Mechanistic understanding for the greater sensitivity of monkeys to antisense oligonucleotide-mediated complement activation compared with humans

Journal of Pharmacology and Experimental Therapeutics

Volumn 351, Issue 3, 2014, Pages 709-717

  Shen, Lijiang ^a   Frazer Abel, Ashley ^b   Reynolds, Paul R ^b   Giclas, Patricia C ^b   Chappell, Alfred ^a   Pangburn, Michael K ^c   Younis, Husam ^a   Henry, Scott P ^a  

^a ISIS PHARMACEUTICALS   (United States)

^b DEPARTMENT OF MEDICINE   (United States)

^c UNIVERSITY OF TEXAS HEALTH CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANTISENSE OLIGONUCLEOTIDE; COMPLEMENT FACTOR H; ISIS 183750; ISIS 426115; PLACEBO; UNCLASSIFIED DRUG;

ADULT; AMINO ACID SEQUENCE; ANIMAL EXPERIMENT; ARTICLE; BINDING AFFINITY; BLOOD LEVEL; CELL SURFACE; CFH GENE; COMPLEMENT ACTIVATION; COMPLEMENT ALTERNATIVE PATHWAY; COMPLEMENT INHIBITION; CONTROLLED STUDY; DOUBLE BLIND PROCEDURE; DRUG DOSE ESCALATION; DRUG SENSITIVITY; FEMALE; GENE SEQUENCE; HUMAN; HUMAN EXPERIMENT; IC50; IN VITRO STUDY; IN VIVO STUDY; MACACA FASCICULARIS; MALE; MAXIMUM PLASMA CONCENTRATION; NONHUMAN; NORMAL HUMAN; PHASE 1 CLINICAL TRIAL; PRIORITY JOURNAL; PROTEIN FOLDING; PROTEIN FUNCTION; PROTEIN PURIFICATION; RANDOMIZED CONTROLLED TRIAL; SENSITIVITY ANALYSIS; SEQUENCE ANALYSIS; SINGLE NUCLEOTIDE POLYMORPHISM; ADOLESCENT; ANIMAL; COMPARATIVE STUDY; COMPREHENSION; DOSE RESPONSE; DRUG EFFECTS; GENETICS; MIDDLE AGED; MOLECULAR GENETICS; PHYSIOLOGY; YOUNG ADULT;

ADOLESCENT; ADULT; AMINO ACID SEQUENCE; ANIMALS; COMPLEMENT ACTIVATION; COMPLEMENT FACTOR H; COMPREHENSION; DOSE-RESPONSE RELATIONSHIP, DRUG; DOUBLE-BLIND METHOD; FEMALE; HUMANS; MACACA FASCICULARIS; MALE; MIDDLE AGED; MOLECULAR SEQUENCE DATA; OLIGONUCLEOTIDES, ANTISENSE; YOUNG ADULT;

EID: 84925554865     PISSN: 00223565     EISSN: 15210103     Source Type: Journal    
DOI: 10.1124/jpet.114.219378     Document Type: Article

References (32)

