New anti-nodal monoclonal antibodies targeting the nodal pre-helix loop involved in cripto-1 binding

International Journal of Molecular Sciences

Volumn 16, Issue 9, 2015, Pages 21342-21362

  Focà, Annalia ^a,b   Sanguigno, Luca ^c   Focà, Giuseppina ^a,b   Strizzi, Luigi ^d   Iannitti, Roberta ^a   Palumbo, Rosanna ^a   Hendrix, Mary J C ^d   Leonardi, Antonio ^b   Ruvo, Menotti ^a   Sandomenico, Annamaria ^a  

^a CNR   (Italy)

^b UNIVERSITY OF NAPLES FEDERICO II   (Italy)

^c Bioker Multimedica   (Italy)

^d NORTHWESTERN UNIVERSITY   (United States)

Author keywords

Fab fragments; Melanoma; Monoclonal antibody; Nodal; SPR

Indexed keywords

ANTIGEN; CRIPTO 1; MONOCLONAL ANTIBODY; PROTEIN NODAL; RECEPTOR; SMAD2 PROTEIN; SMAD3 PROTEIN; UNCLASSIFIED DRUG; EPITOPE; GLYCOSYLPHOSPHATIDYLINOSITOL ANCHORED PROTEIN; GROWTH DIFFERENTIATION FACTOR; IMMUNOGLOBULIN F(AB) FRAGMENT; PEPTIDE; PROTEIN BINDING; SIGNAL PEPTIDE; TDGF1 PROTEIN, HUMAN; TUMOR PROTEIN;

ANTIBODY SPECIFICITY; ANTIBODY TITER; ARTICLE; BLOOD ANALYSIS; CONTROLLED STUDY; DEGLYCOSYLATION; ENZYME LINKED IMMUNOSORBENT ASSAY; EPITOPE MAPPING; FEMALE; FLUORESCENCE ACTIVATED CELL SORTING; HUMAN; HUMAN CELL; HYBRIDOMA; MATRIX ASSISTED LASER DESORPTION IONIZATION TIME OF FLIGHT MASS SPECTROMETRY; MELANOMA; MOUSE; NONHUMAN; PROTEIN ANALYSIS; PROTEIN BINDING; PROTEIN DEGRADATION; PROTEIN PHOSPHORYLATION; SOLID PHASE SYNTHESIS; SURFACE PLASMON RESONANCE; WESTERN BLOTTING; AMINO ACID SEQUENCE; ANTAGONISTS AND INHIBITORS; CHEMISTRY; ISOLATION AND PURIFICATION; METABOLISM; MOLECULAR GENETICS; MOLECULAR MODEL; PROCEDURES; PROTEIN SECONDARY STRUCTURE; SYNTHESIS;

AMINO ACID SEQUENCE; ANTIBODIES, MONOCLONAL; EPITOPE MAPPING; EPITOPES; GPI-LINKED PROTEINS; GROWTH DIFFERENTIATION FACTORS; HUMANS; IMMUNOGLOBULIN FAB FRAGMENTS; INTERCELLULAR SIGNALING PEPTIDES AND PROTEINS; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; NEOPLASM PROTEINS; NODAL PROTEIN; PEPTIDES; PROTEIN BINDING; PROTEIN STRUCTURE, SECONDARY;

EID: 84941253823     PISSN: 16616596     EISSN: 14220067     Source Type: Journal    
DOI: 10.3390/ijms160921342     Document Type: Article

References (43)

