Skip to main content
SpringerLink
Log in

Breaching and Opening Basement Membrane Barriers: The Anchor Cell Leads the Way

  • Chapter
  • First Online:
Extracellular Matrix in Tumor Biology

Part of the book series: Biology of Extracellular Matrix ((BEM))

Abstract

Metastasis is initiated in epithelial-derived tumors when cells at the tumor front breach the epithelial basement membrane (BM). Invasion through BMs is thought to be one of the most rate-limiting steps in cancer progression and thus is a therapeutically attractive target for halting tumor spread. Despite intense interest, it has been challenging to experimentally determine how invasive cells breach and clear BM barriers, which has hindered efforts to block metastasis. Here we discuss how an experimentally tractable developmental invasion event, anchor cell (AC) invasion in the model system C. elegans, is offering powerful new insights into the fundamental mechanisms that invasive cells use to breach BM barriers and how cells at the breach site widen BM gaps through a new mechanism called BM sliding. Finally, we cover studies demonstrating that AC invasion can also be used as a new paradigm to examine how alterations in the tumor microenvironment impinge on cell invasive behavior.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Log in via an institution
Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 84.99
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 109.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 109.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

References

  • Abrams GA, Goodman SL, Nealey PF, Franco M, Murphy CJ (2000) Nanoscale topography of the basement membrane underlying the corneal epithelium of the rhesus macaque. Cell Tissue Res 299(1):39–46

    Article  CAS  PubMed  Google Scholar 

  • Abrams GA, Murphy CJ, Wang ZY, Nealey PF, Bjorling DE (2003) Ultrastructural basement membrane topography of the bladder epithelium. Urol Res 31(5):341–346. doi:10.1007/s00240-003-0347-9

    Article  PubMed  Google Scholar 

  • Aguilera KY, Rivera LB, Hur H, Carbon JG, Toombs JE, Goldstein CD, Dellinger MT, Castrillon DH, Brekken RA (2014) Collagen signaling enhances tumor progression after anti-VEGF therapy in a murine model of pancreatic ductal adenocarcinoma. Cancer Res 74(4):1032–1044. doi:10.1158/0008-5472.CAN-13-2800

    Article  CAS  PubMed  Google Scholar 

  • Akino T, Han X, Nakayama H, McNeish B, Zurakowski D, Mammoto A, Klaqsbrun M, Smith E (2014) Netrin-1 promotes medulloblastoma cell invasiveness and angiogenesis, and demonstrates elevated expression in tumor tissue and urine of patients with pediatric medulloblastoma. Cancer Res 74(14):3716–3726. doi:10.1158/0008-5472.CAN-13-3116

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Armenti ST, Lohmer LL, Sherwood DR, Nance J (2014) Repurposing an endogenous degradation system for rapid and targeted depletion of C. elegans proteins. Development 141(23):4640–4647. doi:10.1242/dev.115048

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Arnold SA, Brekken RA (2009) SPARC: a matricellular regulator of tumorigenesis. J Cell Commun Signal 3(3–4):255–273. doi:10.1007/s12079-009-0072-4

    Article  PubMed  PubMed Central  Google Scholar 

  • Artym VV, Matsumoto K, Mueller SC, Yamada KM (2011) Dynamic membrane remodeling at invadopodia differentiates invadopodia from podosomes. Eur J Cell Biol 90(2–3):172–180. doi:10.1016/j.ejcb.2010.06.006

    Article  CAS  PubMed  Google Scholar 

  • Baluk P, Fuxe J, Hashizume H, Romano T, Lashnits E, Butz S, Vestweber D, Corada M, Molendini C, Dejana E, McDonald DM (2007) Functionally specialized junctions between endothelial cells of lymphatic vessels. J Exp Med 204(10):2349–2362. doi:10.1084/jem.20062596

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Barker TH, Baneyx G, Cardo-Vila M, Workman GA, Weaver M, Menon PM, Dedhar S, Rempel SA, Arap W, Pasqualini R, Vogel V, Sage EH (2005) SPARC regulates extracellular matrix organization through its modulation of integrin-linked kinase activity. J Biol Chem 280(43):36483–36493. doi:10.1074/jbc.M504663200

    Article  CAS  PubMed  Google Scholar 

  • Barsky SH, Siegal GP, Jannotta F, Liotta LA (1983) Loss of basement membrane components by invasive tumors but not by their benign counterparts. Lab Invest 49(2):140–147

    CAS  PubMed  Google Scholar 

  • Barth PJ, Moll R, Ramaswamy A (2005) Stromal remodeling and SPARC (secreted protein acid rich in cysteine) expression in invasive ductal carcinomas of the breast. Virchows Arch 446(5):532–536. doi:10.1007/s00428-005-1256-9

    Article  CAS  PubMed  Google Scholar 

  • Baum PD, Garriga G (1997) Neuronal migrations and axon fasciculation are disrupted in ina-1 integrin mutants. Neuron 19(1):51–62

    Article  CAS  PubMed  Google Scholar 

  • Beerling E, Ritsma L, Vrisekoop N, Derksen PW, van Rheenen J (2011) Intravital microscopy: new insights into metastasis of tumors. J Cell Sci 124(Pt 3):299–310. doi:10.1242/jcs.072728

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Behrens DT, Villone D, Koch M, Brunner G, Sorokin L, Robenek H, Bruckner-Tuderman L, Bruckner P, Hansen U (2012) The epidermal basement membrane is a composite of separate laminin- or collagen IV-containing networks connected by aggregated perlecan, but not by nidogens. J Biol Chem 287(22):18700–18709. doi:10.1074/jbc.M111.336073

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bergman A, Condeelis JS, Gligorijevic B (2014) Invadopodia in context. Cell Adh Migr 8(3):273–279

    Article  PubMed  PubMed Central  Google Scholar 

  • Briggs J, Chamboredon S, Castellazzi M, Kerry JA, Bos TJ (2002) Transcriptional upregulation of SPARC, in response to c-Jun overexpression, contributes to increased motility and invasion of MCF7 breast cancer cells. Oncogene 21(46):7077–7091. doi:10.1038/sj.onc.1205857

    Article  CAS  PubMed  Google Scholar 

  • Candiello J, Balasubramani M, Schreiber EM, Cole GJ, Mayer U, Halfter W, Lin H (2007) Biomechanical properties of native basement membranes. FEBS J 274(11):2897–2908. doi:10.1111/j.1742-4658.2007.05823.x

