Akt/protein kinase B is required for lymphatic network formation, remodeling, and valve development

American Journal of Pathology

Volumn 177, Issue 4, 2010, Pages 2124-2133

  Zhou, Fei ^a   Chang, Zai ^a   Zhang, Luqing ^a   Hong, Young Kwon ^b   Shen, Bin ^a   Wang, Bo ^a   Zhang, Fan ^a   Lu, Guangming ^a   Tvorogov, Denis ^c   Alitalo, Kari ^c   Hemmings, Brian A ^d   Yang, Zhongzhou ^a   He, Yulong ^a  

^a NANJING UNIVERSITY   (China)

^b UNIVERSITY OF SOUTHERN CALIFORNIA   (United States)

^c HELSINKI UNIVERSITY CENTRAL HOSPITAL   (Finland)

^d FRIEDRICH MIESCHER INSTITUTE FOR BIOMEDICAL RESEARCH   (Switzerland)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOVIRUS VECTOR; PROTEIN KINASE B; VASCULOTROPIN C;

ANGIOGENESIS; ANIMAL CELL; ARTICLE; CELL PROLIFERATION; CONTROLLED STUDY; ENDOTHELIUM CELL; HISTOPATHOLOGY; IMMUNOHISTOCHEMISTRY; KNOCKOUT MOUSE; LYMPHANGIOGENESIS; LYMPHANGIOGRAPHY; MOUSE; NONHUMAN; PRIORITY JOURNAL; SIGNAL TRANSDUCTION; WESTERN BLOTTING; WILD TYPE;

EID: 77957365795     PISSN: 00029440     EISSN: 15252191     Source Type: Journal    
DOI: 10.2353/ajpath.2010.091301     Document Type: Article

References (56)

