Translational development of an ADAMTS-5 antibody for osteoarthritis disease modification

Osteoarthritis and Cartilage

Volumn 23, Issue 8, 2015, Pages 1254-1266

  Larkin, J ^a   Lohr, T A ^a   Elefante, L ^a   Shearin, J ^a   Matico, R ^a   Su, J L ^a   Xue, Y ^a   Liu, F ^a   Genell, C ^a   Miller, R E ^b   Tran, P B ^b   Malfait, A M ^b   Maier, C C ^a   Matheny, C J ^a  

^a GLAXOSMITHKLINE   (United States)

^b RUSH UNIVERSITY MEDICAL CENTER   (United States)

Author keywords

ADAMTS 4; ADAMTS 5; Cartilage; Disease modifying osteoarthritis drugs (DMOADs); Monoclonal antibody; Osteoarthritis

Indexed keywords

AGGRECANASE 1; AGGRECANASE 1 MONOCLONAL ANTIBODY; AGGRECANASE 2; AGGRECANASE 2 MONOCLONAL ANTIBODY; ANTIBODY; EPITOPE; GSK 2394000; GSK 2394002; GSK 571949; METALLOPROTEINASE INHIBITOR; MONOCLONAL ANTIBODY; MONOCLONAL ANTIBODY 12F4.1H7; MONOCLONAL ANTIBODY 7B4.1E11; MONOCLONAL ANTIBODY 7C7.1H1; MONOCLONAL ANTIBODY 7E8.1E3; UNCLASSIFIED DRUG; ADAM PROTEIN; AGGRECAN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CARTILAGE; CARTILAGE DEGENERATION; CONTROLLED STUDY; DRUG PENETRATION; DRUG STRUCTURE; ENZYME ACTIVITY; ENZYME INHIBITION; ENZYME METABOLISM; EX VIVO STUDY; EXPLANT; HUMAN; HUMAN TISSUE; IN VITRO STUDY; IN VIVO STUDY; KNOCKOUT MOUSE; MACACA FASCICULARIS; MALE; MOUSE; MOUSE MODEL; NONHUMAN; OSTEOARTHRITIS; PAIN; PREDICTION; PRIORITY JOURNAL; PROTEIN CROSS LINKING; PROTEIN DOMAIN; SINGLE DRUG DOSE; ANIMAL; ANTAGONISTS AND INHIBITORS; ARTICULAR CARTILAGE; DISEASE MODEL; IMMUNOLOGY; METABOLISM; PATHOLOGY;

ADAM PROTEINS; AGGRECANS; ANIMALS; ANTIBODIES, MONOCLONAL; CARTILAGE, ARTICULAR; DISEASE MODELS, ANIMAL; EPITOPES; HUMANS; MICE; OSTEOARTHRITIS;

EID: 84938200539     PISSN: 10634584     EISSN: 15229653     Source Type: Journal    
DOI: 10.1016/j.joca.2015.02.778     Document Type: Article

References (50)

