Skip to main content Accessibility help

We use cookies to distinguish you from other users and to provide you with a better experience on our websites. Close this message to accept cookies or find out how to manage your cookie settings.

Close cookie message
×
Hostname: page-component-76fb5796d-x4r87 Total loading time: 0 Render date: 2024-04-26T16:16:44.129Z Has data issue: false hasContentIssue false

Chapter 2 - Early Development of the Mammalian Lung-Branching Morphogenesis

Published online by Cambridge University Press:  05 April 2016

By
Kathleen M. Stewart  and
Edward E. Morrisey
Edited by
Alan H. Jobe ,
Jeffrey A. Whitsett  and
Steven H. Abman
Alan H. Jobe
Affiliation:
University of Cincinnati
Jeffrey A. Whitsett
Affiliation:
Cincinnati Children’s Hospital
Steven H. Abman
Affiliation:
University of Colorado School of Medicine
Get access

Summary

Abstract

The lung is an essential organ for mammalian health throughout life and represents a critical interface with the external environment in the regulation of gas exchange. To achieve these goals the mammalian lung has evolved into a highly complex system of branching epithelial and vascular structures that connects to a vast network of alveolar gas-exchanging units. The generation of this complex organ involves multiple steps and encompasses events that span prenatal and postnatal life. This chapter focuses on the mechanisms that regulate early lung development and branching morphogenesis and the various signaling molecules, extracellular matrix proteins, and genetic changes that influence this process. These research areas are critical for understanding the various causes of respiratory disease, which are a major contributor to morbidity and mortality at all stages of life.

Type
Chapter
Information
Fetal and Neonatal Lung Development
Clinical Correlates and Technologies for the Future
 , pp. 22 - 33
Publisher: Cambridge University Press
Print publication year: 2016

