LKB1 Controls Human Bronchial Epithelial Morphogenesis through p114RhoGEF-Dependent RhoA Activation

REFERENCES

• Hearle N, Schumacher V, Menko FH, Olschwang S, Boardman LA, Gille JJ, Keller JJ, Westerman AM, Scott RJ, Lim W, Trimbath JD, Giardiello FM, Gruber SB, Offerhaus GJ, de Rooij FW, Wilson JH, Hansmann A, Moslein G, Royer-Pokora B, Vogel T, Phillips RK, Spigelman AD, Houlston RS. 2006. Frequency and spectrum of cancers in the Peutz-Jeghers syndrome. Clin. Cancer Res. 12:3209–3215.
   PubMed Web of Science ®Google Scholar
• Wingo SN, Gallardo TD, Akbay EA, Liang MC, Contreras CM, Boren T, Shimamura T, Miller DS, Sharpless NE, Bardeesy N, Kwiatkowski DJ, Schorge JO, Wong KK, Castrillon DH. 2009. Somatic LKB1 mutations promote cervical cancer progression. PLoS One 4:e5137. doi:10.1371/journal.pone.0005137.
   PubMed Web of Science ®Google Scholar
• Makowski L, Hayes DN. 2008. Role of LKB1 in lung cancer development. Br. J. Cancer 99:683–688.
   PubMed Web of Science ®Google Scholar
• Tiainen M, Ylikorkala A, Makela TP. 1999. Growth suppression by Lkb1 is mediated by a G(1) cell cycle arrest. Proc. Natl. Acad. Sci. U. S. A. 96:9248–9251.
   PubMed Web of Science ®Google Scholar
• Xu XJ, Omelchenko T, Hall A. 2010. LKB1 tumor suppressor protein regulates actin filament assembly through Rho and its exchange factor Dbl independently of kinase activity. BMC Cell Biol. 11:77. doi:10.1186/1471-2121-11-77.
   PubMedGoogle Scholar
• Sanchez-Cespedes M. 2011. The role of LKB1 in lung cancer. Fam. Cancer 10:447–453.
   PubMedGoogle Scholar
• Shah U, Sharpless NE, Hayes DN. 2008. LKB1 and lung cancer: more than the usual suspects. Cancer Res. 68:3562–3565.
   PubMedGoogle Scholar
• Sanchez-Cespedes M. 2007. A role for LKB1 gene in human cancer beyond the Peutz-Jeghers syndrome. Oncogene 26:7825–7832.
   PubMed Web of Science ®Google Scholar
• Sapkota GP, Kieloch A, Lizcano JM, Lain S, Arthur JS, Williams MR, Morrice N, Deak M, Alessi DR. 2001. Phosphorylation of the protein kinase mutated in Peutz-Jeghers cancer syndrome, LKB1/STK11, at Ser431 by p90(RSK) and cAMP-dependent protein kinase, but not its farnesylation at Cys(433), is essential for LKB1 to suppress cell growth. J. Biol. Chem. 276:19469–19482.
   PubMed Web of Science ®Google Scholar
• Baas AF, Boudeau J, Sapkota GP, Smit L, Medema R, Morrice NA, Alessi DR, Clevers HC. 2003. Activation of the tumour suppressor kinase LKB1 by the STE20-like pseudokinase STRAD. EMBO J. 22:3062–3072.
   PubMed Web of Science ®Google Scholar
• Boudeau J, Baas AF, Deak M, Morrice NA, Kieloch A, Schutkowski M, Prescott AR, Clevers HC, Alessi DR. 2003. MO25 alpha/beta interact with STRAD alpha/beta enhancing their ability to bind, activate and localize LKB1 in the cytoplasm. EMBO J. 22:5102–5114.
   PubMed Web of Science ®Google Scholar
• Shaw RJ. 2009. LKB1 and AMP-activated protein kinase control of mTOR signalling and growth. Acta Physiol. (Oxf.) 196:65–80.
   PubMed Web of Science ®Google Scholar
• Alessi DR, Sakamoto K, Bayascas JR. 2006. LKB1-dependent signaling pathways. Annu. Rev. Biochem. 75:137–163.
   PubMed Web of Science ®Google Scholar
• Watts JL, Morton DG, Bestman J, Kemphues KJ. 2000. The C. elegans par-4 gene encodes a putative serine-threonine kinase required for establishing embryonic asymmetry. Development 127:1467–1475.
   PubMed Web of Science ®Google Scholar
• Chartier NT, Ospina DPS, Benkemoun L, Mayer M, Grill SW, Maddox AS, Labbe JC. 2011. PAR-4/LKB1 mobilizes nonmuscle myosin through anillin to regulate C. elegans embryonic polarization and cytokinesis. Curr. Biol. 21:259–269.
   PubMed Web of Science ®Google Scholar
• Martin SG, St Johnston D. 2003. A role for Drosophila LKB1 in anterior-posterior axis formation and epithelial polarity. Nature 421:379–384.
