Generation and preclinical characterization of an antibody specific for SEMA4D

mAbs

Volumn 8, Issue 1, 2016, Pages 150-162

  Fisher, Terrence L ^a   Reilly, Christine A ^a   Winter, Laurie A ^a   Pandina, Tracy ^a   Jonason, Alan ^a   Scrivens, Maria ^a   Balch, Leslie ^a   Bussler, Holm ^a   Torno, Sebold ^a   Seils, Jennifer ^a   Mueller, Loretta ^a   Huang, He ^a   Klimatcheva, Ekaterina ^a   Howell, Alan ^a   Kirk, Renee ^a   Evans, Elizabeth ^a   Paris, Mark ^a   Leonard, John E ^a   Smith, Ernest S ^a   Zauderer, Maurice ^a  

^a VACCINEX INC   (United States)

Author keywords

Arthritis; CD100; Humanized monoclonal antibody; Mab 67 2; SEMA4D; Semaphorin; VX15 2503

Indexed keywords

COLLAGEN; ETANERCEPT; FREUND ADJUVANT; HUMAN MONOCLONAL ANTIBODY; SEMAPHORIN; SEMAPHORIN 4D; TGN1412; UNCLASSIFIED DRUG; VX15 2503; CD100 ANTIGEN; LEUKOCYTE ANTIGEN; MONOCLONAL ANTIBODY; NEUTRALIZING ANTIBODY;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTHRITIS; ARTICLE; AUTOIMMUNE DISEASE; BONE INJURY; CHO CELL LINE; CONTROLLED STUDY; CYTOKINE RELEASE; ENZYME LINKED IMMUNOSORBENT ASSAY; EPITOPE MAPPING; FLOW CYTOMETRY; HUMAN; HUMAN CELL; HUNTINGTON DISEASE LIKE SYNDROME; IMMUNOFLUORESCENCE; IMMUNOHISTOCHEMISTRY; INTERNALIZATION; MOUSE; MULTIPLE SCLEROSIS; NEOPLASM; NEUROLOGIC DISEASE; NONHUMAN; RECEPTOR BLOCKING; RHEUMATOID ARTHRITIS; SURFACE PLASMON RESONANCE; ANIMAL; ANTAGONISTS AND INHIBITORS; ANTIBODY SPECIFICITY; IMMUNOLOGY; KNOCKOUT MOUSE;

ANIMALS; ANTIBODIES, MONOCLONAL, MURINE-DERIVED; ANTIBODIES, NEUTRALIZING; ANTIBODY SPECIFICITY; ANTIGENS, CD; HUMANS; MICE; MICE, KNOCKOUT; SEMAPHORINS;

EID: 84964490224     PISSN: 19420862     EISSN: 19420870     Source Type: Journal    
DOI: 10.1080/19420862.2015.1102813     Document Type: Article

References (47)

