Título: Professor Associado
Laboratório: Laboratório de Imunologia Experimental (LIE)
Telefone: +55 (11) 3091-7487
E-mail: sanunes@usp.br
Lattes: http://lattes.cnpq.br/0736417939241196
Linha de pesquisa
1. “Imunoma” funcional da saliva de artropódes vetores (mosquitos, carrapatos, flebótomos e barbeiros).
2. Interações entre artrópodes hematófagos e o hospedeiro vertebrado.
3. Imunologia de barreiras com enfoque na pele.
4. Modelos experimentais de doenças inflamatórias/autoimunes.
Resumo
O Laboratório de Imunologia Experimental (LIE) estuda as propriedades imunomoduladoras da saliva de artrópodes hematófagos vetores de doenças em diferentes abordagens in vitro e in vivo. As atividades da saliva de mosquitos, carrapatos, flebótomos e barbeiros são avaliadas em culturas celulares de macrófagos, células dendríticas, neutrófilos, mastócitos e linfócitos sob diversos estímulos de ativação. Também avaliamos o perfil imunológico cutâneo e sistêmico de hospedeiros vertebrados expostos a esses artrópodes hematófagos. Diversas moléculas bioativas presentes na saliva e responsáveis pelas atividades abordadas são isoladas e identificadas, podendo ser prospectadas como potenciais imunobiológicos para o tratamento de doenças imunológicas e autoimunes. Pessoas interessadas em explorar o universo das moléculas salivares desses artrópodes são bem vindas ao nosso grupo de pesquisa!
Over the last few years, we have accumulated experience in several areas of immunology. The principal objective of establishing the Laboratory of Experimental Immunology (LEI) was to create a place where students and researchers could work with in vitro systems and animal models for studying diseases, inflammation, natural products and immunobiology of arthropod vectors of disease. We are a young group, with many ideas for projects and open to new work proposals.
Principais publicações
- Lara PG, Esteves E, Sales-Campos H, Assis JB, Henrique MO, Barros MS, Neto LS, Silva PI, Martins JO, Cardoso CRB, Ribeiro JMC, Sá-Nunes A. AeMOPE-1, a Novel Salivary Peptide From Aedes aegypti, Selectively Modulates Activation of Murine Macrophages and Ameliorates Experimental Colitis. Front Immunol. 2021 Jul 19;12:681671. doi: 10.3389/fimmu.2021.681671. eCollection 2021. PMID: 34349757
- Assis JB, Cogliati B, Esteves E, Capurro ML, Fonseca DM, Sá-Nunes A. Aedes aegypti mosquito saliva ameliorates acetaminophen-induced liver injury in mice. PLoS One. 2021 Feb 8;16(2):e0245788. doi: 10.1371/journal.pone.0245788. eCollection 2021. PMID: 33556084 Free PMC article.
- Sá-Nunes A, Oliveira CJF. Dendritic Cells as a Disputed Fortress on the Tick-Host Battlefield. Trends Parasitol. 2021 Apr;37(4):340-354. doi: 10.1016/j.pt.2020.11.004. Epub 2020 Dec 7. PMID: 33303363
- Salina ACG, Brandt SL, Klopfenstein N, Blackman A, Bazzano JMR, Sá-Nunes A, Byers-Glosson N, Brodskyn C, Tavares NM, Da Silva IBS, Medeiros AI, Serezani CH. Leukotriene B4 licenses inflammasome activation to enhance skin host defense. Proc Natl Acad Sci U S A. 2020 Dec 1;117(48):30619-30627. doi: 10.1073/pnas.2002732117. Epub 2020 Nov 12. PMID: 33184178
