Fetal, but not postnatal, deletion of semaphorin-neuropilin-1 signaling affects murine alveolar development

American Journal of Respiratory Cell and Molecular Biology

Volumn 49, Issue 4, 2013, Pages 627-636

  Joza, Stephen ^a,b   Wang, Jinxia ^a   Tseu, Irene ^a   Ackerley, Cameron ^a   Post, Martin ^a,b  

^a HOSPITAL FOR SICK CHILDREN   (Canada)

^b UNIVERSITY OF TORONTO   (Canada)

Author keywords

Alveolarization; Neuropilin; Semaphorin; Vascular development

Indexed keywords

NEUROPILIN 1; SEMAPHORIN; SEMAPHORIN 3; UNCLASSIFIED DRUG; VASCULOTROPIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CAPILLARY DENSITY; CONTROLLED STUDY; DISEASE SEVERITY; FEMALE; GENE DELETION; LUNG ALVEOLUS CELL; LUNG BLOOD VESSEL; LUNG DEVELOPMENT; LUNG DYSPLASIA; LUNG FUNCTION; LUNG HEMORRHAGE; LUNG VASCULAR RESISTANCE; MALE; MOUSE; NEWBORN MORTALITY; NONHUMAN; POSTNATAL DEVELOPMENT; PROTEIN PROTEIN INTERACTION; RAT; RESPIRATORY DISTRESS; SIGNAL TRANSDUCTION;

ANIMALS; CAPILLARIES; ENDOTHELIUM, VASCULAR; FEMALE; FETUS; MALE; MICE; NEUROPILIN-1; PREGNANCY; PULMONARY ALVEOLI; SEMAPHORINS; SEQUENCE DELETION; SIGNAL TRANSDUCTION; VASCULAR ENDOTHELIAL GROWTH FACTOR RECEPTOR-2;

EID: 84886472003     PISSN: 10441549     EISSN: 15354989     Source Type: Journal    
DOI: 10.1165/rcmb.2012-0407OC     Document Type: Article

References (49)

