Cell-cell fusion in the nervous system: Alternative mechanisms of development, injury, and repair

Seminars in Cell and Developmental Biology

Volumn 60, Issue , 2016, Pages 146-154

  Giordano Santini, Rosina ^a   Linton, Casey ^a   Hilliard, Massimo A ^a  

^a UNIVERSITY OF QUEENSLAND   (Australia)

Author keywords

Axonal regeneration; Cell cell fusion; Dendrite remodelling; Fusogen; Heterokaryon; Neuron theory

Indexed keywords

NANOTUBE;

AXON; CELL CELL FUSION; CELL FUSION; CELL REGENERATION; DENDRITE; GENE EXPRESSION; GLIA; GLIA CELL; HUMAN; NERVE FIBER REGENERATION; NERVE REGENERATION; NERVOUS SYSTEM DEVELOPMENT; NERVOUS SYSTEM INJURY; NEURAL STEM CELL; NEUROSCIENCE; NONHUMAN; REVIEW; ANIMAL; BIOLOGICAL MODEL; CHEMISTRY; CYTOLOGY; EMBRYOLOGY; METABOLISM; NERVE CELL; NERVOUS SYSTEM; PATHOLOGY;

ANIMALS; CELL FUSION; HUMANS; MODELS, BIOLOGICAL; NANOTUBES; NERVE REGENERATION; NERVOUS SYSTEM; NEURONS;

EID: 84996671088     PISSN: 10849521     EISSN: 10963634     Source Type: Journal    
DOI: 10.1016/j.semcdb.2016.06.019     Document Type: Review

References (96)

