Increased promoter methylation of the immune regulatory gene SHP-1 in leukocytes of multiple sclerosis subjects

Journal of Neuroimmunology

Volumn 246, Issue 1-2, 2012, Pages 51-57

  Kumagai, Chiharu ^a   Kalman, Bernadette ^a,b   Middleton, Frank A ^a   Vyshkina, Tamara ^c   Massa, Paul T ^a  

^a State University of New York Upstate Medical University: College of Medicine   (United States)

^b SYRACUSE VA MEDICAL CENTER   (United States)

^c Multiple Sclerosis Research Center of New York Inc   (United States)

Author keywords

Bisulfite sequencing; Epigenetics; Immune regulation; Multiple sclerosis; PBMC; Protein tyrosine phosphatase

Indexed keywords

BISULFITE; GENOMIC DNA; PROTEIN TYROSINE PHOSPHATASE SHP 1;

ADULT; AGED; ARTICLE; CONTROLLED STUDY; DNA METHYLATION; EPIGENETICS; FEMALE; GENE; GENE EXPRESSION REGULATION; HUMAN; HUMAN CELL; IMMUNOPATHOGENESIS; IMMUNOREGULATION; INFLAMMATION; LEUKOCYTE; MAJOR CLINICAL STUDY; MALE; MULTIPLE SCLEROSIS; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN DEFICIENCY; SHP 1 GENE; UPREGULATION;

DNA METHYLATION; DOWN-REGULATION; HUMANS; INFLAMMATION; INFLAMMATION MEDIATORS; LEUKOCYTES; MULTIPLE SCLEROSIS; PROMOTER REGIONS, GENETIC; PROTEIN TYROSINE PHOSPHATASE, NON-RECEPTOR TYPE 6; UP-REGULATION;

EID: 84860203756     PISSN: 01655728     EISSN: 18728421     Source Type: Journal    
DOI: 10.1016/j.jneuroim.2012.03.003     Document Type: Article

References (51)