1. Loeser R.F. Age-related changes in the musculoskeletal system and the development of osteoarthritis. Clin Geriatr Med 2010, 26:371-386.
2. Woolfe A.D., Pfleger B. Burden of major musculoskeletal conditions. Bull World Health Organ 2003, 81:646-656.
3. Troeberg L., Nagase H. Proteases involved in cartilage matrix degradation in osteoarthritis. Biochim Biophys Acta 1824, 2012:133-145.
4. Glasson S.S., Askew R., Sheppard B., Carito B., Blanchet T., Ma H.L., et al. Deletion of active ADAMTS5 prevents cartilage degradation in a murine model of osteoarthritis. Nature 2005, 434:644-648.
5. Stanton H., Rogerson F.M., East C.J., Golub S.B., Lawlor K.E., Meeker C.T., et al. ADAMTS5 is the major aggrecanase in mouse cartilage in vivo and in vitro. Nature 2005, 434:648-652.
6. Little C.B., Barai A., Burkhardt D., Smith S.M., Fosang A.J., Werb Z., et al. Matrix metalloproteinase 13-deficient mice are resistant to osteoarthritic cartilage erosion but not chondrocyte hypertrophy or osteophyte development. Arthritis Rheum 2009, 60:3723-3733.
7. Glasson S.S. In vivo osteoarthritis target validation utilizing genetically-modified mice. Curr Drug Targets 2007, 8:367-376.
8. Lark M.W., Bayne E.K., Flanagan J., Harper C.F., Hoerrner L.A., Hutchinson N.I., et al. Aggrecan degradation in human cartilage. Evidence for both matrix metalloproteinase and aggrecanase activity in normal, osteoarthritic, and rheumatoid joints. J Clin Invest 1997, 100:93-106.
9. Little C.B., Meeker C.T., Golub S.B., Lawlor K.E., Farmer P.J., Smith S.M., et al. Blocking aggrecanase cleavage in the aggrecan interglobular domain abrogates cartilage erosion and promotes cartilage repair. J Clin Invest 2007, 117:1627-1636.
10. Struglics A., Hansson M. MMP proteolysis of the human extracellular matrix protein aggrecan is mainly a process of normal turnover. Biochem J 2012, 446:213-223.
11. Durigova M., Nagase H., Mort J.S., Roughley P.J. MMPs are less efficient than ADAMTS5 in cleaving aggrecan core protein. Matrix Biol 2011, 30:145-153.
12. Gu J., Rong J., Guan F., Jiang L., Zhang T., Tao S., et al. Association of ADAMTS5 gene polymorphisms with osteoarthritis in Chinese Han population: a community-based case-control study. Rheumatol Int 2013 Nov, 33(11):2893-2897.
13. Plaas A., Osborn B., Yoshihara Y., Bai Y., Bloom T., Nelson F., et al. Aggrecanolysis in human osteoarthritis: confocal localization and biochemical characterization of ADAMTS5-hyaluronan complexes in articular cartilages. Osteoarthritis Cartilage 2007, 15:719-734.
14. Struglics A., Larsson S., Pratta M.A., Kumar S., Lark M.W., Lohmander L.S. Human osteoarthritis synovial fluid and joint cartilage contain both aggrecanase- and matrix metalloproteinase-generated aggrecan fragments. Osteoarthritis Cartilage 2006, 14:101-113.
15. Verma P., Dalal K. ADAMTS-4 and ADAMTS-5: key enzymes in osteoarthritis. J Cell Biochem 2011, 112:3507-3514.
16. Malfait A.M., Liu R.Q., Ijiri K., Komiya S., Tortorella M.D. Inhibition of ADAM-TS4 and ADAM-TS5 prevents aggrecan degradation in osteoarthritic cartilage. J Biol Chem 2002, 277:22201-22208.
17. Song R.H., Tortorella M.D., Malfait A.M., Alston J.T., Yang Z., Arner E.C., et al. Aggrecan degradation in human articular cartilage explants is mediated by both ADAMTS-4 and ADAMTS-5. Arthritis Rheum 2007, 56:575-585.
18. Naito S., Shiomi T., Okada A., Kimura T., Chijiiwa M., Fujita Y., et al. Expression of ADAMTS4 (aggrecanase-1) in human osteoarthritic cartilage. Pathol Int 2007, 57:703-711.
