Inhibitor of DASH proteases affects expression of adhesion molecules in osteoclasts and reduces myeloma growth and bone disease

British Journal of Haematology

Volumn 145, Issue 6, 2009, Pages 775-787

  Pennisi, Angela ^b,c   Li, Xin ^b   Ling, Wen ^b   Khan, Sharmin ^b   Gaddy, Dana ^b   Suva, Larry J ^b   Barlogie, Bart ^b   Shaughnessy, John D ^b   Aziz, Nazneen ^d   Yaccoby, Shmuel ^a,b  

^a UNIVERSITY OF ARKANSAS FOR MEDICAL SCIENCES   (United States)

^b UNIVERSITY OF ARKANSAS FOR MEDICAL SCIENCES   (United States)

^c UNIVERSITY OF CATANIA   (Italy)

^d Point Therapeutics   (United States)

Author keywords

DPPIV proteases; Fibroblast activation protein; Microenvironment; Myeloma; Osteoclasts

Indexed keywords

CELL ADHESION MOLECULE; DIPEPTIDYL PEPTIDASE 4 ACTIVITY AND STRUCTURE HOMOLOGUES; DIPEPTIDYL PEPTIDASE IV; SERINE PROTEINASE INHIBITOR; TALABOSTAT; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; BONE DISEASE; CELL CULTURE; CONTROLLED STUDY; DRUG EFFECT; DRUG INHIBITION; MOUSE; MYELOMA; NONHUMAN; OSTEOCLAST; PRIORITY JOURNAL; PROTEIN EXPRESSION; REAL TIME POLYMERASE CHAIN REACTION;

ALKALINE PHOSPHATASE; ANIMALS; BONE DENSITY; BONE RESORPTION; BORONIC ACIDS; CELL ADHESION MOLECULES; CELL DIFFERENTIATION; COCULTURE TECHNIQUES; DIPEPTIDES; DIPEPTIDYL PEPTIDASES; GENE EXPRESSION; GENE EXPRESSION PROFILING; HUMANS; IMMUNOGLOBULIN LIGHT CHAINS; IMMUNOHISTOCHEMISTRY; MICE; MICE, SCID; MULTIPLE MYELOMA; NF-KAPPA B; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; OSTEOCLASTS; P38 MITOGEN-ACTIVATED PROTEIN KINASES; PHOSPHORYLATION; TUMOR MARKERS, BIOLOGICAL;

EID: 66849104453     PISSN: 00071048     EISSN: 13652141     Source Type: Journal    
DOI: 10.1111/j.1365-2141.2009.07696.x     Document Type: Article

References (49)

