Stress and substance P but not the substance P-metabolite SP5-11 trigger murine abortion by augmenting TNF-α levels at the feto-maternal interface

Scandinavian Journal of Immunology

Volumn 63, Issue 1, 2006, Pages 42-49

  Fest, S ^a,c   Zenclussen, A C ^a   Joachim, R ^a   Hagen, E ^a   Demuth, H U ^b   Hoffmann, T ^b  

^a HUMBOLDT UNIVERSITY   (Germany)

^b PROBIODRUG AG   (Germany)

^c YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

GAMMA INTERFERON; INTERLEUKIN 10; INTERLEUKIN 12; INTERLEUKIN 4; SUBSTANCE P; SUBSTANCE P [5-11]; TUMOR NECROSIS FACTOR ALPHA; CYTOKINE; PEPTIDE FRAGMENT; SUBSTANCE P METABOLITE 5 11; SUBSTANCE P-METABOLITE 5-11;

ABORTION; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CD8+ T LYMPHOCYTE; CONTROLLED STUDY; CYTOKINE PRODUCTION; DECIDUA; FEMALE; FETOPLACENTAL UNIT; INTERFERON PRODUCTION; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN BLOOD LEVEL; STRESS; TH1 CELL; TH2 CELL; ANIMAL; BLOOD; CBA MOUSE; CHEMICALLY INDUCED DISORDER; CYTOLOGY; DBA MOUSE; DRUG EFFECT; FETOMATERNAL TRANSFUSION; IMMUNOLOGY; LYMPHOCYTE COUNT; METABOLISM; PREGNANCY; SPONTANEOUS ABORTION;

ABORTION, SPONTANEOUS; ANIMALS; CD8-POSITIVE T-LYMPHOCYTES; CYTOKINES; DECIDUA; FEMALE; LYMPHOCYTE COUNT; MATERNAL-FETAL EXCHANGE; MICE; MICE, INBRED CBA; MICE, INBRED DBA; PEPTIDE FRAGMENTS; PREGNANCY; STRESS; SUBSTANCE P; TH1 CELLS; TH2 CELLS; TUMOR NECROSIS FACTOR-ALPHA;

EID: 33644849800     PISSN: 03009475     EISSN: 13653083     Source Type: Journal    
DOI: 10.1111/j.1365-3083.2005.001711.x     Document Type: Article

References (62)

