Death Differ. 1998;5(12):1004–16.CrossRefGoogle ScholarPubMed
Love, S, Barber, R, Srinivasan, A, Wilcock, GK. Activation of caspase-3 in permanent and transient brain ischaemia in man. Neuroreport. 2000;11(11):2495–9.Google Scholar
Stadelman, C, Mews, I, Srinivasan, A, Deckwerth, TL, Lassmann, H, Bruck, W. Expression of cell death-associated proteins in neuronal apoptosis associated with pontosubicular neuron necrosis. Brain Pathol. 2001;11(3):273–81.Google Scholar
Machaalani, R, Radford, JL, Waters, KA. Tissue fixation effects on immunohistochemical staining of caspase-3 in brain tissue. Appl Immunohistochem Mol Morphol. 2007;15(4):463–70.Google Scholar
Rossiter, JP, Anderson, LL, Yang, F, Cole, GM. Caspase-3 activation and caspase-like proteolytic activity in human perinatal hypoxic-ischemic brain injury. Acta Neuropathol. 2002;103(1):66–73.Google Scholar
Schafer, MK, Pfeiffer, A, Jaeckel, M, Pouya, A, Dolga, AM, Methner, A. Regulators of mitochondrial Ca(2+) homeostasis in cerebral ischemia. Cell Tissue Res. 2014;357(2):395–405.CrossRefGoogle ScholarPubMed
Nagley, P, Higgins, GC, Atkin, JD, Beart, PM. Multifaceted deaths orchestrated by mitochondria in neurones. Biochim Biophys Acta. 2010;1802(1):167–85.Google Scholar
Samejima, K, Earnshaw, WC. Trashing the genome: the role of nucleases during apoptosis. Nat Rev Mol Cell Biol. 2005;6(9):677–88.CrossRefGoogle ScholarPubMed
Larsen, BD, Sorensen, CS. The caspase-activated DNase: apoptosis and beyond. FEBS J. 2017;284(8):1160–70.CrossRefGoogle ScholarPubMed
Ruchaud, S, Korfali, N, Villa, P, Kottke, TJ, Dingwall, C, Kaufmann, SH, et al. Caspase-6 gene disruption reveals a requirement for lamin A cleavage in apoptotic chromatin condensation. EMBO J. 2002;21(8):1967–77.Google Scholar
Miller, JA, Ding, SL, Sunkin, SM, Smith, KA, Ng, L, Szafer, A, et al. Transcriptional landscape of the prenatal human brain. Nature. 2014;508(7495):199–206.Google Scholar
Hyman, BT, Yuan, J. Apoptotic and non-apoptotic roles of caspases in neuronal physiology and pathophysiology. Nat Rev Neurosci. 2012;13(6):395–406.Google Scholar
Hooker, DJ, Mobarok, M, Anderson, JL, Rajasuriar, R, Gray, LR, Ellett, AM, et al. A new way of measuring apoptosis by absolute quantitation of inter-nucleosomally fragmented genomic DNA. Nucleic Acids Res. 2012;40(15):e113.Google Scholar
Lesauskaite, V, Epistolato, MC, Ivanoviene, L, Tanganelli, P. Apoptosis of cardiomyocytes in explanted and transplanted hearts. Comparison of results from in situ TUNEL, ISEL, and ISOL reactions. Am J Clin Pathol. 2004;121(1):108–16.Google Scholar
Charriaut-Marlangue, C, Ben-Ari, Y. A cautionary note on the use of the TUNEL stain to determine apoptosis. Neuroreport. 1995;7(1):61–4.Google Scholar
Burke, C, Gobe, G. Pontosubicular apoptosis (“necrosis”) in human neonates with intrauterine growth retardation and placental infarction. Virchows Arch. 2005;446(6):640–5.Google Scholar
Zille, M, Farr, TD, Przesdzing, I, Muller, J, Sommer, C, Dirnagl, U, et al. Visualizing cell death in experimental focal cerebral ischemia: promises, problems, and perspectives. J Cereb Blood Flow Metab. 2012;32(2):213–31.Google Scholar
Didenko, VV, Ngo, H, Minchew, CL, Boudreaux, DJ, Widmayer, MA, Baskin, DS. Visualization of irreparable ischemic damage in brain by selective labeling of double strand blunt-ended DNA breaks. Mol Med. 2002;8(12):818–23.Google Scholar
