Nuclear localization of platelet-activating factor receptor controls retinal neovascularization

Cell Discovery

Volumn 2, Issue , 2016, Pages

  Bhosle, Vikrant ^a,b,c   Rivera, José Carlos ^b,c   Zhou, T ^a,b,c,d   Omri, Samy ^b,c   Sanchez, Melanie ^a,b,c   Hamel, David ^b,c   Zhu, Tang ^b   Rouget, Raphael ^a,b   Rabea, Areej Al ^e   Hou, Xin ^b   Lahaie, Isabelle ^b,c   Ribeiro Da Silva, Alfredo ^a,f   Chemtob, Sylvain ^a,b,c  

^a MCGILL UNIVERSITY   (Canada)

^b UNIVERSITY OF MONTREAL   (Canada)

^c UNIVERSITÉ DE MONTRÉAL   (Canada)

^d MCGILL UNIVERSITY HEALTH CENTRE   (Canada)

^e MONTREAL GENERAL HOSPITAL   (Canada)

^f MCGILL UNIVERSITY   (Canada)

Author keywords

Angiogenesis; importin; nuclear GPCR; Ptafr; rab GTPase

Indexed keywords

APAFANT; GINKGOLIDE B; IMPORTIN 5; KARYOPHERIN; RAB PROTEIN; RAB11A PROTEIN; THROMBOCYTE ACTIVATING FACTOR; THROMBOCYTE ACTIVATING FACTOR RECEPTOR; UNCLASSIFIED DRUG; VASCULOTROPIN;

ANGIOGENESIS; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CAPILLARY ENDOTHELIAL CELL; CARBOXY TERMINAL SEQUENCE; CELL MEMBRANE PERMEABILITY; CELLULAR DISTRIBUTION; CONTROLLED STUDY; EMBRYO; EX VIVO STUDY; FEMALE; HUMAN; HUMAN CELL; IN VITRO STUDY; IN VIVO STUDY; NEWBORN; NONHUMAN; NUCLEAR LOCALIZATION SIGNAL; PHOSPHOLIPID SYNTHESIS; PRIORITY JOURNAL; PROTEIN MOTIF; RAT; RETINA BLOOD VESSEL; RETINA NEOVASCULARIZATION; RETROLENTAL FIBROPLASIA; UPREGULATION;

EID: 85021670713     PISSN: None     EISSN: 20565968     Source Type: Journal    
DOI: 10.1038/celldisc.2016.17     Document Type: Article

References (114)