    Article  CAS  PubMed  Google Scholar 

  • Chen WT (1989) Proteolytic activity of specialized surface protrusions formed at rosette contact sites of transformed cells. J Exp Zool 251(2):167–185. doi:10.1002/jez.1402510206

    Article  CAS  PubMed  Google Scholar 

  • Cheung M, Chaboissier MC, Mynett A, Hirst E, Schedl A, Briscoe J (2005) The transcriptional control of trunk neural crest induction, survival, and delamination. Dev Cell 8(2):179–192. doi:10.1016/j.devcel.2004.12.010

    Article  CAS  PubMed  Google Scholar 

  • Christofori G (2006) New signals from the invasive front. Nature 441(7092):444–450. doi:10.1038/nature04872 (nature04872 [pii])

  • Clevers H (2013) The intestinal crypt, a prototype stem cell compartment. Cell 154(2):274–284. doi:10.1016/j.cell.2013.07.004

    Article  CAS  PubMed  Google Scholar 

  • Cluzel C, Saltel F, Lussi J, Paulhe F, Imhof BA, Wehrle-Haller B (2005) The mechanisms and dynamics of (alpha)v(beta)3 integrin clustering in living cells. J Cell Biol 171(2):383–392. doi:10.1083/jcb.200503017

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • David-Pfeuty T, Singer SJ (1980) Altered distributions of the cytoskeletal proteins vinculin and alpha-actinin in cultured fibroblasts transformed by Rous sarcoma virus. Proc Natl Acad Sci USA 77(11):6687–6691

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Destaing O, Block MR, Planus E, Albiges-Rizo C (2011) Invadosome regulation by adhesion signaling. Curr Opin Cell Biol 23(5):597–606. doi:10.1016/j.ceb.2011.04.002

    Article  CAS  PubMed  Google Scholar 

  • Dickinson DJ, Ward JD, Reiner DJ, Goldstein B (2013) Engineering the Caenorhabditis elegans genome using Cas9-triggered homologous recombination. Nat Methods 10(10):1028–1034. doi:10.1038/nmeth.2641

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Dieterich C, Clifton SW, Schuster LN, Chinwalla A, Delehaunty K, Dinkelacker I, Fulton L, Fulton R, Godfrey J, Minx P, Mitreva M, Roeseler W, Tian H, Witte H, Yang SP, Wilson RK, Sommer RJ (2008) The Pristionchus pacificus genome provides a unique perspective on nematode lifestyle and parasitism. Nat Genet 40(10):1193–1198. doi:10.1038/ng.227

    Article  CAS  PubMed  Google Scholar 

  • Dufour A, Overall CM (2013) Missing the target: matrix metalloproteinase antitargets in inflammation and cancer. Trends Pharmacol Sci 34(4):233–242. doi:10.1016/j.tips.2013.02.004

    Article  CAS  PubMed  Google Scholar 

  • Dumartin L, Quemener C, Laklai H, Herbert J, Bicknell R, Bousquet C, Pyronnet S, Castronovo V, Schilling MK, Bikfalvi A, Hagedorn M (2010) Netrin-1 mediates early events in pancreatic adenocarcinoma progression, acting on tumor and endothelial cells. Gastroenterology 138(4):1595–1606, 1606.e1–8. doi:10.1053/j.gastro.2009.12.061

  • Ell B, Kang Y (2013) Transcriptional control of cancer metastasis. Trends Cell Biol 23(12):603–611. doi:10.1016/j.tcb.2013.06.001

    Article  CAS  PubMed  Google Scholar 

  • Even-Ram S, Yamada KM (2005) Cell migration in 3D matrix. Curr Opin Cell Biol 17(5):524–532

    Article  CAS  PubMed  Google Scholar 

  • Fidler AL, Vanacore RM, Chetyrkin SV, Pedchenko VK, Bhave G, Yin VP, Stothers CL, Rose KL, McDonald WH, Clark TA, Borza DB, Steele RE, Ivy MT, Aspirnauts, Hudson JK, Hudson BG (2014) A unique covalent bond in basement membrane is a primordial innovation for tissue evolution. Proc Natl Acad Sci USA 111(1):331–336. doi:10.1073/pnas.1318499111

    Article  CAS  PubMed  Google Scholar 

  • Fitzgerald MC, Schwarzbauer JE (1998) Importance of the basement membrane protein SPARC for viability and fertility in Caenorhabditis elegans. Curr Biol 8(23):1285–1288. doi:S0960-9822(07)00540-4 [pii]

    Google Scholar 

  • Flug M, Kopf-Maier P (1995) The basement membrane and its involvement in carcinoma cell invasion. Acta Anat 152(2):69–84

    Article  CAS  PubMed  Google Scholar 

  • Fox JW, Mayer U, Nischt R, Aumailley M, Reinhardt D, Wiedemann H, Mann K, Timpl R, Krieg T, Engel J et al (1991) Recombinant nidogen consists of three globular domains and mediates binding of laminin to collagen type IV. EMBO J 10(11):3137–3146

    CAS  PubMed  PubMed Central  Google Scholar 

  • Frei JV (1962) The fine structure of the basement membrane in epidermal tumors. J Cell Biol 15:335–342

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Frittoli E, Palamidessi A, Marighetti P, Confalonieri S, Bianchi F, Malinverno C, Mazzarol G, Viale G, Martin-Padura I, Garré M, Parazzoli D, Mattei V, Cortellino S, Bertalot G, Di Fiore PP, Scita G (2014) A RAB5/RAB4 recycling circuitry induces a proteolytic invasive program and promotes tumor dissemination. J Cell Biol 206(2):307–328. doi:10.1083/jcb.201403127

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gabbert H, Wagner R, Moll R, Gerharz CD (1985) Tumor dedifferentiation: an important step in tumor invasion. Clin Exp Metastasis 3(4):257–279

    Article  CAS  PubMed  Google Scholar 

  • Gayrard C, Borghi N (2016) FRET-based molecular tension microscopy. Methods 94:33–42. doi:10.1016/j.ymeth.2015.07.010

    Article  CAS  PubMed  Google Scholar 

  • Gil-Henn H, Patsialou A, Wang Y, Warren MS, Condeelis JS, Koleske AJ (2013) Arg/Abl2 promotes invasion and attenuates proliferation of breast cancer in vivo. Oncogene 32(21):2622–2630. doi:10.1038/onc.2012.284

    Article  CAS  PubMed  Google Scholar 

  • Golembieski WA, Ge S, Nelson K, Mikkelsen T, Rempel SA (1999) Increased SPARC expression promotes U87 glioblastoma invasion in vitro. Int J Dev Neurosci 17(5–6):463–472. doi:S0736-5748(99)00009-X [pii]

