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Mechanobiology and Vascular Remodeling: From Membrane to Nucleus

  • Ying-Xin Qi
  • Yue Han
  • Zong-Lai Jiang
Chapter
Part of the Advances in Experimental Medicine and Biology book series (AEMB, volume 1097)

Abstract

Vascular endothelial cells (ECs) and smooth muscle cells (VSMCs) are constantly exposed to hemodynamic forces in vivo, including flow shear stress and cyclic stretch caused by the blood flow. Numerous researches revealed that during various cardiovascular diseases such as atherosclerosis, hypertension, and vein graft, abnormal (pathological) mechanical forces play crucial roles in the dysfunction of ECs and VSMCs, which is the fundamental process during both vascular homeostasis and remodeling. Hemodynamic forces trigger several membrane molecules and structures, such as integrin, ion channel, primary cilia, etc., and induce the cascade reaction processes through complicated cellular signaling networks. Recent researches suggest that nuclear envelope proteins act as the functional homology of molecules on the membrane, are important mechanosensitive molecules which modulate chromatin location and gene transcription, and subsequently regulate cellular functions. However, the studies on the roles of nucleus in the mechanotransduction process are still at the beginning. Here, based on the recent researches, we focused on the nuclear envelope proteins and discussed the roles of pathological hemodynamic forces in vascular remodeling. It may provide new insight into understanding the molecular mechanism of vascular physiological homeostasis and pathophysiological remodeling and may help to develop hemodynamic-based strategies for the prevention and management of vascular diseases.

Notes

Acknowledgments

Work in our laboratory is supported by grants from the National Natural Science Foundation of China (Nos. 11625209, 11572199, and 11232010).

