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Discoidin Domain Receptors in Invertebrates

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Discoidin Domain Receptors in Health and Disease

Abstract

Discoidin domain receptors (DDRs) are evolutionary conserved and found in the genomes of all but the simplest metazoans. DDRs have neither been completely lost in larger animal phyla nor expanded beyond a small number of family members. Currently insights into the function of invertebrate DDRs come mainly from studies in Caenorhabditis elegans, which has two DDR genes similar to vertebrates. C. elegans ddr-2 is required for proper navigation of neuronal processes (axons) during nervous system development. In ddr-2 mutants, axonal navigation in several longitudinal axon tracts is affected, most notably in the ventral nerve cord, the major longitudinal axon tract. ddr-1 mutants alone do not have any obvious axon navigation defects, but various defects seen in ddr-2 mutants are substantially enhanced in ddr-1 ddr-2 double mutants, suggesting a role for both DDRs in axonal navigation. Transcriptional GFP-reporter constructs for ddr-1 and ddr-2 are expressed in neurons with axons in the affected nerve tracts and DDR::GFP fusion proteins localize to axons, raising the possibility that DDRs act as receptors in neurons during axonal outgrowth. These recent studies provide first insights into DDR function in invertebrates and establish a novel role for DDRs in axonal navigation.

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References

  1. Reddy PC, Bidaye SS, Ghaskadbi S (2011) Genome-wide screening reveals the emergence and divergence of RTK homologues in basal Metazoan Hydra magnipapillata. J Biosci 36(2):289–296

    Article  CAS  PubMed  Google Scholar 

  2. Putnam NH, Butts T, Ferrier DE, Furlong RF, Hellsten U, Kawashima T, Robinson-Rechavi M, Shoguchi E, Terry A, Yu JK, Benito-Gutierrez EL, Dubchak I, Garcia-Fernandez J, Gibson-Brown JJ, Grigoriev IV, Horton AC, de Jong PJ, Jurka J, Kapitonov VV, Kohara Y, Kuroki Y, Lindquist E, Lucas S, Osoegawa K, Pennacchio LA, Salamov AA, Satou Y, Sauka-Spengler T, Schmutz J, Shin IT, Toyoda A, Bronner-Fraser M, Fujiyama A, Holland LZ, Holland PW, Satoh N, Rokhsar DS (2008) The amphioxus genome and the evolution of the chordate karyotype. Nature 453(7198):1064–1071. doi:10.1038/nature06967, nature06967 [pii]

    Article  CAS  PubMed  Google Scholar 

  3. Dehal P, Satou Y, Campbell RK, Chapman J, Degnan B, De Tomaso A, Davidson B, Di Gregorio A, Gelpke M, Goodstein DM, Harafuji N, Hastings KE, Ho I, Hotta K, Huang W, Kawashima T, Lemaire P, Martinez D, Meinertzhagen IA, Necula S, Nonaka M, Putnam N, Rash S, Saiga H, Satake M, Terry A, Yamada L, Wang HG, Awazu S, Azumi K, Boore J, Branno M, Chin-Bow S, DeSantis R, Doyle S, Francino P, Keys DN, Haga S, Hayashi H, Hino K, Imai KS, Inaba K, Kano S, Kobayashi K, Kobayashi M, Lee BI, Makabe KW, Manohar C, Matassi G, Medina M, Mochizuki Y, Mount S, Morishita T, Miura S, Nakayama A, Nishizaka S, Nomoto H, Ohta F, Oishi K, Rigoutsos I, Sano M, Sasaki A, Sasakura Y, Shoguchi E, Shin-i T, Spagnuolo A, Stainier D, Suzuki MM, Tassy O, Takatori N, Tokuoka M, Yagi K, Yoshizaki F, Wada S, Zhang C, Hyatt PD, Larimer F, Detter C, Doggett N, Glavina T, Hawkins T, Richardson P, Lucas S, Kohara Y, Levine M, Satoh N, Rokhsar DS (2002) The draft genome of Ciona intestinalis: insights into chordate and vertebrate origins. Science 298(5601):2157–2167. doi:10.1126/science.1080049298/5601/2157 [pii]

