Glial alterations in tuberculous and cryptococcal meningitis and their relation to HIV co-infection – A study on human brains

Journal of Infection in Developing Countries

Volumn 8, Issue 11, 2014, Pages 1421-1443

  Tripathi, Surya ^a,b   Patro, Ishan ^b   Mahadevan, Anita ^a   Patro, Nisha ^b   Phillip, Mariamma ^a   Shankar, Susarla Krishna ^a  

^a NATIONAL INSTITUTE OF MENTAL HEALTH AND NEUROSCIENCES   (India)

^b JIWAJI UNIVERSITY   (India)

Author keywords

Astroglia; Cryptococcal meningitis; Microglia; Opportunistic infections; Tuberculous meningitis

Indexed keywords

CASPASE 3; GLIAL FIBRILLARY ACIDIC PROTEIN;

AGGLUTINATION TEST; ANTIBODY LABELING; APOPTOSIS; ARTICLE; ASTROCYTE; BRAIN TISSUE; COMPARATIVE STUDY; CONTROLLED STUDY; CRYPTOCOCCAL MENINGITIS; CRYPTOCOCCUS NEOFORMANS; DENTATE HILUS; DISEASE ASSOCIATION; ENCEPHALITIS; ENZYME LINKED IMMUNOSORBENT ASSAY; GLIA CELL; HIPPOCAMPAL CA1 REGION; HIPPOCAMPUS; HUMAN; HUMAN IMMUNODEFICIENCY VIRUS INFECTION; HUMAN TISSUE; HYPERPLASIA; HYPERTROPHY; IMMUNOHISTOCHEMISTRY; INFLAMMATION; MICROGLIA; MIXED INFECTION; MORPHOMETRICS; OPPORTUNISTIC INFECTION; POLYMERASE CHAIN REACTION; PREFRONTAL CORTEX; TUBERCULOUS MENINGITIS; ADOLESCENT; ADULT; CASE REPORT; COMPLICATION; CYTOCHEMISTRY; FEMALE; FRONTAL LOBE; IMMUNOLOGY; MALE; MICROSCOPY; MIDDLE AGED; PATHOLOGY; YOUNG ADULT;

ANIMALIA;

ADOLESCENT; ADULT; ASTROCYTES; COINFECTION; FEMALE; FRONTAL LOBE; HIPPOCAMPUS; HISTOCYTOCHEMISTRY; HIV INFECTIONS; HUMANS; IMMUNOHISTOCHEMISTRY; MALE; MENINGITIS, CRYPTOCOCCAL; MICROGLIA; MICROSCOPY; MIDDLE AGED; TUBERCULOSIS, MENINGEAL; YOUNG ADULT;

EID: 84924239605     PISSN: 20366590     EISSN: 19722680     Source Type: Journal    
DOI: 10.3855/jidc.3894     Document Type: Article

References (68)

