Considerations in assessing the developmental and reproductive toxicity potential of biopharmaceuticals

Birth Defects Research Part B - Developmental and Reproductive Toxicology

Volumn 86, Issue 3, 2009, Pages 176-203

  Martin, Pauline L ^a   Breslin, William ^b   Rocca, Meredith ^c   Wright, David ^d   Cavagnaro, Joy ^e  

^a CENTOCOR INC   (United States)

^b ELI LILLY AND COMPANY   (United States)

^c AMGEN INC   (United States)

^d PFIZER INC   (United States)

^e Access BIO   (United States)

Author keywords

Biopharmaceuticals; Biotherapeutics; Embryo fetal development; Pregnancy; Reproduction; Risk assessment

Indexed keywords

AGALSIDASE BETA; ALTEPLASE; ARGATROBAN; ASPARAGINASE; BETA1A INTERFERON; BEVACIZUMAB; BOTULINUM TOXIN A; CONSENSUS INTERFERON; EFALIZUMAB; ENFUVIRTIDE; EXENDIN 4; GEMTUZUMAB OZOGAMICIN; HUMAN INSULIN; IDURONATE 2 SULFATASE; INSULIN; LARONIDASE; NESIRITIDE; NOVEL ERYTHROPOIESIS STIMULATING PROTEIN; OCTREOTIDE; PARATHYROID HORMONE[1-34]; PEGADEMASE; PEGINTERFERON ALPHA2A; PEGVISOMANT; PLASMINOGEN ACTIVATOR; RECOMBINANT BLOOD CLOTTING FACTOR 8; RECOMBINANT ERYTHROPOIETIN; RECOMBINANT GLUCAGON; RECOMBINANT GRANULOCYTE COLONY STIMULATING FACTOR; RECOMBINANT HUMAN INSULIN; RECOMBINANT INTERLEUKIN 11; RECOMBINANT LUTEINIZING HORMONE; UNINDEXED DRUG;

ACROMEGALY; ACUTE GRANULOCYTIC LEUKEMIA; ACUTE HEART INFARCTION; ACUTE LYMPHOBLASTIC LEUKEMIA; ANEMIA; BLEPHAROSPASM; CEREBROVASCULAR ACCIDENT; CERVICAL DYSTONIA; COLORECTAL CANCER; CONGESTIVE HEART FAILURE; DEVELOPMENTAL STAGE; DIABETES MELLITUS; DRUG APPROVAL; DRUG MECHANISM; EMBRYO DEVELOPMENT; ENZYME ACTIVITY; FABRY DISEASE; FEMALE INFERTILITY; FETUS DEVELOPMENT; FOOD AND DRUG ADMINISTRATION; GENETIC ENGINEERING; HEMOPHILIA A; HEPATITIS C; HUMAN; HUMAN IMMUNODEFICIENCY VIRUS 1 INFECTION; HUNTER SYNDROME; HURLER SYNDROME; HYBRIDOMA; HYPERHIDROSIS; HYPOGLYCEMIA; IMMUNOGENICITY; KIDNEY FAILURE; LUNG EMBOLISM; METASTASIS; MULTIPLE SCLEROSIS; NEUTROPENIA; NON INSULIN DEPENDENT DIABETES MELLITUS; NONHUMAN; OSTEOPOROSIS; PLACENTAL TRANSFER; POSTNATAL DEVELOPMENT; PRENATAL DEVELOPMENT; PRIORITY JOURNAL; PSORIASIS; REPRODUCTIVE TOXICITY; REVIEW; RISK ASSESSMENT; SEVERE COMBINED IMMUNODEFICIENCY; STRABISMUS; THROMBOCYTOPENIA;

ALGORITHMS; ANIMALS; BIOPHARMACEUTICS; DRUG EVALUATION, PRECLINICAL; DRUG TOXICITY; EMBRYONIC DEVELOPMENT; FEMALE; PLACENTA; PREGNANCY; REPRODUCTION; RISK ASSESSMENT; TOXICITY TESTS;

ANIMALIA; PAN; PRIMATES; RODENTIA;

EID: 67649253050     PISSN: 15429733     EISSN: None     Source Type: Journal    
DOI: 10.1002/bdrb.20197     Document Type: Review

References (76)

