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.
Highlights
Gastropod hemocytes recognize and phagocytize invaders, entrap them through nodulation (Sminia, 1981) and/or they encapsulate foreign objects too large to be engulfed (Godoy et al, 1997; Lemos & Andrade, 2001; Lv et al, 2009b; Sminia, Borghart-Reinders & Van de Linde, 1974; Van der Knaap, Adema & Sminia, 1993; Yousif, Blähser & Lämmler, 1980)
Knowledge on the immune system of Pomacea canaliculata (Lamarck 1822, Ampullariidae) is becoming increasingly important, because of the role of this species as an intermediate host and vector of the nematode Angiostrongylus cantonensis (Chen 1935, Metastrongylidae), the major etiologic agent of eosinophilic meningitis, a parasitic disease that can be disabling in humans, and may be even fatal (Cowie, 2017; Martins, Tanowitz & Kazacos, 2015)
While P. canaliculata, a native of the lower Río de la Plata basin, has invaded China, A. cantonensis is present in Brazil (Morassutti et al, 2014; Thiengo et al, 2013; Valente et al, 2018), i.e., on the verge to overlap the native range of P. canaliculata, which would facilitate the spread of the parasite
Summary
Gastropod hemocytes recognize and phagocytize invaders, entrap them through nodulation (Sminia, 1981) and/or they encapsulate foreign objects too large to be engulfed (Godoy et al, 1997; Lemos & Andrade, 2001; Lv et al, 2009b; Sminia, Borghart-Reinders & Van de Linde, 1974; Van der Knaap, Adema & Sminia, 1993; Yousif, Blähser & Lämmler, 1980). Knowledge on the immune system of Pomacea canaliculata (Lamarck 1822, Ampullariidae) is becoming increasingly important, because of the role of this species as an intermediate host and vector of the nematode Angiostrongylus cantonensis (Chen 1935, Metastrongylidae), the major etiologic agent of eosinophilic meningitis, a parasitic disease that can be disabling in humans, and may be even fatal (Cowie, 2017; Martins, Tanowitz & Kazacos, 2015). Hemocyte-antigen encounters may occur in the systemic blood circulation, but we hypothesized that there are organs acting as immune barriers, whose characteristics may facilitate these encounters. Such characteristics would be: (1) an adequate position of the organ in blood circulation, so as to prevent antigen dissemination, and/or (2) an intricate microcirculation, which would increase the probability of hemocyte-antigen contacts, and/or (3) a locally high hemocyte concentration. The Ampullariidae are part of the clade Caenogastropoda, which encompasses about 60% of extant gastropod species, and gastropod immunobiology may be biased because it is based on just a few families of Panpulmonata (Heterobranchia), i.e., on a small segment of gastropod diversity (Loker, 2010)
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