Anticalins as an alternative to antibody technology

Expert Opinion on Biological Therapy

Volumn 5, Issue 11, 2005, Pages 1453-1462

  Schlehuber, Steffen ^b   Skerra, Arne ^a  

^a TECHNICAL UNIVERSITY OF MUNICH   (Germany)

^b Pieris Pharmaceuticals GmbH   (Germany)

Author keywords

Antagonist; Antidote; Antigen; Binding protein; Combinatorial engineering; Drug targeting; Hapten; Lipocalin; Protein design

Indexed keywords

6B4 ANTIBODY; ANTIBIOTIC AGENT; ANTIBODY; ANTICALIN; ANTICOAGULANT AGENT; ANTIDOTE; ANTITHROMBOCYTIC AGENT; BEVACIZUMAB; BILIN BINDING PROTEIN; BINDING PROTEIN; CORTICOSTEROID; CYTOTOXIC T LYMPHOCYTE ANTIGEN 4; DIGICAL; DIGITALIS; DIGOXIN ANTIBODY; DIGOXIN ANTIBODY F(AB) FRAGMENT; DIGOXIN BINDING PROTEIN; GEMTUZUMAB OZOGAMICIN; HIRUDIN; HISTAMINE BINDING PROTEIN; IMMUNOGLOBULIN; IPILIMUMAB; LIPOCALIN; MOUBATIN; NEUTRALIZING ANTIBODY; NITROPHORIN; PALLIDIPIN; PROTEIN NGAL; PROTEIN TLC; RHODNIUS PROXILUS PLATELET AGGREGATION INHIBITOR; TRIABIN; UNCLASSIFIED DRUG;

ACUTE GRANULOCYTIC LEUKEMIA; ALLERGIC DISEASE; ANAPHYLAXIS; ANTICOAGULANT THERAPY; ANTIMICROBIAL ACTIVITY; ARTERY THROMBOSIS; BODY FLUID; CANCER; CANCER IMMUNOTHERAPY; CLINICAL TRIAL; COMPARATIVE STUDY; COMPLEX FORMATION; DIGITALIS INTOXICATION; DRUG EFFICACY; DRUG EXCRETION; DRUG HALF LIFE; DRUG PENETRATION; DRUG PROTEIN BINDING; HEART ARRHYTHMIA; HEART FAILURE; HUMAN; IMMUNOTOXICITY; INSECT; LIGAND BINDING; LIVER TOXICITY; MACROMOLECULE; MOLECULAR WEIGHT; MYCOSIS; NONHUMAN; PLASMA; PROTEIN ENGINEERING; PROTEIN FAMILY; PROTEIN FOLDING; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; PROTEIN STABILITY; PROTEIN STRUCTURE; PROTEIN SYNTHESIS; PROTEIN TARGETING; PROTEIN TERTIARY STRUCTURE; PROTEIN VARIANT; RECEPTOR BINDING; REVIEW; SEPSIS; SITE DIRECTED MUTAGENESIS; SOLID TUMOR; STORAGE; THROMBOCYTE AGGREGATION INHIBITION; THROMBOCYTOPENIA; TICK;

ANIMALS; ANTIBODIES; CARRIER PROTEINS; HUMANS; LIGANDS; PROTEIN BINDING; PROTEIN ENGINEERING; PROTEINS;

ACARI; DIGITALIS; INSECTA; RHODNIUS;

EID: 27644540066     PISSN: 14712598     EISSN: None     Source Type: Journal    
DOI: 10.1517/14712598.5.11.1453     Document Type: Review

References (93)

