The expanding role of neuropilin: Regulation of transforming growth factor-β and platelet-derived growth factor signaling in the vasculature

Current Opinion in Hematology

Volumn 23, Issue 3, 2016, Pages 260-267

  Kofler, Natalie ^a   Simons, Michael ^a  

^a YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Angiogenesis; Neuropilin; Platelet derived growth factor; Transforming growth factor b; Vascular smooth muscle cell

Indexed keywords

NEUROPILIN; PLATELET DERIVED GROWTH FACTOR; TRANSFORMING GROWTH FACTOR BETA; NEUROPILIN 1;

ANGIOGENESIS; BLOOD VESSEL; CELL MATURATION; ENDOTHELIUM CELL; HUMAN; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; REVIEW; VASCULAR SMOOTH MUSCLE CELL; ANIMAL; METABOLISM; NEOVASCULARIZATION (PATHOLOGY); SIGNAL TRANSDUCTION;

ANIMALS; BLOOD VESSELS; HUMANS; NEOVASCULARIZATION, PATHOLOGIC; NEUROPILIN-1; PLATELET-DERIVED GROWTH FACTOR; SIGNAL TRANSDUCTION; TRANSFORMING GROWTH FACTOR BETA;

EID: 84957636905     PISSN: 10656251     EISSN: 15317048     Source Type: Journal    
DOI: 10.1097/MOH.0000000000000233     Document Type: Review

References (82)

