SIGNIFICANCE OF MOLECULAR BIOMARKERS IN THE DIAGNOSIS OF NEUROMYELITIS OPTICA SPECTRUM DISORDER
Abstract
Discovery of antibodies to aquaporin-4 channels as a laboratory or molecular biomarker for neuromyelitis optica spectrum disorder contributed to a better understanding of the etiopathogenesis with a clear separation of the clinical, neuroradiological and laboratory characteristics of this disease, which resulted in the definition of criteria for establishing the diagnosis of neuromyelitis optica spectrum disorder and a clear distinction in relation to multiple sclerosis. Clinical presentation of the inflammatory diseases of the central nervous system may be highly variable, with numerous, often overlapping symptoms and signs. Therefore, in the differential diagnostic, in addition to the clinical presentation, it is necessary to consider paraclinical characteristics, such as laboratory findings of the blood and cerebrospinal fluid and the neuroradiological examination findings. Since aquaporin-4 is a clearly defined crucial diagnostic biomarker in the neuromyelitis optica spectrum disorder, different methodological approaches were developed to test antibodies to aquaporin-4 taking into account the specificity and sensitivity of the tests themselves. One of the first tests that was routinely applied in clinical practice for the detection of antibodies to aquaporin-4 were tests in the form of an immunoenzymatic assay that showed great variability in the degree of specificity and sensitivity. The second group of tests for the detection of antibodies to aquaporin-4 applied the technique of indirect immunofluorescence on a substrate of animal origin, which achieved a higher degree of sensitivity and specificity with certain disadvantages such as the impossibility of precise quantification as well as difficulties in the interpretation of the results. Special methodological principles of immunoprecipitation such as fluorescent and radioimmunoprecipitation did not achieve a satisfactory level of sensitivity in the detection of antibodies to aquaporin-4. The highest level of sensitivity with absolute specificity has been achieved via developing a cell assay methodology based on the application of human aquaporin-4 transfected cells fixed on a biochip with a negative control when antibodies to aquaporin-4 from serum are detected by indirect immunofluorescence methodology or special cellular assays when these antibodies are quantified by flow cytometry method. The possibility to use this cell assaymethodology is extremely important in order to establish the correct diagnosis of seropositive neuromyelitis optica spectrum disorder.
References
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2. Jarius S, Wildemann B. The history of neuromyelitis optica. J Neuroinflammation. 2013;10:8.
3. Jarius S, Wildemann B. The history of neuromyelitis optica. Part 2: 'Spinal amaurosis', or how it all began. J Neuroinflammation. 2019;16(1):280.
4. Devic E. Myélite aiguë dorso-lombaire avec névrite optique. - Autopsie. Paris: Asselin et Houzeau, Louis Savy; 1895. 434–9 p.
5. Brain W. Critical review: disseminated sclerosis. QJM. 1930;23:343–91
6. Wingerchuk DM, Hogancamp WF, O'Brien PC, Weinshenker BG. The clinical course of neuromyelitis optica (Devic's syndrome). Neurology. 1999;53(5):1107-14.
7. Lennon VA, Wingerchuk DM, Kryzer TJ, Pittock SJ, Lucchinetti CF, Fujihara K, et al. A serum autoantibody marker of neuromyelitis optica: distinction from multiple sclerosis. Lancet. 2004;364(9451):2106-12.
8. Wingerchuk DM, Lennon VA, Pittock SJ, Lucchinetti CF, Weinshenker BG. Revised diagnostic criteria for neuromyelitis optica. Neurology. 2006;66(10):1485-9.
9. Wingerchuk DM, Banwell B, Bennett JL, Cabre P, Carroll W, Chitnis T, et al. International consensus diagnostic criteria for neuromyelitis optica spectrum disorders. Neurology. 2015;85(2):177-89.
10. Solomon AJ, Arrambide G, Brownlee WJ, Flanagan EP, Amato MP, Amezcua L, et al. Differential diagnosis of suspected multiple sclerosis: an updated consensus approach. Lancet Neurol. 2023 Aug;22(8):750-768.
11. Banwell B, Bennett JL, Marignier R, Kim HJ, Brilot F, Flanagan EP, et al. Diagnosis of myelin oligodendrocyte glycoprotein antibody-associated disease: International MOGAD Panel proposed criteria. Lancet Neurol. 2023 Mar;22(3):268-282.
12. Rahimi J, Woehrer A. Overview of cerebrospinal fluid cytology. Handb Clin Neurol. 2017;145:563-571.
13. Hepnar D, Adam P, Žáková H, Krušina M, Kalvach P, Kasík J, et al. Recommendations for cerebrospinal fluid analysis. Folia Microbiol (Praha). 2019 May;64(3):443-452.
