Mathematical modeling of herpes simplex virus distribution in solid tumors: Implications for cancer gene therapy

Clinical Cancer Research

Volumn 15, Issue 7, 2009, Pages 2352-2360

  Mok, Wilson ^a,b   Stylianopoulos, Triantafyllos ^a   Boucher, Yves ^a   Jain, Rakesh K ^a  

^a MASSACHUSETTS GENERAL HOSPITAL   (United States)

^b Massachusetts Institute of Technology Cambridge   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ONCOLYTIC HERPES VIRUS; VIRUS VECTOR;

ARTICLE; BINDING AFFINITY; DEGRADATION; DIFFUSION COEFFICIENT; DRUG DISTRIBUTION; HERPES SIMPLEX VIRUS; INTERNALIZATION; MATHEMATICAL MODEL; NONHUMAN; ONCOLYTIC VIROTHERAPY; PRIORITY JOURNAL; SENSITIVITY ANALYSIS; SOLID TUMOR; VIRAL GENE DELIVERY SYSTEM; VIRUS ATTACHMENT;

ANIMALS; DIFFUSION; GENE THERAPY; GENETIC VECTORS; KINETICS; MODELS, BIOLOGICAL; NEOPLASMS; ONCOLYTIC VIROTHERAPY; ONCOLYTIC VIRUSES; SIMPLEXVIRUS; VIRUS INTERNALIZATION;

EID: 65249107180     PISSN: 10780432     EISSN: None     Source Type: Journal    
DOI: 10.1158/1078-0432.CCR-08-2082     Document Type: Article

References (50)

