Neurovascular congruence results from a shared patterning mechanism that utilizes Semaphorin3A and Neuropilin-1

Developmental Biology

Volumn 255, Issue 1, 2003, Pages 77-98

  Bates, Damien ^a,b   Taylor, G Ian ^b   Minichiello, Joe ^a   Farlie, Peter ^a   Cichowitz, Adam ^a,b   Watson, Nadine ^c   Klagsbrun, Michael ^d   Mamluk, Roni ^d   Newgreen, Donald F ^a  

^a ROYAL CHILDREN'S HOSPITAL   (Australia)

^b ROYAL MELBOURNE HOSPITAL   (Australia)

^c UNIVERSITY OF MELBOURNE   (Australia)

^d BOSTON CHILDREN S HOSPITAL   (United States)

Author keywords

Blood vessels; Endothelium; Flt 1; Forelimb; Nerves; Neuropilin 1; Neurovascular; Pattern formation; Quail; Semaphorin3A; Smooth muscle; VEGF

Indexed keywords

ACTIN; NEUROPILIN 1; PROTEIN; SEMAPHORIN 3A; VASCULOTROPIN;

AGENESIS; ANIMAL TISSUE; ARTICLE; BASEMENT MEMBRANE; BLEEDING; BLOOD VESSEL; CAPILLARY; CONGENITAL BLOOD VESSEL MALFORMATION; CONTROLLED STUDY; ELECTROPORATION; EMBRYO; ENDOTHELIUM; ENDOTHELIUM CELL; FASCICULATION; FORELIMB; HYPOTHESIS; IMMUNOREACTIVITY; NEGATIVE FEEDBACK; NEOVASCULARIZATION (PATHOLOGY); NERVE; NERVE CELL; NEURAL TUBE; NONHUMAN; ORGANOGENESIS; PERIPHERAL NERVE; PRIORITY JOURNAL; QUAIL; TRANSMISSION ELECTRON MICROSCOPY; VASCULAR SMOOTH MUSCLE;

LAMIINAE; PHASIANIDAE;

EID: 0037333506     PISSN: 00121606     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0012-1606(02)00045-3     Document Type: Article

References (101)

