MicroRNAs in Cancer Invasion and Metastasis

  • Ashhar S. Ali
  • Shadan Ali
  • Aamir Ahmad
  • Philip A. Philip
  • Fazlul H. Sarkar


The field of cancer research has received invaluable gifts over the last few decades through novel innovations in molecular understanding and drug development. One area that is currently receiving much attention is that of microRNAs (miRNAs). The miRNAs are small, non-coding molecules that inhibit gene expression post-transcriptionally, and emerging evidence suggests that miRNAs are involved in cell growth, differentiation, and apoptosis. These developments could serve as the catalyst for further research focusing on finding a possible molecular link between miRNAs and cancer. This revolutionary research in the field of cancer has shown great promise in understanding the regulatory role of miRNAs in the development and progression of cancer, emphasizing its biochemical and pathological implications, and in particular, its significant role in cancer invasion and metastasis. For example, it has now been widely accepted that certain miRNAs are oncogenic while others act as tumor suppressors. Additionally, studies have shown that miRNAs can be used to alter sensitivity of drug-resistant tumor cells in order to improve the effects of conventional therapeutics. Furthermore, natural agents have been shown to alter miRNA expression, leading to possible inhibition of cancer cell growth and induction of apoptosis, which may contribute to the inhibition of tumor cell migration, invasion, and metastases. Therefore, selective up- and down-regulation of miRNAs holds a great promise for cancer therapy especially for those patients with invasive and metastatic disease. In this chapter, we will summarize the state of our knowledge regarding the role of miRNAs in cancer invasion and metastasis, and will also provide some information on how miRNAs could be regulated for therapeutic interventions.


Breast Cancer Tumor Cell Invasion Cancer Cell Invasion Cancer Cell Migration Tumor Cell Migration 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.


  1. Ali S, Ahmad A, Banerjee S, et al. Gemcitabine sensitivity can be induced in pancreatic cancer cells through modulation of miR-200 and miR-21 expression by curcumin or its analogue CDF. Cancer Res. 2010;70:3606–17.CrossRefPubMedGoogle Scholar
  2. Asangani IA, Rasheed SA, Nikolova DA, et al. MicroRNA-21 (miR-21) post-transcriptionally downregulates tumor suppressor Pdcd4 and stimulates invasion, intravasation and metastasis in colorectal cancer. Oncogene. 2008;27:2128–36.CrossRefPubMedGoogle Scholar
  3. Baranwal S, Alahari SK. MiRNA control of tumor cell invasion and metastasis. Int J Cancer. 2010;126:1283–90.PubMedGoogle Scholar
  4. Barh D, Malhotra R, Ravi B, et al. MicroRNA let-7: an emerging next-generation cancer therapeutic. Curr Oncol. 2010;17:70–80.CrossRefPubMedGoogle Scholar
  5. Bhaumik D, Scott GK, Schokrpur S, et al. Expression of microRNA-146 suppresses NF-kappaB activity with reduction of metastatic potential in breast cancer cells. Oncogene. 2008;27:5643–7.CrossRefPubMedGoogle Scholar
  6. Bonauer A, Carmona G, Iwasaki M, et al. MicroRNA-92a controls angiogenesis and functional recovery of ischemic tissues in mice. Science. 2009;324:1710–3.CrossRefPubMedGoogle Scholar
  7. Boyerinas B, Park SM, Hau A, et al. The role of let-7 in cell differentiation and cancer. Endocr Relat Cancer. 2010;17:F19–F36.CrossRefPubMedGoogle Scholar
  8. Buysschaert I, Schmidt T, Roncal C, et al. Genetics, epigenetics and pharmaco-(epi)genomics in angiogenesis. J Cell Mol Med. 2008;12:2533–51.CrossRefPubMedGoogle Scholar
