Osteopontin (OPN) as a CSF and blood biomarker for multiple sclerosis: A systematic review and meta-analysis

PLoS ONE

Volumn 13, Issue 1, 2018, Pages

  Agah, Elmira ^a,b   Zardoui, Arshia ^a,b   Saghazadeh, Amene ^a,c   Ahmadi, Mona ^d   Tafakhori, Abbas ^b,d   Rezaei, Nima ^a,e  

^a TEHRAN UNIVERSITY OF MEDICAL SCIENCES   (Iran)

^b NeuroImmunology Research Association (NIRA)   (Iran)

^c Malignancy and Autoimmunity (NIIMA)   (United States)

^d TEHRAN UNIVERSITY OF MEDICAL SCIENCES   (Iran)

^e UNIVERSAL SCIENTIFIC EDUCATION AND RESEARCH NETWORK USERN   (Iran)

Author keywords

[No Author keywords available]

Indexed keywords

OSTEOPONTIN; BIOLOGICAL MARKER;

BLOOD ANALYSIS; CEREBROSPINAL FLUID ANALYSIS; DIAGNOSTIC VALUE; DISEASE ACTIVITY; DISEASE COURSE; DISEASE MARKER; HUMAN; META ANALYSIS; MULTIPLE SCLEROSIS; PROGNOSIS; PROTEIN BLOOD LEVEL; PROTEIN CEREBROSPINAL FLUID LEVEL; REVIEW; SYSTEMATIC REVIEW; BLOOD; CASE CONTROL STUDY; CEREBROSPINAL FLUID; METABOLISM;

BIOMARKERS; CASE-CONTROL STUDIES; HUMANS; MULTIPLE SCLEROSIS; OSTEOPONTIN;

EID: 85040765672     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0190252     Document Type: Review

References (66)

