Microenvironment rigidity modulates responses to the HER2 receptor tyrosine kinase inhibitor lapatinib via YAP and TAZ transcription factors

Molecular Biology of the Cell

Volumn 26, Issue 22, 2015, Pages 3946-3953

  Lin, Chun Han ^a,b   Pelissier, Fanny A ^a,c   Zhang, Hui ^d   Lakins, Jon ^d   Weaver, Valerie M ^d   Park, Catherine ^d   LaBarge, Mark A ^a  

^a LAWRENCE BERKELEY NATIONAL LABORATORY   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c UNIVERSITY OF BERGEN   (Norway)

^d UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

EPIDERMAL GROWTH FACTOR RECEPTOR 2; LAPATINIB; MESSENGER RNA; RHO KINASE; SMALL INTERFERING RNA; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR TAZ; TRANSCRIPTION FACTOR YAP; TRANSFORMING GROWTH FACTOR ALPHA; UNCLASSIFIED DRUG; VERTEPORFIN; ANTINEOPLASTIC AGENT; ERBB2 PROTEIN, HUMAN; NUCLEAR PROTEIN; PORPHYRIN; PROTEIN KINASE INHIBITOR; QUINAZOLINE DERIVATIVE; TAZ PROTEIN, HUMAN; YY1AP1 PROTEIN, HUMAN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIPROLIFERATIVE ACTIVITY; ARTICLE; BREAST CANCER; BREAST CANCER CELL LINE; CANCER RESISTANCE; CANCER SIZE; CELL ADHESION; CELL PROLIFERATION; CONTROLLED STUDY; DOWN REGULATION; EXTRACELLULAR MATRIX; FEMALE; HUMAN; HUMAN CELL; IN VIVO STUDY; MECHANOTRANSDUCTION; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; TRANSCRIPTION INITIATION; TREATMENT RESPONSE; TUMOR MICROENVIRONMENT; YOUNG MODULUS; ANIMAL; ANTAGONISTS AND INHIBITORS; BREAST NEOPLASMS; DRUG EFFECTS; DRUG RESISTANCE; DRUG SCREENING; ENZYMOLOGY; GENETICS; KNOCKOUT MOUSE; METABOLISM; NUDE MOUSE; PATHOLOGY; SIGNAL TRANSDUCTION; TUMOR CELL LINE;

ANIMALS; ANTINEOPLASTIC AGENTS; BREAST NEOPLASMS; CELL LINE, TUMOR; CELL PROLIFERATION; DOWN-REGULATION; DRUG RESISTANCE, NEOPLASM; FEMALE; HUMANS; MICE; MICE, KNOCKOUT; MICE, NUDE; NUCLEAR PROTEINS; PORPHYRINS; PROTEIN KINASE INHIBITORS; QUINAZOLINES; RECEPTOR, ERBB-2; RNA, SMALL INTERFERING; SIGNAL TRANSDUCTION; TRANSCRIPTION FACTORS; TUMOR MICROENVIRONMENT; XENOGRAFT MODEL ANTITUMOR ASSAYS;

EID: 84946781278     PISSN: 10591524     EISSN: 19394586     Source Type: Journal    
DOI: 10.1091/mbc.E15-07-0456     Document Type: Article

References (50)