1. Chaouat G Assal MA Martal J et al. IL-10 prevents naturally occurring fetal loss in the CBA × DBA/2 mating combination, and local defect in IL-10 production in this abortion-prone combination is corrected by in vivo injection of IFN-tau J Immunol 1995 154 4261 8
2. Krishnan L Guilbert LJ Wegmann TG Belosevic M Mosmann TR T helper 1 response against Leishmania major in pregnant C57BL/6 mice increases implantation failure and fetal resorptions. Correlation with increased IFN-gamma and TNF and reduced IL-10 production by placental cells J Immunol 1996 156 653 62
3. Krishnan L Guilbert LJ Russell AS Wegmann TG Mosmann TR Belosevic M Pregnancy impairs resistance of C57BL/6 mice to Leishmania major infection and causes decreased antigen-specific IFN-gamma response and increased production of T helper 2 cytokines J Immunol 1996 156 644 52
4. Hill JA Polgar K Anderson DJ T-helper 1-type immunity to trophoblast in women with recurrent spontaneous abortion JAMA 1995 273 1933 6
5. Makhseed M Raghupathy R Azizieh F Al Azemi MM Hassan NA Bandar A Mitogen-induced cytokine responses of maternal peripheral blood lymphocytes indicate a differential Th-type bias in normal pregnancy and pregnancy failure Am J Reprod Immunol 1999 42 273 81
6. Ho HN Chao KH Chen HF Chen SU Wu MY Yang YS Distribution of Th1 and Th2 cell populations in human peripheral and decidual T cells from normal and anembryonic pregnancies Fertil Steril 2001 76 797 803
7. Zenclussen AC Fest S Sehmsdorf US Hagen E Klapp BF Arck PC Upregulation of decidual P-selectin expression is associated with an increased number of Th1 cell populations in patients suffering from spontaneous abortions Cell Immunol 2001 213 94 103
8. Zenclussen AC Kortebani G Mazzolli A Margni R Malan BI Interleukin-6 and soluble interleukin-6 receptor serum levels in recurrent spontaneous abortion women immunized with paternal white cells Am J Reprod Immunol 2000 44 22 9
9. Bonney EA Maternal tolerance is not critically dependent on interleukin-4 Immunology 2001 103 382 9
10. Zenclussen AC Fest S Busse P Joachim R Klapp BF Arck PC Questioning the Th1/Th2 paradigm in reproduction: peripheral levels of IL-12 are down-regulated in miscarriage patients Am J Reprod Immunol 2002 48 245 51
11. Chaouat G Zourbas S Ostojic S et al. A brief review of recent data on some cytokine expressions at the materno-foetal interface which might challenge the classical Th1/Th2 dichotomy J Reprod Immunol 2002 53 241 56
12. Svensson L Arvola M Sallstrom MA Holmdahl R Mattsson R The Th2 cytokines IL-4 and IL-10 are not crucial for the completion of allogeneic pregnancy in mice J Reprod Immunol 2001 51 3 7
13. Munn DH Zhou M Attwood JT et al. Prevention of allogeneic fetal rejection by tryptophan catabolism Science 1998 281 1191 3
14. Xu C Mao D Holers VM Palanca B Cheng AM Molina H A critical role for murine complement regulator crry in fetomaternal tolerance Science 2000 287 498 501
15. Margni RA Malan BI Paradoxical behavior of asymmetric IgG antibodies Immunol Rev 1998 163 77 87
16. Aluvihare VR Kallikourdis M Betz AG Regulatory T cells mediate maternal tolerance to the fetus Nat Immun 2004 5 266 71
17. + T regulatory cells prevents fetal rejection in a murine abortion model Am J Pathol 2005 166 811 22
18. Arck PC Ferrick DA Steele-Norwood D Croitoru K Clark DA Regulation of abortion by gamma delta T cells Am J Reprod Immunol 1997 37 87 93
19. Arck PC Troutt AB Clark DA Soluble receptors neutralizing TNF-alpha and IL-1 block stress-triggered murine abortion Am J Reprod Immunol 1997 37 262 6
20. Markert UR Arck PC McBey BA et al. Stress triggered abortions are associated with alterations of granulated cells into the decidua Am J Reprod Immunol 1997 37 94 100
21. + decidual cells via substance P Am J Reprod Immunol 2001 45 303 9
22. Sacks GP Clover LM Bainbridge DR Redman CW Sargent IL Flow cytometric measurement of intracellular Th1 and Th2 cytokine production by human villous and extravillous cytotrophoblast Placenta 2001 22 550 9
23. Clark DA Banwatt D Chaouat G Stress-triggered abortion in mice prevented by alloimmunization Am J Reprod Immunol 1993 29 141 7
24. Arck PC Merali FS Manuel J Chaouat G Clark DA Stress-triggered abortion: inhibition of protective suppression and promotion of tumor necrosis factor-alpha (TNF-alpha) release as a mechanism triggering resorptions in mice Am J Reprod Immunol 1995 33 74 80
25. Arck PC Rose M Hertwig K Hagen E Hildebrandt M Klapp BF Stress and immune mediators in miscarriage Hum Reprod 2001 16 1505 11
26. Arck PC Merali FS Stanisz AM et al. Stress-induced murine abortion associated with substance P-dependent alteration in cytokines in maternal uterine decidua Biol Reprod 1995 53 814 9
27. Leeman SE Ferguson SL Substance P: an historical perspective Neuropeptides 2000 34 249 54
28. Euler U Gaddum J An unidentified depressor substance in certain tissue extracts J Physiol 1931 72 74 87
29. Stanisz AM Scicchitano R Dazin P Bienenstock J Payan DG Distribution of substance P receptors on murine spleen and Peyer's patch T and B cells J Immunol 1987 139 749 54
30. Kavelaars A Jeurissen F Heijnen CJ Substance P receptors and signal transduction in leukocytes Immunomethods 1994 5 41 8
31. Kavelaars A Broeke D Jeurissen F et al. Activation of human monocytes via a non-neurokinin substance P receptor that is coupled to Gi protein, calcium, phospholipase D, MAP kinase, and IL-6 production J Immunol 1994 153 3691 9
