Breast cancer cells secreted platelet-derived growth factor-induced motility of vascular smooth muscle cells is mediated through neuropilin-1

Molecular Carcinogenesis

Volumn 45, Issue 11, 2006, Pages 871-880

  Banerjee, Snigdha ^a,b   Sengupta, Krishanu ^a,b   Dhar, Kakali ^a,b   Mehta, Smita ^a,b   D'Amore, Patricia A ^c   Dhar, Gopal ^a,b   Banerjee, Sushanta K ^a,b  

^a VA Medical Center   (United States)

^b UNIVERSITY OF KANSAS SCHOOL OF MEDICINE   (United States)

^c SCHEPENS EYE RESEARCH INSTITUTE   (United States)

Author keywords

Breast tumor cells; Cell cell interactions; Motility; NRP 1; PDGF; Vascular smooth muscle cells

Indexed keywords

NEUROPILIN 1; PLATELET DERIVED GROWTH FACTOR; SHORT HAIRPIN RNA;

ANIMAL CELL; AORTA; ARTICLE; BREAST CANCER; CANCER CELL; CELL INTERACTION; CELL MIGRATION; CELL MOTILITY; CELL STRAIN MCF 7; CELL STRAIN MDA MB 231; CONTROLLED STUDY; GENE EXPRESSION; HUMAN; HUMAN CELL; NONHUMAN; PRIORITY JOURNAL; PROTEIN PROTEIN INTERACTION; SMOOTH MUSCLE FIBER; UPREGULATION; VASCULAR SMOOTH MUSCLE;

BASE SEQUENCE; BREAST NEOPLASMS; CELL LINE, TUMOR; CELL MOVEMENT; CELLS, CULTURED; CULTURE MEDIA, CONDITIONED; DNA PRIMERS; HUMANS; MUSCLE, SMOOTH, VASCULAR; NEUROPILIN-1; PLATELET-DERIVED GROWTH FACTOR; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION;

EID: 33750457687     PISSN: 08991987     EISSN: 10982744     Source Type: Journal    
DOI: 10.1002/mc.20248     Document Type: Article

References (65)

