RHAMM, a receptor for hyaluronan-mediated motility, compensates for CD44 in inflamed CD44-knockout mice: A different interpretation of redundancy (original) (raw)

Abstract

We report here that joint inflammation in collagen-induced arthritis is more aggravated in CD44-knockout mice than in WT mice, and we provide evidence for molecular redundancy as a causal factor. Furthermore, we show that under the inflammatory cascade, RHAMM (receptor for hyaluronan-mediated motility), a hyaluronan receptor distinct from CD44, compensates for the loss of CD44 in binding hyaluronic acid, supporting cell migration, up-regulating genes involved with inflammation (as assessed by microarrays containing 13,000 cDNA clones), and exacerbating collagen-induced arthritis. Interestingly, we further found that the compensation for loss of the CD44 gene does not occur because of enhanced expression of the redundant gene (RHAMM), but rather because the loss of CD44 allows increased accumulation of the hyaluronic acid substrate, with which both CD44 and RHAMM engage, thus enabling augmented signaling through RHAMM. This model enlightens several aspects of molecular redundancy, which is widely discussed in many scientific circles, but the processes are still ill defined.

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References (48)

  1. Devalaraja, M. N. & Richmond, A. (1999) Trends Pharmacol. Sci. 20, 151-156.
  2. Muoio, D. M., MacLean, P. S., Lang, D. B., Li, S., Houmard, J. A., Way, J. M., Winegar, D. A., Corton, J. C., Dohm, G. L. & Kraus, W. E. (2002) J. Biol. Chem. 277, 26089-260997.
  3. Ozaki, K. & Leonard, W. J. (2002) J. Biol. Chem. 277, 29355-29358.
  4. Taylor, N. A., van De Ven, W. J. M. & Creemers, J. W. M. (2003) FASEB J. 17, 1215-1227.
  5. Luross, J. A. & Williams, N. A. (2001) Immunology 103, 407-416.
  6. van Noort, J. M. & Amor, S. (1998) Int. Rev. Cytol. 178, 127-206.
  7. Naor, D., Nedvetzki, S., Golan, I., Melnik, L. & Faitelson, Y. (2002) Crit. Rev. Clin. Lab. Sci. 39, 527-579.
  8. Lesley, J., Hyman, R. & Kincade, P. W. (1993) Adv. Immunol. 54, 271-335.
  9. Naor, D., Vogt-Sionov, R. & Ish-Shalom, D. (1997) Adv. Cancer Res. 71, 241-319.
  10. Tammi, M. I., Day, A. J. & Turley, E. A. (2002) J. Biol. Chem. 277, 4581-4584.
  11. DeGrendele, H. C., Kosfiszer, M., Estess, P. & Siegelman, M. H. (1997) J. Immunol. 159, 2549-2553.
  12. Mohamadzadeh, M., DeGrendele, H., Arizpe, H., Estess, P. & Siegelman, M. (1998) J. Clin. Invest. 101, 97-108.
  13. Day, A. J. & Prestwich, G. D. (2002) J. Biol. Chem. 277, 4585-4588.
  14. Zhang, S., Chang, M. C. Y., Zylka, D., Turley, S., Harrison, R. & Turley, E. A. (1998) J. Biol. Chem. 273, 11342-11348.
  15. Akiyama, Y., Jung, S., Salhia, B., Lee, S., Hubbard, S., Taylor, M., Mainprize, T., Akaishi, K., van Furth, W. & Rutka, J. T. (2001) J. Neuro-Oncol. 53, 115-127.
  16. Lynn, B. D., Turley, E. A. & Nagy, J. I. (2001) J. Neurosci. Res. 65, 6-16.
  17. Turley, E. A., Noble, P. W. & Bourguignon, L. Y. W. (2002) J. Biol. Chem. 277, 4589-4592.
  18. Mohapatra, S., Yang, X., Wright, J. A., Turley, E. A. & Greenberg, A. H. (1996) J. Exp. Med. 183, 1663-1668.
  19. Cheung, W. F., Cruz, T. F. & Turley, E. A. (1999) Biochem. Soc. Trans. 27, 135-142.
  20. Mikecz, K., Brennan, F. R., Kim, J. H. & Glant, T. T. (1995) Nat. Med. 1, 558-563.
  21. Nedvetzki, S., Walmsley, M., Alpert, E., Williams, R. O., Feldmann, M. & Naor, D. (1999) J. Autoimmun. 13, 39-47.
  22. Wittig, B., Schwa ¨rzler, C., Fo ¨hr, N., Gu ¨nthert, U. & Zo ¨ller, M. (1998) J. Immunol. 161, 1069-1073.
  23. Brocke, S., Piercy, C., Steinman, L., Weissman, I. L. & Veromaa, T. (1999) Proc. Natl. Acad. Sci. USA 96, 5896-6901.
  24. Weiss, L., Slavin, S., Reich, S., Cohen, P., Shuster, S., Stern, R., Kaganovsky, E., Okon, E., Rubinstein, A. M. & Naor, D. (2000) Proc. Natl. Acad. Sci. USA 97, 285-290.
