Phase i Clinical Pharmacology Study of F14512, a New Polyamine-Vectorized Anticancer Drug, in Naturally Occurring Canine Lymphoma

Clinical Cancer Research

Volumn 21, Issue 23, 2015, Pages 5314-5323

  Tierny, Dominique ^a   Serres, François ^a   Segaoula, Zacharie ^a,b,c   Bemelmans, Ingrid ^a   Bouchaert, Emmanuel ^a   Pétain, Aurélie ^d   Brel, Viviane ^d   Couffin, Stéphane ^d   Marchal, Thierry ^e   Nguyen, Laurent ^d   Thuru, Xavier ^b,c   Ferré, Pierre ^d   Guilbaud, Nicolas ^d   Gomes, Bruno ^d,f  

^a Oncovet   (France)

^b JEAN PIERRE AUBERT RESEARCH CENTER   (France)

^c UNIV LILLE   (France)

^d INSTITUT DE RECHERCHE PIERRE FABRE   (France)

^e VETAGRO SUP   (France)

^f ITeos Therapeutics   (Belgium)

Author keywords

[No Author keywords available]

Indexed keywords

ANTINEOPLASTIC AGENT; BIOLOGICAL MARKER; F14512; GYRASE INHIBITOR; HISTONE; PODOPHYLLOTOXIN;

ANALOGS AND DERIVATIVES; ANIMAL; CANCER STAGING; CLINICAL TRIAL; DOG; DOG DISEASES; FEMALE; HUMAN; LYMPHOMA; MALE; METABOLISM; PATHOLOGY; PHASE 1 CLINICAL TRIAL; PRECLINICAL STUDY; TREATMENT OUTCOME; TUMOR CELL LINE; VETERINARY;

ANIMALS; ANTINEOPLASTIC AGENTS; BIOMARKERS; CELL LINE, TUMOR; DOG DISEASES; DOGS; DRUG EVALUATION, PRECLINICAL; FEMALE; HISTONES; HUMANS; LYMPHOMA; MALE; NEOPLASM STAGING; PODOPHYLLOTOXIN; TOPOISOMERASE II INHIBITORS; TREATMENT OUTCOME;

EID: 84949438817     PISSN: 10780432     EISSN: 15573265     Source Type: Journal    
DOI: 10.1158/1078-0432.CCR-14-3174     Document Type: Article

References (50)