1. Schier, A.F. Nodal signaling in vertebrate development. Annu. Rev. Cell Dev. Biol. 2003, 19, 589–621.
2. Shen, M.M. Nodal signaling: Developmental roles and regulation. Development 2007, 134, 1023–1034.
3. Schier, A.F. Nodal morphogens. Cold Spring Harb. Perspect. Biol. 2009, 1, a003459.
4. Strizzi, L.; Hardy, K.M.; Kirschmann, D.A.; Ahrlund-Richter, L.; Hendrix, M.J. Nodal expression and detection in cancer: Experience and challenges. Cancer Res. 2012, 72, 1915–1920.
5. Strizzi, L.; Postovit, L.M.; Margaryan, N.V.; Lipavsky, A.; Gadiot, J.; Blank, C.; Seftor, R.E.; Seftor, E.A.; Hendrix, M.J. Nodal as a biomarker for melanoma progression and a new therapeutic target for clinical intervention. Expert. Rev. Dermatol. 2009, 4, 67–78.
6. Strizzi, L.; Hardy, K.M.; Margaryan, N.V.; Hillman, D.W.; Seftor, E.A.; Chen, B.; Geiger, X.J.; Thompson, E.A.; Lingle, W.L.; Andorfer, C.A. et al. Potential for the embryonic morphogen Nodal as a prognostic and predictive biomarker in breast cancer. Breast Cancer Res. 2012, 11, R75.
7. Lawrence, M.G.; Margaryan, N.V.; Loessner, D.; Collins, A.; Kerr, K.M.; Turner, M.; Seftor, E.A.; Stephens, C.R.; Lai, J.; Postovit, L.M. et al. Reactivation of embryonic nodal signaling is associated with tumor progression and promotes the growth of prostate cancer cells. Prostate 2011, 71, 1198–1209.
8. Quail, D.F.; Siegers, G.M.; Jewer, M.; Postovit, L.M. Nodal signalling in embryogenesis and tumorigenesis. Int. J. Biochem. Cell Biol. 2013, 45, 885–898.
9. Topczewska, J.M.; Postovit, L.M.; Margaryan, N.V.; Sam, A.; Hess, A.R.; Wheaton, W.W.; Nickoloff, B.J.; Topczewski, J.; Hendrix, M.J. Embryonic and tumorigenic pathways converge via Nodal signaling: role in melanoma aggressiveness. Nat. Med. 2006, 12, 925–932.
10. Postovit, L.M.; Margaryan, N.V.; Seftor, E.A.; Hendrix, M.J. Role of nodal signaling and the microenvironment underlying melanoma plasticity. Pigment Cell Melanoma Res. 2008, 21, 348–357.
11. Strizzi, L.; Hardy, K.M.; Kirsammer, G.T.; Gerami, P.; Hendrix, M.J. Embryonic signaling in melanoma: Potential for diagnosis and therapy. Lab Investig. 2011, 91, 819–824.
12. Seftor, E.A.; Seftor, R.E.; Weldon, D.S.; Kirsammer, G.T.; Margaryan, N.V.; Gilgur, A.; Hendrix, M.J. Melanoma tumor cell heterogeneity: A molecular approach to study subpopulations expressing the embryonic morphogen nodal. Semin. Oncol. 2014, 41, 259–266.
13. Hardy, K.M.; Strizzi, L.; Margaryan, N.V.; Gupta, K.; Murphy, G.F.; Scolyer, R.A.; Hendrix, M.J. Targeting nodal in conjunction with dacarbazine induces synergistic anticancer effects in metastatic melanoma. Mol. Cancer Res. 2015, 13, 670–680.
14. Postovit, L.M.; Margaryan, N.V.; Seftor, E.A.; Kirschmann, D.A.; Lipavsky, A.; Wheaton, W.W.; Abbott, D.E.; Seftor, R.E.; Hendrix, M.J. Human embryonic stem cell microenvironment suppresses the tumorigenic phenotype of aggressive cancer cells. Proc. Natl. Acad. Sci. USA 2008, 105, 4329–4334.
15. Costa, F.F.; Seftor, E.A.; Bischof, J.M.; Kirschmann, D.A.; Strizzi, L.; Arndt, K.; Bonaldo Mde, F.; Soares, M.B.; Hendrix, M.J. Epigenetically reprogramming metastatic tumor cells with an embryonic microenvironment. Epigenomics 2009, 1, 387–398.
16. Strizzi, L.; Hardy, K.M.; Seftor, E.A.; Costa, F.F.; Kirschmann, D.A.; Seftor, R.E.B.; Postovit, L.-M.; Hendrix, M.J. Development and cancer: at the crossroads of Nodal and Notch signaling. Cancer Res. 2009, 69, 7131–7134.
17. Hardy, K.M.; Kirschmann, D.A.; Seftor, E.A.; Margaryan, N.V.; Postovit, L.M.; Strizzi, L.; Hendrix, M.J. Regulation of the embryonic morphogen Nodal by Notch4 facilitates manifestation of the aggressive melanoma phenotype. Cancer Res. 2010, 70, 10340–10350.
18. Bianco, C.; Adkins, H.B.; Wechselberger, C.; Seno, M.; Normanno, N.; de Luca, A.; Sun, Y.; Khan, N.; Kenney, N.; Ebert, A.; at al. Cripto-1 activates nodal- and ALK4–dependent and -independent signaling pathways in mammary epithelial Cells. Mol. Cell. Biol. 2002, 22, 2586–2597.
19. Reissmann, E.; Jörnvall, H.; Blokzijl, A.; Andersson, O.; Chang, C.; Minchiotti, G.; Persico, M.G.; Ibáñez, C.F.; Brivanlou, A.H. The orphan receptor ALK7 and the Activin receptor ALK4 mediate signaling by Nodal proteins during vertebrate development. Genes Dev. 2001, 15, 2010–2022.
20. Calvanese, L.; Sandomenico, A.; Caporale, A.; Focà, A.; Focà, G.; D’Auria, G.; Falcigno, L.; Ruvo, M. Conformational features and binding affinities to Cripto, ALK7 and ALK4 of Nodal synthetic fragments. J. Pept. Sci. 2015, 21, 283–293.
