Control of the collective migration of enteric neural crest cells by the Complement anaphylatoxin C3a and N-cadherin

Developmental Biology

Volumn 414, Issue 1, 2016, Pages 85-99

  Broders Bondon, Florence ^a,g   Paul Gilloteaux, Perrine ^b,h   Gazquez, Elodie ^a,c,d   Heysch, Julie ^a   Piel, Matthieu ^a   Mayor, Roberto ^e   Lambris, John D ^f   Dufour, Sylvie ^a,c,d  

^a INSTITUT CURIE   (France)

^b Cell and Tissue Imaging Facility   (France)

^c FACULTÉ DE MÉDECINE   (France)

^d INSERM U955   (France)

^e UNIVERSITY COLLEGE LONDON   (United Kingdom)

^f UNIVERSITY OF PENNSYLVANIA   (United States)

^g INSTITUT CURIE   (France)

^h L INSTITUT DU THORAX   (France)

Author keywords

Adhesion; Co attraction; Complement anaphylatoxin C3a; Enteric nervous system; Migration; N cadherin; Neural crest cells

Indexed keywords

COMPLEMENT COMPONENT C3 RECEPTOR; COMPLEMENT COMPONENT C3A; COMPLEMENT COMPONENT C3A RECEPTOR; FIBRONECTIN; NERVE CELL ADHESION MOLECULE; UNCLASSIFIED DRUG; BACTERIAL PROTEIN; C3A-DERIVED ANAPHYLATOXIN RECEPTOR, MOUSE; CADHERIN; CDH2 PROTEIN, MOUSE; G PROTEIN COUPLED RECEPTOR; PHOTOPROTEIN; YELLOW FLUORESCENT PROTEIN, BACTERIA;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CELL ADHESION; CELL MIGRATION; CONFOCAL MICROSCOPY; CONTROLLED STUDY; DISPERSION; EMBRYO; EMBRYO DEVELOPMENT; EX VIVO STUDY; FEMALE; FOCAL ADHESION; INHIBITION KINETICS; MALE; MOLECULAR MODEL; MOUSE; N CADHERIN GENE; NERVE CELL NETWORK; NEURAL CREST CELL; NONHUMAN; PHARMACOLOGICAL BLOCKING; PRIORITY JOURNAL; PROTEIN LOCALIZATION; SURFACE PROPERTY; TRANSGENIC MOUSE; TRIANGULATION; VIDEO MICROSCOPY; AGONISTS; AMINO ACID SEQUENCE; ANIMAL; ANTAGONISTS AND INHIBITORS; CELL MOTION; CROSS BREEDING; CYTOLOGY; DEFICIENCY; EMBRYOLOGY; EXTRACELLULAR MATRIX; FLUORESCENCE MICROSCOPY; GENE EXPRESSION REGULATION; GENETICS; INTESTINE INNERVATION; NEURAL CREST; PHYSIOLOGY; REPORTER GENE; TIME LAPSE IMAGING;

AMINO ACID SEQUENCE; ANIMALS; BACTERIAL PROTEINS; CADHERINS; CELL ADHESION; CELL MOVEMENT; COMPLEMENT C3A; CROSSES, GENETIC; ENTERIC NERVOUS SYSTEM; EXTRACELLULAR MATRIX; FEMALE; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GENES, REPORTER; LUMINESCENT PROTEINS; MALE; MICE; MICROSCOPY, FLUORESCENCE; MICROSCOPY, VIDEO; NEURAL CREST; RECEPTORS, G-PROTEIN-COUPLED; TIME-LAPSE IMAGING;

EID: 84964318813     PISSN: 00121606     EISSN: 1095564X     Source Type: Journal    
DOI: 10.1016/j.ydbio.2016.03.022     Document Type: Article

References (55)

