Platelet-Derived Growth Factor Production by B16 Melanoma Cells Leads to Increased Pericyte Abundance in Tumors and an Associated Increase in Tumor Growth Rate

Cancer Research

Volumn 64, Issue 8, 2004, Pages 2725-2733

  Furuhashi, Masao ^a   Sjöblom, Tobias ^a,c   Abramsson, Alexandra ^b   Ellingsen, Jens ^a   Micke, Patrick ^a   Li, Hong ^a   Bergsten Folestad, Erika ^a   Eriksson, Ulf ^a   Heuchel, Rainer ^a   Betsholtz, Christer ^b   Heldin, Carl Henrik ^a   Östman, Arne ^a  

^a LUDWIG INSTITUTE FOR CANCER RESEARCH   (Sweden)

^b UNIVERSITY OF GOTHENBURG   (Sweden)

^c JOHNS HOPKINS UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

PLATELET DERIVED GROWTH FACTOR; PLATELET DERIVED GROWTH FACTOR BB; PLATELET DERIVED GROWTH FACTOR BETA RECEPTOR; PLATELET DERIVED GROWTH FACTOR DD; UNCLASSIFIED DRUG;

ANGIOGENESIS; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; AUTOCRINE EFFECT; CELL PROLIFERATION; CONTROLLED STUDY; FIBROBLAST; GROWTH RATE; MELANOMA B16; MOUSE; NONHUMAN; PARACRINE SIGNALING; PERICYTE; PRIORITY JOURNAL; PROTEIN SYNTHESIS; SIGNAL TRANSDUCTION; SOLID TUMOR; TUMOR GROWTH;

ANIMALS; APOPTOSIS; CELL DIVISION; CELL LINE, TUMOR; ENDOTHELIUM, VASCULAR; LYMPHOKINES; MELANOMA, EXPERIMENTAL; MICE; MICE, INBRED C57BL; NEOVASCULARIZATION, PATHOLOGIC; PLATELET-DERIVED GROWTH FACTOR; RECEPTOR, PLATELET-DERIVED GROWTH FACTOR BETA;

EID: 16544382996     PISSN: 00085472     EISSN: None     Source Type: Journal    
DOI: 10.1158/0008-5472.CAN-03-1489     Document Type: Article

References (49)

