From Neural Crest Development to Cancer and Vice Versa: How p75NTR and (Pro)neurotrophins Could Act on Cell Migration and Invasion?

Wislet, Sabine; Vandervelden, Geoffrey; Rogister, Bernard

doi:10.3389/fnmol.2018.00244

Article (Scientific journals)

From Neural Crest Development to Cancer and Vice Versa: How p75NTR and (Pro)neurotrophins Could Act on Cell Migration and Invasion?

Wislet, Sabine; Vandervelden, Geoffrey; Rogister, Bernard

2018 • In Frontiers in Molecular Neuroscience, 11

Peer Reviewed verified by ORBi

Permalink
https://hdl.handle.net/2268/232952

DOI
10.3389/fnmol.2018.00244

PubMed
30190671

Files (1)Send to Details Statistics Bibliography Similar publications

Files

Full Text

Frontiers P75 2018.pdf

Publisher postprint (1.25 MB)

Download

All documents in ORBi are protected by a user license.

Send to

RIS BibTex APA Chicago Permalink X Linkedin

Details

Keywords :

Cadherin; Ephrin; Invasion; Kidins220; Migration; Neurotrophin; P75NTR

Abstract :

[en] The p75 neurotrophin receptor (p75NTR), also known as low-affinity nerve growth factor, belongs to the tumor necrosis factor family of receptors. p75NTR is widely expressed in the nervous system during the development, as well as, in the neural crest population, since p75NTR has been described as ubiquitously expressed and considered as a neural crest marker. Neural crest cells (NCCs) constitute an transient population accurately migrating and invading, with precision, defined sites of the embryo. During migration, NCCs are guided along distinct migratory pathways by specialized molecules present in the extracellular matrix or on the surfaces of those cells. Two main processes direct NCC migration during the development: (1) an epithelial-to-mesenchymal transition and (2) a process known as contact inhibition of locomotion. In adults, p75NTR remains expressed by NCCs and has been identified in an increasing number of cancer cells. Nonetheless, the regulation of the expression of p75NTR and the underlying mechanisms in stem cell biology or cancer cells have not yet been sufficiently addressed. The main objective of this review is therefore to analyze elements of our actual knowledge regarding p75NTR roles during the development (mainly focusing on neural crest development) and see how we can transpose that information from development to cancer (and vice versa) to better understand the link between p75NTR and cell migration and invasion. In this review, we successively analyzed the molecular mechanisms of p75NTR when it interacts with several coreceptors and/or effectors. We then analyzed which signaling pathways are the most activated or linked to NCC migration during the development. Regarding cancer, we analyzed the described molecular pathways underlying cancer cell migration when p75NTR was correlated to cancer cell migration and invasion. From those diverse sources of information, we finally summarized potential molecular mechanisms underlying p75NTR activation in cell migration and invasion that could lead to new research areas to develop new therapeutic protocols. © 2018 Wislet, Vandervelden and Rogister.

Disciplines :

Biochemistry, biophysics & molecular biology

Author, co-author :

Wislet, Sabine ; Université de Liège - ULiège > Département des sciences biomédicales et précliniques > Biochimie et physiologie générales, et biochimie humaine

Vandervelden, Geoffrey ; Université de Liège - ULiège > Département des sciences biomédicales et précliniques > Biochimie et physiologie générales, et biochimie humaine

Rogister, Bernard ; Université de Liège - ULiège > Département des sciences biomédicales et précliniques > Biochimie et physiologie générales, et biochimie humaine

Language :

English

Title :

From Neural Crest Development to Cancer and Vice Versa: How p75NTR and (Pro)neurotrophins Could Act on Cell Migration and Invasion?

Publication date :

June 2018

Journal title :

Frontiers in Molecular Neuroscience

eISSN :

1662-5099

Publisher :

Frontiers Media S.A.

Volume :

Peer reviewed :

Peer Reviewed verified by ORBi

Available on ORBi :

since 15 February 2019

Statistics

Number of views

88 (7 by ULiège)

Number of downloads

86 (1 by ULiège)

