Pulmonary infections in swine induce altered porcine surfactant protein D expression and localization to dendritic cells in bronchial‐associated lymphoid tissue

Abstract

SummarySurfactant protein D (SP-D) is a pattern-recognition molecule of the innate immune system that recognizes various microbial surface-specific carbohydrate and lipid patterns. In vitro data has suggested that this binding may lead to increased microbial association with macrophages and dendritic cells. The aim of the present in vivo study was to study the expression of porcine SP-D (pSP-D) in the lung during different pulmonary bacterial infections, and the effect of the routes of infection on this expression was elucidated. Furthermore, the aim was to study the in vivo spatial relationship among pSP-D, pathogens, phagocytic cells and dendritic cells. Lung tissue was collected from experimental and natural bronchopneumonias caused by Actinobacillus pleuropneumoniae or Staphylococcus aureus, and from embolic and diffuse interstitial pneumonia, caused by Staph. aureus or Arcanobacterium pyogenes and Streptococcus suis serotype 2, respectively. By comparing normal and diseased lung tissue from the same lungs, increased diffuse pSP-D immunoreactivity was seen in the surfactant in both acute and chronic bronchopneumonias, while such increased expression of pSP-D was generally not present in the interstitial pneumonias. Co-localization of pSP-D, alveolar macrophages and bacteria was demonstrated, and pSP-D showed a patchy distribution on the membranes of alveolar macrophages. SP-D immunoreactivity was intracellular in dendritic cells. The dendritic cells were identified by their morphology, the absence of macrophage marker immunoreactivity and the presence of dendritic cell marker immunoreactivity. Increased expression of pSP-D in the surfactant coincided with presence of pSP-D-positive dendritic cells in bronchus-associated lymphoid tissue (BALT), indicating a possible transport of pSP-D through the specialized M cells overlying (BALT). In conclusion, we have shown that pSP-D expression in the lung surfactant is induced by bacterial infection by an aerogenous route rather than by a haematogenous route, and that the protein interacts specifically with alveolar macrophages and with dendritic cells in microbial-induced BALT. The function of the interaction between pSP-D and dendritic cells in BALT remain unclear, but pSP-D could represent a link between the innate and adaptive immune system, facilitating the bacterial antigen presentation by dendritic cells in BALT.

Development of Enzyme-Linked Immunosorbent Assay for Bovine Surfactant Protein D in Bronchoalveolar Lavage Fluid

“…Similar observations in bacterial pneumonia have been reported by several authors [25,27]. Extracellular SP-D content is increased after tracheal inoculation with extraintestinal E. coli (CP9) [25].…”

“…Extracellular SP-D content is increased after tracheal inoculation with extraintestinal E. coli (CP9) [25]. Increased diffuse porcine SP-D is observed immunohistologically in the surfactant in acute bronchopneumonias caused by A. pleuropneumoniae and Staphylococcus aureus [27]. McIntosh et al demonstrated that SP-D mRNA expression and SP-D protein in BALF were significantly elevated in rats that received intratracheal lipopolysaccharide, which is a component of Gram-negative bacteria [22].…”

“…Long transport stress decreases the SP-A and SP-D contents of equine surfactant [12]. The immunoreactivity of SP-D varies during pneumonia induced by bacterial or viral inoculation in various species [6,7,22,25,27]. Since SP-D has a pivotal role in innate defense, quantitative measurement of SP-D in BALF would provide useful information on the pulmonary host defense mechanisms.…”

“…SP-D has a role in the regulation of surfactant lipid metabolism [14]; however, it has been emphasized that SP-D is an important molecule in innate immune defense, like the other collectins [18,26]. SP-D binds or agglutinates a broad range of pathogenic microorganisms, including bacteria, viruses, fungi, and yeasts, mediated by the CRD regions in the molecule [18] [6,7,22,25,27]. Since SP-D has a pivotal role in innate defense, quantitative measurement of SP-D in BALF would provide useful information on the pulmonary host defense mechanisms.…”

Glycoprotein analysis of porcine bronchoalveolar lavage fluid reveals potential biomarkers corresponding to resistance toActinobacillus pleuropneumoniaeinfection

“…Expression of pulmonary surfactant protein D (SP-D) was shown as increased during acute and chronic Actinobacillus pleuropneumoniae infection. In that context it was assumed that SP-D could represent a link between the innate and adaptive immune system, facilitating bacterial antigen presentation by dendritic cells in bronchus-associated lymphoid tissue [44].…”