Skip to main content
Top
Published in: Gut Pathogens 1/2019

Open Access 01-12-2019 | Research

NMR metabolomics reveals effects of Cryptosporidium infections on host cell metabolome

Authors: Christopher N. Miller, Charalampos G. Panagos, William R. T. Mosedale, Martin Kváč, Mark J. Howard, Anastasios D. Tsaousis

Published in: Gut Pathogens | Issue 1/2019

Login to get access

Abstract

Background

Cryptosporidium is an important gut microbe whose contributions towards infant and immunocompromise patient mortality rates are steadily increasing. Over the last decade, we have seen the development of various tools and methods for studying Cryptosporidium infection and its interactions with their hosts. One area that is sorely overlooked is the effect infection has on host metabolic processes.

Results

Using a 1H nuclear magnetic resonance approach to metabolomics, we have explored the nature of the mouse gut metabolome as well as providing the first insight into the metabolome of an infected cell line. Statistical analysis and predictive modelling demonstrated new understandings of the effects of a Cryptosporidium infection, while verifying the presence of known metabolic changes. Of note is the potential contribution of host derived taurine to the diarrhoeal aspects of the disease previously attributed to a solely parasite-based alteration of the gut environment, in addition to other metabolites involved with host cell catabolism.

Conclusion

This approach will spearhead our understanding of the Cryptosporidium-host metabolic exchange and provide novel targets for tackling this deadly parasite.
Appendix
Available only for authorised users
Literature
1.
go back to reference Checkley W, White AC Jr, Jaganath D, Arrowood MJ, Chalmers RM, Chen XM, Fayer R, Griffiths JK, Guerrant RL, Hedstrom L, Huston CD, Kotloff KL, Kang G, Mead JR, Miller M, Petri WA Jr, Priest JW, Roos DS, Striepen B, Thompson RC, Ward HD, Van Voorhis WA, Xiao L, Zhu G, Houpt ER. A review of the global burden, novel diagnostics, therapeutics, and vaccine targets for Cryptosporidium. Lancet Infect Dis. 2015;15(1):85–94.PubMedCrossRef Checkley W, White AC Jr, Jaganath D, Arrowood MJ, Chalmers RM, Chen XM, Fayer R, Griffiths JK, Guerrant RL, Hedstrom L, Huston CD, Kotloff KL, Kang G, Mead JR, Miller M, Petri WA Jr, Priest JW, Roos DS, Striepen B, Thompson RC, Ward HD, Van Voorhis WA, Xiao L, Zhu G, Houpt ER. A review of the global burden, novel diagnostics, therapeutics, and vaccine targets for Cryptosporidium. Lancet Infect Dis. 2015;15(1):85–94.PubMedCrossRef
2.
go back to reference Kotloff KL, Nataro JP, Blackwelder WC, Nasrin D, Farag TH, Panchalingam S, Wu Y, Sow SO, Sur D, Breiman RF, Faruque AS, Zaidi AK, Saha D, Alonso PL, Tamboura B, Sanogo D, Onwuchekwa U, Manna B, Ramamurthy T, Kanungo S, Ochieng JB, Omore R, Oundo JO, Hossain A, Das SK, Ahmed S, Qureshi S, Quadri F, Adegbola RA, Antonio M, Hossain MJ, Akinsola A, Mandomando I, Nhampossa T, Acacio S, Biswas K, O’Reilly CE, Mintz ED, Berkeley LY, Muhsen K, Sommerfelt H, Robins-Browne RM, Levine MM. Burden and aetiology of diarrhoeal disease in infants and young children in developing countries (the Global Enteric Multicenter Study, GEMS): a prospective, case-control study. Lancet. 2013;382(9888):209–22.PubMedCrossRef Kotloff KL, Nataro JP, Blackwelder WC, Nasrin D, Farag TH, Panchalingam S, Wu Y, Sow SO, Sur D, Breiman RF, Faruque AS, Zaidi AK, Saha D, Alonso PL, Tamboura B, Sanogo D, Onwuchekwa U, Manna B, Ramamurthy T, Kanungo S, Ochieng JB, Omore R, Oundo JO, Hossain A, Das SK, Ahmed S, Qureshi S, Quadri F, Adegbola RA, Antonio M, Hossain MJ, Akinsola A, Mandomando I, Nhampossa T, Acacio S, Biswas K, O’Reilly CE, Mintz ED, Berkeley LY, Muhsen K, Sommerfelt H, Robins-Browne RM, Levine MM. Burden and aetiology of diarrhoeal disease in infants and young children in developing countries (the Global Enteric Multicenter Study, GEMS): a prospective, case-control study. Lancet. 2013;382(9888):209–22.PubMedCrossRef
3.
go back to reference Striepen B. Parasitic infections: time to tackle cryptosporidiosis. Nature. 2013;503(7475):189–91.PubMedCrossRef Striepen B. Parasitic infections: time to tackle cryptosporidiosis. Nature. 2013;503(7475):189–91.PubMedCrossRef
4.