    Google Scholar 

  • Gonzales KA, Liang H, Lim YS, Chan YS, Yeo JC, Tan CP, Gao B, Le B, Tan ZY, Low KY, Liou YC, Bard F, Ng HH (2015) Deterministic restriction on pluripotent state dissolution by cell-cycle pathways. Cell 162(3):564–579. doi:10.1016/j.cell.2015.07.001

    Article  CAS  PubMed  Google Scholar 

  • Greenwald I (2005) LIN-12/Notch signaling in C. elegans. WormBook 1–16. doi:10.1895/wormbook.1.10.1

  • Hagedorn EJ, Sherwood DR (2011) Cell invasion through basement membrane: the anchor cell breaches the barrier. Curr Opin Cell Biol 23(5):589–596. doi:10.1016/j.ceb.2011.05.002 (S0955-0674(11)00063-9 [pii])

  • Hagedorn EJ, Yashiro H, Ziel JW, Ihara S, Wang Z, Sherwood DR (2009) Integrin acts upstream of netrin signaling to regulate formation of the anchor cell’s invasive membrane in C. elegans. Dev Cell 17(2):187–198. doi:10.1016/j.devcel.2009.06.006 (S1534-5807(09)00247-0 [pii])

  • Hagedorn EJ, Ziel JW, Morrissey MA, Linden LM, Wang Z, Chi Q, Johnson SA, Sherwood DR (2013) The netrin receptor DCC focuses invadopodia-driven basement membrane transmigration in vivo. J Cell Biol 201(6):903–913. doi:10.1083/jcb.201301091

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hagedorn EJ, Kelley LC, Naegeli KM, Wang Z, Chi Q, Sherwood DR (2014) ADF/cofilin promotes invadopodial membrane recycling during cell invasion in vivo. J Cell Biol 204(7):1209–1218. doi:10.1083/jcb.201312098

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Halfter W, Oertle P, Monnier CA, Camenzind L, Reyes-Lua M, Hu H, Candiello J, Labilloy A, Balasubramani M, Henrich PB, Plodinec M (2015) New concepts in basement membrane biology. FEBS J 282(23):4466–4479. doi:10.1111/febs.13495

    Article  CAS  PubMed  Google Scholar 

  • Harris BS, Zhang Y, Card L, Rivera LB, Brekken RA, Bradshaw AD (2011) SPARC regulates collagen interaction with cardiac fibroblast cell surfaces. Am J Physiol Heart Circ Physiol 301(3):H841–H847. doi:10.1152/ajpheart.01247.2010 (ajpheart.01247.2010 [pii])

  • Harunaga JS, Doyle AD, Yamada KM (2014) Local and global dynamics of the basement membrane during branching morphogenesis require protease activity and actomyosin contractility. Dev Biol 394(2):197–205. doi:10.1016/j.ydbio.2014.08.014

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hesselson D, Newman C, Kim KW, Kimble J (2004) GON-1 and fibulin have antagonistic roles in control of organ shape. Curr Biol 14(22):2005–2010. doi:10.1016/j.cub.2004.11.006

    Article  CAS  PubMed  Google Scholar 

  • Hiramatsu R, Matsuoka T, Kimura-Yoshida C, Han SW, Mochida K, Adachi T, Takayama S, Matsuo I (2013) External mechanical cues trigger the establishment of the anterior-posterior axis in early mouse embryos. Dev Cell 27(2):131–144. doi:10.1016/j.devcel.2013.09.026

    Article  CAS  PubMed  Google Scholar 

  • Hoek KS, Eichhoff OM, Schlegel NC, Dobbeling U, Kobert N, Schaerer L, Hemmi S, Dummer R (2008) In vivo switching of human melanoma cells between proliferative and invasive states. Cancer Res 68(3):650–656. doi:10.1158/0008-5472.CAN-07-2491

    Article  CAS  PubMed  Google Scholar 

  • Hohenester E, Yurchenco PD (2013) Laminins in basement membrane assembly. Cell Adh Migr 7(1):56–63. doi:10.4161/cam.21831

    Article  PubMed  PubMed Central  Google Scholar 

  • Hoshino D, Branch KM, Weaver AM (2013) Signaling inputs to invadopodia and podosomes. J Cell Sci 126(Pt 14):2979–2989. doi:10.1242/jcs.079475

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hotary K, Li XY, Allen E, Stevens SL, Weiss SJ (2006) A cancer cell metalloprotease triad regulates the basement membrane transmigration program. Genes Dev 20(19):2673–2686

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hwang BJ, Meruelo AD, Sternberg PW (2007) C. elegans EVI1 proto-oncogene, EGL-43, is necessary for Notch-mediated cell fate specification and regulates cell invasion. Development 134(4):669–679

    Article  CAS  PubMed  Google Scholar 

  • Hynes RO (2012) The evolution of metazoan extracellular matrix. J Cell Biol 196(6):671–679. doi:10.1083/jcb.201109041

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Iacobuzio-Donahue CA, Argani P, Hempen PM, Jones J, Kern SE (2002) The desmoplastic response to infiltrating breast carcinoma: gene expression at the site of primary invasion and implications for comparisons between tumor types. Cancer Res 62(18):5351–5357

    CAS  PubMed  Google Scholar 

  • Ihara S, Hagedorn EJ, Morrissey MA, Chi Q, Motegi F, Kramer JM, Sherwood DR (2011) Basement membrane sliding and targeted adhesion remodels tissue boundaries during uterine-vulval attachment in Caenorhabditis elegans. Nat Cell Biol 13(6):641–651. doi:10.1038/ncb2233 (ncb2233 [pii])

  • Jacob K, Webber M, Benayahu D, Kleinman HK (1999) Osteonectin promotes prostate cancer cell migration and invasion: a possible mechanism for metastasis to bone. Cancer Res 59(17):4453–4457

    CAS  PubMed  Google Scholar 

  • Johnson RP, Kang SH, Kramer JM (2006) C. elegans dystroglycan DGN-1 functions in epithelia and neurons, but not muscle, and independently of dystrophin. Development 133(10):1911–1921. doi:10.1242/dev.02363

    Article  CAS  PubMed  Google Scholar 

  • Joyce JA, Pollard JW (2009) Microenvironmental regulation of metastasis. Nat Rev Cancer 9(4):239–252. doi:10.1038/nrc2618

