Pericytes in the Heart

  • Linda L. Lee
  • Vishnu ChintalgattuEmail author
Part of the Advances in Experimental Medicine and Biology book series (AEMB, volume 1122)


Mural cells known as pericytes envelop the endothelial layer of microvessels throughout the body and have been described to have tissue-specific functions. Cardiac pericytes are abundantly found in the heart, but they are relatively understudied. Currently, their importance is emerging in cardiovascular homeostasis and dysfunction due to their pleiotropism. They are known to play key roles in vascular tone and vascular integrity as well as angiogenesis. However, their dysfunctional presence and/or absence is critical in the mechanisms that lead to cardiac pathologies such as myocardial infarction, fibrosis, and thrombosis. Moreover, they are targeted as a therapeutic potential due to their mesenchymal properties that could allow them to repair and regenerate a damaged heart. They are also sought after as a cell-based therapy based on their healing potential in preclinical studies of animal models of myocardial infarction. Therefore, recognizing the importance of cardiac pericytes and understanding their biology will lead to new therapeutic concepts.


Cardiac pericyte Heart Cardiovascular physiology Cardiovascular pathophysiology Myocardial infarction Myocardial ischemic disease Vascular stem cell Perivascular cell Mural cell Vascular tone Vascular integrity Vascular biology 



