Parasite-Derived MicroRNAs in Host Serum As Novel Biomarkers of Helminth Infection

PLoS Neglected Tropical Diseases

Volumn 8, Issue 2, 2014, Pages

  Hoy, Anna M ^a   Lundie, Rachel J ^b   Ivens, Alasdair ^a   Quintana, Juan F ^a   Nausch, Norman ^a   Forster, Thorsten ^a   Jones, Frances ^c   Kabatereine, Narcis B ^d   Dunne, David W ^c   Mutapi, Francisca ^a   MacDonald, Andrew S ^a,e   Buck, Amy H ^a  

^a UNIVERSITY OF EDINBURGH   (United Kingdom)

^b WALTER AND ELIZA HALL INSTITUTE OF MEDICAL RESEARCH   (Australia)

^c UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^d MINISTRY OF HEALTH   (Uganda)

^e UNIVERSITY OF MANCHESTER   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

BIOLOGICAL MARKER; MICRORNA; SMALL INTERFERING RNA;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BLOOD SAMPLING; CONTROLLED STUDY; HELMINTHIASIS; HOST PARASITE INTERACTION; HUMAN; ILLUMINA SEQUENCING; MICROARRAY ANALYSIS; MOUSE; NONHUMAN; PATHOLOGY; PREVALENCE; PROTEIN EXPRESSION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; RNA EXTRACTION; RNA SEQUENCE; SCHISTOSOMA MANSONI; SEQUENCE ANALYSIS;

ADOLESCENT; ADULT; ANIMALS; BIOLOGICAL MARKERS; CHILD; CHILD, PRESCHOOL; FEMALE; HUMANS; LIVER; MALE; MICE; MICE, INBRED C57BL; MICRORNAS; MIDDLE AGED; RNA, HELMINTH; SCHISTOSOMA MANSONI; SCHISTOSOMIASIS MANSONI; YOUNG ADULT;

EID: 84895730045     PISSN: 19352727     EISSN: 19352735     Source Type: Journal    
DOI: 10.1371/journal.pntd.0002701     Document Type: Article

References (80)