References

  1. AbouAlaiwi WA, Takahashi M, Mell BR, Jones TJ, Ratnam S, Kolb RJ, Nauli SM (2009) Ciliary polycystin-2 is a mechanosensitive calcium channel involved in nitric oxide signaling cascades. Circ Res 104(7):860–869CrossRefGoogle Scholar
  2. Anwar MA, Shalhoub J, Lim CS, Gohel MS, Davies AH (2012) The effect of pressure-induced mechanical stretch on vascular wall differential gene expression. J Vasc Res 49(6):463–478CrossRefGoogle Scholar
  3. Aureille J, Belaadi N, Guilluy C (2017) Mechanotransduction via the nuclear envelope: a distant reflection of the cell surface. Curr Opin Cell Biol 44:59–67CrossRefGoogle Scholar
  4. Bone CR, Tapley EC, Gorjánácz M, Starr DA (2014) The Caenorhabditis elegans SUN protein UNC-84 interacts with Lamin to transfer forces from the cytoplasm to the nucleoskeleton during nuclear migration. Mol Biol Cell 25(18):2853–2865CrossRefGoogle Scholar
  5. Booth-Gauthier EA, Du V, Ghibaudo M, Rape AD, Dahl KN, Ladoux B (2013) Hutchinson-Gilford progeria syndrome alters nuclear shape and reduces cell motility in three dimensional model substrates. Integr Biol 5(3):569–577CrossRefGoogle Scholar
  6. Brosig M, Ferralli J, Gelman L, Chiquet M, Chiquet-Ehrismann R (2010) Interfering with the connection between the nucleus and the cytoskeleton affects nuclear rotation, mechanotransduction and myogenesis. Int J Biochem Cell Biol 42(10):1717–1728CrossRefGoogle Scholar
  7. Caille N, Thoumine O, Tardy Y, Meister JJ (2002) Contribution of the nucleus to the mechanical properties of endothelial cells. J Biomech 35(2):177–187CrossRefGoogle Scholar
  8. Chancellor TJ, Lee J, Thodeti CK, Lele T (2010) Actomyosin tension exerted on the nucleus through nesprin-1 connections influences endothelial cell adhesion, migration, and cyclic strain-induced reorientation. Biophys J 99(1):115–123CrossRefGoogle Scholar
  9. Chen YL, Jan KM, Lin HS, Chien S (1995) Ultrastructural studies on macromolecular permeability in relation to endothelial cell turnover. Atherosclerosis 118(1):89–104CrossRefGoogle Scholar
  10. Cheng J, Du J (2007) Mechanical stretch simulates proliferation of venous smooth muscle cells through activation of the insulin-like growth factor-1 receptor. Arterioscler Thromb Vasc Biol 27:1744–1751CrossRefGoogle Scholar
  11. Cheng C, Tempel D, van Haperen R, van der Baan A, Grosveld F, Daemen MJ, Krams R, de Crom R (2006) Atherosclerotic lesion size and vulnerability are determined by patterns of fluid shear stress. Circulation 113(23):2744–2753CrossRefGoogle Scholar
  12. Chien S (2003) Molecular and mechanical bases of focal lipid accumulation in arterial wall. Prog Biophys Mol Biol 83(2):131–151CrossRefGoogle Scholar
  13. Chien S (2007) Mechanotransduction and endothelial cell homeostasis: the wisdom of the cell. Am J Physiol Heart Circ Physiol 292(3):H1209–H1224CrossRefGoogle Scholar
  14. Chien S (2008) Effects of disturbed flow on endothelial cells. Ann Biomed Eng 36(4):554–562CrossRefGoogle Scholar
  15. Chiu JJ, Chien S (2011) Effects of disturbed flow on vascular endothelium: pathophysiological basis and clinical perspectives. Physiol Rev 91(1):327–387CrossRefGoogle Scholar
  16. Chiu JJ, Wang DL, Chien S, Skalak R, Usami S (1998) Effects of disturbed flow on endothelial cells. J Biomech Eng 120(1):2–8CrossRefGoogle Scholar
  17. Chiu JJ, Usami S, Chien S (2009) Vascular endothelial responses to altered shear stress: pathologic implications for atherosclerosis. Ann Med 41(1):19–28CrossRefGoogle Scholar
