nach oben

Cellular Oncology

Erschienen in:

26.03.2020 | Review

The role of ErbB4 in cancer

verfasst von: Vincent F.M. Segers, Lindsey Dugaucquier, Eline Feyen, Hadis Shakeri, Gilles W. De Keulenaer

Erschienen in: Cellular Oncology | Ausgabe 3/2020

Einloggen, um Zugang zu erhalten

Abstract

Background

The epidermal growth factor receptor family consists of four members, ErbB1 (epidermal growth factor receptor-1), ErbB2, ErbB3, and ErbB4, which all have been found to play important roles in tumor development. ErbB4 appears to be unique among these receptors, because it is the only member with growth inhibiting properties. ErbB4 plays well-defined roles in normal tissue development, in particular the heart, the nervous system, and the mammary gland system. In recent years, information on the role of ErbB4 in a number of tumors has emerged and its general direction points towards a tumor suppressor role for ErbB4. However, there are some controversies and conflicting data, warranting a review on this topic.

Conclusions

Here, we discuss the role of ErbB4 in normal physiology and in breast, lung, colorectal, gastric, pancreatic, prostate, bladder, and brain cancers, as well as in hepatocellular carcinoma, cholangiocarcinoma, and melanoma. Understanding the role of ErbB4 in cancer is not only important for the treatment of tumors, but also for the treatment of other disorders in which ErbB4 plays a major role, e.g. cardiovascular disease.

R.S. Muraoka-Cook, S.-M. Feng, K.E. Strunk, H.S. Earp 3rd, ErbB4/HER4: role in mammary gland development, differentiation and growth inhibition. J. Mammary Gland Biol. Neoplasia 13, 235–246 (2008)PubMedPubMedCentral

D.F. Stern, Tyrosine kinase signalling in breast cancer: ErbB family receptor tyrosine kinases. Breast Cancer Res. 2, 176–183 (2000)PubMedPubMedCentral

A. Gschwind, O.M. Fischer, A. Ullrich, The discovery of receptor tyrosine kinases: targets for cancer therapy. Nat. Rev. Cancer 4, 361 (2004)

N.E. Hynes, H.A. Lane, ERBB receptors and cancer: the complexity of targeted inhibitors. Nat. Rev. Cancer 5, 341 (2005)PubMed

Z. Vermeulen, V.F. Segers, G.W. De Keulenaer, ErbB2 signaling at the crossing between heart failure and cancer. Basic Res. Cardiol. 111, 60 (2016)PubMedPubMedCentral

D.M. Hyman, S.A. Piha-Paul, H. Won, J. Rodon, C. Saura, G.I. Shapiro, D. Juric, D.I. Quinn, V. Moreno, B. Doger, I.A. Mayer, V. Boni, E. Calvo, S. Loi, A.C. Lockhart, J.P. Erinjeri, M. Scaltriti, G.A. Ulaner, J. Patel, J. Tang, H. Beer, S.D. Selcuklu, A.J. Hanrahan, N. Bouvier, M. Melcer, R. Murali, A.M. Schram, L.M. Smyth, K. Jhaveri, B.T. Li, A. Drilon, J.J. Harding, G. Iyer, B.S. Taylor, M.F. Berger, R.E. Cutler Jr., F. Xu, A. Butturini, L.D. Eli, G. Mann, C. Farrell, A.S. Lalani, R.P. Bryce, C.L. Arteaga, F. Meric-Bernstam, J. Baselga, D.B. Solit, HER kinase inhibition in patients with HER2- and HER3-mutant cancers. Nature 554, 189 (2018)

A. Naresh, W. Long, G.A. Vidal, W.C. Wimley, L. Marrero, C.I. Sartor, S. Tovey, T.G. Cooke, J.M.S. Bartlett, F.E. Jones, The ERBB4/HER4 intracellular domain 4ICD is a BH3-only rotein promoting apoptosis of breast cancer cells. Cancer Res. 66, 6412–6420 (2006)

H. Tidcombe, A. Jackson-Fisher, K. Mathers, D.F. Stern, M. Gassmann, J.P. Golding, Neural and mammary gland defects in ErbB4 knockout mice genetically rescued from embryonic lethality. Proc. Natl. Acad. Sci. U. S. A. 100, 8281–8286 (2003)PubMedPubMedCentral

C.-P. Chuu, R.-Y. Chen, J.L. Barkinge, M.F. Ciaccio, R.B. Jones, Systems-level analysis of ErbB4 signaling in breast cancer: A laboratory to clinical perspective. Mol. Cancer Res. 6, 885–891 (2008)

10.

C. Deng, B. Pan, M. Engel, X.F. Huang, Neuregulin-1 signalling and antipsychotic treatment: potential therapeutic targets in a schizophrenia candidate signalling pathway. Psychopharmacology 226, 201–215 (2013)

11.

J. Schroeder, D. Lee, Dynamic expression and activation of ERBB receptors in the developing mouse mammary gland. Cell Growth Differ. 9, 451–464 (1998)PubMed

12.

F.E. Jones, T. Welte, X.Y. Fu, D.F. Stern, ErbB4 signaling in the mammary gland is required for lobuloalveolar development and Stat5 activation during lactation. J. Cell Biol. 147, 77–88 (1999)PubMedPubMedCentral

13.

W. Long, K.-U. Wagner, K.C.K. Lloyd, N. Binart, J.M. Shillingford, L. Hennighausen, F.E. Jones, Impaired differentiation and lactational failure of Erbb4-deficient mammary glands identify ERBB4 as an obligate mediator of STAT5. Developement 130, 5257–5268 (2003)

14.

V.F.M. Segers, D.L. Brutsaert, G.W. De Keulenaer, Cardiac remodeling: Endothelial cells have more to say than just NO. Front. Physiol. 9, 382 (2018)

15.

