Abstract
Although periostin plays a significant role in adult cardiac remodeling diseases, the focus of this review is on periostin as a valvulogenic gene. Periostin is expressed throughout valvular development, initially being expressed in endocardial endothelial cells that have been activated to transform into prevalvular mesenchyme termed “cushion tissues” that sustain expression of periostin throughout their morphogenesis into mature (compacted) valve leaflets. The phenotype of periostin null indicates that periostin is not required for endocardial transformation nor the proliferation of its mesenchymal progeny but rather promotes cellular behaviors that promote migration, survival (anti-apoptotic), differentiation into fibroblastic lineages, collagen secretion and postnatal remodeling/maturation. These morphogenetic activities are promoted or coordinated by periostin signaling through integrin receptors activating downstream kinases in cushion cells that activate hyaluronan synthetase II (Akt/PI3K), collagen synthesis (Erk/MapK) and changes in cytoskeletal organization (Pak1) which regulate postnatal remodeling of cells and associated collagenous matrix into a trilaminar (zonal) histoarchitecture. Pak1 binding to filamin A is proposed as one mechanism by which periostin supports remodeling. The failure to properly remodel cushions sets up a trajectory of degenerative (myxomatous-like) changes that over time reduce biomechanical properties and increase chances for prolapse, regurgitation or calcification of the leaflets. Included in the review are considerations of lineage diversity and the role of periostin as a determinant of mesenchymal cell fate.
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Benson DW (2008) Thar’s tendons in them thar valves! Circ Res 103:914–915
Butcher JT, McQuinn TC, Sedmera D, Turner D, Markwald RR (2007a) Transitions in early embryonic atrioventricular valvular function correspond with changes in cushion biomechanics that are predictable by tissue composition. Circ Res 100:1503–1511
Butcher JT, Norris RA, Hoffman S, Mjaatvedt CH, Markwald RR (2007b) Periostin promotes atrioventricular mesenchyme matrix invasion and remodeling mediated by integrin signaling through Rho/PI 3-kinase. Dev Biol 302:256–266
Conway SJ, Doetschman T, Azhar M (2011) The inter-relationship of periostin, TGF beta, and BMP in heart valve development and valvular heart diseases. Sci World J 11:1509–1524
Conway SJ, Izuhara K, Kudo Y, Litvin J, Markwald R, Ouyang G, Arron JR, Holweg CT, Kudo A (2014) The role of periostin in tissue remodeling across health and disease. Cell Mol Life Sci 71:1279–1288
de la Cruz M, Markwald R (1998) Embryological development of the ventricular inlets. Septation and atrioventricular valve apparatus. In: de la Cruz M, Markwald R (eds) Living morphogenesis of the heart. Springer, Boston, pp 131–156
de la Pompa JL, Epstein JA (2012) Coordinating tissue interactions: notch signaling in cardiac development and disease. Dev Cell 22:244–254
de Lange FJ, Moorman AF, Anderson RH, Manner J, Soufan AT, de Gier-de Vries C, Schneider MD, Webb S, van den Hoff MJ, Christoffels VM (2004) Lineage and morphogenetic analysis of the cardiac valves. Circ Res 95:645–654
de Vlaming A, Sauls K, Hajdu Z, Visconti RP, Mehesz AN, Levine RA, Slaugenhaupt SA, Hagege A, Chester AH, Markwald RR, Norris RA (2012) Atrioventricular valve development: new perspectives on an old theme. Differentiation 84:103–116
