3D culture broadly regulates tumor cell hypoxia response and angiogenesis via pro-inflammatory pathways

Biomaterials

Volumn 55, Issue 1, 2015, Pages 110-118

  DelNero, Peter ^a   Lane, Maureen ^b   Verbridge, Scott S ^c   Kwee, Brian ^a   Kermani, Pouneh ^b   Hempstead, Barbara ^b   Stroock, Abraham ^a   Fischbach, Claudia ^a  

^a Cornell University   (United States)

^b WEILL CORNELL MEDICAL COLLEGE   (United States)

^c VIRGINIA POLYTECHNIC INSTITUTE AND STATE UNIVERSITY   (United States)

Author keywords

3D culture; Angiogenesis; Cancer microenvironment; Hypoxia; Inflammation; Tissue engineering

Indexed keywords

CELL SIGNALING; DISEASES; GENE EXPRESSION; GENES; OXYGEN; TISSUE; TISSUE CULTURE; TUMORS;

3-D CULTURES; ANGIOGENESIS; HYPOXIA; INFLAMMATION; MICROENVIRONMENTS;

TISSUE ENGINEERING;

ALGINIC ACID; INTERLEUKIN 8; OXYGEN; BIOMATERIAL; GLUCURONIC ACID; HEXURONIC ACID; HYDROGEL;

ARTICLE; CARCINOGENESIS; CELL HYPOXIA; CELL INVASION; CELL INVASION ASSAY; GENE EXPRESSION; HUMAN; HUMAN CELL; HUMAN CELL CULTURE; HYDROGEL; IN VITRO STUDY; MICROARRAY ANALYSIS; PHYSICAL CHEMISTRY; PRIORITY JOURNAL; SIGNAL TRANSDUCTION; SPROUTING; TISSUE CULTURE; TUMOR CELL; TUMOR CELL CULTURE; TUMOR MICROENVIRONMENT; TUMOR MODEL; UMBILICAL VEIN ENDOTHELIAL CELL; CELL CULTURE TECHNIQUE; CHEMISTRY; DNA MICROARRAY; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; INFLAMMATION; METABOLISM; NEOPLASM; NEOVASCULARIZATION (PATHOLOGY); PATHOLOGY; PROCEDURES; TISSUE ENGINEERING; TUMOR INVASION; VASCULAR ENDOTHELIUM;

ALGINATES; BIOCOMPATIBLE MATERIALS; CELL CULTURE TECHNIQUES; CELL HYPOXIA; ENDOTHELIUM, VASCULAR; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, NEOPLASTIC; GLUCURONIC ACID; HEXURONIC ACIDS; HUMAN UMBILICAL VEIN ENDOTHELIAL CELLS; HUMANS; HYDROGELS; INFLAMMATION; INTERLEUKIN-8; NEOPLASM INVASIVENESS; NEOPLASMS; NEOVASCULARIZATION, PATHOLOGIC; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; OXYGEN; SIGNAL TRANSDUCTION; TISSUE ENGINEERING; TUMOR CELLS, CULTURED;

EID: 84932617660     PISSN: 01429612     EISSN: 18785905     Source Type: Journal    
DOI: 10.1016/j.biomaterials.2015.03.035     Document Type: Article

References (54)