G.W. De Keulenaer, V.F.M. Segers, F. Zannad, D.L. Brutsaert, The future of pleiotropic therapy in heart failure. Lessons from the benefits of exercise training on endothelial function. Eur. J. Heart Fail. 19, 603–614 (2017)PubMed

16.

H. Shakeri, A.B. Gevaert, D.M. Schrijvers, G.R.Y. De Meyer, G.W. De Keulenaer, P.D.F. Guns, K. Lemmens, V.F. Segers, Neuregulin-1 attenuates stress-induced vascular senescence. Cardiovasc. Res. 114, 1041–1051 (2018)PubMed

17.

G.W. De Keulenaer, E. Feyen, L. Dugaucquier, H. Shakeri, A. Shchendrygina, Y.N. Belenkov, M. Brink, Z. Vermeulen, V.F.M. Segers, Mechanisms of the multitasking endothelial protein NRG-1 as a compensatory factor during chronic heart failure. Circ. Heart Fail. 12, e006288–e006288 (2019)

18.

G.W. De Keulenaer, K. Doggen, K. Lemmens, The vulnerability of the heart as a pluricellular paracrine organ: lessons from unexpected triggers of heart failure in targeted ErbB2 anticancer therapy. Circ. Res. 106, 35–46 (2010)PubMed

19.

K. Lemmens, K. Doggen, G.W. De Keulenaer, Role of neuregulin-1/ErbB signaling in cardiovascular physiology and disease: implications for therapy of heart failure. Circulation 116, 954–960 (2007)PubMed

20.

K. Lemmens, V.F. Segers, M. Demolder, M. Michiels, P. Van Cauwelaert, G.W. De Keulenaer, Endogenous inhibitors of hypertrophy in concentric versus eccentric hypertrophy. Eur. J. Heart Fail. 9, 352–356 (2007)PubMed

21.

C.L. Galindo, S. Ryzhov, D.B. Sawyer, Neuregulin as a heart failure therapy and mediator of reverse remodeling. Curr. Heart Fail. Rep. 11, 40–49 (2014)

22.

O. Odiete, M.F. Hill, D.B. Sawyer, Neuregulin in cardiovascular development and disease. Circ. Res. 111, 1376–1385 (2012)

23.

L. Vandekerckhove, Z. Vermeulen, Z.Z. Liu, S. Boimvaser, A. Patzak, V.F. Segers, G.W. De Keulenaer, Neuregulin-1 attenuates development of nephropathy in a type 1 diabetes mouse model with high cardiovascular risk. Am. J. Physiol. Endocrinol. Metab. 310, E495–E504 (2016)PubMedPubMedCentral

24.

Z. Vermeulen, A.S. Hervent, L. Dugaucquier, L. Vandekerckhove, M. Rombouts, M. Beyens, D.M. Schrijvers, G.R.Y. De Meyer, S. Maudsley, G.W. De Keulenaer, V.F. Segers, Inhibitory actions of the NRG-1/ErbB4 pathway in macrophages during tissue fibrosis in heart, skin and lung. Am. J. Physiol. Heart Circ. Physiol. 313, H934-H945 (2017)

25.

C.L. Galindo, E. Kasasbeh, A. Murphy, S. Ryzhov, S. Lenihan, F.A. Ahmad, P. Williams, A. Nunnally, J. Adcock, Y. Song, F.E. Harrell, T.L. Tran, T.J. Parry, J. Iaci, A. Ganguly, I. Feoktistov, M.K. Stephenson, A.O. Caggiano, D.B. Sawyer, J.H. Cleator, anti-remodeling and anti-fibrotic effects of the neuregulin-1β glial growth factor 2 in a large animal model of heart failure. J. Am. Heart Assoc. 3, e000773 (2014)

26.

K. Lemmens, V.F. Segers, M. Demolder, G.W. De Keulenaer, Role of neuregulin-1/ErbB2 signaling in endothelium-cardiomyocyte cross-talk. J. Biol. Chem. 281, 19469–19477 (2006)PubMed

27.

A. Thybusch-Bernhardt, S. Beckmann, H. Juhl, Comparative analysis of the EGF-receptor family in pancreatic cancer: expression of HER-4 correlates with a favourable tumor stage. Int. J. Surg. Investig. 2, 393–400 (2001)

28.

G.A. Vidal, D.E. Clark, L. Marrero, F.E. Jones, A constitutively active ERBB4/HER4 allele with enhanced transcriptional coactivation and cell-killing activities. Oncogene 26, 462–466 (2007)

29.

E.E. Williams, L.J. Trout, R.M. Gallo, S.E. Pitfield, I. Bryant, D.J. Penington, D.J. Riese 2nd, A constitutively active ErbB4 mutant inhibits drug-resistant colony formation by the DU-145 and PC-3 human prostate tumor cell lines. Cancer Lett. 192, 67–74 (2003)PubMed

30.

C. Bianco, S. Kannan, M. De Santis, M. Seno, C.K. Tang, I. Martinez-Lacaci, N. Kim, B. Wallace-Jones, M.E. Lippman, A.D. Ebert, C. Wechselberger, D.S. Salomon, Cripto-1 indirectly stimulates the tyrosine phosphorylation of erbB-4 through a novel receptor. J. Biol. Chem. 274, 8624–8629 (1999)

31.

T. Uchida, K. Wada, T. Akamatsu, M. Yonezawa, H. Noguchi, A. Mizoguchi, M. Kasuga, C. Sakamoto, A novel epidermal growth factor-like molecule containing two follistatin modules stimulates tyrosine phosphorylation of erbB-4 in MKN28 gastric cancer cells. Biochem. Biophys. Res. Commun. 266, 593–602 (1999)

32.

S.M. Jay, E. Kurtagic, L.M. Alvarez, S. de Picciotto, E. Sanchez, J.F. Hawkins, R.N. Prince, Y. Guerrero, C.L. Treasure, R.T. Lee, L.G. Griffith, Engineered bivalent ligands to bias ErbB receptor-mediated signaling and phenotypes. J. Biol. Chem. 286, 27729–27740 (2011)PubMedPubMedCentral

33.

