Rheumatoid Arthritis Recapitulates Events Relevant in Blastocyst Implantation and Embryogenesis: A Pathogenetic Theory

Seminars in Arthritis and Rheumatism

Volumn 41, Issue 3, 2011, Pages 382-392

  Straub, Rainer H ^a   Cutolo, Maurizio ^b   Fleck, Martin ^a,c  

^a UNIVERSITY HOSPITAL REGENSBURG   (Germany)

^b UNIVERSITY OF GENOA   (Italy)

^c Asclepios Clinic Bad Abbach   (Germany)

Author keywords

Blastocyst implantation; BMP; Embryogenesis; Hormone; NOTCH; Rheumatoid arthritis; WNT

Indexed keywords

BONE MORPHOGENETIC PROTEIN 2; BONE MORPHOGENETIC PROTEIN 4; BONE MORPHOGENETIC PROTEIN 5; BONE MORPHOGENETIC PROTEIN 6; CALCITONIN GENE RELATED PEPTIDE; CORTICOTROPIN RELEASING FACTOR; DICKKOPF 1 PROTEIN; GROWTH DIFFERENTIATION FACTOR 5; LEPTIN; MATRIX METALLOPROTEINASE; NEUROPILIN 2; NOTCH RECEPTOR; PROGESTERONE; SOMATOMEDIN BINDING PROTEIN 1; TISSUE INHIBITOR OF METALLOPROTEINASE; TRANSCRIPTION FACTOR TWIST; TRANSFORMING GROWTH FACTOR BETA; WNT PROTEIN;

ANGIOGENESIS; ARTICLE; CHRONIC ARTHRITIS; CHRONIC INFLAMMATION; CYTOKINE PRODUCTION; DECIDUALIZATION; EMBRYO DEVELOPMENT; EMBRYONIC STEM CELL; HUMAN; MESENCHYMAL STEM CELL; NIDATION; NONHUMAN; OSTEOARTHRITIS; PLURIPOTENT STEM CELL; PRIORITY JOURNAL; RHEUMATOID ARTHRITIS; STEROIDOGENESIS; SYNOVIAL FLUID; SYNOVITIS; TISSUE REPAIR;

ARTHRITIS, RHEUMATOID; EMBRYO IMPLANTATION; EMBRYONIC DEVELOPMENT; HUMANS;

EID: 82955212887     PISSN: 00490172     EISSN: 1532866X     Source Type: Journal    
DOI: 10.1016/j.semarthrit.2011.04.007     Document Type: Article

References (80)