    Article  CAS  PubMed  Google Scholar 

  4. Sodergren E, Weinstock GM, Davidson EH, Cameron RA, Gibbs RA, Angerer RC, Angerer LM, Arnone MI, Burgess DR, Burke RD, Coffman JA, Dean M, Elphick MR, Ettensohn CA, Foltz KR, Hamdoun A, Hynes RO, Klein WH, Marzluff W, McClay DR, Morris RL, Mushegian A, Rast JP, Smith LC, Thorndyke MC, Vacquier VD, Wessel GM, Wray G, Zhang L, Elsik CG, Ermolaeva O, Hlavina W, Hofmann G, Kitts P, Landrum MJ, Mackey AJ, Maglott D, Panopoulou G, Poustka AJ, Pruitt K, Sapojnikov V, Song X, Souvorov A, Solovyev V, Wei Z, Whittaker CA, Worley K, Durbin KJ, Shen Y, Fedrigo O, Garfield D, Haygood R, Primus A, Satija R, Severson T, Gonzalez-Garay ML, Jackson AR, Milosavljevic A, Tong M, Killian CE, Livingston BT, Wilt FH, Adams N, Belle R, Carbonneau S, Cheung R, Cormier P, Cosson B, Croce J, Fernandez-Guerra A, Geneviere AM, Goel M, Kelkar H, Morales J, Mulner-Lorillon O, Robertson AJ, Goldstone JV, Cole B, Epel D, Gold B, Hahn ME, Howard-Ashby M, Scally M, Stegeman JJ, Allgood EL, Cool J, Judkins KM, McCafferty SS, Musante AM, Obar RA, Rawson AP, Rossetti BJ, Gibbons IR, Hoffman MP, Leone A, Istrail S, Materna SC, Samanta MP, Stolc V, Tongprasit W, Tu Q, Bergeron KF, Brandhorst BP, Whittle J, Berney K, Bottjer DJ, Calestani C, Peterson K, Chow E, Yuan QA, Elhaik E, Graur D, Reese JT, Bosdet I, Heesun S, Marra MA, Schein J, Anderson MK, Brockton V, Buckley KM, Cohen AH, Fugmann SD, Hibino T, Loza-Coll M, Majeske AJ, Messier C, Nair SV, Pancer Z, Terwilliger DP, Agca C, Arboleda E, Chen N, Churcher AM, Hallbook F, Humphrey GW, Idris MM, Kiyama T, Liang S, Mellott D, Mu X, Murray G, Olinski RP, Raible F, Rowe M, Taylor JS, Tessmar-Raible K, Wang D, Wilson KH, Yaguchi S, Gaasterland T, Galindo BE, Gunaratne HJ, Juliano C, Kinukawa M, Moy GW, Neill AT, Nomura M, Raisch M, Reade A, Roux MM, Song JL, Su YH, Townley IK, Voronina E, Wong JL, Amore G, Branno M, Brown ER, Cavalieri V, Duboc V, Duloquin L, Flytzanis C, Gache C, Lapraz F, Lepage T, Locascio A, Martinez P, Matassi G, Matranga V, Range R, Rizzo F, Rottinger E, Beane W, Bradham C, Byrum C, Glenn T, Hussain S, Manning G, Miranda E, Thomason R, Walton K, Wikramanayke A, Wu SY, Xu R, Brown CT, Chen L, Gray RF, Lee PY, Nam J, Oliveri P, Smith J, Muzny D, Bell S, Chacko J, Cree A, Curry S, Davis C, Dinh H, Dugan-Rocha S, Fowler J, Gill R, Hamilton C, Hernandez J, Hines S, Hume J, Jackson L, Jolivet A, Kovar C, Lee S, Lewis L, Miner G, Morgan M, Nazareth LV, Okwuonu G, Parker D, Pu LL, Thorn R, Wright R (2006) The genome of the sea urchin Strongylocentrotus purpuratus. Science 314(5801):941–952. doi:10.1126/science.1133609, 314/5801/941 [pii]

  5. Vogel WF, Abdulhussein R, Ford CE (2006) Sensing extracellular matrix: an update on discoidin domain receptor function. Cell Signal 18(8):1108–1116. doi:10.1016/j.cellsig.2006.02.012, S0898-6568(06)00047-7 [pii]

    Google Scholar 

  6. 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, ng.227 [pii]

