ROCK inhibition promotes microtentacles that enhance reattachment of breast cancer cells

Oncotarget

Volumn 6, Issue 8, 2015, Pages 6251-6266

  Bhandary, Lekhana ^a   Whipple, Rebecca A ^a   Vitolo, Michele I ^a   Charpentier, Monica S ^a   Boggs, Amanda E ^a   Chakrabarti, Kristi R ^a   Thompson, Keyata N ^a   Martin, Stuart S ^a  

^a UNIVERSITY OF MARYLAND SCHOOL OF MEDICINE   (United States)

Author keywords

Breast cancer metastasis; Microtentacles; Reattachment; ROCK; Y 27632

Indexed keywords

4 (1 AMINOETHYL) N (4 PYRIDYL)CYCLOHEXANECARBOXAMIDE; ACTIN; MYOSIN ADENOSINE TRIPHOSPHATASE; RHO KINASE; AMIDE; PROTEIN KINASE INHIBITOR; PYRIDINE DERIVATIVE;

ACTIN FILAMENT; ARTICLE; BREAST CANCER CELL LINE; CELL ADHESION; CELL REATTACHMENT; CELL SHAPE; CIRCULATING TUMOR CELL; CONTROLLED STUDY; METASTASIS POTENTIAL; MICROTENTACLE; MICROTUBULE; SIGNAL TRANSDUCTION; ANTAGONISTS AND INHIBITORS; BREAST TUMOR; CYTOSKELETON; DRUG EFFECTS; ENZYMOLOGY; FEMALE; HUMAN; METABOLISM; METASTASIS; PATHOLOGY; TUMOR CELL LINE; TUMOR EMBOLISM;

ACTOMYOSIN; AMIDES; BREAST NEOPLASMS; CELL ADHESION; CELL LINE, TUMOR; CYTOSKELETON; FEMALE; HUMANS; NEOPLASM METASTASIS; NEOPLASTIC CELLS, CIRCULATING; PROTEIN KINASE INHIBITORS; PYRIDINES; RHO-ASSOCIATED KINASES;

EID: 84925606323     PISSN: None     EISSN: 19492553     Source Type: Journal    
DOI: 10.18632/oncotarget.3360     Document Type: Article

References (57)

