An increased population of regulatory T cells improves the pathophysiology of placental ischemia in a rat model of preeclampsia

American Journal of Physiology - Regulatory Integrative and Comparative Physiology

Volumn 309, Issue 8, 2015, Pages R884-R891

  Cornelius, Denise C ^a   Amaral, Lorena M ^a   Harmon, Ashlyn ^a   Wallace, Kedra ^a   Thomas, Alexia J ^a   Campbell, Nathan ^a   Scott, Jeremy ^a   Herse, Florian ^b   Haase, Nadine ^b   Moseley, Janae ^a   Wallukat, Gerd ^b   Dechend, Ralf ^b   LaMarca, Babbette ^a  

^a UNIVERSITY OF MISSISSIPPI SCHOOL OF MEDICINE   (United States)

^b CHARITÉ UNIVERSITÄTSMEDIZIN BERLIN   (Germany)

Author keywords

Hypertension; Inflammation; Oxidative stress; Pregnancy; Regulatory T cells

Indexed keywords

INTERLEUKIN 10; INTERLEUKIN 6; REACTIVE OXYGEN METABOLITE; TUMOR NECROSIS FACTOR ALPHA; CYTOKINE; ENDOTHELIN 1; MESSENGER RNA;

ADOPTIVE TRANSFER; ANALYSIS OF VARIANCE; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BLOOD SAMPLING; CD4+ CD25+ T LYMPHOCYTE; CELL ISOLATION; CONTROLLED STUDY; CYTOKINE PRODUCTION; DISEASE ASSOCIATION; ELEVATED BLOOD PRESSURE; FEMALE; GESTATIONAL AGE; HEART BEAT; IN VITRO STUDY; IN VIVO STUDY; INTRAUTERINE PRESSURE; KIDNEY; KIDNEY CORTEX; MEAN ARTERIAL PRESSURE; NONHUMAN; PATHOPHYSIOLOGY; PERFUSION PRESSURE; PLACENTA; PLACENTA INSUFFICIENCY; PREECLAMPSIA; PREGNANCY; PRIORITY JOURNAL; RAT; REDUCED UTERINE PERFUSION PRESSURE; REGULATORY T LYMPHOCYTE; SPLEEN; STATISTICAL ANALYSIS; T LYMPHOCYTE SUBPOPULATION; ANIMAL; BLOOD PRESSURE; CYTOLOGY; GENE EXPRESSION REGULATION; GENETICS; ISCHEMIA; METABOLISM; PATHOLOGY; PHYSIOLOGY; SPRAGUE DAWLEY RAT; VASCULARIZATION;

ADOPTIVE TRANSFER; ANIMALS; BLOOD PRESSURE; CYTOKINES; ENDOTHELIN-1; FEMALE; GENE EXPRESSION REGULATION; ISCHEMIA; PLACENTA; PRE-ECLAMPSIA; PREGNANCY; RATS; RATS, SPRAGUE-DAWLEY; REACTIVE OXYGEN SPECIES; RNA, MESSENGER; T-LYMPHOCYTES, REGULATORY;

EID: 84944395090     PISSN: 03636119     EISSN: 15221490     Source Type: Journal    
DOI: 10.1152/ajpregu.00154.2015     Document Type: Article

References (47)