More statistics

Scopus citations^®

Scopus citations^®
without self-citations

OpenCitations

Bibliography

Ahn B. Y., Saldanha-Gama R. F. G., Rahn J. J., Hao X., Zhang J., Dang N. H., (2016). Glioma invasion mediated by the p75 neurotrophin receptor (p75NTR/CD271) requires regulated interaction with PDLIM1. Oncogene 35 1411–1422. 10.1038/onc.2015.199 26119933.
Aloe L., (2004). Rita Levi-Montalcini: the discovery of nerve growth factor and modern neurobiology. Trends Cell Biol. 14 395–399. 10.1016/j.tcb.2004.05.011 15246433.
Alshehri M. M., Robbins S. M., Senger D. L., (2017). The role of neurotrophin signaling in gliomagenesis: a focus on the p75 neurotrophin receptor (p75NTR/CD271). Vitam. Horm. 104 367–404. 10.1016/bs.vh.2016.11.001 28215302.
Atapattu L., Lackmann M., Janes P. W., (2014). The role of proteases in regulating Eph/ephrin signaling. Cell Adh. Migr. 8 294–307. 10.4161/19336918.2014.970026 25482632.
Baker R. K., Antin P. B., (2003). Ephs and ephrins during early stages of chick embryogenesis. Dev. Dyn. 228 128–142. 10.1002/dvdy.10354 12950087.
Baldwin A. N., Bitler C. M., Welcher A. A., Shooter E. M., (1992). Studies on the structure and binding properties of the cysteine-rich domain of rat low affinity nerve growth factor receptor (p75NGFR). J. Biol. Chem. 267 8352–8359. 1373724.
Bapat A. A., Munoz R. M., Von Hoff D. D., Han H., (2016). Blocking nerve growth factor signaling reduces the neural invasion potential of pancreatic cancer cells. PLoS One 11:e0165586. 10.1371/journal.pone.0165586 27792755.
Barde Y. A., Edgar D., Thoenen H., (1982). Purification of a new neurotrophic factor from mammalian brain. EMBO J. 1 549–553.
Becker S. F. S., Mayor R., Kashef J., (2013). Cadherin-11 mediates contact inhibition of locomotion during Xenopus neural crest cell migration. PLoS One 8:e85717. 10.1371/journal.pone.0085717 24392028.
Bentley C. A., Lee K.-F., (2000). p75 is important for axon growth and schwann cell migration during development. J. Neurosci. 20 7706–7715. 10.1523/JNEUROSCI.20-20-07706.2000 11027232.
Berghoff J., Jaisimha A. V., Duggan S., MacSharry J., McCarthy J. V., (2015). Gamma-secretase-independent role for cadherin-11 in neurotrophin receptor p75 (p75NTR) mediated glioblastoma cell migration. Mol. Cell. Neurosci. 69 41–53. 10.1016/j.mcn.2015.10.003 26476273.
Birtolo C., Pham H., Morvaridi S., Chheda C., Go V. L. W., Ptasznik A., (2017). Cadherin-11 is a cell surface marker up-regulated in activated pancreatic stellate cells and is involved in pancreatic cancer cell migration. Am. J. Pathol. 187 146–155. 10.1016/j.ajpath.2016.09.012 27855278.
Bogenmann E., Thomas P. S., Li Q., Kim J., Yang L.-T., Pierchala B., (2011). Generation of mice with a conditional allele for the p75(NTR) neurotrophin receptor gene. Genesis 49 862–869. 10.1002/dvg.20747 21413144.
Bong Y.-S., Lee H.-S., Carim-Todd L., Mood K., Nishanian T. G., Tessarollo L., (2007). ephrinB1 signals from the cell surface to the nucleus by recruitment of STAT3. Proc. Natl. Acad. Sci. U.S.A. 104 17305–17310. 10.1073/pnas.0702337104 17954917.
Cai D., Chen S.-C., Prasad M., He L., Wang X., Choesmel-Cadamuro V., (2014). Mechanical feedback through E-cadherin promotes direction sensing during collective cell migration. Cell 157 1146–1159. 10.1016/j.cell.2014.03.045 24855950.
Cai S., Cai J., Jiang W., Ye L., (2017). Kidins220 and tumor development: insights into a complexity of cross-talk among signalling pathways (Review). Int. J. Mol. Med. 40 965–971. 10.3892/ijmm.2017.3093 28849114.
Cao H. H., Chu J. H., Kwan H. Y., Su T., Yu H., Cheng C. Y., (2016). Inhibition of the STAT3 signaling pathway contributes to apigenin-mediated anti-metastatic effect in melanoma. Sci. Rep. 6:21731. 10.1038/srep21731 26911838.