1. Bagnard D., Vaillant C., Khuth S.T., Dufay N., Lohrum M., Puschel A.W., Belin M.F., Bolz J., Thomasset N. Semaphorin 3A-vascular endothelial growth factor-165 balance mediates migration and apoptosis of neural progenitor cells by the recruitment of shared receptor. J. Neurosci. 21:2001;3332-3341.
2. Bates D., Taylor G., Newgreen D. The pattern of neurovascular development in the forelimb of the quail embryo. Dev. Biol. 249:2002;300-320.
3. Behar O., Golden J., Mashimo H., Schoen F., Fishman M. Semaphorin III is needed for normal patterning and growth of nerves, bones and heart. Nature. 383:1996;525-528.
4. Bennett M.R., Davey D.F., Uebel K.E. The growth of segmental nerves from the brachial myotomes into the proximal muscles of the chick forelimb during development. J. Comp. Neurol. 189:1980;335-357.
5. Borisov A.B., Huang S.K., Carlson B.M. Remodeling of the vascular bed and progressive loss of capillaries in denervated skeletal muscle. Anat. Rec. 258:2000;292-304.
6. Brand-Saberi B., Seifert R., Grim M., Wilting J., Kuhlewein M., Christ B. Blood vessel formation in the avian limb bud involves angioblastic and angiotrophic growth. Dev. Dyn. 202:1995;181-194.
7. Caplan A. The vasculature and limb development. Cell Differ. 16:1985;1-11.
8. Caplan A., Koutroupas S. The control of muscle and cartilage development in the chick limb the role of differential vascularization . J. Embryol. Exp. Morphol. 29:1973;571-583.
9. Chen H., Ikeda U., Shimpo M., Maeda Y., Shibuya M., Ozawa K., Shimada K. Inhibition of vascular endothelial growth factor activity by transfection with the soluble FLT-1 gene. J. Cardiovasc. Pharmacol. 36:2000;498-502.
10. Coleman S., Anson B. Arterial patterns in the hand based upon a series of 650 specimens. Surg. Gynecol. Obstet. 113:1961;409-424.
11. DeRuiter M., Poelmann R., VanMunsteren J., Mironov V., Markwald R., Gittenberger-de-Groot A. Embryonic endothelial cells transdifferentiate into mesenchymal cells expressing smooth muscle actins in vivo and in vitro. Circ. Res. 80:1997;444-451.
12. Drake C.J., LaRue A., Ferrara N., Little C.D. VEGF regulates cell behavior during vasculogenesis. Dev. Biol. 224:2000;178-188.
13. Drake C., Little C. Exogenous vascular endothelial growth factor induces malformed and hyperfused vessels during embryonic neovascularization. Proc. Natl. Acad. Sci. USA. 92:1995;7657-7661.
14. Drake C.J., Little C.D. VEGF and vascular fusion implications for normal and pathological vessels . J. Histochem. Cytochem. 47:1999;1351-1356.
15. Drushel R., Pechak D., Caplan A. The anatomy, ultrastructure and fluid dynamics of the developing vasculature of the embryonic chick wing bud. Cell Differ. 16:1985;13-28.
16. Eickholt B., Mackenzie S., Graham A., Walsh F., Doherty P. Evidence for collapsin-1 functioning in the control of neural crest migration in both trunk and hindbrain regions. Development. 126:1999;2181-2189.
17. Enomoto H., Crawford P.A., Gorodinsky A., Heuckeroth R.O., Johnson E.M. Jr., Milbrandt J. RET signaling is essential for migration, axonal growth and axon guidance of developing sympathetic neurons. Development. 128:2001;3963-3974.
18. Fan J., Raper J. Localized collapsing cues can steer growth cones without inducing their full collapse. Neuron. 14:1995;263-274.
19. Feig S., Guillery R. Corticothalamic axons contact blood vessels as well as nerve cells in the thalamus. Eur. J. Neurosci. 12:2000;2195-2198.
20. Feinberg R.N., Latker C.H., Beebe D.C. Localised vascular regression during limb morphogenesis in the chicken embryo. I. Spatial and temporal changes in vascular pattern. Anat. Rec. 214:1986;405-409.
21. Flamme I., Vonreuten M., Drexler H., Syedali S., Risau W. Overexpression of vascular endothelial growth factor in the avian embryo induces hypervascularization and increased vascular permeability without alterations of embryonic pattern formation. Dev. Biol. 171:1995;399-414.
