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Journal of Biosciences

, Volume 28, Issue 3, pp 349–358 | Cite as

Host-pathogen interactions during apoptosis

  • Seyed E. HasnainEmail author
  • Rasheeda Begum
  • K. V. A. Ramaiah
  • Sudhir Sahdev
  • E. M. Shajil
  • Tarvinder K. Taneja
  • Manjari Mohan
  • M. Athar
  • Nand K. Sah
  • M. Krishnaveni
Articles

Abstract

Host pathogen interaction results in a variety of responses, which include phagocytosis of the pathogen, release of cytokines, secretion of toxins, as well as production of reactive oxygen species (ROS). Recent studies have shown that many pathogens exert control on the processes that regulate apoptosis in the host. The induction of apoptosis upon infection results from a complex interaction of parasite proteins with cellular host proteins. Abrogation of host cell apoptosis is often beneficial for the pathogen and results in a successful host invasion. However, in some cases, it has been shown that induction of apoptosis in the infected cells significantly imparts protection to the host from the pathogen. There is a strong correlation between apoptosis and the host protein translation machinery: the pathogen makes all possible efforts to modify this process so as to inhibit cell suicide and ensure that it can survive and, in some cases, establish latent infection. This review discusses the significance of various pathways/steps during virus-mediated modulation of host cell apoptosis.