1. Kofler NM, Simons M. Angiogenesis versus arteriogenesis: neuropilin 1 modulation of VEGF signaling. F1000Prime Rep 2015; 7:26.
2. Plein A, Fantin A, Ruhrberg C. Neuropilin regulation of angiogenesis, arteriogenesis, and vascular permeability. Microcirculation 2014; 21:315-323.
3. Koch S. Neuropilin signalling in angiogenesis. Biochem Soc Trans 2012; 40:20-25.
4. Jubb AM, Strickland LA, Liu SD, et al. Neuropilin-1 expression in cancer and development. J Pathol 2012; 226:50-60.
5. Ball SG, Shuttleworth CA, Kielty CM. Vascular endothelial growth factor can signal through platelet-derived growth factor receptors. J Cell Biol 2007; 177:489-500.
6. Fantin A, Vieira JM, Gestri G, et al. Tissue macrophages act as cellular chaperones for vascular anastomosis downstream of VEGF-mediated endothelial tip cell induction. Blood 2010; 116:829-840.
7. Kitsukawa T, Shimono A, Kawakami A, et al. Overexpression of a membrane protein, neuropilin, in chimeric mice causes anomalies in the cardiovascular system, nervous system and limbs. Development 1995; 121:4309-4318.
8. Pan Q, Chanthery Y, Liang W-C, et al. Blocking neuropilin-1 function has an additive effect with anti-VEGF to inhibit tumor growth. Cancer Cell 2007; 11:53-67.
9. Pellet-Many C, Frankel P, Jia H, Zachary I. Neuropilins: structure, function and role in disease. Biochem J 2008; 411:211-226.
10. Chen H, Chédotal A, He Z, et al. Neuropilin-2, a novel member of the neuropilin family, is a high affinity receptor for the semaphorins Sema E and Sema IV but not Sema III. Neuron 1997; 19:547-559.
11. Mamluk R, Gechtman Z, Kutcher ME, et al. Neuropilin-1 binds vascular endothelial growth factor 165, placenta growth factor-2, and heparin via its b1b2 domain. J Biol Chem 2002; 277:24818-24825.
12. Gu C, Limberg BJ, Whitaker GB, et al. Characterization of neuropilin-1 structural features that confer binding to semaphorin 3A and vascular endothelial growth factor 165. J Biol Chem 2002; 277:18069-18076.
13. Cai H, Reed RR. Cloning and characterization of neuropilin-1-interacting protein: a PSD-95/Dlg/ZO-1 domain-containing protein that interacts with the cytoplasmic domain of neuropilin-1. J Neurosci 1999; 19:6519-6527.
14. Naccache SN, Hasson T, Horowitz A. Binding of internalized receptors to the PDZ domain of GIPC/synectin recruits myosin VI to endocytic vesicles. Proc Natl Acad Sci USA 2006; 103:12735-12740.
15. Chittenden TW, Claes F, Lanahan AA, et al. Selective regulation of arterial branching morphogenesis by synectin. Dev Cell 2006; 10:783-795.
16. Salikhova A, Wang L, Lanahan AA, et al. Vascular endothelial growth factor and semaphorin induce neuropilin-1 endocytosis via separate pathways. Circ Res 2008; 103:e71-e79.
17. Prahst C, Héroult M, Lanahan AA, et al. Neuropilin-1-VEGFR-2 complexing requires the PDZ-binding domain of neuropilin-1. J Biol Chem 2008; 283:25110-25114.
18. Lanahan AA, Hermans K, Claes F, et al. VEGF receptor 2 endocytic trafficking regulates arterial morphogenesis. Dev Cell 2010; 18:713-724.
19. Lanahan A, Zhang X, Fantin A, et al. The neuropilin 1 cytoplasmic domain is required for VEGF-A-dependent arteriogenesis. Dev Cell 2013; 25:156-168.
20. Koch S, van Meeteren LA, Morin E, et al. NRP1 presented in trans to the endothelium arrests VEGFR2 endocytosis, preventing angiogenic signaling and tumor initiation. Dev Cell 2014; 28:633-646.
21. Kitsukawa T, Shimizu M, Sanbo M, et al. Neuropilin-semaphorin III/D-mediated chemorepulsive signals play a crucial role in peripheral nerve projection in mice. Neuron 1997; 19:995-1005.
22. Kawasaki T, Kitsukawa T, Bekku Y, et al. A requirement for neuropilin-1 in embryonic vessel formation. Development 1999; 126:4895-4902.
23. Gerhardt H, Ruhrberg C, Abramsson A, et al. Neuropilin-1 is required for endothelial tip cell guidance in the developing central nervous system. Dev Dyn 2004; 231:503-509.
24. Fantin A, Vieira JM, Plein A, et al. NRP1 acts cell autonomously in endothelium to promote tip cell function during sprouting angiogenesis. Blood 2013; 121:2352-2362.
25. Gu C, Rodriguez ER, Reimert DV, et al. Neuropilin-1 conveys semaphorin and VEGF signaling during neural and cardiovascular development. Dev Cell 2003; 5:45-57.
26. Hirota S, Clements TP, Tang LK, et al. Neuropilin-1 balances β8 integrinactivated TGFβ signaling to control sprouting angiogenesis in the brain. Development 2015; 142:4363-4373.
27. Aspalter IM, Gordon E, Dubrac A, et al. Alk1 and Alk5 inhibition by Nrp1 controls vascular sprouting downstream of Notch. Nat Commun 2015; 6:7264.
28. Fantin A, Herzog B, Mahmoud M, et al. Neuropilin 1 (NRP1) hypomorphism combined with defective VEGF-A binding reveals novel roles for NRP1 in developmental and pathological angiogenesis. Development 2014; 141:556-562.
