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Mechanotransduction in embryonic vascular development

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Abstract

A plethora of biochemical signals provides spatial and temporal cues that carefully orchestrate the complex process of vertebrate embryonic development. The embryonic vasculature develops not only in the context of these biochemical cues, but also in the context of the biomechanical forces imparted by blood flow. In the mature vasculature, different blood flow regimes induce distinct genetic programs, and significant progress has been made toward understanding how these forces are perceived by endothelial cells and transduced into biochemical signals. However, it cannot be assumed that paradigms that govern the mature vasculature are pertinent to the developing embryonic vasculature. The embryonic vasculature can respond to the mechanical forces of blood flow, and these responses are critical in vascular remodeling, certain aspects of sprouting angiogenesis, and maintenance of arterial–venous identity. Here, we review data regarding mechanistic aspects of endothelial cell mechanotransduction, with a focus on the response to shear stress, and elaborate upon the multifarious effects of shear stress on the embryonic vasculature. In addition, we discuss emerging predictive vascular growth models and highlight the prospect of combining signaling pathway information with computational modeling. We assert that correlation of precise measurements of hemodynamic parameters with effects on endothelial cell gene expression and cell behavior is required for fully understanding how blood flow-induced loading governs normal vascular development and shapes congenital cardiovascular abnormalities.

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Abbreviations

Alk1:

Activin receptor-like kinase 1

AP-1:

Activator protein-1

ASS:

Argininosuccinate synthase

ATF-2:

Activating transcription factor-2

CBP:

CREB-binding protein

DLAV:

Dorsal longitudinal anastamotic vessel

DLL4:

Delta-like 4

EDHF:

Endothelial-derived hyperpolarizing factor

EDN:

Endothelin

eNOS:

Endothelial nitric oxide synthase

ERK:

Extracellular signal-related kinase

HDAC:

Histone deacetylase

HH:

Hamburger–Hamilton

HMOX-1:

Heme oxygenase-1

ICAM-1:

Intracellular adhesion molecule

IκB:

Inhibitor of κB

IKK:

IκB kinase

ISV:

Intersegmental vessel

Jag:

Jagged

JNK:

Jun kinase

KLF:

Krüppel-like factor

MAPK:

Mitogen-activated protein kinase

MCP-1:

Macrophage chemotactic protein-1

MEF:

Myocyte enhancer factor

MEK:

Mitogen-activated protein kinase kinase

miR:

MicroRNA

NF-κB:

Nuclear factor kappa B

NIK:

NF-κB-inducing kinase

NO:

Nitric oxide

NRF-2:

Nuclear factor erythroid 2-related factor 2

NRP:

Neuropilin

PECAM-1:

Platelet endothelial cell adhesion molecule

PI3K:

Phosphatidyl inositol-3-kinase

PPAR:

Peroxisome proliferator-activated receptor

PTGDS:

Prostaglandin D2 synthase

RB:

Retinoblastoma protein

RISC:

RNA-induced silencing complex

RPSI:

Relative pulse slope index

RUNX1:

Runt-related transcription factor 1

SELE:

E-selectin

TNNT2:

Cardiac troponin T2

VCAM-1:

Vascular cell adhesion molecule-1

VECAD:

Vascular endothelial cadherin

VEGFR2:

Vascular endothelial growth factor receptor 2

βTRC:

Beta-transducin repeat-containing protein

WSS:

Wall shear stress

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  1. Department of Biological Sciences, University of Pittsburgh, Pittsburgh, PA, USA

    Beth L. Roman

  2. Departments of Biomedical and Mechanical Engineering, Carnegie Mellon University, 700 Technology Drive, Pittsburgh, PA, USA

    Kerem Pekkan

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Funding: R01HL079108 (awarded to B.L.R.) and American Heart Association 0765284U and NSF CAREER 0954465 (awarded to K.P.).

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Roman, B.L., Pekkan, K. Mechanotransduction in embryonic vascular development. Biomech Model Mechanobiol 11, 1149–1168 (2012). https://doi.org/10.1007/s10237-012-0412-9

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