Chang M. S., Arevalo J. C., Chao M. V., (2004). Ternary complex with Trk, p75, and an ankyrin-rich membrane spanning protein. J. Neurosci. Res. 78 186–192. 10.1002/jnr.20262 15378608.
Chiaretti A., Aloe L., Antonelli A., Ruggiero A., Piastra M., Riccardi R., (2004). Intraventricular nerve growth factor infusion improves cerebral blood flow and stimulates doublecortin expression in two infants with hypoxic-ischemic brain injury. Childs Nerv. Syst. 20:412. 10.1179/016164107X247948 18282376.
Cho M. S., Rupaimoole R., Choi H.-J., Noh K., Chen J., Hu Q., (2016). Complement component 3 is regulated by TWIST1 and mediates epithelial–mesenchymal transition. J. Immunol. 196 1412–1418. 10.4049/jimmunol.1501886 26718342.
Chopin V., Lagadec C., Toillon R., Le Bourhis X., (2016). Neurotrophin signaling in cancer stem cells. Cell. Mol. Life Sci. 73 1859–1870. 10.1007/s00018-016-2156-7 26883804.
Clay M. R., Halloran M. C., (2014). Cadherin 6 promotes neural crest cell detachment via F-actin regulation and influences active Rho distribution during epithelial-to-mesenchymal transition. Development 141 2506–2515. 10.1242/dev.105551 24917505.
Coste C., Neirinckx V., Gothot A., Wislet S., Rogister B., (2015). Are neural crest stem cells the missing link between hematopoietic and neurogenic niches? Front. Cell Neurosci. 9:218. 10.3389/fncel.2015.00218 26136659.
De la Cruz-Morcillo M. A., Berger J., Sánchez-Prieto R., Saada S., Naves T., Guillaudeau A., (2016). p75 neurotrophin receptor and pro-BDNF promote cell survival and migration in clear cell renal cell carcinoma. Oncotarget 5 34480–34497. 10.18632/oncotarget.8911 27120782.
Faulkner S., Jobling P., Rowe C. W., Rodrigues Oliveira S. M., Roselli S., Thorne R. F., (2018). Neurotrophin Receptors TrkA, p75NTR, and Sortilin Are Increased and Targetable in Thyroid Cancer. Am. J. Pathol. 188 229–241. 10.1016/j.ajpath.2017.09.008 29037860.
Firulli A. B., Conway S. J., (2008). Phosphoregulation of Twist1 provides a mechanism of cell fate control. Curr. Med. Chem. 15 2641–2647. 10.2174/092986708785908987 18855684.
Forsyth P. A., Krishna N., Lawn S., Valadez J. G., Qu X., Fenstermacher D. A., (2014). P75 neurotrophin receptor cleavage by A- and Γ-secretases is required for neurotrophin-mediated proliferation of brain tumor-initiating cells. J. Biol. Chem. 289 8067–8085. 10.1074/jbc.M113.513762 24519935.
Frisch S. M., Schaller M., Cieply B., (2013). Mechanisms that link the oncogenic epithelial–mesenchymal transition to suppression of anoikis. J. Cell Sci. 126 21–29. 10.1242/jcs.120907 23516327.
Fujita K., Ogawa R., Ito K., (2016). CHD7, Oct3/4, Sox2, and Nanog control FoxD3 expression during mouse neural crest-derived stem cell formation. FEBS J. 283 3791–3806. 10.1111/febs.13843 27579714.
Garcia-Garcia A., de Castillejo C. L. F., Mendez-Ferrer S., (2015). BMSCs and hematopoiesis. Immunol. Lett. 168 129–135. 10.1016/j.imlet.2015.06.020 26192443.
Gaultier A., Cousin H., Darribère T., Alfandari D., (2002). ADAM13 disintegrin and cysteine-rich domains bind to the second heparin-binding domain of fibronectin. J. Biol. Chem. 277 23336–23344. 10.1074/jbc.M201792200 11967265.
Glejzer A., Neirinckx V., Rogister B., Wislet-Gendebien S., (2011). “Neural crest stem cells from adult bone marrow: a new source for cell replacement therapy?” in Advances in Regenerative Medicine, ed. Wislet-Gendebien S., InTech: London. Available at: https://www.intechopen.com/books/advances-in-regenerative-medicine/neural-crest-stem-cells-from-adult-bone-marrow-a-new-source-for-cell-replacement-therapy.
