Home LiteratureArticle Details
PMID: 20572141 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't

Bone vascularization and trabecular bone formation are mediated by PKB alpha/Akt1 in a gene-dosage-dependent manner: in vivo and ex vivo MRI.

Magnetic resonance in medicine ·Vol. 64 ·No. 1 ·2010-07-00 ·Pages 54-64

Vandoorne K, Magland J, Plaks V, Sharir A, Zelzer E, Wehrli F, Hemmings BA, Harmelin A, Neeman M

Abstract

PKBalpha/Akt1, a protein kinase, is a major mediator of angiogenic signaling. The purpose of this study was to determine the role of PKB alpha/Akt1 in bone vascularization and development. For that aim, macromolecular dynamic contrast enhanced MRI was applied to examine in vivo vascular changes in long bones of 40-day-old growing PKB alpha/Akt1-deficient, heterozygous, and wild-type mice. Ex vivo microMRI and microCT were applied to monitor the impact of PKB alpha/Akt1 gene dosage on trabecular bone formation during endochondral bone growth. PKB alpha/Akt1-deficient mice and, remarkably, also heterozygous mice showed significantly reduced blood volume fraction in the humerus compared to wild-type mice. Moreover, PKB alpha/Akt1-deficient mice showed a more severe vascular deficiency with reduced permeability. microCT and microMRI of trabeculae revealed impaired bone formation in both PKB alpha/Akt1-deficient and heterozygous mice, whereas cortical bone parameters were only reduced in PKB alpha/Akt1-deficient mice. Reduction of metaphyseal blood vessel invasion, concomitant with aberrant trabeculae and shorter long bones, demonstrates a gene-dose-dependent role for PKB alpha/Akt1 in regulation of overall size and endochondral bone growth. MRI proved to provide high sensitivity for in vivo detection of subtle gene dose effects leading to impaired bone vascularity and for uncovering changes in trabecular bone.

