Myo9b is a key player in SLIT/ROBO-mediated lung tumor suppression

Journal of Clinical Investigation

Volumn 125, Issue 12, 2015, Pages 4407-4420

  Kong, Ruirui ^a   Yi, Fengshuang ^a,b   Wen, Pushuai ^a   Liu, Jianghong ^a   Chen, Xiaoping ^c   Ren, Jinqi ^a   Li, Xiaofei ^d   Shang, Yulong ^e   Nie, Yongzhan ^e   Wu, Kaichun ^e   Fan, Daiming ^e   Zhu, Li ^a   Feng, Wei ^a   Wu, Jane Y ^a,c  

^a INSTITUTE OF BIOPHYSICS   (China)

^b UNIVERSITY OF CHINESE ACADEMY OF SCIENCES   (China)

^c NORTHWESTERN UNIVERSITY   (United States)

^d FOURTH MILITARY MEDICAL UNIVERSITY   (China)

^e FOURTH MILITARY MEDICAL UNIVERSITY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

MESSENGER RNA; MYOSIN; MYOSIN 9B; PROTEIN CDC42; RHOA GUANINE NUCLEOTIDE BINDING PROTEIN; ROUNDABOUT RECEPTOR; SLIT PROTEIN; SLIT2 PROTEIN; UNCLASSIFIED DRUG; GLYCOPROTEIN; IMMUNOGLOBULIN RECEPTOR; MYOSIN IXB; NERVE PROTEIN; RHOA PROTEIN, HUMAN; SLIT PROTEIN, VERTEBRATE; TUMOR SUPPRESSOR PROTEIN;

A549 CELL LINE; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BINDING SITE; CANCER GROWTH; CANCER INHIBITION; CANCER PROGNOSIS; CARCINOGENESIS; CELL LYSATE; CELL MIGRATION; CELL PROLIFERATION; CONTROLLED STUDY; ENZYME ACTIVATION; ENZYME INACTIVATION; HUMAN; HUMAN CELL; HUMAN TISSUE; INTRACELLULAR SPACE; LUNG CANCER; LUNG CANCER CELL LINE; LUNG METASTASIS; LYMPH NODE METASTASIS; MOUSE; NERVE CELL; NONHUMAN; NUCLEOTIDE SEQUENCE; OVERALL SURVIVAL; PRIORITY JOURNAL; PROGRESSION FREE SURVIVAL; PROTEIN DOMAIN; PROTEIN PROTEIN INTERACTION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION; TUMOR INVASION; ANIMAL; BAGG ALBINO MOUSE; FEMALE; GENETICS; LUNG TUMOR; METABOLISM; NUDE MOUSE; PATHOLOGY; TUMOR CELL LINE;

ANIMALS; CELL LINE, TUMOR; FEMALE; GLYCOPROTEINS; HUMANS; LUNG NEOPLASMS; MICE; MICE, INBRED BALB C; MICE, NUDE; MYOSINS; NERVE TISSUE PROTEINS; RECEPTORS, IMMUNOLOGIC; RHOA GTP-BINDING PROTEIN; SIGNAL TRANSDUCTION; TUMOR SUPPRESSOR PROTEINS;

EID: 84948808434     PISSN: 00219738     EISSN: 15588238     Source Type: Journal    
DOI: 10.1172/JCI81673     Document Type: Article

References (68)