1. Abe, M., Hiura, K., Wilde, J., Shioyasono, A., Moriyama, K., Hashimoto, T., Kido, S., Oshima, T., Shibata, H., Ozaki, S., Inoue, D. Matsumoto, T. (2004) Osteoclasts enhance myeloma cell growth and survival via cell-cell contact: a vicious cycle between bone destruction and myeloma expansion. Blood, 104, 2484 2491. (Pubitemid 39331851)
2. Adams, S., Miller, G.T., Jesson, M.I., Watanabe, T., Jones, B. Wallner, B.P. (2004) PT-100, a small molecule dipeptidyl peptidase inhibitor, has potent antitumour effects and augments antibody-mediated cytotoxicity via a novel immune mechanism. Cancer Research, 64, 5471 5480. (Pubitemid 39006571)
3. Aggarwal, S., Brennen, W.N., Kole, T.P., Schneider, E., Topaloglu, O., Yates, M., Cotter, R.J. Denmeade, S.R. (2008) Fibroblast activation protein peptide substrates identified from human collagen I derived gelatin cleavage sites. Biochemistry, 47, 1076 1086.
4. Asagiri, M. Takayanagi, H. (2007) The molecular understanding of osteoclast differentiation. Bone, 40, 251 264. (Pubitemid 46054562)
5. Bataille, R., Chappard, D., Marcelli, C., Dessauw, P., Baldet, P., Sany, J. Alexandre, C. (1991) Recruitment of new osteoblasts and osteoclasts is the earliest critical event in the pathogenesis of human multiple myeloma. Journal of Clinical Investigation, 88, 62 66.
6. Bauer, S., Jendro, M.C., Wadle, A., Kleber, S., Stenner, F., Dinser, R., Reich, A., Faccin, E., Godde, S., Dinges, H., Muller-Ladner, U. Renner, C. (2006) Fibroblast activation protein is expressed by rheumatoid myofibroblast-like synoviocytes. Arthritis Research & Theraphy, 8, R171.
7. Bendre, M.S., Montague, D.C., Peery, T., Akel, N.S., Gaddy, D. Suva, L.J. (2003) Interleukin-8 stimulation of osteoclastogenesis and bone resorption is a mechanism for the increased osteolysis of metastatic bone disease. Bone, 33, 28 37. (Pubitemid 36952685)
8. Caers, J., Gunthert, U., De Raeve, H., Van Valckenborgh, E., Menu, E., Van Riet, I., Van Camp, B. Vanderkerken, K. (2006) The involvement of osteopontin and its receptors in multiple myeloma cell survival, migration and invasion in the murine 5T33MM model. British Journal of Haematology, 132, 469 477. (Pubitemid 43381618)
9. Cheng, J.D. Weiner, L.M. (2003) Tumours and their microenvironments: tilling the soil. Commentary re: A. M. Scott et al, A Phase I dose-escalation study of sibrotuzumab in patients with advanced or metastatic fibroblast activation protein-positive cancer. Clin. Cancer Res., 9: 1639-1647, 2003. Clinical Cancer Research, 9, 1590 1595.
10. Cheng, J.D., Dunbrack, Jr., R.L., Valianou, M., Rogatko, A., Alpaugh, R.K. Weiner, L.M. (2002) Promotion of tumour growth by murine fibroblast activation protein, a serine protease, in an animal model. Cancer Research, 62, 4767 4772.
11. Cheng, J.D., Valianou, M., Canutescu, A.A., Jaffe, E.K., Lee, H.O., Wang, H., Lai, J.H., Bachovchin, W.W. Weiner, L.M. (2005) Abrogation of fibroblast activation protein enzymatic activity attenuates tumor growth. Molecular Cancer Therapeutics, 4, 351 360. (Pubitemid 40443920)
12. Christiansen, V.J., Jackson, K.W., Lee, K.N. McKee, P.A. (2007) Effect of fibroblast activation protein and alpha(2)-antiplasmin cleaving enzyme on collagen Types I, III, and IV. Archives of Biochemistry and Biophysics, 457, 177 186. (Pubitemid 46048698)
13. Colla, S., Zhan, F., Xiong, W., Wu, X., Xu, H., Stephens, O., Yaccoby, S., Epstein, J., Barlogie, B. Shaughnessy, Jr., J.D. (2007) The oxidative stress response regulates DKK1 expression through the JNK signaling cascade in multiple myeloma plasma cells. Blood, 109, 4470 4477. (Pubitemid 46743417)
14. Coutts, S.J., Kelly, T.A., Snow, R.J., Kennedy, C.A., Barton, R.W., Adams, J., Krolikowski, D.A., Freeman, D.M., Campbell, S.J., Ksiazek, J.F. Bachovchin, W.W. (1996) Structure-activity relationships of boronic acid inhibitors of dipeptidyl peptidase IV. 1. Variation of the P2 position of Xaa-boroPro dipeptides. Journal of Medicinal Chemistry, 39, 2087 2094.
15. Cunningham, C.C. (2007) Talabostat. Expert Opinion on Investigational Drugs, 16, 1459 1465. (Pubitemid 47491415)
16. Edwards, C.M., Zhuang, J. Mundy, G.R. (2008) The pathogenesis of the bone disease of multiple myeloma. Bone, 42, 1007 1013.
