Loss of P2Y2 nucleotide receptors enhances early pathology in the TgCRND8 mouse model of Alzheimer's disease

Molecular Neurobiology

Volumn 49, Issue 2, 2014, Pages 1031-1042

  Ajit, Deepa ^a   Woods, Lucas T ^a   Camden, Jean M ^a   Thebeau, Christina N ^a   El Sayed, Farid G ^a   Greeson, Glen W ^a   Erb, Laurie ^a,b   Petris, Michael J ^a,b   Miller, Douglas C ^a   Sun, Grace Y ^a,b   Weisman, Gary A ^a,b  

^a University of Missouri   (United States)

^b UNIVERSITY OF MISSOURI   (United States)

Author keywords

Alzheimer's disease; A ; Microglia; TgCRND8 mouse

Indexed keywords

AMYLOID BETA PROTEIN; AMYLOID BETA PROTEIN[1-42]; AMYLOID PRECURSOR PROTEIN; CD11B ANTIGEN; PURINERGIC P2Y2 RECEPTOR; AMYLOID BETA-PROTEIN (1-42); PEPTIDE FRAGMENT;

ALZHEIMER DISEASE; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIGEN EXPRESSION; ARTICLE; BRAIN CORTEX; BRAIN REGION; CELL ACTIVATION; CONTROLLED STUDY; DISEASE COURSE; GENE DELETION; GENE MUTATION; HETEROZYGOTE; HIPPOCAMPUS; HOMOZYGOTE; MOUSE; NONHUMAN; PHENOTYPE; UPREGULATION; AMYLOID PLAQUE; ANIMAL; BRAIN; C3H MOUSE; C57BL MOUSE; DEFICIENCY; DISEASE MODEL; FEMALE; GENETICS; HUMAN; MALE; METABOLISM; PATHOLOGY; TRANSGENIC MOUSE;

ALZHEIMER DISEASE; AMYLOID BETA-PEPTIDES; ANIMALS; BRAIN; DISEASE MODELS, ANIMAL; DISEASE PROGRESSION; FEMALE; HUMANS; MALE; MICE; MICE, INBRED C3H; MICE, INBRED C57BL; MICE, TRANSGENIC; PEPTIDE FRAGMENTS; PLAQUE, AMYLOID; RECEPTORS, PURINERGIC P2Y2;

EID: 84896547142     PISSN: 08937648     EISSN: 15591182     Source Type: Journal    
DOI: 10.1007/s12035-013-8577-5     Document Type: Article

References (88)

