Caveolin-1 is a negative regulator of tumor growth in glioblastoma and modulates chemosensitivity to temozolomide

Cell Cycle

Volumn 12, Issue 10, 2013, Pages 1510-1520

  Quann, Kevin ^a   Gonzales, Donna M ^a   Mercier, Isabelle ^a   Wang, Chenguang ^a   Sotgia, Federica ^a,b   Pestell, Richard G ^c   Lisanti, Michael P ^a,b   Jasmin, Jean Francois ^a  

^a THOMAS JEFFERSON UNIVERSITY   (United States)

^b UNIVERSITY OF MANCHESTER   (United Kingdom)

^c THOMAS JEFFERSON UNIVERSITY   (United States)

Author keywords

Brain cancer; Caveolin 1; Chemotherapy; Glioma; Microarray; Mouse model; Temozolomide; Tumor progression; Tumor suppressor

Indexed keywords

CAVEOLIN 1; MAMMALIAN TARGET OF RAPAMYCIN; MITOGEN ACTIVATED PROTEIN KINASE; PHOSPHATIDYLINOSITOL 3 KINASE; PROTEIN KINASE B; TEMOZOLOMIDE; DACARBAZINE; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; TARGET OF RAPAMYCIN KINASE; TUMOR MARKER;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CANCER GROWTH; CARCINOGENICITY; CELL PROLIFERATION; CELL SURVIVAL; CHEMOSENSITIVITY; CONTROLLED STUDY; ENZYME ACTIVATION; GENE EXPRESSION; GLIOBLASTOMA; HUMAN; HUMAN CELL; IN VIVO STUDY; MOUSE; NONHUMAN; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION; STABLE EXPRESSION; VIRAL GENE DELIVERY SYSTEM; ANALOGS AND DERIVATIVES; ANIMAL; APOPTOSIS; BRAIN NEOPLASMS; DOWN REGULATION; DRUG EFFECTS; GENETICS; LENTIVIRINAE; METABOLISM; PATHOLOGY; TUMOR CELL LINE; XENOGRAFT;

ANIMALS; APOPTOSIS; BRAIN NEOPLASMS; CAVEOLIN 1; CELL LINE, TUMOR; DACARBAZINE; DOWN-REGULATION; GLIOBLASTOMA; HUMANS; LENTIVIRUS; MICE; MITOGEN-ACTIVATED PROTEIN KINASE 1; MITOGEN-ACTIVATED PROTEIN KINASE 3; PHOSPHATIDYLINOSITOL 3-KINASES; PROTO-ONCOGENE PROTEINS C-AKT; SIGNAL TRANSDUCTION; TOR SERINE-THREONINE KINASES; TRANSPLANTATION, HETEROLOGOUS; TUMOR MARKERS, BIOLOGICAL;

EID: 84877979838     PISSN: 15384101     EISSN: 15514005     Source Type: Journal    
DOI: 10.4161/cc.24497     Document Type: Article

References (55)

