Lipid rafts, caveolae, and epidermal growth factor receptor family: friends or foes?


Journal

Cell communication and signaling : CCS
ISSN: 1478-811X
Titre abrégé: Cell Commun Signal
Pays: England
ID NLM: 101170464

Informations de publication

Date de publication:
11 Oct 2024
Historique:
received: 18 08 2024
accepted: 05 10 2024
medline: 12 10 2024
pubmed: 12 10 2024
entrez: 11 10 2024
Statut: epublish

Résumé

Lipid rafts are dynamic microdomains enriched with cholesterol and sphingolipids that play critical roles in cellular processes by organizing and concentrating specific proteins involved in signal transduction. The interplay between lipid rafts, raft-associated caveolae and the human epidermal growth factor receptors has significant implications in cancer biology, particularly in breast and gastric cancer therapy resistance. This review examines the structural and functional characteristics of lipid rafts, their involvement in EGFR and HER2 signaling, and the impact of lipid rafts/CXCL12/CXCR4/HER2 axis on bone metastasis. We also discuss the potential of targeting lipid rafts and caveolin-1 to enhance therapeutic strategies against HER2-positive cancers and the impact of co-localization of trastuzumab or antibody drug conjugates with caveolin-1 on therapy response. Emerging evidence suggests that disrupting lipid raft integrity or silencing caveolin-1, through several strategies including cholesterol-lowering molecules, can influence HER2 availability and internalization, enhancing anti-HER2 targeted therapy and offering a novel approach to counteract drug resistance and improve treatment efficacy.

Identifiants

pubmed: 39394159
doi: 10.1186/s12964-024-01876-4
pii: 10.1186/s12964-024-01876-4
doi:

Substances chimiques

ErbB Receptors EC 2.7.10.1
Receptor, ErbB-2 EC 2.7.10.1

Types de publication

Journal Article Review

Langues

eng

Sous-ensembles de citation

IM

Pagination

489

Informations de copyright

© 2024. The Author(s).

