ABSTRACT
In all major parasite groups, new and surprising evidence is emerging every day about the subtlety, complexity and diversity of avoidance mechanisms from host immune system. In the course of millions of years of evolutionary process, mammalian and sand fly hosts have developed defense systems against Leishmania, but Leishmania has not only escaped from their hosts’ defense systems through complex counter-strategies, but has also managed to manipulate them to support their own survival and reproduction. In this study, Leishmania’s survival strategies used in the sand fly and mammalian hosts and the mechanisms that underlie these strategies will be summarized.
Keywords: Leishmania, sand fly, survival strategies, lipophosphoglycan
References
1
Chiragkumar JG, Jimishaben DK. Review on Leishmaniasis. Biomed J Sci & Tech Res 2017;1:5.
2
Lamotte S, Späth GF, Rachidi N, Prina E. The enemy within: Targeting host-parasite interaction for antileishmanial drug discovery. PLoS Negl Trop Dis 2017;11:e0005480.
3
Cetin H, Ozbel Y. Sand Flies and Their Control Methods. Turkiye Parazitol Derg 2017; 41:102-13.
4
Gupta G, Oghumu S, Satoskar AR. Mechanisms of immune evasion in leishmaniasis. Adv Appl Microbiol 2013;82:155-84.
5
Dostálová A, Volf P. Leishmania development in sand flies: parasite-vector interactions overview. Parasit Vectors 2012;5:276.
6
Olivier M, Gregory DJ, Forget G. Subversion mechanisms by which Leishmania parasites can escape the host immune response: a signaling point of view. Clin Microbiol Rev 2005;18:293-305.
7
Ramalho-Ortigao M, Saraiva EM, & Traub-Csekö YM. Sand fly-Leishmania interactions: long relationships are not necessarily easy. Open Parasitol J 2010;4:195-204.
8
Cecílio P, Pérez-Cabezas B, Santarém N, Maciel J, Rodrigues V, Cordeiro da Silva A. Deception and manipulation: the arms of leishmania, a successful parasite. Front Immunol 2014;5:480.
9
Podinovskaia M, Descoteaux A. Leishmania and the macrophage: a multifaceted interaction. Future Microbiol 2015;10:111-29.
10
Santos-Mateus D, Passero F, Rodrigues A, Valério-Bolas A, Silva-Pedrosa R, Pereira M, et al. The battle between Leishmania and the host immune system at a glance. Int Trend Immun 2016;4:28.
11
Naderer T, Vince JE, McConville MJ. Surface determinants of Leishmania parasites and their role in infectivity in the mammalian host. Curr Mol Med 2004;4:649-65.
12
Matlashewski G. Leishmania Infection and Macrophage Function. In: Farrell J.P (editors). Leishmania. World Class Parasites, vol 4. Springer, Boston, MA. 2002.p.105-13.
13
Pimenta PF, Saraiva EM, Sacks DL. The comparative fine structure and surface glycoconjugate expression of three life stages of Leishmania major. Exp Parasitol 1991;72:191-204.
14
Sainz de la Maza MO. Leishmaniasis transmission biology: Role of Promastigote Secretory Gel as a transmission determinant. (dissertation), London School of Hygiene & Tropical Medicine 2014.
15
Sacks DL, Pimenta PF, McConville MJ, Schneider P, Turco SJ. Stage-specific binding of Leishmania donovani to the sand fly vector midgut is regulated by conformational changes in the abundant surface lipophosphoglycan. J Exp Med 1995;181:685-97.
16
Sacks D, Kamhawi S. Molecular aspects of parasite-vector and vector-host interactions in leishmaniasis. Annu Rev Microbiol 2001;55:453-83.
17
Descoteaux A, Turco SJ. Glycoconjugates in Leishmania infectivity. Biochim Biophys Acta 1999 Oct 8;1455:341-52.
18
Schlein Y, Jacobson RL. Resistance of Phlebotomus papatasi to infection with Leishmania donovani is modulated by components of the infective bloodmeal. Parasitology 1998;117:467-73.
19
Warburg A, Tesh RB, McMahon-Pratt D. Studies on the attachment of Leishmania flagella to sand fly midgut epithelium. J Protozool 1989;36:613-7.