Hornsby, PJ, Didenko, VV. In situ ligation: a decade and a half of experience. Methods Mol Biol. 2011;682:49–63.Google Scholar
Nakajima, YI, Kuranaga, E. Caspase-dependent non-apoptotic processes in development. Cell Death Differ. 2017;24(8):1422–30.Google Scholar
Kumar, A, Rothman, JH. Cell death: hook, line and linker. Curr Biol. 2007;17(8):R286-9.Google Scholar
Kutscher, LM, Shaham, S. Non-apoptotic cell death in animal development. Cell Death Differ. 2017;24(8):1326–36.Google Scholar
Gudipaty, SA, Conner, CM, Rosenblatt, J, Montell, DJ. Unconventional ways to live and die: cell death and survival in development, homeostasis, and disease. Annu Rev Cell Dev Biol. 2018;34:311–32.Google Scholar
Loh, KY, Wang, Z, Liao, P. Oncotic cell death in stroke. Rev Physiol Biochem Pharmacol. 2019;176:37–64.CrossRefGoogle ScholarPubMed
Yagami, T, Yamamoto, Y, Koma, H. Pathophysiological roles of intracellular proteases in neuronal development and neurological diseases. Mol Neurobiol. 2019;56(5):3090–112.Google Scholar
Czogalla, A, Sikorski, AF. Spectrin and calpain: a ‘target’ and a ‘sniper’ in the pathology of neuronal cells. Cell Mol Life Sci. 2005;62(17):1913–24.Google Scholar
Vanderklish, PW, Bahr, BA. The pathogenic activation of calpain: a marker and mediator of cellular toxicity and disease states. Int J Exp Pathol. 2000;81(5):323–39.Google Scholar
McCracken, E, Hunter, AJ, Patel, S, Graham, DI, Dewar, D. Calpain activation and cytoskeletal protein breakdown in the corpus callosum of head-injured patients. J Neurotrauma. 1999;16(9):749–61.Google Scholar
Fujikawa, DG. The role of excitotoxic programmed necrosis in acute brain injury. Comput Struct Biotechnol J. 2015;13:212–21.Google Scholar
Varela-Ramirez, A, Abendroth, J, Mejia, AA, Phan, IQ, Lorimer, DD, Edwards, TE, et al. Structure of acid deoxyribonuclease. Nucleic Acids Res. 2017;45(10):6217–27.Google Scholar
Minchew, CL, Didenko, VV. Dual detection of nucleolytic and proteolytic markers of lysosomal cell death: DNase ii-type breaks and cathepsin d. Methods Mol Biol. 2017;1554:229–36.Google Scholar
Uhlen, M, Fagerberg, L, Hallstrom, BM, Lindskog, C, Oksvold, P, Mardinoglu, A, et al. Proteomics. Tissue-based map of the human proteome. Science. 2015;347(6220):1260419.Google Scholar
Grassi Zucconi, G, Cosi, C, Palmieri, M, Furia, A, Bassetti, MA, Carsana, A. A pancreatic-like ribonuclease is synthesized in rat brain. Brain Res Mol Brain Res. 1992;14(1–2):1–6.Google Scholar
Morita, T, Sanda, A, Takizawa, Y, Ohgi, K, Irie, M. Distribution of a kidney acid-ribonuclease-like enzyme and the other ribonucleases in bovine organs and body fluids. Agric Biol Chem. 1987;51(10):2751–61.Google Scholar
Albrecht, J, Yanagihara, T. Effect of anoxia and ischemia on ribonuclease activity in brain. J Neurochem. 1979;32(3):1131–3.Google Scholar
Thornton, C, Hagberg, H. Role of mitochondria in apoptotic and necroptotic cell death in the developing brain. Clin Chim Acta. 2015;451(PartA):35–8.Google Scholar
Grootjans, S, Vanden Berghe, T, Vandenabeele, P. Initiation and execution mechanisms of necroptosis: an overview. Cell Death Differ. 2017;24(7):1184–95.Google Scholar