Références

Li B, Qin Y, Yu X, Xu X, Yu W. Lipid raft involvement in signal transduction in cancer cell survival, cell death and metastasis. Cell Prolif. 2022;55:e13167. https://doi.org/10.1111/cpr.13167 .
doi: 10.1111/cpr.13167 pubmed: 34939255
Simons K, Toomre D. Lipid rafts and signal transduction, Nature reviews. Mol cell Biology. 2000;1:31–9. https://doi.org/10.1038/35036052 .
doi: 10.1038/35036052
Wiechen K, Sers C, Agoulnik A, Arlt K, Dietel M, Schlag PM, Schneider U. Down-regulation of caveolin-1, a candidate tumor suppressor gene, in sarcomas. Am J Pathol. 2001;158:833–9. https://doi.org/10.1016/S0002-9440(10)64031-X .
doi: 10.1016/S0002-9440(10)64031-X pubmed: 11238032 pmcid: 1850346
Greenlee JD, Subramanian T, Liu K, King MR. Rafting down the Metastatic Cascade: the role of lipid rafts in Cancer Metastasis, Cell Death, and clinical outcomes. Cancer Res. 2021;81:5–17. https://doi.org/10.1158/0008-5472.CAN-20-2199 .
doi: 10.1158/0008-5472.CAN-20-2199 pubmed: 32999001
Roskoski R. The ErbB/HER family of protein-tyrosine kinases and cancer. Pharmacol Res. 2014;79:34–74. https://doi.org/10.1016/j.phrs.2013.11.002 .
doi: 10.1016/j.phrs.2013.11.002 pubmed: 24269963
Ayati A, Moghimi S, Salarinejad S, Safavi M, Pouramiri B, Foroumadi A. A review on progression of epidermal growth factor receptor (EGFR) inhibitors as an efficient approach in cancer targeted therapy. Bioorg Chem. 2020;99:103811. https://doi.org/10.1016/j.bioorg.2020.103811 .
doi: 10.1016/j.bioorg.2020.103811 pubmed: 32278207
Swain SM, Shastry M, Hamilton E. Targeting HER2-positive breast cancer: advances and future directions, Nature reviews. Drug Discovery. 2023;22:101–26. https://doi.org/10.1038/s41573-022-00579-0 .
doi: 10.1038/s41573-022-00579-0 pubmed: 36344672
Rimawi MF, de Angelis C, Schiff R. Resistance to Anti-HER2 Therapies in Breast Cancer, American Society of Clinical Oncology educational book. American Society of Clinical Oncology. Annual Meeting (2015) e157-64. https://doi.org/10.14694/EdBook_AM.2015.35.e157
Chong CR, Jänne PA. The quest to overcome resistance to EGFR-targeted therapies in cancer. Nat Med. 2013;19:1389–400. https://doi.org/10.1038/nm.3388 .
doi: 10.1038/nm.3388 pubmed: 24202392 pmcid: 4049336
Chhouri H, Alexandre D, Grumolato L. Mechanisms of Acquired Resistance and Tolerance to EGFR targeted therapy in Non-small Cell Lung Cancer. Cancers. 2023;15. https://doi.org/10.3390/cancers15020504 .
Guidi L, Pellizzari G, Tarantino P, Valenza C, Curigliano G. Resistance to antibody-drug Conjugates Targeting HER2 in breast Cancer: Molecular Landscape and Future challenges. Cancers. 2023;15. https://doi.org/10.3390/cancers15041130 .
Wu S-G, Shih J-Y. Management of acquired resistance to EGFR TKI-targeted therapy in advanced non-small cell lung cancer. Mol Cancer. 2018;17:38. https://doi.org/10.1186/s12943-018-0777-1 .
doi: 10.1186/s12943-018-0777-1 pubmed: 29455650 pmcid: 5817870
Singer SJ, Nicolson GL. The fluid mosaic model of the structure of cell membranes. Sci (New York N Y). 1972;175:720–31. https://doi.org/10.1126/science.175.4023.720 .
doi: 10.1126/science.175.4023.720
Bagatolli LA, Mouritsen OG. Is the fluid mosaic (and the accompanying raft hypothesis) a suitable model to describe fundamental features of biological membranes? What may be missing? Front Plant Sci. 2013;4:457. https://doi.org/10.3389/fpls.2013.00457 .
doi: 10.3389/fpls.2013.00457 pubmed: 24312108 pmcid: 3826152
Yu J, Fischman DA, Steck TL. Selective solubilization of proteins and phospholipids from red blood cell membranes by nonionic detergents. J Supramolecular Struct. 1973;1:233–48. https://doi.org/10.1002/jss.400010308 .
