Metabolic profiling of a Schistosoma mansoni infection in mouse tissues using magic angle spinning-nuclear magnetic resonance spectroscopy

International Journal for Parasitology

Volumn 39, Issue 5, 2009, Pages 547-558

  Li, Jia V ^a,b   Holmes, Elaine ^a   Saric, Jasmina ^a,b   Keiser, Jennifer ^b   Dirnhofer, Stephan ^c   Utzinger, Jürg ^b   Wang, Yulan ^d  

^a Faculty of Medicine   (United Kingdom)

^b SWISS TROPICAL AND PUBLIC HEALTH INSTITUTE   (Switzerland)

^c UNIVERSITY HOSPITAL BASEL   (Switzerland)

^d Wuhan National Laboratory for Optoelectronics   (China)

Author keywords

Chemometrics; Magic angle spinning; Metabolic profiling; Mouse; NMR spectroscopy; Schistosoma mansoni; Schistosomiasis

Indexed keywords

AMINO ACID; FLATWORM; GLUCOSE; HOST-PATHOGEN INTERACTION; METABOLISM; MOLECULAR ANALYSIS; MORTALITY; NUCLEAR MAGNETIC RESONANCE; PHOSPHOLIPID; PRINCIPAL COMPONENT ANALYSIS; RODENT; SCHISTOSOMIASIS; SPECTRAL ANALYSIS; SPECTROSCOPY; URINE;

AMINO ACIDS; ANIMALS; FEMALE; INTESTINES; KIDNEY; LIVER; MAGNETIC RESONANCE SPECTROSCOPY; METABOLOME; METABOLOMICS; MICE; MICE, INBRED STRAINS; PHOSPHOLIPIDS; SCHISTOSOMA MANSONI; SCHISTOSOMIASIS MANSONI; SPLEEN;

AMINO ACID; PHOSPHOLIPID;

ANIMAL; FEMALE; INBRED MOUSE STRAIN; INTESTINE; ISOLATION AND PURIFICATION; KIDNEY; LIVER; METABOLISM; METABOLOME; METABOLOMICS; MOUSE; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; PARASITOLOGY; PATHOLOGY; PROCEDURES; SCHISTOSOMA MANSONI; SCHISTOSOMIASIS MANSONI; SPLEEN;

EID: 59749103024     PISSN: 00207519     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.ijpara.2008.10.010     Document Type: Article

References (64)