  18. Cohen DJ, Osnabrugge RL, Magnuson EA, Wang K, Li H, Chinnakondepalli K, Pinto D, Abdallah MS, Vilain KA, Morice MC, Dawkins KD, Kappetein AP, Mohr FW, Serruys PW (2014) Cost-effectiveness of percutaneous coronary intervention with drug-eluting stents versus bypass surgery for patients with 3-vessel or left main coronary artery disease: final results from the synergy between percutaneous coronary intervention with TAXUS and cardiac surgery (SYNTAX) trial. Circulation 130:1146–1157CrossRefGoogle Scholar
  19. Conway DE, Schwartz MA (2015) Mechanotransduction of shear stress occurs through changes in VE-cadherin and PECAM-1 tension: implications for cell migration. Cell Adhes Migr 9(5):335–339CrossRefGoogle Scholar
  20. Davies PF (1995) Flow-mediated endothelial mechanotransduction. Physiol Rev 75(3):519–560CrossRefGoogle Scholar
  21. Dechat T, Pfleghaar K, Sengupta K, Shimi T, Shumaker DK, Solimando L, Goldman RD (2008) Nuclear lamins: major factors in the structural organization and function of the nucleus and chromatin. Genes Dev 22(7):832–853CrossRefGoogle Scholar
  22. Dou Z, Xu C, Donahue G, Shimi T, Pan JA, Zhu J, Ivanov A, Capell BC, Drake AM, Shah PP, Catanzaro JM, Ricketts MD, Lamark T, Adam SA, Marmorstein R, Zong WX, Johansen T, Goldman RD, Adams PD, Berger SL (2015) Autophagy mediates degradation of nuclear lamina. Nature 527(7576):105–109CrossRefGoogle Scholar
  23. Egorova AD, Khedoe PP, Goumans MJ, Yoder BK, Nauli SM, ten Dijke P, Poelmann RE, Hierck BP (2011) Lack of primary cilia primes shear-induced endothelial-to-mesenchymal transition. Circ Res 108(9):1093–1101CrossRefGoogle Scholar
  24. Florian JA, Kosky JR, Ainslie K, Pang Z, Dull RO, Tarbell JM (2003) Heparan sulfate proteoglycan is a mechanosensor on endothelial cells. Circ Res 93(10):e136–e142CrossRefGoogle Scholar
  25. Fung YC (1990) Biomechanics: motion, flow, stress, and growth. Springer-Verlag, New YorkCrossRefGoogle Scholar
  26. Giddens DP, Zarins CK, Glagov S (1993) The role of fluid mechanics in the localization and detection of atherosclerosis. J Biomech Eng 115(4B):588–594CrossRefGoogle Scholar
  27. Gilbert G, Ducret T, Savineau JP, Marthan R, Quignard JF (2016) Caveolae are involved in mechanotransduction during pulmonary hypertension. Am J Physiol Lung Cell Mol Physiol 310(11):L1078–L1087CrossRefGoogle Scholar
  28. Goldman RD, Gruenbaum Y, Moir RD, Shumaker DK, Spann TP (2002) Nuclear lamins: building blocks of nuclear architecture. Genes Dev 16(5):533–547CrossRefGoogle Scholar
  29. Greve JM, Les AS, Tang BT, Draney Blomme MT, Wilson NM, Dalman RL, Pelc NJ, Taylor CA (2006) Allometric scaling of wall shear stress from mice to humans: quantification using cine phase-contrast MRI and computational fluid dynamics. Am J Physiol Heart Circ Physiol 291(4):H1700–H1708CrossRefGoogle Scholar
  30. Guilluy C, Osborne LD, Van Landeghem L, Sharek L, Superfine R, Garcia-Mata R, Burridge K (2014) Isolated nuclei adapt to force and reveal a mechanotransduction pathway in the nucleus. Nat Cell Biol 16(4):376–381CrossRefGoogle Scholar
  31. Haga JH, Li YS, Chien S (2007) Molecular basis of the effects of mechanical stretch on vascular smooth muscle cells. J Biomech 40(5):947–960CrossRefGoogle Scholar
  32. Han Y, Wang L, Yao QP, Zhang P, Liu B, Wang GL, Shen BR, Cheng BB, Wang YX, Jiang ZL, Qi YX (2015) Nuclear envelope proteins Nesprin2 and LaminA regulate proliferation and apoptosis of vascular endothelial cells in response to shear stress. Biochim Biophys Acta 1853(5):1165–1173CrossRefGoogle Scholar
  33. Han Y, Huang K, Yao QP, Jiang ZL (2017) Mechanobiology in Vascular Remodeling. Natl Sci Rev nwx153Google Scholar
  34. Harada T, Swift J, Irianto J, Shin JW, Spinler KR, Athirasala A, Diegmiller R, Dingal PC, Ivanovska IL, Discher DE (2014) Nuclear lamin stiffness is a barrier to 3D migration, but softness can limit survival. J Cell Biol 204(5):669–682CrossRefGoogle Scholar