1. Tan IL, Smith BR, von Geldern G, Mateen FJ, McArthur JC (2011) HIV-associated opportunistic infections of the CNS. Lancet Neurol 11: 605-617.
2. Joint United Nations Programme on HIV/AIDS (UNAIDS) (2010) Global report: UNAIDS report on the global AIDS epidemic 2010. Geneva: UNAIDS. Available: http://www.unaids.org/globalreport/Global_report.htm. Accessed 28 November 2012.
3. d'Arminio Monforte A, Cinque P, Mocroft A, Goebel FD, Antunes F, Katlama C, Stenz Justesen U, Vella S, Kirk O, Lundgren J (2004) Changing incidence of central nervous system diseases in the EuroSIDA cohort. Ann Neurol 55: 320-328.
4. Garvey L, Winston A, Walsh J, Post F, Porter K, Gazzard B, Fisher M, Leen C, Pillay D, Hill T (2011) HIV-associated central nervous system diseases in the recent combination antiretroviral therapy era. Eur J Neurol 18: 527-534.
5. Kwan CK, Ernst JD (2011) HIV and tuberculosis: a deadly human syndemic. Clin Microbiol Rev 24: 351-376.
6. Rich AR, McCordock HA (1933) The pathogenesis of tuberculous meningitis. Bull Johns Hopkins Hosp 52: 2-37.
7. Jarvis JN, Lawn SD, Vogt M, Bangani N, Wood R, Harrison TS (2009) Screening for cryptococcal antigenemia in patients accessing an antiretroviral treatment program in South Africa. Clin Infect Dis 48: 856-862.
8. Mahadevan A, Shankar SK, Satishchandra P, Ranga U, Chickabasaviah YT, Santosh V, Vasanthapuram R, Pardo CA, Nath A, Zink MC (2007) Characterization of human immunodeficiency virus (HIV)-infected cells in infiltrates associated with CNS opportunistic infections in patients with HIV clade C infection. J Neuropathol Exp Neurol 66: 799-808.
9. Shankar SK, Mahadevan A, Satishchandra P, Uday Kumar R, Yasha TC, Santosh V, Shankar Chandramuki A, Ravi V, Nath A (2005) Neuropathology of HIV/AIDS with an overview of the Indian scene. Indian J Med Res 121: 468-488.
10. Rock RB, Hu S, Gekker G, Sheng WS, May B, Kapur V, Peterson PK (2005) Mycobacterium tuberculosis-induced cytokine and chemokine expression by human microglia and astrocytes: effects of dexamethasone. J Infect Dis 192: 2054-2058.
11. Lee YC, Wang JT, Sun HY, Chen YC (2011) Comparisons of clinical features and mortality of cryptococcal meningitis between patients with and without human immunodeficiency virus infection. J Microbiol Immunol Infect 44: 338-345.
12. Liao CH, Chi CY, Wang YJ, Tseng SW, Chou CH, Ho CM, Lin PC, Ho MW, Wang JH (2012) Different presentations and outcomes between HIV-infected and HIV-uninfected patients with Cryptococcal meningitis. J Microbiol Immunol Infect 45: 296-304.
13. van Elsland SL, Springer P, Steenhuis IHM, van Toorn R, Schoeman JF, van Furth AM (2011) Tuberculous Meningitis: Barriers to Adherence in Home Treatment of Children and Caretaker Perceptions. J Trop Pediatr 58: 275-279.
14. Siddappa NB, Dash PK, Mahadevan A, Jayasuryan N, Hu F, Dice B, Keefe R, Satish KS, Satish B, Sreekanthan K (2004) Identification of subtype C human immunodeficiency virus type 1 by subtype-specific PCR and its use in the characterization of viruses circulating in the southern parts of India. J Clin Microbiol 42: 2742-2751.
15. Bignami A, Eng LF, Dahl D, Uyeda CT (1972) Localization of the glial fibrillary acidic protein in astrocytes by immunofluorescence. Brain Res 43: 429-435.
16. Su JH, Nichol KE, Sitch T, Sheu P, Chubb C, Miller BL, Cotman CW (2000) DNA damage and activated caspase-3 expression in neurons and astrocytes: evidence for apoptosis in frontotemporal dementia. Exp Neurol 163: 9-19.
17. Streit WJ, Braak H, Xue QS, Bechmann I (2009) Dystrophic (senescent) rather than activated microglial cells are associated with tau pathology and likely precede neurodegeneration in Alzheimer’s disease. Acta Neuropathol 118: 475-485.
18. Kettenmann H, Verkhratsky A (2008) Neuroglia: the 150 years after. Trends Neurosci 31: 653.
19. Raivich G, Jones LL, Werner A, Blothmann H, Doetschmann T, Kreutzberg GW (1999) Molecular signals for glial activation: pro-and anti-inflammatory cytokines in the injured brain. Acta Neurochir Suppl 73: 21-30.
20. Sofroniew MV (2009) Molecular dissection of reactive astrogliosis and glial scar formation. Trends Neurosci 32: 638-647.
21. Sofroniew MV, Vinters HV (2010) Astrocytes: biology and pathology. Acta Neuropathol 119: 7-35.