doi: 10.1002/jss.400010308
Sezgin E, Schwille P. Fluorescence techniques to study lipid dynamics, Cold Spring Harbor perspectives in biology 3 (2011) a009803. https://doi.org/10.1101/cshperspect.a009803
Sezgin E, Levental I, Mayor S, Eggeling C. The mystery of membrane organization: composition, regulation and roles of lipid rafts, Nature reviews. Mol cell Biology. 2017;18:361–74. https://doi.org/10.1038/nrm.2017.16 .
doi: 10.1038/nrm.2017.16
Mollinedo F, Gajate C. Lipid rafts as signaling hubs in cancer cell survival/death and invasion: implications in tumor progression and therapy: Thematic Review Series: Biology of lipid rafts. J Lipid Res. 2020;61:611–35. https://doi.org/10.1194/jlr.TR119000439 .
doi: 10.1194/jlr.TR119000439 pubmed: 33715811 pmcid: 7193951
Simons K, van Meer G. Lipid sorting in epithelial cells. Biochemistry. 1988;27:6197–202. https://doi.org/10.1021/bi00417a001 .
doi: 10.1021/bi00417a001 pubmed: 3064805
Simons K, Ikonen E. Functional rafts in cell membranes. Nature. 1997;387:569–72. https://doi.org/10.1038/42408 .
doi: 10.1038/42408 pubmed: 9177342
Pike LJ. Rafts defined: a report on the Keystone Symposium on lipid rafts and cell function. J Lipid Res. 2006;47:1597–8. https://doi.org/10.1194/jlr.E600002-JLR200 .
doi: 10.1194/jlr.E600002-JLR200 pubmed: 16645198
Simons K, Ehehalt R. Cholesterol, lipid rafts, and disease. J Clin Investig. 2002;110:597–603. https://doi.org/10.1172/JCI16390 .
doi: 10.1172/JCI16390 pubmed: 12208858 pmcid: 151114
Reeves VL, Thomas CM, Smart EJ. Lipid rafts, caveolae and GPI-linked proteins, advances in experimental medicine and biology 729 (2012) 3–13. https://doi.org/10.1007/978-1-4614-1222-9_1
Rajendran L, Le Lay S, Illges H. Raft association and lipid droplet targeting of flotillins are independent of caveolin. Biol Chem. 2007;388:307–14. https://doi.org/10.1515/BC.2007.034 .
doi: 10.1515/BC.2007.034 pubmed: 17338638
Murata M, Peränen J, Schreiner R, Wieland F, Kurzchalia TV, Simons K. VIP21/caveolin is a cholesterol-binding protein. Proc Natl Acad Sci USA. 1995;92:10339–43. https://doi.org/10.1073/pnas.92.22.10339 .
doi: 10.1073/pnas.92.22.10339 pubmed: 7479780 pmcid: 40792
Ikonen E, Parton RG. Caveolins and cellular cholesterol balance, traffic (Copenhagen, Denmark) 1 (2000) 212–7. https://doi.org/10.1034/j.1600-0854.2000.010303.x
Williams TM, Lisanti MP. The caveolin proteins, genome biology 5 (2004) 214. https://doi.org/10.1186/gb-2004-5-3-214
Solomon KR, Danciu TE, Adolphson LD, Hecht LE, Hauschka PV. Caveolin-enriched membrane signaling complexes in human and murine osteoblasts. J bone Mineral Research: Official J Am Soc Bone Mineral Res. 2000;15:2380–90. https://doi.org/10.1359/jbmr.2000.15.12.2380 .
doi: 10.1359/jbmr.2000.15.12.2380
Solomon KR, Adolphson LD, Wank DA, McHugh KP, Hauschka PV. Caveolae in human and murine osteoblasts. J bone Mineral Research: Official J Am Soc Bone Mineral Res. 2000;15:2391–401. https://doi.org/10.1359/jbmr.2000.15.12.2391 .
doi: 10.1359/jbmr.2000.15.12.2391
Quest AFG, Leyton L, Párraga M. Caveolins, caveolae, and lipid rafts in cellular transport, signaling, and disease. Biochem cell Biology = Biochimie et Biol cellulaire. 2004;82:129–44. https://doi.org/10.1139/o03-071 .
doi: 10.1139/o03-071
YAMADA E. The fine structure of the gall bladder epithelium of the mouse. J Biophys Biochem Cytol. 1955;1:445–58. https://doi.org/10.1083/jcb.1.5.445 .
doi: 10.1083/jcb.1.5.445 pubmed: 13263332 pmcid: 2229656
