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(Viannia\) Utingensis N . Sp., a Parasite from the Sandfly Lutzomyia

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(Viannia\) Utingensis N . Sp., a Parasite from the Sandfly Lutzomyia Article available at http://www.parasite-journal.org or http://dx.doi.org/10.1051/parasite/2003102111 Le is h m a n ia (V ia n n ia ) u t in g e n s is n . sp., A PARASITE FROM THE SANDFLY LUTZOMYIA (V lANNAMYlA) TUBERCULATA in A m a z o n ia n B r a zil BRAGA R.R.*, LAINSON R.*, ISHIKAWA EA.Y.* & SHAW J.J.** Summary: R ésum é : Leish m a n ia (V iannia) u tin g en sis n . s p ., pa ra site d u P h l é b o t o m e L utzo m yia (V ia n n ia m yia ) tuberculata e n A m a zo n ie A leishmanial parasite isolated in 1977 from a specimen of the BRÉSILIENNE sandfly Lutzomyia tuberculata from Para State, Amazonian Brazil, has been characterized following its comparison with other Une Leishmanie isolée en 1977 d'un spécimen d e Lutzomyia tuberculata species of Leishmania from the same region, using isoenzyme d e l'état d e Pará , Amazonie brésilienne, est profiles, monoclonal antibodies and characterization of the mini­ diffe renciée des autres espèces d e Leishmania d e la même région exon gene repeat, using the polymerase chain reaction technique par les profils enzymatiques, les anti-corps monoclonaux et la (PCR). It is described here under the name of Leishmania {Viannia) caractérisation, par PCR, des mini-exons répétés dans les gènes. utingensis n. sp. Elle est nommée Leishmania (Viannia) utingensis n. sp. KEY WORDS : Leishmania (Viannia) utingensis n. sp., Lutzomyia tuberculata, MOTS CLÉS : Leishmania (Viannia) utingensis n. s p., Lutzomyia tuberculata, sandflies, Brazil. phlébotome, Brésil. INTRODUCTION MATERIALS AND METHODS n 1977 a leishmanial parasite was isolated from a M o r p h o l o g y o f amastigotes a n d promastigotes single specimen of the phlebotomine sandfly, Lut­ Izomyia (Viannamyia) tuberculata (Mangabeira) ollowing retrieval of the parasite (Register Num­ (Fig. 1), taken from the trunk of a large tree in Utinga ber M4964) from our cryobank, it was maintained forest on the outskirts of Belém, Para State, Amazo­ Fin Diffco B45 blood-agar culture medium (Walton nian Brazil. Initially thought to possibly be et al., 1977) and the skin of hamsters inoculated intra- L. (Viannia) braziliensis (Lainson & Shaw, 1979), it dermally with promastigotes into the dorsal surface of was later listed among the “unnamed parasites of the the hind feet. subgenus Viannia" by virtue of its peripylarian deve­ For amastigotes, animals were sacrificed eight days post lopment in the sandfly host, morphology, and beha­ inoculation (d.p.i.) and impression smears made from viour in hamsters and in vitro culture (Lainson & the skin excised from the point of inoculation. Prepa­ Shaw, 1987). In the present paper, we give a more rations were air-dried, fixed in aqueous Bouin’s fluid complete description of the organism and show it to for 20 minutes, and washed repeatedly in 70 % ethyl differ from all those species of Leishm ania previously alcohol until colourless. The smears were then stained recorded in the Amazon Region of Brazil, following for one hour by Giemsa’s method, differentiated in a characterization of the mini-exon gene repeat, using graded series of acetone-xylol mixtures and mounted the polymerase chain reaction technique (PCR), isoen­ under a cover-slip in “Permount”®. zyme electrophoresis profiles, and monoclonal anti­ Promastigotes of 7-day-old cultures were washed twice bodies (McAbs). by centrifugation in pH 7.2 phosphate buffered saline (PBS) and the sediment used to prepare thin smears. These were air-dried, fixed in absolute methyl alcohol and stained by Giemsa’s method. Measurements of 50 amastigotes and 40 promastigotes were made using * Departamento de Parasitologia, Instituto Evandro Chagas, Av. the oil immersion lens, x 10 oculars and an eyepiece Almirante Barroso 492, 66090-000 Belém, Pará, Brazil. ** Departamento de Parasitologia, Instituto de Ciencias Biomédicas, micrometer. All measurements are in pm and given as Universidade de Sao Paulo, Av. Lineu Prestes 1374, 05508-900 Sao means, followed by the standard deviation and the Paulo, Brazil. range in parentheses. Photomicrographs were pre­ Correspondence: Ralph Lainson. pared using a Zeiss “Photomicroscope III” and Kodak Tel: +55 91 211 4453 - Fax: +55 91 226 1284. E-mail: [email protected] TMX 100 film. Parasite, 2003, 10, 111-118 Mémoire 111 BRAGA R.R., LAINSON R„ ISHIKAWA E.A.Y. & SHAW J.J. Fig. 1. — Lutzomyia (Viannamyia) tubercu- lata. Freshly dissected female genitalia (sper- mathecae). Bar = 0.05 mm. P o l y m e r a s e c h a in r e a c t io n (McMahon Pratt et al., 1986; Hanham et al., 1991). They were used together with the indirect immunofluores­ The oligonucleotides used in the PCR were with the cence/fluorescein-labelled avidin technique (Shaw et al., following sequences (Fernandes et al., 1994): S 1629:5'- 1989). GGG-AAT-TCA-ATA-TAG-TAC-AGA-AAC-TG-3' and S 1630:5'-GGG-AAG-CTT-CTG-TAC-TTT-ATT-GGT-A-3'. E xperimental in f e c t io n s Agarose gel (1 %) electrophoresis of mini-exon PCR in l a b o r a t o r y - b r e d s a n d f l ie s amplification products and a molecular weight marker (ΦX 174 DNA/Hae III) were visualized following stai­ Using the membrane-feeding technique of Ward et al. ning with ethidium bromide. A negative control, with (1978), culture forms of both M4964 and L. (V.) brazi­ no added DNA, was included. liensis (M 2903) were separately fed to laboratory-bred Lutzomyia (Lutzomyia) longipalpis and Lutzomyia (Vian­ E n z y m e electrophoresis namyia) furcata. The sandflies were dissected five days later, when all the ingested blood had been digested. We used the enzymes ASAT, ALAT, PGM, GPI, MPI, G6PD, MDH, ACON, PEP and 6PGDH (for methods and abbreviations, see Miles et al., 1980), and the pro­ RESULTS files of isolate M4964 were compared with those of L. (V.) braziliensis (MHOM/BR/1975/M2903) from Serra dos Carajas, Para; L. (V.) braziliensis sensu lato (MHOM/ B e h a v io u r in c u l t u r e m e d iu m BR/1975/M2904) also from Serra dos Carajas; L. (V.) rowth of the parasite is rapid, with the pro­ guyanensis(MHOM/BR/1975/M4l47) from Monte Dou- duction of abundant, large rosettes of dividing rado, Para; L. (V.) lainsoni (MHOM/BR/1981/M6426) forms. The separate flagellates are small and from Benevides, Para; L. (V.) naiffi (MDAS/BR/ G extremely active - a characteristic of most of the species 1979/M5533) from Monte Dourado, Para; L. (V.)shawi within the subgenus Viannia (Lainson & Shaw, 1987). (MCEB/BR/1984/M8408) from Parauapebas, Para; L. (Leish- mania) amazonensis(IFLA/BR/l967/PH8) from Utinga B e h a v io u r in t h e s k in o f h a m s t e r s Forest, Belem, Para; and L. infantum chagasi (MCER/ Following the intradermal inoculation of enormous BR/1981/M6445) from Salvaterra, Marajó island, Pará. numbers of log-phase promastigotes, only a small number of free and intracellular amastigotes could be M o n o c l o n a l a n t ib o d ie s detected in the stained smears of skin excised from the The isolate was tested with 23 McAbs prepared against site of inoculation eight days p.i. No visible skin lesion the above-listed Leishmania (Viannia) species respon­ could be detected up to two months p.i., when para­ sible for cutaneous leishmaniasis in the Amazon Region sites were encountered with great difficulty: in this res­ of Brazil and neighbouring parts of South America pect the parasite resembles L. (V.) naiffi (Lainson & Parasite, 2003, 10, 111-118 112 Mémoire Leishmania u t in g è îsis n . s p . in L it z o m y ia w ber cu la ta Fig. 2. - Leishmania (Viannia) utingensis n. sp. Intracellular and free amastigotes in the skin of a hamster inoculated eight days pre­ viously with promastigotes. a-f. Division stages: one parasite (f), shows the conspicuous fla­ gellar vacuoles of the two daughter amasti­ gotes which are on the point of separation, g- k. Smaller products of division. Bouin fixation, Giemsa staining. Bar = 10.0 pm. Fig. 3. - Leishmania (Viannia) utingensis n. sp. Log-phase promastigotes from an 8-day culture in Diffco B45 blood-agar medium, a- b. Dividing forms, c-f. Small, non-dividing fla­ gellates. Methyl alcohol fixation, Giemsa stai­ ning. Bar = 10.0 pm. Parasite, 2003, 10, 111-118 Mémoire 113 BRAGA R.R., LAINSON R., ISHIKAWA E.A.Y. & SHAW J.J. Shaw, 1989; Lainson et al., 1990) and the newly des­ subgenus Viannia, and differentiates it from the two cribed L. (V.) lindenbergi ( Silveira et a l, 2002). representatives of the subgenus Leishm ania examined, Leishmania infantum chagasi and L. (L.) amazonensis. M orphology o f amastigotes and promastigotes Among species of the subgenus Viannia, the parasite (Figs 2 and 3) could be separated from L. (V.) lainsoni, but not from L. (V.) braziliensis, L. (V.) guyanensis, L. (V.) naiffi, and Mean measurement of amastigotes was 3.0 ± 0.7 x 2.1 L. (V.) shawi. ± 0.3 (2.2-4.0 x 1.5-2.2), n = 50. The parasite shows no morphological features by which to differentiate it Isoenzyme profiles (Fig. 5) from most of the species in the subgenus Viannia, with which it shares the characteristic of very small, com­ Shaw et al.
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