Identification and localization of Chlamydia pneumoniae in the Alzheimer's brain

Medical Microbiology and Immunology

Volumn 187, Issue 1, 1998, Pages 23-42

  Balin, Brian J ^a   Gérard, Hervé C ^a,b   Arking, E James ^a   Appelt, Denah M ^a   Branigan, Patrick J ^a,b   Abrams, J Todd ^a   Whittum Hudson, Judith A ^c,e   Hudson, Alan P ^a,b,d  

^a DREXEL UNIVERSITY COLLEGE OF MEDICINE   (United States)

^b VETERANS AFFAIRS MEDICAL CENTER   (United States)

^c JOHNS HOPKINS UNIVERSITY   (United States)

^d WAYNE STATE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^e Division of Rheumatology   (United States)

Author keywords

Alzheimer's disease; Chlamydia; Dementia; Infection; Inflammation

Indexed keywords

BACTERIAL DNA; RNA;

ADULT; AGED; ALZHEIMER DISEASE; ARTICLE; BACTERIAL GENE; BACTERIUM CULTURE; BACTERIUM IDENTIFICATION; CHLAMYDOPHILA PNEUMONIAE; CLINICAL ARTICLE; CONTROLLED STUDY; ELECTRON MICROSCOPY; FEMALE; GENETIC TRANSCRIPTION; HUMAN; HUMAN CELL; HUMAN TISSUE; IMMUNOELECTRON MICROSCOPY; IMMUNOHISTOCHEMISTRY; MACROGLIA; MALE; MICROGLIA; PERICYTE; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; RISK FACTOR;

AGED; AGED, 80 AND OVER; ALZHEIMER DISEASE; ANTIBODIES, MONOCLONAL; BRAIN; CHLAMYDOPHILA PNEUMONIAE; DNA, BACTERIAL; FEMALE; GENES, BACTERIAL; HUMANS; IMMUNOHISTOCHEMISTRY; MALE; MICROSCOPY, ELECTRON; MIDDLE AGED; POLYMERASE CHAIN REACTION; RNA, BACTERIAL;

EID: 0031857670     PISSN: 03008584     EISSN: None     Source Type: Journal    
DOI: 10.1007/s004300050071     Document Type: Article

References (98)

