Developmental and peri-postnatal study in cynomolgus monkeys with belimumab, a monoclonal antibody directed against B-lymphocyte stimulator

Reproductive Toxicology

Volumn 28, Issue 4, 2009, Pages 443-455

  Auyeung Kim, Diana J ^a   Devalaraja, Madhav N ^b   Migone, Thi Sau ^b   Cai, Wendy ^b   Chellman, Gary J ^a  

^a CHARLES RIVER LABORATORIES   (United States)

^b GLAXOSMITHKLINE   (United States)

Author keywords

Belimumab; BLyS; Cynomolgus; Developmental study; Immunomodulation; Nonhuman primates; Peri postnatal study; Reproduction

Indexed keywords

BELIMUMAB; MONOCLONAL ANTIBODY;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; AREA UNDER THE CURVE; ARTICLE; B LYMPHOCYTE; CARDIOTOXICITY; CONTROLLED STUDY; DEVELOPMENTAL BIOLOGY; DRUG ACCUMULATION; DRUG BLOOD LEVEL; DRUG MECHANISM; DRUG MILK LEVEL; DRUG TOLERABILITY; EMBRYO; FEMALE; FETUS; GESTATION PERIOD; LYMPHOCYTE COUNT; LYMPHOID TISSUE; MALE; MAXIMUM PLASMA CONCENTRATION; MONKEY; NONHUMAN; PERINATAL PERIOD; PRENATAL EXPOSURE; SINGLE DRUG DOSE; SKELETAL MUSCLE; TERATOGENICITY; TOXICOKINETICS; VISCERA;

ANIMALS; ANTIBODIES, MONOCLONAL; AREA UNDER CURVE; B-CELL ACTIVATING FACTOR; B-LYMPHOCYTES; DOSE-RESPONSE RELATIONSHIP, DRUG; DRUG EVALUATION, PRECLINICAL; FEMALE; FETUS; IMMUNOSUPPRESSIVE AGENTS; LYMPHOCYTE ACTIVATION; MACACA FASCICULARIS; MATERNAL-FETAL EXCHANGE; METABOLIC CLEARANCE RATE; PREGNANCY; TIME FACTORS;

MACACA FASCICULARIS; PRIMATES;

EID: 70350212956     PISSN: 08906238     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.reprotox.2009.07.002     Document Type: Article

References (45)

