Immunity to Protozoa

Abstract

Protozoan parasites are microorganisms that live and feed at the expense of a host. Parasites can cause diseases in humans and are worldwide distributed, causing high morbidity and mortality. This article describes the most important defence mechanisms against protozoan parasites of clinical relevance (Plasmodium spp., Leishmania spp., Toxoplasma gondii, Trypanosoma cruzi, Entamoeba histolytica and Giardia lamblia). Protozoans exhibit a high heterogeneity in morphologies and antigenic expression, which is reflected in the different immune responses induced during the infection process. The first line of defence is the mechanisms of the innate immune response as physical and chemical barriers. However, in most cases, the adaptive humoural and cellular responses are implicated in controlling the infection. On the other hand, parasites have developed mechanisms to evade the immune response, hindering the development of vaccines, which offers a broad spectrum of protection among species.

Key Concepts

  • Parasitosis comprises a set of very diverse diseases, caused by different types of parasitic microorganisms.
  • Protozoan infections can be acquired either through direct contact or through vectors.
  • Malaria is the deadliest protozoan infection worldwide.
  • The immune response is divided into two branches: innate and adaptive immunity.
  • Protozoan parasites have developed strategies to evade the immune response.
  • To date, there has been an imminent necessity to develop efficient vaccines against main protozoan infections.

Keywords: protozoan parasites; protective immunity; malaria; Chagas disease; amoebiasis; toxoplasmosis; giardiasis; leishmaniasis

Figure 1. Intracellular protozoans activating different pathways of the immune response. Cells such as neutrophils, macrophages and epithelial cells (EC) participate in the innate immunity. These cells can produce reactive oxygen species (ROS, nitric oxide (NO) and cytokines such as IFN‐γ (gamma interferon) and TNF‐α (tumour necrosis factor alpha) to control the infection). Adaptive immunity is mediated by specific lymphocytes (T and B cells). T cells release cytotoxic proteins and cytokines for the activation of immune cells and B cells produce specific antibodies. Dendritic cells (DCs) and infected cells can present protozoan antigens to CD8‐positive T cells by the major histocompatibility complex class I (MHC I). The activated CD8‐positive T cells secrete cytokines such as TNF‐α to mediate the killing of infected cells. The humoural immunity provided by antibodies can be an effector in the extracellular stage of the protozoan, and B cells can intervene in the maturation of different Th cell subsets that are implicated in most intracellular parasite infections. *Some protozoans such as Toxoplasma gondii and Trypanosoma cruzi can invade different organs, depending on infection site different mechanisms of the immune response may be involved.
Figure 2. The extracellular protozoans activating different pathways of the immune response. The infection sites of Giardia lamblia and Entamoeba histolytica are in small and large gut, respectively. The physical barriers such as mucous membranes, stomach pH and biological peristalsis can control the infection. Owing to that Giardia is a noninfiltrative parasite, the DCs, macrophages and M cells may be able to mobilise Giardia antigens to lamina propria and active the adaptive immune response. Also, the intestinal epithelial cells (IEC) release potent chemokines to recruit immune cells to the invasion site. Activated macrophages release TNF‐α, stimulating neutrophils and macrophages to release ROS and NO, which can kill the parasite. ROS and NO may also contribute to tissue destruction. Major histocompatibility complex class II (MHC II) is implicated in antigen presentation of extracellular protozoans. T and B cells mediate the immune response against parasites through the antibodies IgA/IgG and cytokines of different T‐cell subsets, respectively. *E. histolytica can invade intestinal and other tissues as the liver.
Figure 3. Life cycle of Plasmodium. Malaria parasite life cycle involves two hosts. During a blood meal, a malaria‐infected female mosquito (Anopheles) inoculates sporozoites (1). Sporozoites infect liver cells (2) and mature into liver schizonts (3), which rupture and release merozoites (4). Merozoites infect red blood cells (5) and differentiate into trophozoites. Ring stage trophozoites mature into erythrocytic schizont, and its rupture releases merozoites (6). Some trophozoites mature into sexual gametocytes (7). Blood‐stage merozoites and trophozoites are responsible for clinical manifestations. Gametocytes, male and female, are ingested by mosquitoes during a blood meal (8). In mosquito's stomach, male gametocytes penetrate female gametocytes generating zygotes (9). These become ookinetes (10) which invade the midgut wall of mosquito and differentiate into oocysts (11). Oocysts grow, rupture and release sporozoites (12), which make their own way to salivary glands. The life cycle ends with the inoculation of sporozoites (1) into a new human host.
Figure 4. The life cycle of T. gondii. (a) Enteric reproduction of T. gondii in cats. (1) Tachyzoites in the lumen of the intestine invade EC, here, male and female gamonts are developed. (2) Male gamonts produce microgamonts that can swim to fertilise (3) female macrogamonts and form zygotes. (4) Zygotes mature and expel unsporulated oocysts that are shed in cats faeces. (5) Unsporulated oocysts mature and give rise to sporulated oocysts containing two sporocysts with four sporozoites. (b) Schizogony of T. gondii. (6) Sporulated oocysts are ingested by humans, rodents and livestock (cats can also get infected), bradyzoites are released and rapidly disseminate in the host body and transform into tachyzoites (the same morphology as bradyzoites but with a higher rate of division). (7) Tachyzoites invade muscle or neural tissues and transform into cyst bradyzoites. (8) As well, tachyzoites can invade immune cells to form schizonts and divide until the cell explodes and more tachyzoites are released to the blood stream (9) Tachyzoites can break the placental barrier and infect foetus in pregnant women. (10) Cyst bradyzoites can infect humans and other animals if eaten (infected raw/undercooked meat) completing the life cycle.
close