1. Aaltonen R, Heikkinen T, Hakala K, Laine K, Alanen A. 2005. Transfer of proinflammatory cytokines across term placenta. Obstet Gynecol 160:802-807. (Pubitemid 41362186)
2. Boothby LA, Doering PL. 2001. FDA labeling system for drugs in pregnancy. Ann Pharmacother 35:1485-1489. (Pubitemid 33042087)
3. Boskovic R, Feig DS, Derewlany L, Knie B, Portnoi G, Koren G. 2003. Transfer of insulin lispro across the human placenta. Diabetes Care 26:1390-1394.
4. Boskovic R, Wide R, Wolpin J, Bauer DJ, Koren G. 2005. The reproductive effects of beta interferon therapy in pregnancy. Neurol 65:807-811.
5. Bugelski PJ, Herzyk DJ, Rehm S, Harmsen AG, Gore EV, Williams DM, Maleeff BE, Badger AM, Truneh A, O'Brien SR, Macia RA, Wier PJ, Morgan DG, Hart TK. 2000. Preclinical development of keliximab, a primatized anti-CD4 monoclonal antibody, in human CD4 transgenic mice: characterization of the model and safety studies. Hum Exp Toxicol 19:230-243. (Pubitemid 30428172)
6. Buse E, Habermann G, Osterburg I, Korte R, Weinbauer GF. 2003. Reproductive/developmental toxicity and immunotoxicity assessment in the nonhuman primate model. Toxicology 185:221-227. (Pubitemid 36173739)
7. Cavagnaro JA. 1993. Preclinical safety assessment of biological products. In: Matthieu M, editor. Biologics development: a regulatory overview. Waltham, MA: Parexel Int. p 23-40.
8. Cavagnaro JA. 2002. Preclinical safety evaluation of biotechnology- derived pharmaceuticals. Nature Rev Drug Discov 1:469-475. (Pubitemid 37361490)
9. Clark J, Leach W, Pippig S, Joshi A, Wu B, House R, Beyer J. 2004. Evaluation of a surrogate antibody for preclinical safety testing of an anti-CD11a monoclonal antibody. Regul Toxicol Pharmacol 40:219-226. (Pubitemid 39531303)
10. Coe CL, Kemnitz JW, Scneider ML. 1993. Vulnerability of placental antibody transfer and fetal complement synthesis to disturbance of the pregnant monkey. J Med Primatol 22:294-300.
11. Coe CL, Lubach GR, Izard KM. 1994. Progressive improvement in the transfer of maternal antibody across the order primates. Am J Primatol 32:51-55.
12. Collins TFX. 2006. History and evaluation of reproductive and developmental toxicity guidelines. Curr Pharmaceut Design 12:1449-1465. (Pubitemid 44082105)
13. Crowley C, Spencer SD, Nishimura MC, Chen KS, Pitta-Meek S, Armanini MP, Ling LH, McMahon SB, Shelton DL, Levinson AD, Phillips HS. 1994. Mice lacking nerve growth factor display perinatal loss of sensory and sympathetic neurons yet develop basal forebrain cholinergic neurons. Cell 76:1001-1011. (Pubitemid 24106381)
14. Dreef HC, Van Esch E, De Ru EPCT. 2007. Spermatogenesis in the cynomolgus monkey (macaca fascicularis): a practical guide for routine morphological staging. Toxicol Pathol 35:395-404. (Pubitemid 46450075)
15. Faustman EM, Gohlke JM, Ponce RA, Lewandowski TA, Seeley MR, Whittaker SG, Griffith WC. 2006. Experimental approaches to evaluate mechanisms of developmental toxicity. In: Hood RD, editor. Developmental and reproductive toxicology: a practical approach, 2nd ed. Boca Raton, FL: CRC Press. p 15-60.
16. Ferrara N, Carver-Moore K, Chen H, Dowd M, Lu L, O'Shea KS, Powell-Braxton L, Hillan KJ, Moore MW. 1996. Heterozygous embryonic lethality induced by targeted inactivation of the VEGF gene. Nature 380:439-441. (Pubitemid 26102720)
17. Fujimoto K, Terao K, Cho F, Honjo S. 1983. The placenta transfer of IgG in the cynomolgus monkey. Japan J Med Sci Biol 36:171-176.
18. Gill DS, Damle NK. 2008. Biopharmaceutical drug discovery using novel protein scaffolds. Curr Opin Biotechnol 17:653-658.