1. Amin DN, Sergina N, Ahuja D, McMahon M, Blair JA, Wang D, Hann B, Koch KM, Shokat KM, Moasser MM (2010). Resiliency and vulnerability in the HER2-HER3 tumorigenic driver. Sci Transl Med 2, 16ra17.
2. Baker BM, Chen CS (2012). Deconstructing the third dimension-how 3D culture microenvironments alter cellular cues. J Cell Sci 125, 3015-3024.
3. Burris HA 3rd, Hurwitz HI, Dees EC, Dowlati A, Blackwell KL, O'Neil B, Mar-com PK, Ellis MJ, Overmoyer B, Jones SF, et al. (2005). Phase I safety, pharmacokinetics, and clinical activity study of lapatinib (GW572016), a reversible dual inhibitor of epidermal growth factor receptor tyrosine kinases, in heavily pretreated patients with metastatic carcinomas. J Clin Oncol 23, 5305-5313.
4. Calvo F, Ege N, Grande-Garcia A, Hooper S, Jenkins RP, Chaudhry SI, Harrington K, Williamson P, Moeendarbary E, Charras G, Sahai E (2013). Mechanotransduction and YAP-dependent matrix remodelling is required for the generation and maintenance of cancer-associated fbroblasts. Nat Cell Biol 15, 637-646.
5. Chen CT, Kim H, Liska D, Gao S, Christensen JG, Weiser MR (2012). MET activation mediates resistance to lapatinib inhibition of HER2-amplifed gastric cancer cells. Mol Cancer Ther 11, 660-669.
6. Dupont S, Morsut L, Aragona M, Enzo E, Giulitti S, Cordenonsi M, Zanco-nato F, Le Digabel J, Forcato M, Bicciato S, et al. (2011). Role of YAP/TAZ in mechanotransduction. Nature 474, 179-183.
7. Garrett JT, Olivares MG, Rinehart C, Granja-Ingram ND, Sanchez V, Chakrabarty A, Dave B, Cook RS, Pao W, McKinely E, et al. (2011). Transcriptional and posttranslational up-regulation of HER3 (ErbB3) compensates for inhibition of the HER2 tyrosine kinase. Proc Natl Acad Sci USA 108, 5021-5026.
8. Halder G, Dupont S, Piccolo S (2012). Transduction of mechanical and cyto-skeletal cues by YAP and TAZ. Nat Rev. Mol Cell Biol 13, 591-600.
9. Higginbotham JN, Demory Beckler M, Gephart JD, Franklin JL, Bogatcheva G, Kremers GJ, Piston DW, Ayers GD, McConnell RE, Tyska MJ, Coffey RJ (2011). Amphiregulin exosomes increase cancer cell invasion. Curr Biol 21, 779-786.
10. Hobor S, Van Emburgh BO, Crowley E, Misale S, Di Nicolantonio F, Bardelli A (2014). TGF-alpha and amphiregulin paracrine network promotes resistance to EGFR blockade in colorectal cancer cells. Clin Cancer Res 20, 6429-6438.
11. Hossain Z, Ali SM, Ko HL, Xu J, Ng C P, Guo K, Qi Z, Ponniah S, Hong W, Hunziker W (2007). Glomerulocystic kidney disease in mice with a targeted inactivation of Wwtr1. Proc Natl Acad Sci USA 104, 1631-1636.
12. Hurbin A, Dubrez L, Coll JL, Favrot MC (2002). Inhibition of apoptosis by amphiregulin via an insulin-like growth factor-1 receptor-dependent pathway in non-small cell lung cancer cell lines. J Biol Chem 277, 49127-49133.
13. Kim M, Agarwal S, Tripathy D (2013). Updates on the treatment of human epidermal growth factor receptor type 2-positive breast cancer. Curr Opin Obstet Gynecol 26, 27-33.
14. Kim SK, Jung WH, Koo JS (2014). Yes-associated protein (YAP) is differentially expressed in tumor and stroma according to the molecular subtype of breast cancer. Int J Clin Exp Pathol 7, 3224-3234.
15. Koboldt DC, Fulton RS, McLellan MD, Schmidt H, Kalicki-Veizer J, McMichael JF, Fulton LL, Dooling DJ, Ding L, Mardis ER, et al. (2012). Comprehensive molecular portraits of human breast tumours. Nature 490, 61-70.
16. Kolahi KS, Donjacour A, Liu X, Lin W, Simbulan RK, Bloise E, Maltepe E, Rinaudo P (2012). Effect of substrate stiffness on early mouse embryo development. PLoS One 7, e41717.
17. Kun Y, How LC, Hoon T P, Bajic VB, Lam TS, Aggarwal A, Sze HG, Bok WS, Yin WC, Tan P (2003). Classifying the estrogen receptor status of breast cancers by expression profles reveals a poor prognosis subpopulation exhibiting high expression of the ERBB2 receptor. Hum Mol Genet 12, 3245-3258.