  9. Cao Q, Yu J, Dhanasekaran SM, et al. Repression of E-cadherin by the polycomb group protein EZH2 in cancer. Oncogene. 2008;27:7274–84.CrossRefPubMedGoogle Scholar
  10. Cha ST, Chen PS, Johansson G, et al. MicroRNA-519c suppresses hypoxia-inducible factor-1alpha expression and tumor angiogenesis. Cancer Res. 2010;70:2675–85.CrossRefPubMedGoogle Scholar
  11. Chang KW, Liu CJ, Chu TH, et al. Association between high miR-211 microRNA expression and the poor prognosis of oral carcinoma. J Dent Res. 2008;87:1063–8.CrossRefPubMedGoogle Scholar
  12. Chen Y, Gorski DH. Regulation of angiogenesis through a microRNA (miR-130a) that down-regulates antiangiogenic homeobox genes GAX and HOXA5. Blood. 2008;111:1217–26.CrossRefPubMedGoogle Scholar
  13. Cho WC. Updates in cancer research: insights from the AACR 100th Annual Meeting. Expert Rev Mol Diagn. 2009;9:411–6.CrossRefPubMedGoogle Scholar
  14. Cho WC. MicroRNAs in cancer – from research to therapy. Biochim Biophys Acta. 2010a;1805:209–17.PubMedGoogle Scholar
  15. Cho WC. MicroRNAs: potential biomarkers for cancer diagnosis, prognosis and targets for therapy. Int J Biochem Cell Biol. 2010b;42:1273–81.CrossRefPubMedGoogle Scholar
  16. Choi SH, Takahashi K, Eto H, et al. CD44 s expression in human colon carcinomas influences growth of liver metastases. Int J Cancer. 2000;85:523–6.CrossRefPubMedGoogle Scholar
  17. Chow TF, Mankaruos M, Scorilas A, et al. The miR-17-92 cluster is over expressed in and has an oncogenic effect on renal cell carcinoma. J Urol. 2010;183:743–51.CrossRefPubMedGoogle Scholar
  18. Cloonan N, Brown MK, Steptoe AL, et al. The miR-17-5p microRNA is a key regulator of the G1/S phase cell cycle transition. Genome Biol. 2008;9:R127.Google Scholar
  19. Connolly EC, Van DK, Rogler LE, et al. Overexpression of miR-21 promotes an in vitro metastatic phenotype by targeting the tumor suppressor RHOB. Mol Cancer Res. 2010;8:691–700.CrossRefPubMedGoogle Scholar
  20. Coulouarn C, Factor VM, Andersen JB, et al. Loss of miR-122 expression in liver cancer correlates with suppression of the hepatic phenotype and gain of metastatic properties. Oncogene. 2009;28:3526–36.CrossRefPubMedGoogle Scholar
  21. De PM, Naldini L. Antagonizing metastasis. Nat Biotechnol. 2010;28:331–2.CrossRefGoogle Scholar
  22. Di LG, Croce CM. Roles of small RNAs in tumor formation. Trends Mol Med. 2010;16:257–67.CrossRefGoogle Scholar
  23. Doebele C, Bonauer A, Fischer A, et al. Members of the microRNA-17-92 cluster exhibit a cell intrinsic anti-angiogenic function in endothelial cells. Blood. 2010;115:4944–50.CrossRefPubMedGoogle Scholar
  24. Fish JE, Srivastava D. MicroRNAs: opening a new vein in angiogenesis research. Sci Signal. 2009;2:e1.Google Scholar
  25. Fish JE, Santoro MM, Morton SU, et al. MiR-126 regulates angiogenic signaling and vascular integrity. Dev Cell. 2008;15:272–84.CrossRefPubMedGoogle Scholar
  26. Friedl P. Prespecification and plasticity: shifting mechanisms of cell migration. Curr Opin Cell Biol. 2004;16:14–23.CrossRefPubMedGoogle Scholar
  27. Gao AC, Lou W, Dong JT, et al. CD44 is a metastasis suppressor gene for prostatic cancer located on human chromosome 11p13. Cancer Res. 1997;57:846–9.PubMedGoogle Scholar
  28. Gregory PA, Bert AG, Paterson EL, et al. The miR-200 family and miR-205 regulate epithelial to mesenchymal transition by targeting ZEB1 and SIP1. Nat Cell Biol. 2008a;10:593–601.CrossRefPubMedGoogle Scholar
  29. Gregory PA, Bracken CP, Bert AG, et al. MicroRNAs as regulators of epithelial-mesenchymal transition. Cell Cycle. 2008b;7:3112–8.CrossRefPubMedGoogle Scholar
