Co-regulation of cell polarization and migration by caveolar proteins PTRF/cavin-1 and caveolin-1

PLoS ONE

Volumn 7, Issue 8, 2012, Pages

  Hill, Michelle M ^a   Daud, Noor Huda ^a   Aung, Cho Sanda ^a   Loo, Dorothy ^a   Martin, Sally ^a   Murphy, Samantha ^a,d   Black, Debra M ^a   Barry, Rachael ^a   Simpson, Fiona ^a   Liu, Libin ^b   Pilch, Paul F ^b   Hancock, John F ^a,c   Parat, Marie Odile ^a   Parton, Robert G ^a  

^a UNIVERSITY OF QUEENSLAND   (Australia)

^b BOSTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c UNIVERSITY OF TEXAS MEDICAL SCHOOL   (United States)

^d MONASH UNIVERSITY   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

CAVEOLIN 1; CYTOPLASM PROTEIN; POLYMERASE I AND TRANSCRIPT RELEASE FACTOR; RAC1 PROTEIN; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; CAVEOLA; CELL FRACTIONATION; CELL MIGRATION; CELL POLARITY; CELL TRANSFORMATION; CELLULAR DISTRIBUTION; CONTROLLED STUDY; EMBRYO; EPITHELIAL MESENCHYMAL TRANSITION; FLUORESCENCE IMAGING; FUNCTIONAL PROTEOMICS; MOLECULAR DYNAMICS; MOUSE; NONHUMAN; PROTEIN ANALYSIS; PROTEIN DEPLETION; PROTEIN EXPRESSION; PROTEIN FUNCTION; QUANTITATIVE ANALYSIS;

ANIMALS; BLOTTING, WESTERN; CAVEOLIN 1; CELL MOVEMENT; CELL POLARITY; CHEMOTAXIS; MEMBRANE PROTEINS; MICE; MICROSCOPY, FLUORESCENCE; MICROSCOPY, VIDEO; NEUROPEPTIDES; NIH 3T3 CELLS; RAC GTP-BINDING PROTEINS;

EID: 84865055662     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0043041     Document Type: Article

References (51)