- Martin-Martin I, Smith LB, Chagas AC, Sá-Nunes A, Shrivastava G, Valenzuela-Leon PC, Calvo E. Aedes albopictus D7 Salivary Protein Prevents Host Hemostasis and Inflammation. Biomolecules. 2020 Sep 27;10(10):1372. doi: 10.3390/biom10101372. PMID: 32992542
- Sá-Nunes A, Oliveira CJF, Ribeiro JM. Mast Cells and Basophils: From Malevolent Design to Coevolutionary Arms Race. Trends Parasitol. 2020 Aug;36(8):655-659. doi: 10.1016/j.pt.2020.05.003. Epub 2020 May 21. PMID: 32448702
- Coutinho ML, Bizzarro B, Tirloni L, Berger M, Freire Oliveira CJ, Sá-Nunes A, Silva Vaz I Jr. Rhipicephalus microplus serpins interfere with host immune responses by specifically modulating mast cells and lymphocytes. Ticks Tick Borne Dis. 2020 Jul;11(4):101425. doi: 10.1016/j.ttbdis.2020.101425. Epub 2020 Mar 26. PMID: 32335011
- Henrique MO, Neto LS, Assis JB, Barros MS, Capurro ML, Lepique AP, Fonseca DM, Sá-Nunes A. Evaluation of inflammatory skin infiltrate following Aedes aegypti bites in sensitized and non-sensitized mice reveals saliva-dependent and immune-dependent phenotypes. Immunology. 2019 Sep;158(1):47-59. doi: 10.1111/imm.13096. PMID: 31315156
- Barros MS, Lara PG, Fonseca MT, Moretti EH, Filgueiras LR, Martins JO, Capurro ML, Steiner AA, Sá-Nunes A. Aedes aegypti saliva impairs M1-associated proinflammatory phenotype without promoting or affecting M2 polarization of murine macrophages. Parasit Vectors. 2019 May 16;12(1):239. doi: 10.1186/s13071-019-3487-7. PMID: 31097013
- Sauter IP, Madrid KG, de Assis JB, Sá-Nunes A, Torrecilhas AC, Staquicini DI, Pasqualini R, Arap W, Cortez M. TLR9/MyD88/TRIF signaling activates host immune inhibitory CD200 in Leishmania infection. JCI Insight. 2019 May 16;4(10):e126207. doi: 10.1172/jci.insight.126207. eCollection 2019 May 16. PMID: 31092731
- Esteves E, Bizzarro B, Costa FB, Ramírez-Hernández A, Peti APF, Cataneo AHD, Wowk PF, Timóteo RP, Labruna MB, Silva Junior PI, Silva CL, Faccioli LH, Fogaça AC, Sorgi CA, Sá-Nunes A. Amblyomma sculptum Salivary PGE2 Modulates the Dendritic Cell-Rickettsia rickettsii Interactions in vitro and in vivo. Front Immunol. 2019 Feb 4;10:118. doi: 10.3389/fimmu.2019.00118. eCollection 2019. PMID: 30778355
- Breijo M, Esteves E, Bizzarro B, Lara PG, Assis JB, Rocha S, Pastro L, Fernández C, Meikle A, Sá-Nunes A. Hematobin is a novel immunomodulatory protein from the saliva of the horn fly Haematobia irritans that inhibits the inflammatory response in murine macrophages. Parasit Vectors. 2018 Jul 27;11(1):435. doi: 10.1186/s13071-018-3017-z. PMID: 30053916
- Esteves E, Maruyama SR, Kawahara R, Fujita A, Martins LA, Righi AA, Costa FB, Palmisano G, Labruna MB, Sá-Nunes A, Ribeiro JMC, Fogaça AC. Analysis of the Salivary Gland Transcriptome of Unfed and Partially Fed Amblyomma sculptum Ticks and Descriptive Proteome of the Saliva. Front Cell Infect Microbiol. 2017 Nov 21;7:476. doi: 10.3389/fcimb.2017.00476. eCollection 2017. PMID: 29209593
