Skip to main content
SpringerLink
Log in

Phagocytosis in Entamoeba histolytica

  • Chapter
  • First Online:
Amebiasis

Abstract

Phagocytosis is one of the essential processes that is necessary for the survival and pathogenicity of Entamoeba histolytica. E. histolytica is known to phagocytose red blood cells (RBC), bacteria and other unicellular organisms, immune cells, and apoptotic cells during either proliferation in the gut or invasion in intestinal and extraintestinal tissues. Molecular pathways are not clear about molecular details in E. histolytica and are thought to be different from those known in other systems. In this chapter we describe our current understanding of molecular mechanisms of phagocytosis in E. histolytica and highlight new avenues for research for future drug development.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Log in via an institution
Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 169.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 219.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 219.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

References

  1. Bracha R, Kobiler D, Mirelman D (1982) Attachment and ingestion of bacteria by trophozoites of Entamoeba histolytica. Infect Immun 36:396–406

    CAS  PubMed Central  PubMed  Google Scholar 

  2. Huston CD, Boettner DR, Miller-Sims V, Petri WA Jr (2003) Apoptotic killing and phagocytosis of host cells by the parasite Entamoeba histolytica. Infect Immun 71:964–972

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  3. Tsutsumi V et al (1992) Entamoeba histolytica: erythrophagocytosis, collagenolysis, and liver abscess production as virulence markers. Trans R Soc Trop Med Hyg 86:170–172

    Article  CAS  PubMed  Google Scholar 

  4. Orozco E, Guarneros G, Martinez-Palomo A, Sanchez T (1983) Entamoeba histolytica. Phagocytosis as a virulence factor. J Exp Med 158:1511–1521

    Article  CAS  PubMed  Google Scholar 

  5. Martinez-Palomo A, Gonzales-Robles A, Chavez B et al (1985) Structural bases of the cytolytic mechanism of Entamoeba histolytica. J Protozool 32(1):166–175

    Article  CAS  PubMed  Google Scholar 

  6. Petri WA, Haque R, Mann BJ (2002) The bittersweet interface of parasite and host: lectin carbohydrate interactions during tissue invasion by the parasite Entamoeba histolytica. Annu Rev Microbiol 56:39–64

    Article  CAS  PubMed  Google Scholar 

  7. Sahoo N et al (2004) Calcium binding protein 1 of the protozoan parasite Entamoeba histolytica interacts with actin and is involved in cytoskeleton dynamics. J Cell Sci 117:3625–3634

    Article  CAS  PubMed  Google Scholar 

  8. Swanson JA (2008) Shaping cups into phagosomes and macropinosomes. Nat Rev Mol Cell Biol 9:639–649

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  9. Flannagan RS, Jaumouille V, Grinstein S (2012) The cell biology of phagocytosis. Annu Rev Pathol Mech Dis 7:61–98

    Article  CAS  Google Scholar 

  10. Aderem A, Underhill DM (1999) Mechanism of phagocytosis in macrophages. Annu Rev Immunol 17:593–623

    Article  CAS  PubMed  Google Scholar 

  11. Schlesinger LS, Bellinger-Kawahara CG, Payne NR, Horwitz MA (1990) Phagocytosis of Mycobacterium tuberculosis is mediated by human monocyte complement receptors and complement component C3. J Immunol 144:2771–2780

    CAS  PubMed  Google Scholar 

  12. Swanson JA et al (1999) A contractile activity that closes phagosomes in macrophages. J Cell Sci 112:307–316

    CAS  PubMed  Google Scholar 

  13. Fitzer-Attas CJ et al (2000) Fcγ receptor-mediated phagocytosis in macrophages lacking the Src family tyrosine kinases Hck, Fgr, and Lyn. J Exp Med 191:669–681

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  14. Leverrier Y, Okkenhaug K, Sawyer C, Bilancio A, Vanhaesebroeck B, Ridley AJ (2003) Class I phosphoinositide 3-kinase p110β is required for apoptotic cell and Fcγ receptor-mediated phagocytosis by macrophages. J Biol Chem 278:38437–38442

    Article  CAS  PubMed  Google Scholar 

  15. Tohyama Y, Yamamura H (2009) Protein tyrosine kinase, Syk: a key player in phagocytic cells. J Biochem (Tokyo) 145:267–273

    Article  CAS  Google Scholar 

  16. Marshall JG et al (2001) Restricted accumulation of phosphatidylinositol 3-kinase products in a plasmalemmal subdomains during Fcγ receptor-mediated phagocytosis. J Cell Biol 153:1369–1380