References

Abbas AK, Lichtman AH and Pillai S (2012) Cellular and Molecular Immunology. Philadelphia, PA: Saunders/Elsevier.

Aga E, Katschinski DM, van Zandbergen G, et al. (2002) Inhibition of the spontaneous apoptosis of neutrophil granulocytes by the intracellular parasite Leishmania major. Journal of Immunology 169: 898–905.

Allenbach C, Launois P, Mueller C and Tacchini‐Cottier F (2008) An essential role for transmembrane TNF in the resolution of the inflammatory lesion induced by Leishmania major infection. European Journal of Immunology 38 (3): 720–731.

Alvar J, Vélez ID, Bern C, et al. (2012) Leishmaniasis worldwide and global estimates of its incidence. PLoS One 7 (5): e35671.

Andrade WA, Souza MDC, Martinez ER, et al. (2013) Combined action of nucleic acid‐sensing toll‐like receptors (TLRs) and TLR11/TLR12 heterodimers imparts resistance to Toxoplasma gondii in mice. Cell Host & Microbe 13 (1): 42–53.

Ansong D, Asante KP, Vekemans J, et al. (2011) T cell responses to the RTS,S/AS01E and RTS,S/AS02D malaria candidate vaccines administered according to different schedules to Ghanaian children. PLoS One 6 (4): e18891.

Araujo FG (1992) Depletion of CD4+ T cells but not inhibition of the protective activity of IFN‐gamma prevents cure of toxoplasmosis mediated by drug therapy in mice. Journal of Immunology 149 (9): 3003–3007.

Arce‐Fonseca M, Ballinas‐Verdugo MA, Zenteno ERA, et al. (2013) Specific humoral and cellular immunity induced by Trypanosoma cruzi DNA immunization in a canine model. Veterinary Research 44 (1): 15.

Arnold L, Tyagi RK, Mejia P, et al. (2010) Analysis of innate defences against Plasmodium falciparum in immunodeficient mice. Malaria Journal 9: 197.

Bansal D, Ave P, Kerneis S, et al. (2009) An ex‐vivo human intestinal model to study Entamoeba histolytica pathogenesis. PLoS Neglected Tropical Diseases 3 (11): e551.

Barrias ES, de Carvalho TMU and De Souza W (2013) Trypanosoma cruzi: entry into mammalian host cells and parasitophorous vacuole formation. Frontiers in Immunology 4: 186.

Bautista‐López NL, Ndao M, Camargo FV, et al. (2017) Characterization and diagnostic application of Trypanosoma cruzi trypomastigote excreted‐secreted antigens shed in extracellular vesicles released from infected mammalian cells. Journal of Clinical Microbiology 55 (3): 744–758.

