Decreased lymphatic vessel counts in patients with systemic sclerosis: Association with fingertip ulcers

Arthritis and Rheumatism

Volumn 62, Issue 5, 2010, Pages 1513-1522

  Akhmetshina, Alfiya ^a   Beer, Jürgen ^a   Zwerina, Karin ^a   Englbrecht, Matthias ^a   Palumbo, Katrin ^a   Dees, Clara ^a   Reich, Nicole ^a   Zwerina, Jochen ^a   Szucs, Gabriella ^b   Gusinde, Johannes ^a   Nevskaya, Tatiana ^c   Distler, Oliver ^d   Kerjaschki, Dontscho ^e   Schett, Georg ^a   Distler, Jörg H W ^a  

^a UNIVERSITY OF ERLANGEN NUREMBERG   (Germany)

^b UNIVERSITY OF DEBRECEN   (Hungary)

^c INSTITUTE OF BIOMEDICAL CHEMISTRY   (Russian Federation)

^d UNIVERSITY HOSPITAL ZURICH   (Switzerland)

^e MEDICAL UNIVERSITY OF VIENNA   (Austria)

Author keywords

[No Author keywords available]

Indexed keywords

CD31 ANTIGEN; HOMEODOMAIN PROTEIN; PODOPLANIN; PROTEIN PROX 1; UNCLASSIFIED DRUG;

ADULT; AGED; ARTICLE; BIOPSY TECHNIQUE; CLINICAL ARTICLE; CONTROLLED STUDY; ENDOTHELIUM CELL; FEMALE; HUMAN; HUMAN TISSUE; LYMPH VESSEL; MALE; PRIORITY JOURNAL; SKINFOLD THICKNESS; SYSTEMIC SCLEROSIS; TISSUE INJURY; VASCULAR DISEASE;

ADOLESCENT; ADULT; AGED; ANTIGENS, CD31; BIOPSY; ENDOTHELIAL CELLS; FEMALE; FINGERS; HOMEODOMAIN PROTEINS; HUMANS; LYMPHATIC DISEASES; LYMPHATIC VESSELS; MALE; MEMBRANE GLYCOPROTEINS; MIDDLE AGED; PREVALENCE; SCLERODERMA, SYSTEMIC; SKIN ULCER; TUMOR SUPPRESSOR PROTEINS; YOUNG ADULT;

EID: 77951732927     PISSN: 00043591     EISSN: 15290131     Source Type: Journal    
DOI: 10.1002/art.27406     Document Type: Article

References (41)