18. Labarge MA, Parvin B, Lorens JB (2014). Molecular deconstruction, detection, and computational prediction of microenvironment-modulated cellular responses to cancer therapeutics. Adv Drug Deliv Rev 70, 123-131.
19. Lamar JM, Stern P, Liu H, Schindler JW, Jiang ZG, Hynes RO (2012). The Hippo pathway target, YAP, promotes metastasis through its TEAD-interaction domain. Proc Natl Acad Sci USA 109, E2441-2450.
20. Lee GY, Kenny PA, Lee EH, Bissell MJ (2007). Three-dimensional culture models of normal and malignant breast epithelial cells. Nat Methods 4, 359-365.
21. Levental I, Georges PC, Janmey PA (2007). Soft biological materials and their impact on cell function. Soft Matter 3, 299-306.
22. Liu L, Greger J, Shi H, Liu Y, Greshock J, Annan R, Halsey W, Sathe GM, Martin AM, Gilmer TM (2009). Novel mechanism of lapatinib resistance in HER2-positive breast tumor cells: activation of AXL. Cancer Res 69, 6871-6878.
23. Liu-Chittenden Y, Huang B, Shim JS, Chen Q, Lee SJ, Anders RA, Liu JO, Pan D (2012). Genetic and pharmacological disruption of the TEAD-YAP complex suppresses the oncogenic activity of YAP. Genes Dev 26, 1300-1305.
24. Medina PJ, Goodin S (2008). Lapatinib: a dual inhibitor of human epidermal growth factor receptor tyrosine kinases. Clin Ther 30, 1426-1447.
25. Michels S, Schmidt-Erfurth U (2001). Photodynamic therapy with verteporfn: a new treatment in ophthalmology. Semin Ophthalmol 16, 201-206.
26. Morin-Kensicki EM, Boone BN, Howell M, Stonebraker JR, Teed J, Alb JG, Magnuson TR, O'Neal W, Milgram SL (2006). Defects in yolk sac vascu-logenesis, chorioallantoic fusion, and embryonic axis elongation in mice with targeted disruption of Yap65. Mol Cell Biol 26, 77-87.
27. Mouw JK, Yui Y, Damiano L, Bainer RO, Lakins JN, Acerbi I, Ou G, Wijekoon AC, Levental KR, Gilbert PM, et al. (2014). Tissue mechanics modulate microRNA-dependent PTEN expression to regulate malignant progression. Nat Med 20, 360-367.
28. Neve RM, Chin K, Fridlyand J, Yeh J, Baehner FL, Fevr T, Clark L, Bayani N, Coppe J P, Tong F, et al. (2006). A collection of breast cancer cell lines for the study of functionally distinct cancer subtypes. Cancer Cell 10, 515-527.
29. Nguyen T V, Sleiman M, Moriarty T, Herrick WG, Peyton SR (2014). Sorafenib resistance and JNK signaling in carcinoma during extracellular matrix stiffening. Biomaterials 35, 5749-5759.
30. Paszek MJ, DuFort CC, Rossier O, Bainer R, Mouw JK, Godula K, Hudak JE, Lakins JN, Wijekoon AC, Cassereau L, et al. (2014). The cancer glycoca-lyx mechanically primes integrin-mediated growth and survival. Nature 511, 319-325.
31. Paszek MJ, Zahir N, Johnson KR, Lakins JN, Rozenberg GI, Gefen A, Reinhart-King CA, Margulies SS, Dembo M, Boettiger D, et al. (2005). Tensional homeostasis and the malignant phenotype. Cancer Cell 8, 241-254.
32. Pelissier FA, Garbe JC, Ananthanarayanan B, Miyano M, Lin C, Jokela T, Kumar S, Stampfer MR, Lorens JB, LaBarge MA (2014). Age-related dysfunction in mechanotransduction impairs differentiation of human mammary epithelial progenitors. Cell Rep 7, 1926-1939.
33. Rexer BN, Arteaga CL (2012). Intrinsic and acquired resistance to HER2-targeted therapies in HER2 gene-amplifed breast cancer: mechanisms and clinical implications. Crit Rev Oncog 17, 1-16.
34. Rubashkin MG, Cassereau L, Bainer R, DuFort CC, Yui Y, Ou G, Paszek MJ, Davidson MW, Chen YY, Weaver VM (2014). Force engages vinculin and promotes tumor progression by enhancing PI3K activation of phosphati-dylinositol (3, 4, 5)-triphosphate. Cancer Res 74, 4597-4611.