Belkaid Y, Hoffmann KF, Mendez S, Kamhawi S and Udey MC (2001) The role of interleukin (IL)‐10 in the persistence of Leishmania major in the skin after healing and the therapeutic potential of anti‐IL‐10 receptor antibody for sterile cure. Journal of Experimental Medicine 194 (10): 1497–1506. http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=2193677.

Bern C (2015) Chagas′ disease. New England Journal of Medicine 373 (19): 1881–1882.

Bertholet S, Goldszmid R, Morrot A, et al. (2006) Leishmania antigens are presented to CD8 + ^ T cells by a transporter associated with antigen processing‐independent pathway in vitro and in vivo. Journal of Immunology 177 (6): 3525–3533.

Borghi SM, Fattori V, Conchon‐Costa I, et al. (2017) Leishmania infection: painful or painless? Parasitology Research 116 (2): 465–475.

Bull PC, Kortok M, Kai O, et al. (2000) Plasmodium falciparum‐infected erythrocytes: agglutination by diverse Kenyan plasma is associated with severe disease and young host age. Journal of Infectious Diseases 182 (1): 252–259.

Cacciò SM and Ryan U (2008) Molecular epidemiology of giardiasis. Molecular and Biochemical Parasitology 160 (2): 75–80.

Carrero JC, Díaz MY, Viveros M, et al. (1994) Human secretory immunoglobulin A anti‐Entamoeba histolytica antibodies inhibit adherence of amebae to MDCK cells. Infection and Immunity 62 (2): 764–767.

Chadee K and Meerovitch E (1984) The pathogenesis of experimentally induced amebic liver abscess in the gerbil (Meriones unguiculatus). American Journal of Pathology 117 (1): 71–80.

Ciccarelli A, Araujo L, Batlle A and Lombardo E (2007) Effect of haemin on growth, protein content and the antioxidant defence system in Trypanosoma cruzi. Parasitology 134 (7): 959–965.

Claser C, De Souza JB, Thorburn SG, et al. (2017) Host resistance to plasmodium‐induced acute immune pathology is regulated by interleukin‐10 receptor signaling. Infection and Immunity 85 (6): e00941‐00916.

Correa D, CaÑEdo‐Solares I, Ortiz‐AlegrÍA LB, Caballero‐Ortega H and Rico‐Torres CP (2007) Congenital and acquired toxoplasmosis: diversity and role of antibodies in different compartments of the host. Parasite Immunology 29 (12): 651–660.

Dann SM, Manthey CF, Le C, et al. (2015) IL‐17A promotes protective IgA responses and expression of other potential effectors against the lumen‐dwelling enteric parasite Giardia. Experimental Parasitology 156 (Supplement C): 68–78.

Davis PH, Zhang X, Guo J, Townsend RR and Stanley SL (2006) Comparative proteomic analysis of two Entamoeba histolytica strains with different virulence phenotypes identifies peroxiredoxin as an important component of amoebic virulence. Molecular Microbiology 61 (6): 1523–1532.

De Souza W, De Carvalho TMU and Barrias ES (2010) Review on Trypanosoma cruzi: host cell interaction. International Journal of Cell Biology 2010: 295394.

Denkers EY, Yap G, Scharton‐Kersten T, et al. (1997) Perforin‐mediated cytolysis plays a limited role in host resistance to Toxoplasma gondii. Journal of Immunology 159 (4): 1903.

Dreesen L, De Bosscher K, Grit G, et al. (2014) Giardia muris infection in mice is associated with a protective interleukin 17A response and induction of peroxisome proliferator‐activated receptor alpha. Infection and Immunity 82 (8): 3333–3340.

Dunay IR, Fuchs A and Sibley LD (2010) Inflammatory monocytes but not neutrophils are necessary to control infection with Toxoplasma gondii in mice. Infection and Immunity 78 (4): 1564–1570.

Dziadek B, Gatkowska J, Brzostek A, et al. (2009) Toxoplasma gondii: the immunogenic and protective efficacy of recombinant ROP2 and ROP4 rhoptry proteins in murine experimental toxoplasmosis. Experimental Parasitology 123 (1): 81–89.

