Harnessing high density lipoproteins to block transforming growth factor beta and to inhibit the growth of liver tumor metastases

PLoS ONE

Volumn 9, Issue 5, 2014, Pages

  Medina Echeverz, José ^a   Fioravanti, Jessica ^a   Diáz Valdés, Nancy ^a,b   Frank, Kathrin ^b,c   Aranda, Fernando ^a   Gomar, Celia ^a   Ardaiz, Nuria ^a   Dotor, Javier ^d   Umansky, Viktor ^b,c   Prieto, Jesús ^a,e   Berraondo, Pedro ^a  

^a UNIVERSITY OF NAVARRA   (Spain)

^b GERMAN CANCER RESEARCH CENTER DKFZ   (Germany)

^c UNIVERSITY OF HEIDELBERG   (Germany)

^d Digna Biotech   (Spain)

^e UNIVERSITY CLINIC OF NAVARRA   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

ANTINEOPLASTIC AGENT; APOLIPOPROTEIN A1 P144; GAMMA INTERFERON; GRANULOCYTE MACROPHAGE COLONY STIMULATING FACTOR; HIGH DENSITY LIPOPROTEIN; HYBRID PROTEIN; INTERLEUKIN 2; PARVOVIRUS VECTOR; TRANSFORMING GROWTH FACTOR BETA; UNCLASSIFIED DRUG; AKT1 PROTEIN, MOUSE; CD3 ANTIGEN; PROTEIN KINASE B; PROTEIN RET; RET PROTEIN, MOUSE; TGFB1 PROTEIN, MOUSE; TRANSFORMING GROWTH FACTOR BETA1;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANTINEOPLASTIC ACTIVITY; ARTICLE; CANCER INHIBITION; CD8+ T LYMPHOCYTE; COLORECTAL CANCER; CONTROLLED STUDY; CYTOKINE PRODUCTION; DISEASE ASSOCIATION; DOWN REGULATION; DRUG POTENCY; FEMALE; GENE TARGETING; IN VIVO STUDY; LIVER CELL; LIVER METASTASIS; LYMPHOCYTE COUNT; MELANOMA; MOUSE; NONHUMAN; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN MODIFICATION; PROTEIN PROTEIN INTERACTION; SIGNAL TRANSDUCTION; TRANSFORMING GROWTH FACTOR BETA GENE; UPREGULATION; VIRAL GENE DELIVERY SYSTEM; VIRAL GENE THERAPY; ANIMAL; ANTAGONISTS AND INHIBITORS; BAGG ALBINO MOUSE; C57BL MOUSE; COLORECTAL NEOPLASMS; GENE VECTOR; GENETICS; LIVER; LIVER NEOPLASMS; METABOLISM; MOLECULARLY TARGETED THERAPY; NEOPLASM METASTASIS; PATHOLOGY; PLASMID; TRANSGENIC MOUSE;

ANIMALS; ANTIGENS, CD3; COLORECTAL NEOPLASMS; FEMALE; GENETIC VECTORS; GRANULOCYTE-MACROPHAGE COLONY-STIMULATING FACTOR; HEPATOCYTES; INTERFERON-GAMMA; LIPOPROTEINS, HDL; LIVER; LIVER NEOPLASMS; MICE; MICE, INBRED BALB C; MICE, INBRED C57BL; MICE, TRANSGENIC; MOLECULAR TARGETED THERAPY; NEOPLASM METASTASIS; PLASMIDS; PROTO-ONCOGENE PROTEINS C-AKT; PROTO-ONCOGENE PROTEINS C-RET; TRANSFORMING GROWTH FACTOR BETA1;

EID: 84900395616     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0096799     Document Type: Article

References (35)