Anderson RG. The caveolae membrane system, Annual review of biochemistry 67 (1998) 199–225. https://doi.org/10.1146/annurev.biochem.67.1.199
Galbiati F, Razani B, Lisanti MP. Emerging themes in lipid rafts and caveolae. Cell. 2001;106:403–11. https://doi.org/10.1016/S0092-8674(01)00472-X .
doi: 10.1016/S0092-8674(01)00472-X pubmed: 11525727
Gkantiragas I, Brügger B, Stüven E, Kaloyanova D, Li XY, Löhr K, Lottspeich F, Wieland FT, Helms JB. Sphingomyelin-enriched microdomains at the Golgi complex. Mol Biol Cell. 2001;12:1819–33. https://doi.org/10.1091/mbc.12.6.1819 .
doi: 10.1091/mbc.12.6.1819 pubmed: 11408588 pmcid: 37344
Lucero HA, Robbins PW. Lipid rafts-protein association and the regulation of protein activity, archives of biochemistry and biophysics 426 (2004) 208–24. https://doi.org/10.1016/j.abb.2004.03.020
Pike LJ. Growth factor receptors, lipid rafts and caveolae: an evolving story. Biochim Biophys Acta. 2005;1746:260–73. https://doi.org/10.1016/j.bbamcr.2005.05.005 .
doi: 10.1016/j.bbamcr.2005.05.005 pubmed: 15951036
Williams TM, Lisanti MP. Caveolin-1 in oncogenic transformation, cancer, and metastasis, American journal of physiology. Cell Physiol. 2005;288:C494–506. https://doi.org/10.1152/ajpcell.00458.2004 .
doi: 10.1152/ajpcell.00458.2004
Pereira PMR, Sharma SK, Carter LM, Edwards KJ, Pourat J, Ragupathi A, Janjigian YY, Durack JC, Lewis JS. Caveolin-1 mediates cellular distribution of HER2 and affects trastuzumab binding and therapeutic efficacy. Nat Commun. 2018;9:5137. https://doi.org/10.1038/s41467-018-07608-w .
doi: 10.1038/s41467-018-07608-w pubmed: 30510281 pmcid: 6277446
Quest AFG, Gutierrez-Pajares JL, Torres VA. Caveolin-1: an ambiguous partner in cell signalling and cancer. J Cell Mol Med. 2008;12:1130–50. https://doi.org/10.1111/j.1582-4934.2008.00331.x .
doi: 10.1111/j.1582-4934.2008.00331.x pubmed: 18400052 pmcid: 3865655
Cantiani L, Manara MC, Zucchini C, de Sanctis P, Zuntini M, Valvassori L, Serra M, Olivero M, Di Renzo MF, Colombo MP, Picci P, Scotlandi K. Caveolin-1 reduces osteosarcoma metastases by inhibiting c-Src activity and met signaling. Cancer Res. 2007;67:7675–85. https://doi.org/10.1158/0008-5472.CAN-06-4697 .
doi: 10.1158/0008-5472.CAN-06-4697 pubmed: 17699771
Qian X-L, Pan Y-H, Huang Q-Y, Shi Y-B, Huang Q-Y, Hu Z-Z, Xiong L-X. Caveolin-1: a multifaceted driver of breast cancer progression and its application in clinical treatment. OncoTargets Therapy. 2019;12:1539–52. https://doi.org/10.2147/OTT.S191317 .
doi: 10.2147/OTT.S191317 pubmed: 30881011 pmcid: 6398418
Patel HH, Insel PA. Lipid rafts and caveolae and their role in compartmentation of redox signaling. Antioxid Redox Signal. 2009;11:1357–72. https://doi.org/10.1089/ars.2008.2365 .
doi: 10.1089/ars.2008.2365 pubmed: 19061440 pmcid: 2757136
Martinez-Outschoorn UE, Sotgia F, Lisanti MP. Caveolae and signalling in cancer, Nature reviews. Cancer. 2015;15:225–37. https://doi.org/10.1038/nrc3915 .
doi: 10.1038/nrc3915 pubmed: 25801618
Yarden Y, Sliwkowski MX. Untangling the ErbB signalling network, Nature reviews. Mol cell Biology. 2001;2:127–37. https://doi.org/10.1038/35052073 .
doi: 10.1038/35052073
Yarden Y. Biology of HER2 and its importance in breast Cancer. Oncology. 2001;61:1–13. https://doi.org/10.1159/000055396 .
doi: 10.1159/000055396 pubmed: 11694782
Burgess AW, Cho H-S, Eigenbrot C, Ferguson KM, Garrett TPJ, Leahy DJ, Lemmon MA, Sliwkowski MX, Ward CW, Yokoyama S. An open-and-shut case? Recent insights into the activation of EGF/ErbB receptors, molecular cell 12 (2003) 541–52. https://doi.org/10.1016/s1097-2765(03)00350-2
