1887

Abstract

Immuno-PCR (PCR-amplified immunoassay; I-PCR) is a novel ultrasensitive method combining the versatility of ELISA with the sensitivity of nucleic acid amplification of PCR. The enormous exponential amplification power of PCR in an I-PCR assay leads to at least a 10–10-fold increase in sensitivity compared with an analogous ELISA. I-PCR has been used to detect many biological molecules such as proto-oncogenes, toxins, cytokines, hormones, and biomarkers for autoimmune and Alzheimer’s diseases, as well as microbial antigens and antibodies, and it can be adapted as a novel diagnostic tool for various infectious and non-infectious diseases. Quantitative real-time I-PCR has the potential to become the most analytically sensitive method for the detection of proteins. The sensitivity and specificity of a real-time I-PCR assay can be enhanced further with the use of magnetic beads and nanoparticles. This review is primarily focused on the detection of potential viral, bacterial and parasitic antigens by I-PCR assay, thus enabling their application for immunological research and for early diagnosis of infectious diseases.

Loading

Article metrics loading...

/content/journal/jmm/10.1099/jmm.0.070318-0
2014-05-01
2024-12-14
Loading full text...

Full text loading...

/deliver/fulltext/jmm/63/5/627.html?itemId=/content/journal/jmm/10.1099/jmm.0.070318-0&mimeType=html&fmt=ahah