1. Chambers AF, Groom AC and MacDonald IC. Dissemination and growth of cancer cells in metastatic sites. Nature reviews Cancer. 2002; 2(8):563-572.
2. Yilmaz M and Christofori G. EMT, the cytoskeleton, and cancer cell invasion. Cancer metastasis reviews. 2009; 28(1-2):15-33.
3. Glinsky VV, Glinsky GV, Glinskii OV, Huxley VH, Turk JR, Mossine VV, Deutscher SL, Pienta KJ and Quinn TP. Intravascular metastatic cancer cell homotypic aggregation at the sites of primary attachment to the endothelium. Cancer research. 2003; 63(13):3805-3811.
4. Riento K and Ridley AJ. Rocks: multifunctional kinases in cell behaviour. Nature reviews Molecular cell biology. 2003; 4(6):446-456.
5. Matsui T, Amano M, Yamamoto T, Chihara K, Nakafuku M, Ito M, Nakano T, Okawa K, Iwamatsu A and Kaibuchi K. Rho-associated kinase, a novel serine/threonine kinase, as a putative target for small GTP binding protein Rho. The EMBO journal. 1996; 15(9):2208-2216.
6. Lane J, Martin TA, Watkins G, Mansel RE and Jiang WG. The expression and prognostic value of ROCK I and ROCK II and their role in human breast cancer. International journal of oncology. 2008; 33(3):585-593.
7. Kamai T, Tsujii T, Arai K, Takagi K, Asami H, Ito Y and Oshima H. Significant association of Rho/ROCK pathway with invasion and metastasis of bladder cancer. Clinical cancer research: an official journal of the American Association for Cancer Research. 2003; 9(7):2632-2641.
8. Mertsch S and Thanos S. Opposing signaling of ROCK1 and ROCK2 determines the switching of substrate specificity and the mode of migration of glioblastoma cells. Molecular neurobiology. 2014; 49(2):900-915.
9. Itoh K, Yoshioka K, Akedo H, Uehata M, Ishizaki T and Narumiya S. An essential part for Rho-associated kinase in the transcellular invasion of tumor cells. Nature medicine. 1999; 5(2):221-225.
10. Amano M, Ito M, Kimura K, Fukata Y, Chihara K, Nakano T, Matsuura Y and Kaibuchi K. Phosphorylation and activation of myosin by Rho-associated kinase (Rho-kinase). The Journal of biological chemistry. 1996; 271(34):20246-20249.
11. Kimura K, Ito M, Amano M, Chihara K, Fukata Y, Nakafuku M, Yamamori B, Feng J, Nakano T, Okawa K, Iwamatsu A and Kaibuchi K. Regulation of myosin phosphatase by Rho and Rho-associated kinase (Rho-kinase). Science. 1996; 273(5272):245-248.
12. Maekawa M, Ishizaki T, Boku S, Watanabe N, Fujita A, Iwamatsu A, Obinata T, Ohashi K, Mizuno K and Narumiya S. Signaling from Rho to the actin cytoskeleton through protein kinases ROCK and LIM-kinase. Science. 1999; 285(5429):895-898.
13. Wittmann T and Waterman-Storer CM. Cell motility: can Rho GTPases and microtubules point the way? Journal of cell science. 2001; 114(Pt 21):3795-3803.
14. Wen Y, Eng CH, Schmoranzer J, Cabrera-Poch N, Morris EJ, Chen M, Wallar BJ, Alberts AS and Gundersen GG. EB1 and APC bind to mDia to stabilize microtubules downstream of Rho and promote cell migration. Nature cell biology. 2004; 6(9):820-830.
15. Amano M, Kaneko T, Maeda A, Nakayama M, Ito M, Yamauchi T, Goto H, Fukata Y, Oshiro N, Shinohara A, Iwamatsu A and Kaibuchi K. Identification of Tau and MAP2 as novel substrates of Rho-kinase and myosin phosphatase. Journal of neurochemistry. 2003; 87(3):780-790.
16. Schofield AV, Steel R and Bernard O. Rho-associated coiled-coil kinase (ROCK) protein controls microtubule dynamics in a novel signaling pathway that regulates cell migration. The Journal of biological chemistry. 2012; 287(52):43620-43629.
17. Chang YC, Nalbant P, Birkenfeld J, Chang ZF and Bokoch GM. GEF-H1 couples nocodazole-induced microtubule disassembly to cell contractility via RhoA. Molecular biology of the cell. 2008; 19(5):2147-2153.
18. Krendel M, Zenke FT and Bokoch GM. Nucleotide exchange factor GEF-H1 mediates cross-talk between microtubules and the actin cytoskeleton. Nature cell biology. 2002; 4(4):294-301.
19. Gutjahr MC, Rossy J and Niggli V. Role of Rho, Rac, and Rho-kinase in phosphorylation of myosin light chain, development of polarity, and spontaneous migration of Walker 256 carcinosarcoma cells. Experimental cell research. 2005; 308(2):422-438.
20. Torka R, Thuma F, Herzog V and Kirfel G. ROCK signaling mediates the adoption of different modes of migration and invasion in human mammary epithelial tumor cells. Experimental cell research. 2006; 312(19):3857-3871.