1. Bhatt AJ, Pryhuber GS, Huyck H, Watkins RH, Metlay LA, Maniscalco WM. Disrupted pulmonary vasculature and decreased vascular endothelial growth factor, Flt-1, and TIE-2 in human infants dying with bronchopulmonary dysplasia. Am J Respir Crit Care Med 2001; 164:1971-1980.
2. Maniscalco WM, Watkins RH, Pryhuber GS, Bhatt A, Shea C, Huyck H. Angiogenic factors and alveolar vasculature: development and alterations by injury in very premature baboons. Am J Physiol Lung Cell Mol Physiol 2002;282:L811-L823.
3. Th'baud B, Ladha F, Michelakis ED, Sawicka M, Thurston G, Eaton F, Hashimoto K, Harry G, Haromy A, Korbutt G, et al. Vascular endothelial growth factor gene therapy increases survival, promotes lung angiogenesis, and prevents alveolar damage in hyperoxia-induced lung injury: evidence that angiogenesis participates in alveolarization. Circulation 2005;112:2477-2486.
4. De Paepe ME, Patel C, Tsai A, Gundavarapu S, Mao Q. Endoglin (CD105) up-regulation in pulmonary microvasculature of ventilated preterm infants. Am J Respir Crit Care Med 2008;178:180-187.
5. Le Cras TD, Markham NE, Tuder RM, Voelkel NF, Abman SH. Treatment of newborn rats with a VEGF receptor inhibitor causes pulmonary hypertension and abnormal lung structure. Am J Physiol Lung Cell Mol Physiol 2002;283:L555-L562.
6. McGrath-Morrow SA, Cho C, Cho C, Zhen L, Hicklin DJ, Tuder RM. Vascular endothelial growth factor receptor 2 blockade disrupts postnatal lung development. Am J Respir Cell Mol Biol 2005;32:420-427.
7. Lin YJ, Markham NE, Balasubramaniam V, Tang JR, Maxey A, Kinsella JP, Abman SH. Inhaled nitric oxide enhances distal lung growth after exposure to hyperoxia in neonatal rats. Pediatr Res 2005;58:22-29.
8. Compernolle V, Brusselmans K, Acker T, Hoet P, Tjwa M, Beck H, Plaisance S, Dor Y, Keshet E, Lupu F, et al. Loss of HIF-2alpha and inhibition of VEGF impair fetal lung maturation, whereas treatment with VEGF prevents fatal respiratory distress in premature mice. Nat Med 2002;8:702-710.
9. Tang JR, Markham NE, Lin YJ, McMurtry IF, Maxey A, Kinsella JP, Abman SH. Inhaled nitric oxide attenuates pulmonary hypertension and improves lung growth in infant rats after neonatal treatment with a VEGF receptor inhibitor. Am J Physiol Lung Cell Mol Physiol 2004;287:L344-L351.
10. Bhandari V, Choo-Wing R, Lee CG, Yusuf K, Nedrelow JH, Ambalavanan N, Malkus H, Homer RJ, Elias JA. Developmental regulation of NO-mediated VEGF-induced effects in the lung. Am J Respir Cell Mol Biol 2008;39:420-430.
11. Le Cras TD, Spitzmiller RE, Albertine KH, Greenberg JM,Whitsett JA, Akeson AL. VEGF causes pulmonary hemorrhage, hemosiderosis, and air space enlargement in neonatal mice. Am J Physiol Lung Cell Mol Physiol 2004;287:L134-L142.
12. Abman SH. Impaired vascular endothelial growth factor signaling in the pathogenesis of neonatal pulmonary vascular disease. Adv Exp Med Biol 2010;661:323-335.
13. Pan Q, Chanthery Y, Liang WC, Stawicki S, Mak J, Rathore N, Tong RK, Kowalski J, Yee SF, Pacheco G, et al. Blocking neuropilin-1 function has an additive effect with anti-VEGF to inhibit tumor growth. Cancer Cell 2007;11:53-67.
14. Herzog B, Pellet-Many C, Britton G, Hartzoulakis B, Zachary IC. VEGF binding to NRP1 is essential for VEGF stimulation of endothelial cell migration, complex formation between NRP1 and VEGFR2, and signaling via FAK Tyr407 phosphorylation. Mol Biol Cell 2011;22:2766-2776.
15. Cimato T, Beers J, Ding S, Ma M, McCoy JP, Boehm M, Nabel EG. Neuropilin-1 identifies endothelial precursors in human and murine embryonic stem cells before CD34 expression. Circulation 2009;119: 2170-2178.