1. Adams RH, Alitalo K: Molecular regulation of angiogenesis and lymphangiogenesis. Nat Rev Mol Cell Biol 2007, 8:464-478
2. Alitalo K, Tammela T, Petrova TV: Lymphangiogenesis in development and human disease. Nature 2005, 438:946-953
3. Oliver G, Detmar M: The rediscovery of the lymphatic system: old and new insights into the development and biological function of the lymphatic vasculature. Genes Dev 2002, 16:773-783
4. He Y, Karpanen T, Alitalo K: Role of lymphangiogenic factors in tumor metastasis. Biochim Biophys Acta 2004, 1654:3-12
5. Cueni LN, Detmar M: New insights into the molecular control of the lymphatic vascular system and its role in disease. J Invest Dermatol 2006, 126:2167-2177
6. Baluk P, McDonald DM: Markers for microscopic imaging of lymphangiogenesis and angiogenesis. Ann NY Acad Sci 2008, 1131:1-12
7. Wigle JT, Oliver G: Prox1 function is required for the development of the murine lymphatic system. Cell 1999, 98:769-778
8. Wigle JT, Harvey N, Detmar M, Lagutina I, Grosveld G, Gunn MD, Jackson DG, Oliver G: An essential role for Prox1 in the induction of the lymphatic endothelial cell phenotype. EMBO J 2002, 21:1505-1513 (Pubitemid 34614607)
9. Françcois M, Caprini A, Hosking B, Orsenigo F, Wilhelm D, Browne C, Paavonen K, Karnezis T, Shayan R, Downes M, Davidson T, Tutt D, Cheah KS, Stacker SA, Muscat GE, Achen MG, Dejana E, Koopman P: Sox18 induces development of the lymphatic vasculature in mice. Nature 2008, 456:643-647
10. Mäkinen T, Jussila L, Veikkola T, Karpanen T, Kettunen MI, Pulkkanen KJ, Kauppinen R, Jackson DG, Kubo H, Nishikawa S, Yla-Herttuala S, Alitalo K: Inhibition of lymphangiogenesis with resulting lymphedema in transgenic mice expressing soluble VEGF receptor-3. Nat Med 2001, 7:199-205
11. Karkkainen MJ, Haiko P, Sainio K, Partanen J, Taipale J, Petrova TV, Jeltsch M, Jackson DG, Talikka M, Rauvala H, Betsholtz C, Alitalo K: Vascular endothelial growth factor C is required for sprouting of the first lymphatic vessels from embryonic veins. Nat Immunol 2004, 5:74-80
12. Dummler B, Hemmings BA: Physiological roles of PKB/Akt isoforms in development and disease. Biochem Soc Trans 2007, 35:231-235
13. Shiojima I, Walsh K: Regulation of cardiac growth and coronary angiogenesis by the Akt/PKB signaling pathway. Genes Dev 2006, 20:3347-3365
14. Brazil DP, Yang ZZ, Hemmings BA: Advances in protein kinase B signalling: aKTion on multiple fronts. Trends Biochem Sci 2004, 29:233-242
15. Kim I, Kim HG, So JN, Kim JH, Kwak HJ, Koh GY: Angiopoietin-1 regulates endothelial cell survival through the phosphatidylinositol 3′-kinase/Akt signal transduction pathway. Circ Res 2000, 86:24-29
16. Gerber HP, McMurtrey A, Kowalski J, Yan M, Keyt BA, Dixit V, Ferrara N: Vascular endothelial growth factor regulates endothelial cell survival through the phosphatidylinositol 3′-kinase/Akt signal transduction pathway. Requirement for Flk-1/KDR activation, J Biol Chem 1998, 273:30336-30343
17. Fujio Y, Walsh K: Akt mediates cytoprotection of endothelial cells by vascular endothelial growth factor in an anchorage-dependent manner. J Biol Chem 1999, 274:16349-16354
18. Papapetropoulos A, Fulton D, Mahboubi K, Kalb RG, O'Connor DS, Li F, Altieri DC, Sessa WC: Angiopoietin-1 inhibits endothelial cell apoptosis via the Akt/survivin pathway. J Biol Chem 2000, 275:9102-9105
19. Chan J, Bayliss PE, Wood JM, Roberts TM: Dissection of angiogenic signaling in zebrafish using a chemical genetic approach. Cancer Cell 2002, 1:257-267
20. Jiang BH, Zheng JZ, Aoki M, Vogt PK: Phosphatidylinositol 3-kinase signaling mediates angiogenesis and expression of vascular endothelial growth factor in endothelial cells, Proc Natl Acad Sci USA 2000, 97:1749-1753
21. Shiojima I, Walsh K: Role of Akt signaling in vascular homeostasis and angiogenesis. Circ Res 2002, 90:1243-1250
22. Chen J, Somanath PR, Razorenova O, Chen WS, Hay N, Bornstein P, Byzova TV: Akt1 regulates pathological angiogenesis, vascular maturation and permeability in vivo. Nat Med 2005, 11:1188-1196
