Plexin-B2 negatively regulates macrophage motility, Rac, and Cdc42 activation

PLoS ONE

Volumn 6, Issue 9, 2011, Pages

  Roney, Kelly E ^a,b   O'Connor, Brian P ^c   Wen, Haitao ^a,b   Holl, Eda K ^a,b   Guthrie, Elizabeth H ^b   Davis, Beckley K ^a   Jones, Stephen W ^b   Jha, Sushmita ^b   Sharek, Lisa ^b   Garcia Mata, Rafael ^b   Bear, James E ^b,c   Ting, Jenny P Y ^a,b  

^a UNIVERSITY OF NORTH CAROLINA SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF NORTH CAROLINA   (United States)

^c DEPARTMENT OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CELL SURFACE RECEPTOR; CHEMOATTRACTANT; GUANOSINE TRIPHOSPHATASE; PLEXIN; PLEXIN B2; PROTEIN CDC42; RAC PROTEIN; RHO FACTOR; RHO GUANINE NUCLEOTIDE BINDING PROTEIN; UNCLASSIFIED DRUG; CD45 ANTIGEN; CYTOKINE; NERVE PROTEIN; PLEXIN B2 PROTEIN, MOUSE; RAC1 PROTEIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; CELL INTERACTION; CELL MIGRATION; CELL MOTILITY; CELLULAR IMMUNITY; CONTROLLED STUDY; CYTOKINE PRODUCTION; CYTOKINE RESPONSE; DENDRITIC CELL; ENZYME LINKED IMMUNOSORBENT ASSAY; IMMUNOREGULATION; IN VITRO STUDY; INNATE IMMUNITY; MACROPHAGE; MOUSE; NERVOUS SYSTEM; NONHUMAN; PHAGOCYTOSIS; PROTEIN BINDING; PROTEIN FUNCTION; WILD TYPE; WOUND HEALING; ANIMAL; BONE MARROW CELL; C57BL MOUSE; CELL CULTURE; CELL MOTION; CELL TRANSPLANTATION; CONGENIC STRAIN; CYTOLOGY; FEMALE; FLOW CYTOMETRY; GENETICS; HUMAN; LIVER; MALE; METABOLISM; METHODOLOGY; MOUSE MUTANT; PRENATAL DEVELOPMENT; SPLEEN; WESTERN BLOTTING;

BACTERIA (MICROORGANISMS);

ANIMALS; ANTIGENS, CD45; BLOTTING, WESTERN; BONE MARROW CELLS; CDC42 GTP-BINDING PROTEIN; CELL MOVEMENT; CELL TRANSPLANTATION; CELLS, CULTURED; CYTOKINES; FEMALE; FLOW CYTOMETRY; HUMANS; LIVER; MACROPHAGES; MALE; MICE; MICE, CONGENIC; MICE, INBRED C57BL; MICE, KNOCKOUT; NERVE TISSUE PROTEINS; PHAGOCYTOSIS; PROTEIN BINDING; RAC1 GTP-BINDING PROTEIN; SPLEEN;

EID: 80053106295     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0024795     Document Type: Article

References (78)

