Abstract
The fusion of one cell with another occurs in development, injury and disease. Despite the diversity of fusion events, five steps in sequence appear common. These steps include programming fusion-competent status, chemotaxis, membrane adhesion, membrane fusion, and post-fusion resetting. Recent advances in the field start to reveal the molecules involved in each step. This review focuses on some key molecules and cellular events of cell fusion in mammals. Increasing evidence demonstrates that membrane lipid rafts, adhesion proteins and actin rearrangement are critical in the final step of membrane fusion. Here we propose a new model for the formation and expansion of membrane fusion pores based on recent observations on myotube formation. In this model, membrane lipid rafts first recruit adhesion molecules and align with opposing membranes, with the help of a cortical actin “wall” as a rigid supportive platform. Second, the membrane adhesion proteins interact with each other and trigger actin rearrangement, which leads to rapid dispersion of lipid rafts and flow of a highly fluidic phospholipid bilayer into the site. Finally, the opposing phospholipid bilayers are then pushed into direct contact leading to the formation of fusion pores by the force generated through actin polymerization. The actin polymerization generated force also drives the expansion of the fusion pores. However, several key questions about the process of cell fusion still remain to be explored. The understanding of the mechanisms of cell fusion may provide new opportunities in correcting development disorders or regenerating damaged tissues by inhibiting or promoting molecular events associated with fusion.
Access this chapter
Tax calculation will be finalised at checkout
Purchases are for personal use only
References
Schwann T (1839) Mikroskopische Untersuchungen uber die Uebereunstimmung in der Struktur und dem Wachsten der Thiere und Pflanzen. Sander’schen Buchhanlung, Berlin
Ogle BM, Cascalho M, Platt JL (2005) Biological implications of cell fusion. Nat Rev Mol Cell Biol 6:567–575
Vjugina U, Evans JP (2008) New insights into the molecular basis of mammalian sperm-egg membrane interactions. Front Biosci 13:462–476
Huppertz B, Bartz C, Kokozidou M (2006) Trophoblast fusion: fusogenic proteins, syncytins and ADAMs, and other prerequisites for syncytial fusion. Micron 37:509–517
Rochlin K, Yu S, Roy S et al (2010) Myoblast fusion: when it takes more to make one. Dev Biol 341:66–83
Helming L, Gordon S (2007) The molecular basis of macrophage fusion. Immunobiology 212:785–793
Alvarez-Dolado M (2007) Cell fusion: biological perspectives and potential for regenerative medicine. Front Biosci 12:1–12
Lluis F, Cosma MP (2010) Cell-fusion-mediated somatic-cell reprogramming: a mechanism for tissue regeneration. J Cell Physiol 223:6–13
Helming L, Gordon S (2009) Molecular mediators of macrophage fusion. Trends Cell Biol 19:514–522
DeFife KM, Jenney CR, McNally AK et al (1997) Interleukin-13 induces human monocyte/macrophage fusion and macrophage mannose receptor expression. J Immunol 158:3385–3390
Enelow RI, Sullivan GW, Carper HT et al (1992) Induction of multinucleated giant cell formation from in vitro culture of human monocytes with interleukin-3 and interferon-gamma: comparison with other stimulating factors. Am J Respir Cell Mol Biol 6:57–62
McNally AK, Anderson JM (1995) Interleukin-4 induces foreign body giant cells from human monocytes/macrophages. Differential lymphokine regulation of macrophage fusion leads to morphological variants of multinucleated giant cells. Am J Pathol 147:1487–1499
Coury F, Annels N, Rivollier A et al (2008) Langerhans cell histiocytosis reveals a new IL-17A-dependent pathway of dendritic cell fusion. Nat Med 14:81–87
McInnes A, Rennick DM (1988) Interleukin 4 induces cultured monocytes/macrophages to form giant multinucleated cells. J Exp Med 167:598–611
Horsley V, Jansen KM, Mills ST et al (2003) IL-4 acts as a myoblast recruitment factor during mammalian muscle growth. Cell 113:483–494
Weinberg JB, Hobbs MM, Misukonis MA (1984) Recombinant human gamma-interferon induces human monocyte polykaryon formation. Proc Natl Acad Sci USA 81:4554–4557
Belosevic M, Finbloom DS, Van Der Meide PH et al (1989) Administration of monoclonal anti-IFN-gamma antibodies in vivo abrogates natural resistance of C3H/HeN mice to infection with Leishmania major. J Immunol 143:266–274
Chensue SW, Terebuh PD, Warmington KS et al (1992) Role of IL-4 and IFN-gamma in Schistosoma mansoni egg-induced hypersensitivity granuloma formation. Orchestration, relative contribution, and relationship to macrophage function. J Immunol 148:900–906
Helming L, Gordon S (2007) Macrophage fusion induced by IL-4 alternative activation is a multistage process involving multiple target molecules. Eur J Immunol 37:33–42
Moreno JL, Mikhailenko I, Tondravi MM et al (2007) IL-4 promotes the formation of multinucleated giant cells from macrophage precursors by a STAT6-dependent, homotypic mechanism: contribution of E-cadherin. J Leukoc Biol 82:1542–1553
Van den Bossche J, Bogaert P, van Hengel J et al (2009) Alternatively activated macrophages engage in homotypic and heterotypic interactions through IL-4 and polyamine-induced E-cadherin/catenin complexes. Blood 114:4664–4674
Jones JA, McNally AK, Chang DT et al (2008) Matrix metalloproteinases and their inhibitors in the foreign body reaction on biomaterials. J Biomed Mater Res A 84:158–166
MacLauchlan S, Skokos EA, Meznarich N et al (2009) Macrophage fusion, giant cell formation, and the foreign body response require matrix metalloproteinase 9. J Leukoc Biol 85:617–626
Yagi M, Ninomiya K, Fujita N et al (2007) Induction of DC-STAMP by alternative activation and downstream signaling mechanisms. J Bone Miner Res 22:992–1001
Yagi M, Miyamoto T, Sawatani Y et al (2005) DC-STAMP is essential for cell-cell fusion in osteoclasts and foreign body giant cells. J Exp Med 202:345–351
Stein M, Keshav S, Harris N et al (1992) Interleukin 4 potently enhances murine macrophage mannose receptor activity: a marker of alternative immunologic macrophage activation. J Exp Med 176:287–292
McNally AK, DeFife KM, Anderson JM (1996) Interleukin-4-induced macrophage fusion is prevented by inhibitors of mannose receptor activity. Am J Pathol 149:975–985
Jansen KM, Pavlath GK (2006) Mannose receptor regulates myoblast motility and muscle growth. J Cell Biol 174:403–413