1. Cooper WA, Lam DC, O'Toole SA, Minna JD. Molecular biology of lung cancer. J Thorac Dis. 2013;5(suppl 5):S479-S490.
2. Peifer M, et al. Integrative genome analyses identify key somatic driver mutations of small-cell lung cancer. Nat Genet. 2012;44(10):1104-1110.
3. Valastyan S, Weinberg RA. Tumor metastasis: molecular insights and evolving paradigms. Cell. 2011;147(2):275-292.
4. Park KS, et al. A crucial requirement for Hedgehog signaling in small cell lung cancer. Nat Med. 2011;17(11):1504-1508.
5. Brose K, et al. Slit proteins bind Robo receptors and have an evolutionarily conserved role in repulsive axon guidance. Cell. 1999;96(6):795-806.
6. Li HS, et al. Vertebrate slit, a secreted ligand for the transmembrane protein roundabout, is a repellent for olfactory bulb axons. Cell. 1999;96(6):807-818.
7. Wu W, et al. Directional guidance of neuronal migration in the olfactory system by the protein Slit. Nature. 1999;400(6742):331-336.
8. Ypsilanti AR, Zagar Y, Chedotal A. Moving away from the midline: new developments for Slit and Robo. Development. 2010;137(12):1939-1952.
9. Brantley-Sieders DM, et al. Angiocrine factors modulate tumor proliferation and motility through EphA2 repression of Slit2 tumor suppressor function in endothelium. Cancer Res. 2011;71(3):976-987.
10. Geutskens SB, Hordijk PL, van Hennik PB. The chemorepellent Slit3 promotes monocyte migration. J Immunol. 2010;185(12):7691-7698.
11. Legg JA, Herbert JM, Clissold P, Bicknell R. Slits and Roundabouts in cancer, tumour angiogene-sis and endothelial cell migration. Angiogenesis. 2008;11(1):13-21.
12. Prasad A, Qamri Z, Wu J, Ganju RK. Slit-2/Robo-1 modulates the CXCL12/CXCR4-induced chemo-taxis of T cells. J Leukoc Biol. 2007;82(3):465-476.
13. Wu JY, et al. The neuronal repellent Slit inhibits leukocyte chemotaxis induced by chemotactic factors. Nature. 2001;410(6831):948-952.
14. Ballard MS, Hinck L. A roundabout way to cancer. Adv Cancer Res. 2012;114:187-235.
15. Mehlen P, Delloye-Bourgeois C, Chedotal A. Novel roles for Slits and netrins: axon guidance cues as anticancer targets? Nat Rev Cancer. 2011;11(3):188-197.
16. Nasarre P, Potiron V, Drabkin H, Roche J. Guidance molecules in lung cancer. Cell Adh Migr. 2010;4(1):130-145.
17. Dammann R, et al. CpG island methylation and expression of tumour-associated genes in lung carcinoma. Eur J Cancer. 2005;41(8):1223-1236.
18. Dallol A, et al. SLIT2, a human homologue of the Drosophila Slit2 gene, has tumor suppressor activity is frequently inactivated in lung breast cancers. Cancer Res. 2002;62(20):5874-5880.
19. Kim HK, et al. Slit2 inhibits growth metastasis of fibrosarcoma squamous cell carcinoma. Neopla-sia. 2008;10(12):1411-1420.
20. Tseng RC, et al. SLIT2 attenuation during lung cancer progression deregulates β-catenin E-cad-herin associates with poor prognosis. Cancer Res. 2010;70(2):543-551.
21. Yu J, et al. The neuronal repellent SLIT2 is a target for repression by EZH2 in prostate cancer. Oncogene. 2010;29(39):5370-5380.
22. Liao W, Elfrink K, Bahler M. Head of myosin IX binds calmodulin and moves processively toward the plus-end of actin filaments. J Biol Chem. 2010;285(32):24933-24942.
23. van den Boom F, Dussmann H, Uhlenbrock K, Abouhamed M, Bahler M. The Myosin IXb motor activity targets the myosin IXb RhoGAP domain as cargo to sites of actin polymerization. Mol Biol Cell. 2007;18(4):1507-1518.