1. Hotez PJ, Brindley PJ, Bethony JM, King CH, Pearce EJ, et al. (2008) Helminth infections: the great neglected tropical diseases. The Journal of clinical investigation 118: 1311-1321.
2. Awasthi S, Bundy DA, Savioli L, (2003) Helminthic infections. BMJ 327: 431-433.
3. Organisation WH (2013) Schistosomiasis-Fact sheet 115. WHO.
4. van der Werf MJ, de Vlas SJ, Brooker S, Looman CW, Nagelkerke NJ, et al. (2003) Quantification of clinical morbidity associated with schistosome infection in sub-Saharan Africa. Acta tropica 86: 125-139.
5. King CH, Dickman K, Tisch DJ, (2005) Reassessment of the cost of chronic helmintic infection: a meta-analysis of disability-related outcomes in endemic schistosomiasis. Lancet 365: 1561-1569.
6. Organization WH (2002) Prevention and Control of Schistosomiasia and Soil Transmitted helminthiasia- Report of a WHO Expert Committee. Geneva.
7. Glinz D, Silue KD, Knopp S, Lohourignon LK, Yao KP, et al. (2010) Comparing diagnostic accuracy of Kato-Katz, Koga agar plate, ether-concentration, and FLOTAC for Schistosoma mansoni and soil-transmitted helminths. PLoS neglected tropical diseases 4: e754.
8. Stothard JR, Sousa-Figueiredo JC, Betson M, Adriko M, Arinaitwe M, et al. (2011) Schistosoma mansoni Infections in young children: when are schistosome antigens in urine, eggs in stool and antibodies to eggs first detectable? PLoS neglected tropical diseases 5: e938.
9. Doenhoff MJ, Chiodini PL, Hamilton JV, (2004) Specific and sensitive diagnosis of schistosome infection: can it be done with antibodies? Trends in Parasitology 20: 35-39.
10. Shane HL, Verani JR, Abudho B, Montgomery SP, Blackstock AJ, et al. (2011) Evaluation of urine CCA assays for detection of Schistosoma mansoni infection in Western Kenya. PLoS neglected tropical diseases 5: e951.
11. van Lieshout L, De Jonge N, Mansour MM, Bassily S, Krijger FW, et al. (1993) Circulating cathodic antigen levels in serum and urine of schistosomiasis patients before and after chemotherapy with praziquantel. Transactions of the Royal Society of Tropical Medicine and Hygiene 87: 311-312.
12. van Dam GJ, Bogitsh BJ, van Zeyl RJ, Rotmans JP, Deelder AM, (1996) Schistosoma mansoni: in vitro and in vivo excretion of CAA and CCA by developing schistosomula and adult worms. The Journal of parasitology 82: 557-564.
13. Coulibaly JT, N'Gbesso YK, Knopp S, N'Guessan NA, Silue KD, et al. (2013) Accuracy of urine circulating cathodic antigen test for the diagnosis of Schistosoma mansoni in preschool-aged children before and after treatment. PLoS neglected tropical diseases 7: e2109.
14. Sousa-Figueiredo JC, Betson M, Kabatereine NB, Stothard JR, (2013) The urine circulating cathodic antigen (CCA) dipstick: a valid substitute for microscopy for mapping and point-of-care diagnosis of intestinal schistosomiasis. PLoS neglected tropical diseases 7: e2008.
15. van Dam GJ, de Dood CJ, Lewis M, Deelder AM, van Lieshout L, et al. (2013) A robust dry reagent lateral flow assay for diagnosis of active schistosomiasis by detection of Schistosoma circulating anodic antigen. Exp Parasitol 135: 274-282.
16. Enk MJ, Oliveira e Silva G, Rodrigues NB, (2012) Diagnostic accuracy and applicability of a PCR system for the detection of Schistosoma mansoni DNA in human urine samples from an endemic area. PloS one 7: e38947.
17. Pontes LA, Oliveira MC, Katz N, Dias-Neto E, Rabello A, (2003) Comparison of a polymerase chain reaction and the Kato-Katz technique for diagnosing infection with Schistosoma mansoni. The American journal of tropical medicine and hygiene 68: 652-656.
18. Wichmann D, Panning M, Quack T, Kramme S, Burchard GD, et al. (2009) Diagnosing schistosomiasis by detection of cell-free parasite DNA in human plasma. PLoS neglected tropical diseases 3: e422.