16. Acevedo LM, Barillas S,Weis SM, G'thert JR, Cheresh DA. Semaphorin 3A suppresses VEGF-mediated angiogenesis yet acts as a vascular permeability factor. Blood 2008;111:2674-2680.
17. Kawasaki T, Kitsukawa T, Bekku Y, Matsuda Y, Sanbo M, Yagi T, Fujisawa H. A requirement for neuropilin-1 in embryonic vessel formation. Development 1999;126:4895-4902.
18. Gu C, Rodriguez ER, Reimert DV, Shu T, Fritzsch B, Richards LJ, Kolodkin AL, Ginty DD. Neuropilin-1 conveys semaphorin and VEGF signaling during neural and cardiovascular development. Dev Cell 2003;5: 45-57.
19. Serini G, Valdembri D, Zanivan S, Morterra G, Burkhardt C, Caccavari F, Zammataro L, Primo L, Tamagnone L, Logan M, et al. Class 3 semaphorins control vascular morphogenesis by inhibiting integrin function. Nature 2003;424:391-397.
20. Kutschera S, Weber H, Weick A, De Smet F, Genove G, Takemoto M, Prahst C, Riedel M, Mikelis C, Baulande S, et al. Differential endothelial transcriptomics identifies semaphorin 3G as a vascular class 3 semaphorin. Arterioscler Thromb Vasc Biol 2011;31:151-159.
21. Maione F, Capano S, Regano D, Zentilin L, Giacca M, Casanovas O, Bussolino F, Serini G, Giraudo E. Semaphorin 3A overcomes cancer hypoxia and metastatic dissemination induced by antiangiogenic treatment in mice. J Clin Invest 2012;122:1832-1848.
22. Joza S, Wang J, Fox E, Hillman V, Ackerley C, Post M. Loss of semaphorin-neuropilin-1 signaling causes dysmorphic vascularization reminiscent of alveolar capillary dysplasia. Am J Pathol 2012;181: 2003-2017.
23. Tambunting F, Beharry KD, Waltzman J, Modanlou HD. Impaired lung vascular endothelial growth factor in extremely premature baboons developing bronchopulmonary dysplasia/chronic lung disease. J Investig Med 2005;53:253-262.
24. Jakkula M, Le Cras TD, Gebb S, Hirth KP, Tuder RM, Voelkel NF, Abman SH. Inhibition of angiogenesis decreases alveolarization in the developing rat lung. Am J Physiol Lung Cell Mol Physiol 2000; 279:L600-L607.
25. Adams RH, Lohrum M, Klostermann A, Betz H, P'schel AW. The chemorepulsive activity of secreted semaphorins is regulated by furin-dependent proteolytic processing. EMBO J 1997;16:6077-6086.
26. Le A, Zielinski R, He C, Crow MT, Biswal S, Tuder RM, Becker PM. Pulmonary epithelial neuropilin-1 deletion enhances development of cigarette smoke-induced emphysema. Am J Respir Crit Care Med 2009;180:396-406.
27. Hayashi S, McMahon AP. Efficient recombination in diverse tissues by a tamoxifen-inducible form of Cre: a tool for temporally regulated gene activation/inactivation in the mouse. Dev Biol 2002;244:305-318.
28. Maione F, Molla F, Meda C, Latini R, Zentilin L, Giacca M, Seano G, Serini G, Bussolino F, Giraudo E. Semaphorin 3A is an endogenous angiogenesis inhibitor that blocks tumor growth and normalizes tumor vasculature in transgenic mouse models. J Clin Invest 2009;119:3356-3372.
29. Rock JR, Barkauskas CE, Cronce MJ, Xue Y, Harris JR, Liang J, Noble PW, Hogan BL. Multiple stromal populations contribute to pulmonary fibrosis without evidence for epithelial to mesenchymal transition. Proc Natl Acad Sci USA 2011;108:E1475-E1483.
30. Humphreys BD, Lin SL, Kobayashi A, Hudson TE, Nowlin BT, Bonventre JV, Valerius MT, McMahon AP, Duffield JS. Fate tracing reveals the pericyte and not epithelial origin of myofibroblasts in kidney fibrosis. Am J Pathol 2010;176:85-97.
31. Becker PM, Tran TS, Delannoy MJ, He C, Shannon JM, McGrath-Morrow S. Semaphorin 3A contributes to distal pulmonary epithelial cell differentiation and lung morphogenesis. PLoS ONE 2011;6:e27449.