Y. Sato, M. Yashiro, N. Takakura, Heregulin induces resistance to lapatinib-mediated growth inhibition of HER2-amplified cancer cells. Cancer Sci. 104, 1618–1625 (2013)PubMed

34.

J.M. Daly, C.B. Jannot, R.R. Beerli, D. Graus-Porta, F.G. Maurer, N.E. Hynes, Neu differentiation factor induces ErbB2 down-regulation and apoptosis of ErbB2-overexpressing breast tumor cells. Cancer Res. 57, 3804–3811 (1997)PubMed

35.

R. Gilbertson, R. Hernan, T. Pietsch, L. Pinto, P. Scotting, R. Allibone, D. Ellison, R. Perry, A. Pearson, J. Lunec, Novel ERBB4 juxtamembrane splice variants are frequently expressed in childhood medulloblastoma. Genes Chromosom. Cancer 31, 288–294 (2001)PubMed

36.

V. Kainulainen, M. Sundvall, J.A. Määttä, E. Santiestevan, M. Klagsbrun, K. Elenius, A natural ErbB4 isoform that does not activate phosphoinositide 3-kinase mediates proliferation but not survival or chemotaxis. J. Biol. Chem. 275, 8641–8649 (2000)PubMed

37.

C. Rio, J.D. Buxbaum, J.J. Peschon, G. Corfas, Tumor necrosis factor-α-converting enzyme is required for cleavage of erbB4/HER4. J. Biol. Chem. 275, 10379–10387 (2000)PubMed

38.

M. Vecchi, L.A. Rudolph-Owen, C.L. Brown, P.J. Dempsey, G. Carpenter, Tyrosine phosphorylation and proteolysis: Pervanadate-induced, metalloprotease-dependent cleavage of the ErbB-4 receptor and amohiregulin. J. Biol. Chem. 273, 20589–20595 (1998)

39.

M. Sundvall, K. Iljin, S. Kilpinen, H. Sara, O.P. Kallioniemi, K. Elenius, Role of ErbB4 in breast cancer. J. Mammary Gland Biol. Neoplasia 13, 259–268 (2008)PubMed

40.

A.J. Lodge, J.J. Anderson, W.J. Gullick, B. Haugk, R.C.F. Leonard, B. Angus, Type 1 growth factor receptor expression in node positive breast cancer: adverse prognostic significance of c-erbB-4. J. Clin. Pathol. 56, 300–304 (2003)PubMedPubMedCentral

41.

A.K. Wege, D. Chittka, S. Buchholz, M. Klinkhammer-Schalke, S. Diermeier-Daucher, F. Zeman, O. Ortmann, G. Brockhoff, HER4 expression in estrogen receptor-positive breast cancer is associated with decreased sensitivity to tamoxifen treatment and reduced overall survival of postmenopausal women. Breast Cancer Res. 20, 139–139 (2018)PubMedPubMedCentral

42.

J.Y. Kim, H.H. Jung, I.G. Do, S. Bae, S.K. Lee, S.W. Kim, J.E. Lee, S.J. Nam, J.S. Ahn, Y.H. Park, Y.H. Im, Prognostic value of ERBB4 expression in patients with triple negative breast cancer. BMC Cancer 16, 138 (2016)PubMedPubMedCentral

43.

R.S. Muraoka-Cook, M.A. Sandahl, K.E. Strunk, L.C. Miraglia, C. Husted, D.M. Hunter, K. Elenius, L.A. Chodosh, H.S. Earp 3rd, ErbB4 splice variants Cyt1 and Cyt2 differ by 16 amino acids and exert opposing effects on the mammary epithelium in vivo. Mol. Cell. Biol. 29, 4935–4948 (2009)PubMedPubMedCentral

44.

V.B. Wali, M. Gilmore-Hebert, R. Mamillapalli, J.W. Haskins, K.J. Kurppa, K. Elenius, C.J. Booth, D.F. Stern, Overexpression of ERBB4 JM-a CYT-1 and CYT-2 isoforms in transgenic mice reveals isoform-specific roles in mammary gland development and carcinogenesis. Breast Cancer Res. 16, 501 (2014)PubMedPubMedCentral

45.

J.A. Maatta, M. Sundvall, T.T. Junttila, L. Peri, V.J. Laine, J. Isola, M. Egeblad, K. Elenius, Proteolytic cleavage and phosphorylation of a tumor-associated ErbB4 isoform promote ligand-independent survival and cancer cell growth. Mol. Biol. Cell 17, 67–79 (2006)PubMedPubMedCentral

46.

C.K. Tang, X.Z. Concepcion, M. Milan, X. Gong, E. Montgomery, M.E. Lippman, Ribozyme-mediated down-regulation of ErbB-4 in estrogen receptor-positive breast cancer cells inhibits proliferation both in vitro and in vivo. Cancer Res. 59, 5315–5322 (1999)PubMed

47.

M. Munk, A. Memon, S.S. Poulsen, M. Borre, E. Nexo, B.S. Sorensen, The HER4 isoform JM-a/CYT2 relates to improved survival in bladder cancer patients but only if the estrogen receptor α is not expressed. Scand. J. Clin. Lab. Invest. 73, 503–513 (2013)PubMed

48.

R.M. Gallo, I. Bryant, R. Fry, E.E. Williams, D.J. Riese 2nd, Phosphorylation of ErbB4 on Tyr1056 is critical for inhibition of colony formation by prostate tumor cell lines. Biochem. Biophys. Res. Commun. 349, 372–382 (2006)PubMedPubMedCentral

49.

R. An, J. Feng, C. Xi, J. Xu, L. Sun, miR-146a attenuates sepsis-induced myocardial dysfunction by suppressing IRAK1 and TRAF6 via targeting ErbB4 expression. Oxidative Med. Cell. Longev., 2018, 7163057 (2018)

50.