Ganglioside 3g5


Alpha-smooth muscle actin


Alkaline phosphatase






Endothelial brain-derived neurotrophic factor


C-type natriuretic peptide


Cardiac pericyte


Connective tissue growth factor




Chemokine receptor 3


Extracellular matrix


Glioma-associated oncogene 1


Heparin-binding epidermal growth factor


Hepatocyte growth factor


Low-density lipoprotein receptor-related protein 6


Myocardial infarction


Matrix metalloproteinases


Mesenchymal stem cells


Homeobox transcription factor Nanog


Neural glial 2


Octamer-binding transcription factor 4

p75 NTR

Neurotrophin receptor


Platelet-derived growth factor bb


Platelet-derived growth factor receptor beta


Pro-nerve growth factor


Regulator of G protein signaling 5




Sirtuin 3


Sortilin-related VPS10 domain-containing receptor 2


Sex-determining region box


Saphenous vein-derived pericyte progenitor cells


T-box protein 18


Tissue factor


Transforming growth factor beta


Tropomyosin receptor kinase B


Vascular calcification-associated factor


Vascular endothelial growth factor A


Vascular endothelial growth factor receptor 2


von Willebrand factor


  1. Al Ahmad A, Gassmann M, Ogunshola OO (2009) Maintaining blood-brain barrier integrity: pericytes perform better than astrocytes during prolonged oxygen deprivation. J Cell Physiol 218(3):612–622PubMedCrossRefPubMedCentralGoogle Scholar
  2. Alarcon-Martinez L et al (2018) Capillary pericytes express alpha-smooth muscle actin, which requires prevention of filamentous-actin depolymerization for detection. Elife 7Google Scholar
  3. Alexander MY et al (2005) Identification and characterization of vascular calcification-associated factor, a novel gene upregulated during vascular calcification in vitro and in vivo. Arterioscler Thromb Vasc Biol 25(9):1851–1857PubMedCrossRefPubMedCentralGoogle Scholar
  4. Alvino VV et al (2018) Transplantation of allogeneic pericytes improves myocardial vascularization and reduces interstitial fibrosis in a swine model of reperfused acute myocardial infarction. J Am Heart Assoc 7(2)Google Scholar
  5. Anastasia A et al (2014) Trkb signaling in pericytes is required for cardiac microvessel stabilization. PLoS One 9(1):e87406PubMedPubMedCentralCrossRefGoogle Scholar
  6. Armulik A, Abramsson A, Betsholtz C (2005) Endothelial/pericyte interactions. Circ Res 97(6):512–523PubMedCrossRefPubMedCentralGoogle Scholar
  7. Armulik A et al (2010) Pericytes regulate the blood-brain barrier. Nature 468(7323):557–561CrossRefGoogle Scholar
  8. Armulik A, Genove G, Betsholtz C (2011) Pericytes: developmental, physiological, and pathological perspectives, problems, and promises. Dev Cell 21(2):193–215PubMedCrossRefGoogle Scholar
  9. Avolio E et al (2015a) Expansion and characterization of neonatal cardiac pericytes provides a novel cellular option for tissue engineering in congenital heart disease. J Am Heart Assoc 4(6):e002043PubMedPubMedCentralCrossRefGoogle Scholar
  10. Avolio E et al (2015b) Combined intramyocardial delivery of human pericytes and cardiac stem cells additively improves the healing of mouse infarcted hearts through stimulation of vascular and muscular repair. Circ Res 116(10):e81–e94PubMedCrossRefPubMedCentralGoogle Scholar
  11. Bardeesi ASA et al (2017) A novel role of cellular interactions in vascular calcification. J Transl Med 15(1):95PubMedPubMedCentralCrossRefGoogle Scholar
  12. Bell RD et al (2010) Pericytes control key neurovascular functions and neuronal phenotype in the adult brain and during brain aging. Neuron 68(3):409–427PubMedPubMedCentralCrossRefGoogle Scholar
  13. Benest AV et al (2006) VEGF and angiopoietin-1 stimulate different angiogenic phenotypes that combine to enhance functional neovascularization in adult tissue. Microcirculation 13(6):423–437PubMedCrossRefPubMedCentralGoogle Scholar
  14. Bergers G, Song S (2005) The role of pericytes in blood-vessel formation and maintenance. Neuro Oncol 7(4):452–464PubMedPubMedCentralCrossRefGoogle Scholar
  15. Birbrair A et al (2014) Type-1 pericytes accumulate after tissue injury and produce collagen in an organ-dependent manner. Stem Cell Res Ther 5(6):122PubMedPubMedCentralCrossRefGoogle Scholar
  16. Bischoff FC et al (2017) Identification and functional characterization of hypoxia-induced endoplasmic reticulum stress regulating lncRNA (HypERlnc) in Pericytes. Circ Res 121(4):368–375PubMedCrossRefPubMedCentralGoogle Scholar
