Erratum: Degradation of βII-Spectrin Protein by Calpain-2 and Caspase-3 Under Neurotoxic and Traumatic Brain Injury Conditions (Mol Neurobiol, (2015) 52, 1, (696-709), 10.1007/s12035-014-8898-z);Degradation of βII-Spectrin Protein by Calpain-2 and Caspase-3 Under Neurotoxic and Traumatic Brain Injury Conditions

Molecular Neurobiology

Volumn 52, Issue 1, 2015, Pages 696-709

  Kobeissy, Firas H ^a,d   Liu, Ming Cheng ^a   Yang, Zhihui ^a   Zhang, Zhiqun ^a   Zheng, Wenrong ^a   Glushakova, Olena ^b   Mondello, Stefania ^c   Anagli, John ^b   Hayes, Ronald L ^b   Wang, Kevin K W ^a  

^a UNIVERSITY OF FLORIDA HEALTH   (United States)

^b BANYAN BIOMARKERS INC   (United States)

^c UNIVERSITY OF MESSINA   (Italy)

^d AMERICAN UNIVERSITY OF BEIRUT   (Lebanon)

Author keywords

Calpain 2; Caspase 3; Cell death; Neurodegeneration; Protease; TBI; II Spectrin apoptotic

Indexed keywords

BETA2 SPECTRIN; CALPAIN 2; CALPAIN 3; SPECTRIN; UNCLASSIFIED DRUG; CALPAIN; CASPASE 3; NEUROTOXIN; PROTEINASE INHIBITOR;

ADULT; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; BRAIN CORTEX; BRAIN NERVE CELL; CONTROLLED STUDY; ENZYME ACTIVATION; EXCITOTOXICITY; HIPPOCAMPUS; IN VIVO STUDY; MALE; MOLECULAR WEIGHT; NERVE CELL NECROSIS; NEUROTOXICITY; NONHUMAN; PROTEIN ANALYSIS; PROTEIN DEGRADATION; RAT; SIGNAL TRANSDUCTION; TRAUMATIC BRAIN INJURY; ANIMAL; BRAIN INJURY; CELL CULTURE; DRUG EFFECTS; HUMAN; IMMUNOBLOTTING; METABOLISM; NECROSIS; PATHOLOGY; SPRAGUE DAWLEY RAT; TIME FACTOR; TOXICITY AND INTOXICATION;

ANIMALS; APOPTOSIS; BRAIN INJURIES; CALPAIN; CASPASE 3; CELLS, CULTURED; CEREBRAL CORTEX; HIPPOCAMPUS; HUMANS; IMMUNOBLOTTING; MALE; NECROSIS; NEUROTOXICITY SYNDROMES; NEUROTOXINS; PROTEASE INHIBITORS; PROTEOLYSIS; RATS, SPRAGUE-DAWLEY; SPECTRIN; TIME FACTORS;

EID: 84937979033     PISSN: 08937648     EISSN: 15591182     Source Type: Journal    
DOI: 10.1007/s12035-017-0764-3     Document Type: Erratum

References (86)