14. Jarius S, Aktas O, Ayzenberg I, Bellmann-Strobl J, Berthele A, Giglhuber K, et al. Update on the diagnosis and treatment of neuromyelits optica spectrum disorders (NMOSD) - revised recommendations of the Neuromyelitis Optica Study Group (NEMOS). Part I: Diagnosis and differential diagnosis. J Neurol. 2023 Jul;270(7):3341-3368.
15. Lovato L, Willis SN, Rodig SJ, Caron T, Almendinger SE, Howell OW, et al. Related B cell clones populate the meninges and parenchyma of patients with multiple sclerosis. Brain. 2011 Feb;134(Pt 2):534-41.
16. Racke MK. The role of B cells in multiple sclerosis: rationale for B-cell-targeted therapies. Curr Opin Neurol. 2008 Apr;21 Suppl 1:S9-S18.
17. Petzold A. Intrathecal oligoclonal IgG synthesis in multiple sclerosis. J Neuroimmunol. 2013 Sep 15;262(1-2):1-10.
18. Deisenhammer F, Zetterberg H, Fitzner B, Zettl UK. The Cerebrospinal Fluid in Multiple Sclerosis. Front Immunol. 2019 Apr 12;10:726.
19. Deisenhammer F, Sellebjerg F, Teunissen CE, Tumani H, Deisenhammer F, Sellebjerg F, et al. Cerebrospinal Fluid in Clinical Neurology. 1st ed. Cham; New York, NY; Dordrecht; London: Springer (2015).
20. Carta S, Ferraro D, Ferrari S, Briani C, Mariotto S. Oligoclonal bands: clinical utility and interpretation cues. Crit Rev Clin Lab Sci. 2022 Sep;59(6):391-404.
21. Freedman MS, Thompson EJ, Deisenhammer F, Giovannoni G, Grimsley G, Keir G, et al. Recommended standard of cerebrospinal fluid analysis in the diagnosis of multiple sclerosis: a consensus statement. Arch Neurol. 2005;62(6):865-70.
22. Thompson AJ, Banwell BL, Barkhof F, Carroll WM, Coetzee T, Comi G, et al. Diagnosis of multiple sclerosis: 2017 revisions of the McDonald criteria. Lancet Neurol. 2018 Feb;17(2):162-173.
23. Link H, Huang YM. Oligoclonal bands in multiple sclerosis cerebrospinal fluid: an update on methodology and clinical usefulness. J Neuroimmunol. 2006 Nov;180(1-2):17-28.
24. Olsson T. Multiple sclerosis:cerebrospinal fluid. Ann Neurol. 1994;36 Suppl:S100-2.
25. Dobson R, Ramagopalan S, Davis A, Giovannoni G. Cerebrospinal fluid oligoclonal bands in multiple sclerosis and clinically isolated syndromes: a meta-analysis of prevalence, prognosis and effect of latitude. J Neurol Neurosurg Psychiatry. 2013 Aug;84(8):909-14.
26. Reiber H, Teut M, Pohl D, Rostasy KM, Hanefeld F. Paediatric and adult multiple sclerosis: age-related differences and time course of the neuroimmunological response in cerebrospinal fluid. Mult Scler 2009;15:1466–80.
27. Hegen H, Walde J, Berek K, Arrambide G, Gnanapavan S, Kaplan B, et al. Cerebrospinal fluid kappa free light chains for the diagnosis of multiple sclerosis: A systematic review and meta-analysis. Mult Scler. 2023 Feb;29(2):169-181.
28. O’Riordan JI, Gallagher HL, Thompson AJ, Howard RS, Kingsley DP, Thompson EJ, et al. Clinical, CSF, and MRI findings in Devic’s neuromyelitis optica. J Neurol Neurosurg Psychiatry 1996; 60: 382/87.
29. Jarius S, Paul F, Franciotta D, Ruprecht K, Ringelstein M, Bergamaschi R, et al. Cerebrospinal fluid findings in aquaporin-4 antibody positive neuromyelitis optica: results from 211 lumbar punctures. J Neurol Sci. 2011 Jul 15;306(1-2):82-90.
23. Bergamaschi R, Tonietti S, Franciotta D, Candeloro E, Tavazzi E, Piccolo G, et al. Oligoclonal bands in Devic’s neuromyelitis optica and multiple sclerosis: differences in repeated cerebrospinal fluid examinations. Mult Scler 2004; 10: 2-4.
31. Nakashima I, Fujihara K, Sato S, Itoyama Y. Oligoclonal IgG bands in Japanese patients with multiple sclerosis. A comparative study between isoelectric focusing with IgG immunofixation and high-resolution agarose gel electrophoresis. J Neuroimmunol. 2005 Feb;159(1-2):133-6.