go back to reference Wanyiri JW, Kanyi H, Maina S, Wang DE, Steen A, Ngugi P, Kamau T, Waithera T, O’Connor R, Gachuhi K, Wamae CN, Mwamburi M, Ward HD. Cryptosporidiosis in HIV/AIDS patients in Kenya: clinical features, epidemiology, molecular characterization and antibody responses. Am J Trop Med Hyg. 2014;91(2):319–28.PubMedPubMedCentralCrossRef Wanyiri JW, Kanyi H, Maina S, Wang DE, Steen A, Ngugi P, Kamau T, Waithera T, O’Connor R, Gachuhi K, Wamae CN, Mwamburi M, Ward HD. Cryptosporidiosis in HIV/AIDS patients in Kenya: clinical features, epidemiology, molecular characterization and antibody responses. Am J Trop Med Hyg. 2014;91(2):319–28.PubMedPubMedCentralCrossRef
5.
go back to reference O’Connor RM, Shaffie R, Kang G, Ward HD. Cryptosporidiosis in patients with HIV/AIDS. AIDS. 2011;25(5):549–60.PubMedCrossRef O’Connor RM, Shaffie R, Kang G, Ward HD. Cryptosporidiosis in patients with HIV/AIDS. AIDS. 2011;25(5):549–60.PubMedCrossRef
6.
go back to reference Caccio SM. Molecular epidemiology of human cryptosporidiosis. Parassitologia. 2005;47(2):185–92.PubMed Caccio SM. Molecular epidemiology of human cryptosporidiosis. Parassitologia. 2005;47(2):185–92.PubMed
7.
go back to reference Leoni F, Amar C, Nichols G, Pedraza-Diaz S, McLauchlin J. Genetic analysis of Cryptosporidium from 2414 humans with diarrhoea in England between 1985 and 2000. J Med Microbiol. 2006;55(Pt 6):703–7.PubMedCrossRef Leoni F, Amar C, Nichols G, Pedraza-Diaz S, McLauchlin J. Genetic analysis of Cryptosporidium from 2414 humans with diarrhoea in England between 1985 and 2000. J Med Microbiol. 2006;55(Pt 6):703–7.PubMedCrossRef
9.
go back to reference Wielinga PR, de Vries A, van der Goot TH, Mank T, Mars MH, Kortbeek LM, van der Giessen JW. Molecular epidemiology of Cryptosporidium in humans and cattle in The Netherlands. Int J Parasitol. 2008;38(7):809–17.PubMedCrossRef Wielinga PR, de Vries A, van der Goot TH, Mank T, Mars MH, Kortbeek LM, van der Giessen JW. Molecular epidemiology of Cryptosporidium in humans and cattle in The Netherlands. Int J Parasitol. 2008;38(7):809–17.PubMedCrossRef
10.
go back to reference Doumbo O, Rossignol JF, Pichard E, Traore HA, Dembele TM, Diakite M, Traore F, Diallo DA. Nitazoxanide in the treatment of cryptosporidial diarrhea and other intestinal parasitic infections associated with acquired immunodeficiency syndrome in tropical Africa. Am J Trop Med Hyg. 1997;56(6):637–9.PubMedCrossRef Doumbo O, Rossignol JF, Pichard E, Traore HA, Dembele TM, Diakite M, Traore F, Diallo DA. Nitazoxanide in the treatment of cryptosporidial diarrhea and other intestinal parasitic infections associated with acquired immunodeficiency syndrome in tropical Africa. Am J Trop Med Hyg. 1997;56(6):637–9.PubMedCrossRef
11.
go back to reference Domjahn BT, Hlavsa MC, Anderson B, Schulkin J, Leon J, Jones JL. A survey of US obstetrician-gynecologists’ clinical and epidemiological knowledge of cryptosporidiosis in pregnancy. Zoonoses Public Health. 2014;61(5):356–63.PubMedCrossRef Domjahn BT, Hlavsa MC, Anderson B, Schulkin J, Leon J, Jones JL. A survey of US obstetrician-gynecologists’ clinical and epidemiological knowledge of cryptosporidiosis in pregnancy. Zoonoses Public Health. 2014;61(5):356–63.PubMedCrossRef
12.
go back to reference Hussien SM, Abdella OH, Abu-Hashim AH, Aboshiesha GA, Taha MA, El-Shemy AS, El-Bader MM. Comparative study between the effect of nitazoxanide and paromomycine in treatment of cryptosporidiosis in hospitalized children. J Egypt Soc Parasitol. 2013;43(2):463–70.PubMedCrossRef Hussien SM, Abdella OH, Abu-Hashim AH, Aboshiesha GA, Taha MA, El-Shemy AS, El-Bader MM. Comparative study between the effect of nitazoxanide and paromomycine in treatment of cryptosporidiosis in hospitalized children. J Egypt Soc Parasitol. 2013;43(2):463–70.PubMedCrossRef
13.
go back to reference Manjunatha UH, Vinayak S, Zambriski JA, Chao AT, Sy T, Noble CG, Bonamy GMC, Kondreddi RR, Zou B, Gedeck P, Brooks CF, Herbert GT, Sateriale A, Tandel J, Noh S, Lakshminarayana SB, Lim SH, Goodman LB, Bodenreider C, Feng G, Zhang L, Blasco F, Wagner J, Leong FJ, Striepen B, Diagana TT. A Cryptosporidium PI(4)K inhibitor is a drug candidate for cryptosporidiosis. Nature. 2017;546(7658):376–80.PubMedPubMedCentralCrossRef Manjunatha UH, Vinayak S, Zambriski JA, Chao AT, Sy T, Noble CG, Bonamy GMC, Kondreddi RR, Zou B, Gedeck P, Brooks CF, Herbert GT, Sateriale A, Tandel J, Noh S, Lakshminarayana SB, Lim SH, Goodman LB, Bodenreider C, Feng G, Zhang L, Blasco F, Wagner J, Leong FJ, Striepen B, Diagana TT. A Cryptosporidium PI(4)K inhibitor is a drug candidate for cryptosporidiosis. Nature. 2017;546(7658):376–80.PubMedPubMedCentralCrossRef
14.
