PKC activator therapeutic for mild traumatic brain injury in mice

Neurobiology of Disease

Volumn 41, Issue 2, 2011, Pages 329-337

  Zohar, Ofer ^a   Lavy, Rotem ^a   Zi, Xiaomei ^a   Nelson, Thomas J ^a   Hongpaisan, Jarin ^a   Pick, Chaim G ^b   Alkon, D L ^a  

^a WEST VIRGINIA UNIVERSITY   (United States)

^b TEL AVIV UNIVERSITY   (Israel)

Author keywords

ADAM10; BACE1; Cognitive deficits; Dose dependent; Mild traumatic brain injury; Synaptic structures; Therapeutic; Time frame

Indexed keywords

ADAM10 ENDOPEPTIDASE; ALPHA SECRETASE; AMYLOID PRECURSOR PROTEIN; BETA SECRETASE; BRYOSTATIN 1; PROTEIN KINASE C ACTIVATOR;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DENDRITIC SPINE; DRUG ACTIVITY; DRUG EFFICACY; DRUG POTENCY; ENZYME ACTIVITY; ENZYME SYNTHESIS; IMMUNOHISTOCHEMISTRY; MALE; MAZE TEST; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN CLEAVAGE; PROTEIN FUNCTION; PROTEIN PROCESSING; SYNAPSE; SYNAPSE VESICLE; TRAUMATIC BRAIN INJURY;

ANIMALS; ANTINEOPLASTIC AGENTS; BRAIN INJURIES; BRYOSTATINS; DISEASE MODELS, ANIMAL; ENZYME ACTIVATION; MALE; MICE; MICE, INBRED C57BL; NEUROPROTECTIVE AGENTS; PROTEIN KINASE C;

EID: 78650619283     PISSN: 09699961     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.nbd.2010.10.001     Document Type: Article

References (78)

