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Lung Stem Cells in the Epithelium and Vasculature pp 241–256Cite as

Hematopoietic Stem Cells and Chronic Hypoxia-Induced Pulmonary Vascular Remodelling

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Part of the book series: Stem Cell Biology and Regenerative Medicine ((STEMCELL))

Abstract

Alterations in structure and function of the lung vasculature is a common hallmark of chronic lung diseases with associated hypoxemia which, in turn, can lead to severe and progressive pulmonary hypertension (PH) and right heart failure. Key transcriptional regulators are known to coordinate the cellular response to oxygen deprivation (i.e., early growth response (Egr)-1 and hypoxia-inducible factor (HIF)-1α and HIF-2α), but some of them are also known as key masters involved in the quiescence and mobilization of hematopoietic stem cells (HSCs). Indeed, evidence for CXCL12 (also known as stromal-derived factor-1 [SDF-1]) induction in the pulmonary arterial wall following exposure of mice to chronic hypoxia has been reported. In this review, we will discuss the role of oxygen homeostasis on HSC function and on pulmonary vascular remodelling, focusing on whether a link could exist between these two physiopathological phenomena.

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Abbreviations

AP-1:

Activating protein-1

C/EBPβ:

CCAAT/enhancer binding protein β

CD:

Cluster of differentiation

COPD:

Chronic obstructive pulmonary disease

CPFE:

Syndrome combining pulmonary fibrosis and emphysema

CREB:

Cyclic AMP response element-binding protein

CXCL-12:

C-X-C motif chemokine 12

CXCR:

C-X-C chemokine receptor

EGF:

Epidermal growth factor

FGF-2:

Fibroblast growth factor-2 (basic)

G-CSF:

Granulocyte colony-stimulating factor

GFP:

Green fluorescence protein

HAPE:

High altitude pulmonary edema

Hg:

Mercury

HIF:

Hypoxia inducible factor

HPV:

Hypoxic pulmonary vasoconstriction

HSC:

Hematopoietic stem cells

IL:

Interleukin

IPF:

Idiopathic pulmonary fibrosis

mPAP:

Mean pulmonary arterial pressure

mRNA:

Messenger RNA

NF-κB:

Nuclear factor-kappa B

PAH:

Pulmonary arterial hypertension

PH:

Pulmonary hypertension

PHDs:

Prolyl hydroxylase domain-containing proteins

SDF-1:

Stromal-derived factor-1

TNF-α:

Tumor necrosis factor alpha

References

  • Abraham M, Biyder K, Begin M, Wald H, Weiss ID, Galun E, Nagler A, Peled A (2007) Enhanced unique pattern of hematopoietic cell mobilization induced by the CXCR4 antagonist 4F-benzoyl-TN14003. Stem Cells 25(9):2158–2166. doi:10.1634/stemcells.2007-0161

    Article  CAS  PubMed  Google Scholar 

  • Alarcon R, Koumenis C, Geyer RK, Maki CG, Giaccia AJ (1999) Hypoxia induces p53 accumulation through MDM2 down-regulation and inhibition of E6-mediated degradation. Cancer Res 59(24):6046–6051

    CAS  PubMed  Google Scholar 

  • Bae SK, Bae MH, Ahn MY, Son MJ, Lee YM, Bae MK, Lee OH, Park BC, Kim KW (1999) Egr-1 mediates transcriptional activation of IGF-II gene in response to hypoxia. Cancer Res 59(23):5989–5994

    CAS  PubMed  Google Scholar 

  • Beitner-Johnson D, Millhorn DE (1998) Hypoxia induces phosphorylation of the cyclic AMP response element-binding protein by a novel signaling mechanism. J Biol Chem 273(31):19834–19839

    Article  CAS  PubMed  Google Scholar 

  • Broxmeyer HE, Orschell CM, Clapp DW, Hangoc G, Cooper S, Plett PA, Liles WC, Li X, Graham-Evans B, Campbell TB, Calandra G, Bridger G, Dale DC, Srour EF (2005) Rapid mobilization of murine and human hematopoietic stem and progenitor cells with AMD3100, a CXCR4 antagonist. J Exp Med 201(8):1307–1318. doi:10.1084/jem.20041385

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Carpenter TC, Stenmark KR (2001) Hypoxia decreases lung neprilysin expression and increases pulmonary vascular leak. Am J Physiol Lung Cell Mol Physiol 281(4):L941–L948