1. Alexander BT, Cockrell KL, Massey MB, Bennett WA, Granger JP. Tumor necrosis factor-alpha-induced hypertension in pregnant rats results in decreased renal neuronal nitric oxide synthase expression. Am J Hy-pertens 15: 170-175, 2002.
2. Aluvihare VR, Kallikourdis M, Betz AG. Regulatory T cells mediate maternal tolerance to the fetus. Nat Immunol 5: 266-271, 2004.
3. Bettini M, Vignali DA. Regulatory T cells and inhibitory cytokines in autoimmunity. Curr Opin Immunol 21: 612-618, 2009.
4. Conrad KP, Benyo DF. Placental cytokines and the pathogenesis of preeclampsia. Am J Reprod Immunol 37: 240-249, 1997.
5. Darmochwal-Kolarz D, Kludka-Sternik M, Tabarkiewicz J, Kolarz B, Rolinski J, Leszczynska-Gorzelak B, Oleszczuk J. The predominance of Th17 lymphocytes and decreased number and function of Treg cells in preeclampsia. J Reprod Immunol 93: 75-81, 2012.
6. Dechend R, Homuth V, Wallukat G, Kreuzer J, Park JK, Theuer J, Juepner A, Gulba DC, Mackman N, Haller H, Luft FC. AT1 receptor agonistic antibodies from preeclamptic patients cause vascular cells to express tissue factor. Circulation 101: 2382-2387, 2000.
7. Dechend R, Homuth V, Wallukat G, Muller DN, Krause M, Dudenhausen J, Haller H, Luft FC. Agonistic antibodies directed at the angiotensin II, AT1 receptor in preeclampsia. J Soc Gynecol Invest 13: 79-86, 2006.
8. Geiger TL, Tauro S. Nature and nurture in Foxp3+ regulatory T cell development, stability, and function. Hum Immunol 73: 232-239, 2012.
9. George EM, Granger JP. Recent insights into the pathophysiology of preeclampsia. Expert Rev Obstet Gynecol 5: 557-566, 2010.
10. Gilbert JS, Ryan MJ, LaMarca BB, Sedeek M, Murphy SR, Granger JP. Pathophysiology of hypertension during preeclampsia: linking placen-tal ischemia with endothelial dysfunction. Am J Physiol Heart Circ Physiol 294: H541-H550, 2008.
11. Granger JP, LaMarca BB, Cockrell K, Sedeek M, Balzi C, Chandler D, Bennett W. Reduced uterine perfusion pressure (RUPP) model for studying cardiovascular-renal dysfunction in response to placental ischemia. Methods Mol Med 122: 383-392, 2006.
12. Harmon A, Cornelius D, Amaral L, Paige A, Herse F, Ibrahim T, Wallukat G, Faulkner J, Moseley J, Dechend R, LaMarca B. IL-10 supplementation increases Tregs and decreases hypertension in the RUPP rat model of preeclampsia. Hypertens Preg 34: 1-16, 2015.
13. Hoffmann DS, Weydert CJ, Lazartigues E, Kutschke WJ, Kienzle MF, Leach JE, Sharma JA, Sharma RV, Davisson RL. Chronic tempol prevents hypertension, proteinuria, and poor feto-placental outcomes in BPH/5 mouse model of preeclampsia. Hypertension 51: 1058-1065, 2008.
14. Hoffmann P, Eder R, Boeld TJ, Doser K, Piseshka B, Andreesen R, Edinger M. Only the CD45RA+ subpopulation of CD4+CD25 high T cells gives rise to homogeneous regulatory T-cell lines upon in vitro expansion. Blood 108: 4260-4267, 2006.
15. Hoffmann P, Eder R, Kunz-Schughart LA, Andreesen R, Edinger M. Large-scale in vitro expansion of polyclonal human CD4(+)CD25high regulatory T cells. Blood 104: 895-903, 2004.
16. Hougardy JM, Verscheure V, Locht C, Mascart F. In vitro expansion of CD4+CD25highFOXP3+CD127low/--regulatory T cells from peripheral blood lymphocytes of healthy Mycobacterium tuberculosis-infected humans. Microbes Infect 9: 1325-1332, 2007.
