Amyloid-β peptide protects against microbial infection in mouse and worm models of Alzheimer's disease

Science Translational Medicine

Volumn 8, Issue 340, 2016, Pages

  Kumar, Deepak Kumar Vijaya ^a   Choi, Hoon Se ^a   Washicosky, Kevin J ^a   Eimer, William A ^a   Tucker, Stephanie ^a   Ghofrani, Jessica ^a   Lefkowitz, Aaron ^a   McColl, Gawain ^b   Goldstein, Lee E ^c   Tanzi, Rudolph E ^a   Moir, Robert D ^a  

^a MASSACHUSETTS GENERAL HOSPITAL   (United States)

^b UNIVERSITY OF MELBOURNE   (Australia)

^c BOSTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AMYLOID BETA PROTEIN; CARBOHYDRATE; HEPARIN BINDING PROTEIN;

5XFAD MOUSE; ALZHEIMER DISEASE; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIMICROBIAL ACTIVITY; ARTICLE; BACTERIAL CELL WALL; BACTERIAL INFECTION; BRAIN INFECTION; CAENORHABDITIS ELEGANS; CANDIDA ALBICANS; CELL ADHESION; CELL AGGLUTINATION; CONTROLLED STUDY; FEMALE; FUNGAL CELL WALL; HOST CELL; HUMAN; HUMAN CELL; IN VIVO STUDY; MAMMAL CELL; MOUSE; MYCOSIS; NEMATODE; NONHUMAN; OLIGOMERIZATION; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; SALMONELLA ENTERICA SEROVAR TYPHIMURIUM; WORM; ANIMAL; DISEASE MODEL; GENETICS; INNATE IMMUNITY; METABOLISM; MICROBIOLOGY; PATHOGENICITY; PHYSIOLOGY; TRANSGENIC ANIMAL; TRANSGENIC MOUSE;

ALZHEIMER DISEASE; AMYLOID BETA-PEPTIDES; ANIMALS; ANIMALS, GENETICALLY MODIFIED; CAENORHABDITIS ELEGANS; DISEASE MODELS, ANIMAL; FEMALE; HUMANS; IMMUNITY, INNATE; MICE; MICE, TRANSGENIC; SALMONELLA TYPHIMURIUM;

EID: 84970948063     PISSN: 19466234     EISSN: 19466242     Source Type: Journal    
DOI: 10.1126/scitranslmed.aaf1059     Document Type: Article

References (73)