29. Gelfand MV, Hagan N, Tata A, et al. Neuropilin-1 functions as a VEGFR2 coreceptor to guide developmental angiogenesis independent of ligand binding. eLife 2014; 3:e03720.
30. Fantin A, Schwarz Q, Davidson K, et al. The cytoplasmic domain of neuropilin 1 is dispensable for angiogenesis, but promotes the spatial separation of retinal arteries and veins. Development 2011; 138:4185-4191.
31. Yuan L, Moyon D, Pardanaud L, et al. Abnormal lymphatic vessel development in neuropilin 2 mutant mice. Development 2002; 129:4797-4806.
32. Takashima S, Kitakaze M, Asakura M, et al. Targeting of both mouse neuropilin-1 and neuropilin-2 genes severely impairs developmental yolk sac and embryonic angiogenesis. Proc Natl Acad Sci USA 2002; 99:3657-3662.
33. Lanahan AA, Lech D, Dubrac A, et al. PTP1b is a physiologic regulator of VEGF signaling in endothelial cells. Circulation 2014; 130:902-909.
34. Ren B, Deng Y, Mukhopadhyay A, et al. ERK1/2-Akt1 crosstalk regulates arteriogenesis in mice and zebrafish. J Clin Invest 2010; 120:1217-1228.
35. Blanco R, Gerhardt H. VEGF and notch in tip and stalk cell selection. Cold Spring Harb Perspect Med 2013; 3:a006569.
36. Kofler NM, Shawber CJ, Kangsamaksin T, et al. Notch signaling in developmental and tumor angiogenesis. Genes Cancer 2011; 2:1106-1116.
37. Murga M, Fernandez-Capetillo O, Tosato G. Neuropilin-1 regulates attachment in human endothelial cells independently of vascular endothelial growth factor receptor-2. Blood 2005; 105:1992-1999.
38. Valdembri D, Caswell PT, Anderson KI, et al. Neuropilin-1/GIPC1 signaling regulates alpha5beta1 integrin traffic and function in endothelial cells. PLoS Biol 2009; 7:e25.
39. Robinson SD, Reynolds LE, Kostourou V, et al. Alphav beta3 integrin limits the contribution of neuropilin-1 to vascular endothelial growth factor-induced angiogenesis. J Biol Chem 2009; 284:33966-33981.
40. Ellison TS, Atkinson SJ, Steri V, et al. Suppression of β3-integrin in mice triggers a neuropilin-1-dependent change in focal adhesion remodelling that can be targeted to block pathological angiogenesis. Dis Model Mech 2015; 8:1105-1119.
41. Goumans M-J, Liu Z, Dijke ten P. TGF-beta signaling in vascular biology and dysfunction. Cell Res 2009; 19:116-127.
42. Jakobsson L, van Meeteren LA. Transforming growth factor β family members in regulation of vascular function: in the light of vascular conditional knockouts. Exp Cell Res 2013; 319:1264-1270.
43. Roelen BA, van Rooijen MA, Mummery CL. Expression of ALK-1, a type 1 serine/threonine kinase receptor, coincides with sites of vasculogenesis and angiogenesis in early mouse development. Dev Dyn 1997; 209:418-430.
44. Roelen BA, Lin HY, Knezević V, et al. Expression of TGF-beta s and their receptors during implantation and organogenesis of the mouse embryo. Dev Biol 1994; 166:716-728.
45. Cheifetz S, Bellón T, Calés C, et al. Endoglin is a component of the transforming growth factor-beta receptor system in human endothelial cells. J Biol Chem 1992; 267:19027-19030.
46. Lebrin F, Goumans M-J, Jonker L, et al. Endoglin promotes endothelial cell proliferation and TGF-beta/ALK1 signal transduction. EMBO J 2004; 23:4018-4028.
47. Gougos A, Letarte M. Primary structure of endoglin, an RGD-containing glycoprotein of human endothelial cells. J Biol Chem 1990; 265:8361-8364.
48. Massagué J, Seoane J, Wotton D. Smad transcription factors. Genes Dev Cold Spring Harbor Lab 2005; 19:2783-2810.
49. David L, Mallet C, Mazerbourg S, et al. Identification of BMP9 and BMP10 as functional activators of the orphan activin receptor-like kinase 1 (ALK1) in endothelial cells. Blood 2007; 109:1953-1961.
50. Oh SP, Seki T, Goss KA, et al. Activin receptor-like kinase 1 modulates transforming growth factor-beta 1 signaling in the regulation of angiogenesis. Proc Natl Acad Sci USA 2000; 97:2626-2631.
51. Massagué J. TGFβ signalling in context. Nat Rev Mol Cell Biol 2012; 13:616-630.
52. Larsson J, Goumans MJ, Sjöstrand LJ, et al. Abnormal angiogenesis but intact hematopoietic potential in TGF-beta type I receptor-deficient mice. EMBO J 2001; 20:1663-1673.
53. Oshima M, Oshima H, Taketo MM. TGF-beta receptor type II deficiency results in defects of yolk sac hematopoiesis and vasculogenesis. Dev Biol 1996; 179:297-302.
54. Arthur HM, Ure J, Smith AJ, et al. Endoglin, an ancillary TGFbeta receptor, is required for extraembryonic angiogenesis and plays a key role in heart development. Dev Biol 2000; 217:42-53.
55. Carvalho RLC, Itoh F, Goumans M-J, et al. Compensatory signalling induced in the yolk sac vasculature by deletion of TGFbeta receptors in mice. J Cell Sci 2007; 120 (Pt 24):4269-4277.