1. Hemmer B, Kerschensteiner M, Korn T. Role of the innate and adaptive immune responses in the course of multiple sclerosis. The Lancet Neurology. 2015; 14(4):406–19. Epub 2015/03/21. https://doi.org/10.1016/S1474-4422(14)70305-9 PMID: 25792099.
2. Tullman MJ. Overview of the epidemiology, diagnosis, and disease progression associated with multiple sclerosis. The American journal of managed care. 2013; 19(2 Suppl):S15–20. Epub 2013/04/12. PMID: 23544716.
3. Lublin FD, Reingold SC, Cohen JA, Cutter GR, Sørensen PS, Thompson AJ, et al. Defining the clinical course of multiple sclerosis: The 2013 revisions. Neurology. 2014; 83(3):278–86. https://doi.org/10.1212/WNL.0000000000000560 PMC4117366. PMID: 24871874
4. Chung S-E, Cheong H-K, Park J-H, Kim HJ. Burden of Disease of Multiple Sclerosis in Korea. Epidemiology and Health. 2012; 34:e2012008. https://doi.org/10.4178/epih/e2012008 PMC3521103. PMID: 23251838
5. Teunissen CE, Malekzadeh A, Leurs C, Bridel C, Killestein J. Body fluid biomarkers for multiple sclerosis—the long road to clinical application. Nature reviews Neurology. 2015; 11(10):585–96. Epub 2015/ 09/24. https://doi.org/10.1038/nrneurol.2015.173 PMID: 26392381.
6. Polman CH, Reingold SC, Banwell B, Clanet M, Cohen JA, Filippi M, et al. Diagnostic criteria for multiple sclerosis: 2010 revisions to the McDonald criteria. Annals of neurology. 2011; 69(2):292–302. Epub 2011/03/10. https://doi.org/10.1002/ana.22366 PMID: 21387374; PubMed Central PMCID: PMCPmc3084507.
7. Filippi M, Rocca MA, Ciccarelli O, De Stefano N, Evangelou N, Kappos L, et al. MRI criteria for the diagnosis of multiple sclerosis: MAGNIMS consensus guidelines. The Lancet Neurology. 2016; 15(3):292–303. Epub 2016/01/30. https://doi.org/10.1016/S1474-4422(15)00393-2 PMID: 26822746; PubMed Central PMCID: PMCPmc4760851.
8. Kanekar S, Devgun P. A pattern approach to focal white matter hyperintensities on magnetic resonance imaging. Radiologic clinics of North America. 2014; 52(2):241–61. Epub 2014/03/04. https://doi.org/10.1016/j.rcl.2013.11.010 PMID: 24582339.
9. 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. Archives of neurology. 2005; 62(6):865–70. Epub 2005/06/16. https://doi.org/10.1001/archneur.62.6.865 PMID: 15956157.
10. Giesser BS. Diagnosis of multiple sclerosis. Neurologic clinics. 2011; 29(2):381–8. Epub 2011/03/29. https://doi.org/10.1016/j.ncl.2010.12.001 PMID: 21439447.
11. Comabella M, Montalban X. Body fluid biomarkers in multiple sclerosis. The Lancet Neurology. 2014; 13(1):113–26. Epub 2013/12/18. https://doi.org/10.1016/S1474-4422(13)70233-3 PMID: 24331797.
12. Housley WJ, Pitt D, Hafler DA. Biomarkers in multiple sclerosis. Clinical immunology (Orlando, Fla). 2015; 161(1):51–8. Epub 2015/07/06. https://doi.org/10.1016/j.clim.2015.06.015 PMID: 26143623.
13. Biomarkers and surrogate endpoints: preferred definitions and conceptual framework. Clinical pharmacology and therapeutics. 2001; 69(3):89–95. Epub 2001/03/10. https://doi.org/10.1067/mcp.2001. 113989 PMID: 11240971.
14. Harris VK, Sadiq SA. Biomarkers of therapeutic response in multiple sclerosis: current status. Molecular diagnosis & therapy. 2014; 18(6):605–17. Epub 2014/08/29. https://doi.org/10.1007/s40291-014-0117-0 PMID: 25164543; PubMed Central PMCID: PMCPmc4245485.
15. Bandopadhyay M, Bulbule A, Butti R, Chakraborty G, Ghorpade P, Ghosh P, et al. Osteopontin as a therapeutic target for cancer. Expert opinion on therapeutic targets. 2014; 18(8):883–95. Epub 2014/06/ 06. https://doi.org/10.1517/14728222.2014.925447 PMID: 24899149.
