Induction of hyperhomocysteinemia models vascular dementia by induction of cerebral microhemorrhages and neuroinflammation

Journal of Cerebral Blood Flow and Metabolism

Volumn 33, Issue 5, 2013, Pages 708-715

  Sudduth, Tiffany L ^a   Powell, David K ^a   Smith, Charles D ^a   Greenstein, Abigail ^a   Wilcock, Donna M ^a  

^a UNIVERSITY OF KENTUCKY   (United States)

Author keywords

animal models; hemosiderin; homocysteinemia; inflammation; vascular dementia

Indexed keywords

CYANOCOBALAMIN; FOLIC ACID; GELATINASE A; GELATINASE B; HOMOCYSTEINE; INTERLEUKIN 1BETA; INTERLEUKIN 6; METHIONINE; PYRIDOXINE; TUMOR NECROSIS FACTOR ALPHA;

AMINO ACID BLOOD LEVEL; AMNESIA; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRAIN HEMORRHAGE; BRAIN TISSUE; CONTROLLED STUDY; DIET RESTRICTION; DIETARY INTAKE; DISEASE MODEL; HISTOPATHOLOGY; HYPERHOMOCYSTEINEMIA; MICROGLIA; MULTIINFARCT DEMENTIA; NERVOUS SYSTEM INFLAMMATION; NONHUMAN; NUCLEAR MAGNETIC RESONANCE IMAGING; PHENOTYPE; PRIORITY JOURNAL; PROTEIN EXPRESSION; SPATIAL MEMORY;

ANIMALS; BRAIN; CEREBRAL HEMORRHAGE; DEMENTIA, VASCULAR; DIET; DISEASE MODELS, ANIMAL; FOLIC ACID; HUMANS; HYPERHOMOCYSTEINEMIA; INFLAMMATION; INTERLEUKIN-1BETA; INTERLEUKIN-6; MATRIX METALLOPROTEINASE 2; MATRIX METALLOPROTEINASE 9; MEMORY DISORDERS; METHIONINE; MICE; MICE, INBRED C57BL; VITAMIN B 12; VITAMIN B 6;

EID: 84877577810     PISSN: 0271678X     EISSN: 15597016     Source Type: Journal    
DOI: 10.1038/jcbfm.2013.1     Document Type: Article

References (40)

