1.3 Canine distemper virus
1.3.4 Cell tropism and viral receptors
The tropism of morbillivirus-infectable cells has been correlated to the presence of both well known and unidentified cellular receptors. SLAM, a membrane glycoprotein, is a well known specific morbillivirus receptor expressed on a variety of different lymphoid cell subpopulations, including immature thymocytes, primary B cells, activated T cells, memory T cells, macrophages and mature dendritic cells (Kruse et al., 2001; Ostrakhovitch and Li, 2006). The distribution of SLAM-presenting cells is in accordance with the lymphotropism
and immunosuppression following morbillivirus infection (Schneider-Schaulies and Schneider-Schaulies, 2008; Tatsuo and Yanagi, 2002; Tatsuo et al., 2001; Wenzlow et al., 2007). SLAM acts as an efficient receptor for vaccine and field strains/clinical isolates of morbillivirus (Tatsuo et al., 2000). However, laboratory virus strains infect well known target cells, such as epithelial, endothelial and neuronal cells via a SLAM-independent mechanism as shown by the lack of cellular SLAM receptor expression (Andres et al., 2003; Wenzlow et al., 2007). CD46, a membrane cofactor protein (MCP) or a complement regulatory molecule, represents a primate-specific receptor for the laboratory-adapted Edmonston strain of MV which is expressed on all human cells except erythrocytes (Dörig et al., 1993, 1994). CD9, a tetraspan transmembrane protein, plays a role in a variety of physiological conditions; such as cell adhesion, motility, activation and proliferation, as well as during pathological conditions, including tumor metastases or viral infection. CD9 was found in the myelin and in exosomes of dendritic cells (Bronstein, 2000; Charrin et al., 2001). CD9 is considered an essential factor for CDV uptake by target cells, cell-cell (but not virus-cell) syncytial cell formation and the production of progeny virus (Löffler et al., 1997; Schmid et al., 2000). In addition, an unidentified epithelial cell receptor (EpR) located on the basolateral side of epithelial cell has been reported as a tight junction-related molecule to facilitate viral transmission directly to the airway lumen and to disseminate the pathogen without initial infection of the respiratory epithelium (Leonard et al., 2008; Tahara et al., 2008).
Within the CNS, astrocytes, microglia, oligodendrocytes, neurons, ependymal cells and choroid plexus epithelial cells have been documented as CDV target cells (Alldinger et al., 1993; Seehusen et al., 2007; Stein et al., 2006). Studies of in vivo and in vitro infection revealed differential susceptibility of various glial cell types to specific CDV strains.
Astrocytes represent the first cell target of CDV following CNS infection and play a role for virus persistence and replication leading to chronic demyelinating lesions in the CNS (Headley et al., 2001; Mutinelli et al., 1989; Pearce-Kelling et al., 1990). Recently, Seehusen et al. (2007) demonstrated CDV infection in situ of GFAP+ astrocytes in acute distemper lesions, while vimentin+ astrocyte-like cells were targeted in chronic demyelinating disease.
This finding suggests a change of cell tropism and/or susceptibility of glial cells during disease progression in DL. Subsequently, in vitro experiments using mixed adult canine brain cell cultures demonstrated the differential susceptibility of glial cells following infection with the CDV-R252 strain. The dominant cytopathic effect (CPE) noted in infected GFAP+ astrocytes, especially in the multinucleated syncytial cells, consisted of a ruptured cytoskeleton, whereas vimentin+ cells displayed no change in the filament network. The in vitro findings support a role of immature astrocytes for virus persistence and spread in advanced DL lesions (Seehusen et al., 2007).
Focusing on CDV strain-specific CNS lesions, the virulent CDV Snyder Hill (CDV-SH) strain initiated an acute encephalitis with predominantly induced gray matter lesions, while the demyelinating CDV-A75-17 and CDV-R252 strains resulted in a chronic encephalitis that more strikingly affected the white matter (Summers et al., 1984). In cultures of neonatal dog brains, the attenuated CDV Rockborn (CDV-RO) and the virulent CDV-SH strains rapidly replicated in various cell types, including neurons, astrocytes, bipolar oligodendrocytes and macrophages by 14dpi. Contrary to this, infection with the CDV-A75-17 strain did not affect neurons and replication was delayed until after 28-35dpi. In addition, multipolar oligodendrocytes were rarely infected by any of the virus strains (Pearce-Kelling et al., 1990, 1991). Similarly, the CPE characteristics also differed between different CDV strains. Both CDV-SH and CDV-A75-17 strains induced a non-cytolytic infection whereas CDV-RO caused a cytolysis of infected astrocytes (Pearce-Kelling et al., 1990).
Previously, CDV-mediated demyelination was thought to be caused by a selective infection of myelin-forming oligodendrocytes that leads to morphological changes, metabolic impairment and complete disappearance of oligodendrocytes in demyelinating lesions (Blakemore et al., 1989; Glaus et al., 1990; Summers and Appel, 1987). Although a down-regulation of myelin gene transcription was observed before demyelination occurred; the number of oligodendrocytes was not decreased until demyelination became evident and they remained presented in a significant amount even in chronic, completely demyelinated distemper lesions. These findings suggest that demyelination precedes oligodendrocyte loss (Schobesberger et al., 1999, 2002).
Besides astrocytes and oligodendrocytes that represent pivotal factors in the pathogenesis of distemper demyelination, microglia and peripheral macrophages invading the CNS during the course of the inflammatory response also play an important role in the demyelinating process (Stein et al., 2004; Vandevelde and Zurbriggen, 2005). In vivo and in vitro studies showed a significant upregulation of certain surface molecules, such as CD1c, B7-1, B7-2, MHC I and CD11b, in microglia and peripheral blood monocytes following CDV infection (Stein et al., 2004, 2008). All these molecules play a key role in the host´s immune response, notably antigen presentation and cell adhesion. Therefore, these findings suggest an enhancement of macrophage functions which may facilitate the entry of peripheral monocytes in the CNS leading to effective clearance of the virus but may also increase demyelination via a bystander effect (Stein et al., 2008).
Recently, the infection of the attenuated CDV-Onderstepoort strain expressing the green fluorescent protein (CDV-OndeGFP) and CDV-R252 strain has been investigated in mixed adult canine brain cultures. Infection with the CDV-R252 strain resulted in a preferential affect in microglia and astrocytes compared to CDV-OndeGFP strain. Following infection, a
bipolar spindle-shaped Schwann cell-like population designated presently “Schwann cell-like brain glia (SCBG)” was observed. These cells displayed a high susceptibility to attenuated CDV strains as early as 3dpi (Orlando et al., 2008). So far there are no data available on CDV infection of p75NTR-expressing SCBG in vivo.
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