go back to reference Sparks H, Nair G, Castellanos-Gonzalez A, White AC Jr. Treatment of Cryptosporidium: what we know, gaps, and the way forward. Curr Trop Med Rep. 2015;2(3):181–7.PubMedPubMedCentralCrossRef Sparks H, Nair G, Castellanos-Gonzalez A, White AC Jr. Treatment of Cryptosporidium: what we know, gaps, and the way forward. Curr Trop Med Rep. 2015;2(3):181–7.PubMedPubMedCentralCrossRef
15.
go back to reference Briggs AD, Boxall NS, Van Santen D, Chalmers RM, McCarthy ND. Approaches to the detection of very small, common, and easily missed outbreaks that together contribute substantially to human Cryptosporidium infection. Epidemiol Infect. 2014;142(9):1869–76.PubMedCrossRef Briggs AD, Boxall NS, Van Santen D, Chalmers RM, McCarthy ND. Approaches to the detection of very small, common, and easily missed outbreaks that together contribute substantially to human Cryptosporidium infection. Epidemiol Infect. 2014;142(9):1869–76.PubMedCrossRef
16.
go back to reference Girouard D, Gallant J, Akiyoshi DE, Nunnari J, Tzipori S. Failure to propagate Cryptosporidium spp. in cell-free culture. J Parasitol. 2006;92(2):399–400.PubMedCrossRef Girouard D, Gallant J, Akiyoshi DE, Nunnari J, Tzipori S. Failure to propagate Cryptosporidium spp. in cell-free culture. J Parasitol. 2006;92(2):399–400.PubMedCrossRef
17.
go back to reference Karanis P, Aldeyarbi HM. Evolution of Cryptosporidium in vitro culture. Int J Parasitol. 2011;41(12):1231–42.PubMedCrossRef Karanis P, Aldeyarbi HM. Evolution of Cryptosporidium in vitro culture. Int J Parasitol. 2011;41(12):1231–42.PubMedCrossRef
19.
go back to reference Muller J, Hemphill A. In vitro culture systems for the study of apicomplexan parasites in farm animals. Int J Parasitol. 2013;43(2):115–24.PubMedCrossRef Muller J, Hemphill A. In vitro culture systems for the study of apicomplexan parasites in farm animals. Int J Parasitol. 2013;43(2):115–24.PubMedCrossRef
20.
go back to reference Morada M, Lee S, Gunther-Cummins L, Weiss LM, Widmer G, Tzipori S, Yarlett N. Continuous culture of Cryptosporidium parvum using hollow fiber technology. Int J Parasitol. 2016;46(1):21–9.PubMedCrossRef Morada M, Lee S, Gunther-Cummins L, Weiss LM, Widmer G, Tzipori S, Yarlett N. Continuous culture of Cryptosporidium parvum using hollow fiber technology. Int J Parasitol. 2016;46(1):21–9.PubMedCrossRef
21.
go back to reference Bones AJ, Josse L, More C, Miller CN, Michaelis M, Tsaousis AD. Past and future trends of Cryptosporidium in vitro research. Exp Parasitol. 2019;196:28–37.PubMedPubMedCentralCrossRef Bones AJ, Josse L, More C, Miller CN, Michaelis M, Tsaousis AD. Past and future trends of Cryptosporidium in vitro research. Exp Parasitol. 2019;196:28–37.PubMedPubMedCentralCrossRef
22.
go back to reference Miller CN, Josse L, Brown I, Blakeman B, Povey J, Yiangou L, Price M, Cinatl JJ, Xue WF, Michaelis M, Tsaousis AD. A cell culture platform for Cryptosporidium that enables long-term cultivation and new tools for the systematic investigation of its biology. Int J Parasitol. 2018;48(3–4):197–201.PubMedPubMedCentralCrossRef Miller CN, Josse L, Brown I, Blakeman B, Povey J, Yiangou L, Price M, Cinatl JJ, Xue WF, Michaelis M, Tsaousis AD. A cell culture platform for Cryptosporidium that enables long-term cultivation and new tools for the systematic investigation of its biology. Int J Parasitol. 2018;48(3–4):197–201.PubMedPubMedCentralCrossRef
24.
go back to reference Miller CN, Josse L, Tsaousis AD. Localization of Fe–S biosynthesis machinery in Cryptosporidium parvum mitosome. J Eukaryot Microbiol. 2018;65(6):913–22.PubMedPubMedCentralCrossRef Miller CN, Josse L, Tsaousis AD. Localization of Fe–S biosynthesis machinery in Cryptosporidium parvum mitosome. J Eukaryot Microbiol. 2018;65(6):913–22.PubMedPubMedCentralCrossRef
25.
go back to reference Sponseller JK, Griffiths JK, Tzipori S. The evolution of respiratory Cryptosporidiosis: evidence for transmission by inhalation. Clin Microbiol Rev. 2014;27(3):575–86.PubMedPubMedCentralCrossRef Sponseller JK, Griffiths JK, Tzipori S. The evolution of respiratory Cryptosporidiosis: evidence for transmission by inhalation. Clin Microbiol Rev. 2014;27(3):575–86.PubMedPubMedCentralCrossRef
26.
go back to reference Allman EL, Painter HJ, Samra J, Carrasquilla M, Llinás M. Metabolomic profiling of the malaria box reveals antimalarial target pathways. Antimicrob Agents Chemother. 2016;60(11):6635–49.PubMedPubMedCentralCrossRef Allman EL, Painter HJ, Samra J, Carrasquilla M, Llinás M. Metabolomic profiling of the malaria box reveals antimalarial target pathways. Antimicrob Agents Chemother. 2016;60(11):6635–49.PubMedPubMedCentralCrossRef