1. Liu TC, Galanis E, Kirn D. Clinical trial results with oncolytic virotherapy: a century of promise, a decade of progress. Nat Clin Pract Oncol 2007;4:101-17.
2. Jain RK. The next frontier of molecular medicine: delivery of therapeutics. Nat Med 1998;4:655-7.
3. Sauthoff H, Hu J, Maca C, et al. Intratumoral spread of wild-type adenovirus is limited after local injection of human xenograft tumors: virus persists and spreads systemically at late time points. Hum Gene Ther 2003;14:425-33.
4. van Etten B, ten HagenTL, deVries MR, Ambagtsheer G, Huet T, Eggermont AM. Prerequisites for effective adenovirus mediated gene therapy of colorectal liver metastases in the rat using an intracellular neutralizing antibody fragment to p21-Ras. Br J Cancer 2002;86: 436-42.
5. Yuan F, Leunig M, Huang SK, Berk DA, Papahadjo- poulos D, Jain RK. Microvascular permeability and interstitial penetration of sterically stabilized (stealth) liposomes in a human tumor xenograft. Cancer Res 1994;54:3352-6.
6. McKeeTD, Grandi P, Mok W, et al. Degradation of fibrillar collagen in a human melanoma xenograft improves the efficacy of an oncolytic herpes simplex virus vector. Cancer Res 2006;66:2509-13.
7. NettiPA,BerkDA,SwartzMA,GrodzinskyAJ,Jain RK. Role of extracellular matrix assembly in interstitial transport in solid tumors. Cancer Res 2000;60: 2497-503.
8. Tao Y, Guo Q. The competitive dynamics between tumor cells, a replication-competent virus and an immune response. J Math Biol 2005;51:37-74.
9. Wein LM,Wu JT, Kirn DH. Validation and analysis of a mathematical model ofa replication-competent onco- lytic virus for cancer treatment: implications for virus design and delivery. Cancer Res 2003;63:1317-24.
10. Wodarz D. Viruses as antitumor weapons: defining conditions for tumor remission. Cancer Res 2001;61: 3501 -7.
11. Pluen A, Boucher Y, Ramanujan S, et al. Role of tumor-host interactions in interstitial diffusion ofmac- romolecules: cranial vs. subcutaneous tumors. Proc Natl Acad Sci U S A 2001;98:4628-33.
12. Shukla D, Spear PG. Herpesviruses and heparan sulfate: an intimate relationship in aid of viral entry. J Clin Invest 2001;108:503-10.
13. Herold BC,Visalli RJ, Susmarski N, Brandt CR, Spear PG. Glycoprotein C-independent binding of herpes simplex virus to cells requires cell surfaceheparan sul- phate and glycoprotein B. J GenVirol 1994;75:1211 -22.
14. Shieh MT,Wu Dunn D, Montgomery RI, Esko JD, Spear PG. Cell surface receptors for herpes simplex virus are heparan sulfate proteoglycans. J Cell Biol 1992;116:1273-81.
15. WuDunn D, Spear PG. Initial interaction of herpes simplex virus with cells is binding to heparan sulfate. JVirol 1989;63:52-8.
16. Rux AH, Lou H, Lambris JD, Friedman HM, Eisenberg RJ, Cohen GH. Kinetic analysis of glyco- protein C of herpes simplex virus types1and2binding to heparin, heparan sulfate, and complement component C3b.Virology 2002;294:324-32.
17. Williams RK, Straus SE. Specificity and affinity of binding of herpes simplex virus type 2 glycoprotein B to glycosaminoglycans. J Virol 1997;71:1375-80.
18. Herold BC, Wu Dunn D, Soltys N, Spear PG. Glyco- protein C of herpes simplex virus type1 plays aprinci- pal role in the adsorption of virus to cells and in infectivity. J Virol 1991;65:1090-8.
19. Laquerre S, Argnani R, Anderson DB, Zucchini S, Manservigi R, Glorioso JC. Heparan sulfate proteogly- can binding by herpes simplex virus type1 glycopro- teins B and C, which differ in their contributions to virus attachment, penetration, and cell-to-cell spread. J Virol 1998;72:6119-30.
20. Thurber GM, Wittrup KD. Quantitative spatiotempo- ral analysis of antibody fragment diffusion and endo- cytic consumption in tumor spheroids. Cancer Res 2008;68:3334-41.
21. NemunaitisJ, Khuri F, Ganly I, et al Phase II trial of intratumoral administration of ONYX-015, a replication-selective adenovirus, in patients with refractory head and neck cancer. J Clin Oncol 2001;19:289-98.
22. Baxter LT, Jain RK. Transport of fluid and macromolecules in tumors. I. Role of interstitial pressure and convection. Microvasc Res 1989;37:77-104.
23. Gerlowski LE, Jain RK. Microvascular permeability of normal and neoplastic tissues. Microvasc Res 1986;31:288-305.
24. Mok W, Boucher Y, Jain RK. Matrix metalloprotei- nases-1 and -8 improve the distribution and efficacy of an oncolytic virus. Cancer Res 2007;67:10664-8.
