Expression of Natural Cytotoxicity Receptors on and Intracellular Cytokine Production by NK Cells in Women with Gestational Diabetes Mellitus

American Journal of Reproductive Immunology

Volumn 75, Issue 5, 2016, Pages 529-538

  Chiba, Hitomi ^a   Fukui, Atsushi ^a   Fuchinoue, Kohei ^a   Funamizu, Ayano ^a   Tanaka, Kanji ^a   Mizunuma, Hideki ^a  

^a HIROSAKI UNIVERSITY   (Japan)

Author keywords

IFN ; Peripheral blood NK cells; TGF ; TNF ; VEGF

Indexed keywords

CD16 ANTIGEN; CD56 ANTIGEN; CYTOKINE; GAMMA INTERFERON; NATURAL CYTOTOXICITY TRIGGERING RECEPTOR 1; NATURAL CYTOTOXICITY TRIGGERING RECEPTOR 3; NATURAL KILLER CELL RECEPTOR; TRANSFORMING GROWTH FACTOR BETA; TUMOR NECROSIS FACTOR ALPHA; VASCULOTROPIN; DIFFERENTIATION ANTIGEN;

ADULT; ARTICLE; CELL SURFACE; CLINICAL ARTICLE; CONTROLLED STUDY; CYTOKINE PRODUCTION; FEMALE; FLOW CYTOMETRY; HUMAN; HUMAN CELL; IMPAIRED GLUCOSE TOLERANCE; INTRACELLULAR SPACE; NATURAL KILLER CELL; PREGNANCY DIABETES MELLITUS; PRIORITY JOURNAL; PROSPECTIVE STUDY; PROTEIN EXPRESSION; BLOOD CELL; CELL SEPARATION; CYTOTOXICITY; IMMUNOLOGY; METABOLISM; PREGNANCY;

ADULT; ANTIGENS, DIFFERENTIATION; BLOOD CELLS; CELL SEPARATION; CYTOKINES; CYTOTOXICITY, IMMUNOLOGIC; DIABETES, GESTATIONAL; FEMALE; FLOW CYTOMETRY; HUMANS; KILLER CELLS, NATURAL; PREGNANCY;

EID: 84956678229     PISSN: 10467408     EISSN: 16000897     Source Type: Journal    
DOI: 10.1111/aji.12491     Document Type: Article

References (64)