1. Alonso AC, Grundke-Iqbal I, Iqbal K (1996) Alzheimer's disease hyperphosphorylated tau sequesters normal tau into tangles of filaments and disassembles microtubules. Nat Med 2: 783-787
2. Appelt DM, Kopen GC, Boyne LJ, Balin BJ (1996) Localization of transglutaminase in hippocampal neurons: implications for Alzheimer's disease. J Histochem Cytochem 44: 1421-1427
3. Bauer J, Ganter U, Strauss SS, Stadtmuller G, Frommberger U, Bauer H, Volk B, Berger M (1992) The participation of interleukin-6 in the pathogenesis of Alzheimer's disease. Res Immunol 143: 650-657
4. Belardelli F, Gresser I (1996) The neglected role of type I interferon in the T-cell response: implications for its clinical use. Immunol Today 17: 369-372
5. Beutler AM, Whittum-Hudson JA, Nanagara R, Schumacher HR, Hudson AP (1994) Intracellular location of inapparently infecting Chlamydia in synovial tissue from patients with Reiter's syndrome. Immunol Res 13: 163-171
6. Blacker D, Haines JL, Rodes L, Terwedow H, Go RC, Harrell LE, Perry RT, Bassett SS, Chase G, Meyers D, Albert MS, Tanzi R (1997) APOE-4 and age at onset of Alzheimer's disease -The NIMH Genetics Initiative. Neurology 48: 139-147
7. Block S, Hedrick J, Hammerschlag JR, Cassell GH, Craft JC (1995) Mycoplasma pneumoniae and Chlamydia pneumoniae in pediatric community-acquired pneumonia: comparative efficacy and safety of clarithromycin vs. erythromycin ethylsuccinate. Pediatr Infect Dis 14: 471-477
8. Bolton CF, Yound GB, Zochodne DW (1993) The neurological consequences of sepsis. Ann Neurol 33: 94-100
9. Branigan PJ, Gérard HC, Hudson AP, Schumacher HR (1996) Comparison of synovial tissue and synovial fluid as source of nucleic acids for detection of Chlamydia trachomatis by polymerase chain reaction. Arthritis Rheum 39: 1740-1746
10. Breitner JC (1996) The role of anti-inflammatory drugs in the prevention and treatment of Alzheimer's disease. Annu Rev Med 47: 401-411
11. Breteler MM, Claus JJ, Duijn CM van, Launer LJ, Hofman A (1992) Epidemiology of Alzheimer's disease. Epidemiol Rev 14: 59-82
12. Bretschneider A, Burns W, Morrison A (1981) "Pop-off" technique. The ultrastructure of paraffin-embedded section. Am J Clin Pathol 76: 450-453
13. Burns A, Jacoby R, Luthert P, Levy R (1990) Cause of death in Alzheimer's disease. Age Aging 19: 341-344
14. Campbell F, Birkelund S, Ward ME, Panayi GS, Kingsley GH (1996) Sexually-acquired reactive arthritis synovial T cells respond to Chlamydia trachomatis 57 kD heat shock protein but not the major outer membrane protein. Arthritis Rheum 39 [Suppl]: S184
15. Campbell LA, O'Brien ER, Cappuccio AL, Kuo CC, Wang S-P, Stewart D, Patton DL, Cummings PK, Grayston JT (1995) Detection of Chlamydia pneumoniae TWAR in human coronary atherectomy tissues. J Infect Dis 172: 585-588
16. Capron L (1996) Chlamydia in coronary plaques - hidden culprit or harmless hobo. Nat Med 2: 856-857
17. Chakravarthy U, Stitt AW, McNally J, Bailie JR, Hoey EM, Duprex P (1995) Nitric oxide synthase activity and expression in retinal capillary endothelial cells and pericytes. Curr Eye Res 14: 285-294
18. Clark RF, Goate AM (1993) Molecular genetics of Alzheimer's disease. Arch Neurol 50: 1164-1172
19. Cook DG, Sung JC, Golde TE, Felsenstein KM, Wojczyk BS, Tanzi RE, Trojanowski JQ, Lee VM, Doms RW (1996) Expression and analysis of presenilin 1 in a human neuronal system: localization in cell bodies and dendrites. Proc Natl Acad Sci U S A 93: 9223-9228
