Presenilin-1 processing of ErbB4 in fetal type II cells is necessary for control of fetal lung maturation

Biochimica et Biophysica Acta - Molecular Cell Research

Volumn 1813, Issue 3, 2011, Pages 480-491

  Hoeing, Kristina ^a,b   Zscheppang, Katja ^b   Mujahid, Sana ^c   Murray, Sandy ^a   Volpe, MaryAnn V ^a   Dammann, Christiane E L ^a,b   Nielsen, Heber C ^a,b,c  

^a TUFTS MEDICAL CENTER   (United States)

^b HANNOVER MEDICAL SCHOOL   (Germany)

^c TUFTS UNIVERSITY   (United States)

Author keywords

ErbB receptors; Fetal lung; Gamma secretase; Surfactant proteins; Type II cells; Yes associated protein

Indexed keywords

EPIDERMAL GROWTH FACTOR RECEPTOR 4; MESSENGER RNA; NEU DIFFERENTIATION FACTOR; PRESENILIN 1; PROTEIN KINASE YES; SURFACTANT;

ANIMAL CELL; ARTICLE; CELL ISOLATION; CELL MATURATION; CONTROLLED STUDY; FETUS; FETUS LUNG MATURATION; FRACTIONATION; GENE EXPRESSION; GENETIC TRANSFECTION; IMMUNOFLUORESCENCE; IMMUNOPRECIPITATION; LUNG DEVELOPMENT; MOUSE; NONHUMAN; PHOSPHORYLATION; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN CLEAVAGE; SIGNAL TRANSDUCTION;

ADAPTOR PROTEINS, SIGNAL TRANSDUCING; AMYLOID PRECURSOR PROTEIN SECRETASES; ANIMALS; CELLS, CULTURED; FETUS; GENE EXPRESSION REGULATION, DEVELOPMENTAL; LUNG; MICE; NEUREGULINS; PEPTIDES; PHOSPHOPROTEINS; PRESENILIN-1; RECEPTOR, EPIDERMAL GROWTH FACTOR; RNA, MESSENGER;

EID: 79951901849     PISSN: 01674889     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.bbamcr.2010.12.017     Document Type: Article

References (57)