35. Rusnak DW, Alligood KJ, Mullin RJ, Spehar GM, Arenas-Elliott C, Martin AM, Degenhardt Y, Rudolph SK, Haws TF Jr, Hudson-Curtis BL, Gilmer TM (2007). Assessment of epidermal growth factor receptor (EGFR, ErbB1) and HER2 (ErbB2) protein expression levels and response to lapatinib (Tykerb, GW572016) in an expanded panel of human normal and tumour cell lines. Cell Prolif 40, 580-594.
36. Saruwatari L, Aita H, Butz F, Nakamura HK, Ouyang J, Yang Y, Chiou WA, Ogawa T (2005). Osteoblasts generate harder, stiffer, and more delamination-resistant mineralized tissue on titanium than on polystyrene, associated with distinct tissue micro-and ultrastructure. J Bone Miner Res 20, 2002-2016.
37. Schrader J, Gordon-Walker TT, Aucott RL, van Deemter M, Quaas A, Walsh S, Benten D, Forbes SJ, Wells RG, Iredale JP (2011). Matrix stiffness modulates proliferation, chemotherapeutic response, and dormancy in hepatocellular carcinoma cells. Hepatology 53, 1192-1205.
38. Sharma S, Santiskulvong C, Rao J, Gimzewski JK, Dorigo O (2014). The role of Rho GTPase in cell stiffness and cisplatin resistance in ovarian cancer cells. Integr Biol 6, 611-617.
39. Soof SS, Last JA, Liliensiek SJ, Nealey PF, Murphy CJ (2009). The elastic modulus of Matrigel as determined by atomic force microscopy. J Struct Biol 167, 216-219.
40. Ts e JR, Engler AJ (2010). Preparation of hydrogel substrates with tunable mechanical properties. Curr Protoc Cell Biol Chapter 10, Unit 10.16.
41. Tufail R, Jorda M, Zhao W, Reis I, Nawaz Z (2012). Loss of Yes-associated protein (YAP) expression is associated with estrogen and progesterone receptors negativity in invasive breast carcinomas. Breast Cancer Res Treatment 131, 743-750.
42. Wang X, Su L, Ou Q (2012). Yes-associated protein promotes tumour development in luminal epithelial derived breast cancer. Eur J Cancer 48, 1227-1234.
43. Weaver VM, Lelievre S, Lakins JN, Chrenek MA, Jones JC, Giancotti F, Werb Z, Bissell MJ (2002). beta4 integrin-dependent formation of polarized three-dimensional architecture confers resistance to apoptosis in normal and malignant mammary epithelium. Cancer Cell 2, 205-216.
44. Weigelt B, Lo AT, Park CC, Gray JW, Bissell MJ (2010). HER2 signaling pathway activation and response of breast cancer cells to HER2-target-ing agents is dependent strongly on the 3D microenvironment. Breast Cancer Res Treatment 122, 35-43.
45. Xia W, Petricoin EF 3rd, Zhao S, Liu L, Osada T, Cheng Q, Wulfkuhle JD, Gwin WR, Yang X, Gallagher RI, Bacus S, Lyerly HK, Spector NL (2013). An heregulin-EGFR-HER3 autocrine signaling axis can mediate acquired lapa-tinib resistance in HER2+ breast cancer models. Breast Cancer Res 15, R85.
46. Yotsumoto F, Fukami T, Yagi H, Funakoshi A, Yoshizato T, Kuroki M, Miyamoto S (2010). Amphiregulin regulates the activation of ERK and Akt through epidermal growth factor receptor and HER3 signals involved in the progression of pancreatic cancer. Cancer Sci 101, 2351-2360.
47. Yuan M, Tomlinson V, Lara R, Holliday D, Chelala C, Harada T, Gangeswaran R, Manson-Bishop C, Smith P, Danovi SA, et al. (2008). Yes-associated protein (YAP) functions as a tumor suppressor in breast. Cell Death Differ 15, 1752-1759.
48. Zhang J, Ji JY, Yu M, Overholtzer M, Smolen GA, Wang R, Brugge JS, Dyson NJ, Haber DA (2009). YAP-dependent induction of amphiregulin identifes a non-cell-autonomous component of the Hippo pathway. Nat Cell Biol 11, 1444-1450.
49. Zhao B, Wei X, Li W, Udan RS, Yang Q, Kim J, Xie J, Ikenoue T, Yu J, Li L, et al. (2007). Inactivation of YAP oncoprotein by the Hippo pathway is involved in cell contact inhibition and tissue growth control. Genes Dev 21, 2747-2761.
50. Zustiak S, Nossal R, Sackett DL (2014). Multiwell stiffness assay for the study of cell responsiveness to cytotoxic drugs. Biotechnol Bioeng 111, 396-403.