Lung Cancer Cells That Survive Ionizing Radiation Show Increased Integrin α2β1- and EGFR-Dependent Invasiveness

PLoS ONE

Volumn 8, Issue 8, 2013, Pages

  Li, Xue ^a   Ishihara, Seiichiro ^a   Yasuda, Motoaki ^a   Nishioka, Takeshi ^a   Mizutani, Takeomi ^a   Ishikawa, Masayori ^b   Kawabata, Kazushige ^a   Shirato, Hiroki ^b   Haga, Hisashi ^a  

^a HOKKAIDO UNIVERSITY   (Japan)

^b HOKKAIDO UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA2 INTEGRIN; BETA1 INTEGRIN; EPIDERMAL GROWTH FACTOR RECEPTOR; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; PROTEIN KINASE B; VERY LATE ACTIVATION ANTIGEN 2;

ARTICLE; CANCER CELL CULTURE; CELL ACTIVATION; CELL ELONGATION; CELL LEVEL; CELL STRUCTURE; CELL SURVIVAL; CONTROLLED STUDY; DOSIMETRY; ENZYME ACTIVATION; GENE EXPRESSION; HUMAN; HUMAN CELL; IN VIVO STUDY; IONIZING RADIATION; LUNG CANCER; MOLECULAR DYNAMICS; ONCOGENE; PROTEIN DETERMINATION; PROTEIN EXPRESSION; PROTEIN FUNCTION; SIGNAL TRANSDUCTION; TUMOR INVASION; TUMOR MICROENVIRONMENT;

ADENOCARCINOMA; CELL LINE, TUMOR; EXTRACELLULAR SIGNAL-REGULATED MAP KINASES; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; INTEGRIN ALPHA2BETA1; LUNG; LUNG NEOPLASMS; NEOPLASM INVASIVENESS; PHOSPHATIDYLINOSITOL 3-KINASES; PROTO-ONCOGENE PROTEINS C-AKT; RADIATION, IONIZING; RECEPTOR, EPIDERMAL GROWTH FACTOR; SIGNAL TRANSDUCTION;

EID: 84881341600     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0070905     Document Type: Article

References (55)

