The role of pleiotrophin and β-catenin in fetal lung development

Respiratory Research

Volumn 11, Issue , 2010, Pages

  Weng, Tingting ^a   Liu, Lin ^a  

^a OKLAHOMA STATE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AXIN; BETA CATENIN; BONE MORPHOGENETIC PROTEIN 4; PLEIOTROPHIN; PROTEIN DLK1; PROTEIN TTF 1; REGULATOR PROTEIN; UNCLASSIFIED DRUG; WNT5A PROTEIN; WNT7B PROTEIN; CARRIER PROTEIN; CYTOKINE; WNT PROTEIN;

BREAST CANCER; CELL COMMUNICATION; CELL DIFFERENTIATION; CELL INTERACTION; CELL MATURATION; CELL PROLIFERATION; EPITHELIAL MESENCHYMAL INTERACTION; EPITHELIUM CELL; FETUS DEVELOPMENT; FETUS LUNG; FIBROBLAST; GENE CONTROL; GLIOBLASTOMA; HUMAN; KIDNEY DEVELOPMENT; KNOCKOUT MOUSE; LUNG ALVEOLUS EPITHELIUM; LUNG DEVELOPMENT; LUNG FIBROSIS; MELANOMA; NONHUMAN; ONCOGENE C MYC; PROTEIN EXPRESSION; PROTEIN FUNCTION; REGULATORY MECHANISM; REVIEW; SIGNAL TRANSDUCTION; ANIMAL; LUNG; LUNG DISEASE; METABOLISM; MORPHOGENESIS; PRENATAL DEVELOPMENT;

ANIMALS; BETA CATENIN; CARRIER PROTEINS; CELL COMMUNICATION; CELL DIFFERENTIATION; CELL PROLIFERATION; CYTOKINES; EPITHELIAL CELLS; FIBROBLASTS; HUMANS; LUNG; LUNG DISEASES; MORPHOGENESIS; SIGNAL TRANSDUCTION; WNT PROTEINS;

EID: 77956679638     PISSN: 14659921     EISSN: 1465993X     Source Type: Journal    
DOI: 10.1186/1465-9921-11-80     Document Type: Review

References (111)

1. Maeda Y, Dave V, Whitsett JA. Transcriptional control of lung morphogenesis. Physiol Rev 2007, 87:219-244. 10.1152/physrev.00028.2006, 17237346.
2. Metzger RJ, Klein OD, Martin GR, Krasnow MA. The branching programme of mouse lung development. Nature 2008, 453:745-750. 10.1038/nature07005, 2892995, 18463632.
3. Perl AK, Whitsett JA. Molecular mechanisms controlling lung morphogenesis. Clin Genet 1999, 56:14-27. 10.1034/j.1399-0004.1999.560103.x, 10466413.
4. Brody JS, Williams MC. Pulmonary alveolar epithelial cell differentiation. Annu Rev Physiol 1992, 54:351-371. 10.1146/annurev.ph.54.030192.002031, 1562179.
5. McGowan SE, Synder JM. Development of Alveoli. The lung: development, aging and the environment 2004, 55-73. Academic Press, Harding R, Pinkerton KE, Plopper CG.
6. Minoo P, Su G, Drum H, Bringas P, Kimura S. Defects in tracheoesophageal and lung morphogenesis in Nkx2.1(-/-) mouse embryos. Dev Biol 1999, 209:60-71. 10.1006/dbio.1999.9234, 10208743.
7. Ikeda K, Shaw-White JR, Wert SE, Whitsett JA. Hepatocyte nuclear factor 3 activates transcription of thyroid transcription factor 1 in respiratory epithelial cells. Mol Cell Biol 1996, 16:3626-3636. 231358, 8668179.
8. Bohinski RJ, Di LR, Whitsett JA. The lung-specific surfactant protein B gene promoter is a target for thyroid transcription factor 1 and hepatocyte nuclear factor 3, indicating common factors for organ-specific gene expression along the foregut axis. Mol Cell Biol 1994, 14:5671-5681. 359092, 8065304.
9. Sawaya PL, Luse DS. Two members of the HNF-3 family have opposite effects on a lung transcriptional element; HNF-3 alpha stimulates and HNF-3 beta inhibits activity of region I from the Clara cell secretory protein (CCSP) promoter. J Biol Chem 1994, 269:22211-22216.
