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The Role of NK Cells in the Autoimmune Thyroid Disease-associated Pregnancy Loss

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Abstract

Pregnancy loss is a frequent event. Autoimmune thyroid disorders and altered natural killer (NK) cell functions are two distinct risk factors, which independently could induce adverse pregnancy outcome. Thyroid autoimmunity has been an object of increased attention by investigators in the context of pregnancy loss. Peripheral NK cells and uNK cells comprise distinct cell populations in terms of phenotype and function but they play an important role in the course of a normal human pregnancy via several potential functions. In autoimmune thyroid diseases, several abnormalities of killer cell activity have been described. The functional defects involving NK maturation and/or functional activation observed in Graves’ disease patients could independently influence the reproductive outcome. This suggestion needs extensive investigation and could be important for the therapeutical approach in preventing pregnancy loss in patients with thyroid autoimmunity.

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References

  1. Еdmonds DK, Lindsay KI, Miller JF (1982) Early embryonic mortality in women. Fertil Steril 38:447–453

    Google Scholar 

  2. Baines MG, Gendron RL (1993) Natural and experimental animal models of reproductive faiture. In: Chaouat G (ed) Immunology of pregnancy. CRC Press, Boca Raton, pp 173–203

    Google Scholar 

  3. Alberman E (1988) The epidemiology of repeated abortion. In: Beard RW, Sharp F (eds) Early pregnancy loss: mechanisms and treatment. Springer-Verlag, New York, pp 9–17

    Google Scholar 

  4. Daya S (2002) Habitual abortion. In: Copeland LJ, Jarell JF (eds) Textbook of gynecology, 2nd edn. W.B. Saunders, Philadelphia, pp 227–271

    Google Scholar 

  5. World Health Organization (1977) Recommended definition, terminology and format for statistical tables related to the perinatal period. Acta Obstet Gynecol Scand 56:247–253

    Google Scholar 

  6. Reiss HE (1998) Reproductive medicine: from A to Z. Oxford University Press, Oxford

    Google Scholar 

  7. Li TC, Makris M, Tomsu M, Tuckerman EM, Laird SM (2002) Recurrent miscarriage, aetiology, management and prognosis. Hum Reprod Update 8:463–481

    PubMed  Google Scholar 

  8. Regan L, Rai R (2000) Epidemiology and the medical cause of miscarriage. Bailliere’s Clin Obstet Gynaecol 14:839–854

    Google Scholar 

  9. Clifford K, Rai R, Watson H, Regan L (1994) An informative protocol for the investigation of recurrent miscarriage: preliminary experience of 500 consecutive cases. Hum Reprod 7:1328–1332

    Google Scholar 

  10. Katz VL, Kuller JA (1994) Recurrent miscarriage. Am J Perinatol 11:386–397

    PubMed  Google Scholar 

  11. Stagnaro-Green A, Roman SH, Cobin RH et al (1990) Detection of at-risk pregnancy by means of highly sensitive assays for thyroid autoantibodies. JAMA 264:1422–1425

    PubMed  Google Scholar 

  12. Pratt D, Novotny M, Kaberlein G, Dudkiewicz A, Gleicher N (1993) Antithyroid antibodies and the association with non-organ-specific antibodies in recurrent pregnancy loss. Am J Obstet Gynecol 168:837–841

    PubMed  Google Scholar 

  13. Bussen S, Steck T (1995) Thyroid autoantibodies in euthyroid non-pregnant women with recurrent spontaneous abortions. Hum Reprod 10:2938–2940

    PubMed  Google Scholar 

  14. Bussen SS, Steck T (1997) Thyroid antibodies and their relation to antithrombin antibodies, anticardiolipin antibodies and lupus anticoagulant in women with recurrent spontaneous abortions (antithyroid, anticardiolipin and antithrombin autoantibodies and lupus anticoagulant in habitual aborters). Eur J Obstet Gynecol Reprod Biol 74:139–143

    PubMed  Google Scholar 

  15. Esplin MS, Branch DW, Silver R, Stagnaro-Green A (1998) Thyroid autoantibodies are not associated with recurrent pregnancy loss. Am J Obstet Gynecol 179:1583–1586