1. Albensi B.C. Models of brain injury and alterations in synaptic plasticity. J. Neurosci. Res. 2001, 65:279-283.
2. Alkon D.L., Rasmussen H. A spatial-temporal model of cell activation. Science 1988, 239:998-1005.
3. Alkon D.L., Epstein H., Kuzirian A., Bennett M.C., Nelson T.J. Protein synthesis required for long-term memory is induced by PKC activation on days before associative learning. Proc. Natl. Acad. Sci. U. S. A. 2005, 102:16432-16437.
4. Amador M.L., Jimeno J., Paz-Ares L., Cortes-Funes H., Hidalgo M. Progress in the development and acquisition of anticancer agents from marine sources. Ann. Oncol. 2003, 14:1607-1615.
5. Asai M., Hattori C., Szabo B., Sasagawa N., Maruyama K., Tanuma S., Ishiura S. Putative function of ADAM9, ADAM10, and ADAM17 as APP alpha-secretase. Biochem. Biophys. Res. Commun. 2003, 301:231-235.
6. Assaf Y., Holokovsky A., Berman E., Shapira Y., Shohami E., Cohen Y. Diffusion and perfusion magnetic resonance imaging following closed head injury in rats. J. Neurotrauma 1999, 16:1165-1176.
7. Bank B., DeWeer A., Kuzirian A.M., Rasmussen H., Alkon D.L. Classical conditioning induces long-term translocation of protein kinase C in rabbit hippocampal CA1 cells. Proc. Natl. Acad. Sci. U. S. A. 1988, 85:1988-1992.
8. Basu A. The potential of protein kinase C as a target for anticancer treatment. Pharmacol. Ther. 1993, 59:257-280.
9. Berger E., Leven F., Pirente N., Bouillon B., Neugebauer E. Quality of Life after traumatic brain injury: a systematic review of the literature. Restor. Neurol. Neurosci. 1999, 14:93-102.
10. Bird C.M., Burgess N. The hippocampus and memory: insights from spatial processing. Nat. Rev. Neurosci. 2008, 9:182-194.
11. Blobe G.C., Obeid L.M., Hannun Y.A. Regulation of protein kinase C and role in cancer biology. Cancer Metastasis Rev. 1994, 13:411-431.
12. Bonini J.S., Da Silva W.C., Bevilaqua L.R., Medina J.H., Izquierdo I., Cammarota M. On the participation of hippocampal PKC in acquisition, consolidation and reconsolidation of spatial memory. Neuroscience 2007, 147:37-45.
13. Bruns J., Hauser W.A. The epidemiology of traumatic brain injury: a review. Epilepsia 2003, 44(Suppl 10):2-10.
14. Ciallella J.R., Ikonomovic M.D., Paljug W.R., Wilbur Y.I., Dixon C.E., Kochanek P.M., Marion D.W., DeKosky S.T. Changes in expression of amyloid precursor protein and interleukin-1beta after experimental traumatic brain injury in rats. J. Neurotrauma 2002, 19:1555-1567.
15. Craske M.L., Fivaz M., Batada N.N., Meyer T. Spines and neurite branches function as geometric attractors that enhance protein kinase C action. J. Cell Biol. 2005, 170:1147-1158.
16. Deuss M., Reiss K., Hartmann D. Part-time alpha-secretases: the functional biology of ADAM 9, 10 and 17. Curr. Alzheimer Res. 2008, 5:187-201.
17. Esler W.P., Wolfe M.S. A portrait of Alzheimer secretases - new features and familiar faces. Science 2001, 293:1449-1454.
18. Etcheberrigaray R., Tan M., Dewachter I., Kuiperi C., Van dA I., Wera S., Qiao L., Bank B., Nelson T.J., Kozikowski A.P., Van Leuven F., Alkon D.L. Therapeutic effects of PKC activators in Alzheimer's disease transgenic mice. Proc. Natl. Acad. Sci. U. S. A. 2004, 101:11141-11146.
19. Farrow B., Thomas R.P., Wanq X.F., Evers B.M. Activation of conventional PKC isoforms increases expression of the pro-apoptotic protein Bad and TRAIL receptors. Int. J. Gastrointest. Cancer 2002, 32:63-72.
20. Gentleman S.M., Greenberg B.D., Savage M.J., Noori M., Newman S.J., Roberts G.W., Griffin W.S., Graham D.I. A beta 42 is the predominant form of amyloid beta-protein in the brains of short-term survivors of head injury. NeuroReport 1997, 8:1519-1522.
21. Gescher A. Analogs of staurosporine: potential anticancer drugs?. Gen. Pharmacol. 1998, 31:721-728.