  17. Bjarnegard M et al (2004) Endothelium-specific ablation of PDGFB leads to pericyte loss and glomerular, cardiac and placental abnormalities. Development 131(8):1847–1857PubMedCrossRefPubMedCentralGoogle Scholar
  18. Bobik A et al (1999) Distinct patterns of transforming growth factor-beta isoform and receptor expression in human atherosclerotic lesions. Colocalization implicates TGF-beta in fibrofatty lesion development. Circulation 99(22):2883–2891PubMedCrossRefPubMedCentralGoogle Scholar
  19. Bodnar RJ et al (2013) Pericyte regulation of vascular remodeling through the CXC receptor 3. Arterioscler Thromb Vasc Biol 33(12):2818–2829PubMedPubMedCentralCrossRefGoogle Scholar
  20. Borysova L et al (2013) How calcium signals in myocytes and pericytes are integrated across in situ microvascular networks and control microvascular tone. Cell Calcium 54(3):163–174PubMedPubMedCentralCrossRefGoogle Scholar
  21. Boscolo E et al (2011) JAGGED1 signaling regulates hemangioma stem cell-to-pericyte/vascular smooth muscle cell differentiation. Arterioscler Thromb Vasc Biol 31(10):2181–2192PubMedPubMedCentralCrossRefGoogle Scholar
  22. Cai CL et al (2008a) A myocardial lineage derives from Tbx18 epicardial cells. Nature 454(7200):104–108PubMedPubMedCentralCrossRefGoogle Scholar
  23. Cai J et al (2008b) The angiopoietin/Tie-2 system regulates pericyte survival and recruitment in diabetic retinopathy. Invest Ophthalmol Vis Sci 49(5):2163–2171PubMedCrossRefPubMedCentralGoogle Scholar
  24. Campagnolo P et al (2010) Human adult vena saphena contains perivascular progenitor cells endowed with clonogenic and proangiogenic potential. Circulation 121(15):1735–1745PubMedPubMedCentralCrossRefGoogle Scholar
  25. Canfield AE et al (2000) Role of pericytes in vascular calcification: a review. Z Kardiol 89(Suppl 2):20–27PubMedCrossRefPubMedCentralGoogle Scholar
  26. Caporali A et al (2017) Contribution of pericyte paracrine regulation of the endothelium to angiogenesis. Pharmacol Ther 171:56–64PubMedCrossRefPubMedCentralGoogle Scholar
  27. Cappellari O et al (2013) Dll4 and PDGF-BB convert committed skeletal myoblasts to pericytes without erasing their myogenic memory. Dev Cell 24(6):586–599PubMedCrossRefPubMedCentralGoogle Scholar
  28. Chen CW et al (2013) Human pericytes for ischemic heart repair. Stem Cells 31(2):305–316PubMedPubMedCentralCrossRefGoogle Scholar
  29. Chen WC et al (2015) Human myocardial pericytes: multipotent mesodermal precursors exhibiting cardiac specificity. Stem Cells 33(2):557–573PubMedPubMedCentralCrossRefGoogle Scholar
  30. Chen Q et al (2016) Endothelial cells are progenitors of cardiac pericytes and vascular smooth muscle cells. Nat Commun 7:12422PubMedPubMedCentralCrossRefGoogle Scholar
  31. Chintalgattu V et al (2013) Coronary microvascular pericytes are the cellular target of sunitinib malate-induced cardiotoxicity. Sci Transl Med 5(187):187ra69PubMedCrossRefPubMedCentralGoogle Scholar
  32. Cho H et al (2003) Pericyte-specific expression of Rgs5: implications for PDGF and EDG receptor signaling during vascular maturation. FASEB J 17(3):440–442PubMedCrossRefPubMedCentralGoogle Scholar
  33. Collett GD, Canfield AE (2005) Angiogenesis and pericytes in the initiation of ectopic calcification. Circ Res 96(9):930–938PubMedCrossRefGoogle Scholar
  34. Corselli M et al (2012) The tunica adventitia of human arteries and veins as a source of mesenchymal stem cells. Stem Cells Dev 21(8):1299–1308PubMedCrossRefGoogle Scholar
  35. Costa MA et al (2018) Pericytes constrict blood vessels after myocardial ischemia. J Mol Cell Cardiol 116:1–4PubMedPubMedCentralCrossRefGoogle Scholar
  36. Covas DT et al (2008) Multipotent mesenchymal stromal cells obtained from diverse human tissues share functional properties and gene-expression profile with CD146+ perivascular cells and fibroblasts. Exp Hematol 36(5):642–654PubMedCrossRefGoogle Scholar
  37. Crisan M et al (2008) Purification and long-term culture of multipotent progenitor cells affiliated with the walls of human blood vessels: myoendothelial cells and pericytes. Methods Cell Biol 86:295–309PubMedCrossRefGoogle Scholar
  38. Crisan M et al (2012) Perivascular cells for regenerative medicine. J Cell Mol Med 16(12):2851–2860PubMedPubMedCentralCrossRefGoogle Scholar
  39. Dar A et al (2012) Multipotent vasculogenic pericytes from human pluripotent stem cells promote recovery of murine ischemic limb. Circulation 125(1):87–99PubMedCrossRefGoogle Scholar
