Axenic interspecies and intraclonal hybrid formation in Leishmania: Successful crossings between visceral and cutaneous strains

Diseases caused by trypanosomatids are serious public health concerns in low-income endemic countries. Leishmaniasis is presented in two main clinical forms, visceral leishmaniasis—caused by L . infantum and L . donovani —and cutaneous leishmaniasis—caused by many species, including L . major , L ....

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Published inPLoS neglected tropical diseases Vol. 16; no. 2; p. e0010170
Main Authors Gutiérrez-Corbo, Camino, Domínguez-Asenjo, Bárbara, Pérez-Pertejo, Yolanda, García-Estrada, Carlos, Bello, Felio J, Balaña-Fouce, Rafael, Reguera, Rosa M.
Format Journal Article
LanguageEnglish
Published United States Public Library of Science 01.02.2022
Public Library of Science (PLoS)
Subjects
Analysis
Animals
Antibiotic resistance
Antibiotics
Biology and Life Sciences
Cell Line
Cells
Chromosomes
Cutaneous leishmaniasis
Deoxyribonucleic acid
Disease resistance
DNA
Drug resistance
Experiments
Feasibility studies
Fluorescence
Genes
Genetic aspects
Germfree
Growth
Heredity
Hybridization, Genetic
Hybrids
Immune system
Immunity
Laboratories
Leishmania
Leishmania donovani - genetics
Leishmania major - genetics
Leishmania tropica - genetics
Leishmaniasis, Cutaneous - parasitology
Leishmaniasis, Visceral - parasitology
Medicine and Health Sciences
Mitochondrial DNA
Parasites
Parasitic diseases
Phenotypes
Ploidy
Promastigotes
Psychodidae
Public health
Reproduction
Reproduction (biology)
Reproductive behaviour
Research and Analysis Methods
Sexual reproduction
Species
Strains
Tropical diseases
Tropism
Tropisms
Varieties
Vector-borne diseases
Virulence
Visceral leishmaniasis
Colombia
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Abstract Diseases caused by trypanosomatids are serious public health concerns in low-income endemic countries. Leishmaniasis is presented in two main clinical forms, visceral leishmaniasis—caused by L . infantum and L . donovani —and cutaneous leishmaniasis—caused by many species, including L . major , L . tropica and L . braziliensis . As for certain other trypanosomatids, sexual reproduction has been confirmed in these parasites, and formation of hybrids can contribute to virulence, drug resistance or adaptation to the host immune system. In the present work, the capability of intraclonal and interspecies genetic exchange has been investigated using three parental strains: L . donovani , L . tropica and L . major , which have been engineered to express different fluorescent proteins and antibiotic resistance markers in order to facilitate the phenotypic selection of hybrid parasites after mating events. Stationary and exponential-phase promastigotes of each species were used, in in vitro experiments , some of them containing LULO cells (an embryonic cell line derived from Lutzomyia longipalpis ). Several intraclonal hybrids were obtained with L . tropica as crossing progenitor, but not with L . donovani or L . major . In interspecies crossings, three L . donovani x L . major hybrids and two L . donovani x L . tropica hybrids were isolated, thereby demonstrating the feasibility to obtain in vitro hybrids of parental lines causing different tropism of leishmaniasis. Ploidy analysis revealed an increase in DNA content in all hybrids compared to the parental strains, and nuclear analysis showed that interspecies hybrids are complete hybrids, i.e. each of them showing at least one chromosomal set from each parental. Regarding kDNA inheritance, discrepancies were observed between maxi and minicircle heritage. Finally, phenotypic studies showed either intermediate phenotypes in terms of growth profiles, or a decreased in vitro infection capacity compared to the parental cells. To the best of our knowledge, this is the first time that in vitro interspecies outcrossing has been demonstrated between Leishmania species with different tropism, thus contributing to shed light on the mechanisms underlying sexual reproduction in these parasites.