Gomez D. R., Byers L. A., Nilsson M., Diao L., Wang J., Li L., (2018). Integrative proteomic and transcriptomic analysis provides evidence for TrkB (NTRK2) as a therapeutic target in combination with tyrosine kinase inhibitors for non-small cell lung cancer. Oncotarget 9 14268–14284. 10.18632/oncotarget.24361 29581842.
He J. Y., Han P., Zhang Y., Song S. J., Feng G. K., An Y., (2018). Overexpression of Nogo receptor 3 (NgR3) correlates with poor prognosis and contributes to the migration of epithelial cells of nasopharyngeal carcinoma patients. J. Mol. Med. 96 265–279. 10.1007/s00109-017-1618-1 29327067.
He X. L., Bazan J. F., McDermott G., Park J. B., Wang K., Tessier-Lavigne M., (2003). Structure of the Nogo receptor ectodomain: a recognition module implicated in myelin inhibition. Neuron 38 177–185. 10.1016/S0896-6273(03)00232-0.
Heuer J. G., Fatemie-Nainie S., Wheeler E. F., Bothwell M., (1990). Structure and developmental expression of the chicken NGF receptor. Dev. Biol. 137 287–304. 10.1016/0012-1606(90)90255-H.
Hua Z., Gu X., Dong Y., Tan F., Liu Z., Thiele C. J., (2016). PI3K and MAPK pathways mediate the BDNF/TrkB-increased metastasis in neuroblastoma. Tumor Biol. 37 16227–16236. 10.1007/s13277-016-5433-z 27752996.
Huang E. J., Reichardt L. F., (2001). Neurotrophins: roles in neuronal development and function. Annu. Rev. Neurosci. 24 677–736. 10.1146/annurev.neuro.24.1.677.
Ip N. Y., Ibáñez C. F., Nye S. H., McClain J., Jones P. F., Gies D. R., (1992). Mammalian neurotrophin-4: structure, chromosomal localization, tissue distribution, and receptor specificity. Proc. Natl. Acad. Sci. U.S.A. 89 3060–3064. 10.1073/pnas.89.7.3060 1313578.
Ivanov S. V., Panaccione A., Brown B., Guo Y., Moskaluk C. A., Wick M. J., (2013). TrkC signaling is activated in adenoid cystic carcinoma and requires NT-3 to stimulate invasive behavior. Oncogene 32 3698–3710. 10.1038/onc.2012.377 23027130.
Jia S., Wang W., Hu Z., Shan C., Wang L., Wu B., (2015). BDNF mediated TrkB activation contributes to the EMT progression and the poor prognosis in human salivary adenoid cystic carcinoma. Oral Oncol. 51 64–70. 10.1016/j.oraloncology.2014.10.008. 25456007.
Jiang L., Wang Z., Liu C., Gong Z., Yang Y., Kang H., (2017). TrkB promotes laryngeal cancer metastasis via activation PI3K/AKT pathway. Oncotarget 8 108726–108737. 10.18632/oncotarget.21711 29312563.
Jiang X., Rowitch D. H., Soriano P., McMahon A. P., Sucov H. M., (2000). Fate of the mammalian cardiac neural crest. Development 127 1607–1616. 10.1038/ncb3294 26693916.
Jin H., Pan Y., He L., Zhai H., Li X., Zhao L., (2007). p75 neurotrophin receptor inhibits invasion and metastasis of gastric cancer. Mol. Cancer Res. 5 423–433. 10.1158/1541-7786.MCR-06-0407 17510309.
Jin S. G., Ryu H. H., Li S. Y., Li C. H., Lim S. H., Jang W. Y., (2016). Nogo-A inhibits the migration and invasion of human malignant glioma U87MG cells. Oncol. Rep. 35 3395–3402. 10.3892/or.2016.4737 27109183.
Kanda M., Kodera Y., (2016). Molecular mechanisms of peritoneal dissemination in gastric cancer. World J. Gastroenterol. 22 6829–6840. 10.3748/wjg.v22.i30.6829 27570420.
Ke H., Zhao L., Zhang H., Feng X., Xu H., Hao J., (2018). Loss of TDP43 inhibits progression of triple-negative breast cancer in coordination with SRSF3. Proc. Natl. Acad. Sci. U.S.A. 115 E3426–E3435. 10.1073/pnas.1714573115 29581274.
Khan M. A., Chen H. C., Zhang D., Fu J., (2013). Twist: a molecular target in cancer therapeutics. Tumour Biol. 34 2497–2506. 10.1007/s13277-013-1002-x 23873099.
Kim N.-H., Choi S.-H., Lee T. R., Lee C.-H., Lee A.-Y., (2014). Cadherin 11, a miR-675 target, induces N-Cadherin expression and epithelial-Mesenchymal transition in Melasma. J. Invest. Dermatol. 134 2967–2976. 10.1038/jid.2014.257 24940649.