1. Folkman J, Shing Y. Angiogenesis. J Biol Chem 1992;267:10931-10934.
2. Hanahan D, Folkman J. Patterns and emerging mechanisms of the angiogenic switch during tumorigenesis. Cell 1996;86:353-364.
3. Folkman J. Tumor angiogenesis. Adv Cancer Res 1985;43:175-203.
4. Folkman J. The vascularization of tumors. Sci Am 1976;234:234-258.
5. Banerjee SK, Islam A, Banerjee S. The regulatory roles of estrogen in carcinogenesis: An Overview In: Preuss HG, Bagchi D, editors. Phytopharmaceuticals in cancer chemoprevention and therapy. Boca Raton, FL: CRC Press; 2005.
6. Bergers G, Benjamin LE. Tumorigenesis and the angiogenic switch. Nat Rev Cancer 2003;3:401-410.
7. Ross R. The pathogenesis of atherosclerosis: A perspective for the 1990s. Nature 1993;362:801-809.
8. Schwartz SM, Liaw L. Growth control and morphogenesis in the development and pathology of arteries. J Cardiovasc Pharmacol 1993;21:S31-S49.
9. Hirschi KK, D'Amore PA. Pericytes in the microvasculature. Cardiovasc Res 1996;32:687-698.
10. D'Amore PA, Shima DT. Tumor angiogenesis: A physiological process or genetically determined? Cancer Metastasis Rev 1996;15:205-212.
11. Drake CJ, Hungerford JE, Little CD. Morphogenesis of the first blood vessels. Ann N Y Acad Sci 1998;857:155-179.
12. Bergers G, Benjamin LE. Angiogenesis: Tumorigenesis and the angiogenic switch. Nat Rev Cancer 2003;3:401-410.
13. Benjamin LE, Hemo I, Keshet E. A plasticity window for blood vessel remodelling is defined by pericyte coverage of the preformed endothelial network and is regulated by PDGF-B and VEGF. Development 1998;125:1591-1598.
14. Hellstrom M, Kalen M, Lindahl P, Abramsson A, Betsholtz C. Role of PDGF-B and PDGFR-beta in recruitment of vascular smooth muscle cells and pericytes during embryonic blood vessel formation in the mouse. Development 1999;126:3047-3055.
15. Lindahl P, Bostrom H, Karlsson L, Hellstrom M, Kalen M, Betsholtz C. Role of platelet-derived growth factors in angiogenesis and alveogenesis. Curr Top Pathol 1999;93:27-33.
16. Grosskreutz CL, nand-Apte B, Duplaa C, et al. Vascular endothelial growth factor-induced migration of vascular smooth muscle cells in vitro. Microvasc Res 1999;58:128-136.
17. Heydarkhan-Hagvall S, Helenius G, Johansson BR, Li JY, Mattsson E, Risberg B. Co-culture of endothelial cells and smooth muscle cells affects gene expression of angiogenic factors. J Cell Biochem 2003;89:1250-1259.
18. Axel DI, Riessen R, Athanasiadis A, Runge H, Koveker G, Karsch KR. Growth factor expression of human arterial smooth muscle cells and endothelial cells in a transfilter coculture system. J Mol Cell Cardiol 1997;29:2967-2978.
19. Heldin CH, Westermark B. Growth factors: Mechanism of action and relation to oncogenes. Cell 1984;37:9-20.
20. Heldin CH, Westermark B, Wasteson A. Platelet-derived growth factor in normal and malignant cell growth. Nord Med 1984;99:319-322.
21. Westermark B, Heldin CH. Platelet-derived growth factor. Structure, function and implications in normal and malignant cell growth. Acta Oncol 1993;32:101-105.
22. Rozengurt E, Sinnett-Smith J, Taylor-Papadimitriou J. Production of PDGF-like growth factor by breast cancer cell lines. Int J Cancer 1985;36:247-252.
23. Ariad S, Seymour L, Bezwoda WR. Platelet-derived growth factor (PDGF) in plasma of breast cancer patients: Correlation with stage and rate of progression. Breast Cancer Res Treat 1991;20:11-17.
24. Shao ZM, Nguyen M, Barsky SH. Human breast carcinoma desmoplasia is PDGF initiated. Oncogene 2000;19:4337-4345.
25. Bronzert DA, Pantazis P, Antoniades HN, et al. Synthesis and secretion of platelet-derived growth factor by human breast cancer cell lines. Proc Natl Acad Sci USA 1987;84:5763-5767.
26. Lee P, Goishi K, Davidson AJ, Mannix R, Zon L, Klagsbrun M. Neuropilin-1 is required for vascular development and is a mediator of VEGF-dependent angiogenesis in zebrafish. Proc Natl Acad Sci USA 2002;99:10470-10475.
27. 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.
28. Miao HQ, Klagsbrun M. Neuropilin is a mediator of angiogenesis. Cancer Metastasis Rev 2000;19:29-37.
29. Ortega N, Hutchings H, Plouet J. Signal relays in the VEGF system. Front Biosci 1999;4:0141-0152.
30. 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.
31. Stephenson JM, Banerjee S, Saxena NK, Cherian R, Banerjee SK. Neuropilin-1 is differentially expressed in myoepithelial cells and vascular smooth muscle cells in preneoplastic and neoplastic human breast: A possible marker for the progression of breast cancer. Int J Cancer 2002;101:409-414.
32. Wang L, Zeng H, Wang P, Soker S, Mukhopadhyay D. Neuropilin-1-mediated vascular permeability factor/vascular endothelial growth factor-dependent endothelial cell migration. J Biol Chem 2003;278:48848-48860.
33. Bernatchez PN, Rollin S, Soker S, Sirois MG. Relative effects of VEGF-A and VEGF-C on endothelial cell proliferation, migration and PAF synthesis: Role of neuropilin-1. J Cell Biochem 2002;85:629-639.
34. Neufeld G, Kessler O, Herzog Y. The interaction of Neuropilin-1 and Neuropilin-2 with tyrosine-kinase receptors for VEGF. Adv Exp Med Biol 2002;515:81-90.
35. Banerjee S, Saxena N, Sengupta K, Tawfik O, Mayo MS, Banerjee SK. WISP-2 gene in human breast cancer: Estrogen and progesterone inducible expression and regulation of tumor cell proliferation. Neoplasia 2003;5:63-73.
