Original Article

You have full text access to this OnlineOpen article

Expression and regulation of the novel vascular endothelial growth factor receptor neuropilin-1 by epidermal growth factor in human pancreatic carcinoma

  1. Alexander A. Parikh M.D.1,
  2. Wen Biao Liu M.D.2,
  3. Fan Fan M.S.2,
  4. Oliver Stoeltzing M.D.2,
  5. Niels Reinmuth M.D.2,
  6. Christiane J. Bruns M.D.2,
  7. Corazon D. Bucana Ph.D.2,
  8. Douglas B. Evans M.D.1,
  9. Lee M. Ellis M.D.1,2,†,*

Article first published online: 23 JUN 2003

DOI: 10.1002/cncr.11560

Issue

Cancer

Cancer

Volume 98, Issue 4, pages 720–729, 15 August 2003

Additional Information

How to Cite

Parikh, A. A., Liu, W. B., Fan, F., Stoeltzing, O., Reinmuth, N., Bruns, C. J., Bucana, C. D., Evans, D. B. and Ellis, L. M. (2003), Expression and regulation of the novel vascular endothelial growth factor receptor neuropilin-1 by epidermal growth factor in human pancreatic carcinoma. Cancer, 98: 720–729. doi: 10.1002/cncr.11560

Author Information

  1. 1

    Department of Surgical Oncology, The University of Texas M. D. Anderson Cancer Center, Houston, Texas

  2. 2

    Department of Cancer Biology, The University of Texas M. D. Anderson Cancer Center, Houston, Texas

  1. †

    Fax: (713) 792-4689

*Department of Surgical Oncology, Box 444, The University of Texas M. D. Anderson Cancer Center, 1515 Holcombe Boulevard, Houston, TX 77030-4009

Publication History

  1. Issue published online: 1 AUG 2003
  2. Article first published online: 23 JUN 2003
  3. Manuscript Accepted: 5 MAY 2003
  4. Manuscript Revised: 18 MAR 2003
  5. Manuscript Received: 9 DEC 2002

Funded by

  • National Institutes of Health GRANT. Grant Number: T-32 09599
  • Lustgarten Foundation
  • Lockton Fund for Pancreatic Cancer Research

SEARCH

SEARCH BY CITATION

ARTICLE TOOLS

View Full Article (HTML) Get PDF (792K)

