Research

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Bruce Zetter, PhD

Bruce Zetter PhD
Program:
Vascular Biology Program
Department:
Surgery Research
Academic Title:
Charles Nowiszewski Professor of Cancer Biology in the Department of Surgery

Bruce Zetter is a pioneer in understanding how cell movement affects tumor metastasis. In 1980, he made the key discovery that interferon alpha, which inhibits viral proliferation, also inhibits the locomotion of endothelial cells necessary for angiogenesis. His work led to the use of interferon alpha to treat hemangiomas.

Dr. Zetter's laboratory's current focus is on tumor metastasis and on identifying diagnostic and prognostic markers that can guide treatment decisions, including a new prognostic marker for prostate cancer. Specifically, the investigators are looking at:

  • The mechanisms used by cancer cells to spread or metastasize to distant sites.
  • The genetic, molecular and cellular changes that occur as tumors undergo progression from benign to aggressive.
  • The development of new markers for the diagnosis and prognosis of human cancers.
  • The development of novel therapeutic treatments for metastatic human cancers.

The Zetter lab has developed a panel of markers to predict which tumors are likely to metastasize or to have already produced metastatic colonies. The prototype for this type of molecule is thymosin Beta-15, which stimulates cell migration and promotes metastasis in prostate cancer cells. Tumors in which thymosin Beta-15 cannot be detected are unlikely to develop metastases and may not warrant aggressive treatment, while those expressing thymosin B -15 are more likely to have disseminated metastases and are candidates for aggressive systemic therapy.

About Bruce Zetter

Dr. Zetter received a PhD from the University of Rhode Island. He completed postdoctoral fellowships at MIT and at the Salk Institute in San Diego. He has received numerous national and international awards for his work in the field of cancer research, including a Faculty Research Award from the American Cancer Society and the MERIT award from the US National Cancer Institute.

Publications

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  1. Xu Y, Yang W, Shi J, Zetter BR. Prohibitin 1 regulates tumor cell apoptosis via the interaction with X-linked inhibitor of apoptosis protein. J Mol Cell Biol. 2016 Jun; 8(3):282-5.
  2. Connor Y, Tekleab S, Nandakumar S, Walls C, Tekleab Y, Husain A, Gadish O, Sabbisetti V, Kaushik S, Sehrawat S, Kulkarni A, Dvorak H, Zetter B, R Edelman E, Sengupta S. Physical nanoscale conduit-mediated communication between tumour cells and the endothelium modulates endothelial phenotype. Nat Commun. 2015 Dec 16; 6:8671.
  3. Islam MA, Reesor EK, Xu Y, Zope HR, Zetter BR, Shi J. Biomaterials for mRNA delivery. Biomater Sci. 2015 Dec; 3(12):1519-33.
  4. Bielenberg DR, Zetter BR. The Contribution of Angiogenesis to the Process of Metastasis. Cancer J. 2015 Jul-Aug; 21(4):267-73.
  5. Zhu X, Xu Y, Solis LM, Tao W, Wang L, Behrens C, Xu X, Zhao L, Liu D, Wu J, Zhang N, Wistuba II, Farokhzad OC, Zetter BR, Shi J. Long-circulating siRNA nanoparticles for validating Prohibitin1-targeted non-small cell lung cancer treatment. Proc Natl Acad Sci U S A. 2015 Jun 23; 112(25):7779-84.
  6. Banyard J, Chung I, Migliozzi M, Phan DT, Wilson AM, Zetter BR, Bielenberg DR. Identification of genes regulating migration and invasion using a new model of metastatic prostate cancer. BMC Cancer. 2014 May 30; 14:387.
  7. Shi J, Xu Y, Xu X, Zhu X, Pridgen E, Wu J, Votruba AR, Swami A, Zetter BR, Farokhzad OC. Hybrid lipid-polymer nanoparticles for sustained siRNA delivery and gene silencing. Nanomedicine. 2014 Jul; 10(5):897-900.
  8. Zetter B, Lake F. Advancing treatment of metastatic cancers: from research to communication--where do we need to go? Future Oncol. 2014; 10(9):1535-40.
  9. Zhang Y, Yan W, Collins MA, Bednar F, Rakshit S, Zetter BR, Stanger BZ, Chung I, Rhim AD, di Magliano MP. Interleukin-6 is required for pancreatic cancer progression by promoting MAPK signaling activation and oxidative stress resistance. Cancer Res. 2013 Oct 15; 73(20):6359-74.