10. Sawaya PL, Stripp BR, Whitsett JA, Luse DS. The lung-specific CC10 gene is regulated by transcription factors from the AP-1, octamer, and hepatocyte nuclear factor 3 families. Mol Cell Biol 1993, 13:3860-3871. 359916, 8321193.
11. Tichelaar JW, Wert SE, Costa RH, Kimura S, Whitsett JA. HNF-3/forkhead homologue-4 (HFH-4) is expressed in ciliated epithelial cells in the developing mouse lung. J Histochem Cytochem 1999, 47:823-832.
12. Shannon JM, Hyatt BA. Epithelial-mesenchymal interactions in the developing lung. Annu Rev Physiol 2004, 66:625-645. 10.1146/annurev.physiol.66.032102.135749, 14977416.
13. Lawson KA. Mesenchyme specificity in rodent salivary gland development: the response of salivary epithelium to lung mesenchyme in vitro. J Embryol Exp Morphol 1974, 32:469-493.
14. Wessells NK. Mammalian lung development: interactions in formation and morphogenesis of tracheal buds. J Exp Zool 1970, 175:455-466. 10.1002/jez.1401750405, 5501463.
15. ALESCIO T, CASSINI A. Induction in vitro of tracheal buds by pulmonary mesenchyme grafted on tracheal epithelium. J Exp Zool 1962, 150:83-94. 10.1002/jez.1401500202, 14011906.
16. Shannon JM, Nielsen LD, Gebb SA, Randell SH. Mesenchyme specifies epithelial differentiation in reciprocal recombinants of embryonic lung and trachea. Dev Dyn 1998, 212:482-494. 10.1002/(SICI)1097-0177(199808)212:4<482::AID-AJA2>3.0.CO;2-D, 9707322.
17. Park WY, Miranda B, Lebeche D, Hashimoto G, Cardoso WV. FGF-10 is a chemotactic factor for distal epithelial buds during lung development. Dev Biol 1998, 201:125-134. 10.1006/dbio.1998.8994, 9740653.
18. Bellusci S, Grindley J, Emoto H, Itoh N, Hogan BL. Fibroblast growth factor 10 (FGF10) and branching morphogenesis in the embryonic mouse lung. Development 1997, 124:4867-4878.
19. Weaver M, Dunn NR, Hogan BL. Bmp4 and Fgf10 play opposing roles during lung bud morphogenesis. Development 2000, 127:2695-2704.
20. Hyatt BA, Shangguan X, Shannon JM. FGF-10 induces SP-C and Bmp4 and regulates proximal-distal patterning in embryonic tracheal epithelium. Am J Physiol Lung Cell Mol Physiol 2004, 287:L1116-L1126. 10.1152/ajplung.00033.2004, 15531758.
21. Sekine K, Ohuchi H, Fujiwara M, Yamasaki M, Yoshizawa T, Sato T, et al. Fgf10 is essential for limb and lung formation. Nat Genet 1999, 21:138-141. 10.1038/5096, 9916808.
22. Min H, Danilenko DM, Scully SA, Bolon B, Ring BD, Tarpley JE, et al. Fgf-10 is required for both limb and lung development and exhibits striking functional similarity to Drosophila branchless. Genes Dev 1998, 12:3156-3161. 10.1101/gad.12.20.3156, 317210, 9784490.
23. De ML, 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, 127:483-492.
24. Desai TJ, Malpel S, Flentke GR, Smith SM, Cardoso WV. Retinoic acid selectively regulates Fgf10 expression and maintains cell identity in the prospective lung field of the developing foregut. Dev Biol 2004, 273:402-415. 10.1016/j.ydbio.2004.04.039, 15328022.
25. Maden M. Retinoids in lung development and regeneration. Curr Top Dev Biol 2004, 61:153-189. full_text, 15350401.
26. Zeng X, Wert SE, Federici R, Peters KG, Whitsett JA. VEGF enhances pulmonary vasculogenesis and disrupts lung morphogenesis in vivo. Dev Dyn 1998, 211:215-227. 10.1002/(SICI)1097-0177(199803)211:3<215::AID-AJA3>3.0.CO;2-K, 9520109.
