Advertisement

Periostin pp 163-176 | Cite as

Periostin and Integrin Signaling in Stem Cell Regulation

  • Athira Suresh
  • Atreyi Biswas
  • Saravana Perumal
  • Satish KhuranaEmail author
Chapter
Part of the Advances in Experimental Medicine and Biology book series (AEMB, volume 1132)

Abstract

Stem cell function is regulated by a huge repertoire of external cues along with stem cell intrinsic genetic and epigenetic factors. These interactions come through a variety of cell adhesion receptors, of which integrins are one of the most important classes. They interact with extracellular matrix (ECM) components and various bound proteins. Apart from inside-out signaling through which integrins ensure that the cells are stably bound to the ECM, outside-in integrin signaling, through binding to a variety of ligands, play important roles in cell fate decisions. Periostin is one such ligand whose role in functional regulation of stem cells is emerging due to its wide expression profile. In this review, we discuss the recent advancements made in the field.

Keywords

Periostin Integrins Stem cells Proliferation Stemness Differentiation 

Notes

Acknowledgements

This work was supported by the Wellcome Trust/DBT India Alliance Fellowship (IA/I/15/2/502061) awarded to SK and intramural funds from Indian Institute of Science Education and Research Thiruvananthapuram (IISER TVM). AS is supported by INSPIRE fellowship from Department of Science and Technology, Government of India Scientific and Industrial Research, India. AB is supported by IISER TVM.