1. Martin P., Parkhurst S.M. Parallels between tissue repair and embryo morphogenesis. Development 2004, 131:3021-3034.
2. Williams G.C. Pleiotropy, natural selection, and the evolution of senescence. Evolution 1957, 11:398-411.
3. Straub R.H., Besedovsky H.O. Integrated evolutionary, immunological, and neuroendocrine framework for the pathogenesis of chronic disabling inflammatory diseases. FASEB J 2003, 17:2176-2183.
4. Straub R.H., Del Rey A., Besedovsky H.O. Emerging concepts for the pathogenesis of chronic disabling inflammatory diseases: neuroendocrine-immune interactions and evolutionary biology. R Psychoneuroimmunology 2007, 217-232. Elsevier-Academic Press, San Diego (CA). Ader (Ed.).
5. Zvaifler N.J. Relevance of the stroma and epithelial-mesenchymal transition (EMT) for the rheumatic diseases. Arthritis Res Ther 2006, 8:210.
6. Ostensen M., Lockshin M., Doria A., Valesini G., Meroni P., Gordon C., et al. Update on safety during pregnancy of biological agents and some immunosuppressive anti-rheumatic drugs. Rheumatology (Oxford) 2008, 47(Suppl 3):iii28-iii31. iii28-iii31.
7. Jones E.A., Kinsey S.E., English A., Jones R.A., Straszynski L., Meredith D.M., et al. Isolation and characterization of bone marrow multipotential mesenchymal progenitor cells. Arthritis Rheum 2002, 46:3349-3360.
8. Jones E., Churchman S.M., English A., Buch M.H., Horner E.A., Burgoyne C.H., et al. Mesenchymal stem cells in rheumatoid synovium: Enumeration and functional assessment in relation to synovial inflammation level. Ann Rheum Dis 2009, 69:450-457.
9. Li X., Makarov S.S. An essential role of NF-kappaB in the "tumor-like" phenotype of arthritic synoviocytes. Proc Natl Acad Sci USA 2006, 103:17432-17437.
10. Tyndall A., Walker U.A., Cope A., Dazzi F., De B.C., Fibbe W., et al. Immunomodulatory properties of mesenchymal stem cells: a review based on an interdisciplinary meeting held at the Kennedy Institute of Rheumatology Division. Arthritis Res Ther 2007, 9:301. London, UK, 31 October 2005.
11. Dunn C.L., Kelly R.W., Critchley H.O. Decidualization of the human endometrial stromal cell: an enigmatic transformation. Reprod Biomed Online 2003, 7:151-161.
12. Pap T., Muller-Ladner U., Gay R.E., Gay S. Fibroblast biology. Role of synovial fibroblasts in the pathogenesis of rheumatoid arthritis. Arthritis Res 2000, 2:361-367.
13. Firestein G.S. Invasive fibroblast-like synoviocytes in rheumatoid arthritis. Passive responders or transformed aggressors?. Arthritis Rheum 1996, 39:1781-1790.
14. Paria B.C., Ma W., Tan J., Raja S., Das S.K., Dey S.K., et al. Cellular and molecular responses of the uterus to embryo implantation can be elicited by locally applied growth factors. Proc Natl Acad Sci USA 2001, 98:1047-1052.
15. Poggi S.H., Bostrom K.I., Demer L.L., Skinner H.C., Koos B.J. Placental calcification: a metastatic process?. Placenta 2001, 22:591-596.
16. Rovensky J., Kvetnansky R., Radikova Z., Imrich R., Greguska O., Vigas M., et al. Hormone concentrations in synovial fluid of patients with rheumatoid arthritis. Clin Exp Rheumatol 2005, 23:292-296.
17. Telang N.T., Suto A., Wong G.Y., Osborne M.P., Bradlow H.L. Induction by estrogen metabolite 16 alpha-hydroxyestrone of genotoxic damage and aberrant proliferation in mouse mammary epithelial cells. J Natl Cancer Inst 1992, 84:634-638.
18. Cutolo M., Lahita R.G. Estrogens and arthritis. Rheum Dis Clin North Am 2005, 31:19-27. vii.
19. Straub R.H. The complex role of estrogens in inflammation. Endocr Rev 2007, 28:521-574.
20. Schmidt M., Hartung R., Capellino S., Cutolo M., Pfeifer-Leeg A., Straub R.H. Estrone/17beta-estradiol conversion to, and tumor necrosis factor inhibition by, estrogen metabolites in synovial cells of patients with rheumatoid arthritis and patients with osteoarthritis. Arthritis Rheum 2009, 60:2913-2922.
21. Zoumakis E., Makrigiannakis A., Margioris A., Stournaras C., Gravanis A. Corticotropin releasing hormone (CRH) in normal and pregnant uterus: physiological implications. Front Biosci 1996, 1:e1-e8.