  10. Coughlin MF, Bielenberg DR, Lenormand G, Marinkovic M, Waghorne CG, Zetter BR, Fredberg JJ. Cytoskeletal stiffness, friction, and fluidity of cancer cell lines with different metastatic potential. Clin Exp Metastasis. 2013 Mar; 30(3):237-50.
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  12. Zetter B. Surviving cancer. Nat Med. 2012; 18(6):851.
  13. Piecewicz SM, Pandey A, Roy B, Xiang SH, Zetter BR, Sengupta S. Insulin-like growth factors promote vasculogenesis in embryonic stem cells. PLoS One. 2012; 7(2):e32191.
  14. Cao Y, Arbiser J, D'Amato RJ, D'Amore PA, Ingber DE, Kerbel R, Klagsbrun M, Lim S, Moses MA, Zetter B, Dvorak H, Langer R. Forty-year journey of angiogenesis translational research. Sci Transl Med. 2011 Dec 21; 3(114):114rv3.
  15. Spivey KA, Chung I, Banyard J, Adini I, Feldman HA, Zetter BR. A role for collagen XXIII in cancer cell adhesion, anchorage-independence and metastasis. Oncogene. 2012 May 3; 31(18):2362-72.
  16. Olsen RR, Chung I, Zetter BR. Knockdown of antizyme inhibitor decreases prostate tumor growth in vivo. Amino Acids. 2012 Feb; 42(2-3):549-58.
  17. Olsen RR, Zetter BR. Evidence of a role for antizyme and antizyme inhibitor as regulators of human cancer. Mol Cancer Res. 2011 Oct; 9(10):1285-93.
  18. Holleman A, Chung I, Olsen RR, Kwak B, Mizokami A, Saijo N, Parissenti A, Duan Z, Voest EE, Zetter BR. miR-135a contributes to paclitaxel resistance in tumor cells both in vitro and in vivo. Oncogene. 2011 Oct 27; 30(43):4386-98.
  19. Zetter BR. The scientific contributions of M. Judah Folkman to cancer research. Nat Rev Cancer. 2008 Aug; 8(8):647-54.
  20. Arap W, Trepel M, Zetter BR, Pasqualini R. Meeting report: innovations in prostate cancer research. Cancer Res. 2008 Feb 1; 68(3):635-8.
  21. Mangold U, Hayakawa H, Coughlin M, Münger K, Zetter BR. Antizyme, a mediator of ubiquitin-independent proteasomal degradation and its inhibitor localize to centrosomes and modulate centriole amplification. Oncogene. 2008 Jan 24; 27(5):604-13.
  22. Everley PA, Gartner CA, Haas W, Saghatelian A, Elias JE, Cravatt BF, Zetter BR, Gygi SP. Assessing enzyme activities using stable isotope labeling and mass spectrometry. Mol Cell Proteomics. 2007 Oct; 6(10):1771-7.
  23. Banyard J, Hutchinson LM, Zetter BR. Thymosin beta-NB is the human isoform of rat thymosin beta15. Ann N Y Acad Sci. 2007 Sep; 1112:286-96.
  24. Banyard J, Bao L, Hofer MD, Zurakowski D, Spivey KA, Feldman AS, Hutchinson LM, Kuefer R, Rubin MA, Zetter BR. Collagen XXIII expression is associated with prostate cancer recurrence and distant metastases. Clin Cancer Res. 2007 May 1; 13(9):2634-42.
  25. Kim SW, Mangold U, Waghorne C, Mobascher A, Shantz L, Banyard J, Zetter BR. Regulation of cell proliferation by the antizyme inhibitor: evidence for an antizyme-independent mechanism. J Cell Sci. 2006 Jun 15; 119(Pt 12):2583-91.
  26. Everley PA, Bakalarski CE, Elias JE, Waghorne CG, Beausoleil SA, Gerber SA, Faherty BK, Zetter BR, Gygi SP. Enhanced analysis of metastatic prostate cancer using stable isotopes and high mass accuracy instrumentation. J Proteome Res. 2006 May; 5(5):1224-31.