1. Buckner JC, Brown PD, O'Neill BP, Meyer FB, Wetmore CJ, Uhm JH. Central nervous system tumors. Mayo Clin Proc 2007; 82:1271-86; PMID:17908533; http://dx.doi.org/10.4065/82.10.1271
2. Stupp R, Hegi ME, Mason WP, van den Bent MJ, Taphoorn MJ, Janzer RC, et al.; European Organisation for Research and Treatment of Cancer Brain Tumour and Radiation Oncology Groups; National Cancer Institute of Canada Clinical Trials Group. Effects of radiotherapy with concomitant and adjuvant temozolomide versus radiotherapy alone on survival in glioblastoma in a randomised phase III study: 5-year analysis of the EORTC-NCIC trial. Lancet Oncol 2009; 10:459-66; PMID:19269895; http://dx.doi.org/10.1016/S1470-2045(09)70025-7
3. van Deurs B, Roepstorff K, Hommelgaard AM, Sandvig K. Caveolae: anchored, multifunctional platforms in the lipid ocean. Trends Cell Biol 2003; 13:92-100; PMID:12559760; http://dx.doi.org/10.1016/S0962-8924(02)00039-9
4. García-Cardeña G, Martasek P, Masters BS, Skidd PM, Couet J, Li S, et al. Dissecting the interaction between nitric oxide synthase (NOS) and caveolin. Functional significance of the nos caveolin binding domain in vivo. J Biol Chem 1997; 272:25437-40; PMID:9325253; http://dx.doi.org/10.1074/jbc.272. 41.25437
5. Navarro A, Anand-Apte B, Parat MO. A role for caveolae in cell migration. FASEB J 2004; 18:1801-11; PMID:15576483; http://dx.doi.org/10.1096/fj.04- 2516rev
6. Parton RG, Simons K. The multiple faces of caveolae. Nat Rev Mol Cell Biol 2007; 8:185-94; PMID:17318224; http://dx.doi.org/10.1038/nrm2122
7. Razani B, Woodman SE, Lisanti MP. Caveolae: from cell biology to animal physiology. Pharmacol Rev 2002; 54:431-67; PMID:12223531; http://dx.doi.org/10. 1124/pr.54.3.431
8. Hulit J, Bash T, Fu M, Galbiati F, Albanese C, Sage DR, et al. The cyclin D1 gene is transcriptionally repressed by caveolin-1. J Biol Chem 2000; 275:21203-9; PMID:10747899; http://dx.doi.org/10.1074/jbc.M000321200
9. Patel HH, Murray F, Insel PA. Caveolae as organizers of pharmacologically relevant signal transduction molecules. Annu Rev Pharmacol Toxicol 2008; 48:359-91; PMID:17914930; http://dx.doi.org/10.1146/annurev.pharmtox.48.121506. 124841
10. Williams TM, Lisanti MP. Caveolin-1 in oncogenic transformation, cancer, and metastasis. Am J Physiol Cell Physiol 2005; 288:C494-506; PMID:15692148; http://dx.doi.org/10.1152/ajpcell.00458.2004
11. Goetz JG, Lajoie P, Wiseman SM, Nabi IR. Caveolin-1 in tumor progression: the good, the bad and the ugly. Cancer Metastasis Rev 2008; 27:715-35; PMID:18506396; http://dx.doi.org/10.1007/s10555-008-9160-9
12. Cassoni P, Senetta R, Castellano I, Ortolan E, Bosco M, Magnani I, et al. Caveolin-1 expression is variably displayed in astroglial-derived tumors and absent in oligodendrogliomas: concrete premises for a new reliable diagnostic marker in gliomas. Am J Surg Pathol 2007; 31:760-9; PMID:17460461; http://dx.doi.org/10.1097/01.pas.0000213433.14740.5d
13. Barresi V, Buttarelli FR, Vitarelli EE, Arcella A, Antonelli M, Giangaspero F. Caveolin-1 expression in diffuse gliomas: correlation with the proliferation index, epidermal growth factor receptor, p53, and 1p/19q status. Hum Pathol 2009; 40:1738-46; PMID:19716156; http://dx.doi.org/10.1016/j.humpath. 2009.04.026
14. Senetta R, Trevisan E, Rudà R, Maldi E, Molinaro L, Lefranc F, et al. Caveolin 1 expression independently predicts shorter survival in oligodendrogliomas. J Neuropathol Exp Neurol 2009; 68:425-31; PMID:19287309; http://dx.doi.org/10.1097/NEN.0b013e31819ed0b7