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Bourbon, J, Boucherat, O, Chailley-Heu, B, Delacourt, C. Control mechanisms of lung alveolar development and their disorders in bronchopulmonary dysplasia. Pediatric Research. 2005 May;57(5 Pt 2):38R–46R.CrossRefGoogle ScholarPubMed
Pauling, MH, Vu, TH. Mechanisms and regulation of lung vascular development. Current Topics in Developmental Biology. 2004;64:73–99.CrossRefGoogle ScholarPubMed
Williams, MC. Alveolar type I cells: molecular phenotype and development. Annual Review of Physiology. 2003;65:669–695.CrossRefGoogle ScholarPubMed
Ten Have-Opbroek, AA. Lung development in the mouse embryo. Experimental Lung Research. 1991 Mar-Apr;17(2):111–130.CrossRefGoogle ScholarPubMed
Morrisey, EE, Hogan, BL. Preparing for the first breath: genetic and cellular mechanisms in lung development. Developmental Cell. 2010 Jan 19;18(1):8–23.CrossRefGoogle ScholarPubMed
Domyan, ET, Ferretti, E, Throckmorton, K, Mishina, Y, Nicolis, SK, Sun, X. Signaling through BMP receptors promotes respiratory identity in the foregut via repression of Sox2. Development. 2011 Mar;138(5):971–981.CrossRefGoogle ScholarPubMed
Kaufman, MH. The atlas of mouse development. London England: Harcourt Brace & Company; 1992.Google Scholar
Varner, VD, Nelson, CM. Cellular and physical mechanisms of branching morphogenesis. Development. 2014 Jul;141(14):2750–2759.CrossRefGoogle ScholarPubMed
Watson, CJ, Khaled, WT. Mammary development in the embryo and adult: a journey of morphogenesis and commitment. Development. 2008 Mar;135(6):995–1003.CrossRefGoogle ScholarPubMed
Metzger, RJ, Klein, OD, Martin, GR, Krasnow, MA. The branching programme of mouse lung development. Nature. 2008 Jun 5;453(7196):745–750.CrossRefGoogle ScholarPubMed
Mund, SI, Stampanoni, M, Schittny, JC. Developmental alveolarization of the mouse lung Developmental Dynamics. 2008 Aug;237(8):2108–2116.CrossRefGoogle Scholar
Maeda, Y, Dave, V, Whitsett, JA. Transcriptional control of lung morphogenesis. Physiological Reviews. 2007 Jan;87(1):219–44.CrossRefGoogle ScholarPubMed
Besnard, V, Wert, SE, Hull, WM, Whitsett, JA. Immunohistochemical localization of Foxa1 and Foxa2 in mouse embryos and adult tissues. Gene Expression Patterns. 2004 Dec;5(2):193–208.CrossRefGoogle ScholarPubMed
Zhou, L, Lim, L, Costa, RH, Whitsett, JA. Thyroid transcription factor-1, hepatocyte nuclear factor-3beta, surfactant protein B, C, and Clara cell secretory protein in developing mouse lung. The Journal of Histochemistry and Cytochemistry. 1996 Oct;44(10):1183–1193.CrossRefGoogle Scholar
Wan, H, Dingle, S, Xu, Y, Besnard, V, Kaestner, KH, Ang, SL, et al. Compensatory roles of Foxa1 and Foxa2 during lung morphogenesis. The Journal of Biological Chemistry. 2005 Apr 8;280(14):13809–13816.CrossRefGoogle ScholarPubMed
Shu, W, Lu, MM, Zhang, Y, Tucker, PW, Zhou, D, Morrisey, EE. Foxp2 and Foxp1 cooperatively regulate lung and esophagus development. Development. 2007 May;134(10):1991–2000.CrossRefGoogle ScholarPubMed
Li, S, Wang, Y, Zhang, Y, Lu, MM, DeMayo, FJ, Dekker, JD, et al. Foxp1/4 control epithelial cell fate during lung development and regeneration through regulation of anterior gradient 2. Development. 2012 Jul;139(14):2500–2509.CrossRefGoogle ScholarPubMed
Kalinichenko, VV, Lim, L, Stolz, DB, Shin, B, Rausa, FM, Clark, J, et al. Defects in pulmonary vasculature and perinatal lung hemorrhage in mice heterozygous null for the Forkhead Box f1 transcription factor. Developmental Biology. 2001 Jul 15;235(2):489–506.CrossRefGoogle ScholarPubMed