1. Barbaro JF, Zvaifler NJ. Antigen induced histamine release from platelets of rabbits producing homologous PCA antibody. Proc Soc Exp Biol Med 1966; 122: 1245-1247.
2. Ishii S, Nagase T, Tashiro F et al. Bronchial hyperreactivity, increased endotoxin lethality and melanocytic tumorigenesis in transgenic mice overexpressing plateletactivating factor receptor. EMBO J 1997; 16: 133-142.
3. Stafforini DM, Numao T, Tsodikov A et al. Deficiency of platelet-activating factor acetylhydrolase is a severity factor for asthma. J Clin Invest 1999; 103: 989-997.
4. Cundell DR, Gerard NP, Gerard C, Idanpaan-Heikkila I, Tuomanen EI. Streptococcus pneumoniae anchor to activated human cells by the receptor for plateletactivating factor. Nature 1995; 377: 435-438.
5. Harris ES, Rondina MT, Schwertz H, Weyrich AS, Zimmerman GA. Pathogenesis of sepsis and sepsis-induced acute lung injury. Acute Respiratory Distress Syndrome 2010; 2: 369-419.
6. Vadas P, Gold M, Perelman B et al. Platelet-activating factor, PAF acetylhydrolase, and severe anaphylaxis. N Engl J Med 2008; 358: 28-35.
7. Montrucchio G, Alloatti G, Camussi G. Role of platelet-activating factor in cardiovascular pathophysiology. Physiol Rev 2000; 80: 1669-1699.
8. Imaizumi TA, Stafforini DM, Yamada Y, McIntyre TM, Prescott SM, Zimmerman GA. Platelet-activating factor: a mediator for clinicians. J Intern Med 1995; 238: 5-20.
9. Chao W, Olson MS. Platelet-activating factor: receptors and signal transduction. Biochem J 1993; 292(Pt 3): 617-629.
10. Lynch JM, Henson PM. The intracellular retention of newly synthesized platelet-activating factor. J Immunol 1986; 137: 2653-2661.
11. Liu J, Chen R, Marathe GK, Febbraio M, Zou W, McIntyre TM. Circulating platelet-activating factor is primarily cleared by transport, not intravascular hydrolysis by lipoprotein-associated phospholipase A2/PAF acetylhydrolase. Circ Res 2011; 108: 469-477.
12. Tjoelker LW, Wilder C, Eberhardt C et al. Antiinflammatory properties of a platelet-activating factor acetylhydrolase. Nature 1995; 374: 549-553.
13. Arai H, Koizumi H, Aoki J, Inoue K. Platelet-activating factor acetylhydrolase (PAF-AH). J Biochem 2002; 131: 635-640.
14. Yamanaka S, Miura K, Yukimura T, Okumura M, Yamamoto K. Putative mechanism of hypotensive action of platelet-activating factor in dogs. Circ Res 1992; 70: 893-901.
15. Juncos LA, Ren YL, Arima S, Ito S. Vasodilator and constrictor actions of platelet-activating factor in the isolated microperfused afferent arteriole of the rabbit kidney. Role of endothelium-derived relaxing factor/nitric oxide and cyclooxygenase products. J Clin Invest 1993; 91: 1374-1379.
16. Sanchez FA, Rana R, Kim DD et al. Internalization of eNOS and NO delivery to subcellular targets determine agonist-induced hyperpermeability. Proc Natl Acad Sci USA 2009; 106: 6849-6853.
17. Beauchamp MH, Marrache AM, Hou X et al. Plateletactivating factor in vasoobliteration of oxygen-induced retinopathy. Invest Ophthalmol Vis Sci 2002; 43: 3327-3337.
18. Camussi G, Montrucchio G, Lupia E, Soldi R, Comoglio PM, Bussolino F. Angiogenesis induced in vivo by hepatocyte growth factor is mediated by plateletactivating factor synthesis from macrophages. J Immunol 1997; 158: 1302-1309.
19. Ko HM, Seo KH, Han SJ et al. Nuclear factor kappaB dependency of platelet-activating factor-induced angiogenesis. Cancer Res 2002; 62: 1809-1814.
20. Ferrandon S, Feinstein TN, Castro M et al. Sustained cyclic AMP production by parathyroid hormone receptor endocytosis. Nat Chem Biol 2009; 5: 734-742.
21. Benard G, Massa F, Puente N et al. Mitochondrial CB(1) receptors regulate neuronal energy metabolism. Nat Neurosci 2012; 15: 558-564.
22. Joyal JS, Nim S, Zhu T et al. Subcellular localization of coagulation factor II receptor-like 1 in neurons governs angiogenesis. Nat Med 2014; 20: 1165-1173.
23. Di Benedetto A, Sun L, Zambonin CG et al. Osteoblast regulation via ligand-activated nuclear trafficking of the oxytocin receptor. Proc Natl Acad Sci USA 2014; 111: 16502-16507.