    CAS  PubMed  Google Scholar 

  • Chandel NS, Schumacker PT (2000) Cellular oxygen sensing by mitochondria: old questions, new insight. J Appl Physiol 88(5):1880–1889

    CAS  PubMed  Google Scholar 

  • Chandel NS, Maltepe E, Goldwasser E, Mathieu CE, Simon MC, Schumacker PT (1998) Mitochondrial reactive oxygen species trigger hypoxia-induced transcription. Proc Natl Acad Sci U S A 95(20):11715–11720

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Chandel NS, McClintock DS, Feliciano CE, Wood TM, Melendez JA, Rodriguez AM, Schumacker PT (2000a) Reactive oxygen species generated at mitochondrial complex III stabilize hypoxia-inducible factor-1α during hypoxia: a mechanism of O2 sensing. J Biol Chem 275(33):25130–25138. doi:10.1074/jbc.M001914200

    Article  CAS  PubMed  Google Scholar 

  • Chandel NS, Trzyna WC, McClintock DS, Schumacker PT (2000b) Role of oxidants in NF-kappa B activation and TNF-alpha gene transcription induced by hypoxia and endotoxin. J Immunol 165(2):1013–1021

    Article  CAS  PubMed  Google Scholar 

  • Chen D, Li M, Luo J, Gu W (2003) Direct interactions between HIF-1 alpha and Mdm2 modulate p53 function. J Biol Chem 278(16):13595–13598. doi:10.1074/jbc.C200694200

    Article  CAS  PubMed  Google Scholar 

  • Comerford KM, Leonard MO, Karhausen J, Carey R, Colgan SP, Taylor CT (2003) Small ubiquitin-related modifier-1 modification mediates resolution of CREB-dependent responses to hypoxia. Proc Natl Acad Sci U S A 100(3):986–991. doi:10.1073/pnas.0337412100

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Davie NJ, Crossno JT Jr, Frid MG, Hofmeister SE, Reeves JT, Hyde DM, Carpenter TC, Brunetti JA, McNiece IK, Stenmark KR (2004) Hypoxia-induced pulmonary artery adventitial remodelling and neovascularization: contribution of progenitor cells. Am J Physiol Lung Cell Mol Physiol 286(4):L668–L678. doi:10.1152/ajplung.00108.2003

    Article  CAS  PubMed  Google Scholar 

  • de Raaf MA, Schalij I, Gomez-Arroyo JG, Rol N, Happe C, de Man FS, Vonk-Noordegraaf A, Westerhof N, Voelkel NF, Bogaard HJ (2014) SuHx rat model: partly reversible pulmonary hypertension and progressive intima obstruction. Eur Respir J. doi:10.1183/09031936.00204813

    PubMed  Google Scholar 

  • Deacon K, Onion D, Kumari R, Watson SA, Knox AJ (2012) Elevated SP-1 transcription factor expression and activity drives basal and hypoxia-induced vascular endothelial growth factor (VEGF) expression in non-small cell lung cancer. J Biol Chem 287(47):39967–39981. doi:10.1074/jbc.M112.397042

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Discher DJ, Bishopric NH, Wu X, Peterson CA, Webster KA (1998) Hypoxia regulates beta-enolase and pyruvate kinase-M promoters by modulating Sp1/Sp3 binding to a conserved GC element. J Biol Chem 273(40):26087–26093

    Article  CAS  PubMed  Google Scholar 

  • Fischler M, Maggiorini M, Dorschner L, Debrunner J, Bernheim A, Kiencke S, Mairbaurl H, Bloch KE, Naeije R, Brunner-La Rocca HP (2009) Dexamethasone but not tadalafil improves exercise capacity in adults prone to high-altitude pulmonary edema. Am J Respir Crit Care Med 180(4):346–352. doi:10.1164/rccm.200808-1348OC

    Article  CAS  PubMed  Google Scholar 

  • Frid MG, Brunetti JA, Burke DL, Carpenter TC, Davie NJ, Reeves JT, Roedersheimer MT, van Rooijen N, Stenmark KR (2006) Hypoxia-induced pulmonary vascular remodelling requires recruitment of circulating mesenchymal precursors of a monocyte/macrophage lineage. Am J Pathol 168(2):659–669. doi:10.2353/ajpath.2006.050599

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Frohlich S, Boylan J, McLoughlin P (2013) Hypoxia-induced inflammation in the lung: a potential therapeutic target in acute lung injury? Am J Respir Cell Mol Biol 48(3):271–279. doi:10.1165/rcmb.2012-0137TR

