Biomechanical Force in Blood Development: Extrinsic Physical Cues Drive Pro-hematopoietic Signaling

Overview

Journal Differentiation

Publisher Elsevier

Specialties Cell Biology
Reproductive Medicine

Date 2013 Jul 16

PMID 23850217

Citations 29

Authors

Hyun Jung Lee

Nan Li

Siobahn M Evans

Miguel F Diaz

Pamela L Wenzel

Affiliations

Soon will be listed here.

Abstract

The hematopoietic system is dynamic during development and in adulthood, undergoing countless spatial and temporal transitions during the course of one's life. Microenvironmental cues in the many unique hematopoietic niches differ, characterized by distinct soluble molecules, membrane-bound factors, and biophysical features that meet the changing needs of the blood system. Research from the last decade has revealed the importance of substrate elasticity and biomechanical force in determination of stem cell fate. Our understanding of the role of these factors in hematopoiesis is still relatively poor; however, the developmental origin of blood cells from the endothelium provides a model for comparison. Many endothelial mechanical sensors and second messenger systems may also determine hematopoietic stem cell fate, self renewal, and homing behaviors. Further, the intimate contact of hematopoietic cells with mechanosensitive cell types, including osteoblasts, endothelial cells, mesenchymal stem cells, and pericytes, places them in close proximity to paracrine signaling downstream of mechanical signals. The objective of this review is to present an overview of the sensors and intracellular signaling pathways activated by mechanical cues and highlight the role of mechanotransductive pathways in hematopoiesis.

Citing Articles

Mechanobiology and Primary Cilium in the Pathophysiology of Bone Marrow Myeloproliferative Diseases.

Tiberio F, Coda A, Tosi D, Luzi D, Polito L, Liso A Int J Mol Sci. 2024; 25(16).

PMID: 39201546 PMC: 11354938. DOI: 10.3390/ijms25168860.

The spatiotemporal heterogeneity of the biophysical microenvironment during hematopoietic stem cell development: from embryo to adult.

Shi G, Zhang P, Zhang X, Li J, Zheng X, Yan J Stem Cell Res Ther. 2023; 14(1):251.

PMID: 37705072 PMC: 10500792. DOI: 10.1186/s13287-023-03464-8.

Pumping up the blood progenitors by Piezo.

Kapoor A, Kumar A, Mukherjee T Proc Natl Acad Sci U S A. 2023; 120(23):e2306004120.

PMID: 37228115 PMC: 10265945. DOI: 10.1073/pnas.2306004120.

De Novo Generation of Human Hematopoietic Stem Cells from Pluripotent Stem Cells for Cellular Therapy.

Ding J, Li Y, Larochelle A Cells. 2023; 12(2).

PMID: 36672255 PMC: 9857267. DOI: 10.3390/cells12020321.

Enhancing Mesenchymal Stromal Cell Potency: Inflammatory Licensing Mechanotransduction.

Skibber M, Olson S, Prabhakara K, Gill B, Cox Jr C Front Immunol. 2022; 13:874698.

PMID: 35874742 PMC: 9297916. DOI: 10.3389/fimmu.2022.874698.

References

Gibb D, El Shikh M, Kang D, Rowe W, Sayed R, Cichy J . ADAM10 is essential for Notch2-dependent marginal zone B cell development and CD23 cleavage in vivo. J Exp Med. 2010; 207(3):623-35. PMC: 2839139. DOI: 10.1084/jem.20091990. View

Larsen M, Artym V, Green J, Yamada K . The matrix reorganized: extracellular matrix remodeling and integrin signaling. Curr Opin Cell Biol. 2006; 18(5):463-71. DOI: 10.1016/j.ceb.2006.08.009. View

Kissa K, Herbomel P . Blood stem cells emerge from aortic endothelium by a novel type of cell transition. Nature. 2010; 464(7285):112-5. DOI: 10.1038/nature08761. View

Brayden J, Earley S, Nelson M, Reading S . Transient receptor potential (TRP) channels, vascular tone and autoregulation of cerebral blood flow. Clin Exp Pharmacol Physiol. 2008; 35(9):1116-20. PMC: 4193799. DOI: 10.1111/j.1440-1681.2007.04855.x. View