19. Lodh N, Mwansa JC, Mutengo MM, Shiff CJ, (2013) Diagnosis of Schistosoma mansoni without the Stool: Detecting DNA from Filtered Urine Comparison of Three Diagnostic Tests to Detect Schistosoma mansoni Infection from Filtered Urine in Zambia. Am J Trop Med Hyg 89: 46-50.
20. Ibironke OA, Phillips AE, Garba A, Lamine SM, Shiff C, (2011) Diagnosis of Schistosoma haematobium by detection of specific DNA fragments from filtered urine samples. The American journal of tropical medicine and hygiene 84: 998-1001.
21. Bartel DP, (2009) MicroRNAs: target recognition and regulatory functions. Cell 136: 215-233.
22. Fabian MR, Sonenberg N, (2012) The mechanics of miRNA-mediated gene silencing: a look under the hood of miRISC. Nature structural & molecular biology 19: 586-593.
23. Sullivan CS, Ganem D, (2005) MicroRNAs and viral infection. Molecular cell 20: 3-7.
24. Xiao C, Rajewsky K, (2009) MicroRNA control in the immune system: basic principles. Cell 136: 26-36.
25. Mendell JT, Olson EN, (2012) MicroRNAs in stress signaling and human disease. Cell 148: 1172-1187.
26. Valadi H, Ekstrom K, Bossios A, Sjostrand M, Lee JJ, et al. (2007) Exosome-mediated transfer of mRNAs and microRNAs is a novel mechanism of genetic exchange between cells. Nature cell biology 9: 654-659.
27. Mitchell PS, Parkin RK, Kroh EM, Fritz BR, Wyman SK, et al. (2008) Circulating microRNAs as stable blood-based markers for cancer detection. Proceedings of the National Academy of Sciences of the United States of America 105: 10513-10518.
28. Xu L, Yang BF, Ai J, (2013) MicroRNA transport: a new way in cell communication. Journal of cellular physiology 228: 1713-1719.
29. Creemers EE, Tijsen AJ, Pinto YM, (2012) Circulating microRNAs: novel biomarkers and extracellular communicators in cardiovascular disease? Circulation research 110: 483-495.
30. Chen X, Ba Y, Ma L, Cai X, Yin Y, et al. (2008) Characterization of microRNAs in serum: a novel class of biomarkers for diagnosis of cancer and other diseases. Cell research 18: 997-1006.
31. Etheridge A, Lee I, Hood L, Galas D, Wang K, (2011) Extracellular microRNA: A new source of biomarkers. Mutation Research-Fundamental and Molecular Mechanisms of Mutagenesis 717: 85-90.
32. Kosaka N, Iguchi H, Ochiya T, (2010) Circulating microRNA in body fluid: a new potential biomarker for cancer diagnosis and prognosis. Cancer Science 101: 2087-2092.
33. Weiland M, Gao XH, Zhou L, Mi QS, (2012) Small RNAs have a large impact Circulating microRNAs as biomarkers for human diseases. Rna Biology 9: 850-859.
34. Shrivastava S, Petrone J, Steele R, Lauer GM, Bisceglie AM, et al. (2013) Upregulation of circulating miR-20a is correlated with hepatitis C virus mediated liver disease progression. Hepatology 58: 863-71.
35. Li LM, Hu ZB, Zhou ZX, Chen X, Liu FY, et al. (2010) Serum microRNA profiles serve as novel biomarkers for HBV infection and diagnosis of HBV-positive hepatocarcinoma. Cancer research 70: 9798-9807.
36. Qi Y, Cui L, Ge Y, Shi Z, Zhao K, et al. (2012) Altered serum microRNAs as biomarkers for the early diagnosis of pulmonary tuberculosis infection. BMC infectious diseases 12: 384.
37. Zhang L, Hou D, Chen X, Li D, Zhu L, et al. (2012) Exogenous plant MIR168a specifically targets mammalian LDLRAP1: evidence of cross-kingdom regulation by microRNA. Cell research 22: 107-126.
38. Kabatereine NB, Vennervald BJ, Ouma JH, Kemijumbi J, Butterworth AE, et al. (1999) Adult resistance to schistosomiasis mansoni: age-dependence of reinfection remains constant in communities with diverse exposure patterns. Parasitology 118 (Pt 1) (): 101-105.
39. Mott KE, (1983) A reusable polyamide filter for diagnosis of S. haematobium infection by urine filtration. Bulletin de la Societe de pathologie exotique et de ses filiales 76: 101-104.