22. Goekjian P.G., Jirousek M.R. Protein kinase C inhibitors as novel anticancer drugs. Expert. Opin. Investig. Drugs 2001, 10:2117-2140.
23. Gorrie C., Oakes S., Duflou J., Blumbergs P., Waite P.M. Axonal injury in children after motor vehicle crashes: extent, distribution, and size of axonal swellings using beta-APP immunohistochemistry. J. Neurotrauma 2002, 19:1171-1182.
24. Graham D.I., McIntosh T.K., Maxwell W.L., Nicoll J.A. Recent advances in neurotrauma. J. Neuropathol. Exp. Neurol. 2000, 59:641-651.
25. Hoge C.W., McGurk D., Thomas J.L., Cox A.L., Engel C.C., Castro C.A. Mild traumatic brain injury in U.S. soldiers returning from Iraq. N. Engl. J. Med. 2008, 358:453-463.
26. Hongpaisan J., Alkon D.L. A structural basis for enhancement of long-term associative memory in single dendritic spines regulated by PKC. Proc. Natl. Acad. Sci. U. S. A. 2007, 104:19571-19576.
27. Iwata A., Chen X.H., McIntosh T.K., Browne K.D., Smith D. Long-term accumulation of amyloid-beta in axons following brain trauma without persistent upregulation of amyloid precursor protein genes. J. Neuropathol. Exp. Neurol. 2002, 61:1056-1068.
28. Jin G., Huang X., Black R., Wolfson M., Rauch C., McGregor H., Ellestad G., Cowling R. A continuous fluorimetric assay for tumor necrosis factor-alpha converting enzyme. Anal. Biochem. 2002, 302:269-275.
29. Johnston A.J., Gupta A.K. Advanced monitoring in the neurology intensive care unit: microdialysis. Curr. Opin. Crit. Care 2002, 8:121-127.
30. Jones P.A., Andrews P.J., Midgley S., Anderson S.I., Piper I.R., Tocher J.L., Housley A.M., Corrie J.A., Slattery J., Dearden N.M. Measuring the burden of secondary insults in head-injured patients during intensive care. J. Neurosurg. Anesthesiol. 1994, 6:4-14.
31. Karkkainen I., Rybnikova E., Pelto-Huikko M., Huovila A.P. Metalloprotease-disintegrin (ADAM) genes are widely and differentially expressed in the adult CNS. Mol. Cell. Neurosci. 2000, 15:547-560.
32. Kibby M.Y., Long C.J. Minor head injury: attempts at clarifying the confusion. Brain Inj. 1996, 10:159-186.
33. Kojro E., Fahrenholz F. The non-amyloidogenic pathway: structure and function of alpha-secretases. Subcell. Biochem. 2005, 38:105-127.
34. Kortmansky J., Schwartz G.K. Bryostatin-1: a novel PKC inhibitor in clinical development. Cancer Investig. 2003, 21:924-936.
35. Kuzirian A.M., Epstein H.T., Gagliardi C.J., Nelson T.J., Sakakibara M., Taylor C., Scioletti A.B., Alkon D.L. Bryostatin enhancement of memory in Hermissenda. Biol. Bull. 2006, 210:201-214.
36. Lan J.Y., Skeberdis V.A., Jover T., Grooms S.Y., Lin Y., Araneda R.C., Zheng X., Bennett M.V., Zukin R.S. Protein kinase C modulates NMDA receptor trafficking and gating. Nat. Neurosci. 2001, 4:382-390.
37. Lewen A., Li G.L., Nilsson P., Olsson Y., Hillered L. Traumatic brain injury in rat produces changes of beta-amyloid precursor protein immunoreactivity. NeuroReport 1995, 6:357-360.
38. Lewin N.E., Pettit G.R., Kamano Y., Blumberg P.M. Binding of [26-3H]-epi-bryostatin 4 to protein kinase C. Cancer Commun. 1991, 3:67-70.
39. Lorenzo P.S., Bogi K., Acs P., Pettit G.R., Blumberg P.M. The catalytic domain of protein kinase Cdelta confers protection from down-regulation induced by bryostatin 1. J. Biol. Chem. 1997, 272:33338-33343.
40. Lorenzo P.S., Bogi K., Hughes K.M., Beheshti M., Bhattacharyya D., Garfield S.H., Pettit G.R., Blumberg P.M. Differential roles of the tandem C1 domains of protein kinase C delta in the biphasic down-regulation induced by bryostatin 1. Cancer Res. 1999, 59:6137-6144.
41. Majewski H., Kotsonis P., Iannazzo L., Murphy T.V., Musgrave I.F. Protein kinase C and transmitter release. Clin. Exp. Pharm. Physiol. 1997, 24:619-623.