Elnekave K, Siman‐Tov R and Ankri S (2003) Consumption of L‐arginine mediated by Entamoeba histolytica L‐arginase (EhArg) inhibits amoebicidal activity and nitric oxide production by activated macrophages. Parasite Immunology 25 (11–12): 597–608.

Faria DR, Souza PE, Durães FV, et al. (2009) Recruitment of CD8(+) T cells expressing granzyme A is associated with lesion progression in human cutaneous leishmaniasis. Parasite Immunology 31 (8): 432–439.

Fink MY and Singer SM (2017) The intersection of immune responses, microbiota, and pathogenesis in giardiasis. Trends in Parasitology 33 (11): 901–913.

Gazzinelli R, Kalantari P, Fitzgerald KA and Golenbock DT (2014) Innate sensing of malaria parasites. Nature Reviews. Immunology 14 (11): 744–757.

Gomes PS, Bhardwaj J, Rivera‐Correa J, Freire‐De‐Lima CG and Morrot A (2016) Immune escape strategies of malaria parasites. Frontiers in Microbiology 7: 1617.

Guo X, Stroup SE and Houpt ER (2008) Persistence of Entamoeba histolytica infection in CBA mice owes to intestinal IL‐4 production and inhibition of protective IFN‐gamma. Mucosal Immunology 1 (2): 139–146.

Guo X, Barroso L, Becker SM, et al. (2009) Protection against intestinal amebiasis by a recombinant vaccine is transferable by T cells and mediated by gamma interferon. Infection and Immunity 77 (9): 3909–3918.

Guo X, Barroso L, Lyerly DM, Petri WA and Houpt ER (2011) CD4+ and CD8+ T cell‐ and IL‐17‐mediated protection against Entamoeba histolytica Induced by a recombinant vaccine. Vaccine 29 (4): 772–777.

Haque R, Mondal D, Karim A, et al. (2009) Prospective case–control study of the association between common enteric protozoal parasites and diarrhea in Bangladesh. Clinical Infectious Diseases 48 (9): 1191–1197.

Helegbe GK, Huy NT, Yanagi T, et al. (2009) Rate of red blood cell destruction varies in different strains of mice infected with Plasmodium berghei‐ANKA after chronic exposure. Malaria Journal 8 (1): 91.

Helk E, Bernin H, Ernst T, et al. (2013) TNFα‐mediated liver destruction by Kupffer cells and Ly6Chi monocytes during Entamoeba histolytica infection. PLoS Pathogens 9 (1): e1003096.

Horn D (2014) Antigenic variation in African trypanosomes. Molecular and Biochemical Parasitology 195 (2): 123–129.

Hou Y, Mortimer L and Chadee K (2010) Entamoeba histolytica cysteine proteinase 5 binds integrin on colonic cells and stimulates NFκB‐mediated pro‐inflammatory responses. Journal of Biological Chemistry 285 (46): 35497–35504.

Ivory CPA, Prystajecky M, Jobin C and Chadee K (2008) Toll‐like receptor 9‐dependent macrophage activation by Entamoeba histolytica DNA. Infection and Immunity 76 (1): 289–297.

Kester KE, Cummings JF, Ofori‐Anyinam O, et al. (2009) Randomized, double‐blind, phase 2a trial of falciparum malaria vaccines RTS,S/AS01B and RTS,S/AS02A in malaria‐naive adults: safety, efficacy, and immunologic associates of protection. Journal of Infectious Diseases 200 (3): 337–346.

Kima PE, Ruddle NH and McMahon‐Pratt D (1997) Presentation via the class I pathway by Leishmania amazonensis‐infected macrophages of an endogenous leishmanial antigen to CD8+ T Cells. Journal of Immunology 159 (4): 1828.

Koblansky AA, Jankovic D, Oh H, et al. (2013) Recognition of profilin by toll‐like receptor 12 is critical for host resistance to Toxoplasma gondii. Immunity 38 (1): 119–130.

Koo S‐J, Chowdhury IH, Szczesny B, Wan X and Garg NJ (2016) Macrophages promote oxidative metabolism to drive nitric oxide generation in response to Trypanosoma cruzi. Infection and Immunity 84 (12): 3527–3541.