- Vernal S, Pepinelli M, Casanova C, Goulart TM, Kim O, De Paula NA, Pinto MC, Sá-Nunes A, Roselino AM. Insights into the epidemiological link between biting flies and pemphigus foliaceus in southeastern Brazil. Acta Trop. 2017 Dec;176:455-462. doi: 10.1016/j.actatropica.2017.09.015. Epub 2017 Sep 21. PMID: 28941730
- Barros MS, Gomes E, Gueroni DI, Ramos AD, Mirotti L, Florsheim E, Bizzarro B, Lino CN, Maciel C, Lino-Dos-Santos-Franco A, Tavares-de-Lima W, Capurro ML, Russo M, Sá-Nunes A. Exposure to Aedes aegypti Bites Induces a Mixed-Type Allergic Response following Salivary Antigens Challenge in Mice. PLoS One. 2016 May 20;11(5):e0155454. doi: 10.1371/journal.pone.0155454. eCollection 2016. PMID: 27203689
- Sales-Campos H, de Souza PR, Basso PJ, Ramos AD, Nardini V, Chica JE, Capurro ML, Sá-Nunes A, de Barros Cardoso CR. Aedes aegypti salivary gland extract ameliorates experimental inflammatory bowel disease. Int Immunopharmacol. 2015 May;26(1):13-22. doi: 10.1016/j.intimp.2015.03.002. Epub 2015 Mar 12. PMID: 25770821
- Maciel C, Fujita A, Gueroni DI, Ramos AD, Capurro ML, Sá-Nunes A. Evans blue as a simple method to discriminate mosquitoes’ feeding choice on small laboratory animals. PLoS One. 2014 Oct 21;9(10):e110551. doi: 10.1371/journal.pone.0110551. eCollection 2014. PMID: 25333369
- Costa-da-Silva AL, Marinotti O, Ribeiro JM, Silva MC, Lopes AR, Barros MS, Sá-Nunes A, Kojin BB, Carvalho E, Suesdek L, Silva-Neto MA, James AA, Capurro ML. Transcriptome sequencing and developmental regulation of gene expression in Anopheles aquasalis. PLoS Negl Trop Dis. 2014 Jul 17;8(7):e3005. doi: 10.1371/journal.pntd.0003005. eCollection 2014 Jul. PMID: 25033462
- Francischetti IM, Gordon E, Bizzarro B, Gera N, Andrade BB, Oliveira F, Ma D, Assumpção TC, Ribeiro JM, Pena M, Qi CF, Diouf A, Moretz SE, Long CA, Ackerman HC, Pierce SK, Sá-Nunes A, Waisberg M. Tempol, an intracellular antioxidant, inhibits tissue factor expression, attenuates dendritic cell function, and is partially protective in a murine model of cerebral malaria. PLoS One. 2014 Feb 28;9(2):e87140. doi: 10.1371/journal.pone.0087140. eCollection 2014. PMID: 24586264
- Bizzarro B, Barros MS, Maciel C, Gueroni DI, Lino CN, Campopiano J, Kotsyfakis M, Amarante-Mendes GP, Calvo E, Capurro ML, Sá-Nunes A. Effects of Aedes aegypti salivary components on dendritic cell and lymphocyte biology. Parasit Vectors. 2013 Nov 15;6:329. doi: 10.1186/1756-3305-6-329. PMID: 24238038
- Oliveira CJ, Anatriello E, de Miranda-Santos IK, Francischetti IM, Sá-Nunes A, Ferreira BR, Ribeiro JM. Proteome of Rhipicephalus sanguineus tick saliva induced by the secretagogues pilocarpine and dopamine. Ticks Tick Borne Dis. 2013 Dec;4(6):469-77. doi: 10.1016/j.ttbdis.2013.05.001. Epub 2013 Sep 9. PMID: 24029695
- Barboza R, Câmara NO, Gomes E, Sá-Nunes A, Florsheim E, Mirotti L, Labrada A, Alcântara-Neves NM, Russo M. Endotoxin Exposure during Sensitization to Blomia tropicalis Allergens Shifts TH2 Immunity Towards a TH17-Mediated Airway Neutrophilic Inflammation: Role of TLR4 and TLR2. PLoS One. 2013 Jun 21;8(6):e67115. doi: 10.1371/journal.pone.0067115. Print 2013. PMID: 23805294