Garrett TPJ, McKern NM, Lou M, Elleman TC, Adams TE, Lovrecz GO, Kofler M, Jorissen RN, Nice EC, Burgess AW, Ward CW. The crystal structure of a truncated ErbB2 ectodomain reveals an active conformation, poised to interact with other ErbB receptors, molecular cell 11 (2003) 495–505. https://doi.org/10.1016/s1097-2765(03)00048-0
Roepstorff K, Thomsen P, Sandvig K, van Deurs B. Sequestration of epidermal growth factor receptors in non-caveolar lipid rafts inhibits ligand binding. J Biol Chem. 2002;277:18954–60. https://doi.org/10.1074/jbc.M201422200 .
doi: 10.1074/jbc.M201422200 pubmed: 11886870
Ringerike T, Blystad FD, Levy FO, Madshus IH, Stang E. Cholesterol is important in control of EGF receptor kinase activity but EGF receptors are not concentrated in caveolae. J Cell Sci. 2002;115:1331–40. https://doi.org/10.1242/jcs.115.6.1331 .
doi: 10.1242/jcs.115.6.1331 pubmed: 11884532
Nagy P, Vereb G, Sebestyén Z, Horváth G, Lockett SJ, Damjanovich S, Park JW, Jovin TM, Szöllosi J. Lipid rafts and the local density of ErbB proteins influence the biological role of homo- and heteroassociations of ErbB2. J Cell Sci. 2002;115:4251–62. https://doi.org/10.1242/jcs.00118 .
doi: 10.1242/jcs.00118 pubmed: 12376557
Orr G, Hu D, Ozçelik S, Opresko LK, Wiley HS, Colson SD. Cholesterol dictates the freedom of EGF receptors and HER2 in the plane of the membrane. Biophys J. 2005;89:1362–73. https://doi.org/10.1529/biophysj.104.056192 .
doi: 10.1529/biophysj.104.056192 pubmed: 15908575 pmcid: 1366621
Campbell MR, Ruiz-Saenz A, Zhang Y, Peterson E, Steri V, Oeffinger J, Sampang M, Jura N, Moasser MM. Extensive conformational and physical plasticity protects HER2-HER3 tumorigenic signaling. Cell Rep. 2022;38:110285. https://doi.org/10.1016/j.celrep.2021.110285 .
doi: 10.1016/j.celrep.2021.110285 pubmed: 35108526 pmcid: 8865943
Kazazic M, Roepstorff K, Johannessen LE, Pedersen NM, van Deurs B, Stang E, Madshus IH. EGF-induced activation of the EGF receptor does not trigger mobilization of caveolae. Traffic. 2006;7:1518–27. https://doi.org/10.1111/j.1600-0854.2006.00487.x .
doi: 10.1111/j.1600-0854.2006.00487.x pubmed: 16984407
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. https://doi.org/10.1038/sj.onc.1207911 .
doi: 10.1038/sj.onc.1207911 pubmed: 15273741
Couet J, Sargiacomo M, Lisanti MP. Interaction of a receptor tyrosine kinase, EGF-R, with caveolins. Caveolin binding negatively regulates tyrosine and serine/threonine kinase activities. J Biol Chem. 1997;272:30429–38. https://doi.org/10.1074/jbc.272.48.30429 .
doi: 10.1074/jbc.272.48.30429 pubmed: 9374534
Pereira PMR, Mandleywala K, Ragupathi A, Lewis JS. Acute Statin Treatment improves antibody Accumulation in EGFR- and PSMA-Expressing tumors, clinical cancer research. Official J Am Association Cancer Res. 2020;26:6215–29. https://doi.org/10.1158/1078-0432.CCR-20-1960 .
doi: 10.1158/1078-0432.CCR-20-1960
Nagy P, Jenei A, Kirsch AK, Szöllosi J, Damjanovich S, Jovin TM. Activation-dependent clustering of the erbB2 receptor tyrosine kinase detected by scanning near-field optical microscopy. J Cell Sci. 1999;112(11):1733–41. https://doi.org/10.1242/jcs.112.11.1733 .
doi: 10.1242/jcs.112.11.1733 pubmed: 10318765
Albanell J, Baselga J. Trastuzumab, a humanized anti-HER2 monoclonal antibody, for the treatment of breast cancer. Drugs Today (Barcelona Spain: 1998). 1999;35:931–46.
doi: 10.1358/dot.1999.35.12.564040
Alawin OA, Ahmed RA, Ibrahim BA, Briski KP, Sylvester PW. Antiproliferative effects of γ-tocotrienol are associated with lipid raft disruption in HER2-positive human breast cancer cells. J Nutr Biochem. 2016;27:266–77. https://doi.org/10.1016/j.jnutbio.2015.09.018 .