Kropf P, Freudenberg MA, Modolell M, et al. (2004) Toll‐like receptor 4 contributes to efficient control of infection with the protozoan parasite Leishmania major. Infection and Immunity 72 (4): 1920–1928.

Langford TD, Housley MP, Boes M, et al. (2002) Central importance of immunoglobulin A in host defense against Giardia spp. Infection and Immunity 70 (1): 11–18.

Laucella SA, Postan M, Martin D, et al. (2004) Frequency of interferon‐γ‐producing T cells specific for Trypanosoma cruzi inversely correlates with disease severity in chronic human Chagas Disease. Journal of Infectious Diseases 189 (5): 909–918.

Lauwaet T, Davids BJ, Reiner DS and Gillin FD (2007) Encystation of Giardia lamblia: a model for other parasites. Current Opinion in Microbiology 10 (6): 554–559.

Li E, Zhou P, Petrin Z and Singer SM (2004) Mast cell‐dependent control of Giardia lamblia infections in mice. Infection and Immunity 72 (11): 6642–6649.

Lidani KCF, Bavia L, Ambrosio AR and de Messias‐Reason IJ (2017) The complement system: a prey of Trypanosoma cruzi. Frontiers in Microbiology 8: 607.

Liese J, Schleicher U and Bogdan C (2007) TLR9 signaling is essential for the innate NK cell response in murine cutaneous leishmaniasis. European Journal of Immunology 37 (12): 3424–3434.

Lopez‐Romero G, Quintero J, Astiazarán‐García H and Velazquez C (2015) Host defences against Giardia lamblia. Parasite Immunology 37 (8): 394–406.

Luján HD and Svärd S (2011) Giardia a Model Organism. Wien/New York: Springer.

Maspi N, Ghaffarifar F, Dalimi A, et al. (2017) Comparative assessment of induced immune responses following intramuscular immunization with fusion and cocktail of LeIF, LACK and TSA genes against cutaneous leishmaniasis in BALB/c mice. Archivum Immunologiae et Therapiae Experimentalis. https://doi.org/10.1007/s00005‐017‐0484‐4

Miyahira Y, Takashima Y, Kobayashi S, et al. (2005) Immune responses against a single CD8(+)‐T‐cell epitope induced by virus vector vaccination can successfully control Trypanosoma cruzi infection. Infection and Immunity 73 (11): 7356–7365.

Montoya JG and Liesenfeld O (2004) Toxoplasmosis. Lancet 363 (9425): 1965–1976.

Moreira OC, Ramírez JD, Velázquez E, et al. (2013) Towards the establishment of a consensus real‐time qPCR to monitor Trypanosoma cruzi parasitemia in patients with chronic Chagas disease cardiomyopathy: a substudy from the BENEFIT trial. Acta Tropica 125 (1): 23–31.

Müller I, Kropf P, Louis JA and Milon G (1994) Expansion of gamma interferon‐producing CD8+ T cells following secondary infection of mice immune to Leishmania major. Infection and Immunity 62 (6): 2575–2581.

Nateghi Rostami M, Keshavarz H, Edalat R, et al. (2010) CD8+ T cells as a source of IFN‐γ production in human cutaneous leishmaniasis. PLoS Neglected Tropical Diseases 4 (10): e845.

Ngobeni R, Abhyankar MM, Jiang NM, et al. (2017) Entamoeba histolytica‐encoded homolog of macrophage migration inhibitory factor contributes to mucosal inflammation during amebic colitis. Journal of Infectious Diseases 215 (8): 1294–1302.

Painter JE, Gargano JW, Collier SA, Yoder JS and Centers for Disease Control & Prevention (2015) Giardiasis surveillance – United States, 2011–2012. MMWR Supplements 64 (3): 15–25.

Pappas G, Roussos N and Falagas ME (2009) Toxoplasmosis snapshots: global status of Toxoplasma gondii seroprevalence and implications for pregnancy and congenital toxoplasmosis. International Journal for Parasitology 39 (12): 1385–1394.

Perez‐Mazliah D and Langhorne J (2014) CD4 T‐cell subsets in malaria: TH1/TH2 revisited. Frontiers in Immunology 5: 671.