    PubMed  Google Scholar 

  16. Kutteh WH, Yetman DL, Carr AC, Beck LA, Scott RT Jr (1999) Increased prevalence of antithyroid antibodies identified in women with recurrent pregnancy loss but not in women undergoing assisted reproduction. Fertil Steril 71:843–848

    PubMed  Google Scholar 

  17. Dendrinos S, Papasteriades C, Tarassi K, Christodoulakos G, Prasinos G, Creatsas G (2000) Thyroid autoimmunity in patients with recurrent spontaneous miscarriages. Gynecol Endocrinol 14:270–274

    PubMed  Google Scholar 

  18. Mecacci F, Parretti E, Cioni R et al (2000) Thyroid autoimmunity and its association with non-organ-specific antibodies and subclinical alterations of thyroid function in women with a history of pregnancy loss or preeclampsia. J Reprod Immunol 46:39–50

    PubMed  Google Scholar 

  19. Bagis T, Gokcel A, Saygili ES (2001) Autoimmune thyroid disease in pregnancy and the postpartum period: relationship to spontaneous abortion. Thyroid 11:1049–1053

    PubMed  Google Scholar 

  20. Glinoer D, Soto MF, Bourdoux P et al (1991) Pregnancy in patients with mild thyroid abnormalities: maternal and neonatal repercussions. J Clin Endocrinol Metab 73:421–427

    PubMed  Google Scholar 

  21. Pratt DE, Kaberlein G, Dudkiewicz A, Karande V, Gleicher N (1993) The association of antithyroid antibodies in euthyroid nonpregnant women with recurrent first trimester abortions in the next pregnancy. Fertil Steril 60:1001–1005

    PubMed  Google Scholar 

  22. Lejeune B, Grun JP, de Nayer P, Servais G, Glinoer D (1993) Antithyroid antibodies underlying thyroid abnormalities and miscarriage or pregnancy induced hypertension. Br J Obstet Gynaecol 100:669–672

    PubMed  Google Scholar 

  23. Singh A, Dantas ZN, Stone SC, Asch RH (1995) Presence of thyroid antibodies in early reproductive failure: biochemical versus clinical pregnancies. Fertil Steril 63:277–281

    PubMed  Google Scholar 

  24. Iijima T, Tada H, Hidaka Y, Mitsuda N, Murata Y, Amino N (1997) Effects of autoantibodies on the course of pregnancy and fetal growth. Obstet Gynecol 90:364–369

    PubMed  Google Scholar 

  25. Kim CH, Chae HD, Kang BM, Chang YS (1998) Influence of antithyroid antibodies in euthyroid women on in vitro fertilization-embryo transfer outcome. Am J Reprod Immunol 40:2–8

    PubMed  Google Scholar 

  26. Muller AF, Verhoeff A, Mantel MJ, Berghout A (1999) Thyroid autoimmunity and abortion: a prospective study in women undergoing in vitro fertilization. Fertil Steril 71:30–34

    PubMed  Google Scholar 

  27. Rushworth FH, Backos M, Rai R, Chilcott IT, Baxter N, Regan L (2000) Prospective pregnancy outcome in untreated recurrent miscarries with thyroid autoantibodies. Hum Reprod 15:1637–1639

    PubMed  Google Scholar 

  28. Poppe K, Glinoer D, Tournaye H et al (2003) Assisted reproduction and thyroid autoimmunity: an unfortunate combination? J Clin Endocrinol Metab 88:4149–4252

    PubMed  Google Scholar 

  29. Prummel MF, Wiersinga WM (2004) Thyroid autoimmunity and miscarriage. Eur J Endocrinol 150:751–755

    PubMed  Google Scholar 

  30. Sandercock P (1989) The odds ratio: a useful tool in neurosciences. J Neurol Neurosurg Psychiatry 52:817–820

    PubMed  Google Scholar 

  31. Iravani AT, Saeedi MM, Pakravesh J, Hamidi S, Abbasi M (2008) Thyroid autoimmunity and recurrent spontaneous abortion in Iran: a case-control study. Endocr Pract 14:458–464