27. Bostrom H, Willetts K, Pekny M, Leveen P, Lindahl P, Hedstrand H, et al. PDGF-A signaling is a critical event in lung alveolar myofibroblast development and alveogenesis. Cell 1996, 85:863-873. 10.1016/S0092-8674(00)81270-2, 8681381.
28. Bellusci S, Furuta Y, Rush MG, Henderson R, Winnier G, Hogan BL. Involvement of Sonic hedgehog (Shh) in mouse embryonic lung growth and morphogenesis. Development 1997, 124:53-63.
29. Urase K, Mukasa T, Igarashi H, Ishii Y, Yasugi S, Momoi MY, et al. Spatial expression of Sonic hedgehog in the lung epithelium during branching morphogenesis. Biochem Biophys Res Commun 1996, 225:161-166. 10.1006/bbrc.1996.1147, 8769111.
30. Litingtung Y, Lei L, Westphal H, Chiang C. Sonic hedgehog is essential to foregut development. Nat Genet 1998, 20:58-61. 10.1038/1717, 9731532.
31. Kumar VH, Ryan RM. Growth factors in the fetal and neonatal lung. Front Biosci 2004, 9:464-480. 10.2741/1245, 14766383.
32. Merenmies J, Rauvala H. Molecular cloning of the 18-kDa growth-associated protein of developing brain. J Biol Chem 1990, 265:16721-16724.
33. Milner PG, Li YS, Hoffman RM, Kodner CM, Siegel NR, Deuel TF. A novel 17 kD heparin-binding growth factor (HBGF-8) in bovine uterus: purification and N-terminal amino acid sequence. Biochem Biophys Res Commun 1989, 165:1096-1103. 10.1016/0006-291X(89)92715-0, 2610682.
34. Rauvala H. An 18-kd heparin-binding protein of developing brain that is distinct from fibroblast growth factors. EMBO J 1989, 8:2933-2941. 401361, 2583087.
35. Kadomatsu K, Tomomura M, Muramatsu T. cDNA cloning and sequencing of a new gene intensely expressed in early differentiation stages of embryonal carcinoma cells and in mid-gestation period of mouse embryogenesis. Biochem Biophys Res Commun 1988, 151:1312-1318. 10.1016/S0006-291X(88)80505-9, 3355557.
36. Antoine M, Tag CG, Wirz W, Borkham-Kamphorst E, Sawitza I, Gressner AM, et al. Upregulation of pleiotrophin expression in rat hepatic stellate cells by PDGF and hypoxia: implications for its role in experimental biliary liver fibrogenesis. Biochem Biophys Res Commun 2005, 337:1153-1164. 10.1016/j.bbrc.2005.09.173, 16226713.
37. Herradon G, Ezquerra L, Nguyen T, Silos-Santiago I, Deuel TF. Midkine regulates pleiotrophin organ-specific gene expression: evidence for transcriptional regulation and functional redundancy within the pleiotrophin/midkine developmental gene family. Biochem Biophys Res Commun 2005, 333:714-721. 10.1016/j.bbrc.2005.05.160, 15985215.
38. Muramatsu T. Midkine and pleiotrophin: two related proteins involved in development, survival, inflammation and tumorigenesis. J Biochem 2002, 132:359-371.
39. Kadomatsu K, Muramatsu T. Midkine and pleiotrophin in neural development and cancer. Cancer Lett 2004, 204:127-143. 10.1016/S0304-3835(03)00450-6, 15013213.
40. Mitsiadis TA, Salmivirta M, Muramatsu T, Muramatsu H, Rauvala H, Lehtonen E, et al. Expression of the heparin-binding cytokines, midkine (MK) and HB-GAM (pleiotrophin) is associated with epithelial-mesenchymal interactions during fetal development and organogenesis. Development 1995, 121:37-51.
41. Li YS, Milner PG, Chauhan AK, Watson MA, Hoffman RM, Kodner CM, et al. Cloning and expression of a developmentally regulated protein that induces mitogenic and neurite outgrowth activity. Science 1990, 250:1690-1694. 10.1126/science.2270483, 2270483.