References

  1. 1.
    Melton D (2014) Chapter 2 – ‘Stemness’: definitions, criteria, and standards. In: Lanza R, Atala A (eds) Essentials of stem cell biology, 3rd edn. Academic, Boston, pp 7–17CrossRefGoogle Scholar
  2. 2.
    Cheung TH, Rando TA (2013) Molecular regulation of stem cell quiescence. Nat Rev Mol Cell Biol 14(6):329–340PubMedCrossRefGoogle Scholar
  3. 3.
    Jones DL, Wagers AJ (2008) No place like home: anatomy and function of the stem cell niche. Nat Rev Mol Cell Biol 9(1):11–21PubMedCrossRefGoogle Scholar
  4. 4.
    Beerman I, Seita J, Inlay MA, Weissman IL, Rossi DJ (2014) Quiescent hematopoietic stem cells accumulate DNA damage during aging that is repaired upon entry into cell cycle. Cell Stem Cell 15(1):37–50PubMedPubMedCentralCrossRefGoogle Scholar
  5. 5.
    So WK, Cheung TH (2018) Molecular regulation of cellular quiescence: a perspective from adult stem cells and its niches. Cell Quiescence Methods Protoc 1686:1–25CrossRefGoogle Scholar
  6. 6.
    Lombard DB, Chua KF, Mostoslavsky R, Franco S, Gostissa M, Alt FW (2005) DNA repair, genome stability, and aging. Cell 120(4):497–512PubMedCrossRefGoogle Scholar
  7. 7.
    Tothova Z, Gilliland DG (2007) FoxO transcription factors and stem cell homeostasis: insights from the hematopoietic system. Cell Stem Cell 1(2):140–152PubMedCrossRefGoogle Scholar
  8. 8.
    Khurana S (2016) The effects of proliferation and DNA damage on hematopoietic stem cell function determine aging. Dev Dyn 245(7):739–750PubMedCrossRefGoogle Scholar
  9. 9.
    Bjornson CRR, Cheung TH, Liu L, Tripathi PV, Steeper KM, Rando TA (2012) Notch signaling is necessary to maintain quiescence in adult muscle stem cells. Stem Cells 30(2):232–242PubMedPubMedCentralCrossRefGoogle Scholar
  10. 10.
    Simon MC, Keith B (2008) The role of oxygen availability in embryonic development and stem cell function. Nat Rev Mol Cell Biol 9(4):285–296PubMedPubMedCentralCrossRefGoogle Scholar
  11. 11.
    Roy IM, Biswas A, Verfaillie C, Khurana S (2018) Energy producing metabolic pathways in functional regulation of the hematopoietic stem cells. IUBMB Life 70(7):612–624PubMedCrossRefGoogle Scholar
  12. 12.
    Legate KR, Wickstrom SA, Fassler R (2009) Genetic and cell biological analysis of integrin outside-in signaling. Genes Dev 23(4):397–418PubMedCrossRefGoogle Scholar
  13. 13.
    Kudo Y, Siriwardena BS, Hatano H, Ogawa I, Takata T (2007) Periostin: novel diagnostic and therapeutic target for cancer. Histol Histopathol 22(10):1167–1174PubMedPubMedCentralGoogle Scholar
  14. 14.
    Takeshita S, Kikuno R, Tezuka K, Amann E (1993) Osteoblast-specific factor 2: cloning of a putative bone adhesion protein with homology with the insect protein fasciclin I. Biochem J 294(Pt 1):271–278CrossRefPubMedPubMedCentralGoogle Scholar
  15. 15.
    Merle B, Garnero P (2012) The multiple facets of periostin in bone metabolism. Osteoporos Int 23(4):1199–1212CrossRefPubMedGoogle Scholar
  16. 16.
    Bornstein P (2009) Matricellular proteins: an overview. J Cell Commun Signal 3(3–4):163–165PubMedPubMedCentralCrossRefGoogle Scholar
  17. 17.
    Kudo A (2011) Periostin in fibrillogenesis for tissue regeneration: periostin actions inside and outside the cell. Cell Mol Life Sci 68(19):3201–3207PubMedPubMedCentralCrossRefGoogle Scholar
  18. 18.
    Kudo A (2017) Introductory review: periostin-gene and protein structure. Cell Mol Life Sci 74(23):4259–4268CrossRefPubMedGoogle Scholar
  19. 19.
    Ruan K, Bao S, Ouyang G (2009) The multifaceted role of periostin in tumorigenesis. Cell Mol Life Sci 66(14):2219–2230PubMedPubMedCentralCrossRefGoogle Scholar
  20. 20.
    Rios H, Koushik SV, Wang H et al (2005) periostin null mice exhibit dwarfism, incisor enamel defects, and an early-onset periodontal disease-like phenotype. Mol Cell Biol 25(24):11131–11144PubMedPubMedCentralCrossRefGoogle Scholar
  21. 21.