G. Song, H. Zhang, C. Chen, L. Gong, B. Chen, S. Zhao, J. Shi, J. Xu, Z. Ye, miR-551b regulates epithelial-mesenchymal transition and metastasis of gastric cancer by inhibiting ERBB4 expression. Oncotarget 8, 45725-45735 (2017)PubMedPubMedCentral

51.

M. Zhang, L. Zhang, M. Cui, W. Ye, P. Zhang, S. Zhou, J. Wang, miR-302b inhibits cancer-related inflammation by targeting ERBB4, IRF2 and CXCR4 in esophageal cancer. Oncotarget 8, 49053–49063 (2017)PubMedPubMedCentral

52.

H. Liang, M. Liu, X. Yan, Y. Zhou, W. Wang, X. Wang, Z. Fu, N. Wang, S. Zhang, Y. Wang, K. Zen, C.-Y. Zhang, D. Hou, J. Li, X. Chen, miR-193a-3p functions as a tumor suppressor in lung cancer by down-regulating ERBB4. J. Biol. Chem. 290, 926–940 (2015)PubMed

53.

W.X. Schulze, L. Deng, M. Mann, Phosphotyrosine interactome of the ErbB-receptor kinase family. Mol. Syst. Biol. 1, 2005.0008–2005.0008 (2005)PubMedPubMedCentral

54.

A. Kaushansky, A. Gordus, B.A. Budnik, W.S. Lane, J. Rush, G. MacBeath, System-wide investigation of ErbB4 reveals 19 sites of Tyr phosphorylation that are unusually selective in their recruitment properties. Chem. Biol. 15, 808–817 (2008)PubMedPubMedCentral

55.

K. Ishibashi, Y. Fukumoto, H. Hasegawa, K. Abe, S. Kubota, K. Aoyama, S. Kubota, Y. Nakayama, N. Yamaguchi, Nuclear ErbB4 signaling through H3K9me3 is antagonized by EGFR-activated c-Src. J. Cell Sci. 126, 625–637 (2013)PubMed

56.

R. Roskoski, The ErbB/HER family of protein-tyrosine kinases and cancer. Pharmacol. Res. 79, 34–74 (2014)PubMed

57.

K. Elenius, C.J. Choi, S. Paul, E. Santiestevan, E. Nishi, M. Klagsbrun, Characterization of a naturally occurring ErbB4 isoform that does not bind or activate phosphatidyl inositol 3-kinase. Oncogene 18, 2607 (1999)PubMed

58.

A. Komuro, M. Nagai, N.E. Navin, M. Sudol, 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. 278, 33334–33341 (2003)PubMed

59.

R.I. Aqeilan, V. Donati, A. Palamarchuk, F. Trapasso, M. Kaou, Y. Pekarsky, M. Sudol, C.M. Croce, WW domain–containing proteins, WWOX and YAP, compete for interaction with ErbB-4 and modulate its transcriptional function. Cancer Res. 65, 6764–6772 (2005)

60.

R.I. Aqeilan, V. Donati, E. Gaudio, M.S. Nicoloso, M. Sundvall, A. Korhonen, J. Lundin, J. Isola, M. Sudol, H. Joensuu, C.M. Croce, K. Elenius, Association of Wwox with ErbB4 in breast cancer. Cancer Res. 67, 9330–9336 (2007)

61.

C.-Y. Ni, M.P. Murphy, T.E. Golde, G. Carpenter, γ-secretase cleavage and nuclear localization of ErbB-4 receptor tyrosine kinase. Science 294, 2179–2181 (2001)

62.

S.P. Sardi, J. Murtie, S. Koirala, B.A. Patten, G. Corfas, Presenilin-dependent ErbB4 nuclear signaling regulates the timing of astrogenesis in the developing brain. Cell 127, 185–197 (2006)

63.

B. Icli, A. Bharti, L. Pentassuglia, X. Peng, D.B. Sawyer, ErbB4 localization to cardiac myocyte nuclei, and its role in myocyte DNA damage response. Biochem. Biophys. Res. Commun. 418, 116–121 (2012)PubMedPubMedCentral

64.

S. Yamada, M. Marutsuka, M. Inoue, J. Zhang, S. Abe, K. Ishibashi, N. Yamaguchi, K. Eto, The interaction of the ErbB4 intracellular domain p80 with alpha-enolase in the nuclei is associated with the inhibition of the neuregulin1-dependent cell proliferation. Int. J. Biochem. Mol. Biol. 5, 21–29 (2014)

65.

K.E. Strunk, C. Husted, L.C. Miraglia, M. Sandahl, W.A. Rearick, D.M. Hunter, H.S. Earp 3rd, R.S. Muraoka-Cook, HER4 D-box sequences regulate mitotic progression and degradation of the nuclear HER4 cleavage product s80HER4. Cancer Res. 67, 6582–6590 (2007)PubMedPubMedCentral

66.

Y. Iwakura, H. Nawa, ErbB1-4-dependent EGF/neuregulin signals and their cross talk in the central nervous system: pathological implications in schizophrenia and Parkinson's disease. Front. Cell. Neurosci. 7, 4 (2013)PubMedPubMedCentral

67.

S.E. Telesco, R. Vadigepalli, R. Radhakrishnan, Molecular modeling of ErbB4/HER4 kinase in the context of the HER4 signaling network helps rationalize the effects of clinically identified HER4 somatic mutations on the cell phenotype. Biotechnol. J. 8, 1452–1464 (2013)PubMedPubMedCentral

68.

M. Rokavec, C. Justenhoven, W. Schroth, M.A. Istrate, S. Haas, H.-P. Fischer, C. Vollmert, T. Illig, U. Hamann, Y.-D. Ko, D. Glavač, H. Brauch, A novel polymorphism in the promoter region of ERBB4 is associated with breast and colorectal cancer risk. Clin. Cancer Res. 13, 7506–7514 (2007)

69.