  27. Everley PA, Zetter BR. Proteomics in tumor progression and metastasis. Ann N Y Acad Sci. 2005 Nov; 1059:1-10.
  28. Zetter BR, Mangold U. Ubiquitin-independent degradation and its implication in cancer. Future Oncol. 2005 Oct; 1(5):567-70.
  29. Hutchinson LM, Chang EL, Becker CM, Shih MC, Brice M, DeWolf WC, Gaston SM, Zetter BR. Use of thymosin beta15 as a urinary biomarker in human prostate cancer. Prostate. 2005 Jul 1; 64(2):116-27.
  30. Hutchinson LM, Chang EL, Becker CM, Ushiyama N, Behonick D, Shih MC, DeWolf WC, Gaston SM, Zetter BR. Development of a sensitive and specific enzyme-linked immunosorbent assay for thymosin beta15, a urinary biomarker of human prostate cancer. Clin Biochem. 2005 Jun; 38(6):558-71.
  31. Short SM, Derrien A, Narsimhan RP, Lawler J, Ingber DE, Zetter BR. Inhibition of endothelial cell migration by thrombospondin-1 type-1 repeats is mediated by beta1 integrins. J Cell Biol. 2005 Feb 14; 168(4):643-53.
  32. Chatterjee SK, Zetter BR. Cancer biomarkers: knowing the present and predicting the future. Future Oncol. 2005 Feb; 1(1):37-50.
  33. Cheng GC, Schulze PC, Lee RT, Sylvan J, Zetter BR, Huang H. Oxidative stress and thioredoxin-interacting protein promote intravasation of melanoma cells. Exp Cell Res. 2004 Nov 1; 300(2):297-307.
  34. Newman RM, Mobascher A, Mangold U, Koike C, Diah S, Schmidt M, Finley D, Zetter BR. Antizyme targets cyclin D1 for degradation. A novel mechanism for cell growth repression. J Biol Chem. 2004 Oct 1; 279(40):41504-11.
  35. Lader AS, Ramoni MF, Zetter BR, Kohane IS, Kwiatkowski DJ. Identification of a transcriptional profile associated with in vitro invasion in non-small cell lung cancer cell lines. Cancer Biol Ther. 2004 Jul; 3(7):624-31.
  36. Everley PA, Krijgsveld J, Zetter BR, Gygi SP. Quantitative cancer proteomics: stable isotope labeling with amino acids in cell culture (SILAC) as a tool for prostate cancer research. Mol Cell Proteomics. 2004 Jul; 3(7):729-35.
  37. Bartelink H, Benz C, Cleveland D, Dorn R, Gralow J, Gradishar WJ, Grant K, Heimann R, Hellman S, Hudis C, Kerbel R, Lippman M, Lung J, Posner MC, Steeg P, Vestal R, Weichselbaum RR, Zetter B. Expedition Inspiration Fund for Breast Cancer Research Meeting 2003. Breast Cancer Res Treat. 2003 Jul; 80(2):139-44.
  38. Banyard J, Bao L, Zetter BR. Type XXIII collagen, a new transmembrane collagen identified in metastatic tumor cells. J Biol Chem. 2003 Jun 6; 278(23):20989-94.
  39. Kisker O, Onizuka S, Becker CM, Fannon M, Flynn E, D'Amato R, Zetter B, Folkman J, Ray R, Swamy N, Pirie-Shepherd S. Vitamin D binding protein-macrophage activating factor (DBP-maf) inhibits angiogenesis and tumor growth in mice. Neoplasia. 2003 Jan-Feb; 5(1):32-40.
  40. Zetter BR, Banyard J. Cancer. The silence of the genes. Nature. 2002 Oct 10; 419(6907):572-3.
  41. Becker CM, Farnebo FA, Iordanescu I, Behonick DJ, Shih MC, Dunning P, Christofferson R, Mulligan RC, Taylor GA, Kuo CJ, Zetter BR. Gene therapy of prostate cancer with the soluble vascular endothelial growth factor receptor Flk1. Cancer Biol Ther. 2002 Sep-Oct; 1(5):548-53.
  42. Parsons JT, Zetter B, Mohla S. Shifting paradigms in tumor metastasis: challenges and opportunities. Cancer Biol Ther. 2002 Sep-Oct; 1(5):582-5.
