Integrated cytokine and metabolic analysis of pathological responses to parasite exposure in rodents

Journal of Proteome Research

Volumn 9, Issue 5, 2010, Pages 2255-2264

  Saric, Jasmina ^a   Li, Jia V ^a   Swann, Jonathan R ^a   Utzinger, Jürg ^b   Calvert, Gail ^c   Nicholson, Jeremy K ^a   Dirnhofer, Stephan ^d   Dallman, Maggie J ^a   Bictash, Magda ^a   Holmes, Elaine ^a  

^a IMPERIAL COLLEGE LONDON   (United Kingdom)

^b SWISS TROPICAL AND PUBLIC HEALTH INSTITUTE   (Switzerland)

^c Meso Scale Discovery   (United States)

^d UNIVERSITY HOSPITAL BASEL   (Switzerland)

Author keywords

1H NMR Spectroscopy; Cytokine Patterns; Fasciola hepatica; Metabolic Profiling; Multivariate Data Analysis; Plasmodium berghei; Schistosoma mansoni; Systems Integration; Trypanosoma brucei brucei

Indexed keywords

3 HYDROXYBUTYRIC ACID; CHOLINE; CYTOKINE; GAMMA INTERFERON; INTERLEUKIN 4; INTERLEUKIN 5; LACTIC ACID;

ARTICLE; FASCIOLA HEPATICA; NONHUMAN; PARASITE; PARASITOSIS; PLASMODIUM BERGHEI; PRIORITY JOURNAL; PROTON NUCLEAR MAGNETIC RESONANCE; RAT; SCHISTOSOMA MANSONI; TRYPANOSOMA BRUCEI;

ANIMALS; CYTOKINES; DISCRIMINANT ANALYSIS; DISEASE MODELS, ANIMAL; FASCIOLA HEPATICA; FEMALE; HISTOCYTOCHEMISTRY; HOST-PARASITE INTERACTIONS; METABOLOME; MICE; MULTIVARIATE ANALYSIS; NUCLEAR MAGNETIC RESONANCE, BIOMOLECULAR; PARASITIC DISEASES; PHENOTYPE; PLASMODIUM BERGHEI; PRINCIPAL COMPONENT ANALYSIS; RATS; SCHISTOSOMA MANSONI; TRYPANOSOMA BRUCEI BRUCEI;

ANIMALIA; FASCIOLA HEPATICA; MAMMALIA; MURINAE; MUS; PLASMODIUM BERGHEI; PROTOZOA; RATTUS; RODENTIA; SCHISTOSOMA MANSONI; TRYPANOSOMA BRUCEI BRUCEI; VERMES;

EID: 77952019690     PISSN: 15353893     EISSN: 15353907     Source Type: Journal    
DOI: 10.1021/pr901019z     Document Type: Article

References (53)