1. Giger RJ, Hollis ER, Tuszynski MH. Guidance molecules in axon regeneration. Cold Spring Harb Perspect Biol 2010 Jul; 2:a001867; PMID: 20519341
2. Ch'ng ES, Kumanogoh A. Roles of Sema4D and Plexin-B1 in tumor progression. Mol Cancer 2010; 9:251; PMID:20858260; http://dx.doi.org/10.1186/1476-4598-9-251
3. Nkyimbeng-Takwi E, Chapoval SP. Biology and function of neuroimmune semaphorins 4A and 4D. Immunol Res 2011 Jan 4; 50:10-21; PMID: 21203905; http://dx.doi.org/10.1007/s12026-010-8201-y
4. Zhang Y, Liu B, Ma Y, Jin B. Sema 4D/CD100-plexin B is a multifunctional counter-receptor. Cell Mol Immunol 2012 Dec 24; 10:97-8; PMID: 23262975; http://dx.doi.org/10.1038/cmi.2012.65
5. Suzuki K, Kumanogoh A, Kikutani H. Semaphorins and their receptors in immune cell interactions. Nat Immunol 2008 Jan; 9:17-23; PMID: 18087252; http://dx.doi.org/10.1038/ni1553
6. Hall KT, Boumsell L, Schultze JL, Boussiotis VA, Dorfman DM, Cardoso AA, Bensussan A, Nadler LM, Freeman GJ. Human CD100, a novel leukocyte semaphorin that promotes B-cell aggregation and differentiation. Proc Natl Acad Sci U.S.A 1996 Oct 15; 93:11780-5; PMID: 8876214; http://dx.doi.org/10.1073/pnas.93.21.11780
7. Takamatsu H, Okuno T, Kumanogoh A. Regulation of immune cell responses by semaphorins and their receptors. Cell Mol Immunol 2010 Mar; 7:83-8; PMID: 20118971; http://dx.doi.org/10.1038/cmi.2009.111
8. Zhu L, Bergmeier W, Wu J, Jiang H, Stalker TJ, Cieslak M, Fan R, Boumsell L, Kumanogoh A, Kikutani H, et al. Regulated surface expression and shedding support a dual role for semaphorin 4D in platelet responses to vascular injury. Proc Natl Acad Sci U.S.A 2007 Jan 23; 104:1621-6; http://dx.doi.org/10.1073/pnas.0606344104
9. Moreau-Fauvarque C, Kumanogoh A, Camand E, Jaillard C, Barbin G, Boquet I, Love C, Jones EY, Kikutani H, Lubetzki C, et al. The transmembrane semaphorin Sema4D/CD100, an inhibitor of axonal growth, is expressed on oligodendrocytes and upregulated after CNS lesion. J Neurosci 2003 Oct 8; 23:9229-39
10. Smith ES, Jonason AJ, Reilly C, Veeraraghavan J, Fisher T, Doherty M, Klimatcheva E, Mallow C, Cornelius C, Leonard JE, et al. SEMA4D compromises blood-brain barrier, activates microglia, and inhibits remyelination in neurodegenerative disease. Neurobiol Dis 2014; 73:254-68; http://dx.doi.org/10.1016/j. nbd.2014.10.008
11. Tamagnone L, Artigiani S, Chen H, He Z, Ming GI, Song H, Chedotal A, Winberg ML, Goodman CS, Poo M, et al. Plexins are a large family of receptors for transmembrane, secreted, and GPI-anchored semaphorins in vertebrates. Cell 1999 Oct 1; 99:71-80; PMID: 10520995; http://dx.doi.org/10.1016/S0092-8674(00)80063-X
12. Giordano S, Corso S, Conrotto P, Artigiani S, Gilestro G, Barberis D, Tamagnone L, Comoglio PM. The semaphorin 4D receptor controls invasive growth by coupling with Met. Nat Cell Biol 2002 Sep; 4:720-4; PMID: 12198496; http://dx.doi.org/10.1038/ncb843
13. Giraudon P, Vincent P, Vuaillat C, Verlaeten O, Cartier L, Marie-Cardine A, Mutin M, Bensussan A, Belin MF, Boumsell L. Semaphorin CD100 from activated T lymphocytes induces process extension collapse in oligodendrocytes and death of immature neural cells. J Immunol 2004 Jan 15; 172:1246-55; http://dx.doi. org/10.4049/jimmunol.172.2.1246