17. Epstein, J. Yaccoby, S. (2003) Consequences of interactions between the bone marrow stroma and myeloma. Hematology Journal, 4, 310 314. (Pubitemid 37259347)
18. Ge, Y., Zhan, F., Barlogie, B., Epstein, J., Shaughnessy, J. Yaccoby, Y. (2006) Fibroblast activation protein (FAP) is upregulated in myelomatous bone and supports myeloma cell survival. British Journal of Haematology, 133, 83 92. (Pubitemid 43327202)
19. Ghersi, G., Dong, H., Goldstein, L.A., Yeh, Y., Hakkinen, L., Larjava, H.S. Chen, W.T. (2002) Regulation of fibroblast migration on collagenous matrix by a cell surface peptidase complex. Journal of Biological Chemistry, 277, 29231 29241.
20. Gorrell, M.D., Wang, X.M., Park, J., Ajami, K., Yu, D.M., Knott, H., Seth, D. McCaughan, G.W. (2006) Structure and function in dipeptidyl peptidase IV and related proteins. Advances in Experimental Medicine and Biology, 575, 45 54.
21. Havre, P.A., Abe, M., Urasaki, Y., Ohnuma, K., Morimoto, C. Dang, N.H. (2008) The role of CD26/dipeptidyl peptidase IV in cancer. Frontiers in Bioscience, 13, 1634 1645.
22. Hecht, M., von Metzler, I., Sack, K., Kaiser, M. Sezer, O. (2008) Interactions of myeloma cells with osteoclasts promote tumour expansion and bone degradation through activation of a complex signalling network and upregulation of cathepsin K, matrix metalloproteinases (MMPs) and urokinase plasminogen activator (uPA). Experimental Cell Research, 314, 1082 1093.
23. Huang, Y., Wang, S. Kelly, T. (2004) Seprase promotes rapid tumour growth and increased microvessel density in a mouse model of human breast cancer. Cancer Research, 64, 2712 2716. (Pubitemid 38500606)
24. Huber, M.A., Kraut, N., Park, J.E., Schubert, R.D., Rettig, W.J., Peter, R.U. Garin-Chesa, P. (2003) Fibroblast activation protein: differential expression and serine protease activity in reactive stromal fibroblasts of melanocytic skin tumours. Journal of Investigative Dermatology, 120, 182 188. (Pubitemid 36513065)
25. Jones, B., Adams, S., Miller, G.T., Jesson, M.I., Watanabe, T. Wallner, B.P. (2003) Hematopoietic stimulation by a dipeptidyl peptidase inhibitor reveals a novel regulatory mechanism and therapeutic treatment for blood cell deficiencies. Blood, 102, 1641 1648. (Pubitemid 37022555)
26. Joyce, J.A. (2005) Therapeutic targeting of the tumour microenvironment. Cancer Cell, 7, 513 520.
27. Kelly, T. (2005) Fibroblast activation protein-alpha and dipeptidyl peptidase IV (CD26): cell-surface proteases that activate cell signaling and are potential targets for cancer therapy. Drug Resistance Updates, 8, 51 58. (Pubitemid 40797956)
28. Lee, K.N., Jackson, K.W., Christiansen, V.J., Lee, C.S., Chun, J.G. McKee, P.A. (2006) Antiplasmin-cleaving enzyme is a soluble form of fibroblast activation protein. Blood, 107, 1397 1404. (Pubitemid 43242374)
29. Li, X., Udagawa, N., Takami, M., Sato, N., Kobayashi, Y. Takahashi, N. (2003) p38 Mitogen-activated protein kinase is crucially involved in osteoclast differentiation but not in cytokine production, phagocytosis, or dendritic cell differentiation of bone marrow macrophages. Endocrinology, 144, 4999 5005. (Pubitemid 37378415)
30. Nakamura, I., Duong, l.T., Rodan, S.B. Rodan, G.A. (2007) Involvement of alpha(v)beta3 integrins in osteoclast function. Journal of Bone and Mineral Metabolism, 25, 337 344.
31. Narra, K., Mullins, S.R., Lee, H.O., Strzemkowski-Brun, B., Magalong, K., Christiansen, V.J., McKee, P.A., Egleston, B., Cohen, S.J., Weiner, L.M., Meropol, N.J. Cheng, J.D. (2007) Phase II trial of single agent Val-boroPro (Talabostat) inhibiting Fibroblast Activation Protein in patients with metastatic colorectal cancer. Cancer Biology and Therapy, 6, 1691 1699.
32. Nemunaitis, J., Vukelja, S.J., Richards, D., Cunningham, C., Senzer, N., Nugent, J., Duncan, H., Jones, B., Haltom, E. Uprichard, M.J. (2006) Phase I trial of PT-100 (PT-100), a cytokine-inducing small molecule, following chemotherapy for solid tumour malignancy. Cancer Investigation, 24, 553 561. (Pubitemid 44422917)
33. Niedermeyer, J., Enenkel, B., Park, J.E., Lenter, M., Rettig, W.J., Damm, K. Schnapp, A. (1998) Mouse fibroblast-activation protein - conserved Fap gene organization and biochemical function as a serine protease. European Journal of Biochemistry, 254, 650 654. (Pubitemid 28308118)