   PubMed Web of Science ®Google Scholar
• Partanen JI, Tervonen TA, Myllynen M, Lind E, Imai M, Katajisto P, Dijkgraaf GJP, Kovanen PE, Makela TP, Werb Z, Klefstrom J. 2012. Tumor suppressor function of liver kinase B1 (Lkb1) is linked to regulation of epithelial integrity. Proc. Natl. Acad. Sci. U. S. A. 109:E388–E397.
   PubMedGoogle Scholar
• Hezel AF, Gurumurthy S, Granot Z, Swisa A, Chu GC, Bailey G, Dor Y, Bardeesy N, DePinho RA. 2008. Pancreatic Lkb1 deletion leads to acinar polarity defects and cystic neoplasms. Mol. Cell. Biol. 28:2414–2425.
   PubMed Web of Science ®Google Scholar
• Baas AF, Kuipers J, van der Wel NN, Batlle E, Koerten HK, Peters PJ, Clevers HC. 2004. Complete polarization of single intestinal epithelial cells upon activation of LKB1 by STRAD. Cell 116:457–466.
   PubMed Web of Science ®Google Scholar
• Ten Klooster JP, Jansen M, Yuan J, Oorschot V, Begthel H, Di Giacomo V, Colland F, de Koning J, Maurice MM, Hornbeck P, Clevers H. 2009. Mst4 and Ezrin induce brush borders downstream of the Lkb1/Strad/Mo25 polarization complex. Dev. Cell 16:551–562.
   PubMed Web of Science ®Google Scholar
• Gloerich M, Ten Klooster JP, Vliem MJ, Koorman T, Zwartkruis FJ, Clevers H, Bos JL. 2012. Rap2A links intestinal cell polarity to brush border formation. Nat. Cell Biol. 14:793–801.
   PubMedGoogle Scholar
• Roy BC, Kohno T, Iwakawa R, Moriguchi T, Kiyono T, Morishita K, Sanchez-Cespedes M, Akiyama T, Yokota J. 2010. Involvement of LKB1 in epithelial-mesenchymal transition (EMT) of human lung cancer cells. Lung Cancer 70:136–145.
   PubMedGoogle Scholar
• Upadhyay S, Liu CY, Chatterjee A, Hoque MO, Kim MS, Engles J, Westra W, Trink B, Ratovitski E, Sidransky D. 2006. LKB1/STK11 suppresses cyclooxygenase-2 induction and cellular invasion through PEA3 in lung cancer. Cancer Res. 66:7870–7879.
   PubMed Web of Science ®Google Scholar
• Gao Y, Xiao Q, Ma H, Li L, Liu J, Feng Y, Fang Z, Wu J, Han X, Zhang J, Sun Y, Wu G, Padera R, Chen H, Wong KK, Ge G, Ji H. 2010. LKB1 inhibits lung cancer progression through lysyl oxidase and extracellular matrix remodeling. Proc. Natl. Acad. Sci. U. S. A. 107:18892–18897.
   PubMedGoogle Scholar
• Carretero J, Shimamura T, Rikova K, Jackson AL, Wilkerson MD, Borgman CL, Buttarazzi MS, Sanofsky BA, McNamara KL, Brandstetter KA, Walton ZE, Gu TL, Silva JC, Crosby K, Shapiro GI, Maira SM, Ji H, Castrillon DH, Kim CF, Garcia-Echeverria C, Bardeesy N, Sharpless NE, Hayes ND, Kim WY, Engelman JA, Wong KK. 2010. Integrative genomic and proteomic analyses identify targets for Lkb1-deficient metastatic lung tumors. Cancer Cell 17:547–559.
   PubMed Web of Science ®Google Scholar
• Ji H, Ramsey MR, Hayes DN, Fan C, McNamara K, Kozlowski P, Torrice C, Wu MC, Shimamura T, Perera SA, Liang MC, Cai D, Naumov GN, Bao L, Contreras CM, Li D, Chen L, Krishnamurthy J, Koivunen J, Chirieac LR, Padera RF, Bronson RT, Lindeman NI, Christiani DC, Lin X, Shapiro GI, Janne PA, Johnson BE, Meyerson M, Kwiatkowski DJ, Castrillon DH, Bardeesy N, Sharpless NE, Wong KK. 2007. LKB1 modulates lung cancer differentiation and metastasis. Nature 448:807–810.
   PubMed Web of Science ®Google Scholar
• Hemminki A, Markie D, Tomlinson I, Avizienyte E, Roth S, Loukola A, Bignell G, Warren W, Aminoff M, Hoglund P, Jarvinen H, Kristo P, Pelin K, Ridanpaa M, Salovaara R, Toro T, Bodmer W, Olschwang S, Olsen AS, Stratton MR, de la Chapelle A, Aaltonen LA. 1998. A serine/threonine kinase gene defective in Peutz-Jeghers syndrome. Nature 391:184–187.