  35. Helmke BP, Thakker DB, Goldman RD, Davies PF (2001) Spatiotemporal analysis of flow-induced intermediate filament displacement in living endothelial cells. Biophys J 80(1):184–194CrossRefGoogle Scholar
  36. Hieda M (2017) Implications for diverse functions of the LINC complexes based on the structure. Cell 6(1):pii: E3CrossRefGoogle Scholar
  37. Ho CY, Lammerding J (2012) Lamins at a glance. J Cell Sci 125(Pt 9):2087–2093CrossRefGoogle Scholar
  38. Ho CY, Jaalouk DE, Vartiainen MK, Lammerding J (2013) Lamin a/C and emerin regulate MKL1-SRF activity by modulating actin dynamics. Nature 497(7450):507–511CrossRefGoogle Scholar
  39. Hoger JH, Ilyin VI, Forsyth S, Hoger A (2002) Shear stress regulates the endothelial Kir2.1 ion channel. Proc Natl Acad Sci U S A 99(11):7780–7785CrossRefGoogle Scholar
  40. Holaska JM (2008) Emerin and the nuclear lamina in muscle and cardiac disease. Circ Res 103(1):16–23CrossRefGoogle Scholar
  41. Huang K, Bao H, Yan ZQ, Wang L, Zhang P, Yao QP, Shi Q, Chen XH, Wang KX, Shen BR, Qi YX, Jiang ZL (2017) MicroRNA-33 protects against neointimal hyperplasia induced by arterial mechanical stretch in the grafted vein. Cardiovasc Res 113(5):488–497PubMedGoogle Scholar
  42. Huber F, Boire A, López MP, Koenderink GH (2015) Cytoskeletal crosstalk: when three different personalities team up. Curr Opin Cell Biol 32:39–47CrossRefGoogle Scholar
  43. Humphrey JD, Dufresne ER, Schwartz MA (2014) Mechanotransduction and extracellular matrix homeostasis. Nat Rev Mol Cell Biol 15(12):802–812CrossRefGoogle Scholar
  44. Humphrey JD, Schwartz MA, Tellides G, Milewicz DM (2015) Role of mechanotransduction in vascular biology: focus on thoracic aortic aneurysms and dissections. Circ Res 116(8):1448–1461CrossRefGoogle Scholar
  45. Jufri NF, Mohamedali A, Avolio A, Baker MS (2015) Mechanical stretch: physiological and pathological implications for human vascular endothelial cells. Vasc Cell 7:8CrossRefGoogle Scholar
  46. Kim DW, Langille BL, Wong MK, Gotlieb AI (1989) Patterns of endothelial microfilament distribution in the rabbit aorta in situ. Circ Res 64(1):21–31CrossRefGoogle Scholar
  47. Lammerding J, Schulze PC, Takahashi T, Kozlov S, Sullivan T, Kamm RD, Stewart CL, Lee RT (2004) LaminA/C deficiency causes defective nuclear mechanics and mechanotransduction. J Clin Invest 113(3):370–378CrossRefGoogle Scholar
  48. Lammerding J, Hsiao J, Schulze PC, Kozlov S, Stemart CL, Lee RT (2005) Abnormal nuclear shape and impaired mechanotransduction in emerin-deficient cells. J Cell Biol 170(5):781–791CrossRefGoogle Scholar
  49. Lombardi ML, Jaalouk DE, Shanahan CM, Burke B, Roux KJ, Lammerding J (2011) The interaction between nesprins and sun proteins at the nuclear envelope is critical for force transmission between the nucleus and cytoskeleton. J Biol Chem 286(30):26743–26753CrossRefGoogle Scholar
  50. Lu CJ, Du H, Wu J, Jansen DA, Jordan KL, Xu N, Sieck GC, Qian Q (2008) Non-random distribution and sensory functions of primary cilia in vascular smooth muscle cells. Kidney Blood Press Res 31(3):171–184CrossRefGoogle Scholar
  51. Macek Jilkova Z, Lisowska J, Manet S, Verdier C, Deplano V, Geindreau C, Faurobert E, Albigès-Rizo C, Duperray A (2014) CCM proteins control endothelial β1 integrin dependent response to shear stress. Biol Open 3(12):1228–1235CrossRefGoogle Scholar
  52. Miao H, Hu YL, Shiu YT, Yuan S, Zhao Y, Kaunas R, Wang Y, Jin G, Usami S, Chien S (2005) Effects of flow patterns on the localization and expression of VE-cadherin at vascular endothelial cell junctions: in vivo and in vitro investigations. J Vasc Res 42(1):77–89CrossRefGoogle Scholar