15. Martin S, Cosset EC, Terrand J, Maglott A, Takeda K, Dontenwill M. Caveolin-1 regulates glioblastoma aggressiveness through the control of alpha(5) beta(1) integrin expression and modulates glioblastoma responsiveness to SJ749, an alpha(5)beta(1) integrin antagonist. Biochim Biophys Acta 2009; 1793:354-67; PMID:18992284; http://dx.doi.org/10.1016/j.bbamcr.2008.09.019
16. Cosset EC, Godet J, Entz-Werlé N, Guérin E, Guenot D, Froelich S, et al. Involvement of the TGFβ pathway in the regulation of á5 â1 integrins by caveolin-1 in human glioblastoma. Int J Cancer 2012; 131:601-11; PMID:21901744; http://dx.doi.org/10.1002/ijc.26415
17. Abulrob A, Giuseppin S, Andrade MF, McDermid A, Moreno M, Stanimirovic D. Interactions of EGFR and caveolin-1 in human glioblastoma cells: evidence that tyrosine phosphorylation regulates EGFR association with caveolae. Oncogene 2004; 23:6967-79; PMID:15273741; http://dx.doi.org/10.1038/sj.onc.1207911
18. Forget MA, Desrosiers RR, Del M, Moumdjian R, Shedid D, Berthelet F, et al. The expression of rho proteins decreases with human brain tumor progression: potential tumor markers. Clin Exp Metastasis 2002; 19:9-15; PMID:11918088; http://dx.doi.org/10.1023/A:1013884426692
19. Cameron PL, Liu C, Smart DK, Hantus ST, Fick JR, Cameron RS. Caveolin-1 expression is maintained in rat and human astroglioma cell lines. Glia 2002; 37:275-90; PMID:11857686; http://dx.doi.org/10.1002/glia.10036
20. Engelman JA, Chu C, Lin A, Jo H, Ikezu T, Okamoto T, et al. Caveolin-mediated regulation of signaling along the p42/44 MAP kinase cascade in vivo. A role for the caveolin-scaffolding domain. FEBS Lett 1998; 428:205-11; PMID:9654135; http://dx.doi.org/10.1016/S0014-5793(98)00470-0
21. Cohen AW, Park DS, Woodman SE, Williams TM, Chandra M, Shirani J, et al. Caveolin-1 null mice develop cardiac hypertrophy with hyperactivation of p42/44 MAP kinase in cardiac fibroblasts. Am J Physiol Cell Physiol 2003; 284:C457-74; PMID:12388077
22. Han F, Gu D, Chen Q, Zhu H. Caveolin-1 acts as a tumor suppressor by down-regulating epidermal growth factor receptor-mitogen-activated protein kinase signaling pathway in pancreatic carcinoma cell lines. Pancreas 2009; 38:766-74; PMID:19893453; http://dx.doi.org/10.1097/MPA.0b013e3181b2bd11
23. Schmitz M, Zerr I, Althaus HH. Effect of cavtratin, a caveolin-1 scaffolding domain peptide, on oligodendroglial signaling cascades. Cell Mol Neurobiol 2011; 31:991-7; PMID:21523467; http://dx.doi.org/10.1007/s10571-011- 9694-1
24. Xia H, Khalil W, Kahm J, Jessurun J, Kleidon J, Henke CA. Pathologic caveolin-1 regulation of PTEN in idiopathic pulmonary fibrosis. Am J Pathol 2010; 176:2626-37; PMID:20395445; http://dx.doi.org/10.2353/ajpath.2010.091117
25. Feng S, Wang Y, Wang X, Wang Z, Cui Y, Liu J, et al. Caveolin-1 gene silencing promotes the activation of PI3K/AKT dependent on Eralpha36 and the transformation of MCF10ACE. Science China. Life Sci 2010; 53:598-605; http://dx.doi.org/10.1007/s11427-010-0100-x
26. Mercier I, Camacho J, Titchen K, Gonzales DM, Quann K, Bryant KG, et al. Caveolin-1 and accelerated host aging in the breast tumor microenvironment: chemoprevention with rapamycin, an mTOR inhibitor and anti-aging drug. Am J Pathol 2012; 181:278-93; PMID:22698676; http://dx.doi.org/10.1016/j.ajpath.2012. 03.017
27. Huse JT, Holland EC. Targeting brain cancer: advances in the molecular pathology of malignant glioma and medulloblastoma. Nat Rev Cancer 2010; 10:319-31; PMID:20414201; http://dx.doi.org/10.1038/nrc2818
28. Kita D, Yonekawa Y, Weller M, Ohgaki H. PIK3CA alterations in primary (de novo) and secondary glioblastomas. Acta Neuropathol 2007; 113:295-302; PMID:17235514; http://dx.doi.org/10.1007/s00401-006-0186-1