1. Rivest S (2009) Regulation of innate immune responses in the brain. Nat Rev Immunol 9:429-439
2. Wyss-Coray T, Rogers J (2012) Inflammation in Alzheimer disease - a brief review of the basic science and clinical literature. Cold Spring Harb Perspect Med 2:a006346
3. Glezer I, Simard AR, Rivest S (2007) Neuroprotective role of the innate immune system by microglia. Neuroscience 147:867-883 (Pubitemid 47102534)
4. Griffiths M, Neal JW, Gasque P (2007) Innate immunity and protective neuroinflammation: new emphasis on the role of neuroimmune regulatory proteins. Int Rev Neurobiol 82:29-55
5. Rozemuller AJ, van Gool WA, Eikelenboom P (2005) The neuroinflammatory response in plaques and amyloid angiopathy in Alzheimer's disease: therapeutic implications. Curr Drug Targets CNS Neurol Disord 4:223-233 (Pubitemid 40754159)
6. McGeer EG, Klegeris A, McGeer PL (2005) Inflammation, the complement system and the diseases of aging. Neurobiol Aging 26(Suppl 1):94-97
7. Klegeris A,McGeer EG,McGeer PL (2007) Therapeutic approaches to inflammation in neurodegenerative disease. Curr Opin Neurol 20: 351-357 (Pubitemid 46743120)
8. 2 receptor interactions in neuroinflammation. Mol Neurobiol 46:96-113
9. Burnstock G (2012) Purinergic signalling: its unpopular beginning, its acceptance and its exciting future. Bioessays 34:218-225
10. Burnstock G (2007) Purine and pyrimidine receptors. Cell Mol Life Sci 64:1471-1483
11. Bodin P, Burnstock G (2001) Purinergic signalling: ATP release. Neurochem Res 26:959-969 (Pubitemid 33021422)
12. Butt AM (2011) ATP: a ubiquitous gliotransmitter integrating neuron-glial networks. Semin Cell Dev Biol 22:205-213
13. Ferrero ME (2012) Purinoceptors in inflammation: potential as anti-inflammatory therapeutic targets. Front Biosci 17:2172-2186
14. 2 receptors by UTP and ATP stimulates mitogen-activated kinase activity through a pathway that involves related adhesion focal tyrosine kinase and protein kinase C. J Biol Chem 273:2653-2660
15. Lustig KD, Sportiello MG, Erb L,Weisman GA (1992) A nucleotide receptor in vascular endothelial cells is specifically activated by the fully ionized forms of ATP and UTP. Biochem J 284(Pt 3):733-739
16. Erb L, Lustig KD, Sullivan DM, Turner JT, Weisman GA (1993) Functional expression and photoaffinity labeling of a cloned P2Upurinergic receptor. Proc Natl Acad Sci U S A 90:10449-10453 (Pubitemid 23347059)
17. Hussl S, Boehm S (2006) Functions of neuronal P2Y receptors. Pflugers Arch 452:538-551 (Pubitemid 44015089)
18. 2 nucleotide receptor-mediated responses in brain cells. Mol Neurobiol 41:356-366
19. 2receptor. Purinergic Signal 8:559-578
20. 2 nucleotide receptor mRNA expression is an immediate early gene response in activated thymocytes. Proc Natl Acad Sci U S A 94: 831-836
21. Turner JT, Weisman GA, Landon LA, Park M, Camden JM (1998) Salivary gland nucleotide receptors: evidence for functional expression of both P2X and P2Y subtypes. Eur J Morphol 36(Suppl):170-175
22. 2nucleotide receptors mediate uridine 5′-triphosphate-induced intimal hyperplasia in collared rabbit carotid arteries. Circulation 106:2720- 2726
23. 2 purinoceptor in intimal lesions of the rat aorta. Arterioscler Thromb Vasc Biol 17: 3602-3610
24. 2 receptor. J Neurochem 109:1300-1310
25. 2 receptor activation. J Neurochem 121:228-238
26. Erb L, Weisman GA (2012) Coupling of P2Y receptors to G proteins and other signaling pathways. WIREsMembr Transp Signal 1:789-803
27. Lee YJ, Han SB, Nam SY, Oh KW, Hong JT (2010) Inflammation and Alzheimer's disease. Arch Pharm Res 33:1539-1556
28. Cacabelos R, Alvarez XA, Franco-Maside A, Fernandez-Novoa L, Caamano J (1994) Serum tumor necrosis factor (TNF) in Alzheimer's disease and multi-infarct dementia. Methods Find Exp Clin Pharmacol 16:29-35 (Pubitemid 24067673)
29. BurgosM, Neary JT, Gonzalez FA (2007) P2Y2 nucleotide receptors inhibit trauma-induced death of astrocytic cells. J Neurochem 103: 1785-1800 (Pubitemid 350126610)