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  17. Baumeister MA, Martinu L, Rossman KL, Sondek J, Lemmon MA, Chou MM (2003) Loss of phosphatidylinositol 3-phosphate binding by C-terminal Tiam-1 pleckstrin homology domain prevents in vivo Rac 1 activation without affecting membrane targeting. J Biol Chem 278:11457–11464

    Article  CAS  PubMed  Google Scholar 

  18. Takai Y, Sasaki T, Matozaki T (2001) Small GTP-binding proteins. Physiol Rev 81:153–208

    CAS  PubMed  Google Scholar 

  19. Venkateswarlu K, Cullen PJ (2000) Signalling vis ADP-ribosylation factor 6 lies downstream of phosphatidylinositide-3 kinase. Biochem J 345:719–724

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  20. Patel JC, Hall A, Caron E (2002) Vav regulates activation of Rac but not Cdc42 during FcγR-mediated phagocytosis. Mol Biol Cell 13:1215–1226

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  21. Cox D, Tseng CC, Bjekic G, Greenberg S (1999) A requirement for phosphatidylinositol 3-kinase in pseudopod extension. J Biol Chem 274:1240–1247

    Article  CAS  PubMed  Google Scholar 

  22. Araki N, Johnson MT, Swanson JA (1996) A role for phosphoinositide 3-kinase in the completion of macropinocytosis and phagocytosis by macrophages. J Cell Biol 135:1249–1260

    Article  CAS  PubMed  Google Scholar 

  23. Booth JW, Trimble WS, Grinstein S (2001) Membrane dynamics in phagocytosis. Semin Immunol 13:357–364

    Article  CAS  PubMed  Google Scholar 

  24. Allen LH, Aderem A (1995) A role for MARCKS, the alpha isozyme of protein kinase C and myosin I in zymosan phagocytosis by macrophages. J Exp Med 182:829–840

    Article  CAS  PubMed  Google Scholar 

  25. Diakonova M, Bokoch G, Swanson JA (2002) Dynamics of cytoskeletal proteins during Fcgamma receptor-mediated phagocytosis in macrophages. Mol Biol Cell 13:402–411

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  26. Cox D et al (2002) Myosin X is a downstream effector of PI(3)K during phagocytosis. Nat Cell Biol 4:469–477

    CAS  PubMed  Google Scholar 

  27. Berg JS, Derfler BH, Pennisi CM, Corey DP, Cheney RE (2000) Myosin-X, a novel myosin with pleckstrin homology domains, associates with regions of dynamic actin. J Cell Sci 113:3439–3451

    CAS  PubMed  Google Scholar 

  28. Homma K, Saito J, Ikebe R, Ikebe M (2001) Motor function and regulation of myosin X. J Biol Chem 276:34348–34354

    Article  CAS  PubMed  Google Scholar 

  29. Titus MA (1999) A class VII unconventional myosin is required for phagocytosis. Curr Biol 9:1297–1303

    Article  CAS  PubMed  Google Scholar 

  30. Tuxworth RI et al (2001) A role for myosin VII in dynamic cell adhesion. Curr Biol 11:318–329

    Article  CAS  PubMed  Google Scholar 

  31. Hancock JF (2003) Ras proteins: different signals from different locations. Nat Rev Mol Cell Biol 4:373–384

    Article  CAS  PubMed  Google Scholar 

  32. Jaffe AB, Hall A (2005) Rho GTPases: biochemistry and biology. Annu Rev Cell Dev Biol 21:247–269

    Article  CAS  PubMed  Google Scholar 

  33. Miki H, Suetsugu S, Takenawa T (1998) WAVE, a novel WASP-family protein involved in actin reorganization induced by Rac. EMBO J 17:6932–6941

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  34. Tolias KF et al (2000) Type Ia phosphatidylinositol-4-phosphate 5-kinase mediates Rac-dependent actin assembly. Curr Biol 10:153–156

    Article  CAS  PubMed  Google Scholar 

  35. Edwards DC, Sanders LC, Bokoch GM, Gill GM (1999) Activation of LIM-kinase by Pak1 couplesRac/Cdc42 GTPase signalling to actin cytoskeletal dynamics. Nat Cell Biol 1:253–259

    Article  CAS  PubMed  Google Scholar 

  36. Beemiller P, Hoppe AD, Swanson JA (2006) A phosphatidylinositol-3-kinase-dependent signal transition regulates ARF1 and ARF6 during Fcγ receptor-mediated phagocytosis. PLoS Biol 4:e162