1. R. E. Tanzi, L. Bertram, Twenty years of the Alzheimer's disease amyloid hypothesis: A genetic perspective. Cell 120, 545-555 (2005).
2. S. Luna, D. J. Cameron, D. W. Ethell, Amyloid-b and APP deficiencies cause severe cerebrovascular defects: Important work for an old villain. PLOS One 8, e75052 (2013).
3. S. J. Soscia, J. E. Kirby, K. J. Washicosky, S. M. Tucker, M. Ingelsson, B. Hyman, M. A. Burton, L. E. Goldstein, S. Duong, R. E. Tanzi, R. D. Moir, The Alzheimer's disease-associated amyloid b-protein is an antimicrobial peptide. PLOS One 5, e9505 (2010).
4. B. L. Kagan, H. Jang, R. Capone, F. Teran Arce, S. Ramachandran, R. Lal, R. Nussinov, Antimicrobial properties of amyloid peptides. Mol. Pharm. 9, 708-717 (2012).
5. J. Wiesner, A. Vilcinskas, Antimicrobial peptides: The ancient arm of the human immune system. Virulence 1, 440-464 (2010).
6. Y. Yamaguchi, T. Nagase, T. Tomita, K. Nakamura, S. Fukuhara, T. Amano, H. Yamamoto, Y. Ide, M. Suzuki, S. Teramoto, T. Asano, K. Kangawa, N. Nakagata, Y. Ouchi, H. Kurihara, b-Defensin overexpression induces progressive muscle degeneration in mice. Am. J. Physiol. Cell Physiol.292, C2141-C2149 (2007).
7. M. Reinholz, T. Ruzicka, J. Schauber, Cathelicidin LL-37: An antimicrobial peptide with a role in inflammatory skin disease. Ann. Dermatol. 24, 126-135 (2012).
8. Y. Cao, S. Chtarbanova, A. J. Petersen, B. Ganetzky, Dnr1 mutations cause neurodegeneration in Drosophila by activating the innate immune response in the brain. Proc. Natl. Acad. Sci.U.S.A. 110, E1752-E1760 (2013).
9. A. Krause, C. Liepke, M. Meyer, K. Adermann, W. G. Forssmann, E. Maronde, Human natriuretic peptides exhibit antimicrobial activity. Eur. J. Med. Res. 6, 215-218 (2001).
10. M. R. White, R. Kandel, S. Tripathi, D. Condon, L. Qi, J. Taubenberger, K. L. Hartshorn, Alzheimer's associated b-amyloid protein inhibits influenza A virus and modulates viral interactions with phagocytes. PLOS One 9, e101364 (2014).
11. K. Bourgade, H. Garneau, G. Giroux, A. Y. Le Page, C. Bocti, G. Dupuis, E. H. Frost, T. Fülöp Jr., b-Amyloid peptides display protective activity against the human Alzheimer's disease-associated herpes simplex virus-1. Biogerontology 16, 85-98 (2015).
12. H. Oakley, S. L. Cole, S. Logan, E.Maus, P. Shao, J. Craft, A. Guillozet-Bongaarts, M. Ohno, J. Disterhoft, L. Van Eldik, R. Berry, R. Vassar, Intraneuronal b-amyloid aggregates, neurodegeneration, and neuron loss in transgenic mice with five familial Alzheimer's disease mutations: Potential factors in amyloid plaque formation. J. Neurosci. 26, 10129-10140 (2006).
13. H. Zheng, M. Jiang, M. E. Trumbauer, R. Hopkins, D. J. S. Sirinathsinghji, K. A. Stevens, M. W. Conner, H. H. Slunt, S. S. Sisodia, H. Y. Chen, L. H. T. Van der Ploeg, Mice deficient for the amyloid precursor protein gene. Ann. N.Y. Acad. Sci. 777, 421-426 (1996).
14. G. McColl, B. R. Roberts, T. L. Pukala, V. B. Kenche, C. M. Roberts, C. D. Link, T. M. Ryan, C. L. Masters, K. J. Barnham, A. I. Bush, R. A. Cherny, Utility of an improved model of amyloid-beta (Ab1-42) toxicity in Caenorhabditis elegans for drug screening for Alzheimer's disease. Mol. Neurodegener.7, 57 (2012).
15. J. P. Ardizzi, H. F. Epstein, Immunochemical localization of myosin heavy chain isoforms and paramyosin in developmentally and structurally diverse muscle cell types of the nematode Caenorhabditis elegans. J. Cell Biol. 105, 2763-2770 (1987).
16. C. I. Nussbaum-Krammer, K.-W. Park, L. Li, R. Melki, R. I. Morimoto, Spreading of a prion domain from cell-to-cell by vesicular transport in Caenorhabditis elegans. PLOS Genet. 9, e1003351 (2013).
17. D. Pisa, R. Alonso, A. Rábano, I. Rodal, L. Carrasco, Different brain regions are infected with fungi in Alzheimer's disease. Sci. Rep. 5, 15015 (2015).
18. R. Alonso, D. Pisa, A. I. Marina, E. Morato, A. Rábano, L. Carrasco, Fungal infection in patients with Alzheimer's disease. J. Alzheimers Dis. 41, 301-311 (2014).