Keywords

Antioxidant baculovirus host-pathogen eIF2α-kinase P35 PKR 

Abbreviations used

AcNPV

Autographa californica nuclear polyhydrosis virus

EMCV

encephalomyocarditis virus

FADD

Fas-associated death domain protein

Wt

wild-type

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References

  1. Balachandran S, Kim C N, Yeh W C, Mak T W, Bhalla K and Barber G N 1998 Activation of the dsRNA-dependent protein kinase, PKR, induces apoptosis through FADD-mediated death signaling;EMBO J. 17 6888–6902CrossRefGoogle Scholar
  2. Balachandran S, Roberts P C, Kipperman T, Bhalla K N, Compans R W, Archer D R and Barber G N 2000 Alpha/beta interferons potentiate virus-induced apoptosis through activation of FADD/caspase-8 death signalling pathway;J. Virol. 74 1513–1523CrossRefGoogle Scholar
  3. Barry M and McFadden G 1998 Apoptosis regulators from DNA viruses;Curr. Opin. Immunol. 10 422–430CrossRefGoogle Scholar
  4. Beattie E, Denzler K L, Tartaglia J, Perkus M E, Paoletti E and Jacobs B L 1995 Reversal of the interferon-sensitive phenotype of a vaccinia virus lacking E3L by expression of the reovirus S4 gene;J. Virol. 69 499–505PubMedPubMedCentralGoogle Scholar
  5. Begum R, Taneja T K, Mohan M, Pathak N, Athar M, Sah N K and Hasnain S E 1999 The control and execution of programmed cell death; inRec. Asp. Cell. App. Rad. (eds) F H A Schneewiees and R N Sharma (Foschungszentrum, Julisch, Gmbh, Germany) pp 23–45Google Scholar
  6. Bertin J, Mendrysa S M, LaCount D J, Gaur S, Krebs J F, Armstrong R C, Tomaselli K J and Friesen P D 1996 Apoptotic suppression by baculovirus P35 involves cleavage by and inhibition of a virus-induced CED-3/ICE-like protease;J. Virol. 70 6251–6259PubMedPubMedCentralGoogle Scholar
  7. Bump N J, Hackett M, Hugunin M, Seshagiri S, Brady K, Chen P, Ferenz C, Franklin S, Ghayur T, Li P, Licari P, Mankovich J, Shi L, Greenberg A H, Miller L K and Wong W W 1995 Inhibition of ICE family proteases by baculovirus antiapoptotic protein p35;Science 269 1885–1888CrossRefGoogle Scholar
  8. Cassady K A, Gross M and Roizman B 1998 The herpes simplex virus US 11 protein effectively compensates for the γl(34-5) gene if present before activation of protein kinase R by precluding its phosphorylation and that of the a subunit of eukaryotic translation initiation factor 2;J. Virol. 72 8620–8626PubMedPubMedCentralGoogle Scholar
  9. Chang H W, Watson J C and Jacobs B L 1992 The E3L gene of vaccinia virus encodes an inhibitor of the interferon-induced, double-stranded RNA-dependent protein kinase;Proc. Natl. Acad. Sci. USA 89 4825–4829CrossRefGoogle Scholar
  10. Chang H Y and Yang X 2000 Proteases for Cell Suicide: Functions and Regulation of Caspases;Microbiol. Mol. Biol. Rev. 5 821–846CrossRefGoogle Scholar
  11. Chatterji U, Ahmad R, Venkaiah B and Hasnain S E 1996 A recombination-efficient baculovirus vector for simultaneous expression of multiple genes;Gene 171 209–213CrossRefGoogle Scholar
  12. Chu W M, Ostertag D, Li Z W, Chang L, Chen Y, Hu Y, Williams B, Perrault J and Karin M 1999 JNK2 and IKK beta are required for activating the innate response to viral infection;Immunity 11 721–731CrossRefGoogle Scholar
  13. Dever T E, Sripriya J R, McLachlin J, Lu J, Fabian R, Kimball S R and Miller L K 1998 Disruption of cellular translation control by a viral truncated eukaryotic translation initiation factor 2 alpha kinase homologue;Proc. Natl. Acad. Sci. USA. 95 4164–4169CrossRefGoogle Scholar
  14. Diaz-Guerra M, Rivas C and Esteban M 1997 Activation of the IFN-inducible enzyme RNase L causes apoptosis of animal cells;Virology 236 354–363CrossRefGoogle Scholar
  15. Fesq H, Bacher M, Nain M and Gemsa D 1994 Programmed cell death (apoptosis) in human monocytes infected by influenza virus;Immunobiology 190 175–182CrossRefGoogle Scholar
  16. Fisher A J, Cruz D W, Zoog J S, Schneider, Paul D F 1999 Crystal structure of baculovirus P35: role of a novel reactive site loop in apoptotic caspase inhibition;EMBO J. 18 2031–2039CrossRefGoogle Scholar
