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Along a TNF-paved road from dead parasites in red cells to cerebral malaria, and beyond

Published online by Cambridge University Press:  19 May 2009

I. A. CLARK
I. A. CLARK*
Affiliation:
School of Biochemistry and Molecular Biology, Australian National University, Canberra, ACT 0200, Australia
*
*Fax: +61 2 6125 0313. E-mail: [email protected]
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Summary

This is a personal account of how tumour necrosis factor (TNF) the prototype of a group of host-origin mediators, often known as pro-inflammatory cytokines, came into parasitology, and was subsequently realised to be central to the pathogenesis of most disease pathology. This contribution summarizes an example of how a curiosity-driven outsider, with initially no intention of heading this way, and no relevant experience, and with no more than the simplest of plans but an ambition to read as widely as it takes, and (most importantly) allowed to follow his head, can be what is required to give fresh insight into understanding a disease. It also gives the author's views on aspects of how the field of malaria disease pathogenesis seems to be developing. The hope is to inspire another generation to follow a similarly original course.

Keywords

TNFmalariavaccinediseasebabesiamitochondria
Type
Research Article
Information
Parasitology , Volume 136 , Special Issue 12: Special Centenary Issue – Parasitology 1908–2008 , October 2009 , pp. 1457 - 1468
Copyright
Copyright © Cambridge University Press 2009

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References

REFERENCES

Abernathy, R. S., Bradley, G. M. and Spink, W. W. (1958). Increased susceptibility of mice with brucellosis to bacterial endotoxins. Journal of Immunology 81, 271–275.CrossRefGoogle ScholarPubMed
Aggarwal, B. B., Kohr, W. J., Hass, P. E., Moffat, B., Spencer, S. A., Henzel, W. J., Bringman, T. S., Nedwin, G. E., Goeddel, D. V. and Harkins, R. N. (1985). Human tumor necrosis factor: production, purification, and characterization. Journal of Biological Chemistry 260, 2345–2354.CrossRefGoogle ScholarPubMed
Ahmed, K., Al Matrouk, K. A., Martinez, G., Oishi, K., Rotimi, V. O. and Nagatake, T. (1999). Increased serum levels of interferon-gamma and interleukin-12 during human brucellosis. American Journal of Tropical Medicine and Hygiene 61, 425–427.CrossRefGoogle ScholarPubMed
Anstey, N. M., Jacups, S. P., Cain, T., Pearson, T., Ziesing, P. J., Fisher, D. A., Currie, B. J., Marks, P. J. and Maguire, G. P. (2002). Pulmonary manifestations of uncomplicated falciparum and vivax malaria: Cough, small airways obstruction, impaired gas transfer, and increased pulmonary phagocytic activity. Journal of Infectious Diseases 185, 1326–1334.CrossRefGoogle ScholarPubMed
Arsenijevic, D., Girardier, L., Seydoux, J., Chang, H. R. and Dulloo, A. G. (1997). Altered energy balance and cytokine gene expression in a murine model of chronic infection with Toxoplasma gondii. American Journal of Physiology 272, E908–E917.Google Scholar
Bajaj, M. S., Kuppuswamy, M. N., Manepalli, A. N. and Bajaj, S. P. (1999). Transcriptional expression of tissue factor pathway inhibitor, thrombomodulin and von Willebrand factor in normal human tissues. Thrombosis and Haemostasis 82, 1047–1052.Google ScholarPubMed
Bate, C. A., Taverne, J., Bootsma, H. J., Mason, R. C., Skalko, N., Gregoriadis, G. and Playfair, J. H. (1992). Antibodies against phosphatidylinositol and inositol monophosphate specifically inhibit tumour necrosis factor induction by malaria exoantigens. Immunology 76, 35–41.Google ScholarPubMed