1. Baranzini S.E., Mudge J., van Velkinburgh J.C., Khankhanian P., Khrebtukova I., Miller N.A., Zhang L., Farmer A.D., Bell C.J., Kim R.W., May G.D., Woodward J.E., Caillier S.J., McElroy J.P., Gomez R., Pando M.J., Clendenen L.E., Ganusova E.E., Schilkey F.D., Ramaraj T., Khan O.A., Huntley J.J., Luo S., Kwok P.Y., Wu T.D., Schroth G.P., Oksenberg J.R., Hauser S.L., Kingsmore S.F. Genome, epigenome and RNA sequences of monozygotic twins discordant for multiple sclerosis. Nature 2010, 464:1351-1356.
2. Brooks W.H., le Dantec C., Pers J.O., Youinou P., Renaudineau Y. Epigenetics and autoimmunity. J. Autoimmun. 2010, 34:J207-J219.
3. Burrell A.M., Handel A.E., Ramagopalan S.V., Ebers G.C., Morahan J.M. Epigenetic mechanisms in multiple sclerosis and the major histocompatibility complex (MHC). Discov. Med. 2011, 11:187-196.
4. Casaccia-Bonnefil P., Pandozy G., Mastronardi F. Evaluating epigenetic landmarks in the brain of multiple sclerosis patients: a contribution to the current debate on disease pathogenesis. Prog. Neurobiol. 2008, 86:368-378.
5. Cheng J., Kydd A.R., Nakase K., Noonan K.M., Murakami A., Tao H., Dwyer M., Xu C., Zhu Q., Marasco W.A. Negative regulation of the SH2-homology-containing protein-tyrosine phosphatase-1 (SHP-1) P2 promoter by the HTLV-1 tax oncoprotein. Blood 2007, 110:2110-2120.
6. Christophi G.P., Hudson C.A., Gruber R., Christophi C.P., Massa P.T. Promoter-specific induction of the phosphatase SHP-1 by viral infection and cytokines in CNS glia. J. Neurochem. 2008, 105:2511-2523.
7. Christophi G.P., Hudson C.A., Gruber R.C., Christophi C.P., Mihai C., Mejico L.J., Jubelt B., Massa P.T. SHP-1 deficiency and increased inflammatory gene expression in PBMCs of multiple sclerosis patients. Lab. Invest. 2008, 88:243-255.
8. Christophi G.P., Hudson C.A., Panos M., Gruber R., Massa P.T. Modulation of macrophage infiltration and inflammatory activity by the phosphatase SHP-1 in virus-induced demyelinating disease. J. Virol. 2009, 83:522-539.
9. Christophi G.P., Panos M., Hudson C.A., Christophi R.L., Gruber R.C., Mersich A.T., Blystone S.D., Jubelt B., Massa P.T. Macrophages of multiple sclerosis patients display deficient SHP-1 expression and enhanced inflammatory phenotype. Lab. Invest. 2009, 89:742-759.
10. Christophi G.P., Gruber R.C., Panos M., Christophi R.L., Jubelt B., Massa P.T. Interleukin-33 upregulation in peripheral leukocytes and CNS of multiple sclerosis patients. Clin. Immunol. 2012, 142:308-319.
11. Croker B.A., Lawson B.R., Berger M., Eidenschenk C., Blasius A.L., Moresco E.M., Sovath S., Cengia L., Shultz L.D., Theofilopoulos A.N., Pettersson S., Beutler B.A. Inflammation and autoimmunity caused by a SHP1 mutation depend on IL-1, MyD88, and a microbial trigger. Proc. Natl. Acad. Sci. U. S. A. 2008, 105:15028-15033.
12. Croker B.A., Lewis R.S., Babon J.J., Mintern J.D., Jenne D.E., Metcalf D., Zhang J.G., Cengia L.H., O'Donnell J.A., Roberts A.W. Neutrophils require SHP1 to regulate IL-1beta production and prevent inflammatory skin disease. J. Immunol. 2011, 186:1131-1139.
13. David M., Chen H.E., Goelz S., Larner A.C., Neel B.G. Differential regulation of the alpha/beta interferon-stimulated Jak/Stat pathway by the SH2 domain-containing tyrosine phosphatase SHPTP1. Mol. Cell. Biol. 1995, 15:7050-7058.
14. de Rosbo N.K., Ben-Nun A. T-cell responses to myelin antigens in multiple sclerosis; relevance of the predominant autoimmune reactivity to myelin oligodendrocyte glycoprotein. J. Autoimmun. 1998, 11:287-299.
15. Deng C., Minguela A., Hussain R.Z., Lovett-Racke A.E., Radu C., Ward E.S., Racke M.K. Expression of the tyrosine phosphatase SRC homology 2 domain-containing protein tyrosine phosphatase 1 determines T cell activation threshold and severity of experimental autoimmune encephalomyelitis. J. Immunol. 2002, 168:4511-4518.
16. Deng C., Wu B., Yang H., Hussain R.Z., Lovett-Racke A.E., Christadoss P., Racke M.K. Decreased expression of Src homology 2 domain-containing protein tyrosine phosphatase 1 reduces T cell activation threshold but not the severity of experimental autoimmune myasthenia gravis. J. Neuroimmunol. 2003, 138:76-82.