  17. Gale M Jr, Blakely C M, Kwieciszewski B, Tan S L, Dossett M, Tang N M, Korth M J, Polyak S J, Gretch D R and Katze M G 1998 Control of PKR protein kinase by hepatitis C virus nonstructural 5A protein: Molecular mechanisms of kinase regulation;Mol. Cell. Biol. 18 5208–5218CrossRefGoogle Scholar
  18. Gale M Jr, Kwieciszewski B, Dossett M, Nakao H and Katze M G 1999 Anti-apoptotic and oncogenic potentials of hepatitis C virus are linked to interferon resistance by viral repression of the PKR protein kinase;J. Virol. 73 6506–6516PubMedPubMedCentralGoogle Scholar
  19. Gao L Y and Kwaik Y A 2000 The modulation of host cell apoptosis by intracellular bacterial pathogens;Trends Microbiol. 8 306–313CrossRefGoogle Scholar
  20. Gil J, Alcami J and Esteban M 1999 Induction of apoptosis by double-stranded-RNA-dependent protein kinase (PKR) involves the a subunit of eukaryotic translation initiation factor 2 and NFkB;Mol. Cell. Biol. 19 4653–4663CrossRefGoogle Scholar
  21. Granville D J, Carthy C M, Yang D, Hunt D W and McManus B M 1998 Interaction of viral proteins with host cell death machinery;Cell. Death. Differ. 8 653–659CrossRefGoogle Scholar
  22. Green D R and Reed J C 1998 Mitochondria and apoptosis;Science 281 1309–1312CrossRefGoogle Scholar
  23. Gunda A, Bhuyan A K, Sahdev S, Hasnain S E, Kaufman R J and Ramaiah K V A 2002 Caspase-dependent stimulation in eIF2α phosphorylation inSpodoptera frugiperda (Sf9) cells; inTranslational control meeting (eds) Matthia Hentz, Europian Molecular Biology Lab, Germany (New York: Cold Spring Harbor Laboratory) p. 19Google Scholar
  24. Gunnery S, Green S R and Mathews M B 1992 Tat-responsive region RNA of human immunodeficiency virus type 1 stimulates protein synthesisin vivo andin vitro: Relationship between structure and function;Proc. Natl. Acad. Sci. USA 89 11557–11561CrossRefGoogle Scholar
  25. Hasnain S E, Jain A, Habib S, Ghosh S, Chatterji U, Ramachandran A, Das P, Venkaiah B, Pandey S, Liang B, Ranjan A, Natarajan K and Azim C A 1997 Involvement of host factors in transcription from baculovirus very late promoters-a review;Gene 190 113–118CrossRefGoogle Scholar
  26. Hasnain S E, Taneja T K, Sah N K, Mohan M, Pathak N, Sahdev S, Athar M and Begum R 1999In-vitro culturedSpodoptera frugiperda insect cells: Model for oxidative stress induced apoptosis;J. Biosci. 24 101–107CrossRefGoogle Scholar
  27. Hawkins C J, Uren A G, Hacker G, Medcalf R L and Vaux D L 1996 Inhibition of interleukin 1 beta-converting enzymemediated apoptosis of mammalian cells by baculovirus IAP;Proc. Natl. Acad. Sci. USA 93 13786–13790CrossRefGoogle Scholar
  28. Hengartner M O 1998 Death cycle and Swiss army knives;Nature (London) 391 441–442CrossRefGoogle Scholar
  29. Hovanessian A G and Galabru J 1987 The double-stranded RNA-dependent protein kinase is also activated by heparin;Eur. J. Biochem. 167 467–473CrossRefGoogle Scholar
  30. Ito T, Yang M and May W S 1999 Rax, a cellular activator for double-stranded RNA dependent protein kinase during stress signaling;J. Biol. Chem. 274 15427–15432CrossRefGoogle Scholar
  31. Katoch B, Sebestian S, Sahdev S, Padh H, Hasnain S E and Begum R 2002 Programmed cell death and its implications;Indian J. Exp. Biol. 40 513–524PubMedGoogle Scholar
  32. Kaufman R J 1999 Stress signaling from the lumen of the endoplasmic reticulum: coordination of gene transcriptional and translational control;Genes Dev. 13 1211–1233CrossRefGoogle Scholar
  33. Lee S B and Esteban M 1994 The interferon-induced double stranded RNA activated protein kinase induces apoptosis;Virology 199 491–496CrossRefGoogle Scholar
  34. Lee S B, Rodriguez D, Rodriguez J R and Esteban M 1997 The apoptosis pathway triggered by the interferon-induced protein kinase PKR requires the third basic domain, initiates upstream of Bcl-2 and involves ICE-like proteases;Virology 231 81–88CrossRefGoogle Scholar
  35. Li X D, Makela T P, Guo D, Soliymani R, Koistinen V, Vapalahti V, Vaheri A and Lankinen H 2002 Hanta-virus nucleocapsid protein interacts with the Fas-mediated apoptosis enhancer Daxx;J. Gen. Virol. 83 759–766CrossRefGoogle Scholar
  36. Liles W C 1997 Apoptosis: role in infection and inflammation;Curr. Opin. Infect. Dis. 10 165–170CrossRefGoogle Scholar