  40. Darland DC et al (2003) Pericyte production of cell-associated VEGF is differentiation-dependent and is associated with endothelial survival. Dev Biol 264(1):275–288PubMedCrossRefPubMedCentralGoogle Scholar
  41. Davaine JM et al (2014) Osteoprotegerin, pericytes and bone-like vascular calcification are associated with carotid plaque stability. PLoS One 9(9):e107642PubMedPubMedCentralCrossRefGoogle Scholar
  42. Dellavalle A et al (2007) Pericytes of human skeletal muscle are myogenic precursors distinct from satellite cells. Nat Cell Biol 9(3):255–267PubMedCrossRefGoogle Scholar
  43. Dewi NA et al (2018) Mechanism of retinal pericyte migration through angiopoietin/Tie-2 signaling pathway on diabetic rats. Int J Ophthalmol 11(3):375–381PubMedPubMedCentralGoogle Scholar
  44. Dias Moura Prazeres PH et al (2017) Pericytes are heterogeneous in their origin within the same tissue. Dev Biol 427(1):6–11PubMedCrossRefPubMedCentralGoogle Scholar
  45. Dias DO et al (2018) Reducing pericyte-derived scarring promotes recovery after spinal cord injury. Cell 173(1):153–165. e22PubMedPubMedCentralCrossRefGoogle Scholar
  46. Eilken HM et al (2017) Pericytes regulate VEGF-induced endothelial sprouting through VEGFR1. Nat Commun 8(1):1574PubMedPubMedCentralCrossRefGoogle Scholar
  47. Ellison-Hughes GM, Madeddu P (2017) Exploring pericyte and cardiac stem cell secretome unveils new tactics for drug discovery. Pharmacol Ther 171:1–12PubMedPubMedCentralCrossRefGoogle Scholar
  48. Fang S, Salven P (2011) Stem cells in tumor angiogenesis. J Mol Cell Cardiol 50(2):290–295PubMedCrossRefPubMedCentralGoogle Scholar
  49. Farrington-Rock C et al (2004) Chondrogenic and adipogenic potential of microvascular pericytes. Circulation 110(15):2226–2232PubMedCrossRefPubMedCentralGoogle Scholar
  50. Feng J et al (2011) Dual origin of mesenchymal stem cells contributing to organ growth and repair. Proc Natl Acad Sci U S A 108(16):6503–6508PubMedPubMedCentralCrossRefGoogle Scholar
  51. Fernandez-Klett F et al (2010) Pericytes in capillaries are contractile in vivo, but arterioles mediate functional hyperemia in the mouse brain. Proc Natl Acad Sci U S A 107(51):22290–22295PubMedPubMedCentralCrossRefGoogle Scholar
  52. Franco M et al (2011) Pericytes promote endothelial cell survival through induction of autocrine VEGF-A signaling and Bcl-w expression. Blood 118(10):2906–2917PubMedPubMedCentralCrossRefGoogle Scholar
  53. Fuxe J et al (2011) Pericyte requirement for anti-leak action of angiopoietin-1 and vascular remodeling in sustained inflammation. Am J Pathol 178(6):2897–2909PubMedPubMedCentralCrossRefGoogle Scholar
  54. Geevarghese A, Herman IM (2014) Pericyte-endothelial crosstalk: implications and opportunities for advanced cellular therapies. Transl Res 163(4):296–306PubMedPubMedCentralCrossRefGoogle Scholar
  55. Gerhardt H, Betsholtz C (2003) Endothelial-pericyte interactions in angiogenesis. Cell Tissue Res 314(1):15–23PubMedCrossRefPubMedCentralGoogle Scholar
  56. Greenhalgh SN, Iredale JP, Henderson NC (2013) Origins of fibrosis: pericytes take Centre stage. F1000Prime Rep 5:37PubMedPubMedCentralCrossRefGoogle Scholar
  57. Gubernator M et al (2015) Epigenetic profile of human adventitial progenitor cells correlates with therapeutic outcomes in a mouse model of limb ischemia. Arterioscler Thromb Vasc Biol 35(3):675–688PubMedCrossRefPubMedCentralGoogle Scholar
  58. Guimaraes-Camboa N et al (2017) Pericytes of multiple organs do not behave as mesenchymal stem cells in vivo. Cell Stem Cell 20(3):345–359. e5PubMedPubMedCentralCrossRefGoogle Scholar
  59. Hall CN et al (2014) Capillary pericytes regulate cerebral blood flow in health and disease. Nature 508(7494):55–60PubMedPubMedCentralCrossRefGoogle Scholar
  60. Hamilton NB, Attwell D, Hall CN (2010) Pericyte-mediated regulation of capillary diameter: a component of neurovascular coupling in health and disease. Front Neuroenergetics 2Google Scholar
  61. He Q, Spiro MJ (1995) Isolation of rat heart endothelial cells and pericytes: evaluation of their role in the formation of extracellular matrix components. J Mol Cell Cardiol 27(5):1173–1183PubMedCrossRefPubMedCentralGoogle Scholar
  62. He X, Zeng H, Chen JX (2016) Ablation of SIRT3 causes coronary microvascular dysfunction and impairs cardiac recovery post myocardial ischemia. Int J Cardiol 215:349–357PubMedPubMedCentralCrossRefGoogle Scholar
  63. Hellstrom M et al (2001) Lack of pericytes leads to endothelial hyperplasia and abnormal vascular morphogenesis. J Cell Biol 153(3):543–553PubMedPubMedCentralCrossRefGoogle Scholar