21. Patel RA, Liu Y, Wang B, Li R and Sebti SM. Identification of novel ROCK inhibitors with anti-migratory and anti-invasive activities. Oncogene. 2014; 33(5):550-555.
22. Cristofanilli M, Budd GT, Ellis MJ, Stopeck A, Matera J, Miller MC, Reuben JM, Doyle GV, Allard WJ, Terstappen LW and Hayes DF. Circulating tumor cells, disease progression, and survival in metastatic breast cancer. The New England journal of medicine. 2004; 351(8):781-791.
23. Banys M, Muller V, Melcher C, Aktas B, Kasimir-Bauer S, Hagenbeck C, Hartkopf A and Fehm T. Circulating tumor cells in breast cancer. Clinica chimica acta; international journal of clinical chemistry. 2013; 423:39-45.
24. Camara O, Kavallaris A, Noschel H, Rengsberger M, Jorke C and Pachmann K. Seeding of epithelial cells into circulation during surgery for breast cancer: the fate of malignant and benign mobilized cells. World journal of surgical oncology. 2006; 4:67.
25. Goldfarb Y and Ben-Eliyahu S. Surgery as a risk factor for breast cancer recurrence and metastasis: mediating mechanisms and clinical prophylactic approaches. Breast disease. 2006; 26:99-114.
26. Whipple RA, Cheung AM and Martin SS. Detyrosinated microtubule protrusions in suspended mammary epithelial cells promote reattachment. Experimental cell research. 2007; 313(7):1326-1336.
27. Matrone MA, Whipple RA, Balzer EM and Martin SS. Microtentacles tip the balance of cytoskeletal forces in circulating tumor cells. Cancer research. 2010; 70(20):7737-7741.
28. Whipple RA, Matrone MA, Cho EH, Balzer EM, Vitolo MI, Yoon JR, Ioffe OB, Tuttle KC, Yang J and Martin SS. Epithelial-to-mesenchymal transition promotes tubulin detyrosination and microtentacles that enhance endothelial engagement. Cancer research. 2010; 70(20):8127-8137.
29. Balzer EM, Whipple RA, Thompson K, Boggs AE, Slovic J, Cho EH, Matrone MA, Yoneda T, Mueller SC and Martin SS. c-Src differentially regulates the functions of microtentacles and invadopodia. Oncogene. 2010; 29(48):6402-6408.
30. Matrone MA, Whipple RA, Thompson K, Cho EH, Vitolo MI, Balzer EM, Yoon JR, Ioffe OB, Tuttle KC, Tan M and Martin SS. Metastatic breast tumors express increased tau, which promotes microtentacle formation and the reattachment of detached breast tumor cells. Oncogene. 2010; 29(22):3217-3227.
31. Fan Z, Sun Y, Di C, Tay D, Chen W, Deng CX and Fu J. Acoustic tweezing cytometry for live-cell subcellular modulation of intracellular cytoskeleton contractility. Scientific reports. 2013; 3:2176.
32. Uehata M, Ishizaki T, Satoh H, Ono T, Kawahara T, Morishita T, Tamakawa H, Yamagami K, Inui J, Maekawa M and Narumiya S. Calcium sensitization of smooth muscle mediated by a Rho-associated protein kinase in hypertension. Nature. 1997; 389(6654):990-994.
33. Vicente-Manzanares M, Ma X, Adelstein RS and Horwitz AR. Non-muscle myosin II takes centre stage in cell adhesion and migration. Nature reviews Molecular cell biology. 2009; 10(11):778-790.
34. Schmidt G, Sehr P, Wilm M, Selzer J, Mann M and Aktories K. Gln 63 of Rho is deamidated by Escherichia coli cytotoxic necrotizing factor-1. Nature. 1997; 387(6634):725-729.
35. Ren XD, Kiosses WB and Schwartz MA. Regulation of the small GTP-binding protein Rho by cell adhesion and the cytoskeleton. The EMBO journal. 1999; 18(3):578-585.
36. Balzer EM, Whipple RA, Cho EH, Matrone MA and Martin SS. Antimitotic chemotherapeutics promote adhesive responses in detached and circulating tumor cells. Breast cancer research and treatment. 2010; 121(1):65-78.
37. Vitolo MI, Boggs AE, Whipple RA, Yoon JR, Thompson K, Matrone MA, Cho EH, Balzer EM and Martin SS. Loss of PTEN induces microtentacles through PI3K-independent activation of cofilin. Oncogene. 2013; 32(17):2200-2210.
38. Ingber DE. Tensegrity I. Cell structure and hierarchical systems biology. Journal of cell science. 2003; 116(Pt 7):1157-1173.
39. Palazzo AF, Cook TA, Alberts AS and Gundersen GG. mDia mediates Rho-regulated formation and orientation of stable microtubules. Nature cell biology. 2001; 3(8):723-729.
40. Whipple RA, Vitolo MI, Boggs AE, Charpentier MS, Thompson K and Martin SS. Parthenolide and costunolide reduce microtentacles and tumor cell attachment by selectively targeting detyrosinated tubulin independent from NF-kappaB inhibition. Breast cancer research: BCR. 2013; 15(5):R83.