  53. Min J, Reznichenko M, Poythress RH, Gallant CM, Vetterkind S, Li Y, Morgan KG (2012) Src modulates contractile vascular smooth muscle function via regulation of focal adhesions. J Cell Physiol 227(11):3585–3592CrossRefGoogle Scholar
  54. Mohieldin AM, Zubayer HS, Al Omran AJ, Saternos HC, Zarban AA, Nauli SM, AbouAlaiwi WA (2016) Vascular endothelial primary Cilia: mechanosensation and hypertension. Curr Hypertens Rev 12(1):57–67CrossRefGoogle Scholar
  55. Moiseeva EP (2001) Adhesion receptors of vascular smooth muscle cells and their functions. Cardiovasc Res 52(3):372–386CrossRefGoogle Scholar
  56. Muchir A, Worman HJ (2007) Emery-Dreifuss muscular dystrophy. Curr Neurol Neurosic Rep 7(1):78–83CrossRefGoogle Scholar
  57. Nauli SM, Kawanabe Y, Kaminski JJ, Pearce WJ, Ingber DE, Zhou J (2008) Endothelial cilia are fluid shear sensors that regulate calcium signaling and nitric oxide production through polycystin-1. Circulation 117(9):1161–1171CrossRefGoogle Scholar
  58. Osmanagic-Myers S, Dechat T, Foisner R (2015) Lamins at the crossroads of mechanosignaling. Genes Dev 29(3):225–237CrossRefGoogle Scholar
  59. Owens GK, Kumar MS, Wamhoff BR (2004) Molecular regulation of vascular smooth muscle cell differentiation in development and disease. Physiol Rev 84:767–801CrossRefGoogle Scholar
  60. Pang L, Rusch NJ (2009) High-conductance, Ca(2+) -activated K+ channels: altered expression profiles in aging and cardiovascular disease. Mol Interv 9:230–233CrossRefGoogle Scholar
  61. Parizek M, Novotna K, Bacakova L (2011) The role of smooth muscle cells in vessel wall pathophysiology and reconstruction using bioactive synthetic polymers. Physiol Res 60:419–437PubMedGoogle Scholar
  62. Qi YX, Yao QP, Huang K, Shi Q, Zhang P, Wang GL, Han Y, Bao H, Wang L, Li HP, Shen BR, Wang Y, Chien S, Jiang ZL (2016) Nuclear envelope proteins modulate proliferation of vascular smooth muscle cells during cyclic stretch application. Proc Natl Acad Sci U S A 113(19):5293–5298CrossRefGoogle Scholar
  63. Rajgor D, Shanahan CM (2013) Nesprins: from the nuclear envelope and beyond. Expert Rev Mol Med 15:e5CrossRefGoogle Scholar
  64. Rothballer A, Kutay U (2013) The diverse functional LINCs of the nuclear envelope to the cytoskeleton and chromatin. Chromosoma 122(5):415–429CrossRefGoogle Scholar
  65. Sausbier M, Arntz C, Bucurenciu I, Zhao H, Zhou XB, Sausbier U, Feil S, Kamm S, Essin K, Sailer CA, Abdullah U, Krippeit-Drews P, Feil R, Hofmann F, Knaus HG, Kenyon C, Shipston MJ, Storm JF, Neuhuber W, Korth M, Schubert R, Gollasch M, Ruth P (2005) Elevated blood pressure linked to primary hyperaldosteronism and impaired vasodilation in BK channel-deficient mice. Circulation 112:60–68CrossRefGoogle Scholar
  66. Scimia MC, Hurtado C, Ray S, Metzler S, Wei K, Wang J, Woods CE, Purcell NH, Catalucci D, Akasaka T, Bueno OF, Vlasuk GP, Kaliman P, Bodmer R, Smith LH, Ashley E, Mercola M, Brown JH, Ruiz-Lozano P (2012) APJ acts as a dual receptor in cardiac hypertrophy. Nature 488(7411):394–398CrossRefGoogle Scholar
  67. Shah P, Wolf K, Lammerding J (2017) Bursting the bubble—nuclear envelope rupture as a path to genomic instability? Trends Cell Biol 27(8):546–555CrossRefGoogle Scholar
  68. Shyy JY, Chien S (1997) Role of integrins in cellular responses to mechanical stress and adhesion. Cur Opin Cell Biol. 9(5):707–713CrossRefGoogle Scholar
  69. Song M, San H, Anderson SA, Cannon RO 3rd, Orlic D (2014) Shear stress-induced mechanotransduction protein deregulation and vasculopathy in a mouse model of progeria. Stem Cell Res Ther 5(2):41CrossRefGoogle Scholar