  64. Henderson NC et al (2013) Targeting of alphav integrin identifies a core molecular pathway that regulates fibrosis in several organs. Nat Med 19(12):1617–1624PubMedCrossRefPubMedCentralGoogle Scholar
  65. Hughes S, Chan-Ling T (2004) Characterization of smooth muscle cell and pericyte differentiation in the rat retina in vivo. Invest Ophthalmol Vis Sci 45(8):2795–2806PubMedCrossRefPubMedCentralGoogle Scholar
  66. Ivanov D et al (2001) Expression of cell adhesion molecule T-cadherin in the human vasculature. Histochem Cell Biol 115(3):231–242PubMedPubMedCentralGoogle Scholar
  67. Ivanova EA, Orekhov AN (2016) Cellular model of Atherogenesis based on pluripotent vascular wall pericytes. Stem Cells Int 2016:7321404PubMedPubMedCentralCrossRefGoogle Scholar
  68. Ivarsson M et al (1996) Recruitment of type I collagen producing cells from the microvasculature in vitro. Exp Cell Res 229(2):336–349PubMedCrossRefPubMedCentralGoogle Scholar
  69. Juchem G et al (2010) Pericytes in the macrovascular intima: possible physiological and pathogenetic impact. Am J Physiol Heart Circ Physiol 298(3):H754–H770PubMedCrossRefPubMedCentralGoogle Scholar
  70. Kaminski WE et al (2001) Basis of hematopoietic defects in platelet-derived growth factor (PDGF)-B and PDGF beta-receptor null mice. Blood 97(7):1990–1998PubMedCrossRefPubMedCentralGoogle Scholar
  71. Katare RG, Madeddu P (2013) Pericytes from human veins for treatment of myocardial ischemia. Trends Cardiovasc Med 23(3):66–70PubMedPubMedCentralCrossRefGoogle Scholar
  72. Katare R et al (2011) Transplantation of human pericyte progenitor cells improves the repair of infarcted heart through activation of an angiogenic program involving micro-RNA-132. Circ Res 109(8):894–906PubMedPubMedCentralCrossRefGoogle Scholar
  73. Kelly-Goss MR et al (2014) Targeting pericytes for angiogenic therapies. Microcirculation 21(4):345–357PubMedPubMedCentralCrossRefGoogle Scholar
  74. Keramati AR et al (2011) Wild-type LRP6 inhibits, whereas atherosclerosis-linked LRP6R611C increases PDGF-dependent vascular smooth muscle cell proliferation. Proc Natl Acad Sci U S A 108(5):1914–1918PubMedPubMedCentralCrossRefGoogle Scholar
  75. Kim J, Braun T (2015) Targeting the cellular origin of organ fibrosis. Cell Stem Cell 16(1):3–4PubMedCrossRefPubMedCentralGoogle Scholar
  76. Kirton JP et al (2006) Dexamethasone downregulates calcification-inhibitor molecules and accelerates osteogenic differentiation of vascular pericytes: implications for vascular calcification. Circ Res 98(10):1264–1272PubMedCrossRefPubMedCentralGoogle Scholar
  77. Kirton JP et al (2007) Wnt/beta-catenin signaling stimulates chondrogenic and inhibits adipogenic differentiation of pericytes: potential relevance to vascular disease? Circ Res 101(6):581–589PubMedCrossRefPubMedCentralGoogle Scholar
  78. Klein D et al (2011) Vascular wall-resident CD44+ multipotent stem cells give rise to pericytes and smooth muscle cells and contribute to new vessel maturation. PLoS One 6(5):e20540PubMedPubMedCentralCrossRefGoogle Scholar
  79. Kotecki M et al (2010) Calpain- and Talin-dependent control of microvascular pericyte contractility and cellular stiffness. Microvasc Res 80(3):339–348PubMedPubMedCentralCrossRefGoogle Scholar
  80. Kovacic JC et al (2012) Epithelial-to-mesenchymal and endothelial-to-mesenchymal transition: from cardiovascular development to disease. Circulation 125(14):1795–1808PubMedPubMedCentralCrossRefGoogle Scholar
  81. Kramann R et al (2015a) Pharmacological GLI2 inhibition prevents myofibroblast cell-cycle progression and reduces kidney fibrosis. J Clin Invest 125(8):2935–2951PubMedPubMedCentralCrossRefGoogle Scholar
  82. Kramann R et al (2015b) Perivascular Gli1+ progenitors are key contributors to injury-induced organ fibrosis. Cell Stem Cell 16(1):51–66PubMedCrossRefPubMedCentralGoogle Scholar
  83. Kramann R et al (2017) Gli1(+) Pericyte loss induces capillary rarefaction and proximal tubular injury. J Am Soc Nephrol 28(3):776–784PubMedCrossRefPubMedCentralGoogle Scholar
  84. Kumar A et al (2017) Specification and diversification of Pericytes and smooth muscle cells from Mesenchymoangioblasts. Cell Rep 19(9):1902–1916PubMedPubMedCentralCrossRefGoogle Scholar
  85. Lee S et al (2010) Pericyte actomyosin-mediated contraction at the cell-material interface can modulate the microvascular niche. J Phys Condens Matter 22(19):194115PubMedCrossRefPubMedCentralGoogle Scholar