H.C. Kim, J.Y. Lee, H. Sung, J.Y. Choi, S.K. Park, K.M. Lee, Y.J. Kim, M.J. Go, L. Li, Y.S. Cho, M. Park, D.J. Kim, J.H. Oh, J.W. Kim, J.P. Jeon, S.Y. Jeon, H. Min, H.M. Kim, J. Park, K.Y. Yoo, D.Y. Noh, S.H. Ahn, M.H. Lee, S.W. Kim, J.W. Lee, B.W. Park, W.Y. Park, E.H. Kim, M.K. Kim, W. Han, S.A. Lee, K. Matsuo, C.Y. Shen, P.E. Wu, C.N. Hsiung, J.Y. Lee, H.L. Kim, B.G. Han, D. Kang, A genome-wide association study identifies a breast cancer risk variant in ERBB4 at 2q34: results from the Seoul Breast Cancer Study. Breast Cancer Res. 14, R56 (2012)PubMedPubMedCentral

70.

M. Mansouri Bidkani, H. Tabatabaeian, S. Parsafar, N. Ghanei, M. Fazilati, K. Ghaedi, ErbB4 receptor polymorphism 2368A>C and risk of breast cancer. Breast 42, 157–163 (2018)

71.

K. Tomizawa, K. Suda, R. Onozato, H. Kuwano, Y. Yatabe, T. Mitsudomi, Analysis of ERBB4 mutations and expression in japanese patients with lung cancer. J. Thorac. Oncol. 5, 1859–1861 (2010)PubMed

72.

H. Sasaki, K. Okuda, O. Kawano, K. Endo, H. Yukiue, T. Yokoyama, M. Yano, Y. Fujii, ErbB4 expression and mutation in Japanese patients with lung cancer. Clin. Lung Cancer 8, 429–433 (2007)

73.

L. Ding, G. Getz, D.A. Wheeler, E.R. Mardis, M.D. McLellan, K. Cibulskis, C. Sougnez, H. Greulich, D.M. Muzny, M.B. Morgan, L. Fulton, R.S. Fulton, Q. Zhang, M.C. Wendl, M.S. Lawrence, D.E. Larson, K. Chen, D.J. Dooling, A. Sabo, A.C. Hawes, H. Shen, S.N. Jhangiani, L.R. Lewis, O. Hall, Y. Zhu, T. Mathew, Y. Ren, J. Yao, S.E. Scherer, K. Clerc, G.A. Metcalf, B. Ng, A. Milosavljevic, M.L. Gonzalez-Garay, J.R. Osborne, R. Meyer, X. Shi, Y. Tang, D.C. Koboldt, L. Lin, R. Abbott, T.L. Miner, C. Pohl, G. Fewell, C. Haipek, H. Schmidt, B.H. Dunford-Shore, A. Kraja, S.D. Crosby, C.S. Sawyer, T. Vickery, S. Sander, J. Robinson, W. Winckler, J. Baldwin, L.R. Chirieac, A. Dutt, T. Fennell, M. Hanna, B.E. Johnson, R.C. Onofrio, R.K. Thomas, G. Tonon, B.A. Weir, X. Zhao, L. Ziaugra, M.C. Zody, T. Giordano, M.B. Orringer, J.A. Roth, M.R. Spitz, I.I. Wistuba, B. Ozenberger, P.J. Good, A.C. Chang, D.G. Beer, M.A. Watson, M. Ladanyi, S. Broderick, A. Yoshizawa, W.D. Travis, W. Pao, M.A. Province, G.M. Weinstock, H.E. Varmus, S.B. Gabriel, E.S. Lander, R.A. Gibbs, M. Meyerson, R.K. Wilson, Somatic mutations affect key pathways in lung adenocarcinoma. Nature 455, 1069–1075 (2008)PubMedPubMedCentral

74.

K.J. Kurppa, K. Denessiouk, M.S. Johnson, K. Elenius, Activating ERBB4 mutations in non-small cell lung cancer. Oncogene 35, 1283–1291 (2016)

75.

Y. Zhang, L. Zhang, R. Li, D.W. Chang, Y. Ye, J.D. Minna, J.A. Roth, B. Han, X. Wu, Genetic variations in cancer-related significantly mutated genes and lung cancer susceptibility. Ann. Oncol. 28, 1625–1630 (2017)PubMedPubMedCentral

76.

N. Boku, HER2-positive gastric cancer. Gastric Cancer 17, 1–12 (2014)PubMed

77.

B.S. Jaiswal, N.M. Kljavin, E.W. Stawiski, E. Chan, C. Parikh, S. Durinck, S. Chaudhuri, K. Pujara, J. Guillory, K.A. Edgar, V. Janakiraman, R.P. Scholz, K.K. Bowman, M. Lorenzo, H. Li, J. Wu, W. Yuan, B.A. Peters, Z. Kan, J. Stinson, M. Mak, Z. Modrusan, C. Eigenbrot, R. Firestein, H.M. Stern, K. Rajalingam, G. Schaefer, M.A. Merchant, M.X. Sliwkowski, F.J. de Sauvage, S. Seshagiri, Oncogenic ERBB3 mutations in human cancers. Cancer Cell 23, 603–617 (2013)PubMed

78.

K. Chen, D. Yang, X. Li, B. Sun, F. Song, W. Cao, D.J. Brat, Z. Gao, H. Li, H. Liang, Y. Zhao, H. Zheng, M. Li, J. Buckner, S.D. Patterson, X. Ye, C. Reinhard, A. Bhathena, D. Joshi, P.S. Mischel, C.M. Croce, Y.M. Wang, S. Raghavakaimal, H. Li, X. Lu, Y. Pan, H. Chang, S. Ba, L. Luo, W.K. Cavenee, W. Zhang, X. Hao, Mutational landscape of gastric adenocarcinoma in Chinese: implications for prognosis and therapy. Proc. Natl. Acad. Sci. U. S. A. 112, 1107–1112 (2015)PubMedPubMedCentral

79.