Bauer, K. A., Cate, H. T., Barzeger, S., Spriggs, D. R., Sherman, M. L. and Rosenberg, R. D. (1989). Tumor necrosis factor infusions have a procoagulant effect on the hemostatic mechanism of humans. Blood 74, 165–172.CrossRefGoogle ScholarPubMed
Beattie, E. C., Stellwagen, D., Morishita, W., Bresnahan, J. C., Ha, B. K., Von Zastrow, M., Beattie, M. S. and Malenka, R. C. (2002). Control of synaptic strength by glial TNFalpha. Science 295, 2282–2285.CrossRefGoogle ScholarPubMed
Bernardino, L., Agasse, F., Silva, B., Ferreira, R., Grade, S. and Malva, J. O. (2008). Tumor necrosis factor-alpha modulates survival, proliferation, and neuronal differentiation in neonatal subventricular zone cell cultures. Stem Cells 26, 2361–2371.CrossRefGoogle ScholarPubMed
Berry, L. J., Moore, R. N., Goodrum, K. J. and Couch, R. E. (1977). Cellular requirements for enzyme inhibition by endotoxin in mice. Microbiology 1977 (ed. Schlessinger, D.), pp. 321–325. American Society of Microbiology, Washington D.C., USA.Google Scholar
Beutler, B. and Cerami, A. (1987). Cachectin-tumour necrosis factor: a cytokine that mediates injury initiated by invasive parasites. Parasitology Today 3, 345–346.CrossRefGoogle ScholarPubMed
Beutler, B., Greenwald, D., Hulmes, J. D., Chang, M., Pan, Y.-C., Mathison, J., Ulevitch, R. and Cerami, A. (1985 a). Identity of tumour necrosis factor and the macrophage-secreted factor cachectin. Nature 316, 552–554.CrossRefGoogle ScholarPubMed
Beutler, B., Mahoney, J., Le, T. N., Pekala, P. and Cerami, A. (1985 b). Purification of cachectin, a lipoprotein lipase-suppressing hormone secreted by endotoxin-induced RAW 264.7 cells. Journal of Experimental Medicine 161, 984–995.CrossRefGoogle ScholarPubMed
Bhutta, Z. A., Mansoorali, N. and Hussain, R. (1997). Plasma cytokines in paediatric typhoidal salmonellosis: correlation with clinical course and outcome. Journal of Infection 35, 253–256.CrossRefGoogle ScholarPubMed
Bour, E. S., Ward, L. K., Cornman, G. A. and Isom, H. C. (1996). Tumor necrosis factor-alpha-induced apoptosis in hepatocytes in long-term culture. American Journal of Pathology 148, 485–495.Google ScholarPubMed
Brealey, D., Karyampudi, S., Jacques, T. S., Novelli, M., Stidwill, R., Taylor, V., Smolenski, R. T. and Singer, M. (2004). Mitochondrial dysfunction in a long-term rodent model of sepsis and organ failure. American Journal of Physiology 286, R491–R497.Google Scholar
Budd, A., Alleva, L., Alsharifi, M., Koskinen, A., Smythe, V., Mullbacher, A., Wood, J. and Clark, I. (2007). Increased survival after gemfibrozil treatment of severe mouse influenza. Antimicrobial Agents and Chemotherapy 51, 2965–2968.CrossRefGoogle ScholarPubMed
Butcher, G. A., Bannister, L. H. and Mitchell, G. H. (1976). Immune damage to intracellular malaria parasites. Transactions of the Royal Society of Tropical Medicine and Hygiene 70, 11.Google Scholar
Butcher, G. A., Garland, T., Adjukiewicz, A. B. and Clark, I. A. (1990). Serum TNF associated with malaria in patients in the Solomon Islands. Transactions of the Royal Society of Tropical Medicine and Hygiene 84, 658–661.CrossRefGoogle ScholarPubMed
Butcher, G. A., Mitchell, G. H. and Cohen, S. (1978). Antibody mediated mechanisms of immunity to malaria induced by vaccination with Plasmodium knowlesi merozoites. Immunology 34, 77–86.Google ScholarPubMed