1. Avery M.E., Mead J. Surface properties in relation to atelectasis and hyaline membrane disease. AMA J. Dis. Child. 1959, 97:517-523.
2. Jobe A.H., Ikegami M. Surfactant metabolism. Clin. Perinatol. 1993, 20:683-696.
3. Dammann C.E., Nielsen H.C., Carraway K.L. Role of neuregulin1b in the developing lung. Am. J. Resp. Crit. Care Med. 2003, 167:1711-1716.
4. Zscheppang K., Liu W., Volpe M.V., Nielsen H.C., Dammann C.E.L. ErbB4 regulates fetal surfactant phospholipid synthesis in primary fetal rat type II cells. Am. J. Physiol. Lung Cell. Mol. Physiol. 2007, 293:429-435.
5. Liu W., Zscheppang K., Murray S., Nielsen H.C., Dammann C.E.L. The ErbB4 receptor in fetal rat lung fibroblasts and type II cells. Biochim. Biophys. Acta 2007, 1772:737-747.
6. Gassmann M., Casagranda F., Orioll D., Simon H., Lai C., Klein R., Lemke G. Aberrant neural and cardiac development in mice lacking the ErbB4 neuregulin receptor. Nature 1995, 378:390-394.
7. Lee K.-F., Simon H., Chen H., Bates B., Hung M.-C., Hauser C. Requirement for neuregulin receptor erbB2 in neural and cardiac development. Nature 1995, 378:394-398.
8. Meyer D., Birchmeier C. Multiple essential functions of neuregulin in development. Nature 1995, 378:386-390.
9. Riethmacher D., Sonnenberg-Riethmacher E., Brinkmann V., Yamaai T., Lewin G.R., Birchmeier C. Severe neuropathies in mice with targeted mutations in the ErbB3 receptor. Nature 1997, 389:725-730.
10. Liu W., Purevdorj E., Zscheppang K., von Mayersbach D., Behrens J., Brinkhaus M.-J., Nielsen H.C., Schmiedl A., Dammann C.E.L. ErbB4 regulates the timely progression of late fetal lung development. Biochim. Biophys. Acta 2010, 1803:832-839.
11. Purevdorj E., Zscheppang K., Hoymann H.G., Braun A., von Mayersbach D., Brinkhaus M.-J., Schmiedl A., Dammann C.E.L. 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.
12. Zscheppang K., Korenbaum E., Bueter W., Ramadurai S., Nielsen H.C., Dammann C.E.L. ErbB4 receptor dimerization, localization and co-localization in mouse lung type II epithelial cells. Pediatr. Pulmonol. 2006, 41:1205-1212.
13. Ni C.-Y., Murphy M.P., Golde T.E., Carpenter G. g-Secretase cleavage and nuclear localization of ErbB-4 receptor tyrosine kinase. Science 2001, 294:2179-2181.
14. Vecchi M., Baulida J., Carpenter G. Selective cleavage of the heregulin receptor ErbB-4 by protein kinase C activation. J. Biol. Chem. 1996, 271:18989-18995.
15. Zhou W., Carpenter G. Heregulin-dependent trafficking and cleavage of ErbB-4. J. Biol. Chem. 2000, 275:34737-34743.
16. Rio C., Buxbaum J.D., Peschon J.J., Corfas G. Tumor necrosis factor-alpha-converting enzyme is required for cleavage of erbB4/HER4. J. Biol. Chem. 2000, 275:10379-10387.
17. Cheng Q.C., Tikhomirov O., Zhou W., Carpenter G. Ectodomain cleavage of ErbB-4: characterization of the cleavage site and m80 fragment. J. Biol. Chem. 2003, 278:38421-38427.
18. Lee H.J., Jung K.M., Huang Y.Z., Bennett L.B., Lee J.S., Mei L., Kim T.W. Presenilin-dependent gamma-secretase-like intramembrane cleavage of ErbB4. J. Biol. Chem. 2002, 277:6318-6323.
19. Capell A., Grunberg J., Pesold B., Diehlmann A., Citron M., Nixon R., Beyreuther K., Selkoe D.J., Haass C. The proteolytic fragments of the Alzheimer's disease-associated presenilin-1 form heterodimers and occur as a 100-150-kDa molecular mass complex. J. Biol. Chem. 1998, 273:3205-3211.
20. Chen F., Yu G., Arawaka S., Nishimura M., Kawarai T., Yu H., Tandon A., Supala A., Song Y.Q., Rogaeva E., Milman P., Sato C., Yu C., Janus C., Lee J., Song L., Zhang L., Fraser P.E., St George-Hyslop P.H. Nicastrin binds to membrane-tethered Notch. Nat. Cell Biol. 2001, 3:751-754.
21. Edbauer D., Winkler E., Regula J.T., Pesold B., Steiner H., Haass C. Reconstitution of gamma-secretase activity. Nat. Cell Biol. 2003, 5:486-488.
22. Esler W.P., Kimberly W.T., Ostaszewski B.L., Diehl T.S., Moore C.L., Tsai J.Y., Rahmati T., Xia W., Selkoe D.J., Wolfe M.S. Transition-state analogue inhibitors of gamma-secretase bind directly to presenilin-1. Nat. Cell Biol. 2000, 2:428-434.
