Molecular mechanisms of tubal pregnancy

Expert Review of Obstetrics and Gynecology

Volumn 5, Issue 6, 2010, Pages 727-739

  Gebeh, Alpha K ^a   Willets, Jonathon M ^a   Marczylo, Timothy H ^a   Lam, Patricia M W ^a   Taylor, Anthony H ^a   Konje, Justin C ^a  

^a UNIVERSITY OF LEICESTER   (United Kingdom)

Author keywords

activins; anandamide; biomarker; cysteine rich secretory protein 3; cytokines; ectopic pregnancy; endocannabinoids; inducible nitric oxide synthase; integrins; interleukins; leukemia inhibitory factor; mucins; prokineticins; VEGF

Indexed keywords

ACTIVIN; ACTIVIN A; ALPHA INTEGRIN; BETA INTEGRIN; CANNABINOID 1 RECEPTOR; CANNABINOID 2 RECEPTOR; ENDOCANNABINOID; FATTY ACID AMIDASE; INDUCIBLE NITRIC OXIDE SYNTHASE; INTEGRIN; INTERLEUKIN 1; INTERLEUKIN 1 RECEPTOR; INTERLEUKIN 1 RECEPTOR BLOCKING AGENT; INTERLEUKIN 11; INTERLEUKIN 1BETA; INTERLEUKIN 6; JANUS KINASE; LEUKEMIA INHIBITORY FACTOR; MITOGEN ACTIVATED PROTEIN KINASE; MUCIN 1; MYELOPID; STAT3 PROTEIN; VASCULOTROPIN; VERY LATE ACTIVATION ANTIGEN 3;

CHLAMYDIA; DIAGNOSTIC VALUE; ECTOPIC PREGNANCY; FERTILIZATION; HUMAN; INFERTILITY THERAPY; INTRAUTERINE CONTRACEPTIVE DEVICE; NIDATION; NONHUMAN; PATHOPHYSIOLOGY; PELVIC INFLAMMATORY DISEASE; PROTEIN BLOOD LEVEL; PROTEIN FUNCTION; REVIEW; RISK FACTOR; SALPINGITIS; SENSITIVITY AND SPECIFICITY; SIGNAL TRANSDUCTION; SMOKING; UTERINE TUBE DISEASE; UTERINE TUBE PREGNANCY; UTERINE TUBE SURGERY;

EID: 78249277169     PISSN: 17474108     EISSN: None     Source Type: Journal    
DOI: 10.1586/eog.10.61     Document Type: Review

References (156)

1. Lewis G. Confidential Enquiries into Maternal Deaths in the United Kingdom, Confidential Enquiry into Maternal and Child Health, CEMACH. Saving Mothers' Lives: Reviewing Maternal Deaths to Make Motherhood Safer - 2003-2005: the Seventh Report of the Confidential Enquiries into Maternal Deaths in the United Kingdom. CEMACH, London, UK (2007).
2. Pisarska MD, Carson SA. Incidence and risk factors for ectopic pregnancy. Clin. Obstet. Gynecol. 42(1), 2-8 (1999).
3. Wedderburn CJ, Warner P, Graham B, Duncan WC, Critchley HO, Horne AW. Economic evaluation of diagnosing and excluding ectopic pregnancy. Hum. Reprod. 25(2), 328-333 (2010).
4. Farquhar CM. Ectopic pregnancy. Lancet 366(9485), 583-591 (2005).
5. Sadler TW, Langman J. Langman's Medical Embryology. Lippincott William & Wilkins, MD, USA (2009).
6. Attar E. Endocrinology of ectopic pregnancy. Obstet. Gynecol. Clin. North Am. 31(4), 779-794, x (2004).
7. Guzeloglu-Kayisli O, Kayisli UA, Taylor HS. The role of growth factors and cytokines during implantation: endocrine and paracrine interactions. Semin. Reprod. Med. 27(1), 62-79 (2009).
8. Battista N, Pasquariello N, Di Tommaso M, Maccarrone M. Interplay between endocannabinoids, steroids and cytokines in the control of human reproduction. J. Neuroendocrinol. 20 (Suppl. 1), 82-89 (2008).
9. Arredondo JL, Diaz V, Gaitan H et al. Oral clindamycin and ciprofloxacin versus intramuscular ceftriaxone and oral doxycycline in the treatment of mild-tomoderate pelvic inflammatory disease in outpatients. Clin. Infect. Dis. 24(2), 170-178 (1997).
10. Barnhart KT, Sammel MD, Gracia CR, Chittams J, Hummel AC, Shaunik A. Risk factors for ectopic pregnancy in women with symptomatic first-trimester pregnancies. Fertil. Steril. 86(1), 36-43 (2006).
11. Brodowska A, Szydlowska I, Starczewski A et al. [Analysis of risk factors for ectopic pregnancy in own material in the years 1993-2002]. Pol. Merkur. Lekarski. 18(103), 74-77 (2005).