19. P. A. Lewis, S. Piper, M. Baker, L. Onstead, M. P. Murphy, J. Hardy, R. Wang, E. McGowan, T. E. Golde, Expression of BRI-amyloid b peptide fusion proteins: A novel method for specific high-level expression of amyloid b peptides. Biochim. Biophys. Acta 1537, 58-62 (2001).
20. S. Hahn, T. Brüning, J. Ness, E. Czirr, S. Baches, H. Gijsen, C. Korth, C. U. Pietrzik, B. Bulic, S. Weggen, Presenilin-1 but not amyloid precursor protein mutations present in mouse models of Alzheimer's disease attenuate the response of cultured cells to g-secretase modulators regardless of their potency and structure. J. Neurochem. 116, 385-395 (2011).
21. C. Hock, S. Golombowski, F. Müller-Spahn, W. Naser, K. Beyreuther, U. Mönning, D. Schenk, C. Vigo-Pelfrey, A. M. Bush, R. Moir, R. Tanzi, J. H. Growdon, R. M. Nitsch, Cerebrospinal fluid levels of amyloid precursor protein and amyloid b-peptide in Alzheimer's disease and major depression-Inverse correlation with dementia severity. Eur. Neurol. 39, 111-118 (1998).
22. P.-W. Tsai, C.-Y. Yang, H.-T. Chang, C.-Y. Lan, Human antimicrobial peptide LL-37 inhibits adhesion of Candida albicans by interacting with yeast cell-wall carbohydrates. PLOS One 6, e17755 (2011).
23. A. M. Weidner, M. Housley, M. P. Murphy, H. LeVine III, Purified high molecular weight synthetic Ab(1-42) and biological Ab oligomers are equipotent in rapidly inducing MTT formazan exocytosis. Neurosci. Lett. 497, 1-5 (2011).
24. M. P. Lambert, A. K. Barlow, B. A. Chromy, C. Edwards, R. Freed, M. Liosatos, T. E. Morgan, I. Rozovsky, B. Trommer, K. L. Viola, P. Wals, C. Zhang, C. E. Finch, G. A. Krafft, W. L. Klein, Diffusible, nonfibrillar ligands derived from Ab1-42 are potent central nervous system neurotoxins. Proc. Natl. Acad. Sci. U.S.A. 95, 6448-6453 (1998).
25. T. Yang, S. Hong, T. O'Malley, R. A. Sperling, D. M. Walsh, D. J. Selkoe, New ELISAs with high specificity for soluble oligomers of amyloid b-protein detect natural Ab oligomers in human brain but not CSF. Alzheimers Dement. 9, 99-112 (2013).
26. R. Sood, Y. Domanov, M. Pietiäinen, V. P. Kontinen, P. K. J. Kinnunen, Binding of LL-37 to model biomembranes: Insight into target vs host cell recognition. Biochim. Biophys. Acta 1778, 983-996 (2008).
27. R. Feder, A. Dagan, A. Mor, Structure-activity relationship study of antimicrobial dermaseptin S4 showing the consequences of peptide oligomerization on selective cytotoxicity. J. Biol.Chem. 275, 4230-4238 (2000).
28. L. Leonova, V. N. Kokryakov, G. Aleshina, T. Hong, T. Nguyen, C. Zhao, A. J. Waring, R. I. Lehrer, Circular minidefensins and posttranslational generation of molecular diversity. J. Leukoc. Biol.70, 461-464 (2001).
29. R. I. Lehrer, Paradise lost and paradigm found. Nat. Immunol. 5, 775-776 (2004).
30. N. Sal-Man, Z. Oren, Y. Shai, Preassembly of membrane-active peptides is an important factor in their selectivity toward target cells. Biochemistry 41, 11921-11930 (2002).
31. D. J. Watson, A. D. Lander, D. J. Selkoe, Heparin-binding properties of the amyloidogenic peptides Ab and amylin. Dependence on aggregation state and inhibition by Congo red. J. Biol. Chem. 272, 31617-31624 (1997).
32. P.-W. Tsai, C.-Y. Yang, H.-T. Chang, C.-Y. Lan, Characterizing the role of cell-wall b-1,3-exoglucanase Xog1p in Candida albicans adhesion by the human antimicrobial peptide LL-37. PLOS One 6, e21394 (2011).
33. J. J. Calvete, M. A. Campanero-Rhodes, M. Raida, L. Sanz, Characterisation of the conformational and quaternary structure-dependent heparin-binding region of bovine seminal plasma protein PDC-109. FEBS Lett. 444, 260-264 (1999).
34. J. van Horssen, P. Wesseling, L. P. W. J. van den Heuvel, R. M. W. de Waal, M. M. Verbeek, Heparan sulphate proteoglycans in Alzheimer's disease and amyloid-related disorders.Lancet Neurol. 2, 482-492 (2003).
35. M. Torrent, D. Pulido, M. V. Nogués, E. Boix, Exploring new biological functions of amyloids: Bacteria cell agglutination mediated by host protein aggregation. PLOS Pathog. 8, e1003005 (2012).