1. Heldin C-H, Östman A, Rönnstrand L. Signal transduction via platelet-derived growth factor receptors. Biochim Biophys Acta 1998;1378:F79-113.
2. Pietras K, Sjöblom T, Rubin K, Heldin C-H, Östman A. PDGF receptors as cancer drug targets. Cancer Cell 2003;3:439-43.
3. Buchdunger E, Zimmermann J, Mett H, et al. Inhibition of the Abl protein-tyrosine kinase in vitro and in vivo by a 2-phenylaminopyrimidine derivative. Cancer Res 1996;56:100-4.
4. Östman A, Heldin C-H. Involvement of platelet-derived growth factor in disease: development of specific antagonists. Adv Cancer Res 2001;80:1-38.
5. Capdeville R, Buchdunger E, Zimmermann J, Matter A. Glivec (STI571, imatinib), a rationally developed, targeted anticancer drug. Nat Rev Drug Discov 2002;1:493-502.
6. Bergsten E, Uutela M, Li X, et al. PDGF-D is a specific, protease-activated ligand for the PDGF β-receptor. Nat Cell Biol 2001;3:512-6.
7. LaRochelle WJ, Jeffers M, McDonald WF, et al. PDGF-D, a new protease-activated growth factor. Nat Cell Biol 2001;3:517-21.
8. Li X, Pontén A, Aase K, et al. PDGF-C is a new protease-activated ligand for the PDGF α-receptor. Nat Cell Biol 2000;2:302-9.
9. Heldin C-H, Westermark B. Mechanism of action and in vivo role of platelet-derived growth factor. Physiol Rev 1999;79:1283-316.
10. Gilbertson DG, Duff ME, West JW, et al. Platelet-derived growth factor C (PDGF-C), a novel growth factor that binds to PDGF α and β receptor. J Biol Chem 2001;276:27406-14.
11. Sjöblom T, Shimizu A, O'Brien KP, et al. Growth inhibition of dermatofibrosarcoma protuberans tumors by the platelet-derived growth factor receptor antagonist STI571 through induction of apoptosis. Cancer Res 2001;61:5778-83.
12. Greco A, Fusetti L, Villa R, et al. Transforming activity of the chimeric sequence formed by the fusion of collagen gene COL1A1 and the platelet derived growth factor b-chain gene in dermatofibrosarcoma protuberans. Oncogene 1998;17:1313-9.
13. Kilic T, Alberta JA, Zdunek PR, et al. Intracranial inhibition of platelet-derived growth factor-mediated glioblastoma cell growth by an orally active kinase inhibitor of the 2-phenylaminopyrimidine class. Cancer Res 2000;60:5143-50.
14. Shamah SM, Stiles CD, Guha A. Dominant-negative mutants of platelet-derived growth factor revert the transformed phenotype of human astrocytoma cells. Mol Cell Biol 1993;13:7203-12.
15. Shimizu A, O'Brien KP, Sjöblom T, et al. The dermatofibrosarcoma protuberans-associated collagen type 1α1/platelet-derived growth factor (PDGF) B-chain fusion gene generates a transforming protein that is processed to functional PDGF-BB. Cancer Res 1999;59:3719-23.
16. Maki RG, Awan RA, Dixon RH, Jhanwar S, Antonescu CR. Differential sensitivity to imatinib of 2 patients with metastatic sarcoma arising from dermatofibrosarcoma protuberans. Int J Cancer 2002;100:623-6.
17. Rubin BP, Schuetze SM, Eary JF, et al. Molecular targeting of platelet-derived growth factor B by imatinib mesylate in a patient with metastatic dermatofibrosarcoma protuberans. J Clin Oncol 2002;20:3586-91.
18. Skobe M, Fusenig NE. Tumorigenic conversion of immortal human keratinocytes through stromal cell activation. Proc Natl Acad Sci USA 1998;95:1050-5.
19. Forsberg K, Valyi-Nagy I, Heldin, C-H, Herlyn M, Westermark B. Platelet-derived growth factor (PDGF) in oncogenesis: development of a vascular connective tissue stroma in xenotransplanted human melanoma producing PDGF-BB. Proc Natl Acad Sci USA 1993;90:393-7.
20. Pietras K, Östman A, Sjöquist M, et al. Inhibition of platelet-derived growth factor receptors reduces interstitial hypertension and increases transcapillary transport in tumors. Cancer Res 2001;61:2929-34.
21. Pietras K, Rubin K, Sjöblom T, et al. Inhibition of PDGF receptor signaling in tumor stroma enhances antitumor effect of chemotherapy. Cancer Res 2002;62:5476-84.
22. Pietras K, Stumm M, Hubert M, et al. STI571 enhances the therapeutic index of epothilone B (EPO906) by a tumor-selective increase of drug uptake. Clin Cancer Res 2003;9:3779-87.
23. Battegay EJ, Rupp J, Iruela-Arispe L, Sage EH, Pech M. PDGF-BB modulates endothelial proliferation and angiogenesis in vitro via PDGF β-receptors. J Cell Biol 1994;125:917-28.
24. Risau W, Drexler H, Mironov V, et al. Platelet-derived growth factor is angiogenic in vivo. Growth Factors 1992;7:261-6.
25. Cao R, Bråkenhielm E, Li X, et al. Angiogenesis stimulated by PDGF-CC, a novel member in the PDGF family, involves activation of PDGFR-αα and -αβ receptors. FASEB J 2002;16:1575-83.
26. Lindahl P, Johansson BR, Levéen P, Betsholtz C. Pericyte loss and microaneurysm formation in PDGF-B-deficient mice. Science (Wash DC) 1997;277:242-5.