  43. Furman C, Short SM, Subramanian RR, Zetter BR, Roberts TM. DEF-1/ASAP1 is a GTPase-activating protein (GAP) for ARF1 that enhances cell motility through a GAP-dependent mechanism. J Biol Chem. 2002 Mar 8; 277(10):7962-9.
  44. Zetter BR. Hold that line. Angiomotin regulates endothelial cell motility. J Cell Biol. 2001 Mar 19; 152(6):F35-6.
  45. Bao L, Zetter BR. Molecular cloning and structural characterization of the rat thymosin beta15 gene. Gene. 2000 Dec 30; 260(1-2):37-44.
  46. Eadie JS, Kim SW, Allen PG, Hutchinson LM, Kantor JD, Zetter BR. C-terminal variations in beta-thymosin family members specify functional differences in actin-binding properties. J Cell Biochem. 2000 Mar; 77(2):277-87.
  47. Zhu J, Tseng YH, Kantor JD, Rhodes CJ, Zetter BR, Moyers JS, Kahn CR. Interaction of the Ras-related protein associated with diabetes rad and the putative tumor metastasis suppressor NM23 provides a novel mechanism of GTPase regulation. Proc Natl Acad Sci U S A. 1999 Dec 21; 96(26):14911-8.
  48. Koike C, Chao DT, Zetter BR. Sensitivity to polyamine-induced growth arrest correlates with antizyme induction in prostate carcinoma cells. Cancer Res. 1999 Dec 15; 59(24):6109-12.
  49. Arbiser JL, Karalis K, Viswanathan A, Koike C, Anand-Apte B, Flynn E, Zetter B, Majzoub JA. Corticotropin-releasing hormone stimulates angiogenesis and epithelial tumor growth in the skin. J Invest Dermatol. 1999 Nov; 113(5):838-42.
  50. Grosskreutz CL, Anand-Apte B, Dupláa C, Quinn TP, Terman BI, Zetter B, D'Amore PA. Vascular endothelial growth factor-induced migration of vascular smooth muscle cells in vitro. Microvasc Res. 1999 Sep; 58(2):128-36.
  51. Bao L, Loda M, Zetter BR. Thymosin beta15 expression in tumor cell lines with varying metastatic potential. Clin Exp Metastasis. 1998 Apr; 16(3):227-33.
  52. Zetter BR. Angiogenesis and tumor metastasis. Annu Rev Med. 1998; 49:407-24.
  53. Banyard J, Zetter BR. The role of cell motility in prostate cancer. Cancer Metastasis Rev. 1998-1999; 17(4):449-58.
  54. Zetter BR. On target with tumor blood vessel markers. Nat Biotechnol. 1997 Nov; 15(12):1243-4.
  55. Gold JS, Bao L, Ghoussoub RA, Zetter BR, Rimm DL. Localization and quantitation of expression of the cell motility-related protein thymosin beta15 in human breast tissue. Mod Pathol. 1997 Nov; 10(11):1106-12.
  56. Blatch GL, Lässle M, Zetter BR, Kundra V. Isolation of a mouse cDNA encoding mSTI1, a stress-inducible protein containing the TPR motif. Gene. 1997 Jul 31; 194(2):277-82.
  57. Anand-Apte B, Pepper MS, Voest E, Montesano R, Olsen B, Murphy G, Apte SS, Zetter B. Inhibition of angiogenesis by tissue inhibitor of metalloproteinase-3. Invest Ophthalmol Vis Sci. 1997 Apr; 38(5):817-23.
  58. Lässle M, Blatch GL, Kundra V, Takatori T, Zetter BR. Stress-inducible, murine protein mSTI1. Characterization of binding domains for heat shock proteins and in vitro phosphorylation by different kinases. J Biol Chem. 1997 Jan 17; 272(3):1876-84.
  59. Anand-Apte B, Zetter B. Signaling mechanisms in growth factor-stimulated cell motility. Stem Cells. 1997; 15(4):259-67.
  60. Bao L, Loda M, Janmey PA, Stewart R, Anand-Apte B, Zetter BR. Thymosin beta 15: a novel regulator of tumor cell motility upregulated in metastatic prostate cancer. Nat Med. 1996 Dec; 2(12):1322-8.
