The RhoGAP activity of myosin IXB is critical for osteoclast podosome patterning, motility, and resorptive capacity

PLoS ONE

Volumn 9, Issue 1, 2014, Pages

  McMichael, Brooke K ^a   Scherer, Katharine F ^a   Franklin, Nicole C ^a   Lee, Beth S ^a  

^a THE OHIO STATE UNIVERSITY COLLEGE OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

INTEGRIN; MYOSIN; MYOSIN IXB; PROTEIN TYROSINE KINASE; RAC PROTEIN; RHO GUANINE NUCLEOTIDE BINDING PROTEIN; SMALL INTERFERING RNA; TUBULIN; TUMOR NECROSIS FACTOR ALPHA; UNCLASSIFIED DRUG;

ACTIN FILAMENT; ANIMAL CELL; ARTICLE; CELL MOTILITY; CELLULAR DISTRIBUTION; CONTROLLED STUDY; MACROPHAGE; MICROTUBULE; MOUSE; NONHUMAN; OSTEOCLAST; PODOSOME;

ACTINS; ANIMALS; BLOTTING, WESTERN; BONE RESORPTION; CELL ADHESION MOLECULES; CELL MOVEMENT; IMMUNOHISTOCHEMISTRY; INDOLES; MICE; MICROSCOPY, CONFOCAL; MULTIPROTEIN COMPLEXES; MYOSINS; OSTEOCLASTS; RNA INTERFERENCE;

EID: 84899839173     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0087402     Document Type: Article

References (61)