    Norris RA, Kern CB, Wessels A, Moralez EI, Markwald RR, Mjaatvedt CH (2004) Identification and detection of the periostin gene in cardiac development. Anat Rec A Discov Mol Cell Evol Biol 281(2):1227–1233PubMedCrossRefGoogle Scholar
  22. 22.
    Kii I, Nishiyama T, Li M et al (2010) Incorporation of tenascin-C into the extracellular matrix by periostin underlies an extracellular meshwork architecture. J Biol Chem 285(3):2028–2039CrossRefPubMedGoogle Scholar
  23. 23.
    Norris RA, Damon B, Mironov V et al (2007) Periostin regulates collagen fibrillogenesis and the biomechanical properties of connective tissues. J Cell Biochem 101(3):695–711PubMedPubMedCentralCrossRefGoogle Scholar
  24. 24.
    Horiuchi K, Amizuka N, Takeshita S et al (1999) Identification and characterization of a novel protein, periostin, with restricted expression to periosteum and periodontal ligament and increased expression by transforming growth factor beta. J Bone Miner Res 14(7):1239–1249CrossRefPubMedGoogle Scholar
  25. 25.
    Klamer S, Voermans C (2014) The role of novel and known extracellular matrix and adhesion molecules in the homeostatic and regenerative bone marrow microenvironment. Cell Adhes Migr 8(6):563–577CrossRefGoogle Scholar
  26. 26.
    Zhang F, Rong Z, Wang Z et al (2017) Periostin promotes ectopic osteogenesis of CTLA4-modified bone marrow mesenchymal stem cells. Cell Tissue Res 370(1):143–151CrossRefPubMedGoogle Scholar
  27. 27.
    Bonnet N, Standley KN, Bianchi EN et al (2009) The matricellular protein periostin is required for sost inhibition and the anabolic response to mechanical loading and physical activity. J Biol Chem 284(51):35939–35950PubMedPubMedCentralCrossRefGoogle Scholar
  28. 28.
    Gillan L, Matei D, Fishman DA, Gerbin CS, Karlan BY, Chang DD (2002) Periostin secreted by epithelial ovarian carcinoma is a ligand for alpha(V)beta(3) and alpha(V)beta(5) integrins and promotes cell motility. Cancer Res 62(18):5358–5364PubMedGoogle Scholar
  29. 29.
    Luo BH, Carman CV, Springer TA (2007) Structural basis of integrin regulation and signaling. Annu Rev Immunol 25:619–647PubMedPubMedCentralCrossRefGoogle Scholar
  30. 30.
    Hynes RO (2002) Integrins: bidirectional, allosteric signaling machines. Cell 110(6):673–687PubMedCrossRefGoogle Scholar
  31. 31.
    Takada Y, Ye X, Simon S (2007) The integrins. Genome Biol 8(5):215PubMedPubMedCentralCrossRefGoogle Scholar
  32. 32.
    Amlot PL, Hayes AE (1985) Impaired human antibody response to the thymus-independent antigen, DNP-Ficoll, after splenectomy. Implications for post-splenectomy infections. Lancet 1(8436):1008–1011PubMedCrossRefGoogle Scholar
  33. 33.
    Barczyk M, Carracedo S, Gullberg D (2010) Integrins. Cell Tissue Res 339(1):269–280PubMedCrossRefGoogle Scholar
  34. 34.
    Dorn GW (2007) Periostin and myocardial repair, regeneration, and recovery. N Engl J Med 357(15):1552–1554PubMedCrossRefGoogle Scholar
  35. 35.
    Bao SD, Ouyang G, Bai XF et al (2004) Periostin potently promotes metastatic growth of colon cancer by augmenting cell survival via the Akt/PKB pathway. Cancer Cell 5(4):329–339PubMedCrossRefGoogle Scholar
  36. 36.
    Bilezikian JP, Raisz LG, Martin TJ (2008) Principles of bone biology, 3rd edn, vol 2. Preface to the Third Edition, pp xxi–xxiCrossRefGoogle Scholar
  37. 37.
    Duchamp de Lageneste O, Julien A, Abou-Khalil R et al (2018) Periosteum contains skeletal stem cells with high bone regenerative potential controlled by Periostin. Nat Commun 9(1):773PubMedPubMedCentralCrossRefGoogle Scholar
  38. 38.
    Nakazawa T, Nakajima A, Seki N et al (2004) Gene expression of periostin in the early stage of fracture healing detected by cDNA microarray analysis. J Orthop Res 22(3):520–525CrossRefPubMedGoogle Scholar
  39. 39.
    Canalis E, Economides AN, Gazzerro E (2003) Bone morphogenetic proteins, their antagonists, and the skeleton. Endocr Rev 24(2):218–235PubMedCrossRefGoogle Scholar