12. Bouyer J, Coste J, Shojaei T et al. Risk factors for ectopic pregnancy: a comprehensive analysis based on a large case-control, population-based study in France. Am. J. Epidemiol. 157(3), 185-194 (2003).
13. Bouyer J. [Epidemiology of ectopic pregnancy: incidence, risk factors and outcomes]. J. Gynecol. Obstet. Biol. Reprod. (Paris) 32 (7 Suppl.), S8-S17 (2003).
14. Ankum WM, Mol BW, Van der Veen F, Bossuyt PM. Risk factors for ectopic pregnancy: a meta-analysis. Fertil. Steril. 65(6), 1093-1099 (1996).
15. Xiong X, Buekens P, Wollast E. IUD use and the risk of ectopic pregnancy: a meta-analysis of case-control studies. Contraception 52(1), 23-34 (1995).
16. Mol BW, Ankum WM, Bossuyt PM, Van der Veen F. Contraception and the risk of ectopic pregnancy: a meta-analysis. Contraception 52(6), 337-341 (1995).
17. Pisarska MD, Carson SA, Buster JE. Ectopic pregnancy. Lancet 351(9109), 1115-1120 (1998).
18. Qublan HS, Malkawi HY, Tahat YA et al. In vitro fertilisation treatment: factors affecting its results and outcome. J. Obstet. Gynaecol. 25(7), 689-693 (2005).
19. Klemetti R, Sevon T, Gissler M, Hemminki E. Complications of IVF and ovulation induction. Hum. Reprod. 20(12), 3293-3300 (2005).
20. Gelbaya TA. Short and long-term risks to women who conceive through in vitro fertilization. Hum. Fertil. (Camb.) 13(1), 19-27 (2009).
21. Dubuisson JB, Aubriot FX, Mathieu L, Foulot H, Mandelbrot L, de Joliere JB. Risk factors for ectopic pregnancy in 556 pregnancies after in vitro fertilization: implications for preventive management. Fertil. Steril. 56(4), 686-690 (1991).
22. Ribic-Pucelj M, Tomazevic T, Vogler A, Meden-Vrtovec H. Risk factors for ectopic pregnancy after in vitro fertilization and embryo transfer. J. Assist. Reprod. Genet. 12(9), 594-598 (1995).
23. Clayton HB, Schieve LA, Peterson HB, Jamieson DJ, Reynolds MA, Wright VC. Ectopic pregnancy risk with assisted reproductive technology procedures. Obstet. Gynecol. 107(3), 595-604 (2006).
24. Pyrgiotis E, Sultan KM, Neal GS, Liu HC, Grifo JA, Rosenwaks Z. Ectopic pregnancies after in vitro fertilization and embryo transfer. J. Assist. Reprod. Genet. 11(2), 79-84 (1994).
25. Habana AE, Palter SF. Is tubal embryo transfer of any value? A meta-analysis and comparison with the Society for Assisted Reproductive Technology database. Fertil. Steril. 76(2), 286-293 (2001).
26. Jee BC, Suh CS, Kim SH. Ectopic pregnancy rates after frozen versus fresh embryo transfer: a meta-analysis. Gynecol. Obstet. Invest. 68(1), 53-57 (2009).
27. Bunyavejchevin S, Havanond P, Wisawasukmongchol W. Risk factors of ectopic pregnancy. J. Med. Assoc. Thai. 86 (Suppl. 2), S417-S421 (2003).
28. Dekeyser-Boccara J, Milliez J. [Smoking and ectopic pregnancy: is there a causal relationship?]. J. Gynecol. Obstet. Biol. Reprod. (Paris) 34 Spec No 1, 3S119-3S123 (2005).
29. Coste J, Job-Spira N, Fernandez H, Papiernik E, Spira A. Risk factors for ectopic pregnancy: a case-control study in France, with special focus on infectious factors. Am. J. Epidemiol. 133(9), 839-849 (1991).
30. Job-Spira N, Collet P, Coste J, Bremond A, Laumon B. [Risk factors for ectopic pregnancy. Results of a case-control study in the Rhone-Alpes region]. Contracept. Fertil. Sex. 21(4), 307-312 (1993).
31. Talbot P, Riveles K. Smoking and reproduction: the oviduct as a target of cigarette smoke. Reprod. Biol. Endocrinol. 3, 52(2005).
32. Weigert M, Gruber D, Pernicka E, Bauer P, Feichtinger W. Previous tubal ectopic pregnancy raises the incidence of repeated ectopic pregnancies in in vitro fertilizationembryo transfer patients. J. Assist. Reprod. Genet. 26(1), 13-17 (2009).
33. Skjeldestad FE, Hadgu A, Eriksson N. Epidemiology of repeat ectopic pregnancy: a population-based prospective cohort study. Obstet. Gynecol. 91(1), 129-135 (1998).