R.S. Muraoka-Cook, L.S. Caskey, M.A. Sandahl, D.M. Hunter, C. Husted, K.E. Strunk, C.I. Sartor, W.A. Rearick Jr., W. McCall, M.K. Sgagias, K.H. Cowan, H.S. Earp 3rd, Heregulin-dependent delay in mitotic progression requires HER4 and BRCA1. Mol. Cell. Biol. 26, 6412–6424 (2006)PubMedPubMedCentral

80.

V.F. Segers, A.B. Gevaert, J.R. Boen, E.M. Van Craenenbroeck, G.W. De Keulenaer, Epigenetic regulation of intercellular communication in the heart. Am. J. Physiol. Heart Circ. Physiol. 316, H1417-H1425 (2019)

81.

P.M. Das, A.D. Thor, S.M. Edgerton, S.K. Barry, D.F. Chen, F.E. Jones, Reactivation of epigenetically silenced HER4/ERBB4 results in apoptosis of breast tumor cells. Oncogene 29, 5214–5219 (2010)PubMedPubMedCentral

82.

M.R. Frey, K.L. Edelblum, M.T. Mullane, D. Liang, D.B. Polk, The ErbB4 growth factor receptor is required for colon epithelial cell survival in the presence of TNF. Gastroenterology 136, 217–226 (2009)PubMed

83.

C.S. Williams, J.K. Bernard, M. Demory Beckler, D. Almohazey, M.K. Washington, J.J. Smith, M.R. Frey, ERBB4 is over-expressed in human colon cancer and enhances cellular transformation. Carcinogenesis 36, 710–718 (2015)PubMedPubMedCentral

84.

Y. Liu, L. Song, H. Ni, L. Sun, W. Jiao, L. Chen, Q. Zhou, T. Shen, H. Cui, T. Gao, J. Li, ERBB4 acts as a suppressor in the development of hepatocellular carcinoma. Carcinogenesis 38, 465–473 (2017)PubMed

85.

T.Y. Lee, K.T. Kim, S.Y. Han, Expression of ErbB receptor proteins and TGF-alpha during diethylnitrosamine-induced hepatocarcinogenesis in the rat liver. Korean J. Hepatol. 13, 70–80 (2007)

86.

J. Xu, L. Gong, Z. Qian, G. Song, J. Liu, ERBB4 promotes the proliferation of gastric cancer cells via the PI3K/Akt signaling pathway. Oncol. Rep. 39, 2892–2898 (2018)PubMed

87.

T.D. Prickett, N.S. Agrawal, X. Wei, K.E. Yates, J.C. Lin, J.R. Wunderlich, J.C. Cronin, P. Cruz, S.A. Rosenberg, Y. Samuels, Analysis of the tyrosine kinome in melanoma reveals recurrent mutations in ERBB4. Nat. Genet. 41, 1127–1132 (2009)PubMedPubMedCentral

88.

M.A. Schumacher, M. Hedl, C. Abraham, J.K. Bernard, P.R. Lozano, J.J. Hsieh, D. Almohazey, E.B. Bucar, S. Punit, P.J. Dempsey, M.R. Frey, ErbB4 signaling stimulates pro-inflammatory macrophage apoptosis and limits colonic inflammation. Cell Death Amp. Disease 8, e2622 (2017)

89.

B. de Unamuno Bustos, R. Murria Estal, G. Perez Simo, I. de Juan Jimenez, B. Escutia Munoz, M. Rodriguez Serna, V. Alegre de Miquel, M. Llavador Ros, R. Ballester Sanchez, E. Nagore Enguidanos, S. Palanca Suela, R. Botella Estrada, Towards personalized medicine in melanoma: Implementation of a clinical next-generation sequencing panel. Sci. Rep. 7, 495 (2017)

90.

Q.M. Zhou, W. Li, Y.X. Guan, X. Zhang, X.C. Chen, Y. Ding, X.Z. Wen, R.Q. Peng, S.M. Yan, X.S. Zhang, The absence of the ERBB4 hotspot mutations in melanomas in patients from southern China. Chin. J. Cancer 32, 410–414 (2013)

91.

A. Manca, A. Lissia, A. Cossu, C. Rubino, P.A. Ascierto, I. Stanganelli, G. Palmieri, Mutations in ERBB4 may have a minor role in melanoma pathogenesis. J. Invest. Dermatol. 133, 1685–1687 (2013)

92.

A. Pellat, J. Vaquero, L. Fouassier, Role of ErbB/HER family of receptor tyrosine kinases in cholangiocyte biology. Hepatology 67, 762–773 (2018)

93.

M. Hashemi, N. Moradi, M. Rezaei, S. Sanaei, S.A. Ziaee, B. Narouie, M. Sotoudeh, G. Bahari, S. Ghavami, ERBB4 gene polymorphisms and the risk of prostate cancer in a sample of Iranian Population. Cell. Mol. Biol. 62, 43–48 (2016)PubMed

94.

C. Lopez-Haber, L. Barrio-Real, V. Casado-Medrano, M.G. Kazanietz, Heregulin/ErbB3 signaling enhances CXCR4-driven Rac1 activation and breast cancer cell motility via hypoxia-inducible factor 1alpha. Mol. Cell. Biol. 36, 2011–2026 (2016)

95.

J. Wang, J. Yin, Q. Yang, F. Ding, X. Chen, B. Li, X. Tian, Human epidermal growth factor receptor 4 (HER4) is a favorable prognostic marker of breast cancer: a systematic review and meta-analysis. Oncotarget 7, 76693–76703 (2016)

96.

K. Mitsui, M. Yonezawa, A. Tatsuguchi, S. Shinji, K. Gudis, S. Tanaka, S. Fujimori, C. Sakamoto, Localization of phosphorylated ErbB1-4 and heregulin in colorectal cancer. BMC Cancer 14, 863–863 (2014)PubMedPubMedCentral

97.