29. Sunayama J, Matsuda K, Sato A, Tachibana K, Suzuki K, Narita Y, et al. Crosstalk between the PI3K/mTOR and MEK/ERK pathways involved in the maintenance of self-renewal and tumorigenicity of glioblastoma stem-like cells. Stem Cells 2010; 28:1930-9; PMID:20857497; http://dx.doi.org/10.1002/stem.521
30. Mizoguchi M, Betensky RA, Batchelor TT, Bernay DC, Louis DN, Nutt CL. Activation of STAT3, MAPK, and AKT in malignant astrocytic gliomas: correlation with EGFR status, tumor grade, and survival. J Neuropathol Exp Neurol 2006; 65:1181-8; PMID:17146292; http://dx.doi.org/10.1097/01.jnen.0000248549.14962.b2
31. Lopez-Gines C, Gil-Benso R, Benito R, Mata M, Pereda J, Sastre J, et al. The activation of ERK1/2 MAP kinases in glioblastoma pathobiology and its relationship with EGFR amplification. Neuropathology 2008; 28:507-15; PMID:18410277; http://dx.doi.org/10.1111/j.1440-1789.2008.00911.x
32. Ohgaki H, Kleihues P. Genetic pathways to primary and secondary glioblastoma. Am J Pathol 2007; 170:1445-53; PMID:17456751; http://dx.doi.org/ 10.2353/ajpath.2007.070011
33. Louis DN. Molecular pathology of malignant gliomas. Annu Rev Pathol 2006; 1:97-117; PMID:18039109; http://dx.doi.org/10.1146/annurev.pathol.1.110304. 100043
34. Williams TM, Medina F, Badano I, Hazan RB, Hutchinson J, Muller WJ, et al. Caveolin-1 gene disruption promotes mammary tumorigenesis and dramatically enhances lung metastasis in vivo. Role of Cav-1 in cell invasiveness and matrix metalloproteinase (MMP-2/9) secretion. J Biol Chem 2004; 279:51630-46; PMID:15355971; http://dx.doi.org/10.1074/jbc.M409214200
35. Kim HN, Chung HS. Caveolin-1 inhibits membranetype 1 matrix metalloproteinase activity. BMB Rep 2008; 41:858-62; PMID:19123976; http://dx.doi.org/10.5483/BMBRep.2008.41.12.858
36. Han F, Zhu HG. Caveolin-1 regulating the invasion and expression of matrix metalloproteinase (MMPs) in pancreatic carcinoma cells. J Surg Res 2010; 159:443-50; PMID:20031158; http://dx.doi.org/10.1016/j.jss.2009.03.079
37. Reunanen N, Westermarck J, Häkkinen L, Holmström TH, Elo I, Eriksson JE, et al. Enhancement of fibroblast collagenase (matrix metalloproteinase-1) gene expression by ceramide is mediated by extracellular signal-regulated and stress-activated protein kinase pathways. J Biol Chem 1998; 273:5137-45; PMID:9478967; http://dx.doi.org/10.1074/jbc.273.9.5137
38. Kim S, Lee Y, Lee DH, Kim Y, Cho KH, Chung JH. Basal and UV-induced MMP-1 expression are inhibited by p53 in human dermal fibroblasts. Exp Dermatol 2008; 17:939-45; PMID:18557930; http://dx.doi.org/10.1111/j.1600-0625.2008.00729.x
39. Sun Y, Sun Y, Wenger L, Rutter JL, Brinckerhoff CE, Cheung HS. p53 down-regulates human matrix metal-loproteinase-1 (Collagenase-1) gene expression. J Biol Chem 1999; 274:11535-40; PMID:10206959; http://dx.doi.org/10. 1074/jbc.274.17.11535
40. Shetty P, Velusamy T, Bhandary YP, Shetty RS, Liu MC, Shetty S. Urokinase expression by tumor suppressor protein p53: a novel role in mRNA turnover. Am J Respir Cell Mol Biol 2008; 39:364-72; PMID:18390474; http://dx.doi.org/10.1165/ rcmb.2007-0406OC
41. Park J, Bae E, Lee C, Yoon SS, Chae YS, Ahn KS, et al. RNA interference-directed caveolin-1 knockdown sensitizes SN12CPM6 cells to doxorubicin-induced apoptosis and reduces lung metastasis. Tumour Biol 2010; 31:643-50; PMID:20820979; http://dx.doi.org/10.1007/s13277-010-0081-1
