Adenoviral expression of vascular endothelial growth factor splice variants differentially regulate bone marrow-derived mesenchymal stem cells

Journal of Cellular Physiology

Volumn 216, Issue 2, 2008, Pages 458-468

  Lin, Huey ^a   Shabbir, Arsalan ^a   Molnar, Merced ^a   Yang, Jingwei ^a   Marion, Susan ^a   Canty Jr , John M ^a   Lee, Techung ^a  

^a UNIVERSITY AT BUFFALO   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

NITRIC OXIDE; OSTEOGENIC PROTEIN 1; VASCULOTROPIN;

ADENOVIRUS; ANIMAL CELL; ARTICLE; BONE DEVELOPMENT; BONE MARROW; CELL DEATH; CELL DIFFERENTIATION; CELL PROLIFERATION; CONTROLLED STUDY; GENE AMPLIFICATION; MESENCHYME CELL; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN EXPRESSION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; VIRUS EXPRESSION;

ADENOVIRIDAE; ALTERNATIVE SPLICING; ANIMALS; ANOXIA; BONE MARROW CELLS; CELL DIFFERENTIATION; CELL PROLIFERATION; CYTOKINES; GENE EXPRESSION REGULATION; HUMANS; MESENCHYMAL STEM CELLS; MYOCYTES, CARDIAC; PROTEIN ISOFORMS; RATS; SWINE; VASCULAR ENDOTHELIAL GROWTH FACTOR A; VASCULAR ENDOTHELIAL GROWTH FACTOR RECEPTOR-1; VASCULAR ENDOTHELIAL GROWTH FACTOR RECEPTOR-2;

RATTUS;

EID: 46049099374     PISSN: 00219541     EISSN: None     Source Type: Journal    
DOI: 10.1002/jcp.21414     Document Type: Article

References (73)