22. Crofford L.J., Sano H., Karalis K., Webster E.L., Goldmuntz E.A., Chrousos G.P., et al. Local secretion of corticotropin-releasing hormone in the joints of Lewis rats with inflammatory arthritis. J Clin Invest 1992, 90:2555-2564.
23. Crofford L.J., Sano H., Karalis K., Friedman T.C., Epps H.R., Remmers E.F., et al. Corticotropin-releasing hormone in synovial fluids and tissues of patients with rheumatoid arthritis and osteoarthritis. J Immunol 1993, 151:1587-1596.
24. Webster E.L., Barrientos R.M., Contoreggi C., Isaac M.G., Ligier S., Gabry K.E., et al. Corticotropin releasing hormone (CRH) antagonist attenuates adjuvant induced arthritis: role of CRH in peripheral inflammation. J Rheumatol 2002, 29:1252-1261.
25. Masuzaki H., Ogawa Y., Sagawa N., Hosoda K., Matsumoto T., Mise H., et al. Nonadipose tissue production of leptin: leptin as a novel placenta-derived hormone in humans. Nat Med 1997, 3:1029-1033.
26. Gonzalez R.R., Leary K., Petrozza J.C., Leavis P.C. Leptin regulation of the interleukin-1 system in human endometrial cells. Mol Hum Reprod 2003, 9:151-158.
27. Busso N., So A., Chobaz-Peclat V., Morard C., Martinez-Soria E., Talabot-Ayer D., et al. Leptin signaling deficiency impairs humoral and cellular immune responses and attenuates experimental arthritis. J Immunol 2002, 168:875-882.
28. Otero M., Lago R., Lago F., Casanueva F.F., Dieguez C., Gomez-Reino J.J., et al. Leptin, from fat to inflammation: old questions and new insights. FEBS Lett 2005, 579:295-301.
29. Strakova Z., Srisuparp S., Fazleabas A.T. IL-1beta during in vitro decidualization in primate. J Reprod Immunol 2002, 55:35-47.
30. Kim J.J., Fazleabas A.T. Uterine receptivity and implantation: the regulation and action of insulin-like growth factor binding protein-1 (IGFBP-1), HOXA10 and forkhead transcription factor-1 (FOXO-1) in the baboon endometrium. Reprod Biol Endocrinol 2004, 2:34.
31. Khosravi M.J., Diamandi A., Mistry J. Immunoassay of insulin-like growth factor binding protein-1. Clin Chem 1997, 43:523-532.
32. Ludikhuize J., de L.D., Groot D., Smeets T.J., Vinkenoog M., Sanders M.E., et al. Inhibition of forkhead box class O family member transcription factors in rheumatoid synovial tissue. Arthritis Rheum 2007, 56:2180-2191.
33. Halder J.B., Zhao X., Soker S., Paria B.C., Klagsbrun M., Das S.K., et al. Differential expression of VEGF isoforms and VEGF(164)-specific receptor neuropilin-1 in the mouse uterus suggests a role for VEGF(164) in vascular permeability and angiogenesis during implantation. Genesis 2000, 26:213-224.
34. Plaisier M., Rodrigues S., Willems F., Koolwijk P., van H.V., Helmerhorst F.M. Different degrees of vascularization and their relationship to the expression of vascular endothelial growth factor, placental growth factor, angiopoietins, and their receptors in first-trimester decidual tissues. Fertil Steril 2007, 88:176-187.
35. Ma W., Tan J., Matsumoto H., Robert B., Abrahamson D.R., Das S.K., et al. Adult tissue angiogenesis: evidence for negative regulation by estrogen in the uterus. Mol Endocrinol 2001, 15:1983-1992.
36. Morales D.E., McGowan K.A., Grant D.S., Maheshwari S., Bhartiya D., Cid M.C., et al. Estrogen promotes angiogenic activity in human umbilical vein endothelial cells in vitro and in a murine model. Circulation 1995, 91:755-763.
37. Seo K.H., Lee H.S., Jung B., Ko H.M., Choi J.H., Park S.J., et al. Estrogen enhances angiogenesis through a pathway involving platelet-activating factor-mediated nuclear factor-kappaB activation. Cancer Res 2004, 64:6482-6488.
38. Fraisl P., Mazzone M., Schmidt T., Carmeliet P. Regulation of angiogenesis by oxygen and metabolism. Dev Cell 2009, 16:167-179.
39. Taylor P.C., Sivakumar B. Hypoxia and angiogenesis in rheumatoid arthritis. Curr Opin Rheumatol 2005, 17:293-298.