Carswell, E. A., Old, L. J., Kassel, R. L., Green, S., Fiore, N. and Williamson, B. (1975). An endotoxin-induced serum factor that causes necrosis of tumors. Proceedings of the National Academy of Sciences, USA 72, 3666–3670.CrossRefGoogle ScholarPubMed
Charles, P., Elliott, M. J., Davis, D., Potter, A., Kalden, J. R., Antoni, C., Breedveld, F. C., Smolen, J. S., Eberl, G., deWoody, K., Feldmann, M. and Maini, R. N. (1999). Regulation of cytokines, cytokine inhibitors, and acute-phase proteins following anti-TNF-alpha therapy in rheumatoid arthritis. Journal of Immunology 163, 1521–1528.CrossRefGoogle ScholarPubMed
Clark, I. A. (1973). The pathogenesis of St George disease of cattle. Research in Veterinary Science 14, 341–349.CrossRefGoogle Scholar
Clark, I. A. (1978). Does endotoxin cause both the disease and parasite death in acute malaria and babesiosis? Lancet ii, 75–77.CrossRefGoogle Scholar
Clark, I. A. (1979). Protection of mice against Babesia microti with cord factor, COAM, zymosan, glucan, Salmonella and Listeria. Parasite Immunology 1, 179–196.CrossRefGoogle ScholarPubMed
Clark, I. A. (1982 a). Correlation between susceptibility to malaria and babesia parasites and to endotoxin. Transactions of the Royal Society of Tropical Medicine and Hygiene 76, 4–7.CrossRefGoogle Scholar
Clark, I. A. (1982 b). Suggested importance of monokines in pathophysiology of endotoxin shock and malaria. Klinische Wochenschrift 60, 756–758.CrossRefGoogle ScholarPubMed
Clark, I. A. (1987 a). Cell-mediated immunity in protection and pathology of malaria. Parasitology Today 3, 300–305.CrossRefGoogle ScholarPubMed
Clark, I. A. (1987 b). Monokines and lymphokines in malarial pathology. Annals of Tropical Medicine and Parasitology 81, 577–585.CrossRefGoogle ScholarPubMed
Clark, I. A. (2007). How TNF was recognized to be a key mechanism of disease. Cytokine and Growth Factor Reviews 18, 335–343.CrossRefGoogle ScholarPubMed
Clark, I. A., Alleva, L. E., Mills, A. C. and Cowden, W. B. (2004). Pathogenesis in malaria and clinically similar conditions. Clinical Microbiology Reviews 17, 509–539.CrossRefGoogle ScholarPubMed
Clark, I. A., Alleva, L. M., Budd, A. C. and Cowden, W. B. (2008 a). Understanding the role of inflammatory cytokines in malaria and related diseases. Travel Medicine and Infectious Disease 6, 67–81.CrossRefGoogle ScholarPubMed
Clark, I. A., Allison, A. C. and Cox, F. E. (1976). Protection of mice against Babesia and Plasmodium with BCG. Nature, London 259, 309–311.CrossRefGoogle ScholarPubMed
Clark, I. A., Budd, A. C. and Alleva, L. M. (2008 b). Sickness behaviour pushed too far – the basis of the syndrome seen in severe protozoal, bacterial and viral diseases and post-trauma. Malaria Journal 7, 208.CrossRefGoogle ScholarPubMed
Clark, I. A., Budd, A. C., Alleva, L. M. and Cowden, W. B. (2006). Human malarial disease: a consequence of inflammatory cytokine release. Malaria Journal 5, 85.CrossRefGoogle ScholarPubMed
Clark, I. A. and Chaudhri, G. (1988 a). Tumor necrosis factor in malaria-induced abortion. American Journal of Tropical Medicine and Hygiene 39, 246–249.CrossRefGoogle ScholarPubMed
Clark, I. A. and Chaudhri, G. (1988 b). Tumour necrosis factor may contribute to the anaemia of malaria by causing dyserythropoiesis and erythrophagocytosis. British Journal of Haematology 70, 99–103.CrossRefGoogle Scholar
Clark, I. A. and Cowden, W. B. (1989). Is TNF a key to acute infectious illness? Today's Life Science 1, 26–29.Google Scholar
Clark, I. A. and Cowden, W. B. (2003). The pathophysiology of falciparum malaria. Pharmacology and Therapeutics 99, 221–260.CrossRefGoogle ScholarPubMed
