Role of Apoptosis in Microbial Infection

Faris Q. Alenzi, Ahmed Q. Alotaibi, Gdhi M. Almotiri, Anwar M. Alanazi, Faisal M. Alanazi, Mohammed S. Alenazi, Khalaf A. Alanazi, Mohammed J. Alenzi, Shamweel Y. Ahmad

Deparment of Medical Laboratory Sciences, College of Applied Medical Sciences, Salman Bin Abdulaziz University, Al-Kharj, Saudi Arabia.
Medical College, Al-Jouf University, Sakaka, Saudi Arabia.
Ministry of Health, Riyadh, Saudi Arabia.

DOI: 10.4236/ojapo.2014.32004                

Abstract

Apoptosis plays a central role in the pathogenesis of a number of human diseases. Because apoptosis represents a fundamental process in the response to such infections, it may represent a therapeutic target for their treatment. There is thus likely to be future clinical relevance in harnessing our growing knowledge both of apoptotic mechanisms, and their regulation, in the search to achieve modalities for therapeutic benefit. This brief review aims to summarize what we currently know about the role of apoptosis in response to a range of microbial infections (including bacterial and viral).

Keywords

Apoptosis, Microbial Pathogens, Infection, Therapy

Conflicts of Interest

The authors declare no conflicts of interest.