1. Al-Khaldi A, Eliopoulos N, Martineau D, Lejeune L, Lachapelle K, Galipeau J. 2003. Postnatal bone marrow stromal cells elicit a potent VEGF-dependent neoangiogenic response in vivo. Gene Ther 10:621-629.
2. Ball SG, Shuttleworth CA, Kielty CM. 2007. Vascular endothelial growth factor can signal through platelet-derived growth factor receptors. J Cell Biol 177:489-500.
3. Blanes MG, Oubaha M, Rautureau Y, Gratton JP. 2007. Phosphorylation of tyrosine 801 of vascular endothelial growth factor receptor-2 is necessary for Akt-dependent endothelial nitric-oxide synthase activation and nitric oxide release from endothelial cells. J Biol Chem 282:10660-10669.
4. Breier G, Albrecht U, Sterrer S, Risau W. 1992. Expression of vascular endothelial growth factor during embryonic angiogenesis and endothelial cell differentiation. Development 114:521-532.
5. Carmeliet P, Ferreira V, Breier G, Pollefeyt S, Kieckens L, Gertsenstein M, Fahrig M, Vandenhoeck A, Harpal K, Eberhardt C, Declercq C, Pawling J, Moons L, Collen D, Risau W, Nagy A. 1996. Abnormal blood vessel development and lethality in embryos lacking a single VEGF allele. Nature 380:435-439.
6. Carmeliet P, Ng YS, Nuyens D, Theilmeier G, Brusselmans K, Cornelissen I, Ehler E, Kakkar VV, Stalmans I, Mattot V, Perriard JC, Dewerchin M, Flameng W, Nagy A, Lupu F, Moons L, Collen D, D'Amore PA, Shima DT. 1999. Impaired myocardial angiogenesis and ischemic cardiomyopathy in mice lacking the vascular endothelial growth factor isoforms VEGF164 and VE GF188. Nat Med 5:495-502.
7. Celletti FL, Waugh JM, Amabile PG, Brendolan A, Hilfiker PR, Dake MD. 2001. Vascular endothelial growth factor enhances atherosclerotic plaque progression. Nat Med 7:425-429.
8. Chen SJ, Bradley ME, Lee TC. 1998. Chemical hypoxia triggers apoptosis of cultured neonatal rat cardiac myocytes: Modulation by calcium-regulated proteases and protein kinases. Mol Cell Biochem 178:141-149.
9. Cheung N, Wong MP, Yuen ST, Leung SY, Chung LP. 1998. Tissue-specific expression pattern of vascular endothelial growth factor isoforms in the malignant transformation of lung and colon. Hum Pathol 29:910-914.
10. Coultas L, Chawengsaksophak K, Rossant J. 2005. Endothelial cells and VEGF in vascular development. Nature 438:937-945.
11. Dai J, Kitagawa Y, Zhang J, Yao Z, Mizokami A, Cheng S, Nor J, McCauley LK, Taichman RS, Keller ET. 2004. Vascular endothelial growth factor contributes to the prostate cancer-induced osteoblast differentiation mediated by bone morphogenetic protein. Cancer Res 64:994-999.
12. Damoulis PD, Drakos DE, Gagari E, Kaplan DL. 2007. Osteogenic differentiation of human mesenchymal bone marrow cells in silk scaffolds is regulated by nitric oxide. Ann NY Acad Sci 1117:367-376.
13. Darland DC, Massingham LJ, Smith SR, Piek E, Saint-Geniez M, D'Amore PA. 2003. Pericyte production of cell-associated VEGF is differentiation-dependent and is associated with endothelial survival. Dev Biol 264:275-288.
14. Devine SM. 2002. Mesenchymal stem cells: Will they have a role in the clinic? J Cell Biochem Suppl 38:73-79.
15. Dexter TM, Allen TD, Lajtha LG. 1997. Conditions controlling the proliferation of haemopoietic stem cells in vitro. J Cell Physiol 91:335-344.
16. Dore-Duffy P, Wang X, Mehedi A, Kreipke CW, Rafols JA. 2007. Differential expression of capillary VEGF isoforms following traumatic brain injury. Neurol Res 29:395-403.
17. Espey MG, Miranda KM, Feelisch M, Fukuto J, Grisham MB, Vitek MP, Wink DA. 2000. Mechanisms of cell death governed by the balance between nitrosative and oxidative stress. Ann NY Acad Sci 899:209-221.
18. Ferrara N. 1996. Vascular endothelial growth factor. Eur J Cancer 32A:2413-2422.
19. Ferrara N. 2004. Vascular endothelial growth factor: Basic science and clinical progress. Endocr Rev 25:581-611.
20. Ferrari G, Pintucci G, Seghezzi G, Hyman K, Galloway AC, Mignatti P. 2006. VEGF, a prosurvival factor, acts in concert with TGF-beta1 to induce endothelial cell apoptosis. Proc Natl Acad Sci USA 103:17260-17265.
