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| Sl No | Author year | Cells or tissue and the viral strain used | Viral strain | Conclusion
Apoptosis present or not, if so which cells |
|
| (1) | Adle-Biassette et al., 1996 [15] | Human tissue | Street virus | Apoptotic neurons identified in the brain stem and hippocampus in the vicinity of inflammatory foci but not in noninflammatory areas |
| (2) | Jackson and Rossiter, 1997 [12] | Cultured rat prostatic adenocarcinoma (AT3) cells
Adult ICR mice inoculated intracerebrally with CVS | Challenge virus standard (CVS) strain of fixed rabies virus | Cultured rat prostatic adenocarcinoma (AT3) cells showed apoptosis (DNA laddering and Bax protein expression). Adult ICR mice showed apoptosis in neurons of hippocampus and cerebral cortex. Apoptosis plays an important role in the pathogenesis of rabies virus infection |
| (3) | Thoulouze et al., 1997 [33] | Activated murine lymphocytes and the human lymphoblastoid Jurkat T-cell lines | Challenge virus standard (CVS) and attenuated strain ERA | (i) Rabies virus infects lymphocytes, (ii) lymphocyte infection with the attenuated ERA rabies virus strain causes apoptosis but not with CVS, and (iii) apoptosis does not hinder rabies virus production. Apoptosis of infected Jurkat T cells was concomitant with viral glycoprotein expression, suggesting that this protein has a role in the induction of apoptosis |
| (4) | Ubol et al., 1998 [34] | Neuroblastoma cell line | CVS 11 | Apoptosis present (DNA laddering, TUNEL, caspase 1, Bax) |
| (5) | Jackson and Park, 1998 [35] | Suckling mice (6-day-old ICR mice) | Challenge virus standard (CVS) strain of fixed rabies virus, intracerebral inoculation | Widespread neuronal apoptosis (TUNEL staining, increased Bax expression) in hippocampus and cerebral cortex, in rabies-virus-infected neurons. Apoptosis was more in suckling mice than in adult mice, explaining the greater neurovirulence of rabies virus in younger mice |
| (6) |
Theerasurakarn and Ubol, 1998 [36] | Suckling mouse brain | CVS 11 | Apoptosis detected in neurons (TUNEL, DNA fragmentation) and is the earliest death mechanism detected in these mice |
| (7) | Jackson, 1999 [39] | Five- to 7-day-old bax-deficient mice and their wild-type littermates | CVS or the RV194-2 variant of rabies virus inoculated intracerebrally | Apoptosis was less severe in the cerebral cortex, hippocampus, and cerebellum of the bax-deficient mice compared to wild-type mice |
| (8) |
Jackson and Park, 1999 [41] | 6-day-old p75 neurotrophin receptor-deficient mice and wild-type mice | CVS (Challenge virus standard strain) of fixed rabies virus inoculated intracerebrally | Widespread apoptosis in brain (TUNEL stain) |
| (9) | Ubol and Kasisith, 2000 [37] | Adult and suckling mice | Bat strain and a primary canine rabies virus | Expression of Nedd-2 correlated with the appearance of apoptotic nuclei within the brain. Apoptosis required for elimination of virally infected cells |
| (10) | Reid and Jackson, 2001 [13] | Fruit eating adult bats (Artibeus jamaicensis ) | CVS-N2c and CVS-B2c (stable variants of CVS-24), inoculated into the right masseter muscle | Apoptosis (DNA fragmentation) not observed in rabies infected neurons with either virus strain |
| (11) | Yan et al., 2001 [14] | Mice | Street rabies virus (silver-haired bat rabies virus, SHBRV) and mouse-adapted laboratory rabies virus strain (CVS-24) | Apoptosis (TUNEL staining) was observed in the brain with CVS-24-infected mice but not SHBRV infected mice. Apoptosis is not an essential pathogenic mechanism for the outcome of street rabies virus infection |
| (12) | Rutherford and Jackson, 2004 [40] | Immunodeficient adult C57BL/6J mice with nude mice (T-cell deficient) and Rag1 mice (T- and B- cell deficient) | Challenge virus standard-11 strain (CVS), intracerebral inoculation | Neuronal apoptosis prominent in immunodeficient mice |
| (13) | Juntrakul et al., 2005 [49] | Brain and spinal cord of 10 rabies patients | Street virus | Apoptosis present and correlated with the presence of rabies virus antigen |
| (14) | Sarmento et al., 2005 [45] | ICR Mice (4–6 weeks) | Recombinant RVs with replacement of G gene, and wild-type virus (SHRBV), intracerebral route and intramuscular route | With attenuated RV (IC or IM route), mice showed prominent inflammation and apoptosis and inversely correlated with G protein. With wild-type virus inoculated by IC or IM route, apoptosis was minimal. Glycoprotein-mediated induction of apoptosis limits the spread of attenuated rabies viruses in the central nervous system of mice |
| (15) | Ubol et al., 2005 [38] | Neonatal mice | Street virus, intracerebral inoculation | Proapoptotic genes upregulated |
| (16) | Jackson et al., 2006 [48] | Two-day-old ICR mice inoculated in a hindlimb thigh muscle | Recombinant rabies virus vaccine strain SAD-L16 (L16) or SAD-D29 (D29), which contains an attenuating substitution of Arg333 in the rabies virus glycoprotein | Less virulent virus was a stronger inducer of neuronal apoptosis |
| (17) | Weli et al., 2006 [11] | Cultures derived from the cerebral cortices and hippocampi of 17-day-old mouse fetuses | CVS strain of rabies virus | Apoptotic features and activated caspase 3 expression in cultures. Caspase inhibitors were neuroprotective |
| (18) | Scott et al., 2008 [42] | Six-week-old mice | CVS strain of fixed virus inoculated in the hindlimb footpad | Few apoptotic cells in the cerebral cortex and hippocampus. (TUNEL labeling and caspase-3 immunostaining) |
| (19) | Jackson et al., 2008 [16] | 12 cases of human rabies (four different countries) | Street virus | No evidence of neuronal apoptosis (TUNEL staining) in cerebral cortex, hippocampus, and brainstem. Caspase-3 immunostaining was absent in neurons, but observed in microglial processes |
| (20) | Suja et al., 2009 [17] | 10 canine brains | Street virus | No neuronal apoptosis (DNA laddering) |
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