References

[1]	Torchinsky, M.B., Garaude, J. and Blander, J.M. (2010) Infection and Apoptosis as a Combined Inflammatory Trigger. Current Opinion in Immunology, 22, 55-62. http://dx.doi.org/10.1016/j.coi.2010.01.003
[2]	Ameisen, J.C., Idziorek, T., Billaut-Mulot, O., Loyens, M., Tissier, J.P., Potentier, A. and Ouaissi, A. (1995) Apoptosis in a Unicellular Eukaryote (Trypanosoma cruzi): Implications for the Evolutionary Origin and Role of Programmed Cell Death in the Control of Cell Proliferation, Differentiation and Survival. Cell Death & Differentiation, 2, 285-300.
[3]	Christensen, S.T., Wheatley, D.N., Rasmussen, M.I. and Rasmussen, L. (1995) Mechanisms Controlling Death, Survival and Proliferation in a Model Unicellular Eukaryote Tetrahymena thermophila. Cell Death & Differentiation, 2, 301-308.
[4]	Cornillon, S., Foa, C., Davoust, J., Buonavista, N., Gross, J.D. and Golstein, P. (1994) Programmed Cell Death in Dictyostelium. Journal of Cell Science, 107, 2691-2704.
[5]	Piacenza, L., Peluffo, G. and Radi, R. (2001) L-Arginine-Dependent Suppression of Apoptosis in Trypanosoma cruzi: Contribution of the Nitric Oxide and Polyamine Pathways. Proceedings of the National Academy of Sciences, 98, 7301-7306. http://dx.doi.org/10.1073/pnas.121520398
[6]	Welburn, S.C., Dale, C., Ellis, D., Beecroft, R. and Pearson, T.W. (1996) Apoptosis in Procyclic Trypanosoma brucei Rhodesiense in Vitro. Cell Death & Differentiation, 3, 229-236.
[7]	Butler, R.E., Brodin, P., Jang, J., Jang, M.S., Robertson, B.D., Gicquel, B. and Stewart, G.R. (2012) The Balance of Apoptotic and Necrotic Cell Death in Mycobacterium tuberculosis Infected Macrophages Is Not Dependent on Bacterial Virulence. PLoS one, 7, Article ID: e47573. http://dx.doi.org/10.1371/journal.pone.0047573
[8]	Lopez, M., Sly, L.M., Luu, Y., Young, D. and Cooper, H. (2003) The 19-kDa Mycobacterium tuberculosis Protein Induces Macrophage Apoptosis through Toll-Like Receptor-2. Journal of Immunology, 170, 2409-2416.
[9]	Oddo, M., Renno, T., Attinger, A., Bakker, T., MacDonald, H.R. and Meylan, P.R. (1998) Fas Ligand-Induced Apoptosis of Infected Human Macrophages Reduces the Viability of Intracellular Mycobacterium tuberculosis. Journal of Immunology, 160, 5448-5454.
[10]	Lammas, D.A., Stober, C., Harvey, C.J., Kendrick, N., Panchalingam, S. and Kumararatne, D.S. (1997) ATP-Induced Killing of Mycobacteria by Human Macrophages Is Mediated by Purinergic P2Z(P2X7) Receptors. Immunity, 7, 433- 444. http://dx.doi.org/10.1016/S1074-7613(00)80364-7
[11]	Molloy, A., Laochumroonvorapong, P. and Kaplan, G. (1994) Apoptosis, But Not Necrosis, of Infected Monocytes Is Coupled with Killing of Intracellular Bacillus Calmette-Guerin. Journal of Experimental Medicine, 180, 1499-1509. http://dx.doi.org/10.1084/jem.180.4.1499
[12]	Thoma-Uszynski, S., Stenger, S., Takeuchi, O., Ochoa, M.T., Engele, M., Sieling, P.A., Barnes, P.F., Rollinghoff, M., Bolcskei, P.L., Wagner, M., Akira, S., Norgard, M.V., Belisle, J.T., Godowski, P.J., Bloom, B.R. and Modlin, R.L. (2001) Induction of Direct Antimicrobial Activity through Mammalian Toll-Like Receptors. Science, 291, 1544-1547. http://dx.doi.org/10.1126/science.291.5508.1544
[13]	Schaible, U.E., Winau, F., Sieling, P.A., Fischer, K., Collins, H.L., Hagens, K., Modlin, R.L., Brinkmann, V. and Kaufmann, S.H. (2003) Apoptosis Facilitates Antigen Presentation to T Lymphocytes through MHC-I and CD1 in Tuberculosis. Nature Medicine, 9, 1039-1046. http://dx.doi.org/10.1038/nm906
[14]	Winau, F., Kaufmann, S.H. and Schaible, U.E. (2004) Apoptosis Paves the Detour Path for CD8 T Cell Activation against Intracellular Bacteria. Cellular Microbiology, 6, 599-607. http://dx.doi.org/10.1111/j.1462-5822.2004.00408.x
[15]	Winau, F., Weber, S., Sad, S., de Diego, J., Hoops, S.L., Breiden, B., Sandhoff, K., Brinkmann, V., Kaufmann, S.H. and Schaible, U.E. (2006) Apoptotic Vesicles Crossprime CD8 T Cells and Protect against Tuberculosis. Immunity, 24, 105-117. http://dx.doi.org/10.1016/j.immuni.2005.12.001