22. Fujisawa H., Kitsukawa T., Kawakami A., Takagi S., Shimizu M., Hirata T. Roles of a neuronal cell-surface molecule, neuropilin, in nerve fiber fasciculation and guidance. Cell Tissue Res. 290:1997;465-470.
23. Gagliardini V., Fankhauser C. Semaphorin III can induce death in sensory neurons. Mol. Cell. Neurosci. 14:1999;301-316.
24. Gagnon M.L., Bielenberg D.R., Gechtman Z., Miao H.Q., Takashima S., Soker S., Klagsbrun M. Identification of a natural soluble neuropilin-1 that binds vascular endothelial growth factor in vivo expression and antitumor activity . Proc. Natl. Acad. Sci. USA. 97:2000;2573-2578.
25. Giger R.J., Wolfer D.P., DeWit G.M.J., Verhaagen J. Anatomy of rat semaphorin III collapsin-1 mRNA expression and relationship to developing nerve tracts during neuroembryogenesis. J. Comp. Neurol. 375:1996;378-392.
26. Gu X.H., Terenghi G., Kangesu T., Navsaria H.A., Springall D.R., Leigh I.M., Green C.J., Polak J.M. Regeneration pattern of blood vessels and nerves in cultured keratinocyte grafts assessed by confocal laser scanning microscopy. Br. J. Dermatol. 132:1995;376-383.
27. Gupta K., Kshirsagar S., Li W., Gui L., Ramakrishnan S., Gupta P., Law P., Hebbel R. VEGF prevents apoptosis of human microvascular endothelial cells via opposing effects on MAPK/ERK and SAPK/JNK signaling. Exp. Cell Res. 247:1999;495-504.
28. Hallmann R., Feinberg R., Latker C., Sasse J., Rissau W. Regression of blood vessels precedes cartilage differentiation during chick limb development. Differentiation. 34:1987;98-105.
29. Hamburger V., Hamilton H. A series of normal stages in the development of the chick embryo. J. Morphol. 88:1951;49-92.
30. Herzog Y., Kalcheim C., Kahane N., Reshef R., Neufeld G. Differential expression of neuropilin-1 and neuropilin-2 in arteries and veins. Mech. Dev. 109:2001;115-119.
31. Hobson M.I., Brown R., Green C.J., Terenghi G. Inter-relationships between angiogenesis and nerve regeneration a histochemical study . Br. J. Plast. Surg. 50:1997;125-131.
32. Hollyday M. Specificity of initial axonal projections to embryonic chick wing. J. Comp. Neurol. 302:1990;589-602.
33. Honma Y., Araki T., Gianino S., Bruce A., Heuckeroth R., Johnson E., Milbrandt J. Artemin is a vascular-derived neurotropic factor for developing sympathetic neurons. Neuron. 35:2002;267-282.
34. Inoue T., Krumlauf R. An impulse to the brain-using in vivo electroporation. Nat. Neurosci. 4:2001;1156-1158.
35. Itasaki N., Bel-Vialar S., Krumlauf R. 'Shocking' developments in chick embryology electroporation and in ovo gene expression . Nat. Cell Biol. 1:1999;E203-E207.
36. Jin K.L., Mao X.O., Greenberg D.A. Vascular endothelial growth factor direct neuroprotective effect in in vitro ischemia . Proc. Natl. Acad. Sci. USA. 97:2000;10242-10247.
37. Kawakami A., Kitsukawa T., Takagi S., Fujisawa H. Developmentally regulated expression of a cell surface protein, neuropilin, in the mouse nervous system. J. Neurobiol. 29:1996;1-17.
38. Kawasaki T., Kitsukawa T., Bekku Y., Matsuda Y., Sanbo M., Yagi T., Fujisawa H. A requirement for neuropilin-1 in embryonic vessel formation. Development. 126:1999;4895-4902.
39. Kendall R., Thomas K. Inhibition of vascular endothelial growth factor activity by endogenously encoded soluble receptor. Proc. Natl. Acad. Sci. USA. 90:1993;10705-10709.
40. Kitsukawa T., Shimizu M., Sanbo M., Hirata T., Taniguchi M., Bekku Y., Yagi T., Fujisawa H. Neuropilin-semaphorin III/D-mediated chemorepulsive signals play a crucial role in peripheral nerve projection in mice. Neuron. 19:1997;995-1005.
41. Kitsukawa T., Shimono A., Kawakami A., Kondoh H., Fujisawa H. Overexpression of a membrane protein, neuropilin, in chimeric mice causes abnormalities in the cardiovascular system, nervous system and limbs. Development. 121:1995;4309-4318.