Lacey DL, Timms E, Tan HL et al (1998) Osteoprotegerin ligand is a cytokine that regulates osteoclast differentiation and activation. Cell 93:165–176
Yasuda H, Shima N, Nakagawa N et al (1998) Osteoclast differentiation factor is a ligand for osteoprotegerin/osteoclastogenesis-inhibitory factor and is identical to TRANCE/RANKL. Proc Natl Acad Sci USA 95:3597–3602
Takayanagi H, Kim S, Koga T et al (2002) Induction and activation of the transcription factor NFATc1 (NFAT2) integrate RANKL signaling in terminal differentiation of osteoclasts. Dev Cell 3:889–901
Kim K, Lee SH, Ha Kim J et al (2008) NFATc1 induces osteoclast fusion via up-regulation of Atp6v0d2 and the dendritic cell-specific transmembrane protein (DC-STAMP). Mol Endocrinol 22:176–185
Feng H, Cheng T, Steer JH et al (2009) Myocyte enhancer factor 2 and microphthalmia-associated transcription factor cooperate with NFATc1 to transactivate the V-ATPase d2 promoter during RANKL-induced osteoclastogenesis. J Biol Chem 284:14667–14676
Lee SH, Rho J, Jeong D et al (2006) v-ATPase V0 subunit d2-deficient mice exhibit impaired osteoclast fusion and increased bone formation. Nat Med 12:1403–1409
Simonet WS, Lacey DL, Dunstan CR et al (1997) Osteoprotegerin: a novel secreted protein involved in the regulation of bone density. Cell 89:309–319
Yasuda H, Shima N, Nakagawa N et al (1998) Identity of osteoclastogenesis inhibitory factor (OCIF) and osteoprotegerin (OPG): a mechanism by which OPG/OCIF inhibits osteoclastogenesis in vitro. Endocrinology 139:1329–1337
Helming L, Tomasello E, Kyriakides TR et al (2008) Essential role of DAP12 signaling in macrophage programming into a fusion-competent state. Sci Signal 1:ra11
Paloneva J, Mandelin J, Kiialainen A et al (2003) DAP12/TREM2 deficiency results in impaired osteoclast differentiation and osteoporotic features. J Exp Med 198:669–675
Kaifu T, Nakahara J, Inui M et al (2003) Osteopetrosis and thalamic hypomyelinosis with synaptic degeneration in DAP12-deficient mice. J Clin Invest 111:323–332
Peng Q, Malhotra S, Torchia JA et al (2010) TREM2- and DAP12-dependent activation of PI3K requires DAP10 and is inhibited by SHIP1. Sci Signal 3:ra38
Turnbull IR, Colonna M (2007) Activating and inhibitory functions of DAP12. Nat Rev Immunol 7:155–161
Zou W, Reeve JL, Liu Y et al (2008) DAP12 couples c-Fms activation to the osteoclast cytoskeleton by recruitment of Syk. Mol Cell 31:422–431
Sessions A, Horwitz AF (1983) Differentiation-related differences in the plasma membrane phospholipid asymmetry of myogenic and fibrogenic cells. Biochim Biophys Acta 728:103–111
Adler RR, Ng AK, Rote NS (1995) Monoclonal antiphosphatidylserine antibody inhibits intercellular fusion of the choriocarcinoma line, JAR. Biol Reprod 53:905–910
Gadella BM, Harrison RA (2000) The capacitating agent bicarbonate induces protein kinase A-dependent changes in phospholipid transbilayer behavior in the sperm plasma membrane. Development 127:2407–2420
Helming L, Winter J, Gordon S (2009) The scavenger receptor CD36 plays a role in cytokine-induced macrophage fusion. J Cell Sci 122:453–459
Leventis PA, Grinstein S (2010) The distribution and function of phosphatidylserine in cellular membranes. Annu Rev Biophys 39:407–427
Gauster M, Huppertz B (2010) The paradox of caspase 8 in human villous trophoblast fusion. Placenta 31:82–88
Rote NS, Wei BR, Xu C et al (2010) Caspase 8 and human villous cytotrophoblast differentiation. Placenta 31:89–96
Harrison RA, Gadella BM (2005) Bicarbonate-induced membrane processing in sperm capacitation. Theriogenology 63:342–351
Gadella BM, Harrison RA (2002) Capacitation induces cyclic adenosine 3′,5′-monophosphate-dependent, but apoptosis-unrelated, exposure of aminophospholipids at the apical head plasma membrane of boar sperm cells. Biol Reprod 67:340–350
Flesch FM, Brouwers JF, Nievelstein PF et al (2001) Bicarbonate stimulated phospholipid scrambling induces cholesterol redistribution and enables cholesterol depletion in the sperm plasma membrane. J Cell Sci 114:3543–3555
Harrison RA, Ashworth PJ, Miller NG (1996) Bicarbonate/CO2, an effector of capacitation, induces a rapid and reversible change in the lipid architecture of boar sperm plasma membranes. Mol Reprod Dev 45:378–391
Litvin TN, Kamenetsky M, Zarifyan A et al (2003) Kinetic properties of “soluble” adenylyl cyclase. Synergism between calcium and bicarbonate. J Biol Chem 278:15922–15926
Harrison RA, Miller NG (2000) cAMP-dependent protein kinase control of plasma membrane lipid architecture in boar sperm. Mol Reprod Dev 55:220–228
Harrison RA (1996) Capacitation mechanisms, and the role of capacitation as seen in eutherian mammals. Reprod Fertil Dev 8:581–594
de Vries KJ, Wiedmer T, Sims PJ et al (2003) Caspase-independent exposure of aminophospholipids and tyrosine phosphorylation in bicarbonate responsive human sperm cells. Biol Reprod 68:2122–2134
Callahan MK, Williamson P, Schlegel RA (2000) Surface expression of phosphatidylserine on macrophages is required for phagocytosis of apoptotic thymocytes. Cell Death Differ 7:645–653
MacKenzie A, Wilson HL, Kiss-Toth E et al (2001) Rapid secretion of interleukin-1beta by microvesicle shedding. Immunity 15:825–835
Van den Eijnde SM, Boshart L, Reutelingsperger CP et al (1997) Phosphatidylserine plasma membrane asymmetry in vivo: a pancellular phenomenon which alters during apoptosis. Cell Death Differ 4:311–316
van den Eijnde SM, van den Hoff MJ, Reutelingsperger CP et al (2001) Transient expression of phosphatidylserine at cell-cell contact areas is required for myotube formation. J Cell Sci 114:3631–3642
Lyden TW, Vogt E, Ng AK et al (1992) Monoclonal antiphospholipid antibody reactivity against human placental trophoblast. J Reprod Immunol 22:1–14
Lyden TW, Ng AK, Rote NS (1993) Modulation of phosphatidylserine epitope expression by BeWo cells during forskolin treatment. Placenta 14:177–186
Vogt E, Ng AK, Rote NS (1996) A model for the antiphospholipid antibody syndrome: monoclonal antiphosphatidylserine antibody induces intrauterine growth restriction in mice. Am J Obstet Gynecol 174:700–707
Daleke DL (2007) Phospholipid flippases. J Biol Chem 282:821–825
Florman HM, Jungnickel MK, Sutton KA (2008) Regulating the acrosome reaction. Int J Dev Biol 52:503–510
Wassarman PM, Litscher ES (2008) Mammalian fertilization is dependent on multiple membrane fusion events. Methods Mol Biol 475:99–113