  86. Leszczynska A, Murphy JM (2018) Vascular calcification: is it rather a stem/progenitor cells driven phenomenon? Front Bioeng Biotechnol 6:10PubMedPubMedCentralCrossRefGoogle Scholar
  87. Lin SL et al (2008) Pericytes and perivascular fibroblasts are the primary source of collagen-producing cells in obstructive fibrosis of the kidney. Am J Pathol 173(6):1617–1627PubMedPubMedCentralCrossRefGoogle Scholar
  88. Liu Y et al (2007) Hepatocyte growth factor and c-met expression in pericytes: implications for atherosclerotic plaque development. J Pathol 212(1):12–19PubMedCrossRefPubMedCentralGoogle Scholar
  89. Magnusson PU et al (2007) Platelet-derived growth factor receptor-beta constitutive activity promotes angiogenesis in vivo and in vitro. Arterioscler Thromb Vasc Biol 27(10):2142–2149PubMedCrossRefPubMedCentralGoogle Scholar
  90. Maisonpierre PC et al (1997) Angiopoietin-2, a natural antagonist for Tie2 that disrupts in vivo angiogenesis. Science 277(5322):55–60PubMedCrossRefPubMedCentralGoogle Scholar
  91. Matsugi T, Chen Q, Anderson DR (1997) Adenosine-induced relaxation of cultured bovine retinal pericytes. Invest Ophthalmol Vis Sci 38(13):2695–2701PubMedPubMedCentralGoogle Scholar
  92. Matsuki M et al (2015) Ninjurin1 is a novel factor to regulate angiogenesis through the function of pericytes. Circ J 79(6):1363–1371PubMedCrossRefPubMedCentralGoogle Scholar
  93. Matthews BG et al (2016) Osteogenic potential of alpha smooth muscle actin expressing muscle resident progenitor cells. Bone 84:69–77PubMedCrossRefPubMedCentralGoogle Scholar
  94. Mazzoni J, Cutforth T, Agalliu D (2015) Dissecting the role of smooth muscle cells versus Pericytes in regulating cerebral blood flow using in vivo optical imaging. Neuron 87(1):4–6PubMedCrossRefPubMedCentralGoogle Scholar
  95. McCullough PA, Olobatoke A, Vanhecke TE (2011) Galectin-3: a novel blood test for the evaluation and management of patients with heart failure. Rev Cardiovasc Med 12(4):200–210PubMedPubMedCentralGoogle Scholar
  96. McGuire PG et al (2011) Pericyte-derived sphingosine 1-phosphate induces the expression of adhesion proteins and modulates the retinal endothelial cell barrier. Arterioscler Thromb Vasc Biol 31(12):e107–e115PubMedPubMedCentralCrossRefGoogle Scholar
  97. Mishra A et al (2014) Imaging pericytes and capillary diameter in brain slices and isolated retinae. Nat Protoc 9(2):323–336PubMedCrossRefPubMedCentralGoogle Scholar
  98. Mitchell TS et al (2008) RGS5 expression is a quantitative measure of pericyte coverage of blood vessels. Angiogenesis 11(2):141–151PubMedCrossRefPubMedCentralGoogle Scholar
  99. Murray IR et al (2017) Skeletal and cardiac muscle pericytes: functions and therapeutic potential. Pharmacol Ther 171:65–74PubMedCrossRefPubMedCentralGoogle Scholar
  100. Murshed M, McKee MD (2010) Molecular determinants of extracellular matrix mineralization in bone and blood vessels. Curr Opin Nephrol Hypertens 19(4):359–365PubMedCrossRefPubMedCentralGoogle Scholar
  101. Nadal JA et al (2002) Angiotensin II stimulates migration of retinal microvascular pericytes: involvement of TGF-beta and PDGF-BB. Am J Physiol Heart Circ Physiol 282(2):H739–H748PubMedCrossRefPubMedCentralGoogle Scholar
  102. Nakagawa S et al (2009) A new blood-brain barrier model using primary rat brain endothelial cells, pericytes and astrocytes. Neurochem Int 54(3–4):253–263PubMedCrossRefPubMedCentralGoogle Scholar
  103. Nakamura Y et al (1995) Expression of local hepatocyte growth factor system in vascular tissues. Biochem Biophys Res Commun 215(2):483–488PubMedCrossRefPubMedCentralGoogle Scholar
  104. Nees S et al (2012a) Isolation, bulk cultivation, and characterization of coronary microvascular pericytes: the second most frequent myocardial cell type in vitro. Am J Physiol Heart Circ Physiol 302(1):H69–H84PubMedCrossRefPubMedCentralGoogle Scholar
  105. Nees S et al (2012b) Wall structures of myocardial precapillary arterioles and postcapillary venules reexamined and reconstructed in vitro for studies on barrier functions. Am J Physiol Heart Circ Physiol 302(1):H51–H68PubMedCrossRefPubMedCentralGoogle Scholar
  106. Nees S et al (2013) Abundant Pericytes in the venous intima and the vasa Venarum: evidence for their key role in venous thrombosis. J Vasc Surg Venous Lymphat Disord 1(1):113PubMedCrossRefPubMedCentralGoogle Scholar