REFERENCES

  • 1
    Takahashi Y, Kitadai Y, Bucana CD, Cleary KR, Ellis LM. Expression of vascular endothelial growth factor and its receptor, KDR, correlates with vascularity, metastasis, and proliferation of human colon cancer. Cancer Res. 1995; 55: 3964–3968.
  • 2
    Price DJ, Miralem T, Jiang S, Steinberg R, Avraham H. Role of vascular endothelial growth factor in the stimulation of cellular invasion and signaling of breast cancer cells. Cell Growth Diff. 2001; 12: 129–135.
  • 3
    Neufeld G, Cohen T, Gengrinovitch S, Poltorak Z. Vascular endothelial growth factor (VEGF) and its receptors. FASEB J. 1999; 13: 9–22.
  • 4
    Pidgeon GP, Barr MP, Harmey JH, Foley DA, Bouchier-Hayes DJ. Vascular endothelial growth factor (VEGF) upregulates BCL-2 and inhibits apoptosis in human and murine mammary adenocarcinoma cells. Br J Cancer. 2001; 85: 273–278.
  • 5
    Lacal PM, Failla CM, Pagani E, et al. Human melanoma cells secrete and respond to placenta growth factor and vascular endothelial growth factor. J Invest Dermatol. 2000; 115: 1000–1007.
  • 6
    Fujisawa H, Kitsukawa T. Receptors for collapsin/semaphorins. Curr Opin Neurobiol. 1998; 8: 587–592.
  • 7
    Soker S, Takashima S, Miao HQ, Neufeld G, Klagsbrun M. Neuropilin-1 is expressed by endothelial and tumor cells as an isoform-specific receptor for vascular endothelial growth factor. Cell. 1998; 92: 735–745.
  • 8
    Miao HQ, Klagsbrun M. Neuropilin is a mediator of angiogenesis. Cancer Metast Rev. 2000; 19: 29–37.
  • 9
    Soker S, Fidder H, Neufeld G, Klagsbrun M. Characterization of novel vascular endothelial growth factor (VEGF) receptors on tumor cells that bind VEGF165 via its exon 7-encoded domain. J Biol Chem. 1996; 271: 5761–5767.
  • 10
    Bachelder RE, Crago A, Chung J, et al. Vascular endothelial growth factor is an autocrine survival factor for neuropilin-expressing breast carcinoma cells. Cancer Res. 2001; 61: 5736–5740.
  • 11
    Latil A, Bieche I, Pesche S, et al. VEGF overexpression in clinically localized prostate tumors and neuropilin-1 overexpression in metastatic forms. Int J Cancer. 2000; 89: 167–171.
    Direct Link:
  • 12
    Miao HQ, Lee P, Lin H, Soker S, Klagsbrun M. Neuropilin-1 expression by tumor cells promotes tumor angiogenesis and progression. FASEB J. 2000; 14: 2532–2539.
  • 13
    Fakhari M, Pullirsch D, Abraham D, et al. Selective upregulation of vascular endothelial growth factor receptors neuropilin-1 and -2 in human neuroblastoma. Cancer. 2002; 94: 258–263.
    Direct Link:
  • 14
    Bruns CJ, Harbison MT, Kuniyasu H, Eue I, Fidler IJ. In vivo selection and characterization of metastatic variants from human pancreatic adenocarcinoma by using orthotopic implantation in nude mice. Neoplasia. 1999; 1: 50–62.
  • 15
    Jung YD, Nakano K, Liu W, Gallick GE, Ellis LM. Extracellular signal-regulated kinase activation is required for up-regulation of vascular endothelial growth factor by serum starvation in human colon carcinoma cells. Cancer Res. 1999; 59: 4804–4807.
  • 16
    Bruns CJ, Solorzano CC, Harbison MT, et al. Blockade of the epidermal growth factor receptor signaling by a novel tyrosine kinase inhibitor leads to apoptosis of endothelial cells and therapy of human pancreatic carcinoma. Cancer Res. 2000; 60: 2926–2935.
  • 17
    Ding H, Wu X, Roncari L, et al. Expression and regulation of neuropilin-1 in human astrocytomas. Int J Cancer. 2000; 88: 584–592.
    Direct Link:
  • 18
    Giraudo E, Primo L, Audero E, et al. Tumor necrosis factor-alpha regulates expression of vascular endothelial growth factor receptor-2 and of its co-receptor neuropilin-1 in human vascular endothelial cells. J Biol Chem. 1998; 273: 22128–22135.
  • 19
    Fuh G, Garcia KC, de Vos AM. The interaction of neuropilin-1 with vascular endothelial growth factor and its receptor flt-1. J Biol Chem. 2000; 275: 26690–26695.
  • 20
    Takahashi T, Nakamura F, Jin Z, Kalb RG, Strittmatter SM. Semaphorins A and E act as antagonists of neuropilin-1 and agonists of neuropilin-2 receptors. Nat Neurosci. 1998; 1: 487–493.
  • 21
    Kitsukawa T, Shimono A, Kawakami A, Kondoh H, Fujisawa H. Overexpression of a membrane protein, neuropilin, in chimeric mice causes anomalies in the cardiovascular system, nervous system and limbs. Development. 1995; 121: 4309–4318.