1. Varga J, Abraham D. Systemic sclerosis: a prototypic multisystem fibrotic disorder. J Clin Invest 2007;117:557-567 (Pubitemid 46348510)
2. Kahaleh B. Vascular disease in scleroderma: mechanisms of vascular injury. Rheum Dis Clin North Am 2008;34:57-71; vi.
3. Sgonc R, Gruschwitz MS, Dietrich H, Recheis H, Gershwin ME, Wick G. Endothelial cell apoptosis is a primary pathogenetic event underlying skin lesions in avian and human scleroderma. J Clin Invest 1996;98:785-792 (Pubitemid 26349184)
4. Bukhari M, Hollis S, Moore T, Jayson MI, Herrick AL. Quantitation of microcirculatory abnormalities in patients with primary Raynaud's phenomenon and systemic sclerosis by video capillaroscopy. Rheumatology (Oxford) 2000;39:506-512 (Pubitemid 30352954)
5. Cutolo M, Sulli A, Pizzorni C, Accardo S. Nailfold videocapillaroscopy assessment of microvascular damage in systemic sclerosis. J Rheumatol 2000;27:155-160 (Pubitemid 30058643)
6. Distler JH, Gay S, Distler O. Angiogenesis and vasculogenesis in systemic sclerosis. Rheumatology (Oxford) 2006;45 Suppl 3:iii26-7.
7. Guiducci S, Giacomelli R, Cerinic MM. Vascular complications of scleroderma. Autoimmun Rev 2007;6:520-523
8. Kriehuber E, Breiteneder-Geleff S, Groeger M, Soleiman A, Schoppmann SF, Stingl G, et al. Isolation and characterization of dermal lymphatic and blood endothelial cells reveal stable and functionally specialized cell lineages. J Exp Med 2001;194:797-808. (Pubitemid 32983015)
9. Liersch R, Detmar M. Lymphangiogenesis in development and disease. Thromb Haemost 2007;98:304-310
10. Ryan TJ. Structure and function of lymphatics. J Invest Dermatol 1989;93 Suppl:18-24S.
11. Adams RH, Alitalo K. Molecular regulation of angiogenesis and lymphangiogenesis. Nat Rev Mol Cell Biol 2007;8:464-478
12. Mallon EC, Ryan TJ. Lymphedema and wound healing. Clin Dermatol 1994;12:89-93.
13. Karpanen T, Alitalo K. Molecular biology and pathology of lymphangiogenesis. Annu Rev Pathol 2008;3:367-397
14. Tabibiazar R, Cheung L, Han J, Swanson J, Beilhack A, An A, et al. Inflammatory manifestations of experimental lymphatic insufficiency. PLoS Med 2006;3:e254.
15. Alitalo K, Tammela T, Petrova TV. Lymphangiogenesis in development and human disease. Nature 2005;438:946-953
16. LeRoy EC, Medsger TA Jr. Criteria for the classification of early systemic sclerosis. J Rheumatol 2001;28:1573-1576 (Pubitemid 32660630)
17. LeRoy EC, Black C, Fleischmajer R, Jablonska S, Krieg T, Medsger TA Jr, et al. Scleroderma (systemic sclerosis): classification, subsets and pathogenesis. J Rheumatol 1988;15:202-205 (Pubitemid 18073738)
18. Clements P, Lachenbruch P, Seibold J, White B, Weiner S, Martin R, et al. Inter and intraobserver variability of total skin thickness score (modified Rodnan TSS) in systemic sclerosis. J Rheumatol 1995;22:1281-1285
19. Breiteneder-Geleff S, Soleiman A, Horvat R, Amann G, Kowalski H, Kerjaschki D. Podoplanin: a specific marker for lymphatic endothelium expressed in angiosarcoma. Verh Dtsch Ges Pathol 1999;83:270-5. In German.
20. Weninger W, Partanen TA, Breiteneder-Geleff S, Mayer C, Kowalski H, Mildner M, et al. Expression of vascular endothelial growth factor receptor-3 and podoplanin suggests a lymphatic endothelial cell origin of Kaposi's sarcoma tumor cells. Lab Invest 1999;79:243-251 (Pubitemid 29110654)
21. Petrova TV, Makinen T, Makela TP, Saarela J, Virtanen I, Ferrell RE, et al. Lymphatic endothelial reprogramming of vascular endothelial cells by the Prox-1 homeobox transcription factor. EMBO J 2002;21:4593-4599 (Pubitemid 34984346)
22. Albelda SM, Muller WA, Buck CA, Newman PJ. Molecular and cellular properties of PECAM-1 (endoCAM/CD31): a novel vascular cell-cell adhesion molecule. J Cell Biol 1991;114:1059-1068
23. Lampugnani MG, Resnati M, Raiteri M, Pigott R, Pisacane A, Houen G, et al. A novel endothelial-specific membrane protein is a marker of cell-cell contacts. J Cell Biol 1992;118:1511-1522
