Home LiteratureArticle Details
PMID: 20225083 Published · ppublish English Journal Article Research Support, N.I.H., Extramural Research Support, Non-U.S. Gov't Research Support, U.S. Gov't, Non-P.H.S.

Targeting activated integrin alphavbeta3 with patient-derived antibodies impacts late-stage multiorgan metastasis.

Clinical & experimental metastasis ·Vol. 27 ·No. 4 ·2010-04-00 ·Pages 217-31

Staflin K, Krueger JS, Hachmann J, Forsyth JS, Lorger M, Steiniger SC, Mee J, Pop C, Salvesen GS, Janda KD, Felding-Habermann B

Abstract

Advanced metastatic disease is difficult to manage and specific therapeutic targets are rare. We showed earlier that metastatic breast cancer cells use the activated conformer of adhesion receptor integrin alphavbeta3 for dissemination. We now investigated if targeting this form of the receptor can impact advanced metastatic disease, and we analyzed the mechanisms involved. Treatment of advanced multi-organ metastasis in SCID mice with patient-derived scFv antibodies specific for activated integrin alphavbeta3 caused stagnation and regression of metastatic growth. The antibodies specifically localized to tumor lesions in vivo and inhibited alphavbeta3 ligand binding at nanomolar levels in vitro. At the cellular level, the scFs associated rapidly with high affinity alphavbeta3 and dissociated extremely slowly. Thus, the scFvs occupy the receptor on metastatic tumor cells for prolonged periods of time, allowing for inhibition of established cell interaction with natural alphavbeta3 ligands. Potential apoptosis inducing effects of the antibodies through interaction with caspase-3 were studied as potential additional mechanism of treatment response. However, in contrast to a previous concept, neither the RGD-containing ligand mimetic scFvs nor RGD peptides bound or activated caspase-3 at the cellular or molecular level. This indicates that the treatment effects seen in the animal model are primarily due to antibody interference with alphavbeta3 ligation. Inhibition of advanced metastatic disease by treatment with cancer patient derived single chain antibodies against the activated conformer of integrin alphavbeta3 identifies this form of the receptor as a suitable target for therapy.