1. Roth, E., Jr. Plasmodium falciparum carbohydrate metabolism: a connection between host cell and parasite Blood Cells 1990, 16 (2-3), 453 - 60, Discussion 461-6.
2. Wang, Y.; Holmes, E.; Nicholson, J. K.; Cloarec, O.; Chollet, J.; Tanner, M.; Singer, B. H.; Utzinger, J. Metabonomic investigations in mice infected with Schistosoma mansoni: an approach for biomarker identification Proc. Natl. Acad. Sci. U.S.A. 2004, 101 (34) 12676-81
3. Li, J. V.; Wang, Y.; Saric, J.; Nicholson, J. K.; Dirnhofer, S.; Singer, B. H.; Tanner, M.; Wittlin, S.; Holmes, E.; Utzinger, J. Global metabolic responses of NMRI mice to an experimental Plasmodium berghei infection J. Proteome Res. 2008, 7 (9) 3948-56
4. King, C. H.; Dangerfield-Cha, M. The unacknowledged impact of chronic schistosomiasis Chronic Illn. 2008, 4 (1) 65-79
5. Mackintosh, C. L.; Beeson, J. G.; Marsh, K. Clinical features and pathogenesis of severe malaria Trends Parasitol. 2004, 20 (12) 597-603
6. Noël, W.; Raes, G.; Hassanzadeh Ghassabeh, G.; De Baetselier, P.; Beschin, A. Alternatively activated macrophages during parasite infections Trends Parasitol. 2004, 20 (3) 126-33
7. Hotez, P. J.; Molyneux, D. H.; Fenwick, A.; Ottesen, E.; Ehrlich Sachs, S.; Sachs, J. D. Incorporating a rapid-impact package for neglected tropical diseases with programs for HIV/AIDS, tuberculosis, and malaria PLoS Med. 2006, 3 (5 e102
8. Amole, B. O.; Clarkson, A. B., Jr.; Shear, H. L. Pathogenesis of anemia in Trypanosoma brucei- infected mice Infect. Immun. 1982, 36 (3) 1060-8
9. Stoltzfus, R. J.; Chwaya, H. M.; Tielsch, J. M.; Schulze, K. J.; Albonico, M.; Savioli, L. Epidemiology of iron deficiency anemia in Zanzibari schoolchildren: the importance of hookworms Am. J. Clin. Nutr. 1997, 65 (1) 153-9
10. Anumudu, C.; Afolami, M.; Igwe, C.; Nwagwu, M.; Keshinro, O. Nutritional anaemia and malaria in preschool and school age children Ann. Afr. Med. 2008, 7 (1) 11-7
11. Saric, J.; Wang, Y.; Li, J.; Coen, M.; Utzinger, J.; Marchesi, J. R.; Keiser, J.; Veselkov, K.; Lindon, J. C.; Nicholson, J. K.; Holmes, E. Species variation in the fecal metabolome gives insight into differential gastrointestinal function J. Proteome Res. 2008, 7 (1) 352-60
12. Longfils, P.; Heang, U. K.; Soeng, H.; Sinuon, M. Weekly iron and folic acid supplementation as a tool to reduce anemia among primary school children in Cambodia Nutr. Rev. 2005, 63 (12 Pt. 2) S139-45
13. Alexander, J.; Bryson, K. T helper (h)1/Th2 and Leishmania: paradox rather than paradigm Immunol. Lett. 2005, 99 (1) 17-23
14. Peters, N.; Sacks, D. Immune privilege in sites of chronic infection: Leishmania and regulatory T cells Immunol. Rev. 2006, 213, 159-79
15. Belkaid, Y.; Blank, R. B.; Suffia, I. Natural regulatory T cells and parasites: a common quest for host homeostasis Immunol. Rev. 2006, 212, 287-300
16. Joosten, S. A.; Ottenhoff, T. H. Human CD4 and CD8 regulatory T cells in infectious diseases and vaccination Hum. Immunol. 2008, 69 (11) 760-70
17. Bettelli, E.; Korn, T.; Kuchroo, V. K. Th17: the third member of the effector T cell trilogy Curr. Opin. Immunol. 2007, 19 (6) 652-7
18. Mosmann, T. R.; Coffman, R. L. TH1 and TH2 cells: different patterns of lymphokine secretion lead to different functional properties Annu. Rev. Immunol. 1989, 7, 145-73
19. Mosmann, T. R.; Sad, S. The expanding universe of T-cell subsets: Th1, Th2 and more Immunol. Today 1996, 17 (3) 138-46