42. Vanderwinden JM, Mailleux P, Schiffmann SN, Vanderhaeghen JJ. Cellular distribution of the new growth factor pleiotrophin (HB-GAM) mRNA in developing and adult rat tissues. Anat Embryol (Berl) 1992, 186:387-406.
43. Neame PJ, Treep JT, Young CN. An 18-kDa glycoprotein from bovine nasal cartilage. Isolation and primary structure of small, cartilage-derived glycoprotein. J Biol Chem 1990, 265:9628-9633.
44. Tare RS, Oreffo RO, Clarke NM, Roach HI. Pleiotrophin/Osteoblast-stimulating factor 1: dissecting its diverse functions in bone formation. J Bone Miner Res 2002, 17:2009-2020. 10.1359/jbmr.2002.17.11.2009, 12412809.
45. Imai S, Kaksonen M, Raulo E, Kinnunen T, Fages C, Meng X, et al. Osteoblast recruitment and bone formation enhanced by cell matrix-associated heparin-binding growth-associated molecule (HB-GAM). J Cell Biol 1998, 143:1113-1128. 10.1083/jcb.143.4.1113, 2132954, 9817766.
46. Dreyfus J, Brunet-de CN, Duprez D, Raulais D, Vigny M. HB-GAM/pleiotrophin but not RIHB/midkine enhances chondrogenesis in micromass culture. Exp Cell Res 1998, 241:171-180. 10.1006/excr.1998.4040, 9633525.
47. Sato Y, Takita H, Ohata N, Tamura M, Kuboki Y. Pleiotrophin regulates bone morphogenetic protein (BMP)-induced ectopic osteogenesis. J Biochem 2002, 131:877-886.
48. Li G, Bunn JR, Mushipe MT, He Q, Chen X. Effects of pleiotrophin (PTN) over-expression on mouse long bone development, fracture healing and bone repair. Calcif Tissue Int 2005, 76:299-306. 10.1007/s00223-004-0145-6, 15812580.
49. Sakurai H, Bush KT, Nigam SK. Identification of pleiotrophin as a mesenchymal factor involved in ureteric bud branching morphogenesis. Development 2001, 128:3283-3293.
50. Yeh HJ, He YY, Xu J, Hsu CY, Deuel TF. Upregulation of pleiotrophin gene expression in developing microvasculature, macrophages, and astrocytes after acute ischemic brain injury. J Neurosci 1998, 18:3699-3707.
51. Deuel TF, Zhang N, Yeh HJ, Silos-Santiago I, Wang ZY. Pleiotrophin: a cytokine with diverse functions and a novel signaling pathway. Arch Biochem Biophys 2002, 397:162-171. 10.1006/abbi.2001.2705, 11795867.
52. Brewster L, Brey EM, Addis M, Xue L, Husak V, Ellinger J, et al. Improving endothelial healing with novel chimeric mitogens. Am J Surg 2006, 192:589-593. 10.1016/j.amjsurg.2006.08.005, 17071189.
53. Wellstein A, Fang WJ, Khatri A, Lu Y, Swain SS, Dickson RB, et al. A heparin-binding growth factor secreted from breast cancer cells homologous to a developmentally regulated cytokine. J Biol Chem 1992, 267:2582-2587.
54. Riegel AT, Wellstein A. The potential role of the heparin-binding growth factor pleiotrophin in breast cancer. Breast Cancer Res Treat 1994, 31:309-314. 10.1007/BF00666163, 7533562.
55. Garver RI, Radford DM, Donis-Keller H, Wick MR, Milner PG. Midkine and pleiotrophin expression in normal and malignant breast tissue. Cancer 1994, 74:1584-1590. 10.1002/1097-0142(19940901)74:5<1584::AID-CNCR2820740514>3.0.CO;2-V, 7520350.
56. Wu H, Barusevicius A, Babb J, Klein-Szanto A, Godwin A, Elenitsas R, et al. Pleiotrophin expression correlates with melanocytic tumor progression and metastatic potential. J Cutan Pathol 2005, 32:125-130. 10.1111/j.0303-6987.2005.00282.x, 15606670.
57. Seykora JT, Jih D, Elenitsas R, Horng WH, Elder DE. Gene expression profiling of melanocytic lesions. Am J Dermatopathol 2003, 25:6-11. 10.1097/00000372-200302000-00002, 12544092.
