Hyaluronan impairs vascular function and drug delivery in a mouse model of pancreatic cancer

Gut

Volumn 62, Issue 1, 2013, Pages 112-120

  Jacobetz, Michael A ^a   Chan, Derek S ^a,b   Neesse, Albrecht ^a   Bapiro, Tashinga E ^a,b   Cook, Natalie ^a,b   Frese, Kristopher K ^a   Feig, Christine ^a   Nakagawa, Tomoaki ^a   Caldwell, Meredith E ^a   Zecchini, Heather I ^a   Lolkema, Martijn P ^a   Jiang, Ping ^c   Kultti, Anne ^c   Thompson, Curtis B ^c   Maneval, Daniel C ^c   Jodrell, Duncan I ^a   Frost, Gregory I ^c   Shepard, H M ^c   Skepper, Jeremy N ^d   Tuveson, David A ^a,b  

^a CANCER RESEARCH UK CAMBRIDGE RESEARCH INSTITUTE   (United Kingdom)

^b CAMBRIDGE UNIVERSITY HOSPITALS NHS FOUNDATION TRUST   (United Kingdom)

^c Halozyme Therapeutics Inc   (United States)

^d UNIVERSITY OF CAMBRIDGE   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

DOXORUBICIN; GEMCITABINE; HYALURONIC ACID; MACROGOL; RECOMBINANT HYALURONIDASE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTINEOPLASTIC ACTIVITY; ARTICLE; BIOACCUMULATION; BLOOD VESSEL PERMEABILITY; CANCER COMBINATION CHEMOTHERAPY; CANCER INHIBITION; CANCER LOCALIZATION; CANCER SURVIVAL; CONTROLLED STUDY; DRUG DELIVERY SYSTEM; DRUG EFFECT; DRUG EFFICACY; DRUG POTENTIATION; DRUG TARGETING; MOLECULAR PATHOLOGY; MONOTHERAPY; MOUSE; NONHUMAN; PANCREAS ADENOCARCINOMA; PRIORITY JOURNAL; TISSUE PERFUSION; VASCULAR PATENCY;

ANIMALS; ANTINEOPLASTIC AGENTS; ANTINEOPLASTIC COMBINED CHEMOTHERAPY PROTOCOLS; CARCINOMA, PANCREATIC DUCTAL; CELL ADHESION MOLECULES; DEOXYCYTIDINE; DOXORUBICIN; DRUG DELIVERY SYSTEMS; DRUG RESISTANCE, NEOPLASM; HYALURONIC ACID; HYALURONOGLUCOSAMINIDASE; IMMUNOHISTOCHEMISTRY; KAPLAN-MEIER ESTIMATE; MICE; MICE, TRANSGENIC; PANCREATIC NEOPLASMS; RECOMBINANT PROTEINS; TISSUE ARRAY ANALYSIS; TREATMENT OUTCOME; TUMOR MARKERS, BIOLOGICAL;

EID: 84871157346     PISSN: 00175749     EISSN: 14683288     Source Type: Journal    
DOI: 10.1136/gutjnl-2012-302529     Document Type: Article

References (43)

