PDGF-C induces maturation of blood vessels in a model of glioblastoma and attenuates the response to anti-VEGF treatment

PLoS ONE

Volumn 4, Issue 4, 2009, Pages

  di Tomaso, Emmanuelle ^a   London, Nyall ^a,b   Fuja, Daniel ^a,c   Logie, James ^a,d   Tyrrell, James A ^a,e   Kamoun, Walid ^a   Munn, Lance L ^a   Jain, Rakesh K ^a  

^a MASSACHUSETTS GENERAL HOSPITAL   (United States)

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

^c BAYLOR COLLEGE OF MEDICINE   (United States)

^d UNIVERSITY OF EDINBURGH   (United Kingdom)

^e THOMSON REUTERS   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

MONOCLONAL ANTIBODY DC101; PLATELET DERIVED GROWTH FACTOR C; SMALL INTERFERING RNA; ANGIOGENESIS INHIBITOR; LYMPHOKINE; MONOCLONAL ANTIBODY; PLATELET DERIVED GROWTH FACTOR; PLATELET-DERIVED GROWTH FACTOR C; VASCULOTROPIN A;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BLOOD VESSEL DIAMETER; BLOOD VESSEL PERMEABILITY; BRAIN BLOOD VESSEL; CANCER CELL CULTURE; CONTROLLED STUDY; DRUG RESPONSE; GENE OVEREXPRESSION; GENETIC TRANSFECTION; GLIOBLASTOMA; HISTOPATHOLOGY; HUMAN; HUMAN CELL; INHIBITION KINETICS; MALE; MICROSCOPY; MOUSE; NEUROPATHOLOGY; NONHUMAN; NUCLEOTIDE SEQUENCE; NUDE MOUSE; PROTEIN ANALYSIS; PROTEIN FUNCTION; TUMOR VASCULARIZATION; ANIMAL; CANCER TRANSPLANTATION; CAPILLARY PERMEABILITY; DRUG ANTAGONISM; METABOLISM; NEOVASCULARIZATION (PATHOLOGY); PHYSIOLOGY; TUMOR CELL LINE; VASCULARIZATION;

MUS MUSCULUS;

ANGIOGENESIS INHIBITORS; ANIMALS; ANTIBODIES, MONOCLONAL; CAPILLARY PERMEABILITY; CELL LINE, TUMOR; GLIOBLASTOMA; HUMANS; LYMPHOKINES; MICE; MICE, NUDE; NEOPLASM TRANSPLANTATION; NEOVASCULARIZATION, PATHOLOGIC; PLATELET-DERIVED GROWTH FACTOR; VASCULAR ENDOTHELIAL GROWTH FACTOR A;

EID: 65249183165     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0005123     Document Type: Article

References (43)