1. [1] Albeg, A., et al. C. elegans multi-dendritic sensory neurons: morphology and function. Mol. Cell. Neurosci. 46 (2011), 308–317.
2. [2] Salzberg, Y., et al. Skin-derived cues control arborization of sensory dendrites in Caenorhabditis elegans. Cell 155 (2013), 308–320.
3. [3] Smith, C.J., Watson, J.D., VanHoven, M.K., Colon-Ramos, D.A., Miller, D.M. 3rd, Netrin (UNC-6) mediates dendritic self-avoidance. Nat. Neurosci. 15 (2012), 731–737.
4. [4] Dong, X., Liu, O.W., Howell, A.S., Shen, K., An extracellular adhesion molecule complex patterns dendritic branching and morphogenesis. Cell 155 (2013), 296–307.
5. [5] Liu, O.W., Shen, K., The transmembrane LRR protein DMA-1 promotes dendrite branching and growth in C. elegans. Nat. Neurosci. 15 (2012), 7–63.
6. [6] Dong, X., Shen, K., Bulow, H.E., Intrinsic and extrinsic mechanisms of dendritic morphogenesis. Annu. Rev. Physiol. 77 (2015), 271–300.
7. [7] Oren-Suissa, M., Hall, D.H., Treinin, M., Shemer, G., Podbilewicz, B., The fusogen EFF-1 controls sculpting of mechanosensory dendrites. Science 328 (2010), 128–1288.
8. [8] Mohler, W.A., et al. The type I membrane protein EFF-1 is essential for developmental cell fusion. Dev. Cell 2 (2002), 355–362.
9. [9] Spooner, B.S., Luduena, M.A., Wessells, N.K., Membrane fusion in the growth cone-microspike region of embryonic nerve cells undergoing axon elongation in cell culture. Tissue Cell 6 (1974), 399–409.
10. [10] Sumida, G.M., Yamada, S., Self-contact elimination by membrane fusion. Proc. Natl. Acad. Sci. U. S. A. 110 (2013), 18958–18963.
11. [11] Lenard, A., et al. Endothelial cell self-fusion during vascular pruning. PLoS Biol., 13, 2015, e1002126.
12. [12] Hoy, R.R., Bittner, G.D., Kennedy, D., Regeneration in crustacean motoneurons: evidence for axonal fusion. Science 156 (1967), 251–252.
13. [13] Frank, E., Jansen, J.K., Rinvik, E., A multisomatic axon in the central nervous system of the leech. J. Comp. Neurol. 159 (1975), 1–13.
14. [14] Deriemer, S.A., Elliott, E.J., Macagno, E.R., Muller, K.J., Morphological evidence that regenerating axons can fuse with severed axon segments. Brain Res. 272 (1983), 157–161.
15. [15] Birse, S.C., Bittner, G.D., Regeneration of giant axons in earthworms. Brain Res. 113 (1976), 575–581.
16. [16] Bedi, S.S., Glanzman, D.L., Axonal rejoining inhibits injury-induced long-term changes in Aplysia sensory neurons in vitro. J. Neurosci. 21 (2001), 9667–9677.
17. [17] Ghosh-Roy, A., Wu, Z., Goncharov, A., Jin, Y., Chisholm, A.D., Calcium and cyclic AMP promote axonal regeneration in Caenorhabditis elegans and require DLK-1 kinase. J. Neurosci. 30 (2010), 3175–3183.
18. [18] Neumann, B., Nguyen, K.C., Hall, D.H., Ben-Yakar, A., Hilliard, M.A., Axonal regeneration proceeds through specific axonal fusion in transected C. elegans neurons. Dev. Dyn. 240 (2011), 1365–1372.
19. [19] Neumann, B., et al. EFF-1-mediated regenerative axonal fusion requires components of the apoptotic pathway. Nature 517 (2015), 219–222.
20. [20] van den Eijnde, S.M., et al. Transient expression of phosphatidylserine at cell-cell contact areas is required for myotube formation. J. Cell Sci. 114 (2001), 3631–3642.
21. [21] Hochreiter-Hufford, A.E., et al. Phosphatidylserine receptor BAI1 and apoptotic cells as new promoters of myoblast fusion. Nature 497 (2013), 263–267.
22. [22] Huppertz, B., Bartz, C., Kokozidou, M., Trophoblast fusion: fusogenic proteins, syncytins and ADAMs, and other prerequisites for syncytial fusion. Micron 37 (2006), 509–517.
23. [23] Helming, L., Gordon, S., Molecular mediators of macrophage fusion. Trends Cell Biol. 19 (2009), 514–522.
24. [24] Helming, L., Winter, J., Gordon, S., The scavenger receptor CD36 plays a role in cytokine-induced macrophage fusion. J. Cell Sci. 122 (2009), 453–459.
25. [25] Mercer, J., Helenius, A., Vaccinia virus uses macropinocytosis and apoptotic mimicry to enter host cells. Science 320 (2008), 531–535.
26. [26] Zaitseva, E., Yang, S.T., Melikov, K., Pourmal, S., Chernomordik, L.V., Dengue virus ensures its fusion in late endosomes using compartment-specific lipids. PLoS Pathog., 6, 2010, e1001131.