  30. Hao-Xiang T, Qian W, Lian-Zhou C, et al. MicroRNA-9 reduces cell invasion and E-cadherin secretion in SK-Hep-1 cell. Med Oncol. 2010;27:654–60.CrossRefGoogle Scholar
  31. He XY, Chen JX, Zhang Z, et al. The let-7a microRNA protects from growth of lung carcinoma by suppression of k-Ras and c-Myc in nude mice. J Cancer Res Clin Oncol. 2010;136:1023–8.CrossRefPubMedGoogle Scholar
  32. Hiyoshi Y, Kamohara H, Karashima R, et al. MicroRNA-21 regulates the proliferation and invasion in esophageal squamous cell carcinoma. Clin Cancer Res. 2009;15:1915–22.CrossRefPubMedGoogle Scholar
  33. Hossain A, Kuo MT, Saunders GF, Mi R-. 17-5p regulates breast cancer cell proliferation by inhibiting translation of AIB1 mRNA. Mol Cell Biol. 2006;26:8191–201.CrossRefPubMedGoogle Scholar
  34. Huang Q, Gumireddy K, Schrier M, et al. The microRNAs miR-373 and miR-520c promote tumour invasion and metastasis. Nat Cell Biol. 2008;10:202–10.CrossRefPubMedGoogle Scholar
  35. Hurst DR, Edmonds MD, Scott GK, et al. Breast cancer metastasis suppressor 1 up-regulates miR-146, which suppresses breast cancer metastasis. Cancer Res. 2009;69:1279–83.CrossRefPubMedGoogle Scholar
  36. Iorio MV, Ferracin M, Liu CG, et al. MicroRNA gene expression deregulation in human breast cancer. Cancer Res. 2005;65:7065–70.CrossRefPubMedGoogle Scholar
  37. Iwatsuki M, Mimori K, Yokobori T, et al. Epithelial-mesenchymal transition in cancer development and its clinical significance. Cancer Sci. 2010;101:293–9.CrossRefPubMedGoogle Scholar
  38. Jakymiw A, Patel RS, Deming N, et al. Overexpression of dicer as a result of reduced let-7 MicroRNA levels contributes to increased cell proliferation of oral cancer cells. Genes Chromosomes Cancer. 2010;49:549–59.CrossRefPubMedGoogle Scholar
  39. Jiang L, Liu X, Kolokythas A, et al. Downregulation of the Rho GTPase signaling pathway is involved in the microRNA-138 mediated inhibition of cell migration and invasion in tongue squamous cell carcinoma. Int J Cancer. 2010;127:505–12.CrossRefPubMedGoogle Scholar
  40. Kong W, Yang H, He L, et al. MicroRNA-155 is regulated by the transforming growth factor beta/Smad pathway and contributes to epithelial cell plasticity by targeting RhoA. Mol Cell Biol. 2008;28:6773–84.CrossRefPubMedGoogle Scholar
  41. Kuehbacher A, Urbich C, Dimmeler S. Targeting microRNA expression to regulate angiogenesis. Trends Pharmacol Sci. 2008;29:12–5.CrossRefPubMedGoogle Scholar
  42. Laios A, O’Toole S, Flavin R, et al. Potential role of miR-9 and miR-223 in recurrent ovarian cancer. Mol Cancer. 2008;7:35.Google Scholar
  43. Lan FF, Wang H, Chen YC, et al. Hsa-let-7 g inhibits proliferation of hepatocellular carcinoma cells by down-regulation of c-Myc and up-regulation of p16(INK4A). Int J Cancer. 2011;128:319–31.CrossRefPubMedGoogle Scholar
  44. Lawler S, Chiocca EA. Emerging functions of microRNAs in glioblastoma. J Neurooncol. 2009;92:297–306.CrossRefPubMedGoogle Scholar
  45. Lee YS, Dutta A. MicroRNAs in cancer. Annu Rev Pathol. 2009;4:199–227.CrossRefPubMedGoogle Scholar
  46. Li N, Fu H, Tie Y, et al. MiR-34a inhibits migration and invasion by down-regulation of c-Met expression in human hepatocellular carcinoma cells. Cancer Lett. 2009a;275:44–53.CrossRefPubMedGoogle Scholar
  47. Li Y, Kong D, Wang Z, et al. Regulation of microRNAs by natural agents: an emerging field in chemoprevention and chemotherapy research. Pharm Res. 2010a;27:1027–41.CrossRefPubMedGoogle Scholar