doi: 10.1016/j.jnutbio.2015.09.018 pubmed: 26507543
Sottocornola E, Misasi R, Mattei V, Ciarlo L, Gradini R, Garofalo T, Berra B, Colombo I, Sorice M. Role of gangliosides in the association of ErbB2 with lipid rafts in mammary epithelial HC11 cells. FEBS J. 2006;273:1821–30. https://doi.org/10.1111/j.1742-4658.2006.05203.x .
doi: 10.1111/j.1742-4658.2006.05203.x pubmed: 16623716
Jeong J, Shin JH, Li W, Hong JY, Lim J, Hwang JY, Chung J-J, Yan Q, Liu Y, Choi J, Wysolmerski J. MAL2 mediates the formation of stable HER2 signaling complexes within lipid raft-rich membrane protrusions in breast cancer cells. Cell Rep. 2021;37:110160. https://doi.org/10.1016/j.celrep.2021.110160 .
doi: 10.1016/j.celrep.2021.110160 pubmed: 34965434 pmcid: 8762588
Sung M, Tan X, Lu B, Golas J, Hosselet C, Wang F, Tylaska L, King L, Zhou D, Dushin R, Myers JS, Rosfjord E, Lucas J, Gerber H-P, Loganzo F. Caveolae-Mediated Endocytosis as a Novel mechanism of resistance to Trastuzumab Emtansine (T-DM1), molecular cancer therapeutics 17 (2018) 243–53. https://doi.org/10.1158/1535-7163.MCT-17-0403
Pereira PMR, Mandleywala K, Monette S, Lumish M, Tully KM, Panikar SS, Cornejo M, Mauguen A, Ragupathi A, Keltee NC, Mattar M, Janjigian YY, Lewis JS. Caveolin-1 temporal modulation enhances antibody drug efficacy in heterogeneous gastric cancer. Nat Commun. 2022;13:2526. https://doi.org/10.1038/s41467-022-30142-9 .
doi: 10.1038/s41467-022-30142-9 pubmed: 35534471 pmcid: 9085816
Pereira PMR, Mandleywala K, Ragupathi A, Carter LM, Goos JACM, Janjigian YY, Lewis JS. Temporal modulation of HER2 membrane availability increases Pertuzumab Uptake and Pretargeted Molecular Imaging of Gastric Tumors, Journal of nuclear medicine: official publication. Soc Nuclear Med. 2019;60:1569–78. https://doi.org/10.2967/jnumed.119.225813 .
doi: 10.2967/jnumed.119.225813
Manafi-Farid R, Ataeinia B, Ranjbar S, Jamshidi Araghi Z, Moradi MM, Pirich C, Beheshti M. ImmunoPET: antibody-based PET imaging in solid tumors. Front Med. 2022;9:916693. https://doi.org/10.3389/fmed.2022.916693 .
doi: 10.3389/fmed.2022.916693
Brown EL, Shmuel S, Mandleywala K, Panikar SS, Berry N-K, Rao Y, Zidel A, Lewis JS, Pereira PMR. Immuno-PET detects antibody-drug potency on Coadministration with statins, Journal of nuclear medicine: official publication. Soc Nuclear Med. 2023;64:1638–46. https://doi.org/10.2967/jnumed.122.265172 .
doi: 10.2967/jnumed.122.265172
Rao Y, Samuels Z, Carter LM, Monette S, Panikar SS, Pereira PMR, Lewis JS. Statins enhance the efficacy of HER2-targeting radioligand therapy in drug-resistant gastric cancers. Proc Natl Acad Sci USA. 2023;120:e2220413120. https://doi.org/10.1073/pnas.2220413120 .
doi: 10.1073/pnas.2220413120 pubmed: 36972439 pmcid: 10083538
Surendra Panikar S, Shmuel S, Lewis JS, Pereira PMR. PET and optical imaging of Caveolin-1 in gastric tumors. ACS Omega. 2023;8:35884–92. https://doi.org/10.1021/acsomega.3c03614 .
doi: 10.1021/acsomega.3c03614 pubmed: 37810678 pmcid: 10552508
Valastyan S, Weinberg RA. Tumor metastasis: molecular insights and evolving paradigms. Cell. 2011;147:275–92. https://doi.org/10.1016/j.cell.2011.09.024 .
doi: 10.1016/j.cell.2011.09.024 pubmed: 22000009 pmcid: 3261217
Chinni SR, Yamamoto H, Dong Z, Sabbota A, Bonfil RD, Cher ML. CXCL12/CXCR4 transactivates HER2 in lipid rafts of prostate cancer cells and promotes growth of metastatic deposits in bone. Mol cancer Research: MCR. 2008;6:446–57. https://doi.org/10.1158/1541-7786.MCR-07-0117 .
doi: 10.1158/1541-7786.MCR-07-0117 pubmed: 18337451