  70. Song KH, Lee J, Park H, Kim HM, Park J, Kwon KW, Doh J (2016) Roles of endothelial A-type lamins in migration of T cells on and under endothelial layers. Sci Rep 6:23412CrossRefGoogle Scholar
  71. Speight P, Kofler M, Szászi K, Kapus A (2016) Context-dependent switch in chemo/mechanotransduction via multilevel crosstalk among cytoskeleton-regulated MRTF and TAZ and TGFβ-regulated Smad3. Nat Commun 7:11642CrossRefGoogle Scholar
  72. Spichal M, Fabre E (2017) The emerging role of the cytoskeleton in chromosome dynamics. Front Genet 8:60CrossRefGoogle Scholar
  73. Starr DA (2012) Laminopathies: too much SUN is a bad thing. Curr Biol 22(17):R678–R680CrossRefGoogle Scholar
  74. Suo J, Ferrara DE, Sorescu D, Guldberg RE, Taylor WR, Giddens DP (2007) Hemodynamic shear stresses in mouse aortas: implications for atherogenesis. Arterioscler Thromb Vasc Biol 27(2):346–351CrossRefGoogle Scholar
  75. Swift J, Ivanovska IL, Buxboim A, Harada T, Dingal PC, Pinter J, Pajerowski JD, Spinler KR, Shin JW, Tewari M, Rehfeldt F, Speicher DW, Discher DE (2013) Nuclear Lamin-a scales with tissue stiffness and enhances matrix-directed differentiation. Science 341(6149):1240104CrossRefGoogle Scholar
  76. Tapley EC, Starr DA (2013) Connecting the nucleus to the cytoskeleton by SUN-KASH bridges across the nuclear envelope. Curr Opin Cell Biol 25(1):57–62CrossRefGoogle Scholar
  77. Tzima E, Irani-Tehrani M, Kiosses WB, Dejana E, Schultz DA, Engelhardt B, Cao G, DeLisser H, Schwartz MA (2005) A mechanosensory complex that mediates the endothelial cell response to fluid shear stress. Nature 437(7057):426–431CrossRefGoogle Scholar
  78. Ungricht R, Kutay U (2017) Mechanisms and functions of nuclear envelope remodelling. Nat Rev Mol Cell Biol 18(4):229–245CrossRefGoogle Scholar
  79. Vartanian KB, Berny MA, McCarty OJ, Hanson SR, Hinds MT (2010) Cytoskeletal structure regulates endothelial cell immunogenicity independent of fluid shear stress. Am J Physiol Cell Physiol 298(2):C333–C341CrossRefGoogle Scholar
  80. Wan XJ, Zhao HC, Zhang P, Huo B, Shen BR, Yan ZQ, Qi YX, Jiang ZL (2015) Involvement of BK channel in differentiation of vascular smooth muscle cells induced by mechanical stretch. Int J Biochem Cell Biol 59:21–29CrossRefGoogle Scholar
  81. Wang Y, Shyy JY, Chien S (2008) Fluorescence proteins, live-cell imaging, and mechanobiology: seeing is believing. Annu Rev Biomed Eng 10:1–38CrossRefGoogle Scholar
  82. Wilson KL, Berk JM (2010) The nuclear envelope at a glance. J Cell Sci 123(Pt 12):1973–1978CrossRefGoogle Scholar
  83. Wu X, Yang Y, Gui P, Sohma Y, Meininger GA, Davis GE, Braun AP, Davis MJ (2008) Potentiation of large conductance, Ca2+−activated K+ (BK) channels by α5β1 integrin activation in arteriolar smooth muscle. J Physiol 586(6):1699–1713CrossRefGoogle Scholar
  84. Yang B, Lieu ZZ, Wolfenson H, Hameed FM, Bershadsky AD, Sheetz MP (2016) Mechanosensing controlled directly by tyrosine kinases. Nano Lett 16(9):5951–5961CrossRefGoogle Scholar
  85. Ye GJ, Nesmith AP, Parker KK (2014) The role of mechanotransduction on vascular smooth muscle myocytes cytoskeleton and contractile function. Anat Rec 297(9):1758–1769CrossRefGoogle Scholar
  86. Zhou J, Li YS, Chien S (2014) Shear stress-initiated signaling and its regulation of endothelial function. Arterioscler Thromb Vasc Biol 34(10):2191–2198CrossRefGoogle Scholar

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© Springer International Publishing AG, part of Springer Nature 2018

Authors and Affiliations

  1. 1.Institute of Mechanobiology and Medical Engineering, School of Life Sciences and BiotechnologyShanghai Jiao Tong UniversityShanghaiChina

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