    Article  CAS  PubMed  Google Scholar 

  • Gambaryan N, Perros F, Montani D, Cohen-Kaminsky S, Mazmanian M, Renaud JF, Simonneau G, Lombet A, Humbert M (2011) Targeting of c-kit + haematopoietic progenitor cells prevents hypoxic pulmonary hypertension. Eur Respir J 37(6):1392–1399. doi:10.1183/09031936.00045710

    Article  CAS  PubMed  Google Scholar 

  • Grover RF, Wagner WW, McMurtry IF, Reeves JT (2011) Pulmonary circulation. In: Compr Physiol. Wiley. doi:10.1002/cphy.cp020304

    Google Scholar 

  • Hayashida K, Fujita J, Miyake Y, Kawada H, Ando K, Ogawa S, Fukuda K (2005) Bone marrow-derived cells contribute to pulmonary vascular remodelling in hypoxia-induced pulmonary hypertension. Chest 127(5):1793–1798. doi:10.1378/chest.127.5.1793

    Article  PubMed  Google Scholar 

  • Hoggatt J, Mohammad KS, Singh P, Hoggatt AF, Chitteti BR, Speth JM, Hu P, Poteat BA, Stilger KN, Ferraro F, Silberstein L, Wong FK, Farag SS, Czader M, Milne GL, Breyer RM, Serezani CH, Scadden DT, Guise TA, Srour EF, Pelus LM (2013) Differential stem- and progenitor-cell trafficking by prostaglandin E2. Nature 495(7441):365–369. doi:10.1038/nature11929

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Howell K, Preston RJ, McLoughlin P (2003) Chronic hypoxia causes angiogenesis in addition to remodelling in the adult rat pulmonary circulation. J Physiol 547(Pt 1):133–145. doi:10.1113/jphysiol.2002.030676

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Hyvelin JM, Howell K, Nichol A, Costello CM, Preston RJ, McLoughlin P (2005) Inhibition of Rho-kinase attenuates hypoxia-induced angiogenesis in the pulmonary circulation. Circ Res 97(2):185–191. doi:10.1161/01.RES.0000174287.17953.83

    Article  CAS  PubMed  Google Scholar 

  • Imanirad P, Dzierzak E (2013) Hypoxia and HIFs in regulating the development of the hematopoietic system. Blood Cells Mol Dis 51(4):256–263. doi:10.1016/j.bcmd.2013.08.005

    Article  CAS  PubMed  Google Scholar 

  • Ishikawa Y, Ito T (1988) Kinetics of hemopoietic stem cells in a hypoxic culture. Eur J Haematol 40(2):126–129

    Article  CAS  PubMed  Google Scholar 

  • Itkin T, Ludin A, Gradus B, Gur-Cohen S, Kalinkovich A, Schajnovitz A, Ovadya Y, Kollet O, Canaani J, Shezen E, Coffin DJ, Enikolopov GN, Berg T, Piacibello W, Hornstein E, Lapidot T (2012) FGF-2 expands murine hematopoietic stem and progenitor cells via proliferation of stromal cells, c-Kit activation, and CXCL12 down-regulation. Blood 120(9):1843–1855. doi:10.1182/blood-2011-11-394692

    Article  CAS  PubMed  Google Scholar 

  • Jin N, Hatton N, Swartz DR, Xia X, Harrington MA, Larsen SH, Rhoades RA (2000) Hypoxia activates jun-N-terminal kinase, extracellular signal-regulated protein kinase, and p38 kinase in pulmonary arteries. Am J Respir Cell Mol Biol 23(5):593–601. doi:10.1165/ajrcmb.23.5.3921

    Article  CAS  PubMed  Google Scholar 

  • Killilea DW, Hester R, Balczon R, Babal P, Gillespie MN (2000) Free radical production in hypoxic pulmonary artery smooth muscle cells. Am J Physiol Lung Cell Mol Physiol 279(2):L408–L412

    CAS  PubMed  Google Scholar 

  • Koong AC, Chen EY, Giaccia AJ (1994) Hypoxia causes the activation of nuclear factor kappa B through the phosphorylation of I kappa B alpha on tyrosine residues. Cancer Res 54(6):1425–1430

    CAS  PubMed  Google Scholar 

  • Kubo K, Yamaguchi S, Fujimoto K, Hanaoka M, Hayasaka M, Honda T, Sodeyama T, Kiyosawa K (1996) Bronchoalveolar lavage fluid findings in patients with chronic hepatitis C virus infection. Thorax 51(3):312–314