1. Gandara D, Narayan S, Lara Jr PN, Goldberg Z, Davies A, et al. (2005) Integration of novel therapeutics into combined modality therapy of locally advanced non-small cell lung cancer. Clin Cancer Res 11: 5057-5062.
2. von Essen CF, (1991) Radiation enhancement of metastasis: a review. Clin Exp Metastasis 9: 77-104.
3. Ling C, Xie Y, Zhao D, Zhu Y, Xiang J, et al. (2012) Enhanced radiosensitivity of non-small-cell lung cancer (NSCLC) by adenovirus-mediated ING4 gene therapy. Cancer Gene Ther 19: 697-706.
4. Cordes N, (2004) Overexpression of hyperactive integrin-linked kinase leads to increased cellular radiosensitivity. Cancer Res 64: 5683-5692.
5. Bouquet F, Pal A, Pilones KA, Demaria S, Hann B, et al. (2011) TGFβ 1 inhibition increases the radiosensitivity of breast cancer cells in vitro and promotes tumor control by radiation in vivo. Clin Cancer Res 17: 6754-6765.
6. Eke I, Schneider L, Förster C, Zips D, Kunz-Schughart LA, et al. (2013) EGFR/JIP-4/JNK2 signaling attenuates Cetuximab-mediated radiosensitization of squamous cell carcinoma cells. Cancer Res 73: 297-306.
7. Wild-Bode C, Weller M, Rimner A, Dichgans J, Wick W, (2001) Sublethal irradiation promotes migration and invasiveness of glioma cells: implications for radiotherapy of human glioblastoma. Cancer Res 61: 2744-2750.
8. Yao H, Zeng ZZ, Fay KS, Veine DM, Staszewski ED, et al. (2011) Role of α5β1 integrin up-regulation in radiation-induced invasion by human pancreatic cancer cells. Transl Oncol 4: 282-292.
9. Gogineni VR, Nalla AK, Gupta R, Gujrati M, Klopfenstein JD, et al. (2011) α3β1 integrin promotes radiation-induced migration of meningioma cells. Inter J Oncology 38: 1615-1624.
10. Ishihara S, Haga H, Yasuda M, Mizutani T, Kawabata K, et al. (2010) Integrin β1-dependent invasive migration of irradiation-tolerant human lung adenocarcinoma cells in 3D collagen matrix. Biochem Biophys Res Commun 396: 651-655.
11. Nalla AK, Asuthkar S, Bhoopathi P, Gujrati M, Dinh DH, et al. (2010) Suppression of uPAR retards radiation-induced invasion and migration mediated by integrin β1/FAK signaling in medulloblastoma. PLoS ONE 5: e13006.
12. Zhai GG, Malhotra R, Delaney M, Latham D, Nestler U, et al. (2006) Radiation enhances the invasive potential of primary glioblastoma cells via activation of the Rho signaling pathway. J Neurooncol 76: 227-237.
13. Park CM, Park MJ, Kwak HJ, Lee HC, Kim MS, et al. (2006) Ionizing radiation enhances matrix metalloproteinase-2 secretion and invasion of glioma cells through src/epidermal growth factor receptor-mediated p38/Akt and phosphatidylinositol 3-kinase/Akt signaling pathways. Cancer Res 66: 8511-8519.
14. Chu SH, Ma YB, Zhu ZA, Zhang H, Feng DF, et al. (2007) Radiation-enhanced hepatocyte growth factor secretion in malignant glioma cell lines. Surg Neurol 68: 610-614.
15. Sanz-Moreno V, Gadea G, Ahn J, Paterson H, Marra P, et al. (2008) Rac activation and inactivation control plasticity of tumor cell movement. Cell 135: 510-523.
16. De Wever O, Hendrix A, De Boeck A, Westbroek W, Braems G, et al. (2010) Modeling and quantification of cancer cell invasion through collagen type I matrices. Int. J. Dev. Biol. 54: 887-896.
17. Hood JD, Cheresh DA, (2002) Role of integrins in cell invasion and migration. Nat Rev Cancer 2: 91-100.
18. Humphries JD, Byron A, Humphries MJ, (2006) Integrin ligands at a glance. J Cell Sci 119: 3901-3903.
19. Gazdar AF, Minna JD, (2008) Deregulated EGFR signaling during lung cancer progression: mutations, amplicons, and autocrine loops. Cancer Prev Res 1: 156-160.
