Fibrinogen and altered hemostasis in Alzheimer's disease

Journal of Alzheimer's Disease

Volumn 32, Issue 3, 2012, Pages 599-608

  Cortes Canteli, Marta ^a   Zamolodchikov, Daria ^a   Ahn, Hyung Jin ^a   Strickland, Sidney ^a   Norris, Erin H ^a  

^a ROCKEFELLER UNIVERSITY   (United States)

Author keywords

Blood brain barrier; blood coagulation; cerebral amyloid angiopathy; fibrinogen; hemostasis; thrombosis

Indexed keywords

ANTICOAGULANT AGENT; FIBRINOGEN; LOW MOLECULAR WEIGHT HEPARIN;

ALZHEIMER DISEASE; ANTICOAGULANT THERAPY; BLOOD BRAIN BARRIER; BLOOD CLOTTING; BRAIN BLOOD FLOW; CELL SURFACE; CELL VIABILITY; CEREBROVASCULAR ACCIDENT; CEREBROVASCULAR DISEASE; COGNITIVE DEFECT; HUMAN; IN VIVO STUDY; NERVE DEGENERATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN PROTEIN INTERACTION; REVIEW; VASCULAR AMYLOIDOSIS;

EID: 84872230307     PISSN: 13872877     EISSN: 18758908     Source Type: Journal    
DOI: 10.3233/JAD-2012-120820     Document Type: Review

References (94)