17. Housley WJ, Adams CO, Nichols FC, Puddington L, Lingenheld EG, Zhu L, Rajan TV, Clark RB. Natural but not inducible regulatory T cells require TNF-a signaling for in vivo function. J Immunol 186: 6779-6787, 2011.
18. LaMarca B, Cornelius D, Wallace K. Elucidating immune mechanisms causing hypertension during pregnancy. Physiology 28: 225-233, 2013.
19. LaMarca B, Parrish M, Ray LF, Murphy SR, Roberts L, Glover P, Wallukat G, Wenzel K, Cockrell K, Martin JN Jr, Ryan MJ, Dechend R. Hypertension in response to autoantibodies to the angiotensin II type I receptor (AT1-AA) in pregnant rats: role of endothelin-1. Hypertension 54: 905-909, 2009.
20. LaMarca B, Speed J, Fournier L, Babcock SA, Berry H, Cockrell K, Granger JP. Hypertension in response to chronic reductions in uterine perfusion in pregnant rats: effect of tumor necrosis factor-alpha blockade. Hypertension 52: 1161-1167, 2008.
21. LaMarca B, Wallace K, Herse F, Wallukat G, Martin JN Jr, Weimer A, Dechend R. Hypertension in response to placental ischemia during pregnancy: role of B lymphocytes. Hypertension 57: 865-871, 2011.
22. LaMarca B, Wallukat G, Llinas M, Herse F, Dechend R, Granger JP. Autoantibodies to the angiotensin type I receptor in response to placental ischemia and tumor necrosis factor alpha in pregnant rats. Hypertension 52: 1168-1172, 2008.
23. LaMarca BB, Bennett WA, Alexander BT, Cockrell K, Granger JP. Hypertension produced by reductions in uterine perfusion in the pregnant rat: role of tumor necrosis factor-alpha. Hypertension 46: 1022-1025, 2005.
24. LaMarca BB, Cockrell K, Sullivan E, Bennett W, Granger JP. Role of endothelin in mediating tumor necrosis factor-induced hypertension in pregnant rats. Hypertension 46: 82-86, 2005.
25. LaMarca BD, Alexander BT, Gilbert JS, Ryan MJ, Sedeek M, Murphy SR, Granger JP. Pathophysiology of hypertension in response to placental ischemia during pregnancy: a central role for endothelin? Gender Med 5 Suppl A: S133-S138, 2008.
26. LaMarca BD, Gilbert J, Granger JP. Recent progress toward the understanding of the pathophysiology of hypertension during preeclampsia. Hypertension 51: 982-988, 2008.
27. Li J, LaMarca B, Reckelhoff JF. A model of preeclampsia in rats: the reduced uterine perfusion pressure (RUPP) model. Am J Physiol Heart Circ Physiol 303: H1-H8, 2012.
28. Matsubara K, Higaki T, Matsubara Y, Nawa A. Nitric oxide and reactive oxygen species in the pathogenesis of preeclampsia. Int J Mol Sci 16: 4600-4614, 2015.
29. Noris M, Perico N, Remuzzi G. Mechanisms of disease: Pre-eclampsia. Nat Clin Pract Nephrol 1: 98-114; quiz 120, 2005.
30. Novotny S, Wallace K, Herse F, Moseley J, Darby M, Heath J, Gill J, Wallukat G, Martin JN, Dechend R, Lamarca B. CD4+ T cells play a critical role in mediating hypertension in response to placental ischemia. J Hypertens 2: 14873, 2013.
31. Page EW. The relation between hydatid moles, relative ischemia of the gravid uterus, and the placentaal origin of eclampsia. Am J Obstet Gynecol 37: 291-293, 1939.
32. Parrish MR, Murphy SR, Rutland S, Wallace K, Wenzel K, Wallukat G, Keiser S, Ray LF, Dechend R, Martin JN, Granger JP, LaMarca B. The effect of immune factors, tumor necrosis factor-alpha, and agonistic autoantibodies to the angiotensin II type I receptor on soluble fms-like tyrosine-1 and soluble endoglin production in response to hypertension during pregnancy. Am J Hypertens 23: 911-916, 2010.