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Laderoute KR (2005) The interaction between HIF-1 and AP-1 transcription factors in response to low oxygen. Semin Cell Dev Biol 16(4–5):502–513. doi:10.1016/j.semcdb.2005.03.005

    Article  CAS  PubMed  Google Scholar 

  • Larochelle A, Savona M, Wiggins M, Anderson S, Ichwan B, Keyvanfar K, Morrison SJ, Dunbar CE (2011) Human and rhesus macaque hematopoietic stem cells cannot be purified based only on SLAM family markers. Blood 117(5):1550–1554. doi:10.1182/blood-2009-03-212803

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Larsen M, Tazzyman S, Lund EL, Junker N, Lewis CE, Kristjansen PE, Murdoch C (2008) Hypoxia-induced secretion of macrophage migration-inhibitory factor from MCF-7 breast cancer cells is regulated in a hypoxia-inducible factor-independent manner. Cancer Lett 265(2):239–249. doi:10.1016/j.canlet.2008.02.012

    Article  CAS  PubMed  Google Scholar 

  • Launay JM, Herve P, Callebert J, Mallat Z, Collet C, Doly S, Belmer A, Diaz SL, Hatia S, Cote F, Humbert M, Maroteaux L (2012) Serotonin 5-HT2B receptors are required for bone-marrow contribution to pulmonary arterial hypertension. Blood 119(7):1772–1780. doi:10.1182/blood-2011-06-358374

    Article  CAS  PubMed  Google Scholar 

  • Leeper-Woodford SK, Detmer K (1999) Acute hypoxia increases alveolar macrophage tumor necrosis factor activity and alters NF-kappaB expression. Am J Physiol 276(6 Pt 1):L909–L916

    CAS  PubMed  Google Scholar 

  • Liles WC, Broxmeyer HE, Rodger E, Wood B, Hubel K, Cooper S, Hangoc G, Bridger GJ, Henson GW, Calandra G, Dale DC (2003) Mobilization of hematopoietic progenitor cells in healthy volunteers by AMD3100, a CXCR4 antagonist. Blood 102(8):2728–2730. doi:10.1182/blood-2003-02-0663

    Article  CAS  PubMed  Google Scholar 

  • Liu L, Salnikov AV, Bauer N, Aleksandrowicz E, Labsch S, Nwaeburu C, Mattern J, Gladkich J, Schemmer P, Werner J, Herr I (2014) Triptolide reverses hypoxia-induced epithelial-mesenchymal transition and stem-like features in pancreatic cancer by NF-kappaB downregulation. Int J Cancer 134(10):2489–2503. doi:10.1002/ijc.28583

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Lord BI, Murphy MJ Jr (1973) Hematopoietic stem cell regulation. II. Chronic effects of hypoxic-hypoxia on CFU kinetics. Blood 42(1):89–98

    CAS  PubMed  Google Scholar 

  • Madjdpour C, Jewell UR, Kneller S, Ziegler U, Schwendener R, Booy C, Klausli L, Pasch T, Schimmer RC, Beck-Schimmer B (2003) Decreased alveolar oxygen induces lung inflammation. Am J Physiol Lung Cell Mol Physiol 284(2):L360–L367. doi:10.1152/ajplung.00158.2002

    Article  CAS  PubMed  Google Scholar 

  • Maggiorini M, Brunner-La Rocca HP, Peth S, Fischler M, Bohm T, Bernheim A, Kiencke S, Bloch KE, Dehnert C, Naeije R, Lehmann T, Bartsch P, Mairbaurl H (2006) Both tadalafil and dexamethasone may reduce the incidence of high-altitude pulmonary edema: a randomized trial. Ann Intern Med 145(7):497–506

    Article  PubMed  Google Scholar 

  • Marsch E, Sluimer JC, Daemen MJ (2013) Hypoxia in atherosclerosis and inflammation. Curr Opin Lipidol 24(5):393–400. doi:10.1097/MOL.0b013e32836484a4

    CAS  PubMed  Google Scholar 

  • Matsui H, Ihara Y, Fujio Y, Kunisada K, Akira S, Kishimoto T, Yamauchi-Takihara K (1999) Induction of interleukin (IL)-6 by hypoxia is mediated by nuclear factor (NF)-kappa B and NF-IL6 in cardiac myocytes. Cardiovasc Res 42(1):104–112