1. FLOWER DR: The lipocalin protein family: structure and function. Biochem. J. (1996) 318:1-14.
2. SKERRA A: Lipocalins as a scaffold. Biochim. Biophys. Acta (2000) 1482:337-350.
3. BISHOP RE, WEINER JH: 'Outlier' lipocalins more than peripheral. Trends Biochem. Sci. (1996) 21:127.
4. NEWCOMER ME, JONES TA, AQVIST J et al.: The three-dimensional structure of retinol-binding protein. EMBO J. (1984) 3:1451-1454.
5. FLOWER DR: Multiple molecular recognition properties of the lipocalin protein family. J. Mol. Recognit. (1995) 8:185-195.
6. COWAN S, NEWCOMER M, JONES T: Crystallographic refinement of human serum retinol binding protein at 2Å resolution. Proteins (1990) 8:44-61.
7. BIANCHET MA, BAINS G, PELOSI P et al.: The three-dimensional structure of bovine odorant binding protein and its mechanism of odor recognition. Nat. Struct. Biol. (1996) 3:934-939.
8. BOCSKEIZ, GROOM CR, FLOWER DR et al.: Pheromone binding to two rodent urinary proteins revealed by X-ray crystallography. Nature (1992) 360:186-188.
9. URADE Y, HAYAISHI O: Biochemical, structural, genetic, physiological, and pathophysiological features of lipocalin-type prostaglandin D synthase. Biochim. Biophys. Acta (2000) 1482:259-271.
10. GOETZ DH, HOLMES MA, BORREGAARD N, BLUHM ME, RAYMOND KN, STRONG RK: The neutrophil lipocalin NGAL is a bacteriostatic agent that interferes with siderophore-mediated iron acquisition. Mol. Cell (2002) 10:1033-1043.
11. FLO TH, SMITH KD, SATO S et al.: Lipocalin 2 mediates an innate immune response to bacterial infection by sequestrating iron. Nature (2004) 432:917-921.
12. BREUSTEDT DA, KORNDÖRFER IP, REDL B, SKERRA A: The 1.8-A crystal structure of human tear lipocalin reveals an extended branched cavity with capacity for multiple ligands. J. Biol. Chem. (2005) 280:484-493.
13. GLASGOW BJ, ABDURAGIMOV AR, FARAHBAKHSH ZT, FAULL KF, HUBBELL WL: Tear lipocalins bind a broad array of lipid ligands. Curr. Eye Res. (1995) 14:363-372.
14. REDL B: Human tear lipocalin. Biochim. Biophys. Acta (2000) 1482:241-248.
15. REDL B, HOLZFEIND P, LOTTSPEICH F: cDNA cloning and sequencing reveals human tear prealbumin to be a member of the lipophilic-ligand carrier protein superfamily. J. Biol. Chem. (1992) 267:20282-20287.
16. GASYMOV OK, ABDURAGIMOV AR, YUSIFOV TN, GLASGOW BJ: Relaxation of β-structure in tear lipocalin and enhancement of retinoid binding. Invest. Ophthalmol. Vis. Sci. (2002) 43:3165-3173.
17. LECHNER M, WOJNAR P, REDL B: Human tear lipocalin acts as an oxidativestress-induced scavenger of potentially harmful lipid peroxidation products in a cell culture system. Biochem. J. (2001) 356:129-135.
18. FLUCKINGER M, HAAS H, MERSCHAK P, GLASGOW BJ, REDL B: Human tear lipocalin exhibits antimicrobial activity by scavenging microbial siderophores. Antimicrob. Agents Chemother. (2004) 48:3367-3372.
19. GASYMOV OK, ABDURAGIMOV AR, GASIMOV EO, YUSIFOV TN, DOOLEY AN, GLASGOW BJ: Tear lipocalin: potential for selective delivery of rifampin. Biochim. Biophys. Acta (2004) 1688:102-111.