20. Sawhney RS, Sharma B, Humphrey LE, Brattain MG, (2003) Integrin α2 and extracellular signaling-regulated kinase are functionally linked in highly malignant autocrine transforming growth factor-α-driven colon cancer cells. J Biol Chem 278: 19861-19869.
21. Ramis G, Thomàs-Moyà E, Fernández de Mattos S, Rodríguez J, Villalonga P, (2012) EGFR inhibition in glioma cells modulates Rho signaling to inhibit cell motility and invasion and cooperates with temozolomide to reduce cell growth. PLoS ONE 7: e38770.
22. Cabodi S, Morello V, Masi A, Cicchi R, Broggio C, et al. (2009) Convergence of integrins and EGF receptor signaling via PI3K/Akt/FoxO pathway in early gene Egr-1 expression. J Cell Physiol 218: 294-303.
23. Wang CZ, Su HW, Hsu YC, Shen MR, Tang MJ, (2006) A discoidin domain receptor 1/SHP-2 signaling complex inhibits α2β1-integrin-mediated signal transducers and activators of transcription1/3 activation and cell migration. Mol Biol Cell 17: 2839-2852.
24. Klekotka PA, Santoro S, Zutter MM, (2001) α2 integrin subunit cytoplasmic domain-dependent cellular migration requires p38 MAPK. J Biol Chem 276: 9503-9511.
25. Jung JW, Hwang SY, Hwang JS, Oh ES, Park S, et al. (2007) Ionising radiation induces changes associated with epithelial-mesenchymal transdifferentiation and increased cell motility of A549 lung epithelial cells. Eur. J. Cancer 43: 1214-1224.
26. Edick MJ, Tesfay L, Lamb LE, Knudsen BS, Miranti CK, (2007) Inhibition of integrin-mediated crosstalk with epidermal growth factor receptor/Erk or Src signaling pathways in autophagic prostate epithelial cells induces caspase-independent death. Mol Biol Cell 18: 2481-2490.
27. Gan Y, Shi C, Inge L, Hibner M, Balducci J, et al. (2010) Differential roles of ERK and Akt pathways in regulation of EGFR-mediated signaling and motility in prostate cancer cells. Oncogene 29: 4947-4958.
28. Baumann M, Krause M, Hill R, (2008) Exploring the role of cancer stem cells in radioresistance. Nat Rev Cancer 8: 545-554.
29. Suki B, Ito S, Stamenovié D, Lutchen KR, Ingenito EP, (2005) Biomenchanics of the lung parenchyma: critical roles of collagen and mechanical forces. J Appl Physiol 98: 1892-1899.
30. Klein CE, Dressel D, Steinmayer T, Mauch C, Eckes B, et al. (1991) Integrin alpha 2 beta 1 is upregulated in fibroblasts and highly aggressive melanoma cells in three-dimensional collagen lattices and mediates the reorganization of collagen I fibrils. J Cell Biol 115: 1427-1436.
31. Shield K, Riley C, Quinn MA, Rice GE, Ackland ML, et al. (2007) α2β1 integrin affects metastatic potential of ovarian carcinoma spheroids by supporting disaggregation and proteolysis. J Carcinog 6: 11.
32. Slambrouck SV, Jenkins AR, Romero A, Steelant WFA, (2009) Reorganization of the integrin a2 subunit controls cell adhesion and cancer cell invasion in prostate cancer. Int J Oncol 34: 1717-1726.
33. Chen FA, Repasky EA, Bankert RB, (1991) Human lung tumor-associated antigen identified as an extracellular matrix adhesion molecule. J Exp Med 173: 1111-1119.
34. Langholz O, Röckel D, Mauch C, Kozlowska E, Bank I, et al. (1995) Collagen and collagenase gene expression in three-dimensional collagen lattices are differentially regulated by α1β1 and α2β1 integrins. J Cell Biol 131: 1903-1915.
35. Mattila E, Pellinen T, Nevo J, Vuoriluoto K, Arjonen A, et al. (2005) Negative regulation of EGFR signalling through integrin-α1β1-mediated activation of protein tyrosine phosphatase TCPTP. Nat Cell Biol 7: 78-85.
36. Yu X, Miyamoto S, Mekada E, (2000) Integrin α2β1-dependent EGF receptor activation at cell-cell contact sites. J Cell Sci 113: 2139-2147.
37. Wang M, Morsbach F, Sander D, Gheorghiu L, Nanda A, et al. (2011) EGF receptor inhibition radiosensitizes NSCLC cells by inducing senescence in cells sustaining DNA double-strand breaks. Cancer Res 71: 6261-6269.
