Myosin 1e promotes breast cancer malignancy by enhancing tumor cell proliferation and stimulating tumor cell de-differentiation

Oncotarget

Volumn 7, Issue 29, 2016, Pages 46419-46432

  Ouderkirk Pecone, Jessica L ^a   Goreczny, Gregory J ^a   Chase, Sharon E ^a   Tatum, Arthur H ^a   Turner, Christopher E ^a   Krendel, Mira ^a  

^a State University of New York Upstate Medical University: College of Medicine   (United States)

Author keywords

Animal models of cancer; Breast cancer; Myosin; Therapeutic targets; Tumor promotion and progression

Indexed keywords

CYCLIN D1; KI 67 ANTIGEN; MYOSIN; MYOSIN 1E; UNCLASSIFIED DRUG; MYO1E PROTEIN, MOUSE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BREAST CANCER; CANCER CELL; CANCER SURVIVAL; CANCER TISSUE; CELL DEDIFFERENTIATION; CELL ISOLATION; CELL PROLIFERATION; CONTROLLED STUDY; EPITHELIUM CELL; HISTOLOGY; IMMUNOHISTOCHEMISTRY; LUNG METASTASIS; MAMMARY GLAND; MOUSE; NONHUMAN; TUMOR VOLUME; ANIMAL; BREAST TUMOR; C57BL MOUSE; FEMALE; HUMAN; KAPLAN MEIER METHOD; KNOCKOUT MOUSE; METABOLISM; MORTALITY; PATHOLOGY; PHYSIOLOGY; PROGNOSIS;

ANIMALS; BREAST NEOPLASMS; CELL DEDIFFERENTIATION; CELL PROLIFERATION; FEMALE; HUMANS; KAPLAN-MEIER ESTIMATE; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MYOSINS; PROGNOSIS;

EID: 84979920428     PISSN: None     EISSN: 19492553     Source Type: Journal    
DOI: 10.18632/oncotarget.10139     Document Type: Article

References (51)