16. Lund SA, Giachelli CM, Scatena M. The role of osteopontin in inflammatory processes. Journal of cell communication and signaling. 2009; 3(3–4):311–22. Epub 2009/10/03. https://doi.org/10.1007/s12079-009-0068-0 PMID: 19798593; PubMed Central PMCID: PMCPmc2778587.
17. Rittling SR, Singh R. Osteopontin in Immune-mediated Diseases. Journal of dental research. 2015; 94 (12):1638–45. Epub 2015/09/06. https://doi.org/10.1177/0022034515605270 PMID: 26341976; PubMed Central PMCID: PMCPmc4681477.
18. Chabas DE, Steinman L, Rittling SR, Sobel R, Lock C, Mitchell D, et al. Elevated osteopontin transcripts in MS brain libraries and its role in the development of progressive versus remitting autoimmune encephalomyelitis. Faseb Journal. 2001; 15(4):A354–A. WOS:000167438102025.
19. Hur EM, Youssef S, Haws ME, Zhang SY, Sobel RA, Steinman L. Osteopontin-induced relapse and progression of autoimmune brain disease through enhanced survival of activated T cells. Nature immunology. 2007; 8(1):74–83. Epub 2006/12/05. https://doi.org/10.1038/ni1415 PMID: 17143274.
20. Vogt MH, Lopatinskaya L, Smits M, Polman CH, Nagelkerken L. Elevated osteopontin levels in active relapsing-remitting multiple sclerosis. Annals of neurology. 2003; 53(6):819–22. Epub 2003/06/05. https://doi.org/10.1002/ana.10606 PMID: 12783433.
21. Chabas D, Baranzini SE, Mitchell D, Bernard CC, Rittling SR, Denhardt DT, et al. The influence of the proinflammatory cytokine, osteopontin, on autoimmune demyelinating disease. Science (New York, NY). 2001; 294(5547):1731–5. Epub 2001/11/27. https://doi.org/10.1126/science.1062960 PMID: 11721059.
22. Chiocchetti A, Comi C, Indelicato M, Castelli L, Mesturini R, Bensi T, et al. Osteopontin gene haplotypes correlate with multiple sclerosis development and progression. Journal of neuroimmunology. 2005; 163 (1–2):172–8. Epub 2005/05/12. https://doi.org/10.1016/j.jneuroim.2005.02.020 PMID: 15885319.
23. Comi C, Castelli L, Cerutti E, Chiocchetti A, Galimberti D, Fenoglio C, et al. Osteopontin gene variations protect against multiple sclerosis development and evolution. Multiple Sclerosis. 2007; 13:S194–S. WOS:000251423400597.
24. Vogt MH, Floris S, Killestein J, Knol DL, Smits M, Barkhof F, et al. Osteopontin levels and increased disease activity in relapsing-remitting multiple sclerosis patients. Journal of neuroimmunology. 2004; 155 (1–2):155–60. Epub 2004/09/03. https://doi.org/10.1016/j.jneuroim.2004.06.007 PMID: 15342207.
25. Altintas A, Saruhan-Direskeneli G, Benbir G, Demir M, Purisa S. The role of osteopontin: a shared pathway in the pathogenesis of multiple sclerosis and osteoporosis? Journal of the neurological sciences. 2009; 276(1–2):41–4. Epub 2008/10/11. https://doi.org/10.1016/j.jns.2008.08.031 PMID: 18845306.
26. Assadi M, Salimipour H, Akbarzadeh S, Nemati R, Jafari SM, Bargahi A, et al. Correlation of circulating omentin-1 with bone mineral density in multiple sclerosis: the crosstalk between bone and adipose tissue. PloS one. 2011; 6(9):e24240. Epub 2011/09/22. https://doi.org/10.1371/journal.pone.0024240 PMID: 21935388; PubMed Central PMCID: PMCPmc3174149.
27. Bornsen L, Khademi M, Olsson T, Sorensen PS, Sellebjerg F. Osteopontin concentrations are increased in cerebrospinal fluid during attacks of multiple sclerosis. Multiple sclerosis (Houndmills, Basingstoke, England). 2011; 17(1):32–42. Epub 2010/10/06. https://doi.org/10.1177/ 1352458510382247 PMID: 20921238.
28. Braitch M, Nunan R, Niepel G, Edwards LJ, Constantinescu CS. Increased osteopontin levels in the cerebrospinal fluid of patients with multiple sclerosis. Archives of neurology. 2008; 65(5):633–5. Epub 2008/05/14. https://doi.org/10.1001/archneur.65.5.633 PMID: 18474739.