40. Katz N, Chaves A, Pellegrino J, (1972) A simple device for quantitative stool thick-smear technique in Schistosomiasis mansoni. Revista do Instituto de Medicina Tropical de Sao Paulo 14: 397-400.
41. Buck AH, Santoyo-Lopez J, Robertson KA, Kumar DS, Reczko M, et al. (2007) Discrete clusters of virus-encoded micrornas are associated with complementary strands of the genome and the 7.2-kilobase stable intron in murine cytomegalovirus. J Virol 81: 13761-13770.
42. Ruckerl D, Jenkins SJ, Laqtom NN, Gallagher IJ, Sutherland TE, et al. (2012) Induction of IL-4Ralpha-dependent microRNAs identifies PI3K/Akt signaling as essential for IL-4-driven murine macrophage proliferation in vivo. Blood 120: 2307-2316.
43. Livak KJ, Schmittgen TD, (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2(T)(-Delta Delta C) method. Methods 25: 402-408.
44. Mendell JT, Olson EN, (2012) MicroRNAs in Stress Signaling and Human Disease. Cell 148: 1172-1187.
45. Pearce EJ, MacDonald AS, (2002) The immunobiology of schistosomiasis. Nature reviews Immunology 2: 499-511.
46. Wynn TA, Thompson RW, Cheever AW, Mentink-Kane MM, (2004) Immunopathogenesis of schistosomiasis. Immunological reviews 201: 156-167.
47. Iizuka M, Ogawa T, Enomoto M, Motoyama H, Yoshizato K, et al. (2012) Induction of microRNA-214-5p in human and rodent liver fibrosis. Fibrogenesis & tissue repair 5: 12.
48. Murakami Y, Toyoda H, Tanaka M, Kuroda M, Harada Y, et al. (2011) The progression of liver fibrosis is related with overexpression of the miR-199 and 200 families. PloS one 6: e16081.
49. Girard M, Jacquemin E, Munnich A, Lyonnet S, Henrion-Caude A, (2008) miR-122, a paradigm for the role of microRNAs in the liver. Journal of hepatology 48: 648-656.
50. Hu J, Xu Y, Hao J, Wang S, Li C, et al. (2012) MiR-122 in hepatic function and liver diseases. Protein & cell 3: 364-371.
51. Moore DV, Sandground JH, (1956) The relative egg producing capacity of Schistosoma mansoni and Schistosoma japonicum. The American journal of tropical medicine and hygiene 5: 831-840.
52. Waidmann O, Koberle V, Brunner F, Zeuzem S, Piiper A, et al. (2012) Serum microRNA-122 predicts survival in patients with liver cirrhosis. PloS one 7: e45652.
53. Farid WR, Pan Q, van der Meer AJ, de Ruiter PE, Ramakrishnaiah V, et al. (2012) Hepatocyte-derived microRNAs as serum biomarkers of hepatic injury and rejection after liver transplantation. Liver transplantation: official publication of the American Association for the Study of Liver Diseases and the International Liver Transplantation Society 18: 290-297.
54. Starkey Lewis PJ, Merz M, Couttet P, Grenet O, Dear J, et al. (2012) Serum microRNA biomarkers for drug-induced liver injury. Clinical pharmacology and therapeutics 92: 291-293.
55. Wang LG, Gu J, (2012) Serum microRNA-29a is a promising novel marker for early detection of colorectal liver metastasis. Cancer epidemiology 36: e61-67.
56. Zhang Y, Jia Y, Zheng R, Guo Y, Wang Y, et al. (2010) Plasma microRNA-122 as a biomarker for viral-, alcohol-, and chemical-related hepatic diseases. Clinical chemistry 56: 1830-1838.
57. Weiland M, Gao XH, Zhou L, Mi QS, (2012) Small RNAs have a large impact: circulating microRNAs as biomarkers for human diseases. RNA biology 9: 850-859.
58. Scholer N, Langer C, Dohner H, Buske C, Kuchenbauer F, (2010) Serum microRNAs as a novel class of biomarkers: a comprehensive review of the literature. Experimental hematology 38: 1126-1130.
59. Hoy AM, Buck AH, (2012) Extracellular small RNAs: what, where, why? Biochemical Society transactions 40: 886-890.