1. Abdallahi O.M.S., Hanna S., De Reggi M., and Gharib B. Visualization of oxygen radical production in mouse liver in response to infection with Schistosoma mansoni. Liver 19 (1999) 495-500
2. Ahmed S.A., and Gad M.Z. Effect of schistosomal infection and its treatment on some key enzymes of glucose metabolism in mice livers. Arzneimittelforschung 45 (1995) 1324-1328
3. Badr S.G.E., Pica-Mattoccia L., Moroni R., Angelico M., and Cioli D. Effect of bile salts on oviposition in vitro by Schistosoma mansoni. Parasitol. Res. 85 (1999) 421-423
4. Balemba O.B., Mbassa G.K., Assey R.J., Kahwa C.K.B., Makundi A.E., Hay-Schmidt A., Dantzer V., and Semuguruka W.D. Lesions of the enteric nervous system and the possible role of mast cells in the pathogenic mechanisms of migration of schistosome eggs in the small intestine of cattle during Schistosoma bovis infection. Vet. Parasitol. 90 (2000) 57-71
5. Balemba O.B., Semuguruka W.D., Hay-Schmidt A., Johansen M.V., and Dantzer V. Vasoactive intestinal peptide and substance P-like immunoreactivities in the enteric nervous system of the pig correlate with the severity of pathological changes induced by Schistosoma japonicum. Int. J. Parasitol. 31 (2001) 1503-1514
6. 1H magnetic resonance spectroscopy in inflammatory bowel diseases: distinguishing ulcerative colitis from Crohn's disease. J. Gastroenterol. 96 (2001) 442-448
7. Bezerra A.S.A., D'Ippolito G., Caldana R.P., Cecin A.O., Ahmed M., and Szejnfeld J. Chronic hepatosplenic schistosomiasis mansoni: magnetic resonance imaging and magnetic resonance angiography findings. Acta Radiol. 48 (2007) 125-134
8. Blennerhassett M.G., Vignjevic P., Vermillion D.L., and Collins S.M. Inflammation causes hyperplasia and hypertrophy in smooth-muscle of rat small-intestine. Am. J. Physiol. 262 (1992) G1041-G1046
9. Bogers J., Moreels T., De Man J., Vrolix G., Jacobs W., Pelckmans P., and Van Marck E. Schistosoma mansoni infection causing diffuse enteric inflammation and damage of the enteric nervous system in the mouse small intestine. Neurogastroenterol. Motil. 12 (2000) 431-440
10. Boros D.L. Immunopathology of Schistosoma mansoni infection. Clin. Microbiol. Rev. 2 (1989) 250-269
11. 1H NMR-based metabonomics. Nat. Med. 8 (2002) 1439-1444
12. Cheng L.L., Ma M.J., Becerra L., Ptak T., Tracey I., Lackner A., and Gonzalez R.G. Quantitative neuropathology by high resolution magic angle spinning proton magnetic resonance spectroscopy. Proc. Natl. Acad. Sci. U.S.A 94 (1997) 6408-6413
13. Cho S.G., Kim M.Y., Kim H.J., Kim Y.S., Choi W., Shin S.H., Hong K.C., Kim Y.B., Lee J.H., and Suh C.H. Chronic hepatitis: In vivo proton MR spectroscopic evaluation of the liver and correlation with histopathologic findings. Radiology 221 (2001) 740-746
14. Clegg J.A. In vitro cultivation of Schistosoma mansoni. Exp. Parasitol. 16 (1965) 133-147
15. Das J., Ghosh J., Manna P., and Sil P.C. Taurine provides antioxidant defense against NaF-induced cytotoxicity in murine hepatocytes. Pathophysiology 15 (2008) 181-190
16. Daugherty J., Garson S., and Heyneman D. The effect of Schistosoma mansoni infections on liver function in mice. I. amino acid oxidase and ammonia. Am. J. Trop. Med. Hyg. 3 (1954) 511-517
17. De Jonge F., Van Nassauw L., Adriaensen D., Van Meir F., Miller H.R.P., Van Marck E., and Timmermans J.P. Effect of intestinal inflammation on capsaicin-sensitive afferents in the ileum of Schistosoma mansoni-infected mice. Histochem. Cell Biol. 119 (2003) 477-484
18. De Jonge F., Van Nassauw L., De Man J.G., De Winter B.Y., Van Meir F., Depoortere I., Peeters T.L., Pelckmans P.A., Van Marck E., and Timmermans J.P. Effects of Schistosoma mansoni infection on somatostatin and somatostatin receptor 2A expression in mouse ileum. Neurogastroenterol. Motil. 15 (2003) 149-159
19. De Jonge W.J., Marescau B., D'Hooge R., De Deyn P.P., Hallemeesch M.M., Deutz N.E., Ruijter J.M., and Lamers W.H. Overexpression of arginase alters circulating and tissue amino acids and guanidino compounds and affects neuromotor behavior in mice. J. Nutr. 131 (2001) 2732-2740