  37. Luder C G K, Gross U and Lopes M F 2001 Intracellular protozoan parasites and apoptosis: diverse strategies to modulate parasite-host interactions;Trends Parasitol. 17 480–486CrossRefGoogle Scholar
  38. Melville M W, Hansen W J, Freeman B C, Welch W J and Katze M G 1997 The molecular chaperone hsp40 regulates the activity of P58IPK, the cellular inhibitor of PKR;Proc. Natl. Acad. Sci. USA 94 97–102CrossRefGoogle Scholar
  39. Melville M W, Tan S L, Wambach M, Song J, Morimoto R I and Katze M G 1999 The cellular inhibitor of the PKR protein kinase, P58(IPK), is an influenza virus-activated cochaperone that modulates heat shock protein 70 activity;J. Biol. Chem. 274 3797–3803CrossRefGoogle Scholar
  40. Meurs E F, Watanabe Y, Kadereit S, Barber G N, Katze M G, Chong K, Williams B R and Hovanessian A G 1992 Constitutive expression of human double-stranded RNA-activated p68 kinase in murine cells mediates phosphorylation of eukaryotic initiation factor 2 and partial resistance to encephalomyocarditis virus growth;J. Virol. 66 5804–5814Google Scholar
  41. Miller L K 1997 Baculovirus interaction with host apoptotic pathways;J. Cell Physiol. 173 178–182CrossRefGoogle Scholar
  42. Mohan R R, Kim W J and Wilson S E 2000 Modulation of TNF-alpha-induced apoptosis in corneal fibroblasts by transcription factor NF-kappaB;Invest Ophthalmol. Vis. Sci. 41 1327–1336PubMedGoogle Scholar
  43. Mohan M, Taneja T K, Sahdev S, Mohareer K, Begum R, Athar M, Sah N K and Hasnain S E 2003 Antioxidants prevent UV-induced apoptosis by inhibiting mitochondrial cytochrome c release and caspase activation inSpodoptera frugiperda (Sf9) cells;Cell Biol. Int. (in press)Google Scholar
  44. Mulvey M, Poppers J, Ladd A and Mohr I 1999 A herpesvirus ribosome-associated, RNA-binding protein confers a growth advantage upon mutants deficient in a GADD34-related function;J. Virol. 73 3375–3385PubMedPubMedCentralGoogle Scholar
  45. Pantaleo G and Fauci A 1995 New concepts in the immunopathogenesis of HIV infection;Annu. Rev. Immunol. 13 487–512CrossRefGoogle Scholar
  46. Patel R C and Sen G C 1998 PACT, a protein activator of the interferon-induced protein kinase, PKR;EMBO J. 17 4379–4390CrossRefGoogle Scholar
  47. Ploegh H L 1998 Viral strategies of immune evasion;Science 280 248–253CrossRefGoogle Scholar
  48. Ramachandran A, Bashyam M D, Viswanathan P, Ghosh S, Kumar M S and Hasnain S E 2001 The bountiful and baffling baculovirus: The story of polyhedrin transcription;Curr. Sci. 81 998–1010Google Scholar
  49. Reichel P A, Merrick W C, Siekierka J and Mathews M B 1985 Regulation of a protein synthesis initiation factor by adenovirus virus-associated RNAI;Nature (London) 313 196–200CrossRefGoogle Scholar
  50. Rivas C, Gil J, Melkova Z, Esteban M and Diaz-Guerra M 1998 Vaccinia virus E3L protein is an inhibitor of the interferon (i.f.n.)-induced 2–5A synthetase enzyme;Virology 243 406–414CrossRefGoogle Scholar
  51. Robertson H D, Manche L and Mathews M B 1996 Paradoxical interactions between human delta hepatitis agent RNA and the cellular protein kinase PKR;J. Virol. 70 5611–5617PubMedPubMedCentralGoogle Scholar
  52. Saelens X, Kalai M and Vandenabeele P 2001 Translation inhibition in apoptosis: caspase-dependent PKR activation and eIF2-alpha phosphorylation;J. Biol. Chem. 276 41620–41628CrossRefGoogle Scholar
  53. Sah N K, Taneja T K, Pathak N, Begum R, Athar M and Hasnain S E 1999 The baculovirus antiapoptotic p35 gene also functions via an oxidant-dependent pathway;Proc. Natl. Acad. Sci. USA 96 4838–4843CrossRefGoogle Scholar
  54. Shen Y and Shenk T E 1995 Viruses and apoptosis;Curr. Opin. Genet. Dev. 5 105–111CrossRefGoogle Scholar
  55. Shi Y 2002 Mechanisms of caspase activation and inhibition during apoptosis;Mol. Cell 9 459–470CrossRefGoogle Scholar
  56. Spriggs M 1996 One step ahead of the game: viral immunomodulatory molecules;Annu. Rev. Immunol. 14 101–130CrossRefGoogle Scholar
  57. Srivastava S P, Kumar K U and Kaufman R J 1998 Phosphorylation of eukaryotic translation initiation factor 2 mediates apoptosis in response to activation of the double-stranded RNA-dependent protein kinase;J. Biol. Chem. 273 2416–2423CrossRefGoogle Scholar