1. Bulmer JN, Williams PJ, Lash GE: Immune cells in the placental bed. Int J Dev Biol 2010; 54:281-294.
2. King A, Balendran N, Wooding P, Carter NP, Loke YW: CD3- leukocytes present in the human uterus during early placentation: phenotypic and morphologic characterization of the CD56++ population. Dev Immunol 1991; 1:169-190.
3. Whitelaw PF, Croy BA: Granulated lymphocytes of pregnancy. Placenta 1996; 17:533-543.
4. Robson A, Harris LK, Innes BA, Lash GE, Aljunaidy MM, Aplin JD, Baker PN, Robson SC, Bulmer JN: Uterine natural killer cells initiate spiral artery remodeling in human pregnancy. FASEB J 2012; 26:4876-4885.
5. Hanna J, Goldman-Wohl D, Hamani Y, Avraham I, Greenfield C, Natanson-Yaron S, Prus D, Cohen-Daniel L, Arnon TI, Manaster I, Gazit R, Yutkin V, Benharroch D, Porgador A, Keshet E, Yagel S, Mandelboim O: Decidual NK cells regulate key developmental processes at the human fetal-maternal interface. Nat Med 2006; 12:1065-1074.
6. Lash GE, Robson SC, Bulmer JN: Review: functional role of uterine natural killer (uNK) cells in human early pregnancy decidua. Placenta 2010; 31(Suppl):S87-S92.
7. Acar N, Ustunel I, Demir R: Uterine natural killer (uNK) cells and their missions during pregnancy: a review. Acta Histochem 2011; 113:82-91.
8. Burton GJ, Jauniaux E, Watson AL: Maternal arterial connections to the placental intervillous space during the first trimester of human pregnancy: the Boyd collection revisited. Am J Obstet Gynecol 1999; 181:718-724.
9. Caniggia I, Winter J, Lye SJ, Post M: Oxygen and placental development during the first trimester: implications for the pathophysiology of pre-eclampsia. Placenta 2000; 21(Suppl A):S25-S30.
10. Guibourdenche J, Fournier T, Malassine A, Evain-Brion D: Development and hormonal functions of the human placenta. Folia Histochem Cytobiol 2009; 47:S35-S40.
11. Fukui A, Funamizu A, Yokota M, Yamada K, Nakamua R, Fukuhara R, Kimura H, Mizunuma H: Uterine and circulating natural killer cells and their roles in women with recurrent pregnancy loss, implantation failure and preeclampsia. J Reprod Immunol 2011; 90:105-110.
12. Fukui A, Kwak-Kim J, Ntrivalas E, Gilman-Sachs A, Lee SK, Beaman K: Intracellular cytokine expression of peripheral blood natural killer cell subsets in women with recurrent spontaneous abortions and implantation failures. Fertil Steril 2008; 89:157-165.
13. Fukui A, Ntrivalas E, Fukuhara R, Fujii S, Mizunuma H, Gilman-Sachs A, Beaman K, Kwak-Kim J: Correlation between natural cytotoxicity receptors and intracellular cytokine expression of peripheral blood NK cells in women with recurrent pregnancy losses and implantation failures. Am J Reprod Immunol 2009; 62:371-380.
14. Fukui A, Ntrivalas E, Gilman-Sachs A, Kwak-Kim J, Lee SK, Levine R, Beaman K: Expression of natural cytotoxicity receptors and a2V-ATPase on peripheral blood NK cell subsets in women with recurrent spontaneous abortions and implantation failures. Am J Reprod Immunol 2006; 56:312-320.
15. Fukui A, Yokota M, Funamizu A, Nakamua R, Fukuhara R, Yamada K, Kimura H, Fukuyama A, Kamoi M, Tanaka K, Mizunuma H: Changes of NK cells in preeclampsia. Am J Reprod Immunol 2012; 67:278-286.
16. Ategbo JM, Grissa O, Yessoufou A, Hichami A, Dramane KL, Moutairou K, Miled A, Grissa A, Jerbi M, Tabka Z, Khan NA: Modulation of adipokines and cytokines in gestational diabetes and macrosomia. J Clin Endocrinol Metab 2006; 91:4137-4143.