20. Mosmann, T. R.; Cherwinski, H.; Bond, M. W.; Giedlin, M. A.; Coffman, R. L. Two types of murine helper T cell clone. I. Definition according to profiles of lymphokine activities and secreted proteins J. Immunol. 1986, 136 (7) 2348-57
21. Pearce, E. J.; Kane, C. M.; Sun, J.; Taylor, J. J.; McKee, A. S.; Cervi, L. Th2 response polarization during infection with the helminth parasite Schistosoma mansoni Immunol. Rev. 2004, 201, 117-26
22. Hall, L. R.; Mehlotra, R. K.; Higgins, A. W.; Haxhiu, M. A.; Pearlman, E. An essential role for interleukin-5 and eosinophils in helminth-induced airway hyperresponsiveness Infect. Immun. 1998, 66 (9) 4425-30
23. Wilson, M. S.; Mentink-Kane, M. M.; Pesce, J. T.; Ramalingam, T. R.; Thompson, R.; Wynn, T. A. Immunopathology of schistosomiasis Immunol. Cell. Biol. 2007, 85 (2) 148-54
24. Korn, T.; Oukka, M.; Kuchroo, V.; Bettelli, E. Th17 cells: effector T cells with inflammatory properties Semin. Immunol. 2007, 19 (6) 362-71
25. Basso, A. S.; Cheroutre, H.; Mucida, D. More stories on Th17 cells Cell Res. 2009, 19 (4) 399-411
26. Jankovic, D.; Sher, A.; Yap, G. Th1/Th2 effector choice in parasitic infection: decision making by committee Curr. Opin. Immunol. 2001, 13 (4) 403-9
27. Keun, H. C.; Sidhu, J.; Pchejetski, D.; Lewis, J. S.; Marconell, H.; Patterson, M.; Bloom, S. R.; Amber, V.; Coombes, R. C.; Stebbing, J. Serum molecular signatures of weight change during early breast cancer chemotherapy Clin. Cancer Res. 2009, 15 (21) 6716-23
28. Martin, F. P. J.; Rezzi, S.; Philippe, D.; Tornier, L.; Messlik, A.; Hoelzlwimmer, G.; Bauer, P.; Quintanilla-Fend, L.; Loh, G.; Blaut, M.; Blum, S.; Kochhar, A.; Haller, D. Metabolic assessment of gradual development of moderate experimental colitis in IL-10 deficient mice J. Proteome Res. 2009, 8 (5) 2376-87
29. Grootveld, M.; Claxson, A. W. D.; Chaman, L. C.; Haycock, P.; Blake, D. R.; Haqwkes, G. E. High resolution proton NMR investigations of rat blood plasma FEBS. 1993, 322 (3) 266-276
30. Wang, Y.; Utzinger, J.; Saric, J.; Li, J. V.; Burckhardt, J.; Dirnhofer, S.; Nicholson, J. K.; Singer, B. H.; Brun, R.; Holmes, E. Global metabolic responses of mice to Trypanosoma brucei brucei infection Proc. Natl. Acad. Sci. U.S.A. 2008, 105 (16) 6127-32
31. Martins, Y. C.; Smith, M. J.; Pelajo-Machado, M.; Werneck, G. L.; Lenzi, H. L.; Daniel-Ribeiro, C. T.; Carvalho, L. J. Characterization of cerebral malaria in the outbred Swiss Webster mouse infected by Plasmodium berghei ANKA Int. J. Exp. Pathol. 2009, 90 (2) 119-30
32. Keita, M.; Bouteille, B.; Enanga, B.; Vallat, J. M.; Dumas, M. Trypanosoma brucei brucei: a long-term model of human African trypanosomiasis in mice, meningo-encephalitis, astrocytosis, and neurological disorders Exp. Parasitol. 1997, 85 (2) 183-92
33. el-Cheikh, M. C.; Borojevic, R. Extramedullar proliferation of eosinophil granulocytes in chronic schistosomiasis mansoni is mediated by a factor secreted by inflammatory macrophages Infect. Immun. 1990, 58 (3) 816-21
34. Murell, K. D.; Fried, B. Food-Borne Parasitic Zoonoses: Fish and Plant Borne Parasites; Springer: New York, NY, 2007; Vol. 11.
35. Chowdhury, F.; Williams, A.; Johnson, P. Validation and comparison of two multiplex technologies, Luminex and Mesoscale Discovery, for human cytokine profiling J. Immunol. Methods 2009, 340 (1) 55-64