Durst R, Sauls K, Peal DS, deVlaming A, Toomer K, Leyne M, Salani M, Talkowski ME, Brand H, Perrocheau M, Simpson C, Jett C, Stone MR, Charles F, Chiang C, Lynch SN, Bouatia-Naji N, Delling FN, Freed LA, Tribouilloy C, Le Tourneau T, LeMarec H, Fernandez-Friera L, Solis J, Trujillano D, Ossowski S, Estivill X, Dina C, Bruneval P, Chester A, Schott JJ, Irvine KD, Mao Y, Wessels A, Motiwala T, Puceat M, Tsukasaki Y, Menick DR, Kasiganesan H, Nie X, Broome AM, Williams K, Johnson A, Markwald RR, Jeunemaitre X, Hagege A, Levine RA, Milan DJ, Norris RA, Slaugenhaupt SA (2015) Mutations in DCHS1 cause mitral valve prolapse. Nature 525:109–113
Eisenberg LM, Markwald RR (1995) Molecular regulation of atrioventricular valvuloseptal morphogenesis. Circ Res 77:1–6
Evans HJ, Sweet JK, Price RL, Yost M, Goodwin RL (2003) Novel 3D culture system for study of cardiac myocyte development. Am J Physiol Heart Circ Physiol 285:H570–H578
Furtado MB, Costa MW, Pranoto EA, Salimova E, Pinto AR, Lam NT, Park A, Snider P, Chandran A, Harvey RP, Boyd R, Conway SJ, Pearson J, Kaye DM, Rosenthal NA (2014) Cardiogenic genes expressed in cardiac fibroblasts contribute to heart development and repair. Circ Res 114:1422–1434
Ghatak S, Misra S, Hascal VC, Leone GV, Markwald RR (2019) Periostin b1 integrin interaction regulates p21-activated kinases in valvular interstitial cell survival and in actin cytoskeleton reorganization. Biochim Biophys Acta
Ghatak S, Misra S, Norris RA, Moreno-Rodriguez RA, Hoffman S, Levine RA, Hascall VC, Markwald RR (2014) Periostin induces intracellular cross-talk between kinases and hyaluronan in atrioventricular valvulogenesis. J Biol Chem 289:8545–8561
Goodwin RL, Nesbitt T, Price RL, Wells JC, Yost MJ, Potts JD (2005) Three-dimensional model system of valvulogenesis. Dev Dyn 233:122–129
Grinnell F (2003) Fibroblast biology in three-dimensional collagen matrices. Trends Cell Biol 13:264–269
Hajdu Z, Romeo SJ, Fleming PA, Markwald RR, Visconti RP, Drake CJ (2011) Recruitment of bone marrow-derived valve interstitial cells is a normal homeostatic process. J Mol Cell Cardiol 51:955–965
Hinton RB, Yutzey KE (2011) Heart valve structure and function in development and disease. Annu Rev Physiol 73:29–46
Kolditz DP, Wijffels MC, Blom NA, van der Laarse A, Hahurij ND, Lie-Venema H, Markwald RR, Poelmann RE, Schalij MJ, Gittenberger-de Groot AC (2008) Epicardium-derived cells in development of annulus fibrosis and persistence of accessory pathways. Circulation 117:1508–1517
Kruithof BP, Krawitz SA, Gaussin V (2007) Atrioventricular valve development during late embryonic and postnatal stages involves condensation and extracellular matrix remodeling. Dev Biol 302:208–217
Kudo A (2011) Periostin in fibrillogenesis for tissue regeneration: periostin actions inside and outside the cell. Cell Mol Life Sci 68:3201–3207
Kudo A, Kii I (2018) Periostin function in communication with extracellular matrices. J Cell Commun Signal 12:301–308
Levay AK, Peacock JD, Lu Y, Koch M, Hinton RB Jr, Kadler KE, Lincoln J (2008) Scleraxis is required for cell lineage differentiation and extracellular matrix remodeling during murine heart valve formation in vivo. Circ Res 103:948–956
Levine RA, Hagege AA, Judge DP, Padala M, Dal-Bianco JP, Aikawa E, Beaudoin J, Bischoff J, Bouatia-Naji N, Bruneval P, Butcher JT, Carpentier A, Chaput M, Chester AH, Clusel C, Delling FN, Dietz HC, Dina C, Durst R, Fernandez-Friera L, Handschumacher MD, Jensen MO, Jeunemaitre XP, Le Marec H, Le Tourneau T, Markwald RR, Merot J, Messas E, Milan DP, Neri T, Norris RA, Peal D, Perrocheau M, Probst V, Puceat M, Rosenthal N, Solis J, Schott JJ, Schwammenthal E, Slaugenhaupt SA, Song JK, Yacoub MH (2015) Mitral valve disease--morphology and mechanisms. Nat Rev Cardiol 12:689–710
Lie-Venema H, Eralp I, Markwald RR, van den Akker NM, Wijffels MC, Kolditz DP, van der Laarse A, Schalij MJ, Poelmann RE, Bogers AJ, Gittenberger-de Groot AC (2008) Periostin expression by epicardium-derived cells is involved in the development of the atrioventricular valves and fibrous heart skeleton. Differentiation 76:809–819
