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Pericyte-like spreading by disseminated cancer cells activates YAP and MRTF for metastatic colonization

Er, Ekrem Emrah, Valiente, Manuel, Ganesh, Karuna, Zou, Yilong, Agrawal, Saloni, Hu, Jing, Griscom, Bailey, Rosenblum, Marc +6 more·2018·Nature Cell Biology
DOI 10.1038/s41556-018-0138-8PMC PMC6467203
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  1. [1]Massague J & Obenauf AC Metastatic colonization by circulating tumour cells. Nature 529, 298– 306 (2016). 26791720 PMC5029466
  2. [2]Sosa MS, Bragado P & Aguirre-Ghiso JA Mechanisms of disseminated cancer cell dormancy: an awakening field. Nat. Rev. Cancer 14, 611– 622 (2014). 25118602 PMC4230700
  3. [3]Lambert AW, Pattabiraman DR & Weinberg RA Emerging Biological Principles of Metastasis. Cell 168, 670– 691 (2017). 28187288 PMC5308465
  4. [4]Obenauf AC & Massague J Surviving at a distance: organ specific metastasis. Trends in cancer 1, 76– 91 (2015). PMC4673677 28741564
  5. [5]Kienast Y Real-time imaging reveals the single steps of brain metastasis formation. Nat. Med 16, 116– 122 (2010). 20023634
  6. [6]Entenberg D In vivo subcellular resolution optical imaging in the lung reveals early metastatic proliferation and motility. Intravital 4 (2015). PMC4737962 26855844
  7. [7]Ritsma L Intravital microscopy through an abdominal imaging window reveals a pre-micrometastasis stage during liver metastasis. Science translational medicine 4, 158ra145 (2012). 23115354
  8. [9]Rafii S, Butler JM & Ding BS Angiocrine functions of organ-specific endothelial cells. Nature 529, 316– 325 (2016). 26791722 PMC4878406
  9. [12]Zhao C Distinct contributions of angiogenesis and vascular co-option during the initiation of primary microtumors and micrometastases. Carcinogenesis 32, 1143– 1150 (2011). 21515914
  10. [13]Donnem T Vessel co-option in primary human tumors and metastases: an obstacle to effective anti-angiogenic treatment? Cancer medicine 2, 427– 436 (2013). 24156015 PMC3799277
  11. [14]Valiente M Serpins promote cancer cell survival and vascular co-option in brain metastasis. Cell 156, 1002– 1016 (2014). 24581498 PMC3988473
  12. [15]Altevogt P, Doberstein K & Fogel M L1CAM in human cancer. Int. J. Cancer 138, 1565– 1576 (2016). 26111503
  13. [16]Ebeling O L1 adhesion molecule on human lymphocytes and monocytes: expression and involvement in binding to alpha v beta 3 integrin. Eur. J. Immunol 26, 2508– 2516 (1996). 8898967
  14. [17]Itoh K & Fushiki S The role of L1cam in murine corticogenesis, and the pathogenesis of hydrocephalus. Pathology international 65, 58– 66 (2015). 25641508
  15. [18]Kiefel H L1CAM: a major driver for tumor cell invasion and motility. Cell adhesion & migration 6, 374– 384 (2012). 22796939 PMC3478260
  16. [19]Nguyen DX WNT/TCF signaling through LEF1 and HOXB9 mediates lung adenocarcinoma metastasis. Cell 138, 51– 62 (2009). 19576624 PMC2742946
  17. [20]Bos PD Genes that mediate breast cancer metastasis to the brain. Nature 459, 1005– 1009 (2009). 19421193 PMC2698953
  18. [21]Armulik A, Genove G & Betsholtz C Pericytes: developmental, physiological, and pathological perspectives, problems, and promises. Dev. Cell 21, 193– 215 (2011). 21839917
  19. [22]Minn AJ Genes that mediate breast cancer metastasis to lung. Nature 436, 518– 524 (2005). 16049480 PMC1283098
  20. [23]Shibue T & Weinberg RA Integrin beta1-focal adhesion kinase signaling directs the proliferation of metastatic cancer cells disseminated in the lungs. Proceedings of the National Academy of Sciences of the United States of America 106, 10290– 10295 (2009). 19502425 PMC2700942
  21. [24]Shibue T, Brooks MW & Weinberg RA An integrin-linked machinery of cytoskeletal regulation that enables experimental tumor initiation and metastatic colonization. Cancer Cell 24, 481– 498 (2013). 24035453 PMC3864118
  22. [26]Winslow MM Suppression of lung adenocarcinoma progression by Nkx2–1. Nature 473, 101– 104 (2011). 21471965 PMC3088778
  23. [28]Zhao B, Li L, Lei Q & Guan KL The Hippo-YAP pathway in organ size control and tumorigenesis: an updated version. Genes Dev. 24, 862– 874 (2010). 20439427 PMC2861185