14. Witherden DA, Watanabe M, Garijo O, Rieder SE, Sarkisyan G, Cronin SJ, Verdino P, Wilson IA, Kumanogoh A, Kikutani H, et al. The CD100 receptor interacts with Its plexin B2 ligand to regulate epidermal gammadelta T cell function. Immunity. 2012 Aug 14; 37:314-25; http://dx.doi.org/10.1016/j.immuni.2012. 05.026
15. Kumanogoh A, Watanabe C, Lee I, Wang X, ShiW, Araki H, Hirata H, Iwahori K, Uchida J, Yasui T, et al. Identification of CD72 as a lymphocyte receptor for the class IV semaphorin CD100: a novel mechanism for regulating B cell signaling. Immunity. 2000 Nov; 13:621-31; http://dx.doi. org/10.1016/S1074-7613(00)00062-5
16. Kumanogoh A, Kikutani H. The CD100-CD72 interaction: a novel mechanism of immune regulation. Trends Immunol. 2001 Dec; 22:670-6; PMID: 11738997; http://dx.doi.org/10.1016/S1471-4906(01)02087-7
17. Ishida I, Kumanogoh A, Suzuki K, Akahani S, Noda K, Kikutani H. Involvement of CD100, a lymphocyte semaphorin, in the activation of the human immune system via CD72: implications for the regulation of immune and inflammatory responses. Int Immunol 2003 Aug; 15:1027-34; PMID: 12882840; http://dx. doi.org/10.1093/intimm/dxg098
18. Delaire S, Billard C, Tordjman R, Chedotal A, Elhabazi A, Bensussan A, Boumsell L. Biological activity of soluble CD100. II. Soluble CD100, similarly to HSemaIII, inhibits immune cell migration. J Immunol 2001 Apr 1; 166:4348-54; PMID: 11254688; http://dx.doi.org/10.4049/jimmunol.166.7.4348
19. Elhabazi A, Delaire S, Bensussan A, Boumsell L, Bismuth G. Biological activity of soluble CD100. I. The extracellular region of CD100 is released from the surface of T lymphocytes by regulated proteolysis. J Immunol 2001 Apr 1; 166:4341-7; http://dx.doi.org/10.4049/jimmunol.166.7.4341
20. Shi W, Kumanogoh A, Watanabe C, Uchida J, Wang X, Yasui T, Yukawa K, Ikawa M, Okabe M, Parnes JR, et al. The class IV semaphorin CD100 plays nonredundant roles in the immune system: defective B and T cell activation in CD100-deficient mice. Immunity. 2000 Nov; 13:633-42; http://dx.doi.org/10.1016/S1074-7613(00)00063-7
21. Leonard JE, Fisher TL, Winter LA, Cornelius CA, Reilly C, Smith ES, Zauderer M. Nonclinical safety evaluation of VX15/2503, a humanized IgG4 anti-SEMA4D antibody. Mol Cancer Ther 2015 Apr; 14:964-72; PMID: 25657333; http://dx.doi.org/10.1158/1535-7163.MCT-14-0924
22. Takamatsu H, Takegahara N, Nakagawa Y, Tomura M, Taniguchi M, Friedel RH, Rayburn H, Tessier-Lavigne M, Yoshida Y, Okuno T, et al. Semaphorins guide the entry of dendritic cells into the lymphatics by activating myosin II. Nat Immunol 2010 May 30; 11:594-600; PMID: 20512151; http://dx.doi.org/10.1038/ni.1885
23. Basile JR, Castilho RM, Williams VP, Gutkind JS. Semaphorin 4D provides a link between axon guidance processes and tumor-induced angiogenesis. Proc Natl Acad Sci U.S.A 2006 Jun 13; 103:9017-22; PMID: 16754882; http://dx.doi.org/10.1073/pnas.0508825103
24. Campos M, DE Campos SG, Ribeiro GG, Eguchi FC, Silva SR, DE Oliveira CZ, DA Costa AM, Curcelli EC, Nunes MC, Penna V, et al. Ki-67 and CD100 immunohistochemical expression is associated with local recurrence and poor prognosis in soft tissue sarcomas, respectively. Oncol Lett 2013 May; 5:1527-35
