IL-10 supplementation increases Tregs and decreases hypertension in the RUPP rat model of preeclampsia

Hypertension in Pregnancy

Volumn 34, Issue 3, 2015, Pages 291-306

  Harmon, Ashlyn ^a   Cornelius, Denise ^a   Amaral, Lorena ^a   Paige, Adrienne ^a   Herse, Florian ^b   Ibrahim, Tarek ^a   Wallukat, Gerd ^b   Faulkner, Jessica ^a   Moseley, Janae ^a   Dechend, Ralf ^b   LaMarca, Babbette ^a,c  

^a UNIVERSITY OF MISSISSIPPI MEDICAL CENTER   (United States)

^b MAX DELBRÜCK CENTER FOR MOLECULAR MEDICINE   (Germany)

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

Author keywords

Hypertension; inflammation; pregnancy

Indexed keywords

ANGIOTENSIN 1 RECEPTOR; INTERLEUKIN 10; INTERLEUKIN 6; MESSENGER RNA; NITRIC OXIDE; PREPROENDOTHELIN; REACTIVE OXYGEN METABOLITE; SUPEROXIDE; TRANSFORMING GROWTH FACTOR BETA; TUMOR NECROSIS FACTOR ALPHA; TUMOR NECROSIS FACTOR;

ANIMAL CELL; ANIMAL MODEL; ARTERIAL PRESSURE; ARTICLE; CD4+ T LYMPHOCYTE; COLLATERAL CIRCULATION; CONTROLLED STUDY; ENZYME LINKED IMMUNOSORBENT ASSAY; FEMALE; FETUS; FETUS WEIGHT; GENE EXPRESSION; GESTATIONAL AGE; IMPLANTABLE PUMP; ISCHEMIA; MATERNAL HYPERTENSION; MEAN ARTERIAL PRESSURE; NONHUMAN; OVARY BLOOD FLOW; OXIDATIVE STRESS; PERFUSION PRESSURE; PLACENTA DISORDER; PLACENTAL ISCHEMIA; PREECLAMPSIA; RAT; REDUCED UTERINE PERFUSION PRESSURE; REGULATORY T LYMPHOCYTE; SUPPLEMENTATION; ANIMAL; BLOOD; BLOOD PRESSURE; DISEASE MODEL; DRUG EFFECTS; HYPERTENSION; METABOLISM; PATHOPHYSIOLOGY; PLACENTA; PRE-ECLAMPSIA; PREGNANCY; SPRAGUE DAWLEY RAT; VASCULARIZATION;

ANIMALS; BLOOD PRESSURE; DISEASE MODELS, ANIMAL; FEMALE; HYPERTENSION; INTERLEUKIN-10; INTERLEUKIN-6; ISCHEMIA; PLACENTA; PRE-ECLAMPSIA; PREGNANCY; RATS, SPRAGUE-DAWLEY; T-LYMPHOCYTES, REGULATORY; TUMOR NECROSIS FACTOR-ALPHA;

EID: 84938598445     PISSN: 10641955     EISSN: 15256065     Source Type: Journal    
DOI: 10.3109/10641955.2015.1032054     Document Type: Article

References (53)