1. Siegel R, Naishadham D, Jemal A. Cancer statistics, 2013. CA Cancer J Clin 2013;63:11-30.
2. Younes A, Thieblemont C, Morschhauser F, Flinn I, Friedberg JW, Amorim S, et al. Combination of ibrutinib with rituximab, cyclophosphamide, doxorubicin, vincristine, and prednisone (R-CHOP) for treatment-naive patients with CD20-positive B-cell non-Hodgkin lymphoma: A non-randomised, phase 1b study. Lancet Oncol 2014;15:1019-26.
3. Casero RA Jr, Marton LJ. Targeting polyamine metabolism and function in cancer and other hyperproliferative diseases. Nat Rev Drug Discov 2007;6:373-90.
4. Barret JM, Kruczynski A, Visp-e S, Annereau JP, Brel V, Guminski Y, et al. F14512, a potent antitumor agent targeting topoisomerase II vectored into cancer cells via the polyamine transport system.Cancer Res 2008;68: 9845-53.
5. Annereau JP, Brel V, Dumontet C, Guminski Y, Imbert T, Broussas M, et al. A fluorescent biomarker of the polyamine transport system to select patients with AML for F14512 treatment. Leuk Res 2010;34: 1383-9.
6. Brel V, Annereau JP, Visp-e S, Kruczynski A, Bailly C, Guilbaud N. Cytotoxicity and cell death mechanisms induced by the polyamine-vectorized anti-cancer drug F14512 targeting topoisomerase II. Biochem Pharmacol 2011;82:1843-52.
7. Gentry AC, Pitts SL, Jablonsky MJ, Bailly C, Graves DE, Osheroff N. Interactions between the etoposide derivative F14512 and human type II topoisomerases: Implications for the C4 spermine moiety in promoting enzyme-mediated DNA cleavage. Biochemistry 2011;50:3240-9.
8. Kruczynski A, Vandenberghe I, Pillon A, Pesnel S,Goetsch L, Barret JM, et al. Preclinical activity of F14512, designed to target tumors expressing an active polyamine transport system. Invest New Drugs 2011;29:9-21.
9. Kruczynski A, Pillon A, Cr-eancier L, Vandenberghe I, Gomes B, Brel V, et al. F14512, a polyamine-vectorized anti-cancer drug, currently in clinical trials exhibits a marked preclinical anti-leukemic activity. Leukemia 2013;27: 2139-48.
10. Mouawad F, Gros A, Rysman B, Bal-Mahieu C, Bertheau C, Horn S, et al. The antitumor drug F14512 enhances cisplatin and ionizing radiation effects in head and neck squamous carcinoma cell lines. Oral Oncol 2014;50:113-9.
11. Leblond P, Boulet E, Bal-Mahieu C, Pillon A, Kruczynski A, Guilbaud N, et al. Activity of the polyamine-vectorized anti-cancer drug F14512 against pediatric glioma and neuroblastoma cell lines. Invest New Drugs 2014; 32:883-92.
12. De Botton S, Berthon C, Bulabois CE, Prebet T, Vey N, Chevallier P , et al. F14512 a novel polyamine-vectorized anti-cancer drug targeting topoisomerase II in adults patients with acute myeloid leukemia (AML): Results from a phase I study. EHA 17th Congress. 14-17 June 2012; Amsterdam.
13. Marconato L, Gelain ME, Comazzi S. The dog as a possible animal model for human non-Hodgkin lymphoma: A review. Hematol Oncol 2013;31: 1-9.
14. Ponce F, Marchal T, Magnol JP, Turinelli V, Ledieu D, Bonnefont C, et al. A morphological study of 608 cases of canine malignant lymphoma in France with a focus on comparative similarities between canine and human lymphoma morphology. Vet Pathol 2010;47:414-33.
15. Ranieri G, Gadaleta CD, Patruno R, Zizzo N, Daidone MG, Hansson MG, et al. A model of study for human cancer: Spontaneous occurring tumors in dogs. Biological features and translation for new anticancer therapies. Crit Rev Oncol Hematol 2013;88:187-97.
16. Richards KL, Motsinger-Reif AA, Chen HW, Fedoriw Y, Fan C, Nielsen DM, et al. Gene profiling of canine B-cell lymphoma reveals germinal center and postgerminal center subtypes with different survival times, modeling human DLBCL. Cancer Res 2013;73:5029-39.
17. Mudaliar MA, Haggart RD, Miele G, Sellar G, Tan KA, Goodlad JR, et al. Comparative gene expression profiling identifies common molecular signatures of NF-kB activation in canine and human diffuse large B-cell lymphoma (DLBCL). PLoS ONE 2013;8:e72591.
18. Marconato L, Frayssinet P, Rouquet N, Comazzi S, Leone VF, Laganga P, et al. Randomized, placebo-controlled, double-blinded chemoimmunotherapy clinical trial in a pet dog model of diffuse large B-cell lymphoma. Clin Cancer Res 2014;20:668-77.
19. Ito D, Frantz AM, Modiano JF. Canine lymphoma as a comparative model for human non-Hodgkin lymphoma: Recent progress and applications. Vet Immunol Immunopathol 2014;159:192-201.
20. Igwemezie LN, Kaul S, Barbhaiya RH. Assessment of toxicokinetics and toxicodynamics following intravenous administration of etoposide phosphate in beagle dogs. Pharm Res 1995;12:117-23.
21. Flory AB, Rassnick KM, Balkman CE, Kiselow MA, Autio K, Beaulieu BB, et al. Oral bioavailability of etoposide after administration of a single dose to tumor-bearing dogs. Am J Vet Res 2008;69:1316-22.
22. Lana S, U'ren L, Plaza S, Elmslie R, GustafsonD, Morley P, et al. Continuous low-dose oral chemotherapy for adjuvant therapy of splenic hemangiosarcoma in dogs. J Vet Intern Med 2007;21:764-9.
23. Willmann M, Müllauer L, Schwendenwein I, Wolfesberger B, Kleiter M, Pagitz M, et al. Chemotherapy in canine acute megakaryoblastic leukemia: A case report and review of the literature. In Vivo 2009;23:911-8.
24. Hohenhaus AE, Matus RE. Etoposide (VP-16). Retrospective analysis of treatment in 13 dogs with lymphoma. J Vet Intern Med 1990;4:239-41.