References

  1. Adams N. M., Jackson S. R., Haselton F. R., Wright D. W. 2012; Design, synthesis, and characterization of nucleic-acid-functionalized gold surfaces for biomarker detection. Langmuir 28:1068–1082 [View Article][PubMed]
    [Google Scholar]
  2. Adler M., Schulz S., Fischer R., Niemeyer C. M. 2005; Detection of Rotavirus from stool samples using a standardized immuno-PCR (“Imperacer”) method with end-point and real-time detection. Biochem Biophys Res Commun 333:1289–1294 [View Article][PubMed]
    [Google Scholar]
  3. Adler M., Wacker R., Niemeyer C. M. 2008; Sensitivity by combination: immuno-PCR and related technologies. Analyst (Lond) 133:702–718 [View Article][PubMed]
    [Google Scholar]
  4. Allen R. C., Rogelj S., Cordova S. E., Kieft T. L. 2006; An immuno-PCR method for detecting Bacillus thuringiensis Cry1Ac toxin. J Immunol Methods 308:109–115 [View Article][PubMed]
    [Google Scholar]
  5. Babu D., Muriana P. M. 2011; Immunomagnetic bead-based recovery and real time quantitative PCR (RT iq-PCR) for sensitive quantification of aflatoxin B1 . J Microbiol Methods 86:188–194 [View Article][PubMed]
    [Google Scholar]
  6. Baheti N. N., Sreedharan M., Krishnamoorthy T., Nair M. D., Radhakrishnan K. 2008; Eosinophilic meningitis and an ocular worm in a patient from Kerala, south India. J Neurol Neurosurg Psychiatry 79:271 [View Article][PubMed]
    [Google Scholar]
  7. Barletta J. M., Edelman D. C., Constantine N. T. 2004; Lowering the detection limits of HIV-1 viral load using real-time immuno-PCR for HIV-1 p24 antigen. Am J Clin Pathol 122:20–27 [View Article][PubMed]
    [Google Scholar]
  8. Barletta J. M., Edelman D. C., Highsmith W. E., Constantine N. T. 2005; Detection of ultra-low levels of pathologic prion protein in scrapie infected hamster brain homogenates using real-time immuno-PCR. J Virol Methods 127:154–164 [View Article][PubMed]
    [Google Scholar]
  9. Barletta J., Bartolome A., Constantine N. T. 2009; Immunomagnetic quantitative immuno-PCR for detection of less than one HIV-1 virion. J Virol Methods 157:122–132 [View Article][PubMed]
    [Google Scholar]
  10. Cao Y., Kopplow K., Liu G. Y. 2000; In-situ immuno-PCR to detect antigens. Lancet 356:1002–1003 [View Article][PubMed]
    [Google Scholar]
  11. Chang T. C., Huang S. H. 1997; A modified immuno-polymerase chain reaction for the detection of β-glucuronidase from Escherichia coli . J Immunol Methods 208:35–42 [View Article][PubMed]
    [Google Scholar]
  12. Chao H. Y., Wang Y. C., Tang S. S., Liu H. W. 2004; A highly sensitive immuno-polymerase chain reaction assay for Clostridium botulinum neurotoxin type A. Toxicon 43:27–34 [View Article][PubMed]
    [Google Scholar]
  13. Chen L., Wei H., Guo Y., Cui Z., Zhang Z., Zhang X. E. 2009; Gold nanoparticle enhanced immuno-PCR for ultrasensitive detection of Hantaan virus nucleocapsid protein. J Immunol Methods 346:64–70 [View Article][PubMed]
    [Google Scholar]
  14. Chye S. M., Yen C. M., Chen E. R. 1997; Detection of circulating antigen by monoclonal antibodies for immunodiagnosis of angiostrongyliasis. Am J Trop Med Hyg 56:408–412[PubMed]
    [Google Scholar]
  15. Chye S. M., Lin S. R., Chen Y. L., Chung L. Y., Yen C. M. 2004; Immuno-PCR for detection of antigen to Angiostrongylus cantonensis circulating fifth-stage worms. Clin Chem 50:51–57 [View Article][PubMed]
    [Google Scholar]
  16. Deng M. J., Xiao X. Z., Zhang Y. M., Wu X. H., Zhu L. H., Xin X. Q., Wu D. L. 2011a; A highly sensitive immuno-PCR assay for detection of H5N1 avian influenza virus. Mol Biol Rep 38:1941–1948 [View Article][PubMed]
    [Google Scholar]
  17. Deng M., Long L., Xiao X., Wu Z., Zhang F., Zhang Y., Zheng X., Xin X., Wang Q., Wu D. 2011b; Immuno-PCR for one step detection of H5N1 avian influenza virus and Newcastle disease virus using magnetic gold particles as carriers. Vet Immunol Immunopathol 141:183–189 [View Article][PubMed]
    [Google Scholar]
  18. Ding Y. Z., Liu Y. S., Zhou J. H., Chen H. T., Zhang J., Ma L. N., Wei G. 2011; A highly sensitive detection for foot-and-mouth disease virus by gold nanopariticle improved immuno-PCR. Virol J 8:148 [View Article][PubMed]
    [Google Scholar]