24. Gobeil F, Fortier A, Zhu T et al. G-protein-coupled receptors signalling at the cell nucleus: an emerging paradigm. Can J Physiol Pharmacol 2006; 84: 287-297.
25. Joyal JS, Bhosle VK, Chemtob S. Subcellular G-protein coupled receptor signaling hints at greater therapeutic selectivity. Expert Opin Ther Targets 2015; 19: 717-721.
26. Marrache AM, Gobeil F Jr, Bernier SG et al. Proinflammatory gene induction by platelet-activating factor mediated via its cognate nuclear receptor. J Immunol 2002; 169: 6474-6481.
27. D'Souza-Schorey C, Chavrier P. ARF proteins: roles in membrane traffic and beyond. Nat Rev Mol Cell Biol 2006; 7: 347-358.
28. Hutagalung AH, Novick PJ. Role of Rab GTPases in membrane traffic and cell physiology. Physiol Rev 2011; 91: 119-149.
29. Chook YM, Suel KE. Nuclear import by karyopherinbetas: recognition and inhibition. Biochim Biophys Acta 2011; 1813: 1593-1606.
30. Lee DK, Lanca AJ, Cheng R et al. Agonist-independent nuclear localization of the Apelin, angiotensin AT1, and bradykinin B2 receptors. J Biol Chem 2004; 279: 7901-7908.
31. McCudden CR, Hains MD, Kimple RJ, Siderovski DP, Willard FS. G-protein signaling: back to the future. Cell Mol Life Sci 2005; 62: 551-577.
32. DeFea KA. Beta-arrestins as regulators of signal termination and transduction: how do they determine what to scaffold? Cell Signal 2011; 23: 621-629.
33. Lukashova V, Chen Z, Duhe RJ, Rola-Pleszczynski M, Stankova J. Janus kinase 2 activation by the platelet-activating factor receptor (PAFR): roles of Tyk2 and PAFR C terminus. J Immunol 2003; 171: 3794-3800.
34. Campden R, Audet N, Hebert TE. Nuclear G protein signaling: new tricks for old dogs. J Cardiovasc Pharmacol 2015; 65: 110-122.
35. Beaulieu JM, Caron MG. Beta-arrestin goes nuclear. Cell 2005; 123: 755-757.
36. Zhang Y, Matkovich SJ, Duan X, Gold JI, Koch WJ, DornGWII. Nuclear effects of G-protein receptor kinase 5 on histone deacetylase 5-regulated gene transcription in heart failure. Circ Heart Fail 2011; 4: 659-668.
37. Wright CD, Chen Q, Baye NL et al. Nuclear alpha1-adrenergic receptors signal activated ERK localization to caveolae in adult cardiac myocytes. Circ Res 2008; 103: 992-1000.
38. Vaniotis G, Del Duca D, Trieu P, Rohlicek CV, Hebert TE, Allen BG. Nuclear beta-adrenergic receptors modulate gene expression in adult rat heart. Cell Signal 2011; 23: 89-98.
39. Zhu T, Gobeil F, Vazquez-Tello A et al. Intracrine signaling through lipid mediators and their cognate nuclear G-protein-coupled receptors: a paradigm based on PGE2, PAF, and LPA1 receptors. Can J Physiol Pharmacol 2006; 84: 377-391.
40. Bhosle VK, Gobeil F Jr, Rivera JC, Ribeiro-da-Silva A, Chemtob S. High resolution imaging and function of nuclear G protein-coupled receptors (GPCRs). Methods Mol Biol 2015; 1234: 81-97.
41. Peirce MJ, Wait R, Begum S, Saklatvala J, Cope AP. Expression profiling of lymphocyte plasma membrane proteins. Mol Cell Proteomics 2004; 3: 56-65.
42. Carolan EJ, Casale TB. Degree of platelet activating factor-induced neutrophil migration is dependent upon the molecular species. J Immunol 1990; 145: 2561-2565.
43. Macia E, Ehrlich M, Massol R, Boucrot E, Brunner C, Kirchhausen T. Dynasore, a cell-permeable inhibitor of dynamin. Dev Cell 2006; 10: 839-850.
44. Self TJ, Oakley SM, Hill SJ. Clathrin-independent internalization of the human histamine H1-receptor in CHO-K1 cells. Br J Pharmacol 2005; 146: 612-624.
45. Prescott SM, Zimmerman GA, Stafforini DM, McIntyre TM. Platelet-activating factor and related lipid mediators. Annu Rev Biochem 2000; 69: 419-445.
46. Murakami M, Taketomi Y, Miki Y, Sato H, Hirabayashi T, Yamamoto K. Recent progress in phospholipase A(2) research: from cells to animals to humans. Prog Lipid Res 2011; 50: 152-192.
47. Dingwall C, Laskey RA. Nuclear targeting sequences-a consensus? Trends Biochem Sci 1991; 16: 478-481.