Mahlapuu, M, Ormestad, M, Enerback, S, Carlsson, P. The forkhead transcription factor Foxf1 is required for differentiation of extra-embryonic and lateral plate mesoderm. Development. 2001 Jan;128(2):155–166.CrossRefGoogle ScholarPubMed
Sen, P, Yang, Y, Navarro, C, Silva, I, Szafranski, P, Kolodziejska, KE, et al. Novel FOXF1 mutations in sporadic and familial cases of alveolar capillary dysplasia with misaligned pulmonary veins imply a role for its DNA binding domain. Human Mutation. 2013 Jun;34(6):801–811.CrossRefGoogle ScholarPubMed
Miranda, J, Rocha, G, Soares, P, Morgado, H, Baptista, MJ, Azevedo, I, et al. A novel mutation in FOXF1 gene associated with alveolar capillary dysplasia with misalignment of pulmonary veins, intestinal malrotation and annular pancreas. Neonatology. 2013;103(4):241–245.CrossRefGoogle ScholarPubMed
Sen, P, Gerychova, R, Janku, P, Jezova, M, Valaskova, I, Navarro, C, et al. A familial case of alveolar capillary dysplasia with misalignment of pulmonary veins supports paternal imprinting of FOXF1 in human. European Journal of Human Genetics. 2013 Apr;21(4):474–477.CrossRefGoogle ScholarPubMed
Krumlauf, R. Hox genes in vertebrate development. Cell. 1994 Jul 29;78(2):191–201.CrossRefGoogle ScholarPubMed
Aubin, J, Lemieux, M, Tremblay, M, Berard, J, Jeannotte, L. Early postnatal lethality in Hoxa-5 mutant mice is attributable to respiratory tract defects. Developmental Biology. 1997 Dec 15;192(2):432–445.CrossRefGoogle ScholarPubMed
Herriges, JC, Yi, L, Hines, EA, Harvey, JF, Xu, G, Gray, PA, et al. Genome-scale study of transcription factor expression in the branching mouse lung. Developmental Dynamics. 2012 Sep;241(9):1432–1453.CrossRefGoogle ScholarPubMed
Boucherat, O, Montaron, S, Berube-Simard, FA, Aubin, J, Philippidou, P, Wellik, DM, et al. Partial functional redundancy between Hoxa5 and Hoxb5 paralog genes during lung morphogenesis. American Journal of Physiology–Lung Cellular and Molecular Physiology. 2013 Jun 15;304(12):L817–830.CrossRefGoogle ScholarPubMed
Volpe, MV, Ramadurai, SM, Pham, LD, Nielsen, HC. Hoxb-5 down regulation alters Tenascin-C, FGF10 and Hoxb gene expression patterns in pseudoglandular period fetal mouse lung. Frontiers in Bioscience. 2007;12:860–873.CrossRefGoogle ScholarPubMed
Roth-Kleiner, M, Hirsch, E, Schittny, JC. Fetal lungs of tenascin-C-deficient mice grow well, but branch poorly in organ culture. American Journal of Respiratory Cell and Molecular Biology. 2004 Mar;30(3):360–366.CrossRefGoogle ScholarPubMed
Charron, J, Malynn, BA, Fisher, P, Stewart, V, Jeannotte, L, Goff, SP, et al. Embryonic lethality in mice homozygous for a targeted disruption of the N-myc gene. Genes & Development. 1992 Dec;6(12A):2248–2257.CrossRefGoogle ScholarPubMed
Stanton, BR, Perkins, AS, Tessarollo, L, Sassoon, DA, Parada, LF. Loss of N-myc function results in embryonic lethality and failure of the epithelial component of the embryo to develop. Genes & Development. 1992 Dec;6(12A):2235–2247.CrossRefGoogle ScholarPubMed
Sawai, S, Shimono, A, Wakamatsu, Y, Palmes, C, Hanaoka, K, Kondoh, H. Defects of embryonic organogenesis resulting from targeted disruption of the N-myc gene in the mouse. Development. 1993 Apr;117(4):1445–1455.CrossRefGoogle ScholarPubMed
Moens, CB, Auerbach, AB, Conlon, RA, Joyner, AL, Rossant, J.A targeted mutation reveals a role for N-myc in branching morphogenesis in the embryonic mouse lung. Genes & Development. 1992 May;6(5):691–704.CrossRefGoogle ScholarPubMed