32. Nakamura M, Nakashima I, Sato S, Miyazawa I, Fujihara K, Itoyama Y. Clinical and laboratory features of neuromyelitis optica with oligoclonal IgG bands. Mult Scler. 2007 Apr;13(3):332-5.
33. Foo JN, Liu JJ, Tan EK. Whole-genome and whole-exome sequencing in neurological diseases. Nat Rev Neurol. 2012;8(9):508-17.
34. Verma M, Kulshrestha S, Puri A. Genome Sequencing. Methods Mol Biol. 2017;
1525:3-33.
35. Hu T, Chitnis N, Monos D, Dinh A. Next-generation sequencing technologies: An overview. Hum Immunol. 2021;82(11):801-11.
36. Xue Y, Ankala A, Wilcox WR, Hegde MR. Solving the molecular diagnostic testing conundrum for Mendelian disorders in the era of next-generation sequencing: single-gene, gene panel, or exome/genome sequencing. Genet Med. 2015;17(6):444-51.
37. Wolburg H, Wolburg-Buchholz K, Fallier-Becker P, Noell S, Mack AF. Structure and functions of aquaporin-4-based orthogonal arrays of particles. Int Rev Cell Mol Biol. 2011;287:1-41.
38. Li S, Li C, Wang W. Molecular aspects of aquaporins. Vitam Horm. 2020;113:129-81.
39. Lu M, Lee MD, Smith BL, Jung JS, Agre P, Verdijk MA, et al. The human AQP4 gene: definition of the locus encoding two water channel polypeptides in brain. Proc Natl Acad Sci U S A. 1996;93(20):10908-12.
40. Yang B, Ma T, Verkman AS. cDNA cloning, gene organization, and chromosomal localization of a human mercurial insensitive water channel. Evidence for distinct transcriptional units. J Biol Chem. 1995;270(39):22907-13.
41. Neely JD, Christensen BM, Nielsen S, Agre P. Heterotetrameric composition of aquaporin-4 water channels. Biochemistry. 1999;38(34):11156-63.
42. Rash JE, Yasumura T, Hudson CS, Agre P, Nielsen S. Direct immunogold labeling of aquaporin-4 in square arrays of astrocyte and ependymocyte plasma membranes in rat brain and spinal cord. Proc Natl Acad Sci U S A. 1998;95(20):11981-6.
43. Venero JL, Vizuete ML, Machado A, Cano J. Aquaporins in the central nervous system. Prog Neurobiol. 2001;63(3):321-36.
44. Hasegawa H, Ma T, Skach W, Matthay MA, Verkman AS. Molecular cloning of a mercurial-insensitive water channel expressed in selected water-transporting tissues. J Biol Chem. 1994;269(8):5497-500.
45. Nicchia GP, Mastrototaro M, Rossi A, Pisani F, Tortorella C, Ruggieri M, et al. Aquaporin-4 orthogonal arrays of particles are the target for neuromyelitis optica autoantibodies. Glia. 2009;57:1363–1373.
46. Pisani F, Mastrototaro M, Rossi A, Nicchia GP, Tortorella C, Ruggieri M, et al. Identification of two major conformational aquaporin-4 epitopes for neuromyelitis optica autoantibody binding. J Biol Chem. 2011;286: 9216–9224.
47. Pisani F, Sparaneo A, Tortorella C, Ruggieri M, Trojano M, Mola MG, et al. Aquaporin-4 autoantibodies in Neuromyelitis Optica: AQP4 isoform-dependent sensitivity and specificity. PLoS One. 2013;8(11):e79185.
48. Waters PJ, Pittock SJ, Bennett JL, Jarius S, Weinshenker BG, Wingerchuk DM. Evaluation of aquaporin-4 antibody assays. Clin Exp Neuroimmunol. 2014;5(3):290-303.
49. Redenbaugh V, Montalvo M, Sechi E, Buciuc M, Fryer JP, McKeon A, et al. Diagnostic value of aquaporin-4-IgG live cell based assay in neuromyelitis optica spectrum disorders. Mult Scler J Exp Transl Clin. 2021;7(4):20552173211052656.
50. Tabatabaei MS, Ahmed M. Enzyme-Linked Immunosorbent Assay (ELISA). Methods Mol Biol. 2022;2508:115-134.
51. Hayrapetyan H, Tran T, Tellez-Corrales E, Madiraju C. Enzyme-Linked Immunosorbent Assay: Types and Applications. Methods Mol Biol. 2023;2612:1-17.
52. Hayakawa S, Mori M, Okuta A, Kamegawa A, Fujiyoshi Y, Yoshiyama Y, et al. Neuromyelitis optica and anti-aquaporin-4 antibodies measured by an enzyme-linked immunosorbent assay. J Neuroimmunol. 2008;196(1–2):181–7.
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2025/12/19
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