Neuregulin receptor ErbB4 functions as a transcriptional cofactor for the expression of surfactant protein B in the fetal lung

American Journal of Respiratory Cell and Molecular Biology

Volumn 45, Issue 4, 2011, Pages 761-767

  Zscheppang, Katja ^a   Dörk, Thilo ^a   Schmiedl, Andreas ^a   Jones, Frank E ^b   Dammann, Christiane E L ^a,c  

^a HANNOVER MEDICAL SCHOOL   (Germany)

^b Tulane University   (United States)

^c TUFTS MEDICAL CENTER   (United States)

Author keywords

Lung development; Stat5a; Surfactant; Type II cell

Indexed keywords

EPIDERMAL GROWTH FACTOR RECEPTOR 4; MESSENGER RNA; NEU DIFFERENTIATION FACTOR; STAT5A PROTEIN; SURFACTANT PROTEIN A; SURFACTANT PROTEIN B; SURFACTANT PROTEIN C; SURFACTANT PROTEIN D;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CELL PROLIFERATION; CONTROLLED STUDY; FETUS LUNG; LUNG ALVEOLUS EPITHELIUM; MOUSE; NONHUMAN; PROMOTER REGION; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN PROTEIN INTERACTION; PROTEIN TRANSPORT; TRANSCRIPTION REGULATION;

ACTIVE TRANSPORT, CELL NUCLEUS; ANIMALS; BINDING SITES; CELLS, CULTURED; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GENES, REPORTER; GESTATIONAL AGE; HUMANS; LUNG; MICE; MICE, KNOCKOUT; MICE, TRANSGENIC; NEUREGULIN-1; PNEUMOCYTES; PROMOTER REGIONS, GENETIC; PULMONARY SURFACTANT-ASSOCIATED PROTEIN B; RECEPTOR, EPIDERMAL GROWTH FACTOR; RNA, MESSENGER; STAT5 TRANSCRIPTION FACTOR; TIME FACTORS; TRANSCRIPTION, GENETIC; TRANSFECTION;

EID: 80053633156     PISSN: 10441549     EISSN: None     Source Type: Journal    
DOI: 10.1165/rcmb.2010-0179OC     Document Type: Article

References (53)