36. H. Chu, M. Pazgier, G. Jung, S.-P. Nuccio, P. A. Castillo, M. F. de Jong, M. G. Winter, S. E. Winter, J. Wehkamp, B. Shen, N. H. Salzman, M. A. Underwood, R. M. Tsolis, G. M. Young, W. Lu, R. I. Lehrer, A. J. Bäumler, C. L. Bevins, Human a-defensin 6 promotes mucosal innate immunity through self-assembled peptide nanonets. Science 337, 477-481 (2012).
37. K. Pütsep, G. Carlsson, H. G. Boman, M. Andersson, Deficiency of antibacterial peptides in patients with morbus Kostmann: An observation study. Lancet 360, 1144-1149 (2002).
38. C. D. Ciornei, H. Tapper, A. Bjartell, N. H. Sternby, M. Bodelsson, Human antimicrobial peptide LL-37 is present in atherosclerotic plaques and induces death of vascular smooth muscle cells: A laboratory study. BMC Cardiovas. Disord. 6, 49 (2006).
39. J. M. Kahlenberg, M. J. Kaplan, Little peptide, big effects: The role of LL-37 in inflammation and autoimmune disease. J. Immunol. 191, 4895-4901 (2013).
40. Y. Shinkai, M. Morishima-Kawashima, Y. Ihara, M. Yoshimura, H. Shimada, Y. Ito, K. Yanagisawa, Amyloid b-protein deposition in the leptomeninges and cerebral cortex. Ann. Neurol. 42, 899-908 (1997).
41. L.-O. Brandenburg, D. Varoga, N. Nicolaeva, S. L. Leib, H. Wilms, R. Podschun, C. J. Wruck, J.-M. Schröder, T. Pufe, R. Lucius, Role of glial cells in the functional expression of LL-37/rat cathelin-related antimicrobial peptide in meningitis. J. Neuropathol. Exp. Neurol. 67, 1041-1054 (2008).
42. M. A. Wozniak, R. F. Itzhaki, S. J. Shipley, C. B. Dobson, Herpes simplex virus infection causes cellular b-amyloid accumulation and secretase upregulation. Neurosci. Lett. 429, 95-100 (2007).
43. J. Miklossy, Chronic inflammation and amyloidogenesis in Alzheimer's disease-Role of Spirochetes. J. Alzheimers Dis. 13, 381-391 (2008).
44. E. Boelen, F. R. M. Stassen, A. J. A. M. van der Ven, M. A. M. Lemmens, H. P. J. Steinbusch, C. A. Bruggeman, C. Schmitz, H. W. M. Steinbusch, Detection of amyloid beta aggregates in the brain of BALB/c mice after Chlamydia pneumoniae infection. Acta Neuropathol. 114, 255-261 (2007).
45. C. S. Little, C. J. Hammond, A. MacIntyre, B. J. Balin, D. M. Appelt, Chlamydia pneumoniae induces Alzheimer-like amyloid plaques in brains of BALB/c mice. Neurobiol. Aging 25, 419-429 (2004).
46. N. Papo, Y. Shai, Can we predict biological activity of antimicrobial peptides from their interactions with model phospholipid membranes? Peptides 24, 1693-1703 (2003).
47. V. H. Pomin, Heparin-binding proteins (chemokines and defensins) and their complexes with glycosaminoglycans from the solution NMR perspective. Curr. Protein Pept. Sci. 15, 738-744 (2014).
48. J. Wang, Y. Li, X. Wang, W. Chen, H. Sun, J. Wang, Lipopolysaccharide induces amyloid formation of antimicrobial peptide HAL-2. Biochim. Biophys. Acta 1838, 2910-2918 (2014).
49. O. Goldmann, E. Medina, The expanding world of extracellular traps: Not only neutrophils but much more. Front. Immunol. 3, 420 (2013).
50. S. S. Wilson, M. E. Wiens, J. G. Smith, Antiviral mechanisms of human defensins. J. Mol. Biol.425, 4965-4980 (2013).
51. P. Bergman, L. Johansson, H. Wan, A. Jones, R. L. Gallo, G. H. Gudmundsson, T. Hökfelt, A.-B. Jonsson, B. Agerberth, Induction of the antimicrobial peptide CRAMP in the blood-brain barrier and meninges after meningococcal infection. Infect. Immun. 74, 6982-6991 (2006).
52. R. Bals, D. J. Weiner, A. D. Moscioni, R. L. Meegalla, J. M. Wilson, Augmentation of innate host defense by expression of a cathelicidin antimicrobial peptide. Infect. Immun. 67, 6084-6089 (1999).
53. S. Eggert, K. Paliga, P. Soba, G. Evin, C. L. Masters, A. Weidemann, K. Beyreuther, The proteolytic processing of the amyloid precursor protein gene family members APLP-1 and APLP-2 involves a-, b-, g-, and D-like cleavages: Modulation of APLP-1 processing by nglycosylation.J. Biol. Chem. 279, 18146-18156 (2004).