Inoue N, Ikawa M, Isotani A et al (2005) The immunoglobulin superfamily protein Izumo is required for sperm to fuse with eggs. Nature 434:234–238
Myles DG, Koppel DE, Cowan AE et al (1987) Rearrangement of sperm surface antigens prior to fertilization. Ann N Y Acad Sci 513:262–273
Miranda PV, Allaire A, Sosnik J et al (2009) Localization of low-density detergent-resistant membrane proteins in intact and acrosome-reacted mouse sperm. Biol Reprod 80:897–904
Sosnik J, Miranda PV, Spiridonov NA et al (2009) Tssk6 is required for Izumo relocalization and gamete fusion in the mouse. J Cell Sci 122:2741–2749
Bleil JD, Wassarman PM (1983) Sperm–egg interactions in the mouse: sequence of events and induction of the acrosome reaction by a zona pellucida glycoprotein. Dev Biol 95:317–324
Arnoult C, Zeng Y, Florman HM (1996) ZP3-dependent activation of sperm cation channels regulates acrosomal secretion during mammalian fertilization. J Cell Biol 134:637–645
Florman HM, Tombes RM, First NL et al (1989) An adhesion-associated agonist from the zona pellucida activates G protein-promoted elevations of internal Ca2+ and pH that mediate mammalian sperm acrosomal exocytosis. Dev Biol 135:133–146
Arnoult C, Cardullo RA, Lemos JR et al (1996) Activation of mouse sperm T-type Ca2+ channels by adhesion to the egg zona pellucida. Proc Natl Acad Sci USA 93:13004–13009
Fukami K, Nakao K, Inoue T et al (2001) Requirement of phospholipase Cdelta4 for the zona pellucida-induced acrosome reaction. Science 292:920–923
Fukami K, Yoshida M, Inoue T et al (2003) Phospholipase Cdelta4 is required for Ca2+ mobilization essential for acrosome reaction in sperm. J Cell Biol 161:79–88
Jungnickel MK, Sutton KA, Wang Y et al (2007) Phosphoinositide-dependent pathways in mouse sperm are regulated by egg ZP3 and drive the acrosome reaction. Dev Biol 304:116–126
Achuthan A, Masendycz P, Lopez JA et al (2008) Regulation of the endosomal SNARE protein syntaxin 7 by colony-stimulating factor 1 in macrophages. Mol Cell Biol 28:6149–6159
Tomes CN, De Blas GA, Michaut MA et al (2005) alpha-SNAP and NSF are required in a priming step during the human sperm acrosome reaction. Mol Hum Reprod 11:43–51
Tomes CN, Michaut M, De Blas G et al (2002) SNARE complex assembly is required for human sperm acrosome reaction. Dev Biol 243:326–338
Lamkanfi M, Festjens N, Declercq W et al (2007) Caspases in cell survival, proliferation and differentiation. Cell Death Differ 14:44–55
Black S, Kadyrov M, Kaufmann P et al (2004) Syncytial fusion of human trophoblast depends on caspase 8. Cell Death Differ 11:90–98
Gauster M, Siwetz M, Orendi K et al (2010) Caspases rather than calpains mediate remodelling of the fodrin skeleton during human placental trophoblast fusion. Cell Death Differ 17:336–345
Martens S, McMahon HT (2008) Mechanisms of membrane fusion: disparate players and common principles. Nat Rev Mol Cell Biol 9:543–556
Mandal D, Mazumder A, Das P et al (2005) Fas-, caspase 8-, and caspase 3-dependent signaling regulates the activity of the aminophospholipid translocase and phosphatidylserine externalization in human erythrocytes. J Biol Chem 280:39460–39467
Gauster M, Siwetz M, Huppertz B (2009) Fusion of villous trophoblast can be visualized by localizing active caspase 8. Placenta 30:547–550
Murray TV, McMahon JM, Howley BA et al (2008) A non-apoptotic role for caspase-9 in muscle differentiation. J Cell Sci 121:3786–3793
Fernando P, Kelly JF, Balazsi K et al (2002) Caspase 3 activity is required for skeletal muscle differentiation. Proc Natl Acad Sci USA 99:11025–11030
Goll DE, Thompson VF, Li H et al (2003) The calpain system. Physiol Rev 83:731–801
Balcerzak D, Poussard S, Brustis JJ et al (1995) An antisense oligodeoxyribonucleotide to m-calpain mRNA inhibits myoblast fusion. J Cell Sci 108 (Pt 5):2077–2082
Kuchay SM, Kim N, Grunz EA et al (2007) Double knockouts reveal that protein tyrosine phosphatase 1B is a physiological target of calpain-1 in platelets. Mol Cell Biol 27:6038–6052
Honda M, Masui F, Kanzawa N et al (2008) Specific knockdown of m-calpain blocks myogenesis with cDNA deduced from the corresponding RNAi. Am J Physiol Cell Physiol 294:C957–965
Kramerova I, Kudryashova E, Tidball JG et al (2004) Null mutation of calpain 3 (p94) in mice causes abnormal sarcomere formation in vivo and in vitro. Hum Mol Genet 13:1373–1388
Kramerova I, Kudryashova E, Wu B et al (2006) Regulation of the M-cadherin-beta-catenin complex by calpain 3 during terminal stages of myogenic differentiation. Mol Cell Biol 26:8437–8447
Charrasse S, Comunale F, Grumbach Y et al (2006) RhoA GTPase regulates M-cadherin activity and myoblast fusion. Mol Biol Cell 17:749–759
Kim YS, Nakanishi G, Lewandoski M et al (2003) GLIS3, a novel member of the GLIS subfamily of Kruppel-like zinc finger proteins with repressor and activation functions. Nucleic Acids Res 31:5513–5525
Duan H, Nguyen HT (2006) Distinct posttranscriptional mechanisms regulate the activity of the Zn finger transcription factor lame duck during Drosophila myogenesis. Mol Cell Biol 26:1414–1423
Duan H, Skeath JB, Nguyen HT (2001) Drosophila Lame duck, a novel member of the Gli superfamily, acts as a key regulator of myogenesis by controlling fusion-competent myoblast development. Development 128:4489–4500
Furlong EE, Andersen EC, Null B et al (2001) Patterns of gene expression during Drosophila mesoderm development. Science 293:1629–1633
Ruiz-Gomez M, Coutts N, Suster ML et al (2002) myoblasts incompetent encodes a zinc finger transcription factor required to specify fusion-competent myoblasts in Drosophila. Development 129:133–141
Watanabe N, Hiramatsu K, Miyamoto R et al (2009) A murine model of neonatal diabetes mellitus in Glis3-deficient mice. FEBS Lett 583:2108–2113
Kang HS, Kim YS, ZeRuth G et al (2009) Transcription factor Glis3, a novel critical player in the regulation of pancreatic beta-cell development and insulin gene expression. Mol Cell Biol 29:6366–6379
Brand-Saberi B, Muller TS, Wilting J et al (1996) Scatter factor/hepatocyte growth factor (SF/HGF) induces emigration of myogenic cells at interlimb level in vivo. Dev Biol 179:303–308
Corti S, Salani S, Del Bo R et al (2001) Chemotactic factors enhance myogenic cell migration across an endothelial monolayer. Exp Cell Res 268:36–44
Lafreniere JF, Mills P, Bouchentouf M et al (2006) Interleukin-4 improves the migration of human myogenic precursor cells in vitro and in vivo. Exp Cell Res 312:1127–1141