17. Egger G., Liang G., Aparicio A., Jones P.A. Epigenetics in human disease and prospects for epigenetic therapy. Nature 2004, 429:457-463.
18. Feng X., Petraglia A., Chen M., Byskosh P., Boos M., Reder A. Low expression of interferon-stimulated genes in active multiple sclerosis is linked to subnormal phosphorylation of STAT1. J. Neuroimmunol. 2002, 129:205.
19. Frisullo G., Angelucci F., Caggiula M., Nociti V., Iorio R., Patanella A.K., Sancricca C., Mirabella M., Tonali P.A., Batocchi A.P. pSTAT1, pSTAT3, and T-bet expression in peripheral blood mononuclear cells from relapsing-remitting multiple sclerosis patients correlates with disease activity. J. Neurosci. Res. 2006, 84:1027-1036.
20. Gobin S.J., Montagne L., van Zutphen M., van der Valk P., van den Elsen P.J., de Groot C.J. Upregulation of transcription factors controlling MHC expression in multiple sclerosis lesions. Glia 2001, 36:68-77.
21. Hellings N., Baree M., Verhoeven C., D'hooghe M.B., Medaer R., Bernard C.C., Raus J., Stinissen P. T-cell reactivity to multiple myelin antigens in multiple sclerosis patients and healthy controls. J. Neurosci. Res. 2001, 63:290-302.
22. Herman J.G., Umar A., Polyak K., Graff J.R., Ahuja N., Issa J.P., Markowitz S., Willson J.K., Hamilton S.R., Kinzler K.W., Kane M.F., Kolodner R.D., Vogelstein B., Kunkel T.A., Baylin S.B. Incidence and functional consequences of hMLH1 promoter hypermethylation in colorectal carcinoma. Proc. Natl. Acad. Sci. U. S. A. 1998, 95:6870-6875.
23. Howell B.W., Herrick T.M., Hildebrand J.D., Zhang Y., Cooper J.A. Dab1 tyrosine phosphorylation sites relay positional signals during mouse brain development. Curr. Biol. 2000, 10:877-885.
24. Issa J.P. CpG island methylator phenotype in cancer. Nat. Rev. Cancer 2004, 4:988-993.
25. Jiao H., Berrada K., Yang W., Tabrizi M., Platanias L.C., Yi T. Direct association with and dephosphorylation of Jak2 kinase by the SH2-domain-containing protein tyrosine phosphatase SHP-1. Mol. Cell. Biol. 1996, 16:6985-6992.
26. Johnson K.G., Leroy F.G., Borysiewicz L.K., Matthews R.J. TCR signaling thresholds regulating T cell development and activation are dependent upon SHP-1. J. Immunol. 1999, 162:3802-3813.
27. Kanai Y. Genome-wide DNA methylation profiles in precancerous conditions and cancers. Cancer Sci. 2010, 101:36-45.
28. Kornek B., Lassmann H. Neuropathology of multiple sclerosis-new concepts. Brain Res. Bull. 2003, 61:321-326.
29. Koyama M., Oka T., Ouchida M., Nakatani Y., Nishiuchi R., Yoshino T., Hayashi K., Akagi T., Seino Y. Activated proliferation of B-cell lymphomas/leukemias with the SHP1 gene silencing by aberrant CpG methylation. Lab. Invest. 2003, 83:1849-1858.
30. Kruger J., Butler J.R., Cherapanov V., Dong Q., Ginzberg H., Govindarajan A., Grinstein S., Siminovitch K.A., Downey G.P. Deficiency of Src homology 2-containing phosphatase 1 results in abnormalities in murine neutrophil function: studies in motheaten mice. J. Immunol. 2000, 165:5847-5859.
31. Liggett T., Melnikov A., Tilwalli S., Yi Q., Chen H., Replogle C., Feng X., Reder A., Stefoski D., Balabanov R., Levenson V. Methylation patterns of cell-free plasma DNA in relapsing-remitting multiple sclerosis. J. Neurol. Sci. 2010, 290:16-21.
32. Massa P.T., Ropka S.L., Saha S., Fecenko K.L., Beuler K.L. Critical role for protein tyrosine phosphatase SHP-1 in controlling infection of central nervous system glia and demyelination by Theiler's murine encephalomyelitis virus. J. Virol. 2002, 76:8335-8346.
33. McDonald W.I., Compston A., Edan G., Goodkin D., Hartung H.P., Lublin F.D., McFarland H.F., Paty D.W., Polman C.H., Reingold S.C., Sandberg-Wollheim M., Sibley W., Thompson A., van den Noort S., Weinshenker B.Y., Wolinsky J.S. Recommended diagnostic criteria for multiple sclerosis: guidelines from the international panel on the diagnosis of multiple sclerosis. Ann. Neurol. 2001, 50:121-127.