  48. Li T, Li D, Sha J, et al. MicroRNA-21 directly targets MARCKS and promotes apoptosis resistance and invasion in prostate cancer cells. Biochem Biophys Res Commun. 2009b;383:280–5.CrossRefPubMedGoogle Scholar
  49. Li F, Tiede B, Massague J, et al. Beyond tumorigenesis: cancer stem cells in metastasis. Cell Res. 2007;17:3–14.CrossRefPubMedGoogle Scholar
  50. Li Y, Vandenboom TG, Kong D, et al. Up-regulation of miR-200 and let-7 by natural agents leads to the reversal of epithelial-to-mesenchymal transition in gemcitabine-resistant pancreatic cancer cells. Cancer Res. 2009c;69:6704–12.CrossRefPubMedGoogle Scholar
  51. Li Y, Vandenboom TG, Wang Z, et al. MiR-146a suppresses invasion of pancreatic cancer cells. Cancer Res. 2010b;70:1486–95.CrossRefPubMedGoogle Scholar
  52. Lin SL, Chiang A, Chang D, et al. Loss of miR-146a function in hormone-refractory prostate cancer. RNA. 2008;14:417–24.CrossRefPubMedGoogle Scholar
  53. Liu X, Jiang L, Wang A, et al. MicroRNA-138 suppresses invasion and promotes apoptosis in head and neck squamous cell carcinoma cell lines. Cancer Lett. 2009b;286:217–22.CrossRefPubMedGoogle Scholar
  54. Liu B, Peng XC, Zheng XL, et al. MiR-126 restoration down-regulate VEGF and inhibit the growth of lung cancer cell lines in vitro and in vivo. Lung Cancer. 2009a;66:169–75.CrossRefPubMedGoogle Scholar
  55. Ma L, Teruya-Feldstein J, Weinberg RA. Tumour invasion and metastasis initiated by microRNA-10b in breast cancer. Nature. 2007;449:682–8.CrossRefPubMedGoogle Scholar
  56. Ma L, Weinberg RA. Micromanagers of malignancy: role of microRNAs in regulating metastasis. Trends Genet. 2008;24:448–56.CrossRefPubMedGoogle Scholar
  57. Ma L, Young J, Prabhala H, et al. MiR-9, a MYC/MYCN-activated microRNA, regulates E-cadherin and cancer metastasis. Nat Cell Biol. 2010;12:247–56.PubMedGoogle Scholar
  58. McConkey DJ, Choi W, Marquis L, et al. Role of epithelial-to-mesenchymal transition (EMT) in drug sensitivity and metastasis in bladder cancer. Cancer Metastasis Rev. 2009;28:335–44.CrossRefPubMedGoogle Scholar
  59. Mu G, Liu H, Zhou F, et al. Correlation of overexpression of HMGA1 and HMGA2 with poor tumor differentiation, invasion, and proliferation associated with let-7 down-regulation in retinoblastomas. Hum Pathol. 2010;41:493–502.CrossRefPubMedGoogle Scholar
  60. Nass D, Rosenwald S, Meiri E, et al. MiR-92b and miR-9/9* are specifically expressed in brain primary tumors and can be used to differentiate primary from metastatic brain tumors. Brain Pathol. 2009;19:375–83.CrossRefPubMedGoogle Scholar
  61. Nasser MW, Datta J, Nuovo G, et al. Down-regulation of micro-RNA-1 (miR-1) in lung cancer. Suppression of tumorigenic property of lung cancer cells and their sensitization to doxorubicin-induced apoptosis by miR-1. J Biol Chem. 2008;283:33394–405.CrossRefPubMedGoogle Scholar
  62. Negrini M, Calin GA. Breast cancer metastasis: a microRNA story. Breast Cancer Res. 2008;10:203.Google Scholar
  63. Nicoloso MS, Spizzo R, Shimizu M, et al. MicroRNAs–the micro steering wheel of tumour metastases. Nat Rev Cancer. 2009;9:293–302.CrossRefPubMedGoogle Scholar
  64. Pang RT, Leung CO, Ye TM, et al. MicroRNA-34a suppresses invasion through down-regulation of Notch1 and Jagged1 in cervical carcinoma and choriocarcinoma cells. Carcinogenesis. 2010;31:1037–44.CrossRefPubMedGoogle Scholar
  65. Park SY, Lee JH, Ha M, et al. MiR-29 miRNAs activate p53 by targeting p85 alpha and CDC42. Nat Struct Mol Biol. 2009;16:23–9.CrossRefPubMedGoogle Scholar
  66. Pass HI, Goparaju C, Ivanov S, et al. Hsa-miR-29c* is linked to the prognosis of malignant pleural mesothelioma. Cancer Res. 2010;70:1916–24.CrossRefPubMedGoogle Scholar