1. Humpel C (2011) Chronic mild cerebrovascular dysfunction as a cause for alzheimer's disease? Exp Gerontol 46, 225232.
2. Iadecola C (2010) The overlap between neurodegenerative and vascular factors in the pathogenesis of dementia. Acta Neuropathol 120, 287-296.
3. de la Torre JC (2004) Is alzheimer's disease a neurodegenerative or a vascular disorder? Data, dogma, and dialectics. Lancet Neurol 3, 184-190. (Pubitemid 38232669)
4. Zlokovic BV (2010) Neurodegeneration and the neurovascular unit. Nat Med 16, 1370-1371.
5. Hardy J, Selkoe DJ (2002) The amyloid hypothesis of alzheimer's disease: Progress and problems on the road to therapeutics. Science 297, 353-356. (Pubitemid 34790756)
6. Wood H (2010) alzheimer disease: Fibrinogen links amyloid with vascular dysfunction. Nat Rev Neurol 6, 413.
7. Weisel JW (2005) Fibrinogen and fibrin. Adv Protein Chem 70, 247-299. (Pubitemid 40544785)
8. Mustard JF, Packham MA, Kinlough-Rathbone RL, Perry DW,Regoeczi E (1978) Fibrinogen and ADP-induced platelet aggregation. Blood 52, 453-466.
9. Lominadze D, Dean WL, Tyagi SC, Roberts AM (2010) Mechanisms of fibrinogen-induced microvascular dysfunction during cardiovascular disease. Acta Physiol 198, 1-13.
10. Ernst E, Resch KL (1993) Fibrinogen as a cardiovascular risk factor:Ameta-Analysis and reviewof the literature. Ann Intern Med 118, 956-963. (Pubitemid 23164134)
11. Xu G, Zhang H, Zhang S, FanX, LiuX(2008) Plasma fibrinogen is associated with cognitive decline and risk for dementia in patients with mild cognitive impairment. Int J Clin Pract 62, 1070-1075. (Pubitemid 351793581)
12. van Oijen M,Witteman JC, Hofman A,Koudstaal PJ, Breteler MM (2005) Fibrinogen is associated with an increased risk of alzheimer disease and vascular dementia. Stroke 36, 26372641.
13. Thambisetty M, Simmons A, Hye A, Campbell J, Westman E, Zhang Y, Wahlund LO, Kinsey A, Causevic M, Killick R, Kloszewska I, Mecocci P, Soininen H, Tsolaki M, Vellas B, Spenger C, Lovestone S (2011) Plasma biomarkers of brain atrophy in alzheimer's disease. Plos One 6, e28527.
14. Cortes-Canteli M, Paul J, Norris EH, Bronstein R, Ahn HJ, Zamolodchikov D, Bhuvanendran S, Fenz KM, Strickland S (2010) Fibrinogen and beta-Amyloid association alters thrombosis and fibrinolysis: A possible contributing factor to alzheimer's disease. Neuron 66, 695-709.
15. Fiala M, Liu QN, Sayre J, PopV, BrahmandamV, Graves MC, Vinters HV (2002) Cyclooxygenase-2-positive macrophages infiltrate the alzheimer's disease brain and damage the bloodbrain barrier. Eur J Clin Invest 32, 360-371. (Pubitemid 36228397)
16. Jantaratnotai N, Schwab C, Ryu JK, McGeer PL, McLarnon JG (2010) Converging perturbed microvasculature and microglial clusters characterize alzheimer disease brain. Curr alzheimer Res 7, 625-636.
17. Lipinski B, Sajdel-Sulkowska EM (2006) New insight into alzheimer disease: Demonstration of fibrin(ogen)-Serum albumin insoluble deposits in brain tissue. alzheimer Dis Assoc Disord 20, 323-326. (Pubitemid 44900953)
18. Paul J, Strickland S, Melchor JP (2007) Fibrin deposition accelerates neurovascular damage and neuroinflammation in mouse models of alzheimer's disease. J Exp Med 204, 19992008. (Pubitemid 47236333)
19. Ryu JK, McLarnon JG (2009) A leaky blood-Brain barrier, fibrinogen infiltration and microglial reactivity in inflamed alzheimer's disease brain. J Cell Mol Med 13, 29112925.
20. Viggars AP,Wharton SB, Simpson JE, Matthews FE, Brayne C, Savva GM, Garwood C, Drew D, Shaw PJ, Ince PG (2011) Alterations in the blood brain barrier in ageing cerebral cortex in relationship to Alzheimer-Type pathology: A study in the MRC-CFASpopulation neuropathology cohort. Neurosci Lett 505, 25-30.