36. Banerjee S, Sengupta K, Saxena NK, Dhar K, Banerjee SK. Epidermal growth factor induces WISP-2/CCN5 expression in Estrogen Receptor-{alpha}-Positive Breast Tumor. Cells through Multiple Molecular Cross-talks. Mol Cancer Res 2005;3:151-162.
37. Sengupta K, Banerjee S, Saxena NK, Jonathan NB, Campbell DR, Banerjee SK. Differential expression of VEGF-A mRNA by 17beta-estradiol in breast tumor cells lacking classical ER-alpha may be mediated through a variant form of ER-alpha. Mol Cell Biochem 2004;262:215-224.
38. Dickson RB, Lippman ME. Growth factors in breast cancer. Endocr Rev 1995;16:559-589.
39. Lippman ME, Dickson RB, Gelmann EP, et al. Growth regulation of human breast carcinoma occurs through regulated growth factor secretion. J Cell Biochem 1987;35:1-16.
40. Heidaran MA, Pierce JH, Yu JC, et al. Role of alpha beta receptor heterodimer formation in beta platelet-derived growth factor (PDGF) receptor activation by PDGF-AB. J Biol Chem 1991;266:20232-20237.
41. Witmer AN, Vrensen GF, Van Noorden CJ, Schlingemann RO, Vascular endothelial growth factors and angiogenesis in eye disease. Prog Retin Eye Res 2003;22:1-29.
42. Grotendorst GR, Chang T, Seppa HE, Kleinman HK, Martin GR. Platelet-derived growth factor is a chemoattractant for vascular smooth muscle cells. J Cell Physiol 1982;113:261-266.
43. Cospedal R, Abedi H, Zachary I. Platelet-derived growth factor-BB (PDGF-BB) regulation of migration and focal adhesion kinase phosphorylation in rabbit aortic vascular smooth muscle cells: Roles of phosphatidylinositol 3-kinase and mitogen-activated protein kinases. Cardiovasc Res 1999;41:708-721.
44. Hughes AD, Clunn GF, Refson J, moliou-Mason C. Platelet-derived growth factor (PDGF): Actions and mechanisms in vascular smooth muscle. Gen Pharmacol 1996;27:1079-1089.
45. Zempo N, Koyama N, Kenagy RD, Lea HJ, Clowes AW. Regulation of vascular smooth muscle cell migration and proliferation in vitro and in injured rat arteries by a synthetic matrix metalloproteinase inhibitor. Arterioscler Thromb Vasc Biol 1996;16:28-33.
46. Grosskreutz CL, nand-Apte B, Duplaa C, et al. Vascular endothelial growth factor-induced migration of vascular smooth muscle cells in vitro. Microvasc Res 1999;58:128-136.
47. Lyden D, Hattori K, Dias S, et al. Impaired recruitment of bone-marrow-derived endothelial and hematopoietic precursor cells blocks tumor angiogenesis and growth. Nat Med 2001;7:1194-1201.
48. Plate KH, Breier G, Weich HA, Risau W. Vascular endothelial growth factor is a potential tumour angiogenesis factor in human gliomas in vivo. Nature 1992;359:845-848.
49. Myoken Y, Kayada Y, Okamoto T, Kan M, Sato GH, Sato JD. Vascular endothelial growth factor (VEGF) produced by A-431 human epidermoid carcinoma cells and identification of VEGF membrane binding sites. Proc Natl Acad Sci 1991;88:5819-5823.
50. Betsholtz C, Karlsson L, Lindahl P. Developmental roles of platelet-derived growth factors. Bioessays 2001;23:494-507.
51. Morikawa S, Baluk P, Kaidoh T, Haskell A, Jain RK, McDonald DM. Abnormalities in pericytes on blood vessels and endothelial sprouts in tumors. Am J Pathol 2002;160:985-1000.
52. Jain RK. Molecular regulation of vessel maturation. Nat Med 2003;9:685-693.
53. Jain RK, Booth MF. What brings pericytes to tumor vessels? J Clin Invest 2003;112:1134-1136.
54. Carmeliet P. Angiogenesis in health and disease. Nat Med 2003;9:653-660.
55. Nicosia RF, Villaschi S. Rat aortic smooth muscle cells become pericytes during angiogenesis in vitro. Lab Invest 1995;73:658-666.
56. Lindahl P, Johansson BR, Leveen P, Betsholtz C. Pericyte loss and microaneurysm formation in PDGF-B-deficient mice. Science 1997;277:242-245.
57. Beck L, Jr., D'Amore PA. Vascular development: Cellular and molecular regulation. FASEB J 1997;11:365-373.
58. Sato Y, Asada Y, Marutsuka K, Hatakeyama K, Sumiyoshi A. Tissue factor induces migration of cultured aortic smooth muscle cells. Thromb Haemost 1996;75:389-392.
59. Casscells W. Smooth muscle cell growth factors. Prog Growth Factor Res 1991;3:177-206.
60. Wang H, Keiser JA. Vascular endothelial growth factor upregulates the expression of matrix metalloproteinases in vascular smooth muscle cells: Role of flt-1. Circ Res 1998;83:832-840.
61. Witmer AN, Vrensen GF, Van Noorden CJ, Schlingemann RO. Vascular endothelial growth factors and angiogenesis in eye disease. Prog Retin Eye Res 2003;22:1-29.
62. Grotendorst GR, Chang T, Seppa HE, Kleinman HK, Martin GR. Platelet-derived growth factor is a chemoattractant for vascular smooth muscle cells. J Cell Physiol 1982;113:261-266.
63. Cospedal R, Abedi H, Zachary I. Platelet-derived growth factor-BB (PDGF-BB) regulation of migration and focal adhesion kinase phosphorylation in rabbit aortic vascular smooth muscle cells: Roles of phosphatidylinositol 3-kinase and mitogen-activated protein kinases. Cardiovasc Res 1999;41:708-721.
64. Hughes AD, Clunn GF, Refson J, moliou-Mason C. Platelet-derived growth factor (PDGF): Actions and mechanisms in vascular smooth muscle. Gen Pharmacol 1996;27:1079-1089.
65. Grosskreutz CL, nand-Apte B, Duplaa C, et al. Vascular endothelial growth factor-induced migration of vascular smooth muscle cells in vitro. Microvasc Res 1999;58:128-136.