42. Koch M., Murrell J.R., Hunter D.D., Olson P.F., Jin W., Keene D.R., Brunken W.J., Burgeson R.E. A novel member of the netrin family, beta-netrin, shares homology with the beta chain of laminin. Identification, expression, and functional characterization. J. Cell. Biol. 151:2000;221-234.
43. Labastie M.C. MB1, a quail leukocyte-endothelium antigen further characterization of soluble and cell-associated forms . Cell Differ. Dev. 27:1989;151-162.
44. Lengele B., Dhem A. Unusual variations of the vasculonervous elements of the human axilla. Report of three cases. Arch. Anat. Histol. Embryol. 72:1989;57-67.
45. Lewis W. The development of the arm in man. Am. J. Anat. 1:1902;145-185.
46. Lucas, A., Stettenheim, P., 1972. Avian anatomy: integument, in: Handbook No. 362, United States Department of Agriculture, Washington D.C.
47. Luo Y.L., Raible D., Raper J.A. Collapsin a protein in brain that induces the collapse and paralysis of neuronal growth cones . Cell. 75:1993;217-227.
48. Mackinnon S., Dellon A. Surgery of the Peripheral Nerve. 1988;Thieme Medical Publishers, Inc, New York.
49. Martin P., Khan A., Lewis J. Cutaneous nerves of the embryonic chick wing do not develop in regions denuded of ectoderm. Development. 106:1989;335-346.
50. Martin P., Lewis J. Origins of the neurovascular bundle interactions between developing nerves and blood vessels in embryonic chick skin . Int. J. Dev. Biol. 33:1989;379-387.
51. Messersmith E., Leonardo E., Schatz C., Tessier-Lavigne M., Goodman C., Kolodkin A. Semaphorin III can function as a selective chemorepellent to pattern sensory projections in the spinal cord. Neuron. 14:1995;949-959.
52. Miao H.Q., Soker S., Feiner L., Alonso J.L., Raper J.A., Klagsbrun M. Neuropilin-1 mediates collapsin-1/semaphorin III inhibition of endothelial cell motility functional competition of collapsin-1 and vascular endothelial growth factor-165 . J. Cell. Biol. 146:1999;233-241.
53. Miller R. Observations upon the arrangement of the axillary artery and brachial plexus. Am. J. Anat. 64:1939;143-163.
54. Morales-Ruiz M., Fulton D., Sowa G., Languino L.R., Fujio Y., Walsh K., Sessa W.C. Vascular endothelial growth factor-stimulated actin reorganization and migration of endothelial cells is regulated via the serine/threonine kinase Akt. Circ. Res. 86:2000;892-896.
55. Mukouyama Y., Shin D., Britsch S., Taniguchi M., Anderson D. Sensory nerves determine the pattern of arterial differentiation and blood vessel branching in the skin. Cell. 109:2002;693-705.
56. Newgreen D.F., Minichiello J. Control of epitheliomesenchymal transformation. I. Events in the onset of neural crest cell migration are separable and inducible by protein kinase inhibitors. Dev. Biol. 170:1995;91-101.
57. Noakes P., Bennett M., Stratford J. Migration of Schwann cells and axons into developing chick forelimb muscles following removal of either the neural tube or the neural Crest. J. Comp. Neurol. 277:1988;214-233.
58. Ogunshola O.O., Stewart W.B., Mihalcik V., Solli T., Madri J.A., Ment L.R. Neuronal VEGF expression correlates with angiogenesis in postnatal developing rat brain. Brain Res. Dev. Brain Res. 119:2000;139-153.
59. Oosthuyse B., Moons L., Storkebaum E., Beck H., Nuyens D., Brusselmans K., Van Dorpe J., Hellings P., Gorselink M., Heymans S., Theilmeier G., Dewerchin M., Laudenbach V., Vermylen P., Raat H., Acker T., Vleminckx V., Van Den Bosch L., Cashman N., Fujisawa H., Drost M.R., Sciot R., Bruyninckx F., Hicklin D.J., Ince C., Gressens P., Lupu F., Plate K.H., Robberecht W., Herbert J.M., Collen D., Carmeliet P. Deletion of the hypoxia-response element in the vascular endothelial growth factor promoter causes motor neuron degeneration. Nat. Genet. 28:2001;131-138.