Kong H., Boulter J., Weber J. L., Lai C., Chao M. V., (2001). An evolutionarily conserved transmembrane protein that is a novel downstream target of neurotrophin and ephrin receptors. J. Neurosci. 21 176–185. 10.1523/JNEUROSCI.21-01-00176.2001 11150334.
Kumar S., Park S. H., Cieply B., Schupp J., Killiam E., Zhang F., (2011). A Pathway for the Control of Anoikis Sensitivity by E-Cadherin and Epithelial-to-Mesenchymal Transition. Mol. Cell. Biol. 31 4036–4051. 10.1128/MCB.01342-10 21746881.
Kupferman M., Jiffar T., El-Naggar A., Yilmaz T., Zhou G., Xie T., (2010). TrkB induces EMT and has a key role in invasion of head and neck squamous cell carcinoma. Oncogene 29 2047–2059. 10.1038/onc.2009.486 20101235.
Lagadec C., Meignan S., Adriaenssens E., Foveau B., Vanhecke E., Romon R., (2009). TrkA overexpression enhances growth and metastasis of breast cancer cells. Oncogene 28 1960–1970. 10.1038/onc.2009.61 19330021.
Lee R., Kermani P., Teng K. K., Hempstead B. L., (2001). Regulation of cell survival by secreted proneurotrophins. Science 294 1945–1948. 10.1126/science.1065057 11729324.
Li Y., Guo Z., Chen H., Dong Z., Pan Z. K., Ding H., (2011). HOXC8-dependent cadherin 11 expression facilitates breast cancer cell migration through trio and rac. Genes Cancer 2 880–888. 10.1177/1947601911433129 22593800.
Li Z., Takenobu H., Setyawati A. N., Akita N., Haruta M., Satoh S., (2018). EZH2 regulates neuroblastoma cell differentiation via NTRK1 promoter epigenetic modifications. Oncogene 37 2714–2727. 10.1038/s41388-018-0133-3 29507419.
Liao Y. H., Hsu S. M., Yang H. L., Tsai M. S., Huang P. H., (2011). Upregulated ankyrin repeat-rich membrane spanning protein contributes to tumour progression in cutaneous melanoma. Br. J. Cancer 104 982–988. 10.1038/bjc.2011.18 21343931.
Lin K. T., Sloniowski S., Ethell D. W., Ethell I. M., (2008). Ephrin-B2-induced cleavage of EphB2 receptor is mediated by matrix metalloproteinases to trigger cell repulsion. J. Biol. Chem. 283 28969–28979. 10.1074/jbc.M804401200 18713744.
Lin Z., Tann J. Y., Goh E. T. H., Kelly C., Lim K. B., Gao J. F., (2015). Structural basis of death domain signaling in the p75 neurotrophin receptor. eLife 4:e11692. 10.7554/eLife.11692 26646181.
Lombard A., Goffart N., Rogister B., (2015). Glioblastoma circulating cells: reality, trap or illusion? Stem Cells Int. 2015:182985. 10.1155/2015/182985 26078762.
Maisonpierre P. C., Le Beau M. M., Espinosa R., Ip N. Y., Belluscio L., de la Monte S. M., (1991). Human and rat brain-derived neurotrophic factor and neurotrophin-3: gene structures, distributions, and chromosomal localizations. Genomics 10 558–568. 10.1016/0888-7543(91)90436-I 1889806.
Marler K. J. M., Poopalasundaram S., Broom E. R., Wentzel C., Drescher U., (2010). Pro-neurotrophins secreted from retinal ganglion cell axons are necessary for ephrinA-p75 NTR -mediated axon guidance. Neural. Dev. 5:30. 10.1186/1749-8104-5-30 21044296.
Mathavan K., Khedgikar V., Bartolo V., Alfandari D., (2017). The ectodomain of cadherin-11 binds to erbB2 and stimulates Akt phosphorylation to promote cranial neural crest cell migration. PLoS One 12:e0188963. 10.1371/journal.pone.0188963 29190819.
Meeker R., Williams K., (2014). Dynamic nature of the p75 neurotrophin receptor in response to injury and disease. J. Neuroimmune Pharmacol. 9 615–628. 10.1007/s11481-014-9566-9 25239528.
Mochizuki M., Tamai K., Imai T., Sugawara S., Ogama N., Nakamura M., (2016). CD271 regulates the proliferation and motility of hypopharyngeal cancer cells. Sci. Rep. 6:30707. 10.1038/srep30707 27469492.
Molloy N. H., Read D. E., Gorman A. M., (2011). Nerve growth factor in cancer cell death and survival. Cancers 3 510–530. 10.3390/cancers3010510 24212627.