[16]	Golstein, P. and Kroemer, G. (2007) Cell Death by Necrosis: Towards a Molecular Definition. Trends in Biochemical Sciences, 32, 37-43. http://dx.doi.org/10.1016/j.tibs.2006.11.001
[17]	Cho, Y.S., Challa, S., Moquin, D., Genga, R., Ray, T.D., Guildford, M. and Chan, F.K. (2009) Phosphorylationdriven Assembly of the RIP1-RIP3 Complex Regulates Programmed Necrosis and Virus-Induced Inflammation. Cell, 137, 1112-1123. http://dx.doi.org/10.1016/j.cell.2009.05.037
[18]	Lee, J., Repasy, T., Papavinasasundaram, K., Sassetti, C. and Kornfeld, H. (2011) Mycobacterium tuberculosis Induces an Atypical Cell Death Mode to Escape from Infected Macrophages. PLoS ONE, 6, Article ID: e18367. http://dx.doi.org/10.1371/journal.pone.0018367
[19]	Keane, J., Remold, H.G. and Kornfeld, H. (2000) Virulent Mycobacterium Tuberculosis Strains Evade Apoptosis of Infected Alveolar Macrophages. Journal of Immunology, 164, 2016-2020.
[20]	O’Sullivan, M.P., O’Leary, S., Kelly, D.M. and Keane, J. (2007) A Caspase-Independent Pathway Mediates Macrophage Cell Death in Response to Mycobacterium Tuberculosis Infection. Infection and Immunity, 75, 1984-1993. http://dx.doi.org/10.1128/IAI.01107-06
[21]	Lee, J., Remold, H.G., Ieong, M.H. and Kornfeld, H. (2006) Macrophage Apoptosis in Response to High Intracellular Burden of Mycobacterium Tuberculosis Is Mediated by a Novel Caspase-Independent Pathway. Journal of Immunology, 176, 4267-4274.
[22]	Park, J.S., Tamayo, M.H., Gonzalez-Juarrero, M., Orme, I.M. and Ordway, D.J. (2006) Virulent Clinical Isolates of Mycobacterium tuberculosis Grow Rapidly and Induce Cellular Necrosis but Minimal Apoptosis in Murine Macrophages. Journal of Leukocyte Biology, 79, 80-86. http://dx.doi.org/10.1189/jlb.0505250
[23]	Chen, M., Gan, H. and Remold, H.G. (2006) A Mechanism of Virulence: Virulent Mycobacterium Tuberculosis Strain H37Rv, but Not Attenuated H37Ra, Causes Significant Mitochondrial Inner Membrane Disruption in Macrophages Leading to Necrosis. Journal of Immunology, 176, 3707-3716.
[24]	Zhang, J., Jiang, R., Takayama, H. and Tanaka, Y. (2005) Survival of Virulent Mycobacterium tuberculosis Involves Preventing Apoptosis Induced by Bcl-2 Upregulation and Release Resulting from Necrosis in J774 Macrophages. Microbiology and Immunology, 49, 845-852. http://dx.doi.org/10.1111/j.1348-0421.2005.tb03673.x
[25]	Sohn, H., Lee, K.S., Kim, S.Y., Shin, D.M., Shin, S.J., Jo, E.K., Park, J.K. and Kim, H.J. (2009) Induction of Cell Death in Human Macrophages by a Highly Virulent Korean Isolate of Mycobacterium tuberculosis and the Virulent Strain H37Rv. Scandinavian Journal of Immunology, 69, 43-50. http://dx.doi.org/10.1111/j.1348-0421.2005.tb03673.x
[26]	Velmurugan, K., Chen, B., Miller, J.L., Azogue, S., Gurses, S., Hsu, T., Glickman, M., Jacobs Jr., W.R., Porcelli, S.A. and Briken, V. (2007) Mycobacterium tuberculosis nuoG Is a Virulence Gene That Inhibits Apoptosis of Infected Host Cells. PLOS Pathogens, 3, Article ID: e110. http://dx.doi.org/10.1371/journal.ppat.0030110
[27]	Hinchey, J., Lee, S., Jeon, B.Y., Basaraba, R.J., Venkataswamy, M.M., Chen, B., Chan, J., Braunstein, M., Orme, I.M., Derrick, S.C., Morris, S.L., Jacobs Jr., W.R. and Porcelli, S.A. (2007) Enhanced Priming of Adaptive Immunity by a Proapoptotic Mutant of Mycobacterium tuberculosis. Journal of Clinical Investigation, 117, 2279-2288. http://dx.doi.org/10.1172/JCI31947
[28]	Ohl, M.E. and Miller, S.I. (2001) Salmonella: A Model for Bacterial Pathogenesis. Annual Review of Medicine, 52, 259-274.
[29]	Galán, J.E. (2001) Salmonella Interactions with Host Cells: Type III Secretion at Work. Annual Review of Cell and Developmental Biology, 17, 53-86. http://dx.doi.org/10.1146/annurev.cellbio.17.1.53
