Interstitial Pressure in Pancreatic Ductal Adenocarcinoma Is Dominated by a Gel-Fluid Phase

Biophysical Journal

Volumn 110, Issue 9, 2016, Pages 2106-2119

  Dufort, Christopher C ^a   DelGiorno, Kathleen E ^a   Carlson, Markus A ^a   Osgood, Ryan J ^b   Zhao, Chunmei ^b   Huang, Zhongdong ^b   Thompson, Curtis B ^b   Connor, Robert J ^b   Thanos, Christopher D ^b   Scott Brockenbrough, J ^a   Provenzano, Paolo P ^a   Frost, Gregory I ^b   Michael Shepard, H ^b   Hingorani, Sunil R ^a,c  

^a Fred Hutchinson Cancer Research Center   (United States)

^b Halozyme Therapeutics Inc   (United States)

^c UNIVERSITY OF WASHINGTON SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

HYALURONIC ACID;

ADENOCARCINOMA; ANIMAL; DRUG EFFECTS; EXTRACELLULAR FLUID; HYDROSTATIC PRESSURE; METABOLISM; MOUSE; NIH 3T3 CELL LINE; PANCREAS TUMOR; PATHOLOGY; VISCOSITY;

ADENOCARCINOMA; ANIMALS; EXTRACELLULAR FLUID; HYALURONIC ACID; HYDROSTATIC PRESSURE; MICE; NIH 3T3 CELLS; PANCREATIC NEOPLASMS; VISCOSITY;

EID: 84966394797     PISSN: 00063495     EISSN: 15420086     Source Type: Journal    
DOI: 10.1016/j.bpj.2016.03.040     Document Type: Article

References (74)