Hribljan, V, Lisjak, D, Petrovic, DJ, Mitrecic, D. Necroptosis is one of the modalities of cell death accompanying ischemic brain stroke: from pathogenesis to therapeutic possibilities. Croat Med J. 2019;60(2):121–6.Google Scholar
Liu, T, Bao, YH, Wang, Y, Jiang, JY. The role of necroptosis in neurosurgical diseases. Braz J Med Biol Res. 2015;48(4):292–8.Google Scholar
Dunai, Z, Bauer, PI, Mihalik, R. Necroptosis: biochemical, physiological and pathological aspects. Pathol Oncol Res. 2011;17(4):791–800.Google Scholar
Jouan-Lanhouet, S, Riquet, F, Duprez, L, Vanden Berghe, T, Takahashi, N, Vandenabeele, P. Necroptosis, in vivo detection in experimental disease models. Semin Cell Dev Biol. 2014;35:2–13.CrossRefGoogle ScholarPubMed
Degterev, A, Zhou, W, Maki, JL, Yuan, J. Assays for necroptosis and activity of RIP kinases. Methods Enzymol. 2014;545:1–33.Google Scholar
Ofengeim, D, Ito, Y, Najafov, A, Zhang, Y, Shan, B, DeWitt, JP, et al. Activation of necroptosis in multiple sclerosis. Cell Rep. 2015;10(11):1836–49.CrossRefGoogle ScholarPubMed
Fan, H, Tang, HB, Kang, J, Shan, L, Song, H, Zhu, K, et al. Involvement of endoplasmic reticulum stress in the necroptosis of microglia/macrophages after spinal cord injury. Neuroscience. 2015;311:362–73.Google Scholar
Wang, Y, An, R, Umanah, GK, Park, H, Nambiar, K, Eacker, SM, et al. A nuclease that mediates cell death induced by DNA damage and poly(ADP-ribose) polymerase-1. Science. 2016;354(6308):pii:aad6872.Google Scholar
Sairanen, T, Szepesi, R, Karjalainen-Lindsberg, ML, Saksi, J, Paetau, A, Lindsberg, PJ. Neuronal caspase-3 and PARP-1 correlate differentially with apoptosis and necrosis in ischemic human stroke. Acta Neuropathol. 2009;118(4):541–52.Google Scholar
Stockwell, BR, Friedmann Angeli, JP, Bayir, H, Bush, AI, Conrad, M, Dixon, SJ, et al. Ferroptosis: a regulated cell death nexus linking metabolism, redox biology, and disease. Cell. 2017;171(2):273–85.Google Scholar
Li, Q, Weiland, A, Chen, X, Lan, X, Han, X, Durham, F, et al. Ultrastructural characteristics of neuronal death and white matter injury in mouse brain tissues after intracerebral hemorrhage: coexistence of ferroptosis, autophagy, and necrosis. Front Neurol. 2018;9:581.Google Scholar
Wenzel, SE, Tyurina, YY, Zhao, J, St Croix, CM, Dar, HH, Mao, G, et al. PEBP1 wardens ferroptosis by enabling lipoxygenase generation of lipid death signals. Cell. 2017;171(3):628–41.Google Scholar
Cui, D, Sun, D, Wang, X, Yi, L, Kulikowicz, E, Reyes, M, et al. Impaired autophagosome clearance contributes to neuronal death in a piglet model of neonatal hypoxic-ischemic encephalopathy. Cell Death Dis. 2017;8(7):e2919.Google Scholar
Galluzzi, L, Pedro, JM, Blomgren, K, Kroemer, G. Autophagy in acute brain injury. Nat Rev Neurosci. 2016;17(8):467–84.Google Scholar
Descloux, C, Ginet, V, Clarke, PG, Puyal, J, Truttmann, AC. Neuronal death after perinatal cerebral hypoxia-ischemia: Focus on autophagy-mediated cell death. Int J Dev Neurosci. 2015;45:75–85.CrossRefGoogle ScholarPubMed
Button, RW, Luo, S, Rubinsztein, DC. Autophagic activity in neuronal cell death. Neurosci Bull. 2015;31(4):382–94.CrossRefGoogle ScholarPubMed
Uchiyama, Y, Koike, M, Shibata, M, Sasaki, M. Autophagic neuron death. Methods Enzymol. 2009;453:33–51.Google Scholar