40. Szekanecz Z., Koch A.E. Mechanisms of disease: angiogenesis in inflammatory diseases. Nat Clin Pract Rheumatol 2007, 3:635-643.
41. Bottomley M.J., Webb N.J., Watson C.J., Holt L., Bukhari M., Denton J., et al. Placenta growth factor (PlGF) induces vascular endothelial growth factor (VEGF) secretion from mononuclear cells and is co-expressed with VEGF in synovial fluid. Clin Exp Immunol 2000, 119:182-188.
42. Latini C., Frontini A., Morroni M., Marzioni D., Castellucci M., Smith P.G. Remodeling of uterine innervation. Cell Tissue Res 2008, 334:1-6.
43. Brauer M.M. Cellular and molecular mechanisms underlying plasticity in uterine sympathetic nerves. Auton Neurosci 2008, 140:1-16.
44. Weidler C., Holzer C., Harbuz M., Hofbauer R., Angele P., Scholmerich J., et al. Low density of sympathetic nerve fibres and increased density of brain derived neurotrophic factor positive cells in RA synovium. Ann Rheum Dis 2005, 64:13-20.
45. Del Rey A., Wolff C., Wildmann J., Randolf A., Hahnel A., Besedovsky H.O., et al. Disrupted joint-immune-brain communication during experimental arthritis. Arthritis Rheum 2008, 58:3090-3099.
46. Miller L.E., Weidler C., Falk W., Angele P., Schaumburger J., Schölmerich J., et al. Increased prevalence of semaphorin 3C, a repellent of sympathetic nerve fibers, in the synovial tissue of patients with rheumatoid arthritis. Arthritis Rheum 2004, 50:1156-1163.
47. Fassold A., Falk W., Anders S., Hirsch T., Mirsky V.M., Straub R.H. Soluble neuropilin-2, a nerve repellent receptor, is increased in rheumatoid arthritis synovium and aggravates sympathetic fiber repulsion and arthritis. Arthritis Rheum 2009, 60:2892-2901.
48. Zoubina E.V., Fan Q., Smith P.G. Variations in uterine innervation during the estrous cycle in rat. J Comp Neurol 1998, 397:561-571.
49. Schmidt C., Lobos E., Spanel-Borowski K. Pregnancy-induced changes in substance P and neurokinin 1 receptor (NK1-R) expression in the rat uterus. Reproduction 2003, 126:451-458.
50. Dirmeier M., Capellino S., Schubert T., Angele P., Anders S., Straub R.H. Lower density of synovial nerve fibres positive for calcitonin gene-related peptide relative to substance P in rheumatoid arthritis but not in osteoarthritis. Rheumatology (Oxford) 2008, 47:36-40.
51. Fox F.E., Kubin M., Cassin M., Niu Z., Hosoi J., Torii H., et al. Calcitonin gene-related peptide inhibits proliferation and antigen presentation by human peripheral blood mononuclear cells: effects on B7, interleukin 10, and interleukin 12. J Invest Dermatol 1997, 108:43-48.
52. Torii H., Hosoi J., Beissert S., Xu S., Fox F.E., Asahina A., et al. Regulation of cytokine expression in macrophages and the Langerhans cell-like line XS52 by calcitonin gene-related peptide. J Leukoc Biol 1997, 61:216-223.
53. Sen M. Wnt signalling in rheumatoid arthritis. Rheumatology (Oxford) 2005, 44:708-713.
54. Sen M., Lauterbach K., El Gabalawy H., Firestein G.S., Corr M., Carson D.A. Expression and function of wingless and frizzled homologs in rheumatoid arthritis. Proc Natl Acad Sci U S A 2000, 97:2791-2796.
55. Weidler C., Schaumburger J., Miller L.E., Scholmerich J., Straub R.H. Synovial density of frizzled 5-positive cells does not differ between patients with RA and OA and is independent of inflammation. J Rheumatol 2004, 31:1874-1875.
56. Diarra D., Stolina M., Polzer K., Zwerina J., Ominsky M.S., Dwyer D., et al. Dickkopf-1 is a master regulator of joint remodeling. Nat Med 2007, 13:156-163.
57. Pinzone J.J., Hall B.M., Thudi N.K., Vonau M., Qiang Y.W., Rosol T.J., et al. The role of Dickkopf-1 in bone development, homeostasis, and disease. Blood 2009, 113:517-525.
58. Afshar Y., Stanculescu A., Miele L., Fazleabas A.T. The role of chorionic gonadotropin and Notch1 in implantation. J Assist Reprod Genet 2007, 24:296-302.
59. Dunwoodie S.L. The role of Notch in patterning the human vertebral column. Curr Opin Genet Dev 2009, 19:329-337.