1. Vincent A, Herman J, Schulick R, et al. Pancreatic cancer. Lancet 2011;378:607-20.
2. Burris HA 3rd, Moore MJ, Andersen J, et al. Improvements in survival and clinical benefit with gemcitabine as first-line therapy for patients with advanced pancreas cancer: a randomized trial. J Clin Oncol 1997;15:2403-13. (Pubitemid 27251144)
3. Sultana A, Smith CT, Cunningham D, et al. Meta-analyses of chemotherapy for locally advanced and metastatic pancreatic cancer. J Clin Oncol 2007;25:2607-15. (Pubitemid 47041235)
4. Aguirre AJ, Bardeesy N, Sinha M, et al. Activated Kras and Ink4a/Arf deficiency cooperate to produce metastatic pancreatic ductal adenocarcinoma. Genes Dev 2003;17:3112-26. (Pubitemid 38040774)
5. Hingorani SR, Wang L, Multani AS, et al. Trp53R172H and KrasG12D cooperate to promote chromosomal instability and widely metastatic pancreatic ductal adenocarcinoma in mice. Cancer Cell 2005;7:469-83. (Pubitemid 40719130)
6. Bardeesy N, Aguirre AJ, Chu GC, et al. Both p16(Ink4a) and the p19(Arf)-p53 pathway constrain progression of pancreatic adenocarcinoma in the mouse. Proc Natl Acad Sci USA 2006;103:5947-52.
7. Olive KP, Jacobetz MA, Davidson CJ, et al. Inhibition of Hedgehog signaling enhances delivery of chemotherapy in a mouse model of pancreatic cancer. Science 2009;324:1457-61.
8. Olson P, Chu GC, Perry SR, et al. Imaging guided trials of the angiogenesis inhibitor sunitinib in mouse models predict efficacy in pancreatic neuroendocrine but not ductal carcinoma. Proc Natl Acad Sci USA 2011;108:E1275-84.
9. Komar G, Kauhanen S, Liukko K, et al. Decreased blood flow with increased metabolic activity: a novel sign of pancreatic tumor aggressiveness. Clin Cancer Res 2009;15:5511-17.
10. Young JS, Lumsden CE, Stalker AL. The significance of the tissue pressure of normal testicular and of neoplastic (Brown-Pearce carcinoma) tissue in the rabbit. J Pathol Bacteriol 1950;62:313-33.
11. Goldacre RJ, Sylven B. On the access of blood-borne dyes to various tumour regions. Br J Cancer 1962;16:306-22.
12. Stohrer M, Boucher Y, Stangassinger M, et al. Oncotic pressure in solid tumors is elevated. Cancer Res 2000;60:4251-5. (Pubitemid 30636613)
13. Heldin CH, Rubin K, Pietras K, et al. High interstitial fluid pressure - an obstacle in cancer therapy. Nat Rev Cancer 2004;4:806-13. (Pubitemid 39331152)
14. Jain RK. Normalization of tumor vasculature: an emerging concept in antiangiogenic therapy. Science 2005;307:58-62. (Pubitemid 40093472)
15. Toole BP, Slomiany MG. Hyaluronan: a constitutive regulator of chemoresistance and malignancy in cancer cells. Semin Cancer Biol 2008;18:244-50.
16. Chahine NO, Chen FH, Hung CT, et al. Direct measurement of osmotic pressure of glycosaminoglycan solutions by membrane osmometry at room temperature. Biophys J 2005;89:1543-50. (Pubitemid 41233512)
17. Beckenlehner K, Bannke S, Spruss T, et al. Hyaluronidase enhances the activity of adriamycin in breast cancer models in vitro and in vivo. J Cancer Res Clin Oncol 1992;118:591-6.
18. Brekken C, de Lange Davies C. Hyaluronidase reduces the interstitial fluid pressure in solid tumours in a non-linear concentration-dependent manner. Cancer Lett 1998;131:65-70. (Pubitemid 28467042)
19. Whatcott CJ, Han H, Posner RG, et al. Targeting the tumor microenvironment in cancer: why hyaluronidase deserves a second look. Cancer Discov 2011;1:291-6.
20. Thompson CB, Shepard HM, O'Connor PM, et al. Enzymatic depletion of tumor hyaluronan induces antitumor responses in preclinical animal models. Mol Cancer Ther 2010;9:3052-64.
21. Mahlbacher V, Sewing A, Elsässer HP, et al. Hyaluronan is a secretory product of human pancreatic adenocarcinoma cells. Eur J Cell Biol 1992;58:28-34.
22. Theocharis AD, Tsara ME, Papageorgacopoulou N, et al. Pancreatic carcinoma is characterized by elevated content of hyaluronan and chondroitin sulfate with altered disaccharide composition. Biochim Biophys Acta 2000;1502:201-6.