Auteurs

Francesca Ruzzi (F)

Laboratory of Immunology and Biology of Metastasis, Department of Medical and Surgical Sciences (DIMEC), University of Bologna, Bologna, 40126, Italy.

Chiara Cappello (C)

Laboratory of Immunology and Biology of Metastasis, Department of Medical and Surgical Sciences (DIMEC), University of Bologna, Bologna, 40126, Italy.

Maria Sofia Semprini (MS)

Laboratory of Immunology and Biology of Metastasis, Department of Medical and Surgical Sciences (DIMEC), University of Bologna, Bologna, 40126, Italy.

Laura Scalambra (L)

Laboratory of Immunology and Biology of Metastasis, Department of Medical and Surgical Sciences (DIMEC), University of Bologna, Bologna, 40126, Italy.

Stefania Angelicola (S)

Laboratory of Immunology and Biology of Metastasis, Department of Medical and Surgical Sciences (DIMEC), University of Bologna, Bologna, 40126, Italy.
IRCCS Azienda Ospedaliera Universitaria di Bologna, Bologna, 40138, Italy.

Olga Maria Pittino (OM)

Laboratory of Immunology and Biology of Metastasis, Department of Medical and Surgical Sciences (DIMEC), University of Bologna, Bologna, 40126, Italy.

Lorena Landuzzi (L)

Experimental Oncology Laboratory, IRCCS Istituto Ortopedico Rizzoli, Bologna, 40136, Italy.

Arianna Palladini (A)

Department of Molecular Medicine, University of Pavia, Pavia, 27100, Italy.
Unità Operativa di Oncologia, Fondazione IRCCS Policlinico San Matteo, Pavia, 27100, Italy.

Patrizia Nanni (P)

Laboratory of Immunology and Biology of Metastasis, Department of Medical and Surgical Sciences (DIMEC), University of Bologna, Bologna, 40126, Italy.

Pier-Luigi Lollini (PL)

Laboratory of Immunology and Biology of Metastasis, Department of Medical and Surgical Sciences (DIMEC), University of Bologna, Bologna, 40126, Italy. pierluigi.lollini@unibo.it.
IRCCS Azienda Ospedaliera Universitaria di Bologna, Bologna, 40138, Italy. pierluigi.lollini@unibo.it.

Articles similaires

[Redispensing of expensive oral anticancer medicines: a practical application].

Lisanne N van Merendonk, Kübra Akgöl, Bastiaan Nuijen
1.00
Humans Antineoplastic Agents Administration, Oral Drug Costs Counterfeit Drugs

Smoking Cessation and Incident Cardiovascular Disease.

Jun Hwan Cho, Seung Yong Shin, Hoseob Kim et al.
1.00
Humans Male Smoking Cessation Cardiovascular Diseases Female
Humans United States Aged Cross-Sectional Studies Medicare Part C
1.00
Humans Yoga Low Back Pain Female Male

Classifications MeSH