29. Chowdhury SA, Lin J, Sadiq SA. Specificity and correlation with disease activity of cerebrospinal fluid osteopontin levels in patients with multiple sclerosis. Archives of neurology. 2008; 65(2):232–5. Epub 2008/02/13. https://doi.org/10.1001/archneurol.2007.33 PMID: 18268193.
30. Comabella M, Pericot I, Goertsches R, Nos C, Castillo M, Blas Navarro J, et al. Plasma osteopontin levels in multiple sclerosis. Journal of neuroimmunology. 2005; 158(1–2):231–9. Epub 2004/12/14. https://doi.org/10.1016/j.jneuroim.2004.09.004 PMID: 15589058.
31. Comi C, Cappellano G, Chiocchetti A, Orilieri E, Buttini S, Ghezzi L, et al. The impact of osteopontin gene variations on multiple sclerosis development and progression. Clinical & developmental immunology. 2012; 2012:212893. Epub 2012/09/26. https://doi.org/10.1155/2012/212893 PMID: 23008732; PubMed Central PMCID: PMCPmc3447190.
32. Edwards LJ, Sharrack B, Ismail A, Tench CR, Gran B, Dhungana S, et al. Increased levels of interleu-kins 2 and 17 in the cerebrospinal fluid of patients with idiopathic intracranial hypertension. American journal of clinical and experimental immunology. 2013; 2(3):234–44. Epub 2013/11/02. PMID: 24179731; PubMed Central PMCID: PMCPmc3808932.
33. Ferret-Sena V, Maia ESA, Sena A. Natalizumab Treatment Modulates Peroxisome Proliferator-Acti-vated Receptors Expression in Women with Multiple Sclerosis. 2016; 2016:5716415. https://doi.org/10.1155/2016/5716415 PMID: 28077943.
34. Iaffaldano P, Ruggieri M, Viterbo RG, Mastrapasqua M, Trojano M. The improvement of cognitive functions is associated with a decrease of plasma Osteopontin levels in Natalizumab treated relapsing multiple sclerosis. Brain, behavior, and immunity. 2014; 35:176–81. Epub 2013/09/03. https://doi.org/10.1016/j.bbi.2013.08.009 PMID: 23994630.
35. Kariya Y, Kariya Y, Saito T, Nishiyama S, Honda T, Tanaka K, et al. Increased cerebrospinal fluid osteopontin levels and its involvement in macrophage infiltration in neuromyelitis optica. BBA clinical. 2015; 3:126–34. Epub 2015/12/18. https://doi.org/10.1016/j.bbacli.2015.01.003 PMID: 26673877; PubMed Central PMCID: PMCPmc4661545.
36. Khademi M, Bornsen L, Rafatnia F, Andersson M, Brundin L, Piehl F, et al. The effects of natalizumab on inflammatory mediators in multiple sclerosis: prospects for treatment-sensitive biomarkers. European journal of neurology. 2009; 16(4):528–36. Epub 2009/02/18. https://doi.org/10.1111/j.1468-1331.2009.02532.x PMID: 19220425.
37. Khademi M, Dring AM, Gilthorpe JD, Wuolikainen A, Al Nimer F, Harris RA, et al. Intense inflammation and nerve damage in early multiple sclerosis subsides at older age: a reflection by cerebrospinal fluid biomarkers. PloS one. 2013; 8(5):e63172. Epub 2013/05/15. https://doi.org/10.1371/journal.pone. 0063172 PMID: 23667585; PubMed Central PMCID: PMCPmc3646751.
38. Kivisakk P, Healy BC, Francois K, Gandhi R, Gholipour T, Egorova S, et al. Evaluation of circulating osteopontin levels in an unselected cohort of patients with multiple sclerosis: relevance for biomarker development. Multiple sclerosis (Houndmills, Basingstoke, England). 2014; 20(4):438–44. Epub 2013/ 09/06. https://doi.org/10.1177/1352458513503052 PMID: 24005026.
39. Ma N, He Y, Xiao H, Han G, Chen G, Wang Y, et al. BAFF maintains T-cell survival by inducing OPN expression in B cells. Molecular immunology. 2014; 57(2):129–37. Epub 2013/10/03. https://doi.org/10.1016/j.molimm.2013.08.014 PMID: 24084099.
40. Ratzer R, Iversen P, Bornsen L, Dyrby TB, Romme Christensen J, Ammitzboll C, et al. Monthly oral methylprednisolone pulse treatment in progressive multiple sclerosis. Multiple sclerosis (Houndmills, Basingstoke, England). 2015. Epub 2015/10/04. https://doi.org/10.1177/1352458515605908 PMID: 26432857.
