2,544
Views
16
CrossRef citations to date
0
Altmetric
Review Article

Balancing in a black box: Potential immunomodulatory roles for TGF-β signaling during blood-stage malaria

ORCID Icon &
Pages 159-169 | Received 04 Sep 2019, Accepted 16 Jan 2020, Published online: 11 Feb 2020

References

  • “World malaria report 2019.,” (World Health Organization, 2019).
  • Olotu A, Fegan G, Wambua J. Seven-year efficacy of RTS,S/AS01 malaria vaccine among young African children. N Engl J Med. 2016;374:2519–2529.
  • Neafsey DE, Juraska M, Bedford T, et al. Genetic diversity and protective efficacy of the RTS,S/AS01 malaria vaccine. N Engl J Med. 2015;373:2025–2037.
  • Tinto H, Otieno W, Gesase S, et al. Long-term incidence of severe malaria following RTS,S/AS01 vaccination in children and infants in Africa: an open-label 3-year extension study of a phase 3 randomised controlled trial. Lancet Infect Dis. 2019;19:821–832.
  • RTS,S clinical trials partnership. Efficacy and safety of RTS,S/AS01 malaria vaccine with or without a booster dose in infants and children in Africa: final results of a phase 3, individually randomised, controlled trial. Lancet. 2015;386:31–45.
  • Sinnis P, Zavala F. The skin: where malaria infection and the host immune response begin. Semin Immunopathol. 2012;34:787–792.
  • Baer K, Klotz C, Kappe SH, et al. Release of hepatic Plasmodium yoelii merozoites into the pulmonary microvasculature. PLoS Pathog. 2007;3:e171.
  • Burda PC, Caldelari R, Heussler VT. Manipulation of the host cell membrane during plasmodium liver stage egress. MBio. 2017;8:e00139–17.
  • Sturm A, Amino R, van de Sand C, et al. Manipulation of host hepatocytes by the malaria parasite for delivery into liver sinusoids. Science. 2006;313:1287–1290.
  • Cowman AF, Healer J, Marapana D, et al. Malaria: biology and disease. Cell. 2016;167:610–624.
  • Mikolajczak SA, Kappe SH. A clash to conquer: the malaria parasite liver infection. Mol Microbiol. 2006;62:1499–1506.
  • Mueller AK, Labaied M, Kappe SH, et al. Genetically modified Plasmodium parasites as a protective experimental malaria vaccine. Nature. 2005;433:164–167.
  • Portugal S, Moebius J, Skinner J, et al. Exposure-dependent control of malaria-induced inflammation in children. PLoS Pathog. 2014;10:e1004079.
  • Wells TN, Burrows JN, Baird JK. Targeting the hypnozoite reservoir of Plasmodium vivax: the hidden obstacle to malaria elimination. Trends Parasitol. 2010;26:145–151.
  • Artavanis-Tsakonas K, Tongren JE, Riley EM. The war between the malaria parasite and the immune system: immunity, immunoregulation and immunopathology. Clin Exp Immunol. 2003;133:145–152.
  • de Souza JB, Hafalla JC, Riley EM, et al. Cerebral malaria: why experimental murine models are required to understand the pathogenesis of disease. Parasitology. 2010;137:755–772.
  • Omer FM, Kurtzhals JA, Riley EM. Maintaining the immunological balance in parasitic infections: a role for TGF-beta? Parasitol Today. 2000;16:18–23.
  • Oh SA, Li MO. TGF-β: guardian of T cell function. J Immunol. 2013;191:3973–3979.
  • Morikawa M, Derynck R, Miyazono K. TGF-beta and the TGF-beta family: context-dependent roles in cell and tissue physiology. Cold Spring Harb Perspect Biol. 2016;8:a021873.
  • Li MO, Flavell RA. TGF-beta: a master of all T cell trades. Cell. 2008;134:392–404.
  • Kulkarni AB, Huh CG, Becker D, et al. Transforming growth factor beta 1 null mutation in mice causes excessive inflammatory response and early death. Proc Natl Acad Sci U S A. 1993;90:770–774.
  • Shull MM, Ormsby I, Kier AB, et al. Targeted disruption of the mouse transforming growth factor-beta 1 gene results in multifocal inflammatory disease. Nature. 1992;359:693–699.
  • Sanjabi S, Oh SA, Li MO. Regulation of the immune response by TGF-beta: from conception to autoimmunity and infection. Cold Spring Harb Perspect Biol. 2017;9:a022236.