21. Forte G, Minieri M, Cossa P, Antenucci D, Sala M, Gnocchi V, Fiaccavento R, Carotenuto F, De Vito P, Baldini PM, Prat M, Di Nardo P. 2006. Hepatocyte growth factor effects on mesenchymal stem cells: Proliferation, migration, and differentiation. Stem Cells 24:23-33.
22. Fulton D, Gratton JP, McCabe TJ, Fontana J, Fujio Y, Walsh K, Franke TF, Papapetropoulos A, Sessa WC. 1999. Regulation of endothelium-derived nitric oxide production by the protein kinase Akt. Nature 399:597-601.
23. Gerber HP, McMurtrey A, Kowalski J, Yan M, Keyt BA, Dixit V, Ferrara N. 1998. Vascular endothelial growth factor regulates endothelial cell survival through the phosphatidylinositol 3′-kinase/Akt signal transduction pathway. Requirement for Flk-1/KDR activation. J Biol Chem 273:30336-30343.
24. Giordano A, Galderisi U, Marino IR. 2007. From the laboratory bench to the patient's bedside: An update on clinical trials with mesenchymal stem cells. J Cell Physiol 211:27-35.
25. Gnecchi M, He H, Liang OD, Melo LG, Morello F, Mu H, Noiseux N, Zhang L, Pratt RE, Ingwall JS, Dzau VJ. 2005. Paracrine action accounts for marked protection of ischemic heart by Akt-modified mesenchymal stem cells. Nat Med 11:367-368.
26. Gnecchi M, He H, Noiseux N, Liang OD, Zhang L, Morello F, Mu H, Melo LG, Pratt RE, Ingwall JS, Dzau VJ. 2006. Evidence supporting paracrine hypothesis for Akt-modified mesenchymal stem cell-mediated cardiac protection and functional improvement. FASEB J 20:661-669.
27. Gratton JP, Morales-Ruiz M, Kureishi Y, Fulton D, Walsh K, Sessa WC. 2001. Akt down-regulation of p38 signaling provides a novel mechanism of vascular endothelial growth factor-mediated cytoprotection in endothelial cells. J Biol Chem 276:30359-30365.
28. Gui C, Wang JA, He AN, Chen TL, Luo RH, Jiang J, Hu XY, Xie XJ. 2007. Heregulin protects mesenchymal stem cells from serum deprivation and hypoxia-induced apoptosis. Mol Cell Biochem 305:171-178.
29. He C, Chen X. 2005. Transcription regulation of the vegf gene by the BMP/Smad pathway in the angioblast of zebrafish embryos. Biochem Biophys Res Commun 329:324-330.
30. Houck KA, Leung DW, Rowland AM, Winer J, Ferrara N. 1992. Dual regulation of vascular endothelial growth factor bioavailability by genetic and proteolytic mechanisms. J Biol Chem 267:26031-26037.
31. Imabayashi H, Mori T, Gojo S, Kiyono T, Sugiyama T, Irie R, Isogai T, Hata J, Toyama Y, Umezawa A. 2003. Redifferentiation of dedifferentiated chondrocytes and chondrogenesis of human bone marrow stromal cells via chondrosphere formation with expression profiling by large-scale cDNA analysis. Exp Cell Res 288:35-50.
32. Iwaguro H, Yamaguchi J, Kalka C, Murasawa S, Masuda H, Hayashi S, Silver M, Li T, Isner JM, Asahara T. 2002. Endothelial progenitor cell vascular endothelial growth factor gene transfer for vascular regeneration. Circulation 105:732-738.
33. Jian H, Shen X, Liu I, Semenov M, He X, Wang XF. 2006. Smad3-dependent nuclear translocation of beta-catenin is required for TGF-beta1-induced proliferation of bone marrow-derived adult human mesenchymal stem cells. Genes Dev 20:666-674.
34. Jiang Y, Jahagirdar BN, Reinhardt RL, Schwartz RE, Keene CD, Ortiz-Gonzalez XR, Reyes M, Lenvik T, Lund T, Blackstad M, Du J, Aldrich S, Lisberg A, Low WC, Largaespada DA, Verfaillie CM. 2002. Pluripotency of mesenchymal stem cells derived from adult marrow. Nature 418:41-49.
35. Keyt BA, Berleau LT, Nguyen HV, Chen H, Heinsohn H, Vandlen R, Ferrara N. 1996. The carboxyl-terminal domain (111-165) of vascular endothelial growth factor is critical for its mitogenic potency. J Biol Chem 271:7788-7795.
36. Kinnaird T, Stabile E, Burnett MS, Lee CW, Barr S, Fuchs S, Epstein SE. 2004. Marrow-derived stromal cells express genes encoding a broad spectrum of arteriogenic cytokines and promote in vitro and in vivo arteriogenesis through paracrine mechanisms. Circ Res 94:678-685.
37. Kositprapa C, Zhang B, Berger S, Canty JMJ, Lee TC. 2000. Calpain-mediated proteolytic cleavage of troponin 1 induced by hypoxia or metabolic inhibition in cultured neonatal cardiomyocytes. Mol Cell Biochem 214:47-55.