20. Corder EH, Saunders AM, Strittmatter WJ, Schmechel EE, Gaskell PC, Small GW, Roses AD, Haines JL, Pericak-Vance MA (1993) Gene dose of apolipoprotein E type 4 allele and the risk of Alzheimer's disease in late onset families. Science 261: 921-923
21. Doty RL (1991) Olfactory capacities in aging and Alzheimer's disease. Psychophysical and anatomic considerations. Ann N Y Acad Sci 640: 20-27
22. Duff K, Eckman C, Zehr C, Yu X, Prada CM, Perez-tur J, Hutton M, Buee L, Harigaya Y, Yager D, Morgan D, Gordon MN, Holcomb L, Refolo L, Zenk B, Hardy J, Younkin S (1996) Increased amyloid-β42(43) in brains of mice expressing mutant presenilin I. Nature 383: 710-713
23. Duffy PE, Rapport M, Graf L (1980) Glial fibrillary acidic protein and Alzheimer-like senile dementia. Neurology 30: 778-782
24. Eng LF (1985) Glial fibrillary acid protein (GFAP): the major protein of glial intermediate filaments in differentiated astrocytes. J Neuroimmunol 8: 203-214
25. Evans DA, Funkenstein HH, Albert MS, Scherr PA, Cook NR, Chown MJ, Hebert LE, Taylor JO (1989) Prevalence of Alzheimer's disease in a community population of older persons. J Am Med Assoc 262: 2551-2556
26. Friedland RP, May C, Dahlberg J (1990) The viral hypothesis of Alzheimer's disease. Absence of antibodies to lentiviruses. Arch Neurol 47: 177-178
27. Gautrin D, Gauthier S (1989) Alzheimer's disease: environmental factors and etiologic hypotheses. Can J Neurol Sci 16: 375-387
28. Gaydos CA, TC Quinn, Eiden JJ (1992) Identification of Chlamydia pneumoniae by DNA amplification of the 16S rRNA gene. J Clin Microbiol 30: 796-800
29. Goedert M (1993) Tau protein and the neurofibrillary pathology of Alzheimer's disease. Trends Neurosci 16: 460-465
30. Gran JT, Hjetland R, Andreassen AH (1993) Pneumonia, myocarditis and reactive arthritis due to Chlamydia pneumoniae. Scand J Rheumatol 22: 43-44
31. Grayston JT (1992) Chlamydia pneumoniae, strain TWAR pneumoniae. Annu Rev Med 43: 317-323
32. Grayston JT, Campbell LA, Kuo CC, Mordhorst CC, Saikku P, Thom DH, Wang S-P (1990) A new respiratory tract pathogen: Chlamydia pneumoniae strain TWAR. J Infect Dis 161: 618-625
33. Grayston JT, Aldous MB, Easton A, Wang S-P, Kuo CC, Campbell LA, Altman J (1993) Evidence that Chlamydia pneumoniae causes pneumonia and bronchitis. J Infect Dis 168: 1231-1235
34. Greenberg SG, Davies P (1990) A preparation of Alzheimer paired helical filaments that displays distinct tau-proteins by polyacrylamide gel electrophoresis. Proc Natl Acad Sci USA 87: 5827-5831
35. Griffin DE, Hess JL, Moench TR (1987) Immune responses in the central nervous system. Toxicol Pathol 15: 294-302
36. Hahn DL, Dodge RW, Golubjatnikov R (1991) Association of Chlamydia pneumoniae (strain TWAR) infection with wheezing, asthmatic bronchitis, adult-onset asthma. J Am Med Assoc 266: 225-230
37. Hassler O (1966) Deep cerebral venous system in man. A microangiographic study on its areas of drainage and its anastomoses with the superficial cerebral veins. Neurology 16: 505-511
38. Hixson JE, Vernier DT (1990) Restriction isotyping of human apolipoprotein E by gene amplification and cleavage with HhaI. J Lipid Res 31: 545-548
39. Hofman A, Ott A, Breteler MM, Bots ML, Slooter AJ, Van Harskamp F, Duijn CN van, Broeckhoven C van, Grobee DE (1997) Atherosclerosis, apolipoprotein E, and prevalence of dementia and Alzheimer's disease in the Rotterdam study. Lancet 349: 151-153
40. Hyman CL, Roblin PM, Gaydos CA, Quinn TC, Schachter J, Hammerschlag MR (1995) Prevalence of asymptomatic naso-pharyngeal carriage of Chlamydia pneumoniae in subjectively healthy adults: assessment by polymerase chain reaction-enzyme immunoassay and culture. Clin Infect Dis 20: 1174-1178
