Neurobiology of Aging
Volume 30, Issue 11 , Pages 1792-1804 , November 2009

Aβ peptide conformation determines uptake and interleukin-1α expression by primary microglial cells

  • Saravanapavan Parvathy

      Affiliations

    • These authors contributed equally to this work.
  • ,
  • Jayakumar Rajadas

      Affiliations

    • These authors contributed equally to this work.
  • ,
  • Heather Ryan
  • ,
  • Sepideh Vaziri
  • ,
  • Laurel Anderson
  • ,
  • Greer M. Murphy Jr.

      Affiliations

    • Corresponding Author InformationCorresponding author at: Neuroscience Research Laboratories, Department of Psychiatry and Behavioral Sciences, Stanford University School of Medicine, Medical School Lab Surge Building, 1201 Welch Road, Stanford, CA 94305-5485, United States. Tel.: +1 650 725 0565; fax: +1 650 498 7761.

Received 25 September 2007 ,Revised 8 January 2008 ,Accepted 18 January 2008.

References 

  1. Akama KT, Van Eldik LJ. β-Amyloid stimulation of inducible nitric-oxide synthase in astrocytes is interleukin-1 beta- and tumor necrosis factor-alpha (TNF alpha)-dependent, and involves a TNF alpha receptor-associated factor- and NF kappa B-inducing kinase-dependent signaling mechanism. J. Biol. Chem. 2000;275(11):7918–7924
  2. Akiyama H, Barger S, Barnum S, Bradt B, Bauer J, Cole GM, et al. Inflammation and Alzheimer's disease. Neurobiol. Aging. 2000;21(3):383–421
  3. Araujo DM, Cotman CW. Beta-amyloid stimulates glial cells in vitro to produce growth factors that accumulate in senile plaques in Alzheimer's disease.. Brain Res. 1992;569(1):141–145
  4. Bamberger ME, Harris ME, McDonald DR, Husemann J, Landreth GE. A cell surface receptor complex for fibrillar beta-amyloid mediates microglial activation. J. Neurosci. 2003;23(7):2665–2674
  5. Bard F, Cannon C, Barbour R, Burke RL, Games D, Grajeda H, et al. Peripherally administered antibodies against amyloid beta-peptide enter the central nervous system and reduce pathology in a mouse model of Alzheimer disease. Nat. Med. 2000;6(8):916–919
  6. Bitan G, Vollers SS, Teplow DB. Elucidation of primary structure elements controlling early amyloid beta-protein oligomerization. J. Biol. Chem. 2003;278(37):34882–34889
  7. Bottenstein JE, Sato GH. Growth of a rat neuroblastoma cell line in serum-free supplemented medium. Proc. Natl. Acad. Sci. U.S.A. 1979;76(1):514–517
  8. Chao CC, Hu S, Molitor TW, Shaskan EG, Peterson PK. Activated microglia mediate neuronal cell injury via a nitric oxide mechanism. J. Immunol. 1992;149(8):2736–2741
  9. Chauhan NB. Intracerebroventricular passive immunization with anti-oligoAbeta antibody in TgCRND8. J. Neurosci. Res. 2007;85(2):451–463
  10. Chromy BA, Nowak RJ, Lambert MP, Viola KL, Chang L, Velasco PT, et al. Self-assembly of Abeta(1–42) into globular neurotoxins. Biochemistry. 2003;42(44):12749–12760
  11. Cleary JP, Walsh DM, Hofmeister JJ, Shankar GM, Kuskowski MA, Selkoe DJ, et al. Natural oligomers of the amyloid-beta protein specifically disrupt cognitive function. Nat. Neurosci. 2005;8(1):79–84