58. Powers C, Aigner A, Stoica GE, McDonnell K, Wellstein A. Pleiotrophin signaling through anaplastic lymphoma kinase is rate-limiting for glioblastoma growth. J Biol Chem 2002, 277:14153-14158. 10.1074/jbc.M112354200, 11809760.
59. Muller S, Kunkel P, Lamszus K, Ulbricht U, Lorente GA, Nelson AM, et al. A role for receptor tyrosine phosphatase zeta in glioma cell migration. Oncogene 2003, 22:6661-6668. 10.1038/sj.onc.1206763, 14555979.
60. Zhang L, Mabuchi T, Satoh E, Maeda S, Nukui H, Naganuma H. Overexpression of heparin-binding growth-associated molecule in malignant glioma cells. Neurol Med Chir (Tokyo) 2004, 44:637-643. 10.2176/nmc.44.637, 15684595.
61. Lu KV, Jong KA, Kim GY, Singh J, Dia EQ, Yoshimoto K, et al. Differential induction of glioblastoma migration and growth by two forms of pleiotrophin. J Biol Chem 2005, 280:26953-26964. 10.1074/jbc.M502614200, 15908427.
62. Zhang N, Zhong R, Perez-Pinera P, Herradon G, Ezquerra L, Wang ZY, et al. Identification of the angiogenesis signaling domain in pleiotrophin defines a mechanism of the angiogenic switch. Biochem Biophys Res Commun 2006, 343:653-658. 10.1016/j.bbrc.2006.03.006, 16554021.
63. Chauhan AK, Li YS, Deuel TF. Pleiotrophin transforms NIH 3T3 cells and induces tumors in nude mice. Proc Natl Acad Sci USA 1993, 90:679-682. 10.1073/pnas.90.2.679, 45727, 8421705.
64. Zhang N, Zhong R, Wang ZY, Deuel TF. Human breast cancer growth inhibited in vivo by a dominant negative pleiotrophin mutant. J Biol Chem 1997, 272:16733-16736. 10.1074/jbc.272.27.16733, 9201975.
65. Amet LE, Lauri SE, Hienola A, Croll SD, Lu Y, Levorse JM, et al. Enhanced hippocampal long-term potentiation in mice lacking heparin-binding growth-associated molecule. Mol Cell Neurosci 2001, 17:1014-1024. 10.1006/mcne.2001.0998, 11414790.
66. Carey DJ, Evans DM, Stahl RC, Asundi VK, Conner KJ, Garbes P, et al. Molecular cloning and characterization of N-syndecan, a novel transmembrane heparan sulfate proteoglycan. J Cell Biol 1992, 117:191-201. 10.1083/jcb.117.1.191, 2289399, 1556152.
67. Raulo E, Chernousov MA, Carey DJ, Nolo R, Rauvala H. Isolation of a neuronal cell surface receptor of heparin binding growth-associated molecule (HB-GAM). Identification as N-syndecan (syndecan-3). J Biol Chem 1994, 269:12999-13004.
68. Kinnunen T, Kaksonen M, Saarinen J, Kalkkinen N, Peng HB, Rauvala H. Cortactin-Src kinase signaling pathway is involved in N-syndecan-dependent neurite outgrowth. J Biol Chem 1998, 273:10702-10708. 10.1074/jbc.273.17.10702, 9553134.
69. Iwahara T, Fujimoto J, Wen D, Cupples R, Bucay N, Arakawa T, et al. Molecular characterization of ALK, a receptor tyrosine kinase expressed specifically in the nervous system. Oncogene 1997, 14:439-449. 10.1038/sj.onc.1200849, 9053841.
70. Morris SW, Naeve C, Mathew P, James PL, Kirstein MN, Cui X, et al. ALK, the chromosome 2 gene locus altered by the t(2;5) in non-Hodgkin's lymphoma, encodes a novel neural receptor tyrosine kinase that is highly related to leukocyte tyrosine kinase (LTK). Oncogene 1997, 14:2175-2188. 10.1038/sj.onc.1201062, 9174053.