41. Romme Christensen J, Bornsen L, Khademi M, Olsson T, Jensen PE, Sorensen PS, et al. CSF inflammation and axonal damage are increased and correlate in progressive multiple sclerosis. Multiple sclerosis (Houndmills, Basingstoke, England). 2013; 19(7):877–84. Epub 2012/11/28. https://doi.org/10.1177/1352458512466929 PMID: 23178691.
42. Romme Christensen J, Ratzer R, Bornsen L, Lyksborg M, Garde E, Dyrby TB, et al. Natalizumab in progressive MS: results of an open-label, phase 2A, proof-of-concept trial. Neurology. 2014; 82(17):1499–507. Epub 2014/04/01. https://doi.org/10.1212/WNL.0000000000000361 PMID: 24682973.
43. Shimizu Y, Ota K, Ikeguchi R, Kubo S, Kabasawa C, Uchiyama S. Plasma osteopontin levels are associated with disease activity in the patients with multiple sclerosis and neuromyelitis optica. Journal of neuroimmunology. 2013; 263(1–2):148–51. Epub 2013/08/06. https://doi.org/10.1016/j.jneuroim.2013.07.005 PMID: 23910387.
44. Stilund M, Gjelstrup MC, Petersen T, Moller HJ, Rasmussen PV, Christensen T. Biomarkers of inflammation and axonal degeneration/damage in patients with newly diagnosed multiple sclerosis: contributions of the soluble CD163 CSF/serum ratio to a biomarker panel. PloS one. 2015; 10(4):e0119681. Epub 2015/04/11. https://doi.org/10.1371/journal.pone.0119681 PMID: 25860354; PubMed Central PMCID: PMCPmc4393241.
45. Strehlow F, Bauer S, Martus P, Weller M, Roth P, Schlegel U, et al. Osteopontin in cerebrospinal fluid as diagnostic biomarker for central nervous system lymphoma. 2016; 129(1):165–71. https://doi.org/10.1007/s11060-016-2162-5 PMID: 27294357.
46. Szalardy L, Zadori D, Simu M, Bencsik K, Vecsei L, Klivenyi P. Evaluating biomarkers of neuronal degeneration and neuroinflammation in CSF of patients with multiple sclerosis-osteopontin as a potential marker of clinical severity. Journal of the neurological sciences. 2013; 331(1–2):38–42. Epub 2013/ 05/28. https://doi.org/10.1016/j.jns.2013.04.024 PMID: 23706476.
47. Tumani H, Kassubek J, Hijazi M, Lehmensiek V, Unrath A, Sussmuth S, et al. Patterns of TH1/TH2 cytokines predict clinical response in multiple sclerosis patients treated with glatiramer acetate. European neurology. 2011; 65(3):164–9. Epub 2011/03/05. https://doi.org/10.1159/000324035 PMID: 21372576.
48. Vogt MH, ten Kate J, Drent RJ, Polman CH, Hupperts R. Increased osteopontin plasma levels in multiple sclerosis patients correlate with bone-specific markers. Multiple sclerosis (Houndmills, Basingstoke, England). 2010; 16(4):443–9. Epub 2010/01/21. https://doi.org/10.1177/1352458509359723 PMID: 20086024.
49. Wen SR, Liu GJ, Feng RN, Gong FC, Zhong H, Duan SR, et al. Increased levels of IL-23 and osteopontin in serum and cerebrospinal fluid of multiple sclerosis patients. Journal of neuroimmunology. 2012; 244(1–2):94–6. Epub 2012/02/15. https://doi.org/10.1016/j.jneuroim.2011.12.004 PMID: 22329905.
50. Moher D, Liberati A, Tetzlaff J, Altman DG. Preferred reporting items for systematic reviews and meta-analyses: the PRISMA statement. BMJ (Clinical research ed). 2009; 339:b2535. Epub 2009/07/23. https://doi.org/10.1136/bmj.b2535 PMID: 19622551; PubMed Central PMCID: PMCPmc2714657.
51. Wells GA, Shea B, O’connell D, Peterson JE, Welch V, Losos M, et al. The Newcastle–Ottawa scale (NOS) for assessing the quality of nonrandomised studies in meta-analyses. 2000.
52. Higgins JP, Green S. Cochrane handbook for systematic reviews of interventions: John Wiley & Sons; 2011.
53. Egger M, Davey Smith G, Schneider M, Minder C. Bias in meta-analysis detected by a simple, graphical test. BMJ (Clinical research ed). 1997; 315(7109):629–34. Epub 1997/10/06. PMID: 9310563; PubMed Central PMCID: PMCPmc2127453.