    Article  CAS  PubMed  Google Scholar 

  7. Adams MD, Celniker SE, Holt RA, Evans CA, Gocayne JD, Amanatides PG, Scherer SE, Li PW, Hoskins RA, Galle RF, George RA, Lewis SE, Richards S, Ashburner M, Henderson SN, Sutton GG, Wortman JR, Yandell MD, Zhang Q, Chen LX, Brandon RC, Rogers YH, Blazej RG, Champe M, Pfeiffer BD, Wan KH, Doyle C, Baxter EG, Helt G, Nelson CR, Gabor GL, Abril JF, Agbayani A, An HJ, Andrews-Pfannkoch C, Baldwin D, Ballew RM, Basu A, Baxendale J, Bayraktaroglu L, Beasley EM, Beeson KY, Benos PV, Berman BP, Bhandari D, Bolshakov S, Borkova D, Botchan MR, Bouck J, Brokstein P, Brottier P, Burtis KC, Busam DA, Butler H, Cadieu E, Center A, Chandra I, Cherry JM, Cawley S, Dahlke C, Davenport LB, Davies P, de Pablos B, Delcher A, Deng Z, Mays AD, Dew I, Dietz SM, Dodson K, Doup LE, Downes M, Dugan-Rocha S, Dunkov BC, Dunn P, Durbin KJ, Evangelista CC, Ferraz C, Ferriera S, Fleischmann W, Fosler C, Gabrielian AE, Garg NS, Gelbart WM, Glasser K, Glodek A, Gong F, Gorrell JH, Gu Z, Guan P, Harris M, Harris NL, Harvey D, Heiman TJ, Hernandez JR, Houck J, Hostin D, Houston KA, Howland TJ, Wei MH, Ibegwam C, Jalali M, Kalush F, Karpen GH, Ke Z, Kennison JA, Ketchum KA, Kimmel BE, Kodira CD, Kraft C, Kravitz S, Kulp D, Lai Z, Lasko P, Lei Y, Levitsky AA, Li J, Li Z, Liang Y, Lin X, Liu X, Mattei B, McIntosh TC, McLeod MP, McPherson D, Merkulov G, Milshina NV, Mobarry C, Morris J, Moshrefi A, Mount SM, Moy M, Murphy B, Murphy L, Muzny DM, Nelson DL, Nelson DR, Nelson KA, Nixon K, Nusskern DR, Pacleb JM, Palazzolo M, Pittman GS, Pan S, Pollard J, Puri V, Reese MG, Reinert K, Remington K, Saunders RD, Scheeler F, Shen H, Shue BC, Siden-Kiamos I, Simpson M, Skupski MP, Smith T, Spier E, Spradling AC, Stapleton M, Strong R, Sun E, Svirskas R, Tector C, Turner R, Venter E, Wang AH, Wang X, Wang ZY, Wassarman DA, Weinstock GM, Weissenbach J, Williams SM, Woodage T, Worley KC, Wu D, Yang S, Yao QA, Ye J, Yeh RF, Zaveri JS, Zhan M, Zhang G, Zhao Q, Zheng L, Zheng XH, Zhong FN, Zhong W, Zhou X, Zhu S, Zhu X, Smith HO, Gibbs RA, Myers EW, Rubin GM, Venter JC (2000) The genome sequence of Drosophila melanogaster. Science 287(5461):2185–2195, 8392 [pii]