22. Hu J, Ferreira A, Van Eldik LJ (1997) S100β induces neuronal cell death through nitric oxide release from astrocytes. J Neurochem 69: 2294-2301.
23. Patro N, Shrivastava M, Tripathi S, Patro IK (2009) S100β upregulation: a possible mechanism of deltamethrin toxicity and motor coordination deficits. Neurotoxicol Teratol 31: 169-176.
24. Van Eldik LJ, Wainwright MS (2003) The Janus face of glial-derived S100B: beneficial and detrimental functions in the brain. Restor Neurol Neurosci 21: 97-108.
25. Huttunen HJ, Kuja-Panula J, Sorci G, Agneletti AL, Donato R, Rauvala H (2000) Coregulation of neurite outgrowth and cell survival by amphoterin and S100 proteins through receptor for advanced glycation end products (RAGE) activation. J Biol Chem 275: 40096-40105.
26. Li Y, Wang J, Sheng JG, Liu L, Barger SW, Jones RA, Van Eldik LJ, Mrak RE, Griffin WST (1998) S100β Increases Levels of β-Amyloid Precursor Protein and Its Encoding mRNA in Rat Neuronal Cultures. J Neurochem 71: 1421-1428.
27. Rickmann M, Wolff JR (1995) S100 protein expression in subpopulations of neurons of rat brain. Neuroscience 67: 977-991.
28. Petrova TV, Hu J, Van Eldik LJ (2000) Modulation of glial activation by astrocyte-derived protein S100B: differential responses of astrocyte and microglial cultures. Brain Res 853: 74-80.
29. Esposito G, De Filippis D, Cirillo C, Sarnelli G, Cuomo R, Iuvone T (2006) The astroglial-derived S100β protein stimulates the expression of nitric oxide synthase in rodent macrophages through p38 MAP kinase activation. Life Sci 78: 2707-2715.
30. Anders K, Steinsapir KD, Iverson DJ, Glasgow BJ, Layfield LJ, Brown WJ, Cancilla PA, Verity MA, Vinters HV (1986) Neuropathologic findings in the acquired immunodeficiency syndrome (AIDS). Clin Neuropath 5: 1.
31. Berger JR, Harris JO, Gregoriost J, Norenbergt M (1990) Cerebrovascular disease in AIDS: a case-control study. AIDS 4: 239.
32. Davalos D, Grutzendler J, Yang G, Kim JV, Zuo Y, Jung S, Littman DR, Dustin ML, Gan WB (2005) ATP mediates rapid microglial response to local brain injury in vivo. Nat Neurosci 8: 752-758.
33. Kreutzberg GW (1996) Microglia: a sensor for pathological events in the CNS. Trends Neurosci 19: 312-318.
34. Nimmerjahn A, Kirchhoff F, Helmchen F (2005) Resting microglial cells are highly dynamic surveillants of brain parenchyma in vivo. Science 308: 1314-1318.
35. Graeber MB, Streit WJ, Kreutzberg GW (1988) The microglial cytoskeleton: vimentin is localized within activated cellsin situ. J Neurocytol 17: 573-580.
36. Solomon JN, Lewis CAB, Ajami B, Corbel SY, Rossi F, Krieger C (2006) Origin and distribution of bone marrow-derived cells in the central nervous system in a mouse model of amyotrophic lateral sclerosis. Glia 53: 744-753.
37. Djukic M, Mildner A, Schmidt H, Czesnik D, Bruck, W, Priller J, Nau R, Prinz M (2006) Circulating monocytes engraft in the brain, differentiate into microglia and contribute to the pathology following meningitis in mice. Brain 129: 2394-2403.
38. Patro IK, Amit, Shrivastava M, Bhumika S, Patro N (2010) Poly I:C induced microglial activation impairs motor activity in adult rats. Indian J Exp Biol 48: 104-109.
39. Kielian T (2004) Microglia and chemokines in infectious diseases of the nervous system: views and reviews. Front Biosci 9: 732-750.
40. Berenguer J, Moreno S, Laguna F, Vicente T, Adrados M, Ortega A, Gonzalez-LaHoz J, Bouza E (1992) Tuberculous meningitis in patients infected with the human immunodeficiency virus. N Engl J Med 326: 668-672.
41. Dube MP, Holtom PD, Larsen RA (1992) Tuberculous meningitis in patients with and without human immunodeficiency virus infection. Am J Med 93: 520-524.
42. Thwaites GE, Duc Bang N, Huy Dung N, Thi Quy H, Thi Tuong Oanh D, Thi Cam Thoa N, Quang Hien N, Tri Thuc N, Ngoc Hai N, Thi Ngoc Lan N, Ngoc Lan N, Hong Duc N, Ngoc Tuan V, Huu Hiep C, Thi Hong Chau T, Phuong Mai P, Thi Dung N, Stepniewska K, Simmons CP, White NJ, Tinh Hien T, Farrar JJ (2005) The influence of HIV infection on clinical presentation, response to treatment, and outcome in adults with tuberculous meningitis. J Infect Dis 192: 2134-2141.
43. Schiefer J, Kampe K, Dodt HU, Zieglgansberger W, Kreutzberg GW (1999) Microglial motility in the rat facial nucleus following peripheral axotomy. J Neurocytol 28: 439-453.