54. Weiner HL. Multiple sclerosis is an inflammatory T-cell-mediated autoimmune disease. Archives of neurology. 2004; 61(10):1613–5. Epub 2004/10/13. https://doi.org/10.1001/archneur.61.10.1613 PMID: 15477521.
55. Murugaiyan G, Mittal A, Weiner HL. Increased osteopontin expression in dendritic cells amplifies IL-17 production by CD4+ T cells in experimental autoimmune encephalomyelitis and in multiple sclerosis. Journal of immunology (Baltimore, Md: 1950). 2008; 181(11):7480–8. Epub 2008/11/20. PMID: 19017937; PubMed Central PMCID: PMCPmc2653058.
56. Denhardt DT, Noda M, O’Regan AW, Pavlin D, Berman JS. Osteopontin as a means to cope with environmental insults: regulation of inflammation, tissue remodeling, and cell survival. The Journal of clinical investigation. 2001; 107(9):1055–61. Epub 2001/05/09. https://doi.org/10.1172/JCI12980 PMID: 11342566; PubMed Central PMCID: PMCPmc209291.
57. Kawamura K, Iyonaga K, Ichiyasu H, Nagano J, Suga M, Sasaki Y. Differentiation, maturation, and survival of dendritic cells by osteopontin regulation. Clinical and diagnostic laboratory immunology. 2005; 12(1):206–12. Epub 2005/01/12. https://doi.org/10.1128/CDLI.12.1.206-212.2005 PMID: 15643009; PubMed Central PMCID: PMCPmc540203.
58. Diao H, Liu X, Wu Z, Kang L, Cui G, Morimoto J, et al. Osteopontin regulates interleukin-17 production in hepatitis. Cytokine. 2012; 60(1):129–37. Epub 2012/07/24. https://doi.org/10.1016/j.cyto.2012.06. 287 PMID: 22818182.
59. Han RK, Cheng YF, Zhou SS, Guo H, He RD, Chi LJ, et al. Increased circulating Th17 cell populations and elevated CSF osteopontin and IL-17 concentrations in patients with Guillain-Barre syndrome. Journal of clinical immunology. 2014; 34(1):94–103. Epub 2013/11/13. https://doi.org/10.1007/s10875-013-9965-3 PMID: 24217817.
60. Jones AP, Kermode AG, Lucas RM, Carroll WM, Nolan D, Hart PH. Circulating immune cells in multiple sclerosis. Clinical and experimental immunology. 2017; 187(2):193–203. Epub 2016/11/03. https://doi.org/10.1111/cei.12878 PMID: 27689339; PubMed Central PMCID: PMCPmc5217886.
61. Carecchio M, Comi C. The role of osteopontin in neurodegenerative diseases. Journal of Alzheimer’s disease: JAD. 2011; 25(2):179–85. Epub 2011/03/02. https://doi.org/10.3233/JAD-2011-102151 PMID: 21358042.
62. Comi C, Carecchio M, Chiocchetti A, Nicola S, Galimberti D, Fenoglio C, et al. Osteopontin is increased in the cerebrospinal fluid of patients with Alzheimer’s disease and its levels correlate with cognitive decline. Journal of Alzheimer’s disease: JAD. 2010; 19(4):1143–8. Epub 2010/03/24. https://doi.org/10.3233/JAD-2010-1309 PMID: 20308780.
63. Sun Y, Yin XS, Guo H, Han RK, He RD, Chi LJ. Elevated osteopontin levels in mild cognitive impairment and Alzheimer’s disease. Mediators of inflammation. 2013; 2013:615745. Epub 2013/04/12. https://doi.org/10.1155/2013/615745 PMID: 23576854; PubMed Central PMCID: PMCPmc3612435.
64. Yu Z, Kastenmuller G, He Y, Belcredi P, Moller G, Prehn C, et al. Differences between human plasma and serum metabolite profiles. PloS one. 2011; 6(7):e21230. Epub 2011/07/16. https://doi.org/10.1371/journal.pone.0021230 PMID: 21760889; PubMed Central PMCID: PMCPmc3132215.
65. Dendrou CA, Fugger L, Friese MA. Immunopathology of multiple sclerosis. Nature reviews Immunology. 2015; 15(9):545–58. Epub 2015/08/08. https://doi.org/10.1038/nri3871 PMID: 26250739.
66. Carvalho AF, Kohler CA, Brunoni AR, Miskowiak KW, Herrmann N, Lanctot KL, et al. Bias in Peripheral Depression Biomarkers. Psychotherapy and psychosomatics. 2016; 85(2):81–90. Epub 2016/01/26. https://doi.org/10.1159/000441457 PMID: 26808272.