1. Jain RK, di Tomaso E, Duda DG, Loeffler JS, Sorensen AG, et al. (2007) Angiogenesis in brain tumours. Nat Rev Neurosci 8: 610-622.
2. Cloughesy TF, Prados MD, Wen PY, Mikkelsen T, Abrey LE, et al. (2008) A phase II, randomized, non-comparative clinical trial of the effect of bevacizumab alone or in combination with irinotecan (CPT-11) on 6-month progression free survival in recurrent, treatment-refractory glioblastoma. J Clin Oncol 26S: abstract 2010b.
3. Vredenburgh JJ, Desjardins A, Herndon JE 2nd, Marcello J, Reardon DA, et al. (2007) Bevacizumab plus irinotecan in recurrent glioblastoma multiforme. J Clin Oncol 25: 4722-4729.
4. Batchelor TT, Sorensen AG, di Tomaso E, Zhang WT, Duda DG, et al. (2007) AZD2171, a pan-VEGF receptor tyrosine kinase inhibitor, normalizes tumor vasculature and alleviates edema in glioblastoma patients. Cancer Cell 11: 83-95.
5. George D (2003) Targeting PDGF receptors in cancer-rationales and proof of concept clinical trials. Adv Exp Med Biol 532: 141-151.
6. Kaplan DR, Chao FC, Stiles CD, Antoniades HN, Scher CD (1979) Platelet alpha granules contain a growth factor for fibroblasts. Blood 53: 1043-1052.
7. Funa K, Papanicolaou V, Juhlin C, Rastad J, Akerstrom G, et al. (1990) Expression of platelet-derived growth factor beta-receptors on stromal tissue cells in human carcinoid tumors. Cancer Res 50: 748-753.
8. Heldin CH, Westermark B (1999) Mechanism of action and in vivo role of platelet-derived growth factor. Physiol Rev 79: 1283-1316.
9. Bhardwaj B, Klassen J, Cossette N, Sterns E, Tuck A, et al. (1996) Localization of platelet-derived growth factor beta receptor expression in the periepithelial stroma of human breast carcinoma. Clin Cancer Res 2: 773-782.
10. Kawai T, Hiroi S, Torikata C (1997) Expression in lung carcinomas of platelet-derived growth factor and its receptors. Lab Invest 77: 431-436.
11. Sundberg C, Branting M, Gerdin B, Rubin K (1997) Tumor cell and connective tissue cell interactions in human colorectal adenocarcinoma. Transfer of platelet-derived growth factor-AB/BB to stromal cells. Am J Pathol 151: 479-492.
12. Jain RK, Lahdenranta J, Fukumura D (2008) Targeting PDGF signaling in carcinoma-associated fibroblasts controls cervical cancer in mouse model. PLoS Med 5: e24.
13. Li J, Perry A, James CD, Gutmann DH (2001) Cancer-related gene expression profiles in NF1-associated pilocytic astrocytomas. Neurology 56: 885-890.
14. Bergsten E, Uutela M, Li X, Pietras K, Ostman A, et al. (2001) PDGF-D is a specific, protease-activated ligand for the PDGF beta-receptor. Nat Cell Biol 3: 512-516.
15. LaRochelle WJ, Jeffers M, McDonald WF, Chillakuru RA, Giese NA, et al. (2001) PDGF-D, a new protease-activated growth factor. Nat Cell Biol 3: 517-521.
16. Li X, Ponten A, Aase K, Karlsson L, Abramsson A, et al. (2000) PDGF-C is a new protease-activated ligand for the PDGF alpha-receptor. Nat Cell Biol 2: 302-309.
17. Lokker NA, Sullivan CM, Hollenbach SJ, Israel MA, Giese NA (2002) Platelet-derived growth factor (PDGF) autocrine signaling regulates survival and mitogenic pathways in glioblastoma cells: evidence that the novel PDGF-C and PDGF-D ligands may play a role in the development of brain tumors. Cancer Res 62: 3729-3735.
18. Dai C, Celestino JC, Okada Y, Louis DN, Fuller GN, et al. (2001) PDGF autocrine stimulation dedifferentiates cultured astrocytes and induces oligodendrogliomas and oligoastrocytomas from neural progenitors and astrocytes in vivo. Gene and Development 15: 1913-1925.
19. Li X, Eriksson U (2003) Novel PDGF family members: PDGF-C and PDGF-D. Cytokine Growth Factor Rev 14: 91-98.
20. Cao R, Brakenhielm E, Li X, Pietras K, Widenfalk J, et al. (2002) Angiogenesis stimulated by PDGF-CC, a novel member in the PDGF family, involves activation of PDGFR-alphaalpha and -alphabeta receptors. Faseb J 16: 1575-1583.
21. Kilic T, Alberta JA, Zdunek PR, Acar M, Iannarelli P, et al. (2000) Intracranial inhibition of platelet-derived growth factor-mediated glioblastoma cell growth by an orally active kinase inhibitor of the 2-phenylaminopyrimidine class. Cancer Res 60: 5143-5150.
22. Hermansson M, Nister M, Betsholtz C, Heldin CH, Westermark B, et al. (1988) Endothelial cell hyperplasia in human glioblastoma: coexpression of mRNA for platelet-derived growth factor (PDGF) B chain and PDGF receptor suggests autocrine growth stimulation. Proc Natl Acad Sci U S A 85: 7748-7752.