Moore R., Theveneau E., Pozzi S., Alexandre P., Richardson J., Merks A., (2013). Par3 controls neural crest migration by promoting microtubule catastrophe during contact inhibition of locomotion. Development 140 4763–4775. 10.1242/dev.098509 24173803.
Morrison J. A., Mclennan R., Wolfe L. A., Gogol M. M., Meier S., McKinney M. C., (2017). Single-cell transcriptome analysis of avian neural crest migration reveals signatures of invasion and molecular transitions. eLife 6:e28415. 10.7554/eLife.28415 29199959.
Nakada M., Anderson E. M., Demuth T., Nakada S., Reavie L. B., Drake K. L., (2010). The phosphorylation of ephrin-B2 ligand promotes glioma cell migration and invasion. Int. J. Cancer 126 1155–1165. 10.1002/ijc.24849 19728339.
Nakada M., Drake K. L., Nakada S., Niska J. A., Berens M. E., (2006). Ephrin-B3 ligand promotes glioma invasion through activation of Rac1. Cancer Res. 66 8492–8500. 10.1158/0008-5472.CAN-05-4211 16951161.
Nakamura H., Nagasaka K., Kawana K., Taguchi A., Uehara Y., Yoshida M., (2016). Expression of Par3 polarity protein correlates with poor prognosis in ovarian cancer. BMC Cancer 16:897. 10.1186/s12885-016-2929-2 27855669.
Neubrand V. E., Cesca F., Benfenati F., Schiavo G., (2012). Kidins220/ARMS as a functional mediator of multiple receptor signalling pathways. J. Cell Sci. 125 1845–1854. 10.1242/jcs.102764 22562556.
Nykjaer A., Willnow T. E., (2012). Sortilin: a receptor to regulate neuronal viability and function. Trends Neurosci. 35 261–270. 10.1016/j.tins.2012.01.003 22341525.
O’Leary D. D. M., Wilkinson D. G., (1999). Eph receptors and ephrins in neural development. Curr. Opin. Neurobiol. 9 65–73. 10.1016/S0959-4388(99)80008-7.
Pan W., Kremer K. L., Kaidonis X., Ludlow V. E., Rogers M. L., Xie J., (2016). Characterization of p75 neurotrophin receptor expression in human dental pulp stem cells. Int. J. Dev. Neurosci. 53 90–98. 10.1016/j.ijdevneu.2016.07.007 27469433.
Patel S. D., Chen C. P., Bahna F., Honig B., Shapiro L., (2003). Cadherin-mediated cell–cell adhesion: sticking together as a family. Curr. Opin. Struct. Biol. 13 690–698. 10.1016/j.sbi.2003.10.007.
Pegoraro C., Monsoro-Burq A. H., (2013). Signaling and transcriptional regulation in neural crest specification and migration: lessons from xenopus embryos. Wiley Interdiscip. Rev. Dev. Biol. 2 247–259. 10.1002/wdev.76 24009035.
Peschon J. J., Slack J. L., Reddy P., Stocking K. L., Sunnarborg S. W., Lee D. C., (1998). An essential role for ectodomain shedding in mammalian development. Science 282 1281–1284. 10.1126/science.282.5392.1281.
Pramanik S., Sulistio Y. A., Heese K., (2016). Neurotrophin signaling and stem cells - implications for neurodegenerative diseases and stem cell therapy. Mol. Neurobiol. 54 7401–7459. 10.1007/s12035-016-0214-7 27815842.
Prasad M. S., Paulson A. F., (2011). A combination of enhancer/silencer modules regulates spatially restricted expression of cadherin-7 in neural epithelium. Dev. Dyn. 240 1756–1768. 10.1002/dvdy.22675 21674686.
Raza M.-Z., Allegrini S., Dumontet C., Jordheim L. P., (2017). Functions of the multi-interacting protein KIDINS220/ARMS in cancer and other pathologies. Genes Chromosomes Cancer 57 114–122. 10.1002/gcc.22514 29181864.
Restivo G., Diener J., Cheng P. F., Kiowski G., Bonalli M., Biedermann T., (2017). The low affinity neurotrophin receptor CD271 regulates phenotype switching in melanoma. Nat. Commun. 8:1988. 10.1038/s41467-017-01573-6 29215016.
Ross A. H., Grob P., Bothwell M., Elder D. E., Ernst C. S., Marano N., (1984). Characterization of nerve growth factor receptor in neural crest tumors using monoclonal antibodies. Proc. Natl. Acad. Sci. U.S.A. 81 6681–6685. 10.1073/pnas.81.21.6681 6093111.
Roycroft A., Mayor R., (2016). Molecular basis of contact inhibition of locomotion. Cell. Mol. Life Sci. 73 1119–1130. 10.1007/s00018-015-2090-0 26585026.