21. Ujiie M, Dickstein DL, Carlow DA, Jefferies WA (2003) Blood-Brain barrier permeability precedes senile plaque formation in an alzheimer disease model. Microcirculation 10, 463-470. (Pubitemid 39004272)
22. Zipser BD, Johanson CE, Gonzalez L, Berzin TM, Tavares R, Hulette CM, Vitek MP, Hovanesian V, Stopa EG (2007) Microvascular injury and blood-Brain barrier leakage in alzheimer's disease. Neurobiol Aging 28, 977-986. (Pubitemid 46635913)
23. DeMattos RB, Bales KR, Cummins DJ, Dodart JC, Paul SM, Holtzman DM (2001) Peripheral anti-A beta antibody alters CNS and plasma A beta clearance and decreases brain A beta burden in a mouse model of alzheimer's disease. Proc Natl Acad Sci U S A 98, 8850-8855. (Pubitemid 32678116)
24. Sagare A, Deane R, Bell RD, Johnson B, Hamm K, Pendu R, Marky A, Lenting PJ, Wu Z, Zarcone T, Goate A, Mayo K, Perlmutter D, Coma M, Zhong Z, Zlokovic BV (2007) Clearance of amyloid-Beta by circulating lipoprotein receptors. Nat Med 13, 1029-1031. (Pubitemid 47517512)
25. Yepes M, Sandkvist M, Moore EG, Bugge TH, Strickland DK, Lawrence DA (2003) Tissue-Type plasminogen activator induces opening of the blood-Brain barrier via the LDL receptor-Related protein. J Clin Invest 112, 15331540. (Pubitemid 38056279)
26. Takechi R, Galloway S, Pallebage-Gamarallage MM, Lam V, Mamo JC (2010) Dietary fats, cerebrovasculature integrity and alzheimer's disease risk. Prog Lipid Res 49, 159170.
27. Weis SM (2008) Vascular permeability in cardiovascular disease and cancer. Curr Opin Hematol 15, 243-249. (Pubitemid 351509347)
28. Wardlaw JM, Sandercock PA, Dennis MS, Starr J (2003) Is breakdown of the blood-Brain barrier responsible for lacunar stroke, leukoaraiosis, and dementia? Stroke 34, 806812.
29. Tyagi N, Roberts AM, Dean WL, Tyagi SC, Lominadze D (2008) Fibrinogen induces endothelial cell permeability. Mol Cell Biochem 307, 13-22. (Pubitemid 350238642)
30. Patibandla PK, Tyagi N, Dean WL, Tyagi SC, Roberts AM, Lominadze D (2009) Fibrinogen induces alterations of endothelial cell tight junction proteins. J Cell Physiol 221, 195-203.
31. Nicoll JA, Yamada M, Frackowiak J, Mazur-Kolecka B, Weller RO (2004) Cerebral amyloid angiopathy plays a direct role in the pathogenesis of alzheimer's disease. Pro-CAA position statement. Neurobiol Aging 25, 589-597; discussion 603-584. (Pubitemid 38686478)
32. Thal DR, Griffin WS, de Vos RA, Ghebremedhin E (2008) Cerebral amyloid angiopathy and its relationship to alzheimer's disease. Acta Neuropathol 115, 599-609.
33. Vinters HV (1987) Cerebral amyloid angiopathy A critical review. Stroke 18, 311-324. (Pubitemid 17059655)
34. Attems J, Jellinger K, Thal DR, Van Nostrand W (2011) Review: Sporadic cerebral amyloid angiopathy. Neuropathol Appl Neurobiol 37, 75-93.
35. Thal DR, Capetillo-Zarate E, Larionov S, Staufenbiel M, Zurbruegg S, Beckmann N (2009) Capillary cerebral amyloid angiopathy is associated with vessel occlusion and cerebral blood flow disturbances. Neurobiol Aging 30, 19361948.
36. Smith EE, Greenberg SM(2009) Beta-Amyloid, blood vessels, and brain function. Stroke 40, 2601-2606.
37. Staffen W, Bergmann J, Schonauer U, Zauner H, Kronbichler M, Golaszewski S, Ladurner G (2009) Cerebral perfusion (HMPAO-SPECT) in patients with depression with cognitive impairment versus those with mild cognitive impairment and dementia of alzheimer's type: A semiquantitative and automated evaluation. Eur J Nucl Med Mol Imaging 36, 801810.
38. Johnson NA, Jahng GH, Weiner MW, Miller BL, Chui HC, Jagust WJ, Gorno-Tempini ML, Schuff N (2005) Pattern of cerebral hypoperfusion in alzheimer disease and mild cognitive impairment measured with arterial spinlabeling MR imaging: Initial experience. Radiology 234, 851-859. (Pubitemid 40250829)