  67. Qian B, Katsaros D, Lu L, et al. High miR-21 expression in breast cancer associated with poor disease-free survival in early stage disease and high TGF-beta1. Breast Cancer Res Treat. 2009;117:131–40.CrossRefPubMedGoogle Scholar
  68. Sachdeva M, Mo YY. MicroRNA-145 suppresses cell invasion and metastasis by directly targeting mucin 1. Cancer Res. 2010;70:378–87.CrossRefPubMedGoogle Scholar
  69. Santarpia L, Nicoloso M, Calin GA. MicroRNAs: a complex regulatory network drives the acquisition of malignant cell phenotype. Endocr Relat Cancer. 2010;17:F51–F75.CrossRefPubMedGoogle Scholar
  70. Sarkar FH, Li Y, Wang Z, et al. Implication of microRNAs in drug resistance for designing novel cancer therapy. Drug Resist Updat. 2010;13:57–66.CrossRefPubMedGoogle Scholar
  71. Schmittgen TD. MiR-31: a master regulator of metastasis? Future Oncol. 2010;6:17–20.CrossRefPubMedGoogle Scholar
  72. Sengupta S, den Boon JA, Chen IH, et al. MicroRNA 29c is down-regulated in nasopharyngeal carcinomas, up-regulating mRNAs encoding extracellular matrix proteins. Proc Natl Acad Sci USA. 2008;105:5874–8.CrossRefPubMedGoogle Scholar
  73. Shi M, Guo N. MicroRNA expression and its implications for the diagnosis and therapeutic strategies of breast cancer. Cancer Treat Rev. 2009;35:328–34.CrossRefPubMedGoogle Scholar
  74. Sossey-Alaoui K, Bialkowska K, Plow EF. The miR200 family of microRNAs regulates WAVE3-dependent cancer cell invasion. J Biol Chem. 2009;284:33019–29.CrossRefPubMedGoogle Scholar
  75. Su JL, Chen PB, Chen YH, et al. Downregulation of MicroRNA miR-520 h by E1A Contributes to Anticancer Activity. Cancer Res. 2010;70:5096–108.CrossRefPubMedGoogle Scholar
  76. Suarez Y, Fernandez-Hernando C, Yu J, et al. Dicer-dependent endothelial microRNAs are necessary for postnatal angiogenesis. Proc Natl Acad Sci USA. 2008;105:14082–7.CrossRefPubMedGoogle Scholar
  77. Suarez Y, Sessa WC. MicroRNAs as novel regulators of angiogenesis. Circ Res. 2009;104:442–54.CrossRefPubMedGoogle Scholar
  78. Subramanian S, Thayanithy V, West RB, et al. Genome-wide transcriptome analyses reveal p53 inactivation mediated loss of miR-34a expression in malignant peripheral nerve sheath tumours. J Pathol. 2010;220:58–70.CrossRefPubMedGoogle Scholar
  79. Takakura S, Mitsutake N, Nakashima M, et al. Oncogenic role of miR-17-92 cluster in anaplastic thyroid cancer cells. Cancer Sci. 2008;99:1147–54.CrossRefPubMedGoogle Scholar
  80. Tavazoie SF, Alarcon C, Oskarsson T, et al. Endogenous human microRNAs that suppress breast cancer metastasis. Nature. 2008;451:147–52.CrossRefPubMedGoogle Scholar
  81. Tian Y, Luo A, Cai Y, et al. MicroRNA-10b promotes migration and invasion through KLF4 in human esophageal cancer cell lines. J Biol Chem. 2010;285:7986–94.CrossRefPubMedGoogle Scholar
  82. Tsai WC, Hsu PW, Lai TC, et al. MicroRNA-122, a tumor suppressor microRNA that regulates intrahepatic metastasis of hepatocellular carcinoma. Hepatology. 2009;49:1571–82.CrossRefPubMedGoogle Scholar
  83. Urbich C, Kuehbacher A, Dimmeler S. Role of microRNAs in vascular diseases, inflammation, and angiogenesis. Cardiovasc Res. 2008;79:581–8.CrossRefPubMedGoogle Scholar
  84. Valastyan S, Reinhardt F, Benaich N, et al. A pleiotropically acting microRNA, miR-31, inhibits breast cancer metastasis. Cell. 2009;137:1032–46.CrossRefPubMedGoogle Scholar
  85. Vandenboom TG, Li Y, Philip PA, et al. MicroRNA and cancer: tiny molecules with major implications. Curr Genomics. 2008;9:97–109.CrossRefGoogle Scholar