    Article  PubMed Central  PubMed  Google Scholar 

  37. Liberali P et al (2008) The closure of Pak1-dependent macropinosomes requires the phosphorylation of CtBP1/BARS. EMBO J 27:970–981

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  38. Hon CC, Nakada-Tsukui K, Nozaki T, Guillen N (2010) Dissecting the actin cytoskeleton from genomic perspective. In: Clark CG, Johnson PJ (eds) Anerobic parasitic protozoa: genomic and molecular biology. Caister Academic Press, Norwich, pp 81–118

    Google Scholar 

  39. Seigneur M, Mounier J, Prevost M-C, Guillen N (2005) A lysine and glutamic acid rich protein, KERP1, from E. histolytica binds human enterocytes. Cell Microbiol 7(4):569–579

    Article  CAS  PubMed  Google Scholar 

  40. Santi-Rocca J, Weber C, Guigon G et al (2008) The lysine and glutamic acid rich protein KERP1 plays a role in E. histolytica liver abscess pathogenesis. Cell Microbiol 10(1):202–217

    CAS  PubMed  Google Scholar 

  41. Garcia-Rivera G, Rodriguez MA, Ocadiz R et al (1999) Entamoeba histolytica: a novel cycteine protease and an adhesion from the 112-kDa surface protein. Mol Microbiol 33(3):556–568

    Article  CAS  PubMed  Google Scholar 

  42. Ocadiz R, Orozco E, Carrillo E et al (2005) EhCP112 is an Entamoeba histolytica secreted cycteine protease that may be involved in the parasite virulence. Cell Microbiol 7(2):221–232

    Article  CAS  PubMed  Google Scholar 

  43. Vats D, Vishwakarma RA, Bhattacharya S, Bhattacharya A (2005) Reduction of cell surface glycosylphosphatidylinositol conjugates in Entamoeba histolytica by antisense blocking of E. histolytica GlcNAc-phosphatidylinositol deacetylase expression: effect on cell proliferation, endocytosis, and adhesion to target cells. Infect Immun 73(12):8381–8392

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  44. Teixeira JE, Heron BT, Huston CD (2008) C1q-and collectin-dependent phagocytosis of apoptotic host cells by the intestinal protozoan E. histolytica. J Infect Dis 198(7):1062–1070

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  45. Laughlin RC, McGugan GC, Powell RR, Welter BH, Temesvari LA (2004) Involvement of raft-like plasma membrane domains of E. histolytica in pinocytosis and adhesion. Infect Immun 72(9):5349–5357

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  46. Goldston AM, Powell RR, Koushik AB, Temesvari LA (2012) Exposure to host ligands correlates with colocalisation of Gal/GalNAc lectin subunits in lipid rafts and phosphatidylinositol (4,5)-bisphosphate signalling in E. histolytica. Eukaryot Cell 11(6):743–751

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  47. Mann BJ (2002) Structure and function of the Entamoeba histolytica Gal/GalNAc lectin. Int Rev Cytol 216:59–80

    Article  CAS  PubMed  Google Scholar 

  48. Boettner DR, Huston CD, Linford AS (2008) Entamoeba histolytica phagocytosis of human erythrocytes involves PATMK, a member of the transmembrane kinase family. PLoS Pathog 4(1):e8

    Article  PubMed Central  PubMed  Google Scholar 

  49. Buss SN et al (2010) Members of the Entamoeba histolytica transmembrane kinase family play non-redundant roles in growth and phagocytosis. Int J Parasitol 40(7):833–843

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  50. Baxt LA, Baker RP, Singh U, Urban S (2008) An E. histolytica rhomboid protease with atypical specificity cleaves a surface lectin involved in phagocytosis and immune evasion. Genes Dev 22(12):1636–1646

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  51. Bailey GB, Day DB, Gasque JW (1985) Rapid polymerisation of Entamoeba histolytica actin induced by interaction with target cells. J Exp Med 162(2):546–558

    Article  CAS  PubMed  Google Scholar 

  52. Jain R et al (2008) Calcium-binding protein 1 of Entamoeba histolytica transiently associates with phagocytic cups in a calcium-independent manner. Cell Microbiol 10(6):1373–1389

    Article  CAS  PubMed  Google Scholar 

  53. Somlata, Bhattacharya S, Bhattacharya A (2011) A C2 domain protein kinase initiates phagocytosis in the protozoan parasite Entamoeba histolytica. Nat Commun 2:230

    Article  CAS  PubMed  Google Scholar 

  54. Somlata, Kamanna S, Agrahari M, Babuta M, Bhattacharya S, Bhattacharya A (2012) Autophosphorylation of Ser428 of EhC2PK plays a critical role in regulating erythrophagocytosis in the parasite Entamoeba histolytica. J Biol Chem 287(14):10844–10852