  12. Coria F, Moreno A, Rubio I, Garcia MA, Morato E, Mayor F. The cellular pathology associated with Alzheimer beta-amyloid deposits in non-demented aged individuals. Neuropathol. Appl. Neurobiol. 1993;19(3):261–268
  13. Dahlgren KN, Manelli AM, Stine WB, Baker LK, Krafft GA, LaDu MJ. Oligomeric and fibrillar species of amyloid-beta peptides differentially affect neuronal viability. J. Biol. Chem. 2002;277(35):32046–32053
  14. Dodart JC, Bales KR, Gannon KS, Greene SJ, DeMattos RB, Mathis C, et al. Immunization reverses memory deficits without reducing brain Abeta burden in Alzheimer's disease model. Nat. Neurosci. 2002;5(5):452–457
  15. Fetler L, Amigorena S. Neuroscience. Brain under surveillance: the microglia patrol. Science. 2005;309(5733):392–393
  16. Findeis MA, Molineaux SM. Design and testing of inhibitors of fibril formation. Methods Enzymol. 1999;309:476–488
  17. Giulian D, Baker TJ. Characterization of ameboid microglia isolated from developing mammalian brain. J. Neurosci. 1986;6(8):2163–2178
  18. Giulian D, Ingeman JE. Colony-stimulating factors as promoters of ameboid microglia. J. Neurosci. 1988;8(12):4707–4717
  19. Glabe CG. Common mechanisms of amyloid oligomer pathogenesis in degenerative disease. Neurobiol. Aging. 2006;27(4):570–575
  20. Goldgaber D, Harris HW, Hla T, Maciag T, Donnelly RJ, Jacobsen JS, et al. Interleukin 1 regulates synthesis of amyloid beta-protein precursor mRNA in human endothelial cells. Proc. Natl. Acad. Sci. U.S.A. 1989;86(19):7606–7610
  21. Goldsbury C, Frey P, Olivieri V, Aebi U, Muller SA. Multiple assembly pathways underlie amyloid-beta fibril polymorphisms. J. Mol. Biol. 2005;352(2):282–298
  22. Greenfield NJ. Using circular dichroism spectra to estimate protein secondary structure. Nat. Protoc. 2006;1(6):2876–2890
  23. Griffin WS, Stanley LC, Ling C, White L, MacLeod V, Perrot LJ, et al. Brain interleukin 1 and S-100 immunoreactivity are elevated in Down syndrome and Alzheimer disease. Proc. Natl. Acad. Sci. U.S.A. 1989;86(19):7611–7615
  24. Griffin WS, Sheng JG, Roberts GW, Mrak RE. Interleukin-1 expression in different plaque types in Alzheimer's disease: significance in plaque evolution. J. Neuropathol. Exp. Neurol. 1995;54(2):276–281
  25. Haass C, Selkoe DJ. Soluble protein oligomers in neurodegeneration: lessons from the Alzheimer's amyloid beta-peptide. Nat. Rev. Mol. Cell Biol. 2007;8(2):101–112
  26. Harper JD, Wong SS, Lieber CM, Lansbury PT. Assembly of A beta amyloid protofibrils: an in vitro model for a possible early event in Alzheimer's disease. Biochemistry. 1999;38(28):8972–8980
  27. Hartley DM, Walsh DM, Ye CP, Diehl T, Vasquez S, Vassilev PM, et al. Protofibrillar intermediates of amyloid beta-protein induce acute electrophysiological changes and progressive neurotoxicity in cortical neurons. J. Neurosci. 1999;19(20):8876–8884
  28. Hennessey JP, Johnson WC. Information content in the circular dichroism of proteins. Biochemistry. 1981;20(5):1085–1094
  29. Johansson AS, Berglind-Dehlin F, Karlsson G, Edwards K, Gellerfors P, Lannfelt L. Physiochemical characterization of the Alzheimer's disease-related peptides A beta 1–42Arctic and A beta 1-42wt. FEBS J. 2006;273(12):2618–2630