48. Mizuno-Yamasaki E, Rivera-Molina F, Novick P. GTPase networks in membrane traffic. Annu Rev Biochem 2012; 81: 637-659.
49. Chavrier P, Parton RG, Hauri HP, Simons K, Zerial M. Localization of low molecular weight GTP binding proteins to exocytic and endocytic compartments. Cell 1990; 62: 317-329.
50. Dupre DJ, Chen Z, Le Gouill C et al. Trafficking, ubiquitination, and down-regulation of the human plateletactivating factor receptor. J Biol Chem 2003; 278: 48228-48235.
51. Pasqualato S, Senic-Matuglia F, Renault L, Goud B, Salamero J, Cherfils J. The structural GDP/GTP cycle of Rab11 reveals a novel interface involved in the dynamics of recycling endosomes. J Biol Chem 2004; 279: 11480-11488.
52. Ren M, Xu G, Zeng J, De Lemos-Chiarandini C, Adesnik M, Sabatini DD. Hydrolysis of GTP on rab11 is required for the direct delivery of transferrin from the pericentriolar recycling compartment to the cell surface but not from sorting endosomes. Proc Natl Acad Sci USA 1998; 95: 6187-6192.
53. Lusk CP, Blobel G, King MC. Highway to the inner nuclear membrane: rules for the road. Nat Rev Mol Cell Biol 2007; 8: 414-420.
54. Mosca TJ, Schwarz TL. The nuclear import of Frizzled2-C by Importins-beta11 and alpha2 promotes postsynaptic development. Nat Neurosci 2010; 13: 935-943.
55. Lee BJ, Cansizoglu AE, Suel KE, Louis TH, Zhang Z, Chook YM. Rules for nuclear localization sequence recognition by karyopherin beta 2. Cell 2006; 126: 543-558.
56. Deane R, Schafer W, Zimmermann HP et al. Ran-binding protein 5 (RanBP5) is related to the nuclear transport factor importin-beta but interacts differently with RanBP1. Mol Cell Biol 1997; 17: 5087-5096.
57. Marcheselli VL, Rossowska MJ, Domingo MT, Braquet P, Bazan NG. Distinct platelet-activating factor binding sites in synaptic endings and in intracellular membranes of rat cerebral cortex. J Biol Chem 1990; 265: 9140-9145.
58. Teather LA, Magnusson JE, Wurtman RJ. Plateletactivating factor antagonists decrease the inflammatory nociceptive response in rats. Psychopharmacology (Berl) 2002; 163: 430-433.
59. Ikegami K, Meade CJ, Heuer HO, Birke F. Hetrazepine PAF antagonists. J Lipid Mediat 1992; 5: 177-182.
60. De Kimpe SJ, Thiemermann C, Vane JR. Role for intracellular platelet-activating factor in the circulatory failure in a model of gram-positive shock. Br J Pharmacol 1995; 116: 3191-3198.
61. Mattson G, Conklin E, Desai S, Nielander G, Savage MD, Morgensen S. A practical approach to crosslinking. Mol Biol Rep 1993; 17: 167-183.
62. Angers S, Salahpour A, Joly E et al. Detection of beta 2-adrenergic receptor dimerization in living cells using bioluminescence resonance energy transfer (BRET). Proc Natl Acad Sci USA 2000; 97: 3684-3689.
63. Barnett JM, Yanni SE, Penn JS. The development of the rat model of retinopathy of prematurity. Doc Ophthalmol 2010; 120: 3-12.
64. Poubelle PE, Gingras D, Demers C et al. Platelet-activating factor (PAF-acether) enhances the concomitant production of tumour necrosis factor-alpha and interleukin-1 by subsets of human monocytes. Immunology 1991; 72: 181-187.
65. Ma X, Ottino P, Bazan HE, Bazan NG. Platelet-activating factor (PAF) induces corneal neovascularization and upregulates VEGF expression in endothelial cells. Invest Ophthalmol Vis Sci 2004; 45: 2915-2921.
66. Bussolati B, Biancone L, Cassoni P et al. PAF produced by human breast cancer cells promotes migration and proliferation of tumor cells and neo-angiogenesis. Am J Pathol 2000; 157: 1713-1725.
67. Aponte M, Jiang W, Lakkis Met al. Activation of plateletactivating factor receptor and pleiotropic effects on tyrosine phospho-EGFR/Src/FAK/paxillin in ovarian cancer. Cancer Res 2008; 68: 5839-5848.
68. Kim HA, Kim KJ, Yoon SY, Lee HK, Im SY. Glutamine inhibits platelet-activating factor-mediated pulmonary tumour metastasis. Eur J Cancer 2012; 48: 1730-1738.
69. Harris JR. The biochemistry and ultrastructure of the nuclear envelope. Biochim Biophys Acta 1978; 515: 55-104.