Tang, D, Kang, R, Berghe, TV, Vandenabeele, P, Kroemer, G. The molecular machinery of regulated cell death. Cell Res. 2019;29(5):347–64.Google Scholar
Weilinger, NL, Maslieieva, V, Bialecki, J, Sridharan, SS, Tang, PL, Thompson, RJ. Ionotropic receptors and ion channels in ischemic neuronal death and dysfunction. Acta Pharmacol Sin. 2013;34(1):39–48.Google Scholar
Serwach, K, Gruszczynska-Biegala, J. STIM proteins and glutamate receptors in neurons: role in neuronal physiology and neurodegenerative diseases. Int J Mol Sci. 2019;20(9):E2289.Google Scholar
Back, SA, Rosenberg, PA. Pathophysiology of glia in perinatal white matter injury. Glia. 2014;62(11):1790–815.Google Scholar
Back, SA. White matter injury in the preterm infant: pathology and mechanisms. Acta Neuropathol. 2017;134(3):331–49.Google Scholar
Fujikawa, DG. Activation of caspase-independent programmed pathways in seizure-induced neuronal necrosis. In: Fujikawa, DG, editor. Acute Neuronal Injury. New York: Springer; 2018. pp. 191–211.Google Scholar
Olney, JW, Rhee, V, Ho, OL. Kainic acid: a powerful neurotoxic analogue of glutamate. Brain Res. 1974;77(3):507–12.Google Scholar
Olney, JW. Glutamate-induced neuronal necrosis in the infant mouse hypothalamus. An electron microscopic study. J Neuropathol Exp Neurol. 1971;30(1):75–90.CrossRefGoogle ScholarPubMed
Bano, D, Ankarcrona, M. Beyond the critical point: An overview of excitotoxicity, calcium overload and the downstream consequences. Neurosci Lett. 2018;663:79–85.Google Scholar
Curcio, M, Salazar, IL, Mele, M, Canzoniero, LM, Duarte, CB. Calpains and neuronal damage in the ischemic brain: The swiss knife in synaptic injury. Prog Neurobiol. 2016;143:1–35.CrossRefGoogle ScholarPubMed
Bonfoco, E, Krainc, D, Ankarcrona, M, Nicotera, P, Lipton, SA. Apoptosis and necrosis: two distinct events induced, respectively, by mild and intense insults with N-methyl-D-aspartate or nitric oxide/superoxide in cortical cell cultures. Proc Natl Acad Sci U S A. 1995;92(16):7162–6.CrossRefGoogle ScholarPubMed
Petito, CK, Pulsinelli, WA. Sequential development of reversible and irreversible neuronal damage following cerebral ischemia. J Neuropathol Exp Neurol. 1984;43(2):141–53.Google Scholar
Garcia, JH, Liu, KF, Ho, KL. Neuronal necrosis after middle cerebral artery occlusion in Wistar rats progresses at different time intervals in the caudoputamen and the cortex. Stroke. 1995;26:636–43.Google Scholar
Pulsinelli, WA, Brierley, JB, Plum, F. Temporal profile of neuronal damage in a model of transient forebrain ischemia. Ann Neurol. 1982;11(5):491–8.Google Scholar
Schmued, LC, Stowers, CC, Scallet, AC, Xu, L. Fluoro-Jade C results in ultra high resolution and contrast labeling of degenerating neurons. Brain Res. 2005;1035(1):24–31.Google Scholar
Xu, X, Lai, Y, Hua, ZC. Apoptosis and apoptotic body: disease message and therapeutic target potentials. Biosci Rep. 2019;39(1):BSR20180992.Google Scholar
Shen, Y, Wang, Z, Li, F, Sun, L. Morphological characteristics of eosinophilic neuronal death after transient unilateral forebrain ischemia in Mongolian gerbils. Neuropathology. 2016;36(3):227–36.Google Scholar
Nitatori, T, Sato, N, Waguri, S, Karasawa, Y, Araki, H, Shibanai, K, et al. Delayed neuronal death in the CA1 pyramidal cell layer of the gerbil hippocampus following transient ischemia is apoptosis. J Neurosci. 1995;15(2):1001–11.Google Scholar