30. Lai MK, Tan MG, Kirvell S, Hobbs C, Lee J, Esiri MM, Chen CP, Francis PT (2008) Selective loss of P2Y2 nucleotide receptor immunoreactivity is associated with Alzheimer's disease neuropathology. J Neural Transm 115:1165-1172
31. Chishti MA, Yang DS, Janus C, Phinney AL, Horne P, Pearson J, Strome R, Zuker N, Loukides J, French J, Turner S, Lozza G, Grilli M, Kunicki S, Morissette C, Paquette J, Gervais F, Bergeron C, Fraser PE, Carlson GA, George-Hyslop PS, Westaway D (2001) Early-onset amyloid deposition and cognitive deficits in transgenic mice expressing a double mutant form of amyloid precursor protein 695. J Biol Chem 276:21562-21570 (Pubitemid 37413154)
32. v integrin mediates astrocyte migration. J Neurochem 95:630-640
33. DaSilva K, Brown ME, Westaway D, McLaurin J (2006) Immunization with amyloid-beta using GM-CSF and IL-4 reduces amyloid burden and alters plaque morphology. Neurobiol Dis 23: 433-444 (Pubitemid 44080847)
34. 2nucleotide receptors in rat salivary gland cells during short-term culture. Am J Physiol 273:C1100-C1107
35. Ma K,Mount HT,McLaurin J (2011) Region-specific distribution of beta-amyloid peptide and cytokine expression in TgCRND8 mice. Neurosci Lett 492:5-10
36. 2 nucleotide receptors enhance α- secretase-dependent amyloid precursor protein processing. J Biol Chem 280:18696-18702
37. Slack BE, Ma LK, Seah CC (2001) Constitutive shedding of the amyloid precursor protein ectodomain is up-regulated by tumour necrosis factor-alpha converting enzyme. Biochem J 357:787-794 (Pubitemid 32735158)
38. Jorissen E, Prox J, Bernreuther C, Weber S, Schwanbeck R, Serneels L, Snellinx A, Craessaerts K, Thathiah A, Tesseur I, Bartsch U, Weskamp G, Blobel CP, Glatzel M, De Strooper B, Saftig P (2010) The disintegrin/metalloproteinase ADAM10 is essential for the establishment of the brain cortex. J Neurosci 30:4833-4844
39. Caccamo A, Oddo S, Billings LM, Green KN, Martinez-Coria H, Fisher A, LaFerla FM (2006) M1 receptors play a central role in modulating AD-like pathology in transgenic mice. Neuron 49:671-682 (Pubitemid 43290127)
40. Donmez G, Wang D, Cohen DE, Guarente L (2010) SIRT1 suppresses β-amyloid production by activating the α-secretase gene ADAM10. Cell 142:320-332
41. Vassar R, Bennett BD, Babu-Khan S, Kahn S, Mendiaz EA, Denis P, Teplow DB, Ross S, Amarante P, Loeloff R, Luo Y, Fisher S, Fuller J, Edenson S, Lile J, Jarosinski MA, Biere AL, Curran E, Burgess T, Louis JC, Collins F, Treanor J, Rogers G, Citron M (1999) Beta-secretase cleavage of Alzheimer's amyloid precursor protein by the transmembrane aspartic protease BACE. Science 286:735-741
42. Vassar R, Kovacs DM, Yan R, Wong PC (2009) The beta-secretase enzyme BACE in health and Alzheimer's disease: regulation, cell biology, function, and therapeutic potential. J Neurosci 29:12787-12794
43. Yang LB, Lindholm K, Yan R, Citron M, Xia W, Yang XL, Beach T, Sue L, Wong P, Price D, Li R, Shen Y (2003) Elevated beta-secretase expression and enzymatic activity detected in sporadic Alzheimer disease. Nat Med 9:3-4 (Pubitemid 36098241)
44. Li R, Lindholm K, Yang LB, Yue X, Citron M, Yan R, Beach T, Sue L, Sabbagh M, Cai H, Wong P, Price D, Shen Y (2004) Amyloid beta peptide load is correlated with increased beta-secretase activity in sporadic Alzheimer's disease patients. Proc Natl Acad Sci U S A 101: 3632-3637 (Pubitemid 38338246)
45. Weitz TM, Town T (2012) Microglia in Alzheimer's disease: it's all about context. Int J Alzheimers Dis 2012:314185
46. Akiyama H, McGeer PL (1990) Brain microglia constitutively express beta-2 integrins. J Neuroimmunol 30:81-93 (Pubitemid 20324759)
47. Le Cabec V, Carreno S, Moisand A, Bordier C, Maridonneau-Parini I (2002) Complement receptor 3 (CD11b/CD18) mediates type I and type II phagocytosis during nonopsonic and opsonic phagocytosis, respectively. J Immunol 169:2003-2009 (Pubitemid 34857664)
48. Lalonde R, Strazielle C (2011) Brain regions and genes affecting limb-clasping responses. Brain Res Rev 67:252-259