AbstractList Diseases caused by trypanosomatids are serious public health concerns in low-income endemic countries. Leishmaniasis is presented in two main clinical forms, visceral leishmaniasis—caused by L . infantum and L . donovani —and cutaneous leishmaniasis—caused by many species, including L . major , L . tropica and L . braziliensis . As for certain other trypanosomatids, sexual reproduction has been confirmed in these parasites, and formation of hybrids can contribute to virulence, drug resistance or adaptation to the host immune system. In the present work, the capability of intraclonal and interspecies genetic exchange has been investigated using three parental strains: L . donovani , L . tropica and L . major , which have been engineered to express different fluorescent proteins and antibiotic resistance markers in order to facilitate the phenotypic selection of hybrid parasites after mating events. Stationary and exponential-phase promastigotes of each species were used, in in vitro experiments , some of them containing LULO cells (an embryonic cell line derived from Lutzomyia longipalpis ). Several intraclonal hybrids were obtained with L . tropica as crossing progenitor, but not with L . donovani or L . major . In interspecies crossings, three L . donovani x L . major hybrids and two L . donovani x L . tropica hybrids were isolated, thereby demonstrating the feasibility to obtain in vitro hybrids of parental lines causing different tropism of leishmaniasis. Ploidy analysis revealed an increase in DNA content in all hybrids compared to the parental strains, and nuclear analysis showed that interspecies hybrids are complete hybrids, i.e. each of them showing at least one chromosomal set from each parental. Regarding kDNA inheritance, discrepancies were observed between maxi and minicircle heritage. Finally, phenotypic studies showed either intermediate phenotypes in terms of growth profiles, or a decreased in vitro infection capacity compared to the parental cells. To the best of our knowledge, this is the first time that in vitro interspecies outcrossing has been demonstrated between Leishmania species with different tropism, thus contributing to shed light on the mechanisms underlying sexual reproduction in these parasites.
Diseases caused by trypanosomatids are serious public health concerns in low-income endemic countries. Leishmaniasis is presented in two main clinical forms, visceral leishmaniasis-caused by L. infantum and L. donovani-and cutaneous leishmaniasis-caused by many species, including L. major, L. tropica and L. braziliensis. As for certain other trypanosomatids, sexual reproduction has been confirmed in these parasites, and formation of hybrids can contribute to virulence, drug resistance or adaptation to the host immune system. In the present work, the capability of intraclonal and interspecies genetic exchange has been investigated using three parental strains: L. donovani, L. tropica and L. major, which have been engineered to express different fluorescent proteins and antibiotic resistance markers in order to facilitate the phenotypic selection of hybrid parasites after mating events. Stationary and exponential-phase promastigotes of each species were used, in in vitro experiments, some of them containing LULO cells (an embryonic cell line derived from Lutzomyia longipalpis). Several intraclonal hybrids were obtained with L. tropica as crossing progenitor, but not with L. donovani or L. major. In interspecies crossings, three L. donovani x L. major hybrids and two L. donovani x L. tropica hybrids were isolated, thereby demonstrating the feasibility to obtain in vitro hybrids of parental lines causing different tropism of leishmaniasis. Ploidy analysis revealed an increase in DNA content in all hybrids compared to the parental strains, and nuclear analysis showed that interspecies hybrids are complete hybrids, i.e. each of them showing at least one chromosomal set from each parental. Regarding kDNA inheritance, discrepancies were observed between maxi and minicircle heritage. Finally, phenotypic studies showed either intermediate phenotypes in terms of growth profiles, or a decreased in vitro infection capacity compared to the parental cells. To the best of our knowledge, this is the first time that in vitro interspecies outcrossing has been demonstrated between Leishmania species with different tropism, thus contributing to shed light on the mechanisms underlying sexual reproduction in these parasites.