    PubMed  Google Scholar 

  32. Bellver J, Soares SR, Alvarez C et al (2008) The role of thrombophilia and thyroid autoimmunity in unexplained infertility, implantation failure and recurrent spontaneous abortion. Hum Reprod 23:278–284

    PubMed  Google Scholar 

  33. Kilic S, Tasdemir N, Yilmaz N, Yuksel B, Gul A, Batioglu S (2008) The effect of anti-thyroid antibodies on endometrial volume, embryo grade and IVF outcome. Gynecol Endocrinol 24:649–655

    PubMed  Google Scholar 

  34. Stuart AE (1994) Autoantibodies and pregnancy loss. Lancet 343:747–748

    Google Scholar 

  35. Glinoer D (1997) The regulation of thyroid function in pregnancy: pathways of endocrine adaptation from physiology to pathology. Endocr Rev 18:404–433

    PubMed  Google Scholar 

  36. Matalon ST, Blank M, Ornoy A, Shoenfeld Y (2001) The association between anti-thyroid antibodies and pregnancy loss. Am J Reprod Immunol 45:72–77

    PubMed  Google Scholar 

  37. Lazarus JH, Kokandi A (2000) Thyroid disease in relation to pregnancy: a decade of change. Clin Endocrinol 53:265–278

    Google Scholar 

  38. Menken J, Trussell J, Larsen U (1986) Age and infertility. Science 233:1389–1394

    PubMed  Google Scholar 

  39. Matalon ST, Blank M, Levy Y et al (2003) The pathogenic role of anti-thyroglobulin antibody on pregnancy: evidence from an active immunization model in mice. Hum Reprod 18:1094–1099

    PubMed  Google Scholar 

  40. Lee YL, Ng HP, Lau KS et al (2008) Increased fetal abortion rate in autoimmune thyroid disease is related to circulating TPO autoantibodies in an autoimmune thyroiditis animal model. Fertil Steril 91(5 Suppl):2104–2109

    PubMed  Google Scholar 

  41. Wilson R et al (1999) Thyroid antibody titer and avidity in patients with recurrent miscarriage. Fertil Steril 71:558–561

    PubMed  Google Scholar 

  42. Robertson MJ, Ritz J (1990) Biology and clinical relevance of human natural killer cells. Blood 76:2421–2438

    PubMed  Google Scholar 

  43. Cooper MA, Fehniger TA, Caligiuri MA (2001) The biology of human natural killer cell subsets. Trends Immunol 22:633–640

    PubMed  Google Scholar 

  44. Naume B, Johnsen AC, Espevik T, Sundan A (1993) Gene expression and secretion of cytokines and cytokine receptors from highly purified CD56+ natural killer cells stimulated with interleukin-2, interleukin-7 and interleukin-12. Eur J Immunol 23:1831–1838

    PubMed  Google Scholar 

  45. Biassoni R, Ferrini S, Prigione I, Pelak VS, Sekaly RP, Long EO (1991) Activated CD3-CD16+ natural killer cells express a subset of the lymphokine genes induced in activated αß + and γδ + T cells. Scand J Immunol 33:247–252

    PubMed  Google Scholar 

  46. King A, Allan DS, Bowen M et al (2000) HLA-E is expressed on trophoblast and interacts with CD94/NKG2 receptors on decidual NK cells. Eur J Immunol 30:1623–1631

    PubMed  Google Scholar 

  47. Lanier LL (2001) On guard—activating NK cell receptors. Nat Immunol 2:23–27

    PubMed  Google Scholar 

  48. Gregory CD, Lee H, Rees GB, Scott IV, Shah LP, Golding PR (1985) Natural killer cells in normal pregnancy: analysis using monoclonal antibodies and single-cell cytotoxicity assays. Clin Exp Immunol 62:121–127

    PubMed  Google Scholar 

  49. Gregory CD, Lee H, Scott IV, Golding PR (1987) Phenotypic heterogeneity and recycling capacity of natural killer cells in normal human pregnancy. J Reprod Immunol 11:135–145

    PubMed  Google Scholar 

  50. Ponte M et al (1999) Inhibitory receptors sensing HLA-G1 molecules in pregnancy: decidua-associated natural killer cells express LIR-1 and CD94/NKG2A and acquire p49, an HLA-G1-specific receptor. Proc Natl Acad Sci USA 96:5674–5679