39. Klohs J, Baltes C, Princz-Kranz F, Ratering D, Nitsch RM, Knuesel I, Rudin M (2012) Contrast-enhanced magnetic resonance microangiography reveals remodeling of the cerebral microvasculature in transgenic ArcAbeta mice. J Neurosci 32, 1705-1713.
40. Ahn HJ, Zamolodchikov D, Cortes-Canteli M, Norris EH, Glickman JF, Strickland S (2010) alzheimer's disease peptide beta-Amyloid interacts with fibrinogen and induces its oligomerization. Proc Natl Acad Sci U S A 107, 2181221817.
41. Garcia-Alloza M, Gregory J, Kuchibhotla KV, Fine S,Wei Y, Ayata C, Frosch MP, Greenberg SM, Bacskai BJ (2011) Cerebrovascular lesions induce transient beta-Amyloid deposition. Brain 134, 3697-3707.
42. Zamolodchikov D, Strickland S (2012) A delays fibrin clot lysis by altering fibrin structure and attenuating plasminogen binding to fibrin. Blood 119, 3342-3351.
43. Lam CK, Yoo T, Hiner B, Liu Z, Grutzendler J (2010) Embolus extravasation is an alternative mechanism for cerebral microvascular recanalization. Nature 465, 478-482.
44. Bergamaschini L, Rossi E, Storini C, Pizzimenti S, Distaso M, Perego C, De Luigi A, Vergani C, De Simoni MG (2004) Peripheral treatment with enoxaparin, a lowmolecular weight heparin, reduces plaques and beta-Amyloid accumulation in a mouse model of alzheimer's disease. J Neurosci 24, 41814186. (Pubitemid 38620793)
45. Timmer NM, van Dijk L, van der Zee CE, Kiliaan A, de Waal RM, Verbeek MM (2010) Enoxaparin treatment administered at both early and late stages of amyloid beta deposition improves cognition of APPswe/PS1dE9 mice with differential effects on brain Abeta levels. Neurobiol Dis 40, 340-347.
46. Ratner J, Rosenberg G, Kral VA, Engelsmann F (1972) Anticoagulant therapy for senile dementia. J Am Geriatr Soc 20, 556-559.
47. Walsh AC (1996) Anticoagulant therapy for alzheimer's disease. J Neuropsychiatry Clin Neurosci 8, 361-362.
48. Walsh AC, Walsh BH, Melaney C (1978) Senile-presenile dementia: Follow-up data on an effective psychotherapyanticoagulant regimen. J Am Geriatr Soc 26, 467-470. (Pubitemid 9042951)
49. Barber M, Tait RC, Scott J, Rumley A, Lowe GD, Stott DJ (2004) Dementia in subjects with atrial fibrillation: Hemostatic function and the role of anticoagulation. J Thromb Haemost 2, 1873-1878. (Pubitemid 40192736)
50. Eikelboom JW, Wallentin L, Connolly SJ, Ezekowitz M, Healey JS, Oldgren J, Yang S, Alings M, Kaatz S, Hohnloser SH, Diener HC, Franzosi MG, Huber K, Reilly P, Varrone J, Yusuf S Risk of bleeding with 2 doses of dabigatran compared with warfarin in older and younger patients with atrial fibrillation: An analysis of the randomized evaluation of longterm anticoagulant therapy (RE-LY) trial. Circulation 123, 2363-2372.
51. Purandare N, Burns A (2009) Cerebral emboli in the genesis of dementia. J Neurol Sci 283, 17-20.
52. Purandare N, Burns A, Morris J, Perry EP, Wren J, McCollum C (2012) Association of cerebral emboli with accelerated cognitive deterioration in alzheimer's disease and vascular dementia. Am J Psychiatry 169, 300-308.
53. Brundel M, de Bresser J, van Dillen JJ, Kappelle LJ, Biessels GJ (2012) Cerebral microinfarcts: A systematic review of neuropathological studies. J Cereb Blood Flow Metab 32, 425-436.
54. Schneider JA, Boyle PA, Arvanitakis Z, Bienias JL, Bennett DA (2007) Subcortical infarcts, alzheimer's disease pathology, and memory function in older persons. Ann Neurol 62, 59-66. (Pubitemid 47235281)
55. Cumming TB, Brodtmann A (2011) Can stroke cause neurodegenerative dementia? Int J Stroke 6, 416-424.
56. Bangen KJ, Delano-Wood L, Wierenga CE, McCauley A, Jeste DV, Salmon DP, Bondi MW (2010) Associations between stroke risk and cognition in normal aging and alzheimer's disease with and without depression. Int J Geriatr Psychiatry 25, 175-182.