Diseases caused by trypanosomatids are serious public health concerns in low-income endemic countries. Leishmaniasis is presented in two main clinical forms, visceral leishmaniasis-caused by L. infantum and L. donovani-and cutaneous leishmaniasis-caused by many species, including L. major, L. tropica and L. braziliensis. As for certain other trypanosomatids, sexual reproduction has been confirmed in these parasites, and formation of hybrids can contribute to virulence, drug resistance or adaptation to the host immune system. In the present work, the capability of intraclonal and interspecies genetic exchange has been investigated using three parental strains: L. donovani, L. tropica and L. major, which have been engineered to express different fluorescent proteins and antibiotic resistance markers in order to facilitate the phenotypic selection of hybrid parasites after mating events. Stationary and exponential-phase promastigotes of each species were used, in in vitro experiments, some of them containing LULO cells (an embryonic cell line derived from Lutzomyia longipalpis). Several intraclonal hybrids were obtained with L. tropica as crossing progenitor, but not with L. donovani or L. major. In interspecies crossings, three L. donovani x L. major hybrids and two L. donovani x L. tropica hybrids were isolated, thereby demonstrating the feasibility to obtain in vitro hybrids of parental lines causing different tropism of leishmaniasis. Ploidy analysis revealed an increase in DNA content in all hybrids compared to the parental strains, and nuclear analysis showed that interspecies hybrids are complete hybrids, i.e. each of them showing at least one chromosomal set from each parental. Regarding kDNA inheritance, discrepancies were observed between maxi and minicircle heritage. Finally, phenotypic studies showed either intermediate phenotypes in terms of growth profiles, or a decreased in vitro infection capacity compared to the parental cells. To the best of our knowledge, this is the first time that in vitro interspecies outcrossing has been demonstrated between Leishmania species with different tropism, thus contributing to shed light on the mechanisms underlying sexual reproduction in these parasites.Diseases caused by trypanosomatids are serious public health concerns in low-income endemic countries. Leishmaniasis is presented in two main clinical forms, visceral leishmaniasis-caused by L. infantum and L. donovani-and cutaneous leishmaniasis-caused by many species, including L. major, L. tropica and L. braziliensis. As for certain other trypanosomatids, sexual reproduction has been confirmed in these parasites, and formation of hybrids can contribute to virulence, drug resistance or adaptation to the host immune system. In the present work, the capability of intraclonal and interspecies genetic exchange has been investigated using three parental strains: L. donovani, L. tropica and L. major, which have been engineered to express different fluorescent proteins and antibiotic resistance markers in order to facilitate the phenotypic selection of hybrid parasites after mating events. Stationary and exponential-phase promastigotes of each species were used, in in vitro experiments, some of them containing LULO cells (an embryonic cell line derived from Lutzomyia longipalpis). Several intraclonal hybrids were obtained with L. tropica as crossing progenitor, but not with L. donovani or L. major. In interspecies crossings, three L. donovani x L. major hybrids and two L. donovani x L. tropica hybrids were isolated, thereby demonstrating the feasibility to obtain in vitro hybrids of parental lines causing different tropism of leishmaniasis. Ploidy analysis revealed an increase in DNA content in all hybrids compared to the parental strains, and nuclear analysis showed that interspecies hybrids are complete hybrids, i.e. each of them showing at least one chromosomal set from each parental. Regarding kDNA inheritance, discrepancies were observed between maxi and minicircle heritage. Finally, phenotypic studies showed either intermediate phenotypes in terms of growth profiles, or a decreased in vitro infection capacity compared to the parental cells. To the best of our knowledge, this is the first time that in vitro interspecies outcrossing has been demonstrated between Leishmania species with different tropism, thus contributing to shed light on the mechanisms underlying sexual reproduction in these parasites.
Diseases caused by trypanosomatids are serious public health concerns in low-income endemic countries. Leishmaniasis is presented in two main clinical forms, visceral leishmaniasis—caused by L . infantum and L . donovani —and cutaneous leishmaniasis—caused by many species, including L . major , L . tropica and L . braziliensis . As for certain other trypanosomatids, sexual reproduction has been confirmed in these parasites, and formation of hybrids can contribute to virulence, drug resistance or adaptation to the host immune system. In the present work, the capability of intraclonal and interspecies genetic exchange has been investigated using three parental strains: L . donovani , L . tropica and L . major , which have been engineered to express different fluorescent proteins and antibiotic resistance markers