  24. [29]Olson EN & Nordheim A Linking actin dynamics and gene transcription to drive cellular motile functions. Nat. Rev. Mol. Cell Biol. 11, 353– 365 (2010). 20414257 PMC3073350
  25. [30]Lamar JM The Hippo pathway target, YAP, promotes metastasis through its TEAD-interaction domain. Proceedings of the National Academy of Sciences of the United States of America 109, E2441– 2450 (2012). 22891335 PMC3443162
  26. [31]Medjkane S, Perez-Sanchez C, Gaggioli C, Sahai E & Treisman R Myocardin-related transcription factors and SRF are required for cytoskeletal dynamics and experimental metastasis. Nat. Cell Biol 11, 257– 268 (2009). 19198601 PMC6089348
  27. [32]Iwamoto M, Bjorklund T, Lundberg C, Kirik D & Wandless TJ A general chemical method to regulate protein stability in the mammalian central nervous system. Chem. Biol 17, 981– 988 (2010). 20851347 PMC2943492
  28. [34]Aragona M A mechanical checkpoint controls multicellular growth through YAP/TAZ regulation by actin-processing factors. Cell 154, 1047– 1059 (2013). 23954413
  29. [35]Elosegui-Artola A Force Triggers YAP Nuclear Entry by Regulating Transport across Nuclear Pores. Cell 171, 1397– 1410 e1314 (2017). 29107331
  30. [36]Zhao B Angiomotin is a novel Hippo pathway component that inhibits YAP oncoprotein. Genes Dev. 25, 51– 63 (2011). 21205866 PMC3012936
  31. [37]Yagi R, Chen LF, Shigesada K, Murakami Y & Ito Y A WW domain-containing yes-associated protein (YAP) is a novel transcriptional co-activator. EMBO J. 18, 2551– 2562 (1999). 10228168 PMC1171336
  32. [38]Zhao B TEAD mediates YAP-dependent gene induction and growth control. Genes Dev. 22, 1962– 1971 (2008). 18579750 PMC2492741
  33. [39]Euer NI Identification of L1CAM, Jagged2 and Neuromedin U as ovarian cancer-associated antigens. Oncol. Rep 13, 375– 387 (2005). 15706405
  34. [40]Dahme M Disruption of the mouse L1 gene leads to malformations of the nervous system. Nat. Genet. 17, 346– 349 (1997). 9354804
  35. [41]McCuskey RS, Urbaschek R & Urbaschek B The microcirculation during endotoxemia. Cardiovascular research 32, 752– 763 (1996). 8915193
  36. [42]Ziegler T Angiopoietin 2 mediates microvascular and hemodynamic alterations in sepsis. J. Clin. Invest (2013). PMC3726157 23863629
  37. [43]Law JW Decreased anxiety, altered place learning, and increased CA1 basal excitatory synaptic transmission in mice with conditional ablation of the neural cell adhesion molecule L1. J. Neurosci 23, 10419– 10432 (2003). 14614101 PMC6741026
  38. [45]Passaniti A A simple, quantitative method for assessing angiogenesis and antiangiogenic agents using reconstituted basement membrane, heparin, and fibroblast growth factor. Lab. Invest 67, 519– 528 (1992). 1279270
  39. [46]Cuvelier D The universal dynamics of cell spreading. Curr. Biol 17, 694– 699 (2007). 17379524
  40. [47]Kogata N, Tribe RM, Fassler R, Way M & Adams RH Integrin-linked kinase controls vascular wall formation by negatively regulating Rho/ROCK-mediated vascular smooth muscle cell contraction. Genes Dev. 23, 2278– 2283 (2009). 19797768 PMC2758749
  41. [48]Abraham S, Kogata N, Fassler R & Adams RH Integrin beta1 subunit controls mural cell adhesion, spreading, and blood vessel wall stability. Circ Res 102, 562– 570 (2008). 18202311
  42. [49]Serrano I, McDonald PC, Lock F, Muller WJ & Dedhar S Inactivation of the Hippo tumour suppressor pathway by integrin-linked kinase. Nature communications 4, 2976 (2013). PMC3905719 24356468
  43. [50]Kadmon G, Montgomery AM & Altevogt P L1 makes immunological progress by expanding its relations. Dev. Immunol 6, 205– 213 (1998). 9814594 PMC2276031
  44. [51]Thelen K The neural cell adhesion molecule L1 potentiates integrin-dependent cell migration to extracellular matrix proteins. J. Neurosci 22, 4918– 4931 (2002). 12077189 PMC6757736
  45. [52]Byron A Anti-integrin monoclonal antibodies. J. Cell Sci 122, 4009– 4011 (2009). 19910492 PMC3329622
  46. [53]Widmaier M, Rognoni E, Radovanac K, Azimifar SB & Fassler R Integrin-linked kinase at a glance. J. Cell Sci 125, 1839– 1843 (2012). 22637643
  47. [54]Ferreira M, Fujiwara H, Morita K & Watt FM An activating beta1 integrin mutation increases the conversion of benign to malignant skin tumors. Cancer Res. 69, 1334– 1342 (2009). 19190332 PMC2644725