1. Hartman MA, Finan D, Sivaramakrishnan S, Spudich JA (2011) Principles of unconventional myosin function and targeting. Annu Rev Cell Dev Biol 27: 133-155.
2. Krendel M, Mooseker MS (2005) Myosins: tails (and heads) of functional diversity. Physiology (Bethesda) 20: 239-251. (Pubitemid 41215198)
3. Woolner S, Bement WM (2009) Unconventional myosins acting unconventionally. Trends Cell Biol 19: 245-252.
4. Odronitz F, Kollmar M (2007) Drawing the tree of eukaryotic life based on the analysis of 2,269 manually annotated myosins from 328 species. Genome Biol 8: R196.
5. Chieregatti E, Gartner A, Stoffler HE, Bahler M (1998) Myr 7 is a novel myosin IX-RhoGAP expressed in rat brain. J Cell Sci 111 (Pt 24): 3597-3608. (Pubitemid 29017558)
6. Wirth JA, Jensen KA, Post PL, Bement WM, Mooseker MS (1996) Human myosin-IXb, an unconventional myosin with a chimerin-like rho/rac GTPase-activating protein domain in its tail. J Cell Sci 109 (Pt 3): 653-661. (Pubitemid 26092686)
7. Bement WM, Hasson T, Wirth JA, Cheney RE, Mooseker MS (1994) Identification and overlapping expression of multiple unconventional myosin genes in vertebrate cell types. Proc Natl Acad Sci U S A 91: 6549-6553. (Pubitemid 24200699)
8. Cooney R, Cummings JR, Pathan S, Beckly J, Geremia A, et al. (2009) Association between genetic variants in myosin IXB and Crohn's disease. Inflamm Bowel Dis 15: 1014-1021.
9. Latiano A, Palmieri O, Valvano MR, D'Inca R, Caprilli R, et al. (2008) The association of MYO9B gene in Italian patients with inflammatory bowel diseases. Aliment Pharmacol Ther 27: 241-248.
10. Monsuur AJ, de Bakker PI, Alizadeh BZ, Zhernakova A, Bevova MR, et al. (2005) Myosin IXB variant increases the risk of celiac disease and points toward a primary intestinal barrier defect. Nat Genet 37: 1341-1344. (Pubitemid 41722189)
11. Nunez C, Oliver J, Mendoza JL, Gomez-Garcia M, Pinero A, et al. (2007) MYO9B polymorphisms in patients with inflammatory bowel disease. Gut 56: 1321-1322. (Pubitemid 47300438)
12. van Bodegraven AA, Curley CR, Hunt KA, Monsuur AJ, Linskens RK, et al. (2006) Genetic variation in myosin IXB is associated with ulcerative colitis. Gastroenterology 131: 1768-1774. (Pubitemid 44958512)
13. Chandhoke SK, Mooseker MS (2012) A role for myosin IXb, a motor-RhoGAP chimera, in epithelial wound healing and tight junction regulation. Mol Biol Cell 23: 2468-2480.
14. Hanley PJ, Xu Y, Kronlage M, Grobe K, Schon P, et al. (2010) Motorized RhoGAP myosin IXb (Myo9b) controls cell shape and motility. Proc Natl Acad Sci U S A 107: 12145-12150.
15. Kambara T, Ikebe M (2006) A unique ATP hydrolysis mechanism of single-headed processive myosin, myosin IX. J Biol Chem 281: 4949-4957. (Pubitemid 43847757)
16. Liao W, Elfrink K, Bahler M (2010) Head of myosin IX binds calmodulin and moves processively toward the plus-end of actin filaments. J Biol Chem 285: 24933-24942.
17. O'Connell CB, Mooseker MS (2003) Native Myosin-IXb is a plus-, not a minus-end-directed motor. Nat Cell Biol 5: 171-172. (Pubitemid 36204201)
18. Bahler M, Elfrink K, Hanley PJ, Thelen S, Xu Y (2011) Cellular functions of class IX myosins in epithelia and immune cells. Biochem Soc Trans 39: 1166-1168.
19. Struchholz S, Elfrink K, Pieper U, Kalhammer G, Honnert U, et al. (2009) Functional role of the extended loop 2 in the myosin 9b head for binding F-actin. J Biol Chem 284: 3663-3671.
20. Reinhard J, Scheel AA, Diekmann D, Hall A, Ruppert C, et al. (1995) A novel type of myosin implicated in signalling by rho family GTPases. Embo J 14: 697-704.
21. Post PL, Bokoch GM, Mooseker MS (1998) Human myosin-IXb is a mechanochemically active motor and a GAP for rho. J Cell Sci 111 (Pt 7): 941-950. (Pubitemid 28196077)
22. Bahler M (2000) Are class III and class IX myosins motorized signalling molecules? Biochim Biophys Acta 1496: 52-59.
23. Anderegg F, Geblinger D, Horvath P, Charnley M, Textor M, et al. (2011) Substrate adhesion regulates sealing zone architecture and dynamics in cultured osteoclasts. PLoS One 6: e28583.
24. Geblinger D, Zink C, Spencer ND, Addadi L, Geiger B (2010) Effects of surface microtopography on the assembly of the osteoclast resorption apparatus. J R Soc Interface 9: 1599-1608.
25. Linder S, Aepfelbacher M (2003) Podosomes: adhesion hot-spots of invasive cells. Trends Cell Biol 13: 376-385. (Pubitemid 36776715)
26. Destaing O, Saltel F, Geminard JC, Jurdic P, Bard F (2003) Podosomes display actin turnover and dynamic self-organization in osteoclasts expressing actingreen fluorescent protein. Mol Biol Cell 14: 407-416. (Pubitemid 36237005)
27. Luxenburg C, Geblinger D, Klein E, Anderson K, Hanein D, et al. (2007) The architecture of the adhesive apparatus of cultured osteoclasts: from podosome formation to sealing zone assembly. PLoS ONE 2: e179.
28. Teitelbaum SL (2000) Bone resorption by osteoclasts. Science 289: 1504-1508.
29. Zhang D, Udagawa N, Nakamura I, Murakami H, Saito S, et al. (1995) The small GTP-binding protein, rho p21, is involved in bone resorption by regulating cytoskeletal organization in osteoclasts. J Cell Sci 108 (Pt 6): 2285-2292.
30. Chellaiah MA, Soga N, Swanson S, McAllister S, Alvarez U, et al. (2000) Rho-A is critical for osteoclast podosome organization, motility, and bone resorption. J Biol Chem 275: 11993-12002. (Pubitemid 30237772)
31. Ory S, Munari-Silem Y, Fort P, Jurdic P (2000) Rho and Rac exert antagonistic functions on spreading of macrophage-derived multinucleated cells and are not required for actin fiber formation. J Cell Sci 113 (Pt 7): 1177-1188. (Pubitemid 30229535)