  19. Fischer A., von Eiff C., Kuczius T., Omoe K., Peters G., Becker K. 2007; A quantitative real-time immuno-PCR approach for detection of staphylococcal enterotoxins. J Mol Med (Berl) 85:461–469 [View Article][PubMed]
    [Google Scholar]
  20. Glass R. I., Bresee J., Jiang B., Gentsch J., Ando T., Fankhauser R., Noel J., Parashar U., Rosen B., Monroe S. S. 2001; Gastroenteritis viruses: an overview. Novartis Found Symp 238:5–19 discussion 19–25 [View Article][PubMed]
    [Google Scholar]
  21. Gofflot S., El Moualij B., Zorzi D., Melen L., Roels S., Quatpers D., Grassi J., Vanopdenbosch E., Heinen E., Zorzi W. 2004; Immuno-quantitative polymerase chain reaction for detection and quantitation of prion protein. J Immunoassay Immunochem 25:241–258 [View Article][PubMed]
    [Google Scholar]
  22. Gofflot S., Deprez M., El Moualij B., Osman A., Thonnart J. F., Hougrand O., Heinen E., Zorzi W. 2005; Immunoquantitative PCR for prion protein detection in sporadic Creutzfeldt–Jakob disease. Clin Chem 51:1605–1611 [View Article][PubMed]
    [Google Scholar]
  23. Griffiths G., Nyström B., Sable S. B., Khuller G. K. 2010; Nanobead-based interventions for the treatment and prevention of tuberculosis. Nat Rev Microbiol 8:827–834 [View Article][PubMed]
    [Google Scholar]
  24. Guo Y. C., Zhou Y. F., Zhang X. E., Zhang Z. P., Qiao Y. M., Bi L. J., Wen J. K., Liang M. F., Zhang J. B. 2006; Phage display mediated immuno-PCR. Nucleic Acids Res 34:e62 [View Article][PubMed]
    [Google Scholar]
  25. Halpern M. D., Jain S., Jewett M. W. 2013; Enhanced detection of host response antibodies to Borrelia burgdorferi using immuno-PCR. Clin Vaccine Immunol 20:350–357 [View Article][PubMed]
    [Google Scholar]
  26. Hashimoto M., Aoki M., Winblad B., Tjernberg L. O. 2012; A novel approach for Aβ1–40 quantification using immuno-PCR. J Neurosci Methods 205:364–367 [View Article][PubMed]
    [Google Scholar]
  27. He X., McMahon S., Henderson T. D. II, Griffey S. M., Cheng L. W. 2010; Ricin toxicokinetics and its sensitive detection in mouse sera or feces using immuno-PCR. PLoS ONE 5:e12858 [View Article][PubMed]
    [Google Scholar]
  28. He X., Qi W., Quiñones B., McMahon S., Cooley M., Mandrell R. E. 2011; Sensitive detection of Shiga toxin 2 and some of its variants in environmental samples by a novel immuno-PCR assay. Appl Environ Microbiol 77:3558–3564 [View Article][PubMed]
    [Google Scholar]
  29. He J., Evers D. L., O’Leary T. J., Mason J. T. 2012; Immunoliposome-PCR: a generic ultrasensitive quantitative antigen detection system. J Nanobiotechnology 10:26 [View Article][PubMed]
    [Google Scholar]
  30. He X., McMahon S., Skinner C., Merrill P., Scotcher M. C., Stanker L. H. 2013; Development and characterization of monoclonal antibodies against Shiga toxin 2 and their application for toxin detection in milk. J Immunol Methods 389:18–28 [View Article][PubMed]
    [Google Scholar]
  31. Huang S. H., Chang T. C. 2004; Detection of Staphylococcus aureus by a sensitive immuno-PCR assay. Clin Chem 50:1673–1674 [View Article][PubMed]
    [Google Scholar]
  32. Kakizaki E., Yoshida T., Kawakami H., Oseto M., Sakai T., Sakai M. 1996; Detection of bacterial antigens using immuno-PCR. Lett Appl Microbiol 23:101–103 [View Article][PubMed]
    [Google Scholar]
  33. Kuczius T., Becker K., Fischer A., Zhang W. 2012; Simultaneous detection of three CNS indicator proteins in complex suspensions using a single immuno-PCR protocol. Anal Biochem 431:4–10 [View Article][PubMed]
    [Google Scholar]
  34. Liang H., Cordova S. E., Kieft T. L., Rogelj S. 2003; A highly sensitive immuno-PCR assay for detecting Group A Streptococcus . J Immunol Methods 279:101–110 [View Article][PubMed]
    [Google Scholar]
  35. Maia M., Takahashi H., Adler K., Garlick R. K., Wands J. R. 1995; Development of a two-site immuno-PCR assay for hepatitis B surface antigen. J Virol Methods 52:273–286 [View Article][PubMed]
    [Google Scholar]
  36. Malou N., Raoult D. 2011; Immuno-PCR: a promising ultrasensitive diagnostic method to detect antigens and antibodies. Trends Microbiol 19:295–302 [View Article][PubMed]
    [Google Scholar]
  37. Malou N., Renvoise A., Nappez C., Raoult D. 2012a; Immuno-PCR for the early serological diagnosis of acute infectious diseases: the Q fever paradigm. Eur J Clin Microbiol Infect Dis 31:1951–1960 [View Article][PubMed]