34. Haines BP, Voyle RB, Rathjen PD. Intracellular and extracellular leukemia inhibitory factor proteins have different cellular activities that are mediated by distinct protein motifs. Mol. Biol. Cell 11(4), 1369-1383 (2000).
35. Kimber SJ. Leukaemia inhibitory factor in implantation and uterine biology. Reproduction 130(2), 131-145 (2005).
36. Pflanz S, Kurth I, Grotzinger J, Heinrich PC, Muller-Newen G. Two different epitopes of the signal transducer gp130 sequentially cooperate on IL-6-induced receptor activation. J. Immunol. 165(12), 7042-7049 (2000).
37. Heinrich PC, Behrmann I, Haan S, Hermanns HM, Muller-Newen G, Schaper F. Principles of interleukin (IL)-6-type cytokine signalling and its regulation. Biochem. J. 374 (Pt 1), 1-20 (2003).
38. O'Shea JJ, Gadina M, Schreiber RD. Cytokine signaling in 2002: new surprises in the Jak/Stat pathway. Cell 109 (Suppl.), S121-S131 (2002).
39. Niemand C, Nimmesgern A, Haan S et al. Activation of STAT3 by IL-6 and IL-10 in primary human macrophages is differentially modulated by suppressor of cytokine signaling 3. J. Immunol. 170(6), 3263-3272 (2003).
40. Wang HY, Cheng Z, Malbon CC. Overexpression of mitogen-activated protein kinase phosphatases MKP1, MKP2 in human breast cancer. Cancer Lett. 191(2), 229-237 (2003).
41. Roussel L, Houle F, Chan C et al. IL-17 promotes p38 MAPK-dependent endothelial activation enhancing neutrophil recruitment to sites of inflammation. J. Immunol. 184(8), 4531-4537 (2010).
42. Lad SP, Fukuda EY, Li J, de la Maza LM, Li E. Up-regulation of the JAK/STAT1 signal pathway during Chlamydia trachomatis infection. J. Immunol. 174(11), 7186-7193 (2005).
43. Mathur AN, Chang HC, Zisoulis DG et al. Stat3 and Stat4 direct development of IL-17-secreting Th cells. J. Immunol. 178(8), 4901-4907 (2007).
44. Lee H, Herrmann A, Deng JH et al. Persistently activated Stat3 maintains constitutive NF-kB activity in tumors. Cancer Cell 15(4), 283-293 (2009).
45. Rebouissou S, Amessou M, Couchy G et al. Frequent in-frame somatic deletions activate gp130 in inflammatory hepatocellular tumours. Nature 457(7226), 200-204 (2009).
46. Ning ZQ, Li J, Arceci RJ. Signal transducer and activator of transcription 3 activation is required for Asp (816) mutant c-Kitmediated cytokine-independent survival and proliferation in human leukemia cells. Blood 97(11), 3559-3567 (2001).
47. Fitzgerald JS, Tsareva SA, Poehlmann TG et al. Leukemia inhibitory factor triggers activation of signal transducer and activator of transcription 3, proliferation, invasiveness, and altered protease expression in choriocarcinoma cells. Int. J. Biochem. Cell Biol. 37(11), 2284-2296 (2005).
48. Poehlmann TG, Fitzgerald JS, Meissner A et al. Trophoblast invasion: tuning through LIF, signalling via Stat3. Placenta 26 (Suppl. A), S37-S41 (2005).
49. Conquet F, Brulet P. Developmental expression of myeloid leukemia inhibitory factor gene in preimplantation blastocysts and in extraembryonic tissue of mouse embryos. Mol. Cell Biol. 10(7), 3801-3805 (1990).
50. Murray R, Lee F, Chiu CP. The genes for leukemia inhibitory factor and interleukin-6 are expressed in mouse blastocysts prior to the onset of hemopoiesis. Mol. Cell Biol. 10(9), 4953-4956 (1990).
51. Charnock-Jones DS, Sharkey AM, Fenwick P, Smith SK. Leukaemia inhibitory factor mRNA concentration peaks in human endometrium at the time of implantation and the blastocyst contains mRNA for the receptor at this time. J. Reprod. Fertil. 101(2), 421-426 (1994).
52. Dunglison GF, Barlow DH, Sargent IL. Leukaemia inhibitory factor significantly enhances the blastocyst formation rates of human embryos cultured in serum-free medium. Hum. Reprod. 11(1), 191-196 (1996).
53. Ptak G, Lopes F, Matsukawa K, Tischner M, Loi P. Leukaemia inhibitory factor enhances sheep fertilization in vitro via an influence on the oocyte. Theriogenology 65(9), 1891-1899 (2006).