  61. Kantor JD, Zetter BR. Cell motility in breast cancer. Cancer Treat Res. 1996; 83:303-23.
  62. Anand-Apte B, Bao L, Smith R, Iwata K, Olsen BR, Zetter B, Apte SS. A review of tissue inhibitor of metalloproteinases-3 (TIMP-3) and experimental analysis of its effect on primary tumor growth. Biochem Cell Biol. 1996; 74(6):853-62.
  63. Smith RC, Litwin MS, Lu Y, Zetter BR. Identification of an endogenous inhibitor of prostatic carcinoma cell growth. Nat Med. 1995 Oct; 1(10):1040-5.
  64. Brightman SE, Blatch GL, Zetter BR. Isolation of a mouse cDNA encoding MTJ1, a new murine member of the DnaJ family of proteins. Gene. 1995 Feb 14; 153(2):249-54.
  65. Meininger CJ, Brightman SE, Kelly KA, Zetter BR. Increased stem cell factor release by hemangioma-derived endothelial cells. Lab Invest. 1995 Feb; 72(2):166-73.
  66. Kundra V, Soker S, Zetter BR. Excess early signaling activity inhibits cellular chemotaxis toward PDGF-BB. Oncogene. 1994 May; 9(5):1429-35.
  67. Yenush L, Kundra V, White MF, Zetter BR. Functional domains of the insulin receptor responsible for chemotactic signaling. J Biol Chem. 1994 Jan 7; 269(1):100-4.
  68. Dethlefsen SM, Matsuura N, Zetter BR. Mast cell accumulation at sites of murine tumor implantation: implications for angiogenesis and tumor metastasis. Invasion Metastasis. 1994-1995; 14(1-6):395-408.
  69. Zetter BR. Adhesion molecules in tumor metastasis. Semin Cancer Biol. 1993 Aug; 4(4):219-29.
  70. Blood CH, Zetter BR. Laminin regulates a tumor cell chemotaxis receptor through the laminin-binding integrin subunit alpha 6. Cancer Res. 1993 Jun 1; 53(11):2661-6.
  71. Kantor JD, McCormick B, Steeg PS, Zetter BR. Inhibition of cell motility after nm23 transfection of human and murine tumor cells. Cancer Res. 1993 May 1; 53(9):1971-3.
  72. Rossi MC, Zetter BR. Selective stimulation of prostatic carcinoma cell proliferation by transferrin. Proc Natl Acad Sci U S A. 1992 Jul 1; 89(13):6197-201.
  73. Meininger CJ, Zetter BR. Mast cells and angiogenesis. Semin Cancer Biol. 1992 Apr; 3(2):73-9.
  74. Meininger CJ, Yano H, Rottapel R, Bernstein A, Zsebo KM, Zetter BR. The c-kit receptor ligand functions as a mast cell chemoattractant. Blood. 1992 Feb 15; 79(4):958-63.
  75. McCormick BA, Zetter BR. Adhesive interactions in angiogenesis and metastasis. Pharmacol Ther. 1992; 53(2):239-60.
  76. Chan BM, Matsuura N, Takada Y, Zetter BR, Hemler ME. In vitro and in vivo consequences of VLA-2 expression on rhabdomyosarcoma cells. Science. 1991 Mar 29; 251(5001):1600-2.
  77. Zetter BR, Brightman SE. Cell motility and the extracellular matrix. Curr Opin Cell Biol. 1990 Oct; 2(5):850-6.
  78. Zetter BR. The cellular basis of site-specific tumor metastasis. N Engl J Med. 1990 Mar 1; 322(9):605-12.
  79. Zetter BR. Cell motility in angiogenesis and tumor metastasis. Cancer Invest. 1990; 8(6):669-71.
  80. Yusa T, Blood CH, Zetter BR. Tumor cell interactions with elastin: implications for pulmonary metastasis. Am Rev Respir Dis. 1989 Nov; 140(5):1458-62.
  81. Matsuura N, Zetter BR. Stimulation of mast cell chemotaxis by interleukin 3. J Exp Med. 1989 Oct 1; 170(4):1421-6.
  82. Chackal-Roy M, Niemeyer C, Moore M, Zetter BR. Stimulation of human prostatic carcinoma cell growth by factors present in human bone marrow. J Clin Invest. 1989 Jul; 84(1):43-50.
  83. Blood CH, Zetter BR. Membrane-bound protein kinase C modulates receptor affinity and chemotactic responsiveness of Lewis lung carcinoma sublines to an elastin-derived peptide. J Biol Chem. 1989 Jun 25; 264(18):10614-20.