27. [27] Young, J.Z., Fused neurons and synaptic contacts in the giant nerve fibres of cephalopods. Philos. Trans. R. Soc. Lond. Series B Biol. Sci. 229 (1939), 465–503.
28. [28] Sotnikov, O.S., Malashko, V.V., Rybakova, G.I., Syncytial coupling of neurons in tissue culture and in early ontogenesis. Morfologiia 131 (2007), 7–15.
29. [29] Sotnikov, O.S., Rybakova, G.I., Solov'eva, I.A., The question of the fusion of neuron processes. Neurosci. Behav. Physiol. 38 (2008), 839–843.
30. [30] Sotnikov, O.S., Paramonova, N.M., Archakova, L.I., Ultrastructural analysis of interneuronal syncytial perforations. Cell Biol. Int. 34 (2010), 361–364.
31. [31] Gonzales Santander, R., Martinez Cuadrado, G., Toledo Lobo, M.V., Martinez Alonso, F.J., Communicating synapses: types and functional interpretation. Acta Anat. 142 (1991), 249–260.
32. [32] Gonzales Santander, R., Martinez Cuadrado, G., Rubio Saez, M., Exceptions to Cajal's neuron theory: communicating synapses. Acta Anat. 132 (1988), 74–76.
33. [33] Harris, H., Watkins, J.F., Ford, C.E., Schoefl, G.I., Artificial heterokaryons of animal cells from different species. J. Cell Sci. 1 (1966), 1–30.
34. [34] Jacobson, C.O., Reactivation of DNA synthesis in mammalian neuron nuclei after fusion with cells of an undifferentiated fibroblast line. Exp. Cell Res. 53 (1968), 316–318.
35. [35] Davis, F.M., Adelberg, E.A., Use of somatic cell hybrids for analysis of the differentiated state. Bacteriol. Rev. 37 (1973), 197–214.
36. [36] Dolivo, M., Beretta, E., Bonifas, V., Foroglou, C., Ultrastructure and function in sympathetic ganglia isolated from rats infected with pseudorabies virus. Brain Res. 140 (1978), 111–123.
37. [37] McCarthy, K.M., Tank, D.W., Enquist, L.W., Pseudorabies virus infection alters neuronal activity and connectivity in vitro. PLoS Pathog., 5, 2009, e1000640.
38. [38] Granstedt, A.E., Bosse, J.B., Thiberge, S.Y., Enquist, L.W., In vivo imaging of alphaherpesvirus infection reveals synchronized activity dependent on axonal sorting of viral proteins. Proc. Natl. Acad. Sci. U. S. A. 110 (2013), E3516–E3525.
39. [39] Reichelt, M., Zerboni, L., Arvin, A.M., Mechanisms of varicella-zoster virus neuropathogenesis in human dorsal root ganglia. J. Virol. 82 (2008), 3971–3983.
40. [40] Grigoryan, S., et al. Direct transfer of viral and cellular proteins from varicella-zoster virus-infected non-neuronal cells to human axons. PLoS One, 10, 2015, e0126081.
41. [41] Zerboni, L., et al. Herpes simplex virus 1 tropism for human sensory ganglion neurons in the severe combined immunodeficiency mouse model of neuropathogenesis. J. Virol. 87 (2013), 2791–2802.
42. [42] Ackman, J.B., Siddiqi, F., Walikonis, R.S., LoTurco, J.J., Fusion of microglia with pyramidal neurons after retroviral infection. J. Neurosci. 26 (2006), 11413–11422.
43. [43] Kramer, T., Enquist, L.W., Alphaherpesvirus infection disrupts mitochondrial transport in neurons. Cell Host Microbe 11 (2012), 504–514.
44. [44] Dempsher, J., Larrabee, M.G., Bang, F.B., Bodian, D., Physiological changes in sympathetic ganglia infected with pseudorabies virus. Am. J. Physiol. 182 (1955), 203–216.
45. [45] Kiraly, M., Dolivo, M., Alteration of the electrophysiological activity in sympathetic ganglia infected with a neurotropic virus I. Presynaptic origin of the spontaneous bioelectric activity. Brain Res. 240 (1982), 43–54.
46. [46] Hammarlund, M., Jorgensen, E.M., Bastiani, M.J., Axons break in animals lacking beta-spectrin. J. Cell Biol. 176 (2007), 269–275.
47. [47] Cusulin, C., et al. Embryonic stem cell-derived neural stem cells fuse with microglia and mature neurons. Stem Cells 30 (2012), 2657–2671.
48. [48] Procko, C., Lu, Y., Shaham, S., Glia delimit shape changes of sensory neuron receptive endings in C. elegans. Development 138 (2011), 1371–1381.
49. [49] Albert, P.S., Riddle, D.L., Developmental alterations in sensory neuroanatomy of the Caenorhabditis elegans dauer larva. J. Comp. Neurol. 219 (1983), 461–481.