36. Eriksson, L.; Antti, H.; Gottfries, J.; Holmes, E.; Johansson, E.; Lindgren, F.; Long, I.; Lundstedt, T.; Trygg, J.; Wold, S. Using chemometrics for navigating in the large data sets of genomics, proteomics, and metabonomics Anal. Bioanal. Chem. 2004, 380 (3) 419-29
37. Trygg, J.; Holmes, E.; Lundstedt, T. Chemometrics in metabonomics J. Proteome Res. 2007, 6 (2) 469-79
38. Trygg, J.; Wold, S. Orthogonal projections to latent structures (O-PLS) J. Chemom. 2002, 16 (3) 119-128
39. 1H NMR spectroscopic metabonomic studies Anal. Chem. 2005, 77 (2) 517-26
40. Nicholls, A. W.; Mortishire-Smith, R. J.; Nicholson, J. K. NMR spectroscopic-based metabonomic studies of urinary metabolite variation in acclimatizing germ-free rats Chem. Res. Toxicol. 2003, 16 (11) 1395-404
41. Yap, I. K. S.; Li, J. V.; Saric, J.; Martin, F. P.; Davies, H.; Wang, Y.; Wilson, I. D.; Nicholson, J. K.; Utzinger, J.; Marchesi, J. R.; Holmes, E. Metabonomic and microbiological analysis of the dynamic effect of vancomycin-induced gut microbiota modification in the mouse J. Proteome Res. 2008, 7 (9) 3718-28
42. Farinati, F.; Cardin, R.; De Maria, N.; Della Libera, G.; Marafin, C.; Lecis, E.; Burra, P.; Floreani, A.; Cecchetto, A.; Naccarato, R. Iron storage, lipid peroxidation and glutathione turnover in chronic anti-HCV positive hepatitis J. Hepatol. 1995, 22 (4) 449-56
43. Hervieu, V.; Lombard-Bohas, C.; Dumortier, J.; Boillot, O.; Scoazec, J. Y. Primary acinar cell carcinoma of the liver Virchows Arch. 2008, 452 (3) 337-41
44. Perlmann, P.; Perlmann, H.; Berzins, K.; Troye-Blomberg, M. Selected problems of malaria blood stage immunity Tokai J. Exp. Clin. Med. 1998, 23 (2) 55-62
45. Caldas, I. R.; Campi-Azevedo, A. C.; Oliveira, L. F.; Silveira, A. M.; Oliveira, R. C.; Gazzinelli, G. Human schistosomiasis mansoni: immune responses during acute and chronic phases of the infection Acta Trop. 2008, 108 (2-3) 109-17
46. Li, J. V.; Holmes, E.; Saric, J.; Keiser, J.; Dirnhofer, S.; Utzinger, J.; Wang, Y. Metabolic profiling of a Schistosoma mansoni infection in mouse tissues using magic angle spinning-nuclear magnetic resonance spectroscopy Int. J. Parasitol. 2009, 39, 547-58
47. Pearce, E. J.; MacDonald, A. S. The immunobiology of schistosomiasis Nat. Rev. Immunol. 2002, 2 (7) 499-511
48. Ajuebor, M. N.; Das, A. M.; Virag, L.; Flower, R. J.; Szabo, C.; Perretti, M. Role of resident peritoneal macrophages and mast cells in chemokine production and neutrophil migration in acute inflammation: evidence for an inhibitory loop involving endogenous IL-10 J. Immunol. 1999, 162 (3) 1685-91
49. Harada, A.; Sekido, N.; Akahoshi, T.; Wada, T.; Mukaida, N.; Matsushima, K. Essential involvement of interleukin-8 (IL-8) in acute inflammation J. Leukocyte Biol. 1994, 56 (5) 559-64
50. Donelson, J. E.; Hill, K. L.; El-Sayed, N. M. Multiple mechanisms of immune evasion by African trypanosomes Mol. Biochem. Parasitol. 1998, 91 (1) 51-66
51. Vincendeau, P.; Bouteille, B. Immunology and immunopathology of African trypanosomiasis An. Acad. Bras. Cienc. 2006, 78 (4) 645-65
52. 1H NMR spectroscopy-based metabolic phenotyping studies Anal. Chem. 2007, 79 (14) 5204-11
53. Teahan, O.; Gamble, S.; Holmes, E.; Waxman, J.; Nicholson, J. K.; Bevan, C.; Keun, H. C. Impact of analytical bias in metabonomic studies of human blood serum and plasma Anal. Chem. 2006, 78 (13) 4307-18