Knockout of plasminogen activator inhibitor 1 gene reduces amyloid beta peptide burden in a mouse model of Alzheimer's disease

Neurobiology of Aging

Volumn 32, Issue 6, 2011, Pages 1079-1089

  Liu, R M ^a   van Groen, T ^b   Katre, A ^a   Cao, D ^c   Kadisha, I ^b   Ballinger, C ^a   Wang, L ^a   Carroll, S L ^d   Li, L ^c  

^a UNIVERSITY OF ALABAMA AT BIRMINGHAM   (United States)

^b UNIVERSITY OF ALABAMA AT BIRMINGHAM   (United States)

^c UNIVERSITY OF ALABAMA SCHOOL OF MEDICINE   (United States)

^d University of Alabama at Birmingham   (United States)

Author keywords

Aging; Alzheimer's disease; Amyloid beta peptide; Knockout; PAI 1; Plasmin

Indexed keywords

AMYLOID BETA PROTEIN[1-40]; AMYLOID BETA PROTEIN[1-42]; AMYLOID PRECURSOR PROTEIN; PLASMIN; PRESENILIN 1; TISSUE PLASMINOGEN ACTIVATOR; UROKINASE;

AGING; ALZHEIMER DISEASE; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BIOACCUMULATION; CARBOXY TERMINAL SEQUENCE; CONTROLLED STUDY; ENZYME ACTIVITY; FEMALE; GENE; GENE EXPRESSION; GENE SILENCING; MOUSE; NONHUMAN; PLASMINOGEN ACTIVATOR INHIBITOR 1 GENE; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN FUNCTION; SENILE PLAQUE; TRANSGENIC MOUSE; WILD TYPE;

AGED; AGED, 80 AND OVER; ALZHEIMER DISEASE; AMYLOID BETA-PEPTIDES; AMYLOID BETA-PROTEIN PRECURSOR; ANIMALS; BRAIN; DISEASE MODELS, ANIMAL; ENZYME-LINKED IMMUNOSORBENT ASSAY; FEMALE; FIBRINOLYSIN; HUMANS; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MICE, TRANSGENIC; PEPTIDE FRAGMENTS; PLASMINOGEN ACTIVATOR INHIBITOR 1; PRESENILIN-1; RNA, MESSENGER; STATISTICS AS TOPIC; UROKINASE-TYPE PLASMINOGEN ACTIVATOR;

EID: 79955954909     PISSN: 01974580     EISSN: 15581497     Source Type: Journal    
DOI: 10.1016/j.neurobiolaging.2009.06.003     Document Type: Article

References (63)