1. Reeves TM, Greer JE, Vanderveer AS, Phillips LL (2010) Proteolysis of submembrane cytoskeletal proteins ankyrin-G and alphaII-spectrin following diffuse brain injury: a role in white matter vulnerability at nodes of Ranvier. Brain Pathol 20(6):1055–1068
2. Kinnunen KM, Greenwood R, Powell JH, Leech R, Hawkins PC, Bonnelle V, Patel MC, Counsell SJ, Sharp DJ (2011) White matter damage and cognitive impairment after traumatic brain injury. Brain 134(Pt 2):449–463
3. Kondo K, Maruishi M, Ueno H, Sawada K, Hashimoto Y, Ohshita T, Takahashi T, Ohtsuki T, Matsumoto M (2010) The pathophysiology of prospective memory failure after diffuse axonal injury–lesion-symptom analysis using diffusion tensor imaging. BMC Neurosci 11:147
4. Bennett M, O’Brien DP, Phillips JP, Farrell MA (1995) Clinicopathologic observations in 100 consecutive patients with fatal head injury admitted to a neurosurgical unit. Irish Med J 88(2):60–62
5. Kampfl A, Posmantur RM, Zhao X, Schmutzhard E, Clifton GL, Hayes RL (1997) Mechanisms of calpain proteolysis following traumatic brain injury: implications for pathology and therapy: implications for pathology and therapy: a review and update. J Neurotrauma 14(3):121–134
6. Buki A, Okonkwo DO, Wang KK, Povlishock JT (2000) Cytochrome c release and caspase activation in traumatic axonal injury. J Neurosci 20(8):2825–2834
7. Medana IM, Esiri MM (2003) Axonal damage: a key predictor of outcome in human CNS diseases. Brain 126(Pt 3):515–530
8. Gale SD, Johnson SC, Bigler ED, Blatter DD (1995) Nonspecific white matter degeneration following traumatic brain injury. J Int Neuropsychol Soc 1(1):17–28
9. Bramlett HM, Dietrich WD (2002) Quantitative structural changes in white and gray matter 1 year following traumatic brain injury in rats. Acta Neuropathol 103(6):607–614
10. Ng HK, Mahaliyana RD, Poon WS (1994) The pathological spectrum of diffuse axonal injury in blunt head trauma: assessment with axon and myelin strains. Clin Neurol Neurosurg 96(1):24–31
11. Liu MC, Kobeissy F, Zheng W, Zhang Z, Hayes RL, Wang KK (2010) Dual vulnerability of tau to calpains and caspase-3 proteolysis under neurotoxic and neurodegenerative conditions. ASN Neuro 3(1):e00051
12. Park E, Liu E, Shek M, Park A, Baker AJ (2007) Heavy neurofilament accumulation and alpha-spectrin degradation accompany cerebellar white matter functional deficits following forebrain fluid percussion injury. Exp Neurol 204(1):49–57
13. Bennett V, Gilligan DM (1993) The spectrin-based membrane skeleton and micron-scale organization of the plasma membrane. Annu Rev Cell Biol 9:27–66
14. Huh GY, Glantz SB, Je S, Morrow JS, Kim JH (2001) Calpain proteolysis of alpha II-spectrin in the normal adult human brain. Neurosci Lett 316(1):41–44
15. De Matteis MA, Morrow JS (2000) Spectrin tethers and mesh in the biosynthetic pathway. J Cell Sci 113(Pt 13):2331–2343
16. Bennett V, Baines AJ (2001) Spectrin and ankyrin-based pathways: metazoan inventions for integrating cells into tissues. Physiol Rev 81(3):1353–1392
17. Backman L, Pekrun A, Gratzer WB (1991) Formation and properties of spectrin containing a truncated beta-chain, generated by an endogenous calcium-dependent protease. J Biol Chem 266(6):3835–3840
18. Viel A, Branton D (1996) Spectrin: on the path from structure to function. Curr Opin Cell Biol 8(1):49–55
19. Goodman SR, Weidner SA (1980) Binding of spectrin alpha 2-beta 2 tetramers to human erythrocyte membranes. J Biol Chem 255(17):8082–8086