    Article  PubMed  Google Scholar 

  8. Werren JH, Richards S, Desjardins CA, Niehuis O, Gadau J, Colbourne JK, Beukeboom LW, Desplan C, Elsik CG, Grimmelikhuijzen CJ, Kitts P, Lynch JA, Murphy T, Oliveira DC, Smith CD, van de Zande L, Worley KC, Zdobnov EM, Aerts M, Albert S, Anaya VH, Anzola JM, Barchuk AR, Behura SK, Bera AN, Berenbaum MR, Bertossa RC, Bitondi MM, Bordenstein SR, Bork P, Bornberg-Bauer E, Brunain M, Cazzamali G, Chaboub L, Chacko J, Chavez D, Childers CP, Choi JH, Clark ME, Claudianos C, Clinton RA, Cree AG, Cristino AS, Dang PM, Darby AC, de Graaf DC, Devreese B, Dinh HH, Edwards R, Elango N, Elhaik E, Ermolaeva O, Evans JD, Foret S, Fowler GR, Gerlach D, Gibson JD, Gilbert DG, Graur D, Grunder S, Hagen DE, Han Y, Hauser F, Hultmark D, Hunter HCt, Hurst GD, Jhangian SN, Jiang H, Johnson RM, Jones AK, Junier T, Kadowaki T, Kamping A, Kapustin Y, Kechavarzi B, Kim J, Kiryutin B, Koevoets T, Kovar CL, Kriventseva EV, Kucharski R, Lee H, Lee SL, Lees K, Lewis LR, Loehlin DW, Logsdon JM Jr, Lopez JA, Lozado RJ, Maglott D, Maleszka R, Mayampurath A, Mazur DJ, McClure MA, Moore AD, Morgan MB, Muller J, Munoz-Torres MC, Muzny DM, Nazareth LV, Neupert S, Nguyen NB, Nunes FM, Oakeshott JG, Okwuonu GO, Pannebakker BA, Pejaver VR, Peng Z, Pratt SC, Predel R, Pu LL, Ranson H, Raychoudhury R, Rechtsteiner A, Reese JT, Reid JG, Riddle M, Robertson HM, Romero-Severson J, Rosenberg M, Sackton TB, Sattelle DB, Schluns H, Schmitt T, Schneider M, Schuler A, Schurko AM, Shuker DM, Simoes ZL, Sinha S, Smith Z, Solovyev V, Souvorov A, Springauf A, Stafflinger E, Stage DE, Stanke M, Tanaka Y, Telschow A, Trent C, Vattathil S, Verhulst EC, Viljakainen L, Wanner KW, Waterhouse RM, Whitfield JB, Wilkes TE, Williamson M, Willis JH, Wolschin F, Wyder S, Yamada T, Yi SV, Zecher CN, Zhang L, Gibbs RA (2010) Functional and evolutionary insights from the genomes of three parasitoid Nasonia species. Science 327(5963):343–348. doi:10.1126/science.1178028, 327/5963/343 [pii]

    Google Scholar 

  9. Mummery-Widmer JL, Yamazaki M, Stoeger T, Novatchkova M, Bhalerao S, Chen D, Dietzl G, Dickson BJ, Knoblich JA (2009) Genome-wide analysis of Notch signalling in Drosophila by transgenic RNAi. Nature 458(7241):987–992. doi:10.1038/nature07936, nature07936 [pii]

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  10. Yin Z, Sadok A, Sailem H, McCarthy A, Xia X, Li F, Garcia MA, Evans L, Barr AR, Perrimon N, Marshall CJ, Wong ST, Bakal C (2013) A screen for morphological complexity identifies regulators of switch-like transitions between discrete cell shapes. Nat Cell Biol 15(7):860–871. doi:10.1038/ncb2764, ncb2764 [pii]

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  11. Bettencourt-Dias M, Giet R, Sinka R, Mazumdar A, Lock WG, Balloux F, Zafiropoulos PJ, Yamaguchi S, Winter S, Carthew RW, Cooper M, Jones D, Frenz L, Glover DM (2004) Genome-wide survey of protein kinases required for cell cycle progression. Nature 432(7020):980–987. doi:10.1038/nature03160, nature03160 [pii]

    Article  CAS  PubMed  Google Scholar 

  12. Zhu X, Mahairas G, Illies M, Cameron RA, Davidson EH, Ettensohn CA (2001) A large-scale analysis of mRNAs expressed by primary mesenchyme cells of the sea urchin embryo. Development 128(13):2615–2627

    PubMed  Google Scholar 

  13. Carafoli F, Hohenester E (2012) Collagen recognition and transmembrane signalling by discoidin domain receptors. Biochim Biophys Acta 1834(10):2187–2194. doi:10.1016/j.bbapap.2012.10.014, S1570-9639(12)00255-5 [pii]

    Article  PubMed  Google Scholar 

  14. Vogel W, Gish GD, Alves F, Pawson T (1997) The discoidin domain receptor tyrosine kinases are activated by collagen. Mol Cell 1(1):13–23, S1097-2765(00)80003-9 [pii]