    Article  CAS  PubMed  Google Scholar 

  • Kai F, Laklai H, Weaver VM (2016) Force matters: biomechanical regulation of cell invasion and migration in disease. Trends Cell Biol 26(7):486–497. doi:10.1016/j.tcb.2016.03.007

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Karp X, Greenwald I (2004) Multiple roles for the E/Daughterless ortholog HLH-2 during C. elegans gonadogenesis. Dev Biol 272(2):460–469. doi:10.1016/j.ydbio.2004.05.015

    Article  CAS  PubMed  Google Scholar 

  • Kato Y, Sakai N, Baba M, Kaneko S, Kondo K, Kubota Y, Yao M, Shuin T, Saito S, Koshika S, Kawase T, Miyagi Y, Aoki I, Nagashima Y (1998) Stimulation of motility of human renal cell carcinoma by SPARC/Osteonectin/BM-40 associated with type IV collagen. Invasion Metastasis 18(2):105–114. doi:24503 [pii]

    Google Scholar 

  • Kaufmann S, Kuphal S, Schubert T, Bosserhoff AK (2009) Functional implication of Netrin expression in malignant melanoma. Cell Oncol 31(6):415–422. doi:10.3233/CLO-2009-0491

    CAS  PubMed  PubMed Central  Google Scholar 

  • Kelley LC, Lohmer LL, Hagedorn EJ, Sherwood DR (2014) Traversing the basement membrane in vivo: a diversity of strategies. J Cell Biol 204(3):291–302. doi:10.1083/jcb.201311112

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Khoshnoodi J, Pedchenko V, Hudson BG (2008) Mammalian collagen IV. Microsc Res Tech 71(5):357–370. doi:10.1002/jemt.20564

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kiontke K, Barriere A, Kolotuev I, Podbilewicz B, Sommer R, Fitch DH, Felix MA (2007) Trends, stasis, and drift in the evolution of nematode vulva development. Curr Biol 17(22):1925–1937. doi:10.1016/j.cub.2007.10.061

    Article  CAS  PubMed  Google Scholar 

  • Ko SY, Blatch GL, Dass CR (2014) Netrin-1 as a potential target for metastatic cancer: focus on colorectal cancer. Cancer Metastasis Rev 33(1):101–113. doi:10.1007/s10555-013-9459-z

    Article  CAS  PubMed  Google Scholar 

  • Kobayashi Y, Nakajima T, Saku T (1995) Loss of basement membranes in the invading front of O-1N, hamster squamous cell carcinoma with high potential of lymph node metastasis: an immunohistochemical study for laminin and type IV collagen. Pathol Int 45(5):327–334

    Article  CAS  PubMed  Google Scholar 

  • Kramer JM (2005) Basement membranes. WormBook 1–15

    Google Scholar 

  • Ledda MF, Adris S, Bravo AI, Kairiyama C, Bover L, Chernajovsky Y, Mordoh J, Podhajcer OL (1997) Suppression of SPARC expression by antisense RNA abrogates the tumorigenicity of human melanoma cells. Nat Med 3(2):171–176

    Article  CAS  PubMed  Google Scholar 

  • Leight ER, Murphy JT, Fantz DA, Pepin D, Schneider DL, Ratliff TM, Mohammad DH, Herman MA, Kornfeld K (2015) Conversion of the LIN-1 ETS protein of Caenorhabditis elegans from a SUMOylated transcriptional repressor to a phosphorylated transcriptional activator. Genetics 199(3):761–775. doi:10.1534/genetics.114.172668

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Leong HS, Robertson AE, Stoletov K, Leith SJ, Chin CA, Chien AE, Hague MN, Ablack A, Carmine-Simmen K, McPherson VA, Postenka CO, Turley EA, Courtneidge SA, Chambers AF, Lewis JD (2014) Invadopodia are required for cancer cell extravasation and are a therapeutic target for metastasis. Cell Rep 8(5):1558–1570. doi:10.1016/j.celrep.2014.07.050

    Article  CAS  PubMed  Google Scholar 

  • Linder S, Wiesner C, Himmel M (2011) Degrading devices: invadosomes in proteolytic cell invasion. Annu Rev Cell Dev Biol 27:185–211. doi:10.1146/annurev-cellbio-092910-154216

    Article  CAS  PubMed  Google Scholar 

  • Lohmer LL, Kelley LC, Hagedorn EJ, Sherwood DR (2014) Invadopodia and basement membrane invasion in vivo. Cell Adh Migr 8(3):246–255

    Article  PubMed  PubMed Central  Google Scholar 

  • Lohmer LL, Clay MR, Naegeli KM, Chi Q, Ziel JW, Hagedorn EJ, Park JE, Jayadev R, Sherwood DR (2016) A sensitized screen for genes promoting invadopodia function in vivo: CDC-42 and Rab GDI-1 direct distinct aspects of invadopodia formation. PLoS Genet 12(1):e1005786. doi:10.1371/journal.pgen.1005786

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Lokman NA, Elder AS, Ricciardelli C, Oehler MK (2012) Chick chorioallantoic membrane (CAM) assay as an in vivo model to study the effect of newly identified molecules on ovarian cancer invasion and metastasis. Int J Mol Sci 13(8):9959–9970. doi:10.3390/ijms13089959

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ma Y, Kanakousaki K, Buttitta L (2015) How the cell cycle impacts chromatin architecture and influences cell fate. Front Genet 6:19. doi:10.3389/fgene.2015.00019

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Madsen CD, Sahai E (2010) Cancer dissemination—lessons from leukocytes. Dev Cell 19(1):13–26. doi:10.1016/j.devcel.2010.06.013 (S1534-5807(10)00303-5 [pii])

  • Martinek N, Zou R, Berg M, Sodek J, Ringuette M (2002) Evolutionary conservation and association of SPARC with the basal lamina in Drosophila. Dev Genes Evol 212(3):124–133. doi:10.1007/s00427-002-0220-9

    Article  CAS  PubMed  Google Scholar 

  • Martinek N, Shahab J, Sodek J, Ringuette M (2007) Is SPARC an evolutionarily conserved collagen chaperone? J Dent Res 86(4):296–305

    Article  CAS  PubMed  Google Scholar 

  • Martinek N, Shahab J, Saathoff M, Ringuette M (2008) Haemocyte-derived SPARC is required for collagen-IV-dependent stability of basal laminae in Drosophila embryos. J Cell Sci 121(Pt 10):1671–1680. doi:10.1242/jcs.021931 (jcs.021931 [pii])