Clark, I. A., Cowden, W. B., Butcher, G. A. and Hunt, N. H. (1987 a). Possible roles of tumor necrosis factor in the pathology of malaria. American Journal of Pathology 129, 192–199.Google ScholarPubMed
Clark, I. A., Cox, F. E. and Allison, A. C. (1977 a). Protection of mice against Babesia spp. and Plasmodium spp. with killed Corynebacterium parvum. Parasitology 74, 9–18.CrossRefGoogle ScholarPubMed
Clark, I. A. and Griffiths, M. J. (2007). The molecular basis of paediatric malarial disease. In Pediatric Infectious Diseases Revisited (ed. Schroten, H. and Wirth, S.), pp. 239–272. Birkhauser, Basel, Switzerland.CrossRefGoogle Scholar
Clark, I. A., Hunt, N. H., Butcher, G. A. and Cowden, W. B. (1987 b). Inhibition of murine malaria (Plasmodium chabaudi) in vivo by recombinant interferon-gamma or tumor necrosis factor, and its enhancement by butylated hydroxyanisole. Journal of Immunology 139, 3493–3496.CrossRefGoogle ScholarPubMed
Clark, I. A., Richmond, J. E., Wills, E. J. and Allison, A. C. (1975). Immunity to intra-erythrocytic protozoa. Lancet ii, 1128–1129.CrossRefGoogle Scholar
Clark, I. A., Richmond, J. E., Wills, E. J. and Allison, A. C. (1977 b). Intra-erythrocytic death of the parasite in mice recovering from infection with Babesia microti. Parasitology 75, 189–196.CrossRefGoogle ScholarPubMed
Clark, I. A. and Rockett, K. A. (1994). The cytokine theory of human cerebral malaria. Parasitology Today 10, 410–412.CrossRefGoogle ScholarPubMed
Clark, I. A., Rockett, K. A. and Cowden, W. B. (1992). Possible central role of nitric oxide in conditions clinically similar to cerebral malaria. Lancet 340, 894–896.CrossRefGoogle ScholarPubMed
Clark, I. A., Virelizier, J.-L., Carswell, E. A. and Wood, P. R. (1981). Possible importance of macrophage-derived mediators in acute malaria. Infection and Immunity 32, 1058–1066.CrossRefGoogle ScholarPubMed
Collins, F. M. and Scott, M. T. (1974). Effect of Corynebacterium parvum on the growth of Salmonella enteritidis in mice. Infection and Immunity 9, 863–869.CrossRefGoogle ScholarPubMed
Cox, F. E. G. (1970). Protective immunity between malaria parasites and piroplasms in mice. Bulletin of the World Health Organization 43, 325–336.Google ScholarPubMed
Crouser, E. D. (2004). Mitochondrial dysfunction in septic shock and multiple organ dysfunction syndrome. Mitochondrion 4, 729–741.CrossRefGoogle ScholarPubMed
Cumiskey, D., Butler, M. P., Moynagh, P. N. and O'Connor, J. J. (2007). Evidence for a role for the group I metabotropic glutamate receptor in the inhibitory effect of tumor necrosis factor-alpha on long-term potentiation. Brain Research 1136, 13–19.CrossRefGoogle Scholar
d'Avila, J. C., Santiago, A. P., Amancio, R. T., Galina, A., Oliveira, M. F. and Bozza, F. A. (2008). Sepsis induces brain mitochondrial dysfunction. Critical Care Medicine 36, 1925–1932.CrossRefGoogle ScholarPubMed
Diehl, A. M. and Rai, R. (1996). Review – regulation of liver regeneration by pro-inflammatory cytokines. Journal of Gastroenterology and Hepatology 11, 466–470.CrossRefGoogle ScholarPubMed
Dubos, R. J. and Schaedler, R. W. (1957). Effect of cellular constituents of Mycobacteria on the resistance of mice to heterologous infection. Journal of Experimental Medicine 106, 703–709.CrossRefGoogle Scholar
Emelyanov, V. V. (2001). Evolutionary relationship of Rickettsiae and mitochondria. FEBS Letters 501, 11–18.CrossRefGoogle ScholarPubMed
Fairhurst, R. M. and Wellems, T. E. (2006). Modulation of malaria virulence by determinants of Plasmodium falciparum erythrocyte membrane protein-1 display. Current Opinion in Hematology 13, 124–130.CrossRefGoogle ScholarPubMed