1. Tamagnone L, Artigiani S, Chen H, He Z, Ming GI, et al. (1999) Plexins are a large family of receptors for transmembrane, secreted, and GPI-anchored semaphorins in vertebrates. Cell 99: 71-80.
2. Ohta K, Takagi S, Asou H, Fujisawa H, (1992) Involvement of neuronal cell surface molecule B2 in the formation of retinal plexiform layers. Neuron 9: 151-161.
3. Ohta K, Mizutani A, Kawakami A, Murakami Y, Kasuya Y, et al. (1995) Plexin: a novel neuronal cell surface molecule that mediates cell adhesion via a homophilic binding mechanism in the presence of calcium ions. Neuron 14: 1189-1199.
4. Serini G, Maione F, Giraudo E, Bussolino F, (2009) Semaphorins and tumor angiogenesis. Angiogenesis 12: 187-193.
5. O'Connor BP, Ting JP, (2008) The evolving role of semaphorins and plexins in the immune system: Plexin-A1 regulation of dendritic cell function. Immunol Res 41: 217-222.
6. Kruger RP, Aurandt J, Guan KL, (2005) Semaphorins command cells to move. Nat Rev Mol Cell Biol 6: 789-800.
7. Zielonka M, Xia J, Friedel RH, Offermanns S, Worzfeld T, (2010) A systematic expression analysis implicates Plexin-B2 and its ligand Sema4C in the regulation of the vascular and endocrine system. Exp Cell Res.
8. Stevens L, McClelland L, Fricke A, Williamson M, Kuo I, et al. (2010) Plexin B1 suppresses c-Met in melanoma: a role for plexin B1 as a tumor-suppressor protein through regulation of c-Met. J Invest Dermatol 130: 1636-1645.
9. Okuno T, Nakatsuji Y, Moriya M, Takamatsu H, Nojima S, et al. (2009) Roles of Sema4D-plexin-B1 interactions in the central nervous system for pathogenesis of experimental autoimmune encephalomyelitis. J Immunol 184: 1499-1506.
10. Li M, O'Sullivan KM, Jones LK, Lo C, Semple T, et al. (2009) Endogenous CD100 promotes glomerular injury and macrophage recruitment in experimental crescentic glomerulonephritis. Immunology 128: 114-122.
11. Harduf H, Goldman S, Shalev E, (2007) Human uterine epithelial RL95-2 and HEC-1A cell-line adhesiveness: the role of plexin B1. Fertil Steril 87: 1419-1427.
12. Harduf H, Goldman S, Shalev E, (2009) Progesterone receptor A and c-Met mediates spheroids-endometrium attachment. Reprod Biol Endocrinol 7: 14.
13. Regev A, Goldman S, Shalev E, (2005) Expression of plexin-B1 in the mouse ovary and its possible role in follicular development. Fertil Steril 84 (Suppl 2): 1210-1219.
14. Gomez Roman JJ, Garay GO, Saenz P, Escuredo K, Sanz Ibayondo C, et al. (2008) Plexin B1 is downregulated in renal cell carcinomas and modulates cell growth. Transl Res 151: 134-140.
15. Pan GQ, Ren HZ, Zhang SF, Wang XM, Wen JF, (2009) Expression of semaphorin 5A and its receptor plexin B3 contributes to invasion and metastasis of gastric carcinoma. World J Gastroenterol 15: 2800-2804.
16. Perrot V, Vazquez-Prado J, Gutkind JS, (2002) Plexin B regulates Rho through the guanine nucleotide exchange factors leukemia-associated Rho GEF (LARG) and PDZ-RhoGEF. J Biol Chem 277: 43115-43120.
17. Basile JR, Barac A, Zhu T, Guan KL, Gutkind JS, (2004) Class IV semaphorins promote angiogenesis by stimulating Rho-initiated pathways through plexin-B. Cancer Res 64: 5212-5224.
18. Aurandt J, Vikis HG, Gutkind JS, Ahn N, Guan KL, (2002) The semaphorin receptor plexin-B1 signals through a direct interaction with the Rho-specific nucleotide exchange factor, LARG. Proc Natl Acad Sci U S A 99: 12085-12090.
19. Driessens MH, Olivo C, Nagata K, Inagaki M, Collard JG, (2002) B plexins activate Rho through PDZ-RhoGEF. FEBS Lett 529: 168-172.