60. Benz F, Roderburg C, Vargas Cardenas D, Vucur M, Gautheron J, et al. (2013) U6 is unsuitable for normalization of serum miRNA levels in patients with sepsis or liver fibrosis. Experimental & molecular medicine 45: e42.
61. Turchinovich A, Weiz L, Burwinkel B, (2012) Extracellular miRNAs: the mystery of their origin and function. Trends in biochemical sciences 37: 460-465.
62. de Souza Gomes M, Muniyappa MK, Carvalho SG, Guerra-Sa R, Spillane C, (2011) Genome-wide identification of novel microRNAs and their target genes in the human parasite Schistosoma mansoni. Genomics 98: 96-111.
63. Kozomara A, Griffiths-Jones S, (2011) miRBase: integrating microRNA annotation and deep-sequencing data. Nucleic acids research 39: D152-157.
64. Wang Z, Xue X, Sun J, Luo R, Xu X, et al. (2010) An "in-depth" description of the small non-coding RNA population of Schistosoma japonicum schistosomulum. PLoS neglected tropical diseases 4: e596.
65. Xue X, Sun J, Zhang Q, Wang Z, Huang Y, et al. (2008) Identification and characterization of novel microRNAs from Schistosoma japonicum. PloS one 3: e4034.
66. Friedlander MR, Mackowiak SD, Li N, Chen W, Rajewsky N, (2012) miRDeep2 accurately identifies known and hundreds of novel microRNA genes in seven animal clades. Nucleic acids research 40: 37-52.
67. Marco A, Kozomara A, Hui JH, Emery AM, Rollinson D, et al. (2013) Sex-biased expression of microRNAs in Schistosoma mansoni. PLoS neglected tropical diseases 7: e2402.
68. Goren Y, Kushnir M, Zafrir B, Tabak S, Lewis BS, et al. (2012) Serum levels of microRNAs in patients with heart failure. European journal of heart failure 14: 147-154.
69. Li Y, Jiang Z, Xu L, Yao H, Guo J, et al. (2011) Stability analysis of liver cancer-related microRNAs. Acta biochimica et biophysica Sinica 43: 69-78.
70. Cheng G, Luo R, Hu C, Cao J, Jin Y, (2013) Deep sequencing-based identification of pathogen-specific microRNAs in the plasma of rabbits infected with Schistosoma japonicum. Parasitology 140: 1751-1761.
71. Wang K, Li H, Yuan Y, Etheridge A, Zhou Y, et al. (2012) The complex exogenous RNA spectra in human plasma: an interface with human gut biota? PloS one 7: e51009.
72. Blank A, Dekker CA, (1981) Ribonucleases of human serum, urine, cerebrospinal fluid, and leukocytes. Activity staining following electrophoresis in sodium dodecyl sulfate-polyacrylamide gels. Biochemistry 20: 2261-2267.
73. Kamm RC, Smith AG, (1972) Ribonuclease activity in human plasma. Clinical biochemistry 5: 198-200.
74. Brennecke J, Hipfner DR, Stark A, Russell RB, Cohen SM, (2003) bantam encodes a developmentally regulated microRNA that controls cell proliferation and regulates the proapoptotic gene hid in Drosophila. Cell 113: 25-36.
75. Schaedel ON, Gerisch B, Antebi A, Sternberg PW, (2012) Hormonal signal amplification mediates environmental conditions during development and controls an irreversible commitment to adulthood. PLoS biology 10: e1001306.
76. Crosby A, Jones FM, Kolosionek E, Southwood M, Purvis I, et al. (2011) Praziquantel reverses pulmonary hypertension and vascular remodeling in murine schistosomiasis. Am J Respir Crit Care Med 184: 467-473.
77. Chen XM, (2009) MicroRNA signatures in liver diseases. World journal of gastroenterology: WJG 15: 1665-1672.
78. Jiang X, Tsitsiou E, Herrick SE, Lindsay MA, (2010) MicroRNAs and the regulation of fibrosis. The FEBS journal 277: 2015-2021.
79. Kang K, Peng X, Luo J, Gou D, (2012) Identification of circulating miRNA biomarkers based on global quantitative real-time PCR profiling. Journal of animal science and biotechnology 3: 4.
80. Dhahbi JM, Spindler SR, Atamna H, Yamakawa A, Boffelli D, et al. (2013) 5′ tRNA halves are present as abundant complexes in serum, concentrated in blood cells, and modulated by aging and calorie restriction. BMC genomics 14: 298.