Anti-CD44-mediated blockade of leukocyte migration in skin-associated immune diseases

Journal of Leukocyte Biology

Volumn 82, Issue 1, 2007, Pages 57-71

  Zöller, Margot ^a,b   Gupta, Pooja ^a   Marhaba, Rachid ^a   Vitacolonna, Mario ^a   Freyschmidt Paul, Pia ^c  

^a GERMAN CANCER RESEARCH CENTER DKFZ   (Germany)

^b UNIVERSITY OF KARLSRUHE   (Germany)

^c UNIVERSITY HOSPITAL MARBURG   (Germany)

Author keywords

Adhesion molecules; Autoimmunity; Cell trafficking; Rodent

Indexed keywords

ALPHA4 INTEGRIN; CD11B ANTIGEN; CD44V ANTIGEN; CHEMOKINE RECEPTOR; HERMES ANTIGEN; INTEGRIN; INTERCELLULAR ADHESION MOLECULE 1;

ALOPECIA AREATA; ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; CELL HOMING; ECZEMA; EFFECTOR CELL; ENDOTHELIUM CELL; EXTRAVASATION; IMMUNOPATHOLOGY; IN VITRO STUDY; IN VIVO STUDY; LEUKOCYTE; LEUKOCYTE MIGRATION; LYMPH NODE; MACROPHAGE MIGRATION; MONOCYTE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; T LYMPHOCYTE;

ALLERGENS; ALOPECIA AREATA; ANIMALS; ANTIBODIES, MONOCLONAL; ANTIGENS, CD44; CELL ADHESION MOLECULES; CHEMOTAXIS, LEUKOCYTE; ECZEMA; IMMUNE SYSTEM DISEASES; MICE; PROTEIN ISOFORMS; SKIN DISEASES;

MUS; RODENTIA;

EID: 34347389899     PISSN: 07415400     EISSN: None     Source Type: Journal    
DOI: 10.1189/jlb.0107063     Document Type: Article

References (75)