38. Kryczek I, Lange A, Mottram P, Alvarez X, Cheng P, Hogan M, Moons L, Wei S, Zou L, Machelon V, Emilie D, Terrassa M, Lackner A, Curiel TJ, Carmeliet P, Zou W. 2005. CXCL12 and vascular endothelial growth factor synergistically induce neoangiogenesis in human ovarian cancers. Cancer Res 65:465-472.
39. Lamalice L, Le Boeuf F, Huot J. 2007. Endothelial cell migration during angiogenesis. Circ Res 100:782-794.
40. Li Q, Ford MC, Lavik EB, Madri JA 2006. Modeling the neurovascular niche: VEGF- and BDNF-mediated cross-talk between neural stem cells and endothelial cells: An in vitro study. J Neurosci Res 84:1656-1668.
41. Li Y, Yu X, Lin S, Li X, Zhang S, Song YH. 2007. Insulin-like growth factor 1 enhances the migratory capacity of mesenchymal stem cells. Biochem Biophys Res Commun 356:780-784.
42. Lin H, Risbood MP, Jain A, Vacanti V, Lee T. 2004. Role and differential expression of calpastatin mRNA and protein in cultured cardiomyocytes exposed to hypoxic stress. Mol Cell Biochem 265:63-70.
43. Lin H, McGrath J, Wang P, Lee T. 2007. Cellular toxicity induced by SRF-mediated transcriptional squelching. Toxicol Sci 96:83-91.
44. Lou J, Xu F, Merkel K, Manske P. 1999. Gene therapy. Adenovirus-mediated human bone morphogenetic protein-2 gene transfer induces mesenchymal progenitor cell proliferation and differentiation in vitro and bone formation in vivo. J Orthop Res 17:43-50.
45. Maity A, Pore N, Lee J, Solomon D, O'Rourke DM. 2000. Epidermal growth factor receptor transcriptionally up-regulates vascular endothelial growth factor expression in human glioblastoma cells via a pathway involving phosphatidylinositol 3′-kinase and distinct from that induced by hypoxia. Cancer Res 60:5879-5886.
46. Majumdar MK, Thiede MA, Mosca JD, Moorman M, Gerson SL. 1998. Phenotypic and functional comparison of cultures of marrow-derived mesenchymal stem cells (MSCs) and stromal cells. J Cell Physiol 176:57-66.
47. Majumdar MK, Thiede MA, Haynesworth SE, Bruder SP, Gerson SL. 2000. Human marrow-derived mesenchymal stem cells (MSCs) express hematopoietic cytokines and support long-term hematopoiesis when differentiated toward stromal and osteogenic lineages. J Hematother Stem Cell Res 9:841-848.
48. Mayr-Wohlfart U, Waltenberger J, Hausser H, Kessler S, Gunther KP, Dehio C, Puhl W, Brenner RE. 2002. Vascular endothelial growth factor stimulates chemotactic migration of primary human osteoblasts. Bone 30:472-477.
49. Midy V, Plouet J. 1994. Vasculotropin/vascular endothelial growth factor induces differentiation in cultured osteoblasts. Biochem Biophys Res Commun 199:380-386.
50. Neufeld G, Cohen T, Gengrinovitch S, Poltorak Z. 1999. Vascular endothelial growth factor (VEGF) and its receptors. FASEB J 13:9-22.
51. Neuhaus T, Stier S, Totzke G, Gruenewald E, Fronhoffs S, Sachinidis A, Vetter H, Ko YD. 2003. Stromal cell-derived factor 1alpha (SDF-1alpha) induces gene-expression of early growth response-1 (Egr-1) and VEGF in human arterial endothelial cells and enhances VEGF induced cell proliferation. Cell Prolif 36:75-86.
52. Nochi H, Sung JH, Lou J, Adkisson HD, Maloney WJ, Hruska KA. 2004. Adenovirus mediated BMP-13 gene transfer induces chondrogenic differentiation of murine mesenchymal progenitor cells. J Bone Miner Res 19:111-122.
53. Okuyama H, Krishnamachary B, Zhou YF, Nagasawa H, Bosch-Marce M, Semenza GL. 2006. Expression of vascular endothelial growth factor receptor 1 in bone marrow-derived mesenchymal cells is dependent on hypoxia-inducible factor 1. J Biol Chem 281:15554-15563.
54. Oswald J, Boxberger S, Jorgensen B, Feldmann S, Ehninger G, Bornhauser M, Werner C. 2004. Mesenchymal stem cells can be differentiated into endothelial cells in vitro. Stem Cells 22:377-384.
55. Pan Q, Chathery Y, Wu Y, Rathore N, Tong RK, Peale FV, Jr., Bagri A, Tessier-Lavigne M, Koch AW, Watts RJ. 2007. Neuropilin-1 binds to VEGF121 and regulates endothelial cell migration and sprouting. J Biol Chem 282:24049-24056.