    PubMed  Google Scholar 

  51. King A (2000) Uterine leukocytes and decidualization. Hum Reprod Update 6:28–36

    PubMed  Google Scholar 

  52. Jokhi PP, King A, Sharkey AM, Smith SK, Loke YW (1994) Screening for cytokine messenger ribonucleic acids in purified human decidual lymphocyte populations by the reverse-transcriptase polymerase chain reaction. J Immunol 153:4427–4435

    PubMed  Google Scholar 

  53. Saito S et al (1993) Cytokine production by CD16-CD56bright natural killer cells in the human early pregnancy decidua. Int Immunol 5:559–563

    PubMed  Google Scholar 

  54. Koopman LA et al (2003) Human decidual natural killer cells are a unique NK cell subset with immunomodulatory potential. J Exp Med 198:1201–1212

    PubMed  Google Scholar 

  55. Croy BA, Chapeau C (1990) Evaluation of the pregnancy immunotrophism hypothesis by assessment of the reproductive performance of young adult mice of genotype scid/scid.bg/bg. J Reprod Fertil 88:231–239

    PubMed  Google Scholar 

  56. Curran EM, Berghaus LJ, Vernetti NJ, Saporita AJ, Lubahn DB, Estes DM (2001) Natural killer cells express estrogen receptor- and estrogen receptor-ß and can respond to estrogen via a non-estrogen receptor-α-mediated pathway. Cell Immunol 214:12–20

    PubMed  Google Scholar 

  57. Henderson TA, Saunders PT, Moffett-King A, Groome NP, Critchley HO (2003) Steroid receptor expression in uterine natural killer cells. J Clin Endocrinol Metab 88:440–449

    PubMed  Google Scholar 

  58. Ehring GR et al (1998) A nongenomic mechanism for progesterone-mediated immunosuppression: inhibition of K + channels, Ca2+ signaling, and gene expression in T lymphocytes. J Exp Med 188:1593–1602

    PubMed  Google Scholar 

  59. Inoue T et al (1996) Progesterone stimulates the induction of human endometrial CD56+ lymphocytes in an in vitro culture system. J Clin Endocrinol Metab 81:1502–1507

    PubMed  Google Scholar 

  60. Seppala M, Taylor RN, Koistinen H, Koistinen R, Milgrom E (2002) Glycodelin: a major lipocalin protein of the reproductive axis with diverse actions in cell recognition and differentiation. Endocr Rev 23:401–430

    PubMed  Google Scholar 

  61. Verma S, Hiby SE, Loke YW, King A (2000) Human decidual natural killer cells express the receptor for and respond to the cytokine interleukin 15. Biol Reprod 62:959–968

    PubMed  Google Scholar 

  62. Kitaya K, Nakayama T, Okubo T, Kuroboshi H, Fushiki S, Honjo H (2003) Expression of macrophage inflammatory protein-1ß in human endometrium: its role in endometrial recruitment of natural killer cells. J Clin Endocrinol Metab 88:1809–1814

    PubMed  Google Scholar 

  63. Ntrivalas EI et al (2001) Status of peripheral blood natural killer cells in women with recurrent spontaneous abortions and infertility of unknown aetiology. Hum Reprod 16:855–861

    PubMed  Google Scholar 

  64. Aoki K et al (1995) Preconceptional natural killer cell activity as a predictor of miscarriage. Lancet 345:1340–1342

    PubMed  Google Scholar 

  65. Emmer PM, Nelen WL, Steegers EA, Hendriks JC, Veerhoek M, Joosten I (2000) Peripheral natural killer cytotoxicity and CD56(pos)CD16(pos) cells increase during early pregnancy in women with a history of recurrent spontaneous abortion. Hum Reprod 15:1163–1169

    PubMed  Google Scholar 

  66. Shimada S et al (2004) No difference in natural killer or natural killer T-cell population, but aberrant T-helper cell population in the endometrium of women with repeated miscarriage. Hum Reprod 19:1018–1024