42. Margulies S. The postconcussion syndrome after mild head trauma: is brain damage over diagnosed? Part 1. J. Clin. Neurosci. 2002, 7:400-408.
43. Mellor H., Parker P.J. The extended protein kinase C superfamily. Biochem. J. 1998, 332(Pt 2):281-292.
44. Milman A., Rosenberg A., Weizman R., Pick C.G. Mild traumatic brain injury induces persistent cognitive deficits and behavioral disturbances in mice. J. Neurotrauma 2005, 22:1003-1010.
45. Moppett I.K. Traumatic brain injury: assessment, resuscitation and early management. Br. J. Anaesth. 2007, 99:18-31.
46. Murai H., Pierce J.E., Raghupathi R., Smith D.H., Saatman K.E., Trojanowski J.Q., Lee V.M., Loring J.F., Eckman C., Younkin S., McIntosh T.K. Twofold overexpression of human beta-amyloid precursor proteins in transgenic mice does not affect the neuromotor, cognitive, or neurodegenerative sequelae following experimental brain injury. J. Comp. Neurol. 1998, 392:428-438.
47. Mutter R., Wills M. Chemistry and clinical biology of the bryostatins. Bioorg. Med. Chem. 2000, 8:1841-1860.
48. Nagano O., Murakami D., Hartmann D., De S.B., Saftig P., Iwatsubo T., Nakajima M., Shinohara M., Saya H. Cell-matrix interaction via CD44 is independently regulated by different metalloproteinases activated in response to extracellular Ca(2+) influx and PKC activation. J. Cell Biol. 2004, 165:893-902.
49. Narayan R.K., Michel M.E., Ansell B., Baethmann A., Biegon A., Bracken M.B., Bullock M.R., Choi S.C., Clifton G.L., Contant C.F., Coplin W.M., Dietrich W.D., Ghajar J., Grady S.M., Grossman R.G., Hall E.D., Heetderks W., Hovda D.A., Jallo J., Katz R.L., Knoller N., Kochanek P.M., Maas A.I., Majde J., Marion D.W., Marmarou A., Marshall L.F., McIntosh T.K., Miller E., Mohberg N., Muizelaar J.P., Pitts L.H., Quinn P., Riesenfeld G., Robertson C.S., Strauss K.I., Teasdale G., Temkin N., Tuma R., Wade C., Walker M.D., Weinrich M., Whyte J., Wilberger J., Young A.B., Yurkewicz L. Clinical trials in head injury. J. Neurotrauma 2002, 19:503-557.
50. Newton A.C. Regulation of protein kinase C. Curr. Opin. cell Biol. 1997, 9:161-167.
51. Nogues X. Protein kinase C, learning and memory: a circular determinism between physiology and behaviour. Prog. Neuropsychopharmacol. Biol. Psychiatry 1997, 21:507-529.
52. Nunan J., Small D.H. Regulation of APP cleavage by alpha-, beta- and gamma-secretases. FEBS Lett. 2000, 483:6-10.
53. Olds J.L., Anderson M.L., McPhie D.L., Staten L.D., Alkon D.L. Imaging of memory specific changes in the distribution of protein kinase C in the hippocampus. Science 1989, 245:866-869. (Ref Type: Journal (Full)).
54. Pan W., Kastin A.J., Rigai T., McLay R., Pick C.G. Increased hippocampal uptake of tumor necrosis factor alpha and behavioral changes in mice. Exp. Brain Res. 2003, 149:195-199.
55. Paterson I., Anderson E.A. Chemistry. The renaissance of natural products as drug candidates. Science 2005, 310:451-453.
56. Pierce J.E., Trojanowski J.Q., Graham D.I., Smith D.H., McIntosh T.K. Immunohistochemical characterization of alterations in the distribution of amyloid precursor proteins and beta-amyloid peptide after experimental brain injury in the rat. J. Neurosci. 1996, 16:1083-1090.
57. Pierce J.E., Smith D.H., Trojanowski J.Q., McIntosh T.K. Enduring cognitive, neurobehavioral and histopathological changes persist for up to one year following severe experimental brain injury in rats. Neuroscience 1998, 87:359-369.
58. Postina R. A closer look at alpha-secretase. Curr. Alzheimer Res. 2008, 5:179-186.
59. Reilly P.L. Brain injury: the pathophysiology of the first hours. 'Talk and die revisited'. J. Clin. Neurosci. 2001, 8:398-403.
60. Roberts G.W., Gentleman S.M., Lynch A., Graham D.I. beta A4 amyloid protein deposition in brain after head trauma. Lancet 1991, 338:1422-1423.