20. Rolius R, Antoniou C, Nazarova LA, Kim SH, Cobb G, Gala P, Rajaram P, Li Q, Fung LW (2010) Inhibition of calpain but not caspase activity by spectrin fragments. Cell Mol Biol Lett 15(3):395–405
21. Hayes NV, Scott C, Heerkens E, Ohanian V, Maggs AM, Pinder JC, Kordeli E, Baines AJ (2000) Identification of a novel C-terminal variant of beta II spectrin: two isoforms of beta II spectrin have distinct intracellular locations and activities. J Cell Sci 113(Pt 11):2023–2034
22. Ursitti JA, Martin L, Resneck WG, Chaney T, Zielke C, Alger BE, Bloch RJ (2001) Spectrins in developing rat hippocampal cells. Brain Res Dev Brain Res 129(1):81–93
23. Musacchio A, Noble M, Pauptit R, Wierenga R, Saraste M (1992) Crystal structure of a Src-homology 3 (SH3) domain. Nat 359(6398):851–855
24. Musacchio A, Gibson T, Lehto VP, Saraste M (1992) SH3–an abundant protein domain in search of a function. FEBS Lett 307(1):55–61
25. Croall DE, Ersfeld K (2007) The calpains: modular designs and functional diversity. Genome Biol 8(6):218
26. Squier MK, Miller AC, Malkinson AM, Cohen JJ (1994) Calpain activation in apoptosis. J Cell Physiol 159(2):229–237
27. Wang KK (2000) Calpain and caspase: can you tell the difference? Trends Neurosci 23(1):20–26
28. Siman R, Noszek JC (1988) Excitatory amino acids activate calpain I and induce structural protein breakdown in vivo. Neuron 1(4):279–287
29. Azuma M, David LL, Shearer TR (1991) Cysteine protease inhibitor E64 reduces the rate of formation of selenite cataract in the whole animal. Curr Eye Res 10(7):657–666
30. Wang DS, Shaw R, Winkelmann JC, Shaw G (1994) Binding of PH domains of beta-adrenergic receptor kinase and beta-spectrin to WD40/beta-transducin repeat containing regions of the beta-subunit of trimeric G-proteins. Biochem Biophys Res Commun 203(1):29–35
31. Nath R, Raser KJ, Stafford D, Hajimohammadreza I, Posner A, Allen H, Talanian RV, Yuen P, Gilbertsen RB, Wang KK (1996) Non-erythroid alpha-spectrin breakdown by calpain and interleukin 1 beta-converting-enzyme-like protease (s) in apoptotic cells: contributory roles of both protease families in neuronal apoptosis. Biochem J 319(Pt 3):683–690
32. Morrow JS (1989) The spectrin membrane skeleton: emerging concepts. Curr Opin Cell Biol 1(1):23–29
33. Cryns VL, Bergeron L, Zhu H, Li H, Yuan J (1996) Specific cleavage of alpha-fodrin during Fas- and tumor necrosis factor-induced apoptosis is mediated by an interleukin-1beta-converting enzyme/Ced-3 protease distinct from the poly (ADP-ribose) polymerase protease. J Biol Chem 271(49):31277–31282
34. Vanags DM, Porn-Ares MI, Coppola S, Burgess DH, Orrenius S (1996) Protease involvement in fodrin cleavage and phosphatidylserine exposure in apoptosis. J Biol Chem 271(49):31075–31085
35. Moldoveanu T, Hosfield CM, Lim D, Elce JS, Jia Z, Davies PL (2002) A Ca (2+) switch aligns the active site of calpain. Cell 108(5):649–660
36. Benveniste H, Drejer J, Schousboe A, Diemer NH (1984) Elevation of the extracellular concentrations of glutamate and aspartate in rat hippocampus during transient cerebral ischemia monitored by intracerebral microdialysis. J Neurochem 43(5):1369–1374
37. Jourdi H, Yanagihara T, Martinez U, Bi X, Lynch G, Baudry M (2005) Effects of positive AMPA receptor modulators on calpain-mediated spectrin degradation in cultured hippocampal slices. Neurochem Int 46(1):31–40