1. E.H. Starling On the absorption of fluids from the connective tissue spaces J. Physiol. 19 1896 312 326
2. A. Katchalsky Polyelectrolytes and their biological interactions Biophys. J. 4 1964 9 41
3. J.S. Young, C.E. Lumsden, and A.L. Stalker The significance of the tissue pressure of normal testicular and of neoplastic (Brown-Pearce carcinoma) tissue in the rabbit J. Pathol. Bacteriol. 62 1950 313 333
4. R.K. Jain Transport of molecules in the tumor interstitium: a review Cancer Res. 47 1987 3039 3051
5. C.H. Heldin, and K. Rubin A. Ostman High interstitial fluid pressure - an obstacle in cancer therapy Nat. Rev. Cancer 4 2004 806 813
6. P.P. Provenzano, and C. Cuevas S.R. Hingorani Enzymatic targeting of the stroma ablates physical barriers to treatment of pancreatic ductal adenocarcinoma Cancer Cell 21 2012 418 429
7. A.C. Guyton A concept of negative interstitial pressure based on pressures in implanted perforated capsules Circ. Res. 12 1963 399 414
8. P.F. Scholander, A.R. Hargens, and S.L. Miller Negative pressure in the interstitial fluid of animals. Fluid tensions are spectacular in plants; in animals they are elusively small, but just as vital Science 161 1968 321 328
9. H.O. Fadnes, R.K. Reed, and K. Aukland Interstitial fluid pressure in rats measured with a modified wick technique Microvasc. Res. 14 1977 27 36
10. A.C. Guyton, H.J. Granger, and A.E. Taylor Interstitial fluid pressure Physiol. Rev. 51 1971 527 563
11. T.G. Simonsen, and J.V. Gaustad E.K. Rofstad High interstitial fluid pressure is associated with tumor-line specific vascular abnormalities in human melanoma xenografts PLoS One 7 2012 e40006
12. P.A. Netti, and L.M. Hamberg R.K. Jain Enhancement of fluid filtration across tumor vessels: implication for delivery of macromolecules Proc. Natl. Acad. Sci. USA 96 1999 3137 3142
13. H. Wiig, and E. Tveit L. Weiss Interstitial fluid pressure in DMBA-induced rat mammary tumours Scand. J. Clin. Lab. Invest. 42 1982 159 164
14. K.P. Olive, and M.A. Jacobetz D.A. Tuveson Inhibition of Hedgehog signaling enhances delivery of chemotherapy in a mouse model of pancreatic cancer Science 324 2009 1457 1461
15. M.A. Jacobetz, and D.S. Chan D.A. Tuveson Hyaluronan impairs vascular function and drug delivery in a mouse model of pancreatic cancer Gut 62 2013 112 120
16. R.A. Brace, and A.C. Guyton Interstitial fluid pressure: capsule, free fluid, gel fluid, and gel absorption pressure in subcutaneous tissue Microvasc. Res. 18 1979 217 228
17. T.C. Laurent, and J.R. Fraser Hyaluronan FASEB J. 6 1992 2397 2404
18. J.R. Fraser, T.C. Laurent, and U.B. Laurent Hyaluronan: its nature, distribution, functions and turnover J. Intern. Med. 242 1997 27 33
19. R.K. Reed, K. Lilja, and T.C. Laurent Hyaluronan in the rat with special reference to the skin Acta Physiol. Scand. 134 1988 405 411
20. J. Hunger, and A. Bernecker R.P. Richter Hydration dynamics of hyaluronan and dextran Biophys. J. 103 2012 L10 L12
21. A. Prusova, F.J. Vergeldt, and J. Kucerik Influence of water content and drying on the physical structure of native hyaluronan Carbohydr. Polym. 95 2013 515 521
22. T.C. Laurent The ultrastructure and physical-chemical properties of interstitial connective tissue Pflugers Arch. 336 Suppl 1972 21 42
23. J.H. Fessler A structural function of mucopolysaccharide in connective tissue Biochem. J. 76 1960 124 132
24. A.C. Guyton, K. Scheel, and D. Murphree Interstitial fluid pressure. 3. Its effect on resistance to tissue fluid mobility Circ. Res. 19 1966 412 419
25. R.A. Brace Progress toward resolving the controversy of positive vs. negative interstitial fluid pressure Circ. Res. 49 1981 281 297
26. S.R. Hingorani, and E.F. Petricoin D.A. Tuveson Preinvasive and invasive ductal pancreatic cancer and its early detection in the mouse Cancer Cell 4 2003 437 450
27. G12D cooperate to promote chromosomal instability and widely metastatic pancreatic ductal adenocarcinoma in mice Cancer Cell 7 2005 469 483