1. Aillaud M.F., Pignol F., Alessi M.C., Harle J.R., Escande M., Mongin M., Juhan-Vague I. Increase in plasma concentration of plasminogen activator inhibitor, fibrinogen, von Willebrand factor, factor VIII:C and in erythrocyte sedimentation rate with age. Thromb. Haemost. 1986, 55:330-332.
2. Aoyagi T., Wada T., Kojima F., Nagai M., Harada S., Takeuchi T. Age-dependent decreases in fibrinolytic enzyme activities in serum of healthy subjects. Biol. Pharm. Bull. 1994, 17:348-351.
3. Arendash G.W., Schleif W., Rezai-Zadeh K., Jackson E.K., Zacharia L.C., Cracchiolo J.R., Shippy D., Tan J. Caffeine protects Alzheimer's mice against cognitive impairment and reduces brain [beta]-amyloid production. Neuroscience 2006, 142:941-952.
4. Bramblett G.T., Goedert M., Jakes R., Merrick S.E., Trojanowski J.Q., Lee V.M. Abnormal tau phosphorylation at Ser396 in Alzheimer's disease recapitulates development and contributes to reduced microtubule binding. Neuron 1993, 10:1089-1099.
5. Cacquevel M., Launay S., Castel H., Benchenane K., Cheenne S., Buee L., Moons L., Delacourte A., Carmeliet P., Vivien D. Ageing and amyloid-beta peptide deposition contribute to an impaired brain tissue plasminogen activator activity by different mechanisms. Neurobiol. Dis. 2007, 27:164-173.
6. Carmeliet P., Kieckens L., Schoonjans L., Ream B., van Nuffelen A., Prendergast G., Cole M., Bronson R., Collen D., Mulligan R.C. Plasminogen activator inhibitor-1 gene-deficient mice. I. Generation by homologous recombination and characterization. J. Clin. Invest. 1993, 92:2746-2755.
7. Chapman P.F., White G.L., Jones M.W., Cooper-Blacketer D., Marshall V.J., Irizarry M., Younkin L., Good M.A., Bliss T.V., Hyman B.T., Younkin S.G., Hsiao K.K. Impaired synaptic plasticity and learning in aged amyloid precursor protein transgenic mice. Nat. Neurosci. 1999, 2:271-276.
8. Comi P., Chiaramonte R., Maier J.A. Senescence-dependent regulation of type 1 plasminogen activator inhibitor in human vascular endothelial cells. Exp. Cell Res. 1995, 219:304-308.
9. Costantini C., Weindruch R., Della Valle G., Puglielli L. A TrkA-to-p75NTR molecular switch activates amyloid beta-peptide generation during aging. Biochem. J. 2005, 391:59-67.
10. Dellas C., Loskutoff D.J. Historical analysis of PAI-1 from its discovery to its potential role in cell motility and disease. Thromb. Haemost. 2005, 93:631-640.
11. Dimova E.Y., Moller U., Herzig S., Fink T., Zachar V., Ebbesen P., Kietzmann T. Transcriptional regulation of plasminogen activator inhibitor-1 expression by insulin-like growth factor-1 via MAP kinases and hypoxia-inducible factor-1 in HepG2 cells. Thromb. Haemost. 2005, 93:1176-1184.
12. Dong J., Fujii S., Imagawa S., Matsumoto S., Matsushita M., Todo S., Tsutsui H., Sobel B.E. IL-1 and IL-6 induce hepatocyte plasminogen activator inhibitor-1 expression through independent signaling pathways converging on C/EBP. Am. J. Physiol. Cell Physiol. 2007, 292:C209-C215.
13. Eckman E.A., Reed D.K., Eckman C.B. Degradation of the Alzheimer's amyloid beta peptide by endothelin-converting enzyme. J. Biol. Chem. 2001, 276:24540-24548.
14. Exley C., Korchazhkina O.V. Plasmin cleaves Abeta42 in vitro and prevents its aggregation into beta-pleated sheet structures. Neuroreport 2001, 12:2967-2970.
15. Farris W., Mansourian S., Chang Y., Lindsley L., Eckman E.A., Frosch M.P., Eckman C.B., Tanzi R.E., Selkoe D.J., Guenette S. Insulin-degrading enzyme regulates the levels of insulin, amyloid beta-protein, and the beta-amyloid precursor protein intracellular domain in vivo. Proc. Natl. Acad. Sci. U.S.A. 2003, 100:4162-4167.