Ferguson, A. R., Christensen, R. N., Gensel, J. C., Miller, B. A., Sun, F., Beattie, E. C., Bresnahan, J. C. and Beattie, M. S. (2008). Cell death after spinal cord injury is exacerbated by rapid TNFalpha-induced trafficking of GluR2-lacking AMPARs to the plasma membrane. Journal of Neuroscience 28, 11391–11400.CrossRefGoogle ScholarPubMed
Fink, M. P. (2001). Cytopathic hypoxia. Mitochondrial dysfunction as mechanism contributing to organ dysfunction in sepsis. Critical Care Clinics 17, 219–237.CrossRefGoogle ScholarPubMed
Genton, B., D'Acremont, V., Rare, L., Baea, K., Reeder, J. C., Alpers, M. P. and Muller, I. (2008). Plasmodium vivax and mixed infections are associated with severe malaria in children: a prospective cohort study from Papua New Guinea. PLoS Medicine 5, e127.CrossRefGoogle ScholarPubMed
Giamarellos-Bourboulis, E. J., Kanellakopoulou, K., Pelekanou, A., Tsaganos, T. and Kotzampassi, K. (2008). Kinetics of angiopoietin-2 in serum of multi-trauma patients: correlation with patient severity. Cytokine 44, 310–313.CrossRefGoogle ScholarPubMed
Giuliano, J. S., Lahni, P. M., Harmon, K., Wong, H. R., Doughty, L. A., Carcillo, J. A., Zingarelli, B., Sukhatme, V. P., Parikh, S. M. and Wheeler, D. S. (2007). Admission angiopoietin levels in children with septic shock. Shock 28, 650–654.CrossRefGoogle ScholarPubMed
Good, M. F., Xu, H. J., Wykes, M. and Engwerda, C. R. (2005). Development and regulation of cell-mediated immune responses to the blood stages of malaria: Implications for vaccine research. Annual Review of Immunology 23, 69–99.CrossRefGoogle Scholar
Haden, D. W., Suliman, H. B., Carraway, M. S., Welty Wolf, K. E., Ali, A. S., Shitara, H., Yonekawa, H. and Piantadosi, C. A. (2007). Mitochondrial biogenesis restores oxidative metabolism during Staphylococcus aureus sepsis. American Journal of Respiratory and Critical Care Medicine 176, 768–777.CrossRefGoogle ScholarPubMed
Halpern, B. N., Biozzi, G., Stiffel, C. and Mouton, D. (1966). Inhibition of tumour growth by abministration of killed Corynebacterium parvum. Nature, London 212, 853–854.CrossRefGoogle Scholar
Hernandez Caselles, T. and Stutman, O. (1993). Immune functions of tumor necrosis factor. I. Tumor necrosis factor induces apoptosis of mouse thymocytes and can also stimulate or inhibit IL-6-induced proliferation depending on the concentration of mitogenic costimulation. Journal of Immunology 151, 3999–4012.CrossRefGoogle ScholarPubMed
Hopkins, S. J. (2007). Central nervous system recognition of peripheral inflammation: A neural, hormonal collaboration. Acta Biomedica 78 (Suppl. 1), 231–247.Google ScholarPubMed
Howard, J. G., Biozzi, G., Halpern, B. N., Stiffel, C. and Mouton, D. (1959). The effect of Mycobacterium tuberculosis (BCG) infection on the resistance of mice to bacterial endotoxin and Salmonella enteritidis infection. British Journal of Experimental Pathology 40, 281–290.Google ScholarPubMed
John, C. C., Panoskaltsis Mortari, A., Opoka, R. O., Park, G. S., Orchard, P. J., Jurek, A. M., Idro, R., Byarugaba, J. and Boivin, M. J. (2008). Cerebrospinal fluid cytokine levels and cognitive impairment in cerebral malaria. American Journal of Tropical Medicine and Hygiene 78, 198–205.CrossRefGoogle ScholarPubMed
Kawakami, M., Pekala, P. H., Lane, M. D. and Cerami, A. (1982). Lipoprotein lipase suppression in 3T3-L1 cells by an endotoxin-induced mediator from exudate cells. Proceedings of the National Academy of Sciences, USA 79, 912–916.CrossRefGoogle ScholarPubMed