  40. 40.
    Litvin J, Selim AH, Montgomery MO et al (2004) Expression and function of periostin-isoforms in bone. J Cell Biochem 92(5):1044–1061CrossRefPubMedGoogle Scholar
  41. 41.
    Bonnet N, Gineyts E, Ammann P, Conway SJ, Garnero P, Ferrari S (2013) Periostin deficiency increases bone damage and impairs injury response to fatigue loading in adult mice. PLoS One 8(10):e78347PubMedPubMedCentralCrossRefGoogle Scholar
  42. 42.
    Zhang F, Luo KY, Rong ZG et al (2017) Periostin upregulates Wnt/beta-Catenin signaling to promote the osteogenesis of CTLA4-modified human bone marrow-mesenchymal stem cells. Sci Rep 7:41634PubMedPubMedCentralCrossRefGoogle Scholar
  43. 43.
    Butcher JT, Norris RA, Hoffman S, Mjaatvedt CH, Markwald RR (2007) Periostin promotes atrioventricular mesenchyme matrix invasion and remodeling mediated by integrin signaling through Rho/PI 3-kinase. Dev Biol 302(1):256–266PubMedCrossRefGoogle Scholar
  44. 44.
    Kim CJ, Isono T, Tambe Y et al (2008) Role of alternative splicing of periostin in human bladder carcinogenesis. Int J Oncol 32(1):161–169PubMedGoogle Scholar
  45. 45.
    Wu ZQ, Dai WY, Wang P et al (2018) Periostin promotes migration, proliferation, and differentiation of human periodontal ligament mesenchymal stem cells. Connect Tissue Res 59(2):108–119PubMedCrossRefGoogle Scholar
  46. 46.
    Tang Y, Liu L, Wang P, Chen DL, Wu ZQ, Tang CB (2017, Dec) Periostin promotes migration and osteogenic differentiation of human periodontal ligament mesenchymal stem cells via the Jun amino-terminal kinases (JNK) pathway under inflammatory conditions. Cell Prolif 50(6)CrossRefGoogle Scholar
  47. 47.
    Heo SC, Lee KO, Shin SH et al (2011) Periostin mediates human adipose tissue-derived mesenchymal stem cell-stimulated tumor growth in a xenograft lung adenocarcinoma model. BBA-Mol Cell Res 1813(12):2061–2070Google Scholar
  48. 48.
    Latroche C, Weiss-Gayet M, Muller L et al (2017) Coupling between myogenesis and angiogenesis during skeletal muscle regeneration is stimulated by restorative macrophages. Stem Cell Rep 9(6):2018–2033CrossRefGoogle Scholar
  49. 49.
    Hong L, Dai SJ, Chen FR, Gang Z, Lei D (2015) Periostin down-regulation attenuates the pro-fibrogenic response of hepatic stellate cells induced by TGF-1. J Cell Mol Med 19(10):2462–2468PubMedPubMedCentralCrossRefGoogle Scholar
  50. 50.
    Jagannathan-Bogdan M, Zon LI (2013) Hematopoiesis. Development 140(12):2463–2467PubMedPubMedCentralCrossRefGoogle Scholar
  51. 51.
    Morrison SJ, Scadden DT (2014) The bone marrow niche for haematopoietic stem cells. Nature 505(7483):327–334PubMedPubMedCentralCrossRefGoogle Scholar
  52. 52.
    Wilson A, Trumpp A (2006) Bone-marrow haematopoietic-stem-cell niches. Nat Rev Immunol 6(2):93–106PubMedCrossRefGoogle Scholar
  53. 53.
    Grassinger J, Haylock DN, Storan MJ et al (2009) Thrombin-cleaved osteopontin regulates hemopoietic stem and progenitor cell functions through interactions with alpha(9)beta(1) and alpha(4)beta(1) integrins. Blood 114(1):49–59PubMedCrossRefGoogle Scholar
  54. 54.
    Papayannopoulou T, Nakamoto B (1993) Peripheralization of hematopoietic progenitors in primates treated with anti-Vla4 integrin. Proc Natl Acad Sci U S A 90(20):9374–9378PubMedPubMedCentralCrossRefGoogle Scholar
  55. 55.
    van der Loo JCM, Xiao XL, McMillin D, Hashino K, Kato I, Williams DA (1998) VLA-5 is expressed by mouse and human long-term repopulating hematopoietic cells and mediates adhesion to extracellular matrix protein fibronectin. J Clin Investig 102(5):1051–1061PubMedCrossRefGoogle Scholar
  56. 56.
    Hirsch E, Iglesias A, Potocnik AJ, Hartmann U, Fassler R (1996) Impaired migration but not differentiation of haematopoietic stem cells in the absence of beta(1) integrins. Nature 380(6570):171–175PubMedCrossRefGoogle Scholar
  57. 57.