  • Silva JS, Twardzik DR, Reed SG. Regulation of trypanosoma cruzi infections in vitro and in vivo by transforming growth factor beta (TGF-beta). J Exp Med. 1991;174:539–545.
  • Barral A, Barral-Netto M, Yong EC, et al. Transforming growth factor beta as a virulence mechanism for Leishmania braziliensis. Proc Natl Acad Sci U S A. 1993;90:3442–3446.
  • Grainger JR, Smith KA, Hewitson JP, et al. Helminth secretions induce de novo T cell Foxp3 expression and regulatory function through the TGF-beta pathway. J Exp Med. 2010;207:2331–2341.
  • Buzoni-Gatel D, Debbabi H, Mennechet FJD, et al. Murine ileitis after intracellular parasite infection is controlled by TGF-beta-producing intraepithelial lymphocytes. Gastroenterology. 2001;120:914–924.
  • de Jong GM, McCall MBB, Dik WA, et al. Transforming growth factor-beta profiles correlate with clinical symptoms and parameters of haemostasis and inflammation in a controlled human malaria infection. Cytokine. 2020;125:154838.
  • Walther M, Woodruff J, Edele F, et al. Innate immune responses to human malaria: heterogeneous cytokine responses to blood-stage Plasmodium falciparum correlate with parasitological and clinical outcomes. J Immunol. 2006;177:5736–5745.
  • Hanisch BR, Bangirana P, Opoka RO, et al. Thrombocytopenia may mediate disease severity in plasmodium falciparum malaria through reduced transforming growth factor beta-1 regulation of proinflammatory and anti-inflammatory Cytokines. Pediatr Infect Dis J. 2015;34:783–788.
  • Wenisch C, Parschalk B, Burgmann H, et al. Decreased serum levels of TGF-beta in patients with acute Plasmodium falciparum malaria. J Clin Immunol. 1995;15:69–73.
  • Chaiyaroj SC, Rutta ASM, Muenthaisong K, et al. Reduced levels of transforming growth factor-beta1, interleukin-12 and increased migration inhibitory factor are associated with severe malaria. Acta Trop. 2004;89:319–327.
  • Perkins DJ, Weinberg JB, Kremsner PG. Reduced interleukin-12 and transforming growth factor-beta1 in severe childhood malaria: relationship of cytokine balance with disease severity. J Infect Dis. 2000;182:988–992.
  • Dodoo D, Omer F, Todd J, et al. Absolute levels and ratios of proinflammatory and anti-inflammatory cytokine production in vitro predict clinical immunity to Plasmodium falciparum malaria. J Infect Dis. 2002;185:971–979.
  • Rovira-Vallbona E, Moncunill G, Bassat Q, et al. Low antibodies against Plasmodium falciparum and imbalanced pro-inflammatory cytokines are associated with severe malaria in Mozambican children: a case-control study. Malar J. 2012;11:181.
  • Ghazanfari N, Mueller SN, Heath WR. Cerebral malaria in mouse and man. Front Immunol. 2018;9.
  • Lourembam SD, Sawian CE, Baruah S. Dysregulation of cytokines expression in complicated falciparum malaria with increased TGF-beta and IFN-gamma and decreased IL-2 and IL-12. Cytokine. 2013;64:503–508.
  • Stephens R, Culleton RL, Lamb TJ. The contribution of Plasmodium chabaudi to our understanding of malaria. Trends Parasitol. 2012;28:73–82.
  • Li C, Seixas E, Langhorne J. Rodent malarias: the mouse as a model for understanding immune responses and pathology induced by the erythrocytic stages of the parasite. Med Microbiol Immunol. 2001;189:115–126.
  • Otsuki H, Kaneko O, Thongkukiatkul A, et al. Single amino acid substitution in Plasmodium yoelii erythrocyte ligand determines its localization and controls parasite virulence. Proc Natl Acad Sci U S A. 2009;106:7167–7172.
  • Nacer A, Movila A, Baer K, et al. Neuroimmunological blood brain barrier opening in experimental cerebral malaria. PLoS Pathog. 2012;8:e1002982.
  • Hunt NH, Grau GE, Engwerda C, et al. Murine cerebral malaria: the whole story. Trends Parasitol. England. 2010;26:272–274.
  • White NJ, Turner GD, Medana IM, et al. The murine cerebral malaria phenomenon. Trends Parasitol. 2010;26:11–15.