Lafreniere JF, Mills P, Tremblay JP et al (2004) Growth factors improve the in vivo migration of human skeletal myoblasts by modulating their endogenous proteolytic activity. Transplantation 77:1741–1747
Webb SE, Lee KK, Tang MK et al (1997) Fibroblast growth factors 2 and 4 stimulate migration of mouse embryonic limb myogenic cells. Dev Dyn 209:206–216
Robertson TA, Maley MA, Grounds MD et al (1993) The role of macrophages in skeletal muscle regeneration with particular reference to chemotaxis. Exp Cell Res 207:321–331
Minniti CP, Luan D, O‘Grady C et al (1995) Insulin-like growth factor II overexpression in myoblasts induces phenotypic changes typical of the malignant phenotype. Cell Growth Differ 6:263–269
Germani A, Di Carlo A, Mangoni A et al (2003) Vascular endothelial growth factor modulates skeletal myoblast function. Am J Pathol 163:1417–1428
Ratajczak MZ, Majka M, Kucia M et al (2003) Expression of functional CXCR4 by muscle satellite cells and secretion of SDF-1 by muscle-derived fibroblasts is associated with the presence of both muscle progenitors in bone marrow and hematopoietic stem/progenitor cells in muscles. Stem Cells 21:363–371
Allen DL, Teitelbaum DH, Kurachi K (2003) Growth factor stimulation of matrix metalloproteinase expression and myoblast migration and invasion in vitro. Am J Physiol Cell Physiol 284:C805–815
Torrente Y, El Fahime E, Caron NJ et al (2003) Tumor necrosis factor-alpha (TNF-alpha) stimulates chemotactic response in mouse myogenic cells. Cell Transplant 12:91–100
Chowdhury SR, Muneyuki Y, Takezawa Y et al (2009) Synergic stimulation of laminin and epidermal growth factor facilitates the myoblast growth through promoting migration. J Biosci Bioeng 108:174–177
Adams JC, Schwartz MA (2000) Stimulation of fascin spikes by thrombospondin-1 is mediated by the GTPases Rac and Cdc42. J Cell Biol 150:807–822
Turner DC, Lawton J, Dollenmeier P et al (1983) Guidance of myogenic cell migration by oriented deposits of fibronectin. Dev Biol 95:497–504
Yao CC, Ziober BL, Sutherland AE et al (1996) Laminins promote the locomotion of skeletal myoblasts via the alpha 7 integrin receptor. J Cell Sci 109 (Pt 13):3139–3150
Bischoff R (1997) Chemotaxis of skeletal muscle satellite cells. Dev Dyn 208:505–515
Rosario M, Birchmeier W (2003) How to make tubes: signaling by the Met receptor tyrosine kinase. Trends Cell Biol 13:328–335
Odemis V, Lamp E, Pezeshki G et al (2005) Mice deficient in the chemokine receptor CXCR4 exhibit impaired limb innervation and myogenesis. Mol Cell Neurosci 30:494–505
Forde S, Tye BJ, Newey SE et al (2007) Endolyn (CD164) modulates the CXCL12-mediated migration of umbilical cord blood CD133+ cells. Blood 109:1825–1833
Bae GU, Gaio U, Yang YJ et al (2008) Regulation of myoblast motility and fusion by the CXCR4-associated sialomucin, CD164. J Biol Chem 283:8301–8309
Miller RJ, Banisadr G, Bhattacharyya BJ (2008) CXCR4 signaling in the regulation of stem cell migration and development. J Neuroimmunol 198:31–38
Nagasawa T (2007) The chemokine CXCL12 and regulation of HSC and B lymphocyte development in the bone marrow niche. Adv Exp Med Biol 602:69–75
Lazarini F, Tham TN, Casanova P et al (2003) Role of the alpha-chemokine stromal cell-derived factor (SDF-1) in the developing and mature central nervous system. Glia 42:139–148
Stumm RK, Rummel J, Junker V et al (2002) A dual role for the SDF-1/CXCR4 chemokine receptor system in adult brain: isoform-selective regulation of SDF-1 expression modulates CXCR4-dependent neuronal plasticity and cerebral leukocyte recruitment after focal ischemia. J Neurosci 22:5865–5878
Yamaguchi J, Kusano KF, Masuo O et al (2003) Stromal cell-derived factor-1 effects on ex vivo expanded endothelial progenitor cell recruitment for ischemic neovascularization. Circulation 107:1322–1328
Fox JM, Chamberlain G, Ashton BA et al (2007) Recent advances into the understanding of mesenchymal stem cell trafficking. Br J Haematol 137:491–502
Hill WD, Hess DC, Martin-Studdard A et al (2004) SDF-1 (CXCL12) is upregulated in the ischemic penumbra following stroke: association with bone marrow cell homing to injury. J Neuropathol Exp Neurol 63:84–96
Togel F, Isaac J, Hu Z et al (2005) Renal SDF-1 signals mobilization and homing of CXCR4-positive cells to the kidney after ischemic injury. Kidney Int 67:1772–1784
Blanchet MR, McNagny KM (2009) Stem cells, inflammation and allergy. Allergy Asthma Clin Immunol 5:13
Kucia M, Ratajczak J, Reca R et al (2004) Tissue-specific muscle, neural and liver stem/progenitor cells reside in the bone marrow, respond to an SDF-1 gradient and are mobilized into peripheral blood during stress and tissue injury. Blood Cells Mol Dis 32:52–57
Davies PS, Powell AE, Swain JR et al (2009) Inflammation and proliferation act together to mediate intestinal cell fusion. PLoS ONE 4:e6530
Nygren JM, Liuba K, Breitbach M et al (2008) Myeloid and lymphoid contribution to non-haematopoietic lineages through irradiation-induced heterotypic cell fusion. Nat Cell Biol 10:584–592
Johansson CB, Youssef S, Koleckar K et al (2008) Extensive fusion of haematopoietic cells with Purkinje neurons in response to chronic inflammation. Nat Cell Biol 10:575–583
Horsley V, Friday BB, Matteson S et al (2001) Regulation of the growth of multinucleated muscle cells by an NFATC2-dependent pathway. J Cell Biol 153:329–338
Sotiropoulos A, Ohanna M, Kedzia C et al (2006) Growth hormone promotes skeletal muscle cell fusion independent of insulin-like growth factor 1 up-regulation. Proc Natl Acad Sci USA 103:7315–7320
Griffin CA, Kafadar KA, Pavlath GK (2009) MOR23 promotes muscle regeneration and regulates cell adhesion and migration. Dev Cell 17:649–661
Fukuda N, Yomogida K, Okabe M et al (2004) Functional characterization of a mouse testicular olfactory receptor and its role in chemosensing and in regulation of sperm motility. J Cell Sci 117:5835–5845
Tangirala RK, Murao K, Quehenberger O (1997) Regulation of expression of the human monocyte chemotactic protein-1 receptor (hCCR2) by cytokines. J Biol Chem 272:8050–8056
Kyriakides TR, Foster MJ, Keeney GE et al (2004) The CC chemokine ligand, CCL2/MCP1, participates in macrophage fusion and foreign body giant cell formation. Am J Pathol 165:2157–2166