1. Carmeliet P., Jain R.K. Angiogenesis in cancer and other diseases. Nature 2000, 407:249-257.
2. Semenza G.L. HIF-1: mediator of physiological and pathophysiological responses to hypoxia. JAppl Physiol 2000, 88:1474-1480.
3. Semenza G.L. Regulation of mammalian O-2 homeostasis by hypoxia- inducible factor 1. Annu Rev Cell Dev Biol 1999, 15:551-578.
4. Bergers G., Benjamin L.E. Tumorigenesis and the angiogenic switch. Nat Rev Cancer 2003, 3:401-410.
5. Dery M.A.C., Michaud M.D., Richard D.E. Hypoxia-inducible factor 1: regulation by hypoxic and non-hypoxic activators. Int J Biochem Cell Biol 2005, 37:535-540.
6. Semenza G.L. Defining the role of hypoxia-inducible factor 1 in cancer biology and therapeutics. Oncogene 2010, 29:625-634.
7. Aung K.Z., Pereira B.P., Tan P.H.S., Han H.C., Nathan S.S. Interstitial fluid pressure as an alternate regulator of angiogenesis independent of hypoxia driven HIF-1a in solid tumors. JOrthop Res 2012, 30:2038-2045.
8. Xu L., Xie K.P., Mukaida N., Matsushima K., Fidler I.J. Hypoxia-induced elevation in interleukin-8 expression by human ovarian carcinoma cells. Cancer Res 1999, 59:5822-5829.
9. Bianchi E., Denti S., Granata A., Bossi G., Geginat J., Villa A., et al. Integrin LFA-1 interacts with the transcriptional co-activator JAB1 to modulate AP-1 activity. Nature 2000, 404:617.
10. Bissell M.J., Radisky D.C., Rizki A., Weaver V.M., Petersen O.W. The organizing principle: microenvironmental influences in the normal and malignant breast. Differentiation 2002, 70:537-546.
11. Yamada K.M., Cukierman E. Modeling tissue morphogenesis and cancer in 3D. Cell 2007, 130:601-610.
12. Griffith L.G., Swartz M.A. Capturing complex 3D tissue physiology invitro. Nat Rev Mol Cell Bio 2006, 7:211-224.
13. Braun R.D., Beatty A.L. Modeling of oxygen transport across tumor multicellular layers. Microvasc Res 2007, 73:113-123.
14. Grimes D.R., Kelly C., Bloch K., Partridge M. Amethod for estimating the oxygenconsumption rate in multicellular tumour spheroids. JR Soc Interface 2014, 11.
15. Verbridge S.S., Choi N.W., Zheng Y., Brooks D.J., Stroock A.D., Fischbach C. Oxygen-controlled three-dimensional cultures to analyze tumor angiogenesis. Tissue Eng Pt A 2010, 16:2133-2141.
16. Bin Kim J., Stein R., O'Hare M.J. Three-dimensional invitro tissue culture models of breast cancer - a review. Breast Cancer Res Treat 2004, 85:281-291.
17. Debnath J., Brugge J.S. Modelling glandular epithelial cancers in three-dimensional cultures. Nat Rev Cancer 2005, 5:675-688.
18. Elliott N.T., Yuan F. Areview of three-dimensional invitro tissue models for drug discovery and transport studies. JPharm Sci 2011, 100:59-74.
19. Kim J.B. Three-dimensional tissue culture models in cancer biology. Seminars Cancer Biol 2005, 15:365-377.
20. Nelson C.M., Bissell M.J. Modeling dynamic reciprocity: engineering three-dimensional culture models of breast architecture, function, and neoplastic transformation. Seminars Cancer Biol 2005, 15:342-352.
21. Fischbach C., Chen R., Matsumoto T., Schmelzle T., Brugge J.S., Polverini P.J., et al. Engineering tumors with 3D scaffolds. Nat Methods 2007, 4:855-860.
22. Seo B.R., DelNero P., Fischbach C. Invitro models of tumor vessels and matrix: engineering approaches to investigate transport limitations and drug delivery in cancer. Adv Drug Deliv Rev 2014, 69-70:205-216.
23. DelNero P., Song Y.H., Fischbach C. Microengineered tumor models: insights & opportunities from a physical sciences-oncology perspective. Biomed Microdevices 2013, 15:583-593.
24. Cross V.L., Zheng Y., Choi N.W., Verbridge S.S., Sutermaster B.A., Bonassar L.J., et al. Dense type I collagen matrices that support cellular remodeling and microfabrication for studies of tumor angiogenesis and vasculogenesis invitro. Biomaterials 2010, 31:8596-8607.
25. Li A.H., Dubey S., Varney M.L., Dave B.J., Singh R.K. IL-8 directly enhanced endothelial cell survival, proliferation, and matrix metalloproteinases production and regulated angiogenesis. JImmunol 2003, 170:3369-3376.
26. Waugh D.J.J., Wilson C. The Interleukin-8 pathway in Cancer. Clin Cancer Res 2008, 14:6735-6741.
27. Gyanchandani R., Sano D., Alves M.V.O., Klein J.D., Knapick B.A., Oh S., et al. Interleukin-8 as a modulator of response to bevacizumab in preclinical models of head and neck squamous cell carcinoma. Oral Oncol 2013, 49:761-770.
28. Richardson A.L., Wang Z.G.C., De Nicolo A., Lu X., Brown M., Miron A., et al. Xchromosomal abnormalities in basal-like human breast cancer. Cancer Cell 2006, 9:121-132.
29. D'Errico M., de Rinaldis E., Blasi M.F., Viti V., Falchetti M., Calcagnile A., et al. Genome-wide expression profile of sporadic gastric cancers with microsatellite instability. Eur J Cancer 2009, 45:461-469.
30. Talbot S.G., Estilo C., Maghami E., Sarkaria I.S., Pham D.K., O-charoenrat P., et al. Gene expression profiling allows distinction between primary and metastatic squamous cell carcinomas in the lung. Cancer Res 2005, 65:3063-3071.