60. Pardanaud L., Altmann C., Kitos P., Dieterlen-Lievre F., Buck C. Vasculogenesis in the early quail blastodisc as studied with a monoclonal antibody recognizing endothelial cells. Development. 100:1987;339-349.
61. Pasterkamp R.J., Verhaagen J. Emerging roles for semaphorins in neural regeneration. Brain Res. Brain Res. Rev. 35:2001;36-54.
62. Peault B., Thiery J., Douarin N.L. Surface marker for hemopoietic and endothelial cell lineages in quail that is defined by a monoclonal antibody. Proc. Natl. Acad. Sci. USA. 80:1983;2976-2980.
63. Puschel A., Adams R., Betz H. Murine semaphorin D/collapsin is a member of a diverse gene family and creates domains inhibitory for axonal extension. Neuron. 14:1995;941-948.
64. Rohm B., Ottemeyer A., Lohrum M., Pueschel Andreas W. Plexin/neuropilin complexes mediate repulsion by the axonal guidance signal semaphorin 3A. Mech. Dev. 93:2000;95-104.
65. Rossignol M., Gagnon M.L., Klagsbrun M. Genomic organization of human neuropilin-1 and neuropilin-2 genes identification and distribution of splice variants and soluble isoforms . Genomics. 70:2000;211-222.
66. Roush W. Receptor links blood vessels, axons. Science. 279:1998;2042.
67. Schratzberger P., Schratzberger G., Silver M., Curry C., Kearney M., Magner M., Alroy J., Adelman L.S., Weinberg D.H., Ropper A.H., Isner J.M. Favorable effect of VEGF gene transfer on ischemic peripheral neuropathy. Nat. Med. 6:2000;405-413.
68. Schratzberger P., Walter D.H., Rittig K., Bahlmann F.H., Pola R., Curry C., Silver M., Krainin J.G., Weinberg D.H., Ropper A.H., Isner J.M. Reversal of experimental diabetic neuropathy by VEGF gene transfer. J. Clin. Invest. 107:2001;1083-1092.
69. Shima D.T., Mailhos C. Vascular developmental biology getting nervous . Curr. Opin. Genet. Dev. 10:2000;536-542.
70. Singer E. Embryological patterns persisting in the arteries of the arm. Anat. Rec. 55:1933;403-409.
71. Singer E. Human brachial plexus united into a single cord. Description and interpretation. Anat. Rec. 55:1933;411-419.
72. Soker S. Neuropilin in the midst of cell migration and retraction. Int. J. Biochem. Cell Biol. 33:2001;433-437.
73. Soker S., Takashima S., Miao H., Neufeld G., Klagsbrun M. Neuropilin-1 is expressed by endothelial and tumor cells as an isoform-specific receptor for vascular endothelial growth factor. Cell. 92:1998;735-745.
74. Sondell M., Lundborg G., Kanje M. Vascular endothelial growth factor has neurotrophic activity and stimulates axonal outgrowth, enhancing cell survival and Schwann cell proliferation in the peripheral nervous system. J. Neurosci. 19:1999;5731-5740.
75. Sondell M., Lundborg G., Kanje M. Vascular endothelial growth factor stimulates Schwann cell invasion and neovascularization of acellular nerve grafts. Brain Res. 846:1999;219-228.
76. Sondell M., Sundler F., Kanje M. Vascular endothelial growth factor is a neurotrophic factor which stimulates axonal outgrowth through the flk-1 receptor. Eur. J. Neurosci. 12:2000;4243-4254.
77. Spence S., Poole T. Developing blood vessels and associated extracellular matrix as substrates for neural crest migration in Japanese quail, Coturnic coturnix japonica. Int. J. Dev. Biol. 38:1994;85-98.
78. Sunderland S. Blood supply of the nerves of the upper limb in man. Arch. Neurol. Psych. 53:1945;91.
79. Suri C., McClain J., Thurston G., McDonald D., Zhou H., Oldmixon E., Sato T., Yancopoulos G. Increased vascularization in mice overexpressing Angiopoietin-1. Science. 282:1998;468-471.
80. Swanson G., Lewis J. The timetable of innervation and its control in the chick wing bud. J. Embryol. Exp. Morphol. 71:1982;121-137.
81. Swartz M., Eberhart J., Mastick G.S., Krull C.E. Sparking new frontiers using in vivo electroporation for genetic manipulations . Dev. Biol. 233:2001;13-21.
82. Takagi S., Tsuj T., Amagai T., Takamatsu T., Fujisawa H. Specific cell surface labels in the visual centers of Xenopus laevis tadpole identified using monoclonal antibodies. Dev. Biol. 122:1987;90-100.