MeSH Terms
Animals Caspase 3/metabolism Disease Models, Animal Humans Integrin alphaVbeta3/antagonists & inhibitors,immunology,metabolism Mice Mice, SCID Neoplasm Metastasis/drug therapy,immunology,pathology,prevention & control Single-Chain Antibodies/immunology,therapeutic use
Chemicals
Integrin alphaVbeta3 Single-Chain Antibodies Caspase 3
Authors & Affiliations
11 authors, click to expand affiliations / ORCID
Staflin Karin
Department of Molecular and Experimental Medicine, The Scripps Research Institute, 10550 North Torrey Pines Road, La Jolla, CA 92037, USA.
Krueger Joseph S
Hachmann Janna
Forsyth Jane S
Lorger Mihaela
Steiniger Sebastian C J
Mee Jenny
Pop Cristina
Salvesen Guy S
Janda Kim D
Felding-Habermann Brunhilde
References (46)
46 references, click to expand
  1. Phage-display library selection of high-affinity human single-chain antibodies to tumor-associated carbohydrate antigens sialyl Lewisx and Lewisx.
    Proc Natl Acad Sci U S A. 1999 Jun 8;96(12):6953-8 PMID: 10359820
  2. Clinical approaches toward tumor angiogenesis: past, present and future.
    Curr Pharm Des. 2008;14(36):3820-34 PMID: 19128235
  3. Requirement of vascular integrin alpha v beta 3 for angiogenesis.
    Science. 1994 Apr 22;264(5158):569-71 PMID: 7512751
  4. Combinatorial antibody libraries from cancer patients yield ligand-mimetic Arg-Gly-Asp-containing immunoglobulins that inhibit breast cancer metastasis.
    Proc Natl Acad Sci U S A. 2004 Dec 7;101(49):17210-5 PMID: 15563590
  5. Activation of integrin alpha(V)beta(3) regulates cell adhesion and migration to bone sialoprotein.
    Exp Cell Res. 2000 Feb 1;254(2):299-308 PMID: 10640428
  6. alpha(v)beta(3) Integrin in central nervous system tumors.
    Hum Pathol. 2005 Jun;36(6):665-9 PMID: 16021573
  7. Down-regulation of caspase 3 in breast cancer: a possible mechanism for chemoresistance.
    Oncogene. 2002 Dec 12;21(57):8843-51 PMID: 12483536
  8. Caspase-3 is required for alpha-fodrin cleavage but dispensable for cleavage of other death substrates in apoptosis.
    J Biol Chem. 1998 Jun 19;273(25):15540-5 PMID: 9624143
  9. Integrins, cations and ligands: making the connection.
    J Thromb Haemost. 2003 Jul;1(7):1642-54 PMID: 12871301
  10. Anti-angiogenic cancer therapy based on integrin alphavbeta3 antagonism.
    Anticancer Agents Med Chem. 2006 Sep;6(5):407-28 PMID: 17017851
  11. Phase I trial of a monoclonal antibody specific for alphavbeta3 integrin (MEDI-522) in patients with advanced malignancies, including an assessment of effect on tumor perfusion.
    Clin Cancer Res. 2005 Nov 1;11(21):7851-60 PMID: 16278408
  12. Get a ligand, get a life: integrins, signaling and cell survival.
    J Cell Sci. 2002 Oct 1;115(Pt 19):3729-38 PMID: 12235283
  13. Binding Affinity of Metal Ions to the CD11b A-domain Is Regulated by Integrin Activation and Ligands.
    J Biol Chem. 2004 Jun 11;279(24):25483-8 PMID: 15070893
  14. Stage-specific expression of integrin alphaVbeta3 in neuroblastic tumors.
    Am J Pathol. 1996 May;148(5):1423-34 PMID: 8623914
  15. Comparison of cell adhesion molecule expression between glioblastoma multiforme and autologous normal brain tissue.
    J Neuroimmunol. 1995 Mar;57(1-2):143-53 PMID: 7535788
  16. Integrin alpha v beta 3 antagonists promote tumor regression by inducing apoptosis of angiogenic blood vessels.
    Cell. 1994 Dec 30;79(7):1157-64 PMID: 7528107
  17. Measures of response: RECIST, WHO, and new alternatives.
    J Clin Oncol. 2006 Jul 10;24(20):3245-51 PMID: 16829648
  18. MDA-MB-435 and M14 cell lines: identical but not M14 melanoma?
    Cancer Res. 2009 Jul 1;69(13):5292-3 PMID: 19549886
  19. Maintenance of caspase-3 proenzyme dormancy by an intrinsic "safety catch" regulatory tripeptide.
    Proc Natl Acad Sci U S A. 2001 May 22;98(11):6132-7 PMID: 11353841
  20. Potent antibody therapeutics by design.
    Nat Rev Immunol. 2006 May;6(5):343-57 PMID: 16622479
  21. Heterogeneity of drug target expression among metastatic lesions: lessons from a breast cancer autopsy program.
    Clin Cancer Res. 2008 Jun 15;14(12):3643-5 PMID: 18559575
  22. RGD peptides induce apoptosis by direct caspase-3 activation.
