Assessment of the kidney and lung as immune barriers and hematopoietic sites in the invasive apple snail Pomacea canaliculata

Abstract

Knowledge on the immune system of Pomacea canaliculata is becoming increasingly important, because of this gastropod’s role as intermediate host and vector of Angiostrongylus cantonensis, the etiologic agent of eosinophilic meningitis in humans and domestic animals. Immune defenses of this gastropod comprise both humoral and cellular components, but they may also involve organs that act as immune barriers to prevent the spread of alien molecules and organisms. Both the kidney and lung are here shown to serve this function, because of (1) their positions in blood circulation, (2) the intricate architecture of their blood spaces, and (3) the proliferative and nodulation reactions of hemocytes to an immune challenge. However, these organs differ in that only the kidney shows permanent hemocyte aggregations. Microcirculation in the kidney was found to flow through an intricate vascular bed containing the permanent aggregations, which occurred either as hemocyte islets anchored by cytoplasmic projections of the renal epithelium or as perivascular accretions. Within 96 h of the injection of yeast cells, hemocyte nodules were formed both in the kidney and lung. Moreover, cell proliferation in renal hemocyte islets was measured by bromodeoxyuridine (BrdU) incorporation. The proportion of BrdU positive nuclei increased 48 h after injection. Signs of nodule regression (apoptotic bodies, lipofuscin-like deposits) and a decrease in the proportion of BrdU positive nuclei were found at 96 h. In addition, the area of renal hemocyte islets was significantly increased 96 h after injection. Nevertheless, the high complexity of the small vascular chambers that constitute the lung’s respiratory lamina would also facilitate hemocyte-antigen contacts, required to elicit cellular aggregation, and hence, nodulation. To our knowledge, this paper includes the first quantitative indication of hemocyte proliferation after an immune challenge among Caenogastropoda.

The Immune Response of the Invasive Golden Apple Snail to a Nematode-Based Molluscicide Involves Different Organs

“…Our data collected after P. hermaphrodita infection are in line with the organ-specific immune response in P. canaliculata, highlighting, in this case, the involvement of the anterior kidney and the gills, organs that have been reported as main players of the apple snail immune response [8,9] and that express genes involved in xenobiotic metabolism and cell growth [1]. Accordingly, a close connection between the anterior kidney and the gills has been described, both in terms of anatomical proximity and blood (i.e., hemolymph) flux [10]. In this context, we observed that circulating hemocytes can display a basal expression of Pc-bpi.…”

“…In this context, we observed that circulating hemocytes can display a basal expression of Pc-bpi. The absence of specific hemocyte markers does not allow to conclude if the levels of expression we registered by qPCR in control animals can be attributed to resident or circulating hemocytes patrolling those organs [6,9,10]. However, in the absence of univocal hemocyte markers [16], it cannot be ruled out that the changes we observed in the anterior kidney and the gills might be also due to changes occurring in the resident hemocyte population [6,9,10].…”

“…The organs we have chosen for this study are characterized by a basal level of expression of Pc-bpi ( Figure 6) and can be patrolled by resident or circulating hemocytes [6,9,10]. Therefore, we sought to address expression of Pc-bpi in circulating hemocytes using FISH.…”

“…Beside circulating hemocytes, other resident hemocytes or hemocyte-like cells have been described in the ampulla, a saccular organ positioned along the main circulatory flux [7,8] and in the posterior kidney [9]. In P. canaliculata and other gastropods, the presence of granular hemocytes and/or immune-related functions have also been identified in the anterior kidney [8], the gills [10], the mantle [8,11], and the pedal ganglia [12]. Like for other freshwater snails, P. canaliculata hematopoiesis takes place in the pericardial cavity, which contains replicating cells with a morphology similar to that of circulating hemocytes [7].…”

Peer Review #1 of "Functional and evolutionary perspectives on gill structures of an obligate air-breathing, aquatic snail (v0.1)"

“…However, the gill is also a potential barrier because of its position in the circulation, as are the kidney and lung in P. canaliculata (Rodriguez et al 2018). Indeed, most blood coming from the cephalopodal mass and the visceral hump has to pass through the gill before reaching the heart to re-enter the general circulation.…”