34. Meda F., Folci M., Baccarelli A., Selmi C. The epigenetics of autoimmunity. Cell. Mol. Immunol. 2011, 8:226-236.
35. Nakase K., Cheng J., Zhu Q., Marasco W.A. Mechanisms of SHP-1 P2 promoter regulation in hematopoietic cells and its silencing in HTLV-1-transformed T cells. J. Leukoc. Biol. 2009, 85:165-174.
36. Ohtani-Fujita N., Dryja T.P., Rapaport J.M., Fujita T., Matsumura S., Ozasa K., Watanabe Y., Hayashi K., Maeda K., Kinoshita S., Matsumura T., Ohnishi Y., Hotta Y., Takahashi R., Kato M.V., Ishizaki K., Sasaki M.S., Horsthemke B., Minoda K., Sakai T. Hypermethylation in the retinoblastoma gene is associated with unilateral, sporadic retinoblastoma. Cancer Genet. Cytogenet. 1997, 98:43-49.
37. Oka T., Yoshino T., Hayashi K., Ohara N., Nakanishi T., Yamaai Y., Hiraki A., Sogawa C.A., Kondo E., Teramoto N., Takahashi K., Tsuchiyama J., Akagi T. Reduction of hematopoietic cell-specific tyrosine phosphatase SHP-1 gene expression in natural killer cell lymphoma and various types of lymphomas/leukemias: combination analysis with cDNA expression array and tissue microarray. Am. J. Pathol. 2001, 159:1495-1505.
38. Oka T., Ouchida M., Koyama M., Ogama Y., Takada S., Nakatani Y., Tanaka T., Yoshino T., Hayashi K., Ohara N., Kondo E., Takahashi K., Tsuchiyama J., Tanimoto M., Shimizu K., Akagi T. Gene silencing of the tyrosine phosphatase SHP1 gene by aberrant methylation in leukemias/lymphomas. Cancer Res. 2002, 62:6390-6394.
39. Pao L.I., Lam K.P., Henderson J.M., Kutok J.L., Alimzhanov M., Nitschke L., Thomas M.L., Neel B.G., Rajewsky K. B cell-specific deletion of protein-tyrosine phosphatase Shp1 promotes B-1a cell development and causes systemic autoimmunity. Immunity 2007, 27:35-48.
40. Pedre X., Mastronardi F., Bruck W., Lopez-Rodas G., Kuhlmann T., Casaccia P. Changed histone acetylation patterns in normal-appearing white matter and early multiple sclerosis lesions. J. Neurosci. 2011, 31:3435-3445.
41. Ruchusatsawat K., Wongpiyabovorn J., Shuangshoti S., Hirankarn N., Mutirangura A. SHP-1 promoter 2 methylation in normal epithelial tissues and demethylation in psoriasis. J. Mol. Med. 2006, 84:175-182.
42. Rush L.J., Plass C. Alterations of DNA methylation in hematologic malignancies. Cancer Lett. 2002, 185:1-12.
43. Sathish J.G., Dolton G., Leroy F.G., Matthews R.J. Loss of Src homology region 2 domain-containing protein tyrosine phosphatase-1 increases CD8+ T cell-APC conjugate formation and is associated with enhanced in vivo CTL function. J. Immunol. 2007, 178:330-337.
44. Stefanova I.I., Hemmer B., Vergelli M., Martin R., Biddison W.E., Germain R.N. TCR ligand discrimination is enforced by competing ERK positive and SHP-1 negative feedback pathways. Nat. Immunol. 2003, 4:248-254.
45. Tost J. DNA methylation: an introduction to the biology and the disease-associated changes of a promising biomarker. Mol. Biotechnol. 2010, 44:71-81.
46. Tsui H.W., Hasselblatt K., Martin A., Mok S.C., Tsui F.W. Molecular mechanisms underlying SHP-1 gene expression. Eur. J. Biochem. 2002, 269:3057-3064.
47. Vaissiere T., Sawan C., Herceg Z. Epigenetic interplay between histone modifications and DNA methylation in gene silencing. Mutat. Res. 2008, 659:40-48.
48. Wlodarski P., Zhang Q., Liu X., Kasprzycka M., Marzec M., Wasik M.A. PU.1 activates transcription of SHP-1 gene in hematopoietic cells. J. Biol. Chem. 2007, 282:6316-6323.
49. Zhang J.Y., Somani A.K., Siminovitch K.A. Roles of the SHP-1 tyrosine phosphatase in the negative regulation of cell signalling. Semin. Immunol. 2000, 12:361-378.
50. Zhang Q., Wang H.Y., Marzec M., Raghunath P.N., Nagasawa T., Wasik M.A. STAT3- and DNA methyltransferase 1-mediated epigenetic silencing of SHP-1 tyrosine phosphatase tumor suppressor gene in malignant T lymphocytes. Proc. Natl. Acad. Sci. U. S. A. 2005, 102:6948-6953.
51. Zhou D., Collins C.A., Wu P., Brown E.J. Protein tyrosine phosphatase SHP-1 positively regulates TLR-induced IL-12p40 production in macrophages through inhibition of phosphatidylinositol 3-kinase. J. Leukoc. Biol. 2010, 87:845-855.