54. S. A. M. Shariati, B. De Strooper, Redundancy and divergence in the amyloid precursor protein family. FEBS Lett. 587, 2036-2045 (2013).
55. K. Beyreuther, P. Pollwein, G. Multhaup, U. Mönning, G. König, T. Dyrks, W. Schubert, C. L. Masters, Regulation and expression of the Alzheimer's b/A4 amyloid protein precursor in health, disease, and Down's syndrome. Ann. N.Y. Acad. Sci. 695, 91-102 (1993).
56. D. Dominguez, J. Tournoy, D. Hartmann, T. Huth, K. Cryns, S. Deforce, L. Serneels, I. E. Camacho, E. Marjaux, K. Craessaerts, A. J. M. Roebroek, M. Schwake, R. D'Hooge, P. Bach, U. Kalinke, D. Moechars, C. Alzheimer, K. Reiss, P. Saftig, B. de Strooper, Phenotypic and biochemical analyses of BACE1-and BACE2-deficient mice. J. Biol. Chem. 280, 30797-30806 (2005).
57. R. H. Falk, R. L. Comenzo, M. Skinner, The systemic amyloidoses. N. Engl. J. Med. 337, 898-909 (1997).
58. B. L. Kagan, Antimicrobial amyloids? Biophys. J. 100, 1597-1598 (2011).
59. L. Wang, Q. Liu, J.-C. Chen, Y.-X. Cui, B. Zhou, Y.-X. Chen, Y.-F. Zhao, Y.-M. Li, Antimicrobial activity of human islet amyloid polypeptides: An insight into amyloid peptides' connection with antimicrobial peptides. Biol. Chem. 393, 641-646 (2012).
60. M. Pasupuleti, M. Roupe, V. Rydengård, K. Surewicz, W. K. Surewicz, A. Chalupka, M. Malmsten, O. E. Sörensen, A. Schmidtchen, Antimicrobial activity of human prion protein is mediated by its N-terminal region. PLOS One 4, e7358 (2009).
61. V. Vernekar, S. Velhal, A. Bandivdekar, Evaluation of cystatin C activities against HIV. Indian J. Med. Res. 141, 423-430 (2015).
62. M. Pasupuleti, M. Davoudi, M. Malmsten, A. Schmidtchen, Antimicrobial activity of a Cterminal peptide from human extracellular superoxide dismutase. BMC Res. Notes 2, 136 (2009).
63. C. Shah, R. Hari-Dass, J. G. Raynes, Serum amyloid A is an innate immune opsonin for Gram-negative bacteria. Blood 108, 1751-1757 (2006).
64. L. Millucci, E. Paccagnini, L. Ghezzi, G. Bernardini, D. Braconi, M. Laschi, M. Consumi, A. Spreafico, P. Tanganelli, P. Lupetti, A. Magnani, A. Santucci, Different factors affecting human ANP amyloid aggregation and their implications in congestive heart failure. PLOS One 6, e21870 (2011).
65. J. Miklossy, Emerging roles of pathogens in Alzheimer disease. Expert Rev. Mol. Med. 13, e30 (2011).
66. X.-L. Bu, X.-Q. Yao, S.-S. Jiao, F. Zeng, Y.-H. Liu, Y. Xiang, C.-R. Liang, Q.-H. Wang, X. Wang, H.-Y. Cao, X. Yi, B. Deng, C.-H. Liu, J. Xu, L.-L. Zhang, C.-Y. Gao, Z.-Q. Xu, M. Zhang, L. Wang, X.-L. Tan, X. Xu, H.-D. Zhou, Y.-J. Wang, A study on the association between infectious burden and Alzheimer's disease. Eur. J. Neurol. 22, 1519-1525 (2015).
67. D. B. Teplow, Preparation of amyloid b-protein for structural and functional studies.Methods Enzymol. 413, 20-33 (2006).
68. M. Bruatto, M. Gremmi, A. Nardacchione, M. Amerio, Effect of glucose starvation on germ-tube production by Candida albicans. Mycopathologia 123, 105-110 (1993).
69. I. M. Stromnes, J. M. Goverman, Active induction of experimental allergic encephalomyelitis.Nat. Protoc. 1, 1810-1819 (2006).
70. S. D. Miller, W. J. Karpus, Experimental autoimmune encephalomyelitis in the mouse. Curr.Protoc. Immunol. Chapter 15, 15.1.1-15.1.20 (2007).
71. S. H. Choi, K. Veeraraghavalu, O. Lazarov, S. Marler, R. M. Ransohoff, J. M. Ramirez, S. S. Sisodia, Non-cell-autonomous effects of presenilin 1 variants on enrichment-mediated hippocampal progenitor cell proliferation and differentiation. Neuron 59, 568-580 (2008).
72. J. R. Powell, F. M. Ausubel, Models of Caenorhabditis elegans infection by bacterial and fungal pathogens. Methods Mol. Biol. 415, 403-427 (2008).
73. M. J. Henry-Stanley, R. M. Garni, C. L. Wells, Adaptation of FUN-1 and Calcofluor white stains to assess the ability of viable and nonviable yeast to adhere to and be internalized by cultured mammalian cells. J. Microbiol. Methods 59, 289-292 (2004).