A phase I clinical trial of systemically delivered NEMO binding domain peptide in dogs with spontaneous activated B-cell like diffuse large B-cell lymphoma

PLoS ONE

Volumn 9, Issue 5, 2014, Pages

  Habineza Ndikuyeze, Georges ^a   Gaurnier Hausser, Anita ^b   Patel, Reema ^c   Baldwin, Albert S ^d,e   May, Michael J ^a   Flood, Patrick ^f   Krick, Erika ^a   Propert, Kathleen J ^g   Mason, Nicola J ^a  

^a UNIVERSITY OF PENNSYLVANIA   (United States)

^b DREXEL UNIVERSITY COLLEGE OF MEDICINE   (United States)

^c ANTECH DIAGNOSTICS   (United States)

^d Theralogics Inc   (United States)

^e UNIVERSITY OF NORTH CAROLINA SCHOOL OF MEDICINE   (United States)

^f UNIVERSITY OF ALBERTA   (Canada)

^g UNIVERSITY OF PENNSYLVANIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CYCLIN D; I KAPPA B KINASE GAMMA; ANTINEOPLASTIC AGENT; I KAPPA B KINASE; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; PEPTIDE;

ANIMAL TISSUE; ANTIPROLIFERATIVE ACTIVITY; APOPTOSIS; ARTICLE; CONTROLLED STUDY; DOG; DRUG DISTRIBUTION; DRUG DOSE ESCALATION; DRUG EFFICACY; DRUG SAFETY; DRUG UPTAKE; FEASIBILITY STUDY; HISTOPATHOLOGY; HUMAN; HUMAN CELL; IN VIVO STUDY; LARGE CELL LYMPHOMA; LIVER DISEASE; LYMPH NODE BIOPSY; MITOSIS INDEX; NONHUMAN; PHASE 1 CLINICAL TRIAL; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION; ANIMAL; B LYMPHOCYTE; DOG DISEASES; DRUG EFFECTS; LYMPHOMA, LARGE B-CELL, DIFFUSE; METABOLISM; PATHOLOGY; PROTEIN TERTIARY STRUCTURE; SENTINEL LYMPH NODE BIOPSY; VETERINARY;

ANIMALS; ANTINEOPLASTIC AGENTS; B-LYMPHOCYTES; DOG DISEASES; DOGS; HUMANS; I-KAPPA B KINASE; LYMPHOMA, LARGE B-CELL, DIFFUSE; NF-KAPPA B; PEPTIDES; PROTEIN STRUCTURE, TERTIARY; SENTINEL LYMPH NODE BIOPSY; SIGNAL TRANSDUCTION;

EID: 84900420238     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0095404     Document Type: Article

References (47)