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  55. Aslam S, Bhattacharya S, Bhattacharya A (2012) The calmodulin-like calcium binding protein EhCaBP3 of Entamoeba histolytica regulates phagocytosis and is involved in actin dynamics. PLoS Pathog. doi:10.1371/journal.ppat.1003055

    PubMed Central  PubMed  Google Scholar 

  56. Ghosh SK, Samuelson J (1996) Involvement of p21racA, phosphoinositide 3-kinase, and vacuolar ATPase in phagocytosis of bacteria and erythrocytes by Entamoeba histolytica: suggestive evidence for coincidental evolution of amebic invasiveness. Infect Immun Gene 173:205–208

    Google Scholar 

  57. Guillen N, Boquet P, Sansonetti P (1998) The small GTP-binding protein RacG regulates uroid formation in the protozoan parasite Entamoeba histolytica. J Cell Sci 111:1729–1739

    CAS  PubMed  Google Scholar 

  58. Aguilar-Rojasa A et al (2005) Entamoeba histolytica: inhibition of cellular functions by overexpression of EhGEF1, a novel Rho/Rac guanine nucleotide exchange factor. Exp Parasitol 109:150–162

    Article  Google Scholar 

  59. González De la Rosa CH et al (2007) EhGEF2, a Dbl-RhoGEF from Entamoeba histolytica has atypical biochemical properties and participates in essential cellular processes. Mol Biochem Parasitol 151:70–80

    Article  PubMed  Google Scholar 

  60. Arias-Romero LE et al (2007) EhGEF3, a novel Dbl family member, regulates EhRacA activation during chemotaxis and capping in Entamoeba histolytica. Cell Motil Cytoskeleton 64(5):390–404

    Article  CAS  PubMed  Google Scholar 

  61. Kettis AA, Lidman K, Fagraeus A (1977) Actin in E. histolytica trophozoites revealed by human actin antibodies. J Parasitol 63:581–583

    Article  CAS  PubMed  Google Scholar 

  62. Meza I, Sabanero M, Cazares F, Bryan J (1983) Isolation and characterization of actin from Entamoeba histolytica. J Biol Chem 258:3936–3941

    CAS  PubMed  Google Scholar 

  63. Voigt H, Olivo JC, Sansonetti P, Guillén N (1999) Myosin IB from Entamoeba histolytica is involved in phagocytosis of human erythrocytes. J Cell Sci 112:1191–1201

    CAS  PubMed  Google Scholar 

  64. Arhets P, Gounon P, Sansonetti P, Guillén N (1995) Myosin II is involved in capping and uroid formation in the human pathogen Entamoeba histolytica. Infect Immun 63(11):4358

    CAS  PubMed Central  PubMed  Google Scholar 

  65. Nakada-Tsukui K, Okada H, Mitra BN, Nozaki T (2009) Phosphatidylinositol-phosphates mediate cytoskeletal reorganization during phagocytosis via a unique modular protein consisting of RhoGEF/DH and FYVE domains in the parasitic protozoon Entamoeba histolytica. Cell Microbiol 11(10):1471–1491

    Article  CAS  PubMed  Google Scholar 

  66. Díaz-Valencia JD et al (2007) Novel structural and functional findings of the ehFLN protein from Entamoeba histolytica. Cell Motil Cytoskeleton 64:880–896

    Article  PubMed  Google Scholar 

  67. Godbold GD, Corbett KD, Mann BJ (2002) A Rho-like small GTPase of Entamoeba histolytica contains an unusual amino acid residue in a conserved GDP-stabilization region and is not a substrate for C3 exoenzyme. Exp Parasitol 101:107–110

    Article  CAS  PubMed  Google Scholar 

  68. Bosch DE, Wittchen ES, Qiu C, Burridge K, Siderovski DP (2011) Unique structural and nucleotide exchange features of the Rho1 GTPase of Entamoeba histolytica. J Biol Chem 286(45):39236–39246

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  69. Labruyère E et al (2002) EhPAK, a member of the p21-activated kinase family, is involved in the control of Entamoeba histolytica migration and phagocytosis. J Cell Sci 116:61–71

    Article  Google Scholar 

  70. Arias Romero EL, Díaz-Valencia JD, de J Almaraz-Barrera M, Rojo-Dominguez A, Vargas M (2006) EhPAK2, a novel p21-activated kinase, is required for collagen invasion and capping in Entamoeba histolytica. Mol Biochem Parasitol 149:17–26