    PubMed  Google Scholar 

  67. Lachapelle MH, Miron P, Hemmings R, Roy DC (1996) Endometrial T, B, and NK cells in patients with recurrent spontaneous abortion. Altered profile and pregnancy outcome. J Immunol 156:4027–4034

    PubMed  Google Scholar 

  68. Clifford K, Flanagan AM, Regan L (1999) Endometrial CD56+ natural killer cells in women with recurrent miscarriage: a histomorphometric study. Hum Reprod 14:2727–2730

    PubMed  Google Scholar 

  69. Quenby S et al (1999) Pre-implantation endometrial leukocytes in women with recurrent miscarriage. Hum Reprod 14:2386–2391

    PubMed  Google Scholar 

  70. Michimata T et al (2002) Distributions of endometrial NK cells, B cells, T cells, and Th2/Tc2 cells fail to predict pregnancy outcome following recurrent abortion. Am J Reprod Immunol 47:196–202

    PubMed  Google Scholar 

  71. Trinchieri G, Kobayashi M, Seehra J, London L, Perussia B (1984) Response of resting human peripheral blood natural killer cells to interleukin 2. J Exp Med 160:1147–1169

    PubMed  Google Scholar 

  72. Baxter AG, Smyth MJ (2002) The role of NK cells in autoimmune disease. Autoimmunity 35:1–14

    PubMed  Google Scholar 

  73. Flodstrom M, Shi FD, Sarvetnick N, Ljunggren HG (2002) The natural killer cell—friend or foe in autoimmune disease? Scand J Immunol 55:432–441

    PubMed  Google Scholar 

  74. Hauser SL, Ault US, Levin MJ, Garovoy MR, Weiner HL (1981) Natural killer cell activity in multiple sclerosis. J Immunol 127:1114–1117

    PubMed  Google Scholar 

  75. Auer IO, Ziemer E, Sommer H (1980) Immune status in Crohn’s disease. Clin Exp Immunol 42:41–47

    PubMed  Google Scholar 

  76. Goto M, Tanimoto K, Chihara T, Horiuchi Y (1981) Natural cell-mediated cytotoxicity in Sjogren’s syndrome and rheumatoid arthritis. Arthritis Rheum 24:1377–1382

    PubMed  Google Scholar 

  77. Yabuhara A et al (1996) A killing defect of natural killer cells as an underlying immunological abnormality in childhood systemic lupus erythematosus. J Rheumatol 23:171–177

    PubMed  Google Scholar 

  78. Smith EM, Phan M, Kruger TE, Coppenhaver DH, Blalock JE (1982) Human lymphocyte production of immunoreactive thyrotropin. Proc Natl Acad Sci USA 80:6010–6013

    Google Scholar 

  79. Kruger TE, Blalock JE (1986) Cellular requirements for thyrotropin enhancement of in vitro antibody production. J Immunol 137:197–200

    PubMed  Google Scholar 

  80. Kruger TE, Smith EM, Harbour DV, Blalock JE (1989) Thyrotropin: an endogenous regulator of the in vitro immune response. J Immunol 142:744–747

    PubMed  Google Scholar 

  81. Bagriacik EU, Zhou Q, Wang H-C, Klein J (2001) Rapid and transient reduction in circulating thyroid hormones following systemic antigen priming: implications for functional collaboration between dendritic cells and thyroid. Cell Immunol 212:92–100

    PubMed  Google Scholar 

  82. Klein JR, Wang H-C (2004) Characterization of a novel set of resident intrathyroidal bone marrow-derived hematopoietic cells: potential for immune-endocrine interactions in thyroid homeostasis. J Exp Biol 207:55–65

    PubMed  Google Scholar 

  83. Wang H-C, Dragoo J, Zhou Q, Klein JR (2003) An intrinsic thyrotropin-mediated pathway of TNF-α production by bone marrow cells. Blood 101:119–123

    PubMed  Google Scholar 

  84. Zhou Q, Wang H-C, Klein JR (2002) Characterization of a novel anti-mouse thyrotropin monoclonal antibody. Hybrid Hybridomics 21:75–79