  30. Kayed R, Head E, Thompson JL, McIntire TM, Milton SC, Cotman CW, et al. Common structure of soluble amyloid oligomers implies common mechanism of pathogenesis. Science. 2003;300(5618):486–489
  31. Klyubin I, Walsh DM, Lemere CA, Cullen WK, Shankar GM, Betts V, et al. Amyloid beta protein immunotherapy neutralizes Abeta oligomers that disrupt synaptic plasticity in vivo. Nat. Med. 2005;11(5):556–561
  32. Kreutzberg GW. Microglia: a sensor for pathological events in the CNS. Trends Neurosci. 1996;19(8):312–318
  33. Kuo YM, Emmerling MR, Vigo-Pelfrey C, Kasunic TC, Kirkpatrick JB, Murdoch GH, et al. Water-soluble Abeta (N-40, N-42) oligomers in normal and Alzheimer disease brains. J. Biol. Chem. 1996;271(8):4077–4081
  34. Lai AY, Todd KG. Hypoxia-activated microglial mediators of neuronal survival are differentially regulated by tetracyclines. Glia. 2006;53(8):809–816
  35. Lambert MP, Barlow AK, Chromy BA, Edwards C, Freed R, Liosatos M, et al. Diffusible, nonfibrillar ligands derived from Abeta1–42 are potent central nervous system neurotoxins. Proc. Natl. Acad. Sci. U.S.A. 1998;95(11):6448–6453
  36. Lindberg C, Selenica ML, Westlind-Danielsson A, Schultzberg M. Beta-amyloid protein structure determines the nature of cytokine release from rat microglia. J. Mol. Neurosci. 2005;27(1):1–12
  37. Luber-Narod J, Rogers J. Immune system associated antigens expressed by cells of the human central nervous system. Neurosci. Lett. 1988;94(1–2):17–22
  38. Lue LF, Rydel R, Brigham EF, Yang LB, Hampel H, Murphy GM, et al. Inflammatory repertoire of Alzheimer's disease and nondemented elderly microglia in vitro. Glia. 2001;35(1):72–79
  39. McGeer PL, McGeer EG. Mechanisms of cell death in Alzheimer disease—immunopathology. J. Neural Transm. Suppl. 1998;54:159–166
  40. McLean CA, Cherny RA, Fraser FW, Fuller SJ, Smith MJ, Beyreuther K, et al. Soluble pool of Abeta amyloid as a determinant of severity of neurodegeneration in Alzheimer's disease. Ann. Neurol. 1999;46(6):860–866
  41. Meda L, Baron P, Prat E, Scarpini E, Scarlato G, Cassatella MA, et al. Proinflammatory profile of cytokine production by human monocytes and murine microglia stimulated with beta-amyloid [25–35]. J. Neuroimmunol. 1999;93(1-2):45–52
  42. Mitrasinovic OM, Murphy GM. Accelerated phagocytosis of amyloid-beta by mouse and human microglia overexpressing the macrophage colony-stimulating factor receptor. J. Biol. Chem. 2002;277(33):29889–29896
  43. Mitrasinovic OM, Grattan A, Robinson CC, Lapustea NB, Poon C, Ryan H, et al. Microglia overexpressing the macrophage colony-stimulating factor receptor are neuroprotective in a microglial-hippocampal organotypic coculture system. J. Neurosci. 2005;25(17):4442–4451
  44. Mrak RE, Griffin WS. Glia and their cytokines in progression of neurodegeneration. Neurobiol. Aging. 2005;26(3):349–354
  45. Necula M, Kayed R, Milton S, Glabe CG. Small molecule inhibitors of aggregation indicate that amyloid beta oligomerization and fibrillization pathways are independent and distinct. J. Biol. Chem. 2007;282(14):10311–10324
  46. Nicoll JA, Barton E, Boche D, Neal JW, Ferrer I, Thompson P, et al. Abeta species removal after abeta42 immunization. J. Neuropathol. Exp. Neurol. 2006;65(11):1040–1048