1. Parton RG, Simons K, ((2007)) The multiple faces of caveolae. Nat Rev Mol Cell Biol 8:: 185--194.
2. Hill MM, Bastiani M, Luetterforst R, Kirkham M, Kirkham A, et al. ((2008)) PTRF-Cavin, a conserved cytoplasmic protein required for caveola formation and function. Cell 132:: 113--124.
3. Liu L, Brown D, McKee M, Lebrasseur NK, Yang D, et al. ((2008)) Deletion of Cavin/PTRF causes global loss of caveolae, dyslipidemia, and glucose intolerance. Cell Metab 8:: 310--317.
4. Hayashi YK, Matsuda C, Ogawa M, Goto K, Tominaga K, et al. ((2009)) Human PTRF mutations cause secondary deficiency of caveolins resulting in muscular dystrophy with generalized lipodystrophy. J Clin Invest 119:: 2623--2633.
5. Rajab A, Straub V, McCann LJ, Seelow D, Varon R, et al. ((2010)) Fatal cardiac arrhythmia and long-QT syndrome in a new form of congenital generalized lipodystrophy with muscle rippling (CGL4) due to PTRF-CAVIN mutations. PLoS Genet 6:: e1000874.
6. McMahon KA, Zajicek H, Li WP, Peyton MJ, Minna JD, et al. ((2009)) SRBC/cavin-3 is a caveolin adapter protein that regulates caveolae function. EMBO J 28:: 1001--1015.
7. Hansen CG, Bright NA, Howard G, Nichols BJ, ((2009)) SDPR induces membrane curvature and functions in the formation of caveolae. Nat Cell Biol 11:: 807--814.
8. Bastiani M, Liu L, Hill MM, Jedrychowski MP, Nixon SJ, et al. ((2009)) MURC/Cavin-4 and cavin family members form tissue-specific caveolar complexes. J Cell Biol 185:: 1259--1273.
9. Parat MO, ((2009)) The biology of caveolae: achievements and perspectives. Int Rev Cell Mol Biol 273:: 117--162.
10. Sowa G, Pypaert M, Sessa WC, ((2001)) Distinction between signaling mechanisms in lipid rafts vs. caveolae. Proc Natl Acad Sci U S A 98:: 14072--14077.
11. Liu L, Pilch PF, ((2008)) A critical role of cavin (polymerase I and transcript release factor) in caveolae formation and organization. J Biol Chem 283:: 4314--4322.
12. Aung CS, Hill MM, Bastiani M, Parton RG, Parat MO, ((2011)) PTRF-cavin-1 expression decreases the migration of PC3 prostate cancer cells: role of matrix metalloprotease 9. European journal of cell biology 90:: 136--142.
13. Parat MO, Anand-Apte B, Fox PL, ((2003)) Differential caveolin-1 polarization in endothelial cells during migration in two and three dimensions. Mol Biol Cell 14:: 3156--3168.
14. Santilman V, Baran J, Anand-Apte B, Fox PL, Parat MO, ((2006)) Caveolin-1 polarization in migrating endothelial cells is directed by substrate topology not chemoattractant gradient. Cell Motil Cytoskeleton 63:: 673--680.
15. Santilman V, Baran J, Anand-Apte B, Evans RM, Parat MO, ((2007)) Caveolin-1 polarization in transmigrating endothelial cells requires binding to intermediate filaments. Angiogenesis 10:: 297--305.
16. Grande-Garcia A, Echarri A, de Rooij J, Alderson NB, Waterman-Storer CM, et al. ((2007)) Caveolin-1 regulates cell polarization and directional migration through Src kinase and Rho GTPases. J Cell Biol 177:: 683--694.
17. Inder KL, Zheng YZ, Davis MJ, Moon H, Loo D,et al. (2012) Expression of PTRF in PC-3 Cells modulates cholesterol dynamics and the actin cytoskeleton impacting secretion pathways. Molecular & cellular proteomics: MCP 11: M111 012245.
18. Mineo C, Ying YS, Chapline C, Jaken S, Anderson RG, ((1998)) Targeting of protein kinase Calpha to caveolae. The Journal of cell biology 141:: 601--610.
19. Shenoy-Scaria AM, Dietzen DJ, Kwong J, Link DC, Lublin DM, ((1994)) Cysteine3 of Src family protein tyrosine kinase determines palmitoylation and localization in caveolae. The Journal of cell biology 126:: 353--363.
20. Smart EJ, Foster DC, Ying YS, Kamen BA, Anderson RG, ((1994)) Protein kinase C activators inhibit receptor-mediated potocytosis by preventing internalization of caveolae. The Journal of cell biology 124:: 307--313.
21. Ko YG, Liu P, Pathak RK, Craig LC, Anderson RG, ((1998)) Early effects of pp60(v-src) kinase activation on caveolae. Journal of cellular biochemistry 71:: 524--535.
22. Buitrago C, Boland R, ((2010)) Caveolae and caveolin-1 are implicated in 1alpha,25(OH)2-vitamin D3-dependent modulation of Src, MAPK cascades and VDR localization in skeletal muscle cells. The Journal of steroid biochemistry and molecular biology 121:: 169--175.
23. Prevostel C, Alice V, Joubert D, Parker PJ, ((2000)) Protein kinase C(alpha) actively downregulates through caveolae-dependent traffic to an endosomal compartment. Journal of cell science 113 (Pt 14):: 2575--2584.
24. Song KS, Sargiacomo M, Galbiati F, Parenti M, Lisanti MP, ((1997)) Targeting of a G alpha subunit (Gi1 alpha) and c-Src tyrosine kinase to caveolae membranes: clarifying the role of N-myristoylation. Cellular and molecular biology 43:: 293--303.
25. Silverman-Gavrila R, Silverman-Gavrila L, Hou G, Zhang M, Charlton M, et al. ((2011)) Rear polarization of the microtubule-organizing center in neointimal smooth muscle cells depends on PKCalpha, ARPC5, and RHAMM. The American journal of pathology 178:: 895--910.
26. Lin CW, Shen SC, Chien CC, Yang LY, Shia LT, et al. ((2010)) 12-O-tetradecanoylphorbol-13-acetate-induced invasion/migration of glioblastoma cells through activating PKCalpha/ERK/NF-kappaB-dependent MMP-9 expression. Journal of cellular physiology 225:: 472--481.