38. Chakrabarty A, Sánchez V, Kuba MG, Rinehart C, Arteaga CL, (2011) Feedback upregulation of HER3 (ErbB3) expression and activity attenuates antitumor effect of PI3K inhibitors. Proc Natl Acad Sci 109: 2718-2723.
39. Serra V, Scaltriti M, Prudkin L, Eichhorn PJA, Ibrahim YH, et al. (2011) PI3K inhibition results in enhanced HER signaling and acquired ERK dependency in HER2-overexpressing breast cancer. Oncogene 30: 2547-2557.
40. Hu C, Huang L, Gest C, Xi X, Janin A, et al. (2012) Opposite regulation by PI3K/Akt and MAPK/ERK pathways of tissue factor expression, cell-associated procoagulant activity and invasiveness in MDA-MB-231 cells. J Hematol Oncol 5: 16.
41. Marampon F, Gravina GL, Di Rocco A, Bonfili P, Di Staso M, et al. (2011) MEK/ERK inhibitor U0126 increases the radiosensitivity of rhabdomyosarcoma cells in vitro and in vivo by downregulating growth and DNA repair signals. Mol Cancer Ther 10: 159-168.
42. Carter S, Auer KL, Reardon DB, Birrer M, Fisher PB, et al. (1998) Inhibition of the mitogen activated protein (MAP) kinase cascade potentiates cell killing by low dose ionizing radiation in A431 squamous carcinoma cells. Oncogene 16: 2787-2796.
43. Alam N, Goel HL, Zarif MJ, Butterfield JE, Perkins HM, et al. (2007) The integrin-growth factor receptor duet. J Cell Physiol 213: 649-653.
44. Ricono JM, Huang M, Barnes LA, Lau SK, Weis SM, et al. (2009) Specific cross-talk between epidermal growth factor receptor and integrin αvβ5 promotes carcinoma cell invasion and metastasis. Cancer Res 69: 1383-1391.
45. Morello V, Cabodi S, Sigismund S, Camacho-Leal MP, Repetto D, et al. (2011) β1 integrin controls EGFR signaling and tumorigenic properties of lung cancer cells. Oncogene 30: 4087-4096.
46. Krensel K, Lichtner RB, (1999) Selective increase of α2-integrin sub-unit expression on human carcinoma cells upon EGF-receptor activation. Int J Cancer 80: 546-552.
47. Hall CL, Dai J, van Golen KL, Keller ET, Long MW, (2006) Type I collagen receptor (α2β1) signaling promotes the growth of human prostate cancer cells within the bone. Cancer Res 66: 8648-8654.
48. Park CC, Zhang H, Pallavicini M, Gray JW, Baehner F, et al. (2006) β1 integrin inhibitory antibody induces apoptosis of breast cancer cells, inhibits growth, and distinguishes malignant from normal phenotype in three dimensional cultures and in vivo. Cancer Res 66: 1526-1535.
49. Ramis G, Thomàs-Moyà E, Fernández de Mattos S, Rodríguez J, Villalonga P, (2012) EGFR Inhibition in Glioma Cells Modulates Rho Signaling to Inhibit Cell Motility and Invasion and Cooperates with Temozolomide to Reduce Cell Growth. PLoS ONE 7: e38770.
50. Chappell WH, Steelman LS, Long JM, Kempf RC, Abrams SL, et al. (2011) Ras/Raf/MEK/ERK and PI3K/PTEN/Akt/mTOR inhibitors: rationale and importance to inhibiting these pathways in human health. Oncotarget 2: 135-64.
51. Liang K, Ang KK, Milas L, Hunter N, Fan Z, (2003) The epidermal growth factor receptor mediates radioresistance. Int J Radiat Oncol Biol Phys 57: 246-254.
52. Thariat J, Milas L, Ang KK, (2007) Integrating radiotherapy with EGFR antagonists and other molecular therapeutics for the treatment of head and neck cancer. Int J Radiat Oncol Biol Phys 69: 974-984.
53. Brugger W, Thomas M, (2012) EGFR-TKI resistant non-small cell lung cancer (NSCLC): new developments and implications for future treatment. Lung Cancer 77: 2-8.
54. Goodman SL, Picard M, (2012) Integrins as therapeutic targets. Trends Pharmacol Sci 33: 405-412.
55. Desgrosellier JS, Cheresh DA, (2010) Integrins in cancer: biological implications and therapeutic opportunities. Nat Rev 10: 9-22.