    Article  CAS  PubMed  Google Scholar 

  • Min IM, Pietramaggiori G, Kim FS, Passegue E, Stevenson KE, Wagers AJ (2008) The transcription factor EGR1 controls both the proliferation and localization of hematopoietic stem cells. Cell Stem Cell 2(4):380–391. doi:10.1016/j.stem.2008.01.015

    Article  CAS  PubMed  Google Scholar 

  • Minamino T, Christou H, Hsieh CM, Liu Y, Dhawan V, Abraham NG, Perrella MA, Mitsialis SA, Kourembanas S (2001) Targeted expression of heme oxygenase-1 prevents the pulmonary inflammatory and vascular responses to hypoxia. Proc Natl Acad Sci U S A 98(15):8798–8803. doi:10.1073/pnas.161272598

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Minet E, Michel G, Mottet D, Piret JP, Barbieux A, Raes M, Michiels C (2001) c-JUN gene induction and AP-1 activity is regulated by a JNK-dependent pathway in hypoxic HepG2 cells. Exp Cell Res 265(1):114–124. doi:10.1006/excr.2001.5180

    Article  CAS  PubMed  Google Scholar 

  • Mohle R, Bautz F, Rafii S, Moore MA, Brugger W, Kanz L (1998) The chemokine receptor CXCR-4 is expressed on CD34+ hematopoietic progenitors and leukemic cells and mediates transendothelial migration induced by stromal cell-derived factor-1. Blood 91(12):4523–4530

    CAS  PubMed  Google Scholar 

  • Montani D, Perros F, Gambaryan N, Girerd B, Dorfmuller P, Price LC, Huertas A, Hammad H, Lambrecht B, Simonneau G, Launay JM, Cohen-Kaminsky S, Humbert M (2011) C-kit-positive cells accumulate in remodeled vessels of idiopathic pulmonary arterial hypertension. Am J Respir Crit Care Med 184(1):116–123. doi:10.1164/rccm.201006-0905OC

    Article  PubMed  Google Scholar 

  • Murphy MJ Jr, Lord BI (1973) Hematopoietic stem cell regulation. I. Acute effects of hypoxic-hypoxia on CFU kinetics. Blood 42(1):81–87

    PubMed  Google Scholar 

  • Nakayama T, Mutsuga N, Tosato G (2007) Effect of fibroblast growth factor 2 on stromal cell-derived factor 1 production by bone marrow stromal cells and hematopoiesis. J Natl Cancer Inst 99(3):223–235. doi:10.1093/jnci/djk031

    Article  CAS  PubMed  Google Scholar 

  • Nallamshetty S, Chan SY, Loscalzo J (2013) Hypoxia: a master regulator of microRNA biogenesis and activity. Free Radic Biol Med 64:20–30. doi:10.1016/j.freeradbiomed.2013.05.022

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Newman JH, Holt TN, Hedges LK, Womack B, Memon SS, Willers ED, Wheeler L, Phillips JA 3rd, Hamid R (2011) High-altitude pulmonary hypertension in cattle (brisket disease): candidate genes and gene expression profiling of peripheral blood mononuclear cells. Pulm Circ 1(4):462–469. doi:10.4103/2045-8932.93545

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Nishi H, Nishi KH, Johnson AC (2002) Early growth response-1 gene mediates up-regulation of epidermal growth factor receptor expression during hypoxia. Cancer Res 62(3):827–834

    CAS  PubMed  Google Scholar 

  • Orlic D, Kajstura J, Chimenti S, Limana F, Jakoniuk I, Quaini F, Nadal-Ginard B, Bodine DM, Leri A, Anversa P (2001) Mobilized bone marrow cells repair the infarcted heart, improving function and survival. Proc Natl Acad Sci U S A 98(18):10344–10349. doi:10.1073/pnas.181177898

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Pamenter ME, Haddad GG (2014) Do BK channels mediate glioma hypoxia-tolerance? Channels 8(3)

    Google Scholar 

  • Park YK, Park H (2010) Prevention of CCAAT/enhancer-binding protein beta DNA binding by hypoxia during adipogenesis. J Biol Chem 285(5):3289–3299. doi:10.1074/jbc.M109.059212

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Parmar K, Mauch P, Vergilio JA, Sackstein R, Down JD (2007) Distribution of hematopoietic stem cells in the bone marrow according to regional hypoxia. Proc Natl Acad Sci U S A 104(13):5431–5436. doi:10.1073/pnas.0701152104