57. Furie B, FurieBC(2008) Mechanisms of thrombus formation. N Engl J Med 359, 938-949.
58. Mari D, Parnetti L, Coppola R, Bottasso B, Reboldi GP, Senin U, MannucciPM(1996) Hemostasis abnormalities in patients with vascular dementia and alzheimer's disease. Thromb Haemost 75, 216-218. (Pubitemid 26081469)
59. Gupta A, Watkins A, Thomas P, Majer R, Habubi N, Morris G, Pansari K (2005) Coagulation and inflammatory markers in alzheimer's and vascular dementia. Int J Clin Pract 59, 52-57. (Pubitemid 40260114)
60. Bots ML, vanKooten F, Breteler MM, Slagboom PE, Hofman A, Haverkate F, Meijer P, Koudstaal PJ, Grobbee DE, Kluft C (1998) Response to activated protein C in subjects with and without dementia The Dutch Vascular Factors in Dementia Study. Haemostasis 28, 209-215. (Pubitemid 29309602)
61. Peyvandi F, Garagiola I, Baronciani L (2011) Role of von Willebrand factor in the haemostasis. Blood Transfus 9(Suppl 2), s3-S8.
62. Stott DJ, Robertson M, Rumley A, Welsh P, Sattar N, Packard CJ, Shepherd J, Trompet S, Westendorp RG, de Craen AJ, Jukema JW, Buckley B, Ford I, Lowe GD (2010) Activation of hemostasis and decline in cognitive function in older people. Arterioscler Thromb Vasc Biol 30, 605611.
63. Wolberg AS, Campbell RA (2008) Thrombin generation, fibrin clot formation and hemostasis. Transfus Apher Sci 38, 15-23.
64. Grammas P, Samany PG, Thirumangalakudi L (2006) Thrombin and inflammatory proteins are elevated in alzheimer's disease microvessels: Implications for disease pathogenesis. J Alzheimers Dis 9, 51-58.
65. Yin X,Wright J,Wall T, Grammas P (2010) Brain endothelial cells synthesize neurotoxic thrombin in alzheimer's disease. Am J Pathol 176, 1600-1606.
66. Ledesma MD, Da Silva JS, Crassaerts K, Delacourte A, De Strooper B, Dotti CG (2000) Brain plasmin enhances APP alpha-cleavage and Abeta degradation and is reduced in alzheimer's disease brains. EMBO Rep 1, 530-535.
67. Fabbro S, Seeds NW (2009) Plasminogen activator activity is inhibited while neuroserpin is up-Regulated in the alzheimer disease brain. J Neurochem 109, 303-315.
68. Melchor JP, Pawlak R, Strickland S (2003) The tissue plasminogen activator-plasminogen proteolytic cascade accelerates amyloid-Beta (Abeta) degradation and inhibits Abeta-induced neurodegeneration. J Neurosci 23, 88678871. (Pubitemid 37210899)
69. Sevush S, JyW, Horstman LL, MaoWW,Kolodny L, Ahn YS (1998) Platelet activation in alzheimer disease. Arch Neurol 55, 530-536. (Pubitemid 28182700)
70. Ciabattoni G, Porreca E, Di Febbo C, Di Iorio A, Paganelli R, Bucciarelli T, Pescara L, Del Re L, Giusti C, Falco A, Sau A, Patrono C, Davi G (2007) Determinants of platelet activation in alzheimer's disease. Neurobiol Aging 28, 336342.
71. Dale GL (2005) Coated-platelets: An emerging component of the procoagulant response. J Thromb Haemost 3, 21852192. (Pubitemid 41727196)
72. Prodan CI, Ross ED, Vincent AS, Dale GL (2007) Coatedplatelets correlate with disease progression in alzheimer disease. J Neurol 254, 548-549. (Pubitemid 46786713)
73. Prodan CI, Ross ED, Vincent AS, Dale GL (2008) Rate of progression in alzheimer's disease correlates with coated-platelet levels-A longitudinal study. Transl Res 152, 99-102.
74. Tang K, Hynan LS, Baskin F, Rosenberg RN (2006) Platelet amyloid precursor protein processing: A bio-marker for alzheimer's disease. J Neurol Sci 240, 53-58. (Pubitemid 41814953)
75. Amor S, Puentes F, Baker D, van der Valk P (2010) Inflammation in neurodegenerative diseases. Immunology 129, 154-169.
76. Levi M, van der Poll T, Buller HR (2004) Bidirectional relation between inflammation and coagulation. Circulation 109, 2698-2704. (Pubitemid 38737913)