    Article  CAS  PubMed  Google Scholar 

  15. Vogel W, Brakebusch C, Fassler R, Alves F, Ruggiero F, Pawson T (2000) Discoidin domain receptor 1 is activated independently of beta(1) integrin. J Biol Chem 275(8):5779–5784

    Article  CAS  PubMed  Google Scholar 

  16. Matsuyama W, Kamohara H, Galligan C, Faure M, Yoshimura T (2003) Interaction of discoidin domain receptor 1 isoform b (DDR1b) with collagen activates p38 mitogen-activated protein kinase and promotes differentiation of macrophages. FASEB J 17(10):1286–1288. doi:10.1096/fj.02-0320fje02-0320fje [pii]

    CAS  PubMed  Google Scholar 

  17. Koo DH, McFadden C, Huang Y, Abdulhussein R, Friese-Hamim M, Vogel WF (2006) Pinpointing phosphotyrosine-dependent interactions downstream of the collagen receptor DDR1. FEBS Lett 580(1):15–22. doi:10.1016/j.febslet.2005.11.035, S0014-5793(05)01398-0 [pii]

    Article  CAS  PubMed  Google Scholar 

  18. Slack BE, Siniaia MS, Blusztajn JK (2006) Collagen type I selectively activates ectodomain shedding of the discoidin domain receptor 1: involvement of Src tyrosine kinase. J Cell Biochem 98(3):672–684. doi:10.1002/jcb.20812

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  19. Lemeer S, Bluwstein A, Wu Z, Leberfinger J, Muller K, Kramer K, Kuster B (2011) Phosphotyrosine mediated protein interactions of the discoidin domain receptor 1. J Proteomics 75(12):3465–3477. doi:10.1016/j.jprot.2011.10.007, S1874-3919(11)00493-3 [pii]

    Article  PubMed  Google Scholar 

  20. Mohamed AM, Chin-Sang ID (2011) The C. elegans nck-1 gene encodes two isoforms and is required for neuronal guidance. Dev Biol 354(1):55–66. doi:10.1016/j.ydbio.2011.03.019, S0012-1606(11)00183-7 [pii]

    Article  CAS  PubMed  Google Scholar 

  21. Unsoeld T, Park JO, Hutter H (2012) Discoidin domain receptors guide axons along longitudinal tracts in C. elegans. Dev Biol 374(1):142–152. doi:10.1016/j.ydbio.2012.11.001, S0012-1606(12)00604-5 [pii]

    Article  PubMed  Google Scholar 

  22. Ikeda K, Wang LH, Torres R, Zhao H, Olaso E, Eng FJ, Labrador P, Klein R, Lovett D, Yancopoulos GD, Friedman SL, Lin HC (2002) Discoidin domain receptor 2 interacts with Src and Shc following its activation by type I collagen. J Biol Chem 277(21):19206–19212. doi:10.1074/jbc.M201078200M201078200 [pii]

    Article  CAS  PubMed  Google Scholar 

  23. Yang K, Kim JH, Kim HJ, Park IS, Kim IY, Yang BS (2005) Tyrosine 740 phosphorylation of discoidin domain receptor 2 by Src stimulates intramolecular autophosphorylation and Shc signaling complex formation. J Biol Chem 280(47):39058–39066. doi:10.1074/jbc.M506921200, M506921200 [pii]

    Article  CAS  PubMed  Google Scholar 

  24. White J, Southgate E, Thomson J, Brenner S (1986) The structure of the nervous system of the nematode Caenorhabditis elegans. Philos Trans R Soc Lond B 314:1–340

    Article  CAS  Google Scholar 

  25. Albertson DG, Thomson JN (1976) The pharynx of Caenorhabditis elegans. Philos Trans R Soc Lond B Biol Sci 275(938):299–325

    Article  CAS  PubMed  Google Scholar 

  26. Hall DH, Russell RL (1991) The posterior nervous system of the nematode Caenorhabditis elegans: serial reconstruction of identified neurons and complete pattern of synaptic interactions. J Neurosci 11(1):1–22

    CAS  PubMed  Google Scholar 

  27. White JG, Southgate E, Thomson JN, Brenner S (1976) The structure of the ventral nerve cord of Caenorhabditis elegans. Philos Trans R Soc Lond B Biol Sci 275(938):327–348