  • Matus DQ, Li XY, Durbin S, Agarwal D, Chi Q, Weiss SJ, Sherwood DR (2010) In vivo identification of regulators of cell invasion across basement membranes. Sci Signal 3(120):ra35. doi:10.1126/scisignal.2000654 (3/120/ra35 [pii])

  • Matus DQ, Chang E, Makohon-Moore SC, Hagedorn MA, Chi Q, Sherwood DR (2014) Cell division and targeted cell cycle arrest opens and stabilizes basement membrane gaps. Nat Commun 5:4184. doi:10.1038/ncomms5184

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Matus DQ, Lohmer LL, Kelley LC, Schindler AJ, Kohrman AQ, Barkoulas M, Zhang W, Chi Q, Sherwood DR (2015) Invasive cell fate requires G1 cell-cycle arrest and histone deacetylase-mediated changes in gene expression. Dev Cell 35(2):162–174. doi:10.1016/j.devcel.2015.10.002

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • McClung HM, Thomas SL, Osenkowski P, Toth M, Menon P, Raz A, Fridman R, Rempel SA (2007) SPARC upregulates MT1-MMP expression, MMP-2 activation, and the secretion and cleavage of galectin-3 in U87MG glioma cells. Neurosci Lett 419(2):172–177. doi:10.1016/j.neulet.2007.04.037 (S0304-3940(07)00479-X [pii])

  • Minn AJ, Gupta GP, Siegel PM, Bos PD, Shu W, Giri DD, Viale A, Olshen AB, Gerald WL, Massague J (2005) Genes that mediate breast cancer metastasis to lung. Nature 436(7050):518–524. doi:10.1038/nature03799

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Monteiro P, Rosse C, Castro-Castro A, Irondelle M, Lagoutte E, Paul-Gilloteaux P, Desnos C, Formstecher E, Darchen F, Perrais D, Gautreau A, Hertzog M, Chavrier P (2013) Endosomal WASH and exocyst complexes control exocytosis of MT1-MMP at invadopodia. J Cell Biol 203(6):1063–1079. doi:10.1083/jcb.201306162

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Morrissey MA, Hagedorn EJ, Sherwood DR (2013) Cell invasion through basement membrane: the netrin receptor DCC guides the way. WormBook 2(3):e26169. doi:10.4161/worm.26169

    Google Scholar 

  • Morrissey MA, Keeley DP, Hagedorn EJ, McClatchey ST, Chi Q, Hall DH, Sherwood DR (2014) B-LINK: a hemicentin, plakin, and integrin-dependent adhesion system that links tissues by connecting adjacent basement membranes. Dev Cell 31(3):319–331. doi:10.1016/j.devcel.2014.08.024

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Morrissey MA, Jayadev R, Miley GR, Blebea CA, Chi Q, Ihara S, Sherwood DR (2016) SPARC promotes cell invasion in vivo by decreasing type IV collagen levels in the basement membrane. PLoS Genet 12(2):e1005905. doi:10.1371/journal.pgen.1005905

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Moshfegh Y, Bravo-Cordero JJ, Miskolci V, Condeelis J, Hodgson L (2014) A Trio-Rac1-Pak1 signalling axis drives invadopodia disassembly. Nat Cell Biol 16(6):574–586. doi:10.1038/ncb2972

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mummery CL, van Rooijen MA, van den Brink SE, de Laat SW (1987) Cell cycle analysis during retinoic acid induced differentiation of a human embryonal carcinoma-derived cell line. Cell Differ 20(2–3):153–160

    Article  CAS  PubMed  Google Scholar 

  • Murphy DA, Courtneidge SA (2011) The ‘ins’ and ‘outs’ of podosomes and invadopodia: characteristics, formation and function. Nat Rev Mol Cell Biol 12(7):413–426. doi:10.1038/nrm3141

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Nagaraju GP, Dontula R, El-Rayes BF, Lakka SS (2014) Molecular mechanisms underlying the divergent roles of SPARC in human carcinogenesis. Carcinogenesis 35(5):967–973. doi:10.1093/carcin/bgu072

    Article  CAS  PubMed  Google Scholar 

  • Nakaya Y, Sukowati EW, Wu Y, Sheng G (2008) RhoA and microtubule dynamics control cell-basement membrane interaction in EMT during gastrulation. Nat Cell Biol 10(7):765–775. doi:10.1038/ncb1739 (ncb1739 [pii])

  • Nguyen DX, Bos PD, Massague J (2009) Metastasis: from dissemination to organ-specific colonization. Nat Rev Cancer 9(4):274–284. doi:10.1038/nrc2622

    Article  CAS  PubMed  Google Scholar 

  • Nguyen-Ngoc KV, Cheung KJ, Brenot A, Shamir ER, Gray RS, Hines WC, Yaswen P, Werb Z, Ewald AJ (2012) ECM microenvironment regulates collective migration and local dissemination in normal and malignant mammary epithelium. Proc Natl Acad Sci USA 109(39):E2595–E2604. doi:10.1073/pnas.1212834109

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Overall CM, Kleifeld O (2006) Tumour microenvironment – opinion: validating matrix metalloproteinases as drug targets and anti-targets for cancer therapy. Nat Rev Cancer 6(3):227–239. doi:10.1038/nrc1821 (nrc1821 [pii])

  • Ozanne BW, Spence HJ, McGarry LC, Hennigan RF (2006) Invasion is a genetic program regulated by transcription factors. Curr Opin Genet Dev 16(1):65–70. doi:10.1016/j.gde.2005.12.012 (S0959-437X(05)00225-X [pii])

  • Ozbek S, Balasubramanian PG, Chiquet-Ehrismann R, Tucker RP, Adams JC (2010) The evolution of extracellular matrix. Mol Biol Cell 21(24):4300–4305. doi:10.1091/mbc.E10-03-0251

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Page-McCaw A, Ewald AJ, Werb Z (2007) Matrix metalloproteinases and the regulation of tissue remodelling. Nat Rev Mol Cell Biol 8(3):221–233. doi:10.1038/nrm2125 (nrm2125 [pii])

  • Patel J, Landers KA, Mortimer RH, Richard K (2012) Expression and uptake of the thyroxine-binding protein transthyretin is regulated by oxygen in primary trophoblast placental cells. J Endocrinol 212(2):159–167. doi:10.1530/JOE-11-0348

    Article  CAS  PubMed  Google Scholar 

  • Pflicke H, Sixt M (2009) Preformed portals facilitate dendritic cell entry into afferent lymphatic vessels. J Exp Med 206(13):2925–2935. doi:10.1084/jem.20091739