38. Seubert P, Lee K, Lynch G (1989) Ischemia triggers NMDA receptor-linked cytoskeletal proteolysis in hippocampus. Brain Res 492(1–2):366–370
39. Seubert P, Nakagawa Y, Ivy G, Vanderklish P, Baudry M, Lynch G (1989) Intrahippocampal colchicine injection results in spectrin proteolysis. Neurosci 31(1):195–202
40. Roberts-Lewis JM, Savage MJ, Marcy VR, Pinsker LR, Siman R (1994) Immunolocalization of calpain I-mediated spectrin degradation to vulnerable neurons in the ischemic gerbil brain. J Neurosci 14(6):3934–3944
41. Nath R, Raser KJ, McGinnis K, Nadimpalli R, Stafford D, Wang KK (1996) Effects of ICE-like protease and calpain inhibitors on neuronal apoptosis. Neuroreport 8(1):249–255
42. Pike BR, Flint J, Dutta S, Johnson E, Wang KK, Hayes RL (2001) Accumulation of non-erythroid alpha II-spectrin and calpain-cleaved alpha II-spectrin breakdown products in cerebrospinal fluid after traumatic brain injury in rats. J Neurochem 78(6):1297–1306
43. Pike BR, Flint J, Dave JR, Lu XC, Wang KK, Tortella FC, Hayes RL (2004) Accumulation of calpain and caspase-3 proteolytic fragments of brain-derived alphaII-spectrin in cerebral spinal fluid after middle cerebral artery occlusion in rats. J Cereb Blood Flow Metab 24(1):98–106
44. Pike BR, Zhao X, Newcomb JK, Posmantur RM, Wang KK, Hayes RL (1998) Regional calpain and caspase-3 proteolysis of alpha-spectrin after traumatic brain injury. Neuroreport 9(11):2437–2442
45. Wang KK, Posmantur R, Nath R, McGinnis K, Whitton M, Talanian RV, Glantz SB, Morrow JS (1998) Simultaneous degradation of alphaII- and betaII-spectrin by caspase 3 (CPP32) in apoptotic cells. J Biol Chem 273(35):22490–22497
46. Lofvenberg L, Backman L (1999) Calpain-induced proteolysis of beta-spectrins. FEBS Lett 443(2):89–92
47. Roberts-Lewis JM, Siman R (1993) Spectrin proteolysis in the hippocampus: a biochemical marker for neuronal injury and neuroprotection. Ann N Y Acad Sci 679:78–86
48. Siman R, Toraskar N, Dang A, McNeil E, McGarvey M, Plaum J, Maloney E, Grady MS (2009) A panel of neuron-enriched proteins as markers for traumatic brain injury in humans. J Neurotrauma 26(11):1867–1877
49. Glantz SB, Cianci CD, Iyer R, Pradhan D, Wang KK, Morrow JS (2007) Sequential degradation of alphaII and betaII spectrin by calpain in glutamate or maitotoxin-stimulated cells. Biochem 46(2):502–513
50. Nath R, Scott M, Nadimpalli R, Gupta R, Wang KK (2000) Activation of apoptosis-linked caspase(s) in NMDA-injured brains in neonatal rats. Neurochem Int 36(2):119–126
51. Zhang Z, Larner SF, Liu MC, Zheng W, Hayes RL, Wang KK (2009) Multiple alphaII-spectrin breakdown products distinguish calpain and caspase dominated necrotic and apoptotic cell death pathways. Apoptosis 14(11):1289–1298
52. Waterhouse N, Kumar S, Song Q, Strike P, Sparrow L, Dreyfuss G, Alnemri ES, Litwack G, Lavin M, Watters D (1996) Heteronuclear ribonucleoproteins C1 and C2, components of the spliceosome, are specific targets of interleukin 1beta-converting enzyme-like proteases in apoptosis. J Biol Chem 271(46):29335–29341
53. Chiesa R, Angeretti N, Del Bo R, Lucca E, Munna E, Forloni G (1998) Extracellular calcium deprivation in astrocytes: regulation of mRNA expression and apoptosis. J Neurochem 70(4):1474–1483