1. Roman GC. Vascular dementia revisited: diagnosis, pathogenesis, treatment, and prevention. Med Clin North Am 2002; 86: 477-499.
2. Dubois MF, Hebert R. The incidence of vascular dementia in Canada: a comparison with Europe and East Asia. Neuroepidemiology 2001; 20: 179-187.
3. Kammoun S, Gold G, Bouras C, Giannakopoulos P, McGee W, Herrmann F et al. Immediate causes of death of demented and non-demented elderly. Acta Neurol Scand Suppl 2000; 176: 96-99.
4. Schneider JA, Arvanitakis Z, Leurgans SE, Bennett DA. The neuropathology of probable Alzheimer disease and mild cognitive impairment. Ann Neurol 2009; 66: 200-208.
5. Gorelick PB, Scuteri A, Black SE, Decarli C, Greenberg SM, Iadecola C et al. Vascular contributions to cognitive impairment and dementia: a statement for healthcare professionals from the American Heart Association/American Stroke Association. Stroke 2011; 42: 2672-2713.
6. Mudd SH, Finkelstein JD, Irreverre F, Laster L. Homocystinuria: an enzymatic defect. Science 1964; 143: 1443-1445.
7. Troen AM, Shea-Budgell M, Shukitt-Hale B, Smith DE, Selhub J, Rosenberg IH. B-vitamin deficiency causes hyperhomocysteinemia and vascular cognitive impairment in mice. Proc Natl Acad Sci USA 2008; 105: 12474-12479.
8. Hofmann MA, Lalla E, Lu Y, Gleason MR, Wolf BM, Tanji N et al. Hyperhomocysteinemia enhances vascular inflammation and accelerates atherosclerosis in a murine model. J Clin Invest 2001; 107: 675-683.
9. Pirchl M, Ullrich C, Humpel C. Differential effects of short-and long-term hyperhomocysteinaemia on cholinergic neurons, spatial memory and microbleedings in vivo in rats. Eur J Neurosci 2010; 32: 1516-1527.
10. Alamed J, Wilcock DM, Diamond DM, Gordon MN, Morgan D. Two-day radial-arm water maze learning and memory task; robust resolution of amyloid-related memory deficits in transgenic mice. Nat Protoc 2006; 1: 1671-1679.
11. Wilcock DM, Lewis MR, Van Nostrand WE, Davis J, Previti ML, Gharkholonarehe N et al. Progression of amyloid pathology to Alzheimer's disease pathology in an amyloid precursor protein transgenic mouse model by removal of nitric oxide synthase 2. J Neurosci 2008; 28: 1537-1545.
12. Wilcock DM, Rojiani A, Rosenthal A, Subbarao S, Freeman MJ, Gordon MN et al. Passive immunotherapy against Abeta in aged APP-transgenic mice reverses cognitive deficits and depletes parenchymal amyloid deposits in spite of increased vascular amyloid and microhemorrhage. J Neuroinflammation 2004; 1: 24.
13. Sudduth TL, Wilson JG, Everhart A, Colton CA, Wilcock DM. Lithium treatment of APPSwDI/NOS2-/-mice leads to reduced hyperphosphorylated tau, increased amyloid deposition and altered inflammatory phenotype. PLoS ONE 2012; 7: e31993.
14. Wilcock DM, Zhao Q, Morgan D, Gordon MN, Everhart A, Wilson JG et al. Diverse inflammatory responses in transgenic mouse models of AD and the effect of immunotherapy on these responses. ASN neuro 2011; 3: 249-258.
15. Livak KJ, Schmittgen TD. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. Methods 2001; 25: 402-408.
16. Ernest S, Hosack A, O'Brien WE, Rosenblatt DS, Nadeau JH. Homocysteine levels in A/J and C57BL/6J mice: genetic, diet, gender, and parental effects. Physiol Genomics 2005; 21: 404-410.
17. Wilcock DM, Morgan D, Gordon MN, Taylor TL, Ridnour LA, Wink DA et al. Activation of matrix metalloproteinases following anti-Abeta immunotherapy; implications for microhemorrhage occurrence. J Neuroinflammation 2011; 8: 115.
18. Jiwa NS, Garrard P, Hainsworth AH. Experimental models of vascular dementia and vascular cognitive impairment: a systematic review. J Neurochem 2010; 115: 814-828.
19. Eikelboom JW, Lonn E, Genest Jr J, Hankey G, Yusuf S. Homocyst(e)ine and cardiovascular disease: a critical review of the epidemiologic evidence. Ann Intern Med 1999; 131: 363-375.
20. Bostom AG, Rosenberg IH, Silbershatz H, Jacques PF, Selhub J, D'Agostino RB et al. Nonfasting plasma total homocysteine levels and stroke incidence in elderly persons: the Framingham Study. Ann Intern Med 1999; 131: 352-355.
21. Van Dam F, Van Gool WA. Hyperhomocysteinemia and Alzheimer's disease: a systematic review. Arch Gerontol Geriatr 2009; 48: 425-430.