1. Lenz G, Davis RE, Ngo VN, Lam L, George TC, et al (2008) Oncogenic CARD11 mutations in human diffuse large B cell lymphoma. Science 319:1676-9. (Pubitemid 351432507)
2. Alizadeh AA, Eisen MB, Davis RE, Ma C, Lossos IS, et al (2000) Distinct types of diffuse large B-cell lymphoma identified by gene expression profiling. Nature 403:503-11. (Pubitemid 30082188)
3. Rosenwald A, Wright G, Leroy K, Yu X, Gaulard P, et al (2003) Molecular diagnosis of primary mediastinal B cell lymphoma identifies a clinically favorable subgroup of diffuse large B cell lymphoma related to Hodgkin lymphoma. J Exp Med 198:851-62. (Pubitemid 37152922)
4. Bea S, Zettl A, Wright G, Salaverria I, Jehn P, et al (2005) Diffuse large B-cell lymphoma subgroups have distinct genetic profiles that influence tumor biology and improve gene-expression-based survival prediction. Blood 106:3183-90. (Pubitemid 41565917)
5. Davis RE, Brown KD, Siebenlist U, Staudt LM (2001) Constitutive nuclear factor kappaB activity is required for survival of activated B cell-like diffuse large B cell lymphoma cells. J Exp Med 194:1861-74. (Pubitemid 34028664)
6. Lam LT, Davis RE, Pierce J, Hepperle M, Xu Y, et al (2005) Small molecule inhibitors of IkappaB kinase are selectively toxic for subgroups of diffuse large B-cell lymphoma defined by gene expression profiling. Clin Cancer Res 11:28-40. (Pubitemid 40075775)
7. Hinz M, Loser P, Mathas S, Krappmann D, Dorken B, et al (2001) Constitutive NF-kappaB maintains high expression of a characteristic gene network, including CD40, CD86, and a set of antiapoptotic genes in Hodgkin/Reed-Sternberg cells. Blood 97:2798-807.
8. Li Q, Verma IM (2002) NF-kappaB regulation in the immune system. Nat Rev Immunol 2:725-34.
9. Staudt LM (2010) Oncogenic activation of NF-kappaB. Cold Spring Harb Perspect Biol. 2:a000109.
10. Ngo VN, Young RM, Schmitz R, Jhavar S, Xiao W, et al (2011) Oncogenically active MYD88 mutations in human lymphoma. Nature 470:115-9.
11. Liu F, Xia Y, Parker AS, Verma IM (2012) IKK biology. Immunol Rev 246:239-53.
12. Israel A. The IKK complex, a central regulator of NF-kappaB activation (2010) Cold Spring Harbor Perspect Biol 2:a000158.
13. May MJ, Marienfeld RB, Ghosh S (2002) Characterization of the Ikappa Bkinase NEMO binding domain. J Biol Chem 277:45992-6000. (Pubitemid 35417584)
14. Karin M, Yamamoto Y, Wang QM (2004) The IKK NF-kappa B system: a treasure trove for drug development. Nat Rev Drug Discov 3:17-26. (Pubitemid 38088695)
15. May MJ, D'Acquisto F, Madge LA, Glockner J, Pober JS, et al (2000) Selective inhibition of NF-kappaB activation by a peptide that blocks the interaction of NEMO with the IkappaB kinase complex. Science 289:1550-4.
16. Ethridge RT, Hashimoto K, Chung DH, Ehlers RA, Rajaraman S, et al (2002) Selective inhibition of NF-kappaB attenuates the severity of cerulein-induced acute pancreatitis. J Am Coll Surg 195:497-505.
17. di Meglio P, Ianaro A, Ghosh S (2005) Amelioration of acute inflammation by systemic administration of a cell-permeable peptide inhibitor of NF-kappaB activation. Arthritis Rheum 52:951-8. (Pubitemid 40365119)
18. Dasgupta S, Jana M, Zhou Y, Fung YK, Ghosh S, et al (2004) Antineuroinflammatory effect of NF-kappaB essential modifier-binding domain peptides in the adoptive transfer model of experimental allergic encephalomyelitis. J Immunol 173:1344-54. (Pubitemid 38924314)
19. Jimi E, Aoki K, Saito H, D9Acquisto F, May MJ, et al (2004) Selective inhibition of NF-kappa B blocks osteoclastogenesis and prevents inflammatory bone destruction in vivo. Nat Med 10:617-24. (Pubitemid 38796853)
20. Peterson JM, Kline W, Canan BD, Ricca DJ, Kaspar B, et al (2011) Peptide-based inhibition of NF-kappaB rescues diaphragm muscle contractile dysfunction in a murine model of Duchenne muscular dystrophy. Mol Med 17:508-15.
21. Ianaro A, Tersigni M, Belardo G, Di Martino S, Napolitano M, et al (2009) NEMO-binding domain peptide inhibits proliferation of human melanoma cells. Cancer Lett 274:331-6.
22. Kiessling MK, Klemke CD, Kaminski MM, Galani IE, Krammer PH, et al (2009) Inhibition of constitutively activated nuclear factor-kappaB induces reactive oxygen species- and iron-dependent cell death in cutaneous T-cell lymphoma. Cancer Res 69:2365-74.
23. Hayakawa Y, Maeda S, Nakagawa H, Hikiba Y, Shibata W, et al (2009) Effectiveness of IkappaB kinase inhibitors in murine colitis-associated tumorigenesis. J Gastroenterol 44:935-43.
24. Furuta H, Osawa K, Shin M, Ishikawa A, Matsuo K, et al (2012) Selective inhibition of NF-kappaB suppresses bone invasion by oral squamous cell carcinoma in vivo. Int J Cancer 131:E625-35.
25. Gaurnier-Hausser A, Patel R, Baldwin AS, May MJ, Mason NJ (2011) NEMO-binding domain peptide inhibits constitutive NF-kappaB activity and reduces tumor burden in a canine model of relapsed, refractory diffuse large B-cell lymphoma. Clin Cancer Res 17:4661-71.