24. Abouhamed M, et al. Myosin IXa regulates epithelial differentiation and its deficiency results in hydro-cephalus. Mol Biol Cell. 2009;20(24):5074-5085.
25. Hanley PJ, et al. Motorized RhoGAP myosin IXb (Myo9b) controls cell shape motility. Proc Natl Acad Sci USA. 2010;107(27):12145-12150.
26. Xu Y, et al. Dendritic cell motility and T cell activation requires regulation of Rho-cofilin signaling by the Rho-GTPase activating protein myosin IXb. J Immunol. 2014;192(8):3559-3568.
27. Post PL, Bokoch GM, Mooseker MS. Human myo-sin-IXb is a mechanochemically active motor and a GAP for rho. J Cell Sci. 1998;111(pt 7):941-950.
28. Saeki N, Tokuo H, Ikebe M. BIG1 is a binding partner of myosin IXb and regulates its Rho-GT-Pase activating protein activity. J Biol Chem. 2005;280(11):10128-10134.
29. Wirth JA, Jensen KA, Post PL, Bement WM, Mooseker MS. Human myosin-IXb, an unconventional myosin with a chimerin-like rho/rac GTPase-activating protein domain in its tail. J Cell Sci. 1996;109(pt 3):653-661.
30. Heasman SJ, Ridley AJ. Mammalian Rho GTPases: new insights into their functions from in vivo studies. Nat Rev Mol Cell Biol. 2008;9(9):690-701.
31. Parsons JT, Horwitz AR, Schwartz MA. Cell adhesion: integrating cytoskeletal dynamics and cellular tension. Nat Rev Mol Cell Biol. 2010;11(9):633-643.
32. Yuasa-Kawada J, Kinoshita-Kawada M, Rao Y, Wu JY. Deubiquitinating enzyme USP33/VDU1 is required for Slit signaling in inhibiting breast cancer cell migration. Proc Natl Acad Sci USA. 2009;106(34):14530-14535.
33. Wong K, et al. Signal transduction in neuronal migration: roles of GTPase activating proteins and the small GTPase Cdc42 in the Slit-Robo pathway. Cell. 2001;107(2):209-221.
34. Jaffe AB, Hall A. Rho GTPases: biochemistry and biology. Annu Rev Cell Dev Biol. 2005;21:247-269.
35. Yuasa-Kawada J, Kinoshita-Kawada M, Wu G, Rao Y, Wu JY. Midline crossing and Slit responsiveness of commissural axons require USP33. Nat Neurosci. 2009;12(9):1087-1089.
36. Rhodes DR, et al. ONCOMINE: a cancer microarray database and integrated data-mining platform. Neoplasia. 2004;6(1):1-6.
37. Gyorffy B, Surowiak P, Budczies J, Lanczky A. Online survival analysis software to assess the prognostic value of biomarkers using transcrip-tomic data in non-small-cell lung cancer. PLoS One. 2013;8(12):e82241.
38. Gao J, et al. Integrative analysis of complex cancer genomics and clinical profiles using the cBioPortal. Sci Signal. 2013;6(269):pl1.
39. Spiro SG, Silvestri GA. One hundred years of lung cancer. Am J Respir Crit Care Med. 2005;172(5):523-529.
40. Sanchez-Cespedes M. The role of LKB1 in lung cancer. Fam Cancer. 2011;10(3):447-453.
41. Vaahtomeri K, Makela TP. Molecular mechanisms of tumor suppression by LKB1. FEBS Lett. 2011;585(7):944-951.
42. Yiin JJ, et al. Slit2 inhibits glioma cell invasion in the brain by suppression of Cdc42 activity. Neuro Oncol. 2009;11(6):779-789.
43. Werbowetski-Ogilvie TE, et al. Inhibition of medulloblastoma cell invasion by Slit. Oncogene. 2006;25(37):5103-5112.
44. Greenberg JM, Thompson FY, Brooks SK, Shannon JM, Akeson AL. Slit and robo expression in the developing mouse lung. Dev Dyn. 2004;230(2):350-360.
45. Muller RT, Honnert U, Reinhard J, Bahler M. The rat myosin myr 5 is a GTPase-activating protein for Rho in vivo: essential role of arginine 1695. Mol Biol Cell. 1997;8(10):2039-2053.