1. McElwee, K. J., Tobin, D. J., Bystryn, J. C., King Jr., L. E., Sundberg, J. P. (1999) Alopecia areata: an autoimmune disease? Exp. Dermatol. 8, 371-379.
2. Ito, T., Ito, N., Bettermann, A., Tokura, Y., Takigawa, M., Paus, R. (2004) Collapse and restoration of MHC class-I-dependent immune privilege: exploiting the human hair follicle as a model. Am. J. Pathol. 164, 623-634.
3. Happle, R., Echternacht, K. (1977) Induction of hair growth in alopecia areata with D.N.C.B. Lancet 2, 1002-1003.
4. Freyschmidt-Paul, P., Happle, R., McElwee, K. J., Hoffmann, R. (2003) Alopecia areata: treatment of today and tomorrow. J. Investig. Dermatol. Symp. Proc. 8, 12-17.
5. Dall'oglio, F., Nasca, M. R., Musumeci, M. L., La Torre, G., Ricciardi, G., Potenza, C., Micali, G. (2005) Topical immunomodulator therapy with squaric acid dibutylester (SADBE) is effective treatment for severe alopecia areata (AA): results of an open-label, paired-comparison, clinical trial. J. Dermatolog. Treat. 16, 10-14.
6. McElwee, K. J., Boggess, D., King Jr., L. E., Sundberg, J. P. (1998) Experimental induction of alopecia areata-like hair loss in C3H/HeJ mice using full-thickness skin grafts. J. Invest. Dermatol. 111, 797-803.
7. McElwee, K. J., Yu, M., Park, S. W., Ross, E. K., Finner, A., Shapiro, J. (2005) What can we learn from animal models of alopecia areata? Dermatology 211, 47-53.
8. Freyschmidt-Paul, P., Sundberg, J. P., Happle, R., McElwee, K. J., Metz, S., Boggess, D., Hoffmann, R. (1999) Successful treatment of alopecia areata-like hair loss with the contact sensitizer squaric acid dibutylester (SADBE) in C3H/HeJ mice. J. Invest. Dermatol. 113, 61-68.
9. Zöller, M., Freyschmidt-Paul, P., Vitacolonna, M., McElwee, K. J., Hummel, S., Hoffmann, R. (2004) Chronic delayed-type hypersensitivity reaction as a means to treat alopecia areata. Clin. Exp. Immunol. 135, 398-408.
10. Gupta, P., Freyschmidt-Paul, P., Vitacolonna, M., Kiessling, S., Hummel, S., Hildebrand, D., Marhaba, R., Zöller, M. (2006) A chronic contact eczema impedes migration of antigen presenting cells in alopecia areata. J. Invest. Dermatol. 126, 1559-1573.
11. Freyschmidt-Paul, P., Seiter, S., Zöller, M., König, A., Ziegler, A., Sundberg, J. P., Happle, R., Hoffmann, R. (2000) Treatment with an anti-CD44v10-specific antibody inhibits the onset of alopecia areata in C3H/HeJ mice. J. Invest. Dermatol. 115, 653-657.
12. Rösel, M., Seiter, S., Zöller, M. (1997) CD44v10 expression in the mouse and functional activity in delayed type hypersensitivity. J. Cell. Physiol. 171, 305-317.
13. Goldstein, L. A., Zhou, D. F., Picker, L. J., Minty, C. N., Bargatze, R. F., Ding, J. F., Butcher, E. C. (1989) A human lymphocyte homing receptor, the hermes antigen, is related to cartilage proteoglycan core and link proteins. Cell 56, 1063-1072.
14. Katakai, T., Hara, T., Sugai, M., Gonda, H., Nambu, Y., Matsuda, E., Agata, Y., Shimizu, A. (2002) Chemokine-independent preference for T-helper-1 cells in transendothelial migration. J. Biol. Chem. 277, 50948-50958.
15. Grabbe, S., Varga, G., Beissert, S., Steinert, M., Pendl, G., Seeliger, S., Bloch, W., Peters, T., Schwarz, T., Sunderkotter, C., Scharffetter-Kochanek, K. (2002) β2 integrins are required for skin homing of primed T cells but not for priming naive T cells. J. Clin. Invest. 109, 183-192.
16. Gee, K., Kozlowski, M., Kumar, A. (2003) Tumor necrosis factor-α induces functionally active hyaluronan-adhesive CD44 by activating sialidase through p38 mitogen-activated protein kinase in lipopolysaccharide-stimulated human monocytic cells. J. Biol. Chem. 278, 37275-37287.
17. Leemans, J. C., Florquin, S., Heikens, M., Pals, S. T., van der Neut, R., Van Der Poll, T. (2003) CD44 is a macrophage binding site for Mycobacterium tuberculosis that mediates macrophage recruitment and protective immunity against tuberculosis. J. Clin. Invest. 111, 681-689.
18. Camp, R. L., Scheynius, A., Johansson, C., Pure, E. (1993) CD44 is necessary for optimal contact allergic responses but is not required for normal leukocyte extravasation. J. Exp. Med. 178, 497-507.