1. Abercrombie M., Heaysman J.E. Observations on the social behaviour of cells in tissue culture. I. Speed of movement of chick heart fibroblasts in relation to their mutual contacts. Exp. Cell Res. 1953, 5(1):111-131.
2. Abercrombie M., Heaysman J.E. Observations on the social behaviour of cells in tissue culture. II. Monolayering of fibroblasts. Exp. Cell Res. 1954, 6(2):293-306.
3. Ames R.S., et al. Identification of a selective nonpeptide antagonist of the anaphylatoxin C3a receptor that demonstrates antiinflammatory activity in animal models. J. Immunol. 2001, 166(10):6341-6348.
4. Anderson R.B., et al. The cell adhesion molecule L1 Is required for chain migration of neural crest cells in the developing mouse gut. Gastroenterology 2006, 130(4):1221-1232.
5. Azioune A., et al. Simple and rapid process for single cell micro-patterning. Lab Chip 2009, 9(11):1640-1642.
6. Barlow A., de Graaff E., Pachnis V. Enteric nervous system progenitors are coordinately controlled by the G protein-coupled receptor EDNRB and the receptor tyrosine kinase RET. Neuron 2003, 40(5):905-916.
7. Breau M.A., et al. Lack of beta1 integrins in enteric neural crest cells leads to a Hirschsprung-like phenotype. Development 2006, 133(9):1725-1734.
8. Breau M.A., et al. Beta1 integrins are required for the invasion of the caecum and proximal hindgut by enteric neural crest cells. Development 2009, 136(16):2791-2801.
9. Breau M.A., Dufour S. Biological development of the enteric nervous system. Hirschsprung's Disease: Diagnosis and Treatment. Congenital Disorders - Laboratory and Clinical Research Series 2009, 15-44. Nova, New York. R.N. Núñez, M. López-Alonso (Eds.).
10. Broders-Bondon F., et al. N-cadherin and beta1-integrins cooperate during the development of the enteric nervous system. Dev. Biol. 2012, 364(2):178-191.
11. Carmona-Fontaine C., et al. Contact inhibition of locomotion in vivo controls neural crest directional migration. Nature 2008, 456(7224):957-961.
12. Carmona-Fontaine C., et al. Complement fragment C3a controls mutual cell attraction during collective cell migration. Dev. Cell 2011, 21(6):1026-1037.
13. Desai R.A., et al. Contact inhibition of locomotion probabilities drive solitary versus collective cell migration. J. R. Soc. Interface 2013, 10(88). 20130717.
14. DiScipio R.G., et al. Complement C3a signaling mediates production of angiogenic factors in mesenchymal stem cells. J. Biomed. Sci. Eng. 2013, 06(08):1-13.
15. Doyle A.D., et al. One-dimensional topography underlies three-dimensional fibrillar cell migration. J. Cell Biol. 2009, 184(4):481-490.
16. Druckenbrod N.R., Epstein M.L. The pattern of neural crest advance in the cecum and colon. Dev. Biol. 2005, 287(1):125-133.
17. Druckenbrod N.R., Epstein M.L. Behavior of enteric neural crest-derived cells varies with respect to the migratory wavefront. Dev. Dyn. 2007, 236(1):84-92.
18. Gaidar Y.A., et al. Distribution of N-cadherin and NCAM in neurons and endocrine cells of the human embryonic and fetal gastroenteropancreatic system. Acta Histochem. 1998, 100(1):83-97.
19. Goto A., et al. GDNF and endothelin 3 regulate migration of enteric neural crest-derived cells via protein kinase A and Rac1. J. Neurosci. 2013, 33(11):4901-4912.
20. Hao M.M., Young H.M. Development of enteric neuron diversity. J. Cell. Mol. Med. 2009, 13(7):1193-1210.
21. Hearn C.J., Murphy M., Newgreen D. GDNF and ET-3 differentially modulate the numbers of avian enteric neural crest cells and enteric neurons in vitro. Dev. Biol. 1998, 197(1):93-105.
22. Hoeprich P.D., Hugli T.E. Helical conformation at the carboxy-terminal portion of human C3a is required for full activity. Biochemistry 1986, 25(8):1945-1950.
23. Hotta R., et al. Effects of tissue age, presence of neurones and endothelin-3 on the ability of enteric neurone precursors to colonize recipient gut: implications for cell-based therapies. Neurogastroenterol. Motil. 2010, 22(3). 331-e86.
24. Kulesa P.M., McLennan R. Neural crest migration: trailblazing ahead. F1000prime Rep. 2015, 7:02.
25. Lake J.I., Heuckeroth R.O. Enteric nervous system development: migration, differentiation, and disease. Am. J. Physiol. Gastrointest. Liver Physiol. 2013, 305(1):G1-24.
26. Landman K.A., et al. Building stable chains with motile agents: Insights into the morphology of enteric neural crest cell migration. J. Theor. Biol. 2011, 276(1):250-268.