1. Abrera-Abeleda MA, Nishimura C, Smith JL, Sethi S, McRae JL, Murphy BF, Silvestri G, Skerka C, Józsi M, Zipfel PF, et al. (2006) Variations in the complement regulatory genes factor H (CFH) and factor H related 5 (CFHR5) are associated with membranoproliferative glomerulonephritis type II (dense deposit disease). J Med Genet 43:582-589.
2. Advani R, Lum BL, Fisher GA, Halsey J, Geary RS, Holmlund JT, Kwoh TJ, Dorr FA, and Sikic BI (2005) A phase I trial of aprinocarsen (ISIS 3521/LY900003), an antisense inhibitor of protein kinase C-alpha administered as a 24-hour weekly infusion schedule in patients with advanced cancer. Invest New Drugs 23:467-477.
3. Atkinson JP and Goodship TH (2007) Complement factor H and the hemolytic uremic syndrome. J Exp Med 204:1245-1248.
4. Burns VE, Edwards KM, Ring C, Drayson M, and Carroll D (2008) Complement cascade activation after an acute psychological stress task. Psychosom Med 70:387-396.
5. Chi KN, Eisenhauer E, Fazli L, Jones EC, Goldenberg SL, Powers J, Tu D, and Gleave ME (2005) A phase I pharmacokinetic and pharmacodynamic study of OGX-011, a 2′-methoxyethyl antisense oligonucleotide to clusterin, in patients with localized prostate cancer. J Natl Cancer Inst 97:1287-1296.
6. Crooke ST ed (2001) Antisense drug technology: Basic principles, strategies, and applications. Marcel Dekker, Inc., New York.
7. de Córdoba SR and de Jorge EG (2008) Translational mini-review series on complement factor H: genetics and disease associations of human complement factor H. Clin Exp Immunol 151:1-13.
8. Donoso LA, Vrabec T, and Kuivaniemi H (2010) The role of complement Factor H in age-related macular degeneration: a review. Surv Ophthalmol 55:227-246.
9. Edwards AO, Ritter R, 3rd, Abel KJ, Manning A, Panhuysen C, and Farrer LA (2005) Complement factor H polymorphism and age-related macular degeneration. Science 308:421-424.
10. Galbraith WM, Hobson WC, Giclas PC, Schechter PJ, and Agrawal S (1994) Complement activation and hemodynamic changes following intravenous administration of phosphorothioate oligonucleotides in the monkey. Antisense Res Dev 4:201-206.
11. Glover JM, Leeds JM, Mant TG, Amin D, Kisner DL, Zuckerman JE, Geary RS, Levin AA, and Shanahan WR, Jr (1997) Phase I safety and pharmacokinetic profile of an intercellular adhesion molecule-1 antisense oligodeoxynucleotide (ISIS 2302). J Pharmacol Exp Ther 282:1173-1180.
12. Hageman GS, Anderson DH, Johnson LV, Hancox LS, Taiber AJ, Hardisty LI, Hageman JL, Stockman HA, Borchardt JD, Gehrs KM, et al. (2005) A common haplotype in the complement regulatory gene factor H (HF1/CFH) predisposes individuals to age-related macular degeneration. Proc Natl Acad Sci USA 102:7227-7232.
13. Haines JL, Hauser MA, Schmidt S, Scott WK, Olson LM, Gallins P, Spencer KL, Kwan SY, Noureddine M, Gilbert JR, et al. (2005) Complement factor H variant increases the risk of age-related macular degeneration. Science 308:419-421.
14. Hartmann G, Weiner GJ, and Krieg AM (1999) CpG DNA: a potent signal for growth, activation, and maturation of human dendritic cells. Proc Natl Acad Sci USA 96:9305-9310.
15. Henry SP, Beattie G, Yeh G, Chappel A, Giclas P, Mortari A, Jagels MA, Kornbrust DJ, and Levin AA (2002) Complement activation is responsible for acute toxicities in rhesus monkeys treated with a phosphorothioate oligodeoxynucleotide. Int Immunopharmacol 2:1657-1666.
16. Henry SP, Giclas PC, Leeds J, Pangburn M, Auletta C, Levin AA, and Kornbrust DJ (1997a) Activation of the alternative pathway of complement by a phosphorothioate oligonucleotide: potential mechanism of action. J Pharmacol Exp Ther 281:810-816.
17. Henry SP, Jagels MA, Hugli TE, Manalili S, Geary RS, Giclas PC, and Levin AA (2014) Mechanism of alternative complement pathway dysregulation by a phosphorothioate oligonucleotide in monkey and human serum. Nucleic Acid Ther 24:326-335.