  • de Kossodo S, Grau GE. Profiles of cytokine production in relation with susceptibility to cerebral malaria. J Immunol. 1993;151:4811–4820.
  • Omer FM, Riley EM. Transforming growth factor beta production is inversely correlated with severity of murine malaria infection. J Exp Med. 1998;188:39–48.
  • Omer FM, de Souza JB, Riley EM. Differential induction of TGF-beta regulates proinflammatory cytokine production and determines the outcome of lethal and nonlethal Plasmodium yoelii infections. J Immunol. 2003;171:5430–5436.
  • Tsutsui N, Kamiyama T, Mansfield JM. Transforming growth factor β-induced failure of resistance to infection with blood-stage plasmodium chabaudiin mice. Infect Immun. 1999;67:2306–2311.
  • Keswani T, Bhattacharyya A. Differential role of T regulatory and Th17 in Swiss mice infected with Plasmodium berghei ANKA and Plasmodium yoelii. Exp Parasitol. 2014;141:82–92.
  • Kurup SP, Butler NS, Harty JT. T cell-mediated immunity to malaria. Nat Rev Immunol. 2019;19:457–471.
  • Meding SJ, Cheng SC, Simon-Haarhaus B, et al. Role of gamma interferon during infection with Plasmodium chabaudi chabaudi. Infect Immun. 1990;58:3671–3678.
  • Su Z, Stevenson MM. IL-12 is required for antibody-mediated protective immunity against blood-stage Plasmodium chabaudi AS malaria infection in mice. J Immunol. 2002;168:1348–1355.
  • van der Heyde HC, Pepper B, Batchelder J, et al. The time course of selected malarial infections in cytokine-deficient mice. Exp Parasitol. 1997;85:206–213.
  • Su Z, Stevenson MM. Central role of endogenous gamma interferon in protective immunity against blood-stage plasmodium chabaudi AS infection. Infect Immun. 2000;68:4399–4406.
  • Stevenson MM, Riley EM. Innate immunity to malaria. Nat Rev Immunol. 2004;4:169–180.
  • Amani V, Vigário A, Belnoue E, et al. Involvement of IFN-gamma receptor-medicated signaling in pathology and anti-malarial immunity induced by Plasmodium berghei infection. Eur J Immunol. 2000;30:1646–1655.
  • Day NP, Hien T, Schollaardt T, et al. The prognostic and pathophysiologic role of pro- and antiinflammatory cytokines in severe malaria. J Infect Dis. 1999;180:1288–1297.
  • Kurup SP, Obeng-Adjei N, Anthony SM, et al. Regulatory T cells impede acute and long-term immunity to blood-stage malaria through CTLA-4. Nat Med. 2017;23:1220–1225.
  • Perez-Mazliah D, Langhorne J. CD4 T-cell subsets in malaria: TH1/TH2 revisited. Front Immunol. 2014;5:671.
  • Sakaguchi S, Miyara M, Costantino CM, et al. FOXP3+ regulatory T cells in the human immune system. Nat Rev Immunol. 2010;10:490–500.
  • Dhamne C, Chung Y, Alousi AM, et al. Peripheral and Thymic Foxp3+ regulatory T cells in search of origin, distinction, and function. Front Immunol. 2013;4.
  • Liu Y, Zhang P, Li J, et al. A critical function for TGF-beta signaling in the development of natural CD4+CD25+Foxp3+ regulatory T cells. Nat Immunol. 2008;9:632–640.
  • Chen W, Jin W, Hardegen N, et al. Conversion of peripheral CD4+CD25- naive T cells to CD4+CD25+ regulatory T cells by TGF-beta induction of transcription factor Foxp3. J Exp Med. 2003;198:1875–1886.
  • Selvaraj RK, Geiger TL. A kinetic and dynamic analysis of Foxp3 induced in T cells by TGF-beta. J Immunol. 2007;178:7667–7677.
  • Wei J, Duramad O, Perng OA, et al. Antagonistic nature of T helper 1/2 developmental programs in opposing peripheral induction of Foxp3+ regulatory T cells. Proc Natl Acad Sci U S A. 2007;104:18169–18174.
  • Hansen DS, Schofield L, Manchester M. Natural regulatory T cells in malaria: host or parasite allies? PLoS Pathog. 2010;6:e1000771.