33. Parrish MR, Ryan MJ, Glover P, Brewer J, Ray L, Dechend R, Martin JN Jr, Lamarca BB. Angiotensin II type 1 autoantibody induced hypertension during pregnancy is associated with renal endothelial dysfunction. Gender Med 8: 184-188, 2011.
34. Parrish MR, Wallace K, Tam Tam KB, Herse F, Weimer A, Wenzel K, Wallukat G, Ray LF, Arany M, Cockrell K, Martin JN, Dechend R, LaMarca B. Hypertension in response to AT1-AA: role of reactive oxygen species in pregnancy-induced hypertension. Am J Hypertens 24: 835-840, 2011.
35. Peterson RA. Regulatory T-cells: diverse phenotypes integral to immune homeostasis and suppression. Toxicol Pathol 40: 186-204, 2012.
36. Prins JR, Boelens HM, Heimweg J, Van der Heide S, Dubois AE, Van Oosterhout AJ, Erwich JJ. Preeclampsia is associated with lower percentages of regulatory T cells in maternal blood. Hypertens Pregnancy 28: 300-311, 2009.
37. Saito S. Th17 cells and regulatory T cells: new light on pathophysiology of preeclampsia. Immunol Cell Biol 88: 615-617, 2010.
38. Santner-Nanan B, Peek MJ, Khanam R, Richarts L, Zhu E, Fazekas de St Groth B, Nanan R. Systemic increase in the ratio between Foxp3+ and IL-17-producing CD4+ T cells in healthy pregnancy but not in preeclampsia. J Immunol 183: 7023-7030, 2009.
39. Shima T, Sasaki Y, Itoh M, Nakashima A, Ishii N, Sugamura K, Saito S. Regulatory T cells are necessary for implantation and maintenance of early pregnancy but not late pregnancy in allogeneic mice. J Reprod Immunol 85: 121-129, 2010.
40. Tam Tam KB, George E, Cockrell K, Arany M, Speed J, Martin JN Jr, Lamarca B, Granger JP. Endothelin type A receptor antagonist attenuates placental ischemia-induced hypertension and uterine vascular resistance. Am J Obstet Gynecol 204: 330 e331-e334, 2011.
41. Toldi G, Rigo J Jr, Stenczer B, Vasarhelyi B, Molvarec A. Increased prevalence of IL-17-producing peripheral blood lymphocytes in preeclampsia. Am J Reprod Immunol 66: 223-229, 2011.
42. Toldi G, Saito S, Shima T, Halmos A, Veresh Z, Vasarhelyi B, Rigo J Jr, Molvarec A. The frequency of peripheral blood CD4+ CD25high FoxP3+ and CD4+ CD25-FoxP3+ regulatory T cells in normal pregnancy and pre-eclampsia. Am J Reprod Immunol 68: 175-180, 2012.
43. Toldi G, Svec P, Vasarhelyi B, Meszaros G, Rigo J, Tulassay T, Treszl A. Decreased number of FoxP3+ regulatory T cells in preeclampsia. Acta Obstet Gynecol Scand 87: 1229-1233, 2008.
44. Vacca P, Mingari MC, Moretta L. Natural killer cells in human pregnancy. J Reprod Immunol 97: 14-19, 2013.
45. Vacca P, Moretta L, Moretta A, Mingari MC. Origin, phenotype and function of human natural killer cells in pregnancy. Trends Immunol 32: 517-523, 2011.
46. Wallace K, Richards S, Dhillon P, Weimer A, Edholm ES, Bengten E, Wilson M, Martin JN Jr, LaMarca B. CD4+ T-helper cells stimulated in response to placental ischemia mediate hypertension during pregnancy. Hypertension 57: 949-955, 2011.
47. Zenclussen AC, Fest S, Joachim R, Klapp BF, Arck PC. Introducing a mouse model for pre-eclampsia: adoptive transfer of activated Th1 cells leads to pre-eclampsia-like symptoms exclusively in pregnant mice. Eur J Immunol 34: 377-387, 2004.