17. Xu J, Zhao YH, Chen YP, Yuan XL, Wang J, Zhu H, Lu CM: Maternal circulating concentrations of tumor necrosis factor-alpha, leptin, and adiponectin in gestational diabetes mellitus: a systematic review and meta-analysis. ScientificWorldJournal 2014; 2014:926932.
18. Coughlan MT, Oliva K, Georgiou HM, Permezel JM, Rice GE: Glucose-induced release of tumour necrosis factor-alpha from human placental and adipose tissues in gestational diabetes mellitus. Diabet Med 2001; 18:921-927.
19. Kirwan JP, Hauguel-De Mouzon S, Lepercq J, Challier JC, Huston-Presley L, Friedman JE, Kalhan SC, Catalano PM: TNF-alpha is a predictor of insulin resistance in human pregnancy. Diabetes 2002; 51:2207-2213.
20. Pantham P, Aye IL, Powell TL: Inflammation in maternal obesity and gestational diabetes mellitus. Placenta 2015; 36:709-715.
21. Minakami H, Maeda T, Fujii T, Hamada H, Iitsuka Y, Itakura A, Itoh H, Iwashita M, Kanagawa T, Kanai M, Kasuga Y, Kawabata M, Kobayashi K, Kotani T, Kudo Y, Makino Y, Matsubara S, Matsuda H, Miura K, Murakoshi T, Murotsuki J, Ohkuchi A, Ohno Y, Ohshiba Y, Satoh S, Sekizawa A, Sugiura M, Suzuki S, Takahashi T, Tsukahara Y, Unno N, Yoshikawa H: Guidelines for obstetrical practice in Japan: Japan Society of Obstetrics and Gynecology (JSOG) and Japan Association of Obstetricians and Gynecologists (JAOG) 2014 edition. J Obstet Gynaecol Res 2014; 40:1469-1499.
22. Metzger BE, Gabbe SG, Persson B, Buchanan TA, Catalano PA, Damm P, Dyer AR, Leiva A, Hod M, Kitzmiler JL, Lowe LP, McIntyre HD, Oats JJ, Omori Y, Schmidt MI: International association of diabetes and pregnancy study groups recommendations on the diagnosis and classification of hyperglycemia in pregnancy. Diabetes Care 2010; 33:676-682.
23. Minakami H, Maeda T, Fujii T, Hamada H, Iitsuka Y, Itakura A, Itoh H, Iwashita M, Kanagawa T, Kanai M, Kasuga Y, Kawabata M, Kobayashi K, Kotani T, Kudo Y, Makino Y, Matsubara S, Matsuda H, Miura K, Murakoshi T, Murotsuki J, Ohkuchi A, Ohno Y, Ohshiba Y, Satoh S, Sekizawa A, Sugiura M, Suzuki S, Takahashi T, Tsukahara Y, Unno N, Yoshikawa H: How should patients with hyperglycemic disorders during pregnancy be screened? In Guidelines for obstetrical practice in Japan: Japan Society of Obstetrics and Gynecology (JSOG) and Japan Association of Obstetricians and Gynecologists (JAOG) 2014 edition. 1 edn, H Minakami (ed.) Tokyo, Japan, Japan Society of Obstetrics and Gynecology (JSOG), 2014; pp. 19-23.
24. Van Ryswyk E, Middleton P, Shute E, Hague W, Crowther C: Women's views and knowledge regarding healthcare seeking for gestational diabetes in the postpartum period: a systematic review of qualitative/survey studies. Diabetes Res Clin Pract 2015; 110:109-122.
25. Kampmann U, Madsen LR, Skajaa GO, Iversen DS, Moeller N, Ovesen P: Gestational diabetes: a clinical update. World J Diabetes 2015; 6:1065-1072.
26. Papadopoulou A, Lynch KF, Anderberg E, Landin-Olsson M, Hansson I, Agardh CD, Lernmark A, Berntorp K: HLA-DQB1 genotypes and islet cell autoantibodies against GAD65 and IA-2 in relation to development of diabetes post partum in women with gestational diabetes mellitus. Diabetes Res Clin Pract 2012; 95:260-264.
27. Nilsson C, Ursing D, Torn C, Aberg A, Landin-Olsson M: Presence of GAD antibodies during gestational diabetes mellitus predicts type 1 diabetes. Diabetes Care 2007; 30:1968-1971.
28. Lapolla A, Betterle C, Sanzari M, Zanchetta R, Pfeifer E, Businaro A, Fagiolo U, Plebani M, Marini S, Photiou E, Fedele D: An immunological and genetic study of patients with gestational diabetes mellitus. Acta Diabetol 1996; 33:139-144.