20
Vaidyanathan R. Leishmania parasites (Kinetoplastida: Trypanosomatidae) reversibly inhibit visceral muscle contractions in hemimetabolous and holometabolous insects. J Invertebr Pathol 2004;87:123-8.
21
Killick-Kendrick R, Leaney AJ, Ready PD, Molyneux DH. Leishmania in phlebotomid sandflies. IV. The transmission of Leishmania mexicana amazonensis to hamsters by the bite of experimentally infected Lutzomyia longipalpis. Proc R Soc Lond B Biol Sci 1977;196:105-15.
22
Puentes SM, Sacks DL, da Silva RP, Joiner KA. Complement binding by two developmental stages of Leishmania major promastigotes varying in expression of a surface lipophosphoglycan. J Exp Med 1988;167:887-902.
23
Brittingham A, Mosser D. Exploitation of the complement system by Leishmania promastigotes. Parasitol Today 1996;12:444-7.
24
Peters NC, Egen JG, Secundino N, Debrabant A, Kimblin N., Kamhawi S, et al. In vivo imaging reveals an essential role for neutrophils in leishmaniasis transmitted by sand flies. Science. 2008 Aug 15;321:970-4.
25
Séguin O, Descoteaux A. Leishmania, the phagosome, and host responses: The journey of a parasite. Cell Immunol 2016;309:1-6.
26
Regli IB, Passelli K, Hurrell BP, Tacchini-Cottier F. Survival Mechanisms Used by Some Leishmania Species to Escape Neutrophil Killing. Front Immunol 2017;8:1558.
27
van Zandbergen G, Klinger M, Mueller A, Dannenberg S, Gebert A, Solbach W, et al. Cutting edge: neutrophil granulocyte serves as a vector for Leishmania entry into macrophages. J Immunol 2004;173:6521-5.
28
Martínez-López M, Soto M, Iborra S, Sancho D. Leishmania Hijacks Myeloid Cells for Immune Escape. Front Microbiol 2018;9:883.
29
Chagas AC, Oliveira F, Debrabant A, Valenzuela JG, Ribeiro JM, Calvo E. Lundep, a sand fly salivary endonuclease increases Leishmania parasite survival in neutrophils and inhibits XIIa contact activation in human plasma. PLoS Pathog 2014;10:e1003923.
30
Aga E, Katschinski DM, van Zandbergen G, Laufs H, Hansen B, Müller K, et al. Inhibition of the spontaneous apoptosis of neutrophil granulocytes by the intracellular parasite Leishmania major. J Immunol 2002;169:898-905.
31
Geering B, Simon HU. Peculiarities of cell death mechanisms in neutrophils. Cell Death Differ 2011;18:1457-69.
32
Ribeiro-Gomes FL, Peters NC, Debrabant A, Sacks DL. Efficient capture of infected neutrophils by dendritic cells in the skin inhibits the early anti-leishmania response. PLoS Pathog 2012;8:e1002536.
33
Silverman JM, Reiner NE. Exosomes and other microvesicles in infection biology: organelles with unanticipated phenotypes. Cell Microbiol 2011;13:1-9.
34
Rizvi FS, Ouaissi MA, Marty B, Santoro F, Capron A. The major surface protein of Leishmania promastigotes is a fibronectin-like molecule. Eur J Immunol 1988;18:473-6.
35
Brittingham A, Chen G, McGwire BS, Chang KP, Mosser DM. Interaction of Leishmania gp63 with cellular receptors for fibronectin. Infect Immun 1999;67:4477-84.
36
Majumder S, Dey R, Bhattacharjee S, Rub A, Gupta G, Bhattacharyya Majumdar S, et al. Leishmania-induced biphasic ceramide generation in macrophages is crucial for uptake and survival of the parasite. J Infect Dis 2012;205:1607-16.
37
Rodriguez NE, Gaur U, Wilson ME. Role of caveolae in Leishmania chagasi phagocytosis and intracellular survival in macrophages. Cell Microbiol 2006;8:1106-20.
38
Kaneshiro ES, Gottlieb M, Dwyer DM. Cell surface origin of antigens shed by Leishmania donovani during growth in axenic culture. Infect Immun 1982;37:558-67.