    Nature. 1999 Feb 11;397(6719):534-9 PMID: 10028971
  23. Integrin activation controls metastasis in human breast cancer.
    Proc Natl Acad Sci U S A. 2001 Feb 13;98(4):1853-8 PMID: 11172040
  24. Role of integrin alpha(v)beta3 in vascular biology.
    Thromb Haemost. 1998 Nov;80(5):726-34 PMID: 9843163
  25. Integrin distribution in malignant melanoma: association of the beta 3 subunit with tumor progression.
    Cancer Res. 1990 Oct 15;50(20):6757-64 PMID: 2208139
  26. New insights into the structural basis of integrin activation.
    Blood. 2003 Aug 15;102(4):1155-9 PMID: 12714499
  27. New response evaluation criteria in solid tumours: revised RECIST guideline (version 1.1).
    Eur J Cancer. 2009 Jan;45(2):228-47 PMID: 19097774
  28. Pharmacokinetics and biodistribution of genetically-engineered antibodies.
    Q J Nucl Med. 1998 Dec;42(4):225-41 PMID: 9973838
  29. The role of alpha(v)beta(3) in prostate cancer progression.
    Neoplasia. 2002 May-Jun;4(3):191-4 PMID: 11988838
  30. Expression, purification, and characterization of caspases.
    Curr Protoc Protein Sci. 2003 Feb;Chapter 21:Unit 21.13 PMID: 18429241
  31. An integrin alpha(v)beta(3)-c-Src oncogenic unit promotes anchorage-independence and tumor progression.
    Nat Med. 2009 Oct;15(10):1163-9 PMID: 19734908
  32. The pattern of enhancement of Src kinase activity on platelet-derived growth factor stimulation of glioblastoma cells is affected by the integrin engaged.
    J Biol Chem. 2003 Oct 10;278(41):39882-91 PMID: 12881526
  33. Integrins and angiogenesis.
    Curr Top Dev Biol. 2004;64:207-38 PMID: 15563949
  34. Engineered antibody fragments and the rise of single domains.
    Nat Biotechnol. 2005 Sep;23(9):1126-36 PMID: 16151406
  35. Integrins in cancer: biological implications and therapeutic opportunities.
    Nat Rev Cancer. 2010 Jan;10(1):9-22 PMID: 20029421
  36. Integrin activation and structural rearrangement.
    Immunol Rev. 2002 Aug;186:141-63 PMID: 12234369
  37. Structural basis of integrin regulation and signaling.
    Annu Rev Immunol. 2007;25:619-47 PMID: 17201681
  38. RECIST revisited: a review of validation studies on tumour assessment.
    Eur J Cancer. 2006 May;42(8):1031-9 PMID: 16616487
  39. RGDS peptide induces caspase 8 and caspase 9 activation in human endothelial cells.
    Blood. 2004 Jun 1;103(11):4180-7 PMID: 14982875
  40. Pro-caspase-3 is a major physiologic target of caspase-8.
    J Biol Chem. 1998 Oct 16;273(42):27084-90 PMID: 9765224
  41. RGD peptide-induced apoptosis in human leukemia HL-60 cells requires caspase-3 activation.
    Cell Biol Toxicol. 2000;16(5):275-83 PMID: 11201051
  42. Ligands for mapping alphavbeta3-integrin expression in vivo.
    Acc Chem Res. 2009 Jul 21;42(7):969-80 PMID: 19489579
  43. Phage-displayed random peptide libraries in mice: toxicity after serial panning.
    Cancer Chemother Pharmacol. 2002 Oct;50(4):325-32 PMID: 12357308
  44. Comment Re: MDA-MB-435 and M14 cell lines: identical but not M14 Melanoma?
    Cancer Res. 2009 Oct 1;69(19):7893 PMID: 19723654
  45. Chick embryo chorioallantoic membrane model systems to study and visualize human tumor cell metastasis.
    Histochem Cell Biol. 2008 Dec;130(6):1119-30 PMID: 19005674
  46. Small molecule integrin antagonists in cancer therapy.
    Mini Rev Med Chem. 2009 Oct;9(12):1439-46 PMID: 19929817
Article Info
Journal
Clinical & experimental metastasis
Abbr.
Clin Exp Metastasis
ISSN
1573-7276
Published
2010-04-00
Epub
2010-00-12
Pages
217-31
Language
English
Region
Netherlands
NLM ID
8409970
PMCID
PMC4830478
Subset
IM
Grants
NCI NIH HHS · R01 CA095458 · United States
NCI NIH HHS · R01 CA112287 · United States
NCI NIH HHS · CA095458 · United States
NCI NIH HHS · CA112287 · United States
Analysis Services
Analysis Services

Contact

No. 2 Wenbo Road, Zhangqiu District, Jinan, Shandong

Qilu Normal University · Genelibs Bioinformatics Lab

750 Shunhua Rd, Jinan

2F, Bldg F, University Science Park

Tel: 0531-88819269

WeChat Official Account

Follow our WeChat subscription account for real-time updates and the latest in medical and biological research.


Business Email

E-mail: product@genelibs.com