20. QIN BY, BEWLEY MC, CREAMER LK, BAKER HM, BAKER EN, JAMESON GB: Structural basis of the Tanford transition of bovine β-lactoglobulin. Biochemistry (1998) 37:14014-14023.
21. GOETZ DH, WILLIE ST, ARMEN RS, BRATT T, BORREGAARD N, STRONG RK: Ligand preference inferred from the structure of neutrophil gelatinase associated lipocalin. Biochemistry (2000) 39:1935-1941.
22. RASSART E, BEDIRIAN A, DO CARMO S et al.: Apolipoprotein D. Biochim. Biophys. Acta (2000) 1482:185-198.
23. VOGT M, SKERRA A: Bacterially produced apolipoprotein D binds progesterone and arachidonic acid, but not bilirubin or E-3M2H. J. Mol. Recognit. (2001) 14:79-86.
24. SCHINDLER PA, SETTINERI CA, COLLET X, FIELDING CJ, BURLINGAME AL: Site-specific detection and structural characterization of the glycosylation of human plasma proteins lecithin:cholesterol acyltransferase and apolipoprotein D using HPLC/electrospray mass spectrometry and sequential glycosidase digestion. Protein Sci. (1995) 4:791-803.
25. ZENG C, SPIELMAN AI, VOWELS BR, LEYDEN JJ, BIEMANN K, PRETI G: A human axillary odorant is carried by apolipoprotein D. Proc. Natl. Acad. Sci. USA (1996) 93:6626-6630.
26. COLES M, DIERCKS T, MUEHLENWEG B et al.: The solution structure and dynamics of human neutrophil gelatinase-associated lipocalin. J. Mol. Biol. (1999) 289:139-157.
27. FLOWER DR: Beyond the superfamily: the lipocalin receptors. Biochim. Biophys. Acta (2000) 1482:327-336.
28. HVIDBERG V, JACOBSEN C, STRONG RK, COWLAND JB, MOESTRUP SK, BORREGAARD N: The endocytic receptor megalin binds the iron transporting neutrophil- gelatinase-associated lipocalin with high affinity and mediates its cellular uptake. FEBS Lett. (2005) 579:773-777.
29. YANG J, GOETZ D, LI JY et al.: An iron delivery pathway mediated by a lipocalin. Mol. Cell (2002) 10:1045-1056.
30. MORI K, LEE HT, RAPOPORT D et al.: Endocytic delivery of lipocalin-siderophore-iron complex rescues the kidney from ischemia-reperfusion injury. J. Clin. Invest. (2005) 115:610-621.
31. WOJNAR P, LECHNER M, MERSCHAK P, REDL B: Molecular cloning of a novel lipocalin-1 interacting human cell membrane receptor using phage display. J. Biol. Chem. (2001) 276:20206-20212.
32. MICHAUD GA, SALCIUS M, ZHOU F et al.: Analyzing antibody specificity with whole proteome microarrays. Nat. Biotechnol. (2003) 21:1509-1512.
33. JAIN RK, BAXTER LT: Mechanisms of heterogeneous distribution of monoclonal antibodies and other macromolecules in tumors: significance of elevated interstitial pressure. Cancer Res. (1988) 48:7022-7032.
34. SKERRA A: Engineered protein scaffolds for molecular recognition. J. Mol. Recognit. (2000) 13:167-187.
35. NYGREN PA, SKERRA A: Binding proteins from alternative scaffolds. J. Immunol. Methods (2004) 290:3-28.
36. SCHLEHUBER S, SKERRA A: Tuning ligand affinity, specificity, and folding stability of an engineered lipocalin variant - a so-called 'anticalin' - using a molecular random approach. Biophys. Chem. (2002) 96:213-228.
37. COUILLIN I, MAILLET I, VARGAFTIG BB et al.: Arthropod-derived histamine-binding protein prevents murine allergic asthma. J. Immunol. (2004) 173:3281-3286.
