Dual lentivirus infection potentiates neuroinflammation and neurodegeneration: Viral copassage enhances neurovirulence

Journal of NeuroVirology

Volumn 15, Issue 2, 2009, Pages 139-152

  Afkhami Goli, Amir ^a   Liu, Shu Hong ^c   Zhu, Yu ^a   Antony, Joseph M ^a   Arab, Hosseinali ^b   Power, Christopher ^a,c  

^a UNIVERSITY OF ALBERTA   (Canada)

^b UNIVERSITY OF TEHRAN   (Iran)

^c UNIVERSITY OF CALGARY   (Canada)

Author keywords

Apoptosis; Dual infection; FIV; Glia; Nervous system; Neuroinflammation; Neuron

Indexed keywords

CASPASE 3; INDOLEAMINE 2,3 DIOXYGENASE; INTERLEUKIN 1BETA; SYNAPTOPHYSIN; TUMOR NECROSIS FACTOR ALPHA;

ACQUIRED IMMUNE DEFICIENCY SYNDROME; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BASAL GANGLION; BRAIN CORTEX; CAT; CD4+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; CHOLINERGIC NERVE CELL; CONTROLLED STUDY; FELINE IMMUNODEFICIENCY VIRUS; GABAERGIC SYSTEM; HUMAN; HUMAN CELL; IMMUNE RESPONSE; MACROPHAGE ACTIVATION; MIXED INFECTION; NERVE DEGENERATION; NERVOUS SYSTEM INFLAMMATION; NEUROPATHOLOGY; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; RETROVIRUS INFECTION; SUPERINFECTION; VIRUS LOAD; VIRUS VIRULENCE; ANIMAL; BIOSYNTHESIS; BRAIN; CULTURE TECHNIQUE; FEMALE; IMMUNOLOGY; INFLAMMATION; LYMPHOCYTE COUNT; METABOLISM; PATHOGENICITY; PATHOLOGY; PREGNANCY; VIROLOGY; VIRULENCE;

ANIMALIA; FELIDAE; FELINE IMMUNODEFICIENCY VIRUS; LENTIVIRUS;

ANIMALS; CATS; CELL CULTURE TECHNIQUES; CEREBRUM; FEMALE; HUMANS; IMMUNODEFICIENCY VIRUS, FELINE; INDOLEAMINE-PYRROLE 2,3,-DIOXYGENASE; INFLAMMATION; INTERLEUKIN-1BETA; LENTIVIRUS INFECTIONS; LYMPHOCYTE COUNT; NERVE DEGENERATION; PREGNANCY; SYNAPTOPHYSIN; TUMOR NECROSIS FACTOR-ALPHA; VIRULENCE;

EID: 67650306628     PISSN: 13550284     EISSN: None     Source Type: Journal    
DOI: 10.1080/13550280802534763     Document Type: Article

References (54)