25. Sun Q, Zhou H, Binmadi NO, Basile JR. Hypoxia inducible factor-1-mediated regulation of Semaphorin 4D affects tumor growth and vascularity. J Biol Chem 2009 Sep 17; 284:32066-74; PMID: 19762474; http://dx.doi.org/10.1074/jbc.M109.057166
26. Evans EE, Jonason AS, Jr., Bussler H, Torno S, Veeraraghavan J, Reilly C, Doherty MA, Seils J, Winter LA, Mallow C, et al. Antibody blockade of semaphorin 4D promotes immune infiltration into tumor and enhances response to other immunomodulatory therapies. Cancer Immunol Res 2015 Jan 22; 3:689-701; PMID: 25614511; http://dx.doi.org/10.1158/2326-6066. CIR-14-0171
27. Kumanogoh A, Suzuki K, Ch'ng E, Watanabe C, Marukawa S, Takegahara N, Ishida I, Sato T, Habu S, Yoshida K, et al. Requirement for the lymphocyte semaphorin, CD100, in the induction of antigen-specific T cells and the maturation of dendritic cells. J Immunol 2002 Aug 1; 169:1175-81; PMID: 12133937; http://dx.doi.org/10.4049/jimmunol.169.3.1175
28. Okuno T, Nakatsuji Y, Moriya M, TakamatsuH, Nojima S, Takegahara N, Toyofuku T, Nakagawa Y, Kang S, Friedel RH, et al. Roles of sema4D-plexin-B1 interactions in the central nervous system for pathogenesis of experimental autoimmune encephalomyelitis. J Immunol 2010 Feb 1; 184:1499-506; PMID: 20038643; http://dx.doi. org/10.4049/jimmunol.0903302
29. Yang YH, Zhou H, Binmadi NO, Proia P, Basile JR. Plexin-B1 activates NF-kappaB and IL-8 to promote a pro-angiogenic response in endothelial cells. PLoS ONE 2011; 6:e25826; PMID:22028792; http://dx. doi.org/10.1371/journal.pone.0025826
30. Labrijn AF, Aalberse RC, Schuurman J. When binding is enough: nonactivating antibody formats. Curr Opin Immunol 2008 Aug; 20:479-85; http://dx.doi.org/10.1016/j.coi.2008.05.010
31. Labrijn AF, Buijsse AO, van den Bremer ET, Verwilligen AY, Bleeker WK, Thorpe SJ, Killestein J, Polman CH, Aalberse RC, Schuurman J, et al. Therapeutic IgG4 antibodies engage in Fab-arm exchange with endogenous human IgG4 in vivo. Nat Biotechnol 2009 Aug; 27:767-71; http://dx.doi.org/10.1038/nbt.1553
32. Suntharalingam G, Perry MR, Ward S, Brett SJ, Castello-Cortes A, Brunner MD, Panoskaltsis N. Cytokine storm in a phase 1 trial of the anti-CD28 monoclonal antibody TGN1412. N Engl J Med 2006 Sep 7; 355:1018-28; http://dx.doi.org/10.1056/NEJMoa063842
33. Romer PS, Berr S, Avota E, Na SY, Battaglia M, Ten B, I, Einsele H, Hunig T. Preculture of PBMC at high cell density increases sensitivity of T-cell responses, revealing cytokine release by CD28 superagonist TGN1412. Blood 2011 Sep 19; 118:6772-82; PMID: 21931118; http://dx.doi.org/10.1182/blood-2010-12-319780
34. Love CA, Harlos K, Mavaddat N, Davis SJ, Stuart DI, Jones EY, Esnouf RM. The ligand-binding face of the semaphorins revealed by the high-resolution crystal structure of SEMA4D. Nat Struct Biol 2003 Oct; 10:843-8; http://dx.doi.org/10.1038/nsb977
35. Janssen BJ, Robinson RA, Perez-Branguli F, Bell CH, Mitchell KJ, Siebold C, Jones EY. Structural basis of semaphorin-plexin signalling. Nature 2010 Sep 26; 467:1118-22; PMID: 20877282; http://dx.doi.org/10.1038/nature09468