38. SCHMIDT FS, SKERRA A: The bilin-binding protein of Pieris brassicae. cDNA sequence and regulation of expression reveal distinct features of this insect pigment protein. Eur. J. Biochem. (1994) 219:855-863.
39. HUBER R, SCHNEIDER M, MAYR I et al.: Molecular structure of the bilin binding protein (BBP) from Pieris brassicae after refinement at 2.0 A resolution. J. Mol. Biol. (1987) 198:499-513.
40. BESTE G, SCHMIDT FS, STIBORA T, SKERRAA: Small antibody-like proteins with prescribed ligand specificities derived from the lipocalin fold. Proc. Natl. Acad. Sci. USA (1999) 96:1898-1903.
41. SKERRA A: 'Anticalins': a new class of engineered ligand-binding proteins with antibody-like properties. J. Biotechnol. (2001) 74:257-275.
42. VOSS EW: Fluorescein Hapten: An Immunological Probe. Voss EW (Ed.), CRC Press: Boca Raton, FL, USA (1984).
43. MCCREERY T: Digoxigenin labeling. Mol. Biotechnol. (1997) 7:121-124.
44. SCHLEHUBER S, BESTE G, SKERRA A: A novel type of receptor protein, based on the lipocalin scaffold, with specificity for digoxigenin. J. Mol. Biol. (2000) 297:1105-1120.
45. MERCADER JV, SKERRA A: Generation of anticalins with specificity for a nonsymmetric phthalic acid ester. Anal. Biochem. (2002) 308:269-277.
46. KORNDÖRFER IP, BESTE G, SKERRA A: Crystallographic analysis of an 'anticalin' with tailored specificity for fluorescein reveals high structural plasticity of the lipocalin loop region. Proteins (2003) 53:121-129.
47. KORNDÖRFER IP, SCHLEHUBER S, SKERRA A: Structural mechanism of specific ligand recognition by a lipocalin tailored for the complexation of digoxigenin. J Mol. Biol. (2003) 330:385-396.
48. JEFFREY PD, SCHILDBACH JF, CHANG CY, KUSSIE PH, MARGOLIES MN, SHERIFF S: Structure and specificity of the anti-digoxin antibody 40-50. J. Mol. Biol. (1995) 248:344-360.
49. HAUPTMAN PJ, KELLY RA: Digitalis. Circulation (1999) 99:1265-1270.
50. MCMILLIN GA, OWEN WE, LAMBERT TL et al.: Comparable effects of DIGIBIND and DigiFab in thirteen digoxin immunoassays. Clin. Chem. (2002) 48:1580-1584.
51. WARD SB, SJOSTROM L, UJHELYI MR: Comparison of the pharmacokinetics and in vivo bioaffinity of DigiTAb versus Digibind. Ther. Drug Monit. (2000) 22:599-607.
52. LECHAT P, MUDGETT-HUNTER M, MARGOLIES MN, HABER E, SMITH TW: Reversal of lethal digoxin toxicity in guinea pigs using monoclonal antibodies and Fab fragments. J. Pharmacol. Exp. Ther. (1984) 229:210-213.
53. KELLY R, PEIM A, WALZ A et al.: Reversal of digoxin cardiac toxicity by an anticalin (Digical II) in the anaesthetized guinea pig. In: Abstracts of the 'The Physiological Society' Meeting. University College Cork, Ireland (2004).
54. GOODMAN DS: Plasma retinol-binding protein. In: The Retinoids. Sporn R, Goodman D (Eds), Academic Press, Orlando, FL, USA (1984):41-87.
55. AXELSSON L, BERGENFELDT M, OHLSSON K: Studies of the release and turnover of a human neutrophil lipocalin. Scand. J. Clin. Lab. Invest. (1995) 55:577-588.
56. 1,-Microglobulin: a yellow-brown lipocalin. Biochim. Biophys. Acta(2000) 1482:172-184.