Okubo, T, Knoepfler, PS, Eisenman, RN, Hogan, BL. Nmyc plays an essential role during lung development as a dosage-sensitive regulator of progenitor cell proliferation and differentiation. Development. 2005 Mar;132(6):1363–74.CrossRefGoogle ScholarPubMed
Serra, R, Pelton, RW, Moses, HL. TGF beta 1 inhibits branching morphogenesis and N-myc expression in lung bud organ cultures. Development. 1994 Aug;120(8):2153–2161.CrossRefGoogle ScholarPubMed
Lazzaro, D, Price, M, de Felice, M, Di Lauro, R. The transcription factor TTF-1 is expressed at the onset of thyroid and lung morphogenesis and in restricted regions of the foetal brain. Development. 1991 Dec;113(4):1093–1104.CrossRefGoogle ScholarPubMed
Kimura, S. Thyroid-specific enhancer-binding protein Role in thyroid function and organogenesis. Trends in Endocrinology and Metabolism. 1996 Sep;7(7):247–252.CrossRefGoogle ScholarPubMed
Devriendt, K, Vanhole, C, Matthijs, G, de Zegher, F. Deletion of thyroid transcription factor-1 gene in an infant with neonatal thyroid dysfunction and respiratory failure. The New England Journal of Medicine. 1998 Apr 30;338(18):1317–1318.CrossRefGoogle Scholar
DeFelice, M, Silberschmidt, D, DiLauro, R, Xu, Y, Wert, SE, Weaver, TE, et al. TTF-1 phosphorylation is required for peripheral lung morphogenesis, perinatal survival, and tissue-specific gene expression. The Journal of Biological Chemistry. 2003 Sep 12;278(37):35574–35583.CrossRefGoogle ScholarPubMed
LeBoeuf, M, Terrell, A, Trivedi, S, Sinha, S, Epstein, JA, Olson, EN, et al. Hdac1 and Hdac2 act redundantly to control p63 and p53 functions in epidermal progenitor cells. Developmental Cell. 2010 Dec 14;19(6):807–818.CrossRefGoogle ScholarPubMed
Snitow, ME, Li, S, Morley, MP, Rathi, K, Lu, MM, Kadzik, RS, et al. Ezh2 represses the basal cell lineage during lung endoderm development. Development. 2015 Jan 1;142(1):108–117.CrossRefGoogle ScholarPubMed
Hogan, BL, Barkauskas, CE, Chapman, HA, Epstein, JA, Jain, R, Hsia, CC, et al. Repair and regeneration of the respiratory system: complexity, plasticity, and mechanisms of lung stem cell function. Cell Stem Cell. 2014 Aug 7;15(2):123–138.CrossRefGoogle ScholarPubMed
Dong, J, Jiang, G, Asmann, YW, Tomaszek, S, Jen, J, Kislinger, T, et al. MicroRNA networks in mouse lung organogenesis. PLoS One. 2010;5(5):e10854.CrossRefGoogle ScholarPubMed
Lim, L, Kalinichenko, VV, Whitsett, JA, Costa, RH. Fusion of lung lobes and vessels in mouse embryos heterozygous for the forkhead box f1 targeted allele. American Journal of Physiology–Lung Cellular and Molecular Physiology. 2002 May;282(5):L1012–1022.CrossRefGoogle ScholarPubMed
Williams, AE, Moschos, SA, Perry, MM, Barnes, PJ, Lindsay, MA. Maternally imprinted microRNAs are differentially expressed during mouse and human lung development. Developmental Dynamics. 2007 Feb;236(2):572–580.CrossRefGoogle ScholarPubMed
Ventura, A, Young, AG, Winslow, MM, Lintault, L, Meissner, A, Erkeland, SJ, et al. Targeted deletion reveals essential and overlapping functions of the miR-17 through 92 family of miRNA clusters. Cell. 2008 Mar 7;132(5):875–886.CrossRefGoogle ScholarPubMed
Lu, Y, Thomson, JM, Wong, HY, Hammond, SM, Hogan, BL. Transgenic over-expression of the microRNA miR-17–92 cluster promotes proliferation and inhibits differentiation of lung epithelial progenitor cells. Developmental Biology. 2007 Oct 15;310(2):442–453.CrossRefGoogle ScholarPubMed