Bartus, RT, Dean, RL, Mennerick, S, Eveleth, D, Lynch, G. Temporal ordering of pathogenic events following transient global ischemia. Brain Res. 1998;790(1–2):1–13.Google Scholar
Sun, L, Kuroiwa, T, Ishibashi, S, Katsumata, N, Endo, S, Mizusawa, H. Transition of areas of eosinophilic neurons and reactive astrocytes to delayed cortical infarcts after transient unilateral forebrain ischemia in Mongolian gerbils. Acta Neuropathol. 2006;111(1):21–8.Google Scholar
Garcia, JH, Liu, KF, Ye, ZR, Gutierrez, JA. Incomplete infarct and delayed neuronal death after transient middle cerebral artery occlusion in rats. Stroke. 1997;28(11):2303–9.Google Scholar
Colbourne, F, Li, H, Buchan, AM, Clemens, JA. Continuing postischemic neuronal death in CA1: influence of ischemia duration and cytoprotective doses of NBQX and SNX-111 in rats. Stroke. 1999;30(3):662–8.Google Scholar
Friede, RL. Developmental Neuropathology. 2nd edition. Berlin: Springer Verlag; 1989.Google Scholar
Marin-Padilla, M. Developmental neuropathology and impact of perinatal brain damage. III: Gray matter lesions of the neocortex. J Neuropathol Exp Neurol. 1999;58(5):407–29.Google Scholar
Mito, T, Becker, LE, Takashima, S. Neuropathology of central respiratory dysfunction in infancy. Pediatr Neurosurg. 1991;17(2):80–7.Google Scholar
DiMario, FJ, Jr., Clancy, R. Symmetrical thalamic degeneration with calcifications of infancy. Am J Dis Child. 1989;143(9):1056–60.Google Scholar
Rosales, RK, Riggs, HE. Symmetrical thalamic degeneration in infants. J Neuropathol Exp Neurol. 1962;21:372–6.CrossRefGoogle ScholarPubMed
Parisi, JE, Collins, GH, Kim, RC, Crosley, CJ. Prenatal symmetrical thalamic degeneration with flexion spasticity at birth. Ann Neurol. 1983;13(1):94–7.Google Scholar
Leestma, JE, Martin, E. An electron probe and histochemical study of the “ferruginated” neuron. Arch Pathol. 1968;86(6):597–605.Google Scholar
Gayoso, MJ, Al-Majdalawi, A, Garrosa, M, Calvo, B, Diaz-Flores, L. Selective calcification of rat brain lesions caused by systemic administration of kainic acid. Histol Histopathol. 2003;18(3):855–69.Google Scholar
Oehmichen, M. Vitality and time course of wounds. Forensic Sci Int. 2004;144(2–3):221–31.Google Scholar
Portera-Cailliau, C, Price, DL, Martin, LJ. Excitotoxic neuronal death in the immature brain is an apoptosis-necrosis morphological continuum. J Comp Neurol. 1997;378(1):70–87.Google Scholar
Thornton, C, Leaw, B, Mallard, C, Nair, S, Jinnai, M, Hagberg, H. Cell death in the developing brain after hypoxia-ischemia. Front Cell Neurosci. 2017;11:248.Google Scholar
Kuan, CY, Roth, KA, Flavell, RA, Rakic, P. Mechanisms of programmed cell death in the developing brain. Trends Neurosci. 2000;23(7):291–7.Google Scholar
Krajewska, M, Mai, JK, Zapata, JM, Ashwell, KW, Schendel, SL, Reed, JC, et al. Dynamics of expression of apoptosis-regulatory proteins Bid, Bcl-2, Bcl-X, Bax and Bak during development of murine nervous system. Cell Death Differ. 2002;9(2):145–57.Google Scholar
Ludwig-Galezowska, AH, Flanagan, L, Rehm, M. Apoptosis repressor with caspase recruitment domain, a multifunctional modulator of cell death. J Cell Mol Med. 2011;15(5):1044–53.Google Scholar