G. Baiocchi, A. Lopes, R.A. Coudry, B.M. Rossi, F.A. Soares, S. Aguiar, G.C. Guimarães, F.O. Ferreira, W.T. Nakagawa, ErbB family immunohistochemical expression in colorectal cancer patients with higher risk of recurrence after radical surgery. Int. J. Color. Dis. 24, 1059 (2009)

98.

P. Kountourakis, K. Pavlakis, A. Psyrri, D. Rontogianni, N. Xiros, E. Patsouris, D. Pectasides, T. Economopoulos, Prognostic significance of HER3 and HER4 protein expression in colorectal adenocarcinomas. BMC Cancer 6, 46–46 (2006)PubMedPubMedCentral

99.

J.C. Lee, S.T. Wang, N.H. Chow, H.B. Yang, Investigation of the prognostic value of coexpressed erbB family members for the survival of colorectal cancer patients after curative surgery. Eur. J. Cancer 38, 1065–1071 (2002)PubMed

100.

I. Ljuslinder, B. Malmer, M. Isaksson-MettÄVainio, Å. ÖBerg, R. Henriksson, R. Stenling, R. Palmqvist, ErbB 1-4 expression alterations in primary colorectal cancers and their corresponding metastases. Anticancer Res. 29, 1489–1494 (2009)PubMed

101.

C.P. Mill, K.L. Gettinger, D.J. Riese 2nd, Ligand stimulation of ErbB4 and a constitutively-active ErbB4 mutant result in different biological responses in human pancreatic tumor cell lines. Exp. Cell Res. 317, 392–404 (2011)PubMed

102.

S. Gunes, Y. Sullu, Z. Yegin, R. Buyukalpelli, L. Tomak, H. Bagci, ErbB receptor tyrosine kinase family expression levels in urothelial bladder carcinoma. Pathol. Res. Pract. 209, 99–104 (2013)PubMed

103.

N.H. Chow, S.H. Chan, T.S. Tzai, C.L. Ho, H.S. Liu, Expression profiles of ErbB family receptors and prognosis in primary transitional cell carcinoma of the urinary bladder. Clin. Cancer Res. 7, 1957–1962 (2001)PubMed

104.

J.A. Forster, A.B. Paul, P. Harnden, M.A. Knowles, Expression of NRG1 and its receptors in human bladder cancer. Br. J. Cancer 104, 1135–1143 (2011)PubMedPubMedCentral

105.

W. Kassouf, P.C. Black, T. Tuziak, J. Bondaruk, S. Lee, G.A. Brown, L. Adam, C. Wei, K. Baggerly, M. Bar-Eli, D. McConkey, B. Czerniak, C.P. Dinney, Distinctive expression pattern of ErbB family receptors signifies an aggressive variant of bladder cancer. J. Urol. 179, 353–358 (2008)PubMed

106.

A.A. Memon, B.S. Sorensen, P. Melgard, L. Fokdal, T. Thykjaer, E. Nexo, Expression of HER3, HER4 and their ligand heregulin-4 is associated with better survival in bladder cancer patients. Br. J. Cancer 91, 2034–2041 (2004)PubMedPubMedCentral

107.

A.A. Memon, B.S. Sorensen, P. Meldgaard, L. Fokdal, T. Thykjaer, E. Nexo, The relation between survival and expression of HER1 and HER2 depends on the expression of HER3 and HER4: a study in bladder cancer patients. Br. J. Cancer 94, 1703–1709 (2006)PubMedPubMedCentral

108.

J.F. Donoghue, L.T. Kerr, N.W. Alexander, S.A. Greenall, A.B. Longano, N.G. Gottardo, R. Wang, V. Tabar, T.E. Adams, P.S. Mischel, T.G. Johns, Activation of ERBB4 in glioblastoma can contribute to increased tumorigenicity and influence therapeutic response. Cancers 10, pii: E243 (2018)

109.

D.C. Jones, A. Scanteianu, M. DiStefano, M. Bouhaddou, M.R. Birtwistle, Analysis of copy number loss of the ErbB4 receptor tyrosine kinase in glioblastoma. PLoS One 13, e0190664 (2018)PubMedPubMedCentral

110.

E. Tynyakov-Samra, E. Auriel, Y. Levy-Amir, A. Karni, Reduced ErbB4 expression in immune cells of patients with relapsing remitting multiple sclerosis. Mult. Scler. Int. 2011, 561262–561262 (2011)

111.

H. Kataria, A. Alizadeh, G.M. Shahriary, S. Saboktakin Rizi, R. Henrie, K.T. Santhosh, J.A. Thliveris, S. Karimi-Abdolrezaee, Neuregulin-1 promotes remyelination and fosters a pro-regenerative inflammatory response in focal demyelinating lesions of the spinal cord. Glia 66, 538–561 (2018)

112.

B.-R. Lee, B.-E. Kwon, E.-H. Hong, A. Shim, J.-H. Song, H.-M. Kim, S.-Y. Chang, Y.-J. Kim, M.-N. Kweon, J.-I. Youn, H.-J. Ko, Interleukin-10 attenuates tumour growth by inhibiting interleukin-6/signal transducer and activator of transcription 3 signalling in myeloid-derived suppressor cells. Cancer Lett. 381, 156–164 (2016)PubMed

113.

R. Iwamoto, N. Mine, H. Mizushima, E. Mekada, ErbB1 and ErbB4 generate opposing signals regulating mesenchymal cell proliferation during valvulogenesis. J. Cell Sci. 130, 1321–1332 (2017)PubMed

114.

S. Okazaki, F. Nakatani, K. Masuko, K. Tsuchihashi, S. Ueda, T. Masuko, H. Saya, O. Nagano, Development of an ErbB4 monoclonal antibody that blocks neuregulin-1-induced ErbB4 activation in cancer cells. Biochem. Biophys. Res. Commun. 470, 239–244 (2016)PubMed

115.