19. Stoop, R., Gal, I., Glant, T. T., McNeish, J. D., Mikecz, K. (2002) Trafficking of CD44-deficient murine lymphocytes under normal and inflammatory conditions. Eur. J. Immunol. 32, 2532-2542.
20. Aruffo, A., Stamenkovic, I., Melnick, M., Underhill, C. B., Seed, B. (1990) CD44 is the principal cell surface receptor for hyaluronate. Cell 61, 1303-1313.
21. Lesley, J., Hyman, R. (1992) CD44 can be activated to function as an hyaluronic acid receptor in normal murine T cells. Eur. J. Immunol. 22, 2719-2723.
22. DeGrendele, H. C., Estess, P., Picker, L. J., Siegelman, M. H. (1996) CD44 and its ligand hyaluronate mediate rolling under physiologic flow, a novel lymphocyte-endothelial cell primary adhesion pathway. J. Exp. Med. 183, 1119-1130.
23. DeGrendele, H. C., Kosfiszer, M., Estess, P., Siegelman, M. H. (1997) CD44 activation and associated primary adhesion is inducible via T cell receptor stimulation. J. Immunol. 159, 2549-2553.
24. DeGrendele, H. C., Estess, P., Siegelman, M. H. (1997) Requirement for CD44 in activated T cell extravasation into an inflammatory site. Science 278, 672-675.
25. Dunon, D., Piali, L., Imhof, B. A. (1996) To stick or not to stick: the new leukocyte homing paradigm. Curr. Opin. Cell Biol. 8, 714-723.
26. Estess, P., DeGrendele, H. C., Pascual, V., Siegelman, M. H. (1998) Functional activation of lymphocyte CD44 in peripheral blood is a marker of autoimmune disease activity. J. Clin. Invest. 102, 1173-1182.
27. Mohamadzadeh, M., DeGrendele, H., Arizpe, H., Estess, P., Siegelman, M. H. (1998) Proinflammatory stimuli regulate endothelial hyaluronan expression and CD44/HA-dependent primary adhesion. J. Clin. Invest. 101, 97-108.
28. Gee, K., Lim, W., Ma, W., Nandan, D., Diaz-Mitoma, F., Kozlowski, M., Kumar, A. (2002) Differential regulation of CD44 expression by lipopolysaccharide (LPS) and TNF-α in human monocytic cells: distinct involvement of c-Jun N-terminal kinase in LPS-induced CD44 expression. J. Immunol. 169, 5660-5672.
29. Nandi, A., Estess, P., Siegelman, M. H. (2004) Bimolecular complex between rolling and firm adhesion receptors required for cell arrest; CD44 association with VLA-4 in T cell extravasation. Immunity 20, 455-465.
30. Weber, G. F., Ashkar, S., Glimcher, M. J., Cantor, H. (1996) Receptor-ligand interaction between CD44 and osteopontin (Eta-1). Science 271, 509-512.
31. Katagiri, Y. U., Sleeman, J., Fujii, H., Herrlich, P., Hotta, K., Tanaka, K., Chikuma, S., Yagita, H., Okumura, K., Murakami, M., Saiki, I., Chambers, A. F., Uede, T. (1999) CD44 variants but not CD44s cooperate with β1-containing integrins to permit cells to bind to osteopontin independently of arginine-glycine-aspartic acid, thereby stimulating cell motility and chemotaxis. Cancer Res. 59, 219-226.
32. Weber, G. F., Zawaideh, S., Hikita, S., Kumar, V. A., Cantor, H., Ashkar, S. (2002) Phosphorylation-dependent interaction of osteopontin with its receptors regulates macrophage migration and activation. J. Leukoc. Biol. 72, 752-761.
33. Weiss, J. M., Renkl, A. C., Maier, C. S., Kimmig, M., Liaw, L., Ahrens, T., Kon, S., Maeda, M., Hotta, H., Uede, T., Simon, J. C. (2001) Osteopontin is involved in the initiation of cutaneous contact hypersensitivity by inducing Langerhans and dendritic cell migration to lymph nodes. J. Exp. Med. 194, 1219-1229.
34. Suzuki, K., Zhu, B., Rittling, S. R., Denhardt, D. T., Goldberg, H. A., McCulloch, C. A., Sodek, J. (2002) Colocalization of intracellular osteopontin with CD44 is associated with migration, cell fusion, and resorption in osteoclasts. J. Bone Miner. Res. 17, 1486-1497.
35. Zohar, R., Suzuki, N., Suzuki, K., Arora, P., Glogauer, M., McCulloch, C. A., Sodek, J. (2000) Intracellular osteopontin is an integral component of the CD44-ERM complex involved in cell migration. J. Cell. Physiol. 184, 118-130.
36. Roscic-Mrkic, B., Fischer, M., Leemann, C., Manrique, A., Gordon, C. J., Moore, J. P., Proudfoot, A. E., Trkola, A. (2003) RANTES (CCL5) uses the proteoglycan CD44 as an auxiliary receptor to mediate cellular activation signals and HIV-1 enhancement. Blood 102, 1169-1177.