22. Lentz SR, Erger RA, Dayal S, Maeda N, Malinow MR, Heistad DD et al. Folate dependence of hyperhomocysteinemia and vascular dysfunction in cystathionine beta-synthase-deficient mice. Am J Physiol Heart Circ Physiol 2000; 279: H970-H975.
23. Chen Z, Karaplis AC, Ackerman SL, Pogribny IP, Melnyk S, Lussier-Cacan S et al. Mice deficient in methylenetetrahydrofolate reductase exhibit hyperhomocysteinemia and decreased methylation capacity, with neuropathology and aortic lipid deposition. Hum Mol Genet 2001; 10: 433-443.
24. Moore E, Mander A, Ames D, Carne R, Sanders K, Watters D. Cognitive impairment and vitamin B12: a review. Int Psychogeriatr 2012; 24: 541-556.
25. Lotto V, Choi SW, Friso S. Vitamin B6: a challenging link between nutrition and inflammation in CVD. Br J Nutr 2011; 106: 183-195.
26. Kumar M, Tyagi N, Moshal KS, Sen U, Kundu S, Mishra PK et al. Homocysteine decreases blood flow to the brain due to vascular resistance in carotid artery. Neurochem Int 2008; 53: 214-219.
27. Akahoshi N, Kobayashi C, Ishizaki Y, Izumi T, Himi T, Suematsu M et al. Genetic background conversion ameliorates semi-lethality and permits behavioral analyses in cystathionine beta-synthase-deficient mice, an animal model for hyperhomocysteinemia. Hum Mol Genet 2008; 17: 1994-2005.
28. Jadavji NM, Deng L, Leclerc D, Malysheva O, Bedell BJ, Caudill MA et al. Severe methylenetetrahydrofolate reductase deficiency in mice results in behavioral anomalies with morphological and biochemical changes in hippocampus. Mol Genet Metab 2012; 106: 149-159.
29. Luo F, Rustay NR, Seifert T, Roesner B, Hradil V, Hillen H et al. Magnetic resonance imaging detection and time course of cerebral microhemorrhages during passive immunotherapy in living amyloid precursor protein transgenic mice. J Pharmacol Exp Ther 2010; 335: 580-588.
30. Sperling RA, Jack Jr CR, Black SE, Frosch MP, Greenberg SM, Hyman BT et al. Amyloid-related imaging abnormalities in amyloid-modifying therapeutic trials: recommendations from the Alzheimer's Association Research Roundtable Workgroup. Alzheimers Dement 2011; 7: 367-385.
31. Goos JD, Henneman WJ, Sluimer JD, Vrenken H, Sluimer IC, Barkhof F et al. Incidence of cerebral microbleeds: a longitudinal study in a memory clinic population. Neurology 2010; 74: 1954-1960.
32. Yakushiji Y, Nishiyama M, Yakushiji S, Hirotsu T, Uchino A, Nakajima J et al. Brain microbleeds and global cognitive function in adults without neurological disorder. Stroke 2008; 39: 3323-3328.
33. Mosser DM, Edwards JP. Exploring the full spectrum of macrophage activation. Nat Rev Immunol 2008; 8: 958-969.
34. Wilcock DMA. Changing perspective on the role of neuroinflammation in Alzheimer's disease. Int J Alzheimers Dis 2012; 2012: 495243.
35. Kitazawa M, Cheng D, Tsukamoto MR, Koike MA, Wes PD, Vasilevko V et al. Blocking IL-1 signaling rescues cognition, attenuates tau pathology, and restores neuronal beta-catenin pathway function in an Alzheimer's disease model. J Immunol 2011; 187: 6539-6549.
36. Dugan LL, Ali SS, Shekhtman G, Roberts AJ, Lucero J, Quick KL et al. IL-6 mediated degeneration of forebrain GABAergic interneurons and cognitive impairment in aged mice through activation of neuronal NADPH oxidase. PLoS ONE 2009; 4: e5518.
37. Belarbi K, Jopson T, Tweedie D, Arellano C, Luo W, Greig NH et al. TNF-alpha protein synthesis inhibitor restores neuronal function and reverses cognitive deficits induced by chronic neuroinflammation. J Neuroinflammation 2012; 9: 23.
38. Klein T, Bischoff R. Physiology and pathophysiology of matrix metalloproteases. Amino Acids 2011; 41: 271-290.
39. Candelario-Jalil E, Thompson J, Taheri S, Grossetete M, Adair JC, Edmonds E et al. Matrix metalloproteinases are associated with increased blood-brain barrier opening in vascular cognitive impairment. Stroke 2011; 42: 1345-1350.
40. Hernandez-Guillamon M, Martinez-Saez E, Delgado P, Domingues-Montanari S, Boada C, Penalba A et al. MMP-2/MMP-9 plasma level and brain expression in cerebral amyloid angiopathy-associated hemorrhagic stroke. Brain Pathol 2011; 22: 133-141.