23. Francis R., McGrath G., Zhang J., Ruddy D.A., Sym M., Apfeld J., Nicoll M., Maxwell M., Hai B., Ellis M.C., Parks A.L., Xu W., Li J., Gurney M., Myers R.L., Himes C.S., Hiebsch R., Ruble C., Nye J.S., Curtis D. aph-1 and pen-2 are required for Notch pathway signaling, gamma-secretase cleavage of betaAPP, and presenilin protein accumulation. Dev. Cell 2002, 3:85-97.
24. Li Y.M., Lai M.T., Xu M., Huang Q., DiMuzio-Mower J., Sardana M.K., Shi X.P., Yin K.C., Shafer J.A., Gardell S.J. Presenilin 1 is linked with gamma-secretase activity in the detergent solubilized state. Proc. Natl. Acad. Sci. U. S. A 2000, 97:6138-6143.
25. Yu G., Nishimura M., Arawaka S., Levitan D., Zhang L., Tandon A., Song Y.Q., Rogaeva E., Chen F., Kawarai T., Supala A., Levesque L., Yu H., Yang D.S., Holmes E., Milman P., Liang Y., Zhang D.M., Xu D.H., Sato C., Rogaev E., Smith M., Janus C., Zhang Y., Aebersold R., Farrer L.S., Sorbi S., Bruni A., Fraser P., St George-Hyslop P. Nicastrin modulates presenilin-mediated notch/glp-1 signal transduction and betaAPP processing. Nature 2000, 407:48-54.
26. Goutte C., Tsunozaki M., Hale V.A., Priess J.R. APH-1 is a multipass membrane protein essential for the Notch signaling pathway in Caenorhabditis elegans embryos. Proc. Natl. Acad. Sci. U. S. A 2002, 99:775-779.
27. Omerovic J., Puggioni E.M., Napoletano S., Visco V., Fraioli R., Frati L., Gulino A., Alimandi M. Ligand-regulated association of ErbB-4 to the transcriptional co-activator YAP65 controls transcription at the nuclear level. Exp. Cell Res. 2004, 294:469-479.
28. Basu S., Totty N.F., Irwin M.S., Sudol M., Downward J. Akt phosphorylates the Yes-associated protein, YAP, to induce interaction with 14-3-3 and attenuation of p73-mediated apoptosis. Mol. Cell 2003, 11:11-23.
29. Kanai F., Marignani P.A., Sarbassova D., Yagi R., Hall R.A., Donowitz M., Hisaminato A., Fujiwara T., Ito Y., Cantley L.C., Yaffe M.B. TAZ: a novel transcriptional co-activator regulated by interactions with 14-3-3 and PDZ domain proteins. EMBO J. 2000, 19:6778-6791.
30. Komuro A., Nagai M., Navin N.E., Sudol M. WW domain-containing protein YAP associates with ErbB-4 and Acts as a co-transcriptional activator for the carboxyl-terminal fragment of ErbB-4 that translocates to the nucleus. J. Biol. Chem. 2003, 278:33334-33341.
31. Sardi S.P., Murtie J., Koirala S., Patten B.A., Corfas G. Presenilin-dependent ErbB4 nuclear signaling regulates the timing of astrogenesis in the developing brain. Cell 2006, 127:185-197.
32. Volpe M., Wang K.T.W., Nielsen H.C., Chinoy M.R. Unique spatial and temporal expression patterns of Hoxa5, Hoxb4 and Hoxb6 in normal developing murine lung are modified in pulmonary hypoplasia. Birth Defects Res. A 2008, 82:571-584.
33. Villanueva D., Wang K., Nielsen H.C., Ramadurai S.M. Expression of specific protein kinase C isoforms and ligand-specific activation of PKCa in late gestation fetal lung. Exp. Lung Res. 2007, 33:185-196.
34. Bueter W., Dammann O., Zscheppang K., Korenbaum E., Dammann C.E. ErbB receptors in fetal endothelium-a potential linkage point for inflammation-associated neonatal disorders. Cytokine 2006, 36:267-275.
35. Chomczynski P., Sacchi N. Single-step method of RNA isolation by acid guanidium thiocyanate-phenol-chloroform extraction. Anal. Biochem. 1987, 162:156-159.
36. Garratt A.N., Voiculescu O., Topilko P., Charnay P., Birchmeier C. A dual role of erbB2 in myelination and in expansion of the schwann cell precursor pool. J. Cell Biol. 2000, 148:1035-1046.
37. Seiffert D., Bradley J.D., Rominger C.M., Rominger D.H., Yang F., Meredith J.E., Wang Q., Roach A.H., Thompson L.A., Spitz S.M., Higaki J.N., Prakash S.R., Combs A.P., Copeland R.A., Arneric S.P., Hartig P.R., Robertson D.W., Cordell B., Stern A.M., Olson R.E., Zaczek R. Presenilin-1 and -2 are molecular targets for gamma-secretase inhibitors. J. Biol. Chem. 2000, 275:34086-34091.
38. Furukawa K., Pante N., Aebi U., Gerace L. Cloning of a cDNA for lamina-associated polypeptide 2 (LAP2) and identification of regions that specify targeting to the nuclear envelope. EMBO J. 1995, 14:1626-1636.