37. Charnaux, N., Brule, S., Chaigneau, T., Saffar, L., Sutton, A., Hamon, M., Prost, C., Lievre, N., Gattegno, L. (2005) RANTES (CCL5) induces a CCR5-dependent accelerated shedding of syndecan-1 (CD138) and syndecan-4 from HeLa cells and forms complexes with the shed ectodomains of these proteoglycans as well as with those of CD44. Glycobiology 15, 119-130.
38. Marhaba, R., Bourouba, M., Zöller, M. (2005) CD44v6 promotes proliferation by persisting activation of MAP kinases. Cell. Signal. 17, 961-973.
39. Föger, N., Marhaba, R., Zöller, M. (2000) CD44 supports T cell proliferation and apoptosis by apposition of protein kinases. Eur. J. Immunol. 30, 2888-2899.
40. Marhaba, R., Freyschmidt-Paul, P., Zöller, M. (2006) In vivo CD44-CD49d complex formation in autoimmune disease has consequences on T cell activation and apoptosis resistance. Eur. J. Immunol. 36, 3017-3032.
41. Wang, S. J., Greer, P., Auerbach, R. (1996) Isolation and propagation of yolk-sac-derived endothelial cells from a hypervascular transgenic mouse expressing a gain-of-function fps/fes proto-oncogene. In Vitro Cell. Dev. Biol. Anim. 32, 292-299.
42. Picker, L. J., De los Toyos, J., Telen, M. J., Haynes, B. F., Butcher, E. C. (1989) Monoclonal antibodies against the CD44 [In(Lu)-related p80], and Pgp-1 antigens in man recognize the Hermes class of lymphocyte homing receptors. J. Immunol. 142, 2046-2051.
43. Zheng, Z., Katoh, S., He, Q., Oritani, K., Miyake, K., Lesley, J., Hyman, R., Hamik, A., Parkhouse, R. M., Farr, A. G. (1995) Monoclonal antibodies to CD44 and their influence on hyaluronan recognition. J. Cell Biol. 130, 485-495.
44. Hession, C., Moy, P., Tizard, R., Chisholm, P., Williams, C., Wysk, M., Burkly, L., Miyake, K., Kincade, P., Lobb, R. (1992) Cloning of murine and rat vascular cell adhesion molecule-1. Biochem. Biophys. Res. Commun. 183, 163-169.
45. Gonda, A., Gal, I., Szanto, S., Sarraj, B., Glant, T. T., Hunyadi, J., Mikecz, K. (2005) CD44, but not l-selectin, is critically involved in leucocyte migration into the skin in a murine model of allergic dermatitis. Exp. Dermatol. 14, 700-708.
46. Seiter, S., Schadendorf, D., Tilgen, W., Zöller, M. (1998) CD44 variant isoform expression in a variety of skin-associated autoimmune diseases. Clin. Immunol. Immunopathol. 89, 79-93.
47. Steeber, D. A., Venturi, G. M., Tedder, T. F. (2005) A new twist to the leukocyte adhesion cascade: intimate cooperation is key. Trends Immunol. 26, 9-12.
48. Freeman, C. M., Chiu, B. C., Stolberg, V. R., Hu, J., Zeibecoglou, K., Lukacs, S. A., Lira, N. W., Kunkel, S. L., Chensue, S. W. (2005) CCR8 is expressed by antigen-elicited, IL-10-producing CD4+CD25+ T cells, which regulate Th2-mediated granuloma formation in mice. J. Immunol. 174, 1962-1970.
49. Shimonaka, M., Katagiri, K., Nakayama, T., Fujita, N., Tsuruo, T., Yoshie, O., Kinashi, T. (2003) Rap1 translates chemokine signals to integrin activation, cell polarization, and motility across vascular endothelium under flow. J. Cell Biol. 161, 417-427.
50. Rouschop, K. M., Roelofs, J. J., Claessen, N., da Costa Martins, P., Zwaginga, J. J., Pals, S. T., Weening, J. J., Florquin, S. (2005) Protection against renal ischemia reperfusion injury by CD44 disruption. J. Am. Soc. Nephrol. 16, 2034-2043.
51. Toole, B. P. (2004) Hyaluronan: from extracellular glue to pericellular cue. Nat. Rev. Cancer 4, 528-539.
52. Gilhar, A., Kalish, R. R. (2006) Alopecia areata: a tissue specific autoimmune disease of the hair follicle. Autoimmun. Rev. 5, 64-69.
53. Tesch, G. H., Maifert, S., Schwarting, A., Rollins, B. J., Kelley, V. R. (1999) Monocyte chemoattractant protein 1-dependent leukocytic infiltrates are responsible for autoimmune disease in MRL-Fas(lpr) mice. J. Exp. Med. 190, 1813-1824.
54. Kapp, A., Werfel, T. (1999) Allergic inflammation: skin. Allergy 54 (Suppl. 56), 23-24.
55. Nandi, A., Estess, P., Siegelman, M. H. (2000) Hyaluronan anchoring and regulation on the surface of vascular endothelial cells is mediated through the functionally active form of CD44. J. Biol. Chem. 275, 14939-14948.
56. Guo, Y., Wu, Y., Shinde, S., Sy, M. S., Aruffo, A., Liu, Y. (1996) Identification of a costimulatory molecule rapidly induced by CD40L as CD44H. J. Exp. Med. 184, 955-961.