[30]	Weinrauch, Y. and Zychlinsky, A. (1999) The Induction of Apoptosis by Bacterial Pathogens. Annual Review of Microbiology, 53, 155-187. http://dx.doi.org/10.1146/annurev.micro.53.1.155
[31]	Majno, G. and Joris, I. (1995) Apoptosis, Oncosis, and Necrosis. An Overview of Cell Death. American Journal of Pathology, 146, 3-15.
[32]	Hernandez, L.D., Pypaert, M., Flavell, R.A. and Galan, J.E. (2003) A Salmonella Protein Causes Macrophage Cell Death by Inducing Autophagy. Journal of Cell Biology, 163, 1123-1131. http://dx.doi.org/10.1083/jcb.200309161
[33]	Guimarães, C.A. and Linden, R. (2004) Programmed Cell Deaths. Apoptosis and Alternative Deathstyles. European Journal of Biochemistry, 271, 1638-1650. http://dx.doi.org/10.1111/j.1432-1033.2004.04084.x
[34]	Zekri, A.R., Bahnassy, A.A., Hafez, M.M., Hassan, Z.K., Kamel, M., Loutfy, S.A., Sherif, G.M., El-Zayadi, A.R. and Daoud, S.S. (2011) Characterization of Chronic HCV Infection-Induced Apoptosis. Comparative Hepatology, 10, 4. http://dx.doi.org/10.1186/1476-5926-10-4
[35]	Fischer, R., Baumert, T. and Blum, H.E. (2007) Hepatitis C Virus Infection and Apoptosis. World Journal of Gastroenterology, 13, 4865-4872.
[36]	Mankouri, J., Dallas, M.L., Hughes, M.E., Griffin, S.D., Macdonald, A., Peers, C. and Harris, M. (2009) Suppression of a Pro-Apoptotic K+ Channel as a Mechanism for Hepatitis C Virus Persistence. Proceedings of the National Academy of Sciences of the United States of America, 106, 15903-15908. http://dx.doi.org/10.1073/pnas.0906798106
[37]	Shin, E.C., Shin, J.S., Park, J.H., Kim, J.J., Kim, H. and Kim, S.J. (1998) Expression of Fas-Related Genes in Human Hepatocellular Carcinomas. Cancer Letters, 134, 155-162. http://dx.doi.org/10.1016/S0304-3835(98)00251-1
[38]	Clarke, P. and Tyler, K.L. (2003) Reovirus-Induced Apoptosis: A Minireview. Apoptosis, 8, 141-150. http://dx.doi.org/10.1023/A:1022966508671
[39]	DeBiasi, R.L., Edelstein, C.L., Sherry, B. and Tyler, K.L. (2000) Calpain Inhibition Protects against Virus-Induced Apoptotic Myocardial Injury. Journal of Virology, 75, 351-361. http://dx.doi.org/10.1128/JVI.75.1.351-361.2001
[40]	Oberhaus, S.M., Smith, R.L., Clayton, G.H., Dermody, T.S. and Tyler, K.L. (1997) Reovirus Infection and Tissue Injury in the Mouse Central Nervous System Are Associated with Apoptosis. Journal of Virology, 71, 2100-2106.
[41]	Richardson-Burns, S.M., Kominsky, D.J. and Tyler, K.L. (2002) Reovirus-Induced Neuronal Apoptosis is Mediated by Caspase 3 and Is Associated with the Activation of Death Receptors. Journal of Neurovirology, 8, 365-380. http://dx.doi.org/10.1080/13550280260422677
[42]	Clem, R.J., Fechheimer, M. and Miller, L.K. (1991) Prevention of Apoptosis by a Baculovirus Gene during Infection of Insect Cells. Science, 254, 1388-1390. http://dx.doi.org/10.1126/science.1962198
[43]	Sugimoto, A., Friesen, P.D. and Rothman, J.H. (1994) Baculovirus p35 Prevents Developmentally Programmed Cell Death and Rescues a Ced-9 Mutant in the Nematode Caenorhabditis Elegans. EMBO Journal, 13, 2023-2028.
[44]	Ray, C.A., Black, R.A., Kronheim, S.R., Greenstreet, T.A., Sleath, P.R., Salvesen, G.S. and Pickup, D.J. (1992) Viral Inhibition of Inflammation: Cowpox Virus Encodes an Inhibitor of the Interleukin-1 Beta Converting Enzyme. Cell, 69, 597-604.
[45]	Gagliardini, V., Fernandez, P.A., Lee, R.K., Drexler, H.C., Rotello, R.J., Fishman, M.C. and Yuan, J. (1994) Prevention of Vertebrate Neuronal Death by the crmA Gene. Science, 263, 826-828. http://dx.doi.org/10.1126/science.8303301
[46]	Henderson, S., Rowe, M., Gregory, C., Croom-Carter, D., Wang, F., Longnecker, R., Kieff, E. and Rickinson, A. (1991) Induction of bcl-2 Expression by Epstein-Barr Virus Latent Membrane Protein 1 Protects Infected B Cells from Programmed Cell Death. Cell, 65, 1107-1115.