27.
go back to reference Ng JS, Ryan U, Trengove RD, Maker GL. Development of an untargeted metabolomics method for the analysis of human faecal samples using Cryptosporidium-infected samples. Mol Biochem Parasitol. 2012;185(2):145–50.PubMedCrossRef Ng JS, Ryan U, Trengove RD, Maker GL. Development of an untargeted metabolomics method for the analysis of human faecal samples using Cryptosporidium-infected samples. Mol Biochem Parasitol. 2012;185(2):145–50.PubMedCrossRef
28.
go back to reference Ng Hublin JS, Ryan U, Trengove R, Maker G. Metabolomic profiling of faecal extracts from Cryptosporidium parvum infection in experimental mouse models. PLoS ONE. 2013;8(10):e77803.PubMedPubMedCentralCrossRef Ng Hublin JS, Ryan U, Trengove R, Maker G. Metabolomic profiling of faecal extracts from Cryptosporidium parvum infection in experimental mouse models. PLoS ONE. 2013;8(10):e77803.PubMedPubMedCentralCrossRef
29.
go back to reference Saric J, Wang Y, Li J, Coen M, Utzinger J, Marchesi JR, Keiser J, Veselkov K, Lindon JC, Nicholson JK, Holmes E. Species variation in the fecal metabolome gives insight into differential gastrointestinal function. J Proteome Res. 2008;7(1):352–60.PubMedCrossRef Saric J, Wang Y, Li J, Coen M, Utzinger J, Marchesi JR, Keiser J, Veselkov K, Lindon JC, Nicholson JK, Holmes E. Species variation in the fecal metabolome gives insight into differential gastrointestinal function. J Proteome Res. 2008;7(1):352–60.PubMedCrossRef
30.
go back to reference Tedros B, Somorjai RL, Smith IC. MR metabolomics of fecal extracts: applications in the study of bowel diseases. Magn Reson Chem. 2009;47:S54–61.CrossRef Tedros B, Somorjai RL, Smith IC. MR metabolomics of fecal extracts: applications in the study of bowel diseases. Magn Reson Chem. 2009;47:S54–61.CrossRef
31.
go back to reference Hong Y, Ahn Y, Park J, Lee J, Lee H, Huh C, Kim D, Ryu DH, Hwang G. 1H NMR-based metabonomic assessment of probiotic effects in a colitis mouse model. Arch Pharm Res. 2010;33(7):1091–101.PubMedCrossRef Hong Y, Ahn Y, Park J, Lee J, Lee H, Huh C, Kim D, Ryu DH, Hwang G. 1H NMR-based metabonomic assessment of probiotic effects in a colitis mouse model. Arch Pharm Res. 2010;33(7):1091–101.PubMedCrossRef
32.
go back to reference Wu J, An Y, Yao J, Wang Y, Tang H. An optimised sample preparation method for NMR-based faecal metabonomic analysis. Analyst. 2010;135(5):1023–30.PubMedCrossRef Wu J, An Y, Yao J, Wang Y, Tang H. An optimised sample preparation method for NMR-based faecal metabonomic analysis. Analyst. 2010;135(5):1023–30.PubMedCrossRef
33.
go back to reference Jacobs DM, Deltimple N, van Velzen E, van Dorsten FA, Bingham M, Vaughan EE, van Duynhoven J. 1H NMR metabolite profiling of feces as a tool to assess the impact of nutrition on the human microbiome. NMR Biomed. 2008;21(6):615–26.PubMedCrossRef Jacobs DM, Deltimple N, van Velzen E, van Dorsten FA, Bingham M, Vaughan EE, van Duynhoven J. 1H NMR metabolite profiling of feces as a tool to assess the impact of nutrition on the human microbiome. NMR Biomed. 2008;21(6):615–26.PubMedCrossRef
34.
go back to reference Sengupta A, Ghosh S, Das BK, Panda A, Tripathy R, Pied S, Ravindran B, Pathak S, Sharma S, Sonawat HM. Host metabolic responses to Plasmodium falciparum infections evaluated by 1H NMR metabolomics. Mol BioSyst. 2016;12(11):3324–32.PubMedCrossRef Sengupta A, Ghosh S, Das BK, Panda A, Tripathy R, Pied S, Ravindran B, Pathak S, Sharma S, Sonawat HM. Host metabolic responses to Plasmodium falciparum infections evaluated by 1H NMR metabolomics. Mol BioSyst. 2016;12(11):3324–32.PubMedCrossRef
35.
go back to reference Kostidis S. Quantitative analysis of central energy metabolism in cell culture samples. In: Giera M, editor. Clinical metabolomics: methods and protocols. New York: Springer; 2018. p. 329–42.CrossRef Kostidis S. Quantitative analysis of central energy metabolism in cell culture samples. In: Giera M, editor. Clinical metabolomics: methods and protocols. New York: Springer; 2018. p. 329–42.CrossRef
36.
go back to reference Kim TT, Parajuli N, Sung MM, Bairwa SC, Levasseur J, Soltys CM, Wishart DS, Madsen K, Schertzer JD, Dyck JRB. Fecal transplant from resveratrol-fed donors improves glycaemia and cardiovascular features of the metabolic syndrome in mice. Am J Physiol Endocrinol Metab. 2018;315(4):E511–9.PubMedCrossRef Kim TT, Parajuli N, Sung MM, Bairwa SC, Levasseur J, Soltys CM, Wishart DS, Madsen K, Schertzer JD, Dyck JRB. Fecal transplant from resveratrol-fed donors improves glycaemia and cardiovascular features of the metabolic syndrome in mice. Am J Physiol Endocrinol Metab. 2018;315(4):E511–9.PubMedCrossRef