54. Tsai HD, Chang CC, Hsieh YY, Hsu LW, Chang SC, Lo HY. Effect of different concentrations of recombinant leukemia inhibitory factor on different development stage of mouse embryo in vitro. J. Assist. Reprod. Genet. 17(6), 352-355 (2000).
55. Fry RC, Batt PA, Fairclough RJ, Parr RA. Human leukemia inhibitory factor improves the viability of cultured ovine embryos. Biol. Reprod. 46(3), 470-474 (1992).
56. Anegon I, Cuturi MC, Godard A et al. Presence of leukaemia inhibitory factor and interleukin 6 in porcine uterine secretions prior to conceptus attachment. Cytokine 6(5), 493-499 (1994).
57. Yang ZM, Le SP, Chen DB, Harper MJ. Temporal and spatial expression of leukemia inhibitory factor in rabbit uterus during early pregnancy. Mol. Reprod. Dev. 38(2), 148-152 (1994).
58. Bhatt H, Brunet LJ, Stewart CL. Uterine expression of leukemia inhibitory factor coincides with the onset of blastocyst implantation. Proc. Natl Acad. Sci. USA 88(24), 11408-11412 (1991).
59. Mitchell MH, Swanson RJ, Hodgen GD, Oehninger S. Enhancement of in vitro murine embryo development by recombinant leukemia inhibitory factor. J. Soc. Gynecol. Investig. 1(3), 215-219 (1994).
60. Stewart CL, Kaspar P, Brunet LJ et al. Blastocyst implantation depends on maternal expression of leukaemia inhibitory factor. Nature 359(6390), 76-79 (1992).
61. Nardo LG, Sabatini L, Rai R, Nardo F. Pinopode expression during human implantation. Eur. J. Obstet. Gynecol. Reprod. Biol. 101(2), 104-108 (2002).
62. Aghajanova L, Stavreus-Evers A, Nikas Y, Hovatta O, Landgren BM. Coexpression of pinopodes and leukemia inhibitory factor, as well as its receptor, in human endometrium. Fertil. Steril. 79 (Suppl. 1), 808-814 (2003).
63. Quinn CE, Detmar J, Casper RF. Pinopodes are present in Lif null and Hoxa10 null mice. Fertil. Steril. 88 (Suppl. 4), 1021-1028 (2007).
64. Hsieh YY, Tsai HD, Chang CC, Hsu LW, Chang SC, Lo HY. Prolonged culture of human cryopreserved embryos with recombinant human leukemia inhibitory factor. J. Assist. Reprod. Genet. 17(3), 131-134 (2000).
65. Guney M, Erdemoglu E, Oral B, Karahan N, Mungan T. Leukemia inhibitory factor (LIF) is immunohistochemically localized in tubal ectopic pregnancy. Acta Histochem. 110(4), 319-323 (2008).
66. Wanggren K, Lalitkumar PG, Hambiliki F, Stabi B, Gemzell-Danielsson K, Stavreus-Evers A. Leukaemia inhibitory factor receptor and gp130 in the human Fallopian tube and endometrium before and after mifepristone treatment and in the human preimplantation embryo. Mol. Hum. Reprod. 13(6), 391-397 (2007).
67. Ji YF, Chen LY, Xu KH, Yao JF, Shi YF. Locally elevated leukemia inhibitory factor in the inflamed Fallopian tube resembles that found in tubal pregnancy. Fertil. Steril. 91(6), 2308-2314 (2009).
68. Keltz MD, Attar E, Buradagunta S, Olive DL, Kliman HJ, Arici A. Modulation of leukemia inhibitory factor gene expression and protein biosynthesis in the human Fallopian tube. Am. J. Obstet. Gynecol. 175(6), 1611-1619 (1996).
69. Toth M, Jeremias J, Ledger WJ, Witkin SS. In vivo tumor necrosis factor production in women with salpingitis. Surg. Gynecol. Obstet. 174(5), 359-362 (1992).
70. McGee ZA, Jensen RL, Clemens CM, Taylor-Robinson D, Johnson AP, Gregg CR. Gonococcal infection of human Fallopian tube mucosa in organ culture: relationship of mucosal tissue TNF-α concentration to sloughing of ciliated cells. Sex. Transm. Dis. 26(3), 160-165 (1999).
71. Maisey K, Nardocci G, Imarai M et al. Expression of proinflammatory cytokines and receptors by human Fallopian tubes in organ culture following challenge with Neisseria gonorrhoeae. Infect. Immun. 71(1), 527-532 (2003).
72. Kiran G, Kiran H, Ertopcu K, Kilinc M, Ekerbicer HC, Vardar MA. Tuba uterina leukemia inhibitory factor concentration does not increase in tubal pregnancy: a preliminary study. Fertil. Steril. 83(2), 484-486 (2005).
73. Wegner NT, Mershon JL. Evaluation of leukemia inhibitory factor as a marker of ectopic pregnancy. Am. J. Obstet. Gynecol. 184(6), 1074-1076 (2001).