Tian, Y, Zhang, Y, Hurd, L, Hannenhalli, S, Liu, F, Lu, MM, et al. Regulation of lung endoderm progenitor cell behavior by miR302/367. Development. 2011 Apr;138(7):1235–1245.CrossRefGoogle ScholarPubMed
Mujahid, S, Nielsen, HC, Volpe, MV. MiR-221 and miR-130a regulate lung airway and vascular development. PLoS One. 2013;8(2):e55911.CrossRefGoogle ScholarPubMed
Herriges, MJ, Swarr, DT, Morley, MP, Rathi, KS, Peng, T, Stewart, KM, et al. Long noncoding RNAs are spatially correlated with transcription factors and regulate lung development. Genes & Development. 2014 Jun 15;28(12):1363–1379.CrossRefGoogle ScholarPubMed
Alescio, T, Cassini, A. Induction in vitro of tracheal buds by pulmonary mesenchyme grafted on tracheal epithelium. The Journal of Experimental Zoology. 1962 Jul;150:83–94.CrossRefGoogle ScholarPubMed
Shannon, JM. Induction of alveolar type II cell differentiation in fetal tracheal epithelium by grafted distal lung mesenchyme. Developmental Biology. 1994 Dec;166(2):600–614.CrossRefGoogle ScholarPubMed
Taderera, JV. Control of lung differentiation in vitro. Developmental Biology. 1967 Nov;16(5):489–512.CrossRefGoogle ScholarPubMed
Warburton, D, Bellusci, S, De Langhe, S, Del Moral, PM, Fleury, V, Mailleux, A, et al. Molecular mechanisms of early lung specification and branching morphogenesis. Pediatric Research. 2005 May;57(5 Pt 2):26R–37R.CrossRefGoogle ScholarPubMed
Sekine, K, Ohuchi, H, Fujiwara, M, Yamasaki, M, Yoshizawa, T, Sato, T, et al. Fgf10 is essential for limb and lung formation. Nature Genetics. 1999 Jan;21(1):138–141.CrossRefGoogle ScholarPubMed
De Moerlooze, L, Spencer-Dene, B, Revest, JM, Hajihosseini, M, Rosewell, I, Dickson, C. An important role for the IIIb isoform of fibroblast growth factor receptor 2 (FGFR2) in mesenchymal-epithelial signalling during mouse organogenesis. Development. 2000 Feb;127(3):483–492.CrossRefGoogle ScholarPubMed
Arman, E, Haffner-Krausz, R, Gorivodsky, M, Lonai, P. Fgfr2 is required for limb outgrowth and lung-branching morphogenesis. Proceedings of the National Academy of Sciences of the United States of America. 1999 Oct 12;96(21):11895–11899.CrossRefGoogle ScholarPubMed
Abler, LL, Mansour, SL, Sun, X. Conditional gene inactivation reveals roles for Fgf10 and Fgfr2 in establishing a normal pattern of epithelial branching in the mouse lung. Developmental Dynamics. 2009 Aug;238(8):1999–2013.CrossRefGoogle ScholarPubMed
Colvin, JS, White, AC, Pratt, SJ, Ornitz, DM. Lung hypoplasia and neonatal death in Fgf9-null mice identify this gene as an essential regulator of lung mesenchyme. Development. 2001 Jun;128(11):2095–2106.CrossRefGoogle ScholarPubMed
Li, C, Hu, L, Xiao, J, Chen, H, Li, JT, Bellusci, S, et al. Wnt5a regulates Shh and Fgf10 signaling during lung development. Developmental Biology. 2005 Nov 1;287(1):86–97.CrossRefGoogle ScholarPubMed
Li, C, Xiao, J, Hormi, K, Borok, Z, Minoo, P. Wnt5a participates in distal lung morphogenesis. Developmental Biology. 2002 Aug 1;248(1):68–81.CrossRefGoogle ScholarPubMed
Goss, AM, Tian, Y, Cheng, L, Yang, J, Zhou, D, Cohen, ED, et al. Wnt2 signaling is necessary and sufficient to activate the airway smooth muscle program in the lung by regulating myocardin/Mrtf-B and Fgf10 expression. Developmental Biology. 2011 Aug 15;356(2):541–552.CrossRefGoogle Scholar
Finch, PW, He, X, Kelley, MJ, Uren, A, Schaudies, RP, Popescu, NC, et al. Purification and molecular cloning of a secreted, Frizzled-related antagonist of Wnt action. Proceedings of the National Academy of Sciences of the United States of America. 1997 Jun 24;94(13):6770–6775.CrossRefGoogle ScholarPubMed