29. Lotfy M, Adeghate J, Kalasz H, Singh J, Adeghate E: Chronic complications of diabetes mellitus: a mini review. Curr Diabetes Rev 2015; 12:1-8.
30. Berrou J, Fougeray S, Venot M, Chardiny V, Gautier JF, Dulphy N, Toubert A, Peraldi MN: Natural killer cell function, an important target for infection and tumor protection, is impaired in type 2 diabetes. PLoS One 2013; 8:e62418.
31. Burke SD, Dong H, Hazan AD, Croy BA: Aberrant endometrial features of pregnancy in diabetic NOD mice. Diabetes 2007; 56:2919-2926.
32. Dotta F, Fondelli C, Falorni A: Can NK cells be a therapeutic target in human type 1 diabetes? Eur J Immunol 2008; 38:2961-2963.
33. Enk J, Mandelboim O: The role of natural cytotoxicity receptors in various pathologies: emphasis on type I diabetes. Front Immunol 2014; 5:4.
34. Fidan I, Yuksel S, Kalkanci A, Imir T, Kustimur S: Evaluation of the natural killer cytotoxicity and the levels of cytokines in rats with type I diabetes mellitus. Mem Inst Oswaldo Cruz 2005; 100:883-887.
35. Flodstrom M, Maday A, Balakrishna D, Cleary MM, Yoshimura A, Sarvetnick N: Target cell defense prevents the development of diabetes after viral infection. Nat Immunol 2002; 3:373-382.
36. Guo H, Xu B, Gao L, Sun X, Qu X, Li X, Liu S, Feng J, Wang J, Tang Y, Yan G, Gao X, Jiang Y: High frequency of activated natural killer and natural killer T-cells in patients with new onset of type 2 diabetes mellitus. Exp Biol Med (Maywood) 2012; 237:556-562.
37. Gur C, Porgador A, Elboim M, Gazit R, Mizrahi S, Stern-Ginossar N, Achdout H, Ghadially H, Dor Y, Nir T, Doviner V, Hershkovitz O, Mendelson M, Naparstek Y, Mandelboim O: The activating receptor NKp46 is essential for the development of type 1 diabetes. Nat Immunol 2010; 11:121-128.
38. Hayashi T, Morimoto M, Iwata H, Onodera T: Interferon-gamma plays a role in pancreatic islet-cell destruction of reovirus type 2-induced diabetes-like syndrome in DBA/1 suckling mice. Int J Exp Pathol 1998; 79:313-320.
39. Johansson SE, Hall H, Bjorklund J, Hoglund P: Broadly impaired NK cell function in non-obese diabetic mice is partially restored by NK cell activation in vivo and by IL-12/IL-18 in vitro. Int Immunol 2004; 16:1-11.
40. Li M, Song LJ, Qin XY: Advances in the cellular immunological pathogenesis of type 1 diabetes. J Cell Mol Med 2014; 18:749-758.
41. Lindehammer SR, Fex M, Maziarz M, Hanson I, Marsal K, Lernmark A: Early-pregnancy cytokines in mothers to children developing multiple, persistent islet autoantibodies, type 1 diabetes, or both before 7 years of age. Am J Reprod Immunol 2011; 66:495-503.
42. Lo HC, Lin SC, Wang YM: The relationship among serum cytokines, chemokine, nitric oxide, and leptin in children with type 1 diabetes mellitus. Clin Biochem 2004; 37:666-672.
43. Lorini R, Moretta A, Valtorta A, d'Annunzio G, Cortona L, Vitali L, Bozzola M, Severi F: Cytotoxic activity in children with insulin-dependent diabetes mellitus. Diabetes Res Clin Pract 1994; 23:37-42.
44. Matyszewski A, Czarnecka AM, Solarek W, Korzen P, Safir IJ, Kukwa W, Szczylik C: Molecular basis of carcinogenesis in diabetic patients (review). Int J Oncol 2015; 46:1435-1443.
45. Piatkiewicz P, Milek T, Bernat-Karpinska M, Ohams M, Czech A, Ciostek P: The dysfunction of NK cells in patients with type 2 diabetes and colon cancer. Arch Immunol Ther Exp (Warsz) 2013; 61:245-253.
46. Rodacki M, Svoren B, Butty V, Besse W, Laffel L, Benoist C, Mathis D: Altered natural killer cells in type 1 diabetic patients. Diabetes 2007; 56:177-185.