27. Lautenschlager F., Piel M. Microfabricated devices for cell biology: all for one and one for all. Curr. Opin. Cell Biol. 2013, 25(1):116-124.
28. Leibl M.A., et al. Expression of endothelin 3 by mesenchymal cells of embryonic mouse caecum. Gut 1999, 44(2):246-252.
29. Leslie J.D., Mayor R. Complement in animal development: unexpected roles of a highly conserved pathway. Semin. Immunol. 2013, 25(1):39-46.
30. Mastellos D., et al. Novel monoclonal antibodies against mouse C3 interfering with complement activation: description of fine specificity and applications to various immunoassays. Mol. Immunol. 2004, 40(16):1213-1221.
31. McKeown S.J., Wallace A.S., Anderson R.B. Expression and function of cell adhesion molecules during neural crest migration. Dev. Biol. 2013, 373(2):244-257.
32. Nagy N., Goldstein A.M. Endothelin-3 regulates neural crest cell proliferation and differentiation in the hindgut enteric nervous system. Dev. Biol. 2006, 293(1):203-217.
33. Natarajan D., et al. Requirement of signalling by receptor tyrosine kinase RET for the directed migration of enteric nervous system progenitor cells during mammalian embryogenesis. Development 2002, 129(22):5151-5160.
34. Newgreen D.F., et al. Simple rules for a "simple" nervous system? Molecular and biomathematical approaches to enteric nervous system formation and malformation. Dev. Biol. 2013, 382(1):305-319.
35. Nishiyama C., et al. Trans-mesenteric neural crest cells are the principal source of the colonic enteric nervous system. Nat. Neurosci. 2012, 15(9):1211-1218.
36. Pietri T., et al. The human tissue plasminogen activator-Cre mouse: a new tool for targeting specifically neural crest cells and their derivatives in vivo. Dev. Biol. 2003, 259(1):176-187.
37. Pietri T., et al. Conditional beta1-integrin gene deletion in neural crest cells causes severe developmental alterations of the peripheral nervous system. Development 2004, 131(16):3871-3883.
38. Ricklin D., Lambris J.D. Complement in immune and inflammatory disorders: therapeutic interventions. J. Immunol. 2013, 190(8):3839-3847.
39. Scarpa E., et al. A novel method to study contact inhibition of locomotion using micropatterned substrates. Biol. Open 2013, 2(9):901-906.
40. Shinjyo N., et al. Complement-derived anaphylatoxin C3a regulates in vitro differentiation and migration of neural progenitor cells. Stem Cells 2009, 27(11):2824-2832.
41. Simpson M.J., et al. Cell proliferation drives neural crest cell invasion of the intestine. Dev. Biol. 2007, 302(2):553-568.
42. Stanchina L., et al. Interactions between Sox10, Edn3 and Ednrb during enteric nervous system and melanocyte development. Dev. Biol. 2006, 295(1):232-249.
43. Tang Z., et al. C3a mediates epithelial-to-mesenchymal transition in proteinuric nephropathy. J. Am. Soc. Nephrol. 2009, 20(3):593-603.
44. Thery M., et al. Anisotropy of cell adhesive microenvironment governs cell internal organization and orientation of polarity. Proc. Natl. Acad. Sci. USA 2006, 103(52):19771-19776.
45. Thery M., Bornens M. Cell shape and cell division. Curr. Opin. Cell Biol. 2006, 18(6):648-657.
46. Thery M., Piel M. Adhesive micropatterns for cells: a microcontact printing protocol. Cold Spring Harb. Protoc. 2009, (7). pdb prot5255.
47. Theveneau E., et al. Collective chemotaxis requires contact-dependent cell polarity. Dev. Cell 2010, 19(1):39-53.
48. Theveneau E., Mayor R. Can mesenchymal cells undergo collective cell migration? The case of the neural crest. Cell Adhes. Migr. 2011, 5(6):490-498.
49. Watanabe Y., et al. Sox10 and Itgb1 interaction in enteric neural crest cell migration. Dev. Biol. 2013, 379(1):92-106.
50. Woods M.L., et al. Directional collective cell migration emerges as a property of cell interactions. PLoS One 2014, 9(9). e104969.
51. Wynn M.L., et al. Follow-the-leader cell migration requires biased cell-cell contact and local microenvironmental signals. Phys. Biol. 2013, 10(3):035003.
52. Xu Q., Heanue T., Pachnis V. Travelling within the fetal gut: simple rules for an arduous journey. BMC Biol. 2014, 12:50.
53. Young H.M., et al. GDNF is a chemoattractant for enteric neural cells. Dev. Biol. 2001, 229(2):503-516.
54. Young H.M., et al. Dynamics of neural crest-derived cell migration in the embryonic mouse gut. Dev. Biol. 2004, 270(2):455-473.
55. Young H.M., et al. Colonizing while migrating: how do individual enteric neural crest cells behave?. BMC Biol. 2014, 12:23.