74. Daponte A, Pournaras S, Zintzaras E et al. The value of a single combined measurement of VEGF, glycodelin, progesterone, PAPP-A, HPL and LIF for differentiating between ectopic and abnormal intrauterine pregnancy. Hum. Reprod. 20(11), 3163-3166 (2005).
75. Keller DC, Du XX, Srour EF, Hoffman R, Williams DA. Interleukin-11 inhibits adipogenesis and stimulates myelopoiesis in human long-term marrow cultures. Blood 82(5), 1428-1435 (1993).
76. Robb L, Li R, Hartley L, Nandurkar HH, Koentgen F, Begley CG. Infertility in female mice lacking the receptor for interleukin 11 is due to a defective uterine response to implantation. Nat. Med. 4(3), 303-308 (1998).
77. Chen HF, Lin CY, Chao KH, Wu MY, Yang YS, Ho HN. Defective production of interleukin-11 by decidua and chorionic villi in human anembryonic pregnancy. J. Clin. Endocrinol. Metab. 87(5), 2320-2328 (2002).
78. von Rango U, Alfer J, Kertschanska S et al. Interleukin-11 expression: its significance in eutopic and ectopic human implantation. Mol. Hum. Reprod. 10(11), 783-792 (2004).
79. Dimitriadis E, White CA, Jones RL, Salamonsen LA. Cytokines, chemokines and growth factors in endometrium related to implantation. Hum. Reprod. Update 11(6), 613-630 (2005).
80. Prantner D, Darville T, Sikes JD et al. Critical role for interleukin-1β (IL-1β) during Chlamydia muridarum genital infection and bacterial replicationindependent secretion of IL-1β in mouse macrophages. Infect. Immun. 77(12), 5334-5346 (2009).
81. Hvid M, Baczynska A, Deleuran B et al. Interleukin-1 is the initiator of Fallopian tube destruction during Chlamydia trachomatis infection. Cell Microbiol. 9(12), 2795-2803 (2007).
82. Simon C, Piquette GN, Frances A, Westphal LM, Heinrichs WL, Polan ML. Interleukin-1 type I receptor messenger ribonucleic acid expression in human endometrium throughout the menstrual cycle. Fertil. Steril. 59(4), 791-796 (1993). (Pubitemid 23104180)
83. Simon C, Piquette GN, Frances A, Polan ML. Localization of interleukin-1 type I receptor and interleukin-1 β in human endometrium throughout the menstrual cycle. J. Clin. Endocrinol. Metab. 77(2), 549-555 (1993). (Pubitemid 23230073)
84. Huang HY, Chan SH, Wu CH, Wang CW, Lai CH, Soong YK. Interleukin-1 system messenger ribonucleic acid and protein expression in human Fallopian tube may be associated with ectopic pregnancy. Fertil. Steril. 84(5), 1484-1492 (2005).
85. Hess AP, Baston-Buest DM, Schanz A, Hirchenhain J, Bielfeld P, Kruessel JS. Interleukin-1 system in the human Fallopian tube - no spatial but a temporal regulation of mRNA and protein expression. Mol. Cell Endocrinol. 303 (1-2), 7-12 (2009).
86. Andrianifahanana M, Moniaux N, Batra SK. Regulation of mucin expression: mechanistic aspects and implications for cancer and inflammatory diseases. Biochim. Biophys. Acta 1765(2), 189-222 (2006).
87. Brayman M, Thathiah A, Carson DD. MUC1: a multifunctional cell surface component of reproductive tissue epithelia. Reprod. Biol. Endocrinol. 2, 4(2004).
88. Guang W, Ding H, Czinn SJ, Kim KC, Blanchard TG, Lillehoj EP. Muc1 cell surface mucin attenuates epithelial infammation in response to a common mucosal pathogen. J. Biol. Chem. 285(27), 20547-20557 (2010).
89. DeSouza MM, Surveyor GA, Price RE et al. MUC1/episialin: a critical barrier in the female reproductive tract. J. Reprod. Immunol. 45(2), 127-158 (1999).
90. Lopez-Ferrer A, Curull V, Barranco C et al. Mucins as differentiation markers in bronchial epithelium. Squamous cell carcinoma and adenocarcinoma display similar expression patterns. Am. J. Respir. Cell Mol. Biol. 24(1), 22-29 (2001).
91. Gipson IK, Ho SB, Spurr-Michaud SJ et al. Mucin genes expressed by human female reproductive tract epithelia. Biol. Reprod. 56(4), 999-1011 (1997).
92. Meseguer M, Aplin JD, Caballero-Campo P et al. Human endometrial mucin MUC1 is up-regulated by progesterone and down-regulated in vitro by the human blastocyst. Biol. Reprod. 64(2), 590-601 (2001).