  48. [55]Pezzella F Non-small-cell lung carcinoma tumor growth without morphological evidence of neo-angiogenesis. The American journal of pathology 151, 1417– 1423 (1997). 9358768 PMC1858069
  49. [56]Holash J Vessel cooption, regression, and growth in tumors mediated by angiopoietins and VEGF. Science 284, 1994– 1998 (1999). 10373119
  50. [57]Barnhill RL & Lugassy C Angiotropic malignant melanoma and extravascular migratory metastasis: description of 36 cases with emphasis on a new mechanism of tumour spread. Pathology 36, 485– 490 (2004). 15370120
  51. [58]Evidence for novel non-angiogenic pathway in breast-cancer metastasis. Breast Cancer Progression Working Party. Lancet 355, 1787– 1788 (2000). 10832831
  52. [59]Sardari Nia P, Hendriks J, Friedel G, Van Schil P & Van Marck E Distinct angiogenic and non-angiogenic growth patterns of lung metastases from renal cell carcinoma. Histopathology 51, 354– 361 (2007). 17727477
  53. [60]Stessels F Breast adenocarcinoma liver metastases, in contrast to colorectal cancer liver metastases, display a non-angiogenic growth pattern that preserves the stroma and lacks hypoxia. Br. J. Cancer 90, 1429– 1436 (2004). 15054467 PMC2409675
  54. [61]Cheng L Glioblastoma stem cells generate vascular pericytes to support vessel function and tumor growth. Cell 153, 139– 152 (2013). 23540695 PMC3638263
  55. [62]Fransen E L1 knockout mice show dilated ventricles, vermis hypoplasia and impaired exploration patterns. Hum. Mol. Genet 7, 999– 1009 (1998). 9580664
  56. [63]Lebrin F Thalidomide stimulates vessel maturation and reduces epistaxis in individuals with hereditary hemorrhagic telangiectasia. Nat. Med. 16, 420– 428 (2010). 20364125
  57. [64]Hellstrom M, Kalen M, Lindahl P, Abramsson A & Betsholtz C Role of PDGF-B and PDGFR-beta in recruitment of vascular smooth muscle cells and pericytes during embryonic blood vessel formation in the mouse. Development 126, 3047– 3055 (1999). 10375497
  58. [65]Plouffe SW, Hong AW & Guan KL Disease implications of the Hippo/YAP pathway. Trends Mol. Med. 21, 212– 222 (2015). 25702974 PMC4385444
  59. [66]Moroishi T The Hippo Pathway Kinases LATS1/2 Suppress Cancer Immunity. Cell 167, 1525– 1539 e1517 (2016). 27912060 PMC5512418
  60. [67]Kang Y A multigenic program mediating breast cancer metastasis to bone. Cancer Cell 3, 537– 549 (2003). 12842083
  61. [69]Kasai M In vivo effect of anti-asialo GM1 antibody on natural killer activity. Nature 291, 334– 335 (1981). 7231554
  62. [70]van de Wiel-van Kemenade E Adhesion of T and B lymphocytes to extracellular matrix and endothelial cells can be regulated through the beta subunit of VLA. J. Cell Biol 117, 461– 470 (1992). 1560035 PMC2289428
  63. [71]Lawley TJ & Kubota Y Induction of morphologic differentiation of endothelial cells in culture. The Journal of investigative dermatology 93, 59S– 61S (1989). 2754280
  64. [72]Polleux F & Ghosh A The slice overlay assay: a versatile tool to study the influence of extracellular signals on neuronal development. Science’s STKE: signal transduction knowledge environment 2002, pl9 (2002). 12060788
  65. [75]Zhang XH Selection of bone metastasis seeds by mesenchymal signals in the primary tumor stroma. Cell 154, 1060– 1073 (2013). 23993096 PMC3974915
  66. [77]Hopewell EL Lung tumor NF-kappaB signaling promotes T cell-mediated immune surveillance. J. Clin. Invest 123, 2509– 2522 (2013). 23635779 PMC3668836
  67. [80]Fellmann C An optimized microRNA backbone for effective single-copy RNAi. Cell reports 5, 1704– 1713 (2013). 24332856

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Authors
Er, E. E., Valiente, M., Ganesh, K., Zou, Y., Agrawal, S., Hu, J., Griscom, B., Rosenblum, M., Boire, A., Brogi, E., Giancotti, F. G., Schachner, M., Malladi, S., & Massagué, J.
ORCID
Venue
Nature Cell Biology
Publisher
Springer Science and Business Media LLC
Published
2018-07-23
Volume
20
Issue
8
Pages
966-978
ISSN
  • 1465-7392
  • 1476-4679
DOI
10.1038/s41556-018-0138-8
PMC
PMC6467203
Cited by
291
References
13
Language
en
Update notices
correction (2018-12-12)
Licence
www.springer.com/tdm (tdm)

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