21. Aykul, S.; Ni, W.; Mutatu, W.; Martinez-Hackert, E. Human Cerberus prevents nodal-receptor binding, inhibits nodal signaling, and suppresses nodal-mediated phenotypes. PLoS ONE 2015, 10, e0114954.
22. De Luca, A.; Lamura, L.; Strizz, L.; Roma, C.; D’Antonio, A.; Margaryan, N.; Pirozzi, G.; Hsu, M.Y.; Botti, G.; Mari E. et al. Expression and functional role of CRIPTO-1 in cutaneous melanoma. Br. J. Cancer 2011, 105, 1030–1038.
23. Strizzi, L.; Margaryan, N.V.; Gilgur, A.; Hardy, K.M.; Normanno, N.; Salomon, D.S.; Hendrix, M.J. The significance of a Cripto-1 positive subpopulation of human melanoma cells exhibiting stem cell-like characteristics. Cell Cycle 2013, 12, 1450–1456.
24. Quail, D.F.; Zhang, G.; Findlay, S.D.; Hess, D.A.; Postovit, L.M. Nodal promotes invasive phenotypes via a mitogen-activated protein kinase-dependent pathway. Oncogene 2014, 33, 461–473.
25. Kirsammer, G.; Strizzi, L.; Margaryan, N.V.; Gilgur, A.; Hyser, M.; Atkinson, J.; Kirschmann, D.A.; Seftor, E.A.; Hendrix, M.J. Nodal signaling promotes a tumorigenic phenotype in human breast cancer. Semin. Cancer Biol. 2014, 29, 40–50.
26. Karimkhani, C.; Gonzalez, R.; Dellavalle, R.P. A review of novel therapies for melanoma. Am. J. Clin. Dermatol. 2014, 15, 323–337.
27. Hao, M.; Song, F.; Du, X.; Wang, G.; Yang, Y.; Chen, K.; Yang, J. Advances in targeted therapy for unresectable melanoma: New drugs and combinations. Cancer Lett. 2015, 359, 1–8.
28. Spagnolo, F.; Ghiorzo, P.; Orgiano, L.; Pastorino, L.; Picasso, V.; Tornari, E.; Ottaviano, V.; Queirolo, P. BRAF-mutant melanoma: treatment approaches, resistance mechanisms, and diagnostic strategies. Onco Targets Ther. 2015, 8, 157–168.
29. Eggermont, A.M.; Kirkwood, J.M. Re-evaluating the role of dacarbazine in metastatic melanoma: What have we learned in 30 years? Eur. J. Cancer 2004, 12, 1825–1836.
30. Sullivan, R.J.; Flaherty, K.T. Resistance to BRAF-targeted therapy in melanoma. Eur. J. Cancer 2013, 49, 1297–1304.
31. Calvanese, L.; Marasco, D.; Doti, N.; Saporito, A.; D’Auria, G.; Paolillo, L.; Ruvo, M.; Falcigno, L. Structural investigations on the Nodal-Cripto binding: A theoretical and experimental approach. Biopolymers 2010, 93, 1011–1021.
32. Strizzi, L.; Sandomenico, A.; Margayan, N.V.; Focà, A.; Sanguigno, L.; Bodenstine, T.M.; Chandler, G.S.; Reed, D.; Seftor, E.A.; Seftor, R.E.B. et al. Effect of a novel Nodal-targeting monoclonal antibody in cancer. Oncotarget 2015, in press.
33. Saporito, A. Chemical Synthesis of Proteins for BIotechnology Applications. Ph.D. Thesis, Univerisity of Naples “Federico II”, Naples, Italy, 2005.
34. De Caestecker, M. The transforming growth factor-beta superfamily of receptors. Cytokine Growth Factor Rev. 2004, 15, 1–11.
35. Wilson, D.S.; Wu, J.; Peluso, P.; Nock, S. Improved method for pepsinolysis of mouse IgG(1) molecules to F(ab')(2) fragments. J. Immunol. Methods 2002, 260, 29–36.
36. Yamaguchi, Y.; Kim, H.; Kato, K.; Masuda, K.; Shimada, I.; Arata, Y. Proteolytic fragmentation with high specificity of mouse immunoglobulin G. Mapping of proteolytic cleavage sites in the hinge region. J. Immunol. Methods 1995, 181, 259–267.
37. Sondermann, P.; Huber, R.; Oosthuizen, V.; Jacob, U. The 3.2-A crystal structure of the human IgG1 Fc fragment-Fc gamma RIII complex. Nature 2000, 406, 267–273.
38. Fields, G.B.; Noble, R.L. Solid phase peptide synthesis utilizing 9 fluorenylmethoxycarbonyl amino acids. Int. J. Pept. Protein Res. 1990, 35, 161–214.
39. Carter, J.M. Techniques for conjugation of synthetic peptides to carrier molecules. Methods Mol. Biol. 1994, 36, 155–191.
40. Bradford, M.M. Rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem. 1976, 72, 248–254.
41. Kohler, G.; Milstein, C. Derivation of specific antibody-producing tissue culture and tumor lines by cell fusion. Eur. J. Immunol. 1976, 6, 511–519.
42. Johnsson, B.; Lofas, S.; Lindquist, G. Immobilization of proteins to a carboxymethyldextran-modified gold surface for biospecific interaction analysis in surface plasmon resonance sensors. Anal. Biochem. 1991, 198, 268–277.
43. Malchenko, S.; Galat, V.; Seftor, E.A.; Vanin, E.F.; Costa, F.F.; Seftor, R.E.; Soares, M.B.; Hendrix, M.J. Cancer hallmarks in induced pluripotent cells: New insights. J. Cell. Physiol. 2010, 225, 390–393.