71. Stoica GE, Kuo A, Aigner A, Sunitha I, Souttou B, Malerczyk C, et al. Identification of anaplastic lymphoma kinase as a receptor for the growth factor pleiotrophin. J Biol Chem 2001, 276:16772-16779. 10.1074/jbc.M010660200, 11278720.
72. Perez-Pinera P, Zhang W, Chang Y, Vega JA, Deuel TF. Anaplastic lymphoma kinase is activated through the pleiotrophin/receptor protein-tyrosine phosphatase beta/zeta signaling pathway: an alternative mechanism of receptor tyrosine kinase activation. J Biol Chem 2007, 282:28683-28690. 10.1074/jbc.M704505200, 17681947.
73. Gebbink MF, Zondag GC, Wubbolts RW, Beijersbergen RL, van EI, Moolenaar WH. Cell-cell adhesion mediated by a receptor-like protein tyrosine phosphatase. J Biol Chem 1993, 268:16101-16104.
74. Maeda N, Nishiwaki T, Shintani T, Hamanaka H, Noda M. 6B4 proteoglycan/phosphacan, an extracellular variant of receptor-like protein-tyrosine phosphatase zeta/RPTPbeta, binds pleiotrophin/heparin-binding growth-associated molecule (HB-GAM). J Biol Chem 1996, 271:21446-21452. 10.1074/jbc.271.35.21446, 8702927.
75. Meng K, Rodriguez-Pena A, Dimitrov T, Chen W, Yamin M, Noda M, et al. Pleiotrophin signals increased tyrosine phosphorylation of beta beta-catenin through inactivation of the intrinsic catalytic activity of the receptor-type protein tyrosine phosphatase beta/zeta. Proc Natl Acad Sci USA 2000, 97:2603-2608. 10.1073/pnas.020487997, 15975, 10706604.
76. Perez-Pinera P, Alcantara S, Dimitrov T, Vega JA, Deuel TF. Pleiotrophin disrupts calcium-dependent homophilic cell-cell adhesion and initiates an epithelial-mesenchymal transition. Proc Natl Acad Sci USA 2006, 103:17795-17800. 10.1073/pnas.0607299103, 1693826, 17098867.
77. Pariser H, Herradon G, Ezquerra L, Perez-Pinera P, Deuel TF. Pleiotrophin regulates serine phosphorylation and the cellular distribution of beta-adducin through activation of protein kinase C. Proc Natl Acad Sci USA 2005, 102:12407-12412. 10.1073/pnas.0505901102, 1194948, 16116087.
78. Pariser H, Perez-Pinera P, Ezquerra L, Herradon G, Deuel TF. Pleiotrophin stimulates tyrosine phosphorylation of beta-adducin through inactivation of the transmembrane receptor protein tyrosine phosphatase beta/zeta. Biochem Biophys Res Commun 2005, 335:232-239. 10.1016/j.bbrc.2005.07.060, 16105548.
79. Pariser H, Ezquerra L, Herradon G, Perez-Pinera P, Deuel TF. Fyn is a downstream target of the pleiotrophin/receptor protein tyrosine phosphatase beta/zeta-signaling pathway: regulation of tyrosine phosphorylation of Fyn by pleiotrophin. Biochem Biophys Res Commun 2005, 332:664-669. 10.1016/j.bbrc.2005.05.007, 15925565.
80. Perez-Pinera P, Garcia-Suarez O, Menendez-Rodriguez P, Mortimer J, Chang Y, Astudillo A, et al. The receptor protein tyrosine phosphatase (RPTP)beta/zeta is expressed in different subtypes of human breast cancer. Biochem Biophys Res Commun 2007, 362:5-10. 10.1016/j.bbrc.2007.06.050, 2084077, 17706593.
81. Hienola A, Pekkanen M, Raulo E, Vanttola P, Rauvala H. HB-GAM inhibits proliferation and enhances differentiation of neural stem cells. Mol Cell Neurosci 2004, 26:75-88. 10.1016/j.mcn.2004.01.018, 15121180.
82. Zou P, Muramatsu H, Sone M, Hayashi H, Nakashima T, Muramatsu T. Mice doubly deficient in the midkine and pleiotrophin genes exhibit deficits in the expression of beta-tectorin gene and in auditory response. Lab Invest 2006, 86:645-653. 10.1038/labinvest.3700428, 16619002.