23. Fruman DA, Mauvais-Jarvis F, Pollard DA, Yballe CM, Brazil D, Bronson RT, Kahn CR, Cantley LC: Hypoglycaemia, liver necrosis and perinatal death in mice lacking all isoforms of phosphoinositide 3-kinase p85α. Nat Genet 2000, 26:379-382
24. Mouta-Bellum C, Kirov A, Miceli-Libby L, Mancini ML, Petrova TV, Liaw L, Prudovsky I, Thorpe PE, Miura N, Cantley LC, Alitalo K, Fruman DA, Vary CP: Organ-specific lymphangiectasia, arrested lymphatic sprouting, and maturation defects resulting from gene-targeting of the PI3K regulatory isoforms p85α, p55α, and p50α. Dev Dyn 2009, 238:2670-2679
25. Yang ZZ, Tschopp O, Hemmings-Mieszczak M, Feng J, Brodbeck D, Perentes E, Hemmings BA: Protein kinase Bα/Akt1 regulates placental development and fetal growth. J Biol Chem 2003, 278:32124-32131
26. Tschopp O, Yang ZZ, Brodbeck D, Dummler BA, Hemmings-Mieszczak M, Watanabe T, Michaelis T, Frahm J, Hemmings BA: Essential role of protein kinase Bγ(PKBγ/Akt3) in postnatal brain development but not in glucose homeostasis. Development 2005, 132:2943-2954
27. Dummler B, Tschopp O, Hynx D, Yang ZZ, Dirnhofer S, Hemmings BA: Life with a single isoform of Akt: mice lacking Akt2 and Akt3 are viable but display impaired glucose homeostasis and growth deficiencies. Mol Cell Biol 2006, 26:8042-8051
28. Lee S, Kang J, Yoo J, Ganesan SK, Cook SC, Aguilar B, Ramu S, Lee J, Hong YK: Prox1 physically and functionally interacts with COUP-TFII to specify lymphatic endothelial cell fate. Blood 2009, 113:1856-1859
29. Tammela T, He Y, Lyytikka J, Jeltsch M, Markkanen J, Pajusola K, Yla-Herttuala S, Alitalo K: Distinct architecture of lymphatic vessels induced by chimeric vascular endothelial growth factor-C/vascular endothelial growth factor heparin-binding domain fusion proteins. Circ Res 2007, 100:1468-1475
30. Banerji S, Ni J, Wang SX, Clasper S, Su J, Tammi R, Jones M, Jackson DG: LYVE-1, a new homologue of the CD44 glycoprotein, is a lymph-specific receptor for hyaluronan. J Cell Biol 1999, 144:789-801
31. Bazigou E, Xie S, Chen C, Weston A, Miura N, Sorokin L, Adams R, Muro AF, Sheppard D, Makinen T: Integrin-α9 is required for fibronectin matrix assembly during lymphatic valve morphogenesis. Dev Cell 2009, 17:175-186
32. Yang ZZ, Tschopp O, Di-Poi N, Bruder E, Baudry A, Dummler B, Wahli W, Hemmings BA: Dosage-dependent effects of Akt1/protein kinase Bα (PKBα) and Akt3/PKBγ on thymus, skin, and cardiovascular and nervous system development in mice. Mol Cell Biol 2005, 25:10407-10418
33. Peng XD, Xu PZ, Chen ML, Hahn-Windgassen A, Skeen J, Jacobs J, Sundararajan D, Chen WS, Crawford SE, Coleman KG, Hay N: Dwarfism, impaired skin development, skeletal muscle atrophy, delayed bone development, and impeded adipogenesis in mice lacking Akt1 and Akt2. Genes Dev 2003, 17:1352-1365
34. Jones PF, Jakubowicz T, Hemmings BA: Molecular cloning of a second form of rac protein kinase. Cell Regul 1991, 2:1001-1009
35. Altomare DA, Guo K, Cheng JQ, Sonoda G, Walsh K, Testa JR: Cloning, chromosomal localization and expression analysis of the mouse Akt2 oncogene. Oncogene 1995, 11:1055-1060
36. Brodbeck D, Cron P, Hemmings BA: A human protein kinase Bγ with regulatory phosphorylation sites in the activation loop and in the C-terminal hydrophobic domain. J Biol Chem 1999, 274:9133-9136
37. Nakatani K, Sakaue H, Thompson DA, Weigel RJ, Roth RA: Identification of a human Akt3 (protein kinase Bγ) which contains the regulatory serine phosphorylation site. Biochem Biophys Res Commun 1999, 257:906-910
38. Bellacosa A, Franke TF, Gonzalez-Portal ME, Datta K, Taguchi T, Gardner J, Cheng JQ, Testa JR, Tsichlis PN: Structure, expression and chromosomal mapping of c-akt: relationship to v-akt and its implications. Oncogene 1993, 8:745-754
39. Dimmeler S, Fleming I, Fisslthaler B, Hermann C, Busse R, Zeiher AM: Activation of nitric oxide synthase in endothelial cells by Akt-dependent phosphorylation. Nature 1999, 399:601-605