Jay SM, Skokos E, Laiwalla F et al (2007) Foreign body giant cell formation is preceded by lamellipodia formation and can be attenuated by inhibition of Rac1 activation. Am J Pathol 171:632–640
Miyamoto K, Ninomiya K, Sonoda KH et al (2009) MCP-1 expressed by osteoclasts stimulates osteoclastogenesis in an autocrine/paracrine manner. Biochem Biophys Res Commun 383:373–377
Harper CV, Barratt CL, Publicover SJ (2004) Stimulation of human spermatozoa with progesterone gradients to simulate approach to the oocyte. Induction of [Ca(2+)](i) oscillations and cyclical transitions in flagellar beating. J Biol Chem 279:46315–46325
Teves ME, Barbano F, Guidobaldi HA et al (2006) Progesterone at the picomolar range is a chemoattractant for mammalian spermatozoa. Fertil Steril 86:745–749
Teves ME, Guidobaldi HA, Unates DR et al (2010) Progesterone sperm chemoattraction may be modulated by its corticosteroid-binding globulin carrier protein. Fertil Steril 93:2450–2452
Teves ME, Guidobaldi HA, Unates DR et al (2009) Molecular mechanism for human sperm chemotaxis mediated by progesterone. PLoS ONE 4:e8211
Osman RA, Andria ML, Jones AD et al (1989) Steroid induced exocytosis: the human sperm acrosome reaction. Biochem Biophys Res Commun 160:828–833
Hood JD, Cheresh DA (2002) Role of integrins in cell invasion and migration. Nat Rev Cancer 2:91–100
Ocalan M, Goodman SL, Kuhl U et al (1988) Laminin alters cell shape and stimulates motility and proliferation of murine skeletal myoblasts. Dev Biol 125:158–167
Sonnenberg A, Modderman PW, Hogervorst F (1988) Laminin receptor on platelets is the integrin VLA-6. Nature 336:487–489
Kramer RH, McDonald KA, Vu MP (1989) Human melanoma cells express a novel integrin receptor for laminin. J Biol Chem 264:15642–15649
Siegel AL, Atchison K, Fisher KE et al (2009) 3D timelapse analysis of muscle satellite cell motility. Stem Cells 27:2527–2538
Mayer U, Saher G, Fassler R et al (1997) Absence of integrin alpha 7 causes a novel form of muscular dystrophy. Nat Genet 17:318–323
Schwander M, Leu M, Stumm M et al (2003) Beta1 integrins regulate myoblast fusion and sarcomere assembly. Dev Cell 4:673–685
Echtermeyer F, Schober S, Poschl E et al (1996) Specific induction of cell motility on laminin by alpha 7 integrin. J Biol Chem 271:2071–2075
Glenn HL, Wang Z, Schwartz LM (2010) Acheron, a Lupus antigen family member, regulates integrin expression, adhesion, and motility in differentiating myoblasts. Am J Physiol Cell Physiol 298:C46–55
Wang Z, Glenn H, Brown C et al (2009) Regulation of muscle differentiation and survival by Acheron. Mech Dev 126:700–709
Calderwood DA, Shattil SJ, Ginsberg MH (2000) Integrins and actin filaments: reciprocal regulation of cell adhesion and signaling. J Biol Chem 275:22607–22610
Alvarez B, Stroeken PJ, Edel MJ et al (2008) Integrin Cytoplasmic domain-Associated Protein-1 (ICAP-1) promotes migration of myoblasts and affects focal adhesions. J Cell Physiol 214:474–482
Boissy P, Machuca I, Pfaff M et al (1998) Aggregation of mononucleated precursors triggers cell surface expression of alphavbeta3 integrin, essential to formation of osteoclast-like multinucleated cells. J Cell Sci 111(Pt 17):2563–2574
McHugh KP, Hodivala-Dilke K, Zheng MH et al (2000) Mice lacking beta3 integrins are osteosclerotic because of dysfunctional osteoclasts. J Clin Invest 105:433–440
Lakkakorpi PT, Bett AJ, Lipfert L et al (2003) PYK2 autophosphorylation, but not kinase activity, is necessary for adhesion-induced association with c-Src, osteoclast spreading, and bone resorption. J Biol Chem 278:11502–11512
Miyazaki T, Sanjay A, Neff L et al (2004) Src kinase activity is essential for osteoclast function. J Biol Chem 279:17660–17666
Brazier H, Pawlak G, Vives V et al (2009) The Rho GTPase Wrch1 regulates osteoclast precursor adhesion and migration. Int J Biochem Cell Biol 41:1391–1401
Brazier H, Stephens S, Ory S 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
Kim T, Ha HI, Kim N et al (2009) Adrm1 interacts with Atp6v0d2 and regulates osteoclast differentiation. Biochem Biophys Res Commun 390:585–590
Husnjak K, Elsasser S, Zhang N et al (2008) Proteasome subunit Rpn13 is a novel ubiquitin receptor. Nature 453:481–488
Stricker J, Falzone T, Gardel ML (2010) Mechanics of the F-actin cytoskeleton. J Biomech 43:9–14
Nowak SJ, Nahirney PC, Hadjantonakis AK et al (2009) Nap1-mediated actin remodeling is essential for mammalian myoblast fusion. J Cell Sci 122:3282–3293
Kawamura K, Takano K, Suetsugu S et al (2004) N-WASP and WAVE2 acting downstream of phosphatidylinositol 3-kinase are required for myogenic cell migration induced by hepatocyte growth factor. J Biol Chem 279:54862–54871
Vasyutina E, Martarelli B, Brakebusch C et al (2009) The small G-proteins Rac1 and Cdc42 are essential for myoblast fusion in the mouse. Proc Natl Acad Sci USA 106:8935–8940
Wells CM, Walmsley M, Ooi S et al (2004) Rac1-deficient macrophages exhibit defects in cell spreading and membrane ruffling but not migration. J Cell Sci 117:1259–1268
Wheeler AP, Wells CM, Smith SD et al (2006) Rac1 and Rac2 regulate macrophage morphology but are not essential for migration. J Cell Sci 119:2749–2757
Rohatgi R, Ho HY, Kirschner MW (2000) Mechanism of N-WASP activation by CDC42 and phosphatidylinositol 4, 5-bisphosphate. J Cell Biol 150:1299–1310
Morishima S, Morita I, Tokushima T et al (2003) Expression and role of mannose receptor/terminal high-mannose type oligosaccharide on osteoclast precursors during osteoclast formation. J Endocrinol 176:285–292
Taylor ME, Bezouska K, Drickamer K (1992) Contribution to ligand binding by multiple carbohydrate-recognition domains in the macrophage mannose receptor. J Biol Chem 267:1719–1726
Chabot V, Reverdiau P, Iochmann S et al (2006) CCL5-enhanced human immature dendritic cell migration through the basement membrane in vitro depends on matrix metalloproteinase-9. J Leukoc Biol 79:767–778
Rahat MA, Marom B, Bitterman H et al (2006) Hypoxia reduces the output of matrix metalloproteinase-9 (MMP-9) in monocytes by inhibiting its secretion and elevating membranal association. J Leukoc Biol 79:706–718
Barclay AN (2003) Membrane proteins with immunoglobulin-like domains–a master superfamily of interaction molecules. Semin Immunol 15:215–223
Xu Z, Jin B (2010) A novel interface consisting of homologous immunoglobulin superfamily members with multiple functions. Cell Mol Immunol 7:11–19
Sohn RL, Huang P, Kawahara G et al (2009) A role for nephrin, a renal protein, in vertebrate skeletal muscle cell fusion. Proc Natl Acad Sci USA 106:9274–9279