19. Kost T.A., Condreay J.P., Jarvis D.L. Baculovirus as versatile vectors for protein expression in insect and mammalian cells. Nat Biotechnol 2005, 23:567-575.
20. Germaschewski F.M., Matheny C.J., Larkin J., Liu F., Thomas L.R., Saunders J.S., et al. Quantitation OF ARGS aggrecan fragments in synovial fluid, serum and urine from osteoarthritis patients. Osteoarthritis Cartilage 2014, 22:690-697.
21. Pratta M.A., Su J.L., Leesnitzer M.A., Struglics A., Larsson S., Lohmander L.S., et al. Development and characterization of a highly specific and sensitive sandwich ELISA for detection of aggrecanase-generated aggrecan fragments. Osteoarthritis Cartilage 2006, 14:702-713.
22. Glasson S.S., Blanchet T.J., Morris E.A. The surgical destabilization of the medial meniscus (DMM) model of osteoarthritis in the 129/SvEv mouse. Osteoarthritis Cartilage 2007, 15:1061-1069.
23. Glasson S.S., Chambers M.G., Van Den Berg W.B., Little C.B. The OARSI histopathology initiative - recommendations for histological assessments of osteoarthritis in the mouse. Osteoarthritis Cartilage 2010, 18(Suppl 3):S17-S23.
24. Some Homology Data for This Paper Were Retrieved from the NCBI Homologene Database March, 2014, NAtional Center for Biotechnology Information, US National Library of Medicine, Bethesda, Maryland, World Wide Web URL:. http://www.ncbi.nlm.nih.gov/homologene/5109.
25. Deng H., O'Keefe H., Davie C.P., Lind K.E., Acharya R.A., Franklin G.J., et al. Discovery of highly potent and selective small molecule ADAMTS-5 inhibitors that inhibit human cartilage degradation via encoded library technology (ELT). J Med Chem 2012, 55:7061-7079.
26. Gendron C., Kashiwagi M., Lim N.H., Enghild J.J., Thogersen I.B., Hughes C., et al. Proteolytic activities of human ADAMTS-5: comparative studies with ADAMTS-4. J Biol Chem 2007, 282:18294-18306.
27. Lyskov S., Gray J.J. The RosettaDock server for local protein-protein docking. Nucleic Acids Res 2008, 36:W233-W238.
28. Wu T.T. From esoteric theory to therapeutic antibodies. Appl Biochem Biotechnol 1994, 47:107-117. discussion 117-108.
29. Velasco J., Li J., DiPietro L., Stepp M.A., Sandy J.D., Plaas A. Adamts5 deletion blocks murine dermal repair through CD44-mediated aggrecan accumulation and modulation of transforming growth factor beta1 (TGFbeta1) signaling. J Biol Chem 2011, 286:26016-26027.
30. Julovi S.M., Yasuda T., Shimizu M., Hiramitsu T., Nakamura T. Inhibition of interleukin-1beta-stimulated production of matrix metalloproteinases by hyaluronan via CD44 in human articular cartilage. Arthritis Rheum 2004, 50:516-525.
31. Malfait A.M., Ritchie J., Gil A.S., Austin J.S., Hartke J., Qin W., et al. ADAMTS-5 deficient mice do not develop mechanical allodynia associated with osteoarthritis following medial meniscal destabilization. Osteoarthritis Cartilage 2010, 18:572-580.
32. Miller R.E., Tran P.B., Das R., Ghoreishi-Haack N., Ren D., Miller R.J., et al. CCR2 chemokine receptor signaling mediates pain in experimental osteoarthritis. Proc Natl Acad Sci USA 2012 Dec 11, 109(50):20602-20607. 10.1073/pnas.1209294110.
33. Carlson C.S., Loeser R.F., Jayo M.J., Weaver D.S., Adams M.R., Jerome C.P. Osteoarthritis in cynomolgus macaques: a primate model of naturally occurring disease. J Orthop Res 1994, 12:331-339.
34. Gilbert A.M., Bikker J.A., O'Neil S.V. Advances in the development of novel aggrecanase inhibitors. Expert Opin Ther Pat 2011, 21:1-12.