25. Fernandes NC, Guerra JM, R-essio RA, Wasques DG, Etlinger-Colonelli D, Lorente S, et al. Liquid-based cytology and cell block immunocytochemistry in veterinary medicine: Comparison with standard cytology for the evaluation of canine lymphoid samples. Vet Comp Oncol 2015 Feb 9. [Epub ahead of print].
26. Joetzke AE, Eberle N, Nolte I, Mischke R, Simon D. Flow cytometric evaluation of peripheral blood and bone marrow and fine-needle aspirate samples from multiple sites in dogs with multicentric lymphoma. AmJ Vet Res 2012;73:884-93.
27. Williams LE, Broussard MT, Johnson JL, Neel J. Comparison of results of clinicians' assessments, cytologic examination of fine-needle lymph node aspirates, and flow cytometry for determination of remission status of lymphoma in dogs. J Am Vet Med Assoc 2005;226:562-6.
28. Huang X, Darzynkiewicz Z. Cytometric assessment of histone H2AX phosphorylation: A reporter of DNA damage. Methods Mol Biol 2006; 314:73-80.
29. Valli VE, San Myint M, Barthel A, Bienzle D, Caswell J, Colbatzky F, et al. Classification of canine malignant lymphomas according to the World Health Organization criteria. Vet Pathol 2011;48:198-211.
30. Veterinary Co-operative OncologyGroup(VCOG). Veterinary Cooperative Oncology Group-Common Terminology Criteria for Adverse Events (VCOG-CTCAE) following chemotherapy or biological antineo-plastic therapy in dogs and cats v1.0. Vet Comp Oncol 2004;2:195-213.
31. Vail DM, Michels GM, Khanna C, Selting KA, London CA. Veterinary Cooperative Oncology Group. Response evaluation criteria for peripheral nodal lymphoma in dogs (v1.0)-a Veterinary Cooperative Oncology Group (VCOG) consensus document. Vet Comp Oncol 2010;8: 28-37.
32. Modiano JF, Breen M, Burnett RC, Parker HG, Inusah S, Thomas R, et al. Distinct B-cell and T-cell lymphoproliferative disease prevalence among dog breeds indicates heritable risk. Cancer Res 2005;65:5654-61.
33. Paoloni M, Khanna C. Translation of new cancer treatments from pet dogs to humans. Nat Rev Cancer 2008;8:147-56.
34. London CA, Hannah AL, Zadovoskaya R, Chien MB, Kollias-Baker C, Rosenberg M, et al. Phase I dose-escalating study of SU11654, a small molecule receptor tyrosine kinase inhibitor, in dogs with spontaneous malignancies. Clin Cancer Res 2003;9:2755-68.
35. Pryer NK, Lee LB, Zadovaskaya R, Yu X, Sukbuntherng J, Cherrington JM, et al. Proof of target for SU11654: Inhibition of KIT phosphorylation in canine mast cell tumors. Clin Cancer Res 2003;9:5729-34.
36. Richards KL, Suter SE. Man's best friend: What can pet dogs teach us about non-Hodgkin's lymphoma? Immunol Rev 2015;263:173-91.
37. Khanna C, Fan TM, Gorlick R, Helman LJ, Kleinerman ES, Adamson PC, et al. Toward a drug development path that targets metastatic progression in osteosarcoma. Clin Cancer Res 2014;20:4200-9.
38. Fenger JM, London CA, Kisseberth WC. Canine osteosarcoma: A naturally occurring disease to inform pediatric oncology. ILAR J 2014;55:69-85.
39. Milovancev M, Hauck M, Keller C, Stranahan LW,Mansoor A, Malarkey DE. Comparative pathology of canine soft tissue sarcomas: Possible models of human non-rhabdomyosarcoma soft tissue sarcomas. J Comp Pathol 2015;152:22-7.
40. Knapp DW, Ramos-Vara JA, Moore GE, Dhawan D, Bonney PL, Young KE. Urinary bladder cancer in dogs, a naturally occurring model for cancer biology and drug development. ILAR J 2014;55:100-18.
41. Liu D, Xiong H, Ellis AE, Northrup NC, RodriguezCOJr, O'Regan RM, et al. Molecular homology and difference between spontaneous canine mammary cancer and human breast cancer. Cancer Res 2014;74:5045-56.
42. Simon D, Moreno SN, Hirschberger J, Moritz A, Kohn B, Neuman S, et al. Efficacy of a continuous, multiagent chemotherapeutic protocol versus a short-term single-agent protocol in dogs with lymphoma. J Am Vet Med Assoc 2008;232:879-885.
43. Ito D, Brewer S, Modiano JF, Beall MJ. Development of a novel anti-canine CD20 monoclonal antibody with diagnostic and therapeutic potential. Leuk Lymphoma 2015;56:219-25.
44. Honigberg LA, Smith AM, Sirisawad M, Verner E, Loury D, Chang B, et al. 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 2010;107:13075-80.
45. Aalipour A, Advani RH. Bruton tyrosine kinase inhibitors: A promising novel targeted treatment for B-cell lymphomas. Br J Haematol 2013;163: 436-43.
46. Gardner HL, Harrington BK, Izumi R, Hamdy A, Kapstein A, Van Lith B, et al. ACP-196: A second generation Btk inhibitor demonstrates biologic activity in a canine model of B-cell non-Hodgkin lymphoma. AACR 2014 Annual Meeting. 5-9 April. 2014; San Diego. Poster #1744.
47. LeBlanc AK, Mauldin GE, Milner RJ, LaDue TA, Mauldin GN, Bartges JW. Efficacy and toxicity of BOPP and LOPP chemotherapy for the treatment of relapsed canine lymphoma. Vet Comp Oncol 2006;4:21-32.
48. Ma L, Pratt SE, Cao J, Dantzig AH, Moore RE, Slapak CA. Identification and characterization of the caninemultidrug resistance-associated protein. Mol Cancer Ther 2002;1:1335-42.
49. Matthaios D, Hountis P, Karakitsos P, Bouros D, Kakolyris S. H2AX a promising biomarker for lung cancer: A review. Cancer Invest 2013;31: 582-99.
50. De Botton S, Quesnel B, Audoly L, Bailly C, Brandely-Talbo M, Provendier O, et al. Tackling leukemia: Phase I study of F14512 in relapsed or refractory AML patients. 12th International Congress on Targeted Anticancer Therapies, 2014; Washington.