Donoviel DB, Freed DD, Vogel H et al (2001) Proteinuria and perinatal lethality in mice lacking NEPH1, a novel protein with homology to NEPHRIN. Mol Cell Biol 21:4829–4836
Garg P, Verma R, Nihalani D et al (2007) Neph1 cooperates with nephrin to transduce a signal that induces actin polymerization. Mol Cell Biol 27:8698–8712
Krauss RS (2010) Regulation of promyogenic signal transduction by cell-cell contact and adhesion. Exp Cell Res 316:3042–3049
Lu M, Krauss RS (2010) N-cadherin ligation, but not Sonic hedgehog binding, initiates Cdo-dependent p38alpha/beta MAPK signaling in skeletal myoblasts. Proc Natl Acad Sci USA 107:4212–4217
Kang JS, Bae GU, Yi MJ et al (2008) A Cdo-Bnip-2-Cdc42 signaling pathway regulates p38alpha/beta MAPK activity and myogenic differentiation. J Cell Biol 182:497–507
Guasconi V, Puri PL (2009) Chromatin: the interface between extrinsic cues and the epigenetic regulation of muscle regeneration. Trends Cell Biol 19:286–294
Takaesu G, Kang JS, Bae GU et al (2006) Activation of p38alpha/beta MAPK in myogenesis via binding of the scaffold protein JLP to the cell surface protein Cdo. J Cell Biol 175:383–388
Cole F, Zhang W, Geyra A et al (2004) Positive regulation of myogenic bHLH factors and skeletal muscle development by the cell surface receptor CDO. Dev Cell 7:843–854
Bae GU, Yang YJ, Jiang G et al (2009) Neogenin regulates skeletal myofiber size and focal adhesion kinase and extracellular signal-regulated kinase activities in vivo and in vitro. Mol Biol Cell 20:4920–4931
De Vries M, Cooper HM (2008) Emerging roles for neogenin and its ligands in CNS development. J Neurochem 106:1483–1492
Quach NL, Biressi S, Reichardt LF et al (2009) Focal adhesion kinase signaling regulates the expression of caveolin 3 and beta1 integrin, genes essential for normal myoblast fusion. Mol Biol Cell 20:3422–3435
Dickson G, Gower HJ, Barton CH et al (1987) Human muscle neural cell adhesion molecule (N-CAM): identification of a muscle-specific sequence in the extracellular domain. Cell 50:1119–1130
Povlsen GK, Ditlevsen DK (2010) The neural cell adhesion molecule NCAM and lipid rafts. Adv Exp Med Biol 663:183–198
Dickson G, Peck D, Moore SE et al (1990) Enhanced myogenesis in NCAM-transfected mouse myoblasts. Nature 344:348–351
Baldwin TJ, Fazeli MS, Doherty P et al (1996) Elucidation of the molecular actions of NCAM and structurally related cell adhesion molecules. J Cell Biochem 61:502–513
Charlton CA, Mohler WA, Blau HM (2000) Neural cell adhesion molecule (NCAM) and myoblast fusion. Developmental Biology 221:112–119
Okabe M, Adachi T, Takada K et al (1987) Capacitation-related changes in antigen distribution on mouse sperm heads and its relation to fertilization rate in vitro. J Reprod Immunol 11:91–100
Ellerman DA, Pei J, Gupta S et al (2009) Izumo is part of a multiprotein family whose members form large complexes on mammalian sperm. Mol Reprod Dev 76:1188–1199
Lundberg P, Koskinen C, Baldock PA et al (2007) Osteoclast formation is strongly reduced both in vivo and in vitro in the absence of CD47/SIRPalpha-interaction. Biochem Biophys Res Commun 352:444–448
Han X, Sterling H, Chen Y et al (2000) CD47, a ligand for the macrophage fusion receptor, participates in macrophage multinucleation. J Biol Chem 275:37984–37992
Saginario C, Qian HY, Vignery A (1995) Identification of an inducible surface molecule specific to fusing macrophages. Proc Natl Acad Sci USA 92:12210–12214
Matozaki T, Murata Y, Okazawa H et al (2009) Functions and molecular mechanisms of the CD47-SIRPalpha signalling pathway. Trends Cell Biol 19:72–80
Oldenborg PA, Gresham HD, Lindberg FP (2001) CD47-signal regulatory protein alpha (SIRPalpha) regulates Fcgamma and complement receptor-mediated phagocytosis. J Exp Med 193:855–862
Motegi S, Okazawa H, Ohnishi H et al (2003) Role of the CD47-SHPS-1 system in regulation of cell migration. EMBO J 22:2634–2644
Brown EJ, Frazier WA (2001) Integrin-associated protein (CD47) and its ligands. Trends Cell Biol 11:130–135
Borghi N, James Nelson W (2009) Intercellular adhesion in morphogenesis: molecular and biophysical considerations. Curr Top Dev Biol 89:1–32
Krauss RS, Cole F, Gaio U et al (2005) Close encounters: regulation of vertebrate skeletal myogenesis by cell-cell contact. J Cell Sci 118:2355–2362
Rufas O, Fisch B, Ziv S et al (2000) Expression of cadherin adhesion molecules on human gametes. Mol Hum Reprod 6:163–169
Marin-Briggiler CI, Lapyckyj L, Gonzalez Echeverria MF et al (2010) Neural cadherin is expressed in human gametes and participates in sperm-oocyte interaction events. Int J Androl 33:e228–239
Radice GL, Rayburn H, Matsunami H et al (1997) Developmental defects in mouse embryos lacking N-cadherin. Dev Biol 181:64–78
Charlton CA, Mohler WA, Radice GL et al (1997) Fusion competence of myoblasts rendered genetically null for N-cadherin in culture. J Cell Biol 138:331–336
Huttenlocher A, Lakonishok M, Kinder M et al (1998) Integrin and cadherin synergy regulates contact inhibition of migration and motile activity. J Cell Biol 141:515–526
Charrasse S, Comunale F, Fortier M et al (2007) M-cadherin activates Rac1 GTPase through the Rho-GEF trio during myoblast fusion. Mol Biol Cell 18:1734–1743
Mukai A, Kurisaki T, Sato SB et al (2009) Dynamic clustering and dispersion of lipid rafts contribute to fusion competence of myogenic cells. Exp Cell Res 315:3052–3063
Hsiao SP, Chen SL (2010) Myogenic regulatory factors regulate M-cadherin expression by targeting its proximal promoter elements. Biochem J 428:223–233
Zeschnigk M, Kozian D, Kuch C et al (1995) Involvement of M-cadherin in terminal differentiation of skeletal muscle cells. J Cell Sci 108 (Pt 9):2973–2981
Kuch C, Winnekendonk D, Butz S et al (1997) M-cadherin-mediated cell adhesion and complex formation with the catenins in myogenic mouse cells. Exp Cell Res 232:331–338
Hollnagel A, Grund C, Franke WW et al (2002) The cell adhesion molecule M-cadherin is not essential for muscle development and regeneration. Mol Cell Biol 22:4760–4770
Mbalaviele G, Chen H, Boyce BF et al (1995) The role of cadherin in the generation of multinucleated osteoclasts from mononuclear precursors in murine marrow. J Clin Invest 95:2757–2765
Floridon C, Nielsen O, Holund B et al (2000) Localization of E-cadherin in villous, extravillous and vascular trophoblasts during intrauterine, ectopic and molar pregnancy. Mol Hum Reprod 6:943–950