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Podhajcer OL, Benedetti L, Girotti MR, Prada F, Salvatierra E, Llera AS (2008) The role of the matricellular protein SPARC in the dynamic interaction between the tumor and the host. Cancer Metastasis Rev 27(3):523–537. doi:10.1007/s10555-008-9135-x

    Article  CAS  PubMed  Google Scholar 

  • Poincloux R, Lizarraga F, Chavrier P (2009) Matrix invasion by tumour cells: a focus on MT1-MMP trafficking to invadopodia. J Cell Sci 122(Pt 17):3015–3024. doi:10.1242/jcs.034561 (122/17/3015 [pii])

  • Poschl E, Schlotzer-Schrehardt U, Brachvogel B, Saito K, Ninomiya Y, Mayer U (2004) Collagen IV is essential for basement membrane stability but dispensable for initiation of its assembly during early development. Development 131(7):1619–1628. doi:10.1242/dev.01037

    Article  PubMed  CAS  Google Scholar 

  • Quail DF, Joyce JA (2013) Microenvironmental regulation of tumor progression and metastasis. Nat Med 19(11):1423–1437. doi:10.1038/nm.3394

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rich JN, Shi Q, Hjelmeland M, Cummings TJ, Kuan CT, Bigner DD, Counter CM, Wang XF (2003) Bone-related genes expressed in advanced malignancies induce invasion and metastasis in a genetically defined human cancer model. J Biol Chem 278(18):15951–15957. doi:10.1074/jbc.M211498200

    Article  CAS  PubMed  Google Scholar 

  • Rimann I, Hajnal A (2007) Regulation of anchor cell invasion and uterine cell fates by the egl-43 Evi-1 proto-oncogene in Caenorhabditis elegans. Dev Biol 308(1):187–195

    Article  CAS  PubMed  Google Scholar 

  • Rodriguez-Jimenez FJ, Caldes T, Iniesta P, Vidart JA, Garcia-Asenjo JL, Benito M (2007) Overexpression of SPARC protein contrasts with its transcriptional silencing by aberrant hypermethylation of SPARC CpG-rich region in endometrial carcinoma. Oncol Rep 17(6):1301–1307

    CAS  PubMed  Google Scholar 

  • Rowe RG, Weiss SJ (2008) Breaching the basement membrane: who, when and how? Trends Cell Biol 18(11):560–574. doi:10.1016/j.tcb.2008.08.007 (S0962-8924(08)00235-3 [pii])

  • Ruijtenberg S, van den Heuvel S (2015) G1/S inhibitors and the SWI/SNF complex control cell-cycle exit during muscle differentiation. Cell 162(2):300–313. doi:10.1016/j.cell.2015.06.013

    Article  CAS  PubMed  Google Scholar 

  • Sage H, Vernon RB, Funk SE, Everitt EA, Angello J (1989) SPARC, a secreted protein associated with cellular proliferation, inhibits cell spreading in vitro and exhibits Ca+2-dependent binding to the extracellular matrix. J Cell Biol 109(1):341–356

    Article  CAS  PubMed  Google Scholar 

  • Sameni M, Cavallo-Medved D, Dosescu J, Jedeszko C, Moin K, Mullins SR, Olive MB, Rudy D, Sloane BF (2009) Imaging and quantifying the dynamics of tumor-associated proteolysis. Clin Exp Metastasis 26(4):299–309. doi:10.1007/s10585-008-9218-7

    Article  CAS  PubMed  Google Scholar 

  • Sasaki T, Hohenester E, Gohring W, Timpl R (1998) Crystal structure and mapping by site-directed mutagenesis of the collagen-binding epitope of an activated form of BM-40/SPARC/osteonectin. EMBO J 17(6):1625–1634. doi:10.1093/emboj/17.6.1625

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sato N, Fukushima N, Maehara N, Matsubayashi H, Koopmann J, Su GH, Hruban RH, Goggins M (2003) SPARC/osteonectin is a frequent target for aberrant methylation in pancreatic adenocarcinoma and a mediator of tumor-stromal interactions. Oncogene 22(32):5021–5030. doi:10.1038/sj.onc.1206807

    Article  CAS  PubMed  Google Scholar 

  • Saunders LR, McClay DR (2014) Sub-circuits of a gene regulatory network control a developmental epithelial-mesenchymal transition. Development 141(7):1503–1513. doi:10.1242/dev.101436

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Schindler AJ, Sherwood DR (2011) The transcription factor HLH-2/E/Daughterless regulates anchor cell invasion across basement membrane in C. elegans. Dev Biol 357(2):380–391. doi:10.1016/j.ydbio.2011.07.012

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Schindler AJ, Sherwood DR (2013) Morphogenesis of the caenorhabditis elegans vulva. Wiley Interdiscip Rev Dev Biol 2(1):75–95. doi:10.1002/wdev.87

    Article  CAS  PubMed  Google Scholar 

  • Schoumacher M, Goldman RD, Louvard D, Vignjevic DM (2010) Actin, microtubules, and vimentin intermediate filaments cooperate for elongation of invadopodia. J Cell Biol 189(3):541–556. doi:10.1083/jcb.200909113 (jcb.200909113 [pii])

  • Schoumacher M, Glentis A, Gurchenkov VV, Vignjevic DM (2013) Basement membrane invasion assays: native basement membrane and chemoinvasion assay. Methods Mol Biol 1046:133–144. doi:10.1007/978-1-62703-538-5_8

    Article  PubMed  CAS  Google Scholar 

  • Schultz C, Lemke N, Ge S, Golembieski WA, Rempel SA (2002) Secreted protein acidic and rich in cysteine promotes glioma invasion and delays tumor growth in vivo. Cancer Res 62(21):6270–6277

    CAS  PubMed  Google Scholar 

  • Seano G, Chiaverina G, Gagliardi PA, di Blasio L, Puliafito A, Bouvard C, Sessa R, Tarone G, Sorokin L, Helley D, Jain RK, Serini G, Bussolino F Primo L (2014) Endothelial podosome rosettes regulate vascular branching in tumour angiogenesis. Nat Cell Biol 16(10):931–941, 931–938. doi:10.1038/ncb3036

  • Seguin L, Desgrosellier JS, Weis SM, Cheresh DA (2015) Integrins and cancer: regulators of cancer stemness, metastasis, and drug resistance. Trends Cell Biol 25(4):234–240. doi:10.1016/j.tcb.2014.12.006

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Shahab J, Baratta C, Scuric B, Godt D, Venken KJ, Ringuette MJ (2015) Loss of SPARC dysregulates basal lamina assembly to disrupt larval fat body homeostasis in Drosophila melanogaster. Dev Dyn 244(4):540–552. doi:10.1002/dvdy.24243