32. Gerhardt H, Ruhrberg C, Abramsson A, Fujisawa H, Shima D, Betsholtz C. Neuropilin-1 is required for endothelial tip cell guidance in the developing central nervous system. Dev Dyn 2004;231:503-509.
33. Mund SI, Stampanoni M, Schittny JC. Developmental alveolarization of the mouse lung. Dev Dyn 2008;237:2108-2116.
34. Schittny JC,Mund SI, Stampanoni M. Evidence and structural mechanism for late lung alveolarization. Am J Physiol Lung Cell Mol Physiol 2008; 294:L246-L254.
35. Yi M, Jankov RP, Belcastro R, Humes D, Copland I, Shek S, Sweezey NB, Post M, Albertine KH, Auten RL, et al. Opposing effects of 60% oxygen and neutrophil influx on alveologenesis in the neonatal rat. Am J Respir Crit Care Med 2004;170:1188-1196.
36. Jankov RP, Johnstone L, Luo X, Robinson BH, Tanswell AK. Macrophages as a major source of oxygen radicals in the hyperoxic newborn rat lung. Free Radic Biol Med 2003;35:200-209.
37. Bourbon JR, Boucherat O, Boczkowski J, Crestani B, Delacourt C. Bronchopulmonary dysplasia and emphysema: in search of common therapeutic targets. Trends Mol Med 2009;15:169-179.
38. Le Cras TD, Hardie WD, Deutsch GH, Albertine KH, Ikegami M, Whitsett JA, Korfhagen TR. Transient induction of TGF-alpha disrupts lung morphogenesis, causing pulmonary disease in adulthood. Am J Physiol Lung Cell Mol Physiol 2004;287:L718-L729.
39. Tomashefski JF Jr, Farver CF. Anatomy and histology of the lung. In: Tomashefski JF, Jr., Cagle PT, Farver CF, Fraire AE, editors. Dail and Hammar's pulmonary pathology, 3rd ed. New York: Springer Science; 2008. pp. 20-48.
40. Beasley MB. Acute lung injury. In: Tomashefski JF, Jr., Cagle PT, Farver CF, Fraire AE, editors. Dail and Hammar's pulmonary pathology, 3rd ed. New York: Springer Science; 2008. pp. 64-83.
41. Marwick JA, Stevenson CS, Giddings J, MacNee W, Butler K, Rahman I, Kirkham PA. Cigarette smoke disrupts VEGF165-VEGFR-2 receptor signaling complex in rat lungs and patients with COPD: morphological impact of VEGFR-2 inhibition. Am J Physiol Lung Cell Mol Physiol 2006;290:L897-L908.
42. Ferrara N, Carver-Moore K, Chen H, Dowd M, Lu L, O'Shea KS, Powell-Braxton L, Hillan KJ, Moore MW. Heterozygous embryonic lethality induced by targeted inactivation of the VEGF gene. Nature 1996;380:439-442.
43. Gerber HP, Hillan KJ, Ryan AM, Kowalski J, Keller GA, Rangell L, Wright BD, Radtke F, Aguet M, Ferrara N. VEGF is required for growth and survival in neonatal mice. Development 1999;126:1149-1159.
44. Shalaby F, Rossant J, Yamaguchi TP, Gertsenstein M, Wu XF, Breitman ML, Schuh AC. Failure of blood-island formation and vasculogenesis in Flk-1-deficient mice. Nature 1995;376:62-66.
45. Fong GH, Rossant J, Gertsenstein M, Breitman ML. Role of the Flt-1 receptor tyrosine kinase in regulating the assembly of vascular endothelium. Nature 1995;376:66-70.
46. Holmes DI, Zachary IC. Vascular endothelial growth factor regulates stanniocalcin-1 expression via neuropilin-1-dependent regulation of KDR and synergism with fibroblast growth factor-2. Cell Signal 2008; 20:569-579.
47. Raoul W, Chailley-Heu B, Barlier-Mur AM, Delacourt C, Ma'tre B, Bourbon JR. Effects of vascular endothelial growth factor on isolated fetal alveolar type II cells. Am J Physiol Lung Cell Mol Physiol 2004; 286:L1293-L1301.
48. G'ritz C, Dias DO, Tomilin N, Barbacid M, Shupliakov O, Fris'n J. A pericyte origin of spinal cord scar tissue. Science 2011;333:238-242.
49. Reidy KJ, Villegas G, Teichman J, Veron D, Shen W, Jimenez J, Thomas D, Tufro A. Semaphorin3a regulates endothelial cell number and podocyte differentiation during glomerular development. Development 2009;136:3979-3989.