19. Gitlin D, Kumate J, Urrust J, Morales C. 1964. The selectivity of the human placenta in the transfer of plasma proteins from mother to fetus. J Clin Invest 43:1938-1951.
20. Gregor H, Egarter C, Levin D, Sternberger B, Heinze G, Leitich H, Reisenberger K. 1999. The passage of granulocyte-macrophage colony-stimulating factor across the human placenta perfused in vitro. J Soc Gynecol Invest 6:307-310. (Pubitemid 30009762)
21. Henck JW, Hilbish KG, Serabian MA, Cavagnaro JA, Hendrickx AG, Agnish ND, Kung AHC, Mordenti J. 1996. Reproductive toxicity testing of therapeutic biotechnology agents. Teratology 53:185-195. (Pubitemid 26190891)
22. Henck DJ, Bugelski PJ, Hart TK, Wier PJ. 2002. Practical aspects of including functional endpoints in developmental toxicity studies. Case study: immune function in HuCD4 transgenic mice exposed to anti-CD4 Mab in utero. Hum Exp Toxicol 21:507-512.
23. Hendrickx AG, Makori N, Peterson P. 2000. Nonhuman primates: their role in assessing developmental effects of immunomodulatory agents. Hum Exp Toxicol 19:219-225. (Pubitemid 30428169)
24. Hendrickx AG, Peterson PE, Makori NM. 2005. The nonhuman primate as a model of developmental immunotoxicity. In: Holladay SD, editor. Developmental Immunotoxicity. Boca Raton, FL: CRC Press. p 117-138.
25. Hendrie TA, Peterson PE, Short JJ, Tarantal AF, Rothgarn E, Hendrie MI, Hendrickx AG. 1996. Frequency of prenatal loss in a macaque breeding colony. Am J Primatol 40:41-53. (Pubitemid 26351375)
26. Hofmann T, Horstmann G, Stammberger I. 2002. Evaluation of the reproductive toxicity and embryotoxcity of insulin glargine (LANTUS) in rats and rabbits. Int J Toxicol 21:181-189. (Pubitemid 34803493)
27. Holsapple MP, West LJ, Landreth KS. 2003. Species comparison of anatomical and functional immune system development. Birth Def Res B 68:321-334. (Pubitemid 37238421)
28. ICH M3: Guidance on Nonclinical Safety Studies for the Conduct of Human Clinical Trials and Marketing Authorization for Pharmaceuticals. 1997. www.ich.org
29. ICH M3(R2): Guidance on Nonclinical Safety Studies for the Conduct of Human Clinical Trials and Marketing Authorization for Pharmaceuticals. Draft Step 3 2008. www.ich.org
30. ICH S5(R2): Guidance on Reproductive Toxicology and Male Fertility: Detection of Toxicity to Reproduction for Medicinal Products. 2005. www.ich.org
31. ICH S6: Preclinical Safety Evaluation of Biotechnology-derived Pharmaceuticals. 1997. www.ich.org
32. Jauniaux E, Gulbis B. 2000. In vivo investigation of placental transfer early in human pregnancy. Eur J Obst Gynecol 92:45-49.
33. Jayaprasad N, Johnson F, Venugopal K. 2006. Congenital complete heart block and maternal connective tissue disease. Int J Cardiol 112:153-158. (Pubitemid 44353801)
34. Karlsson M, Danielsson BR, Nilsson MF. 2007. New proposals for testing drugs with IKr-blocking activity to determine their teratogenic potential. Curr Pharmaceut Design 13:2979-2988. (Pubitemid 350130965)
35. Lanning LL, Creasy DM, Chapin RE, Mann PC, Barlow NJ, Regan KS, Goodman DG. 2002. Society of Toxicologic Pathology Position Paper: recommended approaches for the evaluation of testicular and epididymal toxicity. Toxicol Pathol 30:507-520.
36. Leader R, Baca QJ, Golan DE. 2008. Protein therapeutics: a summary and pharmacological classification. Nature Rev 7:21-39.
37. Lee LA. 2005. Transient autoimmunity related to maternal autoantibodies: neonatal lupus. Autoimmun Rev 4: 207-213.
38. Malek A, Sager R, Kuhn P, Nicholaides KH, Schneider H. 1996. Evaluation of maternofetal transport of immunoglobulins during human pregnancy. Am J Reprod Immunol 36:248-255. (Pubitemid 26383975)