83. Takahashi Y., Imanaka T., Takano T. Spatial and temporal pattern of smooth muscle cell differentiation during development of the vascular system in the mouse embryo. Anat. Embryol. (Berl.). 194:1996;515-526.
84. Takashima S., Kitakaze M., Asakura M., Asanuma H., Sanada S., Tashiro F., Niwa H., Miyazaki Ji J., Hirota S., Kitamura Y., Kitsukawa T., Fujisawa H., Klagsbrun M., Hori M. Targeting of both mouse neuropilin-1 and neuropilin-2 genes severely impairs developmental yolk sac and embryonic angiogenesis. Proc. Natl. Acad. Sci. USA. 99:2002;3657-3662.
85. Taniguchi M., Yuasa S., Fujisawa H., Naruse I., Saga S., Mishina M., Yagi T. Disruption of semaphorinIII/D gene causes severe abnormality in peripheral nerve projection. Neuron. 19:1997;519-530.
86. Taylor G., Gianoutsos M., Morris S. The neurovascular territories of the skin and muscles anatomic study and clinical implications . Plastic Reconstructive Surg. 94:1994;1-36.
87. Taylor G., Minabe T. The Angiosomes of the mammals and other vertebrates. Plast. Reconstr. Surg. 89:1992;181-215.
88. Teillet M.A., Le Douarin N.M. Consequences of neural tube and notochord excision on the development of the peripheral nervous system in the chick embryo. Dev. Biol. 98:1983;192-211.
89. Tosney K.W., Landmesser L.T. Development of the major pathways for neurite outgrowth in the chick hindlimb. Dev. Biol. 109:1985;193-214.
90. Upton J., Coombs C.J., Mulliken J.B., Burrows P.E., Pap S. Vascular malformations of the upper limb a review of 270 patients . J. Hand Surg. [Am]. 24A:1999;1019-1035.
91. Vargesson N., Laufer E. Smad7 misexpression during embryonic angiogenesis causes vascular dilation and malformations independently of vascular smooth muscle cell function. Dev. Biol. 240:2001;499-516.
92. Weddell G. Axonal regeneration in cutaneous nerve plexuses. J. Anat. 77:1942;49-62.
93. Wheater P., Burkitt H., Stevens A., Lowe J. Basic Histopathology: A Color Atlas and Text. 1985;Churchill Livingstone, New York.
94. Whitaker G.B., Limberg B.J., Rosenbaum J.S. Vascular endothelial growth factor receptor- 2 and neuropilin-1 form a receptor complex that is responsible for the differential signaling potency of vegf165 and vegf121. J. Biol. Chem. 276:2001;25520-25531.
95. Wilson D. Development of avascularity during cartilage differentiation in the embryonic limb. Differentiation. 30:1986;183-187.
96. Wilting J., Birkenhager R., Eichmann A., Kurz H., Martiny-Baron G., Marme D., McCarthy J., Christ B., Weich H. VEGF(121) induces proliferation of vascular endothelial cells and expression of flk-1 without affecting lymphatic vessels of the chorioallantoic membrane. Dev. Biol. 176:1996;76-85.
97. Wilting J., Eichmann A., Christ B. Expression of the avian VEGF receptor homologues Quek1 and Quek2 in blood-vascular and lymphatic endothelial and non-endothelial cells during quail embryonic development. Cell Tissue Res. 288:1997;207-222.
98. Wright D.E., White F.A., Gerfen R.W., Silossantiago I., Snider W.D. The guidance molecule semaphorin-III is expressed in regions of spinal-cord and periphery avoided by growing sensory axons. J. Comp. Neurol. 361:1995;321-333.
99. Yamada Y., Takakura N., Yasue H., Ogawa H., Fujisawa H., Suda T. Exogenous clustered neuropilin 1 enhances vasculogenesis and angiogenesis. Blood. 97:2001;1671-1678.
100. Yang Y., Drossopoulou G., Chuang P.T., Duprez D., Marti E., Bumcrot D., Vargesson N., Clarke J., Niswander L., McMahon A., Tickle C. Relationship between dose, distance and time in Sonic Hedgehog-mediated regulation of anteroposterior polarity in the chick limb. Development. 124:1997;4393-4404.
101. Yin M., Pacifici M. Vascular regression is required for mesenchymal condensation and chondrogenesis in the developing limb. Dev. Dyn. 222:2001;522-533.