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Peers C, Kemp PJ (2004) Ion channel regulation by chronic hypoxia in models of acute oxygen sensing. Cell Calcium 36(3–4):341–348. doi:10.1016/j.ceca.2004.02.005

    Article  CAS  PubMed  Google Scholar 

  • Peled A, Grabovsky V, Habler L, Sandbank J, Arenzana-Seisdedos F, Petit I, Ben-Hur H, Lapidot T, Alon R (1999) The chemokine SDF-1 stimulates integrin-mediated arrest of CD34(+) cells on vascular endothelium under shear flow. J Clin Invest 104(9):1199–1211. doi:10.1172/JCI7615

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Raoul W, Wagner-Ballon O, Saber G, Hulin A, Marcos E, Giraudier S, Vainchenker W, Adnot S, Eddahibi S, Maitre B (2007) Effects of bone marrow-derived cells on monocrotaline- and hypoxia-induced pulmonary hypertension in mice. Respir Res 8:8. doi:10.1186/1465-9921-8-8

    Article  PubMed Central  PubMed  Google Scholar 

  • Reeves G (2014) Overview of use of G-CSF and GM-CSF in the treatment of acute radiation injury. Health Phys 106(6):699–703. doi:10.1097/HP.0000000000000090

    Article  CAS  PubMed  Google Scholar 

  • Ricard N, Tu L, Le Hiress M, Huertas A, Phan C, Thuillet R, Sattler C, Fadel E, Seferian A, Montani D, Dorfmuller P, Humbert M, Guignabert C (2014) Increased pericyte coverage mediated by endothelial-derived fibroblast growth factor-2 and interleukin-6 is a source of smooth muscle-like cells in pulmonary hypertension. Circulation 129(15):1586–1597. doi:10.1161/CIRCULATIONAHA.113.007469

    Article  CAS  PubMed  Google Scholar 

  • Ryan MA, Nattamai KJ, Xing E, Schleimer D, Daria D, Sengupta A, Kohler A, Liu W, Gunzer M, Jansen M, Ratner N, Le Cras TD, Waterstrat A, Van Zant G, Cancelas JA, Zheng Y, Geiger H (2010) Pharmacological inhibition of EGFR signaling enhances G-CSF-induced hematopoietic stem cell mobilization. Nat Med 16(10):1141–1146. doi:10.1038/nm.2217

    Article  CAS  PubMed  Google Scholar 

  • Ryan J, Bloch K, Archer SL (2011) Rodent models of pulmonary hypertension: harmonisation with the world health organisation’s categorisation of human PH. Int J Clin Pract Suppl 172:15–34. doi:10.1111/j.1742-1241.2011.02710.x

    Article  PubMed  Google Scholar 

  • Salnikow K, Kluz T, Costa M, Piquemal D, Demidenko ZN, Xie K, Blagosklonny MV (2002) The regulation of hypoxic genes by calcium involves c-Jun/AP-1, which cooperates with hypoxia-inducible factor 1 in response to hypoxia. Mol Cell Biol 22(6):1734–1741

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Sata M, Saiura A, Kunisato A, Tojo A, Okada S, Tokuhisa T, Hirai H, Makuuchi M, Hirata Y, Nagai R (2002) Hematopoietic stem cells differentiate into vascular cells that participate in the pathogenesis of atherosclerosis. Nat Med 8(4):403–409. doi:10.1038/nm0402-403

    Article  CAS  PubMed  Google Scholar 

  • Schmedtje JF Jr, Ji YS, Liu WL, DuBois RN, Runge MS (1997) Hypoxia induces cyclooxygenase-2 via the NF-kappaB p65 transcription factor in human vascular endothelial cells. J Biol Chem 272(1):601–608

    Article  CAS  PubMed  Google Scholar 

  • Schoene RB, Swenson ER, Pizzo CJ, Hackett PH, Roach RC, Mills WJ Jr, Henderson WR Jr, Martin TR (1988) The lung at high altitude: bronchoalveolar lavage in acute mountain sickness and pulmonary edema. J Appl Physiol 64(6):2605–2613

    CAS  PubMed  Google Scholar 

  • Schofield CJ, Ratcliffe PJ (2004) Oxygen sensing by HIF hydroxylases. Nat Rev Mol Cell Biol 5(5):343–354. doi:10.1038/nrm1366