50. [50] Ying, Q.L., Nichols, J., Evans, E.P., Smith, A.G., Changing potency by spontaneous fusion. Nature 416 (2002), 545–548.
51. [51] Alvarez-Dolado, M., et al. Fusion of bone-marrow-derived cells with Purkinje neurons, cardiomyocytes and hepatocytes. Nature 425 (2003), 968–973.
52. [52] Weimann, J.M., Charlton, C.A., Brazelton, T.R., Hackman, R.C., Blau, H.M., Contribution of transplanted bone marrow cells to Purkinje neurons in human adult brains. Proc. Natl. Acad. Sci. U. S. A. 100 (2003), 2088–2093.
53. [53] Weimann, J.M., Johansson, C.B., Trejo, A., Blau, H.M., Stable reprogrammed heterokaryons form spontaneously in Purkinje neurons after bone marrow transplant. Nat. Cell Biol. 5 (2003), 959–966.
54. [54] Kemp, K., et al. Fusion between human mesenchymal stem cells and rodent cerebellar Purkinje cells. Neuropathol. Appl. Neurobiol. 37 (2011), 166–178.
55. [55] Corti, S., et al. Wild-type bone marrow cells ameliorate the phenotype of SOD1-G93A ALS mice and contribute to CNS, heart and skeletal muscle tissues. Brain 127 (2004), 2518–2532.
56. [56] Johansson, C.B., et al. Extensive fusion of haematopoietic cells with Purkinje neurons in response to chronic inflammation. Nat. Cell Biol. 10 (2008), 575–583.
57. [57] Bae, J.S., et al. Bone marrow-derived mesenchymal stem cells promote neuronal networks with functional synaptic transmission after transplantation into mice with neurodegeneration. Stem Cells 25 (2007), 1307–1316.
58. [58] Kemp, K., Wilkins, A., Scolding, N., Cell fusion in the brain: two cells forward, one cell back. Acta Neuropathol. 128 (2014), 629–638.
59. [59] Kemp, K., Gray, E., Wilkins, A., Scolding, N., Purkinje cell fusion and binucleate heterokaryon formation in multiple sclerosis cerebellum. Brain 135 (2012), 2962–2972.
60. [60] Wiersema, A., Dijk, F., Dontje, B., van der Want, J.J., de Haan, G., Cerebellar heterokaryon formation increases with age and after irradiation. Stem Cell Res. 1 (2007), 150–154.
61. [61] Nygren, J.M., et al. Myeloid and lymphoid contribution to non-haematopoietic lineages through irradiation-induced heterotypic cell fusion. Nat. Cell Biol. 10 (2008), 584–592.
62. [62] Espejel, S., Romero, R., Alvarez-Buylla, A., Radiation damage increases Purkinje neuron heterokaryons in neonatal cerebellum. Ann. Neurol. 66 (2009), 100–109.
63. [63] Nern, C., et al. Fusion of hematopoietic cells with Purkinje neurons does not lead to stable heterokaryon formation under noninvasive conditions. J. Neurosci. 29 (2009), 3799–3807.
64. [64] Bae, J.S., et al. Neurodegeneration augments the ability of bone marrow-derived mesenchymal stem cells to fuse with Purkinje neurons in Niemann-Pick type C mice. Hum. Gene Ther. 16 (2005), 1006–1011.
65. [65] Magrassi, L., et al. Induction and survival of binucleated Purkinje neurons by selective damage and aging. J. Neurosci. 27 (2007), 9885–9892.
66. [66] Jones, J., et al. Mesenchymal stem cells rescue Purkinje cells and improve motor functions in a mouse model of cerebellar ataxia. Neurobiol. Dis. 40 (2010), 415–423.
67. [67] Gibson, A.J., et al. Dermal fibroblasts convert to a myogenic lineage in mdx mouse muscle. J. Cell Sci. 108:Pt. 1 (1995), 207–214.
68. [68] Vassilopoulos, G., Wang, P.R., Russell, D.W., Transplanted bone marrow regenerates liver by cell fusion. Nature 422 (2003), 901–904.
69. [69] Wang, X., et al. Cell fusion is the principal source of bone-marrow-derived hepatocytes. Nature 422 (2003), 897–901.
70. [70] Alvarez-Dolado, M., Martinez-Losa, M., Cell fusion and tissue regeneration. Adv. Exp. Med. Biol. 713 (2011), 161–175.
71. [71] Sankavaram, S.R., Svensson, M.A., Olsson, T., Brundin, L., Johansson, C.B., Cell fusion along the anterior-posterior neuroaxis in mice with experimental autoimmune encephalomyelitis. PLoS One, 10, 2015, e0133903.
72. [72] Sanges, D., et al. Wnt/beta-catenin signaling triggers neuron reprogramming and regeneration in the mouse retina. Cell Rep. 4 (2013), 271–286.
73. [73] Recio, J.S., et al. Bone marrow contributes simultaneously to different neural types in the central nervous system through different mechanisms of plasticity. Cell Transplant. 20 (2011), 1179–1192.