35. Chiusaroli R., Visentini M., Galimberti C., Casseler C., Mennuni L., Covaceuszach S., et al. Targeting of ADAMTS5's ancillary domain with the recombinant mAb CRB0017 ameliorates disease progression in a spontaneous murine model of osteoarthritis. Osteoarthritis Cartilage 2013, 21:1807-1810.
36. Devy L., Huang L., Naa L., Yanamandra N., Pieters H., Frans N., et al. Selective inhibition of matrix metalloproteinase-14 blocks tumor growth, invasion, and angiogenesis. Cancer Res 2009, 69:1517-1526.
37. Sela-Passwell N., Kikkeri R., Dym O., Rozenberg H., Margalit R., Arad-Yellin R., et al. Antibodies targeting the catalytic zinc complex of activated matrix metalloproteinases show therapeutic potential. Nat Med 2011, 18:143-147.
38. Manka S.W., Carafoli F., Visse R., Bihan D., Raynal N., Farndale R.W., et al. Structural insights into triple-helical collagen cleavage by matrix metalloproteinase 1. Proc Natl Acad Sci USA 2012, 109:12461-12466.
39. Arner E.C. Aggrecanase-mediated cartilage degradation. Curr Opin Pharmacol 2002, 2:322-329.
40. Majumdar M.K., Askew R., Schelling S., Stedman N., Blanchet T., Hopkins B., et al. Double-knockout of ADAMTS-4 and ADAMTS-5 in mice results in physiologically normal animals and prevents the progression of osteoarthritis. Arthritis Rheum 2007, 56:3670-3674.
41. Fosang A.J., Rogerson F.M. Identifying the human aggrecanase. Osteoarthritis Cartilage 2010, 18:1109-1116.
42. Gao G., Westling J., Thompson V.P., Howell T.D., Gottschall P.E., Sandy J.D. Activation of the proteolytic activity of ADAMTS4 (aggrecanase-1) by C-terminal truncation. J Biol Chem 2002, 277:11034-11041.
43. Zeng W., Corcoran C., Collins-Racie L.A., Lavallie E.R., Morris E.A., Flannery C.R. Glycosaminoglycan-binding properties and aggrecanase activities of truncated ADAMTSs: comparative analyses with ADAMTS-5, -9, -16 and -18. Biochim Biophys Acta 2006, 1760:517-524.
44. Rogerson F.M., Stanton H., East C.J., Golub S.B., Tutolo L., Farmer P.J., et al. Evidence of a novel aggrecan-degrading activity in cartilage: studies of mice deficient in both ADAMTS-4 and ADAMTS-5. Arthritis Rheum 2008, 58:1664-1673.
45. Carlson C.S., Loeser R.F., Purser C.B., Gardin J.F., Jerome C.P. Osteoarthritis in cynomolgus macaques. III: effects of age, gender, and subchondral bone thickness on the severity of disease. J Bone Min Res 1996, 11:1209-1217.
46. Chockalingam P.S., Sun W., Rivera-Bermudez M.A., Zeng W., Dufield D.R., Larsson S., et al. Elevated aggrecanase activity in a rat model of joint injury is attenuated by an aggrecanase specific inhibitor. Osteoarthritis Cartilage 2011, 19:315-323.
47. Swearingen C.A., Chambers M.G., Lin C., Marimuthu J., Rito C.J., Carter Q.L., et al. A short-term pharmacodynamic model for monitoring aggrecanase activity: injection of monosodium iodoacetate (MIA) in rats and assessment of aggrecan neoepitope release in synovial fluid using novel ELISAs. Osteoarthritis Cartilage 2010, 18:1159-1166.
48. Dupuis L.E., McCulloch D.R., McGarity J.D., Bahan A., Wessels A., Weber D., et al. Altered versican cleavage in ADAMTS5 deficient mice; a novel etiology of myxomatous valve disease. Dev Biol 2011, 357:152-164.
49. Didangelos A., Mayr U., Monaco C., Mayr M. Novel role of ADAMTS-5 protein in proteoglycan turnover and lipoprotein retention in atherosclerosis. J Biol Chem 2012, 287:19341-19345.
50. Wang V.M., Bell R.M., Thakore R., Eyre D.R., Galante J.O., Li J., et al. Murine tendon function is adversely affected by aggrecan accumulation due to the knockout of ADAMTS5. J Orthop Res 2012, 30:620-626.