M. Hollmen, J.A. Maatta, L. Bald, M.X. Sliwkowski, K. Elenius, Suppression of breast cancer cell growth by a monoclonal antibody targeting cleavable ErbB4 isoforms. Oncogene 28, 1309–1319 (2009)

116.

I. Paatero, H. Lassus, T.T. Junttila, M. Kaskinen, R. Butzow, K. Elenius, CYT-1 isoform of ErbB4 is an independent prognostic factor in serous ovarian cancer and selectively promotes ovarian cancer cell growth in vitro. Gynecol. Oncol. 129, 179–187 (2013)PubMed

117.

F. Rauf, F. Festa, J.G. Park, M. Magee, S. Eaton, C. Rinaldi, C.M. Betanzos, L. Gonzalez-Malerva, J. LaBaer, Ibrutinib inhibition of ERBB4 reduces cell growth in a WNT5A-dependent manner. Oncogene 37, 2237–2250 (2018)PubMedPubMedCentral

Titel: The role of ErbB4 in cancer
verfasst von: Vincent F.M. Segers
Lindsey Dugaucquier
Eline Feyen
Hadis Shakeri
Gilles W. De Keulenaer
Publikationsdatum: 26.03.2020
Verlag: Springer Netherlands
Erschienen in: Cellular Oncology / Ausgabe 3/2020
Print ISSN: 2211-3428
Elektronische ISSN: 2211-3436
DOI: https://doi.org/10.1007/s13402-020-00499-4

Author Correction: The therapeutic potential of mesenchymal stem cells in lung cancer: benefits, risks and challenges

Author Correction

Salivary microRNAs identified by small RNA sequencing as potential predictors of response to intensity-modulated radiotherapy in head and neck cancer patients

Short Communication

CXCL-10: a new candidate for melanoma therapy?

Review

Long noncoding RNA LINC01234 silencing exerts an anti-oncogenic effect in esophageal cancer cells through microRNA-193a-5p-mediated CCNE1 downregulation

Original paper

Dp44mT, an iron chelator, suppresses growth and induces apoptosis via RORA-mediated NDRG2-IL6/JAK2/STAT3 signaling in glioma

Original paper

FAM83D promotes epithelial-mesenchymal transition, invasion and cisplatin resistance through regulating the AKT/mTOR pathway in non-small-cell lung cancer

Original paper

Neu im Fachgebiet Pathologie

DNA mixture deconvolution using fully continuous models EuroForMix and EFMrep

Open Access
Originalien

Mixture deconvolution is a powerful tool for inferring individual DNA profiles from DNA mixtures for subsequent transmission to a database or database queries. To carry out deconvolution, a mixed trace can be interpreted either manually by an …

Energie und Verletzungspotenzial von gezielt aus einem Fahrzeug abgeworfenen Steinen nach Durchschlag durch eine Pkw-Windschutzscheibe

Open Access
Schädelfrakturen
Originalie

Wir berichten aus Anlass eines Strafverfahrens über Versuche und deren biomechanische Bewertung hinsichtlich des möglichen Verletzungspotenzials von Steinen, welche vorsätzlich im Begegnungsverkehr auf entgegenkommende Fahrzeuge geworfen werden …

Durchführungsrealität der Komplexmethode zur Todeszeiteingrenzung an deutschen rechtsmedizinischen Instituten

Open Access
Rechtsmedizin
Originalie

Die Komplexmethode nach Henssge und Madea gilt als der Goldstandard für die Eingrenzung des Todeszeitintervalls im frühen postmortalen Intervall [ 1 , 2 ]. Der temperaturbasierte Methodenanteil gilt als gut etabliert [ 1 ]. Dies gilt nur mit …

Stellungnahme der Spurenkommission zu Ringversuchen zum Zweck der Qualitätssicherung in forensisch-molekulargenetischen Laboratorien

Open Access
Rechtsmedizin
Übersichtsartikel

Die Spurenkommission wurde in den 1980er-Jahren gegründet und bildet eine Arbeitsgruppe innerhalb der Deutschen Gesellschaft für Rechtsmedizin (DGRM). Zu den Kernaufgaben der Spurenkommission gehören das Verfassen von Empfehlungen für die …

Springer Medizin

The role of ErbB4 in cancer

Abstract

Background

Conclusions

Weitere Artikel der Ausgabe 3/2020

Author Correction: The therapeutic potential of mesenchymal stem cells in lung cancer: benefits, risks and challenges

Salivary microRNAs identified by small RNA sequencing as potential predictors of response to intensity-modulated radiotherapy in head and neck cancer patients

CXCL-10: a new candidate for melanoma therapy?

Long noncoding RNA LINC01234 silencing exerts an anti-oncogenic effect in esophageal cancer cells through microRNA-193a-5p-mediated CCNE1 downregulation

Dp44mT, an iron chelator, suppresses growth and induces apoptosis via RORA-mediated NDRG2-IL6/JAK2/STAT3 signaling in glioma

FAM83D promotes epithelial-mesenchymal transition, invasion and cisplatin resistance through regulating the AKT/mTOR pathway in non-small-cell lung cancer

Neu im Fachgebiet Pathologie

DNA mixture deconvolution using fully continuous models EuroForMix and EFMrep

Energie und Verletzungspotenzial von gezielt aus einem Fahrzeug abgeworfenen Steinen nach Durchschlag durch eine Pkw-Windschutzscheibe

Durchführungsrealität der Komplexmethode zur Todeszeiteingrenzung an deutschen rechtsmedizinischen Instituten

Stellungnahme der Spurenkommission zu Ringversuchen zum Zweck der Qualitätssicherung in forensisch-molekulargenetischen Laboratorien

Springer Medizin

Abstract

Background

Conclusions

Bitte loggen Sie sich ein, um Zugang zu diesem Inhalt zu erhalten