    Scott LM, Priestley GV, Papayannopoulou T (2003) Deletion of alpha 4 integrins from adult hematopoietic cells reveals roles in homeostasis, regeneration, and homing. Mol Cell Biol 23(24):9349–9360PubMedPubMedCentralCrossRefGoogle Scholar
  58. 58.
    Umemoto T, Yamato M, Shiratsuchi Y et al (2008) CD61 enriches long-term repopulating hematopoietic stem cells. Biochem Biophys Res Commun 365(1):176–182PubMedCrossRefGoogle Scholar
  59. 59.
    Umemoto T, Yamato M, Shiratsuchi Y et al (2006) Expression of integrin beta(3) is correlated to the properties of quiescent hemopoietic stem cells possessing the side population phenotype. J Immunol 177(11):7733–7739PubMedCrossRefGoogle Scholar
  60. 60.
    Khurana S, Schouteden S, Manesia JK et al (2016) Outside-in integrin signalling regulates haematopoietic stem cell function via Periostin-Itgav axis. Nat Commun 7:13500PubMedPubMedCentralCrossRefGoogle Scholar
  61. 61.
    Siewe BT, Kalis SL, Le PT et al (2011) In vitro requirement for periostin in B lymphopoiesis. Blood 117(14):3770–3779PubMedPubMedCentralCrossRefGoogle Scholar
  62. 62.
    Umemoto T, Yamato M, Ishihara J et al (2012) Integrin-alpha v beta 3 regulates thrombopoietin-mediated maintenance of hematopoietic stem cells. Blood 119(1):83–94PubMedPubMedCentralCrossRefGoogle Scholar
  63. 63.
    Umemoto T, Matsuzaki Y, Shiratsuchi Y et al (2017) Integrin alpha v beta 3 enhances the suppressive effect of interferon-gamma on hematopoietic stem cells. EMBO J 36(16):2390–2403PubMedPubMedCentralCrossRefGoogle Scholar
  64. 64.
    Dzierzak E, Bigas A (2018) Blood development: hematopoietic stem cell dependence and independence. Cell Stem Cell 22(5):639–651PubMedCrossRefGoogle Scholar
  65. 65.
    Potocnik AJ, Brakebusch C, Fassler R (2000) Fetal and adult hematopoietic stem cells require beta 1 integrin function for colonizing fetal liver, spleen, and bone marrow. Immunity 12(6):653–663PubMedCrossRefGoogle Scholar
  66. 66.
    Boisset JC, Clapes T, van der Linden R, Dzierzak E, Robin C (2013) Integrin alpha(IIb) (CD41) plays a role in the maintenance of hematopoietic stem cell activity in the mouse embryonic aorta. Biol Open 2(5):525–532PubMedPubMedCentralCrossRefGoogle Scholar
  67. 67.
    Bergiers I, Andrews T, Bolukbasi OV et al (2018, Mar 20) Single-cell transcriptomics reveals a new dynamical function of transcription factors during embryonic hematopoiesis. Elife 7Google Scholar
  68. 68.
    Huang K, Gao J, Du J et al (2016) Generation and analysis of GATA2w/eGFP human ESCs reveal ITGB3/CD61 as a reliable marker for defining hemogenic endothelial cells during hematopoiesis. Stem Cell Rep 7(5):854–868CrossRefGoogle Scholar
  69. 69.
    Altman J, Das GD (1965) Autoradiographic and histological evidence of postnatal hippocampal neurogenesis in rats. J Comp Neurol 124(3):319PubMedCrossRefGoogle Scholar
  70. 70.
    Bond AM, Ming GL, Song HJ (2015) Adult mammalian neural stem cells and neurogenesis: five decades later. Cell Stem Cell 17(4):385–395PubMedPubMedCentralCrossRefGoogle Scholar
  71. 71.
    Weiss S, Reynolds BA, Vescovi AL, Morshead C, Craig CG, vanderKooy D (1996) Is there a neural stem cell in the mammalian forebrain? Trends Neurosci 19(9):387–393PubMedCrossRefGoogle Scholar
  72. 72.
    Ming GL, Song HJ (2011) Adult neurogenesis in the mammalian brain: significant answers and significant questions. Neuron 70(4):687–702PubMedPubMedCentralCrossRefGoogle Scholar
  73. 73.
    Bonaguidi MA, Wheeler MA, Shapiro JS et al (2011) In vivo clonal analysis reveals self-renewing and multipotent adult neural stem cell characteristics. Cell 145(7):1142–1155PubMedPubMedCentralCrossRefGoogle Scholar
  74. 74.
    Calzolari F, Michel J, Baumgart EV, Theis F, Gotz M, Ninkovic J (2015) Fast clonal expansion and limited neural stem cell self-renewal in the adult subependymal zone. Nat Neurosci 18(4):490PubMedCrossRefGoogle Scholar
  75. 75.