27. Verma P, Ostermeyer-Fay AG, Brown DA, ((2010)) Caveolin-1 induces formation of membrane tubules that sense actomyosin tension and are inhibited by polymerase I and transcript release factor/cavin-1. Mol Biol Cell 21:: 2226--2240.
28. Engelman JA, Wykoff CC, Yasuhara S, Song KS, Okamoto T, et al. ((1997)) Recombinant expression of caveolin-1 in oncogenically transformed cells abrogates anchorage-independent growth. J Biol Chem 272:: 16374--16381.
29. Zhang W, Razani B, Altschuler Y, Bouzahzah B, Mostov KE, et al. ((2000)) Caveolin-1 inhibits epidermal growth factor-stimulated lamellipod extension and cell migration in metastatic mammary adenocarcinoma cells (MTLn3). Transformation suppressor effects of adenovirus-mediated gene delivery of caveolin-1. J Biol Chem 275:: 20717--20725.
30. Galbiati F, Volonte D, Liu J, Capozza F, Frank PG, et al. ((2001)) Caveolin-1 expression negatively regulates cell cycle progression by inducing G(0)/G(1) arrest via a p53/p21(WAF1/Cip1)-dependent mechanism. Mol Biol Cell 12:: 2229--2244.
31. Liu J, Lee P, Galbiati F, Kitsis RN, Lisanti MP, ((2001)) Caveolin-1 expression sensitizes fibroblastic and epithelial cells to apoptotic stimulation. Am J Physiol Cell Physiol 280:: C823--835.
32. Fiucci G, Ravid D, Reich R, Liscovitch M, ((2002)) Caveolin-1 inhibits anchorage-independent growth, anoikis and invasiveness in MCF-7 human breast cancer cells. Oncogene 21:: 2365--2375.
33. Williams TM, Medina F, Badano I, Hazan RB, Hutchinson J, et al. ((2004)) 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 279:: 51630--51646.
34. Sloan EK, Stanley KL, Anderson RL, ((2004)) Caveolin-1 inhibits breast cancer growth and metastasis. Oncogene 23:: 7893--7897.
35. Sunaga N, Miyajima K, Suzuki M, Sato M, White MA, et al. ((2004)) Different roles for caveolin-1 in the development of non-small cell lung cancer versus small cell lung cancer. Cancer Res 64:: 4277--4285.
36. Fang K, Fu W, Beardsley AR, Sun X, Lisanti MP, et al. ((2007)) Overexpression of caveolin-1 inhibits endothelial cell proliferation by arresting the cell cycle at G0/G1 phase. Cell Cycle 6:: 199--204.
37. Nakashima H, Hamamura K, Houjou T, Taguchi R, Yamamoto N, et al. ((2007)) Overexpression of caveolin-1 in a human melanoma cell line results in dispersion of ganglioside GD3 from lipid rafts and alteration of leading edges, leading to attenuation of malignant properties. Cancer Sci 98:: 512--520.
38. Wu P, Wang X, Li F, Qi B, Zhu H, et al. ((2008)) Growth suppression of MCF-7 cancer cell-derived xenografts in nude mice by caveolin-1. Biochem Biophys Res Commun 376:: 215--220.
39. Shatz M, Lustig G, Reich R, Liscovitch M (2010) Caveolin-1 mutants P132L and Y14F are dominant negative regulators of invasion, migration and aggregation in H1299 lung cancer cells. Exp Cell Res.
40. Thomas NB, Hutcheson IR, Campbell L, Gee J, Taylor KM, et al. ((2010)) Growth of hormone-dependent MCF-7 breast cancer cells is promoted by constitutive caveolin-1 whose expression is lost in an EGF-R-mediated manner during development of tamoxifen resistance. Breast Cancer Res Treat 119:: 575--591.
41. Zhu H, Cai C, Chen J, ((2004)) Suppression of P-glycoprotein gene expression in Hs578T/Dox by the overexpression of caveolin-1. FEBS Lett 576:: 369--374.
42. Rajjayabun PH, Garg S, Durkan GC, Charlton R, Robinson MC, et al. ((2001)) Caveolin-1 expression is associated with high-grade bladder cancer. Urology 58:: 811--814.
43. Ito Y, Yoshida H, Nakano K, Kobayashi K, Yokozawa T, et al. ((2002)) Caveolin-1 overexpression is an early event in the progression of papillary carcinoma of the thyroid. Br J Cancer 86:: 912--916.
44. Kato K, Hida Y, Miyamoto M, Hashida H, Shinohara T, et al. ((2002)) Overexpression of caveolin-1 in esophageal squamous cell carcinoma correlates with lymph node metastasis and pathologic stage. Cancer 94:: 929--933.
45. Lee H, Park DS, Razani B, Russell RG, Pestell RG, et al. ((2002)) Caveolin-1 mutations (P132L and null) and the pathogenesis of breast cancer: caveolin-1 (P132L) behaves in a dominant-negative manner and caveolin-1 (-/-) null mice show mammary epithelial cell hyperplasia. Am J Pathol 161:: 1357--1369.
46. Campbell L, Gumbleton M, Griffiths DF, ((2003)) Caveolin-1 overexpression predicts poor disease-free survival of patients with clinically confined renal cell carcinoma. Br J Cancer 89:: 1909--1913.
47. Tanase CP, ((2008)) Caveolin-1: a marker for pancreatic cancer diagnosis. Expert Rev Mol Diagn 8:: 395--404.
48. Zhang ZB, Cai L, Zheng SG, Xiong Y, Dong JH, ((2009)) Overexpression of caveolin-1 in hepatocellular carcinoma with metastasis and worse prognosis: correlation with vascular endothelial growth factor, microvessel density and unpaired artery. Pathol Oncol Res 15:: 495--502.
49. Yeh D, Chen C, Sun MZ, Shao S, Hao L, et al. ((2009)) Caveolin-1 is an important factor for the metastasis and proliferation of human small cell lung cancer NCI-H446 cell. Anat Rec (Hoboken) 292:: 1584--1592.
50. Felicetti F, Parolini I, Bottero L, Fecchi K, Errico MC, et al. ((2009)) Caveolin-1 tumor-promoting role in human melanoma. Int J Cancer 125:: 1514--1522.
51. Thompson TC, Tahir SA, Li L, Watanabe M, Naruishi K, et al. ((2010)) The role of caveolin-1 in prostate cancer: clinical implications. Prostate Cancer Prostatic Dis 13:: 6--11.