25. Chary SR, Jain RK. Direct measurement of interstitial convection and diffusion of albumin in normal and neoplastic tissues by fluorescence photobleaching. Proc Natl Acad Sci U S A1989;86:5385-9.
26. Phillips RJ, Deen WM, BradyJF. Hindered transport in fibrous membranes and gels. AIChE J 1989;35: 1761 -9.
27. Solomentsev YE, Anderson JL. Rotation of a sphere in Brinkman fluids. Phys Fluids 1996;8:1119-21.
28. Griffon-Etienne G, BoucherY, Brekken C, Suit HD, Jain RK. Taxane-induced apoptosis decompresses blood vessels and lowers interstitial fluid pressure in solid tumors: clinical implications. Cancer Res 1999; 59:3776-82.
29. Ramanujan S, Pluen A, McKeeTD, Brown EB, BoucherY, Jain RK. Diffusion and convection in collagen gels: implications for transport in the tumor inter- stitium. Biophys J 2002;83:1650-60.
30. Sodeik B, Ebersold MW, Helenius A. Microtubule- mediated transport of incoming herpes simplex virus1 capsids to the nucleus. J Cell Biol 1997;136:1007-21.
31. Day YS, Baird CL, Rich RL, Myszka DG. Direct comparison of binding equilibrium, thermodynamic, and rate constants determined by surface- and solution-based biophysical methods. Protein Sci 2002;11:1017-25.
32. Deinum J, Gustavsson L, Gyzander E, Kullman- Magnusson M, Edstrom A, Karlsson R. A thermody- namic characterization of the binding of thrombin inhibitors to human thrombin, combining biosensor technology, stopped-flow spectrophotometry, and microcalorimetry. Anal Biochem 2002;300:152-62.
33. Oddie GW, Gruen LC, Odgers GA, King LG, Kortt AA. Identification and minimization of nonideal binding effects in BIA core analysis: ferritin/anti-ferritin Fab' interaction as a model system. Anal Biochem 1997;244:301-11.
34. Roos H, Karlsson R, Nilshans H, Persson A Ther- modynamic analysis of protein interactions with biosensor technology. J Mol Recognit 1998;11:204-10.
35. Krol A, MarescaJ, Dewhirst MW,Yuan F. Available volume fraction of macromolecules in the extravascu- lar space of a fibrosarcoma: implications for drug delivery. Cancer Res 1999;59:4136-41.
36. Knipe DM, Howley PM. Fields Virology. 5th ed: Lippincott Williams and Wilkins; 2007.
37. Willis SH, Rux AH, Peng C, et al. Examination of the kinetics of herpes simplex virus glycoprotein D binding to the herpesvirus entry mediator, using surface plasmon resonance. J Virol 1998;72:5937-47.
38. Brown E, McKeeT, dTomaso E, et al. Dynamic imaging of collagen and its modulation in tumors in vivo using second-harmonic generation. Nat Med 2003;9:796-800.
39. Bakay L. The extracellular space in brain tumours. I. Morphological considerations. Brain 1970;93:693-8.
40. Gullino PM, Grantham FH, Smith SH. The interstitial water space of tumors. Cancer Res 1965;25:727-31.
41. O'Connor SW, Bale WF. Accessibility of circulating immunoglobulin G to the extravascular compartment of solid rat tumors. Cancer Res 1984;44:3719-23.
42. Cai WZ, Person S, Warner SC, Zhou JH, De Luca NA. Linker-insertion nonsense and restriction-site deletion mutations of the gB glycoprotein gene of herpes simplex virus type 1. J Virol 1987;61: 714-21.
43. Post DE, Fulci G, Chiocca EA,Van Meir EG. Replica- tive oncolytic herpes simplex viruses in combination cancer therapies. Curr GeneTher 2004;4:41 -51.
44. Jain RK. Delivery of molecular and cellular medicine to solid tumors. Adv Drug Deliv Rev 2001;46: 149-68.
45. Currier MA, Adams LC, Mahller YY, Cripe TP. Widespread intratumoral virus distribution with fractionated injection enables local control of large human rhabdomyosarcoma xenografts by oncolytic herpes simplex viruses. Cancer Gene Ther 2005;12: 407-16.
46. Bobo RH, Laske DW, Akbasak A, Morrison PF, Dedrick RL, Oldfield EH. Convection-enhanced deliv- ery of macromolecules in the brain. Proc Natl Acad Sci U SA1994;91:2076-80.
47. Boucher Y, Brekken C, Netti PA, Baxter LT, Jain RK. Intratumoral infusion of fluid: estimation of hydraulic conductivity and implications for the delivery of therapeutic agents. Br J Cancer 1998;78:1442-8.
48. Nagano S, Perentes JY, Jain RK, Boucher Y Cancer cell death enhances the penetration and efficacy of oncolytic herpes simplex virus in tumors. Cancer Res 2008;68:3795-802.
49. DingwellKS, Brunetti CR,Hendricks RL,et al. Herpes simplex virus glycoproteins E and I facilitate cell- to-cell spread in vivo and across junctions of cultured cells. J Virol 1994;68:834-45.
50. WangY, Hu JK, Krol A, LiYP, Li CY,Yuan F. Systemic dissemination of viral vectors during intratumoral injection. Mol CancerTher 2003;2:1233-42.