    PubMed  Google Scholar 

  85. Scofield VL, Montufar-Solis D, Cheng E, Estes MK, Klein JR (2005) Intestinal TSH production is localized in villus “hotblocks” and is coupled to IL-7 production: evidence for involvement of TSH during acute virus infection. Immunol Lett 99:36–44

    PubMed  Google Scholar 

  86. Klein JR (2006) The immune system as a regulator of thyroid hormone activity. Exp Biol Med 231:229–236

    Google Scholar 

  87. Coutelier JP, Kehrl JH, Bellur SS, Kohn LD, Notkins AL, Prabhakar BS (1990) Binding and functional effects of thyroid stimulating hormone to human immune cells. J Clin Immunol 10:204–210

    PubMed  Google Scholar 

  88. Bagriacik EU, Klein JR (2000) The thyrotropin (thyroid stimulating hormone) receptor is expressed on murine dendritic cells and on a subset of CD43RBhigh lymph node T cells: functional role of thyroid stimulating hormone during immune activation. J Immunol 164:6158–6165

    PubMed  Google Scholar 

  89. Kruger TE (1996) Immunomodulation of peripheral lymphocytes by hormones of the hypothalamus-pituitary-thyroid axis. Adv Neuroimmunol 6:387–395

    PubMed  Google Scholar 

  90. Fabris N, Mochegiani E, Provinciali M (1995) Pituitary-thyroid axis and immune system: a reciprocal neuroendocrine-immune interaction. Horm Res 43:29–38

    PubMed  Google Scholar 

  91. Provinciali M, Di Stefano G, Fabris N (1992) Improvement in the proliferative capacity and natural killer cell activity of murine spleen lymphocytes by thyrotropin. Int J Immunopharmacol 14:865–870

    PubMed  Google Scholar 

  92. Migita K et al (1989) Cytotoxic activity of interleukin-2 (Il-2) activated killer cells toward thyroid epithelial cells. Clin Exp Immunol 77:196–201

    PubMed  Google Scholar 

  93. Atkins MB, Mier JW, Parkinson DR, Gould JA, Berkman EM, Kaplan MM (1988) Hypothyroidism after treatment with interleukin-2 and lymphokine-activated killer cells. N Engl J Med 318(24):1557–1563

    PubMed  Google Scholar 

  94. Benhadi N, Wiersinga WM, Reitsma JB, Vrijkotte TG, Bonsel GJ (2009) Higher maternal TSH levels in pregnancy are associated with increased risk for miscarriage, fetal or neonatal death. Eur J Endocrinol 160(6):985–991

    PubMed  Google Scholar 

  95. Elizabeth N (2008) Association of first trimester thyroid function test values with thyroperoxidase antibody status, smoking, and multi-vitamin use. Endocr Pract 14(1):33–39

    Google Scholar 

  96. Stagnaro-Green A, Roman SH, Cobin RH, el-Harazy E, Wallenstein S, Davies TF (1992) A prospective study of lymphocyte-initiated immunosuppression in normal pregnancy: evidence of a T-cell etiology for postpartum thyroid dysfunction. J Clin Endocrinol Metab 74:645–653

    PubMed  Google Scholar 

  97. Casey BM, Dashe JS, Wells CE et al (2005) Subclinical hypothyroidism and pregnancy outcomes. Obstet Gynecol 105(2):239–245

    PubMed  Google Scholar 

  98. Spencer C, Lee R, Kazarosyan M et al (2005) Thyroid reference ranges in pregnancy: studies on an iodine sufficient cohort. Thyroid 15(1):1–16

    Google Scholar 

  99. Glinoer D, Riahi M, Grün JP, Kinthaert J (1994) Risk of subclinical hypothyroidism in pregnant women with asymptomatic autoimmune thyroid disorders. J Clin Endocrinol Metab 79:197–204

    PubMed  Google Scholar 

  100. Abalovich M, Gutierrez S, Alcaraz G, Maccallini G, Garcia A, Levalle O (2002) Overt and subclinical hypothyroidism complicating pregnancy. Thyroid 12:63–68

    PubMed  Google Scholar 

  101. Negro R (2006) Levothyroxine treatment in euthyroid pregnant women with autoimmune thyroid disease: effects on obstetrical complications. J Clin Endocrinol Metabol 91(7):2587–2591