  • Finney OC, Riley EM, Walther M. Regulatory T cells in malaria–friend or foe? Trends Immunol. 2010;31:63–70.
  • Couper KN, Blount DG, de Souza JB, et al. Incomplete depletion and rapid regeneration of Foxp3+ regulatory T cells following anti-CD25 treatment in malaria-infected mice. J Immunol. 2007;178:4136–4146.
  • Keswani T, Sarkar S, Sengupta A, et al. Role of TGF-beta and IL-6 in dendritic cells, Treg and Th17 mediated immune response during experimental cerebral malaria. Cytokine. 2016;88:154–166.
  • Scholzen A, Mittag D, Rogerson SJ, et al. Plasmodium falciparum-mediated induction of human CD25Foxp3 CD4 T cells is independent of direct TCR stimulation and requires IL-2, IL-10 and TGFbeta. PLoS Pathog. 2009;5:e1000543.
  • Walther M, Tongren JE, Andrews L, et al. Upregulation of TGF-beta, FOXP3, and CD4+CD25+ regulatory T cells correlates with more rapid parasite growth in human malaria infection. Immunity. 2005;23:287–296.
  • Omer FM, de Souza JB, Corran PH, et al. Activation of transforming growth factor β by malaria parasite-derived metalloproteinases and a thrombospondin-like molecule. J Exp Med. 2003;198:1817–1827.
  • Wahl SM, Hunt DA, Wakefield LM, et al. Transforming growth factor type beta induces monocyte chemotaxis and growth factor production. Proc Natl Acad Sci U S A. 1987;84:5788–5792.
  • Chantry D, Turner M, Abney E, et al. Modulation of cytokine production by transforming growth factor-beta. J Immunol. 1989;142:4295–4300.
  • Ortega-Pajares A, Rogerson SJ. The rough guide to monocytes in malaria infection. Front Immunol. 2018;9.
  • Langhorne J, R. Albano F, Hensmann M, et al. Dendritic cells, pro-inflammatory responses, and antigen presentation in a rodent malaria infection. Immunol Rev. 2004;201:35–47.
  • Jaramillo M, Gowda DC, Radzioch D, et al. Hemozoin increases IFN-gamma-inducible macrophage nitric oxide generation through extracellular signal-regulated kinase- and NF-kappa B-dependent pathways. J Immunol. 2003;171:4243–4253.
  • Bastos KR, Barboza R, Elias RM, et al. Impaired macrophage responses may contribute to exacerbation of blood-stage Plasmodium chabaudi chabaudi malaria in interleukin-12-deficient mice. J Interferon Cytokine Res. 2002;22:1191–1199.
  • Pérez-Mazliah D, Nguyen MP, Hosking C, et al. Follicular helper T cells are essential for the elimination of plasmodium infection. EBioMedicine. 2017;24:216–230.
  • Sebina I, Fogg LG, James KR, et al. IL-6 promotes CD4+ T cell and B cell activation during Plasmodium infection. Parasite Immunol. 2017;39:e12455.
  • Schmitt N, Liu Y, Bentebibel S-E, et al. The cytokine TGF-β co-opts signaling via STAT3-STAT4 to promote the differentiation of human TFH cells. Nat Immunol. 2014;15:856–865.
  • Marshall HD, Ray JP, Laidlaw BJ, et al. The transforming growth factor beta signaling pathway is critical for the formation of CD4 T follicular helper cells and isotype-switched antibody responses in the lung mucosa. Elife. 2015;4:e04851.
  • Cambos M, Belanger B, Jacques A, et al. Natural regulatory (CD4+CD25+FOXP+) T cells control the production of pro-inflammatory cytokines during Plasmodium chabaudi adami infection and do not contribute to immune evasion. Int J Parasitol. 2008;38:229–238.
  • Nie CQ, Bernard NJ, Schofield L, et al. CD4+ CD25+ regulatory T cells suppress CD4+ T-cell function and inhibit the development of Plasmodium berghei-specific TH1 responses involved in cerebral malaria pathogenesis. Infect Immun. 2007;75:2275–2282.
  • Li MO, Wan YY, Flavell RA. T cell-produced transforming growth factor-beta1 controls T cell tolerance and regulates Th1- and Th17-cell differentiation. Immunity. 2007;26:579–591.
  • Butler NS, Harris TH, Blader IJ. Regulation of immunopathogenesis during Plasmodium and Toxoplasma infections: more parallels than distinctions? Trends Parasitol. 2013;29:593–602.