32. Destaing O, Saltel F, Gilquin B, Chabadel A, Khochbin S, et al. (2005) A novel Rho-mDia2-HDAC6 pathway controls podosome patterning through microtubule acetylation in osteoclasts. J Cell Sci 118: 2901-2911. (Pubitemid 41136367)
33. Ory S, Brazier H, Pawlak G, Blangy A (2008) Rho GTPases in osteoclasts: orchestrators of podosome arrangement. Eur J Cell Biol 87: 469-477.
34. Saltel F, Destaing O, Bard F, Eichert D, Jurdic P (2004) Apatite-mediated actin dynamics in resorbing osteoclasts. Mol Biol Cell 15: 5231-5241. (Pubitemid 39564720)
35. Bianchi ML (2010) Inflammatory bowel diseases, celiac disease, and bone. Arch Biochem Biophys 503: 54-65.
36. Ghishan FK, Kiela PR (2011) Advances in the understanding of mineral and bone metabolism in inflammatory bowel diseases. Am J Physiol Gastrointest Liver Physiol 300: G191-201.
37. Kotadiya P, McMichael BK, Lee BS (2008) High molecular weight tropomyosins regulate osteoclast cytoskeletal morphology. Bone 43: 951-960.
38. McMichael BK, Kotadiya P, Singh T, Holliday LS, Lee BS (2006) Tropomyosin isoforms localize to distinct microfilament populations in osteoclasts. Bone 39: 694-705. (Pubitemid 44311723)
39. McMichael BK, Lee BS (2008) Tropomyosin 4 regulates adhesion structures and resorptive capacity in osteoclasts. Exp Cell Res 314: 564-573.
40. Krits I, Wysolmerski RB, Holliday LS, Lee BS (2002) Differential localization of myosin II isoforms in resting and activated osteoclasts. Calcif Tissue Int 71: 530-538. (Pubitemid 36935470)
41. McMichael BK, Cheney RE, Lee BS (2010) Myosin X regulates sealing zone patterning in osteoclasts through linkage of podosomes and microtubules. J Biol Chem 285: 9506-9515.
42. McMichael BK, Meyer SM, Lee BS (2010) c-Src-mediated phosphorylation of thyroid hormone receptor-interacting protein 6 (TRIP6) promotes osteoclast sealing zone formation. J Biol Chem 285: 26641-26651.
43. McMichael BK, Wysolmerski RB, Lee BS (2009) Regulated proteolysis of nonmuscle myosin IIA stimulates osteoclast fusion. J Biol Chem 284: 12266-12275.
44. Marchisio PC, Cirillo D, Teti A, Zambonin-Zallone A, Tarone G (1987) Rous sarcoma virus-transformed fibroblasts and cells of monocytic origin display a peculiar dot-like organization of cytoskeletal proteins involved in microfilament-membrane interactions. Exp Cell Res 169: 202-214. (Pubitemid 17043787)
45. Tcherkezian J, Lamarche-Vane N (2007) Current knowledge of the large RhoGAP family of proteins. Biol Cell 99: 67-86. (Pubitemid 46242033)
46. Soriano P, Montgomery C, Geske R, Bradley A (1991) Targeted disruption of the c-src proto-oncogene leads to osteopetrosis in mice. Cell 64: 693-702. (Pubitemid 121001157)
47. Boyce BF, Yoneda T, Lowe C, Soriano P, Mundy GR (1992) Requirement of pp60c-src expression for osteoclasts to form ruffled borders and resorb bone in mice. J Clin Invest 90: 1622-1627.
48. Horne WC, Sanjay A, Bruzzaniti A, Baron R (2005) The role(s) of Src kinase and Cbl proteins in the regulation of osteoclast differentiation and function. Immunol Rev 208: 106-125. (Pubitemid 41746388)
49. Sanjay A, Houghton A, Neff L, DiDomenico E, Bardelay C, et al. (2001) Cbl associates with Pyk2 and Src to regulate Src kinase activity, alpha(v)beta(3) integrin-mediated signaling, cell adhesion, and osteoclast motility. J Cell Biol 152: 181-195. (Pubitemid 32102446)
50. Leso V, Leggio L, Armuzzi A, Gasbarrini G, Gasbarrini A, et al. (2010) Role of the tumor necrosis factor antagonists in the treatment of inflammatory bowel disease: an update. Eur J Gastroenterol Hepatol 22: 779-786.
51. Veerappan SG, O'Morain CA, Daly JS, Ryan BM (2011) Review article: the effects of antitumour necrosis factor-alpha on bone metabolism in inflammatory bowel disease. Aliment Pharmacol Ther 33: 1261-1272.
52. Mathew SJ, Haubert D, Kronke M, Leptin M (2009) Looking beyond death: a morphogenetic role for the TNF signalling pathway. J Cell Sci 122: 1939-1946.
53. Fuller K, Murphy C, Kirstein B, Fox SW, Chambers TJ (2002) TNFalpha potently activates osteoclasts, through a direct action independent of and strongly synergistic with RANKL. Endocrinology 143: 1108-1118. (Pubitemid 34164059)
54. Russell RG (2007) Bisphosphonates: mode of action and pharmacology. Pediatrics 119 Suppl 2: S150-162.
55. Brazier H, Stephens S, Ory S, Fort P, Morrison N, et al. (2006) Expression profile of RhoGTPases and RhoGEFs during RANKL-stimulated osteoclastogenesis: identification of essential genes in osteoclasts. J Bone Miner Res 21: 1387-1398. (Pubitemid 44300045)
56. Pertz O (2010) Spatio-temporal Rho GTPase signaling - where are we now? J Cell Sci 123: 1841-1850.
57. O'Neill GM, Stehn J, Gunning PW (2008) Tropomyosins as interpreters of the signalling environment to regulate the local cytoskeleton. Semin Cancer Biol 18: 35-44. (Pubitemid 350266370)
58. Gil-Henn H, Destaing O, Sims NA, Aoki K, Alles N, et al. (2007) Defective microtubule-dependent podosome organization in osteoclasts leads to increased bone density in Pyk2(-/-) mice. J Cell Biol 178: 1053-1064. (Pubitemid 47443326)
59. Young KG, Copeland JW (2010) Formins in cell signaling. Biochim Biophys Acta 1803: 183-190.
60. Yamana N, Arakawa Y, Nishino T, Kurokawa K, Tanji M, et al. (2006) The Rho-mDia1 pathway regulates cell polarity and focal adhesion turnover in migrating cells through mobilizing Apc and c-Src. Mol Cell Biol 26: 6844-6858. (Pubitemid 44387634)
61. Janke C, Bulinski JC (2011) Post-translational regulation of the microtubule cytoskeleton: mechanisms and functions. Nat Rev Mol Cell Biol 12: 773-786.