34. Park, J.E., Lenter, M.C., Zimmermann, R.N., Garin-Chesa, P., Old, L.J. Rettig, W.J. (1999) Fibroblast activation protein, a dual specificity serine protease expressed in reactive human tumour stromal fibroblasts. Journal of Biological Chemistry, 274, 36505 36512.
35. Rao, H., Lu, G., Kajiya, H., Garcia-Palacios, V., Kurihara, N., Anderson, J., Patrene, K., Sheppard, D., Blair, H.C., Windle, J.J., Choi, S.J. Roodman, G.D. (2006) Alpha9beta1: a novel osteoclast integrin that regulates osteoclast formation and function. Journal of Bone Mineral Research, 21, 1657 1665.
36. Rettig, W.J., Garin-Chesa, P., Beresford, H.R., Oettgen, H.F., Melamed, M.R. Old, L.J. (1988) Cell-surface glycoproteins of human sarcomas: differential expression in normal and malignant tissues and cultured cells. Proceedings of the National Academy of Sciences of the United States of America, 85, 3110 3114. (Pubitemid 18138165)
37. Richardson, P.G., Barlogie, B., Berenson, J., Singhal, S., Jagannath, S., Irwin, D., Rajkumar, S.V., Srkalovic, G., Alsina, M., Alexanian, R., Siegel, D., Orlowski, R.Z., Kuter, D., Limentani, S.A., Lee, S., Hideshima, T., Esseltine, D.L., Kauffman, M., Adams, J., Schenkein, D.P. Anderson, K.C. (2003) A phase 2 study of bortezomib in relapsed, refractory myeloma. New England Journal of Medicine, 348, 2609 2617. (Pubitemid 36741588)
38. Roodman, G.D. (2004) Pathogenesis of myeloma bone disease. Blood Cells Molecules and Diseases, 32, 290 292. (Pubitemid 38296693)
39. Shreder, K.R., Wong, M.S., Corral, S., Yu, Z., Winn, D.T., Wu, M., Hu, Y., Nomanbhoy, T., Alemayehu, S., Fuller, S.R., Rosenblum, J.S. Kozarich, J.W. (2005) Boro-norleucine as a P1 residue for the design of selective and potent DPP7 inhibitors. Bioorganic & Medicinal Chemistry Letters, 15, 4256 4260. (Pubitemid 41187997)
40. Singhal, S., Mehta, J., Desikan, R., Ayers, D., Roberson, P., Eddlemon, P., Munshi, N., Anaissie, E., Wilson, C., Dhodapkar, M., Zeddis, J. Barlogie, B. (1999) Antitumour activity of thalidomide in refractory multiple myeloma. New England Journal of Medicine, 341, 1565 1571.
41. Vande Broek, I., Vanderkerken, K., De Greef, C., Asosingh, K., Straetmans, N., Van Camp, B. Van Riet, I. (2001) Laminin-1-induced migration of multiple myeloma cells involves the high-affinity 67 kD laminin receptor. British Journal of Cancer, 85, 1387 1395. (Pubitemid 33081937)
42. Yaccoby, S. Epstein, J. (1999) The proliferative potential of myeloma plasma cells manifest in the SCID-hu host. Blood, 94, 3576 3582. (Pubitemid 29536154)
43. Yaccoby, S., Barlogie, B. Epstein, J. (1998) Primary myeloma cells growing in SCID-hu mice: a model for studying the biology and treatment of myeloma and its manifestations. Blood, 92, 2908 2913. (Pubitemid 28469106)
44. Yaccoby, S., Pearse, R.N., Johnson, C.L., Barlogie, B., Choi, Y. Epstein, J. (2002) Myeloma interacts with the bone marrow microenvironment to induce osteoclastogenesis and is dependent on osteoclast activity. British Journal of Haematology, 116, 278 290. (Pubitemid 34156975)
45. Yaccoby, S., Wezeman, M.J., Henderson, A., Cottler-Fox, M., Yi, Q., Barlogie, B. Epstein, J. (2004) Cancer and the microenvironment: myeloma-osteoclast interactions as a model. Cancer Research, 64, 2016 2023. (Pubitemid 38339448)
46. Yaccoby, S., Wezeman, M.J., Zangari, M., Walker, R., Cottler-Fox, M., Gaddy, D., Ling, W., Saha, R., Barlogie, B., Tricot, G. Epstein, J. (2006) Inhibitory effects of osteoblasts and increased bone formation on myeloma in novel culture systems and a myelomatous mouse model. Haematologica, 91, 192 199. (Pubitemid 43304138)
47. Yaccoby, S., Ling, W., Zhan, F., Walker, R., Barlogie, B. Shaughnessy, Jr., J.D. (2007) Antibody-based inhibition of DKK1 suppresses tumour-induced bone resorption and multiple myeloma growth in vivo. Blood, 109, 2106 2111. (Pubitemid 46348212)
48. Yaccoby, S., Pennisi, A., Li, X., Dillon, S.R., Zhan, F., Barlogie, B. Shaughnessy, Jr., J.D. (2008) Atacicept (TACI-Ig) inhibits growth of TACI(high) primary myeloma cells in SCID-hu mice and in coculture with osteoclasts. Leukemia, 22, 406 413.
49. Yu, D.M., Wang, X.M., McCaughan, G.W. Gorrell, M.D. (2006) Extraenzymatic functions of the dipeptidyl peptidase IV-related proteins DP8 and DP9 in cell adhesion, migration and apoptosis. FEBS Journal, 273, 2447 2460. (Pubitemid 43736658)