  84. Blood CH, Sasse J, Brodt P, Zetter BR. Identification of a tumor cell receptor for VGVAPG, an elastin-derived chemotactic peptide. J Cell Biol. 1988 Nov; 107(5):1987-93.
  85. Silverman KJ, Lund DP, Zetter BR, Lainey LL, Shahood JA, Freiman DG, Folkman J, Barger AC. Angiogenic activity of adipose tissue. Biochem Biophys Res Commun. 1988 May 31; 153(1):347-52.
  86. Zetter BR. Angiogenesis. State of the art. Chest. 1988 Mar; 93(3 Suppl):159S-166S.
  87. Chung DC, Zetter BR, Brodt P. Lewis lung carcinoma variants with differing metastatic specificities adhere preferentially to different defined extracellular matrix molecules. Invasion Metastasis. 1988; 8(2):103-17.
  88. Sitaras NM, Sariban E, Pantazis P, Zetter B, Antoniades HN. Human iliac artery endothelial cells express both genes encoding the chains of platelet-derived growth factor (PDGF) and synthesize PDGF-like mitogen. J Cell Physiol. 1987 Aug; 132(2):376-80.
  89. Tobias JW, Bern MM, Netland PA, Zetter BR. Monocyte adhesion to subendothelial components. Blood. 1987 Apr; 69(4):1265-8.
  90. Zetter BR. Assay of capillary endothelial cell migration. Methods Enzymol. 1987; 147:135-44.
  91. Netland PA, Zetter BR. Melanoma cell adhesion to defined extracellular matrix components. Biochem Biophys Res Commun. 1986 Sep 14; 139(2):515-22.
  92. Netland PA, Zetter BR, Via DP, Voyta JC. In situ labelling of vascular endothelium with fluorescent acetylated low density lipoprotein. Histochem J. 1985 Dec; 17(12):1309-20.
  93. Netland PA, Zetter BR. Metastatic potential of B16 melanoma cells after in vitro selection for organ-specific adherence. J Cell Biol. 1985 Sep; 101(3):720-4.
  94. Zetter BR, Rasmussen N, Brown L. An in vivo assay for chemoattractant activity. Lab Invest. 1985 Sep; 53(3):362-8.
  95. Voyta JC, Via DP, Butterfield CE, Zetter BR. Identification and isolation of endothelial cells based on their increased uptake of acetylated-low density lipoprotein. J Cell Biol. 1984 Dec; 99(6):2034-40.
  96. Makris A, Ryan KJ, Yasumizu T, Hill CL, Zetter BR. The nonluteal porcine ovary as a source of angiogenic activity. Endocrinology. 1984 Nov; 115(5):1672-7.
  97. Netland PA, Zetter BR. Organ-specific adhesion of metastatic tumor cells in vitro. Science. 1984 Jun 8; 224(4653):1113-5.
  98. Poole TJ, Zetter BR. Stimulation of rat peritoneal mast cell migration by tumor-derived peptides. Cancer Res. 1983 Dec; 43(12 Pt 1):5857-61.
  99. Tapper D, Albert DM, Robinson NL, Zetter BR. Capillary endothelial cell migration: stimulating activity of aqueous humor from patients with ocular cancers. J Natl Cancer Inst. 1983 Sep; 71(3):501-5.
  100. Azizkhan J, Sullivan R, Azizkhan R, Zetter BR, Klagsbrun M. Stimulation of increased capillary endothelial cell motility by chondrosarcoma cell-derived factors. Cancer Res. 1983 Jul; 43(7):3281-6.
  101. Buzney SM, Massicotte SJ, Hetu N, Zetter BR. Retinal vascular endothelial cells and pericytes. Differential growth characteristics in vitro. Invest Ophthalmol Vis Sci. 1983 Apr; 24(4):470-80.
  102. Glassberg MK, Bern MM, Coughlin SR, Haudenschild CC, Hoyer LW, Antoniades HN, Zetter BR. Cultured endothelial cells derived from the human iliac arteries. In Vitro. 1982 Oct; 18(10):859-66.
  103. Mulliken JB, Zetter BR, Folkman J. In vitro characteristics of endothelium from hemangiomas and vascular malformations. Surgery. 1982 Aug; 92(2):348-53.