1. Altfeld, M., Allen, TM, Yu, XG, Johnston, MN, Agrawal, D., Korber, BT, Montefiori, DC, O'Connor, DH, Davis, BT, Lee, PK, Maier, EL, Harlow, J., Goulder, PJ, Brander, C., Rosenberg, ES and Walker, BD (2002) HIV-1 superinfection despite broad CD8+ T-cell responses containing replication of the primary virus. Nature, 420, pp. 434-439.
2. Andersson, S., Norrgren, H., Dias, F., Biberfeld, G. and Albert, J. (1999) Molecular characterization of human immunodeficiency virus (HIV)-1 and -2 in individuals from guinea-bissau with single or dual infections: Predominance of a distinct HIV-1 subtype A/G recombinant in West Africa. Virology., 262, pp. 312-320.
3. Becker-Pergola, G., Mellquist, JL, Guay, L., Mmiro, F., Ndugwa, C., Kataaha, P., Jackson, JB and Eshleman, SH (2000) Identification of diverse HIV type 1 subtypes and dual HIV type 1 infection in pregnant Ugandan women. AIDS Res Hum Retroviruses., 16, pp. 1099-1104.
4. Bendinelli, M., Pistello, M., Lombardi, S., Poli, A., Garzelli, C., Matteucci, D., Ceccherini-Nelli, L., Malvaldi, G. and Tozzini, F. (1995) Feline immunodeficiency virus: An interesting model for AIDS studies and an important cat pathogen. Clin Microbiol Rev., 8, pp. 87-112.
5. Blackard, JT, Cohen, DE and Mayer, KH (2002) Human immunodeficiency virus superinfection and recombination: Current state of knowledge and potential clinical consequences. Clin Infect Dis., 34, pp. 1108-1114.
6. Brumme, ZL and Harrigan, PR (2006) The impact of human genetic variation on HIV disease in the era of HAART. AIDS Rev., 8, pp. 78-87.
7. Fang, G., Weiser, B., Kuiken, C., Philpott, SM, Rowland-Jones, S., Plummer, F., Kimani, J., Shi, B., Kaul, R., Bwayo, J., Anzala, O. and Burger, H. (2004) Recombination following superinfection by HIV-1. AIDS., 18, pp. 153-159.
8. Georges-Courbot, MC, Lu, CY, Makuwa, M., Telfer, P., Onanga, R., Dubreuil, G., Chen, Z., Smith, SM, Georges, A., Gao, F., Hahn, BH and Marx, PA (1998) Natural infection of a household pet red-capped mangabey (Cercocebus torquatus torquatus) with a new simian immunodeficiency virus. J Virol., 72, pp. 600-608.
9. Hu, DJ, Subbarao, S., Vanichseni, S., Mock, PA, Ramos, A., Nguyen, L., Chaowanachan, T., Griensven, F., Choopanya, K., Mastro, TD and Tappero, JW (2005) Frequency of HIV-1 dual subtype infections, including intersubtype superinfections, among injection drug users in Bangkok, Thailand. AIDS., 19, pp. 303-308.
10. Iversen, AK, Learn, GH, Fugger, L., Gerstoft, J., Mullins, JI and Skinhoj, P. (1999) Presence of multiple HIV subtypes and a high frequency of subtype chimeric viruses in heterosexually infected women. J Acquir Immune Defic Syndr., 22, pp. 325-332.
11. Jin, MJ, Hui, H., Robertson, DL, Muller, MC, Barre-Sinoussi, F., Hirsch, VM, Allan, JS, Shaw, GM, Sharp, PM and Hahn, BH (1994) Mosaic genome structure of simian immunodeficiency virus from west African green monkeys. EMBO J., 13, pp. 2935-2947.
12. Johnston, JB, Jiang, Y., van Marle, G., Mayne, MB, Ni, W., Holden, J., McArthur, JC and Power, C. (2000) Lentivirus infection in the brain induces matrix metalloproteinase expression: Role of envelope diversity. J Virol., 74, pp. 7211-7220.