77. McGeer EG, McGeer PL (2001) Innate immunity in alzheimer's disease: A model for local inflammatory reactions. Mol Interventions 1, 22-29.
78. Shen Y, Meri S (2003) Yin and Yang: Complement activation and regulation in alzheimer's disease. Prog Neurobiol 70, 463-472. (Pubitemid 37249427)
79. Rogers J, Cooper NR, Webster S, Schultz J, McGeer PL, Styren SD, Civin WH, Brachova L, Bradt B, Ward P (1992) Complement activation by beta-Amyloid in alzheimer disease. Proc Natl Acad Sci U S A 89, 1001610020.
80. Shen Y, Lue L-F, Yang L-B, Roher A, Kuo Y-M, Strohmeyer R, Goux WJ, Lee V, Johnson GVW, Webster SD, Cooper NR, Bradt B, Rogers J (2001) Complement activation by neurofibrillary tangles in alzheimer's disease. Neurosci Lett 305, 165-168. (Pubitemid 32525831)
81. Yasojima K, Schwab C, McGeer EG, McGeer PL (1999) Up-Regulated production and activation of the complement system in alzheimer's disease brain. Am J Pathol 154, 927936.
82. Webster S, Lue LF, Brachova L, Tenner AJ, McGeer PL, Terai K,Walker DG, Bradt B, Cooper NR, Rogers J (1997) Molecular and cellular characterization of the membrane attack complex, C5b-9, in alzheimer's disease. Neurobiol Aging 18, 415-421. (Pubitemid 27436086)
83. Amara U, Flierl MA, Rittirsch D, Klos A, Chen H, Acker B, Brückner UB, Nilsson B, Gebhard F, Lambris JD, HuberLang M (2010) Molecular intercommunication between the complement and coagulation systems. J Immunol 185, 56285636.
84. Hess K, Alzahrani SH, Mathai M, Schroeder V, Carter AM, Howell G, Koko T, Strachan MW, Price JF, Smith KA, Grant PJ, Ajjan RA (2012) A novel mechanism for hypofibrinolysis in diabetes: The role of complement C3. Diabetologia 55, 1103-1113.
85. Ikeda K, Nagasawa K, Horiuchi T, Tsuru T, Nishizaka H, Niho Y (1997) C5a induces tissue factor activity on endothelial cells. Thromb Haemost 77, 394-398. (Pubitemid 27084936)
86. Wojta J, Huber K, Valent P (2003) New aspects in thrombotic research: Complement induced switch in mast cells from a profibrinolytic to a prothrombotic phenotype. Pathophysiol Haemost Thromb 33, 438-441. (Pubitemid 40278721)
87. Ritis K, Doumas M, Mastellos D, Micheli A, Giaglis S, Magotti P, Rafail S, Kartalis G, Sideras P, Lambris JD (2006) A novel C5a receptor-Tissue factor cross-Talk in neutrophils links innate immunity to coagulation pathways. J Immunol 177, 4794-4802. (Pubitemid 44469814)
88. Solito E, Sastre M (2012) Microglia function in alzheimer's disease. Front Pharmacol 3, 14.
89. Flick MJ,DuX,WitteDP, JirouskovaM, SolovievDA, Busuttil SJ, Plow EF, Degen JL (2004) Leukocyte engagement of fibrin(ogen) via the integrin receptor alphaMbeta2/Mac-1 is critical for host inflammatory response in vivo. J Clin Invest 113, 1596-1606. (Pubitemid 39071683)
90. Davalos D, Akassoglou K (2012) Fibrinogen as a key regulator of inflammation in disease. Semin Immunopathol 34, 43-62.
91. Cortes-Canteli M, Strickland S (2009) Fibrinogen, a possible key player in alzheimer's disease. J Thromb Haemost 7(Suppl 1), 146-150.
92. Craig-Schapiro R, Kuhn M, Xiong C, Pickering EH, Liu J, Misko TP, Perrin RJ, Bales KR, Soares H, Fagan AM, Holtzman DM (2011) Multiplexed immunoassay panel identifies novel CSF biomarkers for alzheimer's disease diagnosis and prognosis. Plos One 6, e18850.
93. Vafadar-Isfahani B, Ball G, Coveney C, Lemetre C, Boocock D, Minthon L, Hansson O, Miles AK, Janciauskiene SM, Warden D, Smith AD, Wilcock G, Kalsheker N, Rees R, Matharoo-Ball B, Morgan K (2012) Identification of SPARClike 1 protein as part of a biomarker panel for alzheimer's disease in cerebrospinal fluid. J Alzheimers Dis 28, 625636.
94. Lee JW, Namkoong H, Kim HK, Kim S, Hwang DW, Na HR, Ha SA, Kim JR, Kim JW (2007) Fibrinogen gamma-A chain precursor in CSF: A candidate biomarker for alzheimer's disease. BMC Neurol 7, 14.