39
Verma JK, Rastogi R, Mukhopadhyay A. Leishmania donovani resides in modified early endosomes by upregulating Rab5a expression via the downregulation of miR-494. PLoS Pathog 2017;13:e1006459.
40
Matheoud D, Moradin N, Bellemare-Pelletier A, Shio MT, Hong WJ, Olivier M, et al. Leishmania evades host immunity by inhibiting antigen cross-presentation through direct cleavage of the SNARE VAMP8. Cell Host Microbe 2013;14:15-25.
41
Proudfoot L, Nikolaev AV, Feng GJ, Wei WQ, Ferguson MA, Brimacombe JS et al. Regulation of the expression of nitric oxide synthase and leishmanicidal activity by glycoconjugates of Leishmania lipophosphoglycan in murine macrophages. Proc Natl Acad Sci USA 1996;93:10984-9.
42
Broz P, Monack DM. Newly described pattern recognition receptors team up against intracellular pathogens. Nat Rev Immunol 2013;13:551-65.
43
de Veer MJ, Curtis JM, Baldwin TM, DiDonato JA, Sexton A, McConville MJ, et al. MyD88 is essential for clearance of Leishmania major: possible role for lipophosphoglycan and Toll-like receptor 2 signaling. Eur J Immunol.2003;33:2822-31.
44
Delgado-Domínguez J, González-Aguilar H, Aguirre-García M, Gutiérrez-Kobeh L, Berzunza-Cruz M, Ruiz-Remigio A, et al. Leishmania mexicana lipophosphoglycan differentially regulates PKCalpha-induced oxidative burst in macrophages of BALB/c and C57BL/6 mice. Parasite Immunol 2010;32:440-9.
45
Gupta P, Giri J, Srivastav S, Chande AG, Mukhopadhyaya R, Das PK, et al. Leishmania donovani targets tumor necrosis factor receptor-associated factor (TRAF) 3 for impairing TLR4-mediated host response. FASEB J 2014;28:1756-68.
46
Bogdan C, Röllinghoff M. How do protozoan parasites survive inside macrophages? Parasitol Today 1999;15:22-8.
47
Diaz-Gandarilla JA, Osorio-Trujillo C, Hernandez-Ramirez VI , Talamas- Rohana P. PPAR activation induces M1 macrophage polarization via cPLA(2)- COX-inhibition, activating ROS production against Leishmania mexicana. Biomed Res Int 2013; Article ID: 215283.
48
Kropf P, Fuentes JM, Fahnrich E, Arpa L, Herath S, Weber V, et al. Arginase and polyamine synthesis are key factors in the regulation of experimental leishmaniasis in vivo. FASEB J 2005;19:1000-2.
49
Carrera L, Gazzinelli RT, Badolato R, Hieny S, Muller W, Kuhn R et al. Leishmania promastigotes selectively inhibit interleukin 12 induction in bone marrow-derived macrophages from susceptible and resistant mice. J Exp Med 1996;183:515-26.
50
Nylen S, Gautam S. Immunological perspectives of leishmaniasis. J Glob Infect Dis. 2010;2:135-46.
51
Buates S, Matlashewski G. General suppression of macrophage gene expression during Leishmania donovani infection. J Immunol 2001;166:3416-22.
52
Silverman JM, Clos J, de’oliveira CC, Shirvani O, Fang Y, Wang C, et al. An exosome-based secretion pathway is responsible for protein export from Leishmania and communication with macrophages. J Cell Sci 2010;123:842-52.
53
Chakraborty D, Banerjee S, Sen A, Banerjee KK, Das P, Roy S. Leishmania donovani affects antigen presentation of macrophage by disrupting lipid rafts. J Immunol 2005;175:3214-24.
54
Buates S, Matlashewski G. Treatment of experimental leishmaniasis with the immunomodulators imiquimod and S-28463: efficacy and mode of action. J Infect Dis 1999;179:1485-94.
55
De Muylder G, Vanhollebeke B, Caljon G, Wolfe AR, McKerrow J, Dujardin JC. Naloxonazine, an Amastigote-Specific Compound, Affects Leishmania Parasites through Modulation of Host-Encoded Functions. PLoS Negl Trop Dis 2016;10:e0005234.