Saha N., Kolev M., Nikolov D. B., (2014). Structural features of the Nogo receptor signaling complexes at the neuron/myelin interface. Neurosci. Res. 87 1–7. 10.1016/j.neures.2014.06.003 24956133.
Satcher R. L., Pan T., Bilen M. A., Li X., Lee Y.-C., Ortiz A., (2015). Cadherin-11 endocytosis through binding to clathrin promotes cadherin-11-mediated migration in prostate cancer cells. J. Cell Sci. 128 4629–4641. 10.1242/jcs.176081 26519476.
Schmieg N., Thomas C., Yabe A., Lynch D. S., Iglesias T., Chakravarty P., (2015). Novel Kidins220/ARMS splice isoforms: potential specific regulators of neuronal and cardiovascular development. PLoS One 10:e0129944. 10.1371/journal.pone.0129944 26083449.
Shelton E. L., Yutzey K. E., (2008). Twist1 function in endocardial cushion cell proliferation, migration, and differentiation during heart valve development. Dev. Biol. 317 282–295. 10.1016/j.ydbio.2008.02.037 18353304.
Shimizu D., Kanda M., Sugimoto H., Sueoka S., Takami H., Ezaka K., (2016). NRAGE promotes the malignant phenotype of hepatocellular carcinoma. Oncol. Lett. 11 1847–1854. 10.3892/ol.2016.4120 26998088.
Shonukan O., Bagayogo I., McCrea P., Chao M., Hempstead B., (2003). Neurotrophin-induced melanoma cell migration is mediated through the actin-bundling protein fascin. Oncogene 22 3616–3623. 10.1038/sj.onc.1206561 12789270.
Skeldal S., Matusica D., Nykjaer A., Coulson E. J., (2011). Proteolytic processing of the p75 neurotrophin receptor: a prerequisite for signalling?: neuronal life, growth and death signalling are crucially regulated by intra-membrane proteolysis and trafficking of p75NTR. Bioessays 33 614–625. 10.1002/bies.201100036 21717487.
Smeets B., Alert R., Pešek J., Pagonabarraga I., Ramon H., Vincent R., (2016). Emergent structures and dynamics of cell colonies by contact inhibition of locomotion. Proc. Natl. Acad. Sci. U.S.A. 113 14621–14626. 10.1073/pnas.1521151113 27930287.
Song H., Moon A., (2006). Glial cell-derived neurotrophic factor (GDNF) promotes low-grade Hs683 glioma cell migration through JNK, ERK-1/2 and p38 MAPK signaling pathways. Neurosci. Res. 56 29–38. 10.1016/j.neures.2006.04.019 16814421.
Steinle J. J., Meininger C. J., Forough R., Wu G., Wu M. H., Granger H. J., (2002). Eph B4 receptor signaling mediates endothelial cell migration and proliferation via the phosphatidyl- inositol 3-kinase pathway. J. Biol. Chem. 277 43830–43835. 10.1074/jbc.M207221200 12235151.
Suraneni M. V., Badeaux M. D., (2013). Tumor-Initiating Cells, Cancer Metastasis and Therapeutic Implications. Available at: https://www.ncbi.nlm.nih.gov/books/NBK169227/.
Sutter A., Riopelle R. J., Harris R. M., Warrick E. M., (1979). Shooter nerve growth factor receptors. characterization of two distinct classes of binding sites on chick embryo sensory ganglia cells. J. Biol. Chem. 254 5972–5982. 571871.
Tep C., Kim M. L., Opincariu L. I., Limpert A. S., Chan J. R., Appel B., (2012). Brain-derived neurotrophic factor (BDNF) induces polarized signaling of small GTPase (Rac1) protein at the onset of schwann cell myelination through partitioning-defective 3 (Par3) protein. J. Biol. Chem. 287 1600–1608. 10.1074/jbc.M111.312736 22128191.
Theveneau E., Mayor R., (2012). Neural crest delamination and migration: from epithelium-to-mesenchyme transition to collective cell migration. Dev. Biol. 366 34–54. 10.1016/j.ydbio.2011.12.041 22261150.
Truzzi F., Marconi A., Lotti R., Dallaglio K., French L. E., Hempstead B. L., (2008). Neurotrophins and their receptors stimulate melanoma cell proliferation and migration. J. Invest. Dermatol. 128 2031–2040. 10.1038/jid.2008.21 18305571.