1. Moore P.A., Belvedere O., Orr A., Pieri K., LaFleur D.W., Feng P., et al. BLyS: member of the tumor necrosis factor family and B lymphocyte stimulator. Science 285 5425 (1999) 260-263
2. Avery D.T., Kalled S.L., Ellyard J.I., Ambrose C., Bixler S.A., Thien M., et al. BAFF selectively enhances the survival of plasmablasts generated from human memory B cells. J Clin Invest 112 2 (2003) 286-297
3. Gross J.A., Johnston J., Mudri S., Enselman R., Dillon S.R., Madden K., et al. TACI and BCMA are receptors for a TNF homologue implicated in B-cell autoimmune disease. Nature 404 6781 (2000) 995-999
4. Xia X.Z., Treanor J., Senaldi G., Khare S.D., Boone T., Kelley M., et al. TACI is a TRAF-interacting receptor for TALL-1, a tumor necrosis factor family member involved in B cell regulation. J Exp Med 192 1 (2000) 137-143
5. Yan M., Brady J.R., Chan B., Lee W.P., Hsu B., Harless S., et al. Identification of a novel receptor for B lymphocyte stimulator that is mutated in a mouse strain with severe B cell deficiency. Curr Biol 11 19 (2001) 1547-1552
6. Yan M., Marsters S.A., Grewal I.S., Wang H., Ashkenazi A., and Dixit V.M. Identification of a receptor for BLyS demonstrates a crucial role in humoral immunity. Nat Immunol 1 1 (2000) 37-41
7. Thompson J.S., Bixler S.A., Qian F., Vora K., Scott M.L., Cachero T.G., et al. BAFF-R, a newly identified TNF receptor that specifically interacts with BAFF. Science 293 5537 (2001) 2108-2111
8. Tan S.M., Xu D., Roschke V., Perry J.W., Arkfeld D.G., Ehresmann G.R., et al. Local production of B lymphocyte stimulator protein and APRIL in arthritic joints of patients with inflammatory arthritis. Arthritis Rheum 48 4 (2003) 982-992
9. Zhang J., Roschke V., Baker K.P., Wang Z., Alarcon G.S., Fessler B.J., et al. Cutting edge: a role for B lymphocyte stimulator in systemic lupus erythematosus. J Immunol 166 1 (2001) 6-10
10. Cheema G.S., Roschke V., Hilbert D.M., and Stohl W. Elevated serum B lymphocyte stimulator levels in patients with systemic immune-based rheumatic diseases. Arthritis Rheum 44 6 (2001) 1313-1319
11. Cambridge G., Isenberg D.A., Edwards J.C., Leandro M.J., Migone T.S., Teodorescu M., et al. B cell depletion therapy in systemic lupus erythematosus: relationships among serum B lymphocyte stimulator levels, autoantibody profile and clinical response. Ann Rheum Dis 67 7 (2008) 1011-1016
12. Petri M., Stohl W., Chatham W., McCune W.J., Chevrier M., Ryel J., et al. Association of plasma B lymphocyte stimulator levels and disease activity in systemic lupus erythematosus. Arthritis Rheum 58 8 (2008) 2453-2459
13. Baker K.P., Edwards B.M., Main S.H., Choi G.H., Wager R.E., Halpern W.G., et al. Generation and characterization of LymphoStat-B, a human monoclonal antibody that antagonizes the bioactivities of B lymphocyte stimulator. Arthritis Rheum 48 11 (2003) 3253-3265
14. Ding C. Belimumab, an anti-BLyS human monoclonal antibody for potential treatment of inflammatory autoimmune diseases. Expert Opin Biol Ther 8 11 (2008) 1805-1814
15. Furie R., Stohl W., Ginzler E.M., Becker M., Mishra N., Chatham W., et al. Biologic activity and safety of belimumab, a neutralizing anti-B-lymphocyte stimulator (BLyS) monoclonal antibody: a phase I trial in patients with systemic lupus erythematosus. Arthritis Res Ther 10 5 (2008) R109
16. Belimumab: anti-BLyS human monoclonal antibody, anti-BLyS monoclonal antibody, BmAb, human monoclonal antibody to B-lymphocyte stimulator. Drugs R D 9 3 (2008) 197-202
17. Ding C., Foote S., and Jones G. B-cell-targeted therapy for systemic lupus erythematosus: an update. BioDrugs 22 4 (2008) 239-249
18. Chatham W., Aranow C., Furie R., Weisman M.H., Stohl W., Petri M., et al. Progressive normalization of autoantibody, immunoglobulin, and complement levels over 3 years of belimumab (fully human monoclonal antibody to BLyS) therapy in systemic lupus erythematosus (SLE) patients. Annual Congress of the European League Against Rheumatism (EULAR 2008) (2008) Ref Type: Abstract
19. Merrill J.T., Wallace D.J., McKay J., Ginzler E.M., Lee E., McCain A., et al. Long-term safety profile of belimumab (fully human monoclonal antibody to BLyS) in patients with systemic lupus erythematosus (SLE). Annual Congress of the European League Against Rheumatism (EULAR 2008) (2008) Ref Type: Abstract
20. Simister N.E. Placental transport of immunoglobulin G. Vaccine 21 24 (2003) 3365-3369