40. Fulton D, Gratton JP, McCabe TJ, Fontana J, Fujio Y, Walsh K, Franke TF, Papapetropoulos A, Sessa WC: Regulation of endothelium-derived nitric oxide production by the protein kinase Akt. Nature 1999, 399:597-601
41. Dixit M, Loot AE, Mohamed A, Fisslthaler B, Boulanger CM, Ceacareanu B, Hassid A, Busse R, Fleming I: Gab1, SHP2, and protein kinase A are crucial for the activation of the endothelial NO synthase by fluid shear stress, Circ Res 2005, 97:1236-1244
42. Lawlor MA, Alessi DR: PKB/Akt: a key mediator of cell proliferation, survival and insulin responses?. J Cell Sci 2001, 114:2903-2910
43. Gale N, Thurston G, Hackett S, Renard R, Wang Q, McClain J, Martin C, Witte C, Witte M, Jackson D, Suri C, Campochiaro P, Wiegand S, Yancopoulos G: Angiopoietin-2 is required for postnatal angiogenesis and lymphatic patterning, and only the latter role is rescued by angiopoietin-1. Dev Cell 2002, 3:411-423
44. Mäkinen T, Adams RH, Bailey J, Lu Q, Ziemiecki A, Alitalo K, Klein R, Wilkinson GA: PDZ interaction site in ephrinB2 is required for the remodeling of lymphatic vasculature. Genes Dev 2005, 19:397-410
45. Petrova TV, Karpanen T, Norrmen C, Mellor R, Tamakoshi T, Finegold D, Ferrell R, Kerjaschki D, Mortimer P, Yla-Herttuala S, Miura N, Alitalo K: Defective valves and abnormal mural cell recruitment underlie lymphatic vascular failure in lymphedema distichiasis. Nat Med 2004, 10:974-981
46. Hellström M, Kalen M, Lindahl P, Abramsson A, Betsholtz C: Role of PDGF-B and PDGFR-β in recruitment of vascular smooth muscle cells and pericytes during embryonic blood vessel formation in the mouse. Development 1999, 126:3047-3055
47. Suri C, Jones PF, Patan S, Bartunkova S, Maisonpierre PC, Davis S, Sato TN, Yancopoulos GD: Requisite role of angiopoietin-1, a ligand for the TIE2 receptor, during embryonic angiogenesis. Cell 1996, 87:1171-1180
48. Kumar SR, Singh J, Xia G, Krasnoperov V, Hassanieh L, Ley EJ, Scehnet J, Kumar NG, Hawes D, Press MF, Weaver FA, Gill PS: Receptor tyrosine kinase EphB4 is a survival factor in breast cancer. Am J Pathol 2006, 169:279-293
49. Adams RH, Wilkinson GA, Weiss C, Diella F, Gale NW, Deutsch U, Risau W, Klein R: Roles of ephrinB ligands and EphB receptors in cardiovascular development: demarcation of arterial/venous domains, vascular morphogenesis, and sprouting angiogenesis. Genes Dev 1999, 13:295-306
50. Wang HU, Chen ZF, Anderson DJ: Molecular distinction and angiogenic interaction between embryonic arteries and veins revealed by ephrin-B2 and its receptor Eph-B4. Cell 1998, 93:741-753
51. Shworak NW: Angiogenic modulators in valve development and disease: does valvular disease recapitulate developmental signaling pathways?. Curr Opin Cardiol 2004, 19:140-146
52. Ackah E, Yu J, Zoellner S, Iwakiri Y, Skurk C, Shibata R, Ouchi N, Easton RM, Galasso G, Birnbaum MJ, Walsh K, Sessa WC: Akt1/protein kinase Bβ is critical for ischemic and VEGF-mediated angiogenesis. J Clin Invest 2005, 115:2119-2127
53. Cho H, Thorvaldsen JL, Chu Q, Feng F, Birnbaum MJ: Akt1/PKBα is required for normal growth but dispensable for maintenance of glucose homeostasis in mice. J Biol Chem 2001, 276:38349-38352
54. Chen WS, Xu PZ, Gottlob K, Chen ML, Sokol K, Shiyanova T, Roninson I, Weng W, Suzuki R, Tobe K, Kadowaki T, Hay N: Growth retardation and increased apoptosis in mice with homozygous disruption of the Akt1 gene. Genes Dev 2001, 15:2203-2208
55. Petrova TV, Makinen T, Makela TP, Saarela J, Virtanen I, Ferrell RE, Finegold DN, Kerjaschki D, Yla-Herttuala S, Alitalo K: Lymphatic endothelial reprogramming of vascular endothelial cells by the Prox-1 homeobox transcription factor. EMBO J 2002, 21:4593-4599
56. Hirakawa S, Hong YK, Harvey N, Schacht V, Matsuda K, Libermann T, Detmar M: Identification of vascular lineage-specific genes by transcriptional profiling of isolated blood vascular and lymphatic endothelial cells. Am J Pathol 2003, 162:575-586