    Article  CAS  PubMed  Google Scholar 

  • Shekarabi M, Moore SW, Tritsch NX, Morris SJ, Bouchard JF, Kennedy TE (2005) Deleted in colorectal cancer binding netrin-1 mediates cell substrate adhesion and recruits Cdc42, Rac1, Pak1, and N-WASP into an intracellular signaling complex that promotes growth cone expansion. J Neurosci 25(12):3132–3141

    Article  CAS  PubMed  Google Scholar 

  • Sherwood DR (2015) A developmental biologist’s “outside-the-cell” thinking. J Cell Biol 210(3):369–372. doi:10.1083/jcb.201501083

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sherwood DR, Sternberg PW (2003) Anchor cell invasion into the vulval epithelium in C. elegans. Dev Cell 5(1):21–31

    Article  CAS  PubMed  Google Scholar 

  • Sherwood DR, Butler JA, Kramer JM, Sternberg PW (2005) FOS-1 promotes basement-membrane removal during anchor-cell invasion in C. elegans. Cell 121(6):951–962

    Article  CAS  PubMed  Google Scholar 

  • Shi Q, Bao S, Song L, Wu Q, Bigner DD, Hjelmeland AB, Rich JN (2007) Targeting SPARC expression decreases glioma cellular survival and invasion associated with reduced activities of FAK and ILK kinases. Oncogene 26(28):4084–4094. doi:10.1038/sj.onc.1210181

    Article  CAS  PubMed  Google Scholar 

  • Shimizu A, Nakayama H, Wang P, Konig C, Akino T, Sandlund J, Coma S, Italiano JE Jr, Mammoto A, Bielenberg DR, Klagsbrun M (2012) Netrin-1 promotes glioblastoma cell invasiveness and angiogenesis by multiple pathways involving activation of RhoA, cathepsin B and CREB. J Biol Chem 288(4):2210–2222. doi:10.1074/jbc.M112.397398

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Spaderna S, Schmalhofer O, Hlubek F, Berx G, Eger A, Merkel S, Jung A, Kirchner T, Brabletz T (2006) A transient, EMT-linked loss of basement membranes indicates metastasis and poor survival in colorectal cancer. Gastroenterology 131(3):830–840. doi:10.1053/j.gastro.2006.06.016

    Article  CAS  PubMed  Google Scholar 

  • Spencer WC, McWhirter R, Miller T, Strasbourger P, Thompson O, Hillier LW, Waterston RH, Miller DM 3rd (2014) Isolation of specific neurons from C. elegans larvae for gene expression profiling. PloS One 9(11):e112102. doi:10.1371/journal.pone.0112102

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Srivastava A, Pastor-Pareja JC, Igaki T, Pagliarini R, Xu T (2007) Basement membrane remodeling is essential for Drosophila disc eversion and tumor invasion. Proc Natl Acad Sci USA 104(8):2721–2726. doi:10.1073/pnas.0611666104 (0611666104 [pii])

  • Steeg PS (2003) Metastasis suppressors alter the signal transduction of cancer cells. Nat Rev Cancer 3(1):55–63. doi:10.1038/nrc967 (nrc967 [pii])

  • Stengel K, Zheng Y (2011) Cdc42 in oncogenic transformation, invasion, and tumorigenesis. Cell Signal 23(9):1415–1423. doi:10.1016/j.cellsig.2011.04.001

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ting DT, Wittner BS, Ligorio M, Vincent Jordan N, Shah AM, Miyamoto DT, Aceto N, Bersani F, Brannigan BW, Xega K, Ciciliano JC, Zhu H, MacKenzie OC, Trautwein J, Arora KS, Shahid M, Ellis HL, Qu N, Bardeesy N, Rivera MN, Deshpande V, Ferrone CR, Kapur R, Ramaswamy S, Shioda T, Toner M, Maheswaran S, Haber DA (2014) Single-cell RNA sequencing identifies extracellular matrix gene expression by pancreatic circulating tumor cells. Cell Rep 8(6):1905–1918. doi:10.1016/j.celrep.2014.08.029

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Trier JS, Allan CH, Abrahamson DR, Hagen SJ (1990) Epithelial basement membrane of mouse jejunum. Evidence for laminin turnover along the entire crypt-villus axis. J Clin Investig 86(1):87–95. doi:10.1172/JCI114720

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Trimble WS, Grinstein S (2015) Barriers to the free diffusion of proteins and lipids in the plasma membrane. J Cell Biol 208(3):259–271. doi:10.1083/jcb.201410071

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Vanacore R, Ham AJ, Voehler M, Sanders CR, Conrads TP, Veenstra TD, Sharpless KB, Dawson PE, Hudson BG (2009) A sulfilimine bond identified in collagen IV. Science 325(5945):1230–1234. doi:10.1126/science.1176811

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Vega S, Morales AV, Ocana OH, Valdes F, Fabregat I, Nieto MA (2004) Snail blocks the cell cycle and confers resistance to cell death. Genes Dev 18(10):1131–1143. doi:10.1101/gad.294104

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Verghese E, Schocken J, Jacob S, Wimer AM, Royce R, Nesmith JE, Baer GM, Clever S, McCain E, Lakowski B, Wightman B (2011) The tailless ortholog nhr-67 functions in the development of the C. elegans ventral uterus. Dev Biol 356(2):516–528. doi:10.1016/j.ydbio.2011.06.007

    Article  CAS  PubMed  Google Scholar 

  • Voisin MB, Woodfin A, Nourshargh S (2009) Monocytes and neutrophils exhibit both distinct and common mechanisms in penetrating the vascular basement membrane in vivo. Arterioscler Thromb Vasc Biol 29(8):1193–1199. doi:10.1161/ATVBAHA.109.187450

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Voisin MB, Probstl D, Nourshargh S (2010) Venular basement membranes ubiquitously express matrix protein low-expression regions: characterization in multiple tissues and remodeling during inflammation. Am J Pathol 176(1):482–495. doi:10.2353/ajpath.2010.090510

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wang Z, Sherwood DR (2011) Dissection of genetic pathways in C. elegans. Methods Cell Biol 106:113–157. doi:10.1016/B978-0-12-544172-8.00005-0

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wang W, Goswami S, Lapidus K, Wells AL, Wyckoff JB, Sahai E, Singer RH, Seqall JE, Condeelis JS (2004) Identification and testing of a gene expression signature of invasive carcinoma cells within primary mammary tumors. Cancer Res 64(23):8585–8594. doi:10.1158/0008-5472.CAN-04-1136