20. De Man J.G., Chatterjee S., De Winter B.Y., Vrolix G., Van Marck E.A., Herman A.G., and Pelckmans P.A. Effect of somatostatin on gastrointestinal contractility in Schistosoma mansoni infected mice. Int. J. Parasitol. 32 (2002) 1309-1320
21. Dunn M.A., Rojkind M., Warren K.S., Hait P.K., Rifas L., and Seifter S. Liver collagen-synthesis in murine schistosomiasis. J. Clin. Invest. 59 (1977) 666-674
22. El-Garem A.A. Schistosomiasis. Digestion 59 (1998) 589-605
23. Eriksson L., Antti H., Gottfries J., Holmes E., Johansson E., Lindgren F., Long I., Lundstedt T., Trygg J., and Wold S. Using chemometrics for navigating in the large data sets of genomics, proteomics, and metabonomics (gpm). Anal. Bioanal. Chem. 380 (2004) 419-429
24. Fan W.M.T. Metabolite profiling by one- and two-dimensional NMR analysis of complex mixtures. Prog. Nucl. Magn. Reson. Spectrosc. 28 (1996) 161-219
25. Freitas C.R.L., Barbosa A.A., Fernandes A.L.M., and Andrade Z.A. Pathology of the spleen in hepatosplenic schistosomiasis. Morphometric evaluation and extracellular matrix changes. Mem. Inst. Oswaldo Cruz 94 (1999) 815-822
26. Gryseels B., Polman K., Clerinx J., and Kestens L. Human schistosomiasis. Lancet 368 (2006) 1106-1118
27. Harvie M., Jordan T.W., and La Flamme A.C. Differential liver protein expression during schistosomiasis. Infect. Immun. 75 (2007) 736-744
28. Huxtable R.J. Physiological actions of taurine. Physiol. Rev. 72 (1992) 101-163
29. Isseroff H., Bock K., Owczarek A., and Smith K.R. Schistosomiasis - proline production and pelease by ova. J. Parasitol. 69 (1983) 285-289
30. Johansen M.V., Simonsen P.E., Butterworth A.E., Ouma J.H., Mbugua G.G., Sturrock R.F., Orinda D.A.O., and Christensen N.O. A survey for Schistosoma mansoni induced kidney-disease in children in an endemic area of Machakos district, Kenya. Acta Trop. 58 (1994) 21-28
31. Kazura J.W., Fanning M.M., Blumer J.L., and Mahmoud A.A.F. Role of cell-generated hydrogen peroxide in granulocyte-mediated killing of schistosomula of Schistosoma mansoni in vitro. J. Clin. Invest. 67 (1981) 93-102
32. Khan W.I., and Collins S.M. Gut motor function: immunological control in enteric infection and inflammation. Clin. Exp. Immunol. 143 (2006) 389-397
33. King C.H., and Dangerfield-Cha M. The unacknowledged impact of chronic schistosomiasis. Chronic Illn. 4 (2008) 65-79
34. Klimberg V.S., and McClellan J.L. Glutamine, cancer, and its therapy. Am. J. Surg. 172 (1996) 418-424
35. Lambertucci J.R., Serufo J.C., Gerspacher-Lara R., Rayes A.A.M., Teixeira R., Nobre V., and Antunes C.M.F. Schistosoma mansoni: assessment of morbidity before and after control. Acta Trop. 77 (2000) 101-109
36. Lambertucci J.R., Silva L.C., Andrade L.M., de Queiroz L.C., Carvalho V.T., Voieta I., and Antunes C.M. Imaging techniques in the evaluation of morbidity in schistosomiasis mansoni. Acta Trop. 108 (2008) 209-217
37. Lindon J.C., Holmes E., Bollard M.E., Stanley E.G., and Nicholson J.K. Metabonomics technologies and their applications in physiological monitoring, drug safety assessment and disease diagnosis. Biomarkers 9 (2004) 1-31
38. Lukacs N.W., Kunkel S.L., Strieter R.M., Warmington K., and Chensue S.W. The role of macrophage inflammatory protein-1-alpha in Schistosoma mansoni egg-induced granulomatous inflammation. J. Exp. Med. 177 (1993) 1551-1559
39. Maher J.J., and Mcguire R.F. Extracellular-matrix gene-expression increases preferentially in rat lipocytes and sinusoidal endothelial-cells during hepatic-fibrosis in vivo. J. Clin. Invest. 86 (1990) 1641-1648
40. Martin F.P.J., Verdu E.F., Wang Y.L., Dumas M.E., Yap I.K.S., Cloarec O., Bergonzelli G.E., Corthesy-Theulaz I., Kochhar S., Holmes E., Lindon J.C., Collins S.M., and Nicholson J.K. Transgenomic metabolic interactions in a mouse disease model: interactions of Trichinella spiralis infection with dietary Lactobacillus paracasei supplementation. J. Proteome Res. 5 (2006) 2185-2193
41. Miller T.J., Hanson R.D., and Yancey P.H. Developmental changes in organic osmolytes in prenatal and postnatal rat tissues. Comp. Biochem. Physiol. A Mol. Integr. Physiol. 125 (2000) 45-56
42. Moore D.V., and Sandground J.H. The relative egg producing capacity of Schistosoma mansoni and Schistosoma japonicum. Am. J. Trop. Med. Hyg. 5 (1956) 831-840