1. George EM, Granger JP. Recent insights into the pathophysiology of preeclampsia. Expert Rev Obstet Gynecol 2010; 5: 557-66
2. Noris M, Perico N, Remuzzi G. Mechanisms of disease: pre-eclampsia. Nat Clin Pract Nephrol 2005; 1: 98-114; quiz 120
3. LaMarca B, Wallace K, Granger J. Role of angiotensin ii type i receptor agonistic autoantibodies (at1-aa) in preeclampsia. Curr Opin Pharmacol 2011; 11: 175-9
4. Leik CE, Walsh SW. Neutrophils infiltrate resistance-sized vessels of subcutaneous fat in women with preeclampsia. Hypertension 2004; 44: 72-7
5. Lindheimer MD, Romero R. Emerging roles of antiangiogenic and angiogenic proteins in pathogenesis and prediction of preeclampsia. Hypertension 2007; 50: 35-6
6. Roberts JM, Lain KY. Recent insights into the pathogenesis of pre-eclampsia. Placenta 2002; 23: 359-72
7. Duncombe G, Veldhuizen RA, Gratton RJ, et al. Il-6 and tnfalpha across the umbilical circulation in term pregnancies: relationship with labour events. Early Hum Dev 2010; 86: 113-17
8. Sharma A, Satyam A, Sharma JB. Leptin, il-10 and inflammatory markers (tnf-alpha, il-6 and il-8) in pre-eclamptic, normotensive pregnant and healthy non-pregnant women. Am J Reprod Immunol 2007; 58: 21-30
9. Dhillion P, Wallace K, Herse F, et al. Il-17-mediated oxidative stress is an important stimulator of at1-aa and hypertension during pregnancy. Am J Physiol. Regul, Integr Comp Physiol 2012; 303: R353-8
10. Lamarca B. The role of immune activation in contributing to vascular dysfunction and the pathophysiology of hypertension during preeclampsia. Minerva Ginecol 2010; 62: 105-20
11. Santner-Nanan B, Peek MJ, Khanam R, et al. Systemic increase in the ratio between foxp3 + and il-17-producing cd4+ t cells in healthy pregnancy but not in preeclampsia. J Immunol 2009; 183: 7023-30
12. Makris A, Xu B, Yu B, et al. Placental deficiency of interleukin-10 (il-10) in preeclampsia and its relationship to an il10 promoter polymorphism. Placenta 2006; 27: 445-51
13. Sowmya S, Ramaiah A, Sunitha T, et al. Evaluation of interleukin-10 (g-1082a) promoter polymorphism in preeclampsia. J Reprod Infertil 2013; 14: 62-6
14. Sowmya S, Ramaiah A, Sunitha T, et al. Role of il-10-819(t/c) promoter polymorphism in preeclampsia. Inflammation 2014; 37: 1022-7
15. Darby MM, Kedra W, Cornelius D, et al. Vitamin d supplementation suppresses hypoxia-stimulated placental cytokine secretion, hypertension and cd4+ t cell stimulation in response to placental ischemia. Med J Obstet Gynecol 2013; 1: 1012-8
16. Chatterjee P, Chiasson VL, Seerangan G, et al. Cotreatment with interleukin 4 and interleukin 10 modulates immune cells and prevents hypertension in pregnant mice. Am J Hypertension 2015; 281: 135-42
17. Dechend R, Gratze P, Wallukat G, et al. Agonistic autoantibodies to the at1 receptor in a transgenic rat model of preeclampsia. Hypertension 2005; 45: 742-6
18. Dechend R, Homuth V, Wallukat G, et al. Agonistic antibodies directed at the angiotensin ii, at1 receptor in preeclampsia. J Soc Gynecol Investig 2006; 13: 79-86
19. Dechend R, Muller DN, Wallukat G, et al. Activating auto-antibodies against the at1 receptor in preeclampsia. Autoimmun Rev 2005; 4: 61-5
20. Novotny SR, Wallace K, Heath J, et al. Activating autoantibodies to the angiotensin ii type i receptor play an important role in mediating hypertension in response to adoptive transfer of cd4+ t lymphocytes from placental ischemic rats. Am J Physiol. Regul, Integr Comp Physiol 2012; 302: R1197-201
21. Wallukat G, Neichel D, Nissen E, et al. Agonistic autoantibodies directed against the angiotensin ii at1 receptor in patients with preeclampsia. Can J Physiol Pharmacol 2003; 81: 79-83
22. Granger JP, Alexander BT, Bennett WA, Khalil RA. Pathophysiology of pregnancy-induced hypertension. Am J Hypertension 2001; 14: 178S-85S
23. LaMarca B, Parrish M, Ray LF, et al. Hypertension in response to autoantibodies to the angiotensin ii type i receptor (at1-aa) in pregnant rats: role of endothelin-1. Hypertension 2009; 54: 905-9
24. LaMarca BB, Bennett WA, Alexander BT, et al. Hypertension produced by reductions in uterine perfusion in the pregnant rat: role of tumor necrosis factor-alpha. Hypertension 2005; 46: 1022-5
25. 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 2012; 303: H1-8
26. Wallace K, Richards S, Dhillon P, et al. Cd4+ t-helper cells stimulated in response to placental ischemia mediate hypertension during pregnancy. Hypertension 2011; 57: 949-55
27. Cornelius DC, Hogg JP, Scott J, et al. Administration of interleukin-17 soluble receptor c suppresses th17 cells, oxidative stress, and hypertension in response to placental ischemia during pregnancy. Hypertension 2013; 62: 1068-73