Lockhart MM, van den Hoff M, Wessels A (2016) The role of the epicardium in the formation of the cardiac valves in the mouse. In: Nakanishi T, Markwald RR, Baldwin HS, Keller BB, Srivastava D, Yamagishi H (eds) Etiology and morphogenesis of congenital heart disease: from gene function and cellular interaction to morphology. Springer, Tokyo, pp 161–167
Markwald RR, Norris RA, Moreno-Rodriguez R, Levine RA (2010) Developmental basis of adult cardiovascular diseases: valvular heart diseases. Ann N Y Acad Sci 1188:177–183. Review
Mjaatvedt CH, Nakaoka T, Moreno-Rodriguez R, Norris RA, Kern MJ, Eisenberg CA, Turner D, Markwald RR (2001) The outflow tract of the heart is recruited from a novel heart-forming Field. Dev Biol 238:97–109
Nakano H, Liu X, Arshi A, Nakashima Y, van Handel B, Sasidharan R, Harmon AW, Shin JH, Schwartz RJ, Conway SJ, Harvey RP, Pashmforoush M, Mikkola HK, Nakano A (2013) Haemogenic endocardium contributes to transient definitive haematopoiesis. Nat Commun 4:1564
Niu Z, Iyer D, Conway SJ, Martin JF, Ivey K, Srivastava D, Nordheim A, Schwartz RJ (2008) Serum response factor orchestrates nascent sarcomerogenesis and silences the biomineralization gene program in the heart. Proc Natl Acad Sci U S A 105:17824–17829
Nkomo VT, Gardin JM, Skelton TN, Gottdiener JS, Scott CG, Enriquez-Sarano M (2006) Burden of valvular heart diseases: a population-based study. Lancet 368:1005–1011
Norris RA, Damon B, Mironov V, Kasyanov V, Ramamurthi A, Moreno-Rodriguez R, Trusk T, Potts JD, Goodwin RL, Davis J, Hoffman S, Wen X, Sugi Y, Kern CB, Mjaatvedt CH, Turner DK, Oka T, Conway SJ, Molkentin JD, Forgacs G, Markwald RR (2007) Periostin regulates collagen fibrillogenesis and the biomechanical properties of connective tissues. J Cell Biochem 101:695–711
Norris RA, Moreno-Rodriguez RA, Sugi Y, Hoffman S, Amos J, Hart MM, Potts JD, Goodwin RL, Markwald RR (2008) Periostin regulates atrioventricular valve maturation. Dev Biol 316:200–213
Norris RA, Moreno-Rodriguez R, Hoffman S, Markwald RR (2009a) The many facets of the matricelluar protein periostin during cardiac development, remodeling, and pathophysiology. J Cell Commun Signal 3:275–286
Norris RA, Potts JD, Yost MJ, Junor L, Brooks T, Tan H, Hoffman S, Hart MM, Kern MJ, Damon B, Markwald RR, Goodwin RL (2009b) Periostin promotes a fibroblastic lineage pathway in atrioventricular valve progenitor cells. Dev Dyn 238:1052–1063
Norris RA, Moreno-Rodriguez R, Wessels A, Merot J, Bruneval P, Chester AH, Yacoub MH, Hagège A, Slaugenhaupt SA, Aikawa E, Schott JJ, Lardeux A, Harris BS, Williams LK, Richards A, Levine RA, Markwald RR (2010) Expression of the familial cardiac valvular dystrophy gene, filamin-A, during heart morphogenesis. Dev Dyn 239(7):2118–2127
Oku E, Kanaji T, Takata Y, Oshima K, Seki R, Morishige S, Imamura R, Ohtsubo K, Hashiguchi M, Osaki K, Yakushiji K, Yoshimoto K, Ogata H, Hamada H, Izuhara K, Sata M, Okamura T (2008) Periostin and bone marrow fibrosis. Int J Hematol 88:57–63
Person AD, Klewer SE, Runyan RB (2005) Cell biology of cardiac cushion development. Int Rev Cytol 243:287–335
Rog-Zielinska EA, Norris RA, Kohl P, Markwald R (2016) The living scar--cardiac fibroblasts and the injured heart. Trends Mol Med 22:99–114
Sauls K, de Vlaming A, Harris BS, Williams K, Wessels A, Levine RA, Slaugenhaupt SA, Goodwin RL, Pavone LM, Merot J, Schott JJ, Le Tourneau T, Dix T, Jesinkey S, Feng Y, Walsh C, Zhou B, Baldwin S, Markwald RR, Norris RA (2012) Developmental basis for filamin-A-associated myxomatous mitral valve disease. Cardiovasc Res 96:109–119