38.
go back to reference Kvac M, Havrdova N, Hlaskova L, Dankova T, Kandera J, Jezkova J, Vitovec J, Sak B, Ortega Y, Xiao L, Modry D, Chelladurai JR, Prantlova V, McEvoy J. Cryptosporidium proliferans n. sp. (Apicomplexa: Cryptosporidiidae): molecular and biological evidence of cryptic species within gastric cryptosporidium of mammals. PLoS ONE. 2016;11(1):e0147090.PubMedPubMedCentralCrossRef Kvac M, Havrdova N, Hlaskova L, Dankova T, Kandera J, Jezkova J, Vitovec J, Sak B, Ortega Y, Xiao L, Modry D, Chelladurai JR, Prantlova V, McEvoy J. Cryptosporidium proliferans n. sp. (Apicomplexa: Cryptosporidiidae): molecular and biological evidence of cryptic species within gastric cryptosporidium of mammals. PLoS ONE. 2016;11(1):e0147090.PubMedPubMedCentralCrossRef
39.
go back to reference Novak P, Tepes P, Fistric I, Bratos I, Gabelica V. The application of LC-NMR and LC–MS for the separation and rapid structure elucidation of an unknown impurity in 5-aminosalicylic acid. J Pharm Biomed Anal. 2006;40(5):1268–72.PubMedCrossRef Novak P, Tepes P, Fistric I, Bratos I, Gabelica V. The application of LC-NMR and LC–MS for the separation and rapid structure elucidation of an unknown impurity in 5-aminosalicylic acid. J Pharm Biomed Anal. 2006;40(5):1268–72.PubMedCrossRef
40.
go back to reference Abrahamsen MS, Templeton TJ, Enomoto S, Abrahante JE, Zhu G, Lancto CA, Deng M, Liu C, Widmer G, Tzipori S, Buck GA, Xu P, Bankier AT, Dear PH, Konfortov BA, Spriggs HF, Iyer L, Anantharaman V, Aravind L, Kapur V. Complete genome sequence of the apicomplexan, Cryptosporidium parvum. Science. 2004;304(5669):441–5.PubMedCrossRef Abrahamsen MS, Templeton TJ, Enomoto S, Abrahante JE, Zhu G, Lancto CA, Deng M, Liu C, Widmer G, Tzipori S, Buck GA, Xu P, Bankier AT, Dear PH, Konfortov BA, Spriggs HF, Iyer L, Anantharaman V, Aravind L, Kapur V. Complete genome sequence of the apicomplexan, Cryptosporidium parvum. Science. 2004;304(5669):441–5.PubMedCrossRef
41.
go back to reference Doyle PS, Kanaani J, Wang CC. Hypoxanthine, guanine, xanthine phosphoribosyltransferase activity in Cryptosporidium parvum. Exp Parasitol. 1998;89(1):9–15.PubMedCrossRef Doyle PS, Kanaani J, Wang CC. Hypoxanthine, guanine, xanthine phosphoribosyltransferase activity in Cryptosporidium parvum. Exp Parasitol. 1998;89(1):9–15.PubMedCrossRef
43.
go back to reference Feng H, Nie W, Sheoran A, Zhang Q, Tzipori S. Bile acids enhance invasiveness of Cryptosporidium spp. into cultured cells. Infect Immun. 2006;74(6):3342–6.PubMedPubMedCentralCrossRef Feng H, Nie W, Sheoran A, Zhang Q, Tzipori S. Bile acids enhance invasiveness of Cryptosporidium spp. into cultured cells. Infect Immun. 2006;74(6):3342–6.PubMedPubMedCentralCrossRef
44.
go back to reference Gold D, Stein B, Tzipori S. The utilization of sodium taurocholate in excystation of Cryptosporidium parvum and infection of tissue culture. J Parasitol. 2001;87(5):997–1000.PubMedCrossRef Gold D, Stein B, Tzipori S. The utilization of sodium taurocholate in excystation of Cryptosporidium parvum and infection of tissue culture. J Parasitol. 2001;87(5):997–1000.PubMedCrossRef
45.
go back to reference King BJ, Keegan AR, Phillips R, Fanok S, Monis PT. Dissection of the hierarchy and synergism of the bile derived signal on Cryptosporidium parvum excystation and infectivity. Parasitology. 2012;139(12):1533–46.PubMedCrossRef King BJ, Keegan AR, Phillips R, Fanok S, Monis PT. Dissection of the hierarchy and synergism of the bile derived signal on Cryptosporidium parvum excystation and infectivity. Parasitology. 2012;139(12):1533–46.PubMedCrossRef
46.
go back to reference Kar S, Daugschies A, Cakmak A, Yilmazer N, Dittmar K, Bangoura B. Cryptosporidium parvum oocyst viability and behaviour of the residual body during the excystation process. Parasitol Res. 2011;109(6):1719–23.PubMedCrossRef Kar S, Daugschies A, Cakmak A, Yilmazer N, Dittmar K, Bangoura B. Cryptosporidium parvum oocyst viability and behaviour of the residual body during the excystation process. Parasitol Res. 2011;109(6):1719–23.PubMedCrossRef
47.