1. Flavell RA, Sanjabi S, Wrzesinski SH, Licona-Limon P (2010) The polarization of immune cells in the tumour environment by TGFbeta. Nature reviewsImmunology 10: 554-567.
2. Padua D, Massague J (2009) Roles of TGFbeta in metastasis. Cell Res 19: 89-102.
3. Thiery JP (2002) Epithelial-mesenchymal transitions in tumour progression. Nature Reviews Cancer 2: 442-454.
4. Pertovaara L, Kaipainen A, Mustonen T, Orpana A, Ferrara N, et al. (1994) Vascular endothelial growth factor is induced in response to transforming growth factor-beta in fibroblastic and epithelial cells. J Biol Chem 269: 6271-6274. (Pubitemid 24190991)
5. Chou YT, Wang H, Chen Y, Danielpour D, Yang YC (2006) Cited2 modulates TGF-beta-mediated upregulation of MMP9. Oncogene 25: 5547-5560. (Pubitemid 44344105)
6. Malanchi I, Santamaria-Martinez A, Susanto E, Peng H, Lehr HA, et al. (2012) Interactions between cancer stem cells and their niche govern metastatic colonization. Nature 481: 85-U95.
7. Yang L, Pang Y, Moses HL (2010) TGF-beta and immune cells: an important regulatory axis in the tumor microenvironment and progression. Trends Immunol 31: 220-227.
8. Akhurst RJ, Hata A (2012) Targeting the TGFbeta signalling pathway in disease. Nat Rev Drug Discov 11: 790-811.
9. Ezquerro IJ, Lasarte JJ, Dotor J, Castilla-Cortazar I, Bustos M, et al. (2003) A synthetic peptide from transforming growth factor beta type III receptor inhibits liver fibrogenesis in rats with carbon tetrachloride liver injury. Cytokine 22: 12-20. (Pubitemid 37222298)
10. Santiago B, Gutierrez-Canas I, Dotor J, Palao G, Lasarte JJ, et al. (2005) Topical application of a peptide inhibitor of transforming growth factor-beta1 ameliorates bleomycin-induced skin fibrosis. J Invest Dermatol 125: 450-455.
11. Hermida N, Lopez B, Gonzalez A, Dotor J, Lasarte JJ, et al. (2009) A synthetic peptide from transforming growth factor-beta1 type III receptor prevents myocardial fibrosis in spontaneously hypertensive rats. Cardiovasc Res 81: 601-609.
12. Cao WM, Murao K, Imachi H, Yu X, Abe H, et al. (2004) A mutant high-density lipoprotein receptor inhibits proliferation of human breast cancer cells. Cancer Res 64: 1515-1521. (Pubitemid 38235625)
13. Shahzad MM, Mangala LS, Han HD, Lu C, Bottsford-Miller J, et al. (2011) Targeted delivery of small interfering RNA using reconstituted high-density lipoprotein nanoparticles. Neoplasia 13: 309-319.
14. Sevko A, Sade-Feldman M, Kanterman J, Michels T, Falk CS, et al. (2013) Cyclophosphamide promotes chronic inflammation-dependent immunosuppression and prevents antitumor response in melanoma. J Invest Dermatol 133: 1610-1619.
15. Melero I, Duarte M, Ruiz J, Sangro B, Galofre J, et al. (1999) Intratumoral injection of bone-marrow derived dendritic cells engineered to produce interleukin-12 induces complete regression of established murine transplantable colon adenocarcinomas. Gene Ther 6: 1779-1784. (Pubitemid 29485955)
16. Fioravanti J, Gonzalez I, Medina-Echeverz J, Larrea E, Ardaiz N, et al. (2011) Anchoring interferon alpha to apolipoprotein A-I reduces hematological toxicity while enhancing immunostimulatory properties. Hepatology 53: 1864-1873.
17. Zabala M, Lasarte JJ, Perret C, Sola J, Berraondo P, et al. (2007) Induction of immunosuppressive molecules and regulatory T cells counteracts the antitumor effect of interleukin-12-based gene therapy in a transgenic mouse model of liver cancer. J Hepatol 47: 807-815. (Pubitemid 350051122)