Sauls K, Toomer K, Williams K, Johnson AJ, Markwald RR, Hajdu Z, Norris RA (2015) Increased infiltration of extra-cardiac cells in myxomatous valve disease. J Cardiovas Dev Dis 2:200–213
Sedmera D, Pexieder T, Rychterova V, Hu N, Clark EB (1999) Remodeling of chick embryonic ventricular myoarchitecture under experimentally changed loading conditions. Anat Rec 254:238–252
Seifert GJ (2018) Fascinating fasciclins: a surprisingly widespread family of proteins that mediate interactions between the cell exterior and the cell surface. Int J Mol Sci 19
Snider P, Hinton RB, Moreno-Rodriguez RA, Wang J, Rogers R, Lindsley A, Li F, Ingram DA, Menick D, Field L, Firulli AB, Molkentin JD, Markwald R, Conway SJ (2008) Periostin is required for maturation and extracellular matrix stabilization of noncardiomyocyte lineages of the heart. Circ Res 102:752–760
Sugi Y, Ito N, Szebenyi G, Myers K, Fallon JF, Mikawa T, Markwald RR (2003) Fibroblast growth factor (FGF)-4 can induce proliferation of cardiac cushion mesenchymal cells during early valve leaflet formation. Dev Biol 258:252–263
Sugi Y, Kern MJ, Markwald RR, Burnside JL (2012) Periostin expression is altered in aortic valves in Smad6 mutant mice. J Neonatal Biol 1
Sugi Y, Sasse J, Lough J (1993) Inhibition of Precardiac mesoderm cell proliferation by antisense Oligodeoxynucleotide complementary to fibroblast growth Factor-2 (FGF-2). Dev Biol 157:28–37
Sugi Y, Yamamura H, Okagawa H, Markwald RR (2004) Bone morphogenetic protein-2 can mediate myocardial regulation of atrioventricular cushion mesenchymal cell formation in mice. Dev Biol 269:505–518
Tanabe H, Takayama I, Nishiyama T, Shimazaki M, Kii I, Li M, Amizuka N, Katsube K, Kudo A (2010) Periostin associates with Notch1 precursor to maintain Notch1 expression under a stress condition in mouse cells. PLoS One 5:e12234
Tkatchenko TV, Moreno-Rodriguez RA, Conway SJ, Molkentin JD, Markwald RR, Tkatchenko AV (2009) Lack of periostin leads to suppression of Notch1 signaling and calcific aortic valve disease. Physiol Genomics 39:160–168
Toomer K, Sauls K, Fulmer D, Guo L, Moore K, Glover J, Stairley R, Bischoff J, Levine RA, Norris RA (2019) Filamin-A as a balance between Erk/Smad activities during cardiac valve development. Anat Rec 302(1):117–124
Toomer KA, Fulmer D, Guo L, Drohan A, Peterson N, Swanson P, Brooks B, Mukherjee R, Body S, Lipschutz JH, Wessels A, Norris RA (2017) A role for primary cilia in aortic valve development and disease. Dev Dyn 246:625–634
Vadlamudi RK, Li F, Adam L, Nguyen D, Ohta Y, Stossel TP, Kumar R (2002) Filamin is essential in actin cytoskeletal assembly mediated by p21-activated kinase 1. Nat Cell Biol 4:681–690
Visconti RP, Ebihara Y, LaRue AC, Fleming PA, McQuinn TC, Masuya M, Minamiguchi H, Markwald RR, Ogawa M, Drake CJ (2006) An in vivo analysis of hematopoietic stem cell potential: hematopoietic origin of cardiac valve interstitial cells. Circ Res 98:690–696
Visconti RP, Markwald RR (2006) Recruitment of new cells into the postnatal heart: potential modification of phenotype by periostin. Ann N Y Acad Sci 1080:19–33
Yost MJ, Baicu CF, Stonerock CE, Goodwin RL, Price RL, Davis JM, Evans H, Watson PD, Gore CM, Sweet J, Creech L, Zile MR, Terracio L (2004) A novel tubular scaffold for cardiovascular tissue engineering. Tissue Eng 10:273–284
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Markwald, R.R., Moreno-Rodriguez, R.A., Ghatak, S., Misra, S., Norris, R.A., Sugi, Y. (2019). Role of Periostin in Cardiac Valve Development. In: Kudo, A. (eds) Periostin. Advances in Experimental Medicine and Biology, vol 1132. Springer, Singapore. https://doi.org/10.1007/978-981-13-6657-4_17
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