93. Dharmaraj N, Gendler SJ, Carson DD. Expression of human MUC1 during early pregnancy in the human MUC1 transgenic mouse model. Biol. Reprod. 81(6), 1182-1188 (2009).
94. Aplin JD, Meseguer M, Simon C, Ortiz ME, Croxatto H, Jones CJ. MUC1, glycans and the cell-surface barrier to embryo implantation. Biochem. Soc. Trans. 29 (Pt 2), 153-156 (2001).
95. Savaris RF, da Silva LC, Moraes Gda S, Edelweiss MI. Expression of MUC1 in tubal pregnancy. Fertil. Steril. 89(4), 1015-1017 (2008).
96. Al-Azemi M, Refaat B, Aplin J, Ledger W. The expression of MUC1 in human Fallopian tube during the menstrual cycle and in ectopic pregnancy. Hum. Reprod. 24(10), 2582-2587 (2009).
97. de Kretser DM, Hedger MP, Loveland KL, Phillips DJ. Inhibins, activins and follistatin in reproduction. Hum. Reprod. Update 8(6), 529-541 (2002).
98. Hotten G, Neidhardt H, Schneider C, Pohl J. Cloning of a new member of the TGF-β family: a putative new activin β C chain. Biochem. Biophys. Res. Commun. 206(2), 608-613 (1995).
99. Oda S, Nishimatsu S, Murakami K, Ueno N. Molecular cloning and functional analysis of a new activin β subunit: a dorsal mesoderm-inducing activity in Xenopus. Biochem. Biophys. Res. Commun. 210(2), 581-588 (1995).
100. Fang J, Yin W, Smiley E, Wang SQ, Bonadio J. Molecular cloning of the mouse activin β E subunit gene. Biochem. Biophys. Res. Commun. 228(3), 669-674 (1996).
101. Phillips DJ, de Kretser DM, Hedger MP. Activin and related proteins in inflammation: not just interested bystanders. Cytokine Growth Factor Rev. 20(2), 153-164 (2009).
102. Sako D, Grinberg AV, Liu J et al. Characterization of the ligand binding functionality of the extracellular domain of activin receptor type IIb. J. Biol. Chem. 285(27), 21037-21048 (2010).
103. Gribi R, Tanaka T, Harper-Summers R, Yu J. Expression of activin A in inflammatory arthropathies. Mol. Cell Endocrinol. 180 (1-2), 163-167 (2001).
104. Hubner G, Brauchle M, Gregor M, Werner S. Activin A: a novel player and inflammatory marker in inflammatory bowel disease? Lab. Invest. 77(4), 311-318 (1997).
105. Zhang YQ, Resta S, Jung B, Barrett KE, Sarvetnick N. Upregulation of activin signaling in experimental colitis. Am. J. Physiol. Gastrointest. Liver Physiol. 297(4), G768-G780 (2009).
106. Ota F, Maeshima A, Yamashita S et al. Activin A induces cell proliferation of fibroblast-like synoviocytes in rheumatoid arthritis. Arthritis Rheum. 48(9), 2442-2449 (2003).
107. Gandolfi F, Modina S, Brevini TA et al. Activin β A subunit is expressed in bovine oviduct. Mol. Reprod. Dev. 40(3), 286-291 (1995).
108. Refaat BA, Bahathiq AO, Sockanathan S, Stewart RL, Wells M, Ledger WL. Production and localization of activins and activin type IIA and IIB receptors by the human endosalpinx. Reproduction 128(2), 249-255 (2004).
109. Bahathiq AO, Stewart RL, Wells M, Moore HD, Pacey AA, Ledger WL. Production of activins by the human endosalpinx. J. Clin. Endocrinol. Metab. 87(11), 5283-5289 (2002).
110. Refaat B, Amer S, Ola B, Chapman N, Ledger W. The expression of activin-βA-and-βB-subunits, follistatin, and activin type II receptors in Fallopian tubes bearing an ectopic pregnancy. J. Clin. Endocrinol. Metab. 93(1), 293-299 (2008).
111. Refaat B, Al-Azemi M, Geary I, Eley A, Ledger W. Role of activins and inducible nitric oxide in the pathogenesis of ectopic pregnancy in patients with or without Chlamydia trachomatis infection. Clin. Vaccine Immunol. 16(10), 1493-1503 (2009).
112. Florio P, Severi FM, Bocchi C et al. Single serum activin a testing to predict ectopic pregnancy. J. Clin. Endocrinol. Metab. 92(5), 1748-1753 (2007).
113. Kirk E, Papageorghiou AT, Van Calster B et al. The use of serum inhibin A and activin A levels in predicting the outcome of 'pregnancies of unknown location'. Hum. Reprod. 24(10), 2451-2456 (2009).
114. Habayeb OM, Bell SC, Konje JC. Endogenous cannabinoids: metabolism and their role in reproduction. Life Sci. 70(17), 1963-1977 (2002).