16. Fukumoto H., Asami-Odaka A., Suzuki N., Shimada H., Ihara Y., Iwatsubo T. Amyloid beta protein deposition in normal aging has the same characteristics as that in Alzheimer's disease. Predominance of A beta 42(43) and association of A beta 40 with cored plaques. Am. J. Pathol. 1996, 148:259-265.
17. Gunstad J., Spitznagel M.B., Glickman E., Alexander T., Juvancic-Heltzel J., Walter K., Murray L. {beta}-Amyloid is Associated with Reduced Cognitive Function in Healthy Older Adults. J. Neuropsychiatry Clin. Neurosci. 2008, 20:327-330.
18. Hashimoto Y., Kobayashi A., Yamazaki N., Sugawara Y., Takada Y., Takada A. Relationship between age and plasma t-PA, PA-inhibitor, and PA activity. Thromb. Res. 1987, 46:625-633.
19. Head E., Torp R. Insights into Abeta and presenilin from a canine model of human brain aging. Neurobiol. Dis. 2002, 9:1-10.
20. Hsiao K., Chapman P., Nilsen S., Eckman C., Harigaya Y., Younkin S., Yang F., Cole G. Correlative memory deficits, Abeta elevation, and amyloid plaques in transgenic mice [see comments]. Science 1996, 274:99-102.
21. Hsiao K.K., Borchelt D.R., Olson K., Johannsdottir R., Kitt C., Yunis W., Xu S., Eckman C., Younkin S., Price D., Iadecola C., Clark H.B., Carlson G. Age-related CNS disorder and early death in transgenic FVB/N mice overexpressing Alzheimer amyloid precursor proteins. Neuron 1995, 15:1203-1218.
22. Inestrosa N.C., Reyes A.E., Chacon M.A., Cerpa W., Villalon A., Montiel J., Merabachvili G., Aldunate R., Bozinovic F., Aboitiz F. Human-like rodent amyloid-beta-peptide determines Alzheimer pathology in aged wild-type Octodon degu. Neurobiol. Aging 2005, 26:1023-1028.
23. Iwata N., Tsubuki S., Takaki Y., Shirotani K., Lu B., Gerard N.P., Gerard C., Hama E., Lee H.J., Saido T.C. Metabolic regulation of brain Abeta by neprilysin. Science 2001, 292:1550-1552.
24. Jacobsen J.S., Comery T.A., Martone R.L., Elokdah H., Crandall D.L., Oganesian A., Aschmies S., Kirksey Y., Gonzales C., Xu J., Zhou H., Atchison K., Wagner E., Zaleska M.M., Das I., Arias R.L., Bard J., Riddell D., Gardell S.J., Abou-Gharbia M., Robichaud A., Magolda R., Vlasuk G.P., Bjornsson T., Reinhart P.H., Pangalos M.N. Enhanced clearance of Abeta in brain by sustaining the plasmin proteolysis cascade. Proc. Natl. Acad. Sci. U.S.A. 2008, 105:8754-8759.
25. Jankowsky J.L., Slunt H.H., Ratovitski T., Jenkins N.A., Copeland N.G., Borchelt D.R. Co-expression of multiple transgenes in mouse CNS: a comparison of strategies. Biomol. Eng. 2001, 17:157-165.
26. Kawarabayashi T., Younkin L.H., Saido T.C., Shoji M., Ashe K.H., Younkin S.G. Age-dependent changes in brain, CSF, and plasma amyloid (beta) protein in the Tg2576 transgenic mouse model of Alzheimer's disease. J. Neurosci. 2001, 21:372-381.
27. Klyubin I., Walsh D.M., Lemere C.A., Cullen W.K., Shankar G.M., Betts V., Spooner E.T., Jiang L., Anwyl R., Selkoe D.J., Rowan M.J. Amyloid beta protein immunotherapy neutralizes Abeta oligomers that disrupt synaptic plasticity in vivo. Nat. Med. 2005, 11:556-561.
28. Lambert M.P., Barlow A.K., Chromy B.A., Edwards C., Freed R., Liosatos M., Morgan T.E., Rozovsky I., Trommer B., Viola K.L., Wals P., Zhang C., Finch C.E., Krafft G.A., Klein W.L. Diffusible, nonfibrillar ligands derived from Abeta1-42 are potent central nervous system neurotoxins. Proc. Natl. Acad. Sci. U.S.A. 1998, 95:6448-6453.
29. Ledesma M.D., Da Silva J.S., Crassaerts K., Delacourte A., De Strooper B., Dotti C.G. Brain plasmin enhances APP alpha-cleavage and Abeta degradation and is reduced in Alzheimer's disease brains. EMBO Rep. 2000, 1:530-535.
30. Ledesma M.D., Abad-Rodriguez J., Galvan C., Biondi E., Navarro P., Delacourte A., Dingwall C., Dotti C.G. Raft disorganization leads to reduced plasmin activity in Alzheimer's disease brains. EMBO Rep. 2003, 4:1190-1196.