  • 22
    Gluzman-Poltorak Z, Cohen T, Herzog Y, Neufeld G. Neuropilin-2 is a receptor for the vascular endothelial growth factor (VEGF) forms VEGF-145 and VEGF-165. J Biol Chem. 2000; 275: 29922.
  • 23
    Kawasaki T, Kitsukawa T, Bekku Y, et al. A requirement for neuropilin-1 in embryonic vessel formation. Development. 1999; 126: 4895–4902.
  • 24
    Kitsukawa T, Shimizu M, Sanbo M, et al. Neuropilin-semaphorin III/D-mediated chemorepulsive signals play a crucial role in peripheral nerve projection in mice. Neuron. 1997; 19: 995–1005.
  • 25
    Tordjman R, Ortega N, Coulombel L, Plouet J, Romeo PH, Lemarchandel V. Neuropilin-1 is expressed on bone marrow stromal cells: a novel interaction with hematopoietic cells? Blood. 1999; 94: 2301–2309.
  • 26
    Soker S, Gollamudi-Payne S, Fidder H, Charmahelli H, Klagsbrun M. Inhibition of vascular endothelial growth factor (VEGF)-induced endothelial cell proliferation by a peptide corresponding to the exon 7-encoded domain of VEGF165. J Biol Chem. 1997; 272: 31582–31588.
  • 27
    Miao HQ, Soker S, Feiner L, Alonso JL, Raper JA, Klagsbrun M. Neuropilin-1 mediates collapsin-1/semaphorin III inhibition of endothelial cell motility: functional competition of collapsin-1 and vascular endothelial growth factor-165. J Cell Biol. 1999; 146: 233–242.
  • 28
    Shimoyama S, Gansauge F, Gansauge S, Negri G, Oohara T, Beger HG. Increased angiogenin expression in pancreatic cancer is related to cancer aggressiveness. Cancer Res. 1996; 56: 2703–2706.
  • 29
    Ellis LM, Takahashi Y, Fenoglio CJ, Cleary KR, Bucana CD, Evans DB. Vessel counts and vascular endothelial growth factor expression in pancreatic adenocarcinoma. Eur J Cancer. 1998; 34: 337–340.
  • 30
    Fujimoto K, Hosotani R, Wada M, et al. Expression of two angiogenic factors, vascular endothelial growth factor and platelet-derived endothelial cell growth factor in human pancreatic cancer, and its relationship to angiogenesis. Eur J Cancer. 1998; 34: 1439–1447.
  • 31
    Ikeda N, Adachi M, Taki T, et al. Prognostic significance of angiogenesis in human pancreatic cancer. Br J Cancer. 1999; 79: 1553–1563.
  • 32
    Kuehn R, Lelkes PI, Bloechle C, Niendorf A, Izbicki JR. Angiogenesis, angiogenic growth factors, and cell adhesion molecules are upregulated in chronic pancreatic diseases: angiogenesis in chronic pancreatitis and in pancreatic cancer. Pancreas. 1999; 18: 96–103.
  • 33
    Bruns CJ, Shrader M, Harbison MT, et al. Effect of the vascular endothelial growth factor receptor-2 antibody DC101 plus gemcitabine on growth, metastasis, and angiogenesis of human pancreatic cancer growing orthotopically in nude mice. Int J Cancer. 2002; 102: 101–108.
    Direct Link:
  • 34
    Goldman CK, Kim J, Wong WL, King V, Brock T, Gillespie GY. Epidermal growth factor stimulates vascular endothelial growth factor production by human malignant glioma cells: a model of glioblastoma multiforme pathophysiology. Mol Biol Cell. 1993; 4: 121–133.
  • 35
    Azuma M, Tamatani T, Fukui K, Yuki T, Yoshida H, Bando T, et al. Identification of EGF as an angiogenic factor present in conditioned medium from human salivary gland adenocarcinoma cell clones with varying degrees of metastatic potential. Cancer Lett. 1994; 84: 189–198.
  • 36
    Baker CH, Solorzano CC, Fidler IJ. Blockade of vascular endothelial growth factor receptor and epidermal growth factor receptor signaling for therapy of metastatic human pancreatic cancer. Cancer Res. 2002; 62: 1996–2003.
  • 37
    Matsuda K, Idezawa T, You XJ, Kothari NH, Fan H, Korc M. Multiple mitogenic pathways in pancreatic cancer cells are blocked by a truncated epidermal growth factor receptor. Cancer Res. 2002; 62: 5611–5617.
  • 38
    Wagner M, Cao T, Lopez ME, et al. Expression of a truncated EGF receptor is associated with inhibition of pancreatic cancer cell growth and enhanced sensitivity to cisplatinum. Int J Cancer. 1996; 68: 782–787.
    Direct Link:
  • 39
    Clarke K, Smith K, Gullick WJ, Harris AL. Mutant epidermal growth factor receptor enhances induction of vascular endothelial growth factor by hypoxia and insulin-like growth factor-1 via a PI3 kinase dependent pathway. Br J Cancer. 2001; 84: 1322–1329.
View Full Article (HTML) Get PDF (792K)