70. Ungricht R, Klann M, Horvath P, Kutay U. Diffusion and retention are major determinants of protein targeting to the inner nuclear membrane. J Cell Biol 2015; 209: 687-703.
71. Dong C, Filipeanu CM, Duvernay MT, Wu G. Regulation of G protein-coupled receptor export trafficking. Biochim Biophys Acta 2007; 1768: 853-870.
72. Schievella AR, Regier MK, Smith WL, Lin LL. Calciummediated translocation of cytosolic phospholipase A2 to the nuclear envelope and endoplasmic reticulum. J Biol Chem 1995; 270: 30749-30754.
73. Bahmanyar S. Spatial regulation of phospholipid synthesis within the nuclear envelope domain of the endoplasmic reticulum. Nucleus 2015; 6: 102-106.
74. Ribbes G, Ninio E, Fontan P et al. Evidence that biosynthesis of platelet-activating factor (paf-acether) by human neutrophils occurs in an intracellular membrane. FEBS Lett 1985; 191: 195-199.
75. Bhattacharya M, Peri KG, Almazan G et al. Nuclear localization of prostaglandin E2 receptors. Proc Natl Acad Sci USA 1998; 95: 15792-15797.
76. Bhattacharya M, Peri K, Ribeiro-da-Silva A et al. Localization of functional prostaglandin E2 receptors EP3 and EP4 in the nuclear envelope. J Biol Chem 1999; 274: 15719-15724.
77. Gobeil F Jr, Dumont I, Marrache AM et al. Regulation of eNOS expression in brain endothelial cells by perinuclear EP(3) receptors. Circ Res 2002; 90: 682-689.
78. Alon T, Hemo I, Itin A, Pe'er J, Stone J, Keshet E. Vascular endothelial growth factor acts as a survival factor for newly formed retinal vessels and has implications for retinopathy of prematurity. Nat Med 1995; 1: 1024-1028.
79. Murohara T, Asahara T, Silver M et al. Nitric oxide synthase modulates angiogenesis in response to tissue ischemia. J Clin Invest 1998; 101: 2567-2578.
80. Ullrich O, Reinsch S, Urbe S, Zerial M, Parton RG. Rab11 regulates recycling through the pericentriolar recycling endosome. J Cell Biol 1996; 135: 913-924.
81. Urbe S, Huber LA, Zerial M, Tooze SA, Parton RG. Rab11, a small GTPase associated with both constitutive and regulated secretory pathways in PC12 cells. FEBS Lett 1993; 334: 175-182.
82. Wilcke M, Johannes L, Galli T, Mayau V, Goud B, Salamero J. Rab11 regulates the compartmentalization of early endosomes required for efficient transport from early endosomes to the trans-Golgi network. J Cell Biol 2000; 151: 1207-1220.
83. Cox D, Lee DJ, Dale BM, Calafat J, Greenberg S. A Rab11-containing rapidly recycling compartment in macrophages that promotes phagocytosis. Proc Natl Acad Sci USA 2000; 97: 680-685.
84. Horgan CP, Walsh M, Zurawski TH, McCaffrey MW. Rab11-FIP3 localises to a Rab11-positive pericentrosomal compartment during interphase and to the cleavage furrow during cytokinesis. Biochem Biophys Res Commun 2004; 319: 83-94.
85. McDonold CM, Fromme JC. Four GTPases differentially regulate the Sec7 Arf-GEF to direct traffic at the trans-Golgi network. Dev Cell 2014; 30: 759-767.
86. Kosugi S, Hasebe M, Matsumura N et al. Six classes of nuclear localization signals specific to different binding grooves of importin alpha. J Biol Chem 2009; 284: 478-485.
87. Jakel S, Gorlich D. Importin beta, transportin, RanBP5 and RanBP7 mediate nuclear import of ribosomal proteins in mammalian cells. EMBO J 1998; 17: 4491-4502.
88. Deng T, Engelhardt OG, Thomas B, Akoulitchev AV, Brownlee GG, Fodor E. Role of ran binding protein 5 in nuclear import and assembly of the influenza virus RNA polymerase complex. J Virol 2006; 80: 11911-11919.
89. Le Gouill C, Parent JL, Rola-Pleszczynski M, Stankova J. Structural and functional requirements for agonist-induced internalization of the human platelet-activating factor receptor. J Biol Chem 1997; 272: 21289-21295.
90. Rivera JC, Sitaras N, Noueihed B et al. Microglia and interleukin-1beta in ischemic retinopathy elicit microvascular degeneration through neuronal semaphorin-3A. Arterioscler Thromb Vasc Biol 2013; 33: 1881-1891.
91. Choudhury A, Dominguez M, Puri V et al. Rab proteins mediate Golgi transport of caveola-internalized glycosphingolipids and correct lipid trafficking in Niemann-Pick C cells. J Clin Invest 2002; 109: 1541-1550.
