The role of promastigote secretory gel in the origin and transmission of the infective stage of Leishmania mexicana by the sandfly Lutzomyia longipalpis

Abstract

Transmission of leishmaniasis is effected by a specific developmental stage, the metacyclic promastigote. The precursors of metacyclic promastigotes were a distinct subpopulation of parasites, identified for the first time as a new stage in the life-cycle and named leptomonad promastigotes. Microdissection of infected sandflies into 4 midgut regions and foregut allowed precursor-product relationships to be established for amastigote-procyclic promastigote, procyclic-nectomonad promastigote, nectomonad-leptomonad promastigote and leptomonad-metacyclic promastigote developmental switches. Metacyclic promastigotes occurred mainly in the thoracic midgut and cardia, coincident with the accumulation of a promastigote secretory gel (PSG) plug in these anterior regions. The gel-like plug was isolated from flies with mature infections and found to contain predominantly leptomonad promastigotes. The PSG plug also contained the majority (75 %) of the total metacyclic promastigote population in the sandflies, which were concentrated at the anterior pole. The PSG plug was found to be the main site of metacyclogenesis, and acted as a reservoir of leptomonad promastigotes from which metacyclic forms differentiated and migrated forward to promote the infective potential of the fly. The PSG plug occluded and distorted the midgut, forcing the stomodeal valve open and affecting the feeding success of the sandflies, such that they experienced difficulty in taking a full meal. Collectively, these data support the role of the PSG in the transmission of leishmaniasis, by conditioning the midgut environment for metacyclogenesis and altering the feeding ability of infected sandflies.Key words : Leishmania, sandfly, metacyclic promastigote, promastigote secretory gel (PSG), transmission. Parasites of the genus Leishmania are protozoa that occur within the phagolysosomes of the mammalian macrophages as non-flagellated amastigotes, and as motile flagellated promastigotes in phlebotomine sandflies. Infection of the sandfly begins after taking a bloodmeal from an infected host. Ingested amastigotes transform within the digesting bloodmeal and undergo development as a number of promastigote morphological forms (Killick-Kendrick, 1979). Upon engorgement the bloodmeal is encased by a peritrophic matrix, a chitinous sac formed from secretions of the midgut epithelium. Therein amastigotes transform into ovoid procyclic and long slender nectomonad forms, which initiate the growth of the infection. Towards the end of digestion of the bloodmeal the parasites escape from the peritrophic matrix to avoid expulsion during defecation, and further resist this process by attaching to the midgut microvillar border (Pimenta et al. 1992 ; Sacks et al. 1994). Subsequently, colonization of the anterior * Corresponding author : Tel : j44 151 708 9393. Fax : j44 151 708 9007. E-mail : m.e.rogers!liverpool.ac.uk regions of the midgut is accompanied by transformation to a variety of morphological forms, which include broad attached haptomonad pr...

Development of Leishmania (Leishmania) infantum chagasi in Its Natural Sandfly Vector Lutzomyia longipalpis

“…Colonization of the stomodeal valve and a gelatinous substance similar to the promastigote secretory gel described by Rogers and others 21 in Lu. longipalpis infected with L. amazonensis, a non-natural vector-parasite pair, were showing from left to right an amastigote ingested from an infective bloodmeal; a procyclic promastigote, a short, ovoid, slightly motile, first promastigote that appears in the sandfly; a nectomonad promastigote, a long slender form; a haptomonad promastigote, a shorter and broader form; a paramastigote promastigote, a rare form with the kinetoplast adjacent to the nucleus; and a metacyclic promastigote, a short, slender, highly active, infective form for the vertebrate host.…”

“…22 In contrast, there are few published data relating to New World species; for example, there are only a few studies on L. infantum chagasi and L. mexicana in Lu. longipalpis 21,23,24 and L. amazonensis and L. braziliensis in Lu. migonei and Lu.…”

“…19 Only metacyclic forms transmitted through sandfly bites are able to begin an infection in vertebrate hosts. 20,21 Studies on Leishmania-vector interactions are needed to understand the processes involved in parasite development and transmission. Much information regarding Old World Leishmania species and their vectors is available, as reviewed recently by Sacks and others.…”

Yersinia pestis Biofilm in the Flea Vector and Its Role in the Transmission of Plague

“…The phytopathogen Xylella fastidiosa forms a biofilm of polarly attached cells in the foregut of its vectors, which are sap-feeding insects in the leafhopper family (Newman et al 2004;Purcell et al 1979); and transmission of Leishmania depends on blockage of the anterior midgut of the sandfly vector by parasites embedded in a polysaccharide-containing secretory gel. (Rogers et al 2002;Stierhof et al 1999). The body of evidence that has accumulated in support of the biofilm model of plague transmission is presented in the following sections.…”

Quantification of the infectious dose ofLeishmania majortransmitted to the skin by single sand flies

“…The lumen is also packed with parasites embedded in a parasite-derived matrix, the promastigote secretary gel (PSG) (3). Many of these cells are the metacyclic forms that are preadapted to survival in a subsequent mammalian host and are therefore considered the infective form (4,5).…”