1. Birchmeier C. ErbB receptors and the development of the nervous system. Exp Cell Res 2009;315:611-618.
2. Michailov GV, Sereda MW, Brinkmann BG, Fischer TM, Haug B, Birchmeier C, Role L, Lai C, Schwab MH, Nave KA. Axonal neuregulin-1 regulates myelin sheath thickness. Science 2004;304:700-703. (Pubitemid 38560869)
3. Tidcombe H, Jackson-Fisher A, Mathers K, Stern DF, Gassmann M, Golding JP. Neural and mammary gland defects in ErbB4 knockout mice genetically rescued from embryonic lethality. Proc Natl Acad Sci USA 2003;100:8281-8286. (Pubitemid 36842536)
4. Dammann CE, Nielsen HC, Carraway KL. Role of neuregulin1{beta} in the developing lung. Am J Respir Crit Care Med 2003;167:1711-1716.
5. Liu W, Purevdorj E, Zscheppang K, von Mayersbach D, Behrens J, Brinkhaus MJ, Nielsen HC, Schmiedl A, Dammann CE. ErbB4 regulates the timely progression of late fetal lung development. Biochim Biophys Acta 2010;1803:832-839.
6. Nielsen HC. Epidermal growth factor influences the development clock regulating maturation of the fetal lung fibroblast. Biochim Biophys Acta 1989;1012:201-206. (Pubitemid 19181754)
7. Langston C, Kida K, Reed M. Human lung growth in late gestation and in the neonate. Am Rev Respir Dis 1984;129:607-613. (Pubitemid 14126782)
8. Liu W, Zscheppang K, Murray S, Nielsen HC, Dammann CE. The ErbB4 receptor in fetal rat lung fibroblasts and epithelial Type II cells. Biochim Biophys Acta 2007;1772:737-747.
9. Zscheppang K, Liu W, Volpe MV, Nielsen HC, Dammann CE. ErbB4 regulates fetal surfactant phospholipid synthesis in primary fetal rat Type II cells. Am J Physiol Lung Cell Mol Physiol 2007;293:L429-L435. (Pubitemid 47205023)
10. Purevdorj E, Zscheppang K, Hoymann HG, Braun A, von Mayersbach D, Brinkhaus MJ, Schmiedl A, Dammann CE. ErbB4 deletion leads to changes in lung function and structure similar to bronchopulmonary dysplasia. Am J Physiol Lung Cell Mol Physiol 2008;294:L516-L522. (Pubitemid 351468851)
11. Prevot V, Lomniczi A, Corfas G, Ojeda SR. ErbB-1 and ErbB-4 receptors act in concert to facilitate female sexual development and mature reproductive function. Endocrinology 2005;146:1465-1472. (Pubitemid 40289336)
12. Jones FE. HER4 intracellular domain (4ICD) activity in the developing mammary gland and breast cancer. J Mammary Gland Biol Neoplasia 2008;13:247-258.
13. Golub MS, Germann SL, Lloyd KCK. Behavioral characteristics of a nervous system-specific ErbB4 knock-out mouse. Behav Brain Res 2004 2004;153:159-170.
14. Rio C, Buxbaum JD, Peschon JJ, Corfas G. Tumor necrosis factor-alpha-converting enzyme is required for cleavage of ErbB4/HER4. J Biol Chem 2000;275:10379-10387. (Pubitemid 30202097)
15. Ni CY, Murphy MP, Golde TE, Carpenter G. Gamma-secretase cleavage and nuclear localization of ErbB-4 receptor tyrosine kinase. Science 2001;294:2179-2181. (Pubitemid 33150677)
16. Lee HJ, Jung KM, Huang YZ, Bennett LB, Lee JS, Mei L, Kim TW. Presenilin-dependent gamma-secretase-like intramembrane cleavage of ErbB4. J Biol Chem 2002;277:6318-6323. (Pubitemid 34968424)
17. Williams CC, Allison JG, Vidal GA, Burow ME, Beckman BS, Marrero L, Jones FE. The ERBB4/HER4 receptor tyrosine kinase regulates gene expression by functioning as a STAT5A nuclear chaperone. J Cell Biol 2004;167:469-478. (Pubitemid 39489055)
18. Li C, Zhu NL, Tan RC, Ballard PL, Derynck R, Minoo P. Transforming growth factor-beta inhibits pulmonary surfactant protein B gene transcription through SMAD3 interactions with NKX2.1 and HNF- 3 transcription factors. J Biol Chem 2002;277:38399-38408. (Pubitemid 35154696)
19. Glasser SW, Korfhagen TR, Bruno MD, Dey C, Whitsett JA. Structure and expression of the pulmonary surfactant protein SP-C gene in the mouse. J Biol Chem 1990;265:21986-21991. (Pubitemid 120014253)
20. Kalina M, Mason RJ, Shannon JM. Surfactant protein C is expressed in alveolar Type II cells but not in Clara cells of rat lung. Am J Respir Cell Mol Biol 1992;6:594-600.
21. Boggaram V. Thyroid transcription factor-1 (TTF-1/Nkx2.1/TITF1) gene regulation in the lung. Clin Sci (Lond) 2009;116:27-35.
22. Smith BT. Lung maturation in the fetal rat: acceleration by injection of fibroblast pneumocyte factor. Science 1979;204:1094-1095. (Pubitemid 10199156)
23. Stefansson H, Sigurdsson E, Steinthorsdottir V, Bjornsdottir S, Sigmundsson T, Ghosh S, Brynjolfsson J, Gunnarsdottir S, Ivarsson O, Chou TT, et al. Neuregulin 1 and susceptibility to schizophrenia. Am J Hum Genet 2002;71:877-892. (Pubitemid 135750519)
24. Roy K, Murtie JC, El-Khodor BF, Edgar N, Sardi SP, Hooks BM, Benoit-Marand M, Chen C, Moore H, O'Donnell P, et al. Loss of ErbB signaling in oligodendrocytes alters myelin and dopaminergic function, a potential mechanism for neuropsychiatric disorders. Proc Natl Acad Sci USA 2007;104:8131-8136. (Pubitemid 47185887)
25. Dammann O, Cesario A, Hallen M. NEOBRAIN: an EU-funded project committed to protect the newborn brain. Neonatology 2007;92:217-218. (Pubitemid 350125277)
26. Li Y, Xu Z, Ford GD, Croslan DR, Cairobe T, Li Z, Ford BD. Neuroprotection by neuregulin-1 in a rat model of permanent focal cerebral ischemia. Brain Res 2007;1184:277-283. (Pubitemid 350160568)