47. Schloot NC, Hanifi-Moghaddam P, Goebel C, Shatavi SV, Flohe S, Kolb H, Rothe H: Serum IFN-gamma and IL-10 levels are associated with disease progression in non-obese diabetic mice. Diabetes Metab Res Rev 2002; 18:64-70.
48. Zhang QL, Zang SF: Correlation of T lymphocyte subsets with blood glucose level and the first-phase insulin secretion in patients with type 2 diabetes mellitus. Zhongguo Yi Xue Ke Xue Yuan Xue Bao 2012; 34:254-257.
49. Hotamisligil GS: Inflammation and metabolic disorders. Nature 2006; 444:860-867.
50. Yamada H, Kato EH, Kobashi G, Ebina Y, Shimada S, Morikawa M, Sakuragi N, Fujimoto S: High NK cell activity in early pregnancy correlates with subsequent abortion with normal chromosomes in women with recurrent abortion. Am J Reprod Immunol 2001; 46:132-136.
51. Orange JS, Ballas ZK: Natural killer cells in human health and disease. Clin Immunol 2006; 118:1-10.
52. Rodacki M, Milech A, de Oliveira JE: NK cells and type 1 diabetes. Clin Dev Immunol 2006; 13:101-107.
53. Ibarra Urizar A, Friberg J, Christensen DP, Lund Christensen G, Billestrup N: Inflammatory cytokines stimulate bone morphogenetic protein-2 expression and release from pancreatic beta cells. J Interferon Cytokine Res 2015; 36:20-29, doi: 10.1089/jir.2014.0199.
54. Swaroop JJ, Rajarajeswari D, Naidu JN: Association of TNF-alpha with insulin resistance in type 2 diabetes mellitus. Indian J Med Res 2012; 135:127-130.
55. Semenchenko I, Sharafetdinov K, Plotnikova OA, Alekseeva RI, Sentsova TB, Vorozhko IV: [Markers of immune inflammation in patients with type 2 diabetes and obesity]. Vopr Pitan 2013; 82:46-50.
56. Ayatollahi M, Geramizadeh B, Samsami A: Transforming growth factor beta-1 influence on fetal allografts during pregnancy. Transpl Proc 2005; 37:4603-4604.
57. Ibrahim S, Rashed L: Estimation of transforming growth factor-beta 1 as a marker of renal injury in type II diabetes mellitus. Saudi Med J 2007; 28:519-523.
58. Hosomi N, Noma T, Ohyama H, Takahashi T, Kohno M: Vascular proliferation and transforming growth factor-beta expression in pre- and early stage of diabetes mellitus in Otsuka Long-Evans Tokushima fatty rats. Atherosclerosis 2002; 162:69-76.
59. Molvarec A, Ito M, Shima T, Yoneda S, Toldi G, Stenczer B, Vasarhelyi B, Rigo Jr J, Saito S: Decreased proportion of peripheral blood vascular endothelial growth factor-expressing T and natural killer cells in preeclampsia. Am J Obstet Gynecol 2010; 203:567.e561-568.
60. Ruszkowska-Ciastek B, Sokup A, Wernik T, Rhone P, Goralczyk K, Bielawski K, Fijalkowska A, Nowakowska A, Rhone E, Rosc D: Low-grade risk of hypercoagulable state in patients suffering from diabetes mellitus type 2. J Zhejiang Univ Sci B 2015; 16:788-795.
61. Kubisz P, Chudy P, Stasko J, Galajda P, Holly P, Vysehradsky R, Mokan M: Circulating vascular endothelial growth factor in the normo- and/or microalbuminuric patients with type 2 diabetes mellitus. Acta Diabetol 2010; 47:119-124.
62. Tsuda H, Sakai M, Michimata T, Tanebe K, Hayakawa S, Saito S: Characterization of NKT cells in human peripheral blood and decidual lymphocytes. Am J Reprod Immunol 2001; 45:295-302.
63. Burke SD, Seaward AV, Ramshaw H, Smith GN, Virani S, Croy BA, Lima PD: Homing receptor expression is deviated on CD56+ blood lymphocytes during pregnancy in Type 1 diabetic women. PLoS One 2015; 10:e0119526.
64. Lee PT, Putnam A, Benlagha K, Teyton L, Gottlieb PA, Bendelac A: Testing the NKT cell hypothesis of human IDDM pathogenesis. J Clin Investig 2002; 110:793-800.