  58. Sudhakar A, Krishnamoorthy T, Jain A, Chatterjee U, Hasnain S E, Kaufman R J and Ramaiah K V A 1999 Serine 48 in initiation factor 2 alpha (eIF2 alpha) is required for highaffinity interaction between eIF2 alpha(P) and eIF2B;Biochemistry 38 15398–15405CrossRefGoogle Scholar
  59. Swaminathan S, Huneycutt B S, Reiss C S and Kieff E 1992 Epstein-Barr virus-encoded small RNAs (EBERs) do not modulate interferon effects in infected lymphocytes;J. Virol. 66 5133–5136PubMedPubMedCentralGoogle Scholar
  60. Takizawa T 1996 Mechanism of the induction of apoptosis by influenza virus infection;Nippon Rinsho 54 1836–1841PubMedGoogle Scholar
  61. Thornberry N A and Lazebnik Y 1998 Caspases: enemies within;Science 281 1313–1316CrossRefGoogle Scholar
  62. Trapani J A, Davis J, Sutton V R and Smyth M J 2000 Proapoptotic functions of cytotoxic lymphocyte granule constituentsin vivo andin vitro;Curr. Opin. Immunol. 12 323–329CrossRefGoogle Scholar
  63. Vaux D L and Strasser A 1996 The molecular biology of apoptosis;Proc. Natl. Acad. Sci. USA 93 2239–2244CrossRefGoogle Scholar
  64. Williams G T 1994 Programmed cell death: a fundamental protective response to pathogens;Trends Microbiol. 2 463–464CrossRefGoogle Scholar
  65. Wong A H, Tam N W, Yang Y L, Cuddihy A R, Li S, Kirchhoff S, Hauser H, Decker T and Koromilas A E 1997 Physical association between STAT1 and the interferons inducible protein kinase PKR and implications for interferon and double stranded RNA signaling pathways;EMBO J. 16 1291–1304CrossRefGoogle Scholar
  66. Xue D and Horvitz H R 1995 Inhibition of theCaenorhabditis elegans cell-death protease CED-3 by a CED-3 cleavage site in baculovirus protein;Nature (London) 377 248–251CrossRefGoogle Scholar
  67. Yan L J, Levine R L and Sohal R S 1997 Oxidative damage during aging targets mitochondrial aconitase;Proc. Natl. Acad. Sci. USA 94 11168–11172CrossRefGoogle Scholar
  68. Yang Y C, Hsu T Y, Lin R H, Su I J, Chen J Y and Yang C S 2002 Resistance to tumour necrosis factor-alpha-induced apoptosis in human T-lymphotropic virus type I-infected T cell lines;AIDS Res. Hum. Retroviruses 18 207–212CrossRefGoogle Scholar
  69. Yeung M C, Chang D L, Camantigue R E and Lau AS 1999 Inhibitory role of the host apoptogenic gene PKR in the establishment of persistent infection by encephalomyocarditis virus in U937 cells;Proc. Natl. Acad. Sci. USA 96 11860–11865CrossRefGoogle Scholar
  70. Yuan J 1997 Tranducing signals of life and death;Curr. Opin. Cell Biol. 9 247–251CrossRefGoogle Scholar
  71. Zhou A, Paranjape J, Brown T L, Nie H, Naik S, Dong B, Chang A, Trapp B, Fairchild R, Colmenares C and Silverman R H 1997 Interferon action and apoptosis are defective in mice devoid of 2′, 5′-oligoadenylate-dependent RNase L;EMBO J. 16 6355–6363CrossRefGoogle Scholar
  72. Zhou Q, Krebs J F, Snipas S J, Price A, Alnemri E S, Tomaselli K J and Salvesen G S 1998 Interaction of the baculovirus anti-apoptotic protein p35 with caspases. Specificity, kinetics and characterization of the caspase/p35 complex;Biochemistry 37 10757–10765CrossRefGoogle Scholar

Copyright information

© Indian Academy of Sciences 2003

Authors and Affiliations

  • Seyed E. Hasnain
    • 1
    • 2
    • 3
    Email author
  • Rasheeda Begum
    • 4
  • K. V. A. Ramaiah
    • 5
  • Sudhir Sahdev
    • 1
  • E. M. Shajil
    • 4
  • Tarvinder K. Taneja
    • 2
  • Manjari Mohan
    • 2
  • M. Athar
    • 6
  • Nand K. Sah
    • 2
  • M. Krishnaveni
    • 1
  1. 1.Laboratory of Molecular and Cellular BiologyCentre for DNA Fingerprinting and DiagnosticsHyderabadIndia
  2. 2.Eukaryotic Gene Expression LabNational Institute of ImmunologyNew DelhiIndia
  3. 3.Jawaharlal Nehru Centre for Advanced Scientific ResearchBangaloreIndia
  4. 4.Department of BiochemistryM S University of BarodaVadodaraIndia
  5. 5.Department of BiochemistryUniversity of HyderabadHyderabadIndia
  6. 6.Department of Medical Elementology and ToxicologyJamia HamdardNew DelhiIndia

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