32. Jeurissen F Kavelaars A Korstjens M et al. Monocytes express a non-neurokinin substance P receptor that is functionally coupled to MAP kinase J Immunol 1994 152 2987 94
33. Mapp CE Miotto D Braccioni F et al. The distribution of neurokinin-1 and neurokinin-2 receptors in human central airways Am J Respir Crit Care Med 2000 161 207 15
34. Marx L Arck P Kieslich C Mitterlechner S Kapp M Dietl J Decidual mast cells might be involved in the onset of human first-trimester abortion Am J Reprod Immunol 1999 41 34 40
35. Lotz M Vaughan JH Carson DA Effect of neuropeptides on production of inflammatory cytokines by human monocytes Science 1988 241 1218 21
36. Ansel JC Brown JR Payan DG Brown MA Substance P selectively activates TNF-alpha gene expression in murine mast cells J Immunol 1993 150 4478 85
37. Mentlein R Dipeptidyl-peptidase IV (CD26) - role in the inactivation of regulatory peptides Regul Pept 1999 85 9 24
38. Hildebrandt M Arck PC Kruber S Demuth HU Reutter W Klapp BF Inhibition of dipeptidyl peptidase IV (DP IV, CD26) activity abrogates stress-induced, cytokine-mediated murine abortions Scand J Immunol 2001 53 449 54
39. Hartung HP Wolters K Toyka KV Substance P: binding properties and studies on cellular responses in guinea pig macrophages J Immunol 1986 136 3856 63
40. Grouzmann E Monod M Landis B et al. Loss of dipeptidylpeptidase IV activity in chronic rhinosinusitis contributes to the neurogenic inflammation induced by substance P in the nasal mucosa FASEB J 2002 16 1132 4
41. Zenclussen AC Blois S Stumpo R et al. Murine abortion is associated with enhanced interleukin-6 levels at the feto-maternal interface Cytokine 2003 24 150 60
42. Hunt JS Cytokine networks in the uteroplacental unit: macrophages as pivotal regulatory cells J Reprod Immunol 1989 16 1 17
43. Mizuno M Aoki K Kimbara T Functions of macrophages in human decidual tissue in early pregnancy Am J Reprod Immunol 1994 31 180 8
44. Duclos AJ Haddad EK Baines MG Presence of activated macrophages in a murine model of early embryo loss Am J Reprod Immunol 1995 33 354 66
45. Maes M Song C Lin A et al. The effects of psychological stress on humans: increased production of pro-inflammatory cytokines and a Th1-like response in stress-induced anxiety Cytokine 1998 10 313 8
46. Marshall GD Jr Agarwal SK Lloyd C Cohen L Henninger EM Morris GJ Cytokine dysregulation associated with exam stress in healthy medical students Brain Behav Immun 1998 12 297 307
47. Iwakabe K Shimada M Ohta A et al. The restraint stress drives a shift in Th1/Th2 balance toward Th2-dominant immunity in mice Immunol Lett 1998 62 39 43
48. Arck PC Ferrick DA Steele-Norwood D Croitoru K Clark DA Murine T cell determination of pregnancy outcome: I. Effects of strain, alphabeta T cell receptor, gammadelta T cell receptor, and gammadelta T cell subsets Am J Reprod Immunol 1997 37 492 502
49. Lea RG Underwood J Flanders KC et al. A subset of patients with recurrent spontaneous abortion is deficient in transforming growth factor beta-2-producing "suppressor cells" in uterine tissue near the placental attachment site Am J Reprod Immunol 1995 34 52 64
50. Erlebacher A Zhang D Parlow AF Glimcher LH Ovarian insufficiency and early pregnancy loss induced by activation of the innate immune system J Clin Invest 2004 114 39 48
51. Hill JA Haimovici F Anderson DJ Products of activated lymphocytes and macrophages inhibit mouse embryo development in vitro J Immunol 1987 139 2250 4
52. Clark DA Ding JW Chaouat G Coulam CB August C Levy GA The emerging role of immunoregulation of fibrinogen-related procoagulant Fgl2 in the success or spontaneous abortion of early pregnancy in mice and humans Am J Reprod Immunol 1999 42 37 43
53. Gorivodsky M Zemlyak I Orenstein H et al. TNF-alpha messenger RNA and protein expression in the uteroplacental unit of mice with pregnancy loss J Immunol 1998 160 4280 8
54. Yaron A Naider F Proline-dependent structural and biological properties of peptides and proteins Crit Rev Biochem Mol Biol 1993 28 31 81
55. Campbell RM Stricker P Miller R et al. Enhanced stability and potency of novel growth hormone-releasing factor (GRF) analogues derived from rodent and human GRF sequences Peptides 1994 15 489 95
56. Croft M Carter L Swain SL Dutton RW Generation of polarized antigen-specific CD8 effector populations: reciprocal action of interleukin (IL)-4 and IL-12 in promoting type 2 versus type 1 cytokine profiles J Exp Med 1994 180 1715 28
57. Ng SC Gilman-Sachs A Thaker P Beaman KD Beer AE Kwak-Kim J Expression of intracellular Th1 and Th2 cytokines in women with recurrent spontaneous abortion, implantation failures after IVF/ET or normal pregnancy Am J Reprod Immunol 2002 48 77 86
58. + T cells as a basis for stress-triggered substance P-mediated abortion in mice Cell Immunol 1996 171 226 30
59. Szekeres-Bartho J Autran B Debre P Andreu G Denver L Chaouat G Immunoregulatory effects of a suppressor factor from healthy pregnant women's lymphocytes after progesterone induction Cell Immunol 1989 122 281 94
60. Faust Z Laskarin G Rukavina D Szekeres-Bartho J Progesterone-induced blocking factor inhibits degranulation of natural killer cells Am J Reprod Immunol 1999 42 71 5
61. + T cells J Immunol 1998 161 5236 44
62. + T cell subsets TC1 and TC2 cause different histopathologic forms of murine cardiac allograft rejection Transplantation 2001 71 606 10