56. Sato K, Ozaki K, Oh I, Meguro A, Hatanaka K, Nagai T, Muroi K, Ozawa K. 2007. Nitric oxide plays a critical role in suppression of T-cell proliferation by mesenchymal stem cells. Blood 109:228-234.
57. Schmidt A, Ladage D, Schinkothe T, Klausmann U, Ulrichs C, Klinz FJ, Brixius K, Arnhold S, Desai B, Mehlhorn U, Schwinger RH, Staib P, Addicks K, Bloch W. 2006. Basic fibroblast growth factor controls migration in human mesenchymal stem cells. Stem Cells 24:1750-1758.
58. Sekiya I, Larson BL, Vuoristo JT, Reger RL, Prockop DJ. 2005. Comparison of effect of BMP-2, -4, and -6 on in vitro cartilage formation of human adult stem cells from bone marrow stroma. Cell Tissue Res 320:269-276.
59. Siner JM, Jiang G, Cohen ZI, Shan P, Zhang X, Lee CG, Elias JA, Lee PJ. 2007. VEGF-induced heme oxygenase-1 confers cytoprotection from lethal hyperoxia in vivo. FASEB J 21:1422-1432.
60. Soker S, Fidder H, Neufeld G, Klagsbrun M. 1996. Characterization of novel vascular endothelial growth factor (VEGF) receptors on tumor cells that bind VEGF165 via its exon 7-encoded domain. J Biol Chem 271:5761-5767.
61. Soker S, Takashima S, Miao HQ, Neufeld G, Klagsbrun M. 1998. Neuropilin-1 is expressed by endothelial and tumor cells as an isoform-specific receptor for vascular endothelial growth factor. Cell 92:735-745.
62. Street J, Bao M, deGuzman L, Bunting S, Peale FV, Jr., Ferrara N, Steinmetz H, Hoeffel J, Cleland JL, Daugherty A, van Bruggen N, Redmond HP, Carano RA, Filvaroff EH. 2002. Vascular endothelial growth factor stimulates bone repair by promoting angiogenesis and bone turnover. Proc Natl Acad Sci USA 99:9656-9661.
63. Suzuki G, Lee TC, Fallavollita JA, Canty JM, Jr. 2005. Adenoviral gene transfer of FGF-5 to hibernating myocardium improves function and stimulates myocytes to hypertrophy and reenter the cell cycle. Circ Res 96:767-775.
64. Tamama K, Fan VH, Griffith LG, Blair HC, Wells A. 2006. Epidermal growth factor as a candidate for ex vivo expansion of bone marrow-derived mesenchymal stem cells. Stem Cells 24:686-695.
65. Tang YL, Zhao Q, Qin X, Shen L, Cheng L, Ge J, Phillips MI. 2005. Paracrine action enhances the effects of autologous mesenchymal stem cell transplantation on vascular regeneration in rat model of myocardial infarction. Ann Thorac Surg 80:229-236.
66. Vacanti V, Kong E, Suzuki G, Sato K, Canty JM, Jr., Lee T. 2005. Phenotypic changes of adult porcine mesenchymal stem cells induced by prolonged passaging in culture. J Cell Physiol 205:194-201.
67. Vogt RR, Unda R, Yeh LC, Vidro EK, Lee JC, Tsin AT. 2006. Bone morphogenetic protein-4 enhances vascular endothelial growth factor secretion by human retinal pigment epithelial cells. J Cell Biochem 98:1196-1202.
68. Wada T, Haigh JJ, Ema M, Hitoshi S, Chaddah R, Rossant J, Nagy A, van der Kooy D. 2006. Vascular endothelial growth factor directly inhibits primitive neural stem cell survival but promotes definitive neural stem cell survival. J Neurosci 26:6803-6812.
69. Walowitz JL, Bradley ME, Chen SJ, Lee TC. 1998. Proteolytic regulation of the zinc finger transcription factor YY1, a repressor of muscle-restricted gene expression. J Biol Chem 273:6656-6661.
70. Wang X, Hu Q, Mansoor A, Lee J, Wang Z, Lee T, From AH, Zhang J. 2006. Bioenergetic and functional consequences of stem cell-based VEGF delivery in pressure-overloaded swine hearts. Am J Physiol Heart Circ Physiol 290:H1393-H1405.
71. Wieczorek G, Steinhoff C, Schulz R, Scheller M, Vingron M, Ropers HH, Nuber UA 2003. Gene expression profile of mouse bone marrow stromal cells determined by cDNA microarray analysis. Cell Tissue Res 311:227-237.
72. Yla-Herttuala S, Rissanen TT, Vajanto I, Hartikainen J. 2007. Vascular endothelial growth factors: Biology and current status of clinical applications in cardiovascular medicine. J Am Coll Cardiol 49:1015-1026.
73. Zhang H-T, Scott P, Morbidelli L, Peak S, Moore J, Turley H, Harris AL, Ziehe M, Bicknell R. 2000. The 121 amino acid isoform of vascular endothelial growth factor is more strongly tumorigenic than other splice variants in vivo. Br J Cancer 83:63-68.