61. Shapira Y., Setton D., Artru A.A., Shohami E. Blood-brain barrier permeability, cerebral edema, and neurologic function after closed head injury in rats. Anesth. Analg. 1993, 77:141-148.
62. Smith D.H., Nakamura M., McIntosh T.K., Wang J., Rodriguez A., Chen X.H., Raghupathi R., Saatman K.E., Clemens J., Schmidt M.L., Lee V.M., Trojanowski J.Q. Brain trauma induces massive hippocampal neuron death linked to a surge in beta-amyloid levels in mice overexpressing mutant amyloid precursor protein. Am. J. Pathol. 1998, 153:1005-1010.
63. Smith D.H., Chen X.H., Iwata A., Graham D.I. Amyloid beta accumulation in axons after traumatic brain injury in humans. J. Neurosurg. 2003, 98:1072-1077.
64. Sun M.K., Alkon D.L. Dual effects of bryostatin-1 on spatial memory and depression. Eur. J. Pharmacol. 2005, 512:43-51.
65. Sun M.K., Alkon D.L. Bryostatin-1: pharmacology and therapeutic potential as a CNS drug. CNS Drug Rev. 2006, 12:1-8.
66. Sun M.K., Hongpaisan J., Alkon D.L. Postischemic PKC activation rescues retrograde and anterograde long-term memory. Proc. Natl. Acad. Sci. U. S. A. 2009, 106:14676-14680.
67. Tashlykov V., Katz Y., Gazit V., Zohar O., Schreiber S., Pick C.G. Apoptotic changes in the cortex and hippocampus following minimal brain trauma in mice. Brain Res. 2007, 1130:197-205.
68. Tashlykov V., Katz Y., Volkov A., Gazit V., Schreiber S., Zohar O., Pick C.G. Minimal traumatic brain injury induce apoptotic cell death in mice. J. Mol. Neurosci. 2009, 37:16-24.
69. Thornhill S., Teasdale G.M., Murray G.D., McEwen J., Roy C.W., Penny K.I. Disability in young people and adults one year after head injury: prospective cohort study. BMJ 2000, 320:1631-1635.
70. Tweedie D., Milman A., Holloway H.W., Li Y., Harvey B.K., Shen H., Pistell P.J., Lahiri D.K., Hoffer B.J., Wang Y., Pick C.G., Greig N.H. Apoptotic and behavioral sequelae of mild brain trauma in mice. J. Neurosci. Res. 2007, 85:805-815.
71. Uryu K., Laurer H., McIntosh T., Pratico D., Martinez D., Leight S., Lee V.M., Trojanowski J.Q. Repetitive mild brain trauma accelerates Abeta deposition, lipid peroxidation, and cognitive impairment in a transgenic mouse model of Alzheimer amyloidosis. J. Neurosci. 2002, 22:446-454.
72. Van der Zee E.A., Luiten P.G., Disterhoft J.F. Learning-induced alterations in hippocampal PKC-immunoreactivity: a review and hypothesis of its functional significance. Prog. Neuropsychopharmacol. Biol. Psychiatry 1997, 21:531-572.
73. van der N.J., van Zomeren A.H., Sluiter W.J., Minderhoud J.M. One year outcome in mild to moderate head injury: the predictive value of acute injury characteristics related to complaints and return to work. J. Neurol. Neurosurg. Psychiatry 1999, 66:207-213.
74. Wang D., Darwish D.S., Schreurs B.G., Alkon D.L. Analysis of long-term cognitive-enhancing effects of bryostatin-1 on the rabbit (Oryctolagus cuniculus) nictitating membrane response. Behav. Pharmacol. 2008, 19:245-256.
75. Waxweiler R.J., Thurman D., Sniezek J., Sosin D., O'Neil J. Monitoring the impact of traumatic brain injury: a review and update. J. Neurotrauma 1995, 12:509-516.
76. Zhang X., Zhang R., Zhao H., Cai H., Gush K.A., Kerr R.G., Pettit G.R., Kraft A.S. Preclinical pharmacology of the natural product anticancer agent bryostatin 1, an activator of protein kinase C. Cancer Res. 1996, 56:802-808.
77. Zohar O., Schreiber S., Getslev V., Schwartz J.P., Mullins P.G., Pick C.G. Closed-head minimal traumatic brain injury produces long-term cognitive deficits in mice. Neuroscience 2003, 118:949-955.
78. Zohar O., Getslev V., Miller A.L., Schreiber S., Pick C.G. Morphine protects for head trauma induced cognitive deficits in mice. Neurosci. lett. 2006, 394:239-242.