in order to facilitate the phenotypic selection of hybrid parasites after mating events. Stationary and exponential-phase promastigotes of each species were used, in in vitro experiments , some of them containing LULO cells (an embryonic cell line derived from Lutzomyia longipalpis ). Several intraclonal hybrids were obtained with L . tropica as crossing progenitor, but not with L . donovani or L . major . In interspecies crossings, three L . donovani x L . major hybrids and two L . donovani x L . tropica hybrids were isolated, thereby demonstrating the feasibility to obtain in vitro hybrids of parental lines causing different tropism of leishmaniasis. Ploidy analysis revealed an increase in DNA content in all hybrids compared to the parental strains, and nuclear analysis showed that interspecies hybrids are complete hybrids, i.e. each of them showing at least one chromosomal set from each parental. Regarding kDNA inheritance, discrepancies were observed between maxi and minicircle heritage. Finally, phenotypic studies showed either intermediate phenotypes in terms of growth profiles, or a decreased in vitro infection capacity compared to the parental cells. To the best of our knowledge, this is the first time that in vitro interspecies outcrossing has been demonstrated between Leishmania species with different tropism, thus contributing to shed light on the mechanisms underlying sexual reproduction in these parasites. Neglected Tropical Diseases (NTDs) represent a serious threat to humans, especially for those living in poor or developing countries. Leishmanianiosis is considered a zoonotic NTD transmitted by the bite of female phlebotomine sandflies, and is manifested mainly as a visceral form (caused by L . infantum and L . donovani ) and a cutaneous form (caused by many species including L . major , L . tropica and L . braziliensis ). Although it is now known that sexual reproduction occurs in these parasites, more studies are necessary to characterize the ability of Leishmania to generate hybrids, which may represent an important mechanism for virulence, drug resistance or adaptation to the host immune system. Therefore, several experiments were conducted to generate either intraclonal or interspecies hybrids in vitro . Results demonstrated that hybrids can be formed even with outcrosses between parasites causing visceral and cutaneous forms of the disease. Characterization of hybrids in terms of ploidy, kDNA content, growth rate and infection capacity provide important information about sexual reproduction in these parasites.
Audience Academic
Author Balaña-Fouce, Rafael
Bello, Felio J
Reguera, Rosa M.
Gutiérrez-Corbo, Camino
García-Estrada, Carlos
Pérez-Pertejo, Yolanda
Domínguez-Asenjo, Bárbara
AuthorAffiliation University of Washington, UNITED STATES
1 Departamento de Ciencias Biomédicas, Facultad de Veterinaria, Universidad de León, León, Spain
2 Facultad de Ciencias Agropecuarias, Programa de Medicina Veterinaria, Universidad de la Salle, Bogotá, Colombia
AuthorAffiliation_xml – name: 2 Facultad de Ciencias Agropecuarias, Programa de Medicina Veterinaria, Universidad de la Salle, Bogotá, Colombia
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BackLink https://www.ncbi.nlm.nih.gov/pubmed/35139072$$D View this record in MEDLINE/PubMed
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The authors have declared that no competing interests exist.
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Snippet Diseases caused by trypanosomatids are serious public health concerns in low-income endemic countries. Leishmaniasis is presented in two main clinical forms,...
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doaj
pubmedcentral
proquest
gale
pubmed
crossref
SourceType Open Website
Open Access Repository
Aggregation Database
Index Database
Enrichment Source
StartPage e0010170
SubjectTerms Analysis
Animals
Antibiotic resistance
Antibiotics
Biology and Life Sciences
Cell Line
Cells
Chromosomes
Cutaneous leishmaniasis
Deoxyribonucleic acid
Disease resistance
DNA
Drug resistance
Experiments
Feasibility studies
Fluorescence
Genes
Genetic aspects
Germfree
Growth
Heredity
Hybridization, Genetic
Hybrids
Immune system
Immunity
Laboratories
Leishmania
Leishmania donovani - genetics
Leishmania major - genetics
Leishmania tropica - genetics
Leishmaniasis, Cutaneous - parasitology
Leishmaniasis, Visceral - parasitology
Medicine and Health Sciences
Mitochondrial DNA
Parasites
Parasitic diseases
Phenotypes
Ploidy
Promastigotes
Psychodidae
Public health
Reproduction
Reproduction (biology)
Reproductive behaviour
Research and Analysis Methods
Sexual reproduction
Species
Strains
Tropical diseases
Tropism
Tropisms
Varieties
Vector-borne diseases
Virulence
Visceral leishmaniasis
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Title Axenic interspecies and intraclonal hybrid formation in Leishmania: Successful crossings between visceral and cutaneous strains
URI https://www.ncbi.nlm.nih.gov/pubmed/35139072
https://www.proquest.com/docview/2640118484
https://www.proquest.com/docview/2627483534
https://pubmed.ncbi.nlm.nih.gov/PMC8827483
https://doaj.org/article/1a3d3a4d134040efb23d32397d561526
http://dx.doi.org/10.1371/journal.pntd.0010170
Volume 16
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