  104. Bernstein LR, Antoniades H, Zetter BR. Migration of cultured vascular cells in response to plasma and platelet-derived factors. J Cell Sci. 1982 Aug; 56:71-82.
  105. Lopez R, Rand LI, Zetter BR. Absence of mast cells in diabetic retinopathy. Microvasc Res. 1982 Jul; 24(1):87-93.
  106. Chodak GW, Scheiner CJ, Zetter BR. Urine from patients with transitional-cell carcinoma stimulates migration of capillary endothelial cells. N Engl J Med. 1981 Oct 8; 305(15):869-74.
  107. Tapper D, Scheiner C, Frissora H, Zetter B. The stimulation of capillary endothelial cell migration by aqueous humor. J Surg Res. 1981 Mar; 30(3):262-8.
  108. Zetter BR. The endothelial cells of large and small blood vessels. Diabetes. 1981; 30(Suppl 2):24-8.
  109. Coughlin SR, Moskowitz MA, Zetter BR, Antoniades HN, Levine L. Platelet-dependent stimulation of prostacyclin synthesis by platelet-derived growth factor. Nature. 1980 Dec 11; 288(5791):600-2.
  110. Azizkhan RG, Azizkhan JC, Zetter BR, Folkman J. Mast cell heparin stimulates migration of capillary endothelial cells in vitro. J Exp Med. 1980 Oct 1; 152(4):931-44.
  111. Brouty-Boyé D, Zetter BR. Inhibition of cell motility by interferon. Science. 1980 May 2; 208(4443):516-8.
  112. Zetter BR. Migration of capillary endothelial cells is stimulated by tumour-derived factors. Nature. 1980 May 1; 285(5759):41-3.
  113. Folkman J, Haudenschild CC, Zetter BR. Long-term culture of capillary endothelial cells. Proc Natl Acad Sci U S A. 1979 Oct; 76(10):5217-21.
  114. Zetter BR, Daniels TE, Quadra-White C, Greenspan JS. LETS protein in normal and pathological human oral epithelium. J Dent Res. 1979 Jan; 58(1):484-8.
  115. Zetter BR, Antoniades HN. Stimulation of human vascular endothelial cell growth by a platelet-derived growth factor and thrombin. J Supramol Struct. 1979; 11(3):361-70.
  116. Zetter BR, Johnson LK, Shuman MA, Gospodarowicz D. The isolation of vascular endothelial cell lines with altered cell surface and platelet-binding properties. Cell. 1978 Jul; 14(3):501-9.
  117. Buchanan JM, Chen LB, Zetter BR. Are high-molecular-weight glycoproteins regulators of cellular growth? Ann N Y Acad Sci. 1978 Jun 20; 312:293-8.
  118. Zetter BR, Martin GR, Birdwell CR, Gospodarowicz D. Role of the high-molecular-weight glycoprotein in cellular morphology, adhesion, and differentiation. Ann N Y Acad Sci. 1978 Jun 20; 312:299-316.
  119. Gospodarowicz D, Brown KD, Birdwell CR, Zetter BR. Control of proliferation of human vascular endothelial cells. Characterization of the response of human umbilical vein endothelial cells to fibroblast growth factor, epidermal growth factor, and thrombin. J Cell Biol. 1978 Jun; 77(3):774-88.
  120. Zetter BR, Martin GR. Expression of a high molecular weight cell surface glycoprotein (LETS protein) by preimplantation mouse embryos and teratocarcinoma stem cells. Proc Natl Acad Sci U S A. 1978 May; 75(5):2324-8.
  121. Zetter BR, Chen LB, Buchanan JM. Mitogenic response of cells in tissue culture to thrombin. Natl Cancer Inst Monogr. 1978 May; (48):157-65.
  122. Gospodarowicz D, Greenburg G, Bialecki H, Zetter BR. Factors involved in the modulation of cell proliferation in vivo and in vitro: the role of fibroblast and epidermal growth factors in the proliferative response of mammalian cells. In Vitro. 1978 Jan; 14(1):85-118.
  123. Zetter BR, Sun TT, Chen LB, Buchanan JM. Thrombin potentiates the mitogenic response of cultured fibroblasts to serum and other growth promoting agents. J Cell Physiol. 1977 Aug; 92(2):233-9.