[47]	Gregory, C.D., Dive, C., Henderson, S., Smith, C.A., Williams, G.T., Gordon, J. and Rickinson, A.B. (1991) Activation of Epstein-Barr Virus Latent Genes Protects Human B Cells from Death by Apoptosis. Nature, 349, 612-614. http://dx.doi.org/10.1038/349612a0
[48]	Zhang, Q., Ding, Y., He, L., Wang, W., Zhang, J., Wang, H., Cai, J., Geng, J., Lu, Y. and Luo, Y. (2003) Detection of Cell Apoptosis in the Pathological Tissues of Patients with SARS and Its Significance. Di Yi Jun Yi Da Xue Xue Bao, 23, 770-773.
[49]	Sabri, F., Titanji, K., De Milito, A. and Chiodi, F. (2003) Astrocytes Activation and Apoptosis: Their Roles in the Neuropathology of HIV Infection. Brain Pathology, 13, 84-94. http://dx.doi.org/10.1111/j.1750-3639.2003.tb00009.x
[50]	Zauli, G., Gibellini, D., Caputo, A., Bassini, A., Negrini, M., Monne, M., Mazzoni, M. and Capitani, S. (1995) The Human Immunodeficiency Virus Type-1 Tat Protein Upregulates Bcl-2 Gene Expression in Jurkat T-Cell Lines and Primary Peripheral Blood Mononuclear Cells. Blood, 86, 3823-3834.
[51]	Gougeon, M.L., Olivier, R., Garcia, S., Guetard, D., Dragic, T., Dauguet, C. and Montagnier, L. (1991) Demonstration of an Engagement Process towards Cell Death by Apoptosis in Lymphocytes of HIV Infected Patients. Comptes Rendus de l Académie des Sciences—Series III, 312, 529-537. (in French)
[52]	Meyaard, L., Otto, S.A., Jonker, R.R., Mijnster, M.J., Keet, R.P. and Miedema, F. (1992) Programmed Death of T Cells in HIV-1 Infection. Science, 257, 217-219.
[53]	Meyaard, L., Otto, S.A., Schuitemaker, H. and Miedema, F. (1992) Effects of HIV-1 Tat Protein on Human T Cell Proliferation. European Journal of Immunology, 22, 2729-2732. http://dx.doi.org/10.1002/eji.1830221038
[54]	Groux, H., Torpier, G., Monte, D., Mouton, Y., Capron, A. and Ameisen, J.C. (1992) Activation-Induced Death by Apoptosis in CD4+ T Cells from Human Immunodeficiency Virus-Infected Asymptomatic Individuals. Journal of Experimental Medicine, 175, 331-340. http://dx.doi.org/10.1084/jem.175.2.331
[55]	Amendola, A., Gougeon, M.L., Poccia, F., Bondurand, A., Fesus, L. and Piacentini, M. (1996) Induction of “Tissue” Transglutaminase in HIV Pathogenesis: Evidence for High Rate of Apoptosis of CD4+ T Lymphocytes and Accessory Cells in Lymphoid Tissues. Proceedings of the National Academy of Sciences of the United States of America, 93, 11057-11062. http://dx.doi.org/10.1073/pnas.93.20.11057
[56]	van Noesel, C.J., Gruters, R.A., Terpstra, F.G., Schellekens, P.T., van Lier, R.A. and Miedema, F. (1990) Functional and Phenotypic Evidence for a Selective Loss of Memory T Cells in Asymptomatic Human Immunodeficiency Virus-Infected Men. Journal Clinical Investigation, 86, 293-299. http://dx.doi.org/10.1172/JCI114698
[57]	Meyaard, L., Otto, S.A., Keet, I.P., Roos, M.T. and Miedema, F. (1994) Programmed Death of T Cells in Human Immunodeficiency Virus Infection. No Correlation with Progression to Disease. Journal Clinical Investigation, 93, 982-988. http://dx.doi.org/10.1172/JCI117105
[58]	Gougeon, M.L., Lecoeur, H., Dulioust, A., Enouf, M.G., Crouvoiser, M., Goujard, C., Debord, T. and Montagnier, L. (1996) Programmed Cell Death in Peripheral Lymphocytes from HIV-Infected Persons: Increased Susceptibility to Apoptosis of CD4 and CD8 T Cells Correlates with Lymphocyte Activation and with Disease Progression. Journal of Immunology, 156, 3509-3520.
[59]	Finkel, T.H., Tudor-Williams, G., Banda, N.K., Cotton, M.F., Curiel, T., Monks, C., Baba, T.W., Ruprecht, R.M. and Kupfer, A. (1995) Apoptosis Occurs Predominantly in Bystander Cells and Not in Productively Infected Cells of HIV-and SIV-Infected Lymph Nodes. Nature Medicine, 1, 129-134. http://dx.doi.org/10.1038/nm0295-129
[60]	Oyaizu, N., McCloskey, T.W., Coronesi, M., Chirmule, N., Kalyanaraman, V.S. and Pahwa, S. (1993) Accelerated Apoptosis in Peripheral Blood Mononuclear Cells (PBMCs) from Human Immunodeficiency Virus Type-1 Infected Patients and in CD4 Cross-Linked PBMCs from Normal Individuals. Blood, 82, 3392-400.