    Article  CAS  PubMed  Google Scholar 

  28. Chalfie M, Tu Y, Euskirchen G, Ward WW, Prasher DC (1994) Green fluorescent protein as a marker for gene expression. Science 263(5148):802–805

    Article  CAS  PubMed  Google Scholar 

  29. Yurchenco PD, Wadsworth WG (2004) Assembly and tissue functions of early embryonic laminins and netrins. Curr Opin Cell Biol 16(5):572–579. doi:10.1016/j.ceb.2004.07.013S0955-0674(04)00112-7 [pii]

    Article  CAS  PubMed  Google Scholar 

  30. McKay SJ, Johnsen R, Khattra J, Asano J, Baillie DL, Chan S, Dube N, Fang L, Goszczynski B, Ha E, Halfnight E, Hollebakken R, Huang P, Hung K, Jensen V, Jones SJ, Kai H, Li D, Mah A, Marra M, McGhee J, Newbury R, Pouzyrev A, Riddle DL, Sonnhammer E, Tian H, Tu D, Tyson JR, Vatcher G, Warner A, Wong K, Zhao Z, Moerman DG (2003) Gene expression profiling of cells, tissues, and developmental stages of the nematode C. elegans. Cold Spring Harb Symp Quant Biol 68:159–169

    Article  CAS  PubMed  Google Scholar 

  31. Alves F, Vogel W, Mossie K, Millauer B, Hofler H, Ullrich A (1995) Distinct structural characteristics of discoidin I subfamily receptor tyrosine kinases and complementary expression in human cancer. Oncogene 10(3):609–618

    CAS  PubMed  Google Scholar 

  32. Leitinger B (2014) Discoidin domain receptor functions in physiological and pathological conditions. Int Rev Cell Mol Biol 310:39–87. doi:10.1016/B978-0-12-800180-6.00002-5, B978-0-12-800180-6.00002-5 [pii]

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  33. Lai C, Lemke G (1994) Structure and expression of the Tyro 10 receptor tyrosine kinase. Oncogene 9(3):877–883

    CAS  PubMed  Google Scholar 

  34. Sanchez MP, Tapley P, Saini SS, He B, Pulido D, Barbacid M (1994) Multiple tyrosine protein kinases in rat hippocampal neurons: isolation of Ptk-3, a receptor expressed in proliferative zones of the developing brain. Proc Natl Acad Sci U S A 91(5):1819–1823

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  35. Zerlin M, Julius MA, Goldfarb M (1993) NEP: a novel receptor-like tyrosine kinase expressed in proliferating neuroepithelia. Oncogene 8(10):2731–2739

    CAS  PubMed  Google Scholar 

  36. Durbin RM (1987) Studies on the development and organisation of the nervous system of Caenorhabditis elegans. Ph.D. Thesis, University of Cambridge

    Google Scholar 

  37. Garriga G, Desai C, Horvitz HR (1993) Cell interactions control the direction of outgrowth, branching and fasciculation of the HSN axons of Caenorhabditis elegans. Development 117(3):1071–1087

    CAS  PubMed  Google Scholar 

  38. Shrivastava A, Radziejewski C, Campbell E, Kovac L, McGlynn M, Ryan TE, Davis S, Goldfarb MP, Glass DJ, Lemke G, Yancopoulos GD (1997) An orphan receptor tyrosine kinase family whose members serve as nonintegrin collagen receptors. Mol Cell 1(1):25–34, S1097-2765(00)80004-0 [pii]

    Article  CAS  PubMed  Google Scholar 

  39. Hou G, Vogel W, Bendeck MP (2001) The discoidin domain receptor tyrosine kinase DDR1 in arterial wound repair. J Clin Invest 107(6):727–735. doi:10.1172/JCI10720

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  40. Leitinger B, Kwan AP (2006) The discoidin domain receptor DDR2 is a receptor for type X collagen. Matrix Biol 25(6):355–364. doi:10.1016/j.matbio.2006.05.006, S0945-053X(06)00058-8 [pii]

    Article  CAS  PubMed  Google Scholar 

  41. Consortium CS (1998) Genome sequence of the nematode C. elegans: a platform for investigating biology. Science 282(5396):2012–2018