  124. Zetter BR, Chen LB, Buchanan JM. Binding and internalization of thrombin by normal and transformed chick cells. Proc Natl Acad Sci U S A. 1977 Feb; 74(2):596-600.
  125. Gospodarowicz D, Zetter BR. The use of fibroblast and epidermal growth factors to lower the serum requirement for growth of normal diploid cells in early passage: a new method for cloning. Dev Biol Stand. 1976 Dec 13-15; 37:109-30.
  126. Zetter BR, Chen LB, Buchanan JM. Effects of protease treatment on growth, morphology, adhesion, and cell surface proteins of secondary chick embryo fibroblasts. Cell. 1976 Mar; 7(3):407-12.
  127. Zetter BR, Cohen PS. Post-transcriptional regulation of T4 enzyme synthesis. Arch Biochem Biophys. 1974 Jun; 162(2):560-7.
  128. Cohen PS, Zetter BR, Walsh ML. Evidence that more deoxynucleotide kinase mRNA is transcribed than translated during T4 infection of Escherichia coli. Virology. 1972 Sep; 49(3):808-10.
  129. Yang W, Cai Q, Lui VW, Everley PA, Kim J, Bhola N, Quesnelle KM, Zetter BR, Steen H, Freeman MR, Grandis JR. Quantitative proteomics analysis reveals molecular networks regulated by epidermal growth factor receptor level in head and neck cancer. J Proteome Res. 2010 Jun 4; 9(6):3073-82.
  130. Kundra V, Anand-Apte B, Feig LA, Zetter BR. The chemotactic response to PDGF-BB: evidence of a role for Ras. J Cell Biol. 1995 Aug; 130(3):725-31.
  131. Hemler ME, Elices MJ, Chan BM, Zetter B, Matsuura N, Takada Y. Multiple ligand binding functions for VLA-2 (alpha 2 beta 1) and VLA-3 (alpha 3 beta 1) in the integrin family. Cell Differ Dev. 1990 Dec 2; 32(3):229-38.
  132. Yoshida A, Anand-Apte B, Zetter BR. Differential endothelial migration and proliferation to basic fibroblast growth factor and vascular endothelial growth factor. Growth Factors. 1996; 13(1-2):57-64.
  133. Claesson-Welsh L, Welsh M, Ito N, Anand-Apte B, Soker S, Zetter B, O'Reilly M, Folkman J. Angiostatin induces endothelial cell apoptosis and activation of focal adhesion kinase independently of the integrin-binding motif RGD. Proc Natl Acad Sci U S A. 1998 May 12; 95(10):5579-83.
  134. Banyard J, Barrows C, Zetter BR. Differential regulation of human thymosin beta 15 isoforms by transforming growth factor beta 1. Genes Chromosomes Cancer. 2009 Jun; 48(6):502-9.
  135. Feldman AS, Banyard J, Wu CL, McDougal WS, Zetter BR. Cystatin B as a tissue and urinary biomarker of bladder cancer recurrence and disease progression. Clin Cancer Res. 2009 Feb 1; 15(3):1024-31.
  136. Anand-Apte B, Zetter BR, Viswanathan A, Qiu RG, Chen J, Ruggieri R, Symons M. Platelet-derived growth factor and fibronectin-stimulated migration are differentially regulated by the Rac and extracellular signal-regulated kinase pathways. J Biol Chem. 1997 Dec 5; 272(49):30688-92.
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  143. Iordanescu I, Becker C, Zetter B, Dunning P, Taylor GA. Tumor vascularity: evaluation in a murine model with contrast-enhanced color Doppler US effect of angiogenesis inhibitors. Radiology. 2002 Feb; 222(2):460-7.
  144. Blood CH, Zetter BR. Tumor interactions with the vasculature: angiogenesis and tumor metastasis. Biochim Biophys Acta. 1990 Jun 1; 1032(1):89-118.
  145. Mu CJ, Lavan DA, Langer RS, Zetter BR. Self-assembled gold nanoparticle molecular probes for detecting proteolytic activity in vivo. ACS Nano. 2010 Mar 23; 4(3):1511-20.
  146. Banyard J, Chung I, Wilson AM, Vetter G, Le Béchec A, Bielenberg DR, Zetter BR. Regulation of epithelial plasticity by miR-424 and miR-200 in a new prostate cancer metastasis model. Sci Rep. 2013 Nov 06; 3:3151.
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