  47. Nimmerjahn A, Kirchhoff F, Helmchen F. Resting microglial cells are highly dynamic surveillants of brain parenchyma in vivo. Science. 2005;308(5726):1314–1318
  48. Nybo M, Svehag SE, Holm Nielsen E. An ultrastructural study of amyloid intermediates in A beta1–42 fibrillogenesis. Scand. J. Immunol. 1999;49(3):219–223
  49. Rabchevsky AG, Streit WJ. Grafting of cultured microglial cells into the lesioned spinal cord of adult rats enhances neurite outgrowth. J. Neurosci. Res. 1997;47(1):34–48
  50. Sasaki A, Yamaguchi H, Ogawa A, Sugihara S, Nakazato Y. Microglial activation in early stages of amyloid beta protein deposition. Acta Neuropathol. (Berl.). 1997;94(4):316–322
  51. Saura J, Tusell JM, Serratosa J. High-yield isolation of murine microglia by mild trypsinization. Glia. 2003;44(3):183–189
  52. Shankar GM, Bloodgood BL, Townsend M, Walsh DM, Selkoe DJ, Sabatini BL. Natural oligomers of the Alzheimer amyloid-beta protein induce reversible synapse loss by modulating an NMDA-type glutamate receptor-dependent signaling pathway. J. Neurosci. 2007;27(11):2866–2875
  53. Stine WB, Dahlgren KN, Krafft GA, LaDu MJ. In vitro characterization of conditions for amyloid-beta peptide oligomerization and fibrillogenesis. J. Biol. Chem. 2003;278(13):11612–11622
  54. Verdier Y, Zarandi M, Penke B. Amyloid beta-peptide interactions with neuronal and glial cell plasma membrane: binding sites and implications for Alzheimer's disease. J. Pept. Sci. 2004;10(5):229–248
  55. Walsh DM, Lomakin A, Benedek GB, Condron MM, Teplow DB. Amyloid beta-protein fibrillogenesis. Detection of a protofibrillar intermediate. J. Biol. Chem. 1997;272(35):22364–22372
  56. Walsh DM, Hartley DM, Kusumoto Y, Fezoui Y, Condron MM, Lomakin A, et al. Amyloid beta-protein fibrillogenesis. Structure and biological activity of protofibrillar intermediates. J. Biol. Chem. 1999;274(36):25945–25952
  57. Walsh DM, Klyubin I, Fadeeva JV, Cullen WK, Anwyl R, Wolfe MS, et al. Naturally secreted oligomers of amyloid beta protein potently inhibit hippocampal long-term potentiation in vivo. Nature. 2002;416(6880):535–539
  58. Ward RV, Jennings KH, Jepras R, Neville W, Owen DE, Hawkins J, et al. Fractionation and characterization of oligomeric, protofibrillar and fibrillar forms of beta-amyloid peptide. Biochem. J. 2000;348(Pt1):137–144
  59. White JA, Manelli AM, Holmberg KH, Van Eldik LJ, Ladu MJ. Differential effects of oligomeric and fibrillar amyloid-beta 1–42 on astrocyte-mediated inflammation. Neurobiol. Dis. 2005;18(3):459–465
  60. Yan SD, Chen X, Fu J, Chen M, Zhu HJ, Roher A, et al. RAGE and amyloid-beta peptide neurotoxicity in Alzheimer's disease. Nature. 1996;382(6593):685–691
  61. Yates SL, Burgess LH, Kocsis-Angle J, Antal JM, Dority MD, Embury PB, et al. Amyloid beta and amylin fibrils induce increases in proinflammatory cytokine and chemokine production by THP-1 cells and murine microglia. J. Neurochem. 2000;74(3):1017–1025

PII: S0197-4580(08)00027-4

doi: 10.1016/j.neurobiolaging.2008.01.011

Neurobiology of Aging
Volume 30, Issue 11 , Pages 1792-1804 , November 2009