42. Yang X, Xiong H, Guan ZZ, Okai I, Ye D, Song Y, et al. Higher expression of Caveolin-1 inhibits human small cell lung cancer (SCLC) apoptosis in vitro. Cancer Invest 2012; 30:453-62; PMID:22545709; http://dx.doi.org/10.3109/ 07357907.2012.675384
43. Zhang M, Lee SJ, An C, Xu JF, Joshi B, Nabi IR, et al. Caveolin-1 mediates Fas-BID signaling in hyperoxia-induced apoptosis. Free Radic Biol Med 2011; 50:1252-62; PMID:21382479; http://dx.doi.org/10.1016/j.freeradbiomed.2011. 02.031
44. Torres VA, Tapia JC, Rodríguez DA, Párraga M, Lisboa P, Montoya M, et al. Caveolin-1 controls cell proliferation and cell death by suppressing expression of the inhibitor of apoptosis protein survivin. J Cell Sci 2006; 119:1812-23; PMID:16608879; http://dx.doi.org/10.1242/jcs.02894
45. Zhang M, Lin L, Lee SJ, Mo L, Cao J, Ifedigbo E, et al. Deletion of caveolin-1 protects hyperoxia-induced apoptosis via survivin-mediated pathways. Am J Physiol Lung Cell Mol Physiol 2009; 297:L945-53; PMID:19767411; http://dx.doi.org/10.1152/ajplung.00081.2009
46. Lin MI, Yu J, Murata T, Sessa WC. Caveolin-1-deficient mice have increased tumor microvascular permeability, angiogenesis, and growth. Cancer Res 2007; 67:2849-56; PMID:17363608; http://dx.doi.org/10.1158/0008-5472.CAN-06- 4082
47. Bruyère C, Abeloos L, Lamoral-Theys D, Senetta R, Mathieu V, Le Mercier M, et al. Temozolomide modifies caveolin-1 expression in experimental malignant gliomas in vitro and in vivo. Transl Oncol 2011; 4:92-100; PMID:21461172
48. Deeken JF, Löscher W. The blood-brain barrier and cancer: transporters, treatment, and Trojan horses. Clin Cancer Res 2007; 13:1663-74; PMID:17363519; http://dx.doi.org/10.1158/1078-0432.CCR-06-2854
49. Jodoin J, Demeule M, Fenart L, Cecchelli R, Farmer S, Linton KJ, et al. P-glycoprotein in blood-brain barrier endothelial cells: interaction and oligomerization with caveolins. J Neurochem 2003; 87:1010-23; PMID:14622130; http://dx.doi.org/10.1046/j.1471-4159.2003.02081.x
50. Guo Z, Zhu J, Zhao L, Luo Q, Jin X. Expression and clinical significance of multidrug resistance proteins in brain tumors. Journal of experimental & clinical cancer research. CR (East Lansing, Mich) 2010; 29:122
51. Mercier I, Casimiro MC, Wang C, Rosenberg AL, Quong J, Minkeu A, et al. Human breast cancer-associated fibroblasts (CAFs) show caveolin-1 downregulation and RB tumor suppressor functional inactivation: Implications for the response to hormonal therapy. Cancer Biol Ther 2008; 7:1212-25; PMID:18458534; http://dx.doi.org/10.4161/cbt.7.8.6220
52. Ho CC, Kuo SH, Huang PH, Huang HY, Yang CH, Yang PC. Caveolin-1 expression is significantly associated with drug resistance and poor prognosis in advanced non-small cell lung cancer patients treated with gemcitabine-based chemotherapy. Lung Cancer 2008; 59:105-10; PMID:17850918; http://dx.doi.org/10. 1016/j.lungcan.2007.07.024
53. Nakatani K, Wada T, Nakamura M, Uzawa K, Tanzawa H, Fujita S. Expression of caveolin-1 and its correlation with cisplatin sensitivity in oral squamous cell carcinoma. J Cancer Res Clin Oncol 2005; 131:445-52; PMID:15856296; http://dx.doi.org/10.1007/s00432-004-0662-8
54. Subramanian A, Tamayo P, Mootha VK, Mukherjee S, Ebert BL, Gillette MA, et al. Gene set enrichment analysis: a knowledge-based approach for interpreting genome-wide expression profiles. Proc Natl Acad Sci USA 2005; 102:15545-50; PMID:16199517; http://dx.doi.org/10.1073/pnas.0506580102
55. Ashburner M, Ball CA, Blake JA, Botstein D, Butler H, Cherry JM, et al.; The Gene Ontology Consortium. Gene ontology: tool for the unification of biology. Nat Genet 2000; 25:25-9; PMID:10802651; http://dx.doi.org/10.1038/75556