46. Jelen F, Lachowicz P, Apostoluk W, Mateja A, Derewenda ZS, Otlewski J. Dissecting the thermodynamics of GAP-RhoA interactions. J Struct Biol. 2009;165(1):10-18.
47. Ridley AJ. Life at the leading edge. Cell. 2011;145(7):1012-1022.
48. Besson A, Gurian-West M, Schmidt A, Hall A, Roberts JM. p27Kip1 modulates cell migration through the regulation of RhoA activation. Genes Dev. 2004;18(8):862-876.
49. Kurokawa K, Matsuda M. Localized RhoA activation as a requirement for the induction of membrane ruffling. Mol Biol Cell. 2005;16(9):4294-4303.
50. Wu X, Liu T, Fang O, Leach LJ, Hu X, Luo Z. miR-194 suppresses metastasis of non-small cell lung cancer through regulating expression of BMP1 p27(kip1). Oncogene. 2014;33(12):1506-1514.
51. Liu Y, et al. Ablation of p120-catenin enhances invasion and metastasis of human lung cancer cells. Cancer Sci. 2009;100(3):441-448.
52. Cools J. RHOA mutations in peripheral T cell lymphoma. Nat Genet. 2014;46(4):320-321.
53. Kakiuchi M, et al. Recurrent gain-of-function mutations of RHOA in diffuse-type gastric carcinoma. Nat Genet. 2014;46(6):583-587.
54. Palomero T, et al. Recurrent mutations in epigenetic regulators, RHOA and FYN kinase in peripheral T cell lymphomas. Nat Genet. 2014;46(2):166-170.
55. Sakata-Yanagimoto M, et al. Somatic RHOA mutation in angioimmunoblastic T cell lym-phoma. Nat Genet. 2014;46(2):171-175.
56. Wang K, et al. Whole-genome sequencing and comprehensive molecular profiling identify new driver mutations in gastric cancer. Nat Genet. 2014;46(6):573-582.
57. Yoo HY, et al. A recurrent inactivating mutation in RHOA GTPase in angioimmunoblastic T cell lymphoma. Nat Genet. 2014;46(4):371-375.
58. Zhou J, Hayakawa Y, Wang TC, Bass AJ. RhoA mutations identified in diffuse gastric cancer. Cancer Cell. 2014;26(1):9-11.
59. Battye TG, Kontogiannis L, Johnson O, Powell HR, Leslie AG. iMOSFLM: a new graphical interface for diffraction-image processing with MOSFLM. Acta Crystallogr D Biol Crystallogr. 2011;67(pt 4):271-281.
60. Dodson EJ, Winn M, Ralph A. Collaborative Computational Project, number 4: providing programs for protein crystallography. Me thods Enzymol. 1997;277:620-633.
61. McCoy AJ. Solving structures of protein complexes by molecular replacement with Phaser. Acta Crystallogr D Biol Crystallogr. 2007;63(pt 1):32-41.
62. Emsley P, Cowtan K. Coot: model-building tools for molecular graphics. Acta Crystallogr D Biol Crystallogr. 2004;60(pt 12 pt 1):2126-2132.
63. Adams PD, et al. PHENIX: a comprehensive Python-based system for macromolecular structure solution. Acta Crystallogr D Biol Crystallogr. 2010;66(pt 2):213-221.
64. Laskowski RA, Macarthur MW, Moss DS, Thornton JM. Procheck-A program to check the ste-reochemical quality of protein structures. J Appl Cryst. 1993;26(2):283-291.
65. Phillips JC, et al. Scalable molecular dynamics with NAMD. J Comput Chem. 2005;26(16):1781-1802.
66. MacKerell AD, et al. All-atom empirical potential for molecular modeling and dynamics studies of proteins. J Phys Chem B. 1998;102(18):3586-3616.
67. Humphrey W, Dalke A, Schulten K. VMD: visual molecular dynamics. J Mol Graph. 1996;14(1):33-38.
68. Tong X, et al. Decreased TIP30 expression promotes tumor metastasis in lung cancer. Am J Pathol. 2009;174(5):1931-1939.