28. Boonstra A, Rajsbaum R, Holman M, et al. Macrophages and myeloid dendritic cells, but not plasmacytoid dendritic cells, produce il-10 in response to myd88-and trif-dependent tlr signals, and tlr-independent signals. J Immunol 2006; 177: 7551-8
29. Jiang HR, Muckersie E, Robertson M, et al. Secretion of interleukin-10 or interleukin-12 by lps-activated dendritic cells is critically dependent on time of stimulus relative to initiation of purified dc culture. J Leukocyte Biol 2002; 72: 97885
30. Shaw MH, Freeman GJ, Scott MF, et al. Tyk2 negatively regulates adaptive th1 immunity by mediating il-10 signaling and promoting ifn-gamma-dependent il-10 reactivation. J Immunol 2006; 176: 7263-71
31. Jankovic D, Kullberg MC, Feng CG, et al. Conventional t-bet(+)foxp3(-) th1 cells are the major source of host-protective regulatory il-10 during intracellular protozoan infection. J Exp Med 2007; 204: 273-83
32. Fiorentino DF, Bond MW, Mosmann TR. Two types of mouse t helper cell. Iv. Th2 clones secrete a factor that inhibits cytokine production by th1 clones. J Exp Med 1989; 170: 2081-95
33. Gu Y, Yang J, Ouyang X, et al. Interleukin 10 suppresses th17 cytokines secreted by macrophages and t cells. Eur J Immunol 2008; 38: 1807-13
34. Moore KW, de Waal Malefyt R, Coffman RL, O'Garra A. Interleukin-10 and the interleukin-10 receptor. Annu Rev Immunol 2001; 19: 683-765
35. Gregori S, Tomasoni D, Pacciani V, et al. Differentiation of type 1 t regulatory cells (tr1) by tolerogenic dc-10 requires the il-10-dependent ilt4/hla-g pathway. Blood 2010; 116: 935-44
36. Heo YJ, Joo YB, Oh HJ, et al. Il-10 suppresses th17 cells and promotes regulatory t cells in the cd4+ t cell population of rheumatoid arthritis patients. Immunol Lett 2010; 127: 150-6
37. Lochner M, Peduto L, Cherrier M, et al. In vivo equilibrium of proinflammatory il-17+ and regulatory il-10+ foxp3+ rorgamma t+ t cells. J Exp Med 2008; 205: 1381-93
38. Ivanov II, McKenzie BS, Zhou L, et al. The orphan nuclear receptor rorgammat directs the differentiation program of proinflammatory il-17+ t helper cells. Cell 2006; 126: 1121-33
39. Nevers T, Kalkunte S, Sharma S. Uterine regulatory t cells, il-10 and hypertension. Am J Reprod Immunol 2011; 66: 88-92
40. Tinsley JH, South S, Chiasson VL, Mitchell BM. Interleukin-10 reduces inflammation, endothelial dysfunction, and blood pressure in hypertensive pregnant rats. Am J Physiol. Regul, Integr Comp Physiol 2010; 298: R713-19
41. Zemse SM, Hilgers RH, Simkins GB, et al. Restoration of endothelin-1-induced impairment in endothelium-dependent relaxation by interleukin-10 in murine aortic rings. Can J Physiol Pharmacol 2008; 86: 557-65
42. Lai Z, Kalkunte S, Sharma S. A critical role of interleukin-10 in modulating hypoxia-induced preeclampsia-like disease in mice. Hypertension 2011; 57: 505-14
43. Chatterjee P, Chiasson VL, Kopriva SE, et al. Interleukin 10 deficiency exacerbates toll-like receptor 3-induced preeclampsia-like symptoms in mice. Hypertension 2011; 58: 489-96
44. Dechend R, Homuth V, Wallukat G, et al. At(1) receptor agonistic antibodies from preeclamptic patients cause vascular cells to express tissue factor. Circulation 2000; 101: 2382-7
45. LaMarca B, Wallace K, Herse F, et al. Hypertension in response to placental ischemia during pregnancy: role of b lymphocytes. Hypertension 2011; 57: 865-71
46. Parrish MR, Murphy SR, Rutland S, et al. 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 Hypertension 2010; 23: 911-6
47. Parrish MR, Ryan MJ, Glover P, et al. Angiotensin ii type 1 autoantibody induced hypertension during pregnancy is associated with renal endothelial dysfunction. Gender Med 2011; 8: 184-8
48. Parrish MR, Wallace K, Tam Tam KB, et al. Hypertension in response to at1-aa: role of reactive oxygen species in pregnancy-induced hypertension. Am J Hypertension 2011; 24: 835-40
49. Madazli R, Aydin S, Uludag S, et al. Maternal plasma levels of cytokines in normal and preeclamptic pregnancies and their relationship with diastolic blood pressure and fibronectin levels. Acta Obstet Gynecol Scand 2003; 82: 797-802
50. Ayatollahi M, Geramizadeh B, Samsami A. Transforming growth factor beta-1 influence on fetal allografts during pregnancy. Transplant Proc 2005; 37: 4603-4
51. Perucci LO, Gomes KB, Freitas LG, et al. Soluble endoglin, transforming growth factor-beta 1 and soluble tumor necrosis factor alpha receptors in different clinical manifestations of preeclampsia. PLoS One 2014; 9: e97632
52. Tran DQ. Tgf-beta: the sword, the wand, and the shield of foxp3(+) regulatory t cells. J Mol Cell Biol 2012; 4: 29-37
53. Chen W, Konkel JE. Tgf-beta and adaptive foxp3(+) regulatory t cells. J Mol Cell Biol 2010; 2: 30-6