18. Henry SP, Monteith D, Kornbrust DJ, and Levin AA (1997b) Effects of intravenous infusion of phosphorothioate oligonucleotides on coagulation, complement activation and hemodynamics. Nucleosides Nucleotides 16:1673-1676.
19. Jalanko H, Peltonen S, Koskinen A, Puntila J, Isoniemi H, Holmberg C, Pinomaki A, Armstrong E, Koivusalo A, Tukiainen E, et al. (2008) Successful liver-kidney transplantation in two children with aHUS caused by a mutation in complement factor H. Am J Transplant 8:216-221.
20. Kastelein JJ, Wedel MK, Baker BF, Su J, Bradley JD, Yu RZ, Chuang E, Graham MJ, and Crooke RM (2006) Potent reduction of apolipoprotein B and low-density lipoprotein cholesterol by short-term administration of an antisense inhibitor of apolipoprotein B. Circulation 114:1729-1735.
21. Klinman DM, Takeshita F, Gursel I, Leifer C, Ishii KJ, Verthelyi D, and Gursel M (2002) CpG DNA: recognition by and activation of monocytes. Microbes Infect 4:897-901.
22. Lehtinen MJ, Rops AL, Isenman DE, van der Vlag J, and Jokiranta TS (2009) Mutations of factor H impair regulation of surface-bound C3b by three mechanisms in atypical hemolytic uremic syndrome. J Biol Chem 284:15650-15658.
23. Licht C, Heinen S, Józsi M, Löschmann I, Saunders RE, Perkins SJ, Waldherr R, Skerka C, Kirschfink M, Hoppe B, et al. (2006) Deletion of Lys224 in regulatory domain 4 of Factor H reveals a novel pathomechanism for dense deposit disease (MPGN II). Kidney Int 70:42-50.
24. Nemunaitis J, Holmlund JT, Kraynak M, Richards D, Bruce J, Ognoskie N, Kwoh TJ, Geary R, Dorr A, Von Hoff D, et al. (1999) Phase I evaluation of ISIS 3521, an antisense oligodeoxynucleotide to protein kinase C-alpha, in patients with advanced cancer. J Clin Oncol 17:3586-3595.
25. Pickering MC, Cook HT, Warren J, Bygrave AE, Moss J, Walport MJ, and Botto M (2002) Uncontrolled C3 activation causes membranoproliferative glomerulonephritis in mice deficient in complement factor H. Nat Genet 31:424-428.
26. Rudin CM, Holmlund J, Fleming GF, Mani S, Stadler WM, Schumm P, Monia BP, Johnston JF, Geary R, Yu RZ, et al. (2001) Phase I Trial of ISIS 5132, an antisense oligonucleotide inhibitor of c-raf-1, administered by 24-hour weekly infusion to patients with advanced cancer. Clin Cancer Res 7:1214-1220.
27. Sethi S, Gamez JD, Vrana JA, Theis JD, Bergen HR, 3rd, Zipfel PF, Dogan A, and Smith RJ (2009) Glomeruli of Dense Deposit Disease contain components of the alternative and terminal complement pathway. Kidney Int 75:952-960.
28. Sewell KL, Geary RS, Baker BF, Glover JM, Mant TGK, Yu RZ, Tami JA, and Dorr FA (2002) Phase I trial of ISIS 104838, a 2′-methoxyethyl modified antisense oligonucleotide targeting tumor necrosis factor-alpha. J Pharmacol Exp Ther 303:1334-1343.
29. Talbot DC, Ranson M, Davies J, Lahn M, Callies S, André V, Kadam S, Burgess M, Slapak C, Olsen AL, et al. (2010) Tumor survivin is downregulated by the antisense oligonucleotide LY2181308: a proof-of-concept, first-in-human dose study. Clin Cancer Res 16:6150-6158.
30. Tanioka M, Nokihara H, Yamamoto N, Yamada Y, Yamada K, Goto Y, Fujimoto T, Sekiguchi R, Uenaka K, Callies S, et al. (2011) Phase I study of LY2181308, an antisense oligonucleotide against survivin, in patients with advanced solid tumors. Cancer Chemother Pharmacol 68:505-511.
31. Taylor CM (2001) Hemolytic-uremic syndrome and complement factor H deficiency: clinical aspects. Semin Thromb Hemost 27:185-190.
32. Yu RZ, Kim T-W, Hong A, Watanabe TA, Gaus HJ, and Geary RS (2007) Cross-species pharmacokinetic comparison from mouse to man of a second-generation antisense oligonucleotide, ISIS 301012, targeting human apolipoprotein B-100. Drug Metab Dispos 35:460-468.