Vega-Lopez G. A., Cerrizuela S., Aybar M. J., (2017). Trunk neural crest cells: formation, migration and beyond. Int. J. Dev. Biol. 61 5–15. 10.1387/ijdb.160408gv 28287247.
Vincentz J. W., Barnes R. M., Rodgers R., Firulli B. A., Conway S. J., Firulli A. B., (2008). An absence of Twist1 results in aberrant cardiac neural crest morphogenesis. Dev. Biol. 320 131–139. 10.1016/j.ydbio.2008.04.037 18539270.
Wang B., Fujisawa H., Zhuang L., Kondo S., Shivji G. M., Kim C. S., (1997). Depressed langerhans cell migration and reduced contact hypersensitivity response in mice lacking tnf receptor p75. J. Immunol. 159 6148–6155. 9550416.
Wang B., Lindley L. E., Fernandez-Vega V., Rieger M. E., Sims A. H., Briegel K. J., (2012). The T Box transcription factor TBX2 promotes epithelial-mesenchymal transition and invasion of normal and malignant breast epithelial cells. PLoS One 7:e41355. 10.1371/journal.pone.0041355 22844464.
Wang L., Rahn J. J., Lun X., Sun B., Kelly J. J. P., Weiss S., (2008). Gamma-Secretase represents a therapeutic target for the treatment of invasive glioma mediated by the p75 neurotrophin receptor. PLoS Biol. 6:e289. 10.1371/journal.pbio.0060289 19067488.
Wang T.-C., Luo S., Lin C.-L., Chang P.-J., Chen M.-F., (2015). Modulation of p75 neurotrophin receptor under hypoxic conditions induces migration and invasion of C6 glioma cells. Clin. Exp. Metastasis 32 73–81. 10.1007/s10585-014-9692-z 25527128.
Wei S., Xu G., Bridges L. C., Williams P., White J. M., DeSimone D. W., (2010). ADAM13 induces cranial neural crest by cleaving class b ephrins and regulating Wnt signaling. Dev. Cell 19 345–352. 10.1016/j.devcel.2010.07.012 20708595.
Wilson C. M., Naves T., Saada S., Pinet S., Vincent F., Lalloué F., (2014). The implications of sortilin/vps10p domain receptors in neurological and human diseases. CNS Neurol. Disord. Drug Targets 13 1354–1365. 10.2174/1871527313666141023151642 25345507.
Xi R., Pan S., Chen X., Hui B., Zhang L., Fu S., (2016). HPV16 E6-E7 induces cancer stem-like cells phenotypes in esophageal squamous cell carcinoma through the activation of PI3K/Akt signaling pathway in vitro and in vivo. Oncotarget 7 57050–57065. 10.18632/oncotarget.10959 27489353.
Xiong H., Nie X., Zou Y., Gong C., Li Y., Wu H., (2017). Twist1 enhances hypoxia induced radioresistance in cervical cancer cells by promoting nuclear EGFR localization. J. Cancer 8 345–353. 10.7150/jca.16607 28261334.
Xiong J., Zhou L., Yang M., Lim Y., Zhu Y. H., Fu D. L., (2013). ProBDNF and its receptors are upregulated in glioma and inhibit the growth of glioma cells in vitro. Neuro Oncol. 15 990–1007. 10.1093/neuonc/not039 23576602.
Yang N. Y., Pasquale E. B., Owen L. B., Ethell I. M., (2006). The EphB4 receptor-tyrosine kinase promotes the migration of melanoma cells through Rho-mediated actin cytoskeleton reorganization. J. Biol. Chem. 281 32574–32586. 10.1074/jbc.M604338200 16950769.
Yap A. S., Kovacs E. M., (2003). Direct cadherin-activated cell signaling. J. Cell Biol. 160 11–16. 10.1083/jcb.200208156 12507993.
Yuanlong H., Haifeng J., Xiaoyin Z., Jialin S., Jie L., Li Y., (2008). The inhibitory effect of p75 neurotrophin receptor on growth of human hepatocellular carcinoma cells. Cancer Lett. 268 110–119. 10.1016/j.canlet.2008.03.038 18462868.
Zanin J. P., Battiato N. L., Rovasio R. A., (2013). Neurotrophic factor NT-3 displays a non-canonical cell guidance signaling function for cephalic neural crest cells. Eur. J. Cell Biol. 92 264–279. 10.1016/j.ejcb.2013.10.006 24252516.
Zhang F., Yu J., Yang T., Xu D., Chi Z., Xia Y., (2016). A novel c-Jun N-terminal kinase (JNK) signaling complex involved in neuronal migration during brain development. J. Biol. Chem. 291 11466–11475. 10.1074/jbc.M116.716811 27026702.