  86. Varambally S, Cao Q, Mani RS, et al. Genomic loss of microRNA-101 leads to overexpression of histone methyltransferase EZH2 in cancer. Science. 2008;322:1695–9.CrossRefPubMedGoogle Scholar
  87. Volinia S, Calin GA, Liu CG, et al. A microRNA expression signature of human solid tumors defines cancer gene targets. Proc Natl Acad Sci USA. 2006;103:2257–61.CrossRefPubMedGoogle Scholar
  88. Wang S, Aurora AB, Johnson BA, et al. The endothelial-specific microRNA miR-126 governs vascular integrity and angiogenesis. Dev Cell. 2008;15:261–71.CrossRefPubMedGoogle Scholar
  89. Wang Z, Li Y, Kong D, et al. Cross-talk between miRNA and Notch signaling pathways in tumor development and progression. Cancer Lett. 2010;292:141–8.CrossRefPubMedGoogle Scholar
  90. Wang S, Olson EN. AngiomiRs–key regulators of angiogenesis. Curr Opin Genet Dev. 2009;19:205–11.CrossRefPubMedGoogle Scholar
  91. Weiss FU, Marques IJ, Woltering JM, et al. Retinoic acid receptor antagonists inhibit miR-10a expression and block metastatic behavior of pancreatic cancer. Gastroenterology. 2009;137:2136–45.CrossRefPubMedGoogle Scholar
  92. Wu H, Zhu S, Mo YY. Suppression of cell growth and invasion by miR-205 in breast cancer. Cell Res. 2009;19:439–48.CrossRefPubMedGoogle Scholar
  93. Wurdinger T, Tannous BA. Glioma angiogenesis: towards novel RNA therapeutics. Cell Adh Migr. 2009;3:230–5.CrossRefPubMedGoogle Scholar
  94. Wurdinger T, Tannous BA, Saydam O, et al. MiR-296 regulates growth factor receptor overexpression in angiogenic endothelial cells. Cancer Cell. 2008;14:382–93.CrossRefPubMedGoogle Scholar
  95. Xia H, Qi Y, Ng SS, et al. MicroRNA-146b inhibits glioma cell migration and invasion by targeting MMPs. Brain Res. 2009;1269:158–65.CrossRefPubMedGoogle Scholar
  96. Yamakuchi M, Lotterman CD, Bao C, et al. P53-induced microRNA-107 inhibits HIF-1 and tumor angiogenesis. Proc Natl Acad Sci USA. 2010;107:6334–9.CrossRefPubMedGoogle Scholar
  97. Yan D, Zhou X, Chen X, et al. MicroRNA-34a inhibits uveal melanoma cell proliferation and migration through downregulation of c-Met. Invest Ophthalmol Vis Sci. 2009;50:1559–65.CrossRefPubMedGoogle Scholar
  98. Yang F, Yin Y, Wang F, et al. MiR-17-5p Promotes migration of human hepatocellular carcinoma cells through the p38 mitogen-activated protein kinase-heat shock protein 27 pathway. Hepatology. 2010;51:1614–23.CrossRefPubMedGoogle Scholar
  99. Yu Z, Wang C, Wang M, et al. A cyclin D1/microRNA 17/20 regulatory feedback loop in control of breast cancer cell proliferation. J Cell Biol. 2008;182:509–17.CrossRefPubMedGoogle Scholar
  100. Yu Z, Willmarth NE, Zhou J, et al. MicroRNA 17/20 inhibits cellular invasion and tumor metastasis in breast cancer by heterotypic signaling. Proc Natl Acad Sci USA. 2010;107:8231–6.CrossRefPubMedGoogle Scholar
  101. Zhao T, Li J, Chen AF. MicroRNA-34a induces endothelial progenitor cell senescence and impedes its angiogenesis via suppressing silent information regulator 1. Am J Physiol Endocrinol Metab. 2010;299:E110–6.CrossRefPubMedGoogle Scholar

Copyright information

© Springer Netherlands 2011

Authors and Affiliations

  • Ashhar S. Ali
    • 1
  • Shadan Ali
    • 2
  • Aamir Ahmad
    • 1
  • Philip A. Philip
    • 2
  • Fazlul H. Sarkar
    • 3
  1. 1.Department of PathologyKarmanos Cancer Institute, Wayne State UniversityDetroitUSA
  2. 2.Division of Hematology and OncologyKarmanos Cancer Institute, Wayne State UniversityDetroitUSA
  3. 3.Department of PathologySchool of Medicine, Karmanos Cancer Institute, Wayne State University, 740 Hudson Webber Cancer Research CenterDetroitUSA

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