Persson CM, Lambert H, Vutova PP, et al. (2009) Transmission of Toxoplasma gondii from infected dendritic cells to natural killer cells. Infection and Immunity 77 (3): 970–976.

Plattner F, Yarovinsky F, Romero S, et al. (2008) Toxoplasma profilin is essential for host cell invasion and TLR11‐dependent induction of an interleukin‐12 response. Cell Host & Microbe 3 (2): 77–87.

Plebanski M and Hill AVS (2000) The immunology of malaria infection. Current Opinion in Immunology 12 (4): 437–441.

Prucca CG, Slavin I, Quiroga R, et al. (2008) Antigenic variation in Giardia lamblia is regulated by RNA interference. Nature 456 (7223): 750–754.

Que X and Reed SL (1997) The role of extracellular cysteine proteinases in pathogenesis of Entamoeba histolytica invasion. Parasitology Today 13 (5): 190–194.

Ravdin JI, Abd‐Alla MD, Welles SL, Reddy S and Jackson TFHG (2003) Intestinal antilectin immunoglobulin A antibody response and immunity to Entamoeba dispar infection following cure of amebic liver abscess. Infection and Immunity 71 (12): 6899–6905.

Roitt I, Brostoff J and Male D (2001) Immunology. St. Louis, MO: Mosby.

Roncolato EC, Teixeira JE, Barbosa JE, Zambelli Ramalho LN and Huston CD (2015) Immunization with the Entamoeba histolytica surface metalloprotease EhMSP‐1 protects hamsters from amebic liver abscess. Infection and Immunity 83 (2): 713–720.

Rottenberg ME, Riarte A, Sporrong L, et al. (1995) Outcome of infection with different strains of Trypanosoma cruzi in mice lacking CD4 and/or CD8. Immunology Letters 45 (1–2): 53–60.

Roxström‐Lindquist K, Palm D, Reiner D, Ringqvist E and Svärd SG (2006) Giardia immunity: an update. Trends in Parasitology 22 (1): 26–31.

Scott P, Artis D, Uzonna J and Zaph C (2004) The development of effector and memory T cells in cutaneous leishmaniasis: the implications for vaccine development. Immunological Reviews 201 (1): 318–338.

Seydel KB, Zhang T and Stanley SL (1997) Neutrophils play a critical role in early resistance to amebic liver abscesses in severe combined immunodeficient mice. Infection and Immunity 65 (9): 3951–3953.

Sherling ES and van Ooij C (2016) Host cell remodeling by pathogens: the exomembrane system in Plasmodium‐infected erythrocytes. FEMS Microbiology Reviews 40 (5): 701–721.

Silva JS, Machado FS and Martins GA (2003) The role of nitric oxide in the pathogenesis of Chagas disease. Frontiers in Bioscience 8: s314–s325.

Singer SM and Nash TE (2000) T‐cell‐dependent control of acute Giardia lamblia infections in mice. Infection and Immunity 68 (1): 170–175.

Sousa LM, Carneiro MB, Resende ME, et al. (2014) Neutrophils have a protective role during early stages of Leishmania amazonensis infection in BALB/c mice. Parasite Immunology 36 (1): 13–31.

Tanowitz HB and Weiss LM (2017) A new development in Trypanosoma cruzi detection. Journal of Clinical Microbiology 55 (3): 690–692.

Uzonna JE, Joyce KL and Scott P (2004) Low dose Leishmania major promotes a transient T helper cell type 2 response that is down‐regulated by interferon gamma‐producing CD8+ T cells. Journal of Experimental Medicine 199 (11): 1559–1566.

Vasconcelos JR, Hiyane M, Marinho C, et al. (2004) Protective immunity against Trypanosoma cruzi infection in a highly susceptible mouse strain after vaccination with genes encoding the amastigote surface protein‐2 and trans‐sialidase. Human Gene Therapy 15 (9): 878–886.

Velazquez C, Shibayama‐Salas M, Aguirre‐Garcia J, Tsutsumi V and Calderon J (1998) Role of neutrophils in innate resistance to Entamoeba histolytica liver infection in mice. Parasite Immunology 20 (6): 255–262.

Villarino N and Schmidt NW (2013) CD8(+) T cell responses to plasmodium and intracellular parasites. Current Immunology Reviews 9 (3): 169–178.