54. Koumura A, Nonaka Y, Hyakkoku K, Oka T, Shimazawa M, Hozumi I, Inuzuka T, Hara H (2008) A novel calpain inhibitor, ((1S)-1((((1S)-1-benzyl-3-cyclopropylamino-2,3-di-oxopropyl)amino)carbonyl)-3-methylbutyl) carbamic acid 5-methoxy-3-oxapentyl ester, protects neuronal cells from cerebral ischemia-induced damage in mice. Neurosci 157(2):309–318
55. Shirasaki Y, Miyashita H, Yamaguchi M, Inoue J, Nakamura M (2005) Exploration of orally available calpain inhibitors: peptidyl alpha-ketoamides containing an amphiphile at P3 site. Bioorg Med Chem 13(14):4473–4484
56. Pockros PJ, Schiff ER, Shiffman ML, McHutchison JG, Gish RG, Afdhal NH, Makhviladze M, Huyghe M, Hecht D, Oltersdorf T, Shapiro DA (2007) Oral IDN-6556, an antiapoptotic caspase inhibitor, may lower aminotransferase activity in patients with chronic hepatitis C. Hepatol 46(2):324–329
57. Hoglen NC, Anselmo DM, Katori M, Kaldas M, Shen XD, Valentino KL, Lassman C, Busuttil RW, Kupiec-Weglinski JW, Farmer DG (2007) A caspase inhibitor, IDN-6556, ameliorates early hepatic injury in an ex vivo rat model of warm and cold ischemia. Liver Transpl 13(3):361–366
58. Baskin-Bey ES, Washburn K, Feng S, Oltersdorf T, Shapiro D, Huyghe M, Burgart L, Garrity-Park M, van Vilsteren FG, Oliver LK, Rosen CB, Gores GJ (2007) Clinical trial of the pan-caspase inhibitor, IDN-6556, in human liver preservation injury. Am J Transplant 7(1):218–225
59. Poordad FF (2004) IDN-6556 idun pharmaceuticals Inc. Curr Opin Investig Drugs 5(11):1198–1204
60. Liu MC, Akle V, Zheng W, Kitlen J, O’Steen B, Larner SF, Dave JR, Tortella FC, Hayes RL, Wang KK (2006) Extensive degradation of myelin basic protein isoforms by calpain following traumatic brain injury. J Neurochem 98(3):700–712
61. Beneke R, Bihn D, Hutler M, Leithauser RM (2005) Haemolysis caused by alterations of alpha- and beta-spectrin after 10 to 35 min of severe exercise. Eur J Appl Physiol 95(4):307–312
62. Chen Z, Kontonotas D, Friedmann D, Pitts-Kiefer A, Frederick JR, Siman R, Neumar RW (2005) Developmental status of neurons selectively vulnerable to rapidly triggered post-ischemic caspase activation. Neurosci Lett 376(3):166–170
63. Neumar RW, Meng FH, Mills AM, Xu YA, Zhang C, Welsh FA, Siman R (2001) Calpain activity in the rat brain after transient forebrain ischemia. Exp Neurol 170(1):27–35
64. Brophy GM, Pineda JA, Papa L, Lewis SB, Valadka AB, Hannay HJ, Heaton SC, Demery JA, Liu MC, Tepas JJ 3rd, Gabrielli A, Robicsek S, Wang KK, Robertson CS, Hayes RL (2009) alphaII-Spectrin breakdown product cerebrospinal fluid exposure metrics suggest differences in cellular injury mechanisms after severe traumatic brain injury. J Neurotrauma 26(4):471–479
65. Kobeissy FH, Ottens AK, Zhang Z, Liu MC, Denslow ND, Dave JR, Tortella FC, Hayes RL, Wang KK (2006) Novel differential neuroproteomics analysis of traumatic brain injury in rats. Mol Cell Proteomics 5(10):1887–1898
66. Gavett BE, Stern RA, Cantu RC, Nowinski CJ, McKee AC (2010) Mild traumatic brain injury: a risk factor for neurodegeneration. Alzheimers Res Ther 2(3):18
67. Ivy G, Seubert P, Lynch G, Baudry M (1988) Lesions of entorhinal cortex produce a calpain-mediated degradation of brain spectrin in dentate gyrus. II. Anatomical studies. Brain Res 459(2):233–240
68. del Cerro S, Arai A, Kessler M, Bahr BA, Vanderklish P, Rivera S, Lynch G (1994) Stimulation of NMDA receptors activates calpain in cultured hippocampal slices. Neurosci Lett 167(1–2):149–152