    [Google Scholar]
  38. Malou N., Tran T. N., Nappez C., Signoli M., Le Forestier C., Castex D., Drancourt M., Raoult D. 2012b; Immuno-PCR – a new tool for paleomicrobiology: the plague paradigm. PLoS ONE 7:e31744 [View Article][PubMed]
    [Google Scholar]
  39. Matsushita T., Shirasaki N., Tatsuki Y., Matsui Y. 2013; Investigating norovirus removal by microfiltration, ultrafiltration, and precoagulation-microfiltration processes using recombinant norovirus virus-like particles and real-time immuno-PCR. Water Res 47:5819–5827 [View Article][PubMed]
    [Google Scholar]
  40. McKie A., Samuel D., Cohen B., Saunders N. A. 2002a; A quantitative immuno-PCR assay for the detection of mumps-specific IgG. J Immunol Methods 270:135–141 [View Article][PubMed]
    [Google Scholar]
  41. McKie A., Samuel D., Cohen B., Saunders N. A. 2002b; Development of a quantitative immuno-PCR assay and its use to detect mumps-specific IgG in serum. J Immunol Methods 261:167–175 [View Article][PubMed]
    [Google Scholar]
  42. Mehta P. K., Raj A., Singh N., Khuller G. K. 2012a; Diagnosis of extrapulmonary tuberculosis by PCR. FEMS Immunol Med Microbiol 66:20–36 [View Article][PubMed]
    [Google Scholar]
  43. Mehta P. K., Kalra M., Khuller G. K., Behera D., Verma I. 2012b; Development of an ultrasensitive polymerase chain reaction-amplified immunoassay based on mycobacterial RD antigens: implications for the serodiagnosis of tuberculosis. Diagn Microbiol Infect Dis 72:166–174 [View Article][PubMed]
    [Google Scholar]
  44. Monjezi R., Tan S. W., Tey B. T., Sieo C. C., Tan W. S. 2013; Detection of hepatitis B virus core antigen by phage display mediated TaqMan real-time immuno-PCR. J Virol Methods 187:121–126 [View Article][PubMed]
    [Google Scholar]
  45. Morin I., Schaeffer P. M. 2012; Combining RNA–DNA swapping and quantitative polymerase chain reaction for the detection of influenza A nucleoprotein. Anal Biochem 420:121–126[PubMed] [CrossRef]
    [Google Scholar]
  46. Musser J. M., Kapur V., Szeto J., Pan X., Swanson D. S., Martin D. R. 1995; Genetic diversity and relationships among Streptococcus pyogenes strains expressing serotype M1 protein: recent intercontinental spread of a subclone causing episodes of invasive disease. Infect Immun 63:994–1003[PubMed]
    [Google Scholar]
  47. Mweene A. S., Ito T., Okazaki K., Ono E., Shimizu Y., Kida H. 1996; Development of immuno-PCR for diagnosis of bovine herpesvirus 1 infection. J Clin Microbiol 34:748–750[PubMed]
    [Google Scholar]
  48. Nam J. M., Thaxton C. S., Mirkin C. A. 2003; Nanoparticle-based bio-bar codes for the ultrasensitive detection of proteins. Science 301:1884–1886 [View Article][PubMed]
    [Google Scholar]
  49. Niemeyer C. M., Adler M., Blohm D. 1997; Fluorometric polymerase chain reaction (PCR) enzyme-linked immunosorbent assay for quantification of immuno-PCR products in microplates. Anal Biochem 246:140–145 [View Article][PubMed]
    [Google Scholar]
  50. Niemeyer C. M., Adler M., Wacker R. 2005; Immuno-PCR: high sensitivity detection of proteins by nucleic acid amplification. Trends Biotechnol 23:208–216 [View Article][PubMed]
    [Google Scholar]
  51. Niemeyer C. M., Adler M., Wacker R. 2007; Detecting antigens by quantitative immuno-PCR. Nat Protoc 2:1918–1930 [View Article][PubMed]
    [Google Scholar]
  52. Ogunjimi A. A., Choudary P. V. 1999; Adsorption of endogenous polyphenols relieves the inhibition by fruit juices and fresh produce of immuno-PCR detection of Escherichia coli O157 : H7. FEMS Immunol Med Microbiol 23:213–220 [View Article][PubMed]
    [Google Scholar]
  53. Ozaki H., Sugita S., Kida H. 2001; A rapid and highly sensitive method for diagnosis of equine influenza by antigen detection using immuno-PCR. Jpn J Vet Res 48:187–195[PubMed]
    [Google Scholar]
  54. Perez J. W., Vargis E. A., Russ P. K., Haselton F. R., Wright D. W. 2011; Detection of respiratory syncytial virus using nanoparticle amplified immuno-polymerase chain reaction. Anal Biochem 410:141–148 [View Article][PubMed]
    [Google Scholar]
  55. Perez J. W., Adams N. M., Zimmerman G. R., Haselton F. R., Wright D. W. 2013; Detecting respiratory syncytial virus using nanoparticle-amplified immuno-PCR. Methods Mol Biol 1026:93–110 [View Article][PubMed]