21. Chapman K., Pullen N., Graham M., and Ragan I. Preclinical safety testing of monoclonal antibodies: the significance of species relevance. Nat Rev Drug Discov 6 2 (2007) 120-126
22. Institute of Laboratory Animal Research, Commission on Life Sciences, and National Research Council. Guide for the Care and Use of Laboratory Animals. 7th ed. (2006), National Academy Press, Washington, D.C.
23. Buckley L.A., Benson K., vis-Bruno K., Dempster M., Finch G.L., Harlow P., et al. Nonclinical aspects of biopharmaceutical development: discussion of case studies at a PhRMA-FDA workshop. Int J Toxicol 27 4 (2008) 303-312
24. Tarantal A.F., and Hendrickx A.G. Prenatal growth in the cynomolgus and rhesus macaque (Macaca fascicularis and Macaca mulatta): a comparison by ultrasonography. Am J Prim 15 (1988) 309-323
25. Golub M.S. Use of monkey neonatal neurobehavioral test batteries in safety testing protocols. Neurotoxicol Teratol 12 5 (1990) 537-541
26. Golub M.S., and Gershwin M.E. Standardized neonatal assessment in the rhesus monkey. In: Nathanielsz P.W., and Parer J.T. (Eds). Research in perinatal medicine (2004), Perinatology Press 56-86
27. Switzer J.W., Valerio D.A., Martin D.P., Valerio M.G., and Rininger B.F. Hematologic changes associated with pregnancy and parturition in Macaca mulatta. Lab Anim Care 20 5 (1970) 930-939
28. Hendrickx A.G., and Cukierski M.A. Reproductive and developmental toxicology in nonhuman primates. Prog Clin Biol Res 235 (1987) 73-88
29. Hendrickx A.G., and Dukelow W.R. Reproductive biology. In: Bennett B.T., Abee C.R., and Henrickson R. (Eds). Nonhuman primates in biomedical research biology and management. 1st ed. (2005), Academic Press, New York 147-191
30. Medina K.L., and Kincade P.W. Pregnancy-related steroids are potential negative regulators of B lymphopoiesis. Proc Natl Acad Sci USA 91 12 (1994) 5382-5386
31. Hendrie T.A., Peterson P.E., Short J.J., Tarantal A.F., Rothgarn E., Hendrie M.I., et al. Frequency of prenatal loss in a macaque breeding colony. Am J Primatol 40 1 (1996) 41-53
32. Hendrickx A.G., Peterson P.E., and Makori N.M. The nonhuman primate as a model of developmental immunotoxicity. In: Holladay S.D. (Ed). Developmental immuntoxicology. 1st ed. (2005), CRC Press LLC, Boca Raton 117-136
33. Fujimoto K., Terao K., Cho F., and Honjo S. The placental transfer of IgG in the cynomolgus monkey. Jpn J Med Sci Biol 36 3 (1983) 171-176
34. Coe C.L., Kemnitz J.W., and Schneider M.L. Vulnerability of placental antibody transfer and fetal complement synthesis to disturbance of the pregnant monkey. J Med Primatol 22 5 (1993) 294-300
35. Gardin J.F., Jerome C.P., Jayo M.J., and Weaver D.S. Maternal factors affecting reproduction in a breeding colony of cynomolgus macaques (Macaca fascicularis). Lab Anim Sci 39 3 (1989) 205-212
36. Hird D.W., Henrickson R.V., and Hendrickx A.G. Infant mortality in Macaca mulatta: neonatal and post-neonatal mortality at the California Primate Research Center, 1968-1972. A retrospective study. J Med Primatol 4 1 (1975) 4-22
37. Buse E. Development of the immune system in the cynomolgus monkey: the appropriate model in human targeted toxicology?. J Immunol Toxicol 2 (2005) 211-216
38. Fujimoto K., Terao K., Cho F., Nakamura F., and Honjo S. Age-related immunoglobulin levels in cynomolgus monkeys. Jpn J Med Sci Biol 35 1 (1982) 17-23
39. Rituxan (rituximab). Physician's desk reference. 63rd ed. (2009), Thomson Reuters, Montvale, NJ p. 1223-1228
40. Leach J.L., Sedmak D.D., Osborne J.M., Rahill B., Lairmore M.D., and Anderson C.L. Isolation from human placenta of the IgG transporter, FcRn, and localization to the syncytiotrophoblast: implications for maternal-fetal antibody transport. J Immunol 157 8 (1996) 3317-3322
41. Cole M.F., and Bowen W.H. Immunoglobulins A, G, and M in serum and in some secretions of monkeys (Macaca fascicularis syn. irus). Infect Immun 13 5 (1976) 1354-1359
42. Malek A., Sager R., and Schneider H. Maternal-fetal transport of immunoglobulin G and its subclasses during the third trimester of human pregnancy. Am J Reprod Immunol 32 1 (1994) 8-14
43. Malek A., Sager R., Kuhn P., Nicolaides K.H., and Schneider H. Evolution of maternofetal transport of immunoglobulins during human pregnancy. Am J Reprod Immunol 36 5 (1996) 248-255
44. Van de P.P. Transfer of antibody via mother's milk. Vaccine 21 24 (2003) 3374-3376
45. Stewart J. Developmental toxicity testing of monoclonal antibodies: an enhanced pre- and postnatal study design option. Reprod Toxicol 28 (2009) 220-225