Kern, P., Hemmer, C. J., Van Damme, J., Gruss, H.-J. and Dietrich, M. (1989). Elevated tumour necrosis factor alpha and interleukin-6 serum levels as markers for complicated Plasmodium falciparum malaria. American Journal of Medicine 87, 139–143.CrossRefGoogle ScholarPubMed
Kwiatkowski, D., Hill, A. V. S., Sambou, I., Twumasi, P., Castracane, J., Manogue, K. R., Cerami, A., Brewster, D. R. and Greenwood, B. M. (1990). TNF concentration in fatal cerebral, non-fatal cerebral, and uncomplicated Plasmodium falciparum malaria. Lancet 336, 1201–1204.CrossRefGoogle ScholarPubMed
Langhorne, J., Butcher, G. A., Mitchell, G. H. and Cohen, S. (1979). Preliminary investigations on the role of the spleen in immunity to Plasmodium knowlesi malaria. In Role of the Spleen in the Immunology of Parasitic Diseases. Schwabe, Basel, Switzerland. UNDP/World Bank/WHO.Google Scholar
MacPherson, G. G., Warrell, M. J., White, N. J., Looareesuwan, S. and Warrell, D. A. (1985). Human cerebral malaria. A quantitative ultrastructural analysis of parasitised erythrocyte sequestration. American Journal of Pathology 119, 385–401.Google Scholar
Maegraith, B. G. (1938). Meningococcal broth culture filtrates: failure of protection experiments. British Journal of Experimental Pathology 19, 95–99.Google Scholar
Maegraith, B. G. (1954). Physiological aspects of protozoan infection. Annual Review of Microbiology 8, 273–288.CrossRefGoogle ScholarPubMed
Maegraith, B. G. and Findlay, G. M. (1944). Oliguria in blackwater fever. Lancet ii, 403–404.CrossRefGoogle Scholar
Maier, A. G., Rug, M., O'Neill, M. T., Brown, M., Chakravorty, S., Szestak, T., Chesson, J., Wu, Y., Hughes, K., Coppel, R. L., Newbold, C., Beeson, J. G., Craig, A., Crabb, B. S. and Cowman, A. F. (2008). Exported proteins required for virulence and rigidity of Plasmodium falciparum-infected human erythrocytes. Cell 134, 48–61.CrossRefGoogle ScholarPubMed
Margulis, L. and Chapman, M. J. (1998). Endosymbioses: cyclical and permanent in evolution. Trends in Microbiology 6, 342–345; discussion 345–346.CrossRefGoogle ScholarPubMed
Murphy, S. C. and Breman, J. G. (2001). Gaps in the childhood malaria burden in Africa: Cerebral malaria, neurological sequelae, anemia, respiratory distress, hypoglycemia, and complications of pregnancy. American Journal of Tropical Medicine and Hygiene 64, 57–67.CrossRefGoogle ScholarPubMed
Nakane, A., Yamada, K., Hasegawa, S., Mizuki, D., Mizuki, M., Sasaki, S. and Miura, T. (1999). Endogenous cytokines during a lethal infection with Listeria monocytogenes in mice. FEMS Microbiology Letters 175, 133–142.CrossRefGoogle ScholarPubMed
Nisoli, E. and Carruba, M. O. (2006). Nitric oxide and mitochondrial biogenesis. Journal of Cell Science 119, 2855–2862.CrossRefGoogle ScholarPubMed
Old, L. J., Clarke, D. A. and Benacerraf, B. (1959). Effect of Bacillus Calmette Guérin infection on transplanted tumours in the mouse. Nature, London 184, 291–292.CrossRefGoogle Scholar
Park, K. M., Yule, D. I. and Bowers, W. J. (2008). Tumor necrosis factor-alpha potentiates intraneuronal Ca2+ signaling via regulation of the inositol 1,4,5-trisphosphate receptor. Journal of Biological Chemistry 6, 33069–33079.CrossRefGoogle Scholar
Pickering, M., Cumiskey, D. and O'Connor, J. J. (2005). Actions of TNF-alpha on glutamatergic synaptic transmission in the central nervous system. Experimental Physiology 90, 663–670.CrossRefGoogle ScholarPubMed
Pirsch, J. B., Mika, L. A. and van der Maaten, M. J. (1957). Hyperreactivity of Coxiella burnetii infected guines pigs to subsequent injections of bacterial endotoxins. Proceedings of the Society for Experimental Biology 96, 376–380.CrossRefGoogle Scholar