23. Jain RK, Munn LL, Fukumura D (2002) Dissecting tumour pathophysiology using intravital microscopy. Nature Rev Cancer 2: 266-276.
24. Winkler F, Kozin SV, Tong RT, Chae SS, Booth MF, et al. (2004) Kinetics of vascular normalization by VEGFR2 blockade governs brain tumor response to radiation: role of oxygenation, angiopoietin-1, and matrix metalloproteinases. Cancer Cell 6: 553-563.
25. Tyrrell JA, di Tomaso E, Fuja D, Tong R, Kozak K, et al. (2007) Robust 3-D modeling of vasculature imagery using superellipsoids. IEEE Trans Med Imaging 26: 223-237.
26. di Tomaso E, Capen D, Haskell A, Hart J, Logie J, et al. (2005) Mosaic tumor vessels: cellular basis and ultrastructure of focal regions lacking endothelial cell markers. Cancer Research 65: 5740-5749.
27. Yuan F, Salehi HA, Boucher Y, Vasthare US, Tuma RF, et al. (1994) Vascular permeability and microcirculation of gliomas and mammary carcinomas transplanted in rat and mouse cranial windows. Cancer Res 54: 4564-4568.
28. Black P, Carroll R, Glowacka D (1996) Expression of platelet-derived growth factor transcripts in medulloblastomas and ependymomas. Pediatr Neurosurg 24: 74-78.
29. Gerhardt H, Betsholtz C (2003) Endothelial-pericyte interactions in angiogenesis. Cell Tissue Res 314: 15-23.
30. Kamoun W, Ley C, Farrar C, Duyvernman A, Lahdenranta J, et al. (in press) Edema control by cediranib, a VEGF targeted kinase inhibitor, prolongs survival despite persistent brain tumor growth in mice. JCO.
31. Bergers G, Hanahan D (2008) Modes of resistance to anti-angiogenic therapy. Nat Rev Cancer 8: 592-603.
32. Crawford Y, Kasman I, Yu L, Zhong C, Wu X, et al. (2009) PDGF-C mediates the angiogenic and tumorigenic properties of fibroblasts associated with tumors refractory to anti-VEGF treatment. Cancer Cell 15: 21-34.
33. Eitner F, Bucher E, van Roeyen C, Kunter U, Rong S, et al. (2008) PDGF-C is a proinflammatory cytokine that mediates renal interstitial fibrosis. J Am Soc Nephrol 19: 281-289.
34. Fraizer GE, Bowen-Pope DF, Vogel AM (1987) Production of platelet-derived growth factor by cultured Wilms' tumor cells and fetal kidney cells. J Cell Physiol 133: 169-174.
35. Gordon GJ, Rockwell GN, Jensen RV, Rheinwald JG, Glickman JN, et al. (2005) Identification of novel candidate oncogenes and tumor suppressors in malignant pleural mesothelioma using large-scale transcriptional profiling. Am J Pathol 166: 1827-1840.
36. Tejada ML, Yu L, Dong J, Jung K, Meng G, et al. (2006) Tumor-driven paracrine platelet-derived growth factor receptor alpha signaling is a key determinant of stromal cell recruitment in a model of human lung carcinoma. Clin Cancer Res 12: 2676-2688.
37. Campbell JS, Johnson MM, Bauer RL, Hudkins KL, Gilbertson DG, et al. (2007) Targeting stromal cells for the treatment of platelet-derived growth factor C-induced hepatocellular carcinogenesis. Differentiation 75: 843-852.
38. Su EJ, Fredriksson L, Geyer M, Folestad E, Cale J, et al. (2008) Activation of PDGF-CC by tissue plasminogen activator impairs blood-brain barrier integrity during ischemic stroke. Nat Med 14: 731-737.
39. Jayson GC, Parker GJ, Mullamitha S, Valle JW, Saunders M, et al. (2005) Blockade of platelet-derived growth factor receptor-beta by CDP860, a humanized, PEGylated di-Fab', leads to fluid accumulation and is associated with increased tumor vascularized volume. J Clin Oncol 23: 973-981.
40. Hagendoorn J, Tong R, Fukumura D, Lin Q, Lobo J, et al. (2006) Onset of abnormal blood and lymphatic vessel function and interstitial hypertension in early stages of carcinogenesis. Cancer Res 66: 3360-3364.
41. Shimizu F, Sano Y, Maeda T, Abe MA, Nakayama H, et al. (2008) Peripheral nerve pericytes originating from the blood-nerve barrier expresses tight junctional molecules and transporters as barrier-forming cells. J Cell Physiol 217: 388-399.
42. Anderberg C, Li H, Fredriksson L, Andrae J, Betsholtz C, et al. (2009) Paracrine signaling by platelet-derived growth factor-CC promotes tumor growth by recruitment of cancer-associated fibroblasts. Cancer Res 69: 369-378.
43. Gerstner ER, Duda DG, di Tomaso E, Sorensen G, Jain RK, et al. (2007) Antiangiogenic agents for the treatment of glioblastoma. Expert Opin Investig Drugs 16: 1895-1908.