60. Ando K., Kanazawa S., Tetsuka T., Ohta S., Jiang X., Tada T., et al. Induction of Notch signaling by tumor necrosis factor in rheumatoid synovial fibroblasts. Oncogene 2003, 22:7796-7803.
61. Nakazawa M., Ishii H., Aono H., Takai M., Honda T., Aratani S., et al. Role of Notch-1 intracellular domain in activation of rheumatoid synoviocytes. Arthritis Rheum 2001, 44:1545-1554.
62. Kijima M., Iwata A., Maekawa Y., Uehara H., Izumi K., Kitamura A., et al. Jagged1 suppresses collagen-induced arthritis by indirectly providing a negative signal in CD8+ T cells. J Immunol 2009, 182:3566-3572.
63. Li X., Cao X. BMP signaling and skeletogenesis. Ann NY Acad Sci 2006, 1068:26-40.
64. Schmidt J.E., Suzuki A., Ueno N., Kimelman D. Localized BMP-4 mediates dorsal/ventral patterning in the early Xenopus embryo. Dev Biol 1995, 169:37-50.
65. Gamer L.W., Nove J., Levin M., Rosen V. BMP-3 is a novel inhibitor of both activin and BMP-4 signaling in Xenopus embryos. Dev Biol 2005, 285:156-168.
66. Lories R.J., Derese I., Ceuppens J.L., Luyten F.P. Bone morphogenetic proteins 2 and 6, expressed in arthritic synovium, are regulated by proinflammatory cytokines and differentially modulate fibroblast-like synoviocyte apoptosis. Arthritis Rheum 2003, 48:2807-2818.
67. Bramlage C.P., Haupl T., Kaps C., Ungethum U., Krenn V., Pruss A., et al. Decrease in expression of bone morphogenetic proteins 4 and 5 in synovial tissue of patients with osteoarthritis and rheumatoid arthritis. Arthritis Res Ther 2006, 8:R58.
68. Reinhold M.I., Kapadia R.M., Liao Z., Naski M.C. The Wnt-inducible transcription factor Twist1 inhibits chondrogenesis. J Biol Chem 2006, 281:1381-1388.
69. Howard T.D., Paznekas W.A., Green E.D., Chiang L.C., Ma N., Ortiz de Luna R.I., et al. Mutations in TWIST, a basic helix-loop-helix transcription factor, in Saethre-Chotzen syndrome. Nat Genet 1997, 15:36-41.
70. Niesner U., Albrecht I., Janke M., Doebis C., Loddenkemper C., Lexberg M.H., et al. Autoregulation of Th1-mediated inflammation by twist1. J Exp Med 2008, 205:1889-1901.
71. Edwards C.J., Francis-West P.H. Bone morphogenetic proteins in the development and healing of synovial joints. Semin Arthritis Rheum 2001, 31:33-42.
72. Bramlage C.P., Kaps C., Ungethum U., Bramlage P., Koziolek M., Wessels J., et al. Modulatory effects of inflammation and therapy on GDF-5 expression in rheumatoid arthritis synovium. Scand J Rheumatol 2008, 37:401-409.
73. Liu F.L., Lin L.H., Sytwu H.K., Chang D.M. GDF-5 is suppressed by IL-1beta and enhances TGF-beta3-mediated chondrogenic differentiation in human rheumatoid fibroblast-like synoviocytes. Exp Mol Pathol 2010, 88:163-170.
74. Inada M., Wang Y., Byrne M.H., Rahman M.U., Miyaura C., Lopez-Otin C., et al. Critical roles for collagenase-3 (Mmp13) in development of growth plate cartilage and in endochondral ossification. Proc Natl Acad Sci USA 2004, 101:17192-17197.
75. Burrage P.S., Mix K.S., Brinckerhoff C.E. Matrix metalloproteinases: role in arthritis. Front Biosci 2006, 11:529-543.
76. Giles W., O'Callaghan S., Read M., Gude N., King R., Brennecke S. Placental nitric oxide synthase activity and abnormal umbilical artery flow velocity waveforms. Obstet Gynecol 1997, 89:49-52.
77. Vossenaar E.R., Despres N., Lapointe E., van der H.A., Lora M., Senshu T., et al. Rheumatoid arthritis specific anti-Sa antibodies target citrullinated vimentin. Arthritis Res Ther 2004, 6:R142-R150.
78. Cutolo M., Picasso M., Ponassi M., Sun M.Z., Balza E. Tenascin and fibronectin distribution in human normal and pathological synovium. J Rheumatol 1992, 19:1439-1447.
79. Chevalier X., Groult N., Larget-Piet B., Zardi L., Hornebeck W. Tenascin distribution in articular cartilage from normal subjects and from patients with osteoarthritis and rheumatoid arthritis. Arthritis Rheum 1994, 37:1013-1022.
80. Glant T.T., Cs-Szabo G., Nagase H., Jacobs J.J., Mikecz K. Progressive polyarthritis induced in BALB/c mice by aggrecan from normal and osteoarthritic human cartilage. Arthritis Rheum 1998, 41:1007-1018.