Goss, AM, Tian, Y, Tsukiyama, T, Cohen, ED, Zhou, D, Lu, MM, et al. Wnt2/2b and beta-catenin signaling are necessary and sufficient to specify lung progenitors in the foregut. Developmental Cell. 2009 Aug;17(2):290–298.CrossRefGoogle ScholarPubMed
Miller, MF, Cohen, ED, Baggs, JE, Lu, MM, Hogenesch, JB, Morrisey, EE. Wnt ligands signal in a cooperative manner to promote foregut organogenesis. Proceedings of the National Academy of Sciences of the United States of America. 2012 Sep 18;109(38):15348–15353.CrossRefGoogle Scholar
Kadzik, RS, Cohen, ED, Morley, MP, Stewart, KM, Lu, MM, Morrisey, EE. Wnt ligand/Frizzled 2 receptor signaling regulates tube shape and branch-point formation in the lung through control of epithelial cell shape. Proceedings of the National Academy of Sciences of the United States of America. 2014 Aug 26;111(34):12444–12449.CrossRefGoogle ScholarPubMed
Pepicelli, CV, Lewis, PM, McMahon, AP. Sonic hedgehog regulates branching morphogenesis in the mammalian lung. Current Biology. 1998 Sep 24;8(19):1083–1086.CrossRefGoogle ScholarPubMed
Weaver, M, Batts, L, Hogan, BL. Tissue interactions pattern the mesenchyme of the embryonic mouse lung. Developmental Biology. 2003 Jun 1;258(1):169–184.CrossRefGoogle ScholarPubMed
Litingtung, Y, Lei, L, Westphal, H, Chiang, C. Sonic hedgehog is essential to foregut development. Nature Genetics. 1998 Sep;20(1):58–61.CrossRefGoogle ScholarPubMed
Bellusci, S, Henderson, R, Winnier, G, Oikawa, T, Hogan, BL. Evidence from normal expression and targeted misexpression that bone morphogenetic protein (Bmp-4) plays a role in mouse embryonic lung morphogenesis. Development. 1996 Jun;122(6):1693–1702.CrossRefGoogle Scholar
Eblaghie, MC, Reedy, M, Oliver, T, Mishina, Y, Hogan, BL. Evidence that autocrine signaling through Bmpr1a regulates the proliferation, survival and morphogenetic behavior of distal lung epithelial cells. Developmental Biology. 2006 Mar 1;291(1):67–82.CrossRefGoogle ScholarPubMed
Thibeault, DW, Mabry, SM, Ekekezie, II, Zhang, X, Truog, WE. Collagen scaffolding during development and its deformation with chronic lung disease. Pediatrics. 2003 Apr;111(4 Pt 1):766–776.CrossRefGoogle ScholarPubMed
Wasowicz, M, Biczysko, W, Marszalek, A, Yokoyama, S, Nakayama, I. Ultrastructural studies on selected elements of the extracellular matrix in the developing rat lung alveolus. Folia Histochemica et Cytobiologica. 1998;36(1):3–13.Google ScholarPubMed
Hilfer, SR. Morphogenesis of the lung: control of embryonic and fetal branching. Annual Review of Physiology. 1996;58:93–113.CrossRefGoogle ScholarPubMed
Minoo, P, King, RJ. Epithelial-mesenchymal interactions in lung development. Annual Review of Physiology. 1994;56:13–45.CrossRefGoogle ScholarPubMed
Grobstein, C, Cohen, J. Collagenase: effect on the morphogenesis of embryonic salivary epithelium in vitro. Science. 1965 Oct 29;150(3696):626–628.CrossRefGoogle ScholarPubMed
Wessells, NK, Cohen, JH. Effects of collagenase on developing epithelia in vitro: lung, ureteric bud, and pancreas. Developmental Biology. 1968 Sep;18(3):294–309.CrossRefGoogle ScholarPubMed
Spooner, BS, Faubion, JM. Collagen involvement in branching morphogenesis of embryonic lung and salivary gland. Developmental Biology. 1980 Jun 1;77(1):84–102.CrossRefGoogle ScholarPubMed