    Article  CAS  PubMed  Google Scholar 

  • Scholz CC, Taylor CT (2013) Hydroxylase-dependent regulation of the NF-kappaB pathway. Biol Chem 394(4):479–493. doi:10.1515/hsz-2012-0338

    Article  CAS  PubMed  Google Scholar 

  • Semenza GL (2000) Oxygen-regulated transcription factors and their role in pulmonary disease. Respir Res 1(3):159–162. doi:10.1186/rr27

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Serebrovskaya TV, Nikolsky IS, Nikolska VV, Mallet RT, Ishchuk VA (2011) Intermittent hypoxia mobilizes hematopoietic progenitors and augments cellular and humoral elements of innate immunity in adult men. High Alt Med Biol 12(3):243–252. doi:10.1089/ham.2010.1086

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Sermeus A, Michiels C (2011) Reciprocal influence of the p53 and the hypoxic pathways. Cell Death Dis 2:e164. doi:10.1038/cddis.2011.48

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Stenmark KR, Bouchey D, Nemenoff R, Dempsey EC, Das M (2000) Hypoxia-induced pulmonary vascular remodelling: contribution of the adventitial fibroblasts. Physiol Res 49(5):503–517

    CAS  PubMed  Google Scholar 

  • Stenmark KR, Gerasimovskaya E, Nemenoff RA, Das M (2002) Hypoxic activation of adventitial fibroblasts: role in vascular remodelling. Chest 122(6 Suppl):326S–334S

    Article  CAS  PubMed  Google Scholar 

  • Stenmark KR, Meyrick B, Galie N, Mooi WJ, McMurtry IF (2009) Animal models of pulmonary arterial hypertension: the hope for etiological discovery and pharmacological cure. Am J Physiol Lung Cell Mol Physiol 297(6):L1013–L1032. doi:10.1152/ajplung.00217.2009

    Article  CAS  PubMed  Google Scholar 

  • Sugiyama T, Kohara H, Noda M, Nagasawa T (2006) Maintenance of the hematopoietic stem cell pool by CXCL12-CXCR4 chemokine signaling in bone marrow stromal cell niches. Immunity 25(6):977–988. doi:10.1016/j.immuni.2006.10.016

    Article  CAS  PubMed  Google Scholar 

  • Takubo K, Goda N, Yamada W, Iriuchishima H, Ikeda E, Kubota Y, Shima H, Johnson RS, Hirao A, Suematsu M, Suda T (2010) Regulation of the HIF-1alpha level is essential for hematopoietic stem cells. Cell Stem Cell 7(3):391–402. doi:10.1016/j.stem.2010.06.020

    Article  CAS  PubMed  Google Scholar 

  • Taraseviciene-Stewart L, Kasahara Y, Alger L, Hirth P, Mc Mahon G, Waltenberger J, Voelkel NF, Tuder RM (2001) Inhibition of the VEGF receptor 2 combined with chronic hypoxia causes cell death-dependent pulmonary endothelial cell proliferation and severe pulmonary hypertension. FASEB J 15(2):427–438. doi:10.1096/fj.00-0343com

    Article  CAS  PubMed  Google Scholar 

  • Taylor CT, Furuta GT, Synnestvedt K, Colgan SP (2000) Phosphorylation-dependent targeting of cAMP response element binding protein to the ubiquitin/proteasome pathway in hypoxia. Proc Natl Acad Sci U S A 97(22):12091–12096. doi:10.1073/pnas.220211797

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Tzeng YS, Li H, Kang YL, Chen WC, Cheng WC, Lai DM (2011) Loss of Cxcl12/Sdf-1 in adult mice decreases the quiescent state of hematopoietic stem/progenitor cells and alters the pattern of hematopoietic regeneration after myelosuppression. Blood 117(2):429–439. doi:10.1182/blood-2010-01-266833

    Article  CAS  PubMed  Google Scholar 

  • Vergadi E, Chang MS, Lee C, Liang OD, Liu X, Fernandez-Gonzalez A, Mitsialis SA, Kourembanas S (2011) Early macrophage recruitment and alternative activation are critical for the later development of hypoxia-induced pulmonary hypertension. Circulation 123(18):1986–1995. doi:10.1161/CIRCULATIONAHA.110.978627

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Villarruel SM, Boehm CA, Pennington M, Bryan JA, Powell KA, Muschler GF (2008) The effect of oxygen tension on the in vitro assay of human osteoblastic connective tissue progenitor cells. J Orthop Res 26(10):1390–1397. doi:10.1002/jor.20666