83. Muramatsu H, Zou P, Kurosawa N, Ichihara-Tanaka K, Maruyama K, Inoh K, et al. Female infertility in mice deficient in midkine and pleiotrophin, which form a distinct family of growth factors. Genes Cells 2006, 11:1405-1417. 10.1111/j.1365-2443.2006.01028.x, 17121547.
84. Pavlov I, Voikar V, Kaksonen M, Lauri SE, Hienola A, Taira T, et al. Role of heparin-binding growth-associated molecule (HB-GAM) in hippocampal LTP and spatial learning revealed by studies on overexpressing and knockout mice. Mol Cell Neurosci 2002, 20:330-342. 10.1006/mcne.2002.1104, 12093164.
85. Hashimoto-Gotoh T, Ohnishi H, Tsujimura A, Tsunezuka H, Imai K, Masuda H, et al. Bone mass increase specific to the female in a line of transgenic mice overexpressing human osteoblast stimulating factor-1. J Bone Miner Metab 2004, 22:278-282. 10.1007/s00774-003-0485-8, 15108072.
86. Masuda H, Tsujimura A, Yoshioka M, Arai Y, Kuboki Y, Mukai T, et al. Bone mass loss due to estrogen deficiency is compensated in transgenic mice overexpressing human osteoblast stimulating factor-1. Biochem Biophys Res Commun 1997, 238:528-533. 10.1006/bbrc.1997.7188, 9299545.
87. Weng T, Chen Z, Jin N, Gao L, Liu L. Gene expression profiling identifies regulatory pathways involved in the late stage of rat fetal lung development. Am J Physiol Lung Cell Mol Physiol 2006, 291:L1027-L1037. 10.1152/ajplung.00435.2005, 16798779.
88. Weng T, Gao L, Bhaskaran M, Guo Y, Gou D, Narayanaperumal J, et al. Pleiotrophin regulates lung epithelial cell proliferation and differentiation during fetal lung development via {beta}-catenin and Dlk1. J Biol Chem 2009, 2788854, 19661059.
89. Chen HM, Campbell RA, Chang YC, Li MJ, Wang CS, Li J, et al. Pleiotrophin produced by multiple myeloma induces transdifferentiation of monocytes into vascular endothelial cells: a novel mechanism of tumor-induced vasculogenesis. Blood 2009, 113:1992-2002. 10.1182/blood-2008-02-133751, 2651013, 19060246.
90. Shu W, Guttentag S, Wang Z, Andl T, Ballard P, Lu MM, et al. Wnt/beta-catenin signaling acts upstream of N-myc, BMP4, and FGF signaling to regulate proximal-distal patterning in the lung. Dev Biol 2005, 283:226-239. 10.1016/j.ydbio.2005.04.014, 15907834.
91. Levay-Young BK, Navre M. Growth and developmental regulation of wnt-2 (irp) gene in mesenchymal cells of fetal lung. Am J Physiol 1992, 262:L672-L683.
92. Lako M, Strachan T, Bullen P, Wilson DI, Robson SC, Lindsay S. Isolation, characterisation and embryonic expression of WNT11, a gene which maps to 11q13.5 and has possible roles in the development of skeleton, kidney and lung. Gene 1998, 219:101-110. 10.1016/S0378-1119(98)00393-X, 9757009.
93. Weidenfeld J, Shu W, Zhang L, Millar SE, Morrisey EE. The WNT7b promoter is regulated by TTF-1, GATA6, and Foxa2 in lung epithelium. J Biol Chem 2002, 277:21061-21070. 10.1074/jbc.M111702200, 11914369.
94. Li C, Xiao J, Hormi K, Borok Z, Minoo P. Wnt5a participates in distal lung morphogenesis. Dev Biol 2002, 248:68-81. 10.1006/dbio.2002.0729, 12142021.
95. Konigshoff M, Balsara N, Pfaff EM, Kramer M, Chrobak I, Seeger W, et al. Functional Wnt signaling is increased in idiopathic pulmonary fibrosis. PLoS One 2008, 3:e2142. 10.1371/journal.pone.0002142, 2374879, 18478089.