69. Ringger NC, O’Steen BE, Brabham JG, Silver X, Pineda J, Wang KK, Hayes RL, Papa L (2004) A novel marker for traumatic brain injury: CSF alphaII-spectrin breakdown product levels. J Neurotrauma 21(10):1443–1456
70. Mondello S, Robicsek SA, Gabrielli A, Brophy GM, Papa L, Tepas J, Robertson C, Buki A, Scharf D, Jixiang M, Akinyi L, Muller U, Wang KK, Hayes RL (2010) alphaII-spectrin breakdown products (SBDPs): diagnosis and outcome in severe traumatic brain injury patients. J Neurotrauma 27(7):1203–1213
71. Tang Y, Katuri V, Dillner A, Mishra B, Deng CX, Mishra L (2003) Disruption of transforming growth factor-beta signaling in ELF beta-spectrin-deficient mice. Sci 299(5606):574–577
72. Stankewich MC, Cianci CD, Stabach PR, Ji L, Nath A, Morrow JS (2011) Cell organization, growth, and neural and cardiac development require alphaII-spectrin. J Cell Sci 124(Pt 23):3956–3966
73. Zhang C, Susuki K, Zollinger DR, Dupree JL, Rasband MN (2013) Membrane domain organization of myelinated axons requires betaII spectrin. J Cell Biol 203(3):437–443
74. Harris AS, Morrow JS (1990) Calmodulin and calcium-dependent protease I coordinately regulate the interaction of fodrin with actin. Proc Natl Acad Sci U S A 87(8):3009–3013
75. Povlishock JT (1992) Traumatically induced axonal injury: pathogenesis and pathobiological implications. Brain Pathol 2(1):1–12
76. Di Stasi AM, Gallo V, Ceccarini M, Petrucci TC (1991) Neuronal fodrin proteolysis occurs independently of excitatory amino acid-induced neurotoxicity. Neuron 6(3):445–454
77. Hu RJ, Bennett V (1991) In vitro proteolysis of brain spectrin by calpain I inhibits association of spectrin with ankyrin-independent membrane binding site(s). J Biol Chem 266(27):18200–18205
78. Czogalla A, Jaszewski AR, Diakowski W, Bok E, Jezierski A, Sikorski AF (2007) Structural insight into an ankyrin-sensitive lipid-binding site of erythroid beta-spectrin. Mol Membr Biol 24(3):215–224
79. Davis LH, Bennett V (1994) Identification of two regions of beta G spectrin that bind to distinct sites in brain membranes. J Biol Chem 269(6):4409–4416
80. Garbe DS, Das A, Dubreuil RR, Bashaw GJ (2007) beta-Spectrin functions independently of Ankyrin to regulate the establishment and maintenance of axon connections in the Drosophila embryonic CNS. Dev 134(2):273–284
81. Kizhatil K, Sandhu NK, Peachey NS, Bennett V (2009) Ankyrin-B is required for coordinated expression of beta-2-spectrin, the Na/K-ATPase and the Na/Ca exchanger in the inner segment of rod photoreceptors. Exp Eye Res 88(1):57–64
82. Berger RP, Hayes RL, Richichi R, Beers SR, Wang KK (2012) Serum concentrations of ubiquitin C-terminal hydrolase-L1 and alphaII-spectrin breakdown product 145 kDa correlate with outcome after pediatric TBI. J Neurotrauma 29(1):162–167
83. Siman R, Giovannone N, Hanten G, Wilde EA, McCauley SR, Hunter JV, Li X, Levin HS, Smith DH (2013) Evidence that the blood biomarker SNTF predicts brain imaging changes and persistent cognitive dysfunction in mild TBI patients. Front Neurol 4:190
84. Raghupathi R, Graham DI, McIntosh TK (2000) Apoptosis after traumatic brain injury. J Neurotrauma 17(10):927–938
85. Raghupathi R (2004) Cell death mechanisms following traumatic brain injury. Brain Pathol 14(2):215–222
86. Liu MC, Akle V, Zheng W, Dave JR, Tortella FC, Hayes RL, Wang KK (2006) Comparing calpain- and caspase-3-mediated degradation patterns in traumatic brain injury by differential proteome analysis. Biochem J 394(Pt 3):715–725