26. Al-Katib A, Arnold AA, Aboukameel A, Sosin A, Smith P, et al (2010) I-kappa-kinase-2 (IKK-2) inhibition potentiates vincristine cytotoxicity in non-Hodgkin's lymphoma. Mol Cancer 9:228.
27. Breen M, Modiano JF (2008) Evolutionarily conserved cytogenetic changes in hematological malignancies of dogs and humans-man and his best friend share more than companionship Chromosome Res 16:145-54. (Pubitemid 351294788)
28. Mudaliar MA, Haggart RD, Miele G, Sellar G, Tan KA, et al (2013) Comparative gene expression profiling identifies common molecular signatures of NF-kappaB activation in canine and human diffuse large B cell lymphoma (DLBCL). PLoS One 8:e72591.
29. Richards KL, Motsinger-Reif AA, Chen HW, Fedoriw Y, Fan C, et al (2013) Gene profiling of canine B-cell lymphoma reveals germinal center and postgerminal center subtypes with different survival times, modeling human DLBCL. Cancer Res 73:5029-39.
30. Honigberg LA, Smith AM, Sirisawad M, Verner E, Loury D, et al (2010) The Bruton tyrosine kinase inhibitor PCI-32765 blocks B-cell activation and is efficacious in models of autoimmune disease and B-cell malignancy. Proc Natl Acad Sci U S A 107:13075-80.
31. Vail DM, Thamm DH, Reiser H, Ray AS, Wolfgang GH, et al (2009) Assessment of GS-9219 in a pet dog model of non-Hodgkin's lymphoma. Clinical cancer research: an official journal of the American Association for Cancer Res 15:3503-10.
32. Vail DM, Michels GM, Khanna C, Selting KA, London CA (2010) Response evaluation criteria for peripheral nodal lymphoma in dogs (v1.0)-a Veterinary Cooperative Oncology Group (VCOG) consensus document. Vet Comp Oncol 8:28-37.
33. Veterinary cooperative oncology group (2011) common terminology criteria for adverse events (VCOG-CTCAE) following chemotherapy or biological antineoplastic therapy in dogs and cats v1.1. Vet Comp Oncol.
34. Schneider CA, Rasband WS, Eliceiri KW (2012) "NIH Image to ImageJ: 25 years of image analysis". Nat Methods 9:671-5.
35. Spee B, Arends B, van den Ingh TS, Penning LC, Rothuizen J (2006) Copper metabolism and oxidative stress in chronic inflammatory and cholestatic liver diseases in dogs. J Vet Intern Med 20:1085-92. (Pubitemid 44621036)
36. von Bismarck P, Winoto-Morbach S, Herzberg M, Uhlig U, Schutze S, et al (2012) IKK NBD peptide inhibits LPS induced pulmonary inflammation and alters sphingolipid metabolism in a murine model. Pulm Pharmacol Ther 25:228-35.
37. Gamble C, McIntosh K, Scott R, Ho KH, Plevin R, et al (2012) Inhibitory kappa B Kinases as targets for pharmacological regulation. Br J Pharmacol 165:802-19.
38. Lam LT, Davis RE, Ngo VN, Lenz G, Wright G, et al (2008) Compensatory IKKalpha activation of classical NF-kappaB signaling during IKKbeta inhibition identified by an RNA interference sensitization screen. Proc Natl Acad Sci U S A. 105:20798-803.
39. Pham LV, Fu L, Tamayo AT, Bueso-Ramos C, Drakos E, et al (2011) Constitutive BR3 receptor signaling in diffuse, large B-cell lymphomas stabilizes nuclear factor-kappaB-inducing kinase while activating both canonical and alternative nuclear factor-kappaB pathways. Blood 117:200-10.
40. Ankermann T, Reisner A, Wiemann T, Krams M, Kohler H, et al (2005) Topical inhibition of nuclear factor-kappaB enhances reduction in lung edema by surfactant in a piglet model of airway lavage. Crit Care Med 33:1384-91. (Pubitemid 40827394)
41. Dai S, Hirayama T, Abbas S, Abu-Amer Y (2004) The IkappaB kinase (IKK) inhibitor, NEMO-binding domain peptide, blocks osteoclastogenesis and bone erosion in inflammatory arthritis. J Biol Chem 279:37219-22. (Pubitemid 39195425)
42. De Plaen IG, Liu SX, Tian R, Neequaye I, May MJ, et al (2007) Inhibition of nuclear factor-kappaB ameliorates bowel injury and prolongs survival in a neonatal rat model of necrotizing enterocolitis. Pediatr Res 61:716-21. (Pubitemid 46800282)
43. Ghosh A, Roy A, Liu X, Kordower JH, Mufson EJ, et al (2007) Selective inhibition of NF-kappaB activation prevents dopaminergic neuronal loss in a mouse model of Parkinson's disease. Proc Natl Acad Sci U S A. 104:18754-9. (Pubitemid 350210769)
44. Nadjar A, Bluthe RM, May MJ, Dantzer R, Parnet P (2005) Inactivation of the cerebral NFkappaB pathway inhibits interleukin-1beta-induced sickness behavior and c-Fos expression in various brain nuclei. Neuropsychopharmacology 30:1492-9. (Pubitemid 41153121)
45. Cardozo AK, Buchillier V, Mathieu M, Chen J, Ortis F, et al (2007) Cell-permeable peptides induce dose- and length-dependent cytotoxic effects. Biochim Biophys Acta 1768:2222-34. (Pubitemid 47379621)
46. Jones SW, Christison R, Bundell K, Voyce CJ, Brockbank SM, et al (2005) Characterisation of cell-penetrating peptide-mediated peptide delivery. Br J Pharmacol 145:1093-102. (Pubitemid 43079982)
47. Lam LT, Wright G, Davis RE, Lenz G, Farinha P, et al (2008) Cooperative signaling through the signal transducer and activator of transcription 3 and nuclear factor-kB pathways in subtypes of diffuse large B-cell lymphoma. Blood 111:3701-13.