   PubMed Web of Science ®Google Scholar
• Nezu J, Oku A, Shimane M. 1999. Loss of cytoplasmic retention ability of mutant LKB1 found in Peutz-Jeghers syndrome patients. Biochem. Biophys. Res. Commun. 261:750–755.
   PubMedGoogle Scholar
• Karuman P, Gozani O, Odze RD, Zhou XC, Zhu H, Shaw R, Brien TP, Bozzuto CD, Ooi D, Cantley LC, Yuan JY. 2001. The Peutz-Jegher gene product LKB1 is a mediator of p53-dependent cell death. Mol. Cell 7:1307–1319.
   PubMed Web of Science ®Google Scholar
• Kim DW, Chung HK, Park KC, Hwang JH, Jo YS, Chung J, Kalvakolanu DV, Resta N, Shong M. 2007. Tumor suppressor LKB1 inhibits activation of signal transducer and activator of transcription 3 (STAT3) by thyroid oncogenic tyrosine kinase rearranged in transformation (RET)/papillary thyroid carcinoma (PTC). Mol. Endocrinol. 21:3039–3049.
   PubMedGoogle Scholar
• Wallace SW, Magalhaes A, Hall A. 2011. The Rho target PRK2 regulates apical junction formation in human bronchial epithelial cells. Mol. Cell. Biol. 31:81–91.
   PubMedGoogle Scholar
• Wallace SW, Durgan J, Jin D, Hall A. 2010. Cdc42 regulates apical junction formation in human bronchial epithelial cells through PAK4 and Par6B. Mol. Biol. Cell 21:2996–3006.
   PubMedGoogle Scholar
• Terry SJ, Zihni C, Elbediwy A, Vitiello E, San LCIV, Balda MS, Matter K. 2011. Spatially restricted activation of RhoA signalling at epithelial junctions by p114RhoGEF drives junction formation and morphogenesis. Nat. Cell Biol. 13:159–166.
   PubMed Web of Science ®Google Scholar
• Nakajima H, Tanoue T. 2011. Lulu2 regulates the circumferential actomyosin tensile system in epithelial cells through p114RhoGEF. J. Cell Biol. 195:245–261.
   PubMedGoogle Scholar
• Sebbagh M, Santoni MJ, Hall B, Borg JP, Schwartz MA. 2009. Regulation of LKB1/STRAD localization and function by E-cadherin. Curr. Biol. 19:37–42.
   PubMed Web of Science ®Google Scholar
• Rauch J, Volinsky N, Romano D, Kolch W. 2011. The secret life of kinases: functions beyond catalysis. Cell Commun. Signal. 9:23. doi:10.1186/1478-811X-9-23.
   PubMed Web of Science ®Google Scholar
• Speroni J, Federico MB, Mansilla SF, Soria G, Gottifredi V. 2012. Kinase-independent function of checkpoint kinase 1 (Chk1) in the replication of damaged DNA. Proc. Natl. Acad. Sci. U. S. A. 109:7344–7349.
   PubMed Web of Science ®Google Scholar
• Lo B, Strasser G, Sagolla M, Austin CD, Junttila M, Mellman I. 2012. Lkb1 regulates organogenesis and early oncogenesis along AMPK-dependent and -independent pathways. J. Cell Biol. 199:1117–1130.
   PubMedGoogle Scholar
• Forcet C, Etienne-Manneville S, Gaude H, Fournier L, Debilly S, Salmi M, Baas A, Olschwang S, Clevers H, Billaud M. 2005. Functional analysis of Peutz-Jeghers mutations reveals that the LKB1 C-terminal region exerts a crucial role in regulating both the AMPK pathway and the cell polarity. Hum. Mol. Genet. 14:1283–1292.
   PubMedGoogle Scholar
• Zhang L, Li J, Young LH, Caplan MJ. 2006. AMP-activated protein kinase regulates the assembly of epithelial tight junctions. Proc. Natl. Acad. Sci. U. S. A. 103:17272–17277.
   PubMed Web of Science ®Google Scholar
• Zheng B, Cantley LC. 2007. Regulation of epithelial tight junction assembly and disassembly by AMP-activated protein kinase. Proc. Natl. Acad. Sci. U. S. A. 104:819–822.
   PubMed Web of Science ®Google Scholar
• Amin N, Khan A, St Johnston D, Tomlinson I, Martin S, Brenman J, McNeill H. 2009. LKB1 regulates polarity remodeling and adherens junction formation in the Drosophila eye. Proc. Natl. Acad. Sci. U. S. A. 106:8941–8946.
   PubMed Web of Science ®Google Scholar
• Niu J, Profirovic J, Pan H, Vaiskunaite R, Voyno-Yasenetskaya T. 2003. G Protein betagamma subunits stimulate p114RhoGEF, a guanine nucleotide exchange factor for RhoA and Rac1: regulation of cell shape and reactive oxygen species production. Circ. Res. 93:848–856.
   PubMed Web of Science ®Google Scholar