39. Martin PL. 2002. Effects of a lymphotoxin-b receptor-IgG1 (LTβR-Ig) fusion protein on lymph node development. In: Korte R, Vogel F, Weinbauer GF, editors. Primate models in pharmaceutical drug development. Münster, Germany: Waxmann Verlag GmbH. p 105-118.
40. Martin PL. 2008. Reproductive toxicity testing for biopharmaceuticals. In: Cavagnaro JA, editor. Preclinical safety evaluation of biopharmaceuticals. Hoboken, NJ: John Wiley & Sons. p 357-377.
41. Martin PL, Buse E. 2008. Developmental immunotoxicity in nonhuman primates. In: Herzyk DJ, Bussiere JL, editors. Imunotoxicology strategies for pharmaceutical safety assessment. Hoboken, NJ: John Wiley & Sons. p 299-317.
42. Martin PL, Cornacoff JB, Treacy G, Eirikas E, Marini J, White KL, Peachee V, Hoberman A. 2008. Effects of administration of a monoclonal antibody against mouse tumor necrosis factor alpha during pregnancy and lactation on the pre- and postnatal development of the mouse immune system. Int J Toxicol 27:341-347.
43. Martin PL, Oneda S, Treacy G. 2007. Effects of an anti-TNFa monoclonal antibody, administered throughout pregnancy and lactation, on the development of the macaque immune system. Am J Reprod Immunol. 58:138-149. (Pubitemid 47097380)
44. Meyer JK, Fitzsimmons D, Hastings TF, Chellman GJ. 2006. Methods for the prediction of breeding success in male cynomolgus monkeys (macaca fasciculararis) used for reproductive toxicology studies. J Am Assoc Lab Animal Sci 45:31-36. (Pubitemid 43835588)
45. Miettinen PJ, Berger JE, Meneses J, Phung Y, Pedersen RA, Werb Z, R. 1995. Epithelial immaturity and multiorgan failure in mice lacking epidermal growth factor receptor. Nature 376:337-341.
46. Miller RK, Koszalka TR, Brent RL. 1976. The transport of molecules across placenta membranes. In: Poste G, Nicolson GL, editors. The cell surface in animal embryogenesis and development. Amsterdam: North Holland Biomedical Press. p 145-223.
47. Miller RK, Mace K, Polliotti B, DeRita R, Hall W, Treacy G. 2003. Marginal transfer of ReoProTM (Abciximab) compared with immunoglobulin G (F105), inulin and water in the perfused human placenta in vitro. Placenta 24:727-738. (Pubitemid 37184795)
48. Morgan DJ. 1997. Drug disposition in mother and foetus. Clin Exp Pharmacol Physiol 24:869-873. (Pubitemid 27448583)
49. Morphis LG, Gitlin D. 1970. Maturation of the embryofetal transport system for human globulin in the mouse. Nature 228:573.
50. Murphy HR, Rayman G, Lewis K, Kelly S, Johal B, Duffield K, Fowler D, Campbell PJ, Temple RC. 2008. Effectiveness of continuous glucose monitoring in pregnant women with diabetes: randomized clinical trial. Br Med J 337:907-910.
51. Palfi M, Selbring A. 1998. Placental transport of maternal immunoglobulin G. Am J Reprod Immunol 39:24-26. (Pubitemid 27527141)
52. Presta LG. 2006. Engineering of therapeutic antibodies to minimize immunogenicity and optimize function. Adv Drug Deliv Rev 58:640-656. (Pubitemid 44262411)
53. Reisenberger K, Egarter C, Vogl S, Sternberger B, Kiss H, Husslein P. 1996. The transfer of interleukin-8 across the human placenta perfused in vitro. Obstet Gynecol 87:613-616. (Pubitemid 26102751)
54. Rennert PD, Browning JL, Hochman PS. 1997. Selective disruption of lymphotoxin ligands reveals a novel set of mucosal lymph nodes and unique effects on lymph node cellular organization. Int Immunol 11:1627-1639. (Pubitemid 27494126)
55. Roopenian DC, Akilesh S. 2007. FcRn: the neonatal Fc receptor comes of age. Nature Rev Immunol 7:715-725. (Pubitemid 47327396)
56. Shepard TH. 1998. Catalog of teratogenic agents, 9th ed. Baltimore: The Johns Hopkins University Press.