31. Lee J.Y., Kweon H.S., Cho E., Byun H.R., Kim D.H., Kim Y.H., Han P.L., Koh J.Y. Upregulation of tPA/plasminogen proteolytic system in the periphery of amyloid deposits in the Tg2576 mouse model of Alzheimer's disease. Neurosci. Lett. 2007, 423:82-87.
32. Li L., Cao D., Garber D.W., Kim H., Fukuchi K. Association of aortic atherosclerosis with cerebral beta-amyloidosis and learning deficits in a mouse model of Alzheimer's disease. Am. J. Pathol. 2003, 163:2155-2164.
33. Liu R.-M., Choi J. Age-associated decline of gamma-glutamylcysteine synthetase gene expression in rats. Free Radical Biol. Med. 2000, 28:566-574.
34. Loskutoff D.J., Samad F. The adipocyte and hemostatic balance in obesity: studies of PAI-1. Arterioscler Thromb. Vasc. Biol. 1998, 18:1-6.
35. Loskutoff D.J., Sawdey M., Keeton M., Schneiderman J. Regulation of PAI-1 gene expression in vivo. Thromb. Haemost. 1993, 70:135-137.
36. Maldonado T.A., Jones R.E., Norris D.O. Timing of neurodegeneration and beta-amyloid (Abeta) peptide deposition in the brain of aging kokanee salmon. J. Neurobiol. 2002, 53:21-35.
37. McKhann G., Drachman D., Folstein M., Katzman R., Price D., Stadlan E.M. Clinical diagnosis of Alzheimer's disease: report of the NINCDS-ADRDA Work Group under the auspices of Department of Health and Human Services Task Force on Alzheimer's Disease. Neurology 1984, 34:939-944.
38. Melchor J.P., Pawlak R., Strickland S. The tissue plasminogen activator-plasminogen proteolytic cascade accelerates amyloid-beta (Abeta) degradation and inhibits Abeta-induced neurodegeneration. J. Neurosci. 2003, 23:8867-8871.
39. Mizutani A., Saito H., Matsuki N. Possible involvement of plasmin in long-term potentiation of rat hippocampal slices. Brain Res. 1996, 739:276-281.
40. Mu X.C., Higgins P.J. Differential growth state-dependent regulation of plasminogen activator inhibitor type-1 expression in senescent IMR-90 human diploid fibroblasts. J. Cell. Physiol. 1995, 165:647-657.
41. Nakagami Y., Abe K., Nishiyama N., Matsuki N. Laminin degradation by plasmin regulates long-term potentiation. J. Neurosci. 2000, 20:2003-2010.
42. Ohno M., Cole S.L., Yasvoina M., Zhao J., Citron M., Berry R., Disterhoft J.F., Vassar R. BACE1 gene deletion prevents neuron loss and memory deficits in 5XFAD APP/PS1 transgenic mice. Neurobiol. Disease 2007, 26:134-145.
43. Oyama F., Sawamura N., Kobayashi K., Morishima-Kawashima M., Kuramochi T., Ito M., Tomita T., Maruyama K., Saido T.C., Iwatsubo T., Capell A., Walter J., Grunberg J., Ueyama Y., Haass C., Ihara Y. Mutant presenilin 2 transgenic mouse: effect on an age-dependent increase of amyloid beta-protein 42 in the brain. J. Neurochem. 1998, 71:313-322.
44. Pang P.T., Teng H.K., Zaitsev E., Woo N.T., Sakata K., Zhen S., Teng K.K., Yung W.-H., Hempstead B.L., Lu B. Cleavage of proBDNF by tPA/plasmin is essential for long-term hippocampal plasticity. Science 2004, 306:487-491.
45. Park S.Y., Choi B., Cheon H., Pak Y.K., Kulawiec M., Singh K.K., Lee M.S. Cellular aging of mitochondrial DNA-depleted cells. Biochem. Biophys. Res. Commun. 2004, 325:1399-1405.
46. Selkoe D.J. The genetics and molecular pathology of Alzheimer's disease: roles of amyloid and the presenilins. Neurol. Clin. 2000, 18:903-922.
47. Selkoe D.J. Clearing the brain's amyloid cobwebs. Neuron 2001, 32:177-180.
48. Sturchler-Pierrat C., Abramowski D., Duke M., Wiederhold K.H., Mistl C., Rothacher S., Ledermann B., Burki K., Frey P., Paganetti P.A., Waridel C., Calhoun M.E., Jucker M., Probst A., Staufenbiel M., Sommer B. Two amyloid precursor protein transgenic mouse models with Alzheimer disease-like pathology. Proc. Natl. Acad. Sci. U.S.A. 1997, 94:13287-13292.