115. Godlewski G, Offertaler L, Wagner JA, Kunos G. Receptors for acylethanolamides-GPR55 and GPR119. Prostaglandins Other Lipid Mediat. 89 (3-4), 105-111 (2009).
116. Taylor AH, Amoako AA, Bambang K et al. Endocannabinoids and pregnancy. Clin. Chim. Acta 411 (13-14), 921-930 (2010).
117. Liu J, Wang L, Harvey-White J et al. A biosynthetic pathway for anandamide. Proc. Natl Acad. Sci. USA 103(36), 13345-13350 (2006).
118. Wang J, Ueda N. Biology of endocannabinoid synthesis system. Prostaglandins Other Lipid Mediat. 89 (3-4), 112-119 (2009).
119. Dinh TP, Carpenter D, Leslie FM et al. Brain monoglyceride lipase participating in endocannabinoid inactivation. Proc. Natl Acad. Sci. USA 99(16), 10819-10824 (2002).
120. Saario SM, Laitinen JT. Monoglyceride lipase as an enzyme hydrolyzing 2-arachidonoylglycerol. Chem. Biodivers. 4(8), 1903-1913 (2007).
121. Wang H, Guo Y, Wang D et al. Aberrant cannabinoid signaling impairs oviductal transport of embryos. Nat. Med. 10(10), 1074-1080 (2004).
122. Paria BC, Song H, Wang X et al. Dysregulated cannabinoid signaling disrupts uterine receptivity for embryo implantation. J. Biol. Chem. 276(23), 20523-20528 (2001).
123. Wang H, Xie H, Guo Y et al. Fatty acid amide hydrolase deficiency limits early pregnancy events. J. Clin. Invest. 116(8), 2122-2131 (2006).
124. Shaw JL, Dey SK, Critchley HO, Horne AW. Current knowledge of the aetiology of human tubal ectopic pregnancy. Hum. Reprod. Update 16(4), 432-444 (2010).
125. Al-Azemi M, Refaat B, Amer S, Ola B, Chapman N, Ledger W. The expression of inducible nitric oxide synthase in the human Fallopian tube during the menstrual cycle and in ectopic pregnancy. Fertil. Steril. 94(3), 833-840 (2009).
126. Shaw JL, Denison FC, Evans J et al. Evidence of prokineticin dysregulation in Fallopian tube from women with ectopic pregnancy. Fertil. Steril. 94(5), 1601-1608.e1 (2010).
127. Horne AW, King AE, Shaw E et al. Attenuated sex steroid receptor expression in Fallopian tube of women with ectopic pregnancy. J. Clin. Endocrinol. Metab. 94(12), 5146-5154 (2009).
128. Land JA, Arends JW. Immunohistochemical analysis of estrogen and progesterone receptors in Fallopian tubes during ectopic pregnancy. Fertil. Steril. 58(2), 335-337 (1992).
129. Lam PM, Briton-Jones C, Cheung CK, Leung SW, Cheung LP, Haines C. Increased messenger RNA expression of vascular endothelial growth factor and its receptors in the implantation site of the human oviduct with ectopic gestation. Fertil. Steril. 82(3), 686-690 (2004). (Pubitemid 39243193)
130. von Rango U, Classen-Linke I, Kertschanska S, Kemp B, Beier HM. Effects of trophoblast invasion on the distribution of leukocytes in uterine and tubal implantation sites. Fertil. Steril. 76(1), 116-124 (2001).
131. Ekerhovd E, Brannstrom M, Alexandersson M, Norstrom A. Evidence for nitric oxide mediation of contractile activity in isolated strips of the human Fallopian tube. Hum. Reprod. 12(2), 301-305 (1997).
132. Perez Martinez S, Viggiano M, Franchi AM et al. Effect of nitric oxide synthase inhibitors on ovum transport and oviductal smooth muscle activity in the rat oviduct. J. Reprod. Fertil. 118(1), 111-117 (2000).
133. Jiao J, Han D, Meng N, Jin S, Zhang L. Regulation of tracheal ciliary beat frequency by nitric oxide synthase substrate L-arginine. ORL J. Otorhinolaryngol. Relat. Spec. 72(1), 6-11 (2010).
134. Shao R, Zhang SX, Weijdegard B et al. Nitric oxide synthases and tubal ectopic pregnancies induced by Chlamydia infection: basic and clinical insights. Mol. Hum. Reprod. DOI: 10.1093/molehr/gaq063 (2010) (Epub ahead of print).
135. Daniel Y, Geva E, Lerner-Geva L et al. Levels of vascular endothelial growth factor are elevated in patients with ectopic pregnancy: is this a novel marker? Fertil. Steril. 72(6), 1013-1017 (1999).
136. Felemban A, Sammour A, Tulandi T. Serum vascular endothelial growth factor as a possible marker for early ectopic pregnancy. Hum. Reprod. 17(2), 490-492 (2002).