Zaslona Z, Serezani C, Okunishi K, Aronoff D, Peters-Golden M . Prostaglandin E2 restrains macrophage maturation via E prostanoid receptor 2/protein kinase A signaling. Blood. 2012; 119(10):2358-67. PMC: 3311259. DOI: 10.1182/blood-2011-08-374207. View

North T, Gu T, Stacy T, Wang Q, Howard L, Binder M . Cbfa2 is required for the formation of intra-aortic hematopoietic clusters. Development. 1999; 126(11):2563-75. DOI: 10.1242/dev.126.11.2563. View

Ranjan V, Xiao Z, Diamond S . Constitutive NOS expression in cultured endothelial cells is elevated by fluid shear stress. Am J Physiol. 1995; 269(2 Pt 2):H550-5. DOI: 10.1152/ajpheart.1995.269.2.H550. View

Koshida R, Rocic P, Saito S, Kiyooka T, Zhang C, Chilian W . Role of focal adhesion kinase in flow-induced dilation of coronary arterioles. Arterioscler Thromb Vasc Biol. 2005; 25(12):2548-53. DOI: 10.1161/01.ATV.0000188511.84138.9b. View

Armeanu S, Buhring H, Reuss-Borst M, Muller C, Klein G . E-cadherin is functionally involved in the maturation of the erythroid lineage. J Cell Biol. 1995; 131(1):243-9. PMC: 2120602. DOI: 10.1083/jcb.131.1.243. View

10.

Krasnov P, Michurina T, Packer M, Stasiv Y, Nakaya N, Moore K . Neuronal nitric oxide synthase contributes to the regulation of hematopoiesis. Mol Med. 2007; 14(3-4):141-9. PMC: 2140250. DOI: 10.2119/2007-00011.Krasnov. View

11.

Pelling A, Horton M . An historical perspective on cell mechanics. Pflugers Arch. 2007; 456(1):3-12. DOI: 10.1007/s00424-007-0405-1. View

12.

Medvinsky A, Rybtsov S, Taoudi S . Embryonic origin of the adult hematopoietic system: advances and questions. Development. 2011; 138(6):1017-31. DOI: 10.1242/dev.040998. View

13.

Ranheim E, Kwan H, Reya T, Wang Y, Weissman I, Francke U . Frizzled 9 knock-out mice have abnormal B-cell development. Blood. 2004; 105(6):2487-94. DOI: 10.1182/blood-2004-06-2334. View

14.

Takada Y, Kato C, Kondo S, Korenaga R, Ando J . Cloning of cDNAs encoding G protein-coupled receptor expressed in human endothelial cells exposed to fluid shear stress. Biochem Biophys Res Commun. 1997; 240(3):737-41. DOI: 10.1006/bbrc.1997.7734. View

15.

Ciau-Uitz A, Liu F, Patient R . Genetic control of hematopoietic development in Xenopus and zebrafish. Int J Dev Biol. 2010; 54(6-7):1139-49. DOI: 10.1387/ijdb.093055ac. View

16.

Weber S, Saftig P . Ectodomain shedding and ADAMs in development. Development. 2012; 139(20):3693-709. DOI: 10.1242/dev.076398. View

17.

Huber M, Azoitei N, Baumann B, Grunert S, Sommer A, Pehamberger H . NF-kappaB is essential for epithelial-mesenchymal transition and metastasis in a model of breast cancer progression. J Clin Invest. 2004; 114(4):569-81. PMC: 503772. DOI: 10.1172/JCI21358. View

18.

Kiel M, Acar M, Radice G, Morrison S . Hematopoietic stem cells do not depend on N-cadherin to regulate their maintenance. Cell Stem Cell. 2009; 4(2):170-9. PMC: 2681089. DOI: 10.1016/j.stem.2008.10.005. View

19.

Iida A, Sakaguchi K, Sato K, Sakurai H, Nishimura D, Iwaki A . Metalloprotease-dependent onset of blood circulation in zebrafish. Curr Biol. 2010; 20(12):1110-6. DOI: 10.1016/j.cub.2010.04.052. View

20.

Even-Ram S, Artym V, Yamada K . Matrix control of stem cell fate. Cell. 2006; 126(4):645-7. DOI: 10.1016/j.cell.2006.08.008. View