Kreidberg, JA, Donovan, MJ, Goldstein, SL, Rennke, H, Shepherd, K, Jones, RC, et al. Alpha 3 beta 1 integrin has a crucial role in kidney and lung organogenesis. Development. 1996 Nov;122(11):3537–3547.CrossRefGoogle Scholar
Timpl, R, Brown, JC. The laminins. Matrix Biology. 1994 Aug;14(4):275–281.CrossRefGoogle ScholarPubMed
Ehrig, K, Leivo, I, Engvall, E. Merosin and laminin. Molecular relationship and role in nerve-muscle development. Annals of the New York Academy of Sciences. 1990;580:276–280.CrossRefGoogle ScholarPubMed
Galliano, MF, Aberdam, D, Aguzzi, A, Ortonne, JP, Meneguzzi, G. Cloning and complete primary structure of the mouse laminin alpha 3 chain. Distinct expression pattern of the laminin alpha 3A and alpha 3B chain isoforms. The Journal of Biological Chemistry. 1995 Sep 15;270(37):21820–21826.CrossRefGoogle ScholarPubMed
Koch, M, Olson, PF, Albus, A, Jin, W, Hunter, DD, Brunken, WJ, et al. Characterization and expression of the laminin gamma3 chain: a novel, non-basement membrane-associated, laminin chain. The Journal of Cell Biology. 1999 May 3;145(3):605–618.CrossRefGoogle Scholar
Pierce, RA, Griffin, GL, Mudd, MS, Moxley, MA, Longmore, WJ, Sanes, JR, et al. Expression of laminin alpha3, alpha4, and alpha5 chains by alveolar epithelial cells and fibroblasts. American Journal of Respiratory Cell and Molecular Biology. 1998 Aug;19(2):237–244.CrossRefGoogle ScholarPubMed
Sunada, Y, Bernier, SM, Kozak, CA, Yamada, Y, Campbell, KP. Deficiency of merosin in dystrophic dy mice and genetic linkage of laminin M chain gene to dy locus. The Journal of Biological Chemistry. 1994 May 13;269(19):13729–13732.CrossRefGoogle ScholarPubMed
Vuolteenaho, R, Nissinen, M, Sainio, K, Byers, M, Eddy, R, Hirvonen, H, et al. Human laminin M chain (merosin): complete primary structure, chromosomal assignment, and expression of the M and A chain in human fetal tissues. The Journal of Cell Biology. 1994 Feb;124(3):381–394.CrossRefGoogle Scholar
Miner, JH, Cunningham, J, Sanes, JR. Roles for laminin in embryogenesis: exencephaly, syndactyly, and placentopathy in mice lacking the laminin alpha5 chain. The Journal of Cell Biology. 1998 Dec 14;143(6):1713–1723.CrossRefGoogle ScholarPubMed
Miner, JH, Lewis, RM, Sanes, JR. Molecular cloning of a novel laminin chain, alpha 5, and widespread expression in adult mouse tissues. The Journal of Biological Chemistry. 1995 Dec 1;270(48):28523–28526.CrossRefGoogle ScholarPubMed
Nguyen, NM, Miner, JH, Pierce, RA, Senior, RM. Laminin alpha 5 is required for lobar septation and visceral pleural basement membrane formation in the developing mouse lung. Developmental Biology. 2002 Jun 15;246(2):231–244.CrossRefGoogle ScholarPubMed
Schuger, L, O'Shea, S, Rheinheimer, J, Varani, J. Laminin in lung development: effects of anti-laminin antibody in murine lung morphogenesis. Developmental Biology. 1990 Jan;137(1):26–32.CrossRefGoogle ScholarPubMed
Wu, JE, Santoro, SA. Differential expression of integrin alpha subunits supports distinct roles during lung branching morphogenesis. Developmental Dynamics. 1996 Jun;206(2):169–181.3.0.CO;2-G>CrossRefGoogle ScholarPubMed
Hynes, RO. Specificity of cell adhesion in development: the cadherin superfamily. Current Opinion in Genetics & Development. 1992 Aug;2(4):621–624.CrossRefGoogle ScholarPubMed
Chen, YP, O'Toole, TE, Leong, L, Liu, BQ, Diaz-Gonzalez, F, Ginsberg, MH. Beta 3 integrin-mediated fibrin clot retraction by nucleated cells: differing behavior of alpha IIb beta 3 and alpha v beta 3. Blood. 1995 Oct 1;86(7):2606–2615.CrossRefGoogle ScholarPubMed