23. Fries H, Elsässer HP, Mahlbacher V, et al. Localisation of hyaluronate (HA) in primary tumors and nude mouse xenografts of human pancreatic carcinomas using a biotinylated HA-binding protein. Virchows Arch 1994;424:7-12. (Pubitemid 24102376)
24. Sironen RK, Tammi M, Tammi R, et al. Hyaluronan in human malignancies. Exp Cell Res 2011;317:383-91.
25. Bapiro TE, Richards FM, Goldgraben MA, et al. A novel method for quantification of gemcitabine and its metabolites 2′,2′- difluorodeoxyuridine and gemcitabine triphosphate in tumour tissue by LC-MS/MS: comparison with (19)F NMR spectroscopy. Cancer Chemother Pharmacol 2011;68:1243-53.
26. Dreher MR, Liu W, Michelich CR, et al. Tumor vascular permeability, accumulation, and penetration of macromolecular drug carriers. J Natl Cancer Inst 2006;98:335-44. (Pubitemid 43338213)
27. Roberts WG, Palade GE. Increased microvascular permeability and endothelial fenestration induced by vascular endothelial growth factor. J Cell Sci 1995;108:2369-79.
28. Roberts WG, Palade GE. Neovasculature induced by vascular endothelial growth factor is fenestrated. Cancer Res 1997;57:765-72. (Pubitemid 27085664)
29. Hashizume H, Baluk P, Morikawa S, et al. Openings between defective endothelial cells explain tumor vessel leakiness. Am J Pathol 2000;156:1363-80. (Pubitemid 30660013)
30. Mueller MT, Hermann PC, Witthauer J, et al. Combined targeted treatment to eliminate tumorigenic cancer stem cells in human pancreatic cancer. Gastroenterology 2009;137:1102-13.
31. Tian H, Callahan CA, DuPree KJ, et al. Hedgehog signaling is restricted to the stromal compartment during pancreatic carcinogenesis. Proc Natl Acad Sci USA 2009;106:4254-9.
32. Walter K, Omura N, Hong SM, et al. Overexpression of smoothened activates the sonic hedgehog signaling pathway in pancreatic cancer-associated fibroblasts. Clin Cancer Res 2010;16:1781-9.
33. Hobbs SK, Monsky WL, Yuan F, et al. Regulation of transport pathways in tumor vessels: role of tumor type and microenvironment. Proc Natl Acad Sci USA 1998;95:4607-12. (Pubitemid 28207960)
34. Kisker O, Onizuka S, Banyard J, et al. Generation of multiple angiogenesis inhibitors by human pancreatic cancer. Cancer Res 2001;61:7298-304. (Pubitemid 32946528)
35. Erkan M, Reiser-Erkan C, Michalski CW, et al. Cancer-stellate cell interactions perpetuate the hypoxia-fibrosis cycle in pancreatic ductal adenocarcinoma. Neoplasia 2009;11:497-508.
36. Xie L, Duncan MB, Pahler J, et al. Counterbalancing angiogenic regulatory factors control the rate of cancer progression and survival in a stage-specific manner. Proc Natl Acad Sci USA 2011;108:9939-44.
37. Kindler HL, Niedzwiecki D, Hollis D, et al. Gemcitabine plus bevacizumab compared with gemcitabine plus placebo in patients with advanced pancreatic cancer: phase III trial of the Cancer and Leukemia Group B (CALGB 80303). J Clin Oncol 2010;28:3617-22.
38. O'Reilly EM, Niedzwiecki D, Hall M, et al. A Cancer and Leukemia Group B phase II study of sunitinib malate in patients with previously treated metastatic pancreatic adenocarcinoma (CALGB 80603). Oncologist 2010;15:1310-19.
39. Kindler HL, Ioka T, Richel DJ, et al. Axitinib plus gemcitabine versus placebo plus gemcitabine in patients with advanced pancreatic adenocarcinoma: a double-blind randomised phase 3 study. Lancet Oncol 2011;12:256-62.
40. Singleton PA, Mirzapoiazova T, Guo Y, et al. High-molecular-weight hyaluronan is a novel inhibitor of pulmonary vascular leakiness. Am J Physiol Lung Cell Mol Physiol 2010;299:L639-51.
41. Tanaka Y, Makiyama Y, Mitsui Y. Anti-CD44 monoclonal antibody (IM7) induces murine systemic shock mediated by platelet activating factor. J Autoimmun 2002;18:9-15. (Pubitemid 34252589)
42. Lennon FE, Singleton PA. Hyaluronan regulation of vascular integrity. Am J Cardiovasc Dis 2011;1:200-13.
43. Jain RK, Baxter LT. Mechanisms of heterogeneous distribution of monoclonal antibodies and other macromolecules in tumors: significance of elevated interstitial pressure. Cancer Res 1988;48:7022-32. (Pubitemid 19013976)