    Article  CAS  PubMed  Google Scholar 

  71. Dutta S, Sardar A, Ray D, Raha S (2007) Molecular and functional characterization of EhPAK3, a p21 activated kinase from Entamoeba histolytica. Gene (Amst) 402(1–2):57–67

    Article  CAS  Google Scholar 

  72. Virel A, Backman L (2006) Characterization of Entamoeba histolytica alpha-actinin. Mol Biochem Parasitol 145(1):11–7

    Article  CAS  PubMed  Google Scholar 

  73. Virel A, Addario B, Backman L (2007) Characterization of Entamoeba histolytica alpha-actinin 2. Mol Biochem Parasitol 154:82–89

    Article  CAS  PubMed  Google Scholar 

  74. Addario B, Huang S, Sauer UH, Backman B (2011) Crystallization and preliminary X-ray analysis of the Entamoeba histolytica α-actinin-2 rod domain. Acta Crystallogr F 67:1214–1217

    Article  CAS  Google Scholar 

  75. Saito-Nakano Y, Yasuda T, Nakada-Tsukui K, Leippe M, Nozaki T (2004) Rab5-associated vacuoles play a unique role in phagocytosis of the enteric protozoan parasite Entamoeba histolytica. J Biol Chem 279:49497–49507

    Article  CAS  PubMed  Google Scholar 

  76. Marion S, Laurent C, Guillén N (2005) Signalization and cytoskeleton activity through myosin IB during the early steps of phagocytosis in Entamoeba histolytica: a proteomic approach. Cell Microbiol 7(10):1504–1518

    Article  CAS  PubMed  Google Scholar 

  77. Majumder S, Lohia A (2008) Entamoeba histolytica encodes unique formins, a subset of which regulates DNA content and cell division. Infect Immun 76(6):2368–2378

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  78. Bosch DE, Yang B, Siderovski DP (2012) Entamoeba histolytica Rho1 regulates actin polymerization through a divergent, diaphanous-related formin. Biochemistry 51:8791–8801

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  79. Byekova YA, Powell RR, Welter BH, Temesvari LA (2010) Localisation of phosphatidylinositol (3,4,5)-triphosphate to phagosomes in Entamoeba histolytica achieved using glutathione S-transferase and green fluorescent protein-tagged lipid biosensors. Infect Immun 78(1):125–137

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  80. Saito-Nakano Y, Loftus BJ, Hall N, Nozaki T (2005) The diversity of Rab GTPases in Entamoeba histolytica. Exp Parasitol 110(3):244–252

    Article  CAS  PubMed  Google Scholar 

  81. Mitra BN, Saito-Nakano Y, Nakada-Tsukui K, Sato D, Nozaki T (2007) Rab11B small GTPase regulates secretion of cysteine proteases in the enteric protozoan parasite Entamoeba histolytica. Cell Microbiol 9(9):2112–2125

    Article  CAS  PubMed  Google Scholar 

  82. Saito-Nakano Y, Mitra BN, Nakada-Tsukui K, Sato D, Nozaki T (2007) Two Rab7 isotypes, EhRab7A and EhRab7B, play distinct roles in biogenesis of lysosomes and phagosomes in the enteric protozoan parasite Entamoeba histolytica. Cell Microbiol 9(7):1796–1808

    Article  CAS  PubMed  Google Scholar 

  83. Teixeira JE, Huston CD (2008) Participation of the serine-rich Entamoeba histolytica protein in amoebic phagocytosis of apoptotic host cells. Infect Immun 76(3):959–966

    Article  CAS  PubMed Central  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. School of Life Sciences Jawahalal Nehru University, New Delhi, India

    Somlata & Alok Bhattacharya

Authors
  1. Somlata
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Alok Bhattacharya
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Alok Bhattacharya .

Editor information

Editors and Affiliations

  1. Department of Parasitology, National Institute of Infectious Diseases, Shinjuku-ku, Tokyo, Japan

    Tomoyoshi Nozaki

  2. Jawaharlal Nehru University, New Delhi, India

    Alok Bhattacharya

Rights and permissions

Reprints and permissions

Copyright information

© 2015 Springer Japan

About this chapter

Cite this chapter

Somlata, Bhattacharya, A. (2015). Phagocytosis in Entamoeba histolytica . In: Nozaki, T., Bhattacharya, A. (eds) Amebiasis. Springer, Tokyo. https://doi.org/10.1007/978-4-431-55200-0_12

Download citation

Publish with us

Policies and ethics

Search

Navigation