57. Simister NE. 2003. Placental transport of immunoglobulin G. Vaccine 21:3365-3369. (Pubitemid 36792087)
58. Simister NE, Story CM. 1997. Human placental Fc receptors and the transmission of antibodies from mother to fetus. J Reprod Immunol 37:1-23. (Pubitemid 28052668)
59. Tanigawa K, Kawaguchi M, Tanaka O, Kato Y. 1991. Skeletal malformations in rat off spring. Long-term effects of maternal-insulin induced hypoglycemia during organogenesis. Diabetes 40:1115-1121.
60. Treacy G. 2000. Using an analogous monoclonal antibody to evaluate the reproductive and chronic toxicity potential for a humanized anti-TNFα monoclonal antibody. Human Exp Toxicol 19:226-228. (Pubitemid 30428170)
61. Trown PW, Wills RJ, Kamm JJ. 1986. The preclinical development of Roferon®-A. Cancer 57:1648-1656. (Pubitemid 16114311)
62. Van der Aa EM, Peereboom-Stegeman JHJC, Noordhoek J, Gribnau FWJ, Russel FGM. 1997. Mechanisms of drug transfer across the placenta. Pharmacy World Sci 20:139-148.
63. Van de Perre P. 2003. Transfer of antibody via mothers's milk. Vaccine 21:3374-3376. (Pubitemid 36792089)
64. Van den Bulck K, De Schaepdrijver L, Fransen J, Delille P, Vriens K, Martin P, Kwok D, Powers G, Coussement W. 2008. Placental transfer and developmental toxicity testing of a human monoclonal antibody in the rabbit. Reprod Toxicol 26:4.
65. Vogel F, Bee W. 1999. Reproductive toxicology in primates: an overview of methods and techniques. In: Weinbauer GF, Korte R, editors. Reproduction in nonhuman primates. Münster, Germany: Waxmann Verlag GmbH. p 95-110.
66. Walthall K, Cappon GD, Hurtt ME, Zoetis T. 2005. Postnatal development of the gastrointestinal system: a species comparison. Birth Def Res (Part B) 74:132-156. (Pubitemid 40632147)
67. Weinbauer GF. 2002. The non-human primate as a model in developmental and reporductive toxcity. In: Korte R, Weinbauer GF, editors. Primate models in pharmaceutical drug development. Münster, Germany: Waxmann Verlag GmbH. p 49-66.
68. Weinbauer GF, Frings W, Fuchs A, Niehaus M, Osterburg I. 2008. Reproductive/developmental toxicity assessment of biopharmaceuticals in nonhuman primates. In: Cavagnaro JA, editor. Preclinical safety evaluation of biopharmaceuticals. Hoboken, NJ: John Wiley & Sons. p 379-397.
69. Wood SL, Beyer BK, Cappon GD. 2003. Species comparison of postnatal CNS development: Functional measures. Birth Def Res B 68:391-407. (Pubitemid 38222015)
70. Wyasbort A, Giroux M, Mansat V, Teixeira M, Dumas JC, Puel J. 1993. Experimental study of transplacental passage of alpha interferon by two assay techniques. Antimicrob Agents Chemother 37:1232-1237. (Pubitemid 23166719)
71. Yang JT, Rayburn H, Hynes RO. 1995. Cell adhesion events mediated by alpha 4 integrins are essential in placental and cardiac development. Development 121:549-560.
72. Zaretsky MV, Alexander JM, Byrd W, Bawdon RE. 2004. Transfer of inflammatory cytokines across the placenta. Obstet Gynecol 103:546-550. (Pubitemid 40459072)
73. Zoetis T, Hurtt ME. 2003a. Species comparison of anatomical and functional renal development. Birth Def Res B 68:111-120. (Pubitemid 38222008)
74. Zoetis T, Hurtt ME. 2003b. Species comparison of lung development. Birth Def Res 68:121-124. (Pubitemid 38222009)
75. Zoetis T, Tassinari MS, Bagi C, Walthall K, Hurtt ME. 2003. Species comparison of postnatal bone growth and development. Birth Def Res B 68:86-110. (Pubitemid 38228376)
76. Zuhlke U, Korte S, Niggerman B, Fuchs A, Muller W. 2002. The common marmoset (callithrix jacchus) as a model in biotechnology. In: Korte R, Vogel F, Weinbauer GF, editors. Primate models in pharmaceutical development. Münster, Germany: Waxmann Verlag GmbH. p 119-126.