74. [74] Terashima, T., et al. The fusion of bone-marrow-derived proinsulin-expressing cells with nerve cells underlies diabetic neuropathy. Proc. Natl. Acad. Sci. U. S. A. 102 (2005), 12525–12530.
75. [75] Chen, K.A., et al. Cellular fusion for gene delivery to SCA1 affected Purkinje neurons. Mol. Cell. Neurosci. 47 (2011), 61–70.
76. [76] Diaz, D., Alonso, J.R., Weruaga, E., Bone marrow transplantation for research and regenerative therapies in the central nervous system. Methods Mol. Biol. 1254 (2015), 317–325.
77. [77] Rustom, A., Saffrich, R., Markovic, I., Walther, P., Gerdes, H.H., Nanotubular highways for intercellular organelle transport. Science 303 (2004), 1007–1010.
78. [78] Gerdes, H.H., Bukoreshtliev, N.V., Barroso, J.F., Tunneling nanotubes: a new route for the exchange of components between animal cells. FEBS Lett. 581 (2007), 2194–2201.
79. [79] Sowinski, S., et al. Membrane nanotubes physically connect T cells over long distances presenting a novel route for HIV-1 transmission. Nat. Cell Biol. 10 (2008), 211–219.
80. [80] Gousset, K., et al. Prions hijack tunnelling nanotubes for intercellular spread. Nat. Cell Biol. 11 (2009), 328–336.
81. [81] Wang, Y., Cui, J., Sun, X., Zhang, Y., Tunneling-nanotube development in astrocytes depends on p53 activation. Cell Death Differ. 18 (2011), 732–742.
82. [82] Sapir, A., et al. AFF-1, a FOS-1-regulated fusogen, mediates fusion of the anchor cell in C. elegans. Dev. Cell 12 (2007), 683–698.
83. [83] Mi, S., et al. Syncytin is a captive retroviral envelope protein involved in human placental morphogenesis. Nature 403 (2000), 785–789.
84. [84] Blond, J.L., et al. 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 (2000), 3321–3329.
85. [85] Blaise, S., de Parseval, N., Benit, L., Heidmann, T., Genomewide screening for fusogenic human endogenous retrovirus envelopes identifies syncytin 2, a gene conserved on primate evolution. Proc. Natl. Acad. Sci. U. S. A. 100 (2003), 13013–13018.
86. [86] Antony, J.M., et al. Human endogenous retrovirus glycoprotein-mediated induction of redox reactants causes oligodendrocyte death and demyelination. Nat. Neurosci. 7 (2004), 1088–1095.
87. [87] Mameli, G., et al. Epitopes of HERV-Wenv induce antigen-specific humoral immunity in multiple sclerosis patients. J. Neuroimmunol. 280 (2015), 66–68.
88. [88] Perron, H., et al. Molecular characteristics of Human Endogenous Retrovirus type-W in schizophrenia and bipolar disorder. Transl. Psychiatry, 2, 2012, e201.
89. [89] Perron, H., et al. Human endogenous retrovirus type W envelope expression in blood and brain cells provides new insights into multiple sclerosis disease. Mult. Scler. 18 (2012), 1721–1736.
90. [90] Leboyer, M., Tamouza, R., Charron, D., Faucard, R., Perron, H., Human endogenous retrovirus type W (HERV-W) in schizophrenia: a new avenue of research at the gene-environment interface. World J. Biol. Psychiatry 14 (2013), 80–90.
91. [91] Douville, R.N., Nath, A., Human endogenous retroviruses and the nervous system. Handb. Clin. Neurol. 123 (2014), 465–485.
92. [92] Dupressoir, A., et al. Syncytin-A and syncytin-B, two fusogenic placenta-specific murine envelope genes of retroviral origin conserved in Muridae. Proc. Natl. Acad. Sci. U. S. A. 102 (2005), 725–730.
93. [93] Gonzalez Santander, R., Martinez Cuadrado, G., Rubio Saez, M., Exceptions to Cajal's neuron theory: communicating synapses. Acta Anat. (Basel) 132 (1988), 74–76.
94. [94] Sotnikov, O.S., Rybakova, G.I., Solov'eva, I.A., The question of the fusion of neuron processes. Neurosci. Behav. Physiol. 38 (2008), 839–843.
95. [95] Paramonova, N.M., Sotnikov, O.S., Cytoplasmic syncytial connections between neuron bodies in the CNS of adult animals. Neurosci. Behav. Physiol. 40 (2010), 73–77.
96. [96] Archakova, L.I., Sotnikov, O.S., Novakovskaya, S.A., Solov'eva, I.A., Krasnova, T.V., Syncytial cytoplasmic anastomoses between neurites in caudal mesenteric ganglion cells in adult cats. Neurosci. Behav. Physiol. 40 (2010), 447–450.