28. C.B. Thompson, and H.M. Shepard G.I. Frost Enzymatic depletion of tumor hyaluronan induces antitumor responses in preclinical animal models Mol. Cancer Ther. 9 2010 3052 3064
29. K.E. DelGiorno, and M.A. Carlson S.R. Hingorani Interstitial pressure and vascular collapse in pancreas cancer-fluids and solids, measurement and meaning Cancer Cell 26 2014 16 17
30. L. Jadin, and L. Huang H.M. Shepard Characterization of a novel recombinant hyaluronan binding protein for tissue hyaluronan detection J. Histochem. Cytochem. 62 2014 672 683
31. R.F. Reinoso, B.A. Telfer, and M. Rowland Tissue water content in rats measured by desiccation J. Pharmacol. Toxicol. Methods 38 1997 87 92
32. R.H. Hruban, and N.V. Adsay D.A. Tuveson Pathology of genetically engineered mouse models of pancreatic exocrine cancer: consensus report and recommendations Cancer Res. 66 2006 95 106
33. K. Aukland, and R.K. Reed Interstitial-lymphatic mechanisms in the control of extracellular fluid volume Physiol. Rev. 73 1993 1 78
34. A.C. Guyton Interstitial fluid presure. II. Pressure-volume curves of interstitial space Circ. Res. 16 1965 452 460
35. G.B. Forbes, and R.W. Deisher A.F. Hartmann Effect of hyaluronidase on the subcutaneous absorption of electrolytes in humans Science 111 1950 177 179
36. O. Hechter, S.K. Dopkeen, and M.H. Yudell The clinical use of hyaluronidase in hypodermoclysis J. Pediatr. 30 1947 645 656
37. W.R. Webb Effect of hyaluronidase on rate of absorption of subcutaneous fluids AMA Arch. Surg. 65 1952 770 773
38. L.S. Sannella The effect of testicular extract on the distribution and absorption of subcutaneous saline solution Yale J. Biol. Med. 12 1940 433 439
39. J. Schwartzman, A.T. Henderson, and W.E. King Hyaluronidase in fluid administration; a preliminary report J. Pediatr. 33 1948 267 273
40. K.P. Sunnergren, and M.J. Rovetto The effects of hyaluronidase on interstitial hydration, plasma protein exclusion, and microvascular permeability in the isolated perfused rat heart Microvasc. Res. 30 1985 286 297
41. R.A. Wolf, and L.Y. Chaung E. Braunwald Intravenous bovine testicular hyaluronidase depolymerizes myocardial hyaluronic acid in dogs with coronary artery occlusion Circ. Res. 48 1981 88 95
42. E. Braunwald, P.R. Maroko, and P. Libby Reduction of infarct size following coronary occlusion Circ. Res. 35 Suppl 3 1974 192 201
43. R. Stern, and M.J. Jedrzejas Hyaluronidases: their genomics, structures, and mechanisms of action Chem. Rev. 106 2006 818 839
44. M.J. Jedrzejas, and R. Stern Structures of vertebrate hyaluronidases and their unique enzymatic mechanism of hydrolysis Proteins 61 2005 227 238
45. T. Kaneiwa, and S. Mizumoto S. Yamada Identification of human hyaluronidase-4 as a novel chondroitin sulfate hydrolase that preferentially cleaves the galactosaminidic linkage in the trisulfated tetrasaccharide sequence Glycobiology 20 2010 300 309
46. T. Honda, and T. Kaneiwa S. Yamada Hyaluronidases have strong hydrolytic activity toward chondroitin 4-sulfate comparable to that for hyaluronan Biomolecules 2 2012 549 563
47. J.L. Wike-Hooley, J. Haveman, and H.S. Reinhold The relevance of tumour pH to the treatment of malignant disease Radiother. Oncol. 2 1984 343 366
48. I.F. Tannock, and D. Rotin Acid pH in tumors and its potential for therapeutic exploitation Cancer Res. 49 1989 4373 4384
49. P.P. Provenzano, and S.R. Hingorani Hyaluronan, fluid pressure, and stromal resistance in pancreas cancer Br. J. Cancer 108 2013 1 8
50. H. Wiig, R.K. Reed, and K. Aukland Micropuncture measurement of interstitial fluid pressure in rat subcutis and skeletal muscle: comparison to wick-in-needle technique Microvasc. Res. 21 1981 308 319
51. Y. Boucher, and R.K. Jain Microvascular pressure is the principal driving force for interstitial hypertension in solid tumors: implications for vascular collapse Cancer Res. 52 1992 5110 5114