    Reynolds BA, Weiss S (1992) Generation of neurons and astrocytes from isolated cells of the adult mammalian central-nervous-system. Science 255(5052):1707–1710PubMedCrossRefGoogle Scholar
  76. 76.
    Delgado AC, Ferron SR, Vicente D et al (2014) Endothelial NT-3 delivered by vasculature and CSF promotes quiescence of subependymal neural stem cells through nitric oxide induction. Neuron 83(3):572–585PubMedCrossRefGoogle Scholar
  77. 77.
    Kazanis I, Ffrench-Constant C (2011) Extracellular matrix and the neural stem cell niche. Dev Neurobiol 71(11):1006–1017PubMedPubMedCentralCrossRefGoogle Scholar
  78. 78.
    Porcheri C, Suter U, Jessberger S (2014) Dissecting integrin-dependent regulation of neural stem cell proliferation in the adult brain. J Neurosci 34(15):5222–5232PubMedCrossRefGoogle Scholar
  79. 79.
    Zhu SM, Barbe MF, Amin N et al (2008) Immunolocalization of periostin-like factor and periostin during embryogenesis. J Histochem Cytochem 56(4):329–345PubMedPubMedCentralCrossRefGoogle Scholar
  80. 80.
    Shimamura M, Taniyama Y, Katsuragi N et al (2012) Role of central nervous system periostin in cerebral ischemia. Stroke 43(4):1108–U1341PubMedCrossRefGoogle Scholar
  81. 81.
    Chao CC, Ma YL, Chu KY, Lee EHY (2003) Integrin alpha v and NCAM mediate the effects of GDNF on DA neuron survival, outgrowth, DA turnover and motor activity in rats. Neurobiol Aging 24(1):105–116PubMedCrossRefGoogle Scholar
  82. 82.
    Gary DS, Milhavet O, Camandola S, Mattson MP (2003) Essential role for integrin linked kinase in Akt-mediated integrin survival signaling in hippocampal neurons. J Neurochem 84(4):878–890PubMedCrossRefGoogle Scholar
  83. 83.
    Ma SM, Chen LX, Lin YF et al (2015) Periostin promotes neural stem cell proliferation and differentiation following hypoxic-ischemic injury. PLoS One 10(4):e0123585PubMedPubMedCentralCrossRefGoogle Scholar
  84. 84.
    Clevers H (2011) The cancer stem cell: premises, promises and challenges. Nat Med 17(3):313–319PubMedCrossRefGoogle Scholar
  85. 85.
    Malanchi I, Santamaria-Martinez A, Susanto E et al (2012) Interactions between cancer stem cells and their niche govern metastatic colonization. Nature 481(7379):85–U95CrossRefGoogle Scholar
  86. 86.
    Xu DY, Xu H, Ren Y et al (2012) Cancer stem cell-related gene periostin: a novel prognostic marker for breast cancer. PLoS One 7(10):e46670PubMedPubMedCentralCrossRefGoogle Scholar
  87. 87.
    Lambert AW, Wong CK, Ozturk S et al (2016) Tumor cell-derived periostin regulates cytokines that maintain breast cancer stem cells. Mol Cancer Res 14(1):103–113PubMedCrossRefGoogle Scholar
  88. 88.
    Wang XW, Liu J, Wang Z et al (2013) Periostin contributes to the acquisition of multipotent stem cell-like properties in human mammary epithelial cells and breast cancer cells. PLoS One 8(8):e72962PubMedPubMedCentralCrossRefGoogle Scholar
  89. 89.
    Liu GX, Xi HQ, Sun XY, Wei B (2015) Role of periostin and its antagonist PNDA-3 in gastric cancer metastasis. World J Gastroenterol 21(9):2605–2613PubMedPubMedCentralCrossRefGoogle Scholar
  90. 90.
    Mikheev AM, Mikheeva SA, Trister AD et al (2015) Periostin is a novel therapeutic target that predicts and regulates glioma malignancy. Neuro-Oncology 17(3):372–382PubMedCrossRefGoogle Scholar
  91. 91.
    Miller PG, Al-Shahrour F, Hartwell KA et al (2013) In vivo RNAi screening identifies a leukemia-specific dependence on integrin beta 3 signaling. Cancer Cell 24(1):45–58PubMedPubMedCentralCrossRefGoogle Scholar

Copyright information

© Springer Nature Singapore Pte Ltd. 2019

Authors and Affiliations

  • Athira Suresh
    • 1
  • Atreyi Biswas
    • 1
  • Saravana Perumal
    • 1
  • Satish Khurana
    • 1
    Email author
  1. 1.School of BiologyIndian Institute of Science Education and Research Thiruvananthapuram (IISER TVM)ThiruvananthapuramIndia

Personalised recommendations