1. ACS. (2015). Cancer Facts & Figures 2015. (Atlanta: American Cancer Society).
2. Wagner KU, McAllister K, Ward T, Davis B, Wiseman R, Hennighausen L. Spatial and temporal expression of the Cre gene under the control of the MMTV-LTR in different lines of transgenic mice. Transgenic research. 2001; 10:545-553.
3. Guy CT, Cardiff RD, Muller WJ. Induction of mammary tumors by expression of polyomavirus middle T oncogene: a transgenic mouse model for metastatic disease. Molecular and cellular biology. 1992; 12:954-961.
4. Smith BA, Shelton DN, Kieffer C, Milash B, Usary J, Perou CM, Bernard PS, Welm BE. Targeting the PyMT Oncogene to Diverse Mammary Cell Populations Enhances Tumor Heterogeneity and Generates Rare Breast Cancer Subtypes. Genes & cancer. 2012; 3:550-563.
5. Courtneidge SA, Smith AE. Polyoma virus transforming protein associates with the product of the c-src cellular gene. Nature. 1983; 303:435-439.
6. Courtneidge SA, Heber A. An 81 kd protein complexed with middle T antigen and pp60c-src: a possible phosphatidylinositol kinase. Cell. 1987; 50:1031-1037.
7. Cheng SH, Harvey R, Espino PC, Semba K, Yamamoto T, Toyoshima K, Smith AE. Peptide antibodies to the human c-fyn gene product demonstrate pp59c-fyn is capable of complex formation with the middle-T antigen of polyomavirus. The EMBO journal. 1988; 7:3845-3855.
8. Fluck MM, Schaffhausen BS. Lessons in signaling and tumorigenesis from polyomavirus middle T antigen. Microbiology and molecular biology reviews: MMBR. 2009; 73:542-563, Table of Contents.
9. Dankort DL, Muller WJ. Signal transduction in mammary tumorigenesis: a transgenic perspective. Oncogene. 2000; 19:1038-1044.
10. Lin EY, Jones JG, Li P, Zhu L, Whitney KD, Muller WJ, Pollard JW. Progression to malignancy in the polyoma middle T oncoprotein mouse breast cancer model provides a reliable model for human diseases. Am J Pathol. 2003; 163:2113-2126.
11. Mallon E, Osin P, Nasiri N, Blain I, Howard B, Gusterson B. The basic pathology of human breast cancer. Journal of mammary gland biology and neoplasia. 2000; 5:139-163.
12. Ouderkirk JL, Krendel M. Non-muscle myosins in tumor progression, cancer cell invasion, and metastasis. Cytoskeleton (Hoboken, NJ). 2014; 71:447-463.
13. Mazzolini R, Dopeso H, Mateo-Lozano S, Chang W, Rodrigues P, Bazzocco S, Alazzouzi H, Landolfi S, Hernandez-Losa J, Andretta E, Alhopuro P, Espin E, Armengol M, et al. Brush border myosin Ia has tumor suppressor activity in the intestine. Proc Natl Acad Sci U S A. 109:1530-1535.
14. Schramek D, Sendoel A, Segal JP, Beronja S, Heller E, Oristian D, Reva B, Fuchs E. Direct in vivo RNAi screen unveils myosin IIa as a tumor suppressor of squamous cell carcinomas. Science. 2014; 343:309-313.
15. Dunn TA, Chen S, Faith DA, Hicks JL, Platz EA, Chen Y, Ewing CM, Sauvageot J, Isaacs WB, De Marzo AM, Luo J. A novel role of myosin VI in human prostate cancer. Am J Pathol. 2006; 169:1843-1854.
16. Cao R, Chen J, Zhang X, Zhai Y, Qing X, Xing W, Zhang L, Malik YS, Yu H, Zhu X. Elevated expression of myosin X in tumours contributes to breast cancer aggressiveness and metastasis. British journal of cancer. 2014; 111:539-550.
17. Hallett RM, Dvorkin-Gheva A, Bane A, Hassell JA. A gene signature for predicting outcome in patients with basal-like breast cancer. Scientific reports. 2012; 2:227.
18. Krendel M, Kim SV, Willinger T, Wang T, Kashgarian M, Flavell RA, Mooseker MS. Disruption of Myosin 1e promotes podocyte injury. J Am Soc Nephrol. 2009; 20:86-94.
19. Kim SV, Mehal WZ, Dong X, Heinrich V, Pypaert M, Mellman I, Dembo M, Mooseker MS, Wu D, Flavell RA. Modulation of cell adhesion and motility in the immune system by Myo1f. Science. 2006; 314:136-139.
20. Petryszak R, Burdett T, Fiorelli B, Fonseca NA, Gonzalez-Porta M, Hastings E, Huber W, Jupp S, Keays M, Kryvych N, McMurry J, Marioni JC, Malone J, et al. Expression Atlas update-a database of gene and transcript expression from microarray-and sequencing-based functional genomics experiments. Nucleic acids research. 2014; 42:D926-932.
21. Tiede B, Kang Y. From milk to malignancy: the role of mammary stem cells in development, pregnancy and breast cancer. Cell research. 2011; 21:245-257.
22. Taylor-Papadimitriou J, Stampfer M, Bartek J, Lewis A, Boshell M, Lane EB, Leigh IM. Keratin expression in human mammary epithelial cells cultured from normal and malignant tissue: relation to in vivo phenotypes and influence of medium. Journal of cell science. 1989; 94:403-413.
23. Plante I, Stewart MK, Laird DW. Evaluation of mammary gland development and function in mouse models. Journal of visualized experiments: JoVE. 2011.
24. Dairkee SH, Puett L, Hackett AJ. Expression of basal and luminal epithelium-specific keratins in normal, benign, and malignant breast tissue. Journal of the National Cancer Institute. 1988; 80:691-695.
25. Wetzels RH, Holland R, van Haelst UJ, Lane EB, Leigh IM, Ramaekers FC. Detection of basement membrane components and basal cell keratin 14 in noninvasive and invasive carcinomas of the breast. The American journal of pathology. 1989; 134:571-579.
26. Zhang Q, Sakamoto K, Wagner KU. D-type Cyclins are important downstream effectors of cytokine signaling that regulate the proliferation of normal and neoplastic mammary epithelial cells. Mol Cell Endocrinol. 2014; 382:583-592.