go back to reference Goodgame RW, Kimball K, Ou CN, White AC Jr, Genta RM, Lifschitz CH, Chappell CL. Intestinal function and injury in acquired immunodeficiency syndrome-related cryptosporidiosis. Gastroenterology. 1995;108(4):1075–82.PubMedCrossRef Goodgame RW, Kimball K, Ou CN, White AC Jr, Genta RM, Lifschitz CH, Chappell CL. Intestinal function and injury in acquired immunodeficiency syndrome-related cryptosporidiosis. Gastroenterology. 1995;108(4):1075–82.PubMedCrossRef
48.
go back to reference Kapembwa MS, Bridges C, Joseph AE, Fleming SC, Batman P, Griffin GE. Ileal and jejunal absorptive function in patients with AIDS and enterococcidial infection. J Infect. 1990;21(1):43–53.PubMedCrossRef Kapembwa MS, Bridges C, Joseph AE, Fleming SC, Batman P, Griffin GE. Ileal and jejunal absorptive function in patients with AIDS and enterococcidial infection. J Infect. 1990;21(1):43–53.PubMedCrossRef
49.
go back to reference Augagneur Y, Jaubert L, Schiavoni M, Pachikara N, Garg A, Usmani-Brown S, Wesolowski D, Zeller S, Ghosal A, Cornillot E, Said HM, Kumar P, Altman S, Ben Mamoun C. Identification and functional analysis of the primary pantothenate transporter, PfPAT, of the human malaria parasite Plasmodium falciparum. J Biol Chem. 2013;288(28):20558–67.PubMedPubMedCentralCrossRef Augagneur Y, Jaubert L, Schiavoni M, Pachikara N, Garg A, Usmani-Brown S, Wesolowski D, Zeller S, Ghosal A, Cornillot E, Said HM, Kumar P, Altman S, Ben Mamoun C. Identification and functional analysis of the primary pantothenate transporter, PfPAT, of the human malaria parasite Plasmodium falciparum. J Biol Chem. 2013;288(28):20558–67.PubMedPubMedCentralCrossRef
50.
go back to reference Tsaousis AD, Kunji ER, Goldberg AV, Lucocq JM, Hirt RP, Embley TM. A novel route for ATP acquisition by the remnant mitochondria of Encephalitozoon cuniculi. Nature. 2008;453(7194):553–6.PubMedCrossRef Tsaousis AD, Kunji ER, Goldberg AV, Lucocq JM, Hirt RP, Embley TM. A novel route for ATP acquisition by the remnant mitochondria of Encephalitozoon cuniculi. Nature. 2008;453(7194):553–6.PubMedCrossRef
51.
go back to reference Giris M, Depboylu B, Dogru-Abbasoglu S, Erbil Y, Olgac V, Alis H, Aykac-Toker G, Uysal M. Effect of taurine on oxidative stress and apoptosis-related protein expression in trinitrobenzene sulphonic acid-induced colitis. Clin Exp Immunol. 2008;152(1):102–10.PubMedPubMedCentralCrossRef Giris M, Depboylu B, Dogru-Abbasoglu S, Erbil Y, Olgac V, Alis H, Aykac-Toker G, Uysal M. Effect of taurine on oxidative stress and apoptosis-related protein expression in trinitrobenzene sulphonic acid-induced colitis. Clin Exp Immunol. 2008;152(1):102–10.PubMedPubMedCentralCrossRef
52.
go back to reference Green TR, Fellman JH, Eicher AL, Pratt KL. Antioxidant role and subcellular location of hypotaurine and taurine in human neutrophils. Biochim Biophys Acta. 1991;1073(1):91–7.PubMedCrossRef Green TR, Fellman JH, Eicher AL, Pratt KL. Antioxidant role and subcellular location of hypotaurine and taurine in human neutrophils. Biochim Biophys Acta. 1991;1073(1):91–7.PubMedCrossRef
53.
go back to reference Zhang M, Izumi I, Kagamimori S, Sokejima S, Yamagami T, Liu Z, Qi B. Role of taurine supplementation to prevent exercise-induced oxidative stress in healthy young men. Amino Acids. 2004;26(2):203–7.PubMedCrossRef Zhang M, Izumi I, Kagamimori S, Sokejima S, Yamagami T, Liu Z, Qi B. Role of taurine supplementation to prevent exercise-induced oxidative stress in healthy young men. Amino Acids. 2004;26(2):203–7.PubMedCrossRef
54.
go back to reference Lin S, Sanders DS, Gleeson JT, Osborne C, Messham L, Kurien M. Long-term outcomes in patients diagnosed with bile-acid diarrhoea. Eur J Gastroenterol Hepatol. 2016;28(2):240–5.PubMedCrossRef Lin S, Sanders DS, Gleeson JT, Osborne C, Messham L, Kurien M. Long-term outcomes in patients diagnosed with bile-acid diarrhoea. Eur J Gastroenterol Hepatol. 2016;28(2):240–5.PubMedCrossRef
55.
go back to reference Niggli V, Sigel E, Carafoli E. Inhibition of the purified and reconstituted calcium pump of erythrocytes by micro M levels of DIDS and NAP-taurine. FEBS Lett. 1982;138(2):164–6.PubMedCrossRef Niggli V, Sigel E, Carafoli E. Inhibition of the purified and reconstituted calcium pump of erythrocytes by micro M levels of DIDS and NAP-taurine. FEBS Lett. 1982;138(2):164–6.PubMedCrossRef
56.
go back to reference Yu H, Guo Z, Shen S, Shan W. Effects of taurine on gut microbiota and metabolism in mice. Amino Acids. 2016;48(7):1601–17.PubMedCrossRef Yu H, Guo Z, Shen S, Shan W. Effects of taurine on gut microbiota and metabolism in mice. Amino Acids. 2016;48(7):1601–17.PubMedCrossRef
57.