27. Hellström M, Kalén M, Lindahl P, Abramsson A, Betsholtz C. Role of PDGF-B and PDGFR-β in recruitment of vascular smooth muscle cells and pericytes during embryonic blood vessel formation in the mouse. Development 1999;126:3047-55.
28. Enge M, Bjarnegard M, Gerhardt H, et al. Endothelium-specific platelet-derived growth factor-B ablation mimics diabetic retinopathy. EMBO J 2002;21:4307-16.
29. Sundberg C, Ljungström M, Lindmark G, Gerdin B, Rubin K. Microvascular pericytes express platelet-derived growth factor-β receptors in human healing wounds and colorectal adenocarcinoma. Am J Pathol 1993;143:1377-88.
30. Abramsson A, Berlin O, Papayan H, et al. Analysis of mural cell recruitment to tumor vessels. Circulation 2002;105:112-7.
31. Hermanson M, Funa K, Hartman M, et al. Platelet-derived growth factor and its receptors in human glioma tissue: expression of messenger RNA and protein suggests the presence of autocrine and paracrine loops. Cancer Res 1992;52:3213-9.
32. Uehara H, Kim SJ, Karashima T, et al. Effects of blocking platelet-derived growth factor-receptor signaling in a mouse model of experimental prostate cancer bone metastases. J Natl Cancer Inst (Bethesda) 2003;95:458-70.
33. Guo P, Hu B, Gu W, et al. Platelet-derived growth factor-B enhances glioma angiogenesis by stimulating vascular endothelial growth factor expression in tumor endothelia and by promoting pericyte recruitment. Am J Pathol 2003;162:1083-93.
34. Li H, Fredriksson L, Li X, Eriksson U. PDGF-D is a potent transforming and angiogenic growth factor. Oncogene 2003;22:1501-10.
35. Thyberg J, Östman A, Bäckström G, Westermark B, Heldin, C-H. Localization of platelet-derived growth factor (PDGF) in CHO cells transfected with PDGF A- or B-chain cDNA: retention of PDGF-BB in the endoplasmic reticulum and Golgi complex. J Cell Sci 1990;97:219-29.
36. Workman P, Balmain A, Hickman JA, et al. UKCCCR guidelines for the welfare of animals in experimental neoplasia. Lab Anim 1988;22:195-201.
37. Heuchel R, Berg A, Tallquist M, et al. Platelet-derived growth factor β receptor regulates interstitial fluid homeostasis through phosphatidylinositol-3′ kinase signaling. Proc Natl Acad Sci USA 1999;96:11410-5.
38. Gundersen HJG, Bendtsen TF, Korbo L, et al. Some new, simple and efficient stereological methods and their use in pathological research and diagnosis. APMIS 1988;96:379-94.
39. Wassberg E, Hedborg F, Skoldenberg E, Stridsberg M, Christofferson R. Inhibition of angiogenesis induces chromaffin differentiation and apoptosis in neuroblastoma. Am J Pathol 1999;154:395-403.
40. Schlingemann RO, Rietveld FJ, de Waal RM, Ferrone S, Ruiter DJ. Expression of the high molecular weight melanoma-associated antigen by pericytes during angiogenesis in tumors and in healing wounds. Am J Pathol 1990;136:1393-405.
41. Schlingemann RO, Rietveld FJR, Kwaspen F, et al. Differential expression of markers for endothelial cells, pericytes, and basal lamina in the microvasculature of tumors and granulation tissue. Am J Pathol 138:1335-47.
42. Eberhard AI, Kahlert S, Goede V, et al. Heterogeneity of angiogenesis and blood vessel maturation in human tumors: implications for antiangiogenic therapies. Cancer Res 60:1388-93.
43. Shao Z-M, Nguyen M, Barsky SH. Human breast carcinoma desmoplasia is PDGF initiated. Oncogene 2000;19:4337-45.
44. Nicosia RF, Nicosia SV, Smith M. Vascular endothelial growth factor, platelet-derived growth factor, and insulin-like growth factor-1 promote rat aortic angiogenesis in vitro. Am J Pathol 1994;145:1023-9.
45. Abramsson A, Lindblom P, Betsholtz C. Endothelial and non-endothelial sources of PDGF-B regulate pericyte recruitment and influence vascular pattern formation in tumors. J Clin Investig 2003;112:1142-51.
46. Gee MS, Procopio WN, Makonnen S, et al. Tumor vessel development and maturation impose limits on the effectiveness of anti-vascular therapy. Am J Pathol 2003;162:183-93.
47. Benjamin LE, Golijanin D, Itin A, Pode D, Keshet E. Selective ablation of immature blood vessels in established human tumors follows vascular endothelial growth factor withdrawal. J Clin Investig 1999;103:159-65.
48. Bergers G, Song S, Meyer-Morse N, Bergsland E, Hanahan D. Benefits of targeting both pericytes and endothelial cells in the tumor vasculature with kinase inhibitors. J Clin Investig 2003;111:1287-95.
49. Erber R, Thurner A, Katsen AD, et al. Combined inhibition of VEGF- and PDGF-signaling enforces tumor vessel regression by interfering with pericyte-mediated endothelial cell survival mechanisms. FASEB J 2004;18:338-40.