57. McElwee, K. J., Freyschmidt-Paul, P., Hoffmann, R., Kissling, S., Hummel, S., Vitacolonna, M., Zöller, M. (2005) Transfer of CD8(+) cells induces localized hair loss whereas CD4(+)/CD25(-) cells promote systemic alopecia areata and CD4(+)/CD25(+) cells blockade disease onset in the C3H/HeJ mouse model. J. Invest. Dermatol. 124, 947-957.
58. Wagner, S. N., Wagner, C., Reinhold, U., Funk, R., Zöller, M., Goos, M. (1998) Predominant expression of CD44 splice variant v10 in malignant and reactive human skin lymphocytes. J. Invest. Dermatol. 111, 464-471.
59. Yoshinari, C., Mizusawa, N., Byers, H. R., Akasaka, T. (1999) CD44 variant isoform CD44v10 expression of human melanoma cell lines is upregulated by hyaluronate and correlates with migration. Melanoma Res. 9, 223-231.
60. Lesley, J., Hyman, R., Kincade, P. W. (1993) CD44 and its interaction with extracellular matrix. Adv. Immunol. 54, 271-335.
61. Avin, E., Haimovich, J., Hollander, N. (2004) Anti-idiotype x anti-CD44 bispecific antibodies inhibit invasion of lymphoid organs by B cell lymphoma. J. Immunol. 173, 4736-4743.
62. Shi, M., Dennis, K., Peschon, J. J., Chandrasekaran, R., Mikecz, K. (2001) Antibody-induced shedding of CD44 from adherent cells is linked to the assembly of the cytoskeleton. J. Immunol. 167, 123-131.
63. Mikecz, K., Dennis, K., Shi, M., Kim, J. H. (1999) Modulation of hyaluronan receptor (CD44) function in vivo in a murine model of rheumatoid arthritis. Arthritis Rheum. 42, 659-668.
64. Stein, J. V., Nombela-Arrieta, C. (2005) Chemokine control of lymphocyte trafficking: a general overview. Immunology 116, 1-12.
65. Wenzel, J., Henze, S., Worenkamper, E., Basner-Tschakarjan, E., Sokolowska-Wojdylo, M., Steitz, J., Bieber, T., Tuting, T. (2005) Role of the chemokine receptor CCR4 and its ligand thymus- and activation-regulated chemokine/CCL17 for lymphocyte recruitment in cutaneous lupus erythematosus. J. Invest. Dermatol. 124, 1241-1248.
66. Dieu-Nosjean, M. C., Massacrier, C., Homey, B., Vanbervliet, B., Pin, J. J., Vicari, A., Lebecque, S., Dezutter-Dambuyant, C., Schmitt, D., Zlotnik, A., Caux, C. (2000) Macrophage inflammatory protein 3α is expressed at inflamed epithelial surfaces and is the most potent chemokine known in attracting Langerhans cell precursors. J. Exp. Med. 192, 705-718.
67. Campbell, J. J., Hedrick, J., Zlotnik, A., Siani, M. A., Thompson, D. A., Butcher, E. C. (1998) Chemokines and the arrest of lymphocytes rolling under flow conditions. Science 279, 381-384.
68. Millan, J., Montoya, M. C., Sancho, D., Sanchez-Madrid, F., Alonso, M. D. (2002) Lipid rafts mediate biosynthetic transport to the T lymphocyte uropod subdomain and are necessary for uropod integrity and function. Blood 99, 978-984.
69. Shimonaka, M., Katagiri, K., Nakayama, T., Fujita, N., Tsuruo, T., Yoshie, O., Kinashi, T. (2003) Rap1 translates chemokine signals to integrin activation, cell polarization, and motility across vascular endothelium under flow. J. Cell Biol. 161, 417-427.
70. Lee, J. H., Katakai, T., Hara, T., Gonda, H., Sugai, M., Shimizu, A. (2004) Roles of p-ERM and Rho-ROCK signaling in lymphocyte polarity and uropod formation. J. Cell Biol. 167, 327-337.
71. Tsukita, S., Oishi, K., Sato, N., Sagara, J., Kawai, A., Tsukita, S. (1994) ERM family members as molecular linkers between the cell surface glycoprotein CD44 and actin-based cytoskeletons. J. Cell Biol. 126, 391-401.
72. Legg, J. W., Lewis, C. A., Parsons, M., Ng, T., Isacke, C. M. (2002) A novel PKC-regulated mechanism controls CD44 ezrin association and directional cell motility. Nat. Cell Biol. 4, 399-407.
73. Del Pozo, M. A., Vicente-Manzanares, M., Tejedor, R., Serrador, J. M., Sanches-Madrid, F. (1999) Rho GTPases control migration and polarization of adhesion molecules and cytoskeletal ERM components in T lymphocytes. Eur. J. Immunol. 29, 3609-3620.
74. Seveau, S., Eddy, R. J., Maxfield, F. R., Pierini, L. M. (2001) Cytoskeleton-dependent membrane domain segregation during neutrophil polarization. Mol. Biol. Cell 12, 3550-3562.
75. Föger, N., Marhaba, R., Zöller, M. (2001) Involvement of CD44 in cytoskeleton rearrangement and raft reorganization in T cells. J. Cell Sci. 114, 1169-1178.