Ranges, G. E., Zlotnik, A., Espevik, T., Dinarello, C. A., Cerami, A. and Palladino, M. A. (1988). Tumor necrosis factor alpha/cachectin is a growth factor for thymocytes. Synergistic interactions with other cytokines. Journal of Experimental Medicine 167, 1472–1478.CrossRefGoogle ScholarPubMed
Raziuddin, S., Abdalla, R. E., el Awad, E. H. and al Janadi, M. (1994). Immunoregulatory and proinflammatory cytokine production in visceral and cutaneous leishmaniasis. Journal of Infectious Diseases 170, 1037–1040.CrossRefGoogle ScholarPubMed
Rebel, V. I., Hartnett, S., Hill, G. R., Lazo Kallanian, S. B., Ferrara, J. L. and Sieff, C. A. (1999). Essential role for the p55 tumor necrosis factor receptor in regulating hematopoiesis at a stem cell level. Journal of Experimental Medicine 190, 1493–1504.CrossRefGoogle Scholar
Riazi, K., Galic, M. A., Kuzmiski, J. B., Ho, W., Sharkey, K. A. and Pittman, Q. J. (2008). Microglial activation and TNF{alpha} production mediate altered CNS excitability following peripheral inflammation. Proceedings of the National Academy of Sciences, USA 105, 17151–17156.CrossRefGoogle ScholarPubMed
Riley, M. V. and Maegraith, B. G. (1962). A factor in the serum of malaria-infected animals capable of inhibiting the in vitro oxidative metabolism of normal liver mitochondria. Annals of Tropical Medicine and Parasitology 55, 489–497.CrossRefGoogle Scholar
Rook, G. A. W., Taverne, J., Leveton, C. and Steele, J. (1987). The role of gamma-interferon, vitamin D3 metabolites and tumour necrosis factor in the pathogenesis of tuberculosis. Immunology 62, 229–234.Google ScholarPubMed
Ross, R. (1911). The Prevention of Malaria. John Murray, London, UK.Google ScholarPubMed
Rubenstein, M., Mulholland, J. H., Jeffery, G. M. and Wolff, S. M. (1965). Malaria-induced endotoxin tolerance. Proceedings of the Society for Experimental Biology and Medicine 118, 283–287.CrossRefGoogle ScholarPubMed
Salvin, S. B., Ribi, E., Granger, D. L. and Youngner, J. S. (1975). Migration inhibitory factor and type II interferon in the circulation of mice sensitized with mycobacterial components. Journal of Immunology 114, 354–359.CrossRefGoogle ScholarPubMed
Sanderson, C. J., Clark, I. A. and Taylor, G. A. (1975). Different effector cell types in antibody-dependent cell-mediated cytotoxicity. Nature, London 253, 376–377.CrossRefGoogle ScholarPubMed
Schofield, L. and Hackett, F. (1993). Signal transduction in host cells by a glycosylphosphatidylinositol toxin of malaria parasites. Journal of Experimental Medicine 177, 145–153.CrossRefGoogle ScholarPubMed
Smrkovski, L. L. and Larson, C. L. (1977). Effect of treatment with BCG on the course of visceral leishmaniasis in BALB/c mice. Infection and Immunity 16, 249–257.CrossRefGoogle ScholarPubMed
Spriggs, D. R., Sherman, M. L., Michie, H., Arthur, K. A., Imamura, K., Wilmore, D., Frei, E. and Kufe, D. W. (1988). Recombinant human tumor necrosis factor administered as a 24-hour intravenous infusion. A phase 1 and pharmacologic study. Journal of the National Cancer Institute 80, 1039–1044.CrossRefGoogle Scholar
Steinert, J. R., Kopp Scheinpflug, C., Baker, C., Challiss, R. A., Mistry, R., Haustein, M. D., Griffin, S. J., Tong, H., Graham, B. P. and Forsythe, I. D. (2008). Nitric oxide is a volume transmitter regulating postsynaptic excitability at a glutamatergic synapse. Neuron 60, 642–656.CrossRefGoogle Scholar