137. Kucera-Sliutz E, Schiebel I, Konig F, Leodolter S, Sliutz G, Koelbl H. Vascular endothelial growth factor (VEGF) and discrimination between abnormal intrauterine and ectopic pregnancy. Hum. Reprod. 17(12), 3231-3234 (2002).
138. Venter JC, Adams MD, Myers EW et al. The sequence of the human genome. Science 291(5507), 1304-1351 (2001).
139. van der Flier A, Sonnenberg A. Function and interactions of integrins. Cell Tissue Res. 305(3), 285-298 (2001).
140. Kim TH, Kim HI, Soung YH, Shaw LA, Chung J. Integrin (α6β4) signals through Src to increase expression of S100A4, a metastasis-promoting factor: implications for cancer cell invasion. Mol. Cancer Res. 7(10), 1605-1612 (2009).
141. Lindberg K, Strom A, Lock JG, Gustafsson JA, Haldosen LA, Helguero LA. Expression of estrogen receptor β increases integrin α1 and integrin β1 levels and enhances adhesion of breast cancer cells. J. Cell Physiol. 222(1), 156-167 (2010).
142. Hecht JL, Dolinski BM, Gardner HA, Violette SM, Weinreb PH. Overexpression of the αvβ6 integrin in endometrial cancer. Appl. Immunohistochem. Mol. Morphol. 16(6), 543-547 (2008).
143. Lindberg K, Strom A, Lock JG, Gustafsson JA, Haldosen LA, Helguero LA. Expression of estrogen receptor β increases integrin a1 and integrin β1 levels and enhances adhesion of breast cancer cells. J. Cell Physiol. 222(1), 156-167 (2010).
144. Takeyama H, Funahashi H, Sawai H et al. Expression of α6 integrin subunit is associated with malignancy in gastric gastrointestinal stromal tumors. Med. Sci. Monit. 13(2), CR51-CR56 (2007).
145. Lessey BA, Damjanovich L, Coutifaris C, Castelbaum A, Albelda SM, Buck CA. Integrin adhesion molecules in the human endometrium. Correlation with the normal and abnormal menstrual cycle. J. Clin. Invest. 90(1), 188-195 (1992).
146. Lessey BA, Ilesanmi AO, Lessey MA, Riben M, Harris JE, Chwalisz K. Luminal and glandular endometrial epithelium express integrins differentially throughout the menstrual cycle: implications for implantation, contraception, and infertility. Am. J. Reprod. Immunol. 35(3), 195-204 (1996).
147. Ruck P, Marzusch K, Kaiserling E et al. Distribution of cell adhesion molecules in decidua of early human pregnancy. An immunohistochemical study. Lab. Invest. 71(1), 94-101 (1994). (Pubitemid 24246026)
148. Lessey BA. Endometrial integrins and the establishment of uterine receptivity. Hum. Reprod. 13 (Suppl. 3), 247-258 (1998).
149. Makrigiannakis A, Karamouti M, Petsas G, Makris N, Nikas G, Antsaklis A. The expression of receptivity markers in the Fallopian tube epithelium. Histochem. Cell Biol. 132(2), 159-167 (2009).
150. Illera MJ, Cullinan E, Gui Y, Yuan L, Beyler SA, Lessey BA. Blockade of the α (v) β (3) integrin adversely affects implantation in the mouse. Biol. Reprod. 62(5), 1285-1290 (2000).
151. Inan S, Giray G, Vatansever HS, Ozbilgin K, Kuscu NK, Sayhan S. Immunolocalization of integrins and fibronectin in tubal pregnancy. Acta Histochem. 106(3), 235-243 (2004).
152. Maldonado-Perez D, Evans J, Denison F, Millar R P, Jabbour HN. Potential roles of the prokineticins in reproduction. Trends Endocrinol. Metab. 18(2), 66-72 (2007).
153. Evans J, Catalano RD, Brown P et al. Prokineticin 1 mediates fetal-maternal dialogue regulating endometrial leukemia inhibitory factor. FASEB J. 23(7), 2165-2175 (2009).
154. Horne AW, Duncan WC, King AE et al. Endometrial cysteine-rich secretory protein 3 is inhibited by human chorionic gonadotrophin, and is increased in the decidua of tubal ectopic pregnancy. Mol. Hum. Reprod. 15(5), 287-294 (2009).
155. Kratzschmar J, Haendler B, Eberspaecher U, Roosterman D, Donner P, Schleuning WD. The human cysteine-rich secretory protein (CRISP) family. Primary structure and tissue distribution of CRISP-1, CRISP-2 and CRISP-3. Eur. J. Biochem. 236(3), 827-836 (1996).
156. Cartwright J, Duncan WC, Critchley HO, Horne AW. Serum biomarkers of tubal ectopic pregnancy: current candidates and future possibilities. Reproduction 138(1), 9-22 (2009).