36. Vugmeyster Y, Xu X, Theil FP, Khawli LA, Leach MW. Pharmacokinetics and toxicology of therapeutic proteins: Advances and challenges. World J Biol Chem 2012 Apr 26; 3:73-92; PMID: 22558487; http://dx. doi.org/10.4331/wjbc.v3.i4.73
37. Beers SA, French RR, Chan HT, Lim SH, Jarrett TC, Vidal RM, Wijayaweera SS, Dixon SV, Kim H, Cox KL, et al. Antigenic modulation limits the efficacy of anti-CD20 antibodies: implications for antibody selection. Blood 2010 Jun 24; 115:5191-201; PMID: 20223920; http://dx.doi.org/10.1182/blood-2010-01-263533
38. Southwell AL, Franciosi S, Villanueva EB, Xie Y, Winter LA, Veeraraghavan J, Jonason A, Felczak B, Zhang W, Kovalik V, et al. Anti-semaphorin 4D immunotherapy ameliorates neuropathology and some cognitive impairment in the YAC128 mouse model of Huntington disease. Neurobiol Dis 2015 Feb 3; 76:46-56; http://dx.doi.org/10.1016/j.nbd.2015.01.002
39. Brown DM, Fisher TL, Wei C, Frelinger JG, Lord EM. Tumours can act as adjuvants for humoral immunity. Immunology 2001 Apr; 102:486-97; http://dx.doi.org/10.1046/j.1365-2567.2001.01213.x
40. Fisher TL, Nocera M, Willis RA, Turner MJ, Abdul Alim CS, Brown DM, Bourne PA, di Sant'Agnese PA, Messing EM, Lord EM, et al. Generation of monoclonal antibodies specific for human kallikrein 2 (hK2) using hK2-expressing tumors. Prostate 2002 May 15; 51:153-65; PMID: 11967950; http://dx.doi.org/10.1002/pros.10071
41. Lewis KB, Meengs B, Bondensgaard K, Chin L, Hughes SD, Kjaer B, Lund S, Wang L. Comparison of the ability of wild type and stabilized human IgG(4) to undergo Fab arm exchange with endogenous IgG(4)in vitro and in vivo. Mol Immunol 2009 Oct; 46:3488-94; PMID: 19683345; http://dx.doi.org/10.1016/j. molimm.2009.07.009
42. Timmerman P, Puijk WC, Meloen RH. Functional reconstruction and synthetic mimicry of a conformational epitope using CLIPS technology. J Mol Recognit 2007 Sep; 20:283-99; http://dx.doi.org/10.1002/jmr.846
43. Yoshida Y, Ogata A, Kang S, Ebina K, Shi K, Nojima S, Kimura T, Ito D, Morimoto K, Nishide M, et al. Semaphorin 4D contributes to rheumatoid arthritis by inducing inflammatory cytokine production: Pathogenic and therapeutic implications. Arthritis Rheumatol. 2015 Feb 23; 67:1481-90; PMID: 25707877; http://dx.doi.org/10.1002/art.39086
44. Takamatsu H, Kumanogoh A. Diverse roles for semaphorin-plexin signaling in the immune system. Trends Immunol. 2012 Mar; 33:127-35; http://dx.doi.org/10.1016/j.it.2012.01.008
45. Negishi-Koga T, Shinohara M, Komatsu N, Bito H, Kodama T, Friedel RH, Takayanagi H. Suppression of bone formation by osteoclastic expression of semaphorin 4D. Nat Med 2011 Oct 23; 17:1473-80; PMID: 22019888; http://dx.doi.org/10.1038/nm.2489
46. Okamoto K, Takayanagi H. Regulation of bone by the adaptive immune system in arthritis. Arthritis Res Ther 2011; 13:219; PMID:21635718; http://dx.doi.org/10.1186/ar3323
47. Heider KH, Kiefer K, Zenz T, Volden M, Stilgenbauer S, Ostermann E, Baum A, Lamche H, Kupcu Z, Jacobi A, et al. A novel Fc-engineered monoclonal antibody to CD37 with enhanced ADCC and high proapoptotic activity for treatment of B-cell malignancies. Blood 2011 Oct 13; 118:4159-68; PMID: 21795744; http://dx.doi.org/10.1182/blood-2011-04-351932