  107. Neuhaus AA et al (2017) Novel method to study pericyte contractility and responses to ischaemia in vitro using electrical impedance. J Cereb Blood Flow Metab 37(6):2013–2024PubMedCrossRefPubMedCentralGoogle Scholar
  108. Nisancioglu MH et al (2008) Generation and characterization of rgs5 mutant mice. Mol Cell Biol 28(7):2324–2331PubMedPubMedCentralCrossRefGoogle Scholar
  109. O’Farrell FM, Attwell D (2014) A role for pericytes in coronary no-reflow. Nat Rev Cardiol 11(7):427–432PubMedCrossRefPubMedCentralGoogle Scholar
  110. O’Farrell FM et al (2017) Capillary pericytes mediate coronary no-reflow after myocardial ischaemia. Elife 6Google Scholar
  111. Osterud B, Bjorklid E (2006) Sources of tissue factor. Semin Thromb Hemost 32(1):11–23PubMedCrossRefPubMedCentralGoogle Scholar
  112. Paik JH et al (2004) Sphingosine 1-phosphate receptor regulation of N-cadherin mediates vascular stabilization. Genes Dev 18(19):2392–2403PubMedPubMedCentralCrossRefGoogle Scholar
  113. Peppiatt CM et al (2006) Bidirectional control of CNS capillary diameter by pericytes. Nature 443(7112):700–704PubMedPubMedCentralCrossRefGoogle Scholar
  114. Pinto AR et al (2016) Revisiting cardiac cellular composition. Circ Res 118(3):400–409PubMedCrossRefPubMedCentralGoogle Scholar
  115. Psaltis PJ et al (2010) Enrichment for STRO-1 expression enhances the cardiovascular paracrine activity of human bone marrow-derived mesenchymal cell populations. J Cell Physiol 223(2):530–540PubMedPubMedCentralGoogle Scholar
  116. Ribatti D, Nico B, Crivellato E (2011) The role of pericytes in angiogenesis. Int J Dev Biol 55(3):261–268PubMedCrossRefPubMedCentralGoogle Scholar
  117. Sa da Bandeira D, Casamitjana J, Crisan M (2017) Pericytes, integral components of adult hematopoietic stem cell niches. Pharmacol Ther 171:104–113PubMedCrossRefPubMedCentralGoogle Scholar
  118. Sagare AP et al (2013) Pericyte loss influences Alzheimer-like neurodegeneration in mice. Nat Commun 4:2932PubMedPubMedCentralCrossRefGoogle Scholar
  119. Schrimpf C, Duffield JS (2011) Mechanisms of fibrosis: the role of the pericyte. Curr Opin Nephrol Hypertens 20(3):297–305PubMedCrossRefPubMedCentralGoogle Scholar
  120. Sengillo JD et al (2013) Deficiency in mural vascular cells coincides with blood-brain barrier disruption in Alzheimer’s disease. Brain Pathol 23(3):303–310PubMedCrossRefPubMedCentralGoogle Scholar
  121. Shepro D, Morel NM (1993) Pericyte physiology. FASEB J 7(11):1031–1038PubMedCrossRefPubMedCentralGoogle Scholar
  122. Shiwen X et al (2009) Pericytes display increased CCN2 expression upon culturing. J Cell Commun Signal 3(1):61–64PubMedPubMedCentralCrossRefGoogle Scholar
  123. Siao CJ et al (2012) ProNGF, a cytokine induced after myocardial infarction in humans, targets pericytes to promote microvascular damage and activation. J Exp Med 209(12):2291–2305PubMedPubMedCentralCrossRefGoogle Scholar
  124. Sims DE (1986) The pericyte—a review. Tissue Cell 18(2):153–174PubMedCrossRefPubMedCentralGoogle Scholar
  125. Spiranec K et al (2018) Endothelial C-type natriuretic peptide acts on Pericytes to regulate microcirculatory flow and blood pressure. Circulation 138(5):494–508PubMedCrossRefPubMedCentralGoogle Scholar
  126. Stallcup WB (2013) Bidirectional myoblast-pericyte plasticity. Dev Cell 24(6):563–564PubMedCrossRefPubMedCentralGoogle Scholar
  127. Stapor PC et al (2014) Pericyte dynamics during angiogenesis: new insights from new identities. J Vasc Res 51(3):163–174PubMedPubMedCentralCrossRefGoogle Scholar
  128. Stratman AN, Davis GE (2012) Endothelial cell-pericyte interactions stimulate basement membrane matrix assembly: influence on vascular tube remodeling, maturation, and stabilization. Microsc Microanal 18(1):68–80PubMedCrossRefPubMedCentralGoogle Scholar
  129. Stratman AN et al (2010) Endothelial-derived PDGF-BB and HB-EGF coordinately regulate pericyte recruitment during vasculogenic tube assembly and stabilization. Blood 116(22):4720–4730PubMedPubMedCentralCrossRefGoogle Scholar
  130. Sundberg C et al (1996) Pericytes as collagen-producing cells in excessive dermal scarring. Lab Investig 74(2):452–466PubMedPubMedCentralGoogle Scholar
  131. Tao YK et al (2017) Notch3 deficiency impairs coronary microvascular maturation and reduces cardiac recovery after myocardial ischemia. Int J Cardiol 236:413–422PubMedPubMedCentralCrossRefGoogle Scholar
  132. Tattersall IW et al (2016) In vitro modeling of endothelial interaction with macrophages and pericytes demonstrates notch signaling function in the vascular microenvironment. Angiogenesis 19(2):201–215PubMedPubMedCentralCrossRefGoogle Scholar