  25. Trowbridge, I. S., Lesley, J., Schulte, R., Hyman, R. & Trotter, J. (1982) Immunogenetics 15, 299-312.
  26. Miyake, K., Medina, K. L., Hayashi, S., Ono, S., Hamaoka, T. & Kincade, P. W. (1990) J. Exp. Med. 171, 477-488.
  27. Maloney, D. G., Kaminski, M. S., Burowski, D., Haimovich, J. & Levy, R. (1985) Hybridoma 4, 191-209.
  28. Pilarski, L. M., Pruski, E., Wizniak, J., Paine, D., Seeberger, K., Mant, M. J., Brown, C. B. & Belch, A. R. (1999) Blood 93, 2918-2927.
  29. Schmits, R., Filmus, J., Gerwin, N., Senaldi, G., Kiefer, F., Kundig, T., Wakeham, A., Shahinian, A., Catzavelos, C., Rak, J., et al. (1997) Blood 90, 2217-2233.
  30. Miller, E. J. (1972) Biochemistry 11, 4903-4909.
  31. Bonaventure, P., Guo, H., Tian, B., Liu, X., Bittner, A., Roland, B., Salunga, R., Ma, X. J., Kamme, F., Meurers, B., et al. (2002) Brain Res. 943, 38-47.
  32. Shaw, K. J., Miller, N., Liu, X., Lerner, D., Wan, J., Bittner, A. & Morrow, B. J. (2003) J. Mol. Microbiol. Biotechnol. 5, 105-122.
  33. Reich, R., Thompson, E. W., Iwamoto, Y., Martin, G. R., Deason, J. R., Fuller, G. C. & Miskin, R. (1988) Cancer Res. 48, 3307-3312.
  34. Nedvetzki, S., Golan, I., Assayag, N., Gonen, E., Caspi, D., Gladnikoff, M., Yayon, A. & Naor, D. (2003) J. Clin. Invest. 111, 1211-1220.
  35. Protin, U., Schweighoffer, T., Jochum, W. & Hilberg, F. (1999) J. Immunol. 163, 4917-4923.
  36. Stoop, R., Kotani, H., McNeish, J. D., Otterness, I. G. & Mikecz, K. (2001) Arthritis Rheum. 44, 2922-2931.
  37. Knudson, W., Chow, G. & Knudson, C. B. (2002) Matrix Biol. 21, 15-23.
  38. Hofmann, M., Fieber, C., Assmann, V., Gottlicher, M., Sleeman, J., Plug, R., Howel von Stein, O., Ponta, H. & Herrlich, P. (1998) J. Cell Sci. 111, 1673-1684.
  39. Assmann, V., Marshall, J. F., Fieber, C., Hofmann, M. & Hart, I. R. (1998) J. Cell Sci. 111, 1685-1694.
  40. Yang, B., Hall, C. L., Yang, B. L., Savani, R. C. & Turley, E. A. (1994) J. Cell Biochem. 56, 455-468.
  41. Savani, R. C., Wang, C., Yang, B., Zhang, S., Kinsella, M. G., Wight, T. N., Stern, R., Nance, D. M. & Turley, E. A. (1995) J. Clin. Invest. 95, 1158-1168.
  42. Avigdor, A., Goichberg, P., Shivtiel, S., Dar, A., Peled, A., Samira, S., Kollet, O., Hershkoviz, R., Alon, R., Hardan, I., et al. (2004) Blood 103, 2981-2989.
  43. Nagy, J. I., Hossain, M. Z., Lynn, B. D., Curpen, G. E., Yang, S. & Turley, E. A. (1996) Cell Growth Differ. 7, 745-751.
  44. Hall, C. L., Collis, L. A., Bo, A. J., Lange, L., McNicol, A., Gerrard, J. M. & Turley, E. A. (2001) Matrix Biol. 20, 183-192.
  45. Teder, P., Vandivier, R. W., Jiang, D., Liang, J., Cohn, L., Pure, E., Henson, P. M. & Noble, P. W. (2002) Science 296, 155-158.
  46. Wittig, B. M., Johansson, B., Zoller, M., Schwarzler, C. & Gunthert, U. (2000) J. Exp. Med. 191, 2053-2064.
  47. Correction IMMUNOLOGY. For the article ''RHAMM, a receptor for hyalu- ronan-mediated motility, compensates for CD44 in inflamed CD44-knockout mice: A different interpretation of redun- dancy,'' by Shlomo Nedvetzki, Erez Gonen, Nathalie Assayag, Reuven Reich, Richard O. Williams, Robin L. Thurmond, Jing-Feng Huang, Birgit A. Neudecker, Fu-Shang Wang, Eva A. Turley, and David Naor, which appeared in issue 52, December 28, 2004, of Proc. Natl. Acad. Sci. USA (101, 18081-18086; first published December 13, 2004; 10.1073͞pnas.0407378102), the name Fu-Shang Wang should have appeared as Fu-Sheng Wang. The online version has been corrected. The corrected author line appears below.
  48. Shlomo Nedvetzki, Erez Gonen, Nathalie Assayag, Reuven Reich, Richard O. Williams, Robin L. Thurmond, Jing-Feng Huang, Birgit A. Neudecker, Fu-Sheng Wang, Eva A. Turley, and David Naor www.pnas.org͞cgi͞doi͞10.1073͞pnas.0409514102