Study of the Salivary Glands in Triatominae (Hemiptera, Reduviidae, Triatominae): Their Color and Application to the Chagas Disease Vector Evolution

Jader de Oliveira Laboratório de Parasitologia, Departamento de Ciências Biológicas, Faculdade de Ciências Farmacêuticas, Universidade Estadual Paulista “Júlio de Mesquita Filho” (FCFAR/UNESP), Araraquara, Brazil;

Search for other papers by Jader de Oliveira in
Current site
Google Scholar
PubMed
Close
,
Amanda Ravazi Laboratório de Biologia Celular, Departamento de Biologia, Instituto de Biociências, Letras e Ciências Exatas, Universidade Estadual Paulista “Júlio de Mesquita Filho” (IBILCE/UNESP), São José do Rio Preto, Brazil;

Search for other papers by Amanda Ravazi in
Current site
Google Scholar
PubMed
Close
,
Eder dos Santos Souza Laboratório de Parasitologia, Departamento de Ciências Biológicas, Faculdade de Ciências Farmacêuticas, Universidade Estadual Paulista “Júlio de Mesquita Filho” (FCFAR/UNESP), Araraquara, Brazil;

Search for other papers by Eder dos Santos Souza in
Current site
Google Scholar
PubMed
Close
,
Felipe Ferraz Figueiredo Moreira Laboratório de Biodiversidade Entomológica, Instituto Oswaldo Cruz (LABE/IOC/FIOCRUZ), Rio de Janeiro, Brazil;

Search for other papers by Felipe Ferraz Figueiredo Moreira in
Current site
Google Scholar
PubMed
Close
,
Cleber Galvão Laboratório Nacional e Internacional de Referência em Taxonomia de Triatomíneos, Instituto Oswaldo Cruz (LNIRTT/IOC/FIOCRUZ), Rio de Janeiro, Brazil

Search for other papers by Cleber Galvão in
Current site
Google Scholar
PubMed
Close
,
João Aristeu da Rosa Laboratório de Parasitologia, Departamento de Ciências Biológicas, Faculdade de Ciências Farmacêuticas, Universidade Estadual Paulista “Júlio de Mesquita Filho” (FCFAR/UNESP), Araraquara, Brazil;

Search for other papers by João Aristeu da Rosa in
Current site
Google Scholar
PubMed
Close
, and
Kaio Cesar Chaboli Alevi Laboratório de Biologia Celular, Departamento de Biologia, Instituto de Biociências, Letras e Ciências Exatas, Universidade Estadual Paulista “Júlio de Mesquita Filho” (IBILCE/UNESP), São José do Rio Preto, Brazil;

Search for other papers by Kaio Cesar Chaboli Alevi in
Current site
Google Scholar
PubMed
Close
Restricted access

Chagas disease is caused by Trypanosoma cruzi and transmitted by feces of a triatomine that has the habit of defecating during blood feeding. The salivary glands of triatomines are important to hematophagy because their saliva is rich in anticoagulant and hemolytic proteins. The salivary glands of some Rhodnius species analyzed are reddish due to the presence of nitrophorins (antihemostatic activity). The present study aimed to analyze the color pattern of the salivary glands of 67 triatomine species to evaluate whether the presence of nitrophorins is a synapomorphy of Rhodnius or the tribe Rhodniini, or if it is shared with triatomines of the tribes Triatomini and Cavernicolini. Since only the species of the tribe Rhoniini present red glands, it is admitted that the presence of nitrophorin proteins is a synapomorphy of the tribe Rhodniini and that this tribe has derived more recently when compared with Triatomini and Cavernicolini.

Author Notes

Address correspondence to Jader de Oliveira, Faculdade de Ciências Farmacêuticas, Universidade Estadual Paulista (FCFAR/UNESP), Rodovia Araraquara-Jaú km 1, 14801-902, Araraquara, Sao Paulo, Brazil. E-mail: jdr.oliveira@hotmail.com

Financial support: The study was supported by Fundação de Amparo à Pesquisa do Estado de São Paulo (Process numbers 2013/19764-0, 2013/08826-5, and 2015/11372-1, FAPESP, Brazil) and Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq, Brazil process: 142284/2015-7).

Authors’ addresses: Jader de Oliveira, Eder dos Santos Souza, and João Aristeu da Rosa, Laboratório de Parasitologia, Departamento de Ciências Biológicas, Faculdade de Ciências Farmacêuticas, Universidade Estadual Paulista “Júlio de Mesquita Filho” (FCFAR/UNESP), Araraquara, Brazil, E-mails: jdr.oliveira@hotmail.com, ederss1@hotmail.com, and rosaja@fcfar.unesp.br. Amanda Ravazi and Kaio Cesar Chaboli Alevi, Laboratório de Biologia Celular, Departamento de Biologia, Instituto de Biociências, Letras e Ciências Exatas, Universidade Estadual Paulista “Júlio de Mesquita Filho” (IBILCE/UNESP), São José do Rio Preto, Brazil, E-mails: amandaravazi95@gmail.com and kaiochaboli@hotmail.com. Felipe Ferraz Figueiredo Moreira, Laboratório de Biodiversidade Entomológica, Instituto Oswaldo Cruz Fundacao Oswaldo Cruz, (LBE/IOC/FIOCRUZ), Rio de Janeiro, Brazil, E-mail: felipento@hotmail.com. Cleber Galvão, Laboratório Nacional e Internacional de Referência em Taxonomia de Triatomíneos, Instituto Oswaldo Cruz, Rio de Janeiro, Brazil, E-mail: clebergalvao@gmail.com.