Yuan, J, Amin, P, Ofengeim D. Necroptosis and RIPK1-mediated neuroinflammation in CNS diseases. Nat Rev Neurosci. 2019;20(1):19–33.Google Scholar
Hill, CS, Coleman, MP, Menon, DK. Traumatic axonal injury: mechanisms and translational opportunities. Trends Neurosci. 2016;39(5):311–24.Google Scholar
Cornejo, VH, Luarte, A, Couve, A. Global and local mechanisms sustain axonal proteostasis of transmembrane proteins. Traffic. 2017;18(5):255–66.Google Scholar
Iwata, A, Stys, PK, Wolf, JA, Chen, XH, Taylor, AG, Meaney, DF, et al. Traumatic axonal injury induces proteolytic cleavage of the voltage-gated sodium channels modulated by tetrodotoxin and protease inhibitors. J Neurosci. 2004;24(19):4605–13.CrossRefGoogle ScholarPubMed
Simon, DJ, Weimer, RM, McLaughlin, T, Kallop, D, Stanger, K, Yang, J, et al. A caspase cascade regulating developmental axon degeneration. J Neurosci. 2012;32(49):17540–53.Google Scholar
Arrazola, MS, Saquel, C, Catalan, RJ, Barrientos, SA, Hernandez, DE, Martinez, NW, et al. Axonal degeneration is mediated by necroptosis activation. J Neurosci. 2019;39(20):3832–44.Google Scholar
Arrazola, MS, Court, FA. Compartmentalized necroptosis activation in excitotoxicity-induced axonal degeneration: a novel mechanism implicated in neurodegenerative disease pathology. Neural Regen Res. 2019;14(8):1385–6.Google Scholar
Hernandez, DE, Salvadores, NA, Moya-Alvarado, G, Catalan, RJ, Bronfman, FC, Court, FA. Axonal degeneration induced by glutamate excitotoxicity is mediated by necroptosis. J Cell Sci. 2018;131(22):jcs214684.Google Scholar
Ding, C, Hammarlund, M. Mechanisms of injury-induced axon degeneration. Curr Opin Neurobiol. 2019;57:171–8.Google Scholar
Sherriff, FE, Bridges, LR, Gentleman, SM, Sivaloganathan, S, Wilson, S. Markers of axonal injury in post mortem human brain. Acta Neuropathol. 1994;88(5):433–9.Google Scholar
Baiden Amissah, K, Joashi, U, Blumberg, R, Mehmet, H, Edwards, AD, Cox, PM. Expression of amyloid precursor protein (beta-APP) in the neonatal brain following hypoxic ischaemic injury. Neuropathol Appl Neurobiol. 1998;24(5):346–52.Google Scholar
Bell, JE, Becher, JC, Wyatt, B, Keeling, JW, McIntosh, N. Brain damage and axonal injury in a Scottish cohort of neonatal deaths. Brain. 2005;128(Pt. 5):1070–81.Google Scholar
Johnson, VE, Stewart, W, Weber, MT, Cullen, DK, Siman, R, Smith, DH. SNTF immunostaining reveals previously undetected axonal pathology in traumatic brain injury. Acta Neuropathol. 2016;131(1):115–35.Google Scholar
Liu, CH, Rasband, MN. Axonal spectrins: nanoscale organization, functional domains and spectrinopathies. Front Cell Neurosci. 2019;13:234.Google Scholar
Siman, R, Baudry, M, Lynch, G. Brain fodrin: substrate for calpain I, an endogenous calcium-activated protease. Proc Natl Acad Sci U S A. 1984;81(11):3572–6.Google Scholar
Sokolowski, JD, Gamage, KK, Heffron, DS, Leblanc, AC, Deppmann, CD, Mandell, JW. Caspase-mediated cleavage of actin and tubulin is a common feature and sensitive marker of axonal degeneration in neural development and injury. Acta Neuropathol Commun. 2014;2:16.Google Scholar
Maor-Nof, M, Yaron, A. Neurite pruning and neuronal cell death: spatial regulation of shared destruction programs. Curr Opin Neurobiol. 2013;23(6):990–6.Google Scholar

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