41. Itzhaki R, Lin WR, Shang D, Wilcock GK, Faragher B, Jamieson GA (1997) Herpes simplex virus type 1 in brain and risk of Alzheimer's disease. Lancet 349: 241-244
42. Johnson RT (1994) Emerging infections of the nervous system. J Neurol Sci 124: 3-14
43. Kalaria RN (1992) The blood-brain barrier and cerebral microcirculation in Alzheimer's disease. Cerebrovasc Brain Metab Rev 4: 226-260
44. Keefover RW (1996) The clinical epidemiology of Alzheimer's disease. Neurol Clin 14: 337-351
45. Kingsbury AE, Foster OJ, Nisbet AP, Cairns N, Bray L, Eve DJ, Lee AJ, Marsden CD (1995) Tissue pH as an indicator of mRNA preservation in human post-mortem brain. Mol Brain Res 28: 311-318
46. Koskiniemi M, Gencay M, Salonen O, Puolakkainen M, Farkkila M, Saikku P, Vaheri A (1996) Chlamydia pneumoniae associated with central nervous system infections. Eur Neurol 36: 160-163
47. Kukull WA, Brenner DE, Speck CE, Nochlin D, Bowen J, McCormick W, Teri L, Pfanschmidt ML, Larson EB (1994) Causes of death associated with Alzheimer's disease: variation by level of cognitive impairment before death. J Am Geriatr Soc 42: 723-726
48. Lee MK, Slunt HH, Martin LJ, Thinakaran G, Kim G, Gandy SE, Seeger M, Koo E, Price DL, Sisodia SS (1996) Expression of presenilin 1 and 2 (PS1 and PS2) in human and murine tissues. J Neurosci 16: 7513-7525
49. Lee VM-Y, Balin BJ, Otvos L, Trojanowski JQ (1991) A 68 - a major subunit of paired helical filaments and derivatized forms of normal tau. Science 251: 675-679
50. Leinonen M (1993) Pathogenetic mechanisms and epidemiology of Chlamydia pneumoniae. Eur Heart J 14: 57-61
51. Lemere CA, Lopera F, Kosik KS, Lendon CL, Ossa J, Saido TC, Yamaguchi H, Ruiz A, Martinez A, Madrigal L, Hincapie L, Arango JC, Anthony DC, Koo EH, Goate AM, Selkoe DJ, Arango JC (1996) The E280A presenilin 1 Alzheimer mutation produces increased Aβ42 deposition and severe cerebellar pathology. Nat Med 2: 1146-1150
52. Li F, Bulbul R, Schumacher HR, Kieber-Emmons T, Callegari PE, Feldt JM von, Norden D, Freundlich B, Wang, Imonitie V, Chang CP, Nachamkin I, Weiner DB, Williams WV (1996) Molecular detection of bacterial DNA in venereal-associated arthritis. Arthritis Rheum 39: 950-958
53. Lippa CF, Saunders AM, Smith TW, Swearer JM, Drachman DA, Ghetti B, Nee L, Pulaski-Salo D, Dickson D, Robitaille Y, Bergeron C, Crain B, Benson MD, Farlow M, Hyman BT, St. George-Hyslop SP, Roses AD, Pollen DA (1996) Familial and sporadic Alzheimer's disease: neuropathology cannot exclude a final common pathway. Neurology 46: 406-412
54. Lobau S, Momat U, Brabetz W, Brade H (1994) Molecular cloning, sequence analysis, and functional characterization of the liposaccharide biosynthetic gene kdta encoding 3-deoxy-alpha-D-manno-octulosonic acid transferase of Chlamydia pneumoniae strain TW 183. Mol Microbiol 18: 391-399
55. Lomax MI, Welch MD, Darras BT, Grancke U, Grossman LI (1990) Novel use of a chimpanzee pseudogene for chromosomal mapping of human cytochrome c oxidase subunit IV. Gene 86: 209-216
56. Lue L-H, Brachova L, Civin WH, Rogers J (1996) Inflammation, Aβ deposition, and neurofibrillary tangle formation as correlates of Alzheimer's disease neurodegeneration. J Neuropathol Exp Neurol 55: 1083-1088
57. Malinverni R (1996) The role of cytokines in chlamydial infection. Curr Opin Infect Dis 9: 150-156
58. Mann DM, Trinkler AM, Yates PO (1983) Neurological disease and herpes simplex virus. An immunohistochemical study. Acta Neurol 60: 24-28
59. Mathews WB (1986) Unconventional virus infection and neurological disease. Neuropathol Appl Neurobiol 12: 111-116