go back to reference Guo F, Zhang H, Payne HR, Zhu G. Differential gene expression and protein localization of Cryptosporidium parvum fatty acyl-CoA synthetase isoforms. J Eukaryot Microbiol. 2016;63(2):233–46.PubMedCrossRef Guo F, Zhang H, Payne HR, Zhu G. Differential gene expression and protein localization of Cryptosporidium parvum fatty acyl-CoA synthetase isoforms. J Eukaryot Microbiol. 2016;63(2):233–46.PubMedCrossRef
58.
go back to reference Seeber F, Soldati-Favre D. Metabolic pathways in the apicoplast of apicomplexa. Int Rev Cell Mol Biol. 2010;281:161–228.PubMedCrossRef Seeber F, Soldati-Favre D. Metabolic pathways in the apicoplast of apicomplexa. Int Rev Cell Mol Biol. 2010;281:161–228.PubMedCrossRef
59.
go back to reference Meloni BP, Andrew Thompson RC. Simplified methods for obtaining purified oocysts from mice and for growing Cryptosporidium parvum in vitro. J Parasitol. 1996;82(5):757–62.PubMedCrossRef Meloni BP, Andrew Thompson RC. Simplified methods for obtaining purified oocysts from mice and for growing Cryptosporidium parvum in vitro. J Parasitol. 1996;82(5):757–62.PubMedCrossRef
60.
go back to reference Milacek P, Vitovec J. Differential staining of Cryptosporidia by aniline-carbol-methyl violet and tartrazine in smears from faeces and scrapings of intestinal mucosa. 1985;32(1):50. Milacek P, Vitovec J. Differential staining of Cryptosporidia by aniline-carbol-methyl violet and tartrazine in smears from faeces and scrapings of intestinal mucosa. 1985;32(1):50.
61.
go back to reference Morgan-Ryan UM, Fall A, Ward LA, Hijjawi N, Sulaiman I, Fayer R, Thompson RC, Olson M, Lal A, Xiao L. Cryptosporidium hominis n. sp. (Apicomplexa: Cryptosporidiidae) from Homo sapiens. J Eukaryot Microbiol. 2002;49(6):433–40.PubMedCrossRef Morgan-Ryan UM, Fall A, Ward LA, Hijjawi N, Sulaiman I, Fayer R, Thompson RC, Olson M, Lal A, Xiao L. Cryptosporidium hominis n. sp. (Apicomplexa: Cryptosporidiidae) from Homo sapiens. J Eukaryot Microbiol. 2002;49(6):433–40.PubMedCrossRef
62.
go back to reference Bastow EL, Peswani AR, Tarrant DSJ, Pentland DR, Chen X, Morgan A, Staniforth GL, Tullet JM, Rowe ML, Howard MJ, Tuite MF, Gourlay CW. New links between SOD1 and metabolic dysfunction from a yeast model of amyotrophic lateral sclerosis. J Cell Sci. 2016;129(21):4118.PubMedPubMedCentral Bastow EL, Peswani AR, Tarrant DSJ, Pentland DR, Chen X, Morgan A, Staniforth GL, Tullet JM, Rowe ML, Howard MJ, Tuite MF, Gourlay CW. New links between SOD1 and metabolic dysfunction from a yeast model of amyotrophic lateral sclerosis. J Cell Sci. 2016;129(21):4118.PubMedPubMedCentral
63.
go back to reference Holyoake LV, Hunt S, Sanguinetti G, Cook GM, Howard MJ, Rowe ML, Poole RK, Shepherd M. CydDC-mediated reductant export in Escherichia coli controls the transcriptional wiring of energy metabolism and combats nitrosative stress. Biochem J. 2016;473(6):693–701.PubMedCrossRef Holyoake LV, Hunt S, Sanguinetti G, Cook GM, Howard MJ, Rowe ML, Poole RK, Shepherd M. CydDC-mediated reductant export in Escherichia coli controls the transcriptional wiring of energy metabolism and combats nitrosative stress. Biochem J. 2016;473(6):693–701.PubMedCrossRef
64.
go back to reference Tarrant DJ, Stirpe M, Rowe M, Howard MJ, von der Haar T, Gourlay CW. Inappropriate expression of the translation elongation factor 1A disrupts genome stability and metabolism. J Cell Sci. 2016;129(24):4455–65.PubMedPubMedCentralCrossRef Tarrant DJ, Stirpe M, Rowe M, Howard MJ, von der Haar T, Gourlay CW. Inappropriate expression of the translation elongation factor 1A disrupts genome stability and metabolism. J Cell Sci. 2016;129(24):4455–65.PubMedPubMedCentralCrossRef
65.
go back to reference Wagstaff JL, Masterton RJ, Povey JF, Smales CM, Howard MJ. (1)H NMR spectroscopy profiling of metabolic reprogramming of Chinese hamster ovary cells upon a temperature shift during culture. PLoS ONE. 2013;8(10):e77195.PubMedPubMedCentralCrossRef Wagstaff JL, Masterton RJ, Povey JF, Smales CM, Howard MJ. (1)H NMR spectroscopy profiling of metabolic reprogramming of Chinese hamster ovary cells upon a temperature shift during culture. PLoS ONE. 2013;8(10):e77195.PubMedPubMedCentralCrossRef
Metadata
Title
NMR metabolomics reveals effects of Cryptosporidium infections on host cell metabolome
Authors
Christopher N. Miller
Charalampos G. Panagos
William R. T. Mosedale
Martin Kváč
Mark J. Howard
Anastasios D. Tsaousis
Publication date
01-12-2019
Publisher
BioMed Central
Published in
Gut Pathogens / Issue 1/2019
Electronic ISSN: 1757-4749
DOI
https://doi.org/10.1186/s13099-019-0293-x