20. Hirotani M, Ohoka Y, Yamamoto T, Nirasawa H, Furuyama T, et al. (2002) Interaction of plexin-B1 with PDZ domain-containing Rho guanine nucleotide exchange factors. Biochem Biophys Res Commun 297: 32-37.
21. Swiercz JM, Kuner R, Behrens J, Offermanns S, (2002) Plexin-B1 directly interacts with PDZ-RhoGEF/LARG to regulate RhoA and growth cone morphology. Neuron 35: 51-63.
22. Chabbert-de Ponnat I, Marie-Cardine A, Pasterkamp RJ, Schiavon V, Tamagnone L, et al. (2005) Soluble CD100 functions on human monocytes and immature dendritic cells require plexin C1 and plexin B1, respectively. Int Immunol 17: 439-447.
23. Granziero L, Circosta P, Scielzo C, Frisaldi E, Stella S, et al. (2003) CD100/Plexin-B1 interactions sustain proliferation and survival of normal and leukemic CD5+ B lymphocytes. Blood 101: 1962-1969.
24. Driessens MH, Hu H, Nobes CD, Self A, Jordens I, et al. (2001) Plexin-B semaphorin receptors interact directly with active Rac and regulate the actin cytoskeleton by activating Rho. Curr Biol 11: 339-344.
25. Saito Y, Oinuma I, Fujimoto S, Negishi M, (2009) Plexin-B1 is a GTPase activating protein for M-Ras, remodelling dendrite morphology. EMBO Rep 10: 614-621.
26. Oinuma I, Ishikawa Y, Katoh H, Negishi M, (2004) The Semaphorin 4D receptor Plexin-B1 is a GTPase activating protein for R-Ras. Science 305: 862-865.
27. Mulloy JC, Cancelas JA, Filippi MD, Kalfa TA, Guo F, et al. (2010) Rho GTPases in hematopoiesis and hemopathies. Blood 115: 936-947.
28. Etienne-Manneville S, Hall A, (2002) Rho GTPases in cell biology. Nature 420: 629-635.
29. Hu H, Marton TF, Goodman CS, (2001) Plexin B mediates axon guidance in Drosophila by simultaneously inhibiting active Rac and enhancing RhoA signaling. Neuron 32: 39-51.
30. Vikis HG, Li W, He Z, Guan KL, (2000) The semaphorin receptor plexin-B1 specifically interacts with active Rac in a ligand-dependent manner. Proc Natl Acad Sci U S A 97: 12457-12462.
31. Friedel RH, Kerjan G, Rayburn H, Schuller U, Sotelo C, et al. (2007) Plexin-B2 controls the development of cerebellar granule cells. J Neurosci 27: 3921-3932.
32. Hirschberg A, Deng S, Korostylev A, Paldy E, Costa MR, et al. (2010) Gene deletion mutants reveal a role for semaphorin receptors of the plexin-B family in mechanisms underlying corticogenesis. Mol Cell Biol 30: 764-780.
33. Yu D, Cook MC, Shin DM, Silva DG, Marshall J, et al. (2008) Axon growth and guidance genes identify T-dependent germinal centre B cells. Immunol Cell Biol 86: 3-14.
34. Eun SY, O'Connor BP, Wong AW, van Deventer HW, Taxman DJ, et al. (2006) Cutting edge: rho activation and actin polarization are dependent on plexin-A1 in dendritic cells. J Immunol 177: 4271-4275.
35. Wong AW, Brickey WJ, Taxman DJ, van Deventer HW, Reed W, et al. (2003) CIITA-regulated plexin-A1 affects T-cell-dendritic cell interactions. Nat Immunol 4: 891-898.
36. Takamatsu H, Takegahara N, Nakagawa Y, Tomura M, Taniguchi M, et al. (2010) Semaphorins guide the entry of dendritic cells into the lymphatics by activating myosin II. Nat Immunol 11: 594-600.
37. Wu C, Orozco C, Boyer J, Leglise M, Goodale J, et al. (2009) BioGPS: an extensible and customizable portal for querying and organizing gene annotation resources. Genome Biol 10: R130.
38. Deng S, Hirschberg A, Worzfeld T, Penachioni JY, Korostylev A, et al. (2007) Plexin-B2, but not Plexin-B1, critically modulates neuronal migration and patterning of the developing nervous system in vivo. J Neurosci 27: 6333-6347.