39. Tidcombe H., Jackson-Fisher A., Mathers K., Stern D.F., Gassmann M., Golding J.P. Neural and mammary gland defects in ErbB4 knockout mice genetically rescued from embryonic lethality. Proc. Natl Acad. Sci. USA 2003, 100:8281-8286.
40. Shen J., Bronson R.T., Chen D.F., Xia W., Selkoe D.J., Tonegawa S. Skeletal and CNS defects in presenilin-1-deficient mice. Cell 1997, 89:629-639.
41. Herreman A., Hartmann D., Annaert W., Saftig P., Craessaerts K., Serneels L., Umans L., Schrijvers V., Checler F., Vanderstichele H., Baekelandt V., Dressel R., Cupers P., Huylebroeck D., Zwijsen A., Van L.F., De S.B. Presenilin 2 deficiency causes a mild pulmonary phenotype and no changes in amyloid precursor protein processing but enhances the embryonic lethal phenotype of presenilin 1 deficiency. Proc. Natl. Acad. Sci. U. S. A 1999, 96:11872-11877.
42. Mastrangelo P., Mathews P.M., Chishti M.A., Schmidt S.D., Gu Y., Yang J., Mazzella M.J., Coomaraswamy J., Horne P., Strome B., Pelly H., Levesque G., Ebeling C., Jiang Y., Nixon R.A., Rozmahel R., Fraser P.E., St George-Hyslop P., Carlson G.A., Westaway D. Dissociated phenotypes in presenilin transgenic mice define functionally distinct gamma-secretases. Proc. Natl. Acad. Sci. U. S. A 2005, 102:8972-8977.
43. Lai M.T., Chen E., Crouthamel M.C., DiMuzio-Mower J., Xu M., Huang Q., Price E., Register R.B., Shi X.P., Donoviel D.B., Bernstein A., Hazuda D., Gardell S.J., Li Y.M. Presenilin-1 and presenilin-2 exhibit distinct yet overlapping gamma-secretase activities. J. Biol. Chem. 2003, 278:22475-22481.
44. Morin-Kensicki E.M., Boone B.N., Howell M., Stonebraker J.R., Teed J., Alb J.G., Magnuson T.R., O'Neal W., Milgram S.L. Defects in yolk sac vasculogenesis, chorioallantoic fusion, and embryonic axis elongation in mice with targeted disruption of Yap65. Mol. Cell. Biol. 2006, 26:77-87.
45. Burri P.H. Fetal and postnatal development of the lung. Annu. Rev. Physiol. 1984, 46:617-628.
46. Wen P.H., Friedrich V.L., Shioi J., Robakis N.K., Elder G.A. Presenilin-1 is expressed in neural progenitor cells in the hippocampus of adult mice. Neurosci. Lett. 2002, 318:53-56.
47. Uemura K., Kuzuya A., Shimozono Y., Aoyagi N., Ando K., Shimohama S., Kinoshita A. GSK3beta activity modifies the localization and function of presenilin 1. J. Biol. Chem. 2007, 282:15823-15832.
48. Li J., Xu M., Zhou H., Ma J., Potter H. Alzheimer presenilins in the nuclear membrane, interphase kinetochores, and centrosomes suggest a role in chromosome segregation. Cell 1997, 90:917-927.
49. Jeong S.J., Kim H.S., Chang K.A., Geum D.H., Park C.H., Seo J.H., Rah J.C., Lee J.H., Choi S.H., Lee S.G., Kim K., Suh Y.H. Subcellular localization of presenilins during mouse preimplantation development. FASEB J. 2000, 14:2171-2176.
50. Van G.G., Annaert W., Van B.C. Binding partners of Alzheimer's disease proteins: are they physiologically relevant?. Neurobiol. Dis. 2000, 7:135-151.
51. Parks A.L., Curtis D. Presenilin diversifies its portfolio. Trends Genet. 2007, 23:140-150.
52. Dillen K., Annaert W. A two decade contribution of molecular cell biology to the centennial of Alzheimer's disease: are we progressing toward therapy?. Int. Rev. Cytol. 2006, 254:215-300.
53. Kim J., Hamamoto S., Ravazzola M., Orci L., Schekman R. Uncoupled packaging of amyloid precursor protein and presenilin 1 into coat protein complex II vesicles. J. Biol. Chem. 2005, 280:7758-7768.
54. Selkoe D., Kopan R. Notch and presenilin: regulated intramembrane proteolysis links development and degeneration. Annu. Rev. Neurosci. 2003, 26:565-597.
55. Carpenter G., Liao H.J. Trafficking of receptor tyrosine kinases to the nucleus. Exp. Cell Res. 2009, 315:1556-1566.
56. Muraoka-Cook R.S., Sandahl M.A., Strunk K.E., Miraglia L.C., Husted C., Hunter D.M., Elenius K., Chodosh L.A., Earp H.S. ErbB4 splice variants Cyt1 and Cyt2 differ by 16 amino acids and exert opposing effects on the mammary epithelium in vivo. Mol. Cell. Biol. 2009, 29:4935-4948.
57. Ritzkat A., Pringa E., Scapin C., Guengoeze O., Dere M., Volpe M.V., Dammann C.E.L., Nielsen H.C. Knock-down of presenilin-1 blocks ErbB4-regulated surfactant synthesis in MLE-12 cells. E-PAS 2010, 3701.21.