    Google Scholar 

  102. Amino N et al (1982) Peripheral K lymphocytes in autoimmune thyroid disease: decrease in Graves’ disease and increase in Hashimoto’s disease. J Clin Endocrinol Metab 54:587–591

    PubMed  Google Scholar 

  103. Sawada K, Saturami T, Imura H, Iwamori M, Nabai Y (1980) Anti-asialo-GMI antibody in sera from patients with Graves’ disease and Hashimoto’s thyroiditis [letter]. Lancet 2:198

    PubMed  Google Scholar 

  104. Papic M, Stein-Streilein J, Zakarija M, McKenzie JM, Guffee J, Fletcher MA (1987) Suppression of peripheral blood natural killer cell activity by excess thyroid hormone. J Clin Invest 79:404–408

    PubMed  Google Scholar 

  105. Wang PW, Luo SF, Huang BY, Lin JD, Huang MJ (1988) Depressed natural killer cell activity in Graves’ disease and during antithyroid medication. Clin Endocrinol 28:205–214

    Google Scholar 

  106. Marazuela M, Vargas JA, Alvarez-Mon M, Albarran F, Lucas T, Durantez A (1995) Impaired natural killer cell cytotoxicity in peripheral blood mononuclear cells in Graves’ disease. Eur J Endocrinol 132:175–180

    PubMed  Google Scholar 

  107. Calder EA, Irvine WJ, Davidson NM, Wu FT (1976) B and K cells in autoimmune thyroid disease. Clin Exp Immunol 25:17–23

    PubMed  Google Scholar 

  108. Tezuka H et al (1988) Natural killer and natural killer-like activity of peripheral blood and intrathyroidal mononuclear cells from patients with Graves’ disease. J Clin Endocrinol Metabol 66:702–707

    Google Scholar 

  109. Pedersen BK, Feldt-Rasmussen U, Bech K, Perrild H, Klarlund K, Hoier-Madsen M (1989) Characterization of the natural killer activity in Hashimoto’s and Graves’ diseases. Allergy 44:477–481

    PubMed  Google Scholar 

  110. Pruzanski W, Capes H, Baur R, Wenzel BE, Row VV, Volpe R (1984) Biological activity of lymphocytotoxic antibodies in Graves’ disease and Hashimoto’s thyroiditis. J Endocrinol Invest 7:7–13

    PubMed  Google Scholar 

  111. Hidaka Y et al (1992) Increase in peripheral natural killer cell activity in patients with autoimmune thyroid disease. Autoimmunity 11:239–246

    PubMed  Google Scholar 

  112. Wenzel BE, Chow A, Baur R, Schleusener H, Wall JR (1998) Natural killer cell activity in patients with Graves’ disease and Hashimoto’s thyroiditis. Thyroid 8:1019–1022

    PubMed  Google Scholar 

  113. Solerte SB (2005) Defect of a subpopulation of natural killer immune cells in Graves' disease and Hashimoto's thyroiditis: normalizing effect of dehydroepiandrosterone sulfate. Eur J Endocrinol 152:703–712

    PubMed  Google Scholar 

  114. Solovera J, Alverez-Mon M, Casas J, Carballido J, Durantez A (1987) Inhibition of human natural killer (NK) activity by calcium channel modulators and a calmodulin antagonist. J Immunol 139:876–880

    PubMed  Google Scholar 

  115. Weetman AP, Gunn C, Hall R, McGregor AM (1985) The absence of any effect of methimazole on in vitro cell-mediated cytotoxicity. Clin Endocrinol 22:57–64

    Google Scholar 

  116. Solerte SB, Cravello L, Ferrari E, Fioravanti M (2000) Overproduction of IFN-γ and TNF-α from natural killer (NK) cells is associated with abnormal NK reactivity and cognitive derangement in Alzheimer’s disease. Ann NY Acad Sci 917:331–340

    PubMed  Google Scholar 

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    Emiliana Konova

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Konova, E. The Role of NK Cells in the Autoimmune Thyroid Disease-associated Pregnancy Loss. Clinic Rev Allerg Immunol 39, 176–184 (2010). https://doi.org/10.1007/s12016-010-8201-7

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