44. Yamada K, Tanaka N, Nakanishi K, Kamei N, Ishikawa M, Mizuno T, Igarashi K, Ochi M (2008) Modulation of the secondary injury process after spinal cord injury in Bach1-deficient mice by heme oxygenase-1. J Neurosurg Spine 9: 611-620.
45. Bezuidenhout J, Roberts T, Muller L, Van Helden P, Walzl G (2009) Pleural tuberculosis in patients with early HIV infection is associated with increased TNF-alpha expression and necrosis in granulomas. PLoS One 4: e4228.
46. de Noronha AL, Bafica A, Nogueira L, Barral A, Barral-Netto M (2008) Lung granulomas from Mycobacterium tuberculosis/HIV-1 co-infected patients display decreased in situ TNF production. Pathol Res Pract 204: 155.
47. Lawn SD, Butera ST, Shinnick TM (2002) Tuberculosis unleashed: the impact of human immunodeficiency virus infection on the host granulomatous response to Mycobacterium tuberculosis. Microbes Infect 4: 635-646.
48. Goldman DL, Khine H, Abadi J, Lindenberg DJ, Pirofski L, Niang R, Casadevall A (2001) Serologic evidence for Cryptococcus neoformansinfection in early childhood. Pediatrics 107: e66-e66.
49. Aguirre K, Miller S (2002) MHC class II-positive perivascular microglial cells mediate resistance to Cryptococcus neoformans brain infection. Glia 39: 184-188.
50. Chao CC, Gekker G, Hu S, Peterson PK (1994) Human microglial cell defense against Toxoplasma gondii. The role of cytokines. J Immunol 152: 1246-1252.
51. Peterson PK, Hu S, Anderson WR, Chao CC (1994) Nitric oxide production and neurotoxicity mediated by activated microglia from human versus mouse brain. J Infect Dis 170: 457-460.
52. Lipovsky MM, Gekker G, Hu S, Hoepelman AIM, Peterson PK (1998) Morphine Enhances Complement Receptor-Mediated Phagocytosis of Cryptococcus neoformans by Human Microglia. Clin Immunol Immunopathol 87: 163-167.
53. Lee SC, Kress Y, Zhao ML, Dickson DW, Casadevall A (1995) Cryptococcus neoformans survive and replicate in human microglia. Lab Invest 73: 871.
54. Eugenin EA, Berman JW (2003) Chemokine-dependent mechanisms of leukocyte trafficking across a model of the blood-brain barrier. Methods 29: 351-361.
55. Lee R, Kermani P, Teng KK, Hempstead BL (2001) Regulation of cell survival by secreted proneurotrophins. Science 294: 1945-1948.
56. Liu B, Wang K, Gao HM, Mandavilli B, Wang JY, Hong JS (2001) Molecular consequences of activated microglia in the brain: overactivation induces apoptosis. J Neurochem 77: 182-189.
57. Suk K, Lee J, Hur J, Kim YS, Lee MS, Cha S, Yeou Kim S, Kim H (2001) Activation-induced cell death of rat astrocytes. Brain Res 900: 342-347.
58. Polazzi E, Contestabile A (2006) Overactivation of LPS-stimulated microglial cells by co-cultured neurons or neuron-conditioned medium. J Neuroimmunol 172: 104-111.
59. Garden GA, Budd SL, Tsai E, Hanson L, Kaul M, D'Emilia DM, Friedlander RM, Yuan J, Masliah E, Lipton SA (2002) Caspase cascades in human immunodeficiency virus-associated neurodegeneration. J Neurosci 22: 4015-4024.
60. Kaul M, Garden GA, Lipton SA (2001) Pathways to neuronal injury and apoptosis in HIV-associated dementia. Nature 410: 988-994.
61. Atzori C, Ghetti B, Piva R, Srinivasan AN, Zolo P, Delisle MB, Mirra SS, Migheli A (2001) Activation of the JNK/p38 pathway occurs in diseases characterized by tau protein pathology and is related to tau phosphorylation but not to apoptosis. J Neuropathol Exp Neurol 60: 1190-1197.
62. Gleckman AM, Jiang Z, Liu Y, Smith TW (1999) Neuronal and glial DNA fragmentation in Pick’s disease. Acta Neuropathol 98: 55-61.
63. McLaughlin BA, Hartnett KA, Erhardt JA, Legos JJ, White RF, Barone FC, Aizenman E (2003) Caspase 3 activation is essential for neuroprotection in preconditioning. Proc Natl Acad Sci USA 100: 715-720.
64. Broe M, Kril J, Halliday GM (2004) Astrocytic degeneration relates to the severity of disease in frontotemporal dementia. Brain 127: 2214-2220.
65. Martin JA, Craft DK, Su JH, Kim RC, Cotman CW (2001) Astrocytes degenerate in frontotemporal dementia: possible relation to hypoperfusion. Neurobiol Aging 22: 195-207.
66. Zhang Y, Stone J (1997) Role of astrocytes in the control of developing retinal vessels. Invest Ophthalmol Vis Sci 38: 1653-1666.
67. Anthony IC, Bell PJE (2008) The neuropathology of HIV/AIDS. Int Rev Psychiatry 20: 15-24.
68. Boisse L, Gill MJ, Power C (2008) HIV infection of the central nervous system: clinical features and neuropathogenesis. Neurol Clin 26: 799-819.