MacCalman CD, Furth EE, Omigbodun A et al (1996) Regulated expression of cadherin-11 in human epithelial cells: a role for cadherin-11 in trophoblast-endometrium interactions? Dev Dyn 206:201–211
Getsios S, MacCalman CD (2003) Cadherin-11 modulates the terminal differentiation and fusion of human trophoblastic cells in vitro. Dev Biol 257:41–54
Le Naour F, Andre M, Boucheix C et al (2006) Membrane microdomains and proteomics: lessons from tetraspanin microdomains and comparison with lipid rafts. Proteomics 6:6447–6454
Ziyyat A, Rubinstein E, Monier-Gavelle F et al (2006) CD9 controls the formation of clusters that contain tetraspanins and the integrin alpha 6 beta 1, which are involved in human and mouse gamete fusion. J Cell Sci 119:416–424
Kaji K, Oda S, Shikano T et al (2000) The gamete fusion process is defective in eggs of Cd9-deficient mice. Nat Genet 24:279–282
Le Naour F, Rubinstein E, Jasmin C et al (2000) Severely reduced female fertility in CD9-deficient mice. Science 287:319–321
Miyado K, Yamada G, Yamada S et al (2000) Requirement of CD9 on the egg plasma membrane for fertilization. Science 287:321–324
Rubinstein E, Ziyyat A, Prenant M et al (2006) Reduced fertility of female mice lacking CD81. Dev Biol 290:351–358
Kaji K, Oda S, Miyazaki S et al (2002) Infertility of CD9-deficient mouse eggs is reversed by mouse CD9, human CD9, or mouse CD81; polyadenylated mRNA injection developed for molecular analysis of sperm-egg fusion. Dev Biol 247:327–334
Zhu GZ, Miller BJ, Boucheix C et al (2002) Residues SFQ (173-175) in the large extracellular loop of CD9 are required for gamete fusion. Development 129:1995–2002
Runge KE, Evans JE, He ZY et al (2007) Oocyte CD9 is enriched on the microvillar membrane and required for normal microvillar shape and distribution. Dev Biol 304:317–325
Takeda Y, Tachibana I, Miyado K et al (2003) Tetraspanins CD9 and CD81 function to prevent the fusion of mononuclear phagocytes. J Cell Biol 161:945–956
Parthasarathy V, Martin F, Higginbottom A et al (2009) Distinct roles for tetraspanins CD9, CD63 and CD81 in the formation of multinucleated giant cells. Immunology 127:237–248
Ishii M, Iwai K, Koike M et al (2006) RANKL-induced expression of tetraspanin CD9 in lipid raft membrane microdomain is essential for cell fusion during osteoclastogenesis. J Bone Miner Res 21:965–976
Tachibana I, Hemler ME (1999) Role of transmembrane 4 superfamily (TM4SF) proteins CD9 and CD81 in muscle cell fusion and myotube maintenance. J Cell Biol 146:893–904
Brzoska E, Bello V, Darribere T et al (2006) Integrin alpha3 subunit participates in myoblast adhesion and fusion in vitro. Differentiation 74:105–118
Puissegur MP, Lay G, Gilleron M et al (2007) Mycobacterial lipomannan induces granuloma macrophage fusion via a TLR2-dependent, ADAM9- and beta1 integrin-mediated pathway. J Immunol 178:3161–3169
McNally AK, Anderson JM (2002) Beta1 and beta2 integrins mediate adhesion during macrophage fusion and multinucleated foreign body giant cell formation. Am J Pathol 160:621–630
Coonrod SA, Naaby-Hansen S, Shetty J et al (1999) Treatment of mouse oocytes with PI-PLC releases 70-kDa (pI 5) and 35- to 45-kDa (pI 5.5) protein clusters from the egg surface and inhibits sperm-oolemma binding and fusion. Dev Biol 207:334–349
Alfieri JA, Martin AD, Takeda J et al (2003) Infertility in female mice with an oocyte-specific knockout of GPI-anchored proteins. J Cell Sci 116:2149–2155
Tousseyn T, Jorissen E, Reiss K et al (2006) (Make) stick and cut loose–disintegrin metalloproteases in development and disease. Birth Defects Res C Embryo Today 78:24–46
Kurisaki T, Masuda A, Sudo K et al (2003) Phenotypic analysis of Meltrin alpha (ADAM12)-deficient mice: involvement of Meltrin alpha in adipogenesis and myogenesis. Mol Cell Biol 23:55–61
Kukita T, Wada N, Kukita A et al (2004) RANKL-induced DC-STAMP is essential for osteoclastogenesis. J Exp Med 200:941–946
Mensah KA, Ritchlin CT, Schwarz EM (2010) RANKL induces heterogeneous DC-STAMP(lo) and DC-STAMP(hi) osteoclast precursors of which the DC-STAMP(lo) precursors are the master fusogens. J Cell Physiol 223:76–83
Hotokezaka H, Sakai E, Ohara N et al (2007) Molecular analysis of RANKL-independent cell fusion of osteoclast-like cells induced by TNF-alpha, lipopolysaccharide, or peptidoglycan. J Cell Biochem 101:122–134
Yang M, Birnbaum MJ, MacKay CA et al (2008) Osteoclast stimulatory transmembrane protein (OC-STAMP), a novel protein induced by RANKL that promotes osteoclast differentiation. J Cell Physiol 215:497–505
Sapir A, Avinoam O, Podbilewicz B et al (2008) Viral and developmental cell fusion mechanisms: conservation and divergence. Dev Cell 14:11–21
Oren-Suissa M, Podbilewicz B (2007) Cell fusion during development. Trends Cell Biol 17:537–546
Chernomordik LV, Zimmerberg J, Kozlov MM (2006) Membranes of the world unite! J Cell Biol 175:201–207
Jahn R, Lang T, Sudhof TC (2003) Membrane fusion. Cell 112:519–533
Costa M, Raich W, Agbunag C et al (1998) A putative catenin-cadherin system mediates morphogenesis of the Caenorhabditis elegans embryo. J Cell Biol 141:297–308
Ding M, Woo WM, Chisholm AD (2004) The cytoskeleton and epidermal morphogenesis in C. elegans. Exp Cell Res 301:84–90
McKeown C, Praitis V, Austin J (1998) sma-1 encodes a betaH-spectrin homolog required for Caenorhabditis elegans morphogenesis. Development 125:2087–2098
Duan R, Gallagher PJ (2009) Dependence of myoblast fusion on a cortical actin wall and nonmuscle myosin IIA. Dev Biol 325:374–385
Swailes NT, Colegrave M, Knight PJ et al (2006) Non-muscle myosins 2A and 2B drive changes in cell morphology that occur as myoblasts align and fuse. J Cell Sci 119:3561–3570
Chen A, Leikina E, Melikov K et al (2008) Fusion-pore expansion during syncytium formation is restricted by an actin network. J Cell Sci 121:3619–3628
Richard JP, Leikina E, Chernomordik LV (2009) Cytoskeleton reorganization in influenza hemagglutinin-initiated syncytium formation. Biochim Biophys Acta 1788:450–457
Wurth MA, Schowalter RM, Smith EC et al (2010) The actin cytoskeleton inhibits pore expansion during PIV5 fusion protein-promoted cell-cell fusion. Virology 404:117–126
Berger S, Schafer G, Kesper DA et al (2008) WASP and SCAR have distinct roles in activating the Arp2/3 complex during myoblast fusion. J Cell Sci 121:1303–1313