18. Gately MK, Renzetti LM, Magram J, Stern AS, Adorini L, et al. (1998) The interleukin-12/interleukin-12-receptor system: role in normal and pathologic immune responses. Annu Rev Immunol 16: 495-521. (Pubitemid 28183374)
19. Takaku S, Terabe M, Ambrosino E, Peng J, Lonning S, et al. (2010) Blockade of TGF-beta enhances tumor vaccine efficacy mediated by CD8(+) T cells. International journal of cancerJournal international du cancer 126: 1666-1674.
20. Grieger JC, Samulski RJ (2005) Adeno-associated virus as a gene therapy vector: vector development, production and clinical applications. Adv Biochem Eng Biotechnol 99: 119-145. (Pubitemid 44617179)
21. Nakai H, Fuess S, Storm TA, Muramatsu S, Nara Y, et al. (2005) Unrestricted hepatocyte transduction with adeno-associated virus serotype 8 vectors in mice. J Virol 79: 214-224. (Pubitemid 39650967)
22. Massague J (2008) TGFbeta in Cancer. Cell 134: 215-230.
23. Derynck R, Akhurst RJ, Balmain A (2001) TGF-beta signaling in tumor suppression and cancer progression. Nat Genet 29: 117-129. (Pubitemid 32952643)
24. Neil JR, Johnson KM, Nemenoff RA, Schiemann WP (2008) Cox-2 inactivates Smad signaling and enhances EMT stimulated by TGF-beta through a PGE2-dependent mechanisms. Carcinogenesis 29: 2227-2235.
25. Shirakihara T, Horiguchi K, Miyazawa K, Ehata S, Shibata T, et al. (2011) TGF-beta regulates isoform switching of FGF receptors and epithelial- mesenchymal transition. EMBO J 30: 783-795.
26. Malanchi I, Santamaria-Martinez A, Susanto E, Peng H, Lehr HA, et al. (2011) Interactions between cancer stem cells and their niche govern metastatic colonization. Nature 481: 85-89.
27. Kato M, Takahashi M, Akhand AA, Liu W, Dai Y, et al. (1998) Transgenic mouse model for skin malignant melanoma. Oncogene 17: 1885-1888. (Pubitemid 28482792)
28. Umansky V, Abschuetz O, Osen W, Ramacher M, Zhao F, et al. (2008) Melanoma-specific memory T cells are functionally active in Ret transgenic mice without macroscopic tumors. Cancer Res 68: 9451-9458.
29. Abschuetz O, Osen W, Frank K, Kato M, Schadendorf D, et al. (2012) T-Cell Mediated Immune Responses Induced in ret Transgenic Mouse Model of Malignant Melanoma. Cancers (Basel) 4: 490-503.
30. Pickup M, Novitskiy S, Moses HL (2013) The roles of TGFbeta in the tumour microenvironment. Nat Rev Cancer 13: 788-799.
31. Gu X, Trigatti B, Xu S, Acton S, Babitt J, et al. (1998) The efficient cellular uptake of high density lipoprotein lipids via scavenger receptor class B type I requires not only receptor-mediated surface binding but also receptor-specific lipid transfer mediated by its extracellular domain. J Biol Chem 273: 26338-26348. (Pubitemid 28471637)
32. Pussinen PJ, Karten B, Wintersperger A, Reicher H, McLean M, et al. (2000) The human breast carcinoma cell line HBL-100 acquires exogenous cholesterol from high-density lipoprotein via CLA-1 (CD-36 and LIMPII analogous 1)-mediated selective cholesteryl ester uptake. Biochem J 349: 559-566. (Pubitemid 30465791)
33. Lacko AG, Nair M, Paranjape S, Mooberry L, McConathy WJ (2006) Trojan horse meets magic bullet to spawn a novel, highly effective drug delivery model. Chemotherapy 52: 171-173. (Pubitemid 43882414)
34. Schlingensiepen KH, Schlingensiepen R, Steinbrecher A, Hau P, Bogdahn U, et al. (2006) Targeted tumor therapy with the TGF-beta 2 antisense compound AP 12009. Cytokine Growth Factor Rev 17: 129-139. (Pubitemid 43117522)
35. Nam JS, Terabe M, Mamura M, Kang MJ, Chae H, et al. (2008) An antitransforming growth factor beta antibody suppresses metastasis via cooperative effects on multiple cell compartments. Cancer Res 68: 3835-3843.