MeSH Terms
Animals Bone Density Gene Dosage Humerus/blood supply,diagnostic imaging,growth & development Immunohistochemistry Magnetic Resonance Imaging Mice Mice, Knockout Proto-Oncogene Proteins c-akt/genetics Radiography
Chemicals
Proto-Oncogene Proteins c-akt
Authors & Affiliations
9 authors, click to expand affiliations / ORCID
Vandoorne Katrien
Biological Regulation, The Weizmann Institute of Science, Rehovot, Israel.
Magland Jeremy
Plaks Vicki
Sharir Amnon
Zelzer Elazar
Wehrli Felix
Hemmings Brian A
Harmelin Alon
Neeman Michal
References (33)
33 references, click to expand
  1. Degradation of PKB/Akt protein by inhibition of the VEGF receptor/mTOR pathway in endothelial cells.
    Oncogene. 2004 Jun 3;23(26):4624-35 PMID: 15064712
  2. Tissue specific regulation of VEGF expression during bone development requires Cbfa1/Runx2.
    Mech Dev. 2001 Aug;106(1-2):97-106 PMID: 11472838
  3. Bone development.
    Annu Rev Cell Dev Biol. 2000;16:191-220 PMID: 11031235
  4. Overexpression of vascular endothelial growth factor 165 drives peritumor interstitial convection and induces lymphatic drain: magnetic resonance imaging, confocal microscopy, and histological tracking of triple-labeled albumin.
    Cancer Res. 2002 Nov 15;62(22):6731-9 PMID: 12438274
  5. Macromolecular dynamic contrast-enhanced (DCE)-MRI detects reduced vascular permeability in a prostate cancer bone metastasis model following anti-platelet-derived growth factor receptor (PDGFR) therapy, indicating a drop in vascular endothelial growth factor receptor (VEGFR) activation.
    Magn Reson Med. 2008 Oct;60(4):822-33 PMID: 18816866
  6. Modulation of the pharmacokinetics of macromolecular contrast material by avidin chase: MRI, optical, and inductively coupled plasma mass spectrometry tracking of triply labeled albumin.
    Magn Reson Med. 2003 Nov;50(5):904-14 PMID: 14587000
  7. Akt1 in osteoblasts and osteoclasts controls bone remodeling.
    PLoS One. 2007 Oct 24;2(10):e1058 PMID: 17957242
  8. Skeletal defects in VEGF(120/120) mice reveal multiple roles for VEGF in skeletogenesis.
    Development. 2002 Apr;129(8):1893-904 PMID: 11934855
  9. Lymphatics and bone.
    Hum Pathol. 2008 Jan;39(1):49-55 PMID: 17904616
  10. Topology-based orientation analysis of trabecular bone networks.
    Med Phys. 2003 Feb;30(2):158-68 PMID: 12607833
  11. Akt1/PKBalpha is required for normal growth but dispensable for maintenance of glucose homeostasis in mice.
    J Biol Chem. 2001 Oct 19;276(42):38349-52 PMID: 11533044
  12. Bone marrow angiogenesis magnetic resonance imaging in patients with acute myeloid leukemia: peak enhancement ratio is an independent predictor for overall survival.
    Blood. 2009 Apr 2;113(14):3161-7 PMID: 18988863
  13. VEGF couples hypertrophic cartilage remodeling, ossification and angiogenesis during endochondral bone formation.
    Nat Med. 1999 Jun;5(6):623-8 PMID: 10371499
  14. The genetic transformation of bone biology.
    Genes Dev. 1999 Dec 1;13(23):3037-51 PMID: 10601030
  15. The role of Akt1 in terminal stages of endochondral bone formation: angiogenesis and ossification.
    Bone. 2009 Dec;45(6):1133-45 PMID: 19679212
  16. Longitudinal MRI tracking of the angiogenic response to hind limb ischemic injury in the mouse.
    Magn Reson Med. 2004 Feb;51(2):304-11 PMID: 14755656
  17. Expression of VEGF121 and VEGF165 in hypertrophic chondrocytes of the human growth plate and epiphyseal cartilage.
    J Anat. 2002 Aug;201(2):153-7 PMID: 12220123
  18. Growth retardation and increased apoptosis in mice with homozygous disruption of the Akt1 gene.
    Genes Dev. 2001 Sep 1;15(17):2203-8 PMID: 11544177
  19. VEGFA is necessary for chondrocyte survival during bone development.
    Development. 2004 May;131(9):2161-71 PMID: 15073147
  20. Imaging anti-angiogenic treatment response with DCE-VCT, DCE-MRI and DWI in an animal model of breast cancer bone metastasis.
    Eur J Radiol. 2010 Feb;73(2):280-7 PMID: 19070445
  21. ZD6474 inhibits vascular endothelial growth factor signaling, angiogenesis, and tumor growth following oral administration.
    Cancer Res. 2002 Aug 15;62(16):4645-55 PMID: 12183421
  22. Multiple roles of vascular endothelial growth factor (VEGF) in skeletal development, growth, and repair.
    Curr Top Dev Biol. 2005;65:169-87 PMID: 15642383
  23. MRI and fluorescence microscopy of the acute vascular response to VEGF165: vasodilation, hyper-permeability and lymphatic uptake, followed by rapid inactivation of the growth factor.
    NMR Biomed. 2002 Apr;15(2):120-31 PMID: 11870908
  24. Angiogenesis and bone growth.
    Trends Cardiovasc Med. 2000 Jul;10(5):223-8 PMID: 11282299
  25. Acute hematogenous osteomyelitis in children: recognition and management.
    Paediatr Drugs. 2004;6(6):333-46 PMID: 15612835
  26. Dynamic contrast-enhanced MRI in Paget's disease of bone--correlation of regional microcirculation and bone turnover.
    Eur Radiol. 2008 May;18(5):1005-11 PMID: 18175121
  27. MRI analysis of angiogenesis during mouse embryo implantation.
    Magn Reson Med. 2006 May;55(5):1013-22 PMID: 16598729
  28. Angiogenesis in ectopic ovarian xenotransplantation: multiparameter characterization of the neovasculature by dynamic contrast-enhanced MRI.
    Magn Reson Med. 2004 Oct;52(4):741-50 PMID: 15389965
  29. Dosage-dependent effects of Akt1/protein kinase Balpha (PKBalpha) and Akt3/PKBgamma on thymus, skin, and cardiovascular and nervous system development in mice.
    Mol Cell Biol. 2005 Dec;25(23):10407-18 PMID: 16287854
  30. Osteogenesis and angiogenesis: the potential for engineering bone.
    Eur Cell Mater. 2008 May 02;15:100-14 PMID: 18454418
  31. Protein kinase B alpha/Akt1 regulates placental development and fetal growth.
    J Biol Chem. 2003 Aug 22;278(34):32124-31 PMID: 12783884
  32. Impaired angiogenesis and endochondral bone formation in mice lacking the vascular endothelial growth factor isoforms VEGF164 and VEGF188.
    Mech Dev. 2002 Feb;111(1-2):61-73 PMID: 11804779
  33. Akt1 regulates pathological angiogenesis, vascular maturation and permeability in vivo.
    Nat Med. 2005 Nov;11(11):1188-96 PMID: 16227992
Article Info
Journal
Magnetic resonance in medicine
Abbr.
Magn Reson Med
ISSN
1522-2594
Published
2010-07-00
Pages
54-64
Language
English
Region
United States
NLM ID
8505245
PMCID
PMC3558735
Subset
IM
Grants
European Research Council · 232640 · International
Analysis Services
Analysis Services

Contact

No. 2 Wenbo Road, Zhangqiu District, Jinan, Shandong

Qilu Normal University · Genelibs Bioinformatics Lab

750 Shunhua Rd, Jinan

2F, Bldg F, University Science Park

Tel: 0531-88819269

WeChat Official Account

Follow our WeChat subscription account for real-time updates and the latest in medical and biological research.


Business Email

E-mail: [email protected]