60. McKee AC, Kosik KJ, Kowall NW (1991) Neuritic pathology and dementia in Alzheimer's disease. Ann Neurol 30: 156-165
61. Melgosa-Perez PM, Kuo CC, Campbell LA (1991) Sequence analysis of the major outer membrane protein gene of Chlamydia pneumoniae. Infect Immun 59: 2195-2199
62. Merrill JE, Jonakait GM (1995) Interactions of the nervous and immune systems in development, normal brain homeostasis, and disease. FASEB J 9: 611-618
63. Merrill JE, Ignarro LJ, Sherman MP, Melinek J, Lane TE (1993) Microglial cell cytotoxicity of oligodendrocytes is mediated through nitric oxide. J Immunol 151: 2132-2141
64. Mirra SS, Heyman A McKeel D, Sumi SM, Crain BJ, Brownlee LM, Vogel FS, Hughes JP, Belle G van, Berg L (1991) Consortium to establish a registry for Alzheimer's disease (CER-AD). Part II. Standardization of the neuropathologic assessment of Alzheimer's disease. Neurology 41: 479-486
65. Miyashita N, Kanamoto Y, Matsumoto A (1993) The morphology of Chlamydia pneumoniae. J Med Microbiol 38: 418-425
66. Moazed TC, Kuo CC, Patton DL, Grayston JT, Campbell LA (1996) Experimental rabbit models of Chlamydia pneumoniae infection. Am J Pathol 148: 667-676
67. Montarras D, Pinset C, Chelly J, Kahn A (1994) RT-PCR and gene expression. In: Mullis KB, Ferre F, Gibbs FA (eds) The polymerase chain reaction. Birkhäuser Press, Boston, pp 277-294
68. Mooradian AD (1988) Effect of aging on the blood-brain barrier. Neurobiol Aging 9: 31-39
69. Muhlestein JB, Hammond EH, Carlquist JF, Radicke E, Thomson EH, Karagounis LA, Woods ML, Anderson JL (1996) Increased incidence of Chlamydia species within the coronary arteries of patients with symptomatic atherosclerosis versus other forms of cardiovascular disease. J Am Coll Cardiol 27: 1555-1561
70. Nanagara R, Li F, Beutler AM, Hudson AP, Schumacher HR (1995) Alteration of Chlamydia trachomatis biological behavior in synovial membranes: suppression of surface antigen production in reactive arthritis and Reiter's syndrome. Arthritis Rheum 38: 1410-1417
71. Nevel-McGarvey CA, Levin RM, Hudson AP (1997) Transcription of mitochondrial and mitochondria-related nuclear genes in rabbit bladder after partial outlet obstruction. Mol Cell Biochem 173: 95-102
72. Nicoll JAR, Roberts GW, Graham DI (1995) Apolipoprotein E ε4 allele is associated with deposition of amyloid β-protein following head injury. Nat Med 1: 135-137
73. Numazaki K, Suzuki K, Chiba S (1995) Replication of Chlamydia trachomatis and C. pneumoniae in the human monocytic cell line U-937. J Med Microbiol 42: 191-195
74. Perez-Melgosa PM, Kuo CC, Campbell LA (1994) Isolation and characterization of a gene encoding a Chlamydia pneumoniae 76-kilodalton protein containing a species-specific epitope. Infect Immun 62: 880-886
75. Perl DP, Good PF (1991) Aluminium, Alzheimer's disease, and the olfactory system. Ann N Y Acad Sci 640: 8-13
76. Pogo BG, Casals J, Elizan TS (1987) A study of viral genomes and antigens in brains of patients with Alzheimer's disease. Brain 110: 907-915
77. Poulakkainen M, Parker J, Kuo CC, Grayston JT, Campbell LA (1995) Further characterization of Chlamydia pneumoniae specific monoclonal antibodies. Microbiol Immunol 39: 551-554
78. Reacher MH, Pe'er J, Rapoza PA, Whittum-Hudson JA, Taylor HR (1991) T cells and trachoma. Their role in cicatricial disease. Ophthalmology 98: 334-341
79. Renvoize EB, Awad IO, Hambling MH (1987) A sero-epidemiological study of conventional infectious agents in Alzheimer's disease. Age Ageing 16: 311-314