Walther M, Woodruff J, Edele F, et al. (2006) Innate immune responses to human malaria: heterogeneous cytokine responses to blood‐stage Plasmodium falciparum correlate with parasitological and clinical outcomes. Journal of Immunology 177 (8): 5736–5745.

Wang W, Keller K and Chadee K (1994) Entamoeba histolytica modulates the nitric oxide synthase gene and nitric oxide production by macrophages for cytotoxicity against amoebae and tumour cells. Immunology 83 (4): 601–610.

Wang W and Chadee K (1995) Entamoeba histolytica suppresses gamma interferon‐induced macrophage class II major histocompatibility complex Ia molecule and I‐A beta mRNA expression by a prostaglandin E2‐dependent mechanism. Infection and Immunity 63 (1089–3).

Watanabe K, Gilchrist CA, Uddin MJ, et al. (2017) Microbiome‐mediated neutrophil recruitment via CXCR2 and protection from amebic colitis. PLoS Pathogens 13 (8): e1006513.

White NJ, Pukrittayakamee S, Hien TT, et al. (2014) Malaria. Lancet 383 (9918): 723–735.

WHO (2015) WHO Estimates of the Global Burden of Foodborne Diseases: Foodborne Disease Burden Epidemiology Reference Group 2007–2015. Geneva: World Health Organization.

WHO (2016) World Malaria Report 2016. Geneva: World Health Organization.

WHO (2017) Chagas Disease. Geneva: World Health Organization.

van Zandbergen G, Hermann N, Laufs H, Solbach W and Laskay T (2002) Leishmania promastigotes release a granulocyte chemotactic factor and induce interleukin‐8 release but inhibit gamma interferon‐inducible protein 10 production by neutrophil granulocytes. Infection and Immunity 70 (8): 4177–4184.

Zhou J, Feng G, Beeson J, et al. (2015) CD14(hi)CD16+ monocytes phagocytose antibody‐opsonised Plasmodium falciparum infected erythrocytes more efficiently than other monocyte subsets, and require CD16 and complement to do so. BMC Medicine 13: 154.

Zimmermann S, Murray PJ, Heeg K and Dalpke AH (2006) Induction of suppressor of cytokine signaling‐1 by Toxoplasma gondii contributes to immune evasion in macrophages by blocking IFN‐gamma signaling. Journal of Immunology 176 (3): 1840–1847.

Further Reading

Adam RD (2001) Biology of Giardia lamblia. Clinical Microbiology Reviews 14(3): 447–475.

Bethony JM, Cole RN, Guo X, et al.. (2011) Vaccines to combat the neglected tropical diseases. Immunological Reviews 239 (1): 237–270.

Dumonteil E, Bottazzi ME, Zhan B, et al.. (2012) Accelerating the development of a therapeutic vaccine for human Chagas disease: rationale and prospects. Expert Review of Vaccines 11 (9). 10.1586/erv.12.85.

Munoz M, Liesenfeld O, and Heimesaat MM (2011) Immunology of Toxoplasma gondii. Immunological Reviews 240 (1): 269–285.

Murphy K, Weaver C (2016) Janeway's Immunobiology, 9th edn. New York: Garland Science/Taylor & Francis Group, LLC.

Quach J, St-Pierre J, and Chadee K (2014) The future for vaccine development against Entamoeba histolytica. Human Vaccines & Immunotherapeutics 10 (6): 1514–1521.

Scorza BM, Carvalho EM, and Wilson ME (2017) Cutaneous Manifestations of Human and Murine Leishmaniasis. International Journal of Molecular Sciences 18 (6): 1296.

Silvie O, Amino R, and Hafalla JC (2017) Tissue‐specific cellular immune responses to malaria pre‐erythrocytic stages. Curr Opin Microbiol 40: 160–167.

Contact Editor close
Submit a note to the editor about this article by filling in the form below.

* Required Field

How to Cite close
Velazquez, Carlos, Dominguez, Victor, Garzon, Thania, and Rascon, Raul(Feb 2018) Immunity to Protozoa. In: eLS. John Wiley & Sons Ltd, Chichester. http://www.els.net [doi: 10.1002/9780470015902.a0000483.pub2]