41. Bravo-Cordero JJ, Hodgson L and Condeelis J. Directed cell invasion and migration during metastasis. Current opinion in cell biology. 2012; 24(2):277-283.
42. Kishi T, Hirooka Y, Masumoto A, Ito K, Kimura Y, Inokuchi K, Tagawa T, Shimokawa H, Takeshita A and Sunagawa K. Rho-kinase inhibitor improves increased vascular resistance and impaired vasodilation of the forearm in patients with heart failure. Circulation. 2005; 111(21):2741-2747.
43. Ishikura K, Yamada N, Ito M, Ota S, Nakamura M, Isaka N and Nakano T. Beneficial acute effects of rho-kinase inhibitor in patients with pulmonary arterial hypertension. Circulation journal: official journal of the Japanese Circulation Society. 2006; 70(2):174-178.
44. Nohria A, Grunert ME, Rikitake Y, Noma K, Prsic A, Ganz P, Liao JK and Creager MA. Rho kinase inhibition improves endothelial function in human subjects with coronary artery disease. Circulation research. 2006; 99(12):1426-1432.
45. Korb T, Schluter K, Enns A, Spiegel HU, Senninger N, Nicolson GL and Haier J. Integrity of actin fibers and microtubules influences metastatic tumor cell adhesion. Experimental cell research. 2004; 299(1):236-247.
46. Birukova AA, Birukov KG, Smurova K, Adyshev D, Kaibuchi K, Alieva I, Garcia JG and Verin AD. Novel role of microtubules in thrombin-induced endothelial barrier dysfunction. FASEB journal: official publication of the Federation of American Societies for Experimental Biology. 2004; 18(15):1879-1890.
47. Bidard FC, Fehm T, Ignatiadis M, Smerage JB, Alix-Panabieres C, Janni W, Messina C, Paoletti C, Muller V, Hayes DF, Piccart M and Pierga JY. Clinical application of circulating tumor cells in breast cancer: overview of the current interventional trials. Cancer metastasis reviews. 2013; 32(1-2):179-188.
48. Naumov GN, Townson JL, MacDonald IC, Wilson SM, Bramwell VH, Groom AC and Chambers AF. Ineffectiveness of doxorubicin treatment on solitary dormant mammary carcinoma cells or late-developing metastases. Breast cancer research and treatment. 2003; 82(3):199-206.
49. Hekimian K, Meisezahl S, Trompelt K, Rabenstein C and Pachmann K. Epithelial cell dissemination and readhesion: analysis of factors contributing to metastasis formation in breast cancer. ISRN oncology. 2012; 2012:601810.
50. Krawczyk N, Meier-Stiegen F, Banys M, Neubauer H, Ruckhaeberle E and Fehm T. Expression of stem cell and epithelial-mesenchymal transition markers in circulating tumor cells of breast cancer patients. BioMed research international. 2014; 2014:415721.
51. Ohgushi M, Matsumura M, Eiraku M, Murakami K, Aramaki T, Nishiyama A, Muguruma K, Nakano T, Suga H, Ueno M, Ishizaki T, Suemori H, Narumiya S, Niwa H and Sasai Y. Molecular pathway and cell state responsible for dissociation-induced apoptosis in human pluripotent stem cells. Cell stem cell. 2010; 7(2):225-239.
52. Watanabe K, Ueno M, Kamiya D, Nishiyama A, Matsumura M, Wataya T, Takahashi JB, Nishikawa S, Nishikawa S, Muguruma K and Sasai Y. A ROCK inhibitor permits survival of dissociated human embryonic stem cells. Nature biotechnology. 2007; 25(6):681-686.
53. Chen G, Hou Z, Gulbranson DR and Thomson JA. Actin-myosin contractility is responsible for the reduced viability of dissociated human embryonic stem cells. Cell stem cell. 2010; 7(2):240-248.
54. Nanba D, Toki F, Matsushita N, Matsushita S, Higashiyama S and Barrandon Y. Actin filament dynamics impacts keratinocyte stem cell maintenance. EMBO molecular medicine. 2013; 5(4):640-653.
55. Ohata H, Ishiguro T, Aihara Y, Sato A, Sakai H, Sekine S, Taniguchi H, Akasu T, Fujita S, Nakagama H and Okamoto K. Induction of the stem-like cell regulator CD44 by Rho kinase inhibition contributes to the maintenance of colon cancer-initiating cells. Cancer research. 2012; 72(19):5101-5110.
56. Liu X, Ory V, Chapman S, Yuan H, Albanese C, Kallakury B, Timofeeva OA, Nealon C, Dakic A, Simic V, Haddad BR, Rhim JS, Dritschilo A, Riegel A, McBride A and Schlegel R. ROCK inhibitor and feeder cells induce the conditional reprogramming of epithelial cells. The American journal of pathology. 2012; 180(2):599-607.
57. Charpentier MS, Whipple RA, Vitolo MI, Boggs AE, Slovic J, Thompson KN, Bhandary L and Martin SS. Curcumin targets breast cancer stem-like cells with microtentacles that persist in mammospheres and promote reattachment. Cancer research. 2014; 74(4):1250-1260.