52. Y. Boucher, L.T. Baxter, and R.K. Jain Interstitial pressure gradients in tissue-isolated and subcutaneous tumors: implications for therapy Cancer Res. 50 1990 4478 4484
53. P.A. Netti, and L.T. Baxter R.K. Jain Time-dependent behavior of interstitial fluid pressure in solid tumors: implications for drug delivery Cancer Res. 55 1995 5451 5458
54. J.A. Nagy, and H.F. Dvorak Heterogeneity of the tumor vasculature: the need for new tumor blood vessel type-specific targets Clin. Exp. Metastasis 29 2012 657 662
55. A.J. Combest, and P.J. Roberts W.C. Zamboni Genetically engineered cancer models, but not xenografts, faithfully predict anticancer drug exposure in melanoma tumors Oncologist 17 2012 1303 1316
56. H. Sikder, and D.L. Huso R.M. Alani Disruption of Id1 reveals major differences in angiogenesis between transplanted and autochthonous tumors Cancer Cell 4 2003 291 299
57. M. Singh, and N. Ferrara Modeling and predicting clinical efficacy for drugs targeting the tumor milieu Nat. Biotechnol. 30 2012 648 657
58. V.P. Chauhan, and Y. Boucher R.K. Jain Compression of pancreatic tumor blood vessels by hyaluronan is caused by solid stress and not interstitial fluid pressure Cancer Cell 26 2014 14 15
59. T. Stylianopoulos, and J.D. Martin R.K. Jain Causes, consequences, and remedies for growth-induced solid stress in murine and human tumors Proc. Natl. Acad. Sci. USA 109 2012 15101 15108
60. U. Ozerdem, and A.R. Hargens A simple method for measuring interstitial fluid pressure in cancer tissues Microvasc. Res. 70 2005 116 120
61. A.G. Ogston On water binding Fed. Proc. 25 1966 986 989
62. T.C. Laurent, and A.G. Ogston The interaction between polysaccharides and other macromolecules. 4. The osmotic pressure of mixtures of serum albumin and hyaluronic acid Biochem. J. 89 1963 249 253
63. L. Rodén Structure and metabolism of connective tissue proteoglycans W.J. Lennarz, The Biochemistry of Glycoproteins and Proteoglycans 1980 Springer Boston, MA 267 371
64. L. Roden, and T. Koerner N.B. Schwartz Mechanisms of chain initiation in the biosynthesis of connective tissue polysaccharides Fed. Proc. 44 1985 373 380
65. T. Hardingham Chapter 1. Solution properties of hyaluronan H.G. Garg, C.A. Hales, Chemistry and Biology of Hyaluronan 2004 Elsevier Science, Oxford United Kingdom 1 19
66. W.E. Krause, E.G. Bellomo, and R.H. Colby Rheology of sodium hyaluronate under physiological conditions Biomacromolecules 2 2001 65 69
67. T.P. Padera, and B.R. Stoll R.K. Jain Pathology: cancer cells compress intratumour vessels Nature 427 2004 695
68. R.H. Hruban Tumors of the pancreas R.H. Hruban, M.B. Pitman, D.S. Klimstra, Atlas of Tumor Pathology 2007 Armed Forces Institute of Pathology Washington, DC
69. J. Klein, and F.A. Meyer Tissue structure and macromolecular diffusion in umbilical cord. Immobilization of endogenous hyaluronic acid Biochim. Biophys. Acta 755 1983 400 411
70. F.A. Meyer Macromolecular basis of globular protein exclusion and of swelling pressure in loose connective tissue (umbilical cord) Biochim. Biophys. Acta 755 1983 388 399
71. E.M. Landis, and J.R. Pappenheimer Exchange of substances through the capillary walls W.F. Hamilton, Handbook of Physiology. Circulation 1963 American Physiological Society Washington, DC 961 1034
72. S.R. Hingorani, and W.P. Harris C.E. Devoe Phase Ib study of PEGylated recombinant human hyaluronidase and gemcitabine in patients with advanced pancreatic cancer Clin. Cancer Res. 2016 10.1158/1078-0432.CCR-15-2010 Published online January 26, 2016
73. S.R. Hingorani, and W.P. Harris P. Jiang High response rate and PFS with PEGPH20 added to nab-paclitaxel/gemcitabine in stage IV previously untreated pancreatic cancer patients with high-HA tumors: interim results of a randomized phase II study J. Clin. Oncol. 33 2015 4006
74. S.R. Hingorani, and W.P. Harris A.J. Bullock Interim results of a randomized phase II study of PEGPH20 added to nab-paclitaxel/gemcitabine in patients with stage IV previously untreated pancreatic cancer J. Clin. Oncol. 34 2016 439