13. Johnston, JB, Silva, C., Hiebert, T., Buist, R., Dawood, MR, Peeling, J. and Power, C. (2002) Neurovirulence depends on virus input titer in brain in feline immunodeficiency virus infection: Evidence for activation of innate immunity and neuronal injury. J NeuroVirol., 8, pp. 420-431.
14. Johnston, JB, Silva, C. and Power, C. (2002) Envelope gene-mediated neurovirulence in feline immunodeficiency virus infection: Induction of matrix metalloproteinases and neuronal injury. J Virol., 76, pp. 2622-2633.
15. Jost, S., Bernard, MC, Kaiser, L., Yerly, S., Hirschel, B., Samri, A., Autran, B., Goh, LE and Perrin, L. (2002) A patient with HIV-1 superinfection. N Engl J Med., 347, pp. 731-736.
16. Kantor, R. and Katzenstein, D. (2004) Drug resistance in non-subtype B HIV-1. J Clin Virol., 29, pp. 152-159.
17. Kim, JH, McLinden, RJ, Mosca, JD, Burke, DS, Boswell, RN, Birx, DL and Redfield, RR (1996) Transcriptional effects of superinfection in HIV chronically infected T cells: Studies in dually infected clones. J Acquir Immune Defic Syndr Hum Retrovirol., 12, pp. 329-342.
18. Kim, JH, Mosca, JD, Vahey, MT, McLinden, RJ, Burke, DS and Redfield, RR (1993) Consequences of human immunodeficiency virus type 1 superinfection of chronically infected cells. AIDS Res Hum Retroviruses., 9, pp. 875-882.
19. Klausner, RD, Fauci, AS, Corey, L., Nabel, GJ, Gayle, H., Berkley, S., Haynes, BF, Baltimore, D., Collins, C., Douglas, RG, Esparza, J., Francis, DP, Ganguly, NK, Gerberding, JL, Johnston, MI, Kazatchkine, MD, McMichael, AJ, Makgoba, MW, Pantaleo, G., Piot, P., Shao, Y., Tramont, E., Varmus, H. and Wasserheit, JN (2003) Medicine. The need for a global HIV vaccine enterprise. Science., 300, pp. 2036-2039.
20. Koelsch, KK, Smith, DM, Little, SJ, Ignacio, CC, Macaranas, TR, Brown, AJ, Petropoulos, CJ, Richman, DD and Wong, JK (2003) Clade B HIV-1 superinfection with wild-type virus after primary infection with drug-resistant clade B virus. AIDS., 17, pp. F11-F16.
21. Long, EM, Martin Jr, HL, Kreiss, JK, Rainwater, SM, Lavreys, L., Jackson, DJ, Rakwar, J., Mandaliya, K. and Overbaugh, J. (2000) Gender differences in HIV-1 diversity at time of infection. Nat Med., 6, pp. 71-75.
22. McCutchan, FE, Hoelscher, M., Tovanabutra, S., Piyasirisilp, S., Sanders-Buell, E., Ramos, G., Jagodzinski, L., Polonis, V., Maboko, L., Mmbando, D., Hoffmann, O., Riedner, G., von Sonnenburg, F., Robb, M. and Birx, DL (2005) In-depth analysis of a heterosexually acquired human immunodeficiency virus type 1 superinfection: Evolution, temporal fluctuation, and intercompartment dynamics from the seronegative window period through 30 months postinfection. J Virol., 79, pp. 11693-11704.
23. Nath, A., Conant, K., Chen, P., Scott, C. and Major, EO (1999) Transient exposure to HIV-1 Tat protein results in cytokine production in macrophages and astrocytes. A hit and run phenomenon. J Biol Chem., 274, pp. 17098-17102.
24. Nethe, M., Berkhout, B. and van der Kuyl, AC (2005) Retroviral superinfection resistance. Retrovirology., 2, p. 52.
25. Noorbakhsh, F., Tang, Q., Liu, S., Silva, C., van Marle, G. and Power, C. (2006) Lentivirus envelope protein exerts differential neuropathogenic effects depending on the site of expression and target cell. Virology., 348, pp. 260-276.