49. Carter RJ, Lione LA, Humby T, Mangiarini L, Mahal A, Bates GP, Dunnett SB, Morton AJ (1999) Characterization of progressive motor deficits in mice transgenic for the human Huntington's disease mutation. J Neurosci 19:3248-3257 (Pubitemid 29174016)
50. Hetze S, Romer C, Teufelhart C, Meisel A, Engel O (2012) Gait analysis as a method for assessing neurological outcome in a mouse model of stroke. J Neurosci Methods 206:7-14
51. Neumann M, Wang Y, Kim S, Hong SM, Jeng L, Bilgen M, Liu J (2009) Assessing gait impairment following experimental traumatic brain injury in mice. J Neurosci Methods 176:34-44
52. 2 nucleotide receptor up-regulation in submandibular gland cells from the NOD.B10 mouse model of Sjogren's syndrome. Arch Oral Biol 50: 533-540
53. 2 receptor transcription is increased by NF-κB and stimulates cyclooxygenase- 2 expression and PGE2 release by intestinal epithelial cells. J Immunol 183:4521-4529
54. Tharp WG, Lee YH, Greene SM, Vincellete E, Beach TG, Pratley RE (2012) Measurement of altered AbetaPP isoform expression in frontal cortex of patients with Alzheimer's disease by absolute quantification real-time PCR. J Alzheimers Dis 29:449-457
55. Schmidt ML, DiDario AG, Lee VM, Trojanowski JQ (1994) An extensive network of PHF tau-rich dystrophic neurites permeates neocortex and nearly all neuritic and diffuse amyloid plaques in Alzheimer disease. FEBS Lett 344:69-73 (Pubitemid 2083206)
56. Selkoe DJ (1989) The deposition of amyloid proteins in the aging mammalian brain: implications for Alzheimer's disease.Ann Med 21: 73-76
57. Woodhouse A, Vickers JC, Adlard PA, Dickson TC (2009) Dystrophic neurites in TgCRND8 and Tg2576 mice mimic human pathological brain aging. Neurobiol Aging 30:864-874
58. Cummings BJ, Su JH, Geddes JW, Van Nostrand WE, Wagner SL, Cunningham DD, Cotman CW (1992) Aggregation of the amyloid precursor protein within degenerating neurons and dystrophic neurites in Alzheimer's disease. Neuroscience 48:763-777
59. Lue LF, Kuo YM, Roher AE, Brachova L, Shen Y, Sue L, Beach T, Kurth JH, Rydel RE, Rogers J (1999) Soluble amyloid beta peptide concentration as a predictor of synaptic change in Alzheimer's disease. Am J Pathol 155:853-862 (Pubitemid 29426831)
60. McLean CA, Cherny RA, Fraser FW, Fuller SJ, Smith MJ, Beyreuther K, Bush AI, Masters CL (1999) Soluble pool of Abeta amyloid as a determinant of severity of neurodegeneration in Alzheimer's disease. Ann Neurol 46:860-866
61. Sisodia SS (1992) Beta-amyloid precursor protein cleavage by a membrane-bound protease. Proc Natl Acad Sci U S A 89:6075-6079
62. Roberts SB, Ripellino JA, Ingalls KM, Robakis NK, Felsenstein KM (1994) Non-amyloidogenic cleavage of the beta-amyloid precursor protein by an integral membrane metalloendopeptidase. J Biol Chem 269:3111-3116
63. O'Brien RJ, Wong PC (2011) Amyloid precursor protein processing and Alzheimer's disease. Annu Rev Neurosci 34:185-204
64. Skovronsky DM, Moore DB, Milla ME, Doms RW, Lee VM (2000) Protein kinase C-dependent alpha-secretase competes with beta-secretase for cleavage of amyloid-beta precursor protein in the trans-golgi network. J Biol Chem 275:2568-2575 (Pubitemid 30082022)
65. Lichtenthaler SF (2012) Alpha-secretase cleavage of the amyloid precursor protein: proteolysis regulated by signaling pathways and protein trafficking. Curr Alzheimer Res 9:165-177
66. Bolmont T, Haiss F, Eicke D, Radde R, Mathis CA, Klunk WE, Kohsaka S, Jucker M, Calhoun ME (2008) Dynamics of the microglial/amyloid interaction indicate a role in plaque maintenance. J Neurosci 28:4283-4292
67. Simard AR, Soulet D, Gowing G, Julien JP, Rivest S (2006) Bone marrow-derived microglia play a critical role in restricting senile plaque formation in Alzheimer's disease. Neuron 49:489-502 (Pubitemid 43221886)
68. Hao W, Liu Y, Liu S, Walter S, Grimm MO, Kiliaan AJ, Penke B, Hartmann T, Rube CE, Menger MD, Fassbender K (2011) Myeloid differentiation factor 88-deficient bone marrow cells improve Alzheimer's disease-related symptoms and pathology. Brain 134: 278-292