80. Ridker PM, Cushman M, Stampfer MJ, Tracy RP, Hennekens CH (1997) Inflammation, aspirin, and the risk of cardiovascular disease in apparently healthy men. N Engl J Med 336: 973-979
81. Roberts E (1986) Alzheimer's disease may begin in the nose and may be caused by aluminosilicates. Neurobiol Aging 7: 561-567
82. Rogers J, Mufson EJ (1990) Demonstrating immune-related antigens in Alzheimer's disease brain tissue. Neurobiol Aging 11: 477-479
83. Roses AD (1996) Apolipoprotein E alleles as risk factor in Alzheimer's disease. Annu Rev Med 47: 387-400
84. Schellenberg GD (1995) Genetic dissection of Alzheimer's disease, a heterogeneous disorder. Proc Natl Acad Sci U S A 92: 8552-8559
85. Scheuner D, Eckman C, Jensen M, Song X, Citron M, Suzuki N, Bird TD, Hardy J, Hutton M, Kukull W, Larson E, Levy-Lahad E, Viitanen M, Peskind E, Poorkaj P, Schellenberg G, Tanzi R, Wasco W, Lannfelt L, Selkoe D, Younkin S (1996) Secreted amyloid β-protein similar to that in the senile plaques of Alzheimer's disease is increased in vivo by the presenilin 1 and 2 mutations linked to familial Alzheimer's disease. Nat Med 2: 864-870
86. Sheng JG, Mrak RE, Griffin WST (1997) Glial-neuronal interactions in Alzheimer disease - progressive association of IL-1-alpha (+) microglia and S100-beta (+) astrocytes with neurofibrillary tangle stages. J Neuropathol Exp Neurol 56: 285-290
87. Simon AK, Seipelt E, Wu P, Wenzel B, Braun J, Seiper J (1993) Analysis of cytokine profiles in synovial T cell clones from chlamydial reactive arthritis patients: predominance of the TH1 subset. Clin Exp Immunol 94: 122-126
88. Smith MA, Taneda S, Richey PL, Miyata S, Yan SD, Stern D, Sayre LM, Monnier VM, Perry G (1995) Advanced Maillard reaction end products are associated with Alzheimer disease pathology. Proc Natl Acad Sci U S A 92: 2016-2020
89. Stephens RS (1994) Cell biology of Chlamydia infections. In: Orfila J, Byrne GI, Chernesky, MA, Grayston JT, Jones RB, Ridgway GL, Saikku P, Schachter J, Stamm WE, Stephens RS (eds) Chlamydial infections. Societa Editrice Esculapio, Bologna, pp 377-386
90. Styren SD, Civin WH, Rogers J (1990) Molecular, cellular, and pathologic characterization of HLA-DR immunoreactivity in normal elderly and Alzheimer's disease brain. Exp Neurol 110: 93-104
91. Wang J-Z, Grundke-Iqbal I, Iqbal K (1996) Glycosylation of microtubule-associated protein tau: an abnormal post-translational modification in Alzheimer's disease. Nat Med 2: 871-875
92. Whittum-Hudson JA, Prendergast RA, Taylor HR (1986) Changes in conjunctival lymphocyte populations induced by oral immunization with Chlamydia trachomatis. Curr Eye Res 5: 973-979
93. Whittum-Hudson JA, Taylor HR, Farazdaghi M, Prendergast RA (1986) Immunohistochemical study of the local inflammatory response to chlamydial ocular infection. Invest Ophthalmol Vis Sci 27: 64-69
94. Whittum-Hudson JA, Prendergast RA, Taylor HR (1987) Conjunctival immune response to Chlamydia trachomatis: effects of oral preimmunization on conjunctival lymphocyte subsets. Adv Exp Med Biol 216B: 1839-1846
95. Wimmer ML, Sandmann-Strupp R, Saikku P, Haberl RL (1996) Association of chlamydial infection with cerebrovascular disease. Stroke 27: 2207-2210
96. Wisniewski HM, Wrzolek M (1988) Pathogenesis of amyloid formation in Alzheimer's disease. Down's syndrome and serapie. Ciba Found Symp 135: 224-238
97. Wood PL, Choksi S, Bocchini V (1994) Inducible microglial nitric oxide synthase: a large membrane pool. Neuroreport 5: 977-980
98. Yankner BA (1996) New clues to Alzheimer's disease: unraveling the roles of amyloid and tau. Nat Med 2: 850-852