57. MISHRA J, MORI K, MA Q et al.: Amelioration of ischemic acute renal injury by neutrophil gelatinase-associated lipocalin. J. Am. Soc. Nephrol. (2004) 15:3073-3082.
58. WALSH G: Biopharmaceutical benchmarks - 2003. Nat. Biotechnol. (2003) 21:865-870.
59. VOGT M, SKERRA A: Construction of an artificial receptor protein ('anticalin') based on the human apolipoprotein D. Chembiochem. (2004) 5:191-199.
60. ALLISON JP, KRUMMEL MF: The Yin and Yang of T cell costimulation. Science (1995) 270:932-933.
61. DAVIS SJ, IKEMIZU S, EVANS EJ, FUGGER L, BAKKER TR, VAN DER MERWE PA: The nature of molecular recognition by T cells. Nat. Immunol. (2003) 4:217-224.
62. LEACH DR, KRUMMEL MF, ALLISON JP: Enhancement of antitumor immunity by CTLA-4 blockade. Science (1996)271:1734-1736.
63. KELER T, HALK E, VITALE L et al.: Activity and safety of CTLA-4 blockade combined with vaccines in cynomolgus macaques. J. Immunol. (2003) 171:6251-6259.
64. PHAN GQ, YANG JC, SHERRY RM et al.: Cancer regression and autoimmunity induced by cytotoxic T lymphocyte-associated antigen 4 blockade in patients with metastatic melanoma. Proc. Natl. Acad. Sci. USA (2003) 100:8372-8377.
65. CAMACHO LH, RIBAS A, GLASPY JA et al.: Phase I clinical trial of anti-CTLA4 human monoclonal antibody CP-675,206 in patients (pts) with advanced solid malignancies. J Clin. Oncol. (Meeting Abstracts) (2004) 22:Abstract #2505.
66. MANS BJ, NEITZ AW: Adaptation of ticks to a blood-feeding environment: evolution from a functional perspective. Insect Biochem. Mol. Biol. (2004) 34:1-17.
67. RIBEIRO JM, ANDERSEN J, SILVA-NETO MA, PHAM VM, GARFIELD MK, VALENZUELA JG: Exploring the sialome of the blood-sucking bug Rhodnius prolixus. Insect Biochem. Mol. Biol. (2004) 34:61-79.
68. PAESEN GC, ADAMS PL, HARLOS K, NUTTALL PA, STUART DI: Tick histamine-binding proteins: isolation, cloning, and three-dimensional structure. Mol. Cell (1999) 3:661-671.
69. KEMP DH, BOURNE A: Boophilus microplus: the effect of histamine on the attachment of cattle-tick larvae-studies in vivo and in vitro. Parasitology (1980) 80:487-496.
70. NOESKE-JUNGBLUT C, HAENDLER B, DONNER P, ALAGON A, POSSANI L, SCHLEUNING WD: Triabin, a highly potent exosite inhibitor of thrombin. J. Biol. Chem. (1995) 270:28629-28634.
71. FUENTES-PRIOR P, NOESKE-JUNGBLUT C, DONNER P, SCHLEUNING WD, HUBER R, BODE W: Structure of the thrombin complex with triabin, a lipocalin-like exosite-binding inhibitor derived from a triatomine bug. Proc. Natl. Acad. Sci. USA (1997) 94:11845-11850.
72. GLUSA E, BRETSCHNEIDER E, DAUM J, NOESKE-JUNGBLUT C: Inhibition of thrombin-mediated cellular effects by triabin, a highly potent anion-binding exosite thrombin inhibitor. Thromb. Haemost. (1997) 77:1196-1200.
73. FRANCISCHETTI IM, RIBEIRO JM, CHAMPAGNE D, ANDERSEN J: Purification, cloning, expression, and mechanism of action of a novel platelet aggregation inhibitor from the salivary gland of the blood-sucking bug, Rhodnius prolixus. J. Biol. Chem. (2000) 275:12639-12650.