69. Shie FS, Breyer RM, Montine TJ (2005) Microglia lacking E prostanoid receptor subtype 2 have enhanced Abeta phagocytosis yet lack Abeta-activated neurotoxicity. Am J Pathol 166:1163-1172 (Pubitemid 40524440)
70. Jiang Q, Lee CY, Mandrekar S, Wilkinson B, Cramer P, Zelcer N, Mann K, Lamb B, Willson TM, Collins JL, Richardson JC, Smith JD, Comery TA, Riddell D, Holtzman DM, Tontonoz P, Landreth GE (2008) ApoE promotes the proteolytic degradation of Abeta. Neuron 58:681-693 (Pubitemid 351778466)
71. Nicoll JA,Wilkinson D, Holmes C, Steart P, Markham H, Weller RO (2003) Neuropathology of human Alzheimer disease after immunization with amyloid-beta peptide: a case report. Nat Med 9: 448-452 (Pubitemid 36460079)
72. Boche D, Denham N, Holmes C, Nicoll JA (2010) Neuropathology after active Abeta42 immunotherapy: implications for Alzheimer's disease pathogenesis. Acta Neuropathol 120:369-384
73. Schenk D, Barbour R, Dunn W, Gordon G, Grajeda H, Guido T, Hu K, Huang J, Johnson-Wood K, Khan K, Kholodenko D, Lee M, Liao Z, Lieberburg I, Motter R, Mutter L, Soriano F, Shopp G, Vasquez N, Vandevert C, Walker S, Wogulis M, Yednock T, Games D, Seubert P (1999) Immunization with amyloid-beta attenuates Alzheimer-disease- like pathology in the PDAPP mouse. Nature 400:173-177 (Pubitemid 29327547)
74. El Khoury J, Toft M, Hickman SE, Means TK, Terada K, Geula C, Luster AD (2007) Ccr2 deficiency impairs microglial accumulation and accelerates progression of Alzheimer-like disease. Nat Med 13: 432-438 (Pubitemid 46559828)
75. Shaftel SS, Kyrkanides S, Olschowka JA, Miller JN, Johnson RE, O'Banion MK (2007) Sustained hippocampal IL-1 beta overexpression mediates chronic neuroinflammation and ameliorates Alzheimer plaque pathology. J Clin Invest 117:1595-1604 (Pubitemid 46871344)
76. o-mediated signal transduction. J Cell Biol 153:491-501
77. o and induce cell migration. J Biol Chem 280:39050-39057
78. 12. J Cell Sci 120:1654-1662
79. Knauer MF, Soreghan B, Burdick D, Kosmoski J, Glabe CG (1992) Intracellular accumulation and resistance to degradation of the Alzheimer amyloid A4/beta protein. Proc Natl Acad Sci U S A 89: 7437-7441
80. Bamberger ME, Harris ME, McDonald DR, Husemann J, Landreth GE (2003) A cell surface receptor complex for fibrillar beta-amyloid mediates microglial activation. J Neurosci 23:2665-2674 (Pubitemid 36418601)
81. Koenigsknecht J, Landreth G (2004) Microglial phagocytosis of fibrillar beta-amyloid through a β1 integrin-dependent mechanism. J Neurosci 24:9838-9846 (Pubitemid 39463564)
82. Mangiarini L, Sathasivam K, Seller M, Cozens B, Harper A, Hetherington C, Lawton M, Trottier Y, Lehrach H, Davies SW, Bates GP (1996) Exon 1 of the HD gene with an expanded CAG repeat is sufficient to cause a progressive neurological phenotype in transgenic mice. Cell 87:493-506 (Pubitemid 26374323)
83. Komatsu M,Waguri S, Chiba T,Murata S, Iwata J, Tanida I, Ueno T, Koike M, Uchiyama Y, Kominami E, Tanaka K (2006) Loss of autophagy in the central nervous system causes neurodegeneration in mice. Nature 441:880-884
84. Maquet D, Lekeu F, Warzee E, Gillain S, Wojtasik V, Salmon E, Petermans J, Croisier JL (2010) Gait analysis in elderly adult patients with mild cognitive impairment and patients with mild Alzheimer's disease: simple versus dual task: a preliminary report. Clin Physiol Funct Imaging 30:51-56
85. 2 receptor activates nerve growth factor/TrkA signaling to enhance neuronal differentiation. Proc Natl Acad Sci U S A 102:19138-19143
86. 2 nucleotide receptor mediate neurite extension in IL-1β-treated mouse primary cortical neurons. J Neurochem 125:885-896
87. Yang CN, Shiao YJ, Shie FS, Guo BS, Chen PH, Cho CY, Chen YJ, Huang FL, Tsay HJ (2011) Mechanism mediating oligomeric Abeta clearance by naive primary microglia. Neurobiol Dis 42:221-230
88. Kukulski F, Ben Yebdri F, Bahrami F, Fausther M, Tremblay A, Sevigny J (2010) Endothelial P2Y2 receptor regulates LPS-induced neutrophil transendothelial migration in vitro. Mol Immunol 47, 991-999