92. Cortes C, Rzomp KA, Tvinnereim A, Scidmore MA, Wizel B. Chlamydia pneumoniae inclusion membrane protein Cpn0585 interacts with multiple Rab GTPases. Infect Immun 2007; 75: 5586-5596.
93. Boussif O, Lezoualc'h F, Zanta MA et al. A versatile vector for gene and oligonucleotide transfer into cells in culture and in vivo: polyethylenimine. Proc Natl Acad Sci USA 1995; 92: 7297-7301.
94. Davies J, Jimenez A. A new selective agent for eukaryotic cloning vectors. Am J Trop Med Hyg 1980; 29: 1089-1092.
95. Bradford MM. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 1976; 72: 248-254.
96. Laemmli UK. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 1970; 227: 680-685.
97. Schneider CA, Rasband WS, Eliceiri KW. NIH Image to ImageJ: 25 years of image analysis. Nat Methods 2012; 9: 671-675.
98. Street IP, Lin HK, Laliberte F et al. Slow-and tight-binding inhibitors of the 85-kDa human phospholipase A2. Biochemistry 1993; 32: 5935-5940.
99. Reynolds LJ, Hughes LL, Yu L, Dennis EA. 1-Hexadecyl-2-arachidonoylthio-2-deoxy-sn-glycero-3-phosphorylcholine as a substrate for the microtiterplate assay of human cytosolic phospholipase A2. Anal Biochem 1994; 217: 25-32.
100. cPLA2 activity kit from Cayman Chemical. Available at: https://www. caymanchem. com/app/template/Product. vm/catalog/765021 (last accessed 30 November 2011).
101. Prakash YS, Pabelick CM, Kannan MS, Sieck GC. Spatial and temporal aspects of ACh-induced [Ca2+]i oscillations in porcine tracheal smooth muscle. Cell Calcium 2000; 27: 153-162.
102. Werry TD, Wilkinson GF, Willars GB. Mechanisms of cross-talk between G-protein-coupled receptors resulting in enhanced release of intracellular Ca2+. Biochem J 2003; 374: 281-296.
103. Rees DD, Palmer RM, Schulz R, Hodson HF, Moncada S. Characterization of three inhibitors of endothelial nitric oxide synthase in vitro and in vivo. Br J Pharmacol 1990; 101: 746-752.
104. Hirafuji M, Shinoda H. Platelet-leukocyte interaction in adhesion to endothelial cells induced by platelet-activating factor in vitro. Br J Pharmacol 1991; 103: 1333-1338.
105. Hirafuji M, Shinoda H. Antagonism of platelet-activating factor-induced increase in cytosolic free calcium concentration in human endothelial cells. Jpn J Pharmacol 1992; 58: 231-241.
106. Ye J, Coulouris G, Zaretskaya I, Cutcutache I, Rozen S, Madden TL. Primer-BLAST: a tool to design targetspecific primers for polymerase chain reaction. BMC Bioinform 2012; 13: 134.
107. Peri KG, Hardy P, Li DY, Varma DR, Chemtob S. Prostaglandin G/H synthase-2 is a major contributor of brain prostaglandins in the newborn. J Biol Chem 1995; 270: 24615-24620.
108. Li DY, Varma DR, Chemtob S. Up-regulation of brain PGE2 and PGF2 alpha receptors and receptor-coupled second messengers by cyclooxygenase inhibition in newborn pigs. J Pharmacol Exp Ther 1995; 272: 15-19.
109. Hellstrom A, Smith LE, Dammann O. Retinopathy of prematurity. Lancet 2013; 382: 1445-1457.
110. Stahl A, Connor KM, Sapieha P et al. Computer-aided quantification of retinal neovascularization. Angiogenesis 2009; 12: 297-301.
111. McDonald D, Carrero G, Andrin C, de Vries G, Hendzel MJ. Nucleoplasmic beta-actin exists in a dynamic equilibrium between low-mobility polymeric species and rapidly diffusing populations. JCell Biol 2006; 172: 541-552.
112. Bucci C, Parton RG, Mather IH et al. The small GTPase rab5 functions as a regulatory factor in the early endocytic pathway. Cell 1992; 70: 715-728.
113. Bucci C, Thomsen P, Nicoziani P, McCarthy J, van Deurs B. Rab7: a key to lysosome biogenesis. Mol Biol Cell 2000; 11: 467-480.
114. Garcia Rodriguez C, Cundell DR, Tuomanen EI, Kolakowski LF Jr, Gerard C, Gerard NP. The role of N-glycosylation for functional expression of the human platelet-activating factor receptor. Glycosylation is required for efficient membrane trafficking. J Biol Chem 1995; 270: 25178-25184.