- Collin N, Assumpção TC, Mizurini DM, Gilmore DC, Dutra-Oliveira A, Kotsyfakis M, Sá-Nunes A, Teixeira C, Ribeiro JM, Monteiro RQ, Valenzuela JG, Francischetti IM. Lufaxin, a novel factor Xa inhibitor from the salivary gland of the sand fly Lutzomyia longipalpis blocks protease-activated receptor 2 activation and inhibits inflammation and thrombosis in vivo. Arterioscler Thromb Vasc Biol. 2012 Sep;32(9):2185-98. doi: 10.1161/ATVBAHA.112.253906. Epub 2012 Jul 12. PMID: 22796577
- Francischetti IM, Oliveira CJ, Ostera GR, Yager SB, Debierre-Grockiego F, Carregaro V, Jaramillo-Gutierrez G, Hume JC, Jiang L, Moretz SE, Lin CK, Ribeiro JM, Long CA, Vickers BK, Schwarz RT, Seydel KB, Iacobelli M, Ackerman HC, Srinivasan P, Gomes RB, Wang X, Monteiro RQ, Kotsyfakis M, Sá-Nunes A, Waisberg M. Defibrotide interferes with several steps of the coagulation-inflammation cycle and exhibits therapeutic potential to treat severe malaria. Arterioscler Thromb Vasc Biol. 2012 Mar;32(3):786-98. doi: 10.1161/ATVBAHA.111.240291. Epub 2011 Nov 23. PMID: 22116094
- Carregaro V, Sá-Nunes A, Cunha TM, Grespan R, Oliveira CJ, Lima-Junior DS, Costa DL, Verri WA Jr, Milanezi CM, Pham VM, Brand DD, Valenzuela JG, Silva JS, Ribeiro JM, Cunha FQ. Nucleosides from Phlebotomus papatasi salivary gland ameliorate murine collagen-induced arthritis by impairing dendritic cell functions. J Immunol. 2011 Oct 15;187(8):4347-59. doi: 10.4049/jimmunol.1003404. Epub 2011 Sep 19. PMID: 21930966
- Calvo E, Mizurini DM, Sá-Nunes A, Ribeiro JM, Andersen JF, Mans BJ, Monteiro RQ, Kotsyfakis M, Francischetti IM. Alboserpin, a factor Xa inhibitor from the mosquito vector of yellow fever, binds heparin and membrane phospholipids and exhibits antithrombotic activity. J Biol Chem. 2011 Aug 12;286(32):27998-8010. doi: 10.1074/jbc.M111.247924. Epub 2011 Jun 14. PMID: 21673107
- Oliveira CJ, Sá-Nunes A, Francischetti IM, Carregaro V, Anatriello E, Silva JS, Santos IK, Ribeiro JM, Ferreira BR. Deconstructing tick saliva: non-protein molecules with potent immunomodulatory properties. J Biol Chem. 2011 Apr 1;286(13):10960-9. doi: 10.1074/jbc.M110.205047. Epub 2011 Jan 26. PMID: 21270122
- The function and three-dimensional structure of a thromboxane A2/cysteinyl leukotriene-binding protein from the saliva of a mosquito vector of the malaria parasite. Alvarenga PH, Francischetti IM, Calvo E, Sá-Nunes A, Ribeiro JM, Andersen JF. PLoS Biol. 2010 Nov 30;8(11):e1000547. doi: 10.1371/journal.pbio.1000547. PMID: 21152418 Free PMC article.
- Sá-Nunes A, Bafica A, Antonelli LR, Choi EY, Francischetti IM, Andersen JF, Shi GP, Chavakis T, Ribeiro JM, Kotsyfakis M. The immunomodulatory action of sialostatin L on dendritic cells reveals its potential to interfere with autoimmunity. J Immunol. 2009 Jun 15;182(12):7422-9. doi: 10.4049/jimmunol.0900075. PMID: 19494265
- Sá-Nunes A, Bafica A, Lucas DA, Conrads TP, Veenstra TD, Andersen JF, Mather TN, Ribeiro JM, Francischetti IM. Prostaglandin E2 is a major inhibitor of dendritic cell maturation and function in Ixodes scapularis saliva. J Immunol. 2007 Aug 1;179(3):1497-505. doi: 10.4049/jimmunol.179.3.1497. PMID: 17641015