    Article  PubMed  Google Scholar 

  • Weir EK, Archer SL (1995) The mechanism of acute hypoxic pulmonary vasoconstriction: the tale of two channels. FASEB J 9(2):183–189

    CAS  PubMed  Google Scholar 

  • West JB, American College of Physicians, American Physiological Society (2004) The physiologic basis of high-altitude diseases. Ann Intern Med 141(10):789–800

    Article  PubMed  Google Scholar 

  • Yan SF, Tritto I, Pinsky D, Liao H, Huang J, Fuller G, Brett J, May L, Stern D (1995) Induction of interleukin 6 (IL-6) by hypoxia in vascular cells. Central role of the binding site for nuclear factor-IL-6. J Biol Chem 270(19):11463–11471

    Article  CAS  PubMed  Google Scholar 

  • Yan SF, Zou YS, Gao Y, Zhai C, Mackman N, Lee SL, Milbrandt J, Pinsky D, Kisiel W, Stern D (1998) Tissue factor transcription driven by Egr-1 is a critical mechanism of murine pulmonary fibrin deposition in hypoxia. Proc Natl Acad Sci U S A 95(14):8298–8303

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Yan SF, Lu J, Zou YS, Soh-Won J, Cohen DM, Buttrick PM, Cooper DR, Steinberg SF, Mackman N, Pinsky DJ, Stern DM (1999) Hypoxia-associated induction of early growth response-1 gene expression. J Biol Chem 274(21):15030–15040

    Article  CAS  PubMed  Google Scholar 

  • Yang Y, Liu S, Fan Z, Li Z, Liu J, Xing F (2014) Sp1 modification of human endothelial nitric oxide synthase promoter increases the hypoxia-stimulated activity. Microvasc Res 93:80–86. doi:10.1016/j.mvr.2014.03.004

    Article  CAS  PubMed  Google Scholar 

  • Yin T, Li L (2006) The stem cell niches in bone. J Clin Invest 116(5):1195–1201. doi:10.1172/JCI28568

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Yokota T, Oritani K, Butz S, Ewers S, Vestweber D, Kanakura Y (2012) Markers for hematopoietic stem cells: histories and recent achievements. In: Pelayo R (ed) Advances in hematopoietic stem cell research. InTech, Rijeka. doi:10.5772/32381

    Google Scholar 

  • Zampetaki A, Minamino T, Mitsialis SA, Kourembanas S (2003) Effect of heme oxygenase-1 overexpression in two models of lung inflammation. Exp Biol Med 228(5):442–446

    CAS  Google Scholar 

  • Zepeda AB, Pessoa A Jr, Castillo RL, Figueroa CA, Pulgar VM, Farias JG (2013) Cellular and molecular mechanisms in the hypoxic tissue: role of HIF-1 and ROS. Cell Biochem Funct 31(6):451–459. doi:10.1002/cbf.2985

    Article  CAS  PubMed  Google Scholar 

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Authors and Affiliations

  1. INSERM UMR_S 999, LabEx LERMIT, Centre Chirurgical Marie Lannelongue, Le Plessis-Robinson, France

    Alice Huertas, Marc Humbert & Christophe Guignabert Ph.D.

  2. Univ Paris-Sud, School of medicine, Kremlin-Bicêtre, France

    Alice Huertas, Marc Humbert & Christophe Guignabert Ph.D.

  3. AP-HP, Service de Pneumologie, Centre de Référence de l’Hypertension Pulmonaire Sévère DHU Thorax Innovation, Hôpital de Bicêtre, Le Kremlin-Bicêtre, France

    Alice Huertas & Marc Humbert

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  1. Alice Huertas
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  2. Marc Humbert
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  3. Christophe Guignabert Ph.D.
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Correspondence to Christophe Guignabert Ph.D. .

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  1. Laboratory of Genetics, Salk Institute for Biological Studies, La Jolla, California, USA

    Amy Firth

  2. Department of Medicine, The Univsersity of Arizona, Tucson, Arizona, USA

    Jason X.-J. Yuan

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Huertas, A., Humbert, M., Guignabert, C. (2015). Hematopoietic Stem Cells and Chronic Hypoxia-Induced Pulmonary Vascular Remodelling. In: Firth, A., Yuan, JJ. (eds) Lung Stem Cells in the Epithelium and Vasculature. Stem Cell Biology and Regenerative Medicine. Springer, Cham. https://doi.org/10.1007/978-3-319-16232-4_13

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