26. Otten, RA, Ellenberger, DL, Adams, DR, Fridlund, CA, Jackson, E., Pieniazek, D. and Rayfield, MA (1999) Identification of a window period for susceptibility to dual infection with two distinct human immunodeficiency virus type 2 isolates in a Macaca nemestrina (pig-tailed macaque) model. J Infect Dis., 180, pp. 673-684.
27. Patrick, MK, Johnston, JB and Power, C. (2002) Lentiviral neuropathogenesis: Comparative neuroinvasion, neurotropism, neurovirulence, and host neurosusceptibility. J Virol., 76, pp. 7923-7931.
28. Persidsky, Y., Buttini, M., Limoges, J., Bock, P. and Gendelman, HE (1997) An analysis of HIV-1-associated inflammatory products in brain tissue of humans and SCID mice with HIV-1 encephalitis. J NeuroVirol., 3, pp. 401-416.
29. Phillips, TR, Prospero-Garcia, O., Puaoi, DL, Lerner, DL, Fox, HS, Olmsted, RA, Bloom, FE, Henriksen, SJ and Elder, JH (1994) Neurological abnormalities associated with feline immunodeficiency virus infection. J Gen Virol, 75, pp. 979-987.
30. Power, C. (2001) Retroviral diseases of the nervous system: Pathogenic host response or viral gene-mediated neurovirulence?. Trends Neurosci., 24, pp. 162-169.
31. Power, C., Buist, R., Johnston, JB, Del Bigio, MR, Ni, W., Dawood, MR and Peeling, J. (1998) Neurovirulence in feline immunodeficiency virus-infected neonatal cats is viral strain specific and dependent on systemic immune suppression. J Virol., 72, pp. 9109-9115.
32. Power, C., Henry, S., Del Bigio, MR, Larsen, PH, Corbett, D., Imai, Y., Yong, VW and Peeling, J. (2003) Intracerebral hemorrhage induces macrophage activation and matrix metalloproteinases. Ann Neurol., 53, pp. 731-742.
33. Power, C., Moench, T., Peeling, J., Kong, PA and Langelier, T. (1997) Feline immunodeficiency virus causes increased glutamate levels and neuronal loss in brain. Neuroscience., 77, pp. 1175-1185.
34. Prospero-Garcia, O., Huitron-Resendiz, S., Casalman, SC, Sanchez-Alavez, M., Diaz-Ruiz, O., Navarro, L., Lerner, DL, Phillips, TR, Elder, JH and Henriksen, SJ (1999) Feline immunodeficiency virus envelope protein (FIVgp120) causes electrophysiological alterations in rats. Brain Res., 836, pp. 203-209.
35. Ramos, A., Hu, DJ, Nguyen, L., Phan, KO, Vanichseni, S., Promadej, N., Choopanya, K., Callahan, M., Young, NL, McNicholl, J., Mastro, TD, Folks, TM and Subbarao, S. (2002) Intersubtype human immunodeficiency virus type 1 superinfection following seroconversion to primary infection in two injection drug users. J Virol., 76, pp. 7444-7452.
36. Ramos, A., Tanuri, A., Schechter, M., Rayfield, MA, Hu, DJ, Cabral, MC, Bandea, CI, Baggs, J. and Pieniazek, D. (1999) Dual and recombinant infections: An integral part of the HIV-1 epidemic in Brazil. Emerg Infect Dis., 5, pp. 65-74.
37. Salemi, M., Lamers, SL, Yu, S., de Oliveira, T., Fitch, WM and McGrath, MS (2005) Phylodynamic analysis of human immunodeficiency virus type 1 in distinct brain compartments provides a model for the neuropathogenesis of AIDS. J Virol., 79, pp. 11343-11352.
38. Sardar, AM and Reynolds, GP (1995) Frontal cortex indoleamine-2,3-dioxygenase activity is increased in HIV-1-associated dementia. Neurosci Lett., 187, pp. 9-12.
39. Sarr, AD, Sankale, JL, Gueye-Ndiaye, A., Essex, M., Mboup, S. and Kanki, PJ (2000) Genetic analysis of HIV type 2 in monotypic and dual HIV infections. AIDS Res Hum Retroviruses., 16, pp. 295-298.