24. Jackowski S, Janusch M, Fiedler E, Marsch WC, Ulbrich EJ, Gaisbauer G, et al. Radiogenic lymphangiogenesis in the skin. Am J Pathol 2007;171:338-348
25. Roder K, Sieler H. Lymphographic studies in progressive scleroderma. Z Gesamte Inn Med 1972;27:80-2. In German.
26. Leu AJ, Gretener SB, Enderlin S, Bruhlmann P, Michel BA, Kowal-Bielecka O, et al. Lymphatic microangiopathy of the skin in systemic sclerosis. Rheumatology (Oxford) 1999;38:221-227 (Pubitemid 29507157)
27. Distler O, Del Rosso A, Giacomelli R, Cipriani P, Conforti ML, Guiducci S, et al. Angiogenic and angiostatic factors in systemic sclerosis: increased levels of vascular endothelial growth factor are a feature of the earliest disease stages and are associated with the absence of fingertip ulcers. Arthritis Res 2002;4:R11.
28. Distler O, Distler JH, Scheid A, Acker T, Hirth A, Rethage J, et al. Uncontrolled expression of vascular endothelial growth factor and its receptors leads to insufficient skin angiogenesis in patients with systemic sclerosis. Circ Res 2004;95:109-116 (Pubitemid 38931842)
29. Kuwana M, Okazaki Y, Yasuoka H, Kawakami Y, Ikeda Y. Defective vasculogenesis in systemic sclerosis. Lancet 2004;364:603-610
30. Wipff J, Avouac J, Borderie D, Zerkak D, Lemarechal H, Kahan A, et al. Disturbed angiogenesis in systemic sclerosis: high levels of soluble endoglin. Rheumatology (Oxford) 2008;47:972-975 (Pubitemid 351865917)
31. Dor Y, Djonov V, Abramovitch R, Itin A, Fishman GI, Carmeliet P, et al. Conditional switching of VEGF provides new insights into adult neovascularization and pro-angiogenic therapy. EMBO J 2002;21:1939-1947 (Pubitemid 34437191)
32. Chitale S, Al-Mowallad AF, Wang Q, Kumar S, Herrick A. High circulating levels of VEGF-C suggest abnormal lymphangiogenesis in systemic sclerosis. Rheumatology (Oxford) 2008;47:1727-1728
33. Bordron A, Dueymes M, Levy Y, Jamin C, Leroy JP, Piette JC, et al. The binding of some human antiendothelial cell antibodies induces endothelial cell apoptosis. J Clin Invest 1998;101:2029-2035 (Pubitemid 28244086)
34. Worda M, Sgonc R, Dietrich H, Niederegger H, Sundick RS, Gershwin ME, et al. In vivo analysis of the apoptosis-inducing effect of anti-endothelial cell antibodies in systemic sclerosis by the chorionallantoic membrane assay. Arthritis Rheum 2003;48:2605-2614
35. Lunardi C, Bason C, Navone R, Millo E, Damonte G, Corrocher R, et al. Systemic sclerosis immunoglobulin G autoantibodies bind the human cytomegalovirus late protein UL94 and induce apoptosis in human endothelial cells. Nat Med 2000;6:1183-1186
36. Wick N, Saharinen P, Saharinen J, Gurnhofer E, Steiner CW, Raab I, et al. Transcriptomal comparison of human dermal lymphatic endothelial cells ex vivo and in vitro. Physiol Genomics 2007;28:179-192 (Pubitemid 46702006)
37. Kerjaschki D, Huttary N, Raab I, Regele H, Bojarski-Nagy K, Bartel G, et al. Lymphatic endothelial progenitor cells contribute to de novo lymphangiogenesis in human renal transplants. Nat Med 2006;12:230-234 (Pubitemid 43214751)
38. Avouac J, Juin F, Wipff J, Couraud PO, Chiocchia G, Kahan A, et al. Circulating endothelial progenitor cells in systemic sclerosis: association with disease severity. Ann Rheum Dis 2008;67:1455-1460
39. Del Papa N, Colombo G, Fracchiolla N, Moronetti LM, Ingegnoli F, Maglione W, et al. Circulating endothelial cells as a marker of ongoing vascular disease in systemic sclerosis. Arthritis Rheum 2004;50:1296-1304 (Pubitemid 38480841)
40. Del Papa N, Quirici N, Soligo D, Scavullo C, Cortiana M, Borsotti C, et al. Bone marrow endothelial progenitors are defective in systemic sclerosis. Arthritis Rheum 2006;54:2605-2615 (Pubitemid 44205023)
41. Distler JH, Allanore Y, Avouac J, Giacomelli R, Guiducci S, Moritz F, et al. EULAR Scleroderma Trials and Research group statement and recommendations on endothelial precursor cells. Ann Rheum Dis 2009;68:163-168