Otey, CA, Vasquez, GB, Burridge, K, Erickson, BW. Mapping of the alpha-actinin binding site within the beta 1 integrin cytoplasmic domain. The Journal of Biological Chemistry. 1993 Oct 5;268(28):21193–21197.CrossRefGoogle ScholarPubMed
Chan, BM, Kassner, PD, Schiro, JA, Byers, HR, Kupper, TS, Hemler, ME. Distinct cellular functions mediated by different VLA integrin alpha subunit cytoplasmic domains. Cell. 1992 Mar 20;68(6):1051–1060.CrossRefGoogle ScholarPubMed
Kassner, PD, Hemler, ME. Interchangeable alpha chain cytoplasmic domains play a positive role in control of cell adhesion mediated by VLA-4, a beta 1 integrin. The Journal of Experimental Medicine. 1993 Aug 1;178(2):649–660.CrossRefGoogle ScholarPubMed
Kawaguchi, S, Hemler, ME. Role of the alpha subunit cytoplasmic domain in regulation of adhesive activity mediated by the integrin VLA-2. The Journal of Biological Chemistry. 1993 Aug 5;268(22):16279–16285.CrossRefGoogle ScholarPubMed
Clark, EA, Brugge, JS. Integrins and signal transduction pathways: the road taken. Science. 1995 Apr 14;268(5208):233–239.CrossRefGoogle ScholarPubMed
Chen, J, Krasnow, MA. Integrin Beta 1 suppresses multilayering of a simple epithelium. PLoS One. 2012;7(12):e52886.CrossRefGoogle ScholarPubMed
Plosa, EJ, Young, LR, Gulleman, PM, Polosukhin, VV, Zaynagetdinov, R, Benjamin, JT, et al. Epithelial beta1 integrin is required for lung branching morphogenesis and alveolarization. Development. 2014 Dec;141(24):4751–4762.CrossRefGoogle ScholarPubMed
Nelson, CM, Gleghorn, JP. Sculpting organs: mechanical regulation of tissue development. Annual Review of Biomedical Engineering. 2012;14:129–154.CrossRefGoogle ScholarPubMed
Chi, X, Michos, O, Shakya, R, Riccio, P, Enomoto, H, Licht, JD, et al. Ret-dependent cell rearrangements in the Wolffian duct epithelium initiate ureteric bud morphogenesis. Development Cell. 2009 Aug;17(2):199–209.CrossRefGoogle ScholarPubMed
Schnatwinkel, C, Niswander, L. Multiparametric image analysis of lung-branching morphogenesis. Developmental Dynamics. 2013 Jun;242(6):622–637.CrossRefGoogle ScholarPubMed

Save book to Kindle

To save this book to your Kindle, first ensure coreplatform@cambridge.org is added to your Approved Personal Document E-mail List under your Personal Document Settings on the Manage Your Content and Devices page of your Amazon account. Then enter the ‘name’ part of your Kindle email address below. Find out more about saving to your Kindle.

Note you can select to save to either the @free.kindle.com or @kindle.com variations. ‘@free.kindle.com’ emails are free but can only be saved to your device when it is connected to wi-fi. ‘@kindle.com’ emails can be delivered even when you are not connected to wi-fi, but note that service fees apply.

Find out more about the Kindle Personal Document Service.

Available formats
×

Save book to Dropbox

To save content items to your account, please confirm that you agree to abide by our usage policies. If this is the first time you use this feature, you will be asked to authorise Cambridge Core to connect with your account. Find out more about saving content to Dropbox.

Available formats
×

Save book to Google Drive

To save content items to your account, please confirm that you agree to abide by our usage policies. If this is the first time you use this feature, you will be asked to authorise Cambridge Core to connect with your account. Find out more about saving content to Google Drive.

Available formats
×