31. Peng C.H., Liao C.T., Peng S.C., Chen Y.J., Cheng A.J., Juang J.L., et al. Anovel molecular signature identified by systems genetics approach predicts prognosis in oral squamous cell carcinoma. Plos One 2011, 6.
32. Masuya D., Huang C.L., Liu D., Kameyama K., Hayashi E., Yamauchi A., et al. The intratumoral expression of vascular endothelial growth factor and interleukin-8 associated with angiogenesis in nonsmall cell lung carcinoma patients. Cancer 2001, 92:2628-2638.
33. Heidemann J., Ogawa H., Dwinell M.B., Rafiee P., Maaser C., Gockel H.R., et al. Angiogenic effects of interleukin 8 (CXCL8) in human intestinal microvascular endothelial cells are mediated by CXCR2. JBiol Chem 2003, 278:8508-8515.
34. He J.W., Genetos D.C., Yellowley C.E., Leach J.K. Oxygen tension differentially influences osteogenic differentiation of human adipose stem cells in 2D and 3D cultures. JCell Biochem 2010, 110:87-96.
35. Levin V.A., Panchabhai S., Shen L., Baggerly K.A. Protein and phosphoprotein levels in glioma and adenocarcinoma cell lines grown in normoxia and hypoxia in monolayer and three-dimensional cultures. Proteome Sci 2012, 10.
36. Rak J., Yu J.L., Klement G., Kerbel R.S. Oncogenes and angiogenesis: signaling three-dimensional tumor growth. JInvestig Dermatol Symp Proc 2000, 5:24-33.
37. Leslie K., Gao S.P., Berishaj M., Podsypanina K., Ho H., Ivashkiv L., et al. Differential interleukin-6/Stat3 signaling as a function of cellular context mediates Ras-induced transformation. Breast Cancer Res 2010, 12.
38. Vogel T.W., Zhuang Z.P., Li J., Okamoto H., Furuta M., Lee Y.S., et al. Proteins and protein pattern differences between glioma cell lines and glioblastoma multiforme. Clin Cancer Res 2005, 11:3624-3632.
39. Ertel A., Verghese A., Byers S.W., Ochs M., Tozeren A. Pathway-specific differences between tumor cell lines and normal and tumor tissue cells. Mol Cancer 2006, 5.
40. Smith D.R., Polverini P.J., Kunkel S.L., Orringer M.B., Whyte R.I., Burdick M.D., et al. Inhibition of Interleukin-8 Attenuates angiogenesis in Bronchogenic-carcinoma. JExp Med 1994, 179:1409-1415.
41. Kitadai Y., Haruma K., Sumii K., Yamamoto S., Ue T., Yokozaki H., et al. Expression of interleukin-8 correlates with vascularity in human gastric carcinomas. Am J Pathol 1998, 152:93-100.
42. Fujimoto J., Aoki I., Khatun S., Toyoki H., Tamaya T. Clinical implications of expression of interleukin-8 related to myometrial invasion with angiogenesis in uterine endometrial cancers. Ann Oncol 2002, 13:430-434.
43. Desbaillets I., Diserens A.C., deTribolet N., Hamou M.F., Van Meir E.G. Upregulation of interleukin 8 by oxygen-deprived cells in glioblastoma suggests a role in leukocyte activation, chemotaxis, and angiogenesis. JExp Med 1997, 186:1201-1212.
44. Kubo F., Ueno S., Hiwatashi K., Sakoda M., Kawaida K., Nuruki K., et al. Interleukin 8 in human hepatocellular carcinoma correlates with cancer cell invasion of vessels but not with tumor angiogenesis. Ann Surg Oncol 2005, 12:800-807.
45. Akiba J., Yano H., Ogasawara S., Higaki K., Kojiro M. Expression and function of interleukin-8 in human hepatocellular carcinoma. Int J Oncol 2001, 18:257-264.
46. Huang D., Ding Y., Zhou M., Rini B.I., Petillo D., Qian C.N., et al. Interleukin-8 mediates resistance to antiangiogenic agent sunitinib in renal cell carcinoma. Cancer Res 2010, 70:1063-1071.
47. Nolan D.J., Ginsberg M., Israely E., Palikuqi B., Poulos M.G., James D., et al. Molecular signatures of tissue-specific microvascular endothelial cell heterogeneity in organ maintenance and regeneration. Dev Cell 2013, 26:204-219.
48. Aird W.C. Molecular heterogeneity of tumor endothelium. Cell Tissue Res 2009, 335:271-281.
49. Dudley A.C. Tumor endothelial cells. Csh Perspect Med 2012, 2.
50. Arenberg D.A., Kunkel S.L., Polverini P.J., Glass M., Burdick M.D., Strieter R.M. Inhibition of interleukin-8 reduces tumorigenesis of human non-small cell lung cancer in SCID mice. JClin Invest 1996, 97:2792-2802.
51. Strieter R.M., Kunkel S.L., Elner V.M., Martonyi C.L., Koch A.E., Polverini P.J., et al. Interleukin-8-a corneal factor that induces neovascularization. Am J Pathol 1992, 141:1279-1284.
52. Inoue K., Slaton J.W., Eve B.Y., Kim S.J., Perrotte P., Balbay M.D., et al. Interleukin 8 expression regulates tumorigenicity and metastases in androgen-independent prostate cancer. Clin Cancer Res 2000, 6:2104-2119.
53. Luca M., Huang S.Y., Gershenwald J.E., Singh R.K., Reich R., BarEli M. Expression of interleukin-8 by human melanoma cells up-regulates MMP-2 activity and increases tumor growth and metastasis. Am J Pathol 1997, 151:1105-1113.
54. Fujimoto J., Sakaguchi H., Aoki I., Tamaya T. Clinical implications of expression of interleukin 8 related to angiogenesis in uterine cervical cancers. Cancer Res 2000, 60:2632-2635.