Other articles of this Issue 1/2019

Gut Pathogens 1/2019 Go to the issue
Live Webinar | 27-06-2024 | 18:00 (CEST)

Keynote webinar | Spotlight on medication adherence

Live: Thursday 27th June 2024, 18:00-19:30 (CEST)

WHO estimates that half of all patients worldwide are non-adherent to their prescribed medication. The consequences of poor adherence can be catastrophic, on both the individual and population level.

Join our expert panel to discover why you need to understand the drivers of non-adherence in your patients, and how you can optimize medication adherence in your clinics to drastically improve patient outcomes.

Prof. Kevin Dolgin
Prof. Florian Limbourg
Prof. Anoop Chauhan
Developed by: Springer Medicine
Obesity Clinical Trial Summary

At a glance: The STEP trials

A round-up of the STEP phase 3 clinical trials evaluating semaglutide for weight loss in people with overweight or obesity.

Developed by: Springer Medicine

Highlights from the ACC 2024 Congress

Year in Review: Pediatric cardiology

Watch Dr. Anne Marie Valente present the last year's highlights in pediatric and congenital heart disease in the official ACC.24 Year in Review session.

Year in Review: Pulmonary vascular disease

The last year's highlights in pulmonary vascular disease are presented by Dr. Jane Leopold in this official video from ACC.24.

Year in Review: Valvular heart disease

Watch Prof. William Zoghbi present the last year's highlights in valvular heart disease from the official ACC.24 Year in Review session.

Year in Review: Heart failure and cardiomyopathies

Watch this official video from ACC.24. Dr. Biykem Bozkurt discusses last year's major advances in heart failure and cardiomyopathies.