96. Eberhart CG, Argani P. Wnt signaling in human development: beta-catenin nuclear translocation in fetal lung, kidney, placenta, capillaries, adrenal, and cartilage. Pediatr Dev Pathol 2001, 4:351-357. 10.1007/s10024001-0037-y, 11441336.
97. Tebar M, Destree O, de Vree WJ, Ten Have-Opbroek AA. Expression of Tcf/Lef and sFrp and localization of beta-catenin in the developing mouse lung. Mech Dev 2001, 109:437-440. 10.1016/S0925-4773(01)00556-1, 11731265.
98. 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, 17:290-298. 10.1016/j.devcel.2009.06.005, 2763331, 19686689.
99. Shu W, Jiang YQ, Lu MM, Morrisey EE. Wnt7b regulates mesenchymal proliferation and vascular development in the lung. Development 2002, 129:4831-4842.
100. De Langhe SP, Carraro G, Tefft D, Li C, Xu X, Chai Y, et al. Formation and differentiation of multiple mesenchymal lineages during lung development is regulated by beta-catenin signaling. PLoS One 2008, 3:e1516. 10.1371/journal.pone.0001516, 2211394, 18231602.
101. Mucenski ML, Wert SE, Nation JM, Loudy DE, Huelsken J, Birchmeier W, et al. beta-Catenin is required for specification of proximal/distal cell fate during lung morphogenesis. J Biol Chem 2003, 278:40231-40238. 10.1074/jbc.M305892200, 12885771.
102. Mucenski ML, Nation JM, Thitoff AR, Besnard V, Xu Y, Wert SE, et al. Beta-catenin regulates differentiation of respiratory epithelial cells in vivo. Am J Physiol Lung Cell Mol Physiol 2005, 289:L971-L979. 10.1152/ajplung.00172.2005, 16040629.
103. Rajagopal J, Carroll TJ, Guseh JS, Bores SA, Blank LJ, Anderson WJ, et al. Wnt7b stimulates embryonic lung growth by coordinately increasing the replication of epithelium and mesenchyme. Development 2008, 135:1625-1634. 10.1242/dev.015495, 2556060, 18367557.
104. Cohen ED, Ihida-Stansbury K, Lu MM, Panettieri RA, Jones PL, Morrisey EE. Wnt signaling regulates smooth muscle precursor development in the mouse lung via a tenascin C/PDGFR pathway. Journal of Clinical Investigation 2009, 119:2538-2549. 10.1172/JCI38079, 2735923, 19690384.
105. Morrisey EE, Shu WG, Lu MM. Wnt7b regulates vascular smooth muscle development in the lung. Circulation 2002, 106:686.
106. Okubo T, Hogan BL. Hyperactive Wnt signaling changes the developmental potential of embryonic lung endoderm. J Biol 2004, 3:11. 10.1186/jbiol3, 469027, 15186480.
107. Nemeth MJ, Topol L, Anderson SM, Yang Y, Bodine DM. Wnt5a inhibits canonical Wnt signaling in hematopoietic stem cells and enhances repopulation. Proc Natl Acad Sci USA 2007, 104:15436-15441. 10.1073/pnas.0704747104, 1986571, 17881570.
108. Vuga LJ, Ben-Yehudah A, Kovkarova-Naumovski E, Oriss T, Gibson KF, Feghali-Bostwick C, et al. WNT5A Is a Regulator of Fibroblast Proliferation and Resistance to Apoptosis. Am J Respir Cell and Mol Biol 2009, 41:583-589.
109. Pongracz JE, Stockley RA. Wnt signalling in lung development and diseases. Respir Res 2006, 7:15. 10.1186/1465-9921-7-15, 1397816, 16438732.
110. Liu L, Carron B, Yee HT, Yie TA, Hajjou M, Rom WN. Wnt Pathway in Pulmonary Fibrosis in the Bleomycin Mouse Model. J Environ Pathol Toxicol Oncol 2009, 28:99-108.
111. Dasgupta C, Sakurai R, Wang Y, Guo P, Ambalavanan N, Torday JS, et al. Hyperoxia-induced neonatal rat lung injury involves activation of TGF-{beta} and Wnt signaling and is protected by rosiglitazone. Am J Physiol Lung Cell Mol Physiol 2009, 296:L1031-L1041. 10.1152/ajplung.90392.2008, 19304912.