27. Crowley PA. Antenatal corticosteroid therapy: a meta-analysis of the randomized trials, 1972 to 1994. Am J Obstet Gynecol 1995;173:322-335.
28. Jobe AJ. The new BPD: an arrest of lung development. Pediatr Res 1999;46:641-643.
29. Bonanno C, Wapner RJ. Antenatal corticosteroid treatment: what's happened since Drs. Liggins and Howie? Am J Obstet Gynecol 2009;200:448-457.
30. Jobe AH, Bancalari E. Bronchopulmonary dysplasia. Am J Respir Crit Care Med 2001;163:1723-1729. (Pubitemid 32578778)
31. Bose CL, Dammann CE, Laughon MM. Bronchopulmonary dysplasia and inflammatory biomarkers in the premature neonate. Arch Dis Child Fetal Neonatal Ed 2008;93:F455-F461.
32. Zscheppang K, Korenbaum E, Bueter W, Ramadurai SM, Nielsen HC, Dammann CE. ErbB receptor dimerization, localization, and colocalization in mouse lung Type II epithelial cells. Pediatr Pulmonol 2006;41:1205-1212. (Pubitemid 44893875)
33. Burri PH. Fetal and postnatal development of the lung. Annu Rev Physiol 1984;46:617-628. (Pubitemid 14147819)
34. Adamson IY, Bowden DH. Derivation of Type 1 epithelium from Type 2 cells in the developing rat lung. Lab Invest 1975;32:736-745.
35. 2. Exp Mol Pathol 1975;22:142-150.
36. Rooney SA. Regulation of surfactant secretion. Comp Biochem Physiol A Mol Integr Physiol 2001;129:233-243. (Pubitemid 32455721)
37. Nogee LM, de Mello DE, Dehner LP, Colten HR. Brief report: deficiency of pulmonary surfactant protein B in congenital alveolar proteinosis. N Engl J Med 1993;328:406-410. (Pubitemid 23042289)
38. Hamm H, Kroegel C, Hohlfeld J. Surfactant: a review of its functions and relevance in adult respiratory disorders. Respir Med 1996;90:251-270. (Pubitemid 26169605)
39. Liu J, Kern JA. Neuregulin-1 activates the JAK-STAT pathway and regulates lung epithelial cell proliferation. Am J Respir Cell Mol Biol 2002;27:306-313. (Pubitemid 34979288)
40. Grimley PM, Dong F, Rui H. Stat5a and Stat5b: fraternal twins of signal transduction and transcriptional activation. Cytokine Growth Factor Rev 1999;10:131-157. (Pubitemid 29446377)
41. D'Amore-Bruno MA, Wikenheiser KA, Carter JE, Clark JC, Whitsett JA. Sequence, ontogeny, and cellular localization of murine surfactant protein B mRNA. Am J Physiol 1992;262:L40-L47.
42. Margana RK, Boggaram V. Rabbit surfactant protein B gene: structure and functional characterization of the promoter. Am J Physiol 1996;270:L601-L612.
43. Pryhuber GS. Regulation and function of pulmonary surfactant protein B. Mol Genet Metab 1998;64:217-228. (Pubitemid 28460219)
44. Lin SY, Makino K, Xia W, Matin A, Wen Y, Kwong KY, Bourguignon L, Hung MC. Nuclear localization of EGF receptor and its potential new role as a transcription factor. Nat Cell Biol 2001;3:802-808. (Pubitemid 32842685)
45. Hung LY, Tseng JT, Lee YC, Xia W, Wang YN, Wu ML, Chuang YH, Lai CH, Chang WC. Nuclear epidermal growth factor receptor (EGFR) interacts with signal transducer and activator of transcription 5 (STAT5) in activating Aurora-A gene expression. Nucleic Acids Res 2008;36:4337-4351.
46. Wang SC, Lien HC, Xia W, Chen IF, Lo HW, Wang Z, Ali-Seyed M, Lee DF, Bartholomeusz G, Ou-Yang F, et al. Binding at and transactivation of the COX-2 promoter by nuclear tyrosine kinase receptor ErbB-2. Cancer Cell 2004;6:251-261. (Pubitemid 39222038)
47. Wang SC, Hung MC. Nuclear translocation of the epidermal growth factor receptor family membrane tyrosine kinase receptors. Clin Cancer Res 2009;15:6484-6489.
48. Blagoev B, Kratchmarova I, Ong SE, Nielsen M, Foster LJ, Mann M. A proteomics strategy to elucidate functional protein-protein interactions applied to EGF signaling. Nat Biotechnol 2003;21:315-318. (Pubitemid 36314817)
49. Olayioye MA, Beuvink I, Horsch K, Daly JM, Hynes NE. ErbB receptor-induced activation of Stat transcription factors is mediated by Src tyrosine kinases. J Biol Chem 1999;274:17209-17218.
50. Naresh A, Long W, Vidal GA, Wimley WC, Marrero L, Sartor CI, Tovey S, Cooke TG, Bartlett JM, Jones FE. The ERBB4/HER4 intracellular domain 4ICD is a BH3-only protein promoting apoptosis of breast cancer cells. Cancer Res 2006;66:6412-6420.
51. Zhu Y, Sullivan LL, Nair SS, Williams CC, Pandey AK, Marrero L, Vadlamudi RK, Jones FE. Coregulation of estrogen receptor by ERBB4/HER4 establishes a growth-promoting autocrine signal in breast tumor cells. Cancer Res 2006;66:7991-7998. (Pubitemid 44299163)
52. Cannella B, Hoban CJ, Gao YL, Garcia-Arenas R, Lawson D, Marchionni M, Gwynne D, Raine CS. The neuregulin, glial growth factor 2, diminishes autoimmune demyelination and enhances remyelination in a chronic relapsing model for multiple sclerosis. Proc Natl Acad Sci USA 1998;95:10100-10105. (Pubitemid 28415301)
53. Jabbour A, Hayward CS, Keogh AM, Kotlyar E, McCrohon JA, England JF, Amor R, Liu X, Li XY, Zhou MD. et al. Parenteral administration of recombinant human neuregulin-1 to patients with stable chronic heart failure produces favourable acute and chronic haemodynamic responses. Eur J Heart Fail 2011;13:83-92.