    Article  Google Scholar 

  42. Page AP, Johnstone IL (2007) The cuticle. WormBook 1–15. doi:10.1895/wormbook.1.138.1

  43. Kramer JM (2005) Basement membranes. WormBook 1–15. doi:10.1895/wormbook.1.16.1

  44. Guo XD, Johnson JJ, Kramer JM (1991) Embryonic lethality caused by mutations in basement membrane collagen of C. elegans. Nature 349(6311):707–709. doi:10.1038/349707a0

    Article  CAS  PubMed  Google Scholar 

  45. Gupta MC, Graham PL, Kramer JM (1997) Characterization of alpha1(IV) collagen mutations in Caenorhabditis elegans and the effects of alpha1 and alpha2(IV) mutations on type IV collagen distribution. J Cell Biol 137(5):1185–1196

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  46. Sibley MH, Graham PL, von Mende N, Kramer JM (1994) Mutations in the alpha 2(IV) basement membrane collagen gene of Caenorhabditis elegans produce phenotypes of differing severities. EMBO J 13(14):3278–3285

    CAS  PubMed  PubMed Central  Google Scholar 

  47. Kang SH, Kramer JM (2000) Nidogen is nonessential and not required for normal type IV collagen localization in Caenorhabditis elegans. Mol Biol Cell 11(11):3911–3923

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  48. Kim S, Wadsworth WG (2000) Positioning of longitudinal nerves in C. elegans by nidogen. Science 288(5463):150–154

    Article  CAS  PubMed  Google Scholar 

  49. Aumailley M, Battaglia C, Mayer U, Reinhardt D, Nischt R, Timpl R, Fox JW (1993) Nidogen mediates the formation of ternary complexes of basement membrane components. Kidney Int 43(1):7–12

    Article  CAS  PubMed  Google Scholar 

  50. Kohfeldt E, Sasaki T, Gohring W, Timpl R (1998) Nidogen-2: a new basement membrane protein with diverse binding properties. J Mol Biol 282(1):99–109. doi:10.1006/jmbi.1998.2004, S0022-2836(98)92004-6 [pii]

    Article  CAS  PubMed  Google Scholar 

  51. Ackley BD, Crew JR, Elamaa H, Pihlajaniemi T, Kuo CJ, Kramer JM (2001) The NC1/endostatin domain of Caenorhabditis elegans type XVIII collagen affects cell migration and axon guidance. J Cell Biol 152(6):1219–1232

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  52. Xu H, Raynal N, Stathopoulos S, Myllyharju J, Farndale RW, Leitinger B (2011) Collagen binding specificity of the discoidin domain receptors: binding sites on collagens II and III and molecular determinants for collagen IV recognition by DDR1. Matrix Biol 30(1):16–26. doi:10.1016/j.matbio.2010.10.004, S0945-053X(10)00154-X [pii]

    Article  PubMed  PubMed Central  Google Scholar 

  53. Gallo M, Mah AK, Johnsen RC, Rose AM, Baillie DL (2006) Caenorhabditis elegans dpy-14: an essential collagen gene with unique expression profile and physiological roles in early development. Mol Genet Genomics 275(6):527–539. doi:10.1007/s00438-006-0110-3

    Article  CAS  PubMed  Google Scholar 

  54. Sund M, Vaisanen T, Kaukinen S, Ilves M, Tu H, Autio-Harmainen H, Rauvala H, Pihlajaniemi T (2001) Distinct expression of type XIII collagen in neuronal structures and other tissues during mouse development. Matrix Biol 20(4):215–231, S0945-053X(01)00134-2 [pii]

    Article  CAS  PubMed  Google Scholar 

  55. Tanaka T, Wakabayashi T, Oizumi H, Nishio S, Sato T, Harada A, Fujii D, Matsuo Y, Hashimoto T, Iwatsubo T (2014) CLAC-P/collagen type XXV is required for the intramuscular innervation of motoneurons during neuromuscular development. J Neurosci 34(4):1370–1379. doi:10.1523/JNEUROSCI.2440-13.2014, 34/4/1370 [pii]

    Google Scholar 

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Correspondence to Harald Hutter .

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Unsoeld, T., Taylor, J., Hutter, H. (2016). Discoidin Domain Receptors in Invertebrates. In: Fridman, R., Huang, P. (eds) Discoidin Domain Receptors in Health and Disease. Springer, New York, NY. https://doi.org/10.1007/978-1-4939-6383-6_5

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