Gildor B, Massarwa R, Shilo BZ et al (2009) The SCAR and WASp nucleation-promoting factors act sequentially to mediate Drosophila myoblast fusion. EMBO Rep 10:1043–1050
Massarwa R, Carmon S, Shilo BZ et al (2007) WIP/WASp-based actin-polymerization machinery is essential for myoblast fusion in Drosophila. Dev Cell 12:557–569
Pollard TD, Borisy GG (2003) Cellular motility driven by assembly and disassembly of actin filaments. Cell 112:453–465
Saarikangas J, Zhao H, Lappalainen P (2010) Regulation of the actin cytoskeleton-plasma membrane interplay by phosphoinositides. Physiol Rev 90:259–289
Harmon B, Campbell N, Ratner L (2010) Role of Abl kinase and the Wave2 signaling complex in HIV-1 entry at a post-hemifusion step. PLoS Pathog 6:e1000956
Laurin M, Fradet N, Blangy A et al (2008) The atypical Rac activator Dock180 (Dock1) regulates myoblast fusion in vivo. Proc Natl Acad Sci USA 105:15446–15451
Pajcini KV, Pomerantz JH, Alkan O et al (2008) Myoblasts and macrophages share molecular components that contribute to cell-cell fusion. J Cell Biol 180:1005–1019
O‘Brien SP, Seipel K, Medley QG et al (2000) Skeletal muscle deformity and neuronal disorder in Trio exchange factor-deficient mouse embryos. Proc Natl Acad Sci USA 97:12074–12078
Chen EH, Pryce BA, Tzeng JA et al (2003) Control of myoblast fusion by a guanine nucleotide exchange factor, loner, and its effector ARF6. Cell 114:751–762
Dunphy JL, Moravec R, Ly K et al (2006) The Arf6 GEF GEP100/BRAG2 regulates cell adhesion by controlling endocytosis of beta1 integrins. Curr Biol 16:315–320
Faix J, Breitsprecher D, Stradal TE et al (2009) Filopodia: Complex models for simple rods. Int J Biochem Cell Biol 41:1656–1664
Lingwood D, Simons K (2010) Lipid rafts as a membrane-organizing principle. Science 327:46–50
Prives J, Shinitzky M (1977) Increased membrane fluidity precedes fusion of muscle cells. Nature 268:761–763
Sekiya T, Takenawa T, Nozawa Y (1984) Reorganization of membrane cholesterol during membrane fusion in myogenesis in vitro: a study using the filipin-cholesterol complex. Cell Struct Funct 9:143–155
Waheed AA, Freed EO (2009) Lipids and membrane microdomains in HIV-1 replication. Virus Res 143:162–176
Kielian M, Rey FA (2006) Virus membrane-fusion proteins: more than one way to make a hairpin. Nat Rev Microbiol 4:67–76
Pontow SE, Heyden NV, Wei S et al (2004) Actin cytoskeletal reorganizations and coreceptor-mediated activation of rac during human immunodeficiency virus-induced cell fusion. J Virol 78:7138–7147
Mohler WA, Shemer G, del Campo JJ et al (2002) The type I membrane protein EFF-1 is essential for developmental cell fusion. Dev Cell 2:355–362
Sapir A, Choi J, Leikina E et al (2007) AFF-1, a FOS-1-regulated fusogen, mediates fusion of the anchor cell in C. elegans. Dev Cell 12:683–698
Mi S, Lee X, Li X et al (2000) Syncytin is a captive retroviral envelope protein involved in human placental morphogenesis. Nature 403:785–789
Blaise S, de Parseval N, Benit L et al (2003) Genomewide screening for fusogenic human endogenous retrovirus envelopes identifies syncytin 2, a gene conserved on primate evolution. Proc Natl Acad Sci USA 100:13013–13018
Frendo JL, Olivier D, Cheynet V et al (2003) Direct involvement of HERV-W Env glycoprotein in human trophoblast cell fusion and differentiation. Mol Cell Biol 23:3566–3574
Blond JL, Lavillette D, Cheynet V et al (2000) An envelope glycoprotein of the human endogenous retrovirus HERV-W is expressed in the human placenta and fuses cells expressing the type D mammalian retrovirus receptor. J Virol 74:3321–3329
Marin M, Lavillette D, Kelly SM et al (2003) N-linked glycosylation and sequence changes in a critical negative control region of the ASCT1 and ASCT2 neutral amino acid transporters determine their retroviral receptor functions. J Virol 77:2936–2945
Sun QY (2003) Cellular and molecular mechanisms leading to cortical reaction and polyspermy block in mammalian eggs. Microsc Res Tech 61:342–348
Castellucci M, Kaufmann P, Bischof P (1990) Extracellular matrix influences hormone and protein production by human chorionic villi. Cell Tissue Res 262:135–142
Demonbreun AR, Posey AD, Heretis K et al (2010) Myoferlin is required for insulin-like growth factor response and muscle growth. FASEB J 24:1284–1295
Doherty KR, Demonbreun AR, Wallace GQ et al (2008) The endocytic recycling protein EHD2 interacts with myoferlin to regulate myoblast fusion. J Biol Chem 283:20252–20260
Doherty KR, Cave A, Davis DB et al (2005) Normal myoblast fusion requires myoferlin. Development 132:5565–5575
Demonbreun AR, Lapidos KA, Heretis K et al (2010) Myoferlin regulation by NFAT in muscle injury, regeneration and repair. J Cell Sci 123:2413–2422
Adams JM, Cory S (1998) The Bcl-2 protein family: arbiters of cell survival. Science 281:1322–1326
Sakuragi N, Matsuo H, Coukos G et al (1994) Differentiation-dependent expression of the BCL-2 proto-oncogene in the human trophoblast lineage. J Soc Gynecol Investig 1:164–172
Chang DW, Xing Z, Pan Y et al (2002) c-FLIP(L) is a dual function regulator for caspase-8 activation and CD95-mediated apoptosis. EMBO J 21:3704–3714
Ka H, Hunt JS (2006) FLICE-inhibitory protein: expression in early and late gestation human placentas. Placenta 27:626–634
Ogle BM, Butters KB, Plummer TB et al (2004) Spontaneous fusion of cells between species yields transdifferentiation and retroviral in vivo. FASEB J 18:548–550
Ferrari G, Cusella-De Angelis G, Coletta M et al (1998) Muscle regeneration by bone marrow-derived myogenic progenitors. Science 279:1528–1530
Wang X, Willenbring H, Akkari Y et al (2003) Cell fusion is the principal source of bone-marrow-derived hepatocytes. Nature 422:897–900
Author information
Authors and Affiliations
Corresponding author
Editor information
Editors and Affiliations
Rights and permissions
Copyright information
© 2011 Springer Science+Business Media B.V.
About this chapter
Cite this chapter
Zhou, X., Platt, J.L. (2011). Molecular and Cellular Mechanisms of Mammalian Cell Fusion. In: Dittmar, T., Zänker, K.S. (eds) Cell Fusion in Health and Disease. Advances in Experimental Medicine and Biology, vol 713. Springer, Dordrecht. https://doi.org/10.1007/978-94-007-0763-4_4
Download citation
DOI: https://doi.org/10.1007/978-94-007-0763-4_4
Publisher Name: Springer, Dordrecht
Print ISBN: 978-94-007-0762-7
Online ISBN: 978-94-007-0763-4
eBook Packages: Biomedical and Life SciencesBiomedical and Life Sciences (R0)