    [Google Scholar]
  56. Peroni L. A., Reis J. R., Coletta-Filho H. D., de Souza A. A., Machado M. A., Stach-Machado D. R. 2008; Assessment of the diagnostic potential of immmunocapture-PCR and immuno-PCR for Citrus variegated chlorosis. J Microbiol Methods 75:302–307 [View Article][PubMed]
    [Google Scholar]
  57. Potůčková L., Franko F., Bambousková M., Dráber P. 2011; Rapid and sensitive detection of cytokines using functionalized gold nanoparticle-based immuno-PCR, comparison with immuno-PCR and ELISA. J Immunol Methods 371:38–47 [View Article][PubMed]
    [Google Scholar]
  58. Rajkovic A., El Moualij B., Uyttendaele M., Brolet P., Zorzi W., Heinen E., Foubert E., Debevere J. 2006; Immunoquantitative real-time PCR for detection and quantification of Staphylococcus aureus enterotoxin B in foods. Appl Environ Microbiol 72:6593–6599 [View Article][PubMed]
    [Google Scholar]
  59. Romeis J., Meissle M., Bigler F. 2006; Transgenic crops expressing Bacillus thuringiensis toxins and biological control. Nat Biotechnol 24:63–71 [View Article][PubMed]
    [Google Scholar]
  60. Sano T., Smith C. L., Cantor C. R. 1992; Immuno-PCR: very sensitive antigen detection by means of specific antibody–DNA conjugates. Science 258:120–122 [View Article][PubMed]
    [Google Scholar]
  61. Shirasaki N., Matsushita T., Matsui Y., Oshiba A., Ohno K. 2010; Estimation of norovirus removal performance in a coagulation–rapid sand filtration process by using recombinant norovirus VLPs. Water Res 44:1307–1316 [View Article][PubMed]
    [Google Scholar]
  62. Sims P. W., Vasser M., Wong W. L., Williams P. M., Meng Y. G. 2000; Immunopolymerase chain reaction using real-time polymerase chain reaction for detection. Anal Biochem 281:230–232 [View Article][PubMed]
    [Google Scholar]
  63. Singer D., Soininen H., Alafuzoff I., Hoffmann R. 2009; Immuno-PCR-based quantification of multiple phosphorylated tau-epitopes linked to Alzheimer’s disease. Anal Bioanal Chem 395:2263–2267 [View Article][PubMed]
    [Google Scholar]
  64. Tian P., Mandrell R. 2006; Detection of norovirus capsid proteins in faecal and food samples by a real time immuno-PCR method. J Appl Microbiol 100:564–574 [View Article][PubMed]
    [Google Scholar]
  65. Tran T. N., Aboudharam G., Raoult D., Drancourt M. 2011; Beyond ancient microbial DNA: nonnucleotidic biomolecules for paleomicrobiology. Biotechniques 50:370–380 [View Article][PubMed]
    [Google Scholar]
  66. Wacker, R. (2006). Infect Dis Workshop 1. Immuno-PCR- maximizing immunoassay sensitivity. In: Chimera Biotec Association for Molecular Pathology. Annual Meeting & Exhibition, Orlando, FL, USA, 17 November 2006
  67. Wacker R., Ceyhan B., Alhorn P., Schueler D., Lang C., Niemeyer C. M. 2007; Magneto immuno-PCR: a novel immunoassay based on biogenic magnetosome nanoparticles. Biochem Biophys Res Commun 357:391–396 [View Article][PubMed]
    [Google Scholar]
  68. Wu H. C., Huang Y. L., Lai S. C., Huang Y. Y., Shaio M. F. 2001; Detection of Clostridium botulinum neurotoxin type A using immuno-PCR. Lett Appl Microbiol 32:321–325 [View Article][PubMed]
    [Google Scholar]
  69. Zhang G., Pan Q., Weintraub A. 1998; Identification of Bacteroides fragilis by a modified immuno polymerase chain reaction (mIPCR), using a specific monoclonal antibody. Anaerobe 4:189–196 [View Article][PubMed]
    [Google Scholar]
  70. Zhang W., Bielaszewska M., Friedrich A. W., Kuczius T., Karch H. 2005; Transcriptional analysis of genes encoding Shiga toxin 2 and its variants in Escherichia coli . Appl Environ Microbiol 71:558–561 [View Article][PubMed]
    [Google Scholar]
  71. Zhang W., Bielaszewska M., Pulz M., Becker K., Friedrich A. W., Karch H., Kuczius T. 2008; New immuno-PCR assay for detection of low concentrations of Shiga toxin 2 and its variants. J Clin Microbiol 46:1292–1297 [View Article][PubMed]
    [Google Scholar]
  72. Zhou H., Fisher R. J., Papas T. S. 1993; Universal immuno-PCR for ultra-sensitive target protein detection. Nucleic Acids Res 21:6038–6039 [View Article][PubMed]
    [Google Scholar]
/content/journal/jmm/10.1099/jmm.0.070318-0
Loading
/content/journal/jmm/10.1099/jmm.0.070318-0
Loading

Data & Media loading...

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error