  133. Teichert M et al (2017) Pericyte-expressed Tie2 controls angiogenesis and vessel maturation. Nat Commun 8:16106PubMedPubMedCentralCrossRefGoogle Scholar
  134. Tillet E et al (2005) N-cadherin deficiency impairs pericyte recruitment, and not endothelial differentiation or sprouting, in embryonic stem cell-derived angiogenesis. Exp Cell Res 310(2):392–400PubMedCrossRefPubMedCentralGoogle Scholar
  135. Tintut Y et al (2003) Multilineage potential of cells from the artery wall. Circulation 108(20):2505–2510PubMedCrossRefPubMedCentralGoogle Scholar
  136. Toma I, McCaffrey TA (2012) Transforming growth factor-beta and atherosclerosis: interwoven atherogenic and atheroprotective aspects. Cell Tissue Res 347(1):155–175PubMedCrossRefPubMedCentralGoogle Scholar
  137. Travers JG et al (2016) Cardiac fibrosis: the fibroblast awakens. Circ Res 118(6):1021–1040PubMedPubMedCentralCrossRefGoogle Scholar
  138. van Amerongen MJ et al (2008) Bone marrow-derived myofibroblasts contribute functionally to scar formation after myocardial infarction. J Pathol 214(3):377–386PubMedCrossRefPubMedCentralGoogle Scholar
  139. van Dijk CG et al (2015) The complex mural cell: pericyte function in health and disease. Int J Cardiol 190:75–89PubMedCrossRefGoogle Scholar
  140. Volz KS et al (2015) Pericytes are progenitors for coronary artery smooth muscle. Elife 4Google Scholar
  141. Wakui S et al (2006) Localization of Ang-1, −2, Tie-2, and VEGF expression at endothelial-pericyte interdigitation in rat angiogenesis. Lab Investig 86(11):1172–1184PubMedCrossRefPubMedCentralGoogle Scholar
  142. Wanjare M, Kusuma S, Gerecht S (2013) Perivascular cells in blood vessel regeneration. Biotechnol J 8(4):434–447PubMedPubMedCentralCrossRefGoogle Scholar
  143. Watanabe N et al (2004) Three-dimensional microstructural abnormality of the coronary capillary network after myocardial reperfusion—comparison between ‘reflow’ and ‘no-reflow’. Circ J 68(9):868–872PubMedCrossRefPubMedCentralGoogle Scholar
  144. Weiss DR et al (2009) Extensive deendothelialization and thrombogenicity in routinely prepared vein grafts for coronary bypass operations: facts and remedy. Int J Clin Exp Med 2(2):95–113PubMedPubMedCentralGoogle Scholar
  145. Weiss RM, Miller JD, Heistad DD (2013) Fibrocalcific aortic valve disease: opportunity to understand disease mechanisms using mouse models. Circ Res 113(2):209–222PubMedPubMedCentralCrossRefGoogle Scholar
  146. Winkler EA, Bell RD, Zlokovic BV (2010) Pericyte-specific expression of PDGF beta receptor in mouse models with normal and deficient PDGF beta receptor signaling. Mol Neurodegener 5:32PubMedPubMedCentralCrossRefGoogle Scholar
  147. Winkler EA, Bell RD, Zlokovic BV (2011) Central nervous system pericytes in health and disease. Nat Neurosci 14(11):1398–1405PubMedPubMedCentralCrossRefGoogle Scholar
  148. Wong SP et al (2015) Pericytes, mesenchymal stem cells and their contributions to tissue repair. Pharmacol Ther 151:107–120PubMedCrossRefGoogle Scholar
  149. Wu M, Rementer C, Giachelli CM (2013) Vascular calcification: an update on mechanisms and challenges in treatment. Calcif Tissue Int 93(4):365–373PubMedPubMedCentralCrossRefGoogle Scholar
  150. Yannarelli G et al (2013) Human umbilical cord perivascular cells exhibit enhanced cardiomyocyte reprogramming and cardiac function after experimental acute myocardial infarction. Cell Transplant 22(9):1651–1666PubMedCrossRefPubMedCentralGoogle Scholar
  151. Yemisci M et al (2009) Pericyte contraction induced by oxidative-nitrative stress impairs capillary reflow despite successful opening of an occluded cerebral artery. Nat Med 15(9):1031–1037PubMedCrossRefPubMedCentralGoogle Scholar
  152. Zeng H et al (2016) LPS causes pericyte loss and microvascular dysfunction via disruption of Sirt3/angiopoietins/Tie-2 and HIF-2alpha/Notch3 pathways. Sci Rep 6:20931PubMedPubMedCentralCrossRefGoogle Scholar
  153. Zhou Z et al (2016) Induction of initial steps of angiogenic differentiation and maturation of endothelial cells by pericytes in vitro and the role of collagen IV. Histochem Cell Biol 145(5):511–525PubMedCrossRefPubMedCentralGoogle Scholar

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© Springer Nature Switzerland AG 2019

Authors and Affiliations

  1. 1.Department of CardioMetabolic Disorders, Amgen Research and DiscoveryAmgen Inc.South San FranciscoUSA

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