39. Hu B, Guo P, Bar-Joseph I, Imanishi Y, Jarzynka MJ, et al. (2007) Neuropilin-1 promotes human glioma progression through potentiating the activity of the HGF/SF autocrine pathway. Oncogene 26: 5577-5586.
40. O'Connor BP, Eun SY, Ye Z, Zozulya AL, Lich JD, et al. (2008) Semaphorin 6D regulates the late phase of CD4+ T cell primary immune responses. Proc Natl Acad Sci U S A 105: 13015-13020.
41. Deaglio S, Vaisitti T, Bergui L, Bonello L, Horenstein AL, et al. (2004) CD38 and CD100 lead a network of surface receptors relaying positive signals for B-CLL growth and survival. Blood.
42. Kumanogoh A, Shikina T, Watanabe C, Takegahara N, Suzuki K, et al. (2005) Requirement for CD100-CD72 interactions in fine-tuning of B-cell antigen receptor signaling and homeostatic maintenance of the B-cell compartment. Int Immunol 17: 1277-1282.
43. Takamatsu H, Okuno T, Kumanogoh A, (2010) Regulation of immune cell responses by semaphorins and their receptors. Cell Mol Immunol 7: 83-88.
44. Liew FY, Xu D, Brint EK, O'Neill LA, (2005) Negative regulation of toll-like receptor-mediated immune responses. Nat Rev Immunol 5: 446-458.
45. Watarai H, Sekine E, Inoue S, Nakagawa R, Kaisho T, et al. (2008) PDC-TREM, a plasmacytoid dendritic cell-specific receptor, is responsible for augmented production of type I interferon. Proc Natl Acad Sci U S A 105: 2993-2998.
46. Wen H, Lei Y, Eun SY, Ting JP, (2010) Plexin-A4-semaphorin 3A signaling is required for Toll-like receptor- and sepsis-induced cytokine storm. J Exp Med 207: 2943-2957.
47. Campana L, Bosurgi L, Bianchi ME, Manfredi AA, Rovere-Querini P, (2009) Requirement of HMGB1 for stromal cell-derived factor-1/CXCL12-dependent migration of macrophages and dendritic cells. J Leukoc Biol 86: 609-615.
48. Kheir WA, Gevrey JC, Yamaguchi H, Isaac B, Cox D, (2005) A WAVE2-Abi1 complex mediates CSF-1-induced F-actin-rich membrane protrusions and migration in macrophages. J Cell Sci 118: 5369-5379.
49. Vemula S, Ramdas B, Hanneman P, Martin J, Beggs HE, et al. (2010) Essential role for focal adhesion kinase in regulating stress hematopoiesis. Blood 116: 4103-4115.
50. Pankov R, Endo Y, Even-Ram S, Araki M, Clark K, et al. (2005) A Rac switch regulates random versus directionally persistent cell migration. J Cell Biol 170: 793-802.
51. Heasman SJ, Ridley AJ, (2008) Mammalian Rho GTPases: new insights into their functions from in vivo studies. Nat Rev Mol Cell Biol 9: 690-701.
52. Sander EE, van Delft S, ten Klooster JP, Reid T, van der Kammen RA, et al. (1998) Matrix-dependent Tiam1/Rac signaling in epithelial cells promotes either cell-cell adhesion or cell migration and is regulated by phosphatidylinositol 3-kinase. J Cell Biol 143: 1385-1398.
53. Arthur WT, Burridge K, (2001) RhoA inactivation by p190RhoGAP regulates cell spreading and migration by promoting membrane protrusion and polarity. Mol Biol Cell 12: 2711-2720.
54. Aurandt J, Li W, Guan KL, (2006) Semaphorin 4D activates the MAPK pathway downstream of plexin-B1. Biochem J 394: 459-464.
55. Fenteany G, Glogauer M, (2004) Cytoskeletal remodeling in leukocyte function. Curr Opin Hematol 11: 15-24.
56. Park H, Cox D, (2009) Cdc42 regulates Fc gamma receptor-mediated phagocytosis through the activation and phosphorylation of Wiskott-Aldrich syndrome protein (WASP) and neural-WASP. Mol Biol Cell 20: 4500-4508.
57. Cox D, Chang P, Zhang Q, Reddy PG, Bokoch GM, et al. (1997) Requirements for both Rac1 and Cdc42 in membrane ruffling and phagocytosis in leukocytes. J Exp Med 186: 1487-1494.