43. Nicholson J.K., Connelly J., Lindon J.C., and Holmes E. Metabonomics: a platform for studying drug toxicity and gene function. Nat. Rev. Drug Discov. 1 (2002) 153-161
44. Nicholson J.K., Lindon J.C., and Holmes E. 'Metabonomics': understanding the metabolic responses of living systems to pathophysiological stimuli via multivariate statistical analysis of biological NMR spectroscopic data. Xenobiotica 29 (1999) 1181-1189
45. 1H NMR study of metabolic alterations in the small-intestine of rats infected with Hymenolepis-diminuta. Int. J. Biochem. 25 (1993) 1587-1591
46. Ross A.G.P., Bartley P.B., Sleigh A.C., Olds G.R., Li Y.S., Williams G.M., and McManus D.P. Schistosomiasis. N. Engl. J. Med. 346 (2002) 1212-1220
47. Ross A.G.P., Sleigh A.C., Li Y.S., Davis G.M., Williams G.M., Jiang Z., Feng Z., and McManus D.P. Schistosomiasis in the People's Republic of China: prospects and challenges for the 21st century. Clin. Microbiol. Rev. 14 (2001) 270-295
48. Shen G.J., Jiao M.D., Li Q.Y., Xu H., Han J.M., and Xin X.M. Study on histopathology, ultrasonography and some special serum enzymes and collagens for 38 advanced patients of schistosomiasis japonica. Acta Trop. 82 (2002) 235-246
49. Schlotterbeck G., Ross A., Dieterle F., and Senn H. Metabolic profiling technologies for biomarker discovery in biomedicine and drug development. Pharmacogenomics 7 (2006) 1055-1075
50. Silva L.M., Fernandes A.L.M., Barbosa A., Oliveira I.R., and Andrade Z.A. Significance of schistosomal granuloma modulation. Mem. Inst. Oswaldo Cruz 95 (2000) 353-361
51. Sobh M., Moustafa F., Ramzy R., Saad M., Deelder A., and Ghoneim M. Schistosoma mansoni nephropathy in Syrian golden hamsters: effect of dose and duration of infection. Nephron 59 (1991) 121-130
52. Son M., Ko J.I., Kim W.B., Kang H.K., and Kim B.K. Taurine can ameliorate inflammatory bowel disease in rats. Adv. Exp. Med. Biol. 442 (1998) 291-298
53. Steinmann P., Keiser J., Bos R., Tanner M., and Utzinger J. Schistosomiasis and water resources development: systematic review, meta-analysis, and estimates of people at risk. Lancet Infect. Dis. 6 (2006) 411-425
54. Trygg J., and Wold S. Orthogonal projections to latent structures (O-PLS). J. Chemometr. 16 (2002) 119-128
55. Utzinger J., Chollet J., Tu Z.W., Xiao S.H., and Tanner M. Comparative study of the effects of artemether and artesunate on juvenile and adult Schistosoma mansoni in experimentally infected mice. Trans. R. Soc. Trop. Med. Hyg. 96 (2002) 318-323
56. Wang L.J., Cao Y., and Shi H.N. Helminth infections and intestinal inflammation. World J. Gastroenterol. 14 (2008) 5125-5132
57. Wang Y.L., Holmes E., Nicholson J.K., Cloarec O., Chollet J., Tanner M., Singer B.H., and Utzinger J. Metabonomic investigations in mice infected with Schistosoma mansoni: an approach for biomarker identification. Proc. Natl. Acad. Sci. U.S.A 101 (2004) 12676-12681
58. 1H NMR spectroscopy and multivariate data analysis. J. Proteome Res. 4 (2005) 1324-1329
59. Wang Y.L., Tang H.R., Nicholson J.K., Hylands P.J., Sampson J., and Holmes E. A metabonomic strategy for the detection of the metabolic effects of chamomile (Matricaria recutita L) ingestion. J. Agric. Food Chem. 53 (2005) 191-196
60. Wang Y.L., Utzinger J., Xiao S.H., Xue J., Nicholson J.K., Tanner M., Singer B.H., and Holmes E. System level metabolic effects of a Schistosoma japonicum infection in the Syrian hamster. Mol. Biochem. Parasitol. 146 (2006) 1-9
61. Waters N.J., Holmes E., Williams A., Waterfield C.J., Farrant R.D., and Nicholson J.K. NMR and pattern recognition studies on the time-related metabolic effects of alpha-naphthylisothiocyanate on liver, urine, and plasma in the rat: an integrative metabonomic approach. Chem. Res. Toxicol. 14 (2001) 1401-1412
62. Weinstock J.V. Vasoactive intestinal peptide regulation of granulomatous inflammation in murine schistosomiasis mansoni. Adv. Neuroimmunol. 6 (1996) 95-105
63. Westerhuis J.A., Kourti T., and MacGregor J.F. Analysis of multiblock and hierarchical PCA and PLS models. J. Chemometr. 12 (1998) 301-321
64. Yaqoob P., and Calder P.C. Glutamine requirement of proliferating T lymphocytes. Nutrition 13 (1997) 646-651