56. Lan Y, Liu B, Yao H, et al. Essential role of endothelial Smad4 in vascular remodeling and integrity. Mol Cell Biol 2007; 27:7683-7692.
57. Nguyen H-L, Lee YJ, Shin J, et al. TGF-β signaling in endothelial cells, but not neuroepithelial cells, is essential for cerebral vascular development. Lab Invest 2011; 91:1554-1563.
58. Robson A, Allinson KR, Anderson RH, et al. The TGFβ type II receptor plays a critical role in the endothelial cells during cardiac development. Dev Dyn 2010; 239:2435-2442.
59. Allinson KR, Lee HS, Fruttiger M, et al. Endothelial expression of TGFβ type II receptor is required to maintain vascular integrity during postnatal development of the central nervous system. PLoS One 2012; 7:e39336.
60. Arnold TD, Ferrero GM, Qiu H, et al. Defective retinal vascular endothelial cell development as a consequence of impaired integrin αVβ8-mediated activation of transforming growth factor-β. J Neurosci 2012; 32:1197-1206.
61. Itoh F, Itoh S, Adachi T, et al. Smad2/Smad3 in endothelium is indispensable for vascular stability via S1PR1 and N-cadherin expressions. Blood 2012; 119:5320-5328.
62. Moya IM, Umans L, Maas E, et al. Stalk cell phenotype depends on integration of Notch and Smad1/5 signaling cascades. Dev Cell 2012; 22:501-514.
63. Larrivée B, Prahst C, Gordon E, et al. ALK1 signaling inhibits angiogenesis by cooperating with the Notch pathway. Dev Cell 2012; 22:489-500.
64. Ricard N, Ciais D, Levet S, et al. BMP9 and BMP10 are critical for postnatal retinal vascular remodeling. Blood 2012; 119:6162-6171.
65. Glinka Y, Prud'homme GJ. Neuropilin-1 is a receptor for transforming growth factor beta-1, activates its latent form, and promotes regulatory T cell activity. J Leukoc Biol 2008; 84:302-310.
66. Glinka Y, Stoilova S, Mohammed N, Prud'homme GJ. Neuropilin-1 exerts coreceptor function for TGF-beta-1 on the membrane of cancer cells and enhances responses to both latent and active TGF-beta. Carcinogenesis 2011; 32:613-621.
67. Cao Y, Szabolcs A, Dutta SK, et al. Neuropilin-1 mediates divergent R-Smad signaling and the myofibroblast phenotype. J Biol Chem 2010; 285:31840-31848.
68. Majesky MW, Dong XR, Regan JN, Hoglund VJ. Vascular smooth muscle progenitor cells: building and repairing blood vessels. Circ Res 2011; 108:365-377.
69. Gomez D, Owens GK. Smooth muscle cell phenotypic switching in atherosclerosis. Cardiovasc Res 2012; 95:156-164.
70. Andrae J, Gallini R, Betsholtz C. Role of platelet-derived growth factors in physiology and medicine. Genes Dev 2008; 22:1276-1312.
71. Chen P-H, Chen X, He X. Platelet-derived growth factors and their receptors: structural and functional perspectives. Biochim Biophys Acta 2013; 1834:2176-2186.
72. Hellström M, Kalén M, Lindahl P, et al. Role of PDGF-B and PDGFR-beta in recruitment of vascular smooth muscle cells and pericytes during embryonic blood vessel formation in the mouse. Development 1999; 126:3047-3055.
73. Levéen P, Pekny M, Gebre-Medhin S, et al. Mice deficient for PDGF B show renal, cardiovascular, and hematological abnormalities. Genes Dev 1994; 8:1875-1887.
74. Lindahl P. Pericyte loss and microaneurysm formation in PDGF-B-deficient mice. Science 1997; 277:242-245.
75. Pellet-Many C, Frankel P, Evans IM, et al. Neuropilin-1 mediates PDGF stimulation of vascular smooth muscle cell migration and signalling via p130Cas. Biochem J 2011; 435:609-618.
76. Pellet-Many C, Mehta V, Fields L, et al. Neuropilins 1 and 2 mediate neointimal hyperplasia and re-endothelialization following arterial injury. Cardiovasc Res 2015; 108:288-298.
77. Banerjee S, Sengupta K, Dhar K, et al. Breast cancer cells secreted plateletderived growth factor-induced motility of vascular smooth muscle cells is mediated through neuropilin-1. Mol Carcinog 2006; 45:871-880.
78. Shintani Y, Takashima S, Asano Y, et al. Glycosaminoglycan modification of neuropilin-1 modulates VEGFR2 signaling. EMBO J 2006; 25:3045-3055.
79. Liu W, Parikh AA, Stoeltzing O, et al. Upregulation of neuropilin-1 by basic fibroblast growth factor enhances vascular smooth muscle cell migration in response to VEGF. Cytokine 2005; 32:206-212.
80. Stephenson JM, Banerjee S, Saxena NK, et al. Neuropilin-1 is differentially expressed in myoepithelial cells and vascular smooth muscle cells in preneoplastic and neoplastic human breast: a possible marker for the progression of breast cancer. Int J Cancer 2002; 101:409-414.
81. Ball SG, Bayley C, Shuttleworth CA, Kielty CM. Neuropilin-1 regulates platelet-derived growth factor receptor signalling in mesenchymal stem cells. Biochem J 2010; 427:29-40.
82. Yamaji M, Mahmoud M, Evans IM, Zachary IC. Neuropilin 1 is essential for gastrointestinal smooth muscle contractility and motility in aged mice. PLoS One 2015; 10:e0115563.