58. Caron E, Hall A, (1998) Identification of two distinct mechanisms of phagocytosis controlled by different Rho GTPases. Science 282: 1717-1721.
59. Massol P, Montcourrier P, Guillemot JC, Chavrier P, (1998) Fc receptor-mediated phagocytosis requires CDC42 and Rac1. Embo J 17: 6219-6229.
60. Ji JD, Park-Min KH, Ivashkiv LB, (2009) Expression and function of semaphorin 3A and its receptors in human monocyte-derived macrophages. Hum Immunol 70: 211-217.
61. Liang CC, Park AY, Guan JL, (2007) In vitro scratch assay: a convenient and inexpensive method for analysis of cell migration in vitro. Nat Protoc 2: 329-333.
62. Masuda K, Furuyama T, Takahara M, Fujioka S, Kurinami H, et al. (2004) Sema4D stimulates axonal outgrowth of embryonic DRG sensory neurones. Genes Cells 9: 821-829.
63. Yukawa K, Tanaka T, Yoshida K, Takeuchi N, Ito T, et al. (2010) Sema4A induces cell morphological changes through B-type plexin-mediated signaling. Int J Mol Med 25: 225-230.
64. Hota PK, Buck M, (2009) Thermodynamic characterization of two homologous protein complexes: associations of the semaphorin receptor plexin-B1 RhoGTPase binding domain with Rnd1 and active Rac1. Protein Sci 18: 1060-1071.
65. Bouguet-Bonnet S, Buck M, (2008) Compensatory and long-range changes in picosecond-nanosecond main-chain dynamics upon complex formation: 15 N relaxation analysis of the free and bound states of the ubiquitin-like domain of human plexin-B1 and the small GTPase Rac1. J Mol Biol 377: 1474-1487.
66. Li X, Lee AY, (2010) Semaphorin 5A and plexin-B3 inhibit human glioma cell motility through RhoGDIalpha-mediated inactivation of Rac1 GTPase. J Biol Chem 285: 32436-32445.
67. Wong OG, Nitkunan T, Oinuma I, Zhou C, Blanc V, et al. (2007) Plexin-B1 mutations in prostate cancer. Proc Natl Acad Sci U S A 104: 19040-19045.
68. Gruenheid S, DeVinney R, Bladt F, Goosney D, Gelkop S, et al. (2001) Enteropathogenic E. coli Tir binds Nck to initiate actin pedestal formation in host cells. Nat Cell Biol 3: 856-859.
69. Holmes S, Downs AM, Fosberry A, Hayes PD, Michalovich D, et al. (2002) Sema7A is a potent monocyte stimulator. Scand J Immunol 56: 270-275.
70. Perala N, Jakobson M, Ola R, Fazzari P, Penachioni JY, et al. (2011) Sema4C-Plexin B2 signalling modulates ureteric branching in developing kidney. Differentiation 81: 81-91.
71. Maier V, Jolicoeur C, Rayburn H, Takegahara N, Kumanogoh A, et al. (2011) Semaphorin 4C and 4G are ligands of Plexin-B2 required in cerebellar development. Mol Cell Neurosci 46: 419-431.
72. Hartwig C, Veske A, Krejcova S, Rosenberger G, Finckh U, (2005) Plexin B3 promotes neurite outgrowth, interacts homophilically, and interacts with Rin. BMC Neurosci 6: 53.
73. Neufeld G, Lange T, Varshavsky A, Kessler O, (2007) Semaphorin signaling in vascular and tumor biology. Adv Exp Med Biol 600: 118-131.
74. Waimey KE, Cheng HJ, (2006) Axon pruning and synaptic development: how are they per-plexin? Neuroscientist 12: 398-409.
75. Godin I, Cumano A, (2002) The hare and the tortoise: an embryonic haematopoietic race. Nat Rev Immunol 2: 593-604.
76. Abramoff MD, Magelhaes PJ, Ram SJ, (2004) Image Processing with ImageJ. Biophotonics International 11: 36-42.
77. Noren NK, Arthur WT, Burridge K, (2003) Cadherin engagement inhibits RhoA via p190RhoGAP. J Biol Chem 278: 13615-13618.
78. Scott RS, McMahon EJ, Pop SM, Reap EA, Caricchio R, et al. (2001) Phagocytosis and clearance of apoptotic cells is mediated by MER. Nature 411: 207-211.