    Article  CAS  PubMed  Google Scholar 

  • Wang S, Voisin MB, Larbi KY, Dangerfield J, Scheiermann C, Tran M, Maxwell PH, Sorokin L, Nourshargh S (2006) Venular basement membranes contain specific matrix protein low expression regions that act as exit points for emigrating neutrophils. J Exp Med 203(6):1519–1532

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wang Z, Chi Q, Sherwood DR (2014a) MIG-10 (lamellipodin) has netrin-independent functions and is a FOS-1A transcriptional target during anchor cell invasion in C. elegans. Development 141(6):1342–1353. doi:10.1242/dev.102434

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wang Z, Linden LM, Naegeli KM, Ziel JW, Chi Q, Hagedorn EJ, Savage NS, Sherwood DR (2014b) UNC-6 (netrin) stabilizes oscillatory clustering of the UNC-40 (DCC) receptor to orient polarity. J Cell Biol 206(5):619–633. doi:10.1083/jcb.201405026

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wang L, Shen W, Lei S, Matus D, Sherwood D, Wang Z (2014c) MIG-10 (Lamellipodin) stabilizes invading cell adhesion to basement membrane and is a negative transcriptional target of EGL-43 in C. elegans. Biochem Biophys Res Commun 452(3):328–333. doi:10.1016/j.bbrc.2014.08.049

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wickstrom SA, Fassler R (2011) Regulation of membrane traffic by integrin signaling. Trends Cell Biol 21(5):266–273. doi:10.1016/j.tcb.2011.02.003

    Article  PubMed  CAS  Google Scholar 

  • Williams KC, Coppolino MG (2011) Phosphorylation of membrane type 1-matrix metalloproteinase (MT1-MMP) and its vesicle-associated membrane protein 7 (VAMP7)-dependent trafficking facilitate cell invasion and migration. J Biol Chem 286(50):43405–43416. doi:10.1074/jbc.M111.297069

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wolf K, Te Lindert M, Krause M, Alexander S, Te Riet J, Willis AL, Hoffman RM, Figdor CG, Weiss SJ, Friedl P (2013) Physical limits of cell migration: control by ECM space and nuclear deformation and tuning by proteolysis and traction force. J Cell Biol 201(7):1069–1084. doi:10.1083/jcb.201210152

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wu ZQ, Brabletz T, Fearon E, Willis AL, Hu CY, Li XY, Weiss SJ (2012) Canonical Wnt suppressor, Axin2, promotes colon carcinoma oncogenic activity. Proc Natl Acad Sci USA 109(28):11312–11317. doi:10.1073/pnas.1203015109

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yamaguchi H, Oikawa T (2010) Membrane lipids in invadopodia and podosomes: key structures for cancer invasion and metastasis. Oncotarget 1(5):320–328

    Article  PubMed  PubMed Central  Google Scholar 

  • Yang J, Weinberg RA (2008) Epithelial-mesenchymal transition: at the crossroads of development and tumor metastasis. Dev Cell 14(6):818–829. doi:10.1016/j.devcel.2008.05.009

    Article  CAS  PubMed  Google Scholar 

  • Yano S, Zhang Y, Miwa S, Tome Y, Hiroshima Y, Uehara F, Yamamoto M, Suetsugu A, Kishimoto H, Tazawa H, Zhao M, Bouvet M, Fujiwara T, Hoffman RM (2014) Spatial-temporal FUCCI imaging of each cell in a tumor demonstrates locational dependence of cell cycle dynamics and chemoresponsiveness. Cell Cycle 13(13):2110–2119. doi:10.4161/cc.29156

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Young MR, Colburn NH (2006) Fra-1 a target for cancer prevention or intervention. Gene 379:1–11. doi:10.1016/j.gene.2006.05.001

    Article  CAS  PubMed  Google Scholar 

  • Yurchenco PD (2011) Basement membranes: cell scaffoldings and signaling platforms. Cold Spring Harb Perspect Biol 3(2). doi:10.1101/cshperspect.a004911 (a004911 [pii])

  • Yurchenco PD, Ruben GC (1987) Basement membrane structure in situ: evidence for lateral associations in the type IV collagen network. J Cell Biol 105(6 Pt 1):2559–2568

    Article  CAS  PubMed  Google Scholar 

  • Zhang Y, LeRoy G, Seelig HP, Lane WS, Reinberg D (1998) The dermatomyositis-specific autoantigen Mi2 is a component of a complex containing histone deacetylase and nucleosome remodeling activities. Cell 95(2):279–289

    Article  CAS  PubMed  Google Scholar 

  • Ziel JW, Sherwood DR (2010) Roles for netrin signaling outside of axon guidance: a view from the worm. Dev Dyn 239(5):1296–1305. doi:10.1002/dvdy.22225

    CAS  PubMed  PubMed Central  Google Scholar 

  • Ziel JW, Hagedorn EJ, Audhya A, Sherwood DR (2009a) UNC-6 (netrin) orients the invasive membrane of the anchor cell in C. elegans. Nat Cell Biol 11(2):183–189. doi:10.1038/ncb1825 (ncb1825 [pii])

  • Ziel JW, Matus DQ, Sherwood DR (2009b) An expression screen for RhoGEF genes involved in C. elegans gonadogenesis. Gene Expr Patterns GEP 9(6):397–403. doi:10.1016/j.gep.2009.06.005

    Article  CAS  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Department of Biology, Duke University, Durham, NC, USA

    Daniel Keeley & David R. Sherwood

Authors
  1. Daniel Keeley
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. David R. Sherwood
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to David R. Sherwood .

Editor information

Editors and Affiliations

  1. Hamon Center for Therapeutic Oncology Research, UT Southwestern Medical Center , Dallas, Texas, USA

    Rolf A. Brekken

  2. Department of Reproductive Medicine, University of California , La Jolla, California, USA

    Dwayne Stupack

Rights and permissions

Reprints and permissions

Copyright information

© 2017 Springer International Publishing AG

About this chapter

Cite this chapter

Keeley, D., Sherwood, D.R. (2017). Breaching and Opening Basement Membrane Barriers: The Anchor Cell Leads the Way. In: Brekken, R., Stupack, D. (eds) Extracellular Matrix in Tumor Biology. Biology of Extracellular Matrix. Springer, Cham. https://doi.org/10.1007/978-3-319-60907-2_6

Download citation

Publish with us

Policies and ethics

Search

Navigation