Stellwagen, D. and Malenka, R. C. (2006). Synaptic scaling mediated by glial TNF-alpha. Nature, London 440, 1054–1059.CrossRefGoogle ScholarPubMed
Suliman, H. B., Welty Wolf, K. E., Carraway, M., Tatro, L. and Piantadosi, C. A. (2004). Lipopolysaccharide induces oxidative cardiac mitochondrial damage and biogenesis. Cardiovascular Research 64, 279–288.CrossRefGoogle ScholarPubMed
Suliman, H. B., Welty Wolf, K. E., Carraway, M. S., Schwartz, D. A., Hollingsworth, J. W. and Piantadosi, C. A. (2005). Toll-like receptor 4 mediates mitochondrial DNA damage and biogenic responses after heat-inactivated E. coli. FASEB Journal 19, 1531–1533.CrossRefGoogle ScholarPubMed
Suter, E., Ullman, G. E. and Hoffman, R. G. (1958). Sensitivity of mice to endotoxin after vaccination with BCG (Bacillus Calmette-Guérin). Proceedings of the Society for Experimental Biology 99, 167–169.CrossRefGoogle ScholarPubMed
Swartzberg, J. E., Krahenbuhl, J. L. and Remington, J. S. (1975). Dichotomy between macrophage activation and degree of protection against Listeria monocytogenes and Toxoplasma gondii in mice stimulated with Corynebacterium parvum. Infection and Immunity 12, 1037–1043.CrossRefGoogle ScholarPubMed
Takeda, K., Iwamoto, S., Sugimoto, H., Takuma, T., Kawatani, N., Noda, M., Masaki, A., Morise, H., Arimura, H. and Konno, K. (1986). Identity of differentiation inducing factor and tumour necrosis factor. Nature, London 323, 338–340.CrossRefGoogle ScholarPubMed
Taverne, J., Bate, C. A. W. and Playfair, J. H. L. (1989). Induction of TNF in vitro as a model for the identification of toxic malaria antigens. Lymphokine Research 8, 317–322.Google Scholar
Taylor, T. E., Fu, W. J. J., Carr, R. A., Whitten, R. O., Mueller, J. G., Fosiko, N. G., Lewallen, S., Liomba, N. G. and Molyneux, M. E. (2004). Differentiating the pathologies of cerebral malaria by postmortem parasite counts. Nature Medicine 10, 143–145.CrossRefGoogle ScholarPubMed
Tjitra, E., Anstey, N. M., Sugiarto, P., Warikar, N., Kenangalem, E., Karyana, M., Lampah, D. A. and Price, R. N. (2008). Multidrug-resistant Plasmodium vivax associated with severe and fatal malaria: a prospective study in Papua, Indonesia. PLoS Medicine 5, e128.CrossRefGoogle ScholarPubMed
Tobinick, E. L., Gross, H., Weinberger, A. and Cohen, H. (2006). TNF-alpha modulation for treatment of Alzheimer's disease: A 6-month pilot study. MedGenMed Neurology and Neurosurgery 8, 25.Google ScholarPubMed
Turco, J. and Winkler, H. H. (1993). Role of the nitric oxide synthase pathway in inhibition of growth of interferon-sensitive and interferon-resistant Rickettsia prowazekii strains in L929 cells treated with tumor necrosis factor alpha and gamma interferon. Infection and Immunity 61, 4317–4325.CrossRefGoogle ScholarPubMed
Witzenbichler, B., Westermann, D., Knueppel, S., Schultheiss, H. P. and Tschope, C. (2005). Protective role of angiopoietin-1 in endotoxic shock. Circulation 111, 97–105.CrossRefGoogle ScholarPubMed
Xu, J., Qu, J., Cao, L., Sai, Y., Chen, C., He, L. and Yu, L. (2008). Mesenchymal stem cell-based angiopoietin-1 gene therapy for acute lung injury induced by lipopolysaccharide in mice. Journal of Pathology 214, 472–481.CrossRefGoogle ScholarPubMed
Yeo, T. W., Lampah, D. A., Gitawati, R., Tjitra, E., Kenangalem, E., Piera, K., Price, R. N., Duffull, S. B., Celermajer, D. S. and Anstey, N. M. (2008). Angiopoietin-2 is associated with decreased endothelial nitric oxide and poor clinical outcome in severe falciparum malaria. Proceedings of the National Academy of Sciences, USA 105, 17097–17102.CrossRefGoogle ScholarPubMed