40. Schwarcz, R. and Pellicciari, R. (2002) Manipulation of brain kynurenines: Glial targets, neuronal effects, and clinical opportunities. J Pharmacol Exp Ther., 303, pp. 1-10.
41. Silva, C., Zhang, K., Tsutsui, S., Holden, JK, Gill, MJ and Power, C. (2003) Growth hormone prevents human immunodeficiency virus-induced neuronal p53 expression. Ann Neurol., 54, pp. 605-614.
42. Smit, TK, Brew, BJ, Tourtellotte, W., Morgello, S., Gelman, BB and Saksena, NK (2004) Independent evolution of human immunodeficiency virus (HIV) drug resistance mutations in diverse areas of the brain in HIV-infected patients, with and without dementia, on antiretroviral treatment. J Virol., 78, pp. 10133-10148.
43. Smith, DM, Wong, JK, Hightower, GK, Ignacio, CC, Koelsch, KK, Petropoulos, CJ, Richman, DD and Little, SJ (2005) HIV drug resistance acquired through superinfection. AIDS., 19, pp. 1251-1256.
44. Takeb, EY, Kusagawa, S. and Motomura, K. (2004) Molecular epidemiology of HIV: Tracking AIDS pandemic. Pediatr Int., 46, pp. 236-244.
45. Takehisa, J., Zekeng, L., Miura, T., Ido, E., Yamashita, M., Mboudjeka, I., Gurtler, LG, Hayami, M. and Kaptue, L. (1997) Triple HIV-1 infection with group O and Group M of different clades in a single Cameroonian AIDS patient. J Acquir Immune Defic Syndr Hum Retrovirol., 14, pp. 81-82.
46. Taylor, BS, Sobieszczyk, ME, McCutchan, FE and Hammer, SM (2008) The challenge of HIV-1 subtype diversity. N Engl J Med., 358, pp. 1590-1602.
47. Thomson, MM, Delgado, E., Manjon, N., Ocampo, A., Villahermosa, ML, Marino, A., Herrero, I., Cuevas, MT, Vazquez-de Parga, E, Perez-Alvarez, L., Medrano, L., Taboada, JA and Najera, R. (2001) HIV-1 genetic diversity in Galicia Spain: BG intersubtype recombinant viruses circulating among injecting drug users. AIDS., 15, pp. 509-516.
48. Tsutsui, S., Schnermann, J., Noorbakhsh, F., Henry, S., Yong, VW, Winston, BW, Warren, K. and Power, C. (2004) A1 adenosine receptor upregulation and activation attenuates neuroinflammation and demyelination in a model of multiple sclerosis. J Neurosci., 24, pp. 1521-1529.
49. van Marle, G., Antony, JM, Silva, C., Sullivan, A. and Power, C. (2005) Aberrant cortical neurogenesis in a pediatric neuroAIDS model: neurotrophic effects of growth hormone. AIDS., 19, pp. 1781-1791.
50. Weed, MR, Hienz, RD, Brady, JV, Adams, RJ, Mankowski, JL, Clements, JE and Zink, MC (2003) Central nervous system correlates of behavioral deficits following simian immunodeficiency virus infection. J NeuroVirol., 9, pp. 452-464.
51. Yerly, S., Jost, S., Monnat, M., Telenti, A., Cavassini, M., Chave, JP, Kaiser, L., Burgisser, P. and Perrin, L. (2004) HIV-1 co/super-infection in intravenous drug users. AIDS., 18, pp. 1413-1421.
52. Zhang, K., Hawken, M., Rana, F., Welte, FJ, Gartner, S., Goldsmith, MA and Power, C. (2001) Human immunodeficiency virus type 1 clade A and D neurotropism: Molecular evolution, recombination, and coreceptor use. Virology., 283, pp. 19-30.
53. Zink, MC and Clements, JE (2002) A novel simian immunodeficiency virus model that provides insight into mechanisms of human immunodeficiency virus central nervous system disease. J NeuroVirol., 8, pp. 42-48.
54. Zink, MC, Laast, VA, Helke, KL, Brice, AK, Barber, SA, Clements, JE and Mankowski, JL (2006) From mice to macaques-animal models of HIV nervous system disease. Curr HIV Res., 4, pp. 293-305.