74. MONTFORT WR, WEICHSEL A, ANDERSEN JF: Nitrophorins and related amihemostatic lipocalins from Rhodnius prolixus and other blood-sucking arthropods. Biochim. Biophys. Acta (2000) 1482:110-118.
75. KELLER PM, WAXMAN L, ARNOLD BA, SCHULTZ LD, CONDRA C, CONNOLLY TM: Cloning of the cDNA and expression of moubatin, an inhibitor of platelet aggregation. J Biol. Chem. (1993) 268:5450-5456.
76. WAXMAN L, CONNOLLY TM: Isolation of an inhibitor selective for collagen-stimulated platelet aggregation from the soft tick Ornithodoros moubata. J. Biol. Chem. (1993) 268:5445-5449.
77. NOESKE-JUNGBLUT C, KRATZSCHMAR J, HAENDLER B et al.: An inhibitor of collagen-induced platelet aggregation from the saliva of Triatoma pallidipennis. J. Biol. Chem. (1994) 269:5050-5053.
78. ANDERSEN JF, FRANCISCHETTI IM, VALENZUELA JG, SCHUCK P, RIBEIRO JM: Inhibition of hemostasis by a high affinity biogenic amine-binding protein from the saliva of a blood-feeding insect. J. Biol. Chem. (2003) 278:4611-4617.
79. BRAUN V, KILLMANN H: Bacterial solutions to the iron-supply problem. Trends Biochem. Sci. (1999) 24:104-109.
80. RATLEDGE C, DOVER LG: Iron metabolism in pathogenic bacteria. Annu. Rev. Microbiol. (2000) 54:881-941.
81. FLOWER DR: Benzon Symposium no. 50: The lipocalin protein superfamily. Targets (2003) 2:235-236.
82. SAMAMA MM, GEROTZIAFAS GT: Evaluation of the pharmacological properties and clinical results of the synthetic pentasaccharide (fondaparinux). Thromb. Res. (2003) 109:1-11.
83. MUHSIN M, GRAHAM J, KIRKPATRICK P: Bevacizumab. Nat. Rev. DrugDiscov. (2004) 3:995-996.
84. BONNEFOY A, VERMYLEN J, HOYLAERTS MF: Inhibition of von Willebrand factor-GPIb/IX/V interactions as a strategy to prevent arterial thrombosis. Expert Rev. Cardiovasc. Ther. (2003) 1:257-269.
85. CAUWENBERGHS N, MEIRING M, VAUTERIN S et al.: Antithrombotic effect of platelet glycoprotein Ib-blocking monoclonal antibody Fab fragments in nonhuman primates. Arterioscler. Thromb. Vasc. Biol. (2000) 20:1347-1353.
86. OSBORN BL, OLSEN HS, NARDELLI B et al.: Pharmacokinetic and pharmacodynamic studies of a human serum albumin-interferon-a fusion protein in cynomolgus monkeys. J. Pharmacol. Exp. Ther. (2002) 303:540-548.
87. HARRIS JM, CHESS RB: Effect of pegylation on pharmaceuticals. Nat. Rev. Drug Discov. (2003) 2:214-221.
88. SCHELLEKENS H: Immunogenicity of therapeutic proteins: clinical implications and future prospects. Clin. Ther. (2002) 24:1720-1740.
89. PASTAN I: Immunotoxins containing Pseudomonas exotoxin A: a short history. Cancer Immunol. Immunother. (2003) 52:338-341.
90. BRINKMANN U, PASTAN I: Immunotoxins against cancer. Biochim. Biophys. Acta (1994) 1198:27-45.
91. CARTER P: Improving the efficacy of antibody-based cancer therapies. Nat. Rev. Cancer (2001) 1:118-129.
92. GILES F, ESTEY E, O'BRIEN S: Gemtuzumab ozogamicin in the treatment of acute myeloid leukemia. Cancer (2003) 98:2095-2104.
93. GILES FJ: Gemtuzumab ozogamicin: promise and challenge in patients with acute myeloid leukemia. Expert Rev. Anticancer Ther. (2002) 2:630-640.