49. Sundell I.B., Nilsson T.K., Ranby M., Hallmans G., Hellsten G. Fibrinolytic variables are related to age, sex, blood pressure, and body build measurements: a cross-sectional study in Norsjo, Sweden. J. Clin. Epidemiol. 1989, 42:719-723.
50. Sutton R., Keohane M.E., VanderBerg S.R., Gonias S.L. Plasminogen activator inhibitor-1 in the cerebrospinal fluid as an index of neurological disease. Blood Coagul. Fibrinolysis 1994, 5:167-171.
51. Takeshita K., Yamamoto K., Ito M., Kondo T., Matsushita T., Hirai M., Kojima T., Nishimura M., Nabeshima Y., Loskutoff D.J., Saito H., Murohara T. Increased expression of plasminogen activator inhibitor-1 with fibrin deposition in a murine model of aging, "Klotho" mouse. Semin. Thromb. Hemost. 2002, 28:545-554.
52. Takeuchi A., Irizarry M.C., Duff K., Saido T.C., Hsiao Ashe K., Hasegawa M., Mann D.M., Hyman B.T., Iwatsubo T. Age-related amyloid beta deposition in transgenic mice overexpressing both Alzheimer mutant presenilin 1 and amyloid beta precursor protein Swedish mutant is not associated with global neuronal loss. Am. J. Pathol. 2000, 157:331-339.
53. Tofler G.H., Massaro J., Levy D., Mittleman M., Sutherland P., Lipinska I., Muller J.E., D'Agostino R.B. Relation of the prothrombotic state to increasing age (from the Framingham Offspring Study). Am. J. Cardiol. 2005, 96:1280-1283.
54. Tucker H.M., Kihiko-Ehmann M., Wright S., Rydel R.E., Estus S. Tissue plasminogen activator requires plasminogen to modulate amyloid-beta neurotoxicity and deposition. J. Neurochem. 2000, 75:2172-2177.
55. Tucker H.M., Kihiko M., Caldwell J.N., Wright S., Kawarabayashi T., Price D., Walker D., Scheff S., McGillis J.P., Rydel R.E., Estus S. The plasmin system is induced by and degrades amyloid-beta aggregates. J. Neurosci. 2000, 20:3937-3946.
56. Van Nostrand W.E., Porter M. Plasmin cleavage of the amyloid beta-protein: alteration of secondary structure and stimulation of tissue plasminogen activator activity. Biochemistry 1999, 38:11570-11576.
57. Vaucher E., Aumont N., Pearson D., Rowe W., Poirier J., Kar S. Amyloid beta peptide levels and its effects on hippocampal acetylcholine release in aged, cognitively-impaired and -unimpaired rats. J. Chem. Neuroanat. 2001, 21:323-329.
58. Vayalil P.K., Olman M., Murphy-Ullrich J.E., Postlethwait E.M., Liu R.M. Glutathione restores collagen degradation in TGF-beta-treated fibroblasts by blocking plasminogen activator inhibitor-1 expression and activating plasminogen. Am. J. Physiol. Lung Cell. Mol. Physiol. 2005, 289:L937-945.
59. Walsh D.M., Klyubin I., Fadeeva J.V., Cullen W.K., Anwyl R., Wolfe M.S., Rowan M.J., Selkoe D.J. Naturally secreted oligomers of amyloid beta protein potently inhibit hippocampal long-term potentiation in vivo. Nature 2002, 416:535-539.
60. West M.D., Shay J.W., Wright W.E., Linskens M.H. Altered expression of plasminogen activator and plasminogen activator inhibitor during cellular senescence. Exp. Gerontol. 1996, 31:175-193.
61. Yamamoto K., Takeshita K., Kojima T., Takamatsu J., Saito H. Aging and plasminogen activator inhibitor-1 (PAI-1) regulation: implication in the pathogenesis of thrombotic disorders in the elderly. Cardiovasc. Res. 2005, 66:276-285.
62. Yan P., Hu X., Song H., Yin K., Bateman R.J., Cirrito J.R., Xiao Q., Hsu F.F., Turk J.W., Xu J., Hsu C.Y., Holtzman D.M., Lee J.M. Matrix metalloproteinase-9 degrades amyloid-beta fibrils in vitro and compact plaques in situ. J. Biol. Chem. 2006, 281:24566-24574.
63. Zhou S., Zhou H., Walian P.J., Jap B.K. CD147 is a regulatory subunit of the gamma-secretase complex in Alzheimer's disease amyloid beta-peptide production. Proc. Natl. Acad. Sci. U.S.A. 2005, 102:7499-7504.