27. Schonk DM, Kuijpers HJ, van Drunen E, van Dalen CH, Geurts van Kessel AH, Verheijen R, Ramaekers FC. Assignment of the gene(s) involved in the expression of the proliferation-related Ki-67 antigen to human chromosome
28. Bi J, Chase SE, Pellenz CD, Kurihara H, Fanning AS, Krendel M. Myosin 1e is a component of the glomerular slit diaphragm complex that regulates actin reorganization during cell-cell contact formation in podocytes. Am J Physiol Renal Physiol. 2013; 305:F532-544.
29. Gumbiner BM, Kim NG. The Hippo-YAP signaling pathway and contact inhibition of growth. Journal of cell science. 2014; 127:709-717.
30. Kavanagh E, Buchert M, Tsapara A, Choquet A, Balda MS, Hollande F, Matter K. Functional interaction between the ZO-1-interacting transcription factor ZONAB/DbpA and the RNA processing factor symplekin. Journal of cell science. 2006; 119:5098-5105.
31. Sourisseau T, Georgiadis A, Tsapara A, Ali RR, Pestell R, Matter K, Balda MS. Regulation of PCNA and cyclin D1 expression and epithelial morphogenesis by the ZO-1-regulated transcription factor ZONAB/DbpA. Molecular and cellular biology. 2006; 26:2387-2398.
32. Zhao B, Wei X, Li W, Udan RS, Yang Q, Kim J, Xie J, Ikenoue T, Yu J, Li L, Zheng P, Ye K, Chinnaiyan A, Halder G, Lai ZC, Guan KL. Inactivation of YAP oncoprotein by the Hippo pathway is involved in cell contact inhibition and tissue growth control. Genes & development. 2007; 21:2747-2761.
33. Lima WR, Parreira KS, Devuyst O, Caplanusi A, N'Kuli F, Marien B, Van Der Smissen P, Alves PM, Verroust P, Christensen EI, Terzi F, Matter K, Balda MS, Pierreux CE, Courtoy PJ. ZONAB promotes proliferation and represses differentiation of proximal tubule epithelial cells. Journal of the American Society of Nephrology: JASN. 2010; 21:478-488.
34. Mihaly Z, Kormos M, Lanczky A, Dank M, Budczies J, Szasz MA, Gyorffy B. A meta-analysis of gene expressionbased biomarkers predicting outcome after tamoxifen treatment in breast cancer. Breast cancer research and treatment. 2013; 140:219-232.
35. Arjonen A, Kaukonen R, Mattila E, Rouhi P, Hognas G, Sihto H, Miller BW, Morton JP, Bucher E, Taimen P, Virtakoivu R, Cao Y, Sansom OJ, Joensuu H, Ivaska J. Mutant p53-associated myosin-X upregulation promotes breast cancer invasion and metastasis. The Journal of clinical investigation. 2014; 124:1069-1082.
36. Pal SK, Lau SK, Kruper L, Nwoye U, Garberoglio C, Gupta RK, Paz B, Vora L, Guzman E, Artinyan A, Somlo G. Papillary carcinoma of the breast: an overview. Breast Cancer Res Treat. 2010; 122:637-645.
37. Ueng SH, Mezzetti T, Tavassoli FA. Papillary neoplasms of the breast: a review. Arch Pathol Lab Med. 2009; 133:893-907.
38. Maroulakou IG, Oemler W, Naber SP, Tsichlis PN. Akt1 ablation inhibits, whereas Akt2 ablation accelerates, the development of mammary adenocarcinomas in mouse mammary tumor virus (MMTV)-ErbB2/neu and MMTVpolyoma middle T transgenic mice. Cancer research. 2007; 67:167-177.
39. Cardiff RD, Wellings SR. The comparative pathology of human and mouse mammary glands. J Mammary Gland Biol Neoplasia. 1999; 4:105-122.
40. Arun G, Diermeier S, Akerman M, Chang KC, Wilkinson JE, Hearn S, Kim Y, MacLeod AR, Krainer AR, Norton L, Brogi E, Egeblad M, Spector DL. Differentiation of mammary tumors and reduction in metastasis upon Malat1 lncRNA loss. Genes Dev. 2016; 30:34-51.
41. Davie SA, Maglione JE, Manner CK, Young D, Cardiff RD, MacLeod CL, Ellies LG. Effects of FVB/NJ and C57Bl/6J strain backgrounds on mammary tumor phenotype in inducible nitric oxide synthase deficient mice. Transgenic research. 2007; 16:193-201.
42. Skowron JF, Bement WM, Mooseker MS. Human brush border myosin-I and myosin-Ic expression in human intestine and Caco-2BBe cells. Cell Motil Cytoskeleton. 1998; 41:308-324.
43. Baselga J. Targeting the phosphoinositide-3 (PI3) kinase pathway in breast cancer. Oncologist. 2011; 16:12-19.
44. Ouderkirk JL, Krendel M. Myosin 1e is a component of the invadosome core that contributes to regulation of invadosome dynamics. Exp Cell Res. 2014; 322:265-276.
45. Krendel M, Osterweil EK, Mooseker MS. Myosin 1E interacts with synaptojanin-1 and dynamin and is involved in endocytosis. FEBS Lett. 2007; 581:644-650.
46. Swanson JA, Johnson MT, Beningo K, Post P, Mooseker M, Araki N. A contractile activity that closes phagosomes in macrophages. J Cell Sci. 1999; 112:307-316.
47. Chase SE, Encina CV, Stolzenburg LR, Tatum AH, Holzman LB, Krendel M. Podocyte-specific knockout of myosin 1e disrupts glomerular filtration. Am J Physiol Renal Physiol. 2012; 303:F1099-1106.
48. Euhus DM, Hudd C, LaRegina MC, Johnson FE. Tumor measurement in the nude mouse. J Surg Oncol. 1986; 31:229-234.
49. Bi J, Pellenz CD, Krendel M. Visualization of cytoskeletal dynamics in podocytes using adenoviral vectors. Cytoskeleton (Hoboken, NJ). 2014; 71:145-156.
50. DeNardo DG, Barreto JB, Andreu P, Vasquez L, Tawfik D, Kolhatkar N, Coussens LM. CD4(+) T cells regulate pulmonary metastasis of mammary carcinomas by enhancing protumor properties of macrophages. Cancer cell. 2009; 16:91-102.
51. Györffy B, Lanczky A, Eklund AC, Denkert C, Budczies J, Li Q, Szallasi Z. An online survival analysis tool to rapidly assess the effect of 22,277 genes on breast cancer prognosis using microarray data of 1,809 patients. Breast Cancer Res Treat. 2010; 123:725-731.