  • 1.

    World Health Organization, 2015. Chagas disease (American trypanosomiasis). Wkly Epidemiol Rec 90: 3344.

  • 2.

    Galvão C, 2014. Vetores da Doença de Chagas no Brasil. Curitiba, Brazil: Sociedade Brasileira de Zoologia.

  • 3.

    Justi S, Galvão C, 2017. The evolutionary origin of diversity in Chagas disease vectors. Trends Parasitol 33: 4252.

  • 4.

    Schofield CJ, 1988. The biosystematics of Triatominae. Service MW, ed. Biosystematics of Haematophagous Insects, Systematics Association Special. Oxford, United Kingdom: Clarenden Press, 284312.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 5.

    Hellmann K, Hawkins RI, 1965. Prolixins-S and prolixin-G; two anticoagulants from Rhodnius prolixus Stal. Nature 207: 265267.

  • 6.

    Ribeiro JM, Hazzard JM, Nussenzveig RH, Champagne DE, Walker FA, 1993. Reversible binding of nitric oxide by a salivary heme protein from a bloodsucking insect. Science 260: 539541.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 7.

    Lacombe D, 1999. Anatomia e histologia de glândulas salivares de triatomíneos. Mem Inst Oswaldo Cruz 94: 557564.

  • 8.

    Montandon CE, Barros E, Vidigal PM, Mendes MT, Anhê ANBM, Ramos HJO, Oliveira CJF, Mafra C, 2016. Comparative proteomic analysis of the saliva of the Rhodnius prolixus, Triatoma lecticularia and Panstrongylus herreri triatomines reveals a high interspecific functional biodiversity. Insect Biochem Mol Biol 71: 8390.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 9.

    Anhê AC, Azeredo-Oliveira MT, 2008. Cytochemical characterization of Triatoma infestans and Panstrongylus megistus salivary gland cells (Hemiptera, Reduviidae, Triatominae). Micron 39: 11261133.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 10.

    Champagne DE, Nussenzveig RH, Ribeiro JMC, 1995. Purification, partial characterization and cloning of nitric oxide-carrying heme proteins (nitrophorins) from salivary glands of the blood-sucking insect Rhodnius prolixus .J Biol Chem 270: 86918695.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 11.

    Montfort WR, Weichsel A, Andersen JF, 2000. Nitrophorins and related antihemostatic lipocalins from Rhodnius prolixus and other blood-sucking arthropods. Biochim Biophys Acta 1482: 110118.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 12.

    Soares RPP, Gontijo NF, Romanha AJ, Diotaiuti L, Pereira MH, 1998. Salivary heme proteins distinguish Rhodnius prolixus from Rhodnius robustus (Hemiptera: Reduviidae: Triatominae). Acta Trop 71: 285291.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 13.

    Pacheco DE, 2014. Nitroforinas salivares de Rhodnius prolixus (Hemiptera: Reduviidae): Avaliação do RNAi parental e do papel da albumina do hospedeiro na sua atividade biológica. Available at: http://www.bibliotecadigital.ufmg.br/dspace/bitstream/handle/1843/BUOS-9KXJS7/dissertfinal.pdf?sequence=1. Accessed February 22, 2017.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 14.

    Meirelles RM, Rodrigues IS, Steindel M, Soares MJ, 2003. Ultrastructure of the salivary glands of Rhodnius domesticus Neiva and Pinto, 1923 (Hemiptera: Reduviidae). J Submicrosc Cytol Pathol 35: 199207.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 15.

    Bargues MD, Marcilla A, Ramsey J, Dujardin JP, Schofield CJ, Mas-Coma S, 2000. Nuclear rDNA-based molecular clock of the evolution of Triatominae (Hemiptera: Reduviidae), vectors of Chagas disease. Mem Inst Oswaldo Cruz 95: 567573.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 16.

    Justi SA, Galvão C, Schrago CG, 2016. Geological changes of the Americas and their influence on the diversification of the neotropical kissing bugs (Hemiptera: Reduviidae: Triatominae). PLoS Negl Trop Dis 10: e0004527.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 17.

    Ribeiro JMC, Schneider M, Guimaraes JA, 1995. Purification and characterization of Prolixin S (Nitrophorin 2), the salivary anticoagulant of the blood sucking bug, Rhodnius prolixus .Biochem J 308: 243249.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 18.

    Noeske-Jungblut C, Kratzschmar J, Haendler B, Alagon A, Possani L, Verhallen P, Donner P, Schleuning WD, 1994. An inhibitor of collagen-induced platelet aggregation from the saliva of Triatoma pallidipennis .J Biol Chem 269: 50505053.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 19.

    Isawa H, Orito Y, Jingushi N, Iwanaga S, Morita A, Chinzei Y, Yuda M, 2007. Identification and characterization of plasma kallikrein-kinin system inhibitors from salivar glands of the blood-sucking insect Triatoma infestans .FEBS J 274: 42714286.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 20.

    Ribeiro JMC, Assumpcao TC, Francischetti IMB, 2012. An insight into the sialomes of bloodsucking Heteroptera. Psyche (Stuttg) 2012: 16.

Past two years Past Year Past 30 Days
Abstract Views 88 88 11
Full Text Views 348 25 1
PDF Downloads 113 17 1
 
 
 
 
Affiliate Membership Banner
 
 
Research for Health Information Banner
 
 
CLOCKSS
 
 
 
Society Publishers Coalition Banner
Save